Intrinsically disordered proteins aggregate at fungal cell-to-cell channels and regulate intercellular connectivity

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 39, 2012, Pages 15781-15786

  Lai, Julian ^a   Koh, Chuan Hock ^a   Tjota, Monika ^a   Pieuchot, Laurent ^a   Raman, Vignesh ^a   Chandrababu, Karthik Balakrishna ^a   Yang, Daiwen ^a   Wong, Limsoon ^a   Jedd, Gregory ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Filamentous fungus; Multicellular organization; Neurospora crassa

Indexed keywords

FUNGAL PROTEIN;

ARTICLE; CELL COMPARTMENTALIZATION; FUNGAL CELL; FUNGAL STRUCTURES; FUNGUS SPORE; IN VITRO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN STRUCTURE;

CELL MEMBRANE; FUNGAL PROTEINS; MULTIPROTEIN COMPLEXES; NEUROSPORA CRASSA; PROTEIN STRUCTURE, SECONDARY;

ANIMALIA; FUNGI; NEUROSPORA CRASSA;

EID: 84866869780     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1207467109     Document Type: Article

References (45)

1. Bonner J (1999) The origins of multicellularity. Integrative Biology (Camb) 1(1):27- 36.
2. Rokas A (2008) The molecular origins of multicellular transitions. Curr Opin Genet Dev 18:472-478.
3. Zambryski P, Crawford K (2000) Plasmodesmata: Gatekeepers for cell-to-cell transport of developmental signals in plants. Annu Rev Cell Dev Biol 16:393-421. (Pubitemid 32037512)
4. Xu XM, Jackson D (2010) Lights at the end of the tunnel: New views of plasmodesmal structure and function. Curr Opin Plant Biol 13:684- 692.
5. Goodenough DA, Paul DL (2009) Gap junctions. Cold Spring Harb Perspect Biol 1:a002576.
6. Stajich JE, et al. (2009) The fungi. Curr Biol 19(18):R840-R845.
7. Jedd G (2011) Fungal evo-devo: Organelles and multicellular complexity. Trends Cell Biol 21(1):12-19.
8. van Peer AF, et al. (2009) The septal pore cap is an organelle that functions in vegetative growth and mushroom formation of the wood-rot fungus Schizophyllum commune. Environ Microbiol 12:833-844.
9. Jedd G, Chua NH (2000) A new self-assembled peroxisomal vesicle required for efficient resealing of the plasma membrane. Nat Cell Biol 2:226-231.
10. Tenney K, et al. (2000) Hex-1, a gene unique to filamentous fungi, encodes the major protein of the Woronin body and functions as a plug for septal pores. Fungal Genet Biol 31:205-217. (Pubitemid 32202697)
11. Maruyama J-I, Juvvadi PR, Ishi K, Kitamoto K (2005) Three-dimensional image analysis of plugging at the septal pore by Woronin body during hypotonic shock inducing hyphal tip bursting in the filamentous fungus Aspergillus oryzae. Biochem Biophys Res Commun 331:1081-1088. (Pubitemid 40692470)
12. Soundararajan S, et al. (2004) Woronin body function in Magnaporthe grisea is essential for efficient pathogenesis and for survival during nitrogen starvation stress. Plant Cell 16:1564-1574. (Pubitemid 38774249)
13. Trinci AP, Collinge AJ (1973) Structure and plugging of septa of wild type and spreading colonial mutants of Neurospora crassa. Arch Mikrobiol 91:355-364.
14. Read ND, Beckett A (1996) Ascus and ascospore morphogenesis. Mycol Res 100: 1281-1314.
15. Kimbrough JW (1994) Ascomycete Systematics: Problems and Perspectives in the Nineties, ed Hawksworth DL (Plenum, New York), pp 127-141.
16. Lai J, et al. (2010) Marker fusion tagging, a new method for production of chromosomally encoded fusion proteins. Eukaryot Cell 9:827-830.
17. Uversky VN, Dunker AK (2010) Understanding protein non-folding. Biochim Biophys Acta 1804:1231-1264.
18. Uversky VN (2011) Intrinsically disordered proteins from A to Z. Int J Biochem Cell Biol 43:1090-1103.
19. Koh CH, Lin S, Jedd G, Wong L (2009) Sirius PSB: A generic system for analysis of biological sequences. J Bioinform Comput Biol 7:973-990.
20. Denning DP, Patel SS, Uversky V, Fink AL, Rexach M (2003) Disorder in the nuclear pore complex: The FG repeat regions of nucleoporins are natively unfolded. Proc Natl Acad Sci USA 100:2450-2455. (Pubitemid 36297519)
21. Haynes C, Iakoucheva LM (2006) Serine/arginine-rich splicing factors belong to a class of intrinsically disordered proteins. Nucleic Acids Res 34:305 -312.
22. Trinci APJ, Collinge AJ (1974) Occlusion of the septal pores of damaged hyphae of Neurospora crassa by hexagonal crystals. Protoplasma 80(1):57-67.
23. Bouter A, et al. (2011) Annexin-A5 assembled into two-dimensional arrays promotes cell membrane repair. Nat Commun 2:270.
24. Silverman-Gavrila LB, Lew RR (2002) An IP3-activated Ca2+ channel regulates fungal tip growth. J Cell Sci 115:5013-5025. (Pubitemid 36054651)
25. Riedl J, et al. (2008) Lifeact: A versatile marker to visualize F-actin. Nat Methods 5:605-607. (Pubitemid 351911864)
26. Steinberg G (2007) Hyphal growth: A tale of motors, lipids, and the Spitzenkörper. Eukaryot Cell 6:351-360.
27. Fleissner A, Simonin AR, Glass NL (2008) Cell fusion in the filamentous fungus, Neurospora crassa. Methods Mol Biol 475:21- 38.
28. Glass NL, Rasmussen C, Roca MG, Read ND (2004) Hyphal homing, fusion and mycelial interconnectedness. Trends Microbiol 12(3):135-141. (Pubitemid 38314757)
29. Frey S, Richter RP, Görlich D (2006) FG-rich repeats of nuclear pore proteins form a three-dimensional meshwork with hydrogel-like properties. Science 314:815-817. (Pubitemid 44706647)
30. Toyama BH, Weissman JS (2011) Amyloid structure: Conformational diversity and consequences. Annu Rev Biochem 80:557-585.
31. Liu F, et al. (2008) Making two organelles from one: Woronin body biogenesis by peroxisomal protein sorting. J Cell Biol 180:325-339. (Pubitemid 351185919)
32. Fleissner A, Glass NL (2007) SO, a protein involved in hyphal fusion in Neurospora crassa, localizes to septal plugs. Eukaryot Cell 6:84-94. (Pubitemid 46147655)
33. Maruyama J-I, Escaño CS, Kitamoto K (2010) AoSO protein accumulates at the septal pore in response to various stresses in the filamentous fungus Aspergillus oryzae. Biochem Biophys Res Commun 391:868-873.
34. Fiumara F, Fioriti L, Kandel ER, Hendrickson WA (2010) Essential role of coiled coils for aggregation and activity of Q/N-rich prions and PolyQ proteins. Cell 143:1121- 1135.
35. Dunker AK, Silman I, Uversky VN, Sussman JL (2008) Function and structure of inherently disordered proteins. Curr Opin Struct Biol 18:756-764.
36. Wright PE, Dyson HJ (2009) Linking folding and binding. Curr Opin Struct Biol 19:31-38.
37. Demarest SJ, et al. (2002) Mutual synergistic folding in recruitment of CBP/p300 by p160 nuclear receptor coactivators. Nature 415:549-553. (Pubitemid 34130612)
38. Oldfield CJ, et al. (2008) Flexible nets: Disorder and induced fi t in the associations of p53 and 14-3-3 with their partners. BMC Genomics 9(Suppl 1):S1.
39. Serio TR, et al. (2000) Nucleated conformational conversion and the replication of conformational information by a prion determinant. Science 289:1317-1321. (Pubitemid 30656041)
40. Hyman AA, Brangwynne CP (2011) Beyond stereospecificity: Liquids and mesoscale organization of cytoplasm. Dev Cell 21(1):14-16.
41. Li P, et al. (2012) Phase transitions in the assembly of multivalent signalling proteins. Nature 483:336-340.
42. Perutz M (1994) Polar zippers: Their role in human disease. Protein Sci 3: 1629 - 1637.
43. Colot HV, et al. (2006) A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proc Natl Acad Sci USA 103:10352-10357. (Pubitemid 44051170)
44. Kasuga T, Mannhaupt G, Glass NL (2009) Relationship between phylogenetic distribution and genomic features in Neurospora crassa. PLoS ONE 4:e5286.
45. Dosztányi Z, Csizmok V, Tompa P, Simon I (2005) IUPred: Web server for the prediction of intrinsically unstructured regions of proteins based on estimated energy content. Bioinformatics 21:3433-3434. (Pubitemid 41222453)