Stress-induced localization of HSPA6 (HSP70B) and HSPA1A (HSP70-1) proteins to centrioles in human neuronal cells

Cell Stress and Chaperones

Volumn 19, Issue 3, 2014, Pages 321-327

  Khalouei, Sam ^a   Chow, Ari M ^a   Brown, Ian R ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Centrioles; Heat shock; HSPA1A (HSP70 1); HSPA6 (HSP70B); SH SY5Y human neuronal cells

Indexed keywords

GAMMA TUBULIN; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 70 1; HEAT SHOCK PROTEIN 70B; UNCLASSIFIED DRUG; YELLOW FLUORESCENT PROTEIN; HSP70B' PROTEIN, HUMAN; HSPA1A PROTEIN, HUMAN; HYBRID PROTEIN;

ARTICLE; CELL MIGRATION; CELL POLARITY; CENTRIOLE; CONTROLLED STUDY; CYTOPLASM; GENE; HUMAN; HUMAN CELL; NERVE CELL; NERVE CELL DIFFERENTIATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; TEMPERATURE STRESS; CELL LINE; CYTOLOGY; HEAT SHOCK RESPONSE; METABOLISM; PHYSIOLOGICAL STRESS; PROTEIN TRANSPORT;

CELL LINE; CENTRIOLES; HEAT-SHOCK RESPONSE; HSP70 HEAT-SHOCK PROTEINS; HUMANS; NEURONS; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; STRESS, PHYSIOLOGICAL;

EID: 84899115233     PISSN: 13558145     EISSN: 14661268     Source Type: Journal    
DOI: 10.1007/s12192-013-0459-2     Document Type: Article

References (70)

1. Ali YO, Kitay BM, Zhai RG (2010) Dealing with misfolded proteins: examining the neuroprotective role of molecular chaperones in neurodegeneration. Molecules 15:6859-6887. doi: 10.3390/molecules15106859
2. Asea AA, Brown IR (2008) Heat shock proteins and the brain: implications for neurodegenerative diseases and neuroprotection. Springer, New York
3. Avila J, Lucas JJ, Hernandez F (eds) (2011) Animal models for neurodegenerative disease. RSC, Cambridge. doi: 10.1039/9781849732758
4. Azimzadeh J, Bornens M (2007) Structure and duplication of the centrosome. J Cell Sci 120:2139-2142. doi: 10.1242/jcs.005231
5. Azimzadeh J, Marshall WF (2010) Building the centriole. Curr Biol 20:R816-R825. doi: 10.1016/j.cub.2010.08.010
6. Badano JL, Teslovich TM, Katsanis N (2005) The centrosome in human genetic disease. Nat Rev Genet 6:194-205. doi: 10.1038/nrg1557
7. Barnes AP, Polleux F (2009) Establishment of axon-dendrite polarity in developing neurons. Ann Rev Neurosci 32:347-381. doi: 10.1146/annurev.neuro.31. 060407.125536
8. Baudoin JP, Viou L, Launay PS, Luccardini C, Espeso Gil S, Kiyasova V, Irinopoulou T, Alvarez C, Rio JP, Boudier T, Lechaire JP, Kessaris N, Spassky N, Metin C (2012) Tangentially migrating neurons assemble a primary cilium that promotes their reorientation to the cortical plate. Neuron 76:1108-1122. doi: 10.1016/j.neuron.2012.10.027
9. Bettencourt-Dias M, Glover DM (2007) Centrosome biogenesis and function: centrosomics brings new understanding. Nat Rev Mol Cell Biol 8:451-463. doi: 10.1038/nrm2180
10. Bornens M (2002) Centrosome composition and microtubule anchoring mechanisms. Curr Opin Cell Biol 14:25-34. doi: 10.1016/S0955-0674(01)00290-3
11. Bornens M (2012) The centrosome in cells and organisms. Science 335:422-426. doi: 10.1126/science.1209037
12. Bradshaw NJ, Ogawa F, Antolin-Fontes B, Chubb JE, Carlyle BC, Christie S, Claessens A, Porteous DJ, Millar JK (2008) DISC1, PDE4B, and NDE1 at the centrosome and synapse. Biochem Biophys Res Commun 377:1091-1096. doi: 10.1016/j.bbrc.2008.10.120
13. Breunig JJ, Sarkisian MR, Arellano JI, Morozov YM, Ayoub AE, Sojitra S, Wang B, Flavell RA, Rakic P, Town T (2008) Primary cilia regulate hippocampal neurogenesis by mediating sonic hedgehog signaling. Proc Natl Acad Sci U S A 105:13127-13132. doi: 10.1073/pnas.0804558105
14. Brito DA, Gouveia SM, Bettencourt-Dias M (2012) Deconstructing the centriole: structure and number control. Curr Opin Cell Biol 24:4-13. doi: 10.1016/j.ceb.2012.01.003
15. Brocchieri L, de Conway Macario E, Macario AJ (2008) Hsp70 genes in the human genome: conservation and differentiation patterns predict a wide array of overlapping and specialized functions. BMC Evol Biol 8:19. doi: 10.1186/1471-2148-8-19
16. Brown IR (2007) Heat shock proteins and protection of the nervous system. Ann N Y Acad Sci 1113:147-158. doi: 10.1196/annals.1391.032
17. Brown CR, Hong-Brown LQ, Doxsey SJ, Welch WJ (1996) Molecular chaperones and the centrosome. A role for HSP 73 in centrosomal repair following heat shock treatment. J Biol Chem 271:833-840. doi: 10.1074/jbc.271.2.833
18. Chow AM, Brown IR (2007) Induction of heat shock proteins in differentiated human and rodent neurons by celastrol. Cell Stress Chaperones 12:237-244. doi: 10.1379/CSC-269.1
19. Chow AM, Steel R, Anderson RL (2009) Hsp72 chaperone function is dispensable for protection against stress-induced apoptosis. Cell Stress Chaperones 14:253-263. doi: 10.1007/s12192-008-0079-4
20. Chow AM, Mok P, Xiao D, Khalouei S, Brown IR (2010) Heteromeric complexes of heat shock protein 70 (HSP70) family members, including Hsp70B, in differentiated human neuronal cells. Cell Stress Chaperones. doi: 10.1007/s12192-009-0167-0
21. Chow AM, Tang DW, Hanif A, Brown IR (2013) Induction of heat shock proteins in cerebral cortical cultures by celastrol. Cell Stress Chaperones 18:155-160. doi: 10.1007/s12192-012-0364-0
22. Clowry G, Molnar Z, Rakic P (2010) Renewed focus on the developing human neocortex. J Anat 217:276-288. doi: 10.1111/j.1469-7580.2010.01281.x
23. Culmsee C, Landshamer S (2006) Molecular insights into mechanisms of the cell death program: role in the progression of neurodegenerative disorders. Curr Alzheimer Res 3:269-283. doi: 10.2174/156720506778249461
24. Daugaard M, Rohde M, Jaattela M (2007) The heat shock protein 70 family: highly homologous proteins with overlapping and distinct functions. FEBS Lett 581:3702-3710. doi: 10.1016/j.febslet.2007.05.039
25. de Anda FC, Tsai LH (2011) Axon selection: from a polarized cytoplasm to a migrating neuron. Commun Integr Biol 4:304-307. doi: 10.4161/cib.4.3.14781
26. de Anda FC, Meletis K, Ge X, Rei D, Tsai LH (2010) Centrosome motility is essential for initial axon formation in the neocortex. J Neurosci 30:10391-10406. doi: 10.1523/JNEUROSCI.0381-10.2010
27. Di Carlo M, Giacomazza D, San Biagio PL (2012) Alzheimer's disease: biological aspects, therapeutic perspectives and diagnostic tools. J Phys Condens Matter 24:244102. doi: 10.1088/0953-8984/24/24/244102
28. Diaz-Corrales FJ, Asanuma M, Miyazaki I, Miyoshi K, Ogawa N (2005) Rotenone induces aggregation of gamma-tubulin protein and subsequent disorganization of the centrosome: relevance to formation of inclusion bodies and neurodegeneration. Neuroscience 133:117-135. doi: 10.1016/j.neuroscience. 2005.01.044
29. Diaz-Corrales FJ, Miyazaki I, Asanuma M, Ruano D, Rios RM (2011) Centrosomal aggregates and Golgi fragmentation disrupt vesicular trafficking of DAT. Neurobiol Aging 33:2462-2477. doi: 10.1016/j.neurobiolaging.2011.11.014
30. Evans CG, Chang L, Gestwicki JE (2010) Heat shock protein 70 (hsp70) as an emerging drug target. J Med Chem 53:4585-4602. doi: 10.1021/jm100054f
31. Gestwicki JE, Garza D (2012) Protein quality control in neurodegenerative disease. Prog Mol Biol Transl Sci 107:327-353. doi: 10.1016/B978-0-12-385883-2. 00003-5
32. Gonczy P (2012) Towards a molecular architecture of centriole assembly. Nat Rev Mol Cell Biol 13:425-435. doi: 10.1038/nrm3373
33. Green JA, Mykytyn K (2010) Neuronal ciliary signaling in homeostasis and disease. Cell Mol Life Sci 67:3287-3297. doi: 10.1007/s00018-010-0425-4
34. Hageman J, van Waarde MA, Zylicz A, Walerych D, Kampinga HH (2011) The diverse members of the mammalian HSP70 machine show distinct chaperone-like activities. Biochem J 435:127-142. doi: 10.1042/BJ20101247
35. Higginbotham HR, Gleeson JG (2007) The centrosome in neuronal development. Trends Neurosci 30:276-283. doi: 10.1016/j.tins.2007.04.001
36. Hirsch EC (2007) Animal models in neurodegenerative diseases. J Neural Transm Suppl:87-90. doi: 10.1007/978-3-211-73574-9-11
37. Hut HM, Kampinga HH, Sibon OC (2005) Hsp70 protects mitotic cells against heat-induced centrosome damage and division abnormalities. Mol Biol Cell 16:3776-3785. doi: 10.1091/mbc.E05-01-0038
38. Kampinga HH, Hageman J, Vos MJ, Kubota H, Tanguay RM, Bruford EA, Cheetham ME, Chen B, Hightower LE (2009) Guidelines for the nomenclature of the human heat shock proteins. Cell Stress Chaperones 14:105-111. doi: 10.1007/s12192-008-0068-7
39. Kempermann G (2012) New neurons for 'survival of the fittest'. Nat Rev Neurosci 13:727-736. doi: 10.1038/nrn3319
40. Kiang JG, Tsokos GC (1998) Heat shock protein 70 kDa: molecular biology, biochemistry, and physiology. Pharmacol Ther 80:183-201. doi: 10.1016/S0163-7258(98)00028-X
41. Kim YE, Hipp MS, Bracher A, Hayer-Hartl M, Ulrich Hartl F (2013) Molecular chaperone functions in protein folding and proteostasis. Annu Rev Biochem 82:323-355. doi: 10.1146/annurev-biochem-060208-092442
42. Kuijpers M, Hoogenraad CC (2011) Centrosomes, microtubules and neuronal development. Mol Cell Neurosci 48:349-358. doi: 10.1016/j.mcn.2011.05.004
43. Lee JE, Gleeson JG (2011) Cilia in the nervous system: linking cilia function and neurodevelopmental disorders. Curr Opin Neurol 24:98-105. doi: 10.1097/WCO.0b013e3283444d05
44. Letinic K, Rakic P (2001) Telencephalic origin of human thalamic GABAergic neurons. Nat Neurosci 4:931-936. doi: 10.1038/nn0901-931
45. Lindsey BW, Tropepe V (2006) A comparative framework for understanding the biological principles of adult neurogenesis. Prog Neurobiol 80:281-307. doi: 10.1016/j.pneurobio.2006.11.007
46. LoTurco JJ, Bai J (2006) The multipolar stage and disruptions in neuronal migration. Trends Neurosci 29:407-413. doi: 10.1016/j.tins.2006.05.006
47. Louvi A, Grove EA (2011) Cilia in the CNS: the quiet organelle claims center stage. Neuron 69:1046-1060. doi: 10.1016/j.neuron.2011.03.002
48. Ma Z, Izumi H, Kanai M, Kabuyama Y, Ahn NG, Fukasawa K (2006) Mortalin controls centrosome duplication via modulating centrosomal localization of p53. Oncogene 25:5377-5390. doi: 10.1038/sj.onc.1209543
49. Mehler MF, Gokhan S (2000) Mechanisms underlying neural cell death in neurodegenerative diseases: alterations of a developmentally-mediated cellular rheostat. Trends Neurosci 23:599-605. doi: 10.1016/S0166-2236(00)01705-7
50. Ming GL, Song H (2011) Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron 70:687-702. doi: 10.1016/j.neuron.2011.05.001
51. Molla-Herman A, Boularan C, Ghossoub R, Scott MG, Burtey A, Zarka M, Saunier S, Concordet JP, Marullo S, Benmerah A (2008) Targeting of beta-arrestin2 to the centrosome and primary cilium: role in cell proliferation control. PLoS One 3:e3728. doi: 10.1371/journal.pone.0003728
52. Muchowski PJ, Wacker JL (2005) Modulation of neurodegeneration by molecular chaperones. Nat Rev Neurosci 6:11-22. doi: 10.1038/nrn1587
53. Murman DL (2012) Early treatment of Parkinson's disease: opportunities for managed care. Am J Manag Care 18:S183-S188
54. Nadarajah B, Brunstrom JE, Grutzendler J, Wong RO, Pearlman AL (2001) Two modes of radial migration in early development of the cerebral cortex. Nat Neurosci 4:143-150. doi: 10.1038/83967
55. Nigg EA, Stearns T (2011) The centrosome cycle: centriole biogenesis, duplication and inherent asymmetries. Nat Cell Biol 13:1154-1160. doi: 10.1038/ncb2345
56. Noonan EJ, Place RF, Giardina C, Hightower LE (2007a) Hsp70B regulation and function. Cell Stress Chaperones 12:393-402. doi: 10.1379/CSC-278e.1
57. Noonan EJ, Place RF, Rasoulpour RJ, Giardina C, Hightower LE (2007b) Cell number-dependent regulation of Hsp70B expression: evidence of an extracellular regulator. J Cell Physiol 210:201-211. doi: 10.1002/jcp.20875
58. Noonan EJ, Fournier G, Hightower LE (2008a) Surface expression of Hsp70B in response to proteasome inhibition in human colon cells. Cell Stress Chaperones 13:105-110. doi: 10.1007/s12192-007-0003-3
59. Noonan EJ, Giardina C, Hightower L (2008b) Hsp70B and Hsp72 form a complex in stressed human colon cells and each contributes to cytoprotection. Exp Cell Res 314:2468-2476. doi: 10.1016/j.yexcr.2008.05.002
60. Phillips W, Michell A, Pruess H, Barker RA (2009) Animal models of neurodegenerative diseases. Methods Mol Biol 549:137-155. doi: 10.1007/978-1-60327-931-4-10
61. Prodromou NV, Thompson CL, Osborn DP, Cogger KF, Ashworth R, Knight MM, Beales PL, Chapple JP (2012) Heat shock induces rapid resorption of primary cilia. J Cell Sci 125:4297-4305. doi: 10.1242/jcs.100545
62. Rao Y, Wu JY (2001) Neuronal migration and the evolution of the human brain. Nat Neurosci 4:860-862. doi: 10.1038/nn0901-860
63. Scieglinska D, Piglowski W, Mazurek A, Malusecka E, Zebracka J, Filipczak P, Krawczyk Z (2008) The HspA2 protein localizes in nucleoli and centrosomes of heat shocked cancer cells. J Cell Biochem 104:2193-2206. doi: 10.1002/jcb.21778
64. Smith KJ, Twal WO, Soodavar F, Virella G, Lopes-Virella MF, Hammad SM (2010) Heat shock protein 70B' (HSP70B') expression and release in response to human oxidized low density lipoprotein immune complexes in macrophages. J Biol Chem 285:15985-15993. doi: 10.1074/jbc.M110.113605
65. Spassky N, Han YG, Aguilar A, Strehl L, Besse L, Laclef C, Ros MR, Garcia-Verdugo JM, Alvarez-Buylla A (2008) Primary cilia are required for cerebellar development and Shh-dependent expansion of progenitor pool. Dev Biol 317:246-259. doi: 10.1016/j.ydbio.2008.02.026
66. Tavaria M, Gabriele T, Kola I, Anderson RL (1996) A hitchhiker's guide to the human Hsp70 family. Cell Stress Chaperones 1:23-28
67. Tritarelli A, Oricchio E, Ciciarello M, Mangiacasale R, Palena A, Lavia P, Soddu S, Cundari E (2004) p53 localization at centrosomes during mitosis and postmitotic checkpoint are ATM-dependent and require serine 15 phosphorylation. Mol Biol Cell 15:3751-3757. doi: 10.1091/mbc.E03-12-0900
68. Tsai LH, Gleeson JG (2005) Nucleokinesis in neuronal migration. Neuron 46:383-388. doi: 10.1016/j.neuron.2005.04.013
69. Young JC (2010) Mechanisms of the Hsp70 chaperone system. Biochem Cell Biol 88:291-300. doi: 10.1139/o09-175
70. Zhu X, Zhao X, Burkholder WF, Gragerov A, Ogata CM, Gottesman ME, Hendrickson WA (1996) Structural analysis of substrate binding by the molecular chaperone DnaK. Science 272:1606-1614. doi: 10.1126/science.272.5268.1606