Proteomic analysis of the mitochondria from embryonic and postnatal rat brains reveals response to developmental changes in energy demands

Journal of Proteomics

Volumn 109, Issue , 2014, Pages 228-239

  Villeneuve, Lance M ^a   Stauch, Kelly L ^a   Fox, Howard S ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

Bioenergetics electron transfer complex; Development; Mitochondria; Neurodegeneration; Oxidative stress

Indexed keywords

MITOCHONDRIAL PROTEIN; DNA BINDING PROTEIN; HIF1A PROTEIN, RAT; HYPOXIA INDUCIBLE FACTOR 1ALPHA; REGULATORY FACTOR X TRANSCRIPTION FACTORS; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ARTICLE; BIOINFORMATICS; BRAIN CELL; BRAIN MITOCHONDRION; GLYCOLYSIS; MASS SPECTROMETRY; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEOMICS; RAT; SPRAGUE DAWLEY RAT; TRANSCRIPTION REGULATION; ANIMAL TISSUE; CELL MIGRATION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; FETUS; MITOCHONDRIAL DYNAMICS; PROTEIN ANALYSIS; PROTEIN EXPRESSION; ANIMAL; BRAIN; EMBRYOLOGY; ENERGY METABOLISM; GENE EXPRESSION REGULATION; METABOLISM; MITOCHONDRION; PC12 CELL LINE; PHYSIOLOGY;

RATTUS;

ANIMALS; BRAIN; DNA-BINDING PROTEINS; ENERGY METABOLISM; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MITOCHONDRIA; PC12 CELLS; PROTEOMICS; RATS; RATS, SPRAGUE-DAWLEY; TRANSCRIPTION FACTORS;

EID: 84905400274     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2014.07.011     Document Type: Article

References (70)

1. Sinha K., Das J., Pal P.B., Sil P.C. Oxidative stress: the mitochondria-dependent and mitochondria-independent pathways of apoptosis. Arch Toxicol 2013, 87:1157-1180.
2. Williams G.S., Boyman L., Chikando A.C., Khairallah R.J., Lederer W.J. Mitochondrial calcium uptake. Proc Natl Acad Sci U S A 2013, 110:10479-10486.
3. Lill R., Hoffmann B., Molik S., Pierik A.J., Rietzschel N., Stehling O., et al. The role of mitochondria in cellular iron-sulfur protein biogenesis and iron metabolism. Biochim Biophys Acta 1823, 2012:1491-1508.
4. Radak Z., Zhao Z., Koltai E., Ohno H., Atalay M. Oxygen consumption and usage during physical exercise: the balance between oxidative stress and ROS-dependent adaptive signaling. Antioxid Redox Signal 2013, 18:1208-1246.
5. Mootha V.K., Bunkenborg J., Olsen J.V., Hjerrild M., Wisniewski J.R., Stahl E., et al. Integrated analysis of protein composition, tissue diversity, and gene regulation in mouse mitochondria. Cell 2003, 115:629-640.
6. Johnson D.T., Harris R.A., French S., Blair P.V., You J., Bemis K.G., et al. Tissue heterogeneity of the mammalian mitochondrial proteome. Am J Physiol Cell Physiol 2007, 292:C689-C697.
7. McClatchy D.B., Liao L., Lee J.H., Park S.K., Yates J.R. Dynamics of subcellular proteomes during brain development. J Proteome Res 2012, 11:2467-2479.
8. Graham J.W., Williams T.C., Morgan M., Fernie A.R., Ratcliffe R.G., Sweetlove L.J. Glycolytic enzymes associate dynamically with mitochondria in response to respiratory demand and support substrate channeling. Plant Cell 2007, 19:3723-3738.
9. Chaturvedi R.K., Flint Beal M. Mitochondrial diseases of the brain. Free Radic Biol Med 2013, 63:1-29.
10. Nakai A., Taniuchi Y., Asakura H., Oya A., Yokota A., Koshino T., et al. Developmental changes in mitochondrial activity and energy metabolism in fetal and neonatal rat brain. Brain Res Dev Brain Res 2000, 121:67-72.
11. Geiger T., Wehner A., Schaab C., Cox J., Mann M. Comparative proteomic analysis of eleven common cell lines reveals ubiquitous but varying expression of most proteins. Mol Cell Proteomics 2012, 11:M111. [014050].
12. Villeneuve L., Tiede L.M., Morsey B., Fox H.S. Quantitative proteomics reveals oxygen-dependent changes in neuronal mitochondria affecting function and sensitivity to rotenone. J Proteome Res 2013, 12:4599-4606.
13. Gillet L.C., Navarro P., Tate S., Rost H., Selevsek N., Reiter L., et al. Targeted data extraction of the MS/MS spectra generated by data-independent acquisition: a new concept for consistent and accurate proteome analysis. Mol Cell Proteomics 2012, 11:O111. [016717].
14. Wisniewski J.R., Zougman A., Nagaraj N., Mann M. Universal sample preparation method for proteome analysis. Nat Methods 2009, 6:359-362.
15. Scopes R. Measurement of protein by spectrophotometry at 205nm. Anal Biochem 1974, 59:277-282.
16. Smith A.C., Blackshaw J.A., Robinson A.J. MitoMiner: a data warehouse for mitochondrial proteomics data. Nucleic Acids Res 2012, 40:D1160-D1167.
17. Homma K., Suzuki K., Sugawara H. The Autophagy Database: an all-inclusive information resource on autophagy that provides nourishment for research. Nucleic Acids Res 2011, 39:D986-D990.
18. Lubke T., Lobel P., Sleat D.E. Proteomics of the lysosome. Biochim Biophys Acta 2009, 1793:625-635.
19. Jovaisaite V., Mouchiroud L., Auwerx J. The mitochondrial unfolded protein response, a conserved stress response pathway with implications in health and disease. J Exp Biol 2014, 217:137-143.
20. Zhang W., Zhang Y., Zheng H., Zhang C., Xiong W., Olyarchuk J.G., et al. SynDB: a Synapse protein DataBase based on synapse ontology. Nucleic Acids Res 2007, 35:D737-D741.
21. Saeed A.I., Sharov V., White J., Li J., Liang W., Bhagabati N., et al. TM4: a free, open-source system for microarray data management and analysis. Biotechniques 2003, 34:374-378.
22. Huang da W., Sherman B.T., Lempicki R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009, 4:44-57.
23. Kramer A., Green J., Pollard J., Tugendreich S. Causal analysis approaches in Ingenuity Pathway Analysis. Bioinformatics 2014, 30:523-530.
24. Bandeira F., Lent R., Herculano-Houzel S. Changing numbers of neuronal and non-neuronal cells underlie postnatal brain growth in the rat. Proc Natl Acad Sci U S A 2009, 106:14108-14113.
25. Chan N.C., Salazar A.M., Pham A.H., Sweredoski M.J., Kolawa N.J., Graham R.L., et al. Broad activation of the ubiquitin-proteasome system by Parkin is critical for mitophagy. Hum Mol Genet 2011, 20:1726-1737.
26. Zhou Q., Petersen C.C., Nicoll R.A. Effects of reduced vesicular filling on synaptic transmission in rat hippocampal neurones. J Physiol 2000, 525(Pt 1):195-206.
27. Hiesinger P.R., Fayyazuddin A., Mehta S.Q., Rosenmund T., Schulze K.L., Zhai R.G., et al. The v-ATPase V0 subunit a1 is required for a late step in synaptic vesicle exocytosis in Drosophila. Cell 2005, 121:607-620.
28. Poea-Guyon S., Amar M., Fossier P., Morel N. Alternative splicing controls neuronal expression of v-ATPase subunit a1 and sorting to nerve terminals. J Biol Chem 2006, 281:17164-17172.
29. Broccardo C., Nieoullon V., Amin R., Masmejean F., Carta S., Tassi S., et al. ABCA2 is a marker of neural progenitors and neuronal subsets in the adult rodent brain. J Neurochem 2006, 97:345-355.
30. Martinelli P., Rugarli E.I. Emerging roles of mitochondrial proteases in neurodegeneration. Biochim Biophys Acta 2010, 1797:1-10.
31. He Y., Sun S., Sha H., Liu Z., Yang L., Xue Z., et al. Emerging roles for XBP1, a sUPeR transcription factor. Gene Expr 2010, 15:13-25.
32. Schindler A., Foley E. Hexokinase 1 blocks apoptotic signals at the mitochondria. Cell Signal 2013, 25:2685-2692.
33. Majewski N., Nogueira V., Bhaskar P., Coy P.E., Skeen J.E., Gottlob K., et al. Hexokinase-mitochondria interaction mediated by Akt is required to inhibit apoptosis in the presence or absence of Bax and Bak. Mol Cell 2004, 16:819-830.
34. Giege P., Heazlewood J.L., Roessner-Tunali U., Millar A.H., Fernie A.R., Leaver C.J., et al. Enzymes of glycolysis are functionally associated with the mitochondrion in Arabidopsis cells. Plant Cell 2003, 15:2140-2151.
35. Goyal M.S., Hawrylycz M., Miller J.A., Snyder A.Z., Raichle M.E. Aerobic glycolysis in the human brain is associated with development and neotenous gene expression. Cell Metab 2014, 19:49-57.
36. Van Eden C.G., Kros J.M., Uylings H.B. The development of the rat prefrontal cortex. Its size and development of connections with thalamus, spinal cord and other cortical areas. Prog Brain Res 1990, 85:169-183.
37. Eayrs J.T., Goodhead B. Postnatal development of the cerebral cortex in rats. J Anat 1959, 93:385-402.
38. Altman J. Proliferation and migration of undifferentiated precursor cells in the rat during postnatal gliogenesis. Exp Neurol 1966, 16:263-278.
39. Bass N.H., Netsky M.G., Young E. Effects of neonatal malnutrition on developing cerebrum: I. Microchemical and histologic study of cellular differentiation in the rat. Arch Neurol 1970, 23:289-302.
40. Vahsen N., Cande C., Briere J.J., Benit P., Joza N., Larochette N., et al. AIF deficiency compromises oxidative phosphorylation. EMBO J 2004, 23:4679-4689.
41. Apostolova N., Cervera A.M., Victor V.M., Cadenas S., Sanjuan-Pla A., Alvarez-Barrientos A., et al. Loss of apoptosis-inducing factor leads to an increase in reactive oxygen species, and an impairment of respiration that can be reversed by antioxidants. Cell Death Differ 2006, 13:354-357.
42. Artus C., Boujrad H., Bouharrour A., Brunelle M.N., Hoos S., Yuste V.J., et al. AIF promotes chromatinolysis and caspase-independent programmed necrosis by interacting with histone H2AX. EMBO J 2010, 29:1585-1599.
43. Cipolat S., Martins de Brito O., Dal Zilio B., Scorrano L. OPA1 requires mitofusin 1 to promote mitochondrial fusion. Proc Natl Acad Sci U S A 2004, 101:15927-15932.
44. Frank M., Duvezin-Caubet S., Koob S., Occhipinti A., Jagasia R., Petcherski A., et al. Mitophagy is triggered by mild oxidative stress in a mitochondrial fission dependent manner. Biochim Biophys Acta 1823, 2012:2297-2310.
45. Ishihara N., Nomura M., Jofuku A., Kato H., Suzuki S.O., Masuda K., et al. Mitochondrial fission factor Drp1 is essential for embryonic development and synapse formation in mice. Nat Cell Biol 2009, 11:958-966.
46. Mao K., Wang K., Liu X., Klionsky D.J. The scaffold protein Atg11 recruits fission machinery to drive selective mitochondria degradation by autophagy. Dev Cell 2013, 26:9-18.
47. Boumil R.M., Letts V.A., Roberts M.C., Lenz C., Mahaffey C.L., Zhang Z.W., et al. A missense mutation in a highly conserved alternate exon of dynamin-1 causes epilepsy in fitful mice. PLoS Genet 2010, 6.
48. Tondera D., Czauderna F., Paulick K., Schwarzer R., Kaufmann J., Santel A. The mitochondrial protein MTP18 contributes to mitochondrial fission in mammalian cells. J Cell Sci 2005, 118:3049-3059.
49. Hoppins S., Lackner L., Nunnari J. The machines that divide and fuse mitochondria. Annu Rev Biochem 2007, 76:751-780.
50. Verstreken P., Ly C.V., Venken K.J., Koh T.W., Zhou Y., Bellen H.J. Synaptic mitochondria are critical for mobilization of reserve pool vesicles at Drosophila neuromuscular junctions. Neuron 2005, 47:365-378.
51. Noda N.N., Ohsumi Y., Inagaki F. Atg8-family interacting motif crucial for selective autophagy. FEBS Lett 2010, 584:1379-1385.
52. Hediger M.A., Romero M.F., Peng J.B., Rolfs A., Takanaga H., Bruford E.A. The ABCs of solute carriers: physiological, pathological and therapeutic implications of human membrane transport proteins: Introduction. Pflugers Arch 2004, 447:465-468.
53. Parsons S.M. Transport mechanisms in acetylcholine and monoamine storage. FASEB J 2000, 14:2423-2434.
54. Eayrs J.T., Goodhead B. Postnatal development of the cerebral cortex in the rat. J Anat 1959, 93:385-402.
55. Matsuzaki M., Honkura N., Ellis-Davies G.C., Kasai H. Structural basis of long-term potentiation in single dendritic spines. Nature 2004, 429:761-766.
56. Harms K.J., Rioult-Pedotti M.S., Carter D.R., Dunaevsky A. Transient spine expansion and learning-induced plasticity in layer 1 primary motor cortex. J Neurosci 2008, 28:5686-5690.
57. Knott G.W., Holtmaat A., Wilbrecht L., Welker E., Svoboda K. Spine growth precedes synapse formation in the adult neocortex in vivo. Nat Neurosci 2006, 9:1117-1124.
58. 2+ signaling. Nat Neurosci 2013, 16:1409-1416.
59. Lozada A.F., Wang X., Gounko N.V., Massey K.A., Duan J., Liu Z., et al. Glutamatergic synapse formation is promoted by alpha7-containing nicotinic acetylcholine receptors. J Neurosci 2012, 32:7651-7661.
60. Xu Y., Ren X.C., Quinn C.C., Wadsworth W.G. Axon response to guidance cues is stimulated by acetylcholine in Caenorhabditis elegans. Genetics 2011, 189:899-906.
61. Tatsuta T., Langer T. Quality control of mitochondria: protection against neurodegeneration and ageing. EMBO J 2008, 27:306-314.
62. 2 homeostasis by hypoxia-inducible factor 1 alpha. Genes Dev 1998, 12:149-162.
63. DeBerardinis R.J., Lum J.J., Hatzivassiliou G., Thompson C.B. The biology of cancer: metabolic reprogramming fuels cell growth and proliferation. Cell Metab 2008, 7:11-20.
64. Lopez-Campistrous A., Fernandez-Patron C. Proteomic analysis of brain mitochondrial proteome and mitochondrial complexes. Methods Mol Biol 2013, 1005:129-141.
65. Fang X., Lee C.S. Proteome characterization of mouse brain mitochondria using electrospray ionization tandem mass spectrometry. Methods Enzymol 2009, 457:49-62.
66. Lotz C., Lin A.J., Black C.M., Zhang J., Lau E., Deng N., et al. Characterization, design, and function of the mitochondrial proteome: from organs to organisms. J Proteome Res 2014, 13:433-446.
67. Buneeva O.A., Medvedeva M.V., Kopylov A.T., Zgoda V.G., Medvedev A.E. Use of biotinylated ubiquitin for analysis of rat brain mitochondrial proteome and interactome. Int J Mol Sci 2012, 13:11593-11609.
68. Still A.J., Floyd B.J., Hebert A.S., Bingman C.A., Carson J.J., Gunderson D.R., et al. Quantification of mitochondrial acetylation dynamics highlights prominent sites of metabolic regulation. J Biol Chem 2013, 288:26209-26219.
69. Zhao X., Bak S., Pedersen A.J., Jensen O.N., Hojlund K. Insulin increases phosphorylation of mitochondrial proteins in human skeletal muscle in vivo. J Proteome Res 2014, 13(5):2359-2369.
70. Aebersold R., Burlingame A.L., Bradshaw R.A. Western blots versus selected reaction monitoring assays: time to turn the tables?. Mol Cell Proteomics 2013, 12:2381-2382.