Abstract
Amyotrophic Lateral Sclerosis (ALS) is a complex neurodegenerative disease in which multiple cell types and cellular pathways play a role. A pathological hallmark of neurodegenerative disorders, including ALS, is the presence of intracellular aggregates. Heat Shock Proteins (Hsp) are a family of protein chaperones that normally play a key role in protein homeostasis, acting to prevent aggregation of misfolded proteins. In ALS, Hsp are sequestered into aggregates, creating a cytosolic deficit in Hsp availability and function, thereby reducing their ability to respond to cell stress and prevent aggregation of misfolded proteins. Furthermore, not only is the neuronal support normally provided by surrounding glial cells lost ALS, but glia actively contribute towards motor neuron degeneration. Here, we discuss the possibility that dysfunction of Hsp in glia may contribute to non-cell autonomous mechanisms of motor neuron death in ALS, for example by exacerbating inflammatory signalling in glia. Since motor neurons are unable to upregulate Hsp in response to stress, it is possible they rely on surrounding glia to provide them with Hsp, and this support may be lost in ALS. Therefore, therapeutic approaches that augment Hsp levels may have neuroprotective effects on motor neurons and may correct ALS-induced deficits in glia.
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Abbreviations
- ALS:
-
amyotrophic lateral sclerosis
- FUS:
-
fused in sarcoma protein
- HSF-1:
-
heat shock factor-1
- Hsp:
-
heat shock protein and heat shock proteins
- HSR:
-
heat shock response
- NF-κB:
-
nuclear factor kappa-light-chain-enhancer of activated B cells
- SOD1:
-
superoxide dismutase-1
- TDP-43:
-
transactive response DNA binding protein 43 kDa
References
Ahmed M, Machado PM, Miller A, Spicer C, Herbelin L, He JH et al (2016) Targeting protein homeostasis in sporadic inclusion body myositis. Sci Transl Med 8:331).. ARTN 331ra41. https://doi.org/10.1126/scitranslmed.aad4583
Akerfelt M, Morimoto RI, Sistonen L (2010) Heat shock factors: integrators of cell stress, development and lifespan. Nat Rev Mol Cell Biol 11(8):545–555. https://doi.org/10.1038/nrm2938
Al-Chalabi A, van den Berg LH, Veldink J (2017) Gene discovery in amyotrophic lateral sclerosis: implications for clinical management. Nat Rev Neurol 13(2):96–104. https://doi.org/10.1038/nrneurol.2016.182
Alexianu ME, Kozovska M, Appel SH (2001) Immune reactivity in a mouse model of familial ALS correlates with disease progression. Neurology 57(7):1282–1289
Almer G, Guegan C, Teismann P, Naini A, Rosoklija G, Hays AP et al (2001) Increased expression of the pro-inflammatory enzyme cyclooxygenase-2 in amyotrophic lateral sclerosis. Ann Neurol 49(2):176–185
Barreto GE, White RE, Xu LJ, Palm CJ, Giffard RG (2012) Effects of heat shock protein 72 (Hsp72) on evolution of astrocyte activation following stroke in the mouse. Exp Neurol 238(2):284–296. https://doi.org/10.1016/j.expneurol.2012.08.015
Batulan Z, Shinder GA, Minotti S, He BP, Doroudchi MM, Nalbantoglu J et al (2003) High threshold for induction of the stress response in motor neurons is associated with failure to activate HSF1. J Neurosci 23(13):5789–5798
Benatar M, Wuu J, Andersen PM, Atassi N, David W, Cudkowicz M, Schoenfeld D (2018) Randomized, double-blind, placebo-controlled trial of arimoclomol in rapidly progressive SOD1 ALS. Neurology 90(7):E565–E574. https://doi.org/10.1212/Wnl.0000000000004960
Bilsland LG, Nirmalananthan N, Yip J, Greensmith L, Duchen MR (2008) Expression of mutant SOD1 in astrocytes induces functional deficits in motoneuron mitochondria. J Neurochem 107(5):1271–1283. https://doi.org/10.1111/j.1471-4159.2008.05699.x
Boillee S, Yamanaka K, Lobsiger CS, Copeland NG, Jenkins NA, Kassiotis G et al (2006) Onset and progression in inherited ALS determined by motor neurons and microglia. Science 312(5778):1389–1392. https://doi.org/10.1126/science.1123511
Boisvert MM, Erikson GA, Shokhirev MN, Allen NJ (2018) The aging astrocyte transcriptome from multiple regions of the mouse brain. Cell Rep 22(1):269–285. https://doi.org/10.1016/j.celrep.2017.12.039
Brehme M, Voisine C, Rolland T, Wachi S, Soper JH, Zhu Y et al (2014) A chaperome subnetwork safeguards proteostasis in aging and neurodegenerative disease. Cell Rep 9(3):1135–1150. https://doi.org/10.1016/j.celrep.2014.09.042
Bruening W, Roy J, Giasson B, Figlewicz DA, Mushynski WE, Durham HD (1999) Up-regulation of protein chaperones preserves viability of cells expressing toxic Cu/Zn-superoxide dismutase mutants associated with amyotrophic lateral sclerosis. J Neurochem 72(2):693–699. https://doi.org/10.1046/j.1471-4159.1999.0720693.x
Bruijn LI, Becher MW, Lee MK, Anderson KL, Jenkins NA, Copeland NG et al (1997) ALS-linked SOD1 mutant G85R mediates damage to astrocytes and promotes rapidly progressive disease with SOD1-containing inclusions. Neuron 18(2):327–338
Calderwood SK, Murshid A (2017) Molecular chaperone accumulation in cancer and decrease in Alzheimer’s disease: the potential roles of HSF1. Front Neurosci 11.. ARTN:192. https://doi.org/10.3389/fnins.2017.00192
Casciati A, Ferri A, Cozzolino M, Celsi F, Nencini M, Rotilio G, Carri MT (2002) Oxidative modulation of nuclear factor-kappaB in human cells expressing mutant fALS-typical superoxide dismutases. J Neurochem 83(5):1019–1029
Chen HQ, Wu YF, Zhang YQ, Jin LN, Luo L, Xue B et al (2006) Hsp70 inhibits lipopolysaccharide-induced NF-kappa B activation by interacting with TRAF6 and inhibiting its ubiquitination. FEBS Lett 580(13):3145–3152. https://doi.org/10.1016/j.febslet.2006.04.066
Chen HJ, Mitchell JC, Novoselov S, Miller J, Nishimura AL, Scotter EL et al (2016) The heat shock response plays an important role in TDP-43 clearance: evidence for dysfunction in amyotrophic lateral sclerosis. Brain 139:1417–1432. https://doi.org/10.1093/brain/aww028
Clement AM, Nguyen MD, Roberts EA, Garcia ML, Boillee S, Rule M et al (2003) Wild-type nonneuronal cells extend survival of SOD1 mutant motor neurons in ALS mice. Science 302(5642):113–117. https://doi.org/10.1126/science.1086071
Courgeon AM, Maisonhaute C, Bestbelpomme M (1984) Heat-shock proteins are induced by cadmium in drosophila cells. Exp Cell Res 153(2):515–521. https://doi.org/10.1016/0014-4827(84)90618-9
Coyne AN, Lorenzini I, Chou CC, Torvund M, Rogers RS, Starr A et al (2017) Post-transcriptional inhibition of Hsc70-4/HSPA8 expression leads to synaptic vesicle cycling defects in multiple models of ALS. Cell Rep 21(1):110–125. https://doi.org/10.1016/j.celrep.2017.09.028
Crosio C, Valle C, Casciati A, Iaccarino C, Carri MT (2011) Astroglial inhibition of NF-kappaB does not ameliorate disease onset and progression in a mouse model for amyotrophic lateral sclerosis (ALS). PLoS One 6(3):e17187. https://doi.org/10.1371/journal.pone.0017187
Curry HA, Clemens RA, Shah S, Bradbury CM, Botero A, Goswami P, Gius D (1999) Heat shock inhibits radiation-induced activation of NF-kappa B via inhibition of I-kappa B kinase. J Biol Chem 274(33):23061–23067. https://doi.org/10.1074/jbc.274.33.23061
DeJesus-Hernandez M, Mackenzie IR, Boeve BF, Boxer AL, Baker M, Rutherford NJ et al (2011) Expanded GGGGCC hexanucleotide repeat in noncoding region of C9ORF72 causes chromosome 9p-linked FTD and ALS. Neuron 72(2):245–256. https://doi.org/10.1016/j.neuron.2011.09.011
Dokladny K, Zuhl MN, Mandell M, Bhattacharya D, Schneider S, Deretic V, Moseley PL (2013) Regulatory coordination between two major intracellular homeostatic systems: heat shock response and autophagy. J Biol Chem 288(21):14959–14972. https://doi.org/10.1074/jbc.M113.462408
Feinstein DL, Galea E, Aquino DA, Li GC, Xu H, Reis DJ (1996) Heat shock protein 70 suppresses astroglial-inducible nitric-oxide synthase expression by decreasing NF kappa B activation. J Biol Chem 271(30):17724–17732. https://doi.org/10.1074/jbc.271.30.17724
Ferraiuolo L, Higginbottom A, Heath PR, Barber S, Greenald D, Kirby J, Shaw PJ (2011) Dysregulation of astrocyte-motoneuron cross-talk in mutant superoxide dismutase 1-related amyotrophic lateral sclerosis. Brain 134:2627–2641. https://doi.org/10.1093/brain/awr193
Finka A, Goloubinoff P (2013) Proteomic data from human cell cultures refine mechanisms of chaperone-mediated protein homeostasis. Cell Stress Chaperones 18(5):591–605. https://doi.org/10.1007/s12192-013-0413-3
Frakes AE, Ferraiuolo L, Haidet-Phillips AM, Schmelzer L, Braun L, Miranda CJ et al (2014) Microglia induce motor neuron death via the classical NF-kappa B pathway in amyotrophic lateral sclerosis. Neuron 81(5):1009–1023. https://doi.org/10.1016/j.neuron.2014.01.013
Garofalo O, Kennedy PGE, Swash M, Martin JE, Luthert P, Anderton BH, Leigh PN (1991) Ubiquitin and heat-shock protein expression in amyotrophic-lateral-sclerosis. Neuropathol Appl Neurobiol 17(1):39–45. https://doi.org/10.1111/j.1365-2990.1991.tb00692.x
Gifondorwa DJ, Robinson MB, Hayes CD, Taylor AR, Prevette DM, Oppenheim RW et al (2007) Exogenous delivery of heat shock protein 70 increases lifespan in a mouse model of amyotrophic lateral sclerosis. J Neurosci 27(48):13173–13180. https://doi.org/10.1523/Jneurosci.4057-07.2007
Gurney ME, Pu HF, Chiu AY, Dalcanto MC, Polchow CY, Alexander DD et al (1994) Motor-neuron degeneration in mice that express a human Cu,Zn superoxide-dismutase mutation. Science 264(5166):1772–1775. https://doi.org/10.1126/science.8209258
Guzhova IV, Darieva ZA, Melo AR, Margulis BA (1997) Major stress protein Hsp70 interacts with NF-kB regulatory complex in human T-lymphoma cells. Cell Stress Chaperones 2(2):132–139. https://doi.org/10.1379/1466-1268(1997)002<0132:Msphiw>2.3.Co;2
Guzhova I, Kislyakova K, Moskaliova O, Fridlanskaya I, Tytell M, Cheetham M, Margulis B (2001) In vitro studies show that Hsp70 can be released by glia and that exogenous Hsp70 can enhance neuronal stress tolerance. Brain Res 914(1–2):66–73
Haidet-Phillips AM, Hester ME, Miranda CJ, Meyer K, Braun L, Frakes A et al (2011) Astrocytes from familial and sporadic ALS patients are toxic to motor neurons. Nat Biotechnol 29(9):824–828. https://doi.org/10.1038/nbt.1957
Hall ED, Oostveen JA, Gurney ME (1998) Relationship of microglial and astrocytic activation to disease onset and progression in a transgenic model of familial ALS. Glia 23(3):249–256
Hardiman O, Al-Chalabi A, Chio A, Corr EM, Logroscino G, Robberecht W et al (2017) Amyotrophic lateral sclerosis. Nat Rev Dis Primers 3:17085. https://doi.org/10.1038/nrdp.2017.85
Hargitai J, Lewis H, Boros I, Racz T, Fiser A, Kurucz I et al (2003) Bimoclomol, a heat shock protein co-inducer, acts by the prolonged activation of heat shock factor-1. Biochem Biophys Res Commun 307(3):689–695. https://doi.org/10.1016/S0006-291x(03)01254-3
Hegedus J, Putman CT, Tyreman N, Gordon T (2008) Preferential motor unit loss in the SOD1(G93A) transgenic mouse model of amyotrophic lateral sclerosis. J Physiol-Lond 586(14):3337–3351. https://doi.org/10.1113/jphysiol.2007.149286
Heneka MT, Sharp A, Klockgether T, Gavrilyuk V, Feinstein DL (2000) The heat shock response inhibits NF-kappaB activation, nitric oxide synthase type 2 expression, and macrophage/microglial activation in brain. J Cereb Blood Flow Metab 20(5):800–811. https://doi.org/10.1097/00004647-200005000-00006
Hensley K, Fedynyshyn J, Ferrell S, Floyd RA, Gordon B, Grammas P et al (2003) Message and protein-level elevation of tumor necrosis factor alpha (TNF alpha) and TNF alpha-modulating cytokines in spinal cords of the G93A-SOD1 mouse model for amyotrophic lateral sclerosis. Neurobiol Dis 14(1):74–80
Ialenti A, Di Meglio P, D'Acquisto F, Pisano B, Maffia P, Grassia G et al (2005) Inhibition of cyclooxygenase-2 gene expression by the heat shock response in J774 murine macrophages. Eur J Pharmacol 509(2–3):89–96. https://doi.org/10.1016/j.ejphar.2004.10.052
Ikiz B, Alvarez MJ, Re DB, Le Verche V, Politi K, Lotti F et al (2015) The regulatory machinery of neurodegeneration in in vitro models of amyotrophic lateral sclerosis. Cell Rep 12(2):335–345. https://doi.org/10.1016/j.celrep.2015.06.019
Kalmar B, Greensmith L (2017) Cellular chaperones as therapeutic targets in ALS to restore protein homeostasis and improve cellular function. Front Mol Neurosci 10.. ARTN:251. https://doi.org/10.3389/fnmol.2017.00251
Kalmar B, Burnstock G, Vrbova G, Urbanics R, Csermely P, Greensmith L (2002) Upregulation of heat shock proteins rescues motoneurones from axotomy-induced cell death in neonatal rats. Exp Neurol 176(1):87–97. https://doi.org/10.1006/exnr.2002.7945
Kalmar B, Novoselov S, Gray A, Cheetham ME, 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(2):339–350. https://doi.org/10.1111/j.1471-4159.2008.05595.x
Kalmar B, Lu CH, Greensmith L (2014) The role of heat shock proteins in amyotrophic lateral sclerosis: the therapeutic potential of Arimoclomol. Pharmacol Ther 141(1):40–54. https://doi.org/10.1016/j.pharmthera.2013.08.003
Kato S, Hayashi H, Nakashima K, Nanba E, Kato M, Hirano A et al (1997) Pathological characterization of astrocytic hyaline inclusions in familial amyotrophic lateral sclerosis. Am J Pathol 151(2):611–620
Kelley KW, Ben Haim L, Schirmer L, Tyzack GE, Tolman M, Miller JG et al (2018) Kir4.1-dependent astrocyte-fast motor neuron interactions are required for peak strength. Neuron 98(2):306–319.e7. https://doi.org/10.1016/j.neuron.2018.03.010
Kennedy D, Jager R, Mosser DD, Samali A (2014) Regulation of apoptosis by heat shock proteins. IUBMB Life 66(5):327–338. https://doi.org/10.1002/iub.1274
Kieran D, Kalmar B, Dick JR, 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(4):402–405. https://doi.org/10.1038/nm1021
Kwiatkowski TJ Jr, Bosco DA, Leclerc AL, Tamrazian E, Vanderburg CR, Russ C et al (2009) Mutations in the FUS/TLS gene on chromosome 16 cause familial amyotrophic lateral sclerosis. Science 323(5918):1205–1208. https://doi.org/10.1126/science.1166066
Leak RK (2014) Heat shock proteins in neurodegenerative disorders and aging. J Cell Commun Signal 8(4):293–310. https://doi.org/10.1007/s12079-014-0243-9
Lee YS, Song YS, Giffard RG, Chan PH (2006) Biphasic role of nuclear factor-kappa B on cell survival and COX-2 expression in SOD1 Tg astrocytes after oxygen glucose deprivation. J Cereb Blood Flow Metab 26(8):1076–1088. https://doi.org/10.1038/sj.jcbfm.9600261
Leigh PN, Whitwell H, Garofalo O, Buller J, Swash M, Martin JE et al (1991) Ubiquitin-immunoreactive intraneuronal inclusions in amyotrophic-lateral-sclerosis – morphology, distribution, and specificity. Brain 114:775–788. https://doi.org/10.1093/brain/114.2.775
Liao J, Lowthert LA, Ghori N, Omary MB (1995) The 70-Kda heat-shock proteins associate with glandular intermediate filaments in an Atp-dependent manner. J Biol Chem 270(2):915–922. https://doi.org/10.1074/jbc.270.2.915
Lindquist S (1986) The heat-shock response. Annu Rev Biochem 55:1151–1191. https://doi.org/10.1146/annurev.bi.55.070186.005443
Liu J, Shinobu LA, Ward CM, Young D, Cleveland DW (2005) Elevation of the Hsp70 chaperone does not effect toxicity in mouse models of familial amyotrophic lateral sclerosis. J Neurochem 93(4):875–882. https://doi.org/10.1111/j.1471-4159.2005.03054.x
Lopez-Erauskin J, Tadokoro T, Baughn MW, Myers B, McAlonis-Downes M, Chillon-Marinas C et al (2018) ALS/FTD-linked mutation in FUS suppresses intra-axonal protein synthesis and drives disease without nuclear loss-of-function of FUS. Neuron 100:816. https://doi.org/10.1016/j.neuron.2018.09.044
Madji Hounoum B, Mavel S, Coque E, Patin F, Vourc'h P, Marouillat S et al (2017) Wildtype motoneurons, ALS-linked SOD1 mutation and glutamate profoundly modify astrocyte metabolism and lactate shuttling. Glia 65(4):592–605. https://doi.org/10.1002/glia.23114
Malhotra V, Wong HR (2002) Interactions between the heat shock response and the nuclear factor-kappa B signaling pathway. Crit Care Med 30(1):S89–S95. https://doi.org/10.1097/00003246-200201001-00012
Malik B, Nirmalananthan N, Gray AL, La Spada AR, Hanna MG, Greensmith L (2013) Co-induction of the heat shock response ameliorates disease progression in a mouse model of human spinal and bulbar muscular atrophy: implications for therapy. Brain 136:926–943. https://doi.org/10.1093/brain/aws343
Marchetto MC, Muotri AR, Mu Y, Smith AM, Cezar GG, Gage FH (2008) Non-cell-autonomous effect of human SOD1 G37R astrocytes on motor neurons derived from human embryonic stem cells. Cell Stem Cell 3(6):649–657. https://doi.org/10.1016/j.stem.2008.10.001
Marcuccilli CJ, Mathur SK, Morimoto RI, Miller RJ (1996) Regulatory differences in the stress response of hippocampal neurons and glial cells after heat shock. J Neurosci 16(2):478–485
Matsumoto G, Stojanovic A, Holmberg CI, Kim S, Morimoto RI (2005) Structural properties and neuronal toxicity of amyotrophic lateral sclerosis-associated Cu/Zn superoxide dismutase 1 aggregates. J Cell Biol 171(1):75–85. https://doi.org/10.1083/jcb.200504050
Meissner F, Molawi K, Zychlinsky A (2010) Mutant superoxide dismutase 1-induced IL-1beta accelerates ALS pathogenesis. Proc Natl Acad Sci U S A 107(29):13046–13050. https://doi.org/10.1073/pnas.1002396107
Migheli A, Piva R, Atzori C, Troost D, Schiffer D (1997) c-Jun, JNK/SAPK kinases and transcription factor NF-kappa B are selectively activated in astrocytes, but not motor neurons, in amyotrophic lateral sclerosis. J Neuropathol Exp Neurol 56(12):1314–1322
Mordes DA, Prudencio M, Goodman LD, Klim JR, Moccia R, Limone F et al (2018) Dipeptide repeat proteins activate a heat shock response found in C9ORF72-ALS/FTLD patients. Acta Neuropathol Commun 6.. ARTN:55. https://doi.org/10.1186/s40478-018-0555-8
Morimoto RI (1998) Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev 12(24):3788–3796. https://doi.org/10.1101/gad.12.24.3788
Mosser DD, Kotzbauer PT, Sarge KD, Morimoto RI (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(10):3748–3752
Nagai M, Re DB, Nagata T, Chalazonitis A, Jessell TM, Wichterle H, Przedborski S (2007) Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons. Nat Neurosci 10(5):615–622. https://doi.org/10.1038/nn1876
Neef DW, Turski ML, Thiele DJ (2010) Modulation of heat shock transcription factor 1 as a therapeutic target for small molecule intervention in neurodegenerative disease. PLoS Biol 8(1).. ARTN):e1000291. https://doi.org/10.1371/journal.pbio.1000291
Neumann M, Sampathu DM, Kwong LK, Truax AC, Micsenyi MC, Chou TT et al (2006) Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 314(5796):130–133. https://doi.org/10.1126/science.1134108
Nishimura RN, Dwyer BE, Clegg K, Cole R, de Vellis J (1991) Comparison of the heat shock response in cultured cortical neurons and astrocytes. Brain Res Mol Brain Res 9(1–2):39–45
Okado-Matsumoto A, Fridovich I (2002) Amyotrophic lateral sclerosis: a proposed mechanism. Proc Natl Acad Sci U S A 99(13):9010–9014. https://doi.org/10.1073/pnas.132260399
Ouali Alami N, Schurr C, Olde Heuvel F, Tang L, Li Q, Tasdogan A et al (2018) NF-kappaB activation in astrocytes drives a stage-specific beneficial neuroimmunological response in ALS. EMBO J 37:pii: e98697. https://doi.org/10.15252/embj.201798697
Papadeas ST, Kraig SE, O'Banion C, Lepore AC, Maragakis NJ (2011) Astrocytes carrying the superoxide dismutase 1 (SOD1G93A) mutation induce wild-type motor neuron degeneration in vivo. Proc Natl Acad Sci U S A 108(43):17803–17808. https://doi.org/10.1073/pnas.1103141108
Park KJ, Gaynor RB, Kwak YT (2003) Heat shock protein 27 association with the I kappa B kinase complex regulates tumor necrosis factor alpha-induced NF-kappa B activation. J Biol Chem 278(37):35272–35278. https://doi.org/10.1074/jbc.M305095200
Pellerin L, Bouzier-Sore AK, Aubert A, Serres S, Merle M, Costalat R, Magistretti PJ (2007) Activity-dependent regulation of energy metabolism by astrocytes: an update. Glia 55(12):1251–1262. https://doi.org/10.1002/glia.20528
Philips T, Rothstein JD (2014) Glial cells in amyotrophic lateral sclerosis. Exp Neurol 262:111–120. https://doi.org/10.1016/j.expneurol.2014.05.015
Pittet JF, Lee H, Pespeni M, O'Mahony A, Roux J, Welch WJ (2005) Stress-induced inhibition of the NF-kappaB signaling pathway results from the insolubilization of the IkappaB kinase complex following its dissociation from heat shock protein 90. J Immunol 174(1):384–394
Ran R, Lu A, Zhang L, Tang Y, Zhu H, Xu H et al (2004) Hsp70 promotes TNF-mediated apoptosis by binding IKK gamma and impairing NF-kappa B survival signaling. Genes Dev 18(12):1466–1481. https://doi.org/10.1101/gad.1188204
Re DB, Le Verche V, Yu C, Amoroso MW, Politi KA, Phani S et al (2014) Necroptosis drives motor neuron death in models of both sporadic and familial ALS. Neuron 81(5):1001–1008. https://doi.org/10.1016/j.neuron.2014.01.011
Renton AE, Majounie E, Waite A, Simon-Sanchez J, Rollinson S, Gibbs JR et al (2011) A hexanucleotide repeat expansion in C9ORF72 is the cause of chromosome 9p21-linked ALS-FTD. Neuron 72(2):257–268. https://doi.org/10.1016/j.neuron.2011.09.010
Rice JW, Veal JM, Fadden RP, Barabasz AF, Partridge JM, Barta TE et al (2008) Small molecule inhibitors of Hsp90 potently affect inflammatory disease pathways and exhibit activity in models of rheumatoid arthritis. Arthritis Rheum 58(12):3765–3775. https://doi.org/10.1002/art.24047
Richter K, Haslbeck M, Buchner J (2010) The heat shock response: life on the verge of death. Mol Cell 40(2):253–266. https://doi.org/10.1016/j.molcel.2010.10.006
Ritossa F (1962) New puffing pattern induced by temperature shock and dnp in drosophila. Experientia 18(12):571–573. https://doi.org/10.1007/Bf02172188
Robinson MB, Tidwell JL, Gould T, Taylor AR, Newbern JM, Graves J et al (2005) Extracellular heat shock protein 70: a critical component for motoneuron survival. J Neurosci 25(42):9735–9745. https://doi.org/10.1523/JNEUROSCI.1912-05.2005
Rosen DR (1993) Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 364(6435):362. https://doi.org/10.1038/364362c0
Rothstein JD, Vankammen M, Levey AI, Martin LJ, Kuncl RW (1995) Selective loss of glial glutamate transporter Glt-1 in amyotrophic-lateral-sclerosis. Ann Neurol 38(1):73–84. https://doi.org/10.1002/ana.410380114
Sako W, Ito H, Yoshida M, Koizumi H, Kamada M, Fujita K et al (2012) Nuclear factor kappa B expression in patients with sporadic amyotrophic lateral sclerosis and hereditary amyotrophic lateral sclerosis with optineurin mutations. Clin Neuropathol 31(6):418–423. https://doi.org/10.5414/NP300493
Sala AJ, Bott LC, Morimoto RI (2017) Shaping proteostasis at the cellular, tissue, and organismal level. J Cell Biol 216(5):1231–1241. https://doi.org/10.1083/jcb.201612111
San Gil R, Ooi L, Yerbury JJ, Ecroyd H (2017) The heat shock response in neurons and astroglia and its role in neurodegenerative diseases. Mol Neurodegener 12(1):65. https://doi.org/10.1186/s13024-017-0208-6
Sasaki S, Warita H, Abe K, Iwata M (2001) Inducible nitric oxide synthase (iNOS) and nitrotyrosine immunoreactivity in the spinal cords of transgenic mice with a G93A mutant SOD1 gene. J Neuropathol Exp Neurol 60(9):839–846
Sato K, Matsuki N (2002) A 72 kDa heat shock protein is protective against the selective vulnerability of CA1 neurons and is essential for the tolerance exhibited by CA3 neurons in the hippocampus. Neuroscience 109(4):745–756.. Pii S0306-4522(01)00494-8. https://doi.org/10.1016/S0306-4522(01)00494-8
Sevin M, Girodon F, Garrido C, de Thonel A (2015) HSP90 and HSP70: implication in inflammation processes and therapeutic approaches for myeloproliferative neoplasms. Mediat Inflamm 2015:970242. https://doi.org/10.1155/2015/970242
Sharp PS, Dick JR, Greensmith L (2005) The effect of peripheral nerve injury on disease progression in the SOD1(G93A) mouse model of amyotrophic lateral sclerosis. Neuroscience 130(4):897–910. https://doi.org/10.1016/j.neuroscience.2004.09.069
Sharp PS, Akbar MT, Bouri S, Senda A, Joshi K, Chen HJ et al (2008) Protective effects of heat shock protein 27 in a model of ALS occur in the early stages of disease progression. Neurobiol Dis 30(1):42–55. https://doi.org/10.1016/j.nbd.2007.12.002
Sheppard PW, Sun XY, Khammash M, Giffard RG (2014) Overexpression of heat shock protein 72 attenuates NF-kappa B activation using a combination of regulatory mechanisms in microglia. PLoS Comput Biol 10(2):e1003471. https://doi.org/10.1371/journal.pcbi.1003471
Shinder GA, Lacourse MC, Minotti S, Durham HD (2001) Mutant Cu/Zn-superoxide dismutase proteins have altered solubility and interact with heat shock/stress proteins in models of amyotrophic lateral sclerosis. J Biol Chem 276(16):12791–12796. https://doi.org/10.1074/jbc.M010759200
Spierings J, van Eden W (2017) Heat shock proteins and their immunomodulatory role in inflammatory arthritis. Rheumatology 56(2):198–208. https://doi.org/10.1093/rheumatology/kew266
Sreedharan J, Blair IP, Tripathi VB, Hu X, Vance C, Rogelj B et al (2008) TDP-43 mutations in familial and sporadic amyotrophic lateral sclerosis. Science 319(5870):1668–1672. https://doi.org/10.1126/science.1154584
Sulejczak D, Chrapusta SJ, Dziewulska D, Rafalowska J (2015) NF-kappaB deficit in spinal motoneurons in patients with sporadic amyotrophic lateral sclerosis–a pilot study. Folia Neuropathol 53(4):367–376
Taylor JP, Brown RH Jr, Cleveland DW (2016) Decoding ALS: from genes to mechanism. Nature 539(7628):197–206. https://doi.org/10.1038/nature20413
Trautinger F, KindasMugge I, Knobler RM, Honigsmann H (1996) Stress proteins in the cellular response to ultraviolet radiation. J Photochem Photobiol B-Biol 35(3):141–148. https://doi.org/10.1016/S1011-1344(96)07344-7
Tripathi P, Rodriguez-Muela N, Klim JR, de Boer AS, Agrawal S, Sandoe J et al (2017) Reactive astrocytes promote ALS-like degeneration and intracellular protein aggregation in human motor neurons by disrupting autophagy through TGF-beta1. Stem Cell Rep 9(2):667–680. https://doi.org/10.1016/j.stemcr.2017.06.008
Tummala H, Jung C, Tiwari A, Higgins CM, Hayward LJ, Xu Z (2005) Inhibition of chaperone activity is a shared property of several Cu,Zn-superoxide dismutase mutants that cause amyotrophic lateral sclerosis. J Biol Chem 280(18):17725–17731. https://doi.org/10.1074/jbc.M501705200
Tytell M, Greenberg SG, Lasek RJ (1986) Heat shock-like protein is transferred from glia to axon. Brain Res 363(1):161–164. https://doi.org/10.1016/0006-8993(86)90671-2
Tyzack GE, Hall CE, Sibley CR, Cymes T, Forostyak S, Carlino G et al (2017) A neuroprotective astrocyte state is induced by neuronal signal EphB1 but fails in ALS models. Nat Commun 8.. ARTN:1164. https://doi.org/10.1038/s41467-017-01283-z
Van Damme P, Bogaert E, Dewil M, Hersmus N, Kiraly D, Scheveneels W et al (2007) Astrocytes regulate GluR2 expression in motor neurons and their vulnerability to excitotoxicity. Proc Natl Acad Sci U S A 104(37):14825–14830. https://doi.org/10.1073/pnas.0705046104
Vleminckx V, Van Damme P, Goffin K, Delye H, Van den Bosch L, Robberecht W (2002) Upregulation of HSP27 in a transgenic model of ALS. J Neuropathol Exp Neurol 61(11):968–974. https://doi.org/10.1093/jnen/61.11.968
Watanabe M, Dykes-Hoberg M, Culotta VC, Price DL, Wong PC, Rothstein JD (2001) Histological evidence of protein aggregation in mutant SOD1 transgenic mice and in amyotrophic lateral sclerosis neural tissues. Neurobiol Dis 8(6):933–941. https://doi.org/10.1006/nbdi.2001.0443
Wong HR, Ryan M, Wispe JR (1997) The heat shock response inhibits inducible nitric oxide synthase gene expression by blocking I kappa-B degradation and NF-kappa B nuclear translocation. Biochem Biophys Res Commun 231(2):257–263. https://doi.org/10.1006/bbrc.1997.6076
Xu Z, Lee A, Nouwens A, Henderson RD, McCombe PA (2018) Mass spectrometry analysis of plasma from amyotrophic lateral sclerosis and control subjects. Amyotroph Lateral Scler Frontotemporal Degener 19(5–6):362–376. https://doi.org/10.1080/21678421.2018.1433689
Yamanaka K, Boillee S, Roberts EA, Garcia ML, McAlonis-Downes M, Mikse OR et al (2008) Mutant SOD1 in cell types other than motor neurons and oligodendrocytes accelerates onset of disease in ALS mice. Proc Natl Acad Sci U S A 105(21):7594–7599. https://doi.org/10.1073/pnas.0802556105
Yenari MA, Liu J, Zheng Z, Vexler ZS, Lee JE, Giffard RG (2005) Antiapoptotic and anti-inflammatory mechanisms of heat-shock protein protection. Ann N Y Acad Sci 1053:74–83. https://doi.org/10.1196/annals.1344.007
Yu WW, Cao SN, Zang CX, Wang L, Yang HY, Bao XQ, Zhang D (2018) Heat shock protein 70 suppresses neuroinflammation induced by alpha-synuclein in astrocytes. Mol Cell Neurosci 86:58–64. https://doi.org/10.1016/j.mcn.2017.11.013
Zhang PL, Lun MY, Schworer CM, Blasick TM, Masker KK, Jones JB, Carey DJ (2008) Heat shock protein expression is highly sensitive to ischemia-reperfusion injury in rat kidneys. Ann Clin Lab Sci 38(1):57–64
Zhang Q, Lenardo MJ, Baltimore D (2017) 30 years of NF-kappa B: a blossoming of relevance to human pathobiology. Cell 168(1–2):37–57. https://doi.org/10.1016/j.cell.2016.12.012
Zheng Z, Kim JY, Ma HL, Lee JE, Yenari MA (2008) Anti-inflammatory effects of the 70 kDa heat shock protein in experimental stroke. J Cereb Blood Flow Metab 28(1):53–63. https://doi.org/10.1038/sj.jcbfm.9600502
Acknowledgements
BC is in receipt of a Studentship from the MRC Centre for Neuromuscular Diseases. LG is the Graham Watts Senior Research Fellow supported by the Brain Research Trust.
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Clarke, B.E., Kalmar, B., Greensmith, L. (2019). Protective Role of Glial Heat Shock Proteins in Amyotrophic Lateral Sclerosis. In: Asea, A., Kaur, P. (eds) Heat Shock Proteins in Neuroscience. Heat Shock Proteins, vol 20. Springer, Cham. https://doi.org/10.1007/978-3-030-24285-5_11
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