Congenital amegakaryocytic thrombocytopenia iPS cells exhibit defective MPL-mediated signaling

Journal of Clinical Investigation

Volumn 123, Issue 9, 2013, Pages 3802-3814

  Hirata, Shinji ^a   Takayama, Naoya ^a   Jono Ohnishi, Ryoko ^a   Endo, Hiroshi ^a,b   Nakamura, Sou ^a   Dohda, Takeaki ^a   Nishi, Masanori ^c   Hamazaki, Yuhei ^c   Ishii, Ei Ichi ^d   Kaneko, Shin ^a,b   Otsu, Makoto ^b   Nakauchi, Hiromitsu ^b   Kunishima, Shinji ^e   Eto, Koji ^a,b  

^a KYOTO UNIVERSITY   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c SAGA UNIVERSITY   (Japan)

^d EHIME UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^e NATIONAL HOSPITAL ORGANIZATION NAGOYA MEDICAL CENTER   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CD34 ANTIGEN; FIBRINOGEN RECEPTOR; MEMBRANE PROTEIN; MPL PROTEIN; RETROVIRUS VECTOR; TRANSCRIPTION FACTOR FLI 1; UNCLASSIFIED DRUG; FLI1 PROTEIN, HUMAN; MPL PROTEIN, HUMAN; THROMBIN RECEPTOR; THROMBOPOIETIN RECEPTOR;

ARTICLE; CELL DIFFERENTIATION; CONGENITAL AMEGAKARYOCYTIC THROMBOCYTOPENIA; CONTROLLED STUDY; ERYTHROCYTE; ERYTHROPOIESIS; GENE OVEREXPRESSION; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; MEGAKARYOCYTE; MEGAKARYOPOIESIS; MULTIPOTENT HEMATOPOIETIC PROGENITOR; PHENOTYPE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; THROMBOCYTOPENIA; TRANSCRIPTION REGULATION; CELL CULTURE; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MISSENSE MUTATION; PATHOLOGY; PHYSIOLOGY; THROMBOCYTE;

BLOOD PLATELETS; CELL DIFFERENTIATION; CELLS, CULTURED; ERYTHROCYTES; GENE EXPRESSION REGULATION; HEMATOPOIESIS; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MEGAKARYOCYTES; MUTATION, MISSENSE; PHENOTYPE; PLATELET GLYCOPROTEIN GPIB-IX COMPLEX; PROTO-ONCOGENE PROTEIN C-FLI-1; RECEPTORS, THROMBOPOIETIN; SIGNAL TRANSDUCTION; THROMBOCYTOPENIA; TRANSCRIPTION, GENETIC;

EID: 84883495730     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI64721     Document Type: Article

References (56)

1. Yoshihara H, et al. Thrombopoietin/MPL signaling regulates hematopoietic stem cell quiescence and interaction with the osteoblastic niche. Cell Stem Cell. 2007;1(6):685-697. (Pubitemid 350215333)
2. Qian H, et al. Critical role of thrombopoietin in maintaining adult quiescent hematopoietic stem cells. Cell Stem Cell. 2007;1(6):671-684. (Pubitemid 350215331)
3. de Sauvage FJ, et al. Physiological regulation of early and late stages of megakaryocytopoiesis by thrombopoietin. J Exp Med. 1996;183(2):651-656.
4. Alexander WS, Roberts AW, Nicola NA, Li R, Metcalf D. Deficiencies in progenitor cells of multiple hematopoietic lineages and defective megakaryocytopoiesis in mice lacking the thrombopoietic receptor c-Mpl. Blood. 1996;87(6):2162-2170.
5. Kaushansky K. The molecular mechanisms that control thrombopoiesis. J Clin Invest. 2005;115(12):3339-3347. (Pubitemid 43121817)
6. Drachman JG, Griffin JD, Kaushansky K. The c-Mpl ligand (thrombopoietin) stimulates tyrosine phosphorylation of Jak2, Shc, and c-Mpl. J Biol Chem. 1995;270(10):4979-4982.
7. Ihara K, et al. Identification of mutations in the c-mpl gene in congenital amegakaryocytic thrombocytopenia. Proc Natl Acad Sci U S A. 1999;96(6):3132-3136. (Pubitemid 29148856)
8. Ballmaier M, et al. c-mpl mutations are the cause of congenital amegakaryocytic thrombocytopenia. Blood. 2001;97(1):139-146. (Pubitemid 32061253)
9. King S, Germeshausen M, Strauss G, Welte K, Ballmaier M. Congenital amegakaryocytic thrombocytopenia: a retrospective clinical analysis of 20 patients. Br J Haematol. 2005;131(5):636-644. (Pubitemid 43899631)
10. Carver-Moore K, et al. Low levels of erythroid and myeloid progenitors in thrombopoietin-and c-mpl-deficient mice. Blood. 1996;88(3):803-808. (Pubitemid 26333299)
11. Takayama N, Eto K. Pluripotent stem cells reveal the developmental biology of human megakaryocytes provide a source of platelets for clinical application. Cell Mol Life Sci. 2012;69(20):3419-3428.
12. Park IH, et al. Disease-specific induced pluripotent stem cells. Cell. 2008;134(5):877-886.
13. Raya A, et al. Disease-corrected haematopoietic progenitors from Fanconi anaemia induced pluripotent stem cells. Nature. 2009;460(7251):53-59.
14. Ye Z, et al. Human-induced pluripotent stem cells from blood cells of healthy donors and patients with acquired blood disorders. Blood. 2009;114(27):5473-5480.
15. Zou J, Mali P, Huang X, Dowey SN, Cheng L. Site-specific gene correction of a point mutation in human iPS cells derived from an adult patient with sickle cell disease. Blood. 2011;118(17):4599-4608.
16. Zou J, et al. Gene targeting of a disease-related gene in human induced pluripotent stem and embryonic stem cells. Cell Stem Cell. 2009;5(1):97-110.
17. Sun N, et al. Patient-specific induced pluripotent stem cells as a model for familial dilated cardiomyopathy. Sci Transl Med. 2012;4(130):130ra47.
18. Lu SJ, et al. Biologic properties and enucleation of red blood cells from human embryonic stem cells. Blood. 2008;112(12):4475-4484.
19. Kobari L, et al. Human induced pluripotent stem cells can reach complete terminal maturation: in vivo and in vitro evidence in the erythropoietic differentiation model. Haematologica. 2012;97(12):1795-1803.
20. Chang CJ, et al. Production of embryonic and fetal-like red blood cells from human induced pluripotent stem cells. PloS One. 2011;6(10):e25761.
21. Muraoka K, et al. Successful bone marrow transplantation in a patient with c-mpl-mutated congenital amegakaryocytic thrombocytopenia from a carrier donor. Pediatr Transplant. 2005;9(1):101-103. (Pubitemid 40238973)
22. Takayama N, et al. Generation of functional platelets from human embryonic stem cells in vitro via ES-sacs, VEGF-promoted structures that concentrate hematopoietic progenitors. Blood. 2008;111(11):5298-5306.
23. Takayama N, et al. Transient activation of c-MYC expression is critical for efficient platelet generation from human induced pluripotent stem cells. J Exp Med. 2010;207(13):2817-2830.
24. Takayama N, Eto K. In vitro generation of megakaryocytes and platelets from human embryonic stem cells and induced pluripotent stem cells. Methods Mol Biol. 2012;788:205-217.
25. Ory DS, Neugeboren BA, Mulligan RC. A stable human-derived packaging cell line for production of high titer retrovirus/vesicular stomatitis virus G pseudotypes. Proc Natl Acad Sci U S A. 1996;93(21):11400-11406. (Pubitemid 26347133)
26. Muraoka K, et al. Defective response to thrombopoietin and impaired expression of c-mpl mRNA of bone marrow cells in congenital amegakaryocytic thrombocytopenia. Br J Haematol. 1997;96(2):287-292. (Pubitemid 27077361)
27. Vodyanik MA, Thomson JA, Slukvin II. Leukosialin (CD43) defines hematopoietic progenitors in human embryonic stem cell differentiation cultures. Blood. 2006;108(6):2095-2105. (Pubitemid 44395026)
28. Klimchenko O, et al. A common bipotent progenitor generates the erythroid and megakaryocyte lineages in embryonic stem cell-derived primitive hematopoiesis. Blood. 2009;114(8):1506-1517.
29. Nishikii H, et al. Metalloproteinase regulation improves in vitro generation of efficacious platelets from mouse embryonic stem cells. J Exp Med. 2008;205(8):1917-1927.
30. Kobayashi M, Laver JH, Kato T, Miyazaki H, Ogawa M. Recombinant human thrombopoietin (Mpl ligand) enhances proliferation of erythroid progenitors. Blood. 1995;86(7):2494-2499.
31. Parekh C, et al. Novel pathways to erythropoiesis induced by dimerization of intracellular C-Mpl in human hematopoietic progenitors. Stem Cells. 2012;30(4):697-708.
32. Lu J, et al. MicroRNA-mediated control of cell fate in megakaryocyte-erythrocyte progenitors. Dev Cell. 2008;14(6):843-853. (Pubitemid 351757199)
33. Bouilloux F, et al. EKLF restricts megakaryocytic differentiation at the benefit of erythrocytic differentiation. Blood. 2008;112(3):576-584.
34. Dore LC, Crispino JD. Transcription factor networks in erythroid cell and megakaryocyte development. Blood. 2011;118(2):231-239.
35. Starck J, et al. Functional cross-antagonism between transcription factors FLI-1 and EKLF. Mol Cell Biol. 2003;23(4):1390-1402. (Pubitemid 36177047)
36. Wang Y, Fan PS, Kahaleh B. Association between enhanced type I collagen expression and epigenetic repression of the FLI1 gene in scleroderma fibroblasts. Arthritis Rheum. 2006;54(7):2271-2279. (Pubitemid 44051084)
37. Israel MA, et al. Probing sporadic and familial Alzheimer's disease using induced pluripotent stem cells. Nature. 2012;482(7384):216-220.
38. Dimos JT, et al. Induced pluripotent stem cells generated from patients with ALS can be differentiated into motor neurons. Science. 2008;321(5893):1218- 1221.
39. Bilican B, et al. Mutant induced pluripotent stem cell lines recapitulate aspects of TDP-43 proteinopathies and reveal cell-specific vulnerability. Proc Natl Acad Sci U S A. 2012;109(15):5803-5808.
40. Yagi T, et al. Modeling familial Alzheimer's disease with induced pluripotent stem cells. Hum Mol Genet. 2011;20(23):4530-4539.
41. Isken O, Maquat LE. The multiple lives of NMD factors: balancing roles in gene and genome regulation. Nat Rev Genet. 2008;9(9):699-712.
42. Olnes MJ, et al. Eltrombopag and improved hematopoiesis in refractory aplastic anemia. N Engl J Med. 2012;367(1):11-19.
43. Fielder PJ, et al. Regulation of thrombopoietin levels by c-mpl-mediated binding to platelets. Blood. 1996;87(6):2154-2161.
44. Stoffel R, Wiestner A, Skoda RC. Thrombopoietin in thrombocytopenic mice: evidence against regulation at the mRNA level and for a direct regulatory role of platelets. Blood. 1996;87(2):567-573. (Pubitemid 26030312)
45. Hitchcock IS, Chen MM, King JR, Kaushansky K. YRRL motifs in the cytoplasmic domain of the thrombopoietin receptor regulate receptor internalization and degradation. Blood. 2008;112(6):2222-2231.
46. Patel SR, Hartwig JH, Italiano JE Jr. The biogenesis of platelets from megakaryocyte proplatelets. J Clin Invest. 2005;115(12):3348-3354. (Pubitemid 43121818)
47. Pikman Y, et al. MPLW515L is a novel somatic activating mutation in myelofibrosis with myeloid metaplasia. PLoS Med. 2006;3(7):e270.
48. Guglielmelli P, et al. Anaemia characterises patients with myelofibrosis harbouring Mpl mutation. Br J Haematol. 2007;137(3):244-247. (Pubitemid 46537640)
49. Tefferi A. JAK and MPL mutations in myeloid malignancies. Leuk Lymphoma. 2008;49(3):388-397. (Pubitemid 351298324)
50. Kohn AD, Summers SA, Birnbaum MJ, Roth RA. Expression of a constitutively active Akt Ser/Thr kinase in 3T3-L1 adipocytes stimulates glucose uptake and glucose transporter 4 translocation. J Biol Chem. 1996;271(49):31372-31378. (Pubitemid 26408588)
51. Kato Y, et al. Selective activation of STAT5 unveils its role in stem cell self-renewal in normal and leukemic hematopoiesis. J Exp Med. 2005;202(1):169-179. (Pubitemid 41002919)
52. Olthof SG, Fatrai S, Drayer AL, Tyl MR, Vellenga E, Schuringa JJ. Downregulation of signal transducer and activator of transcription 5 (STAT5) in CD34+ cells promotes megakaryocytic development, whereas activation of STAT5 drives erythropoiesis. Stem Cells. 2008;26(7):1732-1742.
53. Amabile G, et al. In vivo generation of transplantable human hematopoietic cells from induced pluripotent stem cells. Blood. 2013;121(8):1255-1264.
54. Suzuki N, et al. Generation of engraftable hematopoietic stem cells from induced pluripotent stem cells by way of teratoma formation molecular therapy: the Journal Of The American Society Of Gene Therapy [published online ahead of print May 14, 2013]. Mol Ther. doi:10.1038/mt.2013.71.
55. Kitamura T, et al. Retrovirus-mediated gene transfer and expression cloning: powerful tools in functional genomics. Exp Hematol. 2003;31(11):1007-1014. (Pubitemid 37329742)
56. Eto K, et al. The WAVE2/Abi1 complex differentially regulates megakaryocyte development and spreading: implications for platelet biogenesis and spreading machinery. Blood. 2007;110(10):3637-3647. (Pubitemid 350159632)