Obesity causes weight increases in prepubertal and pubertal male offspring and is related to changes in spermatogenesis and sperm production in rats
Harish Navya A and Hanumant Narasinhacharya Yajurvedi A B
+ Author Affiliations
- Author Affiliations
A Department of Zoology, University of Mysore, Manasagangotri, Mysore 570 006, Karnataka, India.
B Corresponding author. Email: hnyajurvedi@rediffmail.com
Reproduction, Fertility and Development 29(4) 815-823 https://doi.org/10.1071/RD15480
Submitted: 16 May 2015 Accepted: 6 December 2015 Published: 15 February 2016
Abstract
The effect of obesity on testicular activity in prepubertal and pubertal rats was investigated in the present study. Obesity was induced in adult females by feeding a high-calorie diet (HCD). These females were mated with normal males and were fed an HCD during pregnancy and lactation. The male offspring born to obese mothers and fed an HCD after weaning were found to be obese. Seminiferous tubules of offspring from control mothers (OCM) and offspring from HCD-fed mothers (OHCDM) had the same set of germ cells at different age intervals, namely spermatogonia, leptotene spermatocytes, zygotene spermatocytes, pachytene spermatocytes and round and elongated spermatids on postnatal days (PND) 7, 13, 17, 24 and 36, and on the day of preputial separation, respectively. However, there was a significant decrease in round and elongated spermatids and the epididymal sperm count, coupled with a significant decrease in testosterone and an increase in leptin serum concentrations in OHCDM compared with OCM. These results show that obesity in prepubertal rats does not affect the age-dependent appearance of germ cells according to developmental hierarchy, but it does interfere with spermatid formation, resulting in a reduced sperm count, which may be due to a deficiency of testosterone mediated by hyperleptinaemia.
Additional keywords: abnormal spermatozoa, dam’s obesity, high calorie diet, leptin, preputial separation, spermatid, sperm count, testosterone.
References
Aggerholm, A. S., Thulstrup, A. M., Toft, G., Ramlau-Hansen, C. H., and Bonde, J. P. (2008). Is overweight a risk factor for reduced semen quality and altered serum sex hormone profile? Fertil. Steril. 90, 619–626.| Is overweight a risk factor for reduced semen quality and altered serum sex hormone profile?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtF2qsb7K&md5=c9877cc0a0e07025cc81027f214de1ceCAS | 18068160PubMed |
Ahima, R. S., Dushay, J., Flier, S. N., Prabakaran, D., and Flier, J. S. (1997). Leptin accelerates the onset of puberty in normal female mice. J. Clin. Invest. 99, 391–395.
| Leptin accelerates the onset of puberty in normal female mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhtVKksbw%3D&md5=6e17e345b028a161571590f361d1822dCAS | 9022071PubMed |
Ahmad, N., Biswas, S., Bae, S., Meador, K. E., Huang, R., and Singh, K. P. (2009). Association between obesity and asthma in US children and adolescents. J. Asthma 46, 642–646.
| Association between obesity and asthma in US children and adolescents.Crossref | GoogleScholarGoogle Scholar | 19728197PubMed |
Alhashem, F., Alkhateeb, M., Alshahrani, M., Elrefaey, H., Alsunaidi, M., Alessa, R., Sakr, H., Sarhan, M., Eleawa, S. M., and Khalil, M. A. (2014). Exercise protects against obesity induced semen abnormalities via downregulating stem cell factor, upregulating ghrelin and normalizing oxidative stress. EXCLI J. 13, 551–572.
| 26417283PubMed |
Bakos, H. W., Mitchell, M., Setchell, B. P., and Lane, M. (2011). The effect of paternal diet induced obesity on sperm function and fertilization in a mouse model. Int. J. Androl. 34, 402–410.
| The effect of paternal diet induced obesity on sperm function and fertilization in a mouse model.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlOlu7fP&md5=07814560ba0e86335682456285678fc1CAS | 20649934PubMed |
Barham, D., and Trinder, P. (1972). An improved color reagent for the determination of blood glucose by the oxidase system. Analyst 97, 142–145.
| An improved color reagent for the determination of blood glucose by the oxidase system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE38XhtlOks7Y%3D&md5=de8f6f656f209aeac371bedff197c5afCAS | 5037807PubMed |
Bataineh, H. N., and Nusier, M. K. (2005). Effect of cholesterol diet on reproductive function in male albino rats. Saudi Med. J. 26, 398–404.
| 15806207PubMed |
Caprio, M., Fabbrini, E., Ricci, G., Basciani, S., Gnessi, L., Arizzi, M., Carta, A. R., De Martino, M. U., Isidori, A. M., Frajese, G. V., and Fabbri, A. (2003). Ontogenesis of leptin receptor in rat Leydig cells. Biol. Reprod. 68, 1199–1207.
| Ontogenesis of leptin receptor in rat Leydig cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXisVertL4%3D&md5=7f2b2a7e43b77735700cb3aff74a5443CAS | 12606446PubMed |
Chavarro, J. E., Toth, T. L., Wright, D. L., Meeker, J. D., and Hauser, R. (2010). Body mass index in relation to semen quality, sperm DNA integrity, and serum reproductive hormone levels among men attending an infertility clinic. Fertil. Steril. 93, 2222–2231.
| Body mass index in relation to semen quality, sperm DNA integrity, and serum reproductive hormone levels among men attending an infertility clinic.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXms1yls7c%3D&md5=c163a8b9dc3ac8360e62ab97f5ec0a52CAS | 19261274PubMed |
Chen, X. L., Gong, L. Z., and Xu, J. X. (2013). Antioxidative activity and protective effect of probiotics against high-fat diet induced sperm damage in rats. Animal 7, 287–292.
| Antioxidative activity and protective effect of probiotics against high-fat diet induced sperm damage in rats.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3s%2FitVarsQ%3D%3D&md5=ce8ba1aecb15f7c70f84fca195b87900CAS | 23031185PubMed |
Clermont, Y. (1972). Kinetics of spermatogenesis in mammals: seminiferous epithelium cycle and spermatogonial renewal. Physiol. Rev. 52, 198–236.
| 1:STN:280:DyaE38%2FntVSntw%3D%3D&md5=ef7f61c6a0508063e86772bd83529188CAS | 4621362PubMed |
Du Plessis, S. S., Cabler, S., McAlister, D. A., Sabanegh, E., and Agarwal, A. (2010). The effect of obesity on sperm disorders and male infertility. Nat. Rev. Urol. 7, 153–161.
| The effect of obesity on sperm disorders and male infertility.Crossref | GoogleScholarGoogle Scholar | 20157305PubMed |
Duale, N., Steffensen, I. L., Andersen, J., Brevik, A., Brunborg, G., and Lindeman, B. (2014). Impaired sperm chromatin integrity in obese mice. Andrology 2, 234–243.
| Impaired sperm chromatin integrity in obese mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXjtlOlsLc%3D&md5=2c363fd2e354c6c54a1c859076323afaCAS | 24459046PubMed |
Fernandez, C. D., Bellentani, F. F., Fernandes, G. S., Perobelli, J. E., Favareto, A. P., Nascimento, A. F., Cicogna, A. C., and Kempinas, W. D. G. (2011). Diet-induced obesity in rats leads to a decrease in sperm motility. Reprod. Biol. Endocrinol. 9, 32.
| Diet-induced obesity in rats leads to a decrease in sperm motility.Crossref | GoogleScholarGoogle Scholar | 21396114PubMed |
Freedman, D. S., Khan, L. K., Dietz, W. H., Srinivasan, S. R., and Berenson, G. S. (2001). Relation of childhood obesity to coronary disease risk factors in adulthood. Pediatrics 108, 712–718.
| Relation of childhood obesity to coronary disease risk factors in adulthood.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MvptFSktg%3D%3D&md5=37f8c7f728b25d9719266607c4a505ebCAS | 11533341PubMed |
Galgani, J., and Ravussin, E. (2008). Energy metabolism, fuel selection and body weight regulation. Int. J. Obes. 32, S109–S119.
| Energy metabolism, fuel selection and body weight regulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXksl2kuw%3D%3D&md5=68956cff1365b58dca383d38516940b6CAS |
Gaytan, F., Bellido, C., Aquilar, R., and Aquilar, E. (1988). Balano-preputial separation as an external sign of puberty in the rat: correlated with histologic testicular data. Andrologia 20, 450–453.
| Balano-preputial separation as an external sign of puberty in the rat: correlated with histologic testicular data.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1M%2Fos1Kluw%3D%3D&md5=b6fc2ce5b0752dff88871ada67397e92CAS | 3207205PubMed |
Ghanayem, B. I., Bai, R., Kissling, G. E., Travlos, G., and Hoffler, U. (2010). Diet-induced obesity in male mice is associated with reduced fertility and potentiation of acrylamide-induced reproductive toxicity. Biol. Reprod. 82, 96–104.
| Diet-induced obesity in male mice is associated with reduced fertility and potentiation of acrylamide-induced reproductive toxicity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1WgsrrK&md5=d6fb4d30d8da4ce8241d2525cc5579c7CAS | 19696015PubMed |
Hammoud, A. O., Gibson, M., Peterson, C. M., Hamilton, B. D., and Carrell, D. T. (2006). Obesity and male reproductive potential. J. Androl. 27, 619–626.
| Obesity and male reproductive potential.Crossref | GoogleScholarGoogle Scholar | 16751621PubMed |
Hammoud, A. O., Gibson, M., Peterson, C. M., Meikle, A. W., and Carrell, D. T. (2008). Impact of male obesity on infertility: a critical review of the current literature Obesity and male infertility. Fertil. Steril. 90, 897–904.
| Impact of male obesity on infertility: a critical review of the current literature Obesity and male infertility.Crossref | GoogleScholarGoogle Scholar | 18929048PubMed |
Haron, M. N., D’Souza, U. J. A., Jaafar, H., Zakaria, R., and Singh, H. J. (2010). Exogenous leptin administration decreases sperm count and increases the fraction of abnormal sperm in adult rats. Fertil. Steril. 93, 322–324.
| Exogenous leptin administration decreases sperm count and increases the fraction of abnormal sperm in adult rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXit1WmtLg%3D&md5=59faf32dffb5e4577798a036b6448292CAS | 19709655PubMed |
Herbert, K. (1984). Lipids. In ‘Clinical Chemistry; Theory, Analysis and Co-relation’. (Eds L. A. Kaplar and A. J. Pesce.) pp. 1182–1230. (CV Mosby: Toronto.)
I’Anson, H., Foster, D. L., Foxcroft, G. R., and Booth, P. J. (1991). Nutrition and reproduction. Oxf. Rev. Reprod. Biol. 13, 239–311.
| 1:STN:280:DyaK3szgvFyqsw%3D%3D&md5=c1beae5efb065f18cc2a90916ca71d88CAS | 1845336PubMed |
Ishikawa, T., Fujioka, H., Ishimura, T., Takenaka, A., and Fujisawa, M. (2007). Expression of leptin and leptin receptor in the testis of fertile and infertile patients. Andrologia 39, 22–27.
| Expression of leptin and leptin receptor in the testis of fertile and infertile patients.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXisVKhtr8%3D&md5=ecffbf7d40af2b4c946e1b26742dac4aCAS | 17212806PubMed |
Isidori, A. M., Caprio, M., Strollo, F., Moretti, C., Frajese, G., Isidori, A., and Fabbri, A. (1999). Leptin and androgens in male obesity: evidence for leptin contribution to reduced androgen levels. J. Clin. Endocrinol. Metab. 84, 3673–3680.
| 1:CAS:528:DyaK1MXms1Ohtbg%3D&md5=4a1c247a09f100ef07eb554677d0f9bcCAS | 10523013PubMed |
Jean-Faucher, C., Berger, M., deTurckheim, M., Vevssiere, G., and Jean, C. (1982). The effect of preweaning undernutrition upon the sexual development of male mice. Biol. Neonate 41, 45–51.
| The effect of preweaning undernutrition upon the sexual development of male mice.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL387mtFWgtg%3D%3D&md5=1dcd789b9eb407e8f8801577cb8192cfCAS | 7066438PubMed |
Jensen, T. K., Andersson, A. M., Jørgensen, N., Andersen, A. G., Carlsen, E., Petersen, J. H., and Skakkebæk, N. E. (2004). Body mass index in relation to semen quality and reproductive hormones among 1,558 Danish men. Fertil. Steril. 82, 863–870.
| Body mass index in relation to semen quality and reproductive hormones among 1,558 Danish men.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhvFOjtrg%3D&md5=b049fbb65b616b358f193b78ce244bd7CAS | 15482761PubMed |
Kasturi, S. S., Tannir, J., and Brannigan, R. E. (2008). The metabolic syndrome and male infertility. J. Androl. 29, 251–259.
| The metabolic syndrome and male infertility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXms1WnsrY%3D&md5=a44868938babe96e1ab4fd6abd23dd1bCAS | 18222914PubMed |
Korenbrot, C. C., Huhtaniemi, I. T., and Weiner, R. I. (1977). Preptial separation as an external sign of pubertal development in the male rats. Biol. Reprod. 17, 298–303.
| Preptial separation as an external sign of pubertal development in the male rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2sXlsV2gtbY%3D&md5=3cca111148710ccca0bc4e5f66dcea15CAS | 889997PubMed |
Kort, H. I., Massey, J. B., Elsner, C. W., Mitchell-Leef, D., Shapiro, D. B., Witt, M. A., and Roudebush, W. E. (2006). Impact of body mass index values on sperm quantity and quality. J. Androl. 27, 450–452.
| Impact of body mass index values on sperm quantity and quality.Crossref | GoogleScholarGoogle Scholar | 16339454PubMed |
Malkov, M., Fisher, Y., and Don, J. (1998). Developmental schedule of the postnatal rat testis determined by flow cytometry. Biol. Reprod. 59, 84–92.
| Developmental schedule of the postnatal rat testis determined by flow cytometry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXktFaksbo%3D&md5=5003f93443aa18869264cab7406d4c27CAS | 9674997PubMed |
Marathe, C. K., Shetty, J., and Dighe, R. R. (1995). Selective immunoneutralisation of luteinising hormone results in the apoptotic cell death of pachytene spermatocytes and spermatids in the rat testis. Endocrine 3, 705–709.
| 1:CAS:528:DyaK2MXptFyrsbg%3D&md5=c51916f419e56331ab16ce469b4d3056CAS | 21153158PubMed |
Margetic, S., Gazzola, C., Pegg, G. G., and Hill, R. A. (2002). Leptin: a review of its peripheral actions and interactions. Int. J. Obes. Relat. Metab. Disord. 26, 1407–1433.
| Leptin: a review of its peripheral actions and interactions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XoslGlsbc%3D&md5=1d1ea02e462ad7f012298ac5be5dba2dCAS | 12439643PubMed |
Narayana, K., D’Souza, U. J. A., and Rao, K. P. S. (2002). Ribavirin-induced sperm shape abnormalities in Wistar rat. Mut. Res. 513, 193–196.
| Ribavirin-induced sperm shape abnormalities in Wistar rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXosFOjur4%3D&md5=71248f7414bc81df3beb1f6f0591f633CAS |
Novelli, E. L. B., Diniz, Y. S., Galhardi, C. M., Ebaid, G. M. X., Rodrigues, H. G., Mani, F., Fernandes, A. A. H., Cicogna, A. C., and Filho, J. L. V. B. N. (2007). Anthropometrical parameters and markers of obesity in rats. Lab. Anim. 41, 111–119.
| Anthropometrical parameters and markers of obesity in rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsFGlsbk%3D&md5=d15fd9149f606d75687be21ca8891d06CAS |
O’Donnell, L., McLachlan, R. I., Wreford, N. G., de Kretser, D. M., and Robertson, D. M. (1996). Testosterone withdrawal promotes stage-specific detachment of round spermatids from the rat seminiferous epithelium. Biol. Reprod. 55, 895–901.
| Testosterone withdrawal promotes stage-specific detachment of round spermatids from the rat seminiferous epithelium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xls1Gku7s%3D&md5=5e40adf7fbad3e843593bd8a89097da3CAS | 8879506PubMed |
O’Donnell, L., Meachem, S. J., Stanton, P. G., and McLachlan, R. I. (2006). Endocrine regulation of spermatogenesis. In ‘Physiology of Reproduction’. (Eds E. Knobil and J. D. Neil.) pp. 1017–1069. (Elsevier: St Louis, MO.)
Ojeda, S. R., and Skinner, M. K. (2006). Puberty in rat. In ‘Physiology of Reproduction’. (Eds E. Knobil and J. D. Neil.) pp. 2061–2103. (Elsevier: St Louis, MO.)
Omura, M., Hirata, M., Zhao, M., Tanaka, A., and Inoue, N. (1995). Pesticide causes testicle damage reduces sperm counts. Bull. Environ. Contam. Toxicol. 55, 1–7.
| Pesticide causes testicle damage reduces sperm counts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXlsl2lurk%3D&md5=56cbc138465bd4151087057ba7f5a906CAS | 7663078PubMed |
Palmer, N. O., Fullston, T., Mitchell, M., Setchell, B. P., and Lane, M. (2011). SIRT6 in mouse spermatogenesis is modulated by diet-induced obesity. Reprod. Fertil. Dev. 23, 929–939.
| SIRT6 in mouse spermatogenesis is modulated by diet-induced obesity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVOrtb7J&md5=18bed075a1e82e9326cf3b3ac5151d8fCAS | 21871212PubMed |
Palmer, N. O., Bakos, H. W., Owens, J. A., Setchell, B. P., and Lane, M. (2012). Diet and exercise in an obese mouse fed a high fat diet improve metabolic health and reverse perturbed sperm function. Am. J. Physiol. Endocrinol. Metab. 302, E768–E780.
| Diet and exercise in an obese mouse fed a high fat diet improve metabolic health and reverse perturbed sperm function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xmsl2gtrg%3D&md5=6e1fdad4ccab8fe1fab43eb87547bbcdCAS | 22252945PubMed |
Pentikäinen, V., Erkkilä, K., and Dunkel, L. (1999). Fas regulates germ cell apoptosis in the human testis in vitro. Am. J. Physiol. 276, E310–E316.
| 9950791PubMed |
Ramlau-Hansen, C. H., Nohr, E. A., Thulstrup, A. M., Bonde, J. P., Storgaard, L., and Olsen, J. (2007). Is maternal obesity related to semen quality in the male offspring? A pilot study. Hum. Reprod. 22, 2758–2762.
| Is maternal obesity related to semen quality in the male offspring? A pilot study.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2srlsFChtA%3D%3D&md5=35cbcf8c42ea6659ef9938d8e1e59cd1CAS | 17704100PubMed |
Sallmén, M., Sandler, D. P., Hoppin, J. A., Blair, A., and Baird, D. D. (2006). Reduced fertility among overweight and obese men. Epidemiology 17, 520–523.
| Reduced fertility among overweight and obese men.Crossref | GoogleScholarGoogle Scholar | 16837825PubMed |
Sanaa, R. G., Walaa, G. H., Kamal, A. A., and Shimaa, M. R. (2014). Effects of Orlistat and herbal mixture extract on brain, testes functions oxidative stress biomarkers in a rat model of high fat diet. Beni Suef Uni. J. Appl. Sci. 3, 93–105.
| Effects of Orlistat and herbal mixture extract on brain, testes functions oxidative stress biomarkers in a rat model of high fat diet.Crossref | GoogleScholarGoogle Scholar |
Sanchez-Garrido, M. A., Castellano, J. M., Ruiz-Pino, F., Garcia-Galiano, D., Manfredi-Lozano, M., Leon, S., Romero-Ruiz, A., Dieguez, C., Pinilla, L., and Tena-Sempare, M. (2013). Metabolic programming of puberty: sexually dimorphic responses to early nutritional challenges. Endocrinology 154, 3387–3400.
| Metabolic programming of puberty: sexually dimorphic responses to early nutritional challenges.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsVegsLrJ&md5=8ee2e14f6aca09f2acd41fbdeb1a6728CAS | 23751873PubMed |
Shafik, A., and Olfat, S. (1981). Lipectomy in the treatment of scrotal lipometosis. Br. J. Urol. 53, 55–61.
| Lipectomy in the treatment of scrotal lipometosis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3M7jsVygsg%3D%3D&md5=9bf3b049141c94c5991ba4dddefc30aaCAS | 7470804PubMed |
Sharpe, R. M. (2010). Environmental/lifestyle effects on spermatogenesis. Philos. Trans. R. Soc. Lond. B Biol. Sci. 365, 1697–1712.
| Environmental/lifestyle effects on spermatogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVaisrrE&md5=72196236abff36cf00cdbb74871bb132CAS | 20403879PubMed |
Smith, J. T., and Spencer, S. J. (2012). Pre-weaning over and under feeding alters onset of puberty in rat without affecting kisspeptin. Biol. Reprod. 86, 145.
| Pre-weaning over and under feeding alters onset of puberty in rat without affecting kisspeptin.Crossref | GoogleScholarGoogle Scholar | 22378761PubMed |
Soltani, Y., Aklil, B., Mokrani, Z., Hamouli, Z., and Hadj Bekkouche, F. (2013). Effects of diet induced obesity on the gonadal axis in the male rabbit: impact of leptin. In ‘USTHB-FBS-4th International Congress of the Populations & Animal Communities “Dynamics & Biodiversity of the terrestrial & aquatic Ecosystems” “CIPCA4” TAGHIT (Bechar), Algeria, 19–21 November 2013’. pp. 478–487.
Stewart, T. M., Lui, D. Y., Garrett, C., Jorgensen, N., Brown, E. H., and Baker, H. W. G. (2009). Associations between andrological measures, hormones and semen quality in fertile Australian men: inverse relationship between obesity and sperm output. Hum. Reprod. 24, 1561–1568.
| 1:CAS:528:DC%2BD1MXnslGrsr4%3D&md5=de22dadcc6a41334f12f0dc77d8b16f8CAS | 19351657PubMed |
Tapanainen, J. S., Tilly, J. L., Vihko, K. K., and Hsueh, A. J. (1993). Hormonal control of apoptotic cell death in the testis: gonadotrophins and androgens as testicular cell survival factors. Mol. Endocrinol. 7, 643–650.
| 1:CAS:528:DyaK3sXksVWgtrs%3D&md5=402ce7c7df92fc62f0fc78a4c03dbd57CAS | 8316250PubMed |
Tena-Sempere, M., Pinilla, L., Gonzalez, L. C., Dieguez, C., Casanueva, F. F., and Aguilar, E. (1999). Leptin inhibits testosterone secretion from adult rat testis in vitro. J. Endocrinol. 161, 211–218.
| Leptin inhibits testosterone secretion from adult rat testis in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjs12kt7g%3D&md5=93d2f96da7f832a16c8c85f048ee0901CAS | 10320818PubMed |
Tenscher, A., and Richterich, P. (1971). Enzymatic calorimetric end point method with GOD-POD (GOD: Glucose oxidase, POD: Peroxidase). Schweiz. Med. Wochenschr. 101, 345–352.
Tesarik, J., Guido, M., Mendoza, C., and Greco, E. (1998). Human spermatogenesis in vitro: respective effects of follicle-stimulating hormone and testosterone on meiosis, spermiogenesis, and Sertoli cell apoptosis. J. Clin. Endocrinol. Metab. 83, 4467–4473.
| Human spermatogenesis in vitro: respective effects of follicle-stimulating hormone and testosterone on meiosis, spermiogenesis, and Sertoli cell apoptosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXnvFOrurk%3D&md5=4eadbaf8e0e8f27caeebf2ba05b963beCAS | 9851795PubMed |
Tesarik, J., Martinez, F., Rienzi, L., Iacobelli, M., Ubaldi, F., Mendoza, C., and Greco, E. (2002). In-vitro effects of FSH and testosterone withdrawal on caspase activation and DNA fragmentation in different cell types of human seminiferous epithelium. Hum. Reprod. 17, 1811–1819.
| In-vitro effects of FSH and testosterone withdrawal on caspase activation and DNA fragmentation in different cell types of human seminiferous epithelium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xmt1Glsbs%3D&md5=bafd347a05a6228dc317fd60cf948698CAS | 12093844PubMed |
Vendramini, V., Cedenho, A. P., Miraglia, S. M., and Spaine, D. M. (2014). Reproductive function of the male obese zucker rats: alteration in sperm production and sperm DNA damage. Reprod. Sci. 21, 221–229.
| 1:CAS:528:DC%2BC2cXhslWgurnK&md5=9c0d17e2d958ea81bead319dd2abe876CAS | 23800399PubMed |
Vera, Y., Erkkila, K., Wang, C., Nunez, C., Kyttanen, S., Lue, Y., Dunkel, L., Swerdloff, R. S., and Hikim, A. P. S. (2006). Involvement of p38 mitogen-activated protein kinase and inducible nitric oxide synthase in apoptotic signalling of murine and human male germ cells after hormone deprivation. Mol. Endocrinol. 20, 1597–1609.
| Involvement of p38 mitogen-activated protein kinase and inducible nitric oxide synthase in apoptotic signalling of murine and human male germ cells after hormone deprivation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xms1Gjsb0%3D&md5=7c5c2214214394dcb7223be77b6635f3CAS | 16469770PubMed |
Vigueras-Villaseñor, R. M., Rojas-Castañeda, J. C., Chávez-Saldaña, M., Gutiérrez-Pérez, O., García-Cruz, M. E., Cuevas-Alpuche, O., Reyes-Romero, M. M., and Zambrano, E. (2011). Alterations in the spermatic function generated by obesity in rats. Acta Histochem. 113, 214–220.
| Alterations in the spermatic function generated by obesity in rats.Crossref | GoogleScholarGoogle Scholar | 20149418PubMed |
Vijayalaxmi, K. K., and D’Souza, M. P. (2004). Studies on the genotoxic effects of anticancer drug carboplatin in in vivo mouse. Int. J. Hum. Genet. 4, 249–255.
| 1:CAS:528:DC%2BD2MXjt1Wlur0%3D&md5=f7140de5f96b61e47d78057a5b479f56CAS |
Wang, Y., Liu, X. P., Qin, D. N., Chen, S., and Li, Y. S. (2007). Diet induced obesity affects testis development in pubertal rats. Zhonghua Nan Ke Xue 13, 514–519.
| 1:CAS:528:DC%2BD1cXnsFSmurw%3D&md5=f2bcfaf817e8793c9aab4b39ab58162dCAS | 17615975PubMed |
Whitaker, R. C., Wright, J. A., Pepe, M. S., Seidel, K. D., and Dietz, W. H. (1997). Predicting obesity in young adulthood from childhood and parental obesity. N. Engl. J. Med. 337, 869–873.
| Predicting obesity in young adulthood from childhood and parental obesity.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2svjtlSjtg%3D%3D&md5=5daf3d9ba3cca4f4744eeea0433ef8e0CAS | 9302300PubMed |
Wong, C. H., Xia, W., Lee, N. P., Mruk, D. D., Lee, W. M., and Cheng, C. Y. (2005). Regulation of ectoplasmic specialization dynamics in the seminiferous epithelium by focal adhesion-associated proteins in testosterone-suppressed rat testes. Endocrinology 146, 1192–1204.
| Regulation of ectoplasmic specialization dynamics in the seminiferous epithelium by focal adhesion-associated proteins in testosterone-suppressed rat testes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXitlehtr8%3D&md5=d3c2b525b0952d8e37961bed90a7d8f9CAS | 15591141PubMed |
Yuan, M., Huang, G., Li, J., Zhang, J., Li, F., Li, K., Gao, B., Zeng, L., Shan, W., Lin, P., and Huang, L. (2014). Hyperleptinemia directly affects testicular maturation at different sexual stages in mice, and suppressor of cytokine signaling 3 is involved in this process. Reprod. Biol. Endocrinol. 12, 15.
| Hyperleptinemia directly affects testicular maturation at different sexual stages in mice, and suppressor of cytokine signaling 3 is involved in this process.Crossref | GoogleScholarGoogle Scholar | 24502529PubMed |
Zhao, J., Zhai, L., Liu, Z., Wu, S., and Xu, L. (2014). Leptin level and oxidative stress contribute to obesity induced low testosterone in murine testicular tissue. Oxid. Med. Cell. Longev. 2014, 190945.
| Leptin level and oxidative stress contribute to obesity induced low testosterone in murine testicular tissue.Crossref | GoogleScholarGoogle Scholar | 24829619PubMed |
