Understanding the role of the microenvironment during definitive hemopoietic development

Experimental Hematology

Volumn 41, Issue 9, 2013, Pages 761-768

  Cao, Huimin ^a,b   Oteiza, Ana ^a,c   Nilsson, Susan K ^a,b  

^a CSIRO   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c UNIVERSITY OF TROMSØ   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOPOIETIN; ANGIOPOIETIN LIKE 3; CD31 ANTIGEN; CHEMOKINE RECEPTOR CXCR4; HERMES ANTIGEN; INTERLEUKIN 6; INTERLEUKIN 7; NERVE CELL ADHESION MOLECULE; NOTCH RECEPTOR; OSTEOPONTIN; SOMATOMEDIN B; STEM CELL ANTIGEN 1; STEM CELL FACTOR; TENASCIN; THROMBOPOIETIN; THY 1 ANTIGEN; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1;

ADULT STEM CELL; AORTA GONAD MESONEPHROS; CELL CONTACT; CELL DIFFERENTIATION; CELL MATURATION; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DEVELOPMENTAL STAGE; EPITHELIAL MESENCHYMAL TRANSITION; EXTRACELLULAR MATRIX; FETAL BONE MARROW; FETAL SPLEEN; FETAL STEM CELL; FETUS (ANATOMY); FETUS LIVER; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HEMATOPOIETIC TISSUE; HUMAN; INTRACELLULAR SIGNALING; MESONEPHROS; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; NEONATAL BONE MARROW; NONHUMAN; ONTOGENY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; STEM CELL EXPANSION; STEM CELL NICHE; STROMA CELL; UPREGULATION; WNT SIGNALING PATHWAY;

EID: 84883506421     PISSN: 0301472X     EISSN: 18732399     Source Type: Journal    
DOI: 10.1016/j.exphem.2013.06.005     Document Type: Article

References (103)

1. Schofield R. The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells 1978, 4:7-25.
2. 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.
3. Calvi L.M., Adams G.B., Weibrecht K.W., et al. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 2003, 425:841-846.
4. Kiel M.J., Yilmaz O.H., Iwashita T., Terhorst C., Morrison S.J. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell 2005, 121:1109-1121.
5. Yamate T., Mocharla H., Taguchi Y., Igietseme J.U., Manolagas S.C., Abe E. Osteopontin expression by osteoclast and osteoblast progenitors in the murine bone marrow: demonstration of its requirement for osteoclastogenesis and its increase after ovariectomy. Endocrinology 1997, 138:3047-3055.
6. Hosokawa K., Arai F., Yoshihara H., et al. Function of oxidative stress in the regulation of hematopoietic stem cell-niche interaction. Biochem Biophys Res Commun 2007, 363:578-583.
7. Mazo I.B., Gutierrez-Ramos J.C., Frenette P.S., Hynes R.O., Wagner D.D., von Andrian U.H. Hematopoietic progenitor cell rolling in bone marrow microvessels: parallel contributions by endothelial selectins and vascular cell adhesion molecule 1. J Exp Med 1998, 188:465-474.
8. Newman P.J. The biology of PECAM-1. J Clin Invest 1997, 100:S25-S29.
9. Rossi L., Lin K.K., Boles N.C., et al. Less is more: unveiling the functional core of hematopoietic stem cells through knockout mice. Cell Stem Cell 2012, 11:302-317.
10. Ellis S.L., Grassinger J., Jones A., et al. The relationship between bone, hemopoietic stem cells, and vasculature. Blood 2011, 118:1516-1524.
11. Nilsson S.K., Johnston H.M., Coverdale J.A. Spatial localization of transplanted hemopoietic stem cells: inferences for the localization of stem cell niches. Blood 2001, 97:2293-2299.
12. Wang L., Benedito R., Bixel M.G., et al. Identification of a clonally expanding haematopoietic compartment in bone marrow. EMBO J 2013, 32:219-230.
13. Grassinger J., Haylock D.N., Williams B., Olsen G.H., Nilsson S.K. Phenotypically identical hemopoietic stem cells isolated from different regions of bone marrow have different biological potential. Blood 2010, 116:3185-3196.
14. Nilsson S.K., Johnston H.M., Whitty G.A., et al. Osteopontin, a key component of the hematopoietic stem cell niche and regulator of primitive hematopoietic progenitor cells. Blood 2005, 106:1232-1239.
15. Stier S., Ko Y., Forkert R., et al. Osteopontin is a hematopoietic stem cell niche component that negatively regulates stem cell pool size. JExp Med 2005, 201:1781-1791.
16. Nilsson S.K., Haylock D.N., Johnston H.M., Occhiodoro T., Brown T.J., Simmons P.J. Hyaluronan is synthesized by primitive hemopoietic cells, participates in their lodgment at the endosteum following transplantation, and is involved in the regulation of their proliferation and differentiation invitro. Blood 2003, 101:856-862.
17. Itkin T., Lapidot T. SDF-1 keeps HSC quiescent at home. Blood 2011, 117:373-374.
18. Driessen R.L., Johnston H.M., Nilsson S.K. Membrane-bound stem cell factor is a key regulator in the initial lodgment of stem cells within the endosteal marrow region. Exp Hematol 2003, 31:1284-1291.
19. Avigdor A., Goichberg P., Shivtiel S., et al. CD44 and hyaluronic acid cooperate with SDF-1 in the trafficking of human CD34+ stem/progenitor cells to bone marrow. Blood 2004, 103:2981-2989.
20. Ohta M., Sakai T., Saga Y., Aizawa S., Saito M. Suppression of hematopoietic activity in tenascin-C-deficient mice. Blood 1998, 91:4074-4083.
21. Ekblom M., Fassler R., Tomasini-Johansson B., Nilsson K., Ekblom P. Downregulation of tenascin expression by glucocorticoids in bone marrow stromal cells and in fibroblasts. J Cell Biol 1993, 123:1037-1045.
22. Ren A.H., Zhang Y., Zhao Y.L., Zhao L., Liu X.Y., Zhao S.F. [Comparative study of differentially expressed genes in mouse bone marrow and fetal liver cells]. Zhongguo Shi Yan Xue Ye Xue Za Zhi 2003, 11:444-449.
23. Yoshihara H., Arai F., Hosokawa K., et al. Thrombopoietin/MPL signaling regulates hematopoietic stem cell quiescence and interaction with the osteoblastic niche. Cell Stem Cell 2007, 1:685-697.
24. Morrison S.J., Spradling A.C. Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell 2008, 132:598-611.
25. Heazlewood S.Y., Neaves R.J., Williams B. Megakaryocytes co-localise with hemopoietic stem cells and release cytokines that up-regulate stem cell proliferation. Stem cell Research 2013, 11:782-792.
26. Gomei Y., Nakamura Y., Yoshihara H., et al. Functional differences between two Tie2 ligands, angiopoietin-1 and -2, in regulation of adult bone marrow hematopoietic stem cells. Exp Hematol 2010, 38:82-89.
27. Qian H., Buza-Vidas N., Hyland C.D., et al. Critical role of thrombopoietin in maintaining adult quiescent hematopoietic stem cells. Cell Stem Cell 2007, 1:671-684.
28. Rodriguez Mdel C., Bernad A., Aracil M. Interleukin-6 deficiency affects bone marrow stromal precursors, resulting in defective hematopoietic support. Blood 2004, 103:3349-3354.
29. Himburg H.A., Muramoto G.G., Daher P., et al. Pleiotrophin regulates the expansion and regeneration of hematopoietic stem cells. Nat Med 2010, 16:475-482.
30. Zhang C.C., Lodish H.F. Insulin-like growth factor 2 expressed in a novel fetal liver cell population is a growth factor for hematopoietic stem cells. Blood 2004, 103:2513-2521.
31. Mikkola H.K., Orkin S.H. The journey of developing hematopoietic stem cells. Development 2006, 133:3733-3744.
32. Wilpshaar J., Bhatia M., Kanhai H.H., et al. Engraftment potential of human fetal hematopoietic cells in NOD/SCID mice is not restricted to mitotically quiescent cells. Blood 2002, 100:120-127.
33. Spangrude G.J., Heimfeld S., Weissman I.L. Purification and characterization of mouse hematopoietic stem cells. Science 1988, 241:58-62.
34. Morrison S.J., Weissman I.L. The long-term repopulating subset of hematopoietic stem cells is deterministic and isolatable by phenotype. Immunity 1994, 1:661-673.
35. Orkin S.H., Zon L.I. Hematopoiesis: an evolving paradigm for stem cell biology. Cell 2008, 132:631-644.
36. Yoder M.C., Hiatt K., Mukherjee P. Invivo repopulating hematopoietic stem cells are present in the murine yolk sac at day 9.0 postcoitus. Proc Natl Acad Sci U S A 1997, 94:6776-6780.
37. Galloway J.L., Zon L.I. Ontogeny of hematopoiesis: examining the emergence of hematopoietic cells in the vertebrate embryo. Curr Top Dev Biol 2003, 53:139-158.
38. Lessard J., Faubert A., Sauvageau G. Genetic programs regulating HSC specification, maintenance and expansion. Oncogene 2004, 23:7199-7209.
39. Christensen J.L., Wright D.E., Wagers A.J., Weissman I.L. Circulation and chemotaxis of fetal hematopoietic stem cells. PLoS Biol 2004, 2:E75.
40. Wolber F.M., Leonard E., Michael S., Orschell-Traycoff C.M., Yoder M.C., Srour E.F. Roles of spleen and liver in development of the murine hematopoietic system. Exp Hematol 2002, 30:1010-1019.
41. Dzierzak E. Hematopoietic stem cells and their precursors: developmental diversity and lineage relationships. Immunol Rev 2002, 187:126-138.
42. Kiel M.J., Iwashita T., Yilmaz O.H., Morrison S.J. Spatial differences in hematopoiesis but not in stem cells indicate a lack of regional patterning in definitive hematopoietic stem cells. Dev Biol 2005, 283:29-39.
43. Yoder M.C. Embryonic hematopoiesis in mice and humans. Acta Paediatr Suppl 2002, 91:5-8.
44. Medvinsky A., Dzierzak E. Definitive hematopoiesis is autonomously initiated by the AGM region. Cell 1996, 86:897-906.
45. Matsubara A., Iwama A., Yamazaki S., et al. Endomucin, a CD34-like sialomucin, marks hematopoietic stem cells throughout development. J Exp Med 2005, 202:1483-1492.
46. Dzierzak E., Speck N.A. Of lineage and legacy: the development of mammalian hematopoietic stem cells. Nat Immunol 2008, 9:129-136.
47. Oostendorp R.A., Harvey K.N., Kusadasi N., et al. Stromal cell lines from mouse aorta-gonads-mesonephros subregions are potent supporters of hematopoietic stem cell activity. Blood 2002, 99:1183-1189.
48. Kusadasi N., Oostendorp R.A., Koevoet W.J., Dzierzak E.A., Ploemacher R.E. Stromal cells from murine embryonic aorta-gonad-mesonephros region, liver and gut mesentery expand human umbilical cord blood-derived CAFC(week6) in extended long-term cultures. Leukemia 2002, 16:1782-1790.
49. Matsuoka S., Tsuji K., Hisakawa H., et al. Generation of definitive hematopoietic stem cells from murine early yolk sac and paraaortic splanchnopleures by aorta-gonad-mesonephros region-derived stromal cells. Blood 2001, 98:6-12.
50. Xu M.J., Tsuji K., Ueda T., et al. Stimulation of mouse and human primitive hematopoiesis by murine embryonic aorta-gonad-mesonephros-derived stromal cell lines. Blood 1998, 92:2032-2040.
51. Ohneda O., Fennie C., Zheng Z., et al. Hematopoietic stem cell maintenance and differentiation are supported by embryonic aorta-gonad-mesonephros region-derived endothelium. Blood 1998, 92:908-919.
52. Oostendorp R.A., Medvinsky A.J., Kusadasi N., et al. Embryonal subregion-derived stromal cell lines from novel temperature-sensitive SV40 T antigen transgenic mice support hematopoiesis. JCell Sci 2002, 115:2099-2108.
53. Oostendorp R.A., Robin C., Steinhoff C., et al. Long-term maintenance of hematopoietic stem cells does not require contact with embryo-derived stromal cells in cocultures. Stem Cells 2005, 23:842-851.
54. Durand C., Robin C., Dzierzak E. Mesenchymal lineage potentials of aorta-gonad-mesonephros stromal clones. Haematologica 2006, 91:1172-1179.
55. Li Z., Lan Y., He W., et al. Mouse embryonic head as a site for hematopoietic stem cell development. Cell Stem Cell 2012, 11:663-675.
56. Johnson G.R., Moore M.A. Role of stem cell migration in initiation of mouse foetal liver haemopoiesis. Nature 1975, 258:726-728.
57. Houssaint E. Differentiation of the mouse hepatic primordium. II. Extrinsic origin of the haemopoietic cell line. Cell Differ 1981, 10:243-252.
58. Kumaravelu P., Hook L., Morrison A.M., et al. Quantitative developmental anatomy of definitive haematopoietic stem cells/long-term repopulating units (HSC/RUs): role of the aorta-gonad-mesonephros (AGM) region and the yolk sac in colonisation of the mouse embryonic liver. Development 2002, 129:4891-4899.
59. Gekas C., Dieterlen-Lievre F., Orkin S.H., Mikkola H.K. The placenta is a niche for hematopoietic stem cells. Dev Cell 2005, 8:365-375.
60. Ottersbach K., Dzierzak E. The murine placenta contains hematopoietic stem cells within the vascular labyrinth region. Dev Cell 2005, 8:377-387.
61. Morrison S.J., Hemmati H.D., Wandycz A.M., Weissman I.L. The purification and characterization of fetal liver hematopoietic stem cells. Proc Natl Acad Sci U S A 1995, 92:10302-10306.
62. Lansdorp P.M., Dragowska W., Mayani H. Ontogeny-related changes in proliferative potential of human hematopoietic cells. J Exp Med 1993, 178:787-791.
63. Lansdorp P.M. Developmental changes in the function of hematopoietic stem cells. Exp Hematol 1995, 23:187-191.
64. Friedrich C., Zausch E., Sugrue S.P., Gutierrez-Ramos J.C. Hematopoietic supportive functions of mouse bone marrow and fetal liver microenvironment: dissection of granulocyte, B-lymphocyte, and hematopoietic progenitor support at the stroma cell clone level. Blood 1996, 87:4596-4606.
65. Martin M.A., Bhatia M. Analysis of the human fetal liver hematopoietic microenvironment. Stem Cells Dev 2005, 14:493-504.
66. Arai F., Hosokawa K., Toyama H., Matsumoto Y., Suda T. Role of N-cadherin in the regulation of hematopoietic stem cells in the bone marrow niche. Ann N Y Acad Sci 2012, 1266:72-77.
67. Zhou K., Hu C.H., Huang L.F., Liu W.L., Sun H.Y. [Study on Wnt and Notch signalling involves in regulation of hematopoietic microenvironment.]. Zhonghua Xue Ye Xue Za Zhi 2009, 30:799-803.
68. Wagner W., Saffrich R., Wirkner U., et al. Hematopoietic progenitor cells and cellular microenvironment: behavioral and molecular changes upon interaction. Stem Cells 2005, 23:1180-1191.
69. Wittig O., Paez-Cortez J., Cardier J.E. Liver sinusoidal endothelial cells promote B lymphopoiesis from primitive hematopoietic cells. Stem Cells Dev 2010, 19:341-350.
70. Henningsen J., Rigbolt K.T., Blagoev B., Pedersen B.K., Kratchmarova I. Dynamics of the skeletal muscle secretome during myoblast differentiation. Mol Cell Proteomics 2010, 9:2482-2496.
71. Tsai S., Emerson S.G., Sieff C.A., Nathan D.G. Isolation of a human stromal cell strain secreting hemopoietic growth factors. J Cell Physiol 1986, 127:137-145.
72. Yokota T., Oritani K., Mitsui H., et al. Growth-supporting activities of fibronectin on hematopoietic stem/progenitor cells invitro and invivo: structural requirement for fibronectin activities of CS1 and cell-binding domains. Blood 1998, 91:3263-3272.
73. Iwasaki H., Arai F., Kubota Y., Dahl M., Suda T. Endothelial protein C receptor-expressing hematopoietic stem cells reside in the perisinusoidal niche in fetal liver. Blood 2010, 116:544-553.
74. Aiuti A., Cicchini C., Bernardini S., et al. Hematopoietic support and cytokine expression of murine-stable hepatocyte cell lines (MMH). Hepatology 1998, 28:1645-1654.
75. Chou S., Lodish H.F. Fetal liver hepatic progenitors are supportive stromal cells for hematopoietic stem cells. Proc Natl Acad Sci U S A 2010, 107:7799-7804.
76. Zhang C.C., Kaba M., Ge G., et al. Angiopoietin-like proteins stimulate exvivo expansion of hematopoietic stem cells. Nat Med 2006, 12:240-245.
77. Zhang H., Miao Z., He Z., Yang Y., Wang Y., Feng M. The existence of epithelial-to-mesenchymal cells with the ability to support hematopoiesis in human fetal liver. Cell Biol Int 2005, 29:213-219.
78. Lim Y.S., Kim K.A., Jung J.O., et al. Modulation of cytokeratin expression during invitro cultivation of human hepatic stellate cells: evidence of transdifferentiation from epithelial to mesenchymal phenotype. Histochem Cell Biol 2002, 118:127-136.
79. Chagraoui J., Lepage-Noll A., Anjo A., Uzan G., Charbord P. Fetal liver stroma consists of cells in epithelial-to-mesenchymal transition. Blood 2003, 101:2973-2982.
80. Charbord P., Moore K. Gene expression in stem cell-supporting stromal cell lines. Ann N Y Acad Sci 2005, 1044:159-167.
81. Zou Y.R., Kottmann A.H., Kuroda M., Taniuchi I., Littman D.R. Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature 1998, 393:595-599.
82. Papadopoulos N., Simopoulos C., Sigalas J., Kotini A., Cheva A., Tamiolakis D. Induction of hepatic hematopoiesis with tenascin-C expression during the second trimester of development. Eur J Obstet Gynecol Reprod Biol 2004, 113:56-60.
83. Zhou K., Huang L., Zhou Z., et al. Wnt and Notch signaling pathways selectively regulating hematopoiesis. Ann Hematol 2010, 89:749-757.
84. Murdoch B., Chadwick K., Martin M., et al. Wnt-5A augments repopulating capacity and primitive hematopoietic development of human blood stem cells invivo. Proc Natl Acad Sci U S A 2003, 100:3422-3427.
85. Bafico A., Gazit A., Pramila T., Finch P.W., Yaniv A., Aaronson S.A. Interaction of frizzled related protein (FRP) with Wnt ligands and the frizzled receptor suggests alternative mechanisms for FRP inhibition of Wnt signaling. J Biol Chem 1999, 274:16180-16187.
86. Caricasole A., Ferraro T., Iacovelli L., et al. Functional characterization of WNT7A signaling in PC12 cells: interaction with A FZD5 x LRP6 receptor complex and modulation by Dickkopf proteins. JBiol Chem 2003, 278:37024-37031.
87. Stier S., Cheng T., Dombkowski D., Carlesso N., Scadden D.T. Notch1 activation increases hematopoietic stem cell self-renewal invivo and favors lymphoid over myeloid lineage outcome. Blood 2002, 99:2369-2378.
88. Grassinger J., Haylock D.N., Storan M.J., et al. Thrombin-cleaved osteopontin regulates hemopoietic stem and progenitor cell functions through interactions with alpha9beta1 and alpha4beta1 integrins. Blood 2009, 114:49-59.
89. Iwata M., Awaya N., Graf L., Kahl C., Torok-Storb B. Human marrow stromal cells activate monocytes to secrete osteopontin, which down-regulates Notch1 gene expression in CD34+ cells. Blood 2004, 103:4496-4502.
90. Bertrand J.Y., Desanti G.E., Lo-Man R., Leclerc C., Cumano A., Golub R. Fetal spleen stroma drives macrophage commitment. Development 2006, 133:3619-3628.
91. Morita Y., Iseki A., Okamura S., Suzuki S., Nakauchi H., Ema H. Functional characterization of hematopoietic stem cells in the spleen. Exp Hematol 2011, 39:351-359 e353.
92. Shatry A.M., Levy R.B. Engraftment of splenic tissue as a method to investigate repopulation by hematopoietic cells from host and donor marrow. Stem Cells Dev 2004, 13:390-399.
93. Faissner A., Kruse J. J1/tenascin is a repulsive substrate for central nervous system neurons. Neuron 1990, 5:627-637.
94. Bowie M.B., Kent D.G., Dykstra B., et al. Identification of a new intrinsically timed developmental checkpoint that reprograms key hematopoietic stem cell properties. Proc Natl Acad Sci U S A 2007, 104:5878-5882.
95. Carvalho T.L., Mota-Santos T., Cumano A., Demengeot J., Vieira P. Arrested B lymphopoiesis and persistence of activated B cells in adult interleukin 7(-/)- mice. J Exp Med 2001, 194:1141-1150.
96. Bowie M.B., McKnight K.D., Kent D.G., McCaffrey L., Hoodless P.A., Eaves C.J. Hematopoietic stem cells proliferate until after birth and show a reversible phase-specific engraftment defect. J Clin Invest 2006, 116:2808-2816.
97. Ciriza J., Garcia-Ojeda M.E. Expression of migration-related genes is progressively upregulated in murine Lineage-Sca-1+c-Kit+ population from the fetal to adult stages of development. Stem Cell Res Ther 2010, 1:14.
98. McGrath K.E., Koniski A.D., Maltby K.M., McGann J.K., Palis J. Embryonic expression and function of the chemokine SDF-1 and its receptor, CXCR4. Dev Biol 1999, 213:442-456.
99. Ara T., Tokoyoda K., Sugiyama T., Egawa T., Kawabata K., Nagasawa T. Long-term hematopoietic stem cells require stromal cell-derived factor-1 for colonizing bone marrow during ontogeny. Immunity 2003, 19:257-267.
100. Wright D.E., Bowman E.P., Wagers A.J., Butcher E.C., Weissman I.L. Hematopoietic stem cells are uniquely selective in their migratory response to chemokines. J Exp Med 2002, 195:1145-1154.
101. Peled A., Kollet O., Ponomaryov T., et al. The chemokine SDF-1 activates the integrins LFA-1, VLA-4, and VLA-5 on immature human CD34(+) cells: role in transendothelial/stromal migration and engraftment of NOD/SCID mice. Blood 2000, 95:3289-3296.
102. Lataillade J.J., Clay D., Dupuy C., et al. Chemokine SDF-1 enhances circulating CD34(+) cell proliferation in synergy with cytokines: possible role in progenitor survival. Blood 2000, 95:756-768.
103. Puri M.C., Nagy A. Concise review: Embryonic stem cells versus induced pluripotent stem cells: the game is on. Stem Cells 2012, 30:10-14.