Nitric Oxide Regulation of Bacterial Biofilms

Biochemistry

Volumn 54, Issue 24, 2015, Pages 3717-3728

  Arora, Dhruv P ^a   Hossain, Sajjad ^a   Xu, Yueming ^a   Boon, Elizabeth M ^a  

^a STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NITRIC OXIDE;

BACTERIAL BIOFILM; BIOFILM FORMATION; BROAD SPECTRUM; MULTICELLULAR COMMUNITIES; NATURAL SOURCES; NO CONCENTRATION; SIGNALING MOLECULES; SIGNALING PATHWAYS;

BIOFILMS;

NITRIC OXIDE; PRODRUG; BACTERIAL PROTEIN; HEMOPROTEIN;

BACTERIAL BIOFILM; BACTERIUM; BIOFILM; NONHUMAN; PRIORITY JOURNAL; REVIEW; SENSOR; BIOLOGICAL MODEL; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGY; SECOND MESSENGER;

BACTERIA (MICROORGANISMS);

BACTERIAL PROTEINS; BIOFILMS; GRAM-NEGATIVE BACTERIA; GRAM-POSITIVE BACTERIA; HEMEPROTEINS; MODELS, BIOLOGICAL; NITRIC OXIDE; SECOND MESSENGER SYSTEMS;

EID: 84934892301     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi501476n     Document Type: Review

References (138)

1. Ignarro, L. J., Byrns, R. E., Buga, G. M., and Wood, K. S. (1987) Endothelium-derived relaxing factor from pulmonary artery and vein possesses pharmacologic and chemical properties identical to those of nitric oxide radical Circ. Res. 61, 866-879
2. Ignarro, L. J. (1991) Signal transduction mechanisms involving nitric oxide Biochem. Pharmacol. 41, 485-490
3. Cary, S. P., Winger, J. A., Derbyshire, E. R., and Marletta, M. A. (2006) Nitric oxide signaling: No longer simply on or off Trends Biochem. Sci. 31, 231-239
4. Denninger, J. W. and Marletta, M. A. (1999) Guanylate cyclase and the NO/cGMP signaling pathway Biochim. Biophys. Acta 1411, 334-350
5. Bian, K., Doursout, M. F., and Murad, F. (2008) Vascular system: Role of nitric oxide in cardiovascular diseases J. Clin. Hypertens. (Hoboken, NJ, U.S.) 10, 304-310
6. Culotta E.,Koshland D.E. Jr. (1992) NO news is good news Science 258, 1862-1865
7. Alderton, W. K., Cooper, C. E., and Knowles, R. G. (2001) Nitric oxide synthases: Structure, function and inhibition Biochem. J. 357, 593-615
8. Daff, S. (2010) NO synthase: Structures and mechanisms Nitric Oxide 23, 1-11
9. Stuehr, D. J., Santolini, J., Wang, Z. Q., Wei, C. C., and Adak, S. (2004) Update on mechanism and catalytic regulation in the NO synthases J. Biol. Chem. 279, 36167-36170
10. Derbyshire, E. R. and Marletta, M. A. (2012) Structure and regulation of soluble guanylate cyclase Annu. Rev. Biochem. 81, 533-559
11. Murad, F. (1994) Regulation of cytosolic guanylyl cyclase by nitric oxide: The NO-cyclic GMP signal transduction system Adv. Pharmacol. 26, 19-33
12. MacMicking, J., Xie, Q. W., and Nathan, C. (1997) Nitric oxide and macrophage function Annu. Rev. Immunol. 15, 323-350
13. Bogdan, C. (2001) Nitric oxide and the immune response Nat. Immunol. 2, 907-916
14. Cruz-Ramos, H., Crack, J., Wu, G., Hughes, M. N., Scott, C., Thomson, A. J., Green, J., and Poole, R. K. (2002) NO sensing by FNR: Regulation of the Escherichia coli NO-detoxifying flavohaemoglobin, Hmp EMBO J. 21, 3235-3244
15. D'Autreaux, B., Tucker, N. P., Dixon, R., and Spiro, S. (2005) A non-haem iron centre in the transcription factor NorR senses nitric oxide Nature 437, 769-772
16. Bodenmiller, D. M. and Spiro, S. (2006) The yjeB (nsrR) gene of Escherichia coli encodes a nitric oxide-sensitive transcriptional regulator J. Bacteriol. 188, 874-881
17. Frey, A. D. and Kallio, P. T. (2003) Bacterial hemoglobins and flavohemoglobins: Versatile proteins and their impact on microbiology and biotechnology FEMS Microbiol. Rev. 27, 525-545
18. Tucker, N. P., Le Brun, N. E., Dixon, R., and Hutchings, M. I. (2010) There's NO stopping NsrR, a global regulator of the bacterial NO stress response Trends Microbiol. 18, 149-156
19. Saraiva, L. M., Vicente, J. B., and Teixeira, M. (2004) The role of the flavodiiron proteins in microbial nitric oxide detoxification Adv. Microb. Physiol. 49, 77-129
20. Ascenzi, P. and Visca, P. (2008) Scavenging of reactive nitrogen species by mycobacterial truncated hemoglobins Methods Enzymol. 436, 317-337
21. Field, S. J., Thorndycroft, F. H., Matorin, A. D., Richardson, D. J., and Watmough, N. J. (2008) The respiratory nitric oxide reductase (NorBC) from Paracoccus denitrificans Methods Enzymol. 437, 79-101
22. Poole, R. K. (2005) Nitric oxide and nitrosative stress tolerance in bacteria Biochem. Soc. Trans. 33, 176-180
23. Spiro, S. (2007) Regulators of bacterial responses to nitric oxide FEMS Microbiol. Rev. 31, 193-211
24. Spiro, S. and D'Autreaux, B. (2012) Non-heme iron sensors of reactive oxygen and nitrogen species Antioxid. Redox Signaling 17, 1264-1276
25. Barraud, N., Hassett, D. J., Hwang, S. H., Rice, S. A., Kjelleberg, S., and Webb, J. S. (2006) Involvement of nitric oxide in biofilm dispersal of Pseudomonas aeruginosa J. Bacteriol. 188, 7344-7353
26. Davidson, S., Koropatnick, T., Kossmehl, R., Sycuro, L., and McFall-Ngai, M. (2004) NO means 'yes' in the squid-vibrio symbiosis: Nitric oxide (NO) during the initial stages of a beneficial association Cell. Microbiol. 6, 1139-1151
27. Henares, B. M., Higgins, K. E., and Boon, E. M. (2012) Discovery of a Nitric Oxide Responsive Quorum Sensing Circuit in Vibrio harveyi ACS Chem. Biol. 7, 1331-1336
28. Liu, N., Xu, Y., Hossain, S., Huang, N., Coursolle, D., Gralnick, J. A., and Boon, E. M. (2012) Nitric oxide regulation of cyclic di-GMP synthesis and hydrolysis in Shewanella woodyi Biochemistry 51, 2087-2099
29. Plate, L. and Marletta, M. A. (2012) Nitric Oxide Modulates Bacterial Biofilm Formation through a Multicomponent Cyclic-di-GMP Signaling Network Mol. Cell 46, 449-460
30. Schmidt, I., Steenbakkers, P. J., op den Camp, H. J., Schmidt, K., and Jetten, M. S. (2004) Physiologic and proteomic evidence for a role of nitric oxide in biofilm formation by Nitrosomonas europaea and other ammonia oxidizers J. Bacteriol. 186, 2781-2788
31. Barraud, N., Storey, M. V., Moore, Z. P., Webb, J. S., Rice, S. A., and Kjelleberg, S. (2009) Nitric oxide-mediated dispersal in single- and multi-species biofilms of clinically and industrially relevant microorganisms Microb. Biotechnol. 2, 370-378
32. Partridge, J. D., Bodenmiller, D. M., Humphrys, M. S., and Spiro, S. (2009) NsrR targets in the Escherichia coli genome: New insights into DNA sequence requirements for binding and a role for NsrR in the regulation of motility Mol. Microbiol. 73, 680-694
33. Connelly, L., Palacios-Callender, M., Ameixa, C., Moncada, S., and Hobbs, A. J. (2001) Biphasic regulation of NF-κB activity underlies the pro- and anti-inflammatory actions of nitric oxide J. Immunol. 166, 3873-3881
34. Pacher, P., Beckman, J. S., and Liaudet, L. (2007) Nitric oxide and peroxynitrite in health and disease Physiol. Rev. 87, 315-424
35. Crane, B. R., Sudhamsu, J., and Patel, B. A. (2010) Bacterial nitric oxide synthases Annu. Rev. Biochem. 79, 445-470
36. Iyer, L. M., Anantharaman, V., and Aravind, L. (2003) Ancient conserved domains shared by animal soluble guanylyl cyclases and bacterial signaling proteins BMC Genomics 4, 5-12
37. Barraud, N., Kelso, M. J., Rice, S. A., and Kjelleberg, S. (2015) Nitric oxide: A key mediator of biofilm dispersal with applications in infectious diseases Curr. Pharm. Des. 21, 31-42
38. McDougald, D., Rice, S. A., Barraud, N., Steinberg, P. D., and Kjelleberg, S. (2012) Should we stay or should we go: Mechanisms and ecological consequences for biofilm dispersal Nat. Rev. Microbiol. 10, 39-50
39. Davey, M. E. and O'Toole, G. (2000) Microbial biofilms: From ecology to molecular genetics Microbiol. Mol. Biol. Rev. 64, 847-867
40. Hall-Stoodley, L., Costerton, J. W., and Stoodley, P. (2004) Bacterial biofilms: From the natural environment to infectious diseases Nat. Rev. Microbiol. 2, 95-108
41. Stoodley, P., Sauer, K., Davies, D. G., and Costerton, J. W. (2002) Biofilms as complex differentiated communities Annu. Rev. Microbiol. 56, 187-209
42. Webb, J. S., Givskov, M., and Kjelleberg, S. (2003) Bacterial biofilms: Prokaryotic adventures in multicellularity Curr. Opin. Microbiol. 6, 578-585
43. O'Toole, G., Kaplan, H. B., and Kolter, R. (2000) Biofilm formation as microbial development Annu. Rev. Microbiol. 54, 49-79
44. Flemming, H. C. and Wingender, J. (2010) The biofilm matrix Nat. Rev. Microbiol. 8, 623-633
45. Costerton, J. W., Stewart, P. S., and Greenberg, E. P. (1999) Bacterial biofilms: A common cause of persistent infections Science 284, 1318-1322
46. Donlan, R. M. and Costerton, J. W. (2002) Biofilms: Survival mechanisms of clinically relevant microorganisms Clin. Microbiol. Rev. 15, 167-193
47. Fux, C. A., Costerton, J. W., Stewart, P. S., and Stoodley, P. (2005) Survival strategies of infectious biofilms Trends Microbiol. 13, 34-40
48. Van Wey, A. S., Cookson, A. L., Roy, N. C., McNabb, W. C., Soboleva, T. K., and Shorten, P. R. (2011) Bacterial biofilms associated with food particles in the human large bowel Mol. Nutr. Food Res. 55, 969-978
49. Swidsinski, A., Weber, J., Loening-Baucke, V., Hale, L. P., and Lochs, H. (2005) Spatial organization and composition of the mucosal flora in patients with inflammatory bowel disease J. Clin. Microbiol. 43, 3380-3389
50. Stewart, P. S. and Costerton, J. W. (2001) Antibiotic resistance of bacteria in biofilms Lancet 358, 135-138
51. Hoiby, N., Bjarnsholt, T., Givskov, M., Molin, S., and Ciofu, O. (2010) Antibiotic resistance of bacterial biofilms Int. J. Antimicrob. Agents 35, 322-332
52. Romero, D. and Kolter, R. (2011) Will biofilm disassembly agents make it to market? Trends Microbiol. 19, 304-306
53. Laub, M. T. and Goulian, M. (2007) Specificity in two-component signal transduction pathways Annu. Rev. Genet. 41, 121-145
54. Stock, A. M., Robinson, V. L., and Goudreau, P. N. (2000) Two-component signal transduction Annu. Rev. Biochem. 69, 183-215
55. Mascher, T., Helmann, J. D., and Unden, G. (2006) Stimulus perception in bacterial signal-transducing histidine kinases Microbiol. Mol. Biol. Rev. 70, 910-938
56. Cock, P. J. and Whitworth, D. E. (2007) Evolution of prokaryotic two-component system signaling pathways: Gene fusions and fissions Mol. Biol. Evol. 24, 2355-2357
57. Rodrigue, A., Quentin, Y., Lazdunski, A., Mejean, V., and Foglino, M. (2000) Two-component systems in Pseudomonas aeruginosa: Why so many? Trends Microbiol. 8, 498-504
58. Fuqua, C., Parsek, M. R., and Greenberg, E. P. (2001) Regulation of gene expression by cell-to-cell communication: Acyl-homoserine lactone quorum sensing Annu. Rev. Genet. 35, 439-468
59. Miller, M. B. and Bassler, B. L. (2001) Quorum sensing in bacteria Annu. Rev. Microbiol. 55, 165-199
60. Ng, W. L. and Bassler, B. L. (2009) Bacterial quorum-sensing network architectures Annu. Rev. Genet. 43, 197-222
61. Hengge, R. (2009) Principles of c-di-GMP signalling in bacteria Nat. Rev. Microbiol. 7, 263-273
62. Jenal, U. and Malone, J. (2006) Mechanisms of cyclic-di-GMP signaling in bacteria Annu. Rev. Genet. 40, 385-407
63. Romling, U., Gomelsky, M., and Galperin, M. Y. (2005) C-di-GMP: The dawning of a novel bacterial signalling system Mol. Microbiol. 57, 629-639
64. Romling, U., Galperin, M. Y., and Gomelsky, M. (2013) Cyclic di-GMP: The first 25 years of a universal bacterial second messenger Microbiol. Mol. Biol. Rev. 77, 1-52
65. Ryjenkov, D. A., Tarutina, M., Moskvin, O. V., and 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
66. Dow, J. M., Fouhy, Y., Lucey, J. F., and Ryan, R. P. (2006) The HD-GYP domain, cyclic di-GMP signaling, and bacterial virulence to plants Mol. Plant-Microbe Interact. 19, 1378-1384
67. Schmidt, A. J., Ryjenkov, D. A., and Gomelsky, M. (2005) The ubiquitous protein domain EAL is a cyclic diguanylate-specific phosphodiesterase: Enzymatically active and inactive EAL domains J. Bacteriol. 187, 4774-4781
68. Yoon, S., Hennigan, R., Hilliard, G., Ochsner, U., Parvatiyar, K., Kamani, M., Allen, H., DeKievit, T., Gardner, P., Schwab, U., Rowe, J., Iglewski, B., McDermott, T., Mason, R., Wozniak, D., Hancock, R., Parsek, M., Noah, T., Boucher, R., and Hassett, D. (2002) Pseudomonas aeruginosa anaerobic respiration in biofilms: Relationship to cystic fibrosis pathogenesis Dev. Cell 3, 593-603
69. Davies, D. G., Parsek, M. R., Pearson, J. P., Iglewski, B. H., Costerton, J. W., and Greenberg, E. P. (1998) The involvement of cell-to-cell signals in the development of a bacterial biofilm Science 280, 295-298
70. Whitehead, N. A., Barnard, A. M., Slater, H., Simpson, N. J., and Salmond, G. P. (2001) Quorum-sensing in Gram-negative bacteria FEMS Microbiol. Rev. 25, 365-404
71. Antunes, L. C., Ferreira, R. B., Buckner, M. M., and Finlay, B. B. (2010) Quorum sensing in bacterial virulence Microbiology 156, 2271-2282
72. Galloway, W. R., Hodgkinson, J. T., Bowden, S. D., Welch, M., and Spring, D. R. (2011) Quorum sensing in Gram-negative bacteria: Small-molecule modulation of AHL and AI-2 quorum sensing pathways Chem. Rev. 111, 28-67
73. Schreiber, K., Krieger, R., Benkert, B., Eschbach, M., Arai, H., Schobert, M., and Jahn, D. (2007) The anaerobic regulatory network required for Pseudomonas aeruginosa nitrate respiration J. Bacteriol. 189, 4310-4314
74. Trunk, K., Benkert, B., Quack, N., Munch, R., Scheer, M., Garbe, J., Jansch, L., Trost, M., Wehland, J., Buer, J., Jahn, M., Schobert, M., and Jahn, D. (2010) Anaerobic adaptation in Pseudomonas aeruginosa: Definition of the Anr and Dnr regulons Environ. Microbiol. 12, 1719-1733
75. Giardina, G., Rinaldo, S., Johnson, K. A., Di Matteo, A., Brunori, M., and Cutruzzola, F. (2008) NO sensing in Pseudomonas aeruginosa: Structure of the transcriptional regulator DNR J. Mol. Biol. 378, 1002-1015
76. Barraud, N., Schleheck, D., Klebensberger, J., Webb, J. S., Hassett, D. J., Rice, S. A., and Kjelleberg, S. (2009) Nitric oxide signaling in Pseudomonas aeruginosa biofilms mediates phosphodiesterase activity, decreased cyclic diguanosine-5′-monophosphate levels and enhanced dispersal J. Bacteriol. 00975-00909
77. Morgan, R., Kohn, S., Hwang, S. H., Hassett, D. J., and Sauer, K. (2006) BdlA, a chemotaxis regulator essential for biofilm dispersion in Pseudomonas aeruginosa J. Bacteriol. 188, 7335-7343
78. Petrova, O. E. and Sauer, K. (2012) PAS domain residues and prosthetic group involved in BdlA-dependent dispersion response by Pseudomonas aeruginosa biofilms J. Bacteriol. 194, 5817-5828
79. Petrova, O. E., Cherny, K. E., and Sauer, K. (2015) The diguanylate cyclase GcbA facilitates Pseudomonas aeruginosa biofilm dispersion by activating BdlA J. Bacteriol. 197, 174-187
80. Roy, A. B., Petrova, O. E., and Sauer, K. (2012) The phosphodiesterase DipA (PA5017) is essential for Pseudomonas aeruginosa biofilm dispersion J. Bacteriol. 194, 2904-2915
81. Li, Y., Heine, S., Entian, M., Sauer, K., and Frankenberg-Dinkel, N. (2013) NO-induced biofilm dispersion in Pseudomonas aeruginosa is mediated by an MHYT domain-coupled phosphodiesterase J. Bacteriol. 195, 3531-3542
82. Galperin, M. Y., Nikolskaya, A. N., and Koonin, E. V. (2001) Novel domains of the prokaryotic two-component signal transduction systems FEMS Microbiol. Lett. 203, 11-21
83. Householder, T. C., Fozo, E. M., Cardinale, J. A., and Clark, V. L. (2000) Gonococcal nitric oxide reductase is encoded by a single gene, norB, which is required for anaerobic growth and is induced by nitric oxide Infect. Immun. 68, 5241-5246
84. Householder, T. C., Belli, W. A., Lissenden, S., Cole, J. A., and Clark, V. L. (1999) cis- and trans-acting elements involved in regulation of aniA, the gene encoding the major anaerobically induced outer membrane protein in Neisseria gonorrhoeae J. Bacteriol. 181, 541-551
85. Isabella, V. M., Lapek, J. D., Jr., Kennedy, E. M., and Clark, V. L. (2009) Functional analysis of NsrR, a nitric oxide-sensing Rrf2 repressor in Neisseria gonorrhoeae Mol. Microbiol. 71, 227-239
86. Falsetta, M. L., Bair, T. B., Ku, S. C., Vanden Hoven, R. N., Steichen, C. T., McEwan, A. G., Jennings, M. P., and Apicella, M. A. (2009) Transcriptional profiling identifies the metabolic phenotype of gonococcal biofilms Infect. Immun. 77, 3522-3532
87. Falsetta, M. L., McEwan, A. G., Jennings, M. P., and Apicella, M. A. (2010) Anaerobic metabolism occurs in the substratum of gonococcal biofilms and may be sustained in part by nitric oxide Infect. Immun. 78, 2320-2328
88. Jardeleza, C., Foreman, A., Baker, L., Paramasivan, S., Field, J., Tan, L. W., and Wormald, P. J. (2011) The effects of nitric oxide on Staphylococcus aureus biofilm growth and its implications in chronic rhinosinusitis International Forum of Allergy & Rhinology 1, 438-444
89. Sheffler, L. A., Wink, D. A., Melillo, G., and Cox, G. W. (1995) Characterization of nitric oxide-stimulated ADP-ribosylation of various proteins from the mouse macrophage cell line ANA-1 using sodium nitroprusside and the novel nitric oxide-donating compound diethylamine dinitric oxide J. Leukocyte Biol. 57, 152-159
90. Lundberg, J. O., Farkas-Szallasi, T., Weitzberg, E., Rinder, J., Lidholm, J., Anggaard, A., Hokfelt, T., Lundberg, J. M., and Alving, K. (1995) High nitric oxide production in human paranasal sinuses Nat. Med. 1, 370-373
91. Deja, M., Busch, T., Bachmann, S., Riskowski, K., Campean, V., Wiedmann, B., Schwabe, M., Hell, B., Pfeilschifter, J., Falke, K. J., and Lewandowski, K. (2003) Reduced nitric oxide in sinus epithelium of patients with radiologic maxillary sinusitis and sepsis Am. J. Respir. Crit. Care Med. 168, 281-286
92. Arora, D. P. and Boon, E. M. (2012) Nitric oxide regulated two-component signaling in Pseudoalteromonas atlantica Biochem. Biophys. Res. Commun. 421, 521-526
93. Boon, E. M., Davis, J. H., Tran, R., Karow, D. S., Huang, S. H., Pan, D., Miazgowicz, M. M., Mathies, R. A., and Marletta, M. A. (2006) Nitric oxide binding to prokaryotic homologs of the soluble guanylate cyclase β1 H-NOX domain J. Biol. Chem. 281, 21892-21902
94. Boon, E. M., Huang, S. H., and Marletta, M. A. (2005) A molecular basis for NO selectivity in soluble guanylate cyclase Nat. Chem. Biol. 1, 53-59
95. Boon, E. M. and Marletta, M. A. (2005) Ligand discrimination in soluble guanylate cyclase and the H-NOX family of heme sensor proteins Curr. Opin. Chem. Biol. 9, 441-446
96. Boon, E. M. and Marletta, M. A. (2005) Ligand specificity of H-NOX domains: From sGC to bacterial NO sensors J. Inorg. Biochem. 99, 892-902
97. Carlson, H. K., Vance, R. E., and Marletta, M. A. (2010) H-NOX regulation of c-di-GMP metabolism and biofilm formation in Legionella pneumophila Mol. Microbiol. DOI: 10.1111/j.1365-2958.2010.07259.x
98. Karow, D. S., Pan, D., Tran, R., Pellicena, P., Presley, A., Mathies, R. A., and Marletta, M. A. (2004) Spectroscopic characterization of the soluble guanylate cyclase-like heme domains from Vibrio cholerae and Thermoanaerobacter tengcongensis Biochemistry 43, 10203-10211
99. Ma, X., Sayed, N., Beuve, A., and van den Akker, F. (2007) NO and CO differentially activate soluble guanylyl cyclase via a heme pivot-bend mechanism EMBO J. 26, 578-588
100. Pellicena, P., Karow, D. S., Boon, E. M., Marletta, M. A., and Kuriyan, J. (2004) Crystal structure of an oxygen-binding heme domain related to soluble guanylate cyclases Proc. Natl. Acad. Sci. U.S.A. 101, 12854-12859
101. Price, M. S., Chao, L. Y., and Marletta, M. A. (2007) Shewanella oneidensis MR-1 H-NOX regulation of a histidine kinase by nitric oxide Biochemistry 46, 13677-13683
102. Wang, Y., Dufour, Y. S., Carlson, H. K., Donohue, T. J., Marletta, M. A., and Ruby, E. G. (2010) H-NOX-mediated nitric oxide sensing modulates symbiotic colonization by Vibrio fischeri Proc. Natl. Acad. Sci. U.S.A. 107, 8375-8380
103. Tsai, A. L., Berka, V., Martin, E., and Olson, J. S. (2012) A "sliding scale rule" for selectivity among NO, CO, and O2 by heme protein sensors Biochemistry 51, 172-186
104. Tsai, A. L., Martin, E., Berka, V., and Olson, J. S. (2012) How do heme-protein sensors exclude oxygen? Lessons learned from cytochrome c′, Nostoc puntiforme heme nitric oxide/oxygen-binding domain, and soluble guanylyl cyclase Antioxid. Redox Signaling 17, 1246-1263
105. Plate, L. and Marletta, M. A. (2013) Nitric oxide-sensing H-NOX proteins govern bacterial communal behavior Trends Biochem. Sci. 38, 566-575
106. Liu, N., Pak, T., and Boon, E. M. (2010) Characterization of a diguanylate cyclase from Shewanella woodyi with cyclase and phosphodiesterase activities Mol. BioSyst. 6, 1561-1564
107. Lahiri, T., Luan, B., Raleigh, D. P., and Boon, E. M. (2014) A structural basis for the regulation of an H-NOX-associated cyclic-di-GMP synthase/phosphodiesterase enzyme by nitric oxide-bound H-NOX Biochemistry 53, 2126-2135
108. Zapf, J., Madhusudan, M., Grimshaw, C. E., Hoch, J. A., Varughese, K. I., and Whiteley, J. M. (1998) A source of response regulator autophosphatase activity: The critical role of a residue adjacent to the Spo0F autophosphorylation active site Biochemistry 37, 7725-7732
109. Thormann, K. M., Saville, R. M., Shukla, S., and Spormann, A. M. (2005) Induction of rapid detachment in Shewanella oneidensis MR-1 biofilms J. Bacteriol. 187, 1014-1021
110. Henares, B. M., Xu, Y., and Boon, E. M. (2013) A Nitric Oxide-Responsive Quorum Sensing Circuit in Vibrio harveyi Regulates Flagella Production and Biofilm Formation Int. J. Mol. Sci. 14, 16473-16484
111. Visick, K. L. and Ruby, E. G. (2006) Vibrio fischeri and its host: It takes two to tango Curr. Opin. Microbiol. 9, 632-638
112. Lundberg, J. O., Weitzberg, E., Cole, J. A., and Benjamin, N. (2004) Nitrate, bacteria and human health Nat. Rev. Microbiol. 2, 593-602
113. Hyde, E. R., Luk, B., Cron, S., Kusic, L., McCue, T., Bauch, T., Kaplan, H., Tribble, G., Petrosino, J. F., and Bryan, N. S. (2014) Characterization of the rat oral microbiome and the effects of dietary nitrate Free Radical Biol. Med. 77, 249-257
114. Torreilles, J. (2001) Nitric oxide: One of the more conserved and widespread signaling molecules Front. Biosci. 6, D1161-D1172
115. Kers, J. A., Wach, M. J., Krasnoff, S. B., Widom, J., Cameron, K. D., Bukhalid, R. A., Gibson, D. M., Crane, B. R., and Loria, R. (2004) Nitration of a peptide phytotoxin by bacterial nitric oxide synthase Nature 429, 79-82
116. Shatalin, K., Gusarov, I., Avetissova, E., Shatalina, Y., McQuade, L. E., Lippard, S. J., and Nudler, E. (2008) Bacillus anthracis -derived nitric oxide is essential for pathogen virulence and survival in macrophages Proc. Natl. Acad. Sci. U.S.A. 105, 1009-1013
117. Gusarov, I. and Nudler, E. (2005) NO-mediated cytoprotection: Instant adaptation to oxidative stress in bacteria Proc. Natl. Acad. Sci. U.S.A. 102, 13855-13860
118. Gusarov, I., Shatalin, K., Starodubtseva, M., and Nudler, E. (2009) Endogenous nitric oxide protects bacteria against a wide spectrum of antibiotics Science 325, 1380-1384
119. Patel, B. A., Moreau, M., Widom, J., Chen, H., Yin, L., Hua, Y., and Crane, B. R. (2009) Endogenous nitric oxide regulates the recovery of the radiation-resistant bacterium Deinococcus radiodurans from exposure to UV light Proc. Natl. Acad. Sci. U.S.A. 106, 18183-18188
120. Gusarov, I., Gautier, L., Smolentseva, O., Shamovsky, I., Eremina, S., Mironov, A., and Nudler, E. (2013) Bacterial nitric oxide extends the lifespan of C. elegans Cell 152, 818-830
121. Schreiber, F., Beutler, M., Enning, D., Lamprecht-Grandio, M., Zafra, O., Gonzalez-Pastor, J. E., and de Beer, D. (2011) The role of nitric-oxide-synthase-derived nitric oxide in multicellular traits of Bacillus subtilis 3610: Biofilm formation, swarming, and dispersal BMC Microbiol. 11, 111
122. Yarullina, D. R., Vakatova, L. V., Krivoruchko, A. V., Rubtsova, E. V., and Ilinskaya, O. N. (2013) Effect of exogenous and endogenous nitric oxide on biofilm formation by Lactobacillus plantarum Microbiology 82, 423-427
123. Liu, P. L., Huang, Q. Y., and Chen, W. L. (2012) Heterologous expression of bacterial nitric oxide synthase gene: A potential biological method to control biofilm development in the environment Can. J. Microbiol. 58, 336-344
124. Carpenter, A. W. and Schoenfisch, M. H. (2012) Nitric oxide release: Part II. Therapeutic applications Chem. Soc. Rev. 41, 3742-3752
125. Privett, B. J., Broadnax, A. D., Bauman, S. J., Riccio, D. A., and Schoenfisch, M. H. (2012) Examination of bacterial resistance to exogenous nitric oxide Nitric Oxide 26, 169-173
126. Hetrick, E. M., Shin, J. H., Paul, H. S., and Schoenfisch, M. H. (2009) Anti-biofilm efficacy of nitric oxide-releasing silica nanoparticles Biomaterials 30, 2782-2789
127. Lu, Y., Slomberg, D. L., Shah, A., and Schoenfisch, M. H. (2013) Nitric Oxide-Releasing Amphiphilic Poly(amidoamine) (PAMAM) Dendrimers as Antibacterial Agents Biomacromolecules 14, 3589-3598
128. Lu, Y., Slomberg, D. L., and Schoenfisch, M. H. (2014) Nitric oxide-releasing chitosan oligosaccharides as antibacterial agents Biomaterials 35, 1716-1724
129. Slomberg, D. L., Lu, Y., Broadnax, A. D., Hunter, R. A., Carpenter, A. W., and Schoenfisch, M. H. (2013) Role of Size and Shape on Biofilm Eradication for Nitric Oxide-Releasing Silica Nanoparticles ACS Appl. Mater. Interfaces 5, 9322-9329
130. Marvasi, M., Chen, C., Carrazana, M., Durie, I. A., and Teplitski, M. (2014) Systematic analysis of the ability of Nitric Oxide donors to dislodge biofilms formed by Salmonella enterica and Escherichia coli O157:H7 AMB Express 4, 42
131. Duong, H. T. T., Adnan, N. N. M., Barraud, N., Basuki, J. S., Kutty, S. K., Jung, K., Kumar, N., Davis, T. P., and Boyer, C. (2014) Functional gold nanoparticles for the storage and controlled release of nitric oxide: Applications in biofilm dispersal and intracellular delivery J. Mater. Chem. B 2, 5003-5011
132. Duong, H. T. T., Jung, K., Kutty, S. K., Agustina, S., Adnan, N. N. M., Basuki, J. S., Kumar, N., Davis, T. P., Barraud, N., and Boyer, C. (2014) Nanoparticle (Star Polymer) Delivery of Nitric Oxide Effectively Negates Pseudomonas aeruginosa Biofilm Formation Biomacromolecules 15, 2583-2589
133. Barraud, N., Kardak, B. G., Yepuri, N. R., Howlin, R. P., Webb, J. S., Faust, S. N., Kjelleberg, S., Rice, S. A., and Kelso, M. J. (2012) Cephalosporin-3′-diazeniumdiolates: Targeted NO-donor prodrugs for dispersing bacterial biofilms Angew. Chem., Int. Ed. 51, 9057-9060
134. de la Fuente-Nunez, C., Reffuveille, F., Fairfull-Smith, K. E., and Hancock, R. E. (2013) Effect of nitroxides on swarming motility and biofilm formation, multicellular behaviors in Pseudomonas aeruginosa Antimicrob. Agents Chemother. 57, 4877-4881
135. Sulemankhil, I., Ganopolsky, J. G., Dieni, C. A., Dan, A. F., Jones, M. L., and Prakash, S. (2012) Prevention and treatment of virulent bacterial biofilms with an enzymatic nitric oxide-releasing dressing Antimicrob. Agents Chemother. 56, 6095-6103
136. Engelsman, A. F., Krom, B. P., Busscher, H. J., van Dam, D. G., Ploeg, R. J., and van der Mei, H. C. (2009) Antimicrobial effects of an NO-releasing poly(ethylene vinylacetate) coating on soft-tissue implants in vitro and in a murine model Acta Biomater. 5, 1905-1910
137. Parzuchowski, P. G., Frost, M. C., and Meyerhoff, M. E. (2002) Synthesis and Characterization of Polymethacrylate-Based Nitric Oxide Donors J. Am. Chem. Soc. 124, 12182-12191
138. Kutty, S. K., Barraud, N., Pham, A., Iskander, G., Rice, S. A., Black, D. S., and Kumar, N. (2013) Design, Synthesis, and Evaluation of Fimbrolide-Nitric Oxide Donor Hybrids as Antimicrobial Agents J. Med. Chem. 56, 9517-9529