Two DHH subfamily 1 proteins in Streptococcus pneumoniae possess cyclic Di-AMP phosphodiesterase activity and affect bacterial growth and virulence

Journal of Bacteriology

Volumn 195, Issue 22, 2013, Pages 5123-5132

  Bai, Yinlan ^a,d   Yang, Jun ^a   Eisele, Leslie E ^b   Underwood, Adam J ^a   Koestler, Benjamin J ^c   Waters, Christopher M ^c   Metzger, Dennis W ^a   Bai, Guangchun ^a  

^a ALBANY MEDICAL COLLEGE   (United States)

^b WADSWORTH CENTER   (United States)

^c Michigan State University ^*  (United States)

^d FOURTH MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE; ADENOSINE TRIPHOSPHATE; ADENYLATE CYCLASE; BACTERIUM LYSATE; CYCLIC AMP PHOSPHODIESTERASE; CYCLIC DI AMP PHOSPHODIESTERASE; CYCLIC NUCLEOTIDE PHOSPHODIESTERASE 1; CYCLIC NUCLEOTIDE PHOSPHODIESTERASE 2; DIADENYLATE CYCLASE; ERYTHROMYCIN; KANAMYCIN; PHOSPHOADENYLYL ADENOSINE; STREPTOMYCIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GROWTH; BACTERIAL LOAD; BACTERIAL VIRULENCE; COLONY FORMING UNIT; CONTROLLED STUDY; DELETION MUTANT; ENZYME ACTIVITY; FEMALE; GEL FILTRATION; GENETIC ANALYSIS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; NONHUMAN; PATHOGENESIS; PENICILLIN RESISTANCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; STREPTOCOCCUS PNEUMONIAE; SURVIVAL RATE; SURVIVAL TIME; ULTRAVIOLET RADIATION; WESTERN BLOTTING;

3',5'-CYCLIC-AMP PHOSPHODIESTERASES; ANIMALS; BACTERIAL PROTEINS; DINUCLEOSIDE PHOSPHATES; DISEASE MODELS, ANIMAL; MICE; PNEUMONIA, PNEUMOCOCCAL; STREPTOCOCCUS PNEUMONIAE; VIRULENCE FACTORS;

EID: 84887258278     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00769-13     Document Type: Article

References (64)

1. Davies BW, Bogard RW, Young TS, Mekalanos JJ. 2012. Coordinated regulation of accessory genetic elements produces cyclic di-nucleotides for V. cholerae virulence. Cell 149:358-370.
2. Gomelsky M. 2011. cAMP, c-di-GMP, c-di-AMP and now cGMP:bacteria use them all! Mol. Microbiol. 79:562-565.
3. Camilli A, Bassler BL. 2006. Bacterial small-molecule signaling pathways. Science 311:1113-1116.
4. Hengge R. 2009. Principles of c-di-GMP signalling in bacteria. Nat. Rev. Microbiol. 7:263-273.
5. Hammer BK, Bassler BL. 2009. Distinct sensory pathways in Vibrio cholerae El Tor and classical biotypes modulate cyclic dimeric GMP levels to control biofilm formation. J. Bacteriol. 191:169-177.
6. Kazmierczak BI, Lebron MB, Murray TS. 2006. Analysis of FimX, a phosphodiesterase that governs twitching motility in Pseudomonas aeruginosa. Mol. Microbiol. 60:1026-1043.
7. Kulasakara H, Lee V, Brencic A, Liberati N, Urbach J, Miyata S, Lee DG, Neely AN, Hyodo M, Hayakawa Y, Ausubel FM, Lory S. 2006. Analysis of Pseudomonas aeruginosa diguanylate cyclases and phosphodiesterases reveals a role for bis-(3'-5')-cyclic-GMP in virulence. Proc. Natl. Acad. Sci. U.S.A. 103:2839-2844.
8. Lamprokostopoulou A, Monteiro C, Rhen M, Romling U. 2010. Cyclic di-GMP signalling controls virulence properties of Salmonella enterica serovar Typhimurium at the mucosal lining. Environ. Microbiol. 12:40-53.
9. Lim B, Beyhan S, Yildiz FH. 2007. Regulation of Vibrio polysaccharide synthesis and virulence factor production by CdgC, a GGDEF-EAL domain protein, in Vibrio cholerae. J. Bacteriol. 189:717-729.
10. Martinez-Wilson HF, Tamayo R, Tischler AD, Lazinski DW, Camilli A. 2008. The Vibrio cholerae hybrid sensor kinase VieS contributes to motility and biofilm regulation by altering the cyclic diguanylate level. J. Bacteriol. 190:6439-6447.
11. Ryan RP, Lucey J, O'Donovan K, McCarthy Y, Yang L, Tolker-Nielsen T, Dow JM. 2009. HD-GYP domain proteins regulate biofilm formation and virulence in Pseudomonas aeruginosa. Environ. Microbiol. 11:1126-1136.
12. Tamayo R, Schild S, Pratt JT, Camilli A. 2008. Role of cyclic di-GMP during El Tor biotype Vibrio cholerae infection:characterization of the in vivo-induced cyclic di-GMP phosphodiesterase CdpA. Infect. Immun. 76: 1617-1627.
13. Tischler AD, Camilli A. 2004. Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation. Mol. Microbiol. 53:857-869.
14. Tischler AD, Camilli A. 2005. Cyclic diguanylate regulates Vibrio cholerae virulence gene expression. Infect. Immun. 73:5873-5882.
15. Hisert KB, MacCoss M, Shiloh MU, Darwin KH, Singh S, Jones RA, Ehrt S, Zhang Z, Gaffney BL, Gandotra S, Holden DW, Murray D, Nathan C. 2005. A glutamate-alanine-leucine (EAL) domain protein of Salmonella controls bacterial survival in mice, antioxidant defence and killing of macrophages:role of cyclic diGMP. Mol. Microbiol. 56:1234-1245.
16. Bobrov AG, Kirillina O, Perry RD. 2007. Regulation of biofilm formation in Yersinia pestis. Adv. Exp. Med. Biol. 603:201-210.
17. Borlee BR, Goldman AD, Murakami K, Samudrala R, Wozniak DJ, Parsek MR. 2010. Pseudomonas aeruginosa uses a cyclic-di-GMPregulated adhesin to reinforce the biofilm extracellular matrix. Mol. Microbiol. 75:827-842.
18. Grantcharova N, Peters V, Monteiro C, Zakikhany K, Romling U. 2010. Bistable expression of CsgD in biofilm development of Salmonella enterica serovar Typhimurium. J. Bacteriol. 192:456-466.
19. Krasteva PV, Fong JC, Shikuma NJ, Beyhan S, Navarro MV, Yildiz FH, Sondermann H. 2010. Vibrio cholerae VpsT regulates matrix production and motility by directly sensing cyclic di-GMP. Science 327:866-868.
20. Witte G, Hartung S, Buttner K, Hopfner KP. 2008. Structural biochemistry of a bacterial checkpoint protein reveals diadenylate cyclase activity regulated by DNA recombination intermediates. Mol. Cell 30:167-178.
21. Bejerano-Sagie M, Oppenheimer-Shaanan Y, Berlatzky I, Rouvinski A, Meyerovich M, Ben-Yehuda S. 2006. A checkpoint protein that scans the chromosome for damage at the start of sporulation in Bacillus subtilis. Cell 125:679-690.
22. Corrigan RM, Grundling A. 2013. Cyclic di-AMP:another second messenger enters the fray. Nat. Rev. Microbiol. 11:513-524.
23. Romling U. 2008. Great times for small molecules:c-di-AMP, a second messenger candidate in Bacteria and Archaea. Sci. Signal. 1:pe39. doi:10.1126/scisignal.133pe39.
24. Mehne FM, Gunka K, Eilers H, Herzberg C, Kaever V, Stulke J. 2013. Cyclic di-AMP homeostasis in Bacillus subtilis:both lack and high-level accumulation of the nucleotide are detrimental for cell growth. J. Biol. Chem. 288:2004-2017.
25. Corrigan RM, Abbott JC, Burhenne H, Kaever V, Grundling A. 2011. c-di-AMP is a new second messenger in Staphylococcus aureus with a role in controlling cell size and envelope stress. PLoS Pathog. 7:e1002217. doi:101371/journal.ppat.1002217.
26. Rao F, See RY, Zhang D, Toh DC, Ji Q, Liang ZX. 2010. YybT is a signaling protein that contains a cyclic dinucleotide phosphodiesterase domain and a GGDEF domain with ATPase activity. J. Biol. Chem. 285: 473-482.
27. Oppenheimer-Shaanan Y, Wexselblatt E, Katzhendler J, Yavin E, Ben-Yehuda S. 2011. c-di-AMP reports DNA integrity during sporulation in Bacillus subtilis. EMBO Rep. 12:594-601.
28. Luo Y, Helmann JD. 2012. Analysis of the role of Bacillus subtilis sigma(M) in beta-lactam resistance reveals an essential role for c-di-AMP in peptidoglycan homeostasis. Mol. Microbiol. 83:623-639.
29. Banerjee R, Gretes M, Harlem C, Basuino L, Chambers HF. 2010. A mecA-negative strain of methicillin-resistant Staphylococcus aureus with high-level beta-lactam resistance contains mutations in three genes. Antimicrob. Agents Chemother. 54:4900-4902.
30. Corrigan RM, Campeotto I, Jeganathan T, Roelofs KG, Lee VT, Grundling A. 2013. Systematic identification of conserved bacterial c-di-AMP receptor proteins. Proc. Natl. Acad. Sci. U.S.A. 110:9084-9089.
31. Griffiths JM, O'Neill AJ. 2012. Loss of function of the GdpP protein leads to joint beta-lactam/glycopeptide tolerance in Staphylococcus aureus. Antimicrob. Agents Chemother. 56:579-581.
32. Holland LM, O'Donnell ST, Ryjenkov DA, Gomelsky L, Slater SR, Fey PD, Gomelsky M, O'Gara JP. 2008. A staphylococcal GGDEF domain protein regulates biofilm formation independently of cyclic dimeric GMP. J. Bacteriol. 190:5178-5189.
33. Parvatiyar K, Zhang Z, Teles RM, Ouyang S, Jiang Y, Iyer SS, Zaver SA, Schenk M, Zeng S, Zhong W, Liu ZJ, Modlin RL, Liu YJ, Cheng G. 2012. The helicase DDX41 recognizes the bacterial secondary messengers cyclic di-GMP and cyclic di-AMP to activate a type I interferon immune response. Nat. Immunol. 13:1155-1161.
34. Sauer JD, Sotelo-Troha K, von Moltke J, Monroe KM, Rae CS, Brubaker SW, Hyodo M, Hayakawa Y, Woodward JJ, Portnoy DA, Vance RE. 2011. The N-ethyl-N-nitrosourea-induced Goldenticket mouse mutant reveals an essential function of Sting in the in vivo interferon response to Listeria monocytogenes and cyclic dinucleotides. Infect. Immun. 79: 688-694.
35. Schwartz KT, Carleton JD, Quillin SJ, Rollins SD, Portnoy DA, Leber JH. 2012. Hyperinduction of host beta interferon by a Listeria monocytogenes strain naturally overexpressing the multidrug efflux pump MdrT. Infect. Immun. 80:1537-1545.
36. Woodward JJ, Iavarone AT, Portnoy DA. 2010. c-di-AMP secreted by intracellular Listeria monocytogenes activates a host type I interferon response. Science 328:1703-1705.
37. Yamamoto T, Hara H, Tsuchiya K, Sakai S, Fang R, Matsuura M, Nomura T, Sato F, Mitsuyama M, Kawamura I. 2012. Listeria monocytogenes strain-specific impairment of the TetR regulator underlies the drastic increase in cyclic di-AMP secretion and beta interferon-inducing ability. Infect. Immun. 80:2323-2332.
38. Burdette DL, Monroe KM, Sotelo-Troha K, Iwig JS, Eckert B, Hyodo M, Hayakawa Y, Vance RE. 2011. STING is a direct innate immune sensor of cyclic di-GMP. Nature 478:515-518.
39. Jin L, Hill KK, Filak H, Mogan J, Knowles H, Zhang B, Perraud AL, Cambier JC, Lenz LL. 2011. MPYS is required for IFN response factor 3 activation and type I IFN production in the response of cultured phagocytes to bacterial second messengers cyclic-di-AMP and cyclic-di-GMP. J. Immunol. 187:2595-2601.
40. Bowie AG. 2012. Innate sensing of bacterial cyclic dinucleotides:more than just STING. Nat. Immunol. 13:1137-1139.
41. Kamegaya T, Kuroda K, Hayakawa Y. 2011. Identification of a Streptococcus pyogenes SF370 gene involved in production of c-di-AMP. Nagoya J. Med. Sci. 73:49-57.
42. Lu L, Ma Y, Zhang J-R. 2006. Streptococcus pneumoniae recruits complement factor H through the amino terminus of CbpA. J. Biol. Chem. 281: 15464-15474.
43. Sung CK, Li H, Claverys JP, Morrison DA. 2001. An rpsL cassette, janus, for gene replacement through negative selection in Streptococcus pneumoniae. Appl. Environ. Microbiol. 67:5190-5196.
44. Bai G, Gazdik MA, Schaak DD, McDonough KA. 2007. The Mycobacterium bovis BCG cyclic AMP receptor-like protein is a functional DNA binding protein in vitro and in vivo, but its activity differs from that of its M. tuberculosis ortholog, Rv3676. Infect. Immun. 75:5509-5517.
45. Bai G, McCue LA, McDonough KA. 2005. Characterization of Mycobacterium tuberculosis Rv3676 (CRPMt), a cyclic AMP receptor protein-like DNA binding protein. J. Bacteriol. 187:7795-7804.
46. Bai Y, Yang J, Zhou X, Ding X, Eisele LE, Bai G. 2012. Mycobacterium tuberculosis Rv3586 (DacA) is a diadenylate cyclase that converts ATP or ADP into c-di-AMP. PLoS One 7:e35206. doi:10.1371/journal.pone.0035206.
47. Christen M, Christen B, Folcher M, Schauerte A, Jenal U. 2005. Identification and characterization of a cyclic di-GMP-specific phosphodiesterase and its allosteric control by GTP. J. Biol. Chem. 280:30829-30837.
48. Ryjenkov DA, Tarutina M, Moskvin OV, Gomelsky M. 2005. Cyclic diguanylate is a ubiquitous signaling molecule in bacteria:insights into biochemistry of the GGDEF protein domain. J. Bacteriol. 187:1792-1798.
49. Massie JP, Reynolds EL, Koestler BJ, Cong JP, Agostoni M, Waters CM. 2012. Quantification of high-specificity cyclic diguanylate signaling. Proc. Natl. Acad. Sci. U.S.A. 109:12746-12751.
50. Lanie JA, Ng WL, Kazmierczak KM, Andrzejewski TM, Davidsen TM, Wayne KJ, Tettelin H, Glass JI, Winkler ME. 2007. Genome sequence of Avery's virulent serotype 2 strain D39 of Streptococcus pneumoniae and comparison with that of unencapsulated laboratory strain R6. J. Bacteriol. 189:38-51.
51. Song JH, Ko KS, Lee JY, Baek JY, Oh WS, Yoon HS, Jeong JY, Chun J. 2005. Identification of essential genes in Streptococcus pneumoniae by allelic replacement mutagenesis. Mol. Cells 19:365-374.
52. Cron LE, Stol K, Burghout P, van Selm S, Simonetti ER, Bootsma HJ, Hermans PW. 2011. Two DHH subfamily 1 proteins contribute to pneumococcal virulence and confer protection against pneumococcal disease. Infect. Immun. 79:3697-3710.
53. Rao F, Ji Q, Soehano I, Liang ZX. 2011. Unusual heme-binding PAS domain from YybT family proteins. J. Bacteriol. 193:1543-1551.
54. Smith WM, Pham TH, Lei L, Dou J, Soomro AH, Beatson SA, Dykes GA, Turner MS. 2012. Heat resistance and salt hypersensitivity in Lactococcus lactis due to spontaneous mutation of llmg_1816 (gdpP) induced by high-temperature growth. Appl. Environ. Microbiol. 78:7753-7759.
55. Chen Y, Chai Y, Guo JH, Losick R. 2012. Evidence for cyclic di-GMPmediated signaling in Bacillus subtilis. J. Bacteriol. 194:5080-5090.
56. Gao X, Mukherjee S, Matthews PM, Hammad LA, Kearns DB, Dann CE, III. 26 July 2013. Functional characterization of core components of the Bacillus subtilis c-di-GMP signaling pathway. J. Bacteriol. doi:10.1128/JB.00373-13.
57. Purcell EB, McKee RW, McBride SM, Waters CM, Tamayo R. 2012. Cyclic diguanylate inversely regulates motility and aggregation in Clostridium difficile. J. Bacteriol. 194:3307-3316.
58. Yan W, Qu T, Zhao H, Su L, Yu Q, Gao J, Wu B. 2010. The effect of c-di-GMP (3'-5'-cyclic diguanylic acid) on the biofilm formation and adherence of Streptococcus mutans. Microbiol. Res. 165:87-96.
59. Zhang J, Biswas I. 2009. 3'-Phosphoadenosine-5'-phosphate phosphatase activity is required for superoxide stress tolerance in Streptococcus mutans. J. Bacteriol. 191:4330-4340.
60. Pozzi C, Waters EM, Rudkin JK, Schaeffer CR, Lohan AJ, Tong P, Loftus BJ, Pier GB, Fey PD, Massey RC, O'Gara JP. 2012. Methicillin resistance alters the biofilm phenotype and attenuates virulence in Staphylococcus aureus device-associated infections. PLoS Pathog. 8:e1002626. doi:10.1371/journal.ppat.1002626.
61. Mechold U, Fang G, Ngo S, Ogryzko V, Danchin A. 2007. YtqI from Bacillus subtilis has both oligoribonuclease and pAp-phosphatase activity. Nucleic Acids Res. 35:4552-4561.
62. El Qaidi S, Yang J, Zhang JR, Metzger DW, Bai G. 2013. The vitamin B6 biosynthesis pathway in Streptococcus pneumoniae is controlled by pyridoxal 5'-phosphate and the transcription factor PdxR and has an impact on ear infection. J. Bacteriol. 195:2187-2196.
63. Avery OT, Macleod CM, McCarty M. 1944. Studies on the chemical nature of the substance inducing transformation of pneumococcal types: induction of transformation by a desoxyribonucleic acid fraction isolated from pneumococcus type III. J. Exp. Med. 79:137-158.
64. Macrina FL, Evans RP, Tobian JA, Hartley DL, Clewell DB, Jones KR. 1983. Novel shuttle plasmid vehicles for Escherichia-Streptococcus transgeneric cloning. Gene 25:145-150.