Glycogen synthase kinase-3 is an in vivo regulator of hematopoietic stem cell repopulation

Nature Medicine

Volumn 12, Issue 1, 2006, Pages 89-98

  Trowbridge, Jennifer J ^a,b   Xenocostas, Anargyros ^b,c   Moon, Randall T ^d   Bhatia, Mickie ^a,b,e  

^a ROBARTS RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

^c LONDON HEALTH SCIENCES CENTRE   (Canada)

^d UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^e MCMASTER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 INHIBITOR; NOTCH RECEPTOR; SONIC HEDGEHOG PROTEIN; WNT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL ACTIVITY; CELL MATURATION; CELL POPULATION; CELL SURVIVAL; CONTROLLED STUDY; DRUG MECHANISM; ENZYME ACTIVITY; GENE TARGETING; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; HUMAN CELL; IN VIVO STUDY; MEGAKARYOCYTE; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; RECIPIENT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; STEM CELL;

ANIMALS; BLOOD GLUCOSE; CELL PROLIFERATION; CELL TRANSPLANTATION; CELLS, CULTURED; CULTURE MEDIA, SERUM-FREE; ENZYME INHIBITORS; FETAL BLOOD; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLYCOGEN SYNTHASE KINASE 3; GREEN FLUORESCENT PROTEINS; HEDGEHOG PROTEINS; HEMATOPOIETIC STEM CELLS; HUMANS; LEUKOCYTES, MONONUCLEAR; MEGAKARYOCYTES; MICE; MICE, INBRED C57BL; MICE, SCID; MICE, TRANSGENIC; MODELS, BIOLOGICAL; NEUTROPHILS; RECEPTORS, NOTCH; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STEM CELL TRANSPLANTATION; STEM CELLS; TIME FACTORS; TRANS-ACTIVATORS; WNT PROTEINS;

ANIMALIA; ERINACEIDAE;

EID: 30044444251     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm1339     Document Type: Article

References (48)

1. Baron, F., Storb, R. & Little, M.T. Hematopoietic cell transplantation: five decades of progress. Arch. Med. Res. 34, 528-544 (2003).
2. Giralt, S. Bone marrow transplant in myelodysplastic syndromes: new technologies, same questions. Curr. Hematol. Rep. 3, 165-172 (2004).
3. Vollweiler, J.L., Zielske, S.P., Reese, J.S. & Gerson, S.L. Hematopoietic stem cell gene therapy: progress toward therapeutic targets. Bone Marrow Transplant. 32, 1-7 (2003).
4. Moscardo, F., Sanz, G.F. & Sanz, M.A. Unrelated-donor cord blood transplantation for adult hematological malignancies. Leuk. Lymphoma 45, 11-18 (2004).
5. Cohena, Y. & Nagler, A. Hematopoietic stem-cell transplantation using umbilical-cord blood. Leuk. Lymphoma 44, 1287-1299 (2003).
6. Rocha, V. et al. Transplants of umbilical-cord blood or bone marrow from unrelated donors in adults with acute leukemia. N. Engl. J. Med. 351, 2276-2285 (2004).
7. Laughlin, M.J. et al. Outcomes after transplantation of cord blood or bone marrow from unrelated donors in adults with leukemia. N. Engl. J. Med. 351, 2265-2275 (2004).
8. Srour, E.F., Abonour, R., Cornetta, K. & Traycoff, C.M. Ex vivo expansion of hematopoietic stem and progenitor cells: are we there yet? J. Hematother. 8, 93-102 (1999).
9. Devine, S.M., Lazarus, H.M. & Emerson, S.G. Clinical application of hematopoietic progenitor cell expansion: current status and future prospects. Bone Marrow Transplant. 31, 241-252 (2003).
10. Chabot, B., Stephenson, D.A., Chapman, V.M., Besmer, P. & Bernstein, A. The protooncogene c-kit encoding a transmembrane tyrosine kinase receptor maps to the mouse W locus. Nature 335, 88-89 (1988).
11. Geissler, E.N., Ryan, M.A. & Housman, D.E. The dominant-white spotting (W) locus of the mouse encodes the c-kit proto-oncogene. Cell 55, 185-192 (1988).
12. Frame, S. & Cohen, P. GSK-3 takes centre stage more than 20 years after its discovery. Biochem. J. 359, 1-16 (2001).
13. Cohen, P. The hormonal control of glycogen metabolism in mammalian muscle by multivalent phosphorylation. Biochem. Soc. Trans. 7, 459-480 (1979).
14. Embi, N., Rylatt, D.B. & Cohen, P. Glycogen synthase kinase-3 from rabbit skeletal muscle. Separation from cyclic-AMP-dependent protein kinase and phosphorylase kinase. Eur. J. Biochem. 107, 519-527 (1980).
15. Yost, C. et al. The axis-inducing activity, stability, and subcellular distribution of beta-catenin is regulated in Xenopus embryos by glycogen synthase kinase 3. Genes Dev. 10, 1443-1454 (1996).
16. Jia, J. et al. Shaggy/GSK3 antagonizes Hedgehog signalling by regulating Cubitus interruptus. Nature 416, 548-552 (2002).
17. Foltz, D.R., Santiago, M.C., Berechid, B.E. & Nye, J.S. Glycogen synthase kinase-3b modulates Notch signaling and stability. Curr. Biol. 12, 1006-1011 (2002).
18. Murdoch, B. et al. Wnt-5A augments repopulating capacity and primitive hematopoietic development of human blood stem cells in vivo. Proc. Natl. Acad. Sci. USA 100, 3422-3427 (2003).
19. Reya, T. et al. A role for Wnt signalling in self-renewal of haematopoietic stem cells. Nature 423, 409-414 (2003).
20. Bhardwaj, G. et al. Sonic hedgehog induces the proliferation of primitive human hematopoietic cells via BMP regulation. Nat. Immunol. 2, 172-180 (2001).
21. Karanu, F.N. et al. The notch ligand jagged-1 represents a novel growth factor of human hematopoietic stem cells. J. Exp. Med. 192, 1365-1372 (2000).
22. Duncan, A.W. et al. Integration of Notch and Wnt signaling in hematopoietic stem cell maintenance. Nat. Immunol. 6, 314-322 (2005).
23. Cline, G.W. et al. Effects of a novel glycogen synthase kinase-3 inhibitor on insulin-stimulated glucose metabolism in Zucker diabetic fatty (fa/fa) rats. Diabetes 51, 2903-2910 (2002).
24. Ring, D.B. et al. Selective glycogen synthase kinase 3 inhibitors potentiate insulin activation of glucose transport and utilization in vitro and in vivo. Diabetes 52, 588-595 (2003).
25. Morrison, S.J. & Weissman, I.L. The long-term repopulating subset of hematopoietic stem cells is deterministic and isolatable by phenotype. Immunity 1, 661-673 (1994).
26. Larochelle, A. et al. Identification of primitive human hematopoietic cells capable of repopulating NOD/SCID mouse bone marrow: Implications for gene therapy. Nat. Med. 2, 1329-1337 (1996).
27. Bhatia, M., Wang, J.C., Kapp, U., Bonnet, D. & Dick, J.E. Purification of primitive human hematopoietic cells capable of repopulating immune-deficient mice. Proc. Natl. Acad. Sci. USA 94, 5320-5325 (1997).
28. Behrens, J. et al. Functional interaction of an axin homolog, conductin, with beta-catenin, APC, and GSK3beta. Science 280, 596-599 (1998).
29. DasGupta., R. & Fuchs, E. Multiple roles for activated LEF/TCF transcription complexes during hair follicle development and differentiation. Development 126, 4557-4568 (1999).
30. Yan, D. et al. Elevated expression of axin2 and hnkd mRNA provides evidence that Wnt/beta-catenin signaling is activated in human colon tumors. Proc. Natl. Acad. Sci. USA 98, 14973-14978 (2001).
31. Jho, E.H. et al. Wnt/beta-catenin/Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol. Cell. Biol. 22, 1172-1183 (2002).
32. Issack, P.S. & Ziff, E.B. Altered expression of helix-loop-helix transcriptional regulators and cyclin D1 in Wnt-1-transformed PC12 cells. Cell Growth Differ. 9, 837-845 (1998).
33. Varnum-Finney, B. et al. Pluripotent, cytokine-dependent, hematopoietic stem cells are immortalized by constitutive Notch1 signaling. Nat. Med. 6, 1278-1281 (2000).
34. Jarriault, S. et al. Signalling downstream of activated mammalian Notch. Nature 377, 355-358 (1995).
35. Marigo, V., Johnson, R.L., Vortkamp, A. & Tabin, C.J. Sonic hedgehog differentially regulates expression of GLI and GLI3 during limb development. Dev. Biol. 180, 273-283 (1996).
36. Marigo, V. & Tabin, C.J. Regulation of Patched by Sonic hedgehog in the developing neural tube. Proc. Natl. Acad. Sci. USA 93, 9346-9351 (1996).
37. Goodrich, L.V., Milenkovic, L., Higgins, K.M. & Scott, M.P. Altered neural cell fates and medulloblastoma in mouse patched mutants. Science 277, 1109-1113 (1997).
38. Calvi, L.M. et al. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 425, 841-846 (2003).
39. Reya, T. Regulation of hematopoietic stem cell self-renewal. Recent Prog. Horm. Res. 58, 283-295 (2003).
40. Sato, N., Meijer, L., Skaltsounis, L., Greengard, P. & Brivanlou, A.H. Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor. Nat. Med. 10, 55-63 (2004).
41. Mancini, S.J. et al. Jagged1-dependent Notch signaling is dispensable for hematopoietic stem cell self-renewal and differentiation. Blood 105, 2340-2342 (2005).
42. Cobas, M. et al. Beta-catenin is dispensable for hematopoiesis and lymphopoiesis. J. Exp. Med. 199, 221-229 (2004).
43. Shojaei, F. et al. Hierarchical and ontogenic positions serve to define the molecular basis of human hematopoietic stem cell behavior. Dev. Cell. 8, 651-663 (2005).
44. Cohen, P. & Goedert, M. GSK3 inhibitors: Development and therapeutic potential. Nat. Rev. Drug Discov. 3, 479-487 (2004).
45. Barker, J.N. et al. Transplantation of 2 partially HLA-matched umbilical cord blood units to enhance engraftment in adults with hematologic malignancy. Blood 105, 1343-1347 (2005).
46. Gluckman, E. Current status of umbilical cord blood hematopoietic stem cell transplantation. Exp. Hematol. 28, 1197-1205 (2000).
47. Tsirigotis, M. et al. Analysis of ubiquitination in vivo using a transgenic mouse model. Biotechniques 31, 120-130 (2001).
48. Nikoulina, S.E. et al. Inhibition of glycogen synthase kinase 3 improves insulin action and glucose metabolism in human skeletal muscle. Diabetes 51, 2190-2198 (2002).