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First published online 15 November 2005
doi: 10.1242/jcs.02667

Journal of Cell Science 118, 5499-5511 (2005)
Published by The Company of Biologists 2005
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Research Article

GPI valence and the fate of secretory membrane proteins in African trypanosomes

Kevin J. Schwartz1, Ronald F. Peck1, Ngii N. Tazeh2 and James D. Bangs1,*

1 Department of Medical Microbiology and Immunology, University of Wisconsin-Madison Medical School, Madison, WI 53706, USA
2 Department of Biomolecular Chemistry, University of Wisconsin-Madison Medical School, Madison, WI 53706, USA

* Author for correspondence (e-mail: jdbangs{at}wisc.edu)

Accepted 31 August 2005

Progression of GPI-anchored proteins in bloodstream African trypanosomes correlates with GPI-valence: homodimeric VSG (2 GPI) is a surface protein; heterodimeric transferrin receptor (1 GPI) localizes in the flagellar pocket; homodimeric GPI-minus VSG (0 GPI) is rapidly degraded in the lysosome. We test this relationship using three native secretory/endocytic proteins as monomeric GPI-plus and -minus reporters. GPI-minus procyclin trafficks to the lysosome and is degraded. GPI-plus procyclin trafficks to the flagellar pocket/cell surface and is released (~50%) with an intact anchor, the remainder (~50%) is degraded in the lysosome. GPI-plus BiPNHP, derived from the ER marker BiP, is released quantitatively (>80%), while GPI-plus p67HP, derived from the lysosomal marker p67, turns over by both release (~15%) and lysosomal degradation (>50%). Turnover of endogenous transferrin receptor occurs primarily by lysosomal degradation (>90%). Thus shedding of monovalent GPI reporters correlates inversely with lysosomal targeting. We propose that mono-GPI reporters cycle through the flagellar pocket and endosome until they are disposed of by either shedding or lysosomal targeting. Partitioning between these fates may be a function of individual physical properties. Release is likely due to the exclusive use of C-14:0 myristate in the bloodstream stage GPI anchor. Up-regulation of transferrin receptor by culture in dog serum resulted in prominent cell surface localization, but not in elevated release. Surface receptor was non-functional for ligand binding suggesting that it may be bivalent homodimers of the GPI-anchored ESAG6 receptor subunit.

Key words: Trypanosome, Glycosylphosphatidylinositol, Flagellar pocket, Transferrin receptor, Protein sorting


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