Biophysical Tools and Concepts Enable Understanding of Asexual Blood Stage Malaria

Forces and mechanical properties of cells and tissues set constraints on biological functions, and are key determinants of human physiology. Changes in cell mechanics may arise from disease, or directly contribute to pathogenesis. Malaria gives many striking examples. Plasmodium parasites, the causa...

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Published inFrontiers in cellular and infection microbiology Vol. 12; p. 908241
Main Authors Introini, Viola, Govendir, Matt A., Rayner, Julian C., Cicuta, Pietro, Bernabeu, Maria
Format Journal Article
LanguageEnglish
Published Frontiers Media S.A 31.05.2022
Subjects
biophysics
Cellular and Infection Microbiology
cytoadhesion
imaging
malaria
microfluidics
Plasmodium
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Abstract Forces and mechanical properties of cells and tissues set constraints on biological functions, and are key determinants of human physiology. Changes in cell mechanics may arise from disease, or directly contribute to pathogenesis. Malaria gives many striking examples. Plasmodium parasites, the causative agents of malaria, are single-celled organisms that cannot survive outside their hosts; thus, thost-pathogen interactions are fundamental for parasite’s biological success and to the host response to infection. These interactions are often combinations of biochemical and mechanical factors, but most research focuses on the molecular side. However, Plasmodium infection of human red blood cells leads to changes in their mechanical properties, which has a crucial impact on disease pathogenesis because of the interaction of infected red blood cells with other human tissues through various adhesion mechanisms, which can be probed and modelled with biophysical techniques. Recently, natural polymorphisms affecting red blood cell biomechanics have also been shown to protect human populations, highlighting the potential of understanding biomechanical factors to inform future vaccines and drug development. Here we review biophysical techniques that have revealed new aspects of Plasmodium falciparum invasion of red blood cells and cytoadhesion of infected cells to the host vasculature. These mechanisms occur differently across Plasmodium species and are linked to malaria pathogenesis. We highlight promising techniques from the fields of bioengineering, immunomechanics, and soft matter physics that could be beneficial for studying malaria. Some approaches might also be applied to other phases of the malaria lifecycle and to apicomplexan infections with complex host-pathogen interactions.
AbstractList Forces and mechanical properties of cells and tissues set constraints on biological functions, and are key determinants of human physiology. Changes in cell mechanics may arise from disease, or directly contribute to pathogenesis. Malaria gives many striking examples. Plasmodium parasites, the causative agents of malaria, are single-celled organisms that cannot survive outside their hosts; thus, thost-pathogen interactions are fundamental for parasite’s biological success and to the host response to infection. These interactions are often combinations of biochemical and mechanical factors, but most research focuses on the molecular side. However, Plasmodium infection of human red blood cells leads to changes in their mechanical properties, which has a crucial impact on disease pathogenesis because of the interaction of infected red blood cells with other human tissues through various adhesion mechanisms, which can be probed and modelled with biophysical techniques. Recently, natural polymorphisms affecting red blood cell biomechanics have also been shown to protect human populations, highlighting the potential of understanding biomechanical factors to inform future vaccines and drug development. Here we review biophysical techniques that have revealed new aspects of Plasmodium falciparum invasion of red blood cells and cytoadhesion of infected cells to the host vasculature. These mechanisms occur differently across Plasmodium species and are linked to malaria pathogenesis. We highlight promising techniques from the fields of bioengineering, immunomechanics, and soft matter physics that could be beneficial for studying malaria. Some approaches might also be applied to other phases of the malaria lifecycle and to apicomplexan infections with complex host-pathogen interactions.
Forces and mechanical properties of cells and tissues set constraints on biological functions, and are key determinants of human physiology. Changes in cell mechanics may arise from disease, or directly contribute to pathogenesis. Malaria gives many striking examples. Plasmodium parasites, the causative agents of malaria, are single-celled organisms that cannot survive outside their hosts; thus, thost-pathogen interactions are fundamental for parasite’s biological success and to the host response to infection. These interactions are often combinations of biochemical and mechanical factors, but most research focuses on the molecular side. However, Plasmodium infection of human red blood cells leads to changes in their mechanical properties, which has a crucial impact on disease pathogenesis because of the interaction of infected red blood cells with other human tissues through various adhesion mechanisms, which can be probed and modelled with biophysical techniques. Recently, natural polymorphisms affecting red blood cell biomechanics have also been shown to protect human populations, highlighting the potential of understanding biomechanical factors to inform future vaccines and drug development. Here we review biophysical techniques that have revealed new aspects of Plasmodium falciparum invasion of red blood cells and cytoadhesion of infected cells to the host vasculature. These mechanisms occur differently across Plasmodium species and are linked to malaria pathogenesis. We highlight promising techniques from the fields of bioengineering, immunomechanics, and soft matter physics that could be beneficial for studying malaria. Some approaches might also be applied to other phases of the malaria lifecycle and to apicomplexan infections with complex host-pathogen interactions.
Author Introini, Viola
Rayner, Julian C.
Cicuta, Pietro
Bernabeu, Maria
Govendir, Matt A.
AuthorAffiliation 3 European Molecular Biology Laboratory (EMBL) Barcelona , Barcelona , Spain
1 Cambridge Institute for Medical Research, University of Cambridge , Cambridge , United Kingdom
2 Cavendish Laboratory, University of Cambridge , Cambridge , United Kingdom
AuthorAffiliation_xml – name: 3 European Molecular Biology Laboratory (EMBL) Barcelona , Barcelona , Spain
– name: 1 Cambridge Institute for Medical Research, University of Cambridge , Cambridge , United Kingdom
– name: 2 Cavendish Laboratory, University of Cambridge , Cambridge , United Kingdom
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  givenname: Matt A.
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  fullname: Govendir, Matt A.
– sequence: 3
  givenname: Julian C.
  surname: Rayner
  fullname: Rayner, Julian C.
– sequence: 4
  givenname: Pietro
  surname: Cicuta
  fullname: Cicuta, Pietro
– sequence: 5
  givenname: Maria
  surname: Bernabeu
  fullname: Bernabeu, Maria
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CitedBy_id crossref_primary_10_1021_acsinfecdis_3c00564
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Reviewed by: Catherine Lavazec, U1016 Institut Cochin (INSERM), France; Rajesh Chandramohanadas, Rajiv Gandhi Centre for Biotechnology, India
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ORCID: Viola Introini, orcid.org/0000-0001-9012-4696; Matt A. Govendir, orcid.org/0000-0002-2222-9143; Pietro Cicuta, orcid.org/0000-0002-9193-8496; Julian C. Rayner, orcid.org/0000-0002-9835-1014; Maria Bernabeu, orcid.org/0000-0001-7212-6209
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  year: 2011
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  article-title: Malaria: Surprising Mechanism of Merozoite Egress Revealed
  publication-title: Curr. Biol.
  doi: 10.1016/j.cub.2011.03.066
  contributor:
    fullname: Lew
– volume: 11
  start-page: e9164
  year: 2019
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  article-title: Cerebral Malaria Is Associated With Differential Cytoadherence to Brain Endothelial Cells
  publication-title: EMBO Mol. Med.
  doi: 10.15252/emmm.201809164
  contributor:
    fullname: Storm
– volume: 11
  start-page: 22099
  year: 2021
  ident: B50
  article-title: Pitting of Malaria Parasites in Microfluidic Devices Mimicking Spleen Interendothelial Slits
  publication-title: Sci. Rep.
  doi: 10.1038/s41598-021-01568-w
  contributor:
    fullname: Elizalde-Torrent
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Snippet Forces and mechanical properties of cells and tissues set constraints on biological functions, and are key determinants of human physiology. Changes in cell...
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SubjectTerms biophysics
Cellular and Infection Microbiology
cytoadhesion
imaging
malaria
microfluidics
Plasmodium
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Title Biophysical Tools and Concepts Enable Understanding of Asexual Blood Stage Malaria
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Volume 12
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