Depletion of PtdIns(4,5)P2 underlies retinal degeneration in Drosophila trp mutants

Journal of Cell Science

Volumn 126, Issue 5, 2013, Pages 1247-1259

  Sengupta, Sukanya ^a,c   Barber, Thomas R ^a   Xia, Hongai ^b   Ready, Donald F ^b   Hardie, Roger C ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b PURDUE UNIVERSITY   (United States)

^c TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Actin; Moesin; PtdIns(4,5)P2; Rhodopsin; TRP channels

Indexed keywords

CALCIUM ION; MOESIN; MUTANT PROTEIN; PHOSPHATASE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PHOSPHOLIPASE C; RETINA S ANTIGEN; RHODOPSIN; SIGD PHOSPHATASE; TRANSIENT RECEPTOR POTENTIAL CHANNEL; UNCLASSIFIED DRUG;

ACTIN POLYMERIZATION; ARTICLE; CALCIUM TRANSPORT; CELL STRUCTURE; COMPLEX FORMATION; DEPOLYMERIZATION; DROSOPHILA MELANOGASTER; ENZYME ACTIVITY; ENZYME INHIBITION; MICROVILLUS; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN DEPLETION; PROTEIN PHOSPHORYLATION; RED LIGHT; RETINA DEGENERATION; WILD TYPE;

ACTINS; ANIMALS; DROSOPHILA; MICROFILAMENT PROTEINS; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; RETINAL DEGENERATION; RHODOPSIN; TRANSIENT RECEPTOR POTENTIAL CHANNELS; TYPE C PHOSPHOLIPASES;

EID: 84877918135     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.120592     Document Type: Article

References (85)

1. Alloway, P. G. and Dolph, P. J. (1999). A role for the light-dependent phosphorylation of visual arrestin. Proc. Natl. Acad. Sci. USA 96, 6072-6077.
2. Alloway, P. G., Howard, L. and Dolph, P. J. (2000). The formation of stable rhodopsin-arrestin complexes induces apoptosis and photoreceptor cell degeneration. Neuron 28, 129-138.
3. Barret, C., Roy, C., Montcourrier, P., Mangeat, P. and Niggli, V. (2000). Mutagenesis of the phosphatidylinositol 4,5-bisphosphate (PIP(2)) binding site in the NH(2)-terminal domain of ezrin correlates with its altered cellular distribution. J. Cell Biol. 151, 1067-1080.
4. Berryman, M., Franck, Z. and Bretscher, A. (1993). Ezrin is concentrated in the apical microvilli of a wide variety of epithelial cells whereas moesin is found primarily in endothelial cells. J. Cell Sci. 105, 1025-1043.
5. Bretscher, A. (1999). Regulation of cortical structure by the ezrin-radixin-moesin protein family. Curr. Opin. Cell Biol. 11, 109-116.
6. Bretscher, A., Reczek, D. and Berryman, M. (1997). Ezrin: a protein requiring conformational activation to link microfilaments to the plasma membrane in the assembly of cell surface structures. J. Cell Sci. 110, 3011-3018.
7. Bretscher, A., Edwards, K. and Fehon, R. G. (2002). ERM proteins and merlin: integrators at the cell cortex. Nat. Rev. Mol. Cell Biol. 3, 586-599.
8. Byk, T., Bar-Yaacov, M., Doza, Y. N., Minke, B. and Selinger, Z. (1993). Regulatory arrestin cycle secures the fidelity and maintenance of the fly photoreceptor cell. Proc. Natl. Acad. Sci. USA 90, 1907-1911.
9. Chorna-Ornan, I., Tzarfaty, V., Ankri-Eliahoo, G., Joel-Almagor, T., Meyer, N. E., Huber, A., Payre, F. and Minke, B. (2005). Light-regulated interaction of Dmoesin with TRP and TRPL channels is required for maintenance of photoreceptors. J. Cell Biol. 171, 143-152.
10. Cosens, D. J. and Manning, A. (1969). Abnormal electroretinogram from a Drosophila mutant. Nature 224, 285-287.
11. Cosens, D. and Perry, M. M. (1972). The fine structure of the eye of a visual mutant, Atype of Drosophila melanogaster. J. Insect Physiol. 18, 1773-1786.
12. Di Paolo, G. and De Camilli, P. (2006). Phosphoinositides in cell regulation and membrane dynamics. Nature 443, 651-657.
13. Everett, K. V. (2011). Transient receptor potential genes and human inherited disease. Adv. Exp. Med. Biol. 704, 1011-1032.
14. Fehon, R. G., McClatchey, A. I. and Bretscher, A. (2010). Organizing the cell cortex: the role of ERM proteins. Nat. Rev. Mol. Cell Biol. 11, 276-287.
15. Feiler, R., Bjornson, R., Kirschfeld, K., Mismer, D., Rubin, G. M., Smith, D. P., Socolich, M. and Zuker, C. S. (1992). Ectopic expression of ultraviolet-rhodopsins in the blue photoreceptor cells of Drosophila: visual physiology and photochemistry of transgenic animals. J. Neurosci. 12, 3862-3868.
16. Fiévet, B., Louvard, D. and Arpin, M. (2007). ERM proteins in epithelial cell organization and functions. Biochim. Biophys. Acta 1773, 653-660.
17. Franceschini, N. and Kirschfeld, K. (1971). Etude optique in vivo des éléments photorécepteurs dans l'oeil composé de Drosophila. Kybernetik 8, 1-13.
18. Genescà, M., Sola, A. and Hotter, G. (2006). Actin cytoskeleton derangement induces apoptosis in renal ischemia/reperfusion. Apoptosis 11, 563-571.
19. Gu, Y., Oberwinkler, J., Postma, M. and Hardie, R. C. (2005). Mechanisms of light adaptation in Drosophila photoreceptors. Curr. Biol. 15, 1228-1234.
20. 2+ concentration in Drosophila photoreceptors. J. Neurosci. 16, 2924-2933.
21. Hardie, R. C. (2012). Phototransduction mechanisms in Drosophila microvillar photoreceptors. Wiley Interdiscip. Rev. Membr. Transp. Signal 1, 162-187.
22. 2+ channel in Drosophila photoreceptors. Neuron 8, 643-651.
23. Hardie, R. C., Raghu, P., Moore, S., Juusola, M., Baines, R. A. and Sweeney, S. T. (2001). Calcium influx via TRP channels is required to maintain PIP2 levels in Drosophila photoreceptors. Neuron 30, 149-159.
24. Hardie, R. C., Gu, Y., Martin, F., Sweeney, S. T. and Raghu, P. (2004). In vivo lightinduced and basal phospholipase C activity in Drosophila photoreceptors measured with genetically targeted phosphatidylinositol 4,5-bisphosphate-sensitive ion channels (Kir2.1). J. Biol. Chem. 279, 47773-47782.
25. 2+ and myosin III in Drosophila photoreceptors. J. Neurosci. 32, 9205-9216.
26. Hilgemann, D. W., Feng, S. and Nasuhoglu, C. (2001). The complex and intriguing lives of PIP2 with ion channels and transporters. Sci. STKE 2001, re19.
27. Howes, A. L., Arthur, J. F., Zhang, T., Miyamoto, S., Adams, J. W., Dorn, G. W., 2nd, Woodcock, E. A. and Brown, J. H. (2003). Akt-mediated cardiomyocyte survival pathways are compromised by G alpha q-induced phosphoinositide 4,5- bisphosphate depletion. J. Biol. Chem. 278, 40343-40351.
28. Inoue, R., Jensen, L. J., Shi, J., Morita, H., Nishida, M., Honda, A. and Ito, Y. (2006). Transient receptor potential channels in cardiovascular function and disease. Circ. Res. 99, 119-131.
29. Itoh, T. and Takenawa, T. (2004). Regulation of endocytosis by phosphatidylinositol 4,5-bisphosphate and ENTH proteins. Curr. Top. Microbiol. Immunol. 282, 31-47.
30. Janmey, P. A. and Lindberg, U. (2004). Cytoskeletal regulation: rich in lipids. Nat. Rev. Mol. Cell Biol. 5, 658-666.
31. Karagiosis, S. A. and Ready, D. F. (2004). Moesin contributes an essential structural role in Drosophila photoreceptor morphogenesis. Development 131, 725-732.
32. Katz, B. and Minke, B. (2009). Drosophila photoreceptors and signaling mechanisms. Front. Cell Neurosci. 3, 2.
33. Kiselev, A., Socolich, M., Vinó s, J., Hardy, R. W., Zuker, C. S. and Ranganathan, R. (2000). A molecular pathway for light-dependent photoreceptor apoptosis in Drosophila. Neuron 28, 139-152.
34. Kondo, T., Takeuchi, K., Doi, Y., Yonemura, S., Nagata, S. and Tsukita, S. (1997). ERM (ezrin/radixin/moesin)-based molecular mechanism of microvillar breakdown at an early stage of apoptosis. J. Cell Biol. 139, 749-758.
35. Kosloff, M., Elia, N., Joel-Almagor, T., Timberg, R., Zars, T. D., Hyde, D. R., Minke, B. and Selinger, Z. (2003). Regulation of light-dependent Gqa translocation and morphological changes in fly photoreceptors. EMBO J. 22, 459-468.
36. 2+ selectivity filter in the Drosophila transient receptor potential channel. J. Neurosci. 27, 604-615.
37. Mao, Y. S. and Yin, H. L. (2007). Regulation of the actin cytoskeleton by phosphatidylinositol 4-phosphate 5 kinases. Pflugers Arch. 455, 5-18.
38. Martin, S. S. and Leder, P. (2001). Human MCF10A mammary epithelial cells undergo apoptosis following actin depolymerization that is independent of attachment and rescued by Bcl-2. Mol. Cell. Biol. 21, 6529-6536.
39. Masai, I., Okazaki, A., Hosoya, T. and Hotta, Y. (1993). Drosophila retinal degeneration A gene encodes an eye-specific diacylglycerol kinase with cysteine-rich zinc-finger motifs and ankyrin repeats. Proc. Natl. Acad. Sci. USA 90, 11157-11161.
40. 2 degradation by a bacterial phosphatase. J. Gen. Physiol. 129, 267-283.
41. Matsumoto, H., Kurien, B. T., Takagi, Y., Kahn, E. S., Kinumi, T., Komori, N., Yamada, T., Hayashi, F., Isono, K., Pak, W. L. et al. (1994). Phosrestin I undergoes the earliest light-induced phosphorylation by a calcium/calmodulin-dependent protein kinase in Drosophila photoreceptors. Neuron 12, 997-1010.
42. McCartney, B. M. and Fehon, R. G. (1996). Distinct cellular and subcellular patterns of expression imply distinct functions for the Drosophila homologues of moesin and the neurofibromatosis 2 tumor suppressor, merlin. J. Cell Biol. 133, 843-852.
43. Minke, B. (1982). Light-induced reduction in excitation efficiency in the trp mutant of Drosophila. J. Gen. Physiol. 79, 361-385.
44. Miyamoto, S., Del Re, D. P., Xiang, S. Y., Zhao, X., Florholmen, G. and Brown, J. H. (2010). Revisited and revised: is RhoA always a villain in cardiac pathophysiology? J. Cardiovasc. Transl. Res. 3, 330-343.
45. Montell, C. (2005). The TRP superfamily of cation channels. Sci. STKE 2005, re3.
46. Montell, C. (2012). Drosophila visual transduction. Trends Neurosci. 35, 356-363.
47. Montell, C. and Rubin, G. M. (1989). Molecular characterization of the Drosophila trp locus: a putative integral membrane protein required for phototransduction. Neuron 2, 1313-1323.
48. Neisch, A. L. and Fehon, R. G. (2011). Ezrin, Radixin and Moesin: key regulators of membrane-cortex interactions and signaling. Curr. Opin. Cell Biol. 23, 377-382.
49. Neisch, A. L., Speck, O., Stronach, B. and Fehon, R. G. (2010). Rho1 regulates apoptosis via activation of the JNK signaling pathway at the plasma membrane. J. Cell Biol. 189, 311-323.
50. Niemeyer, B. A., Suzuki, E., Scott, K., Jalink, K. and Zuker, C. S. (1996). The Drosophila light-activated conductance is composed of the two channels TRP and TRPL. Cell 85, 651-659.
51. Nilius, B., Owsianik, G., Voets, T. and Peters, J. A. (2007). Transient receptor potential cation channels in disease. Physiol. Rev. 87, 165-217.
52. Orem, N. R. and Dolph, P. J. (2002). Loss of the phospholipase C gene product induces massive endocytosis of rhodopsin and arrestin in Drosophila photoreceptors. Vision Res. 42, 497-505.
53. Oshiro, N., Fukata, Y. and Kaibuchi, K. (1998). Phosphorylation of moesin by rhoassociated kinase (Rho-kinase) plays a crucial role in the formation of microvilli-like structures. J. Biol. Chem. 273, 34663-34666.
54. Payrastre, B., Missy, K., Giuriato, S., Bodin, S., Plantavid, M. and Gratacap, M. (2001). Phosphoinositides: key players in cell signalling, in time and space. Cell. Signal. 13, 377-387.
55. 2+ influx into Drosophila photoreceptors. J. Gen. Physiol. 104, 1057-1077.
56. Peretz, A., Suss-Toby, E., Rom-Glas, A., Arnon, A., Payne, R. and Minke, B. (1994b). The light response of Drosophila photoreceptors is accompanied by an increase in cellular calcium: effects of specific mutations. Neuron 12, 1257-1267.
57. Phillips, A. M., Bull, A. and Kelly, L. E. (1992). Identification of a Drosophila gene encoding a calmodulin-binding protein with homology to the trp phototransduction gene. Neuron 8, 631-642.
58. Polesello, C., Delon, I., Valenti, P., Ferrer, P. and Payre, F. (2002). Dmoesin controls actin-based cell shape and polarity during Drosophila melanogaster oogenesis. Nat. Cell Biol. 4, 782-789.
59. Raghu, P., Coessens, E., Manifava, M., Georgiev, P., Pettitt, T., Wood, E., Garcia- Murillas, I., Okkenhaug, H., Trivedi, D., Zhang, Q. et al. (2009). Rhabdomere biogenesis in Drosophila photoreceptors is acutely sensitive to phosphatidic acid levels. J. Cell Biol. 185, 129-145.
60. Raghu, P., Yadav, S. and Mallampati, N. B. (2012). Lipid signaling in Drosophila photoreceptors. Biochim. Biophys. Acta 1821, 1154-1165.
61. Ramsey, I. S., Delling, M. and Clapham, D. E. (2006). An introduction to TRP channels. Annu. Rev. Physiol. 68, 619-647.
62. Reuss, H., Mojet, M. H., Chyb, S. and Hardie, R. C. (1997). In vivo analysis of the drosophila light-sensitive channels, TRP and TRPL. Neuron 19, 1249-1259.
63. 2 and phosphorylation in moesin activation during Drosophila development. J. Cell Sci. 123, 2058-2067.
64. Rohacs, T. (2009). Phosphoinositide regulation of non-canonical transient receptor potential channels. Cell Calcium 45, 554-565.
65. Rohde, G., Wenzel, D. and Haucke, V. (2002). A phosphatidylinositol (4,5)- bisphosphate binding site within mu2-adaptin regulates clathrin-mediated endocytosis. J. Cell Biol. 158, 209-214.
66. Selvaraj, S., Sun, Y. and Singh, B. B. (2009). TRPC Channels and their Implication in Neurological Diseases. CNS Neurol. Disord. Drug Targets. 9, 94-104.
67. Simonsen, A., Wurmser, A. E., Emr, S. D. and Stenmark, H. (2001). The role of phosphoinositides in membrane transport. Curr. Opin. Cell Biol. 13, 485-492.
68. Steele, F. R., Washburn, T., Rieger, R. and O'Tousa, J. E. (1992). Drosophila retinal degeneration C (rdgC) encodes a novel serine/threonine protein phosphatase. Cell 69, 669-676.
69. Suria, H., Chau, L. A., Negrou, E., Kelvin, D. J. and Madrenas, J. (1999). Cytoskeletal disruption induces T cell apoptosis by a caspase-3 mediated mechanism. Life Sci. 65, 2697-2707.
70. Takeuchi, K., Sato, N., Kasahara, H., Funayama, N., Nagafuchi, A., Yonemura, S., Tsukita, S. and Tsukita, S. (1994). Perturbation of cell adhesion and microvilli formation by antisense oligonucleotides to ERM family members. J. Cell Biol. 125, 1371-1384.
71. Tamma, G., Klussmann, E., Oehlke, J., Krause, E., Rosenthal, W., Svelto, M. and Valenti, G. (2005). Actin remodeling requires ERM function to facilitate AQP2 apical targeting. J. Cell Sci. 118, 3623-3630.
72. Terebiznik, M. R., Vieira, O. V., Marcus, S. L., Slade, A., Yip, C. M., Trimble, W. S., Meyer, T., Finlay, B. B. and Grinstein, S. (2002). Elimination of host cell PtdIns(4,5)P(2) by bacterial SigD promotes membrane fission during invasion by Salmonella. Nat. Cell Biol. 4, 766-773.
73. Treanor, B., Depoil, D., Bruckbauer, A. and Batista, F. D. (2011). Dynamic cortical actin remodeling by ERM proteins controls BCR microcluster organization and integrity. J. Exp. Med. 208, 1055-1068.
74. Várnai, P. and Balla, T. (1998). Visualization of phosphoinositides that bind pleckstrin homology domains: calcium- and agonist-induced dynamic changes and relationship to myo-[3H]inositol-labeled phosphoinositide pools. J. Cell Biol. 143, 501-510.
75. Vennekens, R. (2011). Emerging concepts for the role of TRP channels in the cardiovascular system. J. Physiol. 589, 1527-1534.
76. Vihtelic, T. S., Hyde, D. R. and O'Tousa, J. E. (1991). Isolation and characterization of the Drosophila retinal degeneration B (rdgB) gene. Genetics 127, 761-768.
77. Vinós, J., Jalink, K., Hardy, R. W., Britt, S. G. and Zuker, C. S. (1997). A G proteincoupled receptor phosphatase required for rhodopsin function. Science 277, 687-690.
78. Wang, T. and Montell, C. (2006). A phosphoinositide synthase required for a sustained light response. J. Neurosci. 26, 12816-12825.
79. Wang, T., Jiao, Y. and Montell, C. (2005). Dissecting independent channel and scaffolding roles of the Drosophila transient receptor potential channel. J. Cell Biol. 171, 685-694.
80. Watanabe, H., Murakami, M., Ohba, T., Takahashi, Y. and Ito, H. (2008). TRP channel and cardiovascular disease. Pharmacol. Ther. 118, 337-351.
81. 2 reveals essential roles for phosphoinositides in flagellar biogenesis. J. Cell Sci. 121, 1076-1084.
82. Wu, L., Niemeyer, B., Colley, N., Socolich, M. and Zuker, C. S. (1995). Regulation of PLC-mediated signalling in vivo by CDP-diacylglycerol synthase. Nature 373, 216- 222.
83. Yin, H. L. and Janmey, P. A. (2003). Phosphoinositide regulation of the actin cytoskeleton. Annu. Rev. Physiol. 65, 761-789.
84. Yonemura, S., Matsui, T., Tsukita, S. and Tsukita, S. (2002). Rho-dependent and - independent activation mechanisms of ezrin/radixin/moesin proteins: an essential role for polyphosphoinositides in vivo. J. Cell Sci. 115, 2569-2580.
85. Zhu, Z., Luo, Z., Ma, S. and Liu, D. (2011). TRP channels and their implications in metabolic diseases. Pflugers Arch. 461, 211-223.