Mammalian target of rapamycin activity is required for expansion of CD34+ hematopoietic progenitor cells

Haematologica

Volumn 94, Issue 7, 2009, Pages 901-910

  Geest, Christian R ^a   Zwartkruis, Fried J ^a   Vellenga, Edo ^b   Coffer, Paul J ^a   Buitenhuis, Miranda ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

CD34+; Hematopoiesis; Mammalian target of rapamycin; mTOR; Myeloid; Rapamycin

Indexed keywords

CD34 ANTIGEN; MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN KINASE; PROTEIN KINASE B; RAPAMYCIN;

ACUTE LEUKEMIA; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CELL SIZE; CONTROLLED STUDY; HEMATOLOGIC MALIGNANCY; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; MYELODYSPLASTIC SYNDROME; MYELOPOIESIS; PROTEIN SYNTHESIS;

ANTIGENS, CD34; APOPTOSIS; CELL DIFFERENTIATION; CELL PROLIFERATION; FETAL BLOOD; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; GRANULOCYTES; HEMATOPOIETIC STEM CELLS; HUMANS; LEUKOCYTES, MONONUCLEAR; MYELOPOIESIS; PROTEIN KINASES; RESEARCH DESIGN; STEM CELLS; TOR SERINE-THREONINE KINASES;

EID: 67650713694     PISSN: 03906078     EISSN: 15928721     Source Type: Journal    
DOI: 10.3324/haematol.13766     Document Type: Article

References (53)

1. Morrison SJ, Weissman IL. The long-term repopulating subset of hematopoietic stem cells is deterministic and isolatable by phenotype. Immunity 1994;1:661-73.
2. Franke TF, Hornik CP, Segev L, Shostak GA, Sugimoto C. PI3K/Akt and apoptosis: size matters. Oncogene 2003;22:8983-8.
3. Buitenhuis M, Verhagen LP, van Deutekom HWM, Castor A, Verploegen S, Koenderman L, et al. Protein kinase B (c-akt) regulates hematopoietic lineage choice decisions during myelopoiesis. Blood 2008;111:112-21.
4. Sujobert P, Bardet V, Cornillet-Lefebvre P, Hayflick JS, Prie N, Verdier F, et al. Essential role for the p110delta isoform in phosphoinositide 3-kinase activation and cell proliferation in acute myeloid leukemia. Blood 2005;106:1063-6.
5. Brandts CH, Sargin B, Rode M, Biermann C, Lindtner B, Schwäble J, et al. Constitutive activation of Akt by Flt3 internal tandem duplications is necessary for increased survival, proliferation, and myeloid transformation. Cancer Res 2005;65:9643-50.
6. Nyåkern M, Tazzari PL, Finelli C, Bosi C, Follo MY, Grafone T, et al. Frequent elevation of Akt kinase phosphorylation in blood marrow and peripheral blood mononuclear cells from high-risk myelodysplastic syndrome patients. Leukemia 2006;20:230-8.
7. Tee AR, Blenis J. mTOR, translational control and human disease. Semin Cell Dev Biol 2005;16:29-37.
8. Navé BT, Ouwens M, Withers DJ, Alessi DR, Shepherd PR. Mammalian target of rapamycin is a direct target for protein kinase B: identification of a convergence point for opposing effects of insulin and amino-acid deficiency on protein translation. Biochem J 1999;344:427-31.
9. Inoki K, Li Y, Zhu T, Wu J, Guan K. Tsc2 is phosphorylated and inhibited by Akt and suppresses mTOR signalling. Nat Cell Biol 2002;4:648-57.
10. Isotani S, Hara K, Tokunaga C, Inoue H, Avruch J, Yonezawa K. Immunopurified mammalian target of rapamycin phosphorylates and activates p70 S6 kinase a in vitro. J Biol Chem 1999;274:34493-8.
11. Hara K, Yonezawa K, Kozlowski MT, Sugimoto T, Andrabi K, Weng QP, et al. Regulation of eIF-4E BP1 phosphorylation by mTOR. J Biol Chem 1997;272:26457-63.
12. Gingras AC, Raught B, Sonenberg N. Regulation of translation initiation by FRAP/mTOR. Genes Dev 2001;15:807-26.
13. Loewith R, Jacinto E, Wullschleger S, Lorberg A, Crespo JL, Bonenfant D, et al. Two TOR complexes, only one of which is rapamycin sensitive, have distinct roles in cell growth control. Mol Cell 2002;10:457-68.
14. Choi J, Chen J, Schreiber SL, Clardy J. Structure of the FKBP12-rapamycin complex interacting with the binding domain of human FRAP. Science 1996;273:239-42.
15. Gangloff Y, Mueller M, Dann SG, Svoboda P, Sticker M, Spetz J, et al. Disruption of the mouse mTOR gene leads to early postimplantation lethality and prohibits embryonic stem cell development. Mol Cell Biol 2004;24:9508-16.
16. Martin PM, Sutherland AE. Exogenous amino acids regulate trophectoderm differentiation in the mouse blastocyst through an mTOR-dependent pathway. Dev Biol 2001;240:182-93.
17. Yoon M, Chen J. PLD regulates myoblast differentiation through the mTOR-IGF2 pathway. J Cell Sci 2008;121:282-9.
18. Phornphutkul C, Wu K, Auyeung V, Chen Q, Gruppuso PA. mTOR signaling contributes to chondrocyte differentiation. Dev Dyn 2008;237:702-12.
19. Butzal M, Loges S, Schweizer M, Fischer U, Gehling UM, Hossfeld DK, et al. Rapamycin inhibits proliferation and differentiation of human endothelial progenitor cells in vitro. Exp Cell Res 2004;300:65-71.
20. Jankiewicz M, Groner B, Desrivières S. Mammalian target of rapamycin regulates the growth of mammary epithelial cells through the inhibitor of deoxyribonucleic acid binding ID1 and their functional differentiation through ID2. Mol Endocrinol 2006;20:2369-81.
21. Singha UK, Jiang Y, Yu S, Luo M, Lu Y, Zhang J, et al. Rapamycin inhibits osteoblast proliferation and differentiation in MC3T3-E1 cells and primary mouse bone marrow stromal cells. J Cell Biochem 2008;103:434-46.
22. Ohanna M, Sobering AK, Lapointe T, Lorenzo L, Praud C, Petroulakis E, et al. Atrophy of S6K1(-/-) skeletal muscle cells reveals distinct mTOR effectors for cell cycle and size control. Nat Cell Biol 2005;7:286-94.
23. Park I, Chen J. Mammalian target of rapamycin (mTOR) signaling is required for a late-stage fusion process during skeletal myotube maturation. J Biol Chem 2005;280:32009-17.
24. Martin KA, Merenick BL, Ding M, Fetalvero KM, Rzucidlo EM, Kozul CD, et al. Rapamycin promotes vascular smooth muscle cell differentiation through insulin receptor substrate-1/phosphatidylinositol 3-kinase/Akt2 feedback signaling. J Biol Chem 2007;282:36112-20.
25. Manz MG, Miyamoto T, Akashi K, Weissman IL. Prospective isolation of human clonogenic common myeloid progenitors. Proc Natl Acad Sci USA 2002;99:11872-7.
26. Inoki K, Ouyang H, Li Y, Guan K. Signaling by target of rapamycin proteins in cell growth control. Microbiol Mol Biol Rev 2005;69:79-100.
27. van Gorp AG, van der Vos KE, Brenkman AB, Bremer A, van den Broek N, Zwartkruis F, et al. AGC kinases regulate phosphorylation and activation of eukaryotic translation initiation factor 4B. Oncogene 2009;28:95-106.
28. Abraham RT, Wiederrecht GJ. Immunopharmacology of rapamycin. Annu Rev Immunol 1996;14:483-510.
29. Decker T, Hipp S, Ringshausen I, Bogner C, Oelsner M, Schneller F, et al. Rapamycin-induced G1 arrest in cycling B-CLL cells is associated with reduced expression of cyclin D3, cyclin E, cyclin A, and survivin. Blood 2003;101:278-85.
30. Fingar DC, Richardson CJ, Tee AR, Cheatham L, Tsou C, Blenis J. mTOR controls cell cycle progression through its cell growth effectors S6K1 and 4E-BP1/eukaryotic translation initiation factor 4E. Mol Cell Biol 2004;24:200-16.
31. Kwon TK, Buchholz MA, Ponsalle P, Chrest FJ, Nordin AA. The regulation of p27kip1 expression following the polyclonal activation of murine G0 T cells. J Immunol 1997;158:5642-8.
32. Wagner EF, Hleb M, Hanna N, Sharma S. A pivotal role of cyclin D3 and cyclin-dependent kinase inhibitor p27 in the regulation of IL-2-, IL-4-, or IL-10-mediated human B cell proliferation. J Immunol 1998;161:1123-31.
33. Nourse J, Firpo E, Flanagan WM, Coats S, Polyak K, Lee MH, et al. Interleukin-2-mediated elimination of the p27kip1 cyclin-dependent kinase inhibitor prevented by rapamycin. Nature 1994;372:570-3.
34. Kawamata S, Sakaida H, Hori T, Maeda M, Uchiyama T. The upregulation of p27kip1 by rapamycin results in G1 arrest in exponentially growing T-cell lines. Blood 1998;91:561-9.
35. Raslova H, Baccini V, Loussaief L, Comba B, Larghero J, Debili N, et al. Mammalian target of rapamycin (mTOR) regulates both proliferation of megakaryocyte progenitors and late stages of megakaryocyte differentiation. Blood 2006;107:2303-10.
36. Drayer AL, Olthof SGM, Vellenga E. Mammalian target of rapamycin is required for thrombopoietin-induced proliferation of megakaryocyte progenitors. Stem Cells 2006;24:105-14.
37. Fingar DC, Salama S, Tsou C, Harlow E, Blenis J. Mammalian cell size is controlled by mTOR and its downstream targets S6K1 and 4EBP1/EIF4E. Genes Dev 2002;16:1472-87.
38. Fingar DC, Blenis J. Target of rapamycin (mTOR): an integrator of nutrient and growth factor signals and coordinator of cell growth and cell cycle progression. Oncogene 2004;23:3151-71.
39. Flick K, Chapman-Shimshoni D, Stuart D, Guaderrama M, Wittenberg C. Regulation of cell size by glucose is exerted via repression of the CLN1 promoter. Mol Cell Biol 1998;18:2492-501.
40. Conlon IJ, Dunn GA, Mudge AW, Raff MC. Extracellular control of cell size. Nat Cell Biol 2001;3:918-21.
41. Gan B, Sahin E, Jiang S, Sanchez-Aguilera A, Scott KL, Chin L, et al. mTORC1-dependent and -independent regulation of stem cell renewal, differentiation, and mobilization. Proc Natl Acad Sci USA 2008;105:19384-9.
42. Zeiser R, Leveson-Gower DB, Zambricki EA, Kambham N, Beilhack A, Loh J, et al. Differential impact of mammalian target of rapamycin inhibition on CD4+ CD25+Foxp3+ regulatory T cells compared with conventional CD4+ T cells. Blood 2008;111:453-62.
43. Gera JF, Mellinghoff IK, Shi Y, Rettig MB, Tran C, Hsu J, et al. Akt activity determines sensitivity to mammalian target of rapamycin (mTOR) inhibitors by regulating cyclin D1 and c-myc expression. J Biol Chem 2004;279:2737-46.
44. Sarbassov DD, Ali SM, Sengupta S, Sheen J, Hsu PP, Bagley AF, et al. Prolonged rapamycin treatment inhibits mTORC2 assembly and Akt/PKB. Mol Cell 2006;22:159-68.
45. Sarbassov DD, Guertin DA, Ali SM, Sabatini DM. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 2005;307:1098-101.
46. Xu Q, Simpson S, Scialla TJ, Bagg A, Carroll M. Survival of acute myeloid leukemia cells requires PI3 kinase activation. Blood 2003;102:972-80.
47. Min YH, Eom JI, Cheong JW, Maeng HO, Kim JY, Jeung HK, et al. Constitutive phosphorylation of Akt/PKB protein in acute myeloid leukemia: its significance as a prognostic variable. Leukemia 2003;17:995-7.
48. Aoki M, Blazek E, Vogt PK. A role of the kinase mTOR in cellular transformation induced by the oncoproteins P3k and Akt. Proc Natl Acad Sci USA 2001;98:136-41.
49. Neshat MS, Mellinghoff IK, Tran C, Stiles B, Thomas G, Petersen R, et al. Enhanced sensitivity of PTEN-deficient tumors to inhibition of FRAP/mTOR. Proc Natl Acad Sci USA 2001;98:10314-9.
50. Récher C, Beyne-Rauzy O, Demur C, Chicanne G, Dos Santos C, Mas VM, et al. Antileukemic activity of rapamycin in acute myeloid leukemia. Blood 2005;105:2527-34.
51. Zeng Z, Sarbassov DD, Samudio IJ, Yee KWL, Munsell MF, Ellen Jackson C, et al. Rapamycin derivatives reduce mTORC2 signaling and inhibit AKT activation in AML. Blood 2007;109:3509-12.
52. Tamburini J, Chapuis N, Bardet V, Park S, Sujobert P, Willems L, et al. Mammalian target of rapamycin (mTOR) inhibition activates phosphatidylinositol 3-kinase/Akt by upregulating insulin-like growth factor-1 receptor signaling in acute myeloid leukemia: rationale for therapeutic inhibition of both pathways. Blood 2008;111:379-82.
53. Sun S, Rosenberg LM, Wang X, Zhou Z, Yue P, Fu H, et al. Activation of Akt and EIF4E survival pathways by rapamycin-mediated mammalian target of rapamycin inhibition. Cancer Res 2005;65:7052-8.