A proteomics and transcriptomics approach to identify leukemic stem cell (LSC) markers

Molecular and Cellular Proteomics

Volumn 12, Issue 3, 2013, Pages 626-637

  Bonardi, Francesco ^a   Fusetti, Fabrizia ^b   Deelen, Patrick ^a   Van Gosliga, Djoke ^a   Vellenga, Edo ^a   Schuringa, Jan Jacob ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA5 INTEGRIN; ALPHA6 INTEGRIN; CD135 ANTIGEN; CD34 ANTIGEN; CD47 ANTIGEN; CD82 ANTIGEN; CD96 ANTIGEN; CD97 ANTIGEN; CD99 ANTIGEN; CELL MARKER; HERMES ANTIGEN; LYMPHOCYTE ANTIGEN; MEMBRANE PROTEIN; PARATHYROID HORMONE RECEPTOR 2; PROTEOME; SCATTER FACTOR RECEPTOR; TRANSCRIPTOME; UNCLASSIFIED DRUG;

ACUTE GRANULOCYTIC LEUKEMIA; ARTICLE; BONE MARROW CELL; CANCER CLASSIFICATION; CELL HETEROGENEITY; CELL MEMBRANE; CELL POPULATION; CLINICAL ARTICLE; CONTROLLED STUDY; FLOW CYTOMETRY; GENE EXPRESSION; HUMAN; HUMAN CELL; LEUKEMIA CELL; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MEMBRANE MARKER; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEOMICS; STEM CELL; TRANSCRIPTOMICS;

ACUTE DISEASE; ANTIGENS, CD34; CELL MEMBRANE; CHROMATOGRAPHY, LIQUID; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, LEUKEMIC; HUMANS; INTEGRIN ALPHA6; LEUKEMIA, MYELOID; NANOTECHNOLOGY; NEOPLASTIC STEM CELLS; PRINCIPAL COMPONENT ANALYSIS; PROTEOME; PROTEOMICS; TANDEM MASS SPECTROMETRY; TUMOR MARKERS, BIOLOGICAL;

EID: 84874600807     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M112.021931     Document Type: Article

References (61)

1. Estey, E., and Dohner, H. (2006) Acute myeloid leukaemia. Lancet 368, 1894-1907 (Pubitemid 44794525)
2. Lowenberg, B., Downing, J. R., and Burnett, A. (1999) Acute myeloid leukemia. N. Engl. J. Med. 341, 1051-1062 (Pubitemid 29451802)
3. Bonnet, D., and Dick, J. E. (1997) Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat. Med. 3, 730-737 (Pubitemid 27298715)
4. Dalerba, P., Cho, R. W., and Clarke, M. F. (2007) Cancer stem cells: Models and concepts. Annu. Rev. Med. 58, 267-284 (Pubitemid 46706514)
5. Doulatov, S., Notta, F., Laurenti, E., and Dick, J. E. (2012) Hematopoiesis: A human perspective. Cell Stem Cell 10, 120-136
6. Lapidot, T., Sirard, C., Vormoor, J., Murdoch, B., Hoang, T., Caceres-Cortes, J., Minden, M., Paterson, B., Caligiuri, M. A., and Dick, J. E. (1994) A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 367, 645-648 (Pubitemid 24067706)
7. Rizo, A., Vellenga, E., de Haan, G., and Schuringa, J. J. (2006) Signaling pathways in self-renewing hematopoietic and leukemic stem cells: Do all stem cells need a niche? Hum. Mol. Genet. 15, R210-R219 (Pubitemid 44446796)
8. Vardiman, J. W., Thiele, J., Arber, D. A., Brunning, R. D., Borowitz, M. J., Porwit, A., Harris, N. L., Le Beau, M. M., Hellstrom-Lindberg, E., Tefferi, A., and Bloomfield, C. D. (2009) The 2008 revision of the World Health Organization (WHO) classification of myeloid neoplasms and acute leukemia: Rationale and important changes. Blood 114, 937-951
9. Kondo, M., Wagers, A. J., Manz, M. G., Prohaska, S. S., Scherer, D. C., Beilhack, G. F., Shizuru, J. A., and Weissman, I. L. (2003) Biology of hematopoietic stem cells and progenitors: Implications for clinical application. Annu. Rev. Immunol. 21, 759-806 (Pubitemid 37174547)
10. Ding, L., Ley, T. J., Larson, D. E., Miller, C. A., Koboldt, D. C., Welch, J. S., Ritchey, J. K., Young, M. A., Lamprecht, T., McLellan, M. D., McMichael, J. F., Wallis, J. W., Lu, C., Shen, D., Harris, C. C., Dooling, D. J., Fulton, R. S., Fulton, L. L., Chen, K., Schmidt, H., Kalicki-Veizer, J., Magrini, V. J., Cook, L., McGrath, S. D., Vickery, T. L., Wendl, M. C., Heath, S., Watson, M. A., Link, D. C., Tomasson, M. H., Shannon, W. D., Payton, J. E., Kulkarni, S., Westervelt, P., Walter, M. J., Graubert, T. A., Mardis, E. R., Wilson, R. K., and DiPersio, J. F. (2012) Clonal evolution in relapsed acute myeloid leukaemia revealed by whole-genome sequencing. Nature 481, 506-510
11. Walter, M. J., Shen, D., Ding, L., Shao, J., Koboldt, D. C., Chen, K., Larson, D. E., McLellan, M. D., Dooling, D., Abbott, R., Fulton, R., Magrini, V., Schmidt, H., Kalicki-Veizer, J., O'Laughlin, M., Fan, X., Grillot, M., Witowski, S., Heath, S., Frater, J. L., Eades, W., Tomasson, M., Westervelt, P., DiPersio, J. F., Link, D. C., Mardis, E. R., Ley, T. J., Wilson, R. K., and Graubert, T. A. (2012) Clonal architecture of secondary acute myeloid leukemia. N. Engl. J. Med. 366, 1090-1098
12. Valk, P. J., Verhaak, R. G., Beijen, M. A., Erpelinck, C. A., Barjesteh van Waalwijk van Doorn-Khosrovani, S., Boer, J. M., Beverloo, H. B., Moorhouse, M. J., van der Spek, P. J., Lowenberg, B., and Delwel, R. (2004) Prognostically useful gene-expression profiles in acute myeloid leukemia. N. Engl. J. Med. 350, 1617-1628 (Pubitemid 38528701)
13. Metzeler, K. H., Hummel, M., Bloomfield, C. D., Spiekermann, K., Braess, J., Sauerland, M. C., Heinecke, A., Radmacher, M., Marcucci, G., Whitman, S. P., Maharry, K., Paschka, P., Larson, R. A., Berdel, W. E., Buchner, T., Wormann, B., Mansmann, U., Hiddemann, W., Bohlander, S. K., and Buske, C. (2008) An 86-probe-set gene-expression signature predicts survival in cytogenetically normal acute myeloid leukemia. Blood 112, 4193-4201
14. de Jonge, H. J., Woolthuis, C. M., Vos, A. Z., Mulder, A., van den Berg, E., Kluin, P. M., van der Weide, K., de Bont, E. S., Huls, G., Vellenga, E., and Schuringa, J. J. (2011) Gene expression profiling in the leukemic stem cell-enriched CD34-fraction identifies target genes that predict prognosis in normal karyotype AML. Leukemia 25, 1825-1833
15. Eppert, K., Takenaka, K., Lechman, E. R., Waldron, L., Nilsson, B., van Galen, P., Metzeler, K. H., Poeppl, A., Ling, V., Beyene, J., Canty, A. J., Danska, J. S., Bohlander, S. K., Buske, C., Minden, M. D., Golub, T. R., Jurisica, I., Ebert, B. L., and Dick, J. E. (2011) Stem cell gene expression programs influence clinical outcome in human leukemia. Nat. Med. 17, 1086-1093
16. Aebersold, R., and Mann, M. (2003) Mass spectrometry-based proteomics. Nature 422, 198-207 (Pubitemid 36362757)
17. Cravatt, B. F., Simon, G. M., and Yates, J. R. 3rd (2007) The biological impact of mass-spectrometry-based proteomics. Nature 450, 991-1000 (Pubitemid 350273629)
18. Patterson, S. D., and Aebersold, R. H. (2003) Proteomics: The first decade and beyond. Nat. Genet. 33, 311-323 (Pubitemid 36278841)
19. van Gosliga, D., Schepers, H., Rizo, A., van der Kolk, D., Vellenga, E., and Schuringa, J. J. (2007) Establishing long-term cultures with self-renewing acute myeloid leukemia stem/progenitor cells. Exp. Hematol. 35, 1538-1549 (Pubitemid 47419138)
20. Schuringa, J. J., and Schepers, H. (2009) Ex vivo assays to study selfrenewal and long-term expansion of genetically modified primary human acute myeloid leukemia stem cells. Methods Mol. Biol. 538, 287-300
21. Gentleman, R. C., Carey, V. J., Bates, D. M., Bolstad, B., Dettling, M., Dudoit, S., Ellis, B., Gautier, L., Ge, Y., Gentry, J., Hornik, K., Hothorn, T., Huber, W., Iacus, S., Irizarry, R., Leisch, F., Li, C., Maechler, M., Rossini, A. J., Sawitzki, G., Smith, C., Smyth, G., Tierney, L., Yang, J. Y., and Zhang, J. (2004) Bioconductor: Open software development for computational biology and bioinformatics. Genome. Biol. 5, R80
22. Du, P., Kibbe, W. A., and Lin, S. M. (2008) lumi: A pipeline for processing Illumina microarray. Bioinformatics 24, 1547-1548 (Pubitemid 351911712)
23. Crijns, A. P., Fehrmann, R. S., de, J. S., Gerbens, F., Meersma, G. J., Klip, H. G., Hollema, H., Hofstra, R. M., te Meerman, G. J., de Vries, E. G., and van der Zee, A. G. (2009) Survival-related profile, pathways, and transcription factors in ovarian cancer. PLoS. Med. 6, e24
24. Alter, O., Brown, P. O., and Botstein, D. (2000) Singular value decomposition for genome-wide expression data processing and modeling. Proc. Natl. Acad. Sci. U.S.A. 97, 10101-10106
25. Mitchell, T. M. (1997) Machine Learning. New York, McGraw-Hill
26. Hope, K. J., Jin, L., and Dick, J. E. (2004) Acute myeloid leukemia originates from a hierarchy of leukemic stem cell classes that differ in self-renewal capacity. Nat. Immunol. 5, 738-743 (Pubitemid 39023306)
27. Washburn, M. P., Wolters, D., and Yates, J. R., 3rd (2001) Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat. Biotechnol. 19, 242-247 (Pubitemid 32220565)
28. Muntel, J., Hecker, M., and Becher, D. (2012) An exclusion list based label-free proteome quantification approach using an LTQ Orbitrap. Rapid Commun. Mass. Spectrom. 26, 701-709
29. Korn, E. L., Troendle, J. F., McShane, L. M., and Simon, R. (2004) Controlling the number of false discoveries: Application to high-dimensional genomic data. J. Stat. Plan. Infer. 124, 379-398 (Pubitemid 38830084)
30. Benjamini, Y., and Hochberg, Y. (1995) Controlling the false discovery rate-a practical and powerful approach to multiple testing. J. Roy. Stat. Soc. B. Met. 57, 289-300
31. Taussig, D. C., Miraki-Moud, F., Anjos-Afonso, F., Pearce, D. J., Allen, K., Ridler, C., Lillington, D., Oakervee, H., Cavenagh, J., Agrawal, S. G., Lister, T. A., Gribben, J. G., and Bonnet, D. (2008) Anti-CD38 antibodymediated clearance of human repopulating cells masks the heterogeneity of leukemia-initiating cells. Blood 112, 568-575
32. Wong, D. J., Liu, H., Ridky, T. W., Cassarino, D., Segal, E., and Chang, H. Y. (2008) Module map of stem cell genes guides creation of epithelial cancer stem cells. Cell Stem Cell 2, 333-344 (Pubitemid 351455242)
33. Neff, T., Sinha, A. U., Kluk, M. J., Zhu, N., Khattab, M. H., Stein, L., Xie, H., Orkin, S. H., and Armstrong, S. A. (2012) Polycomb repressive complex 2 is required for MLL-AF9 leukemia. Proc. Natl. Acad. Sci. U.S.A. 109, 5028-5033
34. Yagi, T., Morimoto, A., Eguchi, M., Hibi, S., Sako, M., Ishii, E., Mizutani, S., Imashuku, S., Ohki, M., and Ichikawa, H. (2003) Identification of a gene expression signature associated with pediatric AML prognosis. Blood 102, 1849-1856 (Pubitemid 37022582)
35. Bruce, S. J., Jonsson, P., Antti, H., Cloarec, O., Trygg, J., Marklund, S. L., and Moritz, T. (2008) Evaluation of a protocol for metabolic profiling studies on human blood plasma by combined ultra-performance liquid chromatography/mass spectrometry: From extraction to data analysis. Anal. Biochem. 372, 237-249 (Pubitemid 350116776)
36. Dormeyer, W., van Hoof, D., Braam, S. R., Heck, A. J., Mummery, C. L., and Krijgsveld, J. (2008) Plasma membrane proteomics of human embryonic stem cells and human embryonal carcinoma cells. J. Proteome. Res. 7, 2936-2951
37. Lund, R., Leth-Larsen, R., Jensen, O. N., and Ditzel, H. J. (2009) Efficient isolation and quantitative proteomic analysis of cancer cell plasma membrane proteins for identification of metastasis-associated cell surface markers. J. Proteome Res. 8, 3078-3090
38. Klimmeck, D., Hansson, J., Raffel, S., Vakhrushev, S. Y., Trumpp, A., and Krijgsveld, J. (27-3-2012) Proteomic cornerstones of hematopoietic stem cell differentiation: Distinct signatures of multipotent progenitors and myeloid committed cells. Mol. Cell Proteomics. Epub ahead of print
39. Rosnet, O., Buhring, H. J., Marchetto, S., Rappold, I., Lavagna, C., Sainty, D., Arnoulet, C., Chabannon, C., Kanz, L., Hannum, C., and Birnbaum, D. (1996) Human FLT3/FLK2 receptor tyrosine kinase is expressed at the surface of normal and malignant hematopoietic cells. Leukemia 10, 238-248 (Pubitemid 26102887)
40. Carow, C. E., Levenstein, M., Kaufmann, S. H., Chen, J., Amin, S., Rockwell, P., Witte, L., Borowitz, M. J., Civin, C. I., and Small, D. (1996) Expression of the hematopoietic growth factor receptor FLT3 (STK-1/ Flk2) in human leukemias. Blood 87, 1089-1096 (Pubitemid 26043536)
41. Nakao, M., Yokota, S., Iwai, T., Kaneko, H., Horiike, S., Kashima, K., Sonoda, Y., Fujimoto, T., and Misawa, S. (1996) Internal tandem duplication of the flt3 gene found in acute myeloid leukemia. Leukemia 10, 1911-1918 (Pubitemid 27019637)
42. Yamamoto, Y., Kiyoi, H., Nakano, Y., Suzuki, R., Kodera, Y., Miyawaki, S., Asou, N., Kuriyama, K., Yagasaki, F., Shimazaki, C., Akiyama, H., Saito, K., Nishimura, M., Motoji, T., Shinagawa, K., Takeshita, A., Saito, H., Ueda, R., Ohno, R., and Naoe, T. (2001) Activating mutation of D835 within the activation loop of FLT3 in human hematologic malignancies. Blood 97, 2434-2439 (Pubitemid 32291491)
43. Ozeki, K., Kiyoi, H., Hirose, Y., Iwai, M., Ninomiya, M., Kodera, Y., Miyawaki, S., Kuriyama, K., Shimazaki, C., Akiyama, H., Nishimura, M., Motoji, T., Shinagawa, K., Takeshita, A., Ueda, R., Ohno, R., Emi, N., and Naoe, T. (2004) Biologic and clinical significance of the FLT3 transcript level in acute myeloid leukemia. Blood 103, 1901-1908 (Pubitemid 38268989)
44. Majeti, R., Chao, M. P., Alizadeh, A. A., Pang, W. W., Jaiswal, S., Gibbs, K. D., Jr., van Rooijen, N., and Weissman, I. L. (2009) CD47 is an adverse prognostic factor and therapeutic antibody target on human acute myeloid leukemia stem cells. Cell 138, 286-299
45. Oldenborg, P. A., Zheleznyak, A., Fang, Y. F., Lagenaur, C. F., Gresham, H. D., and Lindberg, F. P. (2000) Role of CD47 as a marker of self on red blood cells. Science 288, 2051-2054 (Pubitemid 30397687)
46. Yamao, T., Noguchi, T., Takeuchi, O., Nishiyama, U., Morita, H., Hagiwara, T., Akahori, H., Kato, T., Inagaki, K., Okazawa, H., Hayashi, Y., Matozaki, T., Takeda, K., Akira, S., and Kasuga, M. (2002) Negative regulation of platelet clearance and of the macrophage phagocytic response by the transmembrane glycoprotein SHPS-1. J. Biol. Chem. 277, 39833-39839
47. Hosen, N., Park, C. Y., Tatsumi, N., Oji, Y., Sugiyama, H., Gramatzki, M., Krensky, A. M., and Weissman, I. L. (2007) CD96 is a leukemic stem cell-specific marker in human acute myeloid leukemia. Proc. Natl. Acad. Sci. U.S.A. 104, 11008-11013 (Pubitemid 47175217)
48. Bendall, L. J., Kortlepel, K., and Gottlieb, D. J. (1993) Human acute myeloid leukemia cells bind to bone marrow stroma via a combination of beta-1 and beta-2 integrin mechanisms. Blood 82, 3125-3132 (Pubitemid 23334940)
49. Jin, L., Hope, K. J., Zhai, Q., Smadja-Joffe, F., and Dick, J. E. (2006) Targeting of CD44 eradicates human acute myeloid leukemic stem cells. Nat. Med. 12, 1167-1174 (Pubitemid 44527352)
50. Qué ré, R., Andradottir, S., Brun, A. C., Zubarev, R. A., Karlsson, G., Olsson, K., Magnusson, M., Cammenga, J., and Karlsson, S. (2011) High levels of the adhesion molecule CD44 on leukemic cells generate acute myeloid leukemia relapse after withdrawal of the initial transforming event. Leukemia 25, 515-526
51. Charrad, R. S., Li, Y., Delpech, B., Balitrand, N., Clay, D., Jasmin, C., Chomienne, C., and Smadja-Joffe, F. (1999) Ligation of the CD44 adhesion molecule reverses blockage of differentiation in human acute myeloid leukemia. Nat. Med. 5, 669-676 (Pubitemid 29289431)
52. Jordan, C. T., Upchurch, D., Szilvassy, S. J., Guzman, M. L., Howard, D. S., Pettigrew, A. L., Meyerrose, T., Rossi, R., Grimes, B., Rizzieri, D. A., Luger, S. M., and Phillips, G. L. (2000) The interleukin-3 receptor alpha chain is a unique marker for human acute myelogenous leukemia stem cells. Leukemia 14, 1777-1784
53. Jin, L., Lee, E. M., Ramshaw, H. S., Busfield, S. J., Peoppl, A. G., Wilkinson, L., Guthridge, M. A., Thomas, D., Barry, E. F., Boyd, A., Gearing, D. P., Vairo, G., Lopez, A. F., Dick, J. E., and Lock, R. B. (2009) Monoclonal antibody-mediated targeting of CD123, IL-3 receptor alpha chain, eliminates human acute myeloid leukemic stem cells. Cell Stem Cell 5, 31-42
54. Coustan-Smith, E., Song, G., Clark, C., Key, L., Liu, P., Mehrpooya, M., Stow, P., Su, X., Shurtleff, S., Pui, C. H., Downing, J. R., and Campana, D. (2011) New markers for minimal residual disease detection in acute lymphoblastic leukemia. Blood 117, 6267-6276
55. Kikushige, Y., Shima, T., Takayanagi, S., Urata, S., Miyamoto, T., Iwasaki, H., Takenaka, K., Teshima, T., Tanaka, T., Inagaki, Y., and Akashi, K. (2010) TIM-3 is a promising target to selectively kill acute myeloid leukemia stem cells. Cell Stem Cell 7, 708-717
56. Larochelle, A., Gillette, J. M., Desmond, R., Ichwan, B., Cantilena, A., Cerf, A., Barrett, A. J., Wayne, A. S., Lippincott-Schwartz, J., and Dunbar, C. E. (2012) Bone marrow homing and engraftment of human hematopoietic stem and progenitor cells is mediated by a polarized membrane domain. Blood 119, 1848-1855
57. Calvi, L. M., Adams, G. B., Weibrecht, K. W., Weber, J. M., Olson, D. P., Knight, M. C., Martin, R. P., Schipani, E., Divieti, P., Bringhurst, F. R., Milner, L. A., Kronenberg, H. M., and Scadden, D. T. (2003) Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 425, 841-846 (Pubitemid 37351468)
58. Sudo, T., Yokota, T., Oritani, K., Satoh, Y., Sugiyama, T., Ishida, T., Shibayama, H., Ezoe, S., Fujita, N., Tanaka, H., Maeda, T., Nagasawa, T., and Kanakura, Y. (2012) The endothelial antigen ESAM monitors hematopoietic stem cell status between quiescence and self-renewal. J. Immunol. 189, 200-210
59. Gherardi, E., Birchmeier, W., Birchmeier, C., and Vande, Woude, G. (2012) Targeting MET in cancer: Rationale and progress. Nat. Rev. Cancer 12, 89-103
60. Kentsis, A., Reed, C., Rice, K. L., Sanda, T., Rodig, S. J., Tholouli, E., Christie, A., Valk, P. J., Delwel, R., Ngo, V., Kutok, J. L., Dahlberg, S. E., Moreau, L. A., Byers, R. J., Christensen, J. G., Woude, G. V., Licht, J. D., Kung, A. L., Staudt, L. M., and Look, A. T. (10-6-2012) Autocrine activation of the MET receptor tyrosine kinase in acute myeloid leukemia. Nat. Med. Epub ahead of print
61. Notta, F., Doulatov, S., Laurenti, E., Poeppl, A., Jurisica, I., and Dick, J. E. (2011) Isolation of single human hematopoietic stem cells capable of long-term multilineage engraftment. Science 333, 218-221