High-intensity interval training, but not Spirulina supplementation, changes muscle regeneration signaling proteins in aged rats with obesity and diabetes

Submitted: 30 June 2024
Accepted: 5 August 2024
Published: 9 October 2024
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PDF: 100
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This study aimed to investigate changes in protein signaling associated with muscle regeneration in aged rats with obesity and diabetes following high-intensity interval training (HIIT) and SP supplementation. Forty male Wistar rats weighting 280-325 g were used in this study. Obesity was induced by eight weeks of a high-fat diet, and diabetes was induced by intraperitoneal injection of 40 mg/kg streptozocin. Rats were randomly divided into control (CON), sham, SP, HIIT, and HIIT+SP groups. HIIT was performed five times per week during the 8-week period. SP dose was 50 mg/kg. Real-time PCR was used to evaluate the expression of myogenin, MyoD1, and Pax7. The decreases in body mass in the HIIT, HIIT+SP and SP groups were significantly higher than those in the sham and CON groups (p=0.0001). The soleus muscle mass increased significantly only in the HIIT and HIIT+SP groups (p<0.01). HIIT+SP improved fasting blood glucose and insulin levels more than HIIT alone and SP (p<0.05), while HIIT increased the expression levels of myogenic factors more than other groups (p=0.0001). In conclusion HIIT alone had a significant impact on myogenic factors, whereas Spirulina had an effect only when combined with HIIT.

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Izquierdo M, Merchant RA, Morley JE, Anker SD, Aprahamian I, Arai H, Aubertin-Leheudre M, Bernabei R, Cadore EL, Cesari M, Chen LK, de Souto Barreto P, Duque G, Ferrucci L, Fielding RA, García-Hermoso A, Gutiérrez-Robledo LM, Harridge SDR, Kirk B, Kritchevsky S, Landi F, Lazarus N, Martin FC, Marzetti E, Pahor M, Ramírez-Vélez R, Rodriguez-Mañas L, Rolland Y, Ruiz JG, Theou O, Villareal DT, Waters DL, Won Won C, Woo J, Vellas B, Fiatarone Singh M. International Exercise Recommendations in Older Adults (ICFSR): Expert Consensus Guidelines. J Nutr Health Aging. 2021;25(7):824-853. doi: 10.1007/s12603-021-1665-8. PMID: 34409961. DOI: https://doi.org/10.1007/s12603-021-1665-8
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 Oct;2(10):819-29. doi: 10.1016/S2213-8587(14)70034-8. Epub 2014 Mar 6. PMID: 24731660; PMCID: PMC4156923. DOI: https://doi.org/10.1016/S2213-8587(14)70034-8
Perry BD, Caldow MK, Brennan-Speranza TC, Sbaraglia M, Jerums G, Garnham A, Wong C, Levinger P, Asrar Ul Haq M, Hare DL, Price SR, Levinger I. Muscle atrophy in patients with Type 2 Diabetes Mellitus: roles of inflammatory pathways, physical activity and exercise. Exerc Immunol Rev. 2016;22:94-109. PMID: 26859514; PMCID: PMC5545118.
Snijders T, Nederveen JP, Bell KE, Lau SW, Mazara N, Kumbhare DA, Phillips SM, Parise G. Prolonged exercise training improves the acute type II muscle fibre satellite cell response in healthy older men. J Physiol. 2019 Jan;597(1):105-119. doi: 10.1113/JP276260. Epub 2018 Nov 24. PMID: 30370532; PMCID: PMC6312443. DOI: https://doi.org/10.1113/JP276260
Hernández-Hernández JM, García-González EG, Brun CE, Rudnicki MA. The myogenic regulatory factors, determinants of muscle development, cell identity and regeneration. Semin Cell Dev Biol. 2017 Dec;72:10-18. doi: 10.1016/j.semcdb.2017.11.010. Epub 2017 Nov 15. PMID: 29127045; PMCID: PMC5723221. DOI: https://doi.org/10.1016/j.semcdb.2017.11.010
Stokes T, Hector AJ, Morton RW, McGlory C, Phillips SM. Recent Perspectives Regarding the Role of Dietary Protein for the Promotion of Muscle Hypertrophy with Resistance Exercise Training. Nutrients. 2018 Feb 7;10(2):180. doi: 10.3390/nu10020180. PMID: 29414855; PMCID: PMC5852756. DOI: https://doi.org/10.3390/nu10020180
Arrieta-Leandro MC, Moncada-Jiménez J, Morales-Scholz MG, Hernández-Elizondo J. The effect of chronic high-intensity interval training programs on glycaemic control, aerobic resistance, and body composition in type 2 diabetic patients: a meta-analysis. J Endocrinol Invest. 2023 Dec;46(12):2423-2443. doi: 10.1007/s40618-023-02144-x. Epub 2023 Jul 15. PMID: 37454031. DOI: https://doi.org/10.1007/s40618-023-02144-x
Badri Z, Delfan M, Danesh-yar S. The Combined Effect of High-Intensity Interval Training and Metformin on Gene Expression of Myogenin and Myostatin in Skeletal Muscle of Type 2 Diabetic Mice. ijdld. 2022; 22 (4) :199-212. https://ijdld.tums.ac.ir/article-1-6173-en.html
Nederveen JP, Joanisse S, Séguin CM, Bell KE, Baker SK, Phillips SM, Parise G. The effect of exercise mode on the acute response of satellite cells in old men. Acta Physiol (Oxf). 2015 Dec;215(4):177-90. doi: 10.1111/apha.12601. Epub 2015 Oct 14. PMID: 26367861. DOI: https://doi.org/10.1111/apha.12601
Hernández-Lepe MA, Manríquez-Torres JJ, Ramos-Lopez O, Serrano-Medina A, Ortiz-Ortiz M, Aburto-Corona JA, Pozos-Parra MDP, Villalobos-Gallegos LE, Rodríguez-Uribe G, Gómez-Miranda LM. Impact of Spirulina maxima Intake and Exercise (SIE) on Metabolic and Fitness Parameters in Sedentary Older Adults with Excessive Body Mass: Study Protocol of a Randomized Controlled Trial. Int J Environ Res Public Health. 2021 Feb 8;18(4):1605. doi: 10.3390/ijerph18041605. PMID: 33567780; PMCID: PMC7914563. DOI: https://doi.org/10.3390/ijerph18041605
Gómez-Téllez A, Sierra-Puente D, Muñoz-Gómez R, Ibarra-Pitts A, Guevara-Cruz M, Hernández-Ortega M, Gutiérrez-Salmeán G. Effects of a Low-Dose Spirulina/Turmeric Supplement on Cardiometabolic and Antioxidant Serum Markers of Patients With Abdominal Obesity. Front Nutr. 2020 May 19;7:65. doi: 10.3389/fnut.2020.00065. PMID: 32509796; PMCID: PMC7248216. DOI: https://doi.org/10.3389/fnut.2020.00065
Hatami E, Ghalishourani SS, Najafgholizadeh A, Pourmasoumi M, Hadi A, Clark CCT, Assaroudi M, Salehi-Sahlabadi A, Joukar F, Mansour-Ghanaei F. The effect of spirulina on type 2 diabetes: a systematic review and meta-analysis. J Diabetes Metab Disord. 2021 Mar 2;20(1):883-892. doi: 10.1007/s40200-021-00760-z. PMID: 34178867; PMCID: PMC8212345. DOI: https://doi.org/10.1007/s40200-021-00760-z
Brito AF, Silva AS, de Oliveira CVC, de Souza AA, Ferreira PB, de Souza ILL, da Cunha Araujo LC, da Silva Félix G, de Souza Sampaio R, Tavares RL, de Andrade Pereira R, Neto MM, da Silva BA. Spirulina platensis prevents oxidative stress and inflammation promoted by strength training in rats: dose-response relation study. Sci Rep. 2020 Apr 14;10(1):6382. doi: 10.1038/s41598-020-63272-5. PMID: 32286405; PMCID: PMC7156748. DOI: https://doi.org/10.1038/s41598-020-63272-5
Lu HK, Hsieh CC, Hsu JJ, Yang YK, Chou HN. Preventive effects of Spirulina platensis on skeletal muscle damage under exercise-induced oxidative stress. Eur J Appl Physiol. 2006 Sep;98(2):220-6. doi: 10.1007/s00421-006-0263-0. Epub 2006 Aug 30. PMID: 16944194. DOI: https://doi.org/10.1007/s00421-006-0263-0
Calella P, Cerullo G, Di Dio M, Liguori F, Di Onofrio V, Gallè F, Liguori G. Antioxidant, anti-inflammatory and immunomodulatory effects of spirulina in exercise and sport: A systematic review. Front Nutr. 2022 Dec 14;9:1048258. doi: 10.3389/fnut.2022.1048258. PMID: 36590230; PMCID: PMC9795056. DOI: https://doi.org/10.3389/fnut.2022.1048258
Chaouachi M, Vincent S, Groussard C. A Review of the Health-Promoting Properties of Spirulina with a Focus on athletes' Performance and Recovery. J Diet Suppl. 2024;21(2):210-241. doi: 10.1080/19390211.2023.2208663. Epub 2023 May 4. PMID: 37143238. DOI: https://doi.org/10.1080/19390211.2023.2208663
Hernández-Lepe MA, López-Díaz JA, Juárez-Oropeza MA, Hernández-Torres RP, Wall-Medrano A, Ramos-Jiménez A. Effect of Arthrospira (Spirulina) maxima Supplementation and a Systematic Physical Exercise Program on the Body Composition and Cardiorespiratory Fitness of Overweight or Obese Subjects: A Double-Blind, Randomized, and Crossover Controlled Trial. Mar Drugs. 2018 Oct 1;16(10):364. doi: 10.3390/md16100364. PMID: 30275428; PMCID: PMC6213464. DOI: https://doi.org/10.3390/md16100364
Moura LP, Gurjão AL, Jambassi Filho JC, Mizuno J, Suemi C, Mello MA. Spirulina, exercício e controle da glicemia em ratos diabéticos [Spirulina, exercise and serum glucose control in diabetic rats]. Arq Bras Endocrinol Metabol. 2012 Feb;56(1):25-32. Portuguese. doi: 10.1590/s0004-27302012000100005. PMID: 22460192. DOI: https://doi.org/10.1590/S0004-27302012000100005
Jalali S, Jafari M. Effects of High Intensity Interval (HIT) versus continuous trainings on ABCG5 and ABCG8 genes expression in male wistar rats after high fat diet. Research on Medicine. 2019; 43: 216–21. http://pejouhesh.sbmu.ac.ir/article-1-1946-en.html
Bedford TG, Tipton CM, Wilson NC, Oppliger RA, Gisolfi CV. Maximum oxygen consumption of rats and its changes with various experimental procedures. J Appl Physiol Respir Environ Exerc Physiol. 1979 Dec;47(6):1278-83. doi: 10.1152/jappl.1979.47.6.1278. PMID: 536299. DOI: https://doi.org/10.1152/jappl.1979.47.6.1278
Høydal MA, Wisløff 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 Dec;14(6):753-60. doi: 10.1097/HJR.0b013e3281eacef1. PMID: 18043295. DOI: https://doi.org/10.1097/HJR.0b013e3281eacef1
Toti L, Bartalucci A, Ferrucci M, Fulceri F, Lazzeri G, Lenzi P, Soldani P, Gobbi P, La Torre A, Gesi M. High-intensity exercise training induces morphological and biochemical changes in skeletal muscles. Biol Sport. 2013 Dec;30(4):301-9. doi: 10.5604/20831862.1077557. Epub 2013 Nov 25. PMID: 24744502; PMCID: PMC3944543. DOI: https://doi.org/10.5604/20831862.1077557
Simon JP, Baskaran UL, Shallauddin KB, Ramalingam G, Evan Prince S. Evidence of antidiabetic activity of Spirulina fusiformis against streptozotocin-induced diabetic Wistar albino rats. 3 Biotech. 2018 Feb;8(2):129. doi: 10.1007/s13205-018-1156-8. Epub 2018 Feb 13. PMID: 29450119; PMCID: PMC5811412. DOI: https://doi.org/10.1007/s13205-018-1156-8
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 May;23(5):1000-6. doi: 10.1002/oby.21056. Epub 2015 Apr 10. PMID: 25864958. DOI: https://doi.org/10.1002/oby.21056
Naves JPA, Rebelo ACS, Silva LRBE, Silva MS, Ramirez-Campillo R, Ramírez-Vélez R, Gentil P. Cardiorespiratory and perceptual responses of two interval training and a continuous training protocol in healthy young men. Eur J Sport Sci. 2019 Jun;19(5):653-660. doi: 10.1080/17461391.2018.1548650. Epub 2018 Nov 29. PMID: 30496024. DOI: https://doi.org/10.1080/17461391.2018.1548650
Ozaki H, Loenneke JP, Thiebaud RS, Abe T. Cycle training induces muscle hypertrophy and strength gain: strategies and mechanisms. Acta Physiol Hung. 2015 Mar;102(1):1-22. doi: 10.1556/APhysiol.102.2015.1.1. PMID: 25804386. DOI: https://doi.org/10.1556/APhysiol.102.2015.1.1
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 Winter;2(4):295-300. doi: 10.4162/nrp.2008.2.4.295. Epub 2008 Dec 31. PMID: 20016733; PMCID: PMC2788188. DOI: https://doi.org/10.4162/nrp.2008.2.4.295
Ghadery B, Ghazalian F, Hosseini SA, Abed-Natanzy H, Shamsoddini A. Effect of High-Intensity Interval Training with Eryngium Campestre on Lipid Profile and Glycemic Indices in High-Fat Diet-Induced Obese Rats. Hormozgan Medical Journal. 2020;24(2): e98982. doi: 10.5812/hmj.98982. DOI: https://doi.org/10.5812/hmj.98982
Goodwin ML. Blood glucose regulation during prolonged, submaximal, continuous exercise: a guide for clinicians. J Diabetes Sci Technol. 2010 May 1;4(3):694-705. doi: 10.1177/193229681000400325. PMID: 20513337; PMCID: PMC2901048. DOI: https://doi.org/10.1177/193229681000400325
Ambrosi MA, Reinehr CO, Bertolin TE, Costa JAV, Colla LM. Propriedades de saúde de Spirulina spp. Rev. Ciênc. Farm. Básica Apl. 2008; 29(2): 109-117. http://rcfba.fcfar.unesp.br/index.php/ojs/article/view/477.
Karkos PD, Leong SC, Karkos CD, Sivaji N, Assimakopoulos DA. Spirulina in clinical practice: evidence-based human applications. Evid Based Complement Alternat Med. 2011;2011:531053. doi: 10.1093/ecam/nen058. Epub 2010 Oct 19. PMID: 18955364; PMCID: PMC3136577. DOI: https://doi.org/10.1093/ecam/nen058
Azhir S, Alijani E, Martínez-Huenchullán SF, Amni H, Baker JS, Farhani F. Effects of exercise intensity on soleus muscle myostatin and follistatin levels ofhyperglycaemic rats. Retos: nuevas tendencias en educación física, deporte y recreación. 2022; 889–896. doi: 10.47197/retos.v44i0.91770. DOI: https://doi.org/10.47197/retos.v44i0.91770
Mathers JL, Farnfield MM, Garnham AP, Caldow MK, Cameron-Smith D, Peake JM. Early inflammatory and myogenic responses to resistance exercise in the elderly. Muscle Nerve. 2012 Sep;46(3):407-12. doi: 10.1002/mus.23317. PMID: 22907232. DOI: https://doi.org/10.1002/mus.23317
Drummond MJ, Bell JA, Fujita S, Dreyer HC, Glynn EL, Volpi E, Rasmussen BB. Amino acids are necessary for the insulin-induced activation of mTOR/S6K1 signaling and protein synthesis in healthy and insulin resistant human skeletal muscle. Clin Nutr. 2008 Jun;27(3):447-56. doi: 10.1016/j.clnu.2008.01.012. Epub 2008 Mar 14. PMID: 18342407; PMCID: PMC2484120. DOI: https://doi.org/10.1016/j.clnu.2008.01.012
Hyatt JP, McCall GE, Kander EM, Zhong H, Roy RR, Huey KA. PAX3/7 expression coincides with MyoD during chronic skeletal muscle overload. Muscle Nerve. 2008 Jul;38(1):861-6. doi: 10.1002/mus.21006. PMID: 18508329; PMCID: PMC2804252. DOI: https://doi.org/10.1002/mus.21006
Raue U, Slivka D, Jemiolo B, Hollon C, Trappe S. Myogenic gene expression at rest and after a bout of resistance exercise in young (18-30 yr) and old (80-89 yr) women. J Appl Physiol (1985). 2006 Jul;101(1):53-9. doi: 10.1152/japplphysiol.01616.2005. Epub 2006 Apr 6. PMID: 16601301. DOI: https://doi.org/10.1152/japplphysiol.01616.2005
Biglari S, Gaeini A A, Kordi M R, Ghardashi-Afousi A. The Effect of 8 Weeks High-intensity Interval Training on Myostatin and Follistatin Gene Expression in Gastrocnemius Muscle of the Rats. J Arak Uni Med Sci. 2018; 21 (1) :1-10.
Zhao Y, Chen M, Lian D, Li Y, Li Y, Wang J, Deng S, Yu K, Lian Z. Non-Coding RNA Regulates the Myogenesis of Skeletal Muscle Satellite Cells, Injury Repair and Diseases. Cells. 2019 Aug 27;8(9):988. doi: 10.3390/cells8090988. PMID: 31461973; PMCID: PMC6769629. DOI: https://doi.org/10.3390/cells8090988
Gundersen K. Excitation-transcription coupling in skeletal muscle: the molecular pathways of exercise. Biol Rev Camb Philos Soc. 2011 Aug;86(3):564-600. doi: 10.1111/j.1469-185X.2010.00161.x. Epub 2010 Oct 6. PMID: 21040371; PMCID: PMC3170710. DOI: https://doi.org/10.1111/j.1469-185X.2010.00161.x
Krook A, Roth RA, Jiang XJ, Zierath JR, Wallberg-Henriksson H. Insulin-stimulated Akt kinase activity is reduced in skeletal muscle from NIDDM subjects. Diabetes. 1998 Aug;47(8):1281-6. doi: 10.2337/diab.47.8.1281. PMID: 9703329. DOI: https://doi.org/10.2337/diabetes.47.8.1281
Callahan MJ, Parr EB, Hawley JA, Camera DM. Can High-Intensity Interval Training Promote Skeletal Muscle Anabolism? Sports Med. 2021 Mar;51(3):405-421. doi: 10.1007/s40279-020-01397-3. PMID: 33512698. DOI: https://doi.org/10.1007/s40279-020-01397-3
Mao Z, Zhang W. Role of mTOR in Glucose and Lipid Metabolism. Int J Mol Sci. 2018 Jul 13;19(7):2043. doi: 10.3390/ijms19072043. PMID: 30011848; PMCID: PMC6073766. DOI: https://doi.org/10.3390/ijms19072043
Morgan A, Noguchi KS, Tang A, Heisz J, Thabane L, Richardson J. Physical and Cognitive Effects of High-Intensity Interval or Circuit-Based Strength Training for Community-Dwelling Older Adults: A Systematic Review. J Aging Phys Act. 2023 Aug 31;31(6):1051-1074. doi: 10.1123/japa.2022-0425. PMID: 37652435. DOI: https://doi.org/10.1123/japa.2022-0425
Coswig VS, Barbalho M, Raiol R, Del Vecchio FB, Ramirez-Campillo R, Gentil P. Effects of high vs moderate-intensity intermittent training on functionality, resting heart rate and blood pressure of elderly women. J Transl Med. 2020 Feb 17;18(1):88. doi: 10.1186/s12967-020-02261-8. PMID: 32066460; PMCID: PMC7027031. DOI: https://doi.org/10.1186/s12967-020-02261-8
Gentil P, Silva LRBE, Antunes DE, Carneiro LB, de Lira CAB, Batista G, de Oliveira JCM, Cardoso JS, Souza DC, Rebelo ACS. The effects of three different low-volume aerobic training protocols on cardiometabolic parameters of type 2 diabetes patients: A randomized clinical trial. Front Endocrinol (Lausanne). 2023 Jan 23;14:985404. doi: 10.3389/fendo.2023.985404. PMID: 36755928; PMCID: PMC9900112. DOI: https://doi.org/10.3389/fendo.2023.985404
Portela PFM, Neto VGC, Monteiro ER, Santos da Silva R, da Silva VF, Nogueira CJ, Schutz S, Scudese E, Salvino AKS, Valentim-Silva JR. HIIT is most effective than mict on glycemic control of older people with glucose metabolism impairments: A systematic review and metanalysis. Prim Care Diabetes. 2023 Apr;17(2):129-136. doi: 10.1016/j.pcd.2023.01.009. Epub 2023 Feb 3. PMID: 36740492. DOI: https://doi.org/10.1016/j.pcd.2023.01.009
Lynch GS, Cuffe SA, Plant DR, Gregorevic P. IGF-I treatment improves the functional properties of fast- and slow-twitch skeletal muscles from dystrophic mice. Neuromuscul Disord. 2001 Apr;11(3):260-8. doi: 10.1016/s0960-8966(00)00192-9. PMID: 11297941. DOI: https://doi.org/10.1016/S0960-8966(00)00192-9
Meznaric M, Eržen I, Karen P, Cvetko E. Effect of ageing on the myosin heavy chain composition of the human sternocleidomastoid muscle. Ann Anat. 2018 Mar;216:95-99. doi: 10.1016/j.aanat.2017.12.001. Epub 2017 Dec 28. PMID: 29289708. DOI: https://doi.org/10.1016/j.aanat.2017.12.001

How to Cite

Askari, R., Azarniveh, M. S., Haghighi , A. H., Shahrabadi , H., & Gentil, P. (2024). High-intensity interval training, but not Spirulina supplementation, changes muscle regeneration signaling proteins in aged rats with obesity and diabetes. European Journal of Translational Myology. https://doi.org/10.4081/ejtm.2024.12761