Proteome profiling of cancer-associated fibroblasts identifies novel proinflammatory signatures and prognostic markers for colorectal cancer

Clinical Cancer Research

Volumn 19, Issue 21, 2013, Pages 6006-6019

  Torres, Sofia ^a   Bartolomé, Rubén A ^a   Mendes, Marta ^a   Barderas, Rodrigo ^a,e   Fernandez Aceñero, M Jesús ^b   Peláez García, Alberto ^a   Peña, Cristina ^c   Lopez Lucendo, María ^a   Villar Vázquez, Roi ^a   De Herreros, Antonio García ^d   Bonilla, Felix ^c   Casal, J Ignacio ^a  

^a CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^b HOSPITAL UNIVERSITARIO FUNDACIÓN JIMÉNEZ DÍAZ   (Spain)

^c HOSPITAL UNIVERSITARIO PUERTA DE HIERRO   (Spain)

^d Del Mar University Hospital   (Spain)

^e UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CELL EXTRACT; CELL PROTEIN; CYTOKINE; MONOCYTE CHEMOTACTIC PROTEIN 1; MONOCYTE CHEMOTACTIC PROTEIN 2; PROTEIN CALU; PROTEIN CDH11; PROTEIN FSTL1; PROTEIN LTBP2; PROTEIN OLFML3; PROTEOME; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER ASSOCIATED FIBROBLAST; CANCER PROGNOSIS; CANCER SURVIVAL; CELL ISOLATION; CELL MIGRATION; CELL STRAIN; CELL STRAIN KM12; COLORECTAL CARCINOMA; CONTROLLED STUDY; DISEASE FREE SURVIVAL; DISEASE MARKER; EPITHELIUM CELL; FIBROBLAST; HUMAN; HUMAN CELL; HUMAN TISSUE; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS; QUANTITATIVE ANALYSIS; STROMA; TANDEM MASS SPECTROMETRY; TUMOR INVASION; UPREGULATION;

ANIMALS; BIOLOGICAL MARKERS; CELL LINE, TUMOR; COLORECTAL NEOPLASMS; CYTOKINES; DISEASE MODELS, ANIMAL; FIBROBLASTS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INFLAMMATION MEDIATORS; MICE; MYOFIBROBLASTS; PROGNOSIS; PROTEIN INTERACTION MAPS; PROTEOME; REPRODUCIBILITY OF RESULTS; STROMAL CELLS;

EID: 84887108621     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-13-1130     Document Type: Article

References (47)

1. Hanahan D, Coussens LM. Accessories to the crime: functions of cells recruited to the tumor microenvironment. Cancer Cell 2012;21: 309-22.
2. De Wever O, Demetter P, Mareel M, Bracke M. Stromal myofibroblasts are drivers of invasive cancer growth. Int J Cancer 2008;123: 2229-38.
3. Dvorak HF. Tumors: wounds that do not heal. Similarities between tumor stroma generation and wound healing. N Engl J Med 1986;315: 1650-9.
4. Kalluri R, Zeisberg M. Fibroblasts in cancer. Nat Rev Cancer 2006;6: 392-401.
5. Kuperwasser C, Chavarria T, Wu M, Magrane G, Gray JW, Carey L, et al. Reconstruction of functionally normal and malignant human breast tissues in mice. Proc Natl Acad Sci U S A 2004;101: 4966-71.
6. Liao D, Luo Y, Markowitz D, Xiang R, Reisfeld RA. Cancer associated fibroblasts promote tumor growth and metastasis by modulating the tumor immune microenvironment in a 4T1 murine breast cancer model. PLoS One 2009;4:e7965.
7. Erez N, Truitt M, Olson P, Arron ST, Hanahan D. Cancer-associated fibroblasts are activated in incipient neoplasia to orchestrate tumorpromoting inflammation in an NF-kappaB-dependent manner. Cancer Cell 2010;17: 135-47.
8. Swartz MA, Iida N, Roberts EW, Sangaletti S, Wong MH, Yull FE, et al. Tumor microenvironment complexity: emerging roles in cancer therapy. Cancer Res 2012;72: 2473-80.
9. Coulson-Thomas VJ, Coulson-Thomas YM, Gesteira TF, de Paula CA, Mader AM, Waisberg J, et al. Colorectal cancer desmoplastic reaction up-regulates collagen synthesis and restricts cancer cell invasion. Cell Tissue Res 2011;346: 223-36.
10. Karagiannis GS, Petraki C, Prassas I, Saraon P, Musrap N, Dimitromanolakis A, et al. Proteomic signatures of the desmoplastic invasion front reveal collagen type XII as a marker of myofibroblastic differentiation during colorectal cancer metastasis. Oncotarget 2012;3: 267-85.
11. Nambiar PR, Girnun G, Lillo NA, Guda K, Whiteley HE, Rosenberg DW. Preliminary analysis of azoxymethane induced colon tumors in inbred mice commonly used as transgenic/knockout progenitors. Int J Oncol 2003;22: 145-50.
12. Terzic J, Grivennikov S, Karin E, Karin M. Inflammation and colon cancer. Gastroenterology 2010;138: 2101-14.
13. Goetz JG, Minguet S, Navarro-Lerida I, Lazcano JJ, Samaniego R, Calvo E, et al. Biomechanical remodeling of the microenvironment by stromal caveolin-1 favors tumor invasion and metastasis. Cell 2011; 146: 148-63.
14. Dolznig H, Rupp C, Puri C, Haslinger C, Schweifer N, Wieser E, et al. Modeling colon adenocarcinomas in vitro a 3D co-culture system induces cancer-relevant pathways upon tumor cell and stromal fibroblast interaction. Am J Pathol 2011;179: 487-501.
15. Li Z, Adams RM, Chourey K, Hurst GB, Hettich RL, Pan C. Systematic comparison of label-free, metabolic labeling, and isobaric chemical labeling for quantitative proteomics on LTQ orbitrap velos. J Proteome Res 2012;11: 1582-90.
16. Beddy D, Mulsow J, Watson RW, Fitzpatrick JM, O'Connell PR. Expression and regulation of connective tissue growth factor by transforming growth factor beta and tumour necrosis factor alpha in fibroblasts isolated from strictures in patients with Crohn's disease. Br J Surg 2006;93: 1290-6.
17. Morikawa K, Walker SM, Jessup JM, Fidler IJ. In vivo selection of highly metastatic cells from surgical specimens of different primary human colon carcinomas implanted into nude mice. Cancer Res 1988;48: 1943-8.
18. Barderas R, Bartolom-e RA, Fernandez-AceñeroMJ, Torres S,Casal JI. High expression of IL-13 receptor alpha2 in colorectal cancer is associated with invasion, liver metastasis, and poor prognosis. Cancer Res 2012;72: 2780-90.
19. Al-Shahrour F, Diaz-Uriarte R, Dopazo J. FatiGO: a web tool for finding significant associations of Gene Ontology terms with groups of genes. Bioinformatics 2004;20: 578-80.
20. Jankova L, Chan C, Fung CL, Song X, Kwun SY, Cowley MJ, et al. Proteomic comparison of colorectal tumours and non-neoplastic mucosa from paired patient samples using iTRAQ mass spectrometry. Mol Biosyst 2011;7: 2997-3005.
21. Karnoub AE, Weinberg RA. Chemokine networks and breast cancer metastasis. Breast Dis 2006;26: 75-85.
22. Cook AC, Tuck AB, McCarthy S, Turner JG, Irby RB, Bloom GC, et al. Osteopontin induces multiple changes in gene expression that reflect the six "hallmarks of cancer" in a model of breast cancer progression. Mol Carcinog 2005;43: 225-36.
23. Cerami E, Gao J, Dogrusoz U, Gross BE, Sumer SO, Aksoy BA, et al. The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov 2012;2: 401-4.
24. Fijneman RJ, de Wit M, Pourghiasian M, Piersma SR, Pham TV, Warmoes MO, et al. Proximal fluid proteome profiling of mouse colon tumors reveals biomarkers for early diagnosis of human colorectal cancer. Clin Cancer Res 2012;18: 2613-24.
25. Tsujino T, Seshimo I, Yamamoto H, Ngan CY, Ezumi K, Takemasa I, et al. Stromal myofibroblasts predict disease recurrence for colorectal cancer. Clin Cancer Res 2007;13: 2082-90.
26. Levental KR, Yu H, Kass L, Lakins JN, Egeblad M, Erler JT, et al. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 2009;139: 891-906.
27. Ngan CY, Yamamoto H, Seshimo I, Tsujino T, Man-i M, Ikeda JI, et al. Quantitative evaluation of vimentin expression in tumour stroma of colorectal cancer. Br J Cancer 2007;96: 986-92.
28. Henry LR, Lee HO, Lee JS, Klein-Szanto A, Watts P, Ross EA, et al. Clinical implications of fibroblast activation protein in patients with colon cancer. Clin Cancer Res 2007;13: 1736-41.
29. Wajih N, Owen J, Wallin R. Enhanced functional recombinant factor VII production by HEK 293 cells stably transfected with VKORC1 where the gamma-carboxylase inhibitor calumenin is stably suppressed by shRNA transfection. Thromb Res 2008;122: 405-10.
30. Galamb O, Gyorffy B, Sipos F, Spisak S, Nemeth AM, Miheller P, et al. Inflammation, adenoma and cancer: objective classification of colon biopsy specimens with gene expression signature. Dis Markers 2008;25: 1-16.
31. Mikula M, Rubel T, Karczmarski J, Goryca K, Dadlez M, Ostrowski J. Integrating proteomic and transcriptomic high-throughput surveys for search of new biomarkers of colon tumors. Funct Integr Genomics 2011;11: 215-24.
32. Schneider DJ,WuM, Le TT, Cho SH, Brenner MB, Blackburn MR, et al. Cadherin-11 contributes to pulmonary fibrosis: potential role in TGFbeta production and epithelial to mesenchymal transition. FASEB J 2012;26: 503-12.
33. Vered M, Dayan D, Yahalom R, Dobriyan A, Barshack I, Bello IO, et al. Cancer-associated fibroblasts and epithelial-mesenchymal transition in metastatic oral tongue squamous cell carcinoma. Int J Cancer 2010;127: 1356-62.
34. Inomata H, Haraguchi T, Sasai Y. Robust stability of the embryonic axial pattern requires a secreted scaffold for chordin degradation. Cell 2008;134: 854-65.
35. Miljkovic-Licina M, Hammel P, Garrido-Urbani S, Lee BP, Meguenani M, Chaabane C, et al. Targeting olfactomedin-like 3 inhibits tumor growth by impairing angiogenesis and pericyte coverage. Mol Cancer Ther 2012;11: 2588-99.
36. Chaly Y, Marinov AD, Oxburgh L, Bushnell DS, Hirsch R. FSTL1 promotes arthritis in mice by enhancing inflammatory cytokine/chemokine expression. Arthritis Rheum 2012;64: 1082-8.
37. Ouchi N, Oshima Y, Ohashi K, Higuchi A, Ikegami C, Izumiya Y, et al. Follistatin-like 1, a secreted muscle protein, promotes endothelial cell function and revascularization in ischemic tissue through a nitric-oxide synthase-dependent mechanism. J Biol Chem 2008;283: 32802-11.
38. Mangasser-Stephan K, Gartung C, Lahme B, Gressner AM. Expression of isoforms and splice variants of the latent transforming growth factor beta binding protein (LTBP) in cultured human liver myofibroblasts. Liver 2001;21: 105-13.
39. Gabrielsen A, Lawler PR, Yongzhong W, Steinbruchel D, Blagoja D, Paulsson-Berne G, et al. Gene expression signals involved in ischemic injury, extracellular matrix composition and fibrosis defined by global mRNA profiling of the human left ventricular myocardium. J Mol Cell Cardiol 2007;42: 870-83.
40. Turtoi A, Musmeci D, Wang Y, Dumont B, Somja J, Bevilacqua G, et al. Identification of novel accessible proteins bearing diagnostic and therapeutic potential in human pancreatic ductal adenocarcinoma. J Proteome Res 2011;10: 4302-13.
41. Buckley CD, Pilling D, Lord JM, Akbar AN, Scheel-Toellner D, Salmon M. Fibroblasts regulate the switch from acute resolving to chronic persistent inflammation. Trends Immunol 2001;22: 199-204.
42. Calon A, Espinet E, Palomo-Ponce S, Tauriello DV, Iglesias M, Cespedes MV, et al. Dependency of colorectal cancer on a TGFbeta- driven program in stromal cells for metastasis initiation. Cancer Cell 2012;22: 571-84.
43. Uguccioni M, D'Apuzzo M, Loetscher M, Dewald B, Baggiolini M. Actions of the chemotactic cytokines MCP-1, MCP-2, MCP-3, RANTES, MIP-1 alpha and MIP-1 beta on human monocytes. Eur J Immunol 1995;25: 64-8.
44. Taub DD, Proost P, Murphy WJ, Anver M, Longo DL, van Damme J, et al. Monocyte chemotactic protein-1 (MCP-1), -2, and -3 are chemotactic for human T lymphocytes. J Clin Invest 1995;95: 1370-6.
45. Erreni M, Bianchi P, Laghi L, Mirolo M, Fabbri M, Locati M, et al. Expression of chemokines and chemokine receptors in human colon cancer. Methods Enzymol 2009;460: 105-21.
46. Wang D, Dubois RN, Richmond A. The role of chemokines in intestinal inflammation and cancer. Curr Opin Pharmacol 2009;9: 688-96.
47. Kunz-Schughart LA, Knuechel R. Tumor-associated fibroblasts (part I): Active stromal participants in tumor development and progression? Histol Histopathol 2002;17: 599-621.