Tumor suppressive microRNA-137 negatively regulates Musashi-1 and colorectal cancer progression

Oncotarget

Volumn 6, Issue 14, 2015, Pages 12558-12573

  Smith, Amber R ^a   Marquez, Rebecca T ^a   Tsao, Wei Chung ^a   Pathak, Surajit ^c   Roy, Alexandria ^a   Ping, Jie ^c   Wilkerson, Bailey ^a   Lan, Lan ^a   Meng, Wenjian ^c   Neufeld, Kristi L ^a,d   Sun, Xiao Feng ^c   Xu, Liang ^a,b  

^a UNIVERSITY OF KANSAS   (United States)

^b UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

^c LINKÖPING UNIVERSITY   (Sweden)

^d UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

Colon cancer; MicroRNAs; Rectal cancer; RNA binding proteins; Tumor initiating cells

Indexed keywords

MICRORNA; MICRORNA 137; NOTCH RECEPTOR; PROTEIN MSI1; RNA BINDING PROTEIN; UNCLASSIFIED DRUG; WNT PROTEIN; MIRN137 MICRORNA, HUMAN; MSI1 PROTEIN, HUMAN; NERVE PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CANCER INHIBITION; COLONY FORMATION; COLORECTAL CANCER; COLORECTAL CANCER CELL LINE; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOBLOTTING; IN VITRO STUDY; IN VIVO STUDY; LUCIFERASE ASSAY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN INTERACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TUMOR XENOGRAFT; ANIMAL; BIOSYNTHESIS; COLORECTAL TUMOR; DISEASE COURSE; GENE EXPRESSION REGULATION; GENETICS; HCT 116 CELL LINE; IMMUNOHISTOCHEMISTRY; NUDE MOUSE; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; TISSUE MICROARRAY; TUMOR SUPPRESSOR GENE; WESTERN BLOTTING; XENOGRAFT;

ANIMALS; BLOTTING, WESTERN; COLORECTAL NEOPLASMS; DISEASE PROGRESSION; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, TUMOR SUPPRESSOR; HCT116 CELLS; HETEROGRAFTS; HUMANS; IMMUNOHISTOCHEMISTRY; MICE; MICE, NUDE; MICRORNAS; NERVE TISSUE PROTEINS; REAL-TIME POLYMERASE CHAIN REACTION; RNA-BINDING PROTEINS; TISSUE ARRAY ANALYSIS;

EID: 84930014499     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3726     Document Type: Article

References (45)

1. Siegel R, Ma J, Zou Z, Jemal A. Cancer statistics, 2014. CA: a cancer journal for clinicians. 2014; 64: 9-29.
2. GLOBOCAN 2012: Estimated Cancer Incidence, Mortality and Prevalence Worldwide in 2012 [database on the Internet]. International Agency for Research on Cancer. 2013. Available from: http://globocan.iarc.fr.
3. Mirnezami R, Nicholson J, Darzi A. Preparing for Precision Medicine. New England Journal of Medicine. 2012; 366: 489-91.
4. Toward Precision Medicine: Building a Knowledge Network for Biomedical Research and a New Taxonomy of Disease: The National Academies Press; 2011.
5. Driessens G, Beck B, Caauwe A, Simons B, Blanpain C. Defining the mode of tumour growth by clonal analysis. Nature. 2012; 488: 527-30.
6. Nguyen LV, Vanner R, Dirks P, Eaves CJ. Cancer stem cells: an evolving concept. Nat Rev Cancer. 2012; 12: 133-43.
7. Li D, Peng X, Yan D, Tang H, Huang F, Yang Y, Peng Z. Msi-1 is a Predictor of Survival and a Novel Therapeutic Target in Colon Cancer. Annals of Surgical Oncology. 2011; 18: 2074-83.
8. Sureban SM, May R, George RJ, Dieckgraefe BK, McLeod HL, Ramalingam S, Bishnupuri KS, Natarajan G, Anant S, Houchen CW. Knockdown of RNA Binding Protein Musashi-1 Leads to Tumor Regression In Vivo. Gastroenterology. 2008; 134: 1448-58.e2.
9. Imai T, Tokunaga A, Yoshida T, Hashimoto M, Mikoshiba K, Weinmaster G, Nakafuku M, Okano H. The Neural RNA-Binding Protein Musashi1 Translationally Regulates Mammalian numb Gene Expression by Interacting with Its mRNA. Mol Cell Biol. 2001 June 15, 2001; 21: 3888-900.
10. Battelli C, Nikopoulos GN, Mitchell JG, Verdi JM. The RNA-binding protein Musashi-1 regulates neural development through the translational repression of p21WAF-1. Molecular and Cellular Neuroscience. 2006; 31: 85-96.
11. Spears E, Neufeld KL. Novel Double-negative Feedback Loop between Adenomatous Polyposis Coli and Musashi1 in Colon Epithelia. Journal of Biological Chemistry. 2011 February 18, 2011; 286: 4946-50.
12. Kawahara H, Imai T, Imataka H, Tsujimoto M, Matsumoto K, Okano H. Neural RNA-binding protein Musashi1 inhibits translation initiation by competing with eIF4G for PABP. J Cell Biol. 2008 May 19; 181: 639-53.
13. Bartel DP. MicroRNAs: Target Recognition and Regulatory Functions. Cell. 2009; 136: 215-33.
14. Friedman R, Farh K, Burge C, Bartel D. Most mammalian mRNAs are conserved targets of microRNAs. Genome research. 2009; 19: 92-105.
15. Hu Z. Insight into microRNA regulation by analyzing the characteristics of their targets in humans. BMC Genomics. 2009; 10: 594.
16. Dat T. Vo MQ, Andrew D. Smith, Suzanne C. Burns, Andrew J. Brenner and Luiz O.F. Penalva. The oncogenic RNA-binding protein Musashi1 is regulated by tumor suppressor miRNAs. RNA Biology. 2011; 8: 817-28.
17. Krek A, Grün D, Poy M, Wolf R, Rosenberg L, Epstein E, MacMenamin P, da Piedade I, Gunsalus K, Stoffel M, Rajewsky N. Combinatorial microRNA target predictions. Nature genetics. 2005; 37: 495-500.
18. 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.
19. Betel D, Wilson M, Gabow A, Marks DS, Sander C. The microRNA.org resource: targets and expression. Nucleic acids research. 2008 January 1, 2008; 36(suppl 1): D149-D53.
20. Rezza A, Skah S, Roche C, Nadjar J, Samarut J, Plateroti M. The overexpression of the putative gut stem cell marker Musashi-1 induces tumorigenesis through Wnt and Notch activation. J Cell Sci. 2010: jcs.065284.
21. Potten C, Booth C, Tudor G, Booth D, Brady G, Hurley P, Ashton G, Clarke R, Sakakibara S-I, Okano H. Identification of a putative intestinal stem cell and early lineage marker; musashi-1. Differentiation; research in biological diversity. 2003; 71: 28-69.
22. Hideaki Mizuno KK, Kenta Nakai, Akinori Sarai. PrognoScan: a new database for meta-analysis of the prognosis value of genes. BMC Medical Genomics. 2009; 2:18.
23. Wang X-Y, Yu H, Linnoila R, Li L, Li D, Mo B, Okano H, Penalva L, Glazer R. Musashi1 as a potential therapeutic target and diagnostic marker for lung cancer. Oncotarget. 2013; 4: 739-50.
24. Wang X-Y, Penalva L, Yuan H, Linnoila RI, Lu J, Okano H, Glazer R. Musashi1 regulates breast tumor cell proliferation and is a prognostic indicator of poor survival. Molecular Cancer. 2010; 9: 221.
25. Schmoll HJ, Van Cutsem E, Stein A, Valentini V, Glimelius B, Haustermans K, Nordlinger B, van de Velde CJ, Balmana J, Regula J, Nagtegaal ID, Beets-Tan RG, Arnold D, et al. ESMO Consensus Guidelines for management of patients with colon and rectal cancer. A personalized approach to clinical decision making. Annals of Oncology. 2012; 23: 2479-516.
26. Kanellopoulou C, Muljo S, Kung A, Ganesan S, Drapkin R, Jenuwein T, Livingston D, Rajewsky K. Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing. Genes & development. 2005; 19: 489-990.
27. DeSano J, Xu L. MicroRNA Regulation of Cancer Stem Cells and Therapeutic Implications. AAPS J. 2009; 11: 682-92.
28. Sun G, Ye P, Murai K, Lang M-F, Li S, Zhang H, Li W, Fu C, Yin J, Wang A, Ma X, Shi Y. miR-137 forms a regulatory loop with nuclear receptor TLX and LSD1 in neural stem cells. Nature communications. 2011; 2: 529.
29. Silber J, Lim D, Petritsch C, Persson A, Maunakea A, Yu M, Vandenberg S, Ginzinger D, James C, Costello J, Bergers G, Weiss W, Alvarez-Buylla A, et al. miR-124 and miR-137 inhibit proliferation of glioblastoma multiforme cells and induce differentiation of brain tumor stem cells. BMC medicine. 2008; 6: 14.
30. Tarantino C, Paolella G, Cozzuto L, Minopoli G, Pastore L, Parisi S, Russo T. miRNA 34a, 100, and 137 modulate differentiation of mouse embryonic stem cells. FASEB journal: official publication of the Federation of American Societies for Experimental Biology. 2010; 24: 3255-63.
31. Chen L, Wang X, Wang H, Li Y, Yan W, Han L, Zhang K, Zhang J, Wang Y, Feng Y, Pu P, Jiang T, Kang C, et al. miR-137 is frequently down-regulated in glioblastoma and is a negative regulator of Cox-2. European journal of cancer (Oxford, England: 1990). 2012; 48: 3104-11.
32. Luo C, Tetteh P, Merz P, Dickes E, Abukiwan A, Hotz-Wagenblatt A, Holland-Cunz S, Sinnberg T, Schittek B, Schadendorf D, Diederichs S, Eichmüller S. miR-137 inhibits the invasion of melanoma cells through downregulation of multiple oncogenic target genes. The Journal of investigative dermatology. 2013; 133: 768-75.
33. Chen Q, Chen X, Zhang M, Fan Q, Luo S, Cao X. miR-137 is frequently down-regulated in gastric cancer and is a negative regulator of Cdc42. Digestive diseases and sciences. 2011; 56: 2009-16.
34. Balaguer F, Link A, Lozano JJ, Cuatrecasas M, Nagasaka T, Boland CR, Goel A. Epigenetic Silencing of miR-137 Is an Early Event in Colorectal Carcinogenesis. Cancer Research. 2010; 70: 6609-18.
35. Chen D-L, Wang D-S, Wu W-J, Zeng Z-L, Luo H-Y, Qiu M-Z, Ren C, Zhang D-S, Wang Z-Q, Wang F-H, Li Y-H, Kang T-B, Xu R-H. Overexpression of paxillin induced by miR-137 suppression promotes tumor progression and metastasis in colorectal cancer. Carcinogenesis. 2013; 34: 803-11.
36. Liang L, Li X, Zhang X, Lv Z, He G, Zhao W, Ren X, Li Y, Bian X, Liao W, Liu W, Yang G, Ding Y. MicroRNA-137, an HMGA1 target, suppresses colorectal cancer cell invasion and metastasis in mice by directly targeting FMNL2. Gastroenterology. 2013; 144: 624-6350000.
37. Improved Survival with Preoperative Radiotherapy in Resectable Rectal Cancer. New England Journal of Medicine. 1997; 336: 980-7.
38. Holmqvist A, Gao J, Holmlund B, Adell G, Carstensen J, Langford D, Sun X-F. PINCH is an independent prognostic factor in rectal cancer patients without preoperative radiotherapy-a study in a Swedish rectal cancer trial of preoperative radiotherapy. BMC Cancer. 2012; 12: 65.
39. Chan T, Wang Z, Dang L, Vogelstein B, Kinzler K. Targeted inactivation of CTNNB1 reveals unexpected effects of beta-catenin mutation. Proceedings of the National Academy of Sciences of the United States of America. 2002; 99: 8265-70.
40. Ji Q, Hao X, Zhang M, Tang W, Yang M, Li L, Xiang D, DeSano JT, Bommer GT, Fan D, Fearon ER, Lawrence TS, Xu L. MicroRNA miR-34 Inhibits Human Pancreatic Cancer Tumor-Initiating Cells. PLoS ONE. 2009; 4: e6816.
41. Cheng P, Ni Z, Dai X, Wang B, Ding W, Rae Smith A, Xu L, Wu D, He F, Lian J. The novel BH-3 mimetic apogossypolone induces Beclin-1-and ROS-mediated autophagy in human hepatocellular carcinoma [corrected] cells. Cell death & disease. 2013; 4.
42. Wu X, Li M, Qu Y, Tang W, Zheng Y, Lian J, Ji M, Xu L. Design and synthesis of novel Gefitinib analogues with improved anti-tumor activity. Bioorg Med Chem. 2010; 18: 3812-22.
43. Vo DT, Abdelmohsen K, Martindale JL, Qiao M, Tominaga K, Burton TL, Gelfond JAL, Brenner AJ, Patel V, Trageser D, Scheffler B, Gorospe M, Penalva LOF. The Oncogenic RNA-Binding Protein Musashi1 Is Regulated by HuR via mRNA Translation and Stability in Glioblastoma Cells. Molecular Cancer Research. 2012 January 1, 2012; 10: 143-55.
44. Livak TDSKJ. Analyzing real-time PCR data by the comparative Ct method. Nature Protocols. 2008; 3: 1101-8.
45. Li L, Hao X, Qin J, Tang W, He F, Smith A, Zhang M, Simeone D, Qiao X, Chen Z-N, Lawrence T, Xu L. Antibody Against CD44s Inhibits Pancreatic Tumor Initiation and Postradiation Recurrence in Mice. Gastroenterology. 2014; 146: 1108.