CD1d deficiency inhibits the development of abdominal aortic aneurysms in LDL receptor deficient mice

PLoS ONE

Volumn 13, Issue 1, 2018, Pages

  Van Puijvelde, Gijs H M ^a   Foks, Amanda C ^a   van Bochove, Rosemarie E ^a   Bot, Ilze ^a   Habets, Kim L L ^a   De Jager, Saskia C ^a   ter Borg, Mariëtte N D ^a   van Osch, Puck ^a   Boon, Louis ^b   Vos, Mariska ^c   De Waard, Vivian ^c   Kuiper, Johan ^a  

^a LEIDEN UNIVERSITY   (Netherlands)

^b BIOCEROS   (Netherlands)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN II; CD1D ANTIGEN; CYTOKINE; LOW DENSITY LIPOPROTEIN RECEPTOR; CD1D1 PROTEIN, MOUSE;

ABDOMINAL AORTIC ANEURYSM; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL EXPANSION; CELL VIABILITY; CHOLESTEROL BLOOD LEVEL; COMPARATIVE STUDY; CONTROLLED STUDY; DEATH; DISEASE SEVERITY; ENZYME DEGRADATION; ENZYME INHIBITION; EXPERIMENTAL ANEURYSM; HYPERLIPIDEMIA; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATORY CELL; MACROPHAGE; MALE; MOUSE; NATURAL KILLER T CELL; NONHUMAN; TARGET CELL; TYPE 1 NATURAL KILLER T CELL; VASCULAR SMOOTH MUSCLE CELL; ANIMAL; APOPTOSIS; C57BL MOUSE; FLOW CYTOMETRY; GENETICS; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; NIH 3T3 CELL LINE; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; TRANSGENIC MOUSE; VASCULAR SMOOTH MUSCLE;

ANGIOTENSIN II; ANIMALS; ANTIGENS, CD1D; AORTIC ANEURYSM, ABDOMINAL; APOPTOSIS; FLOW CYTOMETRY; LYMPHOCYTE ACTIVATION; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUSCLE, SMOOTH, VASCULAR; NATURAL KILLER T-CELLS; NIH 3T3 CELLS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, LDL;

EID: 85040778152     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0190962     Document Type: Article

References (56)

1. Upchurch GR Jr., Schaub TA. Abdominal aortic aneurysm. Am Fam Physician. 2006; 73(7):1198–204. PMID: 16623206.
2. Silverstein MD, Pitts SR, Chaikof EL, Ballard DJ. Abdominal aortic aneurysm (AAA): cost-effectiveness of screening, surveillance of intermediate-sized AAA, and management of symptomatic AAA. Proc (Bayl Univ Med Cent). 2005; 18(4):345–67. PMID: 16252027; PubMed Central PMCID: PMC1255946.
3. Shimizu K, Mitchell RN, Libby P. Inflammation and cellular immune responses in abdominal aortic aneurysms. Arterioscler Thromb Vasc Biol. 2006; 26(5):987–94. Epub 2006/02/25. https://doi.org/10.1161/01.ATV.0000214999.12921.4f PMID: 16497993.
4. Moehle CW, Bhamidipati CM, Alexander MR, Mehta GS, Irvine JN, Salmon M, et al. Bone marrow-derived MCP1 required for experimental aortic aneurysm formation and smooth muscle phenotypic modulation. J Thorac Cardiovasc Surg. 2011; 142(6):1567–74. Epub 2011/10/15. https://doi.org/10.1016/j.jtcvs.2011.07.053 PMID: 21996300.
5. de Waard V, Bot I, de Jager SC, Talib S, Egashira K, de Vries MR, et al. Systemic MCP1/CCR2 blockade and leukocyte specific MCP1/CCR2 inhibition affect aortic aneurysm formation differently. Atherosclerosis. 2010; 211(1):84–9. Epub 2010/03/04. https://doi.org/10.1016/j.atherosclerosis.2010.01.042PMID: 20197192.
6. Golledge J, Clancy P, Moran C, Biros E, Rush C, Walker P, et al. The novel association of the chemo-kine CCL22 with abdominal aortic aneurysm. Am J Pathol. 2010; 176(5):2098–106. Epub 2010/03/30. https://doi.org/10.2353/ajpath.2010.090416 PMID: 20348247; PubMed Central PMCID: PMC2861076.
7. Ocana E, Perez-Requena J, Bohorquez JC, Brieva JA, Rodriguez C. Chemokine receptor expression on infiltrating lymphocytes from abdominal aortic aneurysms: role of CXCR4-CXCL12 in lymphoid recruitment. Atherosclerosis. 2008; 200(2):264–70. https://doi.org/10.1016/j.atherosclerosis.2007.12. 043 PMID: 18281050.
8. Middleton RK, Lloyd GM, Bown MJ, Cooper NJ, London NJ, Sayers RD. The pro-inflammatory and che-motactic cytokine microenvironment of the abdominal aortic aneurysm wall: a protein array study. J Vasc Surg. 2007; 45(3):574–80. https://doi.org/10.1016/j.jvs.2006.11.020 PMID: 17321344.
9. Golledge AL, Walker P, Norman PE, Golledge J. A systematic review of studies examining inflammation associated cytokines in human abdominal aortic aneurysm samples. Dis Markers. 2009; 26(4):181–8. https://doi.org/10.3233/DMA-2009-0629 PMID: 19729799; PubMed Central PMCID: PMC3833704.
10. Golledge J, Muller J, Daugherty A, Norman P. Abdominal aortic aneurysm: pathogenesis and implications for management. Arterioscler Thromb Vasc Biol. 2006; 26(12):2605–13. Epub 2006/09/16. https://doi.org/10.1161/01.ATV.0000245819.32762.cb PMID: 16973970.
11. Xiong W, Zhao Y, Prall A, Greiner TC, Baxter BT. Key roles of CD4+ T cells and IFN-gamma in the development of abdominal aortic aneurysms in a murine model. J Immunol. 2004; 172(4):2607–12. PMID: 14764734.
12. Yodoi K, Yamashita T, Sasaki N, Kasahara K, Emoto T, Matsumoto T, et al. Foxp3+ regulatory T cells play a protective role in angiotensin II-induced aortic aneurysm formation in mice. Hypertension. 2015; 65(4):889–95. https://doi.org/10.1161/HYPERTENSIONAHA.114.04934 PMID: 25601931.
13. Xiong W, MacTaggart J, Knispel R, Worth J, Persidsky Y, Baxter BT. Blocking TNF-alpha attenuates aneurysm formation in a murine model. J Immunol. 2009; 183(4):2741–6. Epub 2009/07/22. https://doi.org/10.4049/jimmunol.0803164 PMID: 19620291.
14. Galle C, Schandene L, Stordeur P, Peignois Y, Ferreira J, Wautrecht JC, et al. Predominance of type 1 CD4+ T cells in human abdominal aortic aneurysm. Clin Exp Immunol. 2005; 142(3):519–27. Epub 2005/11/22. https://doi.org/10.1111/j.1365-2249.2005.02938.x PMID: 16297165; PubMed Central PMCID: PMC1809544.
15. Harrison SC, Smith AJ, Jones GT, Swerdlow DI, Rampuri R, Bown MJ, et al. Interleukin-6 receptor pathways in abdominal aortic aneurysm. Eur Heart J. 2012. Epub 2012/11/01. https://doi.org/10.1093/eurheartj/ehs354 PMID: 23111417.
16. Johnston WF, Salmon M, Su G, Lu G, Stone ML, Zhao Y, et al. Genetic and pharmacologic disruption of interleukin-1beta signaling inhibits experimental aortic aneurysm formation. Arterioscler Thromb Vasc Biol. 2013; 33(2):294–304. Epub 2013/01/05. https://doi.org/10.1161/ATVBAHA.112.300432PMID: 23288154.
17. Bown MJ, Lloyd GM, Sandford RM, Thompson JR, London NJ, Samani NJ, et al. The interleukin-10-1082’A’ allele and abdominal aortic aneurysms. J Vasc Surg. 2007; 46(4):687–93. Epub 2007/10/02. https://doi.org/10.1016/j.jvs.2007.06.025 PMID: 17903648.
18. Shimizu K, Shichiri M, Libby P, Lee RT, Mitchell RN. Th2-predominant inflammation and blockade of IFN-gamma signaling induce aneurysms in allografted aortas. J Clin Invest. 2004; 114(2):300–8. Epub 2004/07/16. https://doi.org/10.1172/JCI19855 PMID: 15254597; PubMed Central PMCID: PMC449742.
19. Xu J, Ehrman B, Graham LM, Eagleton MJ. Interleukin-5 is a potential mediator of angiotensin II-induced aneurysm formation in apolipoprotein E knockout mice. J Surg Res. 2012; 178(1):512–8. Epub 2012/03/31. https://doi.org/10.1016/j.jss.2011.12.016 PMID: 22459292; PubMed Central PMCID: PMC3394914.
20. Chan WL, Pejnovic N, Hamilton H, Liew TV, Popadic D, Poggi A, et al. Atherosclerotic abdominal aortic aneurysm and the interaction between autologous human plaque-derived vascular smooth muscle cells, type 1 NKT, and helper T cells. Circ Res. 2005; 96(6):675–83. Epub 2005/02/26. https://doi.org/10.1161/01.RES.0000160543.84254.f1 PMID: 15731463.
21. Tupin E, Nicoletti A, Elhage R, Rudling M, Ljunggren HG, Hansson GK, et al. CD1d-dependent activation of NKT cells aggravates atherosclerosis. J Exp Med. 2004; 199(3):417–22. https://doi.org/10.1084/jem.20030997 PMID: 14744994; PubMed Central PMCID: PMC2211791.
22. Nakai Y, Iwabuchi K, Fujii S, Ishimori N, Dashtsoodol N, Watano K, et al. Natural killer T cells accelerate atherogenesis in mice. Blood. 2004; 104(7):2051–9. https://doi.org/10.1182/blood-2003-10-3485PMID: 15113755.
23. Aslanian AM, Chapman HA, Charo IF. Transient role for CD1d-restricted natural killer T cells in the formation of atherosclerotic lesions. Arterioscler Thromb Vasc Biol. 2005; 25(3):628–32. https://doi.org/10.1161/01.ATV.0000153046.59370.13 PMID: 15591216.
24. van Puijvelde GH, Kuiper J. NKT cells in cardiovascular diseases. Eur J Pharmacol. 2017. https://doi.org/10.1016/j.ejphar.2017.03.052 PMID: 28363745.
25. Chan WL, Pejnovic N, Liew TV, Hamilton H. Predominance of Th2 response in human abdominal aortic aneurysm: mistaken identity for IL-4-producing NK and NKT cells? Cell Immunol. 2005; 233(2):109–14. Epub 2005/06/21. https://doi.org/10.1016/j.cellimm.2005.04.020 PMID: 15963967.
26. Sasaguri T, Arima N, Tanimoto A, Shimajiri S, Hamada T, Sasaguri Y. A role for interleukin 4 in production of matrix metalloproteinase 1 by human aortic smooth muscle cells. Atherosclerosis. 1998; 138 (2):247–53. PMID: 9690907.
27. Chizzolini C, Rezzonico R, De Luca C, Burger D, Dayer JM. Th2 cell membrane factors in association with IL-4 enhance matrix metalloproteinase-1 (MMP-1) while decreasing MMP-9 production by granulo-cyte-macrophage colony-stimulating factor-differentiated human monocytes. J Immunol. 2000; 164 (11):5952–60. Epub 2000/05/23. PMID: 10820278.
28. Winzler C, Rovere P, Rescigno M, Granucci F, Penna G, Adorini L, et al. Maturation stages of mouse dendritic cells in growth factor-dependent long-term cultures. J Exp Med. 1997; 185(2):317–28. PMID: 9016880; PubMed Central PMCID: PMCPMC2196118.
29. Lantz O, Bendelac A. An invariant T cell receptor alpha chain is used by a unique subset of major histo-compatibility complex class I-specific CD4+ and CD4-8- T cells in mice and humans. J Exp Med. 1994; 180(3):1097–106. PMID: 7520467; PubMed Central PMCID: PMCPMC2191643.
30. Michon IN, Hauer AD, von der Thusen JH, Molenaar TJ, van Berkel TJ, Biessen EA, et al. Targeting of peptides to restenotic vascular smooth muscle cells using phage display in vitro and in vivo. Biochim Biophys Acta. 2002; 1591(1–3):87–97. PMID: 12183059.
31. Daugherty A, Manning MW, Cassis LA. Angiotensin II promotes atherosclerotic lesions and aneurysms in apolipoprotein E-deficient mice. J Clin Invest. 2000; 105(11):1605–12. Epub 2000/06/07. https://doi.org/10.1172/JCI7818 PMID: 10841519; PubMed Central PMCID: PMC300846.
32. Liu J, Lu H, Howatt DA, Balakrishnan A, Moorleghen JJ, Sorci-Thomas M, et al. Associations of ApoAI and ApoB-containing lipoproteins with AngII-induced abdominal aortic aneurysms in mice. Arterioscler Thromb Vasc Biol. 2015; 35(8):1826–34. https://doi.org/10.1161/ATVBAHA.115.305482 PMID: 26044581; PubMed Central PMCID: PMCPMC4514578.
33. Manning MW, Cassi LA, Huang J, Szilvassy SJ, Daugherty A. Abdominal aortic aneurysms: fresh insights from a novel animal model of the disease. Vasc Med. 2002; 7(1):45–54. Epub 2002/06/27. https://doi.org/10.1191/1358863x02vm413ra PMID: 12083734.
34. Daugherty A, Cassis LA, Lu H. Complex pathologies of angiotensin II-induced abdominal aortic aneurysms. J Zhejiang Univ Sci B. 2011; 12(8):624–8. Epub 2011/07/29. https://doi.org/10.1631/jzus. B1101002 PMID: 21796801; PubMed Central PMCID: PMC3150714.
35. Wang YX CL, Daugherty A. Angiotensin II-induced abdominal aortic aneurysms. In: Q X, editor. A Handbook of Mouse Models for Cardiovascular Disease: John Wiley & Sons; 2006. p. 125–36.
36. Burdin N, Brossay L, Koezuka Y, Smiley ST, Grusby MJ, Gui M, et al. Selective ability of mouse CD1 to present glycolipids: alpha-galactosylceramide specifically stimulates V alpha 14+ NK T lymphocytes. J Immunol. 1998; 161(7):3271–81. PMID: 9759842.
37. Oki S, Tomi C, Yamamura T, Miyake S. Preferential T(h)2 polarization by OCH is supported by incompetent NKT cell induction of CD40L and following production of inflammatory cytokines by bystander cells in vivo. Int Immunol. 2005; 17(12):1619–29. https://doi.org/10.1093/intimm/dxh342 PMID: 16291659.
38. Chiba A, Oki S, Miyamoto K, Hashimoto H, Yamamura T, Miyake S. Suppression of collagen-induced arthritis by natural killer T cell activation with OCH, a sphingosine-truncated analog of alpha-galactosylceramide. Arthritis Rheum. 2004; 50(1):305–13. https://doi.org/10.1002/art.11489 PMID: 14730629.
39. Schonbeck U, Sukhova GK, Gerdes N, Libby P. T(H)2 predominant immune responses prevail in human abdominal aortic aneurysm. Am J Pathol. 2002; 161(2):499–506. https://doi.org/10.1016/ S0002-9440(10)64206-X PMID: 12163375; PubMed Central PMCID: PMC1850720.
40. Cao RY, Amand T, Ford MD, Piomelli U, Funk CD. The Murine Angiotensin II-Induced Abdominal Aortic Aneurysm Model: Rupture Risk and Inflammatory Progression Patterns. Front Pharmacol. 2010; 1:9. https://doi.org/10.3389/fphar.2010.00009 PMID: 21713101; PubMed Central PMCID: PMC3112241.
41. Owens AP 3rd, Rateri DL, Howatt DA, Moore KJ, Tobias PS, Curtiss LK, et al. MyD88 deficiency attenuates angiotensin II-induced abdominal aortic aneurysm formation independent of signaling through Toll-like receptors 2 and 4. Arterioscler Thromb Vasc Biol. 2011; 31(12):2813–9. https://doi.org/10.1161/ATVBAHA.111.238642 PMID: 21960563; PubMed Central PMCID: PMC3220737.
42. Benigni A, Cassis P, Remuzzi G. Angiotensin II revisited: new roles in inflammation, immunology and aging. EMBO Mol Med. 2010; 2(7):247–57. https://doi.org/10.1002/emmm.201000080 PMID: 20597104; PubMed Central PMCID: PMC3377325.
43. Nahmod KA, Vermeulen ME, Raiden S, Salamone G, Gamberale R, Fernandez-Calotti P, et al. Control of dendritic cell differentiation by angiotensin II. FASEB J. 2003; 17(3):491–3. https://doi.org/10.1096/fj. 02-0755fje PMID: 12514109.
44. Nahmod K, Gentilini C, Vermeulen M, Uharek L, Wang Y, Zhang J, et al. Impaired function of dendritic cells deficient in angiotensin II type 1 receptors. J Pharmacol Exp Ther. 2010; 334(3):854–62. https://doi.org/10.1124/jpet.109.161760 PMID: 20516139.
45. Zhang JD, Patel MB, Song YS, Griffiths R, Burchette J, Ruiz P, et al. A novel role for type 1 angiotensin receptors on T lymphocytes to limit target organ damage in hypertension. Circ Res. 2012; 110 (12):1604–17. https://doi.org/10.1161/CIRCRESAHA.111.261768 PMID: 22534490; PubMed Central PMCID: PMC3393036.
46. Hoch NE, Guzik TJ, Chen W, Deans T, Maalouf SA, Gratze P, et al. Regulation of T-cell function by endogenously produced angiotensin II. Am J Physiol Regul Integr Comp Physiol. 2009; 296(2):R208–16. https://doi.org/10.1152/ajpregu.90521.2008 PMID: 19073907; PubMed Central PMCID: PMC2643984.
47. Balce DR, Li B, Allan ER, Rybicka JM, Krohn RM, Yates RM. Alternative activation of macrophages by IL-4 enhances the proteolytic capacity of their phagosomes through synergistic mechanisms. Blood. 2011; 118(15):4199–208. https://doi.org/10.1182/blood-2011-01-328906 PMID: 21846901.
48. Kahnert A, Seiler P, Stein M, Bandermann S, Hahnke K, Mollenkopf H, et al. Alternative activation deprives macrophages of a coordinated defense program to Mycobacterium tuberculosis. Eur J Immunol. 2006; 36(3):631–47. https://doi.org/10.1002/eji.200535496 PMID: 16479545.
49. Sukhova GK, Shi GP, Simon DI, Chapman HA, Libby P. Expression of the elastolytic cathepsins S and K in human atheroma and regulation of their production in smooth muscle cells. J Clin Invest. 1998; 102 (3):576–83. https://doi.org/10.1172/JCI181 PMID: 9691094; PubMed Central PMCID: PMC508918.
50. Geng YJ, Wu Q, Muszynski M, Hansson GK, Libby P. Apoptosis of vascular smooth muscle cells induced by in vitro stimulation with interferon-gamma, tumor necrosis factor-alpha, and interleukin-1 beta. Arterioscler Thromb Vasc Biol. 1996; 16(1):19–27. PMID: 8548421.
51. Golledge J, Norman PE. Atherosclerosis and abdominal aortic aneurysm: cause, response, or common risk factors? Arterioscler Thromb Vasc Biol. 2010; 30(6):1075–7. https://doi.org/10.1161/ATVBAHA.110.206573 PMID: 20484703; PubMed Central PMCID: PMC2874982.
52. Johnsen SH, Forsdahl SH, Singh K, Jacobsen BK. Atherosclerosis in abdominal aortic aneurysms: a causal event or a process running in parallel? The Tromso study. Arterioscler Thromb Vasc Biol. 2010; 30(6):1263–8. https://doi.org/10.1161/ATVBAHA.110.203588 PMID: 20360536.
53. Nambiar J, Clarke AW, Shim D, Mabon D, Tian C, Windloch K, et al. Potent neutralizing anti-CD1d antibody reduces lung cytokine release in primate asthma model. MAbs. 2015; 7(3):638–50. https://doi.org/10.1080/19420862.2015.1016693 PMID: 25751125; PubMed Central PMCID: PMCPMC4623119.
54. Tazawa H, Irei T, Tanaka Y, Igarashi Y, Tashiro H, Ohdan H. Blockade of invariant TCR-CD1d interaction specifically inhibits antibody production against blood group A carbohydrates. Blood. 2013; 122 (15):2582–90. https://doi.org/10.1182/blood-2012-02-407452 PMID: 23943651; PubMed Central PMCID: PMCPMC3795459.
55. Li Y, Kanellakis P, Hosseini H, Cao A, Deswaerte V, Tipping P, et al. A CD1d-dependent lipid antagonist to NKT cells ameliorates atherosclerosis in ApoE-/- mice by reducing lesion necrosis and inflammation. Cardiovasc Res. 2016; 109(2):305–17. https://doi.org/10.1093/cvr/cvv259 PMID: 26604037.
56. Lombardi V, Stock P, Singh AK, Kerzerho J, Yang W, Sullivan BA, et al. A CD1d-dependent antagonist inhibits the activation of invariant NKT cells and prevents development of allergen-induced airway hyperreactivity. J Immunol. 2010; 184(4):2107–15. https://doi.org/10.4049/jimmunol.0901208 PMID: 20083656; PubMed Central PMCID: PMCPMC2845715.