Skip to main content

Heat Shock Gene Expression During Mammalian Gametogenesis and Early Embryogenesis

  • Chapter
Heat Shock and Development

Part of the book series: Results and Problems in Cell Differentiation ((RESULTS,volume 17))

Abstract

The progression of mammalian gametogenesis through mitotic and meiotic divisions, genetic recombination, and morphological differentiation involves varied and complex processes of cellular differentiation. Our laboratory has been interested in elucidating the genetic program that governs these events during mammalian germ-cell differentiation at the molecular level. This effort has been made increasingly feasible by advances in molecular biological approaches that facilitate the identification of specific genes which may play key roles in these processes. The advances have been at both the technical and strategic levels. For example, the use of techniques such as the polymerase chain reaction (PCR) has permitted the detection of specific gene expression in a very limited number of cells, such as in oocytes and early embryos (Rappolee et al. 1988). PCR can also be applied to the cloning of cDNAs from these stages (Welsh et al. 1990), allowing the identification and characterization of new genes which may be critical for gametogenesis and early embryogenesis.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 39.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Allen RL, O’Brien DA, Eddy EM (1988) A novel hsp70-like protein (P70) is present in mouse spermatogenic cells. Mol Cell Biol 8: 828–832

    PubMed  CAS  Google Scholar 

  • Ananthan J, Goldberg AL, Voellmy R (1986) Abnormal proteins serve as eukaryotic stress signals and trigger the activation of heat shock genes. Science 232: 522–524

    Article  PubMed  CAS  Google Scholar 

  • Anderson NL, Giometti CS, Gemell MA, Nance SL, Anderson NG (1982) A two-dimensional electrophoretic analysis of the heat-shock-induced proteins of human cells. Clin Chem 28–4: 1084–1092

    Google Scholar 

  • Barnier JV, Bensaude O, Morange M, Babinet C (1987) Mouse 89 kD heat shock protein. Two polypeptides with distinct developmental induction. Exp Cell Res 170: 186–194

    Google Scholar 

  • Baumgartner AP, Chrisman CL (1981) Ovum morphology after hyperthermic stress during meiotic maturation and ovulation in the mouse. J Reprod Fer 61: 91–96

    Article  CAS  Google Scholar 

  • Beato M (1989) Gene regulation by steroid hormones. Cell 56: 335–344

    Article  PubMed  CAS  Google Scholar 

  • Bellen HJ, O’Kane CJ, Wilson C, Grossniklaus U, Pearson RK, Gehring WJ (1989) P-element mediated enhancer detection: a versatile method to study development in Drosophila. Genes Dev 3: 1288–1300

    Article  PubMed  CAS  Google Scholar 

  • Bellve AR (1972) Viability and survival of mouse embryos following parental exposure to high temperature. J Reprod Fer 30: 71–81

    Article  CAS  Google Scholar 

  • Bellve AR (1973) Development of mouse embryos with abnormalities induced by parental heat stress. J Reprod Fer 35: 393–403

    Article  CAS  Google Scholar 

  • Bellve AR, Cavicchia JC, Millette CF, O’Brien DA, Bhatnagar YM, Dym M (1977) Spermatogenic cells of the prepuberal mouse. Isolation and morphological characterization. J Cell Biol 74: 68–85

    Google Scholar 

  • Bensaude O, Morange M (1983) Spontaneous high expression of heat-shock proteins in mouse embryonal carcinoma cells and ectoderm from day 8 mouse embryo. EMBO J 2: 173–177

    PubMed  CAS  Google Scholar 

  • Bensaude O, Babinet C, Morange M, Jacob F (1983) Heat shock proteins, first major products of zygotic gene activity in mouse embryo. Nature 305: 331–333

    Article  PubMed  CAS  Google Scholar 

  • Brugge JS (1986) Interaction of the Rous sarcoma virus protein with the cellular proteins, pp 50 and pp 90. Curr Top Microbiol Immunol 123: 1–22

    Article  PubMed  CAS  Google Scholar 

  • Catelli MG, Binart N, Jung-Testas I, Renoir JM, Baulieu EE, Feramisco JR, Welch WJ (1985) The common 90-kD protein component of non-transformed `8S’ steroid receptors is a heat-shock protein. EMBO J 4: 3131–3135

    PubMed  CAS  Google Scholar 

  • Chappell TG, Welch WJ, Schlossman DM, Palter KB, Schlessinger MJ, Rothman JE (1986) Uncoating ATPase is a member of the 70 kilodalton family of stress proteins. Cell 45: 3–13

    Article  PubMed  CAS  Google Scholar 

  • Cohen RS, Meselson M (1985) Separate regulatory elements for the heat-inducible and ovarian expression of the Drosophila hsp26 gene. Cell 43: 737–746

    Article  PubMed  CAS  Google Scholar 

  • Craig EA (1985) The heat shock response. Crit Rev Biochem 18: 239–280

    Article  CAS  Google Scholar 

  • Curci A, Bevilacqua A, Mangia F (1987) Lack of heat-shock response in preovulatory mouce oocytes. Dev Biol 123: 154–160

    Article  PubMed  CAS  Google Scholar 

  • Day AR, Lee AS (1989) Transcriptional regulation of the gene encoding the 78-kD glucose-regulated protein GRP78 in mouse Sertoli cells: binding of specific factor(s) to the GRP78 promoter. DNA: 301–310

    Google Scholar 

  • Frohman MA, Martin GR (1989) Cut, paste, and save: new approaches to altering specific genes in mice. Cell 56: 145–147

    Article  PubMed  CAS  Google Scholar 

  • Germain MA, Webster WS, Edwards MJ (1985) Hyperthermia as a teratogen: parameters determining hyperthermia-induced head defects in the rat. Teratology 31: 265–272

    Article  PubMed  CAS  Google Scholar 

  • Giguere V, Ong ES, Segui P, Evans RM (1987) Identification of a receptor for the morphogen retinoic acid. Nature 330: 624–629

    Article  PubMed  CAS  Google Scholar 

  • Glaser RL, Wolfner MF, Lis T (1986) Spatial and temporal pattern of hsp26 during normal development. EMBO J 5: 747–754

    PubMed  CAS  Google Scholar 

  • Goldman DS, Kisseling AA, Millette CF, Cooper GM (1987) Expression of c-mos RNA in germ cells of male and female mice. Proc Natl Acad Sci USA 84: 4509–4513

    Article  PubMed  CAS  Google Scholar 

  • Gossler A, Joyner AL, Rossant J, Skarnes WC (1989) Mouse embryonic stem cells and reporter constructs to detect developmentally regulated genes. Science 244: 463–465

    Article  PubMed  CAS  Google Scholar 

  • Green M (1981) Genetic variants and strains of the laboratory mouse. Gustav Fischer, New York, 476 pp

    Google Scholar 

  • Grossniklaus U, Bellen HJ, Wilson C, Gehring W (1989) P-element mediated enhancer detection applied to the study of oogenesis in Drosophila. Development 107: 189–200

    PubMed  CAS  Google Scholar 

  • Gruppi C, Zakeri ZF, Wolgemuth DJ (1991) Stage and lineage-regulated expression of two hsp90 transcripts during mouse germ cell differentiation and embryogenesis. Mol Reprod Dev (in press)

    Google Scholar 

  • Heikkila JJ, Schultz GA (1984) Different environmental stresses can activate the expression of a heat shock gene in rabbit blastocysts. Gamete Res 10: 45–56

    Article  CAS  Google Scholar 

  • Heikkila JJ, Miller JGO, Schultz GA, Kloc M, Browder LW (1985) Heat shock gene expression during early animal development. In: Atkinson BG, Walden DB (eds) Changes in eukaryotic gene expression in response to environmental stress. Academic Press, Orlando, pp 135–138

    Chapter  Google Scholar 

  • Hickey E, Brandon SE, Smale G, Lloyd D, Weber LA (1989) Sequence and regulation of a gene encoding a human 89-kilodalton heat shock protein. Mol Cell Biol 9: 2615–2626

    PubMed  CAS  Google Scholar 

  • Joab I, Radanyi C, Renoir M, Buchou T, Catelli MG, Binart N, Mester J, Baulieu EE (1984) Common non-hormone binding component-transformed chick oviduct receptors of four steroid hormones. Nature 308: 850–853

    Article  PubMed  CAS  Google Scholar 

  • Kleene K, Distel RJ, Hecht NB (1985) Nucleotide sequence of a cDNA clone encoding mouse protamine 1. Biochemistry 24: 719–722

    Article  PubMed  CAS  Google Scholar 

  • Kost SL, Smith DL, Sullivan WP, Welch WJ, Toft DO (1989) Binding of heat shock proteins to the avian progesterone receptor. Mol Cell Biol 9: 3829–3838

    PubMed  CAS  Google Scholar 

  • Kothary R, Clapoff S, Darling S, Perry MD, Moran LA, Rossant J (1987) Cell-lineage specific expression of the mouse hsp68 gene during embryogenesis. Dev Biol 121: 342–348

    Article  PubMed  CAS  Google Scholar 

  • Kothary R, Clapoff S, Brown A, Campbell R, Peterson A, Rossant J (1988) A transgene containing lacZ inserted into the dystonia locus is expressed in neural tube. Nature 335: 435–437

    Article  PubMed  CAS  Google Scholar 

  • Kothary R, Clapoff S, Darling S, Perry MD, Moran LA, Rossant J (1989) Inducible expression of an hsp68-lacZ hybrid gene in transgenic mice. Development 105: 707–714

    PubMed  CAS  Google Scholar 

  • Koyasu S, Nishida E, Kadowaki T, Matsuzaki F, Iida K, Harada F, Kasuga H, Sakai H, Yahara I (1986) Two mammalian heat shock proteins, hsp90 and hsp100, are actin binding proteins. Proc Natl Acad Sci USA 83: 8054–8058

    Article  PubMed  CAS  Google Scholar 

  • Krawczyk Z, Mali P, Parvinen M (1988) Expression of a testis-specific hsp70 gene-related RNA in defined stages of rat seminiferous epithelium. J Cell Biol 107: 1317–1323

    Article  PubMed  CAS  Google Scholar 

  • Kurtz S, Rossi J, Petko L, Lindquist S (1986) An ancient developmental induction: heat-shock proteins induced in sporulation and oogenesis. Science 231: 1154–1156

    Article  PubMed  CAS  Google Scholar 

  • Lai BT, Chin NW, Stanek AE, Keh W, Lanks KW (1984) Quantitation and intracellular localization of the 85K heat shock protein by using monoclonal and polyclonal antibodies. Mol Cell Biol 4: 2802–2810

    PubMed  CAS  Google Scholar 

  • Lee SJ (1990) Expression of hsp86 in male germ cells. Mol Cell Biol 10: 3239–3242

    PubMed  CAS  Google Scholar 

  • Lenz RW, Ball GD, Leibfried ML, Ax RL, First NL (1983) In vitro maturation and fertilization of bovine oocytes are temperature-dependent processes. Biol Reprod 29: 173–179

    Article  PubMed  CAS  Google Scholar 

  • Levine RA, La Rosa GJ, Gudas LJ (1984) Isolation of cDNA clones for genes exhibiting reduced expression after differentiation of murine teratocarcinoma stem cells. Mol Cell Biol 4: 2142–2150

    PubMed  CAS  Google Scholar 

  • Lindquist S (1986) The heat shock response. Annu Rev Biochem 55: 1151–1191

    Article  PubMed  CAS  Google Scholar 

  • Lowe DG, Moran LA (1986) Molecular cloning and analysis of DNA complementary to three mouse Mr=68000 heat shock protein mRNAs. J Biol Chem 261: 2102–2120

    PubMed  CAS  Google Scholar 

  • Moore CR, Chase D (1923) Heat application and testicular differentiation. Anat Rec 26: 344–345

    Google Scholar 

  • Moore SK, Kozak C, Robinson EA, Ullrich SJ, Apella E (1987) Cloning and nucleotide sequence of the murine hsp84 cDNA and chromosomes assignments of related sequences. Gene 56: 29–40

    Article  PubMed  CAS  Google Scholar 

  • Moore SK, Kozak C, Robinson EA, Ullrich SJ, Apella E (1989) Murine 86- and 84-kDa heat shock proteins cDNA sequences and chromosome assignments and evolutionary origins. J Biol Chem 264: 5343–5351

    PubMed  CAS  Google Scholar 

  • Morange M, Diu A, Bensaude O, Babinet C (1984) Altered expression of heat shock proteins in embryonal carcinoma cells and mouse early embryonic cells. Mol Cell Biol 4: 730–735

    PubMed  CAS  Google Scholar 

  • Mutter GL, Wolgemuth DJ (1987) Distinct developmental patterns of c-mos protooncogene expression in female and male germ cells. Proc Natl Acad Sci USA 84: 5301–5305

    Article  PubMed  CAS  Google Scholar 

  • Mutter GL, Grills GS, Wolgemuth DJ (1988) Evidence for the involvement of the protooncogene c-mos in mammalian meiotic maturation and possibly very early embryogenesis. EMBO J 7: 683–689

    PubMed  CAS  Google Scholar 

  • Nebel BR, Amarose AP, Hackett EM (1961) Calendar of gametogenic development in the prepuberal mouse. Science 134: 832–833

    Article  PubMed  CAS  Google Scholar 

  • Nishida E, Koyasu S, Sakai H, Yaharas I (1986) Calmodulin-regulated binding of the 90-kDa heat shock protein to actin filaments. J Biol Chem 261: 16003–16036

    Google Scholar 

  • Pardue ML (1988) The heat shock response in biology and human disease: a meeting review. Genes Dev 2: 783–785

    Article  PubMed  CAS  Google Scholar 

  • Pelham H (1985) Activation of heat shock genes in eukaryotes. Trends Genet 1: 31–35

    Article  CAS  Google Scholar 

  • Pelham H (1988) Coming in from the cold. Nature 332: 776–777

    Article  PubMed  CAS  Google Scholar 

  • Pelham HRB (1986) Speculations on the functions of the major heat shock and glucose-regulated proteins. Cell 46: 959–961

    Article  PubMed  CAS  Google Scholar 

  • Peschon JJ, Behringer RR, Brinster RL, Palmiter RD (1987) Spermatid-specific expression of protamine 1 in transgenic mice. Proc Natl Acad Sci 84: 5316–5319

    Article  PubMed  CAS  Google Scholar 

  • Peters H (1969) The development of the mouse ovary from birth to maturity. Acta Endocrinol 62: 98–116

    PubMed  CAS  Google Scholar 

  • Petrovich M, Brand NJ, Krout A, Chambon P (1987) A human retinoic acid receptor. Nature 330: 444–450

    Article  Google Scholar 

  • Ponzetto C, Wolgemuth DJ (1985) Haploid expression of a unique c-abl transcript in the mouse male germ line. Mol Cell Biol 5: 1791–1794

    PubMed  CAS  Google Scholar 

  • Pratt WB (1987) Transformation of glucocorticoid and progesterone receptors to the DNA-binding state. J Cell Biochem 35: 51–68

    Article  PubMed  CAS  Google Scholar 

  • Propst F, Rosenberg MP, Iyer A, Kaul K, Vande Woude GF (1987) C-mos proto-oncogene RNA transcripts in mouse tissues: structural features, developmental regulation, and localization in specific cell types. Mol Cell Biol 7: 1629–1637

    Google Scholar 

  • Rappollee DA, Brenner CA, Schultz R, Mark D, Werb Z (1988) Developmental expression of PDGF TGF-alpha and TGF-beta genes in preimplantation mouse embryos. Science 241: 1823–1825

    Article  Google Scholar 

  • Rebagliati MR, Weeks DL, Harvey RP, Melton DA (1985) Identification and cloning of maternal mRNAs in Xenopus eggs. Cell 42: 769–777

    Article  PubMed  CAS  Google Scholar 

  • Rebbe NF, Ware J, Bertina RM, Modrich P, Stafford DW (1987) Nucleotide sequence of a cDNA for a member of the human 90-kDa heat-shock protein family. Gene 53: 235–245

    Article  PubMed  CAS  Google Scholar 

  • Redmond T, Sanchez ER, Bresnick EH, Schlesinger MJ, Toft DO, Pratt WB, Welsh MJ (1989) Immunofluorescence colocalization of the 90-kDa heat-shock protein and microtubules in interphase and miotic mammalian cells. Eur J Cell Biol 50: 66–75

    PubMed  CAS  Google Scholar 

  • Robertson EJ, Bradley A, Kuehn M, Evans M (1986) Germ-line transmission of genes introduced into cultured pluripotential cells by retroviral vectors. Nature 323: 445–447

    Article  PubMed  CAS  Google Scholar 

  • Robinson MO, McCarrey JR, Simon MI (1989) Transcriptional regulatory regions of testis-specific PGK2 defined in transgenic mice. Proc Natl Acad Sci 86: 8437–8441

    Article  PubMed  CAS  Google Scholar 

  • Rock J, Robinson D (1965) Effect of induced intrascrotal hyperthermia on testicular function in man. Am J Obstet Gynecol 93: 793–801

    PubMed  CAS  Google Scholar 

  • Sanchez ER, Toft DO, Schlessinger ML, Pratt WB (1985) Evidence that the 90-kDa phosphoprotein associated with untransformed cell glucocorticoid receptor is a murine heat shock protein. J Biol Chem 260: 12398–12401

    PubMed  CAS  Google Scholar 

  • Schwartzberg P, Goff SP, Robertson EJ (1989) Germ-line transmission of a c-abl mutation produced by targeted gene disruption in ES cells. Science 246: 799–803

    Article  PubMed  CAS  Google Scholar 

  • Thomas KH, Wilkie TM, Tomashefsky P, Bellve AR, Simon MI (1989) Differential gene expression during mouse spermatogenesis. Biol Reprod 41: 729–739

    Article  PubMed  CAS  Google Scholar 

  • Thomas KR, Capecchi MR (1987) Site-directed mutagenesis by gene targeting in mouse embryo-derived stem cells. Cell 51: 503–512

    Article  PubMed  CAS  Google Scholar 

  • Ulberg LC, Sheean LA (1973) Early development of mammalian embryos in elevated ambient temperatures. J Reprod Fertil 19 (Suppl): 155–161

    CAS  Google Scholar 

  • Webster WS, Edwards MJ (1984) Hyperthermia and the induction of neural tube defects in mice. Teratology 29: 417–425

    Article  PubMed  CAS  Google Scholar 

  • Weeks DL, Rebagliati MR, Harvey RP, Melton DA (1985) Localized maternal mRNA in Xenopus laevis eggs. Cold Spring Harbor Symp Quant Biol 50: 21–29

    Article  PubMed  CAS  Google Scholar 

  • Welsh J, Liu JP, Efstratiadis A (1990) Cloning of PCR-amplified total cDNA: construction of a mouse oocyte cDNA library. Genet Anal Techn Appl 7: 5–17

    Article  CAS  Google Scholar 

  • Wolbach SB, Howe PR (1925) Tissue changes following deprivation of fat soluble vitamin A. J Exp Med 42: 753–777

    Article  PubMed  CAS  Google Scholar 

  • Wolgemuth DJ, Gizang-Ginsberg E, Engelmyer E, Gavin BJ, Ponzetto C (1985) Separation of mouse testis cells on a CelsepTM apparatus and their usefulness as a source of high molecular weight DNA or RNA. Gamete Res 12: 1–10

    Article  PubMed  CAS  Google Scholar 

  • Wolgemuth DJ, Engelmeyer E, Duggal RN, Gizang-Ginsberg EE, Mutter GL, Ponzetto C, Vivano C, Zakeri ZF (1986) Isolation of a mouse cDNA coding for a developmentally regulated, testis-specific transcript containing homeo box homology. EMBO J 5: 1229–1235

    PubMed  CAS  Google Scholar 

  • Wolgemuth DJ, Viviano CM, Gizang-Ginsberg E, Frohman MA, Joyner AL, Martin GR (1987) Differential expression of the mouse homeobox-containing gene Hox-1.4 during male germ cell differentiation and embryonic development. Proc Natl Acad Sci USA 84: 5813–5817

    Article  PubMed  CAS  Google Scholar 

  • Wolgemuth DJ, Behringer RR, Mostoller MP, Brinster RL, Palmiter RD (1989) Transgenic mice over-expressing the mouse homeobox-containing gene Hox-1.4 exhibit abnormal gut development. Nature 337: 464–467

    Article  PubMed  CAS  Google Scholar 

  • Young WC (1927) The influence of high temperature on the guinea-pig testis. J Exp Zool 49: 459–499

    Article  Google Scholar 

  • Zakeri ZF, Wolgemuth DJ (1987) Developmental stage specific expression of the hsp70 gene family during differentiation of the mammalian male germ line. Mol Cell Biol 7: 1791–1796

    PubMed  CAS  Google Scholar 

  • Zakeri ZF, Wolgemuth DJ, Hunt CR (1988) 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. Mol Cell Biol 8: 2925–2932

    PubMed  CAS  Google Scholar 

  • Zakeri ZF, Welch WJ, Wolgemuth DJ (1990) Characterization and inducibility of hsp70 proteins in the male mouse germ line. J Cell Biol 111: 1785–1792

    Article  PubMed  CAS  Google Scholar 

  • Zimmerman JL, Petri W, Meselson M (1983) Accumulation of a specific subset of D. melanogaster heat shock mRNAs in normal development without heat shock. Cell 32: 1161–1170

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1991 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Wolgemuth, D.J., Gruppi, C.M. (1991). Heat Shock Gene Expression During Mammalian Gametogenesis and Early Embryogenesis. In: Hightower, L., Nover, L. (eds) Heat Shock and Development. Results and Problems in Cell Differentiation, vol 17. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-46712-0_10

Download citation

  • DOI: https://doi.org/10.1007/978-3-540-46712-0_10

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-662-21993-5

  • Online ISBN: 978-3-540-46712-0

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics