Abstract
Analysis of hepatic nonhistone chromosomal protein (NHCP) expression in male mice from progenitor strains (C3H/HeN, C57BL/6N), their F1 hybrid (B6C3), and seven recombinant inbred strains (RIs) (B6N×C3N) by high-resolution two-dimensional polyacrylamide gel electrophoresis (2D-PAGE) detected 16 NHCPs whose expression in RIs could be correlated to each other and with strain distribution patterns (SDP) of 20 genetic markers differing in the progenitors. Of the 400+ NHCP spots detected in RI 2D-PAGE maps, 172 were common to progenitors and all RIs. There was a characteristic absence of five NHCPs in one RI, Y. Ten C3H-specific and six C57-specific NHCP inherited in B6C3 also appeared in RIs. The SDP of C3H-specific NHCP 2 matched the SDP of beta-glucuronidase on chromosome 5 and carbonic anhydrase on chromosome 3, and C57-specific NHCP 5 SDP corresponded to that for nonagouti trait on chromosome 2. These 16 NHCP genetic marker inheritance differences detected in RIs add to the 23 previously established genetic marker differences between the progenitors.
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Anderson, N. G., and Anderson, N. L. (1978). Analytical techniques for cell fractions. XXI. Two-dimensional analysis of serum and tissue proteins: Multiple isoelectric focusing.Anal. Biochem. 85331.
Anderson, N. L., and Anderson, N. G. (1978). Analytical techniques for cell fractions. XXII. Two-dimensional analysis of serum and tissue proteins: Multiple gradient-slab gel electrophoresis.Anal. Biochem. 85341.
Brown, D. D. (1984). The role of stable complexes that repress and activate eucaryotic genes.Cell 37359.
Chai, L. E., and Sandberg, A. A. (1982). In Padilla, G. M., and McCarty, K. S., Sr. (eds.),Genetic Expression in the Cell Cycle Academic Press, New York and London.
Daban, J. R., and Cantor, C. R. (1982). Role of histone pairs H2A, H2B and H3, H4 in the self assembly of nucleosome core particles.J. Mol. Biol. 156771.
Dunn, T. B. (1965). Spontaneous lesions of mice. In Ribelin, W. E. (ed.),Pathology of Laboratory Animals Charles C Thomas, Springfield, Ill.
Eicher, E. M., Taylor, B. A., Leighton, S. C., and Womack, J. E. (1980). A serum protein polymorphism determinant on chromosome 9 of Mus musculus.Mol. Gen. Genet. 177571.
Elliott, R. W. (1979). Use of two dimensional electrophoresis to identify and map mouse genes.Genetics 91295.
Emerson, B. M., Lewis, C. D., and Felsenfeld, G. (1985). Interaction of specific nuclear factors with the nuclease-hypersensitive region of the chicken adult beta-globin genes. Nature of the binding domain.Cell 4121.
Fox, T. D. (1976). Identification of phage SP01 proteins coded by regulatory genes 33 and 34.Nature 262748.
Giometti, C. S., Anderson, N. G., Tollaksen, S. L., Edwards, J. J., and Anderson, N. L. (1980). Analytical techniques for cell fractions. XXVII. Use of heart proteins as reference standards in two-dimensional electrophoresis.Anal. Biochem. 10247.
Gronow, M. (1983). Chemical carcinogenesis. In Hnilica, L. S. (ed.),Chromosomal Nonhistone Proteins, Vol. I CRC Press, Boca Raton, Fla., pp. 93–126.
Guevara, J., Jr., Johnson, D. A., Ramagli, L. S., Martin, B. A., Capetillo, S., and Rodriguez, L. V. (1982). Quantitative aspects of silver deposition in proteins resolved in complex polyacrylamide gels.Electrophoresis 3197.
Hoffman, H. A. (1984). Laboratory procedures. In Nomura, T., Esaki, K., and Tomita, T. (eds.),ICLAS Manual for Genetic Monitoring of Inbred Mice University of Tokyo Press, Tokyo, pp. 36–100.
Klose, J. (1975). Protein mapping by combined isoelectric focusing and electrophoresis of mouse tissue. A novel approach to testing for induced point mutations in mammals.Humangenetik 26231.
Klose, J. (1982). Genetic variability of soluble proteins studied by two-dimensional electrophoresis on different inbred mouse strains and on different mouse organs.J. Mol. Evol. 18315.
Klose, J., and Feller, M. (1981). Genetic variability of proteins from plasma membranes and cytosols of mouse organs.Biochem. Genet. 19859.
Klose, J., and von Wallenberg-Pachaly, H. (1976). Changes of soluble protein populations during organogenesis of mouse embryos as revealed by protein mapping.Dev. Biol. 51324.
Knudson, A. G., Jr. (1985). Hereditary cancer, oncogenes, and antioncogenes.Cancer Res. 451437.
Milman, G., Lee, E., Ghangas, G. S., McLaughlin, J., and George, M., Jr. (1976). Analysis of HeLa hypoxanthine phosphoribosyltransferase mutants and revertants by two-dimensional polyacrylamide gel electrophoresis: Evidence for silent gene action.Proc. Natl. Acad. Sci. USA 734589.
Miskimins, W. K., Roberts, M. P., McClelland, A., and Ruddle, F. H. (1985). Use of a protein-blotting procedure and a specific DNA probe to identify nuclear proteins that recognize the promoter region of the transferrin receptor gene.Proc. Natl. Acad. Sci. USA 826741.
Nagl, W. (1985). Chromatin organization and the control of gene activity.Int. Rev. Cytol. 9421.
O'Farrell, P. H. (1975). High resolution two-dimensional electrophoresis of proteins.J. Biol. Chem. 2504007.
O'Farrell, P. Z., Goodman, H. M., and O'Farrell, P. H. (1977). High resolution two-dimensional electrophoresis of basic as well as acidic proteins.Cell 121133.
Owen, F. L., Taylor, B. A., Zweidler, A., and Seidman, J. G. (1986). The murine gamma-chain of the T cell receptor is closely linked to a spermatocyte specific histone gene and the beige coat color locus on chromosome 13.J. Immunol. 1371044.
Paigen, K. (1979). Acid hydrolases as models of genetic control.Annu. Rev. Genet. 13417.
Paigen, K., Swank, R. T., Tomino, S., and Ganschow, R. E. (1975). The molecular genetics of mammalian glucuronidase.J. Cell Phys. 85379.
Pederson, T. (1974). Gene activation in eukaryotes: Are nuclear acidic proteins the cause of the effect?Proc. Natl. Acad. Sci. USA 71617.
Racine, R. R., and Langley C. H. (1980). Genetic analysis of variations protein in Mus musculus using two-dimensional electrophoresis.Biochem. Genet. 18185.
Ramagli, L. S., and Rodriguez, L. V. (1985). Quantitation of microgram amounts of protein in two-dimensional polyacrylamide gel electrophoresis sample buffer.Electrophoresis 6559.
Ramagli, L. S., Capetillo, S., Becker, F. F., and Rodriguez, L. V. (1985). Alterations in nonhistone chromatin proteins during hepatocarcinogenesis induced by diverse acting carcinogens.Carcinogenesis 6367.
Rodriguez, L. V., Ramagli, L. S., and Johnston, D. A. (1985). Analysis of normal and neoplastic tissue NHCP by high-resolution two-dimensional gradient electrophoresis and silver staining. In Bekhor, I., Liew, C. C., and Mirell, C. J. (eds.),Recent Advances in Nonhistone Chromosomal Protein Research CRC Press, Boca Raton, Fla., pp. 165–192.
Schlissel, M. S., and Brown, D. D. (1984). The transcriptional regulation of Xenopus 5S RNA genes in chromatin: The roles of active stable transcription complexes and histone H1.Cell 37903.
Staats, J. (1985). Standardized nomenclature for inbred strains of mice: Eighth listing.Cancer Res. 45945.
Stein, G. S., Plumb, M., Stein, J. L., Phillips, I. R., and Shephard, E. A. (1983). Nonhistone proteins in genetic regulation. In Hnilica, L. S. (ed.),Chromosomal Nonhistone Proteins, Vol. I CRC Press, Boca Raton, Fla., pp. 127–186.
Steinberg, R. A., O'Farrell, P. H., Friedrich, U., and Coffino, P. (1977). Mutations causing charge alterations in regulatory subunits of the cAMP-dependent protein kinase of cultured SH9 lymphoma cells.Cell 10381.
Taylor, B. A. (1972). Genetic relationships between inbred strains of mice.J. Hered. 6383.
Taylor, B. A. (1981). Recombinant inbred strains. In Green, M. C. (ed.),Genetic Variants and Strains of the Laboratory Mouse Gustar Fischer Verlag, Stuttgart, pp. 397–407.
Tulchin, N., and Taylor, B. A. (1981). Gamma-glutamyl cyclotransferase: A new genetic polymorphism in the mouse Mus musculus linked to Lyt-2.Genetics 99109.
Womack, J. E., Lynes, M. A., and Taylor, B. A. (1975). Genetic variation of an intestinal Leucine arylaminopeptidase (Lap-1) in the mouse and its location on chromosome 9.Biochem. Genet. 13511.
Zannis, V. I., and Martin, D. W., Jr. (1979). Use of 2-dimensional gel-electrophoresis for detection of post translational protein modification and in the study of genetic protein variants—Investigations of purine nucleoside phosphorylase and hypoxanthine-guanine phosphoribosyl transferase. In Catsimpoolas, N. (ed.),Electrophoresis '78: Developments in Biochemistry, Vol. 2 Elsevier/North Holland, Amsterdam, pp. 305–322.
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This study was supported in part by funds from NIH Grants CA 33305 and CA 16672 and Exxon Corporation, USA.
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Ramagli, L.S., Womack, J.E. & Rodriguez, L.V. Genetic analysis of nonhistone chromosomal protein inheritance in recombinant inbred mouse strains using two-dimensional electrophoresis. Biochem Genet 28, 123–136 (1990). https://doi.org/10.1007/BF00561332
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DOI: https://doi.org/10.1007/BF00561332