HSPB1 Facilitates the Formation of Non-Centrosomal Microtubules

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Almeida Souza, Leonardo ^a,b,e   Asselbergh, Bob ^a,b   De Winter, Vicky ^a,b   Goethals, Sofie ^a,b   Timmerman, Vincent ^a,b   Janssens, Sophie ^a,c,d  

^a UNIVERSITY OF ANTWERP   (Belgium)

^b UNIVERSITY OF ANTWERP   (Belgium)

^c GHENT UNIVERSITY   (Belgium)

^d DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^e MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK PROTEIN 27;

ARTICLE; CELL ASSAY; CELLULAR DISTRIBUTION; CENTROSOME; CONTROLLED STUDY; CYTOARCHITECTURE; IN VITRO STUDY; MICROTUBULE; MICROTUBULE ASSEMBLY; NON CENTROSOMAL MICROTUBULE; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; STEADY STATE;

ANIMALS; CENTROSOME; CHO CELLS; CRICETULUS; HELA CELLS; HSP27 HEAT-SHOCK PROTEINS; HUMANS; MICROSCOPY, IMMUNOELECTRON; MICROTUBULES; PROTEIN BINDING;

MAMMALIA;

EID: 84879474324     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0066541     Document Type: Article

References (56)

1. Kostenko S, Moens U, (2009) Heat shock protein 27 phosphorylation: kinases, phosphatases, functions and pathology. Cell Mol Life Sci 66: 3289-3307.
2. Sun Y, Macrae TH, (2005) The small heat shock proteins and their role in human disease. FEBS J 272: 2613-2627.
3. Evgrafov OV, Mersiyanova I, Irobi J, Van Den Bosch L, Dierick I, et al. (2004) Mutant small heat-shock protein 27 causes axonal Charcot-Marie-Tooth disease and distal hereditary motor neuropathy. Nat Genet 36: 602-606.
4. Almeida-Souza L, Goethals S, De Winter V, Dierick I, Gallardo R, et al. (2010) Increased monomerization of mutant HSPB1 leads to protein hyperactivity in Charcot-Marie-Tooth neuropathy. J Biol Chem 285: 12778-12786.
5. Almeida-Souza L, Asselbergh B, d'Ydewalle C, Moonens K, Goethals S, et al. (2011) Small heat-shock protein HSPB1 mutants stabilize microtubules in Charcot-Marie-Tooth neuropathy. J Neurosci 31: 15320-15328.
6. Bunker JM, Kamath K, Wilson L, Jordan MA, Feinstein SC, (2006) FTDP-17 mutations compromise the ability of tau to regulate microtubule dynamics in cells. J Biol Chem 281: 11856-11863.
7. Hino M, Kurogi K, Okubo MA, Murata-Hori M, Hosoya H, (2000) Small heat shock protein 27 (HSP27) associates with tubulin/microtubules in HeLa cells. Biochem Biophys Res Commun 271: 164-169.
8. Williams KL, Rahimtula M, Mearow KM, (2005) Hsp27 and axonal growth in adult sensory neurons in vitro. BMC Neurosci 6: 24.
9. Salmon P, Trono D (2006) Production and titration of lentiviral vectors. Curr Protoc Neurosci Chapter 4: Unit 12.10.
10. Schneider CA, Rasband WS, Eliceiri KW, (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9: 671-675.
11. Barron DM, Chatterjee SK, Ravindra R, Roof R, Baloglu E, et al. (2003) A fluorescence-based high-throughput assay for antimicrotubule drugs. Anal Biochem 315: 49-56.
12. Thevenaz P, Unser M, (2007) User-friendly semiautomated assembly of accurate image mosaics in microscopy. Microsc Res Tech 70: 135-146.
13. Paul C, Manero F, Gonin S, Kretz-Remy C, Virot S, et al. (2002) Hsp27 as a negative regulator of cytochrome C release. Mol Cell Biol 22: 816-834.
14. Huot J, Roy G, Lambert H, Chretien P, Landry J, (1991) Increased survival after treatments with anticancer agents of Chinese hamster cells expressing the human Mr 27,000 heat shock protein. Cancer Res 51: 5245-5252.
15. Stiess M, Maghelli N, Kapitein LC, Gomis-Ruth S, Wilsch-Brauninger M, et al. (2010) Axon extension occurs independently of centrosomal microtubule nucleation. Science 327: 704-707.
16. Chabin-Brion K, Marceiller J, Perez F, Settegrana C, Drechou A, et al. (2001) The Golgi complex is a microtubule-organizing organelle. Mol Biol Cell 12: 2047-2060.
17. Efimov A, Kharitonov A, Efimova N, Loncarek J, Miller PM, et al. (2007) Asymmetric CLASP-dependent nucleation of noncentrosomal microtubules at the trans-Golgi network. Dev Cell 12: 917-930.
18. Komarova YA, Vorobjev IA, Borisy GG, (2002) Life cycle of MTs: persistent growth in the cell interior, asymmetric transition frequencies and effects of the cell boundary. J Cell Sci 115: 3527-3539.
19. Moores CA, Perderiset M, Kappeler C, Kain S, Drummond D, et al. (2006) Distinct roles of doublecortin modulating the microtubule cytoskeleton. EMBO J 25: 4448-4457.
20. Moores CA, Perderiset M, Francis F, Chelly J, Houdusse A, et al. (2004) Mechanism of microtubule stabilization by doublecortin. Mol Cell 14: 833-839.
21. Al Bassam J, Ozer RS, Safer D, Halpain S, Milligan RA, (2002) MAP2 and tau bind longitudinally along the outer ridges of microtubule protofilaments. J Cell Biol 157: 1187-1196.
22. Howard J, Hyman AA, (2003) Dynamics and mechanics of the microtubule plus end. Nature 422: 753-758.
23. Luders J, Stearns T, (2007) Opinion- Microtubule-organizing centres: a re-evaluation. Nat Rev Mol Cell Biol 8: 161-167.
24. Roll-Mecak A, Mcnally FJ, (2010) Microtubule-severing enzymes. Curr Opin Cell Biol 22: 96-103.
25. Kollman JM, Merdes A, Mourey L, Agard DA, (2011) Microtubule nucleation by gamma-tubulin complexes. Nat Rev Mol Cell Biol 12: 709-721.
26. Lundin VF, Leroux MR, Stirling PC, (2010) Quality control of cytoskeletal proteins and human disease. Trends Biochem Sci 35: 288-297.
27. Rios RM, Sanchis A, Tassin AM, Fedriani C, Bornens M, (2004) GMAP-210 recruits gamma-tubulin complexes to cis-Golgi membranes and is required for Golgi ribbon formation. Cell 118: 323-335.
28. Rivero S, Cardenas J, Bornens M, Rios RM, (2009) Microtubule nucleation at the cis-side of the Golgi apparatus requires AKAP450 and GM130. EMBO J 28: 1016-1028.
29. Vinogradova T, Miller PM, Kaverina I, (2009) Microtubule network asymmetry in motile cells Role of Golgi-derived array. Cell Cycle 8: 2168-2174.
30. Bugnard E, Zaal KJ, Ralston E, (2005) Reorganization of microtubule nucleation during muscle differentiation. Cell Motil Cytoskeleton 60: 1-13.
31. Macurek L, Draberova E, Richterova V, Sulimenko V, Sulimenko T, et al. (2008) Regulation of microtubule nucleation from membranes by complexes of membrane-bound gamma-tubulin with Fyn kinase and phosphoinositide 3-kinase. Biochem J 416: 421-430.
32. Reilein A, Nelson WJ, (2005) APC is a component of an organizing template for cortical microtubule networks. Nat Cell Biol 7: 463-473.
33. Parcellier A, Schmitt E, Gurbuxani S, Seigneurin-Berny D, Pance A, et al. (2003) HSP27 is a ubiquitin-binding protein involved in I-kappaBalpha proteasomal degradation. Mol Cell Biol 23: 5790-5802.
34. Parcellier A, Brunet M, Schmitt E, Col E, Didelot C, et al. (2006) HSP27 favors ubiquitination and proteasomal degradation of p27Kip1 and helps S-phase re-entry in stressed cells. FASEB J 20: 1179-1181.
35. Gibert B, Eckel B, Fasquelle L, Moulin M, Bouhallier F, et al. (2012) Knock down of heat shock protein 27 (HspB1) induces degradation of several putative client proteins. PLoS One 7: e29719.
36. Knapinska AM, Gratacos FM, Krause CD, Hernandez K, Jensen AG, et al. (2011) Chaperone Hsp27 modulates AUF1 proteolysis and AU-rich element-mediated mRNA degradation. Mol Cell Biol 31: 1419-1431.
37. Miron T, Wilchek M, Geiger B, (1988) Identification of a 25 kDa actin capping protein in smooth muscle tissues. J Muscle Res Cell Motil 9: 91.
38. Miron T, Vancompernolle K, Vandekerckhove J, Wilchek M, Geiger B, (1991) A 25-kD inhibitor of actin polymerization is a low molecular mass heat shock protein. J Cell Biol 114: 255-261.
39. Benndorf R, Hayess K, Ryazantsev S, Wieske M, Behlke J, et al. (1994) Phosphorylation and supramolecular organization of murine small heat shock protein HSP25 abolish its actin polymerization-inhibiting activity. J Biol Chem 269: 20780-20784.
40. Pivovarova AV, Chebotareva NA, Chernik IS, Gusev NB, Levitsky DI, (2007) Small heat shock protein Hsp27 prevents heat-induced aggregation of F-actin by forming soluble complexes with denatured actin. FEBS J 274: 5937-5948.
41. Pivovarova AV, Mikhailova VV, Chernik IS, Chebotareva NA, Levitsky DI, et al. (2005) Effects of small heat shock proteins on the thermal denaturation and aggregation of F-actin. Biochem Biophys Res Commun 331: 1548-1553.
42. During RL, Gibson BG, Li W, Bishai EA, Sidhu GS, et al. (2007) Anthrax lethal toxin paralyzes actin-based motility by blocking Hsp27 phosphorylation. EMBO J 26: 2240-2250.
43. Bova MP, Mchaourab HS, Han Y, Fung BK, (2000) Subunit exchange of small heat shock proteins. Analysis of oligomer formation of alphaA-crystallin and Hsp27 by fluorescence resonance energy transfer and site-directed truncations. J Biol Chem 275: 1035-1042.
44. Friedrich KL, Giese KC, Buan NR, Vierling E, (2004) Interactions between small heat shock protein subunits and substrate in small heat shock protein-substrate complexes. J Biol Chem 279: 1080-1089.
45. Wettstein G, Bellaye PS, Micheau O, Bonniaud P, (2012) Small heat shock proteins and the cytoskeleton: An essential interplay for cell integrity? Int J Biochem Cell Biol 44(10): 1680-1686.
46. Bartolini F, Gundersen GG, (2006) Generation of noncentrosomal microtubule arrays. J Cell Sci 119: 4155-4163.
47. Knowlton AA, Kapadia S, Torre-Amione G, Durand JB, Bies R, et al. (1998) Differential expression of heat shock proteins in normal and failing human hearts. J Mol Cell Cardiol 30: 811-818.
48. Chen S, Brown IR, (2007) Neuronal expression of constitutive heat shock proteins: implications for neurodegenerative diseases. Cell Stress Chaperones 12: 51-58.
49. Jonak C, Mildner M, Klosner G, Paulitschke V, Kunstfeld R, et al. (2011) The hsp27kD heat shock protein and p38-MAPK signaling are required for regular epidermal differentiation. J Dermatol Sci 61: 32-37.
50. Mehlen P, Coronas V, Ljubic-Thibal V, Ducasse C, Granger L, et al. (1999) Small stress protein Hsp27 accumulation during dopamine-mediated differentiation of rat olfactory neurons counteracts apoptosis. Cell Death Differ 6: 227-233.
51. Brown DD, Christine KS, Showell C, Conlon FL, (2007) Small heat shock protein Hsp27 is required for proper heart tube formation. Genesis 45: 667-678.
52. Ferns G, Shams S, Shafi S, (2006) Heat shock protein 27: its potential role in vascular disease. Int J Exp Pathol 87: 253-274.
53. Stetler RA, Gao Y, Signore AP, Cao G, Chen J, (2009) HSP27: mechanisms of cellular protection against neuronal injury. Curr Mol Med 9: 863-872.
54. Chen L, Stone MC, Tao J, Rolls MM, (2012) Axon injury and stress trigger a microtubule-based neuroprotective pathway. Proc Natl Acad Sci U S A 109: 11842-11847.
55. Erturk A, Hellal F, Enes J, Bradke F, (2007) Disorganized microtubules underlie the formation of retraction bulbs and the failure of axonal regeneration. J Neurosci 27: 9169-9180.
56. Xiao J, Zhao H, Liang D, Liu Y, Zhang H, et al. (2010) Taxol, a microtubule stabilizer, improves cardiac contractile function during ischemia in vitro. Pharmacology 85: 301-310.