Cited by 292Atherosclerosis and Cardiovascular DiseasesCardiovascular, Neuropeptides, and Oxidative Stress ResearchCerebrovascular and Carotid Artery Diseases

Role of Vascular Smooth Muscle Cell Plasticity and Interactions in Vessel Wall Inflammation

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Sorokin, Vitaly, Vickneson, Keeran, Kofidis, Theo, Woo, Chin Cheng, Lin, Xiao Yun, Foo, Roger, Shanahan, Catherine M.·2020·Frontiers in Immunology

Abstract

The pathobiology of atherosclerotic disease requires further elucidation to discover new approaches to address its high morbidity and mortality. To date, over 17 million cardiovascular-related deaths have been reported annually, despite a multitude of surgical and nonsurgical interventions and advances in medical therapy. Existing strategies to prevent disease progression mainly focus on management of risk factors, such as hypercholesterolemia. Even with optimum current medical therapy, recurrent cardiovascular events are not uncommon in patients with atherosclerosis, and their incidence can reach 10–15% per year. Although treatments targeting inflammation are under investigation and continue to evolve, clinical breakthroughs are possible only if we deepen our understanding of vessel wall pathobiology. Vascular smooth muscle cells (VSMCs) are one of the most abundant cells in vessel walls and have emerged as key players in disease progression. New technologies, including in situ hybridization proximity ligation assays, in vivo cell fate tracing with the CreER T2 -loxP system and single-cell sequencing technology with spatial resolution, broaden our understanding of the complex biology of these intriguing cells. Our knowledge of contractile and synthetic VSMC phenotype switching has expanded to include macrophage-like and even osteoblast-like VSMC phenotypes. An increasing body of data suggests that VSMCs have remarkable plasticity and play a key role in cell-to-cell crosstalk with endothelial cells and immune cells during the complex process of inflammation. These are cells that sense, interact with and influence the behavior of other cellular components of the vessel wall. It is now more obvious that VSMC plasticity and the ability to perform nonprofessional phagocytic functions are key phenomena maintaining the inflammatory state and senescent condition and actively interacting with different immune competent cells.

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  • Vascular smooth muscle cells perform nonprofessional phagocytosis and take part in the development of atherosclerotic plaques.

    “Vascular smooth muscle cells are able to perform nonprofessional phagocytosis and take part in the development of atherosclerotic plaques [106].”

    From MicroRNAs as Regulators of Phagocytosis (2022) · cites this paper as [106]

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  1. [1]Benjamin EJ Muntner P Alonso A Bittencourt MS Callaway CW Carson AP Heart Disease and Stroke Statistics-2019 Update: A Report From the American Heart Association. Circulation (2019) 139: e56– 528. 10.1161/CIR.0000000000000659 30700139 · DOI · Paper page
  2. [2]Libby P Buring JE Badimon L Hansson GK Deanfield J Bittencourt MS Atherosclerosis. Nat Rev Dis Primers (2019) 5: 56. 10.1038/s41572-019-0106-z 31420554 · DOI · Paper page
  3. [3]Ackers-Johnson M Talasila A Sage AP Long X Bot I Morrell NW Myocardin regulates vascular smooth muscle cell inflammatory activation and disease. Arterioscler Thromb Vasc Biol (2015) 35: 817–28. 10.1161/ATVBAHA.114.305218 PMC4390125 25614278 · DOI
  4. [4]Ridker PM Everett BM Thuren T MacFadyen JG Chang WH Ballantyne C Antiinflammatory Therapy with Canakinumab for Atherosclerotic Disease. N Engl J Med (2017) 377: 1119–31. 10.1056/NEJMoa1707914 28845751 · DOI · Paper page
  5. [5]Libby P Interleukin-1 Beta as a Target for Atherosclerosis Therapy: Biological Basis of CANTOS and Beyond. J Am Coll Cardiol (2017) 70: 2278–89. 10.1016/j.jacc.2017.09.028 PMC5687846 29073957 · DOI
  6. [6]Ilhan F Kalkanli ST Atherosclerosis and the role of immune cells. World J Clin Cases (2015) 3: 345–52. 10.12998/wjcc.v3.i4.345 PMC4391004 25879006 · DOI
  7. [7]Kashiwagi M Kitabata H Ozaki Y Imanishi T Akasaka T Fatty streak assessed by optical coherence tomography: early atherosclerosis detection. Eur Heart J Cardiovasc Imaging (2013) 14: 109. 10.1093/ehjci/jes182 22930525 · DOI
  8. [8]Mai J Virtue A Shen J Wang H Yang XF An evolving new paradigm: endothelial cells–conditional innate immune cells. J Hematol Oncol (2013) 6: 61. 10.1186/1756-8722-6-61 23965413 PMC3765446 · DOI
  9. [9]Li M Qian M Kyler K Xu J Endothelial Vascular Smooth Muscle Cells Interactions in Atherosclerosis. Front Cardiovasc Med (2018) 5: 151. 10.3389/fcvm.2018.00151 30406116 PMC6207093 · DOI
  10. [10]Castro PR Barbosa AS Pereira JM Ranfley H Felipetto M Gonçalves CAX Cellular and Molecular Heterogeneity Associated with Vessel Formation Processes. BioMed Res Int (2018) 2018: 6740408. 10.1155/2018/6740408 30406137 PMC6199857 · DOI
  11. [11]Vitiello L Spoletini I Gorini S Pontecorvo L Ferrari D Ferraro E Microvascular inflammation in atherosclerosis. IJC Metab Endocr (2014) 3: 1– 7. 10.1016/j.ijcme.2014.03.002 · DOI
  12. [12]Wang G Jacquet L Karamariti E Xu Q Origin and differentiation of vascular smooth muscle cells. J Physiol (2015) 593: 3013–30. 10.1113/JP270033 PMC4532522 25952975 · DOI
  13. [13]Allahverdian S Chaabane C Boukais K Francis GA Bochaton-Piallat ML Smooth muscle cell fate and plasticity in atherosclerosis. Cardiovasc Res (2018) 114: 540–50. 10.1093/cvr/cvy022 PMC5852505 29385543 · DOI
  14. [14]Seeberg JC Loibl M Moser F Schwegler M Büttner-Herold M Daniel C Non-professional phagocytosis: a general feature of normal tissue cells. Sci Rep (2019) 9: 11875. 10.1038/s41598-019-48370-3 31417141 PMC6695441 · DOI
  15. [15]Bennett MR Sinha S Owens GK Vascular Smooth Muscle Cells in Atherosclerosis. Circ Res (2016) 118: 692– 702. 10.1161/CIRCRESAHA.115.306361 26892967 PMC4762053 · DOI · Paper page
  16. [16]Clarke MC Figg N Maguire JJ Davenport AP Goddard M Littlewood TD Apoptosis of vascular smooth muscle cells induces features of plaque vulnerability in atherosclerosis. Nat Med (2006) 12: 1075–80. 10.1038/nm1459 16892061 · DOI
  17. [17]Silvestre-Roig C de Winther MP Weber C Daemen MJ Lutgens E Soehnlein O Atherosclerotic plaque destabilization: mechanisms, models, and therapeutic strategies. Circ Res (2014) 114: 214–26. 10.1161/CIRCRESAHA.114.302355 24385514 · DOI
  18. [18]Gomez D Baylis RA Durgin BG Newman AAC Alencar GF Mahan S Interleukin-1β promotes atheroprotective effects in advanced atherosclerotic lesions in mice. Nat Med (2018) 24: 1418–29. 10.1038/s41591-018-0124-5 PMC6130822 30038218 · DOI
  19. [19]Buenrostro JD Corces MR Lareau CA Wu B Schep AN Aryee MJ Integrated Single-Cell Analysis maps the continuous regulatory landscape of human hematopoietic differentiation. Cell (2018) 173: 1535–48. 10.1016/j.cell.2018.03.074 PMC5989727 29706549 · DOI · Paper page
  20. [20]Trigueros-Motos L González-Granado JM Cheung C Fernández P Sánchez-Cabo F Dopazo A Embryological-origin-dependent differences in homeobox expression in adult aorta: role in regional phenotypic variability and regulation of NF-kappaB activity. Arterioscler Thromb Vasc Biol (2013) 33: 1248–56. 10.1161/ATVBAHA.112.300539 23448971 · DOI
  21. [21]Cheung C Bernardo AS Trotter MW Pedersen RA Sinha S Generation of vascular smooth muscle cell subtype provide insight into embryological origin-dependant disease susceptibility. Nat Biotechnol (2012) 30: 165–73. 10.1038/nbt.2107 PMC3272383 22252507 · DOI
  22. [22]Chakraborty R Saddouk FZ Carrao AC Krause DS Greif DM Martin KA Promoters to Study Vascular Smooth Muscle. Mistaken Identity? Arterioscler Thromb Vasc Biol (2019) 39: 603–12. 10.1161/ATVBAHA.119.312449 PMC6527360 30727757 · DOI
  23. [23]Rong JX Shapiro M Trogan E Fisher EA Transdifferentiation of mouse aortic smooth muscle cells to a macrophage-like state after cholesterol loading. Proc Natl Acad Sci USA (2003) 100: 13531–6. 10.1073/pnas.1735526100 PMC263848 14581613 · DOI
  24. [24]Kovacic JC Dimmeler S Harvey RP Finkel T Aikawa E Krenning G Endothelial to Mesenchymal Transition in Cardiovascular Disease: JACC State-of-the-Art Review. J Am Coll Cardiol (2019) 73: 190– 209. 10.1016/j.jacc.2018.09.089 30654892 PMC6865825 · DOI
  25. [25]Yu H Stoneman V Clarke M Figg N Xin HB Kotlikoff M Bone Marrow-Derived Smooth Muscle-Like Cells Are Infrequent in Advanced Primary Atherosclerotic Plaques but Promote Atherosclerosis. Arterioscler Thromb Vasc Biol (2011) 31: 1291–9. 10.1161/ATVBAHA.110.218578 21372299 · DOI
  26. [26]Shankman LS Gomez D Cherepanova OA Salmon M Alencar GF Haskins RM KLF4-dependent phenotypic modulation of smooth muscle cells has a key role in atherosclerotic plaque pathogenesis. Nat Med (2015) 21: 628–37. 10.1038/nm.3866 PMC4552085 25985364 · DOI · Paper page
  27. [27]Kuro-o M Nagai R Nakahara K Katoh H Tsai RC Tsuchimochi H cDNA cloning of a myosine heavy chain isoform in embryonic smooth muscle cells and its expression during vascular development and in atherosclerosis. J Biol Chem (1991) 266: 3768–73. 1995631
  28. [28]Neuvelli P Geinoz A Benzonana G Redard M Gabbiani F Ropraz P Cellular retinol binding protein 1 is expressed by distinct subset of rat arterial smooth muscle cells in vitro and in vivo. Am J Pathol (1997) 150: 509–21. PMC1858290 9033267
  29. [30]Gomez D Swiatlowska P Owens GK Epigenetic Control of Smooth Muscle Cell Identity and Lineage Memory. Arterioscler Thromb Vasc Biol (2015) 35: 2508–16. 10.1161/ATVBAHA.115.305044 PMC4662608 26449751 · DOI
  30. [31]Yuan F Wang D Xu K Wang J Zhang Z Yang L Contribution of Vascular Cells to Neointima Formation. PLoS One (2017) 12: e0168914. 10.1371/journal.pone.0168914 28060852 PMC5218548 · DOI
  31. [32]Fernandez DM Rahman AH Fernandez NF Chudnovskiy A Amir ED Amadori L Single-cell immune landscape of human atherosclerotic plaques. Nat Med (2019) 25: 1576–88. 10.1038/s41591-019-0590-4 PMC7318784 31591603 · DOI · Paper page
  32. [33]Rodriques SG Stickels RR Goeva A Martin CA Murray E Vanderburg CR Slide-seq: A scalable technology for measuring genome-wide expression at high spatial resolution. Science (2019) 363: 1463–7. 10.1126/science.aaw1219 PMC6927209 30923225 · DOI · Paper page
  33. [34]Michel JB Phylogenic determinants of cardiovascular frailty, focus on hemodynamics and arterial smooth muscle cells. Physiol Rev (2020) 100: 1779–837. 10.1152/physrev.00022.2019 31999509 · DOI
  34. [35]Wongsurawat T Woo CC Giannakakis A Lin XY Cheow ESH Lee CN Distinctive molecular signature and activated signaling pathways in aortic smooth muscle cells of patients with myocardial infarction. Atherosclerosis (2018) 271: 237–44. 10.1016/j.atherosclerosis.2018.01.024 29395098 · DOI
  35. [36]Libby P Hansson GK From focal lipid storage to systemic inflammation. J Am Coll Cardiol (2019) 74: 1594–607. 10.1016/j.jacc.2019.07.061 PMC6910128 31537270 · DOI
  36. [37]Morioka S Maueröder C Ravichandran KS Living on the edge: Efferocytosis at the interface of homeostasis and pathology. Immunity (2019) 50: 1149–62. 10.1016/j.immuni.2019.04.018 PMC6721617 31117011 · DOI · Paper page
  37. [38]Kolb S Vranckx R Huisse MG Michel JB Meilhac O The phosphatidylserine receptor mediates phagocytosis by vascular smooth muscle cells. J Pathol (2007) 212: 249–59. 10.1002/path.2190 17534843 · DOI
  38. [39]Feil S Fehrenbacher B Lukowski R Essmann F Schulze-Osthoff K Schaller M Transdifferentiation of Vascular Smooth Muscle Cells to Macrophage-Like Cells During Atherogenesis. Circ Res (2014) 115: 662–7. 10.1161/CIRCRESAHA.115.304634 25070003 · DOI · Paper page
  39. [40]Zhao TX Mallat Z Targeting the Immune System in Atherosclerosis. J Am Coll Cardiol (2019) 73: 1691–706. 10.1016/j.jacc.2018.12.083 30947923 · DOI
  40. [41]Hsu S Chu JS Chen FF Wang A Li S Effect of Fluid Shear Stress on a Distinct Population of Vascular Smooth Muscle Cells. Cell Mol Bioeng (2011) 4: 627–36. 10.1007/s12195-011-0205-8 PMC3425612 22924082 · DOI
  41. [42]Thyberg J Differentiated Properties and Proliferation of Arterial Smooth Muscle Cells in Culture. InRev Cytol (1996) 169: 183– 265. 10.1061/s0074-7696(08)61987-7 8843655 · DOI
  42. [43]Wamhoff BR Hoofnagle MH Burns A Sinha S McDonald OG Owens GK. A G/C element mediates repression of the SM22α promoter within phenotypical modulated muscle cells in experimental atherosclerosis. Circ Res (2004) 95: 981–8. 10.1161/01.RES.0000147961 15486317 · DOI
  43. [44]de Carvalho LP Tan SH Ow GS Tang Z Ching J Kovalik JP Plasma Ceramides as Prognostic Biomarkers and Their Arterial and Myocardial Tissue Correlates in Acute Myocardial Infarction. JACC Basic Transl Sci (2018) 3: 163–75. 10.1016/j.jacbts.2017.12.005 PMC6060200 30062203 · DOI
  44. [45]Liu R Jin Y Tang WH Qin L Zhang X Tellides G Ten-eleven translocation-2 (TET2) is a master regulator of smooth muscle cell plasticity. Circulation (2013) 128: 2047–57. 10.1161/CIRCULATIONAHA.113.002887 PMC3899790 24077167 · DOI
  45. [46]Wang Y Dubland JA Allahverdian S Asonye E Sahin B Jaw JE Smooth Muscle Cells Contribute the Majority of Foam Cells in ApoE (Apolipoprotein E)-Deficient Mouse Atherosclerosis. Arterioscler Thromb Vasc Biol (2019) 39: 876–87. 10.1161/ATVBAHA.119.312434 PMC6482082 30786740 · DOI
  46. [47]Liu M Gomez D Smooth Muscle Cell Phenotypic Diversity. Arterioscler Thromb Vasc Biol (2019) 39: 1715–23. 10.1161/ATVBAHA.119.312131 PMC6986347 31340668 · DOI
  47. [48]Vengrenyuk Y Nishi H Long X Ouimet M Savji N Martinez FO Cholesterol Loading Reprograms the MicroRNA-143/145–Myocardin Axis to Convert Aortic Smooth Muscle Cells to a Dysfunctional Macrophage-Like Phenotype. Arterioscler Thromb Vasc Biol (2015) 35: 535–46. 10.1161/ATVBAHA.114.304029 PMC4344402 25573853 · DOI · Paper page
  48. [49]Dubland JA Francis GA So Much Cholesterol: the unrecognized importance of smooth muscle cells in atherosclerotic foam cell formation. Curr Opin Lipidol (2016) 27: 155–61. 10.1097/MOL.0000000000000279 26836481 · DOI
  49. [50]Gu X Xie S Hong D Ding Y An in vitro model of foam cell formation induced by a stretchable microfluidic device. Sci Rep (2019) 9: 7461. 10.1038/s41598-019-43902-3 31097769 PMC6522483 · DOI
  50. [51]Chaabane C Coen M Bochaton-Piallat ML Smooth muscle cell phenotypic switch: implication for foam cell formation. Curr Opin Lipidol (2014) 25: 374–9. 10.1097/MOL.0000000000000113 25110900 · DOI
  51. [52]Wirka RC Wagh D Paik DT Pjanic M Nguyen T Miller CL Atheroprotective roles of smooth muscle cell phenotypic modulation and the TCF21 disease gene as revealed by single-cell analysis. Nat Med (2019) 25: 1280–9. 10.1038/s41591-019-0512-5 PMC7274198 31359001 · DOI
  52. [53]Orr AW Hastings NE Blackman BR Wamhoff BR Complex regulation and function of the inflammatory smooth muscle cell phenotype in atherosclerosis. J Vasc Res (2010) 47: 168–80. 10.1159/000250095 PMC2842170 19851078 · DOI
  53. [54]Rensen SS Doevandans PA van Eys GJ Regulation and characteristics of vascular smooth muscle cell phenotypic diversity. Neth Heart J (2007) 15: 100–8. 10.1007/BF03085963 PMC1847757 17612668 · DOI
  54. [55]Yang L Gao L Nickel T Yang J Zhou J Gilbertsen A Lactate promotes synthetic phenotype in vascular smooth muscle cells. Circ Res (2017) 121: 1251–62. 10.1161/CIRCRESAHA.117.311819 PMC5681426 29021296 · DOI
  55. [56]Forsyth EA Aly HM Neville RF Sidawy AN Proliferation and extracellular matrix production by human infragenicular smooth muscle cells in response to Interleukin 1β. J Vasc Surg (1997) 26: 1002–8. 10.1016/s0741-5214(97)70013-2 9423716 · DOI
  56. [57]Sorokin L The impact of the extracellular matrix on inflammation. Nat Rev (2010) 10: 712–23. 10.1038/nri2852 20865019 · DOI
  57. [58]Kong CH Lin XY Woo CC Wong HC Lee CN Richards AM Characteristics of aortic wall extracellular matrix in patients with acute myocardial infarction: tissue microarray detection of collagen I, collagen III and elastin levels. Interact Cardiovasc Thorac Surg (2013) 16: 11–5. 10.1093/icvts/ivs421 PMC3523627 23049084 · DOI
  58. [59]Moiseeva EP Adhesion receptors of vascular smooth muscle cells and their functions. Cardiovasc Res (2001) 52: 372–86. 10.1016/s0008-6363(01)00399-6 11738054 · DOI
  59. [60]Orr AW Lee MY Lemmon JA Yurdagul A Jr Gomez MF Bortz PD Molecular mechanism of collagen isotype-specific modulation of smooth muscle cell phenotype. Atherioscler Thromb Vasc Biol (2009) 29: 225–31. 10.1161/ATVBAHA.108.178749 PMC2692987 19023090 · DOI
  60. [61]von Wnuck Lipinsky K Keul P Lucke S Heusch G Wohlschlaeger J Baba HA Degraded collagen induces calpin-mediated apoptosis and destruction of the X-chromosome-linked inhibitor of apoptosis (xIAP) in human vascular smooth muscle cells. Cardiovasc Res (2006) 69: 697– 705. 10.1016/j.cardiores.2005.08.005 16223472 · DOI
  61. [62]Adair-Kirk TL Atkinson JJ Broekelmann TJ Doi M Tryggvason K Miner JH A site of laminin α5, AQARSAASKVKVSMKF induce inflammatory cells production of matrix metalloproteinase-9 and chemotaxis. J Immunol (2003) 171: 398– 406. 10.4049/jimmunol.171.1.398 12817023 · DOI
  62. [63]Wang S Voisin MB Larbi KY Dangerfield J Scheiermann C Tran M Venular basement membrane contain specific matrix protein low expression that act as exit points for emigrating neutrophils. J Exp Med (2006) 203: 1519–32. 10.1084/jem.20051210 PMC2118318 16754715 · DOI
  63. [64]Xu J Shi GP Vascular wall extracellular matrix proteins and vascular diseases. Biochim Biophys Acta (2014) 1842: 2106–19. 10.1016/j.bbadis.2014.07.008 PMC4188798 25045854 · DOI
  64. [65]Airhart N Brownstein BH Cobb JP Schierding W Arif B Ennis TL Smooth Muscle Cells from Abdominal Aortic Aneurysms Are Unique and Can Independently and Synergistically Degrade Insoluble Elastin. J Vasc Surg (2014) 60: 1033–41. 10.1016/j.jvs.2013.07.097 PMC3968239 24080131 · DOI
  65. [66]Morrison CJ Butler GS Rodriguez D Overall CM Matrix metalloprotease proteomics: substrate, targets, and therapy. Curr Opin Cell Biol (2009) 21: 645–53. 10.1016/j.ceb.2009.06.006 19616423 · DOI
  66. [67]Durham AL Speer MY Scatena M Giachelli CM Shanahan CM Role of smooth muscle cells in vascular calcification: implications in atherosclerosis and arterial stiffness. Cardiovasc Res (2018) 114: 590– 600. 10.1093/cvr/cvy010 29514202 PMC5852633 · DOI
  67. [68]Leopold JA Vascular Calcification: Mechanisms of Vascular Smooth Muscle Cell Calcification. Trends Cardiovasc Med (2015) 25: 267–74. 10.1016/j.tcm.2014.10.021 PMC4414672 25435520 · DOI · Paper page
  68. [69]Demer LL Tintut Y Vascular calcification: pathobiology of a multifaceted disease. Circulation (2008) 117: 2938–48. 10.1161/CIRCULATIONAHA.107.743161 PMC4431628 18519861 · DOI
  69. [70]Leszczynska A Murphy JM Vascular calcification: is it rather a stem/progenitor cells driven phenomenon? Front Bioeng Biotechnol (2018) 6: 10. 10.3389/fbioe.2018.00010 29479528 PMC5811524 · DOI
  70. [71]Byon CH Javed A Dai Q Kappes JC Clemens TL Darley-Usmar VM Oxidative stress induces vascular calcification through modulation of the osteogenic transcription factor Runx2 by AKT signaling. J Biol Chem (2008) 283: 15319–27. 10.1074/jbc.M800021200 PMC2397455 18378684 · DOI
  71. [72]Komori T Regulation of bone development and extracellular matrix protein genes by RUNX2. Cell Tissue Res (2010) 339: 189–95. 10.1007/s00441-009-0832-8 19649655 · DOI
  72. [73]Speer MY Yang HY Brabb T Leaf E Look A Lin WL Smooth muscle cells give rise to osteochondrogenic precursors and chondrocytes in calcifying arteries. Circ Res (2009) 104: 733–41. 10.1161/CIRCRESAHA.108.183053 PMC2716055 19197075 · DOI
  73. [74]van Varik BJ Rennenberg RJ Reutelingsperger CP Kroon AA de Leeuw PW Schurgers LJ Mechanisms of arterial remodeling: lessons from genetic diseases. Front Genet (2012) 3: 290. 10.3389/fgene.2012.00290 23248645 PMC3521155 · DOI
  74. [75]Cheng C Tempel D van Haperen R van der Baan A Grosveld F Daemen MJ Atherosclerotic Lesion Size and Vulnerability Are Determined by Patterns of Fluid Shear Stress. Circulation (2006) 113: 2744–53. 10.1161/CIRCULATIONAHA.105.590018 16754802 · DOI
  75. [76]Kwak BR Bäck M Bochaton-Piallat ML Caligiuri G Daeman MJ Davies PF Biomechanical factors in atherosclerosis: mechanisms and clinical implications. Eur Heart J (2014) 35: 3013–20d. 10.1093/eurheartj/ehu353 PMC4810806 25230814 · DOI
  76. [77]Yu J Zhang Y Zhang X Rudic RD Bauer PM Altieri DC Endothelium derived nitric oxide synthase negatively regulates the PDFG-survivin pathway during flow-dependant vascular remodelling. PLoS One (2012) 7: e31495. 10.1371/journal.pone.0031495 22355372 PMC3280303 · DOI
  77. [78]Straub AC Zeigler AC Isakson BE The myoendothelial junction: connections that deliver the message. Physiol (Bethesda) (2014) 29: 242–9. 10.1152/physiol.00042.2013 PMC4103062 24985328 · DOI
  78. [79]Jia LX Zhang WM Li TT Liu Y Piao CM Ma YC ER stress dependent microparticles derived from smooth muscle cells promote endothelial dysfunction during thoracic aortic aneurysm and dissection. Clin Sci (Lond) (2017) 131: 1287–99. 10.1042/CS20170252 PMC5461939 28468950 · DOI
  79. [80]Martinelli R Zeiger AS Whitfield M Sciuto TE Dvorak A Van Vliet KJ Probing the biomechanical contribution of the endothelium to lymphocyte migration: diapedesis by the path of less resistance. J Cell Sci (2014) 127: 3720–34. 10.1242/jcs.148619 PMC4150060 25002404 · DOI
  80. [81]Döring Y Drechsler M Soehnlein O Weber C Neutrophils in atherosclerosis: from mice to man. Atherioscler Thromb Vasc Biol (2015) 35: 288–95. 10.1161/ATVBAHA.114.303564 25147339 · DOI
  81. [82]Barlic J Zhang Y Murphy PM Atherogenic lipids induce adhesion of human coronary artery smooth muscle cells to macrophages by up-regulating chemokine CX3CL1 on smooth muscle cells in a TNFα-NFkB-dependant manner. J Biol Chem (2007) 282: 19167–76. 10.1074/jbc.M701642200 17456471 · DOI
  82. [83]Jaipersad AS Lip GY Silverman S Shantsila E The Role of Monocytes in Angiogenesis and Atherosclerosis. Arterioscler Thromb Vasc Biol (2014) 63: 1– 11. 10.1016/j.jacc.2013.09.019 24140662 · DOI
  83. [84]Kapellos TS Bonaguro L Gemünd I Reusch N Saglam A Hinkley ER Human Monocyte Subsets and Phenotypes in Major Chronic Inflammatory Diseases. Front Immunol (2019) 10: 2035. 10.3389/fimmu.2019.02035 31543877 PMC6728754 · DOI
  84. [85]Hamers AAJ Dinh HQ Thomas GD Marcovecchio P Blatchley A Nakao CS Human Monocyte Heterogeneity as Revealed by High-Dimensional Mass Cytometry. Arterioscler Thromb Vasc Biol (2019) 39: 25– 36. 10.1161/ATVBAHA.118.311022 30580568 PMC6697379 · DOI
  85. [86]Verweij SL Duivenvoorden R Stiekema LCA Nurmohamed NS van der Valk FM Versloot M CCR2 expression on circulating monocytes is associated with arterial wall inflammation assessed by 18F-FDG PET/CT in patients at risk for cardiovascular disease. Cardiovasc Res (2017) 114: 468–75. 10.1093/cvr/cvx224 29186373 · DOI
  86. [88]Hambleton S Salem S Bustamante J Bigley V Boisson-Dupuis S Azevedo J IRF8 mutations and human dendritic-cell immunodeficiency. N Engl J Med (2011) 365: 127–38. 10.1056/NEJMoa1100066 PMC3136554 21524210 · DOI
  87. [89]Gundra UM Girgis NM Ruckerl D Jenkins S Ward LN Kurtz ZD Alternatively activated macrophages derived from monocytes and tissue macrophages are phenotypically and functionally distinct. Blood (2014) 123: e110–22. 10.1182/blood-2013-08-520619 PMC4023427 24695852 · DOI · Paper page
  88. [90]Bobryshev YV Ivanova EA Chistiakov DA Nikiforov NG Orekhov AN Macrophages and Their Role in Atherosclerosis: Pathophysiology and Transcriptome Analysis. BioMed Res Int (2016) 2016: 9582430. 10.1155/2016/9582430 27493969 PMC4967433 · DOI
  89. [91]A-Gonzalez N Quintana JA García-Silva S Mazariegos M González de la Aleja A Nicolás-Ávila JA Phagocytosis imprints heterogeneity in tissue-resident macrophages. J Exp Med (2017) 214: 1281–96. 10.1084/jem.20161375 PMC5413334 28432199 · DOI
  90. [92]Lim HY Lim SY Tan CK Thiam CH Goh CC Carbajo D Hyaluronan receptor LYVE-1-expressing macrophages maintain arterial tone through hyaluronan-mediated regulation of smooth muscle cell collagen. Immunity (2018) 49: 326– 41.e7. 10.1016/j.immuni.2018.06.008 30054204 · DOI · Paper page
  91. [94]Lapenna A De Palma M Lewis CE Perivascular macrophages in health and disease. Nat Rev Immunol (2018) 18: 689– 702. 10.1038/s41577-018-0056-9 30127389 · DOI
  92. [95]Parisi L Gini E Baci D Tremolati M Fanuli M Bassani B Macrophage Polarization in Chronic Inflammatory Diseases: Killers or Builders? J Immunol Res (2018) 2018: 8917804. 10.1155/2018/8917804 29507865 PMC5821995 · DOI · Paper page
  93. [96]Orecchioni M Ghosheh Y Pramod AB Ley K Macrophage Polarization: Different Gene Signatures in M1(LPS+) vs. Classically and M2(LPS–) vs. Alternatively Activated Macrophages. Front Immunol (2019) 10: 1084. 10.3389/firmmu.2019.01084 31178859 PMC6543837 · DOI
  94. [97]van der Vorst EPC Weber C Novel Features of Monocytes and Macrophages in Cardiovascular Biology and Disease. Arterioscler Thromb Vasc Biol (2019) 39: e30–7. 10.1161/ATVBAHA.118.312002 30673349 · DOI
  95. [98]Conaway RC Sato S Tomomori-Sato C Yao T Conaway JW The mammalian Mediator complex and its role in transcriptional regulation. Trends Biochem Sci (2005) 30: 250–5. 10.1016/j.tibs.2005.03.002 15896743 · DOI
  96. [99]Tavakoli S Downs K Short JD Nguyen HN Lai Y Jerabek PA Characterization of Macrophage Polarization States Using Combined Measurement of 2-Deoxyglucose and Glutamine Accumulation. Arterioscler Thromb Vasc Biol (2017) 37: 1840–8. 10.1161/ATVBAHA.117.308848 PMC8036006 28798141 · DOI
  97. [100]Ionita MG van den Borne P Catanzariti LM Moll FL de Vries JP Pasterkamp G High neutrophil numbers in human carotid atherosclerotic plaques are associated with characteristics of rupture-prone lesions. Arterioscler Thromb Vasc Biol (2010) 30: 1842–8. 10.1161/ATVBAHA.110.209296 20595650 · DOI
  98. [101]Silvestre-Roig C Braster Q Wichapong K Lee EY Teulon JM Berrebeh N Externalized histone H4 orchestrates chronic inflammation by inducing lytic cell death. Nature (2019) 569: 236–40. 10.1038/s41586-019-1167-6 PMC6716525 31043745 · DOI
  99. [102]Kramann R Goettsch C Wongboonsin J Iwata H Schneider RK Kuppe C Adventitial MSC-like Cells Are Progenitors of Vascular Smooth Muscle Cells and Drive Vascular Calcification in Chronic Kidney Disease. Cell Stem Cell (2016) 19: 628–42. 10.1016/j.stem.2016.08.001 PMC5097006 27618218 · DOI
  100. [103]Roostalu U Aldeiri B Albertini A Humphreys N Simonsen-Jackson M Wong JKF Distinct Cellular Mechanisms Underlie Smooth Muscle Turnover in Vascular Development and Repair. Circ Res (2018) 122: 267–81. 10.1161/CIRCRESAHA.117.312111 PMC5771686 29167274 · DOI
  101. [104]Dobnikar L Taylor AL Chappell J Oldach P Harman JL Oerton E Disease-relevant transcriptional signatures identified in individual smooth muscle cells from healthy mouse vessels. Nat Commun (2018) 9: 4567. 10.1038/s41467-018-06891-x 30385745 PMC6212435 · DOI
  102. [105]Evrard SM Lecce L Michelis KC Nomura-Kitabayashi A Pandey G Purushothaman KR Endothelial to mesenchymal transition is common in atherosclerotic lesions and is associated with plaque instability. Nat Commun (2016) 7: 11853. 10.1038/ncomms11853 27340017 PMC4931033 · DOI
  103. [106]Pérez L Muñoz-Durango N Riedel CA Echeverría C Kalergis AM Cabello-Verrugio C Endothelial-to-mesenchymal transition: Cytokine-mediated pathways that determine endothelial fibrosis under inflammatory conditions. Cytokine Growth Factor Rev (2016) 33: 41– 54. 10.1016/j.cytogfr.2016.09.002 27692608 · DOI
  104. [107]Spillmann F Miteva K Pieske B Tschöpe C Van Linthout S High-Density Lipoproteins Reduce Endothelial-to-Mesenchymal Transition. Arterioscler Thromb Vasc Biol (2015) 35: 1774–7. 10.1161/ATVBAHA.115.305887 26088574 · DOI
  105. [108]Passman JN Dong XR Wu SP Maguire CT Hogan KA Bautch VL A sonic hedgehog signaling domain in the arterial adventitia supports resident Sca1+ smooth muscle progenitor cells. Proc Natl Acad Sci USA (2008) 105: 9349–54. 10.1073/pnas.0711382105 PMC2453724 18591670 · DOI
  106. [109]Tang J Wang H Huang X Li F Zhu H Li Y Arterial Sca1+ Vascular Stem Cells Generate De Novo Smooth Muscle for Artery Repair and Regeneration. Cell Stem Cell (2020) 26: 81– 96. 10.1016/j.stem.2019.11.010 31883835 · DOI
  107. [110]Voll RE Herrmann M Roth EA Stach C Kalden JR Girkontaite I Immunosuppressive effects of apoptotic cells. Nature (1997) 390: 350–1. 10.1038/37022 9389474 · DOI · Paper page
  108. [111]Song Y Shen H Schenten D Shan P Lee PJ Goldstein DR Ageing Enhances the Basal Production of IL-6 and CCL2 in Vascular Smooth Muscle Cells. Arterioscler Thromb Vasc Biol (2012) 32: 103–9. 10.1161/ATVBAHA.111.236349 PMC3241880 22034510 · DOI
  109. [113]Liu Y Drozdov I Shroff R Beltran LE Shanahan CM Prelamin A accelerates vascular calcification via activation of the DNA damage response and senescence-associated secretory phenotype in vascular smooth muscle cells. Circ Res (2013) 112: e99– 109. 10.1161/CIRCRESAHA.111.300543 23564641 · DOI
  110. [114]Kolb JP Oguin TH3 Oberst A Martinez J Programmed cell death and inflammation: winter is coming. Trends Immunol (2017) 38: 705–18. 10.1016/j.it.2017.06.009 PMC5710799 28734635 · DOI
  111. [115]Shoenfeld Y Sherer Y George J Harats D Autoantibodies associated with atherosclerosis. Ann Med (2000) 32: 37– 40. 11209980
  112. [116]Lacolley P Regnault V Nicoletti A Li Z Michel JB The vascular smooth muscle cell in arterial pathology: a cell that can take on multiple roles. Cardiovasc Res (2012) 95: 194– 204. 10.1093/cvr/cvs135 22467316 · DOI
  113. [118]Ponnuswamy P Joffre J Herbin O Esposito B Laurans L Binder CJ Angiotension II synergizes with BAFF to promote atheroprotective regulatory B cells. Sci Rep (2017) 7: 4111. 10.1038/s41598-017-04438-6 28646220 PMC5482806 · DOI
  114. [119]Bhaskar V Yin J Mirza AM Phan D Vanegas S Issafras H Monoclonal antibodies targeting IL-1 beta reduce biomarkers of atherosclerosis in vitro and inhibit atherosclerotic plaque formation in Apolipoprotein E-deficient mice. Atherosclerosis (2011) 216: 313–20. 10.1016/j.atherosclerosis.2011.02.026 21411094 · DOI

Cited by

Sorted by citations

Authors
Sorokin, V., Vickneson, K., Kofidis, T., Woo, C. C., Lin, X. Y., Foo, R., & Shanahan, C. M.
Affiliations
  • National University of Singapore (SG)
  • University of Dundee (GB)
  • National University Hospital (SG)
  • Agency for Science, Technology and Research (SG)
  • King's College London (GB)
Corresponding author
Sorokin, Vitaly
Venue
Frontiers in Immunology
Published
2020-11-26
Volume
11
Pages
599415-599415
ISSN
1664-3224 (ISSN-L)
OpenAlex
W3110282950
Cited by
292
References
5
Citations by year
2026: 30 · 2025: 47 · 2024: 69 · 2023: 55 · 2022: 63 · 2021: 28
FWCI
3.56
Type
journal article
Language
en
Open access
Locations
  • Frontiers in Immunology (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • National University of Singapore (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
British Heart Foundation (RG/17/2/32808)
Topics
  • Life Sciences › Immunology and Microbiology › Immunology › Atherosclerosis and Cardiovascular Diseases
  • Health Sciences › Medicine › Surgery › Cardiovascular, Neuropeptides, and Oxidative Stress Research
  • Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Cerebrovascular and Carotid Artery Diseases
Keywords
vascular smooth muscle cells, vascular inflammation, atherosclerosis, cellular senescence, proximity ligation assay, cell fate tracing
MeSH terms
Animals, Humans, Inflammation, Muscle, Smooth, Vascular, Vasculitis, Myocytes, Smooth Muscle, Atherosclerosis

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