Molecular Profiling of Multiple Human Cancers Defines an Inflammatory Cancer-Associated Molecular Pattern and Uncovers KPNA2 as a Uniform Poor Prognostic Cancer Marker

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Rachidi, Saleh M ^a,b   Qin, Tingting ^a   Sun, Shaoli ^a   Zheng, W Jim ^a,b   Li, Zihai ^a,b  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD36 ANTIGEN; COMPLEMENTARY DNA; CXCL13 CHEMOKINE; TUMOR MARKER;

ARTICLE; BREAST CANCER; CANCER GENETICS; CANCER PROGNOSIS; CANCER SURVIVAL; CD36 GENE; COLON CANCER; CONTROLLED STUDY; CXCL13 GENE; EDNRA GENE; GENE; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION; GENETIC MARKER; GREM1 GENE; HEAD AND NECK CANCER; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNE RESPONSE GENE; IMMUNOHISTOCHEMISTRY; KARYOPHERIN ALPHA 2 GENE; LOX GENE; LUNG CANCER; MOUTH CANCER; ONCOGENE; OVARY CANCER; OVERALL SURVIVAL; PANCREAS CANCER; PROSTATE CANCER; STOMACH CANCER; TISSUE MICROARRAY; TNFAIP6 GENE; UPREGULATION;

ADENOCARCINOMA; ALPHA KARYOPHERINS; CARCINOMA, SQUAMOUS CELL; CELL ADHESION MOLECULES; CLUSTER ANALYSIS; COLONIC NEOPLASMS; DATA MINING; DATABASES, GENETIC; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HEAD AND NECK NEOPLASMS; HUMANS; INFLAMMATION; NEOPLASM STAGING; NEOPLASMS; PROGNOSIS; TUMOR MARKERS, BIOLOGICAL; WORKFLOW;

EID: 84875433210     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0057911     Document Type: Article

References (78)

1. Grivennikov SI, Greten FR, Karin M, (2010) Immunity, inflammation, and cancer. Cell 140: 883-899.
2. Goldstein MG, Li Z, (2009) Heat-shock proteins in infection-mediated inflammation-induced tumorigenesis. J Hematol Oncol 2: 5.
3. Schreiber RD, Old LJ, Smyth MJ, (2011) Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion. Science 331: 1565-1570.
4. Gabrilovich DI, Nagaraj S, (2009) Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 9: 162-174.
5. Zou W, (2006) Regulatory T cells, tumour immunity and immunotherapy. Nat Rev Immunol 6: 295-307.
6. Okazaki IM, Kotani A, Honjo T, (2007) Role of AID in tumorigenesis. Adv Immunol 94: 245-273.
7. Oguma K, Oshima H, Aoki M, Uchio R, Naka K, et al. (2008) Activated macrophages promote Wnt signalling through tumour necrosis factor-alpha in gastric tumour cells. EMBO J 27: 1671-1681.
8. Grivennikov SI, Karin M, (2010) Dangerous liaisons: STAT3 and NF-kappaB collaboration and crosstalk in cancer. Cytokine Growth Factor Rev 21: 11-19.
9. Yang J, Weinberg RA, (2008) Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev Cell 14: 818-829.
10. Turashvili G, Bouchal J, Baumforth K, Wei W, Dziechciarkova M, et al. (2007) Novel markers for differentiation of lobular and ductal invasive breast carcinomas by laser microdissection and microarray analysis. BMC Cancer 7: 55.
11. Skrzypczak M, Goryca K, Rubel T, Paziewska A, Mikula M, et al. (2010) Modeling oncogenic signaling in colon tumors by multidirectional analyses of microarray data directed for maximization of analytical reliability. PLoS One 5.
12. D'Errico M, de Rinaldis E, Blasi MF, Viti V, Falchetti M, et al. (2009) Genome-wide expression profile of sporadic gastric cancers with microsatellite instability. Eur J Cancer 45: 461-469.
13. Hou J, Aerts J, den Hamer B, van Ijcken W, den Bakker M, et al. (2010) Gene expression-based classification of non-small cell lung carcinomas and survival prediction. PLoS One 5: e10312.
14. Ye H, Yu T, Temam S, Ziober BL, Wang J, et al. (2008) Transcriptomic dissection of tongue squamous cell carcinoma. BMC Genomics 9: 69.
15. Badea L, Herlea V, Dima SO, Dumitrascu T, Popescu I, (2008) Combined gene expression analysis of whole-tissue and microdissected pancreatic ductal adenocarcinoma identifies genes specifically overexpressed in tumor epithelia. Hepatogastroenterology 55: 2016-2027.
16. Wang Y, Xia XQ, Jia Z, Sawyers A, Yao H, et al. (2010) In silico estimates of tissue components in surgical samples based on expression profiling data. Cancer Res 70: 6448-6455.
17. Tsoi LC, Qin T, Slate EH, Zheng WJ, (2011) Consistent Differential Expression Pattern (CDEP) on microarray to identify genes related to metastatic behavior. BMC Bioinformatics 12: 438.
18. Gentleman R, Irizarry RA, Martinez-Murillo F, Spencer F, Wu Z, (2004) A Model-Based Background Adjustment for Oligonucleotide Expression Arrays. Journal of the American Statistical Association 99: 909-917.
19. Hong F, Breitling R, McEntee CW, Wittner BS, Nemhauser JL, et al. (2006) RankProd: a bioconductor package for detecting differentially expressed genes in meta-analysis. Bioinformatics 22: 2825-2827.
20. Lunn D, Spiegelhalter D, Thomas A, Best N, (2009) The BUGS project: Evolution, critique and future directions. Stat Med 28: 3049-3067.
21. Camp RL, Dolled-Filhart M, Rimm DL, (2004) X-tile: a new bio-informatics tool for biomarker assessment and outcome-based cut-point optimization. Clin Cancer Res 10: 7252-7259.
22. Tothill RW, Tinker AV, George J, Brown R, Fox SB, et al. (2008) Novel molecular subtypes of serous and endometrioid ovarian cancer linked to clinical outcome. Clin Cancer Res 14: 5198-5208.
23. Dankof A, Fritzsche FR, Dahl E, Pahl S, Wild P, et al. (2007) KPNA2 protein expression in invasive breast carcinoma and matched peritumoral ductal carcinoma in situ. Virchows Arch 451: 877-881.
24. Mortezavi A, Hermanns T, Seifert HH, Baumgartner MK, Provenzano M, et al. (2011) KPNA2 expression is an independent adverse predictor of biochemical recurrence after radical prostatectomy. Clin Cancer Res 17: 1111-1121.
25. Sakai M, Sohda M, Miyazaki T, Suzuki S, Sano A, et al. (2010) Significance of karyopherin-{alpha} 2 (KPNA2) expression in esophageal squamous cell carcinoma. Anticancer Res 30: 851-856.
26. Zheng M, Tang L, Huang L, Ding H, Liao WT, et al. (2010) Overexpression of karyopherin-2 in epithelial ovarian cancer and correlation with poor prognosis. Obstet Gynecol 116: 884-891.
27. Gousias K, Becker AJ, Simon M, Niehusmann P, (2012) Nuclear karyopherin a2: a novel biomarker for infiltrative astrocytomas. J Neurooncol 109: 545-553.
28. Frieman M, Yount B, Heise M, Kopecky-Bromberg SA, Palese P, et al. (2007) Severe acute respiratory syndrome coronavirus ORF6 antagonizes STAT1 function by sequestering nuclear import factors on the rough endoplasmic reticulum/Golgi membrane. J Virol 81: 9812-9824.
29. Umegaki N, Tamai K, Nakano H, Moritsugu R, Yamazaki T, et al. (2007) Differential regulation of karyopherin alpha 2 expression by TGF-beta1 and IFN-gamma in normal human epidermal keratinocytes: evident contribution of KPNA2 for nuclear translocation of IRF-1. J Invest Dermatol 127: 1456-1464.
30. Hendrix ND, Wu R, Kuick R, Schwartz DR, Fearon ER, et al. (2006) Fibroblast growth factor 9 has oncogenic activity and is a downstream target of Wnt signaling in ovarian endometrioid adenocarcinomas. Cancer Res 66: 1354-1362.
31. Lu KH, Patterson AP, Wang L, Marquez RT, Atkinson EN, et al. (2004) Selection of potential markers for epithelial ovarian cancer with gene expression arrays and recursive descent partition analysis. Clin Cancer Res 10: 3291-3300.
32. Welsh JB, Zarrinkar PP, Sapinoso LM, Kern SG, Behling CA, et al. (2001) Analysis of gene expression profiles in normal and neoplastic ovarian tissue samples identifies candidate molecular markers of epithelial ovarian cancer. Proc Natl Acad Sci U S A 98: 1176-1181.
33. Bonome T, Levine DA, Shih J, Randonovich M, Pise-Masison CA, et al. (2008) A gene signature predicting for survival in suboptimally debulked patients with ovarian cancer. Cancer Res 68: 5478-5486.
34. Adib TR, Henderson S, Perrett C, Hewitt D, Bourmpoulia D, et al. (2004) Predicting biomarkers for ovarian cancer using gene-expression microarrays. Br J Cancer 90: 686-692.
35. Kaiser S, Park YK, Franklin JL, Halberg RB, Yu M, et al. (2007) Transcriptional recapitulation and subversion of embryonic colon development by mouse colon tumor models and human colon cancer. Genome Biol 8: R131.
36. Ki DH, Jeung HC, Park CH, Kang SH, Lee GY, et al. (2007) Whole genome analysis for liver metastasis gene signatures in colorectal cancer. Int J Cancer 121: 2005-2012.
37. Smith JJ, Deane NG, Wu F, Merchant NB, Zhang B, et al. (2010) Experimentally derived metastasis gene expression profile predicts recurrence and death in patients with colon cancer. Gastroenterology 138: 958-968.
38. Schwartz DR, Kardia SL, Shedden KA, Kuick R, Michailidis G, et al. (2002) Gene expression in ovarian cancer reflects both morphology and biological behavior, distinguishing clear cell from other poor-prognosis ovarian carcinomas. Cancer Res 62: 4722-4729.
39. Sieben NL, Oosting J, Flanagan AM, Prat J, Roemen GM, et al. (2005) Differential gene expression in ovarian tumors reveals Dusp 4 and Serpina 5 as key regulators for benign behavior of serous borderline tumors. J Clin Oncol 23: 7257-7264.
40. Schaner ME, Ross DT, Ciaravino G, Sorlie T, Troyanskaya O, et al. (2003) Gene expression patterns in ovarian carcinomas. Mol Biol Cell 14: 4376-4386.
41. Moroianu J, Hijikata M, Blobel G, Radu A, (1995) Mammalian karyopherin alpha 1 beta and alpha 2 beta heterodimers: alpha 1 or alpha 2 subunit binds nuclear localization signal and beta subunit interacts with peptide repeat-containing nucleoporins. Proc Natl Acad Sci U S A 92: 6532-6536.
42. Wisniewski HG, Vilcek J, (1997) TSG-6: an IL-1/TNF-inducible protein with anti-inflammatory activity. Cytokine Growth Factor Rev 8: 143-156.
43. Marshall KW, Mohr S, Khettabi FE, Nossova N, Chao S, et al. (2010) A blood-based biomarker panel for stratifying current risk for colorectal cancer. Int J Cancer 126: 1177-1186.
44. Hanahan D, Weinberg RA, (2011) Hallmarks of cancer: the next generation. Cell 144: 646-674.
45. Mlecnik B, Tosolini M, Charoentong P, Kirilovsky A, Bindea G, et al. (2010) Biomolecular network reconstruction identifies T-cell homing factors associated with survival in colorectal cancer. Gastroenterology 138: 1429-1440.
46. Osaki T, Saito H, Fukumoto Y, Yamada Y, Fukuda K, et al. (2009) Inverse correlation between NKG2D expression on CD8+ T cells and the frequency of CD4+CD25+ regulatory T cells in patients with esophageal cancer. Dis Esophagus 22: 49-54.
47. Sers C, Kuner R, Falk CS, Lund P, Sueltmann H, et al. (2009) Down-regulation of HLA Class I and NKG2D ligands through a concerted action of MAPK and DNA methyltransferases in colorectal cancer cells. Int J Cancer 125: 1626-1639.
48. Legrand F, Driss V, Delbeke M, Loiseau S, Hermann E, et al. (2010) Human eosinophils exert TNF-alpha and granzyme A-mediated tumoricidal activity toward colon carcinoma cells. J Immunol 185: 7443-7451.
49. Horne HN, Lee PS, Murphy SK, Alonso MA, Olson JA Jr, et al. (2009) Inactivation of the MAL gene in breast cancer is a common event that predicts benefit from adjuvant chemotherapy. Mol Cancer Res 7: 199-209.
50. Beder LB, Gunduz M, Hotomi M, Fujihara K, Shimada J, et al. (2009) T-lymphocyte maturation-associated protein gene as a candidate metastasis suppressor for head and neck squamous cell carcinomas. Cancer Sci 100: 873-880.
51. Janeway CA Jr, (1989) Approaching the asymptote? Evolution and revolution in immunology. Cold Spring Harb Symp Quant Biol 54: 1-13.
52. Young JC, Major AT, Miyamoto Y, Loveland KL, Jans DA, (2011) Distinct effects of importin alpha2 and alpha4 on Oct3/4 localization and expression in mouse embryonic stem cells. FASEB J 25: 3958-3965.
53. Ly-Huynh JD, Lieu KG, Major AT, Whiley PA, Holt JE, et al. (2011) Importin alpha2-interacting proteins with nuclear roles during mammalian spermatogenesis. Biol Reprod 85: 1191-1202.
54. Li X, Sun L, Jin Y, (2008) Identification of karyopherin-alpha 2 as an Oct4 associated protein. J Genet Genomics 35: 723-728.
55. Jensen JB, Munksgaard PP, Sorensen CM, Fristrup N, Birkenkamp-Demtroder K, et al. (2011) High expression of karyopherin-alpha2 defines poor prognosis in non-muscle-invasive bladder cancer and in patients with invasive bladder cancer undergoing radical cystectomy. Eur Urol 59: 841-848.
56. Wang CI, Wang CL, Wang CW, Chen CD, Wu CC, et al. (2011) Importin subunit alpha-2 is identified as a potential biomarker for non-small cell lung cancer by integration of the cancer cell secretome and tissue transcriptome. Int J Cancer 128: 2364-2372.
57. He L, Ding H, Wang JH, Zhou Y, Li L, et al. (2012) Overexpression of karyopherin 2 in human ovarian malignant germ cell tumor correlates with poor prognosis. PLoS One 7: e42992.
58. Winnepenninckx V, Lazar V, Michiels S, Dessen P, Stas M, et al. (2006) Gene expression profiling of primary cutaneous melanoma and clinical outcome. J Natl Cancer Inst 98: 472-482.
59. Noetzel E, Rose M, Bornemann J, Gajewski M, Knuchel R, et al. (2012) Nuclear transport receptor karyopherin-alpha2 promotes malignant breast cancer phenotypes in vitro. Oncogene 31: 2101-2114.
60. Cardoso F, Van't Veer L, Rutgers E, Loi S, Mook S, et al. (2008) Clinical application of the 70-gene profile: the MINDACT trial. J Clin Oncol 26: 729-735.
61. Paik S, Shak S, Tang G, Kim C, Baker J, et al. (2004) A multigene assay to predict recurrence of tamoxifen-treated, node-negative breast cancer. N Engl J Med 351: 2817-2826.
62. Galon J, Franck P, Marincola FM, Angell HK, Thurin M, et al. (2012) Cancer classification using the Immunoscore: a worldwide task force. J Transl Med 10: 205.
63. Hoosein MM, Dashwood MR, Dawas K, Ali HM, Grant K, et al. (2007) Altered endothelin receptor subtypes in colorectal cancer. Eur J Gastroenterol Hepatol 19: 775-782.
64. Brown LF, Papadopoulos-Sergiou A, Berse B, Manseau EJ, Tognazzi K, et al. (1994) Osteopontin expression and distribution in human carcinomas. Am J Pathol 145: 610-623.
65. Noetzel E, Rose M, Bornemann J, Gajewski M, Knuchel R, et al. (2011) Nuclear transport receptor karyopherin-alpha2 promotes malignant breast cancer phenotypes in vitro. Oncogene.
66. Lange K, Kammerer M, Hegi ME, Grotegut S, Dittmann A, et al. (2007) Endothelin receptor type B counteracts tenascin-C-induced endothelin receptor type A-dependent focal adhesion and actin stress fiber disorganization. Cancer Res 67: 6163-6173.
67. Erler JT, Bennewith KL, Cox TR, Lang G, Bird D, et al. (2009) Hypoxia-induced lysyl oxidase is a critical mediator of bone marrow cell recruitment to form the premetastatic niche. Cancer Cell 15: 35-44.
68. Kodama J, Hasengaowa, Kusumoto T, Seki N, Matsuo T, et al. (2007) Prognostic significance of stromal versican expression in human endometrial cancer. Ann Oncol 18: 269-274.
69. Townes CL, Michailidis G, Nile CJ, Hall J, (2004) Induction of cationic chicken liver-expressed antimicrobial peptide 2 in response to Salmonella enterica infection. Infect Immun 72: 6987-6993.
70. Howard A, Townes C, Milona P, Nile CJ, Michailidis G, et al. (2010) Expression and functional analyses of liver expressed antimicrobial peptide-2 (LEAP-2) variant forms in human tissues. Cell Immunol 261: 128-133.
71. Khattar NH, Lele SM, Kaetzel CS, (2005) Down-regulation of the polymeric immunoglobulin receptor in non-small cell lung carcinoma: correlation with dysregulated expression of the transcription factors USF and AP2. J Biomed Sci 12: 65-77.
72. Ocak S, Pedchenko TV, Chen H, Harris FT, Qian J, et al. (2011) Loss of polymeric immunoglobulin receptor expression is associated with lung tumorigenesis. Eur Respir J.
73. Ai J, Tang Q, Wu Y, Xu Y, Feng T, et al. (2011) The role of polymeric immunoglobulin receptor in inflammation-induced tumor metastasis of human hepatocellular carcinoma. J Natl Cancer Inst 103: 1696-1712.
74. Cho YG, Chang X, Park IS, Yamashita K, Shao C, et al. (2011) Promoter methylation of leukemia inhibitory factor receptor gene in colorectal carcinoma. Int J Oncol 39: 337-344.
75. Okamura Y, Nomoto S, Kanda M, Li Q, Nishikawa Y, et al. (2010) Leukemia inhibitory factor receptor (LIFR) is detected as a novel suppressor gene of hepatocellular carcinoma using double-combination array. Cancer Lett 289: 170-177.
76. Garlanda C, Bottazzi B, Bastone A, Mantovani A, (2005) Pentraxins at the crossroads between innate immunity, inflammation, matrix deposition, and female fertility. Annu Rev Immunol 23: 337-366.
77. Bijsmans IT, Smits KM, de Graeff P, Wisman GB, van der Zee AG, et al. (2011) Loss of SerpinA5 protein expression is associated with advanced-stage serous ovarian tumors. Mod Pathol 24: 463-470.
78. Facciabene A, Peng X, Hagemann IS, Balint K, Barchetti A, et al. (2011) Tumour hypoxia promotes tolerance and angiogenesis via CCL28 and T(reg) cells. Nature 475: 226-230.