VIP deficient mice exhibit resistance to lipopolysaccharide induced endotoxemia with an intrinsic defect in proinflammatory cellular responses

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Abad, Catalina ^a   Tan, Yossan Var ^a   Cheung Lau, Gardenia ^a   Nobuta, Hiroko ^a   Waschek, James A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOTOXIN; I KAPPA B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 12P40; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MESSENGER RNA; RNA; TUMOR NECROSIS FACTOR ALPHA; VASOACTIVE INTESTINAL POLYPEPTIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; ENDOTOXEMIA; FEMALE; HISTOLOGY; IMMUNOCOMPETENT CELL; IN VITRO STUDY; IN VIVO STUDY; KNOCKOUT MOUSE; LUNG; MORTALITY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PERITONEUM CELL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; RNA ISOLATION; SPLEEN; SURVIVAL; TISSUE INJURY;

ANIMALS; ENDOTOXEMIA; ENDOTOXINS; FEMALE; INFLAMMATION; INFLAMMATION MEDIATORS; INTERLEUKIN-12; INTERLEUKIN-6; LIPOPOLYSACCHARIDES; LUNG; MICE; MICE, INBRED C57BL; NEUROPEPTIDES; NF-KAPPA B; RNA, MESSENGER; SPLEEN; TUMOR NECROSIS FACTOR-ALPHA; VASOACTIVE INTESTINAL PEPTIDE;

MURINAE; MUS;

EID: 84861204731     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0036922     Document Type: Article

References (48)

1. Medzhitov R, (2008) Origin and physiological roles of inflammation. Nature 454: 428-435.
2. Jean-Baptiste E, (2007) Cellular mechanisms in sepsis. J Intensive Care Med 22: 63-72.
3. Silva MT, (2010) When two is better than one: macrophages and neutrophils work in concert in innate immunity as complementary and cooperative partners of a myeloid phagocyte system. J Leukoc Biol 87: 93-106.
4. Sadik CD, Kim ND, Luster AD, (2011) Neutrophils cascading their way to inflammation. Trends Immunol 32: 452-460.
5. Stearns-Kurosawa DJ, Osuchowski MF, Valentine C, Kurosawa S, Remick DG, (1991) The pathogenesis of sepsis. Annu Rev Pathol 6: 19-48.
6. Kawai T, Akira S, (2010) The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol 11: 373-384.
7. Lu YC, Yeh WC, Ohashi PS, (2008) LPS/TLR4 signal transduction pathway. Cytokine 42: 145-151.
8. Kawai T, Akira S, (2007) Signaling to NF-kappaB by Toll-like receptors. Trends Mol Med 13: 460-469.
9. Serhan CN, Savill J, (2005) Resolution of inflammation: the beginning programs the end. Nat Immunol 6: 1191-1197.
10. Delgado M, Ganea D, (2008) Anti-inflammatory neuropeptides: a new class of endogenous immunoregulatory agents. Brain Behav Immun 22: 1146-1151.
11. Delgado M, Pozo D, Ganea D, (2004) The significance of vasoactive intestinal peptide in immunomodulation. Pharmacol Rev 56: 249-290.
12. Gomariz RP, Martinez C, Abad C, Leceta J, Delgado M, (2001) Immunology of VIP: a review and therapeutical perspectives. Curr Pharm Des 7: 89-111.
13. Laburthe M, Couvineau A, Tan V, (2007) Class II G protein-coupled receptors for VIP and PACAP: structure, models of activation and pharmacology. Peptides 28: 1631-1639.
14. Delgado M, Ganea D, (2001) Inhibition of endotoxin-induced macrophage chemokine production by vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide in vitro and in vivo. J Immunol 167: 966-975.
15. Ganea D, Delgado M, (2001) Neuropeptides as modulators of macrophage functions. Regulation of cytokine production and antigen presentation by VIP and PACAP. Arch Immunol Ther Exp (Warsz) 49: 101-110.
16. 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.
17. Abad C, Martinez C, Juarranz MG, Arranz A, Leceta J, et al. (2003) Therapeutic effects of vasoactive intestinal peptide in the trinitrobenzene sulfonic acid mice model of Crohn's disease. Gastroenterology 124: 961-971.
18. Delgado M, Martinez C, Pozo D, Calvo JR, Leceta J, et al. (1999) 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.
19. Gonzalez-Rey E, Fernandez-Martin A, Chorny A, Martin J, Pozo D, et al. (2006) Therapeutic effect of vasoactive intestinal peptide on experimental autoimmune encephalomyelitis: down-regulation of inflammatory and autoimmune responses. Am J Pathol 168: 1179-1188.
20. Brandtzaeg P, Oktedalen O, Kierulf P, Opstad PK, (1989) Elevated VIP and endotoxin plasma levels in human gram-negative septic shock. Regul Pept 24: 37-44.
21. Delgado M, Pozo D, Martinez C, Leceta J, Calvo JR, et al. (1999) 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.
22. Ait-Ali D, Stroth N, Sen JM, Eiden LE., PACAP-cytokine interactions govern adrenal neuropeptide biosynthesis after systemic administration of LPS. Neuropharmacology 58: 208-214.
23. Martinez C, Delgado M, Abad C, Gomariz RP, Ganea D, et al. (1999) Regulation of VIP production and secretion by murine lymphocytes. J Neuroimmunol 93: 126-138.
24. Szema AM, Hamidi SA, Lyubsky S, Dickman KG, Mathew S, et al. (2006) Mice lacking the VIP gene show airway hyperresponsiveness and airway inflammation, partially reversible by VIP. Am J Physiol Lung Cell Mol Physiol 291: L880-886.
25. Colwell CS, Michel S, Itri J, Rodriguez W, Tam J, et al. (2003) Disrupted circadian rhythms in VIP- and PHI-deficient mice. Am J Physiol Regul Integr Comp Physiol 285: R939-949.
26. Hamidi SA, Prabhakar S, Said SI, (2008) Enhancement of pulmonary vascular remodelling and inflammatory genes with VIP gene deletion. Eur Respir J 31: 135-139.
27. Abad C, Tan YV, Lopez R, Nobuta H, Dong H, et al. (2010) Vasoactive intestinal peptide loss leads to impaired CNS parenchymal T-cell infiltration and resistance to experimental autoimmune encephalomyelitis. Proc Natl Acad Sci U S A 107: 19555-19560.
28. Matute-Bello G, Winn RK, Jonas M, Chi EY, Martin TR, et al. (2001) Fas (CD95) induces alveolar epithelial cell apoptosis in vivo: implications for acute pulmonary inflammation. Am J Pathol 158: 153-161.
29. Scotland RS, Stables MJ, Madalli S, Watson P, Gilroy DW, (2011) Sex differences in resident immune cell phenotype underlie more efficient acute inflammatory responses in female mice. Blood 118: 5918-5927.
30. Hansen MK, Nguyen KT, Fleshner M, Goehler LE, Gaykema RP, et al. (2000) Effects of vagotomy on serum endotoxin, cytokines, and corticosterone after intraperitoneal lipopolysaccharide. Am J Physiol Regul Integr Comp Physiol 278: R331-336.
31. Batoulis H, Addicks K, Kuerten S, (2010) Emerging concepts in autoimmune encephalomyelitis beyond the CD4/T(H)1 paradigm. Ann Anat 192: 179-193.
32. Li JM, Southerland L, Hossain MS, Giver CR, Wang Y, et al. (2011) Absence of vasoactive intestinal peptide expression in hematopoietic cells enhances Th1 polarization and antiviral immunity in mice. J Immunol 187: 1057-1065.
33. Beutler B, Cerami A, (1988) Tumor necrosis, cachexia, shock, and inflammation: a common mediator. Annu Rev Biochem 57: 505-518.
34. ten Cate H, (2000) Pathophysiology of disseminated intravascular coagulation in sepsis. Crit Care Med 28: S9-11.
35. Zhao K, Kirman I, Tschepen I, Schwab R, Weksler ME, (1997) Peritoneal lavage reduces lipopolysaccharide-induced elevation of serum TNF-alpha and IL-6 mortality in mice. Inflammation 21: 379-390.
36. El-behi M, Rostami A, Ciric B, (2010) Current views on the roles of Th1 and Th17 cells in experimental autoimmune encephalomyelitis. J Neuroimmune Pharmacol 5: 189-197.
37. Agrawal S, Anderson P, Durbeej M, van Rooijen N, Ivars F, et al. (2006) Dystroglycan is selectively cleaved at the parenchymal basement membrane at sites of leukocyte extravasation in experimental autoimmune encephalomyelitis. J Exp Med 203: 1007-1019.
38. Huitinga I, van Rooijen N, de Groot CJ, Uitdehaag BM, Dijkstra CD, (1990) Suppression of experimental allergic encephalomyelitis in Lewis rats after elimination of macrophages. J Exp Med 172: 1025-1033.
39. Bauer J, Huitinga I, Zhao W, Lassmann H, Hickey WF, et al. (1995) The role of macrophages, perivascular cells, and microglial cells in the pathogenesis of experimental autoimmune encephalomyelitis. Glia 15: 437-446.
40. Huang DR, Wang J, Kivisakk P, Rollins BJ, Ransohoff RM, (2001) Absence of monocyte chemoattractant protein 1 in mice leads to decreased local macrophage recruitment and antigen-specific T helper cell type 1 immune response in experimental autoimmune encephalomyelitis. J Exp Med 193: 713-726.
41. Fife BT, Huffnagle GB, Kuziel WA, Karpus WJ, (2000) CC chemokine receptor 2 is critical for induction of experimental autoimmune encephalomyelitis. J Exp Med 192: 899-905.
42. Ellrichmann G, Thone J, Lee DH, Rupec RA, Gold R, et al. (2012) Constitutive activity of NF-kappa B in myeloid cells drives pathogenicity of monocytes and macrophages during autoimmune neuroinflammation. J Neuroinflammation 9: 15.
43. Delgado M, Munoz-Elias EJ, Gomariz RP, Ganea D, (1999) VIP and PACAP inhibit IL-12 production in LPS-stimulated macrophages. Subsequent effect on IFNgamma synthesis by T cells. J Neuroimmunol 96: 167-181.
44. Delgado M, Munoz-Elias EJ, Gomariz RP, Ganea D, (1999) 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.
45. Martinez C, Delgado M, Pozo D, Leceta J, Calvo JR, et al. (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.
46. Martinez C, Delgado M, Pozo D, Leceta J, Calvo JR, et al. (1998) VIP and PACAP enhance IL-6 release and mRNA levels in resting peritoneal macrophages: in vitro and in vivo studies. J Neuroimmunol 85: 155-167.
47. Cai Y, Xin X, Shim GJ, Mokuno Y, Uehara H, et al. (1997) Pituitary adenylate cyclase activating polypeptide (PACAP) and vasoactive intestinal peptide (VIP) stimulate interleukin-6 production through the third subtype of PACAP/VIP receptor in rat bone marrow-derived stromal cells. Endocrinology 138: 2515-2520.
48. Biswas SK, Lopez-Collazo E, (2009) Endotoxin tolerance: new mechanisms, molecules and clinical significance. Trends Immunol 30: 475-487.