Amyloid seeding of transthyretin by ex vivo cardiac fibrils and its inhibition

Saelices, Lorena; Chung, Kevin; Lee, Ji H.; Cohn, Whitaker; Whitelegge, Julian P.; Benson, Merrill D.; Eisenberg, David S.

doi:10.1073/pnas.1805131115

Title: Amyloid seeding of transthyretin by ex vivo cardiac fibrils and its inhibition

Journal Article · 28 June 2018 · Proceedings of the National Academy of Sciences of the United States of America

DOI: https://doi.org/10.1073/pnas.1805131115 · OSTI ID:1457595

^[1]; Chung, Kevin ^[1]; Lee, Ji H. ^[1]; Cohn, Whitaker ^[2]; Whitelegge, Julian P. ^[2]; Benson, Merrill D. ^[3]; Eisenberg, David S. ^[1]

Howard Hughes Medical Institute, University of California, Los Angeles, CA 90095,, UCLA-DOE, University of California, Los Angeles, CA 90095,, Department of Biological Chemistry, University of California, Los Angeles, CA 90095,, Molecular Biology Institute, University of California, Los Angeles, CA 90095,
Neuropsychiatric Institute (NPI)-Semel Institute, University of California, Los Angeles, CA 90024,
Department of Pathology and Laboratory Medicine, Indiana University School of Medicine, Indianapolis, IN 46202

Significance Transthyretin (TTR) cardiac amyloidosis is characterized by the deposition of TTR amyloid fibrils in the heart. No therapy is currently available for wild-type cardiac amyloidosis. Hereditary cases are treated by liver transplantation, a crude form of gene therapy which replaces amyloidogenic mutant TTR by the more stable wild-type form, with the goal of halting further deposition and disease progression. However, wild-type TTR continues to deposit in the heart of many patients after the procedure. Until now, seeding of TTR fibril formation has not been demonstrated in vitro. We show that patient-extracted cardiac fibrils can seed both wild-type and mutant TTR fibril formation in vitro. This process can be inhibited by structure-based peptide inhibitors, thereby providing an alternative approach to therapy.

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Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1457595

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Vol. 115 Journal Issue: 29; ISSN 0027-8424

Publisher:: Proceedings of the National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 45 works

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References (77)

TRANSFER AMYLOIDOSIS: Local and Systemic Amyloidosis in Recipients of Syngeneic Spleen Grafts from Non-Amyloidotic, Casein-Sensitized Donor Mice Hardt, Finn; Ranløv, Poul Acta Pathologica Microbiologica Scandinavica, Vol. 73, Issue 4 https://doi.org/10.1111/j.1699-0463.1968.tb03212.x	journal	September 1968
Liver transplantation in transthyretin amyloidosis: Issues and challenges: Liver Transplantation in Attr Carvalho, Andreia; Rocha, Ana; Lobato, Luísa Liver Transplantation, Vol. 21, Issue 3 https://doi.org/10.1002/lt.24058	journal	February 2015
Why are some amyloidoses systemic? Does hepatic “chaperoning at a distance” prevent cardiac deposition in a transgenic model of human senile systemic (transthyretin) amyloidosis? Buxbaum, Joel N.; Tagoe, Clement; Gallo, Gloria The FASEB Journal, Vol. 26, Issue 6 https://doi.org/10.1096/fj.11-189571	journal	June 2012
Molecular Mechanisms of Amyloidosis Merlini, Giampaolo; Bellotti, Vittorio New England Journal of Medicine, Vol. 349, Issue 6 https://doi.org/10.1056/NEJMra023144	journal	August 2003
Amyloid turnover after liver transplantation in FAP Obayashi, K.; Ueda, M.; Jono, H. Amyloid, Vol. 18, Issue sup1 https://doi.org/10.3109/13506129.2011.574354070	journal	June 2011
Clinical development of an antisense therapy for the treatment of transthyretin-associated polyneuropathy Ackermann, Elizabeth J.; Guo, Shuling; Booten, Sheri Amyloid, Vol. 19, Issue sup1 https://doi.org/10.3109/13506129.2012.673140	journal	April 2012
The Amyloid State of Proteins in Human Diseases Eisenberg, David; Jucker, Mathias Cell, Vol. 148, Issue 6 https://doi.org/10.1016/j.cell.2012.02.022	journal	March 2012
Amyloid deposits in transthyretin-derived amyloidosis: cleaved transthyretin is associated with distinct amyloid morphology Bergström, Joakim; Gustavsson, Åsa; Hellman, Ulf The Journal of Pathology, Vol. 206, Issue 2 https://doi.org/10.1002/path.1759	journal	January 2005
Recipient aging accelerates acquired transthyretin amyloidosis after domino liver transplantation: Recipient Aging Accelerates Acquired TTR Amyloidosis Misumi, Yohei; Narita, Yasuko; Oshima, Toshinori Liver Transplantation, Vol. 22, Issue 5 https://doi.org/10.1002/lt.24371	journal	April 2016
Transthyretin-derived senile systemic amyloidosis: clinicopathologic and structural considerations Westermark, Per; Bergström, Joakim; Solomon, Alan Amyloid, Vol. 10, Issue sup1 https://doi.org/10.1080/13506129.2003.12088568	journal	August 2003
Suppressing transthyretin production in mice, monkeys and humans using 2nd-Generation antisense oligonucleotides Ackermann, Elizabeth J.; Guo, Shuling; Benson, Merrill D. Amyloid, Vol. 23, Issue 3 https://doi.org/10.1080/13506129.2016.1191458	journal	June 2016
Partial denaturation of transthyretin is sufficient for amyloid fibril formation in vitro Colon, Wilfredo; Kelly, Jeffery W. Biochemistry, Vol. 31, Issue 36 https://doi.org/10.1021/bi00151a036	journal	September 1992
An Engineered Transthyretin Monomer that Is Nonamyloidogenic, Unless It Is Partially Denatured ^† Jiang, Xin; Smith, Craig S.; Petrassi, H. Michael Biochemistry, Vol. 40, Issue 38 https://doi.org/10.1021/bi011194d	journal	September 2001
Seeding “one-dimensional crystallization” of amyloid: A pathogenic mechanism in Alzheimer's disease and scrapie? Jarrett, Joseph T.; Lansbury, Peter T. Cell, Vol. 73, Issue 6 https://doi.org/10.1016/0092-8674(93)90635-4	journal	June 1993
Transthyretin amyloidosis: an under-recognized neuropathy and cardiomyopathy Galant, Natalie J.; Westermark, Per; Higaki, Jeffrey N. Clinical Science, Vol. 131, Issue 5 https://doi.org/10.1042/CS20160413	journal	February 2017
Pathogenesis of transthyretin amyloidosis Benson, Merrill D. Amyloid, Vol. 19, Issue sup1 https://doi.org/10.3109/13506129.2012.668501	journal	March 2012
Prion-like aggregates: infectious agents in human disease Westermark, Gunilla T.; Westermark, Per Trends in Molecular Medicine, Vol. 16, Issue 11 https://doi.org/10.1016/j.molmed.2010.08.004	journal	November 2010
Novel conformation-specific monoclonal antibodies against amyloidogenic forms of transthyretin Higaki, Jeffrey N.; Chakrabartty, Avi; Galant, Natalie J. Amyloid, Vol. 23, Issue 2 https://doi.org/10.3109/13506129.2016.1148025	journal	March 2016
Systemic senile amyloidosis. Identification of a new prealbumin (transthyretin) variant in cardiac tissue: immunologic and biochemical similarity to one form of familial amyloidotic polyneuropathy. Gorevic, P. D.; Prelli, F. C.; Wright, J. Journal of Clinical Investigation, Vol. 83, Issue 3 https://doi.org/10.1172/JCI113966	journal	March 1989
Transthyretin Aggregation under Partially Denaturing Conditions Is a Downhill Polymerization ^† Hurshman, Amy R.; White, Joleen T.; Powers, Evan T. Biochemistry, Vol. 43, Issue 23 https://doi.org/10.1021/bi049621l	journal	June 2004
Amyloidosis in mice Produced by Transplantation of Spleen Cells from Casein-Treated mice Werdelin, Ole; RanlØV, Poul Acta Pathologica Microbiologica Scandinavica, Vol. 68, Issue 1 https://doi.org/10.1111/apm.1966.68.1.1	journal	November 1966
Cardiac Amyloid in Patients with Familial Amyloid Polyneuropathy Consists of Abundant Wild-Type Transthyretin Yazaki, Masahide; Tokuda, Takahiko; Nakamura, Akihiro Biochemical and Biophysical Research Communications, Vol. 274, Issue 3 https://doi.org/10.1006/bbrc.2000.3203	journal	August 2000
Transthyretin-derived amyloid deposition in the heart of an elderly Japanese population Su, Y.; Horibata, Y.; Ueda, M. Amyloid, Vol. 18, Issue sup1 https://doi.org/10.3109/13506129.2011.574354067	journal	June 2011
Non-genetic propagation of strain-specific properties of scrapie prion protein Bessen, Richard A.; Kocisko, David A.; Raymond, Gregory J. Nature, Vol. 375, Issue 6533 https://doi.org/10.1038/375698a0	journal	June 1995
Variation in amount of wild-type transthyretin in different fibril and tissue types in ATTR amyloidosis Ihse, Elisabet; Suhr, Ole B.; Hellman, Ulf Journal of Molecular Medicine, Vol. 89, Issue 2 https://doi.org/10.1007/s00109-010-0695-1	journal	November 2010
Cell Damage in Light Chain Amyloidosis: FIBRIL INTERNALIZATION, TOXICITY AND CELL-MEDIATED SEEDING Marin-Argany, Marta; Lin, Yi; Misra, Pinaki Journal of Biological Chemistry, Vol. 291, Issue 38 https://doi.org/10.1074/jbc.M116.736736	journal	July 2016
Clinical, ECG and echocardiographic clues to the diagnosis of TTR-related cardiomyopathy Damy, Thibaud; Maurer, Mathew S.; Rapezzi, Claudio Open Heart, Vol. 3, Issue 1 https://doi.org/10.1136/openhrt-2015-000289	journal	February 2016
Diflunisal Analogues Stabilize the Native State of Transthyretin. Potent Inhibition of Amyloidogenesis Adamski-Werner, Sara L.; Palaninathan, Satheesh K.; Sacchettini, James C. Journal of Medicinal Chemistry, Vol. 47, Issue 2 https://doi.org/10.1021/jm030347n	journal	January 2004
Liver transplantation and transthyretin amyloidosis Benson, Merrill D. Muscle & Nerve, Vol. 47, Issue 2 https://doi.org/10.1002/mus.23521	journal	November 2012
Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips Rappsilber, Juri; Mann, Matthias; Ishihama, Yasushi Nature Protocols, Vol. 2, Issue 8 https://doi.org/10.1038/nprot.2007.261	journal	August 2007
Exogenous Induction of Cerebral -Amyloidogenesis Is Governed by Agent and Host Meyer-Luehmann, M. Science, Vol. 313, Issue 5794 https://doi.org/10.1126/science.1131864	journal	September 2006
Transfer Amyloidosis: Ultrastructure of the Transferred Subcellular Fractions Wanstrup, John; Ranløv, Poul Acta Pathologica Microbiologica Scandinavica, Vol. 74, Issue 2 https://doi.org/10.1111/j.1699-0463.1968.tb03482.x	journal	May 1968
The 3D profile method for identifying fibril-forming segments of proteins Thompson, M. J.; Sievers, S. A.; Karanicolas, J. Proceedings of the National Academy of Sciences, Vol. 103, Issue 11 https://doi.org/10.1073/pnas.0511295103	journal	March 2006
Inclusion formation and neuronal cell death through neuron-to-neuron transmission of -synuclein Desplats, P.; Lee, H. -J.; Bae, E. -J. Proceedings of the National Academy of Sciences, Vol. 106, Issue 31 https://doi.org/10.1073/pnas.0903691106	journal	July 2009
Amyloidogenesis is neither accelerated nor enhanced by injections of preformed fibrils in mice transgenic for wild-type human transthyretin: the question of infectivity Tagoe, Clement E.; French, David; Gallo, Gloria Amyloid, Vol. 11, Issue 1 https://doi.org/10.1080/13506120410001674982	journal	March 2004
Liver transplantation in transthyretin-related familial amyloid polyneuropathy Stangou, Arie J.; Hawkins, Philip N. Current Opinion in Neurology, Vol. 17, Issue 5 https://doi.org/10.1097/00019052-200410000-00012	journal	January 2004
A Unifying Role for Prions in Neurodegenerative Diseases Prusiner, S. B. Science, Vol. 336, Issue 6088 https://doi.org/10.1126/science.1222951	journal	June 2012
Proteopathic tau seeding predicts tauopathy in vivo Holmes, B. B.; Furman, J. L.; Mahan, T. E. Proceedings of the National Academy of Sciences, Vol. 111, Issue 41 https://doi.org/10.1073/pnas.1411649111	journal	September 2014
Transmission and spreading of tauopathy in transgenic mouse brain Clavaguera, Florence; Bolmont, Tristan; Crowther, R. Anthony Nature Cell Biology, Vol. 11, Issue 7 https://doi.org/10.1038/ncb1901	journal	June 2009
Risk of transmission of systemic transthyretin amyloidosis after domino liver transplantation Lladó, Laura; Baliellas, Carme; Casasnovas, Carlos Liver Transplantation, Vol. 16, Issue 12 https://doi.org/10.1002/lt.22174	journal	November 2010
Safety and efficacy of long-term diflunisal administration in hereditary transthyretin (ATTR) amyloidosis Sekijima, Yoshiki; Tojo, Kana; Morita, Hiroshi Amyloid, Vol. 22, Issue 2 https://doi.org/10.3109/13506129.2014.997872	journal	December 2014
Self-Propagating, Molecular-Level Polymorphism in Alzheimer's -Amyloid Fibrils Petkova, A. T. Science, Vol. 307, Issue 5707 https://doi.org/10.1126/science.1105850	journal	January 2005
The pathogenesis of amyloid deposition: A new hypothesis Kisilevsky, Robert; Axelrad, Michael Medical Hypotheses, Vol. 2, Issue 6 https://doi.org/10.1016/S0306-9877(76)80002-3	journal	November 1976
Structure-based design of non-natural amino-acid inhibitors of amyloid fibril formation Sievers, Stuart A.; Karanicolas, John; Chang, Howard W. Nature, Vol. 475, Issue 7354 https://doi.org/10.1038/nature10154	journal	June 2011
Tafamidis, a potent and selective transthyretin kinetic stabilizer that inhibits the amyloid cascade Bulawa, C. E.; Connelly, S.; DeVit, M. Proceedings of the National Academy of Sciences, Vol. 109, Issue 24 https://doi.org/10.1073/pnas.1121005109	journal	May 2012
Fibril in senile systemic amyloidosis is derived from normal transthyretin. Westermark, P.; Sletten, K.; Johansson, B. Proceedings of the National Academy of Sciences, Vol. 87, Issue 7 https://doi.org/10.1073/pnas.87.7.2843	journal	April 1990
Alzheimer's and Parkinson's diseases: The prion concept in relation to assembled A , tau, and -synuclein Goedert, M. Science, Vol. 349, Issue 6248 https://doi.org/10.1126/science.1255555	journal	August 2015
Structure of the toxic core of α-synuclein from invisible crystals Rodriguez, Jose A.; Ivanova, Magdalena I.; Sawaya, Michael R. Nature, Vol. 525, Issue 7570 https://doi.org/10.1038/nature15368	journal	September 2015
Amyloid fibrils containing fragmented ATTR may be the standard fibril composition in ATTR amyloidosis Ihse, Elisabet; Rapezzi, Claudio; Merlini, Giampaolo Amyloid, Vol. 20, Issue 3 https://doi.org/10.3109/13506129.2013.797890	journal	May 2013
Primary structure of an amyloid prealbumin variant in familial polyneuropathy of Jewish origin. Pras, M.; Prelli, F.; Franklin, E. C. Proceedings of the National Academy of Sciences, Vol. 80, Issue 2 https://doi.org/10.1073/pnas.80.2.539	journal	January 1983
Uncovering the Mechanism of Aggregation of Human Transthyretin Saelices, Lorena; Johnson, Lisa M.; Liang, Wilson Y. Journal of Biological Chemistry, Vol. 290, Issue 48 https://doi.org/10.1074/jbc.M115.659912	journal	October 2015
Tissue damage in the amyloidoses: Transthyretin monomers and nonnative oligomers are the major cytotoxic species in tissue culture Reixach, N.; Deechongkit, S.; Jiang, X. Proceedings of the National Academy of Sciences, Vol. 101, Issue 9 https://doi.org/10.1073/pnas.0400062101	journal	February 2004
A Designed Inhibitor of p53 Aggregation Rescues p53 Tumor Suppression in Ovarian Carcinomas Soragni, Alice; Janzen, Deanna M.; Johnson, Lisa M. Cancer Cell, Vol. 29, Issue 1 https://doi.org/10.1016/j.ccell.2015.12.002	journal	January 2016
Detergent-insoluble Aggregates Associated with Amyotrophic Lateral Sclerosis in Transgenic Mice Contain Primarily Full-length, Unmodified Superoxide Dismutase-1 Shaw, Bryan F.; Lelie, Herman L.; Durazo, Armando Journal of Biological Chemistry, Vol. 283, Issue 13 https://doi.org/10.1074/jbc.M707751200	journal	January 2008
Transmission of Systemic Transthyretin Amyloidosis by Means of Domino Liver Transplantation Stangou, Arie J.; Heaton, Nigel D.; Hawkins, Philip N. New England Journal of Medicine, Vol. 352, Issue 22 https://doi.org/10.1056/NEJM200506023522219	journal	June 2005
Sensitive detection of pathological prion protein by cyclic amplification of protein misfolding Saborio, Gabriela P.; Permanne, Bruno; Soto, Claudio Nature, Vol. 411, Issue 6839 https://doi.org/10.1038/35081095	journal	June 2001
The Adoptive Transfer of Experimental Mouse Amyloidosis by Intravenous Injections of Spleen cell Extracts from Casein-Treated Syngeneic Donor mice Ranløv, Poul Acta Pathologica Microbiologica Scandinavica, Vol. 70, Issue 2 https://doi.org/10.1111/j.1699-0463.1967.tb01300.x	journal	September 1967
Partial amino acid sequence homology between an heredofamilial amyloid protein and human plasma prealbumin. Benson, M. D. Journal of Clinical Investigation, Vol. 67, Issue 4 https://doi.org/10.1172/JCI110114	journal	April 1981
Quantification of the Thermodynamically Linked Quaternary and Tertiary Structural Stabilities of Transthyretin and Its Disease-Associated Variants: The Relationship between Stability and Amyloidosis ^† Hurshman Babbes, Amy R.; Powers, Evan T.; Kelly, Jeffery W. Biochemistry, Vol. 47, Issue 26 https://doi.org/10.1021/bi800636q	journal	July 2008
Novel Antibody for the Treatment of Transthyretin Amyloidosis Hosoi, Akihiko; Su, Yu; Torikai, Masaharu Journal of Biological Chemistry, Vol. 291, Issue 48 https://doi.org/10.1074/jbc.M116.738138	journal	October 2016
Iatrogenic Creutzfeldt-Jakob Disease, Final Assessment Brown, Paul; Brandel, Jean-Philippe; Sato, Takeshi Emerging Infectious Diseases, Vol. 18, Issue 6 https://doi.org/10.3201/eid1806.120116	journal	June 2012
In Vitro Generation of Infectious Scrapie Prions Castilla, Joaquín; Saá, Paula; Hetz, Claudio Cell, Vol. 121, Issue 2, p. 195-206 https://doi.org/10.1016/j.cell.2005.02.011	journal	April 2005
Amyloid fibril protein related to prealbumin in familial amyloidotic polyneuropathy. Costa, P. P.; Figueira, A. S.; Bravo, F. R. Proceedings of the National Academy of Sciences, Vol. 75, Issue 9 https://doi.org/10.1073/pnas.75.9.4499	journal	September 1978
Senile Cardiac Amyloid is Related to Prealbumin Sletten, K.; Westermark, P.; Natvig, J. B. Scandinavian Journal of Immunology, Vol. 12, Issue 6 https://doi.org/10.1111/j.1365-3083.1980.tb00098.x	journal	December 1980
Molecular Structure of β-Amyloid Fibrils in Alzheimer’s Disease Brain Tissue Lu, Jun-Xia; Qiang, Wei; Yau, Wai-Ming Cell, Vol. 154, Issue 6 https://doi.org/10.1016/j.cell.2013.08.035	journal	September 2013
Progression of cardiac amyloid deposition in hereditary transthyretin amyloidosis patients after liver transplantation Liepnieks, Juris J.; Benson, Merrill D. Amyloid, Vol. 14, Issue 4 https://doi.org/10.1080/13506120701614032	journal	January 2007
Deposition of transthyretin amyloid is not accelerated by the same amyloid *in vivo* Wei, Lan; Kawano, Hiroo; Fu, Xiaoying Amyloid, Vol. 11, Issue 2 https://doi.org/10.1080/13506120410001726344	journal	June 2004
Noncerebral Amyloidoses: Aspects on Seeding, Cross-Seeding, and Transmission Westermark, Gunilla T.; Fändrich, Marcus; Lundmark, Katarzyna Cold Spring Harbor Perspectives in Medicine, Vol. 8, Issue 1 https://doi.org/10.1101/cshperspect.a024323	journal	January 2017
Disease profile and differential diagnosis of hereditary transthyretin-related amyloidosis with exclusively cardiac phenotype: an Italian perspective Rapezzi, C.; Quarta, C. C.; Obici, L. European Heart Journal, Vol. 34, Issue 7 https://doi.org/10.1093/eurheartj/ehs123	journal	June 2012
The Pathway by Which the Tetrameric Protein Transthyretin Dissociates ^† Foss, Ted R.; Wiseman, R. Luke; Kelly, Jeffery W. Biochemistry, Vol. 44, Issue 47 https://doi.org/10.1021/bi051608t	journal	November 2005
Structure of the cross-β spine of amyloid-like fibrils Nelson, Rebecca; Sawaya, Michael R.; Balbirnie, Melinda Nature, Vol. 435, Issue 7043 https://doi.org/10.1038/nature03680	journal	June 2005
Prion detection by an amyloid seeding assay Colby, D. W.; Zhang, Q.; Wang, S. Proceedings of the National Academy of Sciences, Vol. 104, Issue 52 https://doi.org/10.1073/pnas.0710152105	journal	December 2007
Safety and Efficacy of RNAi Therapy for Transthyretin Amyloidosis Coelho, Teresa; Adams, David; Silva, Ana New England Journal of Medicine, Vol. 369, Issue 9 https://doi.org/10.1056/NEJMoa1208760	journal	August 2013
Effect of Orthotopic Liver Transplantation on the Progression of Familial Amyloidotic Polyneuropathy Pomfret, Elizabeth A.; Lewis, W. David; Jenkins, Roger L. Transplantation, Vol. 65, Issue 7 https://doi.org/10.1097/00007890-199804150-00010	journal	January 1998
PROGRESSIVE CARDIAC AMYLOIDOSIS FOLLOWING LIVER TRANSPLANTATION FOR FAMILIAL AMYLOID POLYNEUROPATHY: Implications for Amyloid Fibrillogenesis Stangou, A. J.; Hawkins, P. N.; Heaton, N. D. Transplantation, Vol. 66, Issue 2 https://doi.org/10.1097/00007890-199807270-00016	journal	January 1998
Seeded growth of -amyloid fibrils from Alzheimer's brain-derived fibrils produces a distinct fibril structure Paravastu, A. K.; Qahwash, I.; Leapman, R. D. Proceedings of the National Academy of Sciences, Vol. 106, Issue 18 https://doi.org/10.1073/pnas.0812033106	journal	April 2009
Propagation of Tau Aggregates and Neurodegeneration Goedert, Michel; Eisenberg, David S.; Crowther, R. Anthony Annual Review of Neuroscience, Vol. 40, Issue 1 https://doi.org/10.1146/annurev-neuro-072116-031153	journal	July 2017

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