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PMID: 6304111 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

ATP serves two distinct roles in protein degradation in reticulocytes, one requiring and one independent of ubiquitin.

The Journal of cell biology ·Vol. 96 ·No. 6 ·1983-06-00 ·Pages 1580-5

Tanaka K, Waxman L, Goldberg AL

Abstract

Protein degradation in rabbit reticulocytes is a nonlysosomal process requiring ATP. Recently, appreciable evidence has been presented that ATP is required for the covalent binding of the polypeptide ubiquitin to epsilon-amino groups on protein substrates. To test whether linkage of ubiquitin to substrates is required for ATP-dependent proteolysis, the amino groups of 3H-methyl-casein and denatured 125I-bovine serum albumin (BSA) were completely (93-99%) blocked by methylation, acetylation, carbamylation, or succinylation. In each case, the proteins lacking amino groups were still degraded by an ATP-stimulated process, although these various treatments altered absolute rates of proteolysis and reduced the magnitude of the ATP stimulation (two- to fourfold) below that seen measured with the unmodified substrates. When ubiquitin was removed by ion exchange chromatography, ATP still stimulated breakdown of casein and carbamylated casein twofold. The addition of ubiquitin in the presence of ATP caused a further twofold increase in the hydrolysis of unmodified casein but did not affect the degradation of casein lacking amino groups. Thus ubiquitin conjugation to substrates appears important in the breakdown of certain substrates (especially of BSA), but this reaction is not essential for ATP-stimulated proteolysis. The ATP-activated step that is independent of ubiquitin probably is also involved in the degradation of unblocked proteins, since both processes require Mg++ and ATP hydrolysis and are inhibited by hemin but not by protoporphyrin IX. These results suggest that ATP has distinct roles at different steps in the degradative pathway.

MeSH Terms
Adenosine Triphosphate/analogs & derivatives,metabolism,pharmacology Animals Caseins/metabolism Chromosomal Proteins, Non-Histone/metabolism Hemin/pharmacology Magnesium/pharmacology Proteins/metabolism Rabbits Reticulocytes/metabolism Ubiquitins
Chemicals
Caseins Chromosomal Proteins, Non-Histone Proteins Ubiquitins 5'-adenylyl (beta,gamma-methylene)diphosphonate Hemin Adenosine Triphosphate Magnesium alpha,beta-methyleneadenosine 5'-triphosphate
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Tanaka K
Waxman L
Goldberg A L
References (33)
33 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. Radioactive labeling of proteins in vitro.
    J Biol Chem. 1971 Feb 10;246(3):831-2 PMID: 5100767
  3. Fluorometric assay of proteins in the nanogram range.
    Arch Biochem Biophys. 1973 Mar;155(1):213-20 PMID: 4736505
  4. Isolation of a polypeptide that has lymphocyte-differentiating properties and is probably represented universally in living cells.
    Proc Natl Acad Sci U S A. 1975 Jan;72(1):11-5 PMID: 1078892
  5. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.
    Anal Biochem. 1976 May 7;72:248-54 PMID: 942051
  6. Intracellular protein degradation in mammalian and bacterial cells: Part 2.
    Annu Rev Biochem. 1976;45:747-803 PMID: 786161
  7. A soluble ATP-dependent proteolytic system responsible for the degradation of abnormal proteins in reticulocytes.
    Proc Natl Acad Sci U S A. 1977 Jan;74(1):54-8 PMID: 264694
  8. Intermediate steps in the degradation of a specific abnormal protein in Escherichia coli.
    J Biol Chem. 1977 Dec 10;252(23):8350-7 PMID: 336618
  9. Deg phenotype of Escherichia coli lon mutants.
    J Bacteriol. 1978 Feb;133(2):844-51 PMID: 146704
  10. A heat-stable polypeptide component of an ATP-dependent proteolytic system from reticulocytes.
    Biochem Biophys Res Commun. 1978 Apr 28;81(4):1100-5 PMID: 666810
  11. Identification and partial purification of an ATP-stimulated alkaline protease in rat liver.
    J Biol Chem. 1979 May 25;254(10):3712-5 PMID: 35530
  12. Labeling of proteins by reductive methylation using sodium cyanoborohydride.
    J Biol Chem. 1979 Jun 10;254(11):4359-65 PMID: 571437
  13. Protein degradation is stimulated by ATP in extracts of Escherichia coli.
    J Biol Chem. 1979 Sep 10;254(17):8194-200 PMID: 112099
  14. Resolution of the ATP-dependent proteolytic system from reticulocytes: a component that interacts with ATP.
    Proc Natl Acad Sci U S A. 1979 Jul;76(7):3107-10 PMID: 290989
  15. Control of protein degradation in reticulocytes and reticulocyte extracts by hemin.
    J Biol Chem. 1980 May 25;255(10):4563-8 PMID: 7372594
  16. ATP-dependent conjugation of reticulocyte proteins with the polypeptide required for protein degradation.
    Proc Natl Acad Sci U S A. 1980 Mar;77(3):1365-8 PMID: 6769112
  17. Proposed role of ATP in protein breakdown: conjugation of protein with multiple chains of the polypeptide of ATP-dependent proteolysis.
    Proc Natl Acad Sci U S A. 1980 Apr;77(4):1783-6 PMID: 6990414
  18. Characterization of the heat-stable polypeptide of the ATP-dependent proteolytic system from reticulocytes.
    J Biol Chem. 1980 Aug 25;255(16):7525-8 PMID: 6249802
  19. Ubiquitin is the ATP-dependent proteolysis factor I of rabbit reticulocytes.
    J Biol Chem. 1980 Aug 25;255(16):7529-32 PMID: 6249803
  20. Determination and characteristics of energy-dependent proteolysis in rabbit reticulocytes.
    Eur J Biochem. 1980 Aug;109(2):405-10 PMID: 7408892
  21. Identification of the active amino acid residue of the polypeptide of ATP-dependent protein breakdown.
    J Biol Chem. 1981 Feb 25;256(4):1525-8 PMID: 6257674
  22. E. coli contains eight soluble proteolytic activities, one being ATP dependent.
    Nature. 1981 Aug 13;292(5824):652-4 PMID: 7019728
  23. ATP hydrolysis-dependent protease activity of the lon (capR) protein of Escherichia coli K-12.
    Proc Natl Acad Sci U S A. 1981 Aug;78(8):4728-32 PMID: 6458036
  24. The product of the lon (capR) gene in Escherichia coli is the ATP-dependent protease, protease La.
    Proc Natl Acad Sci U S A. 1981 Aug;78(8):4931-5 PMID: 6458037
  25. Hemin inhibits ATP-dependent ubiquitin-dependent proteolysis: role of hemin in regulating ubiquitin conjugate degradation.
    Proc Natl Acad Sci U S A. 1981 Nov;78(11):6845-8 PMID: 6273891
  26. Studies of the ATP-dependent proteolytic enzyme, protease La, from Escherichia coli.
    J Biol Chem. 1982 Apr 25;257(8):4187-95 PMID: 7040380
  27. Liver mitochondria contain an ATP-dependent, vanadate-sensitive pathway for the degradation of proteins.
    Proc Natl Acad Sci U S A. 1982 Mar;79(6):1869-73 PMID: 7043466
  28. Mechanisms of intracellular protein breakdown.
    Annu Rev Biochem. 1982;51:335-64 PMID: 6287917
  29. Scope of the ATP--ubiquitin system for intracellular protein degradation.
    FEBS Lett. 1982 Jul 5;143(2):225-7 PMID: 6288460
  30. Demonstration of an ATP-dependent, vanadate-sensitive endoprotease in the matrix of rat liver mitochondria.
    J Biol Chem. 1982 Oct 10;257(19):11673-9 PMID: 6749845
  31. Protease La from Escherichia coli hydrolyzes ATP and proteins in a linked fashion.
    Proc Natl Acad Sci U S A. 1982 Aug;79(16):4883-7 PMID: 6214787
  32. Role for the adenosine triphosphate-dependent proteolytic pathway in reticulocyte maturation.
    Science. 1982 Feb 19;215(4535):978-80 PMID: 7156977
  33. Conjugation of ubiquitin to denatured hemoglobin is proportional to the rate of hemoglobin degradation in HeLa cells.
    Proc Natl Acad Sci U S A. 1982 Oct;79(19):5857-61 PMID: 6310549
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1983-06-00
Pages
1580-5
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2112434
Subset
IM
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