Pseudomonas aeruginosa expresses a functional human natriuretic peptide receptor ortholog: Involvement in biofilm formation

mBio

Volumn 6, Issue 4, 2015, Pages

  Rosay, Thibaut ^a   Bazire, Alexis ^b   Diaz, Suraya ^c   Clamens, Thomas ^a   Blier, Anne Sophie ^a   Mijouin, Lily ^a   Hoffmann, Brice ^d   Sergent, Jacques Aurélien ^e   Bouffartigues, Emeline ^a   Boireau, Wilfrid ^f   Vieillard, Julien ^g   Hulen, Christian ^a   Dufour, Alain ^b   Harmer, Nicholas J ^c   Feuilloley, Marc G J ^a   Lesouhaitier, Olivier ^a  

^a UNIVERSITÉ DE ROUEN   (France)

^b UNIVERSITÉ DE BRETAGNE SUD   (France)

^c UNIVERSITY OF EXETER   (United Kingdom)

^d UNIVERSITÉ PIERRE ET MARIE CURIE   (France)

^e UNIVERSITÉ DE CERGY PONTOISE   (France)

^f UNIVERSITÉ DE FRANCHE COMTÉ   (France)

^g UNIVERSITÉ DE ROUEN   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AMIC AGONIST; ATRIAL NATRIURETIC FACTOR; ATRIAL NATRIURETIC FACTOR[4-23]; BRAIN NATRIURETIC PEPTIDE; HORMONE RECEPTOR STIMULATING AGENT; ISATIN; NATRIURETIC PEPTIDE RECEPTOR C; UNCLASSIFIED DRUG; AMIC PROTEIN, PSEUDOMONAS AERUGINOSA; ATRIAL NATRIURETIC FACTOR (4-23)NH2, DE-GLN(18)-DE-SER(19)-DE-GLY(20,22)-DE-LEU(21)-; NATRIURETIC PEPTIDE TYPE C; PEPTIDE FRAGMENT; PERIPLASMIC BINDING PROTEIN; RECEPTOR; VIRULENCE FACTOR;

AMI GENE; AMIC GENE; ANIMAL CELL; ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BINDING AFFINITY; BIOFILM; BIOSENSOR; COMPUTER MODEL; CONTROLLED STUDY; CYSTIC FIBROSIS; DRUG CYTOTOXICITY; DRUG PROTEIN BINDING; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOCOMPROMISED PATIENT; MICROSCALE THERMOPHORESIS; NONHUMAN; OPERON; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTION; TEMPERATURE MEASUREMENT; THREE DIMENSIONAL IMAGING; TRANSCRIPTION REGULATION; ANTAGONISTS AND INHIBITORS; CHEMISTRY; COMPUTER SIMULATION; CONFORMATION; DRUG EFFECTS; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; X RAY CRYSTALLOGRAPHY;

ATRIAL NATRIURETIC FACTOR; BIOFILMS; COMPUTER SIMULATION; CRYSTALLOGRAPHY, X-RAY; HUMANS; MOLECULAR CONFORMATION; NATRIURETIC PEPTIDE, BRAIN; NATRIURETIC PEPTIDE, C-TYPE; PEPTIDE FRAGMENTS; PERIPLASMIC BINDING PROTEINS; PSEUDOMONAS AERUGINOSA; RECEPTORS, PEPTIDE; VIRULENCE FACTORS;

EID: 84940863131     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.01033-15     Document Type: Article

References (67)

1. Costerton JW, Stewart PS, Greenberg EP. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284:1318-1322. http://dx.doi.org/10.1126/science.284.5418.1318.
2. Bjarnsholt T, Jensen PØ, Fiandaca MJ, Pedersen J, Hansen CR, Ander- sen CB, Pressler T, Givskov M, Høiby N. 2009. Pseudomonas aeruginosa biofilms in the respiratory tract of cystic fibrosis patients. Pediatr Pulmonol 44:547-558. http://dx.doi.org/10.1002/ppul.21011.
3. Høiby N, Bjarnsholt T, Givskov M, Molin S, Ciofu O. 2010. Antibiotic resistance of bacterial biofilms. Int J Antimicrob Agents 35:322-332. http://dx.doi.org/10.1016/j.ijantimicag.2009.12.011.
4. Ashish A, Shaw M, Winstanley C, Ledson MJ, Walshaw MJ. 2012. IncreasingresistanceoftheLiverpoolepidemicstrain(LES)ofPseudomo- nas aeruginosa (Psa) to antibiotics in cystic fibrosis (CF)—a cause for concern? J Cyst Fibros 11:173-179. http://dx.doi.org/10.1016/j.jcf.2011.11.004.
5. Camilli A, Bassler BL. 2006. Bacterial small-molecule signaling pathways. Science 311:1113-1116. http://dx.doi.org/10.1126/science.1121357.
6. Lesouhaitier O, Veron W, Chapalain A, Madi A, Blier AS, Dagorn A, Connil N, Chevalier S, Orange N, Feuilloley M. 2009. Gram-negative bacterial sensors for eukaryotic signal molecules. Sensors (Basel) 9:6967-6990.
7. Sperandio V, Li CC, Kaper JB. 2002. Quorum-sensing Escherichia coli regulatorA:aregulatoroftheLysRfamilyinvolvedintheregulationofthe locus of enterocyte effacement pathogenicity island in enterohemorrhagic E. coli. Infect Immun 70:3085-3093. http://dx.doi.org/10.1128/IAI.70.6.3085-3093.2002.
8. Sperandio V, Torres AG, Kaper JB. 2002. Quorum sensing Escherichia coli regulators B and C (QseBC): a novel two-component regulatory sys- tem involved in the regulation of flagella and motility by quorum sensing in E. coli. Mol Microbiol 43:809-821. http://dx.doi.org/10.1046/j.1365-2958.2002.02803.x.
9. Hughes DT, Sperandio V. 2008. Inter-kingdom signalling: communication between bacteria and their hosts. Nat Rev Microbiol 6:111-120. http://dx.doi.org/10.1038/nrmicro1836.
10. Sperandio V, Torres AG, Jarvis B, Nataro JP, Kaper JB. 2003. Bacteriahost communication: the language of hormones. Proc Natl Acad Sci U S A 100:8951-8956. http://dx.doi.org/10.1073/pnas.1537100100.
11. Rasko DA, Moreira CG, Li DR, Reading NC, Ritchie JM, Waldor MK, Williams N, Taussig R, Wei S, Roth M, Hughes DT, Huntley JF, Fina MW, Falck JR, Sperandio V. 2008. Targeting QseC signaling and viru- lence for antibiotic development. Science 321:1078-1080. http://dx.doi.org/10.1126/science.1160354.
12. Hegde M, Wood TK, Jayaraman A. 2009. The neuroendocrine hormone norepinephrine increases Pseudomonas aeruginosa PA14 virulence through the las quorum-sensing pathway. Appl Microbiol Biotechnol 84: 763-776. http://dx.doi.org/10.1007/s00253-009-2045-1.
13. Wu L, Estrada O, Zaborina O, Bains M, Shen L, Kohler JE, Patel N, Musch MW, Chang EB, Fu YX, Jacobs MA, Nishimura MI, Hancock RE, Turner JR, Alverdy JC. 2005. Recognition of host immune activation by Pseudomonas aeruginosa. Science 309:774-777. http://dx.doi.org/10.1126/science.1112422.
14. Zaborina O, Lepine F, Xiao G, Valuckaite V, Chen Y, Li T, Ciancio M, Zaborin A, Petrof EO, Turner JR, Rahme LG, Chang E, Alverdy JC. 2007. Dynorphin activates quorum sensing quinolone signaling in Pseu- domonas aeruginosa. PLoS Pathog 3:e35. http://dx.doi.org/10.1371/journal.ppat.0030035.
15. Dagorn A, Chapalain A, Mijouin L, Hillion M, Duclairoir-Poc C, Chevalier S, Taupin L, Orange N, Feuilloley MG. 2013. Effect of GABA, a bacterial metabolite, on Pseudomonas fluorescens surface properties and cytotoxicity. Int J Mol Sci 14:12186-12204. http://dx.doi.org/10.3390/ijms140612186.
16. Blier AS, Veron W, Bazire A, Gerault E, Taupin L, Vieillard J, Rehel K, Dufour A, Le Derf F, Orange N, Hulen C, Feuilloley MG, Lesouhaitier O. 2011. C-type natriuretic peptide modulates quorum sensing molecule and toxin production in Pseudomonas aeruginosa. Microbiology 157: 1929-1944. http://dx.doi.org/10.1099/mic.0.046755-0.
17. Veron W, Lesouhaitier O, Pennanec X, Rehel K, Leroux P, Orange N, Feuilloley MG. 2007. Natriuretic peptides affect Pseudomonas aeruginosa and specifically modify lipopolysaccharide biosynthesis. FEBS J 274: 5852-5864. http://dx.doi.org/10.1111/j.1742-4658.2007.06109.x.
18. Drewett JG, Garbers DL. 1994. The family of guanylyl cyclase receptors and their ligands. Endocr Rev 15:135-162. http://dx.doi.org/10.1210/edrv-15-2-135.
19. Nakanishi K, Tajima F, Itoh H, Nakata Y, Hama N, Nakagawa O, Nakao K, Kawai T, Torikata C, Suga T, Takishima K, Aurues T, Ikeda T. 1999. Expression of C-type natriuretic peptide during development of rat lung. Am J Physiol 277:L996-L1002.
20. Nowak A, Breidthardt T, Christ-Crain M, Bingisser R, Meune C, Tanglay Y, Heinisch C, Reiter M, Drexler B, Arenja N, Twerenbold R, Stolz D, Tamm M, Müller B, Müller C. 2012. Direct comparison of three natriuretic peptides for prediction of short- and long-term mortality in patients with community-acquired pneumonia. Chest 141:974-982. http://dx.doi.org/10.1378/chest.11-0824.
21. Vila G, Resl M, Stelzeneder D, Struck J, Maier C, Riedl M, Hülsmann M, Pacher R, Luger A, Clodi M. 2008. Plasma NT-proBNP increases in response to LPS administration in healthy men. J Appl Physiol 105: 1741-1745. http://dx.doi.org/10.1152/japplphysiol.90442.2008.
22. Suga S, Itoh H, Komatsu Y, Ogawa Y, Hama N, Yoshimasa T, Nakao K. 1993. Cytokine-induced C-type natriuretic peptide (CNP) secretion from vascular endothelial cells—evidence for CNP as a novel autocrine/ paracrine regulator from endothelial cells. Endocrinology 133: 3038-3041. http://dx.doi.org/10.1210/endo.133.6.8243333.
23. Coggan KA, Wolfgang MC. 2012. Global regulatory pathways and cross-talk control Pseudomonas aeruginosa environmental lifestyle and viru- lence phenotype. Curr Issues Mol Biol 14:47-70.
24. Klinger JR, Tsai SW, Green S, Grinnell KL, Machan JT, Harrington EO. 2013. Atrial natriuretic peptide attenuates agonist-induced pulmonary edema in mice with targeted disruption of the gene for natriuretic peptide receptor-A. J Appl Physiol 114:307-315. http://dx.doi.org/10.1152/japplphysiol.01249.2011.
25. Potter LR, Abbey-Hosch S, Dickey DM. 2006. Natriuretic peptides, their receptors, and cyclic guanosine monophosphate-dependent signaling functions. Endocr Rev 27:47-72.
26. Holm L, Sander C. 1995. Dali: a network tool for protein structure comparison. Trends Biochem Sci 20:478-480. http://dx.doi.org/10.1016/ S0968-0004(00)89105-7.
27. van den Akker F. 2001. Structural insights into the ligand binding domains of membrane bound guanylyl cyclases and natriuretic peptide re- ceptors. J Mol Biol 311:923-937. http://dx.doi.org/10.1006/jmbi.2001.4922.
28. van den Akker F, Zhang X, Miyagi M, Huo X, Misono KS, Yee VC. 2000. Structure of the dimerized hormone-binding domain of a guanylyl- cyclase-coupled receptor. Nature 406:101-104. http://dx.doi.org/10.1038/35017602.
29. Pearl L, O’Hara B, Drew R, Wilson S. 1994. Crystal structure of AmiC: the controller of transcription antitermination in the amidase operon of Pseudomonas aeruginosa. EMBO J 13:5810-5817.
30. He X, Chow D, Martick MM, Garcia KC. 2001. Allosteric activation of a spring-loaded natriuretic peptide receptor dimer by hormone. Science 293:1657-1662. http://dx.doi.org/10.1126/science.1062246.
31. Russell RB, Barton GJ. 1992. Multiple protein sequence alignment from tertiary structure comparison: assignment of global and residue confidence levels. Proteins 14:309-323. http://dx.doi.org/10.1002/prot.340140216.
32. Standley DM, Toh H, Nakamura H. 2005. GASH: an improved algorithm for maximizing the number of equivalent residues between two protein structures. BMC Bioinformatics 6:221. http://dx.doi.org/10.1186/ 1471-2105-6-221.
33. He XL, Dukkipati A, Garcia KC. 2006. Structural determinants of natriuretic peptide receptor specificity and degeneracy. J Mol Biol 361: 698-714. http://dx.doi.org/10.1016/j.jmb.2006.06.060.
34. Morris GM, Goodsell DS, Halliday RS, Huey R, Hart WE, Belew RK, Olson AJ. 1998. Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function. J Comput Chem 19:1639-1662. http://dx.doi.org/10.1002/(SICI)1096-987X(19981115)19:141639::AID-JCC103.0.CO;2-B.
35. Wilson S, Drew R. 1991. Cloning and DNA sequence of amiC, a new gene regulating expression of the Pseudomonas aeruginosa aliphatic amidase, and purification of the amiC product. J Bacteriol 173:4914-4921.
36. Wilson SA, Wachira SJ, Drew RE, Jones D, Pearl LH. 1993. An titermination of amidase expression in Pseudomonas aeruginosa is controlled by a novel cytoplasmic amide-binding protein. EMBO J 12:3637-3642.
37. Balasubramanian D, Schneper L, Kumari H, Mathee K. 2013. A dynamic and intricate regulatory network determines Pseudomonas aeruginosa virulence. Nucleic Acids Res 41:1-20. http://dx.doi.org/10.1093/nar/gks1039.
38. Ono K, Oka R, Toyofuku M, Sakaguchi A, Hamada M, Yoshida S, Nomura N. 2014. cAMP signaling affects irreversible attachment during biofilm formation by Pseudomonas aeruginosa PAO1. Microbes Environ 29:104-106. http://dx.doi.org/10.1264/jsme2.ME13151.
39. Goldberg JB, Coyne MJ, Jr., Neely AN, Holder IA. 1995. Avirulence of a Pseudomonas aeruginosa algC mutant in a burned-mouse model of infection. Infect Immun 63:4166-4169.
40. Anand-Srivastava MB, Sehl PD, Lowe DG. 1996. Cytoplasmic domain of natriuretic peptide receptor-C inhibits adenylyl cyclase. Involvement of a pertussis toxin-sensitive G protein. J Biol Chem 271:19324-19329. http://dx.doi.org/10.1074/jbc.271.32.19324.
41. O’Hara BP, Norman RA, Wan PT, Roe SM, Barrett TE, Drew RE, Pearl LH. 1999. Crystal structure and induction mechanism of AmiC-AmiR: a ligand-regulated transcription antitermination complex. EMBO J 18: 5175-5186. http://dx.doi.org/10.1093/emboj/18.19.5175.
42. Yamashita K, Kaneko H, Yamamoto S, Konagaya T, Kusugami K, Mitsuma T. 1998. Inhibitory effect of somatostatin on Helicobacter pylori proliferationinvitro. Gastroenterology 115:1123-1130. http://dx.doi.org/10.1016/S0016-5085(98)70083-6.
43. Marinova Z, Vukojevic V, Surcheva S, Yakovleva T, Cebers G, Pasikova N, Usynin I, Hugonin L, Fang W, Hallberg M, Hirschberg D, Bergman T, Langel U, Hauser KF, Pramanik A, Aldrich JV, Gräslund A, Terenius L, Bakalkin G. 2005. Translocation of dynorphin neuropeptides across the plasma membrane. A putative mechanism of signal transmission. J Biol Chem 280:26360-26370. http://dx.doi.org/10.1074/jbc.M412494200.
44. Kourie JI. 1999. Synthetic mammalian C-type natriuretic peptide forms large cation channels. FEBS Lett 445:57-62. http://dx.doi.org/10.1016/S0014-5793(99)00081-2.
45. Dallo SF, Kannan TR, Blaylock MW, Baseman JB. 2002. Elongation factor Tu and E1 beta subunit of pyruvate dehydrogenase complex act as fibronectin binding proteins in Mycoplasma pneumoniae. Mol Microbiol 46:1041-1051. http://dx.doi.org/10.1046/j.1365-2958.2002.03207.x.
46. Kunert A, Losse J, Gruszin C, Hühn M, Kaendler K, Mikkat S, Volke D, Hoffmann R, Jokiranta TS, Seeberger H, Moellmann U, Hellwage J, Zipfel PF. 2007. Immune evasion of the human pathogen Pseudomonas aeruginosa: elongation factor Tuf is a factor H and plasminogen binding protein. J Immunol 179:2979 -2988. http://dx.doi.org/10.4049/jimmunol.179.5.2979.
47. Xie W, Dickson C, Kwiatkowski W, Choe S. 2010. Structure of the cytoplasmic segment of histidine kinase receptor QseC, a key player in bacterial virulence. Protein Pept Lett 17:1383-1391. http://dx.doi.org/10.2174/0929866511009011383.
48. Sugawara E, Nestorovich EM, Bezrukov SM, Nikaido H. 2006. Pseudomonas aeruginosa porin OprF exists in two different conformations. J Biol Chem 281:16220-16229. http://dx.doi.org/10.1074/jbc.M600680200.
49. Medvedev A, Crumeyrolle-Arias M, Cardona A, Sandler M, Glover V. 2005. Natriuretic peptide interaction with [3H]isatin binding sites in rat brain. Brain Res 1042:119-124. http://dx.doi.org/10.1016/j.brainres.2005.02.051.
50. Moffatt P, Thomas G, Sellin K, Bessette MC, Lafrenière F, Akhouayri O, St-Arnaud R, Lanctôt C. 2007. Osteocrin is a specific ligand of the natriuretic peptide clearance receptor that modulates bone growth. J Biol Chem 282:36454-36462. http://dx.doi.org/10.1074/jbc.M708596200.
51. Olson LJ, Lowe DG, Drewett JG. 1996. Novel natriuretic peptide receptor/guanylyl cyclase A-selective agonist inhibits angiotensin II- and forskolin-evoked aldosterone synthesis in a human zona glomerulosa cell line. Mol Pharmacol 50:430-435.
52. Mawatari K, Segawa M, Masatsuka R, Hanawa Y, Iinuma F, Watanabe M. 2001. Fluorimetric determination of isatin in human urine and serum by liquid chromatography postcolumn photoirradiation. Analyst 126: 33-36. http://dx.doi.org/10.1039/b006484j.
53. Lee J, Jayaraman A, Wood TK. 2007. Indole is an inter-species biofilm signal mediated by SdiA. BMC Microbiol 7:42. http://dx.doi.org/10.1186/1471-2180-7-42.
54. Lee J, Bansal T, Jayaraman A, Bentley WE, Wood TK. 2007. Enterohe-morrhagic Escherichia coli biofilms are inhibited by 7-hydroxyindole and stimulated by isatin. Appl Environ Microbiol 73:4100-4109. http://dx.doi.org/10.1128/AEM.00360-07.
55. Zou P, Koh HL. 2007. Determination of indican, isatin, indirubin and indigotin in Isatis indigotica by liquid chromatography/electrospray ionization tandem mass spectrometry. Rapid Commun Mass Spectrom 21: 1239-1246. http://dx.doi.org/10.1002/rcm.2954.
56. Watkins P, Clow A, Glover V, Halket J, Przyborowska A, Sandler M. 1990. Isatin, regional distribution in rat brain and tissues. Neurochem Int 17:321-323. http://dx.doi.org/10.1016/0197-0186(90)90154-L.
57. Medvedev A, Buneeva O, Glover V. 2007. Biological targets for isatin and its analogues: implications for therapy. Biologics Targets Ther 1:151-162.
58. Edelson JD, Makhlina M, Silvester KR, Vengurlekar SS, Chen X, Zhang J, Koziol-White CJ, Cooper PR, Hallam TJ, Hay DW, Panettieri RA, Jr. 2013. In vitro and in vivo pharmacological profile of PL-3994, a novel cyclic peptide (hept-cyclo(Cys-His-Phe-D-Ala-Gly-Arg-D-Nle-Asp-Arg- Ile-Ser-Cys)-Tyr-[Arg mimetic]-NH(2)) natriuretic peptide receptor-A agonist that is resistant to neutral endopeptidase and acts as a bronchodilator. Pulm Pharmacol Ther 26:229-238. http://dx.doi.org/10.1016/j.pupt.2012.11.001.
59. Jacobs MA, Alwood A, Thaipisuttikul I, Spencer D, Haugen E, Ernst S, Will O, Kaul R, Raymond C, Levy R, Chun-Rong L, Guenthner D, Bovee D, Olson MV, Manoil C. 2003. Comprehensive transposon mu- tant library of Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 100: 14339-14344. http://dx.doi.org/10.1073/pnas.2036282100.
60. Liberati NT, Urbach JM, Miyata S, Lee DG, Drenkard E, Wu G, Villanueva J, Wei T, Ausubel FM. 2006. An ordered, nonredundant library of Pseudomonas aeruginosa strain pa14 transposon insertion mutants. ProcNatlAcadSciUSA 103:2833-2838.
61. http://dx.doi.org/10.1073/pnas.0511100103.
62. Bazire A, Shioya K, Soum-Soutéra E, Bouffartigues E, Ryder C, Guentas-Dombrowsky L, Hémery G, Linossier I, Chevalier S, Wozniak DJ, Lesouhaitier O, Dufour A. 2010. The sigma factor AlgU plays a key role in formation of robust biofilms by nonmucoid Pseudomonas aeruginosa. J Bacteriol 192:3001-3010. http://dx.doi.org/10.1128/JB.01633-09.
63. Heydorn A, Nielsen AT, Hentzer M, Sternberg C, Givskov M, Ersbøll BK, Molin S. 2000. Quantification of biofilm structures by the novel computer program COMSTAT. Microbiology 146:2395-2407.
64. Humphrey W, Dalke A, Schulten K. 1996. VMD: visual molecular dynamics. J Mol Graph 14:33-38. http://dx.doi.org/10.1016/0263-7855(96)00018-5.
65. Bazire A, Diab F, Taupin L, Rodrigues S, Jebbar M, Dufour A. 2009. Effects of osmotic stress on rhamnolipid synthesis and time-course production of cell-to-cell signal molecules by Pseudomonas aeruginosa. Open Microbiol J 3:128-135. http://dx.doi.org/10.2174/1874285800903010128.
66. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(- CT) method. Methods 25:402-408. http://dx.doi.org/10.1006/meth.2001.1262.
67. Studier FW. 2005. Protein production by auto-induction in high density shaking cultures. Protein Expr Purif 41:207-234. http://dx.doi.org/10.1016/j.pep.2005.01.016.