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On the Beginnings of Somatic Cell Hybridization Copyright 0 1992 by the Genetics Society of America Perspectives Anecdotal, Historical and Critical Commentaries on Genetics Edited by James F. Crow and William F. Dove On the Beginningsof Somatic Cell Hybridization:BORIS EPHRUSSI and Chromosome Transplantation Doris T. Zallen and Richard M. Burian Center for the Study of Science in Society, Virginia Polytechnic Institute and State University, Blacksburg, Virginia 24061 WO papers published in GENETICS November,in ganisms, he consistently found ways to explant, im- T 1966 represent a key step in a decade of re- plant, or otherwise transfer organs, tissues, cells and search in the laboratories of BORIS EPHRUSSI(1901- nuclei into foreign organismal environments, combin- 1979), research that helped transform mammalian ing these techniques with what he called “the genetical genetics, especially human genetics. These papers, tool.” He used the behavior of the transplant in the coauthored with MARY WEISS,then a graduate stu- new context to test hypotheses about its regulation dent in EPHRUSSI’Slaboratory at Western Reserve and control of its destiny, and about how it interacted University in Cleveland (WEISS and EPHRUSSI with and was influenced by its host. In this respect, 1966a,b), provided the first detailed reports of the his work with somatic cell hybrids is best understood formation of viable and self-perpetuating hybrids be- as a way of transplanting chromosomes, chromosome tween somatic cells of two different species, mouse arms, or blocks of genes into a genetically and cyto- and rat (preliminary reports in EPHRUSSIand WEISS plasmically foreign context. Although it fell short of 1965; EPHRUSSI1966). Such hybrids contributed cru- the ideal of transplanting single genes, it was a natural cially to the development of somatic cell geneticsand extension of EPHRUSSI’Sapproach and allowed him to soon provided an important tool for efforts to gain gain insights (and develop tools for others to gain detailed information about theorganization of genetic insights) into complexities of development that had information in human chromosomes(WEISS and eluded him ever since his early work with tissue cul- GREEN1967). ture and withsea urchin development as a young Although the techniques described in these papers researcher in Paris in the 1920s. played an important role in the development of formal Harnessing transplantation: From the start of his human genetics, this outcome was quite distant from scientific training in France in 1920 as a Russian EPHRUSSI’Sown scientific goals. His primary interest kmigri, EPHRUSSIstudied the initiation and regulation in constructing such “zoological oddities” as interspe- of embryological processesby intracellular and extra- cific hybrids was to develop tools for analyzing the cellular factors. A major strand of his early research processes of determination, differentiation and regu- concerned the effect of temperature on the develop- lation in development, including their bearing on ment of fertilized sea urchin eggs (e.g., EPHRUSSI oncogenesis. We will show that the work on interspe- 1923, 1932). In this work he employed a relatively cific hybrids was a natural culmination of investiga- new apparatus, a micromanipulator. ROBERTCHAM- tions that occupied EPHRUSSIthroughout his career BERS, an American biologist, had developed an accu- and how the investigations described by WEISS and rate manipulator, enabling one to alter single cells by EPHRUSSI(1966a,b) grew out of the EPHRUSSI’S life- inserting (or extracting) small quantities of substances long effort to develop tools for understanding funda- into (or from) them. In Paris in April, 1925, CHAM- mental developmental processes (see BURIAN,GAYON BERS personally instructed LOUISRAPKINE, a fellow and ZALLEN 1991; SAPP1987, Chap. 5). student and a close friend of EPHRUSSI’S,in its use. We will particularly emphasize EPHRUSSI’Sstrategic RAPKINE,interested in chemical processes in the cell, use of methods involving variations on the theme of employed the micromanipulator in a series of studies transplantation. Working with a great variety of or- on cellular physiology during developmental change Genetics 1.32: 1-8 (September, 1992) 2 D. T. Zallen and R. M. Burian to probe the chemical state within individual cells. He that allowed implantation of imaginal disks into Dro- and EPHRUSSI,working singly and together at the sophila larvae. As EPHRUSSIand BEADLEdescribed the Collige de France and the Roscoff Marine Biological procedure they developed: Station, studied chemical changes that occurred dur- The essential part of the technique . is the actual opera- ingthe course of sea urchindevelopment (e.g., tion of injection of the desired tissue by means of a micro- EPHRUSSIand RAPKINE1928). EPHRUSSIthus became pipette. We have used the technique in implanting gonads familiar with the operation of the instrument and the and various imaginal disks . The assembly that we use is opportunities it offeredtotrack developmental that of the standard Chambers micro-injection apparatus changes by probing and altering internal and external (EPHRUSSIand BEADLE1936, pp. 218, 219,221). cellular environments. EPHRUSSI’Ssecond dissertation (two were then Striking results were obtained by implanting ima- standard in France) was a project on tissue culture ginal disks of various genotypes, fated to form eyes, (EPHRUSSI1933a; see also EPHRUSSI1935a). Despite into genetically foreign larvae. EPHRUSSIand BEADLE difficulties associated with the early unsatisfactory tis- demonstrated that flies with wild-type alleles at the sue culture techniques,EPHRUSSI concluded from this vermilion and cinnabar loci produced substances re- quired in successive steps for the production of the work and two explantation studies of brachyury in brown eye pigment normally found in Drosophila. mice (EPHRUSSI1933b, 1935b), that intrinsic factors These and other results obtained by implanting var- (ie., genes) play a key role in development. ious imaginal discs and organs, and injecting hemo- Harnessing genetics: In the next phase of his ca- lymph, provided some insights into the pathways by reer, EPHRUSSIcoupled his embryological concerns to which genes affect phenotypic characteristics by con- a firm conviction that one must understand the role trolling the production of diffusible substances (see of genes in order to decipher embryological processes. BURIAN,GAYON and ZALLEN 1988, pp. 389-400). Supported by a Rockefeller Foundation fellowship, Starting fromthis basis, BEADLEand TATUM,working EPHRUSSIwent to Caltech in 1934-1935 to learn with Neurospora and using morestandard genetic genetics within the intellectual empire of H. T. MOR- approaches, were able to connect gene function with GAN. While there, EPHRUSSIarranged a collaboration the production of specific enzymes as codified in their with GEORGEBEADLE, who joined him in Paris in the “one-gene:one-enzyme” hypothesis. fall of 1935.They aimed at agenetic analysis of Yeast (and cytoplasmic) genetics:After World War development, with BEADLEat first contributing ge- 11, EPHRUSSI,having spent most ofthe war as a refugee netic expertise and EPHRUSSIthe insights and tech- scientist at JohnsHopkins University, returnedto niques of embryology. Their strategy was to subject a France to reinstitute research aimed at disentangling single species to both geneticand embryological attack. the various influences, nuclear and cytoplasmic, on Since such traditional embryological organisms as sea development. This time, EPHRUSSIeschewed the urchins and frogs are ill-suited for standard genetic transplantation of cells and tissues beiween organisms, analysis, EPHRUSSIand BEADLEdecided to apply ex- though he assigned his student PIOTR SLONIMSKIa perimental embryological techniques to a genetic or- thesis based on transplantation of sea urchin nuclei, ganism par excellence, Drosophilamelanogaster (Ho- an attempt that was unsuccessful (P. SLONIMSKI,per- ROWITZ 1990,1991). They were encouraged by STUR- sonal communication). Given the failure of these ef- TEVANT, who provided some leads from his work on forts, he explained his choice of a new experimental flies mosaic for the vermilion mutation (STURTEVANT organism as follows: 1920, 1932). This work suggested that a diffusible substance, present in the wild type, could compensate [Wlhat is needed is direct genetic analysis of somatic cells, for the assumed functional equivalence of irreversibly dif- for the absence of the wild-type product of thevermi- ferentiated somatic cells, however plausible, is only an hy- lion gene. pothesis. Crosses between such cells being impossible, only But could one do experimental embryology with nuclear transplantation from one somatic cell to another, or Drosophila? Drosophila larvae seemed to be too small grafting of fragments of cytoplasm, could provide the re- to permit use of the standardembryological technique quired information; such experiments however will have to of transplantation of parts of a developing embryoto await the developmentof adequate technicaldevices. In the learn about influences of location and of adjacent meantime, the closest approximation to the evidence we tissues on development. And difficulties in identifying would like to have is provided by the study of lower forms imaginal disks added furthercomplications. However, which propagate by vegetative reproductionand possess no isolated germ line (EPHRUSSI1953, p. 5; also in EPHRUSSI EPHRUSSI,aware of the implantation experiments of 1958, p. 37). CASPARI,KUHN,
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