The α crystallin domain of small heat shock protein b8 (Hspb8) acts as survival and differentiation factor in adult hippocampal neurogenesis

Journal of Neuroscience

Volumn 33, Issue 13, 2013, Pages 5785-5796

  Ramírez Rodríguez, Gerardo ^a   Babu, Harish ^b   Klempin, Friederike ^c   Krylyshkina, Olga ^d   Baekelandt, Veerle ^d   Gijsbers, Rik ^e   Debyser, Zeger ^e   Overall, Rupert W ^f   Nicola, Zeina ^f   Fabel, Klaus ^f,g   Kempermann, Gerd ^f,g  

^a INSTITUTO NACIONAL DE PSIQUIATRÍA RAMÓN DE LA FUENTE MUÑIZ   (Mexico)

^b STANFORD UNIVERSITY   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

^d UNIVERSITY OF LEUVEN   (Belgium)

^e DEPARTMENT OF PHARMACEUTICAL AND PHARMACOLOGICAL SCIENCES   (Belgium)

^f CENTER FOR REGENERATIVE THERAPIES DRESDEN   (Germany)

^g GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA CRYSTALLIN; GREEN FLUORESCENT PROTEIN; GROWTH FACTOR; HEAT SHOCK PROTEIN 22; NESTIN; NEURON SPECIFIC NUCLEAR PROTEIN; PROTEIN KINASE B;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BIOINFORMATICS; CELL SURVIVAL; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DENTATE GYRUS; ELECTROPORATION; FEMALE; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; MOUSE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEWBORN; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ADULT STEM CELLS; ALPHA-CRYSTALLINS; ANALYSIS OF VARIANCE; ANIMALS; BROMODEOXYURIDINE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; COMPUTATIONAL BIOLOGY; DENTATE GYRUS; FEMALE; GENE EXPRESSION REGULATION; GENETIC VECTORS; GREEN FLUORESCENT PROTEINS; HEAT-SHOCK PROTEINS, SMALL; MICE; MICE, INBRED C57BL; NERVE GROWTH FACTORS; NERVE TISSUE PROTEINS; NEUROGENESIS; NEURONS; RNA, MESSENGER; S100 PROTEINS; TIME FACTORS; TRANSFECTION;

EID: 84875417970     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.6452-11.2013     Document Type: Article

References (72)

1. Arndt V, Dick N, Tawo R, Dreiseidler M, Wenzel D, Hesse M, Fürst DO, Saftig P, Saint R, Fleischmann BK, Hoch M, Höhfeld J (2010) Chaperone-assisted selective autophagy is essential for muscle maintenance. Curr Biol 20:143-148. CrossRef Medline
2. Arthur DB, Georgi S, Akassoglou K, Insel PA (2006) Inhibition of apoptosis by P2Y2 receptor activation: novel pathways for neuronal survival. J Neurosci 26:3798-3804. CrossRef Medline
3. Babu H, Ramírez-Rodríguez G, Fabel K, Bischofberger J, Kempermann G (2009) Synaptic network activity induces neuronal differentiation of adult hippocampal precursor cells through BDNF signaling. Front Neurosci 3:49. CrossRef Medline
4. Babu H, Claasen JH, Kannan S, Rünker AE, Palmer T, Kempermann G (2011) A protocol for isolation and enriched monolayer cultivation of neural precursor cells from mouse dentate gyrus. Front Neurosci 5:89. CrossRef Medline
5. Bracko O, Singer T, Aigner S, Knobloch M, Winner B, Ray J, Clemenson GD Jr, Suh H, Couillard-Despres S, Aigner L, Gage FH, Jessberger S (2012) Gene expression profiling of neural stem cells and their neuronal progeny reveals IGF2 as a regulator of adult hippocampal neurogenesis. J Neurosci 10:3376-3387. CrossRef Medline
6. Brazil DP, Yang ZZ, Hemmings BA (2004) Advances in protein kinase B signalling: AKTion on multiple fronts. Trends Biochem Sci 29:233-242. CrossRef Medline
7. Carra S (2009) The stress-inducible HspB8-Bag3 complex induces the eIF2alpha kinase pathway: implications for protein quality control and viral factory degradation? Autophagy 5:428-429. CrossRef Medline
8. Carra S, Seguin SJ, Landry J (2008a) HspB8 and Bag3: a new chaperone complex targeting misfolded proteins to macroautophagy. Autophagy 4:237-239. Medline
9. Carra S, Seguin SJ, Lambert H, Landry J (2008b) HspB8 chaperone activity toward poly(Q)-containing proteins depends on its association with Bag3, a stimulator of macroautophagy. J Biol Chem 283:1437-1444. CrossRef Medline
10. Carra S, Brunsting JF, Lambert H, Landry J, Kampinga HH (2009) HspB8 participates in protein quality control by a non-chaperone-like mechanism that requires eIF2 phosphorylation. J Biol Chem 284:5523-5532. CrossRef Medline
11. Carra S, Boncoraglio A, Kanon B, Brunsting JF, Minoia M, Rana A, Vos MJ, Seidel K, Sibon OC, Kampinga HH (2010) Identification of the Drosophila ortholog of HSPB8: implication of HSPB8 loss of function in protein folding diseases. J Biol Chem 285:37811-37822. CrossRef Medline
12. Cleveland DW, Fischer SG, Kirschner MW, Laemmli UK (1977) Peptide mapping by limited proteolysis in sodium dodecyl sulfate and analysis by gel electrophoresis. J Biol Chem 252:1102-1106. Medline
13. Crippa V, Sau D, Rusmini P, Boncoraglio A, Onesto E, Bolzoni E, Galbiati M, Fontana E, Marino M, Carra S, Bendotti C, De Biasi S, Poletti A (2010) The small heat shock protein B8 (HspB8) promotes autophagic removal of misfolded proteins involved in amyotrophic lateral sclerosis (ALS). Hum Mol Genet 19:3440-3456. CrossRef Medline
14. Danan IJ, Rashed ER, Depre C (2007) Therapeutic potential of H11 kinase for the ischemic heart. Cardiovasc Drug Rev 25:14-29. CrossRef Medline
15. David JC, Boelens WC, Grongnet JF (2006) Up-regulation of heat shock protein HSP 20 in the hippocampus as an early response to hypoxia of the newborn. J Neurochem 99:570-581. CrossRef Medline
16. Deckwerth TL, Elliott JL, Knudson CM, Johnson EM Jr, Snider WD, Korsmeyer SJ (1996) BAX is required for neuronal death after trophic factor deprivation and during development. Neuron 17:401-411. CrossRef Medline
17. Dennis G Jr, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, Lempicki RA (2003) DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol 4:P3. CrossRef Medline
18. Depre C, Wang L, Sui X, Qiu H, Hong C, Hedhli N, Ginion A, Shah A, Pelat M, Bertrand L, Wagner T, Gaussin V, Vatner SF (2006) H11 kinase prevents myocardial infarction by preemptive preconditioning of the heart. Circ Res 98:280-288. CrossRef Medline
19. Fitzsimons CP, van Hooijdonk LWA, Schouten M, Zalachoras I, Brinks V, Zheng T, Schouten TG, Saaltink DJ, Dijkmans T, Steindler DA, Verhaagen J, Verbeek FJ, Lucassen P, de Kloet ER, Meijer OC, Karst H, Joels M, Oitzl MS, Vreugdenhil E (2012) Knockdown of the glucocorticoid receptor alters functional integration of newborn neurons in the adult hippocampus and impairs fear-motivated behavior. Mol Psych Advance online publication. Retrieved August 28, 2012. doi:10.1038/mp.2012.123. CrossRef Medline
20. Fuchs M, Poirier DJ, Seguin SJ, Lambert H, Carra S, Charette SJ, Landry J (2009) Identification of the key structural motifs involved in HspB8/ HspB6-Bag3 interaction. Biochem J 425:245-255. CrossRef Medline
21. Galea LA (2008) Gonadal hormone modulation of neurogenesis in the dentate gyrus of adult male and female rodents. Brain Res Rev 57:332-341. CrossRef Medline
22. Geraerts M, Eggermont K, Hernandez-Acosta P, Garcia-Verdugo JM, Baekelandt V, Debyser Z (2006) Lentiviral vectors mediate efficient and stable gene transfer in adult neural stem cells in vivo. Hum Gene Ther 17:635-650. CrossRef Medline
23. Gonzalez-Malerva L, Park J, Zou L, Hu Y, Moradpour Z, Pearlberg J, Sawyer J, Stevens H, Harlow E, LaBaer J (2011) High-throughput ectopic expression screen for tamoxifen resistance identifies an atypical kinase that blocks autophagy. Proc Natl Acad Sci U S A 108:2058-2063. CrossRef Medline
24. Gurusamy N, Lekli I, Gherghiceanu M, Popescu LM, Das DK (2009) BAG-1 induces autophagy for cardiac cell survival. Autophagy 5:120-121. CrossRef Medline
25. Hagemann TL, Boelens WC, Wawrousek EF, Messing A (2009) Suppression of GFAP toxicity by αB-crystallin in mouse models of Alexander disease. Human Mol Genet 18:1190-1199. CrossRef Medline
26. Huang da W, Sherman BT, Lempicki RA (2009a) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4:44-57. CrossRef Medline
27. Huang da W, Sherman BT, Zheng X, Yang J, Imamichi T, Stephens R, Lempicki RA (2009b) Extracting biological meaning from large gene lists with DAVID. Curr Protoc Bioinformatics 13:11. CrossRef Medline
28. Hudson AJ, Munoz DG (1997) A familial syndrome of congenital cataract, mental impairment, and dentate gyrus atrophy. Ann Neurol 41:512-520. CrossRef Medline
29. Hudson AJ, Munoz DG (2003) Familial dementia with dentate atrophy and failure of neurogenesis. Ann Neurol 53:420-421; author reply 421. CrossRef Medline
30. 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, et al (2004) Hot-spot residue in small heat-shock protein 22 causes distal motor neuropathy. Nat Genet 36:597-601. CrossRef Medline
31. Irobi J, Almeida-Souza L, Asselbergh B, De Winter V, Goethals S, Dierick I, Krishnan J, Timmermans JP, Robberecht W, De Jonghe P, Van Den Bosch L, Janssens S, Timmerman V (2010) Mutant HSPB8 causes motor neuron-specific neurite degeneration. Hum Mol Genet 19:3254-3265. CrossRef Medline
32. Jessberger S, Aigner S, Clemenson GD Jr, Toni N, Lie DC, Karalay O, Overall R, Kempermann G, Gage FH (2008) Cdk5 regulates accurate maturation of newborn granule cells in the adult hippocampus. PLoS Biol 6:e272. CrossRef Medline
33. Karch CM, Borchelt DR (2010) An examination of αB-crystallin as a modifier of SOD1 aggregate pathology and toxicity in models of familial amyotrophic lateral sclerosis. J Neurochem 113:1092-1100. CrossRef Medline
34. Kempermann G, Jessberger S, Steiner B, Kronenberg G (2004) Milestones of neuronal development in the adult hippocampus. Trends Neurosci 27:447-452. CrossRef Medline
35. Kempermann G, Chesler EJ, Lu L, Williams RW, Gage FH (2006) Natural variation and genetic covariance in adult hippocampal neurogenesis. Proc Natl Acad Sci U S A 103:780-785. CrossRef Medline
36. Kim JY, Duan X, Liu CY, Jang MH, Guo JU, Pow-anpongkul N, Kang E, Song H, Ming GL (2009) DISC regulates new neuron development in the adult brain via modulation of AKT-mTOR signaling through kiaa1212. Neuron 63:761-773. CrossRef Medline
37. Kim JY, Liu CY, Zhang F, Duan X, Wen Z, Song J, Feighery E, Lu B, Rujescu D, St Clair D, Christian K, Callicott JH, Weinberger DR, Song H, Ming GL (2012) Interplay between DISC1 and GABA signaling regulates neurogenesis in mice and risk for schizophrenia. Cell 148:1051-1064. CrossRef Medline
38. Kirbach BB, Golenhofen N (2011) Differential expression and induction of small heat shock proteins in rat brain and cultured hippocampal neurons. J Neurosci Res 89:162-175. CrossRef Medline
39. Koo JW, Russo SJ, Ferguson D, Nestler EJ, Duman RS (2010) Nuclear factor-B is a critical mediator of stress-impaired neurogenesis and depressive behavior. Proc Natl Acad Sci U S A 107:2669-2674. CrossRef Medline
40. Leuner B, Caponiti JM, Gould E (2012) Oxytocin stimulates adult neurogenesis even under conditions of stress and elevated glucocorticoids. Hippocampus 22:861-868. CrossRef Medline
41. Levine B, Kroemer G (2008) Autophagy in the pathogenesis of disease. Cell 132:27-42. CrossRef Medline
42. Lie DC, Colamarino SA, Song HJ, Désiré L, Mira H, Consiglio A, Lein ES, Jessberger S, Lansford H, Dearie AR, Gage FH (2005) Wnt signaling regulates adult hippocampal neurogenesis. Nature 437:1370-1375. CrossRef Medline
43. Louissant A Jr, Rao S, Leventhal C, Goldman SA (2002) Coordinated inter-action of angiogenesis and neurogenesis in the adult songbird brain. Neuron 34:945-960. CrossRef Medline
44. Mastrangelo MA, Sudol KL, Narrow WC, Bowers WJ (2009) Interferon-differentially affects Alzheimer's disease pathologies and induces neurogenesis in triple transgenic-AD mice. Am J Pathol 175:2076-2088. CrossRef Medline
45. McCollum AK, Casagrande G, Kohn EC (2009) Caught in the middle: the role of Bag3 in disease. Biochem J 425:e1-e3. CrossRef Medline
46. Mueller AD, Pollock MS, Lieblich SE, Epp JR, Galea LA, Mistlberger RE (2008) Sleep deprivation can inhibit adult hippocampal neurogenesis independent of adrenal stress hormones. Am J Physiol Regul Integr Comp Physiol 294:R1693-R1703. CrossRef Medline
47. Ninkovic J, Pinto L, Petricca S, Lepier A, Sun J, Rieger MA, Schroeder T, Cvekl A, Favor J, Götz M (2010) The transcription factor Pax6 regulates survival of dopaminergic olfactory bulb neurons via crystallin A. Neuron 68:682-694. CrossRef Medline
48. Overall RW, Kempermann G, Peirce J, Lu L, Goldowitz D, Gage FH, Goodwin S, Smit AB, Airey DC, Rosen GD, Schalkwyk LC, Sutter TR, Nowakowski RS, Whatley S, Williams RW (2009) Genetics of the hippocampal transcriptome in mouse: a systematic survey and online neurogenomics resource. Front Neurosci 3:55. CrossRef Medline
49. Palmer TD, Willhoite AR, Gage FH (2000) Vascular niche for adult hippocampal neurogenesis. J Comp Neurol 425:479-494. CrossRef Medline
50. Pawluski JL, Brummelte S, Barha CK, Crozier TM, Galea LA (2009) Effects of steroid hormones on neurogenesis in the hippocampus of the adult female rodent during the estrous cycle, pregnancy, lactation and aging. Front Neuroendocrinol 30:343-357. CrossRef Medline
51. Peng Q, Masuda N, Jiang M, Li Q, Zhao M, Ross CA, Duan W (2008) The antidepressant sertraline improves the phenotype, promotes neurogenesis and increases BDNF levels in the R6/2 Huntington's disease mouse model. Exp Neurol 210:154-163. CrossRef Medline
52. Perera TD, Coplan JD, Lisanby SH, Lipira CM, Arif M, Carpio C, Spitzer G, Santarelli L, Scharf B, Hen R, Rosoklija G, Sackeim HA, Dwork AJ (2007) Antidepressant-induced neurogenesis in the hippocampus of adult non-human primates. J Neurosci 27:4894-4901. CrossRef Medline
53. Pieper AA, Xie S, Capota E, Estill SJ, Zhong J, Long JM, Becker GL, Huntington P, Goldman SE, Shen CH, Capota M, Britt JK, Kotti T, Ure K, Brat DJ, Williams NS, MacMillan KS, Naidoo J, Melito L, Hsieh J, De Brabander J, Ready JM, McKnight SL (2010) Discovery of a proneurogenic, neuroprotective chemical. Cell 142:39-51. CrossRef Medline
54. Pinnock SB, Herbert J (2008) Brain-derived neurotropic factor and neuro-genesis in the adult rat dentate gyrus: interactions with corticosterone. Eur J Neurosci 27:2493-2500. CrossRef Medline
55. Putcha GV, Deshmukh M, Johnson EM Jr (1999) BAX translocation is a critical event in neuronal apoptosis: regulation by neuroprotectants, BCL-2, and caspases. J Neurosci 19:7476-7485. Medline
56. Quraishe S, Asuni A, Boelens WC, O'Connor V, Wyttenbach A (2008) Expression of the small heat shock protein family in the mouse CNS: differential anatomical and biochemical compartmentalization. Neuroscience 153:483-491. CrossRef Medline
57. Ramírez-Rodríguez G, Klempin F, Babu H, Benítez-King G, Kempermann G (2009) Melatonin modulates cell survival of new neurons in the hippocampus of adult mice. Neuropsychopharmacology 34:2180-2191. CrossRef Medline
58. Ramírez-Rodríguez G, Ortíz-López L, Domínguez-Alonso A, Benítez-King GA, Kempermann G (2011) Chronic treatment with melatonin stimulates dendrite maturation and complexity in adult hippocampal neurogenesis of mice. J Pineal Res 50:29-37. CrossRef Medline
59. Rossi C, Angelucci A, Costantin L, Braschi C, Mazzantini M, Babbini F, Fabbri ME, Tessarollo L, Maffei L, Berardi N, Caleo M (2006) Brain-derived neurotrophic factor (BDNF) is required for the enhancement of hippocampal neurogenesis following environmental enrichment. Eur J Neurosci 24:1850-1856. CrossRef Medline
60. Sahay A, Scobie KN, Hill AS, O'Carroll CM, Kheirbek MA, Burghardt NS, Fenton AA, Dranovsky A, Hen R (2011) Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature 472:466-470. CrossRef Medline
61. Sanbe A, Daicho T, Mizutani R, Endo T, Miyauchi N, Yamauchi J, Tanonaka K, Glabe C, Tanoue A (2009) Protective effect of geranylgeranylacetone via enhancement of HSPB8 induction in desmin-related cardiomyopathy. PLoS One 4:e5351. CrossRef Medline
62. Seidel K, Vinet J, Dunnen WF, Brunt ER, Meister M, Boncoraglio A, Zijlstra MP, Boddeke HW, Rub U, Kampinga HH, Carra S (2012) The Hspb8-BAG3 chaperone complex is upregulated in astrocytes in the human brain affected by protein aggregation diseases. Neurophatol Appl Neurobiol 1:39-53. CrossRef Medline
63. Shemetov AA, Seit-Nebi AS, Gusev NB (2011) Phosphorylation of human small heat shock protein HspB8 (Hsp22). Mol Cell Biochem 1:47-55. CrossRef Medline
64. Snel B, Lehmann G, Bork P, Huynen MA (2000) STRING: a web-server to retrieve and display the repeatedly occurring neighbourhood of a gene. Nucleic Acids Res 28:3442-3444. CrossRef Medline
65. Sui X, Li D, Qiu H, Gaussin V, Depre C (2009) Activation of the bone morphogenetic protein receptor by H11kinase/Hsp22 promotes cardiac cell growth and survival. Circ Res 104:887-895. CrossRef Medline
66. Szklarczyk D, Franceschini A, Kuhn M, Simonovic M, Roth A, Minguez P, Doerks T, Stark M, Muller J, Bork P, Jensen LJ, von Mering C (2011) The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored. Nucleic Acids Res 39:D561-D568. CrossRef Medline
67. Tang D, Khaleque MA, Jones EL, Theriault JR, Li C, Wong WH, Stevenson MA, Calderwood SK (2005) Expression of heat shock proteins and heat shock protein messenger ribonucleic acid in human prostate carcinoma in vitro and in tumors in vivo. Cell Stress Chaperones 10:46-58. CrossRef Medline
68. van Hooijdonk LW, Ichwan M, Dijkmans TF, Schouten TG, de Backer MW, Adan RA, Verbeek FJ, Vreugdenhil E, Fitzsimons CP (2009) Lentivirus-mediated transgene delivery to the hippocampus reveals sub-field specific differences in expression. BMC Neurosci 10:2. CrossRef Medline
69. Wang L, Zajac A, Hedhli N, Depre C (2004) Increased expression of H11 kinase stimulates glycogen synthesis in the heart. Mol Cell Biochem 265: 71-78. CrossRef Medline
70. Wilhelmus MM, Boelens WC, Otte-Höller I, Kamps B, Kusters B, Maat-Schieman ML, de Waal RM, Verbeek MM (2006) Small heat shock protein HspB8: its distribution in Alzheimer's disease brains and its inhibition of amyloid-β protein aggregation and cerebrovascular amyloidtoxicity. Acta Neuropathol 111:139-149. CrossRef Medline
71. Yew EH, Cheung NS, Choy MS, Qi RZ, Lee AY, Peng ZF, Melendez AJ, Manikandan J, Koay ES, Chiu LL, Ng WL, Whiteman M, Kandiah J, Halliwell B (2005) Proteasome inhibition by lactacystin in primary neuronal cells induces both potentially neuroprotective and proapoptotic transcriptional responses: a microarray analysis. J Neurochem 94:943-956. CrossRef Medline
72. Zhang L, Blomgren K, Kuhn HG, Cooper-Kuhn CM (2009) Effects of postnatal thyroid hormone deficiency on neurogenesis in the juvenile and adult rat. Neurobiol Dis 34:366-374. CrossRef Medline