Membrane curvature generation by a C-terminal amphipathic helix in peripherin-2/rds, a tetraspanin required for photoreceptor sensory cilium morphogenesis

Journal of Cell Science

Volumn 126, Issue 20, 2013, Pages 4659-4670

  Khattree, Nidhi ^a   Ritter, Linda M ^a   Goldberg, Andrew F X ^a  

^a OAKLAND UNIVERSITY   (United States)

Author keywords

Amphipathic helix; Intrinsically disordered; Membrane curvature; Photoreceptor; Retinal degeneration; Tetraspanin

Indexed keywords

LIPOSOME; PERIPHERIN; PHOSPHOLIPID; TETRASPANIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; CELL ORGANELLE; CONTROLLED STUDY; EUKARYOTIC FLAGELLUM; MEMBRANE LEAFLET; MORPHOGENESIS; PHOTORECEPTOR; PHOTORECEPTOR OUTER SEGMENT; PRIORITY JOURNAL; PROTEIN LOCALIZATION; STRUCTURE ACTIVITY RELATION; SURFACE CHARGE; TRANSMISSION ELECTRON MICROSCOPY;

AMPHIPATHIC HELIX; INTRINSICALLY DISORDERED; MEMBRANE CURVATURE; PHOTORECEPTOR; RETINAL DEGENERATION; TETRASPANIN;

AMINO ACID SEQUENCE; ANIMALS; CATTLE; CILIA; HUMANS; MICE; MOLECULAR SEQUENCE DATA; MORPHOGENESIS; PERIPHERINS; PHOTORECEPTOR CELLS; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID; TETRASPANINS;

EID: 84885462612     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.126888     Document Type: Article

References (71)

1. Allen, T. M. and Cleland, L. G. (1980). Serum-induced leakage of liposome contents. Biochim. Biophys. Acta 597, 418-426.
2. Anderson, R. E., and Maude, M. B. (1970). Phospholipids of bovine outer segments. Biochemistry 9, 3624-3628.
3. Antonny, B. (2011). Mechanisms of membrane curvature sensing. Annu. Rev. Biochem. 80, 101-123.
4. Arikawa, K., Molday, L. L., Molday, R. S., and Williams, D. S. (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.
5. Arshavsky, V. Y., and Burns, M. E. (2012). Photoreceptor signaling: supporting vision across a wide range of light intensities. J. Biol. Chem. 287, 1620-1626.
6. Bartlett, G. R. (1959). Phosphorus assay in column chromatography. J. Biol. Chem. 234, 466-468.
7. Bascom, R. A., Manara, S., Collins, L., Molday, R. S., Kalnins, V. I., and McInnes, R. R. (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.
8. Berditchevski, F., and Rubinstein, E. (2013). Tetraspanins. New York, NY: Springer Science.
9. Berger, W., Kloeckener-Gruissem, B., and Neidhardt, J. (2010). The molecular basis of human retinal and vitreoretinal diseases. Prog. Retin. Eye Res. 29, 335-375.
10. Bigay, J., Casella, J. F., Drin, G., Mesmin, B., and Antonny, B. (2005). ArfGAP1 responds to membrane curvature through the folding of a lipid packing sensor motif. EMBO J. 24, 2244-2253.
11. Boesze-Battaglia, K., Lamba, O. P., Napoli, A. A., Jr, Sinha, S., and Guo, Y. (1998). Fusion between retinal rod outer segment membranes and model membranes: a role for photoreceptor peripherin/rds. Biochemistry 37, 9477-9487.
12. Boesze-Battaglia, K., Stefano, F. P., Fenner, M., and Napoli, A. A., Jr (2000). A peptide analogue to a fusion domain within photoreceptor peripherin/rds promotes membrane adhesion and depolarization. Biochim. Biophys. Acta 1463, 343-354.
13. Boesze-Battaglia, K., Goldberg, A. F., Dispoto, J., Katragadda, M., Cesarone, G., and Albert, A. D. (2003). A soluble peripherin/Rds C-terminal polypeptide promotes membrane fusion and changes conformation upon membrane association. Exp. Eye Res. 77, 505-514.
14. Boon, C. J., den Hollander, A. I., Hoyng, C. B., Cremers, F. P., Klevering, B. J., and Keunen, J. E. (2008). The spectrum of retinal dystrophies caused by mutations in the peripherin/RDS gene. Prog. Retin. Eye Res. 27, 213-235.
15. Boucrot, E., Pick, A., Çamdere, G., Liska, N., Evergren, E., McMahon, H. T., and Kozlov, M. M. (2012). Membrane fission is promoted by insertion of amphipathic helices and is restricted by crescent BAR domains. Cell 149, 124-136.
16. Campelo, F., McMahon, H. T., and Kozlov, M. M. (2008). The hydrophobic insertion mechanism of membrane curvature generation by proteins. Biophys. J. 95, 2325-2339.
17. Chakraborty, D., Ding, X. Q., Conley, S. M., Fliesler, S. J., and Naash, M. I. (2009). Differential requirements for retinal degeneration slow intermolecular disulfidelinked oligomerization in rods versus cones. Hum. Mol. Genet. 18, 797-808.
18. Cheng, T., Peachey, N. S., Li, S., Goto, Y., Cao, Y., and Naash, M. I. (1997). The effect of peripherin/rds haploinsufficiency on rod and cone photoreceptors. J. Neurosci. 17, 8118-8128.
19. Clarke, G., Goldberg, A. F., Vidgen, D., Collins, L., Ploder, L., Schwarz, L., Molday, L. L., Rossant, J., Sze'l, A., Molday, R. S. et al. (2000). Rom-1 is required for rod photoreceptor viability and the regulation of disk morphogenesis. Nat. Genet. 25, 67-73.
20. Conley, S. M., and Naash, M. I. (2009). Focus on molecules: RDS. Exp. Eye Res. 89, 278-279.
21. Connell, G. J., and Molday, R. S. (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.
22. Corless, J. M., and Fetter, R. D. (1987). Structural features of the terminal loop region of frog retinal rod outer segment disk membranes: III. Implications of the terminal loop complex for disk morphogenesis, membrane fusion, and cell surface interactions. J. Comp. Neurol. 257, 24-38.
23. Drin, G., and Antonny, B. (2010). Amphipathic helices and membrane curvature. FEBS Lett. 584, 1840-1847.
24. Drin, G., Casella, J. F., Gautier, R., Boehmer, T., Schwartz, T. U., and Antonny, B. (2007). A general amphipathic a-helical motif for sensing membrane curvature. Nat. Struct. Mol. Biol. 14, 138-146.
25. Edrington, T. C., 5th, Lapointe, R., Yeagle, P. L., Gretzula, C. L., and Boesze- Battaglia, K. (2007). Peripherin-2: an intracellular analogy to viral fusion proteins. Biochemistry 46, 3605-3613.
26. Farjo, R., and Naash, M. I. (2006). The role of Rds in outer segment morphogenesis and human retinal disease. Ophthalmic Genet. 27, 117-122.
27. Farsad, K., and De Camilli, P. (2003). Mechanisms of membrane deformation. Curr. Opin. Cell Biol. 15, 372-381.
28. Fliesler, S. J., and Schroepfer, G. J., Jr (1982). Sterol composition of bovine retinal rod outer segment membranes and whole retinas. Biochim. Biophys. Acta 711, 138-148.
29. Folch, J., Lees, M., and Sloane Stanley, G. H. (1957). A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 226, 497-509.
30. Ford, M. G., Mills, I. G., Peter, B. J., Vallis, Y., Praefcke, G. J., Evans, P. R., and McMahon, H. T. (2002). Curvature of clathrin-coated pits driven by epsin. Nature 419, 361-366.
31. Gautier, R., Douguet, D., Antonny, B., and Drin, G. (2008). HELIQUEST: a web server to screen sequences with specific a-helical properties. Bioinformatics 24, 2101- 2102.
32. Gennis, R. B. (1989). The structures and properties of membrane lipids. In Biomembranes: Molecular Structure and Function, pp. 36-84. New York, NY: Springer-Verlag.
33. Goldberg, A. F. (2006). Role of peripherin/rds in vertebrate photoreceptor architecture and inherited retinal degenerations. Int. Rev. Cytol. 253, 131-175.
34. Goldberg, A. F., and Molday, R. S. (1996a). Defective subunit assembly underlies a digenic form of retinitis pigmentosa linked to mutations in peripherin/rds and rom-1. Proc. Natl. Acad. Sci. USA 93, 13726-13730.
35. Goldberg, A. F., and Molday, R. S. (1996b). Subunit composition of the peripherin/rdsrom- 1 disk rim complex from rod photoreceptors: hydrodynamic evidence for a tetrameric quaternary structure. Biochemistry 35, 6144-6149.
36. Goldberg, A. F., and Molday, R. S. (2000). Expression and characterization of peripherin/rds-rom-1 complexes and mutants implicated in retinal degenerative diseases. Methods Enzymol. 316, 671-687.
37. Goldberg, A. F., Moritz, O. L., and Molday, R. S. (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.
38. Goldberg, A. F., Fales, L. M., Hurley, J. B., and Khattree, N. (2001). Folding and subunit assembly of photoreceptor peripherin/rds is mediated by determinants within the extracellular/intradiskal EC2 domain: implications for heterogeneous molecular pathologies. J. Biol. Chem. 276, 42700-42706.
39. Goldberg, A. F., Ritter, L. M., Khattree, N., Peachey, N. S., Fariss, R. N., Dang, L., Yu, M., and Bottrell, A. R. (2007). An intramembrane glutamic acid governs peripherin/rds function for photoreceptor disk morphogenesis. Invest. Ophthalmol. Vis. Sci. 48, 2975-2986.
40. Graham, T. R., and Kozlov, M. M. (2010). Interplay of proteins and lipids in generating membrane curvature. Curr. Opin. Cell Biol. 22, 430-436.
41. Hawkins, R. K., Jansen, H. G., and Sanyal, S. (1985). Development and degeneration of retina in rds mutant mice: photoreceptor abnormalities in the heterozygotes. Exp. Eye Res. 41, 701-720.
42. Jansen, H. G., and Sanyal, S. (1984). Development and degeneration of retina in rds mutant mice: electron microscopy. J. Comp. Neurol. 224, 71-84.
43. Kajiwara, K., Sandberg, M. A., Berson, E. L., and Dryja, T. P. (1993). A null mutation in the human peripherin/RDS gene in a family with autosomal dominant retinitis punctata albescens. Nat. Genet. 3, 208-212.
44. Kedzierski, W., Nusinowitz, S., Birch, D., Clarke, G., McInnes, R. R., Bok, D., and Travis, G. H. (2001). Deficiency of rds/peripherin causes photoreceptor death in mouse models of digenic and dominant retinitis pigmentosa. Proc. Natl. Acad. Sci. USA 98, 7718-7723.
45. Loewen, C. J., and Molday, R. S. (2000). Disulfide-mediated oligomerization of Peripherin/Rds and Rom-1 in photoreceptor disk membranes. Implications for photoreceptor outer segment morphogenesis and degeneration. J. Biol. Chem. 275, 5370-5378.
46. MacDonald, R. C., MacDonald, R. I., Menco, B. P., Takeshita, K., Subbarao, N. K., and Hu, L. R. (1991). Small-volume extrusion apparatus for preparation of large, unilamellar vesicles. Biochim. Biophys. Acta 1061, 297-303.
47. Matsuoka, K., and Schekman, R. (2000). The use of liposomes to study COPII- and COPI-coated vesicle formation and membrane protein sorting. Methods 20, 417-428.
48. McMahon, H. T., and Gallop, J. L. (2005). Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature 438, 590-596.
49. McMahon, H. T., Kozlov, M. M., and Martens, S. (2010). Membrane curvature in synaptic vesicle fusion and beyond. Cell 140, 601-605.
50. Miljanich, G. P., Sklar, L. A., White, D. L., and Dratz, E. A. (1979). Disaturated and dipolyunsaturated phospholipids in the bovine retinal rod outer segment disk membrane. Biochim. Biophys. Acta 552, 294-306.
51. Molday, R. S., Hicks, D., and Molday, L. (1987). Peripherin. A rim-specific membrane protein of rod outer segment discs. Invest. Ophthalmol. Vis. Sci. 28, 50-61.
52. Nickell, S., Park, P. S., Baumeister, W., and Palczewski, K. (2007). Three-dimensional architecture of murine rod outer segments determined by cryoelectron tomography. J. Cell Biol. 177, 917-925.
53. Palczewski, K. (2012). Chemistry and biology of vision. J. Biol. Chem. 287, 1612-1619.
54. Papermaster, D. S. (1982). Preparation of retinal rod outer segments. Methods Enzymol. 81, 48-52.
55. Rajamoorthi, K., Petrache, H. I., McIntosh, T. J., and Brown, M. F. (2005). Packing and viscoelasticity of polyunsaturated omega-3 and omega-6 lipid bilayers as seen by (2)H NMR and X-ray diffraction. J. Am. Chem. Soc. 127, 1576-1588.
56. Ritter, L. M., Boesze-Battaglia, K., Tam, B. M., Moritz, O. L., Khattree, N., Chen, S. C., and Goldberg, A. F. (2004). Uncoupling of photoreceptor peripherin/rds fusogenic activity from biosynthesis, subunit assembly, and targeting: a potential mechanism for pathogenic effects. J. Biol. Chem. 279, 39958-39967.
57. Ritter, L. M., Arakawa, T., and Goldberg, A. F. (2005). Predicted and measured disorder in peripherin/rds, a retinal tetraspanin. Protein Pept. Lett. 12, 677-686.
58. Ritter, L. M., Khattree, N., Tam, B., Moritz, O. L., Schmitz, F., and Goldberg, A. F. (2011). In situ visualization of protein interactions in sensory neurons: glutamic acidrich proteins (GARPs) play differential roles for photoreceptor outer segment scaffolding. J. Neurosci. 31, 11231-11243.
59. Roof, D. J., and Heuser, J. E. (1982). Surfaces of rod photoreceptor disk membranes: integral membrane components. J. Cell Biol. 95, 487-500.
60. Salinas, R. Y., Baker, S. A., Gospe, S. M., 3rd and Arshavsky, V. Y. (2013). A single valine residue plays an essential role in peripherin/rds targeting to photoreceptor outer segments. PLoS ONE 8, e54292.
61. Shibata, Y., Hu, J., Kozlov, M. M., and Rapoport, T. A. (2009). Mechanisms shaping the membranes of cellular organelles. Annu. Rev. Cell Dev. Biol. 25, 329-354.
62. Soubias, O., Teague, W. E., Jr, Hines, K. G., Mitchell, D. C., and Gawrisch, K. (2010). Contribution of membrane elastic energy to rhodopsin function. Biophys. J. 99, 817-824.
63. Steinberg, R. H., Fisher, S. K., and Anderson, D. H. (1980). Disc morphogenesis in vertebrate photoreceptors. J. Comp. Neurol. 190, 501-518.
64. Strandberg, E., Tiltak, D., Ehni, S., Wadhwani, P., and Ulrich, A. S. (2012). Lipid shape is a key factor for membrane interactions of amphipathic helical peptides. Biochim. Biophys. Acta 1818, 1764-1776.
65. Sung, C. H., and Chuang, J. Z. (2010). The cell biology of vision. J. Cell Biol. 190, 953-963.
66. Tam, B. M., Moritz, O. L., and Papermaster, D. S. (2004). The C terminus of peripherin/rds participates in rod outer segment targeting and alignment of disk incisures. Mol. Biol. Cell 15, 2027-2037.
67. Taneva, S. G., Lee, J. M., and Cornell, R. B. (2012). The amphipathic helix of an enzyme that regulates phosphatidylcholine synthesis remodels membranes into highly curved nanotubules. Biochim. Biophys. Acta 1818, 1173-1186.
68. Tate, M. W., and Gruner, S. M. (1987). Lipid polymorphism of mixtures of dioleoylphosphatidylethanolamine and saturated and monounsaturated phosphatidylcholines of various chain lengths. Biochemistry 26, 231-236.
69. Travis, G. H., Groshan, K. R., Lloyd, M., and Bok, D. (1992). Complete rescue of photoreceptor dysplasia and degeneration in transgenic retinal degeneration slow (rds) mice. Neuron 9, 113-119.
70. Wassall, S. R., and Stillwell, W. (2008). Docosahexaenoic acid domains: the ultimate non-raft membrane domain. Chem. Phys. Lipids 153, 57-63.
71. Wrigley, J. D., Ahmed, T., Nevett, C. L., and Findlay, J. B. (2000). Peripherin/rds influences membrane vesicle morphology. Implications for retinopathies. J. Biol. Chem. 275, 13191-13194.