Anti-Aggregating Effect of the Naturally Occurring Dipeptide Carnosine on Aβ1-42 Fibril Formation

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Aloisi, Alessandra ^a   Barca, Amilcare ^b   Romano, Alessandro ^b   Guerrieri, Sara ^a,b,c   Storelli, Carlo ^b   Rinaldi, Rosaria ^a,b   Verri, Tiziano ^b  

^a CNR   (Italy)

^b UNIVERSITY OF SALENTO   (Italy)

^c ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN[1-42]; CARNOSINE; MONOMER; OLIGOMER; THIOFLAVINE;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL TISSUE; ANTIAGGREGATING ACTIVITY; ARTICLE; ATOMIC FORCE MICROSCOPY; COMPUTER MODEL; CONFORMATION; CONTROLLED STUDY; DRUG ACTIVITY; DRUG PROTEIN BINDING; ENZYME INHIBITION; FIBER; FIBRIL FORMATION; IN VITRO STUDY; MOLECULAR DOCKING; NONHUMAN; PATHOGENESIS; PROTEIN AGGREGATION; PROTEIN STRUCTURE;

AMYLOID; AMYLOID BETA-PEPTIDES; CARNOSINE; DOSE-RESPONSE RELATIONSHIP, DRUG; HUMANS; MODELS, MOLECULAR; MOLECULAR CONFORMATION; MOLECULAR DOCKING SIMULATION; PROTEIN BINDING; PROTEIN MULTIMERIZATION;

EID: 84879777967     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0068159     Document Type: Article

References (82)

1. Hipkiss AR, (2009) Carnosine and its possible roles in nutrition and health. Adv Food Nutr Res 57: 87-154.
2. Hoffmann AM, Bakardjiev A, Bauer K, (1996) Carnosine-synthesis in cultures of rat glial cells is restricted to oligodendrocytes and carnosine uptake to astrocytes. Neurosci Lett 215: 29-32.
3. De Marchis S, Melcangi RC, Modena C, Cavaretta I, Peretto P, et al. (1997) Identification of the glial cell types containing carnosine-related peptides in the rat brain. Neurosci Lett 237: 37-40.
4. Bakardjiev A, (1998) Carnosine and beta-alanine release is stimulated by glutamatergic receptors in cultured rat oligodendrocytes. Glia 24: 346-351.
5. Bakardjiev A, Bauer K, (2000) Biosynthesis, release, and uptake of carnosine in primary cultures. Biochemistry (Mosc) 65: 779-782.
6. De Marchis S, Modena C, Peretto P, Giffard C, Fasolo A, (2000) Carnosine-like immunoreactivity in the central nervous system of rats during postnatal development. J Comp Neurol 426: 378-390.
7. Yoshikawa T, Naito Y, Tanigawa T, Yoneta T, Kondo M, (1991) The antioxidant properties of a novel zinc-carnosine chelate compound, N-(3-aminopropionyl)-L-histidinato zinc. Biochim Biophys Acta 1115: 15-22.
8. Hobart LJ, Seibel I, Yeargans GS, Seidler NW, (2004) Anti-crosslinking properties of carnosine: significance of histidine. Life Sci 75: 1379-1389.
9. Guiotto A, Calderan, Ruzza P, Osler A, Rubini C, et al. (2005) Synthesis and evaluation of neuroprotective alpha,beta-unsaturated aldehyde scavenger histidyl-containing analogues of carnosine. Med Chem 48: 6156-6161.
10. Reddy VP, Garrett MR, Perry G, Smith MA, (2005) Carnosine: a versatile antioxidant and antiglycating agent. Sci Aging Knowledge Environ 18: pe12.
11. Hipkiss AR, (2009) Carnosine, diabetes and Alzheimer's disease. Expert Rev Neurother 9: 583-585.
12. Bellia F, Vecchio G, Rizzarelli E, (2012) Carnosine derivatives: new multifunctional drug-like molecules. Amino Acids 43: 153-163.
13. Kulebyakin K, Karpova L, Lakonsteva E, Krasavin M, Boldyrev A, (2012) Carnosine protects neurons against oxidative stress and modulates the time profile of MAPK cascade signaling. Amino acids 43: 91-96.
14. Preston JE, Hipkiss AR, Himsworth DT, Romero IA, Abbott JN, (1998) Toxic effects of beta-amyloid(25-35) on immortalised rat brain endothelial cell: protection by carnosine, homocarnosine and beta-alanine. Neurosci Lett 242: 105-108.
15. Herculano B, Tamura M, Ohba A, Shimatani M, Kutsuna N, et al. (2013) β-alanyl-L-histidine rescues cognitive deficits caused by feeding a high fat diet in a transgenic mouse model of Alzheimer's disease. J Alzheimers Dis 2013 33(4): 983-997.
16. Gallant S, Semyonova M, Yuneva M, (2000) Carnosine as a potential anti-senescence drug. Biochemistry (Mosc) 65: 866-868.
17. Hipkiss AR, (2009) On the enigma of carnosine's anti-ageing actions. Exp Gerontol 44: 237-242.
18. Boldyrev AA, Stvolinsky SL, Fedorova TN, Suslina ZA, (2010) Carnosine as a natural antioxidant and geroprotector: from molecular mechanisms to clinical trials. Rejuvenation Res 13: 156-158.
19. Koyama H, Konoha K, Sadakane Y, Ohkawara S, Kawahara M, (2011) Zinc neurotoxicity and the pathogenesis of vascular-type dementia: involvement of calcium dyshomeostasis and carnosine. J Clin Toxicol S3: 002.
20. Kawahara M, Konoha K, Nagata T, Sadakane Y, (2007) Protective substances against zinc-induced neuronal death after ischemia: carnosine as a target for drug of vascular type of dementia. Recent Pat CNS Drug Discov 2: 145-149.
21. Hipkiss AR, Preston JE, Himsworth DT, Worthington VC, Keown M, et al. (1998) Pluripotent protective effects of carnosine, a naturally occurring dipeptide. Ann. N. Y. Acad. Sci. 854, 37-53.
22. Junn E, Ronchetti RD, Quezado MM, Kim SY, Mouradian MM, (2003) Tissue transglutaminase-induced aggregation of alpha-synuclein: Implications for Lewy body formation in Parkinson's disease and dementia with Lewy bodies. Proc Natl Acad Sci U S A 100: 2047-2052.
23. Andringa G, Lam KY, Chegary M, Wang X, Chase TN, et al. (2004) Tissue transglutaminase catalyzes the formation of alpha-synuclein crosslinks in Parkinson's disease. FASEB J 8: 932-934.
24. Ohkawara T, Nishihira J, Nagashima R, Takeda H, Asaka M, (2006) Polaprezinc protects human colon cells from oxidative injury induced by hydrogen peroxide: relevant to cytoprotective heat shock proteins. World J Gastroenterol 12: 6178-6181.
25. Karpuj M, Steinman L, (2004) The multifaceted role of transglutaminase in neurodegeneration: review article. Amino Acids 26: 373-379.
26. Hipkiss AR, (2007) Could carnosine or related structures suppress Alzheimer's disease? J Alzheimers Dis 11: 229-240.
27. Hipkiss AR, (2011) Energy metabolism, proteotoxic stress and age-related dysfunction- protection by carnosine. Mol Aspects Med 32: 267-278.
28. Kawahara M, Koyama H, Nagata T, Sadakane Y, (2011) Zinc, copper, and carnosine attenuate neurotoxicity of prion fragment PrP106-126. Metallomics 3: 726-734.
29. Fernandez-Busquets X, Ponce J, Bravo R, Arimon M, Martianez T, et al. (2010) Modulation of amyloid beta peptide(1-42) cytotoxicity and aggregation in vitro by glucose and chondroitin sulfate. Curr Alzheimer Res 5: 428-438.
30. Yan H, Guo Y, Zhang J, Ding Z, Ha W, et al. (2008) Effect of carnosine, aminoguanidine, and aspirin drops on the prevention of cataracts in diabetic rats. Mol Vis 14: 2282-2291.
31. Attanasio F, Cataldo S, Fisichella S, Nicoletti S, Nicoletti VG, et al. (2009) Protective effects of L- and D-carnosine on alpha-crystallin amyloid fibril formation: implications for cataract disease. Biochemistry 48: 6522-6531.
32. Münch G, Mayer S, Michaelis J, Hipkiss AR, Riederer P, et al. (1997) Influence of advanced glycation end-products and AGE-inhibitors on nucleation-dependent polymerization of beta-amyloid peptide. Biochim Biophys Acta 1360: 17-29.
33. Fonteh AN, Harrington RJ, Tsai A, Liao P, Harrington MG, (2007) Free amino acid and dipeptide changes in the body fluids from Alzheimer's disease subjects. Amino Acids 32: 213-224.
34. Fu Q, Dai H, Hu W, Fan Y, Shen Y, et al. (2008) Carnosine protects against Abeta42-induced neurotoxicity in differentiated rat PC12 cells. Cell Mol Neurobiol 28: 307-316.
35. Calabrese EJ, (2008) Alzheimer's disease drugs: an application of the hormetic dose-response model. Crit Rev Toxicol 38: 419-451.
36. Cornelli U, (2010) Treatment of Alzheimer's disease with a cholinesterase inhibitor combined with antioxidants. Neurodegener Dis 7: 193-202.
37. Corona C, Frazzini V, Silvestri E, Lattanzio R, La Sorda R, et al. (2011) Effects of dietary supplementation of carnosine on mitochondrial dysfunction, amyloid pathology, and cognitive deficits in 3×Tg-AD mice. PLoS One 6: e17971.
38. Balion CM, Benson C, Raina PS, Papaioannou A, Patterson C, et al. (2007) Brain type carnosinase in dementia: a pilot study. BMC Neurol 7: 38.
39. Perrin RJ, Craig-Schapiro R, Malone JP, Shah AR, Gilmore P, et al. (2011) Identification and validation of novel cerebrospinal fluid biomarkers for staging early Alzheimer's disease. PLoS One 6: e16032.
40. Daniel H, Kottra G, (2004) The proton oligopeptide cotransporter family SLC15 in physiology and pharmacology. Pflugers Arch 447: 610-618.
41. Arisi I, D'Onofrio M, Brandi R, Felsani A, Capsoni S, et al. (2011) Gene expression biomarkers in the brain of a mouse model for Alzheimer's disease: mining of microarray data by logic classification and feature selection. Alzheimers Dis 24: 721-738.
42. Giuffrida ML, Caraci F, Pignataro B, Cataldo S, De Bona P, et al. (2009) Beta-amyloid monomers are neuroprotective. J Neurosci 29: 10582-10587.
43. Ahmed M, Davis J, Aucoin D, Sato T, Ahuja S, et al. (2010) Structural conversion of neurotoxic amyloid-beta(1-42) oligomers to fibrils. Nat Struct Mol Biol 17: 561-567.
44. Katzman R, Terry RD, Bick KL (1978) Alzheimer's disease: senile dementia and related disorders. New York: Raven Press.
45. Lambert MP, Barlow AK, Chromy BA, Edwards C, Freed R, et al. (1998) Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc Natl Acad Sci U S A 95: 6448-6453.
46. Bettens K, Sleegers K, Van Broeckhoven C, (2010) Current status on Alzheimer disease molecular genetics: from past, to present, to future. Hum Mol Genet 19: R4-R11.
47. Mayeux R, Schupf N, (2011) Blood-based biomarkers for Alzheimer's disease: plasma Aβ40 and Aβ42, and genetic variants. Neurobiol Aging 32: S10-S19.
48. Lomakin A, Chung DS, Benedek GB, Kirschner DA, Teplow DB, (1996) On the nucleation and growth of amyloid beta-protein fibrils: detection of nuclei and quantitation of rate constants. Proc Natl Acad Sci U S A 93: 1125-1129.
49. Chiti F, Webster P, Taddei N, Clark A, Stefani M, et al. (1999) Designing conditions for in vitro formation of amyloid protofilaments and fibrils. Proc Natl Acad Sci U S A 96: 3590-3594.
50. Shankar GM, Li S, Mehta TH, Garcia-Munoz A, Shepardson NE, et al. (2008) Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat Med 14: 837-842.
51. Park KM, Yule DI, Bowers WJ, (2010) Impaired TNF-alpha control of IP3R-mediated Ca2+ release in Alzheimer's disease mouse neurons. Cell Signal 22: 519-526.
52. Mitew S, Kirkcaldie MT, Halliday GM, Shepherd CE, Vickers JC, et al. (2010) Focal demyelination in Alzheimer's disease and transgenic mouse models. Acta Neuropathol 119: 567-577.
53. Hickman SE, El Khoury J, (2010) Mechanisms of mononuclear phagocyte recruitment in Alzheimer's disease. CNS Neurol Disord Drug Targets 9: 168-173.
54. Rezai-Zadeh K, Gate D, Gowing G, Town T, (2011) How to get from here to there: macrophage recruitment in Alzheimer's disease. Curr Alzheimer Res 8: 156-163.
55. Lührs T, Ritter C, Adrian M, Riek-Loher D, Bohrmann B, et al. (2005) 3D structure of Alzheimer's amyloid-beta(1-42) fibrils. Proc Natl Acad Sci U S A 102: 17342-17347.
56. Sipe JD, Cohen AS, (2000) Review: history of the amyloid fibril. J Struct Biol 130: 88-98.
57. Chini MG, Scrima M, D'Ursi AM, Bifulco GJ, (2009) Fibril aggregation inhibitory activity of the beta-sheet breaker peptides: a molecular docking approach. Pept Sci 15: 229-234.
58. Wang F, Zhou XL, Yang QG, Xu WH, Wang F, et al. (2011) A peptide that binds specifically to the β-amyloid of Alzheimer's disease: selection and assessment of anti-β-amyloid neurotoxic effects. PLoS One 6: e27649.
59. Amijee H, Madine J, Middleton DA, Doig AJ, (2009) Inhibitors of protein aggregation and toxicity. Biochem Soc Trans 37: 692-696.
60. Wiesehan K, Stöhr J, Nagel-Steger L, van Groen T, Riesner D, et al. (2008) Inhibition of cytotoxicity and amyloid fibril formation by a D-amino acid peptide that specifically binds to Alzheimer's disease amyloid peptide. Protein Eng Des Sel 21: 241-246.
61. Walsh DM, Hartley DM, Kusumoto Y, Fezoui Y, Condron MM, et al. (1999) Amyloid beta-protein fibrillogenesis. Structure and biological activity of protofibrillar intermediates. J Biol Chem 274: 25945-25952.
62. Blackley HK, Sanders GH, Davies MC, Roberts CJ, Tendler SJ, et al. (2000) In-situ atomic force microscopy study of beta-amyloid fibrillization. J Mol Biol 298: 833-840.
63. Mastrangelo IA, Ahmed M, Sato T, Liu W, Wang C, et al. (2006) High-resolution atomic force microscopy of soluble Abeta42 oligomers. J Mol Biol 358: 106-119.
64. Hasegawa K, Yamaguchi I, Omata S, Gejyo F, Naiki H, (1999) Interaction between Aβ(1-42) and Aβ(1-40) in Alzheimer's β-Amyloid fibril formation in vitro. Biochemistry 38: 15514-15521.
65. Liu D, Xu Y, Feng Y, Liu H, Shen X, et al. (2006) Inhibitor discovery targeting the intermediate structure of beta-amyloid peptide on the conformational transition pathway: implications in the aggregation mechanism of beta-amyloid peptide. Biochemistry 45: 10963-10972.
66. Naiki H, Higuchi K, Hosokawa M, Takeda T, (1989) Fluorometric determination of amyloid fibrils in vitro using the fluorescent dye, thioflavin T1. Anal Biochem 177: 244-249.
67. Khurana R, Coleman C, Ionescu-Zanetti C, Carter SA, Krishna V, et al. (2005) Mechanism of thioflavin T binding to amyloid fibrils. Struct Biol 151: 229-238.
68. Fung SY, Keyes C, Duhamel J, Chen P, (2003) Concentration effect on the aggregation of a self-assembling oligopeptide. Biophys J 85: 537-548.
69. Trott O, Olson AJ, (2010) AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J Comput Chem 31: 455-461.
70. Guha R, Howard MT, Hutchison GR, Murray-Rust P, Rzepa H, et al. (2006) The Blue Obelisk-interoperability in chemical informatics. J Chem Inf Model 46: 991-998.
71. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, et al. (2004) UCSF Chimera a visualization system for exploratory research and analysis. J Comput Chem 25: 1605-1612.
72. Hetényi C, Maran U, García-Sosa AT, Karelson M, (2007) Structure-based calculation of drug efficiency indices. Bioinformatics 23: 2678-2685.
73. García-Sosa AT, Hetényi C, Maran U, (2010) Drug efficiency indices for improvement of molecular docking scoring functions. J Comput Chem 31: 174-184.
74. Kohen R, Yamamoto Y, Cundy KC, Ames BN, (1988) Antioxidant activity of carnosine, homocarnosine, and anserine present in muscle and brain. Proc Natl Acad Sci U S A 85: 3175-3179.
75. Tabakman R, Lazarovici P, Kohen RJ, (2002) Neuroprotective effects of carnosine and homocarnosine on pheochromocytoma PC12 cells exposed to ischemia. Neurosci Res 68: 463-469.
76. Arimon M, Díez-Pérez I, Kogan MJ, Durany N, Giralt E, et al. (2005) Fine structure study of Abeta1-42 fibrillogenesis with atomic force microscopy. FASEB J 19: 1344-1346.
77. Ono K, Yamada MJ, (2011) Low-n oligomers as therapeutic targets of Alzheimer's disease. Neurochem 117: 19-28.
78. Hopkins AL, Groom CR, Alex A, (2004) Ligand efficiency: a useful metric for lead selection. Drug Discov Today 9: 430-431.
79. Abad-Zapatero C, Metz JT, (2005) Ligand efficiency indices as guideposts for drug discovery. Drug Discov Today 10: 464-469.
80. Wells JA, McClendon CL, (2007) Reaching for high-hanging fruit in drug discovery at protein-protein interfaces. Nature 450: 1001-1009.
81. García-Sosa AT, Sild S, Maran U, (2008) Design of multi-binding-site inhibitors, ligand efficiency, and consensus screening of avian influenza H5N1 wild-type neuraminidase and of the oseltamivir-resistant H274Y variant. J Chem Inf Model 48: 2074-2080.
82. Ono K, Condron MM, Teplow DB, (2009) Structure-neurotoxicity relationships of amyloid beta-protein oligomers. Proc Natl Acad Sci U S A 106: 14745-14750.