Personalized Proteome Profiles of Healthy and Tumor Human Colon Organoids Reveal Both Individual Diversity and Basic Features of Colorectal Cancer

Cell Reports

Volumn 18, Issue 1, 2017, Pages 263-274

  Cristobal, Alba ^a,b   van den Toorn, Henk W P ^a,b   van de Wetering, Marc ^c   Clevers, Hans ^c,d   Heck, Albert J R ^a,b   Mohammed, Shabaz ^a,b,e,f  

^a UTRECHT UNIVERSITY   (Netherlands)

^b NETHERLANDS PROTEOMICS CENTRE   (Netherlands)

^c University Medical Center Utrecht Princess Máxima Center for Pediatric Oncology   (Netherlands)

^d UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^e UNIVERSITY OF OXFORD   (United Kingdom)

^f UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

colorectal cancer; mass spectrometry; organoids; proteomics

Indexed keywords

PROTEOME; TRANSCRIPTOME;

ADULT; AGED; ARTICLE; CLINICAL ARTICLE; COLON CARCINOGENESIS; COLORECTAL CANCER; CONTROLLED STUDY; CYTOPLASM; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIMIT OF QUANTITATION; MALE; MICROSATELLITE INSTABILITY; MIDDLE AGED; PERSONALIZED MEDICINE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEOMICS; TANDEM MASS SPECTROMETRY; ULTRA PERFORMANCE LIQUID CHROMATOGRAPHY; VERY ELDERLY; COLON; COLORECTAL TUMOR; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC VARIATION; GENETICS; METABOLISM; ORGANOID; PATHOLOGY; PROCEDURES; WNT SIGNALING;

COLON; COLORECTAL NEOPLASMS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENETIC VARIATION; HUMANS; ORGANOIDS; PROTEOME; PROTEOMICS; TRANSCRIPTOME; WNT SIGNALING PATHWAY;

EID: 85009076629     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.12.016     Document Type: Article

References (83)

1. Abbott, A., Cell culture: biology's new dimension. Nature 424 (2003), 870–872.
2. Altelaar, A.F.M., Munoz, J., Heck, A.J.R., Next-generation proteomics: towards an integrative view of proteome dynamics. Nat. Rev. Genet. 14 (2013), 35–48.
3. Baker, S.J., Fearon, E.R., Nigro, J.M., Hamilton, S.R., Preisinger, A.C., Jessup, J.M., vanTuinen, P., Ledbetter, D.H., Barker, D.F., Nakamura, Y., et al. Chromosome 17 deletions and p53 gene mutations in colorectal carcinomas. Science 244 (1989), 217–221.
4. Ballesta, A.M., Molina, R., Filella, X., Jo, J., Giménez, N., Carcinoembryonic antigen in staging and follow-up of patients with solid tumors. Tumour Biol. 16 (1995), 32–41.
5. Bardelli, A., Parsons, D.W., Silliman, N., Ptak, J., Szabo, S., Saha, S., Markowitz, S., Willson, J.K., Parmigiani, G., Kinzler, K.W., et al. Mutational analysis of the tyrosine kinome in colorectal cancers. Science, 300, 2003, 949.
6. Barker, N., van Es, J.H., Kuipers, J., Kujala, P., van den Born, M., Cozijnsen, M., Haegebarth, A., Korving, J., Begthel, H., Peters, P.J., Clevers, H., Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449 (2007), 1003–1007.
7. Barker, N., van de Wetering, M., Clevers, H., The intestinal stem cell. Genes Dev. 22 (2008), 1856–1864.
8. Barker, N., Ridgway, R.A., van Es, J.H., van de Wetering, M., Begthel, H., van den Born, M., Danenberg, E., Clarke, A.R., Sansom, O.J., Clevers, H., Crypt stem cells as the cells-of-origin of intestinal cancer. Nature 457 (2009), 608–611.
9. Barker, N., van Oudenaarden, A., Clevers, H., Identifying the stem cell of the intestinal crypt: strategies and pitfalls. Cell Stem Cell 11 (2012), 452–460.
10. Boersema, P.J., Raijmakers, R., Lemeer, S., Mohammed, S., Heck, A.J., Multiplex peptide stable isotope dimethyl labeling for quantitative proteomics. Nat. Protoc. 4 (2009), 484–494.
11. Boj, S.F., Hwang, C.I., Baker, L.A., Chio, I.I., Engle, D.D., Corbo, V., Jager, M., Ponz-Sarvise, M., Tiriac, H., Spector, M.S., et al. Organoid models of human and mouse ductal pancreatic cancer. Cell 160 (2015), 324–338.
12. Bos, J.L., Fearon, E.R., Hamilton, S.R., Verlaan-de Vries, M., van Boom, J.H., van der Eb, A.J., Vogelstein, B., Prevalence of ras gene mutations in human colorectal cancers. Nature 327 (1987), 293–297.
13. Chen, S., Chen, Y., Hu, C., Jing, H., Cao, Y., Liu, X., Association of clinicopathological features with UbcH10 expression in colorectal cancer. J. Cancer Res. Clin. Oncol. 136 (2010), 419–426.
14. Clevers, H., Modeling Development and Disease with Organoids. Cell 165 (2016), 1586–1597.
15. Collins, C., Rommens, J.M., Kowbel, D., Godfrey, T., Tanner, M., Hwang, S.I., Polikoff, D., Nonet, G., Cochran, J., Myambo, K., et al. Positional cloning of ZNF217 and NABC1: genes amplified at 20q13.2 and overexpressed in breast carcinoma. Proc. Natl. Acad. Sci. USA 95 (1998), 8703–8708.
16. Correa, R.G., de Carvalho, A.F., Pinheiro, N.A., Simpson, A.J., de Souza, S.J., NABC1 (BCAS1): alternative splicing and downregulation in colorectal tumors. Genomics 65 (2000), 299–302.
17. Cox, J., Mann, M., MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26 (2008), 1367–1372.
18. Cox, J., Mann, M., Quantitative, high-resolution proteomics for data-driven systems biology. Annu. Rev. Biochem. 80 (2011), 273–299.
19. Cravatt, B.F., Simon, G.M., Yates, J.R. 3rd, The biological impact of mass-spectrometry-based proteomics. Nature 450 (2007), 991–1000.
20. Daniels, D.L., Weis, W.I., Beta-catenin directly displaces Groucho/TLE repressors from Tcf/Lef in Wnt-mediated transcription activation. Nat. Struct. Mol. Biol. 12 (2005), 364–371.
21. de Wit, M., Kant, H., Piersma, S.R., Pham, T.V., Mongera, S., van Berkel, M.P., Boven, E., Pontén, F., Meijer, G.A., Jimenez, C.R., Fijneman, R.J., Colorectal cancer candidate biomarkers identified by tissue secretome proteome profiling. J. Proteomics 99 (2014), 26–39.
22. Drost, J., van Jaarsveld, R.H., Ponsioen, B., Zimberlin, C., van Boxtel, R., Buijs, A., Sachs, N., Overmeer, R.M., Offerhaus, G.J., Begthel, H., et al. Sequential cancer mutations in cultured human intestinal stem cells. Nature 521 (2015), 43–47.
23. Fearon, E.R., Molecular genetics of colorectal cancer. Annu. Rev. Pathol. 6 (2011), 479–507.
24. Fearon, E.R., Vogelstein, B., A genetic model for colorectal tumorigenesis. Cell 61 (1990), 759–767.
25. Ferreira, A.M., Tuominen, I., van Dijk-Bos, K., Sanjabi, B., van der Sluis, T., van der Zee, A.G., Hollema, H., Zazula, M., Sijmons, R.H., Aaltonen, L.A., et al. High frequency of RPL22 mutations in microsatellite-unstable colorectal and endometrial tumors. Hum. Mutat. 35 (2014), 1442–1445.
26. Frese, C.K., Altelaar, A.F., Hennrich, M.L., Nolting, D., Zeller, M., Griep-Raming, J., Heck, A.J., Mohammed, S., Improved peptide identification by targeted fragmentation using CID, HCD and ETD on an LTQ-Orbitrap Velos. J. Proteome Res. 10 (2011), 2377–2388.
27. Fujita, T., Ikeda, H., Taira, N., Hatoh, S., Naito, M., Doihara, H., Overexpression of UbcH10 alternates the cell cycle profile and accelerate the tumor proliferation in colon cancer. BMC Cancer, 9, 2009, 87.
28. Funakoshi, S., Ezaki, T., Kong, J., Guo, R.J., Lynch, J.P., Repression of the desmocollin 2 gene expression in human colon cancer cells is relieved by the homeodomain transcription factors Cdx1 and Cdx2. Mol. Cancer Res. 6 (2008), 1478–1490.
29. Gao, D., Vela, I., Sboner, A., Iaquinta, P.J., Karthaus, W.R., Gopalan, A., Dowling, C., Wanjala, J.N., Undvall, E.A., Arora, V.K., et al. Organoid cultures derived from patients with advanced prostate cancer. Cell 159 (2014), 176–187.
30. Gay, F., Estornes, Y., Saurin, J.C., Joly-Pharaboz, M.O., Friederich, E., Scoazec, J.Y., Abello, J., In colon carcinogenesis, the cytoskeletal protein gelsolin is down-regulated during the transition from adenoma to carcinoma. Hum. Pathol. 39 (2008), 1420–1430.
31. Gryfe, R., Kim, H., Hsieh, E.T., Aronson, M.D., Holowaty, E.J., Bull, S.B., Redston, M., Gallinger, S., Tumor microsatellite instability and clinical outcome in young patients with colorectal cancer. N. Engl. J. Med. 342 (2000), 69–77.
32. Halvey, P.J., Zhang, B., Coffey, R.J., Liebler, D.C., Slebos, R.J., Proteomic consequences of a single gene mutation in a colorectal cancer model. J. Proteome Res. 11 (2012), 1184–1195.
33. Hampel, H., Frankel, W.L., Martin, E., Arnold, M., Khanduja, K., Kuebler, P., Nakagawa, H., Sotamaa, K., Prior, T.W., Westman, J., et al. Screening for the Lynch syndrome (hereditary nonpolyposis colorectal cancer). N. Engl. J. Med. 352 (2005), 1851–1860.
34. Haugen, A.C., Goel, A., Yamada, K., Marra, G., Nguyen, T.P., Nagasaka, T., Kanazawa, S., Koike, J., Kikuchi, Y., Zhong, X., et al. Genetic instability caused by loss of MutS homologue 3 in human colorectal cancer. Cancer Res. 68 (2008), 8465–8472.
35. Hedberg Oldfors, C., Dios, D.G., Linder, A., Visuttijai, K., Samuelson, E., Karlsson, S., Nilsson, S., Behboudi, A., Analysis of an independent tumor suppressor locus telomeric to Tp53 suggested Inpp5k and Myo1c as novel tumor suppressor gene candidates in this region. BMC Genet., 16, 2015, 80.
36. Hemminki, A., Peltomäki, P., Mecklin, J.P., Järvinen, H., Salovaara, R., Nyström-Lahti, M., de la Chapelle, A., Aaltonen, L.A., Loss of the wild type MLH1 gene is a feature of hereditary nonpolyposis colorectal cancer. Nat. Genet. 8 (1994), 405–410.
37. Hendriks, Y.M.C., Jagmohan-Changur, S., van der Klift, H.M., Morreau, H., van Puijenbroek, M., Tops, C., van Os, T., Wagner, A., Ausems, M.G., Gomez, E., et al. Heterozygous mutations in PMS2 cause hereditary nonpolyposis colorectal carcinoma (Lynch syndrome). Gastroenterology 130 (2006), 312–322.
38. Jimenez, C.R., Fijneman, R.J.A., Proteomics of colorectal cancer in a genomic context: first large-scale mass spectrometry-based analysis from The Cancer Genome Atlas. Clin. Chem. 61 (2015), 1126–1128.
39. Käll, L., Canterbury, J.D., Weston, J., Noble, W.S., MacCoss, M.J., Semi-supervised learning for peptide identification from shotgun proteomics datasets. Nat. Methods 4 (2007), 923–925.
40. Karthaus, W.R., Iaquinta, P.J., Drost, J., Gracanin, A., van Boxtel, R., Wongvipat, J., Dowling, C.M., Gao, D., Begthel, H., Sachs, N., et al. Identification of multipotent luminal progenitor cells in human prostate organoid cultures. Cell 159 (2014), 163–175.
41. Khan, K., Hardy, R., Haq, A., Ogunbiyi, O., Morton, D., Chidgey, M., Desmocollin switching in colorectal cancer. Br. J. Cancer 95 (2006), 1367–1370.
42. Kim, N.-G., Rhee, H., Li, L.S., Kim, H., Lee, J.S., Kim, J.H., Kim, N.K., Kim, H., Identification of MARCKS, FLJ11383 and TAF1B as putative novel target genes in colorectal carcinomas with microsatellite instability. Oncogene 21 (2002), 5081–5087.
43. Larance, M., Lamond, A.I., Multidimensional proteomics for cell biology. Nat. Rev. Mol. Cell Biol. 16 (2015), 269–280.
44. Leushacke, M., Barker, N., Ex vivo culture of the intestinal epithelium: strategies and applications. Gut 63 (2014), 1345–1354.
45. Markowitz, S.D., Bertagnolli, M.M., Molecular origins of cancer: molecular basis of colorectal cancer. N. Engl. J. Med. 361 (2009), 2449–2460.
46. Markowitz, S., Wang, J., Myeroff, L., Parsons, R., Sun, L., Lutterbaugh, J., Fan, R.S., Zborowska, E., Kinzler, K.W., Vogelstein, B., et al. Inactivation of the type II TGF-beta receptor in colon cancer cells with microsatellite instability. Science 268 (1995), 1336–1338.
47. Marshman, E., Booth, C., Potten, C.S., The intestinal epithelial stem cell. BioEssays 24 (2002), 91–98.
48. Matsuyama, T., Ishikawa, T., Mogushi, K., Yoshida, T., Iida, S., Uetake, H., Mizushima, H., Tanaka, H., Sugihara, K., MUC12 mRNA expression is an independent marker of prognosis in stage II and stage III colorectal cancer. Int. J. Cancer 127 (2010), 2292–2299.
49. Morin, P.J., Sparks, A.B., Korinek, V., Barker, N., Clevers, H., Vogelstein, B., Kinzler, K.W., Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC. Science 275 (1997), 1787–1790.
50. Muñoz, J., Stange, D.E., Schepers, A.G., van de Wetering, M., Koo, B.K., Itzkovitz, S., Volckmann, R., Kung, K.S., Koster, J., Radulescu, S., et al. The Lgr5 intestinal stem cell signature: robust expression of proposed quiescent ‘+4′ cell markers. EMBO J. 31 (2012), 3079–3091.
51. Ohmachi, T., Inoue, H., Mimori, K., Tanaka, F., Sasaki, A., Kanda, T., Fujii, H., Yanaga, K., Mori, M., Fatty acid binding protein 6 is overexpressed in colorectal cancer. Clin. Cancer Res. 12 (2006), 5090–5095.
52. Ohta, Y., Sato, T., Intestinal tumor in a dish. Front Med (Lausanne), 1, 2014, 14.
53. Packer, L.M., Williams, S.J., Callaghan, S., Gotley, D.C., McGuckin, M.A., Expression of the cell surface mucin gene family in adenocarcinomas. Int. J. Oncol. 25 (2004), 1119–1126.
54. Plaschke, J., Krüger, S., Jeske, B., Theissig, F., Kreuz, F.R., Pistorius, S., Saeger, H.D., Iaccarino, I., Marra, G., Schackert, H.K., Loss of MSH3 protein expression is frequent in MLH1-deficient colorectal cancer and is associated with disease progression. Cancer Res. 64 (2004), 864–870.
55. Powell, S.M., Zilz, N., Beazer-Barclay, Y., Bryan, T.M., Hamilton, S.R., Thibodeau, S.N., Vogelstein, B., Kinzler, K.W., APC mutations occur early during colorectal tumorigenesis. Nature 359 (1992), 235–237.
56. Raynes, D.A., Graner, M.W., Bagatell, R., McLellan, C., Guerriero, V., Increased expression of the Hsp70 cochaperone HspBP1 in tumors. Tumour Biol. 24 (2004), 281–285.
57. Richards, A.L., Merrill, A.E., Coon, J.J., Proteome sequencing goes deep. Curr. Opin. Chem. Biol. 24 (2015), 11–17.
58. Rodrigues, N.R., Rowan, A., Smith, M.E., Kerr, I.B., Bodmer, W.F., Gannon, J.V., Lane, D.P., p53 mutations in colorectal cancer. Proc. Natl. Acad. Sci. USA 87 (1990), 7555–7559.
59. Roose, J., Molenaar, M., Peterson, J., Hurenkamp, J., Brantjes, H., Moerer, P., van de Wetering, M., Destrée, O., Clevers, H., The Xenopus Wnt effector XTcf-3 interacts with Groucho-related transcriptional repressors. Nature 395 (1998), 608–612.
60. Rubinfeld, B., Souza, B., Albert, I., Müller, O., Chamberlain, S.H., Masiarz, F.R., Munemitsu, S., Polakis, P., Association of the APC gene product with beta-catenin. Science 262 (1993), 1731–1734.
61. Sato, T., Vries, R.G., Snippert, H.J., van de Wetering, M., Barker, N., Stange, D.E., van Es, J.H., Abo, A., Kujala, P., Peters, P.J., Clevers, H., Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459 (2009), 262–265.
62. Sato, T., Stange, D.E., Ferrante, M., Vries, R.G., Van Es, J.H., Van den Brink, S., Van Houdt, W.J., Pronk, A., Van Gorp, J., Siersema, P.D., Clevers, H., Long-term expansion of epithelial organoids from human colon, adenoma, adenocarcinoma, and Barrett's epithelium. Gastroenterology 141 (2011), 1762–1772.
63. Schwanhäusser, B., Busse, D., Li, N., Dittmar, G., Schuchhardt, J., Wolf, J., Chen, W., Selbach, M., Global quantification of mammalian gene expression control. Nature 473 (2011), 337–342.
64. Sinicrope, F.A., Sargent, D.J., Molecular pathways: microsatellite instability in colorectal cancer: prognostic, predictive, and therapeutic implications. Clin. Cancer Res. 18 (2012), 1506–1512.
65. Sirvent, A., Vigy, O., Orsetti, B., Urbach, S., Roche, S., Analysis of SRC oncogenic signaling in colorectal cancer by stable isotope labeling with heavy amino acids in mouse xenografts. Mol. Cell. Proteomics 11 (2012), 1937–1950.
66. Spivak, M., Weston, J., Bottou, L., Käll, L., Noble, W.S., Improvements to the percolator algorithm for Peptide identification from shotgun proteomics data sets. J. Proteome Res. 8 (2009), 3737–3745.
67. Surinova, S., Radová, L., Choi, M., Srovnal, J., Brenner, H., Vitek, O., Hajdúch, M., Aebersold, R., Non-invasive prognostic protein biomarker signatures associated with colorectal cancer. EMBO Mol. Med. 7 (2015), 1153–1165.
68. Surinova, S., Choi, M., Tao, S., Schüffler, P.J., Chang, C.Y., Clough, T., Vysloužil, K., Khoylou, M., Srovnal, J., Liu, Y., et al. Prediction of colorectal cancer diagnosis based on circulating plasma proteins. EMBO Mol. Med. 7 (2015), 1166–1178.
69. Tanner, K., Gottesman, M.M., Beyond 3D culture models of cancer. Sci. Transl. Med., 7, 2015, 283ps9.
70. Thompson, J., Zimmermann, W., Nollau, P., Neumaier, M., Weber-Arden, J., Schrewe, H., Craig, I., Willcocks, T., CGM2, a member of the carcinoembryonic antigen gene family is down-regulated in colorectal carcinomas. J. Biol. Chem. 269 (1994), 32924–32931.
71. Thompson, J., Seitz, M., Chastre, E., Ditter, M., Aldrian, C., Gespach, C., Zimmermann, W., Down-regulation of carcinoembryonic antigen family member 2 expression is an early event in colorectal tumorigenesis. Cancer Res. 57 (1997), 1776–1784.
72. van de Wetering, M., Sancho, E., Verweij, C., de Lau, W., Oving, I., Hurlstone, A., van der Horn, K., Batlle, E., Coudreuse, D., Haramis, A.P., et al. The β-catenin/TCF-4 complex imposes a crypt progenitor phenotype on colorectal cancer cells. Cell 111 (2002), 241–250.
73. van de Wetering, M., Francies, H.E., Francis, J.M., Bounova, G., Iorio, F., Pronk, A., van Houdt, W., van Gorp, J., Taylor-Weiner, A., Kester, L., et al. Prospective derivation of a living organoid biobank of colorectal cancer patients. Cell 161 (2015), 933–945.
74. Vizcaíno, J.A., Csordas, A., del-Toro, N., Dianes, J.A., Griss, J., Lavidas, I., Mayer, G., Perez-Riverol, Y., Reisinger, F., Ternent, T., et al. 2016 update of the PRIDE database and its related tools. Nucleic Acids Res. 44:D1 (2016), D447–D456.
75. Walker, M.G., Volkmuth, W., Sprinzak, E., Hodgson, D., Klingler, T., Prediction of gene function by genome-scale expression analysis: prostate cancer-associated genes. Genome Res. 9 (1999), 1198–1203.
76. Weeber, F., van de Wetering, M., Hoogstraat, M., Dijkstra, K.K., Krijgsman, O., Kuilman, T., Gadellaa-van Hooijdonk, C.G., van der Velden, D.L., Peeper, D.S., Cuppen, E.P., et al. Preserved genetic diversity in organoids cultured from biopsies of human colorectal cancer metastases. Proc. Natl. Acad. Sci. USA 112 (2015), 13308–13311.
77. Wheeler, J.M., Bodmer, W.F., Mortensen, N.J., DNA mismatch repair genes and colorectal cancer. Gut 47 (2000), 148–153.
78. Williams, S.J., McGuckin, M.A., Gotley, D.C., Eyre, H.J., Sutherland, G.R., Antalis, T.M., Two novel mucin genes down-regulated in colorectal cancer identified by differential display. Cancer Res. 59 (1999), 4083–4089.
79. Wiśniewski, J.R., Ostasiewicz, P., Duś, K., Zielińska, D.F., Gnad, F., Mann, M., Extensive quantitative remodeling of the proteome between normal colon tissue and adenocarcinoma. Mol. Syst. Biol., 8, 2012, 611.
80. Woerner, S.M., Kloor, M., Mueller, A., Rueschoff, J., Friedrichs, N., Buettner, R., Buzello, M., Kienle, P., Knaebel, H.P., Kunstmann, E., et al., German HNPCC Consortium. Microsatellite instability of selective target genes in HNPCC-associated colon adenomas. Oncogene 24 (2005), 2525–2535.
81. Xie, C., Powell, C., Yao, M., Wu, J., Dong, Q., Ubiquitin-conjugating enzyme E2C: a potential cancer biomarker. Int. J. Biochem. Cell Biol. 47 (2014), 113–117.
82. Yates, J.R. 3rd, The revolution and evolution of shotgun proteomics for large-scale proteome analysis. J. Am. Chem. Soc. 135 (2013), 1629–1640.
83. Zhang, B., Wang, J., Wang, X., Zhu, J., Liu, Q., Shi, Z., Chambers, M.C., Zimmerman, L.J., Shaddox, K.F., Kim, S., et al., NCI CPTAC. Proteogenomic characterization of human colon and rectal cancer. Nature 513 (2014), 382–387.