Epididymis cholesterol homeostasis and sperm fertilizing ability

Asian Journal of Andrology

Volumn 13, Issue 1, 2011, Pages 11-17

  Saez, Fabrice ^a   Ouvrier, Aurélia ^a   Drevet, Joël R ^a  

^a Faculté de Médecine   (France)

Author keywords

cholesterol homeostasis; epididymosomes; fertility; post testicular maturation; spermatozoa

Indexed keywords

APOLIPOPROTEIN; CHOLESTEROL; DESMOSTEROL;

CHOLESTEROL METABOLISM; CHOLESTEROL SYNTHESIS; EPIDIDYMIS; FERTILIZATION; HOMEOSTASIS AND REGULATION; HUMAN; NONHUMAN; REVIEW; SPERM; SPERMATOZOON MATURATION;

ANIMALS; CHOLESTEROL; EPIDIDYMIS; FEMALE; FERTILIZATION; HOMEOSTASIS; HUMANS; MALE; SPERM MATURATION; SPERM MOTILITY; SPERMATOZOA;

EID: 78650990744     PISSN: 1008682X     EISSN: 17457262     Source Type: Journal    
DOI: 10.1038/aja.2010.64     Document Type: Review

References (96)

1. Davis BK, Byrne R, Hungund B. Studies on the mechanism of capacitation. II. Evidence for lipid transfer between plasma membrane of rat sperm and serum albumin during capacitation in vitro. Biochim Biophys Acta 1979; 558: 257-66.
2. Abou-haila A, Tulsiani DR. Signal transduction pathways that regulate sperm capacitation and the acrosome reaction. Arch Biochem Biophys 2009; 485: 72-81.
3. Hamilton DW, Jones AL, Fawcett DW. Cholesterol biosynthesis in the mouse epididymis and ductus deferens: a biochemical and morphological study. Biol Reprod 1969; 1: 167-84.
4. Evans RR, Johnson AD. The metabolic activity of the bovine epididymis. III. Cholesterol and esterified cholesterol metabolism. J Reprod Fertil 1975; 43: 527-30.
5. Johnston DS, Jelinsky SA, Bang HJ, DiCandeloro P, Wilson E et al. The mouse epididymal transcriptome: transcriptional profiling of segmental gene expression in the epididymis. Biol Reprod 2005; 73: 404-13.
6. Inano H, Machino A, Tamaoki B. In vitro metabolism of steroid hormones by cell-free homogenates of epididymides of adult rats. Endocrinology 1969; 84: 997-1003.
7. Gloyna RE, Wilson JD. A comparative study of the conversion of testosterone to 17- beta-hydroxy-5-alpha-androstan-3-one (Dihydrotestosterone) by prostate and epididymis. J Clin Endocrinol Metab 1969; 29: 970-7.
8. Djoseland O, Hansson V, Haugen HN. Androgen metabolism by rat epididymis. 1. Metabolic conversion of 3H-testosterone in vivo. Steroids 1973; 21: 773-83.
9. Kumari GL, Allag IS, Das RP, Datta JK. Regional differences in steroidogenesis and hormone levels in the epididymis and vas deferens of adult rats. Int J Androl 1980; 3: 267-81.
10. Wiszniewska B. Steroidogenic characteristics of in vitro cultured epididymal epithelial cells of the rat. Reprod Biol 2001; 1: 60-6.
11. Amann RP, Marengo SR, Brown DV. Steroidogenesis and testosterone metabolism in cultured principal cells from the ram epididymis. J Androl 1987; 8: 238-46.
12. Simard J, Melner MH, Breton N, Low KG, Zhao HF et al. Characterization of macaque 3 beta-hydroxy-5-ene steroid dehydrogenase/delta 5-delta 4 isomerase: structure and expression in steroidogenic and peripheral tissues in primate. Mol Cell Endocrinol 1991; 75: 101-10.
13. Jean-Faucher C, Berger M, Gallon C, de Turckheim M, Veyssiere G et al. Regional differences in the testosterone to dihydrotestosterone ratio in the epididymis and vas deferens of adult mice. J Reprod Fertil 1986; 76: 537-43.
14. Awider-Al-Amawi M, Marchlewicz M, Kolasa A, Wenda-Rozewicka L, Wiszniewska B. Rat epididymal epithelial cells and 17beta-estradiol synthesis under hCG stimulation in vitro. Folia Histochem Cytobiol 2007; 45: 255-63.
15. Swider-Al-Amawi M, Kolasa A, Sikorski A, Marchlewicz M, Baranowska-Bosiacka I et al. The immunoexpression of FSH-R in the ductuli efferentes and the epididymis of men and rat: effect of FSH on the morphology and steroidogenic activity of rat epididymal epithelial cells in vitro. J Biomed Biotechnol 2010; 2010: 506762.
16. Hess RA, Bunick D, Lubahn DB, Zhou Q, Bouma J. Morphologic changes in efferent ductules and epididymis in estrogen receptor-alpha knockout mice. J Androl 2000; 21: 107-21.
17. Turner TT, Jones CE, Howards SS, Ewing LL, Zegeye B et al. On the androgen microenvironment of maturing spermatozoa. Endocrinology 1984; 115: 1925-32.
18. Ganjam VK, Amann RP. Steroids in fluids and sperm entering and leaving the bovine epididymis, epididymal tissue, and accessory sex gland secretions. Endocrinology 1976; 99: 1618-30.
19. Turner TT. Necessitys potion: inorganic ions and small organic molecules in the epididymal lumen. In: Robaire B, Hinton BT, editors. The Epididymis: From Molecules to Clinical Practice. A Comprehensive Survey of the Efferent Ducts, the Epididymis and the Vas Deferens. New York: Kluwer Academic/Plenum Publishers; 2002. pp131-50.
20. Avram C, Yeung CH, Nieschlag E, Cooper TG. Regulation of the initial segment of the murine epididymis by dihydrotestosterone and testicular exocrine secretions studied by expression of specific proteins and gene expression. Cell Tissue Res 2004; 317: 13-22.
21. Ikonen E. Cellular cholesterol trafficking and compartmentalization. Nat Rev Mol Cell Biol 2008; 9: 125-38.
22. Chang TY, Chang CC, Ohgami N, Yamauchi Y. Cholesterol sensing, trafficking, and esterification. Annu Rev Cell Dev Biol 2006; 22: 129-57.
23. Baldan A, Tarr P, Lee R, Edwards PA. ATP-binding cassette transporter G1 and lipid homeostasis. Curr Opin Lipidol 2006; 17: 227-32.
24. Oram JF, Vaughan AM. ATP-binding cassette cholesterol transporters and cardiovascular disease. Circ Res 2006; 99: 1031-43.
25. Sporstol M, Mousavi SA, Eskild W, Roos N, Berg T. ABCA1, ABCG1 and SR-BI: hormonal regulation in primary rat hepatocytes and human cell lines. BMC Mol Biol 2007; 8: 5.
26. Tall AR, Yvan-Charvet L, Terasaka N, Pagler T, Wang N. HDL, ABC transporters, and cholesterol efflux: implications for the treatment of atherosclerosis. Cell Metab 2008; 7: 365-75.
27. Temel RE, Trigatti B, DeMattos RB, Azhar S, KriegerMet al. Scavenger receptor class B, type I (SR-BI) is the major route for the delivery of high density lipoprotein cholesterol to the steroidogenic pathway in cultured mouse adrenocortical cells. Proc Natl Acad Sci USA 1997; 94: 13600-5.
28. Landschulz KT, Pathak RK, Rigotti A, Krieger M, Hobbs HH. Regulation of scavenger receptor, class B, type I, a high density lipoprotein receptor, in liver and steroidogenic tissues of the rat. J Clin Invest 1996; 98: 984-95.
29. Kastner P, Mark M, Leid M, Gansmuller A, ChinWet al. Abnormal spermatogenesis in RXR beta mutant mice. Genes Dev 1996; 10: 80-92.
30. Robertson KM, Schuster GU, Steffensen KR, Hovatta O, Meaney S et al. The liver X receptor-beta is essential for maintaining cholesterol homeostasis in the testis. Endocrinology 2005; 146: 2519-30.
31. Selva DM, Hirsch-Reinshagen V, Burgess B, Zhou S, Chan J et al. The ATP-binding cassette transporter 1 mediates lipid efflux from Sertoli cells and influences male fertility. J Lipid Res 2004; 45: 1040-50.
32. Repa JJ, Turley SD, Lobaccaro JA, Medina J, Li L et al. Regulation of absorption and ABC1-mediated efflux of cholesterol by RXR heterodimers. Science 2000; 289: 1524-9.
33. Volle DH, Mouzat K, Duggavathi R, Siddeek B, Dechelotte P et al. Multiple roles of the nuclear receptors for oxysterols liver X receptor to maintain male fertility. Mol Endocrinol 2007; 21: 1014-27.
34. Frenoux JM, Vernet P, Volle DH, Britan A, Saez F et al. Nuclear oxysterol receptors, LXRs, are involved in the maintenance of mouse caput epididymidis structure and functions. J Mol Endocrinol 2004; 33: 361-75.
35. Saez F, Chabory E, Cadet R, Vernet P, Baron S et al. Liver X receptors and epididymal epithelium physiology. Asian J Androl 2007; 9: 574-82.
36. Ouvrier A, Cadet R, Vernet P, Laillet B, Chardigny JM et al. LXR and ABCA1 control cholesterol homeostasis in the proximal mouse epididymis in a cell-specific manner. J Lipid Res 2009; 50: 1766-75.
37. Vaughan AM, Oram JF. ABCA1 and ABCG1 or ABCG4 act sequentially to remove cellular cholesterol and generate cholesterol-rich HDL. J Lipid Res 2006; 47: 2433-43.
38. Morales CR, Marat AL, Ni X, Yu Y, Oko R et al. ATP-binding cassette transporters ABCA1, ABCA7, and ABCG1 in mouse spermatozoa. Biochem Biophys Res Commun 2008; 376: 472-7.
39. Ban N, Sasaki M, Sakai H, Ueda K, Inagaki N. Cloning of ABCA17, a novel rodent sperm-specific ABC (ATP-binding cassette) transporter that regulates intracellular lipid metabolism. Biochem J 2005; 389: 577-85.
40. Butler A, He X, Gordon RE, Wu HS, Gatt S et al. Reproductive pathology and sperm physiology in acid sphingomyelinase-deficient mice. Am J Pathol 2002; 161: 1061-75.
41. Andersen OM, Yeung CH, Vorum H, Wellner M, Andreassen TK et al. Essential role of the apolipoprotein E receptor-2 in sperm development. J Biol Chem 2003; 278: 23989-95.
42. Bailey RW, Aronow B, Harmony JA, Griswold MD. Heat shock-initiated apoptosis is accelerated and removal of damaged cells is delayed in the testis of clusterin/ApoJ knock-out mice. Biol Reprod 2002; 66: 1042-53.
43. Trigatti B, Rayburn H, Vinals M, Braun A, Miettinen H et al. Influence of the high density lipoprotein receptor SR-BI on reproductive and cardiovascular pathophysiology. Proc Natl Acad Sci USA 1999; 96: 9322-7.
44. Huang LS, Voyiaziakis E, Markenson DF, Sokol KA, Hayek T et al. apo B gene knockout in mice results in embryonic lethality in homozygotes and neural tube defects, male infertility, and reduced HDL cholesterol ester and apo A-I transport rates in heterozygotes. J Clin Invest 1995; 96: 2152-61.
45. Huang LS, Voyiaziakis E, Chen HL, Rubin EM, Gordon JW. A novel functional role for apolipoprotein B in male infertility in heterozygous apolipoprotein B knockout mice. Proc Natl Acad Sci USA 1996; 93: 10903-7.
46. Shalaby MA, el-Zorba HY, Kamel GM. Effect of alpha-tocopherol and simvastatin on male fertility in hypercholesterolemic rats. Pharmacol Res 2004; 50: 137-42.
47. Bataineh HN, Nusier MK. Effect of cholesterol diet on reproductive function in male albino rats. Saudi Med J 2005; 26: 398-404.
48. Ramirez-Torres MA, Carrera A, Zambrana M. High incidence of hyperestrogenemia and dyslipidemia in a group of infertile men. Ginecol Obstet Mex 2000; 68: 224-9. Spanish.
49. Kasturi SS, Tannir J, Brannigan RE. The metabolic syndrome and male infertility. J Androl 2008; 29: 251-9.
50. Parks JE, Hammerstedt RH. Development changes occurring in the lipids of ram epididymal spermatozoa plasma membrane. Biol Reprod 1985; 32: 653-68.
51. Aveldano MI, Rotstein NP, Vermouth NT. Lipid remodelling during epididymal maturation of rat spermatozoa. Enrichment in plasmenylcholines containing longchain polyenoic fatty acids of the n-9 series. Biochem J 1992; 283 (Pt 1): 235-41.
52. Awano M, Kawaguchi A, Mohri H. Lipid composition of hamster epididymal spermatozoa. J Reprod Fertil 1993; 99: 375-83.
53. Rejraji H, Sion B, Prensier G, Carreras M, Motta C et al. Lipid remodeling of murine epididymosomes and spermatozoa during epididymal maturation. Biol Reprod 2006; 74: 1104-13.
54. Rana AP, Majumder GC, Misra S, Ghosh A. Lipid changes of goat sperm plasma membrane during epididymal maturation. Biochim Biophys Acta 1991; 1061: 185-96.
55. Nikolopoulou M, Soucek DA, Vary JC. Changes in the lipid content of boar sperm plasma membranes during epididymal maturation. Biochim Biophys Acta 1985; 815: 486-98.
56. Haidl G, Opper C. Changes in lipids and membrane anisotropy in human spermatozoa during epididymal maturation. Hum Reprod 1997; 12: 2720-3.
57. Bleau G, VandenHeuvel WJ. Desmosteryl sulfate and desmosterol in hamster epididymal spermatozoa. Steroids 1974; 24: 549-56.
58. Wechsler A, Brafman A, Shafir M, Heverin M, Gottlieb H et al. Generation of viable cholesterol-free mice. Science 2003; 302: 2087.
59. Heverin M, Meaney S, Brafman A, Shafir M, Olin M et al. Studies on the cholesterolfree mouse: strong activation of LXR-regulated hepatic genes when replacing cholesterol with desmosterol. Arterioscler Thromb Vasc Biol 2007; 27: 2191-7.
60. Singh SK, Chakravarty S. Antispermatogenic and antifertility effects of 20,25- diazacholesterol dihydrochloride in mice. Reprod Toxicol 2003; 17: 37-44.
61. Lindenthal B, Aldaghlas TA, Kelleher JK, Henkel SM, Tolba R et al. Neutral sterols of rat epididymis. High concentrations of dehydrocholesterols in rat caput epididymidis. J Lipid Res 2001; 42: 1089-95.
62. Lin DS, Connor WE, Wolf DP, Neuringer M, Hachey DL. Unique lipids of primate spermatozoa: desmosterol and docosahexaenoic acid. J Lipid Res 1993; 34: 491-9.
63. Sion B, Grizard G, Boucher D. Quantitative analysis of desmosterol, cholesterol and cholesterol sulfate in semen by high-performance liquid chromatography. J Chromatogr A 2001; 935: 259-65.
64. Connor WE, Lin DS, Wolf DP, Alexander M. Uneven distribution of desmosterol and docosahexaenoic acid in the heads and tails of monkey sperm. J Lipid Res 1998; 39: 1404-11.
65. Cross NL. Effect of cholesterol and other sterols on human sperm acrosomal responsiveness. Mol Reprod Dev 1996; 45: 212-7.
66. Nimmo MR, Cross NL. Structural features of sterols required to inhibit human sperm capacitation. Biol Reprod 2003; 68: 1308-17.
67. Sugkraroek P, Kates M, Leader A, Tanphaichitr N. Levels of cholesterol and phospholipids in freshly ejaculated sperm and Percoll-gradient-pelletted sperm from fertile and unexplained infertile men. Fertil Steril 1991; 55: 820-7.
68. Zalata A, Hassan A, Christophe A, Comhaire F, Mostafa T. Cholesterol and desmosterol in two sperm populations separated on Sil-Select gradient. Int J Androl 2010; 33: 528-35.
69. Wathes DC, Abayasekara DR, Aitken RJ. Polyunsaturated fatty acids in male and female reproduction. Biol Reprod 2007; 77: 190-201.
70. Chabory E, Damon C, Lenoir A, Kauselmann G, Kern H et al. Epididymis selenoindependent glutathione peroxidase 5 maintains sperm DNA integrity in mice. J Clin Invest 2009; 119: 2074-85.
71. Aitken RJ. Gpx5 protects the family jewels. J Clin Invest 2009; 119: 1849-51.
72. Jones R. Plasma membrane composition and organisation during maturation of spermatozoa in the epididymis. In: Robaire B, Hinton BT, editors. The Epididymis: From Molecules to Clinical Practice. A Comprehensive Survey of the Efferent Ducts, the Epididymis and the Vas Deferens. New York: Kluwer Academic/Plenum Publishers; 2002. pp405-16.
73. Lin Y, Kan FW. Regionalization and redistribution of membrane phospholipids and cholesterol in mouse spermatozoa during in vitro capacitation. Biol Reprod 1996; 55: 1133-46.
74. James PS, Wolfe CA, Mackie A, Ladha S, PrenticeA et al. Lipid dynamics in the plasma membrane of fresh and cryopreserved human spermatozoa. Hum Reprod 1999; 14: 1827-32.
75. Christova Y, James PS, Cooper TG, Jones R. Lipid diffusion in the plasma membrane of mouse spermatozoa: changes during epididymal maturation, effects of pH, osmotic pressure, and knockout of the c-ros gene. J Androl 2002; 23: 384-92.
76. Christova Y, James P, Mackie A, Cooper TG, Jones R. Molecular diffusion in sperm plasma membranes during epididymal maturation. Mol Cell Endocrinol 2004; 216: 41-6.
77. Selvaraj V, Asano A, Buttke DE, McElwee JL, Nelson JL et al. Segregation of micronscale membrane sub-domains in live murine sperm. J Cell Physiol 2006; 206: 636-46.
78. Selvaraj V, Asano A, Buttke DE, Sengupta P, Weiss RS et al. Mechanisms underlying the micron-scale segregation of sterols and GM1 in live mammalian sperm. J Cell Physiol 2009; 218: 522-36.
79. Asano A, Selvaraj V, Buttke DE, Nelson JL, Green KM et al. Biochemical characterization of membrane fractions in murine sperm: identification of three distinct sub-types of membrane rafts. J Cell Physiol 2009; 218: 537-48.
80. Travis AJ, Kopf GS. The role of cholesterol efflux in regulating the fertilization potential of mammalian spermatozoa. J Clin Invest 2002; 110: 731-6.
81. Flesch FM, Gadella BM. Dynamics of the mammalian sperm plasma membrane in the process of fertilization. Biochim Biophys Acta 2000; 1469: 197-235.
82. Hermo L, Jacks D. Natures ingenuity: bypassing the classical secretory route via apocrine secretion. Mol Reprod Dev 2002; 63: 394-410.
83. Gliozzi TM, Zaniboni L, Maldjian A, Luzi F, Maertens L et al. Quality and lipid composition of spermatozoa in rabbits fed DHA and vitamin E rich diets. Theriogenology 2009; 71: 910-9.
84. Mitre R, Cheminade C, Allaume P, Legrand P, Legrand AB. Oral intake of shark liver oil modifies lipid composition and improves motility and velocity of boar sperm. Theriogenology 2004; 62: 1557-66.
85. Rooke JA, Shao CC, Speake BK. Effects of feeding tuna oil on the lipid composition of pig spermatozoa and in vitro characteristics of semen. Reproduction 2001; 121: 315-22.
86. Cerolini S, Zaniboni L, Maldjian A, Gliozzi T. Effect of docosahexaenoic acid and alpha-tocopherol enrichment in chicken sperm on semen quality, sperm lipid composition and susceptibility to peroxidation. Theriogenology 2006; 66: 877-86.
87. Aumuller G, Renneberg H, Schiemann PJ, Wilhelm B, Seitz J et al. The role of apocrine released proteins in the post-testicular regulation of human sperm function. Adv Exp Med Biol 1997; 424: 193-219.
88. Frenette G, Legare C, Saez F, Sullivan R. Macrophage migration inhibitory factor in the human epididymis and semen. Mol Hum Reprod 2005; 11: 575-82.
89. Gatti JL, Metayer S, Belghazi M, Dacheux F, Dacheux JL. Identification, proteomic profiling, and origin of ram epididymal fluid exosome-like vesicles. Biol Reprod 2005; 72: 1452-65.
90. FornesWM,Sosa MA, Bertini F, Burgos MH. Vesicles in rat epididymal fluid. Existence of two populations differing in ultrastructure and enzymatic composition. Andrologia 1995; 27: 233-7.
91. Yanagimachi R, Kamiguchi Y, Mikamo K, Suzuki F, Yanagimachi H. Maturation of spermatozoa in the epididymis of the Chinese hamster. Am J Anat 1985; 172: 317-30.
92. Frenette G, Sullivan R. Prostasome-like particles are involved in the transfer of P25b from the bovine epididymal fluid to the sperm surface. Mol Reprod Dev 2001; 59: 115-21.
93. Sullivan R, Frenette G, Girouard J. Epididymosomes are involved in the acquisition of new sperm proteins during epididymal transit. Asian J Androl 2007; 9: 483-91.
94. Girouard J, Frenette G, Sullivan R. Compartmentalization of proteins in epididymosomes coordinates the association of epididymal proteins with the different functional structures of bovine spermatozoa. Biol Reprod 2009; 80: 965-72.
95. Moskovtsev SI, Jarvi K, Legare C, Sullivan R, Mullen JB. Epididymal P34H protein deficiency in men evaluated for infertility. Fertil Steril 2007; 88: 1455-7.
96. Boue F, Sullivan R. Cases of human infertility are associated with the absence of P34H an epididymal sperm antigen. Biol Reprod 1996; 54: 1018-24.