Antibodies to variable surface antigens induce antigenic variation in the intestinal parasite Giardia lamblia

Albano H. Tenaglia, Lucas A. Luján, Diego N. Ríos, Cecilia R. Molina, Victor Midlej, Paula A. Iribarren, María A. Berazategui, Alessandro Torri, Alicia Saura, Damián O. Peralta, Macarena Rodríguez-Walker, Elmer A. Fernández, Juan P. Petiti, Marianela C. Serradell, Pablo R. Gargantini, Tim Sparwasser, Vanina E. Alvarez, Wanderley Souza and Hugo D. Luján ()
Additional contact information
Albano H. Tenaglia: Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)/Universidad Católica de Córdoba (UCC)
Lucas A. Luján: Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)/Universidad Católica de Córdoba (UCC)
Diego N. Ríos: Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)/Universidad Católica de Córdoba (UCC)
Cecilia R. Molina: Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)/Universidad Católica de Córdoba (UCC)
Victor Midlej: Universidade Federal do Rio de Janeiro (UFRJ)
Paula A. Iribarren: Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)/Universidad Nacional de General San Martín (UNSAM)
María A. Berazategui: Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)/Universidad Nacional de General San Martín (UNSAM)
Alessandro Torri: Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)/Universidad Católica de Córdoba (UCC)
Alicia Saura: Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)/Universidad Católica de Córdoba (UCC)
Damián O. Peralta: Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)/Universidad Católica de Córdoba (UCC)
Macarena Rodríguez-Walker: Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)/Universidad Católica de Córdoba (UCC)
Elmer A. Fernández: Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)/Universidad Católica de Córdoba (UCC)
Juan P. Petiti: Centro de Microscopía Electrónica, Facultad de Ciencias Médicas. CONICET/Universidad Nacional de Córdoba
Marianela C. Serradell: Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)/Universidad Católica de Córdoba (UCC)
Pablo R. Gargantini: Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)/Universidad Católica de Córdoba (UCC)
Tim Sparwasser: University Medical Center of the Johannes Gutenberg-University Mainz
Vanina E. Alvarez: Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)/Universidad Nacional de General San Martín (UNSAM)
Wanderley Souza: Universidade Federal do Rio de Janeiro (UFRJ)
Hugo D. Luján: Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)/Universidad Católica de Córdoba (UCC)

Nature Communications, 2023, vol. 14, issue 1, 1-13

Abstract: Abstract The genomes of most protozoa encode families of variant surface antigens. In some parasitic microorganisms, it has been demonstrated that mutually exclusive changes in the expression of these antigens allow parasites to evade the host’s immune response. It is widely assumed that antigenic variation in protozoan parasites is accomplished by the spontaneous appearance within the population of cells expressing antigenic variants that escape antibody-mediated cytotoxicity. Here we show, both in vitro and in animal infections, that antibodies to Variant-specific Surface Proteins (VSPs) of the intestinal parasite Giardia lamblia are not cytotoxic, inducing instead VSP clustering into liquid-ordered phase membrane microdomains that trigger a massive release of microvesicles carrying the original VSP and switch in expression to different VSPs by a calcium-dependent mechanism. This novel mechanism of surface antigen clearance throughout its release into microvesicles coupled to the stochastic induction of new phenotypic variants not only changes current paradigms of antigenic switching but also provides a new framework for understanding the course of protozoan infections as a host/parasite adaptive process.

Date: 2023
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DOI: 10.1038/s41467-023-38317-8

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