LKB1/STK11 Inactivation Leads to Expansion of a Prometastatic Tumor Subpopulation in Melanoma

Cancer Cell

Volumn 21, Issue 6, 2012, Pages 751-764

  Liu, Wenjin ^a   Monahan, Kimberly B ^a   Pfefferle, Adam D ^a   Shimamura, Takeshi ^c   Sorrentino, Jessica ^a   Chan, Keefe T ^a   Roadcap, David W ^a   Ollila, David W ^a   Thomas, Nancy E ^a   Castrillon, Diego H ^d   Miller, C Ryan ^a   Perou, Charles M ^a,b   Wong, Kwok Kin ^e   Bear, James E ^a   Sharpless, Norman E ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c LOYOLA UNIVERSITY CHICAGO   (United States)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^e DANA FARBER CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD24 ANTIGEN; K RAS PROTEIN; LENTIVIRUS VECTOR; PROTEIN KINASE LKB1; PROTEIN TYROSINE KINASE; SHORT HAIRPIN RNA; SMALL INTERFERING RNA; WNT PROTEIN;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ARTICLE; CANCER GROWTH; CELL EXPANSION; CLONOGENIC ASSAY; GENE ACTIVATION; GENE DELETION; GENE INACTIVATION; GENE TARGETING; IN VITRO STUDY; IN VIVO STUDY; MELANOCYTE; MELANOMA; METASTASIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMETASTATIC CD24+ T LYMPHOCYTE TUMOR SUBPOPULATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SRC HOMOLOGY DOMAIN; T LYMPHOCYTE SUBPOPULATION; TRANSCRIPTION REGULATION; TUMOR CELL;

EID: 84862119127     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccr.2012.03.048     Document Type: Article

References (53)

1. Ackermann J., Frutschi M., Kaloulis K., McKee T., Trumpp A., Beermann F. Metastasizing melanoma formation caused by expression of activated N-RasQ61K on an INK4a-deficient background. Cancer Res. 2005, 65:4005-4011.
2. Alessi D.R., Sakamoto K., Bayascas J.R. LKB1-dependent signaling pathways. Annu. Rev. Biochem. 2006, 75:137-163.
3. Al-Hajj M., Wicha M.S., Benito-Hernandez A., Morrison S.J., Clarke M.F. Prospective identification of tumorigenic breast cancer cells. Proc. Natl. Acad. Sci. USA 2003, 100:3983-3988.
4. Bardeesy N., Sinha M., Hezel A.F., Signoretti S., Hathaway N.A., Sharpless N.E., Loda M., Carrasco D.R., DePinho R.A. Loss of the Lkb1 tumour suppressor provokes intestinal polyposis but resistance to transformation. Nature 2002, 419:162-167.
5. Baumann P., Cremers N., Kroese F., Orend G., Chiquet-Ehrismann R., Uede T., Yagita H., Sleeman J.P. CD24 expression causes the acquisition of multiple cellular properties associated with tumor growth and metastasis. Cancer Res. 2005, 65:10783-10793.
6. Bennett D.C., Cooper P.J., Dexter T.J., Devlin L.M., Heasman J., Nester B. Cloned mouse melanocyte lines carrying the germline mutations albino and brown: complementation in culture. Development 1989, 105:379-385.
7. Bosenberg M., Muthusamy V., Curley D.P., Wang Z., Hobbs C., Nelson B., Nogueira C., Horner J.W., Depinho R., Chin L. Characterization of melanocyte-specific inducible Cre recombinase transgenic mice. Genesis 2006, 44:262-267.
8. Carretero J., Shimamura T., Rikova K., Jackson A.L., Wilkerson M.D., Borgman C.L., Buttarazzi M.S., Sanofsky B.A., McNamara K.L., Brandstetter K.A., et al. Integrative genomic and proteomic analyses identify targets for Lkb1-deficient metastatic lung tumors. Cancer Cell 2010, 17:547-559.
9. Cheng H., Liu P., Wang Z.C., Zou L., Santiago S., Garbitt V., Gjoerup O.V., Iglehart J.D., Miron A., Richardson A.L., et al. SIK1 couples LKB1 to p53-dependent anoikis and suppresses metastasis. Sci. Signal. 2009, 2:ra35.
10. Chin L., Pomerantz J., Polsky D., Jacobson M., Cohen C., Cordon-Cardo C., Horner J.W., DePinho R.A. Cooperative effects of INK4a and ras in melanoma susceptibility in vivo. Genes Dev. 1997, 11:2822-2834.
11. Damsky W.E., Curley D.P., Santhanakrishnan M., Rosenbaum L.E., Platt J.T., Gould Rothberg B.E., Taketo M.M., Dankort D., Rimm D.L., McMahon M., Bosenberg M. beta-Catenin signaling controls metastasis in Braf-activated Pten-deficient melanomas. Cancer Cell 2011, 20:741-754.
12. Dankort D., Curley D.P., Cartlidge R.A., Nelson B., Karnezis A.N., Damsky W.E., You M.J., DePinho R.A., McMahon M., Bosenberg M. Braf(V600E) cooperates with Pten loss to induce metastatic melanoma. Nat. Genet. 2009, 41:544-552.
13. Deguchi Y., Kimura S., Ashihara E., Niwa T., Hodohara K., Fujiyama Y., Maekawa T. Comparison of imatinib, dasatinib, nilotinib and INNO-406 in imatinib-resistant cell lines. Leuk. Res. 2008, 32:980-983.
14. Esteve-Puig R., Canals F., Colome N., Merlino G., Recio J.A. Uncoupling of the LKB1-AMPKalpha energy sensor pathway by growth factors and oncogenic BRAF. PLoS One 2009, 4:e4771.
15. Forbes S.A., Bindal N., Bamford S., Cole C., Kok C.Y., Beare D., Jia M., Shepherd R., Leung K., Menzies A., et al. COSMIC: mining complete cancer genomes in the Catalogue of Somatic Mutations in Cancer. Nucleic Acids Res. 2011, 39:D945-D950.
16. Gao M.Q., Choi Y.P., Kang S., Youn J.H., Cho N.H. CD24+ cells from hierarchically organized ovarian cancer are enriched in cancer stem cells. Oncogene 2010, 29:2672-2680.
17. Giardiello F.M., Brensinger J.D., Tersmette A.C., Goodman S.N., Petersen G.M., Booker S.V., Cruz-Correa M., Offerhaus J.A. Very high risk of cancer in familial Peutz-Jeghers syndrome. Gastroenterology 2000, 119:1447-1453.
18. Guervos M.A., Marcos C.A., Hermsen M., Nuno A.S., Suarez C., Llorente J.L. Deletions of N33, STK11 and TP53 are involved in the development of lymph node metastasis in larynx and pharynx carcinomas. Cell. Oncol. 2007, 29:327-334.
19. Guldberg P., thor Straten P., Ahrenkiel V., Seremet T., Kirkin A.F., Zeuthen J. Somatic mutation of the Peutz-Jeghers syndrome gene, LKB1/STK11, in malignant melanoma. Oncogene 1999, 18:1777-1780.
20. Guy C.T., Cardiff R.D., Muller W.J. Induction of mammary tumors by expression of polyomavirus middle T oncogene: a transgenic mouse model for metastatic disease. Mol. Cell. Biol. 1992, 12:954-961.
21. Haigis K.M., Kendall K.R., Wang Y., Cheung A., Haigis M.C., Glickman J.N., Niwa-Kawakita M., Sweet-Cordero A., Sebolt-Leopold J., Shannon K.M., et al. Differential effects of oncogenic K-Ras and N-Ras on proliferation, differentiation and tumor progression in the colon. Nat. Genet. 2008, 40:600-608.
22. Hamamura K., Tsuji M., Hotta H., Ohkawa Y., Takahashi M., Shibuya H., Nakashima H., Yamauchi Y., Hashimoto N., Hattori H., et al. Functional Activation of Src Family Kinase Yes Protein Is Essential for the Enhanced Malignant Properties of Human Melanoma Cells Expressing Ganglioside GD3. J. Biol. Chem. 2011, 286:18526-18537.
23. Homsi J., Cubitt C.L., Zhang S., Munster P.N., Yu H., Sullivan D.M., Jove R., Messina J.L., Daud A.I. Src activation in melanoma and Src inhibitors as therapeutic agents in melanoma. Melanoma Res. 2009, 19:167-175.
24. Jeghers H., Mc K.V., Katz K.H. Generalized intestinal polyposis and melanin spots of the oral mucosa, lips and digits; a syndrome of diagnostic significance. N. Engl. J. Med. 1949, 241:1031-1036.
25. Ji H., Ramsey M.R., Hayes D.N., Fan C., McNamara K., Kozlowski P., Torrice C., Wu M.C., Shimamura T., Perera S.A., et al. LKB1 modulates lung cancer differentiation and metastasis. Nature 2007, 448:807-810.
26. Johnson L., Mercer K., Greenbaum D., Bronson R.T., Crowley D., Tuveson D.A., Jacks T. Somatic activation of the K-ras oncogene causes early onset lung cancer in mice. Nature 2001, 410:1111-1116.
27. Jones R.G., Plas D.R., Kubek S., Buzzai M., Mu J., Xu Y., Birnbaum M.J., Thompson C.B. AMP-activated protein kinase induces a p53-dependent metabolic checkpoint. Mol. Cell 2005, 18:283-293.
28. Jonkers J., Meuwissen R., van der Gulden H., Peterse H., van der Valk M., Berns A. Synergistic tumor suppressor activity of BRCA2 and p53 in a conditional mouse model for breast cancer. Nat. Genet. 2001, 29:418-425.
29. Karuman P., Gozani O., Odze R.D., Zhou X.C., Zhu H., Shaw R., Brien T.P., Bozzuto C.D., Ooi D., Cantley L.C., Yuan J. The Peutz-Jegher gene product LKB1 is a mediator of p53-dependent cell death. Mol. Cell 2001, 7:1307-1319.
30. Kluger H.M., Dudek A.Z., McCann C., Ritacco J., Southard N., Jilaveanu L.B., Molinaro A., Sznol M. A phase 2 trial of dasatinib in advanced melanoma. Cancer 2011, 117:2202-2208.
31. Konecny G.E., Glas R., Dering J., Manivong K., Qi J., Finn R.S., Yang G.R., Hong K.L., Ginther C., Winterhoff B., et al. Activity of the multikinase inhibitor dasatinib against ovarian cancer cells. Br. J. Cancer 2009, 101:1699-1708.
32. Kristiansen G., Schluns K., Yongwei Y., Denkert C., Dietel M., Petersen I. CD24 is an independent prognostic marker of survival in nonsmall cell lung cancer patients. Br. J. Cancer 2003, 88:231-236.
33. Lee T.K., Castilho A., Cheung V.C., Tang K.H., Ma S., Ng I.O. CD24(+) liver tumor-initiating cells drive self-renewal and tumor initiation through STAT3-mediated NANOG regulation. Cell Stem Cell 2011, 9:50-63.
34. Lim W., Olschwang S., Keller J.J., Westerman A.M., Menko F.H., Boardman L.A., Scott R.J., Trimbath J., Giardiello F.M., Gruber S.B., et al. Relative frequency and morphology of cancers in STK11 mutation carriers. Gastroenterology 2004, 126:1788-1794.
35. Loganzo F., Dosik J.S., Zhao Y., Vidal M.J., Nanus D.M., Sudol M., Albino A.P. Elevated expression of protein tyrosine kinase c-Yes, but not c-Src, in human malignant melanoma. Oncogene 1993, 8:2637-2644.
36. Marchetti D., Parikh N., Sudol M., Gallick G.E. Stimulation of the protein tyrosine kinase c-Yes but not c-Src by neurotrophins in human brain-metastatic melanoma cells. Oncogene 1998, 16:3253-3260.
37. Matsumoto S., Iwakawa R., Takahashi K., Kohno T., Nakanishi Y., Matsuno Y., Suzuki K., Nakamoto M., Shimizu E., Minna J.D., Yokota J. Prevalence and specificity of LKB1 genetic alterations in lung cancers. Oncogene 2007, 26:5911-5918.
38. Monahan K.B., Rozenberg G.I., Krishnamurthy J., Johnson S.M., Liu W., Bradford M.K., Horner J., Depinho R.A., Sharpless N.E. Somatic p16(INK4a) loss accelerates melanomagenesis. Oncogene 2010, 29:5809-5817.
39. Putnam A.J., Schulz V.V., Freiter E.M., Bill H.M., Miranti C.K. Src, PKCalpha, and PKCdelta are required for alphavbeta3 integrin-mediated metastatic melanoma invasion. Cell Commun. Signal. 2009, 7:10.
40. Rowan A., Bataille V., MacKie R., Healy E., Bicknell D., Bodmer W., Tomlinson I. Somatic mutations in the Peutz-Jeghers (LKB1/STKII) gene in sporadic malignant melanomas. J. Invest. Dermatol. 1999, 112:509-511.
41. Sanchez-Cespedes M. A role for LKB1 gene in human cancer beyond the Peutz-Jeghers syndrome. Oncogene 2007, 26:7825-7832.
42. Scott K.L., Nogueira C., Heffernan T.P., van Doorn R., Dhakal S., Hanna J.A., Min C., Jaskelioff M., Xiao Y., Wu C.J., et al. Proinvasion metastasis drivers in early-stage melanoma are oncogenes. Cancer Cell 2011, 20:92-103.
43. Senner V., Sturm A., Baur I., Schrell U.H., Distel L., Paulus W. CD24 promotes invasion of glioma cells in vivo. J. Neuropathol. Exp. Neurol. 1999, 58:795-802.
44. Shah U., Sharpless N.E., Hayes D.N. LKB1 and lung cancer: more than the usual suspects. Cancer Res. 2008, 68:3562-3565.
45. Sharpless N.E., Alson S., Chan S., Silver D.P., Castrillon D.H., DePinho R.A. p16(INK4a) and p53 deficiency cooperate in tumorigenesis. Cancer Res. 2002, 62:2761-2765.
46. Shields J.M., Thomas N.E., Cregger M., Berger A.J., Leslie M., Torrice C., Hao H., Penland S., Arbiser J., Scott G., et al. Lack of extracellular signal-regulated kinase mitogen-activated protein kinase signaling shows a new type of melanoma. Cancer Res. 2007, 67:1502-1512.
47. Stuelten C.H., Mertins S.D., Busch J.I., Gowens M., Scudiero D.A., Burkett M.W., Hite K.M., Alley M., Hollingshead M., Shoemaker R.H., Niederhuber J.E. Complex display of putative tumor stem cell markers in the NCI60 tumor cell line panel. Stem Cells 2010, 28:649-660.
48. Sviderskaya E.V., Hill S.P., Evans-Whipp T.J., Chin L., Orlow S.J., Easty D.J., Cheong S.C., Beach D., DePinho R.A., Bennett D.C. p16(Ink4a) in melanocyte senescence and differentiation. J. Natl. Cancer Inst. 2002, 94:446-454.
49. Taliaferro-Smith L., Nagalingam A., Zhong D., Zhou W., Saxena N.K., Sharma D. LKB1 is required for adiponectin-mediated modulation of AMPK-S6K axis and inhibition of migration and invasion of breast cancer cells. Oncogene 2009, 28:2621-2633.
50. Weir B.A., Woo M.S., Getz G., Perner S., Ding L., Beroukhim R., Lin W.M., Province M.A., Kraja A., Johnson L.A., et al. Characterizing the cancer genome in lung adenocarcinoma. Nature 2007, 450:893-898.
51. Wingo S.N., Gallardo T.D., Akbay E.A., Liang M.C., Contreras C.M., Boren T., Shimamura T., Miller D.S., Sharpless N.E., Bardeesy N., et al. Somatic LKB1 mutations promote cervical cancer progression. PLoS One 2009, 4:e5137.
52. Zhang Z., Liu S., Shi R., Zhao G. miR-27 promotes human gastric cancer cell metastasis by inducing epithelial-to-mesenchymal transition. Cancer Genet. 2011, 204:486-491.
53. Zheng B., Jeong J.H., Asara J.M., Yuan Y.Y., Granter S.R., Chin L., Cantley L.C. Oncogenic B-RAF negatively regulates the tumor suppressor LKB1 to promote melanoma cell proliferation. Mol. Cell 2009, 33:237-247.