Endocytosed β2-microglobulin amyloid fibrils induce necrosis and apoptosis of rabbit synovial fibroblasts by disrupting endosomal/lysosomal membranes: A novel mechanism on the cytotoxicity of amyloid fibrils

PLoS ONE

Volumn 10, Issue 9, 2015, Pages

  Okoshi, Tadakazu ^a   Yamaguchi, Itaru ^a   Ozawa, Daisaku ^a   Hasegawa, Kazuhiro ^a   Naiki, Hironobu ^a  

^a UNIVERSITY OF FUKUI   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID; BETA 2 MICROGLOBULIN; RECOMBINANT PROTEIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL ADHESION; CELL MEMBRANE; CELL PROLIFERATION; CELL SURFACE; CELL VACUOLE; CELL VIABILITY; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; CYTOPLASM; CYTOSOL; CYTOTOXICITY TEST; ELECTRON MICROSCOPY; ENDOCYTOSIS; ENDOSOME; FIBROBLAST; LYSOSOME MEMBRANE; MITOCHONDRION; NONHUMAN; ADVERSE EFFECTS; AMYLOIDOSIS; ANIMAL; CELL SURVIVAL; DRUG EFFECTS; HEMODIALYSIS; INTRACELLULAR MEMBRANE; LYSOSOME; METABOLISM; NECROSIS; PATHOLOGY; RABBIT; TUMOR CELL LINE;

AMYLOID; AMYLOIDOSIS; ANIMALS; APOPTOSIS; BETA 2-MICROGLOBULIN; CELL LINE, TUMOR; CELL SURVIVAL; ENDOCYTOSIS; ENDOSOMES; FIBROBLASTS; INTRACELLULAR MEMBRANES; LYSOSOMES; NECROSIS; RABBITS; RECOMBINANT PROTEINS; RENAL DIALYSIS;

EID: 84947755191     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0139330     Document Type: Article

References (58)

1. Koch KM. Dialysis-related amyloidosis. Kidney Int. 1992; 41: 1416-1429. PMID: 1614057
2. Floege J, Ehlerding G. β2-microglobulin-associated amyloidosis. Nephron. 1996; 72: 9-26. PMID: 8903856
3. Floege J, Ketteler M. β2-microglobulin-derived amyloidosis: An update. Kidney Int Suppl. 2001; 78: S164-171. PMID: 11169004
4. Charra B, Calemard E, Uzan M, Terrat JC, Vanel T, Laurent G. Carpal tunnel syndrome, shoulder pain and amyloid deposits in long-term haemodialysis patients. Proc Eur Dial Transplant Assoc Eur Ren Assoc. 1985; 21: 291-295. PMID: 3991513
5. Gejyo F, Arakawa M. Dialysis amyloidosis: Current disease concepts and new perspectives for its treatment. Contrib Nephrol. 1990; 78: 47-60. PMID: 2225843
6. Gejyo F, Yamada T, Odani S, Nakagawa Y, Arakawa M, Kunitomo T, et al. A new form of amyloid protein associated with chronic hemodialysis was identified as β2-microglobulin. Biochem Biophys Res Commun. 1985; 129: 701-706. PMID: 3893430
7. Gorevic PD, Munoz PC, Casey TT, DiRaimondo CR, Stone WJ, Prelli FC, et al. Polymerization of intact β2-microglobulin in tissue causes amyloidosis in patients on chronic hemodialysis. Proc Natl Acad Sci U S A. 1986; 83: 7908-7912. PMID: 3532124
8. Campistol JM, Solé M, Bombi JA, Rodriguez R, Mirapeix E, Muñoz-Gomez J, et al. In vitro spontaneous synthesis of β2-microglobulin amyloid fibrils in peripheral blood mononuclear cell culture. Am J Pathol. 1992; 141: 241-247. PMID: 1632465
9. Campistol JM, Bernard D, Papastoitsis G, Solé M, Kasirsky J, Skinner M. Polymerization of normal and intact β2-microglobulin as the amyloidogenic protein in dialysis-amyloidosis. Kidney Int. 1996; 50: 1262-1267. PMID: 8887286
10. Gejyo F, Homma N, Suzuki Y, Arakawa M. Serum levels of β2-microglobulin as a new form of amyloid protein in patients undergoing long-term hemodialysis. N Engl J Med. 1986; 314: 585-586. PMID: 3080684
11. Küchle C, Fricke H, Held E, Schiffl H. High-flux hemodialysis postpones clinical manifestation of dialysis-related amyloidosis. Am J Nephrol. 1996; 16: 484-488. PMID: 8955759
12. van Ypersele de Strihou C, Jadoul M, Malghem J, Maldague B, Jamart J. Effect of dialysis membrane and patient's age on signs of dialysis-related amyloidosis. The Working Party on Dialysis Amyloidosis. Kidney Int. 1991; 39: 1012-1019. PMID: 2067196
13. Davison AM. β2-microglobulin and amyloidosis: Who is at risk? Nephrol Dial Transplant. 1995; 10 (Suppl 10): 48-51. PMID: 8825433
14. Lonnemann G, Koch KM. β2-microglobulin amyloidosis: Effects of ultrapure dialysate and type of dialyzer membrane. J Am Soc Nephrol. 2002; 13(Suppl 1): S72-77. PMID: 11792765
15. Ohashi K, Hara M, Kawai R, Ogura Y, Honda K, Nihei H, et al. Cervical discs are most susceptible to β2-microglobulin amyloid deposition in the vertebral column. Kidney Int. 1992; 41: 1646-1652. PMID: 1501421
16. Garbar C, Jadoul M, Noël H, van Ypersele de Strihou C. Histological characteristics of sternoclavicular β2-microglobulin amyloidosis and clues for its histogenesis. Kidney Int. 1999; 55: 1983-1990. PMID: 10231463
17. Argilés A, García García M, Mourad G. Phagocytosis of dialysis-related amyloid deposits by macrophages. Nephrol Dial Transplant. 2002; 17: 1136-1138. PMID: 12032213
18. García-García M, Argilés A, Gouin-Charnet A, Durfort M, García-Valero J, Mourad G. Impaired lysosomal processing of β2-microglobulin by infiltrating macrophages in dialysis amyloidosis. Kidney Int. 1999; 55: 899-906. PMID: 10027926
19. Naiki H, Nagai Y. Molecular pathogenesis of protein misfolding diseases: Pathological molecular environments versus quality control systems against misfolded proteins. J Biochem. 2009; 146: 751-756. doi: 10.1093/jb/mvp119 PMID: 19643812
20. Bellotti V, Chiti F. Amyloidogenesis in its biological environment: Challenging a fundamental issue in protein misfolding diseases. Curr Opin Struct Biol. 2008; 18: 771-779. doi: 10.1016/j.sbi.2008.10.001 PMID: 18952166
21. Eichner T, Radford SE. Understanding the complex mechanisms of β2-microglobulin amyloid assembly. FEBS J. 2011; 278: 3868-3883. doi: 10.1111/j.1742-4658.2011.08186.x PMID: 21595827
22. Stefani M, Dobson CM. Protein aggregation and aggregate toxicity: New insights into protein folding, misfolding diseases and biological evolution. J Mol Med. 2003; 81: 678-699. PMID: 12942175
23. Eisenberg D, Jucker M. The amyloid state of proteins in human diseases. Cell. 2012; 148: 1188-1203. doi: 10.1016/j.cell.2012.02.022 PMID: 22424229
24. Cecchi C, Stefani M. The amyloid-cell membrane system. The interplay between the biophysical features of oligomers/fibrils and cell membrane defines amyloid toxicity. Biophys Chem. 2013; 182: 30-43. doi: 10.1016/j.bpc.2013.06.003 PMID: 23820236
25. Haass C, Selkoe DJ. Soluble protein oligomers in neurodegeneration: Lessons from the Alzheimer's amyloid -peptide. Nat Rev Mol Cell Biol. 2007; 8: 101-112. PMID: 17245412
26. Okada T, Wakabayashi M, Ikeda K, Matsuzaki K. Formation of toxic fibrils of Alzheimer's amyloid -protein-(1-40) by monosialoganglioside GM1, a neuronal membrane component. J Mol Biol. 2007; 371: 481-489. PMID: 17582434
27. Okada T, Ikeda K, Wakabayashi M, Ogawa M, Matsuzaki K. Formation of toxic A(1-40) fibrils on GM1 ganglioside-containing membranes mimicking lipid rafts: Polymorphisms in A(1-40) fibrils. J Mol Biol. 2008; 382: 1066-1074. doi: 10.1016/j.jmb.2008.07.072 PMID: 18692507
28. Leung E, Guo L, Bu J, Maloof M, El Khoury J, Geula C. Microglia activation mediates fibrillary amyloid-β toxicity in the aged primate cortex. Neurobiol Aging. 2011; 32: 387-397. doi: 10.1016/j.neurobiolaging.2009.02.025 PMID: 19349094
29. Engel MF, Khemtémourian L, Kleijer CC, Meeldijk HJ, Jacobs J, Verkleij AJ, et al. Membrane damage by human islet amyloid polypeptide through fibril growth at the membrane. Proc Natl Acad Sci U S A. 2008; 105: 6033-6038. doi: 10.1073/pnas.0708354105 PMID: 18408164
30. Xue WF, Hellewell AL, Gosal WS, Homans SW, Hewitt EW, Radford SE. Fibril fragmentation enhances amyloid cytotoxicity. J Biol Chem. 2009; 284: 34272-34282. doi: 10.1074/jbc.M109.049809 PMID: 19808677
31. Huang B, He J, Ren J, Yan XY, Zeng CM. Cellular membrane disruption by amyloid fibrils involved intermolecular disulfide cross-linking. Biochemistry. 2009; 48: 5794-5800. doi: 10.1021/bi900219c PMID: 19449893
32. Malchiodi-Albedi F, Contrusciere V, Raggi C, Fecchi K, Rainaldi G, Paradisi S, et al. Lipid raft disruption protects mature neurons against amyloid oligomer toxicity. Biochim Biophys Acta. 2010; 1802: 406-415. doi: 10.1016/j.bbadis.2010.01.007 PMID: 20060899
33. Bucciantini M, Nosi D, Forzan M, Russo E, Calamai M, Pieri L, et al. Toxic effects of amyloid fibrils on cell membranes: The importance of ganglioside GM1. FASEB J. 2012; 26: 818-831. doi: 10.1096/fj.11-189381 PMID: 22071505
34. Walsh P, Vanderlee G, Yau J, Campeau J, Sim VL, Yip CM, et al. The mechanism of membrane disruption by cytotoxic amyloid oligomers formed by prion protein(106-126) is dependent on bilayer composition. J Biol Chem. 2014; 289: 10419-10430. doi: 10.1074/jbc.M113.515866 PMID: 24554723
35. Habib LK, Lee MT, Yang J. Inhibitors of catalase-amyloid interactions protect cells from β-amyloid-induced oxidative stress and toxicity. J Biol Chem. 2010; 285: 38933-38943. doi: 10.1074/jbc.M110.132860 PMID: 20923778
36. Demuro A, Parker I. Cytotoxicity of intracellular Aβ42 amyloid oligomers involves Ca2+ release from the endoplasmic reticulum by stimulated production of inositol trisphosphate. J Neurosci. 2013; 33: 3824-3833. doi: 10.1523/JNEUROSCI.4367-12.2013 PMID: 23447594
37. Meratan AA, Ghasemi A, Nemat-Gorgani M. Membrane integrity and amyloid cytotoxicity: A model study involving mitochondria and lysozyme fibrillation products. J Mol Biol. 2011; 409: 826-838. doi: 10.1016/j.jmb.2011.04.045 PMID: 21565199
38. Porter MY, Routledge KE, Radford SE, Hewitt EW. Characterization of the response of primary cells relevant to dialysis-related amyloidosis to β2-microglobulin monomer and fibrils. PLoS One. 2011; 6: E27353. doi: 10.1371/journal.pone.0027353 PMID: 22096558
39. Sheynis T, Friediger A, Xue WF, Hellewell AL, Tipping KW, Hewitt EW, et al. Aggregation modulators interfere with membrane interactions of β2-microglobulin fibrils. Biophys J. 2013; 105: 745-755. doi: 10.1016/j.bpj.2013.06.015 PMID: 23931322
40. Jakhria T, Hellewell AL, Porter MY, Jackson MP, Tipping KW, Xue WF, et al. β2-Microglobulin amyloid fibrils are nanoparticles that disrupt lysosomal membrane protein trafficking and inhibit protein degradation by lysosomes. J Biol Chem. 2014; 289: 35781-35794. doi: 10.1074/jbc.M114.586222 PMID: 25378395
41. Georgescu HI, Mendelow D, Evans CH. HIG-82: An established cell line from rabbit periarticular soft tissue, which retains the "activatable" phenotype. In Vitro Cell Dev Biol. 1988; 24: 1015-1022. PMID: 2846503
42. Chiba T, Hagihara Y, Higurashi T, Hasegawa K, Naiki H, Goto Y. Amyloid fibril formation in the context of full-length protein: Effects of proline mutations on the amyloid fibril formation of β2-microglobulin. J Biol Chem. 2003; 278: 47016-47024. PMID: 12958308
43. Kihara M, Chatani E, Sakai M, Hasegawa K, Naiki H, Goto Y. Seeding-dependent maturation of β2- microglobulin amyloid fibrils at neutral pH. J Biol Chem. 2005; 280: 12012-12018. PMID: 15659393
44. Ookoshi T, Hasegawa K, Ohhashi Y, Kimura H, Takahashi N, Yoshida H, et al. Lysophospholipids induce the nucleation and extension of β2-microglobulin-related amyloid fibrils at a neutral pH. Nephrol Dial Transplant. 2008; 23: 3247-3255. doi: 10.1093/ndt/gfn231 PMID: 18467373
45. Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, et al. Measurement of protein using bicinchoninic acid. Anal Biochem. 1985; 150: 76-85. PMID: 3843705
46. Wakabayashi M, Matsuzaki K. Formation of amyloids by Aβ-(1-42) on NGF-differentiated PC12 cells: Roles of gangliosides and cholesterol. J Mol Biol. 2007; 371: 924-933. PMID: 17597153
47. Kumar V, Abbas AK, Aster JC. Cell injury, cell death, and adaptations. In: Kumar V, Abbas AK, Aster JC, editors. Robbins Basic Pathology, 9th ed. Philadelphia, PA: Saunders, 2012; pp. 1-28.
48. Hotchkiss RS, Strasser A, McDunn JE, Swanson PE. Cell death. N Engl J Med. 2009; 361: 1570-1583. doi: 10.1056/NEJMra0901217 PMID: 19828534
49. Davies P, Allison AC. Effects of cytochalasin B on endocytosis and exocytosis. Front Biol. 1978; 46: 143-160. PMID: 352738
50. Cooper JA. Effects of cytochalasin and phalloidin on actin. J Cell Biol. 1987; 105: 1473-1478. PMID: 3312229
51. Ditaranto K, Tekirian TL, Yang AJ. Lysosomal membrane damage in soluble Aβ-mediated cell death in Alzheimer's disease. Neurobiol Dis. 2001; 8: 19-31. PMID: 11162237
52. Umeda T, Tomiyama T, Sakama N, Tanaka S, Lambert MP, Klein WL, et al. Intraneuronal amyloid β oligomers cause cell death via endoplasmic reticulum stress, endosomal/lysosomal leakage, and mitochondrial dysfunction in vivo. J Neurosci Res. 2011; 89: 1031-1042. doi: 10.1002/jnr.22640 PMID: 21488093
53. Guan J, Mishra S, Qiu Y, Shi J, Trudeau K, Las G, et al. Lysosomal dysfunction and impaired autophagy underlie the pathogenesis of amyloidogenic light chain-mediated cardiotoxicity. EMBO Mol Med. 2014; 6: 1493-1507. doi: 10.15252/emmm.201404190 PMID: 25319546
54. Barland P, Novikoff AB, Hamerman D. Electron microscopy of the human synovial membrane. J Cell Biol. 1962; 14: 207-220. PMID: 13865038
55. Fell HB. Synoviocytes. J Clin Pathol Suppl. 1978; 12: 14-24.
56. Gharibyan AL, Zamotin V, Yanamandra K, Moskaleva OS, Margulis BA, Kostanyan IA, et al. Lysozyme amyloid oligomers and fibrils induce cellular death via different apoptotic/necrotic pathways. J Mol Biol. 2007; 365: 1337-1349. PMID: 17134716
57. Bullough PG. Joints. In: Mills SE, editor. Histology for Pathologists, 4th ed. Philadelphia, PA: Lippincott Williams & Wilkins; 2012. pp. 107-130.
58. Ritchlin C. Fibroblast biology. Effector signals released by the synovial fibroblast in arthritis. Arthritis Res. 2000; 2: 356-360. PMID: 11094448