Targeting of mouse guanylate cyclase 1 (Gucy2e) to Xenopus laevis rod outer segments

Vision Research

Volumn 51, Issue 21-22, 2011, Pages 2304-2311

  Karan, Sukanya ^a   Tam, Beatrice M ^b   Moritz, Orson L ^b   Baehr, Wolfgang ^a,c,d  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c UNIVERSITY OF UTAH   (United States)

^d UNIVERSITY OF UTAH HEALTH SCIENCES CENTER   (United States)

Author keywords

Guanylate cyclase; Membrane associated EGFP fusion protein; Membrane protein transport; Targeting signals; Transgenic Xenopus

Indexed keywords

GREEN FLUORESCENT PROTEIN; GUANYLATE CYCLASE; HYBRID PROTEIN; RHODOPSIN;

AMINO ACID SEQUENCE; ANIMAL TISSUE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CYTOPLASM; EMBRYO; EXTRACELLULAR SPACE; MEMBRANE TRANSPORT; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOTORECEPTOR; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN TARGETING; RETINA ROD; RETINA ROD OUTER SEGMENT; SIGNAL TRANSDUCTION; XENOPUS LAEVIS;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL MEMBRANE; GUANYLATE CYCLASE; MEMBRANE FUSION PROTEINS; MOLECULAR SEQUENCE DATA; PROTEIN SORTING SIGNALS; RECEPTORS, CELL SURFACE; ROD CELL OUTER SEGMENT; XENOPUS LAEVIS;

EID: 82455192732     PISSN: 00426989     EISSN: 18785646     Source Type: Journal    
DOI: 10.1016/j.visres.2011.09.001     Document Type: Article

References (43)

1. Avasthi P., Watt C.B., Williams D.S., Le Y.Z., Li S., Chen C.K., et al. Trafficking of membrane proteins to cone but not rod outer segments is dependent on heterotrimeric kinesin-II. Journal of Neuroscience 2009, 29:14287-14298.
2. Azadi S., Molday L.L., Molday R.S. RD3, the protein associated with Leber congenital amaurosis type 12, is required for guanylate cyclase trafficking in photoreceptor cells. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:21158-21163.
3. Baehr W., Karan S., Maeda T., Luo D.G., Li S., Bronson J.D., et al. The function of guanylate cyclase 1 and guanylate cyclase 2 in rod and cone photoreceptors. Journal of Biological Chemistry 2007, 282:8837-8847.
4. Baker S.A., Haeri M., Yoo P., Gospe S.M., Skiba N.P., Knox B.E., et al. The outer segment serves as a default destination for the trafficking of membrane proteins in photoreceptors. Journal of Cell Biology 2008, 183:485-498.
5. Bereta G., Wang B., Kiser P.D., Baehr W., Jang G.F., Palczewski K. A functional kinase homology domain is essential for the activity of photoreceptor guanylate cyclase 1. Journal of Biological Chemistry 2010, 285:1899-1908.
6. Bhowmick R., Li M., Sun J., Baker S.A., Insinna C., Besharse J.C. Photoreceptor IFT complexes containing chaperones, guanylyl cyclase 1 and rhodopsin. Traffic 2009, 10:648-663.
7. Concepcion F., Mendez A., Chen J. The carboxyl-terminal domain is essential for rhodopsin transport in rod photoreceptors. Vision Research 2002, 42:417-426.
8. Deretic D. Rab proteins and post-Golgi trafficking of rhodopsin in photoreceptor cells. Electrophoresis 1997, 18:2537-2541.
9. Deretic D. Post-Golgi trafficking of rhodopsin in retinal photoreceptors. Eye 1998, 12(Pt 3b):526-530.
10. Deretic D., Huber L.A., Ransom N., Mancini M., Simons K., Papermaster D.S. Rab8 in retinal photoreceptors may participate in rhodopsin transport and in rod outer segment disk morphogenesis. Journal of Cell Science 1995, 108:215-224.
11. Deretic D., Williams A.H., Ransom N., Morel V., HArgrave P.A., Arendt A. Rhodopsin C terminus, the site of mutations causing retinal disease, regulates trafficking by binding to ADP-ribosylation factor 4 (ARF4). Proceedings of the National Academy of Sciences of the United States of America 2005, 102:3301-3306.
12. Downes S.M., Payne A.M., Kelsell R.E., Fitzke F.W., Holder G.E., Hunt D.M., et al. Autosomal dominant cone-rod dystrophy with mutations in the guanylate cyclase 2D gene encoding retinal guanylate cyclase-1. Archives of Ophthalmology 2001, 119:1667-1673.
13. Duda T., Goraczniak R.M., Surgucheva I., Rudnicka-Nawrot M., Gorczyca W.A., Palczewski K., et al. Calcium modulation of bovine photoreceptor guanylate cyclase. Biochemistry 1996, 35:8478-8482.
14. Fleischman D., Denisevich M., Raveed D., Pannbacker R.G. Association of guanylate cyclase with the axoneme of retinal rods. Biochimica et Biophysica Acta 1980, 630:176-186.
15. Friedman J.S., Chang B., Kannabiran C., Chakarova C., Singh H.P., Jalali S., et al. Premature truncation of a novel protein, RD3, exhibiting subnuclear localization is associated with retinal degeneration. American Journal of Human Genetics 2006, 79:1059-1070.
16. Hallett M.A., Delaat J.L., Arikawa K., Schlamp C.L., Kong F., Williams D.R. Distribution of guanylate cyclase within photoreceptor outer segments. Journal of Cell Science 1996, 109:1803-1812.
17. Humphries M.M., Rancourt D., Farrar G.J., Kenna P., Hazel M., Bush R.A., et al. Retinopathy induced in mice by targeted disruption of the rhodopsin gene. Nature Genetics 1997, 15:216-219.
18. Ishibashi S., Kroll K.L., Amaya E. A method for generating transgenic frog embryos. Methods in Molecular Biology 2008, 461:447-466.
19. Karan S., Frederick J.M., Baehr W. Novel functions of photoreceptor guanylate cyclases revealed by targeted deletion. Molecular and Cellular Biochemistry 2010, 334:141-155.
20. Karan S., Zhang H., Li S., Frederick J.M., Baehr W. A model for transport of membrane-associated phototransduction polypeptides in rod and cone photoreceptor inner segments. Vision Research 2008, 48:442-452.
21. Kizhatil K., Baker S.A., Arshavsky V.Y., Bennett V. Ankyrin-G promotes cyclic nucleotide-gated channel transport to rod photoreceptor sensory cilia. Science 2009, 323:1614-1617.
22. Laura R.P., Dizhoor A.M., Hurley J.B. The membrane guanylyl cyclase, retinal guanylyl cyclase-1, is activated through its intracellular domain. Journal of Biological Chemistry 1996, 271:11646-11651.
23. Laura R.P., Hurley J.B. The kinase homology domain of retinal guanylyl cyclases 1 and 2 specifies the affinity and cooperativity of interaction with guanylyl cyclase activating protein-2. Biochemistry 1998, 37:11264-11271.
24. Lavorgna G., Lestingi M., Ziviello C., Testa F., Simonelli F., Manitto M.P., et al. Identification and characterization of C1orf36, a transcript highly expressed in photoreceptor cells, and mutation analysis in retinitis pigmentosa. Biochemical and Biophysical Research Communications 2003, 308:414-421.
25. Liu X., Seno K., Nishizawa Y., Hayashi F., Yamazaki A., Matsumoto H., et al. Ultrastructural localization of retinal guanylate cyclase in human and monkey retinas. Experimental Eye Research 1994, 59:761-768.
26. Luo W., Marsh-Armstrong N., Rattner A., Nathans J. An outer segment localization signal at the C terminus of the photoreceptor-specific retinol dehydrogenase. Journal of Neuroscience 2004, 24:2623-2632.
27. Morgans C.W., Brandstatter J.H., Kellerman J., Betz H., Wassle H. A SNARE complex containing syntaxin 3 is present in ribbon synapses of the retina. Journal of Neuroscience 1996, 16:6713-6721.
28. Moritz O.L., Tam B.M., Hurd L.L., Peranen J., Deretic D., Papermaster D.S. Mutant rab8 Impairs docking and fusion of rhodopsin-bearing post-Golgi membranes and causes cell death of transgenic Xenopus rods. Molecular Biology of the Cell 2001, 12:2341-2351.
29. Moritz O.L., Tam B.M., Knox B.E., Papermaster D.S. Fluorescent photoreceptors of transgenic Xenopus laevis imaged in vivo by two microscopy techniques. Investigative Ophthalmology and Visual Science 1999, 40:3276-3280.
30. Rodriguez-Boulan E., Kreitzer G., Musch A. Organization of vesicular trafficking in epithelia. Nature Reviews Molecular Cell Biology 2005, 6:233-247.
31. Satoh A.K., O'Tousa J.E., Ozaki K., Ready D.F. Rab11 mediates post-Golgi trafficking of rhodopsin to the photosensitive apical membrane of Drosophila photoreceptors. Development 2005, 132:1487-1497.
32. Sharma N., Low S.H., Misra S., Pallavi B., Weimbs T. Apical targeting of syntaxin 3 is essential for epithelial cell polarity. Journal of Cell Biology 2006, 173:937-948.
33. Jules R.S., Smith S.B., O'Brien P.J. The localization and timing of post-translational modifications of rat rhodopsin. Experimental Eye Research 1990, 51:427-434.
34. Sung C.H., Tai A.W. Rhodopsin trafficking and its role in retinal dystrophies. International Review of Cytology 2000, 195:215-267.
35. Tam B.M., Moritz O.L., Hurd L.B., Papermaster D.S. Identification of an outer segment targeting signal in the COOH terminus of rhodopsin using transgenic Xenopus laevis. Journal of Cell Biology 2000, 151:1369-1380.
36. Tam B.M., Moritz O.L., Papermaster D.S. The C terminus of peripherin/rds participates in rod outer segment targeting and alignment of disk incisures. Molecular Biology of the Cell 2004, 15:2027-2037.
37. Tucker C.L., Woodcock S.C., Kelsell R.E., Ramamurthy V., Hunt D.M., Hurley J.B. Biochemical analysis of a dimerization domain mutation in RetGC-1 associated with dominant cone-rod dystrophy. Proceedings of the National Academy of Sciences of the United States of America 1999, 96:9039-9044.
38. Wilkie S.E., Newbold R.J., Deery E., Walker C.E., Stinton I., Ramamurthy V., et al. Functional characterization of missense mutations at codon 838 in retinal guanylate cyclase correlates with disease severity in patients with autosomal dominant cone-rod dystrophy. Human Molecular Genetics 2000, 9:3065-3073.
39. Wilson E.M., Chinkers M. Identification of sequences mediating guanylyl cyclase dimerization. Biochemistry 1995, 34:4696-4701.
40. Wu M., Gerhart J. Raising Xenopus in the laboratory. Methods in Cell Biology 1991, 36:3-18.
41. Yang R.B., Garbers D.L. Two eye guanylyl cyclases are expressed in the same photoreceptor cells and form homomers in preference to heteromers. Journal of Biological Chemistry 1997, 272:13738-13742.
42. Yang R.B., Robinson S.W., Xiong W.H., Yau K.W., Birch D.G., Garbers D.L. Disruption of a retinal guanylyl cyclase gene leads to cone-specific dystrophy and paradoxical rod behavior. Journal of Neuroscience 1999, 19:5889-5897.
43. Young R.W. The renewal of photoreceptor cell outer segments. Journal of Cell Biology 1967, 33:61-72.