20S proteasomes secreted by the malaria parasite promote its growth

Elya Dekel, Dana Yaffe, Irit Rosenhek-Goldian, Gili Ben-Nissan, Yifat Ofir-Birin, Mattia I. Morandi, Tamar Ziv, Xavier Sisquella, Matthew A. Pimentel, Thomas Nebl, Eugene Kapp, Yael Ohana Daniel, Paula Abou Karam, Daniel Alfandari, Ron Rotkopf, Shimrit Malihi, Tal Block Temin, Debakshi Mullick, Or-Yam Revach, Ariel Rudik, Nir S. Gov, Ido Azuri, Ziv Porat, Giulia Bergamaschi, Raya Sorkin, Gijs J. L. Wuite, Ori Avinoam, Teresa G. Carvalho, Sidney R. Cohen, Michal Sharon () and Neta Regev-Rudzki ()
Additional contact information
Elya Dekel: Weizmann Institute of Science
Dana Yaffe: Weizmann Institute of Science
Irit Rosenhek-Goldian: Weizmann Institute of Science
Gili Ben-Nissan: Weizmann Institute of Science
Yifat Ofir-Birin: Weizmann Institute of Science
Mattia I. Morandi: Weizmann Institute of Science
Tamar Ziv: Technion - Israel Institute of Technology
Xavier Sisquella: The Walter and Eliza Hall Institute of Medical Research
Matthew A. Pimentel: The Walter and Eliza Hall Institute of Medical Research
Thomas Nebl: The Walter and Eliza Hall Institute of Medical Research
Eugene Kapp: The Walter and Eliza Hall Institute of Medical Research
Yael Ohana Daniel: Weizmann Institute of Science
Paula Abou Karam: Weizmann Institute of Science
Daniel Alfandari: Weizmann Institute of Science
Ron Rotkopf: Weizmann Institute of Science
Shimrit Malihi: Weizmann Institute of Science
Tal Block Temin: Weizmann Institute of Science
Debakshi Mullick: Weizmann Institute of Science
Or-Yam Revach: Weizmann Institute of Science
Ariel Rudik: Weizmann Institute of Science
Nir S. Gov: Weizmann Institute of Science
Ido Azuri: Weizmann Institute of Science
Ziv Porat: Flow Cytometry Unit, Life Sciences Core Facilities, Weizmann Institute of Science
Giulia Bergamaschi: Vrije Universiteit Amsterdam
Raya Sorkin: Tel Aviv University
Gijs J. L. Wuite: Vrije Universiteit Amsterdam
Ori Avinoam: Weizmann Institute of Science
Teresa G. Carvalho: La Trobe University
Sidney R. Cohen: Weizmann Institute of Science
Michal Sharon: Weizmann Institute of Science
Neta Regev-Rudzki: Weizmann Institute of Science

Nature Communications, 2021, vol. 12, issue 1, 1-19

Abstract: Abstract Mature red blood cells (RBCs) lack internal organelles and canonical defense mechanisms, making them both a fascinating host cell, in general, and an intriguing choice for the deadly malaria parasite Plasmodium falciparum (Pf), in particular. Pf, while growing inside its natural host, the human RBC, secretes multipurpose extracellular vesicles (EVs), yet their influence on this essential host cell remains unknown. Here we demonstrate that Pf parasites, cultured in fresh human donor blood, secrete within such EVs assembled and functional 20S proteasome complexes (EV-20S). The EV-20S proteasomes modulate the mechanical properties of naïve human RBCs by remodeling their cytoskeletal network. Furthermore, we identify four degradation targets of the secreted 20S proteasome, the phosphorylated cytoskeletal proteins β-adducin, ankyrin-1, dematin and Epb4.1. Overall, our findings reveal a previously unknown 20S proteasome secretion mechanism employed by the human malaria parasite, which primes RBCs for parasite invasion by altering membrane stiffness, to facilitate malaria parasite growth.

Date: 2021
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DOI: 10.1038/s41467-021-21344-8

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