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The 70kDa Heat Shock Protein Family and Learning

  • Martine Ammassari-TeuleEmail author
  • Giuseppina Mariucci
  • Maria Vittoria Ambrosini
Chapter
Part of the Heat Shock Proteins book series (HESP, volume 5)

Abstract:

This chapter examines data supporting the view that heat shock proteins members of the 70 kDa family (HSP70) interfere with the plastic mechanisms underlying learning and memory. In the first part, we present evidence that rodents trained in tasks taxing specific forms of learning show increased levels of inducible (Hsp72) or constitutive (Hsc70) HSP in the brain regions mediating these learning systems. In the second part, we describe experiments in which exposure to a heat shock (also referred to as heat shock preconditioning) prevents the disruptive effect of amnestic agents on learning performance and synaptic plasticity, and interferes with the learning performance in different species. In the third part, we review data aimed at disentangling specific from non-specific learning effects of increased expression of HSP70 in the brain. We conclude that the experimental conditions in which HSP70 are expressed and the loci where this expression takes place suggest a role for these proteins in synaptic plasticity, learning, and memory

Keywords:

70 kDa Heat shock protein heat shock heat shock factors learning stress motor activity 

Abbreviations

AD

Alzheimer’s disease

fEPSP

field excitatory post synaptic potential

HSF

heat shock factor

HSP

heat shock proteins

HD

Huntington’s disease

HSP70

70 kDa heat shock protein family

Hsc70 and Hsp73

constitutive 70 kDa HSP

Hsp70 and Hsp72

inducible 70 kDa HSP

hsp72

stress inducible Hsp72 gene

LTM

long-term memory

LTP

long-term potentiation

PD

Parkinson’s disease

STM

short-term memory

References

  1. Akirav I, Sandi C, Venero C, Richter-Levin G (2001) Differential activation of hippocampus and amygdala following spatial learning under stress. Eur. J. Neurosci. 14, 719–725.CrossRefPubMedGoogle Scholar
  2. Allen GV, Chase T (2001) Induction of heat shock proteins and motor function deficits after focal cerebellar injury. Neuroscience 102, 603–614.CrossRefPubMedGoogle Scholar
  3. Ambrosini MV, Mariucci G, Tantucci M et al. (1999) Induction of cerebellar hsp72 in rats learning a two-way active avoidance task. Brain Res. Mol. Brain Res. 70, 164–169.CrossRefPubMedGoogle Scholar
  4. Ambrosini MV, Mariucci G, Tantucci M et al. (2005) Hippocampal 72-kDa heat shock protein expression varies according to mice learning performance independently from chronic exposure to stress. Hippocampus 15, 413–417.CrossRefPubMedGoogle Scholar
  5. Ammassari-Teule M, Caprioli A (1985) Spatial learning and memory, maze-running strategies and cholinergic mechanisms in two inbred strains of mice. Behav. Brain Res. 17, 9–16.CrossRefPubMedGoogle Scholar
  6. Ammassari-Teule M, Passino E, Restivo L, de Marsanich B (2000) Fear conditioning in C57BL/6 and DBA/2 mice: variability in nucleus accumbens function according to the strain predisposition to show contextual- or cue-based responding. Eur. J. Neurosci. 12, 4467–4474.Google Scholar
  7. Ammon-Treiber S, Grecksch G, Charalampos A, Vezyraki P, Hollt V (2008) Emotional and learning behaviour in mice overexpressing heat shock protein 70. Neurobiol. Learn. Mem. 90, 358–364.Google Scholar
  8. Anokhin KW, Rose SPR (1990) Learning induced increase of immediate early gene messenger RNA in the chick forebrain. Eur. J. Neurosci. 3, 162–167.CrossRefGoogle Scholar
  9. Archer T (1982) DSP4 (N-2-chloroethyl-N-ethyl-2-bromobenzylamine), a new noradrenaline neurotoxin, and stimulus conditions affecting acquisition of two-way active avoidance. J. Comp. Physiol. Psychol. 96, 476–490.CrossRefPubMedGoogle Scholar
  10. Asea A (2006) Initiation of the immune response by extracellular Hsp72: chaperokine activity of Hsp72. Curr. Immunol. Rev. 2, 209–215.CrossRefPubMedGoogle Scholar
  11. Auluck PK, Chan HY, Trojanowski JQ et al. (2002) Chaperone suppression of alpha-synuclein toxicity in a Drosophila model for Parkinson’s disease. Science 295, 865–868.CrossRefPubMedGoogle Scholar
  12. Bertaina-Anglade V, Tramu G, Destrade C (2000) Differential learning- stage dependent pattern of c-Fos protein expression in brain regions during the acquisition and memory consolidation of an operant task in mice. Eur. J. Neurosci. 12, 3803–3812.CrossRefPubMedGoogle Scholar
  13. Bjornebekk A, Mathé AA, Bréné S (2005) The antidepressant effect of running is associated with increased hippocampal cell proliferation. Int. J. Neuropsychopharmacol. 8, 357–368.CrossRefPubMedGoogle Scholar
  14. Brown IR (1990) Induction of heat shock (stress) genes in the mammalian brain by hyperthermia and other traumatic events: a current perspective. J. Neurosci. Res. 27, 247–255.CrossRefPubMedGoogle Scholar
  15. Brown IR (2007) Heat shock proteins and protection of the nervous system. Ann. N. Y. Acad. Sci. 1113, 147–158.CrossRefPubMedGoogle Scholar
  16. Brown DA, Johnson MS, Armstrong CJ, Lynch JM, Caruso NM, Ehlers LB, Fleshner M, Spencer RL, Moore RL (2007) Short-term treadmill running in the rat: what kind of stressor is it? J. Appl. Physiol. 103, 1979–1985.CrossRefPubMedGoogle Scholar
  17. Cabib S, Castellano C, Pattacchioli FR, Cigliana G, Angelucci L, Puglisi-Allegra S (1996) Opposite strain-dependent effects of post-training corticosterone in a passive avoidance task in mice: role of dopamine. Brain Res. 729, 100–118.CrossRefGoogle Scholar
  18. Calabrese V, Scapagnini G, Ravagna A, Colombrita C, Spadaro F, Butterfield DA, Giuffrida Stella AM (2004) Increased expression of heat shock proteins in rats brain during aging: relationship with mitochondrial function and glutathione redox state. Mech. Ageing Dev. 4, 325–335.Google Scholar
  19. Calabrese V, Scapagnini G, Ravagna A, Fariello RG, Giuffrida Stella AM, Abraham NG (2002) Regional distribution of heme oxygenase, HSP70, and glutathione in the brain: relevance for endogenous oxidant/antioxidant balance and stress tolerance. J. Neurosci. Res. 68, 65–75.CrossRefPubMedGoogle Scholar
  20. Campisi J, Fleshner M (2003) Role of extracellular HSP72 in acute stress-induced potentiation of innate immunity in active rats. J. Appl. Physiol. 94, 43–52.PubMedGoogle Scholar
  21. Campisi J, Leem TH, Fleshner M (2003a) Stress-induced extracellular Hsp72 is a functionally significant danger signal to the immune system. Cell Stress Chaperones 8, 272–286.CrossRefPubMedGoogle Scholar
  22. Campisi J, Leem TH, Greenwood BN, Hansen MK, Moraska A, Higgins K, Smith TP, Fleshner M (2003b) Habitual physical activity facilitates stress-induced HSP72 induction in brain, peripheral, and immune tissues. Am. J. Physiol. Regul. Integr. Comp. Physiol. 84, 520–530.Google Scholar
  23. Castellano C, Puglisi-Allegra S (1983) Strain-dependent modulation of memory by stress in mice. Behav. Neural. Biol. 38, 133–138.CrossRefPubMedGoogle Scholar
  24. Chen S, Brown IR (2007) Neuronal expression of constitutive heat shock proteins: implications for neurodegenerative diseases. Cell Stress Chaperones 12, 51–58.CrossRefPubMedGoogle Scholar
  25. Cogan DC, Reeves JL (1979) Passive avoidance learning in hippocampectomized rats under different shock and intertrial interval conditions. Physiol. Behav. 22, 1115–1121.CrossRefPubMedGoogle Scholar
  26. Cohen NJ, Squire LR (1980) Preserved learning and retention of pattern-analyzing skill in amnesia: dissociation of knowing how and knowing that. Science 210, 207–210.CrossRefPubMedGoogle Scholar
  27. Dishman RK, Warren JM, Youngstedt SD, Yoo H, Bunnell BN, Mougey EH, Meyerhoff JL, Jaso-Friedmann L, Evans DL (1995) Activity-wheel running attenuates suppression of natural killer cell activity after footshock. J. Appl. Physiol. 78, 1547–1554.CrossRefPubMedGoogle Scholar
  28. Dou F, Netzer WJ, Tanemura K et al. (2003) Chaperones increase association of tau protein with microtubules. Proc. Natl. Acad. Sci. U. S. A. 100, 721–726.CrossRefPubMedGoogle Scholar
  29. Farmer J, Zhao X, van Praag H, Wodtke K, Gage FH, Christie BR (2004) Effects of voluntary exercise on synaptic plasticity and gene expression in the dentate gyrus of adult male Sprague Dawley rats in vivo. Neuroscience 124, 71–79.CrossRefPubMedGoogle Scholar
  30. Feige U, Polla BS (1994) Hsp70 – a multi-gene, multi-structure, multi-function family with potential clinical applications. Experientia 50, 979–986.CrossRefPubMedGoogle Scholar
  31. Frey U, Morris RG (1998) Synaptic tagging: implications for late maintenance of hippcoampal long-term potentiation. Nature 385, 533–536.CrossRefGoogle Scholar
  32. Fukudo S, Abe K, Itoyama Y, Mochizuki S, Sawai T, Hongo M (1999) Psychophysiological stress induces heat shock cognate protein 70 messenger RNA in the hippocampus of rats. Neuroscience 91, 1205–1208.CrossRefPubMedGoogle Scholar
  33. Fukudo S, Abe K, Hongo M, Utsumi A, Itoyama Y (1995) Psychophysiological stress induces heat shock cognate protein (HSC 70) mRNA in the stomach. Brain Res. 675, 98–102.Google Scholar
  34. Gold PE, Vogt J, Hall JL (1986) Glucose effects on memory: behavioral and pharmacological characteristics. Behav. Neural Biol. 46, 145–155.CrossRefPubMedGoogle Scholar
  35. Gray CC, Amrani M, Yacoub MH (1999) Heat stress proteins and myocardial protection: experimental model or potential clinical tool? Int. J. Biochem. Cell. Biol. 31, 559–573.CrossRefPubMedGoogle Scholar
  36. Greenwood BN, Stong PV, Dorey AA, Fleshner AA (2007) Therapeutic effects of exercise: wheel running reverses stress-induced interference with shuttle box escape. Behav. Neurosci. 121, 992–1000.CrossRefPubMedGoogle Scholar
  37. Grimm R, Tichmeyer W (1997) Complex patterns of immediate early gene induction in rat brain following brightness discrimination training and pseudotraining. Behav. Brain Res. 84, 109–111.CrossRefPubMedGoogle Scholar
  38. Hebb DO (1949) The Organization of Behavior, Wiley-Interscience, New York.Google Scholar
  39. Hightower LE, Sadis SE, Takenaka IM (1994) Interactions of vertebrate Hsc70 and hsp70 with unfolded proteins and peptides. In: Morimoto RI, Tissieres A and Georgopoulos C (eds) The Biology of Heat Shock Proteins and Molecular Chaperones Cold, Spring Harbor Laboratory Press, Plainview, NY.Google Scholar
  40. Hu RQ, Koh S, Torgerson T, Cole A (1998) Neuronal stress an dinjury in C57/BL mice after sustemic kainic acid administration. Brain Res. 810, 229–240.CrossRefPubMedGoogle Scholar
  41. Hung CH, Lin MT, Liao JF, Wang JJ (2004) Scopolamine-induced amnesia can be prevented by heat shock pre-treatment in rats. Neurosci. Lett. 364, 63–66.CrossRefPubMedGoogle Scholar
  42. Hutter JJ, Mestril R, Tam EK, Sievers RE, Dillmann WH, Wolfe CL (1996) Overexpression of heat shock protein 72 in transgenic mice decreases infarct size in vivo. Circulation 94, 1408–1411.PubMedGoogle Scholar
  43. Johnson JD, Fleshner M (2006) Releasing signals, secretory pathways, and immune function of endogenous extracellular heat shock protein 72. J. Leukoc. Biol. 79, 425–434.CrossRefPubMedGoogle Scholar
  44. Kallio M, Chang Y, Manuel M, Alastalo TP, Rallu M, Gitton Y, Pirkkala L, Loones MT, Paslaru L, Larney S, Liard S, Morante M, Sistonen L, Mezger V (2002) Brain abnormalities, defective meiotic chromosome synapsis and female subfertility in HSF2 null mice. EMBO J. 21, 2591–2601.CrossRefPubMedGoogle Scholar
  45. Kelly J, Alheid GF, McDermott L, Halaris A, Grossman SP (1977) Behavioral and biochemical effects of knife cuts that preferentially interrupt principal and efferent connections of the striatum in the rat. Pharmac. Biochem. Behav. 6, 31–45.CrossRefGoogle Scholar
  46. Kelly MP, Deadwyler SA (2002) Acquisition of a novel behavior induces higher levels of Arc mRNA than does overtrained performance. Neuroscience 110, 617–626.CrossRefPubMedGoogle Scholar
  47. Klucken J, Shin Y, Masliah E et al. (2004) Hsp70 reduces alpha-synuclein aggregation and toxicity. J. Biol. Chem. 279, 25497–25502.CrossRefPubMedGoogle Scholar
  48. Kuhl D, Kennedy TE, Barzilai A et al. (1992) Long term sensitization training in Aplysia leads to an increase in the expression of BiP, The major protein chaperon of the ER. J. Cell. Biol. 119, 1069–1076.CrossRefPubMedGoogle Scholar
  49. Lin YW, Yang HW, Min MY, Chiu TH (2004) Heat-shock pretreatments suppression of long term potentiation induced by scopolamine in rat hippcoampal CA1 synapses. Brain Res. 999, 222–226.CrossRefPubMedGoogle Scholar
  50. Lorenzini CA, Baldi E, Bucherelli C, Sacchetti B, Tassoni G (1996) Role of dorsal hippocampus in acquisition, consolidation and retrieval of rat’s passive avoidance response: a tetrodotoxin functional inactivation study. Brain Res. 730, 32–39.CrossRefPubMedGoogle Scholar
  51. Lowenstein DH, Simon RP, Sharp FR (1990) The pattern of 72 kDa heat shock protein-like immunoreactivity in the rat brain following flurothyl-induced status epilepticus. Brain Res. 531, 173–182.CrossRefPubMedGoogle Scholar
  52. Magrané J, Smith RC, Walsh K et al. (2004) Heat shock protein 70 participates in the neuroprotective response to intracellularly expressed beta-amyloid in neurons. J. Neurosci. 24, 1700–1706.CrossRefPubMedGoogle Scholar
  53. Mariucci G, Tantucci M, Giuditta A, Ambrosini MV (2007) Permanent brain ischemia induces marked increments in hsp72 expression and local protein synthesis in synapses of the ischemic hemisphere. Neurosci. Lett. 415, 77–80.CrossRefPubMedGoogle Scholar
  54. Maycox PR, Link E, Reetz A et al. (1992) Clathrin-coated vesicles in nervous tissue are involved primarily in synaptic vesicle recycling. J. Cell Biol. 118, 1379–1388.CrossRefPubMedGoogle Scholar
  55. McDonald RJ, White NM (1993) A triple dissociation of memory systems: hippocampus, amygdala, and dorsal striatum. Behav. Neurosci. 107, 3–22.CrossRefPubMedGoogle Scholar
  56. McGaugh JL, Izquierdo I (2000) The contribution of pharmacology to research on the mechanisms of memory formation. Trends Pharmacol. Sci. 21, 208–210.CrossRefPubMedGoogle Scholar
  57. McLean PJ, Klucken J, Shin Y et al. (2004) Geldanamycin induces Hsp70 and prevents alpha-synuclein aggregation and toxicity in vitro. Biochem. Biophys. Res. Commun. 21, 665–669.CrossRefGoogle Scholar
  58. Mitcham JC, Thomas RK (1972) Effects of substantia nigra and caudate nucleus lesions on avoidance learning in rats. J. Comp. Physiol. Psychol. 81, 101–107.CrossRefPubMedGoogle Scholar
  59. Monfort V, Chapillon P, Mellier D, Lalonde R, Caston J (1998) Timed active avoidance learning in lurcher mutant mice. Behav. Brain Res. 91, 165–172.CrossRefPubMedGoogle Scholar
  60. Montag-Sallaz M, Montag D (2003) Severe cognitive and motor coordination deficits in tenascin-R-deficient mice. Genes Brain Behav. 2, 20–31.CrossRefPubMedGoogle Scholar
  61. Moon IS, Park IS, Schenker LT et al. (2001) Presence of both constitutive and inducible forms of heat shock protein 70 in the cerebral cortex and hippocampal synapses. Cereb. Cortex 11, 238–247.CrossRefPubMedGoogle Scholar
  62. Morgan JR, Prasad K, Jin S et al. (2001) Uncoating of clathrin-coated vesicles in presynaptic terminals: roles for Hsc70 and auxilin. Neuron 32, 289–300.CrossRefPubMedGoogle Scholar
  63. Morris RG, Moser EI, Riedel G, Martin SJ, Sandin J, Day M, O’Carroll C (2003) Elements of a neurobiological theory of the hippocampus: the role of activity-dependent synaptic plasticity in memory. Philos. Trans. R Soc. Lond. B Biol. Sci. 358(1432), 773–786.CrossRefPubMedGoogle Scholar
  64. Muchowski PJ (2002) Protein misfolding, amyloid formation, and neurodegeneration: a critical role for molecular chaperones? Neuron 35, 9–12.CrossRefPubMedGoogle Scholar
  65. Muchowski PJ, Wacker JL (2005) Modulation of neurodegeneration by molecular chaperones. Nat. Rev. Neurosci. 6, 11–22.CrossRefPubMedGoogle Scholar
  66. Naylor AS, Persson AI, Eriksson PS, Jondottir JH, Thorlin T (2005) Effects of chronic treadmill running on neurogenesis n the dentate gyrus of the hippocampus of adult rat. Brain Res. 93, 2406–2414.Google Scholar
  67. Neill DB, Ross JF, Grossman SP (1974) Effects of lesions in the dorsal or ventral striatum on locomotor activity and on locomotor effects of amphetamine. Pharmacol. Biochem. Behav. 2, 697–702.CrossRefPubMedGoogle Scholar
  68. Nevidi E, Hevroni D, Naot D, Israeli D, Citri Y (1992) Numerous candidate plasticity-related genes revealed by differential cDNA cloning. Nature 363, 718–722.Google Scholar
  69. Nikolaev E, Werka T, Kaczmarek L (1992) c-Fos protooncogene expression in rat brain after long term training of two-way active avoidance reaction. Behav. Brain Res. 48, 91–94.CrossRefPubMedGoogle Scholar
  70. Nowak TS, Ikeda J, Nakajima T (1990) 70-kDa heat shock protein and c-fos gene expression after transient ischemia. Stroke 21, 107–111.Google Scholar
  71. O’Keefe J, Nadel L (1978). The Hippocampus as a Cognitive Map, Clarendon Press, Oxford.Google Scholar
  72. Packard MG, Hirsh R, White NM (1989) Differential effects of fornix and caudate nucleus lesions on two radial maze tasks: evidence for multiple memory systems. J. Neurosci. 9, 1465–1472.PubMedGoogle Scholar
  73. Packard MG, McGaugh JL (1992) Double dissociation of fornix and caudate nucleus lesions on acquisition of two water maze tasks: further evidence for multiple memory systems. Behav. Neurosci. 106, 439–446.CrossRefPubMedGoogle Scholar
  74. Packard MG, White NM (1991) Dissociation of hippocampus and caudate nucleus memory systems by posttraining intracerebral injection of dopamine agonists. Behav. Neurosci. 105, 295–306.CrossRefPubMedGoogle Scholar
  75. Papp E, Nardai G, Soti C, Csermely P (2003) Molecular chaperones, stress proteins and redox homeostasis. Biofactors 17, 249–257.CrossRefPubMedGoogle Scholar
  76. Pelham HR (1989) Heat shock and the sorting of luminal ER proteins. EMBO J. 8, 3171–3176.PubMedGoogle Scholar
  77. Pettigrew LC, Holtz ML, Minger SL, Craddock SD (2003) Glutamate receptor antagonists modulate heat shock protein response in focal brain ischemia. Neurol. Res. 25, 201–207.CrossRefPubMedGoogle Scholar
  78. Pizzaro JM, Haro LS, Barea-Rodriguez J (2003) Learning-associated increase in heat shock cognate 70 mRNA and protein expression. Neurobiol. Learn. Mem. 79, 142–151.CrossRefGoogle Scholar
  79. Planas AM, Soriano AA, Estrada A et al. (1997) The heat shock stress response after brain lesions: induction of 72 kDa heat shock protein (cell types involved, axonal transport, transcriptional regulation) and protein synthesis inhibition. Prog. Neurobiol. 5, 607–636.CrossRefGoogle Scholar
  80. Poldrack RA, Clark J, Paré-Blagoev EJ, Shohamy D, Creso Moyano J, Myers C, Gluck MA (2001) Interactive memory systems in the human brain. Nature 414, 546–550.CrossRefPubMedGoogle Scholar
  81. Rankin CH, Beck CD, Chiba CM (1990) Caenorhabditis elegans: a new model system for the study of learning and memory. Behav. Brain Res. 37, 89–92.CrossRefPubMedGoogle Scholar
  82. Reynolds LP, Allen GV (2003) A review of heat shock protein induction following cerebellar injury. Cerebellum 2, 171–177.CrossRefPubMedGoogle Scholar
  83. Rose JK, Kaun KR, Chen SH, Rankin CH (2003) GLR-1, a non-NMDA glutamate receptor homolog, is critical for long-term memory in Caenorhabditis elegans. J. Neurosci. 23, 9595–9599.PubMedGoogle Scholar
  84. Rose JK, Rankin CH (2006) Blocking memory reconsolidation reverses memory-associated changes in glutamate receptor expression. J. Neurosci. 26, 11582–11587.CrossRefPubMedGoogle Scholar
  85. Sahay A, Drew MR, Hen R (2007) Dentate gyrus neurogenesis and depression. Prog. Brain Res. 163, 697–722.CrossRefPubMedGoogle Scholar
  86. 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, 745–756.CrossRefPubMedGoogle Scholar
  87. Scoville WB, Milner B (1957) Loss of recent memory after bilateral hippocampal lesions. J. Neurol. Neurosurg. Psychiatry 20, 1–21.CrossRefGoogle Scholar
  88. Sittler A, Lurz R, Lueder G et al. (2001) Geldanamycin activates a heat shock response and inhibits huntingtin aggregation in a cell culture model of Huntington’s disease. Hum. Mol. Genet. 10, 1307–1315.CrossRefPubMedGoogle Scholar
  89. Solomonia RO, McCabe BJ, Jackson AP et al. (1997) Clathrin proteins and recognition memory. Neuroscience 80, 59–67.CrossRefPubMedGoogle Scholar
  90. Suzuki T, Usuda N, Murata S, Nakazawa A, Ohtsuka K, Takagi H (1999) Presence of molecular chaperones, heat shock cognate (Hsc) 70 and heat shock proteins (hsp) 40 in the postsynaptic structures of rat brain. Brain Res. 816, 99–110.CrossRefPubMedGoogle Scholar
  91. Takayama S, Reed JC, Homma S (2003) Heat-shock proteins as regulator of apoptosis. Oncogene 22, 9041–9047.CrossRefPubMedGoogle Scholar
  92. Terui H, Haga S, Enosawa S, Ohnuma N, Ozaki M (2004) Hypoxia/re-oxygenation-induced, redox-dependent activation of STAT1 (signal transducer and activator of transcription 1) confers resistance to apoptotic cell death via hsp70 induction. Biochem. J. 380, 203–209.CrossRefPubMedGoogle Scholar
  93. Uda M, Ishido M, Kami K, Masahura M (2006) Effects of chronic treadmill running on neurogenesis in the dentate gyrus of the hippocampus of adult rat. Brain Res. 1104, 64–72.CrossRefPubMedGoogle Scholar
  94. Upchurch M, Wehner JM (1989) Inheritance of spatial learning ability in inbred mice: a classical genetic analysis. Behav. Neurosci. 103, 1251–1258.CrossRefPubMedGoogle Scholar
  95. Van Molle W, Wielock B, Takada M, Taniguchi T, Sekikawa K, Libert C (2002) HSP70 protects against TNF-induced lethal inflammatory shock. Immunity 16, 685–695.CrossRefPubMedGoogle Scholar
  96. Wang G, Zhang J, Moskophidis D, Mivechi NF (2003) Targeted disruption of the heat shock transcription factor (hsf)-2 gene results in increased embryonic lethality, neuronal defects, and reduced spermatogenesis. Genesis 36, 48–61.CrossRefPubMedGoogle Scholar
  97. Welch WJ (1991) The role of heat-shock proteins as molecular chaperones. Curr. Opin. Cell Biol. 3, 1033–1038.CrossRefPubMedGoogle Scholar
  98. Welch WJ (1993) Heat shock proteins functioning as molecular chaperones: their roles in normal and stressed cells. Philos. Trans. R Soc. Lond. B Biol. Sci. 339(1289), 327–333.CrossRefPubMedGoogle Scholar
  99. Whitham M, Forbes M (2008) Heat shock protein 72: release and biological significance during exercise. Front Biosci. 13, 1328–1329.CrossRefPubMedGoogle Scholar
  100. Whitlock JR, Heynen AJ, Shuler MG, Bear MF (2006) Learning induces long-term potentiation in the hippocampus. Science 313, 1093–1097.CrossRefPubMedGoogle Scholar
  101. Wojtowicz JM, Askew ML, Winocur G (2008) The effects of running and of inhibiting adult neurogenesis on learning and memory in rats. Eur. J. Neurosci. 27, 1494–1502.CrossRefPubMedGoogle Scholar
  102. Xiao X, Zuo X, Davis AA, McMillan DR, Curry BB, Richadson JA, Benjamin IJ (1999) HSF1 is required for extra-embryonic development, postnatal growth and protection during inflammatory responses in mice. EMBO J. 18, 5943–5952.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Martine Ammassari-Teule
    • 1
    • 2
    Email author
  • Giuseppina Mariucci
    • 3
  • Maria Vittoria Ambrosini
    • 3
  1. 1.Istituto di NeuroscienzeConsiglio Nazionale delle RicercheRomeItaly
  2. 2.Istituto di NeuroscienzeConsiglio Nazionale delle Ricerche and Santa Lucia FoundationRomeItaly
  3. 3.Dipartimento di Medicina Sperimentale e Scienze BiochimicheUniversity of PerugiaPerugiaItaly

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