Identification of EFHD1 as a novel Ca2+ sensor for mitoflash activation

Cell Calcium

Volumn 59, Issue 5, 2016, Pages 262-270

  Hou, Tingting ^a   Jian, Chongshu ^a   Xu, Jiejia ^a   Huang, August Yue ^a   Xi, Jianzhong ^a   Hu, Keping ^b   Wei, Liping ^a   Cheng, Heping ^a   Wang, Xianhua ^a  

^a PEKING UNIVERSITY   (China)

^b INSTITUTE OF MEDICINAL PLANT DEVELOPMENT   (China)

Author keywords

Ca2+ Binding proteins; EFHD1; Mitochondria; Mitochondrial Ca2+ signaling; Mitochondrial flash (mitoflash)

Indexed keywords

EFHD1 PROTEIN; MITOCHONDRIAL PROTEIN; REGULATOR PROTEIN; UNCLASSIFIED DRUG; CALCIUM; CALCIUM BINDING PROTEIN; EFHD1 PROTEIN, HUMAN; REACTIVE OXYGEN METABOLITE;

ARTICLE; BINDING SITE; CALCIUM BINDING; CONTROLLED STUDY; DOWN REGULATION; HYPEROSMOTIC STRESS; MITOCHONDRIAL RESPIRATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; CALCIUM SIGNALING; HUMAN; METABOLISM; MITOCHONDRION; PHYSIOLOGY;

CALCIUM; CALCIUM SIGNALING; CALCIUM-BINDING PROTEINS; DOWN-REGULATION; HUMANS; MITOCHONDRIA; REACTIVE OXYGEN SPECIES;

EID: 84960171598     PISSN: 01434160     EISSN: 15321991     Source Type: Journal    
DOI: 10.1016/j.ceca.2016.03.002     Document Type: Article

References (53)

1. Nunnari J., Suomalainen A. Mitochondria: in sickness and in health. Cell 2012, 148:1145-1159.
2. Wang W., Fang H., Groom L., Cheng A., Zhang W., Liu J., Wang X., Li K., Han P., Zheng M., Yin J., Mattson M.P., Kao J.P., Lakatta E.G., Sheu S.S., Ouyang K., Chen J., Dirksen R.T., Cheng H. Superoxide flashes in single mitochondria. Cell 2008, 134:279-290.
3. Pouvreau S. Superoxide flashes in mouse skeletal muscle are produced by discrete arrays of active mitochondria operating coherently. PLoS One 2010, 5:e13035.
4. Zhang X., Huang Z., Hou T., Xu J., Wang Y., Shang W., Ye T., Cheng H., Gao F., Wang X. Superoxide constitutes a major signal of mitochondrial superoxide flash. Life Sci. 2013, 93:178-186.
5. Schwarzländer M., Logan D.C., Fricker M.D., Sweetlove L.J. The circularly permuted yellow fluorescent protein cpYFP that has been used as a superoxide probe is highly responsive to pH but not superoxide in mitochondria: implications for the existence of superoxide 'flashes'. Biochem. J. 2011, 437:381-387.
6. Schwarzländer M., Logan D.C., Johnston I.G., Jones N.S., Meyer A.J., Fricker M.D., Sweetlove L.J. Pulsing of membrane potential in individual mitochondria: a stress-induced mechanism to regulate respiratory bioenergetics in Arabidopsis. Plant Cell 2012, 24:1188-1201.
7. Wei-LaPierre L., Gong G., Gerstner B.J., Ducreux S., Yule D.I., Pouvreau S., Wang X., Sheu S.S., Cheng H., Dirksen R.T., Wang W. Respective contribution of mitochondrial superoxide and pH to mitochondria-targeted circularly permuted yellow fluorescent protein (mt-cpYFP) flash activity. J. Biol. Chem. 2013, 288:10567-10577.
8. Hou T., Wang X., Ma Q., Cheng H. Mitochondrial flashes: new insights into mitochondrial ROS signalling and beyond. J. Physiol. 2014, 592:3703-3713.
9. Fang H., Chen M., Ding Y., Shang W., Xu J., Zhang X., Zhang W., Li K., Xiao Y., Gao F., Shang S., Li J.C., Tian X.L., Wang S.Q., Zhou J., Weisleder N., Ma J., Ouyang K., Chen J., Wang X., Zheng M., Wang W., Cheng H. Imaging superoxide flash and metabolism-coupled mitochondrial permeability transition in living animals. Cell Res. 2011, 21:1295-1304.
10. Ma Q., Fang H., Shang W., Liu L., Xu Z., Ye T., Wang X., Zheng M., Chen Q., Cheng H. Superoxide flashes: early mitochondrial signals for oxidative stress-induced apoptosis. J. Biol. Chem. 2011, 286:27573-27581.
11. Wei L., Salahura G., Boncompagni S., Kasischke K.A., Protasi F., Sheu S.S., Dirksen R.T. Mitochondrial superoxide flashes: metabolic biomarkers of skeletal muscle activity and disease. FASEB J. 2011, 25:3068-3078.
12. Hou Y., Ouyang X., Wan R., Cheng H., Mattson M.P., Cheng A. Mitochondrial superoxide production negatively regulates neural progenitor proliferation and cerebral cortical development. Stem Cells 2012, 30:2535-2547.
13. 2+ uniport and basal reactive oxygen species elevation. J. Biol. Chem. 2013, 288:4602-4612.
14. Cao Y., Zhang X., Shang W., Xu J., Wang X., Hu X., Ao Y., Cheng H. Proinflammatory cytokines stimulate mitochondrial superoxide flashes in articular chondrocytes in vitro and in situ. PLoS One 2013, 8:e66444.
15. Shen E.Z., Song C.Q., Lin Y., Zhang W.H., Su P.F., Liu W.Y., Zhang P., Xu J., Lin N., Zhan C., Wang X., Shyr Y., Cheng H., Dong M.Q. Mitoflash frequency in early adulthood predicts lifespan in Caenorhabditis elegans. Nature 2014, 508:128-132.
16. Zhang M., Sun T., Jian C., Lei L., Han P., Lv Q., Yang R., Zhou X., Xu J., Hu Y., Men Y., Huang Y., Zhang C., Zhu X., Wang X., Cheng H., Xiong J.W. Remodeling of mitochondrial flashes in muscular development and dystrophy in zebrafish. PLoS One 2015, 10:e0132567.
17. Hou Y., Mattson M.P., Cheng A. Permeability transition pore-mediated mitochondrial superoxide flashes regulate cortical neural progenitor differentiation. PLoS One 2013, 8:e76721.
18. Ding Y., Fang H., Shang W., Xiao Y., Sun T., Hou N., Pan L., Sun X., Ma Q., Zhou J., Wang X., Zhang X., Cheng H. Mitoflash altered by metabolic stress in insulin-resistant skeletal muscle. J. Mol. Med. (Berl.) 2015, 93:1119-1130.
19. Hou Y., Ghosh P., Wan R., Ouyang X., Cheng H., Mattson M.P., Cheng A. Permeability transition pore-mediated mitochondrial superoxide flashes mediate an early inhibitory effect of amyloid beta1-42 on neural progenitor cell proliferation. Neurobiol. Aging 2014, 35:975-989.
20. Ying Z., Chen K., Zheng L., Wu Y., Li L., Wang R., Long Q., Yang L., Guo J., Yao D., Li Y., Bao F., Xiang G., Liu J., Huang Q., Wu Z., Hutchins A.P., Pei D., Liu X. Transient activation of mitoflashes modulates Nanog at the early phase of somatic cell reprogramming. Cell Metab. 2016, 23:220-226.
21. Jian C., Hou T., Yin R., Cheng H., Wang X. Regulation of superoxide flashes by transient and steady mitochondrial calcium elevations. Sci. China Life Sci. 2014, 57:495-501.
22. Gong G., Liu X., Wang W. Regulation of metabolism in individual mitochondria during excitation-contraction coupling. J. Mol. Cell. Cardiol. 2014, 76:235-246.
23. Pagliarini D.J., Calvo S.E., Chang B., Sheth S.A., Vafai S.B., Ong S.E., Walford G.A., Sugiana C., Boneh A., Chen W.K., Hill D.E., Vidal M., Evans J.G., Thorburn D.R., Carr S.A., Mootha V.K. A mitochondrial protein compendium elucidates complex I disease biology. Cell 2008, 134:112-123.
24. UniProt C. UniProt: a hub for protein information. Nucleic Acids Res. 2015, 43:D204-212.
25. de Castro E., Sigrist C.J., Gattiker A., Bulliard V., Langendijk-Genevaux P.S., Gasteiger E., Bairoch A., Hulo N. ScanProsite: detection of PROSITE signature matches and ProRule-associated functional and structural residues in proteins. Nucleic Acids Res. 2006, 34:W362-365.
26. 2+ waves in saponin-permeabilized rat ventricular myocytes. J. Physiol. 1999, 521(Pt 3):575-585.
27. Li K., Zhang W., Fang H., Xie W., Liu J., Zheng M., Wang X., Wang W., Tan W., Cheng H. Superoxide flashes reveal novel properties of mitochondrial reactive oxygen species excitability in cardiomyocytes. Biophys. J. 2012, 102:1011-1021.
28. Patron M., Checchetto V., Raffaello A., Teardo E., Vecellio Reane D., Mantoan M., Granatiero V., Szabo I., De Stefani D., Rizzuto R. MICU1 and MICU2 finely tune the mitochondrial Ca2+ uniporter by exerting opposite effects on MCU activity. Mol. Cell 2014, 53:726-737.
29. Baughman J.M., Perocchi F., Girgis H.S., Plovanich M., Belcher-Timme C.A., Sancak Y., Bao X.R., Strittmatter L., Goldberger O., Bogorad R.L., Koteliansky V., Mootha V.K. Integrative genomics identifies MCU as an essential component of the mitochondrial calcium uniporter. Nature 2011, 476:341-345.
30. De Stefani D., Raffaello A., Teardo E., Szabo I., Rizzuto R. A forty-kilodalton protein of the inner membrane is the mitochondrial calcium uniporter. Nature 2011, 476:336-340.
31. + antiporter. Science 2009, 326:144-147.
32. Nowikovsky K., Pozzan T., Rizzuto R., Scorrano L., Bernardi P. Perspectives on: SGP symposium on mitochondrial physiology and medicine: the pathophysiology of LETM1. J. Gen. Physiol. 2012, 139:445-454.
33. 2+ uptake, interacts with MCU, and induces oxidative stress-mediated cell death. Mol. Biol. Cell 2014, 25:936-947.
34. 2+/Pi transporter) reduces physical endurance and metabolic efficiency in mice. J. Biol. Chem. 2011, 286:11659-11671.
35. 2+ uptake. Nature 2010, 467:291-296.
36. Huang Z., Zhang W., Fang H., Zheng M., Wang X., Xu J., Cheng H., Gong G., Wang W., Dirksen R.T., Sheu S.S. Response to a critical evaluation of cpYFP as a probe for superoxide. Free Radic. Biol. Med. 2011, 51:1937-1940.
37. 2+ transport. J. Bioenerg. Biomembr. 1994, 26:495-508.
38. 2+ uniporter. Cell Metab. 2013, 17:976-987.
39. Kamer K.J., Mootha V.K. MICU1 and MICU2 play nonredundant roles in the regulation of the mitochondrial calcium uniporter. EMBO Rep. 2014, 15:299-307.
40. + homeostasis with a potential role in the Wolf-Hirschhorn syndrome. J. Biol. Chem. 2004, 279:30307-30315.
41. Hasegawa A., van der Bliek A.M. Inverse correlation between expression of the Wolfs Hirschhorn candidate gene Letm1 and mitochondrial volume in C. elegans and in mammalian cells. Hum. Mol. Genet. 2007, 16:2061-2071.
42. McQuibban A.G., Joza N., Megighian A., Scorzeto M., Zanini D., Reipert S., Richter C., Schweyen R.J., Nowikovsky K. A Drosophila mutant of LETM1, a candidate gene for seizures in Wolf-Hirschhorn syndrome. Hum. Mol. Genet. 2010, 19:987-1000.
43. Hashimi H., McDonald L., Stribrna E., Lukes J. Trypanosome Letm1 protein is essential for mitochondrial potassium homeostasis. J. Biol. Chem. 2013, 288:26914-26925.
44. Nowikovsky K., Bernardi P. LETM1 in mitochondrial cation transport. Front. Physiol. 2014, 5:83.
45. + antiporter Letm1. J. Gen. Physiol. 2014, 143:67-73.
46. Satrustegui J., Pardo B., Del Arco A. Mitochondrial transporters as novel targets for intracellular calcium signaling. Physiol. Rev. 2007, 87:29-67.
47. 2+-dependent solute carrier gene family. Gene 2005, 345:173-182.
48. 2+-binding protein with EF-hand and coiled-coil domains. J. Neurochem. 2006, 96:292-304.
49. Dutting S., Brachs S., Mielenz D. Fraternal twins: Swiprosin-1/EFhd2 and Swiprosin-2/EFhd1, two homologous EF-hand containing calcium binding adaptor proteins with distinct functions. Cell Commun. Signal.: CCS 2011, 9:2.
50. Tominaga M., Tomooka Y. Novel genes cloned from a neuronal cell line newly established from a cerebellum of an adult p53(-/-) mouse. Biochem. Biophys. Res. Commun. 2002, 297:473-479.
51. 2+-induced membrane transition in mitochondria. I. The protective mechanisms. Arch. Biochem. Biophys. 1979, 195:453-459.
52. 2+ trigger site. Arch. Biochem. Biophys. 1979, 195:460-467.
53. 2+ release. Arch. Biochem. Biophys. 1979, 195:468-477.