Journal of Isfahan Medical School

Journal of Isfahan Medical School

The Effect of High-Intensity Intermittent Training with Spirulina Powder on Changes in Gene Expression of Inflammation and Atrophy in the Soleus Muscle of Obese Elderly Diabetic Rats

Document Type : Original Article (s)

Authors
Marzieh Sadat Azarniveh 1
Roya Askari 2
Amir Hossein Haghighi 2
1 PhD Student, Department of Sports Sciences, University of Hakim Sabzevari, Sabzevar AND Instructor, Department of Sport Sciences, School of Literature and Humanities, University of Zabol, Zabol, Iran
2 Associate Professor, Department of Sports Sciences, University of Hakim Sabzevari, Sabzevar, Iran
10.22122/jims.v39i652.14485
Abstract
Background: Exercise is a suggested way to reduce inflammation and atrophy and control diabetes. Spirulina supplement also has anti-inflammatory effects. The aim of this study was to investigate the effect of eight weeks of high-intensity interval training (HIIT) with spirulina on changes in the expression of genes of inflammation and atrophy in the soleus muscle of obese elderly diabetic rats.Methods: In this experimental study, 40 old male Wistar rats (20-month-old) with an average weight of 280-325 g became obese after purchase for 8 weeks on a high-fat diet, and then became diabetic by intraperitoneal injection of streptozocin (40 mg/kg). They were divided in 5 equal groups of HIIT, HIIT + supplement, supplement, sham and control. They did 5 sessions of activities on treadmill with an intensity of 90% VO2max per week for eight weeks to perform HIIT in training groups, and used spirulina consumption (50 mg/kg body weight) as supplementation on training days. Expression of genes were measured using real-time polymerase chain reaction (RT-PCR). One-way ANOVA and Tukey post hoc test were used to analyze the data.Findings: Induction of diabetes significantly increased the expression of TWEAK, Fn14, and atrogin-1 genes in study groups compared to controls; but exercise and supplementation significantly reduced these variables more in exercise and supplementation groups compared to other groups. After training, body mass in HIIT, supplement, and HIIT + supplement groups decreased significantly compared to sham and control groups; and soleus muscle mass increased significantly only in HIIT and HIIT + supplement groups compared to control group.Conclusion: According to the results of HIIT + supplementation, it is recommended as an effective method to reduce atrophy and improve muscle health in diabetic elderly.
Keywords
High-Intensity Interval Training
Spirulina
Atrophy
Cytokine TWEAK
Atrogin-1, mouse
  1. Gil-Iturbe E, Felix-Soriano E, Sainz N, Idoate-Bayon A, Castilla-Madrigal R, Moreno-Aliaga MJ, et al. Effect of aging and obesity on GLUT12 expression in small intestine, adipose tissue, muscle, and kidney and its regulation by docosahexaenoic acid and exercise in mice. Appl Physiol Nutr Metab 2020; 45(9): 957-67.
  2. Kalyani RR, Corriere M, Ferrucci L. Age-related and disease-related muscle loss: the effect of diabetes, obesity, and other diseases. Lancet Diabetes Endocrinol 2014; 2(10): 819-29.
  3. Narain JP, Kumar R. Textbook of chronic noncommunicable diseases: the health challenge of 21st century. New Delhi, India: Jaypee Brothers Medical Publishers; 2016.
  4. Chen GQ, Mou CY, Yang YQ, Wang S, Zhao ZW. Exercise training has beneficial anti-atrophy effects by inhibiting oxidative stress-induced MuRF1 upregulation in rats with diabetes. Life Sci 2011; 89(1-2): 44-9.
  5. Perry BD, Caldow MK, Brennan-Speranza TC, Sbaraglia M, Jerums G, Garnham A, et al. Muscle atrophy in patients with Type 2 Diabetes Mellitus: roles of inflammatory pathways, physical activity and exercise. Exerc Immunol Rev 2016; 22: 94-109.
  6. Panahi S, Agha Alinejad H, Gharakhanloo R, Fayazmilani R, Hedayati M, Safarzadeh A, et al. The effect of 4 weeks resistance training on murf1 gene expression and muscle atrophy in diabetic Wistar rats. Med J Tabriz Univ Med Sci 2016; 38(2): 6-13. [In Persian].
  7. Dogra C, Changotra H, Mohan S, Kumar A. Tumor necrosis factor-like weak inducer of apoptosis inhibits skeletal myogenesis through sustained activation of nuclear factor-kappaB and degradation of MyoD protein. J Biol Chem 2006; 281(15): 10327-36.
  8. Burkly LC, Michaelson JS, Zheng TS. TWEAK/Fn14 pathway: An immunological switch for shaping tissue responses. Immunol Rev 2011; 244(1): 99-114.
  9. Peterson JM, Bakkar N, Guttridge DC. NF-kappaB signaling in skeletal muscle health and disease. Curr Top Dev Biol 2011; 96: 85-119.
  10. Teng S, Huang P. The effect of type 2 diabetes mellitus and obesity on muscle progenitor cell function. Stem Cell Res Ther 2019; 10(1): 103.
  11. Rusbana TB, Agista AZ, Saputra WD, Ohsaki Y, Watanabe K, Ardiansyah A, et al. Supplementation with fermented rice bran attenuates muscle atrophy in a diabetic rat model. Nutrients 2020; 12(8): 2409.
  12. Tchernof A, Nolan A, Sites CK, Ades PA, Poehlman ET. Weight loss reduces C-reactive protein levels in obese postmenopausal women. Circulation 2002; 105(5): 564-9.
  13. Kazemi AR, Haghpanah AR, Dakhili AB. The effect of high-intensity exercise training on gene expression of tweak and Fn14 in EDL muscle of aged and adult mice. Research in Sport Medicine and Technology 2020; 9(18): 1-11. [In Persian].
  14. Delfan M, peeri M, Ghouchi Asl S. The comparison of eight weeks of high intensity interval training vs. continuous training on the genes expression of IL-6 and CRP in adipose tissue of diabetic Rats induced by high-fat foods and fructose. Research in Medicine 2020; 44(4): 573-9. [In Persian].
  15. Mascher H, Tannerstedt J, Brink-Elfegoun T, Ekblom B, Gustafsson T, Blomstrand E. Repeated resistance exercise training induces different changes in mRNA expression of MAFbx and MuRF-1 in human skeletal muscle. Am J Physiol Endocrinol Metab 2008; 294(1): E43-E51.
  16. Apro W, Moberg M, Hamilton DL, Ekblom B, van HG, Holmberg HC, et al. Resistance exercise-induced S6K1 kinase activity is not inhibited in human skeletal muscle despite prior activation of AMPK by high-intensity interval cycling. Am J Physiol Endocrinol Metab 2015; 308(6): E470-E481.
  17. Clavel S, Coldefy AS, Kurkdjian E, Salles J, Margaritis I, Derijard B. Atrophy-related ubiquitin ligases, atrogin-1 and MuRF1 are up-regulated in aged rat Tibialis Anterior muscle. Mech Ageing Dev 2006; 127(10): 794-801.
  18. Haddad F, Adams GR. Aging-sensitive cellular and molecular mechanisms associated with skeletal muscle hypertrophy. J Appl Physiol (1985) 2006; 100(4): 1188-203.
  19. Altun M, Besche HC, Overkleeft HS, Piccirillo R, Edelmann MJ, Kessler BM, et al. Muscle wasting in aged, sarcopenic rats is associated with enhanced activity of the ubiquitin proteasome pathway. J Biol Chem 2010; 285(51): 39597-608.
  20. Raue U, Jemiolo B, Yang Y, Trappe S. TWEAK-Fn14 pathway activation after exercise in human skeletal muscle: Insights from two exercise modes and a time course investigation. J Appl Physiol (1985) 2015; 118(5): 569-78.
  21. Golestani F, Mogharnasi M, Erfani-Far M, Abtahi-Eivari SH. The effects of spirulina under high-intensity interval training on levels of nesfatin-1, omentin-1, and lipid profiles in overweight and obese females: A randomized, controlled, single-blind trial. J Res Med Sci 2021; 26: 10.
  22. Hozayen WG, Mahmoud AM, Soliman HA, Mostafa SR. Spirulina versicolor improves insulin sensitivity and attenuates hyperglycemia-mediated oxidative stress in fructose-fed rats. J Intercult Ethnopharmacol 2016; 5(1): 57-64.
  23. Akbarpour M, Samari Z. The effect of aerobic training and Spirulina supplementation on Resistin and C - reactive protein in women with type 2 diabetes with overweight. FEYZ 2020; 24(5): 576-84.
  24. Lee EH, Park JE, Choi YJ, Huh KB, Kim WY. A randomized study to establish the effects of spirulina in type 2 diabetes mellitus patients. Nutr Res Pract 2008; 2(4): 295-300.
  25. Hooshmand B, Attarzade Hosseini SR, Kordi MR, Davaloo T. The Effect of 8-week Aerobic Exercise with Spirulina Supplementation Consumption on Plasma levels of MDA, SOD and TAC in Men with Type 2 Diabetes. SPMI 2019; 10(4): 139-48. [In Persian].
  26. Asad M, Fashami M. The effect of 8 weeks ofendurance training and high intensity interval training on gene expression of MEF2A and MEF2DIN obese male Wistar rats. Sport Physiology and Management Investigations 2017; 9(2): 131-40. [In Persian].
  27. Hedayati S, Riyahi Malayeri S, Hoseini M. The effect of eight weeks of high and moderate intensity interval training along with aloe vera consumption on serum levels of chemerin, glucose and insulin in streptozotocin-induced diabetic rats: An experimental study. J Rafsanjan Univ Med Sci 2018; 17(9): 801-14. [In Persian].
  28. Hoydal MA, Wisloff U, Kemi OJ, Ellingsen O. Running speed and maximal oxygen uptake in rats and mice: practical implications for exercise training. Eur J Cardiovasc Prev Rehabil 2007; 14(6): 753-60.
  29. Gibala MJ, McGee SL. Metabolic adaptations to short-term high-intensity interval training: a little pain for a lot of gain? Exerc Sport Sci Rev 2008; 36(2): 58-63.
  30. Khoramshahi S, Kordi MR, Delfan M, Gaeini A, Safa M. Effect of five weeks of high-intensity interval training on the expression of miR-23a and atrogin-1 in gastrocnemius muscles of diabetic male rats. Iran J Endocrinol Metab 2017; 18(5): 361-7. [In Persian].
  31. Simon JP, Baskaran UL, Shallauddin KB, Ramalingam G, Evan PS. Evidence of antidiabetic activity of Spirulina fusiformis against streptozotocin-induced diabetic Wistar albino rats. 3 Biotech 2018; 8(2): 129.
  32. Tajrishi MM, Sato S, Shin J, Zheng TS, Burkly LC, Kumar A. The TWEAK-Fn14 dyad is involved in age-associated pathological changes in skeletal muscle. Biochem Biophys Res Commun 2014; 446(4): 1219-24.
  33. Mittal A, Bhatnagar S, Kumar A, Lach-Trifilieff E, Wauters S, Li H, et al. The TWEAK-Fn14 system is a critical regulator of denervation-induced skeletal muscle atrophy in mice. J Cell Biol 2010; 188(6): 833-49.
  34. Kazemi A, Dahesh T. The effect of 4 weeks of high intensity training on gene expression of MST1 and MAFbx in EDL muscle of aged mice. SPMI 2019; 11(3): 47-58. [In Persian].
  35. Hudson MB, Woodworth-Hobbs ME, Zheng B, Rahnert JA, Blount MA, Gooch JL, et al. miR-23a is decreased during muscle atrophy by a mechanism that includes calcineurin signaling and exosome-mediated export. Am J Physiol Cell Physiol 2014; 306(6): C551-C558.
  36. Wada S, Kato Y, Okutsu M, Miyaki S, Suzuki K, Asahara H, Et Al. Mir-23a attenuates skeletal muscle atrophy by targeting Mafbx/ATROGIN-1 AND Murf1. Journal of Physiological Sciences 2009; 59(Suppl 1): 216.
  37. Jackson MJ, McArdle A. Age-related changes in skeletal muscle reactive oxygen species generation and adaptive responses to reactive oxygen species. J Physiol 2011; 589(Pt 9): 2139-45.
  38. Wei B, Dui W, Liu D, Xing Y, Yuan Z, Ji G. MST1, a key player, in enhancing fast skeletal muscle atrophy. BMC Biol 2013; 11: 12.
  39. Ribeiro MBT, Guzzoni V, Hord JM, Lopes GN, Marqueti RC, de Andrade RV, et al. Resistance training regulates gene expression of molecules associated with intramyocellular lipids, glucose signaling and fiber size in old rats. Sci Rep 2017; 7(1): 8593.
  40. Sheibani S, Daryanoosh F, Tanideh N, Rahimi M, Jamhiri I, Refahiat MA. Effect of high intensity interval training and detraining on gene expression of AKT/FoxO3a in cardiac and soleus muscle of male rats. Ebnesina 2020; 22(2): 15-23. [In Persian].
  41. Holloway TM, Bloemberg D, da Silva ML, Simpson JA, Quadrilatero J, Spriet LL. High intensity interval and endurance training have opposing effects on markers of heart failure and cardiac remodeling in hypertensive rats. PLoS One 2015; 10(3): e0121138.
  42. Ahmadi F, Ghanbar Zadeh M, Habibi AH, Karimi F. Effect of resistance training with Spirulina platensis on PI3K/Akt/mTOR/p70S6k signaling pathway in cardiac muscle. Sci Sports 2020; 35(2): 91-8.
  43. Karimi M, Eizadi M. The effect of interval training on FOXO1 expression in pancreas tissue of diabetes rats with high fat diet and STZ. Razi J Med Sci 2019; 26(6): 95-104. [In Persian].
  44. Mirghani SJ, Azarbayjani MA, Peeri M. Effects of endurance training and isocaloric high intensity interval training on anthropometric indices and insulin resistance in high fat diet-fed Wistar rats. Med Lab J 2018; 12(6): 12-8. [In Persian].
  45. Shen Y, Xu X, Yue K, Xu G. Effect of different exercise protocols on metabolic profiles and fatty acid metabolism in skeletal muscle in high-fat diet-fed rats. Obesity (Silver Spring) 2015; 23(5): 1000-6.
Journal of Isfahan Medical School
Volume 39, Issue 652 - Serial Number 652
November and December 2022
Pages 922-933

  • Receive Date 25 August 2021
  • Accept Date 06 April 2022