Segmental expression of the bradykinin type 2 receptor in rat efferent ducts and epididymis and its role in the regulation of aquaporin 91

Biology of Reproduction

Volumn 80, Issue 1, 2009, Pages 134-143

  Belleannee C ^a   Da Silva, N ^a   Shum, W W C ^a   Marsolais, M ^b   Laprade, R ^b   Brown, D ^a   Breton, S ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Bradykinin receptor; Efferent ducts; Epididymis; Male reproductive tract; Water channel

Indexed keywords

ANION EXCHANGER AE2; ANTIPORTER; AQUAPORIN 9; BRADYKININ; BRADYKININ B1 RECEPTOR; BRADYKININ B2 RECEPTOR; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; GLYCEROL; MESSENGER RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANION EXCHANGE; APICAL MEMBRANE; ARTICLE; CELL ISOLATION; CILIATED EPITHELIUM; CONTROLLED STUDY; EFFERENT DUCT; EPIDIDYMIS; EPIDIDYMIS TAIL; EPITHELIUM CELL; IMMUNOFLUORESCENCE; KALLIKREIN KININ SYSTEM; LASER CAPTURE MICRODISSECTION; MALE; MALE GENITAL SYSTEM; MEMBRANE PERMEABILITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEREOCILIUM;

ANIMALS; AQUAPORINS; BIOLOGICAL TRANSPORT; BLOTTING, WESTERN; EPIDIDYMIS; EPITHELIAL CELLS; FLUORESCENT ANTIBODY TECHNIQUE; GLYCEROL; MALE; MICROSCOPY, CONFOCAL; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, BRADYKININ B2; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

RATTUS;

EID: 58149496532     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.108.070797     Document Type: Article

References (64)

1. Mukai H, Fitzgibbon WR, Bozeman G, Margolius HS, Ploth DW. Bradykinin B2 receptor antagonist increases chloride and water absorption in rat medullary collecting duct. Am J Physiol 1996; 271:R352-R360.
2. Rowland NE, Fregly MJ, Cimmerer AL. Bradykinin-induced water intake and brain fos-like immunoreactivity in rats. Brain Res 1995; 669:73-78.
3. Bhoola KD, Figueroa CD, Worthy K. Bioregulation of kinins: kallikreins, kininogens, and kininases. Pharmacol Rev 1992; 44:1-80.
4. Prado GN, Taylor L, Zhou X, Ricupero D, Mierke DF, Polgar P. Mechanisms regulating the expression, self-maintenance, and signaling-function of the bradykinin B2 and B1 receptors. J Cell Physiol 2002; 193:275-286.
5. Leeb-Lundberg LM, Marceau F, Muller-Esterl W, Pettibone DJ, Zuraw BL. International union of pharmacology. XLV. Classification of the kinin receptor family: from molecular mechanisms to pathophysiological consequences. Pharmacol Rev 2005; 57:27-77.
6. Atanassova N, Kancheva L, Somlev B. Bradykinin stimulates prepubertal rat germ cell proliferation in vitro. Immunopharmacology 1998; 40:173-178.
7. Cheuk BL, Ko WH, Wong PY. COX-dependent and -independent pathways in bradykinin-induced anion secretion in rat epididymis. J Cell Physiol 2002; 191:217-226.
8. Pierucci-Alves F, Schultz BD. Bradykinin-stimulated cyclooxygenase activity stimulates vas deferens epithelial anion secretion in vitro in swine and humans. Biol Reprod 2008; 79:501-509.
9. Peredo HA, Celuch SM. Bradykinin and electrical stimulation increase prostaglandin production in the rat vas deferens. Prostaglandins Leukot Essent Fatty Acids 2001; 65:9-14.
10. Kaneko S, Moriwaki C. Effects of kinins and dipeptidyl carboxypeptidase on the motility of highly washed human sperm. J Pharmacobiodyn 1981; 4:443-450.
11. Schill WB, Miska W. Possible effects of the kallikrein-kinin system on male reproductive functions. Andrologia 1992; 24:69-75.
12. Somlev B, Subev M. Effect of kininase II inhibitors on bradykinin-stimulated bovine sperm motility. Theriogenology 1998; 50:651-657.
13. Cheung KH, Leung GP, Leung MC, Shum WW, Zhou WL, Wong PY. Cell-cell interaction underlies formation of fluid in the male reproductive tract of the rat. J Gen Physiol 2005; 125:443-454.
14. Clulow J, Hansen LA, Jones RC. In vivo microperfusion of the ductuli efferentes testis of the rat: flow dependence of fluid reabsorption. Exp Physiol 1996; 81:633-644.
15. Clulow J, Jones RC, Hansen LA. Micropuncture and cannulation studies of fluid composition and transport in the ductuli efferentes testis of the rat: comparisons with the homologous metanephric proximal tubule. Exp Physiol 1994; 79:915-928.
16. Clulow J, Jones RC, Hansen LA, Man SY. Fluid and electrolyte reabsorption in the ductuli efferentes testis. J Reprod Fertil Suppl 1998; 53:1-14.
17. Hess RA. Oestrogen in fluid transport in efferent ducts of the male reproductive tract. Rev Reprod 2000; 5:84-92.
18. Johnson AL, Howards SS. Hyperosmolality in intraluminal fluids from hamster testis and epididymis: a micropuncture study. Science 1977; 195:492-493.
19. Levine N, Marsh DJ. Micropuncture studies of the electrochemical aspects of fluid and electrolyte transport in individual seminiferous tubules, the epididymis and the vas deferens in rats. J Physiol 1971; 213:557-570.
20. Turner TT, Cesarini DM. The ability of the rat epididymis to concentrate spermatozoa. Responsiveness to aldosterone. J Androl 1983; 4:197-202.
21. Sedlacek RL, Carlin RW, Singh AK, Schultz BD. Neurotransmitter-stimulated ion transport by cultured porcine vas deferens epithelium. Am J Physiol Renal Physiol 2001; 281:F557-F570.
22. Wong PY. CFTR gene and male fertility. Mol Hum Reprod 1998; 4:107-110.
23. Cooper TG, Brooks DE. Entry of glycerol into the rat epididymis and its utilization by epididymal spermatozoa. J Reprod Fertil 1981; 61:163-169.
24. Cheung KH, Leung CT, Leung GP, Wong PY. Synergistic effects of cystic fibrosis transmembrane conductance regulator and aquaporin-9 in the rat epididymis. Biol Reprod 2003; 68:1505-1510.
25. Pietrement C, Da Silva N, Silberstein C, James M, Marsolais M, Van Hoek A, Brown D, Pastor-Soler N, Ameen N, Laprade R, Ramesh V, Breton S. Role of NHERF1, cystic fibrosis transmembrane conductance regulator, and cAMP in the regulation of aquaporin 9. J Biol Chem 2008; 283:2986-2996.
26. Tsukaguchi H, Shayakul C, Berger UV, Mackenzie B, Devidas S, Guggino WB, van Hoek AN, Hediger MA. Molecular characterization of a broad selectivity neutral solute channel. J Biol Chem 1998; 273:24737-24743.
27. Badran HH, Hermo LS. Expression and regulation of aquaporins 1, 8, and 9 in the testis, efferent ducts, and epididymis of adult rats and during postnatal development. J Androl 2002; 23:358-373.
28. Da Silva N, Pietrement C, Brown D, Breton S. Segmental and cellular expression of aquaporins in the male excurrent duct. Biochim Biophys Acta 2006; 1758:1025-1033.
29. Elkjaer M, Vajda Z, Nejsum LN, Kwon T, Jensen UB, Amiry-Moghaddam M, Frokiaer J, Nielsen S. Immunolocalization of AQP9 in liver, epididymis, testis, spleen, and brain. Biochem Biophys Res Commun 2000; 276:1118-1128.
30. Pastor-Soler N, Bagnis C, Sabolic I, Tyszkowski R, McKee M, Van Hoek A, Breton S, Brown D. Aquaporin 9 expression along the male reproductive tract. Biol Reprod 2001; 65:384-393.
31. Monsees TK, Blocher S, Heidorn F, Winkler A, Siems WE, Muller-Esterl W, Hayatpour J, Miska W, Schill WB. Expression and location of the bradykinin B2 receptor in rat testis. Biol Reprod 2002; 67:1832-1839.
32. Monsees TK, Blocher S, Loddo C, Steger K, Schill WB. Tissue kallikrein and bradykinin B2 receptors in the reproductive tract of the male rat. Andrologia 2003; 35:24-31.
33. Beaulieu V, Da Silva N, Pastor-Soler N, Brown CR, Smith PJ, Brown D, Breton S. Modulation of the actin cytoskeleton via gelsolin regulates vacuolar H+-ATPase recycling. J Biol Chem 2005; 280:8452-8463.
34. Pastor-Soler N, Beaulieu V, Litvin TN, Da Silva N, Chen Y, Brown D, Buck J, Levin LR, Breton S. Bicarbonate-regulated adenylyl cyclase (sAC) is a sensor that regulates pH-dependent V-ATPase recycling. J Biol Chem 2003; 278:49523-49529.
35. Pastor-Soler NM, Hallows KR, Smolak C, Gong F, Brown D, Breton S. Alkaline pH- and cAMP-induced V-ATPase membrane accumulation is mediated by protein kinase A in epididymal clear cells. Am J Physiol Cell Physiol 2008; 294:C488-C494.
36. Da Silva N, Shum WW, El-Annan J, Paunescu TG, McKee M, Smith PJ, Brown D, Breton S. Relocalization of the V-ATPase B2 subunit to the apical membrane of epididymal clear cells of mice deficient in the B1 subunit. Am J Physiol Cell Physiol 2007; 293:C199-C210.
37. Herak-Kramberger CM, Breton S, Brown D, Kraus O, Sabolic I. Distribution of the vacuolar H+ ATPase along the rat and human male reproductive tract. Biol Reprod 2001; 64:1699-1707.
38. Pietrement C, Sun-Wada GH, Silva ND, McKee M, Marshansky V, Brown D, Futai M, Breton S. Distinct expression patterns of different subunit isoforms of the V-ATPase in the rat epididymis. Biol Reprod 2006; 74:185-194.
39. Pastor-Soler N, Isnard-Bagnis C, Herak-Kramberger C, Sabolic I, Van Hoek A, Brown D, Breton S. Expression of aquaporin 9 in the adult rat epididymal epithelium is modulated by androgens. Biol Reprod 2002; 66:1716-1722.
40. Bagnis C, Marsolais M, Biemesderfer D, Laprade R, Breton S. Na+/H+- exchange activity and immunolocalization of NHE3 in rat epididymis. Am J Physiol Renal Physiol 2001; 280:426-436.
41. Jensen LJ, Stuart-Tilley AK, Peters LL, Lux SE, Alper SL, Breton S. Immunolocalization of AE2 anion exchanger in rat and mouse epididymis. Biol Reprod 1999; 61:973-980.
42. Brown D, Lydon J, McLaughlin M, Stuart-Tilley A, Tyszkowski R, Alper S. Antigen retrieval in cryostat tissue sections and cultured cells by treatment with sodium dodecyl sulfate (SDS). Histochem Cell Biol 1996; 105:261-267.
43. Breton S, Wiederhold T, Marshansky V, Nsumu NN, Ramesh V, Brown D. The B1 subunit of the H+ATPase is a PDZ domain-binding protein. Colocalization with NHE-RF in renal B-intercalated cells. J Biol Chem 2000; 275:18219-18224.
44. Da Silva N, Silberstein C, Beaulieu V, Pietrement C, Van Hoek AN, Brown D, Breton S. Postnatal expression of aquaporins in epithelial cells of the rat epididymis. Biol Reprod 2006; 74:427-438.
45. Blaukat A. Structure and signalling pathways of kinin receptors. Andrologia 2003; 35:17-23.
46. Blaukat A, Alla SA, Lohse MJ, Muller-Esterl W. Ligand-induced phosphorylation/dephosphorylation of the endogenous bradykinin B2 receptor from human fibroblasts. J Biol Chem 1996; 271:32366-32374.
47. Regoli D. Neurohumoral regulation of precapillary vessels: the kallikrein-kinin system. J Cardiovasc Pharmacol 1984; 6(suppl 2):S401-S412.
48. Dixon BS, Sharma RV, Dickerson T, Fortune J. Bradykinin and angiotensin II: activation of protein kinase C in arterial smooth muscle. Am J Physiol 1994; 266:C1406-C1420.
49. Kozak M. Some thoughts about translational regulation: forward and backward glances. J Cell Biochem 2007; 102:280-290.
50. Tamma G, Carmosino M, Svelto M, Valenti G. Bradykinin signaling counteracts cAMP-elicited aquaporin 2 translocation in renal cells. J Am Soc Nephrol 2005; 16:2881-2889.
51. Leung GP, Gong XD, Cheung KH, Cheng-Chew SB, Wong PY. Expression of cystic fibrosis transmembrane conductance regulator in rat efferent duct epithelium. Biol Reprod 2001; 64:1509-1515.
52. Yoo D, Flagg TP, Olsen O, Raghuram V, Foskett JK, Welling PA. Assembly and trafficking of a multiprotein ROMK (Kir 1.1) channel complex by PDZ interactions. J Biol Chem 2004; 279:6863-6873.
53. Takano M, Kondo J, Yayama K, Otani M, Sano K, Okamoto H. Molecular cloning of cDNAs for mouse low-molecular-weight and high-molecular-weight prekininogens. Biochim Biophys Acta 1997; 1352:222-230.
54. Scott AC, Wensel R, Davos CH, Georgiadou P, Ceri Davies L, Coats AJ, Francis DP, Piepoli MF. Putative contribution of prostaglandin and bradykinin to muscle reflex hyperactivity in patients on Ace-inhibitor therapy for chronic heart failure. Eur Heart J 2004; 25:1806-1813.
55. Chen Y, Xu L, Lin J, Chen G. Assay of bradykinin-related peptides in human body fluids using capillary electrophoresis with laser-induced fluorescence detection. Electrophoresis 2008; 29:1302-1307.
56. Vickers ER, Goebel C, Mather LE, Mackay L, Wells RJ. High-performance liquid chromatographic determination of bradykinin in saliva: a critical review and a new method. J Chromatogr B Biomed Sci Appl 2001; 755:101-110.
57. Campbell DJ, Kladis A, Duncan AM. Bradykinin peptides in kidney, blood, and other tissues of the rat. Hypertension 1993; 21:155-165.
58. Hagiwara Y, Kojima M, Kuraishi T, Hayashi I, Miyata T, Oh-ishi S. Identification of rat urinary kinin as bradykinin. Life Sci 1995; 57:997-1002.
59. Kato H, Enjyoji K, Miyata T, Hayashi I, Oh-ishi S, Iwanaga S. Demonstration of arginyl-bradykinin moiety in rat HMW kininogen: direct evidence for liberation of bradykinin by rat glandular kallikreins. Biochem Biophys Res Commun 1985; 127:289-295.
60. Gatti JL, Druart X, Guerin Y, Dacheux F, Dacheux JL. A 105- to 94-kilodalton protein in the epididymal fluids of domestic mammals is angiotensin I-converting enzyme (ACE); evidence that sperm are the source of this ACE. Biol Reprod 1999; 60:937-945.
61. Esther CR Jr, Howard TE, Marino EM, Goddard JM, Capecchi MR, Bernstein KE. Mice lacking angiotensin-converting enzyme have low blood pressure, renal pathology, and reduced male fertility. Lab Invest 1996; 74:953-965.
62. Hagaman JR, Moyer JS, Bachman ES, Sibony M, Magyar PL, Welch JE, Smithies O, Krege JH, O'Brien DA. Angiotensin-converting enzyme and male fertility. Proc Natl Acad Sci U S A 1998; 95:2552-2557.
63. Krege JH, John SW, Langenbach LL, Hodgin JB, Hagaman JR, Bachman ES, Jennette JC, O'Brien DA, Smithies O. Male-female differences in fertility and blood pressure in ACE-deficient mice. Nature 1995; 375:146-148.
64. Metayer S, Dacheux F, Guerin Y, Dacheux JL, Gatti JL. Physiological and enzymatic properties of the ram epididymal soluble form of germinal angiotensin I-converting enzyme. Biol Reprod 2001; 65:1332-1339.