EphB4 Expressing Stromal Cells Exhibit an Enhanced Capacity for Hematopoietic Stem Cell Maintenance

Stem Cells

Volumn 33, Issue 9, 2015, Pages 2838-2849

  Nguyen, Thao M ^a,b,c   Arthur, Agnieszka ^a,c,d   Panagopoulos, Romana ^a   Paton, Sharon ^a   Hayball, John D ^b   Zannettino, Andrew C W ^a,c   Purton, Louise E ^e   Matsuo, Koichi ^f   Gronthos, Stan ^a,c  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b UNIVERSITY OF SOUTH AUSTRALIA   (Australia)

^c SOUTH AUSTRALIAN HEALTH AND MEDICAL RESEARCH INSTITUTE   (Australia)

^d Division of Haematology   (Australia)

^e UNIVERSITY OF MELBOURNE   (Australia)

^f KEIO UNIVERSITY   (Japan)

Author keywords

Bone marrow stromal cells; EphB; ephrinB; Haematopoietic stem cells; Mesenchymal stem cells

Indexed keywords

ANGIOPOIETIN 1; COLLAGEN TYPE 1; EPHRIN RECEPTOR B4; FLT3 LIGAND; INTERLEUKIN 6; OSTEOPONTIN; SHORT HAIRPIN RNA; STROMAL CELL DERIVED FACTOR 1; EPHB4 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ARTICLE; CELL HOMING; CONTROLLED STUDY; GENE OVEREXPRESSION; GENE SILENCING; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IN VITRO STUDY; MOUSE; NONHUMAN; OSTEOBLAST; PROTEIN EXPRESSION; STROMA CELL; TRANSGENIC MOUSE; AMINO ACID SEQUENCE; ANIMAL; BIOSYNTHESIS; CELL CULTURE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS;

MUS;

AMINO ACID SEQUENCE; ANIMALS; CELLS, CULTURED; GENE EXPRESSION REGULATION; HEMATOPOIETIC STEM CELLS; HUMANS; MICE; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; RECEPTOR, EPHB4; STROMAL CELLS;

EID: 84940467199     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.2069     Document Type: Article

References (62)

1. Metcalf D,. On Hematopoietic stem cell fate. Immunity 2007; 26: 669-673.
2. Greenbaum A, Hsu YS, Day RB, et al., CXCL12 in early mesenchymal progenitors is required for haematopoietic stem-cell maintenance. Nature 2013; 495: 227-230.
3. Joseph C, Quach JM, Walkley CR, et al., Deciphering hematopoietic stem cells in their niches: A critical appraisal of genetic models, lineage tracing, and imaging strategies. Cell Stem Cell 2013; 13: 520-533.
4. Morrison SJ, Scadden DT,. The bone marrow niche for haematopoietic stem cells. Nature 2014; 505: 327-334.
5. Purton LE, Scadden DT,. Limiting factors in murine hematopoietic stem cell assays. Cell Stem Cell 2007; 1: 263-270.
6. Askmyr M, Sims NA, Martin TJ, et al., What is the true nature of the osteoblastic hematopoietic stem cell niche? Trends Endocrinol Metab 2009; 20: 303-309.
7. Pasquale EB,. The Eph family of receptors. Curr Opin Cell Biol 1997; 9: 608-615.
8. Kullander K, Klein R,. Mechanisms and functions of Eph and ephrin signalling. Nat Rev Mol Cell Biol 2002; 3: 475-486.
9. Prevost N, Woulfe DS, Tognolini M, et al., Signaling by ephrinB1 and Eph kinases in platelets promotes Rap1 activation, platelet adhesion, and aggregation via effector pathways that do not require phosphorylation of ephrinB1. Blood 2004; 103: 1348-1355.
10. Zlotoff D, Schwarz B, Bhandoola A,. The long road to the thymus: the generation, mobilization, and circulation of T-cell progenitors in mouse and man. Sem Immunopathol 2008; 30: 371-382.
11. Xing W, Kim J, Wergedal J, et al., Ephrin B1 Regulates bone marrow stromal cell differentiation and bone formation by influencing TAZ transactivation via complex formation with NHERF1. Mol Cell Biol 2010; 30: 711-721.
12. Luis MAC, Eva Ma T, Beatriz de G, et al., Expression profile of Eph receptors and ephrin ligands in healthy human B lymphocytes and chronic lymphocytic leukemia B-cells. Leuk Res 2009; 33: 395-406.
13. Saint-Vis B, Bouchet C, Gautier G, et al., Human dendritic cells express neuronal Eph receptor tyrosine kinases: role of EphA2 in regulating adhesion to fibronectin. Blood 2004; 102: 4431-4440.
14. Okubo T, Yanai N, Obinata M,. Stromal cells modulate ephrinB2 expression and transmigration of hematopoietic cells. Exp Hematol 2006; 34: 330-338.
15. Ting MJ, Boyd AW,. The role of Eph receptor tyrosine kinases and ephrin ligands in hematopoietic cell development and function. Open Hematol 2008; 2: 103-110.
16. Pasquale EB,. Eph-ephrin bidirectional signaling in physiology and disease. Cell 2008; 133: 38-52.
17. Zhao C, Irie N, Takada Y, et al., Bidirectional ephrinB2-EphB4 signaling controls bone homeostasis. Cell Metabol 2006; 4: 111-121.
18. Valverde-Franco G, Pelletier JP, Fahmi H, et al., In vivo bone-specific EphB4 overexpression in mice protects both subchondral bone and cartilage during osteoarthritis. Arthritis Rheumat 2012; 64: 3614-3625.
19. Arthur A, Panagopoulos RA, Cooper L, et al., EphB4 enhances the process of endochondral ossification and inhibits remodeling during bone fracture repair. J Bone Miner Res 2013; 28: 926-935.
20. Arthur A, Zannettino A, Panagopoulos R, et al., EphB/ephrin-B interactions mediate human MSC attachment, migration and osteochondral differentiation. Bone 2011; 48: 533-542.
21. Gronthos S, Zannettino AC,. A method to isolate and purify human bone marrow stromal stem cells. Meth Mol Biol 2008; 449: 45-57.
22. Gronthos S, Zannettino AC, Hay SJ, et al., Molecular and cellular characterisation of highly purified stromal stem cells derived from human bone marrow. J Cell Sci 2003; 116: 1827-1835.
23. Nguyen TM, Arthur A, Hayball JD, et al., EphB and Ephrin-B interactions mediate human mesenchymal stem cell suppression of activated T-cells. Stem Cells Dev 2013; 22: 2751-2764.
24. Hemming S, Cakouros D, Isenmann S, et al., EZH2 and KDM6A act as an epigenetic switch to regulate mesenchymal stem cell lineage specification. Stem Cells 2014; 32: 802-815.
25. Liu M, Miller CL, Eaves CJ,. Human long-term culture initiating cell assay. Basic Cell Cult Prot 2012: 241-256.
26. Calvi LM, Adams GB, Weibrecht KW, et al., Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 2003; 425: 841-846.
27. 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.
28. Kim S, Prout M, Ramshaw H, et al., Cutting edge: Basophils are transiently recruited into the draining lymph nodes during helminth infection via IL-3, but infection-induced Th2 immunity can develop without basophil lymph node recruitment or IL-3. J Immunol 2010; 184: 1143-1147.
29. Nilsson SK, Johnston HM, Coverdale JA,. Spatial localization of transplanted hemopoietic stem cells: Inferences for the localization of stem cell niches. Blood 2001; 97: 2293-2299.
30. Grassinger J, Nilsson SK,. Methods to analyze the homing efficiency and spatial distribution of hematopoietic stem and progenitor cells and their relationship to the bone marrow endosteum and vascular endothelium. In:, Geiger M-DFaH, ed. Stem Cell Migration: Methods and Protocols. Springer, New York, NY. 2011: 197-214.
31. Williams B, Nilsson SK,. Investigating the interactions between haemopoietic stem cells and their niche: Methods for the analysis of stem cell homing and distribution within the marrow following transplantation. In:, Audet J, Stanford WL, eds. Stem Cells in Regenerative Medicine, Methods and Protocols. Humana Press, New York, NY. 2009: 93-107.
32. Winkler IG, Barbier V, Wadley R, et al., Positioning of bone marrow hematopoietic and stromal cells relative to blood flow in vivo: Serially reconstituting hematopoietic stem cells reside in distinct nonperfused niches. Blood 2010; 116: 375-385.
33. Short BJ, Brouard N, Simmons PJ,. Prospective isolation of mesenchymal stem cells from mouse compact bone. Stem Cell Regen Med 2009; 482: 259-268.
34. Ding L, Morrison SJ,. Haematopoietic stem cells and early lymphoid progenitors occupy distinct bone marrow niches. Nature 2013; 495: 231-235.
35. Fisher LW, Stubbs JT, Young MF,. Antisera and cDNA probes to human and certain animal model bone matrix noncollagenous proteins. Acta Orthop Scand Suppl 1995; 266: 61-65.
36. Wada N, Menicanin D, Shi S, et al., Immunomodulatory properties of human periodontal ligament stem cells. Journal of Cellular Physiology 2009; 219: 667-676.
37. Noll JE, Williams SA, Tong CM, et al., Myeloma plasma cells alter the bone marrow microenvironment by stimulating the proliferation of mesenchymal stromal cells. Haematologica 2014; 99: 163-171.
38. Levesque JP, Helwani FM, Winkler IG,. The endosteal/osteoblastic/niche and its role in hematopoietic stem cell homing and mobilization. Leukemia 2010; 24: 1979-1992.
39. Haylock DN, Nilsson SK,. Osteopontin: a bridge between bone and blood. Br J Haematol 2006; 134: 467-474.
40. Nilsson SK, Johnston HM, Whitty GA, et al., Osteopontin, a key component of the hematopoietic stem cell niche and regulator of primitive hematopoietic progenitor cells. Blood 2005; 106: 1232-1239.
41. Yin T, Li L,. The stem cell niches in bone. Am Soc Clin Invest 2006; 116: 1195-1201.
42. Bianco P,. Stem cells and bone: A historical perspective. Bone 2015; 70: 2-9.
43. Shen Y, Nilsson SK,. Bone, microenvironment and hematopoiesis. Curr Opin Hematol 2012; 19: 250-5;19:250-255.
44. Hamada K, Oike Y, Ito Y, et al., Distinct roles of Ephrin-B2 forward and EphB4 reverse signaling in endothelial cells. Arterioscl Thromb Vasc Biol 2003; 23: 190-197.
45. Till JE, McCulloch EA,. A direct measurement of the radiation sensitivity of normal mouse bone marrow cells. Radiat Res 1961; 14: 213-222.
46. Arai F, Hirao A, Ohmura M, et al., Tie2/Angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell 2004; 118: 149-161.
47. Goldman DC, Bailey AS, Pfaffle DL, et al., BMP4 regulates the hematopoietic stem cell niche. Blood 2009; 114: 4393-4401.
48. 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.
49. Zsebo KM, Williams DA, Geissler EN, et al., Stem cell factor is encoded at the SI locus of the mouse and is the ligand for the c-kit tyrosine kinase receptor. Cell 1990; 63: 213-224.
50. Salvucci O, de la Luz Sierra M, Martina JA, et al., EphB2 and EphB4 receptors forward signaling promotes SDF-1-induced endothelial cell chemotaxis and branching remodeling. Blood 2006; 108: 2914-2922.
51. Hoggatt J, Speth JM, Pelus LM,. Concise Review: Sowing the seeds of a fruitful harvest: Hematopoietic stem cell mobilization. Stem Cells 2013; 31: 2599-2606.
52. Kunkel EJ, Butcher EC,. Plasma-cell homing. Nat Rev Immunol 2003; 3: 822-829.
53. Ansel KM, Cyster JG,. Chemokines in lymphopoiesis and lymphoid organ development. Curr Opin Immunol 2001; 13: 172-179.
54. Akashi K, Kondo M, Cheshier S, et al., Lymphoid development from stem cells and the common lymphocyte progenitors. Cold Spring Harb Symp Quant Biol 1999; 64: 1-12.
55. Kitamura T, Kabuyama Y, Kamataki A, et al., Enhancement of lymphocyte migration and cytokine production by ephrinB1 system in rheumatoid arthritis. Am J Physiol Cell Physiol 2008; 294: C189-C196.
56. Bordeaux-Rego P, Luzo A, Costa FF, et al., Both interleukin-3 and interleukin-6 are necessary for better ex vivo expansion of CD133 + cells from umbilical cord blood. Stem Cells Dev 2010; 19: 413-422.
57. Kovačevic-Filipovic M, Petakov M, Hermitte F, et al., Interleukin-6 (IL-6) and low O2 concentration (1%) synergize to improve the maintenance of hematopoietic stem cells (pre-CFC). J Cell Physiol 2007; 212: 68-75.
58. Bernad A, Kopf M, Kulbacki R, et al., Interleukin-6 is required in vivo for the regulation of stem cells and committed progenitors of the hematopoietic system. Immunity 1994; 1: 725-731.
59. Gilliland DG, Griffin JD,. The roles of FLT3 in hematopoiesis and leukemia. Blood 2002; 100: 1532-1542.
60. Nikhil S, Hediye E, Juha PH, et al., A semisynthetic Eph receptor tyrosine kinase provides insight into ligand-induced kinase activation. Chem Biol 2011; 18: 361-371.
61. Lyman SD, Brasel K, Rousseau AM, et al., The flt3 ligand: a hematopoietic stem cell factor whose activities are distinct from steel factor. Stem Cells 1994; 12: 99-107.
62. Lyman SD,. Biology of flt3 ligand and receptor. Int J Hematol 1995; 62: 63-73.