NOD2-nitric oxide-responsive microRNA-146a activates Sonic hedgehog signaling to orchestrate inflammatory responses in murine model of inflammatory bowel disease

Journal of Biological Chemistry

Volumn 288, Issue 46, 2013, Pages 33037-33048

  Ghorpade, Devram Sampat ^a   Sinha, Akhuri Yash ^a   Holla, Sahana ^a   Singh, Vikas ^a   Balaji, Kithiganahalli Narayanaswamy ^a  

^a INDIAN INSTITUTE OF SCIENCE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

CHRONIC INFLAMMATORY; ENTERIC BACTERIA; GENETIC SUSCEPTIBILITY; GENETIC VARIANTS; INDUCIBLE NITRIC OXIDE SYNTHASE (INOS); INFLAMMATORY BOWEL DISEASE; INFLAMMATORY RESPONSE; PATHOPHYSIOLOGY;

CROSSTALK; GENE EXPRESSION; MACROPHAGES; NITRIC OXIDE; RNA;

SIGNALING;

CASPASE RECRUITMENT DOMAIN PROTEIN 15; INDUCIBLE NITRIC OXIDE SYNTHASE; MICRORNA 146A; NITRIC OXIDE; SONIC HEDGEHOG PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COLITIS; CONTROLLED STUDY; EX VIVO STUDY; GENE FUNCTION; IN VIVO STUDY; MACROPHAGE; MOUSE; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; UPREGULATION;

INFLAMMATION; INFLAMMATORY BOWEL DISEASE; INNATE IMMUNITY; MACROPHAGES; MICRORNA; NITRIC OXIDE; NOD-LIKE RECEPTORS (NLR); SIGNAL TRANSDUCTION; SIGNALING;

ANIMALS; DEXTRAN SULFATE; DISEASE MODELS, ANIMAL; HEDGEHOG PROTEINS; INFLAMMATORY BOWEL DISEASES; MACROPHAGES, PERITONEAL; MICE; MICE, KNOCKOUT; MICRORNAS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; NOD2 SIGNALING ADAPTOR PROTEIN; SIGNAL TRANSDUCTION;

EID: 84887833141     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.492496     Document Type: Article

References (45)

1. Kufer, T. A. (2008) Signal transduction pathways used by NLR-type innate immune receptors. Mol. Biosyst. 4, 380-386
2. Newton, K., and Dixit, V. M. (2012) Signaling in innate immunity and inflammation. Cold Spring Harb. Perspect. Biol. 4, a006049
3. Proell, M., Riedl, S. J., Fritz, J. H., Rojas, A. M., and Schwarzenbacher, R. (2008) The Nod-like receptor (NLR) family: a tale of similarities and differences. PLoS One 3, e2119
4. Cho, J. H., and Abraham, C. (2007) Inflammatory bowel disease genetics: Nod2. Annu. Rev. Med. 58, 401-416
5. Wang, Z. W., Ji, F., Teng, W. J., Yuan, X. G., and Ye, X. M. (2011) Risk factors and gene polymorphisms of inflammatory bowel disease in population of Zhejiang, China. World J. Gastroenterol. 17, 118-122
6. Hanauer, S. B. (2006) Inflammatory bowel disease: epidemiology, pathogenesis, and therapeutic opportunities. Inflamm. Bowel Dis. 12, Suppl. 1, S3-S9
7. Thoreson, R., and Cullen, J. J. (2007) Pathophysiology of inflammatory bowel disease: an overview. Surg. Clin. North Am. 87, 575-585
8. Heliö T., Halme, L., Lappalainen, M., Fodstad, H., Paavola-Sakki, P., Turunen, U., Fäkkilä M., Krusius, T., and Kontula, K. (2003) CARD15/NOD2 gene variants are associated with familially occurring and complicated forms of Crohn's disease. Gut 52, 558-562
9. Eckmann, L., and Karin, M. (2005)NOD2and Crohn's disease: loss or gain of function? Immunity 22, 661-667
10. Netea, M. G., Kullberg, B. J., de Jong, D. J., Franke, B., Sprong, T., Naber, T. H., Drenth, J. P., and Van der Meer, J. W. (2004) NOD2 mediates anti-inflammatory signals induced by TLR2 ligands: implications for Crohn's disease. Eur. J. Immunol. 34, 2052-2059
11. Rumbo, M., Courjault-Gautier, F., Sierro, F., Sirard, J. C., and Felley-Bosco, E. (2005) Polarized distribution of inducible nitric oxide synthase regulates activity in intestinal epithelial cells. FEBS J. 272, 444-453
12. Kolios, G., Valatas, V., and Ward, S. G. (2004) Nitric oxide in inflammatory bowel disease: a universal messenger in an unsolved puzzle. Immunology 113, 427-437
13. Beck, P. L., Li, Y., Wong, J., Chen, C. W., Keenan, C. M., Sharkey, K. A., and McCafferty, D. M. (2007) Inducible nitric oxide synthase from bone marrow-derived cells plays a critical role in regulating colonic inflammation. Gastroenterology 132, 1778-1790
14. Ozturk, H., Tuncer, M. C., Ozturk, H., and Buyukbayram, H. (2007) Nitric oxide regulates expression of Sonic hedgehog and hypoxia-inducible factor-1α in an experimental model of kidney ischemia-reperfusion. Ren. Fail. 29, 249-256
15. de Santa Barbara, P., van den Brink, G. R., and Roberts, D. J. (2003) Development and differentiation of the intestinal epithelium. Cell. Mol. Life Sci. 60, 1322-1332
16. van den Brink, G. R. (2007) Hedgehog signaling in development and homeostasis of the gastrointestinal tract. Physiol. Rev. 87, 1343-1375
17. Ghorpade, D. S., Holla, S., Kaveri, S. V., Bayry, J., Patil, S. A., and Balaji, K. N. (2013) Sonic hedgehog-dependent induction of MicroRNA 31 and MicroRNA 150 regulates Mycobacterium bovis BCG-driven Toll-like receptor 2 signaling. Mol. Cell. Biol. 33, 543-556
18. Zhou, X., Liu, Z., Jang, F., Xiang, C., Li, Y., and He, Y. (2012) Autocrine Sonic hedgehog attenuates inflammation in cerulein-induced acute pancreatitis in mice via upregulation of IL-10. PLoS One 7, e44121
19. Lees, C. W., Zacharias, W. J., Tremelling, M., Noble, C. L., Nimmo, E. R., Tenesa, A., Cornelius, J., Torkvist, L., Kao, J., Farrington, S., Drummond, H. E., Ho, G. T., Arnott, I. D., Appelman, H. D., Diehl, L., Campbell, H., Dunlop, M. G., Parkes, M., Howie, S. E., Gumucio, D. L., and Satsangi, J. (2008) Analysis of germline GLI1 variation implicates hedgehog signalling in the regulation of intestinal inflammatory pathways. PLoS Med. 5, e239
20. Varjosalo, M., and Taipale, J. (2008) Hedgehog: functions and mechanisms. Genes Dev. 22, 2454-2472
21. Bansal, K., and Balaji, K. N. (2011) Intracellular pathogen sensor NOD2 programs macrophages to trigger Notch1 activation. J. Biol. Chem. 286, 5823-5835
22. Brooks, M. N., Rajaram, M. V., Azad, A. K., Amer, A. O., Valdivia-Arenas, M. A., Park, J. H., Núñez, G., and Schlesinger, L. S. (2011) NOD2 controls the nature of the inflammatory response and subsequent fate of Mycobacterium tuberculosis and M. bovis BCG in human macrophages. Cell. Microbiol. 13, 402-418
23. Bansal, K., Trinath, J., Chakravortty, D., Patil, S. A., and Balaji, K. N. (2011) Pathogen-specific TLR2 protein activation programs macrophages to induce Wnt-β-catenin signaling. J. Biol. Chem. 286, 37032-37044
24. Pan, Q., Kravchenko, V., Katz, A., Huang, S., Ii, M., Mathison, J. C., Kobayashi, K., Flavell, R. A., Schreiber, R. D., Goeddel, D., and Ulevitch, R. J. (2006) NF-B-inducing kinase regulates selected gene expression in the Nod2 signaling pathway. Infect. Immun. 74, 2121-2127
25. Di Marcotullio, L., Ferretti, E., Greco, A., De Smaele, E., Po, A., Sico, M. A., Alimandi, M., Giannini, G., Maroder, M., Screpanti, I., and Gulino, A. (2006) Numb is a suppressor of Hedgehog signalling and targets Gli1 for Itch-dependent ubiquitination. Nat. Cell Biol. 8, 1415-1423
26. Stecca, B., Ruiz i Altaba, A. (2010) Context-dependent regulation of the GLI code in cancer by HEDGEHOG and non-HEDGEHOG signals. J. Mol. Cell Biol. 2, 84-95
27. Kuang, W., Tan, J., Duan, Y., Duan, J., Wang, W., Jin, F., Jin, Z., Yuan, X., and Liu, Y. (2009) Cyclic stretch induced miR-146a upregulation delays C2C12 myogenic differentiation through inhibition of Numb. Biochem. Biophys. Res. Commun. 378, 259-263
28. Schaefer, J. S., Montufar-Solis, D., Vigneswaran, N., and Klein, J. R. (2011) Selective upregulation of microRNA expression in peripheral blood leukocytes in IL-10-/- mice precedes expression in the colon. J. Immunol. 187, 5834-5841
29. Sohn, J. J., Schetter, A. J., Yfantis, H. G., Ridnour, L. A., Horikawa, I., Khan, M. A., Robles, A. I., Hussain, S. P., Goto, A., Bowman, E. D., Hofseth, L. J., Bartkova, J., Bartek, J., Wogan, G. N., Wink, D. A., and Harris, C. C. (2012) Macrophages, nitric oxide and microRNAs are associated withDNAdamage response pathway and senescence in inflammatory bowel disease. PLoS One 7, e44156
30. Perě, M., and Cerar, A. (2012) Dextran sodium sulphate colitis mouse model: traps and tricks. J. Biomed. Biotechnol. 2012, 718617
31. Waldner, M. J., and Neurath, M. F. (2009) Chemically induced mouse models of colitis. in Current Protocols in Pharmacol, Chapter 5, Unit 5 55, John Wiley & Sons, Inc., New York
32. Pilichos, C. J., Kouerinis, I. A., Zografos, G. C., Korkolis, D. P., Preza, A. A., Gazouli, M., Menenakos, E. I., Loutsidis, A. E., Zagouri, F., Gorgoulis, V. G., and Fotiadis, C. I. (2004) The effect of nitric oxide synthases inhibitors on inflammatory bowel disease in a rat model. In Vivo 18, 513-516
33. Ferrero-Miliani, L., Nielsen, O. H., Andersen, P. S., and Girardin, S. E. (2007) Chronic inflammation: importance of NOD2 and NALP3 in interleukin-1β generation. Clin. Exp. Immunol. 147, 227-235
34. Kufer, T. A., Banks, D. J., and Philpott, D. J. (2006) Innate immune sensing of microbes by Nod proteins. Ann. N.Y. Acad. Sci. 1072, 19-27
35. Richardson, W. M., Sodhi, C. P., Russo, A., Siggers, R. H., Afrazi, A., Gribar, S. C., Neal, M. D., Dai, S., Prindle, T., Jr., Branca, M., Ma, C., Ozolek, J., and Hackam, D. J. (2010) Nucleotide-binding oligomerization domain-2 inhibits Toll-like receptor-4 signaling in the intestinal epithelium. Gastroenterology 139, 904-917, 917.e901-906
36. Economou, M., Trikalinos, T. A., Loizou, K. T., Tsianos, E. V., and Ioannidis, J. P. (2004) Differential effects of NOD2 variants on Crohn's disease risk and phenotype in diverse populations: a metaanalysis. Am. J. Gastroenterol. 99, 2393-2404
37. Laroux, F. S., Lefer, D. J., Kawachi, S., Scalia, R., Cockrell, A. S., Gray, L., Van der Heyde, H., Hoffman, J. M., and Grisham, M. B. (2000) Role of nitric oxide in the regulation of acute and chronic inflammation. Antioxid. Redox Signal. 2, 391-396
38. Blantz, R. C., and Munger, K. (2002) Role of nitric oxide in inflammatory conditions. Nephron 90, 373-378
39. Cooke, J. P., and Dzau, V. J. (1997) Nitric oxide synthase: role in the genesis of vascular disease. Annu. Rev. Med. 48, 489-509
40. Reiter, C. D., and Gladwin, M. T. (2003) An emerging role for nitric oxide in sickle cell disease vascular homeostasis and therapy. Curr. Opin. Hematol. 10, 99-107
41. Nielsen, C. M., Williams, J., van den Brink, G. R., Lauwers, G. Y., and Roberts, D. J. (2004) Hh pathway expression in human gut tissues and in inflammatory gut diseases. Lab. Invest. 84, 1631-1642
42. El-Zaatari, M., Saqui-Salces, M., Waghray, M., Todisco, A., and Merchant, J. L. (2009) Sonic hedgehog in gastric physiology and neoplastic transformation: friend or foe? Curr. Opin. Endocrinol. Diabetes Obes. 16, 60-65
43. Iborra, M., Bernuzzi, F., Invernizzi, P., and Danese, S. (2012) MicroRNAs in autoimmunity and inflammatory bowel disease: crucial regulators in immune response. Autoimmun. Rev. 11, 305-314
44. Bauersachs, J., and Thum, T. (2011) Biogenesis and regulation of cardiovascular microRNAs. Circ. Res. 109, 334-347
45. Mathé E., Nguyen, G. H., Funamizu, N., He, P., Moake, M., Croce, C. M., and Hussain, S. P. (2012) Inflammation regulates microRNA expression in cooperation with p53 and nitric oxide. Int. J. Cancer 131, 760-765