Early activation of sperm by HCO3- is regulated hormonally in the murine uterus

International Journal of Andrology

Volumn 34, Issue 2, 2011, Pages 153-164

  Mannowetz, N ^a   Wandernoth, P ^a   Hornung, J ^a   Ruffing, U ^a   Raubuch, M ^a   Wennemuth, G ^a  

^a SAARLAND UNIVERSITY   (Germany)

Author keywords

Beat frequency; Capacitation; Cystic fibrosis transmembrane conductance regulator; HCO3 ; Oestrous cycle

Indexed keywords

BICARBONATE; MESSENGER RNA; PROTEIN TYROSINE KINASE; TRANSMEMBRANE CONDUCTANCE REGULATOR;

ADULTHOOD; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; DIESTRUS; ESTRUS; FEMALE; FLAGELLUM; IMMUNOREACTIVITY; MALE; MALE GENITAL SYSTEM; NONHUMAN; OVULATION; PREPUBERTY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PUBERTY; SEXUAL DEVELOPMENT; SPERMATOZOON CAPACITATION; SPERMATOZOON MOTILITY; SUBFERTILITY; UTERUS; UTERUS FLUID;

ANIMALS; BENZOIC ACIDS; BICARBONATES; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; ESTRUS; FEMALE; GLYCINE; HYDRAZINES; MALE; MICE; PUBERTY; RNA, MESSENGER; SPERM CAPACITATION; SPERM MOTILITY; SPERMATOZOA; THIAZOLIDINES; UTERUS;

EID: 79952721595     PISSN: 01056263     EISSN: 13652605     Source Type: Journal    
DOI: 10.1111/j.1365-2605.2010.01067.x     Document Type: Article

References (50)

1. Anderson MP, Berger HA, Rich DP, Gregory RJ, Smith AE & Welsh MJ. (1991) Nucleoside triphosphates are required to open the CFTR chloride channel. Cell 67, 775-784.
2. - channel by specific protein kinases and protein phosphatases. J Biol Chem 268, 2037-2047.
3. Boyle MP. (2003) Nonclassic cystic fibrosis and CFTR-related diseases. Curr Opin Pulm Med 9, 498-503.
4. Buck J, Sinclair ML, Schapal L, Cann MJ & Levin LR. (1999) Cytosolic adenylyl cyclase defines a unique signaling molecule in mammals. Proc Natl Acad Sci USA 96, 79-84.
5. 2+ acts upstream of adenylyl cyclase SACY in the bicarbonate signaled activation of sperm motility. Dev Biol 312, 183-192.
6. Chan LN, Tsang LL, Rowlands DK, Rochelle LG, Boucher RC, Liu CQ & Chan HC. (2002) Distribution and regulation of ENAC subunit and CFTR mRNA expression in murine female reproductive tract. J Membr Biol 185, 165-176.
7. Chen Y, Cann MJ, Litvin TN, Iourgenko V, Sinclair ML, Levin LR & Buck J. (2000) Soluble adenylyl cyclase as an evolutionarily conserved bicarbonate sensor. Science 289, 625-628.
8. - exchanger (SLC26A3) and CFTR. Biol Reprod 80, 115-123.
9. Cheng SH, Rich DP, Marshall J, Gregory RJ, Welsh MJ & Smith AE. (1991) Phosphorylation of the R domain by cAMP-dependent protein kinase regulates the CFTR chloride channel. Cell 66, 1027-1036.
10. Collado ML, Castro G & Hicks JJ. (1979) Effect of spermatozoa upon carbonic anhydrase activity of rabbit endometrium. Biol Reprod 20, 747-750.
11. Crawford I, Maloney PC, Zeitlin PL, Guggino WB, Hyde SC, Turley H, Gatter KC, Harris A & Higgins CF. (1991) Immunocytochemical localization of the cystic fibrosis gene product CFTR. Proc Natl Acad Sci USA 88, 9262-9266.
12. David A, Brackett BG, Garcia CR & Mastroianni L, Jr. (1969) Composition of rabbit oviduct fluid in ligated segments of the Fallopian tube. J Reprod Fertil 19, 285-289.
13. - cotransporter in mouse sperm capacitation. J Biol Chem 278, 7001-7009.
14. Duncan AE & Fraser LR. (1993) Cyclic AMP-dependent phosphorylation of epididymal mouse sperm proteins during capacitation in vitro: identification of an M(r) 95, 000 phosphotyrosine-containing protein. J Reprod Fertil 97, 287-299.
15. Ekstedt E, Holm L & Ridderstrale Y. (2004) Carbonic anhydrase in mouse testis and epididymis; transfer of isozyme IV to spermatozoa during passage. J Mol Histol 35, 167-173.
16. Falk RJ & Hodgen GD. (1972) Carbonic anhydrase isoenzymes in normal human endometrium and erythrocytes. Am J Obstet Gynecol 112, 1047-1051.
17. Florman HM, Jungnickel MK & Sutton KA. (2007) What can we learn about fertilization from cystic fibrosis? Proc Natl Acad Sci USA 104, 11123-11124.
18. Fraser LR & Monks NJ. (1990) Cyclic nucleotides and mammalian sperm capacitation. J Reprod Fertil Suppl 42, 9-21.
19. Friedley NJ & Rosen S. (1975) Carbonic anhydrase activity in the mammalian ovary, fallopian tube, and uterus: histochemical and biochemical studies. Biol Reprod 12, 293-304.
20. Ge ZH & Spicer SS. (1988) Immunocytochemistry of ion transport mediators in the genital tract of female rodents. Biol Reprod 38, 439-452.
21. Hegedus T, Aleksandrov A, Mengos A, Cui L, Jensen TJ & Riordan JR. (2009) Role of individual R domain phosphorylation sites in CFTR regulation by protein kinase A. Biochim Biophys Acta (BBA) - Biomembr 1788, 1341-1349.
22. Hernandez-Gonzalez EO, Trevino CL, Castellano LE, de la Vega-Beltran JL, Ocampo AY, Wertheimer E, Visconti PE & Darszon A. (2007) Involvement of cystic fibrosis transmembrane conductance regulator in mouse sperm capacitation. J Biol Chem 282, 24397-24406.
23. Hihnala S, Kujala M, Toppari J, Kere J, Holmberg C & Hoglund P. (2006) Expression of SLC26A3, CFTR and NHE3 in the human male reproductive tract: role in male subfertility caused by congenital chloride diarrhoea. Mol Hum Reprod 12, 107-111.
24. Hynninen P, Hamalainen JM, Pastorekova S, Pastorek J, Waheed A, Sly WS, Tomas E, Kirkinen P & Parkkila S. (2004) Transmembrane carbonic anhydrase isozymes IX and XII in the female mouse reproductive organs. Reprod Biol Endocrinol 2, 73.
25. Johannesson M, Landgren BM, Csemiczky G, Hjelte L & Gottlieb C. (1998) Female patients with cystic fibrosis suffer from reproductive endocrinological disorders despite good clinical status. Hum Reprod 13, 2092-2097.
26. Karhumaa P, Parkkila S, Tureci O, Waheed A, Grubb JH, Shah G et al. (2000) Identification of carbonic anhydrase XII as the membrane isozyme expressed in the normal human endometrial epithelium. Mol Hum Reprod 6, 68-74.
27. Kopelman H, Corey M, Gaskin K, Durie P, Weizman Z & Forstner G. (1988) Impaired chloride secretion, as well as bicarbonate secretion, underlies the fluid secretory defect in the cystic fibrosis pancreas. Gastroenterology 95, 349-355.
28. Kopito LE, Kosasky HJ & Shwachman H. (1973) Water and electrolytes in cervical mucus from patients with cystic fibrosis. Fertil Steril 24, 512-516.
29. Lutwak-Mann C. (1955) Carbonic anhydrase in the female reproductive tract; occurrence, distribution and hormonal dependence. J Endocrinol 13, 26-38.
30. Lutwak-Mann C & Laser H. (1954) Bicarbonate content of the blastocyst fluid and carbonic anhydrase in the pregnant rabbit uterus. Nature 173, 268-269.
31. Marino CR, Matovcik LM, Gorelick FS & Cohn JA. (1991) Localization of the cystic fibrosis transmembrane conductance regulator in pancreas. J Clin Invest 88, 712-716.
32. Mettus RV & Rane SG. (2003) Characterization of the abnormal pancreatic development, reduced growth and infertility in CDK4 mutant mice. Oncogene 22, 8413-8421.
33. Mularoni A, Beck L, Sadir R, Adessi GL & Nicollier M. (1995) Down-regulation by progesterone of CFTR expression in endometrial epithelial cells: a study by competitive RT-PCR. Biochem Biophys Res Commun 217, 1105-1111.
34. Mulberg AE, Weyler RT, Altschuler SM & Hyde TM. (1998) Cystic fibrosis transmembrane conductance regulator expression in human hypothalamus. Neuroreport 9, 141-144.
35. Oppenheimer EA, Case AL, Esterly JR & Rothberg RM. (1970) Cervical mucus in cystic fibrosis: a possible cause of infertility. Am J Obstet Gynecol 108, 673-674.
36. Parkkila S, Kaunisto K, Kellokumpu S & Rajaniemi H. (1991) A high activity carbonic anhydrase isoenzyme (CA II) is present in mammalian spermatozoa. Histochemistry 95, 477-482.
37. - conductances. JOP 2, 212-218.
38. Trezise AE, Linder CC, Grieger D, Thompson EW, Meunier H, Griswold MD & Buchwald M. (1993) CFTR expression is regulated during both the cycle of the seminiferous epithelium and the oestrous cycle of rodents. Nat Genet 3, 157-164.
39. van der Ven K, Messer L, van der Ven H, Jeyendran RS & Ober C. (1996) Cystic fibrosis mutation screening in healthy men with reduced sperm quality. Hum Reprod 11, 513-517.
40. Visconti PE, Bailey JL, Moore GD, Pan D, Olds-Clarke P & Kopf GS. (1995) Capacitation of mouse spermatozoa. I. Correlation between the capacitation state and protein tyrosine phosphorylation. Development 121, 1129-1137.
41. Wang XF, Zhou CX, Shi QX, Yuan YY, Yu MK, Ajonuma LC et al. (2003) Involvement of CFTR in uterine bicarbonate secretion and the fertilizing capacity of sperm. Nat Cell Biol 5, 902-906.
42. Ward CR & Storey BT. (1984) Determination of the time course of capacitation in mouse spermatozoa using a chlortetracycline fluorescence assay. Dev Biol 104, 287-296.
43. 2+-channel responses: initial events in sperm activation. Development 130, 1317-1326.
44. Wertheimer EV, Salicioni AM, Liu W, Trevino CL, Chavez J, Hernandez-Gonzalez EO, Darszon A & Visconti PE. (2008) Chloride is essential for capacitation and for the capacitation-associated increase in tyrosine phosphorylation. J Biol Chem 283, 35539-35550.
45. Weyler RT, Yurko-Mauro KA, Rubenstein R, Kollen WJ, Reenstra W, Altschuler SM, Egan M & Mulberg AE. (1999) CFTR is functionally active in GnRH-expressing GT1-7 hypothalamic neurons. Am J Physiol 277, C563-C571.
46. Xu WM, Shi QX, Chen WY, Zhou CX, Ni Y, Rowlands DK et al. (2007) Cystic fibrosis transmembrane conductance regulator is vital to sperm fertilizing capacity and male fertility. Proc Natl Acad Sci USA 104, 9816-9821.
47. Yanagimachi R. (ed.) (1994) Mammalian Fertilization. Raven Press, New York.
48. Yang JZ, Ajonuma LC, Tsang LL, Lam SY, Rowlands DK, Ho LS, Zhou CX, Chung YW & Chan HC. (2004) Differential expression and localization of CFTR and ENAC in mouse endometrium during pre-implantation. Cell Biol Int 28, 433-439.
49. Yankaskas JR, Marshall BC, Sufian B, Simon RH & Rodman D. (2004) Cystic fibrosis adult care: consensus conference report. Chest 125, 1S-39S.
50. 3(-)-dependent and arylaminobenzoate-dependent regulatory mechanisms and characterization of their roles in sperm capacitation. Dev Biol 173, 510-520.