WNT/TCF Signaling through LEF1 and HOXB9 Mediates Lung Adenocarcinoma Metastasis

Cell

Volumn 138, Issue 1, 2009, Pages 51-62

  Nguyen, Don X ^a   Chiang, Anne C ^a   Zhang, Xiang H F ^a   Kim, Juliet Y ^a   Kris, Mark G ^a,b   Ladanyi, Marc ^a   Gerald, William L ^a   Massagué, Joan ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

HUMDISEASE; SIGNALING

Indexed keywords

HOX PROTEIN; HOXB9 PROTEIN; LYMPHOID ENHANCER FACTOR 1; T CELL FACTOR PROTEIN; UNCLASSIFIED DRUG; WNT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE METASTASIS; BRAIN METASTASIS; CANCER GROWTH; CANCER INVASION; CANCER RELAPSE; CONTROLLED STUDY; DISEASE FREE SURVIVAL; DISTANT METASTASIS; GENE EXPRESSION PROFILING; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; LUNG ADENOCARCINOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; TUMOR GROWTH;

MUS;

EID: 67649662201     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2009.04.030     Document Type: Article

References (60)

1. Abate-Shen C. Deregulated homeobox gene expression in cancer: cause or consequence?. Nat. Rev. Cancer 2 (2002) 777-785
2. Arce L., Yokoyama N.N., and Waterman M.L. Diversity of LEF/TCF action in development and disease. Oncogene 25 (2006) 7492-7504
3. Bild A.H., Yao G., Chang J.T., Wang Q., Potti A., Chasse D., Joshi M.B., Harpole D., Lancaster J.M., Berchuck A., et al. Oncogenic pathway signatures in human cancers as a guide to targeted therapies. Nature 439 (2006) 353-357
4. Bos P.D., Zhang X.H.F., Nadal C., Shu W., Gomis R.R., Nguyen D.X., Minn A.J., Van de Vijver M., Gerald W.L., Foekens J.A., et al. Genes that mediate breast cancer metastasis to the brain. Nature (2009) 10.1038/nature08021 in press. Published online May 6, 2009
5. Brock M.V., Hooker C.M., Ota-Machida E., Han Y., Guo M., Ames S., Glockner S., Piantadosi S., Gabrielson E., Pridham G., et al. DNA methylation markers and early recurrence in stage I lung cancer. N. Engl. J. Med. 358 (2008) 1118-1128
6. Calvo R., West J., Franklin W., Erickson P., Bemis L., Li E., Helfrich B., Bunn P., Roche J., Brambilla E., et al. Altered HOX and WNT7A expression in human lung cancer. Proc. Natl. Acad. Sci. USA 97 (2000) 12776-12781
7. Chang H.Y., Nuyten D.S., Sneddon J.B., Hastie T., Tibshirani R., Sorlie T., Dai H., He Y.D., van't Veer L.J., Bartelink H., et al. Robustness, scalability, and integration of a wound-response gene expression signature in predicting breast cancer survival. Proc. Natl. Acad. Sci. USA 102 (2005) 3738-3743
8. Chen A.M., Jahan T.M., Jablons D.M., Garcia J., and Larson D.A. Risk of cerebral metastases and neurological death after pathological complete response to neoadjuvant therapy for locally advanced nonsmall-cell lung cancer: clinical implications for the subsequent management of the brain. Cancer 109 (2007) 1668-1675
9. Chitale D., Gong Y., Taylor B., Broderick S., Brennan C., Somwar R., Golas B., Wang L., Motoi N., Szoke J., et al. An integrated genomic analysis of lung cancer reveals loss of DUSP4 in EGFR-mutant tumors. Oncogene (2009) 10.1038/onc.2009.135 in press. Published online June 15, 2009
10. Clevers H. Wnt/beta-catenin signaling in development and disease. Cell 127 (2006) 469-480
11. Ding L., Getz G., Wheeler D.A., Mardis E.R., McLellan M.D., Cibulskis K., Sougnez C., Greulich H., Muzny D.M., Morgan M.B., et al. Somatic mutations affect key pathways in lung adenocarcinoma. Nature 455 (2008) 1069-1075
12. Doki Y., Murakami K., Yamaura T., Sugiyama S., Misaki T., and Saiki I. Mediastinal lymph node metastasis model by orthotopic intrapulmonary implantation of Lewis lung carcinoma cells in mice. Br. J. Cancer 79 (1999) 1121-1126
13. Feld R., Rubinstein L.V., and Weisenberger T.H. Sites of recurrence in resected stage I non-small-cell lung cancer: a guide for future studies. J. Clin. Oncol. 2 (1984) 1352-1358
14. Gaspar L.E. Brain metastases in lung cancer. Expert Rev. Anticancer Ther. 4 (2004) 259-270
15. Gavrilovic I.T., and Posner J.B. Brain metastases: epidemiology and pathophysiology. J. Neurooncol. 75 (2005) 5-14
16. Gottardi C.J., and Gumbiner B.M. Distinct molecular forms of beta-catenin are targeted to adhesive or transcriptional complexes. J. Cell Biol. 167 (2004) 339-349
17. Hatzis P., van der Flier L.G., van Driel M.A., Guryev V., Nielsen F., Denissov S., Nijman I.J., Koster J., Santo E.E., Welboren W., et al. Genome-wide pattern of TCF7L2/TCF4 chromatin occupancy in colorectal cancer cells. Mol. Cell. Biol. 28 (2008) 2732-2744
18. He T.C., Sparks A.B., Rago C., Hermeking H., Zawel L., da Costa L.T., Morin P.J., Vogelstein B., and Kinzler K.W. Identification of c-MYC as a target of the APC pathway. Science 281 (1998) 1509-1512
19. Hess K.R., Varadhachary G.R., Taylor S.H., Wei W., Raber M.N., Lenzi R., and Abbruzzese J.L. Metastatic patterns in adenocarcinoma. Cancer 106 (2006) 1624-1633
20. Hoffman P.C., Mauer A.M., and Vokes E.E. Lung cancer. Lancet 355 (2000) 479-485
21. Hovanes K., Li T.W., Munguia J.E., Truong T., Milovanovic T., Lawrence Marsh J., Holcombe R.F., and Waterman M.L. Beta-catenin-sensitive isoforms of lymphoid enhancer factor-1 are selectively expressed in colon cancer. Nat. Genet. 28 (2001) 53-57
22. Husemann Y., Geigl J.B., Schubert F., Musiani P., Meyer M., Burghart E., Forni G., Eils R., Fehm T., Riethmuller G., et al. Systemic spread is an early step in breast cancer. Cancer Cell 13 (2008) 58-68
23. Jackson E.L., Olive K.P., Tuveson D.A., Bronson R., Crowley D., Brown M., and Jacks T. The differential effects of mutant p53 alleles on advanced murine lung cancer. Cancer Res. 65 (2005) 10280-10288
24. Ji H., Li D., Chen L., Shimamura T., Kobayashi S., McNamara K., Mahmood U., Mitchell A., Sun Y., Al-Hashem R., et al. The impact of human EGFR kinase domain mutations on lung tumorigenesis and in vivo sensitivity to EGFR-targeted therapies. Cancer Cell 9 (2006) 485-495
25. Johnson L., Mercer K., Greenbaum D., Bronson R.T., Crowley D., Tuveson D.A., and Jacks T. Somatic activation of the K-ras oncogene causes early onset lung cancer in mice. Nature 410 (2001) 1111-1116
26. Karnoub A.E., Dash A.B., Vo A.P., Sullivan A., Brooks M.W., Bell G.W., Richardson A.L., Polyak K., Tubo R., and Weinberg R.A. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature 449 (2007) 557-563
27. Karrison T.G., Ferguson D.J., and Meier P. Dormancy of mammary carcinoma after mastectomy. J. Natl. Cancer Inst. 91 (1999) 80-85
28. Kim C.F., Jackson E.L., Woolfenden A.E., Lawrence S., Babar I., Vogel S., Crowley D., Bronson R.T., and Jacks T. Identification of bronchioalveolar stem cells in normal lung and lung cancer. Cell 121 (2005) 823-835
29. Klaus A., and Birchmeier W. Wnt signalling and its impact on development and cancer. Nat. Rev. Cancer 8 (2008) 387-398
30. Klein C.A., Schmidt-Kittler O., Schardt J.A., Pantel K., Speicher M.R., and Riethmuller G. Comparative genomic hybridization, loss of heterozygosity, and DNA sequence analysis of single cells. Proc. Natl. Acad. Sci. USA 96 (1999) 4494-4499
31. Koizumi F., Shimoyama T., Taguchi F., Saijo N., and Nishio K. Establishment of a human non-small cell lung cancer cell line resistant to gefitinib. Int. J. Cancer 116 (2005) 36-44
32. Korinek V., Barker N., Morin P.J., van Wichen D., de Weger R., Kinzler K.W., Vogelstein B., and Clevers H. Constitutive transcriptional activation by a beta-catenin-Tcf complex in APC-/- colon carcinoma. Science 275 (1997) 1784-1787
33. Licchesi J.D., Westra W.H., Hooker C.M., Machida E.O., Baylin S.B., and Herman J.G. Epigenetic alteration of Wnt pathway antagonists in progressive glandular neoplasia of the lung. Carcinogenesis 29 (2008) 895-904
34. Logan C.Y., and Nusse R. The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 20 (2004) 781-810
35. Martini N., Bains M.S., Burt M.E., Zakowski M.F., McCormack P., Rusch V.W., and Ginsberg R.J. Incidence of local recurrence and second primary tumors in resected stage I lung cancer. J. Thorac. Cardiovasc. Surg. 109 (1995) 120-129
36. Mazieres J., He B., You L., Xu Z., and Jablons D.M. Wnt signaling in lung cancer. Cancer Lett. 222 (2005) 1-10
37. Minn A.J., Gupta G.P., Siegel P.M., Bos P.D., Shu W., Giri D.D., Viale A., Olshen A.B., Gerald W.L., and Massagué J. Genes that mediate breast cancer metastasis to lung. Nature 436 (2005) 518-524
38. Minn A.J., Kang Y., Serganova I., Gupta G.P., Giri D.D., Doubrovin M., Ponomarev V., Gerald W.L., Blasberg R., and Massagué J. Distinct organ-specific metastatic potential of individual breast cancer cells and primary tumors. J. Clin. Invest. 115 (2005) 44-55
39. Moon R.T., Kohn A.D., De Ferrari G.V., and Kaykas A. WNT and beta-catenin signalling: diseases and therapies. Nat. Rev. Genet. 5 (2004) 691-701
40. Morin P.J., Sparks A.B., Korinek V., Barker N., Clevers H., Vogelstein B., and Kinzler K.W. Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC. Science 275 (1997) 1787-1790
41. Nguyen D.X., Bos P.D., and Massagué J. Metastasis: from dissemination to organ-specific colonization. Nat. Rev. Cancer 9 (2009) 274-284
42. Omuro A.M., Kris M.G., Miller V.A., Franceschi E., Shah N., Milton D.T., and Abrey L.E. High incidence of disease recurrence in the brain and leptomeninges in patients with nonsmall cell lung carcinoma after response to gefitinib. Cancer 103 (2005) 2344-2348
43. Padua D., Zhang X.H., Wang Q., Nadal C., Gerald W.L., Gomis R.R., and Massagué J. TGFbeta primes breast tumors for lung metastasis seeding through angiopoietin-like 4. Cell 133 (2008) 66-77
44. Phelps R.M., Johnson B.E., Ihde D.C., Gazdar A.F., Carbone D.P., McClintock P.R., Linnoila R.I., Matthews M.J., Bunn Jr. P.A., Carney D., et al. NCI-Navy Medical Oncology Branch cell line data base. J. Cell. Biochem. Suppl. 24 (1996) 32-91
45. Polakis P. The many ways of Wnt in cancer. Curr. Opin. Genet. Dev. 17 (2007) 45-51
46. Politi K., Zakowski M.F., Fan P.D., Schonfeld E.A., Pao W., and Varmus H.E. Lung adenocarcinomas induced in mice by mutant EGF receptors found in human lung cancers respond to a tyrosine kinase inhibitor or to down-regulation of the receptors. Genes Dev. 20 (2006) 1496-1510
47. Rodenhuis S., Slebos R.J., Boot A.J., Evers S.G., Mooi W.J., Wagenaar S.S., van Bodegom P.C., and Bos J.L. Incidence and possible clinical significance of K-ras oncogene activation in adenocarcinoma of the human lung. Cancer Res. 48 (1988) 5738-5741
48. Sasaki Y., Shinkai T., Eguchi K., Tamura T., Ohe Y., Ohmori T., and Saijo N. Prediction of the antitumor activity of new platinum analogs based on their ex vivo pharmacodynamics as determined by bioassay. Cancer Chemother. Pharmacol. 27 (1991) 263-270
49. Schmidt-Kittler O., Ragg T., Daskalakis A., Granzow M., Ahr A., Blankenstein T.J., Kaufmann M., Diebold J., Arnholdt H., Muller P., et al. From latent disseminated cells to overt metastasis: genetic analysis of systemic breast cancer progression. Proc. Natl. Acad. Sci. USA 100 (2003) 7737-7742
50. Sharma S.V., Bell D.W., Settleman J., and Haber D.A. Epidermal growth factor receptor mutations in lung cancer. Nat. Rev. Cancer 7 (2007) 169-181
51. Shedden K., Taylor J.M., Enkemann S.A., Tsao M.S., Yeatman T.J., Gerald W.L., Eschrich S., Jurisica I., Giordano T.J., Misek D.E., et al. Gene expression-based survival prediction in lung adenocarcinoma: a multi-site, blinded validation study. Nat. Med. 14 (2008) 822-827
52. Shu W., Guttentag S., Wang Z., Andl T., Ballard P., Lu M.M., Piccolo S., Birchmeier W., Whitsett J.A., Millar S.E., et al. Wnt/beta-catenin signaling acts upstream of N-myc, BMP4, and FGF signaling to regulate proximal-distal patterning in the lung. Dev. Biol. 283 (2005) 226-239
53. Sweet-Cordero A., Mukherjee S., Subramanian A., You H., Roix J.J., Ladd-Acosta C., Mesirov J., Golub T.R., and Jacks T. An oncogenic KRAS2 expression signature identified by cross-species gene-expression analysis. Nat. Genet. 37 (2005) 48-55
54. ten Dijke P., Korchynskyi O., Valdimarsdottir G., and Goumans M.J. Controlling cell fate by bone morphogenetic protein receptors. Mol. Cell. Endocrinol. 211 (2003) 105-113
55. Thomas A.J., Rock J.P., Johnson C.C., Weiss L., Jacobsen G., and Rosenblum M.L. Survival of patients with synchronous brain metastases: an epidemiological study in southeastern Michigan. J. Neurosurg. 93 (2000) 927-931
56. van de Wetering M., Sancho E., Verweij C., de Lau W., Oving I., Hurlstone A., van der Horn K., Batlle E., Coudreuse D., Haramis A.P., et al. The beta-catenin/TCF-4 complex imposes a crypt progenitor phenotype on colorectal cancer cells. Cell 111 (2002) 241-250
57. Varga A.C., and Wrana J.L. The disparate role of BMP in stem cell biology. Oncogene 24 (2005) 5713-5721
58. Xu L., Shen S.S., Hoshida Y., Subramanian A., Ross K., Brunet J.P., Wagner S.N., Ramaswamy S., Mesirov J.P., and Hynes R.O. Gene expression changes in an animal melanoma model correlate with aggressiveness of human melanoma metastases. Mol. Cancer Res. 6 (2008) 760-769
59. Zhang Y., Goss A.M., Cohen E.D., Kadzik R., Lepore J.J., Muthukumaraswamy K., Yang J., DeMayo F.J., Whitsett J.A., Parmacek M.S., et al. A Gata6-Wnt pathway required for epithelial stem cell development and airway regeneration. Nat. Genet. 40 (2008) 862-870
60. Zheng S., El-Naggar A.K., Kim E.S., Kurie J.M., and Lozano G. A genetic mouse model for metastatic lung cancer with gender differences in survival. Oncogene 26 (2007) 6896-6904