Acta Biomaterialia 10 (2014) 3813–3814
Contents lists available at ScienceDirect
Acta Biomaterialia journal homepage: www.elsevier.com/locate/actabiomat
Editorial
Biomineralization special issue Currently, biomineralization is evolving from its heyday of structural research into one of the most exciting fields of biological materials science, molecular biology, biomedicine and biomimetics. The International Symposia on Biomineralization possess over forty years of tradition. The first symposium was held in Mainz, Germany in 1970. Many highly successful symposia have been held in subsequent years; most recently in Japan (2001), Chile (2005), China (2008) and Australia (2011). This is the second time the symposium has been held in Germany, this time in Freiberg (Saxony). Freiberg (German: free mountain) is a university and mining town in the Free State of Saxony, Germany. The Bergakademie Freiberg is one of the five leading mining schools in the German-speaking countries. It is the oldest in the world, with strong roots in tradition that inform it as a modern center for teaching and research. In recent times Freiberg has made a name for itself throughout Europe as both a high-tech location for micro technology and renewable energy, as well as a center for mineralogy, materials science, and solar technology. Nowadays, the modern equivalents of old Freiberg’s silver are silicon and gallium arsenide. We established the Biomineralogy and Extreme Biomimetics Group at TU Bergakademie Freiberg in October 2010, and in April 2014 we unveiled the new International Master‘s Course in Biomineralogy. The aim of the BIOMIN’12 International Symposium that took place here on 27–30 August 2013 was to bring together more than 200 scientists from different backgrounds, all interested in understanding the principles of biomineralization and bioinspired materials science. Discovery of these natural principles leads to direct, practical applications in numerous directions for biomedicine and technology. It was our special pleasure to welcome our plenary speakers: Arnold J. Kahn (University of California, San Francisco), David Kisailus (Biomimetics and Nanostructured Materials Lab, UC-Riverside), Dirk Schüler (Ludwig-Maximillians-Universität München, Germany), Steve Weiner (Weizmann Institute of Science, Israel) and Rachel Wood (University of Edinburgh, UK). Scientific topics of this symposium included the following: - evolutionary aspects of biomineralization; - molecular and genetic regulation of calcification and silicification from bacteria to vertebrates; - pathological biomineralization and biomineral formation under extreme environmental conditions; and - modern analytical methods and biomimetics. All of these approaches are highlighted in the 19 articles, including two reviews, assembled for this issue. The first review article by Natalie Reznikov, Steve Weiner, Ron Shahar is dedicated to the hierarchical structure of bone in three dimensions. The http://dx.doi.org/10.1016/j.actbio.2014.06.014 1742-7061/Ó 2014 Acta Materialia Inc. Published by Elsevier Ltd. All rights reserved.
authors analyzed current studies with new insights into the 3D structure of various bone materials. These studies revealed the presence of two different materials: the major material being the well-known ordered arrays of mineralized collagen fibrils and associated macromolecules, and the minor component being a relatively disordered material composed of individual collagen fibrils with no preferred orientation, crystals inside – and possibly between – fibrils, and extensive ground mass. A new hierarchical scheme for several bone tissue types that incorporates these two materials is represented in this paper for the first time. The second review prepared by Matej Balázˇ contains modern views on eggshell membrane (ESM) as a platform for applications in materials science. In the first part of this review, the chemical composition and morphology of the ESM is the main issue. The main fields of ESM applications are discussed in the second part. They include its utilization as a biotemplate for the synthesis of nanoparticles, sorbent of heavy metals, organics, dyes, sulfonates and fluorides, the main component of biosensors, the applications in medicine, and a few other fields. The next 17 articles focus on experimentally obtained results. Some of them are traditionally dedicated to molecular and genetic regulation of calcification in bacteria as well as in such invertebrates as mollusks, sponges, echinoderms and fish. For example, consolidation of archaeological gypsum plaster by bacterial biomineralization of calcium carbonate is shown in the contribution from Carlos Rodriguez Navarro. Bernard M. Degnan presents novel data regarding the evolution of the tyrosinase gene family in bivalve molluscs, and confirms independent expansion of the mantle gene repertoire in his work. Biologic control of crystallographic architecture in the mollusk Mytilus edulis is the topic of the article represented by Bernd Jens Maier. Interesting results have been reported in the work by Marcos Farina concerning long range crystalline order in the spicules from the calcareous sponge Paraleucilla magna (Porifera, Calcarea). Novel results on the mesocrystalline nature of sea urchin teeth are represented in the article by Erika Griesshaber. She and co-workers propose the tooth of the sea urchin Paracentrotus lividus to be a hierarchically assembled mesocrystal with a mosaic texture. The self-sharpening feature of the tooth is enabled by the close interplay of the highly evolved microto nanostructure, textural characteristics, distinct calcite grain size variations and a gradation of incorporated organic polymers. Co-location and role of polyphosphates and alkaline phosphatase (ALP) in apatite biomineralization of elasmobranch tesserae is reported by Sidney Omelon. It is proposed that elasmobranch fish skeletal cells control apatite biomineralization by biochemically controlling polyphosphates and ALP production, placement, and activity.
3814
Editorial / Acta Biomaterialia 10 (2014) 3813–3814
Intriguingly, Christoph Simon Füllenbach’s contribution is an article concerning microstructures in shells of the freshwater gastropod Viviparus viviparus, which may be a potential sensor for temperature change. It was observed that the shell’s growth front seems to contain instructions for building specific crystal structure variants irrespective of environmental conditions. However, if this template is missing, the animal forms a deviating crystal structure. Under extremely stressful situations, the gastropod precipitates evolutionarily older crystal structures rather than simple crossed-lamellar structures. Understanding and ultimately mimicking the processes involved in biomineralization may provide new approaches to the fabrication of specialized organic–inorganic hybrid materials. As the research is continuously developed, the main aim is to mimic the syntheses of these biominerals. This scientific direction is represented by the three following articles. In the work of Marc Bohner, the growth kinetics of hexagonal sub-micrometric b-tricalcium phosphate particles in ethylene glycol in vitro is discussed in detail. Katrin Hurle reports on the effect of amorphous phases during the hydraulic conversion of a-tricalcium phosphate into calcium deficient hydroxyapatite. Urease-induced calcification of segmented polymer hydrogels has been proposed by Jörg Tiller in his paper as a step towards artificial biomineralization. Thus, the urease-induced calcification allows formation of carbonate crystals exclusively within the hydrogel, even at room temperature. The influence of network composition, degree of cross-linking, immobilized urease concentration and temperature of calcification were investigated. By varying these parameters, spherical, monolithic clusters – as well as bar-like nanocrystals – with different aspect ratios in spherical or dendritic arrays are formed. It is proposed that this process has the potential to generate a new class of hybrid materials that would be available in macroscopic scale for use in light-weight-design and medicine. Teeth, dentin and enamel are traditional objects of investigations in both classical and modern biomineralogy. This special issue contains three related works. Etienne Balan reported about probing atomic scale transformation of fossil dental enamel using FTIR and NMR spectroscopy. Ultrastructural organization and micromechanical properties of shark tooth enameloid are described and discussed in the article by Helge-Otto Fabritius. Highly sensitive methods such as synchrotron X-ray beam maps, X-ray fluorescence, and X-ray diffraction were used by Stuart Stock in his study on bovine and equine peritubular and intertubular dentin. Recently, exploration as well as application of biomineral-based structures has resulted in the generation of novel materials with specific size, shape, orientation, composition, and hierarchical organization, as well as with specific mechanical properties. Therefore, several articles of our issue are dedicated to mechanical properties of different biocomposites occurring in both invertebrate and vertebrate organisms. Erika Griesshaber investigated the friction and wear behavior, as well as the mechanical properties, of the periostracum of Mytilus sp. The reported results strongly
indicate that the periostracum yields an important contribution to the mollusk shell’s overall wear resistance. Monika Fritz carried out the mapping of nanomechanical properties. She imaged surfaces of freshly grown flat pearl nacre (Haliotis tuberculata) in different stages of growth in seawater using an atomic force microscope (AFM). Characteristic mineral phases of nacre, such as aragonitic stacks of coins, as well as the associated organic sheets are studied in detail. David Kisailus reports on the bio-inspired impact-resistant composites, using the example of a mineralized dactyl club from the smashing predator stomatopod (Odontodactylus scyllarus). This crustacean’s club has been designed to withstand the thousands of high-velocity blows that it delivers to its prey. Through experimental and computational methods, a helicoidal architecture is shown to reduce through-thickness damage propagation in a composite panel during an impact event, resulting in a significant increase in toughness. These findings have implications not only for the design of composite parts for aerospace, but also automotive and armor applications. Finally, the paper by Peter Fratzl and co-workers covers investigations of mechanical and structural properties of bone in noncritical and critical healing in the rat. A fracture in bone results in a dramatic change in the mechanical loading conditions at the site of injury. Usually, bone injuries heal normally but with increasing fracture gaps, healing is retarded, eventually leading to non-unions. The clinical situation of these two processes with different outcomes is well described. However, the exact relation between the mechanical environment and characteristics of the tissues at all levels of structural hierarchy remains unclear. The authors report that in both cases, primary bone formation was followed by secondary bone deposition with mineral particle sizes changed from, on average, short and thick to long and thin particles. Bony bridging occurred at first in the endosteal callus, and the nano- and microstructure developed towards cortical ordered material organization. In contrast, in critical healing, instead of bridging, a marrow cavity closure was formed endosteal; exhibiting tissue structure oriented along the curvature and a periosteal callus with less mature material structure. It is my hope that this issue of Acta Biomaterialia will be interesting not only for the biomineralization community, but also for experts in bioinspired materials chemistry, biomimetics, biophysics, biomedicine and materials science. I cordially thank all of the authors for their impressive contributions, all of the referees for their great work and time, and the editorial staff at Acta Biomaterialia for all of their help in preparing this special issue.
⇑
Hermann Ehrlich Biomineralogy and Extreme Biomimetics Group, Institute of Experimental Physics, TU Bergakademie Freiberg, 09599 Freiberg, Germany ⇑ Tel.:+49 3731 39 2867; fax: +49 3731 39 4314. E-mail address: [email protected] Available online 13 June 2014
Contents lists available at ScienceDirect
Acta Biomaterialia journal homepage: www.elsevier.com/locate/actabiomat
Editorial
Biomineralization special issue Currently, biomineralization is evolving from its heyday of structural research into one of the most exciting fields of biological materials science, molecular biology, biomedicine and biomimetics. The International Symposia on Biomineralization possess over forty years of tradition. The first symposium was held in Mainz, Germany in 1970. Many highly successful symposia have been held in subsequent years; most recently in Japan (2001), Chile (2005), China (2008) and Australia (2011). This is the second time the symposium has been held in Germany, this time in Freiberg (Saxony). Freiberg (German: free mountain) is a university and mining town in the Free State of Saxony, Germany. The Bergakademie Freiberg is one of the five leading mining schools in the German-speaking countries. It is the oldest in the world, with strong roots in tradition that inform it as a modern center for teaching and research. In recent times Freiberg has made a name for itself throughout Europe as both a high-tech location for micro technology and renewable energy, as well as a center for mineralogy, materials science, and solar technology. Nowadays, the modern equivalents of old Freiberg’s silver are silicon and gallium arsenide. We established the Biomineralogy and Extreme Biomimetics Group at TU Bergakademie Freiberg in October 2010, and in April 2014 we unveiled the new International Master‘s Course in Biomineralogy. The aim of the BIOMIN’12 International Symposium that took place here on 27–30 August 2013 was to bring together more than 200 scientists from different backgrounds, all interested in understanding the principles of biomineralization and bioinspired materials science. Discovery of these natural principles leads to direct, practical applications in numerous directions for biomedicine and technology. It was our special pleasure to welcome our plenary speakers: Arnold J. Kahn (University of California, San Francisco), David Kisailus (Biomimetics and Nanostructured Materials Lab, UC-Riverside), Dirk Schüler (Ludwig-Maximillians-Universität München, Germany), Steve Weiner (Weizmann Institute of Science, Israel) and Rachel Wood (University of Edinburgh, UK). Scientific topics of this symposium included the following: - evolutionary aspects of biomineralization; - molecular and genetic regulation of calcification and silicification from bacteria to vertebrates; - pathological biomineralization and biomineral formation under extreme environmental conditions; and - modern analytical methods and biomimetics. All of these approaches are highlighted in the 19 articles, including two reviews, assembled for this issue. The first review article by Natalie Reznikov, Steve Weiner, Ron Shahar is dedicated to the hierarchical structure of bone in three dimensions. The http://dx.doi.org/10.1016/j.actbio.2014.06.014 1742-7061/Ó 2014 Acta Materialia Inc. Published by Elsevier Ltd. All rights reserved.
authors analyzed current studies with new insights into the 3D structure of various bone materials. These studies revealed the presence of two different materials: the major material being the well-known ordered arrays of mineralized collagen fibrils and associated macromolecules, and the minor component being a relatively disordered material composed of individual collagen fibrils with no preferred orientation, crystals inside – and possibly between – fibrils, and extensive ground mass. A new hierarchical scheme for several bone tissue types that incorporates these two materials is represented in this paper for the first time. The second review prepared by Matej Balázˇ contains modern views on eggshell membrane (ESM) as a platform for applications in materials science. In the first part of this review, the chemical composition and morphology of the ESM is the main issue. The main fields of ESM applications are discussed in the second part. They include its utilization as a biotemplate for the synthesis of nanoparticles, sorbent of heavy metals, organics, dyes, sulfonates and fluorides, the main component of biosensors, the applications in medicine, and a few other fields. The next 17 articles focus on experimentally obtained results. Some of them are traditionally dedicated to molecular and genetic regulation of calcification in bacteria as well as in such invertebrates as mollusks, sponges, echinoderms and fish. For example, consolidation of archaeological gypsum plaster by bacterial biomineralization of calcium carbonate is shown in the contribution from Carlos Rodriguez Navarro. Bernard M. Degnan presents novel data regarding the evolution of the tyrosinase gene family in bivalve molluscs, and confirms independent expansion of the mantle gene repertoire in his work. Biologic control of crystallographic architecture in the mollusk Mytilus edulis is the topic of the article represented by Bernd Jens Maier. Interesting results have been reported in the work by Marcos Farina concerning long range crystalline order in the spicules from the calcareous sponge Paraleucilla magna (Porifera, Calcarea). Novel results on the mesocrystalline nature of sea urchin teeth are represented in the article by Erika Griesshaber. She and co-workers propose the tooth of the sea urchin Paracentrotus lividus to be a hierarchically assembled mesocrystal with a mosaic texture. The self-sharpening feature of the tooth is enabled by the close interplay of the highly evolved microto nanostructure, textural characteristics, distinct calcite grain size variations and a gradation of incorporated organic polymers. Co-location and role of polyphosphates and alkaline phosphatase (ALP) in apatite biomineralization of elasmobranch tesserae is reported by Sidney Omelon. It is proposed that elasmobranch fish skeletal cells control apatite biomineralization by biochemically controlling polyphosphates and ALP production, placement, and activity.
3814
Editorial / Acta Biomaterialia 10 (2014) 3813–3814
Intriguingly, Christoph Simon Füllenbach’s contribution is an article concerning microstructures in shells of the freshwater gastropod Viviparus viviparus, which may be a potential sensor for temperature change. It was observed that the shell’s growth front seems to contain instructions for building specific crystal structure variants irrespective of environmental conditions. However, if this template is missing, the animal forms a deviating crystal structure. Under extremely stressful situations, the gastropod precipitates evolutionarily older crystal structures rather than simple crossed-lamellar structures. Understanding and ultimately mimicking the processes involved in biomineralization may provide new approaches to the fabrication of specialized organic–inorganic hybrid materials. As the research is continuously developed, the main aim is to mimic the syntheses of these biominerals. This scientific direction is represented by the three following articles. In the work of Marc Bohner, the growth kinetics of hexagonal sub-micrometric b-tricalcium phosphate particles in ethylene glycol in vitro is discussed in detail. Katrin Hurle reports on the effect of amorphous phases during the hydraulic conversion of a-tricalcium phosphate into calcium deficient hydroxyapatite. Urease-induced calcification of segmented polymer hydrogels has been proposed by Jörg Tiller in his paper as a step towards artificial biomineralization. Thus, the urease-induced calcification allows formation of carbonate crystals exclusively within the hydrogel, even at room temperature. The influence of network composition, degree of cross-linking, immobilized urease concentration and temperature of calcification were investigated. By varying these parameters, spherical, monolithic clusters – as well as bar-like nanocrystals – with different aspect ratios in spherical or dendritic arrays are formed. It is proposed that this process has the potential to generate a new class of hybrid materials that would be available in macroscopic scale for use in light-weight-design and medicine. Teeth, dentin and enamel are traditional objects of investigations in both classical and modern biomineralogy. This special issue contains three related works. Etienne Balan reported about probing atomic scale transformation of fossil dental enamel using FTIR and NMR spectroscopy. Ultrastructural organization and micromechanical properties of shark tooth enameloid are described and discussed in the article by Helge-Otto Fabritius. Highly sensitive methods such as synchrotron X-ray beam maps, X-ray fluorescence, and X-ray diffraction were used by Stuart Stock in his study on bovine and equine peritubular and intertubular dentin. Recently, exploration as well as application of biomineral-based structures has resulted in the generation of novel materials with specific size, shape, orientation, composition, and hierarchical organization, as well as with specific mechanical properties. Therefore, several articles of our issue are dedicated to mechanical properties of different biocomposites occurring in both invertebrate and vertebrate organisms. Erika Griesshaber investigated the friction and wear behavior, as well as the mechanical properties, of the periostracum of Mytilus sp. The reported results strongly
indicate that the periostracum yields an important contribution to the mollusk shell’s overall wear resistance. Monika Fritz carried out the mapping of nanomechanical properties. She imaged surfaces of freshly grown flat pearl nacre (Haliotis tuberculata) in different stages of growth in seawater using an atomic force microscope (AFM). Characteristic mineral phases of nacre, such as aragonitic stacks of coins, as well as the associated organic sheets are studied in detail. David Kisailus reports on the bio-inspired impact-resistant composites, using the example of a mineralized dactyl club from the smashing predator stomatopod (Odontodactylus scyllarus). This crustacean’s club has been designed to withstand the thousands of high-velocity blows that it delivers to its prey. Through experimental and computational methods, a helicoidal architecture is shown to reduce through-thickness damage propagation in a composite panel during an impact event, resulting in a significant increase in toughness. These findings have implications not only for the design of composite parts for aerospace, but also automotive and armor applications. Finally, the paper by Peter Fratzl and co-workers covers investigations of mechanical and structural properties of bone in noncritical and critical healing in the rat. A fracture in bone results in a dramatic change in the mechanical loading conditions at the site of injury. Usually, bone injuries heal normally but with increasing fracture gaps, healing is retarded, eventually leading to non-unions. The clinical situation of these two processes with different outcomes is well described. However, the exact relation between the mechanical environment and characteristics of the tissues at all levels of structural hierarchy remains unclear. The authors report that in both cases, primary bone formation was followed by secondary bone deposition with mineral particle sizes changed from, on average, short and thick to long and thin particles. Bony bridging occurred at first in the endosteal callus, and the nano- and microstructure developed towards cortical ordered material organization. In contrast, in critical healing, instead of bridging, a marrow cavity closure was formed endosteal; exhibiting tissue structure oriented along the curvature and a periosteal callus with less mature material structure. It is my hope that this issue of Acta Biomaterialia will be interesting not only for the biomineralization community, but also for experts in bioinspired materials chemistry, biomimetics, biophysics, biomedicine and materials science. I cordially thank all of the authors for their impressive contributions, all of the referees for their great work and time, and the editorial staff at Acta Biomaterialia for all of their help in preparing this special issue.
⇑
Hermann Ehrlich Biomineralogy and Extreme Biomimetics Group, Institute of Experimental Physics, TU Bergakademie Freiberg, 09599 Freiberg, Germany ⇑ Tel.:+49 3731 39 2867; fax: +49 3731 39 4314. E-mail address: [email protected] Available online 13 June 2014
