MAP4 mechanism that stabilizes mitochondrial permeability transition in hypoxia: Microtubule enhancement and DYNLT1 interaction with VDAC1

PLoS ONE

Volumn 6, Issue 12, 2011, Pages

  Fang, Ya dong ^a   Xu, Xue ^b   Dang, Yong ming ^a   Zhang, Yi ming ^a   Zhang, Jia ping ^a   Hu, Jiong yu ^a   Zhang, Qiong ^a   Dai, Xia ^a   Teng, Miao ^a   Zhang, Dong xia ^a   Huang, Yue sheng ^a  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

^b 324 Hospital of PLA   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; ALPHA TUBULIN; DYNEIN ADENOSINE TRIPHOSPHATASE; DYNEIN LIGHT CHAIN TCTEX TYPE 1; MICROTUBULE ASSOCIATED PROTEIN 4; TUBULIN; UNCLASSIFIED DRUG; VOLTAGE DEPENDENT ANION CHANNEL 1; DYNLT1 PROTEIN, HUMAN; GREEN FLUORESCENT PROTEIN; MAP4; MICROTUBULE ASSOCIATED PROTEIN; RECOMBINANT PROTEIN; VDAC1 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL VIABILITY; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; CYTOSOL; ENERGY METABOLISM; HEART MUSCLE CELL; HUMAN; HUMAN CELL; HYPOXIA; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; MEMBRANE DAMAGE; MICROTUBULE; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL PERMEABILITY; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN POLYMERIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; RAT; TWO HYBRID SYSTEM; UPREGULATION; WESTERN BLOTTING; ANIMAL; ANOXIA; CELL SURVIVAL; CONFOCAL MICROSCOPY; GENE EXPRESSION REGULATION; HELA CELL; METABOLISM; METHODOLOGY; MITOCHONDRION; PERMEABILITY; SPRAGUE DAWLEY RAT;

ADENOSINE TRIPHOSPHATE; ANIMALS; ANOXIA; CELL SURVIVAL; DYNEINS; GENE EXPRESSION REGULATION; GREEN FLUORESCENT PROTEINS; HELA CELLS; HUMANS; MICROSCOPY, CONFOCAL; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MITOCHONDRIA; PERMEABILITY; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT PROTEINS; TWO-HYBRID SYSTEM TECHNIQUES; VOLTAGE-DEPENDENT ANION CHANNEL 1;

EID: 82555173722     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0028052     Document Type: Article

References (47)

1. Henze K, Martin W, (2003) Evolutionary biology: essence of mitochondria. Nature 426: 127-128.
2. McBride HM, Neuspiel M, Wasiak S, (2006) Mitochondria: More than just a powerhouse. Curr Biol 16: R551-R560.
3. Lesnefsky EJ, Moghaddas S, Tandler B, Kerner J, Hoppel CL, (2001) Mitochondrial dysfunction in cardiac disease: ischemia-reperfusion, aging, and heart failure. J Mol Cell Cardiol 33: 1065-1089.
4. White RJ, Reynolds IJ, (1996) Mitochondrial depolarization in glutamate-stimulated neurons: an early signal specific to excitotoxin exposure. J Neurosci 16: 5688-5697.
5. Cao LC, Honeyman TW, Cooney R, Kennington L, Scheid CR, et al. (2004) Mitochondrial dysfunction is a primary event in renal cell oxalate toxicity. Kidney Int 66: 1890-1900.
6. Stavrovskaya IG, Kristal BS, (2005) The powerhouse takes control of the cell: is the mitochondrial permeability transition a viable therapeutic target against neuronal dysfunction and death? Free Radic Biol Med 38: 687-697.
7. Quinsay MN, Thomas RL, Lee Y, Gustafsson AB, (2010) Bnip3-mediated mitochondrial autophagy is independent of the mitochondrial permeability transition pore. Autophagy 6: 855-862.
8. Rasola A, Bernardi P, (2007) The mitochondrial permeability transition pore and its involvement in cell death and in disease pathogenesis. Apoptosis 12: 815-833.
9. Baines CP, Kaiser RA, Sheiko T, Craigen WJ, Molkentin JD, (2007) Voltage-dependent anion channels are dispensable for mitochondrial-dependent cell death. Nat Cell Biol 9: 550-U122.
10. Tomasello F, Messina A, Lartigue L, Schembri L, Medina C, et al. (2009) Outer membrane VDAC1 controls permeability transition of the inner mitochondrial membrane in cellulo during stress-induced apoptosis. Cell Res 19: 1363-1376.
11. Shoshan-Barmatz V, Keinan N, Abu-Hamad S, Tyomkin D, Aram L, (2010) Apoptosis is regulated by the VDAC1 N-terminal region and by VDAC oligomerization: release of cytochrome c, AIF and Smac/Diablo. BBA-Bioenergetics 1797: 1281-1291.
12. Krestinina OV, Grachev DE, Odinokova IV, Reiser G, Evtodienko YV, et al. (2009) Effect of peripheral benzodiazepine receptor (PBR/TSPO) ligands on opening of Ca2+-induced pore and phosphorylation of 3.5-kDa polypeptide in rat brain mitochondria. Biochemistry-Moscow+ 74: 421-429.
13. Webster DR, (1997) Regulation of post-translationally modified microtubule populations during neonatal cardiac development. J Mol Cell Cardiol 29: 1747-1761.
14. Rogers SL, Gelfand VI, (2000) Membrane trafficking, organelle transport, and the cytoskeleton. Curr Opin Cell Biol 12: 57-62.
15. Sato H, Hori M, Kitakaze M, Iwai K, Takashima S, et al. (1993) Reperfusion after brief ischemia disrupts the microtubule network in canine hearts. Circ Res 72: 361-375.
16. Akhmanova A, Steinmetz MO, (2008) Tracking the ends: a dynamic protein network controls the fate of microtubule tips. Nat Rev Mol Cell Bio 9: 309-322.
17. Al-Bassam J, Ozer RS, Safer D, Halpain S, Milligan RA, (2002) MAP2 and tau bind longitudinally along the outer ridges of microtubule protofilaments. J Cell Biol 157: 1187-1196.
18. Morrison EE, (2007) Action and interactions at microtubule ends. Cell Mol Life Sci 64: 307-317.
19. Permana S, Hisanaga S, Nagatomo Y, Iida J, Hotani H, et al. (2005) Truncation of the projection domain of MAP4 (microtubule-associated protein 4) leads to attenuation of microtubule dynamic instability. Cell Struct Funct 29: 147-157.
20. Takahashi M, Shiraishi H, Ishibashi Y, Blade KL, McDermott PJ, et al. (2003) Phenotypic consequences of beta1-tubulin expression and MAP4 decoration of microtubules in adult cardiocytes. Am J Physiol Heart Circ Physiol 285: H2072-2083.
21. Sato H, Nagai T, Kuppuswamy D, Narishige T, Koide M, et al. (1997) Microtubule stabilization in pressure overload cardiac hypertrophy. J Cell Biol 139: 963-973.
22. Li DD, Marks JD, Schumacker PT, Young RM, Brorson JR, (2005) Physiological hypoxia promotes survival of cultured cortical neurons. Eur J Neurosci 22: 1319-1326.
23. Hu JY, Chu ZG, Han J, Dang YM, Yan H, et al. (2010) The p38/MAPK pathway regulates microtubule polymerization through phosphorylation of MAP4 and Op18 in hypoxic cells. Cell Mol Life Sci 67: 321-333.
24. Hendrickson WA, Williams JC, Roulhac PL, Roy AG, Vallee RB, et al. (2007) Structural and thermodynamic characterization of a cytoplasmic dynein light chain-intermediate chain complex. P Natl Acad Sci USA 104: 10028-10033.
25. Barbar E, Hall J, Karplus PA, (2009) Multivalency in the Assembly of Intrinsically Disordered Dynein Intermediate Chain. J Biol Chem 284: 33115-33121.
26. Carter AP, Cho C, Jin L, Vale RD, (2011) Crystal structure of the dynein motor domain. Science 331: 1159-1165.
27. Schwarzer C, Barnikol-Watanabe S, Thinnes FP, Hilschmann N, (2002) Voltage-dependent anion-selective channel (VDAC) interacts with the dynein light chain Tctex1 and the heat-shock protein PBP74. Int J Biochem Cell Biol 34: 1059-1070.
28. Kapitein LC, Schlager MA, Kuijpers M, Wulf PS, van Spronsen M, et al. (2010) Mixed Microtubules Steer Dynein-Driven Cargo Transport into Dendrites. Curr Biol 20: 290-299.
29. McNaughton L, Tikhonenko I, Banavali NK, LeMaster DM, Koonce MP, (2010) A Low Affinity Ground State Conformation for the Dynein Microtubule Binding Domain. J Biol Chem 285: 15994-16002.
30. Cheng G, Iijima Y, Ishibashi Y, Kuppuswamy D, Cooper Gt, (2002) Inhibition of G protein-coupled receptor trafficking in neuroblastoma cells by MAP 4 decoration of microtubules. Am J Physiol Heart Circ Physiol 283: H2379-2388.
31. Rostovtseva TK, Sheldon KL, Hassanzadeh E, Monge C, Saks V, et al. (2008) Tubulin binding blocks mitochondrial voltage-dependent anion channel and regulates respiration. P Natl Acad Sci USA 105: 18746-18751.
32. Maldonado EN, Patnaik J, Mullins MR, Lemasters JJ, (2010) Free Tubulin Modulates Mitochondrial Membrane Potential in Cancer Cells. Cancer Res 70: 10192-10201.
33. Nadano D, Nakayama J, Matsuzawa S, Sato TA, Matsuda T, et al. (2002) Human tastin, a proline-rich cytoplasmic protein, associates with the microtubular cytoskeleton. Biochem J 364: 669-677.
34. Nagano F, Orita S, Sasaki T, Naito A, Sakaguchi G, et al. (1998) Interaction of Doc2 with tctex-1, a light chain of cytoplasmic dynein- Implication in dynein-dependent vesicle transport. J Biol Chem 273: 30065-30068.
35. Chuang JZ, Yeh TY, Bollati F, Conde C, Canavosio F, et al. (2005) The dynein light chain Tctex-1 has a dynein-independent role in actin remodeling during neurite outgrowth. Dev Cell 9: 75-86.
36. Lange S, Auerbach D, McLoughlin P, Perriard E, Schafer BW, et al. (2002) Subcellular targeting of metabolic enzymes to titin in heart muscle may be mediated by DRAL/FHL-2. J Cell Sci 115: 4925-4936.
37. Seko Y, Takahashi N, Tobe K, Kadowaki T, Yazaki Y, (1997) Hypoxia and hypoxia/reoxygenation activate p65PAK, p38 mitogen-activated protein kinase (MAPK), and stress-activated protein kinase (SAPK) in cultured rat cardiac myocytes. Biochem Biophys Res Commun 239: 840-844.
38. Vandroux D, Schaeffer C, Tissier C, Lalande A, Bes S, et al. (2004) Microtubule alteration is an early cellular reaction to the metabolic challenge in ischemic cardiomyocytes. Mol Cell Biochem 258: 99-108.
39. Feng P, Liang C, Shin YC, Xiaofei E, Zhang W, et al. (2007) A novel inhibitory mechanism of mitochondrion-dependent apoptosis by a herpesviral protein. PLoS Pathog 3: e174.
40. Paddison PJ, Cleary M, Silva JM, Chang K, Sheth N, et al. (2004) Cloning of short hairpin RNAs for gene knockdown in mammalian cells. Nat Methods 1: 163-167.
41. Cheng TL, Chang WT, (2007) Construction of simple and efficient DNA vector-based short hairpin RNA expression systems for specific gene silencing in mammalian cells. Methods Mol Biol 408: 223-241.
42. Putnam AJ, Cunningham JJ, Dennis RG, Linderman JJ, Mooney DJ, (1998) Microtubule assembly is regulated by externally applied strain in cultured smooth muscle cells. J Cell Sci 111: 3379-3387.
43. Saeed U, Durgadoss L, Valli RK, Joshi DC, Joshi PG, et al. (2008) Knockdown of cytosolic glutaredoxin 1 leads to loss of mitochondrial membrane potential: implication in neurodegenerative diseases. PLoS One 3: e2459.
44. Scharstuhl A, Mutsaers HA, Pennings SW, Russel FG, Wagener FA, (2009) Involvement of VDAC, Bax and ceramides in the efflux of AIF from mitochondria during curcumin-induced apoptosis. PLoS One 4: e6688.
45. Zhdanov AV, Dmitriev RI, Papkovsky DB, (2011) Bafilomycin A1 activates respiration of neuronal cells via uncoupling associated with flickering depolarization of mitochondria. Cell Mol Life Sci 68: 903-917.
46. Petronilli V, Miotto G, Canton M, Brini M, Colonna R, et al. (1999) Transient and long-lasting openings of the mitochondrial permeability transition pore can be monitored directly in intact cells by changes in mitochondrial calcein fluorescence. Biophys J 76: 725-734.
47. Petronilli V, Penzo D, Scorrano L, Bernardi P, Di Lisa F, (2001) The mitochondrial permeability transition, release of cytochrome c and cell death. Correlation with the duration of pore openings in situ. J Biol Chem 276: 12030-12034.