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Consumption of low-protein or high-fat diets during peripubertal age alter spermatozoa, testis and epididymis of pubertal rats

Published online by Cambridge University Press:  17 March 2025

Letícia Pazin Bomfim ,
Maria Stacy dos Santos Silva ,
Ivana Regina da Costa ,
Karen Gomes Luiz ,
Débora Hipólito Quadreli ,
Mariana Beirigo Bispo ,
Paulo Cezar de Freitas Mathias Open the ORCID record for Paulo Cezar de Freitas Mathias [Opens in a new window]  and
Glaura Scantamburlo Alves Fernandes Open the ORCID record for Glaura Scantamburlo Alves Fernandes [Opens in a new window]
Letícia Pazin Bomfim
Affiliation:
Department of General Biology, State University of Londrina, Londrina, Paraná, Brazil
Maria Stacy dos Santos Silva
Affiliation:
Department of General Biology, State University of Londrina, Londrina, Paraná, Brazil
Ivana Regina da Costa
Affiliation:
Department of Immunology, Parasitology and General Pathology, State University of Londrina, Londrina, Paraná, Brazil
Karen Gomes Luiz
Affiliation:
Department of General Biology, State University of Londrina, Londrina, Paraná, Brazil
Débora Hipólito Quadreli
Affiliation:
Department of Immunology, Parasitology and General Pathology, State University of Londrina, Londrina, Paraná, Brazil
Mariana Beirigo Bispo
Affiliation:
Department of Genetics and Molecular Biology, State University of Londrina, Londrina, Paraná, Brazil
Paulo Cezar de Freitas Mathias
Affiliation:
Laboratory of Secretion Cell Biology, Department of Cell Biology and Genetics, Center of Biological Sciences, State University of Maringá, Maringá, Paraná, Brazil
Glaura Scantamburlo Alves Fernandes*
Affiliation:
Department of General Biology, State University of Londrina, Londrina, Paraná, Brazil
*
Corresponding author: Glaura Scantamburlo Alves Fernandes; Email: [email protected]
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Abstract

Since the 1980s, research has linked environmental factors to adult-onset diseases. The DOHaD theory suggests that exposures during development can permanently affect organ function, predisposing individuals to adult diseases. Studies indicate that protein restriction or a high-fat diet (HFD) during this phase impacts adult metabolism since programmed dysfunctions may depend on changes established during puberty, such as the reproductive system. However, there are no studies on the impact of low-protein (LP) or HFD on male testicles during this phase. For this, Male Wistar rats were categorized into three dietary groups: LP (isocaloric low-protein pelletized); HFD; and Control (balanced commercial) until PND 60. This study was approved by the CEUA-UEM. On postnatal day 61, the animals were euthanized for histopathological, sperm count, and oxidative stress assessments in the testis and epididymis. Statistical analyses were conducted following established ethical principles in animal research. The research revealed significant alterations in daily sperm production and transit through the epididymis. Sperm morphology was affected in the experimental groups. Mitochondrial activity increased in the HFD group. Testicular and epididymal histopathology, seminiferous tubule diameter, and germinal epithelium height, as well as the number of Sertoli and Leydig cells, remained unchanged. Stereological analysis revealed tissue remodeling in the epididymis, particularly in the LP group. LP group showed an increase in lipid peroxidation in the oxidative damage test. In conclusion, low-protein and HFD during peripubertal age did not affect postnatal testicular development in rats. However, they impacted sperm quality, potentially affecting fertility and male reproductive system development.

Topics structure

Topic(s)

Research Variable

Subtopic(s)

Nutrition/Diet

Keywords

Reproductionnutritionunbalancedevelopmentpuberty
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 16 , 2025 , e15
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Copyright
© The Author(s), 2025. Published by Cambridge University Press in association with The International Society for Developmental Origins of Health and Disease (DOHaD)

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References

Silveira, PP, Portella, AK, Goldani, MZ, Barbieri, MA. Developmental origins of health and disease (DOHaD). J Pediat. 2007; 83(6), 494–504.CrossRefGoogle ScholarPubMed
Khazipov, R, Luhmann, HJ. Early patterns of electrical activity in the developing cerebral cortex of humans and rodents. Trends Neurosci. 2006; 29(7), 414–418.CrossRefGoogle ScholarPubMed
Barker, D. The developmental origins of chronic adult disease. Acta Paediatr. 2004; 93(s446), 26–33.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, 807.CrossRefGoogle ScholarPubMed
Barker, D, Eriksson, J, Forsén, T, Osmond, C. Fetal origins of adult disease: strength of effects and biological basis. Int J Epidemiol. 2002; 31(6), 1235–1239.CrossRefGoogle ScholarPubMed
De Oliveira, JC, Lisboa, PC, De Moura, EG, et al. Poor pubertal protein nutrition disturbs glucose-induced insulin secretion process in pancreatic islets and programs rats in adulthood to increase fat accumulation. J Endocrinol. 2013; 216(2), 195–206.CrossRefGoogle ScholarPubMed
De Oliveira, JC, De Moura, EG, Miranda, RA, et al. Low-protein diet in puberty impairs testosterone output and energy metabolism in male rats. J Endocrinol. 2018; 237(3), 243–254.CrossRefGoogle ScholarPubMed
Salam, RA, Bhutta, ZA, Koletzko, B, et al. 2.7 Adolescent Nutrition. In Koletzko, B, Bhatia, J, Bhutta, ZA, Cooper, P, Makrides, M, Uauy, R, Wang, W. eds. World Review of Nutrition and Dietetics. S. Karger AG, 2015; 122–126.Google Scholar
Beeram, E, Suman, B, Divya, B. Proteins as the molecular markers of male fertility. J Hum Reprod Sci. 2019; 12(1), 19.CrossRefGoogle Scholar
Ajuogu, PK, Al-Aqbi, MA, Hart, RA, Wolden, M, et al. The effect of dietary protein intake on factors associated with male infertility: a systematic literature review and meta-analysis of animal clinical trials in rats. Nutr Health. 2020; 26(1), 53–64.CrossRefGoogle ScholarPubMed
Crean, AJ, Senior, AM. High-fat diets reduce male reproductive success in animal models: a systematic review and meta-analysis. Obes Rev. 2019; 20(6), 921–933.CrossRefGoogle ScholarPubMed
Associação Brasileira de Enfermagem (ABEn Nacional). (2017). Revista Adolescer - Capítulo 06. Available in https://pt.scribd.com/document/340949457/Revista-Adolescer-ABEn-Nacional Google Scholar
Robb, GW, Amann, RP, Killian, GJ. Daily sperm production and epididymal sperm reserves of pubertal and adult rats. Reproduction. 1978; 54(1), 103–107.CrossRefGoogle ScholarPubMed
Siervo, GEML, Vieira, HR, Ogo, FM, et al. Spermatic and testicular damages in rats exposed to ethanol: influence of lipid peroxidation but not testosterone. Toxicology. 2015; 330, 1–8.CrossRefGoogle Scholar
Fernandes, GSA, Arena, AC, Fernandez, CDB, et al. Reproductive effects in male rats exposed to diuron. Reprod Toxicol. 2007; 23(1), 106–112.CrossRefGoogle ScholarPubMed
Silva, EJR, Vendramini, V, Restelli, A, et al. Impact of adrenalectomy and dexamethasone treatment on testicular morphology and sperm parameters in rats: insights into the adrenal control of male reproduction. Andrology. 2014; 2(6), 835–846.CrossRefGoogle ScholarPubMed
Favareto, APA, De Toledo, FC, Kempinas, WDG. Paternal treatment with cisplatin impairs reproduction of adult male offspring in rats. Reprod Toxicol. 2011; 32(4), 425–433.CrossRefGoogle ScholarPubMed
Nassr, ACC, Arena, AC, Toledo, FC, et al. Effects of Gestational and Lactational Fenvalerate Exposure on Immune and Reproductive Systems of Male Rats. J Toxicol Env Health, Part A. 2010; 73(13-14), 952–964.CrossRefGoogle ScholarPubMed
Guerra, MT, Sanabria, M, Leite, GAA, et al. Maternal exposure to butyl paraben impairs testicular structure and sperm quality on male rats. Environ Toxicol. 2017; 32(4), 1273–1289.CrossRefGoogle ScholarPubMed
Teerds, KJ, Huhtaniemi, IT. Morphological and functional maturation of leydig cells: from rodent models to primates. Hum Reprod Update. 2015; 21(3), 310–328.CrossRefGoogle ScholarPubMed
Bradford, M. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976; 72(1-2), 284–254.CrossRefGoogle Scholar
Erthal, RP, Siervo, GEMDL, Frigoli, GF, et al. Malathion exposure during juvenile and peripubertal periods downregulate androgen receptor and 17-ß-HSD testicular gene expression and compromised sperm quality in rats. J Dev Orig Hlth Dis. 2023; 14(2), 286–293.CrossRefGoogle ScholarPubMed
Aviram, M, Eias, K. Dietary olive oil reduces low-density lipoprotein uptake by macrophages and decreases the susceptibility of the lipoprotein to undergo lipid peroxidation. Ann Nutr Metab. 1993; 37(2), 75–84.CrossRefGoogle ScholarPubMed
Parfitt, VJ, Desomeaux, K, Bolton, CH, Hartog, M. Effects of high monounsaturated and polyunsaturated fat diets on plasma lipoproteins and lipid peroxidation in Type 2 Diabetes mellitus. Diabetic Med. 1994; 11(1), 85–91.CrossRefGoogle ScholarPubMed
Jiang, Z, Woollard, ACS, Wolff, SP. Lipid hydroperoxide measurement by oxidation of fe 2+ in the presence of xylenol orange. Comparison with the TBA assay and an iodometric method. Lipids. 1991; 26(10), 853–856.CrossRefGoogle Scholar
Rahman, I, Kode, A, Biswas, SK. Assay for quantitative determination of glutathione and glutathione disulfide levels using enzymatic recycling method. Nat Protoc. 2006; 1(6), 3159–3165.CrossRefGoogle ScholarPubMed
Martin, LJ. Cell interactions and genetic regulation that contribute to testicular leydig cell development and differentiation. Mol Reprod Dev. 2016; 83(6), 470–487.CrossRefGoogle ScholarPubMed
Griswold, MD. The central role of sertoli cells in spermatogenesis. Semin Cell Dev Biol. 1998; 9(4), 411–416.CrossRefGoogle ScholarPubMed
Sofikitis, N, Giotitsas, N, P. Tsounapi, etal, hormonal regulation of spermatogenesis and spermiogenesis. J Steroid Biochem Mol Biol. 2008; 109(3-5), 323–330.CrossRefGoogle Scholar
Sun, EL, Flickinger, CJ. Development of cell types and of regional differences in the postnatal rat epididymis. Am J Anat. 1979; 154(1), 27–55.CrossRefGoogle ScholarPubMed
Robaire, B, Viger, RS. Regulation of Epididymal Epithelial Cell Functions1. Biol Reprod. 1995; 52(2), 226–236.CrossRefGoogle Scholar
Elfgen, V, Mietens, A, Mewe, M, Hau, T, Middendorff, R. Contractility of the epididymal duct - function, regulation and potential drug effects. Reproduction. 2018; 156(4), R125–R141.Google ScholarPubMed
Cornwall, GA. New insights into epididymal biology and function. Hum Reprod Update. 2008; 15(2), 213–227.CrossRefGoogle Scholar
Dacheux, J-L, Dacheux, F. New insights into epididymal function in relation to sperm maturation. REPRODUCTION. 2014; 147(2), R27–R42.CrossRefGoogle ScholarPubMed
Fernandez, CDB, Porto, EM, Arena, AC, Kempinas, WDG. Effects of altered epididymal sperm transit time on sperm quality. Int J Androl. 2008; 31(4), 427–437.CrossRefGoogle ScholarPubMed
Souza, APBD, Schorr-Lenz, Â.M, Lucca, F, Bustamante, IC. The epididymis and its role on sperm quality and male fertility. Anim Reprod. 2017; 14(Suppl), 1234–1244.CrossRefGoogle Scholar
Devi, A, Kushwaha, B, Maikhuri, JP, Singh, R, Gupta, G. Cell signaling in sperm midpiece ensures quiescence and survival in cauda epididymis. Reproduction. 2021; 162(5), 339–351.CrossRefGoogle ScholarPubMed
Aon, MA, Bhatt, N, Cortassa, SC. Mitochondrial and cellular mechanisms for managing lipid excess. Front Physiol. 2014; 5, 282.CrossRefGoogle ScholarPubMed
Piner, P, Üner, N. Oxidative stress and apoptosis was induced by bio-insecticide spinosad in the liver of oreochromis niloticus. Environ Toxicol Phar. 2013; 36(3), 956–963.CrossRefGoogle ScholarPubMed
Salem, EA, Salem, NA, Maarouf, AM, et al. Selenium and lycopene attenuate cisplatin-induced testicular toxicity associated with oxidative stress in wistar rats. Urology. 2012; 79(5), 1184.e1–1184.e6.CrossRefGoogle ScholarPubMed
O’Flaherty, C, Scarlata, E. OXIDATIVE STRESS AND REPRODUCTIVE FUNCTION: the protection of mammalian spermatozoa against oxidative stress. Reproduction. 2022; 164(6), F67–F78.CrossRefGoogle ScholarPubMed