Nek1 regulates cell death and mitochondrial membrane permeability through phosphorylation of VDAC1

Cell Cycle

Volumn 8, Issue 2, 2009, Pages 257-267

  Chen, Yumay ^a   Craigen, William J ^c   Riley, Daniel J ^a,b,d  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^b Mays Cancer Center at UT Health San Antonio   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

^d SOUTH TEXAS VETERANS HEALTH CARE SYSTEM   (United States)

Author keywords

Apoptosis; Cytochrome c; DNA damage; Kat mouse; Nek1; Polycystic kidney disease; VDAC1

Indexed keywords

GLUTATHIONE; MATRIX METALLOPROTEINASE; NIMA RELATED PROTEIN KINASE 1; PROTEIN KINASE; SERINE; SERINE 193; UNCLASSIFIED DRUG; VOLTAGE DEPENDENT ANION CHANNEL 1;

ANIMAL EXPERIMENT; ARTICLE; CELL DEATH; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DNA DAMAGE; IMMUNOPRECIPITATION; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL PERMEABILITY; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; ULTRAVIOLET IRRADIATION; YEAST;

MAMMALIA;

EID: 58549095067     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.8.2.7551     Document Type: Article

References (54)

1. Wang X. The expanding role of mitochondria in apoptosis. Genes Dev 2001; 15:2922-33.
2. Vander Heiden MG, Thompson CB. Bcl-2 proteins: regulators of apoptosis or of mitochondrial homeostasis? Nat Cell Biol 1999; 1:209-16.
3. Kroemer G, Zamzami N, Susin SA. Mitochondrial control of apoptosis. Immunol Today 1997; 18:44-51.
4. Crompton M. The mitochondrial permeability transition pore and its role in cell death. Biochem J 1999; 341:233-49.
5. Crompton M. Mitochondrial intermembrane junctional complexes and their role in cell death. J Physiol 2000; 529:11-21.
6. Shimizu S, Narita M, Tsujimoto Y. Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC. Nature 1999; 399:483-7.
7. Rostovtseva TK, Antonsson B, Suzuki M, Youle RJ, Colombini M, Bezrukov SM. Bid, but not Bax, regulates VDAC channels. J Biol Chem 2004; 279:13575-83.
8. Rostovtseva TK, Tan W, Colombini M. On the role of VDAC in apoptosis: fact and fiction. J Bioenerg Biomembr 2005; 37:129-42.
9. Colombini M. VDAC: the channel at the interface between mitochondria and the cytosol. Mol Cell Biochem 2004; 257:107-15.
10. Green DR, Kroemer G. The pathophysiology of mitochondrial cell death. Science 2004; 305:626-9.
11. Halestrap A. Biochemistry: a pore way to die. Nature 2005; 434:578-9.
12. Slee EA, Harte MT, Kluck RM, Wolf BB, Casiano CA, Newmeyer DD, et al. Ordering the cytochrome c-initiated caspase cascade: hierarchical activation of caspases-2, -3, -6, -7, -8 and -10 in a caspase-9-dependent manner. J Cell Biol 1999; 144:281-92.
13. Goldstein JC, Waterhouse NJ, Juin P, Evan GI, Green DR. The coordinate release of cytochrome c during apoptosis is rapid, complete and kinetically invariant. Nat Cell Biol 2000; 2:156-62.
14. Vander Heiden MG, Chandel NS, Li XX, Schumacker PT, Colombini M, Thompson CB. Outer mitochondrial membrane permeability can regulate coupled respiration and cell survival. Proc Natl Acad Sci USA 2000; 97:4666-71.
15. L promotes the open configuration of the voltage-dependent anion channel and metabolite passage through the outer mitochondrial membrane. J Biol Chem 2001; 276:19414-9.
16. Tsujimoto Y, Shimizu S. The voltage-dependent anion channel: an essential player in apoptosis. Biochimie 2002; 84:187-93.
17. Zoratti M, Szabo I. The mitochondrial permeability transition. Biochim Biophys Acta 1995; 1241:139-76.
18. Baines CP, Kaiser RA, Kaiser RA, Sheiko T, Craigen WJ, Molkentin JD. Voltage-dependent anion channels are dispensable for mitochondrial-dependent cell death. Nat Cell Biol 2007; 9:550-5.
19. Basso E, Fante L, Fowlkes J, Petronilli V, Forte MA, Bernardi P. Properties of the permeability transition pore in mitochondria devoid of cyclophilin D. J Biol Chem 2005; 280:18558-61.
20. Nakagawa T, Shimizu S, Watanabe T, Yamaguchi O, Otsu K, Yamagata H, et al. Cyclophilin D-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death. Nature 2005; 434:652-8.
21. Schinzel AC, Takeuchi O, Huang Z, Fisher JK, Zhou Z, Rubens J, et al. Cyclophilin D is a component of mitochondrial permeability transition and mediates neuronal cell death after focal cerebral ischemia. Proc Natl Acad Sci USA 2005; 102:12005-10.
22. Halestrap AP, Brennerb C. The adenine nucleotide translocase: a central component of the mitochondrial permeability transition pore and key player in cell death. Curr Med Chem 2003; 10:1507-25.
23. Zoratti M, Szabo I, DeMarchi U. Mitochondrial permeability transitions: how many doors to the house? Biochim Biophys Acta 2005; 1706:40-52.
24. Abu-Hamad S, Zaid H, Israelson A, Nahon E, Shoshan-Barmatz V. Hexokinase-I protection against apoptotic cell death is mediated via interaction with the voltage-dependent anion channel-1: mapping the site of binding. J Biol Chem 2008; 283:13482-90.
25. Azoulay-Zohar H, Israelson A, Abu-Hamad S, Shoshan-Barmatz V. In self-defence: hexokinase promotes voltage-dependent anion channel closure and prevents mitochondria-mediated apoptotic cell death. Biochem J 2004; 377:347-55.
26. Sun L, Shukair S, Naik TJ, Moazed F, Ardehali H. Glucose phosphorylation and mitochondrial binding are required for the protective effects of hexokinases I and II. Mol Cell Biol 2008; 28:1007-17.
27. Bera AK, Ghosh S, Das S. Mitochondrial VDAC can be phosphorylated by cyclic AMP-dependent protein kinase. Biochem Biophys Res Commun 1995; 209:213-7.
28. 2-specific gene that encodes a potential protein kinase. Cell 1988; 53:237-44.
29. Osmani AH, McGuire SL, Osmani SA. Parallel activation of the NIMA and p34cdc2 cell cycle-regulated protein kinases is required to initiate mitosis in A. nidulans. Cell 1991; 67:283-91.
30. O'Connell MJ, Krien MJ, Hunter T. Never say never. The NIMA-related protein kinases in mitotic control. Trends Cell Biol 2003; 13:221-8.
31. Quarmby LM, Mahjoub MR. Caught Nek-ing: cilia and centrioles. J Cell Sci 2005; 118:5161-9.
32. Letwin K, Mizzen L, Motro B, Ben-David Y, Bernstein A, Pawson T. A mammalian dual specificity protein kinase, Nek1, is related to the NIMA cell cycle regulator and highly expressed in meiotic germ cells. EMBO J 1992; 11:3521-31.
33. Polci R, Peng A, Chen P-L, Riley DJ, Chen Y. NIMA-related protein kinase 1 is involved early in the ionizing radiation-induced DNA damage response. Cancer Res 2004; 64:8800-3.
34. Chen Y, Chen P-L, Chen C-F, Jiang X, Riley DJ. Never-in-mitosis related kinase 1 functions in DNA damage response and checkpoint control. Cell Cycle 2008; 7:3194-201.
35. Surpili MJ, Delben TM, Kobarg J. Identification of proteins that interact with the central coiled-coil region of the human protein kinase NEK1. Biochemistry 2003; 42:15369-76.
36. Feige E, Shalom O, Tsuriel S, Yissachar N, Motro B. Nek1 shares structural and functional similarities with NIMA kinase. Biochim Biophys Acta 2006; 1763:272-81.
37. Oakley BR, Morris NR. A mutation in Aspergillus nidulans that blocks the transition from interphase to prophase. J Cell Biol 1983; 96:1155-8.
38. Chen Y, Riley DJ, Zheng L, Chen P-L, Lee W-H. Phosphorylation of the mitotic regulator protein Hec1 by Nek2 kinase is essential for faithful chromosome segregation. J Biol Chem 2002; 277:49408-16.
39. Bayrhuber M, Meins T, Habeck M, Becker S, Giller K, Villinger S, et al. Structure of the human voltage-dependent anion channel. Proc Natl Acad Sci USA 2008; 105:15370-5.
40. Hiller S, Garces RG, Malia TJ, Orekho VY, Colombini M, Wagner G. Solution structure of the integral human membrane protein VDAC-1 in detergent micelles. Science 2008; 321:1206-10.
41. Lu KP, Kemp BE, Means AR. Identification of substrate specificity determinants for the cell cycle-regulated NIMA protein kinase. J Biol Chem 1994; 269:6603-7.
42. Songyang Z, Lu KP, Kwon YT, Tsai LH, Filhol O, Cochet C, et al. A structural basis for substrate specificities of protein Ser/Thr kinases: primary sequence preference of casein kinases I and II, NIMA, phosphorylase kinase, calmodulin-dependent kinase II, CDK5 and Erk1. Mol Cell Biol 1996; 16:6486-93.
43. Casadio R, Jacoboni I, Messina A, DePinto V. A 3D model of the voltage-dependent anion channel (VDAC). FEBS Lett 2002; 520:1-7.
44. Vogler C, Homan S, Pung A, Thorpe C, Barker J, Birkenmeier EH, et al. Clinical and pathologic findings in two new allelic murine models of polycystic kidney disease. J Am Soc Nephrol 1999; 10:2534-9.
45. Upadhya P, Birkenmeier EH, Birkenmeier CS, Barker JE. Mutations in a NIMA-related kinase gene, Nek1, cause pleiotropic effects including a progressive polycystic kidney disease in mice. Proc Natl Acad Sci USA 2000; 97:217-21.
46. Abu-Hamad S, Sivan S, Shoshan-Barmatz V. The expression level of the voltage-dependent anion channel controls life and death of the cell. Proc Natl Acad Sci USA 2006; 103:5787-92.
47. Woo D. Apoptosis and loss of renal tissue in polycystic kidney diseases. N Engl J Med 1995; 333:18-25.
48. Zhou XJ, Kukes G. Pathogenesis of autosomal dominant polycystic kidney disease: role of apoptosis. Diagn Mol Pathol 1998; 7:65-8.
49. Torres VE. Apoptosis in cystogenesis: hands on or hands off? Kidney Int 1999; 55:334-5.
50. Wu S, Sampson MJ, Decker WK, Craigen WJ. Each mammalian mitochondrial outer membrane porin protein is dispensable: effects on cellular respiration. Biochim Biophys Acta 1999; 1452:68-78.
51. Durfee T, Mancini MA, Jones D, Elledge SJ, Lee W-H. The amino-terminal region of the retinoblastoma gene product binds a novel nuclear matrix protein that co-localizes to centers for RNA processing. J Cell Biol 1994; 127:609-22.
52. Chen Y, Riley DJ, Chen P-L, Lee W-H. HEC, a novel nuclear protein rich in leucine heptad repeats specifically involved in mitosis. Mol Cell Biol 1997; 17:6049-56.
53. Cossarizza A, Baccarani-Contri M, Kalashnikova G, Franceschi C. A new method for the cytofluorimetric analysis of mitochondrial membrane potential using the J-aggregate forming lipophilic cation 5,5′,6,6′- tetrachloro-1,1′,3,3′-tetraethylbenzimidazolcarbocyanine iodide (JC-1). Biochem Biophys Res Commun 1993; 197:40-5.
54. Reers M, Smith TW, Chen LB. J-aggregate formation of a carbocyanine as a quantitative fluorescent indicator of membrane potential. Biochemistry 1991; 30:4480-6.