Phosphorylation status of heat shock protein 27 influences neurite growth in adult dorsal root ganglion sensory neurons in vitro

Journal of Neuroscience Research

Volumn 89, Issue 8, 2011, Pages 1160-1172

  Williams, Kristy L ^a   Mearow, Karen M ^a  

^a MEMORIAL UNIVERSITY OF NEWFOUNDLAND   (Canada)

Author keywords

Actin polymerization; Heat shock proteins; HSP; Neurite outgrowth; Sensory neurons; Serine phosphorylation

Indexed keywords

ACTIN; COMPLEMENTARY DNA; ENHANCED GREEN FLUORESCENT PROTEIN; HEAT SHOCK PROTEIN 27; OLIGOMER; PHALLOIDIN; SMALL INTERFERING RNA;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DIMERIZATION; IMMUNOCYTOCHEMISTRY; MUTATIONAL ANALYSIS; NERVE FIBER GROWTH; NEURITE; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; QUALITATIVE ANALYSIS; RAT; SENSORY NERVE CELL; SPINAL GANGLION; STAINING;

ACTINS; ANIMALS; CELLS, CULTURED; CRICETINAE; GANGLIA, SPINAL; HSP27 HEAT-SHOCK PROTEINS; NEURITES; PHOSPHORYLATION; POSTERIOR HORN CELLS; RATS; RATS, SPRAGUE-DAWLEY; RNA, SMALL INTERFERING; TRANSFECTION;

EID: 79957870682     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.22634     Document Type: Article

References (55)

1. Ackerley S, James PA, Kalli A, French S, Davies KE, Talbot K. 2006. A mutation in the small heat-shock protein HSPB1 leading to distal hereditary motor neuronopathy disrupts neurofilament assembly and the axonal transport of specific cellular cargoes. Hum Mol Genet 15: 347-354.
2. Arrigo AP. 2007. The cellular "networking" of mammalian Hsp27 and its functions in the control of protein folding, redox state and apoptosis. Adv Exp Med Biol 594: 14-26.
3. Benn SC, Perrelet D, Kato AC, Scholz J, Decosterd I, Mannion RJ, Bakowska JC, Woolf CJ. 2002. Hsp27 upregulation and phosphorylation is required for injured sensory and motor neuron survival. 36: 45-56.
4. Benndorf R, Welsh MJ. 2004. Shocking degeneration. Nat Genet 36: 547-548.
5. Benndorf R, Hayess K, Ryazantsev S, Wieske M, Behlke J, Lutsch G. 1994. Phosphorylation and supramolecular organization of murine small heat shock protein HSP25 abolish its actin polymerization-inhibiting activity. 269: 20780-20784.
6. Chaudhuri S, Smith PG. 2008. Cyclic strain-induced HSP27 phosphorylation modulates actin filaments in airway smooth muscle cells. Am J Respir Cell Mol Biol 39: 270-278.
7. Costigan M, Mannion RJ, Kendall G, Lewis SE, Campagna JA, Coggeshall RE, Meridith-Middleton J, Tate S, Woolf CJ. 1998. Heat shock protein 27: developmental regulation and expression after peripheral nerve injury. J Neurosci 18: 5891-5900.
8. Dent EW, Gertler FB. 2003. Cytoskeletal dynamics and transport in growth cone motility and axon guidance. Neuron 40: 209-227.
9. Doshi BM, Hightower LE, Lee J. 2009. The role of Hsp27 and actin in the regulation of movement in human cancer cells responding to heat shock. Cell Stress Chaperones 14: 445-457.
10. Doshi BM, Hightower LE, Lee J. 2010. HSPB1, actin filament dynamics, and aging cells. Ann N Y Acad Sci 1197: 76-84.
11. During RL, Gibson BG, Li W, Bishai EA, Sidhu GS, Landry J, Southwick FS. 2007. Anthrax lethal toxin paralyzes actin-based motility by blocking Hsp27 phosphorylation. EMBO J 26: 2240-2250.
12. Evgrafov OV, Mersiyanova I, Irobi J, Van Den Bosch L, Dierick I, Leung CL, Schagina O, Verpoorten N, Van Impe K, Fedotov V, Dadali E, Auer-Grumbach M, Windpassinger C, Wagner K, Mitrovic Z, Hilton-Jones D, Talbot K, Martin JJ, Vasserman N, Tverskaya S, Polyakov A, Liem RK, Gettemans J, Robberecht W, De Jonghe P, Timmerman V. 2004. Mutant small heat-shock protein 27 causes axonal Charcot-Marie-Tooth disease and distal hereditary motor neuropathy. Nat Genet 36: 602-606.
13. Gaestel M. 2006. MAPKAP kinases-MKs-two's company, three's a crowd. Nat Rev Mol Cell Biol 7: 120-130.
14. Gallo G, Letourneau PC. 2004. Regulation of growth cone actin filaments by guidance cues. J Neurobiol 58: 92-102.
15. Garcia MC, Ray DM, Lackford B, Rubino M, Olden K, Roberts JD. 2009. Arachidonic acid stimulates cell adhesion through a novel p38 MAPK-RhoA signaling pathway that involves heat shock protein 27. J Biol Chem 284: 20936-20945.
16. Gehler S, Shaw AE, Sarmiere PD, Bamburg JR, Letourneau PC. 2004. Brain-derived neurotrophic factor regulation of retinal growth cone filopodial dynamics is mediated through actin depolymerizing factor/cofilin. J Neurosci 24: 10741-10749.
17. Gerthoffer WT, Gunst SJ. 2001. Invited review: focal adhesion and small heat shock proteins in the regulation of actin remodeling and contractility in smooth muscle. J Appl Physiol 91: 963-972.
18. Guay J, Lambert H, Gingras-Breton G, Lavoie JN, Huot J, Landry J. 1997. Regulation of actin filament dynamics by p38 map kinase-mediated phosphorylation of heat shock protein 27. J Cell Sci 110: 357-368.
19. Haslbeck M, Franzmann T, Weinfurtner D, Buchner J. 2005. Some like it hot: the structure and function of small heat-shock proteins. Nat Struct Mol Biol 12: 842-846.
20. Hong Z, Zhang QY, Liu J, Wang ZQ, Zhang Y, Xiao Q, Lu J, Zhou HY, Chen SD. 2009. Phosphoproteome study reveals Hsp27 as a novel signaling molecule involved in GDNF-induced neurite outgrowth. JProteome Res 8: 2768-2787.
21. Houlden H, Laura M, Wavrant-De Vrieze F, Blake J, Wood N, Reilly MM. 2008. Mutations in the HSP27 (HSPB1) gene cause dominant, recessive, and sporadic distal HMN/CMT type 2. Neurology 71: 1660-1668.
22. Huot J, Lambert H, Lavoie JN, Guimond A, Houle F, Landry J. 1995. Characterization of 45-kDa/54-kDa HSP27 kinase, a stress-sensitive kinase which may activate the phosphorylation-dependent protective function of mammalian 27-kDa heat-shock protein HSP27. Eur J Biochem 227: 416-427.
23. Huot J, Houle F, Marceau F, Landry J. 1997. Oxidative stress-induced actin reorganization mediated by the p38 mitogen-activated protein kinase/heat shock protein 27 pathway in vascular endothelial cells. Circ Res 80: 383-392.
24. Irobi J, Van Impe K, Seeman P, Jordanova A, Dierick I, Verpoorten N, Michalik A, De Vriendt E, Jacobs A, Van Gerwen V, Vennekens K, Mazanec R, Tournev I, Hilton-Jones D, Talbot K, Kremensky I, Van Den Bosch L, Robberecht W, Van Vandekerckhove J, Van Broeckhoven C, Gettemans J, De Jonghe P, Timmerman V. 2004. Hot-spot residue in small heat-shock protein 22 causes distal motor neuropathy. Nat Genet 36: 597-601.
25. Jia Y, Wu SL, Isenberg JS, Dai S, Sipes JM, Field L, Zeng B, Bandle RW, Ridnour LA, Wink DA, Ramchandran R, Karger BL, Roberts DD. 2010. Thiolutin inhibits endothelial cell adhesion by perturbing Hsp27 interactions with components of the actin and intermediate filament cytoskeleton. Cell Stress Chaperones 15: 165-181.
26. Jones DM, Tucker BA, Rahimtula M, Mearow KM. 2003. The synergistic effects of NGF and IGF-1 on neurite growth in adult sensory neurons: convergence on the PI 3-kinase signaling pathway. J Neurochem 86: 1116-1128.
27. King M, Nafar F, Clarke J, Mearow K. 2009. The small heat shock protein Hsp27 protects cortical neurons against the toxic effects of beta-amyloid peptide. J Neurosci Res 87: 3161-3175.
28. Lambert H, Charette SJ, Bernier AF, Guimond A, Landry J. 1999. HSP27 multimerization mediated by phosphorylation-sensitive intermolecular interactions at the amino terminus. J Biol Chem 274: 9378-9385.
29. Landry J, Lambert H, Zhou M, Lavoie JN, Hickey E, Weber LA, Anderson CW. 1992. Human HSP27 is phosphorylated at serines 78 and 82 by heat shock and mitogen-activated kinases that recognize the same amino acid motif as S6 kinase II. J Biol Chem 267: 794-803.
30. Lavoie JN, Lambert H, Hickey E, Weber LA, Landry J. 1995. Modulation of cellular thermoresistance and actin filament stability accompanies phosphorylation-induced changes in the oligomeric structure of heat shock protein 27. Mol Cell Biol 15: 505-516.
31. Lee JW, Kwak HJ, Lee JJ, Kim YN, Park MJ, Jung SE, Hong SI, Lee JH, Lee JS. 2008. HSP27 regulates cell adhesion and invasion via modulation of focal adhesion kinase and MMP-2 expression. Eur J Cell Biol 87: 377-387.
32. Mehlen P, Arrigo AP. 1994. The serum-induced phosphorylation of mammalian hsp27 correlates with changes in its intracellular localization and levels of oligomerization. Eur J Biochem 221: 327-334.
33. Meijering E, Jacob M, Sarria JC, Steiner P, Hirling H, Unser M. 2004. Design and validation of a tool for neurite tracing and analysis in fluorescence microscopy images. Cytometry A 58: 167-176.
34. 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.
35. Mounier N, Arrigo AP. 2002. Actin cytoskeleton and small heat shock proteins: how do they interact? Cell Stress Chaperones 7: 167-176.
36. Murashov AK, Haq IU, Hill C, Park E, Smith M, Wang X, Goldberg DJ, Wolgemuth DJ. 2001. Crosstalk between p38, Hsp25 and Akt in spinal motor neurons after sciatic nerve injury. Brain Res Mol Brain Res 93: 199-208.
37. Patil SB, Pawar MD, Bitar KN. 2004. Phosphorylated HSP27 essential for acetylcholine-induced association of RhoA with PKCalpha. Am J Physiol Gastrointest Liver Physiol 286: G635-G644.
38. Perng MD, Cairns L, van den IP, Prescott A, Hutcheson AM, Quinlan RA. 1999. Intermediate filament interactions can be altered by HSP27 and alphaB-crystallin. J Cell Sci 112: 2099-2112.
39. Pichon S, Bryckaert M, Berrou E. 2004. Control of actin dynamics by p38 MAP kinase-Hsp27 distribution in the lamellipodium of smooth muscle cells. J Cell Sci 117: 2569-2577.
40. Piotrowicz RS, Hickey E, Levin EG. 1998. Heat shock protein 27 kDa expression and phosphorylation regulates endothelial cell migration. FASEB J 12: 1481-1490.
41. 2-mediated disruption actin cytoskeleton, a protection which appears related to the redox change mediated by Hsp25. Cell Stress Chaperones 3: 177-187.
42. Read DE, Gorman AM. 2009. Heat shock protein 27 in neuronal survival and neurite outgrowth. Biochem Biophys Res Commun 382: 6-8.
43. Rogalla T, Ehrnsperger M, Preville X, Kotlyarov A, Lutsch G, Ducasse C, Paul C, Wieske M, Arrigo AP, Buchner J, Gaestel M. 1999. Regulation of Hsp27 oligomerization, chaperone function, and protective activity against oxidative stress/tumor necrosis factor alpha by phosphorylation. J Biol Chem 274: 18947-18956.
44. Schafer C, Clapp P, Welsh MJ, Benndorf R, Williams JA. 1999. HSP27 expression regulates CCK-induced changes of the actin cytoskeleton in CHO-CCK-A cells. Am J Physiol 277: C1032-C1043.
45. Schneider GB, Hamano H, Cooper LF. 1998. In vivo evaluation of hsp27 as an inhibitor of actin polymerization: hsp27 limits actin stress fiber and focal adhesion formation after heat shock. J Cell Physiol 177: 575-584.
46. Theriault JR, Lambert H, Chavez-Zobel AT, Charest G, Lavigne P, Landry J. 2004. Essential role of the NH2-terminal WD/EPF motif in the phosphorylation-activated protective function of mammalian Hsp27. J Biol Chem 279: 23463-23471.
47. Tradewell ML, Durham HD, Mushynski WE, Gentil BJ. 2009. Mitochondrial and axonal abnormalities precede disruption of the neurofilament network in a model of Charcot-Marie-Tooth disease type 2E and are prevented by heat shock proteins in a mutant-specific fashion. J Neuropathol Exp Neurol 68: 642-652.
48. Tucker BA, Rahimtula M, Mearow KM. 2005a. Integrin activation and neurotrophin signaling cooperate to enhance neurite outgrowth in sensory neurons. J Comp Neurol 486: 267-280.
49. Tucker BA, Rahimtula M, Mearow KM. 2005b. A procedure for selecting and culturing subpopulations of neurons from rat dorsal root ganglia using magnetic beads. Brain Res Brain Res Protoc 16: 50-57.
50. Tucker BA, Rahimtula M, Mearow KM. 2008. Src and FAK are key early signalling intermediates required for neurite growth in NGF-responsive adult DRG neurons. Cell Signal 20: 241-257.
51. van Montfort RL, Basha E, Friedrich KL, Slingsby C, Vierling E. 2001. Crystal structure and assembly of a eukaryotic small heat shock protein. Nat Struct Biol 8: 1025-1030.
52. Vigilanza P, Aquilano K, Rotilio G, Ciriolo MR. 2008. Transient cytoskeletal alterations after SOD1 depletion in neuroblastoma cells. Cell Mol Life Sci 65: 991-1004.
53. Williams KL, Rahimtula M, Mearow KM. 2005. Hsp27 and axonal growth in adult sensory neurons in vitro. BMC Neurosci 6: 24.
54. Williams KL, Rahimtula M, Mearow KM. 2006. Heat shock protein 27 is involved in neurite extension and branching of dorsal root ganglion neurons in vitro. J Neurosci Res 84: 716-723.
55. Zhai J, Lin H, Julien JP, Schlaepfer WW. 2007. Disruption of neurofilament network with aggregation of light neurofilament protein: a common pathway leading to motor neuron degeneration due to Charcot-Marie-Tooth disease-linked mutations in NFL and HSPB1. Hum Mol Genet 16: 3103-3116.