Theriogenology
Volume 74, Issue 9 , Pages 1661-1669 , December 2010

Undernutrition during foetal to prepubertal life affects aquaporin 9 but not aquaporins 1 and 2 expression in the male genital tract of adult rats

  • S. Arrighi

      Affiliations

    • Department of Veterinary Sciences and Technologies for Food Safety, Laboratory of Anatomy, Università degli Studi di Milano, Italy
    • Corresponding Author InformationCorresponding author. Tel.: +39.0250315741; fax: +39.0250315771
  • ,
  • M. Aralla

      Affiliations

    • Department of Veterinary Sciences and Technologies for Food Safety, Laboratory of Anatomy, Università degli Studi di Milano, Italy
  • ,
  • P. Genovese

      Affiliations

    • Department of Morphology and Development, Veterinary Faculty, University of Uruguay, Montevideo, Uruguay
  • ,
  • N. Picabea

      Affiliations

    • Department of Morphology and Development, Veterinary Faculty, University of Uruguay, Montevideo, Uruguay
  • ,
  • A. Bielli

      Affiliations

    • Department of Morphology and Development, Veterinary Faculty, University of Uruguay, Montevideo, Uruguay

Received 9 March 2010 ,Revised 23 June 2010 ,Accepted 29 June 2010.

References 

  1. McCance RA. Food, growth and time. Lancet. 1962;2:271–272
  2. Barker DJ, Winter PD, Osmond C, Margetts B, Simmonds SJ. Weight in infancy and death from ischaemic heart disease. Lancet. 1989;334:577–580
  3. Barker DJ. Maternal nutrition, fetal nutrition, and disease in later life. Nutrition. 1997;13:807–813
  4. Bateson P, Barker D, Clutton-Brock T, Deb D, D'Udine B, Foley RA, et al. Developmental plasticity and human health. Nature. 2004;430:419–421
  5. Nijland MJ, Ford SP, Nathanielsz PW. Prenatal origins of adult disease. Curr Opin Obstet Gynecol. 2008;20:132–138
  6. Lucas A. Long-term programming effects of early nutrition - Implications for the preterm infant. J Perinatol. 2005;25:S2–S6Review
  7. Gardner DS, Ozanne SE, Sinclair KD. Effect of the early-life nutritional environment on fecundity and fertility of mammals. Phil Trans R Soc B. 2009;364:3419–3427Review
  8. Rhind SM. Effects of maternal nutrition on fetal and neonatal reproductive development and function. Anim Reprod Sci. 2004;82/83:169–181
  9. Rhind SM, Rae MT, Brooks AN. Effects of nutrition and environmental factors on the fetal programming of the reproductive axis. Reproduction. 2001;122:205–214Review
  10. Jung JS, Bhat RV, Preston GM, Guggino WB, Baraban JM, Agre P. Molecular characterization of an aquaporin cDNA from brain: candidate osmoreceptor and regulator of water balance. Proc Natl Acad Sci USA. 1994;91:13052–13056
  11. Agre P, King LS, Yasui M, Guggino WB, Ottersen OP, Fujiyoshi Y, et al. Aquaporin water channel-from atomic structure to clinical medicine. J Physiol. 2002;542:3–16
  12. 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
  13. Huang HF, He RH, Sun CC, Zhang Y, Meng QX, Ma YY. Function of aquaporins in female and male reproductive systems. Hum Reprod Update. 2006;12:785–795
  14. 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
  15. Hermo L, Krzeczunowicz D, Ruz R. Cell specificity of aquaporins 0, 3, and 10 expressed in the testis, efferent ducts, and epididymis of adult rats. J Androl. 2004;25:494–505
  16. Hermo L, Schellenberg M, Liu LY, Dayanandan B, Zhang T, Mandato CA, et al. Membrane domain specificity in the spatial distribution of aquaporins 5, 7, 9, and 11 in efferent ducts and epididymis of rats. J Histochem Cytochem. 2008;56:1121–1135
  17. Da Silva N, Piétrement C, Brown D, Breton S. Segmental and cellular expression of aquaporins in the male excurrent duct. Biochim Biophys Acta. 2006;1758:1025–1033
  18. Da Silva N, Silberstein C, Beaulieu V, Piétrement C, Van Hoek AN, Brown D, et al. Postnatal expression of aquaporins in epithelial cells of the rat epididymis. Biol Reprod. 2006;74:427–438
  19. Pastor-Soler N, Bagnis C, Sabolic I, Tyszkowski R, McKee M, Van Hoek A, et al. Aquaporin 9 expression along the male reproductive tract. Biol Reprod. 2001;65:384–393
  20. Fisher JS, Turner KJ, Fraser HM, Saunders PTK, Brown D, Sharpe M. Immunoexpression of aquaporin-1 in the efferent ducts of the rat and marmoset monkey during development, its modulation by estrogens, and its possible role in fluid resorption. Endocrinology. 1998;139:3935–3945
  21. Pastor-Soler N, Isnard-Bagnis C, Herak-Kramberger C, Sabolic I, Van Hoek A, Brown D, et al. Expression of aquaporin 9 in the adult rat epididymal epithelium is modulated by androgens. Biol Reprod. 2002;66:1716–1722
  22. Oliveira CA, Carnes K, França LR, Hermo L, Hess RA. Aquaporin-1 and -9 are differentially regulated by oestrogen in the efferent ductule epithelium and initial segment of the epididymis. Biol Cell. 2005;97:385–395
  23. Picciarelli-Lima P, Oliveira AG, Reis AM, Kalapothakis E, Mahecha GA, Hess RA, et al. Effects of 3-beta-diol, an androgen metabolite with intrinsic estrogen-like effects, in modulating the aquaporin-9 expression in the rat efferent ductules. Reprod Biol Endocrinol. 2006;4:51–61
  24. Genovese P, Núñez M, Pombo C, Bielli A. Undernutrition during foetal and post-natal life affects testicular structure and reduces the number of Sertoli cells in the adult rat. Reprod Domest Anim. 2009;
  25. Aralla M, Borromeo V, Groppetti D, Secchi C, Cremonesi F, Arrighi S. A collaboration of aquaporins handles water transport in relation to the estrous cycle in the bitch uterus. Theriogenology. 2009;72:310–321
  26. Arrighi S, Ventriglia G, Aralla M, Zizza S, Di Summa A, Desantis S. Absorptive activities of the efferent ducts evaluated by the immunolocalization of aquaporin water channels and lectin histochemistry in adult cats. Histol Histopathol. 2010;25:433–444
  27. Genovese P, Núñez ME, Picabea N, Pombo C, Bielli A. Rats underfed during fetal to prepubertal life have lighter testes and epididymides, fewer Sertoli cells, but moderate histological changes in the epididymis. Reprod Dom Anim. 2008;43(suppl 3):161
  28. Hamilton DW. Structure and function of the epithelium lining the ductuli efferentes, ductus epididymis and ductus deferens in the rat. In Handbook of Physiology. Section 7: Endocrinology. Vo. V: Male reproductive system. Am Physiol Soc, Washington. 1975. p. 259–301.
  29. Cornwall GA. New insights into epididymal biology and function. Hum Reprod Update. 2009;15:213–227
  30. Arrighi S, Romanello MG, Domeneghini C. Morphological examination of epididymal epithelium in the mule (E. hinnus) in comparison with parental species (E. asinus and E. caballus). Histol Histopathol. 1991;6:325–337
  31. Flickinger CJ, Bush LA, Howards SS, Herr JC. Distribution of leukocytes in the epithelium and interstitium of four regions of the Lewis rat epididymis. Anat Rec. 1997;248:380–390
  32. Da Silva N, Shum WWC, Breton S. Regulation of vacuolar proton pumping ATPase-dependent luminal acidification in the epididymis. Asian J Androl. 2007;9:476–482
  33. Hamilton DW. The epididymis as a possible site for control of fertility in the male. Adv Biosci. 1973;10:127–144
  34. Agre P, Brown D, Nielsen S. Aquaporin water channels: unanswered questions and unresolved controversies. Curr Opin Cell Biol. 1995;7:472–483
  35. Domeniconi RF, Orsi AM, Justulin LA, Leme Beu CC, Felisbino SL. Immunolocalization of aquaporins 1, 2 and 7 in rete testis, efferent ducts, epididymis and vas deferens of adult dog. Cell Tissue Res. 2008;332:329–335
  36. Stevens AL, Breton S, Gustafson CE, Bouley R, Nelson RD, Kohan DE, et al. Aquaporin 2 is a vasopressin-independent, constitutive apical membrane protein in rat vas deferens. Am J Physiol Cell Physiol. 2000;278:C791–C802
  37. Bielli A, Pérez R, Pedrana G, Milton JT, Lopez A, Blackberry MA, et al. Low maternal nutrition during pregnancy reduces the number of Sertoli cells in the newborn lamb. Reprod Fertil Dev. 2002;14:333–337
  38. Kotsampasi B, Balaskas C, Papadomichelakis G, Chadio SE. Reduced Sertoli cell number and altered pituitary responsiveness in male lambs undernourished in utero. Anim Reprod Sci. 2009;114:135–147
  39. Sharpe RM, McKinnell C, Kivlin C, Fiser JS. Proliferation and functional maturation of Sertoli cells. Reproduction. 2003;125:769–784Review
  40. Marty MS, Chapin RE, Parks LG, Thorsrud BA. Development and Maturation of the Male Reproductive System. Birth Defects Res B Dev Reprod Toxicol. 2003;68:125–136
  41. Rae MT, Kyle CE, Miller DW, Hammond AJ, Brooks AN, Rhind SM. The effects of undernutrition, in utero, on reproductive function in adult male and female sheep. Anim Reprod Sci. 2002;72:63–71
  42. Rojek AM, Skowronski MT, Fuchtbauer EM, Fuchtbauer AC, Fenton RA, Agre P, et al. Defective glycerol metabolism in aquaporin 9 (AQP9) knockout mice. Proc Natl Acad Sci USA. 2007;104:3609–3614

PII: S0093-691X(10)00357-2

doi: 10.1016/j.theriogenology.2010.06.039

Theriogenology
Volume 74, Issue 9 , Pages 1661-1669 , December 2010