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Reconstructing the Evolution of the Endocytic System: Insights from Genomics and Molecular Cell Biology

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Eukaryotic Membranes and Cytoskeleton

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 607))

Abstract

Endocytosis is an essential process undertaken by most eukaryotic cells. At its most general, the term refers to the uptake of material from the cell milieu.1 Cell biologists, however, have come to recognise a number of distinct modes of endocytic transport that are accompanied by differences in their underlying molecular mechanisms. Multiple modes can coexist in the same cell type and are frequendy ongoing concurrendy. Broadly, endocytic mechanisms can be subdivided based on the size of the ingested particle or cargo. Phagocytosis, or cell eating, is the uptake of large particles, including whole cells, and is accompanied by transport through large vesicular structures (>250nm in diameter). Pinocytosis, or cell drinking, involves uptake of rather smaller cargo, typically macromolecules and complexes. The study of endocytic pathways has, for very good technical reasons, focused on a small number of taxa, principally metazoa, yeast and a restricted number of protists. This has served well and has allowed the definition of a number of pathways in part by virtue of the molecules that are required for their operation.

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References

  1. Alberts B, Johnson A, Lewis J et al. Molecular biology of the cell. 4th ed. New York: Garland Publishing, 2002.

    Google Scholar 

  2. Simpson AG, Roger AJ. Excavata and the origin of amitochondriate eukaryotes. In: Hirt RP, Horner DS, eds. Organelles, Genomes and Eukaryote Phylogeny: An Evolutionary Synthesis in the Age of Genomics. Boca Raton, Florida, USA: CRC Press, 2004.

    Google Scholar 

  3. Simpson AG, Roger AJ. The real ‘kingdoms’ of eukaryotes. Curr Biol 2004; 14:R693–6.

    Article  PubMed  CAS  Google Scholar 

  4. Stechmann A, Cavalier-Smith T. Rooting the eukaryote tree by using a derived gene fusion. Science 2002; 297(5578):89–91.

    Article  PubMed  CAS  Google Scholar 

  5. Richards TA, Cavalier-Smith T. Myosin domain evolution and the primary divergence of eukaryotes. Nature 2005; 436:1113–1118.

    Article  PubMed  CAS  Google Scholar 

  6. Field MC, Carrington M. Intracellular membrane transport systems in Trypanosoma brucei. Traffic 2004; 5(12):905–13.

    Article  PubMed  CAS  Google Scholar 

  7. Dacks JB, Field MC. Eukaryotic cell evolution from a genomic perspective: The endomembrane system. In: Hirt RP, Horner DS, eds. Organelles, Genomes and Eukaryote Phylogeny: An Evolutionary Synthesis in the Age of Genomics. London: CRC Press, 2004:309–334.

    Google Scholar 

  8. Cavalier-Smith T. The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. Int J Syst Evol Microbiol 2002; 52(Pt 2):297–354.

    PubMed  CAS  Google Scholar 

  9. Bokoch GM. Regulation of innate immunity by Rho GTPases. Trends Cell Biol 2005; 15:163–71.

    Article  PubMed  CAS  Google Scholar 

  10. In: Lee JJ, Leedale GF et al, eds. The Illustrated Guide to the Protozoa. Lawrence, Kansas: Society of Protozoologists, 2002.

    Google Scholar 

  11. Plattner H, Kissmehl R. Molecular aspects of membrane trafficking in paramecium. Int Rev Cytol 2003; 232:185–216.

    Article  PubMed  CAS  Google Scholar 

  12. Morgan GW, Hall BS, Denny PW et al. The kinetoplastida endocytic apparatus. Part I: A dynamic system for nutrition and evasion of host defences. Trends Parasitol 2002; 18(11):491–6.

    Article  PubMed  CAS  Google Scholar 

  13. Wang E, Pennington JG, Goldenring JR et al. Brefeldin A rapidly disrupts plasma membrane polarity by blocking polar sorting in common endosomes of MDCK cells. J Cell Sci 2001; 114:3309–21.

    PubMed  CAS  Google Scholar 

  14. Allen RD, Ma L, Fok AK. Acidosomes: Recipients of multiple sources of membrane and cargo during development and maturation. J Cell Sci 1993; 106(Pt l):411–22.

    PubMed  Google Scholar 

  15. Porto-Carreiro I, Attias M, Miranda K et al. Trypanosoma cruzi epimastigote endocytic pathway: Cargo enters the cytostome and passes through an early endosomal network before storage in reservosomes. Eur J Cell Biol 2000; 79:858–69.

    Article  PubMed  CAS  Google Scholar 

  16. Baldauf SL, Roger AJ, Wenk-Siefert I et al. A kingdom-level phylogeny of eukaryotes based on combined protein data. Science 2000; 290(5493):972–7.

    Article  PubMed  CAS  Google Scholar 

  17. Simpson AG. Cytoskeletal organization, phylogenetic affinities and systematics in the contentious taxon Excavata (Eukaryota). Int J Syst Evol Microbiol 2003; 53(Pt 6):1759–77.

    Article  PubMed  Google Scholar 

  18. Teng FY, Wang Y, Tang B. The syntaxins. Genome Biology 2001–2, (reviews 3012.1–3012.7).

    Google Scholar 

  19. Dacks JB, Doolittle WF. Novel syntaxin gene sequences from Giardia, Trypanosoma and algae: Implications for the ancient evolution of the eukaryotic endomembrane system. J Cell Sci 2002; 115(Pt 8):1635–42.

    PubMed  CAS  Google Scholar 

  20. Lal K, Field MC, Carlton J et al. Identification of a very large Rab GTPase family in the parasitic protozoan Trichomonas vaginalis. Mol Biochem Parasitol; 2005; 143:226–235.

    Article  PubMed  CAS  Google Scholar 

  21. Dacks JB, Doolittle WF. Molecular and phylogenetic characterization of syntaxin genes from parasitic protozoa. Mol Biochem Parasitol 2004; 136(2):123–36.

    Article  PubMed  CAS  Google Scholar 

  22. DeLuca P, Taddei R, Varano L. Cyanidioschyzon merolae: A new alga of thermal acidic environments. Webbia 1978; 33:37–44.

    Google Scholar 

  23. Lujan HD, Touz MC. Protein trafficking in Giardia lamblia. Cell Microbiol 2003; 5:427–34.

    Article  PubMed  CAS  Google Scholar 

  24. Hehl AB, Marti M. Secretory protein trafficking in Giardia intestinalis. Mol Microbiol 2004; 53:19–28.

    Article  PubMed  CAS  Google Scholar 

  25. Tovar J, Leon-Avila G, Sanchez LB et al. Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation. Nature 2003; 426(6963): 172–6.

    Article  PubMed  CAS  Google Scholar 

  26. Hall BS, Pal A, Goulding D et al. Rab4 is an essential regulator of lysosomal trafficking in trypanosomes. J Biol Chem 2004; 279:45047–56.

    Article  PubMed  CAS  Google Scholar 

  27. Conibear E, Cleck JN, Stevens TH. Vps51p mediates the association of the GARP (Vps52/53/54) complex with the late Golgi t-SNARE Tlglp. Mol Biol Cell 2003; 14:1610–23.

    Article  PubMed  CAS  Google Scholar 

  28. Collins KM, Thorngren NL, Fratti RA et al. Secl7p and HOPS, in distinct SNARE complexes, mediate SNARE complex disruption or assembly for fusion. EMBO J 2005; 24:1775–1786.

    Article  PubMed  CAS  Google Scholar 

  29. Van Wye J, Ghori N, Webster P et al. Identification and localization of rab6, separation of rab6 from ERD2 and implications for an ‘unstacked’ Golgi, in Plasmodium falciparum. Mol Biochem Parasitol 1996; 83:107–20.

    Article  PubMed  Google Scholar 

  30. Pelkmans L, Burli T, Zerial M et al. Caveolin-stabilized membrane domains as multifunctional transport and sorting devices in endocytic membrane traffic. Cell 2004; 118:767–80.

    Article  PubMed  CAS  Google Scholar 

  31. Overath P, Engstier M. Endocytosis, membrane recycling and sorting of GPI-anchored proteins: Trypanosoma brucei as a model system. Mol Microbiol 2004; 53:735–44.

    Article  PubMed  CAS  Google Scholar 

  32. Praefcke GJ, McMahon HT. The dynamin superfamily: Universal membrane tubulation and fission molecules? Nat Rev Mol Cell Biol 2004; 5:133–47.

    Article  PubMed  CAS  Google Scholar 

  33. Robinson MS. Adaptable adaptors for coated vesicles. Trends Cell Biol 2004; 14(4):167–74.

    Article  PubMed  CAS  Google Scholar 

  34. Motley A, Bright NA, Seaman MN et al. Clathrin-mediated endocytosis in AP-2-depleted cells. J Cell Biol 2003; 162(5):909–18.

    Article  PubMed  CAS  Google Scholar 

  35. Bonifacino JS, Traub LM. Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu Rev Biochem 2003; 72:395–447.

    Article  PubMed  CAS  Google Scholar 

  36. Ford MG, Mills IG, Peter BJ et al. Curvature of clathrin-coated pits driven by epsin. Nature 2002; 419:361–6.

    Article  PubMed  CAS  Google Scholar 

  37. Dupre S, Urban-Grimal D, Haguenauer-Tsapis R. Ubiquitin and endocytic internalization in yeast and animal cells. Biochim Biophys Acta 2004; 1695:89–111.

    Article  PubMed  CAS  Google Scholar 

  38. Legendre-Guillemin V, Wasiak S, Hussain NK et al. ENTH/ANTH proteins and clathrin-mediated membrane budding. J Cell Sci 2004; 117:9–18.

    Article  PubMed  CAS  Google Scholar 

  39. Stein MP, Feng Y, Cooper KL et al. Human VPS34 and pl50 are Rab7 interacting partners. Traffic 2003; 4:754–71.

    Article  PubMed  CAS  Google Scholar 

  40. Bowers K, Lottridge J, Helliwell SB et al. Protein-protein interactions of ESCRT complexes in the yeast Saccharomyces cerevisiae. Traffic 2004; 5:194–210.

    Article  PubMed  CAS  Google Scholar 

  41. Robibaro B, Hoppe HC, Yang M et al. Endocytosis in different lifestyles of protozoan parasitism: Role in nutrient uptake with special reference to Toxoplasma gondii. Int J Parasitol 2001; 31:1343–53.

    Article  PubMed  CAS  Google Scholar 

  42. Jurgens G. Membrane trafficking in plants. Annu Rev Cell Dev Biol 2004; 20:481–504.

    Article  PubMed  Google Scholar 

  43. Siniossoglou S, Lutzmann M, Santos-Rosa H et al. Structure and assembly of the Nup84p complex. J Cell Biol 2000; 149:41–54.

    Article  PubMed  CAS  Google Scholar 

  44. Devos D, Dokudovskaya S, Alber F et al. Components of coated vesicles and nuclear pore complexes share a common molecular architecture. PLoS Biol 2004; 2:e380.

    Article  PubMed  Google Scholar 

  45. Harper JT, Waanders E, Keeling PJ. On the monophyly of chromalveolates using a six-protein phylogeny of eukaryotes. Int J Syst Evol Microbiol 2005; 55(Pt l):487–96.

    Article  PubMed  CAS  Google Scholar 

  46. Berriman M, Ghedin E, Hertz-Fowler C et al. The genome of the African trypanosome Trypanosoma brucei. Science 2005; 309(5733):416–22.

    Article  PubMed  CAS  Google Scholar 

  47. Lang BF, O’Kelly C, Nerad T et al. The closest unicellular relatives of animals. Curr Biol 2002; 12(20):1773–8.

    Article  PubMed  CAS  Google Scholar 

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Correspondence to Mark C. Field .

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© 2007 Landes Bioscience and Springer Science+Business Media

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Field, M.C., Gabernet-Castello, C., Dacks, J.B. (2007). Reconstructing the Evolution of the Endocytic System: Insights from Genomics and Molecular Cell Biology. In: Eukaryotic Membranes and Cytoskeleton. Advances in Experimental Medicine and Biology, vol 607. Springer, New York, NY. https://doi.org/10.1007/978-0-387-74021-8_7

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