Prion-based nanomaterials and their emerging applications

ABSTRACT Protein misfolding and aggregation into highly ordered fibrillar structures have been traditionally associated with pathological processes. Nevertheless, nature has taken advantage of the particular properties of amyloids for functional purposes, like in the protection of organisms against environmental changing conditions. Over the last decades, these fibrillar structures have inspired the design of new nanomaterials with intriguing applications in biomedicine and nanotechnology such as tissue engineering, drug delivery, adhesive materials, biodegradable nanocomposites, nanowires or biosensors. Prion and prion-like proteins, which are considered a subclass of amyloids, are becoming ideal candidates for the design of new and tunable nanomaterials. In this review, we discuss the particular properties of this kind of proteins, and the current advances on the design of new materials based on prion sequences.

[1]  Anne-Kathrin Born,et al.  Amyloid‐Hydroxyapatite Bone Biomimetic Composites , 2014, Advanced materials.

[2]  Sarah Perrett,et al.  Self-Assembly of Amyloid Fibrils That Display Active Enzymes , 2014, ChemCatChem.

[3]  M. P. Hughes,et al.  Atomic structures of low-complexity protein segments reveal kinked β sheets that assemble networks , 2018, Science.

[4]  Zhiqiang Su,et al.  Self-assembling peptide and protein amyloids: from structure to tailored function in nanotechnology. , 2017, Chemical Society reviews.

[5]  Dong Men,et al.  Seeding-induced self-assembling protein nanowires dramatically increase the sensitivity of immunoassays. , 2009, Nano letters.

[6]  C. Dobson,et al.  Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases , 2002, Nature.

[7]  A. Sánchez de Merás,et al.  Energy interactions in amyloid-like fibrils from NNQQNY. , 2014, Physical chemistry chemical physics : PCCP.

[8]  T. Lu,et al.  Strong underwater adhesives made by self-assembling multi-protein nanofibres. , 2014, Nature nanotechnology.

[9]  G. Vriend,et al.  Amyloids protect the silkmoth oocyte and embryo , 2000, FEBS letters.

[10]  R. Wickner,et al.  Prion-Inducing Domain of Yeast Ure2p and Protease Resistance of Ure2p in Prion-Containing Cells , 1995, Science.

[11]  Jonathan S. Weissman,et al.  The physical basis of how prion conformations determine strain phenotypes , 2006, Nature.

[12]  T. Cech,et al.  RNA seeds higher-order assembly of FUS protein. , 2013, Cell reports.

[13]  W. K. Cullen,et al.  Naturally secreted oligomers of amyloid β protein potently inhibit hippocampal long-term potentiation in vivo , 2002, Nature.

[14]  Meital Reches,et al.  Casting Metal Nanowires Within Discrete Self-Assembled Peptide Nanotubes , 2003, Science.

[15]  Alexander K. Buell,et al.  Opposed Effects of Dityrosine Formation in Soluble and Aggregated α-Synuclein on Fibril Growth , 2017, Journal of molecular biology.

[16]  Markus J Buehler,et al.  Nanomechanics of functional and pathological amyloid materials. , 2011, Nature nanotechnology.

[17]  S. Perrett,et al.  The Yeast Prion Protein Ure2 Shows Glutathione Peroxidase Activity in Both Native and Fibrillar Forms* , 2004, Journal of Biological Chemistry.

[18]  L. Domigan,et al.  Versatile multi-functionalization of protein nanofibrils for biosensor applications. , 2014, Nanoscale.

[19]  H. Jaeger,et al.  Conducting nanowires built by controlled self-assembly of amyloid fibers and selective metal deposition , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[20]  O. Inganäs,et al.  White light with phosphorescent protein fibrils in OLEDs. , 2010, Nano letters.

[21]  S. Ventura,et al.  The Transcription Terminator Rho: A First Bacterial Prion. , 2017, Trends in microbiology.

[22]  Susan Lindquist,et al.  Prions as protein-based genetic elements. , 2002, Annual review of microbiology.

[23]  C. Dobson,et al.  Enzymatically Active Microgels from Self-Assembling Protein Nanofibrils for Microflow Chemistry , 2015, ACS nano.

[24]  Benjamin P. Partlow,et al.  Dityrosine Cross-Linking in Designing Biomaterials. , 2016, ACS biomaterials science & engineering.

[25]  Sunghak Park,et al.  Tyrosine-mediated two-dimensional peptide assembly and its role as a bio-inspired catalytic scaffold , 2014, Nature Communications.

[26]  W. Kay,et al.  Salmonella enteritidis agfBAC operon encoding thin, aggregative fimbriae , 1996, Journal of bacteriology.

[27]  Michael Holzinger,et al.  A synthetic redox biofilm made from metalloprotein-prion domain chimera nanowires. , 2017, Nature chemistry.

[28]  Brian D. Slaughter,et al.  Critical Role of Amyloid-like Oligomers of Drosophila Orb2 in the Persistence of Memory , 2012, Cell.

[29]  Robert A. Grothe,et al.  Structure of the cross-β spine of amyloid-like fibrils , 2005, Nature.

[30]  W. Alves,et al.  L-diphenylalanine microtubes as a potential drug-delivery system: characterization, release kinetics, and cytotoxicity. , 2013, Langmuir : the ACS journal of surfaces and colloids.

[31]  J. Schymkowitz,et al.  Amyloids or prions? That is the question , 2015, Prion.

[32]  U. Şeker,et al.  Self-assembly of bacterial amyloid protein nanomaterials on solid surfaces. , 2018, Journal of colloid and interface science.

[33]  Atanas V Koulov,et al.  Functional Amyloid Formation within Mammalian Tissue , 2005, PLoS biology.

[34]  Yan Liu,et al.  Diverse Supramolecular Nanofiber Networks Assembled by Functional Low-Complexity Domains. , 2017, ACS nano.

[35]  D. Otzen,et al.  Functional bacterial amyloid increases Pseudomonas biofilm hydrophobicity and stiffness , 2015, Front. Microbiol..

[36]  Eric D Ross,et al.  Primary sequence independence for prion formation. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[37]  K. Sakaguchi,et al.  Patterning nanofibrils through the templated growth of multiple modified amyloid peptides , 2016, Scientific Reports.

[38]  Zhongjie Zhang,et al.  Biofunctionalized self-assembly of peptide amphiphile induces the differentiation of bone marrow mesenchymal stem cells into neural cells , 2018, Molecular and Cellular Biochemistry.

[39]  S. Ventura,et al.  Minimalist Prion-Inspired Polar Self-Assembling Peptides. , 2018, ACS nano.

[40]  L. Bi,et al.  An auto-biotinylated bifunctional protein nanowire for ultra-sensitive molecular biosensing. , 2010, Biosensors & bioelectronics.

[41]  Scott J. Hultgren,et al.  Role of Escherichia coli Curli Operons in Directing Amyloid Fiber Formation , 2002, Science.

[42]  Bruce L. Miller,et al.  Ubiquitinated TDP-43 in Frontotemporal Lobar Degeneration and Amyotrophic Lateral Sclerosis , 2006, Science.

[43]  R. Wickner,et al.  Yeast Prions: Structure, Biology, and Prion-Handling Systems , 2015, Microbiology and Molecular Reviews.

[44]  I. Tolstorukov,et al.  Divergence and conservation of SUP2(SUP35) gene of yeasts Pichia pinus and Saccharomyces cerevisiae , 1990, Yeast.

[45]  Xiaochen Wu,et al.  Amyloid-graphene oxide as immobilization platform of Au nanocatalysts and enzymes for improved glucose-sensing activity. , 2017, Journal of colloid and interface science.

[46]  Tuomas P J Knowles,et al.  Amyloid Fibrils as Building Blocks for Natural and Artificial Functional Materials , 2016, Advanced materials.

[47]  C. Soto,et al.  Prion-like characteristics of the bacterial protein Microcin E492 , 2017, Scientific Reports.

[48]  R. Wickner,et al.  [URE3] as an altered URE2 protein: evidence for a prion analog in Saccharomyces cerevisiae. , 1994, Science.

[49]  Kausik Si.  Prions: what are they good for? , 2015, Annual review of cell and developmental biology.

[50]  Xueming Li,et al.  Atomic structures of FUS LC domain segments reveal bases for reversible amyloid fibril formation , 2018, Nature Structural & Molecular Biology.

[51]  O. King,et al.  A Systematic Survey Identifies Prions and Illuminates Sequence Features of Prionogenic Proteins , 2009, Cell.

[52]  R. Mezzenga,et al.  Hybrid Nanocomposites of Gold Single‐Crystal Platelets and Amyloid Fibrils with Tunable Fluorescence, Conductivity, and Sensing Properties , 2013, Advanced materials.

[53]  S. Lindquist,et al.  Heritable Remodeling of Yeast Multicellularity by an Environmentally Responsive Prion , 2013, Cell.

[54]  S. Lindquist,et al.  The yeast prion [PSI+]: molecular insights and functional consequences. , 2001, Advances in protein chemistry.

[55]  Jozef Adamcik,et al.  Biodegradable nanocomposites of amyloid fibrils and graphene with shape-memory and enzyme-sensing properties. , 2012, Nature nanotechnology.

[56]  R. Pappu,et al.  Phase separation of a yeast prion protein promotes cellular fitness , 2018, Science.

[57]  Gregory A. Newby,et al.  Luminidependens (LD) is an Arabidopsis protein with prion behavior , 2016, Proceedings of the National Academy of Sciences.

[58]  A. Gitler,et al.  Molecular Determinants and Genetic Modifiers of Aggregation and Toxicity for the ALS Disease Protein FUS/TLS , 2011, PLoS biology.

[59]  James A. Toombs,et al.  Compositional Determinants of Prion Formation in Yeast , 2009, Molecular and Cellular Biology.

[60]  Asa Ben-Hur,et al.  De novo design of synthetic prion domains , 2012, Proceedings of the National Academy of Sciences.

[61]  Imaging hydrogen peroxide in Alzheimer’s disease via cascade signal amplification , 2016, Scientific reports.

[62]  Jimin Pei,et al.  Cell-free Formation of RNA Granules: Low Complexity Sequence Domains Form Dynamic Fibers within Hydrogels , 2012, Cell.

[63]  S. Prusiner,et al.  Molecular biology of prion diseases , 1991, Science.

[64]  Haijing Yu,et al.  Newly identified prion linked to the chromatin-remodeling factor Swi1 in Saccharomyces cerevisiae , 2008, Nature Genetics.

[65]  Eric R. Kandel,et al.  The Persistence of Hippocampal-Based Memory Requires Protein Synthesis Mediated by the Prion-like Protein CPEB3 , 2015, Neuron.

[66]  E. Kandel,et al.  A Neuronal Isoform of the Aplysia CPEB Has Prion-Like Properties , 2003, Cell.

[67]  A. Esteras-Chopo,et al.  Hacking the Code of Amyloid Formation , 2007, Prion.

[68]  Joost Schymkowitz,et al.  What Makes a Protein Sequence a Prion? , 2015, PLoS Comput. Biol..