An unconventional secretory pathway mediates the cilia targeting of peripherin/rds

Journal of Neuroscience

Volumn 34, Issue 3, 2014, Pages 992-1006

  Tian, Guilian ^a   Ropelewski, Philip ^a   Nemet, Ina ^a   Lee, Richard ^a   Lodowski, Kerrie H ^a   Imanishi, Yoshikazu ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cilia; Peripherin rds; Photoreceptor; Retina; Trafficking; Unconventional secretion

Indexed keywords

BREFELDIN A; ENDOGLYCOSIDASE H; GLYCOSIDASE; MONENSIN; PERIPHERIN; RHODOPSIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BIOTINYLATION; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; ELECTRON MICROSCOPY; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GLYCOSYLATION; GOLGI COMPLEX; HUMAN; IMMUNOFLUORESCENCE MICROSCOPY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOTORECEPTOR; PHOTORECEPTOR CONNECTING CILIUM; PRIORITY JOURNAL; PROTEIN SYNTHESIS; SECRETORY PATHWAY; WESTERN BLOTTING; XENOPUS LAEVIS;

CILIA; PERIPHERIN/RDS; PHOTORECEPTOR; RETINA; TRAFFICKING; UNCONVENTIONAL SECRETION;

AMINO ACID SEQUENCE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CATTLE; CELL LINE; CILIA; HUMANS; PERIPHERINS; PROTEIN TRANSPORT; RETINAL ROD PHOTORECEPTOR CELLS; SECRETORY PATHWAY; XENOPUS LAEVIS;

EID: 84892419205     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3437-13.2014     Document Type: Article

References (56)

1. Aridor M, Bannykh SI, Rowe T, Balch WE (1995) Sequential coupling between COPII and COPI vesicle coats in endoplasmic reticulum to Golgi transport. J Cell Biol 131:875-893. CrossRef Medline
2. Arikawa K, Molday LL, Molday RS, Williams DS (1992) Localization of peripherin/rds in the disk membranes of cone and rod photoreceptors: relationship to disk membrane morphogenesis and retinal degeneration. J Cell Biol 116:659-667. CrossRef Medline
3. Baker SA, Haeri M, Yoo P, Gospe SM 3rd, Skiba NP, Knox BE, Arshavsky VY (2008) The outer segment serves as a default destination for the trafficking of membrane proteins in photoreceptors. J Cell Biol 183:485-498. CrossRef Medline
4. Bascom RA, Manara S, Collins L, Molday RS, Kalnins VI, McInnes RR (1992) Cloning of the cDNA for a novel photoreceptor membrane protein (rom-1) identifies a disk rim protein family implicated in human retinopathies. Neuron 8:1171-1184. CrossRef Medline
5. Basinger S, Bok D, Hall M (1976) Rhodopsin in the rod outer segment plasma membrane. J Cell Biol 69:29-42. CrossRef Medline
6. Berbari NF, Johnson AD, Lewis JS, Askwith CC, Mykytyn K (2008) Identification of ciliary localization sequences within the third intracellular loop of G-protein-coupled receptors. Mol Biol Cell 19:1540-1547. CrossRef Medline
7. Boehlke C, Bashkurov M, Buescher A, Krick T, John AK, Nitschke R, Walz G, Kuehn EW (2010) Differential role of Rab proteins in ciliary trafficking: Rab23 regulates smoothened levels. J Cell Sci 123:1460-1467. CrossRef Medline
8. Boesze-Battaglia K, Song H, Sokolov M, Lillo C, Pankoski-Walker L, Gretzula C, Gallagher B, Rachel RA, Jenkins NA, Copeland NG, Morris F, Jacob J, Yeagle P, Williams DS, Damek-PoprawaM (2007) The tetraspanin protein peripherin-2 forms a complex with melanoregulin, a putative membrane fusion regulator. Biochemistry 46:1256-1272. CrossRef Medline
9. Chudakov DM, Lukyanov S, Lukyanov KA (2007) Tracking intracellular protein movements using photoswitchable fluorescent proteins PS-CFP2 and Dendra2. Nat Protoc 2:2024-2032. CrossRef Medline
10. Connell GJ, Molday RS (1990) Molecular cloning, primary structure, and orientation of the vertebrate photoreceptor cell protein peripherin in the rod outer segment disk membrane. Biochemistry 29:4691-4698. CrossRef Medline
11. Damek-Poprawa M, Krouse J, Gretzula C, Boesze-Battaglia K (2005) A novel tetraspanin fusion protein, peripherin-2, requires a region upstream of the fusion domain for activity. J Biol Chem 280:9217-9224. CrossRef Medline
12. Deretic D, Papermaster DS (1991) Polarized sorting of rhodopsin on post-Golgi membranes in frog retinal photoreceptor cells. J Cell Biol 113:1281-1293. CrossRef Medline
13. Deretic D, Williams AH, Ransom N, Morel V, Hargrave PA, Arendt A (2005) Rhodopsin C terminus, the site of mutations causing retinal disease, regulates trafficking by binding to ADP-ribosylation factor 4 (ARF4). Proc Natl Acad Sci U S A 102:3301-3306. CrossRef Medline
14. Fariss RN, Molday RS, Fisher SK, Matsumoto B (1997) Evidence from normal and degenerating photoreceptors that two outer segment integral membrane proteins have separate transport pathways. J Comp Neurol 387:148-156. CrossRef Medline
15. Farjo R, Skaggs JS, Nagel BA, Quiambao AB, Nash ZA, Fliesler SJ, Naash MI (2006) Retention of function without normal disc morphogenesis occurs in cone but not rod photoreceptors. J Cell Biol 173:59-68. CrossRef Medline
16. Gee HY, Noh SH, Tang BL, Kim KH, Lee MG (2011) Rescue of DeltaF508-CFTR trafficking via a GRASP-dependent unconventional secretion pathway. Cell 146:746-760. CrossRef Medline
17. Giuliani F, Grieve A, Rabouille C (2011) Unconventional secretion: a stress on GRASP. Curr Opin Cell Biol 23:498-504. CrossRef Medline
18. Goedhart J, von Stetten D, Noirclerc-Savoye M, Lelimousin M, Joosen L, Hink MA, van Weeren L, Gadella TW Jr, Royant A (2012) Structureguided evolution of cyan fluorescent proteins towards a quantum yield of 93%. Nat Commun 3:751. CrossRef Medline
19. Goldberg AF, Molday RS (1996) Subunit composition of the peripherin/ rds-rom-1 disk rim complex from rod photoreceptors: hydrodynamic evidence for a tetrameric quaternary structure. Biochemistry 35:6144-6149. CrossRef Medline
20. Goldberg AF, Moritz OL, Molday RS (1995) Heterologous expression of photoreceptor peripherin/rds and Rom-1 in COS-1 cells: assembly, interactions, and localization of multisubunit complexes. Biochemistry 34: 14213-14219. CrossRef Medline
21. Grieve AG, Rabouille C (2011) Golgi bypass: skirting around the heart of classical secretion. Cold Spring Harb Perspect Biol 3:1-15. CrossRef Medline
22. Gurskaya NG, Verkhusha VV, Shcheglov AS, Staroverov DB, Chepurnykh TV, Fradkov AF, Lukyanov S, Lukyanov KA (2006) Engineering of a monomeric green-to-red photoactivatable fluorescent protein induced by blue light. Nat Biotechnol 24:461-465. CrossRef Medline
23. Haeri M, Knox BE (2012) Rhodopsin mutant P23H destabilizes rod photoreceptor disk membranes. PLoS One 7:e30101. CrossRef Medline
24. Hoffmeister H, Babinger K, Gürster S, Cedzich A, Meese C, Schadendorf K, Osten L, de Vries U, Rascle A, Witzgall R (2011) Polycystin-2 takes different routes to the somatic and ciliary plasma membrane. J Cell Biol 192:631-645. CrossRef Medline
25. Khattree N, Ritter LM, Goldberg AF (2013) Membrane curvature generation by a C-terminal amphipathic helix in peripherin-2/rds, a tetraspanin required for photoreceptor sensory cilium morphogenesis. J Cell Sci 126: 4659-4670. CrossRef Medline
26. Kim J, Lee JE, Heynen-Genel S, Suyama E, Ono K, Lee K, Ideker T, Aza-Blanc P, Gleeson JG (2010) Functional genomic screen for modulators of ciliogenesis and cilium length. Nature 464:1048-1051. CrossRef Medline
27. Kuehn MJ, Herrmann JM, Schekman R (1998) COPII-cargo interactions direct protein sorting into ER-derived transport vesicles. Nature 391:187-190. CrossRef Medline
28. Lodowski KH, Lee R, Ropelewski P, Nemet I, Tian G, Imanishi Y (2013) Signals governing the trafficking and mistrafficking of a ciliary GPCR, rhodopsin. J Neurosci 33:13621-13638. CrossRef Medline
29. Loewen CJ, Moritz OL, Tam BM, Papermaster DS, Molday RS (2003) The role of subunit assembly in peripherin-2 targeting to rod photoreceptor disk membranes and retinitis pigmentosa. Mol Biol Cell 14:3400-3413. CrossRef Medline
30. McKenzie D, Arendt A, Hargrave P, McDowell JH, Molday RS (1984) Localization of binding sites for carboxyl terminal specific anti-rhodopsin monoclonal antibodies using synthetic peptides. Biochemistry 23:6544-6549. CrossRef Medline
31. Mazelova J, Astuto-Gribble L, Inoue H, Tam BM, Schonteich E, Prekeris R, Moritz OL, Randazzo PA, DereticD (2009) Ciliary targeting motif VxPx directs assembly of a trafficking module through Arf4. EMBO J 28:183-192. CrossRef Medline
32. Mollenhauer HH, Morré DJ, Rowe LD (1990) Alteration of intracellular traffic by monensin; mechanism, specificity and relationship to toxicity. Biochim Biophys Acta 1031:225-246. CrossRef Medline
33. Moritz OL, Tam BM, Papermaster DS, Nakayama T (2001) A functional rhodopsin-green fluorescent protein fusion protein localizes correctly in transgenic Xenopus laevis retinal rods and is expressed in a timedependent pattern. J Biol Chem 276:28242-28251. CrossRef Medline
34. Muller-Weeks S, Boesze-Battaglia K, FitzgeraldC (2002) Deletional analysis of the rod photoreceptor cell peripherin/RDS carboxy-terminal region. Exp Eye Res 75:143-154. CrossRef Medline
35. Nebenführ A, Ritzenthaler C, Robinson DG (2002) Brefeldin A: deciphering an enigmatic inhibitor of secretion. Plant Physiology 130:1102-1108. CrossRef Medline
36. Nieland TJ, Feng Y, Brown JX, Chuang TD, Buckett PD, Wang J, Xie XS, McGraw TE, Kirchhausen T, Wessling-Resnick M (2004) Chemical genetic screening identifies sulfonamides that raise organellar pH and interfere with membrane traffic. Traffic 5:478-492. CrossRef Medline
37. Nieuwkoop PD, Faber J (1967) Normal table for Xenopus laevis (Daudin): a systematical and chronological survey of the development from the fertilized egg till the end of metamorphosis, Ed 2. Amsterdam: North-Holland.
38. Poetsch A, Molday LL, Molday RS (2001) The cGMP-gated channel and related glutamic acid-rich proteins interact with peripherin-2 at the rim region of rod photoreceptor disc membranes. J Biol Chem 276:48009-48016. CrossRef Medline
39. Rabouille C, Hui N, Hunte F, Kieckbusch R, Berger EG, Warren G, Nilsson T (1995) Mapping the distribution of Golgi enzymes involved in the construction of complex oligosaccharides. J Cell Sci 108:1617-1627. Medline
40. Ritter LM, Khattree N, Tam B, Moritz OL, Schmitz F, Goldberg AF (2011) In situ visualization of protein interactions in sensory neurons: glutamic acid-rich proteins (GARPs) play differential roles for photoreceptor outer segment scaffolding. J Neurosci 31:11231-11243. CrossRef Medline
41. Salinas RY, Baker SA, Gospe SM 3rd, Arshavsky VY (2013) A single valine residue plays an essential role in peripherin/rds targeting to photoreceptor outer segments. PLoS One 8:e54292. CrossRef Medline
42. Scheel J, Pepperkok R, Lowe M, Griffiths G, Kreis TE (1997) Dissociation of coatomer from membranes is required for brefeldin A-induced transfer of Golgi enzymes to the endoplasmic reticulum. J Cell Biol 137:319-333. CrossRef Medline
43. Schotman H, Karhinen L, Rabouille C (2008) dGRASP-mediated noncanonical integrin secretion is required for Drosophila epithelial remodeling. Dev Cell 14:171-182. CrossRef Medline
44. Smith SJ, Fairclough L, Latinkic BV, Sparrow DB, Mohun TJ (2006) Xenopus laevis transgenesis by sperm nuclear injection. Nat Protoc 1:2195-2203. CrossRef Medline
45. Stefano FP, Krouse J, Marta P, Boesze-Battaglia K (2002) Heterologous expression of WT and mutant photoreceptor peripherin/rds in Madin Darby canine kidney cells: an assessment of fusogenic function. Exp Eye Res 74:267-283. CrossRef Medline
46. Tam BM, Moritz OL, Papermaster DS (2004) TheCterminus of peripherin/ rds participates in rod outer segment targeting and alignment of disk incisures. Mol Biol Cell 15:2027-2037. CrossRef Medline
47. Tam BM, Xie G, Oprian DD, Moritz OL (2006) Mislocalized rhodopsin does not require activation to cause retinal degeneration and neurite outgrowth in Xenopus laevis. J Neurosci 26:203-209. CrossRef Medline
48. Tian G, Zhou Y, Hajkova D, Miyagi M, Dinculescu A, Hauswirth WW, Palczewski K, Geng R, Alagramam KN, Isosomppi J, Sankila EM, Flannery JG, Imanishi Y (2009) Clarin-1, encoded by the Usher Syndrome III causative gene, forms a membranous microdomain: possible role of clarin-1 in organizing the actin cytoskeleton. J Biol Chem 284:18980-18993. CrossRef Medline
49. Travis GH, Brennan MB, Danielson PE, Kozak CA, Sutcliffe JG (1989) Identification of a photoreceptor-specificmRNAencoded by the gene responsible for retinal degeneration slow (rds). Nature 338:70-73. CrossRef Medline
50. Trivedi D, Colin E, Louie CM, Williams DS (2012) Live-cell imaging evidence for the ciliary transport of rod photoreceptor opsin by heterotrimeric kinesin-2. J Neurosci 32:10587-10593. CrossRef Medline
51. van Nie R, Iványi D, Démant P (1978) A new H-2-linked mutation, rds, causing retinal degeneration in the mouse. Tissue Antigens 12:106-108. CrossRef Medline
52. Velasco A, Hendricks L, Moremen KW, Tulsiani DR, Touster O, Farquhar MG (1993) Cell type-dependent variations in the subcellular distribution of alpha-mannosidase I and II. J Cell Biol 122:39-51. CrossRef Medline
53. Wang J, Morita Y, Mazelova J, Deretic D (2012) The Arf GAP ASAP1 provides a platform to regulate Arf4-and Rab11-Rab8-mediated ciliary receptor targeting. EMBO J 31:4057-4071. CrossRef Medline
54. Yoo JS, Moyer BD, Bannykh S, Yoo HM, Riordan JR, Balch WE (2002) Non-conventional trafficking of the cystic fibrosis transmembrane conductance regulator through the early secretory pathway. J Biol Chem 277:11401-11409. CrossRef Medline
55. Zhang Y, Molday LL, Molday RS, Sarfare SS, Woodruff ML, Fain GL, Kraft TW, Pittler SJ (2009) Knockout of GARPs and the beta-subunit of the rod cGMP-gated channel disrupts disk morphogenesis and rod outer segment structural integrity. J Cell Sci 122:1192-1200. CrossRef Medline
56. Zhao C, Malicki J (2011) Nephrocystins andMKSproteins interact with IFT particle and facilitate transport of selected ciliary cargos. EMBO J 30: 2532-2544. CrossRef Medline