Differential sensitivity to jak inhibitory drugs by isogenic human erythroblasts and hematopoietic progenitors generated from patient-specific induced pluripotent stem cells

Stem Cells

Volumn 32, Issue 1, 2014, Pages 269-278

  Ye, Zhaohui ^a   Liu, Cyndi F ^a   Lanikova, Lucie ^b   Dowey, Sarah N ^a   He, Chaoxia ^a   Huang, Xiaosong ^a   Brodsky, Robert A ^a   Spivak, Jerry L ^a   Prchal, Josef T ^b   Cheng, Linzhao ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Erythropoiesis; Hematopoietic malignancies; Hematopoietic progenitor cells; Induced pluripotent stem cells; Preclinical drug evaluation

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; CD34 ANTIGEN; CD45 ANTIGEN; FEDRATINIB; FIBROBLAST GROWTH FACTOR 2; JANUS KINASE 2; JANUS KINASE INHIBITOR; MOMELOTINIB; RUXOLITINIB; VASCULOTROPIN;

ARTICLE; BLOOD CELL; CELL CLONE; CELL DIFFERENTIATION; CELL RENEWAL; COLONY FORMING UNIT; CONTROLLED STUDY; DISEASE COURSE; DRUG SCREENING; DRUG SENSITIVITY; ERYTHROBLAST; ERYTHROID CELL; ERYTHROPOIESIS; FLOW CYTOMETRY; GENOTYPE; HEMATOPOIETIC STEM CELL; HETEROZYGOSITY; HOMOZYGOSITY; HUMAN; HUMAN CELL; NEUTROPHIL; PERIPHERAL BLOOD MONONUCLEAR CELL; PLURIPOTENT STEM CELL; SICKLE CELL ANEMIA; SOMATIC MUTATION;

ERYTHROPOIESIS; HEMATOPOIETIC MALIGNANCIES; HEMATOPOIETIC PROGENITOR CELLS; INDUCED PLURIPOTENT STEM CELLS; PRECLINICAL DRUG EVALUATION;

CELL DIFFERENTIATION; ERYTHROBLASTS; ERYTHROPOIESIS; HEMATOPOIESIS; HEMATOPOIETIC STEM CELLS; HUMANS; INDUCED PLURIPOTENT STEM CELLS; JANUS KINASE 2; PROTEIN KINASE INHIBITORS;

EID: 84891820810     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.1545     Document Type: Article

References (50)

1. Yamanaka S. Induced pluripotent stem cells: Past, present, and future. Cell Stem Cell 2012;10:678-684.
2. Trounson A, Shepard KA, DeWitt ND. Human disease modeling with induced pluripotent stem cells. Curr Opin Genet Dev 2012;22:509-516.
3. Ye Z, Chou BK, Cheng L. Promise and challenges of human iPSC-based hematologic disease modeling and treatment. Int J Hematol 2012;95:601-609.
4. Zou J, Sweeney CL, Chou BK et al. Oxidase-deficient neutrophils from X-linked chronic granulomatous disease iPS cells: Functional correction by zinc finger nucleasemediated safe harbor targeting. Blood 2011; 117:5561-5572.
5. Zou J, Mali P, Huang X et al. Site-specific gene correction of a point mutation in human iPS cells derived from an adult patient with sickle cell disease. Blood 2011;118:4599-4608.
6. Sebastiano V, Maeder ML, Angstman JF et al. In situ genetic correction of the sickle cell anemia mutation in human induced pluripotent stem cells using engineered zinc finger nucleases. Stem Cells 2011;29:1717-1726.
7. Raya A, Rodriguez-Piza I, Guenechea G et al. Disease-corrected haematopoietic progenitors from Fanconi anaemia induced pluripotent stem cells. Nature 2009;460:53-59.
8. Müller LU, Milsom MD, Harris CE et al. Overcoming reprogramming resistance of Fanconi anemia cells. Blood 2012;119:5449-5457.
9. Yung SK, Tilgner K, Ledran MH et al. Brief report: Human pluripotent stem cell models of fanconi anemia deficiency reveal an important role for fanconi anemia proteins in cellular reprogramming and survival of hematopoietic progenitors. Stem Cells 2013;31:1022-1029.
10. Chou BK, Mali P, Huang X et al. Efficient human iPS cell derivation by a nonintegrating plasmid from blood cells with unique epigenetic and gene expression signatures. Cell Res 2011;21:518-529.
11. Dowey SN, Huang X, Chou BK et al. Generation of integration-free human induced pluripotent stem cells from postnatal blood mononuclear cells by plasmid vector expression. Nat Protoc 2012;7:2013-2021.
12. Hu K, Yu J, Suknuntha K et al. 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.
13. Kralovics R, Teo S, Li S et al. Acquisition of the V617F mutation of JAK2 is a late genetic event in a subset of patients with myeloproliferative disorders. Blood 2006;108: 1377-1380.
14. Nussenzveig RH, Swierczek SI, Jelinek J et al. Polycythemia vera is not initiated by JAK2V617F mutation. Exp Hematol 2007;35: 32-38.
15. Kaufman D. Toward clinical therapies utilizing hematopoietic cells derived from human pluripotent stem cells. Blood 2009; 114:3513-3523.
16. Dameshek W. Some speculations on the myeloproliferative syndromes. Blood 1951;6: 372-375.
17. Spivak JL. Polycythemia vera: Myths, mechanisms, and management. Blood 2002; 100:4272-4290.
18. Skoda R. The genetic basis of myeloproliferative disorders. Hematol Am Soc Hematol Educ Program 2007:1-10.
19. Levine R, Gilliland D. Myeloproliferative disorders. Blood 2008;112:2190-2198.
20. Prchal JF, Prchal JT. Molecular basis for polycythemia. Curr Opin Hematol 1999;6: 100-109.
21. Lee G, Papapetrou EP, Kim H et al. Modelling pathogenesis and treatment of familial dysautonomia using patient-specific iPSCs. Nature 2009;461:402-406.
22. Lee G, Ramirez CN, Kim H et al. Largescale screening using familial dysautonomia induced pluripotent stem cells identifies compounds that rescue IKBKAP expression. Nat Biotechnol 2012;30:1244-1248.
23. Choi SM, Kim Y, Shim JS et al. Efficient drug screening and gene correction for treating liver disease using patient-specific stem cells. Hepatology 2013;57:2458-2468.
24. Kralovics R, Stockton D, Prchal J. Clonal hematopoiesis in familial polycythemia vera suggests the involvement of multiple mutational events in the early pathogenesis of the disease. Blood 2003;102:3793-3796.
25. Landgren O, Goldin LR, Kristinsson SY et al. Increased risks of polycythemia vera, essential thrombocythemia, and myelofibrosis among 24,577 first-degree relatives of 11,039 patients with myeloproliferative neoplasms in Sweden. Blood 2008;112:2199-2204.
26. Jones A, Chase A, Silver R et al. JAK2 haplotype is a major risk factor for the development of myeloproliferative neoplasms. Nat Genet 2009;41:446-449.
27. Olcaydu D, Harutyunyan A, Jäger R et al. A common JAK2 haplotype confers susceptibility to myeloproliferative neoplasms. Nat Genet 2009;41:450-454.
28. Kilpivaara O, Mukherjee S, Schram A et al. A germline JAK2 SNP is associated with predisposition to the development of JAK2(V617F)-positive myeloproliferative neoplasms. Nat Genet 2009;41:455-459.
29. James C, Ugo V, Le Couedic J et al. A unique clonal JAK2 mutation leading to constitutive signalling causes polycythaemia vera. Nature 2005;434:1144-1148.
30. Kralovics R, Passamonti F, Buser A et al. A gain-of-function mutation of JAK2 in myeloproliferative disorders. N Engl J Med 2005; 352:1779-1790.
31. Levine R, Wadleigh M, Cools J et al. Activating mutation in the tyrosine kinase JAK2 in polycythemia vera, essential thrombocythemia, and myeloid metaplasia with myelofibrosis. Cancer Cell 2005;7:387-397.
32. Zhao R, Xing S, Li Z et al. Identification of an acquired JAK2 mutation in polycythemia vera. J Biol Chem 2005;280:22788-22792.
33. Ye Z, Zhan H, Mali P et al. Humaninduced pluripotent stem cells from blood cells of healthy donors and patients with acquired blood disorders. Blood 2009;114: 5473-5480.
34. Verstovsek S, Kantarjian H, Mesa RA et al. Safety and efficacy of INCB018424, a JAK1 and JAK2 inhibitor, in myelofibrosis. N Engl J Med 2010;363:1117-1127.
35. Verstovsek S, Mesa RA, Gotlib J et al. A double-blind, placebo-controlled trial of ruxolitinib for myelofibrosis. N Engl J Med 2012; 366:799-807.
36. Verstovsek S, Kantarjian HM, Estrov Z et al. Long-term outcomes of 107 patients with myelofibrosis receiving JAK1/JAK2 inhibitor ruxolitinib: Survival advantage in comparison to matched historical controls. Blood 2012;120:1202-1209.
37. Harrison C, Kiladjian JJ, Al-Ali HK et al. JAK inhibition with ruxolitinib versus best available therapy for myelofibrosis. N Engl J Med 2012;366:787-798.
38. Geron I, Abrahamsson AE, Barroga CF et al. Selective inhibition of JAK2-driven erythroid differentiation of polycythemia vera progenitors. Cancer Cell 2008;13:321-330.
39. Lasho TL, Tefferi A, Hood JD et al. TG101348, a JAK2-selective antagonist, inhibits primary hematopoietic cells derived from myeloproliferative disorder patients with JAK2V617F, MPLW515K Or JAK2 Exon 12 mutations as well as mutation negative patients. Leukemia 2008;22:1790-1792.
40. Pardanani A, Gotlib JR, Jamieson C et al. Safety and efficacy of TG101348, a selective JAK2 inhibitor, in myelofibrosis. J Clin Oncol 2011;29:789-796.
41. Pardanani A, Lasho T, Smith G et al. CYT387, a selective JAK1/JAK2 inhibitor: In vitro assessment of kinase selectivity and preclinical studies using cell lines and primary cells from polycythemia vera patients. Leukemia 2009;23:1441-1445.
42. Pardanani A, Laborde RR, Lasho TL et al. Safety and efficacy of CYT387, a JAK1 and JAK2 inhibitor, in myelofibrosis. Leukemia 2013;27:1322-1327.
43. Moliterno A, Williams D, Rogers O et al. Molecular mimicry in the chronic myeloproliferative disorders: Reciprocity between quantitative JAK2 V617F and Mpl expression. Blood 2006;108:3913-3915.
44. Ng E, Davis R, Stanley E et al. A protocol describing the use of a recombinant proteinbased, animal product-free medium (APEL) for human embryonic stem cell differentiation as spin embryoid bodies. Nat Protoc 2008;3:768-776.
45. Moliterno A, Williams D, Rogers O et al. Phenotypic variability within the JAK2 V617Fpositive MPD: Roles of progenitor cell and neutrophil allele burdens. Exp Hematol 2008; 36:1480-1486.
46. Ugo V, Marzac C, Teyssandier I et al. Multiple signaling pathways are involved in erythropoietin-independent differentiation of erythroid progenitors in polycythemia vera. Exp Hematol 2004;32:179-187.
47. Prchal JF, Axelrad AA. Letter: Bonemarrow responses in polycythemia vera. N Engl J Med 1974;290:1382.
48. Jamieson CH, Gotlib J, Durocher JA et al. The JAK2 V617F mutation occurs in hematopoietic stem cells in polycythemia vera and predisposes toward erythroid differentiation. Proc Natl Acad Sci USA 2006;103: 6224-6229.
49. Ishii T, Bruno E, Hoffman R et al. Involvement of various hematopoietic-cell lineages by the JAK2V617F mutation in polycythemia vera. Blood 2006;108:3128-3134.
50. Novelli E, Cheng L, Yang Y et al. Ex vivo culture of cord blood CD341 cells expands progenitor cell numbers, preserves engraftment capacity in nonobese diabetic/ severe combined immunodeficient mice, and enhances retroviral transduction efficiency. Hum Gene Ther 1999;10:2927-2940.