@2024 Afarand., IRAN
ISSN: 2252-0805 The Horizon of Medical Sciences 2017;23(4):331-338
ISSN: 2252-0805 The Horizon of Medical Sciences 2017;23(4):331-338
A Review of Response of Angiogenic and Angiostatic Factors to Exercise
ARTICLE INFO
Article Type
Analytic ReviewAuthors
TaheriChadorneshin H. (*)Ranjbar K. (1)
Nourshahi M. (2)
(*) Sport Sciences Department, Human Sciences Faculty, University of Bojnord, Bojnord, Iran
(1) Physical Education & Sport Science Department, Human Sciences Faculty, Bandar Abbas Branch, Islamic Azad University, Bandar Abbas, Iran
(2) Exercise Physiology Department, Sport Sciences Faculty, Shahid Beheshti University, Tehran, Iran
Correspondence
Article History
Received: September 2, 2016Accepted: May 21, 2017
ePublished: September 28, 2017
ABSTRACT
Aims
Angiogenesis and angiostasis processes mean the forming and
preventing the formation of a new capillary from pre-capillary, respectively.
Angiogenesis due to exercise is controlled by the balance between angiogenic
and angiostatic factors. Angiogenesis due to exercise training by increasing
capillary density in muscle fibers improves the transfer of oxygen and nutrients
to the muscle. The aim of this review was to evaluate the response of each of
these angiogenic and angiostatic factors to exercise.
Conclusion Vascular endothelial growth factor, transforming growth factor-β, angiopoiten and matrix metalloproteinase are most important angiogenic factors that show an up-regulated response following exercise. In contrast, angiostatin, endostatin, thrombospondine 1, and tissue inhibitor of metalloproteinase act as most important angiostatic factors. Although their functions in cell culture are cleared, further research is still necessary to obtain more consistent conclusions about response of inhibiting factors in both of physiologic and pathologic conditions following exercise.
Conclusion Vascular endothelial growth factor, transforming growth factor-β, angiopoiten and matrix metalloproteinase are most important angiogenic factors that show an up-regulated response following exercise. In contrast, angiostatin, endostatin, thrombospondine 1, and tissue inhibitor of metalloproteinase act as most important angiostatic factors. Although their functions in cell culture are cleared, further research is still necessary to obtain more consistent conclusions about response of inhibiting factors in both of physiologic and pathologic conditions following exercise.
CITATION LINKS
[1]Gavin TP, Stallings HW, Zwetsloot KA, Westerkamp LM, Ryan NA, Moore RA, et al. Lower capillary density but no difference in VEGF expression in obese vs. lean young skeletal muscle in humans. J Appl Physiol. 2004;98(1):315-21.
[2]Brown MD. Exercise and coronary vascular remodeling in the healthy heart. Exp Physiol. 2003;88(5):645-58.
[3]Roy S, Khanna S, Sen CK. Redox regulation of the VEGF signaling path and tissue vascularization: hydrogen peroxide, the common link between physical exercise and cutaneous wound healing. Free Radic Biol Med. 2008;44(2):180-92.
[4]Ushio-Fukai M, Nakamura Y. Reactive oxygen species and angiogenesis: NADPH oxidase as target for cancer therapy. Cancer Lett. 2008;266(1):37-52.
[5]Zachary I, Gliki G. Signaling transduction mechanisms mediating biological actions of the vascular endothelial growth factor family. Cardiovasc Res. 2001;49(3):568-81.
[6]Egginton S. Invited review: Activity-induced angiogenesis. Pflugers Arch. 2009; 457(5): 963-77.
[7]Ferrara N, Smith TD. The biology of vascular endothelial growth factor. Endocr Rev. 1997;18(1):4-25.
[8]Prior BM, Yang HT, Terjung RL. What makes vessels grow with exercise training?. J Appl Physiol. 2004;97(3):1119-28.
[9]Nourshahi M, Taheri chadorneshin H, Ranjbar K. The stimulus of angiogenesis during exercise and physical activity. Horizon Med Scien. 2013;18(5):286-96. [Persian]
[10]Lloyd PG, Prior BM, Yang HT, Terjung RL. Angiogenic growth factor expression in rat skeletal muscle in response to exercise training. Am J Physiol Heart Circ Physiol. 2003;284(5):H1668-78.
[11]Olfert IM, Howlett RA, Tang K, Dalton ND, Gu Y, Peterson KL, et al. Muscle-specific VEGF deficiency greatly reduces exercise endurance in mice. J Physiol. 2009;587(Pt 8):1755-67.
[12]Stefanini MO, Wu FTH, Feilim M, Gabhann FM, Popel AS. A compartment model of VEGF distribution in blood, healthy and diseased tissues. BMC Syst Biol. 2008;2:77.
[13]Kraus RM, Stallings HW, Yeager RC, Gavin TP. Circulating plasma VEGF response to exercise in sedentary and endurance-trained men. J Appl Physiol. 2004;96(4):1445-50.
[14]Dantz D, Bewersdorf J, Fruehwald-Schultes B, Kern W, Jelkmann W, Born J, et al. Vascular endothelial growth factor: A novel endocrine defensive response to hypoglycemia. J Clin Endocrinol Metab. 2002;87(2):835-40.
[15]Gavin TP, Wagner PD. Effect of short-term exercise training on angiogenic growth factor gene responses in rats. J Appl Physiol. 2001;90(4):1219-26.
[16]Taheri Chadorneshin H, Nourshahi M, Ranjbar K. Response of vascular endothelial growth factor to exhausted sub maximal exercise and its correlation with VO2max. J Sport Biosci. 2010;2(7):59-75. [Persian]
[17]Ranjbar K, Nourshahi M, Hedayati M, Taheri H. Effect of gender and physical activity on serum vascular endothelial growth factor at rest and response to submaximal exercise. Iran J Endocrinol Metabol. 2011;13(3):294-300. [Persian]
[18]Ranjbar K, Nourshahi M, Hedayati M, Taheri H. A study on the serum levels of angiogenic factors in response to acute long-term submaximal exercise in sedentary men. Physiol Pharmacol. 2011;15(1):124-32. [Persian]
[19]Nourshahi M, Taheri Chadorneshin H, Piroz M. Effect of endurance training in hypoxia-normobaric and normal conditions on serum VEGF concentration, hemoglobin and blood hematocrit. Horizon Med Sci. 2012;18(3):135-40. [Persian]
[20]Ranjbar K, Nazem F, Nazari A, Gholami M, Nezami AR, Ardakanizade M, et al. Synergistic effects of nitric oxide and exercise on revascularisation in the infarcted ventricle in a murine model of myocardial infarction. EXCLI J. 2015;14:1104-15.
[21]Rahmouni K, Haynes W. Endothelial effects of leptin: Implications in health and diseases. Curr Diab Rep. 2005;5(4):260-6.
[22]Nourshahi M, Ebrahim K, Taheri Chadorneshin H. Effect of vitamin E supplementation on angiogenic factor response to exhaustive exercise. Sport Sci. 2011;3(11):81-96. [Persian]
[23]Ranjbar K, Nazem F, Nazari A. Effect of exercise training and l-arginine on oxidative stress and left ventricular function in the post-ischemic failing rat heart. Cardiovasc Toxicol. 2016;16(2):122-9.
[24]Nourshahi M, Hedayati M, Ranjbar K. The correlation between resting serum leptin and serum angiogenic indices at rest and after submaximal exercise. Regul Pept. 2012;173(1-3):6-12.
[25]Gustafsson T, Kraus WE. Exercise-induced angiogenesis-related growth and transcription factors in skeletal mscle, and their modification in muscle pathology. Front Biosci. 2001;6:D75-89.
[26]Kawaguchi N, Toriyama K, Nicodemou-Lena E, Inou K, Torii S, Kitagawa Y. De novo adipogenesis in mice at the site of injection of basement membrane and basic fibroblast growth factor. Proc Natl Acad Sci USA. 1998;95(3):1062-6.
[27]Lijnen RH. Angiogenesis and obesity. Cardiovasc Res. 2008;78(2):286-93.
[28]Roca J, Gavin, TP, Jordan M, Siafakas N, Wagner H, Benoit H, et al. Angiogenic growth factor mRNA responses to passive and contraction-induced hyperperfusion in skeletal muscle. J Appl Physiol. 1998;85(3):1142-9.
[29]Gavin TP, Spector DA, Wagner H, Breen EC, Wagner PD. Nitric oxide synthase inhibition attenuates the skeletal muscle VEGF mRNA response to exercise. J Appl Physiol. 2000;88(4):1192-8.
[30]- Gustafsson T, Puntschart A, Kaijser L, Jansson E, Sundberg CJ. Exercise-induced expression of angiogenesis-related transcription and growth factors in human skeletal muscle. Am J Physiol. 1999;276(2 Pt 2):H679-85.
[31]Olfert IM, Breen EC, Mathieu- Costello O, Wagner PD. Skeletal muscle capillarity and angiogenic mRNA levels after exercise training in normoxia and chronic hypoxia. J Appl Physiol. 2001;91(3):1176-84.
[32]Czarkowska-Paczek B, Bartlomiejczyk I, Przybylski J. The serum levels of growth factors: PDGF, TGF-BETA and VEGF are increased after strenuous physical exercise. J Physiol Pharmacol. 2006;57(2):189-97.
[33]Timmons JA, Jansson E, Fischer H, Gustafsson T, Greenhaff PL, Ridden J, et al. Modulation of extracellular matrix genes reflects the magnitude of physiological adaptation to aerobic exercise training in humans. BMC Biol. 2005;3:19.
[34]Ranjbar K, Rahmani-Nia F, Shahabpour E. Aerobic training and l-arginine supplementation promotes rat heart and hindleg muscles arteriogenesis after myocardial infarction. J Physiol Biochem. 2016;72(3):393-404.
[35]Metheny- Barlow LJ, Lu Yuan LI. The enigmatic role of angiopoietin-1 in tumor angiogenesis. Cell Res. 2003;13(5):309-17.
[36]Karkkainen MJ, Haiko P, Sainio K, Partanen J, Taipale J, Petrova TV, et al. Vascular endothelial growth factor C is required for sprouting of the first lymphatic vessels from embryonic veins. Nat Immunol. 2004;5(1):74-80.
[37]Gavin TP, Drew JL, Kubik CJ, Pofah WE, Hickner RC. Acute resistance exercise increases skeletal muscle angiogenic growth factor expression. Acta Physiol (Oxf). 2007;191(2):139-46.
[38]Gustafsson T, Rundqvist H, Norrbom J, Rullman E, Jansson E, Sundberg CJ. The influence of physical training on the angiopoietin and VEGF-A systems in human skeletal muscle. J Appl Physiol. 2007;103(3):1012-20.
[39]van Hinsbergh VW, Koolwijk P. Endothelial sprouting and angiogenesis: matrix metalloproteinases in the lead. Cardiovasc Res. 2008;78(2):203-12.
[40]Haas TL, Milkiewicz M, Davis SJ, Zhou AL, Egginton S, Brown MD, et al. Matrix metalloproteinase activity is required for activity induced angiogenesis in rat skeletal muscle. Am J Physiol Heart Circ Physiol. 2000;279(4):H1540-7.
[41]Suhr F, Brixius K, de Marées M, Bölck B, Kleinöder H, Achtzehn S, et al. Effects of short-term vibration and hypoxia during high-intensity cycling exercise on circulating levels of angiogenic regulators in humans. J Appl Physiol. 2007;103(2):474-83.
[42]Mackey AL, Donnelly AE, Turpeenniemi-Hujanen T, Roper HP. Skeletal muscle collagen content in humans after high-force eccentric contractions. J Appl Physiol. 2004;97(1):197-203.
[43]Urso ML, Pierce JR, Alemany JA, Harman EA, Nindl BC. Effects of exercise training on the matrix metalloprotease response to acute exercise. Eur J Appl Physiol. 2009;106(5):655-63.
[44]Rullman E, Norrbom J, Stromberg A, Wagsater D, Rundqvist H, Haas T. et al. Endurance exercise activates matrix metalloproteinases in human skeletal muscle. J Appl Physiol. 2009;106(3):804-12.
[45]Taheri Chadorneshin H, Nourshahi M, Ranjbar K. A comparison of angiogenic proteinases in active and non-active men in response to submaximal exercise. Res Sport Sci. 2011;3(10):143-58. [Persian]
[46]Carmeli E, Moas M, Lennon S, Powers SK. High intensity exercise increases expression of matrix metalloproteinases in fast skeletal muscle fibers. Exp Physiol. 2005;90(4):613-9.
[47]Koskinen SO, Heinemeier KM, Olesen JL, Langberg H, Kjaer M. Physical exercise can influence local levels of matrix metalloproteinases and their inhibitors in tendon-related connective tissue. J Appl Physiol. 2004;96(3):861-4.
[48]Roberts CK, Won D, Pruthi S, Kurtovic S, Sindhu RK, Vaziri ND, et al. Effect of a short-term diet and exercise intervention on oxidative stress, inflammation, MMP-9, and monocyte chemotactic activity in men with metabolic syndrome factors. J Appl Physiol. 2006;100(5):1657-65.
[49]Williamson JR, Hoffmann PL, Kohrt WM, Spina RJ, Coggan AR, Holloszy O. Endurance exercise training decreases capillary basement membrane width in older nondiabetic and diabetic adults. J Appl Physiol. 1996;80(3):747-53.
[50]Ranjbar K, Nourshahi M, Gholamali M, Mirzaei S. The effects of gender on serum gelatinases (mmp-2 and mmp-9) at rest and in response to acute endurance exercise. J Sport Biosci. 2012;4(10):61-76. [Persian]
[51]Rullman E, Rundqvist H, Wagsa ter D, Fischer H, Eriksson P, Sundberg CJ, et al. A single bout of exercise activates matrix metalloproteinase in human skeletal muscle. J Appl Physiol. 2007;102(6):2346-51.
[52]O’Reilly MS, Holmgren L, Shing Y, Chen C, Rosenthal RA, Moses M, et al. Angiostatin: A novel angiogenesis inhibitor that mediates the suppression of metastases by Lewis lung carcinoma. Cell. 1994;79(2):315-28.
[53]Drixler TA, Borel Rinkes IH, Ritchie ED, Treffers FW, van Vroonhoven TJ, Gebbink MF, et al. Angiostatin inhibits pathological but not physiological retinal angiogenesis. Invest Ophthalmol Vis Sci. 2001;42(13):3325-30.
[54]O’Reilly MS, Boehm T, Shing Y, Fukai N, Vasios G, Lane WS, et al. Endostatin: An endogenous inhibitor of angiogenesis and tumor growth. Cell. 1997;88(2):277-85.
[55]Ferreras M, Felbor U, Lenhard T, Olsen BR, Delaisse J. Generation and degradation of human endostatin proteins by various proteinases. FEBS Lett. 2000;486(3):247-51.
[56]Gu JW, Shparago M, Tan W, Bailey AP. Tissue endostatin correlates inversely with capillary network in rat heart and skeletal muscles. Angiogenesis. 2006;9(2):93-9.
[57]Gu JW, Gadonski G, Wang J, Makey I, Adair TH. Exercise increases endostatin in circulation of healthy volunteers. BMC Physiol. 2004;4:2.
[58]Brixius K, Schoenberger S, Ladage D, Knigge H, Falkowski G, Hellmich M, et al. Long-term endurance exercise decreases antiangiogenic endostatin signalling in overweight men aged 50-60 years. Br J Sports Med. 2008;42(2):126-9.
[59]Suhr F, Rosenwick C, Vassiliadis A, Bloch W, Brixius K. Regulation of extracellular matrix compounds involved in angiogenic processes in short- and long-track elite runners. Scand J Med Sci Sports. 2010;20(3):441-8.
[60]Nourshahi M, Hedayati M, Nemati J, Ranjbar K, Gholamali M. Effect of 8 weeks endurance training on serum vascular endothelial growth factor and endostatin in Wistar rats. Koomesh. 2012;13(4):474-9. [Persian]
[61]Rodriguez-Manzaneque JC, Lane TF, Ortega MA, Hynes RO, Lawler J, Iruela-Arispe ML. Thrombospondin-1 suppresses spontaneous tumor growth and inhibits activation of matrix metalloproteinase-9 and mobilization of vascular endothelial growth factor. Proc Natl Acad Sci USA. 2001;98(22):12485-90.
[62]Malek MH, Olfert IM. Global deletion of thrombospondin-1 increases cardiac and skeletal muscle capillarity and exercise capacity in mice. Exp Physiol. 2009;94(6):749-60.
[63]Kivelä R, Silvennoinen M, Lehti M, Jalava S, Vihko V, Kainulainen H. Exercise-induced expression of angiogenic growth factors in skeletal muscle and in capillaries of healthy and diabetic mice. Cardiovasc Diabetol. 2008;7:13.
[64]Olfert IM, Breen EC, Gavin TP, Wagner PD. Temporal thrombospondin-1 mRNA response in skeletal muscle exposed to acute and chronic exercise. Growth Factors. 2006;24(4):253-9.
[65]Hoier B, Nordsborg N, Andersen S, Jensen L, Nybo L, Bangsbo J, et al. Pro- and anti-angiogenic factors in human skeletal muscle in response to acute exercise and training. J Physiol. 2012; 590(3):595-606.
[66]Rege TA, Fears CY, Gladson CL. Endogenous inhibitors of angiogenesis in malignant gliomas: Nature’s antiangiogenic therapy. Neuro Oncol. 2005;7(2):106-21.
[67]Hajitou A, Sounni NE, Devy L, Grignet-Debrus C, Lewalle JM, Li H, et al. Down-regulation of vascular endothelial growth factor by tissue inhibitor of metalloproteinase-2: Effect on in vivo mammary tumor growth and angiogenesis. Cancer Res. 2001;61(8):3450-7.
[68]Koskinen SOA, Höyhtyä M, Turpeenniemi-Hujanen T, Martikkala V, Mäkinen TT, Oksa J, et al. Serum concentrations of collagen degrading enzymes and their inhibitors after downhill running. Scand J Med Sci Sports. 2001;11(1):9-15.
[69]Kadoglou NP, Kostomitsopoulos N, Kapelouzou A, Moustardas P, Katsimpoulas M, Giagini A, et al. Effects of exercise training on the severity and composition of atherosclerotic plaque in apoe-deficient mice. J Vasc Res. 2011;48(4):347-56.
[70]Kwak HB, Kim JH, Joshi K, Yeh A, Martinez DA, Lawler JM. Exercise training reduces fibrosis and matrix metalloproteinase dysregulation in the aging rat heart. FASEB J. 2011;25(3):1106-17.
[2]Brown MD. Exercise and coronary vascular remodeling in the healthy heart. Exp Physiol. 2003;88(5):645-58.
[3]Roy S, Khanna S, Sen CK. Redox regulation of the VEGF signaling path and tissue vascularization: hydrogen peroxide, the common link between physical exercise and cutaneous wound healing. Free Radic Biol Med. 2008;44(2):180-92.
[4]Ushio-Fukai M, Nakamura Y. Reactive oxygen species and angiogenesis: NADPH oxidase as target for cancer therapy. Cancer Lett. 2008;266(1):37-52.
[5]Zachary I, Gliki G. Signaling transduction mechanisms mediating biological actions of the vascular endothelial growth factor family. Cardiovasc Res. 2001;49(3):568-81.
[6]Egginton S. Invited review: Activity-induced angiogenesis. Pflugers Arch. 2009; 457(5): 963-77.
[7]Ferrara N, Smith TD. The biology of vascular endothelial growth factor. Endocr Rev. 1997;18(1):4-25.
[8]Prior BM, Yang HT, Terjung RL. What makes vessels grow with exercise training?. J Appl Physiol. 2004;97(3):1119-28.
[9]Nourshahi M, Taheri chadorneshin H, Ranjbar K. The stimulus of angiogenesis during exercise and physical activity. Horizon Med Scien. 2013;18(5):286-96. [Persian]
[10]Lloyd PG, Prior BM, Yang HT, Terjung RL. Angiogenic growth factor expression in rat skeletal muscle in response to exercise training. Am J Physiol Heart Circ Physiol. 2003;284(5):H1668-78.
[11]Olfert IM, Howlett RA, Tang K, Dalton ND, Gu Y, Peterson KL, et al. Muscle-specific VEGF deficiency greatly reduces exercise endurance in mice. J Physiol. 2009;587(Pt 8):1755-67.
[12]Stefanini MO, Wu FTH, Feilim M, Gabhann FM, Popel AS. A compartment model of VEGF distribution in blood, healthy and diseased tissues. BMC Syst Biol. 2008;2:77.
[13]Kraus RM, Stallings HW, Yeager RC, Gavin TP. Circulating plasma VEGF response to exercise in sedentary and endurance-trained men. J Appl Physiol. 2004;96(4):1445-50.
[14]Dantz D, Bewersdorf J, Fruehwald-Schultes B, Kern W, Jelkmann W, Born J, et al. Vascular endothelial growth factor: A novel endocrine defensive response to hypoglycemia. J Clin Endocrinol Metab. 2002;87(2):835-40.
[15]Gavin TP, Wagner PD. Effect of short-term exercise training on angiogenic growth factor gene responses in rats. J Appl Physiol. 2001;90(4):1219-26.
[16]Taheri Chadorneshin H, Nourshahi M, Ranjbar K. Response of vascular endothelial growth factor to exhausted sub maximal exercise and its correlation with VO2max. J Sport Biosci. 2010;2(7):59-75. [Persian]
[17]Ranjbar K, Nourshahi M, Hedayati M, Taheri H. Effect of gender and physical activity on serum vascular endothelial growth factor at rest and response to submaximal exercise. Iran J Endocrinol Metabol. 2011;13(3):294-300. [Persian]
[18]Ranjbar K, Nourshahi M, Hedayati M, Taheri H. A study on the serum levels of angiogenic factors in response to acute long-term submaximal exercise in sedentary men. Physiol Pharmacol. 2011;15(1):124-32. [Persian]
[19]Nourshahi M, Taheri Chadorneshin H, Piroz M. Effect of endurance training in hypoxia-normobaric and normal conditions on serum VEGF concentration, hemoglobin and blood hematocrit. Horizon Med Sci. 2012;18(3):135-40. [Persian]
[20]Ranjbar K, Nazem F, Nazari A, Gholami M, Nezami AR, Ardakanizade M, et al. Synergistic effects of nitric oxide and exercise on revascularisation in the infarcted ventricle in a murine model of myocardial infarction. EXCLI J. 2015;14:1104-15.
[21]Rahmouni K, Haynes W. Endothelial effects of leptin: Implications in health and diseases. Curr Diab Rep. 2005;5(4):260-6.
[22]Nourshahi M, Ebrahim K, Taheri Chadorneshin H. Effect of vitamin E supplementation on angiogenic factor response to exhaustive exercise. Sport Sci. 2011;3(11):81-96. [Persian]
[23]Ranjbar K, Nazem F, Nazari A. Effect of exercise training and l-arginine on oxidative stress and left ventricular function in the post-ischemic failing rat heart. Cardiovasc Toxicol. 2016;16(2):122-9.
[24]Nourshahi M, Hedayati M, Ranjbar K. The correlation between resting serum leptin and serum angiogenic indices at rest and after submaximal exercise. Regul Pept. 2012;173(1-3):6-12.
[25]Gustafsson T, Kraus WE. Exercise-induced angiogenesis-related growth and transcription factors in skeletal mscle, and their modification in muscle pathology. Front Biosci. 2001;6:D75-89.
[26]Kawaguchi N, Toriyama K, Nicodemou-Lena E, Inou K, Torii S, Kitagawa Y. De novo adipogenesis in mice at the site of injection of basement membrane and basic fibroblast growth factor. Proc Natl Acad Sci USA. 1998;95(3):1062-6.
[27]Lijnen RH. Angiogenesis and obesity. Cardiovasc Res. 2008;78(2):286-93.
[28]Roca J, Gavin, TP, Jordan M, Siafakas N, Wagner H, Benoit H, et al. Angiogenic growth factor mRNA responses to passive and contraction-induced hyperperfusion in skeletal muscle. J Appl Physiol. 1998;85(3):1142-9.
[29]Gavin TP, Spector DA, Wagner H, Breen EC, Wagner PD. Nitric oxide synthase inhibition attenuates the skeletal muscle VEGF mRNA response to exercise. J Appl Physiol. 2000;88(4):1192-8.
[30]- Gustafsson T, Puntschart A, Kaijser L, Jansson E, Sundberg CJ. Exercise-induced expression of angiogenesis-related transcription and growth factors in human skeletal muscle. Am J Physiol. 1999;276(2 Pt 2):H679-85.
[31]Olfert IM, Breen EC, Mathieu- Costello O, Wagner PD. Skeletal muscle capillarity and angiogenic mRNA levels after exercise training in normoxia and chronic hypoxia. J Appl Physiol. 2001;91(3):1176-84.
[32]Czarkowska-Paczek B, Bartlomiejczyk I, Przybylski J. The serum levels of growth factors: PDGF, TGF-BETA and VEGF are increased after strenuous physical exercise. J Physiol Pharmacol. 2006;57(2):189-97.
[33]Timmons JA, Jansson E, Fischer H, Gustafsson T, Greenhaff PL, Ridden J, et al. Modulation of extracellular matrix genes reflects the magnitude of physiological adaptation to aerobic exercise training in humans. BMC Biol. 2005;3:19.
[34]Ranjbar K, Rahmani-Nia F, Shahabpour E. Aerobic training and l-arginine supplementation promotes rat heart and hindleg muscles arteriogenesis after myocardial infarction. J Physiol Biochem. 2016;72(3):393-404.
[35]Metheny- Barlow LJ, Lu Yuan LI. The enigmatic role of angiopoietin-1 in tumor angiogenesis. Cell Res. 2003;13(5):309-17.
[36]Karkkainen MJ, Haiko P, Sainio K, Partanen J, Taipale J, Petrova TV, et al. Vascular endothelial growth factor C is required for sprouting of the first lymphatic vessels from embryonic veins. Nat Immunol. 2004;5(1):74-80.
[37]Gavin TP, Drew JL, Kubik CJ, Pofah WE, Hickner RC. Acute resistance exercise increases skeletal muscle angiogenic growth factor expression. Acta Physiol (Oxf). 2007;191(2):139-46.
[38]Gustafsson T, Rundqvist H, Norrbom J, Rullman E, Jansson E, Sundberg CJ. The influence of physical training on the angiopoietin and VEGF-A systems in human skeletal muscle. J Appl Physiol. 2007;103(3):1012-20.
[39]van Hinsbergh VW, Koolwijk P. Endothelial sprouting and angiogenesis: matrix metalloproteinases in the lead. Cardiovasc Res. 2008;78(2):203-12.
[40]Haas TL, Milkiewicz M, Davis SJ, Zhou AL, Egginton S, Brown MD, et al. Matrix metalloproteinase activity is required for activity induced angiogenesis in rat skeletal muscle. Am J Physiol Heart Circ Physiol. 2000;279(4):H1540-7.
[41]Suhr F, Brixius K, de Marées M, Bölck B, Kleinöder H, Achtzehn S, et al. Effects of short-term vibration and hypoxia during high-intensity cycling exercise on circulating levels of angiogenic regulators in humans. J Appl Physiol. 2007;103(2):474-83.
[42]Mackey AL, Donnelly AE, Turpeenniemi-Hujanen T, Roper HP. Skeletal muscle collagen content in humans after high-force eccentric contractions. J Appl Physiol. 2004;97(1):197-203.
[43]Urso ML, Pierce JR, Alemany JA, Harman EA, Nindl BC. Effects of exercise training on the matrix metalloprotease response to acute exercise. Eur J Appl Physiol. 2009;106(5):655-63.
[44]Rullman E, Norrbom J, Stromberg A, Wagsater D, Rundqvist H, Haas T. et al. Endurance exercise activates matrix metalloproteinases in human skeletal muscle. J Appl Physiol. 2009;106(3):804-12.
[45]Taheri Chadorneshin H, Nourshahi M, Ranjbar K. A comparison of angiogenic proteinases in active and non-active men in response to submaximal exercise. Res Sport Sci. 2011;3(10):143-58. [Persian]
[46]Carmeli E, Moas M, Lennon S, Powers SK. High intensity exercise increases expression of matrix metalloproteinases in fast skeletal muscle fibers. Exp Physiol. 2005;90(4):613-9.
[47]Koskinen SO, Heinemeier KM, Olesen JL, Langberg H, Kjaer M. Physical exercise can influence local levels of matrix metalloproteinases and their inhibitors in tendon-related connective tissue. J Appl Physiol. 2004;96(3):861-4.
[48]Roberts CK, Won D, Pruthi S, Kurtovic S, Sindhu RK, Vaziri ND, et al. Effect of a short-term diet and exercise intervention on oxidative stress, inflammation, MMP-9, and monocyte chemotactic activity in men with metabolic syndrome factors. J Appl Physiol. 2006;100(5):1657-65.
[49]Williamson JR, Hoffmann PL, Kohrt WM, Spina RJ, Coggan AR, Holloszy O. Endurance exercise training decreases capillary basement membrane width in older nondiabetic and diabetic adults. J Appl Physiol. 1996;80(3):747-53.
[50]Ranjbar K, Nourshahi M, Gholamali M, Mirzaei S. The effects of gender on serum gelatinases (mmp-2 and mmp-9) at rest and in response to acute endurance exercise. J Sport Biosci. 2012;4(10):61-76. [Persian]
[51]Rullman E, Rundqvist H, Wagsa ter D, Fischer H, Eriksson P, Sundberg CJ, et al. A single bout of exercise activates matrix metalloproteinase in human skeletal muscle. J Appl Physiol. 2007;102(6):2346-51.
[52]O’Reilly MS, Holmgren L, Shing Y, Chen C, Rosenthal RA, Moses M, et al. Angiostatin: A novel angiogenesis inhibitor that mediates the suppression of metastases by Lewis lung carcinoma. Cell. 1994;79(2):315-28.
[53]Drixler TA, Borel Rinkes IH, Ritchie ED, Treffers FW, van Vroonhoven TJ, Gebbink MF, et al. Angiostatin inhibits pathological but not physiological retinal angiogenesis. Invest Ophthalmol Vis Sci. 2001;42(13):3325-30.
[54]O’Reilly MS, Boehm T, Shing Y, Fukai N, Vasios G, Lane WS, et al. Endostatin: An endogenous inhibitor of angiogenesis and tumor growth. Cell. 1997;88(2):277-85.
[55]Ferreras M, Felbor U, Lenhard T, Olsen BR, Delaisse J. Generation and degradation of human endostatin proteins by various proteinases. FEBS Lett. 2000;486(3):247-51.
[56]Gu JW, Shparago M, Tan W, Bailey AP. Tissue endostatin correlates inversely with capillary network in rat heart and skeletal muscles. Angiogenesis. 2006;9(2):93-9.
[57]Gu JW, Gadonski G, Wang J, Makey I, Adair TH. Exercise increases endostatin in circulation of healthy volunteers. BMC Physiol. 2004;4:2.
[58]Brixius K, Schoenberger S, Ladage D, Knigge H, Falkowski G, Hellmich M, et al. Long-term endurance exercise decreases antiangiogenic endostatin signalling in overweight men aged 50-60 years. Br J Sports Med. 2008;42(2):126-9.
[59]Suhr F, Rosenwick C, Vassiliadis A, Bloch W, Brixius K. Regulation of extracellular matrix compounds involved in angiogenic processes in short- and long-track elite runners. Scand J Med Sci Sports. 2010;20(3):441-8.
[60]Nourshahi M, Hedayati M, Nemati J, Ranjbar K, Gholamali M. Effect of 8 weeks endurance training on serum vascular endothelial growth factor and endostatin in Wistar rats. Koomesh. 2012;13(4):474-9. [Persian]
[61]Rodriguez-Manzaneque JC, Lane TF, Ortega MA, Hynes RO, Lawler J, Iruela-Arispe ML. Thrombospondin-1 suppresses spontaneous tumor growth and inhibits activation of matrix metalloproteinase-9 and mobilization of vascular endothelial growth factor. Proc Natl Acad Sci USA. 2001;98(22):12485-90.
[62]Malek MH, Olfert IM. Global deletion of thrombospondin-1 increases cardiac and skeletal muscle capillarity and exercise capacity in mice. Exp Physiol. 2009;94(6):749-60.
[63]Kivelä R, Silvennoinen M, Lehti M, Jalava S, Vihko V, Kainulainen H. Exercise-induced expression of angiogenic growth factors in skeletal muscle and in capillaries of healthy and diabetic mice. Cardiovasc Diabetol. 2008;7:13.
[64]Olfert IM, Breen EC, Gavin TP, Wagner PD. Temporal thrombospondin-1 mRNA response in skeletal muscle exposed to acute and chronic exercise. Growth Factors. 2006;24(4):253-9.
[65]Hoier B, Nordsborg N, Andersen S, Jensen L, Nybo L, Bangsbo J, et al. Pro- and anti-angiogenic factors in human skeletal muscle in response to acute exercise and training. J Physiol. 2012; 590(3):595-606.
[66]Rege TA, Fears CY, Gladson CL. Endogenous inhibitors of angiogenesis in malignant gliomas: Nature’s antiangiogenic therapy. Neuro Oncol. 2005;7(2):106-21.
[67]Hajitou A, Sounni NE, Devy L, Grignet-Debrus C, Lewalle JM, Li H, et al. Down-regulation of vascular endothelial growth factor by tissue inhibitor of metalloproteinase-2: Effect on in vivo mammary tumor growth and angiogenesis. Cancer Res. 2001;61(8):3450-7.
[68]Koskinen SOA, Höyhtyä M, Turpeenniemi-Hujanen T, Martikkala V, Mäkinen TT, Oksa J, et al. Serum concentrations of collagen degrading enzymes and their inhibitors after downhill running. Scand J Med Sci Sports. 2001;11(1):9-15.
[69]Kadoglou NP, Kostomitsopoulos N, Kapelouzou A, Moustardas P, Katsimpoulas M, Giagini A, et al. Effects of exercise training on the severity and composition of atherosclerotic plaque in apoe-deficient mice. J Vasc Res. 2011;48(4):347-56.
[70]Kwak HB, Kim JH, Joshi K, Yeh A, Martinez DA, Lawler JM. Exercise training reduces fibrosis and matrix metalloproteinase dysregulation in the aging rat heart. FASEB J. 2011;25(3):1106-17.