1932

Abstract

The remarkable variety of microbial species of human pathogens and microbiomes generates significant quantities of secreted amyloids, which are structured protein fibrils that serve diverse functions related to virulence and interactions with the host. Human amyloids are associated largely with fatal neurodegenerative and systemic aggregation diseases, and current research has put forward the hypothesis that the interspecies amyloid interactome has physiological and pathological significance. Moreover, functional and molecular-level connections between antimicrobial activity and amyloid structures suggest a neuroimmune role for amyloids that are otherwise known to be pathological. Compared to the extensive structural information that has been accumulated for human amyloids, high-resolution structures of microbial and antimicrobial amyloids are only emerging. These recent structures reveal both similarities and surprising departures from the typical amyloid motif, in accordance with their diverse activities, and advance the discovery of novel antivirulence and antimicrobial agents. In addition, the structural information has led researchers to postulate that amyloidogenic sequences are natural targets for structural mimicry, for instance in host–microbe interactions. Microbial amyloid research could ultimately be used to fight aggressive infections and possibly processes leading to autoimmune and neurodegenerative diseases.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-biochem-032620-105157
2022-06-21
2024-10-08
Loading full text...

Full text loading...

/deliver/fulltext/biochem/91/1/annurev-biochem-032620-105157.html?itemId=/content/journals/10.1146/annurev-biochem-032620-105157&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Maji SK, Perrin MH, Sawaya MR, Jessberger S, Vadodaria K et al. 2009. Functional amyloids as natural storage of peptide hormones in pituitary secretory granules. Science 325:328–32
    [Google Scholar]
  2. 2.
    Soragni A, Yousefi S, Stoeckle C, Soriaga AB, Sawaya MR et al. 2015. Toxicity of eosinophil MBP is repressed by intracellular crystallization and promoted by extracellular aggregation. Mol. Cell 57:1011–21
    [Google Scholar]
  3. 3.
    Hewetson A, Do HQ, Myers C, Muthusubramanian A, Sutton RB et al. 2017. Functional amyloids in reproduction. Biomolecules 7:46
    [Google Scholar]
  4. 4.
    Fowler DM, Koulov AV, Alory-Jost C, Marks MS, Balch WE, Kelly JW 2006. Functional amyloid formation within mammalian tissue. PLOS Biol 4:e6
    [Google Scholar]
  5. 5.
    Kummer MP, Maruyama H, Huelsmann C, Baches S, Weggen S, Koo EH. 2009. Formation of Pmel17 amyloid is regulated by juxtamembrane metalloproteinase cleavage, and the resulting C-terminal fragment is a substrate for γ-secretase. J. Biol. Chem. 284:2296–306
    [Google Scholar]
  6. 6.
    Chapman MR, Robinson LS, Pinkner JS, Roth R, Heuser J et al. 2002. Role of Escherichia coli curli operons in directing amyloid fiber formation. Science 295:851–55
    [Google Scholar]
  7. 7.
    Schwartz K, Syed AK, Stephenson RE, Rickard AH, Boles BR. 2012. Functional amyloids composed of phenol soluble modulins stabilize Staphylococcus aureus biofilms. PLOS Pathog 8:e1002744
    [Google Scholar]
  8. 8.
    Gómez-Pérez D, Chaudhry V, Kemen A, Kemen E. 2021. Amyloid proteins in plant-associated microbial communities. Microb. Physiol. 31:88–98
    [Google Scholar]
  9. 9.
    Shanmugam N, Baker MODG, Ball SR, Steain M, Pham CLL, Sunde M. 2019. Microbial functional amyloids serve diverse purposes for structure, adhesion and defence. Biophys. Rev. 11:287–302
    [Google Scholar]
  10. 10.
    Levkovich SA, Gazit E, Laor Bar-Yosef D. 2021. Two decades of studying functional amyloids in microorganisms. Trends Microbiol 29:251–65
    [Google Scholar]
  11. 11.
    Varadi M, De Baets G, Vranken WF, Tompa P, Pancsa R. 2018. AmyPro: a database of proteins with validated amyloidogenic regions. Nucleic Acids Res 46:D387–92
    [Google Scholar]
  12. 12.
    Cegelski L, Marshall GR, Eldridge GR, Hultgren SJ. 2008. The biology and future prospects of antivirulence therapies. Nat. Rev. Microbiol. 6:17–27
    [Google Scholar]
  13. 13.
    Cegelski L, Pinkner JS, Hammer ND, Cusumano CK, Hung CS et al. 2009. Small-molecule inhibitors target Escherichia coli amyloid biogenesis and biofilm formation. Nat. Chem. Biol. 5:913–19
    [Google Scholar]
  14. 14.
    Prusiner SB. 1998. Prions. PNAS 95:13363–83
    [Google Scholar]
  15. 15.
    Jucker M, Walker LC. 2018. Propagation and spread of pathogenic protein assemblies in neurodegenerative diseases. Nat. Neurosci. 21:1341–49
    [Google Scholar]
  16. 16.
    Casalone C, Hope J. 2018. Atypical and classic bovine spongiform encephalopathy. Handb. Clin. Neurol. 153:121–34
    [Google Scholar]
  17. 17.
    Friedland RP. 2015. Mechanisms of molecular mimicry involving the microbiota in neurodegeneration. J. Alzheimers Dis. 45:349–62
    [Google Scholar]
  18. 18.
    Lin C, Zhao S, Zhu Y, Fan Z, Wang J et al. 2019. Microbiota-gut-brain axis and toll-like receptors in Alzheimer's disease. Comput. Struct. Biotechnol. J. 17:1309–17
    [Google Scholar]
  19. 19.
    Soscia SJ, Kirby JE, Washicosky KJ, Tucker SM, Ingelsson M et al. 2010. The Alzheimer's disease-associated amyloid β-protein is an antimicrobial peptide. PLOS ONE 5:e9505
    [Google Scholar]
  20. 20.
    Kumar DK, Choi SH, Washicosky KJ, Eimer WA, Tucker S et al. 2016. Amyloid-β peptide protects against microbial infection in mouse and worm models of Alzheimer's disease. Sci. Transl. Med. 8:340ra72
    [Google Scholar]
  21. 21.
    Park SC, Moon JC, Shin SY, Son H, Jung YJ et al. 2016. Functional characterization of alpha-synuclein protein with antimicrobial activity. Biochem. Biophys. Res. Commun. 478:924–28
    [Google Scholar]
  22. 22.
    Beatman EL, Massey A, Shives KD, Burrack KS, Chamanian M et al. 2015. Alpha-synuclein expression restricts RNA viral infections in the brain. J. Virol. 90:2767–82
    [Google Scholar]
  23. 23.
    Bourgade K, Garneau H, Giroux G, Le Page AY, Bocti C et al. 2015. β-Amyloid peptides display protective activity against the human Alzheimer's disease-associated herpes simplex virus-1. Biogerontology 16:85–98
    [Google Scholar]
  24. 24.
    Hirakura Y, Carreras I, Sipe JD, Kagan BL. 2002. Channel formation by serum amyloid A: a potential mechanism for amyloid pathogenesis and host defense. Amyloid 9:13–23
    [Google Scholar]
  25. 25.
    Last NB, Miranker AD. 2013. Common mechanism unites membrane poration by amyloid and antimicrobial peptides. PNAS 110:6382–87
    [Google Scholar]
  26. 26.
    Pasupuleti M, Roupe M, Rydengård V, Surewicz K, Surewicz WK et al. 2009. Antimicrobial activity of human prion protein is mediated by its N-terminal region. PLOS ONE 4:e7358
    [Google Scholar]
  27. 27.
    White MR, Kandel R, Tripathi S, Condon D, Qi L et al. 2014. Alzheimer's associated β-amyloid protein inhibits influenza A virus and modulates viral interactions with phagocytes. PLOS ONE 9:e101364
    [Google Scholar]
  28. 28.
    Kobayashi N, Masuda J, Kudoh J, Shimizu N, Yoshida T. 2008. Binding sites on tau proteins as components for antimicrobial peptides. Biocontrol. Sci. 13:49–56
    [Google Scholar]
  29. 29.
    Last NB, Rhoades E, Miranker AD. 2011. Islet amyloid polypeptide demonstrates a persistent capacity to disrupt membrane integrity. PNAS 108:9460–65
    [Google Scholar]
  30. 30.
    Pasupuleti M, Davoudi M, Malmsten M, Schmidtchen A. 2009. Antimicrobial activity of a C-terminal peptide from human extracellular superoxide dismutase. BMC Res. Notes 2:136
    [Google Scholar]
  31. 31.
    Chiou S-J, Ko H-J, Hwang C-C, Hong Y-R. 2021. The double-edged sword of Beta2-microglobulin in antibacterial properties and amyloid fibril-mediated cytotoxicity. Int. J. Mol. Sci. 22:6330
    [Google Scholar]
  32. 32.
    Moir RD, Lathe R, Tanzi RE. 2018. The antimicrobial protection hypothesis of Alzheimer's disease. Alzheimers Dement 14:1602–14
    [Google Scholar]
  33. 33.
    Gallardo R, Ranson NA, Radford SE. 2020. Amyloid structures: much more than just a cross-β fold. Curr. Opin. Struct. Biol. 60:7–16
    [Google Scholar]
  34. 34.
    Sunde M, Serpell LC, Bartlam M, Fraser PE, Pepys MB, Blake CC. 1997. Common core structure of amyloid fibrils by synchrotron X-ray diffraction. J. Mol. Biol. 273:729–39
    [Google Scholar]
  35. 35.
    Nelson R, Sawaya MR, Balbirnie M, Madsen , Riekel C et al. 2005. Structure of the cross-β spine of amyloid-like fibrils. Nature 435:773–78
    [Google Scholar]
  36. 36.
    Nelson R, Eisenberg D. 2006. Recent atomic models of amyloid fibril structure. Curr. Opin. Struct. Biol. 16:260–65
    [Google Scholar]
  37. 37.
    Van Melckebeke H, Wasmer C, Lange A, Ab E, Loquet A et al. 2010. Atomic-resolution three-dimensional structure of HET-s(218–289) amyloid fibrils by solid-state NMR spectroscopy. J. Am. Chem. Soc. 132:13765–75
    [Google Scholar]
  38. 38.
    Xiao Y, Ma B, McElheny D, Parthasarathy S, Long F et al. 2015. Aβ(1–42) fibril structure illuminates self-recognition and replication of amyloid in Alzheimer's disease. Nat. Struct. Mol. Biol. 22:499–505
    [Google Scholar]
  39. 39.
    Colvin MT, Silvers R, Ni QZ, Can TV, Sergeyev I et al. 2016. Atomic resolution structure of monomorphic Aβ42 amyloid fibrils. J. Am. Chem. Soc. 138:9663–74
    [Google Scholar]
  40. 40.
    Walti MA, Ravotti F, Arai H, Glabe CG, Wall JS et al. 2016. Atomic-resolution structure of a disease-relevant Aβ(1–42) amyloid fibril. PNAS 113:E4976–84
    [Google Scholar]
  41. 41.
    Qiang W, Yau WM, Lu JX, Collinge J, Tycko R. 2017. Structural variation in amyloid-β fibrils from Alzheimer's disease clinical subtypes. Nature 541:217–21
    [Google Scholar]
  42. 42.
    Murray DT, Kato M, Lin Y, Thurber KR, Hung I et al. 2017. Structure of FUS protein fibrils and its relevance to self-assembly and phase separation of low-complexity domains. Cell 171:615–27.e16
    [Google Scholar]
  43. 43.
    Rodriguez JA, Ivanova MI, Sawaya MR, Cascio D, Reyes FE et al. 2015. Structure of the toxic core of α-synuclein from invisible crystals. Nature 525:486–90
    [Google Scholar]
  44. 44.
    Schmidt M, Rohou A, Lasker K, Yadav JK, Schiene-Fischer C et al. 2015. Peptide dimer structure in an Aβ(1–42) fibril visualized with cryo-EM. PNAS 112:11858–63
    [Google Scholar]
  45. 45.
    Close W, Neumann M, Schmidt A, Hora M, Annamalai K et al. 2018. Physical basis of amyloid fibril polymorphism. Nat. Commun. 9:699
    [Google Scholar]
  46. 46.
    Iadanza MG, Silvers R, Boardman J, Smith HI, Karamanos TK et al. 2018. The structure of a β2-microglobulin fibril suggests a molecular basis for its amyloid polymorphism. Nat. Commun. 9:4517
    [Google Scholar]
  47. 47.
    Fitzpatrick AWP, Falcon B, He S, Murzin AG, Murshudov G et al. 2017. Cryo-EM structures of tau filaments from Alzheimer's disease. Nature 547:185–90
    [Google Scholar]
  48. 48.
    Guerrero-Ferreira R, Taylor NM, Mona D, Ringler P, Lauer ME et al. 2018. Cryo-EM structure of alpha-synuclein fibrils. eLife 7:e36402
    [Google Scholar]
  49. 49.
    Radamaker L, Lin Y-H, Annamalai K, Huhn S, Hegenbart U et al. 2019. Cryo-EM structure of a light chain-derived amyloid fibril from a patient with systemic AL amyloidosis. Nat. Commun. 10:1103
    [Google Scholar]
  50. 50.
    Li B, Ge P, Murray KA, Sheth P, Zhang M et al. 2018. Cryo-EM of full-length α-synuclein reveals fibril polymorphs with a common structural kernel. Nat. Commun. 9:3609
    [Google Scholar]
  51. 51.
    Li Y, Zhao C, Luo F, Liu Z, Gui X et al. 2018. Amyloid fibril structure of α-synuclein determined by cryo-electron microscopy. Cell Res 28:897–903
    [Google Scholar]
  52. 52.
    Ni X, McGlinchey RP, Jiang J, Lee JC. 2019. Structural insights into α-synuclein fibril polymorphism: effects of Parkinson's disease-related C-terminal truncations. J. Mol. Biol. 431:3913–19
    [Google Scholar]
  53. 53.
    Guerrero-Ferreira R, Taylor NM, Arteni A-A, Kumari P, Mona D et al. 2019. Two new polymorphic structures of human full-length alpha-synuclein fibrils solved by cryo-electron microscopy. eLife 8:e48907
    [Google Scholar]
  54. 54.
    Sun Y, Hou S, Zhao K, Long H, Liu Z et al. 2020. Cryo-EM structure of full-length α-synuclein amyloid fibril with Parkinson's disease familial A53T mutation. Cell Res 30:360–62
    [Google Scholar]
  55. 55.
    Boyer DR, Li B, Sun C, Fan W, Sawaya MR et al. 2019. Structures of fibrils formed by α-synuclein hereditary disease mutant H50Q reveal new polymorphs. Nat. Struct. Mol. Biol. 26:1044–52
    [Google Scholar]
  56. 56.
    Boyer DR, Li B, Sun C, Fan W, Zhou K et al. 2020. The α-synuclein hereditary mutation E46K unlocks a more stable, pathogenic fibril structure. PNAS 117:3592–602
    [Google Scholar]
  57. 57.
    Zhao K, Lim YJ, Liu Z, Long H, Sun Y et al. 2020. Parkinson's disease-related phosphorylation at Tyr39 rearranges α-synuclein amyloid fibril structure revealed by cryo-EM. PNAS 117:20305–15
    [Google Scholar]
  58. 58.
    Schweighauser M, Shi Y, Tarutani A, Kametani F, Murzin AG et al. 2020. Structures of α-synuclein filaments from multiple system atrophy. Nature 585:464–69
    [Google Scholar]
  59. 59.
    Falcon B, Zhang W, Murzin AG, Murshudov G, Garringer HJ et al. 2018. Structures of filaments from Pick's disease reveal a novel tau protein fold. Nature 561:137–40
    [Google Scholar]
  60. 60.
    Zhang W, Falcon B, Murzin AG, Fan J, Crowther RA et al. 2019. Heparin-induced tau filaments are polymorphic and differ from those in Alzheimer's and Pick's diseases. eLife 8:e43584
    [Google Scholar]
  61. 61.
    Falcon B, Zhang W, Schweighauser M, Murzin AG, Vidal R et al. 2018. Tau filaments from multiple cases of sporadic and inherited Alzheimer's disease adopt a common fold. Acta Neuropathol 136:699–708
    [Google Scholar]
  62. 62.
    Falcon B, Zivanov J, Zhang W, Murzin AG, Garringer HJ et al. 2019. Novel tau filament fold in chronic traumatic encephalopathy encloses hydrophobic molecules. Nature 568:420–23
    [Google Scholar]
  63. 63.
    Zhang W, Tarutani A, Newell KL, Murzin AG, Matsubara T et al. 2020. Novel tau filament fold in corticobasal degeneration. Nature 580:283–87
    [Google Scholar]
  64. 64.
    Arakhamia T, Lee CE, Carlomagno Y, Duong DM, Kundinger SR et al. 2020. Posttranslational modifications mediate the structural diversity of tauopathy strains. Cell 180:633–44.e12
    [Google Scholar]
  65. 65.
    Liberta F, Loerch S, Rennegarbe M, Schierhorn A, Westermark P et al. 2019. Cryo-EM fibril structures from systemic AA amyloidosis reveal the species complementarity of pathological amyloids. Nat. Commun. 10:1104
    [Google Scholar]
  66. 66.
    Swuec P, Lavatelli F, Tasaki M, Paissoni C, Rognoni P et al. 2019. Cryo-EM structure of cardiac amyloid fibrils from an immunoglobulin light chain AL amyloidosis patient. Nat. Commun. 10:1269
    [Google Scholar]
  67. 67.
    Schmidt M, Wiese S, Adak V, Engler J, Agarwal S et al. 2019. Cryo-EM structure of a transthyretin-derived amyloid fibril from a patient with hereditary ATTR amyloidosis. Nat. Commun. 10:5008
    [Google Scholar]
  68. 68.
    Kollmer M, Close W, Funk L, Rasmussen J, Bsoul A et al. 2019. Cryo-EM structure and polymorphism of Aβ amyloid fibrils purified from Alzheimer's brain tissue. Nat. Commun. 10:4760
    [Google Scholar]
  69. 69.
    Gremer L, Schölzel D, Schenk C, Reinartz E, Labahn J et al. 2017. Fibril structure of amyloid-β(1–42) by cryo-electron microscopy. Science 358:116–19
    [Google Scholar]
  70. 70.
    Röder C, Kupreichyk T, Gremer L, Schäfer LU, Pothula KR et al. 2020. Cryo-EM structure of islet amyloid polypeptide fibrils reveals similarities with amyloid-β fibrils. Nat. Struct. Mol. Biol. 27:660–67
    [Google Scholar]
  71. 71.
    Cao Q, Boyer DR, Sawaya MR, Ge P, Eisenberg DS. 2020. Cryo-EM structure and inhibitor design of human IAPP (amylin) fibrils. Nat. Struct. Mol. Biol. 27:653–59
    [Google Scholar]
  72. 72.
    Lu J, Cao Q, Hughes MP, Sawaya MR, Boyer DR et al. 2020. CryoEM structure of the low-complexity domain of hnRNPA2 and its conversion to pathogenic amyloid. Nat. Commun. 11:4090
    [Google Scholar]
  73. 73.
    Hervas R, Rau MJ, Park Y, Zhang W, Murzin AG et al. 2020. Cryo-EM structure of a neuronal functional amyloid implicated in memory persistence in Drosophila. Science 367:1230–34
    [Google Scholar]
  74. 74.
    Cao Q, Boyer DR, Sawaya MR, Ge P, Eisenberg DS. 2019. Cryo-EM structures of four polymorphic TDP-43 amyloid cores. Nat. Struct. Mol. Biol. 26:619–27
    [Google Scholar]
  75. 75.
    Guenther EL, Ge P, Trinh H, Sawaya MR, Cascio D et al. 2018. Atomic-level evidence for packing and positional amyloid polymorphism by segment from TDP-43 RRM2. Nat. Struct. Mol. Biol. 25:311–19
    [Google Scholar]
  76. 76.
    Lee M, Ghosh U, Thurber KR, Kato M, Tycko R. 2020. Molecular structure and interactions within amyloid-like fibrils formed by a low-complexity protein sequence from FUS. Nat. Commun. 11:5735
    [Google Scholar]
  77. 77.
    Seuring C, Verasdonck J, Gath J, Ghosh D, Nespovitaya N et al. 2020. The three-dimensional structure of human β-endorphin amyloid fibrils. Nat. Struct. Mol. Biol. 27:1178–84
    [Google Scholar]
  78. 78.
    Gopalswamy M, Kumar A, Adler J, Baumann M, Henze M et al. 2015. Structural characterization of amyloid fibrils from the human parathyroid hormone. Biochim. Biophys. Acta Proteins Proteom. 1854:249–57
    [Google Scholar]
  79. 79.
    Gelenter MD, Smith KJ, Liao S-Y, Mandala VS, Dregni AJ et al. 2019. The peptide hormone glucagon forms amyloid fibrils with two coexisting β-strand conformations. Nat. Struct. Mol. Biol. 26:592–98
    [Google Scholar]
  80. 80.
    Ragonis-Bachar P, Landau M. 2021. Functional and pathological amyloid structures in the eyes of 2020 cryo-EM. Curr. Opin. Struct. Biol. 68:184–93
    [Google Scholar]
  81. 81.
    Luo F, Gui X, Zhou H, Gu J, Li Y et al. 2018. Atomic structures of FUS LC domain segments reveal bases for reversible amyloid fibril formation. Nat. Struct. Mol. Biol. 25:341–46
    [Google Scholar]
  82. 82.
    Kato M, Han TW, Xie S, Shi K, Du X et al. 2012. Cell-free formation of RNA granules: Low complexity sequence domains form dynamic fibers within hydrogels. Cell 149:753–67
    [Google Scholar]
  83. 83.
    Hughes MP, Sawaya MR, Boyer DR, Goldschmidt L, Rodriguez JA et al. 2018. Atomic structures of low-complexity protein segments reveal kinked β sheets that assemble networks. Science 359:698–701
    [Google Scholar]
  84. 84.
    Salinas N, Povolotsky TL, Landau M, Kolodkin-Gal I. 2020. Emerging roles of functional bacterial amyloids in gene regulation, toxicity, and immunomodulation. Microbiol. Mol. Biol. Rev. 85:e00062–20
    [Google Scholar]
  85. 85.
    Tayeb-Fligelman E, Tabachnikov O, Moshe A, Goldshmidt-Tran O, Sawaya MR et al. 2017. The cytotoxic Staphylococcus aureus PSMα3 reveals a cross-α amyloid-like fibril. Science 355:831–33
    [Google Scholar]
  86. 86.
    Yao Z, Cary BP, Bingman CA, Wang C, Kreitler DF et al. 2019. Use of a stereochemical strategy to probe the mechanism of phenol-soluble modulin α3 toxicity. J. Am. Chem. Soc. 141:7660–64
    [Google Scholar]
  87. 87.
    Malishev R, Tayeb-Fligelman E, David S, Meijler MM, Landau M, Jelinek R. 2018. Reciprocal interactions between membrane bilayers and S. aureus PSMα3 cross-α amyloid fibrils account for species-specific cytotoxicity. J. Mol. Biol. 430:1431–41
    [Google Scholar]
  88. 88.
    Tayeb-Fligelman E, Salinas N, Tabachnikov O, Landau M. 2020. Staphylococcus aureus PSMα3 cross-α fibril polymorphism and determinants of cytotoxicity. Structure 28:301–13.e6
    [Google Scholar]
  89. 89.
    Salinas N, Colletier JP, Moshe A, Landau M 2018. Extreme amyloid polymorphism in Staphylococcus aureus virulent PSMα peptides. Nat. Commun. 9:3512
    [Google Scholar]
  90. 90.
    Zaman M, Andreasen M. 2020. Cross-talk between individual phenol-soluble modulins in Staphylococcus aureus biofilm enables rapid and efficient amyloid formation. eLife 9:e59776
    [Google Scholar]
  91. 91.
    Cracchiolo OM, Edun DN, Betti VM, Goldberg JM, Serrano AL. 2022. Cross-α/β polymorphism of PSMα3 fibrils. PNAS 119:e2114923119
    [Google Scholar]
  92. 92.
    Andreasen M, Meisl G, Taylor JD, Michaels TCT, Levin A et al. 2019. Physical determinants of amyloid assembly in biofilm formation. mBio 10:e02279–18
    [Google Scholar]
  93. 93.
    Shewmaker F, McGlinchey RP, Thurber KR, McPhie P, Dyda F et al. 2009. The functional curli amyloid is not based on in-register parallel β-sheet structure. J. Biol. Chem. 284:25065–76
    [Google Scholar]
  94. 94.
    Schubeis T, Yuan P, Ahmed M, Nagaraj M, vanRossum B-J, Ritter C. 2015. Untangling a repetitive amyloid sequence: correlating biofilm-derived and segmentally labeled curli fimbriae by solid-state NMR spectroscopy. Angew. Chem. Int. Ed. 54:14669–72
    [Google Scholar]
  95. 95.
    Perov S, Lidor O, Salinas N, Golan N, Tayeb-Fligelman E et al. 2019. structural insights into curli CsgA cross-β fibril architecture inspire repurposing of anti-amyloid compounds as anti-biofilm agents. PLOS Pathog 15:e1007978
    [Google Scholar]
  96. 96.
    Klein AN, Ziehm T, van Groen T, Kadish I, Elfgen A et al. 2017. Optimization of d-peptides for Aβ monomer binding specificity enhances their potential to eliminate toxic Aβ oligomers. ACS Chem. Neurosci. 8:1889–900
    [Google Scholar]
  97. 97.
    Golan N, Schwartz Perov S, Landau M, Lipke PN. 2021. Structure and conservation of amyloid spines from the Candida albicans Als5 adhesin including similarity to human LARKS. bioRxiv 2021.11.29.470514. https://doi.org/10.1101/2021.11.29.470514
    [Crossref]
  98. 98.
    Jang H, Arce FT, Mustata M, Ramachandran S, Capone R et al. 2011. Antimicrobial protegrin-1 forms amyloid-like fibrils with rapid kinetics suggesting a functional link. Biophys. J. 100:1775–83
    [Google Scholar]
  99. 99.
    Zhao H, Sood R, Jutila A, Bose S, Fimland G et al. 2006. Interaction of the antimicrobial peptide pheromone Plantaricin A with model membranes: implications for a novel mechanism of action. Biochim. Biophys. Acta Biomembr. 1758:1461–74
    [Google Scholar]
  100. 100.
    Auvynet C, El Amri C, Lacombe C, Bruston F, Bourdais J et al. 2008. Structural requirements for antimicrobial versus chemoattractant activities for dermaseptin S9. FEBS J 275:4134–51
    [Google Scholar]
  101. 101.
    Domanov YA, Kinnunen PK. 2006. Antimicrobial peptides temporins B and L induce formation of tubular lipid protrusions from supported phospholipid bilayers. Biophys. J. 91:4427–39
    [Google Scholar]
  102. 102.
    Salinas N, Tayeb-Fligelman E, Sammito MD, Bloch D, Jelinek R et al. 2021. The amphibian antimicrobial peptide uperin 3.5 is a cross-α/cross-β chameleon functional amyloid. PNAS 118:e2014442118
    [Google Scholar]
  103. 103.
    Wang L, Liu Q, Chen JC, Cui YX, Zhou B et al. 2012. Antimicrobial activity of human islet amyloid polypeptides: an insight into amyloid peptides' connection with antimicrobial peptides. Biol. Chem. 393:641–46
    [Google Scholar]
  104. 104.
    Gour S, Kumar V, Singh A, Gadhave K, Goyal P et al. 2019. Mammalian antimicrobial peptide protegrin-4 self assembles and forms amyloid-like aggregates: assessment of its functional relevance. J. Pept. Sci. 25:e3151
    [Google Scholar]
  105. 105.
    Wang CK, King GJ, Conibear AC, Ramos MC, Chaousis S et al. 2016. Mirror images of antimicrobial peptides provide reflections on their functions and amyloidogenic properties. J. Am. Chem. Soc. 138:5706–13
    [Google Scholar]
  106. 106.
    Simonson AW, Aronson MR, Medina SH. 2020. Supramolecular peptide assemblies as antimicrobial scaffolds. Molecules 25:2751
    [Google Scholar]
  107. 107.
    Torrent M, Pulido D, Nogués MV, Boix E. 2012. Exploring new biological functions of amyloids: bacteria cell agglutination mediated by host protein aggregation. PLOS Pathog 8:e1003005
    [Google Scholar]
  108. 108.
    Lee EY, Srinivasan Y, de Anda J, Nicastro LK, Tükel Ç, Wong GCL. 2020. Functional reciprocity of amyloids and antimicrobial peptides: rethinking the role of supramolecular assembly in host defense, immune activation, and inflammation. Front. Immunol. 11:1629
    [Google Scholar]
  109. 109.
    Schwartz K, Ganesan M, Payne DE, Solomon MJ, Boles BR. 2016. Extracellular DNA facilitates the formation of functional amyloids in Staphylococcus aureus biofilms. Mol. Microbiol. 99:123–34
    [Google Scholar]
  110. 110.
    Mao X, Li K, Liu M, Wang X, Zhao T et al. 2019. Directing curli polymerization with DNA origami nucleators. Nat. Commun. 10:1395
    [Google Scholar]
  111. 111.
    Spaulding CN, Dodson KW, Chapman MR, Hultgren SJ. 2015. Fueling the fire with fibers: Bacterial amyloids promote inflammatory disorders. Cell Host Microbe 18:1–2
    [Google Scholar]
  112. 112.
    Kampers T, Friedhoff P, Biernat J, Mandelkow E-M, Mandelkow E. 1996. RNA stimulates aggregation of microtubule-associated protein tau into Alzheimer-like paired helical filaments. FEBS Lett 399:344–49
    [Google Scholar]
  113. 113.
    Biragyn A, Ruffini PA, Leifer CA, Klyushnenkova E, Shakhov A et al. 2002. Toll-like receptor 4-dependent activation of dendritic cells by β-defensin 2. Science 298:1025–29
    [Google Scholar]
  114. 114.
    Landau M. 2018. Mimicking cross-α amyloids. Nat. Chem. Biol. 14:833–34
    [Google Scholar]
  115. 115.
    Rumpret M, von Richthofen HJ, van der Linden M, Westerlaken GHA, Talavera Ormeño C et al. 2021. Signal inhibitory receptor on leukocytes-1 recognizes bacterial and endogenous amphipathic α-helical peptides. FASEB J. 35:e21875
    [Google Scholar]
  116. 116.
    Landreh M, Johansson J, Jornvall H. 2014. Separate molecular determinants in amyloidogenic and antimicrobial peptides. J. Mol. Biol. 426:2159–66
    [Google Scholar]
  117. 117.
    Ghosh D, Singh PK, Sahay S, Jha NN, Jacob RS et al. 2015. Structure based aggregation studies reveal the presence of helix-rich intermediate during α-Synuclein aggregation. Sci. Rep. 5:9228
    [Google Scholar]
  118. 118.
    Hayouka Z, Thomas NC, Mortenson DE, Satyshur KA, Weisblum B et al. 2015. Quasiracemate crystal structures of magainin 2 derivatives support the functional significance of the phenylalanine zipper motif. J. Am. Chem. Soc. 137:11884–87
    [Google Scholar]
  119. 119.
    Bücker R, Seuring C, Cazey C, Veith K, García-Alai M. 2022. The cryo-EM structures of two amphibian antimicrobial cross-β amyloid fibrils. bioRxiv 2022.01.08.475498. https://doi.org/10.1101/2022.01.08.475498
    [Crossref]
  120. 120.
    Stefani M. 2012. Structural features and cytotoxicity of amyloid oligomers: implications in Alzheimer's disease and other diseases with amyloid deposits. Prog. Neurobiol. 99:226–45
    [Google Scholar]
  121. 121.
    Burton MF, Steel PG. 2009. The chemistry and biology of LL-37. Nat. Prod. Rep. 26:1572–84
    [Google Scholar]
  122. 122.
    Epand RF, Wang G, Berno B, Epand RM. 2009. Lipid segregation explains selective toxicity of a series of fragments derived from the human cathelicidin LL-37. Antimicrob. Agents Chemother. 53:3705–14
    [Google Scholar]
  123. 123.
    Engelberg Y, Landau M. 2020. The Human LL-37(17–29) antimicrobial peptide reveals a functional supramolecular structure. Nat. Commun. 11:3894
    [Google Scholar]
  124. 124.
    Rajasekaran G, Kim EY, Shin SY. 2017. LL-37-derived membrane-active FK-13 analogs possessing cell selectivity, anti-biofilm activity and synergy with chloramphenicol and anti-inflammatory activity. Biochim. Biophys. Acta Biomembr. 1859:722–33
    [Google Scholar]
  125. 125.
    Sharon G, Sampson TR, Geschwind DH, Mazmanian SK. 2016. The central nervous system and the gut microbiome. Cell 167:915–32
    [Google Scholar]
  126. 126.
    Miller AL, Bessho S, Grando K, Tükel Ç. 2021. Microbiome or infections: amyloid-containing biofilms as a trigger for complex human diseases. Front. Immunol. 12:638867
    [Google Scholar]
  127. 127.
    Endres K. 2020. Amyloidogenic peptides in human neuro-degenerative diseases and in microorganisms: A sorrow shared is a sorrow halved?. Molecules 25:925
    [Google Scholar]
  128. 128.
    Blacher E, Bashiardes S, Shapiro H, Rothschild D, Mor U et al. 2019. Potential roles of gut microbiome and metabolites in modulating ALS in mice. Nature 572:474–80
    [Google Scholar]
  129. 129.
    Vogt NM, Kerby RL, Dill-McFarland KA, Harding SJ, Merluzzi AP et al. 2017. Gut microbiome alterations in Alzheimer's disease. Sci. Rep. 7:13537
    [Google Scholar]
  130. 130.
    Cattaneo A, Cattane N, Galluzzi S, Provasi S, Lopizzo N et al. 2017. Association of brain amyloidosis with pro-inflammatory gut bacterial taxa and peripheral inflammation markers in cognitively impaired elderly. Neurobiol. Aging 49:60–68
    [Google Scholar]
  131. 131.
    Qian Y, Yang X, Xu S, Wu C, Qin N et al. 2018. Detection of microbial 16S rRNA gene in the blood of patients with Parkinson's disease. Front. Aging Neurosci. 10:156
    [Google Scholar]
  132. 132.
    Bedarf JR, Hildebrand F, Coelho LP, Sunagawa S, Bahram M et al. 2017. Functional implications of microbial and viral gut metagenome changes in early stage L-DOPA-naive Parkinson's disease patients. Genome Med 9:39
    [Google Scholar]
  133. 133.
    Harach T, Marungruang N, Duthilleul N, Cheatham V, McCoy KD et al. 2017. Reduction of Abeta amyloid pathology in APPPS1 transgenic mice in the absence of gut microbiota. Sci. Rep. 7:41802
    [Google Scholar]
  134. 134.
    Daulatzai MA. 2014. Chronic functional bowel syndrome enhances gut-brain axis dysfunction, neuroinflammation, cognitive impairment, and vulnerability to dementia. Neurochem. Res. 39:624–44
    [Google Scholar]
  135. 135.
    Joachim CL, Mori H, Selkoe DJ. 1989. Amyloid β-protein deposition in tissues other than brain in Alzheimer's disease. Nature 341:226–30
    [Google Scholar]
  136. 136.
    Liu B, Fang F, Pedersen NL, Tillander A, Ludvigsson JF et al. 2017. Vagotomy and Parkinson disease: a Swedish register-based matched-cohort study. Neurology 88:1996–2002
    [Google Scholar]
  137. 137.
    Iked K, Akiyama H, Kondo H, Arai T, Arai N, Yagishita S. 1995. Numerous glial fibrillary tangles in oligodendroglia in cases of subacute sclerosing panencephalitis with neurofibrillary tangles. Neurosci. Lett. 194:133–35
    [Google Scholar]
  138. 138.
    de Beer FC, Nel AE, Gie RP, Donald PR, Strachan AF. 1984. Serum amyloid A protein and C-reactive protein levels in pulmonary tuberculosis: relationship to amyloidosis. Thorax 39:196–200
    [Google Scholar]
  139. 139.
    Wangel AG, Wegelius O, Dyrting AE. 1982. A family study of leprosy: subcutaneous amyloid deposits and humoral immune responses. Int. J. Lepr. Other Mycobact. Dis. 50:47–55
    [Google Scholar]
  140. 140.
    Rathore N, Ramani SR, Pantua H, Payandeh J, Bhangale T et al. 2018. Paired immunoglobulin-like type 2 receptor alpha G78R variant alters ligand binding and confers protection to Alzheimer's disease. PLOS Genet 14:e1007427
    [Google Scholar]
  141. 141.
    Hur JY, Frost GR, Wu X, Crump C, Pan SJ et al. 2020. The innate immunity protein IFITM3 modulates γ-secretase in Alzheimer's disease. Nature 586:735–40
    [Google Scholar]
  142. 142.
    Rautenberg M, Joo HS, Otto M, Peschel A. 2011. Neutrophil responses to staphylococcal pathogens and commensals via the formyl peptide receptor 2 relates to phenol-soluble modulin release and virulence. FASEB J 25:1254–63
    [Google Scholar]
  143. 143.
    Le Y, Gong W, Tiffany HL, Tumanov A, Nedospasov S et al. 2001. Amyloid β42 activates a G-protein-coupled chemoattractant receptor, FPR-like-1. J. Neurosci. 21:RC123
    [Google Scholar]
  144. 144.
    Liang TS, Wang JM, Murphy PM, Gao JL. 2000. Serum amyloid A is a chemotactic agonist at FPR2, a low-affinity N-formylpeptide receptor on mouse neutrophils. Biochem. Biophys. Res. Commun. 270:331–35
    [Google Scholar]
  145. 145.
    Tukel C, Wilson RP, Nishimori JH, Pezeshki M, Chromy BA, Baumler AJ. 2009. Responses to amyloids of microbial and host origin are mediated through Toll-like receptor 2. Cell Host Microbe 6:45–53
    [Google Scholar]
  146. 146.
    Tursi SA, Lee EY, Medeiros NJ, Lee MH, Nicastro LK et al. 2017. Bacterial amyloid curli acts as a carrier for DNA to elicit an autoimmune response via TLR2 and TLR9. PLOS Pathog 13:e1006315
    [Google Scholar]
  147. 147.
    Hughes C, Choi ML, Yi J-H, Kim S-C, Drews A et al. 2020. Beta amyloid aggregates induce sensitised TLR4 signalling causing long-term potentiation deficit and rat neuronal cell death. Commun. Biol. 3:79
    [Google Scholar]
  148. 148.
    McGeer PL, McGeer EG. 2002. Local neuroinflammation and the progression of Alzheimer's disease. J. Neurovirol. 8:529–38
    [Google Scholar]
  149. 149.
    Iribarren P, Zhou Y, Hu J, Le Y, Wang JM. 2005. Role of formyl peptide receptor-like 1 (FPRL1/FPR2) in mononuclear phagocyte responses in Alzheimer disease. Immunol. Res. 31:165–76
    [Google Scholar]
  150. 150.
    Friedland RP, McMillan JD, Kurlawala Z. 2020. What are the molecular mechanisms by which functional bacterial amyloids influence amyloid beta deposition and neuroinflammation in neurodegenerative disorders?. Int. J. Mol. Sci. 21:1652
    [Google Scholar]
  151. 151.
    Miklossy J, McGeer PL. 2016. Common mechanisms involved in Alzheimer's disease and type 2 diabetes: a key role of chronic bacterial infection and inflammation. Aging 8:575–88
    [Google Scholar]
  152. 152.
    Harris SA, Harris EA. 2015. Herpes simplex virus type 1 and other pathogens are key causative factors in sporadic Alzheimer's disease. J. Alzheimers Dis. 48:319–53
    [Google Scholar]
  153. 153.
    Jamieson GA, Maitland NJ, Wilcock GK, Craske J, Itzhaki RF. 1991. Latent herpes simplex virus type 1 in normal and Alzheimer's disease brains. J. Med. Virol. 33:224–27
    [Google Scholar]
  154. 154.
    Sequiera LW, Jennings LC, Carrasco LH, Lord MA, Curry A, Sutton RN. 1979. Detection of herpes-simplex viral genome in brain tissue. Lancet 2:609–12
    [Google Scholar]
  155. 155.
    MacDonald AB, Miranda JM. 1987. Concurrent neocortical borreliosis and Alzheimer's disease. Hum. Pathol. 18:759–61
    [Google Scholar]
  156. 156.
    Balin BJ, Gerard HC, Arking EJ, Appelt DM, Branigan PJ et al. 1998. Identification and localization of Chlamydia pneumoniae in the Alzheimer's brain. Med. Microbiol. Immunol. 187:23–42
    [Google Scholar]
  157. 157.
    Little CS, Hammond CJ, MacIntyre A, Balin BJ, Appelt DM. 2004. Chlamydia pneumoniae induces Alzheimer-like amyloid plaques in brains of BALB/c mice. Neurobiol. Aging 25:419–29
    [Google Scholar]
  158. 158.
    Pritchard AB, Crean S, Olsen I, Singhrao SK. 2017. Periodontitis, microbiomes and their role in Alzheimer's disease. Front. Aging Neurosci. 9:336
    [Google Scholar]
  159. 159.
    Chen SG, Stribinskis V, Rane MJ, Demuth DR, Gozal E et al. 2016. Exposure to the functional bacterial amyloid protein curli enhances alpha-synuclein aggregation in aged Fischer 344 rats and Caenorhabditis elegans. Sci. Rep. 6:34477
    [Google Scholar]
  160. 160.
    Friedland RP, Chapman MR. 2017. The role of microbial amyloid in neurodegeneration. PLOS Pathog 13:e1006654
    [Google Scholar]
  161. 161.
    Liu Y, Wu Z, Nakanishi Y, Ni J, Hayashi Y et al. 2017. Infection of microglia with Porphyromonas gingivalis promotes cell migration and an inflammatory response through the gingipain-mediated activation of protease-activated receptor-2 in mice. Sci. Rep. 7:11759
    [Google Scholar]
  162. 162.
    Hill JM, Lukiw WJ. 2015. Microbial-generated amyloids and Alzheimer's disease (AD). Front. . Aging Neurosci 7:9
    [Google Scholar]
  163. 163.
    Sikorska B, Liberski PP, Sobów T, Budka H, Ironside JW. 2009. Ultrastructural study of florid plaques in variant Creutzfeldt-Jakob disease: a comparison with amyloid plaques in kuru, sporadic Creutzfeldt-Jakob disease and Gerstmann-Sträussler-Scheinker disease. Neuropathol. Appl. Neurobiol. 35:46–59
    [Google Scholar]
  164. 164.
    Oli MW, Otoo HN, Crowley PJ, Heim KP, Nascimento MM et al. 2012. Functional amyloid formation by Streptococcus mutans. Microbiology 158:2903–16
    [Google Scholar]
  165. 165.
    Bokranz W, Wang X, Tschape H, Romling U. 2005. Expression of cellulose and curli fimbriae by Escherichia coli isolated from the gastrointestinal tract. J. Med. Microbiol. 54:1171–82
    [Google Scholar]
  166. 166.
    Solomon A, Richey T, Murphy CL, Weiss DT, Wall JS et al. 2007. Amyloidogenic potential of foie gras. PNAS 104:10998–1001
    [Google Scholar]
  167. 167.
    Xing Y, Nakamura A, Chiba T, Kogishi K, Matsushita T et al. 2001. Transmission of mouse senile amyloidosis. Lab. Invest. 81:493–99
    [Google Scholar]
  168. 168.
    Lundmark K, Westermark GT, Olsen A, Westermark P. 2005. Protein fibrils in nature can enhance amyloid protein A amyloidosis in mice: cross-seeding as a disease mechanism. PNAS 102:6098–102
    [Google Scholar]
  169. 169.
    Abbott A. 2020. Are infections seeding some cases of Alzheimer's disease?. Nature 587:22–25
    [Google Scholar]
  170. 170.
    Allnutt MA, Johnson K, Bennett DA, Connor SM, Troncoso JC et al. 2020. Human herpesvirus 6 detection in Alzheimer's disease cases and controls across multiple cohorts. Neuron 105:1027–35.e2
    [Google Scholar]
  171. 171.
    Readhead B, Haure-Mirande JV, Funk CC, Richards MA, Shannon P et al. 2018. Multiscale analysis of independent Alzheimer's cohorts finds disruption of molecular, genetic, and clinical networks by human herpesvirus. Neuron 99:64–82.e7
    [Google Scholar]
  172. 172.
    Cui D, Kawano H, Hoshii Y, Liu Y, Ishihara T. 2008. Acceleration of murine AA amyloid deposition by bovine amyloid fibrils and tissue homogenates. Amyloid 15:77–83
    [Google Scholar]
  173. 173.
    Miglio A, Moscati L, Fruganti G, Pela M, Scoccia E et al. 2013. Use of milk amyloid A in the diagnosis of subclinical mastitis in dairy ewes. J. Dairy Res. 80:496–502
    [Google Scholar]
  174. 174.
    Villar-Pique A, Sabate R, Lopera O, Gibert J, Torne JM et al. 2010. Amyloid-like protein inclusions in tobacco transgenic plants. PLOS ONE 5:e13625
    [Google Scholar]
  175. 175.
    Friedland RP, Tedesco JM, Wilson AC, Atwood CS, Smith MA et al. 2008. Antibodies to potato virus Y bind the amyloid β peptide: immunohistochemical and NMR studies. J. Biol. Chem. 283:22550–56
    [Google Scholar]
  176. 176.
    Zur Hausen H, Bund T, de Villiers EM. 2017. Infectious agents in bovine red meat and milk and their potential role in cancer and other chronic diseases. Curr. Top. Microbiol. Immunol. 407:83–116
    [Google Scholar]
  177. 177.
    Kilic T, Popov AN, Burk-Körner A, Koromyslova A, Zur Hausen H et al. 2019. Structural analysis of a replication protein encoded by a plasmid isolated from a multiple sclerosis patient. Acta Crystallogr. D Struct. Biol. 75:498–504
    [Google Scholar]
  178. 178.
    de Villiers EM, Gunst K, Chakraborty D, Ernst C, Bund T, Zur Hausen H. 2019. A specific class of infectious agents isolated from bovine serum and dairy products and peritumoral colon cancer tissue. Emerg. Microbes Infect. 8:1205–18
    [Google Scholar]
  179. 179.
    Bund T, Nikitina E, Chakraborty D, Ernst C, Gunst K et al. 2021. Analysis of chronic inflammatory lesions of the colon for BMMF Rep antigen expression and CD68 macrophage interactions. PNAS 118:e2025830118
    [Google Scholar]
  180. 180.
    Revilla-García A, Fernández C, Moreno-Del Álamo M, de Los Ríos V, Vorberg IM, Giraldo R 2020. Intercellular transmission of a synthetic bacterial cytotoxic prion-like protein in mammalian cells. mBio 11:e02937–19
    [Google Scholar]
  181. 181.
    Zhou Y, Smith D, Leong BJ, Brannstrom K, Almqvist F, Chapman MR. 2012. Promiscuous cross-seeding between bacterial amyloids promotes interspecies biofilms. J. Biol. Chem. 287:35092–103
    [Google Scholar]
  182. 182.
    Javed I, Zhang Z, Adamcik J, Andrikopoulos N, Li Y et al. 2020. Accelerated amyloid beta pathogenesis by bacterial amyloid FapC. Adv. Sci. 7:2001299
    [Google Scholar]
  183. 183.
    Hartman K, Brender JR, Monde K, Ono A, Evans ML et al. 2013. Bacterial curli protein promotes the conversion of PAP248–286 into the amyloid SEVI: cross-seeding of dissimilar amyloid sequences. PeerJ 1:e5
    [Google Scholar]
  184. 184.
    Sampson TR, Challis C, Jain N, Moiseyenko A, Ladinsky MS et al. 2020. A gut bacterial amyloid promotes α-synuclein aggregation and motor impairment in mice. eLife 9:e53111
    [Google Scholar]
  185. 185.
    Alonso R, Pisa D, Marina AI, Morato E, Rabano A, Carrasco L. 2014. Fungal infection in patients with Alzheimer's disease. J. Alzheimers Dis. 41:301–11
    [Google Scholar]
  186. 186.
    Klotz SA, Sobonya RE, Lipke PN, Garcia-Sherman MC. 2016. Serum amyloid P component and systemic fungal infection: Does it protect the host or is it a Trojan horse?. Open Forum Infect. Dis. 3:ofw166
    [Google Scholar]
  187. 187.
    Otoo HN, Lee KG, Qiu W, Lipke PN. 2008. Candida albicans Als adhesins have conserved amyloid-forming sequences. Eukaryot. Cell 7:776–82
    [Google Scholar]
  188. 188.
    Jain N, Aden J, Nagamatsu K, Evans ML, Li X et al. 2017. Inhibition of curli assembly and Escherichia coli biofilm formation by the human systemic amyloid precursor transthyretin. PNAS 114:12184–89
    [Google Scholar]
  189. 189.
    Rey NL, Wesson DW, Brundina P. 2018. The olfactory bulb as the entry site for prion-like propagation in neurodegenerative diseases. Neurobiol. Dis. 109:226–48
    [Google Scholar]
  190. 190.
    Ghosh U, Yau WM, Tycko R. 2018. Coexisting order and disorder within a common 40-residue amyloid-β fibril structure in Alzheimer's disease brain tissue. Chem. Commun. 54:5070–73
    [Google Scholar]
  191. 191.
    Anfinsen CB. 1973. Principles that govern the folding of protein chains. Science 181:223–30
    [Google Scholar]
  192. 192.
    Rout SK, Friedmann MP, Riek R, Greenwald J. 2018. A prebiotic template-directed peptide synthesis based on amyloids. Nat. Commun. 9:234
    [Google Scholar]
  193. 193.
    Goddard TD, Huang CC, Ferrin TE 2007. Visualizing density maps with UCSF Chimera. J. Struct. Biol 157:28187
    [Google Scholar]
/content/journals/10.1146/annurev-biochem-032620-105157
Loading
/content/journals/10.1146/annurev-biochem-032620-105157
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error