Elastin-derived peptides promote abdominal aortic aneurysm formation by modulating m1/m2 macrophage polarization

Journal of Immunology

Volumn 196, Issue 11, 2016, Pages 4536-4543

  Dale, Matthew A ^a   Xiong, Wanfen ^a   Carson, Jeffrey S ^a   Suh, Melissa K ^a   Karpisek, Andrew D ^a   Meisinger, Trevor M ^a   Casale, George P ^a   Baxter, B Timothy ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ELASTIN; ELASTIN DERIVED PEPTIDE; MATRIX METALLOPROTEINASE; PEPTIDE; UNCLASSIFIED DRUG; MONOCLONAL ANTIBODY; PEPTIDE FRAGMENT;

ABDOMINAL AORTA ANEURYSM; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; C57BL 6 MOUSE; CONTROLLED STUDY; ENZYME ACTIVITY; IN VITRO STUDY; INFLAMMATION; MACROPHAGE; MOUSE; MURINE MODEL; NONHUMAN; PATHOPHYSIOLOGY; POLARIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; VASODILATATION; ABDOMINAL AORTIC ANEURYSM; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CYTOLOGY; IMMUNOLOGY; MACROPHAGE ACTIVATION; MALE;

ANIMALS; ANTIBODIES, MONOCLONAL; AORTIC ANEURYSM, ABDOMINAL; ELASTIN; MACROPHAGE ACTIVATION; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; PEPTIDE FRAGMENTS;

EID: 84975117316     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1502454     Document Type: Article

References (49)

1. Thom, T., N. Haase, W. Rosamond, V. J. Howard, J. Rumsfeld, T. Manolio, Z. J. Zheng, K. Flegal, C. O'Donnell, S. Kittner, et al; American Heart Association Statistics Committee and Stroke Statistics Subcommittee. 2006. Heart disease and stroke statistics-2006 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation 113: e85-e151.
2. Baxter, B. T., M. C. Terrin, and R. L. Dalman. 2008. Medical management of small abdominal aortic aneurysms. Circulation 117: 1883-1889.
3. Shimizu, K., R. N. Mitchell, and P. Libby. 2006. Inflammation and cellular immune responses in abdominal aortic aneurysms. Arterioscler. Thromb. Vasc. Biol. 26: 987-994.
4. Botnar, R. M., A. J. Wiethoff, U. Ebersberger, S. Lacerda, U. Blume, A. Warley, C. H. Jansen, D. C. Onthank, R. R. Cesati, R. Razavi, et al. 2014. In vivo assessment of aortic aneurysm wall integrity using elastin-specific molecular magnetic resonance imaging. Circ. Cardiovasc Imaging 7: 679-689.
5. Blanchevoye, C., N. Floquet, A. Scandolera, S. Baud, P. Maurice, O. Bocquet, S. Blaise, C. Ghoneim, B. Cantarelli, F. Delacoux, et al. 2013. Interaction between the elastin peptide VGVAPG and human elastin binding protein. J. Biol. Chem. 288: 1317-1328.
6. Duca, L., N. Floquet, A. J. Alix, B. Haye, and L. Debelle. 2004. Elastin as a matrikine. Crit. Rev. Oncol. Hematol. 49: 235-244.
7. Mochizuki, S., B. Brassart, and A. Hinek. 2002. Signaling pathways transduced through the elastin receptor facilitate proliferation of arterial smooth muscle cells. J. Biol. Chem. 277: 44854-44863.
8. Senior, R. M., G. L. Griffin, R. P. Mecham, D. S. Wrenn, K. U. Prasad, and D. W. Urry. 1984. Val-Gly-Val-Ala-Pro-Gly, a repeating peptide in elastin, is chemotactic for fibroblasts and monocytes. J. Cell Biol. 99: 870-874.
9. Juvonen, J., H. M. Surcel, J. Satta, A. M. Teppo, A. Bloigu, H. Syrjälä, J. Airaksinen, M. Leinonen, P. Saikku, and T. Juvonen. 1997. Elevated circulating levels of inflammatory cytokines in patients with abdominal aortic aneurysm. Arterioscler. Thromb. Vasc. Biol. 17: 2843-2847.
10. Lindholt, J. S., L. Heickendorff, E. W. Henneberg, and H. Fasting. 1997. Serumelastin-peptides as a predictor of expansion of small abdominal aortic aneurysms. Eur. J. Vasc. Endovasc. Surg. 14: 12-16.
11. Lindholt, J. S., H. A. Ashton, L. Heickendorff, and R. A. Scott. 2001. Serum elastin peptides in the preoperative evaluation of abdominal aortic aneurysms. Eur. J. Vasc. Endovasc. Surg. 22: 546-550.
12. Houghton, A. M., P. A. Quintero, D. L. Perkins, D. K. Kobayashi, D. G. Kelley, L. A. Marconcini, R. P. Mecham, R. M. Senior, and S. D. Shapiro. 2006. Elastin fragments drive disease progression in a murine model of emphysema. J. Clin. Invest. 116: 753-759.
13. Hance, K. A., M. Tataria, S. J. Ziporin, J. K. Lee, and R. W. Thompson. 2002. Monocyte chemotactic activity in human abdominal aortic aneurysms: role of elastin degradation peptides and the 67-kD cell surface elastin receptor. J. Vasc. Surg. 35: 254-261.
14. Hunninghake, G. W., J. M. Davidson, S. Rennard, S. Szapiel, J. E. Gadek, and R. G. Crystal. 1981. Elastin fragments attract macrophage precursors to diseased sites in pulmonary emphysema. Science 212: 925-927.
15. Guo, G., P. Booms, M. Halushka, H. C. Dietz, A. Ney, S. Stricker, J. Hecht, S. Mundlos, and P. N. Robinson. 2006. Induction of macrophage chemotaxis by aortic extracts of the mgR Marfan mouse model and a GxxPG-containing fibrillin-1 fragment. Circulation 114: 1855-1862.
16. Murray, P. J., and T. A. Wynn. 2011. Protective and pathogenic functions of macrophage subsets. Nat. Rev. Immunol. 11: 723-737.
17. Xiong, W., J. MacTaggart, R. Knispel, J. Worth, Y. Persidsky, and B. T. Baxter. 2009. Blocking TNF-αlpha attenuates aneurysm formation in a murine model. J. Immunol. 183: 2741-2746.
18. Karlsson, L., D. Bergqvist, J. Lindbäck, and H. Pärsson. 2009. Expansion of small-diameter abdominal aortic aneurysms is not reflected by the release of inflammatory mediators IL-6, MMP-9 and CRP in plasma. Eur. J. Vasc. Endovasc. Surg. 37: 420-424.
19. Koh, T. J., and L. A. DiPietro. 2011. Inflammation and wound healing: the role of the macrophage. Expert Rev. Mol. Med. 13: e23.
20. Longo, G. M., W. Xiong, T. C. Greiner, Y. Zhao, N. Fiotti, and B. T. Baxter. 2002. Matrix metalloproteinases 2 and 9 work in concert to produce aortic aneurysms. J. Clin. Invest. 110: 625-632.
21. Guo, G., B. Muñoz-García, C. E. Ott, J. Grunhagen, S. A. Mousa, A. Pletschacher, Y. von Kodolitsch, P. Knaus, and P. N. Robinson. 2013. Antagonism of GxxPG fragments ameliorates manifestations of aortic disease in Marfan syndrome mice. Hum. Mol. Genet. 22: 433-443.
22. Weischenfeldt, J., and B. Porse. 2008. Bone marrow-derived macrophages (BMM): isolation and applications. CSH Protoc. 2008: pdb.prot5080.
23. Sharma, A. K., G. Lu, A. Jester, W. F. Johnston, Y. Zhao, V. A. Hajzus, M. R. Saadatzadeh, G. Su, C. M. Bhamidipati, G. S. Mehta, et al. 2012. Experimental abdominal aortic aneurysm formation is mediated by IL-17 and attenuated by mesenchymal stem cell treatment. Circulation 126(Suppl. 1): S38-S45.
24. + T cells and IFN-γamma in the development of abdominal aortic aneurysms in a murine model. J. Immunol. 172: 2607-2612.
25. Petersen, E., F. Wagberg, and K. A. Angquist. 2002. Serum concentrations of elastin-derived peptides in patients with specific manifestations of atherosclerotic disease. Eur. J. Vasc. Endovasc. Surg. 24: 440-444.
26. Thompson, R. W., J. A. Curci, T. L. Ennis, D. Mao, M. B. Pagano, and C. T. Pham. 2006. Pathophysiology of abdominal aortic aneurysms: insights from the elastase-induced model in mice with different genetic backgrounds. Ann. N. Y. Acad. Sci. 1085: 59-73.
27. D'Armiento, J. 2003. Decreased elastin in vessel walls puts the pressure on. J. Clin. Invest. 112: 1308-1310.
28. Hornebeck, W., H. Emonard, J. C. Monboisse, and G. Bellon. 2002. Matrixdirected regulation of pericellular proteolysis and tumor progression. Semin. Cancer Biol. 12: 231-241.
29. Shapiro, S. D., S. K. Endicott, M. A. Province, J. A. Pierce, and E. J. Campbell. 1991. Marked longevity of human lung parenchymal elastic fibers deduced from prevalence of D-aspartate and nuclear weapons-related radiocarbon. J. Clin. Invest. 87: 1828-1834.
30. Shinohara, T., K. Suzuki, M. Okada, M. Shiigai, M. Shimizu, T. Maehara, and F. Ohsuzu. 2003. Soluble elastin fragments in serum are elevated in acute aortic dissection. Arterioscler. Thromb. Vasc. Biol. 23: 1839-1844.
31. Debret, R., F. Antonicelli, A. Theill, W. Hornebeck, P. Bernard, M. Guenounou, and R. Le Naour. 2005. Elastin-derived peptides induce a T-helper type 1 polarization of human blood lymphocytes. Arterioscler. Thromb. Vasc. Biol. 25: 1353-1358.
32. Baranek, T., R. Debret, F. Antonicelli, B. Lamkhioued, A. Belaaouaj, W. Hornebeck, P. Bernard, M. Guenounou, and R. Le Naour. 2007. Elastin receptor (spliced galactosidase) occupancy by elastin peptides counteracts proinflammatory cytokine expression in lipopolysaccharide-stimulated human monocytes through NF-kappaB down-regulation. J. Immunol. 179: 6184-6192.
33. Koch, A. E., G. K. Haines, R. J. Rizzo, J. A. Radosevich, R. M. Pope, P. G. Robinson, and W. H. Pearce. 1990. Human abdominal aortic aneurysms: immunophenotypic analysis suggesting an immune-mediated response. Am. J. Pathol. 137: 1199-1213.
34. Pearce, W. H., and A. E. Koch. 1996. Cellular components and features of immune response in abdominal aortic aneurysms. Ann. N. Y. Acad. Sci. 800: 175-185.
35. Longo, G. M., S. J. Buda, N. Fiotta, W. Xiong, T. Griener, S. Shapiro, and B. T. Baxter. 2005. MMP-12 has a role in abdominal aortic aneurysms in mice. Surgery 137: 457-462.
36. Wang, Y., S. Krishna, and J. Golledge. 2013. The calcium chloride-induced rodent model of abdominal aortic aneurysm. Atherosclerosis 226: 29-39.
37. Tsuruda, T., J. Kato, K. Hatakeyama, K. Kojima, M. Yano, Y. Yano, K. Nakamura, F. Nakamura-Uchiyama, Y. Matsushima, T. Imamura, et al. 2008. Adventitial mast cells contribute to pathogenesis in the progression of abdominal aortic aneurysm. Circ. Res. 102: 1368-1377.
38. Johnston, W. F., M. Salmon, N. H. Pope, A. Meher, G. Su, M. L. Stone, G. Lu, G. K. Owens, G. R. Upchurch, Jr., and G. Ailawadi. 2014. Inhibition of interleukin-1b decreases aneurysm formation and progression in a novel model of thoracic aortic aneurysms. Circulation 130(Suppl. 1): S51-S59.
39. Tieu, B. C., C. Lee, H. Sun, W. Lejeune, A. Recinos, III, X. Ju, H. Spratt, D. C. Guo, D. Milewicz, R. G. Tilton, and A. R. Brasier. 2009. An adventitial IL-6/MCP1 amplification loop accelerates macrophage-mediated vascular inflammation leading to aortic dissection in mice. J. Clin. Invest. 119: 3637-3651.
40. Zhou, Y., W. Wu, J. S. Lindholt, G. K. Sukhova, P. Libby, X. Yu, and G. P. Shi. 2015. Regulatory T cells in human and angiotensin II-induced mouse abdominal aortic aneurysms. Cardiovasc. Res. 107: 98-107.
41. Meng, X., J. Yang, M. Dong, K. Zhang, E. Tu, Q. Gao, W. Chen, C. Zhang, and Y. Zhang. 2016. Regulatory T cells in cardiovascular diseases. Nat. Rev. Cardiol. 13: 167-179.
42. Cao, Q., Y. Wang, D. Zheng, Y. Sun, Y. Wang, V. W. Lee, G. Zheng, T. K. Tan, J. Ince, S. I. Alexander, and D. C. Harris. 2010. IL-10/TGF-βeta-modified macrophages induce regulatory T cells and protect against adriamycin nephrosis. J. Am. Soc. Nephrol. 21: 933-942.
43. + T cells in mice. Immunol. Cell Biol. 89: 130-142.
44. Lumeng, C. N., J. B. DelProposto, D. J. Westcott, and A. R. Saltiel. 2008. Phenotypic switching of adipose tissue macrophages with obesity is generated by spatiotemporal differences in macrophage subtypes. Diabetes 57: 3239-3246.
45. Jenne, C. N., and P. Kubes. 2013. Immune surveillance by the liver. Nat. Immunol. 14: 996-1006.
46. Hinek, A., and M. Rabinovitch. 1994. 67-kD elastin-binding protein is a protective companion of extracellular insoluble elastin and intracellular tropoelastin. J. Cell Biol. 126: 563-574.
47. Privitera, S., C. A. Prody, J. W. Callahan, and A. Hinek. 1998. The 67-kDa enzymatically inactive alternatively spliced variant of beta-galactosidase is identical to the elastin/laminin-binding protein. J. Biol. Chem. 273: 6319-6326.
48. Wrenn, D. S., G. L. Griffin, R. M. Senior, and R. P. Mecham. 1986. Characterization of biologically active domains on elastin: identification of a monoclonal antibody to a cell recognition site. Biochemistry 25: 5172-5176.
49. Grosso, L. E., and Scott, M. 1993. Peptide sequences selected by BA4, a tropoelastin-specific monoclonal antibody, are ligands for the 67-kilodalton bovine elastin receptor. Biochemistry 32: 13369-13374.