Intraflagellar Transport Particles Participate Directly in Cilium-Generated Signaling in Chlamydomonas

Cell

Volumn 125, Issue 3, 2006, Pages 549-562

  Wang, Qian ^a   Pan, Junmin ^a   Snell, William J ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC GMP DEPENDENT PROTEIN KINASE; PROTEIN TYROSINE KINASE;

ADHESION; ARTICLE; CELL TRANSPORT; CHLAMYDOMONAS; ENZYME ACTIVATION; EUKARYOTIC FLAGELLUM; FERTILIZATION; FLAGELLUM; GREEN ALGA; INTRAFLAGELLAR TRANSPORT; MODEL; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

CHLAMYDOMONAS; CHLOROPHYTA; EUKARYOTA;

EID: 33646152956     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2006.02.044     Document Type: Article

References (76)

1. Adair W.S., Hwang C., and Goodenough U.W. Identification and visualization of the sexual agglutinin from the mating-type plus flagellar membrane of Chlamydomonas. Cell 33 (1983) 183-193
2. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., and Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25 (1997) 3389-3402
3. Ann K.S., and Nelson D.L. Protein substrates for cGMP-dependent protein phosphorylation in cilia of wild type and atalanta mutants of Paramecium. Cell Motil. Cytoskeleton 30 (1995) 252-260
4. Asamizu E., Nakamura Y., Sato S., Fukuzawa H., and Tabata S. A large scale structural analysis of cDNAs in a unicellular green alga, Chlamydomonas reinhardtii. I. Generation of 3433 non-redundant expressed sequence tags. DNA Res. 6 (1999) 369-373
5. Avidor-Reiss T., Maer A.M., Koundakjian E., Polyanovsky A., Keil T., Subramaniam S., and Zuker C.S. Decoding cilia function: defining specialized genes required for compartmentalized cilia biogenesis. Cell 117 (2004) 527-539
6. Baker D.A., and Deng W. Cyclic GMP-dependent protein kinases in protozoa. Front. Biosci. 10 (2005) 1229-1238
7. Bastin P., MacRae T.H., Francis S.B., Matthews K.R., and Gull K. Flagellar morphogenesis: protein targeting and assembly in the paraflagellar rod of Trypanosomes. Mol. Cell. Biol. 19 (1999) 8191-8200
8. Bloodgood R.A. Protein targeting to flagella of trypanosomatid protozoa. Cell Biol. Int. 24 (2000) 857-862
9. Boletta A., and Germino G.G. Role of polycystins in renal tubulogenesis. Trends Cell Biol. 13 (2003) 484-492
10. Christensen S.T., Voss J.W., Teilmann S.C., and Lambert I.H. High expression of the taurine transporter TauT in primary cilia of NIH3T3 fibroblasts. Cell Biol. Int. 29 (2005) 347-351
11. Cole D.G., Diener D.R., Himelblau A.L., Beech P.L., Fuster J.C., and Rosenbaum J.L. Chlamydomonas kinesin-II-dependent intraflagellar transport (IFT): IFT particles contain proteins required for ciliary assembly in Caenorhabditis elegans sensory neurons. J. Cell Biol. 141 (1998) 993-1008
12. Corbit K.C., Aanstad P., Singla V., Norman A.R., Stainier D.Y., and Reiter J.F. Vertebrate Smoothened functions at the primary cilium. Nature 437 (2005) 1018-1021
13. Deng W., Parbhu-Patel A., Meyer D.J., and Baker D.A. The role of two novel regulatory sites in the activation of the cGMP-dependent protein kinase from Plasmodium falciparum. Biochem. J. 374 (2003) 559-565
14. Donald R.G., and Liberator P.A. Molecular characterization of a coccidian parasite cGMP dependent protein kinase. Mol. Biochem. Parasitol. 120 (2002) 165-175
15. Fujiwara M., Sengupta P., and McIntire S.L. Regulation of body size and behavioral state of C. elegans by sensory perception and the EGL-4 cGMP-dependent protein kinase. Neuron 36 (2002) 1091-1102
16. Gasteiger E., Gattiker A., Hoogland C., Ivanyi I., Appel R.D., and Bairoch A. ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res. 31 (2003) 3784-3788
17. Gertsberg I., Hellman V., Fainshtein M., Weil S., Silberberg S.D., Danilenko M., and Priel Z. Intracellular Ca2+ regulates the phosphorylation and the dephosphorylation of ciliary proteins via the NO pathway. J. Gen. Physiol. 124 (2004) 527-540
18. Goodenough U.W., and Weiss R.L. Gametic differentiation in Chlamydomonas reinhardtii. III. Cell wall lysis and microfilament-associated mating structure activation in wild-type and mutant strains. J. Cell Biol. 67 (1975) 623-637
19. Gurnett A.M., Liberator P.A., Dulski P.M., Salowe S.P., Donald R.G., Anderson J.W., Wiltsie J., Diaz C.A., Harris G., Chang B., et al. Purification and molecular characterization of cGMP-dependent protein kinase from Apicomplexan parasites. A novel chemotherapeutic target. J. Biol. Chem. 277 (2002) 15913-15922
20. Handel M., Schulz S., Stanarius A., Schreff M., Erdtmann-Vourliotis M., Schmidt H., Wolf G., and Hollt V. Selective targeting of somatostatin receptor 3 to neuronal cilia. Neuroscience 89 (1999) 909-926
21. Harris P.C., and Rossetti S. Molecular genetics of autosomal recessive polycystic kidney disease. Mol. Genet. Metab. 81 (2004) 75-85
22. Huang K., Kunkel T., and Beck C.F. Localization of the blue-light receptor phototropin to the flagella of the green alga Chlamydomonas reinhardtii. Mol. Biol. Cell 15 (2004) 3605-3614
23. Huangfu D., and Anderson K.V. Cilia and Hedgehog responsiveness in the mouse. Proc. Natl. Acad. Sci. USA 102 (2005) 11325-11330
24. Huangfu D., Liu A., Rakeman A.S., Murcia N.S., Niswander L., and Anderson K.V. Hedgehog signalling in the mouse requires intraflagellar transport proteins. Nature 426 (2003) 83-87
25. Iomini C., Babaev-Khaimov V., Sassaroli M., and Piperno G. Protein particles in Chlamydomonas flagella undergo a transport cycle consisting of four phases. J. Cell Biol. 153 (2001) 13-24
26. Kindle K.L., Schnell R.A., Fernandez E., and Lefebvre P.A. Stable nuclear transformation of Chlamydomonas using the Chlamydomonas gene for nitrate reductase. J. Cell Biol. 109 (1989) 2589-2601
27. Koutoulis A., Pazour G.J., Wilkerson C.G., Inaba K., Sheng H., Takada S., and Witman G.B. The Chlamydomonas reinhardtii ODA3 gene encodes a protein of the outer dynein arm docking complex. J. Cell Biol. 137 (1997) 1069-1080
28. Kozminski K.G., Beech P.L., and Rosenbaum J.L. The Chlamydomonas kinesin-like protein FLA10 is involved in motility associated with the flagellar membrane. J. Cell Biol. 131 (1995) 1517-1527
29. Li J.B., Gerdes J.M., Haycraft C.J., Fan Y., Teslovich T.M., May-Simera H., Li H., Blacque O.E., Li L., Leitch C.C., et al. Comparative genomics identifies a flagellar and basal body proteome that includes the BBS5 human disease gene. Cell 117 (2004) 541-552
30. Lin F., Hiesberger T., Cordes K., Sinclair A.M., Goldstein L.S., Somlo S., and Igarashi P. Kidney-specific inactivation of the KIF3A subunit of kinesin-II inhibits renal ciliogenesis and produces polycystic kidney disease. Proc. Natl. Acad. Sci. USA 100 (2003) 5286-5291
31. Liu A., Wang B., and Niswander L.A. Mouse intraflagellar transport proteins regulate both the activator and repressor functions of Gli transcription factors. Development 132 (2005) 3103-3111
32. Lohmann S.M., Vaandrager A.B., Smolenski A., Walter U., and De Jonge H.R. Distinct and specific functions of cGMP-dependent protein kinases. Trends Biochem. Sci. 22 (1997) 307-312
33. Lux III F.G., and Dutcher S.K. Genetic interactions at the FLA10 locus: suppressors and synthetic phenotypes that affect the cell cycle and flagellar function in Chlamydomonas reinhardtii. Genetics 128 (1991) 549-561
34. Marszalek J.R., Liu X., Roberts E.A., Chui D., Marth J.D., Williams D.S., and Goldstein L.S. Genetic evidence for selective transport of opsin and arrestin by kinesin-II in mammalian photoreceptors. Cell 102 (2000) 175-187
35. McGrath J., Somlo S., Makova S., Tian X., and Brueckner M. Two populations of node monocilia initiate left-right asymmetry in the mouse. Cell 114 (2003) 61-73
36. Mendez A., Lem J., Simon M., and Chen J. Light-dependent translocation of arrestin in the absence of rhodopsin phosphorylation and transducin signaling. J. Neurosci. 23 (2003) 3124-3129
37. Mesland D.A., Hoffman J.L., Caligor E., and Goodenough U.W. Flagellar tip activation stimulated by membrane adhesions in Chlamydomonas gametes. J. Cell Biol. 84 (1980) 599-617
38. Miranti C.K., and Brugge J.S. Sensing the environment: a historical perspective on integrin signal transduction. Nat. Cell Biol. 4 (2002) E83-E90
39. Nauli S.M., and Zhou J. Polycystins and mechanosensation in renal and nodal cilia. Bioessays 26 (2004) 844-856
40. Nonaka S., Tanaka Y., Okada Y., Takeda S., Harada A., Kanai Y., Kido M., and Hirokawa N. Randomization of left-right asymmetry due to loss of nodal cilia generating leftward flow of extraembryonic fluid in mice lacking KIF3B motor protein. Cell 95 (1998) 829-837
41. Pan J., and Snell W.J. Signal transduction during fertilization in the unicellular green alga, Chlamydomonas. Curr. Opin. Microbiol. 3 (2000) 596-602
42. Pan J., and Snell W.J. Kinesin-II is required for flagellar sensory transduction during fertilization in Chlamydomonas. Mol. Biol. Cell 13 (2002) 1417-1426
43. Pan J., and Snell W.J. Kinesin II and regulated intraflagellar transport of Chlamydomonas aurora protein kinase. J. Cell Sci. 116 (2003) 2179-2186
44. Pan J., Wang Q., and Snell W.J. An aurora kinase is essential for flagellar disassembly in Chlamydomonas. Dev. Cell 6 (2004) 445-451
45. Pan J., Wang Q., and Snell W.J. Cilium-generated signaling and cilia-related disorders. Lab. Invest. 85 (2005) 452-463
46. Pasquale S.M., and Goodenough U.W. Cyclic AMP functions as a primary sexual signal in gametes of Chlamydomonas reinhardtii. J. Cell Biol. 105 (1987) 2279-2292
47. Pazour G.J., and Witman G.B. The vertebrate primary cilium is a sensory organelle. Curr. Opin. Cell Biol. 15 (2003) 105-110
48. Pazour G.J., Dickert B.L., Vucica Y., Seeley E.S., Rosenbaum J.L., Witman G.B., and Cole D.G. Chlamydomonas IFT88 and its mouse homologue, polycystic kidney disease gene tg737, are required for assembly of cilia and flagella. J. Cell Biol. 151 (2000) 709-718
49. Pazour G.J., Agrin N., Leszyk J., and Witman G.B. Proteomic analysis of a eukaryotic cilium. J. Cell Biol. 170 (2005) 103-113
50. Pedersen L.B., Geimer S., Sloboda R.D., and Rosenbaum J.L. The Microtubule plus end-tracking protein EB1 is localized to the flagellar tip and basal bodies in Chlamydomonas reinhardtii. Curr. Biol. 13 (2003) 1969-1974
51. Piperno G., and Mead K. Transport of a novel complex in the cytoplasmic matrix of Chlamydomonas flagella. Proc. Natl. Acad. Sci. USA 94 (1997) 4457-4462
52. Piperno G., Mead K., and Henderson S. Inner dynein arms but not outer dynein arms require the activity of kinesin homologue protein KHP1(FLA10) to reach the distal part of flagella in Chlamydomonas. J. Cell Biol. 133 (1996) 371-379
53. Poole C.A., Flint M.H., and Beaumont B.W. Analysis of the morphology and function of primary cilia in connective tissues: a cellular cybernetic probe?. Cell Motil. 5 (1985) 175-193
54. Praetorius H.A., Praetorius J., Nielsen S., Frokiaer J., and Spring K.R. Beta1-integrins in the primary cilium of MDCK cells potentiate fibronectin-induced Ca2+ signaling. Am. J. Physiol. Renal Physiol. 287 (2004) F969-F978
55. Qin H., Diener D.R., Geimer S., Cole D.G., and Rosenbaum J.L. Intraflagellar transport (IFT) cargo: IFT transports flagellar precursors to the tip and turnover products to the cell body. J. Cell Biol. 164 (2004) 255-266
56. Qin H., Burnette D.T., Bae Y.-K., Forscher P., Barr M.M., and Rosenbaum J.L. Intraflagellar transport is required for the vectorial movement of TRPV channels in the ciliary membrane. Curr. Biol. 15 (2005) 1695-1699
57. Quarmby L.M., and Mahjoub M.R. Caught Nek-ing: cilia and centrioles. J. Cell Sci. 118 (2005) 5161-5169
58. Rosenbaum J.L., and Witman G.B. Intraflagellar transport. Nat. Rev. Mol. Cell Biol. 3 (2002) 813-825
59. Schneider L., Clement C.A., Teilmann S.C., Pazour G.J., Hoffmann E.K., Satir P., and Christensen S.T. PDGFRalphaalpha signaling is regulated through the primary cilium in fibroblasts. Curr. Biol. 15 (2005) 1861-1866
60. Scholey J.M. Intraflagellar transport. Annu. Rev. Cell Dev. Biol. 19 (2003) 423-443
61. Shabb J.B., Buzzeo B.D., Ng L., and Corbin J.D. Mutating protein kinase cAMP-binding sites into cGMP-binding sites. Mechanism of cGMP selectivity. J. Biol. Chem. 266 (1991) 24320-24326
62. Sineshchekov O.A., Jung K.H., and Spudich J.L. Two rhodopsins mediate phototaxis to low- and high-intensity light in Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA 99 (2002) 8689-8694
63. Snell W.J., Pan J., and Wang Q. Cilia and flagella revealed: from flagellar assembly in Chlamydomonas to human obesity disorders. Cell 117 (2004) 693-697
64. Snow J.J., Ou G., Gunnarson A.L., Walker M.R., Zhou H.M., Brust-Mascher I., and Scholey J.M. Two anterograde intraflagellar transport motors cooperate to build sensory cilia on C. elegans neurons. Nat. Cell Biol. 6 (2004) 1109-1113
65. Tanaka Y., Okada Y., and Hirokawa N. FGF-induced vesicular release of Sonic hedgehog and retinoic acid in leftward nodal flow is critical for left-right determination. Nature 435 (2005) 172-177
66. Teilmann S.C., and Christensen S.T. Localization of the angiopoietin receptors Tie-1 and Tie-2 on the primary cilia in the female reproductive organs. Cell Biol. Int. 29 (2005) 340-346
67. Vaandrager A.B., Smolenski A., Tilly B.C., Houtsmuller A.B., Ehlert E.M., Bot A.G., Edixhoven M., Boomaars W.E., Lohmann S.M., and de Jonge H.R. Membrane targeting of cGMP-dependent protein kinase is required for cystic fibrosis transmembrane conductance regulator Cl- channel activation. Proc. Natl. Acad. Sci. USA 95 (1998) 1466-1471
68. Vondriska T.M., Pass J.M., and Ping P. Scaffold proteins and assembly of multiprotein signaling complexes. J. Mol. Cell. Cardiol. 37 (2004) 391-397
69. Wang Q., and Snell W.J. Flagellar adhesion between mating type plus and mating type minus gametes activates a flagellar protein-tyrosine kinase during fertilization in Chlamydomonas. J. Biol. Chem. 278 (2003) 32936-32942
70. Werlen G., and Palmer E. The T-cell receptor signalosome: a dynamic structure with expanding complexity. Curr. Opin. Immunol. 14 (2002) 299-305
71. White M.A., and Anderson R.G. Signaling networks in living cells. Annu. Rev. Pharmacol. Toxicol. 45 (2005) 587-603
72. Wiersma H.I., Galuska S.E., Tomley F.M., Sibley L.D., Liberator P.A., and Donald R.G. A role for coccidian cGMP-dependent protein kinase in motility and invasion. Int. J. Parasitol. 34 (2004) 369-380
73. Witman G.B., Carlson K., Berliner J., and Rosenbaum J.L. Chlamydomonas flagella. I. Isolation and electrophoretic analysis of microtubules, matrix, membranes, and mastigonemes. J. Cell Biol. 54 (1972) 507-539
74. Yasuda J., Whitmarsh A.J., Cavanagh J., Sharma M., and Davis R.J. The JIP group of mitogen-activated protein kinase scaffold proteins. Mol. Cell. Biol. 19 (1999) 7245-7254
75. Zhang Y., and Snell W.J. Flagellar adhesion-dependent regulation of Chlamydomonas adenylyl cyclase in vitro: a possible role for protein kinases in sexual signaling. J. Cell Biol. 125 (1994) 617-624
76. Zhao Y., Zhang W., and White M.A. Capillary high-performance liquid chromatography/mass spectrometric analysis of proteins from affinity-purified plasma membrane. Anal. Chem. 75 (2003) 3751-3757