Advertisement

The Advances of Nanozyme in Brain Disease

  • Ruofei Zhang
  • Xiyun YanEmail author
  • Kelong FanEmail author
Chapter

Abstract

Reactive oxygen species (ROS), a class of metabolites produced in biological aerobic metabolism, play a key role in conducting cellular signals and maintaining normal nerve functions in central nerve system. However, under some pathological conditions, oxidative stress caused by excessive ROS may become an important factor in the occurrence and deterioration of neurological disease. Therefore, it is crucial to control the level of ROS in the central nervous system in time. Traditional ROS regulators, such as some natural enzymes and assemblies based on them, have not been well applied in brain diseases due to their instability and limited ability to cross the blood–brain barrier (BBB). Nanozymes, stable inorganic nanomaterials that possess intrinsic enzyme-mimic activities, have attracted wide attention in the scientific community in recent years attributed to their efficient ability to alleviate oxidative stress in the central nervous system. This chapter reviews the advances in the application of nanozymes in the treatment of neurological diseases and discusses the challenges and perspectives of nanozymes for their clinical translations. We hope that this chapter will arouse readers’ interest in nanozymes and promote the research and application of nanozymes in brain diseases.

Keywords

Nanozyme Central nervous system disease Neurological disorders Antioxidative therapy 

Notes

Acknowledgments

This work was financially supported by the National Natural Science Foundation of China (No. 31530026, 31871005, 31900981), Chinese Academy of Sciences under Grant No. YJKYYQ20180048, Youth Innovation Promotion Association CAS (2019093), Strategic Priority Research Program (No. XDB29040101), Key Research Program of Frontier Sciences (No. QYZDY-SSW-SMC013), Chinese Academy of Sciences, National Key Research and Development Program of China (No. 2017YFA0205501).

References

  1. 1.
    Hsieh HL, Yang CM. Role of redox signaling in neuroinflammation and neurodegenerative diseases. Biomed Res Int. 2013;2013:484–613.Google Scholar
  2. 2.
    Patel M. Targeting oxidative stress in central nervous system disorders. Trends Pharmacol Sci. 2016;37(9):768–78.PubMedPubMedCentralCrossRefGoogle Scholar
  3. 3.
    Jones DP. Redefining oxidative stress. Antioxid Redox Sign. 2006;8(9–10):1865–79.CrossRefGoogle Scholar
  4. 4.
    Chovatiya R, Medzhitov R. Stress, inflammation, and defense of homeostasis. Mol Cell. 2014;54(2):281–8.PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Jan AT, Azam M, Siddiqui K, Ali A, Choi I, Haq QMR. Heavy metals and human health: mechanistic insight into toxicity and counter defense system of antioxidants. Int J Mol Sci. 2015;16(12):29592–630.PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Murphy MP. How mitochondria produce reactive oxygen species. Biochem J. 2009;417(1):1–13.PubMedCrossRefGoogle Scholar
  7. 7.
    Gao L, Zhuang J, Nie L, Zhang J, Zhang Y, Gu N, Wang T, Feng J, Yang D, Perrett S. Intrinsic peroxidase-like activity of ferromagnetic nanoparticles. Nat Nanotechnol. 2007;2(9):577–83.PubMedCrossRefGoogle Scholar
  8. 8.
    Wei H, Wang E. Nanomaterials with enzyme-like characteristics (nanozymes): next-generation artificial enzymes. Chem Soc Rev. 2013;42(14):6060–93.PubMedCrossRefGoogle Scholar
  9. 9.
    Day BJ. Catalytic antioxidants: a radical approach to new therapeutics. Drug Discov Today. 2004;9(13):557–66.PubMedCrossRefGoogle Scholar
  10. 10.
    Shin HY, Park TJ, Kim MI. Recent research trends and future prospects in nanozymes. J Nanomater. 2015;2015:1–11.Google Scholar
  11. 11.
    Ragg R, Tahir MN, Tremel W. Solids go bio: inorganic nanoparticles as enzyme mimics. Eur J Inorg Chem. 2016;2016(13–14):1906–15.CrossRefGoogle Scholar
  12. 12.
    Loschen G, Flohe L, Chance B. Respiratory chain linked H2O2 production in pigeon heart mitochondria. FEBS Lett. 1971;18(2):261–4.PubMedCrossRefPubMedCentralGoogle Scholar
  13. 13.
    Loschen G, Azzi A, Richter C, Flohé L. Superoxide radicals as precursors of mitochondrial hydrogen peroxide. FEBS Lett. 1974;42(1):68–72.PubMedCrossRefPubMedCentralGoogle Scholar
  14. 14.
    Weisiger RA, Fridovich I. Superoxide dismutase. Organelle specificity. J Biol Chem. 1973;248(10):3582–92.PubMedPubMedCentralGoogle Scholar
  15. 15.
    Turrens JF. Mitochondrial formation of reactive oxygen species. J Physiol. 2010;552(2):335–44.CrossRefGoogle Scholar
  16. 16.
    Silvia S, Karl-Heinz K. NOX enzymes in the central nervous system: from signaling to disease. Antioxid Redox Sign. 2009;11(10):2481–504.CrossRefGoogle Scholar
  17. 17.
    Bedard K, Krause KH. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev. 2007;87(1):245–313.PubMedCrossRefPubMedCentralGoogle Scholar
  18. 18.
    B H. Reactive oxygen species and the central nervous system. J Neurochem. 1992;59(5):1609–23.CrossRefGoogle Scholar
  19. 19.
    Urrutia PJ, Mena NP, Nunez MT. The interplay between iron accumulation, mitochondrial dysfunction, and inflammation during the execution step of neurodegenerative disorders. Front Pharmacol. 2014;5(38):38.PubMedPubMedCentralGoogle Scholar
  20. 20.
    Ortiz GG, Pacheco Moises FP, Mireles-Ramirez M, Flores-Alvarado LJ, Gonzalez-Usigli H, Sanchez-Gonzalez VJ, Sanchez-Lopez AL, Sanchez-Romero L, Diaz-Barba EI, Santoscoy-Gutierrez JF, Rivero-Moragrega P. Oxidative stress: love and hate history in central nervous system. Adv Protein Chem Struct Biol. 2017;108:1–31.PubMedCrossRefPubMedCentralGoogle Scholar
  21. 21.
    Batrakova EV, Li S, Reynolds AD, Mosley RL, Bronich TK, Kabanov AV, Gendelman HE. A macrophage-nanozyme delivery system for Parkinson’s disease. Bioconjug Chem. 2007;18(5):1498–506.PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Brynskikh AM, Zhao Y, Mosley RL, Li S, Boska MD, Klyachko NL, Kabanov AV, Gendelman HE, Batrakova EV. Macrophage delivery of therapeutic nanozymes in a murine model of Parkinson’s disease. Nanomedicine. 2010;5(3):379–96.PubMedCrossRefPubMedCentralGoogle Scholar
  23. 23.
    Rosenbaugh EG, Manickam DS, Batrakova EV, Kabanov AV, Zimmerman MC. Nanoformulated copper/zinc superoxide dismutase increases neuronal uptake via active endocytosis. Free Radical Bio Med. 2010;49:S195–6.CrossRefGoogle Scholar
  24. 24.
    Haney MJ, Zhao Y, Li S, Higginbotham SM, Booth SL, Han H-Y, Vetro JA, Mosley RL, Kabanov AV, Gendelman HE, Batrakova EV. Cell-mediated transfer of catalase nanoparticles from macrophages to brain endothelial, glial and neuronal cells. Nanomedicine. 2011;6(7):1215–30.PubMedCrossRefPubMedCentralGoogle Scholar
  25. 25.
    Zhao Y, Haney MJ, Mahajan V, Reiner BC, Dunaevsky A, Mosley RL, Kabanov AV, Gendelman HE, Batrakova EV. Active targeted macrophage-mediated delivery of catalase to affected brain regions in models of Parkinson’s disease. J Nanomed Nanotechnol. 2011;S4(1):003Google Scholar
  26. 26.
    Manickam DS, Brynskikh AM, Kopanic JL, Sorgen PL, Klyachko NL, Batrakova EV, Bronich TK, Kabanov AV. Well-defined cross-linked antioxidant nanozymes for treatment of ischemic brain injury. J Control Release. 2012;162(3):636–45.PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Jiang Y, Brynskikh AM, S-Manickam D, Kabanov AV. SOD1 nanozyme salvages ischemic brain by locally protecting cerebral vasculature. J Control Release. 2015;213:36–44.PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Lin Y, Ren J, Qu X. Catalytically active nanomaterials: a promising candidate for artificial enzymes. Acc Chem Res. 2014;47(4):1097–105.PubMedCrossRefPubMedCentralGoogle Scholar
  29. 29.
    Guan Y, Li M, Dong K, Gao N, Ren J, Zheng Y, Qu X. Ceria/POMs hybrid nanoparticles as a mimicking metallopeptidase for treatment of neurotoxicity of amyloid-beta peptide. Biomaterials. 2016;98:92–102.PubMedCrossRefPubMedCentralGoogle Scholar
  30. 30.
    Zelko IN, Mariani TJ, Folz RJ. Superoxide dismutase multigene family: a comparison of the CuZn-SOD (SOD1), Mn-SOD (SOD2), and EC-SOD (SOD3) gene structures, evolution, and expression. Free Radic Biol Med. 2002;33(3):337–49.PubMedCrossRefGoogle Scholar
  31. 31.
    McCord JM, Fridovich I. Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J Biol Chem. 1969;244(22):6049–55.PubMedGoogle Scholar
  32. 32.
    Boaro M, Giordano F, Recchia S, Santo VD, Giona M, Trovarelli A. On the mechanism of fast oxygen storage and release in ceria-zirconia model catalysts. Appl Catal B Environ. 2004;52(3):225–37.CrossRefGoogle Scholar
  33. 33.
    Trovarelli A, Leitenburg CD, Boaro M, Dolcetti G. The utilization of ceria in industrial catalysis. Catal Today. 1999;50(2):353–67.CrossRefGoogle Scholar
  34. 34.
    Korsvik C, Patil S, Seal S, Self WT. Superoxide dismutase mimetic properties exhibited by vacancy engineered ceria nanoparticles. Chem Commun (Camb). 2007;(10):1056–8.Google Scholar
  35. 35.
    Deshpande S, Patil S, Kuchibhatla SV, Seal S. Size dependency variation in lattice parameter and valency states in nanocrystalline cerium oxide. Appl Phys Lett. 2005;87(13):223–78.CrossRefGoogle Scholar
  36. 36.
    Ying JY, Tschöpe A. Synthesis and characteristics of non-stoichiometric nanocrystalline cerium oxide-based catalysts. Chem Eng J Biochem Eng J. 1996;64(2):225–37.CrossRefGoogle Scholar
  37. 37.
    Celardo I, Pedersen JZ, Traversa E, Ghibelli L. Pharmacological potential of cerium oxide nanoparticles. Nanoscale. 2011;3(4):1411.PubMedCrossRefGoogle Scholar
  38. 38.
    Krusic PJ, Wasserman E, Keizer PN, Morton JR, Preston KF. Radical reactions of C60. Science. 1991;254(5035):1183–5.PubMedCrossRefPubMedCentralGoogle Scholar
  39. 39.
    Lotharius J, Dugan LL, O’Malley KL. Distinct mechanisms underlie neurotoxin-mediated cell death in cultured dopaminergic neurons. J Neurosci. 1999;19(4):1284–93.PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Lin AM, Chyi BY, Wang SD, Yu HH, Kanakamma PP, Luh TY, Chou CK, Ho LT. Carboxyfullerene prevents iron-induced oxidative stress in rat brain. J Neurochem. 2010;72(4):1634–40.CrossRefGoogle Scholar
  41. 41.
    Dugan LL, Lovett EG, Quick KL, Lotharius J, Lin TT, O’Malley KL. Fullerene-based antioxidants and neurodegenerative disorders. Parkinsonism Relat Disord. 2001;7(3):243–6.PubMedPubMedCentralCrossRefGoogle Scholar
  42. 42.
    Dugan LL, Turetsky DM, Du C, Lobner D, Wheeler M, Almli CR, Shen KF, Luh TY, Choi DW, Lin TS. Carboxyfullerenes as neuroprotective agents. P Natl Acad Sci USA. 1997;94(17):9434–9.CrossRefGoogle Scholar
  43. 43.
    Huang SS, Tsai SK, Chih CL, Chiang L-Y, Hsieh HM, Teng CM, Tsai MC. Neuroprotective effect of hexasulfobutylated C60 on rats subjected to focal cerebral ischemia. Free Radical Bio Med. 2001;30(6):643–9.CrossRefGoogle Scholar
  44. 44.
    Kroto H, Allaf AW, Balm S. C60: Buckminsterfullerene. Chem Rev. 1991;91(6):1213–35.CrossRefGoogle Scholar
  45. 45.
    Dugan LL, Gabrielsen JK, Yu SP, Lin TS, Choi DW. Buckminsterfullerenol free radical scavengers reduce excitotoxic and apoptotic death of cultured cortical neurons. Neurobiol Dis. 1996;3(2):129–35.PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Dugan LL, Turetsky DM, Du C, Lobner D, Wheeler M, Almli CR, Shen CK, Luh TY, Choi DW, Lin TS. Carboxyfullerenes as neuroprotective agents. P Natl Acad Sci USA. 1997;94(17):9434–9.CrossRefGoogle Scholar
  47. 47.
    Bensasson RV, Brettreich M, Frederiksen J, Göttinger H, Hirsch A, Land EJ, Leach S, Mcgarvey DJ, Schönberger H. Reactions of e−aq, CO2 •−, HO, O2 •− and O2(1δg) with a dendro[60]fullerene and C60[C(COOH)2]n (n = 2–6). Free Radical Bio Med. 2000;29(1):26–33.CrossRefGoogle Scholar
  48. 48.
    Okuda K, Hirota T, Hirobe M, Nagano T, Mochizuki M, Mashino T. Synthesis of various water-soluble C60 derivatives and their superoxide-quenching activity. Fuller Sci Technol. 2000;8(1–2):89–104.CrossRefGoogle Scholar
  49. 49.
    Ali SS, Hardt JI, Quick KL, Kim-Han JS, Erlanger BF, Huang TT, Epstein CJ, Dugan LL. A biologically effective fullerene (C60) derivative with superoxide dismutase mimetic properties. Free Radic Biol Med. 2004;37(8):1191–202.PubMedCrossRefGoogle Scholar
  50. 50.
    Ali SS, Hardt JI, Dugan LL. SOD activity of carboxyfullerenes predicts their neuroprotective efficacy: a structure-activity study. Nanomed Nanotechnol. 2008;4(4):283–94.CrossRefGoogle Scholar
  51. 51.
    Belgorodsky B, Fadeev L, Ittah V, Benyamini H, Zelner S. Formation and characterization of stable human serum albumin-tris-malonic acid [C60] fullerene complex. Bioconjug Chem. 2005;16(5):1058–62.PubMedCrossRefGoogle Scholar
  52. 52.
    Errol LGS, Daniela CM, Vladimir B, Brittany RB, Gang W, Austin P, Roderic HF, Robia GP, Thomas AK, Ah-Lim T. Highly efficient conversion of superoxide to oxygen using hydrophilic carbon clusters. P Natl Acad Sci USA. 2015;112(8):2343–8.CrossRefGoogle Scholar
  53. 53.
    Kajita M, Hikosaka K, Iitsuka M, Kanayama A, Toshima N, Miyamoto Y. Platinum nanoparticle is a useful scavenger of superoxide anion and hydrogen peroxide. Free Radic Res. 2007;41(6):615.PubMedCrossRefGoogle Scholar
  54. 54.
    Hamasaki T, Kashiwagi T, Imada T, Nakamichi N, Aramaki S, Toh K, Morisawa S, Shimakoshi H, Hisaeda Y, Shirahata S. Kinetic analysis of superoxide anion radical-scavenging and hydroxyl radical-scavenging activities of platinum nanoparticles. Langmuir. 2008;24(14):7354–64.PubMedCrossRefGoogle Scholar
  55. 55.
    Lianbing Z, Linda L, Wolfram M, Eckhard P, Ulrich GS, Matthias B, Mato K. Reducing stress on cells with apoferritin-encapsulated platinum nanoparticles. Nano Lett. 2010;10(1):219–23.CrossRefGoogle Scholar
  56. 56.
    Clark A, Zhu A, Kai S, Petty HR. Cerium oxide and platinum nanoparticles protect cells from oxidant-mediated apoptosis. J Nanoparti Res. 2011;13(10):5547–55.CrossRefGoogle Scholar
  57. 57.
    Deisseroth A, Dounce AL. Catalase: physical and chemical properties, mechanism of catalysis, and physiological role. Physiol Rev. 1970;50(3):319–75.PubMedCrossRefGoogle Scholar
  58. 58.
    Sumner JB. The chemical nature of catalase. Adv Enzymol Relat Areas Mol Biol. Wiley. 2006, 163–176.Google Scholar
  59. 59.
    Pirmohamed T, Dowding JM, Singh S, Wasserman B, Heckert E, Karakoti AS, King JE, Seal S, Self WT. Nanoceria exhibit redox state-dependent catalase mimetic activity. Chem Commun (Camb). 2010;46(16):2736–8.CrossRefGoogle Scholar
  60. 60.
    Ivanov VK, Shcherbakov AB, Usatenko AV. Structure-sensitive properties and biomedical applications of nanodispersed cerium dioxide. ChemInform. 2010;41(9)Google Scholar
  61. 61.
    Nelson BC, Johnson ME, Walker ML, Riley KR, Sims CM. Antioxidant cerium oxide nanoparticles in biology and medicine. Antioxidants (Basel). 2016;5(2):E5.Google Scholar
  62. 62.
    Chen Z, Yin JJ, Zhou YT, Zhang Y, Song L, Song M, Hu S, Gu N. Dual enzyme-like activities of iron oxide nanoparticles and their implication for diminishing cytotoxicity. ACS Nano. 2012;6(5):4001–12.PubMedCrossRefGoogle Scholar
  63. 63.
    Jianshuai M, Yan W, Min Z, Li Z. Intrinsic peroxidase-like activity and catalase-like activity of Co3O4 nanoparticles. Chem Commun (Camb). 2012;48(19):2540–2.CrossRefGoogle Scholar
  64. 64.
    Jia F, Jun-Jie Y, Bo N, Xiaochun W, Ye H, Mauro F, Anderson GJ, Jingyan W, Yuliang Z, Guangjun N. Direct evidence for catalase and peroxidase activities of ferritin-platinum nanoparticles. Biomaterials. 2011;32(6):1611–8.CrossRefGoogle Scholar
  65. 65.
    Singh N, Savanur MA, Srivastava S, D’Silva P, Mugesh G. A redox modulatory Mn3O4 nanozyme with multi-enzyme activity provides efficient cytoprotection to human cells in a Parkinson’s disease model. Angew Chem Int Edit. 2017;56(45):14267.CrossRefGoogle Scholar
  66. 66.
    Gao L, Yan X. Nanozymes: an emerging field bridging nanotechnology and biology. Sci China Life Sci. 2016;59(4):400–2.PubMedCrossRefGoogle Scholar
  67. 67.
    Wang X, Hu Y, Wei H. Nanozymes in bionanotechnology: from sensing to therapeutics and beyond. Inorg Chem Front. 2016;3(1):41–60.CrossRefGoogle Scholar
  68. 68.
    Sabens Liedhegner EA, Gao XH, Mieyal JJ. Mechanisms of altered redox regulation in neurodegenerative diseases-focus on S-glutathionylation. Antioxid Redox Sign. 2012;16(6):543–66.CrossRefGoogle Scholar
  69. 69.
    Jin H, Chen WQ, Tang XW, Chiang LY, Yang CY, Schloss JV, Wu JY. Polyhydroxylated C60, fullerenols, as glutamate receptor antagonists and neuroprotective agents. J Neurosci Res. 2015;62(4):600–7.CrossRefGoogle Scholar
  70. 70.
    Chen T, Li YY, Zhang JL, Xu B, Lin Y, Wang CX, Guan WC, Wang YJ, Xu SQ. Protective effect of C60 -methionine derivate on lead-exposed human SH-SY5Y neuroblastoma cells. J Appl Toxicol. 2011;31(3):255–61.PubMedCrossRefGoogle Scholar
  71. 71.
    Ren C, Hu X, Zhou Q. Graphene oxide quantum dots reduce oxidative stress and inhibit neurotoxicity in vitro and in vivo through catalase-like activity and metabolic regulation. Adv Sci. 2018;5(5):1700595.CrossRefGoogle Scholar
  72. 72.
    Das M, Patil S, Bhargava N, Kang JF, Riedel LM, Seal S, Hickman JJ. Auto-catalytic ceria nanoparticles offer neuroprotection to adult rat spinal cord neurons. Biomaterials. 2007;28(10):1918–25.PubMedPubMedCentralCrossRefGoogle Scholar
  73. 73.
    Schubert D, Dargusch R, Raitano J, Chan SW. Cerium and yttrium oxide nanoparticles are neuroprotective. Biochem Biophys Res Commun. 2006;342(1):86–91.PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Zeng F, Wu Y, Li X, Ge X, Guo Q, Lou X, Cao Z, Hu B, Long NJ, Mao Y, Li C. Custom-made ceria nanoparticles show a neuroprotective effect by modulating phenotypic polarization of the microglia. Angew Chem Int Edit. 2018;57(20):5808–12.CrossRefGoogle Scholar
  75. 75.
    Ferreira R, Bernardino L. Dual role of microglia in health and disease: pushing the balance toward repair. Front Cell Neurosci. 2015;9:51.PubMedPubMedCentralGoogle Scholar
  76. 76.
    Suenaga J, Hu X, Pu H, Shi Y, Hassan SH, Xu M, Leak RK, Stetler RA, Gao Y, Chen J. White matter injury and microglia/macrophage polarization are strongly linked with age-related long-term deficits in neurological function after stroke. Exp Neurol. 2015;272:109–19.PubMedPubMedCentralCrossRefGoogle Scholar
  77. 77.
    Palwinder KM, Aiste J, Guy CB. Microglia proliferation is regulated by hydrogen peroxide from NADPH oxidase. J Immunol. 2006;176(2):1046–52.CrossRefGoogle Scholar
  78. 78.
    Zhang B, Bailey WM, Mcvicar AL, Gensel JC. Age increases reactive oxygen species production in macrophages and potentiates oxidative damage after spinal cord injury. Neurobiol Aging. 2016;47:157–67.PubMedPubMedCentralCrossRefGoogle Scholar
  79. 79.
    Orihuela R, Mcpherson CA, Harry GJ. Microglial M1/M2 polarization and metabolic states. Brit J Pharmacol. 2016;173(4):649–65.CrossRefGoogle Scholar
  80. 80.
    Wang T, Zhang X, Li JJ. The role of NF-κB in the regulation of cell stress responses. Int Immunopharmacol. 2002;2(11):1509–20.PubMedCrossRefPubMedCentralGoogle Scholar
  81. 81.
    Zhang J, Johnston G, Stebler B, Keller ET. Hydrogen peroxide activates NF-κB and the interleukin-6 promoter through NF-κB-inducing kinase. Antioxid Redox Sign. 2001;3(3):493.CrossRefGoogle Scholar
  82. 82.
    Leuner K, Reichert AS. From mitochondrial dysfunction to amyloid beta formation: novel insights into the pathogenesis of Alzheimer’s disease. Mol Neurobiol. 2012;46(1):186–93.PubMedCrossRefPubMedCentralGoogle Scholar
  83. 83.
    Verri M, Pastoris O, Dossena M, Aquilani R, Guerriero F, Cuzzoni G, Venturini L, Ricevuti G, Bongiorno AI. Mitochondrial alterations, oxidative stress and neuroinflammation in Alzheimer’s disease. Int J Immunopathol Pharmacol. 2012;25(2):345–53.PubMedCrossRefPubMedCentralGoogle Scholar
  84. 84.
    Parisa Y, Ali Y. Advanced glycation end-products and their receptor-mediated roles: inflammation and oxidative stress. Iran J Basic Med Sci. 2011;36(3):154–66.Google Scholar
  85. 85.
    Bornemann KD, Wiederhold KH, Pauli C, Ermini F, Stalder M, Schnell L, Sommer B, Jucker M, Staufenbiel M. A beta-induced inflammatory processes in microglia cells of APP23 transgenic mice. Am J Pathol. 2001;158(1):63–73.PubMedPubMedCentralCrossRefGoogle Scholar
  86. 86.
    Kitazawa M, Yamasaki TR, LaFerla FM. Microglia as a potential bridge between the amyloid beta-peptide and tau. Ann N Y Acad Sci. 2004;1035:85–103.PubMedCrossRefPubMedCentralGoogle Scholar
  87. 87.
    Chay KO, Koong KYN, Hwang S, Kim JK, Bae CS. NADPH oxidase mediates β-amyloid peptide-induced neuronal death in mouse cortical cultures. Chonnam Med J. 2017;53(3):196–202.PubMedPubMedCentralCrossRefGoogle Scholar
  88. 88.
    Wei Z, Wang LZ, Yu JT, Chi ZF, Lan T. Increased expressions of TLR2 and TLR4 on peripheral blood mononuclear cells from patients with Alzheimer’s disease. J Neurol Sci. 2012;315(1–2):67–71.Google Scholar
  89. 89.
    Sung-Chun T, Lathia JD, Selvaraj PK, Dong-Gyu J, Mughal MR, Aiwu C, Siler DA, Markesbery WR, Arumugam TV, Mattson MP. Toll-like receptor-4 mediates neuronal apoptosis induced by amyloid beta-peptide and the membrane lipid peroxidation product 4-hydroxynonenal. Exp Neurol. 2008;213(1):114–21.CrossRefGoogle Scholar
  90. 90.
    Jeong Eun K, Minyung L. Fullerene inhibits beta-amyloid peptide aggregation. Biochem Bioph Res Commun. 2003;303(2):576–9.CrossRefGoogle Scholar
  91. 91.
    Luogang X, Yin L, Dongdong L, Wenhui X, Xinju Y, Guanghong W. The molecular mechanism of fullerene-inhibited aggregation of Alzheimer’s β-amyloid peptide fragment. Nanoscale. 2014;6(16):9752–62.CrossRefGoogle Scholar
  92. 92.
    D’Angelo B, Santucci S, Benedetti E, Loreto SD, Phani RA, Falone S, Amicarelli F, Cerù MP, Cimini A. Cerium oxide nanoparticles trigger neuronal survival in a human Alzheimer disease model by modulating BDNF pathway. Curr Nanosci. 2009;5(2):167–76.CrossRefGoogle Scholar
  93. 93.
    Cimini A, D’Angelo B, Das S, Gentile R, Benedetti E, Singh V, Monaco AM, Santucci S, Seal S. Antibody-conjugated PEGylated cerium oxide nanoparticles for specific targeting of Aβ aggregates modulate neuronal survival pathways. Acta Biomater. 2012;8(6):2056–67.PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    Kwon HJ, Cha MY, Kim D, Kim DK, Soh M, Shin K, Hyeon T, Mook-Jung I. Mitochondria-targeting ceria nanoparticles as antioxidants for Alzheimer’s disease. ACS Nano. 2016;10(2):2860–70.PubMedPubMedCentralCrossRefGoogle Scholar
  95. 95.
    Du H, Guo L, Yan S, Sosunov AA, McKhann GM, Yan SS. Early deficits in synaptic mitochondria in an Alzheimer’s disease mouse model. P Natl Acad Sci USA. 2010;107(43):18670–5.CrossRefGoogle Scholar
  96. 96.
    Misono M. Unique acid catalysis of heteropoly compounds (heteropolyoxometalates) in the solid state. Chem Commun (Camb). 2001;13(13):1141–52.CrossRefGoogle Scholar
  97. 97.
    Izarova NV, Pope MT, Kortz U. Noble metals in polyoxometalates. Angew Chem Int Edit. 2012;51(38):9492–510.CrossRefGoogle Scholar
  98. 98.
    Jie G, Meng L, Jinsong R, Enbo W, Xiaogang Q. Polyoxometalates as inhibitors of the aggregation of amyloid β peptides associated with Alzheimer’s disease. Angew Chem Int Edit. 2011;50(18):4184–8.CrossRefGoogle Scholar
  99. 99.
    Gao N, Sun H, Dong K, Ren J, Duan T, Xu C, Qu X. Transition-metal-substituted polyoxometalate derivatives as functional anti-amyloid agents for Alzheimer’s disease. Nat Commun. 2014;5:3422.PubMedCrossRefPubMedCentralGoogle Scholar
  100. 100.
    Dong A, Zhao H, Ying W, Jinsong X. Polyoxometalate-based nanozyme: design of a multifunctional enzyme for multi-faceted treatment of Alzheimer’s disease. Nano Res. 2016;9(4):1079–90.CrossRefGoogle Scholar
  101. 101.
    Geng J, Li M, Wu L, Ren J, Qu X. Liberation of copper from amyloid plaques: making a risk factor useful for Alzheimer’s disease treatment. J Med Chem. 2012;55(21):9146.PubMedCrossRefPubMedCentralGoogle Scholar
  102. 102.
    Zhang Y, Wang Z, Li X, Wang L, Yin M, Wang L, Chen N, Fan C, Song H. Dietary iron oxide nanoparticles delay aging and ameliorate neurodegeneration in Drosophila. Adv Mater. 2016;28(7):1387–93.PubMedCrossRefPubMedCentralGoogle Scholar
  103. 103.
    Lakhan SE, Kirchgessner A, Hofer M. Inflammatory mechanisms in ischemic stroke: therapeutic approaches. J Transl Med. 2009;7(1):97.PubMedPubMedCentralCrossRefGoogle Scholar
  104. 104.
    Pradillo JM, Fernández-López D, García-Yébenes I, Sobrado M, Hurtado O, Moro MA, Lizasoain I. Toll-like receptor 4 is involved in neuroprotection afforded by ischemic preconditioning. J Neurochem. 2010;109(1):287–94.CrossRefGoogle Scholar
  105. 105.
    Javier RC, Jesús MP, Olivia H, Pedro L, María AM, Ignacio L. Toll-like receptor 4 is involved in brain damage and inflammation after experimental stroke. Circulation. 2007;115(12):1599–608.CrossRefGoogle Scholar
  106. 106.
    Estevez AY, Pritchard S, Harper K, Aston JW, Lynch A, Lucky JJ, Ludington JS, Chatani P, Mosenthal WP, Leiter JC, Andreescu S, Erlichman JS. Neuroprotective mechanisms of cerium oxide nanoparticles in a mouse hippocampal brain slice model of ischemia. Free Radic Biol Med. 2011;51(6):1155–63.PubMedCrossRefPubMedCentralGoogle Scholar
  107. 107.
    Chi Kyung K, Taeho K, In-Young C, Min S, Dohoung K, Young-Ju K, Hyunduk J, Hye-Sung Y, Jun Yup K, Hong-Kyun P. Ceria nanoparticles that can protect against ischemic stroke. Angew Chem Int Edit. 2012;124(44):11334.CrossRefGoogle Scholar
  108. 108.
    Motonori T, Yusei M, Toru Y, Kentaro D, Yasuyuki O, Yoshio I, Tohru M, Koji A. Neurological and pathological improvements of cerebral infarction in mice with platinum nanoparticles. J Neurosci Res. 2011;89(7):1125–33.CrossRefGoogle Scholar
  109. 109.
    Takamiya M, Miyamoto Y, Yamashita T, Deguchi K, Ohta Y, Abe K. Strong neuroprotection with a novel platinum nanoparticle against ischemic stroke- and tissue plasminogen activator-related brain damages in mice. Neuroscience. 2012;221:47–55.PubMedCrossRefPubMedCentralGoogle Scholar
  110. 110.
    Fabian RH, Derry PJ, Rea HC, Dalmeida WV, Nilewski LG, Sikkema WKA, Mandava P, Tsai AL, Mendoza K, Berka V. Efficacy of novel carbon nanoparticle antioxidant therapy in a severe model of reversible middle cerebral artery stroke in acutely hyperglycemic rats. Front Neurol. 2018;9:199.PubMedPubMedCentralCrossRefGoogle Scholar
  111. 111.
    Bitner BR, Marcano DC, Berlin JM, Fabian RH, Leela C, Culver JC, Dickinson ME, Robertson CS, Pautler RG, Kent TA. Antioxidant carbon particles improve cerebrovascular dysfunction following traumatic brain injury. ACS Nano. 2012;6(9):8007–14.PubMedPubMedCentralCrossRefGoogle Scholar
  112. 112.
    Marcano DC, Bitner BR, Berlin JM, Jane J, Lee JM, Aakash J, Fabian RH, Kent TA, Tour JM. Design of poly(ethylene glycol)-functionalized hydrophilic carbon clusters for targeted therapy of cerebrovascular dysfunction in mild traumatic brain injury. J Neurotrauma. 2013;30(9):789–96.PubMedCrossRefGoogle Scholar
  113. 113.
    Olanow C. The pathogenesis of cell death in Parkinson’s disease–2007. Neurology. 2010;22(S17):S335–42.Google Scholar
  114. 114.
    Etienne CH, Stéphane H. Neuroinflammation in Parkinson’s disease: a target for neuroprotection? Lancet Neurol. 2009;8(4):382–97.CrossRefGoogle Scholar
  115. 115.
    Wu DC, Teismann P, Tieu K, Vila M, Jackson-Lewis V, Ischiropoulos H, Przedborski S. NADPH oxidase mediates oxidative stress in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine model of Parkinson’s disease. P Natl Acad Sci USA. 2003;100(10):6145–50.CrossRefGoogle Scholar
  116. 116.
    Pabon MM, Bachstetter AD, Hudson CE, Gemma C, Bickford PC. CX3CL1 reduces neurotoxicity and microglial activation in a rat model of Parkinson’s disease. J Neuroinflammation. 2011;8(1):1–7.CrossRefGoogle Scholar
  117. 117.
    Joglar B, Rey P, Guerra M, Labandeira-Garcia J. The inflammatory response in the MPTP model of Parkinson’s disease is mediated by brain angiotensin: relevance to progression of the disease. J Neurochem. 2010;109(2):656–69.CrossRefGoogle Scholar
  118. 118.
    Dexter DT, Wells FR, Lees AJ, Agid F, Agid Y, Jenner P, Marsden CD. Increased nigral iron content and alterations in other metal ions occurring in brain in Parkinson’s disease. J Neurochem. 1989;52(6):1830–6.PubMedCrossRefGoogle Scholar
  119. 119.
    Sofic E, Paulus W, Jellinger K, Riederer P, Youdim MB. Selective increase of iron in substantia nigra zona compacta of parkinsonian brains. J Neurochem. 1991;56(3):978–82.PubMedCrossRefGoogle Scholar
  120. 120.
    Lin AMY, Chyi BY, Wang SD, Yu HH, Kanakamma PP, Luh TY, Chou CK, Ho LT. Carboxyfullerene prevents iron-induced oxidative stress in rat brain. J Neurochem. 2010;72(4):1634–40.CrossRefGoogle Scholar
  121. 121.
    Drechsel DA, Estévez AG, Barbeito L, Beckman JS. Nitric oxide-mediated oxidative damage and the progressive demise of motor neurons in ALS. Neurotox Res. 2012;22(4):251–64.PubMedPubMedCentralCrossRefGoogle Scholar
  122. 122.
    Gonsette RE. Neurodegeneration in multiple sclerosis: the role of oxidative stress and excitotoxicity. J Neurol Sci. 2008;274(1):48–53.PubMedCrossRefPubMedCentralGoogle Scholar
  123. 123.
    Thomas Z, Alfonse P, Andreas Johann S, Christine S, Wolfgang B, Nicole SW. Molecular changes in white matter adjacent to an active demyelinating lesion in early multiple sclerosis. Brain Pathol. 2010;19(3):459–66.Google Scholar
  124. 124.
    Fischer MT, Rakhi S, Lim JL, Lukas H, Frischer JM, Joost D, Don M, Monika B, Jack VH, Hans L. NADPH oxidase expression in active multiple sclerosis lesions in relation to oxidative tissue damage and mitochondrial injury. Brain. 2012;135(3):886–99.PubMedPubMedCentralCrossRefGoogle Scholar
  125. 125.
    Heckman KL, Decoteau W, Estevez A, Reed KJ, Costanzo W, Sanford D, Leiter JC, Clauss J, Knapp K, Gomez C. Custom cerium oxide nanoparticles protect against a free radical mediated autoimmune degenerative disease in the brain. ACS Nano. 2013;7(12):10582–96.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  1. 1.CAS Engineering Laboratory for Nanozyme, Key Laboratory of Protein and Peptide PharmaceuticalInstitute of Biophysics, Chinese Academy of SciencesBeijingChina

Personalised recommendations