Insertional Mutagenesis Identifies a STAT3/Arid1b/β-catenin Pathway Driving Neurofibroma Initiation

Cell Reports

Volumn 14, Issue 8, 2016, Pages 1979-1990

  Wu, Jianqiang ^a   Keng, Vincent W ^c,d,l   Patmore, Deanna M ^a   Kendall, Jed J ^a   Patel, Ami V ^a   Jousma, Edwin ^a   Jessen, Walter J ^a   Choi, Kwangmin ^a   Tschida, Barbara R ^c,d   Silverstein, Kevin A T ^e   Fan, Danhua ^e   Schwartz, Eric B ^f   Fuchs, James R ^f   Zou, Yuanshu ^b   Kim, Mi Ok ^b   Dombi, Eva ^g   Levy, David E ^h   Huang, Gang ^a   Cancelas, Jose A ^a,i   Stemmer Rachamimov, Anat O ^j   Spinner, Robert J ^k   Largaespada, David A ^c,d   Ratner, Nancy ^a   more..

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^b CINCINNATI CHILDREN S HOSPITAL RESEARCH FOUNDATION   (United States)

^c UNIVERSITY OF MINNESOTA   (United States)

^d UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^e UNIVERSITY OF MINNESOTA   (United States)

^f OHIO STATE UNIVERSITY   (United States)

^g NATIONAL CANCER INSTITUTE   (United States)

^h NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

ⁱ UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^j MASSACHUSETTS GENERAL HOSPITAL   (United States)

^k MAYO CLINIC   (United States)

^l HONG KONG POLYTECHNIC UNIVERSITY   (Hong Kong)

more..

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; CYCLIN D1; MESSENGER RNA; NEUROFIBROMIN; SHORT HAIRPIN RNA; STAT3 PROTEIN; WNT PROTEIN; CTNNB1 PROTEIN, MOUSE; DNA BINDING PROTEIN; DNA HELICASE; GLYCOGEN SYNTHASE KINASE 3BETA; HISTONE; NAA11 PROTEIN, MOUSE; NUCLEAR PROTEIN; PEPTIDE ALPHA N ACETYLTRANSFERASE A; SMALL INTERFERING RNA; SMARCA4 PROTEIN, MOUSE; STAT3 PROTEIN, MOUSE; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY LABELING; ARID1B GENE; ARTICLE; CANCER GROWTH; CARCINOGENESIS; CELL COUNT; CELL NUCLEUS; CELL PROLIFERATION; CELL SELF-RENEWAL; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN IMMUNOPRECIPITATION; CYTOPLASM; GENE; GENE DELETION; GENE EXPRESSION; GLIA CELL; HISTONE MODIFICATION; MOUSE; MUTAGENESIS; NEUROFIBROMA; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PYROSEQUENCING; SCHWANN CELL; TRANSPOSON; TUMOR GROWTH; ANIMAL; ANTAGONISTS AND INHIBITORS; CANCER TRANSPLANTATION; DISEASE MODEL; FEMALE; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; NEURAL STEM CELL; NEUROFIBROMATOSIS TYPE 1; NUDE MOUSE; PATHOLOGY; PERIPHERAL NERVE TUMOR; PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANIMALS; BETA CATENIN; CARCINOGENESIS; DISEASE MODELS, ANIMAL; DNA HELICASES; DNA-BINDING PROTEINS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GLYCOGEN SYNTHASE KINASE 3 BETA; HISTONES; HUMANS; MICE; MICE, NUDE; MUTAGENESIS, INSERTIONAL; N-TERMINAL ACETYLTRANSFERASE A; NEOPLASM TRANSPLANTATION; NEURAL STEM CELLS; NEUROFIBROMATOSIS 1; NEUROFIBROMIN 1; NUCLEAR PROTEINS; PERIPHERAL NERVOUS SYSTEM NEOPLASMS; PHOSPHORYLATION; RNA, SMALL INTERFERING; SCHWANN CELLS; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; TRANSCRIPTION FACTORS;

EID: 84959181076     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.01.074     Document Type: Article

References (40)

1. Banerjee S., Byrd J.N., Gianino S.M., Harpstrite S.E., Rodriguez F.J., Tuskan R.G., Reilly K.M., Piwnica-Worms D.R., Gutmann D.H. The neurofibromatosis type 1 tumor suppressor controls cell growth by regulating signal transducer and activator of transcription-3 activity in vitro and in vivo. Cancer Res. 2010, 70:1356-1366.
2. Barker N., Hurlstone A., Musisi H., Miles A., Bienz M., Clevers H. The chromatin remodelling factor Brg-1 interacts with beta-catenin to promote target gene activation. EMBO J. 2001, 20:4935-4943.
3. Battle T.E., Frank D.A. The role of STATs in apoptosis. Curr. Mol. Med. 2002, 2:381-392.
4. Boyd K.P., Korf B.R., Theos A. Neurofibromatosis type 1. J. Am. Acad. Dermatol. 2009, 61:1-14. quiz 15-16.
5. Chen Z., Liu C., Patel A.J., Liao C.P., Wang Y., Le L.Q. Cells of origin in the embryonic nerve roots for NF1-associated plexiform neurofibroma. Cancer Cell 2014, 26:695-706.
6. Cichowski K., Jacks T. NF1 tumor suppressor gene function: narrowing the GAP. Cell 2001, 104:593-604.
7. De Raedt T., Beert E., Pasmant E., Luscan A., Brems H., Ortonne N., Helin K., Hornick J.L., Mautner V., Kehrer-Sawatzki H., et al. PRC2 loss amplifies Ras-driven transcription and confers sensitivity to BRD4-based therapies. Nature 2014, 514:247-251.
8. Faghihi M.A., Wahlestedt C. Regulatory roles of natural antisense transcripts. Nat. Rev. Mol. Cell Biol. 2009, 10:637-643.
9. Grigoryan T., Stein S., Qi J., Wende H., Garratt A.N., Nave K.A., Birchmeier C., Birchmeier W. Wnt/Rspondin/β-catenin signals control axonal sorting and lineage progression in Schwann cell development. Proc. Natl. Acad. Sci. USA 2013, 110:18174-18179.
10. Helming K.C., Wang X., Wilson B.G., Vazquez F., Haswell J.R., Manchester H.E., Kim Y., Kryukov G.V., Ghandi M., Aguirre A.J., et al. ARID1B is a specific vulnerability in ARID1A-mutant cancers. Nat. Med. 2014, 20:251-254.
11. Jessen W.J., Miller S.J., Jousma E., Wu J., Rizvi T.A., Brundage M.E., Eaves D., Widemann B., Kim M.O., Dombi E., et al. MEK inhibition exhibits efficacy in human and mouse neurofibromatosis tumors. J. Clin. Invest. 2013, 123:340-347.
12. Keng V.W., Villanueva A., Chiang D.Y., Dupuy A.J., Ryan B.J., Matise I., Silverstein K.A., Sarver A., Starr T.K., Akagi K., et al. A conditional transposon-based insertional mutagenesis screen for genes associated with mouse hepatocellular carcinoma. Nat. Biotechnol. 2009, 27:264-274.
13. Khursheed M., Kolla J.N., Kotapalli V., Gupta N., Gowrishankar S., Uppin S.G., Sastry R.A., Koganti S., Sundaram C., Pollack J.R., Bashyam M.D. ARID1B, a member of the human SWI/SNF chromatin remodeling complex, exhibits tumour-suppressor activities in pancreatic cancer cell lines. Br. J. Cancer 2013, 108:2056-2062.
14. Kim D.J., Kataoka K., Rao D., Kiguchi K., Cotsarelis G., Digiovanni J. Targeted disruption of stat3 reveals a major role for follicular stem cells in skin tumor initiation. Cancer Res. 2009, 69:7587-7594.
15. Kroon P., Berry P.A., Stower M.J., Rodrigues G., Mann V.M., Simms M., Bhasin D., Chettiar S., Li C., Li P.K., et al. JAK-STAT blockade inhibits tumor initiation and clonogenic recovery of prostate cancer stem-like cells. Cancer Res. 2013, 73:5288-5298.
16. Lee W., Teckie S., Wiesner T., Ran L., Prieto Granada C.N., Lin M., Zhu S., Cao Z., Liang Y., Sboner A., et al. PRC2 is recurrently inactivated through EED or SUZ12 loss in malignant peripheral nerve sheath tumors. Nat. Genet. 2014, 46:1227-1232.
17. Lesina M., Kurkowski M.U., Ludes K., Rose-John S., Treiber M., Klöppel G., Yoshimura A., Reindl W., Sipos B., Akira S., et al. Stat3/Socs3 activation by IL-6 transsignaling promotes progression of pancreatic intraepithelial neoplasia and development of pancreatic cancer. Cancer Cell 2011, 19:456-469.
18. Lin L., Hutzen B., Zuo M., Ball S., Deangelis S., Foust E., Pandit B., Ihnat M.A., Shenoy S.S., Kulp S., et al. Novel STAT3 phosphorylation inhibitors exhibit potent growth-suppressive activity in pancreatic and breast cancer cells. Cancer Res. 2010, 70:2445-2454.
19. Liu C., Li Y., Semenov M., Han C., Baeg G.H., Tan Y., Zhang Z., Lin X., He X. Control of beta-catenin phosphorylation/degradation by a dual-kinase mechanism. Cell 2002, 108:837-847.
20. Luscan A., Shackleford G., Masliah-Planchon J., Laurendeau I., Ortonne N., Varin J., Lallemand F., Leroy K., Dumaine V., Hivelin M., et al. The activation of the WNT signaling pathway is a Hallmark in neurofibromatosis type 1 tumorigenesis. Clin. Cancer Res. 2014, 20:358-371.
21. Magistri M., Faghihi M.A., St Laurent G., Wahlestedt C. Regulation of chromatin structure by long noncoding RNAs: focus on natural antisense transcripts. Trends Genet. 2012, 28:389-396.
22. Mo W., Chen J., Patel A., Zhang L., Chau V., Li Y., Cho W., Lim K., Xu J., Lazar A.J., et al. CXCR4/CXCL12 mediate autocrine cell- cycle progression in NF1-associated malignant peripheral nerve sheath tumors. Cell 2013, 152:1077-1090.
23. Moh A., Zhang W., Yu S., Wang J., Xu X., Li J., Fu X.Y. STAT3 sensitizes insulin signaling by negatively regulating glycogen synthase kinase-3 beta. Diabetes 2008, 57:1227-1235.
24. Nagl N.G., Wang X., Patsialou A., Van Scoy M., Moran E. Distinct mammalian SWI/SNF chromatin remodeling complexes with opposing roles in cell-cycle control. EMBO J. 2007, 26:752-763.
25. Nakamura T., Colbert M.C., Robbins J. Neural crest cells retain multipotential characteristics in the developing valves and label the cardiac conduction system. Circ. Res. 2006, 98:1547-1554.
26. Ni Z., Bremner R. Brahma-related gene 1-dependent STAT3 recruitment at IL-6-inducible genes. J. Immunol. 2007, 178:345-351.
27. Rahrmann E.P., Watson A.L., Keng V.W., Choi K., Moriarity B.S., Beckmann D.A., Wolf N.K., Sarver A., Collins M.H., Moertel C.L., et al. Forward genetic screen for malignant peripheral nerve sheath tumor formation identifies new genes and pathways driving tumorigenesis. Nat. Genet. 2013, 45:756-766.
28. Sausen M., Leary R.J., Jones S., Wu J., Reynolds C.P., Liu X., Blackford A., Parmigiani G., Diaz L.A., Papadopoulos N., et al. Integrated genomic analyses identify ARID1A and ARID1B alterations in the childhood cancer neuroblastoma. Nat. Genet. 2013, 45:12-17.
29. Serra E., Puig S., Otero D., Gaona A., Kruyer H., Ars E., Estivill X., Lázaro C. Confirmation of a double-hit model for the NF1 gene in benign neurofibromas. Am. J. Hum. Genet. 1997, 61:512-519.
30. Sherry M.M., Reeves A., Wu J.K., Cochran B.H. STAT3 is required for proliferation and maintenance of multipotency in glioblastoma stem cells. Stem Cells 2009, 27:2383-2392.
31. Tolstorukov M.Y., Sansam C.G., Lu P., Koellhoffer E.C., Helming K.C., Alver B.H., Tillman E.J., Evans J.A., Wilson B.G., Park P.J., Roberts C.W. Swi/Snf chromatin remodeling/tumor suppressor complex establishes nucleosome occupancy at target promoters. Proc. Natl. Acad. Sci. USA 2013, 110:10165-10170.
32. Trotter K.W., Archer T.K. The BRG1 transcriptional coregulator. Nucl. Recept. Signal. 2008, 6:e004.
33. Vasileiou G., Ekici A.B., Uebe S., Zweier C., Hoyer J., Engels H., Behrens J., Reis A., Hadjihannas M.V. Chromatin-Remodeling-Factor ARID1B Represses Wnt/β-Catenin Signaling. Am. J. Hum. Genet. 2015, 97:445-456.
34. Watson A.L., Rahrmann E.P., Moriarity B.S., Choi K., Conboy C.B., Greeley A.D., Halfond A.L., Anderson L.K., Wahl B.R., Keng V.W., et al. Canonical Wnt/β-catenin signaling drives human schwann cell transformation, progression, and tumor maintenance. Cancer Discov. 2013, 3:674-689.
35. Williams J.P., Wu J., Johansson G., Rizvi T.A., Miller S.C., Geiger H., Malik P., Li W., Mukouyama Y.S., Cancelas J.A., Ratner N. Nf1 mutation expands an EGFR-dependent peripheral nerve progenitor that confers neurofibroma tumorigenic potential. Cell Stem Cell 2008, 3:658-669.
36. Wu D., Pan W. GSK3: a multifaceted kinase in Wnt signaling. Trends Biochem. Sci. 2010, 35:161-168.
37. Wu J., Williams J.P., Rizvi T.A., Kordich J.J., Witte D., Meijer D., Stemmer-Rachamimov A.O., Cancelas J.A., Ratner N. Plexiform and dermal neurofibromas and pigmentation are caused by Nf1 loss in desert hedgehog-expressing cells. Cancer Cell 2008, 13:105-116.
38. Wu J., Dombi E., Jousma E., Scott Dunn R., Lindquist D., Schnell B.M., Kim M.O., Kim A., Widemann B.C., Cripe T.P., Ratner N. Preclincial testing of sorafenib and RAD001 in the Nf(flox/flox); DhhCre mouse model of plexiform neurofibroma using magnetic resonance imaging. Pediatr. Blood Cancer 2012, 58:173-180.
39. Wu J., Patmore D.M., Jousma E., Eaves D.W., Breving K., Patel A.V., Schwartz E.B., Fuchs J.R., Cripe T.P., Stemmer-Rachamimov A.O., Ratner N. EGFR-STAT3 signaling promotes formation of malignant peripheral nerve sheath tumors. Oncogene 2014, 33:173-180.
40. Zhu Y., Ghosh P., Charnay P., Burns D.K., Parada L.F. Neurofibromas in NF1: Schwann cell origin and role of tumor environment. Science 2002, 296:920-922.