Journal of Korean Neurosurgical Society

  • 제61권3호
  • /
  • Pages.302-311
  • /
  • 2018
  • /
  • 2005-3711(pISSN)
  • /
  • 1598-7876(eISSN)
대한신경외과학회 (The Korean Neurosurgical Society)
권호 표지
DOI QR코드

DOI QR Code

Atypical Teratoid Rhabdoid Tumour : From Tumours to Therapies

  • Richardson, Elizabeth Anne (Department of Laboratory Medicine and Pathobiology, Faculty of Medicine, University of Toronto) ;
  • Ho, Ben (Arthur and Sonia Labatt Brain Tumour Research Centre, Hospital for Sick Children) ;
  • Huang, Annie (Department of Laboratory Medicine and Pathobiology, Faculty of Medicine, University of Toronto)
  • 투고 : 2018.03.16
  • 심사 : 2018.03.29
  • 발행 : 2018.05.01
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

Atypical teratoid rhabdoid tumours (ATRTs) are the most common malignant central nervous system tumours in children ${\leq}1year$ of age and represent approximately 1-2% of all pediatric brain tumours. ATRT is a primarily monogenic disease characterized by the bi-allelic loss of the SMARCB1 gene, which encodes the hSNF5 subunit of the SWI/SNF chromatin remodeling complex. Though conventional dose chemotherapy is not effective in most ATRT patients, high dose chemotherapy with autologous stem cell transplant, radiotherapy and/or intrathecal chemotherapy all show significant potential to improve patient survival. Recent epigenetic and transcriptional studies highlight three subgroups of ATRT, each with distinct clinical and molecular characteristics with corresponding therapeutic sensitivities, including epigenetic targeting, and inhibition of tyrosine kinases or growth/lineage specific pathways.

키워드

참고문헌

  1. Arcaro A, Doepfner KT, Boller D, Guerreiro AS, Shalaby T, Jackson SP, et al. : Novel role for insulin as an autocrine growth factor for malignant brain tumour cells. Biochem J 406 : 57-66, 2007 https://doi.org/10.1042/BJ20070309
  2. Athale UH, Duckworth J, Odame I, Barr R : Childhood atypical teratoid rhabdoid tumor of the central nervous system: a meta-analysis of observational studies. J Pediatr Hematol Oncol 31 : 651-663, 2009 https://doi.org/10.1097/MPH.0b013e3181b258a9
  3. Bartelheim K, Nemes K, Seeringer A, Kerl K, Buechner J, Boos J, et al. : Improved 6-year overall survival in AT/RT-results of the registry study rhabdoid 2007. Cancer Med 5 : 1765-1775, 2016 https://doi.org/10.1002/cam4.741
  4. Biegel JA : Molecular genetics of atypical teratoid/rhabdoid tumors. Neurosurg Focus 20 : 1-7, 2006
  5. Biegel JA, Zhou JY, Rorke LB, Stenstrom C, Wainwright LM, Fogelgren B : Germ-line and acquired mutations of INI1 in atypical teratoid and rhabdoid tumors. Cancer Res 59 : 74-79, 1999
  6. Bikowska B, Grajkowska W, Joz'wiak J : Atypical teratoid/rhabdoid tumor: short clinical description and insight into possible mechanism of the disease. Eur J Neurol 18 : 813-818, 2011 https://doi.org/10.1111/j.1468-1331.2010.03277.x
  7. Birks DK, Donson AM, Patel PR, Dunham C, Muscat A, Algar EM, et al. : High expression of BMP pathway genes distinguishes a subset of atypical teratoid/rhabdoid tumors associated with shorter survival. Neuro Oncol 13 : 1296-1307, 2011 https://doi.org/10.1093/neuonc/nor140
  8. Bourdeaut F, Lequin D, Brugieres L, Reynaud S, Dufour C, Doz F, et al. : Frequent hSNF5/INI1 germline mutations in patients with rhabdoid tumor. Clin Cancer Res 17 : 31-38, 2011 https://doi.org/10.1158/1078-0432.CCR-10-1795
  9. Buscariollo DL, Park HS, Roberts KB, Yu JB : Survival outcomes in atypical teratoid rhabdoid tumor for patients undergoing radiotherapy in a surveillance, epidemiology, and end results analysis. Cancer 118 : 4212-4219, 2012 https://doi.org/10.1002/cncr.27373
  10. Chi SN, Zimmerman MA, Yao X, Cohen KJ, Burger P, Biegel JA, et al. : Intensive multimodality treatment for children with newly diagnosed CNS atypical teratoid rhabdoid tumor. J Clin Oncol 27 : 385-389, 2009 https://doi.org/10.1200/JCO.2008.18.7724
  11. Cohen BH, Geyer JR, Miller DC, Curran JG, Zhou T, Holmes E, et al. : Pilot study of intensive chemotherapy with peripheral hematopoietic cell support for children less than 3 years of age with malignant brain tumors, the CCG-99703 phase I/II study. a report from the Children's Oncology Group. Pediatr Neurol 53 : 31-46, 2015 https://doi.org/10.1016/j.pediatrneurol.2015.03.019
  12. D'cunja J, Shalaby T, Rivera P, von Buren A, Patti R, Heppner FL, et al. : Antisense treatment of IGF-IR induces apoptosis and enhances chemosensitivity in central nervous system atypical teratoid/rhabdoid tumours cells. Eur J Cancer 43 : 1581-1589, 2007 https://doi.org/10.1016/j.ejca.2007.03.003
  13. Dufour C, Beaugrand A, Le Deley MC, Bourdeaut F, Andre N, Leblond P, et al. : Clinicopathologic prognostic factors in childhood atypical teratoid and rhabdoid tumor of the central nervous system: a multicenter study. Cancer 118 : 3812-3821, 2012 https://doi.org/10.1002/cncr.26684
  14. Eaton KW, Tooke LS, Wainwright LM, Judkins AR, Biegel JA : Spectrum of SMARCB1/INI1 mutations in familial and sporadic rhabdoid tumors. Pediatr Blood Cancer 56 : 7-15, 2011 https://doi.org/10.1002/pbc.22831
  15. Fangusaro J, Finlay J, Sposto R, Ji L, Saly M, Zacharoulis S, et al. : Intensive chemotherapy followed by consolidative myeloablative chemotherapy with autologous hematopoietic cell rescue (AuHCR) in young children with newly diagnosed supratentorial primitive neuroectodermal tumors (sPNETs): report of the head start I and I. Pediatr Blood Cancer 50 : 312-318, 2008 https://doi.org/10.1002/pbc.21307
  16. Finkelstein-Shechter T, Gassas A, Mabbott D, Huang A, Bartels U, Tabori U, et al. : Atypical teratoid or rhabdoid tumors: improved outcome with high-dose chemotherapy. J Pediatr Hematol Oncol 32 : e182-e186, 2010 https://doi.org/10.1097/MPH.0b013e3181dce1a2
  17. Fruhwald MC, Biegel JA, Bourdeaut F, Roberts CW, Chi SN : Atypical teratoid/rhabdoid tumors-current concepts, advances in biology, and potential future therapies. Neuro Oncol 18 : 764-778, 2016 https://doi.org/10.1093/neuonc/nov264
  18. Fujisawa H, Misaki K, Takabatake Y, Hasegawa M, Yamashita J : Cyclin D1 is overexpressed in atypical teratoid/rhabdoid tumor with hSNF5/INI1 gene inactivation. J Neurooncol 73 : 117-124, 2005 https://doi.org/10.1007/s11060-004-4276-4
  19. Gardner SL, Asgharzadeh S, Green A, Horn B, McCowage G, Finlay J : Intensive induction chemotherapy followed by high dose chemotherapy with autologous hematopoietic progenitor cell rescue in young children newly diagnosed with central nervous system atypical teratoid rhabdoid tumors. Pediatr Blood Cancer 51 : 235-240, 2008 https://doi.org/10.1002/pbc.21578
  20. Geoerger B, Bourdeaut F, DuBois SG, Fischer M, Geller JI, Gottardo NG, et al. : A phase I study of the CDK4/6 inhibitor ribociclib (LEE011) in pediatric patients with malignant rhabdoid tumors, neuroblastoma, and other solid tumors. Clin Cancer Res 23 : 2433-2441, 2017 https://doi.org/10.1158/1078-0432.CCR-16-2898
  21. Geyer JR, Sposto R, Jennings M, Boyett JM, Axtell RA, Breiger D, et al. : Multiagent chemotherapy and deferred radiotherapy in infants with malignant brain tumors: a report from the Children's Cancer Group. J Clin Oncol 23 : 7621-7631, 2005 https://doi.org/10.1200/JCO.2005.09.095
  22. Ginn KF, Gajjar A : Atypical teratoid rhabdoid tumor: current therapy and future directions. Front Oncol 2 : 114, 2012
  23. Gonzales M : The 2000 World Health Organization classification of tumours of the nervous system. J Clin Neurosci 8 : 1-3, 2001
  24. Haberler C, Laggner U, Slavc I, Czech T, Ambros IM, Ambros PF, et al. : Immunohistochemical analysis of INI1 protein in malignant pediatric CNS tumors: lack of INI1 in atypical teratoid/rhabdoid tumors and in a fraction of primitive neuroectodermal tumors without rhabdoid phenotype. Am J Surg Pathol 30 : 1462-1468, 2006 https://doi.org/10.1097/01.pas.0000213329.71745.ef
  25. Han ZY, Richer W, Freneaux P, Chauvin C, Lucchesi C, Guillemot D, et al. : The occurrence of intracranial rhabdoid tumours in mice depends on temporal control of Smarcb1 inactivation. Nat Commun 7 : 10421, 2016 https://doi.org/10.1038/ncomms10421
  26. Hashizume R, Gupta N, Berger MS, Banerjee A, Prados MD, Ayers-Ringler J, et al. : Morphologic and molecular characterization of ATRT xenografts adapted for orthotopic therapeutic testing. Neuro Oncol 12 : 366-376, 2010 https://doi.org/10.1093/neuonc/nop033
  27. Hasselblatt M, Gesk S, Oyen F, Rossi S, Viscardi E, Giangaspero F, et al. : Nonsense mutation and inactivation of SMARCA4 (BRG1) in an atypical teratoid/rhabdoid tumor showing retained SMARCB1 (INI1) expression. Am J Surg Pathol 35 : 933-935, 2011 https://doi.org/10.1097/PAS.0b013e3182196a39
  28. Hilden JM, Meerbaum S, Burger P, Finlay J, Janss A, Scheithauer BW, et al. : Central nervous system atypical teratoid/rhabdoid tumor: results of therapy in children enrolled in a registry. J Clin Oncol 22 : 2877-2884, 2004 https://doi.org/10.1200/JCO.2004.07.073
  29. Ho DMT, Hsu CY, Wong TT, Ting LT, Chiang H : Atypical teratoid/rhabdoid tumor of the central nervous system: a comparative study with primitive neuroectodermal tumor/medulloblastoma. Acta Neuropathol 99 : 482-488, 2000 https://doi.org/10.1007/s004010051149
  30. Jayanthan A, Bernoux D, Bose P, Riabowol K, Narendran A : Multi-tyrosine kinase inhibitors in preclinical studies for pediatric CNS AT/RT: evidence for synergy with topoisomerase-I inhibition. Cancer Cell Int 11 : 44, 2011 https://doi.org/10.1186/1475-2867-11-44
  31. Jeibmann A, Eikmeier K, Linge A, Kool M, Koos B, Schulz J, et al. : Identification of genes involved in the biology of atypical teratoid/rhabdoid tumours using drosophila melanogaster. Nat Commun 5 : 4005, 2014 https://doi.org/10.1038/ncomms5005
  32. Johann PD, Erkek S, Zapatka M, Kerl K, Buchhalter I, Hovestadt V, et al. : Atypical teratoid/rhabdoid tumors are comprised of three epigenetic subgroups with distinct enhancer landscapes. Cancer Cell 29 : 379-393, 2016 https://doi.org/10.1016/j.ccell.2016.02.001
  33. Kerl K, Holsten T, Fruhwald MC : Rhabdoid tumors: clinical approaches and molecular targets for innovative therapy. Pediatr Hematol Oncol 30 : 587-604, 2013 https://doi.org/10.3109/08880018.2013.791737
  34. Knipstein JA, Birks DK, Donson AM, Alimova I, Foreman NK, Vibhakar R : Histone deacetylase inhibition decreases proliferation and potentiates the effect of ionizing radiation in atypical teratoid/rhabdoid tumor cells. Neuro Oncol 14 : 175-183, 2012 https://doi.org/10.1093/neuonc/nor208
  35. Knutson SK, Warholic NM, Wigle TJ, Klaus CR, Allain CJ, Raimondi A, et al. : Durable tumor regression in genetically altered malignant rhabdoid tumors by inhibition of methyltransferase EZH2. Proc Natl Acad Sci U S A 110 : 7922-7927, 2013 https://doi.org/10.1073/pnas.1303800110
  36. Koos B, Jeibmann A, Lunenburger H, Mertsch S, Nupponen NN, Roselli A, et al. : The tyrosine kinase c-Abl promotes proliferation and is expressed in atypical teratoid and malignant rhabdoid tumors. Cancer 116 : 5075- 5081, 2010 https://doi.org/10.1002/cncr.25420
  37. Kordes U, Gesk S, Fruhwald MC, Graf N, Leuschner I, Hasselblatt M, et al. : Clinical and molecular features in patients with atypical teratoid rhabdoid tumor or malignant rhabdoid tumor. Genes Chromosom Cancer 49 : 176-181, 2010 https://doi.org/10.1002/gcc.20729
  38. Lafay-Cousin L, Hawkins C, Carret AS, Johnston D, Zelcer S, Wilson B, et al. : Central nervous system atypical teratoid rhabdoid tumours: the Canadian Paediatric Brain Tumour Consortium experience. Eur J Cancer 48 : 353-359, 2012 https://doi.org/10.1016/j.ejca.2011.09.005
  39. Lafay-Cousin L, Strother D : Current treatment approaches for infants with malignant central nervous system tumors. Oncologist 14 : 433-444, 2009 https://doi.org/10.1634/theoncologist.2008-0193
  40. Lee J, Kim DS, Han JW, Suh CO : Atypical teratoid/rhabdoid tumors in children treated with multimodal therapies: the necessity of upfront radiotherapy after surgery. Pediatr Blood Cancer 64 : e26663, 2017 https://doi.org/10.1002/pbc.26663
  41. Lee S, Cimica V, Ramachandra N, Zagzag D, Kalpana GV : Aurora A is a repressed effector target of the chromatin remodeling protein INI1/hSNF5 required for rhabdoid tumor cell survival. Cancer Res 71 : 3225-3235, 2011 https://doi.org/10.1158/0008-5472.CAN-10-2167
  42. Louis DN, Perry A, Reifenberger G, von Deimling A, Figarella-Branger D, Cavenee WK, et al. : The 2016 World Health Organization Classification of Tumors of the Central Nervous System: a summary. Acta Neuropathol 131 : 803-820, 2016 https://doi.org/10.1007/s00401-016-1545-1
  43. McKenna ES, Sansam CG, Cho YJ, Greulich H, Evans JA, Thom CS, et al. : Loss of the epigenetic tumor suppressor SNF5 leads to cancer without genomic instability. Mol Cell Biol 28 : 6223-6233, 2008 https://doi.org/10.1128/MCB.00658-08
  44. Nicolaides T, Tihan T, Horn B, Biegel J, Prados M, Banerjee A : High-dose chemotherapy and autologous stem cell rescue for atypical teratoid/rhabdoid tumor of the central nervous system. J Neurooncol 98 : 117-123, 2010 https://doi.org/10.1007/s11060-009-0071-6
  45. Ogino S, Kubo S, Abdul-Karim FW, Cohen ML : Comparative immunohistochemical study of insulin-like growth factor II and insulin-like growth factor receptor type 1 in pediatric brain tumors. Pediatr Dev Pathol 4 : 23-31, 2001 https://doi.org/10.1007/s100240010112
  46. Pai Panandiker AS, Merchant TE, Beltran C, Wu S, Sharma S, Boop FA, et al. : Sequencing of local therapy affects the pattern of treatment failure and survival in children with atypical teratoid rhabdoid tumors of the central nervous system. Int J Radiat Oncol 82 : 1756-1763, 2012 https://doi.org/10.1016/j.ijrobp.2011.02.059
  47. Park ES, Sung KW, Baek HJ, Park KD, Park HJ, Won SC, et al. : Tandem high-dose chemotherapy and autologous stem cell transplantation in young children with atypical teratoid/rhabdoid tumor of the central nervous system. J Korean Med Sci 27 : 135-140, 2012 https://doi.org/10.3346/jkms.2012.27.2.135
  48. Picard D, Miller S, Hawkins CE, Bouffet E, Rogers HA, Chan TS, et al. : Markers of survival and metastatic potential in childhood CNS primitive neuro-ectodermal brain tumours: an integrative genomic analysis. Lancet Oncol 13 : 838-848, 2012 https://doi.org/10.1016/S1470-2045(12)70257-7
  49. Rorke LB, Packer RJ, Biegel JA : Central nervous system atypical teratoid/rhabdoid tumors of infancy and childhood: definition of an entity. J Neurosurg 85 : 56-65, 1996 https://doi.org/10.3171/jns.1996.85.1.0056
  50. Schrey D, Carceller Lechon F, Malietzis G, Moreno L, Dufour C, Chi S, et al. : Multimodal therapy in children and adolescents with newly diagnosed atypical teratoid rhabdoid tumor: individual pooled data analysis and review of the literature. J Neurooncol 126 : 81-90, 2016 https://doi.org/10.1007/s11060-015-1904-0
  51. Sevenet N, Sheridan E, Amram D, Schneider P, Handgretinger R, Delattre O : Constitutional mutations of the hSNF5/INI1 gene predispose to a variety of cancers. Am J Hum Genet 65 : 1342-1348, 1999 https://doi.org/10.1086/302639
  52. Shih CS, Hale GA, Gronewold L, Tong X, Laningham FH, Gilger EA, et al. : High-dose chemotherapy with autologous stem cell rescue for children with recurrent malignant brain tumors. Cancer 112 : 1345-1353, 2008 https://doi.org/10.1002/cncr.23305
  53. Smith ME, Cimica V, Chinni S, Challagulla K, Mani S, Kalpana GV : Rhabdoid tumor growth is inhibited by flavopiridol. Clin Cancer Res 14 : 523-532, 2008 https://doi.org/10.1158/1078-0432.CCR-07-1347
  54. Smith ME, Cimica V, Chinni S, Jana S, Koba W, Yang Z, et al. : Therapeutically targeting cyclin D1 in primary tumors arising from loss of Ini1. Proc Natl Acad Sci U S A 108 : 319-324, 2011 https://doi.org/10.1073/pnas.0913297108
  55. Sung KW, Lim DH, Yi ES, Choi YB, Lee JW, Yoo KH, et al. : Tandem highdose chemotherapy and autologous stem cell transplantation for atypical teratoid/rhabdoid tumor. Cancer Res Treat 48 : 1408-1419, 2016 https://doi.org/10.4143/crt.2015.347
  56. Tang Y, Gholamin S, Schubert S, Willardson MI, Lee A, Bandopadhayay P, et al. : Epigenetic targeting of hedgehog pathway transcriptional output through BET bromodomain inhibition. Nat Med 20 : 732-740, 2014 https://doi.org/10.1038/nm.3613
  57. Tekautz TM, Fuller CE, Blaney S, Fouladi M, Broniscer A, Merchant TE, et al. : Atypical teratoid/rhabdoid tumors (ATRT): improved survival in children 3 years of age and older with radiation therapy and high-dose alkylator-based chemotherapy. J Clin Oncol 23 : 1491-1499, 2005 https://doi.org/10.1200/JCO.2005.05.187
  58. Torchia J, Golbourn B, Feng S, Ho KC, Sin-Chan P, Vasiljevic A, et al. : Integrated (epi)-genomic analyses identify subgroup-specific therapeutic targets in CNS rhabdoid tumors. Cancer Cell 30 : 891-908, 2016 https://doi.org/10.1016/j.ccell.2016.11.003
  59. Torchia J, Picard D, Lafay-Cousin L, Hawkins CE, Kim SK, Letourneau L, et al. : Molecular subgroups of atypical teratoid rhabdoid tumours in children: an integrated genomic and clinicopathological analysis. Lancet Oncol 16 : 569-582, 2015 https://doi.org/10.1016/S1470-2045(15)70114-2
  60. Tsikitis M, Zhang Z, Edelman W, Zagzag D, Kalpana GV : Genetic ablation of cyclin D1 abrogates genesis of rhabdoid tumors resulting from Ini1 loss. Proc Natl Acad Sci U S A 102 : 12129-12134, 2005 https://doi.org/10.1073/pnas.0505300102
  61. Unland R, Borchardt C, Clemens D, Kool M, Dirksen U, Fruhwald MC : Analysis of the antiproliferative effects of 3-deazaneoplanocin A in combination with standard anticancer agents in rhabdoid tumor cell lines. Anticancer Drugs 26 : 301-311, 2015 https://doi.org/10.1097/CAD.0000000000000181
  62. Venkataraman S, Alimova I, Tello T, Harris PS, Knipstein JA, Donson AM, et al. : Targeting aurora kinase A enhances radiation sensitivity of atypical teratoid rhabdoid tumor cells. J Neurooncol 107 : 517-526, 2012 https://doi.org/10.1007/s11060-011-0795-y
  63. Versteege I, Sevenet N, Lange J, Rousseau-Merck MF, Ambros P, Handgretinger R, et al. : Truncating mutations of hSNF5/INI1 in aggressive paediatric cancer. Nature 394 : 203-206, 1998 https://doi.org/10.1038/28212
  64. von Hoff K, Hinkes B, Dannenmann-Stern E, von Bueren AO, Warmuth-Metz M, Soerensen N, et al. : Frequency, risk-factors and survival of children with atypical teratoid rhabdoid tumors (AT/RT) of the CNS diagnosed between 1988 and 2004, and registered to the German HIT database. Pediatr Blood Cancer 57 : 978-985, 2011 https://doi.org/10.1002/pbc.23236
  65. Weinblatt M, Kochen J : Rhabdoid tumor of the central. Med Pediatr Oncol 20 : 258, 1992 https://doi.org/10.1002/mpo.2950200317
  66. Wetmore C, Boyett J, Li S, Lin T, Bendel A, Gajjar A, et al. : Alisertib is active as single agent in recurrent atypical teratoid rhabdoid tumors in 4 children. Neuro Oncol 17 : 882-888, 2015 https://doi.org/10.1093/neuonc/nov017
  67. Wilson BG, Wang X, Shen X, McKenna ES, Lemieux ME, Cho Y, et al. : Epigenetic antagonism between polycomb and SWI/SNF complexes during oncogenic transformation. Cancer Cell 18 : 316-328, 2010 https://doi.org/10.1016/j.ccr.2010.09.006
  68. Woehrer A, Slavc I, Waldhoer T, Heinzl H, Zielonke N, Czech T, et al. : Incidence of atypical teratoid/rhabdoid tumors in children: a populationbased study by the Austrian Brain Tumor Registry, 1996-2006. Cancer 116 : 5725-5732, 2010 https://doi.org/10.1002/cncr.25540
  69. Zimmerman MA, Goumnerova LC, Proctor M, Scott RM, Marcus K, Pomeroy SL, et al. : Continuous remission of newly diagnosed and relapsed central nervous system atypical teratoid/rhabdoid tumor. J Neurooncol 72 : 77-84, 2005 https://doi.org/10.1007/s11060-004-3115-y

피인용 문헌

  1. Imaging features of spinal atypical teratoid rhabdoid tumors in children vol.97, pp.52, 2018, https://doi.org/10.1097/md.0000000000013808
  2. Pediatric Atypical Teratoid/Rhabdoid Tumors of the Brain: Identification of Metabolic Subgroups Using In Vivo 1H-MR Spectroscopy vol.40, pp.5, 2019, https://doi.org/10.3174/ajnr.a6024
  3. Upregulation of Protein Synthesis and Proteasome Degradation Confers Sensitivity to Proteasome Inhibitor Bortezomib in Myc-Atypical Teratoid/Rhabdoid Tumors vol.12, pp.3, 2018, https://doi.org/10.3390/cancers12030752
  4. Outcomes with respect to extent of surgical resection for pediatric atypical teratoid rhabdoid tumors vol.36, pp.4, 2020, https://doi.org/10.1007/s00381-019-04478-5
  5. Drug screening with a novel tumor-derived cell line identified alternative therapeutic options for patients with atypical teratoid/rhabdoid tumor vol.34, pp.1, 2021, https://doi.org/10.1007/s13577-020-00438-3
  6. Atypical Teratoid/Rhabdoid Tumor of the Central Nervous System in Children under the Age of 3 Years vol.53, pp.2, 2018, https://doi.org/10.4143/crt.2020.756
  7. Human SNF5 arming of double-deleted vaccinia virus shows oncolytic and cytostatic activity against central nervous system atypical teratoid/rhabdoid tumor cells vol.28, pp.7, 2018, https://doi.org/10.1038/s41417-020-0199-2
  8. Maternal embryonal leucine zipper kinase immunoreactivity in atypical teratoid/rhabdoid tumors: a study of 50 cases vol.37, pp.12, 2018, https://doi.org/10.1007/s00381-021-05335-0