Skip to main content
Log in

Stage-specific localization of cytoskeletal actin mRNA in murine seminiferous tubules and intestinal epithelia as demonstrated by in-situ hybridization

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

In-situ hybridization experiments have been performed using isoactin (β and γ)-specific riboprobes in various tissues of the rat and mouse. Distribution of the grains of actin mRNAs for both β and γ types was similar throughout sections of the rat testis. Although both mRNAs were evenly distributed in the seminiferous tubule, extremely heavy labeling was observed in about 10% of the seminiferous tubules that could be identified as stage XII of spermatogenesis. At high magnification, grains of the mRNA were found in the cytoplasm of elongating spermatids and in the Sertoli cell cytoplasm at the adluminal side. Much higher density of the grains of mRNA was observed in the neck region of the spermatids at stage XII. Thus, the dense distribution of cytoskeletal actin mRNAs is stage-specific in the tubule during spermatogenesis in the rat. The high expression of both β and γ actin mRNAs was also observed in the epithelial cells of the intestinal crypts.

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

  • Angerer LM, Cox KH, Angerer RC (1987) Demonstration of tissue-specific gene expression by in situ hybridization. In: Berger SL, Kimmel AR (eds) Methods Enzymol Vol 152. Acad Press, Orlando, pp 649–661

    Google Scholar 

  • Baccetti B, Bigliardi E, Burrini AG, Pallini V (1989) Actin filaments and mitochondrial movement in vertebrate spermatogenesis. Gamete Res 3:203–209

    Google Scholar 

  • Bachvarova R, Cohen EM, De Leon V, Tokunaga K, Sakiyama S, Paynton BV (1989) Amounts and modulation of β- and γ-actin mRNAs in mouse oocytes and embryos. Development 106:561–566

    Google Scholar 

  • Begg DA, Rodewald R, Rebhum LI (1978) The visualization of actin filament polarity in thin sections: Evidence for the uniform polarity of membrane-associated filaments. J Cell Biol 79:846–852

    Google Scholar 

  • Chemes HE, Fawcett DW, Dym M (1978) Unusual features of the nuclear envelope in human spermatogenic cells. Anat Rec 192:493–512

    Google Scholar 

  • Cleveland DW, Lopata MA, Macdonald RJ, Cowan NJ, Rutter WJ, Kirschner MW (1980) Number and evolutionary conservation of α- and β-tubulin and cytoplasmic β- and γ-actin genes using specific cloned cDNA probes. Cell 20:95–105

    Google Scholar 

  • Erba HP, Gunning P, Kedes L (1986) Nucleotide sequence of the human cytoskeletal actin mRNA: anomalous evolution of vertebrate non-muscle actin genes. Nucleic Acids Res 14:5275–5294

    Google Scholar 

  • Erba HP, Eddy R, Shows T, Kedes L, Gunning P (1988) Structure, chromosome locaton, and expression of the human γ-actin gene: Differential evolution, location, and expression of the cytoskeletal β- and γ-actin genes. Mol Cell Biol 8:1775–1789

    Google Scholar 

  • Fawcett DW, Phillips DM (1969) The fine structure and development of the neck region of the mammalian spermatozoon. Anat Rec 165:153–184

    Google Scholar 

  • Franke WW, Grund C, Fink A, Weber K, Jockusch BM, Zentgraf A, Osborn M (1978) Location of actin in the microfilament bundles associated with the junctional specializations between Sertoli cells and spermatids. Biol Cell 31:7–14

    Google Scholar 

  • Garrels JI, Gibson W (1976) Identification and characterization of multiple forms of actin. Cell 9:793–805

    Google Scholar 

  • Hecht NB, Penshow JD (1987) In situ localization of mRNAs coding for mouse testicular structural genes. Exp Cell Res 173:274–281

    Google Scholar 

  • Hirokawa N, Keller III TCS, Chasan R, Mooseker MS (1983) Mechanism of brush border contractility studied by quickfreeze, deep-etch method. J Cell Biol 96:1325–1336

    Google Scholar 

  • Kierszenbaum AL, Tres LL (1974) Nucleolar and perichromosomal RNA synthesis during meiotic prophase in the mouse testis. J Cell Biol 60:39–53

    Google Scholar 

  • Kleene KC, Distel RJ, Hecht NB (1984) Translational regulation and deadenylation of a protamine mRNA during spermatogenesis in the mouse. Dev Biol 105:71–79

    Google Scholar 

  • Krawczyk Z, Wisniewski J, Biesiada E (1987) A hsp70-related gene is constitutively highly expressed in testis of rat and mouse. Mol Biol Rep 12:27–34

    Google Scholar 

  • Kretser DM de, Kerr JB (1988) The cytology of the testis. In: Knobil E, Neil JD (eds) Physiol Reprod Vol 1. Raven Press, New York, pp 837–932

    Google Scholar 

  • Lawrence JB, Singer RH (1986) Intracellular localization of messenger RNAs for cytoskeletal proteins. Cell 45:407–415

    Google Scholar 

  • Maekawa M, O'Brien DA, Allen RL, Eddy EM (1989) Heat shock protein (hsp71) and related proteins in mouse spermatogenic cells. Biol Reprod 40:843–852

    Google Scholar 

  • Mali P, Sandberg M, Vuorio E, Yelick PC, Hecht NB, Parvinen M (1988) Localization of protamine 1 mRNA in different stages of the cycle of the rat seminiferous epithelium. J Cell Biol 107:407–412

    Google Scholar 

  • Nudel U, Zakut R, Shani M, Neuman S, Levy Z, Yaffe D (1983) The nucleotide sequence of the rat cytoplasmic β-actin gene. Nucleic Acids Res 11:1759–1771

    Google Scholar 

  • Oakberg EF (1956) Duration of spermatogenesis in the mouse and timing of stages of the cycle of the seminiferous epithelium. Am J Anat 99:507–516

    CAS  PubMed  Google Scholar 

  • Otey CA, Kalnoski MH, Lessard JL, Bulinski JC (1986) Immunolocalization of the gamma isoform of nonmuscle actin in cultured cells. J Cell Biol 102:1726–1736

    Google Scholar 

  • Otey CA, Kalnoski MH, Bulinski JC (1987) Identification and quantitation of actin isoforms in vertebrate cells and tissues. J Cell Biochem 34:113–124

    Google Scholar 

  • Pardue ML (1985) In situ hybridization. In: Hames BD, Higgins SJ (eds) Nucleic acid hybridisation; a practical approach. IRL Press, Oxford, pp 179–202

    Google Scholar 

  • Perey B, Clermont Y, Leblond CP (1961) The wave of the seminiferous epithelium in the rat. Am J Anat 108:47–77

    Google Scholar 

  • Ponte P, Ng SY, Engel J, Gunning P, Kedes R (1984) Evolutionary conservation in the untranslated regions of actin mRNAs. Nucleic Acids Res 12:1687–1696

    Google Scholar 

  • Roosen-Runge EC (1962) The process of spermatogenesis in mammals. Biol Rev 37:343–377

    Google Scholar 

  • Russell L (1977) Membranous structures within nuclei of spermatoytes in the adult male rat. Biol Reprod 17:184–191

    Google Scholar 

  • Russell LD (1979) Further observations on tubulobular complexes formed by late spermatids and Sertoli cells in the rat testis. Anat Rec 194:213–232

    Google Scholar 

  • Russell LD (1980) Sertoli-germ cell interrelations: A review. Gamete Res 3:179–202

    Google Scholar 

  • Russell LD, Malone J (1980) A study of spermatid-Sertoli tubulobular complexes and selected mammals. Tissue Cell 12:263–285

    Google Scholar 

  • Russell LD, Peterson RN (1985) Sertoli cell junctions; morphological and functional correlates. Int Rev Cytol 94:177–211

    Google Scholar 

  • Russell LD, Vogl AW, Weber JE (1987) Actin localization in male germ cell intercellular bridges in the rat and ground squirrel and disruption of bridges by cytochalasin D. Am J Anat 180:25–40

    Google Scholar 

  • Russell LD, Goh JC, Rasshed RMA, Vogl AW (1988) The conseuences of actin distribution at Sertoli ectoplasmic specialization sites facing spermatids after in vivo exposure of rat testis to cytochalasin D. Biol Reprod 39:105–118

    Google Scholar 

  • Sakiyama S, Fujimura S, Sakiyama H (1981) Absence of γ actin expression in the mouse fibroblast L. J Biol Chem 256:31–33

    Google Scholar 

  • Schimenti J, Cebra-Thomas JA, Decker CL, Islam SD, Pider SH, Silver LM (1988) A candidate gene family for the mouse t complex responder (Tcr) locus responsible for haploid effects on sperm function. Cell 55:71–78

    Google Scholar 

  • Setchell BP (1978) The mammalian testis. Cornell University Press, Ithaca

    Google Scholar 

  • Söderström KO, Parvinen M (1976a) Incorporation of (3H) uridine by chromatoid body during rat spermatogenesis. J Cell Biol 70:239–446

    Google Scholar 

  • Söderström KO, Parvinen M (1976b) Transport of material between the nucleus, the chromatoid body and Golgi complex in the early spermatids of the rat. Cell Tissue Res 168:335–342

    Google Scholar 

  • Tokunaga K, Taniguchi H, Yoda K, Shimizu M, Sakiyama S (1986) Nucleotide sequence of a full length cDNA for mouse cytoskeletal β actin. Nucleic Acids Res 14:2829–2829

    Google Scholar 

  • Tokunaga K, Takeda K, Kamiyama K, Kageyama H, Takenaga K, Sakiyama S (1988) Isolation of cDNA clones for mouse cytoskeletal γ-actin and differential expression of cytoskeletal actin mRNAs in mouse cells. Mol Cell Biol 8:3929–3933

    Google Scholar 

  • Toyama Y (1976) Actin-like filaments in the Sertoli cell junctional specializations in the swine and mouse testis. Anat Rec 186:477–492

    Google Scholar 

  • Vandekerckhov J, Weber K (1979) The complete amino acid seuence of actins from bovine aorta, bovine heart, bovine skeletal muscle, and rabbit slow skeletal muscle. Differentiation 14:123–133

    Google Scholar 

  • Vogl AW, Soucy LJ (1985a) Arrangement and possible function of actin filament bundles in ectoplasmic specializations of ground squirrel Sertoli cells. J Cell Biol 100:814–825

    Google Scholar 

  • Vogl AW, Soucy LJ, Lew GJ (1985b) Distribution of actin in isolated seminiferous epithelia and denuded tubule walls of the rat. Anat Rec 213:63–71

    Google Scholar 

  • Vogl AW, Grove BD, Lew GJ (1986) Distribution of actin in Sertoli cell ectoplasmic specializations and associated spermatids in the ground squirrel testis. Anat Rec 215:331–341

    Google Scholar 

  • Waters SH, Distel RJ, Hecht NB (1985) Mouse testes contain two size classes of actin mRNA that are differentially expressed during spermatogenesis. Mol Cell Biol 5:1649–1654

    Google Scholar 

  • Wolber RA, Beals TF, Maassab HF (1989) Ultrastructural localization of herpes simplex virus RNA by in situ hybridization. J Histochem Cytochem 37:97–104

    Google Scholar 

  • Yelick PC, Balhorn R, Johnson PA, Corzett M, Mazrimas JA, Kleene KC, Hecht NB (1987) Mouse protamine2 is synthesized as a precursor whereas mouse protamine1 is not. Mol Cell Biol 7:2173–2179

    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

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sakiyama, S., Nakamura, Y., Tokunaga, K. et al. Stage-specific localization of cytoskeletal actin mRNA in murine seminiferous tubules and intestinal epithelia as demonstrated by in-situ hybridization. Cell Tissue Res. 258, 225–231 (1989). https://doi.org/10.1007/BF00239442

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00239442

Key words

Navigation