Alternative splicing of endothelial fibronectin is induced by disturbed hemodynamics and protects against hemorrhage of the vessel wall

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 34, Issue 9, 2014, Pages 2042-2050

  Murphy, Patrick A ^a   Hynes, Richard O ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

alternative splicing; fibronectins; hemorrhage; macrophages

Indexed keywords

CLODRONIC ACID; FIBRONECTIN; MESSENGER RNA;

ALTERNATIVE RNA SPLICING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERY ENDOTHELIUM; ARTERY INTIMA; ARTICLE; BLEEDING; BLOOD FLOW; BLOOD VESSEL WALL; CAROTID ARTERY LIGATION; CONTROLLED STUDY; EXON; FIBRONECTIN EXTRA DOMAIN A; FIBRONECTIN EXTRA DOMAIN B; GENE DELETION; GENE EXPRESSION; HEMODYNAMICS; HYPERTROPHY; MACROPHAGE; MOLECULAR BIOLOGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION;

ALTERNATIVE SPLICING; FIBRONECTINS; HEMORRHAGE; MACROPHAGES;

ADVENTITIA; ALTERNATIVE SPLICING; ANIMALS; CAROTID STENOSIS; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; ENDOTHELIUM, VASCULAR; EXONS; EXTRACELLULAR MATRIX; FIBRONECTINS; GENE DELETION; HEMORHEOLOGY; HEMORRHAGE; HYPERTROPHY; LIGATION; MACROPHAGES; MICE; MICE, INBRED C57BL; TUNICA INTIMA; TUNICA MEDIA;

EID: 84906935585     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.114.303879     Document Type: Article

References (52)

1. Lindsay ME, Dietz HC. Lessons on the pathogenesis of aneurysm from heritable conditions. Nature. 2011;473:308-316.
2. Gould DB, Phalan FC, Breedveld GJ, van Mil SE, Smith RS, Schimenti JC, Aguglia U, van der Knaap MS, Heutink P, John SW. Mutations in Col4a1 cause perinatal cerebral hemorrhage and porencephaly. Science. 2005;308:1167-1171.
3. Plaisier E, Gribouval O, Alamowitch S, et al. Col4a1 mutations and hereditary angiopathy, nephropathy, aneurysms, and muscle cramps. N Eng J Med. 2007;357:2687-2695.
4. Sadasivan C, Fiorella DJ, Woo HH, Lieber BB. Physical factors effecting cerebral aneurysm pathophysiology. Ann Biomed Eng. 2013;41:1347-1365.
5. Xiang J, Natarajan SK, Tremmel M, Ma D, Mocco J, Hopkins LN, Siddiqui AH, Levy EI, Meng H. Hemodynamic-morphologic discriminants for intracranial aneurysm rupture. Stroke. 2011;42:144-152.
6. Boussel L, Rayz V, McCulloch C, Martin A, Acevedo-Bolton G, Lawton M, Higashida R, Smith WS, Young WL, Saloner D. Aneurysm growth occurs at region of low wall shear stress: patient-specific correlation of hemodynamics and growth in a longitudinal study. Stroke. 2008;39:2997-3002.
7. Conway DE, Schwartz MA. Flow-dependent cellular mechanotransduction in atherosclerosis. J Cell Sci. 2013;126:5101-5109.
8. Peters DG, Kassam AB, Feingold E, Heidrich-O'Hare E, Yonas H, Ferrell RE, Brufsky A. Molecular anatomy of an intracranial aneurysm: coordinated expression of genes involved in wound healing and tissue remodeling. Stroke. 2001;32:1036-1042.
9. Hynes RO. Cell-matrix adhesion in vascular development. J Thromb Haemost. 2007;5(suppl 1):32-40.
10. Singh P, Carraher C, Schwarzbauer JE. Assembly of fibronectin extracellular matrix. Annu Rev Cell Dev Biol. 2010;26:397-419.
11. Orr AW, Sanders JM, Bevard M, Coleman E, Sarembock IJ, Schwartz MA. The subendothelial extracellular matrix modulates NF-kappaB activation by flow: a potential role in atherosclerosis. J Cell Biol. 2005;169:191-202.
12. Feaver RE, Gelfand BD, Wang C, Schwartz MA, Blackman BR. Atheroprone hemodynamics regulate fibronectin deposition to create positive feedback that sustains endothelial inflammation. Circ Res. 2010;106:1703-1711.
13. Hahn C, Schwartz MA. The role of cellular adaptation to mechanical forces in atherosclerosis. Arterioscler Thromb Vasc Biol. 2008;28:2101-2107.
14. Rohwedder I, Montanez E, Beckmann K, Bengtsson E, Dunér P, Nilsson J, Soehnlein O, Fässler R. Plasma fibronectin deficiency impedes atherosclerosis progression and fibrous cap formation. EMBO Mol Med. 2012;4:564-576.
15. Hynes RO. The extracellular matrix: not just pretty fibrils. Science. 2009;326:1216-1219.
16. Astrof S, Hynes RO. Fibronectins in vascular morphogenesis. Angiogenesis. 2009;12:165-175.
17. Hynes RO. The evolution of metazoan extracellular matrix. J Cell Biol. 2012;196:671-679.
18. Dubin D, Peters JH, Brown LF, Logan B, Kent KC, Berse B, Berven S, Cercek B, Sharifi BG, Pratt RE. Balloon catheterization induced arterial expression of embryonic fibronectins. Arterioscler Thromb Vasc Biol. 1995;15:1958-1967.
19. Glukhova MA, Frid MG, Shekhonin BV, Vasilevskaya TD, Grunwald J, Saginati M, Koteliansky VE. Expression of extra domain A fibronectin sequence in vascular smooth muscle cells is phenotype dependent. J Cell Biol. 1989;109:357-366.
20. Tan MH, Sun Z, Opitz SL, Schmidt TE, Peters JH, George EL. Deletion of the alternatively spliced fibronectin EIIIA domain in mice reduces atherosclerosis. Blood. 2004;104:11-18.
21. Fiechter M, Frey K, Fugmann T, Kaufmann PA, Neri D. Comparative in vivo analysis of the atherosclerotic plaque targeting properties of eight human monoclonal antibodies. Atherosclerosis. 2011;214:325-330.
22. Paloschi V, Kurtovic S, Folkersen L, Gomez D, Wågsäter D, Roy J, Petrini J, Eriksson MJ, Caidahl K, Hamsten A, Liska J, Michel JB, Franco- Cereceda A, Eriksson P. Impaired splicing of fibronectin is associated with thoracic aortic aneurysm formation in patients with bicuspid aortic valve. Arterioscler Thromb Vasc Biol. 2011;31:691-697.
23. Nam D, Ni CW, Rezvan A, Suo J, Budzyn K, Llanos A, Harrison D, Giddens D, Jo H. Partial carotid ligation is a model of acutely induced disturbed flow, leading to rapid endothelial dysfunction and atherosclerosis. Am J Physiol Heart Circ Physiol. 2009;297:H1535-H1543.
24. Nam D, Ni CW, Rezvan A, Suo J, Budzyn K, Llanos A, Harrison DG, Giddens DP, Jo H. A model of disturbed flow-induced atherosclerosis in mouse carotid artery by partial ligation and a simple method of rna isolation from carotid endothelium. J Vis Exp. 2010. Jun 22;(40). pii: 1861.
25. Katz Y, Wang ET, Airoldi EM, Burge CB. Analysis and design of RNA sequencing experiments for identifying isoform regulation. Nat Methods. 2010;7:1009-1015.
26. Astrof S, Crowley D, Hynes RO. Multiple cardiovascular defects caused by the absence of alternatively spliced segments of fibronectin. Dev Biol. 2007;311:11-24.
27. Daugherty A, Manning MW, Cassis LA. Angiotensin II promotes atherosclerotic lesions and aneurysms in apolipoprotein E-deficient mice. J Clin Invest. 2000;105:1605-1612.
28. Daugherty A, Cassis LA. Mouse models of abdominal aortic aneurysms. Arterioscler Thromb Vasc Biol. 2004;24:429-434.
29. Walpola PL, Gotlieb AI, Langille BL. Monocyte adhesion and changes in endothelial cell number, morphology, and F-actin distribution elicited by low shear stress in vivo. Am J Pathol. 1993;142:1392-1400.
30. Schievink WI, Raissi SS, Maya MM, Velebir A. Screening for intracranial aneurysms in patients with bicuspid aortic valve. Neurology. 2010;74:1430-1433.
31. Tieu BC, Lee C, Sun H, Lejeune W, Recinos A III, Ju X, Spratt H, Guo DC, Milewicz D, Tilton RG, Brasier AR. An adventitial IL-6/MCP1 amplification loop accelerates macrophage-mediated vascular inflammation leading to aortic dissection in mice. J Clin Invest. 2009;119:3637-3651.
32. Arribillaga L, Durantez M, Lozano T, Rudilla F, Rehberger F, Casares N, Villanueva L, Martinez M, Gorraiz M, Borrás-Cuesta F, Sarobe P, Prieto J, Lasarte JJ. A fusion protein between streptavidin and the endogenous TLR4 ligand EDA targets biotinylated antigens to dendritic cells and induces T cell responses in vivo. Biomed Res Int. 2013; 2013:864720.
33. Dunér P, To F, Beckmann K, Björkbacka H, Fredrikson GN, Nilsson J, Bengtsson E. Immunization of apoE-/- mice with aldehyde-modified fibronectin inhibits the development of atherosclerosis. Cardiovasc Res. 2011;91:528-536.
34. Manabe R, Oh-e N, Sekiguchi K. Alternatively spliced EDA segment regulates fibronectin-dependent cell cycle progression and mitogenic signal transduction. J Biol Chem. 1999;274:5919-5924.
35. Cseh B, Fernandez-Sauze S, Grall D, Schaub S, Doma E, Van Obberghen- Schilling E. Autocrine fibronectin directs matrix assembly and crosstalk between cell-matrix and cell-cell adhesion in vascular endothelial cells. J Cell Sci. 2010;123(Pt 22):3989-3999.
36. Faurobert E, Rome C, Lisowska J, Manet-Dupé S, Boulday G, Malbouyres M, Balland M, Bouin AP, Kéramidas M, Bouvard D, Coll JL, Ruggiero F, Tournier-Lasserve E, Albiges-Rizo C. CCM1-ICAP-1 complex controls 1 integrin-dependent endothelial contractility and fibronectin remodeling. J Cell Biol. 2013;202:545-561.
37. Chauhan AK, Kisucka J, Cozzi MR, Walsh MT, Moretti FA, Battiston M, Mazzucato M, De Marco L, Baralle FE, Wagner DD, Muro AF. Prothrombotic effects of fibronectin isoforms containing the EDA domain. Arterioscler Thromb Vasc Biol. 2008;28:296-301.
38. Jarnagin WR, Rockey DC, Koteliansky VE, Wang SS, Bissell DM. Expression of variant fibronectins in wound healing: cellular source and biological activity of the EIIIA segment in rat hepatic fibrogenesis. J Cell Biol. 1994;127(6 Pt 2):2037-2048.
39. Muro AF, Moretti FA, Moore BB, Yan M, Atrasz RG, Wilke CA, Flaherty KR, Martinez FJ, Tsui JL, Sheppard D, Baralle FE, Toews GB, White ES. An essential role for fibronectin extra type III domain A in pulmonary fibrosis. Am J Respir Crit Care Med. 2008;177:638-645.
40. Olsen AL, Sackey BK, Marcinkiewicz C, Boettiger D, Wells RG. Fibronectin extra domain-A promotes hepatic stellate cell motility but not differentiation into myofibroblasts. Gastroenterology. 2012;142:928-937.e3.
41. George J, Roulot D, Koteliansky VE, Bissell DM. In vivo inhibition of rat stellate cell activation by soluble transforming growth factor beta type II receptor: a potential new therapy for hepatic fibrosis. Proc Natl Acad Sci U S A. 1999;96:12719-12724.
42. Duffield JS, Forbes SJ, Constandinou CM, Clay S, Partolina M, Vuthoori S, Wu S, Lang R, Iredale JP. Selective depletion of macrophages reveals distinct, opposing roles during liver injury and repair. J Clin Invest. 2005;115:56-65.
43. Gibbons MA, MacKinnon AC, Ramachandran P, Dhaliwal K, Duffin R, Phythian-Adams AT, van Rooijen N, Haslett C, Howie SE, Simpson AJ, Hirani N, Gauldie J, Iredale JP, Sethi T, Forbes SJ. Ly6Chi monocytes direct alternatively activated profibrotic macrophage regulation of lung fibrosis. Am J Respir Crit Care Med. 2011;184:569-581.
44. Frösen J, Piippo A, Paetau A, Kangasniemi M, Niemelä M, Hernesniemi J, Jääskeläinen J. Remodeling of saccular cerebral artery aneurysm wall is associated with rupture: histological analysis of 24 unruptured and 42 ruptured cases. Stroke. 2004;35:2287-2293.
45. Kanematsu Y, Kanematsu M, Kurihara C, Tada Y, Tsou TL, van Rooijen N, Lawton MT, Young WL, Liang EI, Nuki Y, Hashimoto T. Critical roles of macrophages in the formation of intracranial aneurysm. Stroke. 2011;42:173-178.
46. Korshunov VA, Berk BC. Strain-dependent vascular remodeling: the "Glagov phenomenon" is genetically determined. Circulation. 2004;110:220-226.
47. Korshunov VA, Berk BC. Flow-induced vascular remodeling in the mouse: a model for carotid intima-media thickening. Arterioscler Thromb Vasc Biol. 2003;23:2185-2191.
48. Chiang HY, Korshunov VA, Serour A, Shi F, Sottile J. Fibronectin is an important regulator of flow-induced vascular remodeling. Arterioscler Thromb Vasc Biol. 2009;29:1074-1079.
49. Jin SX, Shen LH, Nie P, Yuan W, Hu LH, Li DD, Chen XJ, Zhang XK, He B. Endogenous renovascular hypertension combined with low shear stress induces plaque rupture in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol. 2012;32:2372-2379.
50. Virmani R, Kolodgie FD, Burke AP, Finn AV, Gold HK, Tulenko TN, Wrenn SP, Narula J. Atherosclerotic plaque progression and vulnerability to rupture: angiogenesis as a source of intraplaque hemorrhage. Arterioscler Thromb Vasc Biol. 2005;25:2054-2061.
51. Kalsotra A, Cooper TA. Functional consequences of developmentally regulated alternative splicing. Nat Rev Genet. 2011;12:715-729.
52. Merkin J, Russell C, Chen P, Burge CB. Evolutionary dynamics of gene and isoform regulation in Mammalian tissues. Science. 2012;338:1593-1599.