Mechanism of neuroprotective mitochondrial remodeling by pka/akap1

PLoS Biology

Volumn 9, Issue 4, 2011, Pages

  Merrill, Ronald A ^a   Dagda, Ruben K ^a   Dickey, Audrey S ^a   Cribbs, J Thomas ^a   Green, Steven H ^b   Usachev, Yuriy M ^a   Strack, Stefan ^a  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

A KINASE ANCHORING PROTEIN 1; ALANINE; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE ANCHORING PROTEIN; DYNAMIN RELATED PROTEIN 1; GUANOSINE TRIPHOSPHATE; MITOCHONDRIAL PROTEIN; PROTEIN DRP1; SERINE; UNCLASSIFIED DRUG; AKAP1 PROTEIN, RAT; DRP1 PROTEIN, RAT; DYNAMIN; FORSKOLIN;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; BRAIN NERVE CELL; CELL ASSAY; CELL SURVIVAL; CONTROLLED STUDY; CORPUS STRIATUM; GENE OVEREXPRESSION; HIPPOCAMPUS; HUMAN; HUMAN CELL; HYDROLYSIS; IN VITRO STUDY; IN VIVO STUDY; MITOCHONDRIAL ELONGATION; MITOCHONDRIAL FRAGMENTATION; MITOCHONDRIAL FUSION; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL SHAPE; MITOCHONDRION; NERVE CELL NECROSIS; NEUROPROTECTION; NONHUMAN; OLIGOMERIZATION; OUTER MEMBRANE; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RAT; RNA INTERFERENCE; ANIMAL; APOPTOSIS; CELL CULTURE; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; ENZYMOLOGY; HOMEOSTASIS; METABOLISM; NERVE CELL; ORGANELLE SHAPE; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN MULTIMERIZATION; PROTEIN TRANSPORT;

A KINASE ANCHOR PROTEINS; ANIMALS; APOPTOSIS; CELL SURVIVAL; CELLS, CULTURED; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DYNAMINS; FORSKOLIN; HIPPOCAMPUS; HOMEOSTASIS; HUMANS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; NEURONS; ORGANELLE SHAPE; PHOSPHORYLATION; PROTEIN MULTIMERIZATION; PROTEIN TRANSPORT; RATS;

EID: 79955487757     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1000612     Document Type: Article

References (61)

1. Chen H, Chan D. C, (2009) Mitochondrial dynamics-fusion, fission, movement, and mitophagy-in neurodegenerative diseases. Hum Mol Genet 18: R169-R176.
2. Wasilewski M, Scorrano L, (2009) The changing shape of mitochondrial apoptosis. Trends Endocrinol Metab 20: 287-294.
3. Suen D. F, Norris K. L, Youle R. J, (2008) Mitochondrial dynamics and apoptosis. Genes Dev 22: 1577-1590.
4. Hoppins S, Lackner L, Nunnari J, (2007) The machines that divide and fuse mitochondria. Annu Rev Biochem 76: 751-780.
5. Otera H, Wang C, Cleland M. M, Setoguchi K, Yokota S, et al. (2010) Mff is an essential factor for mitochondrial recruitment of Drp1 during mitochondrial fission in mammalian cells. J Cell Biol 191: 1141-1158.
6. Gandre-Babbe S, van der Bliek A. M, (2008) The novel tail-anchored membrane protein Mff controls mitochondrial and peroxisomal fission in mammalian cells. Mol Biol Cell 19: 2402-2412.
7. Zuchner S, Mersiyanova I. V, Muglia M, Bissar-Tadmouri N, Rochelle J, et al. (2004) Mutations in the mitochondrial GTPase mitofusin 2 cause Charcot-Marie-Tooth neuropathy type 2A. Nat Genet 36: 449-451.
8. Alexander C, Votruba M, Pesch U. E, Thiselton D. L, Mayer S, et al. (2000) OPA1, encoding a dynamin-related GTPase, is mutated in autosomal dominant optic atrophy linked to chromosome 3q28. Nat Genet 26: 211-215.
9. Delettre C, Lenaers G, Griffoin J. M, Gigarel N, Lorenzo C, et al. (2000) Nuclear gene OPA1, encoding a mitochondrial dynamin-related protein, is mutated in dominant optic atrophy. Nat Genet 26: 207-210.
10. Waterham H. R, Koster J, van Roermund C. W, Mooyer P. A, Wanders R. J, et al. (2007) A lethal defect of mitochondrial and peroxisomal fission. N Engl J Med 356: 1736-1741.
11. Davies V. J, Hollins A. J, Piechota M. J, Yip W, Davies J. R, et al. (2007) Opa1 deficiency in a mouse model of autosomal dominant optic atrophy impairs mitochondrial morphology, optic nerve structure and visual function. Hum Mol Genet 16: 1307-1318.
12. Chen H, Detmer S. A, Ewald A. J, Griffin E. E, Fraser S. E, et al. (2003) Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. J Cell Biol 160: 189-200.
13. Ishihara N, Nomura M, Jofuku A, Kato H, Suzuki S. O, et al. (2009) Mitochondrial fission factor Drp1 is essential for embryonic development and synapse formation in mice. Nat Cell Biol 11: 958-966.
14. Wakabayashi J, Zhang Z, Wakabayashi N, Tamura Y, Fukaya M, et al. (2009) The dynamin-related GTPase Drp1 is required for embryonic and brain development in mice. J Cell Biol 186: 805-816.
15. Cho D. H, Nakamura T, Fang J, Cieplak P, Godzik A, et al. (2009) S-nitrosylation of Drp1 mediates beta-amyloid-related mitochondrial fission and neuronal injury. Science 324: 102-105.
16. Santel A, Frank S, (2008) Shaping mitochondria: The complex posttranslational regulation of the mitochondrial fission protein DRP1. IUBMB Life 60: 448-455.
17. Cereghetti G. M, Stangherlin A, Martins de Brito O, Chang C. R, Blackstone C, et al. (2008) Dephosphorylation by calcineurin regulates translocation of Drp1 to mitochondria. Proc Natl Acad Sci U S A 105: 15803-15808.
18. Cribbs J. T, Strack S, (2007) Reversible phosphorylation of Drp1 by cyclic AMP-dependent protein kinase and calcineurin regulates mitochondrial fission and cell death. EMBO Rep 8: 939-944.
19. Chang C. R, Blackstone C, (2007) Cyclic AMP-dependent protein kinase phosphorylation of Drp1 regulates its GTPase activity and mitochondrial morphology. J Biol Chem 282: 21583-21587.
20. Han X. J, Lu Y. F, Li S. A, Kaitsuka T, Sato Y, et al. (2008) CaM kinase I alpha-induced phosphorylation of Drp1 regulates mitochondrial morphology. J Cell Biol 182: 573-585.
21. Dagda R. K, Merrill R. A, Cribbs J. T, Chen Y, Hell J. W, et al. (2008) The spinocerebellar ataxia 12 gene product and protein phosphatase 2A regulatory subunit Bbeta2 antagonizes neuronal survival by promoting mitochondrial fission. J Biol Chem 283: 36241-36248.
22. Cribbs J. T, Strack S, (2009) Functional characterization of phosphorylation sites in dynamin-related protein 1. Methods Enzymol 457: 231-253.
23. Smith F. D, Langeberg L. K, Scott J. D, (2006) The where's and when's of kinase anchoring. Trends Biochem Sci 31: 316-323.
24. Affaitati A, Cardone L, de Cristofaro T, Carlucci A, Ginsberg M. D, et al. (2003) Essential role of A-kinase anchor protein 121 for cAMP signaling to mitochondria. J Biol Chem 278: 4286-4294.
25. Newhall K. J, Criniti A. R, Cheah C. S, Smith K. C, Kafer K. E, et al. (2006) Dynamic anchoring of PKA is essential during oocyte maturation. Curr Biol 16: 321-327.
26. Feliciello A, Gottesman M. E, Avvedimento E. V, (2005) cAMP-PKA signaling to the mitochondria: protein scaffolds, mRNA and phosphatases. Cell Signal 17: 279-287.
27. McNally J. G, (2008) Quantitative FRAP in analysis of molecular binding dynamics in vivo. Methods Cell Biol 85: 329-351.
28. Lackner L. L, Nunnari J. M, (2009) The molecular mechanism and cellular functions of mitochondrial division. Biochim Biophys Acta 1792: 1138-1144.
29. Chappie J. S, Acharya S, Leonard M, Schmid S. L, Dyda F, (2010) G domain dimerization controls dynamin's assembly-stimulated GTPase activity. Nature 465: 435-440.
30. Song B. D, Leonard M, Schmid S. L, (2004) Dynamin GTPase domain mutants that differentially affect GTP binding, GTP hydrolysis, and clathrin-mediated endocytosis. J Biol Chem 279: 40431-40436.
31. Sbalzarini I. F, Koumoutsakos P, (2005) Feature point tracking and trajectory analysis for video imaging in cell biology. J Struct Biol 151: 182-195.
32. Harada H, Becknell B, Wilm M, Mann M, Huang L. J, et al. (1999) Phosphorylation and inactivation of BAD by mitochondria-anchored protein kinase A. Mol Cell 3: 413-422.
33. Roy S. S, Madesh M, Davies E, Antonsson B, Danial N, et al. (2009) Bad targets the permeability transition pore independent of Bax or Bak to switch between Ca2+-dependent cell survival and death. Mol Cell 33: 377-388.
34. Schauss A. C, Huang H, Choi S. Y, Xu L, Soubeyrand S, et al. (2010) A novel cell-free mitochondrial fusion assay amenable for high-throughput screenings of fusion modulators. BMC Biol 8: 100.
35. Ma Y, Taylor S. S, (2008) A molecular switch for targeting between endoplasmic reticulum (ER) and mitochondria: conversion of a mitochondria-targeting element into an ER-targeting signal in DAKAP1. J Biol Chem 283: 11743-11751.
36. Cardone L, Carlucci A, Affaitati A, Livigni A, DeCristofaro T, et al. (2004) Mitochondrial AKAP121 binds and targets protein tyrosine phosphatase D1, a novel positive regulator of src signaling. Mol Cell Biol 24: 4613-4626.
37. Rogne M, Stokka A. J, Tasken K, Collas P, Kuntziger T, (2009) Mutually exclusive binding of PP1 and RNA to AKAP149 affects the mitochondrial network. Hum Mol Genet 18: 978-987.
38. Abrenica B, AlShaaban M, Czubryt M. P, (2009) The A-kinase anchor protein AKAP121 is a negative regulator of cardiomyocyte hypertrophy. J Mol Cell Cardiol 46: 674-681.
39. Ginsberg M. D, Feliciello A, Jones J. K, Avvedimento E. V, Gottesman M. E, (2003) PKA-dependent binding of mRNA to the mitochondrial AKAP121 protein. J Mol Biol 327: 885-897.
40. Livigni A, Scorziello A, Agnese S, Adornetto A, Carlucci A, et al. (2006) Mitochondrial AKAP121 links cAMP and src signaling to oxidative metabolism. Mol Biol Cell 17: 263-271.
41. Carlucci A, Adornetto A, Scorziello A, Viggiano D, Foca M, et al. (2008) Proteolysis of AKAP121 regulates mitochondrial activity during cellular hypoxia and brain ischaemia. Embo J 27: 1073-1084.
42. Barsoum M. J, Yuan H, Gerencser A. A, Liot G, Kushnareva Y, et al. (2006) Nitric oxide-induced mitochondrial fission is regulated by dynamin-related GTPases in neurons. EMBO Journal 25: 3900-3911.
43. Wasiak S, Zunino R, McBride H. M, (2007) Bax/Bak promote sumoylation of DRP1 and its stable association with mitochondria during apoptotic cell death. J Cell Biol 177: 439-450.
44. Zunino R, Braschi E, Xu L, McBride H. M, (2009) Translocation of SenP5 from the nucleoli to the mitochondria modulates DRP1-dependent fission during mitosis. J Biol Chem 284: 17783-17795.
45. Figueroa-Romero C, Iniguez-Lluhi J. A, Stadler J, Chang C. R, Arnoult D, et al. (2009) SUMOylation of the mitochondrial fission protein Drp1 occurs at multiple nonconsensus sites within the B domain and is linked to its activity cycle. Faseb J 23: 3917-3927.
46. Wang X, Su B, Lee H. G, Li X, Perry G, et al. (2009) Impaired balance of mitochondrial fission and fusion in Alzheimer's disease. J Neurosci 29: 9090-9103.
47. Bashkirov P. V, Akimov S. A, Evseev A. I, Schmid S. L, Zimmerberg J, et al. (2008) GTPase cycle of dynamin is coupled to membrane squeeze and release, leading to spontaneous fission. Cell 135: 1276-1286.
48. Pucadyil T. J, Schmid S. L, (2008) Real-time visualization of dynamin-catalyzed membrane fission and vesicle release. Cell 135: 1263-1275.
49. Mitra K, Wunder C, Roysam B, Lin G, Lippincott-Schwartz J, (2009) A hyperfused mitochondrial state achieved at G1-S regulates cyclin E buildup and entry into S phase. Proc Natl Acad Sci U S A 106: 11960-11965.
50. Brooks C, Cho S. G, Wang C. Y, Yang T, Dong Z, (2011) Fragmented mitochondria are sensitized to Bax insertion and activation during apoptosis. Am J Physiol Cell Physiol 300: C447-C455.
51. Frieden M, James D, Castelbou C, Danckaert A, Martinou J. C, et al. (2004) Ca(2+) homeostasis during mitochondrial fragmentation and perinuclear clustering induced by hFis1. J Biol Chem 279: 22704-22714.
52. Neuspiel M, Zunino R, Gangaraju S, Rippstein P, McBride H, (2005) Activated mitofusin 2 signals mitochondrial fusion, interferes with Bax activation, and reduces susceptibility to radical induced depolarization. J Biol Chem 280: 25060-25070.
53. Karbowski M, Lee Y. J, Gaume B, Jeong S. Y, Frank S, et al. (2002) Spatial and temporal association of Bax with mitochondrial fission sites, Drp1, and Mfn2 during apoptosis. Journal of Cell Biology 159: 931-938.
54. Bok J, Zha X. M, Cho Y. S, Green S. H, (2003) An extranuclear locus of cAMP-dependent protein kinase action is necessary and sufficient for promotion of spiral ganglion neuronal survival by cAMP. J Neurosci 23: 777-787.
55. Dobson S, Kumar R, Bracchi-Ricard V, Freeman S, Al-Murrani S. W, et al. (2003) Characterization of a unique aspartate-rich protein of the SET/TAF-family in the human malaria parasite, Plasmodium falciparum, which inhibits protein phosphatase 2A. Molecular & Biochemical Parasitology 126: 239-250.
56. Reynolds A, Leake D, Boese Q, Scaringe S, Marshall W. S, et al. (2004) Rational siRNA design for RNA interference. Nature Biotechnology 22: 326-330.
57. Brummelkamp T. R, Bernards R, Agami R, (2002) A system for stable expression of short interfering RNAs in mammalian cells. Science 296: 550-553.
58. Gonzalez-Alegre P, Bode N, Davidson B. L, Paulson H. L, (2005) Silencing primary dystonia: lentiviral-mediated RNA interference therapy for DYT1 dystonia. J Neurosci 25: 10502-10509.
59. Strack S, Ruediger R, Walter G, Dagda R. K, Barwacz C. A, et al. (2002) Protein phosphatase 2A holoenzyme assembly. Identification of contacts between B-family regulatory and scaffolding A subunits. J Biol Chem 277: 20750-20755.
60. Lim I. A, Merrill M. A, Chen Y, Hell J. W, (2003) Disruption of the NMDA receptor-PSD-95 interaction in hippocampal neurons with no obvious physiological short-term effect. Neuropharmacology 45: 738-754.
61. Bolte S, Cordelieres F. P, (2006) A guided tour into subcellular colocalization analysis in light microscopy. J Microsc 224: 213-232.