Early endosomes motility in filamentous fungi: How and why they move

Fungal Biology Reviews

Volumn 29, Issue 1, 2015, Pages 1-6

  Higuchi, Yujiro ^a   Steinberg, Gero ^b  

^a KYUSHU UNIVERSITY   (Japan)

^b UNIVERSITY OF EXETER   (United Kingdom)

Author keywords

Early endosome; Effector protein; Filamentous fungi; Membrane trafficking; Microtubule; Motor protein; Polysome

Indexed keywords

EMERICELLA NIDULANS; FUNGI; USTILAGO MAYDIS;

EID: 84928825909     PISSN: 17494613     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.fbr.2015.02.002     Document Type: Review

References (61)

1. Abenza J.F., Pantazopoulou A., Rodriguez J.M., Galindo A., Peñalva M.A. Long-distance movement of Aspergillus nidulans early endosomes on microtubule tracks. Traffic 2009, 10:57-75.
2. Rab5 integrates acquisition of degradative identity with the long distance movement of early endosomes. Mol. Biol. Cell. 2010, 21:2756-2769.
3. Abenza J.F., Galindo A., Pinar M., Pantazopoulou A., de los Ríos V., Peñalva M.A. Endosomal maturation by Rab conversion in Aspergillus nidulans is coupled to dynein-mediated basipetal movement. Mol. Biol. Cell. 2012, 23:1889-1901.
4. Baron Gaillard C.L., Pallesi-Pocachard E., Massey-Harroche D., Richard F., Arsanto J.P., Chauvin J.P., Lecine P., Krämer H., Borg J.P., Le Bivic A. Hook2 is involved in the morphogenesis of the primary cilium. Mol. Biol. Cell. 2011, 22:4549-4562.
5. Baumann S., Pohlmann T., Jungbluth M., Brachmann A., Feldbrügge M. Kinesin-3 and dynein mediate microtubule-dependent co-transport of mRNPs and endosomes. J. Cell. Sci. 2012, 125:2740-2752.
6. Baumann S., König J., Koepke J., Feldbrügge M. Endosomal transport of septin mRNA and protein indicates local translation on endosomes and is required for correct septin filamentation. EMBO Rep. 2014, 15:94-102.
7. Becht P., König J., Feldbrügge M. The RNA-binding protein Rrm4 is essential for polarity in Ustilago maydis and shuttles along microtubules. J. Cell. Sci. 2006, 119:4964-4973.
8. Bielska E., Schuster M., Roger Y., Berepiki A., Soanes D.M., Talbot N.J., Steinberg G. Hook is an adapter that coordinates kinesin-3 and dynein cargo attachment on early endosomes. J. Cell. Biol. 2014, 204:989-1007.
9. Bielska E., Higuchi Y., Schuster M., Steinberg N., Kilaru S., Talbot N.J., Steinberg G. Long-distance endosome trafficking drives fungal effector production during plant infection. Nat. Commun. 2014, 5:5097.
10. Brefort T., Doehlemann G., Mendoza-Mendoza A., Reissmann S., Djamei A., Kahmann R. Ustilago maydis as a Pathogen. Annu. Rev. Phytopathol. 2009, 47:423-445.
11. Chavrier P., Parton R.G., Hauri H.P., Simons K., Zerial M. Localization of low molecular weight GTP binding proteins to exocytic and endocytic compartments. Cell 1990, 62:317-329.
12. Djamei A., Schipper K., Rabe F., Ghosh A., Vincon V., Kahnt J., Osorio S., Tohge T., Fernie A.R., Feussner I., Feussner K., Meinicke P., Stierhof Y.D., Schwarz H., Macek B., Mann M., Kahmann R. Metabolic priming by a secreted fungal effector. Nature 2011, 478:395-398.
13. Djamei A., Kahmann R. Ustilago maydis: dissecting the molecular interface between pathogen and plant. PLoS Pathog. 2012, 8:e1002955.
14. Egan M.J., Tan K., Reck-Peterson S.L. Lis1 is an initiation factor for dynein-driven organelle transport. J. Cell. Biol. 2012, 197:971-982.
15. Egan M.J., McClintock M.A., Reck-Peterson S.L. Microtubule-based transport in filamentous fungi. Curr. Opin. Microbiol. 2012, 15:637-645.
16. Fisher M.C., Henk D.A., Briggs C.J., Brownstein J.S., Madoff L.C., McCraw S.L., Gurr S.J. Emerging fungal threats to animal, plant and ecosystem health. Nature 2012, 484:186-194.
17. Fischer-Parton S., Parton R.M., Hickey P.C., Dijksterhuis J., Atkinson H.A., Read N.D. Confocal microscopy of FM4-64 as a tool for analysing endocytosis and vesicle trafficking in living fungal hyphae. J. Microsc. 2000, 198:246-259.
18. Fuchs U., Hause G., Schuchardt I., Steinberg G. Endocytosis is essential for pathogenic development in the corn smut fungus Ustilago maydis. Plant Cell. 2006, 18:2066-2081.
19. Ge X., Frank C.L., Calderon de Anda F., Tsai L.H. Hook3 interacts with PCM1 to regulate pericentriolar material assembly and the timing of neurogenesis. Neuron 2010, 65:191-203.
20. Gillooly D.J., Morrow I.C., Lindsay M., Gould R., Bryant N.J., Gaullier J.M., Parton R.G., Stenmark H. Localization of phosphatidylinositol 3-phosphate in yeast and mammalian cells. EMBO J. 2000, 19:4577-4588.
21. Higuchi Y., Nakahama T., Shoji J.Y., Arioka M., Kitamoto K. Visualization of the endocytic pathway in the filamentous fungus Aspergillus oryzae using an EGFP-fused plasma membrane protein. Biochem. Biophys. Res. Commun. 2006, 340:784-791.
22. Higuchi Y., Shoji J.Y., Arioka M., Kitamoto K. Endocytosis is crucial for cell polarity and apical membrane recycling in the filamentous fungus Aspergillus oryzae. Eukaryot. Cell. 2009, 8:37-46.
23. Higuchi Y., Ashwin P., Roger Y., Steinberg G. Early endosome motility spatially organizes polysome distribution. J. Cell. Biol. 2014, 204:343-357.
24. Howe C.L., Mobley W.C. Signaling endosome hypothesis: A cellular mechanism for long distance communication. J. Neurobiol. 2004, 58:207-216.
25. Kämper J., Kahmann R., Bölker M., Ma L.J., Brefort T., Saville B.J., Banuett F., Kronstad J.W., Gold S.E., Müller O., Perlin M.H., Wösten H.A., de Vries R., Ruiz-Herrera J., Reynaga-Peña C.G., Snetselaar K., McCann M., Pérez-Martín J., Feldbrügge M., Basse C.W., Steinberg G., Ibeas J.I., Holloman W., Guzman P., Farman M., Stajich J.E., Sentandreu R., González-Prieto J.M., Kennell J.C., Molina L., Schirawski J., Mendoza-Mendoza A., Greilinger D., Münch K., Rössel N., Scherer M., Vranes M., Ladendorf O., Vincon V., Fuchs U., Sandrock B., Meng S., Ho E.C., Cahill M.J., Boyce K.J., Klose J., Klosterman S.J., Deelstra H.J., Ortiz-Castellanos L., Li W., Sanchez-Alonso P., Schreier P.H., Häuser-Hahn I., Vaupel M., Koopmann E., Friedrich G., Voss H., Schlüter T., Margolis J., Platt D., Swimmer C., Gnirke A., Chen F., Vysotskaia V., Mannhaupt G., Güldener U., Münsterkötter M., Haase D., Oesterheld M., Mewes H.W., Mauceli E.W., DeCaprio D., Wade C.M., Butler J., Young S., Jaffe D.B., Calvo S., Nusbaum C., Galagan J., Birren B.W. Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 2006, 444:97-101.
26. König J., Baumann S., Koepke J., Pohlmann T., Zarnack K., Feldbrügge M. The fungal RNA-binding protein Rrm4 mediates long-distance transport of ubi1 and rho3 mRNAs. EMBO J. 2009, 28:1855-1866.
27. Krämer H., Phistry M. Mutations in the Drosophila hook gene inhibit endocytosis of the boss transmembrane ligand into multivesicular bodies. J. Cell. Biol. 1996, 133:1205-1215.
28. Lemmon M.A. Phosphoinositide recognition domains. Traffic 2003, 4:201-213.
29. Lenz J.H., Schuchardt I., Straube A., Steinberg G. A dynein loading zone for retrograde endosome motility at microtubule plus-ends. EMBO J. 2006, 25:2275-2286.
30. Lesche R., Peetz A., van der Hoeven F., Rüther U. Ft1, a novel gene related to ubiquitin-conjugating enzymes, is deleted in the Fused toes mouse mutation. Mamm. Genome 1997, 8:879-883.
31. Machida M., Asai K., Sano M., Tanaka T., Kumagai T., Terai G., Kusumoto K., Arima T., Akita O., Kashiwagi Y., Abe K., Gomi K., Horiuchi H., Kitamoto K., Kobayashi T., Takeuchi M., Denning D.W., Galagan J.E., Nierman W.C., Yu J., Archer D.B., Bennett J.W., Bhatnagar D., Cleveland T.E., Fedorova N.D., Gotoh O., Horikawa H., Hosoyama A., Ichinomiya M., Igarashi R., Iwashita K., Juvvadi P.R., Kato M., Kato Y., Kin T., Kokubun A., Maeda H., Maeyama N., Maruyama J., Nagasaki H., Nakajima T., Oda K., Okada K., Paulsen I., Sakamoto K., Sawano T., Takahashi M., Takase K., Terabayashi Y., Wortman J.R., Yamada O., Yamagata Y., Anazawa H., Hata Y., Koide Y., Komori T., Koyama Y., Minetoki T., Suharnan S., Tanaka A., Isono K., Kuhara S., Ogasawara N., Kikuchi H. Genome sequencing and analysis of Aspergillus oryzae. Nature 2005, 438:1157-1161.
32. Maldonado-Báez L., Cole N.B., Krämer H., Donaldson J.G. Microtubule-dependent endosomal sorting of clathrin-independent cargo by Hook1. J. Cell. Biol. 2013, 201:233-247.
33. Mellman I. Endocytosis and molecular sorting. Annu. Rev. Cell. Dev. Biol. 1996, 12:575-625.
34. Miaczynska M., Pelkmans L., Zerial M. Not just a sink: endosomes in control of signal transduction. Curr. Opin. Cell. Biol. 2004, 16:400-406.
35. Miaczynska M., Bar-Sagi D. Signaling endosomes: seeing is believing. Curr. Opin. Cell. Biol. 2010, 22:535-540.
36. Nierman W.C., Pain A., Anderson M.J., Wortman J.R., Kim H.S., Arroyo J., Berriman M., Abe K., Archer D.B., Bermejo C., Bennett J., Bowyer P., Chen D., Collins M., Coulsen R., Davies R., Dyer P.S., Farman M., Fedorova N., Fedorova N., Feldblyum T.V., Fischer R., Fosker N., Fraser A., García J.L., García M.J., Goble A., Goldman G.H., Gomi K., Griffith-Jones S., Gwilliam R., Haas B., Haas H., Harris D., Horiuchi H., Huang J., Humphray S., Jiménez J., Keller N., Khouri H., Kitamoto K., Kobayashi T., Konzack S., Kulkarni R., Kumagai T., Lafon A., Latgé J.P., Li W., Lord A., Lu C., Majoros W.H., May G.S., Miller B.L., Mohamoud Y., Molina M., Monod M., Mouyna I., Mulligan S., Murphy L., O'Neil S., Paulsen I., Peñalva M.A., Pertea M., Price C., Pritchard B.L., Quail M.A., Rabbinowitsch E., Rawlins N., Rajandream M.A., Reichard U., Renauld H., Robson G.D., Rodriguez de Córdoba S., Rodríguez-Peña J.M., Ronning C.M., Rutter S., Salzberg S.L., Sanchez M., Sánchez-Ferrero J.C., Saunders D., Seeger K., Squares R., Squares S., Takeuchi M., Tekaia F., Turner G., Vazquez de Aldana C.R., Weidman J., White O., Woodward J., Yu J.H., Fraser C., Galagan J.E., Asai K., Machida M., Hall N., Barrell B., Denning D.W. Genomic sequence of the pathogenic and allergenic filamentous fungus Aspergillus fumigatus. Nature 2005, 438:1151-1156.
37. Peñalva M.A. Tracing the endocytic pathway of Aspergillus nidulans with FM4-64. Fungal. Genet. Biol. 2005, 42:963-975.
38. Peñalva M.A. Endocytosis in filamentous fungi: cinderella gets her reward. Curr. Opin. Microbiol. 2010, 13:684-692.
39. Rink J., Ghigo E., Kalaidzidis Y., Zerial M. Rab conversion as a mechanism of progression from early to late endosomes. Cell 2005, 122:735-749.
40. Saxena M., Mustelin T. Extracellular signals and scores of phosphatases: all roads lead to MAP kinase. Semin. Immunol. 2000, 12:387-396.
41. Schuster M., Kilaru S., Ashwin P., Lin C., Severs N.J., Steinberg G. Controlled and stochastic retention concentrates dynein at microtubule ends to keep endosomes on track. EMBO J. 2011, 30:652-664.
42. Schuster M., Lipowsky R., Assmann M.A., Lenz P., Steinberg G. Transient binding of dynein controls bidirectional long-range motility of early endosomes. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:3618-3623.
43. Schuster M., Kilaru S., Fink G., Collemare J., Roger Y., Steinberg G. Kinesin-3 and dynein cooperate in long-range retrograde endosome motility along a nonuniform microtubule array. Mol. Biol. Cell. 2011, 22:3645-3657.
44. Seaman M.N. Endosome protein sorting: motifs and machinery. Cell. Mol. Life Sci. 2008, 65:2842-2858.
45. Seidel C., Moreno-Velasquez S.D., Riquelme M., Fischer R. Neurospora crassa NKIN2, a kinesin-3 motor, transports early endosomes and is required for polarized growth. Eukaryot. Cell. 2013, 12:1020-1032.
46. Shoji J.Y., Kikuma T., Kitamoto K. Vesicle trafficking, organelle functions, and unconventional secretion in fungal physiology and pathogenicity. Curr. Opin. Microbiol. 2014, 20C:1-9.
47. Sorkin A., Von Zastrow M. Signal transduction and endocytosis: close encounters of many kinds. Nat. Rev. Mol. Cell. Biol. 2002, 3:600-614.
48. Steinberg G., Schliwa M., Lehmler C., Bölker M., Kahmann R., McIntosh J.R. Kinesin from the plant pathogenic fungus Ustilago maydis is involved in vacuole formation and cytoplasmic migration. J. Cell. Sci. 1998, 111:2235-2246.
49. Steinberg G. On the move: endosomes in fungal growth and pathogenicity. Nat. Rev. Microbiol. 2007, 5:309-316.
50. Steinberg G. Endocytosis and early endosome motility in filamentous fungi. Curr. Opin. Microbiol. 2014, 20C:10-18.
51. Sunio A., Metcalf A.B., Krämer H. Genetic dissection of endocytic trafficking in Drosophila using a horseradish peroxidase-bride of sevenless chimera: hook is required for normal maturation of multivesicular endosomes. Mol. Biol. Cell. 1999, 10:847-859.
52. Van Der Sluijs P., Hull M., Zahraoui A., Tavitian A., Goud B., Mellman I. The small GTP-binding protein rab4 is associated with early endosomes. Proc. Natl. Acad. Sci. U. S. A. 1991, 88:6313-6317.
53. Walenta J.H., Didier A.J., Liu X., Krämer H. The Golgi-associated hook3 protein is a member of a novel family of microtubule-binding proteins. J. Cell. Biol. 2001, 152:923-934.
54. Wedlich-Söldner R., Bölker M., Kahmann R., Steinberg G. A putative endosomal t-SNARE links exo- and endocytosis in the phytopathogenic fungus Ustilago maydis. EMBO J. 2000, 19:1974-1986.
55. Wedlich-Söldner R., Straube A., Friedrich M.W., Steinberg G. A balance of KIF1A-like kinesin and dynein organizes early endosomes in the fungus Ustilago maydis. EMBO J. 2002, 21:2946-2957.
56. Xu L., Sowa M.E., Chen J., Li X., Gygi S.P., Harper J.W. An FTS/Hook/p107(FHIP) complex interacts with and promotes endosomal clustering by the homotypic vacuolar protein sorting complex. Mol. Biol. Cell. 2008, 19:5059-5071.
57. Yao X., Wang X., Xiang X. FHIP and FTS proteins are critical for dynein-mediated transport of early endosomes in Aspergillus. Mol. Biol. Cell. 2014, 25:2181-2189.
58. Zhang J., Li S., Fischer R., Xiang X. Accumulation of cytoplasmic dynein and dynactin at microtubule plus ends in Aspergillus nidulans is kinesin dependent. Mol. Biol. Cell. 2003, 14:1479-1488.
59. Zhang J., Zhuang L., Lee Y., Abenza J.F., Peñalva M.A., Xiang X. The microtubule plus-end localization of Aspergillus dynein is important for dynein-early-endosome interaction but not for dynein ATPase activation. J. Cell. Sci. 2010, 123:3596-3604.
60. Zhang J., Qiu R., Arst H.N., Peñalva M.A., Xiang X. HookA is a novel dynein-early endosome linker critical for cargo movement in vivo. J. Cell. Biol. 2014, 204:1009-1026.
61. Zerial M., McBride H. Rab proteins as membrane organizers. Nat. Rev. Mol. Cell. Biol. 2001, 2:107-117.