The effect of eight weeks of swimming training, cell and laser therapy on the expression of IL-2, IL-10 and STAT-3 genes in testicular tissue in azoospermia model rat.
Subject Areas : Effect of Physical Activity on Diseasesseyed sasan Hoseyni 1 , Habib Asgharpour 2 , پروین فرزانگی 3
1 - Department of Physical Education & sports sciences, Aliabad Katoul Branch, Islamic Azad University, Ali Abad Katool, Iran
2 - Department of Exercise Physiology, Ali Abad Katool Branch, Islamic Azad University, Ali Abad Katool, Iran
3 - عضو هیات علمی
Keywords: Azoospermia, swimming training, cell therapy, laser therapy and IL-10/STAT-3 signaling,
Abstract :
purpose: Azoospermia means lack of sperm in semen. One percent of all men and ten percent of infertile men suffer from azoospermia, the purpose of this study is to investigate the effects of eight weeks of swimming training, cell and laser therapy on the expression of IL-2, IL-10 and STAT-3 genes in testicular tissue. It is azoospermia in rats. Methods: Forty 6- to 8-week-old rats were randomly selected, and then the azoospermia model was induced with Busulfan at a dose of 40 mg in mice. One month after induction of the model, stem cells were transplanted once in the vas deferens at the rate of one million cells per mouse. Then, one week after cell transplantation, a laser with a wavelength of 632.8 nm and a power of 10 mW and energy 3 joules were applied in three repetitions throughout the study period with an interval of once a week, and after improving the effects of surgery, swimming training were performed for 30 minutes and 5 days a week for 8 weeks. Results: The results showed that induction of azoospermia model caused a significant increase in IL-2, IL-10 and STAT-3 genes compared to healthy group rats (P≤0.05). Also, performing the interventional methods of laser therapy, cell therapy and exercise significantly reduced the expression of these genes in the testicular tissue of rats compared to the patient group (P≤0.05). Conclusion: Swimming exercise in combination with cell and laser therapy may help the fertility of azoospermia model rats by reducing testicular tissue inflammation signaling.
1. Moskvin SV, Apolikhin OI. Effectiveness of low level laser therapy for treating male infertility. BioMedicine. 2018 Jun;8(2).
2. He Z, Kokkinaki M, Jiang J, Zeng W, Dobrinski I, Dym M. Isolation of human male germ-line stem cells using enzymatic digestion and magnetic-activated cell sorting. Germline Development: Methods and Protocols. 2012:45-57.
3. Loveland KL, Klein B, Pueschl D, Indumathy S, Bergmann M, Loveland BE, Hedger MP, Schuppe HC. Cytokines in male fertility and reproductive pathologies: immunoregulation and beyond. Frontiers in Endocrinology. 2017 Nov 20;8:307.
4. Syriou V, Papanikolaou D, Kozyraki A, Goulis DG. Cytokines and male infertility. European cytokine network. 2018 Sep;29:73-82.
5. Jiang W, Xu J. Immune modulation by mesenchymal stem cells. Cell proliferation. 2020 Jan;53(1):e12712.
6. Tao L, Bei Y, Lin S, Zhang H, Zhou Y, Jiang J, Chen P, Shen S, Xiao J, Li X. Exercise training protects against acute myocardial infarction via improving myocardial energy metabolism and mitochondrial biogenesis. Cellular Physiology and Biochemistry. 2015 Aug 1;37(1):162-75.
7. Rashidpour F, Farzanegi P, Abbaszadeh H. Evaluation of Cyclooxygenase-2 and Prostaglandin E2 Expression in Endometrial Tissue Following 8 Weeks of Swimming Exercise and Omega-3 Intake. Medical Laboratory Journal. 2023 Mar 1;17(2).
8. Urhausen A, Kullmer T, Kindermann W. A 7-week follow-up study of the behaviour of testosterone and cortisol during the competition period in rowers. European journal of applied physiology and occupational physiology. 1987 Sep;56:528-33.
9. Vaamonde D, Garcia-Manso JM, Hackney AC. Impact of physical activity and exercise on male reproductive potential: a new assessment questionnaire. Revista andaluza de medicina del deporte. 2017 Jun 1;10(2):79-93.
10. Thompson M, Mei SH, Wolfe D, Champagne J, Fergusson D, Stewart DJ, et al. Cell therapy with intravascular administration of mesenchymal stromal cells continues to appear safe: an updated systematic review and meta-analysis. EClinicalMedicine. 2020;19:100249.
11. Zhankina R, Baghban N, Askarov M, Saipiyeva D, Ibragimov A, Kadirova B, Khoradmehr A, Nabipour I, Shirazi R, Zhanbyrbekuly U, Tamadon A. Mesenchymal stromal/stem cells and their exosomes for restoration of spermatogenesis in non-obstructive azoospermia: a systemic review. Stem Cell Research & Therapy. 2021 Dec;12:1-2.
12. Manaph NPA, Sivanathan KN, Nitschke J, Zhou X-F, Coates PT, Drogemuller CJ. An overview on small molecule-induced differentiation of mesenchymal stem cells into beta cells for diabetic therapy. Stem Cell Res Ther. 2019; 10(1):293.
13. Qian C, Meng Q, Lu J, Zhang L, Li H, Huang B. Human amnion mesenchymal stem cells restore spermatogenesis in mice with busulfaninduced testis toxicity by inhibiting apoptosis and oxidative stress. Stem Cell Res Ther 2020;11(1):1–12.
14. Yeung CLA, Co N-N, Tsuruga T, Yeung T-L, Kwan S-Y, Leung CS, et al. Exosomal transfer of stroma-derived miR21 confers paclitaxel resistance in ovarian cancer cells through targeting APAF1. Nat Commun. 2016;7(1):1–14.
15. Apolikhin OI, Moskvin SV. Laser therapy for male infertility. Part 1. Etiology and pathogenesis. experimental studies. Urologiia. 2017 Dec 15(5):115-23.
16. Deihimi M, Azornia M, Takzare N. Effect of red and infrared spectrum low level of laser rays on Rat Seminiferous tubules. Journal of Gorgan University of Medical Sciences. 2010 Sep 10;12(3):10-7.
17. Tajalli H, Maleki M, Safavi E, Shahi R, Firoozi F, Akbarpour Z, Sotoudeh Khyaban A. The effects of low-power laser on the promotion of spermatogenesis in a mouse model of azoospermia (in-vivo). International Journal of Biophotonics and Biomedical Engineering. 2022 Dec 28;2(1):15-30.
18. Karami E, Rostamkhani F. The effects of high-intensity interval training on the expression of interleukin-10 and STAT3 genes in the intestinal tissue of rats affected by hepatic steatosis. Journal of Exercise & Organ Cross Talk. 2022 Dec 1;2(4):150-4.
19. Shaw DM, Merien F, Braakhuis A, Dulson D. T-cells and their cytokine production: The anti-inflammatory and immunosuppressive effects of strenuous exercise. Cytokine. 2018 Apr 1;104:136-42.
20. Batista Júnior ML, Lopes RD, Seelaender MC, Lopes AC. Anti-inflammatory effect of physical training in heart failure: role of TNF-α and IL-10. Arquivos Brasileiros de Cardiologia. 2009;93:692-700.
21. Hallsworth K, Thoma C, Hollingsworth KG, Cassidy S, Anstee QM, Day CP, Trenell MI. Modified high-intensity interval training reduces liver fat and improves cardiac function in non-alcoholic fatty liver disease: a randomized controlled trial. Clinical science. 2015 Dec 1;129(12):1097-105.
22. Nicklas BJ, You T, Pahor M. Behavioural treatments for chronic systemic inflammation: effects of dietary weight loss and exercise training. Cmaj. 2005 Apr 26;172(9):1199-209.
23. Vahdat H, Mombini H, Eslami Farsani M, Ab Abzadeh S, Barzegar H. Effect of High-Intensity Interval Training (HIIT) on the levels of Irisin and interleukin-10 in overweight men. Qom University of Medical Sciences Journal. 2018 Apr 10;12(2):35-44.
24. Dorneles GP, Haddad DO, Fagundes VO, Vargas BK, Kloecker A, Romão PR, Peres A. High intensity interval exercise decreases IL-8 and enhances the immunomodulatory cytokine interleukin-10 in lean and overweight–obese individuals. Cytokine. 2016 Jan 1;77:1-9.
25. Glocker EO, Kotlarz D, Boztug K, Gertz EM, Schäffer AA, Noyan F, Perro M, Diestelhorst J, Allroth A, Murugan D, Hätscher N. Inflammatory bowel disease and mutations affecting the interleukin-10 receptor. New England Journal of Medicine. 2009 Nov 19;361(21):2033-45.
26. Rodrigues Brandao-Rangel MA, Bachi AL, Oliveira-Junior MC, Abbasi A, Silva-Renno A, Aparecida de Brito A, Ligeiro de Oliveira AP, Choqueta Toledo-Arruda A, Belvisi MG, Paula Vieira R. Exercise inhibits the effects of smoke-induced COPD involving modulation of STAT3. Oxidative Medicine and Cellular Longevity. 2017 Jan 1;2017.
27. Jia D, Cai M, Xi Y, Du S. Interval exercise training increases LIF expression and prevents myocardial infarction-induced skeletal muscle atrophy in rats. Life sciences. 2018 Jan 15;193:77-86.
28. Hou C, Sun F, Liang Y, Nasab EM, Athari SS. Effect of transduced mesenchymal stem cells with IL-10 gene on control of allergic asthma. Allergologia et Immunopathologia. 2023 Mar 1;51(2):45-51.
29. Knight D, Mutsaers SE, Prêle CM. STAT3 in tissue fibrosis: is there a role in the lung?. Pulmonary pharmacology & therapeutics. 2011 Apr 1;24(2):193-8.
30. Branchett WJ, Stölting H, Oliver RA, Walker SA, Puttur F, Gregory LG, Gabryšová L, Wilson MS, O'Garra A, Lloyd CM. AT cell–myeloid IL-10 axis regulates pathogenic IFN-γ–dependent immunity in a mouse model of type 2–low asthma. Journal of Allergy and Clinical Immunology. 2020 Feb 1;145(2):666-78.
31. Minshawi F, Lanvermann S, McKenzie E, Jeffery R, Couper K, Papoutsopoulou S, Roers A, Muller W. The generation of an engineered interleukin-10 protein with improved stability and biological function. Frontiers in Immunology. 2020 Aug 11;11:1794.
32. Aghamir SMK, Salavati A, Yousefie R, Tootian Z, Ghazaleh N, Jamali M, Azimi P. Does bone marrow–derived mesenchymal stem cell transfusion prevent antisperm antibody production after traumatic testis rupture? Urology. 2014; 84(1):82–6.
33. Abdelaziz MH, Salah El-Din EY, El-Dakdoky MH, Ahmed TA. The impact of mesenchymal stem cells on doxorubicin-induced testicular toxicity and progeny outcome of male prepubertal rats. Birth Defects Res. 2019;111(13): 906–19.
34. Hsiao C-H, Ji AT-Q, Chang C-C, Cheng C-J, Lee L-M, Ho JH-C. Local injection of mesenchymal stem cells protects testicular torsion-induced germ cell injury. Stem Cell Res Ther. 2015;6(1):113. https://doi.org/10.1186/s13287-015- 0079-0.
35. Xing X, Zhang Z, Zhong L, Ju G, Zou X, Zhu Y, Sun J. Differentiation of human umbilical cord mesenchymal stem cells into steroidogenic cells in vitro. Exp Ther Med. 2016;12(6):3527–34. https://doi.org/10.3892/etm.201 6.3815.
36. Ghasemzadeh-Hasankolaei M, Batavani R, Eslaminejad MB, Sayahpour F. Transplantation of autologous bone marrow mesenchymal stem cells into the testes of infertile male rats and new germ cell formation. Int J Stem Cells. 2016;9(2):250–63.
37. Badawy AA, El-Magd MA, AlSadrah SA, Alruwaili MM. Altered expression of some miRNAs and their target genes following mesenchymal stem cell treatment in busulfan-induced azoospermic rats. Gene. 2020;737:144481.
38. Wang DZ, Zhou XH, Yuan YL, Zheng XM. Optimal dose of busulfan for depleting testicular germ cells of recipient mice before spermatogonial transplantation. Asian Journal of Andrology. 2010 Mar;12(2):263.
39. Zohni K, Zhang X, Tan SL, Chan P, Nagano MC. The efficiency of male fertility restoration is dependent on the recovery kinetics of spermatogonial stem cells after cytotoxic treatment with busulfan in mice. Human reproduction. 2012 Jan 1;27(1):44-53.
40. Tamadon A, Mehrabani D, Rahmanifar F, Jahromi AR, Panahi M, Zare S, Khodabandeh Z, Jahromi IR, Tanideh N, Dianatpour M, Ramzi M. Induction of spermatogenesis by bone marrow-derived mesenchymal stem cells in busulfan-induced azoospermia in hamster. International journal of stem cells. 2015 Nov 30;8(2):134-45.
41. Allameh F, Razzaghi M, Hosseini S, Barati M, Razzaghi Z, Salehi S, Ghahestani SM, Shahabi V. The effect of laser acupuncture on semen parameters in infertile men with oligospermia: A randomized clinical trial. Journal of Lasers in Medical Sciences. 2021;12.
42. Gabel CP, Carroll J, Harrison K. Sperm motility is enhanced by low level laser and light emitting diode photobiomodulation with a dose-dependent response and differential effects in fresh and frozen samples. Laser therapy. 2018;27(2):131-6.
43. Firestone RS, Esfandiari N, Moskovtsev SI, Burstein E, Videna GT, Librach C, Bentov Y, Casper RF. The effects of low‐level laser light exposure on sperm motion characteristics and DNA damage. Journal of andrology. 2012 May 6;33(3):469-73.
44. Rezaei F, Bayat M, Nazarian H, Aliaghaei A, Abaszadeh HA, Naserzadeh P, Amini A, Ebrahimi V, Abdi S, Abdollahifar MA. Photobiomodulation therapy improves spermatogenesis in busulfan-induced infertile mouse. Reproductive Sciences. 2021 Oct 1:1-0.