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Brief Autobiography Related to Work on Inbred Mice

Margaret C. Green

The Jackson Laboratory
Bar Harbor, Maine

I became a mouse geneticist by marriage. Shortly before marrying Earl Green, I had received my Ph.D. for work on the genetics and radiation cytogenetics of the grasshopper Chorthippus longicornis. At the time there seemed to be little similarity between Chorthippus and Mus musculus, but I discovered many years later there was, after all, a connection. My Ph.D. advisor was Dr. W.R.B. Robertson, who had noted in a classical paper that the variation in chromosome number between related species of grasshoppers could be accounted for by fusion of two chromosomes with terminal centromeres to make a single chromosome with a median centromere. The species I worked with had three such metacentric chromosomes. These metacentric chromosomes later became known as Robertsonian translocations, and it is now well known that they are characteristic of certain wild subspecies of Mus musculus. They have also occurred in laboratory mice, as one of the most useful cytogenetic variants available in the mouse.

At the time we were married in 1940, Earl had a postdoctoral fellowship ($300 extra for being married) at the University of Chicago and I had a fresh Ph.D. but no other means of support. We decided that we could live on the fellowship, and that instead of my looking for a job we should join forces and work on Earl's fellowship project, the anatomy and development of short-eared ( se/se) mice ( 1, 2, 3). Since the microscope had been my principal research tool, I became responsible for the embryological and histological studies, a line of endeavor that continued with other mutant genes throughout my research career. This was the easy part of converting from grasshoppers to mice. Some other things were harder.

I was afraid of mice. In our research project, Earl was responsible, among other things, for the mouse husbandry, and he continued this activity after we moved to Ohio State University in 1941. But in 1943 he went into military service and I had no escape from the duty of handling mice. I well remember sweating out those ear-punching sessions, particularly with one strain in which the mice were hyperactive and also had short ears that were extremely hard to punch legibly. Fear of being bitten stayed with me for years. It finally disappeared on a memorable occasion after our move to The Jackson Laboratory in 1956. A mouse bit me while I was showing it to a room full of visitors in the auditorium. Fear of making a spectacle in front of the audience overcame fear of being bitten by the mouse, and instead of throwing the mouse across the room as I would have under private circumstances, I stood there calmly and let it bite. I was cured.

My work with mice has been mostly with mutant genes, and any contributions to the development of inbred strains has been incidental to the propagation and use of mutant genes. In our first work with the short-ear gene, we compared two different short-eared inbred strains with a different normal-eared inbred strain. We soon realized that this was not a proper procedure for determining the effects of the mutant gene, and set about producing several strains inbred by brother-sister matings with forced heterozygosis for short-ears. This procedure makes the mutant gene available for comparison with its normal allele uncontaminated by differences at other genetic loci. It also allows of selection for a genetic background compatible with viability and fertility of the mutant mice.

After we moved to The Jackson Laboratory, I became responsible for the Mouse Mutants Stock Center. Some of the stocks in the Center came from George Snell who had also been propagating some of them by inbreeding with forced heterozygosis. We continued the use of this procedure and extended it to many other stocks. We thus produced a number of new inbred strains, some of which have developed characteristics that make them useful for purpose other than propagation of the mutant for which they were originally bred. We used the same breeding system for maintenance of the linkage testing stocks containing multiple dominant genes. These stocks are now highly inbred and some of them have been typed for polymorphic biochemical markers, making them more useful for linkage tests since the additional loci extend the number of chromosomal regions that can be tested in a single linkage cross.

In the operation of our Mouse Mutants Stocks Center, I was lucky enough to become associated with Mrs. Priscilla W. Lane, known as "Skippy," whose enthusiasm and enterprise in developing new stocks and promoting their use have made her a major supplier of mutant mice for research around the world. In addition to all her other activities, Skippy has produced, every two years, a revised list (widely known as the "Lane List") of all the mutant stocks and stocks bearing chromosomal variants at The Jackson Laboratory. An important feature of this list is a section (11 pages in the 1976 list) listing all the congenic and segregating inbred strains at the Laboratory (except for the histocompatibility congenic strains which are listed elsewhere).

Many mutant genes are very deleterious, and it is often difficult to find an inbred background on which the mutant animals are fertile or can survive long enough to be useful for research. This is particularly troublesome for the case of dominant mutations in which the affected mice must be able to reproduce. We devised the procedure of crossing the mutant mice repeatedly to an F1 hybrid to maximize hybrid vigor. The resulting stocks are not genetically homogeneous, but they bear only the background genes of the two parental strains. Although they are about as variable as an F2 generation, their tissues can be transplanted into normal F1 hosts, a procedure that is often useful in studying gene function. This breeding system has greatly increased the ease of maintaining many difficult genes and chromosome variants, including the X/0 stock and several translocations, and has saved considerable time, space, and effort. It is now being used in several other laboratories. The F1 hybrids we have used are (C57BL/6 X CBA/Ca)F1 and (C57BL/6 X C3HeB/Fe)F1.

I began doing linkage studies in the late 1940s with a new mutation that occurred in our stocks at Ohio State University. When we moved to The Jackson Laboratory, I continued linkage tests with many of the unlocated genes in the stocks there. This was before gene mapping became popular and only a handful of mouse geneticists devoted much attention to linkage tests. It was a rather easy routine activity, and I enjoyed watching the loci fall into place on the map. Also, I thought the information was potentially useful, even for genes not intrinsically very interesting in themselves. Any "good" mutant gene, that is, any gene with good viability and fertility, could be a useful marker for studies of other more important loci located in the same vicinity. I always had the feeling that the evidence for the existence of a new locus was not complete until its location was known. Later when the mouse linkage map began to fill up and the advantages of knowing the location of important loci became more obvious, many others entered the field. There is plenty of work to be done, as many known genes are still unlocated, including many very interesting and important biochemical and immunological loci, and new loci are being discovered at an increasing rate.

Perhaps the most useful service I have performed for mouse geneticists has been to summarize linkage information in a linkage map. This effort began in 1958 in preparation for the Tenth International Congress of Genetics held that year in Montreal. Dr. Walter Heston had pointed out that, at the International congress in Cornell University in 1932, the most recent Genetics Congress in North America, the corn geneticists had constructed a living linkage map by planting mutant corn plants in the form of a map. He suggested that it was now time for a living linkage map of the mouse and that The Jackson Laboratory was the institution to do the job. Members of the staff threw themselves enthusiastically into the task. We designed and constructed a large map with 18 chromosomes made of vertically placed cardboard tubing, each about 4 inches in diameter and 5 feet long, and with small plastic cages holding the mutant mice appropriately arranged at intervals beside the chromosomes. The project was a great success.

To prepare the map I had to assemble all the available linkage data, and I devised a card file system for organizing and storing the information. After that, it was relatively easy to keep the file up to date and to revise the linkage map as often as enough new information accumulated. The version of the map used in the Live Linkage Map was published in the Journal of Heredity in 1959 ( 4). Revised versions have appeared in several editions of the Handbook of Biochemistry ( 9), the second edition of the Biology of the Laboratory Mouse in 1966 ( 6), the Handbook of Genetics in 1975 ( 8), several textbooks of genetics, in Mouse News Letter from 1972 through 1975, and in a number of other publications. Tables of the linkage data on which the map is based have appeared in several editions of the Biology Data book published by the Federation of American Societies of Experimental Biology ( 7). Perhaps the most useful form of the map was in the hundreds of Xerox copies distributed to the research staff at The Jackson laboratory, to visitors and students, and to participants in the short courses in medical and mammalian genetics and the workshops in biochemical genetics held at the Laboratory.

The making of linkage maps requires knowledge of methods of analyzing linkage data and of combining data from different sources. Having acquired some experience in these matters, in 1963 I contributed a chapter on methods of testing for linkage to Burdette's book on Methodology in Mammalian Genetics ( 5).

Prior to 1972 the linkage map was arranged in order of linkage groups numbered chronologically as they were discovered. A major change in the map occurred in 1972 after it became possible to identify all the chromosomes of the mouse individually by their distinctive banding patterns, and linkage groups had been located on 14 of the 20 chromosome pairs. As chairman of the Committee on Standardized Genetic Nomenclature for Mice, I arranged for adoption of a standard system for numbering the chromosomes in order of size. The Committee decided to recommend that chromosome numbers be used to replace the old linkage group numbers to bring the cytological and genetic terminology into a single system. The standard numbering system and the Committee's recommendations were published that year in the Journal of Heredity ( 10). The map is now arranged in order of chromosome number, and genes have been assigned to all chromosomes.

Construction of the linkage map has little bearing on the development of inbred strains, the subject of this workshop, but a good linkage map does increase the usefulness of inbred strains. With the recent explosive increase in the number of known biochemical and other polymorphic loci, knowledge of the location of these loci on the map makes the inbred strains more useful as linkage testing stocks. Strains that differ in the alleles they carry at a number of loci on different chromosomes become good linkage testing stocks for new variants that occur in the strains or for differences that are found between the strains. The increasingly complete linkage map will remain a handy tool for users of inbred strains.

REFERENCES

1. Green, E.L., and Green, M.C. (1942). J. Morphol. 70: 1.
See also MGI.

2. Green, M.C. (1951). J. Morphol. 88: 1.
See also MGI.

3. Green, M.C. (1968). J. Exp. Zool. 167: 129.
See also MGI.

4. Green, M.C., and Dickie, M.M. (1959). J. Hered. 10: 1.

5. Green, M.C. (1963). Methodology in Mammalian Genetics (W.J. Burdette, ed.), p. 56. Holden-Day, San Francisco.

6. Green, M.C. (1966). In Biology of the Laboratory Mouse (E.L. Green, ed.), p. 87. McGraw-Hill, New York.

7. Green, M.C. (1972). in "Biology Data Book," 2nd ed., Vol. 1 (P.L. Altman and D.S. Dittmer, eds.), p. 15. FASEB, Washington.

8. Green, M.C. (1975). In Handbook of Genetics, Vol. IV (R.C. King, ed.), p. 203. Plenum Press, New York.

9. Green, M.C. (1976). In Handbook of Biochemistry and Molecular Biology, 3rd ed., Nucleic Acids, Vol. II (G.D. Fasman, ed.), p. 856. Chemical Rubber Co., Cleveland.

10. Committee on Standardized Genetic Nomenclature for Mice, M.C. Green (Chm). (1972). J. Hered. 63: 69.
See also MGI.

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