The intraflagellar transport protein, IFT88, is essential for vertebrate photoreceptor assembly and maintenance

doi:10.1083/jcb.200107108

Published online 26 March 2002. doi:10.1083/jcb.200107108

This Article

	Full Text
	Full Text (PDF, 668K)
	PPT slides of all figures
	Alert me when this article is cited
	Citation Map

Services

	Email this article
	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new content in the JCB
	Download to citation manager

Citing Articles

	Citing Articles via HighWire
	Citing Articles via CrossRef
	Citing Articles via Google Scholar

Google Scholar

	Articles by Pazour, G. J.
	Articles by Besharse, J. C.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Pazour, G. J.
	Articles by Besharse, J. C.


Related Collections

	Related Article

Social Bookmarking

	What's this?

© The Rockefeller University Press, 0021-9525/2002/4/103 $5.00
The Journal of Cell Biology, Volume 157, Number 1, April 1, 2002 103-114

Article

The intraflagellar transport protein, IFT88, is essential for vertebrate photoreceptor assembly and maintenance

Gregory J. Pazour¹, Sheila A. Baker⁴, James A. Deane², Douglas G. Cole³, Bethany L. Dickert¹, Joel L. Rosenbaum², George B. Witman¹ and Joseph C. Besharse⁴

¹ Department of Cell Biology, University of Massachusetts Medical School, Worcester, MA 01655
² Department of Molecular, Cellular, and Developmental Biology, Yale University, New Haven, CT 06520
³ Department of Microbiology, Molecular Biology, and Biochemistry, University of Idaho, Moscow, ID 83844
⁴ Department of Cell Biology, Neurobiology, and Anatomy, Medical College of Wisconsin, Milwaukee, WI 53226

Address correspondence to Dr. Joseph C. Besharse, Department of Cell Biology, Neurobiology, and Anatomy, Medical College of Wisconsin, 8701 Watertown Plank Rd., Milwaukee, WI 53226. Tel.: (414) 456-8260. Fax: (414) 456-6517. E-mail: jbeshars{at}mcw.edu

Approximately 10% of the photoreceptor outer segment (OS) isturned over each day, requiring large amounts of lipid and proteinto be moved from the inner segment to the OS. Defects in intraphotoreceptortransport can lead to retinal degeneration and blindness. Thetransport mechanisms are unknown, but because the OS is a modifiedcilium, intraflagellar transport (IFT) is a candidate mechanism.IFT involves movement of large protein complexes along ciliarymicrotubules and is required for assembly and maintenance ofcilia. We show that IFT particle proteins are localized to photoreceptorconnecting cilia. We further find that mice with a mutationin the IFT particle protein gene, Tg737/IFT88, have abnormalOS development and retinal degeneration. Thus, IFT is importantfor assembly and maintenance of the vertebrate OS.

Key Words: rods and cones; retinitis pigmentosa; blindness; primary cilia; orpk

Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Facebook Add to Reddit Reddit Add to Technorati Technorati Twitter What's this?

Related Article

Seeing through the cilium: Nicole LeBrasseur
J. Cell Biol. 2002 157: 10-11. [Full Text] [PDF]

This article has been cited by other articles:

Avasthi, P., Watt, C. B., Williams, D. S., Le, Y. Z., Li, S., Chen, C.-K., Marc, R. E., Frederick, J. M., Baehr, W. (2009). Trafficking of Membrane Proteins to Cone But Not Rod Outer Segments Is Dependent on Heterotrimeric Kinesin-II. J. Neurosci. 29: 14287-14298 [Abstract] [Full Text]
Krock, B. L., Mills-Henry, I., Perkins, B. D. (2009). Retrograde Intraflagellar Transport by Cytoplasmic Dynein-2 Is Required for Outer Segment Extension in Vertebrate Photoreceptors but Not Arrestin Translocation. IOVS 50: 5463-5471 [Abstract] [Full Text]
Pigino, G., Geimer, S., Lanzavecchia, S., Paccagnini, E., Cantele, F., Diener, D. R., Rosenbaum, J. L., Lupetti, P. (2009). Electron-tomographic analysis of intraflagellar transport particle trains in situ. JCB 187: 135-148 [Abstract] [Full Text]
Tammachote, R., Hommerding, C. J., Sinders, R. M., Miller, C. A., Czarnecki, P. G., Leightner, A. C., Salisbury, J. L., Ward, C. J., Torres, V. E., Gattone, V. H. II, Harris, P. C. (2009). Ciliary and centrosomal defects associated with mutation and depletion of the Meckel syndrome genes MKS1 and MKS3. Hum Mol Genet 18: 3311-3323 [Abstract] [Full Text]
Yamashita, T., Liu, J., Gao, J., LeNoue, S., Wang, C., Kaminoh, J., Bowne, S. J., Sullivan, L. S., Daiger, S. P., Zhang, K., Fitzgerald, M. E. C., Kefalov, V. J., Zuo, J. (2009). Essential and Synergistic Roles of RP1 and RP1L1 in Rod Photoreceptor Axoneme and Retinitis Pigmentosa. J. Neurosci. 29: 9748-9760 [Abstract] [Full Text]
Jiang, S.-T., Chiou, Y.-Y., Wang, E., Chien, Y.-L., Ho, H.-H., Tsai, F.-J., Lin, C.-Y., Tsai, S.-P., Li, H. (2009). Essential role of nephrocystin in photoreceptor intraflagellar transport in mouse. Hum Mol Genet 18: 1566-1577 [Abstract] [Full Text]
van Wijk, E., Kersten, F. F.J., Kartono, A., Mans, D. A., Brandwijk, K., Letteboer, S. J.F., Peters, T. A., Marker, T., Yan, X., Cremers, C. W.R.J., Cremers, F. P.M., Wolfrum, U., Roepman, R., Kremer, H. (2009). Usher syndrome and Leber congenital amaurosis are molecularly linked via a novel isoform of the centrosomal ninein-like protein. Hum Mol Genet 18: 51-64 [Abstract] [Full Text]
Overgaard, C. E., Sanzone, K. M., Spiczka, K. S., Sheff, D. R., Sandra, A., Yeaman, C. (2009). Deciliation Is Associated with Dramatic Remodeling of Epithelial Cell Junctions and Surface Domains. Mol. Biol. Cell 20: 102-113 [Abstract] [Full Text]
Willaredt, M. A., Hasenpusch-Theil, K., Gardner, H. A. R., Kitanovic, I., Hirschfeld-Warneken, V. C., Gojak, C. P., Gorgas, K., Bradford, C. L., Spatz, J., Wolfl, S., Theil, T., Tucker, K. L. (2008). A Crucial Role for Primary Cilia in Cortical Morphogenesis. J. Neurosci. 28: 12887-12900 [Abstract] [Full Text]
Ahmed, N. T., Gao, C., Lucker, B. F., Cole, D. G., Mitchell, D. R. (2008). ODA16 aids axonemal outer row dynein assembly through an interaction with the intraflagellar transport machinery. JCB 183: 313-322 [Abstract] [Full Text]
Brunner, S., Colman, D., Travis, A. J., Luhmann, U. F.O., Shi, W., Feil, S., Imsand, C., Nelson, J., Grimm, C., Rulicke, T., Fundele, R., Neidhardt, J., Berger, W. (2008). Overexpression of RPGR Leads to Male Infertility in Mice Due to Defects in Flagellar Assembly. Biol. Reprod. 79: 608-617 [Abstract] [Full Text]
Hoeng, J. C., Dawson, S. C., House, S. A., Sagolla, M. S., Pham, J. K., Mancuso, J. J., Lowe, J., Cande, W. Z. (2008). High-Resolution Crystal Structure and In Vivo Function of a Kinesin-2 Homologue in Giardia intestinalis. Mol. Biol. Cell 19: 3124-3137 [Abstract] [Full Text]
Krock, B. L., Perkins, B. D. (2008). The intraflagellar transport protein IFT57 is required for cilia maintenance and regulates IFT-particle-kinesin-II dissociation in vertebrate photoreceptors. J. Cell Sci. 121: 1907-1915 [Abstract] [Full Text]
Tsao, C.-C., Gorovsky, M. A. (2008). Different Effects of Tetrahymena IFT172 Domains on Anterograde and Retrograde Intraflagellar Transport. Mol. Biol. Cell 19: 1450-1461 [Abstract] [Full Text]
Jauregui, A. R., Nguyen, K. C.Q., Hall, D. H., Barr, M. M. (2008). The Caenorhabditis elegans nephrocystins act as global modifiers of cilium structure. JCB 180: 973-988 [Abstract] [Full Text]
McClintock, T. S., Glasser, C. E., Bose, S. C., Bergman, D. A. (2008). Tissue expression patterns identify mouse cilia genes. Physiol. Genomics 32: 198-206 [Abstract] [Full Text]
Tan, P. L., Barr, T., Inglis, P. N., Mitsuma, N., Huang, S. M., Garcia-Gonzalez, M. A., Bradley, B. A., Coforio, S., Albrecht, P. J., Watnick, T., Germino, G. G., Beales, P. L., Caterina, M. J., Leroux, M. R., Rice, F. L., Katsanis, N. (2007). From the Cover: Loss of Bardet Biedl syndrome proteins causes defects in peripheral sensory innervation and function. Proc. Natl. Acad. Sci. USA 104: 17524-17529 [Abstract] [Full Text]
Liu, Q., Tan, G., Levenkova, N., Li, T., Pugh, E. N. Jr., Rux, J. J., Speicher, D. W., Pierce, E. A. (2007). The Proteome of the Mouse Photoreceptor Sensory Cilium Complex. Mol. Cell. Proteomics 6: 1299-1317 [Abstract] [Full Text]
Menotti-Raymond, M., David, V. A., Schaffer, A. A., Stephens, R., Wells, D., Kumar-Singh, R., O'Brien, S. J., Narfstrom, K. (2007). Mutation in CEP290 Discovered for Cat Model of Human Retinal Degeneration. J Hered 0: esm019v1- [Abstract] [Full Text]
Krock, B. L., Bilotta, J., Perkins, B. D. (2007). Noncell-autonomous photoreceptor degeneration in a zebrafish model of choroideremia. Proc. Natl. Acad. Sci. USA 104: 4600-4605 [Abstract] [Full Text]
Duriez, B., Duquesnoy, P., Escudier, E., Bridoux, A.-M., Escalier, D., Rayet, I., Marcos, E., Vojtek, A.-M., Bercher, J.-F., Amselem, S. (2007). A common variant in combination with a nonsense mutation in a member of the thioredoxin family causes primary ciliary dyskinesia. Proc. Natl. Acad. Sci. USA 104: 3336-3341 [Abstract] [Full Text]
Hou, Y., Qin, H., Follit, J. A., Pazour, G. J., Rosenbaum, J. L., Witman, G. B. (2007). Functional analysis of an individual IFT protein: IFT46 is required for transport of outer dynein arms into flagella. JCB 176: 653-665 [Abstract] [Full Text]
Bisgrove, B. W., Yost, H. J. (2006). The roles of cilia in developmental disorders and disease. Development 133: 4131-4143 [Abstract] [Full Text]
Fliegauf, M., Horvath, J., von Schnakenburg, C., Olbrich, H., Muller, D., Thumfart, J., Schermer, B., Pazour, G. J., Neumann, H. P.H., Zentgraf, H., Benzing, T., Omran, H. (2006). Nephrocystin Specifically Localizes to the Transition Zone of Renal and Respiratory Cilia and Photoreceptor Connecting Cilia. J. Am. Soc. Nephrol. 17: 2424-2433 [Abstract] [Full Text]
Follit, J. A., Tuft, R. A., Fogarty, K. E., Pazour, G. J. (2006). The Intraflagellar Transport Protein IFT20 Is Associated with the Golgi Complex and Is Required for Cilia Assembly. Mol. Biol. Cell 17: 3781-3792 [Abstract] [Full Text]
Chang, B., Khanna, H., Hawes, N., Jimeno, D., He, S., Lillo, C., Parapuram, S. K., Cheng, H., Scott, A., Hurd, R. E., Sayer, J. A., Otto, E. A., Attanasio, M., O'Toole, J. F., Jin, G., Shou, C., Hildebrandt, F., Williams, D. S., Heckenlively, J. R., Swaroop, A. (2006). In-frame deletion in a novel centrosomal/ciliary protein CEP290/NPHP6 perturbs its interaction with RPGR and results in early-onset retinal degeneration in the rd16 mouse. Hum Mol Genet 15: 1847-1857 [Abstract] [Full Text]
Schrick, J. J., Vogel, P., Abuin, A., Hampton, B., Rice, D. S. (2006). ADP-Ribosylation Factor-Like 3 Is Involved in Kidney and Photoreceptor Development. Am. J. Pathol. 168: 1288-1298 [Abstract] [Full Text]
Moore, A, Escudier, E, Roger, G, Tamalet, A, Pelosse, B, Marlin, S, Clement, A, Geremek, M, Delaisi, B, Bridoux, A-M, Coste, A, Witt, M, Duriez, B, Amselem, S (2006). RPGR is mutated in patients with a complex X linked phenotype combining primary ciliary dyskinesia and retinitis pigmentosa. J. Med. Genet. 43: 326-333 [Abstract] [Full Text]
Davenport, J. R., Yoder, B. K. (2005). An incredible decade for the primary cilium: a look at a once-forgotten organelle. Am. J. Physiol. Renal Physiol. 289: F1159-F1169 [Abstract] [Full Text]
Khanna, H., Hurd, T. W., Lillo, C., Shu, X., Parapuram, S. K., He, S., Akimoto, M., Wright, A. F., Margolis, B., Williams, D. S., Swaroop, A. (2005). RPGR-ORF15, Which Is Mutated in Retinitis Pigmentosa, Associates with SMC1, SMC3, and Microtubule Transport Proteins. J. Biol. Chem. 280: 33580-33587 [Abstract] [Full Text]
Gross, J. M., Perkins, B. D., Amsterdam, A., Egana, A., Darland, T., Matsui, J. I., Sciascia, S., Hopkins, N., Dowling, J. E. (2005). Identification of Zebrafish Insertional Mutants With Defects in Visual System Development and Function. Genetics 170: 245-261 [Abstract] [Full Text]
Nair, K. S., Mendez, A., Blumer, J. B., Rosenzweig, D. H., Slepak, V. Z. (2005). The Presence of a Leu-Gly-Asn Repeat-Enriched Protein (LGN), a Putative Binding Partner of Transducin, in ROD Photoreceptors. IOVS 46: 383-389 [Abstract] [Full Text]
Pazour, G. J. (2004). Intraflagellar Transport and Cilia-Dependent Renal Disease: The Ciliary Hypothesis of Polycystic Kidney Disease. J. Am. Soc. Nephrol. 15: 2528-2536 [Abstract] [Full Text]
Jurczyk, A., Gromley, A., Redick, S., Agustin, J. S., Witman, G., Pazour, G. J., Peters, D. J.M., Doxsey, S. (2004). Pericentrin forms a complex with intraflagellar transport proteins and polycystin-2 and is required for primary cilia assembly. JCB 166: 637-643 [Abstract] [Full Text]
Sun, Z., Amsterdam, A., Pazour, G. J., Cole, D. G., Miller, M. S., Hopkins, N. (2004). A genetic screen in zebrafish identifies cilia genes as a principal cause of cystic kidney. Development 131: 4085-4093 [Abstract] [Full Text]
Blacque, O. E., Reardon, M. J., Li, C., McCarthy, J., Mahjoub, M. R., Ansley, S. J., Badano, J. L., Mah, A. K., Beales, P. L., Davidson, W. S., Johnsen, R. C., Audeh, M., Plasterk, R. H.A., Baillie, D. L., Katsanis, N., Quarmby, L. M., Wicks, S. R., Leroux, M. R. (2004). Loss of C. elegans BBS-7 and BBS-8 protein function results in cilia defects and compromised intraflagellar transport. Genes Dev. 18: 1630-1642 [Abstract] [Full Text]
Peet, J. A., Bragin, A., Calvert, P. D., Nikonov, S. S., Mani, S., Zhao, X., Besharse, J. C., Pierce, E. A., Knox, B. E., Pugh, E. N. Jr (2004). Quantification of the cytoplasmic spaces of living cells with EGFP reveals arrestin-EGFP to be in disequilibrium in dark adapted rod photoreceptors. J. Cell Sci. 117: 3049-3059 [Abstract] [Full Text]
Luo, W., Marsh-Armstrong, N., Rattner, A., Nathans, J. (2004). An Outer Segment Localization Signal at the C Terminus of the Photoreceptor-Specific Retinol Dehydrogenase. J. Neurosci. 24: 2623-2632 [Abstract] [Full Text]
Liu, Q., Lyubarsky, A., Skalet, J. H., Pugh, E. N. Jr, Pierce, E. A. (2003). RP1 Is Required for the Correct Stacking of Outer Segment Discs. IOVS 44: 4171-4183 [Abstract] [Full Text]
Baker, S. A., Freeman, K., Luby-Phelps, K., Pazour, G. J., Besharse, J. C. (2003). IFT20 Links Kinesin II with a Mammalian Intraflagellar Transport Complex That Is Conserved in Motile Flagella and Sensory Cilia. J. Biol. Chem. 278: 34211-34218 [Abstract] [Full Text]
Lin-Jones, J., Parker, E., Wu, M., Knox, B. E., Burnside, B. (2003). Disruption of Kinesin II Function Using a Dominant Negative-Acting Transgene in Xenopus laevis Rods Results in Photoreceptor Degeneration. IOVS 44: 3614-3621 [Abstract] [Full Text]
Brown, J. M., Fine, N. A., Pandiyan, G., Thazhath, R., Gaertig, J. (2003). Hypoxia Regulates Assembly of Cilia in Suppressors of Tetrahymena Lacking an Intraflagellar Transport Subunit Gene. Mol. Biol. Cell 14: 3192-3207 [Abstract] [Full Text]
Gibbs, D., Kitamoto, J., Williams, D. S. (2003). Abnormal phagocytosis by retinal pigmented epithelium that lacks myosin VIIa, the Usher syndrome 1B protein. Proc. Natl. Acad. Sci. USA 100: 6481-6486 [Abstract] [Full Text]
Schafer, J. C., Haycraft, C. J., Thomas, J. H., Yoder, B. K., Swoboda, P. (2003). XBX-1 Encodes a Dynein Light Intermediate Chain Required for Retrograde Intraflagellar Transport and Cilia Assembly in Caenorhabditis elegans. Mol. Biol. Cell 14: 2057-2070 [Abstract] [Full Text]
Ibanez-Tallon, I., Heintz, N., Omran, H. (2003). To beat or not to beat: roles of cilia in development and disease. Hum Mol Genet 12: R27-35 [Abstract] [Full Text]
Luo, Y., Vassilev, P. M., Li, X., Kawanabe, Y., Zhou, J. (2003). Native Polycystin 2 Functions as a Plasma Membrane Ca2+-Permeable Cation Channel in Renal Epithelia. Mol. Cell. Biol. 23: 2600-2607 [Abstract] [Full Text]
Hill, K. L. (2003). Biology and Mechanism of Trypanosome Cell Motility. Eukaryot Cell 2: 200-208 [Full Text]
Zhao, Y., Hong, D.-H., Pawlyk, B., Yue, G., Adamian, M., Grynberg, M., Godzik, A., Li, T. (2003). The retinitis pigmentosa GTPase regulator (RPGR)- interacting protein: Subserving RPGR function and participating in disk morphogenesis. Proc. Natl. Acad. Sci. USA 100: 3965-3970 [Abstract] [Full Text]
Dubruille, R., Laurencon, A., Vandaele, C., Shishido, E., Coulon-Bublex, M., Swoboda, P., Couble, P., Kernan, M., Durand, B. (2002). Drosophila Regulatory factor X is necessary for ciliated sensory neuron differentiation. Development 129: 5487-5498 [Abstract] [Full Text]