ATP-binding cassette transporter G2 activity in the bovine spermatozoa is modulated along the epididymal duct and at ejaculation1

Biology of Reproduction

Volumn 86, Issue 6, 2012, Pages

  Caballero, Julieta ^a   Frenette, Gilles ^a   D'Amours, Olivier ^a   Dufour, Maurice ^a   Oko, Richard ^b   Sullivan, Robert ^a  

^a UNIVERSITÉ LAVAL   (Canada)

^b QUEEN S UNIVERSITY   (Canada)

Author keywords

ABCG2; ATP binding cassette transporters; Bull spermatozoa; Epididymis

Indexed keywords

BREAST CANCER RESISTANCE PROTEIN; CHOLESTEROL SULFATE; HOE 33342; MESSENGER RNA; ABC TRANSPORTER;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BULL (BOVINE); CELL MEMBRANE; CONTROLLED STUDY; EJACULATION; EPIDIDYMIS; LIPID RAFT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; SEMINAL PLASMA; SPERMATOZOON; SPERMATOZOON MATURATION; ANIMAL; CATTLE; MALE; METABOLISM; PHOSPHORYLATION;

BOVINAE;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; CATTLE; EJACULATION; EPIDIDYMIS; MALE; PHOSPHORYLATION; SPERM MATURATION; SPERMATOZOA;

EID: 84863445157     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.111.097477     Document Type: Article

References (60)

1. Cooper TG, Yeung CH. Sperm maturation in the human epididymis. In: De Jonge C, Barratt C (eds.), The Sperm Cell: Production, Maturation, Fertilization, Regeneration. Cambridge, U.K.: Cambridge University Press; 2006:72-107.
2. Langlais J, Zollinger M, Plante L, Chapdelaine A, Bleau G, Roberts KD. Localization of cholesteryl sulfate in human spermatozoa in support of a hypothesis for the mechanism of capacitation. Proc Natl Acad Sci U S A 1981; 78:7266-7270.
3. Frenette G, Leclerc P, D'amours O, Sullivan R. Estrogen sulfotransferase is highly expressed along the bovine epididymis and is secreted into the intraluminal environment. J Androl 2009; 30:580-589.
4. Schinkel AH, Jonker JW. Mammalian drug efflux transporters of the ATP binding cassette (ABC) family: an overview. Adv Drug Deliv Rev 2003; 55:3-29.
5. Janvilisri T, Venter H, Shahi S, Reuter G, Balakrishnan L, van Veen HW. Sterol transport by the human breast cancer resistance protein (ABCG2) expressed in Lactococcus lactis. J Biol Chem 2003; 278:20645-20651.
6. Suzuki M, Suzuki H, Sugimoto Y, Sugiyama Y. ABCG2 transports sulfated conjugates of steroids and xenobiotics. J Biol Chem 2003; 278: 22644-22649.
7. Storch CH, Ehehalt R, Haefeli WE, Weiss J. Localization of the human breast cancer resistance protein (BCRP/ABCG2) in lipid rafts/caveolae and modulation of its activity by cholesterol in vitro. J Pharmacol Exp Ther 2007; 323:257-264.
8. Pál A, Méhn D, Molnár E, Gedey S, Mészáros P, Nagy T, Glavinas H, Janáky T, von Richter O, Báthori G, Szente L, Krajcsi P. Cholesterol potentiates ABCG2 activity in a heterologous expression system: improved in vitro model to study function of human ABCG2. J Pharmacol Exp Ther 2007; 321:1085-1094.
9. Romsicki Y, Sharom FJ. The membrane lipid environment modulates drug interactions with the P-glycoprotein multidrug transporter. Biochemistry 1999; 38:6887-6896.
10. Troost J, Albermann N, Emil Haefeli W, Weiss J. Cholesterol modulates P-glycoprotein activity in human peripheral blood mononuclear cells. Biochem Biophys Res Commun 2004; 316:705-711.
11. Troost J, Lindenmaier H, Haefeli WE, Weiss J. Modulation of cellular cholesterol alters P-glycoprotein activity in multidrug-resistant cells. Mol Pharmacol 2004; 66:1332-1339.
12. Xie Y, Xu K, Linn DE, Yang X, Guo Z, Shimelis H, Nakanishi T, Ross DD, Chen H, Fazli L, Gleave ME, Qiu Y. The 44-kDa Pim-1 kinase phosphorylates BCRP/ABCG2 and thereby promotes its multimerization and drug-resistant activity in human prostate cancer cells. J Biol Chem 2008; 283:3349-3356.
13. Xie Y, Burcu M, Linn DE, Qiu Y, Baer MR. Pim-1 kinase protects Pglycoprotein from degradation and enables its glycosylation and cell surface expression. Mol Pharmacol 2010; 78:310-318.
14. Hardwick LJ, Velamakanni S, Van Veen HW. The emerging pharmacotherapeutic significance of the breast cancer resistance protein (ABCG2). Br J Pharmacol 2007; 151:163-174.
15. Van Herwaarden AE, Schinkel AH. The function of breast cancer resistance protein in epithelial barriers, stem cells and milk secretion of drugs and xenotoxins. Trends Pharmacol Sci 2006; 27:10-16.
16. Polgar O, Robey RW, Bates SE. ABCG2: structure, function and role in drug response. Expert Opin Drug Metab Toxicol 2008; 4:1-15.
17. Enokizono J, Kusuhara H, Ose A, Schinkel AH, Sugiyama Y. Quantitative investigation of the role of breast cancer resistance protein (Bcrp/Abcg2) in limiting brain and testis penetration of xenobiotic compounds. Drug Metab Dispos 2008; 36:995-1002.
18. Mao Q. BCRP/ABCG2 in the placenta: expression, function and regulation. Pharm Res 2008; 25:1244-1255.
19. Maliepaard M, Scheffer GL, Faneyte IF, Van Gastelen MA, Pijnenborg AC, Schinkel AH, Van De Vijver MJ, Scheper RJ, Schellens JH. Subcellular localization and distribution of the breast cancer resistance protein transporter in normal human tissues. Cancer Res 2001; 61: 3458-3464.
20. Bart J, Hollema H, Groen HJ, de Vries EG, Hendrikse NH, Sleijfer DT, Wegman TD, Vaalburg W, Van der Graaf WT. The distribution of drugefflux pumps, P-gp, BCRP, MRP1 and MRP2, in the normal blood-testis barrier and in primary testicular tumours. Eur J Cancer 2004; 40: 2064-2070.
21. Scharenberg C, Mannowetz N, Robey RW, Brendel C, Repges P, Sahrhage T, Jahn T, Wennemuth G. ABCG2 is expressed in late spermatogenesis and is associated with the acrosome. Biochem Biophys Res Commun 2009; 378:302-307.
22. Legault Y, Bleau G, Chapdelaine A, Roberts KD. The binding of sterol sulfates to hamster spermatozoa. Steroids 1979; 34:89-99.
23. Bleau G, Vandenheuvel WJ, Andersen OF, Gwatkin RB. Desmosteryl sulphate of hamster spermatozoa, a potent inhibitor of capacitation in vitro. J Reprod Fertil 1975; 43:175-178.
24. Girouard J, Frenette G, Sullivan R. Seminal plasma proteins regulate the association of lipids and proteins within detergent-resistant membrane domains of bovine spermatozoa. Biol Reprod 2008; 78:921-931.
25. Frenette G, Lessard C, Sullivan R. Selected proteins of "prostasome-like particles" from epididymal cauda fluid are transferred to epididymal caput spermatozoa in bull. Biol Reprod 2002; 67:308-313.
26. Noland TD, Olson GE, Garbers DL. Purification and partial characterization of plasma membranes from bovine spermatozoa. Biol Reprod 1983; 29:987-998.
27. Lalancette C, Faure RL, Leclerc P. Identification of the proteins present in the bull sperm cytosolic fraction enriched in tyrosine kinase activity: a proteomic approach. Proteomics 2006; 6:4523-4540.
28. Lachance C, Fortier M, Thimon V, Sullivan R, Bailey JL, Leclerc P. Localization of Hsp60 and Grp78 in the human testis, epididymis and mature spermatozoa. Int J Androl 2010; 33:33-44.
29. Wessel D, Flugge UI. A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal Biochem 1984; 138:141-143.
30. Pulido MM, Molina AJ, Merino G, Mendoza G, Prieto JG, Alvarez AI. Interaction of enrofloxacin with breast cancer resistance protein (BCRP/ ABCG2): influence of flavonoids and role in milk secretion in sheep. J Vet Pharmacol Ther 2006; 29:279-287.
31. Goodell MA, Brose K, Paradis G, Conner AS, Mulligan RC. Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J Exp Med 1996; 183:1797-1806.
32. Rabindran SK, Ross DD, Doyle LA, Yang W, Greenberger LM. Fumitremorgin C reverses multidrug resistance in cells transfected with the breast cancer resistance protein. Cancer Res 2000; 60:47-50.
33. Cuasnicu PD, Cohen D, Ellerman D, Busso D, DaRos V, Morgenfeld M. Changes in sperm proteins during epididymal maturation. In: Robaire B, Hinton BT (eds.), The Epididymis: From Molecules to Clinical Practice. New York: Plenum Press; 2002:389-404.
34. Strott CA, Higashi Y. Cholesterol sulfate in human physiology: what's it all about? J Lipid Res 2003; 44:1268-1278.
35. Xu X, London E. The effect of sterol structure on membrane lipid domains reveals how cholesterol can induce lipid domain formation. Biochemistry 2000; 39:843-849.
36. Higgins CF, Gottesman MM. Is the multidrug transporter a flippase? Trends Biochem Sci 1992; 17:18-21.
37. Wang DQ. New concepts of mechanisms of intestinal cholesterol absorption. Ann Hepatol 2003; 2:113-121.
38. Mengerink KJ, Vacquier VD. An ATP-binding cassette transporter is a major glycoprotein of sea urchin sperm membranes. J Biol Chem 2002; 277:40729-40734.
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; 389:577-585.
40. Melaine N, Satie AP, Lassurguere J, Desmots S, Jegou B, Samson M. Molecular cloning of several rat ABC transporters including a new ABC transporter, Abcb8, and their expression in rat testis. Int J Androl 2006; 29: 392-399.
41. Ono N, Van der Heijden I, Scheffer GL, Van de Wetering K, Van Deemter E, De Haas M, Boerke A, Gadella BM, De Rooij DG, Neefjes JJ, Groothuis TA, Oomen L, et al. Multidrug resistance-associated protein 9 (ABCC12) is present in mouse and boar sperm. Biochem J 2007; 406: 31-40.
42. Jones SR, Cyr DG. Regulation and characterization of the ATP-binding cassette transporter-B1 in the epididymis and epididymal spermatozoa of the rat. Toxicol Sci 2011; 119:369-379.
43. Lassalle B, Bastos H, Louis JP, Riou L, Testart J, Dutrillaux B, Fouchet P, Allemand I. 'Side Population' cells in adult mouse testis express Bcrp1 gene and are enriched in spermatogonia and germinal stem cells. Development 2004; 131:479-487.
44. Enokizono J, Kusuhara H, Sugiyama Y. Effect of breast cancer resistance protein (Bcrp/Abcg2) on the disposition of phytoestrogens. Mol Pharmacol 2007; 72(4):967-975.
45. Jonker JW, Buitelaar M, Wagenaar E, Van Der Valk MA, Scheffer GL, Scheper RJ, Plosch T, Kuipers F, Elferink RP, Rosing H, Beijnen JH, Schinkel AH. The breast cancer resistance protein protects against a major chlorophyll-derived dietary phototoxin and protoporphyria. Proc Natl Acad Sci U S A 2002; 99(24):15649-15654.
46. Sullivan R, Frenette G, Girouard J. Epididymosomes are involved in the acquisition of new sperm proteins during epididymal transit. Asian J Androl 2007; 9:483-491.
47. Tanaka Y, Slitt AL, Leazer TM, Maher JM, Klaassen CD. Tissue distribution and hormonal regulation of the breast cancer resistance protein (Bcrp/Abcg2) in rats and mice. Biochem Biophys Res Commun 2005; 326:181-187.
48. Wang H, Zhou L, Gupta A, Vethanayagam RR, Zhang Y, Unadkat JD, Mao Q. Regulation of BCRP/ABCG2 expression by progesterone and 17beta-estradiol in human placental BeWo cells. Am J Physiol Endocrinol Metab 2006; 290:E798-E807.
49. Hess RA, Zhou Q, Nie R, Oliveira C, Cho H, Nakaia M, Carnes K. Estrogens and epididymal function. Reprod Fertil Dev 2001; 13:273-283.
50. Jones R, Fournier-Delpech S, Willadsen SA. Identification of androgendependent proteins synthesized in vitro by the ram epididymis. Reprod Nutr Dev 1982; 22:495-504.
51. Ouvrier A, Cadet R, Vernet P, Laillet B, Chardigny JM, Lobaccaro JM, Drevet JR, Saez F. LXR and ABCA1 control cholesterol homeostasis in the proximal mouse epididymis in a cell-specific manner. J Lipid Res 2009; 50:1766-1775.
52. Demeule M, Jodoin J, Gingras D, Beliveau R. P-glycoprotein is localized in caveolae in resistant cells and in brain capillaries. FEBS Lett 2000; 466: 219-224.
53. Hinrichs JW, Klappe K, Hummel I, Kok JW. ATP-binding cassette transporters are enriched in non-caveolar detergent-insoluble glycosphingolipid-enriched membrane domains (DIGs) in human multidrug-resistant cancer cells. J Biol Chem 2004; 279:5734-5738.
54. Parks JE, Arion JW, Foote RH. Lipids of plasma membrane and outer acrosomal membrane from bovine spermatozoa. Biol Reprod 1987; 37: 1249-1258.
55. Gadella BM, Tsai PS, Boerke A, Brewis IA. Sperm head membrane reorganisation during capacitation. Int J Dev Biol 2008; 52:473-480.
56. Kage K, Tsukahara S, Sugiyama T, Asada S, Ishikawa E, Tsuruo T, Sugimoto Y. Dominant-negative inhibition of breast cancer resistance protein as drug efflux pump through the inhibition of S-S dependent homodimerization. Int J Cancer 2002; 97:626-630.
57. Xu J, Liu Y, Yang Y, Bates S, Zhang JT. Characterization of oligomeric human half-ABC transporter ATP-binding cassette G2. J Biol Chem 2004; 279:19781-19789.
58. Diop NK, Hrycyna CA. N-Linked glycosylation of the human ABC transporter ABCG2 on asparagine 596 is not essential for expression, transport activity, or trafficking to the plasma membrane. Biochemistry 2005; 44:5420-5429.
59. Veeramani S, Yuan T, Chen S, Lin F, Petersen J, Shaheduzzaman S, Srivastava S. MacDonald R M. Cellular prostatic acid phosphatase: a protein tyrosine phosphatase involved in androgen-independent proliferation of prostate cancer. Endocr Relat Cancer 2005; 12(4):805-822.
60. Siciliano L, Marciano V, Carpino A. Prostasome-like vesicles stimulate acrosome reaction of pig spermatozoa. Reprod Biol Endocrinol 2008; 6:5.