Molecular evolution of a neurofibroma to malignant peripheral nerve sheath tumor (MPNST) in an NF1 patient: Correlation between histopathological, clinical and molecular findings

Journal of Cancer Research and Clinical Oncology

Volumn 136, Issue 12, 2010, Pages 1869-1880

  Spurlock, Gill ^a   Knight, Samantha J L ^b   Thomas, Nick ^a   Kiehl, Tim Rasmus ^c   Guha, Abhijit ^d   Upadhyaya, Meena ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY HEALTH NETWORK   (Canada)

^d TORONTO WESTERN HOSPITAL   (Canada)

Author keywords

Atypical neurofibroma; Germline mutation; Loss of heterozygosity; Malignant peripheral nervous system tumor (MPNST); Neurofibromatosis type 1 (NF1); Plexiform neurofibroma (PNF); Tumor suppressor gene (TSG)

Indexed keywords

CELL CYCLE PROTEIN; CYCLIN DEPENDENT KINASE INHIBITOR 2A; DNA; NEUROFIBROMIN; PROTEIN P53; PROTEIN RB1; TUMOR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CLINICAL ASSESSMENT; COMPARATIVE GENOMIC HYBRIDIZATION; CONTROLLED STUDY; DIAGNOSTIC VALUE; DNA DETERMINATION; GENE LOCATION; GENE LOSS; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC GAIN; HETEROZYGOSITY LOSS; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; MICROARRAY ANALYSIS; MOLECULAR EVOLUTION; MUTATIONAL ANALYSIS; NEUROFIBROMA; NEUROFIBROMATOSIS; NUCLEOTIDE SEQUENCE; PERIPHERAL NERVE TUMOR; PRIORITY JOURNAL; SOMATIC MUTATION;

ADULT; BASE SEQUENCE; COMPARATIVE GENOMIC HYBRIDIZATION; DISEASE PROGRESSION; DNA MUTATIONAL ANALYSIS; GERM-LINE MUTATION; HUMANS; LOSS OF HETEROZYGOSITY; MALE; MOLECULAR SEQUENCE DATA; NERVE SHEATH NEOPLASMS; NEUROFIBROMA; NEUROFIBROMATOSIS 1; NEUROFIBROMIN 1;

EID: 78649329027     PISSN: 01715216     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00432-010-0846-3     Document Type: Article

References (50)

1. M Altmannsberger K Weber R Droste M Osborn 1985 Desmin is a specific marker for rhabdomyosarcomas of human and rat origin Am J Pathol 118 85 95 1:STN:280:DyaL2M%2FpsVGjtQ%3D%3D 3881039
2. L Angelov A Davis B O'Sullivan R Bell A Guha 1998 Management of neurogenic sarcomas: a University of Toronto experience Neurosurgery 43 56 65 1:STN:280:DyaK1czhvFaksw%3D%3D 10.1097/00006123-199807000-00035 9657189 (Pubitemid 28287782)
3. B Bausch W Borozdin VF Mautner MM Hoffmann D Boehm M Robledo A Cascon T Harenberg F Schiavi C Pawlu M Peczkowska C Letizia S Calvieri G Arnaldi RD Klingenberg-Noftz N Reisch A Fassina L Brunaud MA Walter M Mannelli G MacGregor FF Palazzo M Barontini MK Walz B Kremens G Brabant R Pfäffle AC Koschker F Lohoefner M Mohaupt O Gimm B Jarzab SR McWhinney G Opocher A Januszewicz J Kohlhase C Eng HP Neumann European-American Phaeochromocytoma Registry Study Group 2007 Germline NF1 mutational spectra and loss-of-heterozygosity analyses in patients with pheochromocytoma and neurofibromatosis type 1 J Clin Endocrinol Metab 92 2784 2792 1:CAS:528:DC%2BD2sXotVylt7w%3D 10.1210/jc.2006-2833 17426081 (Pubitemid 47037390)
4. DA Belchis CA Meece FA Benko PK Rogan RA Williams CD Gocke 1996 Loss of heterozygosity and microsatellite instability at the retinoblastoma locus in osteosarcomas Diagn Mol Pathol 5 214 219 1:STN:280:DyaK2s%2FhvFOlsA%3D%3D 10.1097/00019606-199609000-00011 8866236 (Pubitemid 26323983)
5. E Bennett NS Thomas M Upadhyaya 2009 Neurofibromatosis type 1: its association with the Ras/MAPK pathway syndromes J Paeditr Neurol 7 1 5
6. H Brems E Beert T de Ravel E Legius 2009 Mechanisms in the pathogenesis of malignant tumors in neurofibromatosis type 1 Lancet Oncol 10 508 515 1:CAS:528:DC%2BD1MXlsVKhs7w%3D 10.1016/S1470-2045(09)70033-6 19410195
7. H Brems C Park O Maertens A Pemov L Messiaen M Upadhyaya K Claes E Beert K Peeters V Mautner J Sloan L Yao R Lee R Sciot L De Smet E Legius D Stewart 2009 Molecular pathogenesis of NF1 related glomus tumors Can Res 69 7393 7401 1:CAS:528:DC%2BD1MXhtFaku7vO 10.1158/0008-5472.CAN-09-1752
8. RS Bridge Jr JA Bridge JR Neff S Naumann P Althof LA Bruch 2004 Recurrent chromosomal imbalances and structurally abnormal breakpoints within complex karyotypes of malignant peripheral nerve sheath tumor and malignant triton tumor: a cytogenetic and molecular cytogenetic study J Clin Pathol 57 1172 1178 1:CAS:528:DC%2BD2cXhtVKisb3E 10.1136/jcp.2004.019026 15509679 (Pubitemid 39486524)
9. P Cairns TJ Polascik Y Eby K Tokino J Califano A Merlo L Mao J Herath R Jenkins W Westra 1995 Frequency of homozygous deletion at p16/CDKN2 in primary human tumors Nat Genet 11 210 212 1:CAS:528:DyaK2MXosF2rt70%3D 10.1038/ng1095-210 7550353
10. SL Carroll N Ratner 2008 How does the Schwann cell lineage form tumors in NF1? Glia 56 1590 1605 10.1002/glia.20776 18803326
11. GT Chang M Jhamai WM van Weerden G Jenster AO Brinkmann 2004 The TRPS1 transcription factor: androgenic regulation in prostate cancer and high expression in breast cancer Endocr Relat Cancer 11 815 822 1:CAS:528: DC%2BD2MXhtVartrk%3D 10.1677/erc.1.00853 15613454 (Pubitemid 40065553)
12. K Cichowski T Jacks 2001 NF1 tumor suppressor gene function: narrowing the GAP Cell 104 593 604 1:CAS:528:DC%2BD3MXis1Kks7g%3D 10.1016/S0092-8674(01) 00245-8 11239415 (Pubitemid 32201953)
13. PG Coulie V Brichard A Van Pel T Wölfel J Schneider C Traversari S Mattei E De Plaen C Lurquin JP Szikora JC Renauld T Boon 1994 A new gene coding for a differentiation antigen recognized by autologous cytolytic T lymphocytes on HLA-A2 melanomas J Exp Med 180 35 42 1:CAS:528:DyaK2cXlt1Kmtrs%3D 10.1084/jem.180.1.35 8006593 (Pubitemid 24181053)
14. P Dalerba RW Cho MF Clarke 2007 Cancer stem cells: models and concepts Ann Rev Med 58 267 284 1:CAS:528:DC%2BD2sXisV2jtr8%3D 10.1146/annurev.med.58. 062105.204854 17002552 (Pubitemid 46706514)
15. T De Raedt O Maertens M Chmara H Brems I Heyns R Sciot E Majounie M Upadhyaya S De Schepper F Speleman L Messiaen JR Vermeesch E Legius 2006 Somatic loss of wild type NF1 allele in neurofibromas: comparison of NF1 microdeletion and non-microdeletion patients Genes Chromosomes Cancer 45 893 904 10.1002/gcc.20353 16830335 (Pubitemid 44360177)
16. DG Evans ME Baser J McGaughran S Sharif E Howard A Moran 2002 Malignant peripheral nerve sheath tumors in neurofibromatosis 1 J Med Genet 39 311 314 1:STN:280:DC%2BD383nt1Wquw%3D%3D 10.1136/jmg.39.5.311 12011145
17. Y Fang A Elahi RC Denley PH Rao MF Brennan SC Jhanwar 2009 Molecular characterization of permanent cell lines from primary, metastatic and recurrent malignant peripheral nerve sheath tumors (MPNST) with underlying neurofibromatosis-1 Anticancer Res; 29 1255 1262 1:CAS:528:DC%2BD1MXltFCgsrk%3D 19414372
18. PA Futreal JC Barrett RW Wiseman 1991 An Alu polymorphism intragenic to the TP53 gene Nucleic Acids Res 19 6977 1:CAS:528:DyaK38Xlt1Oltg%3D%3D 10.1093/nar/19.24.6977 1762941
19. AM Gowan AM Vogel D Hoak F Gough MA McNutt 1986 Monoclonal antibodies specific for melanocytic tumors distinguish subpopulations of melanocytes Am J Pathol 123 195 203
20. A Guha N Lau I Huvar D Gutmann J Provias T Pawson G Boss 1996 Ras-GTP levels are elevated in human NF1 peripheral nerve tumors Oncogene 12 507 513 1:CAS:528:DyaK28XhtFCms7o%3D 8637706
21. A Hartmann U Rösner G Schlake W Dietmaier D Zaak F Hofstaedter R Knuechel 2000 Clonality and genetic divergence in multifocal low-grade superficial urothelial carcinoma as determined by chromosome 9 and p53 deletion analysis Lab Invest 80 709 718 1:CAS:528:DC%2BD3cXktFGjtb8%3D 10830781
22. Y Kawakami S Eliyahu CH Delgado PF Robbins L Rivoltini SL Topalian T Miki SA Rosenberg 1994 Cloning of the gene coding for a shared human melanoma antigen recognized by autologous T cells infiltrating into tumor Proc Natl Acad Sci USA 91 3515 3519 1:CAS:528:DyaK2cXksFCrtbk%3D 10.1073/pnas.91.9.3515 8170938
23. SH Kresse M Skårn HO Ohnstad HM Namløs B Bjerkehagen O Myklebost LA Meza-Zepeda 2008 DNA copy number changes in high-grade malignant peripheral nerve sheath tumors by array CGH Mol Cancer 7 48 10.1186/1476-4598-7- 48 18522746 (Pubitemid 351998267)
24. S Kumar E Perlman CA Harris M Raffeld M Tsokos 2000 Myogenin is a specific marker for rhabdomyosarcoma: an immunohistochemical study in paraffin-embedded tissues Mod Pathol 13 988 993 1:STN:280:DC%2BD3cvltFemsw%3D%3D 10.1038/modpathol.3880179 11007039
25. S Le Jan N Le Meur A Cazes J Philippe M Le Cunff J Léger P Corvol S Germain 2006 Characterization of the expression of the hypoxia-induced genes Neuritin, TXNIP and IGFBP3 in cancer FEBS Lett 580 3395 3400 1:CAS:528:DC%2BD28XltlensL0%3D 10.1016/j.febslet.2006.05.011 16723126 (Pubitemid 43795919)
26. P Lévy D Vidaud K Leroy I Laurendeau J Wechsler G Bolasco B Parfait P Wolkenstein M Vidaud I Bièche 2004 Molecular profiling of malignant peripheral nerve sheath tumors associated with neurofibromatosis type 1, based on large-scale real-time RT-PCR Mol Cancer 3 20 10.1186/1476-4598-3-20 15255999 (Pubitemid 40230552)
27. P Lévy H Ripoche I Laurendeau V Lazar N Ortonne B Parfait K Leroy J Wechsler I Salmon P Wolkenstein P Dessen M Vidaud D Vidaud I Bièche 2007 Microarray-based identification of tenascin C and tenascin XB, genes possibly involved in tumorigenesis associated with neurofibromatosis type 1 Clin Cancer Res 13 398 407 10.1158/1078-0432.CCR-06-0182 17202312 (Pubitemid 46225342)
28. AS Llaguno J Chen CH Kwon EL Jackson Y Li DK Burns A Alvarez-Buylla LF Parada 2009 Malignant astrocytomas originate from neural stem/progenitor cells in a somatic tumor suppressor mouse model Cancer Cell 15 45 56 1:CAS:528:DC%2BD1MXptVGquw%3D%3D 10.1016/j.ccr.2009.02.008 (Erratum: Cancer Cell 15:240)
29. RA Lothe A Slettan G Saeter A Brøgger AL Børresen JM Nesland 1995 Alterations at chromosome 17 loci in peripheral nerve sheath tumors J Neuropathol Exp Neurol 54 65 73 1:STN:280:DyaK2M7hsVKitg%3D%3D 10.1097/00005072-199501000-00008 7815081
30. RA Lothe R Karhu N Mandahl F Mertens G Saeter S Heim AL Borresen-Dale OP Kallioniemi 1996 Gain of 17q24-qter detected by comparative genomic hybridization in malignant tumors from patients with von Recklinghausen's neurofibromatosis Cancer Res 56 4778 4781 1:CAS:528:DyaK28XmsV2itL4%3D 8840998
31. RA Lothe B Smith-Sørensen M Hektoen AE Stenwig N Mandahl G Saeter F Mertens 2001 Biallelic inactivation of TP53 rarely contributes to the development of malignant peripheral nerve sheath tumors Genes Chromosomes Cancer 30 202 206 1:CAS:528:DC%2BD3MXnsFyhuw%3D%3D 10.1002/1098-2264(2000)9999: 9999<::AID-GCC1079>3.0.CO;2-5 11135438
32. O Maertens H Prenen M Debiec-Rychter A Wozniak R Sciot P Pauwels I De Wever JR Vermeesch T de Raedt A De Paepe F Speleman A van Oosterom L Messiaen E Legius 2006 Molecular pathogenesis of multiple gastrointestinal stromal tumors in NF1 patients Hum Mol Genet 15 1015 1023 1:CAS:528:DC%2BD28XitVGmtrk%3D 10.1093/hmg/ddl016 16461335 (Pubitemid 43338241)
33. KK Mantripragada G Spurlock L Kluwe N Chuzhanova RE Ferner IM Frayling JP Dumanski A Guha V Mautner M Upadhyaya 2008 High-resolution DNA copy number profiling of malignant peripheral nerve sheath tumors using targeted microarray-based comparative genomic hybridization Clin Cancer Res 14 1015 1024 1:CAS:528:DC%2BD1cXhvF2gtbc%3D 10.1158/1078-0432.CCR-07-1305 18281533 (Pubitemid 351302546)
34. KK Mantripragada TD de Ståhl C Patridge U Menzel R Andersson N Chuzhanova L Kluwe A Guha V Mautner JP Dumanski M Upadhyaya 2009 Genome-wide high-resolution analysis of DNA copy number alterations in NF1-associated malignant peripheral nerve sheath tumors using 32 K BAC array Genes Chromosomes Cancer 48 897 907 1:CAS:528:DC%2BD1MXhtValsb%2FF 10.1002/gcc.20695 19603524
35. S Miller JJ Walter T Mehta A Hardiman E Sites S Kaiser A Jegga H Li M Upadhyaya M Giovannini D Muir M Wallace E Lopez E Serra C Lazaro PageG Stemmer-Rachamimov BJ Aronow N Ratner 2009 Integrative genomic analyses show altered Schwann cell development in neurofibromatosis tumors and implicate SOX9 as an addicting oncogene EMBO Mol Med 1 236 248 1:CAS:528:DC%2BD1MXht1CjurrI 10.1002/emmm.200900027 20049725
36. PM Pollock MS Stark JM Palmer MK Walters JF Aitken NG Martin NK Hayward 2001 Mutation analysis of the CDKN2A promoter in Australian melanoma families Genes Chromosomes Cancer 32 89 94 1:CAS:528:DC%2BD3MXmsVOnsr8%3D 10.1002/gcc.1170 11477665 (Pubitemid 32737788)
37. KJ Savinainen MJ Linja OR Saramäki TL Tammela GT Chang AO Brinkmann T Visakorpi 2004 Expression and copy number analysis of TRPS1, EIF3S3 and MYC genes in breast and prostate cancer Br J Cancer 90 1041 1046 1:CAS:528:DC%2BD2cXhslWrsbg%3D 10.1038/sj.bjc.6601648 14997205 (Pubitemid 38495826)
38. S Schubbert K Shannon G Bollag 2007 Hyperactive Ras in developmental disorders and cancer Nat Rev Cancer 7 295 308 1:CAS:528:DC%2BD2sXjtlyhtLs%3D 10.1038/nrc2109 17384584 (Pubitemid 46480970)
39. E Serra T Rosenbaum U Winner R Aledo E Ars X Estivill HG Lenard C Lázaro 2000 Schwann cells harbor the somatic NF1 mutation in neurofibromas: evidence of two different Schwann cell subpopulations Hum Mol Genet 9 3055 3064 1:CAS:528:DC%2BD3MXjt1ai 10.1093/hmg/9.20.3055 11115850
40. L Side B Taylor M Cayouette E Conner P Thompson M Luce K Shannon 1997 Homozygous inactivation of the NF1 gene in bone marrow cells from children with neurofibromatosis type 1 and malignant myeloid disorders N Engl J Med 336 1713 1720 1:STN:280:DyaK2szgs1answ%3D%3D 10.1056/NEJM199706123362404 9180088 (Pubitemid 27251785)
41. CJ Stasik O Tawfik 2006 Malignant peripheral nerve sheath tumor with rhabdomyosarcomatous differentiation (malignant triton tumor) Arch Pathol Lab Med 130 1878 1881 17149968
42. DA Stevenson H Zhou S Ashrafi LM Messiaen JC Carey JL D'Astous SD Santora DH Viskochil 2006 Double inactivation of NF1 in tibial pseudarthrosis Am J Hum Genet 79 143 148 1:CAS:528:DC%2BD28Xmt1ent7c%3D 10.1086/504441 16773574 (Pubitemid 43927385)
43. W Stewart JP Traynor A Cooke S Griffiths NF Onen M Balsitis AA Shah M Upadhyaya ES Tobias 2007 Gastric carcinoid: germline and somatic mutation of the neurofibromatosis type 1 gene Fam Cancer 6 147 152 1:CAS:528: DC%2BD2sXhslWjsbw%3D 10.1007/s10689-006-9002-2 16944271 (Pubitemid 46295294)
44. H Stewart C Bowker S Edees S Smalley M Crocker D Mechan N Forrester G Spurlock M Upadhyaya 2008 Congenital disseminated neurofibromatosis type 1: a clinical and molecular case report Am J Med Genet 146A 1444 1452 1:CAS:528:DC%2BD1cXnvFelt70%3D 10.1002/ajmg.a.32305 18438896 (Pubitemid 351770209)
45. CT Storlazzi HR Brekke N Mandahl O Brosjö S Smeland RA Lothe F Mertens 2006 Identification of a novel amplicon at distal 17q containing the BIRC5/SURVIVIN gene in malignant peripheral nerve sheath tumors J Pathol 209 492 500 1:CAS:528:DC%2BD28XpsVartLc%3D 10.1002/path.1998 16721726 (Pubitemid 44194564)
46. T Tucker P Wolkenstein J Revuz J Zeller JM Friedman 2005 Association between benign and malignant peripheral nerve sheath tumors in NF1 Neurology 65 205 211 1:STN:280:DC%2BD2MzosFylug%3D%3D 10.1212/01.wnl.0000168830.79997.13 16043787 (Pubitemid 41022362)
47. Upadhyaya M and Cooper DN. 1998. NeurofibromatosisType 1: From Genotype to Phenotype Upadhyaya M, Cooper DN (Eds). Oxford: BIOS Scientific Publishers
48. M Upadhyaya S Han C Consoli E Majounie M Horan NS Thomas C Potts S Griffiths M Ruggieri A von Deimling DN Cooper 2004 Characterization of the somatic mutational spectrum of the neurofibromatosis type 1 (NF1) gene in neurofibromatosis patients with benign and malignant tumors Hum Mutat 23 134 146 1:CAS:528:DC%2BD2cXhs1Gqs70%3D 10.1002/humu.10305 14722917 (Pubitemid 38200604)
49. M Upadhyaya L Kluwe G Spurlock B Monem E Majounie K Mantripragada M Ruggieri N Chuzhanova DG Evans R Ferner N Thomas A Guha V Mautner 2008 Germline and somatic NF1 gene mutation spectrum in NF1-associated malignant peripheral nerve sheath tumors (MPNSTs) Hum Mutat 29 74 82 1:CAS:528:DC%2BD1cXhslOltL4%3D 10.1002/humu.20601 17960768
50. M Upadhyaya G Spurlock B Monem N Thomas RE Friedrich L Kluwe V Mautner 2008 Germline and somatic NF1 gene mutations in plexiform neurofibromas Hum Mutat 29 E103 E111 10.1002/humu.20793 18484666