SMAD signaling regulates CXCL12 expression in the bone marrow niche, affecting homing and mobilization of hematopoietic progenitors

Stem Cells

Volumn 32, Issue 11, 2014, Pages 3012-3022

  Khurana, Satish ^a   Melacarne, Alessia ^a   Yadak, Rana ^a   Schouteden, Sarah ^a   Notelaers, Tineke ^a   Pistoni, Mariaelena ^a   Maes, Christa ^a   Verfaillie, Catherine M ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

CXCL12; Hematopoietic stem cells; Homing; Mobilization; Niche; Osteoblasts; SMAD signaling

Indexed keywords

BMP4 PROTEIN, MOUSE; BONE MORPHOGENETIC PROTEIN 4; CHEMOKINE CXCL12; CXCL12 PROTEIN, MOUSE; CXCR4 PROTEIN, MOUSE; RECEPTORS, CXCR4; SMAD PROTEINS;

ANIMALS; BONE MARROW; BONE MARROW CELLS; CELL LINEAGE; CELL MOVEMENT; CELLS, CULTURED; GENE EXPRESSION REGULATION; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HEMATOPOIETIC STEM CELLS; METABOLISM; METHODS; MICE; PHYSIOLOGY; SIGNAL TRANSDUCTION; STEM CELL NICHE;

ANIMALS; BONE MARROW; BONE MARROW CELLS; BONE MORPHOGENETIC PROTEIN 4; CELL LINEAGE; CELL MOVEMENT; CELLS, CULTURED; CHEMOKINE CXCL12; GENE EXPRESSION REGULATION; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HEMATOPOIETIC STEM CELLS; MICE; RECEPTORS, CXCR4; SIGNAL TRANSDUCTION; SMAD PROTEINS; STEM CELL NICHE;

EID: 84907896951     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.1794     Document Type: Article

References (56)

1. Gratwohl A, Baldomero H, Aljurf M, et al. Hematopoietic stem cell transplantation: A global perspective. JAMA 2010; 303: 1617-1624.
2. Calvi LM, Adams GB, Weibrecht KW, et al. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 2003; 425: 841-846.
3. Kiel MJ, Yilmaz OH, Iwashita T, et al. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell 2005; 121: 1109-1121.
4. Scadden DT,. The stem-cell niche as an entity of action. Nature 2006; 441: 1075-1079.
5. Taichman RS,. Blood and bone: Two tissues whose fates are intertwined to create the hematopoietic stem-cell niche. Blood 2005; 105: 2631-2639.
6. Lemoli RM, D'Addio A,. Hematopoietic stem cell mobilization. Haematologica 2008; 93: 321-324.
7. Dar A, Kollet O, Lapidot T,. Mutual, reciprocal SDF-1/CXCR4 interactions between hematopoietic and bone marrow stromal cells regulate human stem cell migration and development in NOD/SCID chimeric mice. Exp Hematol 2006; 34: 967-975.
8. Broxmeyer HE, Orschell CM, Clapp DW, et al. Rapid mobilization of murine and human hematopoietic stem and progenitor cells with AMD3100, a CXCR4 antagonist. J Exp Med 2005; 201: 1307-1318.
9. Aiuti A, Webb IJ, Bleul C, et al. The chemokine SDF-1 is a chemoattractant for human CD34+ hematopoietic progenitor cells and provides a new mechanism to explain the mobilization of CD34+ progenitors to peripheral blood. J Exp Med 1997; 185: 111-120.
10. Sugiyama T, Kohara H, Noda M, et al. Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity 2006; 25: 977-988.
11. Lapidot T, Kollet O,. The essential roles of the chemokine SDF-1 and its receptor CXCR4 in human stem cell homing and repopulation of transplanted immune-deficient NOD/SCID and NOD/SCID/B2m(null) mice. Leukemia 2002; 16: 1992-2003.
12. Yin T, Li L,. The stem cell niches in bone. J Clin Invest 2006; 116: 1195-1201.
13. Greenbaum A, Hsu YM, Day RB, et al. CXCL12 in early mesenchymal progenitors is required for haematopoietic stem-cell maintenance. Nature 2013; 495: 227-230.
14. Ding L, Morrison SJ,. Haematopoietic stem cells and early lymphoid progenitors occupy distinct bone marrow niches. Nature 2013; 495: 231-235.
15. Ceradini DJ, Kulkarni AR, Callaghan MJ, et al. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat Med 2004; 10: 858-864.
16. Calonge E, Alonso-Lobo JM, Escandon C, et al. c/EBPbeta is a major regulatory element driving transcriptional activation of the CXCL12 promoter. J Mol Biol 2010; 396: 463-472.
17. Garcia-Moruja C, Alonso-Lobo JM, Rueda P, et al. Functional characterization of SDF-1 proximal promoter. J Mol Biol 2005; 348: 43-62.
18. Winnier G, Blessing M, Labosky PA, et al. Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev 1995; 9: 2105-2116.
19. Marshall CJ, Kinnon C, Thrasher AJ,. Polarized expression of bone morphogenetic protein-4 in the human aorta-gonad-mesonephros region. Blood 2000; 96: 1591-1593.
20. Cao X, Chen D,. The BMP signaling and in vivo bone formation. Gene 2005; 357: 1-8.
21. Wu XB, Li Y, Schneider A, et al. Impaired osteoblastic differentiation, reduced bone formation, and severe osteoporosis in noggin-overexpressing mice. J Clin Invest 2003; 112: 924-934.
22. Gazzerro E, Pereira RC, Jorgetti V, et al. Skeletal overexpression of gremlin impairs bone formation and causes osteopenia. Endocrinology 2005; 146: 655-665.
23. Kollet O, Dar A, Shivtiel S, et al. Osteoclasts degrade endosteal components and promote mobilization of hematopoietic progenitor cells. Nat Med 2006; 12: 657-664.
24. Lymperi S, Ersek A, Ferraro F, et al. Inhibition of osteoclast function reduces hematopoietic stem cell numbers in vivo. Blood 2011; 117: 1540-1549.
25. Visnjic D, Kalajzic Z, Rowe DW, et al. Hematopoiesis is severely altered in mice with an induced osteoblast deficiency. Blood 2004; 103: 3258-3264.
26. Wright N, de Lera TL, Garcia-Moruja C, et al. Transforming growth factor-beta1 down-regulates expression of chemokine stromal cell-derived factor-1: Functional consequences in cell migration and adhesion. Blood 2003; 102: 1978-1984.
27. Kalajzic I, Kalajzic Z, Kaliterna M, et al. Use of type I collagen green fluorescent protein transgenes to identify subpopulations of cells at different stages of the osteoblast lineage. J Bone Miner Res 2002; 17: 15-25.
28. Khurana S, Margamuljana L, Joseph C, et al. Glypican-3-mediated inhibition of CD26 by TFPI: A novel mechanism in hematopoietic stem cell homing and maintenance. Blood 2013; 121: 2587-2595.
29. Kittler R, Heninger AK, Franke K, et al. Production of endoribonuclease-prepared short interfering RNAs for gene silencing in mammalian cells. Nat Methods 2005; 2: 779-784.
30. Henschel A, Buchholz F, Habermann B,. DEQOR: A web-based tool for the design and quality control of siRNAs. Nucleic Acids Res 2004; 32: W113-120.
31. Pistoni M, Verrecchia A, Doni M, et al. Chromatin association and regulation of rDNA transcription by the Ras-family protein RasL11a. Embo J 2010; 29: 1215-1224.
32. Zigmond SH, Hirsch JG,. Leukocyte locomotion and chemotaxis. New methods for evaluation, and demonstration of a cell-derived chemotactic factor. J Exp Med 1973; 137: 387-410.
33. Khurana S, Buckley S, Schouteden S, et al. A novel role of BMP4 in adult hematopoietic stem and progenitor cell homing via Smad independent regulation of integrin-alpha4 expression. Blood 2013; 121: 781-790.
34. Zimmerman LB, De Jesus-Escobar JM, Harland RM,. The Spemann organizer signal noggin binds and inactivates bone morphogenetic protein 4. Cell 1996; 86: 599-606.
35. Yu PB, Hong CC, Sachidanandan C, et al. Dorsomorphin inhibits BMP signals required for embryogenesis and iron metabolism. Nat Chem Biol 2008; 4: 33-41.
36. Mueller TD, Nickel J,. Promiscuity and specificity in BMP receptor activation. FEBS Lett 2012; 586: 1846-1859.
37. Macias-Silva M, Hoodless PA, Tang SJ, et al. Specific activation of Smad1 signaling pathways by the BMP7 type I receptor, ALK2. J Biol Chem 1998; 273: 25628-25636.
38. Kittler R, Surendranath V, Heninger AK, et al. Genome-wide resources of endoribonuclease-prepared short interfering RNAs for specific loss-of-function studies. Nat Methods 2007; 4: 337-344.
39. Singbrant S, Karlsson G, Ehinger M, et al. Canonical BMP signaling is dispensable for hematopoietic stem cell function in both adult and fetal liver hematopoiesis, but essential to preserve colon architecture. Blood 2010; 115: 4689-4698.
40. Zhang J, Niu C, Ye L, et al. Identification of the haematopoietic stem cell niche and control of the niche size. Nature 2003; 425: 836-841.
41. Christopherson KW 2nd, Hangoc G, Mantel CR, et al. Modulation of hematopoietic stem cell homing and engraftment by CD26. Science 2004; 305: 1000-1003.
42. Petit I, Szyper-Kravitz M, Nagler A, et al. G-CSF induces stem cell mobilization by decreasing bone marrow SDF-1 and up-regulating CXCR4. Nat Immunol 2002; 3: 687-694.
43. Stroncek DF, Clay ME, Smith J, et al. Changes in blood counts after the administration of granulocyte-colony-stimulating factor and the collection of peripheral blood stem cells from healthy donors. Transfusion 1996; 36: 596-600.
44. Kobbe G, Sohngen D, Bauser U, et al. Factors influencing G-CSF-mediated mobilization of hematopoietic progenitor cells during steady-state hematopoiesis in patients with malignant lymphoma and multiple myeloma. Ann Hematol 1999; 78: 456-462.
45. Nademanee A, Sniecinski I, Schmidt GM, et al. High-dose therapy followed by autologous peripheral-blood stem-cell transplantation for patients with Hodgkin's disease and non-Hodgkin's lymphoma using unprimed and granulocyte colony-stimulating factor-mobilized peripheral-blood stem cells. J Clin Oncol 1994; 12: 2176-2186.
46. Stiff PJ,. Management strategies for the hard-to-mobilize patient. Bone Marrow Transplant 1999; 23 Suppl 2: S29-33.
47. Boeve S, Strupeck J, Creech S, et al. Analysis of remobilization success in patients undergoing autologous stem cell transplants who fail an initial mobilization: Risk factors, cytokine use and cost. Bone Marrow Transplant 2004; 33: 997-1003.
48. DiPersio JF, Stadtmauer EA, Nademanee A, et al. Plerixafor and G-CSF versus placebo and G-CSF to mobilize hematopoietic stem cells for autologous stem cell transplantation in patients with multiple myeloma. Blood 2009; 113: 5720-5726.
49. Flomenberg N, Devine SM, Dipersio JF, et al. The use of AMD3100 plus G-CSF for autologous hematopoietic progenitor cell mobilization is superior to G-CSF alone. Blood 2005; 106: 1867-1874.
50. Ramirez P, Rettig MP, Uy GL, et al. BIO5192, a small molecule inhibitor of VLA-4, mobilizes hematopoietic stem and progenitor cells. Blood 2009; 114: 1340-1343.
51. Ogawa M, Nishikawa S, Ikuta K, et al. B cell ontogeny in murine embryo studied by a culture system with the monolayer of a stromal cell clone, ST2: B cell progenitor develops first in the embryonal body rather than in the yolk sac. Embo J 1988; 7: 1337-1343.
52. Massague J,. TGF-beta signal transduction. Annu Rev Biochem 1998; 67: 753-791.
53. Whitman M,. Smads and early developmental signaling by the TGFbeta superfamily. Genes Dev 1998; 12: 2445-2462.
54. Shi Y, Wang YF, Jayaraman L, et al. Crystal structure of a Smad MH1 domain bound to DNA: Insights on DNA binding in TGF-beta signaling. Cell 1998; 94: 585-594.
55. Massague J, Seoane J, Wotton D,. Smad transcription factors. Genes Dev 2005; 19: 2783-2810.
56. Levesque JP, Hendy J, Takamatsu Y, et al. Disruption of the CXCR4/CXCL12 chemotactic interaction during hematopoietic stem cell mobilization induced by GCSF or cyclophosphamide. J Clin Invest 2003; 111: 187-196.