Cross-presentation by intercellular peptide transfer through gap junctions

Joost Neijssen (), Carla Herberts, Jan Wouter Drijfhout, Eric Reits, Lennert Janssen and Jacques Neefjes
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Joost Neijssen: The Netherlands Cancer Institute
Carla Herberts: The Netherlands Cancer Institute
Jan Wouter Drijfhout: University Medical Center
Eric Reits: The Netherlands Cancer Institute
Lennert Janssen: The Netherlands Cancer Institute
Jacques Neefjes: The Netherlands Cancer Institute

Nature, 2005, vol. 434, issue 7029, 83-88

Abstract: Abstract Major histocompatibility complex (MHC) class I molecules present peptides that are derived from endogenous proteins1. These antigens can also be transferred to professional antigen-presenting cells in a process called cross-presentation, which precedes initiation of a proper T-cell response2,3; but exactly how they do this is unclear. We tested whether peptides can be transferred directly from the cytoplasm of one cell into the cytoplasm of its neighbour through gap junctions. Here we show that peptides with a relative molecular mass of up to ∼1,800 diffuse intercellularly through gap junctions unless a three-dimensional structure is imposed. This intercellular peptide transfer causes cytotoxic T-cell recognition of adjacent, innocent bystander cells as well as activated monocytes. Gap-junction-mediated peptide transfer is restricted to a few coupling cells owing to the high cytosolic peptidase activity. We present a mechanism of antigen acquisition for cross-presentation that couples the antigen presentation system of two adjacent cells and is lost in most tumours: gap-junction-mediated intercellular peptide coupling for presentation by bystander MHC class I molecules and transfer to professional antigen presenting cells for cross-priming.

Date: 2005
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DOI: 10.1038/nature03290

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