Statins induce regulatory T cell recruitment via a CCL1 dependent pathway

Journal of Immunology

Volumn 181, Issue 5, 2008, Pages 3524-3534

  Mira, Emilia ^a   León, Beatriz ^a   Barber, Domingo F ^a   Jiménez Baranda, Sonia ^a   Goya, Iñigo ^a   Almonacid, Luis ^a   Márquez, Gabriel ^b   Zaballos, Angel ^a   Martínez A , Carlos ^a   Stein, Jens V ^c   Ardavín, Carlos ^a   Mañes, Santos ^a  

^a CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^b Genetrix   (Spain)

^c UNIVERSITY OF BERN   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CCL1 CHEMOKINE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; MEVINOLIN; CCL1 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CANDIDA ALBICANS; CONTROLLED STUDY; DELAYED HYPERSENSITIVITY; FEMALE; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNOMODULATION; INFLAMMATION; LYMPH NODE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SKIN INFLAMMATION; TH1 CELL; TH2 CELL; UPREGULATION; ANIMAL; DRUG EFFECT; GENETICS; HYPERSENSITIVITY; IMMUNOLOGY; MICROBIOLOGY; MOUSE MUTANT; NEUTROPHIL CHEMOTAXIS; PATHOLOGY; PHYSIOLOGY; T LYMPHOCYTE SUBPOPULATION;

ANIMALS; CANDIDA ALBICANS; CHEMOKINE CCL1; CHEMOTAXIS, LEUKOCYTE; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; HYPERSENSITIVITY; INFLAMMATION; LOVASTATIN; MICE; MICE, KNOCKOUT; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, REGULATORY; TH2 CELLS; UP-REGULATION;

EID: 51549113429     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.5.3524     Document Type: Article

References (53)

1. Tobert, J. A. 2003. Lovastatin and beyond: the history of the HMG-CoA reductase inhibitors. Nat. Rev. Drug Discov. 2: 517-526. (Pubitemid 37361744)
2. Del Real, G., S. Jiménez-Baranda, E. Mira, R. A. Lacalle, P. Lucas, C. Gómez-Moutón, M. Alegret, J. M. Peña, M. Rodríguez-Zapata, M. Alvarez-Mon, et al. 2004. Statins inhibit HIV-1 infection by down-regulating Rho activity. J. Exp. Med. 200: 541-547.
3. Erkkila, L., M. Jauhiainen, K. Laitinen, K. Haasio, T. Tiirola, P. Saikku, and M. Leinonen. 2005. Effect of simvastatin, an established lipid-lowering drug, on pulmonary Chlamydia pneumoniae infection in mice. Antimicrob. Agents Chemother. 49: 3959-3962. (Pubitemid 41233060)
4. Gupta, R., L. C. Plantinga, N. E. Fink, M. L. Melamed, J. Coresh, C. S. Fox, N. W. Levin, and N. R. Powe. 2007. Statin use and hospitalization for sepsis in patients with chronic kidney disease. J. Am. Med. Assoc. 297: 1455-1464. (Pubitemid 46556471)
5. Hackam, D. G., M. Mamdani, P. Li, and D. A. Redelmeier. 2006. Statins and sepsis in patients with cardiovascular disease: a population-based cohort analysis. Lancet 367: 413-418. (Pubitemid 43184262)
6. Aktas, O., S. Waiczies, A. Smorodchenko, J. Dorr, B. Seeger, T. Prozorovski, S. Sallach, M. Endres, S. Brocke, R. Nitsch, and F. Zipp. 2003. Treatment of relapsing paralysis in experimental encephalomyelitis by targeting Th1 cells through atorvastatin. J. Exp. Med. 197: 725-733. (Pubitemid 36350867)
7. Lawman, S., C. Mauri, E. C. Jury, H. T. Cook, and M. R. Ehrenstein. 2004. Atorvastatin inhibits autoreactive B cell activation and delays lupus development in New Zealand Black/White F1 mice. J. Immunol. 173: 7641-7646. (Pubitemid 39628206)
8. McCarey, D. W., I. B. McInnes, R. Madhok, R. Hampson, O. Scherbakov, I. Ford, H. A. Capell, and N. Sattar. 2004. Trial of atorvastatin in rheumatoid arthritis (TARA): double-blind, randomized placebo-controlled trial. Lancet 363: 2015-2021. (Pubitemid 38781100)
9. Youssef, S., O. Stuve, J. C. Patarroyo, P. J. Ruiz, J. L. Radosevich, E. M. Hur, M. Bravo, D. J. Mitchell, R. A. Sobel, L. Steinman, and S. S. Zamvil. 2002. The HMG-CoA reductase inhibitor, atorvastatin, promotes a Th2 bias and reverses paralysis in central nervous system autoimmune disease. Nature 420: 78-84. (Pubitemid 35291443)
10. Kobashigawa, J. A., J. D. Moriguchi, H. Laks, L. Wener, A. Hage, M. A. Hamilton, G. Cogert, A. Marquez, M. E. Vassilakis, J. Patel, and L. Yeatman. 2005. Ten-year follow-up of a randomized trial of pravastatin in heart transplant patients. J. Heart Lung Transplant. 24: 1736-1740. (Pubitemid 41641843)
11. Masterson, R., T. Hewitson, M. Leikis, R. Walker, S. Cohney, and G. Becker. 2005. Impact of statin treatment on 1-year functional and histologic renal allograft outcome. Transplantation 80: 332-338. (Pubitemid 41130874)
12. Dunn, S. E., S. Youssef, M. J. Goldstein, T. Prod'homme, M. S. Weber, S. S. Zamvil, and L. Steinman. 2006. Isoprenoids determine Th1/Th2 fate in pathogenic T cells, providing a mechanism of modulation of autoimmunity by atorvastatin. J. Exp. Med. 203: 401-412.
13. Yilmaz, A., C. Reiss, A. Weng, I. Cicha, C. Stumpf, A. Steinkasserer, W. G. Daniel, and C. D. Garlichs. 2006. Differential effects of statins on relevant functions of human monocyte-derived dendritic cells. J. Leukocyte Biol. 79: 529-538. (Pubitemid 44831230)
14. Cordle, A., J. Koenigsknecht-Talboo, B. Wilkinson, A. Limpert, and G. Landreth. 2005. Mechanisms of statin-mediated inhibition of small G-protein function. J. Biol. Chem. 280: 34202-34209. (Pubitemid 41443145)
15. Greenwood, J., L. Steinman, and S. S. Zamvil. 2006. Statin therapy and autoimmune disease: from protein prenylation to immunomodulation. Nat. Rev. Immunol. 6: 358-370.
16. Blanco-Colio, L. M., J. Tunon, J. L. Martin-Ventura, and J. Egido. 2003. Antiinflammatory and immunomodulatory effects of statins. Kidney Int. 63: 12-23.
17. Greenwood, J., and J. C. Mason. 2007. Statins and the vascular endothelial in- flammatory response. Trends Immunol. 28: 88-98. (Pubitemid 46178495)
18. Ehrenstein, M. R., E. C. Jury, and C. Mauri. 2005. Statins for atherosclerosis: as good as it gets? N. Engl. J. Med. 352: 73-75.
19. Jury, E. C., D. A. Isenberg, C. Mauri, and M. R. Ehrenstein. 2006. Atorvastatin restores Lck expression and lipid raft-associated signaling in T cells from patients with systemic lupus erythematosus. J. Immunol. 177: 7416-7422.
20. Weitz-Schmidt, G., K. Welzenbach, V. Brinkmann, T. Kamata, J. Kallen, C. Bruns, S. Cottens, Y. Takada, and U. Hommel. 2001. Statins selectively inhibit leukocyte function antigen-1 by binding to a novel regulatory integrin site. Nat. Med. 7: 687-692. (Pubitemid 32588024)
21. Giguere, J. F., and M. J. Tremblay. 2004. Statin compounds reduce human immunodeficiency virus type 1 replication by preventing the interaction between virion-associated host intercellular adhesion molecule 1 and its natural cell surface ligand LFA-1. J. Virol. 78: 12062-12065.
22. Schramm, R., M. D. Menger, Y. Harder, R. Schmits, O. Adam, G. Weitz-Schmidt, and H. J. Schafers. 2007. Statins inhibit lymphocyte homing to peripheral lymph nodes. Immunology 120: 315-324. (Pubitemid 46232906)
23. Demierre, M. F., P. D. Higgins, S. B. Gruber, E. Hawk, and S. M. Lippman. 2005. Statins and cancer prevention. Nat. Rev. Cancer 5: 930-942.
24. + human thymocytes. J. Exp. Med. 196: 379-387.
25. Colantonio, L., H. Recalde, F. Sinigaglia, and D. D'Ambrosio. 2002. Modulation of chemokine receptor expression and chemotactic responsiveness during differentiation of human naive T cells into Th1 or Th2 cells. Eur. J. Immunol. 32: 1264-1273. (Pubitemid 34546253)
26. + regulatory T cells. J. Exp. Med. 194: 847-853.
27. Schaerli, P., L. Ebert, K. Willimann, A. Blaser, R. S. Roos, P. Loetscher, and B. Moser. 2004. A skin-selective homing mechanism for human immune surveillance T cells. J. Exp. Med. 199: 1265-1275. (Pubitemid 38620263)
28. + T lymphocytes with regulatory activity. J. Immunol. 166: 996-1002.
29. Zingoni, A., H. Soto, J. A. Hedrick, A. Stoppacciaro, C. T. Storlazzi, F. Sinigaglia, D. D'Ambrosio, A. O'Garra, D. Robinson, M. Rocchi, et al. 1998. The chemokine receptor CCR8 is preferentially expressed in Th2 but not Th1 cells. J. Immunol. 161: 547-551. (Pubitemid 28323513)
30. Torres, M. 1998. The use of embryonic stem cells for the genetic manipulation of the mouse. Curr. Top. Dev. Biol. 36: 99-114.
31. Nombela-Arrieta, C., R. A. Lacalle, M. C. Montoya, Y. Kunisaki, D. Megias, M. Marques, A. C. Carrera, S. Mañes, Y. Fukui, C. Martínez-A., and J. V. Stein. 2004. Differential requirements for DOCK2 and phosphoinositide-3-kinase γ during T and B lymphocyte homing. Immunity 21: 429-441.
32. Metcalf, D., L. Robb, A. R. Dunn, S. Mifsud, and L. Di Rago. 1996. Role of granulocyte-macrophage colony-stimulating factor and granulocyte colony-stimulating factor in the development of an acute neutrophil inflammatory response in mice. Blood 88: 3755-3764. (Pubitemid 26383097)
33. Mira, E., R. A. Lacalle, J. M. Buesa, G. G. de Buitrago, S. Jiménez-Baranda, C. Gómez-Moutón, C. Martínez-A., and S. Mañes. 2004. Secreted MMP9 promotes angiogenesis more efficiently than constitutive active MMP9 bound to the tumor cell surface. J. Cell Sci. 117: 1847-1857.
34. Gegg, M. E., R. Harry, D. Hankey, H. Zambarakji, G. Pryce, D. Baker, P. Adamson, V. Calder, and J. Greenwood. 2005. Suppression of autoimmune retinal disease by lovastatin does not require Th2 cytokine induction. J. Immunol. 174: 2327-2335.
35. Van Nieuw Amerongen, G. P., M. A. Vermeer, P. Negre-Aminou, J. Lankelma, J. J. Emeis, and V. W. van Hinsbergh. 2000. Simvastatin improves disturbed endothelial barrier function. Circulation 102: 2803-2809. (Pubitemid 30954314)
36. Wei, C. Y., K. C. Huang, Y. H. Chou, P. F. Hsieh, K. H. Lin, and W. W. Lin. 2006. The role of Rho-associated kinase in differential regulation by statins of interleukin-1β- and lipopolysaccharide-mediated nuclear factor κB activation and inducible nitric-oxide synthase gene expression in vascular smooth muscle cells. Mol. Pharmacol. 69: 960-967.
37. Ardavín, C. 2007. Subpopulations and differentiation of mouse dendritic cells. In Advances in Molecular and Cellular Microbiology: Dendritic Cell Interactions with Bacteria. M. Rescigno, ed. Cambridge University Press, Cambridge, pp. 3-26.
38. Kwak, B., F. Mulhaupt, S. Myit, and F. Mach. 2000. Statins as a newly recognized type of immunomodulator. Nat. Med. 6: 1399-1402. (Pubitemid 32001026)
39. Arora, M., L. Chen, M. Paglia, I. Gallagher, J. E. Allen, Y. M. Vyas, A. Ray, and P. Ray. 2006. Simvastatin promotes Th2-type responses through the induction of the chitinase family member Ym1 in dendritic cells. Proc. Natl. Acad. Sci. USA 103: 7777-7782. (Pubitemid 43752857)
40. Moser, B., M. Wolf, A. Walz, and P. Loetscher. 2004. Chemokines: multiple levels of leukocyte migration control. Trends Immunol. 25: 75-84. (Pubitemid 38167488)
41. Vestergaard, C., M. Deleuran, B. Gesser, and C. Gronhoj Larsen. 2003. Expression of the T-helper 2-specific chemokine receptor CCR4 on CCR10-positive lymphocytes in atopic dermatitis skin but not in psoriasis skin. Br. J. Dermatol. 149: 457-463. (Pubitemid 37281575)
42. + regulatory and Th2 effector lymphocytes. J. Immunol. 177: 6940-6951.
43. Goya, I., J. Gutierrez, R. Varona, L. Kremer, A. Zaballos, and G. Marquez. 1998. Identification of CCR8 as the specific receptor for the human β-chemokine I-309: cloning and molecular characterization of murine CCR8 as the receptor for TCA-3. J. Immunol. 160: 1975-1981. (Pubitemid 28106488)
44. Chensue, S. W., N. W. Lukacs, T. Y. Yang, X. Shang, K. A. Frait, S. L. Kunkel, T. Kung, M. T. Wiekowski, J. A. Hedrick, D. N. Cook, et al. 2001. Aberrant in vivo T helper type 2 cell response and impaired eosinophil recruitment in CC chemokine receptor 8 knockout mice. J. Exp. Med. 193: 573-584.
45. Gonzalo, J. A., Y. Qiu, J. M. Lora, A. Al-Garawi, J. L. Villeval, J. A. Boyce, A. C. Martinez, G. Marquez, I. Goya, Q. Hamid, et al. 2007. Coordinated involvement of mast cells and T cells in allergic mucosal inflammation: critical role of the CC chemokine ligand 1:CCR8 axis. J. Immunol. 179: 1740-1750.
46. Gombert, M., M. C. Dieu-Nosjean, F. Winterberg, E. Bunemann, R. C. Kubitza, L. Da Cunha, A. Haahtela, S. Lehtimaki, A. Muller, J. Rieker, et al. 2005. CCL1- CCR8 interactions: an axis mediating the recruitment of T cells and Langerhans-type dendritic cells to sites of atopic skin inflammation. J. Immunol. 174: 5082-5091. (Pubitemid 40504594)
47. Bystry, R. S., V. Aluvihare, K. A. Welch, M. Kallikourdis, and A. G. Betz. 2001. B cells and professional APCs recruit regulatory T cells via CCL4. Nat. Immunol. 2: 1126-1132.
48. + suppressor T cells. Eur. J. Immunol. 33: 1488-1496.
49. Müller, V., D. Viemann, M. Schmidt, N. Endres, S. Ludwig, M. Leverkus, J. Roth, and M. Goebeler. 2007. Candida albicans triggers activation of distinct signaling pathways to establish a proinflammatory gene expression program in primary human endothelial cells. J. Immunol. 179: 8435-8445.
50. + regulatory T cells. J. Exp. Med. 199: 303-313.
51. + regulatory T cells. J. Exp. Med. 204: 735-745.
52. Menning, A., U. E. Hopken, K. Siegmund, M. Lipp, A. Hamann, and J. Huehn. 2007. Distinctive role of CCR7 in migration and functional activity of naive- and effector/memory-like Treg subsets. Eur. J. Immunol. 37: 1575-1583. (Pubitemid 46939492)
53. + T cells. Atherosclerosis 197: 829-839.