Changes on the Caco-2 secretome through differentiation analyzed by 2-D differential in-gel electrophoresis (DIGE)

International Journal of Molecular Sciences

Volumn 13, Issue 11, 2012, Pages 14401-14420

  García Lorenzo, Andrés ^a   Rodríguez Piñeiro, Ana M ^a,b   Rodríguez Berrocal, Francisco J ^a   de la Cadena, María Páez ^a   Martínez Zorzano, Vicenta S ^a  

^a UNIVERSITY OF VIGO   (Spain)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

Biomarkers; Caco 2; Colorectal cancer; Differentiation; DIGE; Secretome

Indexed keywords

BIOLOGICAL MARKER; NIEMANN PICK DISEASE TYPE C2 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1; TRANSLATIONALLY CONTROLLED TUMOR PROTEIN; TUMOR PROTEIN; UNCLASSIFIED DRUG; PROTEOME;

ARTICLE; CELL ASSAY; CELL DIFFERENTIATION; CELL STRAIN CACO 2; COLON ADENOCARCINOMA; COLON CARCINOGENESIS; CONTROLLED STUDY; DISEASE MARKER; FUNCTIONAL PROTEOMICS; HUMAN; HUMAN CELL; IN VITRO STUDY; MOLECULAR PATHOLOGY; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; TANDEM MASS SPECTROMETRY; TWO DIMENSIONAL DIFFERENCE GEL ELECTROPHORESIS; CACO 2 CELL LINE; CANCER GRADING; COLORECTAL TUMOR; METABOLISM; PATHOLOGY; PROCEDURES; PROTEOMICS;

BIOLOGICAL MARKERS; CACO-2 CELLS; COLORECTAL NEOPLASMS; HUMANS; NEOPLASM GRADING; PROTEOME; PROTEOMICS; TWO-DIMENSIONAL DIFFERENCE GEL ELECTROPHORESIS;

EID: 84870698552     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms131114401     Document Type: Article

References (66)

1. Schnekenburger, M.; Diederich, M. Epigenetics offer new horizons for colorectal cancer prevention. Curr. Colorectal Cancer Rep. 2012, 8, 66-81.
2. Søreide, K.; Nedrebo, B.S.; Knapp, J.C.; Glomsaker, T.B.; Søreide, J.A.; Korner, H. Evolving molecular classification by genomic and proteomic biomarkers in colorectal cancer: Potential implications for the surgical oncologist. Surg. Oncol. 2009, 18, 31-50.
3. Pinto, M.; Robin-Leon, S.; Appay, M.D.; Kedinger, M.; Triadou, N.; Dussaulx, E.; Lacroix, B.; Simon-Assman, P.; Haffen, K.; Fogh, J.; et al. Enterocyte-like differentiation and polarization of the human colon carcinoma cell line Caco-2 in culture. Biol. Cell. 1983, 47, 323-330.
4. Rousset, M.; Laburthe, M.; Pinto, M.; Chevalier, G.; Rouyer-Fessard, C.; Dussaulx, E.; Trugnan, G.; Boige, N.; Brun, J.L.; Zweibaum, A. Enterocytic differentiation and glucose utilization in the human colon tumor cell line Caco-2: Modulation by forskolin. J. Cell Physiol. 1985, 123, 377-385.
5. Stierum, R.; Gaspari, M.; Dommels, Y.; Ouatas, T.; Pluk, H.; Jespersen, S.; Vogels, J.; Verhoeckx, K.; Groten, J.; van Ommen, B. Proteome analysis reveals novel proteins associated with proliferation and differentiation of the colorectal cancer cell line Caco-2. Biochim. Biophys. Acta 2003, 1650, 73-91.
6. Buhrke, T.; Lengler, I.; Lampen, A. Analysis of proteomic changes induced upon cellular differentiation of the human intestinal cell line Caco-2. Dev. Growth. Differ. 2011, 53, 411-426.
7. Hauck, W.; Stanners, C.P. Control of carcinoembryonic antigen gene family expression in a differentiating colon carcinoma cell line, Caco-2. Cancer Res. 1991, 51, 3526-3533.
8. Volmer, M.W.; Radacz, Y.; Hahn, S.A.; Klein-Scory, S.; Stühler, K.; Zapatka, M.; Schmiegel, W.; Meyer, H.E.; Schwarte-Waldhoff, I. Tumor suppressor Smad4 mediates downregulation of the anti-adhesive invasion-promoting matricellular protein SPARC: Landscaping activity of Smad4 as revealed by a "secretome" analysis. Proteomics 2004, 4, 1324-1334.
9. Wu, C.C.; Chien, K.Y.; Tsang, N.M.; Chang, K.P.; Hao, S.P.; Tsao, C.H.; Chang, Y.S.; Yu, J.S. Cancer cell-secreted proteomes as a basis for searching potential tumor markers: Nasopharyngeal carcinoma as a model. Proteomics 2005, 5, 3173-3182.
10. Wu, C.C.; Chen, H.C.; Chen, S.J.; Liu, H.P.; Hsieh, Y.Y.; Yu, C.J.; Tang, R.; Hsieh, L.L.; Yu, J.S.; Chang, Y.S. Identification of collapsin response mediator protein-2 as a potential marker of colorectal carcinoma by comparative analysis of cancer cell secretomes. Proteomics 2008, 8, 316-332.
11. Tonge, R.; Shaw, J.; Middleton, B.; Rowlinson, R.; Rayner, S.; Young, J.; Pognan, F.; Hawkins, E.; Currie, I.; Davison, M. Validation and development of fluorescence two-dimensional differential gel electrophoresis proteomics technology. Proteomics 2001, 1, 377-396.
12. Alban, A.; David, S.O.; Bjorkesten, L.; Andersson, C.; Sloge, E.; Lewis, S.; Currie, I. A novel experimental design for comparative two-dimensional gel analysis: Two-dimensional difference gel electrophoresis incorporating a pooled internal standard. Proteomics 2003, 3, 36-44.
13. Unlü, M.; Morgan, M.E.; Minden, J.S. Difference gel electrophoresis: A single gel method for detecting changes in protein extracts. Electrophoresis 1997, 18, 2071-2077.
14. Friedman, D.B.; Hill, S.; Keller, J.W.; Merchant, N.B.; Levy, S.E.; Coffey, R.J.; Caprioli, R.M. Proteome analysis of human colon cancer by two-dimensional difference gel electrophoresis and mass spectrometry. Proteomics 2004, 4, 793-811.
15. Alfonso, P.; Núñez, A.; Madoz-Gurpide, J.; Lombardia, L.; Sánchez, L.; Casal, J.I. Proteomic expression analysis of colorectal cancer by two-dimensional differential gel electrophoresis. Proteomics 2005, 5, 2602-2611.
16. Rodríguez-Piñeiro, A.M.; Rodríguez-Berrocal, F.J.; Páez de la Cadena, M. Detection of proteins altered in serum of patients with colorectal cancer by differential in-gel electrophoresis. Revista Real Academia Galega de Ciencias 2006, XXV, 5-25.
17. Seike, M.; Kondo, T.; Fujii, K.; Yamada, T.; Gemma, A.; Kudoh, S.; Hirohashi, S. Proteomic signature of human cancer cells. Proteomics 2004, 4, 2776-2788.
18. Corbo, C.; Orrù, S.; Gemei, M.; Noto, R.D.; Mirabelli, P.; Imperlini, E.; Ruoppolo, M.; Vecchio, L.D.; Salvatore, F. Protein cross-talk in CD133+ colon cancer cells indicates activation of the Wnt pathway and upregulation of SRp20 that is potentially involved in tumorigenicity. Proteomics 2012, 12, 2045-2059.
19. Zeiser, J.J.; Klodmann, J.; Braun, H.P.; Gerhard, R.; Just, I.; Pich, A. Effects of Clostridium difficile Toxin A on the proteome of colonocytes studied by differential 2D electrophoresis. J. Proteomics 2011, 75, 469-479.
20. Turck, N.; Richert, S.; Gendry, P.; Stutzmann, J.; Kedinger, M.; Leize, E.; Simon-Assmann, P.; Van Dorsselaer, A.; Launay, J.F. Proteomic analysis of nuclear proteins from proliferative and differentiated human colonic intestinal epithelial cells. Proteomics 2004, 4, 93-105.
21. Pshezhetsky, A.V.; Fedjaev, M.; Ashmarina, L.; Mazur, A.; Budman, L.; Sinnett, D.; Labuda, D.; Beaulieu, J.F.; Ménard, D.; Nifant'ev, I.; et al. Subcellular proteomics of cell differentiation: Quantitative analysis of the plasma membrane proteome of Caco-2 cells. Proteomics 2007, 7, 2201-2215.
22. Mariadason, J.M.; Arango, D.; Corner, G.A.; Arañes, M.J.; Hotchkiss, K.A.; Yang, W.; Augenlicht, L.H. A gene expression profile that defines colon cell maturation in vitro. Cancer Res. 2002, 62, 4791-4804.
23. Tremblay, E.; Auclair, J.; Delvin, E.; Levy, E.; Ménard, D.; Pshezhetsky, A.V.; Rivard, N.; Seidman, E.G.; Sinnett, D.; Vachon, P.H.; et al. Gene expression profiles of normal proliferating and differentiating human intestinal epithelial cells: A comparison with the Caco-2 cell model. J. Cell. Biochem. 2006, 99, 1175-1186.
24. Volmer, M.W.; Stühler, K.; Zapatka, M.; Schöneck, A.; Klein-Scory, S.; Schmiegel, W.; Meyer, H.E.; Schwarte-Waldhoff, I. Differential proteome analysis of conditioned media to detect Smad4 regulated secreted biomarkers in colon cancer. Proteomics 2005, 5, 2587-2601.
25. Xue, H.; Lü, B.; Zhang, J.; Wu, M.; Huang, Q.; Wu, Q.; Sheng, H.; Wu, D.; Hu, J.; Lai, M. Identification of serum biomarkers for colorectal cancer metastasis using a differential secretome approach. J. Proteome Res. 2010, 9, 545-555.
26. Mbeunkui, F.; Metge, B.J.; Shevde, L.A.; Pannell, L.K. Identification of differentially secreted biomarkers using LC-MS/MS in isogenic cell lines representing a progression of breast cancer. J. Proteome Res. 2007, 6, 2993-3002.
27. Ji, H.; Greening, D.W.; Kapp, E.A.; Moritz, R.L.; Simpson, R.J. Secretome-based proteomics reveals sulindac-modulated proteins released from colon cancer cells. Proteomics Clin. Appl. 2009, 3, 433-451.
28. Yenofsky, R.; Cereghini, S.; Krowczynska, A.; Brawerman, G. Regulation of mRNA utilization in mouse erythroleukemia cells induced to differentiate by exposure to dimethyl sulfoxide. Mol. Cell. Biol. 1983, 3, 1197-1203.
29. Nagano-Ito, M.; Ichikawa, S. Biological effects of Mammalian translationally controlled tumor protein (TCTP) on cell death, proliferation, and tumorigenesis. Biochem. Res. Int. 2012, 2012, 204960-204966.
30. MacDonald, S.M.; Paznekas, W.A.; Jabs, E.W. Chromosomal localization of tumor protein, translationally-controlled 1 (TPT1) encoding the human histamine releasing factor (HRF) to 13q12→q14. Cytogenet. Cell. Genet. 1999, 84, 128-129.
31. Arcuri, F.; Papa, S.; Carducci, A.; Romagnoli, R.; Liberatori, S.; Riparbelli, M.G.; Sanchez, J.C.; Tosi, P.; del Vecchio, M.T. Translationally controlled tumor protein (TCTP) in the human prostate and prostate cancer cells: Expression, distribution, and calcium binding activity. Prostate 2004, 60, 130-140.
32. Li, F.; Zhang, D.; Fujise, K. Characterization of fortilin, a novel antiapoptotic protein. J. Biol. Chem. 2001, 276, 47542-47549.
33. Teshima, S.; Rokutan, K.; Nikawa, T.; Kishi, K. Macrophage colony-stimulating factor stimulates synthesis and secretion of a mouse homolog of a human IgE-dependent histamine-releasing factor by macrophages in vitro and in vivo. J. Immunol. 1998, 161, 6356-6366.
34. Amzallag, N.; Passer, B.J.; Allanic, D.; Segura, E.; Théry, C.; Goud, B.; Amson, R.; Telerman, A. TSAP6 facilitates the secretion of translationally controlled tumor protein/histamine-releasing factor via a nonclassical pathway. Biol. Chem. 2004, 279, 46104-46112.
35. Chung, S.; Kim, M.; Choi, W.J.; Chung, J.K.; Lee, K. Expression of translationally controlled tumor protein mRNA in human colon cancer. Cancer Lett. 2000, 156, 185-190.
36. Ma, Q.; Geng, Y.; Xu, W.; Wu, Y.; He, F.; Shu, W.; Huang, M.; Du, H.; Li, M. The role of translationally controlled tumor protein in tumor growth and metastasis of colon adenocarcinoma cells. J. Proteome Res. 2010, 9, 40-49.
37. Skonier, J.; Neubauer, M.; Madisen, L.; Bennett, K.; Plowman, G.D.; Purchio, A.F. cDNA cloning and sequence analysis of beta ig-h3, a novel gene induced in a human adenocarcinoma cell line after treatment with transforming growth factor-beta. DNA Cell Biol. 1992, 11, 511-522.
38. Skonier, J.; Bennett, K.; Rothwell, V.; Kosowski, S.; Plowman, G.; Wallace, P.; Edelhoff, S.; Disteche, C.; Neubauer, M.; Marquardt, H. Beta ig-h3: A transforming growth factor-beta-responsive gene encoding a secreted protein that inhibits cell attachment in vitro and suppresses the growth of CHO cells in nude mice. DNA Cell Biol. 1994, 13, 571-584.
39. Thapa, N.; Lee, B.H.; Kim, I.S. TGFBIp/betaig-h3 protein: A versatile matrix molecule induced by TGF-beta. Int. J. Biochem. Cell Biol. 2007, 39, 2183-2194.
40. Kitahara, O.; Furukawa, Y.; Tanaka, T.; Kihara, C.; Ono, K.; Yanagawa, R.; Nita, M.E.; Takagi, T.; Nakamura, Y.; Tsunoda, T. Alterations of gene expression during colorectal carcinogenesis revealed by cDNA microarrays after laser-capture microdissection of tumor tissues and normal epithelia. Cancer Res. 2001, 61, 3544-3559.
41. Buckhaults, P.; Rago, C.; St Croix, B.; Romans, K.E.; Saha, S.; Zhang, L.; Vogelstein, B.; Kinzler, K.W. Secreted and cell surface genes expressed in benign and malignant colorectal tumors. Cancer Res. 2001, 61, 6996-7001.
42. Roessler, M.; Rollinger, W.; Palme, S.; Hagmann, M.L.; Berndt, P.; Engel, A.M.; Schneidinger, B.; Pfeffer, M.; Andres, H.; Karl, J.; et al. Identification of nicotinamide N-methyltransferase as a novel serum tumor marker for colorectal cancer. Clin. Cancer Res. 2005, 11, 6550-6557.
43. Ma, C.; Rong, Y.; Radiloff, D.R.; Datto, M.B.; Centeno, B.; Bao, S.; Cheng, A.W.; Lin, F.; Jiang, S.; Yeatman, T.J.; et al. Extracellular matrix protein betaig-h3/TGFBI promotes metastasis of colon cancer by enhancing cell extravasation. Genes Dev. 2008, 22, 308-321.
44. Chang, Y.T.; Wu, C.C.; Shyr, Y.M.; Chen, T.C.; Hwang, T.L.; Yeh, T.S.; Chang, K.P.; Liu, H.P.; Liu, Y.L.; Tsai, M.H.; et al. Secretome-based identification of ULBP2 as a novel serum marker for pancreatic cancer detection. PLoS One 2011, 6, e20029.
45. Naureckiene, S.; Sleat, D.E.; Lackland, H.; Fensom, A.; Vanier, M.T.; Wattiaux, R.; Jadot, M.; Lobel, P. Identification of HE1 as the second gene of Niemann-Pick C disease. Science 2000, 290, 2298-2301.
46. Larsen, L.B.; Ravn, P.; Boisen, A.; Berglund, L.; Petersen, T.E. Primary structure of EPV20, a secretory glycoprotein containing a previously uncharacterized type of domain. Eur. J. Biochem. 1997, 243, 437-441.
47. Kirchhoff, C.; Osterhoff, C.; Young, L. Molecular cloning and characterization of HE1, a major secretory protein of the human epididymis. Biol. Reprod. 1996, 54, 847-856.
48. Klein, A.; Amigo, L.; Retamal, M.J.; Morales, M.G.; Miquel, J.F.; Rigotti, A.; Zanlungo, S. NPC2 is expressed in human and murine liver and secreted into bile: Potential implications for body cholesterol homeostasis. Hepatology 2006, 43, 126-133.
49. Storch, J.; Xu, Z. Niemann-Pick C2 (NPC2) and intracellular cholesterol trafficking. Biochim. Biophys. Acta 2009, 1791, 671-678.
50. Heo, K.; Jariwala, U.; Woo, J.; Zhan, Y.; Burke, K.A.; Zhu, L.; Anderson, W.F.; Zhao, Y. Involvement of Niemann-Pick type C2 protein in hematopoiesis regulation. Stem Cells 2006, 24, 1549-1555.
51. Schrantz, N.; Sagiv, Y.; Liu, Y.; Savage, P.B.; Bendelac, A.; Teyton, L. The Niemann-Pick type C2 protein loads isoglobotrihexosylceramide onto CD1d molecules and contributes to the thymic selection of NKT cells. J. Exp. Med. 2007, 204, 841-852.
52. Csepeggi, C.; Jiang, M.; Frolov, A. Somatic cell plasticity and Niemann-Pick type C2 protein: Adipocyte differentiation and function. J. Biol. Chem. 2010, 285, 30347-30354.
53. Csepeggi, C.; Jiang, M.; Kojima, F.; Crofford, L.J.; Frolov, A. Somatic cell plasticity and Niemann-Pick type C2protein. J. Biol. Chem. 2011, 286, 2078-2087.
54. McDonald, S.L.; Edington, H.D.; Kirkwood, J.M.; Becker, D. Expression analysis of genes identified by molecular profiling of VGP melanomas and MGP melanoma-positive lymph nodes. Cancer Biol. Ther. 2004, 3, 110-120.
55. Van Niel, G.; Raposo, G.; Candalh, C.; Boussac, M.; Hershberg, R.; Cerf-Bensussan, N.; Heyman, M. Intestinal epithelial cells secrete exosome-like vesicles. Gastroenterology 2001, 121, 337-349.
56. Pang, B.; Zhang, H.; Wang, J.; Chen, W.Z.; Li, S.H.; Shi, Q.G.; Liang, R.X.; Xie, B.X.; Wu, R.Q.; Qian, X.L.; et al. Ubiquitous mitochondrial creatine kinase is overexpressed in the conditioned medium and the extract of LNCaP lineaged androgen independent cell lines and facilitates prostate cancer progression. Prostate 2009, 69, 1176-1187.
57. Engstrom, L. Alkaline and acid phosphatase. In Preparative Centrifugation. A Practical Approach; Rickwood, D., Hames, B.D., Eds.; IRL Press: Oxford, UK, 1992; p. 375.
58. Dahlqvist, A. Assay of intestinal disaccharidases. Scand. J. Clin. Lab. Invest. 1984, 44, 169-172.
59. Trinder, P. Determination of blood glucose using an oxidase-peroxidase system with a non-carcinogenic chromogen. J. Clin. Pathol. 1969, 22, 158-161.
60. Trinder, P. Determination of blood glucose using 4-amino phenazone as oxygen acceptor. J. Clin. Pathol. 1969, 22, 246.
61. Bradford, M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72, 248-254.
62. Beyer, E.; Ivleva, T.; Artykova, G.; Wiederschain, G. Change of isoforms' spectra of alpha-L-fucosidase from human skin fibroblasts in intracellular storage of non hydrolyzable substances. Biochim. Biophys. Acta 1995, 1270, 7-11.
63. Laemmli, U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227, 680-685.
64. Ramagli, L.S.; Rodriguez, V.S. Quantitation of microgram amounts of protein in two-dimensional polyacrylamide gel electrophoresis sample buffer. Electrophoresis 1985, 6, 559-563.
65. Rodríguez-Piñeiro, A.M.; Rodríguez-Berrocal, F.J.; Páez de la Cadena, M. Improvements in the search for potential biomarkers by proteomics: Application of principal component and discriminant analyses for two-dimensional maps evaluation. J. Chromatogr. B 2007, 849, 251-260.
66. Bendtsen, J.D.; Jensen, L.J.; Blom, N.; Von Heijne, G.; Brunak, S. Feature-based prediction of non-classical and leaderless protein secretion. Protein Eng. Des. Sel. 2004, 17, 349-356.