Mycobacteriophage D29 holin C-terminal region functionally assists in holin aggregation and bacterial cell death

FEBS Journal

Volumn 283, Issue 1, 2016, Pages 173-190

  Kamilla, Soumya ^a   Jain, Vikas ^a  

^a INDIAN INSTITUTE OF SCIENCE EDUCATION AND RESEARCH BHOPAL   (India)

Author keywords

bacterial cell death; coiled coil motif; endolysin; membrane perforation; transmembrane domain

Indexed keywords

ASPARTIC ACID; GLYCINE; HOLIN; MEMBRANE PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL CELL; CARBOXY TERMINAL SEQUENCE; CELL DEATH; CELL MEMBRANE; CONTROLLED STUDY; CYTOTOXICITY; ESCHERICHIA COLI; MYCOBACTERIOPHAGE; MYCOBACTERIUM SMEGMATIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; CHEMISTRY; CYTOLOGY; GENETICS; METABOLISM; MICROBIAL VIABILITY; PATHOGENICITY; VIROLOGY;

ESCHERICHIA COLI; MICROBIAL VIABILITY; MYCOBACTERIOPHAGES; MYCOBACTERIUM SMEGMATIS; VIRAL PROTEINS;

EID: 84957729059     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.13565     Document Type: Article

References (59)

1. Young I, Wang I, &, Roof WD, (2000) Phages will out: strategies of host cell lysis. Trends Microbiol 8, 120-128.
2. Young R, (1992) Bacteriophage lysis: mechanism and regulation. Microbiol Rev 56, 430-481.
3. Smith DL, Chang CY, &, Young R, (1998) The λ holin accumulates beyond the lethal triggering concentration under hyperexpression conditions. Gene Expr 7, 39-52.
4. Wang IN, Smith DL, &, Young R, (2000) Holins: the protein clocks of bacteriophage infections. Annu Rev Microbiol 54, 799-825.
5. Zagotta MT, &, Wilson DB, (1990) Oligomerization of the bacteriophage lambda S protein in the inner membrane of Escherichia coli. J Bacteriol 172, 912-921.
6. Shi Y, Yan Y, Ji W, Du B, Meng X, Wang H, &, Sun J, (2012) Characterization and determination of holin protein of Streptococcus suis bacteriophage SMP in heterologous host. Virol J 9, 70.
7. Young R, &, Blasi U, (1995) Holins: form and function in bacteriophage lysis. FEMS Microbiol Rev 17, 191-205.
8. Young R, (2002) Bacteriophage holins: deadly diversity. J Mol Microbiol Biotechnol 4, 21-36.
9. Grundling A, Smith DL, Blasi U, &, Young R, (2000) Dimerization between the holin and holin inhibitor of phage lambda. J Bacteriol 182, 6075-6081.
10. Blasi U, &, Young R, (1996) Two beginnings for a single purpose: the dual-start holins in the regulation of phage lysis. Mol Microbiol 21, 675-682.
11. Blasi U, Chang CY, Zagotta MT, Nam KB, &, Young R, (1990) The lethal λ S gene encodes its own inhibitor. EMBO J 9, 981-989.
12. Ryan GL, &, Rutenberg AD, (2007) Clocking out: modeling phage-induced lysis of Escherichia coli. J Bacteriol 189, 4749-4755.
13. White R, Chiba S, Pang T, Dewey JS, Savva CG, Holzenburg A, Pogliano K, &, Young R, (2011) Holin triggering in real time. Proc Natl Acad Sci USA 108, 798-803.
14. Barenboim M, Chang CY, dib Hajj F, &, Young R, (1999) Characterization of the dual start motif of a class II holin gene. Mol Microbiol 32, 715-727.
15. Chang CY, Nam K, &, Young R, (1995) S gene expression and the timing of lysis by bacteriophage lambda. J Bacteriol 177, 3283-3294.
16. Raab R, Neal G, Sohaskey C, Smith J, &, Young R, (1988) Dominance in λ S mutations and evidence for translational control. J Mol Biol 199, 95-105.
17. Walker JT, &, Walker DH, (1980) Mutations in coliphage p1 affecting host cell lysis. J Virol 35, 519-530.
18. Catalao MJ, Gil F, Moniz-Pereira J, &, Pimentel M, (2011) Functional analysis of the holin-like proteins of mycobacteriophage Ms6. J Bacteriol 193, 2793-2803.
19. Park T, Struck DK, Dankenbring CA, &, Young R, (2007) The pinholin of lambdoid phage 21: control of lysis by membrane depolarization. J Bacteriol 189, 9135-9139.
20. Park T, Struck DK, Deaton JF, &, Young R, (2006) Topological dynamics of holins in programmed bacterial lysis. Proc Natl Acad Sci USA 103, 19713-19718.
21. Xu M, Arulandu A, Struck DK, Swanson S, Sacchettini JC, &, Young R, (2005) Disulfide isomerization after membrane release of its SAR domain activates P1 lysozyme. Science 307, 113-117.
22. Xu M, Struck DK, Deaton J, Wang IN, &, Young R, (2004) A signal-arrest-release sequence mediates export and control of the phage P1 endolysin. Proc Natl Acad Sci USA 101, 6415-6420.
23. Pohane AA, &, Jain V, (2015) Insights into the regulation of bacteriophage endolysin: Multiple means to the same end. Microbiology. doi: 10.1099/mic.0.000190 (in press).
24. Payne KM, &, Hatfull GF, (2012) Mycobacteriophage endolysins: diverse and modular enzymes with multiple catalytic activities. PLoS ONE 7, e34052.
25. Hassan S, Dusthackeer A, Subramanyam B, Ponnuraja C, Sivaramakrishnan GN, &, Kumar V, (2010) Lytic efficiency of mycobacteriophages. Open Sys Biol J 3, 21-28.
26. Catalao MJ, Gil F, Moniz-Pereira J, Sao-Jose C, &, Pimentel M, (2013) Diversity in bacterial lysis systems: bacteriophages show the way. FEMS Microbiol Rev 37, 554-571.
27. Pohane AA, Joshi H, &, Jain V, (2014) Molecular dissection of phage endolysin: an interdomain interaction confers host specificity in Lysin A of Mycobacterium phage D29. J Biol Chem 289, 12085-12095.
28. Payne K, Sun Q, Sacchettini J, &, Hatfull GF, (2009) Mycobacteriophage Lysin B is a novel mycolylarabinogalactan esterase. Mol Microbiol 73, 367-381.
29. Tusnady GE, &, Simon I, (2001) The HMMTOP transmembrane topology prediction server. Bioinformatics 17, 849-850.
30. Hirokawa T, Boon-Chieng S, &, Mitaku S, (1998) SOSUI: classification and secondary structure prediction system for membrane proteins. Bioinformatics 14, 378-379.
31. Krogh A, Larsson B, von Heijne G, &, Sonnhammer EL, (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305, 567-580.
32. von Heijne G, (1992) Membrane protein structure prediction. Hydrophobicity analysis and the positive-inside rule. J Mol Biol 225, 487-494.
33. Cserzo M, Eisenhaber F, Eisenhaber B, &, Simon I, (2002) On filtering false positive transmembrane protein predictions. Protein Eng 15, 745-752.
34. Viklund H, &, Elofsson A, (2008) OCTOPUS: improving topology prediction by two-track ANN-based preference scores and an extended topological grammar. Bioinformatics 24, 1662-1668.
35. Kall L, Krogh A, &, Sonnhammer EL, (2007) Advantages of combined transmembrane topology and signal peptide prediction-the Phobius web server. Nucleic Acids Res 35, W429-W432.
36. Bernsel A, Viklund H, Hennerdal A, &, Elofsson A, (2009) TOPCONS: consensus prediction of membrane protein topology. Nucleic Acids Res 37, W465-W468.
37. Reynolds SM, Kall L, Riffle ME, Bilmes JA, &, Noble WS, (2008) Transmembrane topology and signal peptide prediction using dynamic bayesian networks. PLoS Comput Biol 4, e1000213.
38. Kall L, Krogh A, &, Sonnhammer EL, (2005) An HMM posterior decoder for sequence feature prediction that includes homology information. Bioinformatics 21 (Suppl 1), i251-i257.
39. Yuan Z, Mattick JS, &, Teasdale RD, (2004) SVMtm: support vector machines to predict transmembrane segments. J Comput Chem 25, 632-636.
40. Persson B, &, Argos P, (1994) Prediction of transmembrane segments in proteins utilising multiple sequence alignments. J Mol Biol 237, 182-192.
41. Nugent T, &, Jones DT, (2009) Transmembrane protein topology prediction using support vector machines. BMC Bioinformatics 10, 159.
42. Shen H, &, Chou JJ, (2008) MemBrain: improving the accuracy of predicting transmembrane helices. PLoS ONE 3, e2399.
43. Guzman LM, Belin D, Carson MJ, &, Beckwith J, (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177, 4121-4130.
44. Amann E, Ochs B, &, Abel KJ, (1988) Tightly regulated tac promoter vectors useful for the expression of unfused and fused proteins in Escherichia coli. Gene 69, 301-315.
45. Diaz E, Munthali M, Lunsdorf H, Holtje JV, &, Timmis KN, (1996) The two-step lysis system of pneumococcal bacteriophage EJ-1 is functional in gram-negative bacteria: triggering of the major pneumococcal autolysin in Escherichia coli. Mol Microbiol 19, 667-681.
46. Jolliffe LK, Doyle RJ, &, Streips UN, (1981) The energized membrane and cellular autolysis in Bacillus subtilis. Cell 25, 753-763.
47. Reddy BL, &, Saier MH Jr, (2013) Topological and phylogenetic analyses of bacterial holin families and superfamilies. Biochim Biophys Acta 1828, 2654-2671.
48. Lupas A, Van Dyke M, &, Stock J, (1991) Predicting coiled coils from protein sequences. Science 252, 1162-1164.
49. Blasi U, Fraisl P, Chang CY, Zhang N, &, Young R, (1999) The C-terminal sequence of the lambda holin constitutes a cytoplasmic regulatory domain. J Bacteriol 181, 2922-2929.
50. Lella M, &, Mahalakshmi R, (2013) Pro-Gly mediated conformational switch of mycobacteriophage D29 holin transmembrane domain I is lipid concentration driven. Chem Commun 49, 9594-9596.
51. Delisle AL, Barcak GJ, &, Guo M, (2006) Isolation and expression of the lysis genes of Actinomyces naeslundii phage Av-1. Appl Environ Microbiol 72, 1110-1117.
52. Steiner JP, Payne KB, Main CD, D'Alfonso S, Jacobsen KX, Hicks TP, Staines WA, &, Poulter MO, (2010) GPI-1046 increases presenilin-1 expression and restores NMDA channel activity. Can J Neurol Sci 37, 457-467.
53. Pohane AA, Patidar ND, &, Jain V, (2015) Modulation of domain-domain interaction and protein function by a charged linker: a case study of mycobacteriophage D29 endolysin. FEBS Lett 589, 695-701.
54. Thompson JD, Higgins DG, &, Gibson TJ, (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22, 4673-4680.
55. Hall TA, (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41, 95-98.
56. Sambrook J, &, Russell D, (2001) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, New York.
57. Shenoy AR, &, Visweswariah SS, (2003) Site-directed mutagenesis using a single mutagenic oligonucleotide and DpnI digestion of template DNA. Anal Biochem 319, 335-336.
58. Jain V, Saleem-Batcha R, China A, &, Chatterji D, (2006) Molecular dissection of the mycobacterial stringent response protein Rel. Protein Sci 15, 1449-1464.
59. Singh MI, &, Jain V, (2013) Tagging the expressed protein with 6 histidines: rapid cloning of an amplicon with three options. PLoS ONE 8, e63922.