Neurotensin signaling activates microRNAs-21 and -155 and Akt, promotes tumor growth in mice, and is increased in human colon tumors

Gastroenterology

Volumn 141, Issue 5, 2011, Pages 1749-1761.e1

  Bakirtzi, Kyriaki ^a   Hatziapostolou, Maria ^b,c   Karagiannides, Iordanes ^a   Polytarchou, Christos ^d   Jaeger, Savina ^e   Iliopoulos, Dimitrios ^b,c   Pothoulakis, Charalabos ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b DANA FARBER CANCER INSTITUTE   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d TUFTS MEDICAL CENTER   (United States)

^e NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

Colorectal Cancer; Neuropeptide; Signal Transduction; Tumor Suppressor

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MICRORNA; MICRORNA 155; MICRORNA 21; NEUROTENSIN; NEUROTENSIN RECEPTOR; NEUROTENSIN RECEPTOR 1; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PHOSPHOPROTEIN PHOSPHATASE 2A; PROTEIN KINASE B; SUPPRESSOR OF CYTOKINE SIGNALING 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BINDING SITE; BIOINFORMATICS; CANCER GROWTH; CARCINOGENESIS; COLON CANCER; COLON MUCOSA; CONTROLLED STUDY; GROWTH RATE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOBLOTTING; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TUMOR XENOGRAFT;

EID: 80054861706     PISSN: 00165085     EISSN: 15280012     Source Type: Journal    
DOI: 10.1053/j.gastro.2011.07.038     Document Type: Article

References (50)

1. Lagos-Quintana M, Rauhut R, Lendeckel W, et al. Identification of novel genes coding for small expressed RNAs. Science 2001;294:853-858. (Pubitemid 33032103)
2. McKenna LB, Schug J, Vourekas A, et al. MicroRNAs control intestinal epithelial differentiation, architecture, and barrier function. Gastroenterology 2010;139:1654-1664.
3. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009;136:215-233.
4. Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005;120:15-20. (Pubitemid 40094598)
5. Akao Y, Nakagawa Y, Naoe T. let-7 microRNA functions as a potential growth suppressor in human colon cancer cells. Biol Pharm Bull 2006;29:903-906.
6. Meltzer PS. Cancer genomics: small RNAs with big impacts. Nature 2005;435:745-746. (Pubitemid 40839710)
7. Lu J, Getz G, Miska EA, et al. MicroRNA expression profiles classify human cancers. Nature 2005;435:834-838. (Pubitemid 40839735)
8. Iliopoulos D, Jaeger SA, Hirsch HA, et al. STAT3 activation of miR-21 and miR-181b-1 via PTEN and CYLD are part of the epigenetic switch linking inflammation to cancer. Mol Cell 2010;39:493-506.
9. Carraway R, Leeman SE. The isolation of a new hypotensive peptide, neurotensin, from bovine hypothalami. J Biol Chem 1973;248:6854-6861.
10. Carraway R, Leeman SE. Characterization of radioimmunoassayable neurotensin in the rat. Its differential distribution in the central nervous system, small intestine, and stomach. J Biol Chem 1976;251:7045-7052.
11. Zhao D, Zhan Y, Koon HW, et al. Metalloproteinase-dependent transforming growth factor-alpha release mediates neurotensin-stimulated MAP kinase activation in human colonic epithelial cells. J Biol Chem 2004;279:43547-43554. (Pubitemid 39390655)
12. Tasuta M, Iishi H, Baba M, et al. Enhancement by neurotensin of experimental carcinogenesis induced in rat colon by azoxymethane. Br J Cancer 1990;62:368-371. (Pubitemid 20292828)
13. Maoret JJ, Anini Y, Rouyer-Fessard C, et al. 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 1999;80:448-454. (Pubitemid 29019635)
14. Castagliuolo I, Wang CC, Valenick L, et al. Neurotensin is a proinflammatory neuropeptide in colonic inflammation. J Clin Invest 1999;103:843-849. (Pubitemid 29152630)
15. Koon HW, Kim YS, Xu H, et al. Neurotensin induces IL-6 secretion in mouse preadipocytes and adipose tissues during 2,4,6,-trinitrobenzensulphonic acid-induced colitis. Proc Natl Acad Sci U S A 2009;106:8766-8771.
16. Nielsen BS, Jorgensen S, Fog JU, et al. High levels of microRNA-21 in the stroma of colorectal cancers predict short disease-free survival in stage II colon cancer patients. Clin Exp Metastasis 2011;28:27-38.
17. Wang XY, Wu MH, Liu F, et al. Differential miRNA expression and their target genes between NGX6-positive and negative colon cancer cells. Mol Cell Biochem 2010;345:283-290.
18. Zhao D, Keates AC, Kuhnt-Moore S, et al. Signal transduction pathways mediating neurotensin-stimulated interleukin-8 expression in human colonocytes. J Biol Chem 2001;276:44464-44471.
19. Naldini L, Blomer U, Gage FH, et al. Efficient transfer, integration, and sustained long-term expression of the transgene in adult rat brains injected with a lentiviral vector. Proc Natl Acad Sci U S A 1996;93:11382-11388. (Pubitemid 26347130)
20. Warner JB, Philippakis AA, Jaeger SA, et al. Systematic identification of mammalian regulatory motifs' target genes and functions. Nat Methods 2008;5:347-353. (Pubitemid 351459368)
21. Yang A, Zhu Z, Kapranov P, et al. Relationships between p63 binding, DNA sequence, transcription activity, and biological function in human cells. Mol Cell 2006;24:593-602. (Pubitemid 350284225)
22. Iliopoulos D, Lindahl-Allen M, Polytarchou C, et al. Loss of miR-200 inhibition of Suz12 leads to polycomb-mediated repression required for the formation and maintenance of cancer stem cells. Mol Cell 2010;39:761-772.
23. Zhao D, Bakirtzi K, Zhan Y, et al. Insulin-like growth factor-1 receptor transactivation modulates the inflammatory and proliferative response of neurotensin in human colonic epithelial cells. J Biol Chem 2011;286:6092-6099.
24. Jiang S, Zhang HW, Lu MH, et al. MicroRNA-155 functions as an OncomiR in breast cancer by targeting the suppressor of cytokine signaling 1 gene. Cancer Res 2010;70:3119-3127.
25. Hassan S, Dobner PR, Carraway RE. Involvement of MAP-kinase, PI3-kinase and EGF-receptor in the stimulatory effect of neurotensin on DNA synthesis in PC3 cells. Regul Pept 2004;120:155-166. (Pubitemid 38726205)
26. Resjo S, Goransson O, Harndahl L, et al. Protein phosphatase 2A is the main phosphatase involved in the regulation of protein kinase B in rat adipocytes. Cell Signal 2002;14:231-238. (Pubitemid 34102452)
27. Ozes ON, Mayo LD, Gustin JA, et al. NF-kappaB activation by tumour necrosis factor requires the Akt serine-threonine kinase. Nature 1999;401:82-85.
28. Zhang JG, Wang JJ, Zhao F, et al. MicroRNA-21 (miR-21) represses tumor suppressor PTEN and promotes growth and invasion in non-small cell lung cancer (NSCLC). Clin Chim Acta 2010;411:846-852.
29. Liang Z, Wu H, Reddy S, et al. Blockade of invasion and metastasis of breast cancer cells via targeting CXCR4 with an artificial microRNA. Biochem Biophys Res Commun 2007;363:542-546. (Pubitemid 47513664)
30. Taby R, Issa JP. Cancer epigenetics. CA Cancer J Clin 2010;60:376-392.
31. Petrocca F, Visone R, Onelli MR, et al. E2F1-regulated microRNAs impair TGFbeta-dependent cell-cycle arrest and apoptosis in gastric cancer. Cancer Cell 2008;13:272-286. (Pubitemid 351318375)
32. Volinia S, Calin GA, Liu CG, et al. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci U S A 2006;103:2257-2261. (Pubitemid 43271657)
33. Michael MZ, SM OC, van Holst Pellekaan NG, et al. Reduced accumulation of specific microRNAs in colorectal neoplasia. Mol Cancer Res 2003;1:882-891.
34. Saito Y, Suzuki H, Hibi T. The role of microRNAs in gastrointestinal cancers. J Gastroenterol 2009;44(Suppl 19):18-22.
35. Castagliuolo I, Leeman SE, Bartolak-Suki E, et al. A neurotensin antagonist, SR 48692, inhibits colonic responses to immobilization stress in rats. Proc Natl Acad Sci U S A 1996;93: 12611-12615. (Pubitemid 26367192)
36. Brun P, Mastrotto C, Beggiao E, et al. Neuropeptide neurotensin stimulates intestinal wound healing following chronic intestinal inflammation. Am J Physiol Gastrointest Liver Physiol 2005;288:G621-G629. (Pubitemid 40388173)
37. Gross KJ, Pothoulakis C. Role of neuropeptides in inflammatory bowel disease. Inflamm Bowel Dis 2007;13:918-932. (Pubitemid 47203871)
38. Wang X, Wang Q, Ives KL, et al. Curcumin inhibits neurotensin-mediated interleukin-8 production and migration of HCT116 human colon cancer cells. Clin Cancer Res 2006;12:5346-5355. (Pubitemid 44497247)
39. Thompson RC, Herscovitch M, Zhao I, et al. NF-kappaB downregulates expression of the B-lymphoma marker CD10 through a miR-155/PU.1 pathway. J Biol Chem 2011;286:1675-1682.
40. Shin VY, Jin H, Ng EK, et al. NF-kappaB targets miR-16 and miR-21 in gastric cancer: involvement of prostaglandin E receptors. Carcinogenesis 2011;32:240-245.
41. Takagi T, Naito Y, Mizushima K, et al. Increased expression of microRNA in the inflamed colonic mucosa of patients with active ulcerative colitis. J Gastroenterol Hepatol 2010;25(Suppl 1):S129-S133.
42. Wu F, Zhang S, Dassopoulos T, et al. Identification of microRNAs associated with ileal and colonic Crohn's disease. Inflamm Bowel Dis 2010;16:1729-1738.
43. Staal SP. Molecular cloning of the akt oncogene and its human homologues AKT1 and AKT2: amplification of AKT1 in a primary human gastric adenocarcinoma. Proc Natl Acad Sci U S A 1987;84:5034-5037. (Pubitemid 17095859)
44. Vivanco I, Sawyers CL. The phosphatidylinositol 3-Kinase AKT pathway in human cancer. Nat Rev Cancer 2002;2:489-501. (Pubitemid 37328931)
45. Ugi S, Imamura T, Maegawa H, et al. Protein phosphatase 2A negatively regulates insulin's metabolic signaling pathway by inhibiting Akt (protein kinase B) activity in 3T3-L1 adipocytes. Mol Cell Biol 2004;24:8778-8789. (Pubitemid 39245095)
46. Iliopoulos D, Hirsch HA, Struhl K. An epigenetic switch involving NF-kappaB, Lin28, Let-7 MicroRNA, and IL6 links inflammation to cell transformation. Cell 2009;139:693-706.
47. Kent OA, Chivukula RR, Mullendore M, et al. Repression of the miR-143/145 cluster by oncogenic Ras initiates a tumor-promoting feed-forward pathway. Genes Dev 2010;24:2754-2759.
48. Evers BM, Ishizuka J, Chung DH, et al. Neurotensin expression and release in human colon cancers. Ann Surg 1992;216:423-431.
49. Chao C, Tallman ML, Ives KL, et al. Gastrointestinal hormone receptors in primary human colorectal carcinomas. J Surg Res 2005;129:313-321. (Pubitemid 41797070)
50. Bossard C, Souaze F, Jarry A, et al. Over-expression of neurotensin high-affinity receptor 1 (NTS1) in relation with its ligand neurotensin (NT) and nuclear beta-catenin in inflammatory bowel disease-related oncogenesis. Peptides 2007;28:2030-2035. (Pubitemid 47419096)