The GTP- and Phospholipid-Binding Protein TTD14 Regulates Trafficking of the TRPL Ion Channel in Photoreceptor Cells

1. Wang T, Montell C. Phototransduction and retinal degeneration in Drosophila. Pflugers Arch. 2007;454(5):821–847. 17487503

2. Xiong B, Bellen HJ. Rhodopsin homeostasis and retinal degeneration: lessons from the fly. Trends Neurosci. 2013. Nov;36(11):652–660. doi: 10.1016/j.tins.2013.08.003 24012059

3. Galy A, Roux MJ, Sahel JA, Leveillard T, Giangrande A. Rhodopsin maturation defects induce photoreceptor death by apoptosis: a fly model for RhodopsinPro23His human retinitis pigmentosa. Hum Mol Genet. 2005;14(17):2547–2557. 16049034

4. Montell C, Birnbaumer L, Flockerzi V. The TRP channels, a remarkably functional family. Cell. 2002;108(5):595–598. 11893331

5. Clapham DE. TRP channels as cellular sensors. Nature. 2003;426(6966):517–524. 14654832

6. Hardie RC. TRP channels and lipids: from Drosophila to mammalian physiology. J. Physiol. 2007;578(Pt 1):9–24. 16990401

7. Gees M, Colsoul B, Nilius B. The role of transient receptor potential cation channels in Ca2+ signaling. Cold Spring Harb Perspect Biol. 2010;2(10):a003962. doi: 10.1101/cshperspect.a003962 20861159

8. Colley NJ, Baker EK, Stamnes MA, Zuker CS. The cyclophilin homolog ninaA is required in the secretory pathway. Cell. 1991;67(2):255–263. 1913822

9. Rosenbaum EE, Brehm KS, Vasiljevic E, Liu CH, Hardie RC, Colley NJ. XPORT-Dependent Transport of TRP and Rhodopsin. Neuron. 2011;72(4):602–615. doi: 10.1016/j.neuron.2011.09.016 22099462

10. Rosenbaum EE, Hardie RC, Colley NJ. Calnexin is essential for rhodopsin maturation, Ca2+ regulation, and photoreceptor cell survival. Neuron. 2006;49(2):229–241. 16423697

11. Shieh BH, Stamnes MA, Seavello S, Harris GL, Zuker CS. The ninaA gene required for visual transduction in Drosophila encodes a homologue of cyclosporin A-binding protein. Nature. 1989;338(6210):67–70. 2493138

12. Stamnes MA, Shieh BH, Chuman L, Harris GL, Zuker CS. The cyclophilin homolog ninaA is a tissue-specific integral membrane protein required for the proper synthesis of a subset of Drosophila rhodopsins. Cell. 1991;65(2):219–227. 1707759

13. Kunduri G, Yuan C, Parthibane V, Nyswaner KM, Kanwar R, Nagashima K, et al. Phosphatidic acid phospholipase A1 mediates ER-Golgi transit of a family of G protein-coupled receptors. J Cell Biol. 2014;206(1):79–95. doi: 10.1083/jcb.201405020 25002678

14. Satoh A, Tokunaga F, Kawamura S, Ozaki K. In situ inhibition of vesicle transport and protein processing in the dominant negative Rab1 mutant of Drosophila. J Cell Sci. 1997;110(Pt 23):2943–2953. 9359879

15. Satoh AK, O'Tousa JE, Ozaki K, Ready DF. Rab11 mediates post-Golgi trafficking of rhodopsin to the photosensitive apical membrane of Drosophila photoreceptors. Development. 2005;132(7):1487–1497. 15728675

16. Shetty KM, Kurada P, O'Tousa JE. Rab6 regulation of rhodopsin transport in Drosophila. J Biol Chem. 1998;273(32):20425–20430. 9685396

17. Li BX, Satoh AK, Ready DF. Myosin V, Rab11, and dRip11 direct apical secretion and cellular morphogenesis in developing Drosophila photoreceptors. J Cell Biol. 2007;177(4):659–669. 17517962

18. Xiong B, Bayat V, Jaiswal M, Zhang K, Sandoval H, Charng WL, et al. Crag is a GEF for Rab11 required for rhodopsin trafficking and maintenance of adult photoreceptor cells. PLoS Biol. 2012;10(12):e1001438. doi: 10.1371/journal.pbio.1001438 23226104

19. Satoh T, Ohba A, Liu Z, Inagaki T, Satoh AK. dPob/EMC is essential for biosynthesis of rhodopsin and other multi-pass membrane proteins in Drosophila photoreceptors. eLife. 2015;4.

20. Xu H, Lee SJ, Suzuki E, Dugan KD, Stoddard A, Li HS, et al. A lysosomal tetraspanin associated with retinal degeneration identified via a genome-wide screen. EMBO J. 2004;23(4):811–822. 14963491

21. Kiselev A, Socolich M, Vinos J, Hardy RW, Zuker CS, Ranganathan R. A molecular pathway for light-dependent photoreceptor apoptosis in Drosophila. Neuron. 2000;28(1):139–152. 11086990

22. Orem NR, Xia L, Dolph PJ. An essential role for endocytosis of rhodopsin through interaction of visual arrestin with the AP-2 adaptor. J Cell Sci. 2006;119(Pt 15):3141–3148. 16835270

23. Wang S, Tan KL, Agosto MA, Xiong B, Yamamoto S, Sandoval H, et al. The retromer complex is required for rhodopsin recycling and its loss leads to photoreceptor degeneration. PLoS Biol. 2014;12(4):e1001847. doi: 10.1371/journal.pbio.1001847 24781186

24. Cullen PJ, Korswagen HC. Sorting nexins provide diversity for retromer-dependent trafficking events. Nat Cell Biol. 2012;14(1):29–37.

25. Seaman MN. The retromer complex—endosomal protein recycling and beyond. J Cell Sci. 2012;125(Pt 20):4693–4702. doi: 10.1242/jcs.103440 23148298

26. Bonifacino JS, Hurley JH. Retromer. Curr Opin Cell Biol. 2008;20(4):427–436. doi: 10.1016/j.ceb.2008.03.009 18472259

27. Johannes L, Popoff V. Tracing the retrograde route in protein trafficking. Cell. 2008;135(7):1175–1187. doi: 10.1016/j.cell.2008.12.009 19109890

28. Harterink M, Port F, Lorenowicz MJ, McGough IJ, Silhankova M, Betist MC, et al. A SNX3-dependent retromer pathway mediates retrograde transport of the Wnt sorting receptor Wntless and is required for Wnt secretion. Nat Cell Biol. 2011;13(8):914–923. doi: 10.1038/ncb2281 21725319

29. Temkin P, Lauffer B, Jager S, Cimermancic P, Krogan NJ, von Zastrow M. SNX27 mediates retromer tubule entry and endosome-to-plasma membrane trafficking of signalling receptors. Nat Cell Biol. 2011;13(6):715–721. doi: 10.1038/ncb2252 21602791

30. Chen D, Xiao H, Zhang K, Wang B, Gao Z, Jian Y, et al. Retromer is required for apoptotic cell clearance by phagocytic receptor recycling. Science. 2010;327(5970):1261–1264. doi: 10.1126/science.1184840 20133524

31. Hussain NK, Diering GH, Sole J, Anggono V, Huganir RL. Sorting Nexin 27 regulates basal and activity-dependent trafficking of AMPARs. Proc Natl Acad Sci U S A. 2014;111(32):11840–11845. doi: 10.1073/pnas.1412415111 25071192

32. Wang X, Zhao Y, Zhang X, Badie H, Zhou Y, Mu Y, et al. Loss of sorting nexin 27 contributes to excitatory synaptic dysfunction by modulating glutamate receptor recycling in Down's syndrome. Nat Med. 2013;19(4):473–480. doi: 10.1038/nm.3117 23524343

33. Loo LS, Tang N, Al-Haddawi M, Dawe GS, Hong W. A role for sorting nexin 27 in AMPA receptor trafficking. Nat Commun. 2014;5 : 3176. doi: 10.1038/ncomms4176 24458027

34. Bähner M, Frechter S, Da Silva N, Minke B, Paulsen R, Huber A. Light-regulated subcellular translocation of Drosophila TRPL channels induces long-term adaptation and modifies the light-induced current. Neuron. 2002; 34 (1):83–93. 11931743

35. Meyer NE, Joel-Almagor T, Frechter S, Minke B, Huber A. Subcellular translocation of the eGFP-tagged TRPL channel in Drosophila photoreceptors requires activation of the phototransduction cascade. J Cell Sci. 2006;119(Pt 12):2592–2603. 16735439

36. Cronin MA, Lieu MH, Tsunoda S. Two stages of light-dependent TRPL-channel translocation in Drosophila photoreceptors. J Cell Sci. 2006;119 : 2935–2944. 16787936

37. Oberegelsbacher C, Schneidler C, Voolstra O, Cerny A, Huber A. The Drosophila TRPL ion channel shares a Rab-dependent translocation pathway with rhodopsin. Eur J Cell Biol. 2011;90(8):620–630. doi: 10.1016/j.ejcb.2011.02.003 21507505

38. Lieu MH, Vallejos MJ, Michael E, Tsunoda S. Mechanisms underlying stage-1 TRPL channel translocation in Drosophila photoreceptors. PloS One. 2012;7(2):e31622. doi: 10.1371/journal.pone.0031622 22363689

39. Meyer NE, Oberegelsbacher C, Dürr TD, Schäfer A, Huber A. An eGFP-based genetic screen for defects in light-triggered subcelluar translocation of the Drosophila photoreceptor channel TRPL. Fly. 2008;2(1):384–394.

40. Walker JE, Saraste M, Runswick MJ, Gay NJ. Distantly related sequences in the alpha -⁠ and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J. 1982;1(8):945–951. 6329717

41. Bourne HR, Sanders DA, McCormick F. The GTPase superfamily: conserved structure and molecular mechanism. Nature. 1991;349(6305):117–127. 1898771

42. Leipe DD, Wolf YI, Koonin EV, Aravind L. Classification and evolution of P-loop GTPases and related ATPases. J Mol Biol. 2002;317(1):41–72. 11916378

43. Iyer LM, Aravind L. The catalytic domains of thiamine triphosphatase and CyaB-like adenylyl cyclase define a novel superfamily of domains that bind organic phosphates. BMC Genomics. 2002;3(1):33. 12456267

44. Di Paolo G, De Camilli P. Phosphoinositides in cell regulation and membrane dynamics. Nature. 2006;443(7112):651–657. 17035995

45. Cerny AC, Oberacker T, Pfannstiel J, Weigold S, Will C, Huber A. Mutation of light-dependent phosphorylation sites of the Drosophila transient receptor potential-like (TRPL) ion channel affects its subcellular localization and stability. J Biol Chem. 2013;288(22):15600–15613. doi: 10.1074/jbc.M112.426981 23592784

46. Leung HT, Geng C, Pak WL. Phenotypes of trpl mutants and interactions between the transient receptor potential (TRP) and TRP-like channels in Drosophila. J Neurosci. 2000;20(18):6797–6803. 10995823

47. Small SA, Petsko GA. Retromer in Alzheimer disease, Parkinson disease and other neurological disorders. Nat Rev Neurosci. 2015;16(3):126–132. doi: 10.1038/nrn3896 25669742

48. Zimprich A, Benet-Pages A, Struhal W, Graf E, Eck SH, Offman MN, et al. A mutation in VPS35, encoding a subunit of the retromer complex, causes late-onset Parkinson disease. Am J Hum Genet. 2011;89(1):168–175. doi: 10.1016/j.ajhg.2011.06.008 21763483

49. Vilarino-Guell C, Wider C, Ross OA, Dachsel JC, Kachergus JM, Lincoln SJ, et al. VPS35 mutations in Parkinson disease. Am J Hum Genet. 2011;89(1):162–167. doi: 10.1016/j.ajhg.2011.06.001 21763482

50. Wennerberg K, Rossman KL, Der CJ. The Ras superfamily at a glance. J Cell Sci. 2005;118(Pt 5):843–846. 15731001

51. Sundborger AC, Hinshaw JE. Regulating dynamin dynamics during endocytosis. F1000Prime Rep. 2014;6 : 85. doi: 10.12703/P6-85 25374663

52. Alushin GM, Lander GC, Kellogg EH, Zhang R, Baker D, Nogales E. High-resolution microtubule structures reveal the structural transitions in αβ-tubulin upon GTP hydrolysis. Cell. 2014;157(5):1117–1129. doi: 10.1016/j.cell.2014.03.053 24855948

53. Raghu P, Hardie RC. Regulation of Drosophila TRPC channels by lipid messengers. Cell Calcium. 2009;45(6):566–573. doi: 10.1016/j.ceca.2009.03.005 19362736

54. Inoue H, Yoshioka T, Hotta Y. Diacylglycerol kinase defect in a Drosophila retinal degeneration mutant rdgA. J Biol Chem. 1989;264(10):5996–6000. 2538432

55. Raghu P, Coessens E, Manifava M, Georgiev P, Pettitt T, Wood E, et al. Rhabdomere biogenesis in Drosophila photoreceptors is acutely sensitive to phosphatidic acid levels. The J Cell Biol. 2009;185(1):129–145. doi: 10.1083/jcb.200807027 19349583

56. Ponting CP. Novel domains in NADPH oxidase subunits, sorting nexins, and PtdIns 3-kinases: binding partners of SH3 domains? Protein Sci. 1996;5(11):2353–2357. 8931154

57. Ellson CD, Andrews S, Stephens LR, Hawkins PT. The PX domain: a new phosphoinositide-binding module. J Cell Sci. 2002;115(Pt 6):1099–1105. 11884510

58. Xu Y, Hortsman H, Seet L, Wong SH, Hong W. SNX3 regulates endosomal function through its PX-domain-mediated interaction with PtdIns(3)P. Nat Cell Biol. 2001;3(7):658–666. 11433298

59. Lu L, Hong W. From endosomes to the trans-Golgi network. Semin Cell Dev Biol. 2014;31 : 30–39. doi: 10.1016/j.semcdb.2014.04.024 24769370

60. Yoon J, Ben-Ami HC, Hong YS, Park S, Strong LL, Bowman J, et al. Novel mechanism of massive photoreceptor degeneration caused by mutations in the trp gene of Drosophila. J Neurosci. 2000;20(2):649–659. 10632594

61. Raghu P, Usher K, Jonas S, Chyb S, Polyanovsky A, Hardie RC. Constitutive activity of the light-sensitive channels TRP and TRPL in the Drosophila diacylglycerol kinase mutant, rdgA. Neuron. 2000;26(1):169–179. 10798401

62. Colley NJ, Cassill JA, Baker EK, Zuker CS. Defective intracellular transport is the molecular basis of rhodopsin -⁠ dependent dominant retinal degeneration. Proc Natl Acad Sci USA. 1995;92(7):3070–3074. 7708777

63. Satoh AK, O'Tousa JE, Ozaki K, Ready DF. Rab11 mediates post-Golgi trafficking of rhodopsin to the photosensitive apical membrane of Drosophila photoreceptors. Development. 2005;132(7):1487–1497. 15728675

64. O'Tousa JE, Baehr W, Martin RL, Hirsh J, Pak WL, Applebury ML. The Drosophila ninaE gene encodes an opsin. Cell. 1985;40(4):839–850. 2985266

65. Pak WL. Study of photoreceptor function using Drosophila mutants. In: Breakefield X, editor. Neurogenetics: Genetic approaches to the nervous system. Amsterdam: ELSEVIER; 1979. pp. 67–99.

66. Pichaud F, Desplan C. A new visualization approach for identifying mutations that affect differentiation and organization of the Drosophila ommatidia. Development. 2001;128(6):815–826. 11222137

67. Richter D, Katz B, Oberacker T, Tzarfaty V, Belusic G, Minke B, et al. Translocation of the Drosophila transient receptor potential-like (TRPL) channel requires both the N -⁠ and C-terminal regions together with sustained Ca2+ entry. J Biol Chem. 2011;286(39):34234–34243. doi: 10.1074/jbc.M111.278564 21816824

68. Bischof J, Maeda RK, Hediger M, Karch F, Basler K. An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc Natl Acad Sci U S A. 2007;104(9):3312–3317. 17360644

69. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227 : 682–685.