Leukocyte-specific CCL3 deficiency inhibits atherosclerotic lesion development by affecting neutrophil accumulation

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 33, Issue 3, 2013, Pages

  De Jager, Saskia C A ^a   Bot, Ilze ^a   Kraaijeveld, Adriaan O ^a,b   Korporaal, Suzanne J A ^a,c   Bot, Martine ^a   Van Santbrink, Peter J ^a   Van Berkel, Theo J C ^a   Kuiper, Johan ^a   Biessen, Erik A L ^a,d  

^a LEIDEN UNIVERSITY   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^d MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

atherosclerosis; chemokines; inflammation; neutrophils

Indexed keywords

CHEMOKINE RECEPTOR CXCR2; COLLAGEN; CXCL1 CHEMOKINE; LIPOPOLYSACCHARIDE; LOW DENSITY LIPOPROTEIN RECEPTOR; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MONOCYTE CHEMOTACTIC PROTEIN 1; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA SINUS; ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; BONE MARROW; CELL ADHESION; CHIMERA; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; FEMALE; HEMATOPOIETIC CELL; INFLAMMATION; LEUKOCYTE; LEUKOCYTE MIGRATION; MACROPHAGE; MONOCYTE; MOUSE; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NEUTROPHIL COUNT; NONHUMAN; PRIORITY JOURNAL; VASCULAR SMOOTH MUSCLE;

ANIMALS; APOPTOSIS; BONE MARROW TRANSPLANTATION; CAROTID ARTERY DISEASES; CAROTID ARTERY, COMMON; CELL ADHESION; CELLS, CULTURED; CHEMOKINE CCL3; CHEMOKINE CXCL1; CHEMOTAXIS, LEUKOCYTE; CYCLOPHOSPHAMIDE; DIETARY FATS; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION REGULATION; LEUKOCYTES; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUTROPENIA; NEUTROPHIL INFILTRATION; NEUTROPHILS; PLAQUE, ATHEROSCLEROTIC; RECEPTORS, LDL; RNA, MESSENGER; TIME FACTORS; WHOLE-BODY IRRADIATION;

EID: 84874387655     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.112.300857     Document Type: Article

References (43)

1. Ross R. Atherosclerosis-an inflammatory disease. N Engl J Med. 1999;340:115-126.
2. Hansson GK. Inflammation and immune response in atherosclerosis. Curr Atheroscler Rep. 1999;1:150-155.
3. Baetta R, Corsini A. Role of polymorphonuclear neutrophils in atherosclerosis: current state and future perspectives. Atherosclerosis. 2010;210:1-13.
4. van Leeuwen M, Gijbels MJ, Duijvestijn A, Smook M, van de Gaar MJ, Heeringa P, de Winther MP, Tervaert JW. Accumulation of myeloperoxidase-positive neutrophils in atherosclerotic lesions in LDLR-/-mice. Arterioscler Thromb Vasc Biol. 2008;28:84-89.
5. Rotzius P, Thams S, Soehnlein O, Kenne E, Tseng CN, Björkström NK, Malmberg KJ, Lindbom L, Eriksson EE. Distinct infiltration of neutrophils in lesion shoulders in ApoE-/-mice. Am J Pathol. 2010;177:493-500.
6. Zernecke A, Bot I, Djalali-Talab Y, Shagdarsuren E, Bidzhekov K, Meiler S, Krohn R, Schober A, Sperandio M, Soehnlein O, Bornemann J, Tacke F, Biessen EA, Weber C. Protective role of CXC receptor 4/CXC ligand 12 unveils the importance of neutrophils in atherosclerosis. Circ Res. 2008;102:209-217.
7. Drechsler M, Megens RT, van Zandvoort M, Weber C, Soehnlein O. Hyperlipidemia-triggered neutrophilia promotes early atherosclerosis. Circulation. 2010;122:1837-1845.
8. Naruko T, Ueda M, Haze K, van der Wal AC, van der Loos CM, Itoh A, Komatsu R, Ikura Y, Ogami M, Shimada Y, Ehara S, Yoshiyama M, Takeuchi K, Yoshikawa J, Becker AE. Neutrophil infiltration of culprit lesions in acute coronary syndromes. Circulation. 2002;106:2894-2900.
9. Haumer M, Amighi J, Exner M, Mlekusch W, Sabeti S, Schlager O, Schwarzinger I, Wagner O, Minar E, Schillinger M. Association of neutrophils and future cardiovascular events in patients with peripheral artery disease. J Vasc Surg. 2005;41:610-617.
10. Toor IS, Jaumdally RJ, Moss MS, Babu SB. Preprocedural neutrophil count predicts outcome in patients with advanced peripheral vascular disease undergoing percutaneous transluminal angioplasty. J Vasc Surg. 2008;48:1504-1508.
11. Cojocaru IM, Cojocaru M, Iliescu I, Botnaru L, Gurban CV, Sfrijan F, T?n?sescu R. Plasma myeloperoxidase levels in patients with acute ischemic stroke. Rom J Intern Med. 2010;48:101-104.
12. Kraaijeveld AO, de Jager SC, van Berkel TJ, Biessen EA, Jukema JW. Chemokines and atherosclerotic plaque progression: towards therapeutic targeting? Curr Pharm Des. 2007;13:1039-1052.
13. Moos MP, John N, Gräbner R, Nossmann S, Günther 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.
14. Weber C. Platelets and chemokines in atherosclerosis: partners in crime. Circ Res. 2005;96:612-616.
15. Saraswathi V, Hasty AH. The role of lipolysis in mediating the proinflammatory effects of very low density lipoproteins in mouse peritoneal macrophages. J Lipid Res. 2006;47:1406-1415.
16. Ying S, Meng Q, Barata LT, Kay AB. Macrophage inflammatory protein-1alpha and C-C chemokine receptor-1 in allergen-induced skin latephase reactions: relationship to macrophages, neutrophils, basophils, eosinophils and T lymphocytes. Clin Exp Allergy. 2001;31:1724-1731.
17. Montecucco F, Steffens S, Burger F, Da Costa A, Bianchi G, Bertolotto M, Mach F, Dallegri F, Ottonello L. Tumor necrosis factor-alpha (TNFalpha) induces integrin CD11b/CD18 (Mac-1) up-regulation and migration to the CC chemokine CCL3 (MIP-1alpha) on human neutrophils through defined signalling pathways. Cell Signal. 2008;20:557-568.
18. Miyazaki D, Nakamura T, Toda M, Cheung-Chau KW, Richardson RM, Ono SJ. Macrophage inflammatory protein-1alpha as a costimulatory signal for mast cell-mediated immediate hypersensitivity reactions. J Clin Invest. 2005;115:434-442.
19. Ardigo D, Assimes TL, Fortmann SP, Go AS, Hlatky M, Hytopoulos E, Iribarren C, Tsao PS, Tabibiazar R, Quertermous T; ADVANCE Investigators. Circulating chemokines accurately identify individuals with clinically significant atherosclerotic heart disease. Physiol Genomics. 2007;31:402-409.
20. de Jager SC, Kraaijeveld AO, Grauss RW, de Jager W, Liem SS, van der Hoeven BL, Prakken BJ, Putter H, van Berkel TJ, Atsma DE, Schalij MJ, Jukema JW, Biessen EA. CCL3 (MIP-1 alpha) levels are elevated during acute coronary syndromes and show strong prognostic power for future ischemic events. J Mol Cell Cardiol. 2008;45:446-452.
21. de Jager SC, Bongaerts BW, Weber M, Kraaijeveld AO, Rousch M, Dimmeler S, van Dieijen-Visser MP, Cleutjens KB, Nelemans PJ, van Berkel TJ, Biessen EA. Chemokines CCL3/MIP1α, CCL5/RANTES and CCL18/PARC are independent risk predictors of short-term mortality in patients with acute coronary syndromes. PLoS ONE. 2012;7:e45804.
22. von der Thüsen JH, van Berkel TJ, Biessen EA. Induction of rapid atherogenesis by perivascular carotid collar placement in apolipoprotein E-deficient and low-density lipoprotein receptor-deficient mice. Circulation. 2001;103:1164-1170.
23. Korporaal SJ, Meurs I, Hauer AD, Hildebrand RB, Hoekstra M, Cate HT, Praticò D, Akkerman JW, Van Berkel TJ, Kuiper J, Van Eck M. Deletion of the high-density lipoprotein receptor scavenger receptor BI in mice modulates thrombosis susceptibility and indirectly affects platelet function by elevation of plasma free cholesterol. Arterioscler Thromb Vasc Biol. 2011;31:34-42.
24. Hasenberg M, Köhler A, Bonifatius S, Borucki K, Riek-Burchardt M, Achilles J, Männ L, Baumgart K, Schraven B, Gunzer M. Rapid immunomagnetic negative enrichment of neutrophil granulocytes from murine bone marrow for functional studies in vitro and in vivo. PLoS ONE. 2011;6:e17314.
25. Zuluaga AF, Salazar BE, Rodriguez CA, Zapata AX, Agudelo M, Vesga O. Neutropenia induced in outbred mice by a simplified low-dose cyclophosphamide regimen: characterization and applicability to diverse experimental models of infectious diseases. BMC Infect Dis. 2006;6:55.
26. Spellberg BJ, Collins M, French SW, Edwards JE Jr, Fu Y, Ibrahim AS. A phagocytic cell line markedly improves survival of infected neutropenic mice. J Leukoc Biol. 2005;78:338-344.
27. Bot I, de Vries H, Korporaal SJ, Foks AC, Bot M, van Veldhoven J, Ter Borg MN, van Santbrink PJ, van Berkel TJ, Kuiper J, Ijzerman AP. Adenosine A2B receptor agonism inhibits neointimal lesion development after arterial injury in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol. 2012;32:2197-2205.
28. Shah SK, Jimenez F, Walker PA, Aroom KR, Xue H, Feeley TD, Uray KS, Norbury KC, Stewart RH, Laine GA, Cox CS Jr. A novel mechanism for neutrophil priming in trauma: potential role of peritoneal fluid. Surgery. 2010;148:263-270.
29. Kishimoto TK, Jutila MA, Berg EL, Butcher EC. Neutrophil Mac-1 and MEL-14 adhesion proteins inversely regulated by chemotactic factors. Science. 1989;245:1238-1241.
30. Charo IF, Taubman MB. Chemokines in the pathogenesis of vascular disease. Circ Res. 2004;95:858-866.
31. Braunersreuther V, Zernecke A, Arnaud C, Liehn EA, Steffens S, Shagdarsuren E, Bidzhekov K, Burger F, Pelli G, Luckow B, Mach F, Weber C. CCR5 but not CCR1 deficiency reduces development of diet-induced atherosclerosis in mice. Arterioscler Thromb Vasc Biol. 2007;27:373-379.
32. Potteaux S, Combadière C, Esposito B, Casanova S, Merval R, Ardouin P, Gao JL, Murphy PM, Tedgui A, Mallat Z. Chemokine receptor CCR1 disruption in bone marrow cells enhances atherosclerotic lesion development and inflammation in mice. Mol Med. 2005;11:16-20.
33. Kuziel WA, Dawson TC, Quinones M, Garavito E, Chenaux G, Ahuja SS, Reddick RL, Maeda N. CCR5 deficiency is not protective in the early stages of atherogenesis in apoE knockout mice. Atherosclerosis. 2003;167:25-32.
34. Potteaux S, Combadière C, Esposito B, Lecureuil C, Ait-Oufella H, Merval R, Ardouin P, Tedgui A, Mallat Z. Role of bone marrow-derived CC-chemokine receptor 5 in the development of atherosclerosis of lowdensity lipoprotein receptor knockout mice. Arterioscler Thromb Vasc Biol. 2006;26:1858-1863.
35. Veillard NR, Kwak B, Pelli G, Mulhaupt F, James RW, Proudfoot AE, Mach F. Antagonism of RANTES receptors reduces atherosclerotic plaque formation in mice. Circ Res. 2004;94:253-261.
36. Kasama T, Strieter RM, Standiford TJ, Burdick MD, Kunkel SL. Expression and regulation of human neutrophil-derived macrophage inflammatory protein 1 alpha. J Exp Med. 1993;178:63-72.
37. Harrison LM, van den Hoogen C, van Haaften WC, Tesh VL. Chemokine expression in the monocytic cell line THP-1 in response to purified shiga toxin 1 and/or lipopolysaccharides. Infect Immun. 2005;73:403-412.
38. Luo HR, Loison F. Constitutive neutrophil apoptosis: mechanisms and regulation. Am J Hematol. 2008;83:288-295.
39. Savill J. Apoptosis in resolution of inflammation. J Leukoc Biol. 1997;61:375-380.
40. Whyte MK, Meagher LC, MacDermot J, Haslett C. Impairment of function in aging neutrophils is associated with apoptosis. J Immunol. 1993;150:5124-5134.
41. Martin C, Burdon PC, Bridger G, Gutierrez-Ramos JC, Williams TJ, Rankin SM. Chemokines acting via CXCR2 and CXCR4 control the release of neutrophils from the bone marrow and their return following senescence. Immunity. 2003;19:583-593.
42. Suratt BT, Petty JM, Young SK, Malcolm KC, Lieber JG, Nick JA, Gonzalo JA, Henson PM, Worthen GS. Role of the CXCR4/SDF-1 chemokine axis in circulating neutrophil homeostasis. Blood. 2004;104:565-571.
43. Eash KJ, Means JM, White DW, Link DC. CXCR4 is a key regulator of neutrophil release from the bone marrow under basal and stress granulopoiesis conditions. Blood. 2009;113:4711-4719.