Age-associated vascular inflammation promotes monocytosis during atherogenesis

Aging Cell

Volumn 15, Issue 4, 2016, Pages 766-777

  Du, Wei ^a   Wong, Christine ^a   Song, Yang ^a   Shen, Hua ^a   Mori, Daniel ^a   Rotllan, Noemi ^a   Price, Nathan ^a   Dobrian, Anca D ^b   Meng, Hailong ^a   Kleinstein, Steven H ^a,c   Fernandez Hernando, Carlos ^a   Goldstein, Daniel R ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EASTERN VIRGINIA MEDICAL SCHOOL   (United States)

^c YALE UNIVERSITY   (United States)

Author keywords

aging; inflammation and atherosclerosis; monocyte; vasculature

Indexed keywords

INTERLEUKIN 6; LOW DENSITY LIPOPROTEIN; LOW DENSITY LIPOPROTEIN CHOLESTEROL; MONOCYTE CHEMOTACTIC PROTEIN 1; OSTEOPONTIN;

AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; BONE MARROW TRANSPLANTATION; CHEMOTAXIS; CONTROLLED STUDY; ELEVATED BLOOD PRESSURE; FEMALE; HYPERLIPIDEMIA; HYPERTENSION; INSULIN RESISTANCE; LIPID DIET; LIPID STORAGE; LOW FAT DIET; MACROPHAGE; MALE; MONOCYTOSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; VASCULAR SMOOTH MUSCLE CELL; VASCULARIZATION; VASCULITIS;

EID: 84977658618     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/acel.12488     Document Type: Article

References (45)

1. Chiba TT (2011) Estrogen-dependent activation of neutral cholesterol ester hydrolase underlying gender difference of atherogenesis in apoE-/- mice. Atherosclerosis 219, 545–551.
2. Collins AR, Lyon CJ, Xia X, Liu JZ, Tangirala RK, Yin F, Boyadjian R, Bikineyeva A, Praticò D, Harrison DG, Hsueh WA (2009) Age-accelerated atherosclerosis correlates with failure to upregulate antioxidant genes. Circ. Res. 104, e42–e54.
3. Csiszar A, Sosnowska D, Wang M, Lakatta EG, Sonntag WE, Ungvari Z (2012) Age-associated proinflammatory secretory phenotype in vascular smooth muscle cells from the non-human primate Macaca mulatta: reversal by resveratrol treatment. J. Gerontol. A: Bio. Sci. Med. Sci. 67, 811–820.
4. Ding M, Rzucidlo EM, Davey JC, Xie Y, Liu R, Jin Y, Stavola L, Martin KA (2012). Chapter eleven – adiponectin in the heart and vascular system. In Vitamins & Hormones (L Gerald, ed). Vitam Horm. 90, 289–319.
5. Donato AJ, Black AD, Jablonski KL, Gano LB, Seals DR (2008) Aging is associated with greater nuclear NFκB, reduced IκBα, and increased expression of proinflammatory cytokines in vascular endothelial cells of healthy humans. Aging Cell 7, 805–812.
6. Dutta D, Calvani R, Bernabei R, Leeuwenburgh C, Marzetti E (2012) Contribution of impaired mitochondrial autophagy to cardiac aging: mechanisms and therapeutic opportunities. Circ. Res. 110, 1125–1138.
7. Fernandez-Hernando C, Ackah E, Yu J, Suarez Y, Murata T, Iwakiri Y, Prendergast J, Miao RQ, Birnbaum MJ, Sessa WC (2007) Loss of Akt1 leads to severe atherosclerosis and occlusive coronary artery disease. Cell Metab. 6, 446–457.
8. Ferrari AU, Radaelli A, Centola M (2003) Invited Review: aging and the cardiovascular system. J. Appl. Physiol. 95, 2591–2597.
9. Galkina E, Kadl A, Sanders J, Varughese D, Sarembock IJ, Ley K (2006) Lymphocyte recruitment into the aortic wall before and during development of atherosclerosis is partially L-selectin dependent. J. Exp. Med. 203, 1273–1282.
10. Gano LB, Donato AJ, Pasha HM, Hearon CM, Sindler AL, Seals DR (2014) The SIRT1 activator SRT1720 reverses vascular endothelial dysfunction, excessive superoxide production, and inflammation with aging in mice. Am. J. Physiol. Heart Circ. Physiol. 307, H1754–H1763.
11. Geiger H, de Haan G, Florian MC (2013) The ageing haematopoietic stem cell compartment. Nat. Rev. Immunol. 13, 376–389.
12. Geissmann F, Jung S, Littman DR (2003) Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 19, 71–82.
13. Getz GS, Reardon CA (2006) Diet and murine atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 26, 242–249.
14. Gioscia-Ryan RA, LaRocca TJ, Sindler AL, Zigler MC, Murphy MP, Seals DR (2014) Mitochondria-targeted antioxidant (MitoQ) ameliorates age-related arterial endothelial dysfunction in mice. J. Physiol. 592, 2549–2561.
15. Goedeke L, Salerno A, Ramírez CM, Guo L, Allen RM, Yin X, Langley SR, Esau C, Wanschel A, Fisher EA, Suárez Y, Baldán A, Mayr M, Fernández-Hernando C (2014) Long-term therapeutic silencing of miR-33 increases circulating triglyceride levels and hepatic lipid accumulation in mice. EMBO Mol. Med. 6, 1133–1141.
16. Gu L, Okada Y, Clinton SK, Gerard C, Sukhova GK, Libby P, Rollins BJ (1998) Absence of monocyte chemoattractant protein-1 reduces atherosclerosis in low density lipoprotein receptor-deficient mice. Mol. Cell 2, 275–281.
17. Hearps AC, Martin GE, Angelovich TA, Cheng W-J, Maisa A, Landay AL, Jaworowski A, Crowe SM (2012) Aging is associated with chronic innate immune activation and dysregulation of monocyte phenotype and function. Aging Cell 11, 867–875.
18. Hilgendorf I, Swirski FK, Robbins CS (2015) Monocyte fate in atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 35, 272–279.
19. Huber SA, Sakkinen P, Conze D, Hardin N, Tracy R (1999) Interleukin-6 exacerbates early atherosclerosis in mice. Arterioscler. Thromb. Vasc. Biol. 19, 2364–2367.
20. Kanda H, Tateya S, Tamori Y, Kotani K, Hiasa K, Kitazawa R, Kitazawa S, Miyachi H, Maeda S, Egashira K, Kasuga M (2006) MCP-1 contributes to macrophage infiltration into adipose tissue, insulin resistance, and hepatic steatosis in obesity. J. Clin. Invest. 116, 1494–1505.
21. Kiefer FW, Zeyda M, Gollinger K, Pfau B, Neuhofer A, Weichhart T, Säemann MD, Geyeregger R, Schlederer M, Kenner L, Stulnig TM (2010) Neutralization of osteopontin inhibits obesity-induced inflammation and insulin resistance. Diabetes 59, 935–946.
22. Liao X, Sluimer Judith C, Wang Y, Subramanian M, Brown K, Pattison JS, Robbins J, Martinez J, Tabas I (2012) Macrophage autophagy plays a protective role in advanced atherosclerosis. Cell Metab. 15, 545–553.
23. Lumeng C, Bodzin J, Saltiel A (2007) Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J. Clin. Invest. 117, 175–184.
24. Lumeng CN, Liu J, Geletka L, Delaney C, Delproposto J, Desai A, Oatmen K, Martinez-Santibanez G, Julius A, Garg S, Yung RL (2011) Aging is associated with an increase in T cells and inflammatory macrophages in visceral adipose tissue. J. Immunol. 187, 6208–6216.
25. Marchand A, Atassi F, Gaaya A, Leprince P, Le Feuvre C, Soubrier F, Lompré A-M, Nadaud S (2011) The Wnt/beta-catenin pathway is activated during advanced arterial aging in humans. Aging Cell 10, 220–232.
26. Moore KJ, Sheedy FJ, Fisher EA (2013) Macrophages in atherosclerosis: a dynamic balance. Nat. Rev. Immunol. 13, 709–721.
27. Mozaffarian D, Benjamin EJ, Go AS, Arnett DK, Blaha MJ, Cushman M, de Ferranti S, Despres JP, Fullerton HJ, Howard VJ, Huffman MD, Judd SE, Kissela BM, Lackland DT, Lichtman JH, Lisabeth LD, Liu S, Mackey RH, Matchar DB, McGuire DK, Mohler ER 3rd, Moy CS, Muntner P, Mussolino ME, Nasir K, Neumar RW, Nichol G, Palaniappan L, Pandey DK, Reeves MJ, Rodriguez CJ, Sorlie PD, Stein J, Towfighi A, Turan TN, Virani SS, Willey JZ, Woo D, Yeh RW, Turner MB, American Heart Association Statistics C, Stroke Statistics S (2015) Heart disease and stroke statistics–2015 update: a report from the American Heart Association. Circulation 131, e29–e322.
28. Pedersen BK, Febbraio MA (2007) Interleukin-6 does/does not have a beneficial role in insulin sensitivity and glucose homeostasis. J. Appl. Physiol. 102, 814–816.
29. Pereira TM, Nogueira BV, Lima LC, Porto ML, Arruda JA, Vasquez EC, Meyrelles SS (2010) Cardiac and vascular changes in elderly atherosclerotic mice: the influence of gender. Lipids Health Dis. 9, 87.
30. Rauscher FM, Goldschmidt-Clermont PJ, Davis BH, Wang T, Gregg D, Ramaswami P, Pippen AM, Annex BH, Dong C, Taylor DA (2003) Aging, progenitor cell exhaustion, and atherosclerosis. Circulation 108, 457–463.
31. Razani B, Feng C, Coleman T, Emanuel R, Wen H, Hwang S, Ting Jenny P, Virgin Herbert W, Kastan Michael B, Semenkovich Clay F (2012) Autophagy links inflammasomes to atherosclerotic progression. Cell Metab. 15, 534–544.
32. Sadeghi HM, Schnelle JF, Thoma JK, Nishanian P, Fahey JL (1999) Phenotypic and functional characteristics of circulating monocytes of elderly persons. Exp. Gerontol. 34, 959–970.
33. Scheja L, Heese B, Zitzer H, Michael MD, Siesky AM, Pospisil H, Beisiegel U, Seedorf K (2008) Acute-phase serum amyloid A as a marker of insulin resistance in mice. Exp. Diabetes Res. 2008, 11.
34. Song Y, Shen H, Schenten D, Shan P, Lee PJ, Goldstein DR (2012) Aging enhances the basal production of IL-6 and CCL2 in vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 1, 103–109.
35. Spinetti G, Wang M, Monticone R, Zhang J, Zhao D, Lakatta EG (2004) Rat aortic MCP-1 and its receptor CCR2 increase with age and alter vascular smooth muscle cell function. Arterioscler. Thromb. Vasc. Biol. 24, 1397–1402.
36. Sun Y, Byon CH, Yuan K, Chen J, Mao X, Heath JM, Javed A, Zhang K, Anderson PG, Chen Y (2012) Smooth muscle cell-specific Runx2 deficiency inhibits vascular calcification. Circ. Res. 111, 543–552.
37. Swirski FK, Libby P, Aikawa E, Alcaide P, Luscinskas FW, Weissleder R, Pittet MJ (2007) Ly-6Chi monocytes dominate hypercholesterolemia-associated monocytosis and give rise to macrophages in atheromata. J. Clin. Invest. 117, 195–205.
38. Tacke F, Alvarez D, Kaplan T, Jakubzick C, Spanbroek R, Llodra J, Garin A, Liu J, Mack M, van Rooijen N (2007) Monocyte subsets differentially employ CCR2, CCR5, and CX3CR1 to accumulate within atherosclerotic plaques. J. Clin. Invest. 117, 185–194.
39. Tchkonia T, Zhu Y, van Deursen J, Campisi J, Kirkland JL (2013) Cellular senescence and the senescent secretory phenotype: therapeutic opportunities. J. Clin. Invest. 123, 966–972.
40. Ungvari Z, Kaley G, de Cabo R, Sonntag WE, Csiszar A (2010) Mechanisms of vascular aging: new perspectives. J. Gerontol. A Biol. Sci. Med. Sci. 65A, 1028–1041.
41. Vendrov AE, Vendrov KC, Smith A, Yuan J, Sumida A, Robidoux J, Runge MS, Madamanchi NR (2015) NOX4 NADPH oxidase-dependent mitochondrial oxidative stress in aging-associated cardiovascular disease. Antioxid. Redox Signal. 23, 1389–1409.
42. Wang JC, Bennett M (2012) Aging and atherosclerosis: mechanisms, functional consequences, and potential therapeutics for cellular senescence. Circ. Res. 111, 245–259.
43. Wang M, Fu Z, Wu J, Zhang J, Jiang L, Khazan B, Telljohann R, Zhao M, Krug AW, Pikilidou M, Monticone RE, Wersto R, Van Eyk J, Lakatta EG (2012) MFG-E8 activates proliferation of vascular smooth muscle cells via integrin signaling. Aging Cell 11, 500–508.
44. Wang M, Jiang L, Monticone RE, Lakatta EG (2014) Proinflammation: the key to arterial aging. Trends Endocrinol. Metab. 25, 72–79.
45. Woollard KJ, Geissmann F (2010) Monocytes in atherosclerosis: subsets and functions. Nat. Rev. Cardiol. 7, 77–86.