Mechanisms of the motoneuron stress response and its relevance in neurodegeneration

Neurodegeneration: Theory, Disorders and Treatments

Volumn , Issue , 2011, Pages 45-62

  Robinson, Mac B ^a   Gifondorwa, David J ^a   Milligan, Carol ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

Amyotrophic lateral sclerosis; Heat shock protein 70; Heat shock proteins; Motor neuron; Neurodegenerative disease; Stress response

Indexed keywords

EID: 84893449560     PISSN: None     EISSN: None     Source Type: Book    
DOI: None     Document Type: Chapter

References (75)

1. Ahn, S. G. & Thiele, D. J. (2003). Redox regulation of mammalian heat shock factor 1 is essential for Hsp gene activation and protection from stress. Genes Dev, 17, 516-528.
2. Akerfelt, M., Trouillet, A., Mezger, V. & Sistonen. (2007). Heat shock factors at crossroad between stress and development. Ann NY Acad Sci, 1113, 15-27.
3. Arrigo, A. P. (2001). Hsp27: novel regulator of intracellular redox state. IUBMB Life, 52, 303-307.
4. Batulan, Z., Nalbantoglu, J. & Durham, H. D. (2005). Nonsteroidal anti-inflammatory drugs differentially affect the heat shock response in cultured spinal cord cells. Cell Stress Chaperones, 10, 185-196.
5. Batulan, Z., Taylor, D. M., Aarons, R. J., Minotti, S., Doroudchi, M. M., Nalbantoglu, J. & Durham, H. D. (2006). Induction of multiple heat shock proteins and neuroprotection in a primary culture model of familial amyotrophic lateral sclerosis. Neurobiol Dis, 24, 213-225.
6. Batulan, Z., Shinder, G. A., Minotti, S., He, B. P., Doroudchi, M. M., Nalbantoglu, J., Strong, M. J. & Durham, H. D. (2003). High threshold for induction of the stress response in motor neurons is associated with failure to activate HSF1. J Neurosci, 23, 5789-5798.
7. Benatar, M. (2007). Lost in translation: treatment trials in the SOD1 mouse and in human ALS. Neurobiol Dis, 26, 1-13.
8. Bijur, G. N. & Jope, R. S. (2000). Opposing actions of phosphatidylinositol 3-kinase and glycogen synthase kinase-3beta in the regulation of HSF-1 activity. J Neurochem, 75, 2401-2408.
9. Birch-Machin, I., Gao, S., Huen, D., McGirr, R., White, R. A. & Russell, S. (2005). Genomic analysis of heat-shock factor targets in Drosophila. Genome Biol, 6, R63.
10. Boyce, M. & Yuan, J. (2006). Cellular response to endoplasmic reticulum stress: a matter of life or death. Cell Death Diff., 13, 363-373.
11. Brecht, S., Buschmann, T., Grimm, S., Zimmermann, M. & Herdegen, T. (1997). Persisting expression of galanin in axotomized mamillary and septal neurons of adult rats labeled for c-Jun and NADPH-diaphorase. Brain Res Mol Brain Res, 48, 7-16.
12. Bruening, W., Roy, J., Giasson, B., Figlewicz, D. A., Mushynski, W. E. & Durham, H. D. (1999). Up-regulation of protein chaperones preserves viability of cells expressing toxic Cu/Zn-superoxide dismutase mutants associated with amyotrophic lateral sclerosis. In: J Neurochem, 693-699.
13. Gifondorwa, D. J., Robinson, M. B., Hayes, C. D., Taylor, A. R., Prevette, D. M., Oppenheim, R. W., Caress, J. & Milligan, C. E. (2007). Exogenous delivery of heat shock protein 70 increases lifespan in a mouse model of amyotrophic lateral sclerosis. J Neurosci, 27, 13173-13180.
14. Goldbaum, O. & Richter-Landsberg, C. (2001). Stress proteins in oligodendrocytes: differential effects of heat shock and oxidative stress. J Neurochem, 78, 1233-1242.
15. Homma, S., Jin, X., Wang, G., Tu, N., Min, J., Yanasak, N. & Mivechi, N. F. (2007). Demylination, astrogliosis and accumulation of ubiquitinated proteins, hallmoard of CNS disease in hsf1-deficient mice. J. Neurosci., 27, 7974-7986.
16. Jurivich, D. A., Sistonen, L., Kroes, R. A. & Morimoto, R. I. (1992) Effect of sodium salicylate on the human heat shock response. Science, 255, 1243-1245.
17. Kaarniranta, K., Oksala, N., Karjalainen, H. M., Suuronen, T., Sistonen, L., Helminen, H. J., Salminen, A. & Lammi, M. J. (2002) Neuronal cells show regulatory differences in the hsp70 gene response. Brain Res Mol Brain Res, 101, 136-140.
18. Kalmar, B., Burnstock, G., Vrbova, G. & Greensmith, L. (2002). The effect of neonatal nerve injury on the expression of heat shock proteins in developing rat motoneurones. J Neurotrauma, 19, 667-679.
19. Kalmar, B., Novoselov, S., Gray, A., Cheetham, M. E., Margulis, B. & Greensmith, L. (2008). Late stage treatment with arimoclomol delays disease progression and prevents protein aggregation in the SOD1 mouse model of ALS. J Neurochem, 107, 339-350.
20. Kaushik, S. & Cuervo, A. M. (2006). Autophagy as a cell-repair mechanism: activation of chaperone-mediated autophagy during oxidative stress. Mol Aspects Med, 27, 444-454.
21. Kawazoe, Y., Tanabe, M., Sasai, N., Nagata, K. & Nakai, A. (1999). HSF3 is a major heat shock responsive factor duringchicken embryonic development. Eur J Biochem, 265, 688-697.
22. Kieran, D., Kalmar, B., Dick, J. R., Riddoch-Contreras, J., Burnstock, G. & Greensmith, L (2004). Treatment with arimoclomol, a coinducer of heat shock proteins, delays disease progression in ALS mice. Nat Med, 10, 402-405.
23. Kim, Y. H., Park, E. J., Han, S. T., Park, J. W., Kwon, T. K. (2005). Arsenic trioxide induces Hsp70 expression via reactive oxygen species and JNK pathway in MDA231 cells. Life Sci, 77, 2783-2793.
24. Kregel, K. C. (2002). Heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance. J Appl Physiol, 92, 2177-2186.
25. Krishnan, J., Vannuvel, K., Andries, M., Waelkens, E., Robberecht, W. & Van Den Bosch, L. (2008). Over-expression of Hsp27 does not influence disease in the mutant SOD1(G93A) mouse model of amyotrophic lateral sclerosis. J Neurochem, 106, 2170-2183.
26. Lee, J. H. & Schoffl, F. (1996). An Hsp70 antisense gene affects the expression of HSP70/HSC70, the regulation of HSF, and the acquisition of thermotolerance in transgenic Arabidopsis thaliana. Mol Gen Genet, 252, 11-19.
27. Li, L., Oppenheim, R. W. & Milligan, C. E. (2001). Characterization of the execution pathway of developing motoneurons deprived of trophic support. J Neurobiol, 46, 249-264.
28. Lindholm, D., Wootz, H. & Korhonen, L. (2006). ER stress and neurodegenerative diseases. Cell Death and Diff., 13, 385-392.
29. Liu, J., Shinobu, L. A., Ward, C. M., Young, D. & Cleveland, D. W. (2005). Elevation of the Hsp70 chaperone does not effect toxicity in mouse models of familial amyotrophic lateral sclerosis. In: J Neurochem, 875-882.
30. Luders, J., Demand, J. & Hohfeld, J. (2000). The ubiquitin-related BAG-1 provides a link between the molecular chaperones Hsc70/Hsp70 and the proteasome. J Biol Chem, 275, 4613-4617.
31. Maatkamp, A., Vlug, A., Haasdijk, E., Troost, D., French, P. J. & Jaarsma, D. (2004). Decrease of Hsp25 protein expression precedes degeneration of motoneurons in ALS-SOD1 mice. In: Eur J Neurosci, 14-28.
32. Manzerra, P. & Brown, I. R. (1992). Expression of heat shock genes (hsp70) in the rabbit spinal cord: localization of constitutive and hyperthermia-inducible mRNA species. J Neurosci Res, 31, 606-615.
33. Manzerra, P. & Brown, I. R. (1996). The neuronal stress response: nuclear translocation of heat shock proteins as an indicator of hyperthermic stress. Exp Cell Res, 229, 35-47.
34. Marcuccilli, C. J., Mathur, S. K., Morimoto, R. I. & Miller, R. J. (1996). Regulatory differences in the stress response of hippocampal neurons and glial cells after heat shock. J Neurosci, 16, 478-485.
35. Mathur, S. K., Sistonen, L., Brown, I. R., Murphy, S. P., Sarge, K. D. & Morimoto, R. I. (1994). Deficient induction of human hsp70 heat shock gene transcription in Y79 retinoblastoma cells despite activation of heat shock factor 1. Proc Natl Acad Sci, U S A 91, 8695-8699.
36. Morimoto, R. & Fodor, E. (1984). Cell-specific expression of heat shock proteins in chicken reticulocytes and lymphocytes. J Cell Biol, 99, 1316-1323.
37. Morimoto, R. I. (1993). Cells in stress: transcriptional activation of heat shock genes. Science, 259, 1409-1410.
38. Morimoto, R. I., Kline, M. P., Bimston, D. N. & Cotto, J. J. (1997). The heat-shock response: regulation and function of heat-shock proteins and molecular chaperones. Essays Biochem, 32, 17-29.
39. Mosser, D. D., Duchaine, J. & Massie, B. (1993). The DNA-binding activity of the human heat shock transcription factor is regulated in vivo by hsp70. Mol Cell Biol, 13, 5427-5438.
40. Mosser, D. D., Kotzbauer, P. T., Sarge, K. D. & Morimoto, R. I. (1990). In vitro activation of heat shock transcription factor DNA-binding by calcium and biochemical conditions that affect protein conformation. Proc Natl Acad Sci, U S A 87, 3748-3752.
41. Muchowski, P. J. (2002). Protein misfolding, amyloid formation, and neurodegeneration: a critical role for molecular chaperones? Neuron, 35, 9-12.
42. Muchowski, P. J., Schaffar, G., Sittler, A., Wanker, E. E., Hayer-Hartl, M. K. & Hartl, F. U. (2000). Hsp70 and hsp40 chaperones can inhibit self-assembly of polyglutamine proteins into amyloid-like fibrils. Proc Natl Acad Sci, U S A 97, 7841-7846.
43. Murashov, A. K., Ul Haq, I., Hill, C., Park, E., Smith, M., Wang, X., Goldberg, D. J. & Wolgemuth, D. J. (2001). Crosstalk between p38, Hsp25 and Akt in spinal motor neurons after sciatic nerve injury. Brain Res Mol Brain Res, 93, 199-208.
44. Nakai, A., Kawazoe, Y., Tanabe, M., Nagata, K. & Morimoto, R. I. (1995). The DNA-binding properties of two heat shock factors, HSF1 and HSF3, are induced in the avian erythroblast cell line HD6. Mol Cell Biol, 15, 5268-5278.
45. Nover, L., Bharti, K., Doring, P., Mishra, S. K., Ganguli, A. & Scharf, K. D. (2001). Arabidopsis and the heat stress transcription factor world: how many heat stress transcription factors do we need? Cell Stress Chaperones, 6, 177-189.
46. Okado-Matsumoto, A. & Fridovich, I. (2002) Amyotrophic lateral sclerosis: a proposed mechanism. Proc Natl Acad Sci, U S A 99, 9010-9014.
47. Oppenheim, R. W., Haverkamp, L. J., Prevette, D., McManaman, J. L. & Appel, S. H (1988). Reduction of naturally occurring motoneuron death in vivo by a target-derived neurotrophic factor. Science, 240, 919-922.
48. Ostling, P., Bjork, J. K., Roos-Mattjus, P., Mezger, V. & Sistonen, L. (2007). Heat shock factor 2 (HSF2) contributes to inducible expression of hsp genes through interplay with HSF1. J Biol Chem, 282, 7077-7086.
49. Park, J. & Liu, A. Y. (2001). JNK phosphorylates the HSF1 transcriptional activation domain: role of JNK in the regulation of the heat shock response. J Cell Biochem, 82, 326-338.
50. Patel, Y. J., Payne Smith, M. D., de Belleroche, J. & Latchman, D. S. (2005). Hsp27 and Hsp70 administered in combination have a potent protective effect against FALS-associated SOD1-mutant-induced cell death in mammalian neuronal cells. Brain Res Mol Brain Res, 134, 256-274.
51. Pirkkala, L., Nykanen, P. & Sistonen, L. (2001). Roles of the heat shock transcription factors in regulation of the heat shock response and beyond. Faseb J, 15, 1118-1131.
52. Prahlad, V. & Morimoto, R. I. (2009). Integrating the stress response: lessons for neurodegenerative diseases from C. elegans. Trends in Cell Biology, 19, 52-61.
53. Ritossa, F. (1962). A new puffing pattern induced by termperature shock and DNP in Drosophila. Experientia, 15, 571-573.
54. Ritossa, F. (1996). Discovery of the heat shock response. Cell Stress Chaperones, 1, 97-98.
55. Robinson, M. B., Tidwell, J. L., Gould, T., Taylor, A. R., Newbern, J. M., Graves, J., Tytell, M. & Milligan, C. E. (2005). Extracellular heat shock protein 70: a critical component for motoneuron survival. J Neurosci, 25, 9735-9745.
56. Salehi, A. H., Morris, S. J., Ho, W. C., Dickson, K. M., Doucet, G., Milutinovic, S., Durkin, J., Gillard, J. W. & Barker, P. A. (2006). AEG3482 is an antiapoptotic compound that inhibits Jun kinase activity and cell death through induced expression of heat shock protein 70. Chem Biol, 13, 213-223.
57. Santoro, M. G. (2000). Heat shock factors and the control of the stress response. Biochem Pharmacol, 59, 55-63.
58. Satyal, S. H., Chen, D., Fox, S. G., Kramer, J. M. & Morimoto, R. I. (1998). Negative regulation of the heat shock transcriptional response by HSBP1. Genes Dev, 12, 1962-1974.
59. Schlesinger, M. J. (1990). Heat shock proteins. J Biol Chem, 265, 12111-12114.
60. Shabtay, A. & Arad, Z. (2006). Reciprocal activation of HSF1 and HSF3 in brain and blood tissues: is redundancy developmentally related? Am J Physiol Regul Integr Comp Physiol, 291, R566-572.
61. Sharp, F. R., Massa, S. M. & Swanson, R. A. (1999). Heat-shock protein protection. In: Trends Neurosci, 97-99.
62. Shaw, P. J. & Eggett, C. J. (2000). Molecular factors underlying selective vulnerability of motor neurons to neurodegeneration in amyotrophic lateral sclerosis. J Neurol, 247, Suppl 1, I17-27.
63. Soncin, F., Asea, A., Zhang, X., Stevenson, M. A. & Calderwood, S. K. (2000). Role of calcium activated kinases and phosphatases in heat shock factor-1 activation. Int J Mol Med, 6, 705-710.
64. Strey, C. W., Spellman, D., Stieber, A., Gonatas, J. O., Wang, X., Lambris, J. D. & Gonatas, N. K. (2004). Dysregulation of stathmin, a microtubule-destabilizing protein, and up-regulation of Hsp25, Hsp27, and the antioxidant peroxiredoxin 6 in a mouse model of familial amyotrophic lateral sclerosis. In: Am J Pathol, 1701-1718.
65. Tacchini, L., Pogliaghi, G., Radice, L., Anzon, E. & Bernelli-Zazzera, A. (1995). Differential activation of heat-shock and oxidation-specific stress genes in chemically induced oxidative stress. Biochem J, 309, 453-459.
66. Tanabe, M., Kawazoe, Y., Takeda, S., Morimoto, R. I., Nagata, K. & Nakai, A. (1998). Disruption of the HSF3 gene results in the severe reduction of heat shock gene expression and loss of thermotolerance. Embo J, 17, 1750-1758.
67. Taylor, D. M., De Koninck, P., Minotti, S. & Durham, H. D. (2007). Manipulation of protein kinases reveals different mechanisms for upregulation of heat shock proteins in motor neurons and non-neuronal cells. Mol Cell Neurosci, 34, 20-33.
68. Tidwell, J. L., Houenou, L. J. & Tytell, M. (2004). Administration of Hsp70 in vivo inhibits motor and sensory neuron degeneration. Cell Stress Chaperones, 9, 88-98.
69. Welch, W. J. (1992). Mammalian stress response: cell physiology, structure/function of stress proteins, and implications for medicine and disease. Physiol Rev, 72, 1063-1081.
70. Xiao, X. Z., Zuo, X. X., Davis, A. A., McMillan, D. R., Curry, B. B., Richardon, J. A. & Benjamin, I. J. (1999). HSF1 is required for extra-embryonic development, postnatal growth and protection during inflammatory responses in mice. EMBO J., 18, 5943-5942.
71. Yamamoto, N., Takemori, Y., Sakurai, M., Sugiyama, K. & Sakurai, H. (2009). Differential recognition of heath shock elements by members of the heat shock transcription factor family. FEBS J., 276, 1962-1974.
72. Yamashita, H., Kawamata, J., Okawa, K., Kanki, R., Nakamizo, T., Hatayama, T., Yamanaka, K., Takahashi, R. & Shimohama, S. (2007). Heat-shock protein 105 interacts with and suppresses aggregation of mutant Cu/Zn superoxide dismutase: clues to a possible strategy for treating ALS. In: J Neurochem.
73. Yang, J., Bridges, K., Chen, K. Y. & Liu, A. Y. (2008). Riluzole increases the amount of latent HSF1 for an amplified heat shock response and cytoprotection. PLoS ONE, 3:e2864.
74. Yang, Y., Xie, Y., Chai, H., Fan, M., Liu, S., Liu, H., Bruce, I. & Wu, W. (2006). Microarray analysis of gene expression patterns in adult spinal motoneurons after different types of axonal injuries. Brain Res, 1075, 1-12.
75. Zhong, M., Orosz, A. & Wu, C. (1998). Direct sensing of heat and oxidation by Drosophila heat shock transcription factor. Mol Cell, 2, 101-108.