Normal and disordered reticulocyte maturation

Current Opinion in Hematology

Volumn 18, Issue 3, 2011, Pages 152-157

  Ney, Paul A ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

autophagy; enucleation; exosomes; mitochondria; vesicles

Indexed keywords

OUTER MEMBRANE PROTEIN;

ARTICLE; AUTOPHAGY; CELL MATURATION; CELL MIGRATION; DEGRADATION; ENUCLEATION; ERYTHROID CELL; EXOCYTOSIS; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; RETICULOCYTE;

ANIMALS; AUTOPHAGY; ERYTHROPOIESIS; HUMANS; RETICULOCYTES;

EID: 79955030127     PISSN: 10656251     EISSN: 15317048     Source Type: Journal    
DOI: 10.1097/MOH.0b013e328345213e     Document Type: Article

References (81)

1. Gronowicz G, Swift H, Steck TL Maturation of the reticulocyte in vitro. J Cell Sci 1984; 71:177-197.
2. Noble NA, Xu QP, Ward JH. Reticulocytes. I: Isolation and in vitro maturation of synchronized populations. Blood 1989; 74:475-481. (Pubitemid 19187468)
3. Koury MJ, Koury ST, Kopsombut P, Bondurant MC. In vitro maturation of nascent reticulocytes to erythrocytes. Blood 2005; 105:2168-2174. (Pubitemid 40731809)
4. Wiczling P, Krzyzanski W. Flow cytometric assessment of homeostatic aging of reticulocytes in rats. Exp Hematol 2008; 36:119-127.
5. Jandl JH. Textbook of hematology. 2nd ed. New York: Little, Brown and Company; 1996.
6. McGrath KE, Kingsley PD, Koniski AD, et al. Enucleation of primitive erythroid cells generates a transient population of'pyrenocytes' in the mammalian fetus. Blood 2008; 111:2409-2417. (Pubitemid 351451454)
7. Koury ST, Koury MJ, Bondurant MC. Cytoskeletal distribution and function during the maturation and enucleation of mammalian erythroblasts. J Cell Biol 1989; 109:3005-3013. (Pubitemid 20011925)
8. Wickrema A, Koury ST, Dai CH, Krantz SB. Changes in cytoskeletal proteins and their mRNAs during maturation of human erythroid progenitor cells. J Cell Physiol 1994; 160:417-426. (Pubitemid 24288899)
9. Lee JC, Gimm JA, Lo AJ, et al. Mechanism of protein sorting during erythro-blast enucleation: role of cytoskeletal connectivity. Blood 2004; 103:1912-1919. (Pubitemid 38268991)
10. Salomao M, Chen K, Villalobos J, et al. Hereditary spherocytosis and heredi-tary elliptocytosis: aberrant protein sorting during erythroblast enucleation.Blood 2010; 116:267-269.
11. Popova EY, KraussSW, Short SA, et al. Chromatin condensation in terminally differentiating mouse erythroblasts does not involve special architectural proteins but depends on histone deacetylation. Chromosome Res 2009; 17:47-64.
12. Ji P, Yeh V, Ramirez T, et al. Histone deacetylase 2 is required for chromatin condensation and subsequent enucleation of cultured mouse fetal erythro blasts. Haematologica 2010; 95:2013-2021.
13. Zhang L, Flygare J, Wong P, et al. miR-191 regulates mouse erythroblast enucleation by down-regulating Riok3 and Mxi1. Genes Dev 2011; 25:119-124.
14. Spike BT, Dirlam A, Dibling BC, et al. The Rb tumor suppressor is required for stress erythropoiesis. EMBO J 2004; 23:4319-4329. (Pubitemid 39546169)
15. Coschi CH, Martens AL, Ritchie K, et al. Mitotic chromosome condensation mediated by the retinoblastoma protein is tumor-suppressive. Genes Dev 2010; 24:1351-1363.
16. Ngai J, Capetanaki YG, Lazarides E. Differentiation of murine erythroleukemia cells results in the rapid repression of vimentin gene expression. J Cell Biol 1984; 99:306-314. (Pubitemid 14096894)
17. KraussSW, Lo AJ, Short SA, et al. Nuclear substructure reorganization during late-stage erythropoiesis is selective and does not involve caspase cleavage of major nuclear substructural proteins. Blood 2005; 106:2200-2205. (Pubitemid 41291741)
18. Chasis JA, Prenant M, Leung A, Mohandas N. Membrane assembly and remodeling during reticulocyte maturation. Blood 1989; 74:1112-1120. (Pubitemid 19210032)
19. Ji P, Jayapal SR, Lodish HF. Enucleation of cultured mouse fetal erythroblasts requires Rac GTPases and mDia2. Nat Cell Biol 2008; 10:314-321. (Pubitemid 351331018)
20. Dumitriu B, Patrick MR, PetschekJP, et al. Sox6 cell-autonomously stimulates erythroid cell survival, proliferation, and terminal maturation and is thereby an important enhancer of definitive erythropoiesis during mouse development. Blood 2006; 108:1198-1207. (Pubitemid 44232015)
21. Keerthivasan G, Small S, Liu H, et al. Vesicle trafficking plays a novel role in erythroblast enucleation. Blood 2010; 116:3331-3340.
22. Gromley A, Yeaman C, Rosa J, et al. Centriolin anchoring of exocyst and SNARE complexes at the midbody is required forsecretory-vesicle-mediated abscission. Cell 2005; 123:75-87. (Pubitemid 41414530)
23. Mel HC, Prenant M, Mohandas N. Reticulocyte motility and form: studies on maturation and classification. Blood 1977; 49:1001-1009. (Pubitemid 8123867)
24. Waugh RE, McKenney JB, Bauserman RG, et al. Surface area and volume changes during maturation of reticulocytes in the circulation of the baboon. J Lab Clin Med 1997; 129:527-535. (Pubitemid 27285049)
25. Waugh RE, Mantalaris A, Bauserman RG, et al. Membrane instability in late-stage erythropoiesis. Blood 2001; 97:1869-1875. (Pubitemid 32217256)
26. Hentze MW, Muckenthaler MU, Galy B, Camaschella C. Two to tango: regulation of mammalian iron metabolism. Cell 2010; 142:24-38.
27. Lim JE, Jin O, Bennett C, et al. A mutation in Sec15l1 causes anemia in hemoglobin deficit (hbd) mice. Nat Genet 2005; 37:1270-1273. (Pubitemid 41568712)
28. White RA, Boydston LA, Brookshier TR, et al. Iron metabolism mutant hbd mice have a deletion in Sec15l1, which has homology to a yeast gene for vesicle docking. Genomics 2005; 86:668-673. (Pubitemid 41752947)
29. Zhang AS, Sheftel AD, Ponka P. The anemia of 'haemoglobin-deficit' (hbd/ hbd) mice is caused by a defect in transferrin cycling. Exp Hematol 2006; 34:593-598.
30. Garrick MD, Garrick LM. Loss of rapid transferrin receptor recycling due to a mutation in Sec15l1 in hbd mice. Biochim Biophys Acta 2007; 1773:105-108. (Pubitemid 46123615)
31. Harding C, Heuser J, Stahl P. Receptor-mediated endocytosis of transferrin and recycling of the transferrin receptor in rat reticulocytes. J Cell Biol 1983; 97:329-339.
32. Martin-Serrano J, Zang T, Bieniasz PD. Role of ESCRT-I in retroviral budding. J Virol 2003; 77:4794-4804. (Pubitemid 36402829)
33. Saksena S, Sun J, Chu T, Emr SD. ESCRTing proteins in the endocytic pathway. Trends Biochem Sci 2007; 32:561-573. (Pubitemid 350123053)
34. Trajkovic K, Hsu C, Chiantia S, et al. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 2008; 319:1244-1247. (Pubitemid 351323020)
35. Barres C, Blanc L, Bette-Bobillo P, et al. Galectin-5 is bound onto the surface of rat reticulocyte exosomes and modulates vesicle uptake by macrophages. Blood 2010; 115:696-705.
36. Geminard C, DeGA, Blanc L, Vidal M. Degradation of AP2 during reticulocyte maturation enhances binding of hsc70 and Alix to a common site on TFR for sorting into exosomes. Traffic 2004; 5:181-193. (Pubitemid 38379937)
37. Pan BT, Johnstone RM. Fate of the transferrin receptor during maturation of sheep reticulocytes in vitro: selective externalization of the receptor. Cell 1983; 33:967-978.
38. Johnstone RM, Adam M, Hammond JR, et al. Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J Biol Chem 1987; 262:9412-9420.
39. Raposo G, Nijman HW, Stoorvogel W, etal. B lymphocytes secrete antigen-presenting vesicles. J Exp Med 1996; 183:1161-1172. (Pubitemid 26113979)
40. Nguyen DG, Booth A, Gould SJ, Hildreth JE. Evidence that HIV budding in primary macrophages occurs through the exosome release pathway. J Biol Chem 2003; 278:52347-52354. (Pubitemid 38035824)
41. Fevrier B, Vilette D, Archer F, et al. Cells release prions in association with exosomes. Proc Natl Acad Sci USA 2004; 101:9683-9688. (Pubitemid 38869296)
42. Johnstone RM, Bianchini A, Teng K. Reticulocyte maturation and exosome release: transferrin receptor containing exosomes shows multiple plasma membrane functions. Blood 1989; 74:1844-1851. (Pubitemid 19251570)
43. Vidal M, Sainte-Marie J, Philippot JR, Bienvenue A. Asymmetric distribution of phospholipids in the membrane of vesicles released during in vitro maturation of guinea pig reticulocytes: evidence precluding a role for'aminophospholipid translocase'. J Cell Physiol 1989; 140:455-462. (Pubitemid 19241760)
44. Blanc L, Liu J, Vidal M, et al. The water channel aquaporin-1 partitions into exosomes during reticulocyte maturation: implication for the regulation of cell volume. Blood 2009; 114:3928-3934.
45. Blanc L, Vidal M. Reticulocyte membrane remodeling: contribution of the exosome pathway. Curr Opin Hematol 2010; 17:177-183.
46. Gasko O, Danon D. The metabolism of maturing reticulocytes. I. The existence of a functional tricarboxylic acid cycle. Br J Haematol 1972; 23:525-533.
47. Gasko O, Kanon D. The metabolism of maturing reticulocytes. II. Decline in activity of the tricarboxylic acid cycle associated with reticulocyte maturation. Br J Haematol 1972; 23:535-539.
48. Gasko O, Danon D. Deterioration and disappearance of mitochondria during reticulocyte maturation. Exp Cell Res 1972; 75:159-169.
49. Simpson CF, Kling JM. The mechanism of mitochondrial extrusion from phenylhydrazine-induced reticulocytes in the circulating blood. J Cell Biol 1968; 36:103-109.
50. Heynen MJ, Tricot G, Verwilghen RL Autophagy of mitochondria in rat bone marrow erythroid cells. Relation to nuclear extrusion. Cell Tissue Res 1985; 239:235-239.
51. Van Leyen K, Duvoisin RM, Engelhardt H, Wiedmann M. A function for lipoxygenase in programmed organelle degradation. Nature 1998; 395:392-395. (Pubitemid 28450690)
52. Grullich C, Duvoisin RM, Wiedmann M, van Leyen K. Inhibition of 15-lipoxygenase leads to delayed organelle degradation in the reticulocyte. FEBS Lett 2001; 489:51-54. (Pubitemid 32176004)
53. Zhang J, Ney PA. Mechanisms and biology of BNIP3 and NIX. Antioxid Redox Signal 2010 [Epub ahead of print].
54. Aerbajinai W, Giattina M, Lee YT, et al. The proapoptotic factor Nix is coexpressed with Bcl-xL during terminal erythroid differentiation. Blood 2003; 102:712-717. (Pubitemid 36841996)
55. -/- mice reveals a mechanism for apoptotic modulation of erythro-poiesis. Proc Natl Acad Sci USA 2007; 104:6794-6799. (Pubitemid 47175580)
56. Schweers RL, Zhang J, Randall MS, et al. NIX is required for programmed mitochondrial clearance during reticulocyte maturation. Proc Natl Acad Sci USA 2007; 104:19500-19505.
57. Sandoval H, Thiagarajan P, Dasgupta SK, et al. Essential role for Nix in autophagic maturation of erythroid cells. Nature 2008; 4:926-928.
58. Kitada T, Asakawa S, Hattori N, et al. Mutations in the Parkin gene cause autosomal recessive juvenile Parkinsonism. Nature 1998; 392: 605-608. (Pubitemid 28207717)
59. Deas E, Plun-Favreau H, Wood NW. PINK1 function in health and disease. EMBO Mol Med 2009; 1:152-165.
60. Narendra D, Tanaka A, Suen DF, Youle RJ. Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J Cell Biol 2008; 183:795-803.
61. Narendra DP, Jin SM, Tanaka A, et al. PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol 2010; 8:e1000298.
62. Geisler S, Holmstrom KM, Skujat D, etal. PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat Cell Biol 2010; 12:119-131.
63. Ding WX, Ni HM, Li M, etal. Nix is critical to two distinct phases of mitophagy, reactive oxygen species-mediated autophagy induction and Parkin-ubiqui-tin-p62-mediated mitochondrial priming. J Biol Chem 2010; 285:27879-27890.
64. Zhang J, Randall MS, Loyd MR, etal. Mitochondrial clearance is regulated by Atg7-dependent and -independent mechanisms during reticulocyte maturation. Blood 2009; 114:157-164.
65. Schwarten M, Mohrluder J, Ma P, et al. Nix directly binds to GABARAP: a possible crosstalk between apoptosis and autophagy. Autophagy 2009; 5:690-698.
66. Novak I, Kirkin V, McEwan DG, etal. Nix is a selective autophagy receptor for mitochondrial clearance. EMBO Rep 2010; 11:45-51.
67. Bellot G, Garcia-Medina R, Gounon P, et al. Hypoxia-induced autophagy is mediated through hypoxia-inducible factor induction of BNIP3 and BNIP3Lvia their BH3 domains. Mol Cell Biol 2009; 29:2570-2581.
68. Clark SL Jr. Cellular differentiation in the kidneys of newborn mice studies with the electron microscope. J Biophys Biochem Cytol 1957; 3:349-362.
69. Ashford TP, Porter KR. Cytoplasmic components in hepatic cell lysosomes. J Cell Biol 1962; 12:198-202.
70. Xie Z, Klionsky DJ. Autophagosome formation: core machinery and adaptations. Nat Cell Biol 2007; 9:1102-1109. (Pubitemid 47500484)
71. Kanki T, Wang K, Cao Y, et al. Atg32 is a mitochondrial protein that confers selectivity during mitophagy. Dev Cell 2009; 17:98-109.
72. Okamoto K, Kondo-Okamoto N, Ohsumi Y. Mitochondria-anchored receptor Atg32 mediates degradation of mitochondria via selective autophagy. Dev Cell 2009; 17:87-97.
73. 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; 112:1493-1502.
74. Mortensen M, Ferguson DJ, Edelmann M, et al. Loss of autophagy in erythroid cells leads to defective removal of mitochondria and severe anemia in vivo. Proc Natl Acad Sci USA 2010; 107:832-837.
75. Heynen MJ, Verwilghen RL. A quantitative ultrastructural study of normal rat erythroblasts and reticulocytes. Cell Tissue Res 1982; 224:397-408. (Pubitemid 12067494)
76. Tanaka Y. Bi-directional transport of ferritin in guinea pig erythroblasts in vitro. Blood 1970; 35:793-803.
77. Kraft C, Deplazes A, Sohrmann M, Peter M. Mature ribosomes are selectively degraded upon starvation by an autophagy pathway requiring the Ubp3p/ Bre5p ubiquitin protease. Nat Cell Biol 2008; 10:602-610. (Pubitemid 351627380)
78. Valentine WN, Fink K, Paglia DE, et al. Hereditary hemolytic anemia with human erythrocyte pyrimidine 5'-nucleotidase deficiency. J Clin Invest 1974; 54:866-879.
79. Fader CM, Sanchez D, Furlan M, Colombo MI. Induction of autophagy promotes fusion of multivesicular bodies with autophagic vacuoles in k562 cells. Traffic 2008; 9:230-250.
80. Nishida Y, Arakawa S, Fujitani K, et al. Discovery of Atg5/Atg7-independent alternative macroautophagy. Nature 2009; 461:654-658.
81. Bodemann BO, Orvedahl A, Cheng T, etal. RalB and the exocyst mediate the cellular starvation response by direct activation of autophagosome assembly. Cell 2011; 144:253-267.