Genome-wide in vivo screen identifies novel host regulators of metastatic colonization

Nature

Volumn 541, Issue 7636, 2017, Pages 233-236

  Van Der Weyden, Louise ^a   Arends, Mark J ^b   Campbell, Andrew D ^c   Bald, Tobias ^d,e   Wardle Jones, Hannah ^a   Griggs, Nicola ^a   Velasco Herrera, Martin Del Castillo ^a   Tüting, Thomas ^d   Sansom, Owen J ^c   Karp, Natasha A ^a   Clare, Simon ^a   Gleeson, Diane ^a   Ryder, Edward ^a   Galli, Antonella ^a   Tuck, Elizabeth ^a   Cambridge, Emma L ^a   Voet, Thierry ^a,f   MacAulay, Iain C ^a   Wong, Kim ^a   Spiegel, Sarah ^g   Speak, Anneliese O ^a   Adams, David J ^a   more..

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c BEATSON INSTITUTE FOR CANCER RESEARCH   (United Kingdom)

^d UNIVERSITY HOSPITAL MAGDEBURG   (Germany)

^e QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^f UNIVERSITY OF LEUVEN   (Belgium)

^g VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABHD17A PROTEIN; CD4 ANTIGEN; CD69 ANTIGEN; CHEMOKINE RECEPTOR CXCR3; DPH6 PROTEIN; EPSTI1 PROTEIN; GLIPR2 PROTEIN; HERMES ANTIGEN; IMMUNOGLOBULIN HEAVY CHAIN; IMMUNOGLOBULIN HEAVY CHAIN 6; INTERFERON; INTERFERON REGULATORY FACTOR 1; INTERFERON REGULATORY FACTOR 7; INTERLEUKIN 2 RECEPTOR ALPHA; KLRG1 PROTEIN; L SELECTIN; MARCKSL1 PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PLA2G16 PROTEIN; PROTEIN; RANTES; RNF10 PROTEIN; SLC9A3R2 PROTEIN; SPHINGOSINE 1 PHOSPHATE TRANSPORTER SPINSTER HOMOLOGUE 2; UNCLASSIFIED DRUG; ANION TRANSPORT PROTEIN; LYSOPHOSPHOLIPID; SPHINGOSINE; SPHINGOSINE 1-PHOSPHATE; SPNS2 PROTEIN, MOUSE;

CANCER; CAUSE OF DEATH; CELLS AND CELL COMPONENTS; COLONIZATION; GENOME; HOST; IMMUNE SYSTEM; MUTATION; PHOSPHATE; TUMOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL; CD8+ T LYMPHOCYTE; CELL KILLING; CELL LYSATE; CELL MIGRATION; CONTROLLED STUDY; CYTOTOXICITY ASSAY; DOWN REGULATION; EFFECTOR CELL; ENDOTHELIUM CELL; EX VIVO STUDY; EXPERIMENTAL METASTASIS; FEMALE; GENE DELETION; GENE IDENTIFICATION; GENETIC SCREENING; GENOME-WIDE ASSOCIATION STUDY; IN VIVO STUDY; LUNG METASTASIS; LYMPHOCYTE; LYMPHOCYTOPENIA; MALE; MELANOCYTE; MEMORY T LYMPHOCYTE; MOUSE; MOUSE MUTANT; NATURAL KILLER T CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; RNA SEQUENCE; TUMOR MICROENVIRONMENT; UPREGULATION; WILD TYPE; ANALOGS AND DERIVATIVES; ANIMAL; CELL MOTION; CYTOLOGY; DEFICIENCY; DISEASE MODEL; GENETICS; GENOME; GENOMICS; IMMUNOLOGY; LUNG TUMOR; METABOLISM; METASTASIS; NATURAL KILLER CELL; PATHOLOGY; SECONDARY; T LYMPHOCYTE; TUMOR CELL LINE;

MUS;

ANIMALS; ANION TRANSPORT PROTEINS; CELL LINE, TUMOR; CELL MOVEMENT; DISEASE MODELS, ANIMAL; FEMALE; GENOME; GENOMICS; KILLER CELLS, NATURAL; LUNG NEOPLASMS; LYMPHOPENIA; LYSOPHOSPHOLIPIDS; MALE; MICE; NEOPLASM METASTASIS; SPHINGOSINE; T-LYMPHOCYTES; TUMOR MICROENVIRONMENT;

EID: 85012054927     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature20792     Document Type: Article

References (48)

1. Quail, D. F., Joyce, J. A. Microenvironmental regulation of tumor progression and metastasis. Nature Med. 19, 1423-1437 (2013).
2. Chambers, A. F., et al. Critical steps in hematogenous metastasis: an overview. Surg. Oncol. Clin. N. Am. 10, 243-255 (2001).
3. Blank, C., et al. PD-L1/B7H-1 inhibits the effector phase of tumor rejection by T cell receptor (TCR) transgenic CD8+ T cells. Cancer Res. 64, 1140-1145 (2004).
4. van Elsas, A., Hurwitz, A. A., Allison, J. P. Combination immunotherapy of B16 melanoma using anti-cytotoxic T lymphocyte-associated antigen 4 (CTLA-4) and granulocyte/macrophage colony-stimulating factor (GM-CSF)-producing vaccines induces rejection of subcutaneous and metastatic tumors accompanied by autoimmune depigmentation. J. Exp. Med. 190, 355-366 (1999).
5. White, J. K., et al. Genome-wide generation and systematic phenotyping of knockout mice reveals new roles for many genes. Cell 154, 452-464 (2013).
6. Ogasawara, K., et al. Requirement for IRF-1 in the microenvironment supporting development of natural killer cells. Nature 391, 700-703 (1998).
7. Honda, K., et al. IRF-7 is the master regulator of type-I interferon-dependent immune responses. Nature 434, 772-777 (2005).
8. Purtha, W. E., Swiecki, M., Colonna, M., Diamond, M. S., Bhattacharya, D. Spontaneous mutation of the Dock2 gene in Irf5/mice complicates interpretation of type I interferon production and antibody responses. Proc. Natl Acad. Sci. USA 109, E898-E904 (2012).
9. Sasaki, T., et al. Function of PI3K in thymocyte development, T cell activation, neutrophil migration. Science 287, 1040-1046 (2000).
10. Tassi, I., et al. p110 and p110 phosphoinositide 3-kinase signaling pathways synergize to control development and functions of murine NK cells. Immunity 27, 214-227 (2007).
11. Kitamura, D., Roes, J., Kühn, R., Rajewsky, K. A B cell-deficient mouse by targeted disruption of the membrane exon of the immunoglobulin chain gene. Nature 350, 423-426 (1991).
12. Sun, X., et al. CD39/ENTPD1 expression by CD4+Foxp3+ regulatory T cells promotes hepatic metastatic tumor growth in mice. Gastroenterology 139, 1030-1040 (2010).
13. Guerrero, J. A., et al. Gray platelet syndrome: proinflammatory megakaryocytes and-granule loss cause myelofibrosis and confer metastasis resistance in mice. Blood 124, 3624-3635 (2014).
14. Okada, F., et al. The role of nicotinamide adenine dinucleotide phosphate oxidase-derived reactive oxygen species in the acquisition of metastatic ability of tumor cells. Am. J. Pathol. 169, 294-302 (2006).
15. Kang, B. H., et al. Targeted inhibition of mitochondrial Hsp90 suppresses localised and metastatic prostate cancer growth in a genetic mouse model of disease. Br. J. Cancer 104, 629-634 (2011).
16. Takabe, K., Spiegel, S. Export of sphingosine-1-phosphate and cancer progression. J. Lipid Res. 55, 1839-1846 (2014).
17. Fukuhara, S., et al. The sphingosine-1-phosphate transporter Spns2 expressed on endothelial cells regulates lymphocyte trafficking in mice. J. Clin. Invest. 122, 1416-1426 (2012).
18. Mendoza, A., et al. The transporter Spns2 is required for secretion of lymph but not plasma sphingosine-1-phosphate. Cell Reports 2, 1104-1110 (2012).
19. Nagahashi, M., et al. Spns2, a transporter of phosphorylated sphingoid bases, regulates their blood and lymph levels, the lymphatic network. FASEB J. 27, 1001-1011 (2013).
20. Wilkerson, B. A., Argraves, K. M. The role of sphingosine-1-phosphate in endothelial barrier function. Biochim. Biophys. Acta 1841, 1403-1412 (2014).
21. Chiang, E. Y., Henson, M., Stroynowski, I. Correction of defects responsible for impaired Qa-2 class Ib MHC expression on melanoma cells protects mice from tumor growth. J. Immunol. 170, 4515-4523 (2003).
22. Schwab, S. R., et al. Lymphocyte sequestration through S1P lyase inhibition and disruption of S1P gradients. Science 309, 1735-1739 (2005).
23. Nijnik, A., et al. The role of sphingosine-1-phosphate transporter Spns2 in immune system function. J. Immunol. 189, 102-111 (2012).
24. Garris, C. S., Blaho, V. A., Hla, T., Han, M. H. Sphingosine-1-phosphate receptor 1 signalling in T cells: trafficking and beyond. Immunology 142, 347-353 (2014).
25. Walzer, T., et al. Natural killer cell trafficking in vivo requires a dedicated sphingosine 1-phosphate receptor. Nature Immunol. 8, 1337-1344 (2007).
26. Cuff, S., Dolton, G., Matthews, R. J., Gallimore, A. Antigen specificity determines the pro-or antitumoral nature of CD8+ T cells. J. Immunol. 184, 607-614 (2010).
27. Ponnusamy, S., et al. Communication between host organism and cancer cells is transduced by systemic sphingosine kinase 1/sphingosine 1-phosphate signalling to regulate tumour metastasis. EMBO Mol. Med. 4, 761-775 (2012).
28. Visentin, B., et al. Validation of an anti-sphingosine-1-phosphate antibody as a potential therapeutic in reducing growth, invasion, angiogenesis in multiple tumor lineages. Cancer Cell 9, 225-238 (2006).
29. Liu, G., Yang, K., Burns, S., Shrestha, S., Chi, H. The S1P(1)-mTOR axis directs the reciprocal differentiation of T(H)1 and T(reg) cells. Nature Immunol. 11, 1047-1056 (2010).
30. Liu, Y., et al. The sphingosine-1-phosphate receptor agonist FTY720 and its phosphorylated form affect the function of CD4+CD25+ T cells in vitro. Int. J. Mol. Med. 30, 211-219 (2012).
31. Pham, T. H., et al. Lymphatic endothelial cell sphingosine kinase activity is required for lymphocyte egress and lymphatic patterning. J. Exp. Med. 207, 17-27 (2010).
32. Shinkai, Y., et al. RAG-2-deficient mice lack mature lymphocytes owing to inability to initiate V(D)J rearrangement. Cell 68, 855-867 (1992).
33. Kranz, A., et al. An improved Flp deleter mouse in C57Bl/6 based on Flpo recombinase. Genesis 48, 512-520 (2010).
34. Karp, N. A., et al. Impact of temporal variation on design and analysis of mouse knockout phenotyping studies. PLoS ONE 9, e111239 (2014).
35. Kilkenny, C., Browne, W. J., Cuthill, I. C., Emerson, M., Altman, D. G. Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol. 8, e1000412 (2010).
36. Borsig, L., Wong, R., Hynes, R. O., Varki, N. M., Varki, A. Synergistic effects of L-and P-selectin in facilitating tumor metastasis can involve non-mucin ligands and implicate leukocytes as enhancers of metastasis. Proc. Natl Acad. Sci. USA 99, 2193-2198 (2002).
37. Johnstone, C. N., et al. Functional and molecular characterisation of EO771. LMB tumours, a new C57BL/6-mouse-derived model of spontaneously metastatic mammary cancer. Dis. Model. Mech. 8, 237-251 (2015).
38. Bald, T., et al. Ultraviolet-radiation-induced inflammation promotes angiotropism and metastasis in melanoma. Nature 507, 109-113 (2014).
39. Lindsay, C. R., et al. P-Rex1 is required for efficient melanoblast migration and melanoma metastasis. Nature Commun. 2, 555 (2011).
40. Picelli, S., et al. Smart-seq2 for sensitive full-length transcriptome profiling in single cells. Nature Methods 10, 1096-1098 (2013).
41. Picelli, S., et al. Full-length RNA-seq from single cells using Smart-seq2. Nature Protocols 9, 171-181 (2014).
42. Dobin, A., et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15-21 (2013).
43. Anders, S., Pyl, P. T., Huber, W. HTSeq-a Python framework to work with high-throughput sequencing data. Bioinformatics 31, 166-169 (2015).
44. Gentleman, R. C., et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5, R80 (2004).
45. Love, M. I., Huber, W., Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
46. Hait, N. C., et al. Regulation of histone acetylation in the nucleus by sphingosine-1-phosphate. Science 325, 1254-1257 (2009).
47. Curran, P. J., Hussong, A. M. Integrative data analysis: the simultaneous analysis of multiple data sets. Psychol. Methods 14, 81-100 (2009).
48. Hochberg, Y. A sharper Bonferroni procedure for multiple tests of significance. Biometrika 75, 800-802 (1988).