Immunomodulation of innate immune responses by vasoactive intestinal peptide (VIP): Its therapeutic potential in inflammatory disease

Clinical and Experimental Immunology

Volumn 157, Issue 2, 2009, Pages 225-234

  Smalley, S G R ^a   Barrow, P A ^a   Foster, N ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

Cytokine; Innate immunity; TLR; VIP

Indexed keywords

TOLL LIKE RECEPTOR 1; VASOACTIVE INTESTINAL POLYPEPTIDE;

CELL ACTIVATION; CELL FUNCTION; CONTROLLED STUDY; DENDRITIC CELL; EOSINOPHIL; HUMAN; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; IMMUNOPROPHYLAXIS; INFLAMMATORY DISEASE; INNATE IMMUNITY; MACROPHAGE; MAST CELL; MONOCYTE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; REVIEW;

CYTOKINES; DENDRITIC CELLS; HUMANS; IMMUNE SYSTEM DISEASES; IMMUNITY, INNATE; INFLAMMATION MEDIATORS; RECEPTORS, VASOACTIVE INTESTINAL PEPTIDE; TOLL-LIKE RECEPTORS; VASOACTIVE INTESTINAL PEPTIDE;

EID: 67650689306     PISSN: 00099104     EISSN: 13652249     Source Type: Journal    
DOI: 10.1111/j.1365-2249.2009.03956.x     Document Type: Review

References (95)

1. Said SI, Mutt V. A peptide fraction from lung tissue with prolonged vasodilatory activity. Scand J Clin Lab Invest Suppl 1969 107 : 51 6.
2. Said SI, Mutt V. Isolation from porcine intestinal wall of a vasoactive octacosapeptide related to secretin and to glucagon. Eur J Biochem 1972 28 : 199 204.
3. Said SI, Rosenberg RN. Vasoactive intestinal polypeptide: abundant immunoreactivity in neuronal cell lines and normal nervous tissues. Science 1976 192 : 907 8.
4. Henning RJ, Sawmiller DR. Vasoactive intestinal peptide: cardiovascular effects. Cardiovasc Res 2001 49 : 27 37.
5. D'Amato M, De Beurme FA, Lefebvre RA. Comparison of the effect of vasoactive intestinal polypeptide and non-adrenergic non-cholinergic neurone stimulation in the cat gastric fundus. Eur J Pharmacol 1988 152 : 71 82. (Pubitemid 18187803)
6. Grider JR, Rivier JR. Vasoactive intestinal peptide (VIP) as transmitter of inhibitory motor neurones of the gut: evidence from the use of selective VIP antagonists and VIP antiserum. J Pharmacol Exp Ther 1990 253 : 738 42.
7. Vaudry D, Gonzalez BJ, Basille M, Yon L, Fournier A, Vaudry H. Pituitary adenylate cyclase-activating polypeptide and its receptors: from structure to functions. Pharmacol Rev 2000 52 : 269 324. (Pubitemid 30368434)
8. Nishizawa M, Hayakawa Y, Yanaihara N, Okamoto H. Nucleotide sequence divergence and functional constraint in VIP mRNA evolution between human and rat. FEBS Lett 1985 183 : 55 9.
9. Itoh N, Obata K, Yanaihara N, Okamoto H. Human preprovasoactive intestinal polypeptide contains a novel PHI-27-like peptide, PHM-27. Nature 1983 304 : 547 9.
10. Du B-H, Eng J, Hulmes JD, Chang M, Pan EY-C, Yalow RS. Guinea pig has a unique mammalian VIP. Biochem Biophys Res Commun 1985 128 : 1093 8.
11. Chartrel N, Wang Y, Fournier A, Vaudry H, Conlon MJ. Frog vasoactive intestinal peptide and galanin: primary structures and effects on pituitary adenylate cyclase. Endocrinology 1995 136 : 3079 86.
12. Wang Y, Conlon JM. Neuroendocrine peptides (NPY, GRP, VIP, somatostatin) from the brain and stomach of the alligator. Peptides 1993 14 : 573 9.
13. Nilsson A. Structure of the vasoactive intestinal octacosapeptide from chicken intestine. The amino acid sequence. FEBS Lett 1975 60 : 322 6.
14. Thwaites DT, Young J, Thorndyke MC, Dimaline R. The isolation and chemical characterization of a novel vasoactive intestinal peptide-related peptide from a teleost fish, the cod, Gadus morhua. Biochim Biophys Acta 1989 999 : 217 20.
15. Ishihara T, Shigemoto R, Mori K, Takahashi K, Nagata S. Functional expression and tissue distribution of a novel receptor for vasoactive intestinal polypeptide. Neuron 1992 8 : 811 19.
16. Lutz EM, Sheward WJ, West KM, Morrow JA, Fink G, Harmar AJ. The VIP2 receptor: molecular characterisation of a cDNA encoding a novel receptor for vasoactive intestinal peptide. FEBS Lett 1993 334 : 3 8.
17. Couvineau A, Rouyer-Fessard C, Darmoul D et al. Cloning and functional expression of two cDNA encoding proteins with different N-terminal domains. Biochem Biophys Res Commun 1994 200 : 769 76.
18. Harmar AJ, Arimura A, Gozes I et al. International union of pharmacology. XVIII. Nomenclature of receptors for vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide. Pharmacol Rev 1998 50 : 265 70.
19. Laburthe M, Couvineau A. Molecular pharmacology and structure of VPAC receptors for VIP and PACAP. Regul Pept 2002 108 : 165 73.
20. Campbell RM, Scanes CG. Evolution of the growth hormone-releasing factor (GRF) family of peptides. Growth Regul 1992 2 : 175 91.
21. Segre GV, Goldring SR. Receptors for secretin, calcitonin, parathyroid hormone (PTH)/PTH-related peptide, glucagon-like peptide 1, growth hormone-releasing hormone, and glucagon belong to a newly discovered G-protein-linked receptor family. Trends Endocrinol Metab 1993 4 : 309 14.
22. Rawlings SR, Hezareh M. Pituitary adenylate cyclase-activating polypeptide (PACAP) and PACAP/vasoactive intestinal polypeptide receptors: actions on the anterior pituitary gland. Endocr Rev 1996 17 : 4 29. (Pubitemid 26061365)
23. Laburthe M, Rousset M, Boissard C, Chevalier G, Zweibaum A, Rosselin G. Vasoactive intestinal peptide: a potent stimulator of adenosine 3′:5′-cyclic monophosphate accumulation in gut carcinoma cell lines in culture. Proc Natl Acad Sci USA 1978 75 : 2772 5.
24. Salomon R, Couvineau A, Rouyer-Fessard C et al. Characterization of a common VIP-PACAP receptor in human small intestinal epithelium. Am J Physiol 1993 264 : 294 300.
25. MacKenzie CJ, Lutz EM, McCulloch DA, Mitchell R, Harmar AJ. Phospholipase C activation by VIP1 and VIP2 receptors expressed in COS 7 cells involves a pertussis toxin-sensitive mechanism. Ann NY Acad Sci 1996 26 : 579 84.
26. Boissard C, Marie JC, Hejblum G, Gespach C, Rosselin G. Vasoactive intestinal peptide receptor regulation and reversible desensitization in human colonic carcinoma cells in culture. Cancer Res 1986 46 : 4406 13.
27. Kulka M, Sheen CH, Tancowny BP, Grammer LC, Schleimer RP. Neuropeptides activate human mast cell degranulation and chemokine production. Immunology 2008 123 : 398 410. (Pubitemid 351171192)
28. Harfi I, D'Hondt S, Corazza F, Sariban E. Regulation of human polymorphonuclear leukocytes functions by the neuropeptide pituitary adenylate cyclase-activating polypeptide after activation of MAPKs. J Immunol 2004 173 : 4154 63.
29. Lara-Marquez ML, O'Dorisio MS, Karacay B. Vasoactive intestinal peptide (VIP) receptor type 2 (VPAC2) is the predominant receptor expressed in human thymocytes. Ann NY Acad Sci 2000 921 : 45 54. (Pubitemid 32094527)
30. El Zein N, Badran B, Sariban E. VIP differentially activates beta2 integrins, CR1, and matrix metalloproteinase-9 in human monocytes through cAMP/PKA, EPAC, and PI-3K signaling pathways via VIP receptor type 1 and FPRL1. J Leukoc Biol 2008 83 : 972 81.
31. Kojima M, Ito T, Oono T et al. VIP attenuation of the severity of experimental pancreatitis is due to VPAC1 receptor-mediated inhibition of cytokine production. Pancreas 2005 30 : 62 70. (Pubitemid 40070628)
32. Delgado M, Munoz-Elias EJ, Gomariz RP, Ganea D. 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 1999 162 : 4685 96.
33. Delneste Y, Herbault N, Galea B et al. Vasoactive intestinal polypeptide synergizes with TNF-α in inducing human dendritic cell maturation. J Immunol 1999 163 : 3071 5.
34. Delgado M, Reduta A, Sharma V, Ganea D. VIP/PACAP oppositely affects immature and mature dendritic cell expression of CD80/CD86 and the stimulatory activity for CD4(+) T cells. J Leukoc Biol 2004 75 : 1122 30.
35. Cutz E, Chan E, Track NS, Goth A, Said SI. Release of vasoactive intestinal polypeptide in mast cells by histamine liberators. Nature 1978 275 : 661 2.
36. Fjellner B, Hägermark O. Studies on pruritogenic and histamine-releasing effects of some putative peptide neurotransmitters. Acta Derm Venereol 1981 61 : 245 50.
37. Rijnierse A, Nijkamp FP, Kraneveld A. Mast cells and nerve tickle in the tummy. Implications for inflammatory bowel disease and irritable bowel syndrome. Pharmacol Ther 2007 116 : 207 35.
38. Wershil BK, Turck CW, Sreedharan SP et al. Variants of vasoactive intestinal peptide in mouse mast cells and rat basophilic leukaemia cells. Cell Immunol 1993 151 : 369 78.
39. Voice JK, Grinninger C, Kong Y, Bangale Y, Paul S, Goetzl EJ. 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 2003 170 : 308 14.
40. O'Dorisio MS, O'Dorisio TM, Cataland S, Balcerzak SP. Vasoactive intestinal polypeptide as a biochemical marker for polymorphonuclear leukocytes. J Lab Clin Med 1980 96 : 666 72.
41. Pedrera C, Lucas M, Bellido L, López-González MA. Receptor-independent mechanisms are involved in the priming of neutrophil's oxidase by vasoactive intestinal peptide. Regul Pept 1994 54 : 505 11.
42. López-González MA, Lucas M. Priming effect of vasoactive intestinal peptide on the respiratory burst of neutrophils non-mediated by plasma membrane receptors. Experientia 1994 50 : 486 8.
43. Palermo MS, Vermeulen ME, Giordano MN. Human antibody-dependent cellular cytotoxicity mediated by interferon gamma-activated neutrophils is impaired by vasoactive intestinal peptide. J Neuroimmunol 1996 69 : 123 8.
44. Metwali A, Blum A, Ferraris L, Klein J, Fiocchi C, Weinstock J. Eosinophils within the healthy or inflamed human intestine produce substance P and vasoactive intestinal peptide. J Neuroimmunol 1994 52 : 69 78. (Pubitemid 24182248)
45. Dunzendorfer S, Meierhofer C, Wiedermann CJ. Signalling in neuropeptide-induced migration of human eosinophils. J Leukoc Biol 1998 64 : 828 34.
46. Dunzendorfer S, Feistritzer C, Enrich B, Wiedermann CJ. Neuropeptide-induced inhibition of IL-16 release from eosinophils. Neuroimmunomodulation 2002-2003 10 : 217 23.
47. Dewit D, Gourlet P, Amraoui Z et al. The vasoactive intestinal peptide analogue RO25-1553 inhibits the production of TNF and IL-12 by LPS-activated monocytes. Immunol Lett 1998 60 : 57 60. (Pubitemid 28133325)
48. Xin Z, Sriram S. Vasoactive intestinal peptide inhibits IL-12 and nitric oxide production in murine macrophages. J Neuroimmunol 1998 89 : 206 12.
49. Delgado M. Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide inhibit the MEKK1/MEK4/JNK signaling pathway in endotoxin-activated microglia. Biochem Biophys Res Commun 2002 293 : 771 6.
50. Delgado M, Pozo D, Martinez C et al. 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 1999 162 : 2358 67.
51. Foster N, Hulme SD, Barrow PA. Inhibition of IFN-gamma-stimulated proinflammatory cytokines by vasoactive intestinal peptide (VIP) correlates with increased survival of Salmonella enterica serovar typhimurium phoP in murine macrophages. J Interferon Cytokine Res 2005 25 : 31 42. (Pubitemid 40105589)
52. Foster N, Cheetham J, Taylor JJ, Preshaw PM. VIP inhibits Porphyromonas gingivalis LPS-induced immune responses in human monocytes. J Dent Res 2005 84 : 999 1004. (Pubitemid 43828145)
53. Delgado M, Ganea D. Vasoactive intestinal peptide and pituitary adenylate cyclase activating polypeptide inhibit expression of Fas ligand in activated T lymphocytes by regulating c-Myc, NFκB, NF-AT, and early growth factors 2/3. J Immunol 2001 166 : 1028 40.
54. Yang X-J, Ogyzko VV, Nishikawa J, Howard BH, Nakatani Y. A p300/CBP-associated factor that competes with the adenoviral oncoprotein E1A. Nature 1996 382 : 319 24.
55. Delgado M, Munoz-Elias EJ, Gomariz RP, Ganea D VIP and PACAP inhibit IL-12 production in LPS-stimulated macrophages. Subsequent effect on IFN gamma synthesis by T cells. J Neuroimmunol 1999 96 : 167 81.
56. Delgado M, Ganea D. Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide inhibit interleukin-12 transcription by regulating nuclear factor kappaB and Ets activation. J Biol Chem 1999 274 : 31930 40.
57. Delgado M, Ganea D. Vasoactive intestinal peptide and pituitary adenylate cyclase activating polypeptide inhibit the MEKK1/MEK4/JNK signaling pathway in LPS-stimulated macrophages. J Neuroimmunol 2000 110 : 97 105. (Pubitemid 30750460)
58. Foster N, Hulme SD, Barrow PA. Induction of antimicrobial pathways during early-phase immune response to Salmonella spp. in murine macrophages: gamma interferon (IFN-gamma) and upregulation of IFN-gamma receptor alpha expression are required for NADPH phagocytic oxidase gp91-stimulated oxidative burst and control of virulent Salmonella spp. Infect Immun 2003 71 : 4733 41.
59. Foster N, Hulme SD, Barrow PA. Vasoactive intestinal peptide (VIP) prevents killing of virulent and phoP mutant Salmonella typhimurium by inhibiting IFN-gamma stimulated NADPH oxidative pathways in murine macrophages. Cytokine 2006 36 : 134 40.
60. Fields PI, Groisman EA, Heffron F. A Salmonella locus that controls resistance to microbicida proteins from phagocytic cells. Science 1989 243 : 1059 62.
61. Miller SI, Kukral AM, Mekalanos JJ. A two componenet regulatory system (phoP-phoQ) controls Salmonella typhimurium virulence. Proc Natl Acad Sci USA 1989 86 : 5054 8.
62. Ganea D, Delgado M. Vasoactive intestinal peptide (VIP) and pituitary adenylate cyclase-activating polypeptide (PACAP) as modulators of both innate and adaptive immunity. Crit Rev Oral Biol Med 2002 13 : 229 37.
63. Delgado M, Munoz-Elias EJ, Gomariz RP, Ganea D. Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide enhance IL-10 production by murine macrophages: in vitro and in vivo studies. J Immunol 1999 162 : 1707 16.
64. Kim SH, Eisenstein M, Reznikov L et al. Structural requirements of six naturally occurring isoforms of the IL-18 binding protein to inhibit IL-18. Proc Natl Acad Sci USA 2000 97 : 1190 5.
65. Novick D, Schwartsburd B, Pinkus R et al. A novel IL-18BP ELISA shows elevated serum IL-18BP in sepsis and extensive decrease of free IL-18. Cytokine 2001 14 : 334 42.
66. Foster N, Andreadou K, Jamieson L, Preshaw PM, Taylor JJ. VIP inhibits P. gingivalis LPS-induced IL-18 and IL-18BPa in monocytes. J Dent Res 2007 86 : 883 7.
67. Inaba K, Steinman RM. Protein-specific helper T-lymphocyte formation initiated by dendritic cells. Science 1985 229 : 475 9.
68. Joffre O, Nolte MA, Spörri R, Reis e Sousa C. Inflammatory signals in dendritic cell activation and the induction of adaptive immunity. Immunol Rev 2009 227 : 234 47.
69. Chorny A, Gonzalez-Rey E, Fernandez-Martin A, Pozo D, Ganea D, Delgado M. Vasoactive intestinal peptide induces regulatory dendritic cells with therapeutic effects on autoimmune disorders. Proc Natl Acad Sci USA 2005 102 : 13562 7.
70. Gonzalez-Rey E, Chorny A, Fernandez-Martin A, Ganea D, Delgado M. Vasoactive intestinal peptide generates human tolerogenic dendritic cells that induce CD4 and CD8 regulatory T cells. Blood 2006 107 : 3632 8.
71. Gomariz RP, Arranz A, Abad C et al. Time-course expression of Toll-like receptors 2 and 4 in inflammatory bowel disease and homeostatic effect of VIP. J Leukoc Biol 2005 78 : 491 502. (Pubitemid 41061321)
72. Arranz A, Juarranz Y, Leceta J, Gomariz RP, Martínez C. VIP balances innate and adaptive immune responses induced by specific stimulation of TLR2 and TLR4. Peptides 2008 29 : 948 56.
73. Gutiérrez-Cañas I, Juarranz Y, Santiago B et al. VIP down-regulates TLR4 expression and TLR4-mediated chemokine production in human rheumatoid synovial fibroblasts. Rheumatology 2006 45 : 527 32.
74. Musikacharoen T, Matsuguchi T, Kikuchi T, Yoshikai Y. NF-κ and STAT5 play important roles in the regulation of mouse Toll-like receptor 2 gene expression. J Immunol 2001 166 : 4516 24.
75. Delgado M, Munoz-Elias EJ, Kan Y et al. 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 1998 273 : 31427 36.
76. Delgado M, Ganea D. Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide inhibit nuclear factor-κB-dependent gene activation at multiple levels in the human monocytic cell line THP-1. J Biol Chem 2001 276 : 369 80.
77. Rehli M. Of mice and men: species variation of Toll-like receptor variation. Trends Immunol 2002 23 : 375 8.
78. Haehnel V, Schwarzfischer L, Fenton MJ, Rehli M. Transcriptional regulation of the human Toll-like receptor 2 gene in monocytes and macrophages. J Immunol 2002 168 : 5629 37.
79. Rehli M, Poltorak A, Schwarzfischer L, Krause SW, Andreesen R, Beutler B. PU.1 and interferon consensus sequence-binding protein regulate the myeloid expression of the human Toll-like receptor 4 gene. J Biol Chem 2000 275 : 9773 81.
80. Shivdasani RA, Orkin SH. The transcriptional control of hematopoiesis. Blood 1996 87 : 4025 39.
81. Zhang DE, Hetherington CJ, Chen HM, Tenen DG. The macrophage transcription factor PU.1 directs tissue-specific expression of the macrophage colony-stimulating factor receptor. Mol Cell Biol 1994 14 : 373 81.
82. Foster N, Lea SR, Preshaw PM, Taylor JJ. Pivotal advance: vasoactive intestinal peptide inhibits up-regulation of human monocyte TLR2 and TLR4 by LPS and differentiation of monocytes to macrophages. J Leukoc Biol 2007 81 : 893 903. (Pubitemid 46495637)
83. Arranz A, Androulidaki A, Zacharioudaki V et al. Vasoactive intestinal peptide suppresses toll-like receptor 4 expression in macrophages via Akt1 reducing their responsiveness to lipopolysaccharide. Mol Immunol 2008 45 : 2970 80.
84. Arranz A, Abad C, Juarranz Y, Leceta J, Martinez C, Gomariz RP. Vasoactive intestinal peptide as a healing mediator in Crohn's disease. Neuroimmunomodulation 2008 15 : 46 53.
85. Gonzalez-Rey E, Delgado M. Therapeutic treatment of experimental colitis with regulatory dendritic cells generated with vasoactive intestinal peptide. Gastroenterology 2006 131 : 1799 811.
86. Delgado M, Martinez C, Pozo D et al. 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 1999 162 : 1200 5.
87. Delgado M, Abad C, Martinez C, Leceta J, Gomariz RP. Vasoactive intestinal peptide prevents experimental arthritis by downregulating both autoimmune and inflammatory components of the disease. Nat Med 2001 7 : 563 8.
88. Delgado M, Robledo G, Rueda B et al. Genetic association of vasoactive intestinal peptide receptor with rheumatoid arthritis: altered expression and signal in immune cells. Arthritis Rheum 2008 58 : 1010 19.
89. Delgado MD, Ganea D. Vasoactive intestinal peptide prevents activated microglia-induced neurodegeneration under inflammatory conditions: potential therapeutic role in brain trauma. FASEB J 2003 17 : 1922 4.
90. Kim WK, Kan Y, Ganea D, Hart RP, Gozes I, Jonakait GM. Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide inhibit tumor necrosis factor-α production in injured spinal cord and in activated microglia via a cAMP-dependent pathway. J Neurosci 2000 20 : 3622 30.
91. Quintana FJ, Zaltzman R, Fernandez-Montesinos R et al. NAP, a peptide derived from the activity-dependent neuroprotective protein, modulates macrophage function. Ann NY Acad Sci 2006 1070 : 500 6.
92. Rubinstein I. Human VIP-alpha: an emerging biologic response modifier to treat primary pulmonary hypertension. Expert Rev Cardiovasc Ther 2005 3 : 565 9.
93. Gololobov G, Noda Y, Sherman S, Rubinstein I, Baranowska-Kortylewicz J, Paul S. Stabilization of vasoactive intestinal peptide by lipids. J Pharmacol Exp Ther 1998 285 : 753 8.
94. Sethi V, Onyüksel H, Rubinstein I. Liposomal vasoactive intestinal peptide. Methods Enzymol 2005 391 : 377 95.
95. Hajos F, Stark B, Hensler S, Prassl R, Mosgoeller W. Inhalable liposomal formulation for vasoactive intestinal peptide. Int J Pharm 2008 357 : 286 94.