A novel method for the rapid detection of post-translationally modified visinin-like protein 1 in rat models of brain injury

References

• Prevention, C.f.D.C.a. Report to congress on traumatic brain injury in the United States: epidemiology and rebailitation. In: N.C.f.I.P.a.C.D.o.U.I. Prevention, editor. Atlanta, GA: Center for Disease Control and Prevention; 2015.
   Google Scholar
• Taylor BC, Hagel EM, Carlson KF, Cifu DX, Cutting A, Bidelspach DE, Sayer NA. Prevalence and costs of co-occurring traumatic brain injury with and without psychiatric disturbance and pain among afghanistan and Iraq war veteran v.A. users. Med Care. 2012;50(4):342–46. doi:10.1097/MLR.0b013e318245a558.
   PubMed Web of Science ®Google Scholar
• Brasure M, Lamberty GJ, Sayer NA, Nelson NW, MacDonald R, Ouellette J, Tacklind J, Grove M, Rutks IR, Bulter ME, et al. Multidisciplinary postacute rehabilitation for moderate to severe traumatic brain injury in adults. In: A.f.H.R.a. Quality, editor. Rockville, MD: Agency for Healthcare Research and Quality; 2012.
   Google Scholar
• Jagoda AS, Bazarian JJ, Bruns JJ Jr., Cantrill SV, Gean AD, Howard PK, Ghajar J, Riggio S, Wright DW, Wears RL, et al. Clinical policy: neuroimaging and decisionmaking in adult mild traumatic brain injury in the acute setting. J Emerg Nurs. 2009;35(2):e5–40. doi:10.1016/j.jen.2008.12.010.
   PubMed Web of Science ®Google Scholar
• Welch RD, Ayaz SI, Lewis LM, Unden J, Chen JY, Mika VH, Saville B, Tyndall JA, Nash M, Buki A, 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;33(2):203–14. doi:10.1089/neu.2015.4149.
   PubMed Web of Science ®Google Scholar
• Papa L, Lewis LM, Silvestri S, Falk JL, Giordano P, Brophy GM, Demery JA, Liu MC, Mo J, Akinyi L, et al. Serum levels of ubiquitin c-terminal hydrolase distinguish mild traumatic brain injury from trauma controls and are elevated in mild and moderate traumatic brain injury patients with intracranial lesions and neurosurgical intervention. J Trauma Acute Care Surg. 2012;72(5):1335–44. doi:10.1097/TA.0b013e3182491e3d.
   PubMed Web of Science ®Google Scholar
• Wolf H, Frantal S, Pajenda G, Leitgeb J, Sarahrudi K, Hajdu S. Analysis of s100 calcium binding protein b serum levels in different types of traumatic intracranial lesions. J Neurotrauma. 2015;32(1):23–27. doi:10.1089/neu.2013.3202.
   PubMed Web of Science ®Google Scholar
• Papa L, Silvestri S, Brophy GM, Giordano P, Falk JL, Braga CF, Tan CN, Ameli NJ, Demery JA, Dixit NK, et al. Gfap out-performs s100beta in detecting traumatic intracranial lesions on computed tomography in trauma patients with mild traumatic brain injury and those with extracranial lesions. J Neurotrauma. 2014;31(22):1815–22. doi:10.1089/neu.2013.3245.
   PubMed Web of Science ®Google Scholar
• Papa L, Lewis LM, Falk JL, Zhang Z, Silvestri S, Giordano P, Brophy GM, Demery JA, Dixit NK, Ferguson I, et al. Elevated levels of serum glial fibrillary acidic protein breakdown products in mild and moderate traumatic brain injury are associated with intracranial lesions and neurosurgical intervention. Ann Emerg Med. 2012;59(6):471–83. doi:10.1016/j.annemergmed.2011.08.021.
   PubMed Web of Science ®Google Scholar
• Okonkwo DO, Yue JK, Puccio AM, Panczykowski DM, Inoue T, McMahon PJ, Sorani MD, Yuh EL, Lingsma HF, Maas AI, et al. R. Transforming, and I. Clinical knowledge in traumatic brain injury: gfap-bdp as an acute diagnostic marker in traumatic brain injury: results from the prospective transforming research and clinical knowledge in traumatic brain injury study. J Neurotrauma. 2013;30(17):1490–97. doi:10.1089/neu.2013.2883.
   PubMed Web of Science ®Google Scholar
• Yealy DM, Hogan DE. Imaging after head trauma. Who needs what? Emerg Med Cli North Am. 1991;9(4):707–17.
   PubMedGoogle Scholar
• Vollmer DG, Dacey RG Jr. The management of mild and moderate head injuries. Neurosurg Clin N Am. 1991;2(2):437–55.
   PubMedGoogle Scholar
• Herrmann M, Jost S, Kutz S, Ebert AD, Kratz T, Wunderlich MT, Synowitz H. Temporal profile of release of neurobiochemical markers of brain damage after traumatic brain injury is associated with intracranial pathology as demonstrated in cranial computerized tomography. J Neurotrauma. 2000;17(2):113–22. doi:10.1089/neu.2000.17.113.
   PubMed Web of Science ®Google Scholar
• Marangos PJ, Schmechel DE. Neuron specific enolase, a clinically useful marker for neurons and neuroendocrine cells. Annu Rev Neurosci. 1987;10:269–95. doi:10.1146/annurev.ne.10.030187.001413.
   PubMed Web of Science ®Google Scholar
• McMahon PJ, Panczykowski DM, Yue JK, Puccio AM, Inoue T, Sorani MD, Lingsma HF, Maas AI, Valadka AB, Yuh EL, et al.; T.-T. Investigators. Measurement of the glial fibrillary acidic protein and its breakdown products gfap-bdp biomarker for the detection of traumatic brain injury compared to computed tomography and magnetic resonance imaging. J Neurotrauma. 2015;32(8):527–33. doi:10.1089/neu.2014.3635.
   PubMed Web of Science ®Google Scholar
• Unden J, Christensson B, Bellner J, Alling C, Romner B. Serum s100b levels in patients with cerebral and extracerebral infectious disease. Scand J Infect Dis. 2004;36(1):10–13. doi:10.1080/00365540310017294.
   PubMed Web of Science ®Google Scholar
• Johnson VE, Stewart W, Smith DH. Axonal pathology in traumatic brain injury. Exp Neurol. 2013;246:35–43. doi:10.1016/j.expneurol.2012.01.013.
   PubMed Web of Science ®Google Scholar
• Wolf JA, Stys PK, Lusardi T, Meaney D, Smith DH. Traumatic axonal injury induces calcium influx modulated by tetrodotoxin-sensitive sodium channels. J Neurosci. 2001;21(6):1923–30.
   PubMed Web of Science ®Google Scholar
• Saatman KE, Creed J, Raghupathi R. Calpain as a therapeutic target in traumatic brain injury. Neurotherapeutics. 2010;7(1):31–42. doi:10.1016/j.nurt.2009.11.002.
   PubMed Web of Science ®Google Scholar
• Barkhoudarian G, Hovda DA, Giza CC. The molecular pathophysiology of concussive brain injury. Clin Sports Med. 2011;30(1):33–48, vii-iii. doi:10.1016/j.csm.2010.09.001.
   PubMed Web of Science ®Google Scholar
• Giza CC, Hovda DA. The neurometabolic cascade of concussion. J Athl Train. 2001;36(3):228–35.
   PubMed Web of Science ®Google Scholar
• Ikura M. Calcium binding and conformational response in ef-hand proteins. Trends Biochem Sci. 1996;21(1):14–17. doi:10.1016/S0968-0004(06)80021-6.
   PubMed Web of Science ®Google Scholar
• Bernstein HG, Baumann B, Danos P, Diekmann S, Bogerts B, Gundelfinger ED, Braunewell KH. Regional and cellular distribution of neural visinin-like protein immunoreactivities (vilip-1 and vilip-3) in human brain. J Neurocytol. 1999;28(8):655–62. doi:10.1023/A:1007056731551.
   PubMedGoogle Scholar
• Laterza OF, Modur VR, Crimmins DL, Olander JV, Landt Y, Lee JM, Ladenson JH. Identification of novel brain biomarkers. Clin Chem. 2006;52(9):1713–21. doi:10.1373/clinchem.2006.070912.
   PubMed Web of Science ®Google Scholar
• Stejskal D, Sporova L, Svestak M, Karpisek M. Determination of serum visinin like protein-1 and its potential for the diagnosis of brain injury due to the stroke: a pilot study. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub. 2011;155(3):263–68. doi:10.5507/bp.2011.049.
   PubMed Web of Science ®Google Scholar
• Shahim P, Mattsson N, Macy EM, Crimmins DL, Ladenson JH, Zetterberg H, Blennow K, Tegner Y. Serum visinin-like protein-1 in concussed professional ice hockey players. Brain Inj. 2015;29(7–8):872–76. doi:10.3109/02699052.2015.1018324.
   PubMed Web of Science ®Google Scholar
• Furman JL, Sompol P, Kraner SD, Pleiss MM, Putman EJ, Dunkerson J, Mohmmad Abdul H, Roberts KN, Scheff SW, Norris CM. Blockade of astrocytic calcineurin/nfat signaling helps to normalize hippocampal synaptic function and plasticity in a rat model of traumatic brain injury. J Neurosci. 2016;36(5):1502–15. doi:10.1523/JNEUROSCI.1930-15.2016.
   PubMed Web of Science ®Google Scholar
• Foda MA, Marmarou A. A new model of diffuse brain injury in rats. Part ii: morphological characterization. J Neurosurg. 1994;80(2):301–13. doi:10.3171/jns.1994.80.2.0301.
   PubMed Web of Science ®Google Scholar
• Marmarou A, Foda MA, van den Brink W, Campbell J, Kita H, Demetriadou K. A new model of diffuse brain injury in rats. Part i: pathophysiology and biomechanics. J Neurosurg. 1994;80(2):291–300. doi:10.3171/jns.1994.80.2.0291.
   PubMed Web of Science ®Google Scholar
• Schmued LC, Hopkins KJ. Fluoro-jade b: a high affinity fluorescent marker for the localization of neuronal degeneration. Brain Res. 2000;874(2):123–30. doi:10.1016/S0006-8993(00)02513-0.
   PubMed Web of Science ®Google Scholar
• Anderson KJ, Miller KM, Fugaccia I, Scheff SW. Regional distribution of fluoro-jade b staining in the hippocampus following traumatic brain injury. Exp Neurol. 2005;193(1):125–30. doi:10.1016/j.expneurol.2004.11.025.
   PubMed Web of Science ®Google Scholar
• Diaz-Arrastia R, Wang KK, Papa L, Sorani MD, Yue JK, Puccio AM, McMahon PJ, Inoue T, Yuh EL, Lingsma HF, et al.; T.-T. Investigators. Acute biomarkers of traumatic brain injury: relationship between plasma levels of ubiquitin c-terminal hydrolase-l1 and glial fibrillary acidic protein. J Neurotrauma. 2014;31(1):19–25. doi:10.1089/neu.2013.3040.
   PubMed Web of Science ®Google Scholar
• Posti JP, Hossain I, Takala RSK, Liedes H, Newcombe V, Outtrim J, Katila AJ, Frantzen J, Seppala HA, Coles JP, et al.; T. Investigators. Glial fibrillary acidic protein and ubiquitin c-terminal hydrolase-l1 are not specific biomarkers for mild ct-negative traumatic brain injury. J Neurotrauma. 2016;34(7):1–12.
   PubMed Web of Science ®Google Scholar
• Buonora JE, Yarnell AM, Lazarus RC, Mousseau M, Latour LL, Rizoli SB, Baker AJ, Rhind SG, Diaz-Arrastia R, Mueller GP. Multivariate analysis of traumatic brain injury: development of an assessment score. Front Neurol. 2015;6:68. doi:10.3389/fneur.2015.00068.
   PubMed Web of Science ®Google Scholar
• Lee JY, Lee CY, Kim HR, Lee CH, Kim HW, Kim JH. A role of serum-based neuronal and glial markers as potential predictors for distinguishing severity and related outcomes in traumatic brain injury. J Korean Neurosurg Soc. 2015;58(2):93–100. doi:10.3340/jkns.2015.58.2.93.
   PubMed Web of Science ®Google Scholar
• Lee JM, Blennow K, Andreasen N, Laterza O, Modur V, Olander J, Gao F, Ohlendorf M, Ladenson JH. The brain injury biomarker vlp-1 is increased in the cerebrospinal fluid of alzheimer disease patients. Clin Chem. 2008;54(10):1617–23. doi:10.1373/clinchem.2008.104497.
   PubMed Web of Science ®Google Scholar
• Tarawneh R, D’Angelo G, Macy E, Xiong C, Carter D, Cairns NJ, Fagan AM, Head D, Mintun MA, Ladenson JH, et al. Visinin-like protein-1: diagnostic and prognostic biomarker in alzheimer disease. Ann Neurol. 2011;70(2):274–85. doi:10.1002/ana.22448.
   PubMed Web of Science ®Google Scholar
• Tarawneh R, Head D, Allison S, Buckles V, Fagan AM, Ladenson JH, Morris JC, Holtzman DM. Cerebrospinal fluid markers of neurodegeneration and rates of brain atrophy in early alzheimer disease. JAMA Neurol. 2015;72(6):656–65. doi:10.1001/jamaneurol.2015.0202.
   PubMed Web of Science ®Google Scholar
• Tarawneh R, Lee JM, Ladenson JH, Morris JC, Holtzman DM. Csf vilip-1 predicts rates of cognitive decline in early alzheimer disease. Neurology. 2012;78(10):709–19. doi:10.1212/WNL.0b013e318248e568.
   PubMed Web of Science ®Google Scholar
• Luo X, Hou L, Shi H, Zhong X, Zhang Y, Zheng D, Tan Y, Hu G, Mu N, Chan J, et al. Csf levels of the neuronal injury biomarker visinin-like protein-1 in alzheimer’s disease and dementia with lewy bodies. J Neurochem. 2013;127(5):681–90. doi:10.1111/jnc.2013.127.issue-5.
   PubMed Web of Science ®Google Scholar
• Sutphen CL, Jasielec MS, Shah AR, Macy EM, Xiong C, Vlassenko AG, Benzinger TL, Stoops EE, Vanderstichele HM, Brix B, et al. Longitudinal cerebrospinal fluid biomarker changes in preclinical alzheimer disease during middle age. JAMA Neurol. 2015;72(9):1029–42. doi:10.1001/jamaneurol.2015.1285.
   PubMed Web of Science ®Google Scholar
• Mroczko B, Groblewska M, Zboch M, Muszynski P, Zajkowska A, Borawska R, Szmitkowski M, Kornhuber J, Lewczuk P. Evaluation of visinin-like protein 1 concentrations in the cerebrospinal fluid of patients with mild cognitive impairment as a dynamic biomarker of alzheimer’s disease. J Alzheimers Dis. 2015;43(3):1031–37.
   PubMed Web of Science ®Google Scholar
• Kester MI, Teunissen CE, Sutphen C, Herries EM, Ladenson JH, Xiong C, Scheltens P, Van Der Flier WM, Morris JC, Holtzman DM, et al. Cerebrospinal fluid vilip-1 and ykl-40, candidate biomarkers to diagnose, predict and monitor alzheimer’s disease in a memory clinic cohort. Alzheimers Res Ther. 2015;7(1):59. doi:10.1186/s13195-015-0142-1.
   PubMed Web of Science ®Google Scholar
• Scheff SW, Baldwin SA, Brown RW, Kraemer PJ. Morris water maze deficits in rats following traumatic brain injury: lateral controlled cortical impact. J Neurotrauma. 1997;14(9):615–27. doi:10.1089/neu.1997.14.615.
   PubMed Web of Science ®Google Scholar
• Chen ZJ, Sun LJ. Nonproteolytic functions of ubiquitin in cell signaling. Mol Cell. 2009;33(3):275–86. doi:10.1016/j.molcel.2009.01.014.
   PubMed Web of Science ®Google Scholar
• Sun L, Chen ZJ. The novel functions of ubiquitination in signaling. Curr Opin Cell Biol. 2004;16(2):119–26. doi:10.1016/j.ceb.2004.02.005.
   PubMed Web of Science ®Google Scholar
• Welchman RL, Gordon C, Mayer RJ. Ubiquitin and ubiquitin-like proteins as multifunctional signals. Nat Rev Mol Cell Biol. 2005;6(8):599–609. doi:10.1038/nrm1700.
   PubMed Web of Science ®Google Scholar
• Yao X, Liu J, McCabe JT. Ubiquitin and ubiquitin-conjugated protein expression in the rat cerebral cortex and hippocampus following traumatic brain injury (tbi). Brain Res. 2007;1182:116–22. doi:10.1016/j.brainres.2007.08.076.
   PubMed Web of Science ®Google Scholar
• Majetschak M, King DR, Krehmeier U, Busby LT, Thome C, Vajkoczy S, Proctor KG. Ubiquitin immunoreactivity in cerebrospinal fluid after traumatic brain injury: clinical and experimental findings. Crit Care Med. 2005;33(7):1589–94. doi:10.1097/01.CCM.0000169883.41245.23.
   PubMed Web of Science ®Google Scholar
• Plog BA, Dashnaw ML, Hitomi E, Peng W, Liao Y, Lou N, Deane R, Nedergaard M. Biomarkers of traumatic injury are transported from brain to blood via the glymphatic system. J Neurosci. 2015;35(2):518–26. doi:10.1523/JNEUROSCI.3742-14.2015.
   PubMed Web of Science ®Google Scholar
• Wilkinson KD, Lee KM, Deshpande S, Duerksen-Hughes P, Boss JM, Pohl J. The neuron-specific protein pgp 9.5 is a ubiquitin carboxyl-terminal hydrolase. Science. 1989;246(4930):670–73. doi:10.1126/science.2530630.
   PubMed Web of Science ®Google Scholar
• Liu Y, Fallon L, Lashuel HA, Liu Z, Lansbury PT Jr. The uch-l1 gene encodes two opposing enzymatic activities that affect alpha-synuclein degradation and parkinson’s disease susceptibility. Cell. 2002;111(2):209–18. doi:10.1016/S0092-8674(02)01012-7.
   PubMed Web of Science ®Google Scholar
• Osaka H, Wang YL, Takada K, Takizawa S, Setsuie R, Li H, Sato Y, Nishikawa K, Sun YJ, Sakurai M, et al. Ubiquitin carboxy-terminal hydrolase l1 binds to and stabilizes monoubiquitin in neuron. Hum Mol Genet. 2003;12(16):1945–58. doi:10.1093/hmg/ddg211.
   PubMed Web of Science ®Google Scholar
• Li Z, Melandri F, Berdo I, Jansen M, Hunter L, Wright S, Valbrun D, Figueiredo-Pereira ME. Delta12-prostaglandin j2 inhibits the ubiquitin hydrolase uch-l1 and elicits ubiquitin-protein aggregation without proteasome inhibition. Biochem Biophys Res Commun. 2004;319(4):1171–80. doi:10.1016/j.bbrc.2004.05.098.
   PubMed Web of Science ®Google Scholar
• Liu MC, Akinyi L, Scharf D, Mo J, Larner SF, Muller U, Oli MW, Zheng W, Kobeissy F, Papa L, et al. Ubiquitin c-terminal hydrolase-l1 as a biomarker for ischemic and traumatic brain injury in rats. Eur J Neurosci. 2010;31(4):722–32. doi:10.1111/j.1460-9568.2010.07097.x.
   PubMed Web of Science ®Google Scholar
• Lin L, Braunewell KH, Gundelfinger ED, Anand R. Functional analysis of calcium-binding ef-hand motifs of visinin-like protein-1. Biochem Biophys Res Commun. 2002;296(4):827–32. doi:10.1016/S0006-291X(02)00943-9.
   PubMed Web of Science ®Google Scholar
• Rebaud S, Simon A, Wang CK, Mason L, Blum L, Hofmann A, Girard-Egrot A. Comparison of vilip-1 and vilip-3 binding to phospholipid monolayers. PLoS One. 2014;9(4):e93948. doi:10.1371/journal.pone.0093948.
   PubMed Web of Science ®Google Scholar
• Rebaud S, Wang CK, Sarkis J, Mason L, Simon A, Blum LJ, Hofmann A, Girard-Egrot AP. Specific interaction to pip2 increases the kinetic rate of membrane binding of vilips, a subfamily of neuronal calcium sensors (ncs) proteins. Biochim Biophys Acta. 2014;1838(10):2698–707. doi:10.1016/j.bbamem.2014.06.021.
   PubMed Web of Science ®Google Scholar
• Liebl MP, Kaya AM, Tenzer S, Mittenzwei R, Koziollek-Drechsler I, Schild H, Moosmann B, Behl C, Clement AM. Dimerization of visinin-like protein 1 is regulated by oxidative stress and calcium and is a pathological hallmark of amyotrophic lateral sclerosis. Free Radic Biol Med. 2014;72:41–54. doi:10.1016/j.freeradbiomed.2014.04.008.
   PubMed Web of Science ®Google Scholar
• Spilker C, Braunewell KH. Calcium-myristoyl switch, subcellular localization, and calcium-dependent translocation of the neuronal calcium sensor protein vilip-3, and comparison with vilip-1 in hippocampal neurons. Mol Cell Neurosci. 2003;24(3):766–78. doi:10.1016/S1044-7431(03)00242-2.
   PubMed Web of Science ®Google Scholar
• Spilker C, Dresbach T, Braunewell KH. Reversible translocation and activity-dependent localization of the calcium-myristoyl switch protein vilip-1 to different membrane compartments in living hippocampal neurons. J Neurosci. 2002;22(17):7331–39.
   PubMed Web of Science ®Google Scholar
• Braunewell KH, Brackmann M, Schaupp M, Spilker C, Anand R, Gundelfinger ED. Intracellular neuronal calcium sensor (ncs) protein vilip-1 modulates cgmp signalling pathways in transfected neural cells and cerebellar granule neurones. J Neurochem. 2001;78(6):1277–86. doi:10.1046/j.1471-4159.2001.00506.x.
   PubMed Web of Science ®Google Scholar
• Zhao C, Anand R, Braunewell KH. Nicotine-induced ca2+-myristoyl switch of neuronal ca2+ sensor vilip-1 in hippocampal neurons: a possible crosstalk mechanism for nicotinic receptors. Cell Mol Neurobiol. 2009;29(2):273–86. doi:10.1007/s10571-008-9320-z.
   PubMed Web of Science ®Google Scholar
• Zhao CJ, Noack C, Brackmann M, Gloveli T, Maelicke A, Heinemann U, Anand R, Braunewell KH. Neuronal ca2+ sensor vilip-1 leads to the upregulation of functional alpha4beta2 nicotinic acetylcholine receptors in hippocampal neurons. Mol Cell Neurosci. 2009;40(2):280–92. doi:10.1016/j.mcn.2008.11.001.
   PubMed Web of Science ®Google Scholar
• Mathisen PM, Johnson JM, Kawczak JA, Tuohy VK. Visinin-like protein (vilip) is a neuron-specific calcium-dependent double-stranded RNA-binding protein. J Biol Chem. 1999;274(44):31571–76. doi:10.1074/jbc.274.44.31571.
   PubMed Web of Science ®Google Scholar
• Brackmann M, Schuchmann S, Anand R, Braunewell KH. Neuronal ca2+ sensor protein vilip-1 affects cgmp signalling of guanylyl cyclase b by regulating clathrin-dependent receptor recycling in hippocampal neurons. J Cell Sci. 2005;118(Pt 11):2495–505. doi:10.1242/jcs.02376.
   PubMed Web of Science ®Google Scholar