Targeting PI3Kγ activity decreases vascular trauma-induced intimal hyperplasia through modulation of the Th1 response

Journal of Experimental Medicine

Volumn 211, Issue 9, 2014, Pages 1779-1792

  Smirnova, Natalia F ^a   Gayral, Stéphanie ^a   Pedros, Christophe ^b,c   Loirand, Gervaise ^b,d   Vaillant, Nathalie ^b,d   Malet, Nicole ^a   Kassem, Sahar ^b,c   Calise, Denis ^a   Goudounèche, Dominique ^a,e   Wymann, Matthias P ^f   Hirsch, Emilio ^g   Gadeau, Alain Pierre ^h   Martinez, Laurent O ^a   Saoudi, Abdelhadi ^b,c   Laffargue, Muriel ^a  

^a Université de Toulouse   (France)

^b L INSTITUT DU THORAX   (France)

^c UNIVERSITÉ PAUL SABATIER   (France)

^d CNRS 6291   (France)

^e CMEAB   (France)

^f UNIVERSITY OF BASEL   (Switzerland)

^g UNIVERSITY OF TURIN   (Italy)

^h Bordeaux Segalen University   (France)

Author keywords

[No Author keywords available]

Indexed keywords

5 (6 QUINOXALINYLMETHYLENE) 2,4 THIAZOLIDINEDIONE; 5 [5 (4 FLUORO 2 HYDROXYPHENYL)FURFURYLIDENE] 2,4 THIAZOLIDINEDIONE; CYTOKINE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; PHOSPHATIDYLINOSITOL 3 KINASE GAMMA; PLACEBO; RAG2 PROTEIN; RANTES;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERY INJURY; ARTERY INTIMA PROLIFERATION; ARTERY LESION; ARTERY OCCLUSION; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE ASSOCIATION; DOSE RESPONSE; DRUG EFFICACY; DRUG TARGETING; ENZYME ACTIVITY; ENZYME INHIBITION; HEART PROTECTION; IMMUNOMODULATION; LYMPHOCYTE FUNCTION; MONOCYTE; MOUSE; NEOINTIMA; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SMOOTH MUSCLE FIBER; TH1 CELL; TH17 CELL; TREATMENT RESPONSE; WILD TYPE;

ANIMALS; CAROTID ARTERY INJURIES; CLASS IB PHOSPHATIDYLINOSITOL 3-KINASE; ENZYME INHIBITORS; FEMORAL ARTERY; GENE TARGETING; INFLAMMATION MEDIATORS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEOINTIMA; QUINOXALINES; RATS; RATS, SPRAGUE-DAWLEY; TH1 CELLS; THIAZOLIDINEDIONES;

EID: 84906534098     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20131276     Document Type: Article

References (73)

1. Alcázar, I., M. Marqués, A. Kumar, E. Hirsch, M. Wymann, A.C. Carrera, and D.F. Barber. 2007. Phosphoinositide 3-kinase γ participates in T cell receptor-induced T cell activation. J. Exp. Med. 204:2977-2987. http://dx.doi.org/10.1084/jem.20070366
2. Belotti, D., M. Rieppi, M.I. Nicoletti, A.M. Casazza, T. Fojo, G. Taraboletti, and R. Giavazzi. 1996. Paclitaxel (Taxol(R)) inhibits motility of paclitaxelresistant human ovarian carcinoma cells. Clin. Cancer Res. 2:1725-1730.
3. Bennett, M.R. 2003. In-stent stenosis: pathology and implications for the development of drug eluting stents. Heart. 89:218-224. http://dx.doi.org/10.1136/heart.89.2.218
4. Bikkina, M., and J. Koneru. 2011. Long-term effectiveness and safety of sirolimus drug-eluting stents. Med Devices (Auckl). 4:117-124. http://dx.doi.org/10.2147/MDER.S11749
5. Boehm, M., M. Olive, A.L. True, M.F. Crook, H. San, X. Qu, and E.G. Nabel. 2004. Bone marrow-derived immune cells regulate vascular disease through a p27(Kip1)-dependent mechanism. J. Clin. Invest. 114:419-426. http://dx.doi.org/10.1172/JCI200420176
6. Castronuovo, J.J. Jr., S.B. Guss, D. Mysh, A. Sawhney, M. Wolff, and A.M. Gown. 1995. Cytokine therapy for arterial restenosis: inhibition of neointimal hyperplasia by gamma-interferon. Cardiovasc. Surg. 3:463-468. http://dx.doi.org/10.1016/0967-2109(95)94442-Y
7. Costa, M.A., and D.I. Simon. 2005. Molecular basis of restenosis and drugeluting stents. Circulation. 111:2257-2273. http://dx.doi.org/10.1161/01.CIR.0000163587.36485.A7
8. Daemen, J., P. Wenaweser, K. Tsuchida, L. Abrecht, S. Vaina, C. Morger, N. Kukreja, P. Jüni, G. Sianos, G. Hellige, et al. 2007. Early and late coronary stent thrombosis of sirolimus-eluting and paclitaxel-eluting stents in routine clinical practice: data from a large two-institutional cohort study. Lancet. 369:667-678. http://dx.doi.org/10.1016/S0140-6736(07)60314-6
9. Dangas, G.D., B.E. Claessen, A. Caixeta, E.A. Sanidas, G.S. Mintz, and R. Mehran. 2010. In-stent restenosis in the drug-eluting stent era. J. Am. Coll. Cardiol. 56:1897-1907. http://dx.doi.org/10.1016/j.jacc.2010.07.028
10. Dimayuga, P.C., K.Y. Chyu, J. Kirzner, J. Yano, X. Zhao, J. Zhou, P.K. Shah, and B. Cercek. 2011. Enhanced neointima formation following arterial injury in immune deficient Rag-1-/- mice is attenuated by adoptive transfer of CD8+ T cells. PLoS ONE. 6:e20214. http://dx.doi.org/10.1371/journal.pone.0020214
11. hi T cells. J Am Heart Assoc. 2:e000155. http://dx.doi.org/10.1161/JAHA.113.000155
12. Dzau, V.J. 2003. Predicting the future of human gene therapy for cardiovascular diseases: what will the management of coronary artery disease be like in 2005 and 2010? Am. J. Cardiol. 92:32N-35N. http://dx.doi.org/10.1016/S0002-9149(03)00966-4
13. Eid, R.E., D.A. Rao, J. Zhou, S.F. Lo, H. Ranjbaran, A. Gallo, S.I. Sokol, S. Pfau, J.S. Pober, and G. Tellides. 2009. Interleukin-17 and interferon-γ are produced concomitantly by human coronary artery-infiltrating T cells and act synergistically on vascular smooth muscle cells. Circulation. 119:1424-1432. http://dx.doi.org/10.1161/CIRCULATIONAHA.108.827618
14. Farb, A., D.K. Weber, F.D. Kolodgie, A.P. Burke, and R. Virmani. 2002. Morphological predictors of restenosis after coronary stenting in humans. Circulation. 105:2974-2980. http://dx.doi.org/10.1161/01.CIR.0000019071.72887.BD
15. Fougerat, A., S. Gayral, P. Gourdy, A. Schambourg, T. Rückle, M.K. Schwarz, C. Rommel, E. Hirsch, J.F. Arnal, J.P. Salles, et al. 2008. Genetic and pharmacological targeting of phosphoinositide 3-kinase-γ reduces atherosclerosis and favors plaque stability by modulating inflammatory processes. Circulation. 117:1310-1317. http://dx.doi.org/10.1161/CIRCULATIONAHA.107.720466
16. Fougerat, A., S. Gayral, N. Malet, F. Briand-Mesange, M. Breton-Douillon, and M. Laffargue. 2009. Phosphoinositide 3-kinases and their role in inflammation: potential clinical targets in atherosclerosis? Clin. Sci. 116:791-804. http://dx.doi.org/10.1042/CS20080549
17. Fougerat, A., N.F. Smirnova, S. Gayral, N. Malet, E. Hirsch, M.P. Wymann, B. Perret, L.O. Martinez, M. Douillon, and M. Laffargue. 2012. Key role of PI3Kγ in monocyte chemotactic protein-1-mediated amplification of PDGF-induced aortic smooth muscle cell migration. Br. J. Pharmacol. 166:1643-1653. http://dx.doi.org/10.1111/j.1476-5381.2012.01866.x
18. Fujino, S., A. Andoh, S. Bamba, A. Ogawa, K. Hata, Y. Araki, T. Bamba, and Y. Fujiyama. 2003. Increased expression of interleukin 17 in inflammatory bowel disease. Gut. 52:65-70. http://dx.doi.org/10.1136/gut.52.1.65
19. George, J., S. Greenberg, I. Barshack, M. Singh, S. Pri-Chen, S. Laniado, and G. Keren. 2001. Accelerated intimal thickening in carotid arteries of ballooninjured rats after immunization against heat shock protein 70. J. Am. Coll. Cardiol. 38:1564-1569. http://dx.doi.org/10.1016/S0735-1097(01)01579-0
20. Giannakakou, P., R. Robey, T. Fojo, and M.V. Blagosklonny. 2001. Low concentrations of paclitaxel induce cell type-dependent p53, p21 and G1/G2 arrest instead of mitotic arrest: molecular determinants of paclitaxelinduced cytotoxicity. Oncogene. 20:3806-3813. http://dx.doi.org/10.1038/sj.onc.1204487
21. Grassia, G., M. Maddaluno, A. Guglielmotti, G. Mangano, G. Biondi, P. Maffia, and A. Ialenti. 2009. The anti-inflammatory agent bindarit inhibits neointima formation in both rats and hyperlipidaemic mice. Cardiovasc. Res. 84:485-493. http://dx.doi.org/10.1093/cvr/cvp238
22. Gruen, M., C. Rose, C. König, M. Gajda, R. Wetzker, and R. Bräuer. 2010. Loss of phosphoinositide 3-kinase γ decreases migration and activation of phagocytes but not T cell activation in antigen-induced arthritis. BMC Musculoskelet. Disord. 11:63. http://dx.doi.org/10.1186/1471-2474-11-63
23. Gyöngyösi, M., W. Sperker, C. Csonka, D. Bonderman, I. Lang, C. Strehblow, C. Adlbrecht, M. Shirazi, U. Windberger, S. Marlovits, et al. 2003. Inhibition of interleukin-1β convertase is associated with decrease of neointimal hyperplasia after coronary artery stenting in pigs. Mol. Cell. Biochem. 249:39-43. http://dx.doi.org/10.1023/A:1024701715131
24. Hansson, G.K., and J. Holm. 1991. Interferon-gamma inhibits arterial stenosis after injury. Circulation. 84:1266-1272. http://dx.doi.org/10.1161/01.CIR.84.3.1266
25. Hansson, G.K., J. Holm, S. Holm, Z. Fotev, H.J. Hedrich, and J. Fingerle. 1991. T lymphocytes inhibit the vascular response to injury. Proc. Natl. Acad. Sci. USA. 88:10530-10534. http://dx.doi.org/10.1073/pnas.88.23.10530
26. Hirsch, E., V.L. Katanaev, C. Garlanda, O. Azzolino, L. Pirola, L. Silengo, S. Sozzani, A. Mantovani, F. Altruda, and M.P. Wymann. 2000. Central role for G protein-coupled phosphoinositide 3-kinase γ in inflammation. Science. 287:1049-1053. http://dx.doi.org/10.1126/science.287.5455.1049
27. Horvath, C., F.G. Welt, M. Nedelman, P. Rao, and C. Rogers. 2002. Targeting CCR2 or CD18 inhibits experimental in-stent restenosis in primates: inhibitory potential depends on type of injury and leukocytes targeted. Circ. Res. 90:488-494. http://dx.doi.org/10.1161/hh0402.105956
28. Hoshino, A., T. Nagao, N. Nagi-Miura, N. Ohno, M. Yasuhara, K. Yamamoto, T. Nakayama, and K. Suzuki. 2008. MPO-ANCA induces IL-17 production by activated neutrophils in vitro via FC region- and complementdependent manner. J. Autoimmun. 31:79-89. http://dx.doi.org/10.1016/j.jaut.2008.03.006
29. Kawamura, A., S. Miura, M. Fujino, H. Nishikawa, Y. Matsuo, H. Tanigawa, S. Tomita, Y. Tsuchiya, K. Matsuo, and K. Saku. 2003. CXCR3 chemokine receptor-plasma IP10 interaction in patients with coronary artery disease. Circ. J. 67:851-854. http://dx.doi.org/10.1253/circj.67.851
30. Kondo, T., H. Takata, F. Matsuki, and M. Takiguchi. 2009. Cutting edge: Phenotypic characterization and differentiation of human CD8+ T cells producing IL-17. J. Immunol. 182:1794-1798. http://dx.doi.org/10.4049/jimmunol.0801347
31. Kovacic, J.C., R. Gupta, A.C. Lee, M. Ma, F. Fang, C.N. Tolbert, A.D. Walts, L.E. Beltran, H. San, G. Chen, et al. 2010. Stat3-dependent acute Rantes production in vascular smooth muscle cells modulates inflammation following arterial injury in mice. J. Clin. Invest. 120:303-314. http://dx.doi.org/10.1172/JCI40364
32. Laffargue, M., R. Calvez, P. Finan, A. Trifilieff, M. Barbier, F. Altruda, E. Hirsch, and M.P. Wymann. 2002. Phosphoinositide 3-kinase gamma is an essential amplifier of mast cell function. Immunity. 16:441-451. http://dx.doi.org/10.1016/S1074-7613(02)00282-0
33. Lagerqvist, B., S.K. James, U. Stenestrand, J. Lindbäck, T. Nilsson, and L. Wallentin. SCAAR Study Group. 2007. Long-term outcomes with drug-eluting stents versus bare-metal stents in Sweden. N. Engl. J. Med. 356:1009-1019. http://dx.doi.org/10.1056/NEJMoa067722
34. Lin, A.M., C.J. Rubin, R. Khandpur, J.Y. Wang, M. Riblett, S. Yalavarthi, E.C. Villanueva, P. Shah, M.J. Kaplan, and A.T. Bruce. 2011. Mast cells and neutrophils release IL-17 through extracellular trap formation in psoriasis. J. Immunol. 187:490-500. http://dx.doi.org/10.4049/jimmunol.1100123
35. Lindner, V., J. Fingerle, and M.A. Reidy. 1993. Mouse model of arterial injury. Circ. Res. 73:792-796. http://dx.doi.org/10.1161/01.RES.73.5.792
36. Liu, W., Y. Liu, H. Jiang, X. Ding, R. Zhu, B. Li, and Y. Zhao. 2013. Plasma levels of interleukin 18, interleukin 10, and matrix metalloproteinase-9 and -137G/C polymorphism of interleukin 18 are associated with incidence of in-stent restenosis after percutaneous coronary intervention. Inflammation. 36:1129-1135. http://dx.doi.org/10.1007/s10753-013-9647-6
37. Lüscher, T.F., J. Steffel, F.R. Eberli, M. Joner, G. Nakazawa, F.C. Tanner, and R. Virmani. 2007. Drug-eluting stent and coronary thrombosis: biological mechanisms and clinical implications. Circulation. 115:1051-1058. http://dx.doi.org/10.1161/CIRCULATIONAHA.106.675934
38. Mach, F., A. Sauty, A.S. Iarossi, G.K. Sukhova, K. Neote, P. Libby, and A.D. Luster. 1999. Differential expression of three T lymphocyte-activating CXC chemokines by human atheroma-associated cells. J. Clin. Invest. 104:1041-1050. http://dx.doi.org/10.1172/JCI6993
39. Marx, S.O., T. Jayaraman, L.O. Go, and A.R. Marks. 1995. Rapamycin-FKBP inhibits cell cycle regulators of proliferation in vascular smooth muscle cells. Circ. Res. 76:412-417. http://dx.doi.org/10.1161/01.RES.76.3.412
40. Marx, S.O., H. Totary-Jain, and A.R. Marks. 2011. Vascular smooth muscle cell proliferation in restenosis. Circ. Cardiovasc. Interv. 4:104-111. http://dx.doi.org/10.1161/CIRCINTERVENTIONS.110.957332
41. neg iNKT cell population involved in airway neutrophilia. J. Exp. Med. 204:995-1001. http://dx.doi.org/10.1084/jem.20061551
42. Murayama, H., M. Takahashi, M. Takamoto, Y. Shiba, H. Ise, J. Koyama, Y. Tagawa, Y. Iwakura, and U. Ikeda. 2008. Deficiency of tumour necrosis factor-α and interferon-γ in bone marrow cells synergistically inhibits neointimal formation following vascular injury. Cardiovasc. Res. 80:175-180. http://dx.doi.org/10.1093/cvr/cvn250
43. Niida, T., K. Isoda, M. Kitagaki, N. Ishigami, T. Adachi, O. Matsubara, K. Takeda, T. Kishimoto, and F. Ohsuzu. 2012. IκBNS regulates interleukin-6 production and inhibits neointimal formation after vascular injury in mice. Cardiovasc. Res. 93:371-379. http://dx.doi.org/10.1093/cvr/cvr323
44. O'Brien, R.L., C.L. Roark, and W.K. Born. 2009. IL-17-producing γδ T cells. Eur. J. Immunol. 39:662-666. http://dx.doi.org/10.1002/eji.200839120
45. Okamoto, Y., E.J. Folco, M. Minami, A.K. Wara, M.W. Feinberg, G.K. Sukhova, R.A. Colvin, S. Kihara, T. Funahashi, A.D. Luster, and P. Libby. 2008. Adiponectin inhibits the production of CXC receptor 3 chemokine ligands in macrophages and reduces T-lymphocyte recruitment in atherogenesis. Circ. Res. 102:218-225. http://dx.doi.org/10.1161/CIRCRESAHA.107.164988
46. Panzer, U., O.M. Steinmetz, R.R. Reinking, T.N. Meyer, S. Fehr, A. Schneider, G. Zahner, G. Wolf, U. Helmchen, P. Schaerli, et al. 2006. Compartmentspecific expression and function of the chemokine IP-10/CXCL10 in a model of renal endothelial microvascular injury. J. Am. Soc. Nephrol. 17:454-464. http://dx.doi.org/10.1681/ASN.2005040364
47. Parry, T.J., R. Brosius, R. Thyagarajan, D. Carter, D. Argentieri, R. Falotico, and J. Siekierka. 2005. Drug-eluting stents: sirolimus and paclitaxel differentially affect cultured cells and injured arteries. Eur. J. Pharmacol. 524:19-29. http://dx.doi.org/10.1016/j.ejphar.2005.09.042
48. Patrucco, E., A. Notte, L. Barberis, G. Selvetella, A. Maffei, M. Brancaccio, S. Marengo, G. Russo, O. Azzolino, S.D. Rybalkin, et al. 2004. PI3Kγ modulates the cardiac response to chronic pressure overload by distinct kinase-dependent and -independent effects. Cell. 118:375-387. http://dx.doi.org/10.1016/j.cell.2004.07.017
49. Perino, A., A. Ghigo, E. Ferrero, F. Morello, G. Santulli, G.S. Baillie, F. Damilano, A.J. Dunlop, C. Pawson, R. Walser, et al. 2011. Integrating cardiac PIP3 and cAMP signaling through a PKA anchoring function of p110γ. Mol. Cell. 42:84-95. http://dx.doi.org/10.1016/j.molcel.2011.01.030
50. Pires, N.M., D. Eefting, M.R. de Vries, P.H. Quax, and J.W. Jukema. 2007. Sirolimus and paclitaxel provoke different vascular pathological responses after local delivery in a murine model for restenosis on underlying atherosclerotic arteries. Heart. 93:922-927. http://dx.doi.org/10.1136/hrt.2006.102244
51. Poon, M., J.J. Badimon, and V. Fuster. 2002. Overcoming restenosis with sirolimus: from alphabet soup to clinical reality. Lancet. 359:619-622. http://dx.doi.org/10.1016/S0140-6736(02)07751-6
52. Proost, P., S. Struyf, T. Loos, M. Gouwy, E. Schutyser, R. Conings, I. Ronsse, M. Parmentier, B. Grillet, G. Opdenakker, et al. 2006. Coexpression and interaction of CXCL10 and CD26 in mesenchymal cells by synergising inflammatory cytokines: CXCL8 and CXCL10 are discriminative markers for autoimmune arthropathies. Arthritis Res. Ther. 8:R107. http://dx.doi.org/10.1186/ar1997
53. Rachitskaya, A.V., A.M. Hansen, R. Horai, Z. Li, R. Villasmil, D. Luger, R.B. Nussenblatt, and R.R. Caspi. 2008. Cutting edge: NKT cells constitutively express IL-23 receptor and RORγt and rapidly produce IL-17 upon receptor ligation in an IL-6-independent fashion. J. Immunol. 180:5167-5171. http://dx.doi.org/10.4049/jimmunol.180.8.5167
54. Ray, J.L., R. Leach, J.M. Herbert, and M. Benson. 2001. Isolation of vascular smooth muscle cells from a single murine aorta. Methods Cell Sci. 23:185-188. http://dx.doi.org/10.1023/A:1016357510143
55. Rodríguez-Borlado, L., D.F. Barber, C. Hernández, M.A. Rodríguez-Marcos, A. Sánchez, E. Hirsch, M. Wymann, C. Martínez-A, and A.C. Carrera. 2003. Phosphatidylinositol 3-kinase regulates the CD4/CD8 T cell differentiation ratio. J. Immunol. 170:4475-4482. http://dx.doi.org/10.4049/jimmunol.170.9.4475
56. Roque, M., J.T. Fallon, J.J. Badimon, W.X. Zhang, M.B. Taubman, and E.D. Reis. 2000. Mouse model of femoral artery denudation injury associated with the rapid accumulation of adhesion molecules on the luminal surface and recruitment of neutrophils. Arterioscler. Thromb. Vasc. Biol. 20:335-342. http://dx.doi.org/10.1161/01.ATV.20.2.335
57. Sasaki, T., J. Irie-Sasaki, R.G. Jones, A.J. Oliveira-dos-Santos, W.L. Stanford, B. Bolon, A. Wakeham, A. Itie, D. Bouchard, I. Kozieradzki, et al. 2000. Function of PI3Kγ in thymocyte development, T cell activation, and neutrophil migration. Science. 287:1040-1046. http://dx.doi.org/10.1126/science.287.5455.1040
58. Schlegel, P.M., I. Steiert, I. Kötter, and C.A. Müller. 2013. B cells contribute to heterogeneity of IL-17 producing cells in rheumatoid arthritis and healthy controls. PLoS ONE. 8:e82580. http://dx.doi.org/10.1371/journal.pone.0082580
59. Schwartz, R.S., E.J. Topol, P.W. Serruys, G. Sangiorgi, and D.R. Holmes Jr. 1998. Artery size, neointima, and remodeling: time for some standards. J. Am. Coll. Cardiol. 32:2087-2094.
60. Shimokado, K., T. Yokota, N. Kato, C. Kosaka, T. Sasaguri, J. Masuda, J. Ogata, and F. Numano. 1994. Bidirectional regulation of smooth muscle cell proliferation by IFN-γ. J. Atheroscler. Thromb. 1:S29-S33. http://dx.doi.org/10.5551/jat1994.1.Supplemment1_S29
61. Takatori, H., Y. Kanno, W.T. Watford, C.M. Tato, G. Weiss, I.I. Ivanov, D.R. Littman, and J.J. O'Shea. 2009. Lymphoid tissue inducer-like cells are an innate source of IL-17 and IL-22. J. Exp. Med. 206:35-41. http://dx.doi.org/10.1084/jem.20072713
62. Tanaka, K., M. Sata, Y. Hirata, and R. Nagai. 2003. Diverse contribution of bone marrow cells to neointimal hyperplasia after mechanical vascular injuries. Circ. Res. 93:783-790. http://dx.doi.org/10.1161/01.RES.0000096651.13001.B4
63. Tanaka, K., M. Sata, T. Natori, J.R. Kim-Kaneyama, K. Nose, M. Shibanuma, Y. Hirata, and R. Nagai. 2008. Circulating progenitor cells contribute to neointimal formation in nonirradiated chimeric mice. FASEB J. 22:428-436. http://dx.doi.org/10.1096/fj.06-6884com
64. Tenger, C., A. Sundborger, J. Jawien, and X. Zhou. 2005. IL-18 accelerates atherosclerosis accompanied by elevation of IFN-γ and CXCL16 expression independently of T cells. Arterioscler. Thromb. Vasc. Biol. 25:791-796. http://dx.doi.org/10.1161/01.ATV.0000153516.02782.65
65. Toutouzas, K., A. Colombo, and C. Stefanadis. 2004. Inflammation and restenosis after percutaneous coronary interventions. Eur. Heart J. 25:1679-1687. http://dx.doi.org/10.1016/j.ehj.2004.06.011
66. Tulis, D.A. 2007. Rat carotid artery balloon injury model. Methods Mol. Med. 139:1-30. http://dx.doi.org/10.1007/978-1-59745-571-8_1
67. van Dop, W.A., S. Marengo, A.A. te Velde, E. Ciraolo, I. Franco, F.J. ten Kate, G.E. Boeckxstaens, J.C. Hardwick, D.W. Hommes, E. Hirsch, and G.R. van den Brink. 2010. The absence of functional PI3Kγ prevents leukocyte recruitment and ameliorates DSS-induced colitis in mice. Immunol. Lett. 131:33-39. http://dx.doi.org/10.1016/j.imlet.2010.03.008
68. Vargas-Inchaustegui, D.A., A.E. Hogg, G. Tulliano, A. Llanos-Cuentas, J. Arevalo, J.J. Endsley, and L. Soong. 2010. CXCL10 production by human monocytes in response to Leishmania braziliensis infection. Infect. Immun. 78:301-308. http://dx.doi.org/10.1128/IAI.00959-09
69. Wang, Y., Y. Bai, L. Qin, P. Zhang, T. Yi, S.A. Teesdale, L. Zhao, J.S. Pober, and G. Tellides. 2007. Interferon-γ induces human vascular smooth muscle cell proliferation and intimal expansion by phosphatidylinositol 3-kinase dependent mammalian target of rapamycin raptor complex 1 activation. Circ. Res. 101:560-569. http://dx.doi.org/10.1161/CIRCRESAHA.107.151068
70. Xie, J.H., N. Nomura, M. Lu, S.L. Chen, G.E. Koch, Y. Weng, R. Rosa, J. Di Salvo, J. Mudgett, L.B. Peterson, et al. 2003. Antibody-mediated blockade of the CXCR3 chemokine receptor results in diminished recruitment of T helper 1 cells into sites of inflammation. J. Leukoc. Biol. 73:771-780. http://dx.doi.org/10.1189/jlb.1102573
71. Yoshimura, S., R. Morishita, K. Hayashi, K. Yamamoto, H. Nakagami, Y. Kaneda, N. Sakai, and T. Ogihara. 2001. Inhibition of intimal hyperplasia after balloon injury in rat carotid artery model using cis-element 'decoy' of nuclear factor-kB binding site as a novel molecular strategy. Gene Ther. 8:1635-1642. http://dx.doi.org/10.1038/sj.gt.3301566
72. Zohlnhöfer, D., T. Richter, F. Neumann, T. Nührenberg, R. Wessely, R. Brandl, A. Murr, C.A. Klein, and P.A. Baeuerle. 2001. Transcriptome analysis reveals a role of interferon-γ in human neointima formation. Mol. Cell. 7:1059-1069. http://dx.doi.org/10.1016/S1097-2765(01)00239-8
73. Zuojun, H., H. Lingyu, H. Wei, Y. Henghui, Z. Chonggang, W. Jingsong, W. Mian, L. Yong, and W. Shenming. 2012. Interference of IP-10 expression inhibits vascular smooth muscle cell proliferation and intimal hyperplasia in carotid artery: a new insight in the prevention of restenosis. Cell Biochem. Biophys. 62:125-135. http://dx.doi.org/10.1007/s12013-011-9270-9