Genome-wide comparison of the transcriptomes of highly enriched normal and chronic myeloid leukemia stem and progenitor cell populations

Oncotarget

Volumn 4, Issue 5, 2013, Pages 715-728

  Gerber, Jonathan M ^a   Gucwa, Jessica L ^a   Esopi, David ^a   Gurel, Meltem ^a   Haffner, Michael C ^a   Vala, Milada ^a   Nelson, William G ^a   Jones, Richard J ^a   Yegnasubramanian, Srinivasan ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

ALDH; CD25; CD26; CD34; CD38; Chronic myeloid leukemia; CML; DPP4; GAS2; HSC; IL2RA; Leukemic stem cell; LSC; Myeloid progenitor cells; Normal hematopoietic stem cell

Indexed keywords

BONE MORPHOGENETIC PROTEIN; CONTACTIN 1; CYCLIN DEPENDENT KINASE INHIBITOR 1A; DIPEPTIDYL PEPTIDASE IV; INTERLEUKIN 1 RECEPTOR ACCESSORY PROTEIN; INTERLEUKIN 2 RECEPTOR ALPHA; MARCKS PROTEIN; MONOCYTE CHEMOTACTIC PROTEIN 1; PROTEIN TIMELESS; SOMATOMEDIN C RECEPTOR; TRANSCRIPTOME; TRANSFORMING GROWTH FACTOR BETA;

AEROBIC METABOLISM; ARTICLE; CACNA1D GENE; CANCER STEM CELL; CDKN1A GENE; CELL POPULATION; CELL PROLIFERATION; CHRONIC MYELOID LEUKEMIA; COMPARATIVE STUDY; CONTROLLED STUDY; DNA REPAIR; DOWN REGULATION; DPP4 GENE; DUSP12 GENE; EXON; GENE EXPRESSION; GENE TARGETING; HUMAN; HUMAN CELL; HUMAN TISSUE; IL1RAP GENE; IL2RA GENE; KCNK5 GENE; MARCKS GENE; MICROARRAY ANALYSIS; MOLECULAR PATHOLOGY; MYELOID PROGENITOR CELL; NUCLEOTIDE SEQUENCE; ONCOGENE C MYB; PERP GENE; PTPRD GENE; RNA SPLICING; SIGNAL TRANSDUCTION; SLC4A4 GENE; TIMELESS GENE; TUMOR GENE; UPREGULATION;

EID: 84880306032     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.990     Document Type: Article

References (50)

1. Druker BJ, Talpaz M, Resta DJ, Peng B, Buchdunger E, Ford JM, Lydon NB, Kantarjian H, Capdeville R, Ohno- Jones S and Sawyers CL. Efficacy and safety of a specific inhibitor of the BCR-ABL tyrosine kinase in chronic myeloid leukemia. N Engl J Med. 2001; 344(14):1031- 1037.
2. Kantarjian H, Talpaz M, O'Brien S, Garcia-Manero G, Verstovsek S, Giles F, Rios MB, Shan J, Letvak L, Thomas D, Faderl S, Ferrajoli A and Cortes J. High-dose imatinib mesylate therapy in newly diagnosed Philadelphia chromosome-positive chronic phase chronic myeloid leukemia. Blood. 2004; 103(8):2873-2878.
3. Cortes J, O'Brien S and Kantarjian H. Discontinuation of imatinib therapy after achieving a molecular response. Blood. 2004; 104(7):2204-2205.
4. Rousselot P, Huguet F, Rea D, Legros L, Cayuela JM, Maarek O, Blanchet O, Marit G, Gluckman E, Reiffers J, Gardembas M and Mahon FX. Imatinib mesylate discontinuation in patients with chronic myelogenous leukemia in complete molecular remission for more than 2 years. Blood. 2007; 109(1):58-60.
5. Graham SM, Jorgensen HG, Allan E, Pearson C, Alcorn MJ, Richmond L and Holyoake TL. Primitive, quiescent, Philadelphia-positive stem cells from patients with chronic myeloid leukemia are insensitive to STI571 in vitro. Blood. 2002; 99(1):319-325.
6. Angstreich GR, Matsui W, Huff CA, Vala MS, Barber J, Hawkins AL, Griffin CA, Smith BD and Jones RJ. Effects of imatinib and interferon on primitive chronic myeloid leukaemia progenitors. British journal of haematology. 2005; 130(3):373-381.
7. Copland M, Hamilton A, Elrick LJ, Baird JW, Allan EK, Jordanides N, Barow M, Mountford JC and Holyoake TL. Dasatinib (BMS-354825) targets an earlier progenitor population than imatinib in primary CML but does not eliminate the quiescent fraction. Blood. 2006; 107(11):4532-4539.
8. Bhatia R, Holtz M, Niu N, Gray R, Snyder DS, Sawyers CL, Arber DA, Slovak ML and Forman SJ. Persistence of malignant hematopoietic progenitors in chronic myelogenous leukemia patients in complete cytogenetic remission following imatinib mesylate treatment. Blood. 2003; 101(12):4701-4707.
9. Mahon FX, Rea D, Guilhot J, Guilhot F, Huguet F, Nicolini F, Legros L, Charbonnier A, Guerci A, Varet B, Etienne G, Reiffers J and Rousselot P. Discontinuation of imatinib in patients with chronic myeloid leukaemia who have maintained complete molecular remission for at least 2 years: the prospective, multicentre Stop Imatinib (STIM) trial. The lancet oncology. 2010; 11(11):1029-1035.
10. Hughes TP, Hochhaus A, Branford S, Muller MC, Kaeda JS, Foroni L, Druker BJ, Guilhot F, Larson RA, O'Brien SG, Rudoltz MS, Mone M, Wehrle E, Modur V, Goldman JM and Radich JP. Long-term prognostic significance of early molecular response to imatinib in newly diagnosed chronic myeloid leukemia: an analysis from the International Randomized Study of Interferon and STI571 (IRIS). Blood. 2010; 116(19):3758-3765.
11. O'Hare T, Zabriskie MS, Eiring AM and Deininger MW. Pushing the limits of targeted therapy in chronic myeloid leukaemia. Nature reviews Cancer. 2012; 12(8):513-526.
12. Bedi A, Zehnbauer BA, Collector MI, Barber JP, Zicha MS, Sharkis SJ and Jones RJ. BCR-ABL gene rearrangement and expression of primitive hematopoietic progenitors in chronic myeloid leukemia. Blood. 1993; 81(11):2898-2902.
13. Raaijmakers MH, van Emst L, de Witte T, Mensink E and Raymakers RA. Quantitative assessment of gene expression in highly purified hematopoietic cells using real-time reverse transcriptase polymerase chain reaction. Experimental hematology. 2002; 30(5):481-487.
14. Mahon FX, Belloc F, Lagarde V, Chollet C, Moreau- Gaudry F, Reiffers J, Goldman JM and Melo JV. MDR1 gene overexpression confers resistance to imatinib mesylate in leukemia cell line models. Blood. 2003; 101(6):2368- 2373.
15. Jiang G, Yang F, Li M, Weissbecker K, Price S, Kim KC, La Russa VF, Safah H and Ehrlich M. Imatinib (ST1571) provides only limited selectivity for CML cells and treatment might be complicated by silent BCR-ABL genes. Cancer biology & therapy. 2003; 2(1):103-108.
16. Bonnet D. Normal and leukaemic stem cells. British journal of haematology. 2005; 130(4):469-479.
17. Christ O, Lucke K, Imren S, Leung K, Hamilton M, Eaves A, Smith C and Eaves C. Improved purification of hematopoietic stem cells based on their elevated aldehyde dehydrogenase activity. Haematologica. 2007; 92(9):1165-1172.
18. Gerber JM, Smith BD, Ngwang B, Zhang H, Vala MS, Morsberger L, Galkin S, Collector MI, Perkins B, Levis MJ, Griffin CA, Sharkis SJ, Borowitz MJ, Karp JE and Jones RJ. A clinically relevant population of leukemic CD34(+) CD38(-) cells in acute myeloid leukemia. Blood. 2012; 119(15):3571-3577.
19. Vasiliou V, Pappa A and Estey T. Role of human aldehyde dehydrogenases in endobiotic and xenobiotic metabolism. Drug metabolism reviews. 2004; 36(2):279-299.
20. Gerber JM, Qin L, Kowalski J, Smith BD, Griffin CA, Vala MS, Collector MI, Perkins B, Zahurak M, Matsui W, Gocke CD, Sharkis SJ, Levitsky HI and Jones RJ. Characterization of chronic myeloid leukemia stem cells. American journal of hematology. 2011; 86(1):31-37.
21. Huang da W, Sherman BT and Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature protocols. 2009; 4(1):44- 57.
22. Huang da W, Sherman BT and Lempicki RA. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic acids research. 2009; 37(1):1-13.
23. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES and Mesirov JP. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proceedings of the National Academy of Sciences of the United States of America. 2005; 102(43):15545-15550.
24. Irizarry RA, Wang C, Zhou Y and Speed TP. Gene set enrichment analysis made simple. Statistical methods in medical research. 2009; 18(6):565-575.
25. Aryee MJ, Liu W, Engelmann JC, Nuhn P, Gurel M, Haffner MC, Esopi D, Irizarry RA, Getzenberg RH, Nelson WG, Luo J, Xu J, Isaacs WB, Bova GS and Yegnasubramanian S. DNA methylation alterations exhibit intraindividual stability and interindividual heterogeneity in prostate cancer metastases. Science translational medicine. 2013; 5(169):169ra110.
26. Cicuttini FM, Welch K and Boyd AW. Characterization of CD34+HLA-DR-CD38+ and CD34+HLA-DR-CD38- progenitor cells from human umbilical cord blood. Growth Factors. 1994; 10(2):127-134.
27. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, et al. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nature genetics. 2000; 25(1):25-29.
28. Kanehisa M, Goto S, Sato Y, Furumichi M and Tanabe M. KEGG for integration and interpretation of largescale molecular data sets. Nucleic acids research. 2012; 40(Database issue):D109-114.
29. Kanehisa M and Goto S. KEGG: kyoto encyclopedia of genes and genomes. Nucleic acids research. 2000; 28(1):27- 30.
30. Shioda T, Kato H, Ohnishi Y, Tashiro K, Ikegawa M, Nakayama EE, Hu H, Kato A, Sakai Y, Liu H, Honjo T, Nomoto A, Iwamoto A, Morimoto C and Nagai Y. Anti- HIV-1 and chemotactic activities of human stromal cellderived factor 1alpha (SDF-1alpha) and SDF-1beta are abolished by CD26/dipeptidyl peptidase IV-mediated cleavage. Proceedings of the National Academy of Sciences of the United States of America. 1998; 95(11):6331-6336.
31. Sipkins DA, Wei X, Wu JW, Runnels JM, Cote D, Means TK, Luster AD, Scadden DT and Lin CP. In vivo imaging of specialized bone marrow endothelial microdomains for tumour engraftment. Nature. 2005; 435(7044):969-973.
32. Deacon CF, Carr RD and Holst JJ. DPP-4 inhibitor therapy: new directions in the treatment of type 2 diabetes. Frontiers in bioscience : a journal and virtual library. 2008; 13:1780- 1794.
33. Rose JW. Anti-CD25 immunotherapy: regulating the regulators. Science translational medicine. 2012; 4(145):145fs125.
34. Jaras M, Johnels P, Hansen N, Agerstam H, Tsapogas P, Rissler M, Lassen C, Olofsson T, Bjerrum OW, Richter J and Fioretos T. Isolation and killing of candidate chronic myeloid leukemia stem cells by antibody targeting of IL-1 receptor accessory protein. Proceedings of the National Academy of Sciences of the United States of America. 2010; 107(37):16280-16285.
35. Barreyro L, Will B, Bartholdy B, Zhou L, Todorova TI, Stanley RF, Ben-Neriah S, Montagna C, Parekh S, Pellagatti A, Boultwood J, Paietta E, Ketterling RP, Cripe L, Fernandez HF, Greenberg PL, et al. Overexpression of IL-1 receptor accessory protein in stem and progenitor cells and outcome correlation in AML and MDS. Blood. 2012; 120(6):1290-1298.
36. Dinarello CA, Simon A and van der Meer JW. Treating inflammation by blocking interleukin-1 in a broad spectrum of diseases. Nature reviews Drug discovery. 2012; 11(8):633-652.
37. Ren R. Mechanisms of BCR-ABL in the pathogenesis of chronic myelogenous leukaemia. Nature reviews Cancer. 2005; 5(3):172-183.
38. Biernacki MA, Marina O, Zhang W, Liu F, Bruns I, Cai A, Neuberg D, Canning CM, Alyea EP, Soiffer RJ, Brusic V, Ritz J and Wu CJ. Efficacious immune therapy in chronic myelogenous leukemia (CML) recognizes antigens that are expressed on CML progenitor cells. Cancer research. 2010; 70(3):906-915.
39. Bruns I, Czibere A, Fischer JC, Roels F, Cadeddu RP, Buest S, Bruennert D, Huenerlituerkoglu AN, Stoecklein NH, Singh R, Zerbini LF, Jager M, Kobbe G, Gattermann N, Kronenwett R, Brors B, et al. The hematopoietic stem cell in chronic phase CML is characterized by a transcriptional profile resembling normal myeloid progenitor cells and reflecting loss of quiescence. Leukemia. 2009; 23(5):892- 899.
40. Flis K, Irvine D, Copland M, Bhatia R and Skorski T. Chronic myeloid leukemia stem cells display alterations in expression of genes involved in oxidative phosphorylation. Leukemia & lymphoma. 2012; 53(12):2474-2478.
41. Pienta KJ, Machiels JP, Schrijvers D, Alekseev B, Shkolnik M, Crabb SJ, Li S, Seetharam S, Puchalski TA, Takimoto C, Elsayed Y, Dawkins F and de Bono JS. Phase 2 study of carlumab (CNTO 888), a human monoclonal antibody against CC-chemokine ligand 2 (CCL2), in metastatic castration-resistant prostate cancer. Investigational new drugs. 2012.
42. Schwartz GK, LoRusso PM, Dickson MA, Randolph SS, Shaik MN, Wilner KD, Courtney R and O'Dwyer PJ. Phase I study of PD 0332991, a cyclin-dependent kinase inhibitor, administered in 3-week cycles (Schedule 2/1). British journal of cancer. 2011; 104(12):1862-1868.
43. Flaherty KT, Lorusso PM, Demichele A, Abramson VG, Courtney R, Randolph SS, Shaik MN, Wilner KD, O'Dwyer PJ and Schwartz GK. Phase I, dose-escalation trial of the oral cyclin-dependent kinase 4/6 inhibitor PD 0332991, administered using a 21-day schedule in patients with advanced cancer. Clinical cancer research : an official journal of the American Association for Cancer Research. 2012; 18(2):568-576.
44. Monteleone G, Fantini MC, Onali S, Zorzi F, Sancesario G, Bernardini S, Calabrese E, Viti F, Monteleone I, Biancone L and Pallone F. Phase I clinical trial of Smad7 knockdown using antisense oligonucleotide in patients with active Crohn's disease. Molecular therapy : the journal of the American Society of Gene Therapy. 2012; 20(4):870-876.
45. Zhu X, Wang L, Zhang B, Li J, Dou X and Zhao RC. TGFbeta1- induced PI3K/Akt/NF-kappaB/MMP9 signalling pathway is activated in Philadelphia chromosome-positive chronic myeloid leukaemia hemangioblasts. Journal of biochemistry. 2011; 149(4):405-414.
46. Naka K, Hoshii T, Muraguchi T, Tadokoro Y, Ooshio T, Kondo Y, Nakao S, Motoyama N and Hirao A. TGF-beta- FOXO signalling maintains leukaemia-initiating cells in chronic myeloid leukaemia. Nature. 2010; 463(7281):676- 680.
47. Moller GM, Frost V, Melo JV and Chantry A. Upregulation of the TGFbeta signalling pathway by Bcr-Abl: implications for haemopoietic cell growth and chronic myeloid leukaemia. FEBS letters. 2007; 581(7):1329-1334.
48. Roberts AB and Wakefield LM. The two faces of transforming growth factor beta in carcinogenesis. Proceedings of the National Academy of Sciences of the United States of America. 2003; 100(15):8621-8623.
49. Bierie B and Moses HL. Tumour microenvironment: TGFbeta: the molecular Jekyll and Hyde of cancer. Nature reviews Cancer. 2006; 6(7):506-520.
50. Storey JD. A direct approach to false discovery rates. J R Statist Soc B. 2002; 64(Part 3):479-498.