Colorectal carcinogenesis: Connecting K-RAS-induced transformation and CREB activity in vitro and in vivo

Molecular Cancer Research

Volumn 13, Issue 8, 2015, Pages 1248-1262

  Steven, André ^a   Heiduk, Max ^a   Recktenwald, Christian V ^a   Hiebl, Bernhard ^a   Wickenhauser, Claudia ^a   Massa, Chiara ^a   Seliger, Barbara ^a  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; APC PROTEIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; K RAS PROTEIN; KG 501; MATRIX METALLOPROTEINASE; MESSENGER RNA; PROTEIN P53; SHORT HAIRPIN RNA; SMAD4 PROTEIN; UNCLASSIFIED DRUG; CREB1 PROTEIN, HUMAN; CREB1 PROTEIN, MOUSE; RAS PROTEIN; SMALL INTERFERING RNA;

3T3 CELL LINE; ANCHORAGE INDEPENDENT GROWTH; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CANCER GROWTH; CELL CYCLE PROGRESSION; CELL MIGRATION; COLORECTAL CARCINOMA; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; GENE EXPRESSION; GENE MUTATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TUMOR GROWTH; TUMOR SUPPRESSOR GENE; UPREGULATION; WESTERN BLOTTING; ANIMAL; CARCINOMA; CELL CYCLE; CELL MOTION; CELL PROLIFERATION; CELL TRANSFORMATION; COLORECTAL TUMOR; DNA SEQUENCE; FIBROBLAST; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; METABOLISM; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; MUTATION; ONCOGENE RAS; TUMOR CELL LINE; TUMOR INVASION;

ANIMALS; APOPTOSIS; CARCINOMA; CELL CYCLE; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; COLORECTAL NEOPLASMS; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; FIBROBLASTS; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; GENES, RAS; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MITOCHONDRIA; MUTATION; NEOPLASM INVASIVENESS; PHENOTYPE; RAS PROTEINS; RNA, MESSENGER; RNA, SMALL INTERFERING; SEQUENCE ANALYSIS, DNA; SIGNAL TRANSDUCTION;

EID: 84942474681     PISSN: 15417786     EISSN: 15573125     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-14-0590     Document Type: Article

References (49)

1. Kwok RP, Lundblad JR, Chrivia JC, Richards JP, Bachinger HP, Brennan RG, et al. Nuclear protein CBP is a coactivator for the transcription factor CREB. Nature 1994;370:223-6.
2. Radhakrishnan I, Perez-Alvarado GC, Parker D, Dyson HJ, Montminy MR, Wright PE. Solution structure of the KIX domain of CBP bound to the transactivation domain of CREB: a model for activator: coactivator interactions. Cell 1997;91:741-52.
3. Crans-Vargas HN, Landaw EM, Bhatia S, Sandusky G, Moore TB, Sakamoto KM. Expression of cyclic adenosine monophosphate response-element binding protein in acute leukemia. Blood 2002;99:2617-9.
4. Impey S, McCorkle SR, Cha-Molstad H, Dwyer JM, Yochum GS, Boss JM, et al. Defining the CREB regulon: a genome-wide analysis of transcription factor regulatory regions. Cell 2004;119:1041-54.
5. Mayr B, Montminy M. Transcriptional regulation by the phosphorylationdependent factor CREB. Nat Rev Mol Cell Biol 2001;2:599-609.
6. Finkbeiner S. New roles for introns: sites of combinatorial regulation of Ca2+- and cyclic AMP-dependent gene transcription. Sci STKE 2001;2001:pe1.
7. Melnikova VO, Mourad-Zeidan AA, Lev DC, Bar-Eli M. Platelet-activating factor mediates MMP-2 expression and activation via phosphorylation of cAMP-response element-binding protein and contributes to melanoma metastasis. J Biol Chem 2006;281:2911-22.
8. Wen AY, Sakamoto KM, Miller LS. The role of the transcription factor CREB in immune function. J Immunol 2010;185:6413-9.
9. White PC, Shore AM, Clement M, McLaren J, Soeiro I, Lam EW, et al. Regulation of cyclin D2and the cyclin D2promoter by protein kinase Aand CREB in lymphocytes. Oncogene 2006;25:2170-80.
10. Zhang X, Odom DT, Koo SH, Conkright MD, Canettieri G, Best J, et al. Genome-wide analysis of cAMP-response element binding protein occupancy, phosphorylation, and target gene activation in human tissues. Proc Natl Acad Sci U S A 2005;102:4459-64.
11. Siu YT, Jin DY. CREB - A real culprit in oncogenesis. FEBS J 2007;274:3224-32.
12. Abramovitch R, Tavor E, Jacob-Hirsch J, Zeira E, Amariglio N, Pappo O, et al. A pivotal role of cyclic AMP-responsive element binding protein in tumor progression. Cancer Res 2004;64:1338-46.
13. Antonescu CR, Nafa K, Segal NH, Dal Cin P, Ladanyi M. EWS-CREB1: a recurrent variant fusion in clear cell sarcoma-association with gastrointestinal location and absence of melanocytic differentiation. Clin Cancer Res 2006;12:5356-62.
14. Jean D, Bar-Eli M. Regulation of tumor growth and metastasis of human melanoma by the CREB transcription factor family. Mol Cell Biochem 2000;212:19-28.
15. Cheng JC, Kinjo K, Judelson DR, Chang J, Wu WS, Schmid I, et al. CREB is a critical regulator of normal hematopoiesis and leukemogenesis. Blood 2008;111:1182-92.
16. Sakamoto KM, Frank DA. CREB in the pathophysiology of cancer: implications for targeting transcription factors for cancer therapy. Clin Cancer Res 2009;15:2583-7.
17. Melnikova VO, Dobroff AS, Zigler M, Villares GJ, Braeuer RR, Wang H, et al. CREB inhibits AP-2alpha expression to regulate the malignant phenotype of melanoma. PLoS One 2010;5:e12452.
18. Aggarwal S, Kim SW, Ryu SH, Chung WC, Koo JS. Growth suppression of lung cancer cells by targeting cyclicAMPresponse element-binding protein. Cancer Res 2008;68:981-8.
19. Best JL, Amezcua CA, Mayr B, Flechner L, Murawsky CM, Emerson B, et al. Identification of small-molecule antagonists that inhibit an activator: coactivator interaction. Proc Natl Acad Sci U S A 2004;101:17622-7.
20. Li BX, Xiao X. Discovery of a small-molecule inhibitor of the KIX-KID interaction. Chembiochem 2009;10:2721-4.
21. Wei J, Yan W, Li X, Chang WC, Tai HH. Activation of thromboxane receptor alpha induces expression of cyclooxygenase-2 through multiple signaling pathways in A549 human lung adenocarcinoma cells. Biochem Pharmacol 2007;74:787-800.
22. Gupta R, Wajapeyee N. Induction of cellular senescence by oncogenic RAS. Methods Mol Biol 2013;1048:127-33.
23. Campbell PM, der CJ. Oncogenic Ras and its role in tumor cell invasion and metastasis. Semin Cancer Biol 2004;14:105-14.
24. Giehl K. Oncogenic Ras in tumour progression and metastasis. Biol Chem 2005;386:193-205.
25. Fernandez-Medarde A, Santos E. Ras in cancer and developmental diseases. Genes Cancer 2011;2:344-58.
26. Forbes SA, Bindal N, Bamford S, Cole C, Kok CY, Beare D, et al. COSMIC: mining complete cancer genomes in the Catalogue of Somatic Mutations in Cancer. Nucleic Acids Res 2011;39:D945-50.
27. Li Z, Jin K, Lan H, Teng L. Heterogeneity in primary colorectal cancer and its corresponding metastases: a potential reason of EGFR-targeted therapy failure? Hepatogastroenterology 2011;58:411-6.
28. Recktenwald CV, Kellner R, Lichtenfels R, Seliger B. Altered detoxification status and increased resistance to oxidative stress by K-ras transformation. Cancer Res 2008;68:10086-93.
29. Seliger B, Harders C, Lohmann S, Momburg F, Urlinger S, Tampe R, et al. Down-regulation of the MHC class I antigen-processing machinery after oncogenic transformation of murine fibroblasts. Eur J Immunol 1998;28:122-33.
30. Wulfaenger J, Niedling S, Riemann D, Seliger B. Aminopeptidase N (APN)/CD13-dependent CXCR4 downregulation is associated with diminished cell migration, proliferation and invasion. Mol Membr Biol 2008;25:72-82.
31. Ronaghi M. Pyrosequencing sheds light on DNA sequencing. Genome Res 2001;11:3-11.
32. Recktenwald CV, Mendler S, Lichtenfels R, Kellner R, Seliger B. Influence of Ki-ras-driven oncogenic transformation on the protein network of murine fibroblasts. Proteomics 2007;7:385-98.
33. Steven A, Leisz S, Massa C, Iezzi M, Lattanzio R, Lamolinara A, et al. HER-2/neu mediates oncogenic transformation via altered CREB expression and function. Mol Cancer Res 2013;11:1462-77.
34. Snoek-van Beurden PA, Von den Hoff JW. Zymographic techniques for the analysis of matrix metalloproteinases and their inhibitors. Biotechniques 2005;38:73-83.
35. De Bosscher K, Hill CS, Nicolás FJ. Molecular and functional consequences of Smad4 C-terminal missense mutations in colorectal tumour cells. Biochem J 2004;379(Pt 1):209-16.
36. Zhang L, Duan CJ, Binkley C, Li G, Uhler MD, Logsdon CD, et al. A transforming growth factor b-induced Smad3/Smad4 complex directly activates protein kinase A. Mol Cell Biol 2004;24:2169-80.
37. Riemann A, Schneider B, Ihling A, Nowak M, Sauvant C, Thews O, et al. Acidic environment leads to ROS-induced MAPK signaling in cancer cells. PLoS One 2011;6:e22445.
38. Xiao X, Li BX, Mitton B, Ikeda A, Sakamoto KM. Targeting CREB for cancer therapy: friend or foe. Curr Cancer Drug Targets 2010;10:384-91.
39. Pylayeva-Gupta Y, Grabocka E, Bar-Sagi D. RAS oncogenes: weaving a tumorigenic web. Nat Rev Cancer 2011;11:761-74.
40. Mullighan CG, Zhang J, Kasper LH, Lerach S, Payne-Turner D, Phillips LA, et al. CREBBP mutations in relapsed acute lymphoblastic leukaemia. Nature 2011;471:235-9.
41. Murray D, Morrin M, McDonnell S. Increased invasion and expression of MMP-9 in human colorectal cell lines by a CD44-dependent mechanism. Anticancer Res 2004;24:489-94.
42. Shi Y, Liu R, Zhang S, Xia YY, Yang HJ, Guo K, et al. Neural cell adhesion molecule potentiates invasion and metastasis of melanoma cells through CAMP-dependent protein kinase and phosphatidylinositol 3-kinase pathways. Int J Biochem Cell Biol 2011;43:682-90.
43. Satpathy M, Shao M, Emerson R, Donner DB, Matei D. Tissue transglutaminase regulates matrix metalloproteinase-2 in ovarian cancer by modulating cAMP-response element-binding protein activity. J Biol Chem 2009;284:15390-9.
44. Xie S, Price JE, Luca M, Jean D, Ronai Z, Bar-Eli M. Dominant-negative CREB inhibits tumor growth and metastasis of human melanoma cells. Oncogene 1997;15:2069-75.
45. Park JK, Park SH, So K, Bae IH, Yoo YD, Um HD. ICAM-3 enhances the migratory and invasive potential of human non-small cell lung cancer cells by inducing MMP-2 and MMP-9 via Akt and CREB. Int J Oncol 2010;36:181-92.
46. Rozenberg J, Rishi V, Orosz A, Moitra J, Glick A, Vinson C. Inhibition of CREB function in mouse epidermis reduces papilloma formation. Mol Cancer Res 2009;7:654-64.
47. Aucoin R, Reiland J, Roy M, Marchetti D. Dominant-negative CREB inhibits heparanase functionality and melanoma cell invasion. J Cell Biochem 2004;93:215-23.
48. Son J, Lee JH, Kim HN, Ha H, Lee ZH. cAMP-response-elementbinding protein positively regulates breast cancer metastasis and subsequent bone destruction. Biochem Biophys Res Commun 2010;398:309-14.
49. Seo HS, Liu DD, Bekele BN, Kim MK, Pisters K, Lippman SM, et al. Cyclic AMP response element-binding protein overexpression: a feature associated with negative prognosis in never smokers with non-small cell lung cancer. Cancer Res 2008;68:6065-73.