Molecular and Cellular Biology of Novel Cytoskeletal Proteins in Spermatozoa

  • Richard J. Oko
  • Carlos R. Morales
Part of the Serono Symposia USA Norwell, Massachusetts book series (SERONOSYMP)

Abstract

Most of the integral components of the mature mammalian spermatozoon are made up of cytoskeletal proteins that are synthesized and assembled during the haploid phase of spermatogenesis. With the exception of various isoforms of tubulin composing the microtubules of the sperm tail (1,2) and filamentous (3–5) and nonfilamentous (6, 7) forms of actin localized in diverse regions of the sperm head and tail of various species, the majority of sperm cytoskeletal proteins appear to have no protein or structural counterparts in somatic cells. Specialized cytoskeletal elements found in the sperm tail are the outer dense fibers (ODF), the fibrous sheath (FS), the submitochondrial reticulum (8), the annulus, and the striated collar and capitulum of the neck piece [reviewed by Oko and Clermont (9)]. In the sperm head are found the perinuclear theca (PT), the outer periacrosomal layer (OPL), and the basal plate [reviewed by Oko (10)]. The isolation or extraction of many of these sperm elements is made possible by their differential resistance to protein solubilizing agents (11–21). Compositional studies have revealed that most of these elements are made up of a heterogeneous mixture of proteins of various concentrations (11–21).

Keywords

Urea Codon Aldehyde Carboxylate Serine 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Hermo L, Oko R, Hecht NB. Differential post-transcriptional modifications of microtubules in cells of the seminiferous epithelium of the rat: a light and electron microscope immunocytochemical study. Anat Rec 1991;229:31–50.PubMedCrossRefGoogle Scholar
  2. 2.
    Distel RJ, Kleen KC, Hecht NB. Haploid expression of a mouse testis α tubulin gene. Science 1984;224:68–70.PubMedCrossRefGoogle Scholar
  3. 3.
    Flaherty SP, Winfrey VP, Olson GE. Localization of actin in human, bull, rabbit, and hamster sperm by immunoelectron microscopy. Anat Rec 1988;221:599–610.PubMedCrossRefGoogle Scholar
  4. 4.
    Olson GE, Winfrey VP, Flaherty SP. Cytoskeletal assemblies of mammalian spermatozoa. Ann NY Acad Sci 1987;513:222–46.PubMedCrossRefGoogle Scholar
  5. 5.
    Oko R, Hermo L, Hecht NB. Distribution of actin isoforms within cells of the seminiferous epithelium of the rat testis: evidence for a contractile form of actin in spermatids. Anat Rec 1991;232:63–81.CrossRefGoogle Scholar
  6. 6.
    Breed WG, Leigh CM. Distribution of filamentous actin in and around spermatids and in spermatozoa of Australian conilurine rodents. Mol Reprod Dev 1991;30:369–84.PubMedCrossRefGoogle Scholar
  7. 7.
    Flaherty SP, Breed WG, Sarafis V. Localization of actin in the sperm head of the plains mouse, Pseudomys australis. J Exp Zool 1983;225:497–500.PubMedCrossRefGoogle Scholar
  8. 8.
    Wierda A, Zheng L, Bartees LP. Cytoskeletal link between sperm mitochondrial sheath and outer dense fibres. Mol Biol Cell 1994;5:97a (abstract 563).Google Scholar
  9. 9.
    Oko R, Clermont Y. Mammalian spermatozoa; structure and assembly of the tail. In: Gagnon C, ed. Controls of sperm motility; biological and clinical aspects. Boca Raton, FL: CRC Press, 1990:3–27.Google Scholar
  10. 10.
    Oko R. Developmental expression and possible role of perinuclear theca proteins of mammalian spermatozoa. Reprod Fertil Dev 1995;7:777–97.PubMedCrossRefGoogle Scholar
  11. 11.
    Olson GE, Hamilton DW, Fawcett DW. Isolation and characterization of the perforatorium of rat spermatozoa. J Reprod Fertil 1976;47:1–9.CrossRefGoogle Scholar
  12. 12.
    Olson GE, Hamilton DW, Fawcett DW. Isolation and characterization of the fibrous sheath of rat epididymal spermatozoa. Biol Reprod 1976;14:517–30.PubMedCrossRefGoogle Scholar
  13. 13.
    Olson GE, Sammons DW. Structural chemistry of outer dense fibres of rat sperm. Biol Reprod 1980;22:319–32.PubMedCrossRefGoogle Scholar
  14. 14.
    Vera JC, Brito M, Zavic T, Burzio LO. Polypeptide composition of rat sperm outer dense fibres. J Biol Chem 1977;259:5970–77.Google Scholar
  15. 15.
    Longo FJ, Krohne G, Franke WW. Basic proteins of the perinuclear theca of mammalian spermatozoa and spermatids: a novel class of cytoskeletal elements. J Cell Biol 1987;105:1105–20.PubMedCrossRefGoogle Scholar
  16. 16.
    Oko R. Comparative analysis of proteins from fibrous sheath and outer dense fibres of rat spermatozoa. Biol Reprod 1988;39:169–82.PubMedCrossRefGoogle Scholar
  17. 17.
    Oko R, Clermont Y. Isolation, structure and protein composition of the perforatorium of rat spermatozoa. Biol Reprod 1988;39;673–87.PubMedCrossRefGoogle Scholar
  18. 18.
    Fenderson BA, Toshimori K, Muller CH, Lane TF, Eddy EM. Identification of a protein in the fibrous sheath of the sperm flagellum. Biol Reprod 1988;38:345–57.PubMedCrossRefGoogle Scholar
  19. 19.
    Brito M, Figueroa J, Maldonado EU, Vera JC, Burzio LO. The major component of rat sperm fibrous sheath is a phosphoprotein. Gamete Res 1989;22:205–18.PubMedCrossRefGoogle Scholar
  20. 20.
    Eddy EM, O’Brien DA, Fenderson BA, Welch JE. Intermediate filament-like proteins in the fibrous sheath of the mouse sperm flagellum. Ann NY Acad Sci 1991;637;224–39.PubMedCrossRefGoogle Scholar
  21. 21.
    Oko R, Maravei D. Protein composition of the perinuclear theca of bull spermatozoa. Biol Reprod 1994;50:1000–14.PubMedCrossRefGoogle Scholar
  22. 22.
    Oko R, Morales CR. A novel testicular protein, with sequence similarities to a family of lipid binding proteins, is a major component of the rat sperm perinuclear theca. Dev Biol 1994;166:235–45.PubMedCrossRefGoogle Scholar
  23. 23.
    Van Der Hoorn FA, Tarnasky HA, Nordeen SK. A new rat gene RT7 is specifically expressed during spermatogenesis. Dev Biol 1990;142:147–54.PubMedCrossRefGoogle Scholar
  24. 24.
    Burfeind P, Hoyer-Fender S. Sequence and developmental expression of a mRNA encoding a putative protein of rat sperm outer dense fibres. Dev Biol 1991;148:195–204.PubMedCrossRefGoogle Scholar
  25. 25.
    Morales CR, Oko R, Clermont Y. Molecular cloning and developmental expression of an mRNA encoding the 27kDa outer dense fiber protein of rat spermatozoa. Mol Reprod Dev 1994;37:229–40.PubMedCrossRefGoogle Scholar
  26. 26.
    Carrera A, Gerton GL, Moss SB. The major fibrous sheath polypeptide of mouse sperm: structural and functional similarities to the A-kinase anchoring proteins. Dev Biol 1994;165:272–84.PubMedCrossRefGoogle Scholar
  27. 27.
    Fulcher KD, Mori C, Welch JE, O’Brien DA, Klapper DG, Eddy EM. Characterization of Fsc1 cDNA for a mouse sperm fibrous sheath component. Biol Reprod 1995;52:41–9.PubMedCrossRefGoogle Scholar
  28. 28.
    Oko R, Moussakova L, Clermont Y. Regional differences in composition of the perforatorium and outer periacrosomal layer of the rat spermatozoon as revealed by immunocytochemistry. Am J Anat 1990;188:64–73.PubMedCrossRefGoogle Scholar
  29. 29.
    Narayanan U, Barbosa E, Reed R, Tennekoon G. Characterization of a cloned cDNA encoding rabbit myelin P2 protein. J Biol Chem 1988;263:8332–7.PubMedGoogle Scholar
  30. 30.
    Narayanan U, Kaestner KH, Tennekoon GI. Structure of the mouse myelin P2 protein gene. J Neurochem 1991;57:75–80.PubMedCrossRefGoogle Scholar
  31. 31.
    Bernlohr DA, Angus CE, Lane MD, Bolanowski MA, Kelly TJ. Expression of specific mRNAs during adipose differentiation: identification of an mRNA encoding a homologue of myelin P2 protein. Proc Natl Acad Sci USA 1984;81:5468–72.PubMedCrossRefGoogle Scholar
  32. 32.
    Sacchettini JC, Said B, Schulz H, Gordon JI. Rat heart fatty acid-binding protein is highly homologous to the murine adipocyte 422 protein and the P2 protein of peripheral nerve myelin. J Biol Chem 1968;261:8218–23.Google Scholar
  33. 33.
    Ong DE, Newcomer ME, Chytil F. Cellular retinoid-binding proteins. In: Sporn MB, Poberts AB, Goodman DS, eds. The retinoids: biology, chemistry and medicine, 2nd ed. New York: Raven Press, 1994:283–317.Google Scholar
  34. 34.
    Schmitt MC, Jamison RS, Orgebin-Crist M-C, Ong DE. A novel, testis-specific member of the cellular lipophilic transport protein superfamily, deduced from a complementary deoxyribonucleic acid clone. Biol Reprod 1994;51:239–45.PubMedCrossRefGoogle Scholar
  35. 35.
    Martenson RE. A general model of the P2 protein of peripheral nervous system myelin based on secondary structure predictions, tertiary folding principles and experimental observations. J Neurochem 1983;40:951–68.PubMedCrossRefGoogle Scholar
  36. 36.
    Newcomer ME, Jones TA, Aquist J, Sundelin J, Ericksson U, Rask L, Peterson PA. The three-dimensional structure of retinol-binding protein. EMBO J 1984;3:1451–4.PubMedGoogle Scholar
  37. 37.
    Jones TA, Bergfors T, Sedzik J, Unge T. The three-dimensional structure of the P2 myelin protein. EMBO J 1988;7:1597–604.PubMedGoogle Scholar
  38. 38.
    Sacchettini JC, Gordon JI, Banaszuk LJ. The structure of crystalline Escherichia coli derived rat intestinal fatty acid-binding protein at 2.5-Å resolution. J Biol Chem 1988;263:5815–9.PubMedGoogle Scholar
  39. 39.
    Xu Z, Bernlohr DA, Banaszak LJ. Crystal structure of recombinant murine adipocyte lipid-binding protein. Biochemistry 1992;31:3484–92.PubMedCrossRefGoogle Scholar
  40. 40.
    Xu Z, Bernlohr DA, Banaszak LJ. The adipocyte lipid-binding protein at 1.6Å resolution: crystal structures of the apoprotein with bound saturated and unsaturated fatty acids. J Biol Chem 1993;268:7874–84.PubMedGoogle Scholar
  41. 41.
    Cowan SW, Newcomer ME, Jones TA. Crystallographic studies on a family of cellular lipophilic transport proteins. J Mol Biol 1993;230:1225–46.PubMedCrossRefGoogle Scholar
  42. 42.
    Sha RS, Kane CD, Xu Z, Banaszak LJ, Bernlohr DA. Modulation of ligand binding affinity of the adipocyte lipid binding protein by selective mutation: analyses in vitro and in vivo. J Biol Chem 1993;268:7885–92.PubMedGoogle Scholar
  43. 43.
    Zhang J, Liu Z-P, Jones TA, Gierasch LM, Sambrook JF. Mutating the charged residues in the binding pocket of cellular retinoic acid-binding protein simultaneously reduces its binding affinity to retinoic acid and increases its thermostability. Proteins 1992;13:87–99.PubMedCrossRefGoogle Scholar
  44. 44.
    Buelt MK, Bermlohr DA. Modification of the adipocyte lipid binding protein by sulfhydryl reagents and analysis of the fatty acid binding domain. Biochemistry 1990;29:7408–13.PubMedCrossRefGoogle Scholar
  45. 45.
    Uyemura K, Yoshimura K, Suzuki M, Kitamura K. Lipid binding activities of the P2 protein in peripheral nerve myelin. Neurochem Res 1984;9:1509–14.PubMedCrossRefGoogle Scholar
  46. 46.
    Boggs JM, Clement IR, Moscarello MA, Eylar HE, Hushim G. Antibody precipitation of lipid vesicles containing myelin proteins: dependence on lipid composition. J Immunol 1981;126:1207–11.PubMedGoogle Scholar
  47. 47.
    Chapman BE, James GE, Moore WJ. Conformations of P2 protein of peripheral nerve myelin by nuclear magnetic resonance spectroscopy. J Neurochem 1981;36:2032–6.PubMedCrossRefGoogle Scholar
  48. 48.
    Trapp BD, Dubois-Dalcq M, Quarles RH. Ultrastructural localization of P2 protein in actively myelinating rat Schwann cells. J Neurochem 1984;43:944–8.PubMedCrossRefGoogle Scholar
  49. 49.
    Kadlubowski M, Hughes AC, Gregson NA. Experimental allergic neuritis in the Lewis rat: characterization of the activity of peripheral myelin and its major basic protein, P2. Brain Res 1980;184:439–54.PubMedCrossRefGoogle Scholar
  50. 50.
    Shin HC, McFarlane EF, Pollard JD, Watson EGS. Induction of experimental allergic neuritis with synthetic peptides from myelin P2 protein. Neurosci Lett 1989;102:309–12.PubMedCrossRefGoogle Scholar
  51. 51.
    Rostami A, Gregorian SK. Peptide 53–78 of myelin P2 protein is a T cell epitope for the induction of experimental autoimmune neuritis. Cell Immunol 1991; 132:433–41.PubMedCrossRefGoogle Scholar
  52. 52.
    Oko R, Clermont Y. Origin and distribution of perforatorial proteins during spermatogenesis of the rat: an immunocytochemical study. Anat Rec 1991;230:489–501.PubMedCrossRefGoogle Scholar
  53. 53.
    Oko R, Maravei D. Distribution and possible role of perinuclear theca proteins during bovine spermiogenesis. Micro Res Tech 1995;32:520–32.CrossRefGoogle Scholar
  54. 54.
    Calvin HI. Isolation and subfractionation of mammalian sperm heads and tails. In: Prescott DM, ed. Methods in cell biology. New York: Academic Press, 1976;13:85–104.Google Scholar
  55. 55.
    Kuhn R, Schäfer U, Schäfer M. Cis-acting regions sufficient for spermatocyte-specific transcriptional and spermatid-specific translational control of the Drosophila melanogaster gene Mst(3) gl-9. EMBO J 1988;7:447–54.PubMedGoogle Scholar
  56. 56.
    Higgy NA, Pastoor T, Renz C, Tarnasky HA, Van Der Hoorn FA. Testis-specific RT7 protein localizes to the sperm tail and associates with itself. Biol Reprod 1994;50:1357–66.PubMedCrossRefGoogle Scholar
  57. 57.
    Schafer M, Borsch D, Hülster A, Schäfer U. Expression of a gene duplication encoding conserved sperm tail proteins is translationally regulated in Drosophila melanogaster. Mol Cell Biol 1993;13:1708–18.PubMedGoogle Scholar
  58. 58.
    Oko R, Clermont Y. Light microscopic immunocytochemical study of fibrous sheath and outer dense fiber formation in the rat spermatid. Anat Rec 1989;225:46–55.PubMedCrossRefGoogle Scholar
  59. 59.
    Monesi V. Synthetic activity during spermatogenesis in the mouse. RNA and protein synthesis. Exp Cell Res 1965;39:197–224.PubMedCrossRefGoogle Scholar
  60. 60.
    Clermont Y, Oko R, Hermo L. Immunocytochemical study of fibrous sheath and outer dense fiber formation in the rat spermatid. Anat Rec 1990;225:46–55.Google Scholar
  61. 61.
    Oko R, Clermont Y. Biogenesis of specialized cytoskeletal elements of rat spermatozoa. Ann NY Acad Sci USA 1991;637:203–23.CrossRefGoogle Scholar
  62. 62.
    Calvin HI, Bedford JM. Formation of disulfide bonds in the nucleus and accessory structures of mammalian spermatozoa during maturation in the epididymis. J Reprod Fertil 1971;Suppl 13:65–75.Google Scholar
  63. 63.
    Brito M, Figueroa J, Maldonado EU, Vera JC, Burzio LO. The major component of rat sperm fibrous sheath is a phosphoprotein. Gamete Res 1989;22:205–18.PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag New York, Inc. 1996

Authors and Affiliations

  • Richard J. Oko
  • Carlos R. Morales

There are no affiliations available

Personalised recommendations