1932

Abstract

The SWI/SNF complexes, initially identified in yeast 20 years ago, are a family of multi-subunit complexes that use the energy of adenosine triphosphate (ATP) hydrolysis to remodel nucleosomes. Chromatin remodeling processes mediated by the SWI/SNF complexes are critical to the modulation of gene expression across a variety of cellular processes, including stemness, differentiation, and proliferation. The first evidence of the involvement of these complexes in carcinogenesis was provided by the identification of biallelic, truncating mutations of the gene in malignant rhabdoid tumors, a highly aggressive childhood cancer. Subsequently, genome-wide sequencing technologies have identified mutations in genes encoding different subunits of the SWI/SNF complexes in a large number of tumors. / mutations, and the subsequent abnormal function of SWI/SNF complexes, are among the most frequent gene alterations in cancer. The mechanisms by which perturbation of the SWI/SNF complexes promote oncogenesis are not fully elucidated; however, alterations of / genes obviously play a major part in cancer development, progression, and/or resistance to therapy.

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2015-01-24
2024-03-28
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Literature Cited

  1. Gui Y, Guo G, Huang Y, Hu X, Tang A. 1.  et al. 2011. Frequent mutations of chromatin remodeling genes in transitional cell carcinoma of the bladder. Nat. Genet. 43:9875–78 [Google Scholar]
  2. Guo G, Sun X, Chen C, Wu S, Huang P. 2.  et al. 2013. Whole-genome and whole-exome sequencing of bladder cancer identifies frequent alterations in genes involved in sister chromatid cohesion and segregation. Nat. Genet. 45:121459–63 [Google Scholar]
  3. Versteege I, Sévenet N, Lange J, Rousseau-Merck MF, Ambros P. 3.  et al. 1998. Truncating mutations of hSNF5/INI1 in aggressive paediatric cancer. Nature 394:6689203–6 [Google Scholar]
  4. Sévenet N, Sheridan E, Amram D, Schneider P, Handgretinger R, Delattre O. 4.  1999. Constitutional mutations of the hSNF5/INI1 gene predispose to a variety of cancers. Am. J. Hum. Genet. 65:51342–48 [Google Scholar]
  5. Kadoch C, Hargreaves DC, Hodges C, Elias L, Ho L. 5.  et al. 2013. Proteomic and bioinformatic analysis of mammalian SWI/SNF complexes identifies extensive roles in human malignancy. Nat. Genet. 45:6592–601 [Google Scholar]
  6. Neigeborn L, Carlson M. 6.  1984. Genes affecting the regulation of suc2 gene expression by glucose repression in Saccharomyces cerevisiae. Genetics 108:4845–58 [Google Scholar]
  7. Haber JE, Garvik B. 7.  1977. A new gene affecting the efficiency of mating-type interconversions in homothallic strains of Saccharomyces cerevisiae. Genetics 87:133–50 [Google Scholar]
  8. Peterson CL, Herskowitz I. 8.  1992. Characterization of the yeast SWI1, SWI2, and SWI3 genes, which encode a global activator of transcription. Cell 68:3573–83 [Google Scholar]
  9. Khavari PA, Peterson CL, Tamkun JW, Mendel DB, Crabtree GR. 9.  1993. BRG1 contains a conserved domain of the SWI2/SNF2 family necessary for normal mitotic growth and transcription. Nature 366:6451170–74 [Google Scholar]
  10. Mohrmann L, Verrijzer CP. 10.  2005. Composition and functional specificity of SWI2/SNF2 class chromatin remodeling complexes. Biochim. Biophys. Acta 1681:2–359–73 [Google Scholar]
  11. Wang W, Côté J, Xue Y, Zhou S, Khavari PA. 11.  et al. 1996. Purification and biochemical heterogeneity of the mammalian SWI/SNF complex. EMBO J. 15:195370–82 [Google Scholar]
  12. Gutiérrez J, Paredes R, Cruzat F, Hill DA, van Wijnen AJ. 12.  et al. 2007. Chromatin remodeling by SWI/SNF results in nucleosome mobilization to preferential positions in the rat osteocalcin gene promoter. J. Biol. Chem. 282:139445–57 [Google Scholar]
  13. Whitehouse I, Flaus A, Cairns BR, White MF, Workman JL, Owen-Hughes T. 13.  1999. Nucleosome mobilization catalysed by the yeast SWI/SNF complex. Nature 400:6746784–87 [Google Scholar]
  14. Lu P, Roberts CWM. 14.  2013. The SWI/SNF tumor suppressor complex: regulation of promoter nucleosomes and beyond. Nucleus 4:5374–78 [Google Scholar]
  15. Tolstorukov MY, Sansam CG, Lu P, Koellhoffer EC, Helming KC. 15.  et al. 2013. SWI/SNF chromatin remodeling/tumor suppressor complex establishes nucleosome occupancy at target promoters. PNAS 110:2510165–70 [Google Scholar]
  16. King HA, Trotter KW, Archer TK. 16.  2012. Chromatin remodeling during glucocorticoid receptor regulated transactivation. Biochim. Biophys. Acta 1819:7716–26 [Google Scholar]
  17. Ford E, Thanos D. 17.  2010. The transcriptional code of human IFN-β gene expression. Biochim. Biophys. Acta 17993–4328–36
  18. Rafati H, Parra M, Hakre S, Moshkin Y, Verdin E, Mahmoudi T. 18.  2011. Repressive LTR nucleosome positioning by the BAF complex is required for HIV latency. PLOS Biol. 9:11e1001206 [Google Scholar]
  19. De la Serna IL, Carlson KA, Imbalzano AN. 19.  2001. Mammalian SWI/SNF complexes promote MyoD-mediated muscle differentiation. Nat. Genet. 27:2187–90 [Google Scholar]
  20. Gresh L, Bourachot B, Reimann A, Guigas B, Fiette L. 20.  et al. 2005. The SWI/SNF chromatin-remodeling complex subunit SNF5 is essential for hepatocyte differentiation. EMBO J. 24:183313–24 [Google Scholar]
  21. Lessard J, Wu JI, Ranish JA, Wan M, Winslow MM. 21.  et al. 2007. An essential switch in subunit composition of a chromatin remodeling complex during neural development. Neuron 55:2201–15 [Google Scholar]
  22. Kia SK, Gorski MM, Giannakopoulos S, Verrijzer CP. 22.  2008. SWI/SNF mediates polycomb eviction and epigenetic reprogramming of the INK4B-ARF-INK4A locus. Mol. Cell. Biol. 28:103457–64 [Google Scholar]
  23. Versteege I, Medjkane S, Rouillard D, Delattre O. 23.  2002. A key role of the hSNF5/INI1 tumour suppressor in the control of the G1-S transition of the cell cycle. Oncogene 21:426403–12 [Google Scholar]
  24. Cheng SW, Davies KP, Yung E, Beltran RJ, Yu J, Kalpana GV. 24.  1999. C-MYC interacts with hSNF5/INI1 and requires the SWI/SNF complex for transactivation function. Nat. Genet. 22:1102–5 [Google Scholar]
  25. Jagani Z, Mora-Blanco EL, Sansam CG, McKenna ES, Wilson B. 25.  et al. 2010. Loss of the tumor suppressor SNF5 leads to aberrant activation of the hedgehog-GLI pathway. Nat. Med. 16:121429–33 [Google Scholar]
  26. Caramel J, Quignon F, Delattre O. 26.  2008. RhoA-dependent regulation of cell migration by the tumor suppressor hSNF5/INI1. Cancer Res. 68:156154–61 [Google Scholar]
  27. Wilson BG, Wang X, Shen X, McKenna ES, Lemieux ME. 27.  et al. 2010. Epigenetic antagonism between polycomb and SWI/SNF complexes during oncogenic transformation. Cancer Cell 18:4316–28 [Google Scholar]
  28. Flajollet S, Lefebvre B, Cudejko C, Staels B, Lefebvre P. 28.  2007. The core component of the mammalian SWI/SNF complex SMARCD3/BAF60c is a coactivator for the nuclear retinoic acid receptor. Mol. Cell Endocrinol. 270:1–223–32 [Google Scholar]
  29. Salma N, Xiao H, Mueller E, Imbalzano AN. 29.  2004. Temporal recruitment of transcription factors and SWI/SNF chromatin-remodeling enzymes during adipogenic induction of the peroxisome proliferator-activated receptor gamma nuclear hormone receptor. Mol. Cell. Biol. 24:114651–63 [Google Scholar]
  30. Chiba H, Muramatsu M, Nomoto A, Kato H. 30.  1994. Two human homologues of Saccharomyces cerevisiae SWI2/SNF2 and Drosophila brahma are transcriptional coactivators cooperating with the estrogen receptor and the retinoic acid receptor. Nucleic Acids Res. 22:101815–20 [Google Scholar]
  31. Debril M-B, Gelman L, Fayard E, Annicotte J-S, Rocchi S, Auwerx J. 31.  2004. Transcription factors and nuclear receptors interact with the SWI/SNF complex through the BAF60C subunit. J. Biol. Chem. 279:1616677–86 [Google Scholar]
  32. Pedersen TA, Kowenz-Leutz E, Leutz A, Nerlov C. 32.  2001. Cooperation between C/EBPα TBP/TFIIB and SWI/SNF recruiting domains is required for adipocyte differentiation. Genes Dev. 15:233208–16 [Google Scholar]
  33. Young DW, Pratap J, Javed A, Weiner B, Ohkawa Y. 33.  et al. 2005. SWI/SNF chromatin remodeling complex is obligatory for BMP2-induced, RUNX2-dependent skeletal gene expression that controls osteoblast differentiation. J. Cell. Biochem. 94:4720–30 [Google Scholar]
  34. Haas JE, Palmer NF, Weinberg AG, Beckwith JB. 34.  1981. Ultrastructure of malignant rhabdoid tumor of the kidney. A distinctive renal tumor of children. Hum. Pathol. 12:7646–57 [Google Scholar]
  35. Tsuneyoshi M, Daimaru Y, Hashimoto H, Enjoji M. 35.  1985. Malignant soft tissue neoplasms with the histologic features of renal rhabdoid tumors: an ultrastructural and immunohistochemical study. Hum. Pathol. 16:121235–42 [Google Scholar]
  36. Rorke LB, Packer RJ, Biegel JA. 36.  1996. Central nervous system atypical teratoid/rhabdoid tumors of infancy and childhood: definition of an entity. J. Neurosurg. 85:156–65 [Google Scholar]
  37. Trobaugh-Lotrario AD, Tomlinson GE, Finegold MJ, Gore L, Feusner JH. 37.  2009. Small cell undifferentiated variant of hepatoblastoma: adverse clinical and molecular features similar to rhabdoid tumors. Pediatr. Blood Cancer 52:3328–34 [Google Scholar]
  38. Rizzo D, Fréneaux P, Brisse H, Louvrier C, Lequin D. 38.  et al. 2012. SMARCB1 deficiency in tumors from the peripheral nervous system: a link between schwannomas and rhabdoid tumors?. Am. J. Surg. Pathol. 36:7964–72 [Google Scholar]
  39. Sévenet N, Lellouch-Tubiana A, Schofield D, Hoang-Xuan K, Gessler M. 39.  et al. 1999. Spectrum of hSNF5/INI1 somatic mutations in human cancer and genotype-phenotype correlations. Hum. Mol. Genet. 8:132359–68 [Google Scholar]
  40. Biegel JA, Zhou JY, Rorke LB, Stenstrom C, Wainwright LM, Fogelgren B. 40.  1999. Germ-line and acquired mutations of INI1 in atypical teratoid and rhabdoid tumors. Cancer Res. 59:174–79 [Google Scholar]
  41. Lee RS, Stewart C, Carter SL, Ambrogio L, Cibulskis K. 41.  et al. 2012. A remarkably simple genome underlies highly malignant pediatric rhabdoid cancers. J. Clin. Investig. 122:82983–88 [Google Scholar]
  42. Vogelstein B, Papadopoulos N, Velculescu VE, Zhou S, Diaz LA Jr, Kinzler KW. 42.  2013. Cancer genome landscapes. Science 339:61271546–58 [Google Scholar]
  43. Bourdeaut F, Fréneaux P, Thuille B, Lellouch-Tubiana A, Nicolas A. 43.  et al. 2007. hSNF5/INI1-deficient tumours and rhabdoid tumours are convergent but not fully overlapping entities. J. Pathol. 211:3323–30 [Google Scholar]
  44. Hoot AC, Russo P, Judkins AR, Perlman EJ, Biegel JA. 44.  2004. Immunohistochemical analysis of hSNF5/INI1 distinguishes renal and extra-renal malignant rhabdoid tumors from other pediatric soft tissue tumors. Am. J. Surg. Pathol. 28:111485–91 [Google Scholar]
  45. Bourdeaut F, Lequin D, Brugières L, Reynaud S, Dufour C. 45.  et al. 2011. Frequent hSNF5/INI1 germline mutations in patients with rhabdoid tumor. Clin. Cancer Res. 17:131–38 [Google Scholar]
  46. Eaton KW, Tooke LS, Wainwright LM, Judkins AR, Biegel JA. 46.  2011. Spectrum of SMARCB1/INI1 mutations in familial and sporadic rhabdoid tumors. Pediatr. Blood Cancer 56:17–15 [Google Scholar]
  47. Lafay-Cousin L, Payne E, Strother D, Chernos J, Chan M, Bernier FP. 47.  2009. Goldenhar phenotype in a child with distal 22q11.2 deletion and intracranial atypical teratoid rhabdoid tumor. Am. J. Med. Genet. A 149A122855–59
  48. Jackson EM, Shaikh TH, Gururangan S, Jones MC, Malkin D. 48.  et al. 2007. High-density single nucleotide polymorphism array analysis in patients with germline deletions of 22q11.2 and malignant rhabdoid tumor. Hum. Genet. 122:2117–27 [Google Scholar]
  49. Taylor MD, Gokgoz N, Andrulis IL, Mainprize TG, Drake JM, Rutka JT. 49.  2000. Familial posterior fossa brain tumors of infancy secondary to germline mutation of the hSNF5 gene. Am. J. Hum. Genet. 66:41403–6 [Google Scholar]
  50. Janson K, Nedzi LA, David O, Schorin M, Walsh JW. 50.  et al. 2006. Predisposition to atypical teratoid/rhabdoid tumor due to an inherited INI1 mutation. Pediatr. Blood Cancer 47:3279–84 [Google Scholar]
  51. Bruggers CS, Bleyl SB, Pysher T, Barnette P, Afify Z. 51.  et al. 2011. Clinicopathologic comparison of familial versus sporadic atypical teratoid/rhabdoid tumors (AT/RT) of the central nervous system. Pediatr. Blood Cancer 56:71026–31 [Google Scholar]
  52. Ammerlaan ACJ, Ararou A, Houben MPWA, Baas F, Tijssen CC. 52.  et al. 2008. Long-term survival and transmission of INI1-mutation via nonpenetrant males in a family with rhabdoid tumour predisposition syndrome. Br. J. Cancer 98:2474–79 [Google Scholar]
  53. Forest F, David A, Arrufat S, Pierron G, Ranchere-Vince D. 53.  et al. 2012. Conventional chondrosarcoma in a survivor of rhabdoid tumor: enlarging the spectrum of tumors associated with SMARCB1 germline mutations. Am. J. Surg. Pathol. 36:121892–96 [Google Scholar]
  54. Hulsebos TJM, Kenter S, Siebers-Renelt U, Hans V, Wesseling P, Flucke U. 54.  2014. SMARCB1 involvement in the development of leiomyoma in a patient with schwannomatosis. Am. J. Surg. Pathol. 38:3421–25 [Google Scholar]
  55. Hulsebos TJM, Plomp AS, Wolterman RA, Robanus-Maandag EC, Baas F, Wesseling P. 55.  2007. Germline mutation of INI1/SMARCB1 in familial schwannomatosis. Am. J. Hum. Genet. 80:4805–10 [Google Scholar]
  56. Sestini R, Bacci C, Provenzano A, Genuardi M, Papi L. 56.  2008. Evidence of a four-hit mechanism involving SMARCB1 and NF2 in schwannomatosis-associated Schwannomas. Hum. Mutat. 29:2227–31 [Google Scholar]
  57. Smith MJ, Wallace AJ, Bowers NL, Rustad CF, Woods CG. 57.  et al. 2012. Frequency of SMARCB1 mutations in familial and sporadic schwannomatosis. Neurogenetics 13:2141–45 [Google Scholar]
  58. Rousseau G, Noguchi T, Bourdon V, Sobol H, Olschwang S. 58.  2011. SMARCB1/INI1 germline mutations contribute to 10% of sporadic schwannomatosis. BMC Neurol. 11:9 [Google Scholar]
  59. Smith MJ, Walker JA, Shen Y, Stemmer-Rachamimov A, Gusella JF, Plotkin SR. 59.  2012. Expression of SMARCB1 (INI1) mutations in familial schwannomatosis. Hum. Mol. Genet. 21:245239–45 [Google Scholar]
  60. Swensen JJ, Keyser J, Coffin CM, Biegel JA, Viskochil DH, Williams MS. 60.  2009. Familial occurrence of schwannomas and malignant rhabdoid tumour associated with a duplication in SMARCB1. J. Med. Genet. 46:168–72 [Google Scholar]
  61. Bacci C, Sestini R, Provenzano A, Paganini I, Mancini I. 61.  et al. 2010. Schwannomatosis associated with multiple meningiomas due to a familial SMARCB1 mutation. Neurogenetics 11:173–80 [Google Scholar]
  62. Christiaans I, Kenter SB, Brink HC, van Os TAM, Baas F. 62.  et al. 2011. Germline SMARCB1 mutation and somatic NF2 mutations in familial multiple meningiomas. J. Med. Genet. 48:293–97 [Google Scholar]
  63. Boyd C, Smith MJ, Kluwe L, Balogh A, Maccollin M, Plotkin SR. 63.  2008. Alterations in the SMARCB1 (INI1) tumor suppressor gene in familial schwannomatosis. Clin. Genet. 74:4358–66 [Google Scholar]
  64. Schmitz U, Mueller W, Weber M, Sévenet N, Delattre O, von Deimling A. 64.  2001. INI1 mutations in meningiomas at a potential hotspot in exon 9. Br. J. Cancer 84:2199–201 [Google Scholar]
  65. Clark VE, Erson-Omay EZ, Serin A, Yin J, Cotney J. 65.  et al. 2013. Genomic analysis of non-NF2 meningiomas reveals mutations in TRAF7, KLF4, AKT1, and SMO. Science 339:61231077–80 [Google Scholar]
  66. Hornick JL, Dal Cin P, Fletcher CDM. 66.  2009. Loss of INI1 expression is characteristic of both conventional and proximal-type epithelioid sarcoma. Am. J. Surg. Pathol. 33:4542–50 [Google Scholar]
  67. Hollmann TJ, Hornick JL. 67.  2011. INI1-deficient tumors: diagnostic features and molecular genetics. Am. J. Surg. Pathol. 35:10e47–63 [Google Scholar]
  68. Chbani L, Guillou L, Terrier P, Decouvelaere AV, Grégoire F. 68.  et al. 2009. Epithelioid sarcoma: a clinicopathologic and immunohistochemical analysis of 106 cases from the French sarcoma group. Am. J. Clin. Pathol. 131:2222–27 [Google Scholar]
  69. Modena P, Lualdi E, Facchinetti F, Galli L, Teixeira MR. 69.  et al. 2005. SMARCB1/INI1 tumor suppressor gene is frequently inactivated in epithelioid sarcomas. Cancer Res. 65:104012–19 [Google Scholar]
  70. Sullivan LM, Folpe AL, Pawel BR, Judkins AR, Biegel JA. 70.  2013. Epithelioid sarcoma is associated with a high percentage of SMARCB1 deletions. Mod. Pathol. 26:3385–92 [Google Scholar]
  71. Flucke U, Slootweg PJ, Mentzel T, Pauwels P, Hulsebos TJM. 71.  2009. Re: infrequent SMARCB1/INI1 gene alteration in epithelioid sarcoma: a useful tool in distinguishing epithelioid sarcoma from malignant rhabdoid tumor: direct evidence of mutational inactivation of SMARCB1/INI1 in epithelioid sarcoma. Hum. Pathol. 40:91361–64 [Google Scholar]
  72. Kohashi K, Izumi T, Oda Y, Yamamoto H, Tamiya S. 72.  et al. 2009. Infrequent SMARCB1/INI1 gene alteration in epithelioid sarcoma: a useful tool in distinguishing epithelioid sarcoma from malignant rhabdoid tumor. Hum. Pathol. 40:3349–55 [Google Scholar]
  73. Kohashi K, Oda Y, Yamamoto H, Tamiya S, Oshiro Y. 73.  et al. 2008. SMARCB1/INI1 protein expression in round cell soft tissue sarcomas associated with chromosomal translocations involving EWS: a special reference to SMARCB1/INI1 negative variant extraskeletal myxoid chondrosarcoma. Am. J. Surg. Pathol. 32:81168–74 [Google Scholar]
  74. Liu Q, Galli S, Srinivasan R, Linehan WM, Tsokos M, Merino MJ. 74.  2013. Renal medullary carcinoma: molecular, immunohistochemistry, and morphologic correlation. Am. J. Surg. Pathol. 37:3368–74 [Google Scholar]
  75. Calderaro J, Moroch J, Pierron G, Pedeutour F, Grison C. 75.  et al. 2012. SMARCB1/INI1 inactivation in renal medullary carcinoma. Histopathology 61:3428–35 [Google Scholar]
  76. Kreiger PA, Judkins AR, Russo PA, Biegel JA, Lestini BJ. 76.  et al. 2009. Loss of INI1 expression defines a unique subset of pediatric undifferentiated soft tissue sarcomas. Mod. Pathol. 22:1142–50 [Google Scholar]
  77. Hasselblatt M, Oyen F, Gesk S, Kordes U, Wrede B. 77.  et al. 2009. Cribriform neuroepithelial tumor (CRINET): a nonrhabdoid ventricular tumor with INI1 loss and relatively favorable prognosis. J. Neuropathol. Exp. Neurol. 68:121249–55 [Google Scholar]
  78. Mobley BC, McKenney JK, Bangs CD, Callahan K, Yeom KW. 78.  et al. 2010. Loss of SMARCB1/INI1 expression in poorly differentiated chordomas. Acta Neuropathol. 120:6745–53 [Google Scholar]
  79. Agaimy A, Koch M, Lell M, Semrau S, Dudek W. 79.  et al. 2014. SMARCB1 (INI1)-deficient sinonasal basaloid carcinoma: a novel member of the expanding family of SMARCB1-deficient neoplasms. Am. J. Surg. Pathol. 38:91274–81 [Google Scholar]
  80. Bishop JA, Antonescu CR, Westra WH. 80.  2014. SMARCB1 (INI-1)-deficient carcinomas of the sinonasal tract. Am. J. Surg. Pathol. 38:91282–89 [Google Scholar]
  81. Schneppenheim R, Frühwald MC, Gesk S, Hasselblatt M, Jeibmann A. 81.  et al. 2010. Germline nonsense mutation and somatic inactivation of SMARCA4/BGRG1 in a family with rhabdoid tumor predisposition syndrome. Am. J. Hum. Genet. 86:2279–84 [Google Scholar]
  82. Witkowski L, Lalonde E, Zhang J, Albrecht S, Hamel N. 82.  et al. 2013. Familial rhabdoid tumour “avant la lettre”—from pathology review to exome sequencing and back again. J. Pathol. 231:135–43 [Google Scholar]
  83. Smith MJ, O'Sullivan J, Bhaskar SS, Hadfield KD, Poke G. 83.  et al. 2013. Loss-of-function mutations in SMARCE1 cause an inherited disorder of multiple spinal meningiomas. Nat. Genet. 45:3295–98 [Google Scholar]
  84. Tsurusaki Y, Okamoto N, Ohashi H, Kosho T, Imai Y. 84.  et al. 2012. Mutations affecting components of the SWI/SNF complex cause Coffin–Siris syndrome. Nat. Genet. 44:4376–78 [Google Scholar]
  85. Van Houdt JKJ, Nowakowska BA, Sousa SB, van Schaik BDC, Seuntjens E. 85.  et al. 2012. Heterozygous missense mutations in SMARCA2 cause Nicolaides–Baraitser syndrome. Nat. Genet. 44:4445–49 [Google Scholar]
  86. Ho AS, Kannan K, Roy DM, Morris LGT, Ganly I. 86.  et al. 2013. The mutational landscape of adenoid cystic carcinoma. Nat. Genet. 45:7791–98 [Google Scholar]
  87. Love C, Sun Z, Jima D, Li G, Zhang J. 87.  et al. 2012. The genetic landscape of mutations in Burkitt lymphoma. Nat. Genet. 44:121321–25 [Google Scholar]
  88. Imielinski M, Berger AH, Hammerman PS, Hernandez B, Pugh TJ. 88.  et al. 2012. Mapping the hallmarks of lung adenocarcinoma with massively parallel sequencing. Cell 150:61107–20 [Google Scholar]
  89. Dulak AM, Stojanov P, Peng S, Lawrence MS, Fox C. 89.  et al. 2013. Exome and whole-genome sequencing of esophageal adenocarcinoma identifies recurrent driver events and mutational complexity. Nat. Genet. 45:5478–86 [Google Scholar]
  90. Parsons DW, Li M, Zhang X, Jones S, Leary RJ. 90.  et al. 2011. The genetic landscape of the childhood cancer medulloblastoma. Science 331:6016435–39 [Google Scholar]
  91. Jones DTW, Jäger N, Kool M, Zichner T, Hutter B. 91.  et al. 2012. Dissecting the genomic complexity underlying medulloblastoma. Nature 488:7409100–5 [Google Scholar]
  92. Pugh TJ, Weeraratne SD, Archer TC, Pomeranz Krummel DA, Auclair D. 92.  et al. 2012. Medulloblastoma exome sequencing uncovers subtype-specific somatic mutations. Nature 488:7409106–10 [Google Scholar]
  93. Dykhuizen EC, Hargreaves DC, Miller EL, Cui K, Korshunov A. 93.  et al. 2013. BAF complexes facilitate decatenation of DNA by topoisomerase IIα. Nature 497:7451624–27 [Google Scholar]
  94. Jelinic P, Mueller JJ, Olvera N, Dao F, Scott SN. 94.  et al. 2014. Recurrent SMARCA4 mutations in small cell carcinoma of the ovary. Nat. Genet. 46:5424–26 [Google Scholar]
  95. Witkowski L, Carrot-Zhang J, Albrecht S, Fahiminiya S, Hamel N. 95.  et al. 2014. Germline and somatic SMARCA4 mutations characterize small cell carcinoma of the ovary, hypercalcemic type. Nat. Genet. 46:5438–43 [Google Scholar]
  96. Ramos P, Karnezis AN, Craig DW, Sekulic A, Russell ML. 96.  et al. 2014. Small cell carcinoma of the ovary, hypercalcemic type, displays frequent inactivating germline and somatic mutations in SMARCA4. Nat. Genet. 46:5427–29 [Google Scholar]
  97. Jones S, Wang T-L, Shih I-M, Mao T-L, Nakayama K. 97.  et al. 2010. Frequent mutations of chromatin remodeling gene ARID1A in ovarian clear cell carcinoma. Science 330:6001228–31 [Google Scholar]
  98. Wiegand KC, Shah SP, Al-Agha OM, Zhao Y, Tse K. 98.  et al. 2010. ARID1A mutations in endometriosis-associated ovarian carcinomas. N. Engl. J. Med. 363:161532–43 [Google Scholar]
  99. Katagiri A, Nakayama K, Rahman MT, Rahman M, Katagiri H. 99.  et al. 2012. Loss of ARID1A expression is related to shorter progression-free survival and chemoresistance in ovarian clear cell carcinoma. Mod. Pathol. 25:2282–88 [Google Scholar]
  100. Liang H, Cheung LWT, Li J, Ju Z, Yu S. 100.  et al. 2012. Whole-exome sequencing combined with functional genomics reveals novel candidate driver cancer genes in endometrial cancer. Genome Res. 22:112120–29 [Google Scholar]
  101. 101. Cancer Genome Atlas Res. Netw. 2013. Integrated genomic characterization of endometrial carcinoma. Nature 497:744767–73 [Google Scholar]
  102. Le Gallo M, O'Hara AJ, Rudd ML, Urick ME, Hansen NF. 102.  et al. 2012. Exome sequencing of serous endometrial tumors identifies recurrent somatic mutations in chromatin-remodeling and ubiquitin ligase complex genes. Nat. Genet. 44:121310–15 [Google Scholar]
  103. Guichard C, Amaddeo G, Imbeaud S, Ladeiro Y, Pelletier L. 103.  et al. 2012. Integrated analysis of somatic mutations and focal copy-number changes identifies key genes and pathways in hepatocellular carcinoma. Nat. Genet. 44:6694–98 [Google Scholar]
  104. Huang J, Deng Q, Wang Q, Li K-Y, Dai J-H. 104.  et al. 2012. Exome sequencing of hepatitis B virus-associated hepatocellular carcinoma. Nat. Genet. 44:101117–21 [Google Scholar]
  105. 105. Cancer Genome Atlas Res. Netw. 2012. Comprehensive genomic characterization of squamous cell lung cancers. Nature 489:7417519–25 [Google Scholar]
  106. Wang K, Kan J, Yuen ST, Shi ST, Chu KM. 106.  et al. 2011. Exome sequencing identifies frequent mutation of ARID1A in molecular subtypes of gastric cancer. Nat. Genet. 43:121219–23 [Google Scholar]
  107. Zang ZJ, Cutcutache I, Poon SL, Zhang SL, McPherson JR. 107.  et al. 2012. Exome sequencing of gastric adenocarcinoma identifies recurrent somatic mutations in cell adhesion and chromatin remodeling genes. Nat. Genet. 44:5570–74 [Google Scholar]
  108. 108. Cancer Genome Atlas Netw 2012. Comprehensive molecular characterization of human colon and rectal cancer. Nature 487:7407330–37 [Google Scholar]
  109. Biankin AV, Waddell N, Kassahn KS, Gingras M-C, Muthuswamy LB. 109.  et al. 2012. Pancreatic cancer genomes reveal aberrations in axon guidance pathway genes. Nature 491:7424399–405 [Google Scholar]
  110. Jiao Y, Yonescu R, Offerhaus GJA, Klimstra DS, Maitra A. 110.  et al. 2014. Whole-exome sequencing of pancreatic neoplasms with acinar differentiation. J. Pathol. 232:4428–35 [Google Scholar]
  111. Jiao Y, Pawlik TM, Anders RA, Selaru FM, Streppel MM. 111.  et al. 2013. Exome sequencing identifies frequent inactivating mutations in BAP1, ARID1A and PBRM1 in intrahepatic cholangiocarcinomas. Nat. Genet. 45:121470–73 [Google Scholar]
  112. Treon SP, Xu L, Yang G, Zhou Y, Liu X. 112.  et al. 2012. MYD88 L265P somatic mutation in Waldenström's macroglobulinemia. N. Engl. J. Med. 367:9826–33 [Google Scholar]
  113. Sausen M, Leary RJ, Jones S, Wu J, Reynolds CP. 113.  et al. 2013. Integrated genomic analyses identify ARID1A and ARID1B alterations in the childhood cancer neuroblastoma. Nat. Genet. 45:112–17 [Google Scholar]
  114. Li M, Zhao H, Zhang X, Wood LD, Anders RA. 114.  et al. 2011. Inactivating mutations of the chromatin remodeling gene ARID2 in hepatocellular carcinoma. Nat. Genet. 43:9828–29 [Google Scholar]
  115. Fujimoto A, Totoki Y, Abe T, Boroevich KA, Hosoda F. 115.  et al. 2012. Whole-genome sequencing of liver cancers identifies etiological influences on mutation patterns and recurrent mutations in chromatin regulators. Nat. Genet. 44:7760–64 [Google Scholar]
  116. Manceau G, Letouzé E, Guichard C, Didelot A, Cazes A. 116.  et al. 2013. Recurrent inactivating mutations of ARID2 in non-small cell lung carcinoma. Int. J. Cancer 132:92217–21 [Google Scholar]
  117. Hodis E, Watson IR, Kryukov GV, Arold ST, Imielinski M. 117.  et al. 2012. A landscape of driver mutations in melanoma. Cell 150:2251–63 [Google Scholar]
  118. 118. India Proj. Team Int. Cancer Genome Consort 2013. Mutational landscape of gingivo-buccal oral squamous cell carcinoma reveals new recurrently-mutated genes and molecular subgroups. Nat. Commun. 4:2873 [Google Scholar]
  119. Guo G, Gui Y, Gao S, Tang A, Hu X. 119.  et al. 2012. Frequent mutations of genes encoding ubiquitin-mediated proteolysis pathway components in clear cell renal cell carcinoma. Nat. Genet. 44:117–19 [Google Scholar]
  120. Sato Y, Yoshizato T, Shiraishi Y, Maekawa S, Okuno Y. 120.  et al. 2013. Integrated molecular analysis of clear-cell renal cell carcinoma. Nat. Genet. 45:8860–67 [Google Scholar]
  121. 121. Cancer Genome Atlas Res. Netw 2013. Comprehensive molecular characterization of clear cell renal cell carcinoma. Nature 499:745643–49 [Google Scholar]
  122. Varela I, Tarpey P, Raine K, Huang D, Ong CK. 122.  et al. 2011. Exome sequencing identifies frequent mutation of the SWI/SNF complex gene PBRM1 in renal carcinoma. Nature 469:7331539–42 [Google Scholar]
  123. Kapur P, Peña-Llopis S, Christie A, Zhrebker L, Pavía-Jiménez A. 123.  et al. 2013. Effects on survival of BAP1 and PBRM1 mutations in sporadic clear-cell renal-cell carcinoma: a retrospective analysis with independent validation. Lancet Oncol. 14:2159–67 [Google Scholar]
  124. De Keersmaecker K, Real PJ, Gatta GD, Palomero T, Sulis ML. 124.  et al. 2010. The TLX1 oncogene drives aneuploidy in T cell transformation. Nat. Med. 16:111321–27 [Google Scholar]
  125. Satterwhite E, Sonoki T, Willis TG, Harder L, Nowak R. 125.  et al. 2001. The BCL11 gene family: involvement of BCL11A in lymphoid malignancies. Blood 98:123413–20 [Google Scholar]
  126. Zani VJ, Asou N, Jadayel D, Heward JM, Shipley J. 126.  et al. 1996. Molecular cloning of complex chromosomal translocation t(8;14;12)(q24.1;q32.3;q24.1) in a Burkitt lymphoma cell line defines a new gene (BCL7A) with homology to caldesmon. Blood 87:83124–34 [Google Scholar]
  127. Van Doorn R, Zoutman WH, Dijkman R, de Menezes RX, Commandeur S. 127.  et al. 2005. Epigenetic profiling of cutaneous T-cell lymphoma: promoter hypermethylation of multiple tumor suppressor genes including BCL7a, PTPRG, and p73. J. Clin. Oncol. 23:173886–96 [Google Scholar]
  128. Naka N, Takenaka S, Araki N, Miwa T, Hashimoto N. 128.  et al. 2010. Synovial sarcoma is a stem cell malignancy. Stem Cells 28:71119–31 [Google Scholar]
  129. Kohashi K, Oda Y, Yamamoto H, Tamiya S, Matono H. 129.  et al. 2010. Reduced expression of SMARCB1/INI1 protein in synovial sarcoma. Mod. Pathol. 23:7981–90 [Google Scholar]
  130. Kadoch C, Crabtree GR. 130.  2013. Reversible disruption of mSWI/SNF (BAF) complexes by the SS18-SSX oncogenic fusion in synovial sarcoma. Cell 153:171–85 [Google Scholar]
  131. Zorludemir S, Scheithauer BW, Hirose T, Van Houten C, Miller G, Meyer FB. 131.  1995. Clear cell meningioma. A clinicopathologic study of a potentially aggressive variant of meningioma. Am. J. Surg. Pathol. 19:5493–505 [Google Scholar]
  132. Mackay B, Ordónez NG, Khoursand J, Bennington JL. 132.  1987. The ultrastructure and immunocytochemistry of renal cell carcinoma. Ultrastruct. Pathol. 11:5–6483–502 [Google Scholar]
  133. Ohkawa K, Amasaki H, Terashima Y, Aizawa S, Ishikawa E. 133.  1977. Clear cell carcinoma of the ovary: light and electron microscopic studies. Cancer 40:63019–29 [Google Scholar]
  134. Kwon TJ, Ro JY, Tornos C, Ordonez NG. 134.  1996. Reduplicated basal lamina in clear-cell carcinoma of the ovary: an immunohistochemical and electron microscopic study. Ultrastruct. Pathol. 20:6529–36 [Google Scholar]
  135. Kurman RJ, Scully RE. 135.  1976. Clear cell carcinoma of the endometrium: an analysis of 21 cases. Cancer 37:2872–82 [Google Scholar]
  136. Matias-Guiu X, Lerma E, Prat J. 136.  1997. Clear cell tumors of the female genital tract. Semin. Diagn. Pathol. 14:4233–39 [Google Scholar]
  137. Steinberg P, Störkel S, Oesch F, Thoenes W. 137.  1992. Carbohydrate metabolism in human renal clear cell carcinomas. Lab. Investig. 67:4506–11 [Google Scholar]
  138. Wang L, Zhao Z, Meyer MB, Saha S, Yu M. 138.  et al. 2014. Carm1 methylates chromatin remodeling factor BAF155 to enhance tumor progression and metastasis. Cancer Cell 25:121–36 [Google Scholar]
  139. Wang S-CM, Dowhan DH, Eriksson NA, Muscat GEO. 139.  2012. CARM1/PRMT4 is necessary for the glycogen gene expression programme in skeletal muscle cells. Biochem. J. 444:2323–31 [Google Scholar]
  140. Gresh L, Bourachot B, Reimann A, Guigas B, Fiette L. 140.  et al. 2005. The SWI/SNF chromatin-remodeling complex subunit SNF5 is essential for hepatocyte differentiation. EMBO J. 24:183313–24 [Google Scholar]
  141. Helming KC, Wang X, Wilson BG, Vazquez F, Haswell JR. 141.  et al. 2014. ARID1B is a specific vulnerability in ARID1A-mutant cancers. Nat. Med. 20:3251–54 [Google Scholar]
  142. Oike T, Ogiwara H, Tominaga Y, Ito K, Ando O. 142.  et al. 2013. A synthetic lethality-based strategy to treat cancers harboring a genetic deficiency in the chromatin remodeling factor BRG1. Cancer Res. 73:175508–18 [Google Scholar]
  143. Hoffman GR, Rahal R, Buxton F, Xiang K, McAllister G. 143.  et al. 2014. Functional epigenetics approach identifies BRM/SMARCA2 as a critical synthetic lethal target in BRG1-deficient cancers. PNAS 111:83128–33 [Google Scholar]
  144. Prensner JR, Iyer MK, Balbin OA, Dhanasekaran SM, Cao Q. 144.  et al. 2011. Transcriptome sequencing across a prostate cancer cohort identifies PCAT-1, an unannotated lincRNA implicated in disease progression. Nat. Biotechnol. 29:8742–49 [Google Scholar]
  145. Prensner JR, Iyer MK, Sahu A, Asangani IA, Cao Q. 145.  et al. 2013. The long noncoding RNA SChLAP1 promotes aggressive prostate cancer and antagonizes the SWI/SNF complex. Nat. Genet. 45:111392–98 [Google Scholar]
  146. Gao J, Aksoy BA, Dogrusoz U, Dresdner G, Gross B. 146.  et al. 2013. Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Sci. Signal. 6:269pI1 [Google Scholar]
  147. Cerami E, Gao J, Dogrusoz U, Gross BE, Sumer SO. 147.  et al. 2012. The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov 2:5401–4 [Google Scholar]
  148. Knutson SK, Warholic NM, Wigle TJ, Klaus CR, Allain CJ. 148.  et al. 2013. Durable tumor regression in genetically altered malignant rhabdoid tumors by inhibition of methyltransferase EZH2. PNAS 110:197922–27 [Google Scholar]
  149. Lee S, Cimica V, Ramachandra N, Zagzag D, Kalpana GV. 149.  2011. Aurora A is a repressed effector target of the chromatin remodeling protein hSNF5/INI1 required for rhabdoid tumor cell survival. Cancer Res. 71:93225–35 [Google Scholar]
  150. Kerl K, Moreno N, Holsten T, Ahlfeld J, Mertins J. 150.  et al. 2014. Arsenic trioxide inhibits tumor cell growth in malignant rhabdoid tumors in vitro and in vivo by targeting overexpressed Gli1. Int. J. Cancer 135:4989–95 [Google Scholar]
  151. Filippakopoulos P, Qi J, Picaud S, Shen Y, Smith WB. 151.  et al. 2010. Selective inhibition of BET bromodomains. Nature 468:73271067–73 [Google Scholar]
  152. Delmore JE, Issa GC, Lemieux ME, Rahl PB, Shi J. 152.  et al. 2011. BET bromodomain inhibition as a therapeutic strategy to target c-MYC. Cell 146:6904–17 [Google Scholar]
  153. Tang Y, Gholamin S, Schubert S, Willardson MI, Lee A. 153.  et al. 2014. Epigenetic targeting of Hedgehog pathway transcriptional output through BET bromodomain inhibition. Nat. Med. 20:7732–40 [Google Scholar]
  154. Wang X, Sansam CG, Thom CS, Metzger D, Evans JA. 154.  et al. 2009. Oncogenesis caused by loss of the SNF5 tumor suppressor is dependent on activity of BRG1, the ATPase of the SWI/SNF chromatin remodeling complex. Cancer Res. 69:208094–101 [Google Scholar]
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