Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-22T06:02:03.878Z Has data issue: false hasContentIssue false
  • English
  • Français

A paternal hypercaloric diet affects the metabolism and fertility of F1 and F2 Wistar rat generations

Published online by Cambridge University Press:  15 January 2020

Leonardo Toshio Oshio Open the ORCID record for Leonardo Toshio Oshio [Opens in a new window] ,
Ana Eliza Andreazzi ,
Jéssica Ferraz Lopes Open the ORCID record for Jéssica Ferraz Lopes [Opens in a new window] ,
Jackson Pereira de Sá ,
Mariana Bolotari ,
Vinícius Moreira Gonçalves Costa Open the ORCID record for Vinícius Moreira Gonçalves Costa [Opens in a new window] ,
Martha de Oliveira Guerra  and
Vera Maria Peters
Leonardo Toshio Oshio*
Affiliation:
Centro de Biologia da Reprodução, Universidade Federal de Juiz de Fora, Juiz de Fora, Brazil
Ana Eliza Andreazzi
Affiliation:
Departamento de Fisiologia, Instituto de Ciências Biológicas, Universidade Federal de Juiz de Fora, Juiz de Fora, Brazil
Jéssica Ferraz Lopes
Affiliation:
Centro de Biologia da Reprodução, Universidade Federal de Juiz de Fora, Juiz de Fora, Brazil
Jackson Pereira de Sá
Affiliation:
Centro de Biologia da Reprodução, Universidade Federal de Juiz de Fora, Juiz de Fora, Brazil
Mariana Bolotari
Affiliation:
Centro de Biologia da Reprodução, Universidade Federal de Juiz de Fora, Juiz de Fora, Brazil
Vinícius Moreira Gonçalves Costa
Affiliation:
Centro de Biologia da Reprodução, Universidade Federal de Juiz de Fora, Juiz de Fora, Brazil
Martha de Oliveira Guerra
Affiliation:
Centro de Biologia da Reprodução, Universidade Federal de Juiz de Fora, Juiz de Fora, Brazil
Vera Maria Peters
Affiliation:
Centro de Biologia da Reprodução, Universidade Federal de Juiz de Fora, Juiz de Fora, Brazil
*
Address for correspondence: Leonardo Oshio, Centro de Biologia da Reprodução, Universidade Federal de Juiz de Fora, Juiz de Fora, Brazil. Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Increased fat and carbohydrate intakes based on the Western diet are important lifestyle modifications that lead to hypercaloric inputs, obesity, and male fertility negative effects. Epigenetic transmission may also predispose descended generations to chronic diseases, such as obesity, type 2 diabetes, behavioral, and reproductive disorders. The present study sought to evaluate the influence of a high-fat-high-sugar (HFHS) diet supplied to Wistar rats from 25 to 90 days of life on reproductive and metabolic parameters in male generations F0, F1, and F2. The standard group received the normocaloric – Nuvilab Quimtia® –3.86 kcal/kg. The hypercaloric diet (HD) group received the HFHS diet – PragSoluções® –4.77 kcal/kg. Body weight, adiposity, F1 and F2 prepubertal age evaluations, oral glucose tolerance test, insulin tolerance test, organ weights, sperm count and morphology assessments, and histometric testicular analyses were performed. The HFHS diet promoted dyslipidemia, higher adiposity, lower relative organ weights, and higher mean kidney weight, decreased mean testicle and parenchyma weights and lower height of seminiferous epithelium (HE) for the F0 generation. F1 and F2 offspring of HD group displayed early preprepubertal development, although did not alter the metabolic parameters. Decreased HE and tubular testicular compartment volumetric density and increased intertubular testicular compartment volumetric density and volume in the F1 generation of HD group were observed. Alterations in histometry of intertubular testicular compartment were also noted. It is concluded that the HFHS experimental model altered only paternal metabolic parameters. However, reproductive parameters of the three generations were affected.

Keywords

Hypercaloric dietmale infertilityratstestesepigenetic
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 11 , Issue 6 , December 2020 , pp. 653 - 663
Check for updates
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Levine, H, Jørgensen, N, Martino-Andrade, A, et al. Temporal trends in sperm count: a systematic review and meta-regression analysis. Hum Reprod Update. 2017; 23, 646–659.CrossRefGoogle ScholarPubMed
Danielewicz, A, Przybyłowicz, KE, Przybyłowicz, M. Dietary patterns and poor semen quality risk in men: a cross-sectional study. Nutrients 2018; 10, 1–13.CrossRefGoogle ScholarPubMed
Jensen, TK, Andersson, AM, Jørgensen, N, et al. Body mass index in relation to semen quality and reproductive hormones among 1558 Danish men. Fertil Steril. 2004; 82, 863–870.CrossRefGoogle ScholarPubMed
Kort, HI, Massey, JB, Elsner, CW, et al. Impact of body mass index values on sperm quantity and quality. J Androl. 2006; 27, 450–452.CrossRefGoogle ScholarPubMed
Martini, AC, Tissera, A, Estofán, D, et al. Overweight and seminal quality: a study of 794 patients. Fertil Steril. 2010; 94, 1739–1743.CrossRefGoogle ScholarPubMed
Shayeb, AG, Harrild, K, Mathers, E, Bhattacharya, S. An exploration of the association between male body mass index and semen quality. Reprod Biomed Online. 2011; 23, 717–723.CrossRefGoogle ScholarPubMed
Wei, Y, Schatten, H, Sun, QY. Environmental epigenetic inheritance through gametes and implications for human reproduction. Hum Reprod Update. 2015; 21, 194–208.CrossRefGoogle ScholarPubMed
Guerrero-Bosagna, C, Skinner, MK. Environmentally induced epigenetic transgenerational inheritance of male infertility. Curr Opin Genet Dev. 2014; 26, 79–88.CrossRefGoogle ScholarPubMed
Soubry, A, Hoyo, C, Jirtle, RL, Murphy, SK. A paternal environmental legacy: evidence for epigenetic inheritance through the male germ line. BioEssays. 2014; 36, 359–371.CrossRefGoogle ScholarPubMed
Gaskins, AJ, Colaci, DS, Mendiola, J, Swan, SH, Chavarro, JE. Dietary patterns and semen quality in young men. Hum Reprod. 2012; 27, 2899–2907.CrossRefGoogle ScholarPubMed
Fullston, T, Teague, EMCO, Palmer, NO, et al. Paternal obesity initiates metabolic disturbances in two generations of mice with incomplete penetrance to the F2 generation and alters the transcriptional profile of testis and sperm microRNA content. FASEB J. 2013; 27, 4226–4243.CrossRefGoogle ScholarPubMed
Soubry, A. POHaD: why we should study future fathers. Environ Epigenet. 2018; 4, 1–7.CrossRefGoogle ScholarPubMed
Park, S, Harrold, JA, Widdowson, PS, Williams, G. Increased binding at 5-HT(1A), 5-HT(1B), and 5-HT(2A) receptors and 5-HT transporters in diet-induced obese rats. Brain Res. 1999; 847, 90–97.CrossRefGoogle ScholarPubMed
Nery, CS, Pinheiro, IL, Muniz, GS, Vasconcelos, DAA, França, SP, Nascimento, E. Murinometric evaluations and feed efficiency in rats from reduced litter during lactation and submitted or not to swimming exercise. Rev Bras Med Esporte. 2011; 17, 49–55.CrossRefGoogle Scholar
Yamasaki, K, Sawaki, M, Noda, S, Muroi, T, Takatsuki, M. Preputial separation and glans penis changes in normal growing Crj: CD (SD) IGS rats. Reprod Toxicol. 2001; 15, 533–536.CrossRefGoogle ScholarPubMed
Silva, A, Santos, M, Franca, S, et al. Acute and subchronic antihyperglycemic activities of bowdichia virgilioides roots in non diabetic and diabetic rats. J Intercult Ethnopharmacol. 2015; 4, 57.CrossRefGoogle ScholarPubMed
Hirata, AE, Alvarez-Rojas, F, Campello Carvalheira, JB, De Oliveira Carvalho, CR, Dolnikoff, MS, Abdalla Saad, MJ. Modulation of IR/PTP1B interaction and downstream signaling in insulin sensitive tissues of MSG-rats. Life Sci. 2003; 73, 1369–1381.CrossRefGoogle ScholarPubMed
Seed, J, Chapin, RE, Clegg, ED, et al. Methods for assessing sperm motility, morphology, and counts in the rat, rabbit, and dog: a consensus report. Reprod Toxicol. 1996; 10, 237–244.CrossRefGoogle ScholarPubMed
WHO. WHO Laboratory Manual for the Examination and Processing of Human Semen , 2010. Fifth ed. WHO Press, Geneva, Switzerland.Google Scholar
França, LR, Godinho, CL. Testis morphometry, seminiferous epithelium cycle length, and daily sperm production in domestic cats (Felis catus). Biol Reprod. 2003; 68, 1554–1561.CrossRefGoogle Scholar
Oshio, LT, Ribeiro, CCT, Marques, RM, et al. Effect of Ginkgo biloba extract on sperm quality, serum testosterone concentration and histometric analysis of testes from adult Wistar rats. J Med Plants Res. 2015; 9, 122–231.Google Scholar
Johnson, L, Petty, CS, Neaves, WB. A new approach to quantification of spermatogenesis and its application to germinal cell attrition during human spermiogenesis. Biol Reprod. 1981; 25, 217–226.CrossRefGoogle ScholarPubMed
Attal, J, Courot, M. Développement Testiculaire Et Établissement De La Spermatogenèse Chez Le Taureau. Ann Biol Anim Biochim Biophys. 1963; 3, 219–241.CrossRefGoogle Scholar
Fullston, T, Palmer, NO, Owens, JA, Mitchell, M, Bakos, HW, Lane, M. Diet-induced paternal obesity in the absence of diabetes diminishes the reproductive health of two subsequent generations of mice. Hum Reprod. 2012; 27, 1391–1400.CrossRefGoogle ScholarPubMed
Chambers, TJG, Morgan, MD, Heger, AH, et al. High-fat diet disrupts metabolism in two generations of rats in a parent-of-origin specific manner. Sci Rep. 2016; 6, 31857.CrossRefGoogle Scholar
King, V, Dakin, RS, Liu, L, et al. Maternal obesity has little effect on the immediate offspring but impacts on the next generation. Endocrinology 2013; 154, 2514–2524.CrossRefGoogle ScholarPubMed
Dunn, GA, Bale, TL. Maternal high-fat diet effects on third-generation female body size via the paternal lineage. Endocrinology 2011; 152, 2228–2236.CrossRefGoogle ScholarPubMed
Sellers, RS, Morton, D, Michael, B, et al. Society of Toxicologic Pathology position paper: organ weight recommendations for toxicology studies. Toxicol Pathol. 2007; 35, 751–755.CrossRefGoogle ScholarPubMed
Sanchez-Garrido, MA, Ruiz-Pino, F, Velasco, I, et al. Intergenerational Influence of paternal obesity on metabolic and reproductive health parameters of the offspring: male-preferential impact and involvement of kiss1-mediated pathways. Endocrinology 2018; 159, 1005–1018.CrossRefGoogle ScholarPubMed
Esmaili-Nejad, MR, Babaei, H, Kheirandish, R. The effects of long-term leptin administration on morphometrical changes of mice testicular tissue. Iran J Basic Med Sci. 2015; 18, 1176–1182.Google ScholarPubMed
Haron, MN, D’Souza, UJA, Jaafar, H, Zakaria, R, Singh, HJ. Exogenous leptin administration decreases sperm count and increases the fraction of abnormal sperm in adult rats. Fertil Steril. 2010; 93, 322–324.CrossRefGoogle ScholarPubMed
Zhao, J, Zhai, L, Liu, Z, Wu, S, Xu, L. Leptin level and oxidative stress contribute to obesity-induced low testosterone in murine testicular tissue. Oxid Med Cell Longev. 2014; 2014, 190945.CrossRefGoogle ScholarPubMed
Chavarro, JE, Mínguez-Alarcón, L, Mendiola, J, Cutillas-Tolín, A, López-Espín, JJ, Torres-Cantero, AM. Trans fatty acid intake is inversely related to total sperm count in young healthy men. Hum Reprod. 2014; 29, 429–440.CrossRefGoogle ScholarPubMed
Rato, L, Alves, MG, Dias, TR, et al. High-energy diets may induce a pre-diabetic state altering testicular glycolytic metabolic profile and male reproductive parameters. Andrology 2013; 1, 495–504.CrossRefGoogle ScholarPubMed
Ibáñez, CA, Erthal, RP, Ogo, FM, et al. A high fat diet during adolescence in male rats negatively programs reproductive and metabolic function which is partially ameliorated by exercise. Front Physiol. 2017; 8, 1–12.CrossRefGoogle ScholarPubMed
Jia, YF, Feng, Q, Ge, ZY, et al. Obesity impairs male fertility through long-term effects on spermatogenesis. BMC Urol. 2018; 18, 1–8.CrossRefGoogle ScholarPubMed
Revenig, L, Leung, A, Hsiao, W. Ejaculatory physiology and pathophysiology: assessment and treatment in male infertility. Transl Androl Urol. 2014; 3, 41–49.Google ScholarPubMed
Léonhardt, M, Lesage, J, Croix, D, Dutriez-Casteloot, I, Beauvillain, JC, Dupouy, JP. 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. 2004; 68, 390–400.CrossRefGoogle Scholar
Ewing, LL, Zirkin, BR, Cochran, RC, Kromann, N, Peters, C, Ruiz-Bravo, N. Testosterone secretion by rat, rabbit, guinea pig, dog, and hamster testes perfused in vitro: correlation with Leydig cell mass. Endocrinology 1979; 105, 1135–1142.CrossRefGoogle ScholarPubMed
Zirkin, BR, Ewing, LL, Kromann, N, Cochran, RC. Testosterone secretion by rat, rabbit, guinea pig, dog, and hamster testes perfused in vitro: correlation with Leydig cell ultrastructure. Endocrinology 1980; 107, 1867–1874.CrossRefGoogle ScholarPubMed
Mendis-Handagama, SMLC, Zirkin, BR, Ewing, LL. Comparison of components of the testis interstitium with testosterone secretion in hamster, rat, and guinea pig testes perfused in vitro. Am J Anat. 1988; 181, 12–22.CrossRefGoogle ScholarPubMed
Navya, H, Yajurvedi, HN. Obesity causes weight increases in prepubertal and pubertal male offspring and is related to changes in spermatogenesis and sperm production in rats. Reprod Fertil Dev. 2017; 29, 815–823.CrossRefGoogle ScholarPubMed