Erythroblastic islands: Niches for erythropoiesis

Blood

Volumn 112, Issue 3, 2008, Pages 470-478

  Chasis, Joel Anne ^a,b   Mohandas, Narla ^a,b,c  

^a LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c NEW YORK BLOOD CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD163 ANTIGEN; CD69 ANTIGEN; ERYTHROPOIETIN; GAMMA INTERFERON; INTERLEUKIN 6; TRANSCRIPTION FACTOR GATA 1; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; VASCULAR CELL ADHESION MOLECULE 1; VASCULOTROPIN A; VERY LATE ACTIVATION ANTIGEN 4;

ANEMIA; ARTICLE; BONE MARROW; CELL ADHESION; CELL DIFFERENTIATION; CELL FUNCTION; ERYTHROBLAST; ERYTHROPOIESIS; EXTRACELLULAR MATRIX; HUMAN; INFLAMMATION; MACROPHAGE; MYELODYSPLASTIC SYNDROME; NONHUMAN; PRIORITY JOURNAL; THALASSEMIA; CYTOLOGY; FEEDBACK SYSTEM; PHYSIOLOGY; REVIEW;

BONE MARROW; CELL ADHESION; ERYTHROBLASTS; ERYTHROPOIESIS; EXTRACELLULAR MATRIX; FEEDBACK, BIOCHEMICAL; HUMANS; MACROPHAGES;

EID: 50949089311     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2008-03-077883     Document Type: Article

References (99)

1. Bessis M. L'ilot erythroblastique. Unite functionelle de la moelle osseuse. Rev Hematol. 1958; 13:8-11.
2. Bessis MC, Breton-Gorius J. Iron metabolism in the bone marrow as seen by electron microscopy: a critical review. Blood. 1962;19:635-663.
3. Mohandas N, Prenant M. Three-dimensional model of bone marrow. Blood. 1978;51:633-643.
4. Allen TD, Dexter TM. Ultrastructural aspects of erythropoietic differentiation in long-term bone marrow culture. Differentiation. 1982;21:86-94.
5. Bessis M, Mize C, Prenant M. Erythropoiesis: comparison of in vivo and in vitro amplification. Blood Cells. 1978;4:155-174.
6. Le Charpentier Y, Prenant M. [Isolation of erythroblastic islands. Study by optical and scanning electron microscopy (author's transl)]. Nouv Rev Fr Hematol. 1975;15:119-140.
7. Lee SH, Crocker PR, Westaby S, et al. Isolation and immunocytochemical characterization of human bone marrow stromal macrophages in hemopoietic clusters. J Exp Med. 1988;168:1193-1198.
8. Sadahira Y, Mori M. Role of the macrophage in erythropoiesis. Pathol Int. 1999;49:841-848.
9. Yokoyama T, Kitagawa H, Takeuchi T, Tsukahara S, Kannan Y. No apoptotic cell death of erythroid cells of erythroblastic islands in bone marrow of healthy rats. J Vet Med Sci. 2002;64:913-919.
10. Austyn JM, Gordon S. F4/80, a monoclonal antibody directed specifically against the mouse macrophage. Eur J Immunol. 1981;11:805-815.
11. Hume DA, Robinson AP, MacPherson GG, Gordon S. The mononuclear phagocyte system of the mouse defined by immunohistochemical localization of antigen F4/80. Relationship between macrophages, Langerhans cells, reticular cells, and dendritic cells in lymphoid and hematopoietic organs. J Exp Med. 1983;158:1522-1536.
12. McKnight AJ, Macfarlane AJ, Dri P, Turley L, Willis AC, Gordon S. Molecular cloning of F4/80, a murine macrophage-restricted cell surface glycoprotein with homology to the G-protein-linked transmembrane 7 hormone receptor family. J Biol Chem. 1996;271:486-489.
13. Monner DA, Muhlradt PF. Surface expression of Forssman glycosphingolipid antigen on murine bone marrow-derived macrophages is subject to both temporal and population-specific regulation and is modulated by IL-4 and IL-6. Immunobiology. 1993;188:82-98.
14. Sadahira Y, Mori M, Awai M, Watarai S, Yasuda T. Forssman glycosphingolipid as an immunohistochemical marker for mouse stromal macrophages in hematopoietic foci. Blood. 1988;72:42-48.
15. Sadahira Y, Yasuda T, Kimoto T. Regulation of Forssman antigen expression during maturation of mouse stromal macrophages in haematopoietic foci. Immunology. 1991;73:498-504.
16. Yokoyama T, Etoh T, Kitagawa H, Tsukahara S, Kannan Y. Migration of erythroblastic islands toward the sinusoid as erythroid maturation proceeds in rat bone marrow. J Vet Med Sci. 2003; 65:449-452.
17. Hanspal M, Hanspal J. The association of erythroblasts with macrophages promotes erythroid proliferation and maturation: a 30-kD heparin-binding protein is involved in this contact. Blood. 1994;84:3494-3504.
18. Hanspal M, Smockova Y, Uong Q. Molecular identification and functional characterization of a novel protein that mediates the attachment of erythroblasts to macrophages. Blood. 1998;92: 2940-2950.
19. Soni S, Bala S, Kumar A, Hanspal M. Changing pattern of the subcellular distribution of erythroblast macrophage protein (Emp) during macrophage differentiation. Blood Cells Mol Dis. 2007; 38:25-31.
20. Soni S, Bala S, Gwynn B, Sahr KE, Peters LL, Hanspal M. Absence of erythroblast macrophage protein (Emp) leads to failure of erythroblast nuclear extrusion. J Biol Chem. 2006;281:20181-20189.
21. Sadahira Y, Yoshino T, Monobe Y. Very late activation antigen 4-vascular cell adhesion molecule 1 interaction is involved in the formation of erythroblastic islands. J Exp Med. 1995;181:411-415.
22. Kingsley PD, Malik J, Fantauzzo KA, Palis J. Yolk sac-derived primitive erythroblasts enucleate during mammalian embryogenesis. Blood. 2004;104: 19-25.
23. McGrath KE, Kingsley PD, Koniski AD, Porter RL, Bushnell TP, Palis J. Enucleation of primitive erythroid cells generates a transient population of "pyrenocytes" in the mammalian fetus. Blood. 2008;111:2409-2417.
24. Lee G, Lo A, Short SA, et al. Targeted gene deletion demonstrates that the cell adhesion molecule ICAM-4 is critical for erythroblastic island formation. Blood. 2006;108:2064-2071.
25. Lee G, Spring FA, Parsons SF, et al. Novel secreted isoform of adhesion molecule ICAM-4: potential regulator of membrane-associated ICAM-4 interactions. Blood. 2003;101:1790-1797.
26. Crocker PR, Gordon S. Properties and distribution of a lectin-like hemagglutinin differentially expressed by murine stromal tissue macrophages. J Exp Med. 1986;164:1862-1875.
27. Crocker PR, Gordon S. Mouse macrophage hemagglutinin (sheep erythrocyte receptor) with specificity for sialylated glycoconjugates characterized by a monoclonal antibody. J Exp Med. 1989;169:1333-1346.
28. Morris L, Crocker PR, Fraser I, Hill M, Gordon S. Expression of a divalent cation-dependent erythroblast adhesion receptor by stromal macrophages from murine bone marrow. J Cell Sci. 1991;99(Pt 1):141-147.
29. Crocker PR, Werb Z, Gordon S, Bainton DF. Ultrastructural localization of a macrophagerestricted sialic acid binding hemagglutinin, SER, in macrophage-hematopoietic cell clusters. Blood. 1990;76:1131-1138.
30. Barbé E, Huitinga I, Dopp EA, Bauer J, Dijkstra CD. A novel bone marrow frozen section assay for studying hematopoietic interactions in situ: the role of stromal bone marrow macrophages in erythroblast binding. J Cell Sci. 1996;109(Pt 12): 2937-2945.
31. Fabriek BO, Polfliet MM, Vloet RP, et al. The macrophage CD163 surface glycoprotein is an erythroblast adhesion receptor. Blood. 2007;109: 5223-5229.
32. DeMali KA, Wennerberg K, Burridge K. Integrin signaling to the actin cytoskeleton. Curr Opin Cell Biol. 2003;15:572-582.
33. Seki M, Shirasawa H. Role of the reticular cells during maturation process of the erythroblast. 3. The fate of phagocytized nucleus. Acta Pathol Jpn. 1965;15:387-405.
34. Skutelsky E, Danon D. On the expulsion of the erythroid nucleus and its phagocytosis. Anat Rec. 1972;173:123-126.
35. Lee JC, Gimm JA, Lo AJ, et al. Mechanism of protein sorting during erythroblast enucleation: role of cytoskeletal connectivity. Blood. 2004;103: 1912-1919.
36. Yoshida H, Kawane K, Koike M, Mori Y, Uchiyama Y, Nagata S. Phosphatidylserine-dependent engulfment by macrophages of nuclei from erythroid precursor cells. Nature. 2005;437: 754-758.
37. Allen TD, Testa NG. Cellular interactions in erythroblastic islands in long-term bone marrow cultures, as studied by time-lapse video. Blood Cells. 1991;17:29-38, discussion 39-43.
38. Hanayama R, Tanaka M, Miwa K, Shinohara A, Iwamatsu A, Nagata S. Identification of a factor that links apoptotic cells to phagocytes. Nature. 2002;417:182-187.
39. Kawane K, Fukuyama H, Kondoh G, et al. Requirement of DNase II for definitive erythropoiesis in the mouse fetal liver. Science. 2001;292:1546-1549.
40. Leimberg MJ, Prus E, Konijn AM, Fibach E. Macrophages function as a ferritin iron source for cultured human erythroid precursors. J Cell Biochem. 2008;103:1211-1218.
41. Iavarone A, King ER, Dai XM, Leone G, Stanley ER, Lasorella A. Retinoblastoma promotes definitive erythropoiesis by repressing Id2 in fetal liver macrophages. Nature. 2004;432:1040-1045.
42. Clarke AR, Maandag ER, van Roon M, et al. Requirement for a functional Rb-1 gene in murine development. Nature. 1992;359:328-330.
43. Jacks T, Fazeli A, Schmitt E, Bronson R, Goodell M, Weinberg R. Effects of an Rb mutation in the mouse. Nature. 1992;359:295-300.
44. Lee E, Chang C, Hu N, et al. Mice deficient for Rb are nonviable and show defects in neurogenesis and haematopoiesis. Nature. 1992;359:288-294.
45. Spike BT, Dibling BC, Macleod KF. Hypoxic stress underlies defects in erythroblast islands in the Rb-null mouse. Blood. 2007;110:2173-2181.
46. Clark AJ, Doyle KM, Humbert PO. Cell-intrinsic requirement for pRb in erythropoiesis. Blood. 2004;104:1324-1326.
47. Sankaran VG, Orkin SH, Walkley CR. Rb intrinsically promotes erythropoiesis by coupling cell cycle exit with mitochondrial biogenesis. Genes Dev. 2008;22:463-475.
48. Liu XS, Li XH, Wang Y, et al. Disruption of palladin leads to defects in definitive erythropoiesis by interfering with erythroblastic island formation in mouse fetal liver. Blood. 2007;110:870-876.
49. Koury MJ, Bondurant M. Erythropoietin retards DNA breakdown and prevents programmed death in erythroid progenitor cells. Science. 1990; 248:378-381.
50. De Maria R, Zeuner A, Eramo A, et al. Negative regulation of erythropoiesis by caspase-mediated cleavage of GATA-1. Nature. 1999;401:489-493.
51. Socolovsky M, Murrell M, Liu Y, Pop R, Porpiglia E, Levchenko A. Negative autoregulation by FAS mediates robust fetal erythropoiesis. PLoS Biol. 2007;5:e252.
52. Niho Y, Asano Y. Fas/Fas ligand and hematopoietic progenitor cells. Curr Opin Hematol. 1998;5: 163-165.
53. Rhodes MM, Kopsombut P, Bondurant MC, Price JO, Koury MJ. Adherence to macrophages in erythroblastic islands enhances erythroblast proliferation and increases erythrocyte production by a different mechanism than erythropoietin. Blood. 2008;111:1700-1708.
54. Inada T, Iwama A, Sakano S, Ohno M, Sawada K, Suda T. Selective expression of the receptor tyrosine kinase, HTK, on human erythroid progenitor cells. Blood. 1997;89:2757-2765.
55. Suenobu S, Takakura N, Inada T, et al. A role of EphB4 receptor and its ligand, ephrin-B2, in erythropoiesis. Biochem Biophys Res Commun. 2002;293:1124-1131.
56. Muta K, Krantz SB, Bondurant MC, Dai CH. Stem cell factor retards differentiation of normal human erythroid progenitor cells while stimulating proliferation. Blood. 1995;86:572-580.
57. Sadahira Y, Yasuda T, Yoshino T, et al. Impaired splenic erythropoiesis in phlebotomized mice injected with CL2MDP-liposome: an experimental model for studying the role of stromal macrophages in erythropoiesis. J Leukoc Biol. 2000;68: 464-470.
58. Gutiérrez L, Lindeboom F, Langeveld A, Grosveld F, Philipsen S, Whyatt D. Homotypic signalling regulates Gata1 activity in the erythroblastic island. Development. 2004;131:3183-3193.
59. Fujiwara Y, Browne CP, Cunniff K, Goff SC, Orkin SH. Arrested development of embryonic red cell precursors in mouse embryos lacking transcription factor GATA-1. Proc Natl Acad Sci U S A. 1996;93:12355-12358.
60. Pevny L, Lin CS, D'Agati V, Simon MC, Orkin SH, Costantini F. Development of hematopoietic cells lacking transcription factor GATA-1. Development. 1995;121:163-172.
61. Pevny L, Simon MC, Robertson E, et al. Erythroid differentiation in chimaeric mice blocked by a targeted mutation in the gene for transcription factor GATA-1. Nature. 1991;349:257-260.
62. Weiss MJ, Keller G, Orkin SH. Novel insights into erythroid development revealed through in vitro differentiation of GATA-1 embryonic stem cells. Genes Dev. 1994;8:1184-1197.
63. Weiss MJ, Orkin SH. Transcription factor GATA-1 permits survival and maturation of erythroid precursors by preventing apoptosis. Proc Natl Acad Sci U S A. 1995;92:9623-9627.
64. Whyatt D, Lindeboom F, Karis A, et al. An intrinsic but cell-nonautonomous defect in GATA-1-overexpressing mouse erythroid cells. Nature. 2000;406:519-524.
65. Whyatt DJ, Karis A, Harkes IC, et al. The level of the tissue-specific factor GATA-1 affects the cellcycle machinery. Genes Funct. 1997;1:11-24.
66. Kurtz A, Hartl W, Jelkmann W, Zapf J, Bauer C. Activity in fetal bovine serum that stimulates erythroid colony formation in fetal mouse livers is insulinlike growth factor I. J Clin Invest. 1985;76: 1643-1648.
67. Porter P, Ogawa M. Erythroid burst promoting activity (BPA). In: Dunn CDR, ed. Current Concepts in Erythropoiesis. New York: Wiley;1983: 81.
68. Sawada K, Krantz SB, Dessypris EN, Koury ST, Sawyer ST. Human colony-forming unitserythroid do not require accessory cells, but do require direct interaction with insulin-like growth factor I and/or insulin for erythroid development.
69. J Clin Invest. 1989;83:1701-1709.
70. Rich IN, Vogt C, Pentz S. Erythropoietin gene expression in vitro and in vivo detected by in situ hybridization. Blood Cells. 1988;14:505-520.
71. Angelillo-Scherrer A, Burnier L, Lambrechts D, et al. Role of Gas6 in erythropoiesis and anemia in mice. J Clin Invest. 2008;118:583-596.
72. Tordjman R, Delaire S, Plouet J, et al. Erythroblasts are a source of angiogenic factors. Blood. 2001;97:1968-1974.
73. Means RT. Hepcidin and cytokines in anaemia. Hematology. 2004;9:357-362.
74. Dai C, Chung IJ, Jiang S, Price JO, Krantz SB. Reduction of cell cycle progression in human erythroid progenitor cells treated with tumour necrosis factor alpha occurs with reduced CDK6 and is partially reversed by CDK6 transduction. Br J Haematol. 2003;121:919-927.
75. Flores-Figueroa E, Gutierrez-Espindola G, Montesinos JJ, Arana-Trejo RM, Mayani H. In vitro characterization of hematopoietic microenvironment cells from patients with myelodysplastic syndrome. Leuk Res. 2002;26:677-686.
76. Zermati Y, Fichelson S, Valensi F, et al. Transforming growth factor inhibits erythropoiesis by blocking proliferation and accelerating differentiation of erythroid progenitors. Exp Hematol. 2000; 28:885-894.
77. Maddala R, Reddy VN, Epstein DL, Rao V. Growth factor induced activation of Rho and Rac GTPases and actin cytoskeletal reorganization in human lens epithelial cells. Mol Vis. 2003;9:329-336.
78. Zamai L, Secchiero P, Pierpaoli S, et al. TNFrelated apoptosis-inducing ligand (TRAIL) as a negative regulator of normal human erythropoiesis. Blood. 2000;95:3716-3724.
79. Secchiero P, Melloni E, Heikinheimo M, et al. TRAIL regulates normal erythroid maturation through an ERK-dependent pathway. Blood. 2004;103:517-522.
80. Nemeth E, Ganz T. Regulation of iron metabolism by hepcidin. Annu Rev Nutr. 2006;26:323-342.
81. Matsushima T, Nakashima M, Oshima K, et al. Receptor binding cancer antigen expressed on SiSo cells, a novel regulator of apoptosis of erythroid progenitor cells. Blood. 2001;98:313-321.
82. Hanspal M. Importance of cell-cell interactions in regulation of erythropoiesis. Curr Opin Hematol. 1997;4:142-147.
83. Rosemblatt M, Vuilett-Gaugler MH, Leroy C, Coulombel L. Coexpression of two fibronectin receptors, VLA-4 and VLA-5 by immature human erythroblastic precursor cells. J Clin Invest. 1991; 87:6-11.
84. Humphries MJ, Akiyama SK, Komoriya A, Olden K, Yamada KM. Identification of an alternatively spliced site in human plasma fibronectin that mediates cell type-specific adhesion. J Cell Biol. 1986;103:2637-2647.
85. Humphries SE, Cook M, Dubowitz M, Stirling Y, Meade TW. Role of genetic variation at the fibrinogen locus in determination of plasma fibrinogen concentrations. Lancet. 1987;1:1452-1455.
86. Mould AP, Komoriya A, Yamada KM, Humphries MJ. The CS5 peptide is a second site in the IIICS region of fibronectin recognized by the integrin alpha 4 beta 1. Inhibition of alpha 4 beta 1 function by RGD peptide homologues. J Biol Chem. 1991;266:3579-3585.
87. Mould AP, Humphries MJ. Identification of a novel recognition sequence for the integrin alpha 4 beta 1 in the COOH-terminal heparin-binding domain of fibronectin. EMBO J. 1991;10:4089-4095.
88. Vuillett-Gaugler MH, Breton-Gorius Vainchenker W, Guichard J, Leroy C, Tchernia G, Coulombel L. Loss of attachement to fibronectin with terminal erythroid differentiation. Blood. 1990;75:865-873.
89. Patel VP, Lodish HF. A fibronectin matrix is required for differentiation of murine erythroleukemia cells into reticulocytes. J Cell Biol. 1987;105: 3105-3118.
90. Eshghi S, Vogelezang MG, Hynes RO, Griffith LG, Lodish HF. Alpha4beta1 integrin and erythropoietin mediate temporally distinct steps in erythropoiesis: integrins in red cell development. J Cell Biol. 2007;177:871-880.
91. Zen Q, Cottman M, Truskey G, Fraser R, Telen M. Critical factors in basal cell adhesion molecule/lutheran-mediated adhesion to laminin. J Biol Chem. 1999;274:728-734.
92. Udani M, Zen Q, Cottman M, et al. Basal cell adhesion molecule/lutheran protein: The receptor critical for sickle cell adhesion to laminin. J Clin Invest. 1998;101:2550-2558.
93. El Nemer W, Gane P, Colin Y, et al. The lutheran blood group glycoproteins, the erythroid receptors for laminin, are adhesion molecules. J Biol Chem. 1998;273:16686-16693.
94. Rahuel C, Le Van Kim C, Mattei MG, Cartron JP, Colin Y. A unique gene encodes spliceoforms of the basal cell adhesion molecule cell surface glycoprotein of epithelial cancer and of the lutheran blood group glycoprotein. Blood. 1996;88:1865-1872.
95. Parsons SF, Mallison G, Daniels GL, Green CA, Smythe JS, Anstee DJ. Use of domain-deletion mutants to locate Lutheran blood group antigens to each of the five immunoglobulin superfamily domains of the Lutheran glycoprotein: elucidation of the molecular basis of the Lua/Lub and the Aua/Aub polymorphisms. Blood. 1997;89:4219-4225.
96. Parsons SF, Mallinson G, Holmes CH, et al. The Lutheran blood group glycoprotein, a new member of the immunoglobulin superfamily, is widely expressed in human tissues and is developmentally regulated in human liver. Proc Natl Acad Sci U S A. 1995;92:5496-5500.
97. Parsons SF, Lee G, Spring FA, et al. Lutheran blood group glycoprotein and its newly characterized mouse homologue specifically bind alpha5 chain-containing human laminin with high affinity. Blood. 2001;97:312-320.
98. Mankelow TJ, Burton N, Stefansdottir FO, et al. The Laminin 511/521-binding site on the Lutheran blood group glycoprotein is located at the flexible junction of Ig domains 2 and 3. Blood. 2007;110:3398-3406.
99. Gu Y, Sorokin L, Durbeej M, Hjalt T, Jonsson JI, Ekblom M. Characterization of bone marrow laminins and identification of alpha5-containing laminins as adhesive proteins for multipotent hematopoietic FDCP-Mix cells. Blood. 1999;93:2533-2542.