Structural alterations of epididymal epithelial cells in cathepsin A-deficient mice affect the blood-epididymal barrier and lead to altered sperm motility

Journal of Andrology

Volumn 28, Issue 5, 2007, Pages 784-797

  Hermo, Louis ^a   Korah, Nadine ^a   Gregory, Mary ^b   Liu, Lauren Ye ^a   Cyr, Daniel G ^a,b   D'Azzo, Alessandra ^c   Smith, Charles E ^d  

^a MCGILL UNIVERSITY   (Canada)

^b INRS INSTITUT ARMAND FRAPPIER   (Canada)

^c ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^d UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Claudins; Epididymis; Lanthanum nitrate; Principal cells; Sperm counts

Indexed keywords

CARBOXYPEPTIDASE C; CLAUDIN; CLAUDIN 1; CLAUDIN 10; CLAUDIN 3; CLAUDIN 8; LANTHANUM; LANTHANUM NITRATE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD; CELL STRUCTURE; CELL TYPE; COMPUTER ANALYSIS; CONTROLLED STUDY; CYTOPLASM; ENZYME DEFICIENCY; EPIDIDYMIS; EPITHELIUM; EPITHELIUM CELL; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SEMEN ANALYSIS; SPERMATOZOON COUNT; SPERMATOZOON MOTILITY; TIGHT JUNCTION;

ANIMALS; CARBOXYPEPTIDASE C; EPIDIDYMIS; EPITHELIAL CELLS; IMMUNOHISTOCHEMISTRY; LANTHANUM; MALE; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; SPERM MOTILITY; TIGHT JUNCTIONS;

EID: 34548641765     PISSN: 01963635     EISSN: None     Source Type: Journal    
DOI: 10.2164/jandrol.107.002980     Document Type: Article

References (49)

1. Blandau RJ, Rumery RE. The relationship of swimming movements of epididymal spermatozoa to their fertilizing capacity. Fertil Steril. 1964;15:571-579.
2. Breton S. Luminal acidification in the epididymis and vas deferens. In: Hinton BT, Turner TT, eds. Third International Conference on the Epididymis. Charlottesville, Va: Van Doren; 2003:60-72.
3. Colegio OR, Van Itallie CM, McCrea HJ, Rahner C, Anderson JM. Claudins create charge-selective channels in the paracellular pathway between epithelial cells. Am J Physiol Cell Physiol. 2002;283:C142-C147.
4. Cooper TG, Wagenfeld A, Cornwall GA, Hsia N, Chu ST, Orgebin-Crist M-C, Drevet J, Vernet P, Avram C, Nieschlag E, Yeung CH. Gene and protein expression in the epididymis of infertile c-ros receptor tyrosine kinase-deficient mice. Biol Reprod. 2003;69:1750-1762.
5. Cornwall GA, Lareyre J-J, Matusik RJ, Hinton BT, Orgebin-Crist M-C. Gene expression and epididymal function. In: Robaire B, Hinton BT, eds. The Epididymis. From Molecules to Clinical Practice. New York, NY: Kluwer Academic/Plenum Publishers; 2002:169-199.
6. Cornwall GA, Smyth TB, Vindivich D, Harter C, Robinson J, Chang TSK. Induction and enhancement of progressive motility in hamster epididymis. Biol Reprod. 1986;35:1065-1074.
7. Cyr DG, Finnson K, Dugresne J, Gregory M. Cellular interactions and the blood epididymal barrier. In: Robaire B, Hinton BT, eds. The Epididymis, From Molecules to Clinical Practice. New York, NY: Kluwer Academic/Plenum Publishers; 2002:103-118.
8. Cyr DG, Hermo L, Egenberger N, Mertineit C, Trasler J, Laird D. Cellular immunolocalization of occludin during embryonic and postnatal development of the mouse testis and epididymis. Endocrinology. 1999;140:3815-3825.
9. d'Azzo A, Andria G, Strisciuglio P, Galjaard H. Galactosialidosis. In: Scriver C, Beaudet A, Sly W, Valle D, eds. The Metabolic and Molecular Bases of Inherited Disease. Vol 2, 7th ed. New York, NY: McGraw-Hill Publishing Co; 1995:2825-2837.
10. d'Azzo A, Hoogeveen A, Reuser AJ, Robinson D, Galjaard H. Molecular defect in combined P-galactosidase and neuraminidase deficiency in man. Proc Natl Acad Sci U S A. 1982;79:4535-4539.
11. Furuse M, Fujita K, Hiiragi T, Fujimoto K, Tsukita S. Claudin-1 and-2: novel integral membrane proteins localizing at tight junctions with no sequence similarity to occludin. J Cell Biol. 1998;141:1539-1550.
12. Furuse M, Furuse K, Sasaki H, Tsukita S. Conversion of zonulae occludentes from tight to leaky strand type by introducing claudin-2 into Madin-Darby canine kidney I cells. J Cell Biol. 2001;153:263-272.
13. Galjart NJ, Morreau H, Willemsen R, Gillemans N, Bonten EJ, d'Azzo A. Human lysosomal protective protein has cathepsin A-like activity distinct from its protective function. J Biol Chem. 1991;266:14754-14762.
14. Gregory M, Cyr DG. Identification of multiple claudins in the rat epididymis. Mol Reprod Dev. 2006;73:580-588.
15. Gregory M, Dufresne J, Hermo L, Cyr D. Claudin-1 is not restricted to tight junctions in the rat epididymis. Endocrinology. 2001;142:854-863.
16. Guan X, Inai T, Shibata Y. Segment-specific expression of tight junction proteins, claudin-2 and -10, in the rat epididymal epithelium. Arch Histol Cytol. 2005;68:213-225.
17. Hamilton DW. Structure and function of the epithelium lining the ductuli efferentes, ductus epididymidis and ductus deferens in the rat. In: Greep RO, Astwood EB, eds. Handbook of Physiology. Vol 5. Washington, DC: American Physiological Society; 1975:259-301.
18. Hanna WL, Turbov JM, Jackman HL, Tan F, Froelich CJ. Dominant chymotrypsin-like esterase activity in human lymphocyte granules is mediated by the serine carboxypeptidase called cathepsin A-like protective. J Immunol. 1994;153:4663-4672.
19. Hermo L, Green H, Clermont Y. Golgi apparatus of epithelial principal cells of the epididymal initial segment of the rat: structure, relationship with endoplasmic reticulum, and role in the formation of secretory vesicles. Anat Rec. 1991b;229:159-176.
20. Hermo L, Robaire B. Epididymal cell types and their functions. In: Robaire B, Hinton BT, eds. The Epididymis, From Molecules to Clinical Practice. New York, NY: Kluwer Academic/Plenum Publishers; 2002:81-102.
21. Hermo L, Wright J, Oko R, Morales CR. Role of epithelial cells of the male excurrent duct system of the rat in the endocytosis or secretion of sulfated glycoprotein-2 (clusterin). Biol Reprod. 1991a;44:1113-1131.
22. Hess RA. The efferent ductules: structure and functions. In: Robaire B, Hinton BT, eds. The Epididymis, From Molecules to Clinical Practice. New York, NY: Kluwer Academic/Plenum Publishers; 2002:49-80.
23. Hinton BT, Dott HM, Setchell BP. Measurement of the motility of rat spermatozoa collected by micropuncture from the testis and from different regions along the epididymis. J Reprod Fertil. 1979;55:167-172.
24. Itoh K, Kase R, Shimmoto M, Satake A, Sakuraba H, Suzuki Y. Protective protein as an endogenous endothelin degradation enzyme in human tissues. J Biol Chem. 1995;270:515-518.
25. Jackman HL, Morris PW, Deddish PA, Skedgel RA, Erdos EG. Inactivation of endothelin I by deamidase (lysosomal protective protein). J Biol Chem. 1992;267:2872-2875.
26. Karnovsky MJ. Use of ferrocyanide-reduced osmium tetroxide in electron microscopy (abstract). In: Proceedings of the 11th American Society of Cell Biology. New Orleans, La: American Society of Cell Biology; 1971;284:146.
27. Korah N, Smith CE, d'Azzo A, El-Alfy M, Hermo L. An increase in macrophages in the testis of cathepsin A deficient mice suggest an important role for these cells in the interstitial space of this tissue. Mol Reprod Dev. 2003a;64:302-320.
28. Korah N, Smith CE, d'Azzo A, Mui J, Hermo L. Characterization of cell- and region-specific abnormalities in the epididymis of cathepsin A deficient mice. Mol Reprod Dev. 2003b;66:358-373.
29. Morita K, Furuse M, Fujimoto K, Tsukita S. Claudin multigene family encoding four-transmembrane domain protein components of tight junction strands. Proc Natl Acad Sci U S A. 1999;96:511-516.
30. Morton B, Harrigan-Lum J, Albagi L, Jooss T. The activation of motility in quiescent hamster sperm from the epididymis by calcium and cyclic nucleotides. Biochem Biophys Res Commun. 1974;56:372-379.
31. Orgebin-Crist M-C, Danzo BJ, Davies J. Endocrine control of the development and maintenance of sperm fertilizing ability in the epididymis. In: Greep RO, Astwood EB, eds. Handbook of Physiology. Vol 5. Washington, DC: American Physiological Society; 1975:319-338.
32. Orgebin-Crist M-C, Olson GE. Epididymal sperm maturation. In: The Male in Farm Animal Reproduction, Courot M ed., Amsterdam, The Netherlands: Martinus Nijhoff; 1984:80-102.
33. Pholpramool C, Chaturapanich G. Effect of sodium and potassium concentrations and pH in the maintenance of motility of rabbit and rat epididymal spermatozoa. J Reprod Fertil. 1979;7:245-251.
34. Robaire B, Hermo L. Efferent ducts, epididymis, and vas deferens: structure, functions, and their regulation. In: Knobil E, Neill JD, eds. The Physiology of Reproduction. New York, NY: Raven Press; 1988:999-1080.
35. Robaire B, Hinton BT, Orgebin-Crist MC. The epididymis. In: Knobil E, Neill JD, eds. Physiology of Reproduction. 3rd ed. New York, NY: Academic Press; 2006:1071-1147.
36. Rottier RJ, Hahn CN, Mann LW, del Pilar Martin M, Smeyne RJ, Suzuki K, d'Azzo A. Lack of PPCA expression only partially coincides with lysosomal storage in galactosialidosis mice: indirect evidence for spatial requirement of the catalytic rather than the protective function of PPCA. Hum Mol Genet. 1998;7:1787-1794.
37. Ruz R, Gregory M, Smith CE, Cyr DG, Lubahn DB, Hess RA, Hermo L. Expression of aquaporins in the efferent ductules, sperm counts, and sperm motility in estrogen receptor-α deficient mice fed lab chow versus casein. Mol Reprod Dev. 2006;73:226-237.
38. Sohma O, Mizuguchi M, Takashima S, Satake A, Itoh K, Sakuraba H, Suzuki Y, Oyanagi K. Expression of protective protein in human tissue. Pediatr Neurol. 1999;20:210-214.
39. Soler C, Yeung CH, Cooper TG. Development of sperm motility patterns in the murine epididymis. Int J Androl. 1994;17:271-278.
40. Sonoda N, Furuse M, Sasaki H, Yonemura S, Katahira J, Horiguchi Y, Tsukita S. Clostridium perfringens enterotoxin fragment removes specific claudins from tight junction strands: evidence for direct involvement of claudins in tight junction barrier. J Cell Biol. 1999;147:195-204.
41. Tsukita S, Furuse M. Pores in the wall: claudins constitute tight junction strands containing aqueous pores. J Cell Biol. 2000;149:13-16.
42. Turner TT, Howards SS. Factors involved in the initiation of sperm motility. Biol Reprod. 1978;18:571-578.
43. van der Spoel A, Bonten E, d'Azzo A. Transport of human lysosomal neuraminidase to mature lysosomes requires protective protein/cathepsin A. EMBO J. 1998;17:1588-1597.
44. van Itallie CM, Anderson JM. Claudins and epithelial paracellular transport. Annu Rev Physiol. 2006;68:403-429.
45. van Itallie CM, Fanning AS, Anderson JM. Reversal of charge selectivity in cation or anion-selective epithelial lines by expression of different claudins. Am J Physiol Renal Physiol. 2003;285:F1078-F1084.
46. van Pelt J, van Bilsen DG, Kamerling JP, Vliegenthart JF. Structural analysis of O-glycosidic type of sialyloligosaccharide-alditols derived from urinary glycopeptides of a sialidosis patient. Eur J Biochem. 1988;174:183-187.
47. Wong PYD, Lee WM, Tsang AYF. The effects of sodium and amiloride on the motility of caudal epididymal spermatozoa of the rat. Experientia. 1981;37:69-71.
48. Zhou XY, Morreau H, Rottier R, Davis D, Bonten E, Gillemans N, Wenger D, Grosveld FG, Doherty P, Susuki K, Grosveld GC, d'Azzo A. Mouse model for the lysosomal disorder galactosialidosis and correction of the phenotype with overexpressing erythroid precursor cells. Genes Dev. 1995;9:2623-2634.
49. Zhou XY, van der Spoel A, Rottier R, Hale G, Willemsen R, Berry GT, Strisciuglio P, Andria G, d'Azzo A. Molecular and biochemical analysis of protective protein/cathepsin A mutations: correlation with clinical severity in galactosialidosis. Hum Mol Genet. 1996;5:1977-1987.