Metastatic Latency and Immune Evasion through Autocrine Inhibition of WNT

Cell

Volumn 165, Issue 1, 2016, Pages 45-60

  Malladi, Srinivas ^a   MacAlinao, Danilo G ^a,b   Jin, Xin ^a,c   He, Lan ^a   Basnet, Harihar ^a   Zou, Yilong ^a,b   De Stanchina, Elisa ^a   Massagué, Joan ^a,c  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b Gerstner Sloan Kettering Graduate School of Biomedical Sciences   (United States)

^c BROAD INSTITUTE OF MIT AND HARVARD   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DICKKOPF 1 PROTEIN; TRANSCRIPTION FACTOR SOX2; TRANSCRIPTION FACTOR SOX9; DKK1 PROTEIN, HUMAN; SIGNAL PEPTIDE; SOX2 PROTEIN, HUMAN; SOX9 PROTEIN, HUMAN; TRANSCRIPTION FACTOR SOX;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOCRINE EFFECT; BREAST CANCER CELL LINE; CANCER CELL; CANCER INHIBITION; CANCER STAGING; CELL AGING; CELL ISOLATION; CELL SURVIVAL; CELLULAR DISTRIBUTION; DOWN REGULATION; FEMALE; HUMAN; HUMAN CELL; IMMUNE EVASION; IMMUNOSURVEILLANCE; INNATE IMMUNITY; LATENCY COMPETENT CANCER CELL; LONG TERM SURVIVAL; LUNG CANCER CELL LINE; METASTASIS; MOUSE; NATURAL KILLER CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; WNT SIGNALING PATHWAY; ANIMAL; BREAST TUMOR; IMMUNOLOGY; LUNG TUMOR; METABOLISM; NUDE MOUSE; PATHOLOGY; TUMOR CELL LINE; TUMOR ESCAPE;

ANIMALS; AUTOCRINE COMMUNICATION; BREAST NEOPLASMS; CELL LINE, TUMOR; FEMALE; HUMANS; IMMUNOLOGIC SURVEILLANCE; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; KILLER CELLS, NATURAL; LUNG NEOPLASMS; MICE; MICE, NUDE; NEOPLASM METASTASIS; SOX9 TRANSCRIPTION FACTOR; SOXB1 TRANSCRIPTION FACTORS; TUMOR ESCAPE; WNT SIGNALING PATHWAY;

EID: 84961784476     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2016.02.025     Document Type: Article

References (59)

1. M. Al-Hajj, M.S. Wicha, A. Benito-Hernandez, S.J. Morrison, and M.F. Clarke Prospective identification of tumorigenic breast cancer cells Proc. Natl. Acad. Sci. USA 100 2003 3983 3988
2. K. Arnold, A. Sarkar, M.A. Yram, J.M. Polo, R. Bronson, S. Sengupta, M. Seandel, N. Geijsen, and K. Hochedlinger Sox2(+) adult stem and progenitor cells are important for tissue regeneration and survival of mice Cell Stem Cell 9 2011 317 329
3. C.J. Aslakson, and F.R. Miller Selective events in the metastatic process defined by analysis of the sequential dissemination of subpopulations of a mouse mammary tumor Cancer Res. 52 1992 1399 1405
4. A.J. Bass, H. Watanabe, C.H. Mermel, S. Yu, S. Perner, R.G. Verhaak, S.Y. Kim, L. Wardwell, P. Tamayo, I. Gat-Viks, and et al. SOX2 is an amplified lineage-survival oncogene in lung and esophageal squamous cell carcinomas Nat. Genet. 41 2009 1238 1242
5. M. Bradley, A. Zeytun, A. Rafi-Janajreh, P.S. Nagarkatti, and M. Nagarkatti Role of spontaneous and interleukin-2-induced natural killer cell activity in the cytotoxicity and rejection of Fas+ and Fas- tumor cells Blood 92 1998 4248 4255
6. P. Bragado, Y. Estrada, F. Parikh, S. Krause, C. Capobianco, H.G. Farina, D.M. Schewe, and J.A. Aguirre-Ghiso TGF-β2 dictates disseminated tumour cell fate in target organs through TGF-β-RIII and p38α/β signalling Nat. Cell Biol. 15 2013 1351 1361
7. S. Braun, F.D. Vogl, B. Naume, W. Janni, M.P. Osborne, R.C. Coombes, G. Schlimok, I.J. Diel, B. Gerber, G. Gebauer, and et al. A pooled analysis of bone marrow micrometastasis in breast cancer N. Engl. J. Med. 353 2005 793 802
8. D. Croft, A.F. Mundo, R. Haw, M. Milacic, J. Weiser, G. Wu, M. Caudy, P. Garapati, M. Gillespie, M.R. Kamdar, and et al. The Reactome pathway knowledgebase Nucleic Acids Res. 42 2014 D472 D477
9. Y.S. DeRose, G. Wang, Y.C. Lin, P.S. Bernard, S.S. Buys, M.T. Ebbert, R. Factor, C. Matsen, B.A. Milash, E. Nelson, and et al. Tumor grafts derived from women with breast cancer authentically reflect tumor pathology, growth, metastasis and disease outcomes Nat. Med. 17 2011 1514 1520
10. G. Dontu, W.M. Abdallah, J.M. Foley, K.W. Jackson, M.F. Clarke, M.J. Kawamura, and M.S. Wicha In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells Genes Dev. 17 2003 1253 1270
11. R. Duchnowska, R. Dziadziuszko, B. Czartoryska-Arłukowicz, B. Radecka, B. Szostakiewicz, K. Sosińska-Mielcarek, A. Karpińska, E. Starosławska, T. Kubiatowski, and C. Szczylik Risk factors for brain relapse in HER2-positive metastatic breast cancer patients Breast Cancer Res. Treat. 117 2009 297 303
12. G.P. Dunn, L.J. Old, and R.D. Schreiber The immunobiology of cancer immunosurveillance and immunoediting Immunity 21 2004 137 148
13. J. Eyles, A.L. Puaux, X. Wang, B. Toh, C. Prakash, M. Hong, T.G. Tan, L. Zheng, L.C. Ong, Y. Jin, and et al. Tumor cells disseminate early, but immunosurveillance limits metastatic outgrowth, in a mouse model of melanoma J. Clin. Invest. 120 2010 2030 2039
14. C. Fuerer, and R. Nusse Lentiviral vectors to probe and manipulate the Wnt signaling pathway PLoS ONE 5 2010 e9370
15. H. Gao, G. Chakraborty, A.P. Lee-Lim, Q. Mo, M. Decker, A. Vonica, R. Shen, E. Brogi, A.H. Brivanlou, and F.G. Giancotti The BMP inhibitor Coco reactivates breast cancer cells at lung metastatic sites Cell 150 2012 764 779
16. A.F. Gazdar, and J.D. Minna NCI series of cell lines: An historical perspective J. Cell. Biochem. Suppl. 24 1996 1 11
17. A.F. Gazdar, V. Kurvari, A. Virmani, L. Gollahon, M. Sakaguchi, M. Westerfield, D. Kodagoda, V. Stasny, H.T. Cunningham, I.I. Wistuba, and et al. Characterization of paired tumor and non-tumor cell lines established from patients with breast cancer Int. J. Cancer 78 1998 766 774
18. P.E. Goss, and A.F. Chambers Does tumour dormancy offer a therapeutic target? Nat. Rev. Cancer 10 2010 871 877
19. W. Guo, Z. Keckesova, J.L. Donaher, T. Shibue, V. Tischler, F. Reinhardt, S. Itzkovitz, A. Noske, U. Zürrer-Härdi, G. Bell, and et al. Slug and Sox9 cooperatively determine the mammary stem cell state Cell 148 2012 1015 1028
20. T.C. He, A.B. Sparks, C. Rago, H. Hermeking, L. Zawel, L.T. da Costa, P.J. Morin, B. Vogelstein, and K.W. Kinzler Identification of c-MYC as a target of the APC pathway Science 281 1998 1509 1512
21. N.D. Heintzman, G.C. Hon, R.D. Hawkins, P. Kheradpour, A. Stark, L.F. Harp, Z. Ye, L.K. Lee, R.K. Stuart, C.W. Ching, and et al. Histone modifications at human enhancers reflect global cell-type-specific gene expression Nature 459 2009 108 112
22. S. Jin, Y. Deng, J.W. Hao, Y. Li, B. Liu, Y. Yu, F.D. Shi, and Q.H. Zhou NK cell phenotypic modulation in lung cancer environment PLoS ONE 9 2014 e109976
23. M. Kasai, T. Yoneda, S. Habu, Y. Maruyama, K. Okumura, and T. Tokunaga In vivo effect of anti-asialo GM1 antibody on natural killer activity Nature 291 1981 334 335
24. T. Kitamura, B.Z. Qian, and J.W. Pollard Immune cell promotion of metastasis Nat. Rev. Immunol. 15 2015 73 86
25. A. Kobayashi, H. Okuda, F. Xing, P.R. Pandey, M. Watabe, S. Hirota, S.K. Pai, W. Liu, K. Fukuda, C. Chambers, and et al. Bone morphogenetic protein 7 in dormancy and metastasis of prostate cancer stem-like cells in bone J. Exp. Med. 208 2011 2641 2655
26. U. Kordes, and C. Hagel Expression of SOX9 and SOX10 in central neuroepithelial tumor J. Neurooncol. 80 2006 151 155
27. L.L. Lanier NKG2D receptor and its ligands in host defense Cancer Immunol. Res. 3 2015 575 582
28. L. Li, and H. Clevers Coexistence of quiescent and active adult stem cells in mammals Science 327 2010 542 545
29. W.H. Lien, and E. Fuchs Wnt some lose some: Transcriptional governance of stem cells by Wnt/β-catenin signaling Genes Dev. 28 2014 1517 1532
30. E. Lim, D. Wu, B. Pal, T. Bouras, M.L. Asselin-Labat, F. Vaillant, H. Yagita, G.J. Lindeman, G.K. Smyth, and J.E. Visvader Transcriptome analyses of mouse and human mammary cell subpopulations reveal multiple conserved genes and pathways Breast Cancer Res. 12 2010 R21
31. S. Liu, Y. Cong, D. Wang, Y. Sun, L. Deng, Y. Liu, R. Martin-Trevino, L. Shang, S.P. McDermott, M.D. Landis, and et al. Breast cancer stem cells transition between epithelial and mesenchymal states reflective of their normal counterparts Stem Cell Reports 2 2014 78 91
32. H.G. Ljunggren, and K.J. Malmberg Prospects for the use of NK cells in immunotherapy of human cancer Nat. Rev. Immunol. 7 2007 329 339
33. R.M. MacKie, R. Reid, and B. Junor Fatal melanoma transferred in a donated kidney 16 years after melanoma surgery N. Engl. J. Med. 348 2003 567 568
34. R. Maeda, J. Yoshida, T. Hishida, K. Aokage, M. Nishimura, Y. Nishiwaki, and K. Nagai Late recurrence of non-small cell lung cancer more than 5 years after complete resection: Incidence and clinical implications in patient follow-up Chest 138 2010 145 150
35. I. Malanchi, A. Santamaria-Martínez, E. Susanto, H. Peng, H.A. Lehr, J.F. Delaloye, and J. Huelsken Interactions between cancer stem cells and their niche govern metastatic colonization Nature 481 2012 85 89
36. L. Martinet, and M.J. Smyth Balancing natural killer cell activation through paired receptors Nat. Rev. Immunol. 15 2015 243 254
37. J. Massagué TGFβ signalling in context Nat. Rev. Mol. Cell Biol. 13 2012 616 630
38. J. Massagué, and A.C. Obenauf Metastatic colonization by circulating tumour cells Nature 529 2016 298 306 10.1038/nature17038
39. D.X. Nguyen, A.C. Chiang, X.H. Zhang, J.Y. Kim, M.G. Kris, M. Ladanyi, W.L. Gerald, and J. Massagué WNT/TCF signaling through LEF1 and HOXB9 mediates lung adenocarcinoma metastasis Cell 138 2009 51 62
40. T. O'Sullivan, R. Saddawi-Konefka, W. Vermi, C.M. Koebel, C. Arthur, J.M. White, R. Uppaluri, D.M. Andrews, S.F. Ngiow, M.W. Teng, and et al. Cancer immunoediting by the innate immune system in the absence of adaptive immunity J. Exp. Med. 209 2012 1869 1882
41. T. Oskarsson, S. Acharyya, X.H. Zhang, S. Vanharanta, S.F. Tavazoie, P.G. Morris, R.J. Downey, K. Manova-Todorova, E. Brogi, and J. Massagué Breast cancer cells produce tenascin C as a metastatic niche component to colonize the lungs Nat. Med. 17 2011 867 874
42. S.B. Park, K.W. Seo, A.Y. So, M.S. Seo, K.R. Yu, S.K. Kang, and K.S. Kang SOX2 has a crucial role in the lineage determination and proliferation of mesenchymal stem cells through Dickkopf-1 and c-MYC Cell Death Differ. 19 2012 534 545
43. M. Pelleitier, and S. Montplaisir The nude mouse: A model of deficient T-cell function Methods Achiev. Exp. Pathol. 7 1975 149 166
44. C.M. Rudin, S. Durinck, E.W. Stawiski, J.T. Poirier, Z. Modrusan, D.S. Shames, E.A. Bergbower, Y. Guan, J. Shin, J. Guillory, and et al. Comprehensive genomic analysis identifies SOX2 as a frequently amplified gene in small-cell lung cancer Nat. Genet. 44 2012 1111 1116
45. A. Sarkar, and K. Hochedlinger The sox family of transcription factors: Versatile regulators of stem and progenitor cell fate Cell Stem Cell 12 2013 15 30
46. E. Seo, U. Basu-Roy, P.H. Gunaratne, C. Coarfa, D.S. Lim, C. Basilico, and A. Mansukhani SOX2 regulates YAP1 to maintain stemness and determine cell fate in the osteo-adipo lineage Cell Rep. 3 2013 2075 2087
47. L.D. Shultz, B.L. Lyons, L.M. Burzenski, B. Gott, X. Chen, S. Chaleff, M. Kotb, S.D. Gillies, M. King, J. Mangada, and et al. Human lymphoid and myeloid cell development in NOD/LtSz-scid IL2R gamma null mice engrafted with mobilized human hemopoietic stem cells J. Immunol. 174 2005 6477 6489
48. D.K. Sojka, B. Plougastel-Douglas, L. Yang, M.A. Pak-Wittel, M.N. Artyomov, Y. Ivanova, C. Zhong, J.M. Chase, P.B. Rothman, J. Yu, and et al. Tissue-resident natural killer (NK) cells are cell lineages distinct from thymic and conventional splenic NK cells eLife 3 2014 e01659
49. M.S. Sosa, P. Bragado, and J.A. Aguirre-Ghiso Mechanisms of disseminated cancer cell dormancy: An awakening field Nat. Rev. Cancer 14 2014 611 622
50. J.C. Sun, and L.L. Lanier Cutting edge: Viral infection breaks NK cell tolerance to "missing self" J. Immunol. 181 2008 7453 7457
51. K. Takeda, M.J. Smyth, E. Cretney, Y. Hayakawa, N. Yamaguchi, H. Yagita, and K. Okumura Involvement of tumor necrosis factor-related apoptosis-inducing ligand in NK cell-mediated and IFN-gamma-dependent suppression of subcutaneous tumor growth Cell. Immunol. 214 2001 194 200
52. B. Treutlein, D.G. Brownfield, A.R. Wu, N.F. Neff, G.L. Mantalas, F.H. Espinoza, T.J. Desai, M.A. Krasnow, and S.R. Quake Reconstructing lineage hierarchies of the distal lung epithelium using single-cell RNA-seq Nature 509 2014 371 375
53. M. Valiente, A.C. Obenauf, X. Jin, Q. Chen, X.H. Zhang, D.J. Lee, J.E. Chaft, M.G. Kris, J.T. Huse, E. Brogi, and J. Massagué Serpins promote cancer cell survival and vascular co-option in brain metastasis Cell 156 2014 1002 1016
54. M.D. Vesely, M.H. Kershaw, R.D. Schreiber, and M.J. Smyth Natural innate and adaptive immunity to cancer Annu. Rev. Immunol. 29 2011 235 271
55. F.R. Villegas, S. Coca, V.G. Villarrubia, R. Jiménez, M.J. Chillón, J. Jareño, M. Zuil, and L. Callol Prognostic significance of tumor infiltrating natural killer cells subset CD57 in patients with squamous cell lung cancer Lung Cancer 35 2002 23 28
56. M.M. Winslow, T.L. Dayton, R.G. Verhaak, C. Kim-Kiselak, E.L. Snyder, D.M. Feldser, D.D. Hubbard, M.J. DuPage, C.A. Whittaker, S. Hoersch, and et al. Suppression of lung adenocarcinoma progression by Nkx2-1 Nature 473 2011 101 104
57. J. Wu, and L.L. Lanier Natural killer cells and cancer Adv. Cancer Res. 90 2003 127 156
58. D. Xiao, J.C. Craig, J.R. Chapman, B. Dominguez-Gil, A. Tong, and G. Wong Donor cancer transmission in kidney transplantation: A systematic review Am. J. Transplant. 13 2013 2645 2652
59. X.H. Zhang, Q. Wang, W. Gerald, C.A. Hudis, L. Norton, M. Smid, J.A. Foekens, and J. Massagué Latent bone metastasis in breast cancer tied to Src-dependent survival signals Cancer Cell 16 2009 67 78