Quantitative secretome analysis reveals the interactions between epithelia and tumor cells by in vitro modulating colon cancer microenvironment

Journal of Proteomics

Volumn 89, Issue , 2013, Pages 51-70

  Zeng, Xiao ^a   Yang, Pengbo ^a   Chen, Bing ^a   Jin, Xuewen ^a   Liu, Yuling ^a   Zhao, Xia ^b   Liang, Shufang ^a  

^a SICHUAN UNIVERSITY   (China)

^b SICHUAN UNIVERSITY   (China)

Author keywords

Co culture; Quantitative proteomics; Secretome; Tumor microenvironment

Indexed keywords

ALPHA DYSTROGLYCAN; CARBONATE DEHYDRATASE II; CYTOKERATIN 9; ELONGATION FACTOR 1BETA; ERYTHROID POTENTIATING FACTOR; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HEAT SHOCK PROTEIN 70; HERMES ANTIGEN; HYPOCALCIN; LAMIN; LIPOPROTEIN LIPASE; MALATE DEHYDROGENASE; NUCLEOLIN; PEROXIREDOXIN; PEROXIREDOXIN 1; PROGRANULIN; PROSAPOSIN; PROTEASOME; SINGLE STRANDED DNA BINDING PROTEIN; SOMATOMEDIN BINDING PROTEIN 2; SOMATOMEDIN BINDING PROTEIN 6; STABLE ISOTOPE; STEM CELL FACTOR; TRIOSEPHOSPHATE ISOMERASE; VIMENTIN; PROTEOME; TUMOR PROTEIN;

APOPTOSIS; ARTICLE; BIOLOGICAL FUNCTIONS; CANCER CELL; CANCER GROWTH; CELL ADHESION; CELL COMMUNICATION; CELL COUNT; CELL CULTURE; CELL INTERACTION; CELL PROLIFERATION; CELL STRAIN HT29; CELLULAR DISTRIBUTION; COLON ADENOCARCINOMA; COLON CANCER; CONTROLLED STUDY; EPITHELIUM CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; ISOTOPE LABELING; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN SECRETION; PROTEOMICS; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; STROMA CELL; TUMOR INVASION; TUMOR MICROENVIRONMENT; COCULTURE; COLON; COLON TUMOR; INTESTINE MUCOSA; PATHOLOGY; PROCEDURES; SECRETION (PROCESS); TUMOR CELL LINE;

CELL COMMUNICATION; CELL LINE, TUMOR; COCULTURE TECHNIQUES; COLON; COLONIC NEOPLASMS; EPITHELIAL CELLS; HUMANS; INTESTINAL MUCOSA; NEOPLASM PROTEINS; PROTEOME; PROTEOMICS; TUMOR MICROENVIRONMENT;

EID: 84880124478     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2013.05.032     Document Type: Article

References (72)

1. Fukumura D., Jain R.K. Tumor microenvironment abnormalities: causes, consequences, and strategies to normalize. J Cell Biochem 2006, 101:937-949.
2. Mohla S. Tumor microenvironment. J Cell Biochem 2007, 101:801-804.
3. Park J.E., Tan H.S., Datta A., Lai R.C., Zhang H., Meng W., et al. Hypoxic tumor cell modulates its microenvironment to enhance angiogenic and metastatic potential by secretion of proteins and exosomes. Mol Cell Proteomics 2010, 9:1085-1099.
4. Kerr B.A., Miocinovic R., Smith A.K., Klein E.A., Byzova T.V. Comparison of tumor and microenvironment secretomes in plasma and in platelets during prostate cancer growth in a xenograft model. Neoplasia 2010, 12:388-396.
5. Larue L., Bellacosa A. Epithelial-mesenchymal transition in development and cancer: role of phosphatidylinositol 3'kinase/AKT pathways. Oncogene 2005, 24:7443-7454.
6. Zucker S., Vacirca J. Role of matrix metalloproteinases (MMPs) in colorectal cancer. Cancer Metastasis Rev 2004, 23:101-117.
7. Gocheva V., Wang H.W., Gadea B.B., Shree T., Hunter K.E., Garfall A.L., et al. IL-4 induces cathepsin protease activity in tumor-associated macrophages to promote cancer growth and invasion. Gene Dev 2010, 24:241-255.
8. Maestroni G., Hertens E., Galli P. Factor (s) from nonmacrophage bone marrow stromal cells inhibit Lewis lung carcinoma and B16 melanoma growth in mice. Cell Mol Life Sci 1999, 55:663-667.
9. Zhong L., Roybal J., Chaerkady R., Zhang W., Choi K., Alvarez C.A., et al. Identification of secreted proteins that mediate cell-cell interactions in an in vitro model of the lung cancer microenvironment. Cancer Res 2008, 68:7237-7245.
10. Makridakis M., Vlahou A. Secretome proteomics for discovery of cancer biomarkers. J Proteomics 2010, 73:2291-2305.
11. Xue H., Lu B., Lai M. The cancer secretome: a reservoir of biomarkers. J Transl Med 2008, 6:52-63.
12. Vona-Davis L., Rose D.P. Adipokines as endocrine, paracrine, and autocrine factors in breast cancer risk and progression. Endocr Relat Cancer 2007, 14:189-206.
13. Hogan C. Impact of interactions between normal and transformed epithelial cells and the relevance to cancer. Cell Mol Life Sci 2012, 69:203-213.
14. Brabletz T., Hlubek F., Spaderna S., Schmalhofer O., Hiendlmeyer E., Jung A., et al. Invasion and metastasis in colorectal cancer: epithelial-mesenchymal transition, mesenchymal-epithelial transition, stem cells and β-catenin. Cells Tissues Organs 2005, 179:56-65.
15. Van Cutsem E., Köhne C.H., Hitre E., Zaluski J., Chang Chien C.R., Makhson A., et al. Cetuximab and chemotherapy as initial treatment for metastatic colorectal cancer. N Engl J Med 2009, 360:1408-1417.
16. Eleni M., Eftychia O., Michal K., Ladislav A., Takehiko S., Senji S., et al. BRAF and RAS oncogenes regulate Rho GTPase pathways to mediate migration and invasion properties in human colon cancer cells: a comparative study. Mol Cancer 2011, 10:118-138.
17. Patsialou A., Wyckoff J., Wang Y., Goswami S., Stanley E.R., Condeelis J.S. Invasion of human breast cancer cells in vivo requires both paracrine and autocrine loops involving the colony-stimulating factor-1 receptor. Cancer Res 2009, 69:9498-9506.
18. Mann M. Functional and quantitative proteomics using SILAC. Nat Rev Mol Cell Biol 2006, 7:952-958.
19. Xu Y., Liang S., Shen G., Xu X., Liu Q., Xu Z., et al. Application of the SILAC (stable isotope labelling with amino acids in cell culture) technique in quantitative comparisons for tissue proteome expression. Biotechnol Appl Biochem 2009, 54:11-20.
20. Liang S., Xu Z., Xu X., Zhao X., Huang C., Wei Y. Quantitative proteomics for cancer biomarker discovery. Comb Chem High Throughput Screen 2012, 15:221-231.
21. Kuo Y.S., Tang Y.B., Lu T.Y., Wu H.C., Lin C.T. IGFBP-6 plays a role as an oncosuppressor gene in NPC pathogenesis through regulating EGR-1 expression. J Pathol 2010, 222:299-309.
22. He Z., Bateman A. Progranulin (granulin-epithelin precursor, PC-cell-derived growth factor, acrogranin) mediates tissue repair and tumorigenesis. J Mol Med 2003, 81:600-612.
23. Larriba M.J., Casado-Vela J., Pendás-Franco N., Peña R., de Herreros A.G., Berciano M.T., et al. Novel snail1 target proteins in human colon cancer identified by proteomic analysis. PLoS One 2010, 5:e10221.
24. Ben-Shmuel A., Shvab A., Gavert N., Brabletz T., Ben-Ze'ev A. Global analysis of L1-transcriptomes identified IGFBP-2 as a target of ezrin and NF-κB signaling that promotes colon cancer progression. Oncogene 2012, 10.1038/onc.2012.340.
25. Law A., Wong C.K. Stanniocalcin-2 promotes epithelial-mesenchymal transition and invasiveness in hypoxic human ovarian cancer cells. Exp Cell Res 2010, 316:3425-3434.
26. Vuoriluoto K., Haugen H., Kiviluoto S., Mpindi J., Nevo J., Gjerdrum C., et al. Vimentin regulates EMT induction by Slug and oncogenic H-Ras and migration by governing Axl expression in breast cancer. Oncogene 2010, 30:1436-1448.
27. Huet C., Sahuquillo-Merino C., Coudrier E., Louvard D. Absorptive and mucus-secreting subclones isolated from a multipotent intestinal cell line (HT-29) provide new models for cell polarity and terminal differentiation. J Cell Biol 1987, 105:345-357.
28. Moyer M.P., Manzano L.A., Merriman R.L., Stauffer J.S., Tanzer L.R. NCM460, a normal human colon mucosal epithelial cell line. In Vitro Cell Dev Biol Anim 1996, 32:315-317.
29. Liang S., Xu Y., Shen G., Liu Q., Zhao X., Xu Z., et al. Quantitative protein expression profiling of 14-3-3 isoforms in human renal carcinoma shows 14-3-3 epsilon is involved in limitedly increasing renal cell proliferation. Electrophoresis 2009, 30:4152-4162.
30. Liang S., Shen G., Liu Q., Xu Y., Zhou L., Xiao S., et al. Isoform-specific expression and characterization of 14-3-3 proteins in human glioma tissues discovered by stable isotope labeling with amino acids in cell culture-based proteomic analysis. Proteomics Clin Appl 2009, 3:743-753.
31. Zhou J., Liang S., Fang L., Chen L., Tang M., Xu Y., et al. Quantitative proteomic analysis of HepG2 cells treated with quercetin suggests IQGAP1 involved in quercetin-induced regulation of cell proliferation and migration. OMICS 2009, 13:93-103.
32. Liang S., Yu Y., Yang P., Gu S., Xue Y., Chen X. Analysis of the protein complex associated with 14-3-3 epsilon by a deuterated-leucine labeling quantitative proteomics strategy. J Chromatogr B 2009, 877:627-634.
33. Cox J., Michalski A., Mann M. Software lock mass by two-dimensional minimization of peptide mass errors. J Am Soc Mass Spectrom 2011, 22:1373-1380.
34. Cox J., Neuhauser N., Michalski A., Scheltema R.A., Olsen J.V., Mann M. Andromeda: a peptide search engine integrated into the MaxQuant environment. J Proteome Res 2011, 10:1794-1805.
35. He Y., Wu X., Liu X., Yan G., Xu C. LC- MS/MS analysis of ovarian cancer metastasis-related proteins using a nude mouse model: 14-3-3 zeta as a candidate biomarker. J Proteome Res 2010, 9:6180-6190.
36. Chan C.Y., Masui O., Krakovska O., Belozerov V.E., Voisin S., Ghanny S., et al. Identification of differentially regulated secretome components during skeletal myogenesis. Mol Cell Proteomics 2011, 10. [M110.004804].
37. Grønborg M., Kristiansen T.Z., Iwahori A., Chang R., Reddy R., Sato N., et al. Biomarker discovery from pancreatic cancer secretome using a differential proteomic approach. Mol Cell Proteomics 2006, 5:157-171.
38. Ong S.-E., Kratchmarova I., Mann M. Properties of 13C-substituted arginine in stable isotope labeling by amino acids in cell culture (SILAC). J Proteome Res 2003, 2:173-181.
39. Ling B., Liang S.-F., Xu Y.-H., Zhao X.-Y., Tang M.-H., Liu X.-Y., et al. Differential proteomic analysis of HeLa cells treated with Honokiol using a quantitative proteomic strategy. Amino Acids 2008, 35:115-122.
40. Subramaniam V., Gardner H., Jothy S. Soluble CD44 secretion contributes to the acquisition of aggressive tumor phenotype in human colon cancer cells. Exp Mol Pathol 2007, 83:341-346.
41. Montgomery N., Hill A., McFarlane S., Neisen J., O'Grady A., Conlon S., et al. CD44 enhances invasion of basal-like breast cancer cells by upregulating serine protease and collagen-degrading enzymatic expression and activity. Breast Cancer Res 2012, 14:R84.
42. Yeung T.M., Gandhi S.C., Wilding J.L., Muschel R., Bodmer W.F. Cancer stem cells from colorectal cancer-derived cell lines. Proc Natl Acad Sci 2010, 107:3722-3727.
43. Subramaniam V., Vincent I.R., Gardner H., Chan E., Dhamko H., Jothy S. CD44 regulates cell migration in human colon cancer cells via Lyn kinase and AKT phosphorylation. Exp Mol Pathol 2007, 83:207-215.
44. Strillacci A., Valerii M.C., Sansone P., Caggiano C., Sgromo A., Vittori L., et al. Loss of miR-101 expression promotes wnt/β-catenin signalling pathway activation and malignancy in colon cancer cells. J Pathol 2013, 229:379-389.
45. Cairns R.A., Harris I.S., Mak T.W. Regulation of cancer cell metabolism. Nat Rev Cancer 2011, 11:85-95.
46. Xu R., Pelicano H., Zhou Y., Carew J.S., Feng L., Bhalla K.N., et al. Inhibition of glycolysis in cancer cells: a novel strategy to overcome drug resistance associated with mitochondrial respiratory defect and hypoxia. Cancer Res 2005, 65:613-621.
47. Chiang K.P., Niessen S., Saghatelian A., Cravatt B.F. An enzyme that regulates ether lipid signaling pathways in cancer annotated by multidimensional profiling. Chem Biol 2006, 13:1041-1050.
48. Wallace H.M., Duthie J., Evans D.M., Lamond S., Nicoll K.M., Heys S.D. Alterations in polyamine catabolic enzymes in human breast cancer tissue. Clin Cancer Res 2000, 6:3657-3661.
49. Takasu S., Mutoh M., Takahashi M., Nakagama H. Lipoprotein lipase as a candidate target for cancer prevention/therapy. Biochem Res Int 2011, 2012:398697.
50. Kim Y.J. The role of peroxiredoxin 1 in lung cancer: tumor development and radiotherapy resistance 2009, State University of New York, Buffalo.
51. Kang S.Y., Halvorsen O.J., Gravdal K., Bhattacharya N., Lee J.M., Liu N.W., et al. Prosaposin inhibits tumor metastasis via paracrine and endocrine stimulation of stromal p53 and Tsp-1. Proc Natl Acad Sci 2009, 106:12115-12120.
52. Tsalavos S., Segklia K., Passa O., Petryk A., O'Connor M.B., Graf D. Involvement of twisted gastrulation in T cell-independent plasma cell production. J Immunol 2011, 186:6860-6870.
53. Cobianchi F., SenGupta D., Zmudzka B., Wilson S. Structure of rodent helix-destabilizing protein revealed by cDNA cloning. J Biol Chem 1986, 261:3536-3543.
54. Sachdev D., Yee D. The IGF system and breast cancer. Endocr Relat Cancer 2001, 8:197-209.
55. Kozlowski L., Wojtukiewicz M.Z., Ostrowska H. Cathepsin A activity in primary and metastatic human melanocytic tumors. Arch Dermatol Res 2000, 292:68-71.
56. Zhang Z., Neiva K.G., Lingen M.W., Ellis L.M., Nör J.E. VEGF-dependent tumor angiogenesis requires inverse and reciprocal regulation of VEGFR1 and VEGFR2. Cell Death Differ 2009, 17:499-512.
57. Moiola C., De Luca P., Gardner K., Vazquez E., De Siervi A. Cyclin T1 overexpression induces malignant transformation and tumor growth. Cell Cycle 2010, 9:3119-3126.
58. Li M., Aliotta J.M., Asara J.M., Wu Q., Dooner M.S., Tucker L.D., et al. Intercellular transfer of proteins as identified by stable isotope labeling of amino acids in cell culture. J Biol Chem 2010, 285:6285-6297.
59. Matsumura N., Mandai M., Miyanishi M., Fukuhara K., Baba T., Higuchi T., et al. Oncogenic property of acrogranin in human uterine leiomyosarcoma: direct evidence of genetic contribution in in vivo tumorigenesis. Clin Cancer Res 2006, 12:1402-1411.
60. De Muynck L., Van Damme P. Cellular effects of progranulin in health and disease. J Mol Neurosci 2011, 45:549-560.
61. Pieper F.R., Klundert F.A., Raats J.M., Henderik J.B., Schaart G., Ramaekers F.C., et al. Regulation of vimentin expression in cultured epithelial cells. Eur J Biochem 1992, 210:509-519.
62. Gilles C., Polette M., Zahm J.-M., Tournier J.-M., Volders L., Foidart J.-M., et al. Vimentin contributes to human mammary epithelial cell migration. J Cell Sci 1999, 112:4615-4625.
63. Samani A.A., Yakar S., LeRoith D., Brodt P. The role of the IGF system in cancer growth and metastasis: overview and recent insights. Endocr Rev 2007, 28:20-47.
64. Zhang C., Lu L., Li Y., Wang X., Zhou J., Liu Y., et al. IGF binding protein-6 expression in vascular endothelial cells is induced by hypoxia and plays a negative role in tumor angiogenesis. Int J Cancer 2012, 130:2003-2012.
65. Leng S.L., Leeding K.S., Whitehead R.H., Bach L.A. Insulin-like growth factor (IGF)-binding protein-6 inhibits IGF-II-induced but not basal proliferation and adhesion of LIM 1215 colon cancer cells. Mol Cell Endocrinol 2001, 174:121-127.
66. Whiteside T. The tumor microenvironment and its role in promoting tumor growth. Oncogene 2008, 27:5904-5912.
67. Sawant K.V., McMurray D.N. Guinea pig neutrophils infected with Mycobacterium tuberculosis produce cytokines which activate alveolar macrophages in noncontact cultures. Infect Immun 2007, 75:1870-1877.
68. Sundararaj K.P., Samuvel D.J., Li Y., Sanders J.J., Lopes-Virella M.F., Huang Y. Interleukin-6 released from fibroblasts is essential for up-regulation of matrix metalloproteinase-1 expression by U937 macrophages in coculture. J Biol Chem 2009, 284:13714-13724.
69. Mor-Vaknin N., Punturieri A., Sitwala K., Markovitz D.M. Vimentin is secreted by activated macrophages. Nat Cell Biol 2002, 5:59-63.
70. Liao X., Lochhead P., Nishihara R., Morikawa T., Kuchiba A., Yamauchi M., et al. Aspirin use, tumor PIK3CA mutation, and colorectal-cancer survival. N Engl J Med 2012, 367:1596-1606.
71. Taferner A., Micutkova L., Hermann M., Jansen-Dürr P., Pircher H. Purification and characterization of native human insulin-like growth factor binding protein-6. J Cell Commun Signal 2011, 5:277-289.
72. Kim E.J., Schaffer B.S., Kang Y.H., Macdonald R.G., Park J.H. Decreased production of insulin-like growth factor-binding protein (IGFBP)-6 by transfection of colon cancer cells with an antisense IGFBP-6 cDNA construct leads to stimulation of cell proliferation. J Gastroenterol Hepatol 2002, 17:563-570.