Histomorphometric evaluation of the testicular parenchyma of rats submitted to protein restriction during intrauterine and postnatal life

Histomorphometric evaluation of the testicular parenchyma of rats submitted to protein restriction during intrauterine and postnatal life

The critical period of development is highly susceptible to disorders. Environmental contaminants, stress, and poor nutrition may permanently affect structurally and functionally an organism during adulthood. Protein restriction in intrauterine and neonatal periods may impair testicular cells and reduce steroidogenic activity. The current study investigated the effect of low protein diet during intrauterine and postnatal life on testicular function in immature and adult rats. Pregnant Wistar rats were fed either a normal protein diet or a low protein diet during pregnancy until birth and during lactation until weaning. The results showed that undernutrition during intrauterine life reduced epithelium height, tubular volume, Leydig cell volume, and serum testosterone levels, although it increased the support capacity of Sertoli cells. Tubular diameter, tubular volume, epithelium height, and Leydig cell population decreased when protein was restricted during lactation. Pregnant rats submitted to a low protein diet during the two periods generated male rats with a reduction in seminiferous tubule volume and length, Sertoli cell population, Leydig cell population and volume, and sperm production. Undernutrition during both the intrauterine and postnatal periods caused the most drastic testicular effects, as irreversible damage to Sertoli cell population and, consequently, to sperm production in the adult male.

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  • Abercrombie M (1946). Estimation of nuclear populations from microtome sections. Anat Rec 94: 238-248.
  • Almeida FRCL (2009). Sow nutrition and its implication on the quality of the piglet at birth. Acta Sci Vet 37: 31-33 (article in Portuguese with an abstract in English).
  • Amann RP, Almquist JO (1962). Reproductive capacity of dairy bulls. VIII. Direct and indirect measurement of testicular sperm production. J Dairy Sci 45: 774-781.
  • Ariyaratne HBS, Mendis-Handagama SMLC, Hales DB, Mason JI (2000). Studies on the onset of Leydig precursor cell differentiation in the prepubertal rat testis. Biol Reprod 63: 165-171.
  • Barker DJP, Clark PM (1997). Fetal undernutrition and disease in later life. Rev Reprod 2: 105-112.
  • Benton L, Shan LX, Hardy MP (1995). Differentiation of adult Leydig cells. J Steroid Biochem Mol Biol 53: 61-68.
  • Brown J, Walker SE, Steinmain K (2004). Endocrine manual for the reproductive assessment of domestic and non-domestics species. Smithsonian’s National Zoological Park, Virginia, EUA.
  • Caldeira BC, Paula TAR, Matta SLP, Balarini MK, Campos PKA (2010). Morphometry of testis and seminiferous tubules of the adult crab-eating fox (Cerdocyon thous, Linnaeus, 1766). Rev Ceres 57: 569-575.
  • Caron E, Ciofi P, Prevot V, Bouret SG (2012). Alteration in neonatal nutrition causes perturbations in hypothalam neural circuits controlling reproductive function. J Neurosci 32: 11486-11494.
  • Chen H, Ge RS, Zirkin BR (2009). Leydig cells: From stem cells to aging. Mol Cell Endocrinol 306: 9-16.
  • Delbés G, Duquenne C, Szenker J, Taccoen J, Habert R, Levacher C (2007). Developmental changes in testicular sensitivity to estrogens throughout fetal and neonatal life. Toxicol Sci 99: 234-243.
  • Engelbregt MJT, Houdijk MECAM, Popp-Snijders C, DelemarreVan de Waal HA (2000). The effects of intra-uterine growth retardation and postnatal undernutrition on onset of puberty in male and female rats. Pediatr Res 48: 803-807.
  • Ewing LL, Zirkin BR, Cochran RC, Kromann N, Peters C, RuizBravo N (1979). Testosterone secretion by rat, rabbit, guinea pig, dog, and hamster testes perfused in vitro: correlation with Leydig cell mass. Endocrinology 105: 1135-1142.
  • França LR, Avelar GF, Almeida FFL (2005). Spermatogenesis and sperm transit through the epididymis in mammals with emphasis on pigs. Theriogenology 63: 300-318.
  • França LR, Russell LD (1998). The testis of domestic mammals. In: Martínez-Garcia F, Regadera J, editors. Male Reproduction: a Multidisciplinary Overview. Madrid, Spain: Churchill Communications, pp. 198-219.
  • Ge RS, Hardy MP (1997). Decreased cyclin A2 and increased cyclin G1 levels coincide with loss of proliferative capacity in rat Leydig cells during pubertal development. Endocrinology 138: 3719-3726.
  • Genovese P, Núñez ME, Pombo C, Bielli A (2010). Undernutrition during foetal and post-natal life affects testicular structure and reduces the number of Sertoli cells in the adult rat. Reprod Domest Anim 45: 233-236.
  • Godfrey KM, Barker DJP (2001). Fetal programming and adult health. Public Health Nutr 4: 611-624.
  • Guzmán C, Cabrera R, Cárdenas M, Larrea F, Nathanielsz PW, Zambrano E (2006). Protein restriction during fetal and neonatal development in the rat alters reproductive function and accelerates reproductive ageing in female progeny. J Physiol 572: 97-108.
  • Hales CN, Barker DJ (1992). Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia 35: 595-601.
  • Harding JE, Derraik JGB, Bloomfield FH (2010). Maternal undernutrition and endocrine development. Expert Rev Endocrinol Metab 5: 297-312.
  • Hess RA, França LR (2008). Spermatogenesis and cycle of the seminiferous epithelium. Adv Exp Med Biol 636: 1-15.
  • Lejeune H, Habert R, Saez JM (1998). Origin, proliferation and differentiation of Leydig cells. J Mol Endocrinol 20: 1-25.
  • Léonhardt M, Lesage J, Croix D, Dutriez-Casteloot I, Beauvillain JC, Dupouy JP (2003). Effects of perinatal maternal food restriction on pituitary-gonadal axis and plasma leptin level in rat pup at birth and weaning and on timing of puberty. Biol Reprod 68: 390-400.
  • Lucyk JM, Furumoto RV (2008). Food consumption and nutritional needs of pregnancy: a revision. Com Ciências Saúde 19: 353-363 (article in Portuguese with an abstract in English).
  • Melo MC, Almeida FRCL, Caldeira-Brant AL, Parreira GG, Chiarini-Garcia H (2014). Spermatogenesis recovery in protein-restricted rats subjected to a normal protein diet after weaning. Reprod Fertil Dev 26: 787-796.
  • Mendis-Handagama SM, Ariyaratne HB (2001). Differentiation of the adult Leydig cell population in the postnatal testis. Biol Reprod 65: 660-671.
  • Mendis-Handagama SM, Zirkin BR, Ewing LL (1988). Comparison of components of the testis interstitium with testosterone secretion in hamster, rat, and guinea pig testes perfused in vitro. Am J Anat 181: 12-22.
  • Menendez-Patterson A, Menendez E, Fernandez S, Fernandez M, Marín B (1985). Influence of undernutrition during gestation and suckling on development and sexual maturity in the rat. J Nutr 115: 1025-1032.
  • Monteiro JC, Matta SLP, Predes FS, Paula TAR (2012). Testicular morphology of adult Wistar rats treated with Rudgea viburnoides (Cham.) Benth. leaf infusion. Braz Arch Biol Technol 55: 101-105.
  • Navarro RD, De Paula TAR, Matta SLP, Fonseca CC, Neves MTD (2004). Effect of low intensity ultrasound exposure in perinatal period on the Leydig cell and other components of the intertubular space in adult mouse testis. Rev Ceres 51: 445-455 (article in Portuguese with an abstract in English).
  • Nef S, Parada LF (2000). Hormones in male sexual development. Genes Dev 14: 3075-3086.
  • Orth JM (1982). Proliferation of Sertoli cells in fetal and postnatal rats: a quantitative autoradiographic study. Anat Rec 203: 485- 492.
  • Orth JM (1993). Cell biology of testicular development in fetus and neonate. In: Desjardins C, Ewing LL, editors. Cell and Molecular Biology of the Testis. New York, NY, USA: Oxford University Press, pp. 3-42.
  • Queiroz GCD, Oliveira VVG, Gueiros OG, Torres SM, Maia FCL, Tenorio BM, Morais RN, Silva Junior VA (2013). Effect of pentoxifylline on the regeneration of rat testicular germ cells after heat shock. Anim Reprod 10: 45-54.
  • Rae MT, Rhind SM, Kyle CE, Miller DW, Brook AN (2002). Maternal undernutrition alters triiodothyronine concentrations and pituitary response to GnRH in fetal sheep. J Endocrinol 173: 449-455.
  • Rocha DCM, Debeljuk L, França LR (1999). Exposure to constant light during testis development increase daily sperm production in adult Wistar rats. Tissue Cell 31: 372-379. Rodríguez-González GL, Vigueras-Villaseñor RM, Millán S, Moran N, Trejo R, Nathanielsz PW, Larrea F, Zambrano E (2012). Maternal protein restriction in pregnancy and/or lactation affects seminiferous tubule organization in male rat offspring. J Dev Orig Health Dis 3: 1-6.
  • Roseboom TJ, Van Der Meulen JHP, Ravelli ACJ, Osmond C, Barker DJP, Bleker OP (2001). Effects of prenatal exposure to the Dutch famine on adult disease in later life: an overview. Mol Cell Endocrinol 185: 93-98.
  • Russell LD, França LR (1995). Building a testis. Tissue Cell 27: 129- 147.
  • Sharpe RM (1994). Regulation of spermatogenesis. In: Knobil E, Nelly JD, editors. The Physiology of Reproduction. New York, NY, USA: Raven Press, pp. 1363-1434.
  • Sharpe RM, McKinnell C, Kivlin C, Fisher JS (2003). Proliferation and functional maturation of Sertoli cells, and their relevance to disorders of testis function in adulthood. Reproduction 125: 769-784.
  • Sharpe RM, Walker M, Millar MR, Atanassova N, Morris K, McKinnell C, Saunders PTK, Fraser HM (2000). Effect of neonatal gonadotropin-releasing hormone antagonist administration on Sertoli cell number and testicular development in the marmoset: comparison with the rat. Biol Reprod 62: 1685-1693.
  • Silva AAN, Oliveira JS, Oliveira RR, Moraes SRA, Silva Junior VA, Neves EM (2014). Evaluation of quantitative parameters of Leydig cell in diabetic adults rats. Acta Sci Biol Sci 36: 483-489.
  • Silva Junior VA, Vieira AC, Pinto CF,  De Paula TA, Palma MB, Lins Amorim MJ, Amorim Junior AA, Manhães-de-Castro R (2006). Neonatal treatment with naloxone increases the population of Sertoli cells and sperm production in adult rats. Reprod Nutr Dev 46: 157-166.
  • Stoker TE, Laws SC, Guidici DL, Cooper RL (2000). The effects of atrazine metabolites on puberty and thyroid function in the male Wistar rat. Toxicol Sci 58: 50-59. Takashiba KS, Segatelli TM, Moraes SMF, Natali MRM (2011). Testicular morphology in obese and sedentary Wistar rats submitted to physical training. Acta Sci Health Sci 33: 25-33 (article in Portuguese with an abstract in English).
  • Teixeira CV, Silandre D, Souza Santos AM, Delalande C, Sampaio FJ, Carreau S, Fonte Ramos C (2007). Effects of maternal undernutrition during lactation on aromatase, estrogen, and androgen receptors expression in rat testis at weaning. J Endocrinol 192: 301-311.
  • Tenorio BM,  Jimenez GC,  Morais RN,  Torres SM,  Albuquerque Nogueira R, Silva Junior VA (2010). Testicular development evaluation in rats exposed to 60Hz and 1mT electromagnetic field. J Appl Toxicol 31: 223-230.
  • Toledo FC, Perobelli JE, Pedrosa FPC, Anselmo-Franci JÁ, Kempinas WDG (2011). In utero protein restriction causes growth delay and alters sperm parameters in adult male rats. Reprod Biol Endocrinol 9: 94-102.
  • Widdowson EM, McCance RA (1975). A review: new thought on growth. Pediatr Res 9: 154-156.
  • Zambrano E, Rodríguez-González GL, Guzmán C, García-Becerra R, Boeck L, Díaz L, Menjivar M, Larrea F, Nathanielsz PW (2005). A maternal low protein diet during pregnancy and lactation in the rat impairs male reproductive development. J Physiol 563: 275-284.
  • Zirkin BR, Ewing LL, Kromann N, Cochran RC (1980). Testosterone secretion by rat, rabbit, guinea pig, dog, and hamster testes perfused in vitro: correlation with Leydig cell ultrastructure. Endocrinology 107: 1867-1874.
Turkish Journal of Biology-Cover
  • ISSN: 1300-0152
  • Yayın Aralığı: Yılda 6 Sayı
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