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The Effect of Different Exercise Modalities on Sertoli-germ Cells Metabolic Interactions in High-fat Diet-induced Obesity Rat Models: Implication on Glucose and Lactate Transport, Igf1, and Igf1R-dependent Pathways

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Abstract

The study aimed to uncover a unique aspect of obesity-related metabolic disorders in the testicles induced by a high-fat diet (HFD) and explored the potential mitigating effects of exercise modalities on male fertility. Thirty mature male Wistar rats were randomly assigned to control, HFD-sole, moderate-intensity exercise with HFD (HFD+MICT), high-intensity continuous exercise with HFD (HFD+HICT), and high-intensity interval exercise with HFD (HFD+HIIT) groups (n=6/group). Intracytoplasmic carbohydrate (ICC) storage, expression levels of GLUT-1, GLUT-3, MCT-4, Igf1, and Igf1R, and testicular lactate and lactate dehydrogenase (LDH) levels were assessed. ICC storage significantly decreased in HFD-sole rats, along with decreased mRNA and protein levels of GLUT-1, GLUT-3, MCT-4, Igf1, and Igf1R. The HFD-sole group exhibited a notable reduction in testicular lactate and LDH levels (p<0.05). Conversely, exercise, particularly HIIT, upregulated ICC storage, expression levels of GLUT-1, GLUT-3, MCT-4, Igf1, and Igf1R, and enhanced testicular lactate and LDH levels. These results confirm that exercise, especially HIIT, has the potential to mitigate the adverse effects of HFD-induced obesity on testicular metabolism and male fertility. The upregulation of metabolite transporters, LDH, lactate levels, Igf1, and Igf1R expression may contribute to maintaining metabolic interactions and improving the glucose/lactate conversion process. These findings underscore the potential benefits of exercise in preventing and managing obesity-related male fertility issues.

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References

  1. World Health Organization. WHO fact sheet No 311. In: Obesity and overweight. 2021. Available from: https://www.who.int/news-room/fact-sheets/detail/obesity-and-overweight

  2. Elagizi A, Kachur S, Carbone S, Lavie CJ, Blair SN. A Review of Obesity, Physical Activity, and Cardiovascular Disease. Curr Obes Rep. 2020;9(4):571–81.

    Article  PubMed  Google Scholar 

  3. Benjamin EJ, Virani SS, Callaway CW, Chamberlain AM, Chang AR, Cheng S, et al. Heart Disease and Stroke Statistics-2018 Update: A Report From the American Heart Association. Circulation. 2018;137(12):e67–e492.

    Article  PubMed  Google Scholar 

  4. Penzias A, Azziz R, Bendikson K, Falcone T, Hansen K, Hill M, et al. Obesity and reproduction: a committee opinion. Fertil Steril. 2021;116(5):1266–85.

    Article  Google Scholar 

  5. Jia Y-F, Feng Q, Ge Z-Y, Guo Y, Zhou F, Zhang K-S, et al. Obesity impairs male fertility through long-term effects on spermatogenesis. BMC Urol. 2018;18(1):1–8.

    Article  CAS  Google Scholar 

  6. Azar JT, Maleki AH, Moshari S, Razi M. The effect of different types of exercise training on diet-induced obesity in rats, cross-talk between cell cycle proteins and apoptosis in testis. Gene. 2020;754:144850.

    Article  Google Scholar 

  7. Rato L, Alves MG, Socorro S, Duarte AI, Cavaco JE, Oliveira PF. Metabolic regulation is important for spermatogenesis. Nat Rev Urol. 2012;9(6):330–8.

    Article  CAS  PubMed  Google Scholar 

  8. Andersen JM, Herning H, Aschim EL, Hjelmesæth J, Mala T, Hanevik HI, et al. Body Mass Index Is Associated with Impaired Semen Characteristics and Reduced Levels of Anti-Müllerian Hormone across a Wide Weight Range. PLoS One. 2015;10(6):e0130210.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Wang H, Cai Y, Shao Y, Zhang X, Li N, Zhang H, et al. Fish oil ameliorates high-fat diet induced male mouse reproductive dysfunction via modifying the rhythmic expression of testosterone synthesis related genes. Int J Mol Sci. 2018;19(5):1325.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Yan W-j, Mu Y, Yu N, Yi T-l, Zhang Y, Pang X-l, et al. Protective effects of metformin on reproductive function in obese male rats induced by high-fat diet. J Assist Reprod Genetics. 2015;32(7):1097–104.

    Article  Google Scholar 

  11. Miao XL, Gao GM, Jiang L, Xu R, Wan DP. Asiatic acid attenuates high-fat diet-induced impaired spermatogenesis. Exp Therapeut Med. 2018;15(3):2397–403.

    CAS  Google Scholar 

  12. Elmas MA, Ozakpinar OB, Kolgazi M, Sener G, Arbak S, Ercan F. Exercise improves testicular morphology and oxidative stress parameters in rats with testicular damage induced by a high-fat diet. Andrologia. 2022;54(11):e14600.

    Article  CAS  PubMed  Google Scholar 

  13. Wang EH, Yu ZL, Bu YJ, Xu PW, Xi JY, Liang HY. Grape seed proanthocyanidin extract alleviates high-fat diet induced testicular toxicity in rats. RSC Adv. 2019;9(21):11842–50.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Oliveira PF, Sousa M, Silva BM, Monteiro MP, Alves MG. Obesity, energy balance and spermatogenesis. Reproduction. 2017;153(6):R173–r85.

    Article  CAS  PubMed  Google Scholar 

  15. Rato L, Alves MG, Dias TR, Lopes G, Cavaco JE, Socorro S, et al. High-energy diets may induce a pre-diabetic state altering testicular glycolytic metabolic profile and male reproductive parameters. Andrology. 2013;1(3):495–504.

    Article  CAS  PubMed  Google Scholar 

  16. Voigt AL, Thiageswaran S, de Lima EMLN, Dobrinski I. Metabolic Requirements for Spermatogonial Stem Cell Establishment and Maintenance In Vivo and In Vitro. Int J Mol Sci. 2021;22(4):1998.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Soudmand P, Tofighi A, Tolouei Azar J, Razi M, Ghaderi PF. Different continuous exercise training intensities induced effect on sertoli-germ cells metabolic interaction; implication on GLUT-1, GLUT-3 and MCT-4 transporting proteins expression level. Gene. 2021;783:145553.

    Article  CAS  PubMed  Google Scholar 

  18. Mateus I, Feijó M, Espínola LM, Vaz CV, Correia S, Socorro S. Glucose and glutamine handling in the Sertoli cells of transgenic rats overexpressing regucalcin: plasticity towards lactate production. Sci Rep. 2018;8(1):10321.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Yu J, Sun J, Fan Y, Su J, Xie J, Wu Y, et al. Exposure to Pb and Cd alters MCT4/CD147 expression and MCT4/CD147-dependent lactate transport in mice Sertoli cells cultured in vitro. Toxicol In Vitro. 2019;56:30–40.

    Article  CAS  PubMed  Google Scholar 

  20. Jutte NH, Jansen R, Grootegoed J, Rommerts F, Clausen O, Van der Molen H. Regulation of survival of rat pachytene spermatocytes by lactate supply from Sertoli cells. Reproduction. 1982;65(2):431–8.

    Article  CAS  Google Scholar 

  21. Rato L, Alves MG, Socorro S, Carvalho RA, Cavaco JE, Oliveira PF. Metabolic modulation induced by oestradiol and DHT in immature rat Sertoli cells cultured in vitro. Biosci Rep. 2012;32(1):61–9.

    Article  CAS  PubMed  Google Scholar 

  22. Galardo MN, Riera MF, Pellizzari EH, Cigorraga SB, Meroni SB. The AMP-activated protein kinase activator, 5-aminoimidazole-4-carboxamide-1-bD-ribonucleoside, regulates lactate production in rat Sertoli cells. J Mol Endocrinol. 2007;39(4):279–88.

    Article  CAS  PubMed  Google Scholar 

  23. Bonen A. The expression of lactate transporters (MCT1 and MCT4) in heart and muscle. Eur J Appl Physiol. 2001;86(1):6–11.

    Article  CAS  PubMed  Google Scholar 

  24. Oliveira P, Alves M, Rato L, Silva J, Sa R, Barros A, et al. Influence of 5α-dihydrotestosterone and 17β-estradiol on human Sertoli cells metabolism. Int J Androl. 2011;34(6pt2):e612–e20.

    Article  CAS  PubMed  Google Scholar 

  25. Neirijnck Y, Papaioannou MD, Nef S. The Insulin/IGF System in Mammalian Sexual Development and Reproduction. Int J Mol Sci. 2019;20(18):4440.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Pitetti J-L, Calvel P, Zimmermann C, Conne B, Papaioannou MD, Aubry F, et al. An essential role for insulin and IGF1 receptors in regulating sertoli cell proliferation, testis size, and FSH action in mice. Mol Endocrinol. 2013;27(5):814–27.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Neirijnck Y, Calvel P, Kilcoyne KR, Kühne F, Stévant I, Griffeth RJ, et al. Insulin and IGF1 receptors are essential for the development and steroidogenic function of adult Leydig cells. The FASEB J. 2018;32(6):3321–35.

    Article  CAS  PubMed  Google Scholar 

  28. Oonk RB, Jansen R, Grootegoed JA. Differential effects of follicle-stimulating hormone, insulin, and insulin-like growth factor I on hexose uptake and lactate production by rat Sertoli cells. J Cell Physiol. 1989;139(1):210–8.

    Article  CAS  PubMed  Google Scholar 

  29. Escott GM, de Castro AL, Jacobus AP, Loss ES. Insulin and IGF-I actions on IGF-I receptor in seminiferous tubules from immature rats. Biochim Biophys Acta (BBA) -Biomembranes. 2014;1838(5):1332–7.

    Article  CAS  PubMed  Google Scholar 

  30. Spaliviero JA, Handelsman DJ. Effect of epidermal and insulin-like growth factors on vectorial secretion of transferrin by rat Sertoli cells in vitro. Mol Cell Endocrinol. 1991;81(1-3):95–104.

    Article  CAS  PubMed  Google Scholar 

  31. LeRoith D, Werner H, Beitner-Johnson D, Roberts CT Jr. Molecular and cellular aspects of the insulin-like growth factor I receptor. Endocrine Rev. 1995;16(2):143–63.

    Article  CAS  Google Scholar 

  32. Adams TE, Epa V, Garrett T. Structure and function of the type 1 insulin-like growth factor receptor. Cell Mol Life Sci CMLS. 2000;57(7):1050–93.

    Article  CAS  PubMed  Google Scholar 

  33. Aguirre GA, De Ita JR, de la Garza RG, Castilla-Cortazar I. Insulin-like growth factor-1 deficiency and metabolic syndrome. J Transl Med. 2016;14(1):3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Berryman DE, Glad CA, List EO, Johannsson G. The GH/IGF-1 axis in obesity: pathophysiology and therapeutic considerations. Nat Rev Endocrinol. 2013;9(6):346–56.

    Article  CAS  PubMed  Google Scholar 

  35. Weger BD, Gachon F. The Insulin/Insulin-like Growth Factor signalling connects metabolism with sexual differentiation. Wiley Online Library; 2021. p. e13576.

    Google Scholar 

  36. Pojednic R, D'Arpino E, Halliday I, Bantham A. The Benefits of Physical Activity for People with Obesity, Independent of Weight Loss: A Systematic Review. Int J Environ Res Public Health. 2022;19(9):4981.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Paley CA, Johnson MI. Abdominal obesity and metabolic syndrome: exercise as medicine? BMC Sports Sci Med Rehabil. 2018;10:7.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Oppert JM, Bellicha A, van Baak MA, Battista F, Beaulieu K, Blundell JE, et al. Exercise training in the management of overweight and obesity in adults: Synthesis of the evidence and recommendations from the European Association for the Study of Obesity Physical Activity Working Group. Obes Rev. 2021;22(Suppl 4):e13273.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Khalafi M, Habibi Maleki A, Sakhaei MH, Rosenkranz SK, Pourvaghar MJ, Ehsanifar M, et al. The effects of exercise training on body composition in postmenopausal women: a systematic review and meta-analysis. Front Endocrinol. 2023;14:1183765.

    Article  Google Scholar 

  40. Kolnes KJ, Petersen MH, Lien-Iversen T, Højlund K, Jensen J. Effect of Exercise Training on Fat Loss—Energetic Perspectives and the Role of Improved Adipose Tissue Function and Body Fat Distribution. Front Physiol. 2021;1634:737709.

    Article  Google Scholar 

  41. Niemiro GM, Rewane A, Algotar AM. Exercise and fitness effect on obesity. Treasure Island (FL): StatPearls Publishing; 2019.

    Google Scholar 

  42. Litleskare S, Enoksen E, Sandvei M, Støen L, Stensrud T, Johansen E, et al. Sprint Interval Running and Continuous Running Produce Training Specific Adaptations, Despite a Similar Improvement of Aerobic Endurance Capacity-A Randomized Trial of Healthy Adults. Int J Environ Res Public Health. 2020;17(11):3865.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Kuo CH, Harris MB. Abdominal fat reducing outcome of exercise training: fat burning or hydrocarbon source redistribution? Can J Physiol Pharmacol. 2016;94(7):695–8.

    Article  CAS  PubMed  Google Scholar 

  44. Yi X, Gao H, Chen D, Tang D, Huang W, Li T, et al. Effects of obesity and exercise on testicular leptin signal transduction and testosterone biosynthesis in male mice. Am J Physiol Regul Integr Comp Physiol. 2017;312(4):R501–R10.

    Article  PubMed  Google Scholar 

  45. Yi X, Tang D, Cao S, Li T, Gao H, Ma T, et al. Effect of different exercise loads on testicular oxidative stress and reproductive function in obese male mice. Oxid Med Cell Longev. 2020;2020:3071658. https://doi.org/10.1155/2020/3071658

  46. Akbar Gharehbagh S, Tolouei Azar J, Razi M. ROS and metabolomics-mediated autophagy in rat's testicular tissue alter after exercise training; Evidence for exercise intensity and outcomes. Life Sci. 2021;277:119585.

    Article  CAS  PubMed  Google Scholar 

  47. Uysal N, Agilkaya S, Sisman AR, Camsari UM, Gencoglu C, Dayi A, et al. Exercise increases leptin levels correlated with IGF-1 in hippocampus and prefrontal cortex of adolescent male and female rats. J Chem Neuroanat. 2017;81:27–33.

    Article  CAS  PubMed  Google Scholar 

  48. Huang C-Y, Yang A-L, Lin Y-M, Wu F-N, Lin JA, Chan Y-S, et al. Anti-apoptotic and pro-survival effects of exercise training on hypertensive hearts. J Appl Physiol. 2012;112(5):883–91.

    Article  CAS  PubMed  Google Scholar 

  49. Feng L, Li B, Xi Y, Cai M, Tian Z. Aerobic exercise and resistance exercise alleviate skeletal muscle atrophy through IGF-1/IGF-1R-PI3K/Akt pathway in mice with myocardial infarction. Am J Physiol Cell Physiol. 2022;322(2):C164–c76.

    Article  CAS  PubMed  Google Scholar 

  50. Leme JACA, Silveira RF, Gomes RJ, Moura RF, Sibuya CA, Mello MAR, et al. Long-term physical training increases liver IGF-I in diabetic rats. Growth Hormone IGF Res. 2009;19(3):262–6.

    Article  CAS  Google Scholar 

  51. Chavanelle V, Boisseau N, Otero YF, Combaret L, Dardevet D, Montaurier C, et al. Effects of high-intensity interval training and moderate-intensity continuous training on glycaemic control and skeletal muscle mitochondrial function in db/db mice. Sci Rep. 2017;7(1):204.

    Article  PubMed  PubMed Central  Google Scholar 

  52. Burniston JG. Adaptation of the rat cardiac proteome in response to intensity-controlled endurance exercise. Proteomics. 2009;9(1):106–15.

    Article  CAS  PubMed  Google Scholar 

  53. Chaudhuri GR, Das A, Kesh SB, Bhattacharya K, Dutta S, Sengupta P, et al. Obesity and male infertility: multifaceted reproductive disruption. Middle East Fertil Soc J. 2022;27(1):8.

    Article  Google Scholar 

  54. Zhong O, Ji L, Wang J, Lei X, Huang H. Association of diabetes and obesity with sperm parameters and testosterone levels: a meta-analysis. Diabetol Metab Syndr. 2021;13:1–12.

    Article  Google Scholar 

  55. Alves M, Martins A, Rato L, Moreira P, Socorro S, Oliveira P. Molecular mechanisms beyond glucose transport in diabetes-related male infertility. Biochim Biophys Acta (BBA)-Mol Basis Dis. 2013;1832(5):626–35.

    Article  CAS  Google Scholar 

  56. Abbas Z, Sammad A, Hu L, Fang H, Xu Q, Wang Y. Glucose Metabolism and Dynamics of Facilitative Glucose Transporters (GLUTs) under the Influence of Heat Stress in Dairy Cattle. Metabolites. 2020;10(8):312.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Prokai D, Pudasaini A, Kanchwala M, Moehlman AT, Waits AE, Chapman KM, et al. Spermatogonial gene networks selectively couple to glutathione and pentose phosphate metabolism but not cysteine biosynthesis. Iscience. 2021;24(1):101880.

    Article  CAS  PubMed  Google Scholar 

  58. Rato L, Alves MG, Duarte AI, Santos MS, Moreira PI, Cavaco JE, et al. Testosterone deficiency induced by progressive stages of diabetes mellitus impairs glucose metabolism and favors glycogenesis in mature rat Sertoli cells. Int J Biochem Cell Biol. 2015;66:1–10.

    Article  CAS  PubMed  Google Scholar 

  59. Rato L, Duarte AI, Tomás GD, Santos MS, Moreira PI, Socorro S, et al. Pre-diabetes alters testicular PGC1-α/SIRT3 axis modulating mitochondrial bioenergetics and oxidative stress. Biochim Biophys Acta. 2014;1837(3):335–44.

    Article  CAS  PubMed  Google Scholar 

  60. Abbud W, Habinowski S, Zhang J-Z, Kendrew J, Elkairi FS, Kemp BE, et al. Stimulation of AMP-Activated Protein Kinase (AMPK) Is Associated with Enhancement of Glut1-Mediated Glucose Transport. Arch Biochem Biophys. 2000;380(2):347–52.

    Article  CAS  PubMed  Google Scholar 

  61. Fryer LG, Foufelle F, Barnes K, Baldwin SA, Woods A, Carling D. Characterization of the role of the AMP-activated protein kinase in the stimulation of glucose transport in skeletal muscle cells. Biochem J. 2002;363(1):167–74.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Weisová P, Concannon CG, Devocelle M, Prehn JH, Ward MW. Regulation of glucose transporter 3 surface expression by the AMP-activated protein kinase mediates tolerance to glutamate excitation in neurons. J Neurosci. 2009;29(9):2997–3008.

    Article  PubMed  PubMed Central  Google Scholar 

  63. Alves MG, Martins AD, Cavaco JE, Socorro S, Oliveira PF. Diabetes, insulin-mediated glucose metabolism and Sertoli/blood-testis barrier function. Tissue Barriers. 2013;1(2):e23992.

    Article  PubMed  PubMed Central  Google Scholar 

  64. Silva R, Carrageta DF, Alves MG, Oliveira PF. Testicular Glycogen Metabolism: An Overlooked Source of Energy for Spermatogenesis? BioChem. 2022;2(3):198–214.

    Article  Google Scholar 

  65. Luo D, Zhang M, Su X, Liu L, Zhou X, Zhang X, et al. High fat diet impairs spermatogenesis by regulating glucose and lipid metabolism in Sertoli cells. Life Sci. 2020;257:118028.

    Article  CAS  PubMed  Google Scholar 

  66. Alves MG, Neuhaus-Oliveira A, Moreira PI, Socorro S, Oliveira PF. Exposure to 2,4-dichlorophenoxyacetic acid alters glucose metabolism in immature rat Sertoli cells. Reprod Toxicol. 2013;38:81–8.

    Article  CAS  PubMed  Google Scholar 

  67. Suleiman JB, Nna VU, Zakaria Z, Othman ZA, Bakar ABA, Usman UZ, et al. Orlistat reverses intratesticular lactate transport decline and infertility in male obese rats. Reproduction. 2020;160(6):863–72.

    Article  CAS  PubMed  Google Scholar 

  68. Griffeth RJ, Bianda V, Nef S. The emerging role of insulin-like growth factors in testis development and function. Basic Clin Androl. 2014;24:12.

    Article  PubMed  PubMed Central  Google Scholar 

  69. Bagheri-Fam S, Argentaro A, Svingen T, Combes AN, Sinclair AH, Koopman P, et al. Defective survival of proliferating Sertoli cells and androgen receptor function in a mouse model of the ATR-X syndrome. Hum Mol Genet. 2011;20(11):2213–24.

    Article  CAS  PubMed  Google Scholar 

  70. Escott GM, Jacobus AP, Loss ES. PI3K-dependent actions of insulin and IGF-I on seminiferous tubules from immature rats. Pflugers Arch. 2013;465(10):1497–505.

    Article  CAS  PubMed  Google Scholar 

  71. Arjunan A, Sah DK, Woo M, Song J. Identification of the molecular mechanism of insulin-like growth factor-1 (IGF-1): a promising therapeutic target for neurodegenerative diseases associated with metabolic syndrome. Cell Biosci. 2023;13(1):16.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

The authors would like to acknowledge that this research constitutes a segment of the Ph.D. thesis, approved by the Research Deputy of Urmia University. Additionally, the authors express gratitude to the RASTA Specialized Research Institute (RSRI) for their assistance in the laboratory. Lastly, we extend our appreciation to the Faculties of Sport Sciences and Veterinary Medicine for their support.

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Aref Habibi Maleki: Conceptualization, Data curation, Formal analysis, Investigation, Methodology Validation, Writing – original draft.

Javad Tolouei Azar: Conceptualization, Methodology, Formal analysis, Supervised the research, Writing – review & editing.

Mazdak Razi: Conceptualization, Formal analysis, Supervised the laboratory and statistical analyses, Writing – review & editing.

Asghar Tofighi: Conceptualization, Methodology, Review & editing.

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Correspondence to Javad Tolouei Azar.

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Maleki, A.H., Azar, J.T., Razi, M. et al. The Effect of Different Exercise Modalities on Sertoli-germ Cells Metabolic Interactions in High-fat Diet-induced Obesity Rat Models: Implication on Glucose and Lactate Transport, Igf1, and Igf1R-dependent Pathways. Reprod. Sci. (2024). https://doi.org/10.1007/s43032-024-01533-8

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