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Review Article

The endocytic adaptor proteins of pathogenic fungi: charting new and familiar pathways

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Pages 449-457 | Received 30 Aug 2010, Accepted 06 Jan 2011, Published online: 24 Jan 2011

References

  • Mellman I. Endocytosis and molecular sorting. Annu Rev Cell Dev Biol 1996; 12: 575–625.
  • Wendland B, Emr SD, Riezman H. Protein traffic in the yeast endocytic and vacuolar protein sorting pathways. Curr Opin Cell Biol 1998; 10: 513–522.
  • Battey NH, James NC, Greenland AJ, Brownlee C. Exocytosis and endocytosis. Plant Cell 1999; 11: 643–660.
  • Samaj J, Read ND, Volkmann D, Menzel D, Baluska F. The endocytic network in plants. Trends Cell Biol 2005; 15: 425–433.
  • Miaczynska M, Stenmark H. Mechanisms and functions of endocytosis. J Cell Biol 2008; 180: 7–11.
  • Cheung AY, de Vries SC. Membrane trafficking: intracellular highways and country roads. Plant Physiol 2008; 147: 1451–1453.
  • Robinson MS, Watts C, Marino Z. Membrane dynamics in endocytosis. Cell 1996; 84: 13–21.
  • Kirchhausen T. Three ways to make a vesicle. Nat Rev Mol Cell Biol 2000; 1: 187–198.
  • Wickner W, Schekman R. Membrane fusion. Nat Struct Mol Biol 2008; 15: 658–664.
  • Munn AL. The yeast endocytic membrane transport system. Microsc Res Tech 2000; 51: 547–562.
  • Higuchi Y, Shoji JY, Arioka M, . Endocytosis is crucial for cell polarity and apical membrane recycling in the filamentous fungus Aspergillus oryzae. Eukaryot Cell 2009; 8: 37–46.
  • Kim JH, Kim HW, Heo DH, . FgEnd1 is a putative component of the endocytic machinery and mediates ferrichrome uptake in F. graminearum. Curr Genet 2009; 55: 593–600.
  • Fuchs U, Hause G, Schuchardt I, . Endocytosis is essential for pathogenic development in the corn smut fungus Ustilago maydis. Plant Cell 2006; 18: 2066–2081.
  • Fuchs U, Steinberg G. Endocytosis in the plant-pathogenic fungus Ustilago maydis. Protoplasma 2005; 226: 75–80.
  • Steinberg G. On the move: endosomes in fungal growth and pathogenicity. Nat Rev Microbiol 2007; 5: 309–316.
  • Weissman Z, Shemer R, Conibear E, . An endocytic mechanism for haemoglobin-iron acquisition in Candida albicans. Mol Microbiol 2008; 69: 201–217.
  • Johnston DA, Eberle KE, Sturtevant JE, . Role for endosomal and vacuolar GTPases in Candida albicans pathogenesis. Infect Immun 2009; 77: 2343–2355.
  • Palanisamy SK, Ramirez MA, Lorenz M, . Candida albicans PEP12 is required for biofilm integrity and in vivo virulence. Eukaryot Cell 2010; 9: 266–277.
  • Cornet M, Bidard F, Schwarz P, . Deletions of endocytic components VPS28 and VPS32 affect growth at alkaline pH and virulence through both RIM101-dependent and RIM101-independent pathways in Candida albicans. Infect Immun 2005; 73: 7977–7987.
  • Bernardo SM, Khalique Z, Kot J, . Candida albicans VPS1 contributes to protease secretion, filamentation, and biofilm formation. Fungal Genet Biol 2008; 45: 861–877.
  • Wolf JM, Johnson DJ, Chmielewski D, . The Candida albicans ESCRT pathway makes Rim101-dependent and -independent contributions to pathogenesis. Eukaryot Cell 2010; 9: 1203–1215.
  • Douglas LM, Martin SW, Konopka JB. BAR domain proteins Rvs161 and Rvs167 contribute to Candida albicans endocytosis, morphogenesis, and virulence. Infect Immun 2009; 77: 4150–4160.
  • Cornet M, Gaillardin C, Richard ML. Deletions of the endocytic components VPS28 and VPS32 in Candida albicans lead to echinocandin and azole hypersensitivity. Antimicrob Agents Chemother 2006; 50: 3492–3495.
  • Liu X, Hu G, Panepinto J, . Role of a VPS41 homologue in starvation response, intracellular survival and virulence of Cryptococcus neoformans. Mol Microbiol 2006; 61: 1132–1146.
  • Panepinto J, Komperda K, Frases S, . Sec6-dependent sorting of fungal extracellular exosomes and laccase of Cryptococcus neoformans. Mol Microbiol 2009; 71: 1165–1176.
  • Shen G, Whittington A, Song K, . Pleiotropic function of intersectin homologue Cin1 in Cryptococcus neoformans. Mol Microbiol 2010; 76: 662–676.
  • Davis NG, Horecka JL, Sprague GF. Cis- and trans-acting functions required for endocytosis of the yeast pheromone receptors. J Cell Biol 1993; 122: 53–65.
  • Raths S, Rohrer J, Crausaz F, . end3 and end4: two mutants defective in receptor-mediated and fluid-phase endocytosis in Saccharomyces cerevisiae. J Cell Biol 1993; 120: 55–65.
  • Benmerah A, Begue B, Dautry-Varsat A, . The ear of alpha-adaptin interacts with the COOH-terminal domain of the Eps 15 protein. J Biol Chem 1996; 271: 12111–12116.
  • van Delft S, Govers R, Strous GJ, . Epidermal growth factor induces ubiquitination of Eps15. J Biol Chem 1997; 272: 14013–14016.
  • Kaksonen M. Taking apart the endocytic machinery. J Cell Biol 2008; 180: 1059–1060.
  • Toret CP, Drubin DG. The budding yeast endocytic pathway. J Cell Sci 2006; 119: 4585–4587.
  • Borth N, Walther A, Reijnst P, . Candida albicans Vrp1 is required for polarized morphogenesis and interacts with Wal1 and Myo5. Microbiology 2010; 156: 2962–2969.
  • Tang HY, Munn A, Cai M. EH domain proteins Pan1p and End3p are components of a complex that plays a dual role in organization of the cortical actin cytoskeleton and endocytosis in Saccharomyces cerevisiae. Mol Cell Biol 1997; 17: 4294–4304.
  • Wendland B, Emr SD. Pan1p, yeast eps15, functions as a multivalent adaptor that coordinates protein-protein interactions essential for endocytosis. J Cell Biol 1998; 141: 71–84.
  • Benedetti H, Raths S, Crausaz F, . The END3 gene encodes a protein that is required for the internalization step of endocytosis and for actin cytoskeleton organization in yeast. Mol Biol Cell 1994; 5: 1023–1037.
  • Tebar F, Confalonieri S, Carter RE, . Eps15 is constitutively oligomerized due to homophilic interaction of its coiled-coil region. J Biol Chem 1997; 272: 15413–15418.
  • Galan JM, Moreau V, Andre B, . Ubiquitination mediated by the Npi1p/Rsp5p ubiquitin-protein ligase is required for endocytosis of the yeast uracil permease. J Biol Chem 1996; 271: 10946–10952.
  • Zoladek T, Tobiasz A, Vaduva G, . MDP1, a Saccharomyces cerevisiae gene involved in mitochondrial/cytoplasmic protein distribution, is identical to the ubiquitin-protein ligase gene RSP5. Genetics 1997; 145: 595–603.
  • Gagny B, Wiederkehr A, Dumoulin P, . A novel EH domain protein of Saccharomyces cerevisiae, Ede1p, involved in endocytosis. J Cell Sci 2000; 113: 3309–3319.
  • Calderone RA, Fonzi WA. Virulence factors of Candida albicans. Trends Microbiol 2001; 9: 327–335.
  • Cutler JE. Putative virulence factors of Candida albicans. Annu Rev Microbiol 1991; 45: 187–218.
  • Haynes K. Virulence in Candida species. Trends Microbiol 2001; 9: 591–596.
  • Naglik JR, Challacombe SJ, Hube B. Candida albicans secreted aspartyl proteinases in virulence and pathogenesis. Microbiol Mol Biol Rev 2003; 67: 400–428.
  • Veses V, Gow NA. Vacuolar dynamics during the morphogenetic transition in Candida albicans. FEMS Yeast Res 2008; 8: 1339–1348.
  • Palmer GE, Askew DS, Williamson PR. The diverse roles of autophagy in medically important fungi. Autophagy 2008; 4: 982–988.
  • Basrai MA, Naider F, Becker JM. Internalization of lucifer yellow in Candida albicans by fluid phase endocytosis. J Gen Microbiol 1990; 136: 1059–1065.
  • Martin R, Hellwig D, Schaub Y, . Functional analysis of Candida albicans genes whose Saccharomyces cerevisiae homologues are involved in endocytosis. Yeast 2007; 24: 511–522.
  • Veses V, Casanova M, Murgui A, . ABG1, a novel and essential Candida albicans gene encoding a vacuolar protein involved in cytokinesis and hyphal branching. Eukaryot Cell 2005; 4: 1088–1101.
  • Veses V, Casanova M, Murgui A, . Candida albicans ABG1 gene is involved in endocytosis. FEMS Yeast Res 2009; 9: 293–300.
  • Yin Z, Stead D, Selway L, . Proteomic response to amino acid starvation in Candida albicans and Saccharomyces cerevisiae. Proteomics 2004; 4: 2425–2436.
  • Toshima J, Toshima JY, Duncan MC, . Negative regulation of yeast Eps15-like Arp2/3 complex activator, Pan1p, by the Hip1R-related protein, Sla2p, during endocytosis. Mol Biol Cell 2007; 18: 658–668.
  • Gale CA, Leonard MD, Finley KR, . SLA2 mutations cause SWE1-mediated cell cycle phenotypes in Candida albicans and Saccharomyces cerevisiae. Microbiology 2009; 155: 3847–3859.
  • Holtzman DA, Yang S, Drubin DG. Synthetic-lethal interactions identify two novel genes, SLA1 and SLA2, that control membrane cytoskeleton assembly in Saccharomyces cerevisiae. J Cell Biol 1993; 122: 635–644.
  • Reijnst P, Jorde S, Wendland J. Candida albicans SH3-domain proteins involved in hyphal growth, cytokinesis, and vacuolar morphology. Curr Genet 2010; 56: 309–319.
  • Poltermann S, Nguyen M, Gunther J, . The putative vacuolar ATPase subunit Vma7p of Candida albicans is involved in vacuole acidification, hyphal development and virulence. Microbiology 2005; 151: 1645–1655.
  • Alvarez FJ, Douglas LM, Rosebrock A, . The Sur7 protein regulates plasma membrane organization and prevents intracellular cell wall growth in Candida albicans. Mol Biol Cell 2008; 19: 5214–5225.
  • Hibbett DS, Binder M, Bischoff JF, . A higher-level phylogenetic classification of the fungi. Mycol Res 2007; 111: 509–547.
  • Mitchell TG, Perfect JR. Cryptococcosis in the era of AIDS – 100 years after the discovery of Cryptococcus neoformans. Clinical Microbiol Rev 1995; 8: 515–548.
  • Buchanan KL, Murphy JW. What makes Cryptococcus neoformans a pathogen? Emerg Infect Dis 1998; 4: 71–83.
  • Kozel TR, Gotschlich EC. The capsule of Cryptococcus neoformans passively inhibits phagocytosis of the yeast by macrophages. J Immunol 1982; 129: 1675–1680.
  • Kozel TR, Pfrommer GS, Guerlain AS, . Role of the capsule in phagocytosis of Cryptococcus neoformans. Rev Infect Dis 1988; 10 (Suppl. 2): S436–S439.
  • De Jesus M, Nicola AM, Rodrigues ML, . Capsular localization of the Cryptococcus neoformans polysaccharide component galactoxylomannan. Eukaryot Cell 2009; 8: 96–103.
  • Rittershaus PC, Kechichian TB, Allegood JC, . Glucosylceramide synthase is an essential regulator of pathogenicity of Cryptococcus neoformans J Clin Investig 2006; 116: 1651–1659.
  • Salas SD, Bennett JE, Kwon-Chung KJ, . Effect of the laccase gene, CNLAC1, on virulence of Cryptococcus neoformans. J Exp Med 1996; 184: 377–386.
  • Rodrigues ML, Nakayasu ES, Oliveira DL, . Extracellular vesicles produced by Cryptococcus neoformans contain protein components associated with virulence. Eukaryot Cell 2008; 7: 58–67.
  • Yoneda A, Doering TL. A eukaryotic capsular polysaccharide is synthesized intracellularly and secreted via exocytosis. Mol Biol Cell 2006; 17: 5131–5140.
  • Tang HY, Xu J, Cai M. Pan1p, End3p, and S1a1p, three yeast proteins required for normal cortical actin cytoskeleton organization, associate with each other and play essential roles in cell wall morphogenesis. Mol Cell Biol 2000; 20: 12–25.
  • Pucharcós C, Fuentes JJ, Casas C, . Alu-splice cloning of human Intersectin (ITSN), a putative multivalent binding protein expressed in proliferating and differentiating neurons and overexpressed in Down syndrome. Eur J Hum Genet 1999; 7: 704–712.
  • Guipponi M, Scott HS, Chen H, . Two isoforms of a human intersectin (ITSN) protein are produced by brain-specific alternative splicing in a stop codon. Genomics 1998; 53: 369–376.
  • Yamabhai M, Hoffman NG, Hardison NL, . Intersectin, a novel adaptor protein with two Eps15 homology and five Src homology 3 domains. J Biol Chem 1998; 273: 31401–31407.
  • Mayer BJ. SH3 domains: complexity in moderation. J Cell Sci 2001; 114: 1253–1263.
  • Cerione RA, Zheng Y. The Dbl family of oncogenes. Curr Opin Cell Biol 1996; 8: 216–222.
  • Rohatgi R, Ma L, Miki H, . The interaction between N-WASP and the Arp2/3 complex links Cdc42-dependent signals to actin assembly. Cell 1999; 97: 221–231.
  • Hussain NK, Jenna S, Glogauer M, . Endocytic protein intersectin-l regulates actin assembly via Cdc42 and N-WASP. Nat Cell Biol 2001; 3: 927–932.
  • Zamanian JL, Kelly RB. Intersectin 1L guanine nucleotide exchange activity is regulated by adjacent src homology 3 domains that are also involved in endocytosis. Mol Biol Cell 2003; 14: 1624–1637.
  • Wang JB, Wu WJ, Cerione RA. Cdc42 and Ras cooperate to mediate cellular transformation by intersectin-L. J Biol Chem 2005; 280: 22883–22891.
  • Malacombe M, Ceridono M, Calco V, . Intersectin-1L nucleotide exchange factor regulates secretory granule exocytosis by activating Cdc42. EMBO J 2006; 25: 3494–3503.
  • Haslam RJ, Koide HB, Hemmings BA. Pleckstrin domain homology. Nature 1993; 363: 309–310.
  • Shaw G. The pleckstrin homology domain: an intriguing multifunctional protein module. Bioessays 1996; 18: 35–46.
  • Lemmon MA, Ferguson KM. Signal-dependent membrane targeting by pleckstrin homology (PH) domains. Biochem J 2000; 350: 1–18.
  • Chu DS, Pishvaee B, Payne GS. The light chain subunit is required for clathrin function in Saccharomyces cerevisiae. J Biol Chem 1996; 271: 33123–33130.
  • Drubin DG, Mulholland J, Zhu ZM, . Homology of a yeast actin-binding protein to signal transduction proteins and myosin-I. Nature 1990; 343: 288–290.
  • Huang CF, Liu YW, Tung L, . Role for Arf3p in development of polarity, but not endocytosis, in Saccharomyces cerevisiae. Mol Biol Cell 2003; 14: 3834–3847.
  • Goyard S, Knechtle P, Chauvel M, . The Yak1 kinase is involved in the initiation and maintenance of hyphal growth in Candida albicans. Mol Biol Cell 2008; 19: 2251–2266.
  • Moseley JB, Goode BL. The yeast actin cytoskeleton: from cellular function to biochemical mechanism. Microbiol Mol Biol Rev 2006; 70: 605–645.
  • Epp E, Walther A, Lepine G, . Forward genetics in Candida albicans that reveals the Arp2/3 complex is required for hyphal formation, but not endocytosis. Mol Microbiol 2010; 75: 1182–1198.
  • Tong AH, Evangelista M, Parsons AB, . Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 2001; 294: 2364–2368.
  • Soulard A, Lechler T, Spiridonov V, . Saccharomyces cerevisiae Bzz1p is implicated with type I myosins in actin patch polarization and is able to recruit actin-polymerizing machinery in vitro. Mol Cell Biol 2002; 22: 7889–7906.
  • Amatruda JF, Gattermeir DJ, Karpova TS, . Effects of null mutations and overexpression of capping protein on morphogenesis, actin distribution and polarized secretion in yeast. J Cell Biol 1992; 119: 1151–1162.
  • Moon AL, Janmey PA, Louie KA, . Cofilin is an essential component of the yeast cortical cytoskeleton. J Cell Biol 1993; 120: 421–435.
  • Li R. Bee1, a yeast protein with homology to Wiscott-Aldrich syndrome protein, is critical for the assembly of cortical actin cytoskeleton. J Cell Biol 1997; 136: 649–658.
  • Walther A, Wendland J. Polarized hyphal growth in Candida albicans requires the Wiskott-Aldrich syndrome protein homolog Wal1p. Eukaryot Cell 2004; 3: 471–482.
  • Goodson HV, Anderson BL, Warrick HM, . Synthetic lethality screen identifies a novel yeast myosin I gene (MYO5): myosin I proteins are required for polarization of the actin cytoskeleton. J Cell Biol 1996; 133: 1277–1291.
  • Oberholzer U, Marcil A, Leberer E, . Myosin I is required for hypha formation in Candida albicans. Eukaryot Cell 2002; 1: 213–228.
  • Sivadon P, Crouzet M, Aigle M. Functional assessment of the yeast Rvs161 and Rvs167 protein domains. FEBS Lett 1997; 417: 21–27.
  • Adams AE, Botstein D, Drubin DG. A yeast actin-binding protein is encoded by SAC6, a gene found by suppression of an actin mutation. Science 1989; 243: 231–233.
  • Goodman A, Goode BL, Matsudaira P, . The Saccharomyces cerevisiae calponin/transgelin homolog Scp1 functions with fimbrin to regulate stability and organization of the actin cytoskeleton. Mol Biol Cell 2003; 14: 2617–2629.
  • Vater CA, Raymond CK, Ekena K, . The VPS1 protein, a homolog of dynamin required for vacuolar protein sorting in Saccharomyces cerevisiae, is a GTPase with two functionally separable domains. J Cell Biol 1992; 119: 773–786.
  • Mochida J, Yamamoto T, Fujimura-Kamada K, . The novel adaptor protein, Mti1p, and Vrp1p, a homolog of Wiskott-Aldrich syndrome protein-interacting protein (WIP), may antagonistically regulate type I myosins in Saccharomyces cerevisiae. Genetics 2002; 160: 923–934.
  • Dewar H, Warren DT, Gardiner FC, . Novel proteins linking the actin cytoskeleton to the endocytic machinery in Saccharomyces cerevisiae. Mol Biol Cell 2002; 13: 3646–3661.
  • Cope MJ, Yang S, Shang C, . Novel protein kinases Ark1p and Prk1p associate with and regulate the cortical actin cytoskeleton in budding yeast. J Cell Biol 1999; 144: 1203–1218.
  • Blankenship JR, Fanning S, Hamaker JJ, . An extensive circuitry for cell wall regulation in Candida albicans. PLoS Pathog 2010; 6: e1000752.
  • Miliaras NB, Park JH, Wendland B. The function of the endocytic scaffold protein Pan1p depends on multiple domains. Traffic 2004; 5: 963–978.
  • Duncan MC, Cope MJ, Goode BL, . Yeast Eps15-like endocytic protein, Pan1p, activates the Arp2/3 complex. Nat Cell Biol 2001; 3: 687–690.

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