Tissue heterogeneity of the mammalian mitochondrial proteome

D. Thor Johnson, Robert Harris, Stephanie French, Paul V. Blair, Jinsam You, Kerry G. Bemis, Mu Wang, Robert S. Balaban

Research output: Contribution to journalArticle

131 Citations (Scopus)

Abstract

The functionality of the mitochondrion is primarily determined by nuclear encoded proteins. The mitochondrial functional requirements of different tissues vary from a significant biosynthetic role (liver) to a primarily energy metabolism-oriented organelle (heart). The purpose of this study was to compare the mitochondrial proteome from four different tissues of the rat, brain, liver, heart, and kidney, to provide insight into the extent of mitochondrial heterogeneity and to further characterize the overall mitochondrial proteome. Mitochondria were isolated, solubilized, digested, and subjected to quantitative liquid chromatography-mass spectroscopy. Of the 16,950 distinct peptides detected, 8,045 proteins were identified. High-confidence identification threshold was reached by 1,162 peptides, which were further analyzed. Of these 1,162 proteins, 1,149 were significantly different in content (P and q values < 0.05) between at least 2 tissues, whereas 13 were not significantly different between any tissues. Confirmation of the mitochondrial origin of proteins was determined from the literature or via NH2-terminal mitochondrial localization signals. With these criteria, 382 proteins in the significantly different groups were confirmed to be mitochondrial, and 493 could not be confirmed to be mitochondrial but were not definitively localized elsewhere in the cell. A total of 145 proteins were assigned to the rat mitochondrial proteome for the first time via their NH2-terminal mitochondrial localization signals. Among the proteins that were not significantly different between tissues, three were confirmed to be mitochondrial. Most notable of the signifi-cantly different proteins were histone family proteins and several structural proteins, including tubulin and intermediate filaments. The mitochondrial proteome from each tissue had very specific characteristics indicative of different functional emphasis. These data confirm the notion that mitochondria are tuned by the nucleus for specific functions in different tissues.

Original languageEnglish
JournalAmerican Journal of Physiology - Cell Physiology
Volume292
Issue number2
DOIs
StatePublished - Feb 2007

Fingerprint

Proteome
Tissue
Proteins
Mitochondria
Liver
Rats
Peptides
Intermediate Filaments
Mitochondrial Proteins
Tubulin
Nuclear Proteins
Liquid chromatography
Liquid Chromatography
Organelles
Histones
Energy Metabolism
Mass Spectrometry
Brain
Kidney
Spectroscopy

Keywords

  • Brain
  • Electrophoresis
  • Heart
  • Histone
  • Kidney
  • Liquid chromatography
  • Liver
  • Mass spectrometry
  • Oxidative phosphorylation
  • Structural proteins

ASJC Scopus subject areas

  • Clinical Biochemistry
  • Cell Biology
  • Physiology

Cite this

Tissue heterogeneity of the mammalian mitochondrial proteome. / Johnson, D. Thor; Harris, Robert; French, Stephanie; Blair, Paul V.; You, Jinsam; Bemis, Kerry G.; Wang, Mu; Balaban, Robert S.

In: American Journal of Physiology - Cell Physiology, Vol. 292, No. 2, 02.2007.

Research output: Contribution to journalArticle

Johnson, D. Thor ; Harris, Robert ; French, Stephanie ; Blair, Paul V. ; You, Jinsam ; Bemis, Kerry G. ; Wang, Mu ; Balaban, Robert S. / Tissue heterogeneity of the mammalian mitochondrial proteome. In: American Journal of Physiology - Cell Physiology. 2007 ; Vol. 292, No. 2.
@article{3df4e38d98094498b37a449d86f6f642,
title = "Tissue heterogeneity of the mammalian mitochondrial proteome",
abstract = "The functionality of the mitochondrion is primarily determined by nuclear encoded proteins. The mitochondrial functional requirements of different tissues vary from a significant biosynthetic role (liver) to a primarily energy metabolism-oriented organelle (heart). The purpose of this study was to compare the mitochondrial proteome from four different tissues of the rat, brain, liver, heart, and kidney, to provide insight into the extent of mitochondrial heterogeneity and to further characterize the overall mitochondrial proteome. Mitochondria were isolated, solubilized, digested, and subjected to quantitative liquid chromatography-mass spectroscopy. Of the 16,950 distinct peptides detected, 8,045 proteins were identified. High-confidence identification threshold was reached by 1,162 peptides, which were further analyzed. Of these 1,162 proteins, 1,149 were significantly different in content (P and q values < 0.05) between at least 2 tissues, whereas 13 were not significantly different between any tissues. Confirmation of the mitochondrial origin of proteins was determined from the literature or via NH2-terminal mitochondrial localization signals. With these criteria, 382 proteins in the significantly different groups were confirmed to be mitochondrial, and 493 could not be confirmed to be mitochondrial but were not definitively localized elsewhere in the cell. A total of 145 proteins were assigned to the rat mitochondrial proteome for the first time via their NH2-terminal mitochondrial localization signals. Among the proteins that were not significantly different between tissues, three were confirmed to be mitochondrial. Most notable of the signifi-cantly different proteins were histone family proteins and several structural proteins, including tubulin and intermediate filaments. The mitochondrial proteome from each tissue had very specific characteristics indicative of different functional emphasis. These data confirm the notion that mitochondria are tuned by the nucleus for specific functions in different tissues.",
keywords = "Brain, Electrophoresis, Heart, Histone, Kidney, Liquid chromatography, Liver, Mass spectrometry, Oxidative phosphorylation, Structural proteins",
author = "Johnson, {D. Thor} and Robert Harris and Stephanie French and Blair, {Paul V.} and Jinsam You and Bemis, {Kerry G.} and Mu Wang and Balaban, {Robert S.}",
year = "2007",
month = "2",
doi = "10.1152/ajpcell.00108.2006",
language = "English",
volume = "292",
journal = "American Journal of Physiology",
issn = "0193-1857",
publisher = "American Physiological Society",
number = "2",

}

TY - JOUR

T1 - Tissue heterogeneity of the mammalian mitochondrial proteome

AU - Johnson, D. Thor

AU - Harris, Robert

AU - French, Stephanie

AU - Blair, Paul V.

AU - You, Jinsam

AU - Bemis, Kerry G.

AU - Wang, Mu

AU - Balaban, Robert S.

PY - 2007/2

Y1 - 2007/2

N2 - The functionality of the mitochondrion is primarily determined by nuclear encoded proteins. The mitochondrial functional requirements of different tissues vary from a significant biosynthetic role (liver) to a primarily energy metabolism-oriented organelle (heart). The purpose of this study was to compare the mitochondrial proteome from four different tissues of the rat, brain, liver, heart, and kidney, to provide insight into the extent of mitochondrial heterogeneity and to further characterize the overall mitochondrial proteome. Mitochondria were isolated, solubilized, digested, and subjected to quantitative liquid chromatography-mass spectroscopy. Of the 16,950 distinct peptides detected, 8,045 proteins were identified. High-confidence identification threshold was reached by 1,162 peptides, which were further analyzed. Of these 1,162 proteins, 1,149 were significantly different in content (P and q values < 0.05) between at least 2 tissues, whereas 13 were not significantly different between any tissues. Confirmation of the mitochondrial origin of proteins was determined from the literature or via NH2-terminal mitochondrial localization signals. With these criteria, 382 proteins in the significantly different groups were confirmed to be mitochondrial, and 493 could not be confirmed to be mitochondrial but were not definitively localized elsewhere in the cell. A total of 145 proteins were assigned to the rat mitochondrial proteome for the first time via their NH2-terminal mitochondrial localization signals. Among the proteins that were not significantly different between tissues, three were confirmed to be mitochondrial. Most notable of the signifi-cantly different proteins were histone family proteins and several structural proteins, including tubulin and intermediate filaments. The mitochondrial proteome from each tissue had very specific characteristics indicative of different functional emphasis. These data confirm the notion that mitochondria are tuned by the nucleus for specific functions in different tissues.

AB - The functionality of the mitochondrion is primarily determined by nuclear encoded proteins. The mitochondrial functional requirements of different tissues vary from a significant biosynthetic role (liver) to a primarily energy metabolism-oriented organelle (heart). The purpose of this study was to compare the mitochondrial proteome from four different tissues of the rat, brain, liver, heart, and kidney, to provide insight into the extent of mitochondrial heterogeneity and to further characterize the overall mitochondrial proteome. Mitochondria were isolated, solubilized, digested, and subjected to quantitative liquid chromatography-mass spectroscopy. Of the 16,950 distinct peptides detected, 8,045 proteins were identified. High-confidence identification threshold was reached by 1,162 peptides, which were further analyzed. Of these 1,162 proteins, 1,149 were significantly different in content (P and q values < 0.05) between at least 2 tissues, whereas 13 were not significantly different between any tissues. Confirmation of the mitochondrial origin of proteins was determined from the literature or via NH2-terminal mitochondrial localization signals. With these criteria, 382 proteins in the significantly different groups were confirmed to be mitochondrial, and 493 could not be confirmed to be mitochondrial but were not definitively localized elsewhere in the cell. A total of 145 proteins were assigned to the rat mitochondrial proteome for the first time via their NH2-terminal mitochondrial localization signals. Among the proteins that were not significantly different between tissues, three were confirmed to be mitochondrial. Most notable of the signifi-cantly different proteins were histone family proteins and several structural proteins, including tubulin and intermediate filaments. The mitochondrial proteome from each tissue had very specific characteristics indicative of different functional emphasis. These data confirm the notion that mitochondria are tuned by the nucleus for specific functions in different tissues.

KW - Brain

KW - Electrophoresis

KW - Heart

KW - Histone

KW - Kidney

KW - Liquid chromatography

KW - Liver

KW - Mass spectrometry

KW - Oxidative phosphorylation

KW - Structural proteins

UR - http://www.scopus.com/inward/record.url?scp=33847084336&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=33847084336&partnerID=8YFLogxK

U2 - 10.1152/ajpcell.00108.2006

DO - 10.1152/ajpcell.00108.2006

M3 - Article

C2 - 16928776

AN - SCOPUS:33847084336

VL - 292

JO - American Journal of Physiology

JF - American Journal of Physiology

SN - 0193-1857

IS - 2

ER -