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PMID: 19048115 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Neurofibromin 1 (NF1) defects are common in human ovarian serous carcinomas and co-occur with TP53 mutations.

Neoplasia (New York, N.Y.) ·Vol. 10 ·No. 12 ·2008-12-00 ·Pages 1362-72, following 1372

Sangha N, Wu R, Kuick R, Powers S, Mu D, Fiander D, Yuen K, Katabuchi H, Tashiro H, Fearon ER, Cho KR

Abstract

Ovarian serous carcinoma (OSC) is the most common and lethal histologic type of ovarian epithelial malignancy. Mutations of TP53 and dysfunction of the Brca1 and/or Brca2 tumor-suppressor proteins have been implicated in the molecular pathogenesis of a large fraction of OSCs, but frequent somatic mutations in other well-established tumor-suppressor genes have not been identified. Using a genome-wide screen of DNA copy number alterations in 36 primary OSCs, we identified two tumors with apparent homozygous deletions of the NF1 gene. Subsequently, 18 ovarian carcinoma-derived cell lines and 41 primary OSCs were evaluated for NF1 alterations. Markedly reduced or absent expression of Nf1 protein was observed in 6 of the 18 cell lines, and using the protein truncation test and sequencing of cDNA and genomic DNA, NF1 mutations resulting in deletion of exons and/or aberrant splicing of NF1 transcripts were detected in 5 of the 6 cell lines with loss of NF1 expression. Similarly, NF1 alterations including homozygous deletions and splicing mutations were identified in 9 (22%) of 41 primary OSCs. As expected, tumors and cell lines with NF1 defects lacked mutations in KRAS or BRAF but showed Ras pathway activation based on immunohistochemical detection of phosphorylated MAPK (primary tumors) or increased levels of GTP-bound Ras (cell lines). The TP53 tumor-suppressor gene was mutated in all OSCs with documented NF1 mutation, suggesting that the pathways regulated by these two tumor-suppressor proteins often cooperate in the development of ovarian carcinomas with serous differentiation.

MeSH Terms
Alternative Splicing Cell Line, Tumor DNA, Complementary/metabolism Enzyme Activation Exons Female Gene Deletion Gene Expression Regulation, Neoplastic Genes, p53 Homozygote Humans Mutation Neurofibromin 1/genetics,physiology Ovarian Neoplasms/genetics,metabolism Phosphorylation
Chemicals
DNA, Complementary Neurofibromin 1
Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Sangha Navneet
Department of Pathology, The University of Michigan Medical School, Ann Arbor, MI 48109-2200, USA.
Wu Rong
Kuick Rork
Powers Scott
Mu David
Fiander Diane
Yuen Kit
Katabuchi Hidetaka
Tashiro Hironori
Fearon Eric R
Cho Kathleen R
References (59)
59 references, click to expand
  1. Ovarian tumorigenesis: a proposed model based on morphological and molecular genetic analysis.
    Am J Pathol. 2004 May;164(5):1511-8 PMID: 15111296
  2. Inactivation of the NF1 gene in human melanoma and neuroblastoma cell lines without impaired regulation of GTP.Ras.
    Proc Natl Acad Sci U S A. 1993 Jun 15;90(12):5539-43 PMID: 8516298
  3. Identification and characterization of the neurofibromatosis type 1 protein product.
    Proc Natl Acad Sci U S A. 1991 Nov 15;88(22):9914-8 PMID: 1946460
  4. RAS signaling in colorectal carcinomas through alteration of RAS, RAF, NF1, and/or RASSF1A.
    Neoplasia. 2008 Jul;10(7):680-6, 2 p following 686 PMID: 18592002
  5. Oncogenic cooperation and coamplification of developmental transcription factor genes in lung cancer.
    Proc Natl Acad Sci U S A. 2007 Oct 16;104(42):16663-8 PMID: 17925434
  6. Alternate molecular genetic pathways in ovarian carcinomas of common histological types.
    Hum Pathol. 2007 Apr;38(4):607-13 PMID: 17258789
  7. Mutational analysis of K-ras segregates ovarian serous carcinomas into two types: invasive MPSC (low-grade tumor) and conventional serous carcinoma (high-grade tumor).
    Int J Gynecol Pathol. 2003 Jan;22(1):37-41 PMID: 12496696
  8. BRCA1 and BRCA2 mutations account for a large proportion of ovarian carcinoma cases.
    Cancer. 2005 Dec 15;104(12):2807-16 PMID: 16284991
  9. Patterns of somatic mutation in human cancer genomes.
    Nature. 2007 Mar 8;446(7132):153-8 PMID: 17344846
  10. Patterns of p53 mutations separate ovarian serous borderline tumors and low- and high-grade carcinomas and provide support for a new model of ovarian carcinogenesis: a mutational analysis with immunohistochemical correlation.
    Am J Surg Pathol. 2005 Feb;29(2):218-24 PMID: 15644779
  11. Extensive in silico analysis of NF1 splicing defects uncovers determinants for splicing outcome upon 5' splice-site disruption.
    Hum Mutat. 2007 Jun;28(6):599-612 PMID: 17311297
  12. Assessment of TP53 mutation using purified tissue samples of ovarian serous carcinomas reveals a higher mutation rate than previously reported and does not correlate with drug resistance.
    Int J Gynecol Cancer. 2008 May-Jun;18(3):487-91 PMID: 17692090
  13. Inactivation of BRCA1 and BRCA2 in ovarian cancer.
    J Natl Cancer Inst. 2002 Sep 18;94(18):1396-406 PMID: 12237285
  14. Loss of heterozygosity of chromosome 17 in human borderline and invasive epithelial ovarian tumors.
    Oncogene. 1996 May 16;12(10):2147-53 PMID: 8668340
  15. Aberrant regulation of ras proteins in malignant tumour cells from type 1 neurofibromatosis patients.
    Nature. 1992 Apr 23;356(6371):713-5 PMID: 1570015
  16. Aberrant splicing in several human tumors in the tumor suppressor genes neurofibromatosis type 1, neurofibromatosis type 2, and tuberous sclerosis 2.
    Cancer Res. 2002 Mar 1;62(5):1503-9 PMID: 11888927
  17. Integrating signals from RTKs to ERK/MAPK.
    Oncogene. 2007 May 14;26(22):3113-21 PMID: 17496910
  18. Genomic organization of the neurofibromatosis 1 gene (NF1).
    Genomics. 1995 Jan 1;25(1):9-18 PMID: 7774960
  19. NF1 mutations in neurofibromatosis 1 patients with plexiform neurofibromas.
    Hum Mutat. 2002 Mar;19(3):309 PMID: 11857752
  20. TP53 and ovarian cancer.
    Hum Mutat. 2003 Mar;21(3):285-91 PMID: 12619114
  21. Neurofibromatosis 1 and neurofibromatosis 2: a twenty first century perspective.
    Lancet Neurol. 2007 Apr;6(4):340-51 PMID: 17362838
  22. Representational oligonucleotide microarray analysis: a high-resolution method to detect genome copy number variation.
    Genome Res. 2003 Oct;13(10):2291-305 PMID: 12975311
  23. [Ovarian cancer in a female patient with von Recklinghausen's disease].
    Med Clin (Barc). 1991 Feb 2;96(4):138-40 PMID: 1902542
  24. Malignant behavior and resistance to cisplatin of human ovarian carcinoma xenografts established from the same patient at different stages of the disease.
    Cancer Res. 1991 Dec 1;51(23 Pt 1):6358-62 PMID: 1933898
  25. MMP-13 and p53 in the progression of malignant peripheral nerve sheath tumors.
    Neoplasia. 2007 Aug;9(8):671-7 PMID: 17786186
  26. Amplification and overexpression of the L-MYC proto-oncogene in ovarian carcinomas.
    Am J Pathol. 2003 May;162(5):1603-10 PMID: 12707044
  27. Ras/Raf/ERK signalling and NF1.
    Cell Cycle. 2004 Oct;3(10):1255-8 PMID: 15467460
  28. Neurofibromatosis type 1 gene as a mutational target in a mismatch repair-deficient cell type.
    Hum Genet. 2003 Feb;112(2):117-23 PMID: 12522551
  29. Expression of BRCA1 protein in benign, borderline, and malignant epithelial ovarian neoplasms and its relationship to methylation and allelic loss of the BRCA1 gene.
    J Pathol. 2004 Feb;202(2):215-23 PMID: 14743504
  30. Urinary bladder transitional cell carcinogenesis is associated with down-regulation of NF1 tumor suppressor gene in vivo and in vitro.
    Am J Pathol. 1999 Mar;154(3):755-65 PMID: 10079253
  31. Recurrent mutations in the NF1 gene are common among neurofibromatosis type 1 patients.
    J Med Genet. 2003 Jun;40(6):e82 PMID: 12807981
  32. The histologic type and stage distribution of ovarian carcinomas of surface epithelial origin.
    Int J Gynecol Pathol. 2004 Jan;23(1):41-4 PMID: 14668549
  33. Diverse tumorigenic pathways in ovarian serous carcinoma.
    Am J Pathol. 2002 Apr;160(4):1223-8 PMID: 11943707
  34. Nonsense codons in human beta-globin mRNA result in the production of mRNA degradation products.
    Mol Cell Biol. 1992 Mar;12(3):1149-61 PMID: 1545796
  35. Evaluation of the protein truncation test and mutation detection in the NF1 gene: mutational analysis of 15 known and 40 unknown mutations.
    Hum Genet. 1999 Oct;105(4):327-32 PMID: 10543400
  36. Characterization of active mitogen-activated protein kinase in ovarian serous carcinomas.
    Clin Cancer Res. 2004 Oct 1;10(19):6432-6 PMID: 15475429
  37. NF1 gene loss of heterozygosity and expression analysis in sporadic colon cancer.
    Gut. 2005 Aug;54(8):1129-35 PMID: 15840687
  38. Ras regulation. NF is enough of GAP.
    Nature. 1992 Apr 23;356(6371):663-4 PMID: 1570011
  39. Osteopontin as a potential diagnostic biomarker for ovarian cancer.
    JAMA. 2002 Apr 3;287(13):1671-9 PMID: 11926891
  40. Mutations in BRAF and KRAS characterize the development of low-grade ovarian serous carcinoma.
    J Natl Cancer Inst. 2003 Mar 19;95(6):484-6 PMID: 12644542
  41. Characterization and properties of nine human ovarian adenocarcinoma cell lines.
    Cancer Res. 1988 Nov 1;48(21):6166-72 PMID: 3167863
  42. Combinatorial sequencing-by-hybridization: analysis of the NF1 gene.
    Genet Test. 2006 Spring;10(1):8-17 PMID: 16544997
  43. Mutations affecting mRNA splicing are the most common molecular defects in patients with neurofibromatosis type 1.
    Hum Mol Genet. 2000 Jan 22;9(2):237-47 PMID: 10607834
  44. p53 gene mutations and protein accumulation in human ovarian cancer.
    Proc Natl Acad Sci U S A. 1993 Jun 1;90(11):4961-5 PMID: 8506342
  45. Comparative properties of five human ovarian adenocarcinoma cell lines.
    Cancer Res. 1985 Aug;45(8):3668-76 PMID: 4016745
  46. Hyperactivation of p21(ras) and the hematopoietic-specific Rho GTPase, Rac2, cooperate to alter the proliferation of neurofibromin-deficient mast cells in vivo and in vitro.
    J Exp Med. 2001 Jul 2;194(1):57-69 PMID: 11435472
  47. Germline and somatic NF1 gene mutation spectrum in NF1-associated malignant peripheral nerve sheath tumors (MPNSTs).
    Hum Mutat. 2008 Jan;29(1):74-82 PMID: 17960768
  48. Heterozygosity for the neurofibromatosis 1 (NF1) tumor suppressor results in abnormalities in cell attachment, spreading and motility in astrocytes.
    Hum Mol Genet. 2001 Dec 15;10(26):3009-16 PMID: 11751683
  49. Novel mutations of neurofibromatosis type 1 gene in small cell lung cancers.
    Surg Today. 2003;33(5):323-7 PMID: 12734724
  50. NF1 gene and neurofibromatosis 1.
    Am J Epidemiol. 2000 Jan 1;151(1):33-40 PMID: 10625171
  51. Blocking oncogenic Ras signaling for cancer therapy.
    J Natl Cancer Inst. 2001 Jul 18;93(14):1062-74 PMID: 11459867
  52. Distribution of 13 truncating mutations in the neurofibromatosis 1 gene.
    Hum Mol Genet. 1995 Jun;4(6):975-81 PMID: 7655472
  53. A transforming mutation in the pleckstrin homology domain of AKT1 in cancer.
    Nature. 2007 Jul 26;448(7152):439-44 PMID: 17611497
  54. Loss of heterozygosity on chromosome 17q11-21 in cancers of women who have both breast and ovarian cancer.
    Am J Obstet Gynecol. 1995 Mar;172(3):908-13 PMID: 7892884
  55. Exhaustive mutation analysis of the NF1 gene allows identification of 95% of mutations and reveals a high frequency of unusual splicing defects.
    Hum Mutat. 2000;15(6):541-55 PMID: 10862084
  56. Loss of NF1 results in activation of the Ras signaling pathway and leads to aberrant growth in haematopoietic cells.
    Nat Genet. 1996 Feb;12(2):144-8 PMID: 8563751
  57. Disruption of exonic splicing enhancer elements is the principal cause of exon skipping associated with seven nonsense or missense alleles of NF1.
    Hum Mutat. 2004 Dec;24(6):491-501 PMID: 15523642
  58. Evaluation of denaturing high performance liquid chromatography (DHPLC) for the mutational analysis of the neurofibromatosis type 1 ( NF1) gene.
    Hum Genet. 2001 Nov;109(5):487-97 PMID: 11735023
  59. Quantification of NF1 transcripts reveals novel highly expressed splice variants.
    FEBS Lett. 2002 Jul 3;522(1-3):71-6 PMID: 12095621
Article Info
Journal
Neoplasia (New York, N.Y.)
Abbr.
Neoplasia
ISSN
1476-5586
Published
2008-12-00
Pages
1362-72, following 1372
Language
English
Region
United States
NLM ID
100886622
PMCID
PMC2586687
Subset
IM
Grants
NCI NIH HHS · P30 CA046592 · United States
NCI NIH HHS · 2P30 CA046592 · United States
NCI NIH HHS · R01 CA094172 · United States
NCI NIH HHS · 2R01 CA94172 · United States
NCI NIH HHS · R01 CA127547 · United States
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