Self-assembling peptides form immune suppressive amyloid fibrils effective in autoimmune encephalomyelitis

Current Topics in Behavioral Neurosciences

Volumn 26, Issue , 2015, Pages 221-232

  Kurnellas, Michael P ^a   Rothbard, Jonathan B ^a   Steinman, Lawrence ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Amyloid fibrils; Antiinflammatory; Immunosuppression; Molecular chaperones; Multiple sclerosis; Neurodegeneration; Self assembling peptides

Indexed keywords

ALPHA BETA INTERFERON RECEPTOR; AMYLIN; AMYLOID; AMYLOID PROTEIN; APOLIPOPROTEIN E; CHAPERONE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON; INTERLEUKIN 6; PEPTIDE; SMALL HEAT SHOCK PROTEIN; THIOFLAVINE; TUMOR NECROSIS FACTOR ALPHA; NONSTEROID ANTIINFLAMMATORY AGENT;

ALLERGIC ENCEPHALOMYELITIS; HUMAN; NERVOUS SYSTEM INFLAMMATION; PRIORITY JOURNAL; TH1 CELL; TH17 CELL; ANIMAL; CHEMISTRY; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; MOUSE;

AMYLOID; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; HUMANS; MICE; MOLECULAR CHAPERONES; PEPTIDES;

EID: 84943631681     PISSN: 18663370     EISSN: 18663389     Source Type: Book Series    
DOI: 10.1007/7854_2015_377     Document Type: Chapter

References (41)

1. Arac A, Brownell SE, Rothbard JB, Chen C, Ko RM, Pereira MP, Albers GW, Steinman L, Steinberg GK (2011) Systemic augmentation of alphaB-crystallin provides therapeutic benefit twelve hours post-stroke onset via immune modulation. Proc Natl Acad Sci USA 108:13287-13292
2. Axtell RC, de Jong BA, Boniface K, van der Voort LF, Bhat R, De Sarno P, Naves R, Han M, Zhong F, Castellanos JG, Mair R, Christakos A, Kolkowitz I, Katz L, Killestein J, Polman CH, de Waal Malefyt R, Steinman L, Raman C (2010) T helper type 1 and 17 cells determine efficacy of interferon-beta in multiple sclerosis and experimental encephalomyelitis. Nat Med 16:406-412
3. Axtell RC, Raman C, Steinman L (2011) Interferon-beta exacerbates Th17-mediated inflammatory disease. Trends Immunol 32:272-277
4. Axtell RC, Raman C, Steinman L (2012) Type I interferons: beneficial in Th1 and detrimental in Th17 autoimmunity. Clin Rev Allergy Immunol 44:114-120
5. Azevedo EP, Guimaraes-Costa AB, Torezani GS, Braga CA, Palhano FL, Kelly JW, Saraiva EM, Foguel D (2012) Amyloid fibrils trigger the release of neutrophil extracellular traps (NETs), causing fibril fragmentation by NET-associated elastase. J Biol Chem 287:37206-37218
6. Bhattacharyya J, Padmanabha Udupa EG, Wang J, Sharma KK (2006) Mini-alphaB-crystallin: a functional element of alphaB-crystallin with chaperone-like activity. Biochemistry 45:3069-3076
7. Chiti F, Dobson CM (2009) Amyloid formation by globular proteins under native conditions. Nat Chem Biol 5:15-22
8. Doherty GJ, McMahon HT (2009) Mechanisms of endocytosis. Ann Rev Biochem 78:857-902
9. Eisenberg D, Jucker M (2012) The amyloid state of proteins in human diseases. Cell 148:1188-1203
10. Fernandez-Escamilla AM, Rousseau F, Schymkowitz J, Serrano L (2004) Prediction of sequencedependent and mutational effects on the aggregation of peptides and proteins. Nat Biotechnol 22:1302-1306
11. Ghiso J, Matsubara E, Koudinov A, Choi-Miura NH, Tomita M, Wisniewski T, Frangione B (1993) The cerebrospinal-fluid soluble form of Alzheimer’s amyloid beta is complexed to SP-40,40 (apolipoprotein J), an inhibitor of the complement membrane-attack complex. Biochem J 293(Pt 1):27-30
12. Goldschmidt L, Teng PK, Riek R, Eisenberg D (2010) Identifying the amylome, proteins capable of forming amyloid-like fibrils. Proc Natl Acad Sci USA 107:3487-3492
13. Gourdain P, Ballerini C, Nicot AB, Carnaud C (2012) Exacerbation of experimental autoimmune encephalomyelitis in prion protein (PrPc)-null mice: evidence for a critical role of the central nervous system. J Neuroinflammation 9:25
14. Grant JL, Ghosn EE, Axtell RC, Herges K, Kuipers HF, Woodling NS, Andreasson K, Herzenberg LA, Herzenberg LA, Steinman L (2012) Reversal of paralysis and reduced inflammation from peripheral administration of beta-amyloid in TH1 and TH17 versions of experimental autoimmune encephalomyelitis. Sci Transl Med 4:145ra105
15. Greenwald J, Riek R (2010) Biology of amyloid: structure, function, and regulation. Structure 18:1244-1260
16. Han MH, Hwang SI, Roy DB, Lundgren DH, Price JV, Ousman SS, Fernald GH, Gerlitz B, Robinson WH, Baranzini SE, Grinnell BW, Raine CS, Sobel RA, Han DK, Steinman L (2008) Proteomic analysis of active multiple sclerosis lesions reveals therapeutic targets. Nature 451:1076-1081
17. Jakob U, Gaestel M, Engel K, Buchner J (1993) Small heat shock proteins are molecular chaperones. J Biol Chem 268:1517-1520
18. Jang H, Arce FT, Ramachandran S, Capone R, Lal R, Nussinov R (2010) Beta-barrel topology of Alzheimer’s beta-amyloid ion channels. J Mol Biol 404:917-934
19. Ji Z, Ke ZJ, Geng JG (2012) SAP suppresses the development of experimental autoimmune encephalomyelitis in C57BL/6 mice. Immunol Cell Biol 90:388-395
20. Karussis D, Michaelson DM, Grigoriadis N, Korezyn AD, Mizrachi-Koll R, Chapman S, Abramsky O, Chapman J (2003) Lack of apolipoprotein-E exacerbates experimental allergic encephalomyelitis. Mult Scler 9:476-480
21. 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 300:486-489
22. Kurnellas MP, Adams CM, Sobel RA, Steinman L, Rothbard JB (2013) Amyloid fibrils composed of hexameric peptides attenuate neuroinflammation. Sci Transl Med 5:179ra142
23. Kurnellas MP, Brownell SE, Su L, Malkovskiy AV, Rajadas J, Dolganov G, Chopra S, Schoolnik GK, Sobel RA, Webster J, Ousman SS, Becker RA, Steinman L, Rothbard JB (2012) Chaperone activity of small heat shock proteins underlies therapeutic efficacy in experimental autoimmune encephalomyelitis. J Biol Chem 287:36423-36434
24. Kurnellas MP, Schartner JM, Fathman CG, Jagger A, Steinman L, Rothbard JB (2014) Mechanisms of action of therapeutic amyloidogenic hexapeptides in amelioration of inflammatory brain disease. J Exp Med 211:1847-1856
25. Laganowsky A, Liu C, Sawaya MR, Whitelegge JP, Park J, Zhao M, Pensalfini A, Soriaga AB, Landau M, Teng PK, Cascio D, Glabe C, Eisenberg D (2012) Atomic view of a toxic amyloid small oligomer. Science 335:1228-1231
26. Naiki H, Higuchi K, Hosokawa M, Takeda T (1989) Fluorometric determination of amyloid fibrils in vitro using the fluorescent dye, thioflavin T1. Anal Biochem 177:244-249
27. Nelson R, Sawaya MR, Balbirnie M, Madsen AO, Riekel C, Grothe R, Eisenberg D (2005) Structure of the cross-beta spine of amyloid-like fibrils. Nature 435:773-778
28. Ousman SS, Tomooka BH, van Noort JM, Wawrousek EF, O’Conner K, Hafler DA, Sobel RA, Robinson WH, Steinman L (2007) Protective and therapeutic role for alphaB-crystallin in autoimmune demyelination. Nature 448:474-479
29. Pangratz-Fuehrer S, Kaur K, Ousman SS, Steinman L, Liao YJ (2011) Functional rescue of experimental ischemic optic neuropathy with alphaB-crystallin. Eye (Lond) 25:809-817
30. Platten M, Youssef S, Hur EM, Ho PP, Han MH, Lanz TV, Phillips LK, Goldstein MJ, Bhat R, Raine CS, Sobel RA, Steinman L (2009) Blocking angiotensin-converting enzyme induces potent regulatory T cells and modulates TH1-and TH17-mediated autoimmunity. Proc Natl Acad Sci USA 106:14948-14953
31. Quist A, Doudevski I, Lin H, Azimova R, Ng D, Frangione B, Kagan B, Ghiso J, Lal R (2005) Amyloid ion channels: a common structural link for protein-misfolding disease. Proc Natl Acad Sci USA 102:10427-10432
32. Rothbard JB, Kurnellas MP, Brownell S, Adams CM, Su L, Axtell RC, Chen R, Fathman CG, Robinson WH, Steinman L (2012) Therapeutic effects of systemic administration of chaperone alphaB-crystallin associated with binding proinflammatory plasma proteins. J Biol Chem 287:9708-9721
33. Sawaya MR, Sambashivan S, Nelson R, Ivanova MI, Sievers SA, Apostol MI, Thompson MJ, Balbirnie M, Wiltzius JJ, McFarlane HT, Madsen AO, Riekel C, Eisenberg D (2007) Atomic structures of amyloid cross-beta spines reveal varied steric zippers. Nature 447:453-457
34. Sokolowski JD, Mandell JW (2011) Phagocytic clearance in neurodegeneration. Am J Pathol 178:1416-1428
35. Strittmatter WJ, Saunders AM, Schmechel D, Pericak-Vance M, Enghild J, Salvesen GS, Roses AD (1993) Apolipoprotein E: high-avidity binding to beta-amyloid and increased frequency of type 4 allele in late-onset familial Alzheimer disease. Proc Natl Acad Sci USA 90:1977-1981
36. Tanaka N, Tanaka R, Tokuhara M, Kunugi S, Lee YF, Hamada D (2008) Amyloid fibril formation and chaperone-like activity of peptides from alphaA-crystallin. Biochemistry 47:2961-2967
37. Thompson MJ, Sievers SA, Karanicolas J, Ivanova MI, Baker D, Eisenberg D (2006) The 3D profile method for identifying fibril-forming segments of proteins. Proc Natl Acad Sci USA 103:4074-4078
38. Velayudhan L, Killick R, Hye A, Kinsey A, Guntert A, Lynham S, Ward M, Leung R, Lourdusamy A, To AW, Powell J, Lovestone S (2012) Plasma transthyretin as a candidate marker for Alzheimer’s disease. J Alzheimers Dis 28:369-375
39. Velotta JB, Kimura N, Chang SH, Chung J, Itoh S, Rothbard J, Yang PC, Steinman L, Robbins RC, Fischbein MP (2011) AlphaB-crystallin improves murine cardiac function and attenuates apoptosis in human endothelial cells exposed to ischemia-reperfusion. Ann Thorac Surg 91:1907-1913
40. Weinger JG, Davies P, Acker CM, Brosnan CF, Tsiperson V, Bayewitz A, Shafit-Zagardo B (2012) Mice devoid of Tau have increased susceptibility to neuronal damage in myelin oligodendrocyte glycoprotein-induced experimental autoimmune encephalomyelitis. J Neuropathol Exp Neurol 71:422-433
41. Xue WF, Hellewell AL, Gosal WS, Homans SW, Hewitt EW, Radford SE (2009) Fibril fragmentation enhances amyloid cytotoxicity. J Biol Chem 284:34272-34282