Isolation and functional characterization of human erythroblasts at distinct stages: implications for understanding of normal and disordered erythropoiesis in vivo

Blood

Volumn 121, Issue 16, 2013, Pages 3246-3253

  Hu, Jingping ^a,b   Liu, Jing ^a,b   Xue, Fumin ^a   Halverson, Gregory ^a   Reid, Marion ^a   Guo, Anqi ^a   Chen, Lixiang ^a   Raza, Azra ^c   Galili, Naomi ^c   Jaffray, Julie ^d   Lane, Joseph ^e   Chasis, Joel Anne ^a   Taylor, Naomi ^f   Mohandas, Narla ^a   An, Xiuli ^a,g  

^a NEW YORK BLOOD CENTER   (United States)

^b CENTRAL SOUTH UNIVERSITY   (China)

^c NewYork Presbyterian Hospital   (United States)

^d MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^e New York Presbyterian Veterans Administration   (United States)

^f CNRS   (France)

^g ZHENGZHOU UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA4 INTEGRIN; ERYTHROCYTE BAND 3 PROTEIN; CD34 ANTIGEN; CYTOSKELETON PROTEIN; MEMBRANE PROTEIN;

ARTICLE; CELL DIFFERENTIATION; CELL FUNCTION; CELL ISOLATION; CELL POPULATION; CONTROLLED STUDY; DEVELOPMENTAL STAGE; ERYTHROBLAST; ERYTHROID CELL; ERYTHROPOIESIS; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MITOSIS; MYELODYSPLASTIC SYNDROME; PRIORITY JOURNAL; BONE MARROW CELL; CELL CULTURE; CELL SEPARATION; CYTOLOGY; FLOW CYTOMETRY; IMMUNOBLOTTING; METHODOLOGY; PATHOLOGY;

ANION EXCHANGE PROTEIN 1, ERYTHROCYTE; ANTIGENS, CD34; BONE MARROW CELLS; CELL SEPARATION; CELLS, CULTURED; CYTOSKELETAL PROTEINS; ERYTHROBLASTS; ERYTHROPOIESIS; FLOW CYTOMETRY; HUMANS; IMMUNOBLOTTING; INTEGRIN ALPHA4; MEMBRANE PROTEINS; MITOSIS; MYELODYSPLASTIC SYNDROMES;

MLCS; MLOWN;

EID: 84879142151     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2013-01-476390     Document Type: Article

References (35)

1. Stephenson JR, Axelrad AA, McLeod DL, Shreeve MM. Induction of colonies of hemoglobin-synthesizing cells by erythropoietin in vitro. Proc Natl Acad Sci USA. 1971;68(7):1542-1546.
2. Chang H, Langer PJ, Lodish HF. Asynchronous synthesis of erythrocyte membrane proteins. Proc Natl Acad Sci USA. 1976;73(9):3206-3210.
3. Blikstad I, Nelson WJ, Moon RT, Lazarides E. Synthesis and assembly of spectrin during avian erythropoiesis: stoichiometric assembly but unequal synthesis of alpha and beta spectrin. Cell. 1983;32(4):1081-1091.
4. Hanspal M, Hanspal JS, Kalraiya R, Liu SC, Sahr KE, Howard D, Palek J. Asynchronous synthesis of membrane skeletal proteins during terminal maturation of murine erythroblasts. Blood. 1992; 80(2):530-539.
5. Peters LL, White RA, Birkenmeier CS, Bloom ML, Lux SE, Barker JE. Changing patterns in cytoskeletal mRNA expression and protein synthesis during murine erythropoiesis in vivo. Proc Natl Acad Sci USA. 1992;89(13):5749-5753.
6. Chen K, Liu J, Heck S, Chasis JA, 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. 2009; 106(41):17413-17418.
7. Liu J, Mohandas N, An X. Membrane assembly during erythropoiesis. Curr Opin Hematol. 2011; 18(3):133-138.
8. Gronowicz G, Swift H, Steck TL. Maturation of the reticulocyte in vitro. J Cell Sci. 1984;71:177-197.
9. Zhang J, Randall MS, Loyd MR, Dorsey FC, Kundu M, Cleveland JL, Ney PA. Mitochondrial clearance is regulated by Atg7-dependent and -independent mechanisms during reticulocyte maturation. Blood. 2009;114(1):157-164.
10. Kundu M, Lindsten T, Yang CY, et al. Ulk1 plays a critical role in the autophagic clearance of mitochondria and ribosomes during reticulocyte maturation. Blood. 2008;112(4):1493-1502.
11. Waugh RE, McKenney JB, Bauserman RG, Brooks DM, Valeri CR, Snyder LM. Surface area and volume changes during maturation of reticulocytes in the circulation of the baboon. J Lab Clin Med. 1997;129(5):527-535.
12. Chasis JA, Prenant M, Leung A, Mohandas N. Membrane assembly and remodeling during reticulocyte maturation. Blood. 1989;74(3): 1112-1120.
13. Liu J, Guo X, Mohandas N, Chasis JA, An X. Membrane remodeling during reticulocyte maturation. Blood. 2010;115(10):2021-2027.
14. Liu Y, Pop R, Sadegh C, Brugnara C, Haase VH, Socolovsky M. Suppression of Fas-FasL coexpression by erythropoietin mediates erythroblast expansion during the erythropoietic stress response in vivo. Blood. 2006;108(1): 123-133.
15. Zhang J, Socolovsky M, Gross AW, Lodish HF. Role of Ras signaling in erythroid differentiation of mouse fetal liver cells: functional analysis by a flow cytometry-based novel culture system. Blood. 2003;102(12):3938-3946.
16. Flygare J, Rayon Estrada V, Shin C, Gupta S, Lodish HF. HIF1alpha synergizes with glucocorticoids to promote BFU-E progenitor self-renewal. Blood. 2011;117(12):3435-3444.
17. Salomao M, Zhang X, Yang Y, et al. Protein 4.1R-dependent multiprotein complex: new insights into the structural organization of the red blood cell membrane. Proc Natl Acad Sci USA. 2008; 105(23):8026-8031.
18. Satchwell TJ, Bell AJ, Pellegrin S, et al. Critical band 3 multiprotein complex interactions establish early during human erythropoiesis. Blood. 2011; 118(1):182-191.
19. Robinson J, Sieff C, Delia D, Edwards PA, Greaves M. Expression of cell-surface HLA-DR, HLA-ABC and glycophorin during erythroid differentiation. Nature. 1981;289(5793):68-71.
20. Loken MR, Shah VO, Dattilio KL, Civin CI. Flow cytometric analysis of human bone marrow: I. Normal erythroid development. Blood. 1987; 69(1):255-263.
21. Liu J, Zhang J, Ginzburg Y, et al. Quantitative analysis of murine terminal erythroid differentiation in vivo: novel method to study normal and disordered erythropoiesis [published online ahead of print January 3, 2013]. Blood. doi:10.1182/blood-2012-09-456079.
22. Stohlman F Jr, Ebbe S, Morse B, Howard D, Donovan J. Regulation of erythropoiesis. XX. Kinetics of red cell production. Ann N Y Acad Sci. 1968;149(1):156-172.
23. Nimer SD. Myelodysplastic syndromes. Blood. 2008;111(10):4841-4851.
24. Southcott MJ, Tanner MJ, Anstee DJ. The expression of human blood group antigens during erythropoiesis in a cell culture system. Blood. 1999;93(12):4425-4435.
25. Kodippili GC, Spector J, Kang GE, Liu H, Wickrema A, Ritchie K, Low PS. Analysis of the kinetics of band 3 diffusion in human erythroblasts during assembly of the erythrocyte membrane skeleton. Br J Haematol. 2010;150(5):592-600.
26. Giarratana MC, Rouard H, Dumont A, et al. Proof of principle for transfusion of in vitro-generated red blood cells. Blood. 2011;118(19):5071-5079.
27. Mathias LA, Fisher TC, Zeng L, Meiselman HJ, Weinberg KI, Hiti AL, Malik P. Ineffective erythropoiesis in beta-thalassemia major is due to apoptosis at the polychromatophilic normoblast stage. Exp Hematol. 2000;28(12):1343-1353.
28. Claessens YE, Bouscary D, Dupont JM, et al. In vitro proliferation and differentiation of erythroid progenitors from patients with myelodysplastic syndromes: evidence for Fas-dependent apoptosis. Blood. 2002;99(5):1594-1601.
29. Awandare GA, Kempaiah P, Ochiel DO, Piazza P, Keller CC, Perkins DJ. Mechanisms of erythropoiesis inhibition by malarial pigment and malaria-induced proinflammatory mediators in an in vitro model. Am J Hematol. 2011;86(2): 155-162.
30. Narla A, Dutt S, McAuley JR, et al. Dexamethasone and lenalidomide have distinct functional effects on erythropoiesis. Blood. 2011; 118(8):2296-2304.
31. Ji P, Jayapal SR, Lodish HF. Enucleation of cultured mouse fetal erythroblasts requires Rac GTPases and mDia2. Nat Cell Biol. 2008;10(3): 314-321.
32. Keerthivasan G, Small S, Liu H, Wickrema A, Crispino JD. Vesicle trafficking plays a novel role in erythroblast enucleation. Blood. 2010;116(17): 3331-3340.
33. Ubukawa K, Guo YM, Takahashi M, et al. Enucleation of human erythroblasts involves non-muscle myosin IIB. Blood. 2012;119(4): 1036-1044.
34. Konstantinidis DG, Pushkaran S, Johnson JF, et al. Signaling and cytoskeletal requirements in erythroblast enucleation. Blood. 2012;119(25): 6118-6127.
35. Vardiman JW, Harris NL, Brunning RD. The World Health Organization (WHO) classification of the myeloid neoplasms. Blood. 2002;100(7): 2292-2302.