INTIMP-03628; No of Pages 4 International Immunopharmacology xxx (2015) xxx–xxx
Contents lists available at ScienceDirect
International Immunopharmacology journal homepage: www.elsevier.com/locate/intimp
Review
Regulation of immune cell homeostasis and function by coronin 1 Rajesh Jayachandran ⁎, Jean Pieters Biozentrum, University of Basel, Basel, Switzerland
a r t i c l e
i n f o
Article history: Received 4 March 2015 Accepted 28 March 2015 Available online xxxx Keywords: Coronin T cells B cells NK cells Macrophages Macropinocytosis Calcineurin Calcium Mycobacteria SCID Lymphopenia
a b s t r a c t Coronin 1 is the most recent candidate in the list of genes causing severe combined immunodeficiency (SCID) in humans. A distinctive feature of the SCID induced by coronin 1 deficiency is selective naïve T cell lymphopenia in the presence of a normal thymus as well as normal B cell and natural killer cell numbers (T−B+NK+). Coronin 1 is a member of the evolutionarily conserved coronin protein family, members of which are widely expressed across the eukaryotic kingdom. Mammals express seven coronin molecules, numbered from coronin 1 to 7. The different coronin proteins have a distinct but overlapping tissue expression and have been reported to be involved in a wide array of cellular functions including calcium homeostasis, cytoskeletal dynamics, immune and inflammatory responses, neuromuscular transmission as well as cognition and behavior. In this minireview, we describe the role of coronin 1 in the maintenance of immune cell diversity and function. © 2015 Elsevier B.V. All rights reserved.
Contents 1. 2.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . Murine coronin 1 deficiency and modulation of immune cell population 2.1. Macrophages . . . . . . . . . . . . . . . . . . . . . . . . 2.2. T cells . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3. B cells . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.4. Neutrophils . . . . . . . . . . . . . . . . . . . . . . . . . 2.5. Dendritic cells (DCs) . . . . . . . . . . . . . . . . . . . . . 2.6. Natural killer cells (NK cells) . . . . . . . . . . . . . . . . . 2.7. Mast cells . . . . . . . . . . . . . . . . . . . . . . . . . 3. Human coronin 1-deficiency and modulation of immune cell population 4. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
0 0 0 0 0 0 0 0 0 0 0 0 0
1. Introduction Abbreviations: NK cells, natural killer cells; DCs, dendritic cells; ADHD, attention deficit hyperactivity disorder; SCID, severe combined immunodeficiency; NADPH, nicotinamide adenine dinucleotide phosphate; ADA, adenosine deaminase; RAG, recombination activating gene; EAE, experimental autoimmune encephalitis; MOG, myelin-oligodendrocyte glycoprotein; TCR, T cell receptor; IP3, inositol-triphosphate; PI3K, phosphatidyl inositol 3 kinase; BCR, B cell receptor. ⁎ Corresponding author at: Klingelbergstrasse 50, 4156 Basel, Switzerland. Tel.: +41 61 267 14 93; fax: +41 61 267 21 48. E-mail address: [email protected] (R. Jayachandran).
Coronin 1, also known as P57 or TACO (for tryptophan aspartate containing coat protein) is the most widely studied member of the coronin protein family. Coronins are characterized by the presence of multiple WD repeats, that are short domains of approximately 40 amino acid residues terminating with tryptophan-aspartate dipeptide. Coronin 1 is an immune and neuronal lineage-specific protein expressed abundantly in T cells, B cells, macrophages, dendritic cells,
http://dx.doi.org/10.1016/j.intimp.2015.03.045 1567-5769/© 2015 Elsevier B.V. All rights reserved.
Please cite this article as: R. Jayachandran, J. Pieters, Regulation of immune cell homeostasis and function by coronin 1, Int Immunopharmacol (2015), http://dx.doi.org/10.1016/j.intimp.2015.03.045
2
R. Jayachandran, J. Pieters / International Immunopharmacology xxx (2015) xxx–xxx
mast cells, neutrophils and neurons [1,2]. In both mice and human, coronin 1 was found to be important for normal immune cell homeostasis as well as neuronal functioning. With regard to the immune system, coronin 1 deletion predominantly affects the T cell population [3–5] while coronin 1 depletion also causes severe neurobehavioral changes including lowered anxiety, fear memory formation as well as nerve growth factor (NGF)-mediated signaling defects in neurons [6,7]. Upon coronin 1 deficiency in mouse, the total T cell population depletes by almost 80% in the peripheral immune system leaving the other leukocyte population largely intact. Most importantly, the naïve T cells are virtually depleted despite a near normal cellular population in the thymus [3–5,8,9]. In the following sections, we will first discuss in depth the various immune parameters that have been reported to be altered upon depletion of coronin 1 through various gene knockout approaches in mice and secondly briefly review the available information from patients harboring mutations in the coronin 1 gene. 2. Murine coronin 1 deficiency and modulation of immune cell population In mammals, coronin 1 is strongly expressed in all leukocytes in addition to being expressed in neurons. In the following sections, the consequences of coronin 1 deletion in mice on the functionality of the various immune cell populations will be discussed. 2.1. Macrophages Coronin 1 was identified in a screen for host cell factors that were recruited and retained on mycobacterial phagosomes by pathogenic mycobacteria [10,11]. Since pathogenic mycobacteria, such as Mycobacterium tuberculosis, the causative agent of tuberculosis, survives within macrophages by blocking their delivery to lysosomes, it was hypothesized that the absence of coronin 1 would disfavor mycobacterial survival and promote its rapid death and degradation. To test this hypothesis, coronin 1-deficient mice were generated and their bone marrow derived macrophages analyzed. Macrophages lacking coronin 1 did not reveal any abnormalities in number or functional responses including proliferation, phagocytosis of beads and bacteria, migration, chemotaxis, activation, membrane ruffling and morphology [12,13]. However, upon mycobacterial challenge, as hypothesized, these cells efficiently killed M. tuberculosis[12–14], which was found to occur through a defect in the Ca2+/calcineurin activation pathway upon coronin 1-deficiency [12]. More recently, it was shown that trimerization of coronin 1 is a prerequisite for this mycobacteria-mediated calcineurin activation and subsequent mycobacterial survival [15,16]. Additionally, coronin 1 phosphorylation at serine residues under pro-inflammatory situation, mediated via interferon-γ, favors coronin 1 redistribution through its interaction with 14-3-3ζ that ultimately enhances phosphatidyl inositol 3 kinase (PI3K) activity and macropinocytosis thereby switching macrophages from a phagocytic mode to macropinocytic mode and aiding the rapid uptake and clearance of pathogens [17].
signaling and calcineurin activation [3,8,18]. Coronin 1-deficient T cells were furthermore reported to display defective mitochondrial function thereby inducing apoptosis that was linked to defective actin dynamics [5]; However, in a separate study it was found that coronin 1 does not modulate F-actin and that induction of F-actin failed to induce apoptosis [18] and therefore it remains unclear whether or not the deletion of peripheral naïve T cells in the absence of coronin 1 is a consequence of mitochondrial dysfunction or a lack of pro-survival signals normally generated through the T cell receptor [19,20]. Although both CD4+ and CD8+ naïve T cells are depleted upon coronin 1-deficiency, CD8+ T cells from coronin 1-deficient mice are functionally capable of mounting a immune response against various viral challenges [21]. Interestingly, coronin 1 appears to be important for the generation of autoimmune responses. A search for genetic changes that suppresses the lupus phenotype in a mouse model (MRL/LPR) identified a coronin1 mutation resulting in coronin 1 depletion, to be the prime reason for resistance to the lupus phenotype [8]. Also, coronin 1-deficient mice show an attenuated response in an experimental autoimmune encephalitis (EAE) model [22,23]. An important T cell subset regulating autoimmune responses is the Th17 T cell subset that are characterized through the expression of the transcription factor RORγ-t and produce interleukin17 [24]. Interestingly, it was found that Th17 cells in mice lacking coronin 1 expressed both IL-17 and IFNγ quite unlike wild type Th17 cells. This coincided with an increased numbers of IL-17 producing T cells in the central nervous system upon induction of EAE [25]. Thus, coronin 1 appears to play a role in the proper regulation of Th17 immune responses where its absence results in an excessive production of IL-17 along with IFNγ unlike wild type Th17 cells which correlated with defective TGFβR signaling [25]. As mentioned above, the exact reason(s) for naïve T cell depletion upon coronin 1 deficiency remains to be identified, and could well be related to the capacity of coronin 1 to be involved in the processing of cell surface triggers, as is the case for other coronin family members [1,6,26]. 2.3. B cells The population of B cells has been reported to show alteration in total numbers as a result of coronin 1 deletion which was dependent on the source (blood versus spleen versus lymph nodes) analyzed [3, 27]. For example, while in peripheral blood and lymph nodes, B cell numbers are reduced, in spleen their numbers are maintained in near normal numbers [3–5,27]. Coronin 1-deficient B cells show a normal immunoglobulin and B cell receptor expression and development. B cell receptor triggering revealed however attenuated calcium fluxes and proliferation similar to TCR triggered coronin 1-deficient T cells [27]. However, upon coronin 1 deletion, in vivo immune responses against both thymus-dependent and thymus-independent antigens are not significantly different as compared to wild type mice possibly due to the presence of co-stimulatory signals that render coronin 1 dispensable for B cell signaling [27].
2.2. T cells 2.4. Neutrophils While the total leukocyte numbers are around 15 × 106/ml in the peripheral blood of a normal wild type mouse, their numbers were reduced by one-third to approximately 5 × 106/ml in mice lacking coronin 1 [3]. This decrease was almost entirely due to a drastic depletion of peripheral CD3+CD4+ and CD3+CD8+ T lymphocytes [3–5,9]. Analysis of various surface markers within the viable T cells population in coronin 1-deficient mice revealed a specific depletion of the CD62Lhi CD44Lo population that constitutes the naïve T cell subset [3–5]. Unlike wild type T cells, that can be readily activated with T cell receptor (TCR) triggers to elicit cytosolic calcium fluxes, calcineurin activation, and inositol-triphosphate (IP3) production, triggering of the T cell receptors on coronin 1-deficient T cells fails to elicit calcium
Neutrophils form a prime component of the innate immune system and are one of the first immune cell subsets to arrive at the site of inflammation [28,29]. As is the case in other immune cells, coronin 1 is enriched along the leading edge of migrating neutrophils and nascent phagosomes [30]. Neutrophils from coronin 1-deficient mice display no abnormalities with respect to numbers, adherence, membrane dynamics, spreading or chemotaxis [31]. Also, although coronin 1 was shown to interact with PHOX proteins, which are prime components of the NADPH oxidase system [32], no alteration of the oxidative burst was found upon coronin 1 deletion [31]. Furthermore, in a concanavalin A-induced hepatitis model, recruitment of neutrophils to
Please cite this article as: R. Jayachandran, J. Pieters, Regulation of immune cell homeostasis and function by coronin 1, Int Immunopharmacol (2015), http://dx.doi.org/10.1016/j.intimp.2015.03.045
R. Jayachandran, J. Pieters / International Immunopharmacology xxx (2015) xxx–xxx
post-sinusoidal venules and hepatic tissue was shown to be comparable between wild type and coronin 1-deficient mice [33]. 2.5. Dendritic cells (DCs) Bone marrow-derived dendritic cells isolated from coronin 1deficient mice showed that they were comparable to wild type dendritic cells in terms of antigen processing and presentation and subsequent activation of T cells. Thus, coronin 1 appears to be dispensable for antigen processing and presentation by dendritic cells [34]. 2.6. Natural killer cells (NK cells) In terms of their numbers, no striking differences were observed between genotypes, nor with respect to their in vitro cytolytic potential (unpublished observation).
3
1 deficiency per se, remains to be analyzed. Importantly, the single patient analyzed to date with an exclusive coronin 1 deletion in the absence of other genetic aberrations [6,38], shows a normal phenotype with respect to B/NK cell numbers and functionality, although it cannot be excluded that the minimal residual coronin 1 expression may restore some coronin 1 function in this patient. An unrelated study showed that in human neutrophils coronin 1 was able to attenuate apoptosis, and reported that neutrophils from cystic fibrosis patients express elevated levels of coronin 1 thereby possibly suppressing apoptosis and sustaining an inflammatory milieu [46]. Taken together the human data suggest that, as is the case for mouse T cells, coronin 1 is required to provide pro-survival signals, in the absence of which both CD4 as well as CD8 single positive T cells rapidly disappear from the circulation resulting in a severe lymphopenia characterized by a T−NK+B+ SCID phenotype. 4. Conclusions
2.7. Mast cells The role for coronin 1 in murine mast cell function remains presently unclear, with one research group reporting normal functionality of mast cells lacking coronin 1 expression [35] and another group reporting a hyper-degranulation response, reduced cytokine secretion and enhanced passive cutaneous anaphylactic response upon coronin 1 deletion [36]. Whether or not this discrepancy is a result of different mouse strains used in the two studies remains to be established. 3. Human coronin 1-deficiency and modulation of immune cell population Four clinical reports have thus far documented seven individual patients harboring mutations and aberrations in the coronin 1 gene that either result in a total absence or minimal expression of coronin 1 protein [37–40]. It is important to note that only one amongst these four studies report an exclusive coronin 1-deficiency in humans [6,38] while the remaining three case studies document coronin 1 aberration together with other genetic changes, including 16p11.2 micro-deletions, as well as mutations in other genes important for immune function (NLRP7, STAT2, NCF2) [37,39–43]. A comparison of the clinical history of these cases reveals that the affected patients had a widely divergent set of associated health problems, ranging from attention deficient hyperactivity disorder (ADHD), cognitive impairment, aggressiveness, to varied levels of susceptibility to diverse pathogens, including Epstein Barr viral infection, Mycobacterium leprae and human papilloma virus [6,37–39]. Furthermore, the age of onset of symptoms also broadly varied; for instance, whereas several studies report late infancy (7–15 months of age) as the age of onset of clinical manifestation [37,38,44] another study reports that first clinical manifestations are displayed around the age of 7 [39]. The neurocognitive and behavioral defects seen upon coronin 1 deficiency in humans [6,37,44] are reminiscent of the behavioral alterations observed in coronin 1-deficient mice, including aggression, poor memory formation and defective social interaction where they were shown to be due to defects in the cAMP/protein kinase A signaling pathway [6]. At the level of immune cell composition, however, all the patients irrespective of associated genetic aberrations, showed profound naïve T cell lymphopenia, characterized by drastically reduced CD3+ CD4+CD45RA+ and CD3+ CD8+CD45RA+ cells with relatively minor alterations of B cell and NK cell numbers or their function [6, 38,39,44,45]. Also, in one case, coronin 1 deficiency was found to be associated with reduced NK cell numbers and cytolytic function that were reported to be linked to defective actin deconstruction [45]. Whether or not the reported variations in B cell and natural killer (NK) cell numbers and/or functions are related to the associated genetic aberrations in these patients [39,44,45] rather than coronin
Coronin 1 is the latest entrant in the list of human severe combined immunodeficiency (SCID) spectrum of disorders. Interestingly, the coronin 1 SCID phenotype is characterized by a profound naïve T cell deficiency in the presence of functional B and NK cells as well as an intact thymus. This is in contrast to other SCID phenotypes, such as those occurring as a result of deficiencies in adenosine deaminase (ADA) [47], purine nucleoside phosphorylase (PNP) [47–49] or aberrations in genes involved in antigen receptor rearrangement (RAG1/2) [50], where the thymus is completely absent and additional loss of other immune cell subsets along with T cells is noticed. Although there are other SCID cases displaying Tlow B+ NK+ phenotype, such as those associated with mutations in Forkhead box-1 encoding gene (foxn1), a thymic epithelial cell expressed protein supporting T cell development, the deficiency of FoxN1 is still associated with a rudimentary thymus [51]. As a defective FoxN1-mediated SCID necessitates a thymic transplant rather than a hematopoietic stem cell transplant (HSCT), a thorough genetic analysis would aid in the correct diagnosis and appropriate therapy. Thus, any potential case of primary immunodeficiency must now be screened for a possible coronin 1 defect especially when there is a detectable thymus with naïve T cell lymphopenia. How coronin 1 deficiency exclusively affects the naïve T cell population is currently still poorly understood and will require additional experimental work in the coming years to delineate the precise role for coronin 1 in naïve T cell survival. Acknowledgments RJ is a recipient of Prof Max Cloëtta Medical Research Fellowship. Research in the laboratories of RJ and JP is further financed by the Swiss National Science Foundation (31003A_146463), the Gebert Rüf Foundation and the Canton of Basel. References [1] J. Pieters, P. Muller, R. Jayachandran, On guard: coronin proteins in innate and adaptive immunity, Nat. Rev. Immunol. 13 (2013) 510–518. [2] A.C. Uetrecht, J.E. Bear, Coronins: the return of the crown, Trends Cell Biol. 16 (8) (2006) 421–426. [3] P. Mueller, et al., Regulation of T cell survival through coronin-1-mediated generation of inositol-1,4,5-trisphosphate and calcium mobilization after T cell receptor triggering, Nat. Immunol. 9 (4) (2008) 424–431. [4] L.R. Shiow, et al., The actin regulator coronin 1A is mutant in a thymic egressdeficient mouse strain and in a patient with severe combined immunodeficiency, Nat. Immunol. 9 (11) (2008) 1307–1315. [5] N. Foger, et al., Requirement for coronin 1 in T lymphocyte trafficking and cellular homeostasis, Science 313 (5788) (2006) 839–842. [6] R. Jayachandran, et al., Coronin 1 regulates cognition and behavior through modulation of cAMP/protein kinase A signaling, PLoS Biol. 12 (3) (2014) e1001820. [7] D. Suo, et al., Coronin-1 is a neurotrophin endosomal effector that is required for developmental competition for survival, Nat. Neurosci. 17 (1) (2014) 36–45. [8] M.K. Haraldsson, et al., The lupus-related Lmb3 locus contains a disease-suppressing coronin-1A gene mutation, Immunity 28 (1) (2008) 40–51.
Please cite this article as: R. Jayachandran, J. Pieters, Regulation of immune cell homeostasis and function by coronin 1, Int Immunopharmacol (2015), http://dx.doi.org/10.1016/j.intimp.2015.03.045
4
R. Jayachandran, J. Pieters / International Immunopharmacology xxx (2015) xxx–xxx
[9] B. Mugnier, et al., Coronin-1A links cytoskeleton dynamics to TCR alpha betainduced cell signaling, PLoS One 3 (10) (2008) e3467. [10] G. Ferrari, et al., A coat protein on phagosomes involved in the intracellular survival of mycobacteria, Cell 97 (4) (1999) 435–447. [11] J. Gatfield, J. Pieters, Essential role for cholesterol in entry of mycobacteria into macrophages, Science 288 (5471) (2000) 1647–1650. [12] R. Jayachandran, et al., Survival of mycobacteria in macrophages is mediated by coronin 1-dependent activation of calcineurin, Cell 130 (1) (2007) 37–50. [13] R. Jayachandran, et al., RNA interference in J774 macrophages reveals a role for coronin 1 in mycobacterial trafficking but not in actin-dependent processes, Mol. Biol. Cell 19 (3) (2008) 1241–1251. [14] D. Kumar, et al., Genome-wide analysis of the host intracellular network that regulates survival of Mycobacterium tuberculosis, Cell 140 (5) (2010) 731–743. [15] S. Bosedasgupta, J. Pieters, Inflammatory stimuli reprogram macrophage phagocytosis to macropinocytosis for the rapid elimination of pathogens, PLoS Pathog. 10 (1) (2014) e1003879. [16] S. BoseDasgupta, J. Pieters, Coronin 1 trimerization is essential to protect pathogenic mycobacteria within macrophages from lysosomal delivery, FEBS Lett. 588 (21) (2014) 3898–3905. [17] S. BoseDasgupta, et al., Cytokine-induced macropinocytosis in macrophages is regulated by 14-3-3zeta through its interaction with serine-phosphorylated coronin 1, FEBS J. 282 (2015) 1167–1181. [18] P. Mueller, X. Liu, J. Pieters, Migration and homeostasis of naive T cells depends on coronin 1-mediated prosurvival signals and not on coronin 1-dependent filamentous actin modulation, J. Immunol. 186 (7) (2011) 4039–4050. [19] J. Kirberg, A. Berns, H. von Boehmer, Peripheral T cell survival requires continual ligation of the T cell receptor to major histocompatibility complex-encoded molecules, J. Exp. Med. 186 (8) (1997) 1269–1275. [20] S. Takeda, et al., MHC class II molecules are not required for survival of newly generated CD4 + T cells, but affect their long-term life span, Immunity 5 (3) (1996) 217–228. [21] V.S. Tchang, et al., Diverging role for coronin 1 in antiviral CD4 and CD8 T cell responses, Mol. Immunol. 56 (4) (2013) 683–692. [22] K. Siegmund, et al., Coronin 1-mediated naive T cell survival is essential for the development of autoimmune encephalomyelitis, J. Immunol. 186 (6) (2011) 3452–3461. [23] Miller, Stephen D., William J. Karpus, and Todd Scott Davidson. “Experimental Autoimmune Encephalomyelitis in the Mouse. [24] J. Zhu, H. Yamane, W.E. Paul, Differentiation of effector CD4 T cell populations (*), Annu. Rev. Immunol. 28 (2010) 445–489. [25] S. Kaminski, et al., Coronin 1A is an essential regulator of the TGFbeta receptor/ SMAD3 signaling pathway in Th17 CD4(+) T cells, J. Autoimmun. 37 (3) (2011) 198–208. [26] A.F. Vinet, et al., Initiation of multicellular differentiation in Dictyostelium discoideum is regulated by coronin A, Mol. Biol. Cell 25 (5) (2014) 688–701. [27] B. Combaluzier, et al., Coronin 1 is essential for IgM-mediated Ca2+ mobilization in B cells but dispensable for the generation of immune responses in vivo, J. Immunol. 182 (4) (2009) 1954–1961. [28] V. Kumar, A. Sharma, Neutrophils: Cinderella of innate immune system, Int. Immunopharmacol. 10 (11) (2010) 1325–1334. [29] A. Mocsai, Diverse novel functions of neutrophils in immunity, inflammation, and beyond, J. Exp. Med. 210 (7) (2013) 1283–1299. [30] M. Yan, et al., Coronin function is required for chemotaxis and phagocytosis in human neutrophils, J. Immunol. 178 (9) (2007) 5769–5778.
[31] B. Combaluzier, J. Pieters, Chemotaxis and phagocytosis in neutrophils is independent of coronin 1, J. Immunol. 182 (5) (2009) 2745–2752. [32] A. Grogan, et al., Cytosolic phox proteins interact with and regulate the assembly of coronin in neutrophils, J. Cell Sci. 110 (Pt 24) (1997) 3071–3081. [33] K. Siegmund, et al., Coronin 1 is dispensable for leukocyte recruitment and liver injury in concanavalin A-induced hepatitis, Immunol. Lett. 153 (2013) 62–70. [34] K. Westritschnig, et al., Antigen processing and presentation by dendritic cells is independent of coronin 1, Mol. Immunol. 53 (4) (2013) 379–386. [35] S. Arandjelovic, et al., Mast cell function is not altered by coronin-1A deficiency, J. Leukoc. Biol. 88 (4) (2010) 737–745. [36] N. Foger, et al., Differential regulation of mast cell degranulation versus cytokine secretion by the actin regulatory proteins coronin1a and coronin1b, J. Exp. Med. 208 (9) (2011) 1777–1787. [37] L.R. Shiow, et al., Severe combined immunodeficiency (SCID) and attention deficit hyperactivity disorder (ADHD) associated with a coronin-1A mutation and a chromosome 16p11.2 deletion, Clin. Immunol. 131 (2009) 24–30. [38] D. Moshous, et al., Whole-exome sequencing identifies Coronin-1A deficiency in 3 siblings with immunodeficiency and EBV-associated B-cell lymphoproliferation, J. Allergy Clin. Immunol. 131 (6) (2013) 1594–1603. [39] A. Stray-Pedersen, et al., Compound heterozygous CORO1A mutations in siblings with a mucocutaneous-immunodeficiency syndrome of epidermodysplasia verruciformis-HPV, molluscum contagiosum and granulomatous tuberculoid leprosy, J. Clin. Immunol. 34 (7) (2014) 871–890. [40] D. Punwani, et al., Cellular calibrators to quantitate T-cell receptor excision circles (TRECs) in clinical samples, Mol. Genet. Metab. 107 (3) (2012) 586–591. [41] S. Khare, et al., An NLRP7-containing inflammasome mediates recognition of microbial lipopeptides in human macrophages, Immunity 36 (3) (2012) 464–476. [42] J.D. Farrar, et al., Selective loss of type I interferon-induced STAT4 activation caused by a minisatellite insertion in mouse Stat2, Nat. Immunol. 1 (1) (2000) 65–69. [43] D.S. Cunninghame Graham, et al., Association of NCF2, IKZF1, IRF8, IFIH1, and TYK2 with systemic lupus erythematosus, PLoS Genet. 7 (10) (2011) e1002341. [44] D. Punwani, et al., Coronin-1A: immune deficiency in humans and mice, J. Clin. Immunol. 35 (2015) 100–107. [45] E.M. Mace, J.S. Orange, Lytic immune synapse function requires filamentous actin deconstruction by coronin 1A, Proc. Natl. Acad. Sci. U. S. A. 111 (18) (2014) 6708–6713. [46] S. Moriceau, et al., Coronin-1 is associated with neutrophil survival and is cleaved during apoptosis: potential implication in neutrophils from cystic fibrosis patients, J. Immunol. 182 (11) (2009) 7254–7263. [47] M.S. Hershfield, Adenosine deaminase deficiency: clinical expression, molecular basis, and therapy, Semin. Hematol. 35 (4) (1998) 291–298. [48] M.L. Markert, Purine nucleoside phosphorylase deficiency, Immunodefic. Rev. 3 (1) (1991) 45–81. [49] A. Fleischman, et al., Adenosine deaminase deficiency and purine nucleoside phosphorylase deficiency in common variable immunodeficiency, Clin. Diagn. Lab. Immunol. 5 (3) (1998) 399–400. [50] T. Niehues, R. Perez-Becker, C. Schuetz, More than just SCID–the phenotypic range of combined immunodeficiencies associated with mutations in the recombinase activating genes (RAG) 1 and 2, Clin. Immunol. 135 (2) (2010) 183–192. [51] J. Chou, et al., A novel mutation in FOXN1 resulting in SCID: a case report and literature review, Clin. Immunol. 155 (1) (2014) 30–32.
Please cite this article as: R. Jayachandran, J. Pieters, Regulation of immune cell homeostasis and function by coronin 1, Int Immunopharmacol (2015), http://dx.doi.org/10.1016/j.intimp.2015.03.045
Contents lists available at ScienceDirect
International Immunopharmacology journal homepage: www.elsevier.com/locate/intimp
Review
Regulation of immune cell homeostasis and function by coronin 1 Rajesh Jayachandran ⁎, Jean Pieters Biozentrum, University of Basel, Basel, Switzerland
a r t i c l e
i n f o
Article history: Received 4 March 2015 Accepted 28 March 2015 Available online xxxx Keywords: Coronin T cells B cells NK cells Macrophages Macropinocytosis Calcineurin Calcium Mycobacteria SCID Lymphopenia
a b s t r a c t Coronin 1 is the most recent candidate in the list of genes causing severe combined immunodeficiency (SCID) in humans. A distinctive feature of the SCID induced by coronin 1 deficiency is selective naïve T cell lymphopenia in the presence of a normal thymus as well as normal B cell and natural killer cell numbers (T−B+NK+). Coronin 1 is a member of the evolutionarily conserved coronin protein family, members of which are widely expressed across the eukaryotic kingdom. Mammals express seven coronin molecules, numbered from coronin 1 to 7. The different coronin proteins have a distinct but overlapping tissue expression and have been reported to be involved in a wide array of cellular functions including calcium homeostasis, cytoskeletal dynamics, immune and inflammatory responses, neuromuscular transmission as well as cognition and behavior. In this minireview, we describe the role of coronin 1 in the maintenance of immune cell diversity and function. © 2015 Elsevier B.V. All rights reserved.
Contents 1. 2.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . Murine coronin 1 deficiency and modulation of immune cell population 2.1. Macrophages . . . . . . . . . . . . . . . . . . . . . . . . 2.2. T cells . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3. B cells . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.4. Neutrophils . . . . . . . . . . . . . . . . . . . . . . . . . 2.5. Dendritic cells (DCs) . . . . . . . . . . . . . . . . . . . . . 2.6. Natural killer cells (NK cells) . . . . . . . . . . . . . . . . . 2.7. Mast cells . . . . . . . . . . . . . . . . . . . . . . . . . 3. Human coronin 1-deficiency and modulation of immune cell population 4. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
. . . . . . . . . . . . .
0 0 0 0 0 0 0 0 0 0 0 0 0
1. Introduction Abbreviations: NK cells, natural killer cells; DCs, dendritic cells; ADHD, attention deficit hyperactivity disorder; SCID, severe combined immunodeficiency; NADPH, nicotinamide adenine dinucleotide phosphate; ADA, adenosine deaminase; RAG, recombination activating gene; EAE, experimental autoimmune encephalitis; MOG, myelin-oligodendrocyte glycoprotein; TCR, T cell receptor; IP3, inositol-triphosphate; PI3K, phosphatidyl inositol 3 kinase; BCR, B cell receptor. ⁎ Corresponding author at: Klingelbergstrasse 50, 4156 Basel, Switzerland. Tel.: +41 61 267 14 93; fax: +41 61 267 21 48. E-mail address: [email protected] (R. Jayachandran).
Coronin 1, also known as P57 or TACO (for tryptophan aspartate containing coat protein) is the most widely studied member of the coronin protein family. Coronins are characterized by the presence of multiple WD repeats, that are short domains of approximately 40 amino acid residues terminating with tryptophan-aspartate dipeptide. Coronin 1 is an immune and neuronal lineage-specific protein expressed abundantly in T cells, B cells, macrophages, dendritic cells,
http://dx.doi.org/10.1016/j.intimp.2015.03.045 1567-5769/© 2015 Elsevier B.V. All rights reserved.
Please cite this article as: R. Jayachandran, J. Pieters, Regulation of immune cell homeostasis and function by coronin 1, Int Immunopharmacol (2015), http://dx.doi.org/10.1016/j.intimp.2015.03.045
2
R. Jayachandran, J. Pieters / International Immunopharmacology xxx (2015) xxx–xxx
mast cells, neutrophils and neurons [1,2]. In both mice and human, coronin 1 was found to be important for normal immune cell homeostasis as well as neuronal functioning. With regard to the immune system, coronin 1 deletion predominantly affects the T cell population [3–5] while coronin 1 depletion also causes severe neurobehavioral changes including lowered anxiety, fear memory formation as well as nerve growth factor (NGF)-mediated signaling defects in neurons [6,7]. Upon coronin 1 deficiency in mouse, the total T cell population depletes by almost 80% in the peripheral immune system leaving the other leukocyte population largely intact. Most importantly, the naïve T cells are virtually depleted despite a near normal cellular population in the thymus [3–5,8,9]. In the following sections, we will first discuss in depth the various immune parameters that have been reported to be altered upon depletion of coronin 1 through various gene knockout approaches in mice and secondly briefly review the available information from patients harboring mutations in the coronin 1 gene. 2. Murine coronin 1 deficiency and modulation of immune cell population In mammals, coronin 1 is strongly expressed in all leukocytes in addition to being expressed in neurons. In the following sections, the consequences of coronin 1 deletion in mice on the functionality of the various immune cell populations will be discussed. 2.1. Macrophages Coronin 1 was identified in a screen for host cell factors that were recruited and retained on mycobacterial phagosomes by pathogenic mycobacteria [10,11]. Since pathogenic mycobacteria, such as Mycobacterium tuberculosis, the causative agent of tuberculosis, survives within macrophages by blocking their delivery to lysosomes, it was hypothesized that the absence of coronin 1 would disfavor mycobacterial survival and promote its rapid death and degradation. To test this hypothesis, coronin 1-deficient mice were generated and their bone marrow derived macrophages analyzed. Macrophages lacking coronin 1 did not reveal any abnormalities in number or functional responses including proliferation, phagocytosis of beads and bacteria, migration, chemotaxis, activation, membrane ruffling and morphology [12,13]. However, upon mycobacterial challenge, as hypothesized, these cells efficiently killed M. tuberculosis[12–14], which was found to occur through a defect in the Ca2+/calcineurin activation pathway upon coronin 1-deficiency [12]. More recently, it was shown that trimerization of coronin 1 is a prerequisite for this mycobacteria-mediated calcineurin activation and subsequent mycobacterial survival [15,16]. Additionally, coronin 1 phosphorylation at serine residues under pro-inflammatory situation, mediated via interferon-γ, favors coronin 1 redistribution through its interaction with 14-3-3ζ that ultimately enhances phosphatidyl inositol 3 kinase (PI3K) activity and macropinocytosis thereby switching macrophages from a phagocytic mode to macropinocytic mode and aiding the rapid uptake and clearance of pathogens [17].
signaling and calcineurin activation [3,8,18]. Coronin 1-deficient T cells were furthermore reported to display defective mitochondrial function thereby inducing apoptosis that was linked to defective actin dynamics [5]; However, in a separate study it was found that coronin 1 does not modulate F-actin and that induction of F-actin failed to induce apoptosis [18] and therefore it remains unclear whether or not the deletion of peripheral naïve T cells in the absence of coronin 1 is a consequence of mitochondrial dysfunction or a lack of pro-survival signals normally generated through the T cell receptor [19,20]. Although both CD4+ and CD8+ naïve T cells are depleted upon coronin 1-deficiency, CD8+ T cells from coronin 1-deficient mice are functionally capable of mounting a immune response against various viral challenges [21]. Interestingly, coronin 1 appears to be important for the generation of autoimmune responses. A search for genetic changes that suppresses the lupus phenotype in a mouse model (MRL/LPR) identified a coronin1 mutation resulting in coronin 1 depletion, to be the prime reason for resistance to the lupus phenotype [8]. Also, coronin 1-deficient mice show an attenuated response in an experimental autoimmune encephalitis (EAE) model [22,23]. An important T cell subset regulating autoimmune responses is the Th17 T cell subset that are characterized through the expression of the transcription factor RORγ-t and produce interleukin17 [24]. Interestingly, it was found that Th17 cells in mice lacking coronin 1 expressed both IL-17 and IFNγ quite unlike wild type Th17 cells. This coincided with an increased numbers of IL-17 producing T cells in the central nervous system upon induction of EAE [25]. Thus, coronin 1 appears to play a role in the proper regulation of Th17 immune responses where its absence results in an excessive production of IL-17 along with IFNγ unlike wild type Th17 cells which correlated with defective TGFβR signaling [25]. As mentioned above, the exact reason(s) for naïve T cell depletion upon coronin 1 deficiency remains to be identified, and could well be related to the capacity of coronin 1 to be involved in the processing of cell surface triggers, as is the case for other coronin family members [1,6,26]. 2.3. B cells The population of B cells has been reported to show alteration in total numbers as a result of coronin 1 deletion which was dependent on the source (blood versus spleen versus lymph nodes) analyzed [3, 27]. For example, while in peripheral blood and lymph nodes, B cell numbers are reduced, in spleen their numbers are maintained in near normal numbers [3–5,27]. Coronin 1-deficient B cells show a normal immunoglobulin and B cell receptor expression and development. B cell receptor triggering revealed however attenuated calcium fluxes and proliferation similar to TCR triggered coronin 1-deficient T cells [27]. However, upon coronin 1 deletion, in vivo immune responses against both thymus-dependent and thymus-independent antigens are not significantly different as compared to wild type mice possibly due to the presence of co-stimulatory signals that render coronin 1 dispensable for B cell signaling [27].
2.2. T cells 2.4. Neutrophils While the total leukocyte numbers are around 15 × 106/ml in the peripheral blood of a normal wild type mouse, their numbers were reduced by one-third to approximately 5 × 106/ml in mice lacking coronin 1 [3]. This decrease was almost entirely due to a drastic depletion of peripheral CD3+CD4+ and CD3+CD8+ T lymphocytes [3–5,9]. Analysis of various surface markers within the viable T cells population in coronin 1-deficient mice revealed a specific depletion of the CD62Lhi CD44Lo population that constitutes the naïve T cell subset [3–5]. Unlike wild type T cells, that can be readily activated with T cell receptor (TCR) triggers to elicit cytosolic calcium fluxes, calcineurin activation, and inositol-triphosphate (IP3) production, triggering of the T cell receptors on coronin 1-deficient T cells fails to elicit calcium
Neutrophils form a prime component of the innate immune system and are one of the first immune cell subsets to arrive at the site of inflammation [28,29]. As is the case in other immune cells, coronin 1 is enriched along the leading edge of migrating neutrophils and nascent phagosomes [30]. Neutrophils from coronin 1-deficient mice display no abnormalities with respect to numbers, adherence, membrane dynamics, spreading or chemotaxis [31]. Also, although coronin 1 was shown to interact with PHOX proteins, which are prime components of the NADPH oxidase system [32], no alteration of the oxidative burst was found upon coronin 1 deletion [31]. Furthermore, in a concanavalin A-induced hepatitis model, recruitment of neutrophils to
Please cite this article as: R. Jayachandran, J. Pieters, Regulation of immune cell homeostasis and function by coronin 1, Int Immunopharmacol (2015), http://dx.doi.org/10.1016/j.intimp.2015.03.045
R. Jayachandran, J. Pieters / International Immunopharmacology xxx (2015) xxx–xxx
post-sinusoidal venules and hepatic tissue was shown to be comparable between wild type and coronin 1-deficient mice [33]. 2.5. Dendritic cells (DCs) Bone marrow-derived dendritic cells isolated from coronin 1deficient mice showed that they were comparable to wild type dendritic cells in terms of antigen processing and presentation and subsequent activation of T cells. Thus, coronin 1 appears to be dispensable for antigen processing and presentation by dendritic cells [34]. 2.6. Natural killer cells (NK cells) In terms of their numbers, no striking differences were observed between genotypes, nor with respect to their in vitro cytolytic potential (unpublished observation).
3
1 deficiency per se, remains to be analyzed. Importantly, the single patient analyzed to date with an exclusive coronin 1 deletion in the absence of other genetic aberrations [6,38], shows a normal phenotype with respect to B/NK cell numbers and functionality, although it cannot be excluded that the minimal residual coronin 1 expression may restore some coronin 1 function in this patient. An unrelated study showed that in human neutrophils coronin 1 was able to attenuate apoptosis, and reported that neutrophils from cystic fibrosis patients express elevated levels of coronin 1 thereby possibly suppressing apoptosis and sustaining an inflammatory milieu [46]. Taken together the human data suggest that, as is the case for mouse T cells, coronin 1 is required to provide pro-survival signals, in the absence of which both CD4 as well as CD8 single positive T cells rapidly disappear from the circulation resulting in a severe lymphopenia characterized by a T−NK+B+ SCID phenotype. 4. Conclusions
2.7. Mast cells The role for coronin 1 in murine mast cell function remains presently unclear, with one research group reporting normal functionality of mast cells lacking coronin 1 expression [35] and another group reporting a hyper-degranulation response, reduced cytokine secretion and enhanced passive cutaneous anaphylactic response upon coronin 1 deletion [36]. Whether or not this discrepancy is a result of different mouse strains used in the two studies remains to be established. 3. Human coronin 1-deficiency and modulation of immune cell population Four clinical reports have thus far documented seven individual patients harboring mutations and aberrations in the coronin 1 gene that either result in a total absence or minimal expression of coronin 1 protein [37–40]. It is important to note that only one amongst these four studies report an exclusive coronin 1-deficiency in humans [6,38] while the remaining three case studies document coronin 1 aberration together with other genetic changes, including 16p11.2 micro-deletions, as well as mutations in other genes important for immune function (NLRP7, STAT2, NCF2) [37,39–43]. A comparison of the clinical history of these cases reveals that the affected patients had a widely divergent set of associated health problems, ranging from attention deficient hyperactivity disorder (ADHD), cognitive impairment, aggressiveness, to varied levels of susceptibility to diverse pathogens, including Epstein Barr viral infection, Mycobacterium leprae and human papilloma virus [6,37–39]. Furthermore, the age of onset of symptoms also broadly varied; for instance, whereas several studies report late infancy (7–15 months of age) as the age of onset of clinical manifestation [37,38,44] another study reports that first clinical manifestations are displayed around the age of 7 [39]. The neurocognitive and behavioral defects seen upon coronin 1 deficiency in humans [6,37,44] are reminiscent of the behavioral alterations observed in coronin 1-deficient mice, including aggression, poor memory formation and defective social interaction where they were shown to be due to defects in the cAMP/protein kinase A signaling pathway [6]. At the level of immune cell composition, however, all the patients irrespective of associated genetic aberrations, showed profound naïve T cell lymphopenia, characterized by drastically reduced CD3+ CD4+CD45RA+ and CD3+ CD8+CD45RA+ cells with relatively minor alterations of B cell and NK cell numbers or their function [6, 38,39,44,45]. Also, in one case, coronin 1 deficiency was found to be associated with reduced NK cell numbers and cytolytic function that were reported to be linked to defective actin deconstruction [45]. Whether or not the reported variations in B cell and natural killer (NK) cell numbers and/or functions are related to the associated genetic aberrations in these patients [39,44,45] rather than coronin
Coronin 1 is the latest entrant in the list of human severe combined immunodeficiency (SCID) spectrum of disorders. Interestingly, the coronin 1 SCID phenotype is characterized by a profound naïve T cell deficiency in the presence of functional B and NK cells as well as an intact thymus. This is in contrast to other SCID phenotypes, such as those occurring as a result of deficiencies in adenosine deaminase (ADA) [47], purine nucleoside phosphorylase (PNP) [47–49] or aberrations in genes involved in antigen receptor rearrangement (RAG1/2) [50], where the thymus is completely absent and additional loss of other immune cell subsets along with T cells is noticed. Although there are other SCID cases displaying Tlow B+ NK+ phenotype, such as those associated with mutations in Forkhead box-1 encoding gene (foxn1), a thymic epithelial cell expressed protein supporting T cell development, the deficiency of FoxN1 is still associated with a rudimentary thymus [51]. As a defective FoxN1-mediated SCID necessitates a thymic transplant rather than a hematopoietic stem cell transplant (HSCT), a thorough genetic analysis would aid in the correct diagnosis and appropriate therapy. Thus, any potential case of primary immunodeficiency must now be screened for a possible coronin 1 defect especially when there is a detectable thymus with naïve T cell lymphopenia. How coronin 1 deficiency exclusively affects the naïve T cell population is currently still poorly understood and will require additional experimental work in the coming years to delineate the precise role for coronin 1 in naïve T cell survival. Acknowledgments RJ is a recipient of Prof Max Cloëtta Medical Research Fellowship. Research in the laboratories of RJ and JP is further financed by the Swiss National Science Foundation (31003A_146463), the Gebert Rüf Foundation and the Canton of Basel. References [1] J. Pieters, P. Muller, R. Jayachandran, On guard: coronin proteins in innate and adaptive immunity, Nat. Rev. Immunol. 13 (2013) 510–518. [2] A.C. Uetrecht, J.E. Bear, Coronins: the return of the crown, Trends Cell Biol. 16 (8) (2006) 421–426. [3] P. Mueller, et al., Regulation of T cell survival through coronin-1-mediated generation of inositol-1,4,5-trisphosphate and calcium mobilization after T cell receptor triggering, Nat. Immunol. 9 (4) (2008) 424–431. [4] L.R. Shiow, et al., The actin regulator coronin 1A is mutant in a thymic egressdeficient mouse strain and in a patient with severe combined immunodeficiency, Nat. Immunol. 9 (11) (2008) 1307–1315. [5] N. Foger, et al., Requirement for coronin 1 in T lymphocyte trafficking and cellular homeostasis, Science 313 (5788) (2006) 839–842. [6] R. Jayachandran, et al., Coronin 1 regulates cognition and behavior through modulation of cAMP/protein kinase A signaling, PLoS Biol. 12 (3) (2014) e1001820. [7] D. Suo, et al., Coronin-1 is a neurotrophin endosomal effector that is required for developmental competition for survival, Nat. Neurosci. 17 (1) (2014) 36–45. [8] M.K. Haraldsson, et al., The lupus-related Lmb3 locus contains a disease-suppressing coronin-1A gene mutation, Immunity 28 (1) (2008) 40–51.
Please cite this article as: R. Jayachandran, J. Pieters, Regulation of immune cell homeostasis and function by coronin 1, Int Immunopharmacol (2015), http://dx.doi.org/10.1016/j.intimp.2015.03.045
4
R. Jayachandran, J. Pieters / International Immunopharmacology xxx (2015) xxx–xxx
[9] B. Mugnier, et al., Coronin-1A links cytoskeleton dynamics to TCR alpha betainduced cell signaling, PLoS One 3 (10) (2008) e3467. [10] G. Ferrari, et al., A coat protein on phagosomes involved in the intracellular survival of mycobacteria, Cell 97 (4) (1999) 435–447. [11] J. Gatfield, J. Pieters, Essential role for cholesterol in entry of mycobacteria into macrophages, Science 288 (5471) (2000) 1647–1650. [12] R. Jayachandran, et al., Survival of mycobacteria in macrophages is mediated by coronin 1-dependent activation of calcineurin, Cell 130 (1) (2007) 37–50. [13] R. Jayachandran, et al., RNA interference in J774 macrophages reveals a role for coronin 1 in mycobacterial trafficking but not in actin-dependent processes, Mol. Biol. Cell 19 (3) (2008) 1241–1251. [14] D. Kumar, et al., Genome-wide analysis of the host intracellular network that regulates survival of Mycobacterium tuberculosis, Cell 140 (5) (2010) 731–743. [15] S. Bosedasgupta, J. Pieters, Inflammatory stimuli reprogram macrophage phagocytosis to macropinocytosis for the rapid elimination of pathogens, PLoS Pathog. 10 (1) (2014) e1003879. [16] S. BoseDasgupta, J. Pieters, Coronin 1 trimerization is essential to protect pathogenic mycobacteria within macrophages from lysosomal delivery, FEBS Lett. 588 (21) (2014) 3898–3905. [17] S. BoseDasgupta, et al., Cytokine-induced macropinocytosis in macrophages is regulated by 14-3-3zeta through its interaction with serine-phosphorylated coronin 1, FEBS J. 282 (2015) 1167–1181. [18] P. Mueller, X. Liu, J. Pieters, Migration and homeostasis of naive T cells depends on coronin 1-mediated prosurvival signals and not on coronin 1-dependent filamentous actin modulation, J. Immunol. 186 (7) (2011) 4039–4050. [19] J. Kirberg, A. Berns, H. von Boehmer, Peripheral T cell survival requires continual ligation of the T cell receptor to major histocompatibility complex-encoded molecules, J. Exp. Med. 186 (8) (1997) 1269–1275. [20] S. Takeda, et al., MHC class II molecules are not required for survival of newly generated CD4 + T cells, but affect their long-term life span, Immunity 5 (3) (1996) 217–228. [21] V.S. Tchang, et al., Diverging role for coronin 1 in antiviral CD4 and CD8 T cell responses, Mol. Immunol. 56 (4) (2013) 683–692. [22] K. Siegmund, et al., Coronin 1-mediated naive T cell survival is essential for the development of autoimmune encephalomyelitis, J. Immunol. 186 (6) (2011) 3452–3461. [23] Miller, Stephen D., William J. Karpus, and Todd Scott Davidson. “Experimental Autoimmune Encephalomyelitis in the Mouse. [24] J. Zhu, H. Yamane, W.E. Paul, Differentiation of effector CD4 T cell populations (*), Annu. Rev. Immunol. 28 (2010) 445–489. [25] S. Kaminski, et al., Coronin 1A is an essential regulator of the TGFbeta receptor/ SMAD3 signaling pathway in Th17 CD4(+) T cells, J. Autoimmun. 37 (3) (2011) 198–208. [26] A.F. Vinet, et al., Initiation of multicellular differentiation in Dictyostelium discoideum is regulated by coronin A, Mol. Biol. Cell 25 (5) (2014) 688–701. [27] B. Combaluzier, et al., Coronin 1 is essential for IgM-mediated Ca2+ mobilization in B cells but dispensable for the generation of immune responses in vivo, J. Immunol. 182 (4) (2009) 1954–1961. [28] V. Kumar, A. Sharma, Neutrophils: Cinderella of innate immune system, Int. Immunopharmacol. 10 (11) (2010) 1325–1334. [29] A. Mocsai, Diverse novel functions of neutrophils in immunity, inflammation, and beyond, J. Exp. Med. 210 (7) (2013) 1283–1299. [30] M. Yan, et al., Coronin function is required for chemotaxis and phagocytosis in human neutrophils, J. Immunol. 178 (9) (2007) 5769–5778.
[31] B. Combaluzier, J. Pieters, Chemotaxis and phagocytosis in neutrophils is independent of coronin 1, J. Immunol. 182 (5) (2009) 2745–2752. [32] A. Grogan, et al., Cytosolic phox proteins interact with and regulate the assembly of coronin in neutrophils, J. Cell Sci. 110 (Pt 24) (1997) 3071–3081. [33] K. Siegmund, et al., Coronin 1 is dispensable for leukocyte recruitment and liver injury in concanavalin A-induced hepatitis, Immunol. Lett. 153 (2013) 62–70. [34] K. Westritschnig, et al., Antigen processing and presentation by dendritic cells is independent of coronin 1, Mol. Immunol. 53 (4) (2013) 379–386. [35] S. Arandjelovic, et al., Mast cell function is not altered by coronin-1A deficiency, J. Leukoc. Biol. 88 (4) (2010) 737–745. [36] N. Foger, et al., Differential regulation of mast cell degranulation versus cytokine secretion by the actin regulatory proteins coronin1a and coronin1b, J. Exp. Med. 208 (9) (2011) 1777–1787. [37] L.R. Shiow, et al., Severe combined immunodeficiency (SCID) and attention deficit hyperactivity disorder (ADHD) associated with a coronin-1A mutation and a chromosome 16p11.2 deletion, Clin. Immunol. 131 (2009) 24–30. [38] D. Moshous, et al., Whole-exome sequencing identifies Coronin-1A deficiency in 3 siblings with immunodeficiency and EBV-associated B-cell lymphoproliferation, J. Allergy Clin. Immunol. 131 (6) (2013) 1594–1603. [39] A. Stray-Pedersen, et al., Compound heterozygous CORO1A mutations in siblings with a mucocutaneous-immunodeficiency syndrome of epidermodysplasia verruciformis-HPV, molluscum contagiosum and granulomatous tuberculoid leprosy, J. Clin. Immunol. 34 (7) (2014) 871–890. [40] D. Punwani, et al., Cellular calibrators to quantitate T-cell receptor excision circles (TRECs) in clinical samples, Mol. Genet. Metab. 107 (3) (2012) 586–591. [41] S. Khare, et al., An NLRP7-containing inflammasome mediates recognition of microbial lipopeptides in human macrophages, Immunity 36 (3) (2012) 464–476. [42] J.D. Farrar, et al., Selective loss of type I interferon-induced STAT4 activation caused by a minisatellite insertion in mouse Stat2, Nat. Immunol. 1 (1) (2000) 65–69. [43] D.S. Cunninghame Graham, et al., Association of NCF2, IKZF1, IRF8, IFIH1, and TYK2 with systemic lupus erythematosus, PLoS Genet. 7 (10) (2011) e1002341. [44] D. Punwani, et al., Coronin-1A: immune deficiency in humans and mice, J. Clin. Immunol. 35 (2015) 100–107. [45] E.M. Mace, J.S. Orange, Lytic immune synapse function requires filamentous actin deconstruction by coronin 1A, Proc. Natl. Acad. Sci. U. S. A. 111 (18) (2014) 6708–6713. [46] S. Moriceau, et al., Coronin-1 is associated with neutrophil survival and is cleaved during apoptosis: potential implication in neutrophils from cystic fibrosis patients, J. Immunol. 182 (11) (2009) 7254–7263. [47] M.S. Hershfield, Adenosine deaminase deficiency: clinical expression, molecular basis, and therapy, Semin. Hematol. 35 (4) (1998) 291–298. [48] M.L. Markert, Purine nucleoside phosphorylase deficiency, Immunodefic. Rev. 3 (1) (1991) 45–81. [49] A. Fleischman, et al., Adenosine deaminase deficiency and purine nucleoside phosphorylase deficiency in common variable immunodeficiency, Clin. Diagn. Lab. Immunol. 5 (3) (1998) 399–400. [50] T. Niehues, R. Perez-Becker, C. Schuetz, More than just SCID–the phenotypic range of combined immunodeficiencies associated with mutations in the recombinase activating genes (RAG) 1 and 2, Clin. Immunol. 135 (2) (2010) 183–192. [51] J. Chou, et al., A novel mutation in FOXN1 resulting in SCID: a case report and literature review, Clin. Immunol. 155 (1) (2014) 30–32.
Please cite this article as: R. Jayachandran, J. Pieters, Regulation of immune cell homeostasis and function by coronin 1, Int Immunopharmacol (2015), http://dx.doi.org/10.1016/j.intimp.2015.03.045
