Superresolution STED microscopy reveals differential localization in primary cilia

Cytoskeleton

Volumn 70, Issue 1, 2013, Pages 54-65

  Yang, T Tony ^a   Hampilos, Perry J ^b   Nathwani, Bhavik ^a   Miller, Christine H ^a   Sutaria, Nupur D ^a   Liao, Jung Chi ^a  

^a Columbia University ^*  (United States)

^b Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

Adenylyl cyclase type III; IFT88; Intraflagellar transport; Primary cilium; Stimulated emission depletion

Indexed keywords

ADENYLATE CYCLASE; ADENYLYL CYCLASE TYPE III; CELL PROTEIN; INTRAFLAGELLAR TRANSPORT 88 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL ORGANELLE; CELL POLARITY; CELL TYPE; CELLULAR DISTRIBUTION; CILIATED EPITHELIUM; COMPLEX FORMATION; CONTROLLED STUDY; FIBROBLAST; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOHISTOCHEMISTRY; KIDNEY COLLECTING TUBULE; KIDNEY MEDULLA; MICROSCOPY; MOLECULAR IMAGING; NONHUMAN; PRIMARY CILIA; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; STIMULATED EMISSION DEPLETION MICROSCOPY;

CELL LINE; CILIA; FIBROBLASTS; HUMANS; MICROSCOPY;

ERINACEIDAE;

EID: 84872611150     PISSN: 19493584     EISSN: 19493592     Source Type: Journal    
DOI: 10.1002/cm.21090     Document Type: Article

References (47)

1. Absalon S, Blisnick T, Kohl L, Toutirais G, Doré G, Julkowska D, Tavenet A, Bastin P. 2008. Intraflagellar transport and functional analysis of genes required for flagellum formation in trypanosomes. Mol Biol Cell 19( 3): 929-944.
2. Bakalyar HA, Reed RR. 1990. Identification of a specialized adenylyl cyclase that may mediate odorant detection. Science 250( 4986): 1403-1406.
3. Bautista-Harris G, Klotz C, Bordes N, Sandoz D. 1991. An helicoidal structure surrounding the cilium axoneme: visualization by the monoclonal antibody CC-248. Biol Cell 71( 1-2): 191-200.
4. Berbari NF, Bishop GA, Askwith CC, Lewis JS, Mykytyn K. 2007. Hippocampal neurons possess primary cilia in culture. J Neurosci Res 85( 5): 1095-1100.
5. Besschetnova TY, Kolpakova-Hart E, Guan Y, Zhou J, Olsen BR, Shah JV. 2010. Identification of signaling pathways regulating primary cilium length and flow-mediated adaptation. Curr Biol 20( 2): 182-187.
6. Betzig E, Patterson GH, Sougrat R, Lindwasser OW, Olenych S, Bonifacino JS, Davidson MW, Lippincott-Schwartz J, Hess HF. 2006. Imaging intracellular fluorescent proteins at nanometer resolution. Science 313( 5793): 1642-1645.
7. Bisgrove BW, Yost HJ. 2006. The roles of cilia in developmental disorders and disease. Development 133( 21): 4131-4143.
8. Bishop GA, Berbari NF, Lewis J, Mykytyn K. 2007. Type III adenylyl cyclase localizes to primary cilia throughout the adult mouse brain. J Comp Neurol 505( 5): 562-571.
9. Brown JM, Fine NA, 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( 8): 3192-3207.
10. Clement CA, Kristensen SG, Møllgård K, Pazour GJ, Yoder BK, Larsen LA, Christensen ST. 2009. The primary cilium coordinates early cardiogenesis and hedgehog signaling in cardiomyocyte differentiation. J Cell Sci 122( 17): 3070-3082.
11. Cole DG, Diener DR, Himelblau AL, Beech PL, Fuster JC, Rosenbaum JL. 1998. Chlamydomonas kinesin-II-dependent intraflagellar transport (IFT): IFT particles contain proteins required for ciliary assembly in Caenorhabditis elegans sensory neurons. J Cell Biol 141( 4): 993-1008.
12. Defer N, Best-Belpomme M, Hanoune J. 2000. Tissue specificity and physiological relevance of various isoforms of adenylyl cyclase. Am J Physiol Renal Physiol 279( 3): F400-F416.
13. 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( 9): 3781-3792.
14. 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( 7): 1383-1395.
15. Goetz SC, Anderson KV. 2010. The primary cilium: a signalling centre during vertebrate development. Nat Rev Genet 11( 5): 331-344.
16. Haycraft CJ, Swoboda P, Taulman PD, Thomas JH, Yoder BK. 2001. The C. elegans homolog of the murine cystic kidney disease gene Tg737 functions in a ciliogenic pathway and is disrupted in osm-5 mutant worms. Development 128( 9): 1493-1505.
17. Hein B, Willig KI, Hell SW. 2008. Stimulated emission depletion (STED) nanoscopy of a fluorescent protein-labeled organelle inside a living cell. Proceedings of the National Academy of Sciences 105( 38): 14271-14276.
18. Hell SW, Wichmann J. 1994. Breaking the diffraction resolution limit by stimulated emission: stimulated-emission-depletion fluorescence microscopy. Opt Lett 19( 11): 780-782.
19. Igarashi P, Somlo S. 2002. Genetics and pathogenesis of polycystic kidney disease. J Am Soc Nephrol 13( 9): 2384-2398.
20. Ishikawa H, Marshall WF. 2011. Ciliogenesis: building the cell's antenna. Nat Rev Mol Cell Biol 12( 4): 222-234.
21. Klar TA, Jakobs S, Dyba M, Egner A, Hell SW. 2000. Fluorescence microscopy with diffraction resolution barrier broken by stimulated emission. Proc Natl Acad Sci 97( 15): 8206-8210.
22. Klotz C, Bordes N, Laine MC, Sandoz D, Bornens M. 1986. A protein of 175, 000 daltons associated with striated rootlets in ciliated epithelia, as revealed by a monoclonal antibody. Cell Motil Cytoskeleton 6( 1): 56-67.
23. Kozminski KG, Johnson KA, Forscher P, Rosenbaum JL. 1993. A motility in the eukaryotic flagellum unrelated to flagellar beating. Proc Natl Acad Sci 90( 12): 5519-5523.
24. Lauterbach MA, Ullal CK, Westphal V, Hell SW. 2010. Dynamic imaging of colloidal-crystal nanostructures at 200 frames per second. Langmuir 26( 18): 14400-14404.
25. Manley S, Gillette JM, Patterson GH, Shroff H, Hess HF, Betzig E, Lippincott-Schwartz J. 2008. High-density mapping of single-molecule trajectories with photoactivated localization microscopy. Nat Methods 5( 2): 155-157.
26. Miyoshi K, Kasahara K, Miyazaki I, Asanuma M. 2009. Lithium treatment elongates primary cilia in the mouse brain and in cultured cells. Biochem Biophys Res Commun 388( 4): 757-762.
27. Miyoshi K, Kasahara K, Miyazaki I, Asanuma M. 2011. Factors that influence primary cilium length. Acta Medica Okayama 65( 5): 279-285.
28. Ou Y, Ruan Y, Cheng M, Moser JJ, Rattner JB, van der Hoorn FA. 2009. Adenylate cyclase regulates elongation of mammalian primary cilia. Exp Cell Res 315( 16): 2802-2817.
29. Pazour GJ, Dickert BL, Vucica Y, Seeley ES, Rosenbaum JL, Witman GB, Cole DG. 2000. Chlamydomonas IFT88 and its mouse homologue, polycystic kidney disease gene tg737, are required for assembly of cilia and flagella. J Cell Biol 151( 3): 709-718.
30. Pazour GJ, Baker SA, Deane JA, Cole DG, Dickert BL, Rosenbaum JL, Witman GB, Besharse JC. 2002. The intraflagellar transport protein, IFT88, is essential for vertebrate photoreceptor assembly and maintenance. J Cell Biol 157( 1): 103-114.
31. Pedersen LB, Rosenbaum JL. 2008. Chapter two intraflagellar transport (IFT): role in ciliary assembly, resorption and signalling. Curr Top Dev Biol 85: 23-61.
32. Piperno G, Mead K. 1997. Transport of a novel complex in the cytoplasmic matrix of Chlamydomonas flagella. Proc Natl Acad Sci 94( 9): 4457-4462.
33. Robert A, Margall-Ducos G, Guidotti JE, Brégerie O, Celati C, Bréchot C, Desdouets C. 2007. The intraflagellar transport component IFT88/polaris is a centrosomal protein regulating G1-S transition in non-ciliated cells. J Cell Sci 120( 4): 628-637.
34. Rohatgi R, Scott MP. 2007. Patching the gaps in Hedgehog signalling. Nat Cell Biol 9( 9): 1005-1009.
35. Rosenbaum JL, Witman GB. 2002. Intraflagellar transport. Nat Rev Mol Cell Biol 3( 11): 813-825.
36. Rust MJ, Bates M, Zhuang X. 2006. Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat Methods 3( 10): 793-796.
37. Sillibourne JE, Specht CG, Izeddin I, Hurbain I, Tran P, Triller A, Darzacq X, Dahan M, Bornens M. 2011. Assessing the localization of centrosomal proteins by PALM/STORM nanoscopy. Cytoskeleton 68( 11): 619-627.
38. Singla V, Reiter JF. 2006. The primary cilium as the cell's antenna: signaling at a sensory organelle. Science 313( 5787): 629-633.
39. Tikhonov AN, Arsenin VY. 1977. Solutions of Ill-Posed Problems. NewYork: Wiley.
40. Tran PV, Haycraft CJ, Besschetnova TY, Turbe-Doan A, Stottmann RW, Herron BJ, Chesebro AL, Qiu H, Scherz PJ, Shah JV. 2008. THM1 negatively modulates mouse sonic hedgehog signal transduction and affects retrograde intraflagellar transport in cilia. Nat Genet 40( 4): 403-410.
41. Urban NT, Willig KI, Hell SW, Nägerl UV. 2011. STED nanoscopy of actin dynamics in synapses deep inside living brain slices. Biophys J 101( 5): 1277-1284.
42. Wang Z, Phan T, Storm DR. 2011. The type 3 adenylyl cyclase is required for novel object learning and extinction of contextual memory: role of cAMP signaling in primary cilia. J Neurosci 31( 15): 5557-5561.
43. Westphal V, Rizzoli SO, Lauterbach MA, Kamin D, Jahn R, Hell SW. 2008. Video-rate far-field optical nanoscopy dissects synaptic vesicle movement. Science 320( 5873): 246-249.
44. Williams CL, Li C, Kida K, Inglis PN, Mohan S, Semenec L, Bialas NJ, Stupay RM, Chen N, Blacque OE. 2011. MKS and NPHP modules cooperate to establish basal body/transition zone membrane associations and ciliary gate function during ciliogenesis. J Cell Biol 192( 6): 1023-1041.
45. Willig KI, Harke B, Medda R, Hell SW. 2007. STED microscopy with continuous wave beams. Nat Methods 4( 11): 915-918.
46. Wong ST, Trinh K, Hacker B, Chan GCK, Lowe G, Gaggar A, Xia Z, Gold GH, Storm DR. 2000. Disruption of the type III adenylyl cyclase gene leads to peripheral and behavioral anosmia in transgenic mice. Neuron 27( 3): 487-497.
47. Yoder BK, Tousson A, Millican L, Wu JH, Bugg JrCE, Schafer JA, Balkovetz DF. 2002. Polaris, a protein disrupted in orpk mutant mice, is required for assembly of renal cilium. Am J Physiol Renal Physiol 282( 3): F541-F552.