Ubiquitin C-terminal hydrolase-L1 (UCH-L1) as a therapeutic and diagnostic target in neurodegeneration, neurotrauma and neuro-injuries

References

• Jackson P, Thompson RJ. The demonstration of new human brain-specific proteins by high-resolution two-dimensional polyacrylamide gel electrophoresis. J Neurol Sci. 1981 Mar;49:429–438.
   PubMed Web of Science ®Google Scholar
• Doran JF, Jackson P, Kynoch PA, et al. Isolation of PGP 9.5, a new human neurone-specific protein detected by high-resolution two-dimensional electrophoresis. J Neurochem. 1983 Jun;40:1542–1547.
   PubMed Web of Science ®Google Scholar
• Bradbury JM, Thompson RJ. Immunoassay of the neuronal and neuroendocrine marker PGP 9.5 in human tissues. J Neurochem. 1985 Feb;44:651–653.
   PubMed Web of Science ®Google Scholar
• Day IN, Thompson RJ. Molecular cloning of cDNA coding for human PGP 9.5 protein. A novel cytoplasmic marker for neurones and neuroendocrine cells. FEBS Lett. 1987 Jan;210:157–160.
   PubMed Web of Science ®Google Scholar
• Wilkinson KD, Lee KM, Deshpande S, et al. The neuron-specific protein PGP 9.5 is a ubiquitin carboxyl-terminal hydrolase. Science. 1989 Nov;246:670–673.
   PubMed Web of Science ®Google Scholar
• Guingab-Cagmat J, Newsom K, Vakulenko A, et al. others. In vitro MS-based proteomic analysis and absolute quantification of neuronal-glial injury biomarkers in cell culture system. Electrophoresis. Wiley Online Lib. 2012;33:3786–3797.
   PubMed Web of Science ®Google Scholar
• Wilkinson KD, Deshpande S, Larsen CN. Comparisons of neuronal (PGP 9.5) and non-neuronal ubiquitin C-terminal hydrolases. Biochem Soc Trans. Aug 1992;20:631–637. 1992nd ed.
   PubMed Web of Science ®Google Scholar
• Johnston SC, Larsen CN, Cook WJ, et al. Crystal structure of a deubiquitinating enzyme (human UCH-L3) at 1.8 A resolution. EMBO J EMBO Press. 1997 Jul;16:3787–3796.
   PubMed Web of Science ®Google Scholar
• Jensen DE, Proctor M, Marquis ST, et al. BAP1: a novel ubiquitin hydrolase which binds to the BRCA1 RING finger and enhances BRCA1-mediated cell growth suppression. Oncogene. 1998 Mar;16:1097–1112.
   PubMed Web of Science ®Google Scholar
• Maiti TK, Permaul M, Boudreaux DA, et al. Crystal structure of the catalytic domain of UCHL5, a proteasome‐associated human deubiquitinating enzyme, reveals an unproductive form of the enzyme. FEBS J. 2011 Dec;278(24):4917–4926.
   PubMed Web of Science ®Google Scholar
• Das C, Hoang QQ, Kreinbring CA, et al. Structural basis for conformational plasticity of the Parkinson’s disease-associated ubiquitin hydrolase UCH-L1. Proceedings of the National Academy of Sciences. 2006 Mar;103:4675–4680.
   Google Scholar
• Boudreaux DA, Maiti TK, Davies CW, et al. Ubiquitin vinyl methyl ester binding orients the misaligned active site of the ubiquitin hydrolase UCHL1 into productive conformation. Proc Natl Acad Sci USA National Acad Sciences. 2010 May;107:9117–9122.
   PubMed Web of Science ®Google Scholar
• Davies CW, Chaney J, Korbel G, et al. The co-crystal structure of ubiquitin carboxy-terminal hydrolase L1 (UCHL1) with a tripeptide fluoromethyl ketone (Z-VAE(OMe)-FMK). Bioorg Med Chem Lett. 2012 Jun;22:3900–3904.
   PubMed Web of Science ®Google Scholar
• Betarbet R, Sherer TB, Greenamyre JT. Ubiquitin-proteasome system and Parkinson’s diseases. Exp Neurol. 2005 Feb;191(Suppl 1):S17–S27.
   PubMed Web of Science ®Google Scholar
• Tongaonkar P, Chen L, Lambertson D, et al. Evidence for an interaction between ubiquitin-conjugating enzymes and the 26S proteasome. Mol Cell Biol. 2000 Jul;20:4691–4698.
   PubMed Web of Science ®Google Scholar
• Liu Y, Fallon L, Lashuel HA, et al. The UCH-L1 gene encodes two opposing enzymatic activities that affect. Cell. 2002 Oct;111:209–218.
   PubMed Web of Science ®Google Scholar
• Ardley HC, Scott GB, Rose SA, et al. UCH-L1 aggresome formation in response to proteasome impairment indicates a role in inclusion formation in Parkinson’s disease. J Neurochem Blackwell Science Ltd. 2004 Jul;90:379–391.
   PubMed Web of Science ®Google Scholar
• Kabuta T, Setsuie R, Mitsui T, et al. Aberrant molecular properties shared by familial Parkinson’s disease-associated mutant UCH-L1 and carbonyl-modified UCH-L1. Hum Mol Genetics. Oxford Univ. 2008 May;17:1482–1496.
   PubMed Web of Science ®Google Scholar
• Misaghi S, Galardy PJ, Meester WJN, et al. Structure of the ubiquitin hydrolase UCH-L3 complexed with a suicide substrate. J Chem. Am Soc Biochemistry Mol Biol. 2005 Jan;280:1512–1520.
   Google Scholar
• Hansen JE, Lund O, Engelbrecht J, et al. Prediction of O-glycosylation of mammalian proteins: specificity patterns of UDP-GalNAc: polypeptideN-acetylgalactosaminyltransferase. Biochem Journal Portland Limited. 1995 Jun;308:801–813.
   PubMedGoogle Scholar
• Cole RN, Hart GW. Cytosolic O-glycosylation is abundant in nerve terminals. J Neurochem. 2001 Dec;79:1080–1089.
   PubMed Web of Science ®Google Scholar
• Clarke S, Tamanoi F. Fighting cancer by disrupting C-terminal methylation of signaling proteins. J Clin Invest Am Soc Clin Investig. 2004 Feb;113:513–515.
   PubMed Web of Science ®Google Scholar
• Liu Z, Meray RK, Grammatopoulos TN, et al. Membrane-associated farnesylated UCH-L1 promotes -synuclein neurotoxicity and is a therapeutic target for Parkinson’s disease. Proceedings of the National Academy of Sciences. 2009 Mar;106:4635–4640.
   Google Scholar
• Toyama T, Abiko Y, Katayama Y, et al. S-Mercuration of ubiquitin carboxyl-terminal hydrolase L1 through Cys152 by methylmercury causes inhibition of its catalytic activity and reduction of monoubiquitin levels in SH-SY5Y cells. J Toxicol Sci. 2015;40:887–893.
   PubMed Web of Science ®Google Scholar
• Contu VR, Kotake Y, Toyama T, et al. Endogenous neurotoxic dopamine derivative covalently binds to Parkinson’s disease-associated ubiquitin C-terminal hydrolase L1 and alters its structure and function. J Neurochem. 2014 Sep;130:826–838.
   PubMed Web of Science ®Google Scholar
• Guingab-Cagmat JD, Stevens SM, Ratliff MV, et al. Identification of tyrosine nitration in UCH-L1 and GAPDH. Electrophoresis. 2011 Jun;32:1692–1705.
   PubMed Web of Science ®Google Scholar
• Choi J, Levey AI, Weintraub ST, et al. and Down-regulation of Ubiquitin Carboxyl-terminal Hydrolase L1 Associated with Idiopathic Parkinson“s and Alzheimer”s Diseases. J Biol Chem. 2004 Mar;279:13256–13264.
   PubMed Web of Science ®Google Scholar
• Boutaud O, Andreasson KI, Zagol-Ikapitte I, et al. Cyclooxygenase-dependent lipid-modification of brain proteins. Brain Pathol. 2005 Apr;15:139–142.
   PubMed Web of Science ®Google Scholar
• Koharudin LMI, Liu H, Di Maio R, et al. Cyclopentenone prostaglandin-induced unfolding and aggregation of the Parkinson disease-associated UCH-L1. Proc Natl Acad Sci U S A. 2010 Apr;107:6835–6840.
   PubMed Web of Science ®Google Scholar
• Liu Y, Lashuel HA, Choi S, et al. Discovery of inhibitors that elucidate the role of UCH-L1 activity in the H1299 lung cancer cell line. Chem Biol. 2003 Sep;10:837–846.
   PubMed Web of Science ®Google Scholar
• Love KR, Catic A, Schlieker C, et al. Mechanisms, biology and inhibitors of deubiquitinating enzymes. Nat Chem Biol. 2007 Nov;3:697–705.
   PubMed Web of Science ®Google Scholar
• Pham LV, Tamayo AT, Li C, et al. Degrasyn potentiates the antitumor effects of bortezomib in mantle cell lymphoma cells in vitro and in vivo: therapeutic implications. Mol Cancer Therapeutics. Am Assoc Cancer Res. 2010 Jul;9:2026–2036.
   PubMed Web of Science ®Google Scholar
• Liu H, Chen W, Liang C, et al. WP1130 increases doxorubicin sensitivity in hepatocellular carcinoma cells through usp9x-dependent p53 degradation. Cancer Lett Elsevier. 2015 Jun;361:218–225.
   PubMed Web of Science ®Google Scholar
• Xie M, Han Y, Yu Q, et al. UCH-L1 inhibition decreases the microtubule-binding function of tau protein. Zhu L-Q, Editor J Alzheimers Dis IOS Press. 2015;49:353–363.
   Google Scholar
• Setsuie R, Wada K. The functions of UCH-L1 and its relation to neurodegenerative diseases. Neurochem Int. 2007 Jul;51:105–111.
   PubMed Web of Science ®Google Scholar
• Gong B, Leznik E. The role of ubiquitin C-terminal hydrolase L1 in neurodegenerative disorders. Drug News Perspect. Jul-Aug 2007;20:365–370. 2007 ed.
   PubMed Web of Science ®Google Scholar
• De Pril R, Fischer DF, Maat-Schieman MLC, et al. Accumulation of aberrant ubiquitin induces aggregate formation and cell death in polyglutamine diseases. Hum Mol Genetics. Oxford Univ. 2004 Aug;13:1803–1813.
   PubMed Web of Science ®Google Scholar
• Braak H, Del Tredici K. Alzheimer’s pathogenesis: is there neuron-to-neuron propagation? Acta Neuropathol. 2011;121:589–595.
   PubMed Web of Science ®Google Scholar
• Serrano-Pozo A, Frosch MP, Masliah E, et al. Neuropathological alterations in Alzheimer disease. Cold Spring Harb Perspect Med Cold Spring Harbor Laboratory Press. 2011 Sep;1:a006189–a006189.
   PubMed Web of Science ®Google Scholar
• Gentier RJ, Van Leeuwen FW. Misframed ubiquitin and impaired protein quality control: an early event in Alzheimer’s disease. Front Mol Neurosci Frontiers. 2015 Sep;8:4277.
   Web of Science ®Google Scholar
• Van Leeuwen FW, De Kleijn DP, Van Den Hurk HH, et al. Frameshift mutants of beta amyloid precursor protein and ubiquitin-B in Alzheimer’s and Down patients. Science. 1998 Jan;279:242–247.
   PubMed Web of Science ®Google Scholar
• Finley D, Chen X, Walters KJ. Gates, channels, and switches: elements of the proteasome machine. Trends Biochem Sciences. Elsevier. 2016 Jan;41:77–93.
   PubMed Web of Science ®Google Scholar
• Bishop P, Rubin P, Thomson AR, et al. The Ubiquitin C-Terminal Hydrolase L1 (UCH-L1) C terminus plays a key role in protein stability, but its farnesylation is not required for membrane association in primary neurons. J Biol Chem. 2014 Dec;289:36140–36149.
   PubMed Web of Science ®Google Scholar
• Kobeissy FH, Ottens AK, Zhang Z, et al. Novel differential neuroproteomics analysis of traumatic brain injury in rats. Molecular \& Cellular Proteomics [Internet]. 2006 ed. ASBMB; 2006 Jun;5:1887–1898. Available from: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=16801361.
   Google Scholar
• Zhang Z, Mondello S, Kobeissy F, et al. Protein biomarkers for traumatic and ischemic brain injury: from bench to bedside. Translational Stroke Research [Internet]. Springer; 2011 Jun;3:1–32. Available from: http://www.frontiersin.org/Neurotrauma/10.3389/fneur.2012.00147/abstract.
   Google Scholar
• Liu MC, Akinyi L, Scharf D, et al. Ubiquitin C-terminal hydrolase-L1 as a biomarker for ischemic and traumatic brain injury in rats. Eur J Neurosci. 2010 Feb;31:722–732.
   PubMed Web of Science ®Google Scholar
• Zoltewicz JS, Mondello S, Yang B, et al. Biomarkers track damage after graded injury severity in a rat model of penetrating brain injury. J Neurotrauma. 2013 Jul;30:1161–1169.
   PubMed Web of Science ®Google Scholar
• Svetlov SI, Prima V, Kirk DR, et al. Morphologic and biochemical characterization of brain injury in a model of controlled blast overpressure exposure. J Trauma 2010 Ed. 2010 Oct;69:795–804.
   Google Scholar
• Mondello S, Shear DA, Bramlett HM, et al. Insight into pre-clinical models of traumatic brain injury using circulating brain damage biomarkers: operation brain trauma therapy. J Neurotrauma. 2016 Mar;33:595–605.
   PubMed Web of Science ®Google Scholar
• Papa L, Oli MW, Akinyi L, et al. UCH-L1 is a novel biomarker for severe traumatic brain injury in human. Crit Care. 2010;38:138–144.
   Web of Science ®Google Scholar
• Papa L, Robertson CS, Wang KKW, et al. Biomarkers improve clinical outcome predictors of mortality following non-penetrating severe traumatic brain injury. Neurocrit Care. 2014 Jul;22:52–64.
   Web of Science ®Google Scholar
• Berger RP, Hayes RL, Richichi R, et al. Serum concentrations of ubiquitin C-terminal hydrolase-L1 and αII-spectrin breakdown product 145 kDa correlate with outcome after pediatric TBI. J Neurotrauma. 2012 Jan;29:162–167.
   PubMed Web of Science ®Google Scholar
• Welch RD, Ayaz SI, Lewis LM, et al. Ability of serum glial fibrillary acidic protein, ubiquitin c-terminal hydrolase-L1, and s100b to differentiate normal and abnormal head computed tomography findings in patients with suspected mild or moderate traumatic brain injury. J Neurotrauma. 2016 Jan;33:203–214.
   PubMed Web of Science ®Google Scholar
• Posti JP, Takala RSK, Runtti H, et al. The levels of glial fibrillary acidic protein and ubiquitin c-terminal hydrolase-L1 during the first week after a traumatic brain injury. Neurosurgery. 2016 Sep;79(3):456–464.
   PubMed Web of Science ®Google Scholar
• Diaz-Arrastia R, Wang KKW, Papa L, et al. Acute biomarkers of traumatic brain injury: relationship between plasma levels of ubiquitin c-terminal hydrolase-L1 and glial fibrillary acidic protein |abstract. J Neurotrauma. 2014 Jan;31:19–25.
   PubMed Web of Science ®Google Scholar
• Papa L, Silvestri S, Brophy GM, et al. GFAP out-performs S100β in detecting traumatic intracranial lesions on computed tomography in trauma patients with mild traumatic brain injury and those with extracranial lesions. J Neurotrauma. 2014 Nov;31:1815–1822.
   PubMed Web of Science ®Google Scholar
• Papa L, Brophy GM, Welch RD, et al. Time course and diagnostic accuracy of glial and neuronal blood biomarkers GFAP and UCH-L1 in a large cohort of trauma patients with and without mild traumatic brain injury. JAMA Neurol. 2016 May 1;73(5):551–560.
   PubMed Web of Science ®Google Scholar
• Yokobori S, Zhang Z, Moghieb A, et al. Acute diagnostic biomarkers for spinal cord injury: review of the literature and preliminary research report. World Neurosurgery Elsevier Inc. 2015 May;83:867–878.
   PubMed Web of Science ®Google Scholar
• Yokobori S, Hosein K, Wang MY, et al. Biomarkers in spinal cord injury. In: Wang K, Zhang Z, Kobeissy FH, editors. Biomarkers of brain injury & neurological disorders. 1st ed. New York: CRC Press: New York; 2014. p. 340–354.
   Google Scholar
• Foerch C, Curdt I, Yan B, et al. Serum glial fibrillary acidic protein as a biomarker for intracerebral haemorrhage in patients with acute stroke. J Neurol Neurosurg Psychiatry [Internet]. 2006 Feb;77:181–184. Available from. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=16174653
   PubMed Web of Science ®Google Scholar
• Ren C, Kobeissy F, Alawieh A, et al. Assessment of Serum UCH-L1 and GFAP in acute stroke patients. Sci Rep. 2016 Apr 14;6:24588.
   Web of Science ®Google Scholar
• Ehrenreich H, Kästner A, Weissenborn K, et al. Circulating damage marker profiles support a neuroprotective effect of erythropoietin in ischemic stroke patients. Mol Med. 2011;17:1306–1310.
   PubMed Web of Science ®Google Scholar
• Douglas-Escobar M, Yang C, Bennett J, et al. A pilot study of novel biomarkers in neonates with hypoxic-ischemic encephalopathy. Pediatr Res. 2010 Dec;68:531–536.
   PubMed Web of Science ®Google Scholar
• Douglas-Escobar MV, Heaton SC, Bennett J, et al. Weiss MD. UCH-L1 and GFAP serum levels in neonates with hypoxic-ischemic encephalopathy: a single center pilot study. Front Neurol 6 Ed Frontiers. 2014;5:273.
   PubMed Web of Science ®Google Scholar
• Jiang S-H, Wang J-X, Zhang Y-M, et al. [Effect of hypothermia therapy on serum GFAP and UCH-L1 levels in neonates with hypoxic-ischemic encephalopathy]. Zhongguo Dang Dai Er Ke Za Zhi. 2014 Dec;16:1193–1196.
   PubMedGoogle Scholar
• Lv H, Wang Q, Wu S, et al. Clinica Chimica Acta. 2015 Oct;450:282–297. Elsevier B.V.
   PubMed Web of Science ®Google Scholar
• Mondello S, Palmio J, Streeter J, et al. Ubiquitin carboxy-terminal hydrolase L1 (UCH-L1) is increased in cerebrospinal fluid and plasma of patients after epileptic seizure. BMC Neurol Biomed Central. 2012;12:85.
   PubMed Web of Science ®Google Scholar
• Li Y, Wang Z, Zhang B, et al. Cerebrospinal fluid ubiquitin C-terminal hydrolase as a novel marker of neuronal damage after epileptic seizure. Epilepsy Res. 2013 Feb;103:205–210.
   PubMed Web of Science ®Google Scholar
• Arnaoutakis GJ, George TJ, Wang KK, et al. Serum levels of neuron-specific ubiquitin carboxyl-terminal esterase-L1 predict brain injury in a canine model of hypothermic circulatory arrest. J Thorac Cardiovasc Surg. 2011 Oct;142:902–910.e1.
   PubMed Web of Science ®Google Scholar
• Zhang Y-P, Zhu Y-B, Duan DD, et al. Serum UCH-L1 as a novel biomarker to predict neuronal apoptosis following deep hypothermic circulatory arrest. Int J Med Sci. 2015 Jan;12:576–582.
   PubMed Web of Science ®Google Scholar
• Fink EL, Berger RP, Clark RSB, et al. Exploratory study of serum ubiquitin carboxyl-terminal esterase L1 and glial fibrillary acidic protein for outcome prognostication after pediatric cardiac arrest. Resuscitation. 2016 Apr;101:65–70.
   PubMed Web of Science ®Google Scholar
• Suong DNA, Thao DTP, Masamitsu Y, et al. Ubiquitin carboxyl hydrolase L1 significance for human diseases. Protein Pept Lett. 2014 Jul;21:624–630.
   PubMed Web of Science ®Google Scholar
• Caldeira MV, Salazar IL, Curcio M, et al. Role of the ubiquitin-proteasome system in brain ischemia: friend or foe? Prog Neurobiol. 2014 Jan;112:50–69.
   PubMed Web of Science ®Google Scholar
• Hu BR, Martone ME, Jones YZ, et al. Protein aggregation after transient cerebral ischemia. J Neurosci. 2000 May;20:3191–3199.
   PubMed Web of Science ®Google Scholar
• Hu BR, Janelidze S, Ginsberg MD, et al. Protein aggregation after focal brain ischemia and reperfusion. J Cereb Blood Flow Metab SAGE Publicationssage UK: London, England. 2001 Jul;21:865–875.
   PubMed Web of Science ®Google Scholar
• Beręsewicz M, Zabłocka B, Domanska-Janik K. Protein aggregation in postsynaptic density after transient brain ischemia. J Neurochem Blackwell Publishing Ltd. 2003 May;85:19–19.
   Web of Science ®Google Scholar
• Liu CL, Martone ME, Hu BR. Protein ubiquitination in postsynaptic densities after transient cerebral ischemia. J Cereb Blood Flow Metab SAGE Publicationssage UK: London, England. 2004 Nov;22:1219–1225.
   Web of Science ®Google Scholar
• Liu C, Chen S, Kamme F, et al. Ischemic preconditioning prevents protein aggregation after transient cerebral ischemia. Nsc. 2005;134:69–80.
   Google Scholar
• Hochrainer K, Jackman K, Anrather J, et al. Reperfusion rather than ischemia drives the formation of ubiquitin aggregates after middle cerebral artery occlusion. Stroke American Heart Association, Inc. 2012 Aug;43:2229–2235.
   Google Scholar
• Ge P, Luo Y, Wang H, et al. Anti-protein aggregation is a potential target for preventing delayed neuronal death after transient ischemia. Medical Hypotheses. Elsevier. 2009 Dec;73:994–995.
   PubMed Web of Science ®Google Scholar
• Liu MC, Akle V, Zheng W, et al. Comparing calpain- and caspase-3-mediated degradation patterns in traumatic brain injury by differential proteome analysis. Biochem J. 2015;394:715–725.
   Web of Science ®Google Scholar
• Bramlett HM, Dietrich WD. Synuclein aggregation: possible role in traumatic brain injury. Exp Neurol. 2003 Nov;184:27–30.
   PubMed Web of Science ®Google Scholar
• Hawkins BE, Krishnamurthy S, Castillo-Carranza DL, 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. Jun 2013;288:17042–17050. 2013 ed.
   PubMed Web of Science ®Google Scholar
• Washington PM, Morffy N, Parsadanian M, et al. Experimental traumatic brain injury induces rapid aggregation and oligomerization of amyloid-beta in an Alzheimer’s disease mouse model. J. Neurotrauma. 2014 Jan;31:125–134. Mary Ann Liebert. Inc. 140 Huguenot Street, 3rd Floor New Rochelle, NY 10801 USA
   PubMed Web of Science ®Google Scholar
• Tajiri N, Kellogg SL, Shimizu T, et al. Traumatic brain injury precipitates cognitive impairment and extracellular Aβ aggregation in Alzheimer’s disease transgenic mice. Plos ONE. Public Library of Science. 2013;8:e78851.
   PubMed Web of Science ®Google Scholar