Musashi-2 (MSI2) supports TGF-β signaling and inhibits claudins to promote non-small cell lung cancer (NSCLC) metastasis

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 25, 2016, Pages 6955-6960

  Kudinov, Alexander E ^a,b   Deneka, Alexander ^a,c   Nikonova, Anna S ^a   Beck, Tim N ^a,d   Ahn, Young Ho ^e,f   Liu, Xin ^e   Martinez, Cathleen F ^g   Schultz, Fred A ^g   Reynolds, Samuel ^g   Yang, Dong Hua ^a   Cai, Kathy Q ^a,b   Yaghmour, Khaled M ^a   Baker, Karmel A ^a   Egleston, Brian L ^a   Nicolas, Emmanuelle ^a   Chikwem, Adaeze ^a,h   Andrianov, Gregory ^c   Singh, Shelly ^a   Borghaei, Hossein ^a   Serebriiskii, Ilya G ^a,c   Gibbons, Don L ^e   Kurie, Jonathan M ^e   Golemis, Erica A ^a,d   Boumber, Yanis ^a,b   more..

^a FOX CHASE CANCER CENTER   (United States)

^b UNIVERSITY OF NEW MEXICO   (United States)

^c KAZAN FEDERAL UNIVERSITY   (Russian Federation)

^d DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^e UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^f Ewha Womans University School of Medicine   (South Korea)

^g UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

^h TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Claudins; Lung cancer; Metastasis; MSI2; NSCLC

Indexed keywords

BIOLOGICAL MARKER; CLAUDIN; CLAUDIN 3; CLAUDIN 5; CLAUDIN 7; FIBRONECTIN; MESSENGER RNA; MUSASHI 2 PROTEIN; REGULATOR PROTEIN; SHORT HAIRPIN RNA; SMAD3 PROTEIN; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SNAIL; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; UNCLASSIFIED DRUG; UVOMORULIN; MSI2 PROTEIN, HUMAN; RNA BINDING PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CANCER GROWTH; CELL CONTACT; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; EPITHELIAL MESENCHYMAL TRANSITION; GENE OVEREXPRESSION; IN VITRO STUDY; LUNG TUMOR; METASTASIS POTENTIAL; MOUSE; NON SMALL CELL LUNG CANCER; NONHUMAN; OVERALL SURVIVAL; PHENOTYPE; PRIMARY TUMOR; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN SYNTHESIS INHIBITION; RNA TRANSLATION; SURVIVAL RATE; TUMOR INVASION; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; HUMAN; METABOLISM; METASTASIS; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANIMALS; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; CLAUDINS; HUMANS; LUNG NEOPLASMS; MICE; NEOPLASM METASTASIS; RNA-BINDING PROTEINS; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 84975698737     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1513616113     Document Type: Article

References (46)

1. Siegel R, Naishadham D, Jemal A (2013) Cancer statistics, 2013. CA Cancer J Clin 63(1):11-30.
2. Howlader NNA, et al. (2013) SEER Cancer Statistics Review, 1975-2010, ed Cronin KA (National Cancer Institute, Bethesda).
3. Zheng S, El-Naggar AK, Kim ES, Kurie JM, Lozano G (2007) A genetic mouse model for metastatic lung cancer with gender differences in survival. Oncogene 26(48):6896-6904.
4. Mitsudomi T, et al. (1991) Mutations of ras genes distinguish a subset of non-small-cell lung cancer cell lines from small-cell lung cancer cell lines. Oncogene 6(8):1353-1362.
5. Takahashi T, et al. (1989) p53: A frequent target for genetic abnormalities in lung cancer. Science 246(4929):491-494.
6. Bertolini G, et al. (2009) Highly tumorigenic lung cancer CD133+ cells display stem-like features and are spared by cisplatin treatment. Proc Natl Acad Sci USA 106(38):16281-16286.
7. Singh A, Settleman J (2010) EMT, cancer stem cells and drug resistance: An emerging axis of evil in the war on cancer. Oncogene 29(34):4741-4751.
8. Licciulli S, et al. (2013) Notch1 is required for Kras-induced lung adenocarcinoma and controls tumor cell survival via p53. Cancer Res 73(19):5974-5984.
9. Arasada RR, Amann JM, Rahman MA, Huppert SS, Carbone DP (2014) EGFR blockade enriches for lung cancer stem-like cells through Notch3-dependent signaling. Cancer Res 74(19):5572-5584.
10. Hassan KA, et al. (2013) Notch pathway activity identifies cells with cancer stem cell-like properties and correlates with worse survival in lung adenocarcinoma. Clin Cancer Res 19(8):1972-1980.
11. Tirino V, et al. (2013) TGF-β1 exposure induces epithelial to mesenchymal transition both in CSCs and non-CSCs of the A549 cell line, leading to an increase of migration ability in the CD133+ A549 cell fraction. Cell Death Dis 4:e620.
12. Beck TN, Chikwem AJ, Solanki NR, Golemis EA (2014) Bioinformatic approaches to augment study of epithelial-to-mesenchymal transition in lung cancer. Physiol Genomics 46(19):699-724.
13. Gibbons DL, et al. (2009) Contextual extracellular cues promote tumor cell EMT and metastasis by regulating miR-200 family expression. Genes Dev 23(18):2140-2151.
14. Barretina J, et al. (2012) The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity. Nature 483(7391):603-607.
15. Lu Z, et al. (2011) Claudin-7 inhibits human lung cancer cell migration and invasion through ERK/MAPK signaling pathway. Exp Cell Res 317(13):1935-1946.
16. Prat A, et al. (2013) Genomic analyses across six cancer types identify basal-like breast cancer as a unique molecular entity. Sci Rep 3:3544.
17. Bruna A, et al. (2012) TGFβ induces the formation of tumour-initiating cells in claudinlow breast cancer. Nat Commun 3:1055.
18. Liu W, Cheng S, Asa SL, Ezzat S (2008) The melanoma-associated antigen A3 mediates fibronectin-controlled cancer progression and metastasis. Cancer Res 68(19):8104-8112.
19. Urtreger AJ, et al. (2006) Fibronectin is distinctly downregulated in murine mammary adenocarcinoma cells with high metastatic potential. Oncol Rep 16(6):1403-1410.
20. Zhang X, et al. (2009) Up-regulated microRNA-143 transcribed by nuclear factor kappa B enhances hepatocarcinoma metastasis by repressing fibronectin expression. Hepatology 50(2):490-499.
21. Yi M, Ruoslahti E (2001) A fibronectin fragment inhibits tumor growth, angiogenesis, and metastasis. Proc Natl Acad Sci USA 98(2):620-624.
22. Rezza A, et al. (2010) The overexpression of the putative gut stem cell marker Musashi-1 induces tumorigenesis through Wnt and Notch activation. J Cell Sci 123(Pt 19):3256-3265.
23. Ito T, et al. (2010) Regulation of myeloid leukaemia by the cell-fate determinant Musashi. Nature 466(7307):765-768.
24. Park SM, et al. (2014) Musashi-2 controls cell fate, lineage bias, and TGF-β signaling in HSCs. J Exp Med 211(1):71-87.
25. Katz Y, et al. (2014) Musashi proteins are post-transcriptional regulators of the epithelial-luminal cell state. eLife 3:e03915.
26. Kwon MJ (2013) Emerging roles of claudins in human cancer. Int J Mol Sci 14(9):18148-18180.
27. Sakakibara S, Nakamura Y, Satoh H, Okano H (2001) Rna-binding protein Musashi2: Developmentally regulated expression in neural precursor cells and subpopulations of neurons in mammalian CNS. J Neurosci 21(20):8091-8107.
28. Wang S, et al. (2015) Transformation of the intestinal epithelium by the MSI2 RNA-binding protein. Nat Commun 6:6517.
29. Massagué J (2012) TGFβ signalling in context. Nat Rev Mol Cell Biol 13(10):616-630.
30. Sureban SM, et al. (2008) Knockdown of RNA binding protein musashi-1 leads to tumor regression in vivo. Gastroenterology 134(5):1448-1458.
31. Li D, et al. (2011) Msi-1 is a predictor of survival and a novel therapeutic target in colon cancer. Ann Surg Oncol 18(7):2074-2083.
32. Oskarsson T, et al. (2011) Breast cancer cells produce tenascin C as a metastatic niche component to colonize the lungs. Nat Med 17(7):867-874.
33. Kharas MG, et al. (2010) Musashi-2 regulates normal hematopoiesis and promotes aggressive myeloid leukemia. Nat Med 16(8):903-908.
34. Liu J, et al. (2013) Suppression of SCARA5 by Snail1 is essential for EMT-associated cell migration of A549 cells. Oncogenesis 2:e73.
35. Shamir ER, Ewald AJ (2015) Adhesion in mammary development: Novel roles for E-cadherin in individual and collective cell migration. Curr Top Dev Biol 112:353-382.
36. Creighton CJ, et al. (2009) Residual breast cancers after conventional therapy display mesenchymal as well as tumor-initiating features. Proc Natl Acad Sci USA 106(33):13820-13825.
37. Hennessy BT, et al. (2009) Characterization of a naturally occurring breast cancer subset enriched in epithelial-to-mesenchymal transition and stem cell characteristics. Cancer Res 69(10):4116-4124.
38. Choi W, et al. (2014) Intrinsic basal and luminal subtypes of muscle-invasive bladder cancer. Nat Rev Urol 11(7):400-410.
39. Yamamoto T, et al. (2010) Reduced expression of claudin-7 is associated with poor outcome in non-small cell lung cancer. Oncol Lett 1(3):501-505.
40. Akhurst RJ, Hata A (2012) Targeting the TGFβ signalling pathway in disease. Nat Rev Drug Discov 11(10):790-811.
41. Dituri F, et al. (2013) Differential inhibition of the TGF-β signaling pathway in HCC cells using the small molecule inhibitor LY2157299 and the D10 monoclonal antibody against TGF-β receptor type II. PLoS One 8(6):e67109.
42. Park CY, et al. (2014) An novel inhibitor of TGF-β type I receptor, IN-1130, blocks breast cancer lung metastasis through inhibition of epithelial-mesenchymal transition. Cancer Lett 351(1):72-80.
43. Iadevaia S, Lu Y, Morales FC, Mills GB, Ram PT (2010) Identification of optimal drug combinations targeting cellular networks: Integrating phospho-proteomics and computational network analysis. Cancer Res 70(17):6704-6714.
44. Kornblau SM, et al. (2009) Functional proteomic profiling of AML predicts response and survival. Blood 113(1):154-164.
45. Tibes R, et al. (2006) Reverse phase protein array: Validation of a novel proteomic technology and utility for analysis of primary leukemia specimens and hematopoietic stem cells. Mol Cancer Ther 5(10):2512-2521.
46. Saeed AI, et al. (2003) TM4: A free, open-source system for microarray data management and analysis. Biotechniques 34(2):374-378.