Dysregulated CRTC1 activity is a novel component of PGE2 signaling that contributes to colon cancer growth

Oncogene

Volumn 35, Issue 20, 2016, Pages 2602-2614

  Schumacher, Y ^a,b,c   Aparicio, T ^d   Ourabah, S ^a,b,c   Baraille, F ^a,b,c   Martin, A ^d   Wind, P ^d   Dentin, R ^a,b,c   Postic, C ^a,b,c   Guilmeau, S ^a,b,c  

^a INSTITUT COCHIN   (France)

^b CNRS   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d Universite Paris   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CALCINEURIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN REGULATORED TRANSCRIPTION COACTIVATOR 1; CYCLOOXYGENASE 2; CYCLOOXYGENASE 2 INHIBITOR; DEXTRAN SULFATE; INTERLEUKIN 6; METHANE; PROSTAGLANDIN E2; UNCLASSIFIED DRUG; CRTC1 PROTEIN, HUMAN; PROSTAGLANDIN E RECEPTOR 1; PROSTAGLANDIN E RECEPTOR 2; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR AP 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER CELL LINE; CANCER GROWTH; CELL DIVISION; CELL VIABILITY; COLON CANCER; COLON CARCINOGENESIS; CONTROLLED STUDY; ENZYME ACTIVATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN DEPHOSPHORYLATION; SIGNAL TRANSDUCTION; CARCINOGENESIS; CELL PROLIFERATION; COLON TUMOR; METABOLISM; PATHOLOGY; TUMOR CELL LINE;

CARCINOGENESIS; CELL LINE, TUMOR; CELL PROLIFERATION; COLONIC NEOPLASMS; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DINOPROSTONE; HUMANS; RECEPTORS, PROSTAGLANDIN E, EP1 SUBTYPE; RECEPTORS, PROSTAGLANDIN E, EP2 SUBTYPE; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR AP-1; TRANSCRIPTION FACTORS;

EID: 84940054644     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2015.283     Document Type: Article

References (59)

1. Canettieri G, Coni S, Della Guardia M, Nocerino V, Antonucci L, Di Magno L et al. The coactivator CRTC1 promotes cell proliferation and transformation via AP-1. Proc Natl Acad Sci USA 2009; 106: 1445-1450.
2. Iourgenko V, Zhang W, Mickanin C, Daly I, Jiang C, Hexham JM et al. Identification of a family of cAMP response element-binding protein coactivators by genomescale functional analysis in mammalian cells. Proc Natl Acad Sci USA 2003; 100: 12147-12152.
3. Altarejos JY, Montminy M. CREB and the CRTC co-activators: sensors for hormonal and metabolic signals. Nat Rev Mol Cell Biol 2011; 12: 141-151.
4. Siu YT, Ching YP, Jin DY. Activation of TORC1 transcriptional coactivator through MEKK1-induced phosphorylation. Mol Biol Cell 2008; 19: 4750-4761.
5. Breuillaud L, Rossetti C, Meylan EM, Merinat C, Halfon O, Magistretti PJ et al. Deletion of CREB-regulated transcription coactivator 1 induces pathological aggression, depression-related behaviors, neuroplasticity genes dysregulation in mice. Biol Psychiatry 2012; 72: 528-536.
6. Ch'ng TH, Uzgil B, Lin P, Avliyakulov NK, O'Dell TJ, Martin KC. Activity-dependent transport of the transcriptional coactivator CRTC1 from synapse to nucleus. Cell 2012; 150: 207-221.
7. Finsterwald C, Martin JL. Cellular mechanisms underlying the regulation of dendritic development by hepatocyte growth factor. Eur J Neurosci 2011; 34: 1053-1061.
8. Sakamoto K, Norona FE, Alzate-Correa D, Scarberry D, Hoyt KR, Obrietan K. Clock and light regulation of the CREB coactivator CRTC1 in the suprachiasmatic circadian clock. J Neurosci 2013; 33: 9021-9027.
9. Sekeres MJ, Mercaldo V, Richards B, Sargin D, Mahadevan V, Woodin MA et al. Increasing CRTC1 function in the dentate gyrus during memory formation or reactivation increases memory strength without compromising memory quality. J Neurosci 2012; 32: 17857-17868.
10. Wu Z, Huang X, Feng Y, Handschin C, Feng Y, Gullicksen PS et al. Transducer of regulated CREB-binding proteins (TORCs) induce PGC-1alpha transcription and mitochondrial biogenesis in muscle cells. Proc Natl Acad Sci USA 2006; 103: 14379-14384.
11. Altarejos JY, Goebel N, Conkright MD, Inoue H, Xie J, Arias CM et al. The Creb1 coactivator Crtc1 is required for energy balance and fertility. Nat Med 2008; 14: 1112-1117.
12. Choong E, Quteineh L, Cardinaux JR, Gholam-Rezaee M, Vandenberghe F, Dobrinas M et al. Influence of CRTC1 polymorphisms on body mass index and fat mass in psychiatric patients and the general adult population. JAMA Psychiatry 2013; 70: 1011-1019.
13. Eberhard CE, Fu A, Reeks C, Screaton RA. CRTC2 is required for beta-cell function and proliferation. Endocrinology 2013; 154: 2308-2317.
14. Kim SJ, Nian C, Widenmaier S, McIntosh CH. Glucose-dependent insulinotropic polypeptide-mediated up-regulation of beta-cell antiapoptotic Bcl-2 gene expression is coordinated by cyclic AMP (cAMP) response element binding protein (CREB) and cAMP-responsive CREB coactivator 2. Mol Cell Biol 2008; 28: 1644-1656.
15. Muraoka M, Fukushima A, Viengchareun S, Lombes M, Kishi F, Miyauchi A et al. Involvement of SIK2/TORC2 signaling cascade in the regulation of insulin-induced PGC-1alpha and UCP-1 gene expression in brown adipocytes. Am J Physiol Endocrinol Metab 2009; 296: E1430-E1439.
16. Enlund F, Behboudi A,ren Y, Oberg C, Lendahl U, Mark J et al. Altered Notch signaling resulting from expression of a WAMTP1-MAML2 gene fusion in mucoepidermoid carcinomas and benign Warthin's tumors. Exp Cell Res 2004; 292: 21-28.
17. Tonon G, Modi S, Wu L, Kubo A, Coxon AB, Komiya T et al. t(11;19)(q21;p13) translocation in mucoepidermoid carcinoma creates a novel fusion product that disrupts a Notch signaling pathway. Nat Genet 2003; 33: 208-213.
18. Chen Z, Chen J, Gu Y, Hu C, Li JL, Lin S et al. Aberrantly activated AREG-EGFR signaling is required for the growth and survival of CRTC1-MAML2 fusion-positive mucoepidermoid carcinoma cells. Oncogene 2013; 33: 3869-3877.
19. Coxon A, Rozenblum E, Park YS, Joshi N, Tsurutani J, Dennis PA et al. Mect1-Maml2 fusion oncogene linked to the aberrant activation of cyclic AMP/CREB regulated genes. Cancer Res 2005; 65: 7137-7144.
20. Wu L, Liu J, Gao P, Nakamura M, Cao Y, Shen H et al. Transforming activity of MECT1-MAML2 fusion oncoprotein is mediated by constitutive CREB activation. EMBO J 2005; 24: 2391-2402.
21. Feng Y, Wang Y, Wang Z, Fang Z, Li F, Gao Y et al. The CRTC1-NEDD9 signaling axis mediates lung cancer progression caused by LKB1 loss. Cancer Res 2012; 72: 6502-6511.
22. Gu Y, Lin S, Li JL, Nakagawa H, Chen Z, Jin B et al. Altered LKB1/CREB-regulated transcription co-activator (CRTC) signaling axis promotes esophageal cancer cell migration and invasion. Oncogene 2012; 31: 469-479.
23. Kovacs KA, Steullet P, Steinmann M, Do KQ, Magistretti PJ, Halfon O et al. TORC1 is a calcium-and cAMP-sensitive coincidence detector involved in hippocampal long-term synaptic plasticity. Proc Natl Acad Sci USA 2007; 104: 4700-4705.
24. Bittinger MA, McWhinnie E, Meltzer J, Iourgenko V, Latario B, Liu X et al. Activation of cAMP response element-mediated gene expression by regulated nuclear transport of TORC proteins. Curr Biol 2004; 14: 2156-2161.
25. Conkright MD, Canettieri G, Screaton R, Guzman E, Miraglia L, Hogenesch JB et al. TORCs: transducers of regulated CREB activity. Mol Cell 2003; 12: 413-423.
26. Komiya T, Coxon A, Park Y, Chen WD, Zajac-Kaye M, Meltzer P et al. Enhanced activity of the CREB co-activator Crtc1 in LKB1 null lung cancer. Oncogene 2010; 29: 1672-1680.
27. Yamada Y, Mori H. Multistep carcinogenesis of the colon in Apc(Min/+) mouse. Cancer Sci 2007; 98: 6-10.
28. Chell S, Kaidi A, Williams AC, Paraskeva C. Mediators of PGE2 synthesis and signalling downstream of COX-2 represent potential targets for the prevention/treatment of colorectal cancer. Biochim Biophys Acta 2006; 1766: 104-119.
29. Kutchera W, Jones DA, Matsunami N, Groden J, McIntyre TM, Zimmerman GA et al. Prostaglandin H synthase 2 is expressed abnormally in human colon cancer: evidence for a transcriptional effect. Proc Natl Acad Sci USA 1996; 93: 4816-4820.
30. Sinicrope FA, Lemoine M, Xi L, Lynch PM, Cleary KR, Shen Y et al. Reduced expression of cyclooxygenase 2 proteins in hereditary nonpolyposis colorectal cancers relative to sporadic cancers. Gastroenterology 1999; 117: 350-358.
31. Park SW, Kim HS, Choi MS, Jeong WJ, Heo DS, Kim KH et al. The effects of the stromal cell-derived cyclooxygenase-2 metabolite prostaglandin E2 on the proliferation of colon cancer cells. J Pharmacol Exp Ther 2011; 336: 516-523.
32. Guzman MJ, Shao J, Sheng H. Pro-neoplastic effects of amphiregulin in colorectal carcinogenesis. J Gastrointest Cancer 2013; 44: 211-221.
33. Holla VR, Wu H, Shi Q, Menter DG, DuBois RN. Nuclear orphan receptor NR4A2 modulates fatty acid oxidation pathways in colorectal cancer. J Biol Chem 2011; 286: 30003-30009.
34. Nagasaki T, Hara M, Nakanishi H, Takahashi H, Sato M, Takeyama H. Interleukin-6 released by colon cancer-associated fibroblasts is critical for tumour angiogenesis: anti-interleukin-6 receptor antibody suppressed angiogenesis and inhibited tumour-stroma interaction. Br J Cancer 2014; 110: 469-478.
35. Waldner MJ, Foersch S, Neurath MF. Interleukin-6-a key regulator of colorectal cancer development. Int J Biol Sci 2012; 8: 1248-1253.
36. Wang D, Dubois RN. The role of COX-2 in intestinal inflammation and colorectal cancer. Oncogene 2010; 29: 781-788.
37. Zagani R, Hamzaoui N, Cacheux W, de Reynies A, Terris B, Chaussade S et al. Cyclooxygenase-2 inhibitors down-regulate osteopontin and Nr4A2-new therapeutic targets for colorectal cancers. Gastroenterology 2009; 137: e1351-e1353.
38. Liu Y, Dentin R, Chen D, Hedrick S, Ravnskjaer K, Schenk S et al. A fasting inducible switch modulates gluconeogenesis via activator/coactivator exchange. Nature 2008; 456: 269-273.
39. Ravnskjaer K, Kester H, Liu Y, Zhang X, Lee D, Yates JR 3rd et al. Cooperative interactions between CBP and TORC2 confer selectivity to CREB target gene expression. EMBO J 2007; 26: 2880-2889.
40. Dentin R, Liu Y, Koo SH, Hedrick S, Vargas T, Heredia J et al. Insulin modulates gluconeogenesis by inhibition of the coactivator TORC2. Nature 2007; 449: 366-369.
41. MacKenzie KF, Clark K, Naqvi S, McGuire VA, Noehren G, Kristariyanto Y et al. PGE(2) induces macrophage IL-10 production and a regulatory-like phenotype via a protein kinase A-SIK-CRTC3 pathway. J Immunol 2013; 190: 565-577.
42. Samarajeewa NU, Docanto MM, Simpson ER, Brown KA. CREB-regulated transcription co-activator family stimulates promoter II-driven aromatase expression in preadipocytes. Horm Cancer 2013; 4: 233-241.
43. Rasmuson A, Kock A, Fuskevag OM, Kruspig B, Simon-Santamaria J, Gogvadze V et al. Autocrine prostaglandin E2 signaling promotes tumor cell survival and proliferation in childhood neuroblastoma. PLoS One 2012; 7: e29331.
44. Sonoshita M, Takaku K, Sasaki N, Sugimoto Y, Ushikubi F, Narumiya S et al. Acceleration of intestinal polyposis through prostaglandin receptor EP2 in Apc (Delta 716) knockout mice. Nat Med 2001; 7: 1048-1051.
45. Cao C, Gao R, Zhang M, Amelio AL, Fallahi M, Chen Z et al. Role of LKB1-CRTC1 on glycosylated COX-2 and response to COX-2 inhibition in lung cancer. J Natl Cancer Inst 2015; 107: 358.
46. De Leng WW, Westerman AM, Weterman MA, De Rooij FW, Dekken HvH, De Goeij AF et al. Cyclooxygenase 2 expression and molecular alterations in Peutz-Jeghers hamartomas and carcinomas. Clin Cancer Res 2003; 9: 3065-3072.
47. Takeda H, Miyoshi H, Tamai Y, Oshima M, Taketo MM. Simultaneous expression of COX-2 and mPGES-1 in mouse gastrointestinal hamartomas. Br J Cancer 2004; 90: 701-704.
48. Hu M, Peluffo G, Chen H, Gelman R, Schnitt S, Polyak K. Role of COX-2 in epithelialstromal cell interactions and progression of ductal carcinoma in situ of the breast. Proc Natl Acad Sci USA 2009; 106: 3372-3377.
49. Konstantinopoulos PA, Vandoros GP, Karamouzis MV, Gkermpesi M, Sotiropoulou-Bonikou G, Papavassiliou AG. EGF-R is expressed and AP-1 and NF-kappaB are activated in stromal myofibroblasts surrounding colon adenocarcinomas paralleling expression of COX-2 and VEGF. Cell Oncol 2007; 29: 477-482.
50. Clark K, MacKenzie KF, Petkevicius K, Kristariyanto Y, Zhang J, Choi HG et al. Phosphorylation of CRTC3 by the salt-inducible kinases controls the interconversion of classically activated and regulatory macrophages. Proc Natl Acad Sci USA 2012; 109: 16986-16991.
51. Alvarez Y, Municio C, Alonso S, Sanchez Crespo M, Fernandez N. The induction of IL-10 by zymosan in dendritic cells depends on CREB activation by the coactivators CREB-binding protein and TORC2 and autocrine PGE2. J Immunol 2009; 183: 1471-1479.
52. Kuhn R, Lohler J, Rennick D, Rajewsky K, Muller W. Interleukin-10-deficient mice develop chronic enterocolitis. Cell 1993; 75: 263-274.
53. Shouval DS, Ouahed J, Biswas A, Goettel JA, Horwitz BH, Klein C et al. Interleukin 10 receptor signaling: master regulator of intestinal mucosal homeostasis in mice and humans. Adv Immunol 2014; 122: 177-210.
54. Galizia G, Orditura M, Romano C, Lieto E, Castellano P, Pelosio L et al. Prognostic significance of circulating IL-10 and IL-6 serum levels in colon cancer patients undergoing surgery. Clin Immunol 2002; 102: 169-178.
55. Mocellin S, Marincola FM, Young HA. Interleukin-10 and the immune response against cancer: a counterpoint. J Leukoc Biol 2005; 78: 1043-1051.
56. Li B, Alli R, Vogel P, Geiger TL. IL-10 modulates DSS-induced colitis through a macrophage-ROS-NO axis. Mucosal Immunol 2014; 7: 869-878.
57. Gunderson LL, Jessup JM, Sargent DJ, Greene FL, Stewart AK. Revised TN categorization for colon cancer based on national survival outcomes data. J Clin Oncol 2010; 28: 264-271.
58. Suzawa T, Miyaura C, Inada M, Maruyama T, Sugimoto Y, Ushikubi F et al. The role of prostaglandin E receptor subtypes (EP1, EP2, EP3, EP4) in bone resorption: an analysis using specific agonists for the respective EPs. Endocrinology 2000; 141: 1554-1559.
59. Kucharzik T, Lugering N, Winde G, Domschke W, Stoll R. Colon carcinoma cell lines stimulate monocytes and lamina propria mononuclear cells to produce IL-10. Clin Exp Immunol 1997; 110: 296-302.