Heat shock induces rapid resorption of primary cilia

Journal of Cell Science

Volumn 125, Issue 18, 2012, Pages 4297-4305

  Prodromou, Natalia V ^a   Thompson, Clare L ^a,b   Osborn, Daniel P S ^c   Cogger, Kathryn F ^a   Ashworth, Rachel ^d   Knight, Martin M ^b   Beales, Philip L ^c   Chapple, J Paul ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Heat shock; Molecular chaperone; Primary cilia

Indexed keywords

HEAT SHOCK PROTEIN 90; HISTONE DEACETYLASE 6; SONIC HEDGEHOG PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; AXONEME; CELL METABOLISM; CELL RESORPTION; CELL STRESS; CONTROLLED STUDY; EMBRYO; EUKARYOTIC FLAGELLUM; HEAT SHOCK RESPONSE; HEAT TOLERANCE; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; ZEBRA FISH;

ANIMALS; AXONEME; CILIA; HEAT-SHOCK RESPONSE; HEDGEHOG PROTEINS; HISTONE DEACETYLASES; HSP90 HEAT-SHOCK PROTEINS; HUMANS; MICE; NIH 3T3 CELLS; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TEMPERATURE; ZEBRAFISH;

DANIO RERIO; ERINACEIDAE; MAMMALIA;

EID: 84872201378     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.100545     Document Type: Article

References (33)

1. Anckar, J. and Sistonen, L. (2007). Heat shock factor 1 as a coordinator of stress and developmental pathways. Adv. Exp. Med. Biol. 594, 78-88.
2. Baker, K. and Beales, P. L. (2009). Making sense of cilia in disease: the human ciliopathies. Am. J. Med. Genet. C. Semin. Med. Genet. 151C, 281-295.
3. Berbari, N. F., O'Connor, A. K., Haycraft, C. J. and Yoder, B. K. (2009). The primary cilium as a complex signaling center. Curr. Biol. 19, R526-R535.
4. Boyault, C., Zhang, Y., Fritah, S., Caron, C., Gilquin, B., Kwon, S. H., Garrido, C., Yao, T. P., Vourc'h, C., Matthias, P. et al. (2007). HDAC6 controls major cell response pathways to cytotoxic accumulation of protein aggregates. Genes Dev. 21, 2172-2181.
5. Breunig, J. J., Sarkisian, M. R., Arellano, J. I., Morozov, Y. M., Ayoub, A. E., Sojitra, S., Wang, B., Flavell, R. A., Rakic, P. and Town, T. (2008). Primary cilia regulate hippocampal neurogenesis by mediating sonic hedgehog signaling. Proc. Natl. Acad. Sci. USA 105, 13127-13132.
6. Caspary, T., Larkins, C. E. and Anderson, K. V. (2007). The graded response to Sonic Hedgehog depends on cilia architecture. Dev. Cell 12, 767-778.
7. Corbit, K. C., Aanstad, P., Singla, V., Norman, A. R., Stainier, D. Y. and Reiter, J. F. (2005). Vertebrate Smoothened functions at the primary cilium. Nature 437, 1018-1021.
8. Cotto, J. J. and Morimoto, R. I. (1999). Stress-induced activation of the heat-shock response: cell and molecular biology of heat-shock factors. Biochem. Soc. Symp. 64, 105-118.
9. Davenport, J. R. and Yoder, B. K. (2005). An incredible decade for the primary cilium: a look at a once-forgotten organelle. Am. J. Physiol. 289, F1159-F1169.
10. Fliegauf, M., Benzing, T. and Omran, H. (2007). When cilia go bad: cilia defects and ciliopathies. Nat. Rev. Mol. Cell Biol. 8, 880-893.
11. Gherman, A., Davis, E. E. and Katsanis, N. (2006). The ciliary proteome database: an integrated community resource for the genetic and functional dissection of cilia. Nat. Genet. 38, 961-962.
12. Han, Y. G., Kim, H. J., Dlugosz, A. A., Ellison, D. W., Gilbertson, R. J. and Alvarez-Buylla, A. (2009). Dual and opposing roles of primary cilia in medulloblastoma development. Nat. Med. 15, 1062-1065.
13. Haycraft, C. J., Banizs, B., Aydin-Son, Y., Zhang, Q., Michaud, E. J. and Yoder, B. K. (2005). Gli2 and Gli3 localize to cilia and require the intraflagellar transport protein polaris for processing and function. PLoS Genet. 1, e53.
14. Kültz, D. (2005). Molecular and evolutionary basis of the cellular stress response. Annu. Rev. Physiol. 67, 225-257.
15. Lange, B. M., Bachi, A., Wilm, M. and González, C. (2000). Hsp90 is a core centrosomal component and is required at different stages of the centrosome cycle in Drosophila and vertebrates. EMBO J. 19, 1252-1262.
16. McGlashan, S. R., Knight, M. M., Chowdhury, T. T., Joshi, P., Jensen, C. G., Kennedy, S. and Poole, C. A. (2010). Mechanical loading modulates chondrocyte primary cilia incidence and length. Cell Biol. Int. 34, 441-446.
17. Meimaridou, E., Gooljar, S. B., Ramnarace, N., Anthonypillai, L., Clark, A. J. and Chapple, J. P. (2011). The cytosolic chaperone Hsc70 promotes traffic to the cell surface of intracellular retained melanocortin-4 receptor mutants. Mol. Endocrinol. 25, 1650-1660.
18. Nauli, S. M., Alenghat, F. J., Luo, Y., Williams, E., Vassilev, P., Li, X., Elia, A. E., Lu, W., Brown, E. M., Quinn, S. J. et al. (2003). Polycystins 1 and 2 mediate mechanosensation in the primary cilium of kidney cells. Nat. Genet. 33, 129-137.
19. Ng, D. C. and Bogoyevitch, M. A. (2000). The mechanism of heat shock activation of ERK mitogen-activated protein kinases in the interleukin 3-dependent ProB cell line BaF3. J. Biol. Chem. 275, 40856-40866.
20. Nigg, E. A. and Raff, J. W. (2009). Centrioles, centrosomes, and cilia in health and disease. Cell 139, 663-678.
21. Overgaard, C. E., Sanzone, K. M., Spiczka, K. S., Sheff, D. R., Sandra, A. and Yeaman, C. (2009). Deciliation is associated with dramatic remodeling of epithelial cell junctions and surface domains. Mol. Biol. Cell 20, 102-113.
22. Pedersen, L. B., Veland, I. R., Schrøder, J. M. and Christensen, S. T. (2008). Assembly of primary cilia. Dev. Dyn. 237, 1993-2006.
23. Pugacheva, E. N., Jablonski, S. A., Hartman, T. R., Henske, E. P. and Golemis, E. A. (2007). HEF1-dependent Aurora A activation induces disassembly of the primary cilium. Cell 129, 1351-1363.
24. Quarmby, L. M. (2004). Cellular deflagellation. Int. Rev. Cytol. 233, 47-91.
25. Rohatgi, R., Milenkovic, L., Corcoran, R. B. and Scott, M. P. (2009). Hedgehog signal transduction by Smoothened: pharmacologic evidence for a 2-step activation process. Proc. Natl. Acad. Sci. USA 106, 3196-3201.
26. Rosenbaum, J. L. and Witman, G. B. (2002). Intraflagellar transport. Nat. Rev. Mol. Cell Biol. 3, 813-825.
27. Schneider, L., Clement, C. A., Teilmann, S. C., Pazour, G. J., Hoffmann, E. K., Satir, P. and Christensen, S. T. (2005). PDGFRalphaalpha signaling is regulated through the primary cilium in fibroblasts. Curr. Biol. 15, 1861-1866.
28. Seeley, E. S. and Nachury, M. V. (2010). The perennial organelle: assembly and disassembly of the primary cilium. J. Cell Sci. 123, 511-518.
29. Singla, V. and Reiter, J. F. (2006). The primary cilium as the cell's antenna: signaling at a sensory organelle. Science 313, 629-633.
30. Taipale, J., Chen, J. K., Cooper, M. K., Wang, B., Mann, R. K., Milenkovic, L., Scott, M. P. and Beachy, P. A. (2000). Effects of oncogenic mutations in Smoothened and Patched can be reversed by cyclopamine. Nature 406, 1005-1009.
31. Takaki, E., Fujimoto, M., Nakahari, T., Yonemura, S., Miyata, Y., Hayashida, N., Yamamoto, K., Vallee, R. B., Mikuriya, T., Sugahara, K. et al. (2007). Heat shock transcription factor 1 is required for maintenance of ciliary beating in mice. J. Biol. Chem. 282, 37285-37292.
32. Weis, F., Moullintraffort, L., Heichette, C., Chrétien, D. and Garnier, C. (2010). The 90-kDa heat shock protein Hsp90 protects tubulin against thermal denaturation. J. Biol. Chem. 285, 9525-9534.
33. Williams, N. E. and Nelsen, E. M. (1997). HSP70 and HSP90 homologs are associated with tubulin in hetero-oligomeric complexes, cilia and the cortex of Tetrahymena. J. Cell Sci. 110, 1665-1672.