Home LiteratureArticle Details
PMID: 7910943 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Erythroid expression of the heme-regulated eIF-2 alpha kinase.

Molecular and cellular biology ·Vol. 14 ·No. 6 ·1994-06-00 ·Pages 3906-14

Crosby JS, Lee K, London IM, Chen JJ

Abstract

The role of heme-regulated eIF-2 alpha kinase (HRI) in the regulation of protein synthesis in rabbit reticulocytes is well documented. Inhibitors of protein synthesis with properties similar to those of HRI have been described in some nonerythroid cell types, but it has not yet been determined whether these eIF-2 alpha kinase activities are mediated by HRI or one or more as yet uncharacterized kinases. We have studied the expression of mRNA, polypeptide, and kinase activities of HRI in various tissues from both nonanemic and anemic rabbits. Our results indicate that HRI is expressed in an erythroid cell-specific manner. HRI is present in the bone marrow and peripheral blood of both nonanemic and anemic rabbits but not in any of the other tissues tested. HRI mRNA is present at low levels in uninduced mouse erythroleukemic (MEL) cells and human K562 cells and accumulates to higher levels upon induction. The accumulation of HRI mRNA in differentiating MEL cells is dependent upon the presence of heme. The addition of 3-amino-1,2,4-triazole (AT), an inhibitor of heme biosynthesis, to the induction medium markedly reduced HRI mRNA accumulation. Simultaneous addition of hemin and AT to the dimethyl sulfoxide induction medium largely prevented the inhibition of HRI mRNA induction by AT. These findings indicate that HRI is expressed in an erythroid cell-specific manner and that the major physiologic role of HRI is in adjusting the synthesis of globins to the availability of heme.

MeSH Terms
Anemia/enzymology Animals Blotting, Northern Blotting, Western Cell Line Cells, Cultured Erythrocytes/enzymology Gene Expression Regulation, Enzymologic Heme/pharmacology Humans Leukemia, Experimental Leukemia, Myelogenous, Chronic, BCR-ABL Positive Mice Organ Specificity Polymerase Chain Reaction Protein Serine-Threonine Kinases/analysis,biosynthesis,blood RNA, Messenger/isolation & purification,metabolism Rabbits Tumor Cells, Cultured eIF-2 Kinase
Chemicals
RNA, Messenger Heme Protein Serine-Threonine Kinases eIF-2 Kinase
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Crosby J S
Harvard-M.I.T. Division of Health Sciences and Technology, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139.
Lee K
London I M
Chen J J
References (48)
48 references, click to expand
  1. Differentiation in erythroleukemic cells and their somatic hybrids.
    Proc Natl Acad Sci U S A. 1975 Jan;72(1):98-102 PMID: 164031
  2. Disulfide bond formation in the regulation of eIF-2 alpha kinase by heme.
    J Biol Chem. 1989 Jun 5;264(16):9559-64 PMID: 2722851
  3. Relationship between phosphorylation and activity of heme-regulated eukaryotic initiation factor 2 alpha kinase.
    Proc Natl Acad Sci U S A. 1981 Feb;78(2):866-70 PMID: 6940153
  4. Hemin control of globin synthesis: an assay for the inhibitor formed in the absence of hemin and some characteristics of its formation.
    J Mol Biol. 1971 May 28;58(1):317-27 PMID: 5088932
  5. Heat shock-induced translational alterations in HeLa cells. Initiation factor modifications and the inhibition of translation.
    J Biol Chem. 1984 Oct 10;259(19):11882-9 PMID: 6384217
  6. Phosphorylation of eukaryotic initiation factor 2 during physiological stresses which affect protein synthesis.
    J Biol Chem. 1987 Oct 25;262(30):14538-43 PMID: 3667588
  7. Activation of hemin-regulated initiation factor-2 kinase in heat-shocked HeLa cells.
    J Biol Chem. 1986 Jan 5;261(1):338-42 PMID: 3941080
  8. Phosphorylation of eukaryotic initiation factor (eIF) 2 alpha and inhibition of eIF-2B in GH3 pituitary cells by perturbants of early protein processing that induce GRP78.
    J Biol Chem. 1992 Aug 25;267(24):16751-4 PMID: 1512215
  9. Erythroid transcription factor NF-E2 is a haematopoietic-specific basic-leucine zipper protein.
    Nature. 1993 Apr 22;362(6422):722-8 PMID: 8469283
  10. Purification and characterisation of an initiation-factor-2 kinase from uninduced mouse erythroleukaemia cells.
    Eur J Biochem. 1993 Feb 1;211(3):529-38 PMID: 8094668
  11. Nucleotide sequence of katG, encoding catalase HPI of Escherichia coli.
    J Bacteriol. 1988 Sep;170(9):4415-9 PMID: 3045098
  12. Regulation of initiation factors during translational repression caused by serum depletion. Covalent modification.
    J Biol Chem. 1985 May 10;260(9):5493-7 PMID: 3886657
  13. Role of dimerization and modification of the CSF-1 receptor in its activation and internalization during the CSF-1 response.
    EMBO J. 1991 Feb;10(2):277-88 PMID: 1825054
  14. Signal transduction by receptors with tyrosine kinase activity.
    Cell. 1990 Apr 20;61(2):203-12 PMID: 2158859
  15. A 46 base pair enhancer sequence within the locus activating region is required for induced expression of the gamma-globin gene during erythroid differentiation.
    Nucleic Acids Res. 1990 May 11;18(9):2721-31 PMID: 2339058
  16. Effect of 3-amino-1, 2, 4-triazole on delta-amino-levulinic acid dehydrase activity.
    Science. 1957 Jul 26;126(3265):168 PMID: 13442665
  17. Effect of 3-amino-1,2,4-triazole on the stimulation of hepatic microsomal heme synthesis and induction of hepatic microsomal oxidases produced by phenobarbital.
    Mol Pharmacol. 1969 Jan;5(1):10-20 PMID: 4392110
  18. Regulation of protein synthesis in reticulocyte lysates: phosphorylation of methionyl-tRNAf binding factor by protein kinase activity of translational inhibitor isolated from hemedeficient lysates.
    Proc Natl Acad Sci U S A. 1976 Sep;73(9):3112-6 PMID: 184460
  19. Specificity of the protein kinase activity associated with the hemin-controlled repressor of rabbit reticulocyte.
    Proc Natl Acad Sci U S A. 1976 Sep;73(9):3078-82 PMID: 184458
  20. Platelet-derived growth factor (PDGF)-induced disulfide-linked dimerization of PDGF receptor in living cells.
    Mol Cell Biol. 1991 Jul;11(7):3756-61 PMID: 1646395
  21. Differential effect of hemin-controlled eIF-2 alpha kinases from mouse erythroleukemia cells on protein synthesis.
    Eur J Biochem. 1989 Jul 15;183(1):137-43 PMID: 2753041
  22. Tissue distribution and immunoreactivity of heme-regulated eIF-2 alpha kinase determined by monoclonal antibodies.
    Biochemistry. 1991 Mar 5;30(9):2555-62 PMID: 1672093
  23. Tandem AP-1-binding sites within the human beta-globin dominant control region function as an inducible enhancer in erythroid cells.
    Genes Dev. 1990 Jun;4(6):993-1006 PMID: 2116990
  24. Cloning of the cDNA of the heme-regulated eukaryotic initiation factor 2 alpha (eIF-2 alpha) kinase of rabbit reticulocytes: homology to yeast GCN2 protein kinase and human double-stranded-RNA-dependent eIF-2 alpha kinase.
    Proc Natl Acad Sci U S A. 1991 Sep 1;88(17):7729-33 PMID: 1679235
  25. Evidence for an inhibitor in the control of globin synthesis by hemin in a reticulocyte lysate.
    Biochem Biophys Res Commun. 1969 Apr 10;35(1):79-85 PMID: 5779151
  26. In situ phosphorylation of the alpha subunit of eukaryotic initiation factor 2 in reticulocyte lysates inhibited by heme deficiency, double-stranded RNA, oxidized glutathione, or the heme-regulated protein kinase.
    Proc Natl Acad Sci U S A. 1979 May;76(5):2118-22 PMID: 287050
  27. Analysis of phosphorylation of protein synthesis initiation factor eIF-2 by two-dimensional gel electrophoresis.
    Eur J Biochem. 1978 Sep 1;89(2):517-21 PMID: 710407
  28. Regulation by heme of mitochondrial protein transport through a conserved amino acid motif.
    Science. 1993 Jan 22;259(5094):522-5 PMID: 8424176
  29. Characterization of a rat liver factor that inhibits initiation of protein synthesis in rabbit reticulocyte lysates.
    Proc Natl Acad Sci U S A. 1977 Jun;74(6):2264-8 PMID: 196285
  30. The role of heme in the regulation of the late program of Friend cell erythroid differentiation.
    J Cell Physiol. 1979 Sep;100(3):467-79 PMID: 489671
  31. Inhibition of rabbit reticulocyte lysate protein synthesis by heavy metal ions involves the phosphorylation of the alpha-subunit of the eukaryotic initiation factor 2.
    J Biol Chem. 1987 Nov 25;262(33):15939-45 PMID: 3680235
  32. Phosphorylation of initiation factor elF-2 and the control of reticulocyte protein synthesis.
    Cell. 1977 May;11(1):187-200 PMID: 559547
  33. Characterization of a macromolecular inhibitor of polypeptide chain initiation from Ehrlich ascites tumor cells.
    Biochem Biophys Res Commun. 1976 SEP 20;72(2):768-75 PMID: 985647
  34. Glutathione. 8. The effects of glutathione disulfide on initiation of protein synthesis.
    Biochim Biophys Acta. 1972 Jul 31;272(4):623-37 PMID: 5050922
  35. Regulation of protein synthesis in rabbit reticulocyte lysates: purification and initial characterization of the cyclic 3':5'-AMP independent protein kinase of the heme-regulated translational inhibitor.
    Proc Natl Acad Sci U S A. 1976 Dec;73(12):4349-53 PMID: 1069987
  36. Effects of hemin and porphyrin compounds on intersubunit disulfide formation of heme-regulated eIF-2 alpha kinase and the regulation of protein synthesis in reticulocyte lysates.
    J Biol Chem. 1992 Oct 5;267(28):20519-24 PMID: 1356981
  37. Control of protein synthesis in human reticulocytes by heme-regulated and double-stranded RNA dependent eIF-2 alpha kinases.
    Biochem Biophys Res Commun. 1984 Mar 30;119(3):891-9 PMID: 6712675
  38. Mechanism of the inhibition of protein synthesis by vasopressin in rat liver.
    J Biol Chem. 1990 Oct 5;265(28):16794-8 PMID: 2211594
  39. Molecular cloning and characterization of the human double-stranded RNA-activated protein kinase induced by interferon.
    Cell. 1990 Jul 27;62(2):379-90 PMID: 1695551
  40. Purification and characterization of eukaryotic initiation factor (eIF)-2 alpha kinases from Ehrlich ascites tumor cells.
    J Biol Chem. 1993 Jun 15;268(17):12552-9 PMID: 8099583
  41. Control of globin synthesis by hemin: factors influencing formation of an inhibitor of globin chain initiation in reticulocyte lysates.
    Biochim Biophys Acta. 1972 Dec 6;287(2):340-52 PMID: 4680051
  42. Rat hemopexin. Molecular cloning, primary structural characterization, and analysis of gene expression.
    Biochemistry. 1991 Jan 22;30(3):823-9 PMID: 1988069
  43. Presence of haemin-controlled eIF-2 alpha kinases in both undifferentiated and differentiating mouse erythroleukaemia cells.
    Biochem J. 1989 Sep 1;262(2):569-74 PMID: 2803269
  44. Increase in globin chains and globin mRNA in erythroleukemia cells in response to hemin.
    Arch Biochem Biophys. 1977 Feb;179(1):106-12 PMID: 265145
  45. Translational control in mammalian cells.
    Annu Rev Biochem. 1991;60:717-55 PMID: 1883206
  46. Functional dissection and sequence of yeast HAP1 activator.
    Cell. 1989 Jan 27;56(2):291-301 PMID: 2643482
  47. Reduced formation of initiation complexes between Met-tRNAf and 40-S ribosomal subunits in rabbit reticulocyte lysates incubated at elevated temperatures. Activity of the Met-tRNAf binding factor.
    Eur J Biochem. 1978 Mar 15;84(2):601-10 PMID: 639805
  48. Amino acid microsequencing of internal tryptic peptides of heme-regulated eukaryotic initiation factor 2 alpha subunit kinase: homology to protein kinases.
    Proc Natl Acad Sci U S A. 1991 Jan 15;88(2):315-9 PMID: 1671169
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
1994-06-00
Pages
3906-14
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC358757
Subset
IM
Grants
NIDDK NIH HHS · R01 DK016272 · United States
NIDDK NIH HHS · DK-16272 · United States
NIGMS NIH HHS · GM-24825-13 · 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: product@genelibs.com