Reproductive Biology and Endocrinology | |
Glutamate-induced obesity leads to decreased sperm reserves and acceleration of transit time in the epididymis of adult male rats | |
Wilma G Kempinas2  Débora C Damasceno5  Janete A Anselmo-Franci4  Gustavo T Volpato3  Kleber E Campos3  Arielle C Arena2  Glaura SA Fernandes1  | |
[1] Biological Sciences Center, State University of Londrina, UEL, Londrina, PR, Brazil;Department of Morphology, Institute of Biosciences, UNESP - UnivEstadualPaulista, Botucatu, SP, Brazil;Institute of Biological and Health Sciences, Federal University of Mato Grosso, UFMT, Barra do Garça, MT, Brazil;Department of Physiology, Ribeirão Preto Medical School, University of São Paulo, USP, Ribeirão Preto, SP, Brazil;Laboratory of Experimental Research on Gynecology and Obstetrics, Department of Gynecology and Obstetrics, Botucatu Medical School, UNESP - UnivEstadualPaulista, Botucatu, SP, Brazil | |
关键词: Rat; Sperm; Testosterone; Epididymis; Monosodium glutamate; Obesity; | |
Others : 829654 DOI : 10.1186/1477-7827-10-105 |
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received in 2012-08-30, accepted in 2012-11-29, 发布年份 2012 | |
【 摘 要 】
Background
Given the established fact that obesity interferes with male reproductive functions, the present study aimed to evaluate sperm production in the testis and storage in the epididymis in a glutamate-induced model of obesity.
Methods
Male rats were treated neonatally with monosodium glutamate (MSG) at doses of 4 mg/kg subcutaneously, or with saline solution (control group), on postnatal days 2, 4, 6, 8 and 10. On day 120, obesity was confirmed by the Lee index in all MSG-treated rats. After this, all animals from the two experimental groups were anesthetized and killed to evaluate body and reproductive organ weights, sperm parameters, plasma hormone levels (FSH, LH and testosterone), testicular and epididymal histo-morphometry and histopathology.
Results
Significant reductions in absolute and relative weights of testis, epididymis, prostate and seminal vesicle were noted in MSG-treated animals. In these same animals plasma testosterone and follicle-stimulating hormone (FSH) concentrations were decreased, as well as sperm counts in the testis and epididymis and seminiferous epithelium height and tubular diameter. The sperm transit time was accelerated in obese rats. However, the number of Sertoli cells per seminiferous tubule and stereological findings on the epididymis were not markedly changed by obesity.
Conclusions
Neonatal MSG-administered model of obesity lowers sperm production and leads to a reduction in sperm storage in the epididymis of adult male rats. The acceleration of sperm transit time can have implications for the sperm quality of these rats.
【 授权许可】
2012 Fernandes et al.; licensee BioMed Central Ltd.
【 预 览 】
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20140714074713613.pdf | 180KB | download |
【 参考文献 】
- [1]WHO - World Health Organization: World Health Organization. Obesity: preventing and managing the global epidemic. 894. Geneva: WHO Technical Report Series; 2000. Part I: The problem of overweight and obesity
- [2]Pasquali R: Obesity, fat distribution and infertility. Maturitas 2006, 54(4):363-371.
- [3]Visscher TL, Seidell JC: The public health impact of obesity. Annu Rev Public Health 2001, 22(1):355-375.
- [4]Bray GA: Obesity: historical development of scientific and cultural ideas. Int J Obes 1990, 14(11):909-926.
- [5]Strain GW, Zumoff B, Kream J, Strain JJ, Deucher R, Rosenfeld RS, Levin J, Fukushima DK: Mild hypogonadotropichypogonadism in obese men. Metabolism 1982, 31(9):871-875.
- [6]Haffner SM, Valdez RA, Stern MP, Katz MS: Obesity, body fat distribution and sex hormones in men. Int J Obes Relat Metab Disord 1993, 17(11):643-649.
- [7]Magnusdottir EV, Thorsteinsson T, Thorsteinsdottir S, Heimisdottir M, Olafsdottir K: Persistent organochlorines, sedentary occupation, obesity and human male subfertility. Human Reprod 2005, 20(1):208-215.
- [8]Jensen TK, Andersson AM, Jørgensen N, Andersen AG, Carlsen E, Petersen JH, Skakkebæk NE: Body mass index in relation to semen quality and reproductive hormones among 1,558 Danish men. Fertil Steril 2004, 82(4):863-870.
- [9]Sallmen M, Sandler DP, Hoppin JA, Blair A, Baird DD: Reduced fertility among overweight and obese men. Epidemiology 2006, 17(5):520-523.
- [10]Kort HI, Massey JB, Elsner CW, Mitchell-Leef D, Shapiro DB, Witt MA, Roudebush WE: Impact of body mass index values on sperm quantity and quality. J Androl 2006, 27(3):450-452.
- [11]Vigueras-Villaseñor RM, Rojas-Castañeda JC, Chávez-Saldaña M, Gutiérrez-Pérez O, García-Cruz EM, Cuevas-Alpuche O, Reyes-Romero MM, Zambrano E: Alterations in the spermatic function generated by obesity in rats. Acta Histochem 2011, 113(2):214-220.
- [12]York DA: Lessons from animal models of obesity. Endocrinol Metab Clin North Am 1996, 25(4):781-800.
- [13]Sukhanov SN, Andrade IS, Dolnikoff MS, Ferreira A: Neonatal monosodium glutamate treatment alters rat intestinal muscle reactivity to some agonists. Eur J Pharmacol 1999, 386(2–3):247-252.
- [14]Mello MAR, Souza T, Braga LR, Santos W, Ribeiro IA, Gobatto CA: Glucose tolerance and insulin action in monosodium glutamate (MSG) obese exercise-trained rats. Physiol Chem Phys Med NMR 2001, 33(1):63-71.
- [15]Cunha NV, Abreu SB, Panisb C, Grassiollia S, Guarnierb FA, Cecchinib R, Mazzucob TL, Pinge-Filho P, Martins-Pinge MC: Cox-2 inhibition attenuates cardiovascular and inflammatory aspects in monosodium glutamate-induced obese rats. Life Sci 2010, 87:375-381.
- [16]Lyon HN, Hirschhorn JN: Genetics of common forms of obesity: a brief overview. Am J Clin Nutr 2005, 82(1):215S-217S.
- [17]Bueno AA, Oyama LM, Estadella D, Habitante CA, Bernardes BSS, Ribeiro EB, Oller CMN: Lipid metabolism of monosodium glutamate obese rats after partial removal of adipose tissue. Physiol Res 2005, 54(1):57-65.
- [18]França LR, Suescum MO, Miranda JR, Giovambattista A, Perello M, Spinedi E, Calandra RS: Testis structure and function in a nongenetichyperadipose rat model at prepubertal and adult ages. Endocrinology 2006, 147(3):1556-1563.
- [19]Campos KE, Sinzato YK, Pimenta WP, Rudge MVC, Damasceno DC: Effect of maternal obesity on diabetes development in adult rat offspring. Life Sci 2007, 81(19–20):1473-1478.
- [20]Dolnikoff M, Martin-Hidalgo A, Machado UF, Lima FB, Herrera E: Decreased lipolysis and enhanced glycerol and glucose utilization by adipose tissue prior to development of obesity in monosodium glutamate (MSG) treated-rats. Int J Obes Relat Metab Disord 2001, 25(3):426-433.
- [21]Diemen VV, Trindade EN, Trindade MRM: Experimental model to induce obesity in rats. Acta Cir Bras 2006, 21(6):425-429.
- [22]Hermo L, Robaire B: Epididymal cell types and their functions. In The Epididymis – From Molecules to Clinical Practice. Edited by Robaire B, Hinton BT. New York: sKluwer Academic / Plenum Publisher; 2002:81-102.
- [23]Otoya RE, Seltzer AM, Donoso AO: Decrease of (+)-3-[125I]MK-801 binding to NMDA brain receptors revealed at puberty in rats treated neonatally with monosodium glutamate. Brain Res Dev Brain Res 1996, 95(2):149-156.
- [24]Bernardis LL: Prediction of carcass fat, water, and lean body mass from Lee’s “Nutritive Ratio” in rats with hypothalamic obesity. Experientia 1970, 26:789-790.
- [25]Sanabria ER, Pereira MF, Dolninkoff MS, Andrade IS, Ferreira AT, Cavalheiro EA: Deficit in hippocampal long-term potentiation in monosodium glutamate-treated rats. Brain Res Bull 2002, 59(1):47-51.
- [26]Bernardis LL, Patterson BD: Correlation between “Lee index” and carcass fat content in weanling and adult female rats with hypothalamic lesions. J Endocrinol 1968, 40(4):527-528.
- [27]Robb GW, Amann RP, Killian GJ: Daily sperm production and epididymal sperm reserves of pubertal and adult rats. J Reprod Fertil 1978, 54(1):103-107.
- [28]Fernandes GS, Arena AC, Fernandez CDB, Mercadante A, Barbisan LF, Kempinas WG: Reproductive effects in male rats exposed to diuron. ReprodToxicol 2007, 23(1):106-112.
- [29]Ashby J, Tinwell H, Lefevre PA, Joiner R, Haseman J: The effect on sperm production in adult Sprague–Dawley rats exposed by gavage to bisphenol A between postnatal days 91–97. Toxicol Sci 2003, 74(1):129-138.
- [30]Weibel ER: Principles and methods for the morphometric study of the lung and other organs. Lab Invest 1963, 12(1):131-155.
- [31]Leblond CP, Clermont Y: Spermiogenesis of rat, mouse, hamster and guinea pig as revealed by the periodic acid-fuchsin sulfurous acid technique. Am J Anat 1952, 90(2):167-215.
- [32]Kanarek RB, Marks-Kaufman R: Increased carbohydrate consumption induced by neonatal administration of monosodium glutamate to rats. Neuro behav Toxicol Teratol 1981, 3(3):343-350.
- [33]Oida K, Nakai T, Hayashi T, Miyabo S, Takeda R: Plasma lipoproteins of monosodium glutamate-induced obese rats. Int J Obes 1984, 8(5):385-391.
- [34]Papa PC, Vargas AM, Silva JLT, Nunes MT, Machado UF: GLUT4 protein is differently modulated during development of obesity in monosodium glutamate-treated mice. Life Sci 2002, 71(16):1917-1928.
- [35]Mozeš S, Sefeikov Z, Lenhardt L, Racek L: Effect of adrenalectomy on the activity of small intestine enzymes in monosodium glutamate obese rats. Physiol Res 2004, 53(4):415-422.
- [36]Soares A, Schoffen JP, Gouveia EM, Natali MR: Effects of the neonatal treatment with monosodium glutamate on myenteric neurons and the intestine wall in the ileum of rats. J Gastroenterol 2006, 41(7):674-680.
- [37]Broberger C, Johansen J, Johansson C, Schalling M, Hökfelt T: The neuropeptide Y/agouti gene-related protein (AGRP) brain circuitry in normal, anorectic, and monosodium glutamate-treated mice. Proc Natl Acad Sci 1998, 95(25):15043-15048.
- [38]Dawson R, Pelleymounter MA, Millard WJ, Liu S, Eppler B: Attenuation of leptin-mediated effects by monosodium glutamate-induced arcuate nucleus damage. Am J Physiol 1997, 273(1 Pt 1):E202-E206.
- [39]Maletínská L, Toma RS, Pirnik Z, Kiss A, Slaninová J, Haluzík M, Zelezná B: Effect of cholecystokinin on feeding is attenuated in monosodium glutamate obese mice. Regul Pept 2006, 136(1–3):58-63.
- [40]Nakagawa T, Ukai K, Ohyama T, Gomita Y, Okamura H: Effects of chronic administration of sibutramine on body weight, food intake and motor activity in neonatally monosodium glutamate-treated obese female rats: relationship of antiobesity effect with monoamines. Exp Anim 2000, 49:239-249.
- [41]Zenick H, Clegg ED, Perreault SD, Klinefelter GR, Gray LE: Assessment of male reproductive toxicity: a risk assessment approach. In Principles and Methods of Toxicology. 3rd edition. Edited by Hayes AW. New York: Raven; 1994:937-988.
- [42]Dada MO, Blake CA: Administration of monosodium glutamate to neonatal male rats: alterations in the gonadotrophs and in gonadotrophin secretion. Neuroendocrinology 1984, 38(6):490-497.
- [43]Gong SL, Xia FQ, Wei J, Li XY, Sun TH, Lu Z, Liu SZ: Harmful effects of MSG on function of hypothalamus-pituitary-target gland system. Biomed Environ Sci 1995, 8(4):310-317.
- [44]Tena-Sempere M, Pinilla L, Gonzalez LC, Dieguez C, Casanueva FF, Aguilar E: Leptin inhibits testosterone secretion from adult rat testis in vitro. J Endocrinol 1999, 161(2):211-218.
- [45]Badger TM, Millard WJ, Martin JB, Rosenblum PM, Levenson SE: Hypothalamic-pituitary function in adult rats treated neonatally with monosodium glutamate. Endocrinology 1982, 111(6):2031-2038.
- [46]Sridaran R, Rodriguez-Sierra JF, Blake CA: Effects of hypothalamic arcuate nucleus lesions on pulsatile luteinizing hormone concentration in ovariectomized rats. Proc Soc Exp Biol Med 1981, 168(1):38-44.
- [47]Hammoud AO, Gibson M, Peterson CM, Meikle AW, Carrell DT: Impact of male obesity on infertility: a critical review of the current literature. Fertil Steril 2008, 90(4):897-904.
- [48]Orth JM: Cell biology of testicular development in fetus and neonate. In Cell and molecular biology of the testis. Edited by Desjardins C, Ewing LL. New York: Oxford University Press; 1993:3-42.
- [49]Berndtson WE, Igboeli G, Pickett BW: Relationship of absolute numbers of Sertoli cells to testicular size and spermatogenesis in young beef bulls. J AnimSci 1987, 64(1):241-246.
- [50]França LR, Russell LD: The testis of domestic animals. In Male reproduction: a multidisciplinary overview. Edited by Martínez-Garcia F, Regadera J. Madrid: Churchill Communications Europe España; 1998:197-219.
- [51]Kempinas WG, Klinefelter GR: The Epididymis as a Target for Toxicants. In Comprehensive Toxicology. Edited by Charlene A. McQueen: Oxford: Academic Press; 2010:149-166.
- [52]Maffei M, Halaas J, Ravussin E, Pratley RE, Lee GH, Zhang Y, Fei H, Kim S, Lallone R, Ranganathan S: Leptin levels in human and rodent: measurement of plasma leptin and ob RNA in obese and weight reduced subjects. Nat Med 1995, 1(11):1155-1161.
- [53]Considine RV, Sinha MK, Heinman ML, Kriavciunas A, Stephans TW, Nyce MR, Ohannesian JP, Marco CC, McKee LJ, Bauer TL, Caro JF: Serum immunoreactive-leptin concentrations in normal-weight and obese humans. N Engl J Med 1996, 334(5):292-295.
- [54]Fernandez CD, Bellentani FF, Fernandes GS, Perobelli JE, Favareto AP, Nascimento AF, Cicogna AC, Kempinas WD: Diet-induced obesity in rats leads to a decrease in sperm motility. Reprod Biol Endocrinol 2011, 11:9-32.
- [55]Magni P, Motta M, Martini L: Leptin: a possible link between food intake, energy expenditure, and reproductive function. Regul Pepti 2000, 92(1–3):51-56.
- [56]Barash IA, Cheung CC, Weigle DS, Ren H, Kabigting EB, Kuijper JL, Clifton DK, Steiner RA: Leptin is a metabolic signal to the reproductive system. Endocrinology 1996, 137(7):3144-3147.
- [57]Caprio M, Fabbrini E, Isidori AM, Aversa A, Fabbri A: Leptin in reproduction. Trends Endocrinol Metab 2001, 12(2):65-72.
- [58]Smith GD, Jackson LM, Foster DL: Leptin regulation of reproductive function and fertility. Theriogenology 2002, 57(1):73-86.