Intrinsic blue-green fluorescence in amyloyd fibrils

Ivana Sirangelo; Margherita Borriello; Gaetano Irace; Clara Iannuzzi; Ivana Sirangelo; Margherita Borriello; Gaetano Irace; Clara Iannuzzi

doi:10.3934/biophy.2018.2.155

AIMS Biophysics

2018, Volume 5, Issue 2: 155-165. doi: 10.3934/biophy.2018.2.155

Previous Article Next Article

Review Special Issues

Intrinsic blue-green fluorescence in amyloyd fibrils

Department of Precision Medicine, Università degli Studi della Campania “Luigi Vanvitelli”, Via L. De Crecchio 7, 80132 Naples, Italy

Received: 10 May 2018 Accepted: 14 June 2018 Published: 22 June 2018

Proteins and polypeptides containing a high proportion of β-sheets have been recently reported to exhibit, in their amyloid aggregated states, an intrinsic fluorescence in the blue-green range of wavelength where the aromatic residues do not emit. Lately, growing attention has been devoted to the identification of a specific, structure-related fluorophore for the detection of amyloid aggregates due to their implications in the physio-pathology of neurodegenerative diseases and other aggregation-related diseases. Indeed, the appearance of blue-green fluorescence could be used as an alternative method for the investigation and the detection of the aggregation state without using external probes. Several hypotheses have been suggested to explain the molecular bases of this rather unusual intrinsic emission. In particular, it has been related to an expansion of the electronic delocalization of π-electrons of peptide bonds through the backbone-to-backbone hydrogen bonds connecting the β-sheets. Alternatively, the formation of the intrinsic chromophore has been associated to chemical modifications of the aromatic residues or arising from dipolar coupling between excited states of aromatic amino acids densely packed in the ﬁbril structures. More recently, it has been proposed that the blue-green amyloid fluorophore does not require neither the presence of aromatic residues nor multiple bond conjugation. In this study, we critically review the above hypotheses with particular attention to the electronic transitions responsible for the appearance of blue-green fluorescence in amyloid fibrils.
- amyloid aggregation,
- amyloid fibrils,
- cross-β structure,
- intrinsic blue-green fluorescence
Citation: Ivana Sirangelo, Margherita Borriello, Gaetano Irace, Clara Iannuzzi. Intrinsic blue-green fluorescence in amyloyd fibrils[J]. AIMS Biophysics, 2018, 5(2): 155-165. doi: 10.3934/biophy.2018.2.155

Related Papers:

Abstract

Proteins and polypeptides containing a high proportion of β-sheets have been recently reported to exhibit, in their amyloid aggregated states, an intrinsic fluorescence in the blue-green range of wavelength where the aromatic residues do not emit. Lately, growing attention has been devoted to the identification of a specific, structure-related fluorophore for the detection of amyloid aggregates due to their implications in the physio-pathology of neurodegenerative diseases and other aggregation-related diseases. Indeed, the appearance of blue-green fluorescence could be used as an alternative method for the investigation and the detection of the aggregation state without using external probes. Several hypotheses have been suggested to explain the molecular bases of this rather unusual intrinsic emission. In particular, it has been related to an expansion of the electronic delocalization of π-electrons of peptide bonds through the backbone-to-backbone hydrogen bonds connecting the β-sheets. Alternatively, the formation of the intrinsic chromophore has been associated to chemical modifications of the aromatic residues or arising from dipolar coupling between excited states of aromatic amino acids densely packed in the ﬁbril structures. More recently, it has been proposed that the blue-green amyloid fluorophore does not require neither the presence of aromatic residues nor multiple bond conjugation. In this study, we critically review the above hypotheses with particular attention to the electronic transitions responsible for the appearance of blue-green fluorescence in amyloid fibrils.

References

[1]	Cantor CR, Schimmel PR (1980) Techniques for the study of biological structure and function, Biophysical Chemistry, Part II, WH Freeman and Co.
[2]	Chen RF (1990) Fluorescence of proteins and peptides, In: Guilbault GG, Editor, Practical Fluorescence, Revised and Expanded, 2 Eds., Marcel Dekker, 576–682.
[3]	Lakowicz JR (2006) Protein fluorescence, In: Principles of fluorescence spectroscopy, Springer Science Business Media, 443–476.
[4]	Shukla A, Mukherjee S, Sharma S, et al. (2004) A novel UV laser-induced visible blue radiation from protein crystals and aggregates: Scattering artifacts or fluorescence transitions of peptide electrons delocalized through hydrogen bonding? Arch Biochem Biophys 428: 144–153. doi: 10.1016/j.abb.2004.05.007
[5]	Mercato LLD, Pompa PP, Maruccio G, et al. (2007) Charge transport and intrinsic fluorescence in amyloid-like fibrils. P Natl Acad Sci USA 104: 18019–18024.
[6]	Guptasarma P (2008) Solution-state characteristics of the ultraviolet A-induced visible fluorescence from proteins. Arch Biochem Biophys 478: 127–129. doi: 10.1016/j.abb.2008.08.002
[7]	Sharpe S, Simonetti K, Yau J, et al. (2011) Solid-state NMR characterization of autofluorescent fibrils formed by the elastin-derived peptide GVGVAGVG. Biomacromolecules 12: 1546–1555. doi: 10.1021/bm101486s
[8]	Chan FTS, Kaminski GS, Kumita JR, et al. (2013) Protein amyloids develop an intrinsic fluorescence signature during aggregation. Analyst 138: 2156–2162. doi: 10.1039/c3an36798c
[9]	Pinotsi D, Buell AK, Dobson CM, et al. (2013) A label-free, quantitative assay of amyloid fibril growth based on intrinsic fluorescence. Chembiochem 14: 846–850. doi: 10.1002/cbic.201300103
[10]	Giamblanco N, Coglitore D, Janot JM, et al. (2018) Detection of protein aggregate morphology through single antifouling nanopore. Sensor Actuat B-Chem 260: 736–745. doi: 10.1016/j.snb.2018.01.094
[11]	Pinotsi D, Schierle GSK, Kaminski CF (2016) Optical super-resolution imaging of β-amyloid aggregation in vitro and in vivo: Method and techniques. Methods Mol Biol 1303: 125–141. doi: 10.1007/978-1-4939-2627-5_6
[12]	Schierle GSK, Bertoncini CW, Chan FTS, et al. (2011) A FRET sensor for non-invasive imaging of amyloid formation in vivo. Chemphyschem 12: 673–680. doi: 10.1002/cphc.201000996
[13]	Hudson SA, Ecroyd H, Kee TW, et al. (2009) The thioflavin T fluorescence assay for amyloid fibril detection can be biased by the presence of exogenous compounds. FEBS J 276: 5960–5972. doi: 10.1111/j.1742-4658.2009.07307.x
[14]	Chiti F, Dobson CM (2017) Protein misfolding, amyloid formation, and human disease: A summary of progress over the last decade. Annu Rev Biochem 86: 27–68. doi: 10.1146/annurev-biochem-061516-045115
[15]	Chiti F, Dobson CM (2006) Protein misfolding, functional amyloid, and human disease. Annu Rev Biochem 75: 333–366. doi: 10.1146/annurev.biochem.75.101304.123901
[16]	Spadaccini R, Leone S, Rega MF, et al. (2016) Influence of pH on the structure and stability of the sweet protein MNEI. FEBS Lett 590: 3681–3689. doi: 10.1002/1873-3468.12437
[17]	Leone S, Picone D (2016) Molecular dynamics driven design of ph-stabilized mutants of MNEI, a sweet protein. PLoS One 11: e0158372. doi: 10.1371/journal.pone.0158372
[18]	Bouaziz Z, Soussan L, Janot JM, et al. (2017) Structure and antibacterial activity relationships of native and amyloid fibril lysozyme loaded on layered double hydroxide. Colloid Surface B 157: 10–17. doi: 10.1016/j.colsurfb.2017.05.050
[19]	Serpell LS (2000) Alzheimer's amyloid fibrils: Structure and assembly. BBA-Mol Basis Dis 1502: 16–30. doi: 10.1016/S0925-4439(00)00029-6
[20]	Makin OS, Serpell LC (2005) Structures for amyloid fibrils. FEBS J 272: 5950–5961. doi: 10.1111/j.1742-4658.2005.05025.x
[21]	Serpell LC, Sunde M, Benson MD, et al. (2000) The protofilament substructure of amyloid fibrils. J Mol Biol 300: 1033–1039. doi: 10.1006/jmbi.2000.3908
[22]	Fitzpatrick AW, Debelouchina GT, Bayro MJ, et al. (2013) Atomic structure and hierarchical assembly of a cross-β amyloid fibril. P Natl Acad Sci USA 110: 5468–5473. doi: 10.1073/pnas.1219476110
[23]	Lashuel HA, Hartley DM, Petre BM, et al. (2003) Mixtures of wild-type and a pathogenic (E22G) form of Abeta40 in vitro accumulate protofibrils, including amyloid pores. J Mol Biol 332: 795–808. doi: 10.1016/S0022-2836(03)00927-6
[24]	Lee CC, Nayak A, Sethuraman A, et al. (2007) A three-stage kinetic model of amyloid fibrillation. Biophys J 92: 3448–3458.
[25]	Iannuzzi C, Borriello M, Irace G, et al. (2017) Vanillin affects amyloid aggregation and non-enzymatic glycation in human insulin. Sci Rep 7: 15086. doi: 10.1038/s41598-017-15503-5
[26]	Levine H (1993) Thioflavine T interaction with synthetic Alzheimer's disease beta-amyloid peptides: Detection of amyloid aggregation in solution. Protein Sci 2: 404–410.
[27]	Iannuzzi C, Borriello M, Carafa V, et al. (2016) D-ribose-glycation of insulin prevents amyloid aggregation and produces cytotoxic adducts. BBA-Mol Basis Dis 1852: 93–104.
[28]	Tcherkasskaya O (2007) Photo-activity induced by amyloidogenesis. Protein Sci 16: 561–571. doi: 10.1110/ps.062578307
[29]	Hanczyc P, Samoc M, Norden B (2013) Multiphoton absorption in amyloid protein fibres. Nat Photonics 7: 969–972. doi: 10.1038/nphoton.2013.282
[30]	Anand U, Mukherjee M (2013) Exploring the self-assembly of a short aromatic Aβ (16–24) peptide. Langmuir 29: 2713–2721. doi: 10.1021/la304585a
[31]	Pinotsi D, Grisanti L, Mahou P, et al. (2016) Proton transfer and structure-specific fluorescence in hydrogen bond-rich protein structures. J Am Chem Soc 138: 3046–3057. doi: 10.1021/jacs.5b11012
[32]	Grisanti L, Pinotsi D, Gebauer R, et al. (2017) A computational study on how structure influences the optical properties in model crystal structures of amyloid fibrils. Phys Chem Chem Phys 19: 4030–4040. doi: 10.1039/C6CP07564A
[33]	Iannuzzi C, Borriello M, Portaccio M, et al. (2017) Insights into insulin fibril assembly at physiological and acidic pH and related amyloid intrinsic fluorescence. Int J Mol Sci 18: 2551.
[34]	Zou Y, Li Y, Hao W, et al. (2013) Parallel β-sheet fibril and antiparallel β-sheet oligomer: New insights into amyloid formation of hen egg white lysozyme under heat and acidic condition from FTIR spectroscopy. J Phys Chem B 117: 4003–4013. doi: 10.1021/jp4003559
[35]	Zou Y, Hao W, Li H, et al. (2014) New insight into amyloid fibril formation of hen egg white lysozyme using a two-step temperature-dependent FTIR approach. J Phys Chem B 118: 9834–9843. doi: 10.1021/jp504201k
[36]	Lührs T, Ritter C, Adrian M, et al. (2005) 3D structure of Alzheimer's amyloid-beta (1–42) fibrils. P Natl Acad Sci USA 102: 17342–17347.
[37]	Qiang W, Yau WM, Luo Y, et al. (2012) Antiparallel β-sheet architecture in Iowa-mutant β-amyloid fibrils. P Natl Acad Sci USA 109: 4443–4448. doi: 10.1073/pnas.1111305109
[38]	Yoshihara H, Saito J, Tanabe A, et al. (2016) Characterization of novel insulin fibrils that show strong cytotoxicity under physiological pH. J Pharm Sci 105: 1419–1426.
[39]	Luo Y, Ma B, Nussinov R, et al. (2014) Structural insight into tau protein's paradox of intrinsically disordered behavior, self-acetylation activity, and aggregation. J Phys Chem Lett 5: 3026–3031. doi: 10.1021/jz501457f
[40]	Ruxi Q, Yin L, Guanghong W, et al. (2015) Aβ "Stretching-and-Packing" cross-seeding mechanism can trigger tau protein aggregation. J Phys Chem Lett 6: 3276–3282. doi: 10.1021/acs.jpclett.5b01447
[41]	Sakakibara R, Hamaguchi K (1968) Structure of lysozyme: XIV. Acid-base titration of lysozyme. J Biochem 64: 613–618.

Reader Comments

Your name:*

Email:*
© 2018 the Author(s), licensee AIMS Press. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0)