Home LiteratureArticle Details
PMID: 3654759 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.

Erythroid anion transporter assembly is mediated by a developmentally regulated recruitment onto a preassembled membrane cytoskeleton.

The Journal of cell biology ·Vol. 105 ·No. 3 ·1987-09-00 ·Pages 1405-16

Cox JV, Stack JH, Lazarides E

Abstract

Analysis of the expression and assembly of the anion transporter by metabolic pulse-chase and steady-state protein and RNA measurements reveals that the extent of association of band 3 with the membrane cytoskeleton varies during chicken embryonic development. Pulse-chase studies have indicated that band 3 polypeptides do not associate with the membrane cytoskeleton until they have been transported to the plasma membrane. At this time, band 3 polypeptides are slowly recruited, over a period of hours, onto a preassembled membrane cytoskeletal network and the extent of this cytoskeletal assembly is developmentally regulated. Only 3% of the band 3 polypeptides are cytoskeletal-associated in 4-d erythroid cells vs. 93% in 10-d erythroid cells and 36% in 15-d erythroid cells. This observed variation appears to be regulated primarily at the level of recruitment onto the membrane cytoskeleton rather than by different transport kinetics to the membrane or differential turnover of the soluble and insoluble polypeptides and is not dependent upon the lineage or stage of differentiation of the erythroid cells. Steady-state protein and RNA analyses indicate that the low levels of cytoskeletal band 3 very early in development most likely result from limiting amounts of ankyrin and protein 4.1, the membrane cytoskeletal binding sites for band 3. As embryonic development proceeds, ankyrin and protein 4.1 levels increase with a concurrent rise in the level of cytoskeletal band 3 until, on day 10 of development, virtually all of the band 3 polypeptides are cytoskeletal bound. After day 10, the levels of total and cytoskeletal band 3 decline, whereas ankyrin and protein 4.1 continue to accumulate until day 18, indicating that the cytoskeletal association of band 3 is not regulated solely by the availability of membrane cytoskeletal binding sites at later stages of development. Thus, multiple mechanisms appear to regulate the recruitment of band 3 onto the erythroid membrane cytoskeleton during chicken embryonic development.

MeSH Terms
Animals Anion Exchange Protein 1, Erythrocyte/biosynthesis,genetics Chick Embryo Cytoskeleton/metabolism Embryonic and Fetal Development Erythrocyte Membrane/metabolism Erythrocytes/metabolism Membrane Proteins/blood Nucleic Acid Hybridization
Chemicals
Anion Exchange Protein 1, Erythrocyte Membrane Proteins
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Cox J V
Division of Biology, California Institute of Technology, Pasadena 91125.
Stack J H
Lazarides E
References (44)
44 references, click to expand
  1. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  2. Gelsolin is expressed in early erythroid progenitor cells and negatively regulated during erythropoiesis.
    J Cell Biol. 1987 Sep;105(3):1425-33 PMID: 2821013
  3. The organization of proteins in the human red blood cell membrane. A review.
    J Cell Biol. 1974 Jul;62(1):1-19 PMID: 4600883
  4. Changes in cyclic AMP, adrenylate cyclase and protein kinase levels during the development of embryonic chick skeletal muscle.
    Exp Cell Res. 1975 Jun;93(1):55-62 PMID: 166855
  5. Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I.
    J Mol Biol. 1977 Jun 15;113(1):237-51 PMID: 881736
  6. Sizing and mapping of early adenovirus mRNAs by gel electrophoresis of S1 endonuclease-digested hybrids.
    Cell. 1977 Nov;12(3):721-32 PMID: 922889
  7. Copurification of actin and desmin from chicken smooth muscle and their copolymerization in vitro to intermediate filaments.
    J Cell Biol. 1979 Jan;80(1):166-82 PMID: 570568
  8. Identification by peptide analysis of the spectrin-binding protein in human erythrocytes.
    J Biol Chem. 1979 Apr 10;254(7):2526-32 PMID: 429298
  9. 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
  10. In vitro formation of a complex between cytoskeletal proteins of the human erythrocyte.
    Nature. 1979 Aug 30;280(5725):811-4 PMID: 471052
  11. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications.
    Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350-4 PMID: 388439
  12. Spectrin plus band 4.1 cross-link actin. Regulation by micromolar calcium.
    J Cell Biol. 1980 May;85(2):361-76 PMID: 6892816
  13. 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
  14. Band 4.1 causes spectrin-actin gels to become thixiotropic.
    Biochem Biophys Res Commun. 1980 Dec 31;97(4):1429-35 PMID: 6894235
  15. The aldolase-binding site of the human erythrocyte membrane is at the NH2 terminus of band 3.
    J Biol Chem. 1981 Nov 10;256(21):11203-8 PMID: 7287763
  16. Biosynthesis of the erythrocyte anion transport protein.
    J Biol Chem. 1981 Nov 10;256(21):11337-44 PMID: 6793594
  17. Characterization and partial sequence of di-iodosulphophenyl isothiocyanate-binding peptide from human erythrocyte anion-transport protein.
    Biochem J. 1982 Sep 1;205(3):465-75 PMID: 7150226
  18. 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
  19. Spectral and oxygen-release kinetic properties of human hemoglobin bound to the cytoplasmic fragment of band 3 protein in solution.
    Biochim Biophys Acta. 1983 Jun 15;745(2):134-9 PMID: 6849940
  20. Amino acid sequence of the N alpha-terminal 201 residues of human erythrocyte membrane band 3.
    J Biol Chem. 1983 Jul 10;258(13):7981-90 PMID: 6345535
  21. Characterization of the chicken erythrocyte anion exchange protein.
    J Biol Chem. 1983 Aug 10;258(15):9431-6 PMID: 6874695
  22. The human erythrocyte anion-transport protein. Partial amino acid sequence, conformation and a possible molecular mechanism for anion exchange.
    Biochem J. 1983 Sep 1;213(3):577-86 PMID: 6615451
  23. Polypeptides immunologically related to band 3 are present in nucleated somatic cells.
    Proc Natl Acad Sci U S A. 1983 Nov;80(22):6882-6 PMID: 6196779
  24. Tissue-specific expression of two mRNA species transcribed from a single vimentin gene.
    Cell. 1983 Dec;35(2 Pt 1):411-20 PMID: 6317186
  25. 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
  26. Assembly and topogenesis of the spectrin-based membrane skeleton in erythroid development.
    Cell. 1984 Jun;37(2):354-6 PMID: 6233006
  27. 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
  28. 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
  29. 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
  30. Identification of immunoreactive forms of human erythrocyte band 3 in nonerythroid cells.
    Eur J Cell Biol. 1984 May;34(1):144-50 PMID: 6203749
  31. Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter.
    Nucleic Acids Res. 1984 Sep 25;12(18):7035-56 PMID: 6091052
  32. 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
  33. 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
  34. Interactions between protein 4.1 and band 3. An alternative binding site for an element of the membrane skeleton.
    J Biol Chem. 1985 Mar 25;260(6):3676-83 PMID: 3972843
  35. 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
  36. 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
  37. Primary structure and transmembrane orientation of the murine anion exchange protein.
    Nature. 1985 Jul 18-24;316(6025):234-8 PMID: 2410791
  38. Assembly of protein 4.1 during chicken erythroid differentiation.
    J Cell Biol. 1986 Apr;102(4):1157-63 PMID: 3958041
  39. Phosphorylation reduces the affinity of protein 4.1 for spectrin.
    Biochemistry. 1986 Apr 8;25(7):1764-70 PMID: 3707908
  40. Cloning and structural characterization of a human non-erythroid band 3-like protein.
    EMBO J. 1986 Jun;5(6):1205-14 PMID: 3015590
  41. Control of erythroid differentiation: asynchronous expression of the anion transporter and the peripheral components of the membrane skeleton in AEV- and S13-transformed cells.
    J Cell Biol. 1986 Nov;103(5):1789-98 PMID: 2946700
  42. Topoisomerase II: A specific marker for cell proliferation.
    J Cell Biol. 1986 Dec;103(6 Pt 2):2569-81 PMID: 3025219
  43. Regulated expression of multiple chicken erythroid membrane skeletal protein 4.1 variants is governed by differential RNA processing and translational control.
    Proc Natl Acad Sci U S A. 1987 Jul;84(13):4432-6 PMID: 3474611
  44. The erythroid cells and haemoglobins of the chick embryo.
    Philos Trans R Soc Lond B Biol Sci. 1973 Oct 25;266(877):225-305 PMID: 4147843
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1987-09-00
Pages
1405-16
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2114816
Subset
IM
Grants
NIA NIH HHS · AG-06078A · United States
NHLBI NIH HHS · HL-35801A · United States
NIGMS NIH HHS · T32 GM-07616 · United States
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]