IL-4 and IL-13 inhibit IL-1β and TNF-α induced kinin B 1 and B2 receptors through a STAT6-dependent mechanism

British Journal of Pharmacology

Volumn 169, Issue 2, 2013, Pages 400-412

  Souza, P P C ^a,b   Brechter, A B ^a   Reis, R I ^c   Costa, C A S ^b   Lundberg, P ^a   Lerner, U H ^a,d  

^a UMEÅ UNIVERSITY   (Sweden)

^b SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

^c FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^d UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

interleukin 1 ; interleukin 13; interleukin 4; kinin receptors; STAT6; tumour necrosis factor

Indexed keywords

ARGININE; BRADYKININ B1 RECEPTOR; BRADYKININ B2 RECEPTOR; BRADYKININ B2 RECEPTOR AGONIST; BRADYKININ DERIVATIVE; CALCIUM; INTERLEUKIN 13; INTERLEUKIN 1BETA; INTERLEUKIN 4; LYSINE; MESSENGER RNA; SMALL INTERFERING RNA; STAT6 PROTEIN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CALCIUM CELL LEVEL; CALVARIA; CELL STRAIN; CELL STRAIN MG 63; CONTROLLED STUDY; FIBROBLAST; GENE EXPRESSION; GINGIVA; HUMAN; HUMAN CELL; LIGAND BINDING; MOUSE; NONHUMAN; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RECEPTOR BINDING; RNA INTERFERENCE;

ANIMALS; CELL LINE; FIBROBLASTS; GENE KNOCKDOWN TECHNIQUES; GINGIVA; HUMANS; INTERLEUKIN-13; INTERLEUKIN-1BETA; INTERLEUKIN-4; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; OSTEOBLASTS; RECEPTOR, BRADYKININ B1; RECEPTOR, BRADYKININ B2; RNA; RNA, SMALL INTERFERING; STAT6 TRANSCRIPTION FACTOR; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84876901330     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.12116     Document Type: Article

References (51)

1. Andrews AL, Nordgren IK, Kirby I, Holloway JW, Holgate ST, Davies DE, et al. (2009). Cytoplasmic tail of IL-13Ralpha2 regulates IL-4 signal transduction. Biochem Soc Trans 37 (Pt 4): 873-876.
2. Bertram CM, Baltic S, Misso NL, Bhoola KD, Foster PS, Thompson PJ, et al. (2007). Expression of kinin B1 and B2 receptors in immature, monocyte-derived dendritic cells and bradykinin-mediated increase in intracellular Ca2+ and cell migration. J Leukoc Biol 81: 1445-1454.
3. Brechter AB, Lerner UH, (2002). Characterization of bradykinin receptors in a human osteoblastic cell line. Regul Pept 103: 39-51.
4. Brechter AB, Lerner UH, (2007). Bradykinin potentiates cytokine-induced prostaglandin biosynthesis in osteoblasts by enhanced expression of cyclooxygenase 2, resulting in increased RANKL expression. Arthritis Rheum 56: 910-923.
5. Brechter AB, Persson E, Lundgren I, Lerner UH, (2008). Kinin B1 and B2 receptor expression in osteoblasts and fibroblasts is enhanced by interleukin-1 and tumour necrosis factor-alpha. Effects dependent on activation of NF-kappaB and MAP kinases. Bone 43: 72-83.
6. Callard RE, Matthews DJ, Hibbert L, (1996). IL-4 and IL-13 receptors: are they one and the same? Immunol Today 17: 108-110.
7. Clover J, Gowen M, (1994). Are MG-63 and HOS TE85 human osteosarcoma cell lines representative models of the osteoblastic phenotype? Bone 15: 585-591.
8. Couture R, Harrisson M, Vianna RM, Cloutier F, (2001). Kinin receptors in pain and inflammation. Eur J Pharmacol 429: 161-176.
9. Cunha FQ, Poole S, Lorenzetti BB, Veiga FH, Ferreira SH, (1999). Cytokine-mediated inflammatory hyperalgesia limited by interleukin-4. Br J Pharmacol 126: 45-50.
10. David MD, Bertoglio J, Pierre J, (2003). Functional characterization of IL-13 receptor alpha2 gene promoter: a critical role of the transcription factor STAT6 for regulated expression. Oncogene 22: 3386-3394.
11. Fichtner-Feigl S, Strober W, Kawakami K, Puri RK, Kitani A, (2006). IL-13 signaling through the IL-13alpha2 receptor is involved in induction of TGF-beta1 production and fibrosis. Nat Med 12: 99-106.
12. Gordon S, Martinez FO, (2010). Alternative activation of macrophages: mechanism and functions. Immunity 32: 593-604.
13. Hart PH, Vitti GF, Burgess DR, Whitty GA, Piccoli DS, Hamilton JA, (1989). Potential antiinflammatory effects of interleukin 4: suppression of human monocyte tumor necrosis factor alpha, interleukin 1, and prostaglandin E2. Proc Natl Acad Sci U S A 86: 3803-3807.
14. Hart PH, Cooper RL, Finlay-Jones JJ, (1991). IL-4 suppresses IL-1 beta, TNF-alpha and PGE2 production by human peritoneal macrophages. Immunology 72: 344-349.
15. Hebenstreit D, Wirnsberger G, Horejs-Hoeck J, Duschl A, (2006). Signaling mechanisms, interaction partners, and target genes of STAT6. Cytokine Growth Factor Rev 17: 173-188.
16. Joosten LA, Lubberts E, Helsen MM, Saxne T, Coenen-de Roo CJ, Heinegard D, et al. (1999). Protection against cartilage and bone destruction by systemic interleukin-4 treatment in established murine type II collagen-induced arthritis. Arthritis Res 1: 81-91.
17. Kakoki M, Sullivan KA, Backus C, Hayes JM, Oh SS, Hua K, et al. (2010). Lack of both bradykinin B1 and B2 receptors enhances nephropathy, neuropathy, and bone mineral loss in Akita diabetic mice. Proc Natl Acad Sci U S A 107: 10190-10195.
18. Kelly-Welch AE, Hanson EM, Boothby MR, Keegan AD, (2003). Interleukin-4 and interleukin-13 signaling connections maps. Science 300: 1527-1528.
19. Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DG, (2010). NC3Rs Reporting Guidelines Working Group. Br J Pharmacol 160: 1577-1579.
20. Lawrence T, Natoli G, (2011). Transcriptional regulation of macrophage polarization: enabling diversity with identity. Nat Rev Immunol 11: 750-761.
21. Leeb-Lundberg LM, Marceau F, Muller-Esterl W, Pettibone DJ, Zuraw BL, (2005). International union of pharmacology. XLV. Classification of the kinin receptor family: from molecular mechanisms to pathophysiological consequences. Pharmacol Rev 57: 27-77.
22. Lerner U, Hänstrom L, (1987). Human gingival fibroblasts secrete non-dialyzable, prostanoid-independent products which stimulate bone resorption in vitro. J Periodontal Res 22: 284-289.
23. Lerner UH, (1991). Bradykinin synergistically potentiates interleukin-1 induced bone resorption and prostanoid biosynthesis in neonatal mouse calvarial bones. Biochem Biophys Res Commun 175: 775-783.
24. Lerner UH, (1997). The role of kallikrein-kinin system in inflammation-induced bone metabolism. In:, Farmer SG, (ed.). The Kinin System. Academic Press: New York, pp. 219-234.
25. Lerner UH, (2006). Inflammation-induced bone remodeling in periodontal disease and the influence of post-menopausal osteoporosis. J Dent Res 85: 596-607.
26. Lerner UH, Modeer T, (1991). Bradykinin B1 and B2 receptor agonists synergistically potentiate interleukin-1-induced prostaglandin biosynthesis in human gingival fibroblasts. Inflammation 15: 427-436.
27. Lerner UH, Jones IL, Gustafson GT, (1987). Bradykinin, a new potential mediator of inflammation-induced bone resorption. Studies of the effects on mouse calvarial bones and articular cartilage in vitro. Arthritis Rheum 30: 530-540.
28. Lerner UH, Ransjo M, Ljunggren O, (1989). Bradykinin stimulates production of prostaglandin E2 and prostacyclin in murine osteoblasts. Bone Miner 5: 139-154.
29. Lerner UH, Brunius G, Anduren I, Berggren PO, Juntti-Berggren L, Modeer T, (1992). Bradykinin induces a B2 receptor-mediated calcium signal linked to prostanoid formation in human gingival fibroblasts in vitro. Agents Actions 37: 44-52.
30. Ljunggren O, Lerner UH, (1990). Evidence for BK1 bradykinin-receptor- mediated prostaglandin formation in osteoblasts and subsequent enhancement of bone resorption. Br J Pharmacol 101: 382-386.
31. Lubberts E, Joosten LA, Chabaud M, van Den Bersselaar L, Oppers B, Coenen-De Roo CJ, et al. (2000). IL-4 gene therapy for collagen arthritis suppresses synovial IL-17 and osteoprotegerin ligand and prevents bone erosion. J Clin Invest 105: 1697-1710.
32. Marceau F, Hess JF, Bachvarov DR, (1998). The B1 receptors for kinins. Pharmacol Rev 50: 357-386.
33. McGrath J, Drummond G, McLachlan E, Kilkenny C, Wainwright C, (2010). Guidelines for reporting experiments involving animals: the ARRIVE guidelines. Br J Pharmacol 160: 1573-1576.
34. Miossec P, Chomarat P, Dechanet J, Moreau JF, Roux JP, Delmas P, et al. (1994). Interleukin-4 inhibits bone resorption through an effect on osteoclasts and proinflammatory cytokines in an ex vivo model of bone resorption in rheumatoid arthritis. Arthritis Rheum 37: 1715-1722.
35. Moreau ME, Garbacki N, Molinaro G, Brown NJ, Marceau F, Adam A, (2005). The kallikrein-kinin system: current and future pharmacological targets. J Pharmacol Sci 99: 6-38.
36. Moreno JL, Kaczmarek M, Keegan AD, Tondravi M, (2003). IL-4 suppresses osteoclast development and mature osteoclast function by a STAT6-dependent mechanism: irreversible inhibition of the differentiation program activated by RANKL. Blood 102: 1078-1086.
37. Murata T, Obiri NI, Puri RK, (1998). Structure of and signal transduction through interleukin-4 and interleukin-13 receptors (review). Int J Mol Med 1: 551-557.
38. Nagai M, Sato N, (1999). Reciprocal gene expression of osteoclastogenesis inhibitory factor and osteoclast differentiation factor regulates osteoclast formation. Biochem Biophys Res Commun 257: 719-723.
39. Nakao S, Ogata Y, Modeer T, Segawa M, Furuyama S, Sugiya H, (2001). Bradykinin induces a rapid cyclooxygenase-2 mRNA expression via Ca2+ mobilization in human gingival fibroblasts primed with interleukin-1 beta. Cell Calcium 29: 446-452.
40. Okada Y, Lorenzo JA, Freeman AM, Tomita M, Morham SG, Raisz LG, et al. (2000). Prostaglandin G/H synthase-2 is required for maximal formation of osteoclast-like cells in culture. J Clin Invest 105: 823-832.
41. Palmqvist P, Lundberg P, Persson E, Johansson A, Lundgren I, Lie A, et al. (2006). Inhibition of hormone and cytokine-stimulated osteoclastogenesis and bone resorption by interleukin-4 and interleukin-13 is associated with increased osteoprotegerin and decreased RANKL and RANK in a STAT6-dependent pathway. J Biol Chem 281: 2414-2429.
42. Riancho JA, Zarrabeitia MT, Olmos JM, Amado JA, Gonzalez-Macias J, (1993). Effects of interleukin-4 on human osteoblast-like cells. Bone Miner 21: 53-61.
43. Sardi SP, Rey-Ares V, Pujol-Lereis VA, Serrano SA, Rothlin RP, (2002). Further pharmacological evidence of nuclear factor-kappa B pathway involvement in bradykinin B1 receptor-sensitized responses in human umbilical vein. J Pharmacol Exp Ther 301: 975-980.
44. Souza PP, Palmqvist P, Lundberg P, Lundgren I, Hanstrom L, Souza JA, et al. (2012). Interleukin-4 and interleukin-13 inhibit the expression of leukemia inhibitory factor and interleukin-11 in fibroblasts. Mol Immunol 49: 601-610.
45. Stashenko P, Goncalves RB, Lipkin B, Ficarelli A, Sasaki H, Campos-Neto A, (2007). Th1 immune response promotes severe bone resorption caused by Porphyromonas gingivalis. Am J Pathol 170: 203-213.
46. Tabata Y, Khurana Hershey GK, (2007). IL-13 receptor isoforms: breaking through the complexity. Curr Allergy Asthma Rep 7: 338-345.
47. te Velde AA, Huijbens RJ, Heije K, de, Vries JE, Figdor CG, (1990). Interleukin-4 (IL-4) inhibits secretion of IL-1 beta, tumor necrosis factor alpha, and IL-6 by human monocytes. Blood 76: 1392-1397.
48. Woods JM, Katschke KJ, Volin MV, Ruth JH, Woodruff DC, Amin MA, et al. (2001). IL-4 adenoviral gene therapy reduces inflammation, proinflammatory cytokines, vascularization, and bony destruction in rat adjuvant-induced arthritis. J Immunol 166: 1214-1222.
49. Worthy K, Figueroa CD, Dieppe PA, Bhoola KD, (1990). Kallikreins and kinins: mediators in inflammatory joint disease? Int J Exp Pathol 71: 587-601.
50. Zubakova R, Gille A, Faussner A, Hilgenfeldt U, (2008). Ca2+ signalling of kinins in cells expressing rat, mouse and human B1/B2-receptor. Int Immunopharmacol 8: 276-281.
51. Zurawski SM, Chomarat P, Djossou O, Bidaud C, McKenzie AN, Miossec P, et al. (1995). The primary binding subunit of the human interleukin-4 receptor is also a component of the interleukin-13 receptor. J Biol Chem 270: 13869-13878.