The tyrosine phosphatase PTPN13/FAP-1 links calpain-2, TBI and tau tyrosine phosphorylation

Scientific Reports

Volumn 7, Issue 1, 2017, Pages

  Wang, Yubin ^a   Hall, Randy A ^b   Lee, Moses ^a   Kamgar Parsi, Andysheh ^a   Bi, Xiaoning ^a   Baudry, Michel ^a  

^a WESTERN UNIVERSITY OF HEALTH SCIENCES   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALPAIN; CAPN2 PROTEIN, MOUSE; NON RECEPTOR PROTEIN TYROSINE PHOSPHATASE 13; PTPN13 PROTEIN, MOUSE; TAU PROTEIN; TYROSINE;

ANIMAL; GENETICS; KNOCKOUT MOUSE; METABOLISM; MOUSE; PATHOLOGY; PHOSPHORYLATION; TRAUMATIC BRAIN INJURY;

ANIMALS; BRAIN INJURIES, TRAUMATIC; CALPAIN; MICE; MICE, KNOCKOUT; PHOSPHORYLATION; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 13; TAU PROTEINS; TYROSINE;

EID: 85029606355     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-017-12236-3     Document Type: Article

References (56)

1. Ballatore, C., Lee, V. M.-Y. &Trojanowski, J. Q. Tau-mediated neurodegeneration in Alzheimer's disease and related disorders. Nat Rev Neurosci 8, 663-672 (2007).
2. McKee, A. C. et al. Chronic traumatic encephalopathy in athletes: progressive tauopathy after repetitive head injury. J Neuropathol Exp Neurol 68, 709-735 (2009).
3. Johnson, V. E., Stewart, W. &Smith, D. H. Widespread tau and amyloid?beta pathology many years after a single traumatic brain injury in humans. Brain pathology 22, 142-149 (2012).
4. Hanger, D. P., Anderton, B. H. &Noble, W. Tau phosphorylation: the therapeutic challenge for neurodegenerative disease. Trends Mol Med 15, 112-119, https://doi.org/10.1016/j.molmed.2009.01.003 (2009).
5. Wang, J.-Z., Xia, Y.-Y., Grundke-Iqbal, I. &Iqbal, K. Abnormal hyperphosphorylation of tau: sites, regulation, and molecular mechanism of neurofibrillary degeneration. J Alzheimers Dis 33, S123-S139 (2013).
6. Lee, G. et al. Phosphorylation of tau by fyn: implications for Alzheimer's disease. J Neurosci 24, 2304-2312, https://doi.org/10.1523/ JNEUROSCI.4162-03.2004 (2004).
7. Derkinderen, P. et al. Tyrosine 394 is phosphorylated in Alzheimer's paired helical filament tau and in fetal tau with c-Abl as the candidate tyrosine kinase. J Neurosci 25, 6584-6593, https://doi.org/10.1523/JNEUROSCI.1487-05.2005 (2005).
8. Vega, I. E. et al. Increase in tau tyrosine phosphorylation correlates with the formation of tau aggregates. Brain Res Mol Brain Res 138, 135-144, https://doi.org/10.1016/j.molbrainres.2005.04.015 (2005).
9. Tremblay, M. A., Acker, C. M. &Davies, P. Tau phosphorylated at tyrosine 394 is found in Alzheimer's disease tangles and can be a product of the Abl-related kinase, Arg. J Alzheimers Dis 19, 721-733 (2010).
10. Saito, K., Elce, J. S., Hamos, J. E. &Nixon, R. A. Widespread activation of calcium-activated neutral proteinase (calpain) in the brain in Alzheimer disease: a potential molecular basis for neuronal degeneration. Proc Natl Acad Sci USA 90, 2628-2632 (1993).
11. Nixon, R. A. et al. Calcium-activated neutral proteinase (calpain) system in aging and Alzheimer's disease. Ann N Y Acad Sci 747, 77-91 (1994).
12. Grynspan, F., Griffin, W. R., Cataldo, A., Katayama, S. &Nixon, R. A. Active site-directed antibodies identify calpain II as an earlyappearing and pervasive component of neurofibrillary pathology in Alzheimer's disease. Brain Res 763, 145-158 (1997).
13. Lee, M.-s. et al. Neurotoxicity induces cleavage of p35 to p25 by calpain. Nature 405, 360-364 (2000).
14. Medeiros, R. et al. Calpain Inhibitor A-705253 Mitigates Alzheimer's Disease-Like Pathology and Cognitive Decline in Aged 3xTgAD Mice. Am J Pathol 181, 616-625 (2012).
15. Saito, T., Matsuba, Y., Yamazaki, N., Hashimoto, S. &Saido, T. C. Calpain activation in Alzheimer's model mice is an artifact of APP and presenilin overexpression. J Neurosci 36, 9933-9936 (2016).
16. Goñi-Oliver, P., Lucas, J. J., Avila, J. &Hernández, F. N-terminal Cleavage of GSK-3 by Calpain a new form of GSK-3 regulation. J Biol Chem 282, 22406-22413 (2007).
17. Jin, N. et al. Truncation and activation of GSK-3? by calpain I: a molecular mechanism links to tau hyperphosphorylation in Alzheimer's disease. Sci Rep 5, 8187 (2015).
18. Jin, N. et al. Truncation and Activation of Dual Specificity Tyrosine Phosphorylation-regulated Kinase 1A by Calpain Ia Molecular mechanism Linked to Tau Pathology in Alzheimer Disease. J Biol Chem 290, 15219-15237 (2015).
19. Watkins, G. R. et al. Monoubiquitination promotes calpain cleavage of the protein phosphatase 2A (PP2A) regulatory subunit ?4, altering PP2A stability and microtubule-associated protein phosphorylation. J Biol Chem 287, 24207-24215 (2012).
20. Nemetz, P. N. et al. Traumatic brain injury and time to onset of Alzheimer's disease: a population-based study. Am J Epidemiol 149, 32-40 (1999).
21. Lye, T. C. &Shores, E. A. Traumatic brain injury as a risk factor for Alzheimer's disease: a review. Neuropsychol Rev 10, 115-129 (2000).
22. Gavett, B. E., Stern, R. A. &McKee, A. C. Chronic traumatic encephalopathy: a potential late effect of sport-related concussive and subconcussive head trauma. Clin Sports Med 30, 179-188 (2011).
23. Baudry, M. &Bi, X. Calpain-1 and Calpain-2: The Yin and Yang of Synaptic Plasticity and Neurodegeneration. Trends Neurosci, doi:https://doi.org/10.1016/j.tins.2016.01.007 (2016).
24. Wang, Y. et al. A molecular brake controls the magnitude of long-term potentiation. Nat Commun 5, 3051, https://doi.org/10.1038/ ncomms4051 (2014).
25. Liu, Y. et al. A calpain-2 selective inhibitor enhances learning &memory by prolonging ERK activation. Neuropharmacology 105, 471-477, https://doi.org/10.1016/j.neuropharm.2016.02.022 (2016).
26. Wang, Y., Briz, V., Chishti, A., Bi, X. &Baudry, M. Distinct roles for mu-calpain and m-calpain in synaptic NMDAR-mediated neuroprotection and extrasynaptic NMDAR-mediated neurodegeneration. J Neurosci 33, 18880-18892, https://doi.org/10.1523/ JNEUROSCI.3293-13.2013 (2013).
27. Wang, Y. et al. Defects in the CAPN1 Gene Result in Alterations in Cerebellar Development and Cerebellar Ataxia in Mice and Humans. Cell Rep 16, 79-91, https://doi.org/10.1016/j.celrep.2016.05.044 (2016).
28. Wang, Y. et al. Calpain-1 and calpain-2 play opposite roles in retinal ganglion cell degeneration induced by retinal ischemia/ reperfusion injury. Neurobiol Dis 93, 121-128, https://doi.org/10.1016/j.nbd.2016.05.007 (2016).
29. Seinfeld, J., Baudry, N., Xu, X., Bi, X. &Baudry, M. Differential tivation of Calpain-1 and Calpain-2 following Kainate-Induced Seizure Activity in Rats and MiceAc. eNeuro 3, doi:https://doi.org/10.1523/ENEURO.0088-15.2016 (2016).
30. Kim, E. &Sheng, M. PDZ domain proteins of synapses. Nature Rev Neurosci 5, 771-781 (2004).
31. Sato, T., Irie, S., Kitada, S. &Reed, J. C. FAP-1: a protein tyrosine phosphatase that associates with Fas. Science 268, 411-415 (1995).
32. Freiss, G. &Chalbos, D. PTPN13/PTPL1: an important regulator of tumor aggressiveness. Anticancer Agents Med Chem 11, 78-88 (2011).
33. Fam, S. R. et al. P2Y1 receptor signaling is controlled by interaction with the PDZ scaffold NHERF-2. Proc Natl Acad Sci USA 102, 8042-8047 (2005).
34. He, J. et al. Proteomic analysis of ?1-adrenergic receptor interactions with PDZ scaffold proteins. J Biol Chem 281, 2820-2827 (2006).
35. Seubert, P., Baudry, M., Dudek, S. &Lynch, G. Calmodulin stimulates the degradation of brain spectrin by calpain. Synapse 1, 20-24 (1987).
36. Hantschel, O. &Superti-Furga, G. Regulation of the c-Abl and Bcr-Abl tyrosine kinases. Nat Rev Mol Cell Biol 5, 33-44 (2004).
37. Wang, Y. et al. Protection against TBI-induced neuronal death with post-treatment with a selective calpain-2 inhibitor in mice. J Neurotrauma (2017).
38. Hawkins, B. E. et al. Rapid accumulation of endogenous tau oligomers in a rat model of traumatic brain injury possible link between traumatic brain injury and sporadic tauopathies. J Biol Chem 288, 17042-17050 (2013).
39. Berger, Z. et al. Accumulation of pathological tau species and memory loss in a conditional model of tauopathy. J of Neurosci 27, 3650-3662 (2007).
40. A. Lasagna-Reeves, C., L. Castillo-Carranza, D., R. Jackson, G. &Kayed, R. Tau oligomers as potential targets for immunotherapy for Alzheimer's disease and tauopathies. Curr Alzheimer Res 8, 659-665 (2011).
41. Lasagna-Reeves, C. A. et al. Alzheimer brain-derived tau oligomers propagate pathology from endogenous tau. Sci rep 2, 700 (2012).
42. Jucker, M. &Walker, L. C. Self-propagation of pathogenic protein aggregates in neurodegenerative diseases. Nature 501, 45-51 (2013).
43. Saras, J. et al. A novel GTPase-activating protein for Rho interacts with a PDZ domain of the protein-tyrosine phosphatase PTPL1. J Biol Chem 272, 24333-24338 (1997).
44. Imam, S. Z. et al. Novel regulation of parkin function through c-Abl-mediated tyrosine phosphorylation: implications for Parkinson's disease. J of Neurosci 31, 157-163 (2011).
45. Jin, N. et al. Truncation and activation of GSK-3? by calpain I: a molecular mechanism links to tau hyperphosphorylation in Alzheimer's disease. Sci rep 5 (2015).
46. Krapivinsky, G. et al. The NMDA receptor is coupled to the ERK pathway by a direct interaction between NR2B and RasGRF1. Neuron 40, 775-784 (2003).
47. Zadran, S. et al. Brain-derived neurotrophic factor and epidermal growth factor activate neuronal m-calpain via mitogen-activated protein kinase-dependent phosphorylation. J Neurosci 30, 1086-1095 (2010).
48. Papouin, T. &Oliet, S. H. Organization, control and function of extrasynaptic NMDA receptors. Phil. Trans. R. Soc. B 369, 20130601 (2014).
49. Chazot, P. L. The NMDA receptor NR2B subunit: a valid therapeutic target for multiple CNS pathologies. Curr med chem 11, 389-396 (2004).
50. McKee, A. C. et al. The spectrum of disease in chronic traumatic encephalopathy. Brain 136, 43-64 (2013).
51. Siman, R. et al. Evidence That the Blood Biomarker SNTF Predicts Brain Imaging Changes and Persistent Cognitive Dysfunction in Mild TBI Patients. Front Neurol 4, 190, https://doi.org/10.3389/fneur.2013.00190 (2013).
52. Yamada, K. H. et al. Targeted gene inactivation of calpain-1 suppresses cortical degeneration due to traumatic brain injury and neuronal apoptosis induced by oxidative stress. J Biol Chem 287, 13182-13193, https://doi.org/10.1074/jbc.M111.302612 (2012).
53. Smith, D. H. et al. A model of parasagittal controlled cortical impact in the mouse: cognitive and histopathologic effects. J Neurotrauma 12, 169-178 (1995).
54. Hall, E. D. et al. Spatial and temporal characteristics of neurodegeneration after controlled cortical impact in mice: more than a focal brain injury. J Neurotrauma 22, 252-265, https://doi.org/10.1089/neu.2005.22.252 (2005).
55. Romine, J., Gao, X. &Chen, J. Controlled cortical impact model for traumatic brain injury. J Vis Exp e51781-e51781 (2014).
56. Bolte, S. &Cordelieres, F. A guided tour into subcellular colocalization analysis in light microscopy. J microsc 224, 213-232 (2006).