Hypothermic Preconditioning Reverses Tau Ontogenesis in Human Cortical Neurons and is Mimicked by Protein Phosphatase 2A Inhibition

EBioMedicine

Volumn 3, Issue , 2016, Pages 141-154

  Rzechorzek, Nina M ^a,b,c   Connick, Peter ^c   Livesey, Matthew R ^c   Borooah, Shyamanga ^b,c   Patani, Rickie ^c,d   Burr, Karen ^b,c   Story, David ^b,c   Wyllie, David J A ^c   Hardingham, Giles E ^c   Chandran, Siddharthan ^a,b,c  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Human cortical neuron; Hyperphosphorylation; Hypothermia; Neuroprotection; Preconditioning; Protein phosphatase 2A (PP2A); Tau protein

Indexed keywords

CASPASE 3; FOSTRIECIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PHOSPHOPROTEIN PHOSPHATASE 2A; GLUTAMIC ACID; PHOSPHOPROTEIN PHOSPHATASE 2; TAU PROTEIN;

ANTIBODY LABELING; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CELL COUNT; CELL DIFFERENTIATION; CONTROLLED STUDY; ELECTROPHORETIC MOBILITY; ENZYME ACTIVITY; EXCITOTOXIC SPINAL CORD INJURY; HUMAN; HUMAN CELL; HYPOTHERMIA; IMMUNOREACTIVITY; NERVE CELL DIFFERENTIATION; NEUROPROTECTION; ONTOGENY; OXIDATIVE STRESS; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING; ANTAGONISTS AND INHIBITORS; BRAIN CORTEX; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION; GENETICS; INDUCED HYPOTHERMIA; METABOLISM; NERVE CELL; NEURAL STEM CELL; PHOSPHORYLATION; TEMPERATURE;

CEREBRAL CORTEX; GENE EXPRESSION; GLUTAMIC ACID; HUMANS; HYPOTHERMIA; HYPOTHERMIA, INDUCED; NEURAL STEM CELLS; NEURONS; OXIDATIVE STRESS; PHOSPHORYLATION; PROTEIN PHOSPHATASE 2; RECEPTORS, N-METHYL-D-ASPARTATE; TAU PROTEINS; TEMPERATURE;

EID: 84958946375     PISSN: None     EISSN: 23523964     Source Type: Journal    
DOI: 10.1016/j.ebiom.2015.12.010     Document Type: Article

References (46)

1. Aarts E., Verhage M., Veenvliet J.V., Dolan C.V., van der Sluis S. A solution to dependency: using multilevel analysis to accommodate nested data. Nat. Neurosci. 2014, 17:491-496.
2. Andrews P.J.D., Sinclair L., Rodriguez A., Harris B.A., Battison C.G., Rhodes J.K.J., Murray G.D. Hypothermia for intracranial hypertension after traumatic brain injury. N. Engl. J. Med. 2015, Eurotherm3235 Trial Collaborators, (Epub ahead of print).
3. Antonic A., Dottori M., Leung J., Sidon K., Batchelor P.E., Wilson W., Macleod M.R., Howells D.W. Hypothermia protects human neurons. Int. J. Stroke 2014, 9:544-552.
4. Arendt T., Stieler J., Strijkstra A.M., Hut R.A., Rüdiger J., Van der Zee E.A., Harkany T., Holzer M., Härtig W. Reversible paired helical filament-like phosphorylation of tau is an adaptive process associated with neuronal plasticity in hibernating animals. J. Neurosci. 2003, 23:6972-6981.
5. Bilican B., Livesey M.R., Haghi G., Qiu J., Burr K., Siller R., Hardingham G.E., Wyliie D.J., Chandran S. Physiological normoxia and absence of EGF is required for the long-term propagation of anterior neural precursors from human pluripotent cells. PLoS One 2014, 9:e85932.
6. Bretteville A., Marcouiller F., Julien C., El Khoury N.B., Petry F.R., Poitras I., Mouqinot D., Levesque G., Hebert S.S., Planel E. Hypothermia-induced hyperphosphorylation: a new model to study tau kinase inhibitors. Sci. Rep. 2012, 2:480.
7. Brion J.-P., Smith C., Couck A.-M., Gallo J.-M., Anderton B.H. Developmental changes in tau phosphorylation: fetal τ is transiently phosphorylated in a manner similar to paired helical filament-τ characteristic of Alzheimer's disease. J. Neurochem. 1993, 61:2071-2080.
8. Busto R., Globus M.Y., Dietrich W.D., Martinez E., Valdés I., Ginsberg M.D. Effect of mild hypothermia on ischemia-induced release of neurotransmitters and free fatty acids in rat brain. Stroke 1989, 20:904-910.
9. Chip S., Zelmer A., Ogunshola O.O., Felderhoff-Mueser U., Nitsch C., Bührer C., Wellmann S. The RNA binding protein RBM3 is involved in hypothermia induced neuroprotection. Neurobiol. Dis. 2011, 43:388-396.
10. Dietrich W.D., Atkins C.M., Bramlett H.M. Protection in animal models of brain and spinal cord injury with mild to moderate hypothermia. J. Neurotrauma 2009, 26:301-312.
11. Espuny-Camacho I., Michelsen K.A., Gall D., Linaro D., Hasche A., Bonnefont J., Bali C., Orduz D., Bilheu A., Herpoel A., et al. Pyramidal neurons derived from human pluripotent stem cells integrate efficiently into mouse brain circuits in vivo. Neuron 2013, 77:440-456.
12. Goedert M., Jakes R. Expression of separate isoforms of human tau protein: correlation with the tau pattern in brain and effects on tubulin polymerization. EMBO J. 1990, 9:4225-4230.
13. Goedert M., Spillantini M.G., Jakes R., Rutherford D., Crowther R.A. Multiple isoforms of human microtubule-associated protein tau: sequences and localization in neurofibrillary tangles of Alzheimer's disease. Neuron 1989, 3:519-526.
14. Goedert M., Spillantini M.G., Potier M.C., Ulrich J., Crowther R.A. Cloning and sequencing of the cdna encoding an isoform of microtubule-associated protein tau containing four tandem repeats: differential expression of tau protein MRNAs in human brain. EMBO J. 1989, 8:393-399.
15. Gong C.X., Lidsky T., Wegiel J., Zuck L., Grundke-Iqbal I., Iqbal K. Phosphorylation of microtubule-associated protein tau is regulated by protein phosphatase 2A in mammalian brain. Implications for neurofibrillary degeneration in Alzheimer's disease. J. Biol. Chem. 2000, 275:5535-5544.
16. Gupta K., Hardingham G.E., Chandran S. NMDA receptor-dependent glutamate excitotoxicity in human embryonic stem cell-derived neurons. Neurosci. Lett. 2013, 543:95-100.
17. Hardingham G.E., Bading H. Synaptic versus extrasynaptic NMDA receptor signalling: implications for neurodegenerative disorders. Nat. Rev. Neurosci. 2010, 11:682-696.
18. Iqbal K., Liu F., Gong C.X., Alonso Adel C., Grundke-Iqbal I. Mechanisms of tau-induced neurodegeneration. Acta Neuropathol. 2009, 118:53-69.
19. Jacobs S.E., Berg M., Hunt R., Tarno-Mordi W.O., Inder T.E., Davis P.G. Cooling for newborns with hypoxic ischaemic encephalopathy. Cochrane Database Syst. Rev. 2013, 1:CD003311.
20. James O.T., Livesey M.R., Qiu J., Dando O., Bilican B., Haghi G., Rajan R., Burr K., Hardingham G.E., Chandran S., Kind P.C., Wyllie D.J. Ionotropic GABA and glycine receptor subunit composition in human pluripotent stem cell-derived cortical neurones. J. Physiol. 2014, 592:4353-4363.
21. Janke C., Beck M., Stahl T., Holzer M., Brauer K., Bigl V., Arendt T. phylogenetic diversity of the expression of the microtubule associated protein tau: implications for neurodegenerative disorders. Brain Res. Mol. Brain Res. 1999, 68:119-128.
22. Li H.-L., Wang H.H., Liu S.J., Deng Y.Q., Zhang Y.J., Tian Q., Wang X.C., Chen X.Q., Yang Y., Zhang J.Y. Phosphorylation of tau antagonizes apoptosis by stabilizing β-catenin, a mechanism involved in Alzheimer's neurodegeneration. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:3591-3596.
23. Liu X.A., Song J., Jiang Q., Wang Q., Tian Q., Wang J.Z. Expression of the hyperphosphorylated tau attenuates ER stress-induced apoptosis with upregulation of unfolded protein response. Apoptosis 2012, 17:1039-1049.
24. AR reversal potential in hPSC-derived cortical neurons. J. Neurosci. 2014, 34:4070-4075.
25. Lleonart M.E. A new generation of proto-oncogenes: cold-inducible RNA binding proteins. Biochim. Biophys. Acta 2010, 1805:43-52.
26. Lopresti P., Szuchet S., Papasozoomenos S.C., Zinkowski R.P., Binder L.I. Functional implications for the microtubule-associated protein tau: localization in oligodendrocytes. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:10369-10373.
27. Matsuo E.S., Shin R.W., Billingsley M.L., Van deVoorde A., O'Connor M., Trojanowski J.Q., Lee V.M. Biopsy-derived adult human brain tau is phosphorylated at many of the same sites as Alzheimer's disease paired helical filament tau. Neuron 1994, 13:989-1002.
28. Mawal-Dewan M., Henley J., Ven de Voorde A., Trojanowski J.Q., Lee V.M. The phosphorylation state of tau in the developing rat brain is regulated by phosphoprotein phosphatases. J. Biol. Chem. 1994, 269:30981-30987.
29. Meares G.P., Mines M.A., Beurel E., Eom T.Y., Song L., Zmijewska A.A., Jope R.S. Glycogen synthase kinase-3 regulates endoplasmic reticulum (ER) stress-induced CHOP expression in neuronal cells. Exp. Cell Res. 2011, 317:1621-1628.
30. Mondragon-Rodriguez S., Trillaud-Doppia E., Dudilot A., Bourgeois C., Lauzon M., Leclerc N., Boehm J. Interaction of endogenous tau with synaptic proteins is regulated by NMDA-receptor dependent tau phosphorylation. J. Biol. Chem. 2012, 287:32040-32053.
31. Papadia S., Soriano F.X., Léveillé F., Martel M.A., Dakin K.A., Hansen H.H., Kaindl A., Sifringer M., Fowler J., Stefovska V., et al. Synaptic NMDA receptor activity boosts intrinsic antioxidant defences. Nat. Neurosci. 2008, 11:476-487.
32. Peretti D., Bastide A., Radford H., Verity N., Molloy C., Martin M.G., Moreno J.A., Steinert J.R., Smith T., Dinsdale D., et al. RBM3 mediates structural plasticity and protective effects of cooling in neurodegeneration. Nature 2015, 518:236-239.
33. Planel E., Miyasaka T., Launey T., Chui D.H., Tanemura K., Sato S., Murayama O., Ishiquro K., Tatebayashi Y., Takashima A. Alterations in glucose metabolism induce hypothermia leading to tau hyperphosphorylation through differential inhibition of kinase and phosphatase activities: implications for Alzheimer's disease. J. Neurosci. 2004, 24:2401-2411.
34. Planel E., Richter K.E., Nolan C.E., Finley J.E., Liu L., Wen Y., Krishnamurthy P., Herman M., Wang L., Schachter J.B., et al. Anesthesia leads to tau hyperphosphorylation through inhibition of phosphatase activity by hypothermia. J. Neurosci. 2007, 27:3090-3097.
35. Planel E., Bretteville A., Liu L., Virag L., Du A.L., Yu W.H., Dickson D.W., Whittington R.A., Duff K.E. Acceleration and persistence of neurofibrillary pathology in a mouse model of tauopathy following anesthesia. FASEB J. 2009, 23:2595-2604.
36. Rzechorzek N.M., Connick P., Patani R., Selvaraj B.T., Chandran S. Hypothermic preconditioning of human cortical neurons requires proteostatic priming. EBioMedicine 2015, 2:528-535.
37. Saitoh M., Kunitomo J., Kimura E., Iwashita H., Uno Y., Onishi T., Uchiyama N., Kawamoto T., Tanaka T., Mol C.D., et al. 2-(3-[4-(Alkylsulfinyl)phenyl]-1-benzofuran-5-yl)-5-methyl-1,3,4-oxadiazole derivatives as novel inhibitors of glycogen synthase kinase-3β with good brain permeability. J. Med. Chem. 2009, 52:6270-6286.
38. Spillantini M.G., Goedert M. Tau pathology and neurodegeneration. Lancet Neurol. 2013, 12:609-622.
39. Sposito T., Preza E., Mahoney C.J., Seto-Salvia N., Ryan N.S., Morris H.R., Arber C., Devine M.J., Houlden H., Warner T.T., et al. Developmental regulation of tau splicing in stem cell derived neurons from frontotemporal dementia patients with 10 + 16 splice-site mutation in MAPT. Hum. Mol. Genet. 2015, 24:5260-5269.
40. Stieler J.T., Bullmann T., Kohl F., Toien O., Brückner M.K., Härtig W., Barnes B.M., Arendt T. The physiological link between metabolic rate depression and tau phosphorylation in mammalian hibernation. PLoS One 2011, 6:e14530.
41. Trojanowski J.Q., Lee V.M. Phosphorylation of paired helical filament tau in Alzheimer's disease: focusing on phosphatases. FASEB J. 1995, 9:1570-1576.
42. Walsh A.H., Cheng A., Honkanen R.E. Fostriecin, an antitumor antibiotic with inhibitory activity against serine/threonine protein phosphatases types 1 (PP1) and 2A (PP2A) is highly selective for PP2A. FEBS Lett. 1997, 416:230-234.
43. Yenari M.A., Han H.S. Neuroprotective mechanisms of hypothermia in brain ischaemia. Nat. Rev. Neurosci. 2012, 13:267-278.
44. Yu Y., Run X., Liang Z., Li Y., Liu F., Liu Y., Iqbl K., Grundke-Iqbal I., Gong C.X. Developmental regulation of tau phosphorylation, tau kinases, and tau phosphatases. J. Neurochem. 2009, 108:1480-1494.
45. Zell S.C., Kurtz K.J. Severe exposure hypothermia: a resuscitation protocol. Ann. Emerg. Med. 1985, 14:339-345.
46. Zhu X., Zelmer A., Kapfhammer J.P., Wellmann S. Cold-inducible RMB3 inhibits PERK phosphorylation through cooperation with NF90 to protect cells from endoplasmic reticulum stress. FASEB J. 2015, (Epub ahead of print).