Primitive and committed human hematopoietic progenitor cells interact with primary murine neural cells and are induced to undergo self-renewing cell divisions

Experimental Hematology

Volumn 35, Issue 12, 2007, Pages 1858-1871

  Gottschling, Sandra ^a   Eckstein, Volker ^a   Saffrich, Rainer ^a   Jonáš, Alexandr ^b   Uhrig, Markus ^a   Krause, Ulf ^a   Seckinger, Anja ^a   Miesala, Katrin ^a   Horsch, Kerstin ^a   Straub, Beate K ^a   Ho, Anthony D ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; BETA1 INTEGRIN; BETA2 INTEGRIN; INTEGRIN;

ANIMAL CELL; ARTICLE; ASTROCYTE; BONE MARROW CELL; CELL ADHESION; CELL DIFFERENTIATION; CELL DIVISION; CELL INTERACTION; CELL ISOLATION; CELL MIGRATION; CELL RENEWAL; CENTRAL NERVOUS SYSTEM; CHEMOTAXIS; COCULTURE; COLONY FORMING CELL; CONTROLLED STUDY; CULTURE MEDIUM; FLOW CYTOMETRY; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; IMAGE ANALYSIS; IMMUNOHISTOCHEMISTRY; LONG TERM CULTURE INITIATING CELL; MICROSCOPY; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; ASTROCYTES; CELL DIVISION; CELL LINEAGE; CELL MOVEMENT; HEMATOPOIETIC STEM CELLS; HUMANS; MICE;

ANIMALIA; MURINAE;

EID: 36148956146     PISSN: 0301472X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.exphem.2007.06.013     Document Type: Article

References (81)

1. Massengale M., Wagers A.J., Vogel H., and Weissman I.L. Hematopoietic cells maintain hematopoietic fates upon entering the brain. J Exp Med 201 (2005) 1579-1589
2. Davoust N., Vuaillat C., Cavillon G., et al. Bone marrow CD34+/B220+ progenitors target the inflamed brain and display in vitro differentiation potential toward microglia. FASEB J 20 (2006) 2081-2092
3. Cogle C.R., Yachnis A.T., Laywell E.D., Zander D.S., Wingard J.R., and Steindler D.A. Bone marrow transdifferentiation in brain after transplantation: a retrospective study. Lancet 363 (2004) 1432-1437
4. Sanchez-Ramos J.R. Neural cells derived from adult bone marrow and umbilical cord blood. J Neurosci Res 69 (2002) 880-893
5. Vitry S., Bertrand J.Y., Cumano A., and Dubois-Dalcq M. Primordial hematopoietic stem cells generate microglia but not myelin-forming cells in a neural environment. J Neurosci 23 (2003) 10724-10731
6. Tersikh A.V., Easterday M.C., Li L., et al. From hematopoiesis to neuropoesis: evidence of overlapping genetic programs. Proc Natl Acad Sci U S A 98 (2001) 7934-7939
7. Goolsby J., Marty M.C., Heletz D., et al. Hematopoietic progenitors express neural genes. Proc Natl Acad Sci U S A 100 (2003) 14926-14931
8. Kléber M., Lee H.-Y., Wurdak H., et al. Neural crest stem cell maintenance by combinatorial Wnt and BMP signalling. J Cell Biol 169 (2005) 309-320
9. Reya T., Duncan A.W., Ailles L., et al. A role for Wnt signaling in self-renewal of haematopoietic stem cells. Nature 423 (2003) 409-414
10. Stier S., Cheng T., Dombrowski D., Carlesso N., and Scadden D.T. Notch1 activation increases hematopoietic stem cell self-renewal in vivo and favors lymphoid over myeloid lineage outcome. Blood 99 (2002) 2369-2378
11. Mayani H., Dragowska W., and Lansdorp P.M. Lineage commitment in human hemopoiesis involves asymmetric cell division of multipotent progenitors and does not appear to be influenced by cytokines. J Cell Physiol 157 (1993) 579-586
12. Huang S., Law P., Francis K., et al. Symmetry of initial cell divisions among primitive hematopoietic progenitors is independent of ontogenetic age and regulatory molecules. Blood 94 (1999) 2595-2604
13. Punzel M., Liu D., Zhang T., et al. The symmetry of initial divisions of human hematopoietic progenitors is altered only by the cellular microenvironment. Exp Hematol 31 (2003) 339-347
14. Punzel M., and Ho A.D. Divisional history and pluripotency of human hematopoietic stem cells. Ann N Y Acad Sci 938 (2001) 72-81 discussion 81-82
15. Ema H., Takano H., Sudo K., and Nakauchi H. In vitro self-renewal division of hematopoietic stem cells. J Exp Med 192 (2000) 1281-1288
16. Srour E.F., Tong X., Sung K.W., et al. Modulation of in vitro proliferation kinetics and primitive hematopoietic potential of individual human CD34+CD38-/lo cells in G0. Blood 105 (2005) 3109-3116
17. Giebel B., Zhang T., Beckmann J., et al. Primitive human hematopoietic cells give rise to differentially specified daughter cells upon their initial cell division. Blood 107 (2006) 2146-2152
18. Takano H., Ema H., Sudo K., et al. Asymmetric division and lineage commitment at the level of hematopoietic stem cells: interference from differentiation in daughter cell and granddaughter cell pairs. J Exp Med 199 (2004) 295-302
19. Suda T., Suda J., and Ogawa M. Disparate differentiation in mouse hematopoietic colonies derived from paired progenitors. Proc Natl Acad Sci U S A 81 (1984) 2520-2524
20. hi stem cells to bone marrow stroma. J Clin Invest 90 (1992) 358-367
21. 2-integrins and selectins. Blood 98 (2001) 2403-2411
22. Miyake K., Weissman I.L., Greenberger J.S., et al. Evidence for the role of the integrin VLA-4 in lympho-hemopoiesis. J Exp Med 173 (1991) 599-607
23. Arroyo A.G., Yang J.T., Rayburn H., et al. α4 integrins regulate the proliferation/differentiation balance of multilineage hematopoietic progenitors ex vivo. Immunity 11 (1999) 555-566
24. Scott L.M., Priestley G.V., and Papayannopoulou T. Deletion of alpha 4 integrins from adult hematopoietic cells reveals roles in homeostasis, regeneration, and homing. Mol Cell Biol 23 (2003) 9349-9360
25. Priestley G.V., Scott L.M., Ulyanova T., et al. Lack of α4 integrin expression in stem cells restricts competitive function and self-renewal capacity. Blood 107 (2006) 2959-2967
26. Giovino M., Wang H., Sykes M., et al. Role of VLA-4 and VLA-5 in ex vivo maintenance of human and pig hematopoiesis in human stroma-supported long-term cultures. Exp Hematol 33 (2005) 363-370
27. 1-integrin-dependent mechanism. Stem Cells 25 (2007) 798-806
28. Wagner W., Ansorge A., Wirkner U., et al. Molecular evidence for stem cell function of the slow dividing fraction among human hematopoietic progenitor cells by genome wide analysis. Blood 104 (2004) 675-686
29. Moore K.A., Hideo E., and Lemischka I.R. In vitro maintenance of highly purified, transplantable hematopoietic stem cells. Blood 89 (1997) 4337-4347
30. - progenitors to maintain primitive function and immunophenotype in vitro. Exp Hematol 26 (1998) 612-619
31. Majumdar M.K., Thiede M.A., Haynesworth S.E., et al. Human marrow-derived mesenchymal stem cells (MSCs) express hematopoietic cytokines and support long-term hematopoiesis when differentiated toward stromal and osteogenic lineages. J Hematother Stem Cell Res 9 (2000) 841-848
32. Morrison R.S., and de Vellis J. Growth of purified astrocytes in a chemically defined medium. Proc Natl Acad Sci U S A 78 (1981) 7205-7209
33. Raff M.C., Miller R.H., and Noble M. A glial progenitor cell that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium. Nature 303 (1983) 390-396
34. Goslin K., Asmussen H., and Banker G. Rat hippocampal neurons in low-density culture. In: Banker G., and Goslin K. (Eds). Culturing Nerve Cells. 2nd ed. (1998), Massachusetts Institute of Technology, Cambridge, MA 339-379
35. Reyes M., Lund T., Lenvik T., et al. Purification and ex vivo expansion of postnatal human marrow mesodermal progenitor cells. Blood 98 (2001) 2615-2625
36. Wagner W., Wein F., Seckinger A., et al. Comparative characteristics of mesenchymal stem cells from human bone marrow, adipose tissue, and umbilical cord blood. Exp Hematol 33 (2005) 1402-1416
37. Wagner W., Feldmann Jr. R.E., Seckinger A., et al. The heterogeneity of human mesenchymal stem cells preparations-evidence from simultaneous analysis of proteomes and transcriptomes. Exp Hematol 34 (2006) 536-548
38. Dominici M., Le Blanc K., Mueller I., et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8 (2006) 315-317
39. Keating A. Mesenchymal stromal cells. Curr Opin Hematol 13 (2006) 419-425
40. Pittenger M.F., Mackay A.M., Beck S.C., et al. Multilineage potential of adult human mesenchymal stem cells. Science 284 (1999) 143-147
41. Jaiswal N., Haynesworth S.E., Caplan A.I., et al. Osteogenic differentiation of purified, culture-expanded human mesenchymal stem cells in vitro. J Cell Biochem 64 (1997) 295-312
42. Mackay A.M., Beck S.C., Murphy J.M., et al. Chondrogenic differentiation of cultured human mesenchymal stem cells from marrow. Tissue Eng 4 (1998) 415-428
43. Liesveld J.L., Winslow J.M., Frediani K.E., et al. Expression of integrins and examination of their adhesive function in normal and leukemic hematopoietic cells. Blood (1993) 112-121
44. Meerschaert J., and Furie M.B. Monocytes use either CD11/CD18 or VLA-4 to migrate across human endothelium in vitro. J Immunol 152 (1994) 1915-1926
45. Quinlan R.A., and Franke W.W. Molecular interactions in intermediate-sized filaments revealed by chemical crosslinking. Heteropolymers of vimentin and glial filament and protein in cultured human glioma cells. Eur J Biochem 132 (1983) 477-484
46. Taylor C.A., Cheng C.P., Espinosa L.A., Tang B.T., Parker D., and Herfkens R.J. In vivo quantification of blood flow and wall shear stress in the human abdominal aorta during lower limb exercise. Ann Biomed Eng 30 (2002) 402-408
47. Simard A.R., and Rivest S. Bone marrow stem cells have the ability to populate the entire central nervous system into fully differentiated parenchymal microglia. FASEB J 18 (2004) 998-1000
48. Corti S., Locatelli F., Donadoni C., et al. Neuroectodermal and microglial differentiation of bone marrow stem cell in the mouse spinal cord an sensory ganglia. J Neursci Res 70 (2002) 721-733
49. De Wynter E.A., Buck D., Hart C., et al. CD34+AC133+ cells isolated from cord blood are highly enriched in long-term culture-initiating cells, NOD/SCID-repopulating cells and dendritic progenitors. Stem Cells 16 (2001) 387-396
50. Hess D.A., Wirthlin L., Craft T.P., et al. Selection based on CD133 and high aldehyde dehydrogenase activity isolates long-term reconstituting human hematopoietic stem cells. Blood 107 (2006) 2162-2169
51. Ratajczak M.Z., Kucia M., Reca R., Majka M., Janowska-Wieczorek A., and Ratajczak J. Stem cells plasticity revisited: CXCR4-positive cells expressing mRNA for early muscle, liver and neural cells "hide out" in the bone marrow. Leukemia 18 (2004) 29-40
52. Kucia M., Zhang Y.P., Reca R., et al. Cells enriched in markers of neural tissue-committed stem cells reside in the bone marrow and are mobilized into the peripheral blood following stroke. Leukemia 20 (2006) 18-28
53. Kania G., Corbeil D., Fuchs J., et al. Somatic stem cell marker prominin-1/CD133 is expressed in embryonic stem cell-derived progenitors. Stem Cells 23 (2005) 791-804
54. Tamaki S., Eckert K., He D., et al. Engraftment of sorted/expanded human central nervous system stem cells from fetal brain. J Neurosci Res 69 (2002) 976-986
55. Florek M., Haase M., Marzesco A.-M., et al. Prominin-1/CD133, a neural and hematopoietic stem cell marker, is expressed in adult human differentiated cells and certain types of kidney cancer. Cell Tissue Res 319 (2005) 15-26
56. Tham T.N., Lazarini F., Franceschini I.A., Lachapelle F., Amara A., and Dubois-Dalcq M. Developmental pattern of expression of the alpha chemokine stromal cell-derived factor 1 in the rat central nervous system. Eur J Neurosci 13 (2001) 845-856
57. Stumm R.K., Rummel J., Junker V., et al. A dual role for the SDF-1/CXCR4 chemokine receptor system in adult brain: Isoform-selective regulation of SDF-1 expression modulates CXCR4-dependent neuronal plasticity and cerebral leukocyte recruitment after focal ischemia. J Neurosci 22 (2002) 5865-5878
58. Miller J.T., Bartley J.H., Wimborne H.J.C., et al. The neuroblast and angioblast chemotaxic factor SDF-1 (CXCL12) expression is briefly up regulated by reactive astrocytes in brain following neonatal hypoxic-ischemic injury. Neuroscience 6 (2005) 63-73
59. Peled A., Kollet O., Ponomaryov T., et al. The chemokine SDF-1 activates the integrins LFA-1, VLA-4, and VLA-5 on immature CD34+ cells: role in transendothelial/stromal migration and engraftment of NOD/SCID mice. Blood 95 (2000) 3289-3296
60. Liesi P., Kirkwood T., and Vaheri A. Fibronectin is expressed by astrocytes cultured from embryonic and early postnatal rat brain. Exp Cell Res 163 (1986) 175-185
61. Tom V.J., Doller C.M., Malouf A.T., and Silver J. Astrocyte-associated fibronectin is critical for axonal regeneration in adult white matter. J Neurosci 24 (2004) 9282-9290
62. Birdsall H.H., Lane C., Ramser M.N., and Anderson D.C. Induction of VCAM-1 and ICAM-1 on human neural cells and mechanisms of mononuclear leukocyte adherence. J Immunol 148 (1992) 2717-2723
63. Ni H.A.T., Hu S., Sheng W.S., et al. High-level expression of functional chemokine receptor CXCR4 on human neural precursor cells. Brain Res Dev Brain Res 152 (2004) 159-169
64. Belmadani A., Tran P.B., Ren D., Assimacopoulos S., Grove E.A., and Miller R.J. The chemokine stromal cell-derived factor-1 regulates the migration of sensory neuron progenitors. J Neurosci 25 (2005) 3995-4003
65. Pixley S.K. CNS glial cells support in vitro survival, division, and differentiation of dissociated olfactory neuronal progenitor cells. Neuron 8 (1992) 1191-1204
66. Song H., Stevens C.F., and Gage F.H. Astroglia induce neurogenesis from adult neural stem cells. Nature 417 (2002) 39-44
67. Shen Q., Goderie S.K., Jin L., et al. Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science 304 (2004) 1338-1340
68. - cells and SCID-repopulating cells. Blood 105 (2005) 576-583
69. Munoz J.R., Stoutenger B.R., Robinson A.P., Spees J.L., and Prockop D.J. Human stem/progenitor cells from bone marrow promote neurogenesis of endogenous neural stem cells in the hippocampus of mice. Proc Natl Acad Sci U S A 102 (2005) 18171-18176
70. Rivera F.J., Couillard-Despres S., Pedre X., et al. Mesenchymal stem cells instruct oligodendrogenic fate decision on adult neural stem cells. Stem Cells 24 (2006) 2209-2219
71. Tsai R.Y.L., and McKay R.D.G. Cell contact regulates fate choice by cortical stem cells. J Neurosci 20 (2000) 3725-3735
72. Lim D.A., and Alvarez-Buylla A. Interaction between astrocytes and adult subventricular zone precursors simulates neurogenesis. Proc Natl Acad Sci U S A 96 (1999) 7526-7536
73. Hall P.E., Lathia J.D., Miller N.G.A., Caldwell M.A., and Ffrench-Constant C. Integrins are markers of human neural stem cells. Stem Cells 24 (2006) 2078-2084
74. Rapp G., Kunke D., Holter J., et al. Efficient expansion and gene transduction of mouse neural stem/progenitor cells on recombinant fibronectin. Neuroscience 124 (2004) 823-830
75. Flanagan L.A., Rebaza L.M., Derzic S., Schwartz P.H., and Monuki E.S. Regulation of human neural precursor cells by laminin and integrins. J Neurosci Res 83 (2006) 845-856
76. Haydar T.F., Ang Jr. E., and Rakic P. Mitotic spindle rotation and mode of cell division in the developing telencephalon. Proc Natl Acad Sci U S A 100 (2003) 2890-2895
77. Jan Y.N., and Jan L.Y. Asymmetric cell division in the Drosophila nervous system. Nat Rev Neurosci 2 (2001) 772-779
78. Li K., Lee S.M., Su R.J., et al. Multipotent neural precursors express neural and hematopoietic factors, and enhance ex vivo expansion of cord blood CD34+ cells, colony forming units and NOD/SCID-repopulating cells in contact and noncontact cultures. Leukemia 19 (2005) 91-97
79. Nagai A., Nakagawa E., Choi H.B., Hatori K., Kobayashi S., and Kim S.U. Erythropoietin and erythropoietin receptors in human CNS neurons, astrocytes, microglia, and oligodendrocytes grown in culture. J Neuropathol Exp Neurol 60 (2001) 386-392
80. Jiang Y., Henderson D., Blackstad M., Chen A., Miller R.F., and Verfaillie C.M. Neuroectodermal differentiation from mouse multipotent adult progenitor cells. Proc Natl Acad Sci U S A 100 (2003) 11854-11860
81. Ling E.A., and Wong W.C. The origin and nature of ramified and amoeboid microglia: a historical review and current concepts. Glia 7 (1993) 9-18