The phosphatidylinositol transfer protein domain of Drosophila retinal degeneration B protein is essential for photoreceptor cell survival and recovery from light stimulation

Journal of Cell Biology

Volumn 139, Issue 2, 1997, Pages 351-363

  Milligan, Scott C ^a   Alb Jr , James G ^b   Elagina, Raya B ^a   Bankaitis, Vytas A ^b   Hyde, David R ^a  

^a UNIVERSITY OF NOTRE DAME   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; CHIMERIC PROTEIN; MEMBRANE PROTEIN; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLINOSITOL; RHODOPSIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; DROSOPHILA; EUKARYOTE; LIGHT DARK CYCLE; METAZOON; NONHUMAN; PHOTORECEPTOR CELL; PHOTOSTIMULATION; PHOTOTRANSDUCTION; PRIORITY JOURNAL; PROTEIN DOMAIN; RETINA DEGENERATION; SIGNAL TRANSDUCTION;

AGING; ANIMALS; BRAIN; CARRIER PROTEINS; CLONING, MOLECULAR; DROSOPHILA; DROSOPHILA PROTEINS; ELECTROPHYSIOLOGY; EYE PROTEINS; LIGHT; MEMBRANE PROTEINS; PHOSPHATIDYLINOSITOLS; PHOSPHOLIPID TRANSFER PROTEINS; PHOTIC STIMULATION; PHOTORECEPTORS, INVERTEBRATE; POINT MUTATION; POLYMERASE CHAIN REACTION; RATS; RECOMBINANT PROTEINS; THREONINE;

EID: 0030806560     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.139.2.351     Document Type: Article

References (50)

1. Aitken, J.F., G.P.H. van Heusden, M. Temkin, and W. Dowhan. 1990. The gene encoding the phosphatidylinosilol transfer protein is essential for cell growth. J. Biol. Chem. 265:4711-4717.
2. Alb, J.G., A. Gedvilaite, R.T. Cartee, H.B. Skinner, and V.A. Bankaitis. 1995. Mutant rat phosphatidylinositol/phosphatidylcholine transfer proteins specifically defective in phosphatidylinositol transfer: implications for the regulation of phospholipid transfer activity. Proc. Natl. Acad. Sci. USA. 92:8826-8830.
3. Alb, J.G., M.A. Kearns, and V.A. Bankaitis. 1996. Phospholipid metabolism and membrane dynamics. Curr. Opin. Cell Biol. 8:534-541.
4. Ashburner, M. 1989. Drosophila: A Laboratory Handbook. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. 1331 pp.
5. Bankaitis, V.A., D.E. Malehorn, S.D. Emr, and R. Greene. 1989. The Saccharomyces cerevisiae SEC14 gene encodes a cytosolic factor that is required for transport of secretory proteins from the yeast Golgi complex. J. Cell Biol. 108:1271-1281.
6. Bankaitis, V.A., J.F. Aitken, A.E. Cleves, and W. Dowhan. 1990. An essential role for a phospholipid transfer protein in yeast Golgi function. Nature (Lond.). 347:561-562.
7. Bloomquist, B.T., R.D. Shortridge, S. Schneuwly, M. Perdew, C. Montell, H. Stellar, G. Rubin, and W.L. Pak. 1988. Isolation of a putative phospholipase C gene of Drosophila, norpA, and its role in phototransduction. Cell. 54:723-733.
8. Chang, J.T., S. Milligan, Y. Li, C.E. Chew, J. Wiggs, N.G. Copeland, N.A. Jenkins, P.A. Campochiaro, D.R. Hyde, and D.J. Zack. 1997. Mammalian homologue of Drosophila retinal degeneration B rescues the mutant fly phenotype, J. Neurosci. 17:5881-5890.
9. Cleves, A., T. McGee, and V. Bankaitis. 1991. Phospholipid transfer proteins: a biological debut. Trends Cell Biol. 1:30-34.
10. 2. Curr. Biol. 5:775-783.
11. Franceschini, N. 1972. Pupil and pseudopupil in the compound eye of Drosophila. In Information Processing in the Visual Systems of Arthropods. R. Wehners, editor. Springer-Verlag, Berlin, Germany. 75-82.
12. Hamilton, B.A., D.J. Smith, K.L. Mueller, A.W. Kerrebrock, R.T. Bronson, V. van Berkel, M.J. Daly, L. Kruglyak, M.P. Reeve, J.L. Nemhauser, et al. 1997. The vibrator mutation causes neurodegeneration via reduced expression of PITPα: positional complementation cloning and extragenic suppression. Neuron. 18:711-722.
13. Hardie, R.C., A. Peretz, E. Susstoby, A. Romglas, S.A. Bishop, Z. Selinger, and B. Minke. 1993. Protein kinase C is required for light adaptation in Drosophila photoreceptors. Nature (Lond.). 363:634-637.
14. Harris, W.A., and W.S. Stark. 1977. Hereditary retinal degeneration in Drosophila melanogaster: a mutant defect associated with the phototransduction process. J. Gen. Physiol. 69:261-291.
15. 2+-activated secretion. Nature (Lond.). 366:572-575.
16. 2+-activated secretion. Nature (Lond.). 374:173-177.
17. Hurley, J.B. 1995. Phospholipids in action. Nature (Lond.). 373:194-195.
18. Kearns, B.G., T.P. McGee, P. Mayinger, A. Gedvilaite, S.E. Phillips, S. Kagiwada, and V.A. Bankaitis. 1997. Essential role for diacylglycerol in protein transport from the yeast Golgi complex. Nature (Lond.). 387:101-105.
19. Kumar, J.P., and D.E. Ready. 1995. Rhodopsin plays an essential structural role in Drosophila photoreceptor development. Development (Camb.). 121: 4359-4370.
20. Kunkel, T.A., J.D. Roberts, and R.A. Zakour. 1987. Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol. 154: 367-382.
21. Laemmli, U.K. 1970. Cleavage of structural proteins during assembly of the head of bacteriophage T4. Nature (Lond.). 227:680-685.
22. Lee, Y.J., S. Shah, E. Suzuki, T. Zars, P.M. O'Day, and D.R. Hyde. 1994. The Drosophila dgq gene encodes a Gα protein that mediates phototransduction. Neuron. 13:1143-1157.
23. Leonard, D.S., V.D. Bowman, D.F. Ready, and W.L. Pak. 1992. Degeneration of photoreceptors in rhodopsin mutants of Drosophila. J. Neurobiol. 23:605-626.
24. Matsumoto-Suzuki, E., K. Hirosawa, and Y. Hotta. 1989. Structure of the sub-rhabdomeric cisternae in the photoreceptor cells of D. melanogaster. J. Neurocytol. 18:87-93.
25. McGee, T.P., H.B. Skinner, E.A. Whitters, S.A. Henry, and V.A. Bankaitis. 1994. A phosphatidylinositol transfer protein controls the phosphatidylcholine content of yeast Golgi membranes. J. Cell Biol. 124:273-287.
26. Miller, J. 1972. Experiments in Molecular Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. 466 pp.
27. Minke, B., C.T. Rubinstein, I. Sahly, S. Bar-Nachum, R. Timberg, and Z. Selinger. 1990. Phorbol ester induces photoreceptor-specific degeneration in a Drosophila mutant. Proc. Natl. Acad, Sci. USA. 87:113-117.
28. Mismer, D., and G.M. Rubin. 1987. Analysis of the promoter of the ninaE opsin gene in Drosophila melanogaster. Genetics. 116:565-578.
29. Ohashi, M., K.J. De Vries, R. Frank, G. Snoek, V. Bankaitis, K. Wirtz, and W.B. Huttner. 1995. A role for phosphatidylinositol transfer protein in secretory vesicle formation. Nature (Lond.). 377:544-547.
30. O'Tousa., J.E., W. Baehr, R.L. Martin, J. Hirsh, W.L. Pak, and M.L. Apple-bury. 1985. The Drosophila ninaE gene encodes an opsin. Cell. 40:839-850.
31. Ozaki, K., H. Nagatani, M. Ozaki, and F. Tokunaga. 1993. Maturation of major Drosophila rhodopsin, ninaE, requires chromophore 3-hydroxyretinal. Neuron. 10:1113-1119.
32. Ranganathan, R., G.L. Harris, C.F. Stevens, and C.S. Zuker. 1991. A Drosophila mutant defective in extracellular calcium-dependent photoreceptor deactivation and rapid desensitization. Nature (Lond.). 354:230-232.
33. Rubinstein, C.T., S. Bar-Nachum, Z. Selinger, and B. Minke. 1989. Chemically induced retinal degeneration in the rdgB (retinal degeneration B) mutant of Drosophila. Vis. Neurosci. 2:541-551.
34. Sanger, F., S. Nicklen, and A.R. Coulson. 1977. DNA sequencing with chain terminating inhibitors. Proc. Natl. Acad. Sci. USA. 74:5463-5467.
35. Skinner, H.B., J.G. Alb, Jr., E.A. Whitters, G.M. Helmkamp, and V.A. Bankaitis. 1993. Phospholipid transfer activity is relevant to but not sufficient for the essential function of the yeast SEC14 gene product. EMBO (Eur. Mol. Biol. Organ.) J. 12:4775-4784.
36. Skinner, H.B., T.P. McGee, C.R. McMaster, M.R. Fry, R.M. Bell, and V.A. Bankaitis. 1995. The Saccharomyces cerevisiae phosphatidylinositol-transfer protein effects a ligand-dependent inhibition of choline-phosphate cytidylyltransferase activity. Proc. Natl. Acad. Sci. USA. 92:112-116.
37. Smith, D.P., R. Ranganathan, R.W. Hardy, J. Marx, T. Tsuchida, and C.S. Zuker. 1991. Photoreceptor deactivation and retinal degeneration mediated by a photoreceptor-specific protein kinase C. Science (Wash. DC). 254:1478-1484.
38. Stark, W.S., D.-M. Chen, M.A. Johnson, and K.L. Frayer. 1983. The rdgB gene of Drosophila: retinal degeneration in different alleles and inhibition by norpA. J. Insect Physiol. 29:123-131.
39. Stephenson, R.S., J. O'Tousa, N.J. Scavarda, L.L. Randall, and W.L. Pak. 1983. Drosophila mutants with reduced rhodopsin content. In The Biology of Photoreception. D. Cosens and D. Vince-Price, editors. Cambridge University Press, Cambridge, England, pp. 477-501.
40. Suzuki, E., and K. Hiosawa. 1991. Immunoelectron microscopic study of the opsin distribution in the photoreceptor cell of Drosophila melanogaster. JEM (J. Electron Microsc.). 40:187-192.
41. Suzuki, E., and K. Hirosawa. 1994. Immunolocalization of a Drosophila phosphatidylinositol transfer protein (rdgB) in normal and rdgA mutant photoreceptor cells with special reference to the subrhabdomeric cisternae. JEM (J. Electron Microsc.). 43:183-189.
42. Thomas, G.M.H., E. Cunningham, A. Fensome, A. Ball, N.F. Totty, O. Truong, J.J. Hsuan, and S. Cockcroft. 1993. An essential role for phosphatidylinositol transfer protein in phospholipase C-mediated inositol lipid signaling. Cell. 74:919-928.
43. Vihtelic, T.S., D.R. Hyde, and J.E. O'Tousa. 1991. Isolation and characterization of the Drosophila retinal degeneration B (rdgB) gene. Genetics. 127:761-768.
44. Vihtelic, T.S., M. Goebl, S. Milligan, J.E. O'Tousa, and D.R. Hyde. 1993. Localization of Drosophila retinal degeneration B, a membrane-associated phosphatidylinositol transfer protein. J. Cell Biol. 122:1013-1022.
45. Walz, B. 1982. Calcium-sequestering smooth endoplasmic reticulum in retinula-cells of the blowfly. J. Ultrastruct. Res. 81:240-248.
46. Wirtz, K.W.A. 1991. Phospholipid transfer proteins. Annu. Rev. Biochem. 60: 73-99.
47. Wu, L., B. Niemeyer, N. Colley, M. Socolich, and C.S. Zuker. 1995. Regulation of PLC-mediated signalling in vivo by CDP-diacylglycerol synthase. Nature (Lond.). 373:216-222.
48. Zars, T., and D.R. Hyde. 1996. rdgE: a novel retinal degeneration mutation in Drosophila melanogaster. Genetics. 144:127-138.
49. Zuker, C.S. 1996. The biology of vision in Drosophila. Proc. Natl. Acad. Sci. USA. 93:571-576.
50. Zuker, C.S., A.F. Cowman, and G.M. Rubin. 1985. Isolation and structure of a rhodopsin gene from D. melanogaster. Cell. 40:851-858.