Inhibition of RIP2's tyrosine kinase activity limits NOD2-driven cytokine responses

Genes and Development

Volumn 24, Issue 23, 2010, Pages 2666-2677

  Tigno Aranjuez, Justine T ^a   Asara, John M ^b,c   Abbott, Derek W ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Innate immunity; ITCH; NOD2; RIP2; Tyrosine kinase

Indexed keywords

CASPASE RECRUITMENT DOMAIN PROTEIN 15; CYTOKINE; EPIDERMAL GROWTH FACTOR RECEPTOR; ERLOTINIB; GEFITINIB; MURAMYL DIPEPTIDE; PROTEIN TYROSINE KINASE; RECEPTOR INTERACTING PROTEIN 2; TYROSINE; UNCLASSIFIED DRUG;

ANTIINFLAMMATORY ACTIVITY; ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; DRUG INHIBITION; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME INHIBITION; GENE FREQUENCY; GENE MUTATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ACETYLMURAMYL-ALANYL-ISOGLUTAMINE; ANIMALS; CELLS, CULTURED; CYTOKINES; ENZYME ACTIVATION; GENE KNOCKOUT TECHNIQUES; HEK293 CELLS; HT29 CELLS; HUMANS; MICE; NOD2 SIGNALING ADAPTOR PROTEIN; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; QUINAZOLINES; RECEPTOR-INTERACTING PROTEIN SERINE-THREONINE KINASE 2; TYROSINE; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

BACTERIA (MICROORGANISMS);

EID: 78649890151     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1964410     Document Type: Article

References (49)

1. Abbott DW, Wilkins A, Asara JM, Cantley LC. 2004. The Crohn's disease protein, NOD2, requires RIP2 in order to induce ubiquitinylation of a novel site on NEMO. Curr Biol 14: 2217-2227. (Pubitemid 40033358)
2. Abbott DW, Yang Y, Hutti JE, Madhavarapu S, Kelliher MA, Cantley LC. 2007. Coordinated regulation of Toll-like receptor and NOD2 signaling by K63-linked polyubiquitin chains. Mol Cell Biol 27: 6012-6025. (Pubitemid 47326691)
3. Argast GM, Fausto N, Campbell JS. 2005. Inhibition of RIP2/RIck/CARDIAK activity by pyridinyl imidazole inhibitors of p38 MAPK. Mol Cell Biochem 268: 129-140. (Pubitemid 40287835)
4. Barnich N, Aguirre JE, Reinecker HC, Xavier R, Podolsky DK. 2005. Membrane recruitment of NOD2 in intestinal epithelial cells is essential for NF-κB activation in muramyl dipeptide recognition. J Cell Biol 170: 21-26. (Pubitemid 40994092)
5. Bertrand MJ, Doiron K, Labbe K, Korneluk RG, Barker PA, Saleh M. 2009. Cellular inhibitors of apoptosis cIAP1 and cIAP2 are required for innate immunity signaling by the pattern recognition receptors NOD1 and NOD2. Immunity 30: 789-801.
6. Brehmer D, Greff Z, Godl K, Blencke S, Kurtenbach A, Weber M, Müller S, Klebl B, Cotton M, Kéri G, et al. 2005. Cellular targets of gefitinib. Cancer Res 65: 379-382.
7. Chamaillard M, Philpott D, Girardin SE, Zouali H, Lesage S, Chareyre F, Bui TH, Giovannini M, Zaehringer U, Penard-Lacronique V, et al. 2003. Gene-environment interaction modulated by allelic heterogeneity in inflammatory diseases. Proc Natl Acad Sci 100: 3455-3460.
8. Chen G, Shaw MH, Kim YG, Nunez G. 2009. NOD-like receptors: Role in innate immunity and inflammatory disease. Annu Rev Pathol 4: 365-398.
9. Clark NM, Marinis JM, Cobb BA, Abbott DW. 2008. MEKK4 sequesters RIP2 to dictate NOD2 signal specificity. Curr Biol 18: 1402-1408.
10. Daub H, Olsen JV, Bairlein M, Gnad F, Oppermann FS, Körner R, Greff Z, Kéri G, Stemmann O, Mann M. 2008. Kinaseselective enrichment enables qualtitative phosphoproteomics of the kinome across the cell cycle. Mol Cell 31: 438-448.
11. Duncan JA, Bergstralh DT, Wang Y, Willingham SB, Ye Z, Zimmermann AG, Ting JP. 2007. Cryopyrin/NALP3 binds ATP/dATP, is an ATPase, and requires ATP binding to mediate inflammatory signaling. Proc Natl Acad Sci 104: 8041-8046. (Pubitemid 47185872)
12. Eickhoff J, Hanke M, Stein-Gerlach M, Kiang TP, Herzberger K, Habenberger P, Muller S, Klebl B, Marschall M, Stamminger T, et al. 2004. RICK activates a NF-κB-dependent anti-human cytomegalovirus response. J Biol Chem 279: 9642-9652.
13. Faustin B, Lartigue L, Bruey JM, Luciano F, Sergienko E, Bailly-Maitre B, Volkmann N, Hanein D, Rouiller I, Reed JC. 2007. Reconstituted NALP1 inflammasome reveals two-step mechanism of caspase-1 activation. Mol Cell 25: 713-724.
14. Girardin SE, Boneca IG, Viala J, Chamaillard M, Labigne A, Thomas G, Philpott DJ, Sansonetti PJ. 2003. Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J Biol Chem 278: 8869-8872. (Pubitemid 36800360)
15. Hasegawa M, Fujimoto Y, Lucas PC, Nakano H, Fukase K, Núñez G, Inohara N. 2008. A critical role of RICK/RIP2 polyubiquitination in Nod-induced NF-κB activation. EMBO J 27: 373-383. (Pubitemid 351161652)
16. Hugot JP, Chamaillard M, Zouali H, Lesage S, Cezard JP, Belaiche J, Almer S, Tysk C, O'Morain CA, Gassull M, et al. 2001. Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn's disease. Nature 411: 599-603.
17. Hunter T, Sefton BM. 1980. Transforming gene product of Rous sarcoma virus phosphorylates tyrosine. Proc Natl Acad Sci 77: 1311-1315. (Pubitemid 10072278)
18. Hutti JE, Turk BE, Asara JM, Ma A, Cantley LC, Abbott DW. 2007. IκB kinase b phosphorylates the K63 deubiquitinase A20 to cause feedback inhibition of the NF-κB pathway. Mol Cell Biol 27: 7451-7461. (Pubitemid 350033652)
19. Inohara N, del Peso L, Koseki T, Chen S, Núñez G. 1998. RICK, a novel protein kinase containing a caspase recruitment domain, interacts with CLARP and regulates CD95-mediated apoptosis. J Biol Chem 273: 12296-12300. (Pubitemid 28240597)
20. Inohara N, Koseki T, del Peso L, Hu Y, Yee C, Chen S, Carrio R, Merino J, Liu D, Ni J, et al. 1999. Nod1, an Apaf-1-like activator of caspase-9 and nuclear factor-κB. J Biol Chem 274: 14560-14567. (Pubitemid 129518777)
21. Inohara N, Ogura Y, Fontalba A, Gutierrez O, Pons F, Crespo J, Fukase K, Inamura S, Kusumoto S, Hashimoto M, et al. 2003. Host recognition of bacterial muramyl dipeptide mediated through NOD2. Implications for Crohn's disease. J Biol Chem 278: 5509-5512.
22. Kanazawa N, Okafuji I, Kambe N, Nishikomori R, Nakata- Hizume M, Nagai S, Fuji A, Yuasa T, Manki A, Sakurai Y, et al. 2005. Early-onset sarcoidosis and CARD15 mutations with constitutive nuclear factor-κB activation: Common genetic etiology with Blau syndrome. Blood 105: 1195-1197.
23. Kentrup H, Becker W, Heukelbach J, Wilmes A, Schürmann A, Huppertz C, Kainulainen H, Joost HG. 1996. Dyrk, a dual specificity protein kinase with unique structural features whose activity is dependent on tyrosine residues between subdomains VII and VIII. J Biol Chem 271: 3488-3495. (Pubitemid 26065657)
24. Kobayashi K, Inohara N, Hernandez LD, Galan JE, Nunez G, Janeway CA, Medzhitov R, Flavell RA. 2002. RICK/Rip2/CARDIAK mediates signalling for receptors of the innate and adaptive immune systems. Nature 416: 194-199. (Pubitemid 34246479)
25. Kobayashi S, Boggon TJ, Dayaram T, Janne PA, Kocher O, Meyerson M, Johnson BE, Eck MJ, Tenen DG, Halmos B. 2005. EGFR mutation and resistance of non-small-cell lung cancer to gefitinib. N Engl J Med 352: 786-792. (Pubitemid 40271173)
26. Krieg A, Correa RG, Garrison JB, Le Negrate G, Welsh K, Huang Z, Knoefel WT, Reed JC. 2009. XIAP mediates NOD signaling via interaction with RIP2. Proc Natl Acad Sci 106: 14524-14529.
27. Lécine P, Esmiol S, Métais JY, Nicoletti C, Nourry C, McDonald C, Nunez G, Hugot JP, Borg JP, Ollendorff V. 2007. The NOD2-RICK complex signals from the plasma membrane. J Biol Chem 282: 15197-15207.
28. Lochhead PA, Sibbet G, Morrice N, Cleghon V. 2005. Activation-loop autophosphorylation is mediated by novel transitional intermediate form of DYRKs. Cell 121: 925-936.
29. Lohr NJ, Molleston JP, Strauss KA, Torres-Martinez W, Sherman EA, Squires RH, Rider NL, Chikwava KR, Cummings OW, Morton DH, et al. 2010. Human ITCH E3 ubiquitin ligase deficiency causes syndromic multisystem autoimmune disease. Am J Hum Genet 86: 447-453.
30. McCarthy JV, Ni J, Dixit VM. 1998. RIP2 is a novel NF-κB-activating and cell death-inducing kinase. J Biol Chem 273: 16968-16975. (Pubitemid 28311729)
31. McDonald C, Chen FF, Ollendorff V, Ogura Y, Marchetto S, Lecine P, Borg JP, Nunez G. 2005. A role for Erbin in the regulation of Nod2-dependent NF-κB signaling. J Biol Chem 280: 40301-40309.
32. Miceli-Richard C, Lesage S, Rybojad M, Prieur AM, Manouvrier-Hanu S, Hafner R, Chamaillard M, Zouali H, Thomas G, Hugot JP. 2001. CARD15 mutations in Blau syndrome. Nat Genet 29: 19-20.
33. Negroni A, Stronati L, Pierdomenico M, Tirindelli D, Di Nardo G, Mancini V, Maiella G, Cucchiara S. 2009. Activation of NOD2-mediated intestinal pathway in a pediatric population with Crohn's disease. Inflamm Bowel Dis 15: 1145-1154.
34. Nembrini C, Kisielow J, Shamshiev AT, Tortola L, Coyle AJ, Kopf M, Marsland BJ. 2009. The kinase activity of Rip2 determines its stability and consequently Nod1- and Nod2-mediated immune responses. J Biol Chem 284: 19183-19188.
35. Ogura Y, Bonen DK, Inohara N, Nicolae DL, Chen FF, Ramos R, Britton H, Moran T, Karaliuskas R, Duerr RH, et al. 2001a. A frameshift mutation in NOD2 associated with susceptibility to Crohn's disease. Nature 411: 603-606.
36. Ogura Y, Inohara N, Benito A, Chen FF, Yamaoka S, Nunez G. 2001b. Nod2, a Nod1/Apaf-1 family member that is restricted to monocytes and activates NF-κB. J Biol Chem276: 4812-4818.
37. Olsen JV, Blagoev B, Gnad F, Macek B, Kumar C, Mortensen P, Mann M. 2006. Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127: 635-648.
38. Oppermann FS, Gnad F, Olsen JV, Hornberger R, Greff Z, Kéri G, Mann M, Daub H. 2009. Large-scale proteomics analysis of the human kinome. Mol Cell Proteomics 8: 1751-1764.
39. Park JH, Kim YG, McDonald C, Kanneganti TD, Hasegawa M, Body-Malapel M, Inohara N, Nunez G. 2007. RICK/RIP2 mediates innate immune responses induced through Nod1 and Nod2 but not TLRs. J Immunol 178: 2380-2386.
40. -/- locus encodes a novel ubiquitin protein ligase that is disrupted in a18H mice. Nat Genet 18: 143-146.
41. Rosenstiel P, Schreiber S. 2009. NOD-like receptors - Pivotal guardians of the immunological integrity of barrier organs. Adv Exp Med Biol 653: 35-47.
42. Schurmann M, Valentonyte R, Hampe J, Muller-Quernheim J, Schwinger E, Schreiber S. 2003. CARD15 gene mutations in sarcoidosis. Eur Respir J 22: 748-754.
43. Strober W, Murray PJ, Kitani A, Watanabe T. 2006. Signalling pathways and molecular interactions of NOD1 and NOD2. Nat Rev Immunol 6: 9-21.
44. Stronati L, Negroni A, Merola P, Pannone V, Borrelli O, Cirulli M, Annese V, Cucchiara S. 2008. Mucosal NOD2 expression and NF-κB activation in pediatric Crohn's disease. Inflamm Bowel Dis 14: 295-302.
45. Tanabe T, Chamaillard M, Ogura Y, Zhu L, Qiu S, Masumoto J, Ghosh P, Moran A, Predergast MM, Tromp G, et al. 2004. Regulatory regions and critical residues of NOD2 involved in muramyl dipeptide recognition. EMBO J 23: 1587-1597.
46. Tao M, Scacheri PC, Marinis JM, Harhaj EW, Matesic LE, Abbott DW. 2009. ITCH K63-ubiquitinates the NOD2 binding protein, RIP2, to influence inflammatory signaling pathways. Curr Biol 19: 1255-1263.
47. Thome M, Hofmann K, Burns K, Martinon F, Bodmer JL, Mattmann C, Tschopp J. 1998. Identification of CARDIAK, a RIP-like kinase that associates with caspase-1. Curr Biol 8: 885-888.
48. Windheim M, Lang C, Peggie M, Plater LA, Cohen P. 2007. Molecular mechanisms involved in the regulation of cytokine production by muramyl dipeptide. Biochem J 404: 179-190.
49. Yang Y, Yin C, Pandey A, Abbott D, Sassetti C, Kelliher MA. 2007. NOD2 pathway activation by MDP or Mycobacterium tuberculosis infection involves the stable polyubiquitination of Rip2. J Biol Chem 282: 36223-36229.