Document Type : Research Paper I Open Access I Released under CC BY-NC 4.0 license

Authors

1 Department of Sports Physiology, Faculty of Sport Sciences and Health, University of Tehran, Tehran, Iran.

2 Corresponding Author, Sport Sciences Research Institute, Tehran, Iran.

3 Assistant Professor and Faculty Member, Sharif University of Technology , Tehran, Iran

4 Department of Sports Physiology, Payame Noor University, Karaj, Alborz, Iran.

Abstract

Introduction: One of the most important influential factors in the process of human physiological adaptations is angiogenesis; which helps to repair and grow body tissues by continuously creating blood vessels through angiopoietin activity. In the present study, we investigated the effect of three methods of moderate-intensity continuous, high-intensity continuous, and high-intensity intermittent training on the angiopoietin-1 and angiopoietin-2 genes expression in the subcutaneous fat tissue of male Wistar rats.
Methods: For this purpose, 32 male Wistar rats with an average weight of 236.3±34.5 grams and age of 8 weeks were randomly divided into four groups of intense intermittent running aerobic training (including four intense intervals with an intensity of 90% to 100% of VO2max and four low-intensity intervals at 50% to 60% of VO2max in a total time of 38 minutes), moderate-intensity continuous running aerobic training (including running at 65% of VO2max in a total time of 47 minutes), high intensity continuous running aerobic training (including running at 65% of VO2max in a total time of 40 minutes with an incremental incline of the treadmill with a 2% of incline every two weeks), and Control. Twenty-four hours after the last training session, after complete anesthesia, subcutaneous fat tissue samplings of the abdomen were done. The gene expression levels of angiopoietin-1 and angiopoietin-2 in subcutaneous fat tissue were measured by the RT-PCR method. Due to the non-normal distribution of data in some groups, Kruskal-Wallis statistical method was used.
Results: The results showed that the angiopoietin-1 gene expression increased in all three training groups compared with the control group, which was significant in the moderate-intensity continuous group. Also, the angiopoietin-2 expression increased in all three groups compared with the control group, which was significant in the high-intensity continuous group.
 Conclusion: In general, continuous training seems to have a positive effect on the increase of angiopoietin-1 and -2 expression in subcutaneous fat tissue.

Keywords

Main Subjects

  1. Khurana R, Simons M. Insights from angiogenesis trials using fibroblast growth factor for advanced arteriosclerotic disease. Trends in cardiovascular medicine. 2003 Apr 1; 13(3):116-22.

     

    2.Herbert P, Hayes LD, Sculthorpe NF, Grace FM. HIIT produces increases in muscle power and free testosterone in male masters' athletes. Endocrine connections. 2017 Oct 1;6(7):430-6.

    3.Hatano D, Ogasawara J, Endoh S, Sakurai T, Nomura S, Kizaki T, Ohno H, Komabayashi T, Izawa T. Effect of exercise training on the density of endothelial cells in the white adipose tissue of rats. Scandinavian journal of medicine & science in sports. 2011 Dec;21(6):e115-21.

    4.Bachmanov AA, Reed DR, Tordoff MG, Price RA, Beauchamp GK. Nutrient preference and diet-induced adiposity in C57BL/6ByJ and 129P3/J mice. Physiology & behavior. 2001 Mar 1;72(4):603-13.

    5.Kern PA, Ranganathan S, Li C, Wood L, Ranganathan G. Adipose tissue tumor necrosis factor and interleukin-6 expression in human obesity and insulin resistance. American journal of physiology-endocrinology and metabolism. 2001 May 1.

    1. Mokdad AH, Ford ES, Bowman BA, Dietz WH, Vinicor F, Bales VS, Marks JS. Prevalence of obesity, diabetes, and obesity-related health risk factors, 2001. Jama. 2003 Jan 1;289(1):76-9.

    7.Maresky HS, Sharfman Z, Ziv-Baran T, Gomori JM, Copel L, Tal S. Anthropometric assessment of neck adipose tissue and airway volume using multidetector computed tomography: an imaging approach and association with overall mortality. Medicine. 2015 Nov;94(45).

    8.Brown JC, Harhay MO, Harhay MN. Anthropometrically predicted visceral adipose tissue and blood-based biomarkers: a cross-sectional analysis. European journal of nutrition. 2018 Feb;57(1):191-8.

    9.Valenzuela DM, Griffiths JA, Rojas J, Aldrich TH, Jones PF, Zhou H, McClain J, Copeland NG, Gilbert DJ, Jenkins NA, Huang T. Angiopoietins 3 and 4: diverging gene counterparts in mice and humans. Proceedings of the National Academy of Sciences. 1999 Mar 2;96(5):1904-9.

    1. Lee HJ. Exercise training regulates angiogenic gene expression in white adipose tissue. Journal of exercise rehabilitation. 2018 Feb;14(1):16.

    11.Nowak-Sliwinska P, Alitalo K, Allen E, Anisimov A, Aplin AC, Auerbach R, Augustin HG, Bates DO, van Beijnum JR, Bender RH, Bergers G. Consensus guidelines for the use and interpretation of angiogenesis assays. Angiogenesis. 2018 Aug;21(3):425-532.

    12.Ferrara N, Henzel WJ. Pituitary follicular cells secrete a novel heparin-binding growth factor specific for vascular endothelial cells. Biochemical and biophysical research communications. 1989 Jun 15;161(2):851-8.

    13.Dallabrida SM, Zurakowski D, Shih SC, Smith LE, Folkman J, Moulton KS, Rupnick MA. Adipose tissue growth and regression are regulated by angiopoietin-1. Biochemical and biophysical research communications. 2003 Nov 21;311(3):563-71.

    14.Disanzo BL, You T. Effects of exercise training on indicators of adipose tissue angiogenesis and hypoxia in obese rats. Metabolism. 2014 Apr 1;63(4):452-5.

    15.Cullberg KB, Christiansen T, Paulsen SK, Bruun JM, Pedersen SB, Richelsen B. Effect of weight loss and exercise on angiogenic factors in the circulation and in adipose tissue in obese subjects. Obesity. 2013 Mar;21(3):454-60.

    16.Høydal MA, Wisløff U, Kemi OJ, Ellingsen Ø. Running speed and maximal oxygen uptake in rats and mice: practical implications for exercise training. European Journal of Preventive Cardiology. 2007 Dec 1;14(6):753-60.

    17.Gavin TP, Stallings III HW, Zwetsloot KA, Westerkamp LM, Ryan NA, Moore RA, Pofahl WE, Hickner RC. Lower capillary density but no difference in VEGF expression in obese vs. lean young skeletal muscle in humans. Journal of applied physiology. 2005 Jan;98(1):315-21.

    18.Pasarica M, Sereda OR, Redman LM, Albarado DC, Hymel DT, Roan LE, Rood JC, Burk DH, Smith SR. Reduced adipose tissue oxygenation in human obesity: evidence for rarefaction, macrophage chemotaxis, and inflammation without an angiogenic response. Diabetes. 2009 Mar 1;58(3):718-25.

    19.Gómez-Ambrosi J, Catalán V, Rodríguez A, Ramírez B, Silva C, Gil MJ, Salvador J, Frühbeck G. Involvement of serum vascular endothelial growth factor family members in the development of obesity in mice and humans. The Journal of nutritional biochemistry. 2010 Aug 1;21(8):774-80.

    20.Jung YJ, Park W, Nguyen-Thanh T, Kang KP, Jin HY, Kim SH, Suh W, Kim W. COMP-angiopoietin-1 mitigates changes in lipid droplet size, macrophage infiltration of adipose tissue and renal inflammation in streptozotocin-induced diabetic mice. Oncotarget. 2017 Nov 7;8(55):94805.

    1. Soori R, Khosravi N, Mirshafiey SA, Gholijani F, Rezaeian N. Effects of Resistance Training on Angiopoietin-Like Protein 4 and Lipids Profile Levels in Postmenopausal Obese Women. Sport Physiology. 2018 Jan 21;9(36):39-58. (in Persian)
    2. Abbassi Daloii A, Abdi A, Abbaszadeh Sourati H, Sourati M. Angiogenic Mediators plasma response to aerobic exercise with Crataegus elbursensis extract in male’s rat. Journal of Medicinal Plants. 2016 Oct 10;15(60):76-84. (in Persian)
    3. Kolahdouzi, S., Talebi Garakani, E., Hamidian, G., & Safarzade, A. (2018). The Effects of High-Intensity Intermittent Aerobic Training on Adipose Tissue Angiogenesis in Rats Fed a High Fat Diet. Sport Physiology, 10(38), 143-162. (in Persian)

    24.Karbalaeifar S, Gaeini AA, Kordi MR, Nuri R, Ghorbani P. Effect of 6 weeks high intensity interval training on selected factors of cardiac angiogenesis in rats with myocardial infarction. Sport Physiology. 2019 Jul 23;11(42):17-30. (in Persian)

    25.Davis S, Aldrich TH, Jones PF, Acheson A, Compton DL, Jain V, Ryan TE, Bruno J, Radziejewski C, Maisonpierre PC, Yancopoulos GD. Isolation of angiopoietin-1, a ligand for the TIE2 receptor, by secretion-trap expression cloning. Cell. 1996 Dec 27;87(7):1161-9.

    26.Scharpfenecker M, Fiedler U, Reiss Y, Augustin HG. The Tie-2 ligand angiopoietin-2 destabilizes quiescent endothelium through an internal autocrine loop mechanism. Journal of cell science. 2005 Feb 15;118(4):771-80.

    1. Saharinen P, Kerkelä K, Ekman N, Marron M, Brindle N, Lee GM, Augustin H, Koh GY, Alitalo K. Multiple angiopoietin recombinant proteins activate the Tie1 receptor tyrosine kinase and promote its interaction with Tie2. The Journal of cell biology. 2005 Apr 25;169(2):239-43.

    28.Mason SD, Rundqvist H, Papandreou I, Duh R, McNulty WJ, Howlett RA, Olfert IM, Sundberg CJ, Denko NC, Poellinger L, Johnson RS. HIF-1α in endurance training: suppression of oxidative metabolism. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology. 2007 Nov;293(5): R2059-69.

    29.Ameln H, Gustafsson T, Sundberg CJ, Okamoto K, Jansson E, Poellinger L, Makino Y. Physiological activation of hypoxia inducible factor‐1 in human skeletal muscle. The FASEB journal. 2005 Jun;19(8):1009-11.

    1. Arany Z, Foo SY, Ma Y, Ruas JL, Bommi-Reddy A, Girnun G, Cooper M, Laznik D, Chinsomboon J, Rangwala SM, Baek KH. HIF-independent regulation of VEGF and angiogenesis by the transcriptional coactivator PGC-1α. Nature. 2008 Feb;451(7181):1008-12.

    31.Leick L, Hellsten Y, Fentz J, Lyngby SS, Wojtaszewski JF, Hidalgo J, Pilegaard H. PGC-1α mediates exercise-induced skeletal muscle VEGF expression in mice. American Journal of Physiology-Endocrinology and Metabolism. 2009 Jul 1.

    1. Geng T, Li P, Okutsu M, Yin X, Kwek J, Zhang M, Yan Z. PGC-1α plays a functional role in exercise-induced mitochondrial biogenesis and angiogenesis but not fiber-type transformation in mouse skeletal muscle. American Journal of Physiology-Cell Physiology. 2010 Mar;298(3):C572-9.

    33.Wright DC, Geiger PC, Han DH, Jones TE, Holloszy JO. Calcium induces increases in peroxisome proliferator-activated receptor γ coactivator-1α and mitochondrial biogenesis by a pathway leading to p38 mitogen-activated protein kinase activation. Journal of Biological Chemistry. 2007 Jun 29;282(26):18793-9.

    34.Jäger, S., Handschin, C., St.-Pierre, J., & Spiegelman, B. M. (2007). AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1α. Proceedings of the National Academy of Sciences, 104(29), 12017-12022.

    35.Ouchi N, Shibata R, Walsh K. AMP-activated protein kinase signaling stimulates VEGF expression and angiogenesis in skeletal muscle. Circulation research. 2005 Apr 29;96(8):838-46.

    36.Chinsomboon J, Ruas J, Gupta RK, Thom R, Shoag J, Rowe GC, Sawada N, Raghuram S, Arany Z. The transcriptional coactivator PGC-1α mediates exercise-induced angiogenesis in skeletal muscle. Proceedings of the national academy of sciences. 2009 Dec 15;106(50):21401-6.

    37.Hausman GJ, Richardson RL. Adipose tissue angiogenesis. Journal of animal science. 2004 Mar 1; 82(3):925-34.