Home LiteratureArticle Details
PMID: 21097718 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Genetic and structural variation in the gastric cancer kinome revealed through targeted deep sequencing.

Cancer research ·Vol. 71 ·No. 1 ·2011-01-01 ·Pages 29-39

Zang ZJ, Ong CK, Cutcutache I, Yu W, Zhang SL, Huang D, Ler LD, Dykema K, Gan A, Tao J, Lim S, Liu Y, Futreal PA, Grabsch H, Furge KA, Goh LK, Rozen S, Teh BT, Tan P

Abstract

Genetic alterations in kinases have been linked to multiple human pathologies. To explore the landscape of kinase genetic variation in gastric cancer (GC), we used targeted, paired-end deep sequencing to analyze 532 protein and phosphoinositide kinases in 14 GC cell lines. We identified 10,604 single-nucleotide variants (SNV) in kinase exons including greater than 300 novel nonsynonymous SNVs. Family-wise analysis of the nonsynonymous SNVs revealed a significant enrichment in mitogen-activated protein kinase (MAPK)-related genes (P < 0.01), suggesting a preferential involvement of this kinase family in GC. A potential antioncogenic role for MAP2K4, a gene exhibiting recurrent alterations in 2 lines, was functionally supported by siRNA knockdown and overexpression studies in wild-type and MAP2K4 variant lines. The deep sequencing data also revealed novel, large-scale structural rearrangement events involving kinases including gene fusions involving CDK12 and the ERBB2 receptor tyrosine kinase in MKN7 cells. Integrating SNVs and copy number alterations, we identified Hs746T as a cell line exhibiting both splice-site mutations and genomic amplification of MET, resulting in MET protein overexpression. When applied to primary GCs, we identified somatic mutations in 8 kinases, 4 of which were recurrently altered in both primary tumors and cell lines (MAP3K6, STK31, FER, and CDKL5). These results demonstrate that how targeted deep sequencing approaches can deliver unprecedented multilevel characterization of a medically and pharmacologically relevant gene family. The catalog of kinome genetic variants assembled here may broaden our knowledge on kinases and provide useful information on genetic alterations in GC.

MeSH Terms
Amino Acid Sequence Cell Line, Tumor Gene Dosage Genetic Variation Humans MAP Kinase Signaling System/genetics Molecular Sequence Data Protein Kinases/chemistry,metabolism Sequence Homology, Amino Acid Signal Transduction Stomach Neoplasms/enzymology,genetics,pathology
Chemicals
Protein Kinases
Authors & Affiliations
19 authors, click to expand affiliations / ORCID
Zang Zhi Jiang
Cellular and Molecular Research, National Cancer Centre, Singapore.
Ong Choon Kiat
Cutcutache Ioana
Yu Willie
Zhang Shen Li
Huang Dachuan
Ler Lian Dee
Dykema Karl
Gan Anna
Tao Jiong
Lim Siyu
Liu Yujing
Futreal P Andrew
Grabsch Heike
Furge Kyle A
Goh Liang Kee
Rozen Steve
Teh Bin Tean
Tan Patrick
References (50)
50 references, click to expand
  1. COSMIC (the Catalogue of Somatic Mutations in Cancer): a resource to investigate acquired mutations in human cancer.
    Nucleic Acids Res. 2010 Jan;38(Database issue):D652-7 PMID: 19906727
  2. Alteration of the ATM gene occurs in gastric cancer cell lines and primary tumors associated with cellular response to DNA damage.
    Mutat Res. 2004 Jan 10;557(1):41-51 PMID: 14706517
  3. Amplification of c-erbB-2 oncogene in human adenocarcinomas in vivo.
    Lancet. 1986 Apr 5;1(8484):765-7 PMID: 2870269
  4. A novel STK11 germline mutation in two siblings with Peutz-Jeghers syndrome complicated by primary gastric cancer.
    Clin Genet. 2005 Jan;67(1):81-6 PMID: 15617552
  5. Activation of MET by gene amplification or by splice mutations deleting the juxtamembrane domain in primary resected lung cancers.
    J Thorac Oncol. 2009 Jan;4(1):5-11 PMID: 19096300
  6. Patterns of somatic mutation in human cancer genomes.
    Nature. 2007 Mar 8;446(7132):153-8 PMID: 17344846
  7. The protein kinase complement of the human genome.
    Science. 2002 Dec 6;298(5600):1912-34 PMID: 12471243
  8. Multiplex amplification of large sets of human exons.
    Nat Methods. 2007 Nov;4(11):931-6 PMID: 17934468
  9. Guanylyl cyclases and signaling by cyclic GMP.
    Pharmacol Rev. 2000 Sep;52(3):375-414 PMID: 10977868
  10. Genome-wide in situ exon capture for selective resequencing.
    Nat Genet. 2007 Dec;39(12):1522-7 PMID: 17982454
  11. Direct selection of human genomic loci by microarray hybridization.
    Nat Methods. 2007 Nov;4(11):903-5 PMID: 17934467
  12. Targeted next-generation sequencing appoints c16orf57 as clericuzio-type poikiloderma with neutropenia gene.
    Am J Hum Genet. 2010 Jan;86(1):72-6 PMID: 20004881
  13. Enrichment of sequencing targets from the human genome by solution hybridization.
    Genome Biol. 2009;10(10):R116 PMID: 19835619
  14. Microarray-based genomic selection for high-throughput resequencing.
    Nat Methods. 2007 Nov;4(11):907-9 PMID: 17934469
  15. The UCSC Known Genes.
    Bioinformatics. 2006 May 1;22(9):1036-46 PMID: 16500937
  16. dbSNP: the NCBI database of genetic variation.
    Nucleic Acids Res. 2001 Jan 1;29(1):308-11 PMID: 11125122
  17. Massively parallel sequencing of ataxia genes after array-based enrichment.
    Hum Mutat. 2010 Apr;31(4):494-9 PMID: 20151403
  18. Identification of a second MutL DNA mismatch repair complex (hPMS1 and hMLH1) in human epithelial cells.
    J Biol Chem. 2000 May 26;275(21):15728-32 PMID: 10748105
  19. Similarity of protein encoded by the human c-erb-B-2 gene to epidermal growth factor receptor.
    Nature. 1986 Jan 16-22;319(6050):230-4 PMID: 3003577
  20. Diverse somatic mutation patterns and pathway alterations in human cancers.
    Nature. 2010 Aug 12;466(7308):869-73 PMID: 20668451
  21. Somatic mutations of GUCY2F, EPHA3, and NTRK3 in human cancers.
    Hum Mutat. 2006 Oct;27(10):1060-1 PMID: 16941478
  22. Next-generation DNA sequencing.
    Nat Biotechnol. 2008 Oct;26(10):1135-45 PMID: 18846087
  23. TNK2 preserves epidermal growth factor receptor expression on the cell surface and enhances migration and invasion of human breast cancer cells.
    Breast Cancer Res. 2008;10(2):R36 PMID: 18435854
  24. A thousand and one protein kinases.
    Cell. 1987 Sep 11;50(6):823-9 PMID: 3113737
  25. A comprehensive assay for targeted multiplex amplification of human DNA sequences.
    Proc Natl Acad Sci U S A. 2008 Jul 8;105(27):9296-301 PMID: 18599465
  26. Human diabetes associated with a mutation in the tyrosine kinase domain of the insulin receptor.
    Science. 1989 Jul 7;245(4913):66-8 PMID: 2544998
  27. Mutations of the STK11 gene in sporadic gastric carcinoma.
    Int J Oncol. 1998 Sep;13(3):601-4 PMID: 9683800
  28. Human non-synonymous SNPs: server and survey.
    Nucleic Acids Res. 2002 Sep 1;30(17):3894-900 PMID: 12202775
  29. A serine/threonine kinase gene defective in Peutz-Jeghers syndrome.
    Nature. 1998 Jan 8;391(6663):184-7 PMID: 9428765
  30. MAP kinase signalling pathways in cancer.
    Oncogene. 2007 May 14;26(22):3279-90 PMID: 17496922
  31. Doubling up on microtubule stabilizers: synergistic functions of doublecortin-like kinase and doublecortin in the developing cerebral cortex.
    Neuron. 2006 Jan 5;49(1):3-4 PMID: 16387632
  32. Mutations in STK11 gene in Czech Peutz-Jeghers patients.
    BMC Med Genet. 2009 Jul 19;10:69 PMID: 19615099
  33. Solution hybrid selection with ultra-long oligonucleotides for massively parallel targeted sequencing.
    Nat Biotechnol. 2009 Feb;27(2):182-9 PMID: 19182786
  34. Bioconductor: open software development for computational biology and bioinformatics.
    Genome Biol. 2004;5(10):R80 PMID: 15461798
  35. Targeting cancer with small molecule kinase inhibitors.
    Nat Rev Cancer. 2009 Jan;9(1):28-39 PMID: 19104514
  36. Mutations in the TRKA/NGF receptor gene in patients with congenital insensitivity to pain with anhidrosis.
    Nat Genet. 1996 Aug;13(4):485-8 PMID: 8696348
  37. Visualization of genomic data with the Hilbert curve.
    Bioinformatics. 2009 May 15;25(10):1231-5 PMID: 19297348
  38. BioMart--biological queries made easy.
    BMC Genomics. 2009 Jan 14;10:22 PMID: 19144180
  39. Microsatellite instability is associated with genetic alteration but not with low levels of expression of the human mismatch repair proteins hMSH2 and hMLH1.
    Eur J Cancer. 2000 May;36(7):925-31 PMID: 10785599
  40. Gains, losses, and amplifications of genomic materials in primary gastric cancers analyzed by comparative genomic hybridization.
    Genes Chromosomes Cancer. 1999 Apr;24(4):299-305 PMID: 10092127
  41. The effectiveness of trastuzumab (Herceptin) combined with chemotherapy for gastric carcinoma with overexpression of the c-erbB-2 protein.
    Gastric Cancer. 2005;8(4):249-52 PMID: 16328600
  42. Predicting deleterious amino acid substitutions.
    Genome Res. 2001 May;11(5):863-74 PMID: 11337480
  43. Mapping short DNA sequencing reads and calling variants using mapping quality scores.
    Genome Res. 2008 Nov;18(11):1851-8 PMID: 18714091
  44. Escape from Cbl-mediated downregulation: a recurrent theme for oncogenic deregulation of receptor tyrosine kinases.
    Cancer Cell. 2003 Jun;3(6):519-23 PMID: 12842080
  45. Parkinson's disease-associated mutations in leucine-rich repeat kinase 2 augment kinase activity.
    Proc Natl Acad Sci U S A. 2005 Nov 15;102(46):16842-7 PMID: 16269541
  46. A novel germline mutation of the LKB1 gene in a patient with Peutz-Jeghers syndrome with early-onset gastric cancer.
    J Gastroenterol. 2004 Dec;39(12):1210-4 PMID: 15622488
  47. Human mitogen-activated protein kinase kinase 4 as a candidate tumor suppressor.
    Cancer Res. 1997 Oct 1;57(19):4177-82 PMID: 9331070
  48. Detection of large-scale variation in the human genome.
    Nat Genet. 2004 Sep;36(9):949-51 PMID: 15286789
  49. Oncogene mutations, copy number gains and mutant allele specific imbalance (MASI) frequently occur together in tumor cells.
    PLoS One. 2009 Oct 14;4(10):e7464 PMID: 19826477
  50. Gastric cancer.
    Lancet. 2003 Jul 26;362(9380):305-15 PMID: 12892963
Article Info
Journal
Cancer research
Abbr.
Cancer Res
ISSN
1538-7445
Published
2011-01-01
Epub
2010-00-19
Pages
29-39
Language
English
Region
United States
NLM ID
2984705R
PMCID
PMC3719377
Subset
IM
Grants
Wellcome Trust · 077012 · United Kingdom
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com