Obstruction of Small Arterioles in Patients with Critical Limb Ischemia due to Partial Endothelial-to-Mesenchymal Transition

iScience - Tập 23 - Trang 101251 - 2020
Jacqueline Chevalier1,2, Hao Yin1, John-Michael Arpino1,2, Caroline O'Neil1, Zengxuan Nong1, Kevin J. Gilmore3,4, Jason J. Lee1,5,2, Emma Prescott1,2, Matthew Hewak3, Charles L. Rice3,4, Luc Dubois6, Adam H. Power6, Douglas W. Hamilton3, J. Geoffrey Pickering1,5,2,7
1Robarts Research Institute, Schulich School of Medicine and Dentistry, Western University, London, Canada
2Department of Medical Biophysics, Schulich School of Medicine and Dentistry, Western University, London, Canada
3Department of Anatomy and Cell Biology, Schulich School of Medicine and Dentistry, Western University, London, Canada
4School of Kinesiology, Faculty of Health Sciences, Western University, London, Canada
5Department of Medicine, Schulich School of Medicine and Dentistry, Western University, London, Canada
6Department of Surgery, Schulich School of Medicine and Dentistry, Western University, London, Canada
7Department of Biochemistry, Schulich School of Medicine and Dentistry, Western University, London, Canada

Tài liệu tham khảo

Allen, 2009, Plasma nitrite response and arterial reactivity differentiate vascular health and performance, Nitric Oxide, 20, 231, 10.1016/j.niox.2009.01.002 Almasri, 2019, A systematic review and meta-analysis of revascularization outcomes of infrainguinal chronic limb-threatening ischemia, J. Vasc. Surg., 69, 126S, 10.1016/j.jvs.2018.01.071 Annex, 2013, Therapeutic angiogenesis for critical limb ischaemia, Nat. Rev. Cardiol., 10, 387, 10.1038/nrcardio.2013.70 Arpino, 2017, Four-dimensional microvascular analysis reveals that regenerative angiogenesis in ischemic muscle produces a flawed microcirculation, Circ. Res., 120, 1453, 10.1161/CIRCRESAHA.116.310535 Balint, 2019, Seno-destructive smooth muscle cells in the ascending aorta of patients with bicuspid aortic valve disease, EBioMedicine, 43, 54, 10.1016/j.ebiom.2019.04.060 Barbee, 1994, Shear stress-induced reorganization of the surface topography of living endothelial cells imaged by atomic force microscopy, Circ. Res., 74, 163, 10.1161/01.RES.74.1.163 Basile, 1996, Increased transforming growth factor-beta 1 expression in regenerating rat renal tubules following ischemic injury, Am. J. Physiol., 270, F500 Bronner-Fraser, 1992, Effects of antibodies against N-cadherin and N-CAM on the cranial neural crest and neural tube, Dev. Biol., 153, 291, 10.1016/0012-1606(92)90114-V Chu, 2006, Prototypical type I E-cadherin and type II cadherin-7 mediate very distinct adhesiveness through their extracellular domains, J. Biol. Chem., 281, 2901, 10.1074/jbc.M506185200 Clyne, 1985, Calf muscle adaptation to peripheral vascular disease, Cardiovasc. Res., 19, 507, 10.1093/cvr/19.8.507 Coats, 2000, Differential responses in human subcutaneous and skeletal muscle vascular beds to critical limb ischaemia, Eur. J. Vasc. Endovasc. Surg., 19, 387, 10.1053/ejvs.1999.1023 Conrad, 1967, Large and small artery occlusion in diabetics and nondiabetics with severe vascular disease, Circulation, 36, 83, 10.1161/01.CIR.36.1.83 Conrad, 1968, Abnormalities of the digital vasculature as related to ulceration and gangrene, Circulation, 38, 568, 10.1161/01.CIR.38.3.568 Cooley, 2014, TGF-beta signaling mediates endothelial-to-mesenchymal transition (EndMT) during vein graft remodeling, Sci. Transl. Med., 6, 227ra234, 10.1126/scitranslmed.3006927 Dejana, 2017, The molecular basis of endothelial cell plasticity, Nat. Commun., 8, 14361, 10.1038/ncomms14361 Evrard, 2016, Endothelial to mesenchymal transition is common in atherosclerotic lesions and is associated with plaque instability, Nat. Commun., 7, 11853, 10.1038/ncomms11853 Farber, 2016, The current state of critical limb ischemia: a systematic review, JAMA Surg., 151, 1070, 10.1001/jamasurg.2016.2018 Feihl, 2008, Hypertension and microvascular remodelling, Cardiovasc. Res., 78, 274, 10.1093/cvr/cvn022 Frontini, 2011, Fibroblast growth factor 9 delivery during angiogenesis produces durable, vasoresponsive microvessels wrapped by smooth muscle cells, Nat. Biotechnol., 29, 421, 10.1038/nbt.1845 Gerhardt, 2000, N-cadherin mediates pericytic-endothelial interaction during brain angiogenesis in the chicken, Dev. Dyn., 218, 472, 10.1002/1097-0177(200007)218:3<472::AID-DVDY1008>3.0.CO;2-# Gilbertson-Beadling, 1993, A potential role for N-cadherin in mediating endothelial cell-smooth muscle cell interactions in the rat vasculature, Lab. Invest., 69, 203 Ha, 2016, Transforming growth factor-beta 1 produced by vascular smooth muscle cells predicts fibrosis in the gastrocnemius of patients with peripheral artery disease, J. Transl. Med., 14, 39, 10.1186/s12967-016-0790-3 Hammarsten, 1980, Capillary supply and muscle fibre types in patients with intermittent claudication: relationships between morphology and metabolism, Eur. J. Clin. Invest., 10, 301, 10.1111/j.1365-2362.1980.tb00037.x Hillier, 1999, Altered small artery morphology and reactivity in critical limb ischaemia, Clin. Sci. (Lond.), 96, 155, 10.1042/cs0960155 Ho, 2006, Increased endogenous angiogenic response and hypoxia-inducible factor-1alpha in human critical limb ischemia, J. Vasc. Surg., 43, 125, 10.1016/j.jvs.2005.08.042 Isakson, 2008, Incidence of protein on actin bridges between endothelium and smooth muscle in arterioles demonstrates heterogeneous connexin expression and phosphorylation, Am. J. Physiol. Heart Circ. Physiol., 294, H2898, 10.1152/ajpheart.91488.2007 Kovacic, 2019, Endothelial to mesenchymal transition in cardiovascular disease: JACC State-of-the-Art Review, J. Am. Coll. Cardiol., 73, 190, 10.1016/j.jacc.2018.09.089 Laurent, 2015, The structural factor of hypertension: large and small artery alterations, Circ. Res., 116, 1007, 10.1161/CIRCRESAHA.116.303596 Lee, 2004, Temporal patterns of gene expression after acute hindlimb ischemia in mice: insights into the genomic program for collateral vessel development, J. Am. Coll. Cardiol., 43, 474, 10.1016/j.jacc.2003.09.033 Ma, 2014, Arch. Phys. Med. Rehabil., 95, 986, 10.1016/j.apmr.2013.10.032 Man, 2019, The therapeutic potential of targeting the endothelial-to-mesenchymal transition, Angiogenesis, 22, 3, 10.1007/s10456-018-9639-0 McGuigan, 2001, Muscle fiber characteristics in patients with peripheral arterial disease, Med. Sci. Sports Exerc., 33, 2016, 10.1097/00005768-200112000-00007 Nagai, 2018, Downregulation of ERG and FLI1 expression in endothelial cells triggers endothelial-to-mesenchymal transition, PLoS Genet., 14, e1007826, 10.1371/journal.pgen.1007826 Narula, 2018, Pathology of peripheral artery disease in patients with critical limb ischemia, J. Am. Coll. Cardiol., 72, 2152, 10.1016/j.jacc.2018.08.002 Navarro, 1998, Differential localization of VE- and N-cadherins in human endothelial cells: VE-cadherin competes with N-cadherin for junctional localization, J. Cell Biol., 140, 1475, 10.1083/jcb.140.6.1475 Norgren, 2007, Inter-society consensus for the management of peripheral arterial disease (TASC II), J. Vasc. Surg., 45, S5, 10.1016/j.jvs.2006.12.037 Park, 2001, Small artery remodeling is the most prevalent (earliest?) form of target organ damage in mild essential hypertension, J. Hypertens., 19, 921, 10.1097/00004872-200105000-00013 Robbins, 2011, Relationship between leg muscle capillary density and peak hyperemic blood flow with endurance capacity in peripheral artery disease, J. Appl. Physiol. (1985), 111, 81, 10.1152/japplphysiol.00141.2011 Rousso, 2012, Foxp-mediated suppression of N-cadherin regulates neuroepithelial character and progenitor maintenance in the CNS, Neuron, 74, 314, 10.1016/j.neuron.2012.02.024 Said, 2019, Fortifying angiogenesis in ischemic muscle with FGF9-loaded electrospun poly(ester amide) fibers, Adv. Healthc. Mater., 8, e1801294, 10.1002/adhm.201801294 Salomon, 1992, Extrajunctional distribution of N-cadherin in cultured human endothelial cells, J. Cell Sci., 102, 7, 10.1242/jcs.102.1.7 Sanchez-Duffhues, 2016, In brief: endothelial-to-mesenchymal transition, J. Pathol., 238, 378, 10.1002/path.4653 Saygin, 2019, Microvascular involvement in systemic sclerosis and systemic lupus erythematosus, Microcirculation, 26, e12440, 10.1111/micc.12440 Shishehbor, 2016, Critical limb ischemia: an expert statement, J. Am. Coll. Cardiol., 68, 2002, 10.1016/j.jacc.2016.04.071 Springer, 2013, Thrombosis in vasculitis, Curr. Opin. Rheumatol., 25, 19, 10.1097/BOR.0b013e32835ad3ca Tsui, 2002, Potential role of endothelin 1 in ischaemia-induced angiogenesis in critical leg ischaemia, Br. J. Surg., 89, 741, 10.1046/j.1365-2168.2002.02100.x Vafaie, 2014, Collagenase-resistant collagen promotes mouse aging and vascular cell senescence, Aging Cell, 13, 121, 10.1111/acel.12155 Wang, 2013, Endothelial cell sensing of flow direction, Arterioscler. Thromb. Vasc. Biol., 33, 2130, 10.1161/ATVBAHA.113.301826 Welch-Reardon, 2015, A role for partial endothelial-mesenchymal transitions in angiogenesis?, Arterioscler. Thromb. Vasc. Biol., 35, 303, 10.1161/ATVBAHA.114.303220 Wheelock, 2008, Cadherin switching, J. Cell Sci., 121, 727, 10.1242/jcs.000455 Whittaker, 1994, Quantitative assessment of myocardial collagen with picrosirius red staining and circularly polarized light, Basic Res. Cardiol., 89, 397, 10.1007/BF00788278 Yamashita, 1999, Biphasic expression of TGF-beta1 mRNA in the rat brain following permanent occlusion of the middle cerebral artery, Brain Res., 836, 139, 10.1016/S0006-8993(99)01626-1 Yin, 2015, Fibroblast growth factor 9 imparts hierarchy and vasoreactivity to the microcirculation of renal tumors and suppresses metastases, J. Biol. Chem., 290, 22127, 10.1074/jbc.M115.652222