Home LiteratureArticle Details
PMID: 18724359 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Identification of ALK as a major familial neuroblastoma predisposition gene.

Nature ·Vol. 455 ·No. 7215 ·2008-10-16 ·Pages 930-5

Mossé YP, Laudenslager M, Longo L, Cole KA, Wood A, Attiyeh EF, Laquaglia MJ, Sennett R, Lynch JE, Perri P, Laureys G, Speleman F, Kim C, Hou C, Hakonarson H, Torkamani A, Schork NJ, Brodeur GM, Tonini GP, Rappaport E, Devoto M, Maris JM

Abstract

Neuroblastoma is a childhood cancer that can be inherited, but the genetic aetiology is largely unknown. Here we show that germline mutations in the anaplastic lymphoma kinase (ALK) gene explain most hereditary neuroblastomas, and that activating mutations can also be somatically acquired. We first identified a significant linkage signal at chromosome bands 2p23-24 using a whole-genome scan in neuroblastoma pedigrees. Resequencing of regional candidate genes identified three separate germline missense mutations in the tyrosine kinase domain of ALK that segregated with the disease in eight separate families. Resequencing in 194 high-risk neuroblastoma samples showed somatically acquired mutations in the tyrosine kinase domain in 12.4% of samples. Nine of the ten mutations map to critical regions of the kinase domain and were predicted, with high probability, to be oncogenic drivers. Mutations resulted in constitutive phosphorylation, and targeted knockdown of ALK messenger RNA resulted in profound inhibition of growth in all cell lines harbouring mutant or amplified ALK, as well as in two out of six wild-type cell lines for ALK. Our results demonstrate that heritable mutations of ALK are the main cause of familial neuroblastoma, and that germline or acquired activation of this cell-surface kinase is a tractable therapeutic target for this lethal paediatric malignancy.

MeSH Terms
Anaplastic Lymphoma Kinase Base Sequence Cell Line, Tumor Child Chromosomes, Human, Pair 2/genetics Female Gene Dosage Gene Expression Regulation, Neoplastic Genetic Predisposition to Disease/genetics Germ-Line Mutation/genetics Humans Male Models, Molecular Molecular Sequence Data Mutation/genetics Neuroblastoma/enzymology,genetics Pedigree Phosphorylation Protein Structure, Tertiary Protein-Tyrosine Kinases/chemistry,deficiency,genetics Receptor Protein-Tyrosine Kinases
Chemicals
ALK protein, human Anaplastic Lymphoma Kinase Protein-Tyrosine Kinases Receptor Protein-Tyrosine Kinases
Authors & Affiliations
22 authors, click to expand affiliations / ORCID
Mossé Yaël P
Division of Oncology and Center for Childhood Cancer Research, Children's Hospital of Philadelphia, Department of Pediatrics, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania 19104, USA.
Laudenslager Marci
Longo Luca
Cole Kristina A
Wood Andrew
Attiyeh Edward F
Laquaglia Michael J
Sennett Rachel
Lynch Jill E
Perri Patrizia
Laureys Geneviève
Speleman Frank
Kim Cecilia
Hou Cuiping
Hakonarson Hakon
Torkamani Ali
Schork Nicholas J
Brodeur Garrett M
Tonini Gian P
Rappaport Eric
Devoto Marcella
Maris John M
References (48)
48 references, click to expand
  1. Recurrent involvement of 2p23 in inflammatory myofibroblastic tumors.
    Cancer Res. 1999 Jun 15;59(12):2776-80 PMID: 10383129
  2. ALK receptor tyrosine kinase promotes cell growth and neurite outgrowth.
    J Cell Sci. 2004 Jul 1;117(Pt 15):3319-29 PMID: 15226403
  3. Genetic predisposition to familial neuroblastoma: identification of two novel genomic regions at 2p and 12p.
    Hum Hered. 2007;63(3-4):205-11 PMID: 17317969
  4. Familial neuroblastoma. Case reports, literature review, and etiologic considerations.
    Cancer. 1986 May 1;57(9):1887-93 PMID: 3955526
  5. Chromosome 6p22 locus associated with clinically aggressive neuroblastoma.
    N Engl J Med. 2008 Jun 12;358(24):2585-93 PMID: 18463370
  6. Molecular characterization of ALK, a receptor tyrosine kinase expressed specifically in the nervous system.
    Oncogene. 1997 Jan 30;14(4):439-49 PMID: 9053841
  7. Expression of the ALK tyrosine kinase gene in neuroblastoma.
    Am J Pathol. 2000 May;156(5):1711-21 PMID: 10793082
  8. The anaplastic lymphoma kinase in the pathogenesis of cancer.
    Nat Rev Cancer. 2008 Jan;8(1):11-23 PMID: 18097461
  9. Joint modeling of linkage and association: identifying SNPs responsible for a linkage signal.
    Am J Hum Genet. 2005 Jun;76(6):934-49 PMID: 15877278
  10. Treatment of high-risk neuroblastoma with intensive chemotherapy, radiotherapy, autologous bone marrow transplantation, and 13-cis-retinoic acid. Children's Cancer Group.
    N Engl J Med. 1999 Oct 14;341(16):1165-73 PMID: 10519894
  11. Genomic alterations of anaplastic lymphoma kinase may sensitize tumors to anaplastic lymphoma kinase inhibitors.
    Cancer Res. 2008 May 1;68(9):3389-95 PMID: 18451166
  12. Polyalanine expansion and frameshift mutations of the paired-like homeobox gene PHOX2B in congenital central hypoventilation syndrome.
    Nat Genet. 2003 Apr;33(4):459-61 PMID: 12640453
  13. Prediction of cancer driver mutations in protein kinases.
    Cancer Res. 2008 Mar 15;68(6):1675-82 PMID: 18339846
  14. Molecular genetic analysis of familial neuroblastoma.
    Eur J Cancer. 1997 Oct;33(12):1923-8 PMID: 9516825
  15. Global survey of phosphotyrosine signaling identifies oncogenic kinases in lung cancer.
    Cell. 2007 Dec 14;131(6):1190-203 PMID: 18083107
  16. Weak linkage at 4p16 to predisposition for human neuroblastoma.
    Oncogene. 2002 Nov 28;21(54):8356-60 PMID: 12447700
  17. ERBB2 kinase domain mutation in the lung squamous cell carcinoma.
    Cancer Lett. 2006 Jun 8;237(1):89-94 PMID: 16029927
  18. Identification of squamous cell carcinoma associated proteins by proteomics and loss of beta tropomyosin expression in esophageal cancer.
    World J Gastroenterol. 2006 Nov 28;12(44):7104-12 PMID: 17131471
  19. Chromosome localization in normal human cells and neuroblastomas of a gene related to c-myc.
    Nature. 1984 Mar 15-21;308(5956):288-91 PMID: 6700732
  20. Mutation and cancer: neuroblastoma and pheochromocytoma.
    Am J Hum Genet. 1972 Sep;24(5):514-32 PMID: 4340974
  21. Evidence for a hereditary neuroblastoma predisposition locus at chromosome 16p12-13.
    Cancer Res. 2002 Nov 15;62(22):6651-8 PMID: 12438263
  22. Expression and functional analysis of the anaplastic lymphoma kinase (ALK) gene in tumor cell lines.
    Int J Cancer. 2002 Jul 1;100(1):49-56 PMID: 12115586
  23. Biological role of anaplastic lymphoma kinase in neuroblastoma.
    Am J Pathol. 2005 Jul;167(1):213-22 PMID: 15972965
  24. Cancer genes and the pathways they control.
    Nat Med. 2004 Aug;10(8):789-99 PMID: 15286780
  25. Did protein kinase regulatory mechanisms evolve through elaboration of a simple structural component?
    J Mol Biol. 2005 Sep 2;351(5):956-72 PMID: 16051269
  26. Activation of anaplastic lymphoma kinase is responsible for hyperphosphorylation of ShcC in neuroblastoma cell lines.
    Oncogene. 2002 Aug 29;21(38):5823-34 PMID: 12185581
  27. PEDSTATS: descriptive statistics, graphics and quality assessment for gene mapping data.
    Bioinformatics. 2005 Aug 15;21(16):3445-7 PMID: 15947021
  28. Merlin--rapid analysis of dense genetic maps using sparse gene flow trees.
    Nat Genet. 2002 Jan;30(1):97-101 PMID: 11731797
  29. Accurate prediction of deleterious protein kinase polymorphisms.
    Bioinformatics. 2007 Nov 1;23(21):2918-25 PMID: 17855419
  30. Novel D761Y and common secondary T790M mutations in epidermal growth factor receptor-mutant lung adenocarcinomas with acquired resistance to kinase inhibitors.
    Clin Cancer Res. 2006 Nov 1;12(21):6494-501 PMID: 17085664
  31. Activating mutations for the met tyrosine kinase receptor in human cancer.
    Proc Natl Acad Sci U S A. 1997 Oct 14;94(21):11445-50 PMID: 9326629
  32. Targeted expression of MYCN causes neuroblastoma in transgenic mice.
    EMBO J. 1997 Jun 2;16(11):2985-95 PMID: 9214616
  33. Chromosome 1p and 11q deletions and outcome in neuroblastoma.
    N Engl J Med. 2005 Nov 24;353(21):2243-53 PMID: 16306521
  34. Identification of the transforming EML4-ALK fusion gene in non-small-cell lung cancer.
    Nature. 2007 Aug 2;448(7153):561-6 PMID: 17625570
  35. Neuroblastoma.
    Lancet. 2007 Jun 23;369(9579):2106-20 PMID: 17586306
  36. Germline PHOX2B mutation in hereditary neuroblastoma.
    Am J Hum Genet. 2004 Oct;75(4):727-30 PMID: 15338462
  37. The Phox2B homeobox gene is mutated in sporadic neuroblastomas.
    Oncogene. 2004 Dec 9;23(57):9280-8 PMID: 15516980
  38. Increased risk of cancer among siblings of long-term childhood cancer survivors: a report from the childhood cancer survivor study.
    Cancer Epidemiol Biomarkers Prev. 2005 Aug;14(8):1922-7 PMID: 16103438
  39. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method.
    Methods. 2001 Dec;25(4):402-8 PMID: 11846609
  40. Fusion of a kinase gene, ALK, to a nucleolar protein gene, NPM, in non-Hodgkin's lymphoma.
    Science. 1994 Mar 4;263(5151):1281-4 PMID: 8122112
  41. Integrative genomics identifies distinct molecular classes of neuroblastoma and shows that multiple genes are targeted by regional alterations in DNA copy number.
    Cancer Res. 2006 Jun 15;66(12):6050-62 PMID: 16778177
  42. Prevalence and functional consequence of PHOX2B mutations in neuroblastoma.
    Oncogene. 2008 Jan 17;27(4):469-76 PMID: 17637745
  43. Different effects of point mutations within the B-Raf glycine-rich loop in colorectal tumors on mitogen-activated protein/extracellular signal-regulated kinase kinase/extracellular signal-regulated kinase and nuclear factor kappaB pathway and cellular transformation.
    Cancer Res. 2004 May 15;64(10):3428-35 PMID: 15150094
  44. Somatic mutations of ERBB2 kinase domain in gastric, colorectal, and breast carcinomas.
    Clin Cancer Res. 2006 Jan 1;12(1):57-61 PMID: 16397024
  45. Real-time monitoring of morphological changes in living cells by electronic cell sensor arrays: an approach to study G protein-coupled receptors.
    Anal Chem. 2006 Jan 1;78(1):35-43 PMID: 16383308
  46. Genome-wide analysis of neuroblastomas using high-density single nucleotide polymorphism arrays.
    PLoS One. 2007 Feb 28;2(2):e255 PMID: 17327916
  47. Functional analysis of mutations within the kinase activation segment of B-Raf in human colorectal tumors.
    Cancer Res. 2003 Dec 1;63(23):8132-7 PMID: 14678966
  48. Germline mutations of the paired-like homeobox 2B (PHOX2B) gene in neuroblastoma.
    Am J Hum Genet. 2004 Apr;74(4):761-4 PMID: 15024693
Article Info
Journal
Nature
Abbr.
Nature
ISSN
1476-4687
Published
2008-10-16
Epub
2008-00-24
Pages
930-5
Language
English
Region
England
NLM ID
0410462
PMCID
PMC2672043
Subset
IM
Grants
NCI NIH HHS · K08 CA111733 · United States
NCI NIH HHS · R01-CA78454 · United States
NCI NIH HHS · R01 CA078545 · United States
NCRR NIH HHS · UL1 RR025774 · United States
PHS HHS · K08-111733 · United States
NCI NIH HHS · K08 CA111733-04 · United States
NCI NIH HHS · R01-CA87847 · United States
NCI NIH HHS · U10 CA098543 · United States
NCI NIH HHS · R01 CA078545-09 · United States
NCI NIH HHS · R01 CA087847 · United States
NCI NIH HHS · R01 CA124709 · United States
NCI NIH HHS · U10 CA098543-06 · United States
Databases
GENBANK
EU660517, EU660518, EU660519, EU660520, EU660521, EU660522, EU660523, EU660524, EU660525, EU660526, EU660527
Corrections
CommentIn
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