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Originally published In Press as doi:10.1074/jbc.M110055200 on December 20, 2001

J. Biol. Chem., Vol. 277, Issue 11, 9529-9539, March 15, 2002
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Differential Endocytic Functions of Trypanosoma brucei Rab5 Isoforms Reveal a Glycosylphosphatidylinositol-specific Endosomal Pathway*

Arun Pal, Belinda S. Hall, Darren N. NesbethDagger , Helen I. Field§, and Mark C. Field

From the Wellcome Trust Laboratories for Molecular Parasitology, Department of Biological Sciences and Centre for Molecular Microbiology and Infection, Imperial College of Science, Technology and Medicine, Exhibition Road, London SW7 2AY, United Kingdom

We demonstrate the presence of a glycosylphosphatidylinositol (GPI) anchor-specific endosomal pathway in the protozoan pathogen Trypanosoma brucei. In higher eukaryotes evidence indicates that GPI-anchored proteins are transported in both the endocytic and exocytic systems by mechanisms involving sequestration into specific membrane microdomains and consequently sorting into distinct compartments. This is potentially extremely important in trypanosomatids as the GPI anchor is the predominant mechanism for membrane attachment of surface macromolecules, including the variant surface glycoprotein (VSG). A highly complex developmentally regulated endocytic network, vital for nutrient uptake and evasion of the immune response, exists in T. brucei. In common with mammalian cells an early endosomal compartment is defined by Rab5 small GTPases, which control transport processes through the endosomal system. We investigate the function of two trypanosome Rab5 homologues. TbRAB5A and TbRAB5B, which colocalize in the procyclic stage, are distinct in the bloodstream form of the parasite. TbRAB5A endosomes contain VSG and transferrin, endocytosed by the T. brucei GPI-anchored transferrin receptor, whereas TbRAB5B endosomes contain the transmembrane protein ISG100 but neither VSG nor transferrin. These findings indicate the presence of trypanosome endosomal pathways trafficking proteins through specific routes depending on the mode of membrane attachment. Ectopic expression of mutant TbRAB5A or -5B indicates that TbRAB5A plays a role in LDL endocytosis, whereas TbRAB5B does not, but both have a role in fluid phase endocytosis. Hence TbRAB5A and TbRAB5B have distinct functions in the endosomal system of T. brucei. A developmentally regulated GPI-specific endosomal pathway in the bloodstream form suggests that specialized transport of GPI-anchored proteins is required for survival in the mammalian host.

* This work was supported by program grant funding from the Wellcome Trust (to M. C. F.).The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

A late draft of this paper was written in Halifax, Nova Scotia, Canada, following emergency rerouting of flight BA175 after the attacks on the World Trade Center and the Pentagon (11th September 2001). M. C. F. dedicates this paper to the memory of the thousands of innocents who were lost in these atrocities and to the deep kindness of the people of Halifax, Nova Scotia, Canada.

Dagger Present address: Guy's, Kings and St. Thomas' School of Medicine, Dept. of Molecular Medicine, Rayne Institute, 123 Coldharbor Lane, London, SE5 9NU, UK.

§ Present address: Proteometrics LLC, P. O. Box 32323, London SW17 8JZ, UK.

To whom correspondence should be addressed. Tel.: 01144-020-7594-5277; E-mail: mfield@ic.ac.uk.

Copyright © 2002 by The American Society for Biochemistry and Molecular Biology, Inc.
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