The neuropeptide calcitonin gene-related peptide (CGRP) prevents inflammatory liver injury in mice

Journal of Hepatology

Volumn 51, Issue 2, 2009, Pages 342-353

  Kroeger, Irena ^a,b   Erhardt, Annette ^b   Abt, Dominik ^a   Fischer, Michael ^a   Biburger, Markus ^c   Rau, Thomas ^b   Neuhuber, Winfried L ^a   Tiegs, Gisa ^b  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^c UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

Calcitonin gene related peptide; Inducible cAMP early repressor; Interleukin 10; Liver inflammation; TNF

Indexed keywords

ALPHA CALCITONIN GENE RELATED PEPTIDE; AMINOTRANSFERASE; CALCITONIN GENE RELATED PEPTIDE RECEPTOR; CYTOKINE; GALACTOSAMINE; INTERLEUKIN 10; LIPOPOLYSACCHARIDE; OLCEGEPANT; TUMOR NECROSIS FACTOR ALPHA;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DRUG MECHANISM; ENZYME ACTIVITY; HUMAN; HUMAN TISSUE; ICER GENE; IMMUNOCOMPETENT CELL; INFLAMMATION; LIVER CELL; LIVER FAILURE; LIVER INJURY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPRESSOR GENE;

ADULT; AGED; ANIMALS; BASE SEQUENCE; CALCITONIN GENE-RELATED PEPTIDE; CYTOKINES; DNA PRIMERS; FEMALE; GALACTOSAMINE; HEPATITIS; HUMANS; IMMUNIZATION; INFLAMMATION MEDIATORS; INTERLEUKIN-10; LIPOPOLYSACCHARIDES; LIVER; MALE; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; MIDDLE AGED; RECEPTORS, CALCITONIN GENE-RELATED PEPTIDE; RNA, MESSENGER; TUMOR NECROSIS FACTOR-ALPHA;

EID: 67649173064     PISSN: 01688278     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jhep.2009.03.022     Document Type: Article

References (63)

1. Steinman L. Elaborate interactions between the immune and nervous systems. Nat Immunol 5 (2004) 575-581
2. Holzer P., and Holzer-Petsche U. Tachykinins in the gut. Part II. Roles in neural excitation, secretion and inflammation. Pharmacol Ther 73 (1997) 219-263
3. Reinshagen M., Flämig G., Ernst S., Geerling I., Wong H., Walsh J.H., et al. Calcitonin gene-related peptide mediates the protective effect of sensory nerves in a model of colonic injury. J Pharmacol Exp Ther 286 (1998) 657-661
4. Van Nassauw L., Adriaensen D., and Timmermans J P. The bidirectional communication between neurons and mast cells within the gastrointestinal tract. Auton Neurosci 133 (2007) 91-103
5. Yoneda M., Sato Y., Nakamura K., Yokohama S., Kono T., Watanobe H., et al. Involvement of calcitonin gene-related peptide and capsaicin-sensitive afferents in central thyrotropin-releasing hormone-induced hepatic cytoprotection. Eur J Pharmacol 478 (2003) 173-177
6. Casini A., Lippe I., Evangelista S., Geppetti P., Santicioli P., Urso C., et al. Effect of sensory denervation with capsaicin on liver fibrosis induced by common bile duct ligation in rat. J Hepatol 11 (1990) 302-312
7. Tiegs G., Hentschel J., and Wendel A. A T cell-dependent experimental liver injury in mice inducible by concanavalin A. J Clin Invest 90 (1992) 196-203
8. Gantner F., Leist M., Jilg S., Germann P.G., Freudenberg M.A., and Tiegs G. Tumor necrosis factor-induced hepatic DNA fragmentation as an early marker of T cell-dependent liver injury in mice. Gastroenterology 109 (1995) 166-176
9. Schümann J., and Tiegs G. Pathophysiological mechanisms of TNF during intoxication with natural or man-made toxins. Toxicology 138 (1999) 103-126
10. Nagata S. Apoptosis by death factor. Cell 88 (1997) 355-365
11. Neuhuber W.L., and Tiegs G. Innervation of immune cells: evidence for neuroimmunomodulation in the liver. Anat Rec A Discov Mol Cell Evol Biol 280A (2004) 884-892
12. Bang R., Sass G., Kiemer A.K., Vollmar A.M., Neuhuber W.L., and Tiegs G. Neurokinin-1 receptor antagonists CP-96,345 and L-733,060 protect mice from cytokine-mediated liver injury. J Pharmacol Exp Ther 305 (2003) 31-39
13. Bang R., Biburger M., Neuhuber W.L., and Tiegs G. Neurokinin-1 receptor antagonists protect mice from cd95- and tumor necrosis factor-mediated apoptotic liver damage. JPET 308 (2004) 1174-1180
14. Schäfer M, Stein C. Mind over matter: regulation of peripheral inflammation by the CNS. In: Schäfer M, Stein C, editors. In: Parnham Mj, series editor. Basel-Boston-Berlin: Birkhauser Verlag; 2003, IX.
15. Tiegs G., Bang R., and Neuhuber W L. Requirement of peptidergic sensory innervation for disease activity in murine models of immune hepatitis and protection by beta-adrenergic stimulation. J Neuroimmunol 96 (1999) 131-143
16. Amara S.G., Jonas V., Rosenfeld M.G., Ong E.S., and Evans R.M. Alternative RNA processing in calcitonin gene expression generates mRNAs encoding different polypeptide products. Nature 298 (1982) 240-244
17. Rosenfeld M.G., Mermod J.J., Amara S.G., Swanson L.W., Sawchenko P.E., Rivier J., et al. Production of a novel neuropeptide encoded by the calcitonin gene via tissue-specific RNA processing. Nature 304 (1983) 129-135
18. Poyner D.R., Sexton P.M., Marshall I., Smith D.M., Quirion R., Born W., et al. International Union of Pharmacology. XXXII. The mammalian calcitonin gene-related peptides, adrenomedullin, amylin, and calcitonin receptors. Pharmacol Rev 54 (2002) 5233-5402
19. Prado M.A., Evans-Bain B., and Dickerson I.M. Receptor component protein (RCP): a member of a multi-protein complex required for G-protein-coupled signal transduction. Biochem Soc Trans 30 (2002) 460-464
20. Evans B.N., Rosenblatt M.I., Mnayer L.O., Oliver K.R., and Dickerson I.M. CGRP-RCP, a novel protein required for signal transduction at calcitonin gene-related peptide and adrenomedullin receptors. J Biol Chem 275 (2000) 31438-31443
21. van Rossum D., Hanisch U.K., and Quirion R. Neuroanatomical localization, pharmacological characterization and functions of CGRP, related peptides and their receptors. Neurosci Biobehav Rev 21 (1997) 649-678
22. Brain S.D., and Cambridge H. Calcitonin gene-related peptide: vasoactive effects and potential therapeutic role. Gen Pharmacol 27 (1996) 607-611
23. Wimalawansa S.J. Amylin, calcitonin gene-related peptide, calcitonin, and adrenomedullin: a peptide superfamily. Crit Rev Neurobiol 11 (1997) 167-239
24. Schwenger N., Dux M., de Col R., Carr R., and Messlinger K. Interaction of calcitonin gene-related peptide, nitric oxide and histamine release in neurogenic blood flow and afferent activation in the rat cranial dura mater. Cephalalgia 27 (2007) 481-491
25. Holzer P. Implications of tachykinins and calcitonin gene-related peptide in inflammatory bowel disease. Digestion 59 (1988) 269-283
26. Fernandez S., Knopf M.A., Shankar G., and McGillis J.P. Calcitonin gene-related peptide indirectly inhibits IL-7 responses in pre-B cells by induction of IL-6 and TNF-alpha in bone marrow. Cell Immunol 226 (2003) 67-77
27. Tang Y., Feng Y., and Wang X. Calcitonin gene-related peptide potentiates LPS-induced IL-6 release from mouse peritoneal macrophages. J Neuroimmunol 84 (1998) 207-212
28. Ahmed A.A., Mutt V., and Nordlind K. Modulating effects of sensory and autonomic neuropeptides on murine splenocyte proliferation and cytokine secretion induced by Leishmania major. Immunopharmacol Immunotoxicol 21 (1999) 507-526
29. Millet I., Phillips R.J., Sherwin R.S., Ghosh S., Voll R., Flavell R.A., et al. Inhibition of NF-kappaB activity and enhancement of apoptosis by the neuropeptide calcitonin gene-related peptide. J Biol Chem 275 (2000) 15114-15121
30. Harzenetter M.D., Novotny A.R., Gais P., Molina C.A., Altmayr F., and Holzmann B. Negative regulation of TLR responses by the neuropeptide CGRP is mediated by the transcriptional repressor ICER. J Immunol 179 (2007) 607-615
31. Crossman D., McEwan J., MacDermot J., MacIntyre I., and Dollery C.T. Human calcitonin gene-related peptide activates adenylate cyclase and releases prostacyclin from human umbilical vein endothelial cells. Br J Pharmacol 92 (1987) 695-701
32. Jörres A., Dinter H., Topley N., Gahl G.M., Frei U., and Scholz P. Inhibition of tumour necrosis factor production in endotoxin-stimulated human mononuclear leukocytes by the prostacyclin analogue iloprost: cellular mechanisms. Cytokine 9 (1997) 119-125
33. Klebanoff S.J., Vadas M.A., Harlan J.M., Sparks L.H., Gamble J.R., Agosti J.M., et al. Stimulation of neutrophils by tumor necrosis factor. J Immunol 136 (1986) 4220-4225
34. Thiemermann C., Wu C.C., Szabó C., Perretti M., and Vane J.R. Role of tumour necrosis factor in the induction of nitric oxide synthase in a rat model of endotoxin shock. Br J Pharmacol 110 (1993) 177-182
35. Reinshagen M., Rohm H., Steinkamp M., Lieb K., Geerling I., Von Herbay A., et al. Protective role of neurotrophins in experimental inflammation of the rat gut. Gastroenterology 119 (2000) 368-376
36. Gomes R.N., Castro-Faria-Neto H.C., Bozza P.T., Soares M.B., Shoemaker C.B., David J.R., et al. Calcitonin gene-related peptide inhibits local acute inflammation and protects mice against lethal endotoxemia. Shock 24 (2005) 590-594
37. Gonzalez-Rey E., Chorny A., Varela N., Robledo G., and Delgado M. Urocortin and adrenomedullin prevent lethal endotoxemia by down-regulating the inflammatory response. Am J Pathol 168 (2006) 1921-1930
38. Kamiyoshi A., Sakurai T., Ichikawa-Shindo Y., Fukuchi J., Kawate H., Muto S., et al. Endogenous alphaCGRP protects against concanavalin A-induced hepatitis in mice. Biochem Biophys Res Commun 343 (2006) 152-158
39. Leist M., Gantner F., Jilg S., and Wendel A. Activation of the 55 kDa TNF receptor is necessary and sufficient for TNF-induced liver failure, hepatocyte apoptosis, and nitrite release. J Immunol 154 (1995) 1307-1316
40. Josephs M.D., Bahjat F.R., Fukuzuka K., Ksontini R., Solorzano C.C., Edwards C.K., et al. Lipopolysaccharide and d-galactosamine-induced hepatic injury is mediated by TNF-alpha and not by Fas ligand. Am J Physiol Regul Integr Comp Physiol 278 (2000) R1196-R1201
41. Bracq S., Clement B., Pidoux E., Moukhtar M S., and Jullienne A. CGRP is expressed in primary cultures of human hepatocytes and in normal liver. FEBS Lett 351 (1994) 63-66
42. Yamaguchi A., Chiba T., Okimura Y., Yamatani T., Morishita T., Nakamura A., et al. Receptors for calcitonin gene-related peptide on the rat liver plasma membranes. Biochem Biophys Res Commun 152 (1988) 383-391
43. Stangl D., Muff R., Schmolck C., and Fischer J.A. Photoaffinity labeling of rat calcitonin gene-related peptide receptors and adenylate cyclase activation: identification of receptor subtypes. Endocrinology 132 (1993) 744-750
44. Kuhn R., Lohler J., Rennick D., Rajewsky K., and Muller W. Interleukin-10-deficient mice develop chronic enterocolitis. Cell 75 (1993) 263-274
45. Averbeck B., and Reeh P.W. Interactions of inflammatory mediators stimulating release of calcitonin gene-related peptide, substance P and prostaglandin E(2) from isolated rat skin. Neuropharmacology 40 (2001) 416-423
46. Biburger M., and Tiegs G. Alpha-galactosylceramide-induced liver injury in mice is mediated by TNF-alpha but independent of Kupffer cells. J Immunol 175 (2005) 1540-1550
47. Uzan B., de Vernejoul M.C., and Cressent M. RAMPs and CRLR expressions in osteoblastic cells after dexamethasone treatment. Biochem Biophys Res Commun 321 (2004) 802-808
48. Seglen P.O. Preparation of rat liver cells. 3. Enzymatic requirements for tissue dispersion. Exp Cell Res 82 (1973) 391-398
49. Morini S., Carotti S., Carpino G., Franchitto A., Corradini S.G., Merli M., et al. GFAP expression in the liver as an early marker of stellate cells activation. Ital J Anat Embryol 110 (2005) 193-207
50. Sass G., Heinlein S., Agli A., Bang R., Schümann J., and Tiegs G. Cytokine expression in three mouse models of experimental hepatitis. Cytokine 19 (2002) 115-120
51. Gantner F., Kusters S., Wendel A., Hatzelmann A., Schudt C., and Tiegs G. Protection from T cell-mediated murine liver failure by phosphodiesterase inhibitors. J Pharmacol Exp Ther 280 (1997) 53-60
52. Cuesta M.C., Quintero L., Pons H., and Suarez-Roca H. Substance P and calcitonin gene-related peptide increase IL-1 beta, IL-6 and TNF alpha secretion from human peripheral blood mononuclear cells. Neurochem Int 40 (2002) 301-306
53. Aoki-Nagase T., Nagase T., Oh-Hashi Y., Kurihara Y., Yamaguchi Y., Yamamoto H., et al. Calcitonin gene-related peptide mediates acid-induced lung injury in mice. Respirology 12 (2007) 807-813
54. Springer J., Geppetti P., Fischer A., and Groneberg D.A. Calcitonin gene-related peptide as inflammatory mediator. Pulm Pharmacol Ther 16 (2003) 121-130
55. Schümann J., Wolf D., Pahl A., Brune K., Papadopoulos T., van Rooijen N., et al. Importance of Kupffer cells for T-cell-dependent liver injury in mice. Am J Pathol 157 (2000) 1671-1683
56. Doods H., Arndt K., Rudolf K., and Just S. CGRP antagonists: unravelling the role of CGRP in migraine. Trends Pharmacol Sci 28 (2007) 580-587
57. Lee W.I., Xu Y., Fung S.M., and Fung H.L. eNOS-dependent vascular interaction between nitric oxide and calcitonin gene-related peptide in mice: gender selectivity and effects on blood aggregation. Regul Pept 110 (2003) 115-122
58. Wu D., Doods H., Arndt K., and Schindler M. Development and potential of non-peptide antagonists for calcitonin-gene-related peptide (CGRP) receptors: evidence for CGRP receptor heterogeneity. Biochem Soc Trans 30 (2002) 468-473
59. Hughes S.R., and Brain S.D. A calcitonin gene-related peptide (CGRP) antagonist (CGRP8-37) inhibits microvascular responses induced by CGRP and capsaicin in skin. Br J Pharmacol 104 (1991) 738-742
60. Petersen K.A., Birk S., Lesko L., and Olesen J. BIBN4096BS antagonizes human alpha-calcitonin gene related peptide-induced headache and extracerebral artery dilatation. Clin Pharmacol Ther 77 (2005) 202-213
61. Ma W., and Quirion R. Increased calcitonin gene-related peptide in neuroma and invading macrophages is involved in the up-regulation of interleukin-6 and thermal hyperalgesia in a rat model of mononeuropathy. J Neurochem 98 (2006) 180-192
62. Nagaki M., Tanaka M., Sugiyama A., Ohnishi H., and Moriwaki H. Interleukin-10 inhibits hepatic injury and tumor necrosis factor-alpha and interferon-gamma mRNA expression induced by staphylococcal enterotoxin B or lipopolysaccharide in galactosamine-sensitized mice. J Hepatol 31 (1999) 815-824
63. Seldon P.M., Barnes P.J., and Giembycz M.A. Interleukin-10 does not mediate the inhibitory effect of PDE-4 inhibitors and other cAMP-elevating drugs on lipopolysaccharide-induced tumors necrosis factor-alpha generation from human peripheral blood monocytes. Cell Biochem Biophys 29 (1998) 179-201