Comprehensive functional characterization of cancer-testis antigens defines obligate participation in multiple hallmarks of cancer

Nature Communications

Volumn 6, Issue , 2015, Pages

  Maxfield, Kimberly E ^a   Taus, Patrick J ^a,b   Corcoran, Kathleen ^c   Wooten, Joshua ^b   MacIon, Jennifer ^a   Zhou, Yunyun ^d   Borromeo, Mark ^e   Kollipara, Rahul K ^d   Yan, Jingsheng ^a   Xie, Yang ^a,d   Xie, Xian Jin ^a,d   Whitehurst, Angelique W ^a  

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

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

^c UNIVERSITY OF NORTH CAROLINA   (United States)

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

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

Author keywords

[No Author keywords available]

Indexed keywords

BH3 PROTEIN; BIM PROTEIN; CALRETICULIN; CALRETICULIN 3; CANCER TESTIS ANTIGEN; CASPASE 3; CASPASE 7; CHONDROSARCOMA ASSOCIATED GENE 1 PROTEIN; CHONDROSARCOMA ASSOCIATED GENE 3 PROTEIN; COILED COIL DOMAIN CONTAINING 110 PROTEIN; CUTANEOUS T CELL LYMPHOMA ASSOCIATED ANTIGEN 1; CYTOCHROME C OXIDASE; CYTOCHROME C OXIDASE SUBUNIT 6B2; FETAL AND ADULT TESTIS EXPRESSED 1 ANTIGEN; HYPOXIA INDUCIBLE FACTOR; IMMUNOGLOBULIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOGLOBULIN SUPERFAMILY MEMBER 11; INSULIN LIKE GROWTH FACTOR 2 MRNA BINDING PROTEIN 3; LACTATE DEHYDROGENASE C; LUCIFERASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; P ANTIGEN FAMILY MEMBER 4; PROTEIN; SMALL INTERFERING RNA; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; WNT PROTEIN; X ANTIGEN FAMILY MEMBER 1B; ZINC FINGER PROTEIN; ZINC FINGER PROTEIN 165; APOPTOSIS REGULATORY PROTEIN; BIK PROTEIN, HUMAN; DNA BINDING PROTEIN; FATE1 PROTEIN, HUMAN; MEMBRANE PROTEIN; PMEPA1 PROTEIN, HUMAN; SMAD7 PROTEIN; SMAD7 PROTEIN, HUMAN; SMURF2 PROTEIN, HUMAN; TRANSCRIPTION FACTOR; TUMOR ANTIGEN; UBIQUITIN PROTEIN LIGASE; ZNF165 PROTEIN, HUMAN;

ANTIGEN; CANCER; CELLS AND CELL COMPONENTS; GENE EXPRESSION; GENOMICS; IMMUNE SYSTEM; PROTEIN; PROTEOMICS; TOXIC SUBSTANCE; TUMOR;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN DETECTION; ANTIGEN FUNCTION; APOPTOSIS; ARTICLE; BINDING SITE; BONE CANCER; BREAST CANCER CELL LINE; BREAST CARCINOGENESIS; CANCER CELL; CANCER GROWTH; CANCER SURVIVAL; CELL DIVISION; CELL GROWTH; CELL PROLIFERATION; CELL STIMULATION; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; ENZYME REGULATION; FEMALE; FETUS; FUNCTIONAL GENOMICS; GENE EXPRESSION; GENE OVEREXPRESSION; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; LUNG CANCER CELL LINE; MALE; METABOLIC REGULATION; METASTASIS; MOUSE; NEGATIVE FEEDBACK; NONHUMAN; OVARIAN CANCER CELL LINE; OVERALL SURVIVAL; OXIDATIVE PHOSPHORYLATION; PHENOTYPE; PROSTATE CANCER CELL LINE; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN STABILITY; PROTEOMICS; SIGNAL TRANSDUCTION; SKIN CANCER; SPERMATOZOON MIGRATION; SURVIVAL FACTOR; TRANSIENT TRANSFECTION; TRIPLE NEGATIVE BREAST CANCER; TUMOR MICROENVIRONMENT; UNINDEXED SEQUENCE; ADENOCARCINOMA; ANIMAL; CANCER TRANSPLANTATION; CARCINOGENESIS; CELL LINE; COLORECTAL TUMOR; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; GENETICS; HCT 116 CELL LINE; HEK293 CELL LINE; IMMUNOBLOTTING; IMMUNOLOGY; LUNG TUMOR; MORTALITY; NEOPLASM; NONOBESE DIABETIC MOUSE; PROGNOSIS; PROPORTIONAL HAZARDS MODEL; REAL TIME POLYMERASE CHAIN REACTION; TUMOR CELL LINE; WNT SIGNALING PATHWAY;

ADENOCARCINOMA; ANIMALS; ANTIGENS, NEOPLASM; APOPTOSIS REGULATORY PROTEINS; CARCINOGENESIS; CELL LINE; CELL LINE, TUMOR; CELL SURVIVAL; COLORECTAL NEOPLASMS; DNA-BINDING PROTEINS; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION, NEOPLASTIC; HCT116 CELLS; HEK293 CELLS; HUMANS; IMMUNOBLOTTING; IN VITRO TECHNIQUES; LUNG NEOPLASMS; MEMBRANE PROTEINS; MICE, INBRED NOD; NEOPLASM TRANSPLANTATION; NEOPLASMS; PROGNOSIS; PROPORTIONAL HAZARDS MODELS; REAL-TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SMAD7 PROTEIN; TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA; TRIPLE NEGATIVE BREAST NEOPLASMS; UBIQUITIN-PROTEIN LIGASES; WNT SIGNALING PATHWAY;

EID: 84947294079     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms9840     Document Type: Article

References (67)

1. Almeida, L. G. et al. CTdatabase: a knowledge-base of high-throughput and curated data on cancer-testis antigens. Nucleic Acids Res. 37, D816-D819 (2009).
2. Zhao, S., Zhu, W., Xue, S. & Han, D. Testicular defense systems: immune privilege and innate immunity. Cell. Mol. Immunol. 11, 428-437 (2014).
3. Old, L. J. Cancer/testis (CT) antigens - a new link between gametogenesis and cancer. Cancer Immun. 1, 1 (2001).
4. Simpson, A. J., Caballero, O. L., Jungbluth, A., Chen, Y. T. & Old, L. J. Cancer/testis antigens, gametogenesis and cancer. Nat. Rev. Cancer 5, 615-625 (2005).
5. Robbins, P. F. et al. Tumour regression in patients with metastatic synovial cell sarcoma and melanoma using genetically engineered lymphocytes reactive with NY-ESO-1. J. Clin. Oncol. 29, 917-924 (2011).
6. Dhodapkar, M. V. et al. Induction of antigen-specific immunity with a vaccine targeting NY-ESO-1 to the dendritic cell receptor DEC-205. Sci. Transl. Med. 6, 232ra51 (2014).
7. Whitehurst, A. W. Cause and consequence of cancer/testis antigen activation in cancer. Annu. Rev. Pharmacol. Toxicol. 54, 251-272 (2014).
8. Epping, M. T. et al. The human tumour antigen PRAME is a dominant repressor of retinoic acid receptor signalling. Cell 122, 835-847 (2005).
9. Whitehurst, A. W. et al. Synthetic lethal screen identification of chemosensitizer loci in cancer cells. Nature 446, 815-819 (2007).
10. Cappell, K. M. et al. Multiple cancer testes antigens function to support tumour cell mitotic fidelity. Mol. Cell. Biol. 32, 4131-4140 (2012).
11. Doyle, J. M., Gao, J., Wang, J., Yang, M. & Potts, P. R. MAGE-RING protein complexes comprise a family of E3 ubiquitin ligases. Mol. Cell 39, 963-974 (2010).
12. Huttemann, M., Jaradat, S. & Grossman, L. I. Cytochrome c oxidase of mammals contains a testes-specific isoform of subunit VIb - the counterpart to testes-specific cytochrome c? Mol. Reprod. Dev. 66, 8-16 (2003).
13. Ikawa, M. et al. Calsperin is a testis-specific chaperone required for sperm fertility. J. Biol. Chem. 286, 5639-5646 (2011).
14. Ruzzenenti, P. et al. The Ferritin-Heavy-Polypeptide-Like-17 (FTHL17) gene encodes a ferritin with low stability and no ferroxidase activity and with a partial nuclear localization. Biochim. Biophys. Acta 1850, 1267-1273 (2015).
15. Suzuki-Toyota, F. et al. Factors maintaining normal sperm tail structure during epididymal maturation studied in Gopc -/- mice. Biol. Reprod. 77, 71-82 (2007).
16. Gandre-Babbe, S. & van der Bliek, A. M. The novel tail-anchored membrane protein Mff controls mitochondrial and peroxisomal fission in mammalian cells. Mol. Biol. Cell 19, 2402-2412 (2008).
17. Yu, H. et al. Next-generation sequencing to generate interactome datasets. Nat. Methods 8, 478-480 (2011).
18. Rual, J. F. et al. Towards a proteome-scale map of the human protein-protein interaction network. Nature 437, 1173-1178 (2005).
19. Boyd, J. M. et al. Bik, a novel death-inducing protein shares a distinct sequence motif with Bcl-2 family proteins and interacts with viral and cellular survival-promoting proteins. Oncogene 11, 1921-1928 (1995).
20. Germain, M., Mathai, J. P. & Shore, G. C. BH-3-only BIK functions at the endoplasmic reticulum to stimulate cytochrome c release from mitochondria. J. Biol. Chem. 277, 18053-18060 (2002).
21. Chinnadurai, G., Vijayalingam, S. & Rashmi, R. BIK, the founding member of the BH3-only family proteins: mechanisms of cell death and role in cancer and pathogenic processes. Oncogene 27, S20-S29 (2008).
22. García, N. et al. A molecular analysis by gene expression profiling reveals Bik/NBK overexpression in sporadic breast tumour samples of Mexican females. BMC Cancer 5, 93 (2005).
23. Zhu, H. et al. Bik/NBK accumulation correlates with apoptosis-induction by bortezomib (PS-341, Velcade) and other proteasome inhibitors. Oncogene 24, 4993-4999 (2005).
24. Li, W. et al. Role of IGF2BP3 in trophoblast cell invasion and migration. Cell Death Dis. 5, e1025 (2014).
25. Dong, X. Y., Yang, X. A., Wang, Y. D. & Chen, W. F. Zinc-finger protein ZNF165 is a novel cancer-testis antigen capable of eliciting antibody response in hepatocellular carcinoma patients. Br. J. Cancer 91, 1566-1570 (2004).
26. Tirosvoutis, K. N., Divane, A., Jones, M. & Affara, N. A. Characterization of a novel zinc finger gene (ZNF165) mapping to 6p21 that is expressed specifically in testis. Genomics 28, 485-490 (1995).
27. Lee, P. L. et al. Three genes encoding zinc finger proteins on human chromosome 6p21.3: members of a new subclass of the Kruppel gene family containing the conserved SCAN box domain. Genomics 43, 191-201 (1997).
28. Williams, A. J., Blacklow, S. C. & Collins, T. The zinc finger-associated SCAN box is a conserved oligomerization domain. Mol. Cell. Biol. 19, 8526-8535 (1999).
29. Lin, X., Liang, M. & Feng, X. H. Smurf2 is a ubiquitin E3 ligase mediating proteasome-dependent degradation of Smad2 in transforming growth factor-beta signalling. J. Biol. Chem. 275, 36818-36822 (2000).
30. Fournier, P. G. et al. The TGF-beta signalling regulator PMEPA1 suppresses prostate cancer metastases to bone. Cancer Cell 27, 809-821 (2015).
31. Watanabe, Y. et al. TMEPAI, a transmembrane TGF-beta-inducible protein, sequesters Smad proteins from active participation in TGF-beta signalling. Mol. Cell 37, 123-134 (2010).
32. Kavsak, P. et al. Smad7 binds to Smurf2 to form an E3 ubiquitin ligase that targets the TGF beta receptor for degradation. Mol. Cell 6, 1365-1375 (2000).
33. Zhang, Y., Chang, C., Gehling, D. J., Hemmati-Brivanlou, A. & Derynck, R. Regulation of Smad degradation and activity by Smurf2, an E3 ubiquitin ligase. Proc. Natl Acad. Sci. USA 98, 974-979 (2001).
34. Anderson, K. D. et al. Angiogenic sprouting into neural tissue requires Gpr124, an orphan G protein-coupled receptor. Proc. Natl Acad. Sci. USA 108, 2807-2812 (2011).
35. Hayashi, A., Hiatari, R., Tsuji, T., Ohashi, K. & Mizuno, K. p63RhoGEF-mediated formation of a single polarized lamellipodium is required for chemotactic migration in breast carcinoma cells. FEBS Lett. 587, 698-705 (2013).
36. Xu, L., Corcoran, R. B., Welsh, J. W., Pennica, D. & Levine, A. J. WISP-1 is a Wnt-1- and beta-catenin-responsive oncogene. Genes Dev. 14, 585-595 (2000).
37. Kawahara, T. et al. Quantitative proteomic profiling identifies DPYSL3 as pancreatic ductal adenocarcinoma-associated molecule that regulates cell adhesion and migration by stabilization of focal adhesion complex. PloS ONE 8, e79654 (2013).
38. Benassi, B. et al. MYC is activated by USP2a-mediated modulation of microRNAs in prostate cancer. Cancer Discov. 2, 236-247 (2012).
39. Chen, Z. et al. Discovery of structure-based small molecular inhibitor of alphaB-crystallin against basal-like/triple-negative breast cancer development in vitro and in vivo. Breast. Cancer Res. Treat. 145, 45-59 (2014).
40. Hartzell, C. et al. Dysregulated RasGRP1 responds to cytokine receptor input in T cell leukemogenesis. Sci. Signal. 6, ra21 (2013).
41. Luke, C. T., Oki-Idouchi, C. E., Cline, J. M. & Lorenzo, P. S. RasGRP1 overexpression in the epidermis of transgenic mice contributes to tumour progression during multistage skin carcinogenesis. Cancer Res. 67, 10190-10197 (2007).
42. Su, F., Overholtzer, M., Besser, D. & Levine, A. J. WISP-1 attenuates p53-mediated apoptosis in response to DNA damage through activation of the Akt kinase. Genes Dev. 16, 46-57 (2002).
43. Xie, D., Nakachi, K., Wang, H., Elashoff, R. & Koeffler, H. P. Elevated levels of connective tissue growth factor, WISP-1, and CYR61 in primary breast cancers associated with more advanced features. Cancer Res. 61, 8917-8923 (2001).
44. Bieche, I. et al. Prognostic value of chorionic gonadotropin beta gene transcripts in human breast carcinoma. Clin. Cancer Res. 4, 671-676 (1998).
45. Torres, E. M. et al. Effects of aneuploidy on cellular physiology and cell division in haploid yeast. Science 317, 916-924 (2007).
46. Szatrowski, T. P. & Nathan, C. F. Production of large amounts of hydrogen peroxide by human tumour cells. Cancer Res. 51, 794-798 (1991).
47. Abrams, J. M. & White, M. A. Coordination of cell death and the cell cycle: linking proliferation to death through private and communal couplers. Curr. Opin. Cell. Biol. 16, 634-638 (2004).
48. Principe, D. R. et al. TGF-β: duality of function between tumour prevention and carcinogenesis. J. Natl. Cancer Inst. 106, djt369 (2014).
49. Korch, C. et al. DNA profiling analysis of endometrial and ovarian cell lines reveals misidentification, redundancy and contamination. Gynecol. Oncol. 127, 241-248 (2012).
50. Biechele, T. L. & Moon, R. T. Assaying beta-catenin/TCF transcription with beta-catenin/TCF transcription-based reporter constructs. Methods Mol. Biol. 468, 99-110 (2008).
51. Kietzmann, T., Cornesse, Y., Brechtel, K., Modaressi, S. & Jungermann, K. Perivenous expression of the mRNA of the three hypoxia-inducible factor alpha-subunits, HIF1alpha, HIF2alpha and HIF3alpha, in rat liver. Biochem. J. 354, 531-537 (2001).
52. Ferguson, S. S. & Caron, M. G. Green fluorescent protein-tagged beta-arrestin translocation as a measure of G protein-coupled receptor activation. Methods Mol. Biol. 237, 121-126 (2004).
53. Schmittgen, T. D. & Livak, K. J. Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 3, 1101-1108 (2008).
54. McLean, C. Y. et al. GREAT improves functional interpretation of cis-regulatory regions. Nat. Biotechnol. 28, 495-501 (2010).
55. Cerami, E. G., Bader, G. D., Gross, B. E. & Sander, C. cPath: open source software for collecting, storing, and querying biological pathways. BMC bioinformatics 7, 497 (2006).
56. Heinz, S. et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 38, 576-589 (2010).
57. Pei, H. et al. FKBP51 affects cancer cell response to chemotherapy by negatively regulating Akt. Cancer Cell 16, 259-266 (2009).
58. Stearman, R. S. et al. Analysis of orthologous gene expression between human pulmonary adenocarcinoma and a carcinogen-induced murine model. Am. J. Pathol. 167, 1763-1775 (2005).
59. Cancer Genome Atlas N. Comprehensive molecular portraits of human breast tumours. Nature 490, 61-70 (2012).
60. Cancer Genome Atlas N. Comprehensive molecular characterization of human colon and rectal cancer. Nature 487, 330-337 (2012).
61. Wurmbach, E. et al. Genome-wide molecular profiles of HCV-induced dysplasia and hepatocellular carcinoma. Hepatology 45, 938-947 (2007).
62. Yoshihara, K. et al. Gene expression profiling of advanced-stage serous ovarian cancers distinguishes novel subclasses and implicates ZEB2 in tumour progression and prognosis. Cancer Sci. 100, 1421-1428 (2009).
63. Biewenga, P. et al. Gene expression in early stage cervical cancer. Gynecol. Oncol. 108, 520-526 (2008).
64. Sorlie, T. et al. Gene expression patterns of breast carcinomas distinguish tumour subclasses with clinical implications. Proc. Natl Acad. Sci. USA 98, 10869-10874 (2001).
65. Cancer Genome Atlas Research N. Comprehensive molecular profiling of lung adenocarcinoma. Nature 511, 543-550 (2014).
66. Lee, E. S. et al. Prediction of recurrence-free survival in postoperative non-small cell lung cancer patients by using an integrated model of clinical information and gene expression. Clin. Cancer Res. 14, 7397-7404 (2008).
67. Fraley, C. R. & A.E. Model-based clustering, discriminant analysis, and density estimation. J. Am. Stat. Assoc. 97, 611-638 (2002).