Genome-wide multi-omics profiling of colorectal cancer identifies immune determinants strongly associated with relapse

Frontiers in Genetics

Volumn 4, Issue NOV, 2013, Pages

  Madhavan, Subha ^a,b   Gusev, Yuriy ^a,b   Natarajan, Thanemozhi G ^a   Song, Lei ^a,b   Bhuvaneshwar, Krithika ^a,b   Gauba, Robinder ^a,b   Pandey, Abhishek ^a   Haddad, Bassem R ^b   Goerlitz, David ^b   Cheema, Amrita K ^b   Juhl, Hartmut ^c   Kallakury, Bhaskar ^b   Marshall, John L ^b   Byers, Stephen W ^b   Weiner, Louis M ^b  

^a GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

^b GEORGETOWN UNIVERSITY   (United States)

^c Indivumed GmbH   (Germany)

Author keywords

Colorectal cancer; Exome sequencing; Immune response; Integrative analysis; Multi omics; Relapse; Systems biology; Variant analysis

Indexed keywords

EID: 84890262479     PISSN: None     EISSN: 16648021     Source Type: Journal    
DOI: 10.3389/fgene.2013.00236     Document Type: Article

References (71)

1. ACS. (2013). Cancer Facts and Figures 2013. Atlanta, GA: American Cancer Society.
2. Arlot, S., and Celisse, A. (2010). A survey of cross-validation procedures for model selection. Statist Surv. 4, 40-79. doi: 10.1214/09-SS054.
3. Benson, A. B. 3rd, (2006). New approaches to the adjuvant therapy of colon cancer. Oncologist 11, 973-980. doi: 10.1634/theoncologist.11-9-973.
4. Berencsi, K., Meropol, N. J., Hoffman, J. P., Sigurdson, E., Giles, L., Rani, P., et al. (2007). Colon carcinoma cells induce CXCL11-dependent migration of CXCR3-expressing cytotoxic T lymphocytes in organotypic culture. Cancer Immunol. Immunother. 56, 359-370. doi: 10.1007/s00262-006-0190-2.
5. Bolstad, B. M., Irizarry, R. A., Astrand, M., and Speed, T. P. (2003) A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19, 185-193. doi: 10.1093/bioinformatics/19.2.185.
6. Brosens, R. P., Belt, E. J., Haan, J. C., Buffart, T. E., Carvalho, B., Grabsch, H., et al. (2010). Deletion of chromosome 4q predicts outcome in stage II colon cancer patients. Anal Cell Pathol (Amst.) 33, 95-104. doi: 10.1038/nature11252.
7. Brosens, R. P., Belt, E. J., Haan, J. C., Buffart, T. E., Carvalho, B., Grabsch, H., et al. (2011). Deletion of chromosome 4q predicts outcome in stage II colon cancer patients. Cell Oncol (Dordr) 34, 215-223. doi: 10.1007/s13402-011-0042-8.
8. Carlsen, H. S., Baekkevold, E. S., Johansen, F. E., Haraldsen, G., and Brandtzaeg, P. (2002). B cell attracting chemokine 1 (CXCL13) and its receptor CXCR5 are expressed in normal and aberrant gut associated lymphoid tissue. Gut 51, 364-371. doi: 10.1136/gut.51.3.364.
9. Chau, I., and Cunningham, D. (2006). Adjuvant therapy in colon cancer-what, when and how? Ann. Oncol. 17, 1347-1359. doi: 10.1093/annonc/mdl029.
10. Chew, A., Salama, P., Robbshaw, A., Klopcic, B., Zeps, N., Platell, C., et al. (2011). SPARC, FOXP3, CD8 and CD45 correlation with disease recurrence and long-term disease-free survival in colorectal cancer. PLoS ONE 6:e22047. doi: 10.1371/journal.pone.0022047.
11. de Maat, M. F., van de Velde, C. J., van der Werff, M. P., Putter, H., Umetani, N., Klein-Kranenbarg, E. M., et al. (2008). Quantitative analysis of methylation of genomic loci in early-stage rectal cancer predicts distant recurrence. J. Clin. Oncol. 26, 2327-2335. doi: 10.1200/JCO.2007.14.0723.
12. de Souza, A. P., and Bonorino, C. (2012). The immune system: endogenous anticancer mechanism. Front Biosci (Elite Ed.) 4, 2354-2364. doi: 10.2741/E547.
13. Deschoolmeester, V., Baay, M., Van Marck, E., Weyler, J., Vermeulen, P., Lardon, F., et al. (2010). Tumor infiltrating lymphocytes: an intriguing player in the survival of colorectal cancer patients. BMC Immunol. 11:19 doi: 10.1186/1471-2172-11-19.
14. Ding, J., Huang, S., Wu, S., Zhao, Y., Liang, L., Yan, M., et al. (2010). Gain of miR-151 on chromosome 8q24.3 facilitates tumour cell migration and spreading through downregulating RhoGDIA. Nat. Cell Biol. 12, 390-399. doi: 10.1038/ncb2039.
15. Fearon, E. R. (2011). Molecular genetics of colorectal cancer. Annu. Rev. Pathol. 6, 479-507. doi: 10.1146/annurev-pathol-011110-130235.
16. Feng, Y., Yu, G., Wang, T.-L., Shih, L.-M., and Wang, Y. (2010). Analysing DNA copy number changes using Fused Margin Regression. Int. J. Funct. Informatics Pers. Med. 3, 3-15. doi: 10.1504/IJFIPM.2010.033242.
17. Figueredo, A., Coombes, M. E., and Mukherjee, S. (2008). Adjuvant therapy for completely resected stage II colon cancer. Cochrane Database Syst. Rev. 3:CD005390. doi: 10.1002/14651858.CD005390.pub2.
18. Gadaleta, R. M., van Mil, S. W., Oldenburg, B., Siersema, P. D., Klomp, L. W., and van Erpecum, K. J. (2010). Bile acids and their nuclear receptor FXR: Relevance for hepatobiliary and gastrointestinal disease. Biochim. Biophys. Acta 1801, 683-692. doi: 10.1016/j.bbalip.2010.04.006.
19. Galon, J., Costes, A., Sanchez-Cabo, F., Kirilovsky, A., Mlecnik, B., Lagorce-Pages, C., et al. (2006). Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 313, 1960-1964. doi: 10.1126/science.1129139.
20. Ganti, S., Taylor, S. L., Kim, K., Hoppel, C. L., Guo, L., Yang, J., et al. (2012). Urinary acylcarnitines are altered in human kidney cancer. Int. J. Cancer 130, 2791-2800. doi: 10.1002/ijc.26274.
21. Ge, H., Walhout, A. J., and Vidal, M. (2003). Integrating 'omic' information: a bridge between genomics and systems biology. Trends Genet. 19, 551-560. doi: 10.1016/j.tig.2003.08.009.
22. Gentleman, R. C., Carey, V. J., Bates, D. M., Bolstad, B., Dettling, M., Dudoit, S., et al. (2004). Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5:R80. doi: 10.1186/gb-2004-5-10-r80.
23. Giskeodegard, G. F., Grinde, M. T., Sitter, B., Axelson, D. E., Lundgren, S., Fjosne, H. E., et al. (2010). Multivariate modeling and prediction of breast cancer prognostic factors using MR metabolomics. J. Proteome Res. 9, 972-979. doi: 10.1021/pr9008783.
24. Grivennikov, S. I., Greten, F. R., and Karin, M. (2010). Immunity, inflammation, and cancer. Cell 140, 883-899. doi: 10.1016/j.cell.2010.01.025.
25. Guyon, I., Weston, J., Barnhill, S., and Vapnik, V. (2002). Gene selection for cancer classification using support vector machines. Machine Learning 46, 389-422. doi: 10.1023/A:1012487302797.
26. Holcombe, R. F., Jacobson, J., Dakhil, S. R., Stewart, R. M., Betzing, K. S., Kannan, K., et al. (1999). Association of immune parameters with clinical outcome in stage III colon cancer: results of southwest oncology group protocol 9009. Cancer Immunol. Immunother. 48, 533-539. doi: 10.1007/s002620050602.
27. Irizarry, R. A., Bolstad, B. M., Collin, F., Cope, L. M., Hobbs, B., and Speed, T. P. (2003). Summaries of affymetrix GeneChip probe level data. Nucleic Acids Res. 31, e15. doi: 10.1093/nar/gng015.
28. Janssens, S., and Beyaert, R. (2003). Functional diversity and regulation of different interleukin-1 receptor-associated kinase (IRAK) family members. Mol. Cell 11, 293-302. doi: 10.1016/S1097-2765(03)00053-4.
29. Jansson, J., Willing, B., Lucio, M., Fekete, A., Dicksved, J., Halfvarson, J., et al. (2009). Metabolomics reveals metabolic biomarkers of Crohn's disease. PLoS ONE 4:e6386. doi: 10.1371/journal.pone.0006386.
30. Joyce, A. R., and Palsson, B. O. (2006). The model organism as a system: integrating 'omics' data sets. Nat. Rev. Mol. Cell Biol. 7, 198-210. doi: 10.1038/nrm1857.
31. Kawano, A., Ishikawa, H., Kamano, T., Kanoh, M., Sakamoto, K., Nakamura, T., et al. (2010). Significance of fecal deoxycholic acid concentration for colorectal tumor enlargement. Asian Pac. J. Cancer Prev. 11, 1541-1546.
32. Kim, S. Y., Lee, Y. H., and Bae, Y. S. (2012). MiR-186, miR-216b, miR-337-333p, and miR-760 cooperatively induce cellular senescence by targeting alpha subunit of protein kinase CKII in human colorectal cancer cells. Biochem. Biophys. Res. Commun. 429, 173-179. doi: 10.1016/j.bbrc.2012.10.117.
33. Kodeda, K., Asting, A. G., Lonnroth, C., Derwinger, K., Wettergren, Y., Nordgren, S., et al. (2012). Genomic CGH-assessed structural DNA alterations in rectal carcinoma as related to local recurrence following primary operation for cure. Int. J. Oncol. 41, 1397-1404. doi: 10.3892/ijo.2012.1562.
34. Kozomara, A., and Griffiths-Jones, S. (2011) miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res. 39, D152-D157 doi: 10.1093/nar/gkq1027.
35. Kreso, A., O'Brien, C. A., van Galen, P., Gan, O. I., Notta, F., Brown, A. M., et al. (2013). Variable clonal repopulation dynamics influence chemotherapy response in colorectal cancer. Science 339, 543-548. doi: 10.1126/science.1227670.
36. Kuo, K. T., Guan, B., Feng, Y., Mao, T. L., Chen, X., Jinawath, N., et al. (2009). Analysis of DNA copy number alterations in ovarian serous tumors identifies new molecular genetic changes in low-grade and high-grade carcinomas. Cancer Res. 69, 4036-4042. doi: 10.1158/0008-5472.CAN-08-3913.
37. Lagana, A., Forte, S., Giudice, A., Arena, M. R., Puglisi, P. L., Giugno, R., et al. (2009). miRo: a miRNA knowledge base. Database (Oxford) 2009, bap008. doi: 10.1093/database/bap008.
38. Lavery, I. C., and De Campos-Lobato, L. F. (2010). How to evaluate risk and identify stage II patients requiring referral to a medical oncologist: a surgeon's perspective. Oncology (Williston Park) 24, 14-16. Available online at: http://www.cancernetwork.com/supplements-2010-colon-cancer/how-evaluate-risk-and-identify-stage-ii-patients-requiring-referral-medical-oncologist.
39. Li, B., and Leal, S. M. (2008) Methods for detecting associations with rare variants for common diseases: application to analysis of sequence data. Am. J. Hum. Genet. 83, 311-321. doi: 10.1016/j.ajhg.2008.06.024.
40. Li, J., Wang, Y., Luo, J., Fu, Z., Ying, J., Yu, Y., et al. (2012). miR-134 inhibits epithelial to mesenchymal transition by targeting FOXM1 in non-small cell lung cancer cells. FEBS Lett. 586, 3761-3765. doi: 10.1016/j.febslet.2012.09.016.
41. Liu, S., Lachapelle, J., Leung, S., Gao, D., Foulkes, W. D., and Nielsen, T. O. (2012). CD8+ lymphocyte infiltration is an independent favorable prognostic indicator in basal-like breast cancer. Breast Cancer Res. 14, R48. doi: 10.1186/bcr3148.
42. Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402-408. doi: 10.1006/meth.2001.1262.
43. Madhavan, S., Gusev, Y., Harris, M., Tanenbaum, D. M., Gauba, R., Bhuvaneshwar, K., et al. (2011). G-DOC: a systems medicine platform for personalized oncology. Neoplasia 13, 771-783. doi: 10.1593/neo.11806.
44. Maran, R. R., Thomas, A., Roth, M., Sheng, Z., Esterly, N., Pinson, D., et al. (2009). Farnesoid X receptor deficiency in mice leads to increased intestinal epithelial cell proliferation and tumor development. J. Pharmacol. Exp. Ther. 328, 469-477. doi: 10.1124/jpet.108.145409.
45. McMillan, D. C., Fyffe, G. D., Wotherspoon, H. A., Cooke, T. G., and McArdle, C. S. (1997). Prospective study of circulating T-lymphocyte subpopulations and disease progression in colorectal cancer. Dis. Colon Rectum 40, 1068-1071. doi: 10.1007/BF02050931.
46. Modica, S., Murzilli, S., Salvatore, L., Schmidt, D. R., and Moschetta, A. (2008). Nuclear bile acid receptor FXR protects against intestinal tumorigenesis. Cancer Res. 68, 9589-9594. doi: 10.1158/0008-5472.CAN-08-1791.
47. Moller, P., Koretz, K., Leithauser, F., Bruderlein, S., Henne, C., Quentmeier, A., et al. (1994). Expression of APO-1 (CD95), a member of the NGF/TNF receptor superfamily, in normal and neoplastic colon epithelium. Int. J. Cancer 57, 371-377. doi: 10.1002/ijc.2910570314.
48. Muthuswamy, R., Berk, E., Junecko, B. F., Zeh, H. J., Zureikat, A. H., Normolle, D., et al. (2012). NF-kappaB hyperactivation in tumor tissues allows tumor-selective reprogramming of the chemokine microenvironment to enhance the recruitment of cytolytic T effector cells. Cancer Res. 72, 3735-3743. doi: 10.1158/0008-5472.CAN-11-4136.
49. Pages, F., Berger, A., Camus, M., Sanchez-Cabo, F., Costes, A., Molidor, R., et al. (2005). Effector memory T cells, early metastasis, and survival in colorectal cancer. N. Engl. J. Med. 353, 2654-2666. doi: 10.1056/NEJMoa051424.
50. Picard, R. R., and Cook, R. D. (1984). Cross-validation of regression models. J. Am. Stat. Assoc. 79, 575-583. doi: 10.1080/01621459.1984.10478083.
51. Ritchie, A. J., Yam, A. O., Tanabe, K. M., Rice, S. A., and Cooley, M. A. (2003). Modification of in vivo and in vitro T-and B-cell-mediated immune responses by the Pseudomonas aeruginosa quorum-sensing molecule N-(3-oxododecanoyl)-L-homoserine lactone. Infect. Immun. 71, 4421-4431. doi: 10.1128/IAI.71.8.4421-4431.2003.
52. Robin, X., Turck, N., Hainard, A., Tiberti, N., Lisacek, F., Sanchez, J. C., et al. (2011). pROC: an open-source package for R and S+ to analyze and compare ROC curves. BMC Bioinformatics 12:77 doi: 10.1186/1471-2105-12-77.
53. Rodin, A. S., Gogoshin, G., and Boerwinkle, E. (2011). Systems biology data analysis methodology in pharmacogenomics. Pharmacogenomics 12, 1349-1360. doi: 10.2217/pgs.11.76.
54. Rustgi, A. K. (2007). The genetics of hereditary colon cancer. Genes Dev. 21, 2525-2538. doi: 10.1101/gad.1593107.
55. Schmittgen, T. D., Lee, E. J., Jiang, J., Sarkar, A., Yang, L., Elton, T. S., et al. (2008). Real-time PCR quantification of precursor and mature microRNA. Methods 44, 31-38. doi: 10.1016/j.ymeth.2007.09.006.
56. Schrag, D., Cramer, L. D., Bach, P. B., and Begg, C. B. (2001). Age and adjuvant chemotherapy use after surgery for stage III colon cancer. J. Natl. Cancer Inst. 93, 850-857. doi: 10.1093/jnci/93.11.850.
57. Shaw, A. T., Kim, D. W., Nakagawa, K., Seto, T., Crino, L., Ahn, M. J., et al. (2013). Crizotinib versus chemotherapy in advanced ALK-positive lung cancer. N. Engl. J. Med. 368, 2385-2394. doi: 10.1056/NEJMoa1214886.
58. Strater, J., Hinz, U., Hasel, C., Bhanot, U., Mechtersheimer, G., Lehnert, T., et al. (2005). Impaired CD95 expression predisposes for recurrence in curatively resected colon carcinoma: clinical evidence for immunoselection and CD95L mediated control of minimal residual disease. Gut 54, 661-665. doi: 10.1136/gut.2004.052696.
59. Sun, H. X., Chen, Y., and Ye, Y. (2006). Ginsenoside Re and notoginsenoside R1: Immunologic adjuvants with low haemolytic effect. Chem. Biodivers 3, 718-726. doi: 10.1002/cbdv.200690074.
60. TCGA. (2012). Comprehensive molecular characterization of human colon and rectal cancer. Nature 487, 330-337. doi: 10.1038/nature11252.
61. Torres, J., Bao, X., Iuga, A. C., Chen, A., Harpaz, N., Ullman, T., et al. (2013). Farnesoid X receptor expression is decreased in colonic mucosa of patients with primary sclerosing cholangitis and colitis-associated neoplasia. Inflamm. Bowel Dis. 19, 275-282. doi: 10.1097/MIB.0b013e318286ff2e.
62. Tosolini, M., Kirilovsky, A., Mlecnik, B., Fredriksen, T., Mauger, S., Bindea, G., et al. (2011). Clinical impact of different classes of infiltrating T cytotoxic and helper cells (Th1, th2, treg, th17) in patients with colorectal cancer. Cancer Res. 71, 1263-1271. doi: 10.1158/0008-5472.CAN-10-2907.
63. Toyoda, T., and Wada, A. (2004). Omic space: coordinate-based integration and analysis of genomic phenomic interactions. Bioinformatics 20, 1759-1765. doi: 10.1093/bioinformatics/bth165.
64. Venook, A. P., Niedzwiecki, D., Lopatin, M., Ye, X., Lee, M., Friedman, P. N., et al. (2013). Biologic determinants of tumor recurrence in stage II colon cancer: validation study of the 12-gene recurrence score in cancer and leukemia group B (CALGB) 9581. J. Clin. Oncol. 31, 1775-1781. doi: 10.1200/JCO.2012.45.1096.
65. Vlachos, I. S., Kostoulas, N., Vergoulis, T., Georgakilas, G., Reczko, M., Maragkakis, M., et al. (2012). DIANA miRPath v.2.0: investigating the combinatorial effect of microRNAs in pathways. Nucleic Acids Res. 40, W498-W504. doi: 10.1093/nar/gks494.
66. Wagner, J. M., and Cohen, S. (1991). Fibrous myopathy from butorphanol injections. J. Rheumatol. 18, 1934-1935.
67. Wang, D., Dubois, R. N., and Richmond, A. (2009). The role of chemokines in intestinal inflammation and cancer. Curr. Opin. Pharmacol. 9, 688-696. doi: 10.1016/j.coph.2009.08.003.
68. Whiteside, T. L. (2013). Immune responses to cancer: are they potential biomarkers of prognosis? Front. Oncol. 3:107. doi: 10.3389/fonc.2013.00107.
69. Wong, W. H., and Li, C. (2003). "DNA-Chip Analyzer (dChip), Chapter 5," in The Analysis of Gene Expression Data, eds G. Parmigiani, E. Garrett, R. Irizarry and S. L. Zeger (New York, NY: Springer), 120-141.
70. Yeung, D. T., and Hughes, T. P. (2012). Therapeutic targeting of BCR-ABL: prognostic markers of response and resistance mechanism in chronic myeloid leukaemia. Crit. Rev. Oncog. 17, 17-30. doi: 10.1615/CritRevOncog.v17.i1.30.
71. Zlobec, I., Terracciano, L. M., and Lugli, A. (2008). Local recurrence in mismatch repair-proficient colon cancer predicted by an infiltrative tumor border and lack of CD8+ tumor-infiltrating lymphocytes. Clin. Cancer Res. 14, 3792-3797. doi: 10.1158/1078-0432.CCR-08-0048.