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The Epigenome and the Mitochondrion: Bioenergetics and the Environment

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The Epigenome and the Mitochondrion: Bioenergetics and the Environment Downloaded from genesdev.cshlp.org on October 3, 2021 - Published by Cold Spring Harbor Laboratory Press PERSPECTIVE The epigenome and the mitochondrion: bioenergetics and the environment Douglas C. Wallace1 Center for Mitochondrial and Epigenomic Medicine, Children’s Hospital of Philadelphia, Philadelphia, Pennsylvania 19104, USA, and The Department of Pathology and Laboratory Medicine, University of Pennsylvania, Philadelphia, Pennsylvania 19104, USA In the July 15, 2010, issue of Genes & Development, tained from dietary carbohydrates and fatty acids. The Yoon and colleagues (pp. 1507–1518) report that, in a degradation of carbohydrates proceeds through glycolysis siRNA knockdown survey of 6363 genes in mouse to pyruvate. Pyruvate then enters the mitochondrion via C2C12 cells, they discovered 150 genes that regulated pyruvate dehydrogenase to generate NADH + H+ and mitochondrial biogenesis and bioenergetics. Many of acetyl-coenzyme A (acetyl-CoA). Acetyl-CoA proceeds these genes have been studied previously for their im- to the tricarboxylic acid (TCA) cycle, which strips the portance in regulating transcription, protein and nucleic hydrogens from the resulting hydrocarbons and transfers acid modification, and signal transduction. Some notable them to the electron carriers NAD+ and FAD. Fatty acids examples include Brac1, Brac2, Pax4, Sin3A, Fyn, Fes, are degraded in the mitochondrion by b-oxidation, a pro- Map2k7, Map3k2, calmodulin 3, Camk1, Ube3a, and cess that generates NADH + H+, acetyl-CoA, and reduced Wnt. Yoon and colleagues go on to validate their obser- electron transfer flavoprotein (ETF). The electrons from vations by extensively documenting the role of Wnt reduced ETF are transferred to coenzyme Q (CoQ) via the signaling in the regulation of mitochondrial function. ETF dehydrogenase. CoQ is an electron carrier within the mitochondrial inner membrane that accepts two electrons from NADH + H+ via NADH dehydrogenase (respiratory complex I) or reduced flavoprotein dehydro- The discovery that many ‘‘developmental’’ and ‘‘cancer’’ genases such as ETF dehydrogenase or succinate dehy- genes modify mitochondrial function will undoubtedly drogenase (complex II) and passes them on to the bc1 come as a surprise to some readers of Genes & Develop- complex (complex III). From complex III, the electrons are ment. Development is traditionally considered an anatom- transferred to cytochrome c, then to cytochrome c oxidase ical issue involving the ordered proliferation and differen- (complex IV), and finally to oxygen to generate water. The tiation of cells to generate tissues and organs, programmed energy released as the electrons traverse complexes I, III, by the differential expression of nuclear DNA (nDNA)- and IV is used to pump positive charges—protons—out of encoded genes. What does the mitochondrion have to do the mitochondrion to generate an electrochemical gradi- with this? ent across the mitochondrial inner membrane. The inner Development requires cell growth and reproduction, membrane gradient is positive and acidic on the outside, both of which are limited by the availability of energy. and negative and alkaline on the inside. The resulting Thus, caloric energy is an important factor in the cellular electrical field is enormous, involving a membrane poten- environment that can influence cellular gene expression, tial of about À180 mV separated by the thickness of the DNA replication, growth, proliferation, differentiation, mitochondrial inner membrane. This capacitance within and even programmed death. the ;1017 mitochondria in the human body powers our Usable energy is generated from dietary calories pri- lives. marily via the mitochondrion. Therefore, mitochondrial One use of this mitochondrial potential energy is to energy production is essential for all cellular processes, generate ATP via the mitochondrial ATP synthase (com- and regulation of gene expression for growth and differ- plex V). Protons traverse an inner membrane proton entiation must be coordinated with regulation of mito- channel within this rotary machine to drive the conden- chondrial bioenergetics. sation of ADP and phosphate (Pi) to ATP. Mitochondria generate energy by the oxidation of the From this simple summary of mitochondrial bioener- electrons from hydrogen—reducing equivalents—by a re- getics, it is immediately clear that fluctuations in the action with oxygen. The reducing equivalents are ob- availability of calories for the cell must result in fluctu- ations in the intracellular concentrations of the mito- [Keywords: RNAi screen; mitochondria; Wnt signaling; IRS-1] chondrially generated intermediates acetyl-CoA and 1Correspondence. E-MAIL [email protected]; FAX (949) 824-6388. ATP. Electron flow through the mitochondrion also Article is online at http://www.genesdev.org/cgi/doi/10.1101/gad.1960210. modulates the redox status of small molecules such as GENES & DEVELOPMENT 24:1571–1573 Ó 2010 by Cold Spring Harbor Laboratory Press ISSN 0890-9369/10; www.genesdev.org 1571 Downloaded from genesdev.cshlp.org on October 3, 2021 - Published by Cold Spring Harbor Laboratory Press Wallace NAD(P)+/NAD(P)H + H+, glutathione, and other thiol/ maintain the integrated circuit. This is achieved by disulfide couples, and of the thiol/disulfide status, and placing the key electrical wiring elements on the same thus the activity of many enzymes and transcription fac- piece of nonrecombining DNA: the mtDNA. Therefore, tors (Hansen et al. 2006; Kemp et al. 2008; Wallace et al. each new mtDNA mutation that arises occurs on a pre- 2010). existing background of functional variants, and the entire ATP is the coreactant in virtually every signal trans- system is acted on by natural selection as a unit. Unipa- duction pathway, as well as histone phosphorylation. rental inheritance then blocks the mixing of mtDNAs Acetyl-CoA is the coreactant for the acetylation of from different maternal lineages, and thus the exchange histones as well as many other proteins. With phosphor- of circuit components from mtDNAs that are optimized ylation or acetylation, histone tails are converted from for different energetic environments. Consequently, positively charged to negatively charged, resulting in mtDNA lineages can only evolve by the sequential their repulsion from the DNA sugar–phosphate back- accumulation of functional variants along radiating ma- bone. This opens the chromatin, permitting transcription ternal lineages, with each branch of the tree becoming and replication. Thus, to a first-order approximation, optimized to cope with differences in the energetic when calories are abundant, chromatin is phosphory- characteristics of the various regions of the species’ niche. lated, acetylated, and decondensed; genes are expressed; In addition to the mtDNA genes, the mitochondrial and the cell grows and proliferates. When calories are genome encompasses hundreds if not thousands of scarce, the chromatin becomes dephosphorylated and nDNA genes. The nDNA-encoded bioenergetic genes deacetylated and condenses; gene expression subsides; determine the mitochondrion’s structure, replication, and the cell ceases growth until calories again become biogenesis, fission and fusion equilibriums, mitophagy prevalent (Wallace and Fan 2010). turnover rate, intracellular quantity, etc. These genes are Similarly, the redox status of NAD+/NADH + H+ reg- scattered across the chromosomes, yet need to be co- ulates the deacetylation activity of Sirt1, and the redox ordinately regulated to permit optimal energy production. status of NADPH+/NADPH + H+ regulates the redox Unlike mtDNA genes, the anatomical and develop- state of glutathione and the antioxidant defenses. The mental genes found in the nDNA can benefit from NADPH+/NADPH + H+ ratio also regulates the redox recombination. Reassortment of anatomical genes can status of thioredoxins 1 and 2, and of apurinic/apyrimi- lead to new structures. These modified structures may dinic endonuclease/redox factor-1 (APE/Ref1red/ox). The then permit the exploitation of alternative reservoirs of thioredoxin and APE/Ref1red/ox proteins in turn regulate calories within the biosphere, resulting in speciation. the thiol/disulfide status and the activity of a wide variety The mutation rate of the mtDNA is very high, while of proteins, including many of the central transcription that of the nDNA is very low. The high mutation rate of factors for growth, differentiation, antioxidant defenses, the mtDNA, with its vital genes, is potentially quite and inflammation. Hence, there is a direct link between hazardous, since it could result in a high genetic load of the availability of calories in the environment and the deleterious mutations that could erode the vitality of the decision to grow and reproduce, as mediated by the flux species. This problem is ameliorated by the existence of reducing equivalents through the mitochondrion of an intraovarian selection system that eliminates the (Wallace 2009; Wallace and Fan 2010; Wallace et al. 2010). most deleterious mtDNA mutations before ovulation. While the genes for determining the structure of the cell Hence, only the milder and potentially adaptive muta- and the spatial and temporal programs for defining tissue tions are introduced into the population (Fan et al. and organ development are encoded by the Mendelian- 2008; Stewart et al. 2008). This prefertilization selection inherited nDNA, which is encased in chromatin, the key is possible for the mitochondrial genes because energy components for the mitochondrial
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