The ε-subunit of mitochondrial ATP synthase is required for normal spindle orientation during the drosophila embryonic divisions

Genetics

Volumn 170, Issue 2, 2005, Pages 697-708

  Kidd, Thomas ^a,d   Abu Shumays, Robin ^b,e   Katzen, Alisa ^c   Sisson, John C ^b,f   Jiménez, Gerardo ^a,g   Pinchin, Sheena ^a   Sullivan, William ^b   Ish Horowicz, David ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF ILLINOIS   (United States)

^d UNIVERSITY OF NEVADA   (United States)

^e SANTA CLARA UNIVERSITY   (United States)

^f UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^g INSTITUT DE BIOLOGIA MOLECULAR DE BARCELONA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ADENOSINE TRIPHOSPHATE; METHUSELAH RECEPTOR; MITOCHONDRIAL PROTEIN; MOLECULAR MOTOR; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE EPSILON; RECEPTOR; SUN PROTEIN; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATASE; DNA; LIGAND;

ARTICLE; CELL AGING; CELL DIVISION; CELL NUCLEUS; CENTROSOME; CORTICAL DIVISION; DROSOPHILA; EMBRYO DEATH; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; ENZYME SUBUNIT; EXTRACHROMOSOMAL INHERITANCE; GENE; GENE LOSS; GROWTH RETARDATION; INTERPHASE; LARVA; METAPHASE; MITOSIS SPINDLE; MUTATION; NONHUMAN; NUCLEOTIDE SEQUENCE; NULL ALLELE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; SUN GENE; TELOPHASE; ZYGOTE; AMINO ACID SEQUENCE; ANIMAL; BIOLOGICAL MODEL; CELL MOTION; CHEMICAL STRUCTURE; CHEMISTRY; CYTOSKELETON; ENZYMOLOGY; FEMALE; FLUORESCENCE MICROSCOPY; MALE; METABOLISM; MITOCHONDRION; MOLECULAR GENETICS; PHYSIOLOGY; PRENATAL DEVELOPMENT; SEQUENCE HOMOLOGY; ULTRASTRUCTURE;

ACTINS; ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; ANIMALS; CELL MOVEMENT; CELL NUCLEUS; CENTROSOME; CYTOSKELETON; DNA; DROSOPHILA; FEMALE; INTERPHASE; LIGANDS; MALE; MICROSCOPY, FLUORESCENCE; MITOCHONDRIA; MITOCHONDRIAL PROTON-TRANSLOCATING ATPASES; MITOTIC SPINDLE APPARATUS; MODELS, GENETIC; MODELS, MOLECULAR; MOLECULAR MOTOR PROTEINS; MOLECULAR SEQUENCE DATA; PHENOTYPE; SEQUENCE HOMOLOGY, AMINO ACID; TELOPHASE;

EID: 22144496852     PISSN: 00166731     EISSN: None     Source Type: Journal    
DOI: 10.1534/genetics.104.037648     Document Type: Article

References (58)

1. ASHBURNER, M., 1989 Drosophila: A Laboratory Handbook, pp. 345-346. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
2. BOWMAN, B. J., S. E. MAINZER, K. E. ALLEN and C. W. SLAYMAN, 1978 Effects of inhibitors on the plasma membrane and mitochondrial adenosine triphosphatases of Neurospora crassa. Biochim. Biophys. Acta 512: 13-28.
3. BOYER, P. D., 1997 The ATP synthase-a splendid molecular machine. Annu. Rev. Biochem. 66: 717-749.
4. BRITTON. J. S., and B. A. EDGAR, 1998 Environmental control of the cell cycle in Drosophila: nutrition activates mitotic and endoreplicative cells by distinct mechanisms. Development 125:2149-2158.
5. BRODSKY, M. H, J. J. SEKELSKY, G. TSANG, R. S. HAWLEY and G. M. RUBIN, 2000 mus304 encodes a novel DNA damage checkpoint protein required during Drosophila development. Genes Dev. 14: 666-678.
6. CHADWICK, B. P., T. RIDD, D. ISH-HOROWICZ and A. FRISCHAUF, 1999 Cloning, mapping and expression of HCG1, a novel ubiquitin-like gene. Gene 233: 189-195.
7. CHOU, T. B., and N. PERRIMON, 1992 Use of a yeast site-specific recombinase to produce female germline chimeras in Drosophila. Genetics 131: 643-653.
8. CVEJIC, S., Z. ZHU, S. J. FELICE, Y. BERMAN and X.-Y. HUANG, 2004 The endogenous ligand Stunted of the GPCR Methuselah extends lifespan in Drosophila. Nat. Cell Biol. 6: 540-546.
9. DE SAINT PHALLE, B., and W. SULLIVAN, 1998 Spindle assembly and mitosis without centrosomes in parthenogenetic Sciara embryos. J. Cell Biol. 141: 1383-1391.
10. DIGREGORIO, P. J., J. A. UBERSAX and P. H. O'FARRELL, 2001 Hypoxia and nitric oxide induce a rapid reversible cell cycle arrest of the Drosophila syncytial divisions. J. Biol. Chem. 276: 1930-1937.
11. ENDOW, S. A., and D. J. KOMMA, 1996 Centrosome and spindle function of the Drosophila Ned microtubule motor visualized in live embryos using Ncd-GFP fusion proteins. J. Cell Sci. 109: 2429-2442.
12. ENDOW, S. A., R. CHANDRA, D. J. KOMMA, A. H. YAMAMOTO and E. D. SALMON, 1994 Mutants of the Drosophila ncd microtubule motor protein cause centrosomal and spindle pole defects in mitosis. J. Cell Sci. 107: 859-867.
13. FINKEL, T., and N.J. HOLBROOK, 2000 Oxidants, oxidative stress and the biology of aging. Nature 408: 239-247.
14. FOE, V. E., G. M. ODELL and B. A. EDGAR, 1993 Mitosis and morphogenesis in the Drosophila embryo: point and counterpoint, pp. 149-300 in The Development of Drosophila melanogaster, edited by M. BATE and A. MARTINEZ-ARIAS. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
15. FOGARTY, P., S. D. CAMPBELL, R. ABU-SHUMAYS, B. S. PHALLE, K. R. YU et al., 1997 The Drosophila grapes gene is related to checkpoint gene chk1/rad27 and is required for late syncytial division fidelity. Curr. Biol. 7: 418-426.
16. FRENZ, L. M., and D. M. GLOVER, 1996 A maternal requirement for glutamine synthetase 1 for the mitotic cycles of syncytial Drosophila embryos. J. Cell Sci. 109: 2649-2660.
17. GALLONI, M., and B. A. EDGAR, 1999 Cell-autonomous and non-autonomous growth-defective mutants of Drosophila melanogaster. Development 126: 2365-2375.
18. GIOT, L., J. S. BADER, C. BROUWER, A. CHAUDHURI, B. KUANG et al., 2003 A protein interaction map of Drosophila melanogaster. Science 302: 1727-1736.
19. GIRARDOT, F., V. MONNIER and H. TRICOIRE, 2004 Genome wide analysis of common and specific stress responses in adult Drosophila melanogaster. BMC Genomics 5: 74.
20. HARI, K. L., A. SANTERRE, J. J. SEKELSKY, K. S. MCKIM, J, B. BOYD et al., 1995 The mei-41 gene of D. melanogaster is a structural and functional homologue of the human ataxia telangiectasia gene. Cell 82: 815-821.
21. HOCHACHKA, P. W., 2003 Intracellular convection, homeostasis and metabolic regulation. J. Exp. Biol. 206: 2001-2009.
22. JACOBS, H., R. STRATMANN and C. LEHNER, 1998 A screen for lethal mutations in the chromosomal region 59AB suggests that bell-wether encodes the alpha subunit of the mitochondrial ATP synthase in Drosophila. Mol. Gen. Genet. 259: 383-387.
23. KATAYOUN, A., B. STUART and S. A. WASSERMAN, 2000 Functional analysis of the Drosophila Diaphanous FH protein in early embryonic development. Development 127: 1887-1897.
24. KATZEN, A. L., and J. M. BISHOP, 1996 myb provides an essential function during Drosophila development. Proc. Natl. Acad. Sci. USA 93: 13955-13960.
25. KATZEN, A. L., T. B. KORNBERG and J. M. BISHOP, 1985 Isolation of the proto-oncogene c-myb from D. melanogaster. Cell 41:449-456.
26. KATZEN, A. L., J. JACKSON, B. P. HARMON, S. M. FUNG, G. RAMSAY et al., 1998 Drosophila myb is required for the G2/M transition and maintenance of diploidy. Genes Dev. 12: 831-843.
27. KELLOGG, D. R., T. J. MITCHISON and B. M. ALBERTS, 1988 Behavior of microtubules and actin filaments in living Drosophila embryos. Development 103: 675-686.
28. KIDD, T., 1994 Genetic and molecular studies of early embryogenesis in Drosophila. Ph.D. Thesis, Oxford University, Oxford.
29. 1-ATPaSe by expression of the corresponding bovine subunits in yeast Saccharomyces cerevisiae. Eur. J. Biochem. 267: 2409-2418.
30. 1-ATPase in yeast Saccharomyces cerevisiae. EMBO J. 18: 58-64.
31. LI, K., and T. C. KAUFMAN, 1996 The homeotic target gene centrosomin encodes an essential centrosomal component. Cell 85: 585-596.
32. LI, P., D. NIJHAWAN and X. WANG, 2004 Mitochondrial activation of apoptosis. Cell 116: 57-59.
33. LIN, Y. J., L. SEROUDE and S. BENZER, 1998 Extended lifespan and stress resistance in the Drosophila mutant methuselah. Science 282: 943-946.
34. LIU, Y. T., and H. L. YIN, 1998 Identification of the binding partners for flightless I, a novel protein bridging the leucine-rich repeat and the gelsolin superfamilies. J. Biol. Chem. 273: 7920-7927.
35. MINAURO-SANMIGUEL, F., C. BRAVO and J. J. GARCIA, 2002 Cross linking of the endogenous inhibitor protein (IF1) with rotor (γ, ε) and stator (α) subunits of the mitochondrial ATP synthase. J. Bioenerg. Biomembr. 34: 433-443.
36. MINDEN, J. S., D. A. AGARD, J. W. SEDAT and B. M. ALBERTS, 1989 Direct cell lineage analysis in Drosophila melanogaster by time lapse three dimensional optical microscopy of living embryos. J. Cell Biol. 109: 505-516.
37. PAWNARD, P., J. VAILLIEN, B. COULARY, J. SCHAEFFER, V. SOUBANNIER et al., 2003 The ATP synthase is involved in generating mitochondrial cristae morphology. EMBO J. 21: 221-230.
38. PRICE, D., S. RABINOVITCH, P. H. O'FARRELL and S. D. CAMPBELL, 2000 Drosophila wee1 has an essential role in the nuclear divisions of early embryogenesis. Genetics 155: 159-166.
39. ROTHWELL, W. F., and W. SULLIVAN, 1999 Fluorescent analysis of Drosophila embryos, pp. 141-157 in Drosophila Protocols, edited by W. SULLIVAN, A. ASHBURNER and R. S. HAWLEY. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
40. ROTHWELL, W. F., and W. SULLIVAN, 2000 The centrosome in early Drosophila development. Curr. Top. Dev. Biol. 49: 409-447.
41. ROTHWELL, W. F., P. FOGARTY, C. M. FIELD and W. SULLIVAN, 1998 Nuclear-fallout, a Drosophila protein that cycles from the cytoplasm to the centrosomes, regulates cortical microfilament organization. Development 125: 1295-1303.
42. ROTHWELL, W. F., C. X. ZHANG, C. ZELANO, T. S. HSIEH and W. SULLIVAN, 1999 The Drosophila centrosomal protein Nuf is required for recruiting Dah, a membrane associated protein, to furrows in the early embryo. J. Cell Sci. 112: 2885-2893.
43. SCHEJTER, E. D., and E. WIESCHAUS, 1993 Functional elements of the cytoskeleton in the early Drosophila embryo. Annu. Rev. Cell Biol 9: 67-99.
44. SCHMID, K. J., and D. TAUTZ, 1998 Sequence and expression of DmMKLP1, a homolog of the human MKLP1 kinesin-like protein from Drosophila melanogaster. Dev. Genes Evol. 208: 474-476.
45. SCHOLEY, J. M., I. BRUST-MASCHER and A. MOGILNER, 2003 Cell division. Nature 442: 746-752.
46. SCHWEISGUTH, F. C., J.-A. LEPESANT and A. VINCENT, 1990 The serendipity-alpha gene encodes a membrane associated protein required for the cellularization of the Drosophila embryo. Genes Dev. 4: 922-931.
47. SHARP, D. J., K. R. YU, J. C. SISSON, W. SULLIVAN and J. M. SCHOLEY, 1999 Antagonistic microtubule-sliding motors position mitotic centrosomes in Drosophila early embryos. Nat. Cell Biol. 1: 51-54.
48. SIBON, O. C., V. A. STEVENSON and W. E. THEURKAUF, 1997 DNA-replication checkpoint control at the Drosophila midblastula transition. Nature 388: 93-97.
49. SIBON, O. C., A. LAURENCON, R. HAWLEY and W. E. THEURKAUF, 1999 The Drosophila ATM homologue Mei-41 has an essential checkpoint function at the midblastula transition. Curr. Biol. 9: 302-312.
50. SIMPSON, L., and E. WIESCHAUS, 1990 Zygotic activity of the nullo locus is required to stabilize the actin myosin network during cellularization in Drosophila. Development 110: 851-863.
51. SMITH, A. V., and T. L. ORR-WEAVER, 1991 The regulation of the cell cycle during Drosophila embryogenesis: the transition to polyteny. Development 112: 997-1008.
52. SOLAINI, G., A. BARACCA, E. GABELLIERI and G. LENAZ, 1997 Modification of the mitochondrial F1-ATPase ε subunit, enhancement of the ATPase activity of the IF1-F1 complex and IF1 binding dependence of the conformation of the ε subunit. Biochem. J. 327: 443-448.
53. SONG, W., R. RANJAN, K. DAWSON-SCULLY, P. BRONK, L. MARIN et al., 2002 Presynaptic regulation of neurotransmission in Drosophila by the g protein-coupled receptor methuselah. Neuron 36: 105-119.
54. STEVENSON, V., J. KRAMER, J. KUHN and W. E. THEURKAUF, 2001 Centrosomes and the Scrambled protein coordintate microtubule-independent actin reorganization. Nat. Cell Biol. 3: 68-75.
55. SULLIVAN, W., and W. E. THEURKAUF, 1995 The cytoskeleton and morphogenesis of the early Drosophila embryo. Curr. Opin. Cell Biol. 7: 18-22.
56. SULLIVAN, W., P. FOGARTY and W. THEURKAUF, 1993 Mutations affecting the cytoskeletal organization of syncytial Drosophila embryos. Development 118: 1245-1254.
57. VALDES-PEREZ, R. E., and J. S. MINDEN, 1995 Drosophila melanogaster syncytial nuclear divisions are patterned: time-lapse images. Hypothesis and computational evidence. J. Theor. Biol. 175: 525-532.
58. ZHANG, C., M. P. LEE, A. D. CHEN, S. D. BROWN and T.-S. HSIEH, 1996 Isolation and characterization of a Drosophila gene essential for early embryonic development and formation of cortical cleavage furrows. J. Cell Biol. 134: 923-934.