Regulation of lipopolysaccharide-induced inflammatory response and endotoxemia by β-arrestins

Journal of Cellular Physiology

Volumn 225, Issue 2, 2010, Pages 406-416

  Porter, Katie J ^a   Gonipeta, Babu ^a   Parvataneni, Sitaram ^a   Appledorn, Daniel M ^b   Patial, Sonika ^a   Sharma, Deepika ^b   Gangur, Venugopal ^c   Amalfitano, Andrea ^b   Parameswaran, Narayanan ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b Department of Microbiology and Molecular Genetics Michigan State University ^*  (United States)

^c MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA ARRESTIN 1; BETA ARRESTIN 2; CD11B ANTIGEN; CHEMOKINE; CYTOKINE; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOPOLYSACCHARIDE; MITOGEN ACTIVATED PROTEIN KINASE; BETA ARRESTIN; CD11 ANTIGEN; CYCLOOXYGENASE 2; MITOGEN ACTIVATED PROTEIN KINASE KINASE; PTGS2 PROTEIN, MOUSE; RETINA S ANTIGEN; TLR4 PROTEIN, MOUSE; TOLL LIKE RECEPTOR 4;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD LEVEL; CELL TYPE; CHROMATIN; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENDOTOXEMIA; IN VIVO STUDY; INFLAMMATION; KNOCKOUT MOUSE; LETHALITY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; SPLEEN CELL; WILD TYPE; ANIMAL; CHEMICALLY INDUCED; CULTURE TECHNIQUE; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; SIGNAL TRANSDUCTION; SPLEEN; TOXICITY;

MUS;

ANIMALS; ANTIGENS, CD11; ARRESTINS; CELL CULTURE TECHNIQUES; CYCLOOXYGENASE 2; CYTOKINES; ENDOTOXEMIA; GENE EXPRESSION REGULATION; INFLAMMATION; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, KNOCKOUT; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; NF-KAPPA B; SIGNAL TRANSDUCTION; SPLEEN; TOLL-LIKE RECEPTOR 4;

EID: 77956502456     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.22289     Document Type: Article

References (62)

1. Appledorn DM, Patial S, McBride A, Godbehere S, Van Rooijen N, Parameswaran N, Amalfitano A. 2008. Adenovirus vector-induced innate inflammatory mediators, MAPK signaling, as well as adaptive immune responses are dependent upon both TLR2 and TLR9 in vivo. J Immunol 181:2134-2144.
2. Armstrong L, Medford AR, Hunter KJ, Uppington KM, Millar AB. 2004. Differential expression of Toll-like receptor (TLR)-2 and TLR-4 on monocytes in human sepsis. Clin Exp Immunol 136:312-319.
3. Aung HT, Schroder K, Himes SR, Brion K, van Zuylen W, Trieu A, Suzuki H, Hayashizaki Y, Hume DA, Sweet MJ, Ravasi T. 2006. LPS regulates proinflammatory gene expression in macrophages by altering histone deacetylase expression. FASEB J 20:1315-1327.
4. Barnes PJ, Adcock IM, Ito K. 2005. Histone acetylation and deacetylation: Importance in inflammatory lung diseases. Eur Respir J 25:552-563. (Pubitemid 40331188)
5. Beutler B. 2004. Innate immunity: An overview. Mol Immunol 40:845-859.
6. Beutler B. 2005. The Toll-like receptors: Analysis by forward genetic methods. Immunogenetics 57:385-392. (Pubitemid 41396763)
7. Beutler BA. 2009. TLRs and innate immunity. Blood 113:1399-1407.
8. Biswas SK, Lopez-Collazo E. 2009. Endotoxin tolerance: New mechanisms, molecules and clinical significance. Trends Immunol 30:475-487.
9. Blackwell TS, Blackwell TR, Christman JW. 1997. Impaired activation of nuclear factor-kappaB in endotoxin-tolerant rats is associated with down-regulation of chemokine gene expression and inhibition of neutrophilic lung inflammation. J Immunol 158:5934-5940.
10. Buchwald M, Kramer OH, Heinzel T. 2009. HDACi - Targets beyond chromatin. Cancer Lett 280:160-167.
11. Card JW, Carey MA, Bradbury JA, DeGraff LM, Morgan DL, Moorman MP, Flake GP, Zeldin DC. 2006. Gender differences in murine airway responsiveness and lipopolysaccharide-induced inflammation. J Immunol 177:621-630.
12. Choi Y, Park SK, Kim HM, Kang JS, Yoon YD, Han SB, Han JW, Yang JS, Han G. 2008. Histone deacetylase inhibitor KBH-A42 inhibits cytokine production in RAW 264.7 macrophage cells and in vivo endotoxemia model. Exp Mol Med 40:574-581. (Pubitemid 352789098)
13. Choi KC, Jung MG, Lee YH, Yoon JC, Kwon SH, Kang HB, Kim MJ, Cha JH, Kim YJ, Jun WJ, Lee JM, Yoon HG. 2009a. Epigallocatechin-3-gallate, a histone acetyltransferase inhibitor, inhibits EBV-induced B lymphocyte transformation via suppression of RelA acetylation. Cancer Res 69:583-592.
14. Choi KC, Lee YH, Jung MG, Kwon SH, Kim MJ, Jun WJ, Lee J, Lee JM, Yoon HG. 2009b. Gallic acid suppresses lipopolysaccharide-induced nuclear factor-kappaB signaling by preventing RelA acetylation in A549 lung cancer cells. Mol Cancer Res 7:2011-2021.
15. Cook JA. 2005. Eicosanoids. Crit Care Med 33:S488-S491.
16. Daubeuf B, Mathison J, Spiller S, Hugues S, Herren S, Ferlin W, Kosco-Vilbois M, Wagner H, Kirschning CJ, Ulevitch R, Elson G. 2007. TLR4/MD-2 monoclonal antibody therapy affords protection in experimental models of septic shock. J Immunol 179:6107-6114.
17. Deriy LV, Beno DW, Uhing MR, Jiyamapa-Serna VA, Kimura RE. 2002. Splenectomy ablates endotoxin-induced IFNgamma response in rats. Shock 17:312-315.
18. DeWire SM, Ahn S, Lefkowitz RJ, Shenoy SK. 2007. Beta-arrestins and cell signaling. Annu Rev Physiol 69:483-510.
19. Fan H, Luttrell LM, Tempel GE, Senn JJ, Halushka PV, Cook JA. 2007. Beta-arrestins 1 and 2 differentially regulate LPS-induced signaling and pro-inflammatory gene expression. Mol Immunol 44:3092-3099. (Pubitemid 46610509)
20. Foster SL, Hargreaves DC, Medzhitov R. 2007. Gene-specific control of inflammation by TLR-induced chromatin modifications. Nature 447:972-978.
21. Funk CD. 2001. Prostaglandins and leukotrienes: Advances in eicosanoid biology. Science 294:1871-1875.
22. Gao H, Sun Y, Wu Y, Luan B, Wang Y, Qu B, Pei G. 2004. Identification of beta-arrestin2 as aG protein-coupled receptor-stimulated regulator of NF-kappaB pathways. Mol Cell 14:303-317.
23. Greten FR, Arkan MC, Bollrath J, Hsu LC, Goode J, Miething C, Goktuna SI, Neuenhahn M, Fierer J, Paxian S, Van Rooijen N, Xu Y, O'Cain T, Jaffee BB, Busch DH, Duyster J, Schmid RM, Eckmann L, Karin M. 2007. NF-kappaB is a negative regulator of IL-1beta secretion as revealed by genetic and pharmacological inhibition of IKKbeta. Cell 130:918-931.
24. Hayden MS, Ghosh S. 2004. Signaling to NF-kappaB. Genes Dev 18:2195-2224.
25. Kang J, Shi Y, Xiang B, Qu B, Su W, Zhu M, Zhang M, Bao G, Wang F, Zhang X, Yang R, Fan F, Chen X, Pei G, Ma L. 2005. A nuclear function of beta-arrestin1 in GPCR signaling: Regulation of histone acetylation and gene transcription. Cell 123:833-847. (Pubitemid 41721030)
26. Kohler J, Heumann D, Garotta G, LeRoy D, Bailat S, Barras C, Baumgartner JD, Glauser MP. 1993. IFN-gamma involvement in the severity of gram-negative infections in mice. J Immunol 151:916-921.
27. Kuo MH, Allis CD. 1998. Roles of histone acetyltransferases and deacetylases in gene regulation. BioEssays 20:615-626.
28. Lehmann V, Freudenberg MA, Galanos C. 1987. Lethal toxicity of lipopolysaccharide and tumor necrosis factor in normal and D-galactosamine- treated mice. J Exp Med 165:657-663.
29. Leon CG, Tory R, Jia J, Sivak O, Wasan KM. 2008. Discovery and development of toll-like receptor 4 (TLR4) antagonists: A new paradigm for treating sepsis and other diseases. Pharm Res 25:1751-1761.
30. Leoni F, Fossati G, Lewis EC, Lee JK, Porro G, Pagani P, Modena D, Moras ML, Pozzi P, Reznikov LL, Siegmund B, Fantuzzi G, Dinarello CA, Mascagni P. 2005. The histone deacetylase inhibitor ITF2357 reduces production of pro-inflammatory cytokines in vitro and systemic inflammation in vivo. Mol Med 11:1-15.
31. Loniewski KJ, Patial S, Parameswaran N. 2007. Sensitivity of TLR4- and -7-induced NF kappa B1 p105-TPL2-ERK pathway to TNF-receptor-associated-factor-6 revealed by RNAi in mouse macrophages. Mol Immunol 44:3715-3723. (Pubitemid 46817667)
32. Loniewski K, Shi Y, Pestka J, Parameswaran N. 2008. Toll-like receptors differentially regulate GPCR kinases and arrestins in primary macrophages. Mol Immunol 45:2312-2322.
33. Lorenz E, Mira JP, Frees KL, Schwartz DA. 2002. Relevance of mutations in the TLR4 receptor in patients with gram-negative septic shock. Arch Intern Med 162:1028-1032.
34. Marriott I, Huet-Hudson YM. 2006. Sexual dimorphism in innate immune responses to infectious organisms. Immunol Res 34:177-192.
35. Marriott I, Bost KL, Huet-Hudson YM. 2006. Sexual dimorphism in expression of receptors for bacterial lipopolysaccharides in murine macrophages: A possible mechanism for gender-based differences in endotoxic shock susceptibility. J Reprod Immunol 71:12-27. (Pubitemid 43975140)
36. Miggin SM, O'Neill LA. 2006. New insights into the regulation of TLR signaling. J Leukoc Biol 80:220-226.
37. Moeniralam HS, Bemelman WA, Endert E, Koopmans R, Sauerwein HP, Romijn JA. 1997. The decrease in nonsplenic interleukin-6 (IL-6) production after splenectomy indicates the existence of a positive feedback loop of IL-6 production during endotoxemia in dogs. Infect Immun 65:2299-2305.
38. Navuluri L, Parvataneni S, Hassan H, Birmingham NP, Kelly C, Gangur V. 2006. Allergic and anaphylactic response to sesame seeds in mice: Identification of Ses i 3 and basic subunit of 11s globulins as allergens. Int Arch Allergy Immunol 140:270-276.
39. O'Brien GC, Wang JH, Redmond HP. 2005. Bacterial lipoprotein induces resistance to gram-negative sepsis in TLR4-deficient mice via enhanced bacterial clearance. J Immunol 174:1020-1026.
40. O'Neill LA. 2008. 'Fine tuning' TLR signaling. Nat Immunol 9:459-461.
41. Parameswaran N, Pao CS, Leonhard KS, Kang DS, Kratz M, Ley SC, Benovic JL. 2006. Arrestin-2 and G protein-coupled receptor kinase 5 interact with NFkappaB1 p105 and negatively regulate lipopolysaccharide-stimulated ERK1/2 activation inmacrophages. J Biol Chem 281:34159-34170. (Pubitemid 46036624)
42. Parvataneni S, Birmingham NP, Gonipeta B, Gangur V. 2009. Dominant, non-MHC genetic control of food allergy in an adjuvant-free mouse model. Int J Immunogenet 36:261-267.
43. Patial S, Luo J, Porter KJ, Benovic JL, Parameswaran N. 2010. G-protein-coupled-receptor kinases mediate TNFalpha-induced NF-kappaB signalling via direct interaction with and phosphorylation of IkappaBalpha. Biochem J 425:169-178.
44. Rajagopal K, Whalen EJ, Violin JD, Stiber JA, Rosenberg PB, Premont RT, Coffman TM, Rockman HA, Lefkowitz RJ. 2006. Beta-arrestin2-mediated inotropic effects of the angiotensin II type 1A receptor in isolated cardiac myocytes. Proc Natl Acad Sci USA 103:16284-16289.
45. Reddy RC, Chen GH, Tateda K, Tsai WC, Phare SM, Mancuso P, Peters-Golden M, Standiford TJ. 2001. Selective inhibition of COX-2 improves early survival in murine endotoxemia but not in bacterial peritonitis. Am J Physiol Lung Cell Mol Physiol 281:L537-L543.
46. Rettew JA, Huet-Hudson YM, Marriott I. 2008. Testosterone reduces macrophage expression in the mouse of toll-like receptor 4, a trigger for inflammation and innate immunity. Biol Reprod 78:432-437. (Pubitemid 351416468)
47. Rettew JA, Huet YM, Marriott I. 2009. Estrogens augment cell surface TLR4 expression on murine macrophages and regulate sepsis susceptibility in vivo. Endocrinology 150:3877-3884.
48. Rittirsch D, Flierl MA, Ward PA. 2008. Harmful molecular mechanisms in sepsis. Nat Rev Immunol 8:776-787.
49. Sabroe I, Parker LC, Dower SK, Whyte MK. 2008. The role of TLR activation in inflammation. J Pathol 214:126-135.
50. Sailhamer EA, Li Y, Smith EJ, Shuja F, Shults C, Liu B, Soupir C, deMoya M, Velmahos G, Alam HB. 2008. Acetylation: A novel method for modulation of the immune response following trauma/hemorrhage and inflammatory second hit in animals and humans. Surgery 144:204-216.
51. Salomao R, Martins PS, Brunialti MK, Fernandes Mda L, Martos LS, Mendes ME, Gomes NE, Rigato O. 2008. TLR signaling pathway in patients with sepsis. Shock 30:73-77.
52. Senaldi G, Shaklee CL, Guo J, Martin L, Boone T, Mak TW, Ulich TR. 1999. Protection against the mortality associated with disease models mediated by TNF and IFN-gamma in mice lacking IFN regulatory factor-1. J Immunol 163:6820-6826.
53. Seregin SS, Appledorn DM, Patial S, Bujold M, Nance W, Godbehere S, Parameswaran N, Amalfitano A. 2010. Beta-arrestins modulate adenovirus-vector- induced innate immune responses: Differential regulation by beta-arrestin-1 and beta-arrestin-2. Virus Res 147:123-134.
54. Spange S, Wagner T, Heinzel T, Kramer OH. 2009. Acetylation of non-histone proteins modulates cellular signalling at multiple levels. Int J Biochem Cell Biol 41:185-198.
55. Spiller S, Elson G, Ferstl R, Dreher S, Mueller T, Freudenberg M, Daubeuf B, Wagner H, Kirschning CJ. 2008. TLR4-induced IFN-gamma production increases TLR2 sensitivity and drives gram-negative sepsis in mice. J Exp Med 205:1747-1754.
56. Sun SC, Ley SC. 2008. New insights into NF-kappaB regulation and function. Trends Immunol 29:469-478.
57. Symons A, Beinke S, Ley SC. 2006. MAP kinase kinase kinases and innate immunity. Trends Immunol 27:40-48. (Pubitemid 43083563)
58. Wang Y, Tang Y, Teng L, Wu Y, Zhao X, Pei G. 2006. Association of beta-arrestin and TRAF6 negatively regulates Toll-like receptor-interleukin 1 receptor signaling. Nat Immunol 7:139-147. (Pubitemid 43135879)
59. Witherow DS, Garrison TR, Miller WE, Lefkowitz RJ. 2004. Beta-arrestin inhibits NF-kappaB activity by means of its interaction with the NF-kappaB inhibitor IkappaBalpha. Proc Natl Acad Sci USA 101:8603-8607.
60. Wysocka M, Kubin M, Vieira LQ, Ozmen L, Garotta G, Scott P, Trinchieri G. 1995. Interleukin-12 is required for interferon-gamma production and lethality in lipopolysaccharide-induced shock in mice. Eur J Immunol 25:672-676.
61. Yu Z, Zhang W, Kone BC. 2002. Histone deacetylases augment cytokine induction of the iNOS gene. J Am Soc Nephrol 13:2009-2017. (Pubitemid 34790776)
62. Zisman DA, Kunkel SL, Strieter RM, Gauldie J, Tsai WC, Bramson J, Wilkowski JM, Bucknell KA, Standiford TJ. 1997. Anti-interleukin-12 therapy protects mice in lethal endotoxemia but impairs bacterial clearance in murine Escherichia coli peritoneal sepsis. Shock 8:349-356. (Pubitemid 127654348)