Characterization of Proliferating Lesion-Resident Cells During All Stages of Atherosclerotic Growth

Journal of the American Heart Association

Volumn 5, Issue 8, 2016, Pages

  Lhoták, Šárka ^a,b   Gyulay, Gabriel ^a,b   Cutz, Jean Claude ^a   Al Hashimi, Ali ^a,b   Trigatti, Bernardo L ^a   Richards, Carl D ^a   Igdoura, Suleiman A ^a   Steinberg, Gregory R ^a   Bramson, Jonathan ^a   Ask, Kjetil ^a   Austin, Richard C ^a,b  

^a MCMASTER UNIVERSITY   (Canada)

^b MCMASTER UNIVERSITY   (Canada)

Author keywords

Apoptosis; Atherosclerosis; Cardiovascular disease; Lesion; Leukocyte; Macrophage; Proliferation

Indexed keywords

BROXURIDINE; DEOXYURIDINE TRIPHOSPHATE PYROPHOSPHATASE; DNA NUCLEOTIDYLEXOTRANSFERASE; KI 67 ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTERY LESION; ARTICLE; ATHEROSCLEROTIC PLAQUE; CELL DEATH; CELL GROWTH; CELL INFILTRATION; CELL PROLIFERATION; CONTROLLED STUDY; CORONARY ARTERY ATHEROSCLEROSIS; DISEASE ASSOCIATION; DISEASE CLASSIFICATION; DISEASE EXACERBATION; DISEASE SEVERITY; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; INFLAMMATORY CELL; MACROPHAGE; MALE; MONOCYTE; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; T LYMPHOCYTE; ANIMAL; AORTA; APOLIPOPROTEIN E KNOCKOUT MOUSE; CORONARY ARTERY DISEASE; CORONARY ARTERY THROMBOSIS; CORONARY BLOOD VESSEL; DISEASE MODEL; METABOLISM; PATHOLOGY; PHYSIOLOGY;

ANIMALS; AORTA; APOPTOSIS; CELL PROLIFERATION; CORONARY ARTERY DISEASE; CORONARY THROMBOSIS; CORONARY VESSELS; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; KI-67 ANTIGEN; MACROPHAGES; MALE; MICE, KNOCKOUT, APOE; T-LYMPHOCYTES;

EID: 85002645143     PISSN: None     EISSN: 20479980     Source Type: Journal    
DOI: 10.1161/JAHA.116.003945     Document Type: Article

References (40)

1. Viles-Gonzalez JF, Fuster V, Badimon JJ. Atherothrombosis: a widespread disease with unpredictable and life-threatening consequences. Eur Heart J. 2004;25:1197-1207.
2. Ross R. Atherosclerosis-an inflammatory disease. N Engl J Med. 1999;340:115-126.
3. Lusis AJ. Atherosclerosis. Nature. 2000;407:233-241.
4. Hilgendorf I, Swirski FK, Robbins CS. Monocyte fate in atherosclerosis. Arterioscler Thromb Vasc Biol. 2015;35:272-279.
5. Tabas I. Consequences and therapeutic implications of macrophage apoptosis in atherosclerosis: the importance of lesion stage and phagocytic efficiency. Arterioscler Thromb Vasc Biol. 2005;25:2255-2264.
6. Andres V, Pello OM, Silvestre-Roig C. Macrophage proliferation and apoptosis in atherosclerosis. Curr Opin Lipidol. 2012;23:429-438.
7. Murphy AJ, Tall AR. Proliferating macrophages populate established atherosclerotic lesions. Circ Res. 2014;114:236-238.
8. Zhou J, Lhotak S, Hilditch BA, Austin RC. Activation of the unfolded protein response occurs at all stages of atherosclerotic lesion development in apolipoprotein E-deficient mice. Circulation. 2005;111:1814-1821.
9. Robbins CS, Hilgendorf I, Weber GF, Theurl I, Iwamoto Y, Figueiredo JL, Gorbatov R, Sukhova GK, Gerhardt LM, Smyth D, Zavitz CC, Shikatani EA, Parsons M, van Rooijen N, Lin HY, Husain M, Libby P, Nahrendorf M, Weissleder R, Swirski FK. Local proliferation dominates lesional macrophage accumulation in atherosclerosis. Nat Med. 2013;19:1166-1172.
10. Rosenfeld ME. Macrophage proliferation in atherosclerosis: an historical perspective. Arterioscler Thromb Vasc Biol. 2014;34:e21-e22.
11. Randolph GJ. Mechanisms that regulate macrophage burden in atherosclerosis. Circ Res. 2014;114:1757-1771.
12. Randolph GJ. Proliferating macrophages prevail in atherosclerosis. Nat Med. 2013;19:1094-1095.
13. Zhu SN, Chen M, Jongstra-Bilen J, Cybulsky MI. GM-CSF regulates intimal cell proliferation in nascent atherosclerotic lesions. J Exp Med. 2009;206:2141-2149.
14. Orekhov AN, Andreeva ER, Mikhailova IA, Gordon D. Cell proliferation in normal and atherosclerotic human aorta: proliferative splash in lipid-rich lesions. Atherosclerosis. 1998;139:41-48.
15. Gordon D, Reidy MA, Benditt EP, Schwartz SM. Cell proliferation in human coronary arteries. Proc Natl Acad Sci USA. 1990;87:4600-4604.
16. Ammirati E, Moroni F, Magnoni M, Camici PG. The role of T and B cells in human atherosclerosis and atherothrombosis. Clin Exp Immunol. 2015;179:173-187.
17. Galkina E, Kadl A, Sanders J, Varughese D, Sarembock IJ, Ley K. Lymphocyte recruitment into the aortic wall before and during development of atherosclerosis is partially L-selectin dependent. J Exp Med. 2006;203:1273-1282.
18. Moos MP, John N, Grabner R, Nossmann S, Gunther B, Vollandt R, Funk CD, Kaiser B, Habenicht AJ. The lamina adventitia is the major site of immune cell accumulation in standard chow-fed apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol. 2005;25:2386-2391.
19. Yang M, Li S, Liu H, Yang G, Li L. Response to a long-term high-fat diet in the signature of genes involved in lipid metabolism in ApoE(-/-) mice. Am J Med Sci. 2013;346:211-215.
20. Zhou J, Werstuck GH, Lhotak S, Shi YY, Tedesco V, Trigatti B, Dickhout J, Majors AK, DiBello PM, Jacobsen DW, Austin RC. Hyperhomocysteinemia induced by methionine supplementation does not independently cause atherosclerosis in C57BL/6J mice. FASEB J. 2008;22:2569-2578.
21. Lhotak S, Zhou J, Austin RC. Immunohistochemical detection of the unfolded protein response in atherosclerotic plaques. Methods Enzymol. 2011;489:23-46.
22. Scholzen T, Gerdes J. The Ki-67 protein: from the known and the unknown. J Cell Physiol. 2000;182:311-322.
23. Cojocaru E, Trandafirescu M, Leon M, Cotutiu C, Foia L. Immunohistochemical expression of anti-CD68 antibody in atherosclerotic plaque. Rom J Morphol Embryol. 2012;53:61-66.
24. Yahaya B, McLachlan G, Collie DD. BrdU pulse labelling in vivo to characterise cell proliferation during regeneration and repair following injury to the airway wall in sheep. ScientificWorldJournal. 2013;2013:871932.
25. Asano M, Yamamoto T, Tsuruta T, Nishimura N, Sonoyama K. Dual labeling with 5-bromo-2'-deoxyuridine and 5-ethynyl-2'-deoxyuridine for estimation of cell migration rate in the small intestinal epithelium. Dev Growth Differ. 2015;57:68-73.
26. Mohanta SK, Yin C, Peng L, Srikakulapu P, Bontha V, Hu D, Weih F, Weber C, Gerdes N, Habenicht AJ. Artery tertiary lymphoid organs contribute to innate and adaptive immune responses in advanced mouse atherosclerosis. Circ Res. 2014;114:1772-1787.
27. Houtkamp MA, de Boer OJ, van der Loos CM, van der Wal AC, Becker AE. Adventitial infiltrates associated with advanced atherosclerotic plaques: structural organization suggests generation of local humoral immune responses. J Pathol. 2001;193:263-269.
28. McMillan GC, Duff GL. Mitotic activity in the aortic lesions of experimental cholesterol atherosclerosis of rabbits. Arch Pathol. 1948;46:179-182.
29. Brandl R, Richter T, Haug K, Wilhelm MG, Maurer PC, Nathrath W. Topographic analysis of proliferative activity in carotid endarterectomy specimens by immunocytochemical detection of the cell cycle-related antigen Ki-67. Circulation. 1997;96:3360-3368.
30. Lutgens E, de Muinck ED, Kitslaar PJ, Tordoir JH, Wellens HJ, Daemen MJ. Biphasic pattern of cell turnover characterizes the progression from fatty streaks to ruptured human atherosclerotic plaques. Cardiovasc Res. 1999;41:473-479.
31. Jawien J. The role of an experimental model of atherosclerosis: apoE-knockout mice in developing new drugs against atherogenesis. Curr Pharm Biotechnol. 2012;13:2435-2439.
32. Pendse AA, Arbones-Mainar JM, Johnson LA, Altenburg MK, Maeda N. Apolipoprotein E knock-out and knock-in mice: atherosclerosis, metabolic syndrome, and beyond. J Lipid Res. 2009;50(suppl):S178-S182.
33. Campbell KA, Lipinski MJ, Doran AC, Skaflen MD, Fuster V, McNamara CA. Lymphocytes and the adventitial immune response in atherosclerosis. Circ Res. 2012;110:889-900.
34. Matheson PJ, Dittmer ID, Beaumont BW, Merrilees MJ, Pilmore HL. The macrophage is the predominant inflammatory cell in renal allograft intimal arteritis. Transplantation. 2005;79:1658-1662.
35. Koltsova EK, Garcia Z, Chodaczek G, Landau M, McArdle S, Scott SR, von Vietinghoff S, Galkina E, Miller YI, Acton ST, Ley K. Dynamic T cell-APC interactions sustain chronic inflammation in atherosclerosis. J Clin Invest. 2012;122:3114-3126.
36. Meng X, Yang J, Dong M, Zhang K, Tu E, Gao Q, Chen W, Zhang C, Zhang Y. Regulatory T cells in cardiovascular diseases. Nat Rev Cardiol. 2015;13:167-179.
37. Kyaw T, Winship A, Tay C, Kanellakis P, Hosseini H, Cao A, Li P, Tipping P, Bobik A, Toh BH. Cytotoxic and proinflammatory CD8+ T lymphocytes promote development of vulnerable atherosclerotic plaques in apoE-deficient mice. Circulation. 2013;127:1028-1039.
38. Ligocki AJ, Niederkorn JY. Advances on non-CD4 + Foxp3+ T regulatory cells: CD8+, type 1, and double negative T regulatory cells in organ transplantation. Transplantation. 2015;99:1553-1559.
39. Martina MN, Noel S, Saxena A, Rabb H, Hamad AR. Double negative (DN) alphabeta T cells: misperception and overdue recognition. Immunol Cell Biol. 2015;93:305-310.
40. Hegyi L, Skepper JN, Cary NR, Mitchinson MJ. Foam cell apoptosis and the development of the lipid core of human atherosclerosis. J Pathol. 1996;180:423-429.