In Memoriam
Marylou Ingram, M.D. (1920–2013) Alexander Nakeff,* Carleton C. Stewart
MARYLOU INGRAM, M.D.
died peacefully in her sleep on Monday, August 12, 2013 at her home in Pasadena, CA. She recently had been hospitalized for a stroke but was released shortly before her death. As a graduate of the University of Rochester School of Medicine and Dentistry, Rochester, NY, most of her professional career at the Department of Radiation Biology and Biophysics was in academic medicine, medical research, and teaching where she focused her research on experimental hematology, radiation biology, cellular biology, and immunology. As one of the pioneers of cytometry, she was actively engaged in discovery for almost 70 years. Her distinguished career included faculty service at the Universities of Rochester, Miami, and California (Los Alamos National Laboratory and CalTech). At the University of Rochester, she was recruited as a member a US Public Health Service team to perform hematologic studies of uranium miners out of a little trailer lab on the Colorado Plateau (140,000 sq miles) that identified the incidence of the rare binucleate lymphocyte (painstakingly eyeballing 1/2,000 WBC on blood smears) as a highly-sensitive
Alexander Nakeff, Ph.D., Professor Internal Medicine, Henry Ford Health System, Detroit, Michigan (retired) Carleton C. Stewart, Emeritus Director, Laboratory of Flow Cytometry, Roswell Park Cancer Institute, Buffalo, NY (retired) *Correspondence to: Alexander Nakleff, 1314 Bedford Road, Grosse Pointe, MIchigan 48230. E-mail: [email protected]
Cytometry Part A 83A: 1051 1054, 2013
indicator of low dose radiation effects. This painstaking visual work led to a collaboration with Ken Preston from Perkin– Elmer that resulted in the development of one of the first automated image analysis systems (CELLSCAN-G10PR) for hematopoietic cell identification that eventually resulted in the commercial development of the Coulter DIFF-3 technology. As graduate students, we were all involved in cell pattern recognition while viewing microscopic slides of blood cells projected in a dark room to develop criteria for the identification of blood cells (by nuclear size and density) and reduce them to rules for the computer. This work, although published in several major journals (1), was a cover feature of Scientific American (in 1970) under the title “Automatic Analysis of Blood Cells” (2). One of Marylou’s projects in the early 60s was to publish a bibliography entitled “Biological Effects of Ionizing Radiation.” This consisted of more than 12,000 annotated references with extensive cross-referencing from the time of Roentgen to about 1965 and was published by the US Gov. Printing Office in 1966 (TID-3097). All of her students helped her collate all the papers ever written on the subject, a passion that consumed her for several years. It was accomplished
Published online in Wiley Online Library (wileyonlinelibrary.com) DOI: 10.1002/cyto.a.22414 C 2013 International Society for Advancement of Cytometry V
In Memoriam before the time of computers and spreadsheets using the extensive Dewey Decimal style outline that she developed for cross-referencing. This outline was also published as a small companion volume to the abstracts. It was a particularly exciting time to be working with a number of graduate students in Marylou’s lab in 1964–1969 that covered so many aspects of hematopoietic stem cell differentiation and proliferation. This included Carl Stewart in lymphopoiesis (3,4), Alex Nakeff in megakaryocytopoiesis (4,5), Alan Coopersmith in erythropoiesis (6), Nancy Minter in platelet kinetics (7), Phil Cooper in progenitor cell release following radiation exposure and Joe Traynor in radiation effects on megakaryocytes. All these studies were made using early image cytometry (Rochester-style) and computer imaging to automate cell differentials, including early development of “spinner” centrifuge techniques for uniform microscopic slide preparation and staining—all of this so beautifully orchestrated by Marylou with the help of Gladys and Bernice as techs and Chet Herman’s former wife Mary (now Mary Chyun) as her secretary. Work was always followed by fun at Marylou’s many parties where Alan and Nancy wrote and performed songs such as “Who Put the Sugar in My Buffer Blues”; the bonds so created were shared for a lifetime. As a mentor, she always supported her students in front of any critics. On the other hand, when she herself was critical of our work, her suggestions for revisions were inevitably delivered in a positive way, face-to-face. Her open-door policy meant that whenever we needed her advice and counsel she was always there. She took great pride in her students’ accomplishments and gave them credit for them, in addition to being very approachable and favored new ideas. At her home, we attended dinner parties to meet with prominent guest researchers such as Drs. Gene Cronkite, Nat Berlin, Vic Bond, Neal Wald, and Fred Stohlman, a number of whom were appointed to each student’s Ph.D. thesis committee. In addition, she and the students met with numerous company representatives (especially Wallace Coulter) to discuss new ideas. The next day we would again meet in the lab to interact and discuss our research projects with them. She encouraged her “progeny” to publish their work in a timely manner as they finished any particular series of experiments; a great idea for young graduate students because when time came to submit our thesis it was just a matter of putting together our publications. Her desk, piled high, was always in evidence. She relished telling of the time that Alan Coopersmith asked her to read a revision he had just made in his thesis and she told him, “Sure, just put in on my desk.” To this he replied, “Not on your life! That is like putting it on quicksand!” After we had graduated, she continued to keenly follow our subsequent scientific and research careers with great pleasure and pride and our continuing relationships morphed from students to colleagues and then life-long friends. At the University of Rochester, there were only one or two women in the medical school classes she attended (8). She was always non-political and never forgot she was a woman in (at that time) a man’s field. She had to deal with a number of 1052
male scientists many of whom did not like dealing with a woman. She had a great technical acumen and loved instruments and new inventions, keeping many technical oddities both in her office and at home. She had a great zest for life: loving music, both classical and jazz, plants, and old movies. She was also known for her keen sense of humor, hardy laugh and was noted for the flamboyant-bright scarves that she wore each day. At a University of Rochester Alumni Reunion in Los Angeles that we attended with Marylou a few years back, the Provost recognized her as the graduate having the longest tenure as an active research scientist. After leaving Rochester in 1969, she spent several years at the University of California Jet Propulsion Labs in Pasadena where her work was related to the potential impact of low gravity on blood cell function during space travel (9). Her work continued for two years (1975–1977) at the University of California, Los Alamos Scientific Laboratory as Principal Investigator on NCI-funded contract research, “Automated Cancer Cell Analysis and Sorting,” that utilized advanced experimental flow cytometry systems (10). In 1977, Wallace Coulter convinced her to establish the Institute for Cell Analysis at the University of Miami as its first Director where she worked with her colleague Brandon Price (11–14). In 1982, she joined the Huntington Medical Research Institute (HMRI) in Pasadena, CA as a Senior Research Scientist and Head of the Tissue Engineering & In Vitro Systems Program to develop the brain tumor immunotherapy project inspired by HMRI Co-founder, Dr. Hunter Shelden (15). Her pioneered effort led to the development of a microgravity tissue culture method funded by NASA using a NASA bioreactor (16). With subsequent funding by the Coulter Foundation, the patented design and construction of the HMRI Histoid Bioreactor resulted in the generation of 3D tumor models, called histoids, containing both stromal and epithelial cells in a self-assembled, tissue-like architecture (17–19). These human “mini-tumors” of breast, prostate, pancreas, colon, and bladder cancer origin hold great promise for screening new anticancer drugs, representing a reference standard for improved tumor diagnosis and individualized therapy, as well as “seeds” for regenerating replacement tissues in vitro. Marylou again assembled an impressive team, including Dr. Geza Techy and Brenda Ward, who worked diligently with her over her last years perfecting this unique bio-system. She established long-term scientific and personal relationships with many of her HMRI colleagues, including Drs. Faye Eggerding, Michael Harrington, Larry Jones and the late Richard Bing. She never retired but remained actively involved in her research program until the end of her life and enjoyed living every day in her dear Spanish hacienda in the hills of Pasadena, California that she purchased back in 1972. In May of this year, we attended the ISAC CYTO 2013 meeting with Marylou in San Diego where her long-time membership in ISAC and her pioneering contributions to the advancement of cytometry were recognized with the establishment of the Marylou Ingram Lecture. As the first speaker, Dr. Vera Donnenberg (University of Pittsburgh) presented work on tumor In Memoriam
In Memoriam
L-R: Nancy Minter, Alan Coopersmith, Alex Nakeff, John Glover, Carleton Stewart
stem cells and tissue regeneration, the latter dear to Marylou’s heart. A generous bequest from Marylou will be used to establish a continuing legacy in her name to support advances in tissue engineering at the University of Rochester. From the most humble of beginnings in Ashtabula, Ohio, Marylou created a lasting legacy. She was an amazing scientist whose long career was full of discovery, innovation, perseverance, and leadership; an amazing woman who was successful in a predominantly man’s world; and an amazingly loyal mentor and friend who created a role model for the many young scientists to follow. She left, with those of us fortunate to have been her students and colleagues, a profound appreciation of the scientific method with a keen sense of the value of words one uses to communicate, clearly and concisely, complex scientific ideas and concepts. The following summarizes, in her own words, not only the power of poetry but also the power of communication of the written word, a passion she passed on to all of us that shared the privilege of working with her:
ABOUT POEMS When sonnets thrived and, like most poems, grew On formal verbal lattices, they drank Their nutrients through the sturdy frames that held And guided their ascendancies and from The compost where dead words and phrases fell When pruning shaped the verse, and set them free Poems now, no longer tethered, grow Relaxed, colloquial, guided only by The poet’s will to capture and convey A piercing insight, striving to be shared But if the author’s vision is too dim Cytometry Part A 83A: 1051 1054, 2013
Mary Chyun and Marylou Ingram at GLIIFCA meeting , 1994 at the Hotel St. Regis, Detroit
No form or meter, no syntactic trim Can give the writer what true poets need: The power to see the germ within the seed. Marylou Ingram, M.D. Pasadena, CA, 2008 Our memories of Marylou, shared by: Alexander Nakeff Carleton C. Stewart
LITERATURE CITED 1. Ingram M, Preston K Jr. Importance of automatic recognition techniques in the early detection of altered blood-cell production. Ann NY Acad Sci 1964;113:1066–1072. 2. Ingram M, Preston K Jr. Automatic analysis of blood cells. Sci Am 1970;223:72–82. 3. Stewart CC, Ingram M. A method for counting phytohemagglutinin-stimulated lymphocytes. Blood 1967;29:628–639. 4. Stewart CC, Nakeff A, Ingram M. Kinetics of erythrocyte and lymphocyte agglutination by PHA. J Immunol 1968;100:1121–1126. 5. Nakeff A, Ingram M. Platelet count–volume relationships in four mammalian species. J Appl Physiol 1970;28:530–533. 6. Coopersmith A, Ingram M. Red cell volumes and erythropoiesis. I. Age:density:volume relationships of normocytes. Am J Physiol 1968;215:1276–1283. 7. Minter FM, Ingram M. Platelet volume:density relationships in normal and acutelybled dogs. Br J Haematol 1971;20:55–68. 8. Ingram M. Some constructive applications of atomic energy. J Am Med Womans Assoc 1955;10:37–40. 9. Huff JE, Kaufman GE, Ingram M. Hematological changes in mice during and after exposure to severe hypobaric hypoxia. Aviat Space Environ Med 1975;46:1147–1151. 10. Salzman GC, Crowell JM, Hansen KM, Ingram M, Mullaney PF. Gynecologic specimen analysis by multiangle light scattering in a flow system. J Histochem Cytochem 1976;24:308–314. 11. Ingram M, Cleary TJ, Price BJ, Price RL III, Castro A. Rapid detection of Legionella pneumophila by flow cytometry. Cytometry 1982;3:134–137. 12. Martinez OV, Gratzner HG, Malinin TI, Ingram M. The effect of some beta-lactam antibiotics on Escherichia coli studied by flow cytometry. Cytometry 1982;3:129–133. 13. Miller AM, Wu MC, Files N, Ingram M, Yunis AA. Purification of human granulocyte-macrophage progenitor cells (CFU-C) using indirect immunofluorescence and cell sorting. Stem Cells 1982;1:193–205.
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In Memoriam 14. Rabinovitch A, Russell T, Shienvold F, Noel J, Files N, Patel Y, Ingram M. Preparation of rat-islet B-Cell-enriched fractions by light-scatter flow cytometry. Diabetes 1982; 31:939–943. 15. Ingram M, Shelden CH, Jacques S, Skillen RG, Bradley WG, Techy GB, Freshwater DB, Abts RM, Rand RW. Preliminary clinical trial of immunotherapy for malignant glioma. J Biol Response Mod 1987;6:489–498. 16. Ingram M, Techy GB, Saroufeem R, Yazan O, Narayan KS, Goodwin TJ, Spaulding GF. Three-dimensional growth patterns of various human tumor cell lines in simulated microgravity of a NASA bioreactor. In Vitro Cell Dev Biol Anim 1997;33:459–466.
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17. Ingram M, Techy GB, Ward BR, Imam SA, Atkinson R, Ho H, Taylor CR. Tissue engineered tumor models. Biotechnol Histochem 2010;85:213–229. 18. Kaur P, Ward BR, Saha B, Young L, Groshen S, Techy GB, Lu Y, Atkinson R, Taylor CR, Ingram M, Imam SA. Human breast cancer histoid: An in vitro 3-dimensional co-culture model that mimics breast cancer tissue. J Histochem Cytochem 2011;59: 1087–1100. 19. Mehta G, Hsiao AY, Ingram M, Luker GD, Takayama S. Opportunities and challenges for use of tumor spheroids as models to test drug delivery and efficacy. J Control Release 2012;164:192–204.
In Memoriam
Marylou Ingram, M.D. (1920–2013) Alexander Nakeff,* Carleton C. Stewart
MARYLOU INGRAM, M.D.
died peacefully in her sleep on Monday, August 12, 2013 at her home in Pasadena, CA. She recently had been hospitalized for a stroke but was released shortly before her death. As a graduate of the University of Rochester School of Medicine and Dentistry, Rochester, NY, most of her professional career at the Department of Radiation Biology and Biophysics was in academic medicine, medical research, and teaching where she focused her research on experimental hematology, radiation biology, cellular biology, and immunology. As one of the pioneers of cytometry, she was actively engaged in discovery for almost 70 years. Her distinguished career included faculty service at the Universities of Rochester, Miami, and California (Los Alamos National Laboratory and CalTech). At the University of Rochester, she was recruited as a member a US Public Health Service team to perform hematologic studies of uranium miners out of a little trailer lab on the Colorado Plateau (140,000 sq miles) that identified the incidence of the rare binucleate lymphocyte (painstakingly eyeballing 1/2,000 WBC on blood smears) as a highly-sensitive
Alexander Nakeff, Ph.D., Professor Internal Medicine, Henry Ford Health System, Detroit, Michigan (retired) Carleton C. Stewart, Emeritus Director, Laboratory of Flow Cytometry, Roswell Park Cancer Institute, Buffalo, NY (retired) *Correspondence to: Alexander Nakleff, 1314 Bedford Road, Grosse Pointe, MIchigan 48230. E-mail: [email protected]
Cytometry Part A 83A: 1051 1054, 2013
indicator of low dose radiation effects. This painstaking visual work led to a collaboration with Ken Preston from Perkin– Elmer that resulted in the development of one of the first automated image analysis systems (CELLSCAN-G10PR) for hematopoietic cell identification that eventually resulted in the commercial development of the Coulter DIFF-3 technology. As graduate students, we were all involved in cell pattern recognition while viewing microscopic slides of blood cells projected in a dark room to develop criteria for the identification of blood cells (by nuclear size and density) and reduce them to rules for the computer. This work, although published in several major journals (1), was a cover feature of Scientific American (in 1970) under the title “Automatic Analysis of Blood Cells” (2). One of Marylou’s projects in the early 60s was to publish a bibliography entitled “Biological Effects of Ionizing Radiation.” This consisted of more than 12,000 annotated references with extensive cross-referencing from the time of Roentgen to about 1965 and was published by the US Gov. Printing Office in 1966 (TID-3097). All of her students helped her collate all the papers ever written on the subject, a passion that consumed her for several years. It was accomplished
Published online in Wiley Online Library (wileyonlinelibrary.com) DOI: 10.1002/cyto.a.22414 C 2013 International Society for Advancement of Cytometry V
In Memoriam before the time of computers and spreadsheets using the extensive Dewey Decimal style outline that she developed for cross-referencing. This outline was also published as a small companion volume to the abstracts. It was a particularly exciting time to be working with a number of graduate students in Marylou’s lab in 1964–1969 that covered so many aspects of hematopoietic stem cell differentiation and proliferation. This included Carl Stewart in lymphopoiesis (3,4), Alex Nakeff in megakaryocytopoiesis (4,5), Alan Coopersmith in erythropoiesis (6), Nancy Minter in platelet kinetics (7), Phil Cooper in progenitor cell release following radiation exposure and Joe Traynor in radiation effects on megakaryocytes. All these studies were made using early image cytometry (Rochester-style) and computer imaging to automate cell differentials, including early development of “spinner” centrifuge techniques for uniform microscopic slide preparation and staining—all of this so beautifully orchestrated by Marylou with the help of Gladys and Bernice as techs and Chet Herman’s former wife Mary (now Mary Chyun) as her secretary. Work was always followed by fun at Marylou’s many parties where Alan and Nancy wrote and performed songs such as “Who Put the Sugar in My Buffer Blues”; the bonds so created were shared for a lifetime. As a mentor, she always supported her students in front of any critics. On the other hand, when she herself was critical of our work, her suggestions for revisions were inevitably delivered in a positive way, face-to-face. Her open-door policy meant that whenever we needed her advice and counsel she was always there. She took great pride in her students’ accomplishments and gave them credit for them, in addition to being very approachable and favored new ideas. At her home, we attended dinner parties to meet with prominent guest researchers such as Drs. Gene Cronkite, Nat Berlin, Vic Bond, Neal Wald, and Fred Stohlman, a number of whom were appointed to each student’s Ph.D. thesis committee. In addition, she and the students met with numerous company representatives (especially Wallace Coulter) to discuss new ideas. The next day we would again meet in the lab to interact and discuss our research projects with them. She encouraged her “progeny” to publish their work in a timely manner as they finished any particular series of experiments; a great idea for young graduate students because when time came to submit our thesis it was just a matter of putting together our publications. Her desk, piled high, was always in evidence. She relished telling of the time that Alan Coopersmith asked her to read a revision he had just made in his thesis and she told him, “Sure, just put in on my desk.” To this he replied, “Not on your life! That is like putting it on quicksand!” After we had graduated, she continued to keenly follow our subsequent scientific and research careers with great pleasure and pride and our continuing relationships morphed from students to colleagues and then life-long friends. At the University of Rochester, there were only one or two women in the medical school classes she attended (8). She was always non-political and never forgot she was a woman in (at that time) a man’s field. She had to deal with a number of 1052
male scientists many of whom did not like dealing with a woman. She had a great technical acumen and loved instruments and new inventions, keeping many technical oddities both in her office and at home. She had a great zest for life: loving music, both classical and jazz, plants, and old movies. She was also known for her keen sense of humor, hardy laugh and was noted for the flamboyant-bright scarves that she wore each day. At a University of Rochester Alumni Reunion in Los Angeles that we attended with Marylou a few years back, the Provost recognized her as the graduate having the longest tenure as an active research scientist. After leaving Rochester in 1969, she spent several years at the University of California Jet Propulsion Labs in Pasadena where her work was related to the potential impact of low gravity on blood cell function during space travel (9). Her work continued for two years (1975–1977) at the University of California, Los Alamos Scientific Laboratory as Principal Investigator on NCI-funded contract research, “Automated Cancer Cell Analysis and Sorting,” that utilized advanced experimental flow cytometry systems (10). In 1977, Wallace Coulter convinced her to establish the Institute for Cell Analysis at the University of Miami as its first Director where she worked with her colleague Brandon Price (11–14). In 1982, she joined the Huntington Medical Research Institute (HMRI) in Pasadena, CA as a Senior Research Scientist and Head of the Tissue Engineering & In Vitro Systems Program to develop the brain tumor immunotherapy project inspired by HMRI Co-founder, Dr. Hunter Shelden (15). Her pioneered effort led to the development of a microgravity tissue culture method funded by NASA using a NASA bioreactor (16). With subsequent funding by the Coulter Foundation, the patented design and construction of the HMRI Histoid Bioreactor resulted in the generation of 3D tumor models, called histoids, containing both stromal and epithelial cells in a self-assembled, tissue-like architecture (17–19). These human “mini-tumors” of breast, prostate, pancreas, colon, and bladder cancer origin hold great promise for screening new anticancer drugs, representing a reference standard for improved tumor diagnosis and individualized therapy, as well as “seeds” for regenerating replacement tissues in vitro. Marylou again assembled an impressive team, including Dr. Geza Techy and Brenda Ward, who worked diligently with her over her last years perfecting this unique bio-system. She established long-term scientific and personal relationships with many of her HMRI colleagues, including Drs. Faye Eggerding, Michael Harrington, Larry Jones and the late Richard Bing. She never retired but remained actively involved in her research program until the end of her life and enjoyed living every day in her dear Spanish hacienda in the hills of Pasadena, California that she purchased back in 1972. In May of this year, we attended the ISAC CYTO 2013 meeting with Marylou in San Diego where her long-time membership in ISAC and her pioneering contributions to the advancement of cytometry were recognized with the establishment of the Marylou Ingram Lecture. As the first speaker, Dr. Vera Donnenberg (University of Pittsburgh) presented work on tumor In Memoriam
In Memoriam
L-R: Nancy Minter, Alan Coopersmith, Alex Nakeff, John Glover, Carleton Stewart
stem cells and tissue regeneration, the latter dear to Marylou’s heart. A generous bequest from Marylou will be used to establish a continuing legacy in her name to support advances in tissue engineering at the University of Rochester. From the most humble of beginnings in Ashtabula, Ohio, Marylou created a lasting legacy. She was an amazing scientist whose long career was full of discovery, innovation, perseverance, and leadership; an amazing woman who was successful in a predominantly man’s world; and an amazingly loyal mentor and friend who created a role model for the many young scientists to follow. She left, with those of us fortunate to have been her students and colleagues, a profound appreciation of the scientific method with a keen sense of the value of words one uses to communicate, clearly and concisely, complex scientific ideas and concepts. The following summarizes, in her own words, not only the power of poetry but also the power of communication of the written word, a passion she passed on to all of us that shared the privilege of working with her:
ABOUT POEMS When sonnets thrived and, like most poems, grew On formal verbal lattices, they drank Their nutrients through the sturdy frames that held And guided their ascendancies and from The compost where dead words and phrases fell When pruning shaped the verse, and set them free Poems now, no longer tethered, grow Relaxed, colloquial, guided only by The poet’s will to capture and convey A piercing insight, striving to be shared But if the author’s vision is too dim Cytometry Part A 83A: 1051 1054, 2013
Mary Chyun and Marylou Ingram at GLIIFCA meeting , 1994 at the Hotel St. Regis, Detroit
No form or meter, no syntactic trim Can give the writer what true poets need: The power to see the germ within the seed. Marylou Ingram, M.D. Pasadena, CA, 2008 Our memories of Marylou, shared by: Alexander Nakeff Carleton C. Stewart
LITERATURE CITED 1. Ingram M, Preston K Jr. Importance of automatic recognition techniques in the early detection of altered blood-cell production. Ann NY Acad Sci 1964;113:1066–1072. 2. Ingram M, Preston K Jr. Automatic analysis of blood cells. Sci Am 1970;223:72–82. 3. Stewart CC, Ingram M. A method for counting phytohemagglutinin-stimulated lymphocytes. Blood 1967;29:628–639. 4. Stewart CC, Nakeff A, Ingram M. Kinetics of erythrocyte and lymphocyte agglutination by PHA. J Immunol 1968;100:1121–1126. 5. Nakeff A, Ingram M. Platelet count–volume relationships in four mammalian species. J Appl Physiol 1970;28:530–533. 6. Coopersmith A, Ingram M. Red cell volumes and erythropoiesis. I. Age:density:volume relationships of normocytes. Am J Physiol 1968;215:1276–1283. 7. Minter FM, Ingram M. Platelet volume:density relationships in normal and acutelybled dogs. Br J Haematol 1971;20:55–68. 8. Ingram M. Some constructive applications of atomic energy. J Am Med Womans Assoc 1955;10:37–40. 9. Huff JE, Kaufman GE, Ingram M. Hematological changes in mice during and after exposure to severe hypobaric hypoxia. Aviat Space Environ Med 1975;46:1147–1151. 10. Salzman GC, Crowell JM, Hansen KM, Ingram M, Mullaney PF. Gynecologic specimen analysis by multiangle light scattering in a flow system. J Histochem Cytochem 1976;24:308–314. 11. Ingram M, Cleary TJ, Price BJ, Price RL III, Castro A. Rapid detection of Legionella pneumophila by flow cytometry. Cytometry 1982;3:134–137. 12. Martinez OV, Gratzner HG, Malinin TI, Ingram M. The effect of some beta-lactam antibiotics on Escherichia coli studied by flow cytometry. Cytometry 1982;3:129–133. 13. Miller AM, Wu MC, Files N, Ingram M, Yunis AA. Purification of human granulocyte-macrophage progenitor cells (CFU-C) using indirect immunofluorescence and cell sorting. Stem Cells 1982;1:193–205.
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In Memoriam 14. Rabinovitch A, Russell T, Shienvold F, Noel J, Files N, Patel Y, Ingram M. Preparation of rat-islet B-Cell-enriched fractions by light-scatter flow cytometry. Diabetes 1982; 31:939–943. 15. Ingram M, Shelden CH, Jacques S, Skillen RG, Bradley WG, Techy GB, Freshwater DB, Abts RM, Rand RW. Preliminary clinical trial of immunotherapy for malignant glioma. J Biol Response Mod 1987;6:489–498. 16. Ingram M, Techy GB, Saroufeem R, Yazan O, Narayan KS, Goodwin TJ, Spaulding GF. Three-dimensional growth patterns of various human tumor cell lines in simulated microgravity of a NASA bioreactor. In Vitro Cell Dev Biol Anim 1997;33:459–466.
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17. Ingram M, Techy GB, Ward BR, Imam SA, Atkinson R, Ho H, Taylor CR. Tissue engineered tumor models. Biotechnol Histochem 2010;85:213–229. 18. Kaur P, Ward BR, Saha B, Young L, Groshen S, Techy GB, Lu Y, Atkinson R, Taylor CR, Ingram M, Imam SA. Human breast cancer histoid: An in vitro 3-dimensional co-culture model that mimics breast cancer tissue. J Histochem Cytochem 2011;59: 1087–1100. 19. Mehta G, Hsiao AY, Ingram M, Luker GD, Takayama S. Opportunities and challenges for use of tumor spheroids as models to test drug delivery and efficacy. J Control Release 2012;164:192–204.
In Memoriam
