TGF-β (transforming growth factor-β) signaling protects the thoracic and abdominal aorta from angiotensin iiinduced pathology by distinct mechanisms

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 37, Issue 11, 2017, Pages 2102-2113

  Angelov, Stoyan N ^a   Hu, Jie Hong ^a   Wei, Hao ^a   Airhart, Nathan ^a   Shi, Minghui ^a   D'Ichek, David A ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

Aneurysm; Angiotensin II; Aorta; Macrophages; Mice; Smooth muscle; TGF

Indexed keywords

2G7 ANTIBODY; ANGIOTENSIN II; NEUTRALIZING ANTIBODY; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA ANTIBODY; UNCLASSIFIED DRUG; ANTIBODY; PROTEIN SERINE THREONINE KINASE; TGFB1 PROTEIN, MOUSE; TGFB2 PROTEIN, MOUSE; TGFB3 PROTEIN, MOUSE; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA2; TRANSFORMING GROWTH FACTOR BETA3; TRANSFORMING GROWTH FACTOR-BETA TYPE II RECEPTOR;

ABDOMINAL AORTA; ABDOMINAL AORTIC ANEURYSM; ADVENTITIA; ANIMAL EXPERIMENT; AORTIC MEDIAL SMOOTH MUSCLE CELL; AORTIC SMOOTH MUSCLE CELL; AORTIC WALL; ARTICLE; CONTROLLED STUDY; DISEASE SEVERITY; FEMALE; HEMATOMA; HISTOPATHOLOGY; MALE; MOUSE; NONHUMAN; PREVALENCE; PRIORITY JOURNAL; TGF BETA SIGNALING; THORACIC AORTA; ANIMAL; ANTAGONISTS AND INHIBITORS; AORTIC ANEURYSM, ABDOMINAL; AORTIC ANEURYSM, THORACIC; C57BL MOUSE; CHEMICALLY INDUCED; DEFICIENCY; DISEASE MODEL; DRUG EFFECTS; GENETIC PREDISPOSITION; GENETICS; KNOCKOUT MOUSE; LESIONS AND DEFECTS; METABOLISM; PATHOLOGY; PHENOTYPE; SEVERITY OF ILLNESS INDEX; SIGNAL TRANSDUCTION; TUNICA MEDIA; VASCULAR REMODELING; VASCULAR SMOOTH MUSCLE;

ADVENTITIA; ANGIOTENSIN II; ANIMALS; ANTIBODIES; AORTA, ABDOMINAL; AORTA, THORACIC; AORTIC ANEURYSM, ABDOMINAL; AORTIC ANEURYSM, THORACIC; DILATATION, PATHOLOGIC; DISEASE MODELS, ANIMAL; FEMALE; GENETIC PREDISPOSITION TO DISEASE; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUSCLE, SMOOTH, VASCULAR; PHENOTYPE; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SEVERITY OF ILLNESS INDEX; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA2; TRANSFORMING GROWTH FACTOR BETA3; TUNICA MEDIA; VASCULAR REMODELING;

EID: 85025457624     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.117.309401     Document Type: Article

References (49)

1. Guirguis-Blake JM, Beil TL, Senger CA, Whitlock EP. Ultrasonography screening for abdominal aortic aneurysms: A systematic evidence review for the U.S. preventive services task force. Ann Intern Med. 2014;160:321-329. doi: 10.7326/M13-1844.
2. Pande RL, Beckman JA. Abdominal aortic aneurysm: Populations at risk and how to screen. J Vasc Interv Radiol. 2008;19(6 suppl):S2-S8. doi: 10.1016/j.jvir.2008.03.010.
3. LeFevre ML; U.S. Preventive Services Task Force. Screening for abdominal aortic aneurysm: U.S. preventive services task force recommendation statement. Ann Intern Med. 2014;161:281-290. doi: 10.7326/M14-1204.
4. Lin F, Yang X. TGF-signaling in aortic aneurysm: Another round of controversy. J Genet Genomics. 2010;37:583-591. doi: 10.1016/S1673-8527(09)60078-3.
5. Chen X, Lu H, Rateri DL, Cassis LA, Daugherty A. Conundrum of angiotensin II and TGF-interactions in aortic aneurysms. Curr Opin Pharmacol. 2013;13:180-185. doi: 10.1016/j.coph.2013.01.002.
6. King VL, Lin AY, Kristo F, Anderson TJ, Ahluwalia N, Hardy GJ, Owens AP 3rd, Howatt DA, Shen D, Tager AM, Luster AD, Daugherty A, Gerszten RE. Interferon-gamma and the interferon-inducible chemokine CXCL10 protect against aneurysm formation and rupture. Circulation. 2009;119:426-435. doi: 10.1161/CIRCULATIONAHA.108.785949.
7. Rush C, Nyara M, Moxon JV, Trollope A, Cullen B, Golledge J. Whole genome expression analysis within the angiotensin II-apolipoprotein E deficient mouse model of abdominal aortic aneurysm. BMC Genomics. 2009;10:298. doi: 10.1186/1471-2164-10-298.
8. Spin JM, Hsu M, Azuma J, Tedesco MM, Deng A, Dyer JS, Maegdefessel L, Dalman RL, Tsao PS. Transcriptional profiling and network analysis of the murine angiotensin II-induced abdominal aortic aneurysm. Physiol Genomics. 2011;43:993-1003. doi: 10.1152/physiolgenomics.00044.2011.
9. Doyle AJ, Redmond EM, Gillespie DL, Knight PA, Cullen JP, Cahill PA, Morrow DJ. Differential expression of hedgehog/notch and transforming growth factor-in human abdominal aortic aneurysms. J Vasc Surg. 2015;62:464-470. doi: 10.1016/j.jvs.2014.02.053.
10. Dai J, Losy F, Guinault AM, Pages C, Anegon I, Desgranges P, Becquemin JP, Allaire E. Overexpression of transforming growth factor-beta1 stabilizes already-formed aortic aneurysms: A first approach to induction of functional healing by endovascular gene therapy. Circulation. 2005;112:1008-1015. doi: 10.1161/CIRCULATIONAHA.104.523357.
11. Wang Y, Ait-Oufella H, Herbin O, Bonnin P, Ramkhelawon B, Taleb S, Huang J, Offenstadt G, Combadière C, Rénia L, Johnson JL, Tharaux PL, Tedgui A, Mallat Z. TGF-beta activity protects against inflammatory aortic aneurysm progression and complications in angiotensin II-infused mice. J Clin Invest. 2010;120:422-432. doi: 10.1172/JCI38136.
12. Chen X, Rateri DL, Howatt DA, Balakrishnan A, Moorleghen JJ, Cassis LA, Daugherty A. TGF-neutralization enhances AngII-induced aortic rupture and aneurysm in both thoracic and abdominal regions. PLoS One. 2016;11:e0153811. doi: 10.1371/journal.pone.0153811.
13. Hu JH, Wei H, Jaffe M, Airhart N, Du L, Angelov SN, Yan J, Allen JK, Kang I, Wight TN, Fox K, Smith A, Enstrom R, Dichek DA. Postnatal deletion of the type II transforming growth factor-receptor in smooth muscle cells causes severe aortopathy in mice. Arterioscler Thromb Vasc Biol. 2015;35:2647-2656. doi: 10.1161/ATVBAHA.115.306573.
14. 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. doi: 10.1172/JCI7818.
15. Leveén P, Larsson J, Ehinger M, Cilio CM, Sundler M, Sjöstrand LJ, Holmdahl R, Karlsson S. Induced disruption of the transforming growth factor beta type II receptor gene in mice causes a lethal inflammatory disorder that is transplantable. Blood. 2002;100:560-568.
16. Daugherty A, Rateri DL, Charo IF, Owens AP, Howatt DA, Cassis LA. Angiotensin II infusion promotes ascending aortic aneurysms: Attenuation by CCR2 deficiency in apoE-/-mice. Clin Sci (Lond). 2010;118:681-689. doi: 10.1042/CS20090372.
17. Rateri DL, Davis FM, Balakrishnan A, Howatt DA, Moorleghen JJ, Oconnor WN, Charnigo R, Cassis LA, Daugherty A. Angiotensin II induces region-specific medial disruption during evolution of ascending aortic aneurysms. Am J Pathol. 2014;184:2586-2595. doi: 10.1016/j.ajpath.2014.05.014.
18. Isselbacher EM. Thoracic and abdominal aortic aneurysms. Circulation. 2005;111:816-828. doi: 10.1161/01.CIR.0000154569.08857.7A.
19. Lindsay ME, Dietz HC. Lessons on the pathogenesis of aneurysm from heritable conditions. Nature. 2011;473:308-316. doi: 10.1038/nature10145.
20. Klink A, Heynens J, Herranz B, Lobatto ME, Arias T, Sanders HM, Strijkers GJ, Merkx M, Nicolay K, Fuster V, Tedgui A, Mallat Z, Mulder WJ, Fayad ZA. In vivo characterization of a new abdominal aortic aneurysm mouse model with conventional and molecular magnetic resonance imaging. J Am Coll Cardiol. 2011;58:2522-2530. doi: 10.1016/j.jacc.2011.09.017.
21. Tieu BC, Lee C, Sun H, Lejeune W, Recinos A 3rd, 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. doi: 10.1172/JCI38308.
22. Cook JR, Clayton NP, Carta L, Galatioto J, Chiu E, Smaldone S, Nelson CA, Cheng SH, Wentworth BM, Ramirez F. Dimorphic effects of transforming growth factor-signaling during aortic aneurysm progression in mice suggest a combinatorial therapy for Marfan syndrome. Arterioscler Thromb Vasc Biol. 2015;35:911-917. doi: 10.1161/ATVBAHA.114.305150.
23. Gallo EM, Loch DC, Habashi JP, et al. Angiotensin II-dependent TGF-signaling contributes to Loeys-Dietz syndrome vascular pathogenesis. J Clin Invest. 2014;124:448-460. doi: 10.1172/JCI69666.
24. Granata A, Serrano F, Bernard WG, McNamara M, Low L, Sastry P, Sinha S. An iPSC-derived vascular model of Marfan syndrome identifies key mediators of smooth muscle cell death. Nat Genet. 2017;49:97-109. doi: 10.1038/ng.3723.
25. Zacchigna L, Vecchione C, Notte A, et al. Emilin1 links TGF-beta maturation to blood pressure homeostasis. Cell. 2006;124:929-942. doi: 10.1016/j.cell.2005.12.035.
26. Dai X, Shen J, Annam NP, Jiang H, Levi E, Schworer CM, Tromp G, Arora A, Higgins M, Wang XF, Yang M, Li HJ, Zhang K, Kuivaniemi H, Li L. SMAD3 deficiency promotes vessel wall remodeling, collagen fiber reorganization and leukocyte infiltration in an inflammatory abdominal aortic aneurysm mouse model. Sci Rep. 2015;5:10180. doi: 10.1038/srep10180.
27. Saraff K, Babamusta F, Cassis LA, Daugherty A. Aortic dissection precedes formation of aneurysms and atherosclerosis in angiotensin II-infused, apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol. 2003;23:1621-1626. doi: 10.1161/01.ATV.0000085631.76095.64.
28. Daugherty A, Cassis L. Angiotensin II-mediated development of vascular diseases. Trends Cardiovasc Med. 2004;14:117-120. doi: 10.1016/j.tcm.2004.01.002.
29. Li W, Li Q, Jiao Y, Qin L, Ali R, Zhou J, Ferruzzi J, Kim RW, Geirsson A, Dietz HC, Offermanns S, Humphrey JD, Tellides G. Tgfbr2 disruption in postnatal smooth muscle impairs aortic wall homeostasis. J Clin Invest. 2014;124:755-767. doi: 10.1172/JCI69942.
30. Torr EE, Gardner DH, Thomas L, Goodall DM, Bielemeier A, Willetts R, Griffiths HR, Marshall LJ, Devitt A. Apoptotic cell-derived ICAM-3 promotes both macrophage chemoattraction to and tethering of apoptotic cells. Cell Death Differ. 2012;19:671-679. doi: 10.1038/cdd.2011.167.
31. Postlethwaite AE, Kang AH. Collagen-and collagen peptide-induced chemotaxis of human blood monocytes. J Exp Med. 1976;143:1299-1307.
32. Hunninghake GW, Davidson JM, Rennard S, Szapiel S, Gadek JE, Crystal RG. Elastin fragments attract macrophage precursors to diseased sites in pulmonary emphysema. Science. 1981;212:925-927.
33. Reilly CF, McFall RC. Platelet-derived growth factor and transforming growth factor-beta regulate plasminogen activator inhibitor-1 synthesis in vascular smooth muscle cells. J Biol Chem. 1991;266:9419-9427.
34. Tieu BC, Ju X, Lee C, Sun H, Lejeune W, Recinos A 3rd, Brasier AR, Tilton RG. Aortic adventitial fibroblasts participate in angiotensin-induced vascular wall inflammation and remodeling. J Vasc Res. 2011;48:261-272. doi: 10.1159/000320358.
35. Police SB, Thatcher SE, Charnigo R, Daugherty A, Cassis LA. Obesity promotes inflammation in periaortic adipose tissue and angiotensin II-induced abdominal aortic aneurysm formation. Arterioscler Thromb Vasc Biol. 2009;29:1458-1464. doi: 10.1161/ATVBAHA.109.192658.
36. Daugherty A, Cassis LA, Lu H. Complex pathologies of angiotensin II-induced abdominal aortic aneurysms. J Zhejiang Univ Sci B. 2011;12:624-628. doi: 10.1631/jzus.B1101002.
37. Majesky MW, Dong XR, Hoglund V, Mahoney WM Jr, Daum G. The adventitia: A dynamic interface containing resident progenitor cells. Arterioscler Thromb Vasc Biol. 2011;31:1530-1539. doi: 10.1161/ATVBAHA.110.221549.
38. Rateri DL, Moorleghen JJ, Balakrishnan A, Owens AP 3rd, Howatt DA, Subramanian V, Poduri A, Charnigo R, Cassis LA, Daugherty A. Endothelial cell-specific deficiency of Ang II type 1a receptors attenuates Ang II-induced ascending aortic aneurysms in LDL receptor-/-mice. Circ Res. 2011;108:574-581. doi: 10.1161/CIRCRESAHA.110.222844.
39. Lei YM, Chen L, Wang Y, Stefka AT, Molinero LL, Theriault B, Aquino-Michaels K, Sivan AS, Nagler CR, Gajewski TF, Chong AS, Bartman C, Alegre ML. The composition of the microbiota modulates allograft rejection. J Clin Invest. 2016;126:2736-2744. doi: 10.1172/JCI85295.
40. Chukkapalli SS, Rivera MF, Velsko IM, Lee JY, Chen H, Zheng D, Bhattacharyya I, Gangula PR, Lucas AR, Kesavalu L. Invasion of oral and aortic tissues by oral spirochete Treponema denticola in ApoE(-/-) mice causally links periodontal disease and atherosclerosis. Infect Immun. 2014;82:1959-1967. doi: 10.1128/IAI.01511-14.
41. Mizoguchi T, Kasahara K, Yamashita T, Sasaki N, Yodoi K, Matsumoto T, Emoto T, Hayashi T, Kitano N, Yoshida N, Amin HZ, Hirata KI. Oral administration of the lactic acid bacterium pediococcus acidilacticiattenuates atherosclerosis in mice by inducing tolerogenic dendritic cells. Heart Vessels. 2017;32:768-776. doi: 10.1007/s00380-017-0949-8.
42. Bruemmer D, Daugherty A, Lu H, Rateri DL. Relevance of angiotensin II-induced aortic pathologies in mice to human aortic aneurysms. Ann NY Acad Sci. 2011;1245:7-10. doi: 10.1111/j.1749-6632.2011.06332.x.
43. Rateri DL, Moorleghen JJ, Knight V, Balakrishnan A, Howatt DA, Cassis LA, Daugherty A. Depletion of endothelial or smooth muscle cell-specific angiotensin II type 1a receptors does not influence aortic aneurysms or atherosclerosis in LDL receptor deficient mice. PLoS One. 2012;7:e51483. doi: 10.1371/journal.pone.0051483.
44. Topouzis S, Majesky MW. Smooth muscle lineage diversity in the chick embryo. Two types of aortic smooth muscle cell differ in growth and receptor-mediated transcriptional responses to transforming growth factor-beta. Dev Biol. 1996;178:430-445. doi: 10.1006/dbio.1996.0229.
45. Jaffe M, Sesti C, Washington IM, Du L, Dronadula N, Chin MT, Stolz DB, Davis EC, Dichek DA. Transforming growth factor-signaling in myogenic cells regulates vascular morphogenesis, differentiation, and matrix synthesis. Arterioscler Thromb Vasc Biol. 2012;32:e1-e11. doi: 10.1161/ATVBAHA.111.238410.
46. Mehta PK, Griendling KK. Angiotensin II cell signaling: Physiological and pathological effects in the cardiovascular system. Am J Physiol Cell Physiol. 2007;292:C82-C97. doi: 10.1152/ajpcell.00287.2006.
47. Wei H, Hu JH, Angelov SN, Fox K, Yan J, Enstrom R, Smith A, Dichek DA. Aortopathy in a mouse model of marfan syndrome is not mediated by altered transforming growth factor signaling. J Am Heart Assoc. 2017;6: E004968. doi: 10.1161/JAHA.116.004968.
48. Wendling O, Bornert JM, Chambon P, Metzger D. Efficient temporallycontrolled targeted mutagenesis in smooth muscle cells of the adult mouse. Genesis. 2009;47:14-18. doi: 10.1002/dvg.20448.
49. Gao F, Chambon P, Offermanns S, Tellides G, Kong W, Zhang X, Li W. Disruption of TGF-signaling in smooth muscle cell prevents elastaseinduced abdominal aortic aneurysm. Biochem Biophys Res Commun. 2014;454:137-143. doi: 10.1016/j.bbrc.2014.10.053.