Sat, Apr 20, 2024
Volume 16, Issue 1 (Jan-Feb 2022)
mljgoums 2022, 16(1): 32-39 |
Back to browse issues page
Download citation:
BibTeX | RIS | EndNote | Medlars | ProCite | Reference Manager | RefWorks
Send citation to:
BibTeX | RIS | EndNote | Medlars | ProCite | Reference Manager | RefWorks
Send citation to:
Torabi H, Eizadi M, Jalalvand A, Zarrinkalam E. Anti-Diabetic Effect of Long-Term Aerobic Training in Type 2 Diabetic Rats with Emphasis on Adiponectin Expression in Subcutaneous Adipose Tissue. mljgoums 2022; 16 (1) :32-39
URL: http://mlj.goums.ac.ir/article-1-1345-en.html
URL: http://mlj.goums.ac.ir/article-1-1345-en.html
1- Department of Exercise Physiology, Borujerd Branch, Islamic Azad University, Borujerd, Iran
2- Department of Exercise Physiology, Saveh Branch, Islamic Azad University, Saveh, Iran , izadimojtaba2006@yahoo.com
3- Department of Sports Biomechanics, Hamedan Branch, Islamic Azad University, Hamedan, Iran
4- Department of Exercise Physiology, Hamedan Branch, Islamic Azad University, Hamedan, Iran
2- Department of Exercise Physiology, Saveh Branch, Islamic Azad University, Saveh, Iran , izadimojtaba2006@yahoo.com
3- Department of Sports Biomechanics, Hamedan Branch, Islamic Azad University, Hamedan, Iran
4- Department of Exercise Physiology, Hamedan Branch, Islamic Azad University, Hamedan, Iran
Abstract: (3559 Views)
Background and objectives: Clinical evidence has demonstrated the important role of adiponectin in insulin signaling pathways in target tissue. The aim of this study was to determine effects of aerobic training on insulin sensitivity, glucose level, and adiponectin expression in subcutaneous adipose tissue of type 2 diabetic rats.
Methods: Type 2 diabetes was induced in 14 male wistar rats by intraperitoneal injection of nicotine amide and streptozotocin. The rats were randomly divided into an exercise group (n=7) and a control group (n=7). The rats in the exercise group performed aerobic training in from of treadmill running, five sessions a week, for 12 weeks. Subjects in the control group did not perform any training. Glucose level, insulin level, insulin sensitivity, and adiponectin expression in subcutaneous adipose tissue were determined at baseline and 48 hours after the lasting training session. Independent t-test was used for comparing the variables between the study groups.
Results: Aerobic training resulted in a significant increase in serum insulin (p=0.006), insulin sensitivity (p=0.003), and adiponectin expression in subcutaneous adipose tissue (p=0.037) compared with the control group. In addition, the training caused a significant decrease in fasting glucose level compared with the control group (p<0.001).
Conclusion: Based on these findings, the decrease in blood glucose may be attributed to the improvement of adiponectin-dependent insulin signaling pathways in adipose tissue in response to aerobic training. However, more cellular-molecular studies are needed to understand the mechanisms responsible for these changes.
Methods: Type 2 diabetes was induced in 14 male wistar rats by intraperitoneal injection of nicotine amide and streptozotocin. The rats were randomly divided into an exercise group (n=7) and a control group (n=7). The rats in the exercise group performed aerobic training in from of treadmill running, five sessions a week, for 12 weeks. Subjects in the control group did not perform any training. Glucose level, insulin level, insulin sensitivity, and adiponectin expression in subcutaneous adipose tissue were determined at baseline and 48 hours after the lasting training session. Independent t-test was used for comparing the variables between the study groups.
Results: Aerobic training resulted in a significant increase in serum insulin (p=0.006), insulin sensitivity (p=0.003), and adiponectin expression in subcutaneous adipose tissue (p=0.037) compared with the control group. In addition, the training caused a significant decrease in fasting glucose level compared with the control group (p<0.001).
Conclusion: Based on these findings, the decrease in blood glucose may be attributed to the improvement of adiponectin-dependent insulin signaling pathways in adipose tissue in response to aerobic training. However, more cellular-molecular studies are needed to understand the mechanisms responsible for these changes.
Research Article: Original Paper |
Subject:
Sport Physiology
Received: 2020/11/16 | Accepted: 2021/01/1 | Published: 2021/12/29 | ePublished: 2021/12/29
Received: 2020/11/16 | Accepted: 2021/01/1 | Published: 2021/12/29 | ePublished: 2021/12/29
References
1. Cho NH, Shaw JE, Karuranga S, Huang Y, da Rocha Fernandes JD, et al. IDF Diabetes Atlas: Global estimates of diabetes prevalence for 2017 and projections for 2045. Diabetes Res Clin Pract. 2018 ;138:271-281. [View at Publisher] [DOI:10.1016/j.diabres.2018.02.023] [PubMed] [Google Scholar]
2. Larejani B, Zahedi F. Epidemiology of diabetes mellitus in Iran. Iranian Journal Diabetes and Metabolism. 2001; 1(1):1-8. (In Persian). [View at Publisher] [Google Scholar]
3. Sheikh Abumasoudi R, Salarvand S, Fesharaki H, Atashi V, Moghimian M, Kashani F, et al. The effect of electronic education and Short Message Service on hemoglobin A1C, interdialytic weight gain and blood pressure in diabetic patients undergoing hemodialysis. Nursing and Midwifery Journal. 2015; 13(7):9-620. (In Persian). [View at Publisher] [Google Scholar]
4. Meigs JB. The metabolic syndrome. BMJ. 2003 12;327(7406):61-2. [View at Publisher] [DOI:10.1136/bmj.327.7406.61] [PubMed] [Google Scholar]
5. Trujillo ME, Scherer PE. Adiponectin--journey from an adipocyte secretory protein to biomarker of the metabolic syndrome. J Intern Med. 2005 ;257(2):167-75. [View at Publisher] [DOI:10.1111/j.1365-2796.2004.01426.x] [PubMed] [Google Scholar]
6. Takahashi M, Arita Y, Yamagata K, Matsukawa Y, Okutomi K, Horie M, Shimomura I, Hotta K, Kuriyama H, Kihara S, Nakamura T, Yamashita S, Funahashi T, Matsuzawa Y. Genomic structure and mutations in adipose-specific gene, adiponectin. Int J Obes Relat Metab Disord. 2000 ;24(7):861-8. [View at Publisher] [DOI:10.1038/sj.ijo.0801244] [PubMed] [Google Scholar]
7. Kim JY, van de Wall E, Laplante M, Azzara A, Trujillo ME, Hofmann SM, et al. Obesity-associated improvements in metabolic profile through expansion of adipose tissue. J Clin Invest. 2007 ;117(9):2621-37. [DOI:10.1172/JCI31021] [PubMed] [Google Scholar]
8. Kantartzis K, Rittig K, Balletshofer B, Machann J, Schick F, Porubska K, et al . The relationships of plasma adiponectin with a favorable lipid profile, decreased inflammation, and less ectopic fat accumulation depend on adiposity. Clin Chem. 2006 ;52(10):1934-42. [View at Publisher] [DOI:10.1373/clinchem.2006.067397] [PubMed] [Google Scholar]
9. Chandran M, Phillips SA, Ciaraldi T, Henry RR. Adiponectin: more than just another fat cell hormone? Diabetes Care. 2003 ;26(8):2442-50. [DOI:10.2337/diacare.26.8.2442] [PubMed] [Google Scholar]
10. Pischon T, Girman CJ, Hotamisligil GS, Rifai N, Hu FB, Rimm EB. Plasma adiponectin levels and risk of myocardial infarction in men. JAMA 2004; 291:1730-7. [DOI:10.1001/jama.291.14.1730] [PubMed] [Google Scholar]
11. Hu E, Liang P, Spiegelman BM. AdipoQ is a novel adipose-specific gene dysregulated in obesity. J Biol Chem. 1996 3;271(18):10697-703. [View at Publisher] [DOI:10.1074/jbc.271.18.10697] [PubMed] [Google Scholar]
12. Hotta K, Funahashi T, Bodkin NL, Ortmeyer HK, Arita Y, Hansen BC,et al. Circulating concentrations of the adipocyte protein adiponectin are decreased in parallel with reduced insulin sensitivity during the progression to type 2 diabetes in rhesus monkeys. Diabetes. 2001 ;50(5):1126-33. [View at Publisher] [DOI:10.2337/diabetes.50.5.1126] [PubMed] [Google Scholar]
13. Daimon M, Oizumi T, Saitoh T, Kameda W, Hirata A, Yamaguchi H, et al. Decreased serum levels of adiponectin are a risk factor for the progression to type 2 diabetes in the Japanese Population: the Funagata study. Diabetes Care. 2003 ;26(7):2015-20. [View at Publisher] [DOI:10.2337/diacare.26.7.2015] [PubMed] [Google Scholar]
14. Nayak BS, Ramsingh D, Gooding S, Legall G, Bissram S, Mohammed A, et al. Plasma adiponectin levels are related to obesity, inflammation, blood lipids and insulin in type 2 diabetic and non-diabetic Trinidadians. Prim Care Diabetes. 2010 ;4(3):187-92. [View at Publisher] [DOI:10.1016/j.pcd.2010.05.006] [PubMed] [Google Scholar]
15. Pischon T, Girman CJ, Hotamisligil GS, Rifai N, Hu FB, Rimm EB. Plasma adiponectin levels and risk of myocardial infarction in men. JAMA. 2004 14;291(14):1730-7. [DOI:10.1001/jama.291.14.1730] [PubMed] [Google Scholar]
16. Adamczak M, Wiecek A, Funahashi T, Chudek J, Kokot F, et al. Decreased plasma adiponectin concentration in patients with essential hypertension. Am J Hypertens. 2003 ;16(1):72-5. [View at Publisher] [DOI:10.1016/S0895-7061(02)03197-7] [PubMed] [Google Scholar]
17. Bidulescu A, Dinh PC Jr, Sarwary S, Forsyth E, Luetke MC, King DB,et al. Associations of leptin and adiponectin with incident type 2 diabetes and interactions among African Americans: the Jackson heart study. BMC Endocr Disord. 2020 4;20(1):31. [View at Publisher] [DOI:10.1186/s12902-020-0511-z] [PubMed] [Google Scholar]
18. Bauer S, Weigert J, Neumeier M, Wanninger J, Schäffler A, Luchner A, et al. Low-abundant adiponectin receptors in visceral adipose tissue of humans and rats are further reduced in diabetic animals. Arch Med Res. 2010 ;41(2):75-82. [View at Publisher] [DOI:10.1016/j.arcmed.2010.02.010] [PubMed] [Google Scholar]
19. Ye JM, Doyle PJ, Iglesias MA, Watson DG, Cooney GJ, Kraegen EW. Peroxisome proliferator-activated receptor (PPAR)-_ activation lowers muscle lipids and improves insulin sensitivity in high fat-fed rats. Diabetes 2001; 50: 411-417. [View at Publisher] [DOI:10.2337/diabetes.50.2.411] [PubMed] [Google Scholar]
20. Berg AH, Combs TP, Du X, Brownlee M, Scherer PE. The adipocyte-secreted protein Acrp30 enhances hepatic insulin action. Nat Med. 2001 ;7(8):947-53. [View at Publisher] [DOI:10.1038/90992] [PubMed] [Google Scholar]
21. Combs TP, Berg AH, Obici S, Scherer PE, Rossetti L. Endogenous glucose production is inhibited by the adipose-derived protein Acrp30. J Clin Invest. 2001 ;108(12):1875-81. [View at Publisher] [DOI:10.1172/JCI14120] [PubMed] [Google Scholar]
22. Fruebis J, Tsao TS, Javorschi S, Ebbets-Reed D, Erickson MR, Yen FT, et al. Proteolytic cleavage product of 30-kDa adipocyte complement-related protein increases fatty acid oxidation in muscle and causes weight loss in mice. Proc Natl Acad Sci U S A. 2001 13;98(4):2005-10. [View at Publisher] [DOI:10.1073/pnas.98.4.2005] [PubMed] [Google Scholar]
23. Yamauchi T, Kamon J, Waki H. Globular adiponectin protected ob/ob mice from diabetes and ApoE-deficient mice from atherosclerosis. J. Biol. Chem. 2003; 278: 2461-2468. [View at Publisher] [DOI:10.1074/jbc.M209033200] [PubMed] [Google Scholar]
24. Nawrocki AR, Rajala MW, Tomas E. Micelackingadiponectinshow decreased hepatic insulin sensitivity and reduced responsiveness to peroxisome proliferator-activated receptor g agonists. J. Biol. Chem. 2006; 281: 2654-2660. [View at Publisher] [DOI:10.1074/jbc.M505311200] [Google Scholar]
25. Ferguson MA, White LJ, McCoy S, Kim HW, Petty T, Wilsey J. Plasma adiponectin response to acute exercise in healthy subjects. Eur J Appl Physiol. 2004 ;91(2-3):324-9. [View at Publisher] [DOI:10.1007/s00421-003-0985-1] [PubMed] [Google Scholar]
26. Punyadeera C, Zorenc AH, Koopman R, McAinch AJ, Smit E, Manders R, et al. The effects of exercise and adipose tissue lipolysis on plasma adiponectin concentration and adiponectin receptor expression in human skeletal muscle. Eur J Endocrinol 2005; 152:427-436. [DOI:10.1530/eje.1.01872] [PubMed] [Google Scholar]
27. Balagopal P, George D, Yarandi H, Funanage V, Bayne E. Reversal of obesity-related hypoadiponectinemia by lifestyle intervention: a controlled, randomized study in obese adolescents. J Clin Endocrinol Metab. 2005 ;90(11):6192-7. [View at Publisher] [DOI:10.1210/jc.2004-2427] [PubMed] [Google Scholar]
28. Kondo T, Kobayashi I, Murakami M. Effect of exercise on circulating adipokine levels in obese young women. Endocr J. 2006 ;53(2):189-95. [DOI:10.1507/endocrj.53.189] [PubMed] [Google Scholar]
29. Bluher M, Bullen JW, Lee JH, Kralisch S, Fasshauer M, Kloting N, et al. Circulating adiponectin and expression of adiponectin receptors in human skeletal muscle: associations with metabolic parameters and insulin resistance and regulation by physical training. J Clin Endocrinol Metab 2006; 91:2310-2316. [View at Publisher] [DOI:10.1210/jc.2005-2556] [PubMed] [Google Scholar]
30. Oberbach A, Tonjes A, Kloting N, Fasshauer M, Kratzsch J, Busse MW, et al. Effect of a 4 week physical training program on plasma concentrations of inflammatory markers in patients with abnormal glucose tolerance. Eur J Endocrinol 2006; 154:577-585. [DOI:10.1530/eje.1.02127] [PubMed] [Google Scholar]
31. de Bem GF, Costa CA, Santos IB, Cristino Cordeiro VDS, de Carvalho LCRM, de Souza MAV, et al. Antidiabetic effect of Euterpe oleracea Mart. (açaí) extract and exercise training on high-fat diet and streptozotocin-induced diabetic rats: A positive interaction. PLoS One. 2018 19;13(6):e0199207. [View at Publisher] [DOI:10.1371/journal.pone.0199207] [PubMed] [Google Scholar]
32. Polak J, Klimcakova E, Moro C, Viguerie N, Berlan M, Hejnova J,et al. Effect of aerobic training on plasma levels and subcutaneous abdominal adipose tissue gene expression of adiponectin, leptin, interleukin 6, and tumor necrosis factor alpha in obese women. Metabolism. 2006 ;55(10):1375-81. [View at Publisher] [DOI:10.1016/j.metabol.2006.06.008] [PubMed] [Google Scholar]
33. Marcell TJ, McAuley KA, Traustadóttir T, Reaven PD. Exercise training is not associated with improved levels of C-reactive protein or adiponectin. Metabolism. 2005 ;54(4):533-41. [View at Publisher] [DOI:10.1016/j.metabol.2004.11.008] [PubMed] [Google Scholar]
34. Yokoyama H, Emoto M, Araki T, Fujiwara S, Motoyama K, Morioka T, et al. Effect of aerobic exercise on plasma adiponectin levels and insulin resistance in type 2 diabetes. Diabetes Care. 2004 ;27(7):1756-8. [DOI:10.2337/diacare.27.7.1756] [PubMed] [Google Scholar]
35. Eizadi M, Soory R, Ravasi A, Baesy K, Choobineh S. Relationship between TCF7L2 Relative Expression in Pancreas Tissue with Changes in Insulin by High Intensity Interval Training (HIIT) in Type 2 Diabetes Rats . JSSU. 2017; 24 (12) :981-993 [Google Scholar]
36. Eizadi M, Ravasi AA, Soori R, Baesi K, Choubineh S. Effect of three months aerobic training on TCF7L2 expression in pancreatic tissue in type 2 diabet es rats induced by streptozotocin- nicotinamide. Feyz 2017; 21(1): 1-8. [DOI:10.17795/ajmb-34014] [Google Scholar]
37. McAuley KA, Williams SM, Mann JI, Walker RJ, Lewis-Barned NJ, Temple LA, et al. Diagnosing insulin resistance in the general population. Diabetes Care. 2001 [DOI:10.2337/diacare.24.3.460] [PubMed] [Google Scholar]
38. Lopes FL, Desmarais J, Gevry NY, Ledoux S, Murphy BD. Expression of vascular endothelial growth factor isoforms and receptors Flt-1 and KDR during the peri-implantation period in the mink, Mustela vison. Biol Reprod. 2003 [View at Publisher] [DOI:10.1095/biolreprod.102.013441] [PubMed] [Google Scholar]
39. Maltais ML, Perreault K, Courchesne-Loyer A, Lagacé JC, Barsalani R, Dionne IJ. Effect of Resistance Training and Various Sources of Protein Supplementation on Body Fat Mass and Metabolic Profile in Sarcopenic Overweight Older Adult Men: A Pilot Study. Int J Sport Nutr Exerc Metab. 2016 Feb; 26(1):71-7. [DOI:10.1123/ijsnem.2015-0160] [Google Scholar]
40. Vancea DM, Vancea JN, Pires MI, Reis MA, Moura RB, Dib SA. Effect of frequency of physical exercise on glycemic control and body composition in type 2 diabetic patients. Arq Bras Cardiol. 2009 ;92(1):23-30. [DOI:10.1590/S0066-782X2009000100005] [PubMed] [Google Scholar]
41. Glans F, Eriksson KF, Segerström A, Thorsson O, Wollmer P, Groop L. Evaluation of the effects of exercise on insulin sensitivity in Arabian and Swedish women with type 2 diabetes. Diabetes Res Clin Pract. 2009 ;85(1):69-74. [View at Publisher] [DOI:10.1016/j.diabres.2009.04.018] [PubMed] [Google Scholar]
42. Oliveira CAM, Paiva MF, Mota CAS, Ribeiro C, Leme JACA, Luciano E, et al. Exercise at anaerobic threshold intensity and insulin secretion by isolated pancreatic islets of rats. Islets. 2010 ; 2(4):240-6. [DOI:10.4161/isl.2.4.12266] [PubMed] [Google Scholar]
43. Lopes WA, Leite N, da Silva LR, Brunelli DT, Gáspari AF, Radominski RB, et al. Effects of 12 weeks of combined training without caloric restriction on inflammatory markers in overweight girls. J Sports Sci. 2016 ;34(20):1902-12. [View at Publisher] [DOI:10.1080/02640414.2016.1142107] [PubMed] [Google Scholar]
44. Abd El-Kader S, Gari A, Salah El-Den A. Impact of moderate versus mild aerobic exercise training on inflammatory cytokines in obese type 2 diabetic patients: a randomized clinical trial. Afr Health Sci. 2013 ;13(4):857-63. [DOI:10.4314/ahs.v13i4.1] [PubMed] [Google Scholar]
45. Lee S, Norheim F, Langleite TM, Gulseth HL, Birkeland KI, Drevon CA. Effects of long-term exercise on plasma adipokine levels and inflammation-related gene expression in subcutaneous adipose tissue in sedentary dysglycaemic, overweight men and sedentary normoglycaemic men of healthy weight. Diabetologia. 2019 ;62(6):1048-1064. [View at Publisher] [DOI:10.1007/s00125-019-4866-5] [PubMed] [Google Scholar]
46. Dai Y, Pang J, Gong H, Fan W, Zhang TM. Roles and tissue source of adiponectin involved in lifestyle modifications. J Gerontol A Biol Sci Med Sci 2013; 68:117-128. [View at Publisher] [DOI:10.1093/gerona/gls131] [PubMed] [Google Scholar]
47. de Carvalho FP, Moretto TL, Benfato ID, Barthichoto M, Ferreira SM, Costa-Júnior JM, et al. Central and peripheral effects of physical exercise without weight reduction in obese and lean mice. Biosci Rep. 2018 5;38(2):BSR20171033. [DOI:10.1042/BSR20171033] [PubMed] [Google Scholar]
48. Su M, Bai YP, Song WW, Wang M, Shen RR, Du KJ, et al. [Effect of exercise on adiponectin in aged obese rats]. Zhongguo Ying Yong Sheng Li Xue Za Zhi. 2018 8;34(4):345-349. Chinese. [PubMed] [Google Scholar]
49. Asilah Za'don NH, Amirul Farhana MK, Farhanim I, Sharifah Izwan TO, Appukutty M, Salim N, et al. High-intensity interval training induced PGC-1∝ and AdipoR1 gene expressions and improved insulin sensitivity in obese individuals. Med J Malaysia. 2019 ;74(6):461-467. PMID: 31929469. [PubMed] [Google Scholar]
50. Mostowik M, Gajos G, Zalewski J, Nessler J, Undas A. Omega-3 polyunsaturated fatty acids increase plasma adiponectin to leptin ratio in stable coronary artery disease. Cardiovasc Drugs Ther 2013; 27:289-295. [DOI:10.1007/s10557-013-6457-x] [PubMed] [Google Scholar]
51. Lee SH, Hong HR, Han TK, Kang HS. Aerobic training increases the expression of adiponectin receptor genes in the peripheral blood mononuclear cells of young men. Biol Sport. 2015 ;32(3):181-6. [DOI:10.5604/20831862.1150298] [PubMed] [Google Scholar]
52. Krause MP, Milne KJ, Hawke TJ. Adiponectin-Consideration for its Role in Skeletal Muscle Health. Int J Mol Sci. 2019 27;20(7):1528. [DOI:10.3390/ijms20071528] [PubMed] [Google Scholar]
53. Bauer S, Weigert J, Neumeier M, Wanninger J, Schäffler A, Luchner A, et al. Low-abundant adiponectin receptors in visceral adipose tissue of humans and rats are further reduced in diabetic animals. Arch Med Res. 2010 ;41(2):75-82. [View at Publisher] [DOI:10.1016/j.arcmed.2010.02.010] [PubMed] [Google Scholar]
54. Ye JM, Doyle PJ, Iglesias MA, Watson DG, Cooney GJ, Kraegen EW. Peroxisome proliferator-activated receptor (PPAR)-alpha activation lowers muscle lipids and improves insulin sensitivity in high fat-fed rats: comparison with PPAR-gamma activation. Diabetes. 2001 ;50(2):411-7. [View at Publisher] [DOI:10.2337/diabetes.50.2.411] [PubMed] [Google Scholar]
55. Fu Y, Luo N, Klein RL, Garvey WT. Adiponectin promotes adipocyte differentiation, insulin sensitivity,and lipid accumulation.J. Lipid Res. 2005; 46: 1369-1379 [View at Publisher] [DOI:10.1194/jlr.M400373-JLR200] [PubMed] [Google Scholar]
56. Wang C, Mao X, Wang L, Liu M, Wetzel MD, Guan KL, et al. Adiponectin sensitizes insulin signaling by reducing p70 S6 kinase-mediated serine phosphorylation of IRS-1. J Biol Chem. 2007 16;282(11):7991-6. [View at Publisher] [DOI:10.1074/jbc.M700098200] [PubMed] [Google Scholar]
57. Sunmin P, Sang MH, Ji EL, So RS. Exercise improves glucose homeostasis that has been impaired by a high-fat diet by potentiating pancreatic β-cell function and mass through IRS2 in diabetic rats. Journal of Applied Physiology November 2007; 103(5): 1764-1771. [DOI:10.1152/japplphysiol.00434.2007] [PubMed] [Google Scholar]
58. Eizadi M, Soory R, Ravasi A, Baesy K, Choobineh S. Relationship between TCF7L2 Relative Expression in Pancreas Tissue with Changes in Insulin by High Intensity Interval Training (HIIT) in Type 2 Diabetes Rats . JSSU. 2017; 24 (12): 981-993. [Google Scholar]
Send email to the article author
| Rights and permissions | |
 |
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
Enamad
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.