Abstract
The coiled-coil-helix-coiled-coil-helix domain (CHCHD)-containing proteins are evolutionarily conserved nucleus-encoded small mitochondrial proteins with important functions. So far, nine members have been identified in this protein family. All CHCHD proteins have at least one functional coiled-coil-helix-coiled-coil-helix (CHCH) domain, which is stabilized by two pairs of disulfide bonds between two helices. CHCHD proteins have various important pathophysiological roles in mitochondria and other key cellular processes. Mutations of CHCHD proteins have been associated with various human neurodegenerative diseases. Mutations of CHCHD10 are associated with amyotrophic lateral sclerosis (ALS) and/or frontotemporal lobe dementia (FTD), motor neuron disease, and late-onset spinal muscular atrophy and autosomal dominant mitochondrial myopathy. CHCHD10 stabilizes mitochondrial crista ultrastructure and maintains its integrity. In patients with CHCHD10 mutations, there are abnormal mitochondrial crista structure, deficiencies of respiratory chain complexes, impaired mitochondrial respiration, and multiple mitochondrial DNA (mtDNA) deletions. Recently, CHCHD2 mutations are linked with autosomal dominant and sporadic Parkinson’s disease (PD). The CHCHD2 is a multifunctional protein and plays roles in regulation of mitochondrial metabolism, synthesis of respiratory chain components, and modulation of cell apoptosis. With a better understanding of the pathophysiologic roles of CHCHD proteins, they may be potential novel therapeutic targets for human neurodegenerative diseases.
Similar content being viewed by others
Change history
07 October 2016
An erratum to this article has been published.
Abbreviations
- ALS:
-
Amyotrophic lateral sclerosis
- AD:
-
Alzheimer’s disease
- CHCH:
-
Coiled-coil-helix-coiled-coil-helix
- CHCHD:
-
Coiled-coil-helix-coiled-coil-helix domain
- COX:
-
Cytochrome c oxidase
- CPC:
-
Cysteine-proline-cysteine motif
- DA:
-
Dopamine
- EGFR:
-
Epidermal growth factor receptor
- FTD:
-
Frontotemporal lobe dementia
- GBA:
-
Guilt-by-association analysis
- HPA:
-
Human Protein Atlas project
- IMM:
-
The mitochondrial inner membrane
- IMMD:
-
The autosomal dominant mitochondrial myopathy
- IMS:
-
The mitochondrial intermembrane space
- ISE:
-
The mitochondrial iron-sulfur exporter machinery
- ITS:
-
The mitochondrial IMS-targeting signal
- MICOS:
-
The mitochondrial contact site complex
- MOMP:
-
The mitochondrial OMM permeabilization
- mtDNA:
-
Mitochondrial DNA
- MTS:
-
The mitochondrial targeting sequence
- NSCLC:
-
Non-small-cell lung carcinoma
- OMM:
-
The mitochondrial outer membrane
- ORE:
-
Oxygen-responsive element
- OxPhos:
-
The oxidative phosphorylation process
- PD:
-
Parkinson’s disease
- RBPJ:
-
The recombination signal sequence-binding protein Jκ
- ROS:
-
Redox oxygen species
- SMAJ:
-
The late-onset spinal muscular atrophy, Jokela type
- tBID:
-
The truncated form of BID
- WT:
-
Wild type
References
Frey TG, Mannella CA (2000) The internal structure of mitochondria. Trends Biochem Sci 25(7):319–324. doi:10.1016/S0968-0004(00)01609-1
Schmidt O, Pfanner N, Meisinger C (2010) Mitochondrial protein import: from proteomics to functional mechanisms. Nat Rev Mol Cell Biol 11(9):655–667
Dolezal P, Likic V, Tachezy J, Lithgow T (2006) Evolution of the molecular machines for protein import into mitochondria. Science 313(5785):314–318. doi:10.1126/science.1127895
Neupert W, Herrmann JM (2007) Translocation of proteins into mitochondria. Annu Rev Biochem 76:723–749. doi:10.1146/annurev.biochem.76.052705.163409
Osellame LD, Blacker TS, Duchen MR (2012) Cellular and molecular mechanisms of mitochondrial function. Best Pract Res Clin Endocrinol Metab 26(6):711–723. doi:10.1016/j.beem.2012.05.003
Brookes PS, Yoon Y, Robotham JL, Anders MW, Sheu SS (2004) Calcium, ATP, and ROS: a mitochondrial love-hate triangle. Am J Physiol Cell Physiol 287(4):C817–C833. doi:10.1152/ajpcell.00139.2004
Funayama M, Ohe K, Amo T, Furuya N, Yamaguchi J, Saiki S, Li Y, Ogaki K, Ando M, Yoshino H, Tomiyama H, Nishioka K, Hasegawa K, Saiki H, Satake W, Mogushi K, Sasaki R, Kokubo Y, Kuzuhara S, Toda T, Mizuno Y, Uchiyama Y, Ohno K, Hattori N (2015) CHCHD2 mutations in autosomal dominant late-onset Parkinson’s disease: a genome-wide linkage and sequencing study. Lancet Neurol 14(3):274–282. doi:10.1016/S1474-4422(14)70266-2
Bannwarth S, Ait-El-Mkadem S, Chaussenot A, Genin EC, Lacas-Gervais S, Fragaki K, Berg-Alonso L, Kageyama Y, Serre V, Moore DG, Verschueren A, Rouzier C, Le Ber I, Auge G, Cochaud C, Lespinasse F, N’Guyen K, de Septenville A, Brice A, Yu-Wai-Man P, Sesaki H, Pouget J, Paquis-Flucklinger V (2014) A mitochondrial origin for frontotemporal dementia and amyotrophic lateral sclerosis through CHCHD10 involvement. Brain J Neurol 137(Pt 8):2329–2345. doi:10.1093/brain/awu138
Koc EC, Cimen H, Kumcuoglu B, Abu N, Akpinar G, Haque ME, Spremulli LL, Koc H (2013) Identification and characterization of CHCHD1, AURKAIP1, and CRIF1 as new members of the mammalian mitochondrial ribosome. Front Physiol 4:183. doi:10.3389/fphys.2013.00183
Aras S, Pak O, Sommer N, Finley R Jr, Huttemann M, Weissmann N, Grossman LI (2013) Oxygen-dependent expression of cytochrome c oxidase subunit 4-2 gene expression is mediated by transcription factors RBPJ, CXXC5 and CHCHD2. Nucleic Acids Res 41(4):2255–2266. doi:10.1093/nar/gks1454
Aras S, Bai M, Lee I, Springett R, Huttemann M, Grossman LI (2015) MNRR1 (formerly CHCHD2) is a bi-organellar regulator of mitochondrial metabolism. Mitochondrion 20:43–51. doi:10.1016/j.mito.2014.10.003
Liu Y, Clegg HV, Leslie PL, Di J, Tollini LA, He Y, Kim TH, Jin A, Graves LM, Zheng J, Zhang Y (2015) CHCHD2 inhibits apoptosis by interacting with Bcl-x L to regulate Bax activation. Cell Death Differ 22(6):1035–1046. doi:10.1038/cdd.2014.194
Seo M, Lee WH, Suk K (2010) Identification of novel cell migration-promoting genes by a functional genetic screen. FASEB J: Off Publ Fed Am Soc Exp Biol 24(2):464–478. doi:10.1096/fj.09-137562
Darshi M, Perkins GA, Mackey MR, Petrosyan S, Murphy AN, Ellisman MH, Taylor SS (2010) ChChd3, an inner mitochondrial membrane protein is essential for maintaining cristae integrity and mitochondrial function. FASEB J 24
Liu H, Li Y, Li Y, Liu B, Wu H, Wang J, Wang Y, Wang M, Tang SC, Zhou Q, Chen J (2012) Cloning and functional analysis of FLJ20420: a novel transcription factor for the BAG-1 promoter. PLoS One 7(5):e34832. doi:10.1371/journal.pone.0034832
Sztolsztener ME, Brewinska A, Guiard B, Chacinska A (2013) Disulfide bond formation: sulfhydryl oxidase ALR controls mitochondrial biogenesis of human MIA40. Traffic 14(3):309–320. doi:10.1111/tra.12030
Banci L, Bertini I, Cefaro C, Ciofi-Baffoni S, Gallo A, Martinelli M, Sideris DP, Katrakili N, Tokatlidis K (2009) MIA40 is an oxidoreductase that catalyzes oxidative protein folding in mitochondria. Nat Struct Mol Biol 16(2):198–206. doi:10.1038/nsmb.1553
Murari A, Thiriveedi VR, Mohammad F, Vengaldas V, Gorla M, Tammineni P, Krishnamoorthy T, Sepuri NB (2015) Human mitochondrial MIA40 (CHCHD4) is a component of the Fe-S cluster export machinery. Biochem J 471(2):231–241. doi:10.1042/BJ20150012
Hangen E, Feraud O, Lachkar S, Mou H, Doti N, Fimia GM, Lam NV, Zhu C, Godin I, Muller K, Chatzi A, Nuebel E, Ciccosanti F, Flamant S, Benit P, Perfettini JL, Sauvat A, Bennaceur-Griscelli A, Ser-Le Roux K, Gonin P, Tokatlidis K, Rustin P, Piacentini M, Ruvo M, Blomgren K, Kroemer G, Modjtahedi N (2015) Interaction between AIF and CHCHD4 regulates respiratory chain biogenesis. Mol Cell 58(6):1001–1014. doi:10.1016/j.molcel.2015.04.020
An J, Shi J, He Q, Lui K, Liu Y, Huang Y, Sheikh MS (2012) CHCM1/CHCHD6, novel mitochondrial protein linked to regulation of mitofilin and mitochondrial cristae morphology. J Biol Chem 287(10):7411–7426. doi:10.1074/jbc.M111.277103
Ding C, Wu Z, Huang L, Wang Y, Xue J, Chen S, Deng Z, Wang L, Song Z, Chen S (2015) Mitofilin and CHCHD6 physically interact with Sam50 to sustain cristae structure. Sci Rep 5:16064. doi:10.1038/srep16064
Bode M, Longen S, Morgan B, Peleh V, Dick TP, Bihlmaier K, Herrmann JM (2013) Inaccurately assembled cytochrome c oxidase can lead to oxidative stress-induced growth arrest. Antioxid Redox Signal 18(13):1597–1612. doi:10.1089/ars.2012.4685
Bestwick M, Jeong MY, Khalimonchuk O, Kim H, Winge DR (2010) Analysis of Leigh syndrome mutations in the yeast SURF1 homolog reveals a new member of the cytochrome oxidase assembly factor family. Mol Cell Biol 30(18):4480–4491. doi:10.1128/MCB.00228-10
Martherus RS, Sluiter W, Timmer ED, VanHerle SJ, Smeets HJ, Ayoubi TA (2010) Functional annotation of heart enriched mitochondrial genes GBAS and CHCHD10 through guilt by association. Biochem Biophys Res Commun 402(2):203–208. doi:10.1016/j.bbrc.2010.09.109
Arnesano F, Balatri E, Banci L, Bertini I, Winge DR (2005) Folding studies of Cox17 reveal an important interplay of cysteine oxidation and copper binding. Structure 13(5):713–722. doi:10.1016/j.str.2005.02.015
Cavallaro G (2010) Genome-wide analysis of eukaryotic twin CX9C proteins. Mol BioSyst 6(12):2459–2470. doi:10.1039/c0mb00058b
Banci L, Bertini I, Ciofi-Baffoni S, Jaiswal D, Neri S, Peruzzini R, Winkelmann J (2012) Structural characterization of CHCHD5 and CHCHD7: two atypical human twin CX9C proteins. J Struct Biol 180(1):190–200. doi:10.1016/j.jsb.2012.07.007
Darshi M, Mendiola VL, Mackey MR, Murphy AN, Koller A, Perkins GA, Ellisman MH, Taylor SS (2011) ChChd3, an inner mitochondrial membrane protein, is essential for maintaining crista integrity and mitochondrial function. J Biol Chem 286(4):2918–2932. doi:10.1074/jbc.M110.171975
Yang J, Staples O, Thomas LW, Briston T, Robson M, Poon E, Simoes ML, El-Emir E, Buffa FM, Ahmed A, Annear NP, Shukla D, Pedley BR, Maxwell PH, Harris AL, Ashcroft M (2012) Human CHCHD4 mitochondrial proteins regulate cellular oxygen consumption rate and metabolism and provide a critical role in hypoxia signaling and tumor progression. J Clin Invest 122(2):600–611. doi:10.1172/JCI58780
Hofmann S, Rothbauer U, Muhlenbein N, Baiker K, Hell K, Bauer MF (2005) Functional and mutational characterization of human MIA40 acting during import into the mitochondrial intermembrane space. J Mol Biol 353(3):517–528. doi:10.1016/j.jmb.2005.08.064
Ajroud-Driss S, Fecto F, Ajroud K, Lalani I, Calvo SE, Mootha VK, Deng HX, Siddique N, Tahmoush AJ, Heiman-Patterson TD, Siddique T (2015) Mutation in the novel nuclear-encoded mitochondrial protein CHCHD10 in a family with autosomal dominant mitochondrial myopathy. Neurogenetics 16(1):1–9. doi:10.1007/s10048-014-0421-1
Chacinska A, Guiard B, Muller JM, Schulze-Specking A, Gabriel K, Kutik S, Pfanner N (2008) Mitochondrial biogenesis, switching the sorting pathway of the intermembrane space receptor Mia40. J Biol Chem 283(44):29723–29729. doi:10.1074/jbc.M805356200
Subcellular localization of CHCHD5—the Human Protein Atlas project (HPA). http://www.proteinatlas.org/ENSG00000125611-CHCHD5/subcellular. Accessed 15 July 2016
Uhlen M, Oksvold P, Fagerberg L, Lundberg E, Jonasson K, Forsberg M, Zwahlen M, Kampf C, Wester K, Hober S, Wernerus H, Bjorling L, Ponten F (2010) Towards a knowledge-based human protein atlas. Nat Biotechnol 28(12):1248–1250. doi:10.1038/nbt1210-1248
Dudek J, Rehling P, van der Laan M (2013) Mitochondrial protein import: common principles and physiological networks. Biochim Biophys Acta 1833(2):274–285. doi:10.1016/j.bbamcr.2012.05.028
Chacinska A, Koehler CM, Milenkovic D, Lithgow T, Pfanner N (2009) Importing mitochondrial proteins: machineries and mechanisms. Cell 138(4):628–644. doi:10.1016/j.cell.2009.08.005
Bannai H, Tamada Y, Maruyama O, Nakai K, Miyano S (2002) Extensive feature detection of N-terminal protein sorting signals. Bioinformatics 18(2):298–305
Claros MG (1995) MitoProt, a Macintosh application for studying mitochondrial proteins. Comput Appl Biosci 11(4):441–447
Darshi M, Trinh KN, Murphy AN, Taylor SS (2012) Targeting and import mechanism of coiled-coil helix coiled-coil helix domain-containing protein 3 (ChChd3) into the mitochondrial intermembrane space. J Biol Chem 287(47). doi:10.1074/jbc.M112.387696
Westerman BA, Poutsma A, Steegers EA, Oudejans CB (2004) C2360, a nuclear protein expressed in human proliferative cytotrophoblasts, is a representative member of a novel protein family with a conserved coiled coil-helix-coiled coil-helix domain. Genomics 83(6):1094–1104. doi:10.1016/j.ygeno.2003.12.006
Subcellular localization of CHCHD1—the Human Protein Atlas project (HPA). http://www.proteinatlas.org/ENSG00000172586-CHCHD1/subcellular. Accessed 15/7/2016
Soto IC, Fontanesi F, Liu J, Barrientos A (2012) Biogenesis and assembly of eukaryotic cytochrome c oxidase catalytic core. Biochim Biophys Acta 1817(6):883–897. doi:10.1016/j.bbabio.2011.09.005
Khalimonchuk O, Rodel G (2005) Biogenesis of cytochrome c oxidase. Mitochondrion 5(6):363–388. doi:10.1016/j.mito.2005.08.002
Goldschmidt-Reisin S, Kitakawa M, Herfurth E, Wittmann-Liebold B, Grohmann L, Graack HR (1998) Mammalian mitochondrial ribosomal proteins. N-terminal amino acid sequencing, characterization, and identification of corresponding gene sequences. J Biol Chem 273(52):34828–34836
Graack HR, Bryant ML, O’Brien TW (1999) Identification of mammalian mitochondrial ribosomal proteins (MRPs) by N-terminal sequencing of purified bovine MRPs and comparison to data bank sequences: the large subribosomal particle. Biochemistry 38(50):16569–16577
Suzuki T, Terasaki M, Takemoto-Hori C, Hanada T, Ueda T, Wada A, Watanabe K (2001) Structural compensation for the deficit of rRNA with proteins in the mammalian mitochondrial ribosome. Systematic analysis of protein components of the large ribosomal subunit from mammalian mitochondria. J Biol Chem 276(24):21724–21736. doi:10.1074/jbc.M100432200
Koc EC, Burkhart W, Blackburn K, Moseley A, Koc H, Spremulli LL (2000) A proteomics approach to the identification of mammalian mitochondrial small subunit ribosomal proteins. J Biol Chem 275(42):32585–32591. doi:10.1074/jbc.M003596200
Jin C, Myers AM, Tzagoloff A (1997) Cloning and characterization of MRP10, a yeast gene coding for a mitochondrial ribosomal protein. Curr Genet 31(3):228–234. doi:10.1007/s002940050199
Davies KM, Strauss M, Daum B, Kief JH, Osiewacz HD, Rycovska A, Zickermann V, Kuhlbrandt W (2011) Macromolecular organization of ATP synthase and complex I in whole mitochondria. Proc Natl Acad Sci U S A 108(34):14121–14126. doi:10.1073/pnas.1103621108
Vogel F, Bornhovd C, Neupert W, Reichert AS (2006) Dynamic subcompartmentalization of the mitochondrial inner membrane. J Cell Biol 175(2):237–247. doi:10.1083/jcb.200605138
Cogliati S, Frezza C, Soriano ME, Varanita T, Quintana-Cabrera R, Corrado M, Cipolat S, Costa V, Casarin A, Gomes LC, Perales-Clemente E, Salviati L, Fernandez-Silva P, Enriquez JA, Scorrano L (2013) Mitochondrial cristae shape determines respiratory chain supercomplexes assembly and respiratory efficiency. Cell 155(1):160–171. doi:10.1016/j.cell.2013.08.032
Zerbes RM, Bohnert M, Stroud DA, von der Malsburg K, Kram A, Oeljeklaus S, Warscheid B, Becker T, Wiedemann N, Veenhuis M, van der Klei IJ, Pfanner N, van der Laan M (2012) Role of MINOS in mitochondrial membrane architecture: cristae morphology and outer membrane interactions differentially depend on mitofilin domains. J Mol Biol 422(2):183–191. doi:10.1016/j.jmb.2012.05.004
Friedman JR, Mourier A, Yamada J, McCaffery JM, Nunnari J (2015) MICOS coordinates with respiratory complexes and lipids to establish mitochondrial inner membrane architecture. eLife 4. doi:10.7554/eLife.07739
Rabl R, Soubannier V, Scholz R, Vogel F, Mendl N, Vasiljev-Neumeyer A, Korner C, Jagasia R, Keil T, Baumeister W, Cyrklaff M, Neupert W, Reichert AS (2009) Formation of cristae and crista junctions in mitochondria depends on antagonism between Fcj1 and Su e/g. J Cell Biol 185(6):1047–1063. doi:10.1083/jcb.200811099
Harner M, Korner C, Walther D, Mokranjac D, Kaesmacher J, Welsch U, Griffith J, Mann M, Reggiori F, Neupert W (2011) The mitochondrial contact site complex, a determinant of mitochondrial architecture. EMBO J 30(21):4356–4370. doi:10.1038/emboj.2011.379
Xie J, Marusich MF, Souda P, Whitelegge J, Capaldi RA (2007) The mitochondrial inner membrane protein mitofilin exists as a complex with SAM50, metaxins 1 and 2, coiled-coil-helix coiled-coil-helix domain-containing protein 3 and 6 and DnaJC11. FEBS Lett 581(18):3545–3549. doi:10.1016/j.febslet.2007.06.052
Genin EC, Plutino M, Bannwarth S, Villa E, Cisneros-Barroso E, Roy M, Ortega-Vila B, Fragaki K, Lespinasse F, Pinero-Martos E, Auge G, Moore D, Burte F, Lacas-Gervais S, Kageyama Y, Itoh K, Yu-Wai-Man P, Sesaki H, Ricci JE, Vives-Bauza C, Paquis-Flucklinger V (2015) CHCHD10 mutations promote loss of mitochondrial cristae junctions with impaired mitochondrial genome maintenance and inhibition of apoptosis. EMBO Mol Med 8(1):58–72. doi:10.15252/emmm.201505496
Ott C, Ross K, Straub S, Thiede B, Gotz M, Goosmann C, Krischke M, Mueller MJ, Krohne G, Rudel T, Kozjak-Pavlovic V (2012) Sam50 functions in mitochondrial intermembrane space bridging and biogenesis of respiratory complexes. Mol Cell Biol 32(6):1173–1188. doi:10.1128/MCB.06388-11
Baughman JM, Nilsson R, Gohil VM, Arlow DH, Gauhar Z, Mootha VK (2009) A computational screen for regulators of oxidative phosphorylation implicates SLIRP in mitochondrial RNA homeostasis. PLoS Genet 5(8):e1000590. doi:10.1371/journal.pgen.1000590
Norbury CJ, Hickson ID (2001) Cellular responses to DNA damage. Annu Rev Pharmacol Toxicol 41:367–401. doi:10.1146/annurev.pharmtox.41.1.367
Elmore S (2007) Apoptosis: a review of programmed cell death. Toxicol Pathol 35(4):495–516. doi:10.1080/01926230701320337
Cory S, Adams JM (2002) The Bcl2 family: regulators of the cellular life-or-death switch. Nat Rev Cancer 2(9):647–656. doi:10.1038/nrc883
Wei MC, Zong WX, Cheng EH, Lindsten T, Panoutsakopoulou V, Ross AJ, Roth KA, MacGregor GR, Thompson CB, Korsmeyer SJ (2001) Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 292(5517):727–730. doi:10.1126/science.1059108
Liu X, Kim CN, Yang J, Jemmerson R, Wang X (1996) Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86(1):147–157. doi:10.1016/S0092-8674(00)80085-9
Du C, Fang M, Li Y, Li L, Wang X (2000) Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell 102(1):33–42
Willis SN, Chen L, Dewson G, Wei A, Naik E, Fletcher JI, Adams JM, Huang DCS (2005) Proapoptotic Bak is sequestered by mcl-1 and Bcl-xL, but not Bcl-2, until displaced by BH3-only proteins. Genes Dev 19(11):1294–1305. doi:10.1101/gad.1304105
Sattler M, Liang H, Nettesheim D, Meadows RP, Harlan JE, Eberstadt M, Yoon HS, Shuker SB, Chang BS, Minn AJ, Thompson CB, Fesik SW (1997) Structure of Bcl-xL-Bak peptide complex: recognition between regulators of apoptosis. Science 275(5302):983–986. doi:10.1126/science.275.5302.983
Vela L, Gonzalo O, Naval J, Marzo I (2013) Direct interaction of Bax and Bak proteins with Bcl-2 homology domain 3 (BH3)-only proteins in living cells revealed by fluorescence complementation. J Biol Chem 288(7):4935–4946. doi:10.1074/jbc.M112.422204
Liu Y, Zhang Y (2015) CHCHD2 connects mitochondrial metabolism to apoptosis. Mol Cell Oncol 2(4):e1004964. doi:10.1080/23723556.2015.1004964
Herrmann JM, Riemer J (2012) Mitochondrial disulfide relay: redox-regulated protein import into the intermembrane space. J Biol Chem 287(7):4426–4433. doi:10.1074/jbc.R111.270678
Koehler CM, Tienson HL (2009) Redox regulation of protein folding in the mitochondrial intermembrane space. Biochim Biophys Acta 1793(1):139–145. doi:10.1016/j.bbamcr.2008.08.002
Modjtahedi N, Tokatlidis K, Dessen P, Kroemer G (2016) Mitochondrial proteins containing coiled-coil-helix-coiled-coil-helix (CHCH) domains in health and disease. Trends Biochem Sci 41(3):245–260. doi:10.1016/j.tibs.2015.12.004
Terziyska N, Lutz T, Kozany C, Mokranjac D, Mesecke N, Neupert W, Herrmann JM, Hell K (2005) Mia40, a novel factor for protein import into the intermembrane space of mitochondria is able to bind metal ions. FEBS Lett 579(1):179–184. doi:10.1016/j.febslet.2004.11.072
Banci L, Bertini I, Cefaro C, Cenacchi L, Ciofi-Baffoni S, Felli IC, Gallo A, Gonnelli L, Luchinat E, Sideris D, Tokatlidis K (2010) Molecular chaperone function of Mia40 triggers consecutive induced folding steps of the substrate in mitochondrial protein import. Proc Natl Acad Sci U S A 107(47):20190–20195. doi:10.1073/pnas.1010095107
Johnson DC, Dean DR, Smith AD, Johnson MK (2005) Structure, function, and formation of biological iron-sulfur clusters. Annu Rev Biochem 74:247–281. doi:10.1146/annurev.biochem.74.082803.133518
Brzoska K, Meczynska S, Kruszewski M (2006) Iron-sulfur cluster proteins: electron transfer and beyond. Acta Biochim Pol 53(4):685–691
Rouault TA, Tong WH (2008) Iron-sulfur cluster biogenesis and human disease. Trends Genet 24(8):398–407. doi:10.1016/j.tig.2008.05.008
Spiller Michael P, Ang Swee K, Ceh-Pavia E, Fisher K, Wang Q, Rigby Stephen EJ, Lu H (2013) Identification and characterization of mitochondrial Mia40 as an iron–sulfur protein. Biochem J 455(1):27–35. doi:10.1042/bj20130442
Kurosaka S, Kashina A (2008) Cell biology of embryonic migration. Birth Defects Res C Embryo Today 84(2):102–122. doi:10.1002/bdrc.20125
Wei Y, Vellanki RN, Coyaud E, Ignatchenko V, Li L, Krieger JR, Taylor P, Tong J, Pham NA, Liu G, Raught B, Wouters BG, Kislinger T, Tsao MS, Moran MF (2015) CHCHD2 is coamplified with EGFR in NSCLC and regulates mitochondrial function and cell migration. Mol Cancer Res: MCR 13(7):1119–1129. doi:10.1158/1541-7786.mcr-14-0165-t
Lin MT, Beal MF (2006) Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443(7113):787–795. doi:10.1038/nature05292
Radad K, Rausch WD, Gille G (2006) Rotenone induces cell death in primary dopaminergic culture by increasing ROS production and inhibiting mitochondrial respiration. Neurochem Int 49(4):379–386. doi:10.1016/j.neuint.2006.02.003
Dawson TM, Dawson VL (2003) Molecular pathways of neurodegeneration in Parkinson’s disease. Science 302(5646):819–822. doi:10.1126/science.1087753
Mutisya EM, Bowling AC, Beal MF (1994) Cortical cytochrome oxidase activity is reduced in Alzheimer’s disease. J Neurochem 63(6):2179–2184. doi:10.1046/j.1471-4159.1994.63062179.x
Hirai K, Aliev G, Nunomura A, Fujioka H, Russell RL, Atwood CS, Johnson AB, Kress Y, Vinters HV, Tabaton M, Shimohama S, Cash AD, Siedlak SL, Harris PL, Jones PK, Petersen RB, Perry G, Smith MA (2001) Mitochondrial abnormalities in Alzheimer’s disease. J Neurosci Off J Soc Neurosci 21(9):3017–3023
Zhu X, Perry G, Moreira PI, Aliev G, Cash AD, Hirai K, Smith MA (2006) Mitochondrial abnormalities and oxidative imbalance in Alzheimer disease. J Alzheimer Dis: JAD 9(2):147–153
Schulz KL, Eckert A, Rhein V, Mai S, Haase W, Reichert AS, Jendrach M, Muller WE, Leuner K (2012) A new link to mitochondrial impairment in tauopathies. Mol Neurobiol 46(1):205–216. doi:10.1007/s12035-012-8308-3
Crugnola V, Lamperti C, Lucchini V, Ronchi D, Peverelli L, Prelle A, Sciacco M, Bordoni A, Fassone E, Fortunato F, Corti S, Silani V, Bresolin N, Di Mauro S, Comi GP, Moggio M (2010) Mitochondrial respiratory chain dysfunction in muscle from patients with amyotrophic lateral sclerosis. Arch Neurol 67(7):849–854. doi:10.1001/archneurol.2010.128
Wiedemann FR, Manfredi G, Mawrin C, Beal MF, Schon EA (2002) Mitochondrial DNA and respiratory chain function in spinal cords of ALS patients. J Neurochem 80(4):616–625
Vielhaber S, Kunz D, Winkler K, Wiedemann FR, Kirches E, Feistner H, Heinze HJ, Elger CE, Schubert W, Kunz WS (2000) Mitochondrial DNA abnormalities in skeletal muscle of patients with sporadic amyotrophic lateral sclerosis. Brain J Neurol 123(Pt 7):1339–1348
Esteras Gallego N, Wray S, Preza E, Abramov AY (2015) Higher mitochondrial membrane potential induces ROS production in the familiar form of frontotemporal dementia with MAPT mutations. Biophys J 108(2):611a. doi:10.1016/j.bpj.2014.11.3324
Chaussenot A, Le Ber I, Ait-El-Mkadem S, Camuzat A, de Septenville A, Bannwarth S, Genin EC, Serre V, Auge G, French research network on FTD, Ftd ALS, Brice A, Pouget J, Paquis-Flucklinger V (2014) Screening of CHCHD10 in a French cohort confirms the involvement of this gene in frontotemporal dementia with amyotrophic lateral sclerosis patients. Neurobiol Aging 35(12):2884 . doi:10.1016/j.neurobiolaging.2014.07.022e2881-2884
Johnson JO, Glynn SM, Gibbs JR, Nalls MA, Sabatelli M, Restagno G, Drory VE, Chio A, Rogaeva E, Traynor BJ (2014) Mutations in the CHCHD10 gene are a common cause of familial amyotrophic lateral sclerosis. Brain J Neurol 137(Pt 12):e311. doi:10.1093/brain/awu265
Dols-Icardo O, Nebot I, Gorostidi A, Ortega-Cubero S, Hernandez I, Rojas-Garcia R, Garcia-Redondo A, Povedano M, Llado A, Alvarez V, Sanchez-Juan P, Pardo J, Jerico I, Vazquez-Costa J, Sevilla T, Cardona F, Indakoechea B, Moreno F, Fernandez-Torron R, Munoz-Llahuna L, Moreno-Grau S, Rosende-Roca M, Vela A, Munoz-Blanco JL, Combarros O, Coto E, Alcolea D, Fortea J, Lleo A, Sanchez-Valle R, Esteban-Perez J, Ruiz A, Pastor P, Lopez De Munain A, Perez-Tur J, Clarimon J, Dementia Genetics Spanish C (2015) Analysis of the CHCHD10 gene in patients with frontotemporal dementia and amyotrophic lateral sclerosis from Spain. Brain J Neurol 138(Pt 12):e400. doi:10.1093/brain/awv175
Zhang M, Xi Z, Zinman L, Bruni AC, Maletta RG, Curcio SA, Rainero I, Rubino E, Pinessi L, Nacmias B, Sorbi S, Galimberti D, Lang AE, Fox S, Surace EI, Ghani M, Guo J, Sato C, Moreno D, Liang Y, Keith J, Traynor BJ, St George-Hyslop P, Rogaeva E (2015) Mutation analysis of CHCHD10 in different neurodegenerative diseases. Brain J Neurol 138(Pt 9):e380. doi:10.1093/brain/awv082
Muller K, Andersen PM, Hubers A, Marroquin N, Volk AE, Danzer KM, Meitinger T, Ludolph AC, Strom TM, Weishaupt JH (2014) Two novel mutations in conserved codons indicate that CHCHD10 is a gene associated with motor neuron disease. Brain J Neurol 137(Pt 12):e309. doi:10.1093/brain/awu227
Jiao B, Xiao T, Hou L, Gu X, Zhou Y, Zhou L, Tang B, Xu J, Shen L (2016) High prevalence of CHCHD10 mutation in patients with frontotemporal dementia from China. Brain J Neurol 139(Pt 4):e21. doi:10.1093/brain/awv367
Chio A, Mora G, Sabatelli M, Caponnetto C, Traynor BJ, Johnson JO, Nalls MA, Calvo A, Moglia C, Borghero G, Monsurro MR, La Bella V, Volanti P, Simone I, Salvi F, Logullo FO, Nilo R, Battistini S, Mandrioli J, Tanel R, Murru MR, Mandich P, Zollino M, Conforti FL, Brunetti M, Barberis M, Restagno G, Penco S, Lunetta C (2015) CHCH10 mutations in an Italian cohort of familial and sporadic amyotrophic lateral sclerosis patients. Neurobiol Aging 36(4):1767 . doi:10.1016/j.neurobiolaging.2015.01.017e1763-1766
Ronchi D, Riboldi G, Del Bo R, Ticozzi N, Scarlato M, Galimberti D, Corti S, Silani V, Bresolin N, Comi GP (2015) CHCHD10 mutations in Italian patients with sporadic amyotrophic lateral sclerosis. Brain J Neurol 138(Pt 8):e372. doi:10.1093/brain/awu384
Penttila S, Jokela M, Bouquin H, Saukkonen AM, Toivanen J, Udd B (2015) Late onset spinal motor neuronopathy is caused by mutation in CHCHD10. Ann Neurol 77(1):163–172. doi:10.1002/ana.24319
Auranen M, Ylikallio E, Shcherbii M, Paetau A, Kiuru-Enari S, Toppila JP, Tyynismaa H (2015) CHCHD10 variant p.(Gly66Val) causes axonal Charcot-Marie-tooth disease. Neurol Genet 1(1):e1. doi:10.1212/NXG.0000000000000003
Chen H, Vermulst M, Wang YE, Chomyn A, Prolla TA, McCaffery JM, Chan DC (2010) Mitochondrial fusion is required for mtDNA stability in skeletal muscle and tolerance of mtDNA mutations. Cell 141(2):280–289. doi:10.1016/j.cell.2010.02.026
Foo JN, Liu J, Tan EK (2015) CHCHD2 and Parkinson’s disease. Lancet Neurol 14(7):681–682. doi:10.1016/s1474-4422(15)00098-8
Shi CH, Mao CY, Zhang SY, Yang J, Song B, Wu P, Zuo CT, Liu YT, Ji Y, Yang ZH, Wu J, Zhuang ZP, Xu YM (2015) CHCHD2 gene mutations in familial and sporadic Parkinson’s disease. Neurobiol Aging. doi:10.1016/j.neurobiolaging.2015.10.040
Shi CH, Mao CY, Zhang SY, Yang J, Song B, Wu P, Zuo CT, Liu YT, Ji Y, Yang ZH, Wu J, Zhuang ZP, YM X (2016) CHCHD2 gene mutations in familial and sporadic Parkinson’s disease. Neurobiol Aging 38:217 . doi:10.1016/j.neurobiolaging.2015.10.040e219-213
Ogaki K, Koga S, Heckman MG, Fiesel FC, Ando M, Labbe C, Lorenzo-Betancor O, Moussaud-Lamodiere EL, Soto-Ortolaza AI, Walton RL, Strongosky AJ, Uitti RJ, McCarthy A, Lynch T, Siuda J, Opala G, Rudzinska M, Krygowska-Wajs A, Barcikowska M, Czyzewski K, Puschmann A, Nishioka K, Funayama M, Hattori N, Parisi JE, Petersen RC, Graff-Radford NR, Boeve BF, Springer W, Wszolek ZK, Dickson DW, Ross OA (2015) Mitochondrial targeting sequence variants of the CHCHD2 gene are a risk for Lewy body disorders. Neurology 85(23):2016–2025. doi:10.1212/WNL.0000000000002170
Yang X, Zhao Q, An R, Zheng J, Tian S, Chen Y, Xu Y (2016) Mutational scanning of the CHCHD2 gene in Han Chinese patients with Parkinson’s disease and meta-analysis of the literature. Parkinsonism Relat Disord. doi:10.1016/j.parkreldis.2016.05.032
Jansen IE, Bras JM, Lesage S, Schulte C, Gibbs JR, Nalls MA, Brice A, Wood NW, Morris H, Hardy JA, Singleton AB, Gasser T, Heutink P, Sharma M, Ipdgc (2015) CHCHD2 and Parkinson’s disease. Lancet Neurol 14(7):678–679. doi:10.1016/S1474-4422(15)00094-0
Koschmidder E, Weissbach A, Bruggemann N, Kasten M, Klein C, Lohmann K (2016) A nonsense mutation in CHCHD2 in a patient with Parkinson disease. Neurology 86(6):577–579. doi:10.1212/WNL.0000000000002361
Puschmann A, Dickson DW, Englund E, Wszolek ZK, Ross OA (2015) CHCHD2 and Parkinson’s disease. Lancet Neurol 14(7):679. doi:10.1016/S1474-4422(15)00095-2
Zhang M, Xi Z, Fang S, Ghani M, Sato C, Moreno D, Liang Y, Lang AE, Rogaeva E (2015) Mutation analysis of CHCHD2 in Canadian patients with familial Parkinson’s disease. Neurobiol Aging. doi:10.1016/j.neurobiolaging.2015.10.038
Acknowledgments
We thank Singapore National Medical Research Council (STaR and Transition awards and clinical translational research programme in Parkinson’s disease) for their support.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Competing Interests
The authors declare that they have no competing interests.
Funding
This study is supported by Singapore National Medical Research Council (NMRC) grants including STaR and Transition awards and clinical translational research programme in Parkinson’s disease.
Additional information
Zhi-Dong Zhou and Wuan-Ting Saw contribute equally to this work
The original version of this article was revised: The reference citations on Table 2 were incorrect in both pdf and html. In the sentence “Furthermore, CHCHD3 is associated with the regulation of expression of an anti-apoptotic protein, BAG-1 [31].’’, reference citation [31] should be [15].’’
An erratum to this article is available at https://doi.org/10.1007/s12035-016-0160-4.
Electronic Supplementary Material
Supplementary Table 1
Predicted MTS fragment in CHCHD proteins (DOCX 15 kb)
Rights and permissions
About this article
Cite this article
Zhou, ZD., Saw, WT. & Tan, EK. Mitochondrial CHCHD-Containing Proteins: Physiologic Functions and Link with Neurodegenerative Diseases. Mol Neurobiol 54, 5534–5546 (2017). https://doi.org/10.1007/s12035-016-0099-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12035-016-0099-5