Vasoactive intestinal peptide inhibits liver pathology in acute murine schistosomiasis mansoni and modulates IL-10, IL-12 and TNF-α production

Immunobiology

Volumn 212, Issue 8, 2007, Pages 603-612

  Allam, Gamal ^a  

^a Beni Suef University   (Egypt)

Author keywords

Cytokine serum levels; Hepatic granuloma formation; Liver pathology; Murine schistosomiasis mansoni; Vasoactive intestinal peptide

Indexed keywords

ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; CA 19-9 ANTIGEN; COLLAGEN; GAMMA GLUTAMYLTRANSFERASE; INTERLEUKIN 10; INTERLEUKIN 12; TUMOR NECROSIS FACTOR ALPHA; VASOACTIVE INTESTINAL POLYPEPTIDE;

ACUTE DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTHELMINTIC ACTIVITY; ARTICLE; CERCARIA (TREMATODE LARVA); CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE COURSE; DRUG EFFICACY; ENZYME ACTIVITY; LIVER GRANULOMA; LIVER HOMOGENATE; MALE; MOUSE; NONHUMAN; PARASITE IMMUNITY; PARASITIC LIVER DISEASE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN CONTENT; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS; TUMOR VOLUME;

EID: 34548480194     PISSN: 01712985     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.imbio.2007.05.006     Document Type: Article

References (92)

1. Abath F.G., Morais C.N., Montenegro C.E., Wynn T.A., and Montenegro S.M. Immunopathogenic mechanisms in schistosomiasis: what can be learnt from human studies?. Trends Parasitol. 22 (2006) 85-91
2. Abelev G.I. Alpha-fetoprotein (biology). Vestn. Ross. Akad. Med. Nauk. 9 (2001) 77-83
3. Allam G., and Ahmed O.M. Does Salmonella typhimurium lipopolysaccharide have prophylactic potentials against murine Schistosomiasis mansoni ?. Egypt. J. Zool. 45 (2005) 389-408
4. Amiri P., Locksley R.M., Parslow T.G., Sadick M., Rector E., Ritter D., and McKerrow J.H. Tumour necrosis factor alpha restores granulomas and induces parasite egg-laying in schistosome-infected SCID mice. Nature 356 (1992) 604-607
5. Awadalla H.N., Sherif A.F., Shafel A.Z., Khalil H.A., and Guirgis F.K. Enzyme lipids in homogenates of liver from mice infected with S. mansoni and from uninfected mice. Int. J. Parasitol. 5 (1975) 27-31
6. Baykal-Erkilic A., Erkilic E., Erkilic M., and Özden T. The effect of streptozotocin-induced diabetes on renal plasma flow. Exp. Clin. Endocrinol. 103 (1995) 367-372
7. Bergmeyer H.U., Scheibe P., and Wahlefeld A.W. Optimization of methods for aspartate aminotransferase and alanine aminotransferase. Clin. Chem. 24 (1978) 58-73
8. Boros D.L., and Warren K.S. Delayed hypersensitivity-type granuloma formation and dermal reaction induced and elicited by a soluble factor isolated from Schistosoma mansoni eggs. J. Exp. Med. 132 (1970) 488-507
9. Bruce J.I., and Radke M.G. Culturing Biomphalaria and Oncomelania (Gastropoda) for large-scale studies of schistosomiasis: I. Cultivation of Biomphalaria glabrata and maintenance of Schistosoma mansoni in the laboratory. Bio-med. Rep. 406th Med. Lab. 19 (1971) 1-84
10. Brunet L.R., Dunne D.W., and Pearce E.J. Cytokine interaction and immune responses during Schistosoma mansoni infection. Parasitol. Today 14 (1998) 422-427
11. Chan D.W., and Sell S. Tumour markers. In: Burtis C.A., Ashwood E.R., and Aldrich J.E. (Eds). Tietz Fundamentals of Clinical Chemistry (1996), W.B. Saunders Company, Philadelphia 336-350
12. Chatterjee S., Mbaye A., De Man J.G., and Van Marck E.A.E. Does the neuropeptide somatostatin have therapeutic potential against schistosomiasis?. Trends Parasitol. 18 (2002) 295-298
13. Chatterjee S., Mbaye A., Alfidja A.T., Weyler J., Scott J.T., Van Damme P., Van De Vijver K., Deelder A., and Van Marck E.A.E. Circulating levels of the neuropeptide hormone somatostatin may determine hepatic fibrosis in Schistosoma mansoni infections. Acta Tropica 90 (2004) 191-203
14. Cheever A.W. Condition affecting the accuracy of potassium hydroxide digestion techniques for counting Schistosoma mansoni eggs in tissues. Bull. WHO 39 (1968) 311-328
15. Cheever A.W., and Deb S. Persistence of hepatic fibrosis and tissue eggs following treatment of Schistosoma japonicum infected mice. Am. J. Trop. Med. Hyg. 40 (1989) 620-628
16. Cheever A.W., Williams M.E., Wynn T.A., Finkelman F.D., Seder R.A., Cox T.M., Hieny S., Caspar P., and Sher A. Anti-IL-4 treatment of Schistosoma mansoni-infected mice inhibits development of T cells and non-B, non-T cells expressing Th2 cytokines while decreasing egg-induced hepatic fibrosis. J. Immunol. 153 (1994) 753-759
17. Cheever A.W., Finkelman F.D., and Cox T.M. Anti-interleukin-4 treatment diminishes secretion of Th2 cytokines and inhibits hepatic fibrosis in murine schistosomiasis japonica. Parasite Immunol. 17 (1995) 103-109
18. Chen D.S., Sung J.L., Sheu J.C., Lai M.Y., How S.W., Hsu H.C., Lee C.S., and Wei T.C. Serum α-fetoprotein in the early stage of human hepatocellular carcinoma. Gastroenterology 86 (1984) 1404-1409
19. Chesney J., Metz C., Stavitsky A.B., Bacher M., and Bucala R. Regulation production of type I collagen and inflammatory cytokines by peripheral blood fibrocytes. J. Immunol. 160 (1998) 419-425
20. Chitsulo L., Engels A., and Mostreson L.S. The global status of schistosomiasis and its control. Acta Tropica 22 (2000) 41-51
21. Chorny A., Gonzalez-Rey E., Fernandez-Martin A., Pozo D., Ganea D., and Delgado M. Vasoactive intestinal peptide induces regulatory dendritic cells with therapeutic effects on autoimmune disorders. Proc. Natl. Acad. Sci. USA 102 (2005) 13562-13567
22. Czaja M.J., Weiner F.R., Takahashi S., Giambrone M.A., van der Meide P.H., Schellekens H., Biempica L., and Zern M.A. Gamma-interferon treatment inhibits collagen deposition in murine schistosomiasis. Hepatology 10 (1989) 795-800
23. De la Fuente M., Delgado M., Del Río M., Garrido E., Leceta J., Hernanz A., and Gomariz R.P. Vasoactive intestinal peptide modulation of adherence and mobility in rat peritoneal lymphocytes and macrophages. Peptides 15 (1994) 1157-1163
24. Delgado M., and Ganea D. Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide inhibit interleukin-12 transcription by regulating nuclear factor B and Ets activation. J. Biol. Chem. 274 (1999) 31930-31940
25. Delgado M., and Ganea D. Cutting edge: is vasoactive intestinal peptide a type 2 cytokine. J. Immunol. 166 (2001) 2907-2912
26. Delgado M., De la Fuente M., Martinez C., and Gomariz R.P. Pituitary adenylate cyclase-activating polypeptides (PACAP27 and PACAP38) inhibit the mobility of murine thymocytes and splenic lymphocytes: comparison with VIP and implication of cAMP. J. Neuroimmunol. 62 (1995) 137-146
27. Delgado M., Munoz-Elias E.J., Kan Y., Gozes I., Fridkini M., Brenneman D.E., Gomariz R.P., and Ganea D. Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide inhibit tumor necrosis factor-α transcriptional activation by regulating nuclear factor-κB and cAMP response element-binding protein/c-Jun. J. Biol. Chem. 273 (1998) 31427-31436
28. Delgado M., Munoz-Elias E.J., Gomariz R.P., and 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. 162 (1999) 1707-1716
29. Delgado M., Martinez C., Pozo D., Calvo J.R., Leceta J., Ganea D., and Gomariz R.P. VIP and PACAP protect mice from lethal endotoxemia through the inhibition of TNF-α and IL-6. J. Immunol. 162 (1999) 1200-1205
30. Delgado M., Pozo D., Martinez C., Leceta J., Calvo J.R., Ganea D., and Gomariz R.P. Vasoactive intestinal peptide and pituitary adenylate cyclase activating polypeptide inhibit endotoxin-induced TNF-α production by macrophages: in vitro and in vivo studies. J. Immunol. 162 (1999) 2358-2367
31. Delgado M., Leceta J., Sun W., Gomariz R.P., and Ganea D. VIP and PACAP induce shift to a Th2 response by upregulating B7.2 expression. Ann. NY Acad. Sci. 921 (2000) 68-78
32. Delgado M., Abad C., Martinez C., Juarranz M.G., Arranz A., Gomariz R.P., and Leceta J. Vasoactive intestinal peptide in the immune system: potential therapeutic role in inflammatory and autoimmune diseases. J. Mol. Med. 80 (2002) 16-24
33. Delgado M., Pozo D., and Ganea D. The significance of vasoactive intestinal peptide in immunomodulation. Pharmacol. Rev. 56 (2004) 249-290
34. Delgado M., Chorny A., Gonzalez-Rey E., and Ganea D. Vasoactive intestinal peptide generates CD4+CD25+ regulatory T cells in vivo. J. Leukoc. Biol. 78 (2005) 1327-1338
35. dos Santos A.F., de Azevedo D.P., Mata R.S., de Mendonça D.D., and Sant'Ana A.E.G. The lethality of Euphorbia conspicua to adults of Biomphalaria glabrata, cercaria of Schistosoma mansoni and larvae of Artemia salina. Bioresour. Technol. 98 (2007) 135-139
36. Duvall R.H., and DeWitt W.B. An improved perfusion technique for recovering adult schistosomes from laboratory animals. Am. J. Trop. Med. Hyg. 16 (1967) 483-486
37. Frebourg T., Bercoff E., Manchon N., Senant J., Basuyau J.P., Breton P., Janvresse A., Brunelle P., and Bourreille J. The evaluation of CA 19.9 in the early detection of pancreatic cancer. Cancer 62 (1988) 2287-2290
38. Flores-Villanueva P.O., Zheng X.X., Strom T.B., and Stadecker M.J. Recombinant IL-10 and -10/Fc treatment down regulate egg antigen-specific delayed hypersensitivity reaction and egg granuloma formation in schistosomiasis. J. Immunol. 156 (1996) 3315-3320
39. Fouad M., and Khallaf E. CA 19.9 in carcinoma of the bilharzial bladder. J. R. Coll. Surg. Edinb. 39 (1994) 246-248
40. Gomariz R.P., Leceta J., Garrido E., Garrido T., and Delgado M. Vasoactive intestinal peptide (VIP) mRNA expression in rat T and B lymphocytes. Regul. Pept. 50 (1994) 177-184
41. Gomariz R., Leceta J., Martinez C., Abad C., Ganea D., and Delgado M. Anti-inflammatory actions of VIP/PACAP. Role in endotoxemia. Ann. NY Acad. Sci. 921 (2000) 284-288
42. Grimm M.C., Newman R., Hassim Z., Cuan N., Connor S.J., Le Y., Wang J.M., Oppenheim J.J., and Lloyd A.R. Cutting edge: vasoactive intestinal peptide acts as a potent suppressor of inflammation in vivo by trans-deactivating chemokine receptors. J. Immunol. 171 (2003) 4990-4994
43. Hesse M., Piccirillo C.A., Belkaid Y., Prufer J., Mentink-Kane M., Leusink M., Cheever A.W., Shevach E.M., and Wynn T.A. The pathogenesis of schistosomiasis is controlled by cooperating IL-10-producing innate effectors and regulatory T cells. J. Immunol. 172 (2004) 3157-3166
44. Joseph A.L., and Boros D.L. Tumor necrosis factor plays a role in Schistosoma mansoni egg-induced granulomatous inflammation. J. Immunol. 151 (1993) 5461-5471
45. Karlsson S., and Ahren B. Peptide receptor antagonists in the study of insulin and glucagons secretion in mice. Eur. J. Pharmacol. 191 (1990) 457-464
46. Kaviratne M., Hesse M., Leusink M., Cheever A.W., Davies S.J., McKerrow J.H., Wakefield L.M., Letterio J.J., and Wynn T.A. IL-13 activates a mechanism of tissue fibrosis that is completely TGF-β independent. J. Immunol. 173 (2004) 4020-4029
47. Kimata H. Vasoactive intestinal peptide differentially modulates human immunoglobulin production. Adv. Neuroimmunol. 6 (1996) 107-115
48. Leceta J., Martinez C., Delgado M., Garrido E., and Gomariz R.P. Expression of vasoactive intestinal peptide in lymphocytes: a possible endogenous role in the regulation of the immune system. Adv. Neuroimmunol. 6 (1996) 29-36
49. Lichtenberg F.V. The host response to eggs of Schistosoma mansoni: I. Granuloma formation in the unsensitized laboratory mouse. Am. J. Pathol. 41 (1962) 711-719
50. Mahmoud A.A.F., and Warren K.S. Anti-inflammatory effects of tarteremetic and niridazole suppression of schistosoma egg granuloma. J. Immunol. 112 (1974) 222-228
51. Mahmoud M.R., El-Abhar H.S., and Saleh S. The effect of Nigella sativa oil against the liver damage induced by S. mansoni infection in mice. J. Ethnopharmacol. 79 (2002) 1-11
52. Mansour M.M., Farid Z., Bassily S., Salah L.H., and Watten R.H. Serum enzyme tests in hepatosplenic schistosomiasis. Trans. R. Soc. Trop. Med. Hyg. 76 (1982) 109-112
53. Martinez C., Delgado M., Abad C., Gomariz R.P., Ganea D., and Leceta J. Regulation of VIP production and secretion by murine lymphocytes. J. Neuroimmunol. 93 (1999) 126-138
54. Mathew R.C., Cook G.A., Blum A.M., Metwali A., Felman R., and Weinstock J.V. Vasoactive intestinal peptide stimulates T lymphocytes to release IL-5 in murine schistosomiasis mansoni infection. J. Immunol. 148 (1992) 3572-3577
55. McKee A.S., and Pearce E.J. CD25+CD4+ cells contribute to Th2 polarization during helminth infection by suppressing Th1 response development. J. Immunol. 173 (2004) 1224-1231
56. Metwali A., Blum A., Mathew R., Sandor M., Lynch R.G., and Weinstock J.V. Modulation of T lymphocyte proliferation in mice infected with Schistosoma mansoni: VIP suppresses mitogen- and antigen-induced T cell proliferation possibly by inhibiting IL-2 production. Cell. Immunol. 149 (1993) 11-23
57. Metwali A., Elliott D., Blum A.M., Li J., Sandor M., Lynch R., Noben-Trauth N., and Weinstock J.V. The granulomatous response in murine schistosomiasis mansoni does not switch to Th1 in IL-4-deficient C57BL/6 mice. J. Immunol. 157 (1996) 4546-4553
58. Neuman R.E., and Logan M.A. The determination of collagen and elastin in tissues. J. Biol. Chem. 186 (1950) 549-556
59. Neuman R.E., and Logan M.A. The determination of hydroxyproline. J. Biol. Chem. 184 (1950) 299-300
60. Noeman S.A., Sharada K., el Dardiry S., Rahim A.A., and Zaky Y. Significance of tumour markers in colorectal carcinoma associated with schistosomiasis. Bangladesh Med. Res. Counc. Bull. 20 (1994) 12-20
61. Osman A., Allam G., and Saad A.-H. In vivo modulation of granuloma formation in mice infected with Schistosoma mansoni after treatment with vasoactive intestinal peptide (VIP). J. Egypt. Ger. Soc. Zool. 23 (1997) 113-135
62. PC-STAT, 1985. One-way analysis of variance. Version 1A (C) copyright. The University of Georgia. Programs coded by Rao, M., Blane, K. and Zonneberg, M. University of Georgia, USA.
63. Pozo D., and Delgado M. The many faces of VIP in neuroimmunology: a cytokine rather a neuropeptide?. FASEB J. 18 (2004) 1325-1334
64. Pozo D., Delgado M., Martínez C., Guerrero J.M., Leceta J., Gomariz R.P., and Calvo J.R. Immunobiology of vasoactive intestinal peptide (VIP). Immunol. Today 21 (2000) 7-11
65. Reinke E., and Fabry Z. Breaking or making immunological privilege in the central nervous system: the regulation of immunity by neuropeptides. Immunol. Lett. 104 (2006) 102-109
66. Ritter D., and McKerrow J. Intercellular adhesion molecule 1 is the major adhesion molecule expressed during schistosome granuloma formation. Infect. Immun. 64 (1996) 4706-4713
67. Said S. VIP as a modulator of lung inflammation and airway constriction. Am. Rev. Respir. Dis. 143 (1991) 22-24
68. Schubert M. Conditions for drug testing in experimental Schistosomiasis mansoni in mice. Am. J. Trop. Med. 28 (1948) 121-136
69. Schuppan D. Structure of the extracellular matrix in normal and fibrotic liver: collagens and glycoproteins. Semin. Liver Dis. 10 (1990) 1-10
70. Sirianni M.C., Annibale B., Tagliaferri F., Fais S., DeLuca S., Pallone F., Delle Fave G., and Aiiuti F. Modulation of human natural killer activity by vasoactive intestinal peptide (VIP) family, VIP, glucagon and GHRF specifically inhibit NK activity. Regul. Pept. 38 (1992) 79-87
71. Sher A., Coffman R.L., Hieny S., Scott P., and Cheever A.W. Interleukin 5 is required for the blood and tissue eosinophilia but not granuloma formation induced by infection with Schistosoma mansoni. Proc. Natl. Acad. Sci. USA 87 (1990) 61-65
72. Stanisz A.M., Befus D., and Bienenstock J. Differential effects of vasoactive intestinal peptide, substance P, and somatostatin on immunoglobulin synthesis and proliferations by lymphocytes from Peyer's patches, mesenteric lymph nodes, and spleen. J. Immunol. 136 (1986) 152-156
73. Stavitsky A.B. Regulation of granulomatous inflammation in experimental models of schistosomiasis. Infect. Immun. 72 (2004) 1-12
74. Stirewalt M.A., and Bronson J.F. Description of plastic mouse restraining case. J. Parasitol. 41 (1955) 328-334
75. Sun L., and Ganea D. Vasoative intestinal peptide inhibits interleukin (IL)-2 and IL-4 production through different molecular mechanisms in T cells activated via the T cell receptor/CD3 complex. J. Neuroimmunol. 48 (1993) 59-70
76. Sun W., Tadmori I., Yang L., Delgado M., and Ganea D. Vasoactive intestinal peptide (VIP) inhibits TGF-β1 production in murine macrophages. J. Neuroimmunol. 107 (2000) 88-99
77. Tang H., Welton A., and Ganea D. Neuropeptide regulation of cytokine expression. Effects of VIP and Ro25-1553. J. Interferon Cytokine Res. 15 (1995) 993-1003
78. Tuncel N., Töre F., Ahintürk V., Ak D., and Tuncel M. Vasoactive intestinal peptide inhibits degranulation and changes granular content of mast cells: a potential therapeutic strategy in controlling septic shock. Peptides 21 (2000) 81-89
79. Vassiliou E., Jiang X., Delgado M., and Ganea D. TH2 lymphocytes secrete functional VIP upon antigen stimulation. Arch. Physiol. Biochem. 109 (2001) 365-368
80. Voice J.K., Dorsam G., Chan R.C., Grinninger C., Kong Y., and Goetzl E.J. Immunoeffector and immunoregulatory activities of vasoactive intestinal peptide. Regul. Pept. 109 (2002) 199-208
81. Waldmann T.A., and McIntire K.R. The use of radioimmunoassay for alpha-fetoprotein in the diagnosis of malignancy. Cancer 34 (1974) 1505-1510
82. Wang H.Y., Jiang X., Gozes I., Fridkin M., Brenneman D.E., and Ganea D. Vasoactive intestinal peptide inhibits cytokine production in T lymphocytes through cAMP-dependent and cAMP-independent mechanisms. Regul. Pept. 84 (1999) 55-67
83. Warren K.S. The secret of the immunopathogenesis of Schistosomiasis: in vivo models. Immunol. Rev. 61 (1982) 189-213
84. Weinstock J.V. Vasoactive intestinal peptide regulation of granulomatous inflammation in murine Schistosomiasis mansoni. Adv. Neuroimmunol. 6 (1996) 95-105
85. Weinstock J.V., and Blum A.M. Detection of vasoactive intestinal peptide and localization of its mRNA within granulomas of murine schistosomiasis. Cell. Immunol. 125 (1990) 291-300
86. Weinstock J.V., Blum A.M., and Khetarpal S. Granulomas in murine schistosomiasis mansoni contain vasoactive intestinal peptide-responsive lymphocytes. Cell. Immunol. 134 (1991) 458-472
87. Wepsic H.T. Alpha-fetoprotein: its quantitation and relationship to neoplastic disease. In: Krikpatrik A.M., and Nakamura R.M. (Eds). Alpha-Fetoprotein: Laboratory Procedures and Clinical Applications (1981), Masson Publishing, New York 115-129
88. WHO Expert Committee. The control of schistosomiasis. WHO Tech. Rep. Ser. 830 (1993) 1-86
89. Wyler D.L. Fibrosin, a novel fibrogenic protein: discovery, cloning and implications for fibrotic disorders. Int. Arch. Allergy Immunol. 111 (1996) 326-329
90. Wynn T.A., Eltoum I., Cheever A.W., Lewis F.A., Gause W.C., and Sher A. Analysis of cytokine mRNA expression during primary granuloma formation induced by eggs of Schistosoma mansoni. J. Immunol. 151 (1993) 1430-1440
91. Wynn T.A., Cheever A.W., Williams M.E., Hieny S., Caspar P., Kühn R., Müller W., and Sher A. IL-10 regulates liver pathology in acute murine Schistosomiasis mansoni but is not required for immune down-modulation of chronic disease. J. Immunol. 160 (1998) 4473-4480
92. Xin Z., and Sriram S. Vasoactive intestinal peptide inhibits IL-12 and nitric oxide production in murine macrophages. J. Neuroimmunol. 89 (1998) 206-212