Nature's ingenuity: Bypassing the classical secretory route via apocrine secretion

Molecular Reproduction and Development

Volumn 63, Issue 3, 2002, Pages 394-410

  Hermo, Louis ^a   Jacks, Duncan ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

Apical blebs; Epididymis; Immunocytochemistry; Principal cells; Vas deferens

Indexed keywords

GLUTATHIONE TRANSFERASE; UBIQUITIN;

ANIMAL CELL; ANIMAL TISSUE; APICAL MEMBRANE; APOCRINE GLAND; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; EPIDIDYMIS; FERTILITY; IMMUNOCYTOCHEMISTRY; MALE; MALE GENITAL SYSTEM; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SPERMATOZOON MATURATION; VAS DEFERENS;

ANIMALS; EPIDIDYMIS; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICROSCOPY, ELECTRON; VAS DEFERENS;

EID: 0036836540     PISSN: 1040452X     EISSN: None     Source Type: Journal    
DOI: 10.1002/mrd.90023     Document Type: Article

References (71)

1. Agrawal Y, Vanha-Perttula T. 1988. Electron microscopic study of the secretion process in bovine reproductive organs. J Androl 9:307-316.
2. Aitken RJ. 2002. Active oxygen in spermatozoa during epididymal transit. In: Robaire B, Hinton B, editors. The epididymis, from molecules to clinical practice. New York: Kluwer Academic/Plenum Publishers. pp 435-447.
3. Alvarez JG, Storey BT. 1989. Role of glutathione peroxidase in protecting mammalian spermatozoa from loss of motility caused by spontaneous lipid peroxidation. Gamete Res 23:77-90.
4. Andonian S, Hermo L. 1999a. Principal cells of the vas deferens are involved in water transport and steroid synthesis in the adult rat. J Androl 20:158-176.
5. Andonian S, Hermo L. 1999b. Immunocytochemical localization of the Ya, Yb1, Yc, Yf, and Yo subunits of glutathione S-transferases in the cauda epididymidis and vas deferens of adult rats. J Androl 20:145-157.
6. Aumuller G, Seitz J. 1990. Protein secretion and secretory processes in male accessory sex glands. Int Rev Cytol 121:127-231.
7. Aumuller G, Renneberg H, Schiemann PJ, Wilhelm B, Seitz J, Konrad L, Wennemuth G. 1997. The role of apocrine released proteins in the post-testicular regulation of human sperm function. Adv Exp Med Biol 424:193-219.
8. Aumuller G, Wilhelm B, Seitz J. 1999. Apocrine secretion-Fact or artifact? Ann Anat 181:437-446.
9. Bartlett RJ, French FS, Wilson EM. 1984. In vitro synthesis and glycosylation of androgen-dependent secretory proteins of rat dorsal prostate and coagulating gland. Prostate 5:75-91.
10. 5-3-ketosteroid isomerase and the glutathione S-transferases of the liver. Proc Natl Acad Sci USA 74:158-162.
11. Brandes D. 1966. The fine structure and histochemistry of prostatic glands in relation to sex hormones. In: Bourne GH, Danielli JF, editors. Int Rev Cyt. Vol. 20, New York: Academic Press. pp 207-276.
12. Castellon EA, Balbontin JB. 2000. Secretion of glycosidases in human epididymal cell cultures. Arch Androl 45:35-42.
13. Cooper TG. 1986. The epididymis, sperm maturation and fertilization. Berlin: Springer-Verlag. p 117-230.
14. Cooper TG. 1998. Interactions between epididymal secretions and spermatozoa. J Reprod Fertil 53:119-136.
15. Dacheux J-L, Dacheux F. 2002. Protein secretion in the epididymis. In: Robaire B, Hinton B, editors. The epididymis, from molecules to clinical practice. New York: Kluwer Academic/Plenum Publishers. pp 151-168.
16. Daniel V. 1993. Glutathione S-transferases: Gene structure and regulation of expression. Crit Rev Biochem Mol Biol 28:173-207.
17. Djakiew D, Cardullo R. 1986. Lower temperature of the cauda epididymidis facilitates the storage of sperm by enhancing oxygen availability. Gamete Res 15:237-245.
18. Flickinger CJ. 1973. Regional variations in endoplasmic reticulum in the vas deferens of normal and vasectomized rats. Anat Rec 176: 205-224.
19. Flickinger CJ. 1981. Regional differences in synthesis, intracellular transport, and secretion of protein in the mouse epididymis. Biol Reprod 25:871-883.
20. Fornes WM, Sosa MA, Bertini F, Burgos MH. 1995. Vesicles in rat epididymal fluid. Existence of two populations differing in ultra-structure and enzymatic composition. Andrologia 27:233-237.
21. Fraile B, Martin R, De Miguel MP, Arenas MI, Bethencourt FR, Peinado F, Paniagua R, Santamaria L. 1996. Light and electron microscopic immunohistochemical localization of protein gene product 9.5 and ubiquitin immunoreactivities in the human epididymis and vas deferens. Biol Reprod 55:291-297.
22. Fried V, Smith HT, Hildbrandt E, Weiner K. 1987. Ubiquitin has proteolytic activity: Implication for cellular regulation. Proc Natl Acad Sci USA 84:3685-3689.
23. Goyal HO. 1985. Morphology of the bovine epididymis. Am J Anat 172:155-172.
24. Grimalt P, Bertini F, Fornes MW. 2000. High-affinity sites for beta-D-galactosidase on membrane-bound vesicles isolated from rat epididymal fluid. Arch Androl 44:85-91.
25. Groos S, Wilhelm B, Renneberg H, Rive A, Reichelt R, Seitz J, Aumuller G. 1999. Simultaneous apocrine and merocrine secretion in the rat coagulating gland. Cell Tissue Res 295:495-504.
26. Hamilton DW. 1971. Steroid function in the mammalian epididymis. J Reprod Fertil Suppl 13:89-97.
27. Hamilton DW. 1975. Structure and function of the epithelium lining the ductuli efferentes, ductus epididymis, and ductus deferens in the rat. In: Greep RO, Astwood EB, editors. Handbook of physiology. Section 7. Vol. 5, Washington DC: American Physiological Society. pp 303-317.
28. Hayes JD. 1988. Selective elution of rodent glutathione S-transferases and glyoxalase I from the S-hexylglutathione-Sepharose affinity matrix. Biochem J 255:913-922.
29. Hayes JD, Mantle TJ. 1986. Use of immuno-blot techniques to discriminate between the glutathione S-transferase Yf, Yk, Ya, Yn/Yb, and Yc subunits and to study their distribution in extrahepatic tissues. Biochem J 233:779-788.
30. Hermo L, Robaire B. 2002. Epididymal cell types and their functions. In: Robaire B, Hinton B, editors. The epididymis, from molecules to clinical practice. New York: Kluwer Academic/Plenum Publishers. pp 81-102.
31. Hermo L, Dworkin J, Oko R. 1988. Role of epithelial clear cells of the rat epididymis in the disposal of the contents of cytoplasmic droplets detached from spermatozoa. Am J Anat 183:107-124.
32. Hermo L, Oko R, Morales CR. 1994. Secretion and endocytosis in the male reproductive tract: A role in sperm maturation. Int Rev Cytol 154:105-189.
33. Hermo L, Badran H, Andonian S. 2002. The structural organization and functions of the epithelium of the vas deferens. In: Robaire B, Hinton B, editors. The epididymis, from molecules to clinical practice. New York: Kluwer Academic/Plenum Publishers. pp 233-250.
34. Hershko A, Eytan E, Ciechanover A, Hass AL. 1982. Immunochemical analysis of the turnover of ubiquitin-protein conjugates in intact cells. Relationship to the breakdown of abnormal proteins. J Biol Chem 257:13964-13970.
35. Hess RA. 2002. The efferent ductules: Structure and functions. In: Robaire B, Hinton B, editors. The epididymis, from molecules to clinical practice. New York: Kluwer Academic/Plenum Publishers. pp 49-80.
36. Hess RA, Thurston RJ, Biellier HV. 1976. Morphology of the epididymal region and ductus deferens of the turkey (Meleagris gallopavo). J Anat 122:241-252.
37. Hinton BT, Palladino MA, Rudolph DB, Labus JC. 1995. The epididymis as protector of maturing spermatozoa. Reprod Fertil Dev 7:731-745.
38. Karnovsky MJ. 1971. Use of ferrocyanide-reduced osmium tetroxide in electron microscopy (Abstract). 284:146.
39. Kelly RB. 1985. Pathways of protein secretion in eukaryotes. Science 230:25-32.
40. Ketterer B, Fraser G, Meyer DJ. 1990. Nuclear glutathione transferases which detoxify irradiated DNA. Adv Exp Med Biol 264:301-310.
41. Kirchhoff C. 1999. Gene expression in the epididymis. Int Rev Cytol 188:133-202.
42. Lippert TH, Seeger H, Schieferstein G, Voelter W. 1993. Immunoreactive ubiquitin in human seminal plasma. J Androl 14:130-131.
43. Luu-Thé V, Lachance Y, Labrie C, Leblanc G, Thomas JL, Strickler RC, Labrie F. 1989. Full length cDNA structure and deduced amino acid sequence of human 3β-hydroxy-5-ene steroid dehydrogenase. Mol Endocrinol 3:1310-1312.
44. Ma T, Yang B, Kuo WL, Verkman AS. 1996. cDNA cloning and gene structure of a novel water channel expressed exclusively in human kidney: Evidence for a gene cluster of aquaporins at chromosome locus 12q13. Genomics 35:543-550.
45. Manin M, Lecher P, Martinez A, Tournadre S, Jean C. 1995. Exportation of mouse vas deferens protein, a protein without a signal peptide, from mouse vas deferens epithelium: A model of apocrine secretion. Biol Reprod 52:50-62.
46. Martin R, Santamaria L, Fraile B, Paniagua R, Polak JM. 1995. Ultrastructural localization of PGP 9.5 and ubiquitin immunoreactivities in rat ductus epididymis epithelium. Histochem J 27:431-439.
47. Morales A, Cavicchia JC. 1991. Release of cytoplasmic apical protrusions from principal cells of the cat epididymis, an electron microscopic study. Tissue Cell 23:505-513.
48. Niemi M. 1965. The fine structure and histochemistry of the epithelial cells of the rat vas deferens. Acta Anat 60:207-219.
49. Oko R, Clermont Y. 1988. Isolation, structure, and protein composition of the perforatorium of rat spermatozoa. Biol Reprod 39:673-687.
50. Oko R, Clermont Y. 1989. Light immunocytochemical study of fibrous sheath and outer dense fiber formation in the rat spermatid. Anat Rec 225:46-55.
51. Oko R, Hermo L, Chan PTK, Fazel A, Bergeron JJM. 1993. The cytoplasmic droplet of rat epididymal spermatozoa contains saccular elements with Golgi characteristics. J Cell Biol 123:809-821.
52. Papp S, Robaire B, Hermo L. 1995. Immunocytochemical localization of the Ya, Yc, Yb1, andYb2 subunits of glutathione S-transferases in the testis and epididymis of adult rats. Micros Res Tech 30:1-23.
53. Piomboni P. 1997. Microanatomy of the epididymis and vas deferens. J Submicrosc Cytol Pathol 29:583-593.
54. Renneberg H, Konrad L, Aumuller G. 1995. Immunohistochemistry of secretory particles ('vesiculosomes') from the epithelium of bovine seminal vesicles and ampulla of the vas deferens. Acta Anat 153: 273-281.
55. Renneberg H, Albrecht M, Kurek R, Krause E, Lottspeich F, Aumuller G, Wilhelm B. 2001. Identification and characterization of neutral endopeptidase (EC 3. 4. 24. 11) from human prostasomes-localization in prostatic tissue and cell lines. Prostate 46:173-183.
56. Robaire B, Hermo L. 1988. Efferent ducts, epididymis, and vas deferens: Structure, functions, and their regulation. In: Knobil E, Neill J, editors. The physiology of reproduction. New York: Raven Press. pp 999-1080.
57. Santamaria L, Martin R, Paniagua R, Fraile B, Nistal M, Terenghi G, Polak JM. 1993. Protein gene product 9.5 and ubiquitin immunoreactivities in rat epididymis epithelium. Histochemistry 100:131-138.
58. Seitz J, Keppler C, Rausch U, Aumuller G. 1990. Immunohistochemistry of secretory transglutaminase from rodent prostate. Histochemistry 93:525-530.
59. Skudlarek MD, Orgebin-Crist M-C. 1986. Glycosidases in cultured rat epididymal cells: Enzyme activity, synthesis, and secretion. Biol Reprod 35:167-178.
60. Smithwick EB, Young LG. 1997. Sequential histology of the adult chimpanzee epididymis. Tissue Cell 29:383-412.
61. Sonnenberg-Riethmacher E, Walter B, Riethmacher D, Godecke S, Birchmeier C. 1996. The c-ros tyrosine kinase receptor controls regionalization and differentiation of epithelial cells in the epididymis. Gene Dev 10:1184-1193.
62. Steinhoff M, Eicheler W, Holterhus PM, Rausch U, Seitz J, Aumuller G. 1994. Hormonally induced changes in apocrine secretion oftransglutaminase in the rat dorsal prostate and coagulating gland. Eur J Cell Biol 65:49-59.
63. Sutovsky P, Moreno R, Ramalho-Santos J, Dominko T, Thompson WE, Schatten G. 2001. A putative, ubiquitin-dependent mechanism for the recognition and elimination of defective spermatozoa in the mammalian epididymis. J Cell Sci 114:1665-1675.
64. Tulsiani DR, Skudlarek MD, Araki Y, Orgebin-Crist MC. 1995. Purification and characterization of two forms of beta-D-galactosidase from rat epididymal luminal fluid: Evidence for their role in the modification of sperm plasma membrane glycoprotein(s). Biochem J 305:41-50.
65. Tulsiani DR, Orgebin-Crist MC, Skudlarek MD. 1998. Role of luminal fluid glycosyltransferases and glycosidases in the modification of rat sperm plasma membrane glycoproteins during epididymal maturation. J Reprod Fertil Suppl 53:85-97.
66. Veri JP, Hermo L, Robaire B. 1993. Immunocytochemical localization of the Yf subunit of glutathione S-transferase P shows regional variation in the staining of epithelial cells of the testis, efferent ducts, and epididymis of the male rat. J Androl 14:23-44.
67. Veri JP, Hermo L, Robaire B. 1994. Immunocytochemical localization of the glutathione S-transferase Yo subunit in the rat testis and epididymis. J Androl 15:415-434.
68. Wilhelm B, Keppler C, Hoffbauer G, Lottspeich F, Linder D, Meinhardt A, Aumuller G, Seitz J. 1998. Cytoplasmic carbonic anhydrase II of rat coagulating gland is secreted via the apocrine export mode. J Histochem Cytochem 46:505-511.
69. Wing S, Bedard N, Morales C, Hingcamp P, Trasler J. 1996. A novel rat homolog of the saccharomyces cerevisiae ubiquitin conjugating enzymes UBC4 and UBC5 with distinct biochemical features is induced during spermatogenesis. Mol Cell Biol 16:4064-4072.
70. Yanagimachi R, Kamiguchi Y, Mikamo K, Suzuki F, Yanagimachi H. 1985. Maturation of spermatozoa in the epididymis of the Chinese hamster. Am J Anat 172:317-330.
71. Yeung CH, Cooper TG. 2002. Acquisition and development of sperm motility upon maturation in the epididymis. In: Robaire B, Hinton B, editors. The epididymis, from molecules to clinical practice. New York: Kluwer Academic/Plenum Publishers. pp 417-434.