The Phosphoinositide Kinase PIKfyve Promotes Cathepsin-S-Mediated Major Histocompatibility Complex Class II Antigen Presentation

Antigen presentation to T cells in major histocompatibility complex class II (MHC class II) requires the conversion of early endo/phagosomes into lysosomes by a process called maturation. Maturation is driven by the phosphoinositide kinase PIKfyve. Blocking PIKfyve activity by small molecule inhibit...

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Published in	iScience Vol. 11; pp. 160 - 177
Main Authors	Baranov, Maksim V., Bianchi, Frans, Schirmacher, Anastasiya, van Aart, Melissa A.C., Maassen, Sjors, Muntjewerff, Elke M., Dingjan, Ilse, ter Beest, Martin, Verdoes, Martijn, Keyser, Samantha G.L., Bertozzi, Carolyn R., Diederichsen, Ulf, van den Bogaart, Geert
Format	Journal Article
Language	English
Published	United States Elsevier Inc 25.01.2019 Elsevier
Subjects	Immune Response Immunology Molecular Mechanism of Gene Regulation Molecular Mechanism of Gene Regulation Immune Response Immunology
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Abstract	Antigen presentation to T cells in major histocompatibility complex class II (MHC class II) requires the conversion of early endo/phagosomes into lysosomes by a process called maturation. Maturation is driven by the phosphoinositide kinase PIKfyve. Blocking PIKfyve activity by small molecule inhibitors caused a delay in the conversion of phagosomes into lysosomes and in phagosomal acidification, whereas production of reactive oxygen species (ROS) increased. Elevated ROS resulted in reduced activity of cathepsin S and B, but not X, causing a proteolytic defect of MHC class II chaperone invariant chain Ii processing. We developed a novel universal MHC class II presentation assay based on a bio-orthogonal “clickable” antigen and showed that MHC class II presentation was disrupted by the inhibition of PIKfyve, which in turn resulted in reduced activation of CD4+ T cells. Our results demonstrate a key role of PIKfyve in the processing and presentation of antigens, which should be taken into consideration when targeting PIKfyve in autoimmune disease and cancer. [Display omitted] •PIKfyve converts PI(3)P into PI(3,5)P2 on the surface of endosomes and phagosomes•PIKfyve of DCs modulates phagosomal maturation, acidification, and ROS production•PIKfyve defects disrupt cathepsin S trafficking and activity•Inactive cathepin S slows Ii processing for MHC class II trafficking and antigen loading Molecular Mechanism of Gene Regulation; Immunology; Immune Response
AbstractList	Antigen presentation to T cells in major histocompatibility complex class II (MHC class II) requires the conversion of early endo/phagosomes into lysosomes by a process called maturation. Maturation is driven by the phosphoinositide kinase PIKfyve. Blocking PIKfyve activity by small molecule inhibitors caused a delay in the conversion of phagosomes into lysosomes and in phagosomal acidification, whereas production of reactive oxygen species (ROS) increased. Elevated ROS resulted in reduced activity of cathepsin S and B, but not X, causing a proteolytic defect of MHC class II chaperone invariant chain Ii processing. We developed a novel universal MHC class II presentation assay based on a bio-orthogonal “clickable” antigen and showed that MHC class II presentation was disrupted by the inhibition of PIKfyve, which in turn resulted in reduced activation of CD4+ T cells. Our results demonstrate a key role of PIKfyve in the processing and presentation of antigens, which should be taken into consideration when targeting PIKfyve in autoimmune disease and cancer. [Display omitted] •PIKfyve converts PI(3)P into PI(3,5)P2 on the surface of endosomes and phagosomes•PIKfyve of DCs modulates phagosomal maturation, acidification, and ROS production•PIKfyve defects disrupt cathepsin S trafficking and activity•Inactive cathepin S slows Ii processing for MHC class II trafficking and antigen loading Molecular Mechanism of Gene Regulation; Immunology; Immune Response Antigen presentation to T cells in major histocompatibility complex class II (MHC class II) requires the conversion of early endo/phagosomes into lysosomes by a process called maturation. Maturation is driven by the phosphoinositide kinase PIKfyve. Blocking PIKfyve activity by small molecule inhibitors caused a delay in the conversion of phagosomes into lysosomes and in phagosomal acidification, whereas production of reactive oxygen species (ROS) increased. Elevated ROS resulted in reduced activity of cathepsin S and B, but not X, causing a proteolytic defect of MHC class II chaperone invariant chain Ii processing. We developed a novel universal MHC class II presentation assay based on a bio-orthogonal “clickable” antigen and showed that MHC class II presentation was disrupted by the inhibition of PIKfyve, which in turn resulted in reduced activation of CD4 + T cells. Our results demonstrate a key role of PIKfyve in the processing and presentation of antigens, which should be taken into consideration when targeting PIKfyve in autoimmune disease and cancer. • PIKfyve converts PI(3)P into PI(3,5)P 2 on the surface of endosomes and phagosomes • PIKfyve of DCs modulates phagosomal maturation, acidification, and ROS production • PIKfyve defects disrupt cathepsin S trafficking and activity • Inactive cathepin S slows Ii processing for MHC class II trafficking and antigen loading Molecular Mechanism of Gene Regulation; Immunology; Immune Response Antigen presentation to T cells in major histocompatibility complex class II (MHC class II) requires the conversion of early endo/phagosomes into lysosomes by a process called maturation. Maturation is driven by the phosphoinositide kinase PIKfyve. Blocking PIKfyve activity by small molecule inhibitors caused a delay in the conversion of phagosomes into lysosomes and in phagosomal acidification, whereas production of reactive oxygen species (ROS) increased. Elevated ROS resulted in reduced activity of cathepsin S and B, but not X, causing a proteolytic defect of MHC class II chaperone invariant chain Ii processing. We developed a novel universal MHC class II presentation assay based on a bio-orthogonal "clickable" antigen and showed that MHC class II presentation was disrupted by the inhibition of PIKfyve, which in turn resulted in reduced activation of CD4 T cells. Our results demonstrate a key role of PIKfyve in the processing and presentation of antigens, which should be taken into consideration when targeting PIKfyve in autoimmune disease and cancer. Antigen presentation to T cells in major histocompatibility complex class II (MHC class II) requires the conversion of early endo/phagosomes into lysosomes by a process called maturation. Maturation is driven by the phosphoinositide kinase PIKfyve. Blocking PIKfyve activity by small molecule inhibitors caused a delay in the conversion of phagosomes into lysosomes and in phagosomal acidification, whereas production of reactive oxygen species (ROS) increased. Elevated ROS resulted in reduced activity of cathepsin S and B, but not X, causing a proteolytic defect of MHC class II chaperone invariant chain Ii processing. We developed a novel universal MHC class II presentation assay based on a bio-orthogonal "clickable" antigen and showed that MHC class II presentation was disrupted by the inhibition of PIKfyve, which in turn resulted in reduced activation of CD4+ T cells. Our results demonstrate a key role of PIKfyve in the processing and presentation of antigens, which should be taken into consideration when targeting PIKfyve in autoimmune disease and cancer.Antigen presentation to T cells in major histocompatibility complex class II (MHC class II) requires the conversion of early endo/phagosomes into lysosomes by a process called maturation. Maturation is driven by the phosphoinositide kinase PIKfyve. Blocking PIKfyve activity by small molecule inhibitors caused a delay in the conversion of phagosomes into lysosomes and in phagosomal acidification, whereas production of reactive oxygen species (ROS) increased. Elevated ROS resulted in reduced activity of cathepsin S and B, but not X, causing a proteolytic defect of MHC class II chaperone invariant chain Ii processing. We developed a novel universal MHC class II presentation assay based on a bio-orthogonal "clickable" antigen and showed that MHC class II presentation was disrupted by the inhibition of PIKfyve, which in turn resulted in reduced activation of CD4+ T cells. Our results demonstrate a key role of PIKfyve in the processing and presentation of antigens, which should be taken into consideration when targeting PIKfyve in autoimmune disease and cancer. Antigen presentation to T cells in major histocompatibility complex class II (MHC class II) requires the conversion of early endo/phagosomes into lysosomes by a process called maturation. Maturation is driven by the phosphoinositide kinase PIKfyve. Blocking PIKfyve activity by small molecule inhibitors caused a delay in the conversion of phagosomes into lysosomes and in phagosomal acidification, whereas production of reactive oxygen species (ROS) increased. Elevated ROS resulted in reduced activity of cathepsin S and B, but not X, causing a proteolytic defect of MHC class II chaperone invariant chain Ii processing. We developed a novel universal MHC class II presentation assay based on a bio-orthogonal “clickable” antigen and showed that MHC class II presentation was disrupted by the inhibition of PIKfyve, which in turn resulted in reduced activation of CD4+ T cells. Our results demonstrate a key role of PIKfyve in the processing and presentation of antigens, which should be taken into consideration when targeting PIKfyve in autoimmune disease and cancer. : Molecular Mechanism of Gene Regulation; Immunology; Immune Response Subject Areas: Molecular Mechanism of Gene Regulation, Immunology, Immune Response
Author	Verdoes, Martijn ter Beest, Martin van den Bogaart, Geert Dingjan, Ilse Bertozzi, Carolyn R. Keyser, Samantha G.L. Muntjewerff, Elke M. van Aart, Melissa A.C. Maassen, Sjors Bianchi, Frans Baranov, Maksim V. Schirmacher, Anastasiya Diederichsen, Ulf
AuthorAffiliation	4 Department of Chemistry, University of California, Berkeley, CA 94720, USA 5 Department of Chemistry and Howard Hughes Medical Institute, Stanford University, Stanford, CA 94305, USA 3 Department of Molecular Immunology, Groningen Biomolecular Sciences and Biotechnology Institute, University of Groningen, Nijenborgh 7, Groningen 9747 AG, the Netherlands 2 Institute of Organic and Biomolecular Chemistry, Georg-August-University of Göttingen, Tammannstr. 2, 37077 Göttingen, Germany 1 Department of Tumor Immunology, Radboud University Medical Center, Radboud Institute for Molecular Life Sciences, Geert Grooteplein 28, 6525GA Nijmegen, the Netherlands
AuthorAffiliation_xml	– name: 1 Department of Tumor Immunology, Radboud University Medical Center, Radboud Institute for Molecular Life Sciences, Geert Grooteplein 28, 6525GA Nijmegen, the Netherlands – name: 3 Department of Molecular Immunology, Groningen Biomolecular Sciences and Biotechnology Institute, University of Groningen, Nijenborgh 7, Groningen 9747 AG, the Netherlands – name: 4 Department of Chemistry, University of California, Berkeley, CA 94720, USA – name: 5 Department of Chemistry and Howard Hughes Medical Institute, Stanford University, Stanford, CA 94305, USA – name: 2 Institute of Organic and Biomolecular Chemistry, Georg-August-University of Göttingen, Tammannstr. 2, 37077 Göttingen, Germany
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Snippet	Antigen presentation to T cells in major histocompatibility complex class II (MHC class II) requires the conversion of early endo/phagosomes into lysosomes by... Antigen presentation to T cells in major histocompatibility complex class II (MHC class II) requires the conversion of early endo/phagosomes into lysosomes by...
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Title	The Phosphoinositide Kinase PIKfyve Promotes Cathepsin-S-Mediated Major Histocompatibility Complex Class II Antigen Presentation
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