Exercise and Ischemia-Activated Pathways in Limb Muscle Angiogenesis and Vascular Regeneration

Vihang A. Narkar

doi:10.14797/mdcvj.1304

Exercise and Ischemia-Activated Pathways in Limb Muscle Angiogenesis and Vascular Regeneration

Methodist DeBakey Cardiovascular Journal

Volume 19 (2023): Issue 5

By: Vihang A. Narkar

Open Access

|Nov 2023

Brinkmann C. Road map for personalized exercise medicine in T2DM. Trends Endocrinol Metab. 2023 Sep 18:S1043-2760(23)00166-2. doi: 10.1016/j.tem.2023.08.013
Open DOI Search in Google Scholar Back to article
Khemka S, Reddy A, Garcia RI, et al. Role of diet and exercise in aging, Alzheimer’s disease, and other chronic diseases. Ageing Res Rev. 2023;91:102091. doi: 10.1016/j.arr.2023.102091
Open DOI Search in Google Scholar Back to article
Pinto AJ, Bergouignan A, Dempsey PC, et al. Physiology of sedentary behavior. Physiol Rev. 2023 Oct 1;103(4):2561-622. doi: 10.1152/physrev.00022.2022
Open DOI Search in Google Scholar Back to article
McDermott MM, Ferrucci L, Gonzalez-Freire M, et al. Skeletal Muscle Pathology in Peripheral Artery Disease: A Brief Review. Arterioscler Thromb Vasc Biol. 2020 Nov;40(11):2577-85. doi: 10.1161/ATVBAHA.120.313831
Open DOI Search in Google Scholar Back to article
Pizzimenti M, Meyer A, Charles AL, et al. Sarcopenia and peripheral arterial disease: a systematic review. J Cachexia Sarcopenia Muscle. 2020 Aug;11(4):866-86. doi: 10.1002/jcsm.12587
Open DOI Search in Google Scholar Back to article
Golledge J. Update on the pathophysiology and medical treatment of peripheral artery disease. Nat Rev Cardiol. 2022 Jul;19(7):456-74. doi: 10.1038/s41569-021-00663-9
Open DOI Search in Google Scholar Back to article
Shamaki GR, Markson F, Soji-Ayoade D, Agwuegbo CC, Bamgbose MO, Tamunoinemi BM. Peripheral Artery Disease: A Comprehensive Updated Review. Curr Probl Cardiol. 2022 Nov;47(11):101082. doi: 10.1016/j.cpcardiol.2021.101082
Open DOI Search in Google Scholar Back to article
Kotalczyk A, Vallabhaneni SR, Lip GYH. Review new concepts in pharmacotherapy for peripheral arterial disease. Curr Opin Cardiol. 2021 Nov 1;36(6):720-6. doi: 10.1097/HCO.0000000000000883
Open DOI Search in Google Scholar Back to article
Haas TL, Lloyd PG, Yang HT, Terjung RL. Exercise training and peripheral arterial disease. Compr Physiol. 2012 Oct;2(4):2933-3017. doi: 10.1002/cphy.c110065
Open DOI Search in Google Scholar Back to article
Hiatt WR, Armstrong EJ, Larson CJ, Brass EP. Pathogenesis of the limb manifestations and exercise limitations in peripheral artery disease. Circ Res. 2015 Apr 24;116(9):1527-39. doi: 10.1161/CIRCRESAHA.116.303566
Open DOI Search in Google Scholar Back to article
Annex BH, Cooke JP. New Directions in Therapeutic Angiogenesis and Arteriogenesis in Peripheral Arterial Disease. Circ Res. 2021 Jun 11;128(12):1944-57. doi: 10.1161/CIRCRESAHA.121.318266
Open DOI Search in Google Scholar Back to article
Hackler EL 3rd, Hamburg NM, White Solaru KT. Racial and Ethnic Disparities in Peripheral Artery Disease. Circ Res. 2021 Jun 11;128(12):1913-26. doi: 10.1161/CIRCRESAHA.121.318243
Open DOI Search in Google Scholar Back to article
StatPearls [Internet]. Bethesda, MD: National Library of Medicine; c2023. Zemaitis MR, Boll JM, Dreyer MA. Peripheral Arterial Disease; 2023 May 23 [cited 2023 Nov 6]. Available from: https://www.ncbi.nlm.nih.gov/books/NBK430745/
Search in Google Scholar Back to article
Bonaca MP, Hamburg NM, Creager MA. Contemporary Medical Management of Peripheral Artery Disease. Circ Res. 2021 Jun 11;128(12):1868-1884. doi: 10.1161/CIRCRESAHA.121.318258
Open DOI Search in Google Scholar Back to article
Biswas MP, Capell WH, McDermott MM, et al. Exercise Training and Revascularization in the Management of Symptomatic Peripheral Artery Disease. JACC Basic Transl Sci. 2021;6(2):174-88. doi: 10.1016/j.jacbts.2020.08.012
Open DOI Search in Google Scholar Back to article
McDermott MM, dayanidhi S, Kosmac K, et al. Walking Exercise Therapy Effects on Lower Extremity Skeletal Muscle in Peripheral Artery Disease. Circ Res. 2021 Jun 11;128(12):1851-67. doi: 10.1161/CIRCRESAHA.121.318242
Open DOI Search in Google Scholar Back to article
Yang HT, Prior BM, Lloyd PG, et al. Training-induced vascular adaptations to ischemic muscle. J Physiol Pharmacol. 2008 Dec;59(Suppl 7):57-70. PMID: 19258657
Search in Google Scholar Back to article
Olver TD, Ferguson BS, Laughlin MH. Molecular Mechanisms for Exercise Training-Induced Changes in Vascular Structure and Function: Skeletal Muscle, Cardiac Muscle, and the Brain. Prog Mol Biol Transl Sci. 2015;135:227-57. doi: 10.1016/bs.pmbts.2015.07.017
Open DOI Search in Google Scholar Back to article
Ribeiro F, Ribeiro IP, Alves AJ, et al. Effects of exercise training on endothelial progenitor cells in cardiovascular disease: a systematic review. Am J Phys Med Rehabil. 2013 Nov;92(11):1020-30. doi: 10.1097/PHM.0b013e31829b4c4f
Open DOI Search in Google Scholar Back to article
Ross MD. Endothelial Regenerative Capacity and Aging: Influence of Diet, Exercise and Obesity. Curr Cardiol Rev. 2018;14(4):233-44. doi: 10.2174/1573403X14666180726112303
Open DOI Search in Google Scholar Back to article
Gratl A, Wipper S, Frese JP, Raude B, Greiner A, Pesta D. The Role of Mitochondrial Function in Peripheral Arterial Disease: Insights from Translational Studies. Int J Mol Sci. 2021 Aug 6;22(16):8478. doi: 10.3390/ijms2216847824.
Open DOI Search in Google Scholar Back to article
Gorski T, De Bock K. Metabolic regulation of exercise-induced angiogenesis. Vasc Biol. 2019 Mar 11;1(1):H1-H8. doi: 10.1530/VB-19-0008
Open DOI Search in Google Scholar Back to article
Haas TL, Nwadozi E. Regulation of skeletal muscle capillary growth in exercise and disease. Appl Physiol Nutr Metab. 2015 Dec;40(12):1221-32. doi: 10.1139/apnm-2015-0336
Open DOI Search in Google Scholar Back to article
Evans RM, Mangelsdorf DJ. Nuclear Receptors, RXR, and the Big Bang. Cell. 2014 Mar 27;157(1):255-66. doi: 10.1016/j.cell.2014.03.012
Open DOI Search in Google Scholar Back to article
Mangelsdorf DJ, Evans RM. The RXR heterodimers and orphan receptors. Cell. 1995 Dec 15;83(6):841-50. doi: 10.1016/0092-8674(95)90200-7
Open DOI Search in Google Scholar Back to article
Mangelsdorf DJ, Thummel C, Beato M, et al. The nuclear receptor superfamily: the second decade. Cell. 1995 Dec 15;83(6):835-9. doi: 10.1016/0092-8674(95)90199-x
Open DOI Search in Google Scholar Back to article
Mullican SE, Dispirito JR, Lazar MA. The orphan nuclear receptors at their 25-year reunion. J Mol Endocrinol. 2013 Nov 26;51(3):T115-40. doi: 10.1530/JME-13-0212
Open DOI Search in Google Scholar Back to article
Arany Z, Foo SY, Ma Y, et al. HIF-independent regulation of VEGF and angiogenesis by the transcriptional coactivator PGC-1alpha. Nature. 2008 Feb 21;451(7181):1008-12. doi: 10.1038/nature06613
Open DOI Search in Google Scholar Back to article
Rowe GC, Jang C, Patten IS, Arany Z. PGC-1beta regulates angiogenesis in skeletal muscle. Am J Physiol Endocrinol Metab. 2011 Jul;301(1):E155-63. doi: 10.1152/ajpendo.00681.2010
Open DOI Search in Google Scholar Back to article
Matsakas A, Yadav V, Lorca S, Evans RM, Narkar VA. Revascularization of ischemic skeletal muscle by estrogen-related receptor-gamma. Circ Res. 2012 Apr 13;110(8):1087-96. doi: 10.1161/CIRCRESAHA.112.266478
Open DOI Search in Google Scholar Back to article
Sopariwala DH, Likhite N, Pei G, et al. Estrogen-related receptor alpha is involved in angiogenesis and skeletal muscle revascularization in hindlimb ischemia. FASEB J. 2021 May;35(5):e21480. doi: 10.1096/fj.202001794RR
Open DOI Search in Google Scholar Back to article
Badin PM, Vila IK, Sopariwala DH, et al. Exercise-like effects by Estrogen-related receptor-gamma in muscle do not prevent insulin resistance in db/db mice. Sci Rep. 2016 May 25;6:26442. doi: 10.1038/srep26442
Open DOI Search in Google Scholar Back to article
Sopariwala DH, Rios AS, Park MK, Song MS, Kumar A, Narkar VA. Estrogen-related receptor alpha is an AMPK-regulated factor that promotes ischemic muscle revascularization and recovery in diet-induced obese mice. FASEB Bioadv. 2022 Jun 22;4(9):602-18. doi: 10.1096/fba.2022-00015
Open DOI Search in Google Scholar Back to article
Sopariwala DH, Rios AS, Pei G, et al. Innately expressed estrogen-related receptors in the skeletal muscle are indispensable for exercise fitness. FASEB J. 2023 Feb;37(2):e22727. doi: 10.1096/fj.202201518R
Open DOI Search in Google Scholar Back to article
Cartoni R, Leger B, Hock MB, et al. Mitofusins 1/2 and ERRalpha expression are increased in human skeletal muscle after physical exercise. J Physiol. 2005 Aug 15;567(Pt 1):349-58. doi: 10.1113/jphysiol.2005.092031
Open DOI Search in Google Scholar Back to article
Narkar VA, Fan W, Downes M, et al. Exercise and PGC-1alpha-independent synchronization of type I muscle metabolism and vasculature by ERRgamma. Cell Metab. 2011 Mar 2;13(3):283-93. doi: 10.1016/j.cmet.2011.01.019
Open DOI Search in Google Scholar Back to article
Rangwala SM, Wang X, Calvo JA, et al. Estrogen-related receptor gamma is a key regulator of muscle mitochondrial activity and oxidative capacity. J Biol Chem. 2010 Jul 16;285(29):22619-29. doi: 10.1074/jbc.M110.125401
Open DOI Search in Google Scholar Back to article
Chinsomboon J, Ruas J, Gupta RK, et al. The transcriptional coactivator PGC-1alpha mediates exercise-induced angiogenesis in skeletal muscle. Proc Natl Acad Sci U S A. 2009 Dec 15;106(50):21401-6. doi: 10.1073/pnas.0909131106
Open DOI Search in Google Scholar Back to article
Sopariwala DH, Rios AS, Saley A, Kumar A, Narkar VA. Estrogen-Related Receptor Gamma Gene Therapy Promotes Therapeutic Angiogenesis and Muscle Recovery in Preclinical Model of PAD. J Am Heart Assoc. 2023 Aug 15;12(16):e028880. doi: 10.1161/JAHA.122.028880
Open DOI Search in Google Scholar Back to article
Ashoff A, Qadri F, Eggers R, Johren O, Raasch W, Dendorfer A. Pioglitazone prevents capillary rarefaction in streptozotocin-diabetic rats independently of glucose control and vascular endothelial growth factor expression. J Vasc Res. 2012;49(3):260-6. doi: 10.1159/000335214
Open DOI Search in Google Scholar Back to article
Biscetti F, Pecorini G, Arena V, et al. Cilostazol improves the response to ischemia in diabetic mice by a mechanism dependent on PPARgamma. Mol Cell Endocrinol. 2013 Dec 5;381(1-2):80-7. doi: 10.1016/j.mce.2013.07.011
Open DOI Search in Google Scholar Back to article
Biscetti F, Straface G, Arena V, et al. Pioglitazone enhances collateral blood flow in ischemic hindlimb of diabetic mice through an Akt-dependent VEGF-mediated mechanism, regardless of PPARgamma stimulation. Cardiovasc Diabetol. 2009 Sep 8;8:49. doi: 10.1186/1475-2840-8-49
Open DOI Search in Google Scholar Back to article
Gaudel C, Schwartz C, Giordano C, Abumrad NA, Grimaldi PA. Pharmacological activation of PPARbeta promotes rapid and calcineurin-dependent fiber remodeling and angiogenesis in mouse skeletal muscle. Am J Physiol Endocrinol Metab. 2008 Aug;295(2):E297-304. doi: 10.1152/ajpendo.00581.2007
Open DOI Search in Google Scholar Back to article
Khazaei M, Salehi E, Rashidi B, Javanmard SH, Fallahzadeh AR. Role of peroxisome proliferator-activated receptor beta agonist on angiogenesis in hindlimb ischemic diabetic rats. J Diabetes Complications. 2012 Mar-Apr;26(2):137-40. doi: 10.1016/j.jdiacomp.2012.02.005
Open DOI Search in Google Scholar Back to article
Li P, Shibata R, Maruyama S, et al. Fenofibrate promotes ischemia-induced revascularization through the adiponectin-dependent pathway. Am J Physiol Endocrinol Metab. 2010 Oct;299(4):E560-6. doi: 10.1152/ajpendo.00284.2010
Open DOI Search in Google Scholar Back to article
Salehi E, Khazaei M, Rashidi B. Role of fenofibrate in restoring angiogenesis in diabetic and control hind limb ischemic rats. Gen Physiol Biophys. 2012 Sep;31(3):255-60. doi: 10.4149/gpb_2012_033
Open DOI Search in Google Scholar Back to article
Narkar VA, Downes M, Yu RT, et al. AMPK and PPARdelta agonists are exercise mimetics. Cell. 2008 Aug 8;134(3):405-15. doi: 10.1016/j.cell.2008.06.051
Open DOI Search in Google Scholar Back to article
Han JK, Lee HS, Yang HM, et al. Peroxisome proliferator-activated receptor-delta agonist enhances vasculogenesis by regulating endothelial progenitor cells through genomic and nongenomic activations of the phosphatidylinositol 3-kinase/Akt pathway. Circulation. 2008 Sep 2;118(10):1021-33. doi: 10.1161/CIRCULATIONAHA.108.777169
Open DOI Search in Google Scholar Back to article
Huang PH, Sata M, Nishimatsu H, Sumi M, Hirata Y, Nagai R. Pioglitazone ameliorates endothelial dysfunction and restores ischemia-induced angiogenesis in diabetic mice. Biomed Pharmacother. 2008 Jan;62(1):46-52. doi: 10.1016/j.biopha.2007.06.014
Open DOI Search in Google Scholar Back to article
Wu Y, Tang X, Lee S, et al. Endothelial PPARdelta facilitates the post-ischemic vascular repair through interaction with HIF1alpha. Theranostics. 2022 Jan 24;12(4):1855-69. doi: 10.7150/thno.69017
Open DOI Search in Google Scholar Back to article
Luquet S, Lopez-Soriano J, Holst D, et al. Peroxisome proliferator-activated receptor delta controls muscle development and oxidative capability. FASEB J. 2003 Dec;17(15):2299-301. doi: 10.1096/fj.03-0269fje
Open DOI Search in Google Scholar Back to article
Schuler M, Ali F, Chambon C, et al. PGC1alpha expression is controlled in skeletal muscles by PPARbeta, whose ablation results in fiber-type switching, obesity, and type 2 diabetes. Cell Metab. 2006 Nov;4(5):407-14. doi: 10.1016/j.cmet.2006.10.003
Open DOI Search in Google Scholar Back to article
Wang YX, Zhang CL, Yu RT, et al. Regulation of muscle fiber type and running endurance by PPARdelta. PLoS Biol. 2004 Oct;2(10):e294. doi: 10.1371/journal.pbio.0020294
Open DOI Search in Google Scholar Back to article
Fan W, Waizenegger W, Lin CS, et al. PPARdelta Promotes Running Endurance by Preserving Glucose. Cell Metab. 2017 May 2;25(5):1186-93 e4. doi: 10.1016/j.cmet.2017.04.006
Open DOI Search in Google Scholar Back to article
Lam YT, Lecce L, Yuen SC, et al. Androgens Ameliorate Impaired Ischemia-Induced Neovascularization Due to Aging in Male Mice. Endocrinology. 2019 May 1;160(5):1137-49. doi: 10.1210/en.2018-00951
Open DOI Search in Google Scholar Back to article
Yoshida S, Aihara K, Ikeda Y, et al. Androgen receptor promotes sex-independent angiogenesis in response to ischemia and is required for activation of vascular endothelial growth factor receptor signaling. Circulation. 2013 Jul 2;128(1):60-71. doi: 10.1161/CIRCULATIONAHA.113.001533
Open DOI Search in Google Scholar Back to article
Lam YT, Lecce L, Yuen GSC, Wise SG, Handelsman DJ, Ng MKC. Androgen action augments ischemia-induced, bone marrow progenitor cell-mediated vasculogenesis. Int J Biol Sci. 2018 Nov 2;14(14):1985-92. doi: 10.7150/ijbs.27378
Open DOI Search in Google Scholar Back to article
Kyriakides ZS, Petinakis P, Kaklamanis L, et al. Intramuscular administration of estrogen may promote angiogenesis and perfusion in a rabbit model of chronic limb ischemia. Cardiovasc Res. 2001 Feb 16;49(3):626-33. doi: 10.1016/s0008-6363(00)00199-1.
Open DOI Search in Google Scholar Back to article
Matsubara K, Harada H, Ando N, et al. Estrogen deficiency attenuates neovascularization in a murine model of hindlimb ischemia. J Surg Res. 2012 Dec;178(2):1022-8. doi: 10.1016/j.jss.2012.04.067
Open DOI Search in Google Scholar Back to article
Ruifrok WP, de Boer RA, Iwakura A, et al. Estradiol-induced, endothelial progenitor cell-mediated neovascularization in male mice with hind-limb ischemia. Vasc Med. 2009 Feb;14(1):29-36. doi: 10.1177/1358863X08096666
Open DOI Search in Google Scholar Back to article
Chen L, Yang Y, Zhang L, et al. Aucubin promotes angiogenesis via estrogen receptor beta in a mouse model of hindlimb ischemia. J Steroid Biochem Mol Biol. 2017 Sep;172:149-59. doi: 10.1016/j.jsbmb.2017.07.007
Open DOI Search in Google Scholar Back to article
Rowe GC, Raghuram S, Jang C, et al. PGC-1alpha induces SPP1 to activate macrophages and orchestrate functional angiogenesis in skeletal muscle. Circ Res. 2014 Aug 15;115(5):504-17. doi: 10.1161/CIRCRESAHA.115.303829
Open DOI Search in Google Scholar Back to article
Thom R, Rowe GC, Jang C, Safdar A, Arany Z. Hypoxic induction of vascular endothelial growth factor (VEGF) and angiogenesis in muscle by truncated peroxisome proliferator-activated receptor gamma coactivator (PGC)-1alpha. J Biol Chem. 2014 Mar 28;289(13):8810-7. doi: 10.1074/jbc.M114.554394
Open DOI Search in Google Scholar Back to article
Yadav V, Matsakas A, Lorca S, Narkar VA. PGC1beta activates an antiangiogenic program to repress neoangiogenesis in muscle ischemia. Cell Rep. 2014 Aug 7;8(3):783-97. doi: 10.1016/j.celrep.2014.06.040
Open DOI Search in Google Scholar Back to article
Schnyder S, Kupr B, Handschin C. Coregulator-mediated control of skeletal muscle plasticity - A mini-review. Biochimie. 2017 May;136:49-54. doi: 10.1016/j.biochi.2016.12.011
Open DOI Search in Google Scholar Back to article
Qian FY, Li ZL, Guo YD, et al. Hypoxia-inducible factor-prolyl hydroxylase inhibitor ameliorates myopathy in a mouse model of chronic kidney disease. Am J Physiol Renal Physiol. 2019 Nov 1;317(5):F1265-F73. doi: 10.1152/ajprenal.00260.2019
Open DOI Search in Google Scholar Back to article
Schellinger IN, Cordasic N, Panesar J, et al. Hypoxia inducible factor stabilization improves defective ischemia-induced angiogenesis in a rodent model of chronic kidney disease. Kidney Int. 2017 Mar;91(3):616-27. doi: 10.1016/j.kint.2016.09.028
Open DOI Search in Google Scholar Back to article
Rishi MT, Selvaraju V, Thirunavukkarasu M, et al. Deletion of prolyl hydroxylase domain proteins (PHD1, PHD3) stabilizes hypoxia inducible factor-1 alpha, promotes neovascularization, and improves perfusion in a murine model of hind-limb ischemia. Microvasc Res. 2015 Jan;97:181-8. doi: 10.1016/j.mvr.2014.10.009
Open DOI Search in Google Scholar Back to article
Sahara M, Sata M, Morita T, Nakajima T, Hirata Y, Nagai R. A phosphodiesterase-5 inhibitor vardenafil enhances angiogenesis through a protein kinase G-dependent hypoxia-inducible factor-1/vascular endothelial growth factor pathway. Arterioscler Thromb Vasc Biol. 2010 Jul;30(7):1315-24. doi: 10.1161/ATVBAHA.109.201327
Open DOI Search in Google Scholar Back to article
Niemi H, Honkonen K, Korpisalo P, et al. HIF-1alpha and HIF-2alpha induce angiogenesis and improve muscle energy recovery. Eur J Clin Invest. 2014 Oct;44(10):989-99. doi: 10.1111/eci.12333
Open DOI Search in Google Scholar Back to article
Mason SD, Howlett RA, Kim MJ, et al. Loss of skeletal muscle HIF-1alpha results in altered exercise endurance. PLoS Biol. 2004 Oct;2(10):e288. doi: 10.1371/journal.pbio.0020288
Open DOI Search in Google Scholar Back to article
Yang X, Yang S, Wang C, Kuang S. The hypoxia-inducible factors HIF1alpha and HIF2alpha are dispensable for embryonic muscle development but essential for postnatal muscle regeneration. J Biol Chem. 2017 Apr 7;292(14):5981-91. doi: 10.1074/jbc.M116.756312
Open DOI Search in Google Scholar Back to article
Badin PM, Sopariwala DH, Lorca S, Narkar VA. Muscle Arnt/Hif1beta Is Dispensable in Myofiber Type Determination, Vascularization and Insulin Sensitivity. PLoS One. 2016 Dec 22;11(12):e0168457. doi: 10.1371/journal.pone.0168457
Open DOI Search in Google Scholar Back to article
Balestrieri N, Palzkill V, Pass C, et al. Activation of the Aryl Hydrocarbon Receptor in Muscle Exacerbates Ischemic Pathology in Chronic Kidney Disease. Circ Res. 2023 Jul 7;133(2):158-76. doi: 10.1161/CIRCRESAHA.123.322875
Open DOI Search in Google Scholar Back to article
Palzkill VR, Tan J, Yang Q, Morcos J, Laitano O, Ryan TE. Activation of the Aryl Hydrocarbon Receptor in Endothelial Cells Impairs Ischemic Angiogenesis in Chronic Kidney Disease. bioRxiv. Preprint. 2023 Jul 26. doi: 10.1101/2023.07.24.550410
Open DOI Search in Google Scholar Back to article
Thome T, Miguez K, Willms AJ, et al. Chronic aryl hydrocarbon receptor activity phenocopies smoking-induced skeletal muscle impairment. J Cachexia Sarcopenia Muscle. 2022 Feb;13(1):589-604. doi: 10.1002/jcsm.12826
Open DOI Search in Google Scholar Back to article
Zou C, Yu S, Xu Z, et al. ERRalpha augments HIF-1 signalling by directly interacting with HIF-1alpha in normoxic and hypoxic prostate cancer cells. J Pathol. 2014 May;233(1):61-73. doi: 10.1002/path.4329
Open DOI Search in Google Scholar Back to article
Su P, Yu L, Mao X, Sun P. Role of HIF-1alpha/ERRalpha in Enhancing Cancer Cell Metabolism and Promoting Resistance of Endometrial Cancer Cells to Pyroptosis. Front Oncol. 2022 Jun 21;12:881252. doi: 10.3389/fonc.2022.881252
Open DOI Search in Google Scholar Back to article
Spaulding HR, Yan Z. AMPK and the Adaptation to Exercise. Annu Rev Physiol. 2022 Feb 10;84:209-27. doi: 10.1146/annurev-physiol-060721-095517
Open DOI Search in Google Scholar Back to article
Zhu H, Zhang M, Liu Z, et al. AMP-Activated Protein Kinase alpha1 in Macrophages Promotes Collateral Remodeling and Arteriogenesis in Mice In Vivo. Arterioscler Thromb Vasc Biol. 2016 Sep;36(9):1868-78. doi: 10.1161/ATVBAHA.116.307743
Open DOI Search in Google Scholar Back to article
Zwetsloot KA, Westerkamp LM, Holmes BF, Gavin TP. AMPK regulates basal skeletal muscle capillarization and VEGF expression, but is not necessary for the angiogenic response to exercise. J Physiol. 2008 Dec 15;586(24):6021-35. doi: 10.1113/jphysiol.2008.159871
Open DOI Search in Google Scholar Back to article
Ouchi N, Shibata R, Walsh K. AMP-activated protein kinase signaling stimulates VEGF expression and angiogenesis in skeletal muscle. Circ Res. 2005 Apr 29;96(8):838-46. doi: 10.1161/01.RES.0000163633.10240.3b
Open DOI Search in Google Scholar Back to article
Takahashi N, Shibata R, Ouchi N, Sugimoto M, Murohara T, Komori K. Metformin stimulates ischemia-induced revascularization through an eNOS dependent pathway in the ischemic hindlimb mice model. J Vasc Surg. 2015 Feb;61(2):489-96. doi: 10.1016/j.jvs.2013.09.061
Open DOI Search in Google Scholar Back to article
Egan B, Zierath JR. Exercise metabolism and the molecular regulation of skeletal muscle adaptation. Cell Metab. 2013 Feb 5;17(2):162-84. doi: 10.1016/j.cmet.2012.12.012
Open DOI Search in Google Scholar Back to article
Smith JAB, Murach KA, Dyar KA, Zierath JR. Exercise metabolism and adaptation in skeletal muscle. Nat Rev Mol Cell Biol. 2023 Sep;24(9):607-32. doi: 10.1038/s41580-023-00606-x
Open DOI Search in Google Scholar Back to article
Plutzky J. The PPAR-RXR transcriptional complex in the vasculature: energy in the balance. Circ Res. 2011 Apr 15;108(8):1002-16. doi: 10.1161/CIRCRESAHA.110.226860
Open DOI Search in Google Scholar Back to article
Salt IP, Hardie DG. AMP-Activated Protein Kinase: An Ubiquitous Signaling Pathway With Key Roles in the Cardiovascular System. Circ Res. 2017 May 26;120(11):1825-41. doi: 10.1161/CIRCRESAHA.117.309633
Open DOI Search in Google Scholar Back to article
Hart CA, Tsui J, Khanna A, Abraham DJ, Baker DM. Stem cells of the lower limb: their role and potential in management of critical limb ischemia. Exp Biol Med (Maywood). 2013 Oct;238(10):1118-26. doi: 10.1177/1535370213503275
Open DOI Search in Google Scholar Back to article
Landers-Ramos RQ, Sapp RM, Shill DD, Hagberg JM, Prior SJ. Exercise and Cardiovascular Progenitor Cells. Compr Physiol. 2019 Mar 14;9(2):767-97. doi: 10.1002/cphy.c180030
Open DOI Search in Google Scholar Back to article
van Doorslaer de Ten Ryen S, Francaux M, Deldicque L. Regulation of satellite cells by exercise in hypoxic conditions: a narrative review. Eur J Appl Physiol. 2021 Jun;121(6):1531-42. doi: 10.1007/s00421-021-04641-4
Open DOI Search in Google Scholar Back to article
Qi C, Song X, Wang H, Yan Y, Liu B. The role of exercise-induced myokines in promoting angiogenesis. Front Physiol. 2022 Aug 26;13:981577. doi: 10.3389/fphys.2022.981577
Open DOI Search in Google Scholar Back to article
Das A, Huang GX, Bonkowski MS, et al. Impairment of an Endothelial NAD(+)-H(2)S Signaling Network Is a Reversible Cause of Vascular Aging. Cell. 2018 Mar 22;173(1):74-89 e20. doi: 10.1016/j.cell.2018.02.008
Open DOI Search in Google Scholar Back to article
Porporato PE, Payen VL, De Saedeleer CJ, et al. Lactate stimulates angiogenesis and accelerates the healing of superficial and ischemic wounds in mice. Angiogenesis. 2012 Dec;15(4):581-92. doi: 10.1007/s10456-012-9282-0
Open DOI Search in Google Scholar Back to article
Potente M, Ghaeni L, Baldessari D, et al. SIRT1 controls endothelial angiogenic functions during vascular growth. Genes Dev. 2007 Oct 15;21(20):2644-58. doi: 10.1101/gad.435107
Open DOI Search in Google Scholar Back to article
Zhang J, Muri J, Fitzgerald G, et al. Endothelial Lactate Controls Muscle Regeneration from Ischemia by Inducing M2-like Macrophage Polarization. Cell Metab. 2020 Jun 2;31(6):1136-53 e7. doi: 10.1016/j.cmet.2020.05.004
Open DOI Search in Google Scholar Back to article
Kargl CK, Sullivan BP, Middleton D, et al. Peroxisome proliferator-activated receptor gamma coactivator 1-alpha overexpression improves angiogenic signalling potential of skeletal muscle-derived extracellular vesicles. Exp Physiol. 2023 Feb;108(2):240-52. doi: 10.1113/EP090874
Open DOI Search in Google Scholar Back to article
Nie Y, Sato Y, Garner RT, et al. Skeletal muscle-derived exosomes regulate endothelial cell functions via reactive oxygen species-activated nuclear factor-kappaB signalling. Exp Physiol. 2019 Aug;104(8):1262-73. doi: 10.1113/EP087396
Open DOI Search in Google Scholar Back to article

Authors

Metrics

Articles in this issue

DOI: https://doi.org/10.14797/mdcvj.1304 | Journal eISSN: 1947-6108

Journal RSS Feed

Language: English

Page range: 58 - 68

Submitted on: Oct 19, 2023

Accepted on: Oct 26, 2023

Published on: Nov 16, 2023

Published by: Houston Methodist DeBakey Heart & Vascular Center

In partnership with: Paradigm Publishing Services

Keywords:

exercise,

angiogenesis,

limb ischemia,

peripheral artery disease

© 2023 Vihang A. Narkar, published by Houston Methodist DeBakey Heart & Vascular Center
This work is licensed under the Creative Commons Attribution-NonCommercial 4.0 License.

Volume 19 (2023): Issue 5