Genetic analysis in drosophila reveals a role for the mitochondrial protein P32 in synaptic transmission

G3: Genes, Genomes, Genetics

Volumn 2, Issue 1, 2012, Pages 59-69

  Lutas, Andrew ^a   Wahlmark, Christopher J ^a   Acharjee, Shaona ^a   Kawasaki, Fumiko ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

Calcium; Dorsal; Flight muscle; Longitudinal; Neuromuscular; Neurotransmitter; Release; Sensitive; Temperature

Indexed keywords

EID: 84880056944     PISSN: None     EISSN: 21601836     Source Type: Journal    
DOI: 10.1534/g3.111.001586     Document Type: Article

References (61)

1. Al-Anzi, B., V. Sapin, C. Waters, K. Zinn, R. J. Wyman et al., 2009 Obesityblocking neurons in Drosophila. Neuron 63: 329-341.
2. Baird, G. S., D. A. Zacharias, and R. Y. Tsien, 2000 Biochemistry, mutagenesis, and oligomerization of DsRed, a red fluorescent protein from coral. Proc. Natl. Acad. Sci. USA 97: 11984-11989.
3. Beatch, M. D., and T. C. Hobman, 2000 Rubella virus capsid associates with host cell protein p32 and localizes to mitochondria. J. Virol. 74: 5569-5576.
4. Bialucha, C. U., E. C. Ferber, F. Pichaud, S. Y. Peak-Chew, and Y. Yasuyuki 2007 P32 is a novel mammalian Lgl binding protein that enhances the activity of protein kinase Cz and regulates cell polarity. J. Cell Biol. 178: 575-581.
5. Billups, B., and I. D. Forsythe, 2002 Presynaptic mitochondrial calcium sequestration influences transmission at mammalian central synapses. J. Neurosci. 22: 5840-5847.
6. Brand, A. H., and N. Perrimon, 1993 Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-415.
7. Brooks, I. M., R. Felling, M. D. Godeny, and R. W. Ordway, 2002 Genetic modifiers of a temperature-sensitive paralytic calcium channel mutant of Drosophila: genetic, molecular and phenotypic characterization (Abstract) in 43rd Annual Drosophila Research Conference: Programs and Abstracts Volume, April 10-14, 2002, San Diego, California. Genetics Society of America.
8. Brooks, I. M., R. Felling, F. Kawasaki, and R. W. Ordway, 2003 Genetic analysis of a synaptic calcium channel in Drosophila: intragenic modifiers of a temperature-sensitive paralytic mutant of cacophony. Genetics 164: 163-171.
9. Bruni, R., and B. Roizman, 1996 Open reading frame P-a herpes simplex virus gene repressed during productive infection encodes a protein that binds a splicing factor and reduces synthesis of viral proteins made from spliced mRNA. Proc. Natl. Acad. Sci. USA 93: 10423-10427.
10. Chacinska, A., C. M. Koehler, D. Milenkovic, T. Lithgow, and N. Pfanner, 2009 Importing mitochondrial proteins: machineries and mechanisms. Cell 138: 628-644.
11. Chouhan, A. K., J. Zhang, K. E. Zinsmaier, and G. T. Macleod, 2010 Presynaptic mitochondria in functionally different motor neurons exhibit similar affinities for Ca2+ but exert little influence as Ca2+ buffers at nerve firing rates in situ. J. Neurosci. 30: 1869-1881.
12. Danjo, R., F. Kawasaki, and R. W. Ordway, 2011 A tripartite synapse model in Drosophila. PLoS ONE 6: e17131.
13. David, G., and E. F. Barrett, 2003 Mitochondrial Ca2+ uptake prevents desynchronization of quantal release and minimizes depletion during repetitive stimulation of mouse motor nerve terminals. J. Physiol. 548: 425-438.
14. Dedio, J., W. Jahnen-Dechent, M. Bachmann, and W. Müller-Esterl, 1998 The multiligand-binding protein gC1qR, putative C1q receptor, is a mitochondrial protein. J. Immunol. 160: 3534-3542.
15. Dellinger, B. B., R. Felling, and R. W. Ordway, 2000 Genetic modifiers of the Drosophila NSF mutant, comatose, include a temperature-sensitive paralytic allele of the calcium channel a1 subunit gene, cacophony. Genetics 155: 203-211.
16. Fogal, V., A. D. Richardson, P. P. Karmali, I. E. Scheffler, J. W. Smith et al., 2010 Mitochondrial p32 protein is a critical regulator of tumor metabolism via maintenance of oxidative phosphorylation. Mol. Cell. Biol. 30: 1303-1318.
17. Fogal, V., L. Zhang, S. Krajewski, and E. Ruoslahti, 2008 Mitochondrial/ cell-surface protein p32/gC1qR as a molecular target in tumor cells and tumor stroma. Cancer Res. 68: 7210-7218.
18. Ghebrehiwet, B., B. L. Lim, R. Kumar, X. Feng, and E. I. Peerschke, 2001 gC1q-R/p33, a member of a new class of multifunctional and multicompartmental cellular proteins, is involved in inflammation and infection. Immunol. Rev. 180: 65-77.
19. Ghebrehiwet, B., B. L. Lim, E. I. Peerschke, A. C. Willis, and K. B. Reid, 1994 Isolation, cDNA cloning, and overexpression of a 33-kD cell surface glycoprotein that binds to the globular "heads" of C1q. J. Exp. Med. 179: 1809-1821.
20. Guo, X., G. T. Macleod, A. Wellington, F. Hu, S. Panchumarthi et al., 2005 The GTPase dMiro is required for axonal transport of mitochondria to Drosophila synapses. Neuron 47: 379-393.
21. Honoré, B., P. Madsen, H. H. Rasmussen, J. Vandekerckhove, J. E. Celis et al., 1993 Cloning and expression of a cDNA covering the complete coding region of the P32 subunit of human pre-mRNA splicing factor SF2. Gene 134: 283-287.
22. Hsu, S. F., G. J. Augustine, and M. B. Jackson, 1996 Adaptation of Ca(2+)- triggered exocytosis in presynaptic terminals. Neuron 17: 501-512.
23. Itahana, K., and Y. Zhang, 2008 Mitochondrial p32 Is a critical mediator of ARF-induced apoptosis. Cancer Cell 13: 542-553.
24. Jiang, J., Y. Zhang, A. R. Krainer, and R. M. Xu, 1999 Crystal structure of human p32, a doughnut-shaped acidic mitochondrial matrix protein. Proc. Natl. Acad. Sci. USA 96: 3572-3577.
25. Kann, O., and R. Kovács, 2007 Mitochondria and neuronal activity. Am. J. Physiol. Cell Physiol. 292: C641-C657.
26. Kawasaki, F., and R. W. Ordway, 2009 Molecular mechanisms determining conserved properties of short-term synaptic depression revealed in NSF and SNAP-25 conditional mutants. Proc. Natl. Acad. Sci. USA 106: 14658-14663.
27. Kawasaki, F., R. Felling, and R. W. Ordway, 2000 A temperature-sensitive paralytic mutant defines a primary synaptic calcium channel in Drosophila. J. Neurosci. 20: 4885-4889.
28. Kawasaki, F., S. C. Collins, and R. W. Ordway, 2002 Synaptic calcium channel function in Drosophila: analysis and transformation rescue of temperature-sensitive paralytic and lethal mutations of cacophony. J. Neurosci. 22: 5856-5864.
29. Kawasaki, F., B. Zou, X. Xu, and R. W. Ordway, 2004 Active zone localization of presynaptic calcium channels encoded by the cacophony. J. Neurosci. 24: 282-285.
30. Kawasaki, F., J. Iyer, L. L. Posey, E. Sun, S. E. Mammen et al., 2011 The DISABLED protein functions in CLATHRIN-mediated synaptic vesicle endocytosis and exoendocytic coupling at the active zone. Proc. Natl. Acad. Sci. USA 108: E222-E229.
31. Klose, M. K., G. L. Boulianne, R. M. Robertson, and H. L. Atwood, 2009 Role of ATP-dependent calcium regulation in modulation of Drosophila synaptic thermotolerance. J. Neurophysiol. 102: 901-913.
32. Krainer, A. R., A. Mayeda, D. Kozak, and G. Binns, 1991 Functional expression of cloned human splicing factor SF2: homology to RNA-binding proteins, U1 70K, and Drosophila splicing regulators. Cell 66: 383-394.
33. Liu, W., R. Gnanasambandam, J. Benjamin, G. Kaur, P. B. Getman et al., 2007 Mutations in cytochrome c oxidase subunit VIa cause neurodegeneration and motor dysfunction in Drosophila. Genetics 176: 937-946.
34. Luo, Y., H. Yu, and B. M. Peterlin, 1994 Cellular protein modulates effects of human immunodeficiency virus type 1 Rev. J. Virol. 68: 3850-3856.
35. Majumdar, M., J. Meenakshi, S. K. Goswami, and K. Datta, 2002 Hyaluronan binding protein 1 (HABP1)/C1QBP/p32 is an endogenous substrate for MAP kinase and is translocated to the nucleus upon mitogenic stimulation. Biochem. Biophys. Res. Commun. 291: 829-837.
36. Matthews, D. A., and W. C. Russell, 1998 Adenovirus core protein V interacts with p32-a protein which is associated with both the mitochondria and the nucleus. J. Gen. Virol. 79: 1677-1685.
37. Mattson, M. P., M. Gleichmann, and A. Cheng, 2008 Mitochondria in neuroplasticity and neurological disorders. Neuron 60: 748-766.
38. Muta, T., D. Kang, S. Kitajima, T. Fujiwara, and N. Hamasaki, 1997 p32 protein, a splicing factor 2-associated protein, is localized in mitochondrial matrix and is functionally important in maintaining oxidative phosphorylation. J. Biol. Chem. 272: 24363-24370.
39. Nagai, T., S. Yamada, T. Tominaga, M. Ichikawa, and A. Miyawaki, 2004 Expanded dynamic range of fluorescent indicators for Ca2+ by circularly permuted yellow fluorescent proteins. Proc. Natl. Acad. Sci. USA 101: 10554-10559.
40. Park, J., S. B. Lee, S. Lee, Y. Kim, S. Song et al., 2006 Mitochondrial dysfunction in Drosophila PINK1 mutants is complemented by parkin. Nature 441: 1157-1161.
41. Reiff, D. F., A. Ihring, G. Guerrero, E. Y. Isacoff, M. Joesch et al., 2005 In vivo performance of genetically encoded indicators of neural activity in flies. J. Neurosci. 25: 4766-4778.
42. Rezin, G. T., G. Amboni, A. I. Zugno, J. Quevedo, and E. L. Streck, 2009 Mitochondrial dysfunction and psychiatric disorders. Neurochem. Res. 34: 1021-1029.
43. Rikhy, R., M. Ramaswami, and K. S. Krishnan, 2003 A temperature-sensitive allele of Drosophila sesB reveals acute functions for the mitochondrial adenine nucleotide translocase in synaptic transmission and dynamin regulation. Genetics 165: 1243-1253.
44. Rizvi, F., T. Heimann, A. Herrnreiter, and W. J. O'brien, 2011 Mitochondrial dysfunction links ceramide activated HRK expression and cell death. PLoS ONE 6: e18137.
45. Rizzuto, R., M. Brini, P. Pizzo, M. Murgia, and T. Pozzan, 1995 Chimeric green fluorescent protein as a tool for visualizing subcellular organelles in living cells. Curr. Biol. 5: 635-642.
46. Schon, E. A., and S. Przedborski, 2011 Mitochondria: the next (neurode) generation. Neuron 70: 1033-1053.
47. Seytter, T., F. Lottspeich, W. Neupert, and E. Schwarz, 1998 Mam33p, an oligomeric, acidic protein in the mitochondrial matrix of Saccharomyces cerevisiae is related to the human complement receptor gC1q-R. Yeast 14: 303-310.
48. Stowers, R. S., L. J. Megeath, J. Górska-Andrzejak, I. A. Meinertzhagen, and T. L. Schwarz, 2002 Axonal transport of mitochondria to synapses depends on milton, a novel Drosophila protein. Neuron 36: 1063-1077.
49. Sunayama, J., Y. Ando, N. Itoh, A. Tomiyama, K. Sakurada et al., 2004 Physical and functional interaction between BH3-only protein Hrk and mitochondrial pore-forming protein p32. Cell Death Differ. 11: 771-781.
50. Tang, Y., and R. S. Zucker, 1997 Mitochondrial involvement in post-tetanic potentiation of synaptic transmission. Neuron 18: 483-491.
51. Tian, L., S. A. Hires, T. Mao, D. Huber, M. E. Chiappe et al., 2009 Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat. Methods 6: 875-881.
52. Trotta, N., C. K. Rodesch, T. Fergestad, and K. Broadie, 2004 Cellular bases of activity-dependent paralysis in Drosophila stress-sensitive mutants. J. Neurobiol. 60: 328-347.
53. Tweedie, S., M. Ashburner, K. Falls, P. Leyland, P. Mcquilton et al., 2009 FlyBase: enhancing Drosophila Gene Ontology annotations. Nucleic Acids Res. 37: D555-D559.
54. Twig, G., S. A. Graf, J. D. Wikstrom, H. Mohamed, S. E. Haigh et al., 2006 Tagging and tracking individual networks within a complex mitochondrial web with photoactivatable GFP. Am. J. Physiol. Cell Physiol. 291: C176-C184.
55. Verstreken, P., C. V. Ly, K. J. Venken, T. W. Koh, Y. Zhou et al., 2005 Synaptic mitochondria are critical for mobilization of reserve pool vesicles at Drosophila neuromuscular junctions. Neuron 47: 365-378.
56. Vos, M., E. Lauwers, and P. Verstreken, 2010 Synaptic mitochondria in synaptic transmission and organization of vesicle pools in health and disease. Frontiers in Synaptic Neuroscience 2: 1-10.
57. Wang, Y., J. E. Finan, J. M. Middeldorp, and S. D. Hayward, 1997 P32/TAP, a cellular protein that interacts with EBNA-1 of Epstein-Barr virus. Virology 236: 18-29.
58. Whitworth, A. J., and L. J. Pallanck, 2009 The PINK1/Parkin pathway: a mitochondrial quality control system? J. Bioenerg. Biomembr. 41: 499-503.
59. Yang, F., X. P. He, J. Russell, and B. Lu, 2003 Ca2+ influx-independent synaptic potentiation mediated by mitochondrial Na+-Ca2+ exchanger and protein kinase C. J. Cell Biol. 163: 511-523.
60. Yu, L., Z. Zhang, P. M. Loewenstein, K. Desai, Q. Tang et al., 1995 Molecular cloning and characterization of a cellular protein that interacts with the human immunodeficiency virus type 1 Tat transactivator and encodes a strong transcriptional activation domain. J. Virol. 69: 3007-3016.
61. Zou, B., H. Yan, F. Kawasaki, and R. W. Ordway, 2008 MAP1 structural organization in Drosophila: in vivo analysis of FUTSCH reveals heavy and light chain subunits generated by proteolytic processing at a conserved cleavage site. Biochem. J. 414: 63-71.