Amyloidogenic Peptides in Human Neuro-Degenerative Diseases and in Microorganisms: A Sorrow Shared Is a Sorrow Halved?
Abstract
:1. Introduction
2. The Impact of Host Amyloidogenic Peptides on Microbial Commensals
3. Occurrence and Function of Amyloidogenic Peptides in Microbial Organisms
4. Impact of Microbial Amyloids on Host Health and Neurodegeneration
5. Therapeutic Strategies Derived from Microbes against Human Amyloidosis
6. Conclusions
Funding
Acknowledgments
Conflicts of Interest
References
- Otzen, D.; Riek, R. Functional Amyloids. Cold Spring Harb. Perspect. Biol. 2019, 11. [Google Scholar] [CrossRef] [PubMed]
- Bissig, C.; Rochin, L.; van Niel, G. PMEL Amyloid Fibril Formation: The Bright Steps of Pigmentation. Int. J. Mol. Sci. 2016, 17, 1438. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, J.; McQuade, T.; Siemer, A.B.; Napetschnig, J.; Moriwaki, K.; Hsiao, Y.S.; Damko, E.; Moquin, D.; Walz, T.; McDermott, A.; et al. The RIP1/RIP3 necrosome forms a functional amyloid signaling complex required for programmed necrosis. Cell 2012, 150, 339–350. [Google Scholar] [CrossRef] [Green Version]
- Lin, Q.S.; Chen, P.; Wang, W.X.; Lin, C.C.; Zhou, Y.; Yu, L.H.; Lin, Y.X.; Xu, Y.F.; Kang, D.Z. RIP1/RIP3/MLKL mediates dopaminergic neuron necroptosis in a mouse model of Parkinson disease. Lab. Investig. 2019. [Google Scholar] [CrossRef] [PubMed]
- Chiti, F.; Dobson, C.M. Protein Misfolding, Amyloid Formation, and Human Disease: A Summary of Progress over the Last Decade. Annu. Rev. Biochem. 2017, 86, 27–68. [Google Scholar] [CrossRef] [PubMed]
- Joy, T.; Wang, J.; Hahn, A.; Hegele, R.A. APOA1 related amyloidosis: A case report and literature review. Clin. Biochem. 2003, 36, 641–645. [Google Scholar] [CrossRef]
- Granel, B.; Valleix, S.; Serratrice, J.; Cherin, P.; Texeira, A.; Disdier, P.; Weiller, P.J.; Grateau, G. Lysozyme amyloidosis: Report of 4 cases and a review of the literature. Medicine (Baltimore) 2006, 85, 66–73. [Google Scholar] [CrossRef]
- Scheltens, P.; Blennow, K.; Breteler, M.M.; de Strooper, B.; Frisoni, G.B.; Salloway, S.; Van der Flier, W.M. Alzheimer’s disease. Lancet 2016, 388, 505–517. [Google Scholar] [CrossRef]
- Dorsey, E.R.; Sherer, T.; Okun, M.S.; Bloem, B.R. The Emerging Evidence of the Parkinson Pandemic. J. Parkinsons Dis. 2018, 8, S3–S8. [Google Scholar] [CrossRef] [Green Version]
- Endres, K.; Schafer, K.H. Influence of Commensal Microbiota on the Enteric Nervous System and Its Role in Neurodegenerative Diseases. J. Innate Immun. 2018, 10, 172–180. [Google Scholar] [CrossRef]
- Santos, S.F.; de Oliveira, H.L.; Yamada, E.S.; Neves, B.C.; Pereira, A., Jr. The Gut and Parkinson’s Disease-A Bidirectional Pathway. Front. Neurol. 2019, 10, 574. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- D’Argenio, V.; Sarnataro, D. Microbiome Influence in the Pathogenesis of Prion and Alzheimer’s Diseases. Int. J. Mol. Sci. 2019, 20, 4704. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Scheperjans, F.; Derkinderen, P.; Borghammer, P. The Gut and Parkinson’s Disease: Hype or Hope? J. Parkinsons Dis. 2018, 8, S31–S39. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Scheperjans, F.; Aho, V.; Pereira, P.A.; Koskinen, K.; Paulin, L.; Pekkonen, E.; Haapaniemi, E.; Kaakkola, S.; Eerola-Rautio, J.; Pohja, M.; et al. Gut microbiota are related to Parkinson’s disease and clinical phenotype. Mov. Disord. 2015, 30, 350–358. [Google Scholar] [CrossRef]
- Keshavarzian, A.; Green, S.J.; Engen, P.A.; Voigt, R.M.; Naqib, A.; Forsyth, C.B.; Mutlu, E.; Shannon, K.M. Colonic bacterial composition in Parkinson’s disease. Mov. Disord. 2015, 30, 1351–1360. [Google Scholar] [CrossRef]
- Unger, M.M.; Spiegel, J.; Dillmann, K.U.; Grundmann, D.; Philippeit, H.; Burmann, J.; Fassbender, K.; Schwiertz, A.; Schafer, K.H. Short chain fatty acids and gut microbiota differ between patients with Parkinson’s disease and age-matched controls. Parkinsonism Relat. Disord. 2016, 32, 66–72. [Google Scholar] [CrossRef]
- Bedarf, J.R.; Hildebrand, F.; Coelho, L.P.; Sunagawa, S.; Bahram, M.; Goeser, F.; Bork, P.; Wullner, U. Functional implications of microbial and viral gut metagenome changes in early stage L-DOPA-naive Parkinson’s disease patients. Genome Med. 2017, 9, 39. [Google Scholar] [CrossRef]
- Heintz-Buschart, A.; Pandey, U.; Wicke, T.; Sixel-Doring, F.; Janzen, A.; Sittig-Wiegand, E.; Trenkwalder, C.; Oertel, W.H.; Mollenhauer, B.; Wilmes, P. The nasal and gut microbiome in Parkinson’s disease and idiopathic rapid eye movement sleep behavior disorder. Mov. Disord. 2018, 33, 88–98. [Google Scholar] [CrossRef] [Green Version]
- Endres, K. Retinoic Acid and the Gut Microbiota in Alzheimer’s Disease: Fighting Back-to-Back? Curr. Alzheimer Res. 2019, 16, 405–417. [Google Scholar] [CrossRef]
- Sun, M.F.; Zhu, Y.L.; Zhou, Z.L.; Jia, X.B.; Xu, Y.D.; Yang, Q.; Cui, C.; Shen, Y.Q. Neuroprotective effects of fecal microbiota transplantation on MPTP-induced Parkinson’s disease mice: Gut microbiota, glial reaction and TLR4/TNF-alpha signaling pathway. Brain Behav. Immun. 2018, 70, 48–60. [Google Scholar] [CrossRef]
- Sun, J.; Xu, J.; Ling, Y.; Wang, F.; Gong, T.; Yang, C.; Ye, S.; Ye, K.; Wei, D.; Song, Z.; et al. Fecal microbiota transplantation alleviated Alzheimer’s disease-like pathogenesis in APP/PS1 transgenic mice. Transl. Psychiatry 2019, 9, 189. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Paiva, I.; Pinho, R.; Pavlou, M.A.; Hennion, M.; Wales, P.; Schutz, A.L.; Rajput, A.; Szego, E.M.; Kerimoglu, C.; Gerhardt, E.; et al. Sodium butyrate rescues dopaminergic cells from alpha-synuclein-induced transcriptional deregulation and DNA damage. Hum. Mol. Genet. 2017, 26, 2231–2246. [Google Scholar] [CrossRef] [PubMed]
- Kong, Y.; Jiang, B.; Luo, X. Gut microbiota influences Alzheimer’s disease pathogenesis by regulating acetate in Drosophila model. Future Microbiol. 2018, 13, 1117–1128. [Google Scholar] [CrossRef] [PubMed]
- Oakley, H.; Cole, S.L.; Logan, S.; Maus, E.; Shao, P.; Craft, J.; Guillozet-Bongaarts, A.; Ohno, M.; Disterhoft, J.; Van Eldik, L.; et al. Intraneuronal beta-amyloid aggregates, neurodegeneration, and neuron loss in transgenic mice with five familial Alzheimer’s disease mutations: Potential factors in amyloid plaque formation. J. Neurosci. 2006, 26, 10129–10140. [Google Scholar] [CrossRef] [PubMed]
- Zhan, X.; Stamova, B.; Sharp, F.R. Lipopolysaccharide Associates with Amyloid Plaques, Neurons and Oligodendrocytes in Alzheimer’s Disease Brain: A Review. Front. Aging Neurosci. 2018, 10, 42. [Google Scholar] [CrossRef] [Green Version]
- Miklossy, J. Alzheimer’s disease—A neurospirochetosis. Analysis of the evidence following Koch’s and Hill’s criteria. J. Neuroinflammation 2011, 8, 90. [Google Scholar] [CrossRef] [Green Version]
- Lionnet, A.; Leclair-Visonneau, L.; Neunlist, M.; Murayama, S.; Takao, M.; Adler, C.H.; Derkinderen, P.; Beach, T.G. Does Parkinson’s disease start in the gut? Acta Neuropathol. 2018, 135, 1–12. [Google Scholar] [CrossRef]
- Brandscheid, C.; Schuck, F.; Reinhardt, S.; Schafer, K.H.; Pietrzik, C.U.; Grimm, M.; Hartmann, T.; Schwiertz, A.; Endres, K. Altered Gut Microbiome Composition and Tryptic Activity of the 5xFAD Alzheimer’s Mouse Model. J. Alzheimers Dis. 2017, 56, 775–788. [Google Scholar] [CrossRef]
- Joachim, C.L.; Mori, H.; Selkoe, D.J. Amyloid beta-protein deposition in tissues other than brain in Alzheimer’s disease. Nature 1989, 341, 226–230. [Google Scholar] [CrossRef]
- Park, S.C.; Moon, J.C.; Shin, S.Y.; Son, H.; Jung, Y.J.; Kim, N.H.; Kim, Y.M.; Jang, M.K.; Lee, J.R. Functional characterization of alpha-synuclein protein with antimicrobial activity. Biochem. Biophys. Res. Commun. 2016, 478, 924–928. [Google Scholar] [CrossRef]
- Spitzer, P.; Condic, M.; Herrmann, M.; Oberstein, T.J.; Scharin-Mehlmann, M.; Gilbert, D.F.; Friedrich, O.; Gromer, T.; Kornhuber, J.; Lang, R.; et al. Amyloidogenic amyloid-beta-peptide variants induce microbial agglutination and exert antimicrobial activity. Sci. Rep. 2016, 6, 32228. [Google Scholar] [CrossRef] [PubMed]
- Soscia, S.J.; Kirby, J.E.; Washicosky, K.J.; Tucker, S.M.; Ingelsson, M.; Hyman, B.; Burton, M.A.; Goldstein, L.E.; Duong, S.; Tanzi, R.E.; et al. The Alzheimer’s disease-associated amyloid beta-protein is an antimicrobial peptide. PLoS ONE 2010, 5, e9505. [Google Scholar] [CrossRef] [PubMed]
- Liang, K.J.; Carlson, E.S. Resistance, vulnerability and resilience: A review of the cognitive cerebellum in aging and neurodegenerative diseases. Neurobiol. Learn. Mem. 2019. [Google Scholar] [CrossRef] [PubMed]
- Kumar, D.K.; Choi, S.H.; Washicosky, K.J.; Eimer, W.A.; Tucker, S.; Ghofrani, J.; Lefkowitz, A.; McColl, G.; Goldstein, L.E.; Tanzi, R.E.; et al. Amyloid-beta peptide protects against microbial infection in mouse and worm models of Alzheimer’s disease. Sci. Transl. Med. 2016, 8, 340ra372. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gosztyla, M.L.; Brothers, H.M.; Robinson, S.R. Alzheimer’s Amyloid-beta is an Antimicrobial Peptide: A Review of the Evidence. J. Alzheimers Dis. 2018, 62, 1495–1506. [Google Scholar] [CrossRef] [Green Version]
- Erickson, M.A.; Banks, W.A. Age-Associated Changes in the Immune System and Blood(-)Brain Barrier Functions. Int. J. Mol. Sci. 2019, 20, 1632. [Google Scholar] [CrossRef] [Green Version]
- Gerhardt, S.; Mohajeri, M.H. Changes of Colonic Bacterial Composition in Parkinson’s Disease and Other Neurodegenerative Diseases. Nutrients 2018, 10, 708. [Google Scholar] [CrossRef] [Green Version]
- Fowler, D.M.; Koulov, A.V.; Alory-Jost, C.; Marks, M.S.; Balch, W.E.; Kelly, J.W. Functional amyloid formation within mammalian tissue. PLoS Biol. 2006, 4, e6. [Google Scholar] [CrossRef]
- Maji, S.K.; Perrin, M.H.; Sawaya, M.R.; Jessberger, S.; Vadodaria, K.; Rissman, R.A.; Singru, P.S.; Nilsson, K.P.; Simon, R.; Schubert, D.; et al. Functional amyloids as natural storage of peptide hormones in pituitary secretory granules. Science 2009, 325, 328–332. [Google Scholar] [CrossRef] [Green Version]
- Whelly, S.; Johnson, S.; Powell, J.; Borchardt, C.; Hastert, M.C.; Cornwall, G.A. Nonpathological extracellular amyloid is present during normal epididymal sperm maturation. PLoS ONE 2012, 7, e36394. [Google Scholar] [CrossRef] [Green Version]
- Greenwald, J.; Kwiatkowski, W.; Riek, R. Peptide Amyloids in the Origin of Life. J. Mol. Biol. 2018, 430, 3735–3750. [Google Scholar] [CrossRef] [PubMed]
- Costerton, J.W.; Geesey, G.G.; Cheng, K.J. How bacteria stick. Sci. Am. 1978, 238, 86–95. [Google Scholar] [CrossRef] [PubMed]
- Guttenplan, S.B.; Kearns, D.B. Regulation of flagellar motility during biofilm formation. FEMS Microbiol. Rev. 2013, 37, 849–871. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Okshevsky, M.; Meyer, R.L. The role of extracellular DNA in the establishment, maintenance and perpetuation of bacterial biofilms. Crit Rev. Microbiol. 2015, 41, 341–352. [Google Scholar] [CrossRef] [PubMed]
- Serra, D.O.; Hengge, R. A c-di-GMP-Based Switch Controls Local Heterogeneity of Extracellular Matrix Synthesis which Is Crucial for Integrity and Morphogenesis of Escherichia coli Macrocolony Biofilms. J. Mol. Biol. 2019, 431, 4775–4793. [Google Scholar] [CrossRef] [PubMed]
- Zogaj, X.; Bokranz, W.; Nimtz, M.; Romling, U. Production of cellulose and curli fimbriae by members of the family Enterobacteriaceae isolated from the human gastrointestinal tract. Infect. Immun. 2003, 71, 4151–4158. [Google Scholar] [CrossRef] [Green Version]
- Louros, N.N.; Bolas, G.M.P.; Tsiolaki, P.L.; Hamodrakas, S.J.; Iconomidou, V.A. Intrinsic aggregation propensity of the CsgB nucleator protein is crucial for curli fiber formation. J. Struct. Biol. 2016, 195, 179–189. [Google Scholar] [CrossRef]
- Hammer, N.D.; Schmidt, J.C.; Chapman, M.R. The curli nucleator protein, CsgB, contains an amyloidogenic domain that directs CsgA polymerization. Proc. Natl. Acad. Sci. USA 2007, 104, 12494–12499. [Google Scholar] [CrossRef] [Green Version]
- Dueholm, M.S.; Albertsen, M.; Otzen, D.; Nielsen, P.H. Curli functional amyloid systems are phylogenetically widespread and display large diversity in operon and protein structure. PLoS ONE 2012, 7, e51274. [Google Scholar] [CrossRef] [Green Version]
- Brombacher, E.; Baratto, A.; Dorel, C.; Landini, P. Gene expression regulation by the Curli activator CsgD protein: Modulation of cellulose biosynthesis and control of negative determinants for microbial adhesion. J. Bacteriol. 2006, 188, 2027–2037. [Google Scholar] [CrossRef] [Green Version]
- Larsen, P.; Nielsen, J.L.; Dueholm, M.S.; Wetzel, R.; Otzen, D.; Nielsen, P.H. Amyloid adhesins are abundant in natural biofilms. Environ. Microbiol. 2007, 9, 3077–3090. [Google Scholar] [CrossRef] [PubMed]
- Cimdins, A.; Simm, R. Semiquantitative Analysis of the Red, Dry, and Rough Colony Morphology of Salmonella enterica Serovar Typhimurium and Escherichia coli Using Congo Red. Methods Mol. Biol. 2017, 1657, 225–241. [Google Scholar] [CrossRef]
- Goulter-Thorsen, R.M.; Taran, E.; Gentle, I.R.; Gobius, K.S.; Dykes, G.A. CsgA Production by Escherichia coli O157:H7 Alters Attachment to Abiotic Surfaces in Some Growth Environments. Appl. Environ. Microb. 2011, 77, 7339–7344. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Oh, Y.J.; Hubauer-Brenner, M.; Gruber, H.J.; Cui, Y.D.; Traxler, L.; Siligan, C.; Park, S.; Hinterdorfer, P. Curli mediate bacterial adhesion to fibronectin via tensile multiple bonds. Sci. Rep. 2016, 6. [Google Scholar] [CrossRef] [PubMed]
- Gophna, U.; Oelschlaeger, T.A.; Hacker, J.; Ron, E.Z. Role of fibronectin in curli-mediated internalization. FEMS Microbiol. Lett. 2002, 212, 55–58. [Google Scholar] [CrossRef] [PubMed]
- Kock, R.; Becker, K.; Cookson, B.; van Gemert-Pijnen, J.E.; Harbarth, S.; Kluytmans, J.; Mielke, M.; Peters, G.; Skov, R.L.; Struelens, M.J.; et al. Methicillin-resistant Staphylococcus aureus (MRSA): Burden of disease and control challenges in Europe. Euro Surveill 2010, 15, 19688. [Google Scholar] [CrossRef] [PubMed]
- Khorasani, M.R.; Zamanzad, B.; Rostami, S.; Gholipour, A. High prevalence of SCC mec-associated Phenol-soluble modulin gene in clinical isolates of methicillin-resistant Staphylococcus aureus. Ann. Ig 2019, 31, 148–155. [Google Scholar] [CrossRef]
- Tayeb-Fligelman, E.; Tabachnikov, O.; Moshe, A.; Goldshmidt-Tran, O.; Sawaya, M.R.; Coquelle, N.; Colletier, J.P.; Landau, M. The cytotoxic Staphylococcus aureus PSMalpha3 reveals a cross-alpha amyloid-like fibril. Science 2017, 355, 831–833. [Google Scholar] [CrossRef]
- Salinas, N.; Colletier, J.P.; Moshe, A.; Landau, M. Extreme amyloid polymorphism in Staphylococcus aureus virulent PSMalpha peptides. Nat. Commun. 2018, 9, 3512. [Google Scholar] [CrossRef] [Green Version]
- Sztukowska, M.N.; Dutton, L.C.; Delaney, C.; Ramsdale, M.; Ramage, G.; Jenkinson, H.F.; Nobbs, A.H.; Lamont, R.J. Community Development between Porphyromonas gingivalis and Candida albicans Mediated by InlJ and Als3. mBio 2018, 9. [Google Scholar] [CrossRef] [Green Version]
- Saif, Y.M. Immunosuppression induced by infectious bursal disease virus. Vet. Immunol. Immunopathol. 1991, 30, 45–50. [Google Scholar] [CrossRef]
- Zheng, X.; Jia, L.; Hu, B.; Sun, Y.; Zhang, Y.; Gao, X.; Deng, T.; Bao, S.; Xu, L.; Zhou, J. The C-terminal amyloidogenic peptide contributes to self-assembly of Avibirnavirus viral protease. Sci. Rep. 2015, 5, 14794. [Google Scholar] [CrossRef] [Green Version]
- Ohnishi, S.; Koide, A.; Koide, S. Solution conformation and amyloid-like fibril formation of a polar peptide derived from a beta-hairpin in the OspA single-layer beta-sheet. J. Mol. Biol. 2000, 301, 477–489. [Google Scholar] [CrossRef] [PubMed]
- Malabirade, A.; Morgado-Brajones, J.; Trepout, S.; Wien, F.; Marquez, I.; Seguin, J.; Marco, S.; Velez, M.; Arluison, V. Membrane association of the bacterial riboregulator Hfq and functional perspectives. Sci. Rep. 2017, 7, 10724. [Google Scholar] [CrossRef] [PubMed]
- Chiang, Y.L.; Chang, Y.C.; Chiang, I.C.; Mak, H.M.; Hwang, I.S.; Shih, Y.L. Atomic Force Microscopy Characterization of Protein Fibrils Formed by the Amyloidogenic Region of the Bacterial Protein MinE on Mica and a Supported Lipid Bilayer. PLoS ONE 2015, 10, e0142506. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hsieh, C.W.; Lin, T.Y.; Lai, H.M.; Lin, C.C.; Hsieh, T.S.; Shih, Y.L. Direct MinE-membrane interaction contributes to the proper localization of MinDE in E. coli. Mol. Microbiol. 2010, 75, 499–512. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Canale, C.; Torrassa, S.; Rispoli, P.; Relini, A.; Rolandi, R.; Bucciantini, M.; Stefani, M.; Gliozzi, A. Natively folded HypF-N and its early amyloid aggregates interact with phospholipid monolayers and destabilize supported phospholipid bilayers. Biophys. J. 2006, 91, 4575–4588. [Google Scholar] [CrossRef] [Green Version]
- Hammer, N.D.; McGuffie, B.A.; Zhou, Y.; Badtke, M.P.; Reinke, A.A.; Brannstrom, K.; Gestwicki, J.E.; Olofsson, A.; Almqvist, F.; Chapman, M.R. The C-terminal repeating units of CsgB direct bacterial functional amyloid nucleation. J. Mol. Biol. 2012, 422, 376–389. [Google Scholar] [CrossRef] [Green Version]
- Lopez-Ochoa, J.; Montes-Garcia, J.F.; Vazquez, C.; Sanchez-Alonso, P.; Perez-Marquez, V.M.; Blackall, P.J.; Vaca, S.; Negrete-Abascal, E. Gallibacterium elongation factor-Tu possesses amyloid-like protein characteristics, participates in cell adhesion, and is present in biofilms. J. Microbiol. 2017, 55, 745–752. [Google Scholar] [CrossRef]
- Montes Garcia, J.F.; Vaca, S.; Delgado, N.L.; Uribe-Garcia, A.; Vazquez, C.; Sanchez Alonso, P.; Xicohtencatl Cortes, J.; Cruz Cordoba, A.; Negrete Abascal, E. Mannheimia haemolytica OmpP2-like is an amyloid-like protein, forms filaments, takes part in cell adhesion and is part of biofilms. Antonie Van Leeuwenhoek 2018, 111, 2311–2321. [Google Scholar] [CrossRef]
- Wang, L.; Maji, S.K.; Sawaya, M.R.; Eisenberg, D.; Riek, R. Bacterial inclusion bodies contain amyloid-like structure. PLoS Biol. 2008, 6, e195. [Google Scholar] [CrossRef] [PubMed]
- Conrad, W.H.; Osman, M.M.; Shanahan, J.K.; Chu, F.; Takaki, K.K.; Cameron, J.; Hopkinson-Woolley, D.; Brosch, R.; Ramakrishnan, L. Mycobacterial ESX-1 secretion system mediates host cell lysis through bacterium contact-dependent gross membrane disruptions. Proc. Natl. Acad. Sci. USA 2017, 114, 1371–1376. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bleem, A.; Christiansen, G.; Madsen, D.J.; Maric, H.; Stromgaard, K.; Bryers, J.D.; Daggett, V.; Meyer, R.L.; Otzen, D.E. Protein Engineering Reveals Mechanisms of Functional Amyloid Formation in Pseudomonas aeruginosa Biofilms. J. Mol. Biol. 2018, 430, 3751–3763. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zeng, G.; Vad, B.S.; Dueholm, M.S.; Christiansen, G.; Nilsson, M.; Tolker-Nielsen, T.; Nielsen, P.H.; Meyer, R.L.; Otzen, D.E. Functional bacterial amyloid increases Pseudomonas biofilm hydrophobicity and stiffness. Front. Microbiol. 2015, 6, 1099. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Marinelli, P.; Pallares, I.; Navarro, S.; Ventura, S. Dissecting the contribution of Staphylococcus aureus alpha-phenol-soluble modulins to biofilm amyloid structure. Sci. Rep. 2016, 6, 34552. [Google Scholar] [CrossRef] [PubMed]
- Schwartz, K.; Sekedat, M.D.; Syed, A.K.; O’Hara, B.; Payne, D.E.; Lamb, A.; Boles, B.R. The AgrD N-terminal leader peptide of Staphylococcus aureus has cytolytic and amyloidogenic properties. Infect. Immun. 2014, 82, 3837–3844. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lembre, P.; Vendrely, C.; Martino, P.D. Identification of an amyloidogenic peptide from the Bap protein of Staphylococcus epidermidis. Protein Pept. Lett. 2014, 21, 75–79. [Google Scholar] [CrossRef]
- Lin, J.; Oh, S.H.; Jones, R.; Garnett, J.A.; Salgado, P.S.; Rusnakova, S.; Matthews, S.J.; Hoyer, L.L.; Cota, E. The peptide-binding cavity is essential for Als3-mediated adhesion of Candida albicans to human cells. J. Biol. Chem. 2014, 289, 18401–18412. [Google Scholar] [CrossRef] [Green Version]
- Selivanova, O.M.; Glyakina, A.V.; Gorbunova, E.Y.; Mustaeva, L.G.; Suvorina, M.Y.; Grigorashvili, E.I.; Nikulin, A.D.; Dovidchenko, N.V.; Rekstina, V.V.; Kalebina, T.S.; et al. Structural model of amyloid fibrils for amyloidogenic peptide from Bgl2p-glucantransferase of S. cerevisiae cell wall and its modifying analog. New morphology of amyloid fibrils. Biochim. Biophys. Acta 2016, 1864, 1489–1499. [Google Scholar] [CrossRef]
- Zhang, S.M.; Liao, Y.; Neo, T.L.; Lu, Y.; Liu, D.X.; Vahlne, A.; Tam, J.P. Identification and application of self-binding zipper-like sequences in SARS-CoV spike protein. Int. J. Biochem. Cell Biol. 2018, 101, 103–112. [Google Scholar] [CrossRef]
- Ulusoy, A.; Rusconi, R.; Perez-Revuelta, B.I.; Musgrove, R.E.; Helwig, M.; Winzen-Reichert, B.; Di Monte, D.A. Caudo-rostral brain spreading of alpha-synuclein through vagal connections. EMBO Mol. Med. 2013, 5, 1119–1127. [Google Scholar] [CrossRef] [PubMed]
- Suarez, A.N.; Hsu, T.M.; Liu, C.M.; Noble, E.E.; Cortella, A.M.; Nakamoto, E.M.; Hahn, J.D.; de Lartigue, G.; Kanoski, S.E. Gut vagal sensory signaling regulates hippocampus function through multi-order pathways. Nat. Commun. 2018, 9, 2181. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rinaman, L. Ascending projections from the caudal visceral nucleus of the solitary tract to brain regions involved in food intake and energy expenditure. Brain Res. 2010, 1350, 18–34. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Grill, H.J.; Hayes, M.R. Hindbrain neurons as an essential hub in the neuroanatomically distributed control of energy balance. Cell Metab. 2012, 16, 296–309. [Google Scholar] [CrossRef] [Green Version]
- Liu, B.; Fang, F.; Pedersen, N.L.; Tillander, A.; Ludvigsson, J.F.; Ekbom, A.; Svenningsson, P.; Chen, H.; Wirdefeldt, K. Vagotomy and Parkinson disease: A Swedish register-based matched-cohort study. Neurology 2017, 88, 1996–2002. [Google Scholar] [CrossRef] [Green Version]
- Uemura, N.; Yagi, H.; Uemura, M.T.; Hatanaka, Y.; Yamakado, H.; Takahashi, R. Inoculation of alpha-synuclein preformed fibrils into the mouse gastrointestinal tract induces Lewy body-like aggregates in the brainstem via the vagus nerve. Mol. Neurodegener. 2018, 13, 21. [Google Scholar] [CrossRef] [Green Version]
- Kaatz, M.; Fast, C.; Ziegler, U.; Balkema-Buschmann, A.; Hammerschmidt, B.; Keller, M.; Oelschlegel, A.; McIntyre, L.; Groschup, M.H. Spread of classic BSE prions from the gut via the peripheral nervous system to the brain. Am. J. Pathol. 2012, 181, 515–524. [Google Scholar] [CrossRef]
- Marshall, A.; Bradford, B.M.; Clarke, A.R.; Manson, J.C.; Mabbott, N.A. Oral Prion Neuroinvasion Occurs Independently of PrP(C) Expression in the Gut Epithelium. J. Virol. 2018, 92. [Google Scholar] [CrossRef] [Green Version]
- Endres, K.; Reinhardt, S.; Geladaris, A.; Knies, J.; Grimm, M.; Hartmann, T.; Schmitt, U. Transnasal delivery of human A-beta peptides elicits impaired learning and memory performance in wild type mice. BMC Neurosci. 2016, 17, 44. [Google Scholar] [CrossRef] [Green Version]
- Chen, S.G.; Stribinskis, V.; Rane, M.J.; Demuth, D.R.; Gozal, E.; Roberts, A.M.; Jagadapillai, R.; Liu, R.; Choe, K.; Shivakumar, B.; et al. Exposure to the Functional Bacterial Amyloid Protein Curli Enhances Alpha-Synuclein Aggregation in Aged Fischer 344 Rats and Caenorhabditis elegans. Sci. Rep. 2016, 6, 34477. [Google Scholar] [CrossRef]
- Sampson, T.R.; Challis, C.; Jain, N.; Moiseyenko, A.; Ladinsky, M.S.; Shastri, G.G.; Thron, T.; Needham, B.D.; Horvath, I.; Debelius, J.W.; et al. A gut bacterial amyloid promotes alpha-synuclein aggregation and motor impairment in mice. Elife 2020, 9. [Google Scholar] [CrossRef] [PubMed]
- Tatini, F.; Pugliese, A.M.; Traini, C.; Niccoli, S.; Maraula, G.; Ed Dami, T.; Mannini, B.; Scartabelli, T.; Pedata, F.; Casamenti, F.; et al. Amyloid-beta oligomer synaptotoxicity is mimicked by oligomers of the model protein HypF-N. Neurobiol. Aging 2013, 34, 2100–2109. [Google Scholar] [CrossRef] [PubMed]
- Esfandiary, E.; Karimipour, M.; Mardani, M.; Ghanadian, M.; Alaei, H.A.; Mohammadnejad, D.; Esmaeili, A. Neuroprotective effects of Rosa damascena extract on learning and memory in a rat model of amyloid-beta-induced Alzheimer’s disease. Adv. Biomed. Res. 2015, 4, 131. [Google Scholar] [CrossRef] [PubMed]
- Nimgampalle, M.; Kuna, Y. Anti-Alzheimer Properties of Probiotic, Lactobacillus plantarum MTCC 1325 in Alzheimer’s Disease induced Albino Rats. J. Clin. Diagn. Res. 2017, 11, KC01–KC05. [Google Scholar] [CrossRef]
- Kobayashi, Y.; Sugahara, H.; Shimada, K.; Mitsuyama, E.; Kuhara, T.; Yasuoka, A.; Kondo, T.; Abe, K.; Xiao, J.Z. Therapeutic potential of Bifidobacterium breve strain A1 for preventing cognitive impairment in Alzheimer’s disease. Sci. Rep. 2017, 7, 13510. [Google Scholar] [CrossRef]
- Bonfili, L.; Cecarini, V.; Cuccioloni, M.; Angeletti, M.; Berardi, S.; Scarpona, S.; Rossi, G.; Eleuteri, A.M. SLAB51 Probiotic Formulation Activates SIRT1 Pathway Promoting Antioxidant and Neuroprotective Effects in an AD Mouse Model. Mol. Neurobiol. 2018, 55, 7987–8000. [Google Scholar] [CrossRef] [Green Version]
- Athari Nik Azm, S.; Djazayeri, A.; Safa, M.; Azami, K.; Ahmadvand, B.; Sabbaghziarani, F.; Sharifzadeh, M.; Vafa, M. Lactobacilli and bifidobacteria ameliorate memory and learning deficits and oxidative stress in beta-amyloid (1–42) injected rats. Appl. Physiol. Nutr. Metab. 2018, 43, 718–726. [Google Scholar] [CrossRef]
- Rezaei Asl, Z.; Sepehri, G.; Salami, M. Probiotic treatment improves the impaired spatial cognitive performance and restores synaptic plasticity in an animal model of Alzheimer’s disease. Behav. Brain Res. 2019, 376, 112183. [Google Scholar] [CrossRef]
- Rezaeiasl, Z.; Salami, M.; Sepehri, G. The Effects of Probiotic Lactobacillus and Bifidobacterium Strains on Memory and Learning Behavior, Long-Term Potentiation (LTP), and Some Biochemical Parameters in beta-Amyloid-Induced Rat’s Model of Alzheimer’s Disease. Prev. Nutr. Food Sci. 2019, 24, 265–273. [Google Scholar] [CrossRef]
- Leblhuber, F.; Steiner, K.; Schuetz, B.; Fuchs, D.; Gostner, J.M. Probiotic Supplementation in Patients with Alzheimer’s Dementia—An Explorative Intervention Study. Curr. Alzheimer Res. 2018, 15, 1106–1113. [Google Scholar] [CrossRef]
- Jiang, X.; Yan, X.; Gu, S.; Yang, Y.; Zhao, L.; He, X.; Chen, H.; Ge, J.; Liu, D. Biosurfactants of Lactobacillus helveticus for biodiversity inhibit the biofilm formation of Staphylococcus aureus and cell invasion. Future Microbiol. 2019, 14, 1133–1146. [Google Scholar] [CrossRef] [PubMed]
- Christensen, L.F.B.; Jensen, K.F.; Nielsen, J.; Vad, B.S.; Christiansen, G.; Otzen, D.E. Reducing the Amyloidogenicity of Functional Amyloid Protein FapC Increases Its Ability To Inhibit alpha-Synuclein Fibrillation. ACS Omega 2019, 4, 4029–4039. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tetz, G.; Brown, S.M.; Hao, Y.; Tetz, V. Type 1 Diabetes: An Association between Autoimmunity, the Dynamics of Gut Amyloid-producing E. coli and Their Phages. Sci. Rep. 2019, 9, 9685. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pervin, M.; Unno, K.; Ohishi, T.; Tanabe, H.; Miyoshi, N.; Nakamura, Y. Beneficial Effects of Green Tea Catechins on Neurodegenerative Diseases. Molecules 2018, 23, 1297. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hengge, R. Targeting Bacterial Biofilms by the Green Tea Polyphenol EGCG. Molecules 2019, 24, 2403. [Google Scholar] [CrossRef] [Green Version]
- Ryzhova, T.A.; Sopova, J.V.; Zadorsky, S.P.; Siniukova, V.A.; Sergeeva, A.V.; Galkina, S.A.; Nizhnikov, A.A.; Shenfeld, A.A.; Volkov, K.V.; Galkin, A.P. Screening for amyloid proteins in the yeast proteome. Curr. Genet. 2018, 64, 469–478. [Google Scholar] [CrossRef]
- Sopova, J.V.; Koshel, E.I.; Belashova, T.A.; Zadorsky, S.P.; Sergeeva, A.V.; Siniukova, V.A.; Shenfeld, A.A.; Velizhanina, M.E.; Volkov, K.V.; Nizhnikov, A.A.; et al. RNA-binding protein FXR1 is presented in rat brain in amyloid form. Sci. Rep. 2019, 9, 18983. [Google Scholar] [CrossRef] [Green Version]
Name of Peptide or Protein | Disease |
---|---|
α-synuclein | Parkinson’s disease (PD) Lewy body disease Multiple systemic atrophy |
Amyloid-β | Alzheimer’s disease (AD) |
Ataxin | Spirocerebellar ataxia |
F-box protein 7 (FBXO7) | Parkinson’s disease (PD)/Alzheimer’s disease (AD) |
Prion protein (PrPsc) | Transmissible spongiform encephalopathy (TSE) |
Tau (hyperphosphorylated) | Frontotemporal dementia (FTD) Alzheimer’s disease (AD) Niemann Pick disease Progressive supranuclear palsy Amyotrophic lateral sclerosis (ALS) |
Transactive response DNA binding protein 43 (TDP43) | Amyotrophic lateral sclerosis (ALS) Alzheimer’s disease (AD) Frontotemporal lobar degeneration with ubiquitin-positive inclusions (FTLD-U) |
Superoxide dismutase 1 (SOD1) | Amyotrophic lateral sclerosis (ALS) |
Huntingtin (with polyQ tract >33 residues) | Huntington’s disease |
Name of Organism/Family | B = Bacterial F = Fungal V = Viral | Name of Peptide or Protein | Function | Reference |
---|---|---|---|---|
B. burgdorferi | B | Peptide designed from outer surface protein A (Osp)A | nn | [63] |
E. coli | B | RNA binding protein Hfq | Interaction with biological membranes, potentially export of RNA | [64] |
E. coli | B | MinE | Interaction with biological membranes, lipid redistribution | [65,66] |
E. coli | B | Hydrogenase maturation factor HypF (HypF-N) | Permeabilization of membranes | [67] |
Enterobacteriaceae | B | CsgB | Biofilm formation | [47,68] |
Gallibacterium anatis * | B | Elongation factor-Tu (EF-Tu) | Adhesion-like function | [69] |
Mannheimia haemolytica | B | Amyloid-like protein (ALP) | Cell adhesion, biofilm formation | [70] |
Mycobacterium tuberculosis | B | Early secreted antigen 6-kDa protein (ESAT-6) | Potentially pore-formation | [71,72] |
Pseudomonas aeruginosa | B | Functional Amyloid in Pseudomonas (Fap) C | Strengthening of biofilms | [73,74] |
S. aureus | B | Phenol soluble modulins (PSMs) | Resistance of biofilms to various dispersion agents | [75] |
S. aureus | B | N-terminal leader fragment of accessory gene regulatory (Agr) D | Seeding the amyloid polymerization of PSM peptides (in vitro) | [76] |
S. epidermidis | B | C-repeat of Biofilm associated protein (Bap) | Potentially bacteria-bacteria-adhesion | [77] |
C. albicans | F | Agglutinin-like sequence family 3 (Als3) | nn | [78] |
Saccharomyces cerevisiae | F | glucantransferase Bgl2 | Assumed cell protection against oxidative stress | [79] |
Avibirnavirus infectious bursal disease virus (IBDV) | V | Viral protease VP4 | Reduction of cytotoxicity of protease activity in host cells | [62] |
Coronavirus | V | Peptide C6 | nn | [80] |
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Endres, K. Amyloidogenic Peptides in Human Neuro-Degenerative Diseases and in Microorganisms: A Sorrow Shared Is a Sorrow Halved? Molecules 2020, 25, 925. https://doi.org/10.3390/molecules25040925
Endres K. Amyloidogenic Peptides in Human Neuro-Degenerative Diseases and in Microorganisms: A Sorrow Shared Is a Sorrow Halved? Molecules. 2020; 25(4):925. https://doi.org/10.3390/molecules25040925
Chicago/Turabian StyleEndres, Kristina. 2020. "Amyloidogenic Peptides in Human Neuro-Degenerative Diseases and in Microorganisms: A Sorrow Shared Is a Sorrow Halved?" Molecules 25, no. 4: 925. https://doi.org/10.3390/molecules25040925