Novel topography of the rab 11-effector interaction network within a ciliary membrane targeting complex

Small GTPases

Volumn 6, Issue 4, 2015, Pages 165-173

  Vetter, Melanie ^a   Wang, Jing ^b   Lorentzen, Esben ^a   Deretic, Dusanka ^b  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

Author keywords

Cilium; Golgi; GTPase effectors; Membrane trafficking; Rab GTPases

Indexed keywords

CARRIER PROTEIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; RAB PROTEIN; RAB11 PROTEIN; REGULATOR PROTEIN; GERMINAL CENTER KINASES; I KAPPA B KINASE; IKBKG PROTEIN, HUMAN; MULTIENZYME COMPLEX; PROTEIN SERINE THREONINE KINASE;

AMINO ACID SEQUENCE; ARABIDOPSIS THALIANA; CHLAMYDOMONAS REINHARDTII; CILIARY BODY EPITHELIUM; CONFORMATIONAL TRANSITION; ENZYME ACTIVATION; EUKARYOTIC FLAGELLUM; EXOCYTOSIS; HUMAN; LEBER CONGENITAL AMAUROSIS; NONHUMAN; PROTEIN BINDING; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; REVIEW; SENSORY RECEPTOR; TRANS GOLGI NETWORK; ANIMAL; CELL MEMBRANE; CILIOPATHY; CILIUM; ENZYMOLOGY; GENETICS; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; CELL MEMBRANE; CILIA; CILIOPATHIES; HUMANS; I-KAPPA B KINASE; MULTIENZYME COMPLEXES; PROTEIN-SERINE-THREONINE KINASES; RAB GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION;

EID: 84961572460     PISSN: 21541248     EISSN: 21541256     Source Type: Journal    
DOI: 10.1080/21541248.2015.1091539     Document Type: Review

References (81)

1. Mizuno-Yamasaki E, Rivera-Molina F, Novick P. GTPase networks in membrane traffic. Annu Rev Biochem 2012; 81:637-59; PMID:22463690; http://dx.doi.org/10.1146/annurev-biochem-052810-093700
2. Stalder D, Antonny B. Arf GTPase regulation through cascade mechanisms and positive feedback loops. FEBS Lett 2013; 587:2028-35; PMID:23684643; http://dx.doi.org/10.1016/j.febslet.2013.05.015
3. Jackson CL. GEF-effector interactions. Cell Logist 2014; 4, e943616; PMID:25610717; http://dx.doi.org/10.4161/21592780.2014.943616
4. Deretic D. Crosstalk of Arf and Rab GTPases en route to cilia. Small GTPases 2013; 4:70-7.
5. Richardson BC, Fromme JC. Autoregulation of Sec7 Arf-GEF activity and localization by positive feedback. Small GTPases 2012; 3:240-3; PMID:22996016; http://dx.doi.org/10.4161/sgtp.21828
6. McDonold CM, Fromme JC. Four GTPases differentially regulate the Sec7 Arf-GEF to direct traffic at the trans-golgi network. Dev Cell 2014; 30:759-67; PMID:25220393; http://dx.doi.org/10.1016/j.devcel.2014.07.016
7. Wright J, Kahn RA, Sztul E. Regulating the large Sec7 ARF guanine nucleotide exchange factors: the when, where and how of activation. Cell Mol Life Sci 2014; 71(18):3419-38; PMID:24728583
8. Zerial M, McBride H. Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2001; 2:107-17; PMID:11252952; http://dx.doi.org/10.1038/35052055
9. Barr FA. Review series: Rab GTPases and membrane identity: causal or inconsequential? J Cell Biol 2013; 202:191-9; PMID:23878272; http://dx.doi.org/10.1083/jcb.201306010
10. Khan AR, Menetrey J. Structural biology of Arf and Rab GTPases’ effector recruitment and specificity. Structure 2013; 21:1284-97; PMID:23931141; http://dx.doi.org/10.1016/j.str.2013.06.016
11. Fliegauf M, Benzing T, Omran H. When cilia go bad: cilia defects and ciliopathies. Nat Rev Mol Cell Biol 2007; 8:880-93; PMID:17955020; http://dx.doi.org/10.1038/nrm2278
12. Gerdes JM, Davis EE, Katsanis N. The vertebrate primary cilium in development, homeostasis, and disease. Cell 2009; 137:32-45; PMID:19345185; http://dx.doi.org/10.1016/j.cell.2009.03.023
13. Valente EM, Rosti RO, Gibbs E, Gleeson JG. Primary cilia in neurodevelopmental disorders. Nat Rev Neurol 2014; 10:27-36; PMID:24296655; http://dx.doi.org/10.1038/nrneurol.2013.247
14. Sang L, Miller JJ, Corbit KC, Giles RH, Brauer MJ, Otto EA, Baye LM, Wen X, Scales SJ, Kwong M, et al. Mapping the NPHP-JBTS-MKS protein network reveals ciliopathy disease genes and pathways. Cell 2011; 145:513-28; PMID:21565611; http://dx.doi.org/10.1016/j.cell.2011.04.019
15. Rosenbaum JL, Witman GB. Intraflagellar transport. Nat Rev Mol Cell Biol 2002; 3:813-25; PMID:12415299; http://dx.doi.org/10.1038/nrm952
16. Bhogaraju S, Engel BD, Lorentzen E. Intraflagellar transport complex structure and cargo interactions. Cilia 2013; 2:10; PMID:23945166; http://dx.doi.org/10.1186/2046-2530-2-10
17. Qin H, Wang Z, Diener D, Rosenbaum J. Intraflagellar transport protein 27 is a small G protein involved in cell-cycle control. Curr Biol 2007; 17:193-202; PMID:17276912; http://dx.doi.org/10.1016/j.cub.2006.12.040
18. NachuryMV, LoktevAV, ZhangQ,WestlakeCJ, Per€anen J, Merdes A, SlusarskiDC, Scheller RH, Bazan JF, Sheffield VC, et al. A core complex of BBS proteins cooperates with the GTPase Rab8 to promote ciliary membrane biogenesis. Cell 2007; 129:1201-13; PMID:17574030; http://dx.doi.org/10.1016/j.cell.2007.03.053
19. Jin H, White SR, Shida T, Schulz S, Aguiar M, Gygi SP, Bazan JF, Nachury MV. The conserved Bardet-Biedl syndrome proteins assemble a coat that traffics membrane proteins to cilia. Cell 2010; 141:1208-19; PMID:20603001; http://dx.doi.org/10.1016/j.cell.2-010.05.015
20. Liew GM, Ye F, Nager AR, Murphy JP, Lee JS, Aguiar M, Breslow DK, Gygi SP, Nachury MV. The intraflagellar transport protein IFT27 promotes BBSome exit from cilia through the GTPase ARL6/BBS3. Dev Cell 2014; 31:265-78; PMID:25443296; http://dx.doi.org/10.1016/j.devcel.2014.09.004
21. Eguether T, San Agustin JT, Keady BT, Jonassen JA, Liang Y, Francis R, Tobita K, Johnson CA, Abdelhamed ZA, Lo CW, et al. IFT27 links the BBSome to IFT for maintenance of the ciliary signaling compartment. Dev Cell 2014; 31:279-90; PMID:25446516; http://dx.doi.org/10.1016/j.devcel.2014.09.011
22. Mourao A, Nager AR, Nachury MV, Lorentzen E. Structural basis for membrane targeting of the BBSome by ARL6. Nat Struct Mol Biol 2014; 21:1035-41; PMID:25402481; http://dx.doi.org/10.1038/nsmb.2920
23. Bhogaraju S, Taschner M, Morawetz M, Basquin C, Lorentzen E. Crystal structure of the intraflagellar transport complex 25/27. EMBO J 2011; 30:1907-18; PMID:21505417; http://dx.doi.org/10.1038/emboj.2011.110
24. Wang J, Deretic D. Molecular complexes that direct rhodopsin transport to primary cilia. Prog Retin Eye Res 2014; 38:1-19; PMID:24135424; http://dx.doi.org/10.1016/j.preteyeres.2013.08.004
25. Mazelova J, Astuto-Gribble L, Inoue H, Tam BM, Schonteich E, Prekeris R, Moritz OL, Randazzo PA, Deretic D. Ciliary targeting motif VxPx directs assembly of a trafficking module through Arf4. EMBO J 2009; 28:183-92; PMID:19153612; http://dx.doi.org/10.1038/emboj.2008.267
26. Wang J, Morita Y, Mazelova J, Deretic D. The Arf GAP ASAP1 provides a platform to regulate Arf4- and Rab11-Rab8-mediated ciliary receptor targeting. EMBO J 2012; 31:4057-71; PMID:22983554; http://dx.doi.org/10.1038/emboj.2012.253
27. Ward HH, Brown-Glaberman U, Wang J, Morita Y, Alper SL, Bedrick EJ, Gattone VH 2nd, Deretic D, Wandinger-Ness A. A conserved signal and GTPase complex are required for the ciliary transport of polycystin- 1. Mol Biol Cell 2011; 22:3289-305; PMID:21775626; http://dx.doi.org/10.1091/mbc.E11-01-0082
28. Brown MT, Andrade J, Radhakrishna H, Donaldson JG, Cooper JA, Randazzo PA. ASAP1, a phospholipiddependent arf GTPase-activating protein that associates with and is phosphorylated by Src. Mol Cell Biol 1998; 18:7038-51; PMID:9819391
29. Randazzo PA, Hirsch DS. Arf GAPs: multifunctional proteins that regulate membrane traffic and actin remodelling. Cell Signal 2004; 16:401-13; PMID:14709330; http://dx.doi.org/10.1016/j.cellsig.2003.09.012
30. Nie Z, Randazzo PA. Arf GAPs and membrane traffic. J Cell Sci 2006; 119:1203-11; PMID:16554436; http://dx.doi.org/10.1242/jcs.02924
31. Hales CM, Griner R, Hobdy-Henderson KC, Dorn MC, Hardy D, Kumar R, Navarre J, Chan EK, Lapierre LA, Goldenring JR. Identification and characterization of a family of Rab11-interacting proteins. J Biol Chem 2001; 276:39067-75; PMID:11495908; http://dx.doi.org/10.1074/jbc.M104831200
32. Junutula JR, Schonteich E, Wilson GM, Peden AA, Scheller RH, Prekeris R. Molecular characterization of Rab11 interactions with members of the family of Rab11-interacting proteins. J Biol Chem 2004; 279:33430-7; PMID:15173169; http://dx.doi.org/10.1074/jbc.M404633200
33. Hattula K, Furuhjelm J, Arffman A, Peranen J. A Rab8-specific GDP/GTP exchange factor is involved in actin remodeling and polarized membrane transport. Mol Biol Cell 2002; 13:3268-80; PMID:12221131; http://dx.doi.org/10.1091/mbc.E02-03-0143
34. Westlake CJ, Baye LM, Nachury MV, Wright KJ, Ervin KE, Phu L, Chalouni C, Beck JS, Kirkpatrick DS, Slusarski DC, et al. Primary cilia membrane assembly is initiated by Rab11 and transport protein particle II (TRAPPII) complex-dependent trafficking of Rabin8 to the centrosome. Proc Natl Acad Sci U S A 2011; 108:2759-64; PMID:21273506; http://dx.doi.org/10.1073/pnas.1018823108
35. Knodler A, Feng S, Zhang J, Zhang X, Das A, Per€anen J, Guo W. Coordination of Rab8 and Rab11 in primary ciliogenesis. Proc Natl Acad Sci U S A 2010; 107 (14):6346-51.
36. Feng S, Kn€odler A, Ren J, Zhang J, Zhang X, Hong Y, Huang S, Per€anen J, Guo W. A Rab8 guanine nucleotide exchange factor-effector interaction network regulates primary ciliogenesis. J Biol Chem 2012; 287:15602-9; PMID:22433857; http://dx.doi.org/10.1074/jbc.M111.333245
37. Deretic D, Huber LA, Ransom N, Mancini M, Simons K, Papermaster DS. rab8 in retinal photoreceptors may participate in rhodopsin transport and in rod outer segment disk morphogenesis. J Cell Sci 1995; 108:215-24; PMID:7738098
38. Moritz OL, Tam BM, Hurd LL, Per€anen J, Deretic D, Papermaster DS. Mutant rab8 impairs docking and fusion of rhodopsin-bearing post-Golgi membranes and causes cell death of transgenic Xenopus rods. Mol Biol Cell 2001; 12:2341-51; PMID:11514620; http://dx.doi.org/10.1091/mbc.12.8.2341
39. Yoshimura S, Egerer J, Fuchs E, Haas AK, Barr FA. Functional dissection of Rab GTPases involved in primary cilium formation. J Cell Biol 2007; 178:363-9; PMID:17646400; http://dx.doi.org/10.1083/jcb.200703047
40. Murga-Zamalloa CA, Atkins SJ, Peranen J, Swaroop A, Khanna H. Interaction of retinitis pigmentosa GTPase regulator (RPGR) with RAB8A GTPase: implications for cilia dysfunction and photoreceptor degeneration. Hum Mol Genet 2010; 19:3591-8; PMID:20631154; http://dx.doi.org/10.1093/hmg/ddq275
41. Bryant DM, Datta A, Rodríguez-Fraticelli AE, Peränen J, Martín-Belmonte F, Mostov KE. A molecular network for de novo generation of the apical surface and lumen. Nat Cell Biol 2010; 12:1035-45; PMID:20890297; http://dx.doi.org/10.1038/ncb2106
42. Overeem AW, Bryant DM, van ISC. Mechanisms of apical-basal axis orientation and epithelial lumen positioning. Trends Cell Biol 2015; 25(8):476-85; PMID:25941134
43. Wang J, Deretic D. The Arf/Rab11 effector FIP3 acts synergistically with the Arf GAP ASAP1 to direct Rabin8 in ciliary receptor targeting. J Cell Sci 2015; 128(7):1375-85.
44. Ullrich O, Reinsch S, Urbe S, Zerial M, Parton RG. Rab11 regulates recycling through the pericentriolar recycling endosome. J Cell Biol 1996; 135:913-24; PMID:8922376; http://dx.doi.org/10.1083/jcb.135.4.913
45. Chen W, Feng Y, Chen D, Wandinger-Ness A. Rab11 is required for trans-golgi network-to-plasma membrane transport and a preferential target for GDP dissociation inhibitor. Mol Biol Cell 1998; 9:3241-57; PMID:9802909; http://dx.doi.org/10.1091/mbc.9.11.3241
46. Ren M, Xu G, Zeng J, De Lemos-Chiarandini C, Adesnik M, Sabatini DD. Hydrolysis of GTP on rab11 is required for the direct delivery of transferrin from the pericentriolar recycling compartment to the cell surface but not from sorting endosomes. Proc Natl Acad Sci U S A 1998; 95:6187-92; PMID:9600939; http://dx.doi.org/10.1073/pnas.95.11.6187
47. Pellinen T, Ivaska J. Integrin traffic. J Cell Sci 2006; 119:3723-31; PMID:16959902; http://dx.doi.org/10.1242/jcs.03216
48. Knowles BC, Weis VG, Yu S, Roland JT, Williams JA, Alvarado GS, Lapierre LA, Shub MD, Gao N, Goldenring JR. Rab11a regulates syntaxin 3 localization and microvillus assembly in enterocytes. J Cell Sci 2015; 128:1617-26; PMID:25673875; http://dx.doi.org/10.1242/jcs.163303
49. Reish NJ, Boitet ER, Bales KL, Gross AK. Nucleotide bound to rab11a controls localization in rod cells but not interaction with rhodopsin. J Neurosci 2014; 34:14854-63; PMID:25378153; http://dx.doi.org/10.1523/JNEUROSCI.1943-14.2014
50. Grossman GH, Watson RF, Pauer GJ, Bollinger K, Hagstrom SA. Immunocytochemical evidence of Tulp1-dependent outer segment protein transport pathways in photoreceptor cells. Exp Eye Res 2011; 93:658-68; PMID:21867699; http://dx.doi.org/10.1016/j.exer.2011.08.005
51. Barrowman J, Bhandari D, Reinisch K, Ferro-Novick S. TRAPP complexes in membrane traffic: convergence through a common Rab. Nat Rev Mol Cell Biol 2010; 11:759-63; PMID:20966969; http://dx.doi.org/10.1038/nrm2999
52. Morozova N, Liang Y, Tokarev AA, Chen SH, Cox R, Andrejic J, Lipatova Z, Sciorra VA, Emr SD, Segev N. TRAPPII subunits are required for the specificity switch of a Ypt-Rab GEF. Nat Cell Biol 2006; 8:1263-9; PMID:17041589; http://dx.doi.org/10.1038/ncb1489
53. Pinar M, Arst HN, Pantazopoulou A, Tagua VG, de los Ríos V, Rodríguez-Salarichs J, Díaz JF, Peñalva MA. TRAPPII regulates exocytic Golgi exit by mediating nucleotide exchange on the Ypt31 ortholog RabERAB11. Proc Natl Acad Sci U S A 2015; 112:4346-51; PMID:25831508; http://dx.doi.org/10.1073/pnas.1419168112
54. Levine TP, Daniels RD, Wong LH, Gatta AT, Gerondopoulos A, Barr FA. Discovery of new Longin and Roadblock domains that form platforms for small GTPases in Ragulator and TRAPP-II. Small GTPases 2013; 4:62-9; PMID:23511850; http://dx.doi.org/10.4161/sgtp.24262
55. Schou KB, Morthorst SK, Christensen ST, Pedersen LB. Identification of conserved, centrosome-targeting ASH domains in TRAPPII complex subunits and TRAPPC8. Cilia 2014; 3:6; PMID:25018876; http://dx.doi.org/10.1186/2046-2530-3-6
56. Wilson GM, Fielding AB, Simon GC, Yu X, Andrews PD, Hames RS, Frey AM, Peden AA, Gould GW, Prekeris R. The FIP3-Rab11 protein complex regulates recycling endosome targeting to the cleavage furrow during late cytokinesis. Mol Biol Cell 2005; 16:849-60; PMID:15601896; http://dx.doi.org/10.1091/mbc.E04-10-0927
57. Schiel JA, Simon GC, Zaharris C, Weisz J, Castle D, Wu CC, Prekeris R. FIP3-endosome-dependent formation of the secondary ingression mediates ESCRT-III recruitment during cytokinesis. Nat Cell Biol 2012; 14:1068-78; PMID:23000966; http://dx.doi.org/10.1038/ncb2577
58. Fielding AB, Schonteich E, Matheson J, Wilson G, Yu X, Hickson GR, Srivastava S, Baldwin SA, Prekeris R, Gould GW. Rab11-FIP3 and FIP4 interact with Arf6 and the exocyst to control membrane traffic in cytokinesis. Embo J 2005; 24:3389-99; PMID:16148947; http://dx.doi.org/10.1038/sj.emboj.7600803
59. Eathiraj S, Mishra A, Prekeris R, Lambright DG. Structural basis for Rab11-mediated recruitment of FIP3 to recycling endosomes. J Mol Biol 2006; 364:121-35; PMID:17007872; http://dx.doi.org/10.1016/j.jmb.2006.08.064
60. Horgan CP, Oleksy A, Zhdanov AV, Lall PY, White IJ, Khan AR, Futter CE, McCaffrey JG, McCaffrey MW. Rab11-FIP3 is critical for the structural integrity of the endosomal recycling compartment. Traffic 2007; 8:414-30; PMID:17394487; http://dx.doi.org/10.1111/j.1600-0854.2007.00543.x
61. Inoue H, Ha VL, Prekeris R, Randazzo PA. Arf GTPase-activating protein ASAP1 interacts with Rab11 effector FIP3 and regulates pericentrosomal localization of transferrin receptor-positive recycling endosome. Mol Biol Cell 2008; 19:4224-37; PMID:18685082; http://dx.doi.org/10.1091/mbc.E08-03-0290
62. Vetter M, Stehle R, Basquin C, Lorentzen E. Structure of Rab11-FIP3-Rabin8 reveals simultaneous binding of FIP3 and Rabin8 effectors to Rab11. Nat Struct Mol Biol 2015; 22(9):695-702; PMID:26258637
63. Vetter IR, Wittinghofer A. The guanine nucleotidebinding switch in three dimensions. Science 2001; 294:1299-304; PMID:11701921; http://dx.doi.org/10.1126/science.1062023
64. Wu S, Mehta SQ, Pichaud F, Bellen HJ, Quiocho FA. Sec15 interacts with Rab11 via a novel domain and affects Rab11 localization in vivo. Nat Struct Mol Biol 2005; 12:879-85; PMID:16155582; http://dx.doi.org/10.1038/nsmb987
65. Zhang XM, Ellis S, Sriratana A, Mitchell CA, Rowe T. Sec15 is an effector for the Rab11 GTPase in mammalian cells. J Biol Chem 2004; 279:43027-34; PMID:15292201; http://dx.doi.org/10.1074/jbc.M402264200
66. Zeng J, Ren M, Gravotta D, De Lemos-Chiarandini C, Lui M, Erdjument-Bromage H, Tempst P, Xu G, Shen TH, Morimoto T, et al. Identification of a putative effector protein for rab11 that participates in transferrin recycling. Proc Natl Acad Sci U S A 1999; 96:2840-5; PMID:10077598; http://dx.doi.org/10.1073/pnas.96.6.2840
67. Eathiraj S, Pan X, Ritacco C, Lambright DG. Structural basis of family-wide Rab GTPase recognition by rabenosyn-5. Nature 2005; 436:415-9; PMID:16034420; http://dx.doi.org/10.1038/nature03798
68. Shiba T, Koga H, Shin HW, Kawasaki M, Kato R, Nakayama K, Wakatsuki S. Structural basis for Rab11- dependent membrane recruitment of a family of Rab11-interacting protein 3 (FIP3)/Arfophilin-1. Proc Natl Acad Sci U S A 2006; 103:15416-21; PMID:17030804; http://dx.doi.org/10.1073/pnas.0605357103
69. Jagoe WN, Lindsay AJ, Read RJ, McCoy AJ, McCaffrey MW, Khan AR. Crystal structure of rab11 in complex with rab11 family interacting protein 2. Structure 2006; 14:1273-83; PMID:16905101; http://dx.doi.org/10.1016/j.str.2006.06.010
70. Burke JE, Inglis AJ, Perisic O, Masson GR, McLaughlin SH, Rutaganira F, Shokat KM, Williams RL. Structures of PI4KIIIbeta complexes show simultaneous recruitment of Rab11 and its effectors. Science 2014; 344:1035-8; PMID:24876499; http://dx.doi.org/10.1126/science.1253397
71. de Graaf P, Zwart WT, van Dijken RA, Deneka M, Schulz TK, Geijsen N, Coffer PJ, Gadella BM, Verkleij AJ, van der Sluijs P, et al. Phosphatidylinositol 4- kinasebeta is critical for functional association of rab11 with the Golgi complex. Mol Biol Cell 2004; 15:2038-47; PMID:14767056; http://dx.doi.org/10.1091/mbc.E03-12-0862
72. Lee MT, Mishra A, Lambright DG. Structural mechanisms for regulation of membrane traffic by rab GTPases. Traffic 2009; 10:1377-89; PMID: 19522756; http://dx.doi.org/10.1111/j.1600-0854.2009.00942.x
73. Pasqualato S, Senic-Matuglia F, Renault L, Goud B, Salamero J, Cherfils J. The structural GDP/GTP cycle of Rab11 reveals a novel interface involved in the dynamics of recycling endosomes. J Biol Chem 2004; 279:11480-8; PMID:14699104; http://dx.doi.org/10.1074/jbc.M310558200
74. Chiba S, Amagai Y, Homma Y, Fukuda M, Mizuno K. NDR2-mediated Rabin8 phosphorylation is crucial for ciliogenesis by switching binding specificity from phosphatidylserine to Sec15. EMBO J 2013; 32(6):874-85; PMID:23435566
75. Caberoy NB, Zhou Y, Alvarado G, Fan X, Li W. Efficient identification of phosphatidylserine-binding proteins by ORF phage display. Biochem Biophys Res Commun 2009; 386:197-201; PMID:19520055; http://dx.doi.org/10.1016/j.bbrc.2009.06.010
76. Mazelova J, Ransom N, Astuto-Gribble L, Wilson MC, Deretic D. Syntaxin 3 and SNAP-25 pairing, regulated by omega-3 docosahexaenoic acid, controls the delivery of rhodopsin for the biogenesis of cilia-derived sensory organelles, the rod outer segments. J Cell Sci 2009; 122:2003-13; PMID:19454479; http://dx.doi.org/10.1242/jcs.039982
77. Berta AI, Boesze-Battaglia K, Genini S, Goldstein O, O’Brien PJ, Sz[1]el [1]A, Acland GM, Beltran WA, Aguirre GD. Photoreceptor cell death, proliferation and formation of hybrid rod/S-cone photoreceptors in the degenerating STK38L mutant retina. PLoS One 2011; 6, e24074; PMID:21980341; http://dx.doi.org/10.1371/journal.pone.0024074
78. Goldstein O, Kukekova AV, Aguirre GD, Acland GM. Exonic SINE insertion in STK38L causes canine early retinal degeneration (erd). Genomics 2010; 96:362-8; PMID:20887780; http://dx.doi.org/10.1016/j.ygeno.2010.09.003
79. Mizuno-Yamasaki E, Medkova M, Coleman J, Novick P. Phosphatidylinositol 4-phosphate controls both membrane recruitment and a regulatory switch of the Rab GEF Sec2p. Dev Cell 2010; 18:828-40; PMID:20493815; http://dx.doi.org/10.1016/j.devcel.2010.03.016
80. Stalder D, Mizuno-Yamasaki E, Ghassemian M, Novick PJ. Phosphorylation of the Rab exchange factor Sec2p directs a switch in regulatory binding partners. Proc Natl Acad Sci U S A 2013; 110:19995-20002; PMID:24248333; http://dx.doi.org/10.1073/pnas.1320029110
81. Guo Z, Hou X, Goody RS, Itzen A. Intermediates in the guanine nucleotide exchange reaction of Rab8 protein catalyzed by guanine nucleotide exchange factors Rabin8 and GRAB. J Biol Chem 2013; 288:32466-74; PMID:24072714; http://dx.doi.org/10.1074/jbc.M113.498329