Proteomics in studying cancer stem cell biology

Expert Review of Proteomics

Volumn 9, Issue 3, 2012, Pages 325-336

  Kranenburg, Onno ^a   Emmink, Benjamin L ^a   Knol, Jaco ^b   Van Houdt, Winan J ^a   Rinkes, Inne H M Borel ^a   Jimenez, Connie R ^b  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

biomarker; cancer; cancer stem cell; differentiation; interactome; mass spectrometry; multipotency; pluripotency; proteomics; tumor initiating cell

Indexed keywords

BIOLOGICAL MARKER; INTERACTOME; PROTEOME; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

CANCER GROWTH; CANCER STEM CELL; CELL DIFFERENTIATION; CELL HYPOXIA; CELL TYPE; CHROMATIN IMMUNOPRECIPITATION; CONNECTIVE TISSUE; CYTOLOGY; EMBRYONIC STEM CELL; FIBROBLAST; FLUORESCENCE ACTIVATED CELL SORTING; GENETIC HETEROGENEITY; HUMAN; IMMUNOPRECIPITATION; INFLAMMATORY CELL; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MESENCHYMAL STEM CELL; METASTASIS; MULTIPOTENT STEM CELL; NONHUMAN; PLURIPOTENT STEM CELL; PROTEIN PURIFICATION; PROTEOMICS; REVIEW; TANDEM IMMUNOPURIFICATION; TANDEM MASS SPECTROMETRY; TUMOR SPHEROID; TWO DIMENSIONAL GEL ELECTROPHORESIS;

CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL SEPARATION; FLOW CYTOMETRY; HUMANS; MASS SPECTROMETRY; MULTIPOTENT STEM CELLS; NEOPLASMS; NEOPLASTIC STEM CELLS; PROTEOMICS; SIGNAL TRANSDUCTION; TUMOR MARKERS, BIOLOGICAL;

EID: 84864264964     PISSN: 14789450     EISSN: 17448387     Source Type: Journal    
DOI: 10.1586/epr.12.24     Document Type: Review

References (75)

1. Lobo NA, Shimono Y, Qian D, Clarke MF. The biology of cancer stem cells. Annu. Rev. Cell Dev. Biol. 23, 675-699 (2007).
2. Clevers H. The cancer stem cell: Premises, promises and challenges. Nat. Med. 17(3), 313-319 (2011).
3. Kelly PN, Dakic A, Adams JM, Nutt SL, Strasser A. Tumor growth need not be driven by rare cancer stem cells. Science 317(5836), 337 (2007).
4. Quintana E, Shackleton M, Foster HR et al. Phenotypic heterogeneity among tumorigenic melanoma cells from patients that is reversible and not hierarchically organized. Cancer Cell 18(5), 510-523 (2010).
5. Goardon N, Marchi E, Atzberger A et al. Coexistence of LMPP-like and GMP-like leukemia stem cells in acute myeloid leukemia. Cancer Cell 19(1), 138-152 (2011).
6. Gupta PB, Fillmore CM, Jiang G et al. Stochastic state transitions give rise to phenotypic equilibrium in populations of cancer cells. Cell 146(4), 633-644 (2011).
7. Roesch A, Fukunaga-Kalabis M, Schmidt EC et al. A temporarily distinct subpopulation of slow-cycling melanoma cells is required for continuous tumor growth. Cell 141(4), 583-594 (2010).
8. Vermeulen L, De Sousa E Melo F, Van der Heijden M et al. Wnt activity defines colon cancer stem cells and is regulated by the microenvironment. Nat. Cell Biol. 12(5), 468-476 (2010).
9. Mallanna SK, Rizzino A. Systems biology provides new insights into the molecular mechanisms that control the fate of embryonic stem cells. J. Cell Physiol. 227(1), 27-34 (2012).
10. Sjöblom T, Jones S, Wood LD et al. The consensus coding sequences of human breast and colorectal cancers. Science 314(5797), 268-274 (2006).
11. Bonizzi G, Cicalese A, Insinga A, Pelicci PG. The emerging role of p53 in stem cells. Trends Mol. Med. 18(1), 6-12 (2012).
12. Cicalese A, Bonizzi G, Pasi CE et al. The tumor suppressor p53 regulates polarity of self-renewing divisions in mammary stem cells. Cell 138(6), 1083-1095 (2009).
13. Laurenti E, Wilson A, Trumpp A. Myc's other life: Stem cells and beyond. Curr. Opin. Cell Biol. 21(6), 844-854 (2009).
14. Feng Y, Bommer GT, Zhao J et al. Mutant KRAS promotes hyperplasia and alters differentiation in the colon epithelium but does not expand the presumptive stem cell pool. Gastroenterology 141(3), 1003-1013, e1 (2011).
15. Braakman RB, Luider TM, Martens JW, Foekens JA, Umar A. Laser capture microdissection applications in breast cancer proteomics. Methods Mol. Biol. 755, 143-154 (2011).
16. Wisniewski JR, Ostasiewicz P, Mann M. High recovery FASP applied to the proteomic analysis of microdissected formalin fixed paraffin embedded cancer tissues retrieves known colon cancer markers. J. Proteome Res. 10(7), 3040-3049 (2011).
17. Di Palma S, Stange D, Van De Wetering M, Clevers H, Heck AJ, Mohammed S. Highly sensitive proteome analysis of FACS-sorted adult colon stem cells. J. Proteome Res. 10(8), 3814-3819 (2011).
18. Emmink BL, Van Houdt WJ, Vries RG et al. Differentiated human colorectal cancer cells protect tumor-initiating cells from irinotecan. Gastroenterology 141(1), 269-278 (2011).
19. Ricci-Vitiani L, Lombardi DG, Pilozzi E et al. Identification and expansion of human colon-cancer-initiating cells. Nature 445(7123), 111-115 (2007).
20. Sato T, Stange DE, Ferrante M et al. Long-term expansion of epithelial organoids from human colon, adenoma, adenocarcinoma, and Barrett's epithelium. Gastroenterology 141(5), 1762-1772 (2011).
21. Patru C, Romao L, Varlet P et al. CD133, CD15/SSEA-1, CD34 or side populations do not resume tumor-initiating properties of long-term cultured cancer stem cells from human malignant glio-neuronal tumors. BMC Cancer 10, 66 (2010).
22. Van Houdt WJ, Emmink BL, Pham TV et al. Comparative proteomics of colon cancer stem cells and differentiated tumor cells identifies BIRC6 as a potential therapeutic target. Mol. Cell Proteomics 10(12), M111.011353 (2011).
23. Geiger T, Cox J, Mann M. Proteomics on an Orbitrap benchtop mass spectrometer using all-ion fragmentation. Mol. Cell Proteomics 9(10), 2252-2261 (2010).
24. Roth MJ, Plymire DA, Chang AN et al. Sensitive and reproducible intact mass analysis of complex protein mixtures with superficially porous capillary reversedphase liquid chromatography mass spectrometry. Anal. Chem. 83(24), 9586-9592 (2011).
25. Wang D, Hincapie M, Rejtar T, Karger BL. Ultrasensitive characterization of site-specific glycosylation of affinitypurified haptoglobin from lung cancer patient plasma using 10 μm i.d. porous layer open tubular liquid chromatographylinear ion trap collision-induced dissociation/electron transfer dissociation mass spectrometry. Anal. Chem. 83(6), 2029-2037 (2011).
26. Shen Y, Tolic N, Masselon C et al. Ultrasensitive proteomics using highefficiency on-line micro-SPE-nanoLCnanoESI MS and MS/MS. Anal. Chem. 76(1), 144-154 (2004).
27. Luo Q, Yue G, Valaskovic GA, Gu Y, Wu SL, Karger BL. On-line 1D and 2D porous layer open tubular/LC-ESI-MS using 10-microm-i.d. poly(styrenedivinylbenzene) columns for ultrasensitive proteomic analysis. Anal. Chem. 79(16), 6174-6181 (2007).
28. Tian R, Alvarez-Saavedra M, Cheng HY, Figeys D. Uncovering the proteome response of the master circadian clock to light using an AutoProteome system. Mol. Cell Proteomics 10(11), M110.007252 (2011).
29. Wang N, Xu M, Wang P, Li L. Development of mass spectrometry-based shotgun method for proteome analysis of 500 to 5000 cancer cells. Anal. Chem. 82(6), 2262-2271 (2010).
30. Cox J, Mann M. Quantitative, highresolution proteomics for data-driven systems biology. Annu. Rev. Biochem. 80, 273-299 (2011).
31. Jimenez CR, Piersma S, Pham TV. High-throughput and targeted in-depth mass spectrometry-based approaches for biofluid profiling and biomarker discovery. Biomark. Med. 1(4), 541-565 (2007).
32. Piersma SR, Fiedler U, Span S et al. Workflow comparison for label-free, quantitative secretome proteomics for cancer biomarker discovery: Method evaluation, differential analysis, and verification in serum. J. Proteome Res. 9(4), 1913-1922 (2010).
33. Fang Y, Robinson DP, Foster LJ. Quantitative analysis of proteome coverage and recovery rates for upstream fractionation methods in proteomics. J. Proteome Res. 9(4), 1902-1912 (2010).
34. Ostasiewicz P, Zielinska DF, Mann M, Wisniewski JR. Proteome, phosphoproteome, and N-glycoproteome are quantitatively preserved in formalinfixed paraffin-embedded tissue and analyzable by high-resolution mass spectrometry. J. Proteome Res. 9(7), 3688-3700 (2010).
35. Hughes CS, Nuhn AA, Postovit LM, Lajoie GA. Proteomics of human embryonic stem cells. Proteomics 11(4), 675-690 (2011).
36. Whetton AD, Williamson AJ, Krijgsveld J et al. The time is right: Proteome biology of stem cells. Cell Stem Cell 2(3), 215-217 (2008).
37. Williamson AJ, Whetton AD. Development of approaches for systematic analysis of protein networks in stem cells. Adv. Enzyme Regul. 50(1), 273-284 (2010).
38. Williamson AJ, Whetton AD. The requirement for proteomics to unravel stem cell regulatory mechanisms. J. Cell. Physiol. 226(10), 2478-2483 (2011).
39. Liang J, Wan M, Zhang Y et al. Nanog and Oct4 associate with unique transcriptional repression complexes in embryonic stem cells. Nat. Cell Biol. 10(6), 731-739 (2008).
40. Van den Berg DL, Snoek T, Mullin NP et al. An Oct4-centered protein interaction network in embryonic stem cells. Cell Stem Cell 6(4), 369-381 (2010).
41. Wang J, Rao S, Chu J et al. A protein interaction network for pluripotency of embryonic stem cells. Nature 444(7117), 364-368 (2006).
42. Mak AB, Ni Z, Hewel JA et al. A lentiviral functional proteomics approach identifies chromatin remodeling complexes important for the induction of pluripotency. Mol. Cell Proteomics 9(5), 811-823 (2010).
43. Pardo M, Lang B, Yu L et al. An expanded Oct4 interaction network: Implications for stem cell biology, development, and disease. Cell Stem Cell 6(4), 382-395 (2010).
44. Mallanna SK, Ormsbee BD, Iacovino M et al. Proteomic analysis of Sox2-associated proteins during early stages of mouse embryonic stem cell differentiation identifies Sox21 as a novel regulator of stem cell fate. Stem Cells 28(10), 1715-1727 (2010).
45. Wu Q, Chen X, Zhang J et al. Sall4 interacts with Nanog and co-occupies Nanog genomic sites in embryonic stem cells. J. Biol. Chem. 281(34), 24090-24094 (2006).
46. Cox JL, Mallanna SK, Luo X, Rizzino A. Sox2 uses multiple domains to associate with proteins present in Sox2-protein complexes. PLoS ONE 5(11), e15486 (2010).
47. Fang X, Yoon JG, Li L et al. Landscape of the SOX2 protein-protein interactome. Proteomics 11(5), 921-934 (2011).
48. Sánchez C, Sánchez I, Demmers JA, Rodriguez P, Strouboulis J, Vidal M. Proteomics analysis of Ring1B/Rnf2 interactors identifies a novel complex with the Fbxl10/Jhdm1B histone demethylase and the Bcl6 interacting corepressor. Mol. Cell Proteomics 6(5), 820-834 (2007).
49. Neganova I, Vilella F, Atkinson SP et al. An important role for CDK2 in G1 to S checkpoint activation and DNA damage response in human embryonic stem cells. Stem Cells 29(4), 651-659 (2011).
50. Heng JC, Ng HH. Transcriptional regulation in embryonic stem cells. Adv. Exp. Med. Biol. 695, 76-91 (2010).
51. He J, Liu Y, Zhu TS et al. Glycoproteomic analysis of glioblastoma stem cell differentiation. J. Proteome Res. 10(1), 330-338 (2011).
52. Ma S, Chan KW, Lee TK et al. Aldehyde dehydrogenase discriminates the CD133 liver cancer stem cell populations. Mol. Cancer Res. 6(7), 1146-1153 (2008).
53. Fang DD, Kim YJ, Lee CN et al. Expansion of CD133(+) colon cancer cultures retaining stem cell properties to enable cancer stem cell target discovery. Br. J. Cancer 102(8), 1265-1275 (2010).
54. Lee EK, Han GY, Park HW, Song YJ, Kim CW. Transgelin promotes migration and invasion of cancer stem cells. J. Proteome Res. 9(10), 5108-5117 (2010).
55. Dai L, Li C, Shedden KA et al. Quantitative proteomic profiling studies of pancreatic cancer stem cells. J. Proteome Res. 9(7), 3394-3402 (2010).
56. Dormeyer W, Van Hoof D, Braam SR, Heck AJ, Mummery CL, Krijgsveld J. Plasma membrane proteomics of human embryonic stem cells and human embryonal carcinoma cells. J. Proteome Res. 7(7), 2936-2951 (2008).
57. Chaerkady R, Kerr CL, Kandasamy K, Marimuthu A, Gearhart JD, Pandey A. Comparative proteomics of human embryonic stem cells and embryonal carcinoma cells. Proteomics 10(7), 1359-1373 (2010).
58. Dai L, Liu Y, He J et al. Differential profiling studies of N-linked glycoproteins in glioblastoma cancer stem cells upon treatment with ?-secretase inhibitor. Proteomics 11(20), 4021-4028 (2011).
59. Dai L, He J, Liu Y et al. Dose-dependent proteomic analysis of glioblastoma cancer stem cells upon treatment with gammasecretase inhibitor. Proteomics 11(23), 4529-4540 (2011).
60. Nilsson CL, Dillon R, Devakumar A et al. Quantitative phosphoproteomic analysis of the STAT3/IL-6/HIF1alpha signaling network: An initial study in GSC11 glioblastoma stem cells. J. Proteome Res. 9(1), 430-443 (2010).
61. Merlos-Suárez A, Barriga FM, Jung P et al. The intestinal stem cell signature identifies colorectal cancer stem cells and predicts disease relapse. Cell Stem Cell 8(5), 511-524 (2011).
62. Alaiya AA, Al-Mohanna M, Aslam M et al. Proteomics-based signature for human benign prostate hyperplasia and prostate adenocarcinoma. Int. J. Oncol. 38(4), 1047-1057 (2011).
63. Chan EC, Koh PK, Mal M et al. Metabolic profiling of human colorectal cancer using high-resolution magic angle spinning nuclear magnetic resonance (HR-MAS NMR) spectroscopy and gas chromatography mass spectrometry (GC/MS). J. Proteome Res. 8(1), 352-361 (2009).
64. Oakman C, Santarpia L, Di Leo A. Breast cancer assessment tools and optimizing adjuvant therapy. Nat. Rev. Clin. Oncol. 7(12), 725-732 (2010).
65. Kelley RK, Venook AP. Prognostic and predictive markers in stage II colon cancer: Is there a role for gene expression profiling? Clin. Colorectal Cancer 10(2), 73-80 (2011).
66. Aebersold R, Mann M. Mass spectrometry-based proteomics. Nature 422(6928), 198-207 (2003).
67. Nilsson T, Mann M, Aebersold R, Yates III JR, Bairoch A, Bergeron JJ. Mass spectrometry in high-throughput proteomics: Ready for the big time. Nat. Methods 7(9), 681-685 (2010).
68. Yates JR, Ruse CI, Nakorchevsky A. Proteomics by mass spectrometry: Approaches, advances, and applications. Annu. Rev. Biomed. Eng. 11, 49-79 (2009).
69. Michalski A, Damoc E, Hauschild JP et al. Mass spectrometry-based proteomics using Q Exactive, a high-performance benchtop quadrupole Orbitrap mass spectrometer. Mol. Cell Proteomics 10(9), M111.011015 (2011).
70. Thakur SS, Geiger T, Chatterjee B et al. Deep and highly sensitive proteome coverage by LC-MS/MS without prefractionation. Mol. Cell Proteomics 10(8), M110.003699 (2011).
71. Nagaraj N, Kulak NA, Cox J et al. Systems-wide perturbation analysis with near complete coverage of the yeast proteome by single-shot UHPLC runs on a bench-top Orbitrap. Mol. Cell Proteomics. 11(3), M111.013722 (2011).
72. Snippert HJ, Clevers H. Tracking adult stem cells. EMBO Rep. 12(2), 113-122 (2011).
73. De Sousa E Melo F, Colak S, Buikhuisen J et al. Methylation of cancer-stem-cellassociated Wnt target genes predicts poor prognosis in colorectal cancer patients. Cell Stem Cell 9(5), 476-485 (2011).
74. Jung P, Sato T, Merlos-Suárez A et al. Isolation and in vitro expansion of human colonic stem cells. Nat. Med. 17(10), 1225-1227 (2011).
75. He J, Liu Y, Xie X et al. Identification of cell surface glycoprotein markers for glioblastoma-derived stem-like cells using a lectin microarray and LC-MS/MS approach. J. Proteome Res. 9(5), 2565-2572 (2010).