Mertk receptor mutation reduces efferocytosis efficiency and promotes apoptotic cell accumulation and plaque necrosis in atherosclerotic lesions of Apoe-/- mice

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 28, Issue 8, 2008, Pages 1421-1428

  Thorp, Edward ^a   Cui, Dongying ^a   Schrijvers, Dorien M ^a   Kuriakose, George ^a   Tabas, Ira ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

Animal models of human disease; Apoptosis; Atherosclerosis pathophysiology; Phagocytosis

Indexed keywords

APOLIPOPROTEIN E; MER TYROSINE KINASE RECEPTOR; TYROSINE KINASE RECEPTOR; UNCLASSIFIED DRUG; MERTK PROTEIN, MOUSE; ONCOPROTEIN; PROTEIN TYROSINE KINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; CONTROLLED STUDY; GENE MUTATION; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NICK END LABELING; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; ANIMAL; AORTA; DISEASE MODEL; FOAM CELL; GENETICS; MOUSE MUTANT; MUTATION; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; AORTA; APOLIPOPROTEINS E; APOPTOSIS; ATHEROSCLEROSIS; DISEASE MODELS, ANIMAL; FOAM CELLS; IN SITU NICK-END LABELING; MALE; MICE; MICE, KNOCKOUT; MUTATION; PHAGOCYTOSIS; PROTO-ONCOGENE PROTEINS; RECEPTOR PROTEIN-TYROSINE KINASES;

EID: 52449109523     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/ATVBAHA.108.167197     Document Type: Article

References (34)

1. Virmani R, Burke AP, Kolodgie FD, Farb A. Vulnerable plaque: the pathology of unstable coronary lesions. J Interv Cardiol. 2002;15: 439-446.
2. Tabas I. Consequences and therapeutic implications of macrophage apoptosis in atherosclerosis: the importance of lesion stage and phagocytic efficiency. Arteriosder Thromb Vasc Biol. 2005;25:2255-2264.
3. Schrijvers DM, De Meyer GR, Herman AG, Martinet W. Phagocytosis in atherosclerosis: Molecular mechanisms and implications for plaque progression and stability. Cardiovasc Res. 2007;73:470-480.
4. Vandivier RW, Henson PM, Douglas IS. Burying the dead: the impact of failed apoptotic cell removal (efferocytosis) on chronic inflammatory lung disease. Chest. 2006;129:1673-1682.
5. Tabas I. Mouse models of apoptosis and efferocytosis. Curr Drug Targets. In press.
6. Schrijvers DM, De Meyer GR, Kockx MM, Herman AG, Martinet W. Phagocytosis of apoptotic cells by macrophages is impaired in atherosclerosis. Arterioscler Thromb Vasc Biol. 2005;25:1256-1261.
7. Bhatia VK, Yun S, Leung V, Grimsditch DC, Benson GM, Botto MB, Boyle JJ, Haskard DO. Complement C1q reduces early atherosclerosis in low-density lipoprotein receptor-deficient mice. Am J Pathol. 2007;170: 416-426.
8. Ait-Oufella H, Kinugawa K, Zoll J, Simon T, Boddaert J, Heeneman S, Blanc-Brude O, Barateau V, Potteaux S, Merval R, Esposito B, Teissier E, Daemen MJ, Leseche G, Boulanger C, Tedgui A, Mallat Z. Lactadherin deficiency leads to apoptotic cell accumulation and accelerated atherosclerosis in mice. Circulation. 2007;115:2168-2177.
9. Aprahamian T, Rifkin I, Bonegio R, Hugel B, Freyssinet JM, Sato K, Castellot JJ Jr, Walsh K. Impaired clearance of apoptotic cells promotes synergy between atherogenesis and autoimmune disease. J Exp Med. 2004;199:1121-1131.
10. Boisvert WA, Rose DM, Boullier A, Quehenberger O, Sydlaske A, Johnson KA, Curtiss LK, Terkeltaub R. Leukocyte transglutaminase 2 expression limits atherosclerotic lesion size. Arterioscler Thromb Vasc Biol. 2006;26:563-569.
11. Nagata K, Ohashi K, Nakano T, Arita H, Zong C, Hanafusa H, Mizuno K. Identification of the product of growth arrest-specific gene 6 as a common ligand for Axl, Sky, and Mer receptor tyrosine kinases. J Biol Chem. 1996;271:30022-30027.
12. Scott RS, McMahon EJ, Pop SM, Reap EA, Caricchio R, Cohen PL, Earp HS, Matsushima GK. Phagocytosis and clearance of apoptotic cells is mediated by MER. Nature. 2001;411:207-211.
13. Cohen PL, Caricchio R, Abraham V, Camenisch TD, Jennette JC, Roubey RA, Earp HS, Matsushima G, Reap EA. Delayed apoptotic cell clearance and lupus-like autoimmunity in mice lacking the c-mer membrane tyrosine kinase. J Exp Med. 2002;196:135-140.
14. Li Y, Gerbod-Giannone MC, Seitz H, Cui D, Thorp E, Tall AR, Matsushima GK, Tabas I. Cholesterol-induced apoptotic macrophages elicit an inflammatory response in phagocytes, which is partially attenuated by the Mer receptor. J Biol Chem. 2006;281:6707-6717.
15. Feng B, Zhang D, Kuriakose G, Devlin CM, Kockx M, Tabas I. Niemann-Pick C heterozygosity confers resistance to lesional necrosis and macrophage apoptosis in murine atherosclerosis. Proc Natl Acad Sci U S A. 2003;100:10423-10428.
16. Camenisch TD, Koller BH, Earp HS, Matsushima GK. A novel receptor tyrosine kinase, Mer, inhibits TNF-alpha production and lipopolysaccharide- induced endotoxic shock. J Immunol. 1999;162:3498-3503.
17. Taylor PR, Carugati A, Fadok VA, Cook HT, Andrews M, Carroll MC, Savill JS, Henson PM, Botto M, Walport MJ. A hierarchical role for classical pathway complement proteins in the clearance of apoptotic cells in vivo. J Exp Med. 2000;192:359-366.
18. Potter PK, Cortes-Hernandez J, Quartier P, Botto M, Walport MJ. Lupus-prone mice have an abnormal response to thioglycolate and an impaired clearance of apoptotic cells. J Immunol 2003;170:3223-3232.
19. Fernandez-Hernando C, Ackah E, Yu J, Suarez Y, Murata T, Iwakiri Y, Prendergast J, Miao RQ, Birnbaum MJ, Sessa WC. Loss of aktl leads to severe atherosclerosis and occlusive coronary artery disease. Cell Metab. 2007;6:446-457.
20. Lim WS, Timmins JM, Seimon TA, Sadler A, Kolodgie FD, Virmani R, Tabas I. STAT1 is critical for apoptosis in macrophages subjected to endoplasmic reticulum stress in vitro and in advanced atherosclerotic lesions in vivo. Circulation. 2008;117:940-951.
21. Tabas I. Consequences of cellular cholesterol accumulation: basic concepts and physiological implications. J Clin Invest. 2002;110:905-911.
22. Libby P. Inflammation in atherosclerosis. Nature. 2002;420:868-874.
23. Cui D, Thorp E, Li Y, Wang N, Yvan-Charvet L, Tall AR. Tabas I. Pivota J advance: macrophages become resistant to cholesterol-induced death after phagocytosis of apoptotic cells. J Luekoc Set. 2007;82: 1040-1050.
24. Sather S, Kenyon KD, Lefkowitz JB, Liang X, Varnum BC, Henson PM, Graham DK. A soluble form of the Mer receptor tyrosine kinase inhibits macrophage clearance of apoptotic cells and platelet aggregation. Blood. 2007;109:1026-1033.
25. Canault M, Peiretti F, Kopp F, Bonardo B, Bonzi MF, Coudeyre JC, Alessi MC, Juhan-Vague I, Nalbone G. The TNF alpha converting enzyme (TACE/ADAM17) is expressed in the atherosclerotic lesions of apolipoprotein E-deficient mice: possible contribution to elevated plasma levels of soluble TNF alpha receptors. Atherosclerosis. 2006;187:82-91.
26. Melaragno MG, Fridell YW, Berk BC. The Gas6/Axl system: a novel regulator of vascular cell function. Trends Cordiovosc Med. 1999;9: 250-253.
27. Yin J, McLachlan C, Chaufour X, McGuire MA, While G, Turner V. King NJ, Hambly BD. Growth arrest-specific gene 6 expression in proliferating rabbit vascular smooth muscle cells in vitro and in vivo. Electrophoresis. 2000;21:3851-3856.
28. Clarke MC, Figg N, Maguire JJ, Davenport AP, Goddard M, Littlewood TD, Bennett MR. Apoptosis of vascular smooth muscle cells induces features of plaque vulnerability in atherosclerosis. Nat Med. 2006;12:1075-1080.
29. Cheong HS, Lee SO, Choi CB, Song YK, Shin HD, Bae SC. MERTK polymorphisms associated with risk of haematological disorders among Korean SLE patients. Rheumatology (Oxford). 2007;46:209-214.
30. Tabas I, Williams KJ, Boren J. Subendothelial lipoprotein retention as the initiating process in atherosclerosis: update and therapeutic implications. Circulation. 2007;116:1832-1844.
31. Cheruvu PK, Finn AV, Gardner C, Caplan J, Goldstein J, Stone GW, Virmani R, Muller JE. Frequency and distribution of thin-cap fibroatheroma and ruptured plaques in human coronary arteries: a pathologic study. J Am Coll Cardiol. 2007;50:940-949.
32. Braunwald E. Cardiovascular medicine at the turn of the millennium: triumphs, concerns, and opportunities. N Engl J Med. 1997;337: 1360-1369.
33. Libby P. The forgotten majority: unfinished business in cardiovascular risk reduction. J Am Coll Cardiol. 2005;46:1225-1228.
34. Virmani R, Burke AP, Kolodgie F. Morphological characteristics of coronary atherosclerosis in diabetes mellitus. Can J Cardiol. 2006;22 Suppl B:81B-84B.