DOI: 10.1126/science.2538923. A Multiubiquitin Chain Is Confined to Specific Lysine in a Targeted Short-Lived Protein

A Multiubiquitin Chain Is Confined to Specific Lysine in a Targeted Short-Lived Protein

10.1126/science.2538923

Crossref journal-article

American Association for the Advancement of Science (AAAS)

Science (221)

Abstract

The ubiquitin-dependent degradation of a test protein β-galactosidase (βgal) is preceded by ubiquitination of βgal. The many (from 1 to more than 20) ubiquitin moieties attached to a molecule of βgal occur as an ordered chain of branched ubiquitin-ubiquitin conjugates in which the carboxyl-terminal Gly 76 of one ubiquitin is joined to the internal Lys 48 of an adjacent ubiquitin. This multiubiquitin chain is linked to one of two specific Lys residues in βgal. These same Lys residues have been identified by molecular genetic analysis as components of the amino-terminal degradation signal in βgal. The experiments with ubiquitin mutated at its Lys 48 residue indicate that the multiubiquitin chain in a targeted protein is essential for the degradation of the protein.

Bibliography

Chau, V., Tobias, J. W., Bachmair, A., Marriott, D., Ecker, D. J., Gonda, D. K., & Varshavsky, A. (1989). A Multiubiquitin Chain Is Confined to Specific Lysine in a Targeted Short-Lived Protein. Science, 243(4898), 1576â1583.

Authors 7

Vincent Chau (first)
John W. Tobias (additional)
Andreas Bachmair (additional)
David Marriott (additional)
David J. Ecker (additional)
David K. Gonda (additional)
Alexander Varshavsky (additional)

References 39 Referenced 1,199

AEBERSOLD, R.H., INTERNAL AMINO-ACID SEQUENCE-ANALYSIS OF PROTEINS SEPARATED BY ONE-DIMENSIONAL OR TWO-DIMENSIONAL GEL-ELECTROPHORESIS AFTER INSITU PROTEASE DIGESTION ON NITROCELLULOSE, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 84: 6970 (1987). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1987)
ASUBEL F.M. CURRENT PROTOCOLS MO (1987).
10.1016/0092-8674(89)90635-1
10.1126/science.3018930
BALL, E, ARTHRIN, A MYOFIBRILLAR PROTEIN OF INSECT FLIGHT-MUSCLE, IS AN ACTIN UBIQUITIN CONJUGATE, CELL 51: 221 (1987). (10.1016/0092-8674(87)90149-8) / CELL (1987)
BORNSTEIN, P, METHODS IN ENZYMOLOGY 47: 132 (1977). (10.1016/0076-6879(77)47016-2) / METHODS IN ENZYMOLOGY (1977)
CHAU V unpublished data.
CIECHANOVER, A, UBIQUITIN DEPENDENCE OF SELECTIVE PROTEIN-DEGRADATION DEMONSTRATED IN THE MAMMALIAN-CELL CYCLE MUTANT TS85, CELL 37: 57 (1984). (10.1016/0092-8674(84)90300-3) / CELL (1984)
COX, M.J., TRYPTIC PEPTIDE-MAPPING OF UBIQUITIN AND DERIVATIVES USING REVERSE-PHASE HIGH-PERFORMANCE LIQUID-CHROMATOGRAPHY, ANALYTICAL BIOCHEMISTRY 154: 345 (1986). (10.1016/0003-2697(86)90535-X) / ANALYTICAL BIOCHEMISTRY (1986)
ECKER, D.J., CHEMICAL SYNTHESIS AND EXPRESSION OF A CASSETTE ADAPTED UBIQUITIN GENE, JOURNAL OF BIOLOGICAL CHEMISTRY 262: 3524 (1987). (10.1016/S0021-9258(18)61382-1) / JOURNAL OF BIOLOGICAL CHEMISTRY (1987)
ECKER, D.J., GENE SYNTHESIS, EXPRESSION, STRUCTURES, AND FUNCTIONAL ACTIVITIES OF SITE-SPECIFIC MUTANTS OF UBIQUITIN, JOURNAL OF BIOLOGICAL CHEMISTRY 262: 14213 (1987). (10.1016/S0021-9258(18)47925-2) / JOURNAL OF BIOLOGICAL CHEMISTRY (1987)
EDWARDS, L.A., THE USE OF LIMITED PROTEOLYSIS TO PROBE INTERDOMAIN AND ACTIVE-SITE REGIONS OF BETA-GALACTOSIDASE (ESCHERICHIA-COLI), JOURNAL OF BIOLOGICAL CHEMISTRY 263: 1848 (1988). (10.1016/S0021-9258(19)77954-X) / JOURNAL OF BIOLOGICAL CHEMISTRY (1988)
FINLEY, D, THERMOLABILITY OF UBIQUITIN-ACTIVATING ENZYME FROM THE MAMMALIAN-CELL CYCLE MUTANT TS85, CELL 37: 43 (1984). (10.1016/0092-8674(84)90299-X) / CELL (1984)
FINLEY, D, THE YEAST POLYUBIQUITIN GENE IS ESSENTIAL FOR RESISTANCE TO HIGH-TEMPERATURES, STARVATION, AND OTHER STRESSES, CELL 48: 1035 (1987). (10.1016/0092-8674(87)90711-2) / CELL (1987)
FINLEY, D, THE UBIQUITIN SYSTEM - FUNCTIONS AND MECHANISMS, TRENDS IN BIOCHEMICAL SCIENCES 10: 343 (1985). (10.1016/0968-0004(85)90108-2) / TRENDS IN BIOCHEMICAL SCIENCES (1985)
FINLEY, D, UBIQUITIN: 39 (1988). / UBIQUITIN (1988)
GANOTH, D, A MULTICOMPONENT SYSTEM THAT DEGRADES PROTEINS CONJUGATED TO UBIQUITIN - RESOLUTION OF FACTORS AND EVIDENCE FOR ATP-DEPENDENT COMPLEX-FORMATION, JOURNAL OF BIOLOGICAL CHEMISTRY 263: 12412 (1988). (10.1016/S0021-9258(18)37771-8) / JOURNAL OF BIOLOGICAL CHEMISTRY (1988)
10.1126/science.2842867
Gonda, D. K., Journal of Biological Chemistry 264: 16700 (1989). (10.1016/S0021-9258(19)84762-2) / Journal of Biological Chemistry (1989)
GONDA D.K. unpublished data.
HERSHKO, A, OCCURRENCE OF A POLYUBIQUITIN STRUCTURE IN UBIQUITIN-PROTEIN CONJUGATES, BIOCHEMICAL AND BIOPHYSICAL RESEARCH COMMUNICATIONS 128: 1079 (1985). (10.1016/0006-291X(85)91050-2) / BIOCHEMICAL AND BIOPHYSICAL RESEARCH COMMUNICATIONS (1985)
HERSHKO, A, UBIQUITIN-MEDIATED PROTEIN-DEGRADATION, JOURNAL OF BIOLOGICAL CHEMISTRY 263: 15237 (1988). (10.1016/S0021-9258(19)37575-1) / JOURNAL OF BIOLOGICAL CHEMISTRY (1988)
HERSHKO, A, PROPOSED ROLE OF ATP IN PROTEIN BREAKDOWN - CONJUGATION OF PROTEINS WITH MULTIPLE CHAINS OF THE POLYPEPTIDE OF ATP-DEPENDENT PROTEOLYSIS, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES 77: 1783 (1980). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES (1980)
HOUGH, R, UBIQUITIN: 101 (1988). / UBIQUITIN (1988)
JENTSCH, S, THE YEAST DNA-REPAIR GENE RAD6 ENCODES A UBIQUITIN-CONJUGATING ENZYME, NATURE 329: 131 (1987). (10.1038/329131a0) / NATURE (1987)
KANIA, J, FUNCTIONAL REPRESSOR PARTS OF A TETRAMERIC LAC REPRESSOR BETA-GALACTOSIDASE CHIMAERA ARE ORGANIZED AS DIMERS, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 73: 3529 (1976). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1976)
10.1038/227680a0
MESSING, J, GENE 19: 263 (1982). / GENE (1982)
NAGAI, K, SYNTHESIS AND SEQUENCE-SPECIFIC PROTEOLYSIS OF HYBRID PROTEINS PRODUCED IN ESCHERICHIA-COLI, METHODS IN ENZYMOLOGY 153: 461 (1987). (10.1016/0076-6879(87)53072-5) / METHODS IN ENZYMOLOGY (1987)
OZKAYNAK, E, THE YEAST UBIQUITIN GENES - A FAMILY OF NATURAL GENE FUSIONS, EMBO JOURNAL 6: 1429 (1987). (10.1002/j.1460-2075.1987.tb02384.x) / EMBO JOURNAL (1987)
PICKART, C.M., UBIQUITIN CARRIER PROTEIN-CATALYZED UBIQUITIN TRANSFER TO HISTONES - MECHANISM AND SPECIFICITY, JOURNAL OF BIOLOGICAL CHEMISTRY 263: 15076 (1988). (10.1016/S0021-9258(18)68148-7) / JOURNAL OF BIOLOGICAL CHEMISTRY (1988)
PICKART, C.M., UBIQUITIN: 77 (1988). / UBIQUITIN (1988)
SIEGELMAN, M, UBIQUITIN: 239 (1988). / UBIQUITIN (1988)
SILHAVY, T.J., EXPT GENE FUSIONS: 273 (1984). / EXPT GENE FUSIONS (1984)
SWERDLOW, P.S., ENHANCEMENT OF IMMUNOBLOT SENSITIVITY BY HEATING OF HYDRATED FILTERS, ANALYTICAL BIOCHEMISTRY 156: 147 (1986). (10.1016/0003-2697(86)90166-1) / ANALYTICAL BIOCHEMISTRY (1986)
VIJAYKUMAR, S, COMPARISON OF THE 3-DIMENSIONAL STRUCTURES OF HUMAN, YEAST, AND OAT UBIQUITIN, JOURNAL OF BIOLOGICAL CHEMISTRY 262: 6396 (1987). (10.1016/S0021-9258(18)45583-4) / JOURNAL OF BIOLOGICAL CHEMISTRY (1987)
VIJAYKUMAR, S, STRUCTURE OF UBIQUITIN REFINED AT 1.8 A RESOLUTION, JOURNAL OF MOLECULAR BIOLOGY 194: 531 (1987). (10.1016/0022-2836(87)90679-6) / JOURNAL OF MOLECULAR BIOLOGY (1987)
WAXMAN, L, DEMONSTRATION OF 2 DISTINCT HIGH-MOLECULAR-WEIGHT PROTEASES IN RABBIT RETICULOCYTES, ONE OF WHICH DEGRADES UBIQUITIN CONJUGATES, JOURNAL OF BIOLOGICAL CHEMISTRY 262: 2451 (1987). (10.1016/S0021-9258(18)61525-X) / JOURNAL OF BIOLOGICAL CHEMISTRY (1987)
WILKINSON, K.D., UBIQUITIN: 5 (1988). / UBIQUITIN (1988)

Dates

Type	When
Created	18 years, 10 months ago (Oct. 5, 2006, 5:21 p.m.)
Deposited	1 year, 7 months ago (Jan. 12, 2024, 10:08 a.m.)
Indexed	12 hours, 29 minutes ago (Aug. 30, 2025, 1:18 p.m.)
Issued	36 years, 5 months ago (March 24, 1989)
Published	36 years, 5 months ago (March 24, 1989)
Published Print	36 years, 5 months ago (March 24, 1989)

Funders 0

None

BibTeX

@article{Chau_1989, title={A Multiubiquitin Chain Is Confined to Specific Lysine in a Targeted Short-Lived Protein}, volume={243}, ISSN={1095-9203}, url={http://dx.doi.org/10.1126/science.2538923}, DOI={10.1126/science.2538923}, number={4898}, journal={Science}, publisher={American Association for the Advancement of Science (AAAS)}, author={Chau, Vincent and Tobias, John W. and Bachmair, Andreas and Marriott, David and Ecker, David J. and Gonda, David K. and Varshavsky, Alexander}, year={1989}, month=mar, pages={1576–1583} }

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