Discovery of survival factor for primitive chronic myeloid leukemia cells using induced pluripotent stem cells

Stem Cell Research

Volumn 15, Issue 3, 2015, Pages 678-693

  Suknuntha, Kran ^a   Ishii, Yuki ^b   Tao, Lihong ^c   Hu, Kejin ^c   McIntosh, Brian E ^d   Yang, David ^a   Swanson, Scott ^d   Stewart, Ron ^d   Wang, Jean Y J ^b   Thomson, James ^a,d,e   Slukvin, Igor ^a,c  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c UNIVERSITY OF WISCONSIN   (United States)

^d MORGRIDGE INSTITUTE FOR RESEARCH   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN; IMATINIB; OLFACTOMEDIN 4; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BONE MARROW; CANCER RESISTANCE; CELL GROWTH; CELL PROLIFERATION; CELL SURVIVAL; CHRONIC MYELOID LEUKEMIA; CONTROLLED STUDY; HEMATOPOIETIC CELL; HUMAN; HUMAN CELL; LEUKEMIA STEM CELL; LONG TERM SURVIVAL; MOUSE; MYELOID LEUKEMIA CELL LINE; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SOMATIC CELL; STEM CELL; SURVIVAL FACTOR; CYTOLOGY; IMMUNOLOGY; INDUCED PLURIPOTENT STEM CELL; METABOLISM; TUMOR CELL CULTURE;

HUMANS; INDUCED PLURIPOTENT STEM CELLS; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; TUMOR CELLS, CULTURED;

EID: 84946542062     PISSN: 18735061     EISSN: 18767753     Source Type: Journal    
DOI: 10.1016/j.scr.2015.10.015     Document Type: Article

References (68)

1. Bedel A., Pasquet J.M., Lippert E., Taillepierre M., Lagarde V., Dabernat S., Dubus P., Charaf L., Beliveau F., de Verneuil H., et al. Variable behavior of iPSCs derived from CML patients for response to TKI and hematopoietic differentiation. PLoS One 2013, 8:e71596.
2. Bellodi C., Lidonnici M.R., Hamilton A., Helgason G.V., Soliera A.R., Ronchetti M., Galavotti S., Young K.W., Selmi T., Yacobi R., et al. Targeting autophagy potentiates tyrosine kinase inhibitor-induced cell death in Philadelphia chromosome-positive cells, including primary CML stem cells. J. Clin. Invest. 2009, 119:1109-1123.
3. Bhatia R., Munthe H.A., Forman S.J. Abnormal growth factor modulation of beta1-integrin-mediated adhesion in chronic myelogenous leukaemia haematopoietic progenitors. Br. J. Haematol. 2001, 115:845-853.
4. Carette J.E., Pruszak J., Varadarajan M., Blomen V.A., Gokhale S., Camargo F.D., Wernig M., Jaenisch R., Brummelkamp T.R. Generation of iPSCs from cultured human malignant cells. Blood 2010, 115:4039-4042.
5. Chin K.L., Aerbajinai W., Zhu J., Drew L., Chen L., Liu W., Rodgers G.P. The regulation of OLFM4 expression in myeloid precursor cells relies on NF-kappaB transcription factor. Br. J. Haematol. 2008, 143:421-432.
6. Choi K.D., Vodyanik M.A., Slukvin I.I. Generation of mature human myelomonocytic cells through expansion and differentiation of pluripotent stem cell-derived lin-CD34+CD43+CD45+ progenitors. J. Clin. Invest. 2009, 119:2818-2829.
7. Choi K.D., Yu J., Smuga-Otto K., Salvagiotto G., Rehrauer W., Vodyanik M., Thomson J., Slukvin I. Hematopoietic and endothelial differentiation of human induced pluripotent stem cells. Stem Cells 2009, 27:559-567.
8. Clemmensen S.N., Bohr C.T., Rorvig S., Glenthoj A., Mora-Jensen H., Cramer E.P., Jacobsen L.C., Larsen M.T., Cowland J.B., Tanassi J.T., et al. Olfactomedin 4 defines a subset of human neutrophils. J. Leukoc. Biol. 2012, 91:495-500.
9. Copland M., Hamilton A., Elrick L.J., Baird J.W., Allan E.K., Jordanides N., Barow M., Mountford J.C., Holyoake T.L. Dasatinib (BMS-354825) targets an earlier progenitor population than imatinib in primary CML but does not eliminate the quiescent fraction. Blood 2006, 107:4532-4539.
10. Corbin A.S., Agarwal A., Loriaux M., Cortes J., Deininger M.W., Druker B.J. Human chronic myeloid leukemia stem cells are insensitive to imatinib despite inhibition of BCR-ABL activity. J. Clin. Invest. 2011, 121:396-409.
11. Cosgun K.N., Rahmig S., Mende N., Reinke S., Hauber I., Schafer C., Petzold A., Weisbach H., Heidkamp G., Purbojo A., et al. Kit Regulates HSC Engraftment across the Human-Mouse Species Barrier. Cell Stem Cell 2014.
12. Druker B.J., Talpaz M., Resta D.J., Peng B., Buchdunger E., Ford J.M., Lydon N.B., Kantarjian H., Capdeville R., Ohno-Jones S., et al. Efficacy and safety of a specific inhibitor of the BCR-ABL tyrosine kinase in chronic myeloid leukemia. N. Engl. J. Med. 2001, 344:1031-1037.
13. Druker B.J., Guilhot F., O'Brien S.G., Gathmann I., Kantarjian H., Gattermann N., Deininger M.W., Silver R.T., Goldman J.M., Stone R.M., et al. Five-year follow-up of patients receiving imatinib for chronic myeloid leukemia. N. Engl. J. Med. 2006, 355:2408-2417.
14. Gandre-Babbe S., Paluru P., Aribeana C., Chou S.T., Bresolin S., Lu L., Sullivan S.K., Tasian S.K., Weng J., Favre H., et al. Patient-derived induced pluripotent stem cells recapitulate hematopoietic abnormalities of juvenile myelomonocytic leukemia. Blood 2013, 121:4925-4929.
15. Graham S.M., Jorgensen H.G., Allan E., Pearson C., Alcorn M.J., Richmond L., Holyoake T.L. Primitive, quiescent, Philadelphia-positive stem cells from patients with chronic myeloid leukemia are insensitive to STI571 in vitro. Blood 2002, 99:319-325.
16. Grskovic M., Javaherian A., Strulovici B., Daley G.Q. Induced pluripotent stem cells--opportunities for disease modelling and drug discovery. Nat. Rev. Drug Discov. 2011, 10:915-929.
17. Hasselbalch H.C., Skov V., Stauffer Larsen T., Thomassen M., Hasselbalch Riley C., Jensen M.K., Bjerrum O.W., Kruse T.A. Transcriptional profiling of whole blood identifies a unique 5-gene signature for myelofibrosis and imminent myelofibrosis transformation. PLoS One 2014, 9:e85567.
18. Hochedlinger K., Blelloch R., Brennan C., Yamada Y., Kim M., Chin L., Jaenisch R. Reprogramming of a melanoma genome by nuclear transplantation. Genes Dev. 2004, 18:1875-1885.
19. Holtz M.S., Slovak M.L., Zhang F., Sawyers C.L., Forman S.J., Bhatia R. Imatinib mesylate (STI571) inhibits growth of primitive malignant progenitors in chronic myelogenous leukemia through reversal of abnormally increased proliferation. Blood 2002, 99:3792-3800.
20. Holyoake T., Jiang X., Eaves C., Eaves A. Isolation of a highly quiescent subpopulation of primitive leukemic cells in chronic myeloid leukemia. Blood 1999, 94:2056-2064.
21. Holyoake T.L., Jiang X., Jorgensen H.G., Graham S., Alcorn M.J., Laird C., Eaves A.C., Eaves C.J. Primitive quiescent leukemic cells from patients with chronic myeloid leukemia spontaneously initiate factor-independent growth in vitro in association with up-regulation of expression of interleukin-3. Blood 2001, 97:720-728.
22. Hu K., Yu J., Suknuntha K., Tian S., Montgomery K., Choi K.D., Stewart R., Thomson J.A., Slukvin I.I. Efficient generation of transgene-free induced pluripotent stem cells from normal and neoplastic bone marrow and cord blood mononuclear cells. Blood 2011, 117:e109-e119.
23. Huang da W., Sherman B.T., Stephens R., Baseler M.W., Lane H.C., Lempicki R.A. DAVID gene ID conversion tool. Bioinformation 2008, 2:428-430.
24. Huang G., Lu H., Hao A., Ng D.C., Ponniah S., Guo K., Lufei C., Zeng Q., Cao X. GRIM-19, a cell death regulatory protein, is essential for assembly and function of mitochondrial complex I. Mol. Cell. Biol. 2004, 24:8447-8456.
25. Jiang X., Lopez A., Holyoake T., Eaves A., Eaves C. Autocrine production and action of IL-3 and granulocyte colony-stimulating factor in chronic myeloid leukemia. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:12804-12809.
26. Koshida S., Kobayashi D., Moriai R., Tsuji N., Watanabe N. Specific overexpression of OLFM4(GW112/HGC-1) mRNA in colon, breast and lung cancer tissues detected using quantitative analysis. Cancer Sci. 2007, 98:315-320.
27. Kumano K., Arai S., Hosoi M., Taoka K., Takayama N., Otsu M., Nagae G., Ueda K., Nakazaki K., Kamikubo Y., et al. Generation of induced pluripotent stem cells from primary chronic myelogenous leukemia patient samples. Blood 2012, 119:6234-6242.
28. Langmead B., Trapnell C., Pop M., Salzberg S.L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009, 10:R25.
29. Leng N., Dawson J.A., Thomson J.A., Ruotti V., Rissman A.I., Smits B.M., Haag J.D., Gould M.N., Stewart R.M., Kendziorski C. EBSeq: an empirical Bayes hierarchical model for inference in RNA-seq experiments. Bioinformatics 2013, 29:1035-1043.
30. Li B., Dewey C.N. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinforma. 2011, 12:323.
31. Li G., Chan T.M., Leung K.S., Lee K.H. A cluster refinement algorithm for motif discovery. IEEE/ACM Trans. Comput. Biol. Bioinforma. 2010, 7:654-668.
32. Li L., Wang L., Wang Z., Ho Y., McDonald T., Holyoake T.L., Chen W., Bhatia R. Activation of p53 by SIRT1 inhibition enhances elimination of CML leukemia stem cells in combination with imatinib. Cancer Cell 2012, 21:266-281.
33. Liu W., Chen L., Zhu J., Rodgers G.P. The glycoprotein hGC-1 binds to cadherin and lectins. Exp. Cell Res. 2006, 312:1785-1797.
34. Liu W., Lee H.W., Liu Y., Wang R., Rodgers G.P. Olfactomedin 4 is a novel target gene of retinoic acids and 5-aza-2'-deoxycytidine involved in human myeloid leukemia cell growth, differentiation, and apoptosis. Blood 2010, 116:4938-4947.
35. Liu R.H., Yang M.H., Xiang H., Bao L.M., Yang H.A., Yue L.W., Jiang X., Ang N., Wu L.Y., Huang Y. Depletion of OLFM4 gene inhibits cell growth and increases sensitization to hydrogen peroxide and tumor necrosis factor-alpha induced-apoptosis in gastric cancer cells. J. Biomed. Sci. 2012, 19:38.
36. Liu Y., Cheng H., Gao S., Zou Z., He F., Hu L., Hou D., Lu X., Li Y., Zhang H., et al. Reprogramming of MLL-AF9 leukemia cells into pluripotent stem cells. Leukemia 2013.
37. Mahon F.X., Rea D., Guilhot J., Guilhot F., Huguet F., Nicolini F., Legros L., Charbonnier A., Guerci A., Varet B., et al. 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. Lancet Oncol. 2010, 11:1029-1035.
38. McIntosh B.E., Brown M.E., Duffin B.E., Maufort J.P., Vereide D.T., Slukvin I.I., Thomson J.A. Non-irradiated NOD, B6.SCID Il2rg-/- KitW41/W41 (NBSGW) Mice Support Multi-lineage Engraftment of Human Hematopoietic Cells. Stem Cell Rep. 2014, (accepted for publication).
39. Miljkovic-Licina M., Hammel P., Garrido-Urbani S., Lee B.P., Meguenani M., Chaabane C., Bochaton-Piallat M.L., Imhof B.A. Targeting olfactomedin-like 3 inhibits tumor growth by impairing angiogenesis and pericyte coverage. Mol. Cancer Ther. 2012, 11:2588-2599.
40. Oh H.K., Tan A.L., Das K., Ooi C.H., Deng N.T., Tan I.B., Beillard E., Lee J., Ramnarayanan K., Rha S.Y., et al. Genomic loss of miR-486 regulates tumor progression and the OLFM4 antiapoptotic factor in gastric cancer. Clin. Cancer Res. 2011, 17:2657-2667.
41. Park I.H., Zhao R., West J.A., Yabuuchi A., Huo H., Ince T.A., Lerou P.H., Lensch M.W., Daley G.Q. Reprogramming of human somatic cells to pluripotency with defined factors. Nature 2008, 451:141-146. (Epub 2007 Dec 2023).
42. Park K.S., Kim K.K., Piao Z.H., Kim M.K., Lee H.J., Kim Y.C., Lee K.S., Lee J.H., Kim K.E. Olfactomedin 4 suppresses tumor growth and metastasis of mouse melanoma cells through downregulation of integrin and MMP genes. Mol. Cells 2012, 34:555-561.
43. Perlingeiro R.C., Kyba M., Daley G.Q. Clonal analysis of differentiating embryonic stem cells reveals a hematopoietic progenitor with primitive erythroid and adult lymphoid-myeloid potential. Development 2001, 128:4597-4604.
44. Petzer A.L., Eaves C.J., Lansdorp P.M., Ponchio L., Barnett M.J., Eaves A.C. Characterization of primitive subpopulations of normal and leukemic cells present in the blood of patients with newly diagnosed as well as established chronic myeloid leukemia. Blood 1996, 88:2162-2171.
45. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001, 29:e45.
46. Rais Y., Zviran A., Geula S., Gafni O., Chomsky E., Viukov S., Mansour A.A., Caspi I., Krupalnik V., Zerbib M., et al. Deterministic direct reprogramming of somatic cells to pluripotency. Nature 2013, 502:65-70.
47. Ramaraj P., Singh H., Niu N., Chu S., Holtz M., Yee J.K., Bhatia R. Effect of mutational inactivation of tyrosine kinase activity on BCR/ABL-induced abnormalities in cell growth and adhesion in human hematopoietic progenitors. Cancer Res. 2004, 64:5322-5331.
48. Ramos-Mejia V., Montes R., Bueno C., Ayllon V., Real P.J., Rodriguez R., Menendez P. Residual expression of the reprogramming factors prevents differentiation of iPSC generated from human fibroblasts and cord blood CD34+ progenitors. PLoS One 2012, 7:e35824.
49. Schemionek M., Elling C., Steidl U., Baumer N., Hamilton A., Spieker T., Gothert J.R., Stehling M., Wagers A., Huettner C.S., et al. BCR-ABL enhances differentiation of long-term repopulating hematopoietic stem cells. Blood 2010, 115:3185-3195.
50. Sebaugh J.L. Guidelines for accurate EC50/IC50 estimation. Pharm. Stat. 2011, 10:128-134.
51. Sloma I., Jiang X., Eaves A.C., Eaves C.J. Insights into the stem cells of chronic myeloid leukemia. Leukemia 2010, 24:1823-1833.
52. Slukvin I.I. Neoplastic blood cells become pluripotent. Blood 2009, 114:5409-5410.
53. Slukvin I.I. Hematopoietic specification from human pluripotent stem cells: current advances and challenges toward de novo generation of hematopoietic stem cells. Blood 2013, 122:4035-4046.
54. Takahashi K., Tanabe K., Ohnuki M., Narita M., Ichisaka T., Tomoda K., Yamanaka S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007, 131:861-872.
55. Thierry-Mieg D., Thierry-Mieg J. AceView: a comprehensive cDNA-supported gene and transcripts annotation. Genome Biol. 2006, 7(Suppl. 1):S12 11-14.
56. Tomarev S.I., Nakaya N. Olfactomedin domain-containing proteins: possible mechanisms of action and functions in normal development and pathology. Mol. Neurobiol. 2009, 40:122-138.
57. Udomsakdi C., Eaves C.J., Lansdorp P.M., Eaves A.C. Phenotypic heterogeneity of primitive leukemic hematopoietic cells in patients with chronic myeloid leukemia. Blood 1992, 80:2522-2530.
58. Udomsakdi C., Lansdorp P.M., Hogge D.E., Reid D.S., Eaves A.C., Eaves C.J. Characterization of primitive hematopoietic cells in normal human peripheral blood. Blood 1992, 80:2513-2521.
59. van der Flier L.G., Haegebarth A., Stange D.E., van de Wetering M., Clevers H. OLFM4 is a robust marker for stem cells in human intestine and marks a subset of colorectal cancer cells. Gastroenterology 2009, 137:15-17.
60. Vargaftig J., Taussig D.C., Griessinger E., Anjos-Afonso F., Lister T.A., Cavenagh J., Oakervee H., Gribben J., Bonnet D. Frequency of leukemic initiating cells does not depend on the xenotransplantation model used. Leukemia 2012, 26:858-860.
61. Verfaillie C.M., McCarthy J.B., McGlave P.B. Mechanisms underlying abnormal trafficking of malignant progenitors in chronic myelogenous leukemia. Decreased adhesion to stroma and fibronectin but increased adhesion to the basement membrane components laminin and collagen type IV. J. Clin. Invest. 1992, 90:1232-1241.
62. Vo L.T., Daley G.Q. De novo generation of HSCs from somatic and pluripotent stem cell sources. Blood 2015, 125:2641-2648.
63. Vodyanik M.A., Bork J.A., Thomson J.A., Slukvin I.I. Human embryonic stem cell-derived CD34+ cells: efficient production in the coculture with OP9 stromal cells and analysis of lymphohematopoietic potential. Blood 2005, 105:617-626.
64. Vodyanik M.A., Thomson J.A., Slukvin I.I. Leukosialin (CD43) defines hematopoietic progenitors in human embryonic stem cell differentiation cultures. Blood 2006, 108:2095-2105.
65. Ye Z., Zhan H., Mali P., Dowey S., Williams D.M., Jang Y.Y., Dang C.V., Spivak J.L., Moliterno A.R., Cheng L. Human-induced pluripotent stem cells from blood cells of healthy donors and patients with acquired blood disorders. Blood 2009, 114:5473-5480.
66. Yu J., Hu K., Smuga-Otto K., Tian S., Stewart R., Slukvin I.I., Thomson J.A. Human induced pluripotent stem cells free of vector and transgene sequences. Science 2009, 324:797-801.
67. Zhang J., Liu W.L., Tang D.C., Chen L., Wang M., Pack S.D., Zhuang Z., Rodgers G.P. Identification and characterization of a novel member of olfactomedin-related protein family, hGC-1, expressed during myeloid lineage development. Gene 2002, 283:83-93.
68. Zhang X., Huang Q., Yang Z., Li Y., Li C.Y. GW112, a novel antiapoptotic protein that promotes tumor growth. Cancer Res. 2004, 64:2474-2481.