Skip to main content
PMC home page
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1988 Jul;8(7):2925–2932. doi: 10.1128/mcb.8.7.2925

Identification and sequence analysis of a new member of the mouse HSP70 gene family and characterization of its unique cellular and developmental pattern of expression in the male germ line.

Z F Zakeri 1, D J Wolgemuth 1, C R Hunt 1
PMCID: PMC363512  PMID: 3405224

Abstract

A unique member of the mouse HSP70 gene family has been isolated and characterized with respect to its DNA sequence organization and expression. The gene contains extensive similarity to a heat shock-inducible HSP70 gene within the coding region but diverges in both 3' and 5' nontranslated regions. The gene does not yield transcripts in response to heat shock in mouse L cells. Rather, the gene appears to be activated uniquely in the male germ line. Analysis of RNA from different developmental stages and from enriched populations of spermatogenic cells revealed that this gene is expressed during the prophase stage of meiosis. A transcript different in size from the major heat-inducible mouse transcripts is most abundant in meiotic prophase spermatocytes and decreases in abundance in postmeiotic stages of spermatogenesis. This pattern of expression is distinct from that observed for another member of this gene family, which was previously shown to be expressed abundantly in postmeiotic germ cells. These observations suggest that specific HSP70 gene family members play distinct roles in the differentiation of the germ cell lineage in mammals.

Full text

PDF
2925

Images in this article

2927Image
on p.2927
2929Image
on p.2929
2930Image
on p.2930
2930Image
on p.2930

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Attenello J. W., Lee A. S. Regulation of a hybrid gene by glucose and temperature in hamster fibroblasts. Science. 1984 Oct 12;226(4671):187–190. doi: 10.1126/science.6484570. [DOI] [PubMed] [Google Scholar]
  2. Aviv H., Leder P. Purification of biologically active globin messenger RNA by chromatography on oligothymidylic acid-cellulose. Proc Natl Acad Sci U S A. 1972 Jun;69(6):1408–1412. doi: 10.1073/pnas.69.6.1408. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bellvé A. R., Millette C. F., Bhatnagar Y. M., O'Brien D. A. Dissociation of the mouse testis and characterization of isolated spermatogenic cells. J Histochem Cytochem. 1977 Jul;25(7):480–494. doi: 10.1177/25.7.893996. [DOI] [PubMed] [Google Scholar]
  4. Bensaude O., Babinet C., Morange M., Jacob F. Heat shock proteins, first major products of zygotic gene activity in mouse embryo. Nature. 1983 Sep 22;305(5932):331–333. doi: 10.1038/305331a0. [DOI] [PubMed] [Google Scholar]
  5. Bensaude O., Morange M. Spontaneous high expression of heat-shock proteins in mouse embryonal carcinoma cells and ectoderm from day 8 mouse embryo. EMBO J. 1983;2(2):173–177. doi: 10.1002/j.1460-2075.1983.tb01401.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bienz M. Developmental control of the heat shock response in Xenopus. Proc Natl Acad Sci U S A. 1984 May;81(10):3138–3142. doi: 10.1073/pnas.81.10.3138. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bonner J. J., Parks C., Parker-Thornburg J., Mortin M. A., Pelham H. R. The use of promoter fusions in Drosophila genetics: isolation of mutations affecting the heat shock response. Cell. 1984 Jul;37(3):979–991. doi: 10.1016/0092-8674(84)90432-x. [DOI] [PubMed] [Google Scholar]
  8. Cathala G., Savouret J. F., Mendez B., West B. L., Karin M., Martial J. A., Baxter J. D. A method for isolation of intact, translationally active ribonucleic acid. DNA. 1983;2(4):329–335. doi: 10.1089/dna.1983.2.329. [DOI] [PubMed] [Google Scholar]
  9. Craig E. A. The heat shock response. CRC Crit Rev Biochem. 1985;18(3):239–280. doi: 10.3109/10409238509085135. [DOI] [PubMed] [Google Scholar]
  10. Dworniczak B., Mirault M. E. Structure and expression of a human gene coding for a 71 kd heat shock 'cognate' protein. Nucleic Acids Res. 1987 Jul 10;15(13):5181–5197. doi: 10.1093/nar/15.13.5181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  12. Glaser R. L., Wolfner M. F., Lis J. T. Spatial and temporal pattern of hsp26 expression during normal development. EMBO J. 1986 Apr;5(4):747–754. doi: 10.1002/j.1460-2075.1986.tb04277.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hahnel A. C., Gifford D. J., Heikkila J. J., Schultz G. A. Expression of the major heat shock protein (hsp 70) family during early mouse embryo development. Teratog Carcinog Mutagen. 1986;6(6):493–510. doi: 10.1002/tcm.1770060603. [DOI] [PubMed] [Google Scholar]
  14. Holmgren R., Livak K., Morimoto R., Freund R., Meselson M. Studies of cloned sequences from four Drosophila heat shock loci. Cell. 1979 Dec;18(4):1359–1370. doi: 10.1016/0092-8674(79)90246-0. [DOI] [PubMed] [Google Scholar]
  15. Kothary R., Perry M. D., Moran L. A., Rossant J. Cell-lineage-specific expression of the mouse hsp68 gene during embryogenesis. Dev Biol. 1987 Jun;121(2):342–348. doi: 10.1016/0012-1606(87)90170-9. [DOI] [PubMed] [Google Scholar]
  16. Krawczyk Z., Szymik N., Wiśniewski J. Expression of hsp70-related gene in developing and degenerating rat testis. Mol Biol Rep. 1987;12(1):35–41. doi: 10.1007/BF00580648. [DOI] [PubMed] [Google Scholar]
  17. Kurtz S., Rossi J., Petko L., Lindquist S. An ancient developmental induction: heat-shock proteins induced in sporulation and oogenesis. Science. 1986 Mar 7;231(4742):1154–1157. doi: 10.1126/science.3511530. [DOI] [PubMed] [Google Scholar]
  18. Lin A. Y., Chang S. C., Lee A. S. A calcium ionophore-inducible cellular promoter is highly active and has enhancerlike properties. Mol Cell Biol. 1986 Apr;6(4):1235–1243. doi: 10.1128/mcb.6.4.1235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Lindquist S. The heat-shock response. Annu Rev Biochem. 1986;55:1151–1191. doi: 10.1146/annurev.bi.55.070186.005443. [DOI] [PubMed] [Google Scholar]
  20. Lowe D. G., Moran L. A. Molecular cloning and analysis of DNA complementary to three mouse Mr = 68,000 heat shock protein mRNAs. J Biol Chem. 1986 Feb 15;261(5):2102–2112. [PubMed] [Google Scholar]
  21. Lowe D. G., Moran L. A. Proteins related to the mouse L-cell major heat shock protein are synthesized in the absence of heat shock gene expression. Proc Natl Acad Sci U S A. 1984 Apr;81(8):2317–2321. doi: 10.1073/pnas.81.8.2317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Mizusawa S., Nishimura S., Seela F. Improvement of the dideoxy chain termination method of DNA sequencing by use of deoxy-7-deazaguanosine triphosphate in place of dGTP. Nucleic Acids Res. 1986 Feb 11;14(3):1319–1324. doi: 10.1093/nar/14.3.1319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Morimoto R. I., Hunt C., Huang S. Y., Berg K. L., Banerji S. S. Organization, nucleotide sequence, and transcription of the chicken HSP70 gene. J Biol Chem. 1986 Sep 25;261(27):12692–12699. [PubMed] [Google Scholar]
  24. Mues G. I., Munn T. Z., Raese J. D. A human gene family with sequence homology to Drosophila melanogaster Hsp70 heat shock genes. J Biol Chem. 1986 Jan 15;261(2):874–877. [PubMed] [Google Scholar]
  25. Munro S., Pelham H. R. An Hsp70-like protein in the ER: identity with the 78 kd glucose-regulated protein and immunoglobulin heavy chain binding protein. Cell. 1986 Jul 18;46(2):291–300. doi: 10.1016/0092-8674(86)90746-4. [DOI] [PubMed] [Google Scholar]
  26. Mutter G. L., Wolgemuth D. J. Distinct developmental patterns of c-mos protooncogene expression in female and male mouse germ cells. Proc Natl Acad Sci U S A. 1987 Aug;84(15):5301–5305. doi: 10.1073/pnas.84.15.5301. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. NEBEL B. R., AMAROSE A. P., HACKET E. M. Calendar of gametogenic development in the prepuberal male mouse. Science. 1961 Sep 22;134(3482):832–833. doi: 10.1126/science.134.3482.832. [DOI] [PubMed] [Google Scholar]
  28. O'Malley K., Mauron A., Barchas J. D., Kedes L. Constitutively expressed rat mRNA encoding a 70-kilodalton heat-shock-like protein. Mol Cell Biol. 1985 Dec;5(12):3476–3483. doi: 10.1128/mcb.5.12.3476. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Oppi C., Shore S. K., Reddy E. P. Nucleotide sequence of testis-derived c-abl cDNAs: implications for testis-specific transcription and abl oncogene activation. Proc Natl Acad Sci U S A. 1987 Dec;84(23):8200–8204. doi: 10.1073/pnas.84.23.8200. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Pelham H. R., Bienz M. A synthetic heat-shock promoter element confers heat-inducibility on the herpes simplex virus thymidine kinase gene. EMBO J. 1982;1(11):1473–1477. doi: 10.1002/j.1460-2075.1982.tb01340.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Pelham H. R. Speculations on the functions of the major heat shock and glucose-regulated proteins. Cell. 1986 Sep 26;46(7):959–961. doi: 10.1016/0092-8674(86)90693-8. [DOI] [PubMed] [Google Scholar]
  32. Petko L., Lindquist S. Hsp26 is not required for growth at high temperatures, nor for thermotolerance, spore development, or germination. Cell. 1986 Jun 20;45(6):885–894. doi: 10.1016/0092-8674(86)90563-5. [DOI] [PubMed] [Google Scholar]
  33. Ponzetto C., Wolgemuth D. J. Haploid expression of a unique c-abl transcript in the mouse male germ line. Mol Cell Biol. 1985 Jul;5(7):1791–1794. doi: 10.1128/mcb.5.7.1791. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Roccheri M. C., Di Bernardo M. G., Giudice G. Synthesis of heat-shock proteins in developing sea urchins. Dev Biol. 1981 Apr 15;83(1):173–177. doi: 10.1016/s0012-1606(81)80020-6. [DOI] [PubMed] [Google Scholar]
  35. Rothman J. E., Schmid S. L. Enzymatic recycling of clathrin from coated vesicles. Cell. 1986 Jul 4;46(1):5–9. doi: 10.1016/0092-8674(86)90852-4. [DOI] [PubMed] [Google Scholar]
  36. 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]
  37. Wahl G. M., Stern M., Stark G. R. Efficient transfer of large DNA fragments from agarose gels to diazobenzyloxymethyl-paper and rapid hybridization by using dextran sulfate. Proc Natl Acad Sci U S A. 1979 Aug;76(8):3683–3687. doi: 10.1073/pnas.76.8.3683. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Wang J. Y., Baltimore D. Cellular RNA homologous to the Abelson murine leukemia virus transforming gene: expression and relationship to the viral sequence. Mol Cell Biol. 1983 May;3(5):773–779. doi: 10.1128/mcb.3.5.773. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Wolgemuth D. J., Engelmyer E., Duggal R. N., Gizang-Ginsberg E., Mutter G. L., Ponzetto C., Viviano C., Zakeri Z. F. Isolation of a mouse cDNA coding for a developmentally regulated, testis-specific transcript containing homeo box homology. EMBO J. 1986 Jun;5(6):1229–1235. doi: 10.1002/j.1460-2075.1986.tb04351.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Wolgemuth D. J., Gizang-Ginsberg E., Engelmyer E., Gavin B. J., Ponzetto C. Separation of mouse testis cells on a Celsep (TM) apparatus and their usefulness as a source of high molecular weight DNA or RNA. Gamete Res. 1985;12:1–10. doi: 10.1002/mrd.1120120102. [DOI] [PubMed] [Google Scholar]
  41. Wu B. J., Hurst H. C., Jones N. C., Morimoto R. I. The E1A 13S product of adenovirus 5 activates transcription of the cellular human HSP70 gene. Mol Cell Biol. 1986 Aug;6(8):2994–2999. doi: 10.1128/mcb.6.8.2994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Zakeri Z. F., Wolgemuth D. J. Developmental-stage-specific expression of the hsp70 gene family during differentiation of the mammalian male germ line. Mol Cell Biol. 1987 May;7(5):1791–1796. doi: 10.1128/mcb.7.5.1791. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Zimmerman J. L., Petri W., Meselson M. Accumulation of a specific subset of D. melanogaster heat shock mRNAs in normal development without heat shock. Cell. 1983 Apr;32(4):1161–1170. doi: 10.1016/0092-8674(83)90299-4. [DOI] [PubMed] [Google Scholar]

Articles from Molecular and Cellular Biology are provided here courtesy of Taylor & Francis

RESOURCES