Dystrophin is a tumor suppressor in human cancers with myogenic programs

Nature Genetics

Volumn 46, Issue 6, 2014, Pages 601-606

  Wang, Yuexiang ^a   Marino Enriquez, Adrian ^a   Bennett, Richard R ^b   Zhu, Meijun ^a   Shen, Yiping ^b,c   Eilers, Grant ^a   Lee, Jen Chieh ^a,d   Henze, Joern ^a   Fletcher, Benjamin S ^a   Gu, Zhizhan ^a   Fox, Edward A ^e   Antonescu, Cristina R ^f   Fletcher, Christopher D M ^a   Guo, Xiangqian ^g   Raut, Chandrajit P ^a   Demetri, George D ^e   Van De Rijn, Matt ^g   Ordog, Tamas ^h,i   Kunkel, Louis M ^b   Fletcher, Jonathan A ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c SHANGHAI CHILDREN S MEDICAL CENTER   (China)

^d NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

^e DANA FARBER CANCER INSTITUTE   (United States)

^f MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^g STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^h MAYO CLINIC   (United States)

ⁱ MAYO GRADUATE SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DYSTROPHIN;

ANCHORAGE INDEPENDENT GROWTH; ARTICLE; CELL INVASION; CELL MIGRATION; CLINICAL ARTICLE; CONTROLLED STUDY; EMBRYONAL RHABDOMYOSARCOMA; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; GASTROINTESTINAL STROMAL TUMOR; GENE DELETION; GENE EXPRESSION; GENE INACTIVATION; HUMAN; HUMAN CELL; HUMAN TISSUE; LEIOMYOSARCOMA; MALE; MULTIPLEX LIGATION DEPENDENT PROBE AMPLIFICATION; MUSCULAR DYSTROPHY; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SARCOMA CELL; SINGLE NUCLEOTIDE POLYMORPHISM; TRANSCRIPTION INITIATION SITE; TUMOR SUPPRESSOR GENE; X CHROMOSOME;

ANIMALS; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL MOVEMENT; DISEASE PROGRESSION; DYSTROPHIN; FEMALE; GASTROINTESTINAL STROMAL TUMORS; GENE DELETION; GENES, TUMOR SUPPRESSOR; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; INTERSTITIAL CELLS OF CAJAL; LEIOMYOSARCOMA; MALE; MICE; MICE, INBRED BALB C; MUSCLE DEVELOPMENT; MUSCLE, SKELETAL; MUSCULAR DYSTROPHIES; NEOPLASM INVASIVENESS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; POLYMORPHISM, SINGLE NUCLEOTIDE; RHABDOMYOSARCOMA; SARCOMA;

EID: 84901680208     PISSN: 10614036     EISSN: 15461718     Source Type: Journal    
DOI: 10.1038/ng.2974     Document Type: Article

References (45)

1. Corless, C.L., Barnett, C.M. & Heinrich, M.C. Gastrointestinal stromal tumours: origin and molecular oncology. Nat. Rev. Cancer 11, 865-878 (2011).
2. Arndt, C.A. & Crist, W.M. Common musculoskeletal tumors of childhood and adolescence. N. Engl. J. Med. 341, 342-352 (1999).
3. Hernando, E. et al. The AKT-mTOR pathway plays a critical role in the development of leiomyosarcomas. Nat. Med. 13, 748-753 (2007).
4. Corless, C.L., Fletcher, J.A. & Heinrich, M.C. Biology of gastrointestinal stromal tumors. J. Clin. Oncol. 22, 3813-3825 (2004).
5. Taylor, B.S. et al. Advances in sarcoma genomics and new therapeutic targets. Nat. Rev. Cancer 11, 541-557 (2011).
6. Hettmer, S. & Wagers, A.J. Muscling in: uncovering the origins of rhabdomyosarcoma. Nat. Med. 16, 171-173 (2010).
7. Edris, B. et al. Antibody therapy targeting the CD47 protein is effective in a model of aggressive metastatic leiomyosarcoma. Proc. Natl. Acad. Sci. USA 109, 6656-6661 (2012).
8. Würl, P. et al. Frequent occurrence of p53 mutations in rhabdomyosarcoma and leiomyosarcoma, but not in fibrosarcoma and malignant neural tumors. Int. J. Cancer 69, 317-323 (1996).
9. Ognjanovic, S., Olivier, M., Bergemann, T.L. & Hainaut, P. Sarcomas in TP53 germline mutation carriers: a review of the IARC TP53 database. Cancer 118, 1387-1396 (2012).
10. Hirota, S. et al. Gain-of-function mutations of c-kit in human gastrointestinal stromal tumors. Science 279, 577-580 (1998).
11. Heinrich, M.C. et al. PDGFRA activating mutations in gastrointestinal stromal tumors. Science 299, 708-710 (2003).
12. Rossi, S. et al. Molecular and clinicopathologic characterization of gastrointestinal stromal tumors (GISTs) of small size. Am. J. Surg. Pathol. 34, 1480-1491 (2010).
13. Schneider-Stock, R. et al. Loss of p16 protein defines high-risk patients with gastrointestinal stromal tumors: a tissue microarray study. Clin. Cancer Res. 11, 638-645 (2005).
14. Henze, J. et al. p53 modulation as a therapeutic strategy in gastrointestinal stromal tumors. PLoS ONE 7, e37776 (2012).
15. Hoffman, E.P., Brown, R.H. Jr. & Kunkel, L.M. Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell 51, 919-928 (1987).
16. Barretina, J. et al. The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity. Nature 483, 603-607 (2012).
17. Duszczyk, M.M., Wutz, A., Rybin, V. & Sattler, M. The Xist RNA A-repeat comprises a novel AUCG tetraloop fold and a platform for multimerization. RNA 17, 1973-1982 (2011).
18. Muntoni, F., Torelli, S. & Ferlini, A. Dystrophin and mutations: one gene, several proteins, multiple phenotypes. Lancet Neurol. 2, 731-740 (2003).
19. Tadayoni, R., Rendon, A., Soria-Jasso, L.E. & Cisneros, B. Dystrophin Dp71: the smallest but multifunctional product of the Duchenne muscular dystrophy gene. Mol. Neurobiol. 45, 43-60 (2012).
20. Chapdelaine, P. et al. Functional EGFP-dystrophin fusion proteins for gene therapy vector development. Protein Eng. 13, 611-615 (2000).
21. Tang, Y., Cummins, J., Huard, J. & Wang, B. AAV-directed muscular dystrophy gene therapy. Expert Opin. Biol. Ther. 10, 395-408 (2010).
22. Ervasti, J.M. & Campbell, K.P. Membrane organization of the dystrophin-glycoprotein complex. Cell 66, 1121-1131 (1991).
23. Berk, B.C., Fujiwara, K. & Lehoux, S. ECM remodeling in hypertensive heart disease. J. Clin. Invest. 117, 568-575 (2007).
24. Valastyan, S. & Weinberg, R.A. Tumor metastasis: molecular insights and evolving paradigms. Cell 147, 275-292 (2011).
25. Hanahan, D. & Weinberg, R.A. Hallmarks of cancer: the next generation. Cell 144, 646-674 (2011).
26. Murphy, D.A. & Courtneidge, S.A. The 'ins' and 'outs' of podosomes and invadopodia: characteristics, formation and function. Nat. Rev. Mol. Cell Biol. 12, 413-426 (2011).
27. Fernandez, K., Serinagaoglu, Y., Hammond, S., Martin, L.T. & Martin, P.T. Mice lacking dystrophin or α sarcoglycan spontaneously develop embryonal rhabdomyosarcoma with cancer-associated p53 mutations and alternatively spliced or mutant Mdm2 transcripts. Am. J. Pathol. 176, 416-434 (2010).
28. Chamberlain, J.S., Metzger, J., Reyes, M., Townsend, D. & Faulkner, J.A. Dystrophin-deficient mdx mice display a reduced life span and are susceptible to spontaneous rhabdomyosarcoma. FASEB J. 21, 2195-2204 (2007).
29. Schmidt, W.M. et al. DNA damage, somatic aneuploidy, and malignant sarcoma susceptibility in muscular dystrophies. PLoS Genet. 7, e1002042 (2011).
30. Rossbach, H.C., Lacson, A., Grana, N.H. & Barbosa, J.L. Duchenne muscular dystrophy and concomitant metastatic alveolar rhabdomyosarcoma. J. Pediatr. Hematol. Oncol. 21, 528-530 (1999).
31. Jakab, Z., Szegedi, I., Balogh, E., Kiss, C. & Oláh, E. Duchenne muscular dystrophy-rhabdomyosarcoma, ichthyosis vulgaris/acute monoblastic leukemia: association of rare genetic disorders and childhood malignant diseases. Med. Pediatr. Oncol. 39, 66-68 (2002).
32. Barretina, J. et al. Subtype-specific genomic alterations define new targets for soft-tissue sarcoma therapy. Nat. Genet. 42, 715-721 (2010).
33. Gottipati, P. et al. Transcription-associated recombination is dependent on replication in mammalian cells. Mol. Cell. Biol. 28, 154-164 (2008).
34. Körner, H. et al. Digital karyotyping reveals frequent inactivation of the dystrophin/DMD gene in malignant melanoma. Cell Cycle 6, 189-198 (2007).
35. Li, Y. et al. UTRN on chromosome 6q24 is mutated in multiple tumors. Oncogene 26, 6220-6228 (2007).
36. Tinsley, J.M. et al. Daily treatment with SMTC1100, a novel small molecule utrophin upregulator, dramatically reduces the dystrophic symptoms in the mdx mouse. PLoS ONE 6, e19189 (2011).
37. Cirak, S. et al. Exon skipping and dystrophin restoration in patients with Duchenne muscular dystrophy after systemic phosphorodiamidate morpholino oligomer treatment: an open-label, phase 2, dose-escalation study. Lancet 378, 595-605 (2011).
38. Kawahara, G. et al. Drug screening in a zebrafish model of Duchenne muscular dystrophy. Proc. Natl. Acad. Sci. USA 108, 5331-5336 (2011).
39. Gehrig, S.M. et al. Hsp72 preserves muscle function and slows progression of severe muscular dystrophy. Nature 484, 394-398 (2012).
40. Seto, J.T., Ramos, J.N., Muir, L., Chamberlain, J.S. & Odom, G.L. Gene replacement therapies for Duchenne muscular dystrophy using adeno-associated viral vectors. Curr. Gene Ther. 12, 139-151 (2012).
41. Bardsley, M.R. et al. Kitlow stem cells cause resistance to Kit/platelet-derived growth factor α inhibitors in murine gastrointestinal stromal tumors. Gastroenterology 139, 942-952 (2010).
42. Izbeki, F. et al. Loss of Kitlow progenitors, reduced stem cell factor and high oxidative stress underlie gastric dysfunction in progeric mice. J. Physiol. (Lond.) 588, 3101-3117 (2010).
43. Taguchi, T. et al. Conventional and molecular cytogenetic characterization of a new human cell line, GIST-T1, established from gastrointestinal stromal tumor. Lab. Invest. 82, 663-665 (2002).
44. Rasheed, S., Nelson-Rees, W.A., Toth, E.M., Arnstein, P. & Gardner, M.B. Characterization of a newly derived human sarcoma cell line (HT-1080). Cancer 33, 1027-1033 (1974).
45. Patial, S., Luo, J., Porter, K.J., Benovic, J.L. & Parameswaran, N. G-protein-coupled-receptor kinases mediate TNFα-induced NFκB signalling via direct interaction with and phosphorylation of IκBα. Biochem. J. 425, 169-178 (2010).