Tracking erythroid progenitor cells in times of need and times of plenty

Experimental Hematology

Volumn 44, Issue 8, 2016, Pages 653-663

  Koury, Mark J ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONTINUOUS ERYTHROPOIESIS RECEPTOR ACTIVATOR; ELTROMBOPAG; ERYTHROPOIETIN; LUSPATERCEPT; NOVEL ERYTHROPOIESIS STIMULATING PROTEIN; PEGINESATIDE; RECOMBINANT ERYTHROPOIETIN; SOTATERCEPT;

ANEMIA; APOPTOSIS; BURST FORMING UNIT E; CELL DIFFERENTIATION; CELL MOTILITY; CELL POPULATION; CELL PROLIFERATION; CELL SURVIVAL; CELL TRACKING; COLONY FORMING UNIT E; ERYTHROBLAST; ERYTHROBLASTIC ISLAND; ERYTHROID PRECURSOR CELL; ERYTHROPOIESIS; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; STEM CELL EXPANSION; STEM CELL SELF-RENEWAL; ANIMAL; CELL MOTION; CELL SELF-RENEWAL; CYTOLOGY; DRUG EFFECTS; GENETICS; METABOLISM;

ANEMIA; ANIMALS; APOPTOSIS; CELL DIFFERENTIATION; CELL MOVEMENT; CELL PROLIFERATION; CELL SELF RENEWAL; CELL SURVIVAL; ERYTHROID PRECURSOR CELLS; ERYTHROPOIESIS; HUMANS;

EID: 84989771021     PISSN: 0301472X     EISSN: 18732399     Source Type: Journal    
DOI: 10.1016/j.exphem.2015.10.007     Document Type: Review

References (88)

1. 1 Hara, H., Ogawa, M., Erythropoietic precursors in mice under erythropoietic stimulation and suppression. Exp Hematol 5 (1977), 141–148.
2. 2 Stephenson, J.R., Axelrad, A.A., McLeod, D.L., Shreeve, M.M., Induction of colonies of hemoglobin-synthesizing cells by erythropoietin in vitro. Proc Natl Acad Sci USA 68 (1971), 1542–1546.
3. 3 Axelrad, A., McLeod, D., Shreeve, M., Heath, D., Properties of Cells that Produce Erythropoietic Colonies In Vitro. Robinson, W., (eds.) Hemopoiesis in Culture, 1974, U.S. Government Printing Office, Bethesda, MD, 226–237.
4. 4 Eaves, C.J., Humphries, R.K., Eaves, A.C., In Vitro Characterization of Erythroid Precursor Cells and Erythropoietic Differentiation. Stamatoyannopoulos, G., Nienhuis, A.W., (eds.) Cellular and Molecular Regulation of Hemogolobin Switching, 1979, Grune and Stratton, New York, 251–273.
5. 5 McLeod, D.L., Shreeve, M.M., Axelrad, A.A., Chromosome marker evidence for the bipotentiality of BFU-E. Blood 56 (1980), 318–322.
6. 6 Vannucchi, A.M., Paoletti, F., Linari, S., et al. Identification and characterization of a bipotent (erythroid and megakaryocytic) cell precursor from the spleen of phenylhydrazine-treated mice. Blood 95 (2000), 2559–2568.
7. 7 Goldfarb, A.N., Wong, D., Racke, F.K., Induction of megakaryocytic differentiation in primary human erythroblasts: a physiological basis for leukemic lineage plasticity. Am J Pathol 158 (2001), 1191–1198.
8. 8 Mancini, E., Sanjuan-Pla, A., Luciani, L., et al. FOG-1 and GATA-1 act sequentially to specify definitive megakaryocytic and erythroid progenitors. EMBO J 31 (2012), 351–365.
9. 9 Siatecka, M., Bieker, J.J., The multifunctional role of EKLF/KLF1 during erythropoiesis. Blood 118 (2011), 2044–2054.
10. 10 Bianchi, E., Zini, R., Salati, S., et al. c-myb supports erythropoiesis through the transactivation of KLF1 and LMO2 expression. Blood 116 (2010), e99–e110.
11. 11 Bianchi, E., Bulgarelli, J., Ruberti, S., et al. MYB controls erythroid versus megakaryocyte lineage fate decision through the miR-486-3p-mediated downregulation of MAF. Cell Death Differ 22 (2015), 1906–1921.
12. 12 Socolovsky, M., Nam, H., Fleming, M.D., Haase, V.H., Brugnara, C., Lodish, H.F., Ineffective erythropoiesis in Stat5a(−/−)5b(−/−) mice due to decreased survival of early erythroblasts. Blood 98 (2001), 3261–3273.
13. 13 Chen, K., Liu, J., Heck, S., Chasis, J.A., An, X., Mohandas, N., Resolving the distinct stages in erythroid differentiation based on dynamic changes in membrane protein expression during erythropoiesis. Proc Natl Acad Sci USA 106 (2009), 17413–17418.
14. 14 Hu, J., Liu, J., Xue, F., et al. Isolation and functional characterization of human erythroblasts at distinct stages: implications for understanding of normal and disordered erythropoiesis in vivo. Blood 121 (2013), 3246–3253.
15. 15 Erslev, A., Hematology: control of red cell production. Annu Rev Med 11 (1960), 315–332.
16. 16 Cheshier, S.H., Prohaska, S.S., Weissman, I.L., The effect of bleeding on hematopoietic stem cell cycling and self-renewal. Stem Cells Dev 16 (2007), 707–717.
17. 17 Grover, A., Mancini, E., Moore, S., et al. Erythropoietin guides multipotent hematopoietic progenitor cells toward an erythroid fate. J Exp Med 211 (2014), 181–188.
18. 18 Koury, M.J., Erythropoietin: the story of hypoxia and a finely regulated hematopoietic hormone. Exp Hematol 33 (2005), 1263–1270.
19. 19 Papayannopoulou, T., Finch, C.A., On the in vivo action of erythropoietin: a quantitative analysis. J Clin Invest 51 (1972), 1179–1185.
20. 20 Gregory, C.J., Tepperman, A.D., McCulloch, E.A., Till, J.E., Erythropoietic progenitors capable of colony formation in culture: response of normal and genetically anemic W-W-V mice to manipulations of the erythron. J Cell Physiol 84 (1974), 1–12.
21. 21 Iscove, N.N., The role of erythropoietin in regulation of population size and cell cycling of early and late erythroid precursors in mouse bone marrow. Cell Tissue Kinet 10 (1977), 323–334.
22. 22 Pannacciulli, I.M., Massa, G.G., Saviane, A.G., Ghio, R.L., Bianchi, G.L., Bogliolo, G.V., Effect of bleeding on in vivo in vitro colony-forming hemopoietic cells. Acta Haematol 58 (1977), 27–33.
23. 23 Peschle, C., Magli, M.C., Cillo, C., et al. Kinetics of erythroid and myeloid stem cells in post-hypoxia polycythaemia. Br J Haematol 37 (1977), 345–352.
24. 24 Hara, H., Ogawa, M., Erthropoietic precursors in mice with phenylhydrazine-induced anemia. Am J Hematol 1 (1976), 453–458.
25. 25 Miyake, T., Kung, C.K., Goldwasser, E., Purification of human erythropoietin. J Biol Chem 252 (1977), 5558–5564.
26. 26 Ogawa, M., Grush, O.C., O'Dell, R.F., Hara, H., MacEachern, M.D., Circulating erythropoietic precursors assessed in culture: characterization in normal men and patients with hemoglobinopathies. Blood 50 (1977), 1081–1092.
27. 27 Clarke, B.J., Housman, D., Characterization of an erythroid precursor cell of high proliferative capacity in normal human peripheral blood. Proc Natl Acad Sci USA 74 (1977), 1105–1109.
28. 28 Bonig, H., Chang, K.H., Nakamoto, B., Papayannopoulou, T., The p67 laminin receptor identifies human erythroid progenitor and precursor cells and is functionally important for their bone marrow lodgment. Blood 108 (2006), 1230–1233.
29. 29 Broudy, V.C., Lin, N.L., Priestley, G.V., Nocka, K., Wolf, N.S., Interaction of stem cell factor and its receptor c-kit mediates lodgment and acute expansion of hematopoietic cells in the murine spleen. Blood 88 (1996), 75–81.
30. 30 Munugalavadla, V., Kapur, R., Role of c-Kit and erythropoietin receptor in erythropoiesis. Crit Rev Oncol Hematol 54 (2005), 63–75.
31. 31 Ulyanova, T., Jiang, Y., Padilla, S., Nakamoto, B., Papayannopoulou, T., Combinatorial and distinct roles of alpha(5) and alpha(4) integrins in stress erythropoiesis in mice. Blood 117 (2011), 975–985.
32. 32 Gregory, C.J., Eaves, A.C., Three stages of erythropoietic progenitor cell differentiation distinguished by a number of physical and biologic properties. Blood 51 (1978), 527–537.
33. 33 Dai, C.H., Krantz, S.B., Zsebo, K.M., Human burst-forming units-erythroid need direct interaction with stem cell factor for further development. Blood 78 (1991), 2493–2497.
34. 34 Paulson, R.F., Shi, L., Wu, D.C., Stress erythropoiesis: new signals and new stress progenitor cells. Curr Opin Hematol 18 (2011), 139–145.
35. 35 Xiang, J., Wu, D.C., Chen, Y., Paulson, R.F., In vitro culture of stress erythroid progenitors identifies distinct progenitor populations and analogous human progenitors. Blood 125 (2015), 1803–1812.
36. 36 Zhang, L., Prak, L., Rayon-Estrada, V., et al. ZFP36L2 is required for self-renewal of early burst-forming unit erythroid progenitors. Nature 499 (2013), 92–96.
37. 37 Narla, A., Dutt, S., McAuley, J.R., et al. Dexamethasone and lenalidomide have distinct functional effects on erythropoiesis. Blood 118 (2011), 2296–2304.
38. 38 Lee, H.Y., Gao, X., Barrasa, M.I., et al. PPAR-alpha and glucocorticoid receptor synergize to promote erythroid progenitor self-renewal. Nature 522 (2015), 474–477.
39. 39 Chasis, J.A., Mohandas, N., Erythroblastic islands: niches for erythropoiesis. Blood 112 (2008), 470–478.
40. 40 Manwani, D., Bieker, J.J., The erythroblastic island. Curr Top Dev Biol 82 (2008), 23–53.
41. 41 Sadahira, Y., Mori, M., Role of the macrophage in erythropoiesis. Pathol Int 49 (1999), 841–848.
42. 42 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 68 (2000), 464–470.
43. 43 Chow, A., Huggins, M., Ahmed, J., et al. CD169(+) macrophages provide a niche promoting erythropoiesis under homeostasis and stress. Nat Med 19 (2013), 429–436.
44. 44 Ramos, P., Casu, C., Gardenghi, S., et al. Macrophages support pathological erythropoiesis in polycythemia vera and beta-thalassemia. Nat Med 19 (2013), 437–445.
45. 45 Mohandas, N., Prenant, M., Three-dimensional model of bone marrow. Blood 51 (1978), 633–643.
46. 46 Spike, B.T., Dibling, B.C., Macleod, K.F., Hypoxic stress underlies defects in erythroblast islands in the Rb-null mouse. Blood 110 (2007), 2173–2181.
47. 47 Rhodes, M.M., Kopsombut, P., Bondurant, M.C., Price, J.O., Koury, M.J., Adherence to macrophages in erythroblastic islands enhances erythroblast proliferation and increases erythrocyte production by a different mechanism than erythropoietin. Blood 111 (2008), 1700–1708.
48. 48 Haldar, M., Kohyama, M., So, A.Y., et al. Heme-mediated SPI-C induction promotes monocyte differentiation into iron-recycling macrophages. Cell 156 (2014), 1223–1234.
49. 49 Koury, M.J., Bondurant, M.C., Maintenance by erythropoietin of viability and maturation of murine erythroid precursor cells. J Cell Physiol 137 (1988), 65–74.
50. 50 Koury, M.J., Bondurant, M.C., Erythropoietin retards DNA breakdown and prevents programmed death in erythroid progenitor cells. Science 248 (1990), 378–381.
51. 51 Wu, H., Liu, X., Jaenisch, R., Lodish, H.F., Generation of committed erythroid BFU-E and CFU-E progenitors does not require erythropoietin or the erythropoietin receptor. Cell 83 (1995), 59–67.
52. 52 Wickrema, A., Bondurant, M.C., Krantz, S.B., Abundance and stability of erythropoietin receptor mRNA in mouse erythroid progenitor cells. Blood 78 (1991), 2269–2275.
53. 53 Broudy, V.C., Lin, N., Brice, M., Nakamoto, B., Papayannopoulou, T., Erythropoietin receptor characteristics on primary human erythroid cells. Blood 77 (1991), 2583–2590.
54. 54 Wickrema, A., Krantz, S.B., Winkelmann, J.C., Bondurant, M.C., Differentiation and erythropoietin receptor gene expression in human erythroid progenitor cells. Blood 80 (1992), 1940–1949.
55. 55 Kelley, L.L., Koury, M.J., Bondurant, M.C., Koury, S.T., Sawyer, S.T., Wickrema, A., Survival or death of individual proerythroblasts results from differing erythropoietin sensitivities: a mechanism for controlled rates of erythrocyte production. Blood 82 (1993), 2340–2352.
56. 56 De Maria, R., Testa, U., Luchetti, L., et al. Apoptotic role of Fas/Fas ligand system in the regulation of erythropoiesis. Blood 93 (1999), 796–803.
57. 57 Liu, Y., Pop, R., Sadegh, C., Brugnara, C., Haase, V.H., Socolovsky, M., Suppression of Fas-FasL coexpression by erythropoietin mediates erythroblast expansion during the erythropoietic stress response in vivo. Blood 108 (2006), 123–133.
58. 58 Koulnis, M., Liu, Y., Hallstrom, K., Socolovsky, M., Negative autoregulation by Fas stabilizes adult erythropoiesis and accelerates its stress response. PLoS One, 6, 2011, e21192.
59. 59 Eymard, N., Bessonov, N., Gandrillon, O., Koury, M.J., Volpert, V., The role of spatial organization of cells in erythropoiesis. J Math Biol 70 (2015), 71–97.
60. 60 Angelillo-Scherrer, A., Burnier, L., Lambrechts, D., et al. Role of Gas6 in erythropoiesis and anemia in mice. J Clin Invest 118 (2008), 583–596.
61. 61 Tang, H., Chen, S., Wang, H., Wu, H., Lu, Q., Han, D., TAM receptors and the regulation of erythropoiesis in mice. Haematologica 94 (2009), 326–334.
62. 62 Muta, K., Krantz, S.B., Bondurant, M.C., Wickrema, A., Distinct roles of erythropoietin, insulin-like growth factor I, and stem cell factor in the development of erythroid progenitor cells. J Clin Invest 94 (1994), 34–43.
63. 63 Muta, K., Krantz, S.B., Bondurant, M.C., Dai, C.H., Stem cell factor retards differentiation of normal human erythroid progenitor cells while stimulating proliferation. Blood 86 (1995), 572–580.
64. 64 Panzenbock, B., Bartunek, P., Mapara, M.Y., Zenke, M., Growth and differentiation of human stem cell factor/erythropoietin-dependent erythroid progenitor cells in vitro. Blood 92 (1998), 3658–3668.
65. 65 Von Lindern, M., Zauner, W., Mellitzer, G., et al. The glucocorticoid receptor cooperates with the erythropoietin receptor and c-Kit to enhance and sustain proliferation of erythroid progenitors in vitro. Blood 94 (1999), 550–559.
66. 66 Stellacci, E., Di Noia, A., Di Baldassarre, A., Migliaccio, G., Battistini, A., Migliaccio, A.R., Interaction between the glucocorticoid and erythropoietin receptors in human erythroid cells. Exp Hematol 37 (2009), 559–572.
67. 67 Bauer, A., Tronche, F., Wessely, O., et al. The glucocorticoid receptor is required for stress erythropoiesis. Genes Dev 13 (1999), 2996–3002.
68. 68 Rubiolo, C., Piazzolla, D., Meissl, K., et al. A balance between Raf-1 and Fas expression sets the pace of erythroid differentiation. Blood 108 (2006), 152–159.
69. 69 Falchi, M., Varricchio, L., Martelli, F., et al. Dexamethasone targeted directly to macrophages induces macrophage niches that promote erythroid expansion. Haematologica 100 (2015), 178–187.
70. 70 Millot, S., Andrieu, V., Letteron, P., et al. Erythropoietin stimulates spleen BMP4-dependent stress erythropoiesis and partially corrects anemia in a mouse model of generalized inflammation. Blood 116 (2010), 6072–6081.
71. 71 Rhodes, M.M., Kopsombut, P., Bondurant, M.C., Price, J.O., Koury, M.J., Bcl-x(L) prevents apoptosis of late-stage erythroblasts but does not mediate the antiapoptotic effect of erythropoietin. Blood 106 (2005), 1857–1863.
72. 72 Koulnis, M., Porpiglia, E., Porpiglia, P.A., et al. Contrasting dynamic responses in vivo of the Bcl-xL and Bim erythropoietic survival pathways. Blood 119 (2012), 1228–1239.
73. 73 Suragani, R.N., Cadena, S.M., Cawley, S.M., et al. Transforming growth factor-beta superfamily ligand trap ACE-536 corrects anemia by promoting late-stage erythropoiesis. Nat Med 20 (2014), 408–414.
74. 74 Erslev, A.J., Erythropoietin. N Engl J Med 324 (1991), 1339–1344.
75. 75 Koury, M.J., Sugar coating extends half-lives and improves effectiveness of cytokine hormones. Trends Biotechnol 21 (2003), 462–464.
76. 76 Locatelli, F., Reigner, B., C.E.R.A.: pharmacodynamics, pharmacokinetics and efficacy in patients with chronic kidney disease. Expert Opin Investig Drugs 16 (2007), 1649–1661.
77. 77 Horl, W.H., Anaemia management and mortality risk in chronic kidney disease. Nat Rev Nephrol 9 (2013), 291–301.
78. 78 Hedley, B.D., Allan, A.L., Xenocostas, A., The role of erythropoietin and erythropoiesis-stimulating agents in tumor progression. Clin Cancer Res 17 (2011), 6373–6380.
79. 79 Macdougall, I.C., Rossert, J., Casadevall, N., et al. A peptide-based erythropoietin-receptor agonist for pure red-cell aplasia. N Engl J Med 361 (2009), 1848–1855.
80. 80 Desmond, R., Townsley, D.M., Dumitriu, B., et al. Eltrombopag restores trilineage hematopoiesis in refractory severe aplastic anemia that can be sustained on discontinuation of drug. Blood 123 (2014), 1818–1825.
81. 81 Vlachos, A., Ball, S., Dahl, N., et al. Diagnosing and treating Diamond Blackfan anaemia: results of an international clinical consensus conference. Br J Haematol 142 (2008), 859–876.
82. 82 Horos, R., von Lindern, M., Molecular mechanisms of pathology and treatment in diamond blackfan anaemia. Br J Haematol 159 (2012), 514–527.
83. 83 Varricchio, L., Migliaccio, A.R., The role of glucocorticoid receptor (GR) polymorphisms in human erythropoiesis. Am J Blood Res 4 (2014), 53–72.
84. 84 Koury, M.J., Haase, V.H., Anaemia in kidney disease: harnessing hypoxia responses for therapy. Nat Rev Nephrol 11 (2015), 394–410.
85. 85 Besarab, A., Provenzano, R., Hertel, J., et al. Randomized placebo-controlled dose-ranging and pharmacodynamics study of roxadustat (FG-4592) to treat anemia in nondialysis-dependent chronic kidney disease (NDD-CKD) patients. Nephrol Dial Transplant 30 (2015), 1665–1673.
86. 86 Ruckle, J., Jacobs, M., Kramer, W., et al. Single-dose, randomized, double-blind, placebo-controlled study of ACE-011 (ActRIIA-IgG1) in postmenopausal women. J Bone Miner Res 24 (2009), 744–752.
87. 87 Attie, K.M., Allison, M.J., McClure, T., et al. A phase 1 study of ACE-536, a regulator of erythroid differentiation, in healthy volunteers. Am J Hematol 89 (2014), 766–770.
88. 88 Dussiot, M., Maciel, T.T., Fricot, A., et al. An activin receptor IIA ligand trap corrects ineffective erythropoiesis in beta-thalassemia. Nat Med 20 (2014), 398–407.