p53-responsive miR-194 inhibits thrombospondin-1 and promotes angiogenesis in colon cancers

Cancer Research

Volumn 71, Issue 24, 2011, Pages 7490-7501

  Sundaram, Prema ^a   Hultine, Stacy ^a   Smith, Lauren M ^b   Dews, Michael ^a   Fox, Jamie L ^a,b   Biyashev, Dauren ^d   Schelter, Janell M ^e   Huang, Qihong ^b,c   Cleary, Michele A ^e   Volpert, Olga V ^d   Thomas Tikhonenko, Andrei ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c WISTAR INSTITUTE   (United States)

^d NORTHWESTERN UNIVERSITY   (United States)

^e ROSETTA INPHARMATICS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DICER; MATRIGEL; MESSENGER RNA; MICRORNA; MICRORNA 194; PROTEIN P53; RAS PROTEIN; RETROVIRUS VECTOR; THROMBOSPONDIN 1; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL PARAMETERS; BLOOD VESSEL SIZE; CANCER GROWTH; CELL STRAIN HCT116; COLON CARCINOGENESIS; COLON CARCINOMA; COLORECTAL CARCINOMA; CONTROLLED STUDY; GAIN OF FUNCTION MUTATION; GASTROINTESTINAL TRACT; GENE; GENE ACTIVATION; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE OVEREXPRESSION; GENETIC TRANSDUCTION; GROWTH INHIBITION; ISCHEMIA; MICROVASCULAR DENSITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; THBS1 GENE; TISSUE REPAIR; TRANSCRIPTION REGULATION; TUMOR VASCULARIZATION; TUMOR XENOGRAFT; UPREGULATION;

3' UNTRANSLATED REGIONS; ANIMALS; BLOTTING, WESTERN; CELL LINE, TUMOR; COLONIC NEOPLASMS; GENE EXPRESSION REGULATION, NEOPLASTIC; HCT116 CELLS; HUMANS; MICE; MICRORNAS; MUTATION; NEOVASCULARIZATION, PATHOLOGIC; RETROVIRIDAE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; THROMBOSPONDIN 1; TRANSCRIPTION, GENETIC; TRANSDUCTION, GENETIC; TRANSPLANTATION, HETEROLOGOUS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84255170428     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-11-1124     Document Type: Article

References (50)

1. Jimenez B, Volpert OV, Crawford SE, Febbraio M, Silverstein RL, Bouck N. Signals leading to apoptosis-dependent inhibition of neovascularization by thrombospondin-1. Nat Med 2000;6:41-8. (Pubitemid 30048524)
2. Dawson DW, Pearce SF, Zhong R, Silverstein RL, Frazier WA, Bouck NP. CD36 mediates the in vitro inhibitory effects of thrombospondin-1 on endothelial cells. J Cell Biol 1997;138:707-17. (Pubitemid 27349849)
3. Short SM, Derrien A, Narsimhan RP, Lawler J, Ingber DE, Zetter BR. Inhibition of endothelial cell migration by thrombospondin-1 type-1 repeats is mediated by beta1 integrins. J Cell Biol 2005;168:643-53. (Pubitemid 40271029)
4. Rodriguez-Manzaneque JC, Lane TF, Ortega MA, Hynes RO, Lawler J, Iruela-Arispe ML. Thrombospondin-1 suppresses spontaneous tumor growth and inhibits activation of matrix metalloproteinase-9 and mobilization of vascular endothelial growth factor. Proc Natl Acad Sci U S A 2001;98:12485-90. (Pubitemid 33019972)
5. Greenaway J, Lawler J, Moorehead R, Bornstein P, Lamarre J, Petrik J. Thrombospondin-1 inhibits VEGF levels in the ovary directly by binding and internalization via the low density lipoprotein receptor-related protein-1 (LRP-1). J Cell Physiol 2007;210:807-18. (Pubitemid 46185050)
6. Weinstat-Saslow DL, Zabrenetzky VS, VanHoutte K, Frazier WA, Roberts DD, Steeg PS. Transfection of thrombospondin 1 complementary DNA into a human breast carcinoma cell line reduces primary tumor growth, metastatic potential, and angiogenesis. Cancer Res 1994;54:6504-11.
7. Zaslavsky A, Baek KH, Lynch RC, Short S, Grillo J, Folkman J, et al. Platelet-derived thrombospondin-1 is a critical negative regulator and potential biomarker of angiogenesis. Blood 2010;115:4605-13.
8. Dameron KM, Volpert OV, Tainsky MA, Bouck N. Control of angiogenesis in fibroblasts by p53 regulation of thrombospondin-1. Science 1994;265:1582-4. (Pubitemid 24308973)
9. Volpert OV, Dameron KM, Bouck N. Sequential development of an angiogenic phenotype by human fibroblasts progressing to tumorigenicity. Oncogene 1997;14:1495-502. (Pubitemid 27182439)
10. Wen S, Stolarov J, Myers MP, Su JD, Wigler MH, Tonks NK, et al. PTEN controls tumor-induced angiogenesis. Proc Natl Acad Sci U S A 2001;98:4622-7. (Pubitemid 32295026)
11. Schwarte-Waldhoff I, Volpert OV, Bouck NP, Sipos B, Hahn SA, Klein-Scory S, et al. Smad4/DPC4-mediated tumor suppression through suppression of angiogenesis. Proc Natl Acad Sci U S A 2000;97:9624-9. (Pubitemid 30650826)
12. Janz A, Sevignani C, Kenyon K, Ngo C, Thomas-Tikhonenko A. Activation of the Myc oncoprotein leads to increased turnover of thrombospondin-1 mRNA. Nucl Acids Res 2000;28:2268-5.
13. Tikhonenko AT, Black DJ, Linial ML. Viral Myc oncoproteins in infected fibroblasts down-modulate thrombospondin-1, a possible tumor suppressor gene. J Biol Chem 1996;271:30741-7. (Pubitemid 26404093)
14. Watnick RS, Cheng YN, Rangarajan A, Ince TA, Weinberg RA. Ras modulates Myc activity to repress thrombospondin-1 expression and increase tumor angiogenesis. Cancer Cell 2003;3:219-31. (Pubitemid 37443878)
15. Slack JL, Bornstein P. Transformation by v-src causes transient induction followed by repression of mouse thrombospondin-1. Cell Growth Differ 1994;5:1373-80. (Pubitemid 24381526)
16. Dejong V, Degeorges A, Filleur S, Ait SA, Mettouchi A, Bornstein P, et al. The Wilms' tumor gene product represses the transcription of thrombospondin 1 in response to overexpression of c-Jun. Oncogene 1999;18:3143-51. (Pubitemid 29261235)
17. Teodoro JG, Evans SK, Green MR. p53 and angiogenesis. In: Thomas-Tikhonenko A, editor. Cancer genome and tumor microenvironment. 1st ed. New York, Dordrecht, Heidelberg, London: Springer; 2011. p. 189-216.
18. Giuriato S, Ryeom S, Fan AC, Bachireddy P, Lynch RC, Rioth MJ, et al. Sustained regression of tumors upon MYCinactivation requires p53 or thrombospondin-1 to reverse the angiogenic switch. Proc Natl Acad Sci U S A 2006;103:16266-71. (Pubitemid 44715185)
19. Gasparini G, Toi M, Biganzoli E, Dittadi R, Fanelli M, Morabito A, et al. Thrombospondin-1 and -2 in node-negative breast cancer: correlation with angiogenic factors, p53, cathepsin D, hormone receptors and prognosis. Oncology 2001;60:72-80. (Pubitemid 32041435)
20. Linderholm B, Karlsson E, Klaar S, Lindahl T, Borg AL, Elmberger G, et al. Thrombospondin-1 expression in relation to p53 status and VEGF expression in human breast cancers. Eur J Cancer 2004;40:2417-23. (Pubitemid 39424955)
21. Grossfeld GD, Carroll PR, Lindeman N, Meng M, Groshen S, Feng AC, et al. Thrombospondin-1 expression in patients with pathologic stage T3 prostate cancer undergoing radical prostatectomy: association with p53 alterations, tumor angiogenesis, and tumor progression. Urology 2002;59:97-102. (Pubitemid 34059314)
22. Kawahara N, Ono M, Taguchi K, Okamoto M, Shimada M, Takenaka K, et al. Enhanced expression of thrombospondin-1 and hypovascularity in human cholangiocarcinoma. Hepatology 1998;28:1512-7. (Pubitemid 28549120)
23. Tokunaga T, Nakamura M, Oshika Y, Tsuchida T, Kazuno M, Fukushima Y, et al. Alterations in tumour suppressor gene p53 correlate with inhibition of thrombospondin-1 gene expression in colon cancer cells. Virchows Arch 1998;433:415-8. (Pubitemid 28522029)
24. Rojas A, Meherem S, Kim YH, Washington MK, Willis JE, Markowitz SD, et al. The aberrant methylation of TSP1 suppresses TGF-beta1 activation in colorectal cancer. Int J Cancer 2008;123:14-21. (Pubitemid 351705187)
25. Laderoute KR, Alarcon RM, Brody MD, Calaoagan JM, Chen EY, Knapp AM, et al. Opposing effects of hypoxia on expression of the angiogenic inhibitor thrombospondin 1 and the angiogenic inducer vascular endothelial growth factor. Clin Cancer Res 2000;6:2941-50. (Pubitemid 30482137)
26. Cinatl J Jr, Kotchetkov R, Scholz M, Cinatl J, Vogel JU, Driever PH, et al. Human cytomegalovirus infection decreases expression of thrombospondin-1 independent of the tumor suppressor protein p53. Am J Pathol 1999;155:285-92. (Pubitemid 29318726)
27. Dews M, Homayouni A, Yu D, Murphy D, Sevignani C, Wentzel E, et al. Augmentation of tumor angiogenesis by a Myc-activated microRNA cluster. Nat Genet 2006;38:1060-5. (Pubitemid 44325933)
28. Kuehbacher A, Urbich C, Zeiher AM, Dimmeler S. Role of Dicer and Drosha for endothelial microRNA expression and angiogenesis. Circ Res 2007;101:59-68. (Pubitemid 47094624)
29. Braun CJ, Zhang X, Savelyeva I, Wolff S, Moll UM, Schepeler T, et al. p53-Responsive microRNAs 192 and 215 are capable of inducing cell cycle arrest. Cancer Res 2008;68:10094-104.
30. Pichiorri F, Suh SS, Rocci A, De LL, Taccioli C, Santhanam R, et al. Downregulation of p53-inducible microRNAs 192, 194, and 215 impairs the p53/MDM2 autoregulatory loop in multiple myeloma development. Cancer Cell 2010;18:367-81.
31. Cummins JM, He Y, Leary RJ, Pagliarini R, Diaz LA Jr, Sjoblom T, et al. The colorectal microRNAome. Proc Natl Acad Sci U S A 2006;103:3687-92. (Pubitemid 43376616)
32. Linsley PS, Schelter J, Burchard J, Kibukawa M, Martin MM, Bartz SR, et al. Transcripts targeted by the microRNA-16 family cooperatively regulate cell cycle progression. Mol Cell Biol 2007;27:2240-52. (Pubitemid 46418479)
33. Dews M, Fox JL, Hultine S, Sundaram P, Wang W, Liu YY, et al. The Myc-mir-17 ∼92 axis blunts TGFb signaling and production of multiple TGFb-dependent antiangiogenic factors. Cancer Res 2010;70:8233-46.
34. Biyashev D, Veliceasa D, Kwiatek A, Sutanto MM, Cohen RN, Volpert OV. Natural angiogenesis inhibitor signals through Erk5 activation of peroxisome proliferator-activated receptor gamma (PPARgamma). J Biol Chem 2010;285:13517-24.
35. Rhodes DR, Kalyana-Sundaram S, Mahavisno V, Varambally R, Yu J, Briggs BB, et al. Oncomine 3.0: genes, pathways, and networks in a collection of 18,000 cancer gene expression profiles. Neoplasia 2007;9:166-80.
36. Vassilev LT, Vu BT, Graves B, Carvajal D, Podlaski F, Filipovic Z, et al. In vivo activation of the p53 pathway by small-molecule antagonists of MDM2. Science 2004;303:844-8. (Pubitemid 38174664)
37. Suarez Y, Fernandez-Hernando C, Yu J, Gerber SA, Harrison KD, Pober JS, et al. Dicer-dependent endothelial microRNAs are necessary for postnatal angiogenesis. Proc Natl Acad Sci U S A 2008;105:14082-7.
38. Maragkakis M, Reczko M, Simossis VA, Alexiou P, Papadopoulos GL, Dalamagas T, et al. DIANA-microT web server: elucidating microRNA functions through target prediction. Nucleic Acids Res 2009;37:W273-6.
39. Grimson A, Farh KK, Johnston WK, Garrett-Engele P, Lim LP, Bartel DP. MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol Cell 2007;27:91-105. (Pubitemid 46991392)
40. Doebele C, Bonauer A, Fischer A, Scholz A, Reiss Y, Urbich C, et al. Members of the microRNA-17-92 cluster exhibit a cell-intrinsic antiangiogenic function in endothelial cells. Blood 2010;115:4944-50.
41. Liang Y, Ridzon D, Wong L, Chen C. Characterization of microRNA expression profiles in normal human tissues. BMC Genomics 2007;8:166.
42. Hino K, Tsuchiya K, Fukao T, Kiga K, Okamoto R, Kanai T, et al. Inducible expression of microRNA-194 is regulated by HNF-1alpha during intestinal epithelial cell differentiation. RNA 2008;14:1433-42. (Pubitemid 351872199)
43. Krutzfeldt J, Rosch N, Hausser J, Manoharan M, Zavolan M, Stoffel M. MicroRNA-194 is a target of transcription factor 1 (Tcf1, Hnf1alpha) in adult liver and controls expression of frizzled-6. Hepatology 2011.
44. He L, He X, Lowe SW, Hannon GJ. microRNAs join the p53 network - another piece in the tumour-suppression puzzle. Nat Rev Cancer 2007;7:819-22. (Pubitemid 350006254)
45. Mestdagh P, Bostrom AK, Impens F, Fredlund E, Van PG, De AP, et al. The miR-17-92 microRNA cluster regulates multiple components of the TGF-β pathway in neuroblastoma. Mol Cell 2010;40:762-73.
46. Chang TC, Yu D, Lee YS, Wentzel EA, Arking DE, West KM, et al. Widespread microRNA repression by Myc contributes to tumorigenesis. Nat Genet 2008;40:43-50.
47. Carden DL, Granger DN. Pathophysiology of ischaemia-reperfusion injury. J Pathol 2000;190:255-66. (Pubitemid 30141372)
48. Wu B, Qiu W, Wang P, Yu H, Cheng T, Zambetti GP, et al. p53 independent induction of PUMA mediates intestinal apoptosis in response to ischaemia-reperfusion. Gut 2007;56:645-54. (Pubitemid 46662930)
49. Meng Z, Fu X, Chen X, Zeng S, Tian Y, Jove R, et al. miR-194 is a marker of hepatic epithelial cells and suppresses metastasis of liver cancer cells in mice. Hepatology 2010;52:2148-57.
50. Sotillo E, Thomas-Tikhonenko A. Shielding the messenger (RNA): microRNA-based anticancer therapies. Pharmacol Ther 2011;131:18-32.