Widespread reorganization of metabolic enzymes into reversible assemblies upon nutrient starvation

Rammohan Narayanaswamy, Matthew Levy, Mark Tsechansky, Gwendolyn M. Stovall, Jeremy D. O'Connell, Jennifer Mirrielees, Andrew D. Ellington, Edward M. Marcotte

Research output: Contribution to journalArticle

181 Citations (Scopus)

Abstract

Proteins are likely to organize into complexes that assemble and disassemble depending on cellular needs. When ≈800 yeast strains expressing GFP-tagged proteins were grown to stationary phase, a surprising number of proteins involved in intermediary metabolism and stress response were observed to form punctate cytoplasmic foci. The formation of these discrete physical structures was confirmed by immunofluorescence and mass spectrometry of untagged proteins. The purine biosynthetic enzyme Ade4-GFP formed foci in the absence of adenine, and cycling between punctate and diffuse phenotypes could be controlled by adenine subtraction and addition. Similarly, glutamine synthetase (Gln1-GFP) foci cycled reversibly in the absence and presence of glucose. The structures were neither targeted for vacuolar or autophagosome degradation nor colocalized with P bodies or major organelles. Thus, upon nutrient depletion we observe widespread protein assemblies displaying nutrient-specific formation and dissolution.

Original languageEnglish (US)
Pages (from-to)10147-10152
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume106
Issue number25
DOIs
StatePublished - Jun 23 2009

Fingerprint

Starvation
Food
Enzymes
Adenine
Proteins
Glutamate-Ammonia Ligase
Organelles
Fluorescent Antibody Technique
Mass Spectrometry
Yeasts
Phenotype
Glucose

Keywords

  • Aggregation
  • Metabolism
  • Microscopy
  • Proteomics
  • Quiescence

ASJC Scopus subject areas

  • General

Cite this

Narayanaswamy, R., Levy, M., Tsechansky, M., Stovall, G. M., O'Connell, J. D., Mirrielees, J., ... Marcotte, E. M. (2009). Widespread reorganization of metabolic enzymes into reversible assemblies upon nutrient starvation. Proceedings of the National Academy of Sciences of the United States of America, 106(25), 10147-10152. https://doi.org/10.1073/pnas.0812771106

Widespread reorganization of metabolic enzymes into reversible assemblies upon nutrient starvation. / Narayanaswamy, Rammohan; Levy, Matthew; Tsechansky, Mark; Stovall, Gwendolyn M.; O'Connell, Jeremy D.; Mirrielees, Jennifer; Ellington, Andrew D.; Marcotte, Edward M.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 106, No. 25, 23.06.2009, p. 10147-10152.

Research output: Contribution to journalArticle

Narayanaswamy, R, Levy, M, Tsechansky, M, Stovall, GM, O'Connell, JD, Mirrielees, J, Ellington, AD & Marcotte, EM 2009, 'Widespread reorganization of metabolic enzymes into reversible assemblies upon nutrient starvation', Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 25, pp. 10147-10152. https://doi.org/10.1073/pnas.0812771106
Narayanaswamy, Rammohan ; Levy, Matthew ; Tsechansky, Mark ; Stovall, Gwendolyn M. ; O'Connell, Jeremy D. ; Mirrielees, Jennifer ; Ellington, Andrew D. ; Marcotte, Edward M. / Widespread reorganization of metabolic enzymes into reversible assemblies upon nutrient starvation. In: Proceedings of the National Academy of Sciences of the United States of America. 2009 ; Vol. 106, No. 25. pp. 10147-10152.
@article{c91bb7895f824ba1993506e4775cf0e0,
title = "Widespread reorganization of metabolic enzymes into reversible assemblies upon nutrient starvation",
abstract = "Proteins are likely to organize into complexes that assemble and disassemble depending on cellular needs. When ≈800 yeast strains expressing GFP-tagged proteins were grown to stationary phase, a surprising number of proteins involved in intermediary metabolism and stress response were observed to form punctate cytoplasmic foci. The formation of these discrete physical structures was confirmed by immunofluorescence and mass spectrometry of untagged proteins. The purine biosynthetic enzyme Ade4-GFP formed foci in the absence of adenine, and cycling between punctate and diffuse phenotypes could be controlled by adenine subtraction and addition. Similarly, glutamine synthetase (Gln1-GFP) foci cycled reversibly in the absence and presence of glucose. The structures were neither targeted for vacuolar or autophagosome degradation nor colocalized with P bodies or major organelles. Thus, upon nutrient depletion we observe widespread protein assemblies displaying nutrient-specific formation and dissolution.",
keywords = "Aggregation, Metabolism, Microscopy, Proteomics, Quiescence",
author = "Rammohan Narayanaswamy and Matthew Levy and Mark Tsechansky and Stovall, {Gwendolyn M.} and O'Connell, {Jeremy D.} and Jennifer Mirrielees and Ellington, {Andrew D.} and Marcotte, {Edward M.}",
year = "2009",
month = "6",
day = "23",
doi = "10.1073/pnas.0812771106",
language = "English (US)",
volume = "106",
pages = "10147--10152",
journal = "Proceedings of the National Academy of Sciences of the United States of America",
issn = "0027-8424",
number = "25",

}

TY - JOUR

T1 - Widespread reorganization of metabolic enzymes into reversible assemblies upon nutrient starvation

AU - Narayanaswamy, Rammohan

AU - Levy, Matthew

AU - Tsechansky, Mark

AU - Stovall, Gwendolyn M.

AU - O'Connell, Jeremy D.

AU - Mirrielees, Jennifer

AU - Ellington, Andrew D.

AU - Marcotte, Edward M.

PY - 2009/6/23

Y1 - 2009/6/23

N2 - Proteins are likely to organize into complexes that assemble and disassemble depending on cellular needs. When ≈800 yeast strains expressing GFP-tagged proteins were grown to stationary phase, a surprising number of proteins involved in intermediary metabolism and stress response were observed to form punctate cytoplasmic foci. The formation of these discrete physical structures was confirmed by immunofluorescence and mass spectrometry of untagged proteins. The purine biosynthetic enzyme Ade4-GFP formed foci in the absence of adenine, and cycling between punctate and diffuse phenotypes could be controlled by adenine subtraction and addition. Similarly, glutamine synthetase (Gln1-GFP) foci cycled reversibly in the absence and presence of glucose. The structures were neither targeted for vacuolar or autophagosome degradation nor colocalized with P bodies or major organelles. Thus, upon nutrient depletion we observe widespread protein assemblies displaying nutrient-specific formation and dissolution.

AB - Proteins are likely to organize into complexes that assemble and disassemble depending on cellular needs. When ≈800 yeast strains expressing GFP-tagged proteins were grown to stationary phase, a surprising number of proteins involved in intermediary metabolism and stress response were observed to form punctate cytoplasmic foci. The formation of these discrete physical structures was confirmed by immunofluorescence and mass spectrometry of untagged proteins. The purine biosynthetic enzyme Ade4-GFP formed foci in the absence of adenine, and cycling between punctate and diffuse phenotypes could be controlled by adenine subtraction and addition. Similarly, glutamine synthetase (Gln1-GFP) foci cycled reversibly in the absence and presence of glucose. The structures were neither targeted for vacuolar or autophagosome degradation nor colocalized with P bodies or major organelles. Thus, upon nutrient depletion we observe widespread protein assemblies displaying nutrient-specific formation and dissolution.

KW - Aggregation

KW - Metabolism

KW - Microscopy

KW - Proteomics

KW - Quiescence

UR - http://www.scopus.com/inward/record.url?scp=67649875630&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=67649875630&partnerID=8YFLogxK

U2 - 10.1073/pnas.0812771106

DO - 10.1073/pnas.0812771106

M3 - Article

VL - 106

SP - 10147

EP - 10152

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 25

ER -