Heat shock factor 2 is a stress-responsive mediator of neuronal migration defects in models of fetal alcohol syndrome

EMBO Molecular Medicine

Volumn 6, Issue 8, 2014, Pages 1043-1061

  El Fatimy, Rachid ^a,b,c,j   Miozzo, Federico ^a,b,c   Le Mouël, Anne ^a,b   Abane, Ryma ^a,b,c   Schwendimann, Leslie ^b,d   Sabéran Djoneidi, Délara ^a,b   de Thonel, Aurélie ^e,f   Massaoudi, Illiasse ^a,b   Paslaru, Liliana ^g   Hashimoto Torii, Kazue ^h,k,l   Christians, Elisabeth ^c,i   Rakic, Pasko ^h   Gressens, Pierre ^b,d   Mezger, Valérie ^a,b  

^a Université Sorbonne Paris Cité   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c SORBONNE UNIVERSITÉ   (France)

^d HÔPITAL ROBERT DEBRÉ   (France)

^e Chu   (France)

^f UNIVERSITÉ DE BOURGOGNE   (France)

^g CAROL DAVILA UNIVERSITY OF MEDICINE AND PHARMACY   (Romania)

^h YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

ⁱ CNRS   (France)

^j BRIGHAM AND WOMEN S HOSPITAL   (United States)

^k CHILDREN'S NATIONAL MEDICAL CENTER   (United States)

^l GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

more..

Author keywords

Fetal alcohol syndrome; Heat shock factors; Microtubule associated proteins; Radial neuronal migration; Transcription

Indexed keywords

ALCOHOL; DCLK1 PROTEIN; DCX PROTEIN; HEAT SHOCK FACTOR 2 PROTEIN; HEAT SHOCK PROTEIN; HEAT SHOCK TRANSCRIPTION FACTOR 1; PROTEIN; PROTEIN P35; SUMO 1 PROTEIN; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; HSF1 PROTEIN, MOUSE; HSF2 PROTEIN, MOUSE; PROTEIN BINDING; TRANSCRIPTION FACTOR;

ALCOHOL EXPOSURE; ANIMAL EXPERIMENT; ANIMAL MODEL; CELL MIGRATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL STRESS; FETAL ALCOHOL SYNDROME; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MOUSE; NEURONAL MIGRATION DISORDER; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; SUMOYLATION; ANIMAL; BRAIN CORTEX; CHEMICALLY INDUCED; DEFICIENCY; DISEASE MODEL; GENE EXPRESSION REGULATION; KNOCKOUT MOUSE; MALFORMATION OF CORTICAL DEVELOPMENT GROUP II; METABOLISM; PATHOLOGY; PHYSIOLOGICAL STRESS;

ANIMALS; CEREBRAL CORTEX; DISEASE MODELS, ANIMAL; DNA-BINDING PROTEINS; FETAL ALCOHOL SPECTRUM DISORDERS; GENE EXPRESSION REGULATION; HEAT-SHOCK PROTEINS; MALFORMATIONS OF CORTICAL DEVELOPMENT, GROUP II; MICE; MICE, KNOCKOUT; PROTEIN BINDING; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTORS;

EID: 84905404620     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.15252/emmm.201303311     Document Type: Review

References (82)

1. Abane R, Mezger V (2010) Novel aspects of heat shock factors: roles in gametogenesis and development. FEBS J 277: 4150-4172
2. Abravaya K, Phillips B, Morimoto RI (1991) Attenuation of the heat shock response in HeLa cells is mediated by the release of bound heat shock transcription factor and is modulated by changes in growth and in heat shock temperatures. Genes Dev 5: 2117-2127
3. Ahlskog JK, Björk JK, Elsing AN, Aspelin C, Kallio M, Roos-Mattjus P, Sistonen L (2010) Anaphase-promoting complex/cyclosome participates in the acute response to protein-damaging stress. Mol Cell Biol 30: 5608-5620
4. Ahn S-G, Thiele DJ (2003) Redox regulation of mammalian heat shock factor 1 is essential for Hsp gene activation and protection from stress. Genes Dev 17: 516-528
5. Åkerfelt M, Morimoto RI, Sistonen L (2010) Heat shock factors: integrators of cell stress, development and lifespan. Nat Rev Mol Cell 11: 545-555
6. Alkuraya FS, Cai X, Emery C, Mochida GH, Al-Dosari MS, Felie JM, Hill RS, Barry BJ, Partlow JN, Gascon GG et al (2011) Human mutations in NDE1 cause extreme microcephaly with lissencephaly. Am J Hum Genet 88: 536-547
7. Ayala R, Shu T, Tsai LH (2007) Trekking across the brain: the journey of neuronal migration. Cell 128: 29-43
8. Boyault C, Zhang Y, Fritah S, Caron C, Gilquin B, Kwon SH, Garrido C, Yao TP, Vourc'h C, Matthias P et al (2007) HDAC6 controls major cell response pathways to cytotoxic accumulation of protein aggregates. Genes Dev 21: 2172-2181
9. Brocardo PS, Gil-Mohapel J, Christie BR (2011) The role of oxidative stress in fetal alcohol spectrum disorders. Brain Res Rev 67: 209-225
10. Bruce JL, Chen C, Xie Y, Zhong R, Wang YQ, Stevenson MA, Calderwood SK (1999) Activation of heat shock transcription factor 1 to a DNA binding form during the G(1)phase of the cell cycle. Cell Stress Chaperones 4: 36-45
11. Carloni S, Mazzoni E, Balduini W (2004) Caspase-3 and calpain activities after acute and repeated ethanol administration during the rat brain growth spurt. J Neurochem 89: 197-203
12. Chang Y, Östling P, Åkerfelt M, Trouillet D, Rallu M, Gitton Y, El Fatimy R, Fardeau V, Le Crom S, Morange M et al (2006) Role of heat-shock factor 2 in cerebral cortex formation and as a regulator of p35 expression. Genes Dev 20: 836-847
13. Clarke ME, Gibbard WB (2003) Overview of fetal alcohol spectrum disorders for mental health professionals. Can Child Adolesc Psychiatr Rev 12: 57-63
14. Dauphinot L, Ryle R, Rivals I, Tran Dang M, Moldrich RX, Golfier G, Ettwiller L, Toyama K, Rossier J, Personnaz L et al (2005) The cerebellar transcriptome during postnatal development of the Ts1Cje mouse, a segmental trisomy model for down syndrome. Hum Mol Genet 14: 373-384
15. Demyanenko GP, Schachner M, Anton E, Schmid R, Feng G, Sanes J, Maness PF (2004) Close homolog of L1 modulates area-specific neuronal positioning and dendrite orientation in the cerebral cortex. Neuron 44: 423-437
16. Feder JH, Rossi JM, Solomon J, Solomon N, Lindquist S (1992) The consequences of expressing hsp70 in Drosophila cells at normal temperatures. Genes Dev 6: 1402-1413
17. Francis F, Meyer G, Fallet-Bianco C, Moreno S, Kappeler C, Socorro AC, Tuy FP, Beldjord C, Chelly J (2006) Human disorders of cortical development: from past to present. Eur J Neurosci 23: 877-893
18. Fritah S, Col E, Boyault C, Govin J, Sadoul K, Chiocca S, Christians E, Khochbin S, Jolly C, Vourc'h C (2009) Heat-shock factor 1 controls genome-wide acetylation in heat-shocked cells. Mol Biol Cell 20: 4976-4984
19. Fujimoto M, Oshima K, Shinkawa T, Wang BB, Inouye S, Hayashida N, Takii R, Nakai A (2008) Analysis of HSF4 binding regions reveals its necessity for gene regulation during development and heat shock response in mouse lenses. J Biol Chem 283: 29961-29970
20. Fujimoto M, Takaki E, Takii R, Tan K, Prakasam R, Hayashida N, Iemura S, Natsume T, Nakai A (2012) RPA assists HSF1 access to nucleosomal DNA by recruiting histone chaperone FACT. Mol Cell 48: 182-194
21. Gibbard WB, Wass P, Clarke ME (2003) The neuropsychological implications of prenatal alcohol exposure. Can Child Adolesc Psychiatr Rev 12: 72-76
22. Gómez AV, Galleguillos D, Maass JC, Battaglioli E, Kukuljan M, Andrés ME (2008) CoREST represses the heat shock response mediated by HSF1. Mol Cell 31: 222-231
23. Gressens P, Lammens M, Picard JJ, Evrard P (1992) Ethanol-induced disturbances of gliogenesis and neurogenesis in the developing murine brain: an in vitro and in vivo immunohistochemical and ultrastructural study. Alcohol Alcohol 27: 219-226
24. Gressens P, Mesples B, Sahir N, Marret S, Sola A (2001) Environmental factors and disturbances of brain development. Semin Neonatol 6: 185-194
25. Guettouche T, Boellmann F, Lane WS, Voellmy R (2005) Analysis of phosphorylation of human heat shock factor 1 in cells experiencing a stress. BMC Biochem 6: 4
26. Hashimoto-Torii K, Kawasawa YI, Kuhn A, Rakic P (2011) Combined transcriptome analysis of fetal human and mouse cerebral cortex exposed to alcohol. Proc Natl Acad Sci USA 108: 4212-4217
27. Hashimoto-Torii K, Torii M, Fujimoto M, Nakai A, El Fatimy R, Mezger VJu MJ, Ishii S, Chao S, Brennand KJ, Gage FH et al (2014) Roles of Heat Shock Factor 1 in neuronal response to fetal environmental risks and its relevance to brain disorders. Neuron 82: 560-572
28. He H, Soncin F, Grammatikakis N, Li Y, Siganou A, Gong J, Brown SA, Kingston RE, Calderwood SK (2003) Elevated expression of heat shock factor (HSF) 2A stimulates HSF1-induced transcription during stress. J Biol Chem 287: 35465-35475
29. Henderson GI, Devi BG, Perez A, Schenker S (1995) In utero ethanol exposure elicits oxidative stress in the rat fetus. Alcohol Clin Exp Res 19: 714-720
30. Hietakangas V, Ahlskog JK, Jakobsson AM, Hellesuo M, Sahlberg NM, Holmberg CI, Mikhailov A, Palvimo JJ, Pirkkala L, Sistonen L (2003) Phosphorylation of serine 303 is a prerequisite for the stress-inducible SUMO modification of heat shock factor 1. Mol Cell Biol 23: 2953-2968
31. Ieraci A, Daniel G, Herrera DG (2006) Nicotinamide protects against ethanol-induced apoptotic neurodegeneration in the developing mouse brain. PLoS Med 3: 547-557
32. Ieraci A, Daniel G, Herrera DG (2007) Single alcohol exposure in early life damages hippocampal stem/progenitor cells and reduces adult neurogenesis. Neurobiol Dis 26: 597-605
33. Ikonomidou C, Bittigau P, Ishimaru MJ, Wozniak DF, Koch C, Genz K, Price MT, Stefovska V, Hörster F, Tenkova T et al (2000) Ethanol-induced apoptotic neurodegeneration and fetal alcohol syndrome. Science 287: 1056-1060
34. Ikonomidou C, Kaindl AM (2011) Neuronal death and oxidative stress in the developing brain. Antioxid Redox Signal 14: 1535-1550
35. Inouye S, Fujimoto M, Nakamura T, Takaki E, Hayashida N, Hai T, Nakai A (2007) Heat shock transcription factor 1 opens chromatin structure of interleukin-6 promoter to facilitate binding of an activator or a repressor. J Biol Chem 282: 33210-33217
36. Jolly C, Usson Y, Morimoto RI (1999) Rapid and reversible relocalization of heat shock factor 1 within seconds to nuclear stress granules. Proc Natl Acad Sci USA 96: 6769-6774
37. Jones KL, Smith DW (1973) Recognition of the fetal alcohol syndrome in early infancy. Lancet 2: 999-1001
38. Ju XD, Guo Y, Wang NN, Huang Y, Lai MM, Zhai YH, Guo YG, Zhang JH, Cao RJ, Yu HL, Cui L, Li YT, Wang XZ, Ding YQ, Zhu XJ (2014) Both Myosin-10 isoforms are required for radial neuronal migration in the developing cerebral cortex. Cereb Cortex 24: 1259-1268
39. Jurivich D, Sistonen L, Kroes RA, Morimoto RI (1992) Effect of sodium salicylate on the human heat shock response. Science 255: 1243-1245
40. Jurivich DA, Pachetti C, Qiu L, Welk JF (1995) Salicylate triggers heat shock factor differently than heat. J Biol Chem 270: 24489-24495
41. Kallio M, Chang Y, Manuel M, Alastalo T-P, Rallu M, Gitton Y, Pirkkala L, Loones M-T, Paslaru L, Larney S et al (2002) Brain abnormalities, defective meiotic chromosome synapsis and female subfertility in HSF2 null mice. EMBO J 21: 2591-2601
42. Khaleque MA, Bharti A, Gong J, Gray PJ, Sachdev V, Ciocca DR, Stati A, Fanelli M, Calderwood SK (2008) Heat shock factor 1 represses estrogen-dependent transcription through association with MTA1. Oncogene 27: 1886-1893
43. Kim D, Li GC (1999) Proteasome inhibitors lactacystin and MG132 inhibit the dephosphorylation of HSF1 after heat shock and suppress thermal induction of heat shock gene expression. Biochem Biophys Res Com 264: 352-358
44. Kline MP, Morimoto RI (1997) Repression of the heat shock factor 1 transcriptional activation domain is modulated by constitutive phosphorylation. Mol Cell Biol 17: 2107-2115
45. Krebs RA, Feder ME (1997) Deleterious consequences of Hsp70 overexpression in Drosophila melanogaster larvae. Cell Stress Chaperones 2: 60-71
46. Lemoine P, Harousseau H, Borteyru J (1968) Les enfants de parents alcooliques: anomalies observées. Ouest Méd 2: 476-482
47. Le Masson F, Christians E (2011) HSFs and regulation of Hsp70.1 (Hspa1b) in oocytes and preimplantation embryos: new insights brought by transgenic and knockout mouse models. Cell Stress Chaperones 16: 275-285
48. Loison F, Debure L, Nizard P, le Goff P, Michel D, Le Dréan Y (2006) Up-regulation of the clusterin gene after proteotoxic stress: implication of HSF1-HSF2 heterocomplexes. Biochem J 395: 223-231
49. Mathew A, Mathur SK, Jolly C, Fox SG, Kim S, Morimoto RI (2001) Stress-specific activation and repression of heat shock factors 1 and 2. Mol Cell Biol 21: 7163-7171
50. Mendillo ML, Santagata S, Koeva M, Bell GW, Hu R, Tamimi RM, Fraenkel E, Ince TA, Whitesell L, Lindquist S (2012) HSF1 drives a transcriptional program distinct from heat shock to support highly malignant human cancers. Cell 150: 549-562
51. Mezger V, Bensaude O, Morange M (1989) Unusual levels of heat shock element-binding activity in embryonal carcinoma cells. Mol Cell Biol 9: 3888-3896
52. Mosser DD, Theodorakis NG, Morimoto RI (1988) Coordinate changes in heat shock element-binding activity and HSP70 gene transcription rates in human cells. Mol Cell Biol 8: 4736-4744
53. 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: e1000291
54. Neef DW, Jaeger AM, Thiele DJ (2011) Heat shock transcription factor 1 as a therapeutic target in neurodegenerative diseases. Nat Rev Drug Discov 10: 930-944
55. Newton EM, Knauf U, Green M, Kingston RE (1996) The regulatory domain of human heat shock factor 1 is sufficient to sense heat stress. Mol Cell Biol 16: 839-846
56. Olney JW, Tenkovaa T, Dikraniana K, Qina Y-Q, Labruyerea J, Ikonomidou C (2002) Ethanol-induced apoptotic neurodegeneration in the developing C57BL/6 mouse brain. Dev Brain Res 133: 115-126
57. Östling P, Björk JK, 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
58. Pignataro L, Miller AN, Ma L, Midha S, Protiva P, Herrera DG, Harrison NL (2007) Alcohol regulates gene expression in neurons via activation of heat shock factor 1. J Neurosci 27: 12957-12966
59. Rallu M, Loones M, Lallemand Y, Morimoto R, Morange M, Mezger V (1997) Function and regulation of heat shock factor 2 during mouse embryogenesis. Proc Natl Acad Sci USA 94: 2392-2397
60. Raychaudhuri S, Loew C, Körner R, Pinkert S, Theis M, Hayer-Hartl M, Buchholz F, Hartl FU (2014) Interplay of acetyltransferase EP300 and the proteasome system in regulating heat shock transcription factor 1. Cell 156: 975-985
61. Reiner O, Sapir T (2009) Polarity regulation in migrating neurons in the cortex. Mol Neurobiol 40: 1-14
62. Rubert G, Miñana R, Pascual M, Guerri C (2006) Ethanol exposure during embryogenesis decreases the radial glial progenitor pool and affects the generation of neurons and astrocytes. J Neurosci Res 84: 483-496
63. Sandqvist A, Björk JK, Åkerfelt M, Chitikova Z, Grichine A, Vourc'h C, Jolly C, Tiina A, Salminen TA, Nymalm Y et al (2009) Heterotrimerization of heat-shock factors 1 and 2 provides a transcriptional switch in response to distinct stimuli. Mol Biol Cell 20: 1340-1347
64. Santillano DR, Kumar LS, Prock TL, Camarillo C, Tingling JD, Miranda RC (2005) Ethanol induces cell-cycle activity and reduces stem cell diversity to alter both regenerative capacity and differentiation potential of cerebral cortical neuroepithelial precursors. BMC Neurosci 6: 59
65. Sapir T, Sapoznik S, Levy T, Finkelshtein D, Shmueli A, Timm T, Mandelkow EM, Reiner O (2008) Accurate balance of the polarity kinase MARK2/Par-1 is required for proper cortical neuronal migration. J Neurosci 28: 5710-5720
66. Sapir T, Frotscher M, Levy T, Mandelkow EM, Reiner O (2012) Tau's role in the developing brain: implications for intellectual disability. Hum Mol Genet 21: 1681-1692
67. Sarge KD, Murphy SP, Morimoto RI (1993) Activation of heat shock gene transcription by heat shock factor 1 involves oligomerization, acquisition of DNA-binding activity, and nuclear localization and can occur in the absence of stress. Mol Cell Biol 13: 1392-1407
68. Shinkawa T, Tan K, Fujimoto M, Hayashida N, Yamamoto K, Takaki E, Takii R, Prakasam R, Inouye S, Mezger V et al (2011) Heat shock factor 2 is required for maintaining proteostasis against febrile-range thermal stress and polyglutamine aggregation. Mol Biol Cell 22: 3571-3583
69. Sistonen L, Sarge KD, Morimoto RI (1994) Human heat shock factors 1 and 2 are differentially activated and can synergistically induce hsp70 gene transcription. Mol Cell Biol 14: 2087-2099
70. Sullivan EK, Weirich CS, Guyon JR, Sif S, Kingston RE (2001) Transcriptional activation domains of human heat shock factor 1 recruit human SWI/SNF. Mol Cell Biol 21: 5826-5837
71. Tanaka T, Serneo FF, Tseng HC, Kulkarni AB, Tsai LH, Gleeson JG (2004) Cdk5 phosphorylation of doublecortin ser297 regulates its effect on neuronal migration. Neuron 41: 215-227
72. Takahashi Y, Rayman JB, Dynlacht BD (2000) Analysis of promoter binding by the E2F and pRB families in vivo: Distinct E2F proteins mediate activation and repression. Genes & Dev 14: 804-816
73. Thompson BL, Levitt P, Stanwood GD (2009) Prenatal exposure to drugs: effects on brain development and implications for policy and education. Nat Rev Neurosci 10: 303-312
74. Thomson S, Hollis A, Hazzalin CA, Mahadevan LC (2004) Distinct stimulus-specific histone modifications at Hsp70 chromatin targeted by the transcription factor HSF1. Mol Cell 15: 585-594
75. Valenzuela CF, Morton RA, Diaz MR, Topper L (2012) Does moderate drinking harm the fetal brain? Insights from animal models. Trends Neurosci 35: 284-292
76. Vihervaara A, Sergelius C, Vasara J, Blom MA, Elsing AN, Roos-Mattjus P, Sistonen L (2013) Transcriptional response to stress in the dynamic chromatin environment of cycling and mitotic cells. Proc Natl Acad Sci U S A 110: E3388-E3397
77. 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
78. Westerheide SD, Morimoto RI (2005) Heat shock response modulators as therapeutic tools for diseases of protein conformation. J Biol Chem 280: 33097-33100
79. Westerheide SD, Anckar J, Stevens SM Jr, Sistonen L, Morimoto RI (2009) Stress-inducible regulation of heat shock factor 1 by the deacetylase SIRT1. Science 323: 1063-1066
80. Whitesell L, Lindquist S (2009) Inhibiting the transcription factor HSF1 as an anticancer strategy. Expert Opin Ther Targets 13: 469-478
81. Wynshaw-Boris A (2007) Lissencephaly and LIS1: insights into the molecular mechanisms of neuronal migration and development. Clin Genet 72: 296-304
82. Zhou FC, Sari Y, Zhang JK, Goodlett CR, Li T-K (2001) Prenatal alcohol exposure retards the migration and development of serotonin neurons in fetal C57BL mice. Dev Brain Res 126: 147-155