Document Type : Review Article
Authors
1 M.Sc. Student of Exercise Physiology, Faculty of Physical Education and Sport Sciences, Allameh Tabataba’i University, Tehran, Iran.
2 Interventional Cardiologist, Associate Professor of Kermanshah University of Medical Sciences, Kermanshah, Iran.
3 M.Sc. of Exercise Physiology, Faculty of Physical Education and Sport Sciences, Allameh Tabataba’i University, Tehran, Iran.
Abstract
Purpose: The objective of this study is to analyse various articles on the effect of various types of exercise on the angiopoietins family and angiopoietin-like proteins (ANGPTLs). Methods: PubMed, Science Direct, Scopus and Google Scholar databases were searched from 2000 to September 2020. After screening the articles, 19 articles that met the inclusion criteria were studied and analysed. Results: In our body, four types of angiopoietin and eight types of angiopoietin-like proteins have been identified, the functional method of some of them which are still not entirely understood. Angiopoietin-1 and angiopoietin-2 are essential regulators of vascular formation and maintenance. Angiopoietin-1 is found in perivascular and vascular cells within and around smooth muscle cells and plays an important role in growth, vascular stability, and pathological angiogenesis. On the other hand, angiopoietin-2 and angiopoietin-3 are mainly involved in inducing vascular regression, cell death, and inflammation. Angiopoietin-4, like angiopoietin-1, is responsible for the maturation, stabilization, and stasis of blood vessels. Conclusion: Studies show that exercise has a significant effect on increasing capillary density in the human body by increasing angiopoietin as one of the angiogenesis factors. In addition, there are many other benefits such as contribution to fat burning and treatment of coronary artery disease, cancer, asthma, and ischemia. More research is needed on the effects of different types of exercise training on angiopoietins.
Keywords
Abu-Farha, M., Cherian, P., Al-Khairi, I., Madhu, D., Tiss, A., Warsam, S., ... & Abubaker, J. (2017). Plasma and adipose tissue level of angiopoietinlike 7 (ANGPTL7) are increased in obesity and reduced after physical exercise. PloS one, 12(3), e0173024.
Ahmadian, M., Azizbeigi, K., Delfan, M., & Atashak, S. (2019). Effects of 10 week continuous endurance training on angiopoietin-1 gene expression and the tie2 protein in mice with breast cancer. Medical Journal of Tabriz University of Medical Sciences, 41(1), 7-13.
Ahmadian, M., Azizbeigi, K., Delfan, M., & Atashak, S. (2018). The Effect of High Intensity Interval Training on STAT-3 and Angiopoietin-1 Gene Expression, and tie-2 Protein in Mice with Breast Cancer. Iranian Quarterly Journal of Breast Disease, 11(1), 37-46.
Akwii, R. G., Sajib, M. S., Zahra, F. T., & Mikelis, C. M. (2019). Role of angiopoietin-2 in vascular physiology and pathophysiology. Cells, 8(5), 471.
Bahremand, M., Salehi, N., Rai, A., Rezaee, M., & Raeisei, A. A. (2014). Cardiac rehabilitation program with high intensity aerobic exercise can reverse diastolic impairment in patients undergoing coronary artery bypass surgery. Galen Medical Journal, 3(2), 102-108.
Barnard, C. R., Peters, M., Sindler, A. L., Farrell, E. T., Baker, K. R., Palta, M., ... & Bates, M. L. (2020). Increased aortic stiffness and elevated blood pressure in response to exercise in adult survivors of prematurity. Physiological reports, 8(12), e14462.
Barton, W. A., Tzvetkova, D., & Nikolov, D. B. (2005). Structure of the angiopoietin-2 receptor binding domain and identification of surfaces involved in Tie2 recognition. Structure, 13(5), 825-832.
Carbone, C., Piro, G., Merz, V., Simionato, F., Santoro, R., Zecchetto, C., ... & Melisi, D. (2018). Angiopoietin-like proteins in angiogenesis, inflammation and cancer. International journal of molecular sciences, 19(2), 431.
Catoire, M., Alex, S., Paraskevopulos, N., Mattijssen, F., Evers-van Gogh, I., Schaart, G., ... & Kersten, S. (2014). Fatty acid-inducible ANGPTL4 governs lipid metabolic response to exercise. Proceedings of the National Academy of Sciences, 111(11), E1043-E1052.
Chen, H. A., Kuo, T. C., Tseng, C. F., Ma, J. T., Yang, S. T., Yen, C. J., ... & Su, J. L. (2016). Angiopoietin‐like protein 1 antagonizes MET receptor activity to repress sorafenib resistance and cancer stemness in hepatocellular carcinoma. Hepatology, 64(5), 1637-1651.
Chi, X., Shetty, S. K., Shows, H. W., Hjelmaas, A. J., Malcolm, E. K., & Davies, B. S. (2015). Angiopoietin-like 4 modifies the interactions between lipoprotein lipase and its endothelial cell transporter GPIHBP1. Journal of Biological Chemistry, 290(19), 11865-11877.
DeBusk, L. M., Chen, Y., Nishishita, T., Chen, J., Thomas, J. W., & Lin, P. C. (2003). Tie2 receptor tyrosine kinase, a major mediator of tumor necrosis factor α–induced angiogenesis in rheumatoid arthritis. Arthritis & Rheumatism: Official Journal of the American College of Rheumatology, 48(9), 2461-2471.
Dijk, W., Beigneux, A. P., Larsson, M., Bensadoun, A., Young, S. G., & Kersten, S. (2016). Angiopoietin-like 4 promotes intracellular degradation of lipoprotein lipase in adipocytes. Journal of lipid research, 57(9), 1670-1683.
Downs, S. H., & Black, N. (1998). The feasibility of creating a checklist for the assessment of the methodological quality both of randomised and non-randomised studies of health care interventions. Journal of Epidemiology & Community Health, 52(6), 377-384.
Edwards, T., & Pilutti, L. A. (2017). The effect of exercise training in adults with multiple sclerosis with severe mobility disability: a systematic review and future research directions. Multiple sclerosis and related disorders, 16, 31-39.
Eklund, L., Kangas, J., & Saharinen, P. (2017). Angiopoietin–Tie signalling in the cardiovascular and lymphatic systems. Clinical Science, 131(1), 87103.
Eslami, R., Heidary, D., Mehdipour, A., & Heidari, S. (2021). The Effects of Acute Exercise and Exercise Training onPlasma Fibrinogen Levels in Healthy Individuals: A Meta-Analysis. Scientific Journal of Iran Blood Transfus Organ, 18(2), 127-141.
Fagiani, E., & Christofori, G. (2013). Angiopoietins in angiogenesis. Cancer letters, 328(1), 18-26.
Gholijani, F., Khosravi, N., Soori, R., Rezaeian, N., & Rajabi, B. (2016). Effect of One Session of Endurance Training on Serum Levels of ANGPTL4 and Lipids Profile in Sedentary Obese Wemen.
Górecka, M., Krzemiński, K., Buraczewska, M., Kozacz, A., Dąbrowski, J., & Ziemba, A. W. (2020). Effect of mountain ultra-marathon running on plasma angiopoietin-like protein 4 and lipid profile in healthy trained men. European Journal of Applied Physiology, 120(1), 117-125.
Gustafsson, T., Rundqvist, H., Norrbom, J., Rullman, E., Jansson, E., & Sundberg, C. J. (2007). The influence of physical training on the angiopoietin and VEGF-A systems in human skeletal muscle. Journal of Applied Physiology, 103(3), 1012-1020.
Hato, T., Tabata, M., & Oike, Y. (2008). The role of angiopoietin-like proteins in angiogenesis and metabolism. Trends in cardiovascular medicine, 18(1), 6-14.
Heidary, D., & Mehdipour, A. (2020). The effect of 8 weeks of cardio kickboxing exercises on cardiorespiratory endurance, body composition, quality of life and sleep quality of male students living in dormitories. New Approaches in Sport Sciences, 2(4), 197-208.
Higashi, Y., & Murohara, T. (Eds.). (2017). Therapeutic angiogenesis. Springer Singapore.
Hoier, B., Nordsborg, N., Andersen, S., Jensen, L., Nybo, L., Bangsbo, J., & Hellsten, Y. (2012). Pro‐and anti‐angiogenic factors in human skeletal muscle in response to acute exercise and training. The Journal of Physiology, 590(3), 595-606.
Holloway, T. M., Snijders, T., VAN, J. K., VAN, L. L., & Verdijk, L. B. (2018). Temporal response of angiogenesis and hypertrophy to resistance training in young men. Medicine and science in sports and exercise, 50(1), 36-45.
Hu, H., Yuan, G., Wang, X., Sun, J., Gao, Z., Zhou, T., . . . Wang, Z. (2019). Effects of a diet with or without physical activity on angiopoietin-like protein 8 concentrations in overweight/obese patients with newly diagnosed type 2 diabetes: a randomized controlled trial. Endocrine journal, 66(1), 89-105.
Ingerslev, B., Hansen, J. S., Hoffmann, C., Clemmesen, J. O., Secher, N. H., Scheler, M., . . . Weigert, C. (2017). Angiopoietin-like protein 4 is an exercise-induced hepatokine in humans, regulated by glucagon and cAMP. Molecular metabolism, 6(10), 1286-1295.
Isidori, A., Venneri, M., & Fiore, D. (2016). Angiopoietin-1 and Angiopoietin-2 in metabolic disorders: therapeutic strategies to restore the highs and lows of angiogenesis in diabetes. Journal of endocrinological investigation, 39(11), 1235-1246.
Kadomatsu, T., Tabata, M., & Oike, Y. (2011). Angiopoietin‐like proteins:
emerging targets for treatment of obesity and related metabolic diseases. The FEBS journal, 278(4), 559-564.
Kanazawa, H., Tochino, Y., & Asai, K. (2008). Angiopoietin-2 as a contributing factor of exercise-induced bronchoconstriction in asthmatic patients receiving inhaled corticosteroid therapy. Journal of allergy and clinical immunology, 121(2), 390-395.
Karkkainen, M. J., Haiko, P., Sainio, K., Partanen, J., Taipale, J., Petrova, T. V., . . . Rauvala, H. (2004). Vascular endothelial growth factor C is required for sprouting of the first lymphatic vessels from embryonic veins. Nature immunology, 5(1), 74-80.
Kersten, S., Lichtenstein, L., Steenber en, ., Mu e, K., en riks, . ., esselink, M. K., . . . M ller, M. 2009). Caloric restriction and exercise increase plasma ANGPTL4 levels in humans via elevated free fatty acids. Arteriosclerosis, thrombosis, and vascular biology, 29(6), 969-974.
Kissane, R. W., & Egginton, S. (2019). Exercise-mediated angiogenesis. Current Opinion in Physiology, 10, 193-201.
Larouche, J.-F., Yu, C., Luo, X., Farhat, N., Guiraud, T., Lalongé, J., . . . Thorin-Trescases, N. (2015). Acute high-intensity intermittent aerobic exercise reduces plasma angiopoietin-like 2 in patients with coronary artery disease. Canadian Journal of Cardiology, 31(10), 1232-1239.
Lee, E.-C., Desai, U., Gololobov, G., Hong, S., Feng, X., Yu, X.-C., . . . Du, L.-L. (2009). Identification of a new functional domain in angiopoietinlike 3 (ANGPTL3) and angiopoietin-like 4 (ANGPTL4) involved in binding and inhibition of lipoprotein lipase (LPL). Journal of Biological Chemistry, 284(20), 13735-13745.
Li, G., Zhang, H., & Ryan, A. S. (2020). Skeletal Muscle Angiopoietin-Like Protein 4 and Glucose Metabolism in Older Adults after Exercise and Weight Loss. Metabolites, 10(9), 354.
Mattijssen, F., & Kersten, S. (2012). Regulation of triglyceride metabolism by Angiopoietin-like proteins. Biochimica et Biophysica Acta (BBA)Molecular and Cell Biology of Lipids, 1821(5), 782-789.
McQueen, A. E., Kanamaluru, D., Yan, K., Gray, N. E., Wu, L., Li, M.-L., ... Koliwad, S. K. (2017). The C-terminal fibrinogen-like domain of angiopoietin-like 4 stimulates adipose tissue lipolysis and promotes energy expenditure. Journal of Biological Chemistry, 292(39), 1612216134.
Memczak, S., Jens, M., Elefsinioti, A., Torti, F., Krueger, J., Rybak, A., ... Munschauer, M. (2013). Circular RNAs are a large class of animal RNAs with regulatory potency. Nature, 495(7441), 333-338.
Metsios, G. S., Moe, R., van der Esch, M., van Zanten, J. V., Fenton, S., Koutedakis, Y., . . . Bostrom, C. (2020). The effects of exercise on cardiovascular disease risk factors and cardiovascular physiology in rheumatoid arthritis. Rheumatology international, 40(3), 347-357.
Morelli, M. B., Chavez, C., & Santulli, G. (2020). Angiopoietin-like proteins as therapeutic targets for cardiovascular disease: focus on lipid disorders.
Expert opinion on therapeutic targets, 24(1), 79-88.
Mousavizadeh, R., Scott, A., Lu, A., Ardekani, G. S., Behzad, H., Lundgreen, K., . . . Duronio, V. (2016). Angiopoietin‐like 4 promotes angiogenesis in the tendon and is increased in cyclically loaded tendon fibroblasts. The Journal of Physiology, 594(11), 2971-2983.
Naderi, R., Mohaddes, G., Mohammadi, M., Alihemmati, A., Khamaneh, A., Ghyasi, R., & Ghaznavi, R. (2019). The effect of garlic and voluntary exercise on cardiac angiogenesis in diabetes: the role of MiR-126 and MiR-210. Arquivos brasileiros de cardiologia, 112(2), 154-162.
Namkung, J., Koh, S. B., Kong, I. D., Choi, J.-W., & Yeh, B.-I. (2011). Serum levels of angiopoietin-related growth factor are increased in metabolic syndrome. Metabolism, 60(4), 564-568.
Norheim, F., Hjorth, M., Langleite, T. M., Lee, S., Holen, T., Bindesbøll, C., ... Kielland, A. (2014). Regulation of angiopoietin‐like protein 4 production during and after exercise. Physiological Reports, 2(8), e12109.
Park, S., Kim, J., & Lee, J. (2020). Effects of Exercise Intervention on Adults With Both Hypertension and Type 2 Diabetes Mellitus: A Systematic Review and Meta-analysis. The Journal of Cardiovascular Nursing.
Pilegaard, H., Saltin, B., & Neufer, P. D. (2003). Effect of short-term fasting and refeeding on transcriptional regulation of metabolic genes in human skeletal muscle. Diabetes, 52(3), 657-662.
Quagliarini, F., Wang, Y., Kozlitina, J., Grishin, N. V., Hyde, R., Boerwinkle, E., . . . Hobbs, H. H. (2012). Atypical angiopoietin-like protein that regulates ANGPTL3. Proceedings of the National Academy of Sciences, 109(48), 19751-19756.
Robciuc, M. R., Skrobuk, P., Anisimov, A., Olkkonen, V. M., Alitalo, K., Eckel, R. H., . . . Ehnholm, C. (2012). Angiopoietin-like 4 mediates PPAR delta effect on lipoprotein lipase-dependent fatty acid uptake but not on beta-oxidation in myotubes. PloS one, 7(10), e46212.
Salajegheh, A. (2016). Angiogenesis in health, disease and malignancy: Springer.
Sharma, V., Pangtey, G. S., Gupta, R., Rehan, H. S., & Gupta, L. K. (2017). Correlation of long-term glycemic control as measured by glycated hemoglobin with serum angiopoietin-like 6 protein levels in type 2 diabetes mellitus patients. Indian Journal of Pharmacology, 49(3), 250.
Soori, R., & CHoobine, S. (2018). Effect of endurance training on VEGF protein level in tissue of cardiac muscle in STZ-induced diabetic Wistar rats. Yafteh, 20(3), 110-124.
TaheriChadorneshin, H., & Nourshahi, M. (2017). A Review of Response of Angiogenic and Angiostatic Factors to Exercise. The Horizon of Medical Sciences, 23(4), 331-338.
Tan, M. J., Teo, Z., Sng, M. K., Zhu, P., & Tan, N. S. (2012). Emerging roles of angiopoietin-like 4 in human cancer. Molecular Cancer Research, 10(6), 677-688.
Tartibian, B., Heidary, D., Mehdipour, A., & Akbarizadeh, S. (2021). The effect of exercise and physical activity on sleep quality and quality of life in Iranian Older Adults: A systematic review. Journal of Gerontology, 6(1).
Thiagarajan, H., Thiyagamoorthy, U., Shanmugham, I., Nandagopal, G. D., & Kaliyaperumal, A. (2017). Angiogenic growth factors in myocardial infarction: a critical appraisal. Heart failure reviews, 22(6), 665-683.
Thorin-Trescases, N., Hayami, D., Yu, C., Luo, X., Nguyen, A., Larouche, J.F., . . . Gayda, M. (2016). Exercise lowers plasma angiopoietin-like 2 in men with post-acute coronary syndrome. PloS one, 11(10), e0164598.
Wang, L., Geng, T., Guo, X., Liu, J., Zhang, P., Yang, D., . . . Sun, Y. (2015). Co-expression of immunoglobulin-like transcript 4 and angiopoietin-like proteins in human non-small cell lung cancer. Molecular medicine reports, 11(4), 2789-2796.
Xu, L., Guo, Z.-N., Yang, Y., Xu, J., Burchell, S. R., Tang, J., . . . Zhang, J. H. (2015). Angiopoietin-like 4: A double-edged sword in atherosclerosis and ischemic stroke? Experimental neurology, 272, 61-66.
Zheng, Q., Zhu, D., Bai, Y., Wu, Y., Jia, J., & Hu, Y. (2011). Exercise improves recovery after ischemic brain injury by inducing the expression of angiopoietin-1 and Tie-2 in rats. The Tohoku journal of experimental medicine, 224(3), 221-228.
)