Structure, function, and localization of aquaporins: Their possible implications on gamete cryopreservation

Genetics and Molecular Research

Volumn 12, Issue 4, 2013, Pages 6718-6732

  Sales, A D ^a   Lobo, C H ^b   Carvalho, A A ^a   Moura, A A ^b   Rodrigues, A P R ^a  

^a STATE UNIVERSITY OF CEARÁ   (Brazil)

^b FEDERAL UNIVERSITY OF CEARÁ   (Brazil)

Author keywords

Aquaporins; Cryopreservation; Cryoprotective agents; Intracellular ice formation; Preantral follicles

Indexed keywords

AQUAPORIN; AQUAPORIN 1; AQUAPORIN 10; AQUAPORIN 2; AQUAPORIN 4; AQUAPORIN 5; AQUAPORIN 6; AQUAPORIN 8; AQUAPORIN 9; MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

CELL MEMBRANE; CELL SURVIVAL; CRYOPRESERVATION; GAMETE; GERM CELL; GRANULOSA CELL; NONHUMAN; OVARY; OVARY FOLLICLE; OVIDUCT; PORCINE MODEL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVIEW; STRUCTURE ACTIVITY RELATION; UTERUS; WATER TRANSPORT;

ANIMALS; AQUAPORINS; BIOLOGICAL TRANSPORT; CELL MEMBRANE; CRYOPRESERVATION; CRYOPROTECTIVE AGENTS; FEMALE; HUMANS; MALE; OVUM; SPERMATOZOA; WATER;

EID: 84890471847     PISSN: None     EISSN: 16765680     Source Type: Journal    
DOI: 10.4238/2013.December.13.5     Document Type: Review

References (61)

1. Agre P and Kozono D (2003). Aquaporin water channels: molecular mechanisms for human diseases. FEBS Lett. 555: 72-78.
2. Badran HH and Hermo LS (2002). 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. 23: 358-373.
3. Branes MC, Morales B, Rios M and Villalon MJ (2005). Regulation of the immunoexpression of aquaporin 9 by ovarian hormones in the rat oviductal epithelium. Am. J. Physiol. Cell Physiol. 288: C1048-C1057.
4. Buffoli B (2010). Aquaporin biology and nervous system. Curr. Neuropharmacol. 8: 97-104.
5. Calamita G, Mazzone A, Bizzoca A and Svelto M (2001). Possible involvement of aquaporin-7 and -8 in rat testis development and spermatogenesis. Biochem. Biophys. Res. Commun. 288: 619-625.
6. Chandar N and Viselli S (2010). Cell and Molecular Biology (Lippincott's illustrated reviews series). International edn. Lippincott Williams & Wilkins, Philadelphia.
7. Chauvigné F, Zapater C and Cerda J (2011). Role of aquaporins during teleost gametogenesis and early Embryogenesis. Front. Physiol. 2: 66.
8. Cheidde L and Schor N (1999). Review: water transporters. Rev. Assoc. Med. Bras. 45: 71-78.
9. Deen PM, Verdijk MA, Knoers NV, Wieringa B, et al. (1994). Requirement of human renal water channel aquaporin-2 for vasopressin-dependent concentration of urine. Science 264: 92-95.
10. Denker BM, Smith BL, Kuhajda FP and Agre P (1988). Identifcation, purifcation, and partial characterization of a novel Mr 28,000 integral membrane protein from erythrocytes and renal tubules. J. Biol. Chem. 263: 15634-15642.
11. Domeniconi RF, Orsi AM, Justulin LA Jr, Beu CC, et al. (2007). Aquaporin 9 (AQP9) localization in the adult dog testis excurrent ducts by immunohistochemistry. Anat. Rec. 290: 1519-1525.
12. Edashige K, Yamaji Y, Kleinhans FW and Kasai M (2003). Artifcial expression of aquaporin-3 improves the survival of mouse oocytes after cryopreservation. Biol. Reprod. 68: 87-94.
13. Faustino LR, Silva CMG, Rossetto R and Rodrigues GQ (2011). Estado atual e desafos da criopreservação de tecido ovariano em mamíferos. Rev. Bras. Reprod. Anim. 35: 3-15.
14. Fujiyoshi Y, Mitsuoka K, de Groot BL, Philippsen A, et al. (2002). Structure and function of water channels. Curr. Opin. Struct. Biol. 12: 509-515.
15. Gomes D, Agasse A, Thiebaud P, Delrot S, et al. (2009). Aquaporins are multifunctional water and solute transporters highly divergent in living organisms. Biochim. Biophys. Acta 1788: 1213-1228.
16. Gorelick DA, Praetorius J, Tsunenari T, Nielsen S, et al. (2006). Aquaporin-11: a channel protein lacking apparent transport function expressed in brain. BMC Biochem. 7: 14.
17. Hamann S, Zeuthen T, la Cour M, Nagelhus EA, et al. (1998). Aquaporins in complex tissues: distribution of aquaporins 1-5 in human and rat eye. Am. J. Physiol. 274: C1332-C1345.
18. Harries WE, Akhavan D, Miercke LJ, Khademi S, et al. (2004). The channel architecture of aquaporin 0 at a 2.2-A resolution. Proc. Natl. Acad. Sci. U. S. A. 101: 14045-14050.
19. Hermo L and Smith CE (2011). Thirsty business: cell, region, and membrane specifcity of aquaporins in the testis, efferent ducts, and epididymis and factors regulating their expression. J. Androl. 32: 565-575.
20. Hermo L, Krzeczunowicz D and Ruz R (2004). Cell specifcity of aquaporins 0, 3, and 10 expressed in the testis, efferent ducts, and epididymis of adult rats. J. Androl. 25: 494-505.
21. Huang HF, He RH, Sun CC, Zhang Y, et al. (2006). Function of aquaporins in female and male reproductive systems. Hum. Reprod. Update 12: 785-795.
22. Ishibashi K (2009). New members of mammalian aquaporins: AQP10-AQP12. Handb. Exp. Pharmacol. 251-262.
23. Ishibashi K, Sasaki S, Fushimi K, Uchida S, et al. (1994). Molecular cloning and expression of a member of the aquaporin family with permeability to glycerol and urea in addition to water expressed at the basolateral membrane of kidney collecting duct cells. Proc. Natl. Acad. Sci. U. S. A. 91: 6269-6273.
24. Ishibashi K, Morinaga T, Kuwahara M, Sasaki S, et al. (2002). Cloning and identifcation of a new member of water channel (AQP10) as an aquaglyceroporin. Biochim. Biophys. Acta 1576: 335-340.
25. Ishii M, Ohta K, Katano T, Urano K, et al. (2011). Dual functional characteristic of human aquaporin 10 for solute transport. Cell. Physiol. Biochem. 27: 749-756.
26. Jablonski EM, McConnell NA, Hughes FM Jr and Huet-Hudson YM (2003). Estrogen regulation of aquaporins in the mouse uterus: potential roles in uterine water movement. Biol. Reprod. 69: 1481-1487.
27. Jensen MO, Tajkhorshid E and Schulten K (2003). Electrostatic tuning of permeation and selectivity in aquaporin water channels. Biophys. J. 85: 2884-2899.
28. Karp G (2002). Cell and Molecular Biology. 3rd edn. John Wiley & Sons, Inc., New York.
29. Kenny DA, Humpherson PG, Leese HJ, Morris DG, et al. (2002). Effect of elevated systemic concentrations of ammonia and urea on the metabolite and ionic composition of oviductal fuid in cattle. Biol. Reprod. 66: 1797-1804.
30. King LS, Choi M, Fernandez PC, Cartron JP, et al. (2001). Defective urinary-concentrating ability due to a complete defciency of aquaporin-1. N. Engl. J. Med. 345: 175-179.
31. Lehninger AL, Nelson DL and Cox MM (2005). Principles of Biochemistry. 4th edn. W.H. Freeman & Co, New York.
32. Lindsay LA and Murphy CR (2007). Aquaporins are upregulated in glandular epithelium at the time of implantation in the rat. J. Mol. Histol. 38: 87-95.
33. Liu J, Xu J, Gu S, Nicholson BJ, et al. (2011). Aquaporin 0 enhances gap junction coupling via its cell adhesion function and interaction with connexin 50. J. Cell Sci. 124: 198-206.
34. Liu K, Nagase H, Huang CG, Calamita G, et al. (2006). Purifcation and functional characterization of aquaporin-8. Biol. Cell 98: 153-161.
35. Mazur P (1970). Cryobiology: the freezing of biological systems. Science 168: 939-949.
36. Mazur P (1984). Freezing of living cells: mechanisms and implications. Am. J. Physiol. 247: C125-C142.
37. McConnell NA, Yunus RS, Gross SA, Bost KL, et al. (2002). Water permeability of an ovarian antral follicle is predominantly transcellular and mediated by aquaporins. Endocrinology 143: 2905-2912.
38. Murai-Hatano M, Kuwagata T, Sakurai J, Nonami H, et al. (2008). Effect of low root temperature on hydraulic conductivity of rice plants and the possible role of aquaporins. Plant Cell Physiol. 49: 1294-1305.
39. Nielsen S, Kwon TH, Christensen BM, Promeneur D, et al. (1999). Physiology and pathophysiology of renal aquaporins. J. Am. Soc. Nephrol. 10: 647-663.
40. Preston GM, Jung JS, Guggino WB and Agre P (1993). The mercury-sensitive residue at cysteine 189 in the CHIP28 water channel. J. Biol. Chem. 268: 17-20.
41. Rall WF (2001). Cryopreservation of Mammalian Embryos, Gametes, and Ovarian Tissues: Current Issues and Progress. In: Assisted Fertilization and Nuclear Transfer in Mammals (Wolf DP and Zelinski-Wooten MB, eds.). 1st edn. Humana Press Inc., Totowa, 173-187.
42. Richard C, Gao J, Brown N and Reese J (2003). Aquaporin water channel genes are differentially expressed and regulated by ovarian steroids during the periimplantation period in the mouse. Endocrinology 144: 1533-1541.
43. Rodgers RJ and Irving-Rodgers HF (2010). Formation of the ovarian follicular antrum and follicular fuid. Biol. Reprod. 82: 1021-1029.
44. Rodriguez A, Catalan V, Gomez-Ambrosi J and Fruhbeck G (2006). Role of aquaporin-7 in the pathophysiological control of fat accumulation in mice. FEBS Lett. 580: 4771-4776.
45. Rojek A, Praetorius J, Frokiaer J, Nielsen S, et al. (2008). A current view of the mammalian aquaglyceroporins. Annu. Rev. Physiol. 70: 301-327.
46. Romeiro RR, Teixeira AL, Silva RMA, De Marco La, et al. (2006). O papel da aquaporina-4 no edema cerebral. Rev. Neucienc. 14: 220-224.
47. Saadoun S, Papadopoulos MC, Davies DC, Krishna S, et al. (2002). Aquaporin-4 expression is increased in oedematous human brain tumours. J. Neurol. Neurosurg. Psychiatr. 72: 262-265.
48. Santos RR (2005). Criopreservação de Folículos Pré-Antrais Ovinos. Doctoral thesis, Faculdade de Medicina Veterinária, UECE, Fortaleza.
49. Savage DF and Stroud RM (2007). Structural basis of aquaporin inhibition by mercury. J. Mol. Biol. 368: 607-617.
50. Skowronski MT, Kwon TH and Nielsen S (2009). Immunolocalization of aquaporin 1, 5, and 9 in the female pig reproductive system. J. Histochem. Cytochem. 57: 61-67.
51. Sohara E, Uchida S and Sasaki S (2009). Function of aquaporin-7 in the kidney and the male reproductive system. Handb. Exp. Pharmacol. 219-231.
52. Steinfeld S, Cogan E, King LS, Agre P, et al. (2001). Abnormal distribution of aquaporin-5 water channel protein in salivary glands from Sjogren's syndrome patients. Lab. Invest. 81: 143-148.
53. Tait MJ, Saadoun S, Bell BA and Papadopoulos MC (2008). Water movements in the brain: role of aquaporins. Trends Neurosci. 31: 37-43.
54. Thoroddsen A, Dahm-Kahler P, Lind AK, Weijdegard B, et al. (2011). The water permeability channels aquaporins 1-4 are differentially expressed in granulosa and theca cells of the preovulatory follicle during precise stages of human ovulation. J. Clin. Endocrinol. Metab. 96: 1021-1028.
55. Tsubota K, Hirai S, King LS, Agre P, et al. (2001). Defective cellular traffcking of lacrimal gland aquaporin-5 in Sjogren's syndrome. Lancet 357: 688-689.
56. Tsukaguchi H, Shayakul C, Berger UV, Mackenzie B, et al. (1998). Molecular characterization of a broad selectivity neutral solute channel. J. Biol. Chem. 273: 24737-24743.
57. Verkman AS (2005). More than just water channels: unexpected cellular roles of aquaporins. J. Cell Sci. 118: 3225-3232.
58. Verkman AS and Mitra AK (2000). Structure and function of aquaporin water channels. Am. J. Physiol. Renal Physiol. 278: F13-F28.
59. Wan X, Steudle E and Hartung W (2004). Gating of water channels (aquaporins) in cortical cells of young corn roots by mechanical stimuli (pressure pulses): effects of ABA and of HgCl2. J. Exp. Bot. 55: 411-422.
60. Yakata K, Tani K and Fujiyoshi Y (2011). Water permeability and characterization of aquaporin-11. J. Struct. Biol. 174: 315-320.
61. Yamaji Y, Valdez DM Jr, Seki S, Yazawa K, et al. (2006). Cryoprotectant permeability of aquaporin-3 expressed in Xenopus oocytes. Cryobiology 53: 258-267.