A novel mechanism for immunosuppression: From neuropeptides to regulatory T cells

Journal of Neuroimmune Pharmacology

Volumn 1, Issue 4, 2006, Pages 400-409

  Ganea, Doina ^a   Gonzalez Rey, Elena ^b   Delgado, Mario ^b  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b INSTITUTO DE PARASITOLOGÍA Y BIOMEDICINA LÓPEZ NEYRA   (Spain)

Author keywords

Bone marrow transplantation; Collagen induced arthritis; Experimental autoimmune encephalomyelitis; Neuropeptides; Regulatory T cells; Tolerogenic dendritic cells; Vasoactive intestinal peptide

Indexed keywords

NEUROPEPTIDE;

ANIMAL; HUMAN; IMMUNOLOGY; IMMUNOSUPPRESSIVE TREATMENT; METHODOLOGY; REGULATORY T LYMPHOCYTE; REVIEW;

ANIMALS; HUMANS; IMMUNOSUPPRESSION; NEUROPEPTIDES; T-LYMPHOCYTES, REGULATORY;

EID: 33751222594     PISSN: 15571890     EISSN: 15571904     Source Type: Journal    
DOI: 10.1007/s11481-006-9044-0     Document Type: Review

References (61)

1. Abad C, Martinez C, Leceta J, Gomariz RP, Delgado M (2001) Pituitary adenylate cyclase-activating polypeptide inhibits collagen-induced arthritis: an experimental immunomodulatory therapy. J Immunol 167:3182-3189
2. Abad C, Martinez C, Juarranz MG, Arranz A, Leceta J, Delgado M, Gomariz RP (2003) Therapeutic effects of vasoactive intestinal peptide in the trinitrobenzene sulfonic acid mice model of Crohn's disease. Gastroenterology 124:961-971
3. Abad C, Gomariz RP, Waschek JA (2006) Neuropeptide mimetics and antagonists in the treatment of inflammatory disease: focus on VIP and PACAP. Curr Top Med Chem 6:151-163
4. Bandyopadhyay A, Chakder S, Rattan S (1997) Regulation of inducible and neuronal nitric oxide synthase gene expression by interferon-gamma and VIP. Am J Physiol 272:C1790-1797
5. Chorny A, Gonzalez-Rey E, Fernandez-Martin A, Pozo D, Ganea D, Delgado M (2005) Vasoactive intestinal peptide induces regulatory dendritic cells with therapeutic effects on autoimmune disorders. Proc Natl Acad Sci USA 102:13562-13567
6. Chorny A, Gonzalez-Rey E, Fernandez-Martin A, Ganea D, Delgado M (2006) Vasoactive intestinal peptide induces regulatory dendritic cells that can prevent acute graft-versus-host disease while maintain graft-versus-tumor. Blood 107(9):3787-3794
7. Delgado M, Ganea D (1999) Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide inhibit interleukin-12 transcription by regulating nuclear factor kappaB and Ets activation. J Biol Chem 274:31930-31940
8. Delgado M, Ganea D (2001a) Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide inhibit nuclear factor-kappa B-dependent gene activation at multiple levels in the human monocytic cell line THP-1. J Biol Chem 276:369-380
9. Delgado M, Ganea D (2001b) Inhibition of endotoxin-induced macrophage chemokine production by VIP and PACAP in vitro and in vivo. Arch Physiol Biochem 109:377-382
10. Delgado M, Ganea D (2003a) Vasoactive intestinal peptide inhibits IL-8 production in human monocytes by downregulating nuclear factor kappaB-dependent transcriptional activity. Biochem Biophys Res Commun 302:275-283
11. Delgado M, Ganea D (2003b) Neuroprotective effect of vasoactive intestinal peptide (VIP) in a mouse model of Parkinson's disease by blocking microglial activation. FASEB J 17:944-946
12. Delgado M, Ganea D (2003c) Vasoactive intestinal peptide prevents activated microglia-induced neurodegeneration under inflammatory conditions: potential therapeutic role in brain trauma. FASEB J 17:1922-1924
13. Delgado M, Munoz-Elias EJ, Kan Y, Gozes I, Fridkin M, Brenneman DE, Gomariz RP, Ganea D (1998) Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide inhibit tumor necrosis factor alpha transcriptional activation by regulating nuclear factor-kB and cAMP response element-binding protein/c-Jun. J Biol Chem 273:31427-31436
14. Delgado M, Sun W, Leceta J, Ganea D (1999a) VIP and PACAP differentially regulate the costimulatory activity of resting and activated macrophages through the modulation of B7.1 and B7.2 expression. J Immunol 163:4213-4223
15. 2 responses by up-regulating B7.2 expression. J Immunol 163:3629-3635
16. Delgado M, Munoz-Elias EJ, Gomariz RP, Ganea D (1999c) Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide enhance IL-10 production by murine macrophages: in vitro and in vivo studies. J Immunol 162:1707-1716
17. Delgado M, Munoz-Elias EJ, Gomariz RP, Ganea D (1999d) VIP and PACAP inhibit IL-12 production in LPS-stimulated macrophages. Subsequent effect on IFNgamma synthesis by T cells. J Neuroimmunol 96:167-181
18. Delgado M, Munoz-Elias EJ, Gomariz RP, Ganea D (1999e) Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide prevent inducible nitric oxide synthase transcription in macrophages by inhibiting NF-kappa B and IFN regulatory factor 1 activation. J Immunol 162:4685-4696
19. Delgado M, Martinez C, Pozo D, Calvo JR, Leceta J, Ganea D, Gomariz RP (1999f) Vasoactive intestinal peptide (VIP) and pituitary adenylate cyclase-activation polypeptide (PACAP) protect mice from lethal endotoxemia through the inhibition of TNF-alpha and IL-6. J Immunol 162:1200-1205
20. Delgado M, Pozo D, Martinez C, Leceta J, Calvo JR, Ganea D, Gomariz RP (1999g) Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide inhibit endotoxin-induced TNF-alpha production by macrophages: in vitro and in vivo studies. J Immunol 162:2358-2367
21. 2 response by upregulating B7.2 expression. Ann NY Acad Sci 921:68-78
22. Delgado M, Gomariz RP, Martinez C, Abad C, Leceta J (2000b) Anti-inflammatory properties of the type 1 and type 2 vasoactive intestinal peptide receptors: role in lethal endotoxic shock. Eur J Immunol 30:3236-3246
23. Delgado M, Abad C, Martinez C, Leceta J, Gomariz RP (2001) Vasoactive intestinal peptide prevents experimental arthritis by downregulating both autoimmune and inflammatory components of the disease. Nat Med 7:563-568
24. Delgado M, Jonakait GM, Ganea D (2002a) Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide inhibit chemokine production in activated microglia. Glia 39:148-161
25. 2 cells. FASEB J 16:1844-1846
26. Delgado M, Leceta J, Ganea D (2003) Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide inhibit the production of inflammatory mediators by activated microglia. J Leukoc Biol 73:155-164
27. Delgado M, Pozo D, Ganea D (2004a) The significance of vasoactive intestinal peptide in immunomodulation. Pharmacol Rev 56:249-290
28. 2 effectors through differential regulation of chemokine production by dendritic cells. FASEB J 18:1453-1455
29. Delgado M, Reduta A, Sharma V, Ganea D (2004c) VIP/PACAP oppositely affects immature and mature dendritic cell expression of CD80/CD86 and the stimulatory activity for CD4(+) T cells. J Leukoc Biol 75:1122-1130
30. Delgado M, Gonzalez-Rey E, Ganea D (2005a) The neuropeptide vasoactive intestinal peptide generates tolerogenic dendritic cells. J Immunol 175:7311-7324
31. Delgado M, Chorny A, Gonzalez-Rey E, Ganea D (2005b) Vasoactive intestinal peptide generates CD4+CD25+ regulatory T cells in vivo. J Leukoc Biol 78:1327-1338
32. Fernandez-Martin A, Gonzalez-Rey E, Chorny A, Ganea D, Delgado M (2006) Vasoactive intestinal peptide induces regulatory T cells during experimental autoimmune encephalomyelitis. Eur J Immunol 36:318-326
33. Foey AD, Field S, Ahmed S, Jain A, Feldmann M, Brennan FM, Williams R (2003) Impact of VIP and cAMP on the regulation of TNF-alpha and IL-10 production: implications for rheumatoid arthritis. Arthritis Res Ther 5:R317-328
34. Ganea D, Delgado M (2003) The neuropeptides VIP/PACAP and T cells: inhibitors or activators? Curr Pharm Des 9:997-1004
35. Ganea D, Rodriguez R, Delgado M (2003) Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide: players in innate and adaptive immunity. Cell Mol Biol (Noisyle-grand) 49:127-142
36. Goetzl EJ, Voice JK, Shen S, Dorsam G, Kong Y, West KM, Morrison CF, Harmar AJ (2001) Enhanced delayed-type hypersensitivity and diminished immediate-type hypersensitivity in mice lacking the inducible VPAC(2) receptor for vasoactive intestinal peptide. Proc Natl Acad Sci USA 98:13854-13859
37. Gomariz RP, Arranz A, Abad C, Torroba M, Martinez C, Rosignoli F, Garcia-Gomez M, Leceta J, Juarranz Y (2005) Time-course expression of Toll-like receptors 2 and 4 in inflammatory bowel disease and homeostatic effect of VIP. J Leukoc Biol 78:491-502
38. Gonzalez-Rey E, Fernandez-Martin A, Chorny A, Delgado M (2006a) Vasoactive intestinal peptide induces CD4+, CD25+ T regulatory cells with therapeutic effect in collagen-induced arthritis. Arthritis Rheum 54:864-876
39. Gonzalez-Rey E, Fernandez-Martin A, Chorny A, Martin J, Pozo D, Ganea D, Delgado M (2006b) Therapeutic effect of vasoactive intestinal peptide on experimental autoimmune encephalomyelitis: down-regulation of inflammatory and autoimmune responses. Am J Pathol 168:1179-1188
40. Joffre O, van Meerwijk JP (2006) CD4(+)CD25(+) regulatory T lymphocytes in bone marrow transplantation. Semin Immunol 18:128-135
41. Juarranz Y, Abad C, Martinez C, Arranz A, Gutierrez-Canas I, Rosignoli F, Gomariz RP, Leceta J (2005) Protective effect of vasoactive intestinal peptide on bone destruction in the collagen-induced arthritis model of rheumatoid arthritis. Arthritis Res Ther 7:R1034-1045
42. Kaltreider HB, Ichikawa S, Byrd PK, Ingram DA, Kishiyama JL, Sreedharan SP, Warnock ML, Beck JM, Goetzl EJ (1997) Upregulation of neuropeptides and neuropeptide receptors in a murine model of immune inflammation in lung parenchyma. Am J Respir Cell Mol Biol 16:133-144
43. Kato H, Ito A, Kawanokuchi J, Jin S, Mizuno T, Ojika K, Ueda R, Suzumura A (2004) Pituitary adenylate cyclase-activating polypeptide (PACAP) ameliorates experimental autoimmune encephalomyelitis by suppressing the functions of antigen presenting cells. Mult Scler 10:651-659
44. Keino H, Kezuka T, Takeuchi M, Yamakawa N, Hattori T, Usui M (2004) Prevention of experimental autoimmune uveoretinitis by vasoactive intestinal peptide. Arch Ophthalmol 122:1179-1184
45. Kim WK, Kan Y, Ganea D, Hart RP, Gozes I, Jonakait GM (2000) Vasoactive intestinal peptide and pituitary adenylyl cyclase-activating polypeptide inhibit tumor necrosis factor-alpha production in injured spinal cord and in activated microglia via a cAMP-dependent pathway. J Neurosci 20:3622-3630
46. Kim WK, Ganea D, Jonakait GM (2002) Inhibition of microglial CD40 expression by pituitary adenylate cyclase-activating polypeptide is mediated by interleukin-10. J Neuroimmunol 126:16-24
47. Lee CM, Kumar RK, Lubowski DZ, Burcher E (2002) Neuropeptides and nerve growth in inflammatory bowel diseases: a quantitative immunohistochemical study. Dig Dis Sci 47:495-502
48. Levings MK, Gregori S, Tresoldi E, Cazzaniga S, Bonini C, Roncarolo MG (2005) Differentiation of Tr1 cells by immature dendritic cells requires IL-10 but not CD25+CD4+ Tr cells. Blood 105:1162-1169
49. Martinez C, Delgado M, Pozo D, Leceta J, Calvo JR, Ganea D, Gomariz RP (1998) Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide modulate endotoxin-induced IL-6 production by murine peritoneal macrophages. J Leukoc Biol 63:591-601
50. Martinez C, Juarranz Y, Abad C, Arranz A, Miguel BG, Rosignoli F, Leceta J, Gomariz RP (2005) Analysis of the role of the PAC1 receptor in neutrophil recruitment, acute-phase response, and nitric oxide production in septic shock. J Leukoc Biol 77:729-738
51. Mosimann BL, White MV, Hohman RJ, Goldrich MS, Kaulbach HC, Kaliner MA (1993) Substance P, calcitonin gene-related peptide, and vasoactive intestinal peptide increase in nasal secretions after allergen challenge in atopic patients. J Allergy Clin Immunol 92:95-104
52. Nieber K, Baumgarten CR, Rathsack R, Furkert J, Oehme P, Kunkel G (1992) Substance P and beta-endorphin-like immunoreactivity in lavage fluids of subjects with and without allergic asthma. J Allergy Clin Immunol 90:646-652
53. Owens T (2006) Animal models for multiple sclerosis. Adv Neurol 98:77-89
54. Rameshwar P, Gascon P, Oh HS, Denny TN, Zhu G, Ganea D (2002) Vasoactive intestinal peptide (VIP) inhibits the proliferation of bone marrow progenitors through the VPAC1 receptor. Exp Hematol 30:1001-1009
55. 1 effectors. J Immunol 176:97-110
56. Tuncel N, Tore F, Sahinturk V, Ak D, Tuncel M (2000) Vasoactive intestinal peptide inhibits degranulation and changes granular content of mast cells: a potential therapeutic strategy in controlling septic shock. Peptides 21:81-89
57. Voice JK, Dorsam G, Lee H, Kong Y, Goetzl EJ (2001) Allergic diathesis in transgenic mice with constitutive T cell expression of inducible vasoactive intestinal peptide receptor. FASEB J 15:2489-2496
58. Voice JK, Grinninger C, Kong Y, Bangale Y, Paul S, Goetzl EJ (2003) Roles of vasoactive intestinal peptide (VIP) in the expression of different immune phenotypes by wild-type mice and T cell-targeted type II VIP receptor transgenic mice. J Immunol 170:308-314
59. 2 differentiation induced by the type 2 G protein-coupled receptor (VPAC2) for vasoactive intestinal peptide. J Immunol 172:7289-7296
60. Xin Z, Sriram S (1998) Vasoactive intestinal peptide inhibits IL-12 and nitric oxide production in murine macrophages. J Neuroimmunol 89:206-212
61. Zafirova Y, Yordanov M, Kalfin R (2004) Antiarthritic effect of VIP in relation to the host resistance against Candida albicans infection. Int Immunol 16:1125-1131