Induction of ran GTP drives ciliogenesis

Molecular Biology of the Cell

Volumn 22, Issue 23, 2011, Pages 4539-4548

  Fan, Shuling ^a   Whiteman, Eileen L ^a   Hurd, Toby W ^a   McIntyre, Jeremy C ^a   Dishinger, John F ^a   Liu, Chia Jen ^a   Martens, Jeffrey R ^a   Verhey, Kristen J ^a   Sajjan, Uma ^a   Margolis, Ben ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

KARYOPHERIN; PROTEIN; PROTEIN KIF17; RAN PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BIOGENESIS; CONTROLLED STUDY; EUKARYOTIC FLAGELLUM; KINETOSOME; MUCOCILIARY TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT;

ANIMALS; CELL DIFFERENTIATION; CELL LINE; CENTROSOME; CILIA; DOGS; DOWN-REGULATION; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; HUMANS; KINESIN; MICE; NUCLEAR PROTEINS; RAN GTP-BINDING PROTEIN;

EID: 82655181324     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E11-03-0267     Document Type: Article

References (66)

1. Andersen JS, Wilkinson CJ, Mayor T, Mortensen P, Nigg EA, Mann M (2003). Proteomic characterization of the human centrosome by protein correlation profiling. Nature 426, 570-574. (Pubitemid 37522644)
2. Avidor-Reiss T, Maer AM, Koundakjian E, Polyanovsky A, Keil T, Subramaniam S, Zuker CS (2004). Decoding cilia function: defining specialized genes required for compartmentalized cilia biogenesis. Cell 117, 527-539. (Pubitemid 38610237)
3. Babbey CM, Bacallao RL, Dunn KW (2010). Rab10 associates with primary cilia and exocyst complex in renal epithelial cells. Am J Physiol Renal Physiol 299, F495-F506.
4. Badano JL, Mitsuma N, Beales PL, Katsanis N (2006). The ciliopathies: an emerging class of human genetic disorders. Annu Rev Genomics Hum Genet 7, 125-148. (Pubitemid 44627925)
5. Battistoni A, Guarguaglini G, Degrassi F, Pittoggi C, Palena A, Di Matteo G, Pisano C, Cundari E, Lavia P (1997). Deregulated expression of the RanBP1 gene alters cell cycle progression in murine fibroblasts. J Cell Sci 110, 2345-2357. (Pubitemid 127699150)
6. Berbari NF, O'Connor AK, Haycraft CJ, Yoder BK (2009). The primary cilium as a complex signaling center. Curr Biol 19, R526-535.
7. Bischoff FR, Krebber H, Smirnova E, Dong W, Ponstingl H (1995). Coactivation of RanGTPase and inhibition of GTP dissociation by Ran-GTP binding protein RanBP1. EMBO J 14, 705-715.
8. Blacque OE et al. (2005). Functional genomics of the cilium, a sensory organelle. Curr Biol 15, 935-941. (Pubitemid 40772063)
9. Broadhead R et al. (2006). Flagellar motility is required for the viability of the bloodstream trypanosome. Nature 440, 224-227. (Pubitemid 43372101)
10. Clarke PR, Zhang C (2001). Ran GTPase: a master regulator of nuclear structure and function during the eukaryotic cell division cycle. Trends Cell Biol 11, 366-371. (Pubitemid 32900528)
11. Craige B, Tsao CC, Diener DR, Hou Y, Lechtreck KF, Rosenbaum JL, Witman GB (2010). CEP290 tethers flagellar transition zone microtubules to the membrane and regulates flagellar protein content. J Cell Biol 190, 927-940.
12. 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 USA 102, 3301-3306. (Pubitemid 40328040)
13. Di Fiore B, Ciciarello M, Mangiacasale R, Palena A, Tassin AM, Cundari E, Lavia P (2003). Mammalian RanBP1 regulates centrosome cohesion during mitosis. J Cell Sci 116, 3399-3411. (Pubitemid 37038987)
14. Dishinger JF, Kee HL, Jenkins PM, Fan S, Hurd TW, Hammond JW, Truong YN, Margolis B, Martens JR, Verhey KJ (2010). Ciliary entry of the kinesin-2 motor KIF17 is regulated by importin-beta2 and RanGTP. Nat Cell Biol 12, 703-710.
15. Efimenko E, Bubb K, Mak HY, Holzman T, Leroux MR, Ruvkun G, Thomas JH, Swoboda P (2005). Analysis of xbx genes in C. elegans. Development 132, 1923-1934. (Pubitemid 40691781)
16. Eggenschwiler JT, Espinoza E, Anderson KV (2001). Rab23 is an essential negative regulator of the mouse Sonic hedgehog signalling pathway. Nature 412, 194-198. (Pubitemid 32674717)
17. Fan S, Fogg V, Wang Q, Chen XW, Liu CJ, Margolis B (2007). A novel Crumbs3 isoform regulates cell division and ciliogenesis via importin beta interactions. J Cell Biol 178, 387-398. (Pubitemid 47196148)
18. Fliegauf M, Benzing T, Omran H (2007). When cilia go bad: cilia defects and ciliopathies. Nat Rev Mol Cell Biol 8, 880-893. (Pubitemid 47622564)
19. Follit JA, Li L, Vucica Y, Pazour GJ (2010). The cytoplasmic tail of fibrocystin contains a ciliary targeting sequence. J Cell Biol 188, 21-28.
20. Follit JA, Tuft RA, Fogarty KE, Pazour GJ (2006). The intraflagellar transport protein IFT20 is associated with the Golgi complex and is required for cilia assembly. Mol Biol Cell 17, 3781-3792. (Pubitemid 44330865)
21. Geng L, Okuhara D, Yu Z, Tian X, Cai Y, Shibazaki S, Somlo S (2006). Polycystin-2 traffics to cilia independently of polycystin-1 by using an N-terminal RVxP motif. J Cell Sci 119, 1383-1395.
22. Gerdes JM, Davis EE, Katsanis N (2009). The vertebrate primary cilium in development, homeostasis, and disease. Cell 137, 32-45.
23. Gherman A, Davis EE, Katsanis N (2006). The ciliary proteome database: an integrated community resource for the genetic and functional dissection of cilia. Nat Genet 38, 961-962. (Pubitemid 44325911)
24. Gorlich D, Seewald MJ, Ribbeck K (2003). Characterization of Ran-driven cargo transport and the RanGTPase system by kinetic measurements and computer simulation. EMBO J 22, 1088-1100. (Pubitemid 36313593)
25. Guarguaglini G, Battistoni A, Pittoggi C, Di Matteo G, Di Fiore B, Lavia P (1997). Expression of the murine RanBP1 and Htf9-c genes is regulated from a shared bidirectional promoter during cell cycle progression. Biochem J 325, 277-286. (Pubitemid 27322713)
26. Guarguaglini G, Renzi L, D'Ottavio F, Di Fiore B, Casenghi M, Cundari E, Lavia P (2000). Regulated Ran-binding protein 1 activity is required for organization and function of the mitotic spindle in mammalian cells in vivo. Cell Growth Differ 11, 455-465. (Pubitemid 30644369)
27. Harel A, Forbes DJ (2004). Importin beta: conducting a much larger cellular symphony. Mol Cell 16, 319-330. (Pubitemid 39504787)
28. Hayashi N, Yokoyama N, Seki T, Azuma Y, Ohba T, Nishimoto T (1995). RanBP1, a Ras-like nuclear G protein binding to Ran/TC4, inhibits RCC1 via Ran/TC4. Mol Gen Genet 247, 661-669.
29. Haycraft CJ, Banizs B, Aydin-Son Y, Zhang Q, Michaud EJ, Yoder BK (2005). Gli2 and Gli3 localize to cilia and require the intraflagellar transport protein polaris for processing and function. PLoS Genet 1, e53.
30. Huangfu D, Liu A, Rakeman AS, Murcia NS, Niswander L, Anderson KV (2003). Hedgehog signalling in the mouse requires intraflagellar transport proteins. Nature 426, 83-87. (Pubitemid 37432545)
31. Hurd TW, Fan S, Margolis BL (2011). Localization of retinitis pigmentosa 2 to cilia is regulated by importin beta2. J Cell Sci 124, 718-726.
32. Jenkins PM, Hurd TW, Zhang L, McEwen DP, Brown RL, Margolis B, Verhey KJ, Martens JR (2006). Ciliary targeting of olfactory CNG channels requires the CNGB1b subunit and the kinesin-2 motor protein, KIF17. Curr Biol 16, 1211-1216. (Pubitemid 43867290)
33. Johnson JL, Leroux MR (2010). cAMP and cGMP signaling: sensory systems with prokaryotic roots adopted by eukaryotic cilia. Trends Cell Biol 20, 435-444.
34. Kalab P, Pralle A, Isacoff EY, Heald R, Weis K (2006). Analysis of a RanGTP-regulated gradient in mitotic somatic cells. Nature 440, 697-701.
35. Kalab P, Heald R (2008). The RanGTP gradient - a GPS for the mitotic spindle. J Cell Sci 121, 1577-1586. (Pubitemid 351911814)
36. Keller LC, Romijn EP, Zamora I, Yates JR 3rd, Marshall WF (2005). Proteomic analysis of isolated Chlamydomonas centrioles reveals orthologs of ciliary-disease genes. Curr Biol 15, 1090-1098. (Pubitemid 40841351)
37. Keryer G, Di Fiore B, Celati C, Lechtreck KF, Mogensen M, Delouvee A, Lavia P, Bornens M, Tassin AM (2003). Part of Ran is associated with AKAP450 at the centrosome: involvement in microtubule-organizing activity. Mol Biol Cell 14, 4260-4271. (Pubitemid 37186326)
38. Knoddler A, Feng S, Zhang J, Zhang X, Das A, Peranen J, Guo W (2010). Coordination of Rab8 and Rab11 in primary ciliogenesis. Proc Natl Acad Sci USA 107, 6346-6351.
39. Kuhlmann J, Macara I, Wittinghofer A (1997). Dynamic and equilibrium studies on the interaction of Ran with its effector, RanBP1. Biochemistry 36, 12027-12035. (Pubitemid 27440940)
40. Lai KO, Zhao Y, Ch'ng TH, Martin KC (2008). Importin-mediated retrograde transport of CREB2 from distal processes to the nucleus in neurons. Proc Natl Acad Sci USA 105, 17175-17180.
41. Lal M, Song X, Pluznick JL, Di Giovanni V, Merrick DM, Rosenblum ND, Chauvet V, Gottardi CJ, Pei Y, Caplan MJ (2008). Polycystin-1 C-terminal tail associates with beta-catenin and inhibits canonical Wnt signaling. Hum Mol Genet 17, 3105-3117.
42. Li JB et al. (2004). Comparative genomics identifies a flagellar and basal body proteome that includes the BBS5 human disease gene. Cell 117, 541-552. (Pubitemid 38610238)
43. Liu Q, Tan G, Levenkova N, Li T, Pugh EN Jr, Rux JJ, Speicher DW, Pierce EA (2007). The proteome of the mouse photoreceptor sensory cilium complex. Mol Cell Proteomics 6, 1299-1317. (Pubitemid 47365430)
44. Lounsbury KM, Macara IG (1997). Ran-binding protein 1 (RanBP1) forms a ternary complex with Ran and karyopherin beta and reduces Ran GTPase-activating protein (RanGAP) inhibition by karyopherin beta. J Biol Chem 272, 551-555. (Pubitemid 27021193)
45. Nachury MV et al. (2007). A core complex of BBS proteins cooperates with the GTPase Rab8 to promote ciliary membrane biogenesis. Cell 129, 1201-1213. (Pubitemid 46891037)
46. Nachury MV, Maresca TJ, Salmon WC, Waterman-Storer CM, Heald R, Weis K (2001). Importin beta is a mitotic target of the small GTPase Ran in spindle assembly. Cell 104, 95-106. (Pubitemid 32144975)
47. Nonaka S, Shiratori H, Saijoh Y, Hamada H (2002). Determination of left-right patterning of the mouse embryo by artificial nodal flow. Nature 418, 96-99. (Pubitemid 34742578)
48. Pazour GJ, Agrin N, Leszyk J, Witman GB (2005). Proteomic analysis of a eukaryotic cilium. J Cell Biol 170, 103-113. (Pubitemid 40994100)
49. Pazour GJ, Bloodgood RA (2008). Targeting proteins to the ciliary membrane. Curr Top Dev Biol 85, 115-149.
50. Pedersen LB, Rosenbaum JL (2008). Intraflagellar transport (IFT) role in ciliary assembly, resorption and signalling. Curr Top Dev Biol 85, 23-61.
51. Pemberton LF, Paschal BM (2005). Mechanisms of receptor-mediated nuclear import and nuclear export. Traffic 6, 187-198. (Pubitemid 40298153)
52. Pugacheva EN, Jablonski SA, Hartman TR, Henske EP, Golemis EA (2007). HEF1-dependent Aurora A activation induces disassembly of the primary cilium. Cell 129, 1351-1363. (Pubitemid 46962087)
53. Richards SA, Lounsbury KM, Macara IG (1995). The C terminus of the nuclear RAN/TC4 GTPase stabilizes the GDP-bound state and mediates interactions with RCC1, RAN-GAP, and HTF9A/RANBP1. J Biol Chem 270, 14405-14411.
54. Rosenbaum JL, Witman GB (2002). Intraflagellar transport. Nat Rev Mol Cell Biol 3, 813-825. (Pubitemid 35285272)
55. Sajjan U, Keshavjee S, Forstner J (2004). Responses of well-differentiated airway epithelial cell cultures from healthy donors and patients with cystic fibrosis to Burkholderia cenocepacia infection. Infect Immun 72, 4188-4199. (Pubitemid 38821933)
56. Satir P, Christensen ST (2007). Overview of structure and function of mammalian cilia. Annu Rev Physiol 69, 377-400. (Pubitemid 46457649)
57. Schneider L, Clement CA, Teilmann SC, Pazour GJ, Hoffmann EK, Satir P, Christensen ST (2005). PDGFRalphaalpha signaling is regulated through the primary cilium in fibroblasts. Curr Biol 15, 1861-1866. (Pubitemid 41501522)
58. Scholey JM (2008). Intraflagellar transport motors in cilia: moving along the cell's antenna. J Cell Biol 180, 23-29.
59. Schulze H, Dose M, Korpal M, Meyer I, Italiano JE Jr, Shivdasani RA (2008). RanBP10 is a cytoplasmic guanine nucleotide exchange factor that modulates noncentrosomal microtubules. J Biol Chem 283, 14109-14119.
60. Stolc V, Samanta MP, Tongprasit W, Marshall WF (2005). Genome-wide transcriptional analysis of flagellar regeneration in Chlamydomonas reinhardtii identifies orthologs of ciliary disease genes. Proc Natl Acad Sci USA 102, 3703-3707. (Pubitemid 40354675)
61. Tao B, Bu S, Yang Z, Siroky B, Kappes JC, Kispert A, Guay-Woodford LM (2009). Cystin localizes to primary cilia via membrane microdomains and a targeting motif. J Am Soc Nephrol 20, 2570-2580.
62. Tedeschi A, Ciciarello M, Mangiacasale R, Roscioli E, Rensen WM, Lavia P (2007). RANBP1 localizes a subset of mitotic regulatory factors on spindle microtubules and regulates chromosome segregation in human cells. J Cell Sci 120, 3748-3761. (Pubitemid 350187357)
63. Williams CL et al. (2011). MKS and NPHP modules cooperate to establish basal body/transition zone membrane associations and ciliary gate function during ciliogenesis. J Cell Biol 192, 1023-1041.
64. Yoshimura S, Egerer J, Fuchs E, Haas AK, Barr FA (2007). Functional dissection of Rab GTPases involved in primary cilium formation. J Cell Biol 178, 363-369. (Pubitemid 47196146)
65. Yudin D, Fainzilber M (2009). Ran on tracks - cytoplasmic roles for a nuclear regulator. J Cell Sci 122, 587-593.
66. Yudin D et al. (2008). Localized regulation of axonal RanGTPase controls retrograde injury signaling in peripheral nerve. Neuron 59, 241-252. (Pubitemid 352033684)