The PACAP-type I receptor agonist maxadilan from sand fly saliva protects mice against lethal endotoxemia by a mechanism partially dependent on IL-10

European Journal of Immunology

Volumn 28, Issue 10, 1998, Pages 3120-3127

  Bozza, Marcelo ^a,b   Soares, Milena B P ^a,b   Bozza, Patricia T ^b   Satoskar, Abhay R ^a   Diacovo, Thomas G ^c   Brombacher, Frank ^d   Titus, Richard G ^e   Shoemaker, Charles B ^a   David, John R ^a  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^b INSTITUTO OSWALDO CRUZ   (Brazil)

^c HARVARD MEDICAL SCHOOL   (United States)

^d MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

^e Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

Cytokine; LPS endotoxemia; Maxadilan; Neuropeptide; PACAP type 1 receptor

Indexed keywords

ADENYLATE CYCLASE; CYTOKINE; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE RECEPTOR; INTERLEUKIN 10; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MAXADILAN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ENDOTOXEMIA; FLY; INFLAMMATION; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SALIVA; VASODILATATION;

ANIMALS; ENDOTOXEMIA; GALACTOSAMINE; INSECT PROTEINS; INTERLEUKIN-10; INTERLEUKIN-6; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; NEUROPEPTIDES; PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE; PLATELET ACTIVATION; PSYCHODIDAE; RECEPTORS, PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE; RECEPTORS, PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE, TYPE I; RECEPTORS, PITUITARY HORMONE; SALIVARY PROTEINS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 0031660032     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1521-4141(199810)28:10<3120::AID-IMMU3120>3.0.CO;2-3     Document Type: Article

References (44)

1. Hewett, J. A. and Roth, R. A., Hepatic and extrahepatic pathobiology of bacterial lipopolysaccharides. Pharmacol. Rev. 1993. 45: 381-411.
2. Beutler, B., Milsark, I. W. and Cerami, A. C., Passive immunization against cachectin/tumor necrosis factor protects mice from the lethal effect of endotoxin. Science 1985. 229: 869-871.
3. Tracey, K. J., Beutler, B., Lowry, S. F., Merryweather, J., Wolpe, S., Milsark, I. W., Hariri, R. J., Fahey III, T. J., Zentella, A., Albert, J. D., Shires, G. T. and Cerami, A., Shock and tissue injury induced by recombinant human cachectin. Science 1986. 234: 470-474.
4. Lehman, V., Freudenberg, M. A. and Galanos, C., Lethal toxicity of lipopolysaccharide and tumor necrosis factor in normal and D-galactosamine-treated mice. J. Exp. Med. 1987. 165: 657-663.
5. Glauser, M. P., Zanetti, G., Baumgartener, J. D. and Cohen, J., Septic Shock: pathogenesis. Lancet 1991. 338: 732-736.
6. Ribeiro, J. M. R., Role of saliva in blood-feeding by arthropods. Annu. Rev. Entom. 1987. 32: 463-478.
7. Titus, R. G. and Ribeiro, J. M. C., Salivary gland lysates from the sand fly Lutzomyia longipalpis enhance Leishmania infectivity. Science 1988. 239: 1306-1308.
8. Titus, R. G. and Ribeiro, J. M. C., The role of vector saliva in transmission or arthropod-borne disease. Parasitol. Today 1990. 6: 157-160.
9. Theodos, C. M., Ribeiro, J. M. C. and Titus, R. G., Analysis of enhancing effect of sand fly saliva on Leishmania infection in mice. Infect. Immun. 1991. 59: 1592-1598.
10. Theodos, C. M. and Titus, R. G., Salivary gland material from the sand fly Lutzomyia longipalpis has an inhibitory effect on macrophage function in vitro. Parasite Immunol. 1993. 15: 481-487.
11. Hall, L. R. and Titus, R. G., Sand fly saliva selectively modulates macrophage functions that inhibit killing of Leishmania major and nitric oxide production. J. Immunol. 1995. 155: 3501-3506.
12. Lerner, E. A., Ribeiro, J. M. C., Nelson, R. J. and Lerner, M. R., Isolation of maxadilan, a potent vasodilatory peptide from the salivary glands of the sand fly Lutzomyia longipalpis. J. Biol. Chem. 1991. 266: 11234-11236.
13. Lerner, E. A. and Shoemaker, C. B., Maxadilan. Cloning and functional expression of the gene encoding this potent vasodilator peptide. J. Biol. Chem. 1992. 267: 1062-1066.
14. Grevelink, S. A., Osborne, J., Loscalzo, J. and Lerner, E. A., Vasorelaxant and second messenger effects of maxadilan. J. Pharmacol. Exp. Ther. 1995. 272: 33-37.
15. Moro, I. and Lerner, E. A., Maxadilan, the vasodilator peptide from sand flies, is a specific pituitary adenylate cyclase activating peptide type I receptor agonist. J. Biol. Chem. 1996. 272: 966-970.
16. Christophe, J., Type I receptor for PACAP (a neuropeptide even more important than VIP?). Biochem. Biophys. Acta 1993. 1154: 183-199.
17. Qureshi, A. A., Asahina, A., Ohnuma, M., Tajima, M., Granstein, R. D. and Lerner, E. A., Immunomodulatory properties of Maxadilan, the vasodilator peptide from sand fly salivary gland extracts. Am. J. Trop. Med. Hyg. 1996. 54: 665-671.
18. Soares, M. B. P., Titus, R. G., Shoemaker, C. B., David, J. R. and Bozza, M., The vasoactive peptide maxadilan from sand fly saliva inhibits TNF-α and induces IL-6 by mouse macrophages through interaction with the pituitary adenylate cyclase-activating polypeptide (PACAP) receptor. J. Immunol. 1998. 160: 1811-1816.
19. Galanos, C., Freudenberg, M. A. and Reutter, W., Galactosamine-induced sensitization of the lethal effects of endotoxin, Proc. Natl. Acad. Sci. USA 1979. 76: 5939-5943.
20. Van der Poll, T., Buller, H. R., ten Cate, H., Wortel, C. H., Bauer, K. A., van Deventer, S. J. H., Hack, C. E., Sauerwein, H. P., Rosenberg, R. D. and ten Cate, J. W., Activation of coagulation after administration of tumor necrosis factor to normal human subjects. N. Engl. J. Med. 1990. 322: 1622-1627.
21. Piquet, P. F., Vesin, C., Ryser, J. E., Senaldi, G., Grau, G. E. and Tacchini-Cottier, F., An effector role for platelets in systemic and local lipopolysaccaride-induced toxicity in mice, mediated by a CD11a- and CD54-dependent interactions with endothelium. Infect. Immun. 1993. 61: 4182-4187.
22. Nagakawa, J., Hishinuma, I., Hirota, K., Miyamoto, K., Yamanaka, T., Yamatsu, I. and Katayama, K., Protective effects of E3330, a novel quinone derivative, on galactosamine/tumor necrosis factor-a-induced hepatitis in mice. Eur. J. Pharmacol. 1992. 229: 63-67.
23. Libert, C., Brouckaert, P. and Fiers, W., Protection by a1-acid glycoprotein against tumor necrosis factor-induced lethality. J. Exp. Med. 1994. 180: 1571-1575.
24. Ribeiro, J. M. C., Rossignol, P. A. and Spielman, A., Blood-finding strategy of a capillary-feeding sandfly, Lutzomyia longipalpis. Comp. Biochem. Physiol. 1986. 83: 683-686.
25. Waage, A., Brandtzaeg, P., Halstensen, A., Kierulf, P. and Espevic, T., The complex pattern of cytokines in serum from patients with meninigococcal septic shock. Association between interleukin 6, interleukin 1 and fatal outcome. J. Exp. Med. 1989. 169: 333-338.
26. Brouckaert, P., Everaerdt, B. and Fiers, W., The glucocorticoid antagonist RU38486 mimics interleukin-1 in its sensitization to the lethal and interleukin-6-inducing properties of tumor necrosis factor. Eur. J. Immunol. 1992. 22: 981-986.
27. Fattori, E., Cappelletti, M., Costa, P., Sellitto, C., Cantoni, L., Carelli, M., Faggioni, R., Fantuzzi, G., Ghezzi, P. and Poli, V., Defective inflammatory response in interleukin 6 deficient mice. J. Exp. Med. 1994. 180: 1243-1250.
28. Xing, Z., Gauldie, J., Cox, G., Baumann, H., Jordana, M., Lei, X.-F. and Achong, M. K., IL-6 is an antiinflammatory cytokine required for controlling local or systemic acute inflammatory responses. J. Clin. Invest. 1998. 101: 311-320.
29. Aderka, D., Le, J. and Vilcek, J., IL-6 inhibits LPS-induced tumor necrosis factor production in cultured human monocytes, U937, and in mice. J. Immunol. 1989. 143: 3517-3523.
30. de Waal Malefyt, R., Abrams, J., Bennett, B., Figdor, C. and de Vries, J. E., Interleukin 10 (IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes. J. Exp. Med. 1991. 174: 1209-1220.
31. Bogdan, C., Vodovotz, Y. and Nathan, C. F., Macrophage deactivation by interleukin 10. J. Exp. Med. 1991. 174: 1549-1555.
32. Howard, M., Muchamuel, T., Andrade, S. and Menon, S., Interleukin 10 protects mice from lethal endotoxemia. J. Exp. Med. 1993. 177: 1205-1208.
33. Marchant, A., Deviere, J., Byl, B., de Groote, D., Vincent, J.-L. and Goldman, M., Interleukin-10 production during septicemia. Lancet 1994. 343: 707-708.
34. Kuhn, R., Lohler, J., Rennick, D., Rajewsky, K. and Muller, W., Interleukin-10-deficient mice develop chronic enterocolitis. Cell 1993. 75: 263-274.
35. Berg, D. J., Kuhn, R., Rajewsky, K., Muller, W., Menon, S., Davidson, N., Grunig, G. and Rennick, D., Interleukin-10 is a central regulator of the response to LPS in murine models of endotoxic shock and the Shwartzman reaction but not endotoxin tolerance. J. Clin. Invest. 1995. 96: 2339-2347.
36. Absood, A., Chen, D., Wang, Z.-Y. and Hakanson, R., Vascular effects of pituitary adenylate cyclase activating peptide: a comparison with vasoactive intestinal peptide. Regul. Pept. 1992. 40: 323-329.
37. Minkes, R. K., McMahon, T. J., Higuera, T. R., Murphy, W. A., Coy, D. H. and Kadowitz, P. J., Analysis of systemic and pulmonary vascular responses to PACAP and VIP: role of adrenal catecholamines. Am. J. Physiol. 1992. 263: H1659-1669.
38. Warren, J. B., Larkin, S. W., Coughhlan, M., Kajekar, R. and Willians, T. J., Pituitary adenylate cyclase activating polypeptide is a potent vasodilator and oedema potentiator in rabbit skin in vivo. Br. J. Pharmacol. 1992. 106: 331-334.
39. Arimura, A., Somogivari-Vigh, A., Miyata, A., Mizuo, K., Coy, D. H. and Kitada, C., Tissue distribution of PACAP as determined by RIA: highly abundant in the rat brain and testes. Endocrinology 1991. 129: 2787-2789.
40. Przywara, D. A., Guo, X., Angelilli, M. L., Wakade, T. D. and Wakade, A. R., A non-cholinergic transmitter, pituitary adenylate cyclase-activating polypeptide, utilizes a novel mechanism to evoke catecholamine secretion in rat adrenal chromaffin cells. J. Biol. Chem. 1996. 271: 10545-10550.
41. Severn, N., Rapson, N. T., Hunter, C. A. and Liew, F. Y., Regulation of tumor necrosis factor production by adrenaline and b-adrenergic agonists. J. Immunol. 1992. 148: 3441-3445.
42. Monastra, G. and Secchi, E. F., b-adrenergic receptors mediate in vivo the adrenaline inhibition of lipopolisaccharide-induced tumor necrosis factor release. Immunol. Lett. 1993. 38: 127-130.
43. van der Poll, T., Coyle, S. M., Barbosa, K., Braxton, C. C. and Lowry, S. F., Epinephrine inhibits tumor necrosis factor-a and potentiates interleukin 10 production during human endotoxemia. J. Clin. Invest. 1996. 97: 713-719.
44. Zhong, C., Skelly, P. J., Leaffer, D., Cohn, R. L., Caulfield, J. P. and Shoemaker, C. B., Immunolocalization of a Schistosoma mansoni facilitated glucose transporter to the basal, but not the apical membranes of the surface syncytium. Parasitology 1995. 110: 383-394.