IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-34743-2.html
   My bibliography  Save this article

Cryo-EM structure of ex vivo fibrils associated with extreme AA amyloidosis prevalence in a cat shelter

Author

Listed:
  • Tim Schulte

    (IRCCS Policlinico San Donato)

  • Antonio Chaves-Sanjuan

    (Università degli Studi di Milano
    Università degli Studi di Milano)

  • Giulia Mazzini

    (University of Pavia
    Fondazione IRCCS Policlinico San Matteo)

  • Valentina Speranzini

    (Università degli Studi di Milano)

  • Francesca Lavatelli

    (University of Pavia)

  • Filippo Ferri

    (AniCura Istituto Veterinario Novara)

  • Carlo Palizzotto

    (AniCura Istituto Veterinario Novara)

  • Maria Mazza

    (Istituto Zooprofilattico Sperimentale del Piemonte Liguria e Valle d’Aosta, S.C. Diagnostica Specialistica)

  • Paolo Milani

    (University of Pavia
    Fondazione IRCCS Policlinico San Matteo)

  • Mario Nuvolone

    (University of Pavia
    Fondazione IRCCS Policlinico San Matteo)

  • Anne-Cathrine Vogt

    (University of Bern
    University Hospital Bern)

  • Monique Vogel

    (University of Bern
    University Hospital Bern)

  • Giovanni Palladini

    (University of Pavia
    Fondazione IRCCS Policlinico San Matteo)

  • Giampaolo Merlini

    (University of Pavia
    Fondazione IRCCS Policlinico San Matteo)

  • Martino Bolognesi

    (Università degli Studi di Milano
    Università degli Studi di Milano)

  • Silvia Ferro

    (University of Padova)

  • Eric Zini

    (AniCura Istituto Veterinario Novara
    University of Padua
    University of Zurich)

  • Stefano Ricagno

    (IRCCS Policlinico San Donato
    Università degli Studi di Milano)

Abstract

AA amyloidosis is a systemic disease characterized by deposition of misfolded serum amyloid A protein (SAA) into cross-β amyloid in multiple organs in humans and animals. AA amyloidosis occurs at high SAA serum levels during chronic inflammation. Prion-like transmission was reported as possible cause of extreme AA amyloidosis prevalence in captive animals, e.g. 70% in cheetah and 57–73% in domestic short hair (DSH) cats kept in zoos and shelters, respectively. Herein, we present the 3.3 Å cryo-EM structure of AA amyloid extracted post-mortem from the kidney of a DSH cat with renal failure, deceased in a shelter with extreme disease prevalence. The structure reveals a cross-β architecture assembled from two 76-residue long proto-filaments. Despite >70% sequence homology to mouse and human SAA, the cat SAA variant adopts a distinct amyloid fold. Inclusion of an eight-residue insert unique to feline SAA contributes to increased amyloid stability. The presented feline AA amyloid structure is fully compatible with the 99% identical amino acid sequence of amyloid fragments of captive cheetah.

Suggested Citation

  • Tim Schulte & Antonio Chaves-Sanjuan & Giulia Mazzini & Valentina Speranzini & Francesca Lavatelli & Filippo Ferri & Carlo Palizzotto & Maria Mazza & Paolo Milani & Mario Nuvolone & Anne-Cathrine Vogt, 2022. "Cryo-EM structure of ex vivo fibrils associated with extreme AA amyloidosis prevalence in a cat shelter," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-34743-2
    DOI: 10.1038/s41467-022-34743-2
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-34743-2
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-34743-2?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Paolo Swuec & Francesca Lavatelli & Masayoshi Tasaki & Cristina Paissoni & Paola Rognoni & Martina Maritan & Francesca Brambilla & Paolo Milani & Pierluigi Mauri & Carlo Camilloni & Giovanni Palladini, 2019. "Cryo-EM structure of cardiac amyloid fibrils from an immunoglobulin light chain AL amyloidosis patient," Nature Communications, Nature, vol. 10(1), pages 1-9, December.
    2. Akanksha Bansal & Matthias Schmidt & Matthies Rennegarbe & Christian Haupt & Falk Liberta & Sabrina Stecher & Ioana Puscalau-Girtu & Alexander Biedermann & Marcus Fändrich, 2021. "AA amyloid fibrils from diseased tissue are structurally different from in vitro formed SAA fibrils," Nature Communications, Nature, vol. 12(1), pages 1-9, December.
    3. Jay R. Silveira & Gregory J. Raymond & Andrew G. Hughson & Richard E. Race & Valerie L. Sim & Stanley F. Hayes & Byron Caughey, 2005. "The most infectious prion protein particles," Nature, Nature, vol. 437(7056), pages 257-261, September.
    4. Falk Liberta & Sarah Loerch & Matthies Rennegarbe & Angelika Schierhorn & Per Westermark & Gunilla T. Westermark & Bouke P. C. Hazenberg & Nikolaus Grigorieff & Marcus Fändrich & Matthias Schmidt, 2019. "Cryo-EM fibril structures from systemic AA amyloidosis reveal the species complementarity of pathological amyloids," Nature Communications, Nature, vol. 10(1), pages 1-10, December.
    5. Adriano Aguzzi, 2009. "Beyond the prion principle," Nature, Nature, vol. 459(7249), pages 924-925, June.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Sara Karimi-Farsijani & Peter Benedikt Pfeiffer & Sambhasan Banerjee & Julian Baur & Lukas Kuhn & Niklas Kupfer & Ute Hegenbart & Stefan O. Schönland & Sebastian Wiese & Christian Haupt & Matthias Sch, 2024. "Light chain mutations contribute to defining the fibril morphology in systemic AL amyloidosis," Nature Communications, Nature, vol. 15(1), pages 1-8, December.
    2. Martin Wilkinson & Rodrigo U. Gallardo & Roberto Maya Martinez & Nicolas Guthertz & Masatomo So & Liam D. Aubrey & Sheena E. Radford & Neil A. Ranson, 2023. "Disease-relevant β2-microglobulin variants share a common amyloid fold," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    3. Kartikay Sharma & Fabian Stockert & Jayakrishna Shenoy & Mélanie Berbon & Muhammed Bilal Abdul-Shukkoor & Birgit Habenstein & Antoine Loquet & Matthias Schmidt & Marcus Fändrich, 2024. "Cryo-EM observation of the amyloid key structure of polymorphic TDP-43 amyloid fibrils," Nature Communications, Nature, vol. 15(1), pages 1-8, December.
    4. Lynn Radamaker & Sara Karimi-Farsijani & Giada Andreotti & Julian Baur & Matthias Neumann & Sarah Schreiner & Natalie Berghaus & Raoul Motika & Christian Haupt & Paul Walther & Volker Schmidt & Stefan, 2021. "Role of mutations and post-translational modifications in systemic AL amyloidosis studied by cryo-EM," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
    5. Nikolaos Louros & Meine Ramakers & Emiel Michiels & Katerina Konstantoulea & Chiara Morelli & Teresa Garcia & Nele Moonen & Sam D’Haeyer & Vera Goossens & Dietmar Rudolf Thal & Dominique Audenaert & F, 2022. "Mapping the sequence specificity of heterotypic amyloid interactions enables the identification of aggregation modifiers," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    6. Binh An Nguyen & Virender Singh & Shumaila Afrin & Anna Yakubovska & Lanie Wang & Yasmin Ahmed & Rose Pedretti & Maria del Carmen Fernandez-Ramirez & Preeti Singh & Maja Pękała & Luis O. Cabrera Herna, 2024. "Structural polymorphism of amyloid fibrils in ATTR amyloidosis revealed by cryo-electron microscopy," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    7. Tim Schulte & Antonio Chaves-Sanjuan & Valentina Speranzini & Kevin Sicking & Melissa Milazzo & Giulia Mazzini & Paola Rognoni & Serena Caminito & Paolo Milani & Chiara Marabelli & Alessandro Corbelli, 2024. "Helical superstructures between amyloid and collagen in cardiac fibrils from a patient with AL amyloidosis," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    8. Sambhasan Banerjee & Julian Baur & Christoph Daniel & Peter Benedikt Pfeiffer & Manuel Hitzenberger & Lukas Kuhn & Sebastian Wiese & Johan Bijzet & Christian Haupt & Kerstin U. Amann & Martin Zacharia, 2022. "Amyloid fibril structure from the vascular variant of systemic AA amyloidosis," Nature Communications, Nature, vol. 13(1), pages 1-8, December.
    9. Irina Iakovleva & Michael Hall & Melanie Oelker & Linda Sandblad & Intissar Anan & A. Elisabeth Sauer-Eriksson, 2021. "Structural basis for transthyretin amyloid formation in vitreous body of the eye," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    10. Javier Garcia-Pardo & Andrea Bartolomé-Nafría & Antonio Chaves-Sanjuan & Marcos Gil-Garcia & Cristina Visentin & Martino Bolognesi & Stefano Ricagno & Salvador Ventura, 2023. "Cryo-EM structure of hnRNPDL-2 fibrils, a functional amyloid associated with limb-girdle muscular dystrophy D3," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    11. Maximilian Steinebrei & Julian Baur & Anaviggha Pradhan & Niklas Kupfer & Sebastian Wiese & Ute Hegenbart & Stefan O. Schönland & Matthias Schmidt & Marcus Fändrich, 2023. "Common transthyretin-derived amyloid fibril structures in patients with hereditary ATTR amyloidosis," Nature Communications, Nature, vol. 14(1), pages 1-8, December.
    12. Stephen J. Klawa & Michelle Lee & Kyle D. Riker & Tengyue Jian & Qunzhao Wang & Yuan Gao & Margaret L. Daly & Shreeya Bhonge & W. Seth Childers & Tolulope O. Omosun & Anil K. Mehta & David G. Lynn & R, 2024. "Uncovering supramolecular chirality codes for the design of tunable biomaterials," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    13. Mookyung Cheon & Iksoo Chang & Sandipan Mohanty & Leila M Luheshi & Christopher M Dobson & Michele Vendruscolo & Giorgio Favrin, 2007. "Structural Reorganisation and Potential Toxicity of Oligomeric Species Formed during the Assembly of Amyloid Fibrils," PLOS Computational Biology, Public Library of Science, vol. 3(9), pages 1-12, September.
    14. Pamina Kazman & Ramona M. Absmeier & Harald Engelhardt & Johannes Buchner, 2021. "Dissection of the amyloid formation pathway in AL amyloidosis," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    15. Thomas Heerde & Desiree Schütz & Yu-Jie Lin & Jan Münch & Matthias Schmidt & Marcus Fändrich, 2023. "Cryo-EM structure and polymorphic maturation of a viral transduction enhancing amyloid fibril," Nature Communications, Nature, vol. 14(1), pages 1-8, December.
    16. Juan Manuel Ribes & Mitali P. Patel & Hazim A. Halim & Antonio Berretta & Sharon A. Tooze & Peter-Christian Klöhn, 2023. "Prion protein conversion at two distinct cellular sites precedes fibrillisation," Nature Communications, Nature, vol. 14(1), pages 1-19, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-34743-2. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.