Natural killer (NK) cells augment atherosclerosis by cytotoxic-dependent mechanisms

Cardiovascular Research

Volumn 102, Issue 1, 2014, Pages 128-137

  Selathurai, Ahrathy ^a,b,c   Deswaerte, Virginie ^a,b   Kanellakis, Peter ^a   Tipping, Peter ^b   Toh, Ban Hock ^b   Bobik, Alex ^a   Kyaw, Tin ^a,b  

^a BAKER IDI HEART AND DIABETES INSTITUTE   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c MONASH UNIVERSITY   (Australia)

Author keywords

Atherosclerosis; Granzyme B; NK cells; Perforin

Indexed keywords

APOLIPOPROTEIN E; GAMMA INTERFERON; GRANZYME B; INTERLEUKIN 2 RECEPTOR GAMMA; MESSENGER RNA; PERFORIN; RAG2 PROTEIN; VASCULAR CELL ADHESION MOLECULE 1; GRANZYME;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA SINUS; ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL TRANSFER; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOTOXICITY; FLOW CYTOMETRY; GAIN OF FUNCTION MUTATION; IMMUNOHISTOCHEMISTRY; INNATE IMMUNITY; LIPID DIET; LOSS OF FUNCTION MUTATION; MALE; MOUSE; NATURAL KILLER CELL; NATURAL KILLER T CELL; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION; TARGET CELL; ANIMAL; DEFICIENCY; DISEASE MODEL; IMMUNOLOGY; METABOLISM; PATHOLOGY;

ADOPTIVE TRANSFER; ANIMALS; APOLIPOPROTEINS E; ATHEROSCLEROSIS; CYTOTOXICITY, IMMUNOLOGIC; DISEASE MODELS, ANIMAL; GRANZYMES; INTERFERON-GAMMA; KILLER CELLS, NATURAL; MALE; MICE; PERFORIN;

EID: 84897009212     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvu016     Document Type: Article

References (48)

1. Vanderlaan PA, Reardon CA. Thematic review series: the immune system and athero-genesis. The unusualsuspects:anoverviewofthe minor leukocyte populationsinathero-sclerosis. J Lipid Res 2005;46:829-838.
2. Vivier E, Tomasello E, Baratin M, Walzer T, Ugolini S. Functions of natural killer cells. Nat Immunol 2008;9:503-510.
3. Jonasson L, Holm J, Skalli O, Bondjers G, Hansson GK. Regional accumulations of T cells, macrophages, and smooth muscle cells inthe human atherosclerotic plaque. Arteriosclerosis 1986;6:131-138.
4. Kosierkiewicz TA, Factor SM, Dickson DW. Immunocytochemical studies of atherosclerotic lesions of cerebral berry aneurysms. J Neuropathol Exp Neurol 1994;53: 399-406.
5. Bobryshev YV, Lord RS. Identification of natural killer cells in human atherosclerotic plaque. Atherosclerosis 2005;180:423-427.
6. Whitman SC, Rateri DL, Szilvassy SJ, Yokoyama W, Daugherty A. Depletion of natural killer cell function decreases atherosclerosis in low-density lipoprotein receptor null mice. Arterioscler Thromb Vasc Biol 2004;24:1049-1054.
7. Stephens HA. Mica and micb genes: can the enigma of their polymorphism be resolved? Trends Immunol 2001;22:378-385.
8. Schiller NK, Boisvert WA, Curtiss LK. Inflammation in atherosclerosis: lesion formation in LDL receptor-deficient mice with perforin and lyst(beige) mutations. Arterioscler Thromb Vasc Biol 2002;22:1341-1346.
9. Faigle W, Raposo G, Tenza D, Pinet V, Vogt AB, Kropshofer H et al. Deficient peptide loading and MHC class II endosomal sorting in a human genetic immunodeficiency disease: the Chediak-Higashi syndrome. J Cell Biol 1998;141:1121-1134.
10. Ward DM, Griffiths GM, Stinchcombe JC, Kaplan J. Analysis of the lysosomal storage disease Chediak-Higashi syndrome. Traffic 2000;1:816-822.
11. Getz GS. Do natural killer cells participate in a killer vascular disease? Arterioscler Thromb Vasc Biol 2002;22:1251-1253.
12. Kim S, Iizuka K, Aguila HL, Weissman IL, Yokoyama WM. Invivo natural killer cell activities revealed bynatural killer cell-deficient mice. Proc Natl Acad Sci USA 2000;97:2731-2736.
13. Kim S, Song YJ, Higuchi DA, Kang HP, Pratt JR, Yang L et al. Arrested natural killer cell development associated with transgene insertion into the atf2 locus. Blood 2006;107: 1024-1030.
14. 2/2 mice. Arterioscler Thromb Vasc Biol 2009;29:671-677.
15. Oberg L, Eriksson M, Fahlen L, Sentman CL. Expression of ly49a on T cells alters the threshold for T cell responses. Eur J Immunol 2000;30:2849-2856.
16. Kyaw T, Winship A, Tay C, Kanellakis P, Hosseini H, Cao A et al. Cytotoxic and pro-inflammatory CD8+ T lymphocytes promote development of vulnerable atherosclerotic plaques in apoe-deficient mice. Circulation 2013;127:1028-1039.
17. Smyth MJ, Crowe NY, Godfrey DI. Nk cells and NKT cells collaboratein host protection from methylcholanthrene-induced fibrosarcoma. Int Immunol 2001;13:459-463.
18. Kyaw T, Tay C, Khan A, Dumouchel V, Cao A, To K et al. Conventionalb2bcell depletion ameliorates whereas its adoptive transfer aggravates atherosclerosis. J Immul 2010;185: 4410-4419.
19. + T cell subsets and induces early resistance to leishmania major in mice. J Exp Med 1993;178:567-577.
20. Koga M, Kai H, Yasukawa H, Yamamoto T, Kawai Y, Kato S et al. Inhibition of progression and stabilization of plaques by postnatal interferon-gamma function blocking in apoe-knockout mice. Circ Res 2007;101:348-356.
21. Fehniger TA, Cai SF, Cao X, Bredemeyer AJ, Presti RM, French AR et al. Acquisition of murine NK cell cytotoxicity requires the translation of a pre-existing pool of granzyme B and perforin mRNAs. Immunity 2007;26:798-811.
22. Trapani JA, Smyth MJ. Functional significance of the perforin/granzyme cell death pathway. Nat Rev Immunol 2002;2:735-747.
23. Ait-Oufella H, Pouresmail V, Simon T, Blanc-Brude O, Kinugawa K, Merval R et al. Defective MER receptor tyrosine kinasesignaling in bone marrowcells promotes apoptotic cell accumulation and accelerates atherosclerosis. Arterioscler Thromb Vasc Biol 2008;28: 1429-1431.
24. 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.
25. Ait-Oufella H, Kinugawa K, Zoll J, Simon T, Boddaert J, Heeneman S et al. Lactadherin deficiency leads to apoptotic cell accumulation and accelerated atherosclerosis in mice. Circulation 2007;115:2168-2177.
26. Leavenworth JW, Pauza ME. Engagement oftransgenic ly49a inhibits mouse CD4 cell activation by disrupting T cell receptor, but not CD28, signaling. Cell Immunol 2009;257: 88-96.
27. Zhou X, Nicoletti A, Elhage R, Hansson GK. Transfer of CD4(+) T cells aggravates atherosclerosis in immunodeficient apolipoprotein e knockout mice. Circulation 2000;102: 2919-2922.
28. Fledderus JO, van Thienen JV, Boon RA, Dekker RJ, Rohlena J, Volger OL et al. Prolonged shear stress and klf2 suppress constitutive pro-inflammatory transcription through inhibition of atf2. Blood 2007;109:4249-4257.
29. Reimold AM, Kim J, Finberg R, Glimcher LH. Decreased immediate inflammatory gene induction in activating transcription factor-2 mutant mice. Int Immunol 2001;13: 241-248.
30. Petrovan RJ, Yuan Y, Curtiss LK. Expression of the lyst(beige) mutation is atheroprotec-tive in chow-fed apolipoprotein e-deficient mice. J Lipid Res 2008;49:429-437.
31. Wulff S, Pries R, Wollenberg B. Cytokine release of human NK cells solely triggered with poly i:C. Cell Immunol 2010;263:135-137.
32. Gupta S, Pablo AM, Jiang X, Wang N, Tall AR, Schindler C. IFN-gamma potentiates atherosclerosis in apoe knock-out mice. J Clin Investig 1997;99:2752-2761.
33. Ohta H, Wada H, Niwa T, Kirii H, Iwamoto N, Fujii H et al. Disruption of tumor necrosis factor-alpha gene diminishes the development of atherosclerosis in APOE-deficient mice. Atherosclerosis 2005;180:11-17.
34. Huber SA, Sakkinen P, Conze D, Hardin N, Tracy R. Interleukin-6 exacerbates early atherosclerosis in mice. Arterioscler Thromb Vascu Biol 1999;19:2364-2367.
35. Metkar SS, Wang B, Aguilar-Santelises M, Raja SM, Uhlin-Hansen L, Podack E et al. Cyto-toxic cell granule-mediated apoptosis: perforin delivers granzyme b-serglycin complexes into target cells without plasma membrane pore formation. Immunity 2002;16: 417-428.
36. Trapani JA, Jans P, Smyth MJ, Froelich CJ, Williams EA, Sutton VR et al. Perforin-dependent nuclear entry of granzyme B precedes apoptosis, and is not a consequence of nuclear membrane dysfunction. Cell Death Differ 1998;5:488-496.
37. Metkar SS, Wang B, Ebbs ML, Kim JH, Lee YJ, Raja SM et al. Granzyme b activates procaspase-3 which signals a mitochondrial amplification loop for maximal apoptosis. J Cell Biol 2003;160:875-885.
38. Tabas I. Macrophage death and defective inflammation resolutionin atherosclerosis. Nat Rev Immunol 2010;10:36-46.
39. Bhatia VK, Yun S, Leung V, Grimsditch DC, Benson GM, Botto MB et al. Complementc1q reduces early atherosclerosis in low-density lipoprotein receptor-deficient mice. Am J Pathol 2007;170:416-426.
40. Scaffidi P, Misteli T, Bianchi ME. Release of chromatin protein hmgb1 by necrotic cells triggers inflammation. Nature 2002;418:191-195.
41. Iyer SS, Pulskens WP, Sadler JJ, Butter LM, Teske GJ, Ulland TKet al. Necrotic cells trigger a sterile inflammatory response through the nlrp3 inflammasome. Proc Natl Acad Sci USA 2009;106:20388-20393.
42. Zheng Y, Gardner SE, Clarke MC. Celldeath, damage-associatedmolecular patterns, and sterile inflammation in cardiovascular disease. Arterioscler Thromb Vasc Biol 2011;31: 2781-2786.
43. Kanellakis P, Agrotis A, Kyaw TS, Koulis C, Ahrens I, Mori Set al. High-mobility group box protein 1 neutralization reduces development of diet-induced atherosclerosis in apoli-poprotein E-deficient mice. Arterioscler Thromb Vasc Biol 2011;31:313-319.
44. Xia M, Guerra N, Sukhova GK, Yang K, Miller CK, Shi GP et al. Immune activationresulting from nkg2d/ligand interaction promotes atherosclerosis. Circulation 2011;124: 2933-2943.
45. Gonzalez S, Lopez-Soto A, Suarez-Alvarez B, Lopez-Vazquez A, Lopez-Larrea C. Nkg2d ligands: key targets of the immune response. Trends Immunol 2008;29:397-403.
46. Jonasson L, Backteman K, Ernerudh J. Loss of natural killer cell activity in patients with coronary artery disease. Atherosclerosis 2005;183:316-321.
47. Benschop RJ, Nieuwenhuis EE, Tromp EA, Godaert GL, Ballieux RE, van Doornen LJ. Effects of beta-adrenergic blockade on immunologic and cardiovascular changes induced by mental stress. Circulation 1994;89:762-769.
48. Martin-Fontecha A, Thomsen LL, Brett S, Gerard C, Lipp M, Lanzavecchia A et al. Induced recruitment of NK cells to lymph nodes provides IFN-gamma for T(H)1 priming. Nat Immunol 2004;5:1260-1265.