Dual amyloid domains promote differential functioning of the chaplin proteins during Streptomyces aerial morphogenesis

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

Volumn 108, Issue 24, 2011, Pages 9821-9826

  Capstick, David S ^a   Jomaa, Ahmad ^a   Hanke, Chistopher ^a   Ortega, Joaquin ^a   Elliot, Marie A ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

Sporulation; Streptomyces development; Surface ultrastructure

Indexed keywords

AMYLOID PROTEIN; CHAPLIN H; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL SPORE; CARBOXY TERMINAL SEQUENCE; MORPHOGENESIS; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN SECONDARY STRUCTURE; SEQUENCE ANALYSIS; STREPTOMYCES COELICOLOR; ULTRASTRUCTURE;

AMINO ACID SEQUENCE; AMYLOID; AMYLOIDOGENIC PROTEINS; BACTERIAL PROTEINS; GENE DELETION; MICROSCOPY, ELECTRON; MOLECULAR SEQUENCE DATA; MUTATION; SEQUENCE HOMOLOGY, AMINO ACID; STREPTOMYCES COELICOLOR;

STREPTOMYCES; STREPTOMYCES COELICOLOR;

EID: 79959923860     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1018715108     Document Type: Article

References (43)

1. Chiti F, Dobson CM (2006) Protein misfolding, functional amyloid, and human disease. Annu Rev Biochem 75:333-366. (Pubitemid 44118036)
2. Bieler S, et al. (2005) Amyloid formation modulates the biological activity of a bacterial protein. J Biol Chem 280:26880-26885. (Pubitemid 41040722)
3. Oh J, et al. (2007) Amyloidogenesis of type III-dependent harpins from plant pathogenic bacteria. J Biol Chem 282:13601-13609. (Pubitemid 47100514)
4. Alteri CJ, et al. (2007) Mycobacterium tuberculosis produces pili during human infection. Proc Natl Acad Sci USA 104:5145-5150. (Pubitemid 47186190)
5. Romero D, Aguilar C, Losick R, Kolter R (2010) Amyloid fibers provide structural integrity to Bacillus subtilis biofilms. Proc Natl Acad Sci USA 107:2230-2234.
6. Hardy GG, et al. (2010) A localized multimeric anchor attaches the Caulobacter holdfast to the cell pole. Mol Microbiol 76:409-427.
7. Dueholm MS, et al. (2010) Functional amyloid in Pseudomonas. Mol Microbiol 77:1009-1020.
8. Barnhart MM, Chapman MR (2006) Curli biogenesis and function. Annu Rev Microbiol 60:131-147. (Pubitemid 44627943)
9. de Jong W, Wosten HA, Dijkhuizen L, Claessen D (2009) Attachment of Streptomyces coelicolor is mediated by amyloidal fimbriae that are anchored to the cell surface via cellulose. Mol Microbiol 73:1128-1140.
10. Capstick DS, Willey JM, Buttner MJ, Elliot MA (2007) SapB and the chaplins: connections between morphogenetic proteins in Streptomyces coelicolor. Mol Microbiol 64:602-613. (Pubitemid 46653204)
11. Elliot MA, et al. (2003) The chaplins: a family of hydrophobic cell-surface proteins involved in aerial mycelium formation in Streptomyces coelicolor. Genes Dev 17:1727-1740. (Pubitemid 36870336)
12. Claessen D, et al. (2003) A novel class of secreted hydrophobic proteins is involved in aerial hyphae formation in Streptomyces coelicolor by forming amyloid-like fibrils. Genes Dev 17:1714-1726. (Pubitemid 36870335)
13. Elliot MA, Buttner MJ, Nodwell JR (2007) Multicellular development in Streptomyces. Myxobacteria: Multicellularity and Differentiation, ed DE Whitworth (American Society for Microbiology Press, Washington, DC), pp 419-438.
14. Willey JM, Willems A, Kodani S, Nodwell JR (2006) Morphogenetic surfactants and their role in the formation of aerial hyphae in Streptomyces coelicolor. Mol Microbiol 59:731-742.
15. Di Berardo C, et al. (2008) Function and redundancy of the chaplin cell surface proteins in aerial hypha formation, rodlet assembly, and viability in Streptomyces coelicolor. J Bacteriol 190:5879-5889.
16. Claessen D, et al. (2004) The formation of the rodlet layer of streptomycetes is the result of the interplay between rodlins and chaplins. Mol Microbiol 53:433-443. (Pubitemid 38998166)
17. Claessen D, et al. (2002) Two novel homologous proteins of Streptomyces coelicolor and Streptomyces lividans are involved in the formation of the rodlet layer and mediate attachment to a hydrophobic surface. Mol Microbiol 44:1483-1492. (Pubitemid 34639427)
18. Esteras-Chopo A, Serrano L, Lopez de la Paz M (2005) The amyloid stretch hypothesis: recruiting proteins toward the dark side. Proc Natl Acad Sci USA 102:16672-16677.
19. Pastor MT, Esteras-Chopo A, Serrano L (2007) Hacking the code of amyloid formation: the amyloid stretch hypothesis. Prion 1:9-14.
20. LeVine H, III (1999) Quantification of beta-sheet amyloid fibril structures with thioflavin T. Methods Enzymol 309:274-284.
21. Fernandez-Escamilla AM, Rousseau F, Schymkowitz J, Serrano L (2004) Prediction of sequence-dependent and mutational effects on the aggregation of peptides and proteins. Nat Biotechnol 22:1302-1306. (Pubitemid 39336784)
22. Conchillo-Sole O, et al. (2007) AGGRESCAN: a server for the prediction and evaluation of "hot spots" of aggregation in polypeptides. BMC Bioinformatics 8:65.
23. Garbuzynskiy SO, Lobanov MY, Galzitskaya OV (2010) FoldAmyloid: a method of prediction of amyloidogenic regions from protein sequence. Bioinformatics 26:326-332.
24. Bryson K, et al. (2005) Protein structure prediction servers at University College London. Nucleic Acids Res 33(Web Server issue):W36-38.
25. Cole C, Barber JD, Barton GJ (2008) The Jpred 3 secondary structure prediction server. Nucleic Acids Res 36(Web Server issue):W197-201.
26. Otzen D, Nielsen PH (2008) We find them here, we find them there: functional bacterial amyloid. Cell Mol Life Sci 65:910-927.
27. Wang X, Hammer ND, Chapman MR (2008) The molecular basis of functional bacterial amyloid polymerization and nucleation. J Biol Chem 283:21530-21539.
28. Wang X, Smith DR, Jones JW, Chapman MR (2007) In vitro polymerization of a functional Escherichia coli amyloid protein. J Biol Chem 282:3713-3719.
29. Westermark G, et al. (1999) Differences in amyloid deposition in islets of transgenic mice expressing human islet amyloid polypeptide versus human islets implanted into nude mice. Metabolism 48:448-454. (Pubitemid 29174222)
30. Nilsson MR, Raleigh DP (1999) Analysis of amylin cleavage products provides new insights into the amyloidogenic region of human amylin. J Mol Biol 294:1375-1385. (Pubitemid 30008807)
31. Jaikaran ET, et al. (2001) Identification of a novel human islet amyloid polypeptide beta-sheet domain and factors influencing fibrillogenesis. J Mol Biol 308:515-525. (Pubitemid 33027616)
32. BucciantiniM, et al. (2002) Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases. Nature 416:507-511.
33. Caughey B, Lansbury PT (2003) Protofibrils, pores, fibrils, and neurodegeneration: separating the responsible protein aggregates from the innocent bystanders. Annu Rev Neurosci 26:267-298. (Pubitemid 37064935)
34. Kim W, Hecht MH (2006) Generic hydrophobic residues are sufficient to promote aggregation of the Alzheimer's Abeta42 peptide. Proc Natl Acad Sci USA 103:15824-15829. (Pubitemid 44657551)
35. DePace AH, Santoso A, Hillner P, Weissman JS (1998) A critical role for amino-terminal glutamine/asparagine repeats in the formation and propagation of a yeast prion. Cell 93:1241-1252. (Pubitemid 28307428)
36. Michelitsch MD, Weissman JS (2000) A census of glutamine/asparagine-rich regions: implications for their conserved function and the prediction of novel prions. Proc Natl Acad Sci USA 97:11910-11915.
37. Hanahan D (1983) Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166:557-580.
38. MacNeil DJ, et al. (1992) Analysis of Streptomyces avermitilis genes required for avermectin biosynthesis utilizing a novel integration vector. Gene 111:61-68.
39. Paget MS, Chamberlin L, Atrih A, Foster SJ, Buttner MJ (1999) Evidence that the extracytoplasmic function sigma factor sigmaE is required for normal cell wall structure in Streptomyces coelicolor A3(2). J Bacteriol 181:204-211. (Pubitemid 29013672)
40. Kieser T, Bibb MJ, Buttner MJ, Chater KF, Hopwood DA (2000) Practical Streptomyces genetics (The John Innes Foundation, Norwich, United Kingdom).
41. Janssen GR, Bibb MJ (1993) Derivatives of pUC18 that have BglII sites flanking a modified multiple cloning site and that retain the ability to identify recombinant clones by visual screening of Escherichia coli colonies. Gene 124:133-134. (Pubitemid 23065980)
42. Bierman M, et al. (1992) Plasmid cloning vectors for the conjugal transfer of DNA from Escherichia coli to Streptomyces spp. Gene 116:43-49.
43. Haiser HJ, Yousef MR, Elliot MA (2009) Cell wall hydrolases affect germination, vegetative growth, and sporulation in Streptomyces coelicolor. J Bacteriol 191:6501-6512.