KIT receptor gain-of-function in hematopoiesis enhances stem cell self-renewal and promotes progenitor cell expansion

Stem Cells

Volumn 31, Issue 8, 2013, Pages 1683-1695

  Deshpande, Shayu ^a   Bosbach, Benedikt ^a   Yozgat, Yasemin ^a   Park, Christopher Y ^a   Moore, Malcolm A S ^a   Besmer, Peter ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

Erythroid progenitors; Hematopoietic stem cells; Self renewal; Signal transduction

Indexed keywords

FLUOROURACIL; IMATINIB; STEM CELL FACTOR RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD; BONE MARROW; CONTROLLED STUDY; ERYTHROCYTOSIS; ERYTHROID PRECURSOR CELL; FEMALE; FETUS; FETUS LIVER; FLOW CYTOMETRY; GAIN OF FUNCTION MUTATION; GASTROINTESTINAL STROMAL TUMOR; HEMATOCRIT; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; MALE; MOUSE; NONHUMAN; POLYCYTHEMIA VERA; SPLEEN; SPLENECTOMY; STEM CELL; STEM CELL EXPANSION;

ERYTHROID PROGENITORS; HEMATOPOIETIC STEM CELLS; SELF-RENEWAL; SIGNAL TRANSDUCTION;

ANIMALS; CELL GROWTH PROCESSES; DISEASE MODELS, ANIMAL; ERYTHROID CELLS; FEMALE; FLUOROURACIL; HEMATOPOIESIS; HEMATOPOIETIC STEM CELLS; MALE; MICE; MICE, INBRED C57BL; PROTO-ONCOGENE PROTEINS C-KIT; SIGNAL TRANSDUCTION;

EID: 84883339152     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.1419     Document Type: Article

References (37)

1. Morrison SJ, Weissman IL. The long-term repopulating subset of hematopoietic stem cells is deterministic and isolatable by phenotype. Immunity 1994;1:661-673.
2. Sharma Y, Astle CM, Harrison DE. Heterozygous kit mutants with little or no apparent anemia exhibit large defects in overall hematopoietic stem cell function. Exp Hematol 2007;35:214-220.
3. Nocka K, Majumder S, Chabot B et al. Expression of c-kit gene products in known cellular targets of W mutations in normal and W mutant mice - evidence for an impaired c-kit kinase in mutant mice. Genes Dev 1989;3:816-826.
4. Besmer P. The kit ligand encoded at the murine Steel locus: A pleiotropic growth and differentiation factor. Curr Opin Cell Biol 1991;3: 939-946.
5. Russell ES. Hereditary anemias of the mouse: A review for geneticists. Adv Genet 1979;20:357-459.
6. Nocka K, Buck J, Levi E et al. Candidate ligand for the c-kit transmembrane kinase receptor: KL, a fibroblast derived growth factor stimulates mast cells and erythroid progenitors. EMBO J 1990;9:3287-3294.
7. Muta K, Krantz SB, Bondurant MC et al. Stem cell factor retards differentiation of normal human erythroid progenitor cells while stimulating proliferation. Blood 1995;86:572-580.
8. Besmer P. Kit-ligand-stem cell factor. New York, NY: Marcel Dekker, 1997:369-403.
9. Gerbaulet A, Wickenhauser C, Scholten J et al. Mast cell hyperplasia, Bcell malignancy, and intestinal inflammation in mice with conditional expression of a constitutively active kit. Blood 2011;117:2012-2021.
10. Sommer G, Agosti V, Ehlers I et al. Gastrointestinal stromal tumors in a mouse model by targeted mutation of the Kit receptor tyrosine kinase. Proc Natl Acad Sci USA 2003;100:6706-6711.
11. Bosbach B, Deshpande S, Rossi F et al. Imatinib resistance and microcytic erythrocytosis in a KitV558DT669I/+ gatekeeper-mutant mouse model of gastrointestinal stromal tumor. Proc Natl Acad Sci USA 2012;109:E2276-2283.
12. Liu Y, Pop R, Sadegh C et al. Suppression of Fas-FasL coexpression by erythropoietin mediates erythroblast expansion during the erythropoietic stress response in vivo. Blood 2006;108:123-133.
13. Challen GA, Boles N, Lin KK et al. Mouse hematopoietic stem cell identification and analysis. Cytometry A 2009;75:14-24.
14. Amrani YM, Gill J, Matevossian A et al. The Paf oncogene is essential for hematopoietic stem cell function and development. J Exp Med 2011;208:1757-1765.
15. Harrison DE, Jordan CT, Zhong RK et al. Primitive hemopoietic stem cells: Direct assay of most productive populations by competitive repopulation with simple binomial, correlation and covariance calculations. Exp Hematol 1993;21:206-219.
16. Morita Y, Iseki A, Okamura S et al. Functional characterization of hematopoietic stem cells in the spleen. Exp Hematol 2011;39:351-359. e353.
17. Mo JR, Mathur A, Angagaw M et al. Splenectomy normalizes hematocrit in murine polycythemia vera. PLoS One 2009;4:e7286.
18. Akashi K, Traver D, Miyamoto T et al. A clonogenic common myeloid progenitor that gives rise to all myeloid lineages. Nature 2000; 404:193-197.
19. Na Nakorn T, Traver D, Weissman IL et al. Myeloerythroid-restricted progenitors are sufficient to confer radioprotection and provide the majority of day 8 CFU-S. J Clin Invest 2002;109:1579-1585.
20. Czechowicz A, Kraft D, Weissman IL et al. Efficient transplantation via antibody-based clearance of hematopoietic stem cell niches. Science 2007;318:1296-1299.
21. Bowie MB, Kent DG, Copley MR et al. Steel factor responsiveness regulates the high self-renewal phenotype of fetal hematopoietic stem cells. Blood 2007;109:5043-5048.
22. Ikuta K, Weissman IL. Evidence that hematopoietic stem cells express mouse c-kit but do not depend on steel factor for their generation. Proc Natl Acad Sci USA 1992;89:1502-1506.
23. McKinney-Freeman SL, Naveiras O, Yates F et al. Surface antigen phenotypes of hematopoietic stem cells from embryos and murine embryonic stem cells. Blood 2009;114:268-278.
24. Ogawa M, Tajima F, Ito T et al. CD34 expression by murine hematopoietic stem cells. Developmental changes and kinetic alterations. Ann N Y Acad Sci 2001;938:139-145.
25. Agosti V, Karur V, Sathyanarayana P et al. A KIT juxtamembrane PY567-directed pathway provides nonredundant signals for erythroid progenitor cell development and stress erythropoiesis. Exp Hematol 2009;37:159-171.
26. Randall TD, Weissman IL. Phenotypic and functional changes induced at the clonal level in hematopoietic stem cells after 5-fluorouracil treatment. Blood 1997;89:3596-3606.
27. Nemeth MJ, Kirby MR, Bodine DM. Hmgb3 regulates the balance between hematopoietic stem cell self-renewal and differentiation. Proc Natl Acad Sci USA 2006;103:13783-13788.
28. Vogel J, Kiessling I, Heinicke K et al. Transgenic mice overexpressing erythropoietin adapt to excessive erythrocytosis by regulating blood viscosity. Blood 2003;102:2278-2284.
29. Garcia-Montero AC, Jara-Acevedo M, Teodosio C et al. KIT mutation in mast cells and other bone marrow hematopoietic cell lineages in systemic mast cell disorders: A prospective study of the Spanish network on mastocytosis (REMA) in a series of 113 patients. Blood 2006;108:2366-2372.
30. Akada H, Yan D, Zou H et al. Conditional expression of heterozygous or homozygous Jak2V617F from its endogenous promoter induces a polycythemia vera-like disease. Blood 2010;115:3589-3597.
31. Mullally A, Lane SW, Ball B et al. Physiological Jak2V617F expression causes a lethal myeloproliferative neoplasm with differential effects on hematopoietic stem and progenitor cells. Cancer Cell 2010; 17:584-596.
32. Agosti V, Corbacioglu S, Ehlers I et al. Critical role for Kit-mediated Src kinase but not PI 3-kinase signaling in pro T and pro B cell development. J Exp Med 2004;199:867-878.
33. Walkley CR, Shea JM, Sims NA et al. Rb regulates interactions between hematopoietic stem cells and their bone marrow microenvironment. Cell 2007;129:1081-1095.
34. Thoren LA, Liuba K, Bryder D et al. Kit regulates maintenance of quiescent hematopoietic stem cells. J Immunol 2008;180:2045-2053.
35. Miller CL, Rebel VI, Lemieux ME et al. Studies of W mutant mice provide evidence for alternate mechanisms capable of activating hematopoietic stem cells. Exp Hematol 1996;24:185-194.
36. Miller CL, Rebel VI, Helgason CD et al. Impaired steel factor responsiveness differentially affects the detection and long-term maintenance of fetal liver hematopoietic stem cells in vivo. Blood 1997;89: 1214-1223.
37. Lerner C, Harrison DE. 5-Fluorouracil spares hemopoietic stem cells responsible for long-term repopulation. Exp Hematol 1990;18:114-118.