Chris Coulombre—A tribute

Chris Coulombre—A tribute

DEVELOPMENTAL BIOLOGY 92, 1-4 (1982) Chris Coulombre-A Tribute In August 1982, Dr. Alfred J. (Chris) Coulombre will retire from a career of nearl...

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DEVELOPMENTAL

BIOLOGY

92, 1-4 (1982)

Chris Coulombre-A

Tribute

In August 1982, Dr. Alfred J. (Chris) Coulombre will retire from a career of nearly 30 years as a distinguished investigator of ocular morphogenesis. His vigorous assaults upon the wellguarded secrets of nature have produced important new knowledge about that most complex and interesting organ, the eye. Through his students and fellows, the impact of his meticulous scientific method has been felt in numerous fields of the biomedical sciences. He will be missed as an active participant in academic ophthalmology. It seems appropriate now to recall some of the highlights of Chris’ career and personality which have assured him an enduring place in the annals of eye research. Chris was born August 15,1922, in Boston. As it did to many, the Great Depression brought hard times on his family. For this reason, Chris spent several years in an orphanage in French Canada. In spite of these difficulties, he quickly demonstrated a capacity for successful hard work that propelled him through an outstanding career. Given his numerous scientific achievements, it may shock many to learn of the somewhat checkered aspects of Chris’ academic career. He had to repeat the fourth grade. The reasons for this setback are not known. Clearly the reversal was only temporary, as he went ahead to pursue collegiate study at Catholic University with his characteristic enthusiasm and brilliance, earning his degree in biology magna cum laude in 1947. His investigative interests were manifest even then. During a summer research studentship at the Jackson Memorial Laboratory in Bar Harbor, Chris showed motion pictures to groups of dogs at the behest of his behavioral psychologist supervisor. This experience led him to the still unchallenged observation that “as an audience, dogs decidedly are not attentive.” During this important undergraduate period he met and married Jane L. Coulombre (1922-1975). A prominent manifestation of their fruitful relationship was many happy years of partnership in the laboratory. After receiving his Ph.D. degree in 1953 from the Johns Hopkins University, under the preceptorship of Dr. Benjamin Willier, Chris assumed the post of assistant professor in the Department of Anatomy at the Yale University School of Medicine. His early publications emphasized the mechanisms of strict morphogenetic control which must operate in the development of the eye, an organ whose functional role depends so critically upon its structure. From the beginning, Chris and Jane utilized the chick embryo almost exclusively in their work. Masterfully employing the techniques of classical experimental embryology appropriately leavened with biochemical approaches, they elucidated the important influences of intraocular pressure in the development of the chick eye as a whole and in morphogenesis of the cornea in particular. Demonstrating the true scientist’s respect for his subject matter, Chris has influenced generations of students and fellows to come to know the chick embryo as “The Director.” Chris moved from Yale University to Bethesda in 1961 to head the Section on Experimental Embryology in the Laboratory of Neuroanatomical Sciences at the National Institutes of Health. He was promoted in 1962 to be Chief of that Laboratory. During that period, the team of Coulombre and Coulombre continued their explorations into ocular morphogenesis. Their areas of interest were expanded by collaborations with a number of individuals on intestinal development and on ocular influences of avian skull morphogenesis. The work attracted considerable attention and respect, as evidenced by the number of chapters which Chris was invited to contribute. Always open to new challenges, Chris accepted, in 1967, the post of Scientific Director of the National Institute of Child Health and Human Development, a largely administrative position. After one year, however, he answered “The Director’s call” to return to the laboratory, and resumed his productive experimentation in ocular morphogenesis as a member of the Ophthalmology Branch of the National Institute of Neurological Diseases and Blindness. In this position, his frequent contacts with Dr. Ludwig von Sallman stimulated a very productive and personal relationship which continued with unabated affection and respect until Dr. von Sall1 0012-1606/82/070001-04$02.00/O Copyright All rights

0 1982 by Academic Press. Inc. of reproduction in any form reserved.

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TRIBUTE

man’s death in 1975. With the creation of the National Eye Institute, Chris assumed, in 1968, the post of Chief of the Section on Experimental Embryology in the Laboratory of Vision Research, a position in which he continued until retirement. Chris was recognized in 1969 with the Friedenwald Award of the Association for Research in Ophthalmology, one of the highest honors of vision research. In the NIH environment, Chris’ work flourished. He developed a number of techniques which allow perturbation of various developmental interactions in the chick embryo, and thereby produced exciting new knowledge about retinal, lens, and cornea1 morphogenesis. His work with several collaborators also dealt with epithelial-mesenchymal and other tissue interactions. Appreciating the tremendous plasticity of embryologic tissues, Chris and Jane discovered metaplastic induction of feathers and scales in the cornea1 epithelium of the chick embryo, one of the most dramatic demonstrations of the importance of epithelial-mesenchymal interactions in morphogenesis. Their elegant studies of the orthogonal pattern of extracellular matrix lamellas in the primary stroma of the developing avian cornea called attention to the crucial morphogenetic role of extracellular structural macromolecules. Those who have had the privilege to know and work with Chris are most aware of the academic honesty and rigor that hallmarked his many outstanding characteristics. In the early seventies, for example, when interest was beginning to focus on extracellular matrix as an important factor in morphogenesis, Chris was heard to admonish “that concept was first proposed by Laguesse and Ladinjinski back around the turn of the century, and I’m prepared to box the ears of anybody who forgets and tries to claim credit otherwise.” Such rigor was altogether evident in the stylistic and semantic precision of Chris’ writings and was imparted in excruciating detail to all who studied with him. Every Coulombre fellow will indelibly recall the occasions of presenting Chris with a manuscript draft for review. After inquiring courteously if he might “have at it with the red pencil”, Chris would isolate and identify every unsupported conclusion and dangling participle that had escaped the naive author’s scrutiny (Fig. 1). Following Jane’s untimely death in 1975, Chris has continued both to provide important preceptorship to a number of younger investigators at the National Eye Institute and to produce papers which are at once admirable in their logical precision and stimulating in their scientific

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scope. Over the years, moreover, he has stimulated and personally assisted numerous investigators in institutions throughout the world. Chris’ interests have always ranged beyond the laboratory. He has a distinguished record of public service including an assignment with the Office of Strategic Services during World War II. As a member of the Paratroop Command Unit, he undoubtedly saw dangerous and exciting duty behind the lines in China. In recent years, he has expanded his horizons both high and low, having pursued the acquisition of piloting skills, as well as mastery of SCUBA diving. His memberships in many museums include not only the institutions one might expect, but also special interest organizations such as the Textile Museum in Washington, D. C., evidence of Chris’ interest in the arts. Rarely content simply to be an observer, he has even tried his hand at weaving. We will all miss Chris as he moves on to pursue his diverse interests, undoubtedly with the same vigor with which he has pursued his research. We are indebted to him for his rich legacy of scientific contributions and his grateful progeny of contributing scientists. DAVID A. NEWSOME ELIZABETH D. HAY KENNETH R. KENYON

THE COULOMBRIANS

(Past Fellows of Chris Coulombre) Paul Anderson David Beale Daniel B. Drachman John Everly Stephen Goldberg Stanislau JaJszczak Kenneth R. Kenyon

Richard Lederman David A. Newsome Stephen Parker Joram Piatigorsky Gordon W. Philpott David Reese

Sonia Rothschild Robert J. Ruben Robert L. Trelstad Yasuhiku Tsunematsu Carl Verruslo Edward R. Wolpow Keith M. Zinn

BIBLIOGRAPHY 1. COULOMBRE,A. J. (1955). Correlations of structural and biochemical changes in the developing retina of the chick. Amer. J Anat. 96, 153-189.

2. COULOMBRE,A. J. (1956). The role of intraocular pressure in the development of the chick eye. I. Control of eye size. J. Exp. ZooL 133, 211-225. 3. COULOMBRE,A. J. (1957). The role of intraocular pressure in the development of the chick eye. II. Control of cornea1 size. Arch. OphthalmoL 57, 250-253. 4. COULOMBRE,A. J., and COULOMBRE,J. L. (1957). The role of intraocular pressure in the development of the chick eye. III. Ciliary body. Amer. J. OphthalmoL 44, 85-92. 5. COULOMBRE,A. J., and COULOMBRE,J. L. (1958). The role of intraocular pressure in the development of the chick eye. IV. Cornea1 curvature. Arch. OphthalmoL 59, 502-506. 6. COULOMBRE,A. J., and COULOMBRE,J. L. (1958). Cornea1 development I. Cornea1 transparency. J. Cell Camp. PhysioL 61, 1-12. 7. COULOMBRE,A. J., and COULOMBRE,J. L. (1958). Cornea1 development. II. Transparency changes during rapid hydration. Amer. J. OphthalmoL 46, 276-280. 8. COULOMBRE,A. J., and COULOMBRE,J. L. (1958). Intestinal development. I. Morphogenesis of the villi and musculature. J. EmbryoL Exp. Mew-phoL 6, 403-411.

9. COULOMBRE,A. J., and CRELIN, E. S. (1958). The role of the developing eye in the morphogenesis of the avian skull. Amer. J. Phys. AnthropoL 16, 25-37. 10. FORBES,T. R., COULOMBRE,A. J., and COULOMBRE,J. L. (1960). Inactivation of progesterone by cellular fractions of rat liver and kidney in vitro. Endocrinology 58, 858-861. 11. COULOMBRE, A. J. (1960).Eye: Anatomy and histology. In “McGrawHill Encyclopedia of Science and Technology” (Lapeles, D. N., ed.), Vol. 5, pp. 1967-1971. McGraw-Hill, New York. 12. COULOMBRE,A .J. (1961). Cytology of the developing eye. In “International Review of Cytology” (Bourne, G., ed.), pp. 161-191. Academic Press, New York. 13. COULOMBRE,A. J., and COULOMBRE, J. L. (1961). The development of the structural and optic properties of the cornea. In “The Structure of the Eye” (Smelser, G., ed.), pp. 405-420. Academic Press, New York. 14. FORBES,T. R., COULOMBRE,A. J., and COULOMBRE,J. L. (1962). Inactivation of progesterone by fetal mouse tissues in vitro. Proc. Sot. Exp. Biol Med. 109, 642-643. 15. DRACHMAN,D. B., and COULOMBRE,A. J. (1962). Method of continuous infusion of fluids into the chorioallantoic circulation of chick embryo. Science 138, 144-145. 16. DRACHMAN, D. B., and COULOMBRE,A. J. (1962). Experimental

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club-foot and arthrogryposis myliplex congentia. Lancet 2, 523526. 17. COULOMBRE, A. J., COULOMBRE,J. L. and MAHTA, H. (1962). The skeleton of the eye. I. Conjunctival papillae and scleral ossicles. Deu. BioL 5, 383-401. 18. COULOMBRE, A. J., STEINBERG,S. N., and COULOMBRE, J. L. (1963). The role of intraocular pressure in the development of the chick eye. V. Pigmented epithelium. Invest. OphthalmoL 2, 83-89. 19. COULOMBRE, J. L. and COULOMBRE, A. J. (1963). Lens development: Fiber elongation lens orientation. Science 142, 1489-1490. 20. COULOMBRE, A. J., and COULOMBRE, J. L. (1964).Lens development. I. Role of the lens in eye growth. J. Exp. ZooL 156, 39-47. 21. COULOMBRE,A. J., and COULOMBRE,J. L. (1964). Cornea1 development. III. Role of the thyroid in dehydration and the development of transparency. Exp. Eye Res. 3,105-114. 22. COULOMBRE,A. J. (1964). Problems in cornea1 morphogenesis. In “Advances in Morphogenesis” (Abercrombie, M., and Brachet, J., eds.), Vol. 4, pp. 81-109. Academic Press, New York. 23. PHILPOTT,G. W., and COULOMBRE, A. J. (1965). Lens development. II The differentiation of embryonic chick lens epithelial cells in vitro and in vivo. Exp. Cell Res. 38, 635-644. 24. COULOMBRE, A. J. (1965). The eye. In “Organogenesis” (Ursprung, H., and DeHaan, R., eds.), pp. 219-251. Holt, Rinehart & Winston, New York. 25. COULOMBRE, J. L. and COULOMBRE,A. J. (1965). Regeneration of neural retina from the pigmented epithelium in the chick embryo. Dev. BioL 12, 79-92. 26. COULOMBRE,A. J. (1965). Experimental embryology of the vertebrate eye. Invest. Ophthalmol 4, 411-419. 27. DELONG, G., and COULOMBRE,A. J. (1965). Development of the retinotectal topographic projection in the chick embryo. Exp. NeuroL 13,351-363. 28. COULOMBRE,A. J., and HERRMAN, H. (1965). Lens development. III. Relationship between the growth of the lens and the growth of the outer eye coat. Exp. Eye Res. 4, 302-311. 29. COULOMBRE, A. J. (1965). The other heritage. Bioscience 15, 602. 30. REYER,R. W., COULOMBRE, A. J., YAMADA, T., and PAPOCONSTANTINOU,J. (1966). Lens differentiation. Science 154, 1682-1687. 31. COULOMBRE, A. J. (1968). Regulation of ocular morphogenesis. In “Refractive Anomalies of the Eye” (NINDB Monograph No. 5), pp. 48-52. U. S. Department of Health, Education and Welfare, PHS. 32. PHILPOTT,G. W., and COULOMBRE, A. J. (1968). Cytodifferentiation of precultured embryonic chick lens epithelial cells in vitro and in vivo. Exp. Cell Res. 52, 140-146.

33. DELONG, G., and COULOMBRE,A. J. (1968). The specificity of retinotectal connections studied by retinal grafts onto the optic tectom in chick embryos. Dev. Biol. 16, 513-531. 34. COULOMBRE,A. J. (1967). Grafting of embryonic rudiments. In “Methods in Developmental Biology” (Wilt, F. H., and Wessels, N. K., eds.), pp. 457-469. Crowell, New York. 35. COULOMBRE,A. J. (1969). Regulation of ocular morphogenesis. Invest. OphthaZmoL 8, 25-30.

36. COULOMBRE, A. J., and VON SALLMANN,L. (1969). On the presentation of the Friedenwald Award in Ophthalmology to Dr. A. J. Coulombre. Invest. OphthalmoL 8, 245-250. 37. COULOMBRE, J. L., and COULOMBRE, A. J. (1969).Lens development. IV. Size, shape and orientation. Invest. OphthalmoL 8, 251-257.

TRIBUTE

38. COULOMBRE, A. J., et al. (1970). Embryonic vertebrate central nervous system revised terminology. Anat. Rec. 166, 257-261. 39. COULOMBRE,J. L., and COULOMBRE,A. J. (1970). Influence on mouse neural retina on regeneration of chick neural retina from chick embryonic pigment epithelium. Nature (London) 228, 559560. 40. COLILOMBRE, A. J. (1970). Development of the vertebrate motor system. In “Neurosciences Second Study Program” (Schmitt, F. O., ed.), pp. 108-116. Rockefeller Univ. Press, New York. 41. COULOMBRE, J. L., and COULOMBRE, A. J. (1971). Lens development. V. Histological analysis of the mechanism of lens reconstitution from implants of lens epithelium. J. Exp. ZooL 176, 15-24. 42. COULOMBRE,J. L., and COULOMBRE,A. J. (1971). Metaplastic induction of scales and feathers in the cornea1 anterior epithelium of the chick embryo. Dev. BioL 25, 464-478. 43. KARLSBERG,R. C., EMERY,J. M., GREEN,W. R., VALDES-DEPENS, M., and COIJLOMBRE, A. J. (1971). Anomalies of iris and anteriorchamber angle. Arch. OphthalmoL 86, 287-292. 44. COULOMBRE,A. J. (1971). Eye (Vertebrate). In “Encyclopedia of Science and Technology,” 3rd ed., Vol. 5, pp. 176-185. McGrawHill, New York. 45. TRELSTAD,R. L., and COULOMBRE,A. J. (1971). Morphogenesis of the collagenous stroma in the chick cornea. J. Cell Biol. 50, 840858. 46. COULOMBRE,A. J., and COULOMBRE,J. L. (1972). Cornea1 development. IV. Interruption of collagen excretion into the primary stroma of the cornea with L-azetidine-2-carboxylic acid. Dev. BioL 28, 183-190. 47. GOLDBERG,S., and COULOMBRE,A. J. (1972). Topographical development of the ganglion cell fiber layer in the chick retina. A whole mount study. J. Cbmp. NeuroL 146, 507-517. 48. COULOMBRE,A. J., and COULOMBRE,J. L. (1973). The skeleton of the eye. II. Overlap of the scleral ossicles of the domestic fowl. Dev. BioL 33, 257-267.

49. COULOMBRE,A. J., JOHNSTON,M. C., and WESTON,J. A. (1974). Conference on neural crest in normal and abnormal embryogenesis. Dev. BioL 36, fl-f5. 50. COULOMBRE,A. J., and COULOMBRE,J. L. (1975). Mechanisms of ocular development. In “The Developing Visual System. Int. Ophthalmol. Clin.” (Zinn, K. M., ed.), Vol. 15, pp. 7-18. Little, Brown, Boston. 51. COULOMBRE,J., and COULOMBRE,A. J. (1975). Cornea1 development. V. Treatment of five-day-old embryos of domestic fowl with 6-diazo-5-oxo-L-norleucine (DON). Dev. BioL 45, 291-303. 52. COULOMBRE,A. J., and COULOMBRE,J. L. (1977). Abnormal organogenesis in the eye. In “Handbook of Teratology” (Wilson, J. G., and Fraser, F. C., eds.), pp. 329-341. Plenum, New York. 53. COULOMBRE,A. J. Roles of the retinal pigment epithelium in the development of ocular tissues. In “The Retinal Pigment Epithehum” (Zinn, K. M., and Marmor, M. F., eds.), Harvard Univ. Press, Cambridge, Mass. 54. JOHNSTON,M. C., NODEN, D. M., HAZELTON, R. D., COULOMBRE, J. L., and COULOMBRE,A. J. (1979). Origins of avian ocular and periocular tissues. Exp. Eye Res. 29, 27-43. A. J. (1979). Cataractogenesis: Developmental inputs 55. COULOMBRE, and constraints. Amer. J. OphthalmoL 86, 1559-1570. 56. TSUNEMATSU,Y., and COULOMBRE,A. J. (1981). Demonstration of transdifferentiation of neural retina from pigmented retina in culture. Dev. Growth D@r. 23, 297-311.