Neurotensin promotes the development of colitis and intestinal angiogenesis via Hif-1α-MIR-210 signaling

Journal of Immunology

Volumn 196, Issue 10, 2016, Pages 4311-4321

  Bakirtzi, Kyriaki ^a   Law, Ivy Ka Man ^a   Xue, Xiang ^b   Iliopoulos, Dimitrios ^a   Shah, Yatrik M ^b   Pothoulakis, Charalabos ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 [BIS(2 CHLOROETHYL)OXIDOAMINO]PHENYLALANINE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; LOCKED NUCLEIC ACID; MICRORNA 210; NEUROTENSIN; NEUROTENSIN RECEPTOR; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; SMALL INTERFERING RNA; TRINITROBENZENESULFONIC ACID; 2-AMINO-3-(4'-N,N-BIS(2-CHLOROETHYL)AMINO)PHENYLPROPIONIC ACID N-OXIDE; HIF1A PROTEIN, HUMAN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MICRORNA; MIRN210 MICRORNA, HUMAN; MUSTARD GAS DERIVATIVE; NEUROTENSIN TYPE 1 RECEPTOR; PHENYLPROPIONIC ACID DERIVATIVE;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DISEASE EXACERBATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; INTESTINAL TISSUE; INTESTINE EPITHELIUM CELL; MALE; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; ULCERATIVE COLITIS; WILD TYPE; ANIMAL; C57BL MOUSE; COLON; DRUG EFFECTS; EPITHELIUM CELL; GENETICS; INTESTINE MUCOSA; KNOCKOUT MOUSE; METABOLISM; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; TUMOR CELL LINE; UPREGULATION; VASCULARIZATION;

ANIMALS; CELL LINE, TUMOR; COLITIS, ULCERATIVE; COLON; EPITHELIAL CELLS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INTESTINAL MUCOSA; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICRORNAS; MUSTARD COMPOUNDS; NEOVASCULARIZATION, PATHOLOGIC; NEUROTENSIN; NF-KAPPA B; PHENYLPROPIONATES; RECEPTORS, NEUROTENSIN; SIGNAL TRANSDUCTION; TRINITROBENZENESULFONIC ACID; UP-REGULATION;

EID: 84975073422     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1501443     Document Type: Article

References (51)

1. Taylor, C. T., and S. P. Colgan. 2007. Hypoxia and gastrointestinal disease. J. Mol. Med. 85: 1295-1300.
2. Colgan, S. P., and C. T. Taylor. 2010. Hypoxia: an alarm signal during intestinal inflammation. Nat. Rev. Gastroenterol. Hepatol. 7: 281-287.
3. Furuta, G. T., J. R. Turner, C. T. Taylor, R. M. Hershberg, K. Comerford, S. Narravula, D. K. Podolsky, and S. P. Colgan. 2001. Hypoxia-inducible factor 1-dependent induction of intestinal trefoil factor protects barrier function during hypoxia. J. Exp. Med. 193: 1027-1034.
4. Semenza, G. L. 2003. Angiogenesis in ischemic and neoplastic disorders. Annu. Rev. Med. 54: 17-28.
5. Feinman, R., E. A. Deitch, A. C. Watkins, B. Abungu, I. Colorado, K. B. Kannan, S. U. Sheth, F. J. Caputo, Q. Lu, M. Ramanathan, et al. 2010. HIF-1 mediates pathogenic inflammatory responses to intestinal ischemia-reperfusion injury. Am. J. Physiol. Gastrointest. Liver Physiol. 299: G833-G843.
6. Scharte, M., K. Jurk, B. Kehrel, A. Zarbock, H. Van Aken, and K. Singbartl. 2006. IL-4 enhances hypoxia induced HIF-1αlpha protein levels in human transformed intestinal cells. FEBS Lett. 580: 6399-6404.
7. Hellwig-Bürgel, T., D. P. Stiehl, A. E. Wagner, E. Metzen, and W. Jelkmann. 2005. Review: hypoxia-inducible factor-1 (HIF-1): a novel transcription factor in immune reactions. J. Interferon Cytokine Res. 25: 297-310.
8. Bakirtzi, K., G. West, C. Fiocchi, I. K. Law, D. Iliopoulos, and C. Pothoulakis. 2014. The neurotensin-HIF-1α-VEGFa axis orchestrates hypoxia, colonic inflammation, and intestinal angiogenesis. Am. J. Pathol. 184: 3405-3414.
9. Castagliuolo, I., C. C. Wang, L. Valenick, A. Pasha, S. Nikulasson, R. E. Carraway, and C. Pothoulakis. 1999. Neurotensin is a proinflammatory neuropeptide in colonic inflammation. J. Clin. Invest. 103: 843-849.
10. Koon, H. W., Y. S. Kim, H. Xu, A. Kumar, D. Zhao, I. Karagiannides, P. R. Dobner, and C. Pothoulakis. 2009. Neurotensin induces IL-6 secretion in mouse preadipocytes and adipose tissues during 2, 4, 6,-trinitrobenzensulphonic acid-induced colitis. Proc. Natl. Acad. Sci. USA 106: 8766-8771.
11. Brun, P., C. Mastrotto, E. Beggiao, A. Stefani, L. Barzon, G. C. Sturniolo, G. Palù, and I. Castagliuolo. 2005. Neuropeptide neurotensin stimulates intestinal wound healing following chronic intestinal inflammation. Am. J. Physiol. Gastrointest. Liver Physiol. 288: G621-G629.
12. Maoret, J. J., Y. Anini, C. Rouyer-Fessard, D. Gully, and M. Laburthe. 1999. Neurotensin and a non-peptide neurotensin receptor antagonist control human colon cancer cell growth in cell culture and in cells xenografted into nude mice. Int. J. Cancer 80: 448-454.
13. Tasuta, M., H. Iishi, M. Baba, and H. Taniguchi. 1990. Enhancement by neurotensin of experimental carcinogenesis induced in rat colon by azoxymethane. Br. J. Cancer 62: 368-371.
14. McKenna, L. B., J. Schug, A. Vourekas, J. B. McKenna, N. C. Bramswig, J. R. Friedman, and K. H. Kaestner. 2010. MicroRNAs control intestinal epithelial differentiation, architecture, and barrier function. Gastroenterology 139: 1654-1664, 1664.e1.
15. Bartel, D. P. 2009. MicroRNAs: target recognition and regulatory functions. Cell 136: 215-233.
16. Bakirtzi, K., M. Hatziapostolou, I. Karagiannides, C. Polytarchou, S. Jaeger, D. Iliopoulos, and C. Pothoulakis. 2011. Neurotensin signaling activates microRNAs-21 and-155 and Akt, promotes tumor growth in mice, and is increased in human colon tumors. Gastroenterology 141: 1749-1761.e1.
17. Law, I. K., K. Bakirtzi, C. Polytarchou, A. Oikonomopoulos, D. Hommes, D. Iliopoulos, and C. Pothoulakis. 2015. Neurotensin-regulated miR-133a is involved in proinflammatory signalling in human colonic epithelial cells and in experimental colitis. Gut 64: 1095-1104.
18. Kulshreshtha, R., M. Ferracin, S. E. Wojcik, R. Garzon, H. Alder, F. J. Agosto-Perez, R. Davuluri, C. G. Liu, C. M. Croce, M. Negrini, et al. 2007. A microRNA signature of hypoxia. Mol. Cell. Biol. 27: 1859-1867.
19. Huang, X., Q. T. Le, and A. J. Giaccia. 2010. MiR-210-micromanager of the hypoxia pathway. Trends Mol. Med. 16: 230-237.
20. Devlin, C., S. Greco, F. Martelli, and M. Ivan. 2011. miR-210: more than a silent player in hypoxia. IUBMB Life 63: 94-100.
21. Xue, X., S. Ramakrishnan, E. Anderson, M. Taylor, E. M. Zimmermann, J. R. Spence, S. Huang, J. K. Greenson, and Y. M. Shah. 2013. Endothelial PAS domain protein 1 activates the inflammatory response in the intestinal epithelium to promote colitis in mice. Gastroenterology 145: 831-841.
22. Shah, Y. M., T. Matsubara, S. Ito, S. H. Yim, and F. J. Gonzalez. 2009. Intestinal hypoxia-inducible transcription factors are essential for iron absorption following iron deficiency. Cell Metab. 9: 152-164.
23. Zhao, D., A. C. Keates, S. Kuhnt-Moore, M. P. Moyer, C. P. Kelly, and C. Pothoulakis. 2001. Signal transduction pathways mediating neurotensinstimulated interleukin-8 expression in human colonocytes. J. Biol. Chem. 276: 44464-44471.
24. Castagliuolo, I., O. Morteau, A. C. Keates, L. Valenick, C. C. Wang, J. Zacks, B. Lu, N. P. Gerard, and C. Pothoulakis. 2002. Protective effects of neurokinin-1 receptor during colitis in mice: role of the epidermal growth factor receptor. Br. J. Pharmacol. 136: 271-279.
25. Zhao, D., S. Kuhnt-Moore, H. Zeng, J. S. Wu, M. P. Moyer, and C. Pothoulakis. 2003. Neurotensin stimulates IL-8 expression in human colonic epithelial cells through Rho GTPase-mediated NF-kappa B pathways. Am. J. Physiol. Cell Physiol. 284: C1397-C1404.
26. Zhao, D., Y. Zhan, H. Zeng, H. W. Koon, M. P. Moyer, and C. Pothoulakis. 2005. Neurotensin stimulates interleukin-8 expression through modulation of I kappa B alpha phosphorylation and p65 transcriptional activity: involvement of protein kinase C alpha. Mol. Pharmacol. 67: 2025-2031.
27. Huang, X., L. Ding, K. L. Bennewith, R. T. Tong, S. M. Welford, K. K. Ang, M. Story, Q. T. Le, and A. J. Giaccia. 2009. Hypoxia-inducible mir-210 regulates normoxic gene expression involved in tumor initiation. Mol. Cell 35: 856-867.
28. Berra, E., E. Benizri, A. Ginouvès, V. Volmat, D. Roux, and J. Pouysségur. 2003. HIF prolyl-hydroxylase 2 is the key oxygen sensor setting low steady-state levels of HIF-1αlpha in normoxia. EMBO J. 22: 4082-4090.
29. Zhao, D., K. Bakirtzi, Y. Zhan, H. Zeng, H. W. Koon, and C. Pothoulakis. 2011. Insulin-like growth factor-1 receptor transactivation modulates the inflammatory and proliferative responses of neurotensin in human colonic epithelial cells. J. Biol. Chem. 286: 6092-6099.
30. Fasanaro, P., Y. D'Alessandra, V. Di Stefano, R. Melchionna, S. Romani, G. Pompilio, M. C. Capogrossi, and F. Martelli. 2008. MicroRNA-210 modulates endothelial cell response to hypoxia and inhibits the receptor tyrosine kinase ligand Ephrin-A3. J. Biol. Chem. 283: 15878-15883.
31. Zhao, D., Y. Zhan, H. Zeng, H. W. Koon, M. P. Moyer, and C. Pothoulakis. 2007. Neurotensin stimulates expression of early growth response gene-1 and EGF receptor through MAP kinase activation in human colonic epithelial cells. Int. J. Cancer 120: 1652-1656.
32. Zhao, D., Y. Zhan, H. W. Koon, H. Zeng, S. Keates, M. P. Moyer, and C. Pothoulakis. 2004. Metalloproteinase-dependent transforming growth factoralpha release mediates neurotensin-stimulated MAP kinase activation in human colonic epithelial cells. J. Biol. Chem. 279: 43547-43554.
33. Bugni, J. M., L. A. Rabadi, K. Jubbal, I. Karagiannides, G. Lawson, and C. Pothoulakis. 2012. The neurotensin receptor-1 promotes tumor development in a sporadic but not an inflammation-associated mouse model of colon cancer. Int. J. Cancer 130: 1798-1805.
34. Chan, Y. C., J. Banerjee, S. Y. Choi, and C. K. Sen. 2012. miR-210: the master hypoxamir. Microcirculation 19: 215-223.
35. Kokura, S., N. Yoshida, and T. Yoshikawa. 2002. Anoxia/reoxygenation-induced leukocyte-endothelial cell interactions. Free Radic. Biol. Med. 33: 427-432.
36. Kiga, K., H. Mimuro, M. Suzuki, A. Shinozaki-Ushiku, T. Kobayashi, T. Sanada, M. Kim, M. Ogawa, Y. W. Iwasaki, H. Kayo, et al. 2014. Epigenetic silencing of miR-210 increases the proliferation of gastric epithelium during chronic Helicobacter pylori infection. Nat. Commun. 5: 4497.
37. Qi, J., Y. Qiao, P. Wang, S. Li, W. Zhao, and C. Gao. 2012. microRNA-210 negatively regulates LPS-induced production of proinflammatory cytokines by targeting NF-κB1 in murine macrophages. FEBS Lett. 586: 1201-1207.
38. Lorenzen, J. M., J. T. Kielstein, C. Hafer, S. K. Gupta, P. Kümpers, R. Faulhaber-Walter, H. Haller, D. Fliser, and T. Thum. 2011. Circulating miR-210 predicts survival in critically ill patients with acute kidney injury. Clin. J. Am. Soc. Nephrol. 6: 1540-1546.
39. Zhao, M., L. T. Wang, G. P. Liang, P. Zhang, X. J. Deng, Q. Tang, H. Y. Zhai, C. C. Chang, Y. W. Su, and Q. J. Lu. 2014. Up-regulation of microRNA-210 induces immune dysfunction via targeting FOXP3 in CD4(+) T cells of psoriasis vulgaris. Clin. Immunol. 150: 22-30.
40. Bruning, U., L. Cerone, Z. Neufeld, S. F. Fitzpatrick, A. Cheong, C. C. Scholz, D. A. Simpson, M. O. Leonard, M. M. Tambuwala, E. P. Cummins, and C. T. Taylor. 2011. MicroRNA-155 promotes resolution of hypoxia-inducible factor 1alpha activity during prolonged hypoxia. Mol. Cell. Biol. 31: 4087-4096.
41. Ke, Q., and M. Costa. 2006. Hypoxia-inducible factor-1 (HIF-1). Mol. Pharmacol. 70: 1469-1480.
42. Chan, S. Y., and J. Loscalzo. 2010. MicroRNA-210: a unique and pleiotropic hypoxamir. Cell Cycle 9: 1072-1083.
43. McCormick, R. I., C. Blick, J. Ragoussis, J. Schoedel, D. R. Mole, A. C. Young, P. J. Selby, R. E. Banks, and A. L. Harris. 2013. miR-210 is a target of hypoxiainducible factors 1 and 2 in renal cancer, regulates ISCU and correlates with good prognosis. Br. J. Cancer 108: 1133-1142.
44. Cicchillitti, L., V. Di Stefano, E. Isaia, L. Crimaldi, P. Fasanaro, V. Ambrosino, A. Antonini, M. C. Capogrossi, C. Gaetano, G. Piaggio, and F. Martelli. 2012. Hypoxia-inducible factor 1-α induces miR-210 in normoxic differentiating myoblasts. J. Biol. Chem. 287: 44761-44771.
45. Libermann, T. A., and D. Baltimore. 1990. Activation of interleukin-6 gene expression through the NF-kappa B transcription factor. Mol. Cell. Biol. 10: 2327-2334.
46. Collart, M. A., P. Baeuerle, and P. Vassalli. 1990. Regulation of tumor necrosis factor alpha transcription in macrophages: involvement of four kappa B-like motifs and of constitutive and inducible forms of NF-kappa B. Mol. Cell. Biol. 10: 1498-1506.
47. Dong, Z., X. Qi, and I. J. Fidler. 1993. Tyrosine phosphorylation of mitogenactivated protein kinases is necessary for activation of murine macrophages by natural and synthetic bacterial products. J. Exp. Med. 177: 1071-1077.
48. Chauhan, D., S. Kharbanda, H. Uchiyama, M. Urashima, R. Fragoso, J. Sen, D. W. Kufe, and K. C. Anderson. 1994. Identification of upstream signals regulating interleukin-6 gene expression during in vitro treatment of human B cells with pokeweed mitogen. Blood 84: 2243-2252.
49. Kopriva, S. E., V. L. Chiasson, B. M. Mitchell, and P. Chatterjee. 2013. TLR3-induced placental miR-210 down-regulates the STAT6/interleukin-4 pathway. PLoS One 8: e67760.
50. Zhou, H., J. X. Chen, C. S. Yang, M. Q. Yang, Y. Deng, and H. Wang. 2014. Gene regulation mediated by microRNAs in response to green tea polyphenol EGCG in mouse lung cancer. BMC Genomics 15(Suppl. 11): S3.
51. Karhausen, J., G. T. Furuta, J. E. Tomaszewski, R. S. Johnson, S. P. Colgan, and V. H. Haase. 2004. Epithelial hypoxia-inducible factor-1 is protective in murine experimental colitis. J. Clin. Invest. 114: 1098-1106.