Skip to main content
Log in

Isozymes as bioprobes for genetic analysis of nonhuman primates

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

The identification and the utilization of genetically determined electrophoretic differences of enzymes between the individuals of species as well as between cell lines have played an important role in the advancement of mammalian genetics during the past quarter of a century. In an explicit search we found a number of red cell enzyme polymorphisms in each of the following four species: chimpanzees, orang utans, rhesus monkeys and brown capuchins. Allelic distribution patterns among populations have indicated trends of subspeciation among chimpanzees and orang utans due to geographic barriers leading to reproductive isolation. Investigations of quantitative levels of red cell glucose-6-phosphate dehydrogenase have suggested that relative activity profiles of certain enzymes among species may be helpful in studies of the evolution of physiological traits and their biological significance during speciation. A large number of biochemical genetic markers in primate-rodent (i.e., chimpanzee-, gorilla-, orang utan-, rhesus monkey- and African green monkey-Chinese hamster) somatic cell hybrids have been identified and are useful for primate genetic analysis. Some of the biologically relevant observations on the enzyme markers in the above mentioned primate species are discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Alepa, F. P., 1968. Antigenic factors characteristic of human immunoglobulin G, detected in the sera of non-human primates. Primates Med. 1: 1–9.

    Google Scholar 

  • Barnicot, N. A. & Cohen, P., 1970. Red cell enzymes of primates (Anthropoidea). Biochem. Genet. 4: 41–57.

    Google Scholar 

  • Beutler, E., 1983. Glucose-6-phosphate dehydrogenase deficiency. In: Stanbury, J. B., Wyngaarden, J. B., Fredrickson, D. S., Goldstein, J. L., Brown, M. S. (eds.). The Metabolic Basis of Inherited Disease, 5th Edition. McGraw-Hill, New York, pp. 1629–1653.

    Google Scholar 

  • Beutler, E. & West, C., 1978. Glucose-6-phosphate dehydrogenase variants in the chimpanzee. Biochem. Med. 20: 364–370.

    Google Scholar 

  • Bienzle, U., Ayeni, O., Lucas, A. O. & Luzzatto, L., 1972. Glucose-6-phosphate dehydrogenase and malaria. Lancet I: 107–110.

    Google Scholar 

  • Boone, C. M. & Ruddle, F. H., 1969. Interspecific hybridization between human and mouse somatic cells: enzyme and linkage studies. Biochem. Genet. 3: 119–136.

    Google Scholar 

  • Brewer, G. J., 1970. Present applications and the future of isozymology. In: An Introduction to Isozyme Techniques. Academic Press, New York, pp. 138–157.

    Google Scholar 

  • Bruce, E. J. & Ayala, F. J., 1979. Phylogenetic relationships between man and the apes: electrophoretic evidence. Evolution 33: 1040–1056.

    Google Scholar 

  • Ceppellini, R., Siniscalco, M. & Smith, C. A.B., 1955. The estimation of gene frequencies in a random mating population. Ann. hum. Genet. 20: 97–115.

    Google Scholar 

  • De Boer, L. E. M. & Meera Khan, P., 1982. Haemoglobin polymorphisms in Bornean and Sumatran orang utans. In: De Boer, L. E. M. (ed.). The Orang Utan. Its Biology and Conservation. (Perspectives in Vertebrate Science, Vol. 2). Dr W. Junk Publishers, The Hague, pp. 125–134.

    Google Scholar 

  • De Boer, L. E. M. & Seuánez, H. N., 1982. The chromosomes of the orang utan and their relevance to the conservation of the species. In: De Boer, L. E. M. (ed.). The Orang Utan. Its Biology and Conservation. (Perspectives in Vertebrate Science, Vol. 2). Dr W. Junk Publishers, The Hague, pp. 135–170.

    Google Scholar 

  • De Grauchy, J., 1987. Chromosome phylogenies of man, great apes, and old world monkeys. Genetica, this issue.

  • Estop, A. M., Garver, J. J., Egozcue, J., Meera Khan, P. & Pearson, P. L., 1983. Complex chromosome homologies between the rhesus monkey (Macaca mulatta) and man. Cytogenet. cell Genet. 35: 46–50.

    Google Scholar 

  • Estop, A. M., Garver, J. J., Pearson, P. L., Dijksman, T. M., Wijnen, L. M. M. & Meera Khan, P., 1978. Gene assignments to the presumptive homologs of human chromosomes 3, 4, 5, 7, 8, 10, 18, 19, 20 and 21 in the Pongidae and Cercopithecoidea. Cytogenet. cell Genet. 22: 558–563.

    Google Scholar 

  • Garver, J. J., Estop, A. M., Meera Khan, P., Balner, H. & Pearson, P. L., 1980. Evidence of similar organization of the chromosomes carrying the major histocompatibility complex in man and other primates. Cytogenet. cell Genet. 27: 238–245.

    Google Scholar 

  • Garver, J. J., Pearson, P. L., Estop, A. Dijksman, T. M., Wijnen, L. M. M., Westerveld, A. & Meera Khan, P., 1978. Gene assignments to the presumptive homologs of human chromosomes 1, 6, 11, 12 and X in the Pongidae and Cercopithecoidea. Cytogenet. cell Genet. 22: 564–569.

    Google Scholar 

  • Giblett, E. R., 1969. Genetic Markers in Human Blood. Blackwell, Oxford, pp. 557–575 & 600–601.

    Google Scholar 

  • Giblett, E. R., 1977. Genetic polymorphisms in human blood. A. Rev. Genet. 11: 13–28.

    Google Scholar 

  • Goodman, M. & Poulik, M. D., 1968. Genetic Variations and Properties of Protein Macromolecules of Chimpanzees. ARLTR-68–3, 6571st Aeromedical Research Laboratory, Aerospace Medical Division, Holloman Air Force Base, New Mexico.

    Google Scholar 

  • Goodman, M. & Tashian, R. E., 1969. A geographic variation in the serum transferrin and red cell phosphoglucomutase polymorphisms of chimpanzees. Hum. Biol. 41: 237–249.

    Google Scholar 

  • Goodman, S. I., Solomons, C. C., Muschenheim, F., McIntyre, C. A., Miles, B. & O'Brien, D., 1968. A syndrome resembling lathyrism associated with iminodipetiduria. Am. J. Med. 45: 152–159.

    Google Scholar 

  • Harris, H., 1980. The Principles of Human Biochemical Genetics, 3rd, rev. edition. Elsevier/North-Holland Biomedical Press, Amsterdam.

    Google Scholar 

  • Harris, H. & Hopkins, D. A., 1976 (Supplements 1977 & 1978). Handbook of Enzyme Electrophoresis in Human Genetics. North-Holland Publishing Company, Amsterdam.

    Google Scholar 

  • Hopkinson, D. A., Edwards, Y. H. & Harris, H., 1976. The distributions of subunit numbers and subunit sizes of enzymers: a study of the products of 100 human loci. Ann. hum. Genet. 39: 383–411.

    Google Scholar 

  • Hopkinson, D. A. & Harris, H., 1971. Recent work on isozymes in man. A. Rev. Genet. 5: 5–32.

    Google Scholar 

  • Hunter, R. L. & Markert, C. L., 1957. Histochemical demonstration of enzymes separated by zone electrophoresis in starch gels. Science 125: 1294–1295.

    Google Scholar 

  • Kawamoto, Y. & Ischak, Th. M., 1981. Genetic differentiation of the Indonesian crab-eating macaque (Macaca fascicularis): I. Preliminary report on blood protein polymorphism. Primates 22: 237–252.

    Google Scholar 

  • Koenigswald, G. H. R. von, 1982. Distribution and evolution of the orang utan, Pongo pygmaeus (Hoppius). In: De Boer, L. E. M. (ed.), The Orang Utan. Its Biology and Conservation. (Perspectives in Vertebrate Science, Vol. 2). Dr W. Junk Publishers, The Hague, pp. 1–15.

    Google Scholar 

  • Lalley, P. A., 1987. Comparative gene mapping in nonhuman primates: identification of chromosomal homologies with man. (Abstract.) Genetica, this issue.

  • Lalley, P. A. & McKusick, V. A., 1985. Report of the committee on comparative mapping. Cytogenet. cell Genet. 40: 536–566.

    Google Scholar 

  • Leeuwen, A. van, Van der Does, J. A., D'Amare, J., Van der Steen, G., Van Loghem, E., Meera Khan, P., Van Rood, J. J. & Balner, H., 1972. Study of the HL-A System in a colony of chimpanzees. Histocompatibility Testing 1972. 49–53.

    Google Scholar 

  • Lewis, W. H. P., 1973. Common polymorphism of peptidase A: Electrophoretic variants associated with quantitative variation of red cell levels. Ann. hum. Genet. 36: 267–271.

    Google Scholar 

  • Los, W. R. T. & Meera Khan, P., 1977. Red cell NADH-diaphorase polymorphism in macaca mulatta. J. hum. Evol. 6: 227–230.

    Google Scholar 

  • McAlpine, P. J., Shows, T. B., Miller, R. L. & Pakstis, A. J., 1985. The catalog of mapped genes and report of the nomenclature committee. Cytogenet. cell Genet. 40: 8–66.

    Google Scholar 

  • Markert, C. L. (ed.), (1975). Isozymes, Vols. 1–4. Academic Press, New York.

    Google Scholar 

  • Markert, C. L. & Møller, F., 1959. Multiple forms of enzymes: tissue ontogenetic, and species specific patterns. Proc. natn. Acad. Sci., U.S.A. 45: 753–763.

    Google Scholar 

  • Meera Khan, P., 1971. Enzyme electrophoresis on cellulose acetate gel: zymogram patterns in man-mouse and man-Chinese hamster somatic cell hybrids. Arch Biochem. Biophys. 145: 470–483.

    Google Scholar 

  • Meera Khan, P., 1986. Red cell G6PD, PGD, GPX1, LDH, PGP and DIA2 polymorphisms. In: Cavalli-Sforza, L. L. (ed.). African Pygmies. Academic Press Inc., New York, pp. 273–290.

    Google Scholar 

  • Meera Khan, P. & Balner, H., 1972. Polymorphic enzymes in rhesus monkeys and chimpanzees. In: Goldsmith, E. I. & Moor-Jankowski, J. (eds.). Medical Primatology 1972, Part I: General Primatology, Reproduction and Perinatal Studies, Genetics, Phylogenetics and Evolution; Selected Papers from the Third Conference on Experimental Medicine and Surgery in Primates, Lyon, 1972. S. Karger, Basel, pp. 363–371.

    Google Scholar 

  • Meera Khan, P., Rijken, H., Wijnen, J. Th., Wijnen, L. M. M. & De Boer, L. E. M., 1982. Red cell enzyme variation in the orang utan: electrophoretic characterization of 45 enzyme systems in Cellogel. In: De Boor, L. E. M. (ed.). The Orang Utan. Its Biology and Conservation. (Perspectives in Vertebrate Science, Vol. 2). Dr. W. Junk Publishers, The Hague, pp. 61–108.

    Google Scholar 

  • Meera Khan, Van Someren, H., De Jong, W. W. & Vervloet, M., 1972. Red cell enzyme polymorphisms in rhesus monkeys and chimpanzees. Transplantn Proc. 4: 137–140.

    Google Scholar 

  • Meera Khan, P., Wijnen, J. Th., Hagenbeek, A. & Vossen, J. M., 1987. Isozymes as host-donor blood cell “tracers’ in bone marrow transplantation. Isozymes Curr. Top. Biol. med. Res. (in press).

  • Moor-Jankowski, J., Wiener, A. S., Kratochvil, C. H. & Fineg, J., 1966. Seroprimatology of chimpanzees: blood-group distribution as a “racial” characteristic. Science 152: 219–220.

    Google Scholar 

  • Ober, C., Olivier, T. J. & Buettner-Janusch, J., 1980. Genetic aspects of migration in a rhesus monkey population. J. hum. Evol. 9: 197–203.

    Google Scholar 

  • O'Brien, S. J. (ed.), Genetic Maps 1984. (Genetic Maps, Vol. 3). Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y., 1984.

    Google Scholar 

  • Ohno, S., 1970. Evolution by Gene Duplication. Springer-Verlag, Berlin.

    Google Scholar 

  • Pauling, L., Itano, H. A., Singer, S. J. & Wells, I. C., 1949. Sickle cell anemia, a molecular disease. Science 110: 543–548.

    Google Scholar 

  • Pearson, P. L., Garver, J. J., Estop, A., Dijksman, T. M., Wijnen, L. M. M. & Meera Khan, P., 1978. Gene assignments to the presumptive homologs of human chromosomes 2, 9, 13, 14 and 15 in the Pongidae and Cercopithecoidea. Cytogenet. cell Genet. 22: 588–593.

    Google Scholar 

  • Povey, S., Corney, G., Lewis, W. H. P., Robson, E. B., Parrington, J. M. & Harris, H., 1972. The genetics of peptidase C in man. Ann. hum. Genet. 35: 455–465.

    Google Scholar 

  • Powell, J. R., 1975. Protein variation in natural populations of animals. In: Dobzhansky, Th., Hecht, M. & Steere, W. C. (eds.), Evolutionary Biology. Vol. 8. Plenum Press, New York.

    Google Scholar 

  • Rattazzi, M. C., Scandalios, J. G. & Whitt, G. S., (eds.). International Congress on Isozymes, 4 th, Austin, Texas, 1982, Proceedings (Isozymes: Current Topies in Biological and Medical Research, Vols. 7–11). Alan R. Liss, Inc., New York, 1983.

    Google Scholar 

  • Rijksen, H. D., 1978. A Field Study on Sumatran Orang Utans (Pongo pygmaeus abelii Lesson 1827): Ecology, Behaviour and conservation. Mededel. Landbouwhogeschool Wageningen, 78–2: 1–420.

    Google Scholar 

  • Santachiara-Benerecetti, S. A., 1970. Studies on African pygmies. III. Peptidase C polymorphism in Babinga pygmies: A frequent erythrocytic enzyme deficiency. Am. J. hum. Genet. 22: 228–231.

    Google Scholar 

  • Selenka, E., 1898. Menschenaffen: Rassen, Schädel und Bezahnung des Orang-utan. Kriedel, Wiesbaden.

    Google Scholar 

  • Shows, T. B., Alper, C. A., Bootsma, D., Dorf, M., Douglas, T., Huisman, T., Kit, S., Klinger, H. P., Kozak, C., Lalley, P. A., Lindsley, D., McAlpine, P. I., McDougall, J. K., Meera Khan, P., Meisler, M., Morton, N. E., Opitz, J. M., Partridge, C. W., Payne, R., Roderick, T. H., Rubinstein, P., Ruddle, F. H., Shaw, M., Spranger, J. W. & Weiss, K., 1979. International System of Human Gene Nomenclature (1979) ISGN C1979). Cytogenet. cell Genet. 25: 96–116.

    Google Scholar 

  • Smith, D. G., 1980. Paternity exclusion in six captive groups of rhesus monkeys (Macaca mulatta). Am. J. phys. Anthrop. 53: 243–249.

    Google Scholar 

  • Smithies, O., 1955. Zone electrophoresis in starch gels: group variations in the serum proteins of normal human adults. Biochem. J. 61: 629–641.

    Google Scholar 

  • Spector, E. B., Rice, S. C. H., Kern, R. M., Hendrickson, R. & Cederbaum, S. D., 1985. Comparison of arginase activity in red blood cells of lower mammals, primates and man: Evolution to high activity in primates Am. J. hum. Genet. 37: 1138–1145.

    Google Scholar 

  • Van Someren, H., Beijersbergen van Henegouwen, H., Los, W. T., Wurzer-Figurelli, E., Doppert, B., Vervloet, M. & Meera Khan, P., 1974. Enzyme electrophoresis on cellulose acetate gel. II. Zymogram patterns in man-Chinese haster somatic cell hybrids. Humangenetik 25: 189–201.

    Google Scholar 

  • Wijnen, J. Th., Rijken, H., De Boer, L. E. M. & Meera Khan, P., 1982. Glucose-6-phosphate dehydrogenase (G6PD) variation in the orang utan. In: De Boer, L. E. M. (ed.), The Orang Utan. Its Biology and Conservation. (Perspective in Vertebrate Science, Vol. 2). Dr W. Junk Publishers, The Hague, pp. 109–118.

    Google Scholar 

  • Yoshida, A., 1970. Amino acid substitution (histidine to tyrosine) in a glucose-6-phosphate dehydrogenase variant (G6PD Hektoen) associated with over-production. J. Mol. Biol. 52: 483–490.

    Google Scholar 

  • Zouros, E., 1976. Hybrid molecules and the superiority of the heterozygote. Nature 262: 227–229.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Meera Khan, P. Isozymes as bioprobes for genetic analysis of nonhuman primates. Genetica 73, 25–36 (1987). https://doi.org/10.1007/BF00057435

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00057435

Keywords

Navigation