Cloning and identification of two novel NBCe1 splice variants from mouse reproductive tract tissues: A comparative study of NCBT genes

Genomics

Volumn 98, Issue 2, 2011, Pages 112-119

  Liu, Ying ^a   Xu, Jiu Ying ^a   Wang, Deng Ke ^a   Wang, Lei ^a   Chen, Li Ming ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

Alternative splicing; Bicarbonate transporter; NBC1; Reproduction; SLC4A4

Indexed keywords

CARRIER PROTEIN; MESSENGER RNA; NUCLEOTIDE; PROTEIN NBCE1 D; PROTEIN NBCE1 E; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GENE; GENE CASSETTE; GENE EXPRESSION; GENE SEQUENCE; GENETIC CONSERVATION; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; GENITAL SYSTEM; MOLECULAR CLONING; MOLECULAR EVOLUTION; MOUSE; NCBT GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RNA SPLICING; SEQUENCE ANALYSIS; SLC4A4 GENE; SLC4A5 GENE; TISSUE SECTION;

ALTERNATIVE SPLICING; ANIMALS; CLONING, MOLECULAR; FEMALE; GENE EXPRESSION; GENITALIA; MALE; MICE; MICE, INBRED C57BL; PROTEIN ISOFORMS; SEQUENCE ALIGNMENT; SODIUM-BICARBONATE SYMPORTERS; TISSUE DISTRIBUTION;

MURINAE; VERTEBRATA;

EID: 79960700888     PISSN: 08887543     EISSN: 10898646     Source Type: Journal    
DOI: 10.1016/j.ygeno.2011.04.010     Document Type: Article

References (48)

1. Abuladze N., Song M., Pushkin A., Newman D., Lee I., Nicholas S., Kurtz I. Structural organization of the human NBC1 gene: kNBC1 is transcribed from an alternative promoter in intron 3. Gene 2000, 251:109-122.
2. Bevensee M.O., Schmitt B.M., Choi I., Romero M.F., Boron W.F. An electrogenic Na/HCO3 cotransporter (NBC) with a novel C terminus, cloned from rat brain. Am. J. Physiol. Cell Physiol. 2000, 278:C1200-C1211.
3. Boedtkjer E., Praetorius J., Fuchtbauer E.M., Aalkjaer C. Antibody-independent localization of the electroneutral Na+, HCO3- cotransporter NBCn1 (slc4a7) in mice. Am. J. Physiol. Cell Physiol. 2008, 294:C591-C603.
4. Boron W.F., Boulpaep E.L. Intracellular pH regulation in the renal proximal tubule of the salamander: basolateral HCO3- transport. J. Gen. Physiol. 1983, 81:53-94.
5. Boron W.F., Chen L., Parker M.D. Modular structure of sodium-coupled bicarbonate transporters. J. Exp. Biol. 2009, 212:1697-1706.
6. Bouzinova E.V., Praetorius J., Virkki L.V., Nielsen S., Boron W.F., Aalkjær C. Na+-dependent HCO3- uptake into the rat choroid plexus epithelium is partially DIDS sensitive. Am. J. Physiol. Cell Physiol. 2005, 289:C1448-C1456.
7. Carlin R.W., Lee J.H., Marcus D.C., Schultz B.D. Adenosine stimulates anion secretion across cultured and native adult human vas deferens epithelia. Biol. Reprod. 2003, 68:1027-1034.
8. Carlin R.W., Quesnell R.R., Zheng L., Mitchell K.E., Schultz B.D. Functional and molecular evidence for Na+-HCO3- cotransporter in porcine vas deferens epithelia. Am. J. Physiol. Cell Physiol. 2002, 283:C1033-C1044.
9. Carlin R.W., Sedlacek R.L., Quesnell R.R., Pierucci-Alves F., Grieger D.M., Schultz B.D. PVD9902, a porcine vas deferens epithelial cell line that exhibits neurotransmitter-stimulated anion secretion and expresses numerous HCO3- transporters. Am. J. Physiol. Cell Physiol. 2006, 290:C1560-C1571.
10. Chan H.C., Ko W.H., Zhao W., Fu W.O., Wong P.Y. Evidence for independent Cl- and HCO3- secretion and involvement of an apical Na+-HCO3- cotransporter in cultured rat epididymal epithelia. Exp. Physiol. 1996, 81:515-524.
11. Chan H.C., Ruan Y.C., He Q., Chen M.H., Chen H., Xu W.M., Chen W.Y., Xie C., Zhang X.H., Zhou Z. The cystic fibrosis transmembrane conductance regulator in reproductive health and disease. J. Physiol. 2009, 587:2187-2195.
12. Chen Y., Cann M.J., Litvin T.N., Iourgenko V., Sinclair M.L., Levin L.R., Buck J. Soluble adenylyl cyclase as an evolutionarily conserved bicarbonate sensor. Science 2000, 289:625-628.
13. Choi I., Aalkjær C., Boulpaep E.L., Boron W.F. An electroneutral sodium/bicarbonate cotransporter NBCn1 and associated sodium channel. Nature 2000, 405:571-575.
14. Cooper D.S., Lee H.J., Yang H.S., Kippen J., Yun C.C., Choi I. The electroneutral sodium/bicarbonate cotransporter containing an amino terminal 123-amino-acid cassette is expressed predominantly in the heart. J. Biomed. Sci. 2006, 13:593-595.
15. Damkier H.H., Nielsen S., Praetorius J. An anti-NH2-terminal antibody localizes NBCn1 to heart endothelia and skeletal and vascular smooth muscle cells. Am. J. Physiol. Heart Circ. Physiol. 2006, 290:H172-H180.
16. Ding Y., Kobayashi S., Kopito R. Mapping of ankyrin binding determinants on the erythroid anion exchanger, AE1. J. Biol. Chem. 1996, 271:22494-22498.
17. Dominguez I., Sonenshein G.E., Seldin D.C. Protein kinase CK2 in health and disease: CK2 and its role in Wnt and NF-kappaB signaling: linking development and cancer. Cell. Mol. Life Sci. 2009, 66:1850-1857.
18. Gill H.S., Boron W.F. Preliminary X-ray diffraction analysis of the cytoplasmic N-terminal domain of the Na/HCO3 cotransporter NBCe1-A. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 2006, 62:534-537.
19. Grichtchenko I.I., Choi I., Zhong X., Bray-Ward P., Russell J.M., Boron W.F. Cloning, characterization, and chromosomal mapping of a human electroneutral Na+-driven Cl-HCO3 exchanger. J. Biol. Chem. 2001, 276:8358-8363.
20. Gross E., Abuladze N., Pushkin A., Kurtz I., Cotton C.U. The stoichiometry of the electrogenic sodium bicarbonate cotransporter pNBC1 in mouse pancreatic duct cells is 2 HCO3-:1 Na+. J. Physiol. 2001, 531:375-382.
21. Hodges C.A., Palmert M.R., Drumm M.L. Infertility in females with cystic fibrosis is multifactorial: evidence from mouse models. Endocrinology 2008, 149:2790-2797.
22. Höglund P., Haila S., Socha J., Tomaszewski L., Saarialho-Kere U., Karjalainen-Lindsberg M.L., Airola K., Holmberg C., de la Chapelle A., Kere J. Mutations of the Down-regulated in adenoma (DRA) gene cause congenital chloride diarrhoea. Nat. Genet. 1996, 14:316-319.
23. Höglund P., Hihnala S., Kujala M., Tiitinen A., Dunkel L., Holmberg C. Disruption of the SLC26A3-mediated anion transport is associated with male subfertility. Fertil. Steril. 2006, 85:232-235.
24. Jensen L., Schmitt B.M., Brown D., Berger U.V., Hediger M.A., Boron W.F., Breton S. Localization of sodium bicarbonate co-transporter (NBC) protein and mRNA in rat epididymis. Biol. Reprod. 1999, 60:573-579.
25. Joseph A., Hess R.A., Schaeffer D.J., Ko C., Hudgin-Spivey S., Chambon P., Shur B.D. Absence of estrogen receptor alpha leads to physiological alterations in the mouse epididymis and consequent defects in sperm function. Biol. Reprod. 2010, 82:948-957.
26. Klee C.B., Ren H., Wang X. Regulation of the calmodulin-stimulated protein phosphatase, calcineurin. J. Biol. Chem. 1998, 273:13367-13370.
27. Levine N., Marsh D.J. 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.
28. Majumdar D., Maunsbach A.B., Shacka J.J., Williams J.B., Berger U.V., Schultz K.P., Harkins L.E., Boron W.F., Roth K.A., Bevensee M.O. Localization of electrogenic Na/bicarbonate cotransporter NBCe1 variants in rat brain. Neuroscience 2008, 155:818-832.
29. McAlear S.D., Liu X., Williams J.B., McNicholas-Bevensee C.M., Bevensee M.O. Electrogenic Na/HCO3 cotransporter (NBCe1) variants expressed in Xenopus oocytes: functional comparison and roles of the amino and carboxy termini. J. Gen. Physiol. 2006, 127:639-658.
30. Medina J.F., Recalde S., Prieto J., Lecanda J., Saez E., Funk C.D., Vecino P., van Roon M.A., Ottenhoff R., Bosma P.J., Bakker C.T., Elferink R.P. Anion exchanger 2 is essential for spermiogenesis in mice. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:15847-15852.
31. Millar I.D., Brown P.D. NBCe2 exhibits a 3 HCO3-:1 Na+ stoichiometry in mouse choroid plexus epithelial cells. Biochem. Biophys. Res. Commun. 2008, 373:550-554.
32. Mohler P.J. Ankyrins and human disease: what the electrophysiologist should know. J. Cardiovasc. Electrophysiol. 2006, 17:1153-1159.
33. Murdoch R.N., White I.G. The influence of the female genital tract on the metabolism of rabbit spermatozoa. I. Direct effect of tubal and uterine fluids, bicarbonate, and other factors. Aust. J. Biol. Sci. 1968, 21:961-972.
34. Parker M.D., Boron W.F. Splice cassette II within the N terminus of the electroneutral Na+ coupled bicarbonate transporter NBCn1 includes a functional calcineurin Aβ binding site. FASEB J. 2008, 22:759.12.
35. Parker M.D., Bouyer P., Daly C.M., Boron W.F. Cloning and characterization of novel human SLC4A8 gene products encoding Na+-driven Cl-/HCO3- exchanger variants NDCBE-A, -C, and -D. Physiol. Genomics 2008, 34:265-276.
36. Pastor-Soler N., Pietrement C., Breton S. Role of acid/base transporters in the male reproductive tract and potential consequences of their malfunction. Physiology 2005, 20:417-428.
37. Pearce L.R., Komander D., Alessi D.R. The nuts and bolts of AGC protein kinases. Nat. Rev. Mol. Cell Biol. 2010, 11:9-22.
38. Pushkin A., Clark I., Kwon T.H., Nielsen S., Kurtz I. Immunolocalization of NBC3 and NHE3 in the rat epididymis: colocalization of NBC3 and the vacuolar H+-ATPase. J. Androl. 2000, 21:708-720.
39. Romero M.F., Hediger M.A., Boulpaep E.L., Boron W.F. Expression cloning and characterization of a renal electrogenic Na+/HCO3- cotransporter. Nature 1997, 387:409-413.
40. Sassani P., Pushkin A., Gross E., Gomer A., Abuladze N., Dukkipati R., Carpenito G., Kurtz I. Functional characterization of NBC4: a new electrogenic sodium- bicarbonate cotransporter. Am. J. Physiol. Cell Physiol. 2002, 282:C408-C416.
41. Schmitt B.M., Biemesderfer D., Romero M.F., Boulpaep E.L., Boron W.F. Immunolocalization of the electrogenic Na+/HCO3- cotransporter in mammalian and amphibian kidney. Am. J. Physiol. 1999, 276:F27-F36.
42. Shirakabe K., Priori G., Yamada H., Ando H., Horita S., Fujita T., Fujimoto I., Mizutani A., Seki G., Mikoshiba K. IRBIT, an inositol 1,4,5-trisphosphate receptor-binding protein, specifically binds to and activates pancreas-type Na+/HCO3-cotransporter 1 (pNBC1). Proc. Natl. Acad. Sci. U. S. A. 2006, 103:9542-9547.
43. Soleimani M., Grassl S.M., Aronson P.S. Stoichiometry of Na+-HCO3- cotransport in basolateral membrane vesicles isolated from rabbit renal cortex. J. Clin. Invest. 1987, 79:1276-1280.
44. Trudeau M.C., Warmke J.W., Ganetzky B., Robertson G.A. HERG, a human inward rectifier on the voltage-gated potassium channel family. Science 1995, 269:92-95.
45. Vishwakarma P. The pH and bicarbonate-ion content of the oviduct and uterine fluids. Fertil. Steril. 1962, 13:481-485.
46. Wang X.F., Yu M.K., Leung K.M., Yip C.Y., Ko W.H., Liu C.Q., Chan H.C. Involvement of Na+-HCO3- cotransporter in mediating cyclic adenosine 3',5'-monophosphate-dependent HCO3- secretion by mouse endometrial epithelium. Biol. Reprod. 2002, 66:1846-1852.
47. Wang X.F., Zhou C.X., Shi Q.X., Yuan Y.Y., Yu M.K., Ajonuma L.C., Ho L.S., Lo P.S., Tsang L.L., Liu Y., Lam S.Y., Chan L.N., Zhao W.C., Chung Y.W., Chan H.C. Involvement of CFTR in uterine bicarbonate secretion and the fertilizing capacity of sperm. Nat. Cell Biol. 2003, 5:902-906.
48. Zhang D., Kiyatkin A., Bolin J.T., Low P.S. Crystallographic structure and functional interpretation of the cytoplasmic domain of erythrocyte membrane band 3. Blood 2000, 96:2925-2933.