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Protein Nanofibrils as Storage Forms of Peptide Drugs and Hormones

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Biological and Bio-inspired Nanomaterials

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1174))

Abstract

Amyloids are highly organized cross β-sheet protein nanofibrils that are associated with both diseases and functions. Thermodynamically amyloids are stable structures as they represent the lowest free energy state that proteins can attain. However, recent studies suggest that amyloid fibrils can be dissociated by a change in environmental parameters such as pH and ionic strength. This reversibility of amyloids can not only be associated with disease, but function as well. In disease-associated amyloids, fibrils can act as reservoirs of cytotoxic oligomers. Recently, in higher organisms such as mammals, hormones were found to be stored in amyloid-like state, where these were reported to act as a reservoir of functional monomers. These hormone amyloids can dissociate to monomers upon release from the secretory granules, and subsequently bind to their respective receptors and perform their functions. In this book chapter, we describe in detail how these protein nanofibrils represent the densest possible peptide packing and are suitable for long-term storage. Thus, mimicking the feature of amyloids to release functional monomers, it is possible to formulate amyloid-based peptide/protein drugs, which can be used for sustained release.

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References

  1. Jeremy M, Berg JLT, Stryer L (2002) Biochemistry, 5th edn. W H Freeman, New York

    Google Scholar 

  2. Dobson CM (2004) Principles of protein folding, misfolding and aggregation. Semin Cell Dev Biol 15(1):3–16

    Article  CAS  PubMed  Google Scholar 

  3. Kirschner M, Mitchison T (1986) Beyond self-assembly: from microtubules to morphogenesis. Cell 45(3):329–342

    Article  CAS  PubMed  Google Scholar 

  4. Fletcher DA, Mullins RD (2010) Cell mechanics and the cytoskeleton. Nature 463(7280):485–492

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Chiti F, Dobson CM (2006) Protein misfolding, functional amyloid, and human disease. Annu Rev Biochem 75:333–366

    Article  CAS  PubMed  Google Scholar 

  6. Sunde M, Blake C (1997) The structure of amyloid fibrils by electron microscopy and X-ray diffraction. Adv Protein Chem 50:123–159

    Article  CAS  PubMed  Google Scholar 

  7. 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(3):729–739

    Article  CAS  PubMed  Google Scholar 

  8. LeVine H III (1993) Thioflavine T interaction with synthetic Alzheimer’s disease β-amyloid peptides: detection of amyloid aggregation in solution. Protein Sci 2:404–410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Westermark GT, Johnson KH, Westermark P (1999) Staining methods for identification of amyloid in tissue. Methods Enzymol 309:3–25

    Article  CAS  PubMed  Google Scholar 

  10. Meersman F, Dobson CM (2006) Probing the pressure-temperature stability of amyloid fibrils provides new insights into their molecular properties. Biochim Biophys Acta 1764(3):452–460

    Article  CAS  PubMed  Google Scholar 

  11. Mesquida P, Riener CK, MacPhee CE, McKendry RA (2007) Morphology and mechanical stability of amyloid-like peptide fibrils. J Mater Sci Mater Med 18(7):1325–1331

    Article  CAS  PubMed  Google Scholar 

  12. Zurdo J, Guijarro JI, Dobson CM (2001) Preparation and characterization of purified amyloid fibrils. J Am Chem Soc 123(33):8141–8142

    Article  CAS  PubMed  Google Scholar 

  13. Uversky VN, Fink AL (2004) Conformational constraints for amyloid fibrillation: the importance of being unfolded. Biochim Biophys Acta 1698(2):131–153

    Article  CAS  PubMed  Google Scholar 

  14. Haass C, Selkoe DJ (2007) Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer’s amyloid beta-peptide. Nat Rev Mol Cell Biol 8(2):101–112

    Article  CAS  PubMed  Google Scholar 

  15. Kayed R, Head E, Thompson JL, McIntire TM, Milton SC, Cotman CW, Glabe CG (2003) Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300(5618):486–489

    Article  CAS  PubMed  Google Scholar 

  16. Bucciantini M, Giannoni E, Chiti F, Baroni F, Formigli L, Zurdo J, Taddei N, Ramponi G, Dobson CM, Stefani M (2002) Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases. Nature 416(6880):507–511

    Article  CAS  PubMed  Google Scholar 

  17. Walsh DM, Klyubin I, Fadeeva JV, Cullen WK, Anwyl R, Wolfe MS, Rowan MJ, Selkoe DJ (2002) Naturally secreted oligomers of amyloid β protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416(6880):535–539

    Article  CAS  PubMed  Google Scholar 

  18. Harper JD, Lansbury PT Jr (1997) Models of amyloid seeding in Alzheimer’s disease and scrapie: mechanistic truths and physiological consequences of the time-dependent solubility of amyloid proteins. Annu Rev Biochem 66:385–407

    Article  CAS  PubMed  Google Scholar 

  19. Jarrett JT, Lansbury PT Jr (1993) Seeding “one-dimensional crystallization” of amyloid: a pathogenic mechanism in Alzheimer’s disease and scrapie? Cell 73:1055–1058

    Article  CAS  PubMed  Google Scholar 

  20. Ferrone F (1999) Analysis of protein aggregation kinetics. Methods Enzymol 309:256–274

    Article  CAS  PubMed  Google Scholar 

  21. Naiki H, Hashimoto N, Suzuki S, Kimura H, Nakakuki K, Gejyo F (1997) Establishment of a kinetic model of dialysis-related amyloid fibril extension in vitro. Amyl Int J Exp Clin Investig 4(4):223–232

    CAS  Google Scholar 

  22. Serio TR, Cashikar AG, Kowal AS, Sawicki GJ, Moslehi JJ, Serpell L, Arnsdorf MF, Lindquist SL (2000) Nucleated conformational conversion and the replication of conformational information by a prion determinant. Science 289(5483):1317–1321

    Article  CAS  PubMed  Google Scholar 

  23. Wright CF, Teichmann SA, Clarke J, Dobson CM (2005) The importance of sequence diversity in the aggregation and evolution of proteins. Nature 438(7069):878–881

    Article  CAS  PubMed  Google Scholar 

  24. Wetzel R (2006) Kinetics and thermodynamics of amyloid fibril assembly. Acc Chem Res 39(9):671–679

    Article  CAS  PubMed  Google Scholar 

  25. Knowles TPJ, Vendruscolo M, Dobson CM (2014) The amyloid state and its association with protein misfolding diseases. Nat Rev Mol Cell Biol 15(6):384–396

    Article  CAS  PubMed  Google Scholar 

  26. Maji SK, Perrin MH, Sawaya MR, Jessberger S, Vadodaria K, Rissman RA, Singru PS, Nilsson KP, Simon R, Schubert D, Eisenberg D, Rivier J, Sawchenko P, Vale W, Riek R (2009) Functional amyloids as natural storage of peptide hormones in pituitary secretory granules. Science 325(5938):328–332

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Maji SK, Schubert D, Rivier C, Lee S, Rivier JE, Riek R (2008) Amyloid as a depot for the formulation of long-acting drugs. PLoS Biol 6(2):e17

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. MacPhee CE, Dobson CM (2000) Chemical dissection and reassembly of amyloid fibrils formed by a peptide fragment of transthyretin. J Mol Biol 297(5):1203–1215

    Article  CAS  PubMed  Google Scholar 

  29. Carulla N, Caddy GL, Hall DR, Zurdo J, Gairi M, Feliz M, Giralt E, Robinson CV, Dobson CM (2005) Molecular recycling within amyloid fibrils. Nature 436(7050):554–558

    Article  CAS  PubMed  Google Scholar 

  30. Tipping KW, Karamanos TK, Jakhria T, Iadanza MG, Goodchild SC, Tuma R, Ranson NA, Hewitt EW, Radford SE (2015) pH-induced molecular shedding drives the formation of amyloid fibril-derived oligomers. Proc Natl Acad Sci U S A 112(18):5691–5696

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Cremades N, Cohen SI, Deas E, Abramov AY, Chen AY, Orte A, Sandal M, Clarke RW, Dunne P, Aprile FA, Bertoncini CW, Wood NW, Knowles TP, Dobson CM, Klenerman D (2012) Direct observation of the interconversion of normal and toxic forms of α-synuclein. Cell 149(5):1048–1059

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Fowler DM, Koulov AV, Balch WE, Kelly JW (2007) Functional amyloid – from bacteria to humans. Trends Biochem Sci 32(5):217–224

    Article  CAS  PubMed  Google Scholar 

  33. Chapman MR, Robinson LS, Pinkner JS, Roth R, Heuser J, Hammar M, Normark S, Hultgren SJ (2002) Role of Escherichia coli curli operons in directing amyloid fiber formation. Science 295(5556):851–855

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Otzen D, Nielsen PH (2008) We find them here, we find them there: functional bacterial amyloid. Cell Mol Life Sci 65(6):910–927

    Article  CAS  PubMed  Google Scholar 

  35. Hall-Stoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2(2):95–108

    Article  CAS  PubMed  Google Scholar 

  36. Oh J, Kim JG, Jeon E, Yoo CH, Moon JS, Rhee S, Hwang I (2007) Amyloidogenesis of type III-dependent harpins from plant pathogenic bacteria. J Biol Chem 282(18):13601–13609

    Article  CAS  PubMed  Google Scholar 

  37. Alteri CJ, Xicohtencatl-Cortes J, Hess S, Caballero-Olin G, Giron JA, Friedman RL (2007) Mycobacterium tuberculosis produces pili during human infection. Proc Natl Acad Sci U S A 104(12):5145–5150

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Gebbink MF, Claessen D, Bouma B, Dijkhuizen L, Wosten HA (2005) Amyloids – a functional coat for microorganisms. Nat Rev Microbiol 3(4):333–341

    Article  CAS  PubMed  Google Scholar 

  39. Talbot NJ (2003) Aerial morphogenesis: enter the chaplins. Curr Biol 13(18):R696–R698

    Article  CAS  PubMed  Google Scholar 

  40. Ramsook CB, Tan C, Garcia MC, Fung R, Soybelman G, Henry R, Litewka A, O’Meally S, Otoo HN, Khalaf RA, Dranginis AM, Gaur NK, Klotz SA, Rauceo JM, Jue CK, Lipke PN (2010) Yeast cell adhesion molecules have functional amyloid-forming sequences. Eukaryot Cell 9(3):393–404

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Hammer ND, Wang X, McGuffie BA, Chapman MR (2008) Amyloids: friend or foe? J Alzheimers Dis 13(4):407–419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Osherovich LZ, Weissman JS (2002) The utility of prions. Dev Cell 2(2):143–151

    Article  CAS  PubMed  Google Scholar 

  43. True HL, Lindquist SL (2000) A yeast prion provides a mechanism for genetic variation and phenotypic diversity. Nature 407(6803):477–483

    Article  CAS  PubMed  Google Scholar 

  44. Uptain SM, Lindquist S (2002) Prions as protein-based genetic elements. Annu Rev Microbiol 56:703–741

    Article  CAS  PubMed  Google Scholar 

  45. Chien P, Weissman JS, DePace AH (2004) Emerging principles of conformation-based prion inheritance. Annu Rev Biochem 73:617–656

    Article  CAS  PubMed  Google Scholar 

  46. Iconomidou VA, Vriend G, Hamodrakas SJ (2000) Amyloids protect the silkmoth oocyte and embryo. FEBS Lett 479(3):141–145

    Article  CAS  PubMed  Google Scholar 

  47. Fowler DM, Koulov AV, Alory-Jost C, Marks MS, Balch WE, Kelly JW (2006) Functional amyloid formation within mammalian tissue. PLoS Biol 4(1):100–107

    CAS  Google Scholar 

  48. Cherny I, Gazit E (2008) Amyloids: not only pathological agents but also ordered nanomaterials. Angew Chem Int Ed Engl 47(22):4062–4069

    Article  CAS  PubMed  Google Scholar 

  49. Knowles TP, Mezzenga R (2016) Amyloid fibrils as building blocks for natural and artificial functional materials. Adv Mater 28(31):6546–6561

    Article  CAS  PubMed  Google Scholar 

  50. Palade G (1975) Intracellular aspects of the process of protein synthesis. Science 189(4200):347–358

    Article  CAS  PubMed  Google Scholar 

  51. Lacy PE (1975) Endocrine secretory mechanisms. A review. Am J Pathol 79(1):170–188

    CAS  PubMed  PubMed Central  Google Scholar 

  52. Tooze SA (1998) Biogenesis of secretory granules in the trans-Golgi network of neuroendocrine and endocrine cells. Biochim Biophys Acta 1404(1–2):231–244

    Article  CAS  PubMed  Google Scholar 

  53. Arvan P, Castle D (1998) Sorting and storage during secretory granule biogenesis: looking backward and looking forward. Biochem J 332(Pt 3):593–610

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Kelly RB (1985) Pathways of protein secretion in eukaryotes. Science 230(4721):25–32

    Article  CAS  PubMed  Google Scholar 

  55. Kelly RB (1987) Protein transport. from organelle to organelle. Nature 326(6108):14–15

    Article  CAS  PubMed  Google Scholar 

  56. Stefan Y, Meda P, Neufeld M, Orci L (1987) Stimulation of insulin secretion reveals heterogeneity of pancreatic B cells in vivo. J Clin Invest 80(1):175–183

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Loh YP, Kim T, Rodriguez YM, Cawley NX (2004) Secretory granule biogenesis and neuropeptide sorting to the regulated secretory pathway in neuroendocrine cells. J Mol Neurosci 22(1–2):63–71

    Article  PubMed  Google Scholar 

  58. Hide I, Bennett JP, Pizzey A, Boonen G, Bar-Sagi D, Gomperts BD, Tatham PE (1993) Degranulation of individual mast cells in response to Ca2+ and guanine nucleotides: an all-or-none event. J Cell Biol 123(3):585–593

    Article  CAS  PubMed  Google Scholar 

  59. Turner MD, Rennison ME, Handel SE, Wilde CJ, Burgoyne RD (1992) Proteins are secreted by both constitutive and regulated secretory pathways in lactating mouse mammary epithelial cells. J Cell Biol 117(2):269–278

    Article  CAS  PubMed  Google Scholar 

  60. Kim T, Gondre-Lewis MC, Arnaoutova I, Loh YP (2006) Dense-core secretory granule biogenesis. Physiology (Bethesda) 21:124–133

    CAS  Google Scholar 

  61. Tooze SA (1991) Biogenesis of secretory granules. Implications arising from the immature secretory granule in the regulated pathway of secretion. FEBS Lett 285(2):220–224

    Article  CAS  PubMed  Google Scholar 

  62. Wu MM, Grabe M, Adams S, Tsien RY, Moore HP, Machen TE (2001) Mechanisms of pH regulation in the regulated secretory pathway. J Biol Chem 276(35):33027–33035

    Article  CAS  PubMed  Google Scholar 

  63. Steiner DF, Smeekens SP, Ohagi S, Chan SJ (1992) The new enzymology of precursor processing endoproteases. J Biol Chem 267(33):23435–23438

    CAS  PubMed  Google Scholar 

  64. Kuliawat R, Prabakaran D, Arvan P (2000) Proinsulin endoproteolysis confers enhanced targeting of processed insulin to the regulated secretory pathway. Mol Biol Cell 11(6):1959–1972

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Dannies PS (2002) Mechanisms for storage of prolactin and growth hormone in secretory granules. Mol Genet Metab 76(1):6–13

    Article  CAS  PubMed  Google Scholar 

  66. Giannattasio G, Zanini A, Meldolesi J (1975) Molecular organization of rat prolactin granules. I. In vitro stability of intact and “membraneless” granules. J Cell Biol 64(1):246–251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Morvan J, Tooze SA (2008) Discovery and progress in our understanding of the regulated secretory pathway in neuroendocrine cells. Histochem Cell Biol 129(3):243–252

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Dannies P (2003) Manipulating the reversible aggregation of protein hormones in secretory granules: potential impact on biopharmaceutical development. BioDrugs 17(5):315–324

    Article  CAS  PubMed  Google Scholar 

  69. Dannies PS (1999) Protein hormone storage in secretory granules: mechanisms for concentration and sorting. Endocr Rev 20(1):3–21

    CAS  PubMed  Google Scholar 

  70. Dannies PS (2001) Concentrating hormones into secretory granules: layers of control. Mol Cell Endocrinol 177(1–2):87–93

    Article  CAS  PubMed  Google Scholar 

  71. Maji SK, Riek R (2010) Formation of secretory granules involves the amyloid structure. In: Rigacci S, Bucciantini M (eds) Functional amyloid aggregation. Kerala, Research Signpost, pp 135–155

    Google Scholar 

  72. Hutton JC (1982) The internal pH and membrane potential of the insulin-secretory granule. Biochem J 204(1):171–178

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Orci L, Ravazzola M, Amherdt M, Madsen O, Perrelet A, Vassalli JD, Anderson RG (1986) Conversion of proinsulin to insulin occurs coordinately with acidification of maturing secretory vesicles. J Cell Biol 103(6 Pt 1):2273–2281

    Article  CAS  PubMed  Google Scholar 

  74. Urbe S, Tooze SA, Barr FA (1997) Formation of secretory vesicles in the biosynthetic pathway. Biochim Biophys Acta 1358(1):6–22

    Article  CAS  PubMed  Google Scholar 

  75. Huttner WB, Natori S (1995) Regulated secretion. Helper proteins for neuroendocrine secretion. Curr Biol 5(3):242–245

    Article  CAS  PubMed  Google Scholar 

  76. Kolset SO, Prydz K, Pejler G (2004) Intracellular proteoglycans. Biochem J 379(Pt 2):217–227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Miller F, de Harven E, Palade GE (1966) The structure of eosinophil leukocyte granules in rodents and in man. J Cell Biol 31:349–362

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Howell SL, Fink CJ, Lacy PE (1969) Isolation and properties of secretory granules from rat islets of Langerhans: I. Isolation of a secretory granule fraction. J Cell Biol 41(1):154–161

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. van Grondelle W, Iglesias CL, Coll E, Artzner F, Paternostre M, Lacombe F, Cardus M, Martinez G, Montes M, Cherif-Cheikh R, Valery C (2007) Spontaneous fibrillation of the native neuropeptide hormone Somatostatin-14. J Struct Biol 160(2):211–223

    Article  PubMed  CAS  Google Scholar 

  80. Keeler C, Hodsdon ME, Dannies PS (2004) Is there structural specificity in the reversible protein aggregates that are stored in secretory granules? J Mol Neurosci 22(1–2):43–49

    Article  PubMed  Google Scholar 

  81. Arvan P, Zhang BY, Feng L, Liu M, Kuliawat R (2002) Lumenal protein multimerization in the distal secretory pathway/secretory granules. Curr Opin Cell Biol 14(4):448–453

    Article  CAS  PubMed  Google Scholar 

  82. Howell SL, Young DA, Lacy PE (1969) Isolation and properties of secretory granules from rat islets of Langerhans. 3. Studies of the stability of the isolated beta granules. J Cell Biol 41(1):167–176

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Jacob RS, Das S, Ghosh S, Anoop A, Jha NN, Khan T, Singru P, Kumar A, Maji SK (2016) Amyloid formation of growth hormone in presence of zinc: relevance to its storage in secretory granules. Sci Rep 6:23370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Dannies PS (2012) Prolactin and growth hormone aggregates in secretory granules: the need to understand the structure of the aggregate. Endocr Rev 33(2):254–270

    Article  CAS  PubMed  Google Scholar 

  85. Gellermann GP, Appel TR, Tannert A, Radestock A, Hortschansky P, Schroeckh V, Leisner C, Lütkepohl T, Shtrasburg S, Röcken C, Pras M, Linke RP, Diekmann S, Fändrich M (2005) Raft lipids as common components of human extracellular amyloid fibrils. Proc Natl Acad Sci U S A 102(18):6297–6302

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Perry EK, Oakley AE, Candy JM, Perry RH (1981) Properties and possible significance of substance P and insulin fibrils. Neurosci Lett 25(3):321–325

    Article  CAS  PubMed  Google Scholar 

  87. Nespovitaya N, Gath J, Barylyuk K, Seuring C, Meier BH, Riek R (2016) Dynamic assembly and disassembly of functional β-endorphin amyloid fibrils. J Am Chem Soc 138(3):846–856

    Article  CAS  PubMed  Google Scholar 

  88. Zhu YL, Conway-Campbell B, Waters MJ, Dannies PS (2002) Prolonged retention after aggregation into secretory granules of human R183H-growth hormone (GH), a mutant that causes autosomal dominant GH deficiency type II. Endocrinology 143(11):4243–4248

    Article  CAS  PubMed  Google Scholar 

  89. Deladoey J, Gex G, Vuissoz JM, Strasburger CJ, Wajnrajch MP, Mullis PE (2002) Effect of different growth hormone (GH) mutants on the regulation of GH-receptor gene transcription in a human hepatoma cell line. Eur J Endocrinol 146(4):573–581

    Article  CAS  PubMed  Google Scholar 

  90. Deladoey J, Stocker P, Mullis PE (2001) Autosomal dominant GH deficiency due to an Arg183His GH-1 gene mutation: clinical and molecular evidence of impaired regulated GH secretion. J Clin Endocrinol Metab 86(8):3941–3947

    Article  CAS  PubMed  Google Scholar 

  91. Anoop A, Ranganathan S, Das Dhaked B, Jha NN, Pratihar S, Ghosh S, Sahay S, Kumar S, Das S, Kombrabail M, Agarwal K, Jacob RS, Singru P, Bhaumik P, Padinhateeri R, Kumar A, Maji SK (2014) Elucidating the role of disulfide bond on amyloid formation and fibril reversibility of somatostatin-14: relevance to its storage and secretion. J Biol Chem 289(24):16884–16903

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Sambashivan S, Liu Y, Sawaya MR, Gingery M, Eisenberg D (2005) Amyloid-like fibrils of ribonuclease A with three-dimensional domain-swapped and native-like structure. Nature 437(7056):266–269

    Article  CAS  PubMed  Google Scholar 

  93. Ivanova MI, Sawaya MR, Gingery M, Attinger A, Eisenberg D (2004) An amyloid-forming segment of β2-microglobulin suggests a molecular model for the fibril. Proc Natl Acad Sci U S A 101(29):10584–10589

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Baglioni S, Casamenti F, Bucciantini M, Luheshi LM, Taddei N, Chiti F, Dobson CM, Stefani M (2006) Prefibrillar amyloid aggregates could be generic toxins in higher organisms. J Neurosci 26(31):8160–8167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Jha NN, Anoop A, Ranganathan S, Mohite GM, Padinhateeri R, Maji SK (2013) Characterization of amyloid formation by glucagon-like peptides: role of basic residues in heparin-mediated aggregation. Biochemistry 52(49):8800–8810

    Article  CAS  PubMed  Google Scholar 

  96. Christensen LF, Malmos KG, Christiansen G, Otzen DE (2016) A complex dance: the importance of glycosaminoglycans and zinc in the aggregation of human prolactin. Biochemistry 55(26):3674–3684

    Article  CAS  PubMed  Google Scholar 

  97. Langer R (2001) Drug delivery. Drugs on target. Science 293(5527):58–59

    Article  CAS  PubMed  Google Scholar 

  98. Orive G, Hernandez RM, Rodriguez Gascon A, Dominguez-Gil A, Pedraz JL (2003) Drug delivery in biotechnology: present and future. Curr Opin Biotechnol 14(6):659–664

    Article  CAS  PubMed  Google Scholar 

  99. Brader ML, Sukumar M, Pekar AH, McClellan DS, Chance RE, Flora DB, Cox AL, Irwin L, Myers SR (2002) Hybrid insulin cocrystals for controlled release delivery. Nat Biotechnol 20(8):800–804

    Article  CAS  PubMed  Google Scholar 

  100. Jen A, Madorin K, Vosbeck K, Arvinte T, Merkle HP (2002) Transforming growth factor β-3 crystals as reservoirs for slow release of active TGF-β3. J Control Release 78(1–3):25–34

    Article  CAS  PubMed  Google Scholar 

  101. Tennent GA, Lovat LB, Pepys MB (1995) Serum amyloid P component prevents proteolysis of the amyloid fibrils of Alzheimer disease and systemic amyloidosis. Proc Natl Acad Sci U S A 92(10):4299–4303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Suk JY, Zhang F, Balch WE, Linhardt RJ, Kelly JW (2006) Heparin accelerates gelsolin amyloidogenesis. Biochemistry 45(7):2234–2242

    Article  CAS  PubMed  Google Scholar 

  103. Guptabansal R, Frederickson RCA, Brunden KR (1995) Proteoglycan-mediated inhibition of Aβ proteolysis – a potential cause of senile plaque accumulation. J Biol Chem 270(31):18666–18671

    Article  CAS  Google Scholar 

  104. Cotman SL, Halfter W, Cole GJ (2000) Agrin binds to beta-amyloid (Aβ), accelerates aβ fibril formation, and is localized to Aβ deposits in Alzheimer’s disease brain. Mol Cell Neurosci 15(2):183–198

    Article  CAS  PubMed  Google Scholar 

  105. Herbst KL (2003) Gonadotropin-releasing hormone antagonists. Curr Opin Pharmacol 3(6):660–666

    Article  CAS  PubMed  Google Scholar 

  106. Kirkitadze MD, Bitan G, Teplow DB (2002) Paradigm shifts in Alzheimer’s disease and other neurodegenerative disorders: the emerging role of oligomeric assemblies. J Neurosci Res 69(5):567–577

    Article  CAS  PubMed  Google Scholar 

  107. Shahnawaz M, Soto C (2012) Microcin amyloid fibrils A are reservoir of toxic oligomeric species. J Biol Chem 287(15):11665–11676

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Krebs MR, Morozova-Roche LA, Daniel K, Robinson CV, Dobson CM (2004) Observation of sequence specificity in the seeding of protein amyloid fibrils. Protein Sci 13(7):1933–1938

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Tanaka M, Chien P, Yonekura K, Weissman JS (2005) Mechanism of cross-species prion transmission: an infectious conformation compatible with two highly divergent yeast prion proteins. Cell 121(1):49–62

    Article  CAS  PubMed  Google Scholar 

  110. Ghosh D, Singh PK, Sahay S, Jha NN, Jacob RS, Sen S, Kumar A, Riek R, Maji SK (2015) Structure based aggregation studies reveal the presence of helix-rich intermediate during α-Synuclein aggregation. Sci Rep 5:9228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Sahay S, Anoop A, Krishnamoorthy G, Maji SK (2014) Site-specific fluorescence dynamics of α-synuclein fibrils using time-resolved fluorescence studies: effect of familial Parkinson’s disease-associated mutations. Biochemistry 53(5):807–809

    Article  CAS  PubMed  Google Scholar 

  112. Sahay S, Ghosh D, Dwivedi S, Anoop A, Mohite GM, Kombrabail M, Krishnamoorthy G, Maji SK (2015) Familial Parkinson disease-associated mutations alter the site-specific microenvironment and dynamics of α-synuclein. J Biol Chem 290(12):7804–7822

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Ghosh D, Mondal M, Mohite GM, Singh PK, Ranjan P, Anoop A, Ghosh S, Jha NN, Kumar A, Maji SK (2013) The Parkinson’s disease-associated H50Q mutation accelerates α-Synuclein aggregation in vitro. Biochemistry 52(40):6925–6927

    Article  CAS  PubMed  Google Scholar 

  114. Ghosh D, Sahay S, Ranjan P, Salot S, Mohite GM, Singh PK, Dwivedi S, Carvalho E, Banerjee R, Kumar A, Maji SK (2014) The newly discovered Parkinson’s disease associated Finnish mutation (A53E) attenuates α-synuclein aggregation and membrane binding. Biochemistry 53(41):6419–6421

    Article  CAS  PubMed  Google Scholar 

  115. Pertinhez TA, Conti S, Ferrari E, Magliani W, Spisni A, Polonelli L (2009) Reversible self-assembly: a key feature for a new class of autodelivering therapeutic peptides. Mol Pharm 6(3):1036–1039

    Article  CAS  PubMed  Google Scholar 

  116. Gupta S, Chattopadhyay T, Pal Singh M, Surolia A (2010) Supramolecular insulin assembly II for a sustained treatment of type 1 diabetes mellitus. Proc Natl Acad Sci U S A 107(30):13246–13251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Burn P (2010) Type 1 diabetes. Nature reviews. Drug Discov 9(3):187–188

    Article  CAS  Google Scholar 

  118. Nelson R, Eisenberg D (2006) Recent atomic models of amyloid fibril structure. Curr Opin Struct Biol 16(2):260–265

    Article  CAS  PubMed  Google Scholar 

  119. Calamai M, Kumita JR, Mifsud J, Parrini C, Ramazzotti M, Ramponi G, Taddei N, Chiti F, Dobson CM (2006) Nature and significance of the interactions between amyloid fibrils and biological polyelectrolytes. Biochemistry 45(42):12806–12815

    Article  CAS  PubMed  Google Scholar 

  120. Ghosh D, Dutta P, Chakraborty C, Singh PK, Anoop A, Jha NN, Jacob RS, Mondal M, Mankar S, Das S, Malik S, Maji SK (2014) Complexation of amyloid fibrils with charged conjugated polymers. Langmuir 30(13):3775–3786

    Article  CAS  PubMed  Google Scholar 

  121. Jha NN, Ghosh D, Das S, Anoop A, Jacob RS, Singh PK, Ayyagari N, Namboothiri IN, Maji SK (2016) Effect of curcumin analogs on α-synuclein aggregation and cytotoxicity. Sci Rep 6:28511

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Nagai Y, Unsworth LD, Koutsopoulos S, Zhang S (2006) Slow release of molecules in self-assembling peptide nanofiber scaffold. J Control Release 115(1):18–25

    Article  CAS  PubMed  Google Scholar 

  123. Koutsopoulos S, Unsworth LD, Nagai Y, Zhang S (2009) Controlled release of functional proteins through designer self-assembling peptide nanofiber hydrogel scaffold. Proc Natl Acad Sci U S A 106(12):4623–4628

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Mazza M, Notman R, Anwar J, Rodger A, Hicks M, Parkinson G, McCarthy D, Daviter T, Moger J, Garrett N, Mead T, Briggs M, Schatzlein AG, Uchegbu IF (2013) Nanofiber-based delivery of therapeutic peptides to the brain. ACS Nano 7(2):1016–1026

    Article  CAS  PubMed  Google Scholar 

  125. Shimanovich U, Efimov I, Mason TO, Flagmeier P, Buell AK, Gedanken A, Linse S, Akerfeldt KS, Dobson CM, Weitz DA, Knowles TP (2015) Protein microgels from amyloid fibril networks. ACS Nano 9(1):43–51

    Article  CAS  PubMed  Google Scholar 

  126. Li C, Bolisetty S, Chaitanya K, Adamcik J, Mezzenga R (2013) Tunable carbon nanotube/protein core-shell nanoparticles with NIR- and enzymatic-responsive cytotoxicity. Adv Mater 25(7):1010–1015

    Article  CAS  PubMed  Google Scholar 

  127. Shen Y, Posavec L, Bolisetty S, Hilty FM, Nystrom G, Kohlbrecher J, Hilbe M, Rossi A, Baumgartner J, Zimmermann MB, Mezzenga R (2017) Amyloid fibril systems reduce, stabilize and deliver bioavailable nanosized iron. Nat Nanotechnol 12(7):642–647

    Article  CAS  PubMed  Google Scholar 

  128. Mains J, Lamprou DA, McIntosh L, Oswald ID, Urquhart AJ (2013) Beta-adrenoceptor antagonists affect amyloid nanostructure; amyloid hydrogels as drug delivery vehicles. Chem Commun (Camb) 49(44):5082–5084

    Article  CAS  Google Scholar 

  129. Ahn M, Kang S, Koo HJ, Lee JH, Lee YS, Paik SR (2010) Nanoporous protein matrix made of amyloid fibrils of β2-microglobulin. Biotechnol Prog 26(6):1759–1764

    Article  CAS  PubMed  Google Scholar 

  130. Bhak G, Lee S, Park JW, Cho S, Paik SR (2010) Amyloid hydrogel derived from curly protein fibrils of α-synuclein. Biomaterials 31(23):5986–5995

    Article  CAS  PubMed  Google Scholar 

  131. Raynes JK, Pearce FG, Meade SJ, Gerrard JA (2011) Immobilization of organophosphate hydrolase on an amyloid fibril nanoscaffold: towards bioremediation and chemical detoxification. Biotechnol Prog 27(2):360–367

    Article  CAS  PubMed  Google Scholar 

  132. Knowles TP, Oppenheim TW, Buell AK, Chirgadze DY, Welland ME (2010) Nanostructured films from hierarchical self-assembly of amyloidogenic proteins. Nat Nanotechnol 5(3):204–207

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Gras SL (2009) Surface- and solution-based assembly of amyloid fibrils for biomedical and nanotechnology applications. Adv Chem Eng 35:161–209

    Article  CAS  Google Scholar 

  134. Mankar S, Anoop A, Sen S, Maji SK (2011) Nanomaterials: amyloids reflect their brighter side. Nano Rev 2:6032

    Article  Google Scholar 

  135. Reches M, Gazit E (2003) Casting metal nanowires within discrete self-assembled peptide nanotubes. Science 300(5619):625–627

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors wish to acknowledge DBT (BT/PR9797/NNT/28/774/2014) Government of India and Wadhwani Research Centre for Bioengineering (WRCB) for financial support.

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Authors and Affiliations

  1. Department of Biosciences and Bioengineering, Indian Institute of Technology Bombay, Mumbai, Maharashtra, India

    Reeba Susan Jacob, A. Anoop & Samir K. Maji

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  1. Reeba Susan Jacob
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  2. A. Anoop
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  3. Samir K. Maji
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Correspondence to Samir K. Maji .

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Editors and Affiliations

  1. National Laboratory of Biomacromolecules, Institute of Biophysics Chinese Academy of Sciences, Beijing, China

    Sarah Perrett

  2. Department of Biotechnology and Biomedicine, Technical University of Denmark DTU, Lyngby, Denmark

    Alexander K. Buell

  3. Department of Chemistry, University of Cambridge, Cambridge, UK

    Tuomas P.J. Knowles

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Jacob, R.S., Anoop, A., Maji, S.K. (2019). Protein Nanofibrils as Storage Forms of Peptide Drugs and Hormones. In: Perrett, S., Buell, A., Knowles, T. (eds) Biological and Bio-inspired Nanomaterials. Advances in Experimental Medicine and Biology, vol 1174. Springer, Singapore. https://doi.org/10.1007/978-981-13-9791-2_8

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