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Toxicity of eosinophil MBP is repressed by intracellular crystallization and promoted by extracellular aggregation.

Soragni A, Yousefi S, Stoeckle C, Soriaga AB, Sawaya MR, Kozlowski E, Schmid I, Radonjic-Hoesli S, Boutet S, Williams GJ, Messerschmidt M, Seibert MM, Cascio D, Zatsepin NA, Burghammer M, Riekel C, Colletier JP, Riek R, Eisenberg DS, Simon HU
Mol Cell 57 1011-1021 (2015)
Cited: 53 times
EuropePMC logo PMID: 25728769

Abstract

Eosinophils are white blood cells that function in innate immunity and participate in the pathogenesis of various inflammatory and neoplastic disorders. Their secretory granules contain four cytotoxic proteins, including the eosinophil major basic protein (MBP-1). How MBP-1 toxicity is controlled within the eosinophil itself and activated upon extracellular release is unknown. Here we show how intragranular MBP-1 nanocrystals restrain toxicity, enabling its safe storage, and characterize them with an X-ray-free electron laser. Following eosinophil activation, MBP-1 toxicity is triggered by granule acidification, followed by extracellular aggregation, which mediates the damage to pathogens and host cells. Larger non-toxic amyloid plaques are also present in tissues of eosinophilic patients in a feedback mechanism that likely limits tissue damage under pathological conditions of MBP-1 oversecretion. Our results suggest that MBP-1 aggregation is important for innate immunity and immunopathology mediated by eosinophils and clarify how its polymorphic self-association pathways regulate toxicity intra- and extracellularly.

Articles - 4qxx mentioned but not cited (2)

  1. Toxicity of eosinophil MBP is repressed by intracellular crystallization and promoted by extracellular aggregation. Soragni A, Yousefi S, Stoeckle C, Soriaga AB, Sawaya MR, Kozlowski E, Schmid I, Radonjic-Hoesli S, Boutet S, Williams GJ, Messerschmidt M, Seibert MM, Cascio D, Zatsepin NA, Burghammer M, Riekel C, Colletier JP, Riek R, Eisenberg DS, Simon HU. Mol Cell 57 1011-1021 (2015)
  2. Autonomous aggregation suppression by acidic residues explains why chaperones favour basic residues. Houben B, Michiels E, Ramakers M, Konstantoulea K, Louros N, Verniers J, van der Kant R, De Vleeschouwer M, Chicória N, Vanpoucke T, Gallardo R, Schymkowitz J, Rousseau F. EMBO J 39 e102864 (2020)


Reviews citing this publication (23)

  1. Cellular and molecular immunologic mechanisms in patients with atopic dermatitis. Werfel T, Allam JP, Biedermann T, Eyerich K, Gilles S, Guttman-Yassky E, Hoetzenecker W, Knol E, Simon HU, Wollenberg A, Bieber T, Lauener R, Schmid-Grendelmeier P, Traidl-Hoffmann C, Akdis CA. J Allergy Clin Immunol 138 336-349 (2016)
  2. Functional Amyloids. Otzen D, Riek R. Cold Spring Harb Perspect Biol 11 a033860 (2019)
  3. Alzheimer's Amyloid-β is an Antimicrobial Peptide: A Review of the Evidence. Gosztyla ML, Brothers HM, Robinson SR. J Alzheimers Dis 62 1495-1506 (2018)
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  5. Eosinophils in Autoimmune Diseases. Diny NL, Rose NR, Čiháková D. Front Immunol 8 484 (2017)
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  9. Rethinking neutrophils and eosinophils in chronic rhinosinusitis. Delemarre T, Bochner BS, Simon HU, Bachert C. J Allergy Clin Immunol 148 327-335 (2021)
  10. Eosinophilic Granulomatosis With Polyangiitis: Dissecting the Pathophysiology. Fagni F, Bello F, Emmi G. Front Med (Lausanne) 8 627776 (2021)
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  12. The Use of Antimicrobial and Antiviral Drugs in Alzheimer's Disease. Iqbal UH, Zeng E, Pasinetti GM. Int J Mol Sci 21 E4920 (2020)
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  17. Eosinophilia in Dermatologic Disorders. de Graauw E, Beltraminelli H, Simon HU, Simon D. Immunol Allergy Clin North Am 35 545-560 (2015)
  18. Eosinophils in skin diseases. Radonjic-Hoesli S, Brüggen MC, Feldmeyer L, Simon HU, Simon D. Semin Immunopathol 43 393-409 (2021)
  19. Intestinal eosinophils, homeostasis and response to bacterial intrusion. Gurtner A, Gonzalez-Perez I, Arnold IC. Semin Immunopathol 43 295-306 (2021)
  20. Eosinophil-mediated inflammation in the absence of eosinophilia. Miyabe Y, Kobayashi Y, Fukuchi M, Saga A, Moritoki Y, Saga T, Akuthota P, Ueki S. Asia Pac Allergy 11 e30 (2021)
  21. Structural insights into functional amyloid inhibition in Gram -ve bacteria. Hawthorne W, Rouse S, Sewell L, Matthews SJ. Biochem Soc Trans 44 1643-1649 (2016)
  22. Galectin-10 as a Potential Biomarker for Eosinophilic Diseases. Tomizawa H, Yamada Y, Arima M, Miyabe Y, Fukuchi M, Hikichi H, Melo RCN, Yamada T, Ueki S. Biomolecules 12 1385 (2022)
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Articles citing this publication (28)

  1. The transcription factor XBP1 is selectively required for eosinophil differentiation. Bettigole SE, Lis R, Adoro S, Lee AH, Spencer LA, Weller PF, Glimcher LH. Nat Immunol 16 829-837 (2015)
  2. Eosinophil-platelet interactions promote atherosclerosis and stabilize thrombosis with eosinophil extracellular traps. Marx C, Novotny J, Salbeck D, Zellner KR, Nicolai L, Pekayvaz K, Kilani B, Stockhausen S, Bürgener N, Kupka D, Stocker TJ, Weckbach LT, Pircher J, Moser M, Joner M, Desmet W, Adriaenssens T, Neumann FJ, Gerschlick AH, Ten Berg JM, Lorenz M, Stark K. Blood 134 1859-1872 (2019)
  3. Eosinophils suppress Th1 responses and restrict bacterially induced gastrointestinal inflammation. Arnold IC, Artola-Borán M, Tallón de Lara P, Kyburz A, Taube C, Ottemann K, van den Broek M, Yousefi S, Simon HU, Müller A. J Exp Med 215 2055-2072 (2018)
  4. Evidence for a role of eosinophils in blister formation in bullous pemphigoid. de Graauw E, Sitaru C, Horn M, Borradori L, Yousefi S, Simon HU, Simon D. Allergy 72 1105-1113 (2017)
  5. Extracellular eosinophilic traps in association with Staphylococcus aureus at the site of epithelial barrier defects in patients with severe airway inflammation. Gevaert E, Zhang N, Krysko O, Lan F, Holtappels G, De Ruyck N, Nauwynck H, Yousefi S, Simon HU, Bachert C. J Allergy Clin Immunol 139 1849-1860.e6 (2017)
  6. Preeclampsia: novel insights from global RNA profiling of trophoblast subpopulations. Gormley M, Ona K, Kapidzic M, Garrido-Gomez T, Zdravkovic T, Fisher SJ. Am J Obstet Gynecol 217 200.e1-200.e17 (2017)
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  8. Extreme amyloid polymorphism in Staphylococcus aureus virulent PSMα peptides. Salinas N, Colletier JP, Moshe A, Landau M. Nat Commun 9 3512 (2018)
  9. Structural Insights into Curli CsgA Cross-β Fibril Architecture Inspire Repurposing of Anti-amyloid Compounds as Anti-biofilm Agents. Perov S, Lidor O, Salinas N, Golan N, Tayeb-Fligelman E, Deshmukh M, Willbold D, Landau M. PLoS Pathog 15 e1007978 (2019)
  10. Electrostatically-guided inhibition of Curli amyloid nucleation by the CsgC-like family of chaperones. Taylor JD, Hawthorne WJ, Lo J, Dear A, Jain N, Meisl G, Andreasen M, Fletcher C, Koch M, Darvill N, Scull N, Escalera-Maurer A, Sefer L, Wenman R, Lambert S, Jean J, Xu Y, Turner B, Kazarian SG, Chapman MR, Bubeck D, de Simone A, Knowles TP, Matthews SJ. Sci Rep 6 24656 (2016)
  11. A new class of hybrid secretion system is employed in Pseudomonas amyloid biogenesis. Rouse SL, Hawthorne WJ, Berry JL, Chorev DS, Ionescu SA, Lambert S, Stylianou F, Ewert W, Mackie U, Morgan RML, Otzen D, Herbst FA, Nielsen PH, Dueholm M, Bayley H, Robinson CV, Hare S, Matthews S. Nat Commun 8 263 (2017)
  12. Eosinophil extracellular traps drive asthma progression through neuro-immune signals. Lu Y, Huang Y, Li J, Huang J, Zhang L, Feng J, Li J, Xia Q, Zhao Q, Huang L, Jiang S, Su S. Nat Cell Biol 23 1060-1072 (2021)
  13. The three-dimensional structure of human β-endorphin amyloid fibrils. Seuring C, Verasdonck J, Gath J, Ghosh D, Nespovitaya N, Wälti MA, Maji SK, Cadalbert R, Güntert P, Meier BH, Riek R. Nat Struct Mol Biol 27 1178-1184 (2020)
  14. Cystatin F Ensures Eosinophil Survival by Regulating Granule Biogenesis. Matthews SP, McMillan SJ, Colbert JD, Lawrence RA, Watts C. Immunity 44 795-806 (2016)
  15. Eosinophil ETosis-Mediated Release of Galectin-10 in Eosinophilic Granulomatosis With Polyangiitis. Fukuchi M, Kamide Y, Ueki S, Miyabe Y, Konno Y, Oka N, Takeuchi H, Koyota S, Hirokawa M, Yamada T, Melo RCN, Weller PF, Taniguchi M. Arthritis Rheumatol 73 1683-1693 (2021)
  16. Eosinophil-derived CCL-6 impairs hematopoietic stem cell homeostasis. Zhang C, Yi W, Li F, Du X, Wang H, Wu P, Peng C, Luo M, Hua W, Wong CC, Lee JJ, Li W, Chen Z, Ying S, Ju Z, Shen H. Cell Res 28 323-335 (2018)
  17. Editorial New future of cell biology and toxicology: thinking deeper. Gu J, Wang X. Cell Biol Toxicol 32 1-3 (2016)
  18. RhoH is a negative regulator of eosinophilopoiesis. Stoeckle C, Geering B, Yousefi S, Rožman S, Andina N, Benarafa C, Simon HU. Cell Death Differ 23 1961-1972 (2016)
  19. The Cryo-EM structures of two amphibian antimicrobial cross-β amyloid fibrils. Bücker R, Seuring C, Cazey C, Veith K, García-Alai M, Grünewald K, Landau M. Nat Commun 13 4356 (2022)
  20. Identification of gene expression predictors of occupational benzene exposure. Schiffman C, McHale CM, Hubbard AE, Zhang L, Thomas R, Vermeulen R, Li G, Shen M, Rappaport SM, Yin S, Lan Q, Smith MT, Rothman N. PLoS One 13 e0205427 (2018)
  21. Rapid Evolution of Primate Type 2 Immune Response Factors Linked to Asthma Susceptibility. Barber MF, Lee EM, Griffin H, Elde NC. Genome Biol Evol 9 1757-1765 (2017)
  22. Cyclophilin D regulates necrosis, but not apoptosis, of murine eosinophils. Zhu X, Hogan SP, Molkentin JD, Zimmermann N. Am J Physiol Gastrointest Liver Physiol 310 G609-17 (2016)
  23. CCL4 Regulates Eosinophil Activation in Eosinophilic Airway Inflammation. Chu HH, Kobayashi Y, Bui DV, Yun Y, Nguyen LM, Mitani A, Suzuki K, Asako M, Kanda A, Iwai H. Int J Mol Sci 23 16149 (2022)
  24. Multi-Dimensional Structure and Dynamics Landscape of Proteins in Mammalian Cells Revealed by In-Cell NMR. Kadavath H, Cecilia Prymaczok N, Eichmann C, Riek R, Gerez JA. Angew Chem Int Ed Engl 62 e202213976 (2023)
  25. article-commentary Novel roles for XBP1 in hematopoietic development. Bettigole SE, Glimcher LH. Cell Cycle 15 1653-1654 (2016)
  26. Serum Levels of Eosinophil-derived Neurotoxin in Patients with Chronic Urticaria. Saleh AA, Al-Obaidi AM, Behiry EG, Hamed AM. J Clin Aesthet Dermatol 13 21-23 (2020)
  27. GWAS of genetic factors affecting white blood cell morphological parameters in Sardinians uncovers influence of chromosome 11 innate immunity gene cluster on eosinophil morphology. Marongiu M, Pérez-Mejías G, Orrù V, Steri M, Sidore C, Díaz-Quintana A, Mulas A, Busonero F, Maschio A, Walter K, Tardaguila M, Akbari P, Soranzo N, Fiorillo E, Gorospe M, Schlessinger D, Díaz-Moreno I, Cucca F, Zoledziewska M. Hum Mol Genet 32 790-797 (2023)
  28. Eosinophils of patients with localized and diffuse cutaneous leishmaniasis: Differential response to Leishmania mexicana, with insights into mechanisms of damage inflicted upon the parasites by eosinophils. Salaiza-Suazo N, Porcel-Aranibar R, Cañeda-Guzmán IC, Ruiz-Remigio A, Zamora-Chimal J, Delgado-Domínguez J, Cervantes-Sarabia R, Carrada-Figueroa G, Sánchez-Barragán B, Leal-Ascencio VJ, Pérez-Torres A, Rodríguez-Martínez HA, Becker I. PLoS One 19 e0296887 (2024)


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