Pleiotropic function of intersectin homologue Cin1 in Cryptococcus neoformans

Molecular Microbiology

Volumn 76, Issue 3, 2010, Pages 662-676

  Shen, Gui ^a   Whittington, Amy ^b   Song, Kejing ^a   Wang, Ping ^a,b  

^a LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^b LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CRYPTOCOCCAL INTERSECTIN 1 PROTEIN; FUNGAL PROTEIN; MESSENGER RNA; PROTEIN CDC42; PROTEIN SH3; UNCLASSIFIED DRUG; INTERSECTIN 1; PROTEIN BINDING; VESICULAR TRANSPORT ADAPTOR PROTEIN;

ALTERNATIVE RNA SPLICING; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CRYPTOCOCCUS NEOFORMANS; CYTOKINESIS; CYTOSKELETON; FUNGAL VIRULENCE; FUNGUS GROWTH; GENE DISRUPTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SEQUENCE HOMOLOGY; CHEMISTRY; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PROTEIN TERTIARY STRUCTURE;

FILOBASIDIELLA NEOFORMANS; FUNGI;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; CRYPTOCOCCUS NEOFORMANS; CYTOKINESIS; FUNGAL PROTEINS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY;

EID: 77951607840     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2010.07121.x     Document Type: Article

References (59)

1. Alspaugh, J.A., Perfect, J.R. Heitman, J. (1997) Cryptococcus neoformans mating and virulence are regulated by the G-protein alpha subunit GPA1 and cAMP. Genes Dev 11 : 3206 3217. (Pubitemid 27528060)
2. Ballou, E.R., Nichols, C.B., Miglia, K.J., Kozubowski, L. Alspaugh, J.A. (2009) Two CDC42 paralogues modulate Cryptococcus neoformans thermotolerance and morphogenesis under host physiological conditions. Mol Microbiol 75 : 763 780.
3. Buchanan, K.L. Murphy, J.W. (1998) What makes Cryptococcus neoformans a pathogen? Emerg Infect Dis 4 : 71 83.
4. Cerione, R.A. Zheng, Y. (1996) The Dbl family of oncogenes. Curr Opin Cell Biol 8 : 216 222. (Pubitemid 26109095)
5. Chabu, C. Doe, C.Q. (2008) Dap160/intersectin binds and activates aPKC to regulate cell polarity and cell cycle progression. Development 135 : 2739 2746.
6. Chen, L.C., Blank, E.S. Casadevall, A. (1996) Extracellular proteinase activity of Cryptococcus neoformans. Clin Diagn Lab Immunol 3 : 570 574. (Pubitemid 26326285)
7. Chen, S.C., Muller, M., Zhou, J.Z., Wright, L.C. Sorrell, T.C. (1997) Phospholipase activity in Cryptococcus neoformans: a new virulence factor? J Infect Dis 175 : 414 420. (Pubitemid 27052248)
8. Confalonieri, S. Di Fiore, P.P. (2002) The Eps15 homology (EH) domain. FEBS Lett 513 : 24 29. (Pubitemid 34242974)
9. Cox, G.M., Mukherjee, J., Cole, G.T., Casadevall, A. Perfect, J.R. (2000) Urease as a virulence factor in experimental cryptococcosis. Infect Immun 68 : 443 448. (Pubitemid 30056492)
10. De Jesus, M., Nicola, A.M., Rodrigues, M.L., Janbon, G. Casadevall, A. (2009) Capsular localization of the Cryptococcus neoformans polysaccharide component galactoxylomannan. Eukaryot Cell 8 : 96 103.
11. Duncan, M.C., Cope, M.J., Goode, B.L., Wendland, B. Drubin, D.G. (2001) Yeast Eps15-like endocytic protein, Pan1p, activates the Arp2/3 complex. Nat Cell Biol 3 : 687 690. (Pubitemid 32624427)
12. Fairhead, C., Llorente, B., Denis, F., Soler, M. Dujon, B. (1996) New vectors for combinatorial deletions in yeast chromosomes and for gap-repair cloning using 'split-marker' recombination. Yeast 12 : 1439 1457. (Pubitemid 26393225)
13. Gasman, S., Chasserot-Golaz, S., Malacombe, M., Way, M. Bader, M.F. (2004) Regulated exocytosis in neuroendocrine cells: a role for subplasmalemmal Cdc42/N-WASP-induced actin filaments. Mol Biol Cell 15 : 520 531. (Pubitemid 38146470)
14. Guipponi, M., Scott, H.S., Chen, H., Schebesta, A., Rossier, C. Antonarakis, S.E. (1998) Two isoforms of a human intersectin (ITSN) protein are produced by brain-specific alternative splicing in a stop codon. Genomics 53 : 369 376. (Pubitemid 28527640)
15. Haslam, R.J., Koide, H.B. Hemmings, B.A. (1993) Pleckstrin domain homology. Nature 363 309 310.
16. Huang, B. Cai, M. (2007) Pan1p: an actin director of endocytosis in yeast. Int J Biochem Cell Biol 39 : 1760 1764. (Pubitemid 47321338)
17. Hussain, N.K., Jenna, S., Glogauer, M., Quinn, C.C., Wasiak, S., Guipponi, M., et al 2001) Endocytic protein intersectin-l regulates actin assembly via Cdc42 and N-WASP. Nat Cell Biol 3 : 927 932. (Pubitemid 32952259)
18. Kelly, L.E. Phillips, A.M. (2005) Molecular and genetic characterization of the interactions between the Drosophila stoned-B protein and DAP-160 (intersectin). Biochem J 388 : 195 204.
19. Kopecka, M., Gabriel, M., Takeo, K., Yamaguchi, M., Svoboda, A., Ohkusu, M., et al 2001) Microtubules and actin cytoskeleton in Cryptococcus neoformans compared with ascomycetous budding and fission yeasts. Eur J Cell Biol 80 : 303 311. (Pubitemid 32390148)
20. Kozel, T.R. (1995) Virulence factors of Cryptococcus neoformans. Trends Microbiol 3 : 295 299.
21. Lemmon, M.A. Ferguson, K.M. (2000) Signal-dependent membrane targeting by pleckstrin homology (PH) domains. Biochem J 350 1 18.
22. Lengeler, K.B., Davidson, R.C., D'Souza, C., Harashima, T., Shen, W.-C., Wang, P., et al 2000) Signal transduction cascades regulating fungal development and virulence. Microbiol Mol Biol Rev 64 : 746 785. (Pubitemid 32475930)
23. Li, L., Shen, G., Zhang, Z.G., Wang, Y.L., Thompson, J.K. Wang, P. (2007) Canonical heterotrimeric G proteins regulating mating and virulence of Cryptococcus neoformans. Mol Biol Cell 18 : 4201 4209. (Pubitemid 350064226)
24. Malacombe, M., Ceridono, M., Calco, V., Chasserot-Golaz, S., McPherson, P.S., Bader, M.F. Gasman, S. (2006) Intersectin-1L nucleotide exchange factor regulates secretory granule exocytosis by activating Cdc42. EMBO J 25 : 3494 3503. (Pubitemid 44264860)
25. Martina, J.A., Bonangelino, C.J., Aguilar, R.C. Bonifacino, J.S. (2001) Stonin 2: an adaptor-like protein that interacts with components of the endocytic machinery. J Cell Biol 153 : 1111 1120.
26. Mayer, B.J. (2001) SH3 domains: complexity in moderation. J Cell Sci 114 : 1253 1263.
27. Miliaras, N.B., Park, J.H. Wendland, B. (2004) The function of the endocytic scaffold protein Pan1p depends on multiple domains. Traffic 5 : 963 978. (Pubitemid 39534488)
28. Mitchell, T.G. Perfect, J.R. (1995) Cryptococcosis in the era of AIDS - 100 years after the discovery of Cryptococcus neoformans. Clin Microbiol Rev 8 : 515 548.
29. Mohney, R.P., Das, M., Bivona, T.G., Hanes, R., Adams, A.G., Philips, M.R. O'Bryan, J.P. (2003) Intersectin activates Ras but stimulates transcription through an independent pathway involving JNK. J Biol Chem 278 : 47038 47045. (Pubitemid 37452288)
30. Nichols, C.B., Perfect, Z.H. Alspaugh, J.A. (2007) A Ras1-Cdc24 signal transduction pathway mediates thermotolerance in the fungal pathogen Cryptococcus neoformans. Mol Microbiol 63 : 1118 1130.
31. Nosanchuk, J.D., Nimrichter, L., Casadevall, A. Rodrigues, M.L. (2008) A role for vesicular transport of macromolecules across cell walls in fungal pathogenesis. Commun Integr Biol 1 : 37 39.
32. Okamoto, M., Schoch, S. Südhof, T.C. (1999) EHSH1/intersectin, a protein that contains EH and SH3 domains and binds to dynamin and SNAP-25. A protein connection between exocytosis and endocytosis? J Biol Chem 274 : 18446 18454. (Pubitemid 129529021)
33. Palmer, D.A., Thompson, J.K., Li, L., Prat, A. Wang, P. (2006) Gib2, a novel Gbeta-like/RACK1 homolog, functions as a Gbeta subunit in cAMP signaling and is essential in Cryptococcus neoformans. J Biol Chem 281 : 32596 32605. (Pubitemid 46036814)
34. Panepinto, J., Komperda, K., Frases, S., Park, Y.D., Djordjevic, J.T., Casadevall, A. Williamson, P.R. (2009) Sec6-dependent sorting of fungal extracellular exosomes and laccase of Cryptococcus neoformans. Mol Microbiol 71 : 1165 1176.
35. Paunola, E., Mattila, P.K. Lappalainen, P. (2002) WH2 domain: a small, versatile adapter for actin monomers. FEBS Lett 513 : 92 97. (Pubitemid 34242984)
36. Price, M.F., Wilkinson, I.D. Gentry, L.O. (1982) Plate method for detection of phospholipase activity in Candida albicans. Sabouraudia 20 : 7 14.
37. Pucharcós, C., Fuentes, J.J., Casas, C., Luna, S., Alcántara, S., Arbonés, M.L., et al 1999) 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 7 : 704 712.
38. Ram, A.F.J. Klis, F.M. (2006) Identification of fngal cell wall mutants using susceptibility assays based on Calcofluor white and Congo red. Nat Protoc 1 : 2253 2256.
39. Rodrigues, M.L., Nakayasu, E.S., Oliveira, D.L., Nimrichter, L., Nosanchuk, J.D., Almeida, I.C. Casadevall, A. (2008) Extracellular vesicles produced by Cryptococcus neoformans contain protein components associated with virulence. Eukaryot Cell 7 : 58 67. (Pubitemid 351959594)
40. Rohatgi, R., Ma, L., Miki, H., Lopez, M., Kirchhausen, T., Takenawa, T. Kirschner, M.W. (1999) The interaction between N-WASP and the Arp2/3 complex links Cdc42-dependent signals to actin assembly. Cell 97 : 221 231. (Pubitemid 129746811)
41. Roos, J. Kelly, R.B. (1998) Dap160, a neural-specific Eps15 homology and multiple SH3 domain-containing protein that interacts with Drosophila dynamin. J Biol Chem 273 : 19108 19119. (Pubitemid 28366307)
42. Sengar, A.S., Wang, W., Bishay, J., Cohen, S. Egan, S.E. (1999) The EH and SH3 domain Ese proteins regulate endocytosis by linking to dynamin and Eps15. EMBO J 18 : 1159 1171. (Pubitemid 29110301)
43. Shaw, G. (1996) The pleckstrin homology domain: an intriguing multifunctional protein module. Bioessays 18 35 46. (Pubitemid 3023116)
44. Shen, G., Wang, Y.L., Whittington, A., Li, L. Wang, P. (2008) The RGS protein Crg2 regulates pheromone and cyclic AMP signaling in Cryptococcus neoformans. Eukaryot Cell 7 : 1540 1548.
45. Snapper, S.B., Takeshima, F., Anton, I., Liu, C.H., Thomas, S.M., Nguyen, D., et al 2001) N-WASP deficiency reveals distinct pathways for cell surface projections and microbial actin-based motility. Nat Cell Biol 3 : 897 904. (Pubitemid 32952254)
46. Symons, M., Derry, J.M., Karlak, B., Jiang, S., Lemahieu, V., McCormick, F., et al 1996) Wiskott-Aldrich syndrome protein, a novel effector for the GTPase CDC42Hs, is implicated in actin polymerization. Cell 84 : 723 734. (Pubitemid 26094202)
47. Tong, X.K., Hussain, N.K., de Heuvel, E., Kurakin, A., Abi-Jaoude, E., Quinn, C.C., et al 2000) The endocytic protein intersectin is a major binding partner for the Ras exchange factor mSos1 in rat brain. EMBO J 19 : 1263 1271. (Pubitemid 30151022)
48. Vida, T.A. Emr, S.D. (1995) A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast. J Cell Biol 128 : 779 792.
49. Wang, P. Heitman, J. (1999) Signal transduction cascades regulating mating, filamentation, and virulence in Cryptococcus neoformans. Curr Opin Microbiol. 2 : 358 362. (Pubitemid 29366955)
50. Wang, P., Perfect, J.R. Heitman, J. (2000) The G-protein beta subunit GPB1 is required for mating and haploid fruiting in Cryptococcus neoformans. Mol Cell Biol 20 : 352 362. (Pubitemid 30002576)
51. Wang, P., Nichols, C.B., Lengeler, K.B., Cardenas, M.E., Cox, G.M., Perfect, J.R. Heitman, J. (2002) Mating-type-specific and non-specific PAK kinases play shared and divergent roles in Cryptococcus neoformans. Eukaryot Cell 1 : 257 272. (Pubitemid 36562402)
52. Wang, P., Cutler, J.E., King, J. Palmer, D. (2004) Mutation of the regulator of G protein signaling Crg1 increases virulence in Cryptococcus neoformans. Eukaryot Cell 3 : 1028 1035. (Pubitemid 39098878)
53. Wang, J.B., Wu, W.J. Cerione, R.A. (2005) Cdc42 and Ras cooperate to mediate cellular transformation by intersectin-L. J Biol Chem 280 : 22883 22891.
54. Waterman, S.R., Hacham, M., Panepinto, J., Hu, G.W., Shin, S.W. Williamson, P.R. (2007) Cell wall targeting of laccase of Cryptococcus neoformans during infection of mice. Infect Immun 75 : 714 722. (Pubitemid 46203433)
55. Wendland, B. Emr, S.D. (1998) Pan1p, yeast eps15, functions as a multivalent adaptor that coordinates protein-protein interactions essential for endocytosis. J Cell Biol 141 : 71 84. (Pubitemid 28182642)
56. Xue, C., Bahn, Y.S., Cox, G.M. Heitman, J. (2006) G protein-coupled receptor Gpr4 senses amino acids and activates the cAMP-PKA pathway in Cryptococcus neoformans. Mol Biol Cell 17 : 667 679. (Pubitemid 43191102)
57. Yamabhai, M., Hoffman, N.G., Hardison, N.L., McPherson, P.S., Castagnoli, L., Cesareni, G. Kay, B.K. (1998) Intersectin, a novel adaptor protein with two Eps15 homology and five Src homology 3 domains. J Biol Chem 273 : 31401 31407. (Pubitemid 28533159)
58. Yoneda, A. Doering, T.L. (2006) A eukaryotic capsular polysaccharide is synthesized intracellularly and secreted via exocytosis. Mol Biol Cell 17 : 5131 5140. (Pubitemid 44907356)
59. Zamanian, J.L. Kelly, R.B. (2003) Intersectin 1L guanine nucleotide exchange activity is regulated by adjacent src homology 3 domains that are also involved in endocytosis. Mol Biol Cell 14 : 1624 1637.