Home LiteratureArticle Details
PMID: 2946700 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Control of erythroid differentiation: asynchronous expression of the anion transporter and the peripheral components of the membrane skeleton in AEV- and S13-transformed cells.

The Journal of cell biology ·Vol. 103 ·No. 5 ·1986-11-00 ·Pages 1789-98

Woods CM, Boyer B, Vogt PK, Lazarides E

Abstract

Chicken erythroblasts transformed with avian erythroblastosis virus or S13 virus provide suitable model systems with which to analyze the maturation of immature erythroblasts into erythrocytes. The transformed cells are blocked in differentiation at around the colony-forming unit-erythroid stage of development but can be induced to differentiate in vitro. Analysis of the expression and assembly of components of the membrane skeleton indicates that these cells simultaneously synthesize alpha-spectrin, beta-spectrin, ankyrin, and protein 4.1 at levels that are comparable to those of mature erythroblasts. However, they do not express any detectable amounts of anion transporter. The peripheral membrane skeleton components assemble transiently and are subsequently rapidly catabolized, resulting in 20-40-fold lower steady-state levels than are found in maturing erythrocytes. Upon spontaneous or chemically induced terminal differentiation of these cells expression of the anion transporter is initiated with a concommitant increase in the steady-state levels of the peripheral membrane-skeletal components. These results suggest that during erythropoiesis, expression of the peripheral components of the membrane skeleton is initiated earlier than that of the anion transporter. Furthermore, they point a key role for the anion transporter in conferring long-term stability to the assembled erythroid membrane skeleton during terminal differentiation.

MeSH Terms
Alpharetrovirus Animals Anion Exchange Protein 1, Erythrocyte/metabolism Ankyrins Blood Proteins/metabolism Cell Differentiation Cell Membrane/metabolism Cell Transformation, Viral Chickens Cytoskeletal Proteins Erythroblasts/cytology,metabolism Erythropoiesis Membrane Proteins/metabolism Neuropeptides Retroviridae Spectrin/metabolism
Chemicals
Anion Exchange Protein 1, Erythrocyte Ankyrins Blood Proteins Cytoskeletal Proteins Membrane Proteins Neuropeptides erythrocyte membrane band 4.1 protein erythrocyte membrane protein band 4.1-like 1 Spectrin
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Woods C M
Boyer B
Vogt P K
Lazarides E
References (80)
80 references, click to expand
  1. Spectrin and protein 4.1 as an actin filament capping complex.
    FEBS Lett. 1984 Apr 24;169(2):161-4 PMID: 6538852
  2. Membrane skeletal protein 4.1 of avian erythrocytes is composed of multiple variants that exhibit tissue-specific expression.
    Cell. 1984 Jun;37(2):595-607 PMID: 6373017
  3. Biogenesis of the avian erythroid membrane skeleton: receptor-mediated assembly and stabilization of ankyrin (goblin) and spectrin.
    J Cell Biol. 1984 May;98(5):1899-904 PMID: 6233291
  4. Goblin (ankyrin) in striated muscle: identification of the potential membrane receptor for erythroid spectrin in muscle cells.
    Proc Natl Acad Sci U S A. 1984 Jun;81(11):3292-6 PMID: 6233607
  5. Association of gag-myc proteins from avian myelocytomatosis virus wild-type and mutants with chromatin.
    EMBO J. 1982;1(8):919-27 PMID: 6329716
  6. Differentiation of murine erythroleukemia cells results in the rapid repression of vimentin gene expression.
    J Cell Biol. 1984 Jul;99(1 Pt 1):306-14 PMID: 6376521
  7. Spectrin deficient inherited hemolytic anemias in the mouse: characterization by spectrin synthesis and mRNA activity in reticulocytes.
    Cell. 1984 Jul;37(3):721-9 PMID: 6234993
  8. Reformation of the marginal band of avian erythrocytes in vitro using calf-brain tubulin: peripheral determinants of microtubule form.
    J Cell Biol. 1984 Dec;99(6):2108-13 PMID: 6542106
  9. Tissue-specific expression of distinct spectrin and ankyrin transcripts in erythroid and nonerythroid cells.
    J Cell Biol. 1985 Jan;100(1):152-60 PMID: 2981230
  10. Appearance of new variants of membrane skeletal protein 4.1 during terminal differentiation of avian erythroid and lenticular cells.
    Nature. 1985 Jan 17-23;313(5999):238-41 PMID: 3855501
  11. Protein phosphorylation at tyrosine is induced by the v-erbB gene product in vivo and in vitro.
    Cell. 1985 Mar;40(3):609-18 PMID: 2982500
  12. Antibodies against a synthetic peptide as a probe for the kinase activity of the avian EGF receptor and v-erbB protein.
    Cell. 1985 Mar;40(3):619-25 PMID: 2982501
  13. Degradation of unassembled alpha- and beta-spectrin by distinct intracellular pathways: regulation of spectrin topogenesis by beta-spectrin degradation.
    Cell. 1985 Apr;40(4):959-69 PMID: 2985271
  14. Anion transporter: highly cell-type-specific expression of distinct polypeptides and transcripts in erythroid and nonerythroid cells.
    J Cell Biol. 1985 May;100(5):1548-57 PMID: 3838751
  15. Interleukin 3 promotes erythroid burst formation in "serum-free" cultures without detectable erythropoietin.
    Proc Natl Acad Sci U S A. 1985 May;82(10):3291-5 PMID: 3923475
  16. S13, a rapidly oncogenic replication-defective avian retrovirus.
    Virology. 1985 Aug;145(1):141-53 PMID: 2990096
  17. Properties and development of erythropoietic stem cells in the chick embryo.
    J Embryol Exp Morphol. 1976 Oct;36(2):247-60 PMID: 12240
  18. Changes in the composition of plasma membrane proteins during differentiation of embryonic chick erythroid cell.
    Proc Natl Acad Sci U S A. 1977 Mar;74(3):1062-6 PMID: 265550
  19. Induction of spectrin in erythroleukemic cells transformed by Friend virus.
    Proc Natl Acad Sci U S A. 1977 Sep;74(9):3898-902 PMID: 410028
  20. Three stages of erythropoietic progenitor cell differentiation distinguished by a number of physical and biologic properties.
    Blood. 1978 Mar;51(3):527-37 PMID: 623913
  21. Membrane protein synthesis in embryonic chick erythroid cells.
    J Biol Chem. 1978 Mar 25;253(6):1892-7 PMID: 564900
  22. Erythroleukemic differentiation.
    Annu Rev Biochem. 1978;47:419-48 PMID: 354501
  23. Temperature-sensitive mutant of avian erythroblastosis virus suggests a block of differentiation as mechanism of leukaemogenesis.
    Nature. 1978 Oct 12;275(5680):496-501 PMID: 211440
  24. Avian leukemia viruses: interaction with their target cells in vivo and in vitro.
    Biochim Biophys Acta. 1978 Nov 17;516(3):269-99 PMID: 215208
  25. Proviruses of avian sarcoma virus are terminally redundant, co-extensive with unintegrated linear DNA and integrated at many sites.
    Cell. 1978 Dec;15(4):1397-410 PMID: 215325
  26. Defectiveness of avian erythroblastosis virus: synthesis of a 75K gag-related protein.
    Virology. 1979 Jan 15;92(1):31-45 PMID: 217166
  27. Identification by peptide analysis of the spectrin-binding protein in human erythrocytes.
    J Biol Chem. 1979 Apr 10;254(7):2526-32 PMID: 429298
  28. Identification and partial purification of ankyrin, the high affinity membrane attachment site for human erythrocyte spectrin.
    J Biol Chem. 1979 Apr 10;254(7):2533-41 PMID: 372182
  29. Response of hemopoietic cells to avian acute leukemia viruses: effects on the differentiation of the target cells.
    Cell. 1979 Mar;16(3):627-38 PMID: 222465
  30. Three-dimensional view of the chromatin in freeze-fractured chicken erythrocyte nuclei.
    J Microsc. 1979 Apr;115(3):225-34 PMID: 458848
  31. The membrane attachment protein for spectrin is associated with band 3 in human erythrocyte membranes.
    Nature. 1979 Aug 9;280(5722):468-73 PMID: 379653
  32. In vitro formation of a complex between cytoskeletal proteins of the human erythrocyte.
    Nature. 1979 Aug 30;280(5725):811-4 PMID: 471052
  33. Avian erythroblastosis virus: transformation-specific sequences form a contiguous segment of 3.25 kb located in the middle of the 6-kb genome.
    Virology. 1979 Sep;97(2):366-77 PMID: 224587
  34. Isolation and transformation of primary mesenchymal cells of the chick embryo.
    Cell. 1979 Aug;17(4):801-11 PMID: 487430
  35. Antigenic characterization of chick erythrocytes and erythropoietic precursors: identification of several definitive populations during embryogenesis.
    Dev Biol. 1979 Sep;72(1):155-66 PMID: 92428
  36. Association between ankyrin and the cytoplasmic domain of band 3 isolated from the human erythrocyte membrane.
    J Biol Chem. 1980 Jul 10;255(13):6424-32 PMID: 6446557
  37. Avian retrovirus S13: properties of the genome and of the transformation-specific protein.
    Virology. 1985 Aug;145(1):154-64 PMID: 2990097
  38. The putative transforming protein of S13 avian erythroblastosis virus is a transmembrane glycoprotein with an associated protein kinase activity.
    Proc Natl Acad Sci U S A. 1985 Dec;82(23):8237-41 PMID: 2999798
  39. Immunofluorescence examination of beta tubulin expression and marginal band formation in developing chicken erythroblasts.
    J Cell Biol. 1986 Feb;102(2):628-35 PMID: 3511076
  40. Sequence and expression of human estrogen receptor complementary DNA.
    Science. 1986 Mar 7;231(4742):1150-4 PMID: 3753802
  41. Human oestrogen receptor cDNA: sequence, expression and homology to v-erb-A.
    Nature. 1986 Mar 13-19;320(6058):134-9 PMID: 3754034
  42. Assembly of protein 4.1 during chicken erythroid differentiation.
    J Cell Biol. 1986 Apr;102(4):1157-63 PMID: 3958041
  43. Stabilizing infrastructure of cell membranes.
    Annu Rev Cell Biol. 1985;1:531-61 PMID: 3916322
  44. Fractionation of the avian erythrocyte: an ultrastructural study.
    J Ultrastruct Res. 1971 Jul;36(1):8-23 PMID: 4105480
  45. Primitive erythropoiesis in early chick embryogenesis. I. Cell cycle kinetics and the control of cell division.
    J Cell Biol. 1971 Sep;50(3):652-68 PMID: 5098864
  46. Purification of biologically active globin messenger RNA by chromatography on oligothymidylic acid-cellulose.
    Proc Natl Acad Sci U S A. 1972 Jun;69(6):1408-12 PMID: 4504350
  47. Erythrocyte membrane-specific antigens in Friend virus-induced leukemia cells.
    Bibl Haematol. 1973;39:955-67 PMID: 4591441
  48. Selective solubilization of proteins and phospholipids from red blood cell membranes by nonionic detergents.
    J Supramol Struct. 1973;1(3):233-48 PMID: 4804838
  49. Differentiation in erythroleukemic cells and their somatic hybrids.
    Proc Natl Acad Sci U S A. 1975 Jan;72(1):98-102 PMID: 164031
  50. Biogenesis of erythrocyte membrane proteins. In vitro studies with rabbit reticulocytes.
    Biochim Biophys Acta. 1975 Apr 21;389(1):177-87 PMID: 1138907
  51. Erythropoietin sensitivity as a differentiation marker in the hemopoietic system: studies of three erythropoietic colony responses in culture.
    J Cell Physiol. 1976 Oct;89(2):289-301 PMID: 987043
  52. Asynchronous synthesis of erythrocyte membrane proteins.
    Proc Natl Acad Sci U S A. 1976 Sep;73(9):3206-10 PMID: 1067613
  53. Properties and structural role of the subunits of human spectrin.
    Eur J Biochem. 1980 Jun;107(2):355-61 PMID: 7398646
  54. Evidence that spectrin binds to macromolecular complexes on the inner surface of the red cell membrane.
    J Cell Sci. 1980 Apr;42:1-22 PMID: 7400228
  55. Biosynthesis of erythrocyte membrane protein band 3 in DMSO-induced Friend erythroleukemia cells.
    J Cell Physiol. 1980 Aug;104(2):261-8 PMID: 6931832
  56. Reassociation of ankyrin with band 3 in erythrocyte membranes and in lipid vesicles.
    J Biol Chem. 1980 Dec 25;255(24):11965-72 PMID: 6449514
  57. Hemopoietic stem cell differentiation.
    Biochim Biophys Acta. 1980 Nov 26;605(4):431-59 PMID: 7006701
  58. Early precursors in the erythroid lineage are the specific target cells of avian erythroblastosis virus in vitro.
    Cell. 1980 Dec;22(3):683-91 PMID: 6257394
  59. In vitro development of CFU-E and BFU-E in cultures of embryonic and post-embryonic chicken hematopoietic cells.
    J Cell Physiol. 1980 Dec;105(3):553-63 PMID: 7462339
  60. Characterization of the hematopoietic target cells of AEV, MC29 and AMV avian leukemia viruses.
    Exp Cell Res. 1981 Feb;131(2):331-43 PMID: 6258948
  61. Interaction of cytoskeletal proteins on the human erythrocyte membrane.
    Cell. 1981 Apr;24(1):24-32 PMID: 6453651
  62. Proposal for naming host cell-derived inserts in retrovirus genomes.
    J Virol. 1981 Dec;40(3):953-7 PMID: 7321107
  63. Isolation and characterization of chicken DNA homologous to the two putative oncogenes of avian erythroblastosis virus.
    Cell. 1982 Jan;28(1):135-43 PMID: 6279309
  64. Erythroblast cell lines transformed by a temperature-sensitive mutant of avian erythroblastosis virus: a model system to study erythroid differentiation in vitro.
    J Cell Physiol Suppl. 1982;1:195-207 PMID: 6279674
  65. Hormone-dependent terminal differentiation in vitro of chicken erythroleukemia cells transformed by ts mutants of avian erythroblastosis virus.
    Cell. 1982 Apr;28(4):907-19 PMID: 6954007
  66. Target cells infected by avian erythroblastosis virus differentiate and become transformed.
    Cell. 1982 Apr;28(4):921-9 PMID: 7094018
  67. Temperature-sensitive changes in the structure of globin chromatin in lines of red cell precursors transformed by ts-AEV.
    Cell. 1982 Apr;28(4):931-40 PMID: 7094019
  68. Structural associations of synemin and vimentin filaments in avian erythrocytes revealed by immunoelectron microscopy.
    Cell. 1982 Aug;30(1):263-75 PMID: 6751558
  69. Widespread occurrence of avian spectrin in nonerythroid cells.
    Cell. 1982 Jul;29(3):821-33 PMID: 6758951
  70. Transforming capacities of avian erythroblastosis virus mutants deleted in the erbA or erbB oncogenes.
    Cell. 1983 Jan;32(1):227-38 PMID: 6297784
  71. Identification and characterization of the avian erythroblastosis virus erbB gene product as a membrane glycoprotein.
    Cell. 1983 Feb;32(2):579-88 PMID: 6297801
  72. Structural and dynamic states of actin in the erythrocyte.
    J Cell Biol. 1983 Mar;96(3):768-75 PMID: 6682109
  73. Synthesis and assembly of spectrin during avian erythropoiesis: stoichiometric assembly but unequal synthesis of alpha and beta spectrin.
    Cell. 1983 Apr;32(4):1081-91 PMID: 6220807
  74. Role of the v-erbA and v-erbB oncogenes of avian erythroblastosis virus in erythroid cell transformation.
    Cell. 1983 Aug;34(1):7-9 PMID: 6309413
  75. The erbB gene of avian erythroblastosis virus is a member of the src gene family.
    Cell. 1983 Nov;35(1):71-8 PMID: 6313229
  76. Tissue-specific expression of two mRNA species transcribed from a single vimentin gene.
    Cell. 1983 Dec;35(2 Pt 1):411-20 PMID: 6317186
  77. Glycophorin is linked by band 4.1 protein to the human erythrocyte membrane skeleton.
    Nature. 1984 Feb 16-22;307(5952):655-8 PMID: 6694756
  78. The membrane glycoprotein encoded by the retroviral oncogene v-erb-B is structurally related to tyrosine-specific protein kinases.
    Proc Natl Acad Sci U S A. 1984 Feb;81(3):704-7 PMID: 6322166
  79. Temperature-sensitive mutants of avian erythroblastosis virus: surface expression of the erbB product correlates with transformation.
    Cell. 1984 Apr;36(4):963-72 PMID: 6323030
  80. Co-expression of spectrin and fodrin in Friend erythroleukemic cells treated with DMSO.
    Exp Cell Res. 1984 May;152(1):15-21 PMID: 6585301
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
DOI
10.1083/jcb.103.5.1789
Published
1986-11-00
Pages
1789-98
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2114368
Subset
IM
Grants
NIA NIH HHS · AGO6078A-01 · United States
NCI NIH HHS · CA13213 · United States
NCI NIH HHS · CA29777 · United States
External Links
PubMed source DOI: 10.1083/jcb.103.5.1789 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2