Generic placeholder image

CNS & Neurological Disorders - Drug Targets

Editor-in-Chief

ISSN (Print): 1871-5273
ISSN (Online): 1996-3181

Review Article

Pharmacological and Pathological Relevance of S100 Proteins in Neurological Disorders

Author(s): Deepali Goswami, Urati Anuradha, Anok Angati, Nisha Kumari and Rakesh Kumar Singh*

Volume 22, Issue 10, 2023

Published on: 13 January, 2023

Page: [1403 - 1416] Pages: 14

DOI: 10.2174/1871527322666221128160653

Price: $65

Abstract

The S100 protein is one of the calcium-binding proteins associated with Alzheimer’s disease, Parkinson’s disease, and amyotrophic lateral sclerosis. S100 proteins are expressed in the central nervous system by oligodendrocytes, astrocytes and neurons during both normal and disease conditions. Although amyloid-beta aggregation and hyperphosphorylated tau plaques are the main pathological hallmarks of Alzheimer’s disease, the S100 protein family is closely associated with neuroinflammation in several neurodegenerative disorders, such as Alzheimer’s disease, Parkinson’s disease, amyotrophic lateral sclerosis in addition to various types of cancer and other brain diseases. This review aims to present the key role of S100 proteins and their different relevant isoforms, along with the various approaches used for the regulation of these proteins in several neurodegenerative disorders.

Keywords: S100 protein, neurodegenerative disease, brain biomarker, Alzheimer’s disease, neuroinflammation, CNS.

Next »
Graphical Abstract
[1]
Berridge MJ, Lipp P, Bootman MD. The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol 2000; 1(1): 11-21.
[http://dx.doi.org/10.1038/35036035] [PMID: 11413485]
[2]
Kretsinger RH, Wasserman RH. Structure and evolution of calcium-modulated proteins. Crit Rev Biochem 1980; 8(2): 119-74.
[http://dx.doi.org/10.3109/10409238009105467] [PMID: 6105043]
[3]
Yardan T, Erenler AK, Baydin A, Aydin K, Cokluk C. Usefulness of S100B protein in neurological disorders. J Pak Med Assoc 2011; 61(3): 276-81.
[PMID: 21465945]
[4]
Langeh U, Singh S. Targeting S100B protein as a surrogate biomarker and its role in various neurological disorders. Curr Neuropharmacol 2020; 19(2): 265-77.
[http://dx.doi.org/10.2174/1570159X18666200729100427] [PMID: 32727332]
[5]
Lodeiro M, Puerta E, Ismail MA, et al. Aggregation of the inflammatory s100a8 precedes aβ plaque formation in transgenic app mice: positive feedback for s100a8 and aβ productions. J Gerontol A Biol Sci Med Sci 2017; 72(3): 319-28.
[PMID: 27131040]
[6]
Heizmann CW. S100 proteins: Diagnostic and prognostic biomarkers in laboratory medicine. Biochim Biophys Acta Mol Cell Res 2019; 1866(7): 1197-206.
[http://dx.doi.org/10.1016/j.bbamcr.2018.10.015] [PMID: 30392897]
[7]
Sreejit G, Flynn MC, Patil M, Krishnamurthy P, Murphy AJ, Nagareddy PR. S100 family proteins in inflammation and beyond. Adv Clin Chem 2020; 98: 173-231.
[http://dx.doi.org/10.1016/bs.acc.2020.02.006] [PMID: 32564786]
[8]
Green AJE, Harvey RJ, Thompson EJ, Rossor MN. Increased S100β in the cerebrospinal fluid of patients with frontotemporal dementia. Neurosci Lett 1997; 235(1-2): 5-8.
[http://dx.doi.org/10.1016/S0304-3940(97)00701-5] [PMID: 9389582]
[9]
Fox NC, Freeborough PA. Brain atrophy progression measured from registered serial MRI: Validation and application to alzheimer’s disease. J Magn Reson Imaging 1997; 7(6): 1069-75.
[http://dx.doi.org/10.1002/jmri.1880070620] [PMID: 9400851]
[10]
Peña LA, Brecher CW, Marshak DR. β-Amyloid regulates gene expression of glial trophic substance S100β in C6 glioma and primary astrocyte cultures. Brain Res Mol Brain Res 1995; 34(1): 118-26.
[http://dx.doi.org/10.1016/0169-328X(95)00145-I] [PMID: 8750867]
[11]
Steiner J, Bernstein HG, Bielau H, et al. Evidence for a wide extra-astrocytic distribution of S100B in human brain. BMC Neurosci 2007; 8(1): 2.
[http://dx.doi.org/10.1186/1471-2202-8-2] [PMID: 17199889]
[12]
Donato R. S100: a multigenic family of calcium-modulated proteins of the EF-hand type with intracellular and extracellular functional roles. Int J Biochem Cell Biol 2001; 33(7): 637-68.
[http://dx.doi.org/10.1016/S1357-2725(01)00046-2] [PMID: 11390274]
[13]
Rothermundt M, Peters M, Prehn JHM, Arolt V. S100B in brain damage and neurodegeneration. Microsc Res Tech 2003; 60(6): 614-32.
[http://dx.doi.org/10.1002/jemt.10303] [PMID: 12645009]
[14]
Sheng JG, Mrak RE, Griffin WST. S100? protein expression in Alzheimer disease: Potential role in the pathogenesis of neuritic plaques. J Neurosci Res 1994; 39(4): 398-404.
[http://dx.doi.org/10.1002/jnr.490390406] [PMID: 7884819]
[15]
Roltsch E, Holcomb L, Young KA, Marks A, Zimmer DB. PSAPP mice exhibit regionally selective reductions in gliosis and plaque dep-osition in response to S100B ablation. J Neuroinflammation 2010; 7(1): 78.
[http://dx.doi.org/10.1186/1742-2094-7-78] [PMID: 21080947]
[16]
Mori T, Koyama N, Arendash GW, Horikoshi-Sakuraba Y, Tan J, Town T. Overexpression of human S100B exacerbates cerebral amy-loidosis and gliosis in the Tg2576 mouse model of Alzheimer’s disease. Glia 2010; 58(3): 300-14.
[PMID: 19705461]
[17]
Boom A, Pochet R, Authelet M, et al. Astrocytic calcium/zinc binding protein S100A6 over expression in Alzheimer’s disease and in PS1/APP transgenic mice models. Biochim Biophys Acta Mol Cell Res 2004; 1742(1-3): 161-8.
[http://dx.doi.org/10.1016/j.bbamcr.2004.09.011] [PMID: 15590066]
[18]
Weissmann R, Hüttenrauch M, Kacprowski T, et al. Gene expression profiling in the APP/PS1KI mouse model of familial Alzheimer’s Disease. J Alzheimers Dis 2016; 50(2): 397-409.
[http://dx.doi.org/10.3233/JAD-150745] [PMID: 26639971]
[19]
Teigelkamp S, Bhardwaj RS, Roth J, Meinardus-Hager G, Karas M, Sorg C. Calcium-dependent complex assembly of the myeloic differ-entiation proteins MRP-8 and MRP-14. J Biol Chem 1991; 266(20): 13462-7.
[http://dx.doi.org/10.1016/S0021-9258(18)98862-9] [PMID: 2071612]
[20]
Qin W, Ho L, Wang J, Peskind E, Pasinetti GM. S100A7, a novel Alzheimer’s disease biomarker with non-amyloidogenic alpha-secretase activity acts via selective promotion of ADAM-10. PLoS One 2009; 4(1)e4183
[http://dx.doi.org/10.1371/journal.pone.0004183] [PMID: 19159013]
[21]
Carvalho A, Lu J, Francis JD, et al. S100A12 in Digestive Diseases and Health: A Scoping Review. Gastroenterol Res Pract 2020; 2020: 1-11.
[http://dx.doi.org/10.1155/2020/2868373] [PMID: 32184815]
[22]
Heizmann CW. Ca2+-binding S100 proteins in the central nervous system. Neurochem Res 1999; 24(9): 1097-100.
[http://dx.doi.org/10.1023/A:1020700117665] [PMID: 10485579]
[23]
Astrand R, Undén J, Romner B. Clinical use of the calcium-binding S100B protein. Methods Mol Biol 2013; 963: 373-84.
[http://dx.doi.org/10.1007/978-1-62703-230-8_23] [PMID: 23296623]
[24]
Moore BW. A soluble protein characteristic of the nervous system. Biochem Biophys Res Commun 1965; 19(6): 739-44.
[http://dx.doi.org/10.1016/0006-291X(65)90320-7] [PMID: 4953930]
[25]
Isobe T, Okuyama T. The amino-acid sequence of the alpha subunit in bovine brain S-100a protein. Eur J Biochem 1981; 116(1): 79-86.
[http://dx.doi.org/10.1111/j.1432-1033.1981.tb05303.x] [PMID: 7250124]
[26]
Isobe T, Okuyama T. The amino-acid sequence of S-100 protein (PAP I-b protein) and its relation to the calcium-binding proteins. Eur J Biochem 1978; 89(2): 379-88.
[http://dx.doi.org/10.1111/j.1432-1033.1978.tb12539.x] [PMID: 710399]
[27]
Zimmer DB, Cornwall EH, Landar A, Song W. The S100 protein family: History, function, and expression. Brain Res Bull 1995; 37(4): 417-29.
[http://dx.doi.org/10.1016/0361-9230(95)00040-2] [PMID: 7620916]
[28]
Steiner J, Bogerts B, Schroeter ML, Bernstein HG. S100B protein in neurodegenerative disorders. Clin Chem Lab Med 2011; 49(3): 409-24.
[http://dx.doi.org/10.1515/CCLM.2011.083] [PMID: 21303299]
[29]
Leclerc E, Fritz G, Vetter SW, Heizmann CW. Binding of S100 proteins to RAGE: An update. Biochim Biophys Acta Mol Cell Res 2009; 1793(6): 993-1007.
[http://dx.doi.org/10.1016/j.bbamcr.2008.11.016] [PMID: 19121341]
[30]
Heizmann CW, Fritz G, Schäfer BW. S100 proteins: structure, functions and pathology. Front Biosci: J Virtual Librar 2002; 7: d1356-68.
[31]
Donato R. Functional roles of S100 proteins, calcium-binding proteins of the EF-hand type. Biochim Biophys Acta Mol Cell Res 1999; 1450(3): 191-231.
[http://dx.doi.org/10.1016/S0167-4889(99)00058-0] [PMID: 10395934]
[32]
Ferguson PL, Shaw GS. Role of the N-terminal helix I for dimerization and stability of the calcium-binding protein S100B. Biochemistry 2002; 41(11): 3637-46.
[http://dx.doi.org/10.1021/bi0118052] [PMID: 11888280]
[33]
Michetti F, Di Sante G, Clementi ME, et al. Growing role of S100B protein as a putative therapeutic target for neurological- and nonneurological-disorders. Neurosci Biobehav Rev 2021; 127: 446-58.
[http://dx.doi.org/10.1016/j.neubiorev.2021.04.035] [PMID: 33971224]
[34]
Donato R, Cannon B, Sorci G, Riuzzi F, Hsu K, Weber D, et al. Functions of S100 proteins. Curr Mol Med 2012; 13.
[PMID: 22834835]
[35]
Mori T, Asano T, Town T. Targeting S100B in cerebral ischemia and in Alzheimer’s disease. Cardiovasc Psychiatry Neurol 2010; 2010687067
[36]
Marenholz I, Heizmann CW, Fritz G. S100 proteins in mouse and man: from evolution to function and pathology (including an update of the nomenclature). Biochem Biophys Res Commun 2004; 322(4): 1111-22.
[http://dx.doi.org/10.1016/j.bbrc.2004.07.096] [PMID: 15336958]
[37]
Marenholz I, Lovering RC, Heizmann CW. An update of the S100 nomenclature. Biochimica et Biophysica Acta (BBA) -. Molecular Cell Research 2006; 1763(11): 1282-3.
[38]
Kizawa K, Takahara H, Unno M, Heizmann CW. S100 and S100 fused-type protein families in epidermal maturation with special focus on S100A3 in mammalian hair cuticles. Biochimie 2011; 93(12): 2038-47.
[http://dx.doi.org/10.1016/j.biochi.2011.05.028] [PMID: 21664410]
[39]
Xia C, Braunstein Z, Toomey AC, Zhong J, Rao X. S100 proteins as an important regulator of macrophage inflammation. Front Immunol 2018; 8: 1908.
[http://dx.doi.org/10.3389/fimmu.2017.01908] [PMID: 29379499]
[40]
Arcuri C, Bianchi R, Brozzi F, Donato R. S100B increases proliferation in PC12 neuronal cells and reduces their responsiveness to nerve growth factor via Akt activation. J Biol Chem 2005; 280(6): 4402-14.
[http://dx.doi.org/10.1074/jbc.M406440200] [PMID: 15572370]
[41]
Santamaria-Kisiel L, Rintala-Dempsey AC, Shaw GS. Calcium-dependent and -independent interactions of the S100 protein family. Biochem J 2006; 396(2): 201-14.
[http://dx.doi.org/10.1042/BJ20060195] [PMID: 16683912]
[42]
Mrak R, Griffinbc WS. The role of activated astrocytes and of the neurotrophic cytokine S100B in the pathogenesis of Alzheimer’s dis-ease. Neurobiol Aging 2001; 22(6): 915-22.
[http://dx.doi.org/10.1016/S0197-4580(01)00293-7] [PMID: 11754999]
[43]
de Souza DF, Leite MC, Quincozes-Santos A, et al. S100B secretion is stimulated by IL-1β in glial cultures and hippocampal slices of rats: Likely involvement of MAPK pathway. J Neuroimmunol 2009; 206(1-2): 52-7.
[http://dx.doi.org/10.1016/j.jneuroim.2008.10.012] [PMID: 19042033]
[44]
Nardin P, Tortorelli L, Quincozes-Santos A, et al. S100B secretion in acute brain slices: modulation by extracellular levels of Ca(2+) and K.(+) Neurochem Res 2009; 34(9): 1603-11.
[http://dx.doi.org/10.1007/s11064-009-9949-0] [PMID: 19288274]
[45]
Tramontina AC, Tramontina F, Bobermin LD, et al. Secretion of S100B, an astrocyte-derived neurotrophic protein, is stimulated by fluoxetine via a mechanism independent of serotonin. Prog Neuropsychopharmacol Biol Psychiatry 2008; 32(6): 1580-3.
[http://dx.doi.org/10.1016/j.pnpbp.2008.06.001] [PMID: 18582527]
[46]
Donato R, Sorci G, Riuzzi F, et al. S100B’s double life: Intracellular regulator and extracellular signal. Biochim Biophys Acta Mol Cell Res 2009; 1793(6): 1008-22.
[http://dx.doi.org/10.1016/j.bbamcr.2008.11.009] [PMID: 19110011]
[47]
Sedaghat F, Notopoulos A. S100 protein family and its application in clinical practice. Hippokratia 2008; 12(4): 198-204.
[PMID: 19158963]
[48]
Harpio R, Einarsson R. S100 proteins as cancer biomarkers with focus on S100B in malignant melanoma. Clin Biochem 2004; 37(7): 512-8.
[http://dx.doi.org/10.1016/j.clinbiochem.2004.05.012] [PMID: 15234232]
[49]
Sathe K, Maetzler W, Lang JD, et al. S100B is increased in Parkinson’s disease and ablation protects against MPTP-induced toxicity through the RAGE and TNF-α pathway. Brain 2012; 135(11): 3336-47.
[http://dx.doi.org/10.1093/brain/aws250] [PMID: 23169921]
[50]
Hofmann MA, Drury S, Fu C, et al. RAGE mediates a novel proinflammatory axis: A central cell surface receptor for S100/] calgranulin polypeptides. Cell 1999; 97(7): 889-901.
[http://dx.doi.org/10.1016/S0092-8674(00)80801-6] [PMID: 10399917]
[51]
Cristóvão JS, Gomes CM. S100 Proteins in Alzheimer’s Disease. Front Neurosci 2019; 13: 463.
[http://dx.doi.org/10.3389/fnins.2019.00463] [PMID: 31156365]
[52]
Botelho HM, Fritz G, Gomes CM. Analysis of S100 oligomers and amyloids. Methods Mol Biol 2012; 849: 373-86.
[http://dx.doi.org/10.1007/978-1-61779-551-0_25] [PMID: 22528103]
[53]
Businaro R, Leone S, Fabrizi C, et al. S100B protects LAN-5 neuroblastoma cells against Aβ amyloid-induced neurotoxicity via RAGE engagement at low doses but increases Aβ amyloid neurotoxicity at high doses. J Neurosci Res 2006; 83(5): 897-906.
[http://dx.doi.org/10.1002/jnr.20785] [PMID: 16477616]
[54]
LaFerla FM. Calcium dyshomeostasis and intracellular signalling in alzheimer’s disease. Nat Rev Neurosci 2002; 3(11): 862-72.
[http://dx.doi.org/10.1038/nrn960] [PMID: 12415294]
[55]
Wang X, Wang W, Li L, Perry G, Lee H, Zhu X. Oxidative stress and mitochondrial dysfunction in Alzheimer’s disease. Biochim Biophys Acta Mol Basis Dis 2014; 1842(8): 1240-7.
[http://dx.doi.org/10.1016/j.bbadis.2013.10.015] [PMID: 24189435]
[56]
Xiong Z, O’Hanlon D, Becker LE, Roder J, MacDonald JF, Marks A. Enhanced calcium transients in glial cells in neonatal cerebellar cultures derived from S100B null mice. Exp Cell Res 2000; 257(2): 281-9.
[http://dx.doi.org/10.1006/excr.2000.4902] [PMID: 10837142]
[57]
Masters CL, Bateman R, Blennow K, Rowe CC, Sperling RA, Cummings JL. Alzheimer’s disease. Nat Rev Dis Primers 2015; 1(1): 15056.
[http://dx.doi.org/10.1038/nrdp.2015.56] [PMID: 27188934]
[58]
Weiner HL, Frenkel D. Immunology and immunotherapy of Alzheimer’s disease. Nat Rev Immunol 2006; 6(5): 404-16.
[http://dx.doi.org/10.1038/nri1843] [PMID: 16639431]
[59]
Sen J, Belli A. S100B in neuropathologic states: The CRP of the brain? J Neurosci Res 2007; 85(7): 1373-80.
[http://dx.doi.org/10.1002/jnr.21211] [PMID: 17348038]
[60]
Petzold A, Jenkins R, Watt HC, et al. Cerebrospinal fluid S100B correlates with brain atrophy in Alzheimer’s disease. Neurosci Lett 2003; 336(3): 167-70.
[http://dx.doi.org/10.1016/S0304-3940(02)01257-0] [PMID: 12505619]
[61]
Wilhelm KR, Yanamandra K, Gruden MA, et al. Immune reactivity towards insulin, its amyloid and protein S100B in blood sera of Par-kinson’s disease patients. Eur J Neurol 2007; 14(3): 327-34.
[http://dx.doi.org/10.1111/j.1468-1331.2006.01667.x] [PMID: 17355556]
[62]
Leclerc E, Sturchler E, Vetter SW. The S100B/RAGE Axis in Alzheimer’s Disease. Cardiovasc Psychiatry Neurol 2010; 2010: 1-11.
[http://dx.doi.org/10.1155/2010/539581] [PMID: 20672051]
[63]
González-Reyes RE, Nava-Mesa MO, Vargas-Sánchez K, Ariza-Salamanca D, Mora-Muñoz L. Involvement of astrocytes in alzheimer’s disease from a neuroinflammatory and oxidative stress perspective. Front Mol Neurosci 2017; 10: 427.
[http://dx.doi.org/10.3389/fnmol.2017.00427] [PMID: 29311817]
[64]
Zimmer DB, Chaplin J, Baldwin A, Rast M. S100-mediated signal transduction in the nervous system and neurological diseases Cellular and molecular biology (Noisy-le-Grand, France) 2005; 51(2): 201-14.
[65]
Chang KA, Kim HJ, Suh YH. The role of S100a9 in the pathogenesis of Alzheimer’s disease: the therapeutic effects of S100a9 knock-down or knockout. Neurodegener Dis 2012; 10(1-4): 27-9.
[http://dx.doi.org/10.1159/000333781] [PMID: 22301734]
[66]
Wu L, Zhou X, Xiao Z, et al. Functional expression, characterization, and application of human S100B. Oncol Rep 2017; 38(4): 2309-16.
[http://dx.doi.org/10.3892/or.2017.5922] [PMID: 28849099]
[67]
Angelopoulou E, Paudel YN, Piperi C. Emerging role of S100B protein implication in Parkinson’s disease pathogenesis. Cell Mol Life Sci 2021; 78(4): 1445-53.
[http://dx.doi.org/10.1007/s00018-020-03673-x] [PMID: 33052436]
[68]
Muramatsu Y, Kurosaki R, Watanabe H, et al. Expression of S-100 protein is related to neuronal damage in MPTP-treated mice. Glia 2003; 42(3): 307-13.
[http://dx.doi.org/10.1002/glia.10225] [PMID: 12673835]
[69]
Isobe T, Ishioka N, Masuda T, Takahashi Y, Ganno S, Okuyama T. A rapid separation of S100 subunits by high performance liquid chromatography: the subunit compositions of S100 proteins. Biochem Int 1983; 6(3): 419-26.
[PMID: 6679332]
[70]
Michetti F, D’Ambrosi N, Toesca A, et al. The S100B story: from biomarker to active factor in neural injury. J Neurochem 2019; 148(2): 168-87.
[http://dx.doi.org/10.1111/jnc.14574] [PMID: 30144068]
[71]
Huttunen HJ, Kuja-Panula J, Sorci G, Agneletti AL, Donato R. Coregulation of neurite outgrowth and cell survival by amphoterin and S100 proteins through receptor for advanced glycation end products (RAGE) activation. 2000; 275(51): 40096-105.
[72]
Selinfreund RH, Barger SW, Pledger WJ, Van Eldik LJ. Neurotrophic protein S100 beta stimulates glial cell proliferation. Proc Natl Acad Sci 1991; 88(9): 3554-8.
[http://dx.doi.org/10.1073/pnas.88.9.3554] [PMID: 1902567]
[73]
Hagmeyer S, Cristóvão JS, Mulvihill JJE, Boeckers TM, Gomes CM, Grabrucker AM. Zinc binding to S100B affords regulation of trace metal homeostasis and excitotoxicity in the brain. Front Mol Neurosci 2018; 10: 456.
[http://dx.doi.org/10.3389/fnmol.2017.00456] [PMID: 29386995]
[74]
Baudier J, Cole RD. Interactions between the microtubule-associated tau proteins and S100b regulate tau phosphorylation by the Ca2+/calmodulin-dependent protein kinase II. J Biol Chem 1988; 263(12): 5876-83.
[http://dx.doi.org/10.1016/S0021-9258(18)60647-7] [PMID: 2833519]
[75]
Landar A, Caddell G, Chessher J, Zimmer DB. Identification of an S100A1/S100B target protein: phosphoglucomutase. Cell Calcium 1996; 20(3): 279-85.
[http://dx.doi.org/10.1016/S0143-4160(96)90033-0] [PMID: 8894274]
[76]
Zimmer DB, Van Eldik LJ. Identification of a molecular target for the calcium-modulated protein S100. Fructose-1,6-bisphosphate al-dolase. J Biol Chem 1986; 261(24): 11424-8.
[http://dx.doi.org/10.1016/S0021-9258(18)67402-2] [PMID: 3733759]
[77]
Jönsson H, Johnsson P, Höglund P, Alling C, Blomquist S. Elimination of S100B and renal function after cardiac surgery. J Cardiothorac Vasc Anesth 2000; 14(6): 698-701.
[http://dx.doi.org/10.1053/jcan.2000.18444] [PMID: 11139112]
[78]
Braak H, Braak E. Development of Alzheimer-related neurofibrillary changes in the neocortex inversely recapitulates cortical myelogene-sis. Acta Neuropathol 1996; 92(2): 197-201.
[http://dx.doi.org/10.1007/s004010050508] [PMID: 8841666]
[79]
Cristóvão JS, Morris VK, Cardoso I, Leal SS, Martínez J, Botelho HM, et al. The neuronal S100B protein is a calcium-tuned suppressor of amyloid-β aggregation. Science advances 2018; 4(6): eaaq1702.
[80]
Prosser BL, Hernández-Ochoa EO, Schneider MF. S100A1 and calmodulin regulation of ryanodine receptor in striated muscle. Cell Calcium 2011; 50(4): 323-31.
[http://dx.doi.org/10.1016/j.ceca.2011.06.001] [PMID: 21784520]
[81]
Afanador L, Roltsch EA, Holcomb L, et al. The Ca2+ sensor S100A1 modulates neuroinflammation, histopathology and Akt activity in the PSAPP Alzheimer’s disease mouse model. Cell Calcium 2014; 56(2): 68-80.
[http://dx.doi.org/10.1016/j.ceca.2014.05.002] [PMID: 24931125]
[82]
Del Prete D, Checler F, Chami M. Ryanodine receptors: physiological function and deregulation in Alzheimer disease. Mol Neurodegener 2014; 9(1): 21.
[http://dx.doi.org/10.1186/1750-1326-9-21] [PMID: 24902695]
[83]
Hooper C, Killick R, Lovestone S. The GSK3 hypothesis of Alzheimer’s disease. J Neurochem 2008; 104(6): 1433-9.
[http://dx.doi.org/10.1111/j.1471-4159.2007.05194.x] [PMID: 18088381]
[84]
Schäfer BW, Heizmann CW. The S100 family of EF-hand calcium-binding proteins: functions and pathology. Trends Biochem Sci 1996; 21(4): 134-40.
[http://dx.doi.org/10.1016/S0968-0004(96)80167-8] [PMID: 8701470]
[85]
Hoyaux D, Alao J, Fuchs J, Kiss R, Keller B, Heizmann CW, et al. S100A6, a calcium-and zinc-binding protein, is overexpressed in SOD1 mutant mice, a model for amyotrophic lateral sclerosis. Biochimica et Biophysica Acta (BBA)-. Molecular Cell Research 2000; 1498(2-3): 264-72.
[PMID: 11108968]
[86]
Shaw P, Eggett CJ. Molecular factors underlying selective vulnerability of motor neurons to neurodegeneration in amyotrophic lateral sclerosis. J Neurol 2000; 247 (Suppl. 1): I17-27.
[http://dx.doi.org/10.1007/BF03161151] [PMID: 10795883]
[87]
Wong PC, Pardo CA, Borchelt DR, et al. An adverse property of a familial ALS-linked SOD1 mutation causes motor neuron disease characterized by vacuolar degeneration of mitochondria. Neuron 1995; 14(6): 1105-16.
[http://dx.doi.org/10.1016/0896-6273(95)90259-7] [PMID: 7605627]
[88]
Bruijn LI, Becher MW, Lee MK, et al. ALS-linked SOD1 mutant G85R mediates damage to astrocytes and promotes rapidly progressive disease with SOD1-containing inclusions. Neuron 1997; 18(2): 327-38.
[http://dx.doi.org/10.1016/S0896-6273(00)80272-X] [PMID: 9052802]
[89]
Filipek A, Leśniak W. S100A6 and its brain ligands in neurodegenerative disorders. Int J Mol Sci 2020; 21(11): 3979.
[http://dx.doi.org/10.3390/ijms21113979] [PMID: 32492924]
[90]
Mueller C, Zhou W, VanMeter A, et al. The heme degradation pathway is a promising serum biomarker source for the early detection of Alzheimer’s disease. J Alzheimers Dis 2010; 19(3): 1081-91.
[http://dx.doi.org/10.3233/JAD-2010-1303] [PMID: 20157261]
[91]
Shen L, Liao L, Chen C, et al. Proteomics analysis of blood serums from alzheimer’s disease patients using itraq labeling technology. J Alzheimers Dis 2017; 56(1): 361-78.
[http://dx.doi.org/10.3233/JAD-160913] [PMID: 27911324]
[92]
Shepherd CE, Goyette J, Utter V, et al. Inflammatory S100A9 and S100A12 proteins in Alzheimer’s disease. Neurobiol Aging 2006; 27(11): 1554-63.
[http://dx.doi.org/10.1016/j.neurobiolaging.2005.09.033] [PMID: 16253391]
[93]
Kummer MP, Vogl T, Axt D, et al. Mrp14 deficiency ameliorates amyloid β burden by increasing microglial phagocytosis and modula-tion of amyloid precursor protein processing. J Neurosci 2012; 32(49): 17824-9.
[http://dx.doi.org/10.1523/JNEUROSCI.1504-12.2012] [PMID: 23223301]
[94]
Zhang C, Liu Y, Gilthorpe J, van der Maarel JRC. MRP14 (S100A9) protein interacts with Alzheimer beta-amyloid peptide and induces its fibrillization. PLoS One 2012; 7(3)e32953
[http://dx.doi.org/10.1371/journal.pone.0032953] [PMID: 22457725]
[95]
Ha TY, Chang KA, Kim J, et al. S100a9 knockdown decreases the memory impairment and the neuropathology in Tg2576 mice, AD animal model. PLoS One 2010; 5(1)e8840
[http://dx.doi.org/10.1371/journal.pone.0008840] [PMID: 20098622]
[96]
Venegas C, Heneka MT. Danger-associated molecular patterns in Alzheimer’s disease. J Leukoc Biol 2017; 101(1): 87-98.
[http://dx.doi.org/10.1189/jlb.3MR0416-204R] [PMID: 28049142]
[97]
Xu Y, Li G, Chen H, Cheng L, Zhao R, Zhao J. Amyloid precursor-like protein 2 C-terminal fragments upregulate S100A9 gene and protein expression in BV2 cells. Neural Regen Res 2014; 9(21): 1923-8.
[http://dx.doi.org/10.4103/1673-5374.145362] [PMID: 25558244]
[98]
Markowitz J, Carson WE III. Review of S100A9 biology and its role in cancer. Biochim Biophys Acta 2013; 1835(1): 100-9.
[PMID: 23123827]
[99]
Roth J, Vogl T, Sorg C, Sunderkötter C. Phagocyte-specific S100 proteins: a novel group of proinflammatory molecules. Trends Immunol 2003; 24(4): 155-8.
[http://dx.doi.org/10.1016/S1471-4906(03)00062-0] [PMID: 12697438]
[100]
Horvath I, Jia X, Johansson P, et al. Pro-inflammatory s100a9 protein as a robust biomarker differentiating early stages of cognitive impairment in Alzheimer’s Disease. ACS Chem Neurosci 2016; 7(1): 34-9.
[http://dx.doi.org/10.1021/acschemneuro.5b00265] [PMID: 26550994]
[101]
Wilkinson MM, Busuttil A, Hayward C, Brock DJ, Dorin JR, Van Heyningen V. Expression pattern of two related cystic fibrosis-associated calcium-binding proteins in normal and abnormal tissues. J Cell Sci 1988; 91(2): 221-30.
[http://dx.doi.org/10.1242/jcs.91.2.221] [PMID: 3267695]
[102]
Potts BC, Carlström G, Okazaki K, Hidaka H, Chazin WJ. 1H NMR assignments of apo calcyclin and comparative structural analysis with calbindin D9k and S100 beta. Protein science : a publication of the Protein Society 1996; 5(11): 2162-74.
[103]
Botelho HM, Koch M, Fritz G, Gomes CM. Metal ions modulate the folding and stability of the tumor suppressor protein S100A2. FEBS J 2009; 276(6): 1776-86.
[http://dx.doi.org/10.1111/j.1742-4658.2009.06912.x] [PMID: 19267779]
[104]
Heizmann CW, Cox JA. New perspectives on S100 proteins: a multi-functional Ca(2+)-, Zn(2+)- and Cu(2+)-binding protein family. Biometals : an international journal on the role of metal ions in biology, biochemistry, and medicine 1998; 11(4): 383-97.
[105]
Steinbakk M, Naess-Andresen C-F, Fagerhol MK, Lingaas E, Dale I, Brandtzaeg P. Antimicrobial actions of calcium binding leucocyte L1 protein, calprotectin. Lancet 1990; 336(8718): 763-5.
[http://dx.doi.org/10.1016/0140-6736(90)93237-J] [PMID: 1976144]
[106]
Yanamandra K, Alexeyev O, Zamotin V, et al. Amyloid formation by the pro-inflammatory S100A8/A9 proteins in the ageing prostate. PLoS One 2009; 4(5)e5562
[http://dx.doi.org/10.1371/journal.pone.0005562] [PMID: 19440546]
[107]
Hoyaux D, Decaestecker C, Heizmann CW, et al. S100 proteins in Corpora amylacea from normal human brain. Brain Res 2000; 867(1-2): 280-8.
[http://dx.doi.org/10.1016/S0006-8993(00)02393-3] [PMID: 10837826]
[108]
Salama I, Malone PS, Mihaimeed F, Jones JL. A review of the S100 proteins in cancer. Eur J Surg Oncol 2008; 34(4): 357-64.
[http://dx.doi.org/10.1016/j.ejso.2007.04.009]
[109]
van Lent PLEM, Grevers L, Blom AB, et al. Myeloid-related proteins S100A8/S100A9 regulate joint inflammation and cartilage destruc-tion during antigen-induced arthritis. Ann Rheum Dis 2008; 67(12): 1750-8.
[http://dx.doi.org/10.1136/ard.2007.077800] [PMID: 18055478]
[110]
Gonzalez LL, Garrie K, Turner MD. Role of S100 proteins in health and disease. Biochim Biophys Acta Mol Cell Res 2020; 1867(6)118677
[http://dx.doi.org/10.1016/j.bbamcr.2020.118677] [PMID: 32057918]
[111]
Vogl T, Gharibyan AL, Morozova-Roche LA. Pro-inflammatory S100A8 and S100A9 proteins: self-assembly into multifunctional native and amyloid complexes. Int J Mol Sci 2012; 13(3): 2893-917.
[http://dx.doi.org/10.3390/ijms13032893] [PMID: 22489132]
[112]
Kayed R, Head E, Sarsoza F, et al. Fibril specific, conformation dependent antibodies recognize a generic epitope common to amyloid fibrils and fibrillar oligomers that is absent in prefibrillar oligomers. Mol Neurodegener 2007; 2(1): 18.
[http://dx.doi.org/10.1186/1750-1326-2-18] [PMID: 17897471]
[113]
Wang S, Song R, Wang Z, Jing Z, Wang S, Ma J. S100A8/A9 in Inflammation. Front Immunol 2018; 9: 1298.
[http://dx.doi.org/10.3389/fimmu.2018.01298] [PMID: 29942307]
[114]
Zhang L, Bukulin M, Kojro E, et al. Receptor for advanced glycation end products is subjected to protein ectodomain shedding by metal-loproteinases. J Biol Chem 2008; 283(51): 35507-16.
[http://dx.doi.org/10.1074/jbc.M806948200] [PMID: 18952609]
[115]
Bianchi R, Giambanco I, Donato R. S100B/RAGE-dependent activation of microglia via NF-kappaB and AP-1 Co-regulation of COX-2 expression by S100B, IL-1beta and TNF-alpha. Neurobiol Aging 2010; 31(4): 665-77.
[http://dx.doi.org/10.1016/j.neurobiolaging.2008.05.017] [PMID: 18599158]
[116]
Yang W, Nam K, Ju J, Lee K, Oh S, Shin I. S100A4 negatively regulates β-catenin by inducing the Egr-1-PTEN-Akt-GSK3β degradation pathway. Cell Signal 2014; 26(10): 2096-106.
[http://dx.doi.org/10.1016/j.cellsig.2014.06.007] [PMID: 24975844]
[117]
Park SY, Kim JY, Choi JH, et al. Inhibition of LEF1-Mediated DCLK1 by niclosamide attenuates colorectal cancer stemness. Clin Cancer Res 2019; 25(4): 1415-29.
[http://dx.doi.org/10.1158/1078-0432.CCR-18-1232] [PMID: 30446587]
[118]
Bresnick AR. S100 proteins as therapeutic targets. Biophys Rev 2018; 10(6): 1617-29.
[http://dx.doi.org/10.1007/s12551-018-0471-y] [PMID: 30382555]
[119]
Gao H, Zhang IY, Zhang L, et al. S100B suppression alters polarization of infiltrating myeloid-derived cells in gliomas and inhibits tu-mor growth. Cancer Lett 2018; 439: 91-100.
[http://dx.doi.org/10.1016/j.canlet.2018.07.034] [PMID: 30076898]
[120]
Malashkevich VN, Dulyaninova NG, Ramagopal UA, et al. Phenothiazines inhibit S100A4 function by inducing protein oligomerization. Proc Natl Acad Sci 2010; 107(19): 8605-10.
[http://dx.doi.org/10.1073/pnas.0913660107] [PMID: 20421509]
[121]
Schmidt AM, Yan SD, Yan SF, Stern DM. The multiligand receptor RAGE as a progression factor amplifying immune and inflammatory responses. J Clin Invest 2001; 108(7): 949-55.
[http://dx.doi.org/10.1172/JCI200114002] [PMID: 11581294]
[122]
Cho H, Son S, Jin S, Hong H, Shin D, Kim S, et al. RAGE regulates BACE1 and Aβ generation via NFAT1 activation in Alzheimer's dis-ease animal model 2009; 23(8): 2639-49.
[123]
Salminen A, Kaarniranta K, Haapasalo A, Soininen H. AMP‐activated protein kinase: a potential player in Alzheimer’s disease 2011; 118(4): 460-74.
[124]
Son SM, Jung ES, Shin HJ, Byun J. Aβ-induced formation of autophagosomes is mediated by RAGE-CaMKKβ-AMPK signaling 2012; 33(5): 1006. e11.
[125]
Li XH, Lv BL, Xie JZ, Liu J, Zhou XW. AGEs induce Alzheimer-like tau pathology and memory deficit via RAGE-mediated GSK-3 activation 2012; 33(7): 1400-0.
[126]
Webster B, Hansen L, Adame A, Crews L, Torrance M, Thal L, et al. Astroglial activation of extracellular-regulated kinase in early stages of Alzheimer disease 2006; 65(2): 42-51.
[http://dx.doi.org/10.1097/01.jnen.0000199599.63204.6f]
[127]
Han YT, Choi GI, Son D, et al. Ligand-based design, synthesis, and biological evaluation of 2-aminopyrimidines, a novel series of re-ceptor for advanced glycation end products (RAGE) inhibitors. J Med Chem 2012; 55(21): 9120-35.
[128]
Han YT, Kim K, Choi GI, et al. Pyrazole-5-carboxamides, novel inhibitors of receptor for advanced glycation end products (RAGE). Eur J Med Chem 2014; 79: 128-42.
[129]
Choi K, Lim KS, Shin J, et al. 6-Phenoxy-2-phenylbenzoxazoles, novel inhibitors of receptor for advanced glycation end products (RAGE). Bioorg Med Chem 2015; 23(15): 4919-35.
[130]
Herbert J, Augereau J, Gleye J, Maffrand JJB. Chelerythrine is a potent and specific inhibitor of protein kinase C. Biochem Biophys Res Commun 1990; 172(3): 993.
[131]
Koppaka V, Thompson DC, Chen Y, Ellermann M, Nicolaou KC, Juvonen RO, et al. Aldehyde dehydrogenase inhibitors: a comprehen-sive review of the pharmacology, mechanism of action, substrate specificity, and clinical application. Pharmacol Rev 2012; 64(3): 520-39.
[http://dx.doi.org/10.1124/pr.111.005538]
[132]
Palanski BA, Khosla CJB. Cystamine and disulfiram inhibit human transglutaminase 2 via an oxidative mechanism. Biochemistry 2018; 57(24): 3359-63.
[http://dx.doi.org/10.1021/acs.biochem.8b00204]
[133]
Cirillo C, Capoccia E, Iuvone T, et al. S100B inhibitor pentamidine attenuates reactive gliosis and reduces neuronal loss in a mouse model of Alzheimer’s Disease. BioMed Res Int 2015; 2015: 1-11.
[http://dx.doi.org/10.1155/2015/508342] [PMID: 26295040]
[134]
Agamennone M, Cesari L, Lalli D, et al. Fragmenting the S100B-p53 interaction: combined virtual/biophysical screening approaches to identify ligands. ChemMedChem 2010; 5(3): 428-35.
[http://dx.doi.org/10.1002/cmdc.200900393] [PMID: 20077460]
[135]
Cavalier MC, Pierce AD, Wilder PT, Alasady MJ, Hartman KG, Neau DB, et al. Covalent small molecule inhibitors of ca2+-bound s100b. Biochemistry 2014; 53(42): 6628-40.
[136]
Rani SG, Mohan SK, Yu CJB. Molecular level interactions of S100A13 with amlexanox: inhibitor for formation of the multiprotein com-plex in the nonclassical pathway of acidic fibroblast growth factor. Biochemistry 2010; 49(11): 2585-92.
[http://dx.doi.org/10.1021/bi9019077]
[137]
Wilder PT, Charpentier TH, Liriano MA, Gianni K, Varney KM, Pozharski E, et al. In vitro screening and structural characterization of inhibitors of the S100B-p53 interaction. Int J High Throughput Screen 2010; 2010(1): 109.
[138]
Charpentier TH, Wilder PT, Liriano MA, et al. Divalent metal ion complexes of S100B in the absence and presence of pentamidine. J Molecul Biol 2008; 382(1): 56-73.
[http://dx.doi.org/10.1016/j.jmb.2008.06.047]
[139]
Süssmuth SD, Tumani H, Ecker D, Ludolph AC. Amyotrophic lateral sclerosis: disease stage related changes of tau protein and S100 beta in cerebrospinal fluid and creatine kinase in serum. Neurosci Lett 2003; 353(1): 57-60.
[http://dx.doi.org/10.1016/j.neulet.2003.09.018] [PMID: 14642437]
[140]
Chen L, Hu X, Wu H, et al. Over-expression of S100B protein as a serum marker of brain metastasis in non-small cell lung cancer and its prognostic value. Pathol Res Pract 2019; 215(3): 427-32.
[http://dx.doi.org/10.1016/j.prp.2018.11.011] [PMID: 30455129]
[141]
Wright NT, Cannon BR, Zimmer DB, Weber DJ. S100A1: Structure, Function, and Therapeutic Potential. Curr Chem Biol 2009; 3(2): 138-45.
[PMID: 19890475]
[142]
Tian ZY, Wang CY, Wang T, Li YC, Wang ZY. Glial S100A6 Degrades β-amyloid aggregation through targeting competition with zinc ions. Aging Dis 2019; 10(4): 756-69.
[http://dx.doi.org/10.14336/AD.2018.0912] [PMID: 31440382]
[143]
Masters SL, O’Neill LAJ. Disease-associated amyloid and misfolded protein aggregates activate the inflammasome. Trends Mol Med 2011; 17(5): 276-82.
[http://dx.doi.org/10.1016/j.molmed.2011.01.005] [PMID: 21376667]
[144]
Wasik U, Schneider G, Mietelska-Porowska A, et al. Calcyclin binding protein and Siah-1 interacting protein in Alzheimer’s disease pathology: neuronal localization and possible function. Neurobiol Aging 2013; 34(5): 1380-8.
[http://dx.doi.org/10.1016/j.neurobiolaging.2012.11.007] [PMID: 23260124]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy