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. 1988 Aug;8(8):3168–3174. doi: 10.1128/mcb.8.8.3168

Structure and expression of B-myc, a new member of the myc gene family.

S Ingvarsson 1, C Asker 1, H Axelson 1, G Klein 1, J Sümegi 1
PMCID: PMC363545  PMID: 2850482

Abstract

The myc family of genes contains five functional members. We describe the cloning of a new member of the myc family from rat genomic and cDNA libraries, designated B-myc. A fragment of cloned B-myc was used to map the corresponding rat locus by Southern blotting of DNA prepared from rat X mouse somatic cell hybrids. B-myc mapped to rat chromosome 3. We have previously mapped the c-myc to rat chromosome 7 (J. Sümegi, J. Spira, H. Bazin, J. Szpirer, G. Levan, and G. Klein, Nature [London] 306:497-498, 1983) and N-myc and L-myc to rat chromosomes 6 and 5, respectively (S. Ingvarsson, C. Asker, Z. Wirschubsky, J. Szpirer, G. Levan, G. Klein, and J. Sümegi, Somat. Cell Mol. Genet. 13:335-339, 1987). A partial sequence of B-myc had extensive sequence homology to the c-myc protein-coding region, and the detection of intron homology further indicated that these two genes are closely related. The DNA regions conserved among the myc family members, designated myc boxes, were highly conserved between c-myc and B-myc. A lower degree of homology was detected in other parts of the coding region in c-myc and B-myc not present in N-myc and L-myc. A 1.3-kilobase B-myc-specific mRNA was detected in most rat tissues, with the highest expression in the brain. This resembled the expression pattern of c-myc, although at different relative levels, and was in contrast to the more tissue-specific expression of N-myc and L-myc. B-myc was expressed at uniformly high levels in all fetal tissues and during subsequent postnatal development, in contrast to the stage-specific expression of c-myc.

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  1. Akhurst R. J., Calzone F. J., Lee J. J., Britten R. J., Davidson E. H. Structure and organization of the CyIII actin gene subfamily of the sea urchin, Strongylocentrotus purpuratus. J Mol Biol. 1987 Mar 20;194(2):193–203. doi: 10.1016/0022-2836(87)90368-8. [DOI] [PubMed] [Google Scholar]
  2. Bernard O., Cory S., Gerondakis S., Webb E., Adams J. M. Sequence of the murine and human cellular myc oncogenes and two modes of myc transcription resulting from chromosome translocation in B lymphoid tumours. EMBO J. 1983;2(12):2375–2383. doi: 10.1002/j.1460-2075.1983.tb01749.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Dalla-Favera R., Wong-Staal F., Gallo R. C. Onc gene amplification in promyelocytic leukaemia cell line HL-60 and primary leukaemic cells of the same patient. Nature. 1982 Sep 2;299(5878):61–63. doi: 10.1038/299061a0. [DOI] [PubMed] [Google Scholar]
  4. DePinho R. A., Legouy E., Feldman L. B., Kohl N. E., Yancopoulos G. D., Alt F. W. Structure and expression of the murine N-myc gene. Proc Natl Acad Sci U S A. 1986 Mar;83(6):1827–1831. doi: 10.1073/pnas.83.6.1827. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. DePinho R., Mitsock L., Hatton K., Ferrier P., Zimmerman K., Legouy E., Tesfaye A., Collum R., Yancopoulos G., Nisen P. Myc family of cellular oncogenes. J Cell Biochem. 1987 Apr;33(4):257–266. doi: 10.1002/jcb.240330404. [DOI] [PubMed] [Google Scholar]
  6. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Feinberg A. P., Vogelstein B. "A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity". Addendum. Anal Biochem. 1984 Feb;137(1):266–267. doi: 10.1016/0003-2697(84)90381-6. [DOI] [PubMed] [Google Scholar]
  8. Glisin V., Crkvenjakov R., Byus C. Ribonucleic acid isolated by cesium chloride centrifugation. Biochemistry. 1974 Jun 4;13(12):2633–2637. doi: 10.1021/bi00709a025. [DOI] [PubMed] [Google Scholar]
  9. Hayashi K., Makino R., Kawamura H., Arisawa A., Yoneda K. Characterization of rat c-myc and adjacent regions. Nucleic Acids Res. 1987 Aug 25;15(16):6419–6436. doi: 10.1093/nar/15.16.6419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hayward W. S., Neel B. G., Astrin S. M. Activation of a cellular onc gene by promoter insertion in ALV-induced lymphoid leukosis. Nature. 1981 Apr 9;290(5806):475–480. doi: 10.1038/290475a0. [DOI] [PubMed] [Google Scholar]
  11. Ingvarsson S., Asker C., Wirschubsky Z., Szpirer J., Levan G., Klein G., Sümegi J. Mapping of Lmyc and Nmyc to rat chromosomes 5 and 6. Somat Cell Mol Genet. 1987 Jul;13(4):335–339. doi: 10.1007/BF01534927. [DOI] [PubMed] [Google Scholar]
  12. Kohl N. E., Legouy E., DePinho R. A., Nisen P. D., Smith R. K., Gee C. E., Alt F. W. Human N-myc is closely related in organization and nucleotide sequence to c-myc. Nature. 1986 Jan 2;319(6048):73–77. doi: 10.1038/319073a0. [DOI] [PubMed] [Google Scholar]
  13. Kozak M. Bifunctional messenger RNAs in eukaryotes. Cell. 1986 Nov 21;47(4):481–483. doi: 10.1016/0092-8674(86)90609-4. [DOI] [PubMed] [Google Scholar]
  14. Legouy E., DePinho R., Zimmerman K., Collum R., Yancopoulos G., Mitsock L., Kriz R., Alt F. W. Structure and expression of the murine L-myc gene. EMBO J. 1987 Nov;6(11):3359–3366. doi: 10.1002/j.1460-2075.1987.tb02657.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Little C. D., Nau M. M., Carney D. N., Gazdar A. F., Minna J. D. Amplification and expression of the c-myc oncogene in human lung cancer cell lines. Nature. 1983 Nov 10;306(5939):194–196. doi: 10.1038/306194a0. [DOI] [PubMed] [Google Scholar]
  16. Mitani K., Kurosawa H., Suzuki A., Hayashi Y., Hanada R., Yamamoto K., Komatsu A., Kobayashi N., Nakagome Y., Yamada M. Amplification of N-myc in a rhabdomyosarcoma. Jpn J Cancer Res. 1986 Nov;77(11):1062–1065. [PubMed] [Google Scholar]
  17. Nau M. M., Brooks B. J., Battey J., Sausville E., Gazdar A. F., Kirsch I. R., McBride O. W., Bertness V., Hollis G. F., Minna J. D. L-myc, a new myc-related gene amplified and expressed in human small cell lung cancer. Nature. 1985 Nov 7;318(6041):69–73. doi: 10.1038/318069a0. [DOI] [PubMed] [Google Scholar]
  18. Nesbitt M. N. Evolutionary relationships between rat and mouse chromosomes. Chromosoma. 1974 Jun 11;46(2):217–224. doi: 10.1007/BF00332519. [DOI] [PubMed] [Google Scholar]
  19. Nisen P. D., Zimmerman K. A., Cotter S. V., Gilbert F., Alt F. W. Enhanced expression of the N-myc gene in Wilms' tumors. Cancer Res. 1986 Dec;46(12 Pt 1):6217–6222. [PubMed] [Google Scholar]
  20. Norrander J., Kempe T., Messing J. Construction of improved M13 vectors using oligodeoxynucleotide-directed mutagenesis. Gene. 1983 Dec;26(1):101–106. doi: 10.1016/0378-1119(83)90040-9. [DOI] [PubMed] [Google Scholar]
  21. Ralston R., Bishop J. M. The protein products of the myc and myb oncogenes and adenovirus E1a are structurally related. Nature. 1983 Dec 22;306(5945):803–806. doi: 10.1038/306803a0. [DOI] [PubMed] [Google Scholar]
  22. Ramsay G., Stanton L., Schwab M., Bishop J. M. Human proto-oncogene N-myc encodes nuclear proteins that bind DNA. Mol Cell Biol. 1986 Dec;6(12):4450–4457. doi: 10.1128/mcb.6.12.4450. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Rigby P. W., Dieckmann M., Rhodes C., Berg P. Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I. J Mol Biol. 1977 Jun 15;113(1):237–251. doi: 10.1016/0022-2836(77)90052-3. [DOI] [PubMed] [Google Scholar]
  24. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Sargent T. D., Wu J. R., Sala-Trepat J. M., Wallace R. B., Reyes A. A., Bonner J. The rat serum albumin gene: analysis of cloned sequences. Proc Natl Acad Sci U S A. 1979 Jul;76(7):3256–3260. doi: 10.1073/pnas.76.7.3256. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Sarid J., Halazonetis T. D., Murphy W., Leder P. Evolutionarily conserved regions of the human c-myc protein can be uncoupled from transforming activity. Proc Natl Acad Sci U S A. 1987 Jan;84(1):170–173. doi: 10.1073/pnas.84.1.170. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Schwab M., Ramsay G., Alitalo K., Varmus H. E., Bishop J. M., Martinsson T., Levan G., Levan A. Amplification and enhanced expression of the c-myc oncogene in mouse SEWA tumour cells. Nature. 1985 May 23;315(6017):345–347. doi: 10.1038/315345a0. [DOI] [PubMed] [Google Scholar]
  28. Seeger R. C., Brodeur G. M., Sather H., Dalton A., Siegel S. E., Wong K. Y., Hammond D. Association of multiple copies of the N-myc oncogene with rapid progression of neuroblastomas. N Engl J Med. 1985 Oct 31;313(18):1111–1116. doi: 10.1056/NEJM198510313131802. [DOI] [PubMed] [Google Scholar]
  29. Sejersen T., Rahm M., Szabo G., Ingvarsson S., Sümegi J. Similarities and differences in the regulation of N-myc and c-myc genes in murine embryonal carcinoma cells. Exp Cell Res. 1987 Oct;172(2):304–317. doi: 10.1016/0014-4827(87)90389-2. [DOI] [PubMed] [Google Scholar]
  30. Showe L. C., Ballantine M., Nishikura K., Erikson J., Kaji H., Croce C. M. Cloning and sequencing of a c-myc oncogene in a Burkitt's lymphoma cell line that is translocated to a germ line alpha switch region. Mol Cell Biol. 1985 Mar;5(3):501–509. doi: 10.1128/mcb.5.3.501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Slamon D. J., Boone T. C., Seeger R. C., Keith D. E., Chazin V., Lee H. C., Souza L. M. Identification and characterization of the protein encoded by the human N-myc oncogene. Science. 1986 May 9;232(4751):768–772. doi: 10.1126/science.3008339. [DOI] [PubMed] [Google Scholar]
  32. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  33. Staden R. A new computer method for the storage and manipulation of DNA gel reading data. Nucleic Acids Res. 1980 Aug 25;8(16):3673–3694. doi: 10.1093/nar/8.16.3673. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Stanton L. W., Schwab M., Bishop J. M. Nucleotide sequence of the human N-myc gene. Proc Natl Acad Sci U S A. 1986 Mar;83(6):1772–1776. doi: 10.1073/pnas.83.6.1772. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Stanton L. W., Watt R., Marcu K. B. Translocation, breakage and truncated transcripts of c-myc oncogene in murine plasmacytomas. Nature. 1983 Jun 2;303(5916):401–406. doi: 10.1038/303401a0. [DOI] [PubMed] [Google Scholar]
  36. Stone J., de Lange T., Ramsay G., Jakobovits E., Bishop J. M., Varmus H., Lee W. Definition of regions in human c-myc that are involved in transformation and nuclear localization. Mol Cell Biol. 1987 May;7(5):1697–1709. doi: 10.1128/mcb.7.5.1697. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Szpirer J., Levan G., Thörn M., Szpirer C. Gene mapping in the rat by mouse-rat somatic cell hybridization: synteny of the albumin and alpha-fetoprotein genes and assignment to chromosome 14. Cytogenet Cell Genet. 1984;38(2):142–149. doi: 10.1159/000132047. [DOI] [PubMed] [Google Scholar]
  38. Sümegi J., Hedberg T., Björkholm M., Godal T., Mellstedt H., Nilsson M. G., Perlman C., Klein G. Amplification of the c-myc oncogene in human plasma-cell leukemia. Int J Cancer. 1985 Sep 15;36(3):367–371. [PubMed] [Google Scholar]
  39. Sümegi J., Spira J., Bazin H., Szpirer J., Levan G., Klein G. Rat c-myc oncogene is located on chromosome 7 and rearranges in immunocytomas with t(6:7) chromosomal translocation. Nature. 1983 Dec 1;306(5942):497–498. doi: 10.1038/306497a0. [DOI] [PubMed] [Google Scholar]
  40. Taya Y., Mizusawa S., Nishimura S. Nucleotide sequence of the coding region of the mouse N-myc gene. EMBO J. 1986 Jun;5(6):1215–1219. doi: 10.1002/j.1460-2075.1986.tb04349.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Tso J. Y., Sun X. H., Kao T. H., Reece K. S., Wu R. Isolation and characterization of rat and human glyceraldehyde-3-phosphate dehydrogenase cDNAs: genomic complexity and molecular evolution of the gene. Nucleic Acids Res. 1985 Apr 11;13(7):2485–2502. doi: 10.1093/nar/13.7.2485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Yoshida M. C. Rat gene mapping by rat-mouse somatic cell hybridization and a comparative Q-banding analysis between rat and mouse chromosomes. Cytogenet Cell Genet. 1978;22(1-6):606–609. doi: 10.1159/000131034. [DOI] [PubMed] [Google Scholar]
  43. Zimmerman K. A., Yancopoulos G. D., Collum R. G., Smith R. K., Kohl N. E., Denis K. A., Nau M. M., Witte O. N., Toran-Allerand D., Gee C. E. Differential expression of myc family genes during murine development. 1986 Feb 27-Mar 5Nature. 319(6056):780–783. doi: 10.1038/319780a0. [DOI] [PubMed] [Google Scholar]

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