Structure and effects of cyanobacterial lipopolysaccharides

Marine Drugs

Volumn 13, Issue 7, 2015, Pages 4217-4230

  Durai, Prasannavenkatesh ^a   Batool, Maria ^a   Choi, Sangdun ^a  

^a Ajou University   (South Korea)

Author keywords

Cyanobacteria; Cyanotoxin; Endotoxin; Lipid A; LPS; Sepsis; TLR

Indexed keywords

3 DEOXY MANNO OCTULOSONIC ACID; BACTERIUM LIPOPOLYSACCHARIDE; FATTY ACID DERIVATIVE; HEPTOSE; LIPID A; PHOSPHATE; TOLL LIKE RECEPTOR 4; LIPOPOLYSACCHARIDE;

AUTOIMMUNE DISEASE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BIOLOGICAL ACTIVITY; CARBOHYDRATE ANALYSIS; CYANOBACTERIUM; GRAM NEGATIVE BACTERIUM; HUMAN; IMMUNOREGULATION; INFLAMMATION; INNATE IMMUNITY; MARINE BACTERIUM; MARINE SPECIES; NONHUMAN; OUTER MEMBRANE; REVIEW; SEPSIS; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS; ANTAGONISTS AND INHIBITORS; AQUATIC SPECIES; CHEMISTRY; DRUG EFFECTS; ISOLATION AND PURIFICATION; PATHOPHYSIOLOGY;

CYANOBACTERIA; NEGIBACTERIA;

AQUATIC ORGANISMS; CYANOBACTERIA; GRAM-NEGATIVE BACTERIA; HUMANS; LIPOPOLYSACCHARIDES; SEPSIS; TOLL-LIKE RECEPTOR 4;

EID: 84938272089     PISSN: None     EISSN: 16603397     Source Type: Journal    
DOI: 10.3390/md13074217     Document Type: Review

References (63)

1. Berg, K. A.; Lyra, C.; Sivonen, K.; Paulin, L.; Suomalainen, S.; Tuomi, P.; Rapala, J. High diversity of cultivable heterotrophic bacteria in association with cyanobacterial water blooms. ISME J. 2009, 3, 314-325.
2. Sotero-Santos, R. B.; Silva, C. R.; Verani, N. F.; Nonaka, K. O.; Rocha, O. Toxicity of a cyanobacteria bloom in barra bonita reservoir (middle tiete river, Sao Paulo, Brazil). Ecotoxicol. Environ. Saf. 2006, 64, 163-170.
3. Tan, L. T. Bioactive natural products from marine cyanobacteria for drug discovery. Phytochemistry 2007, 68, 954-979.
4. Dixit, R. B.; Suseela, M. R. Cyanobacteria: Potential candidates for drug discovery. Antonie Van Leeuwenhoek 2013, 103, 947-961.
5. Chorus, I.; Falconer, I. R.; Salas, H. J.; Bartram, J. Health risks caused by freshwater cyanobacteria in recreational waters. J. Toxicol. Environ. Health B Crit. Rev. 2000, 3, 323-347.
6. Wang, L.; Liang, X. F.; Liao, W. Q.; Lei, L. M.; Han, B. P. Structural and functional characterization of microcystin detoxification-related liver genes in a phytoplanktivorous fish, nile tilapia (Oreochromis niloticus). Comp. Biochem. Physiol. C Toxicol. Pharmacol. 2006, 144, 216-227.
7. Wiegand, C.; Pflugmacher, S. Ecotoxicological effects of selected cyanobacterial secondary metabolites: A short review. Toxicol. Appl. Pharmacol. 2005, 203, 201-218.
8. Anwar, M. A.; Choi, S. Gram-negative marine bacteria: Structural features of lipopolysaccharides and their relevance for economically important diseases. Mar. Drugs 2014, 12, 2485-2514.
9. Molinaro, A.; Holst, O.; Di Lorenzo, F.; Callaghan, M.; Nurisso, A.; D'Errico, G.; Zamyatina, A.; Peri, F.; Berisio, R.; Jerala, R.; et al. Chemistry of lipid a: At the heart of innate immunity. Chemistry 2015, 21, 500-519.
10. Hoiczyk, E.; Hansel, A. Cyanobacterial cell walls: News from an unusual prokaryotic envelope. J. Bacteriol. 2000, 182, 1191-1199.
11. Leone, S.; Silipo, A.; Nazarenko, E. L.; Lanzetta, R.; Parrilli, M.; Molinaro, A. Molecular structure of endotoxins from Gram-negative marine bacteria: An update. Mar. Drugs 2007, 5, 85-112.
12. Snyder, D. S.; Brahamsha, B.; Azadi, P.; Palenik, B. Structure of compositionally simple lipopolysaccharide from marine synechococcus. J. Bacteriol. 2009, 191, 5499-5509.
13. Caroff, M.; Karibian, D. Structure of bacterial lipopolysaccharides. Carbohydr. Res. 2003, 338, 2431-2447.
14. Wang, X.; Quinn, P. J. Lipopolysaccharide: Biosynthetic pathway and structure modification. Prog. Lipid Res. 2010, 49, 97-107.
15. Sperandeo, P.; Deho, G.; Polissi, A. The lipopolysaccharide transport system of Gram-negative bacteria. Biochim. Biophys. Acta 2009, 1791, 594-602.
16. Stewart, I.; Schluter, P. J.; Shaw, G. R. Cyanobacterial lipopolysaccharides and human health - A review. Environ. Health 2006, 5, 7.
17. Hunter, P. R. Cyanobacterial toxins and human health. Symp. Ser. Soc. Appl. Microbiol. 1998, 27, 35S-40S.
18. Wilkinson, S. G. Bacterial lipopolysaccharides-Themes and variations. Prog. Lipid Res. 1996, 35, 283-343.
19. Moran, A. P. Molecular structure, biosynthesis, and pathogenic roles of lipopolysaccharides. In Helicobacter pylori: Physiology and Genetics; Mobley H. L. T., Mendz, G. L., Hazell, S. L., Eds.; ASM Press: Washington, DC, USA, 2001.
20. Raziuddin, S.; Siegelman, H. W.; Tornabene, T. G. Lipopolysaccharides of the cyanobacterium Microcystis aeruginosa. Eur. J. Biochem. 1983, 137, 333-336.
21. Martin, C.; Codd, G. A.; Siegelman, H. W.; Weckesser, J. Lipopolysaccharides and polysaccharides of the cell envelope of toxic Microcystis aeruginosa strains. Arch. Microbiol. 1989, 152, 90-94.
22. Fujii, M.; Sato, Y.; Ito, H.; Masago, Y.; Omura, T. Monosaccharide composition of the outer membrane lipopolysaccharide and O-chain from the freshwater cyanobacterium Microcystis aeruginosa NIES-87. J. Appl. Microbiol. 2012, 113, 896-903.
23. Weise, G.; Drews, G.; Jann, B.; Jann, K. Identification and analysis of a lipopolysaccharide in cell walls of the blue-green alga Anacystis nidulans. Arch. Mikrobiol. 1970, 71, 89-98.
24. Katz, A.; Weckesser, J.; Drews, G.; Mayer, H. Chemical and biological studies on the lipopolysaccharide (O-antigen) of Anacystis nidulans. Arch. Microbiol. 1977, 113, 247-256.
25. Buttke, T. M.; Ingram, L. O. Comparison of lipopolysaccharides from Agmenellum quadruplicatum to Escherichia coli and Salmonella typhimurium by using thin-layer chromatography. J. Bacteriol. 1975, 124, 1566-1573.
26. Keleti, G.; Sykora, J. L.; Lippy, E. C.; Shapiro, M. A. Composition and biological properties of lipopolysaccharides isolated from Schizothrix calcicola (Ag.) Gomont (Cyanobacteria). Appl. Environ. Microbiol. 1979, 38, 471-477.
27. Keleti, G.; Sykora, J. L. Production and properties of cyanobacterial endotoxins. Appl. Environ. Microbiol. 1982, 43, 104-109.
28. Tornabene, T.; Bourne, T.; Raziuddin, S.; Ben-Amotz, A. Lipid and lipopolysaccharide constituents of cyanobacterium Spirulina platensis (Cyanophyceae, Nostocales). Mar. Ecol. Prog. Ser. 1985, 22, 121-125.
29. Carillo, S.; Pieretti, G.; Bedini, E.; Parrilli, M.; Lanzetta, R.; Corsaro, M. M. Structural investigation of the antagonist LPS from the cyanobacterium Oscillatoria planktothrix FP1. Carbohydr. Res. 2014, 388, 73-80.
30. Mikheyskaya, L. V.; Ovodova, R. G.; Ovodov, Y. S. Isolation and characterization of lipopolysaccharides from cell walls of blue-green algae of the genus Phormidium. J. Bacteriol. 1977, 130, 1-3.
31. Ianaro, A.; Tersigni, M.; D'Acquisto, F. New insight in LPS antagonist. Mini Rev. Med. Chem. 2009, 9, 306-317.
32. Savva, A.; Roger, T. Targeting Toll-like receptors: Promising therapeutic strategies for the management of sepsis-associated pathology and infectious diseases. Front. Immunol. 2013, 4, 387.
33. Kumar, H.; Kawai, T.; Akira, S. Pathogen recognition by the innate immune system. Int. Rev. Immunol. 2011, 30, 16-34.
34. Roach, J. C.; Glusman, G.; Rowen, L.; Kaur, A.; Purcell, M. K.; Smith, K. D.; Hood, L. E.; Aderem, A. The evolution of vertebrate Toll-like receptors. Proc. Natl. Acad. Sci. USA 2005, 102, 9577-9582.
35. Akira, S.; Uematsu, S.; Takeuchi, O. Pathogen recognition and innate immunity. Cell 2006, 124, 783-801.
36. Botos, I.; Segal, D. M.; Davies, D. R. The structural biology of Toll-like receptors. Structure 2011, 19, 447-459.
37. Durai, P.; Govindaraj, R. G.; Choi, S. Structure and dynamic behavior of Toll-like receptor 2 subfamily triggered by malarial glycosylphosphatidylinositols of Plasmodium falciparum. FEBS J. 2013, 280, 6196-6212.
38. Akira, S.; Takeda, K. Toll-like receptor signalling. Nat. Rev. Immunol. 2004, 4, 499-511.
39. Kang, J. Y.; Lee, J. O. Structural biology of the Toll-like receptor family. Annu. Rev. Biochem. 2011, 80, 917-941.
40. Park, B. S.; Song, D. H.; Kim, H. M.; Choi, B. S.; Lee, H.; Lee, J. O. The structural basis of lipopolysaccharide recognition by the TLR4-MD-2 complex. Nature 2009, 458, 1191-1195.
41. Kawai, T.; Akira, S. The role of pattern-recognition receptors in innate immunity: Update on Toll-like receptors. Nat. Immunol. 2010, 11, 373-384.
42. Kawasaki, T.; Kawai, T. Toll-like receptor signaling pathways. Front. Immunol. 2014, 5, 461.
43. Kawai, T.; Akira, S. TLR signaling. Cell Death Differ. 2006, 13, 816-825.
44. Kondo, T.; Kawai, T.; Akira, S. Dissecting negative regulation of Toll-like receptor signaling. Trends Immunol. 2012, 33, 449-458.
45. Jin, M. S.; Lee, J. O. Structures of the Toll-like receptor family and its ligand complexes. Immunity 2008, 29, 182-191.
46. Nijland, R.; Hofland, T.; van Strijp, J. A. Recognition of LPS by TLR4: Potential for anti-inflammatory therapies. Mar. Drugs 2014, 12, 4260-4273.
47. Macagno, A.; Molteni, M.; Rinaldi, A.; Bertoni, F.; Lanzavecchia, A.; Rossetti, C.; Sallusto, F. A cyanobacterial LPS antagonist prevents endotoxin shock and blocks sustained TLR4 stimulation required for cytokine expression. J. Exp. Med. 2006, 203, 1481-1492.
48. Thorgersen, E. B.; Macagno, A.; Rossetti, C.; Mollnes, T. E. Cyanobacterial LPS antagonist (CyP) - A novel and efficient inhibitor of Escherichia coli LPS-induced cytokine response in the pig. Mol. Immunol. 2008, 45, 3553-3557.
49. Jemmett, K.; Macagno, A.; Molteni, M.; Heckels, J. E.; Rossetti, C.; Christodoulides, M. A cyanobacterial lipopolysaccharide antagonist inhibits cytokine production induced by Neisseria meningitidis in a human whole-blood model of septicemia. Infect. Immun. 2008, 76, 3156-3163.
50. Oliver, R.; Staples, K. J.; Heckels, J.; Rossetti, C.; Molteni, M.; Christodoulides, M. Coadministration of the cyanobacterial lipopolysaccharide antagonist CyP with antibiotic inhibits cytokine production by an in vitro meningitis model infected with Neisseria meningitidis. J. Antimicrob. Chemother. 2012, 67, 1145-1154.
51. De Paola, M.; Mariani, A.; Bigini, P.; Peviani, M.; Ferrara, G.; Molteni, M.; Gemma, S.; Veglianese, P.; Castellaneta, V.; Boldrin, V.; et al. Neuroprotective effects of Toll-like receptor 4 antagonism in spinal cord cultures and in a mouse model of motor neuron degeneration. Mol. Med. 2012, 18, 971-981.
52. Raetz, C. R.; Reynolds, C. M.; Trent, M. S.; Bishop, R. E. Lipid a modification systems in Gram-negative bacteria. Annu. Rev. Biochem. 2007, 76, 295-329.
53. Beasley, A. S.; Cotter, R. J.; Vogel, S. N.; Inzana, T. J.; Qureshi, A. A.; Qureshi, N. A variety of novel lipid a structures obtained from Francisella tularensis live vaccine strain. Innate. Immun. 2012, 18, 268-278.
54. Schilling, B.; McLendon, M. K.; Phillips, N. J.; Apicella, M. A.; Gibson, B. W. Characterization of lipid a acylation patterns in Francisella tularensis, Francisella novicida, and Francisella philomiragia using multiple-stage mass spectrometry and matrix-assisted laser desorption/ionization on an intermediate vacuum source linear ion trap. Anal. Chem. 2007, 79, 1034-1042.
55. Rose, J. R.; Christ, W. J.; Bristol, J. R.; Kawata, T.; Rossignol, D. P. Agonistic and antagonistic activities of bacterially derived Rhodobacter sphaeroides lipid A: Comparison with activities of synthetic material of the proposed structure and analogs. Infect. Immun. 1995, 63, 833-839.
56. Blahova, L.; Adamovsky, O.; Kubala, L.; Svihalkova Sindlerova, L.; Zounkova, R.; Blaha, L. The isolation and characterization of lipopolysaccharides from Microcystis aeruginosa, a prominent toxic water bloom forming cyanobacteria. Toxicon 2013, 76, 187-196.
57. Zanchett, G.; Oliveira-Filho, E. C. Cyanobacteria and cyanotoxins: From impacts on aquatic ecosystems and human health to anticarcinogenic effects. Toxins (Basel) 2013, 5, 1896-1917.
58. Rapala, J.; Lahti, K.; Rasanen, L. A.; Esala, A. L.; Niemela, S. I.; Sivonen, K. Endotoxins associated with cyanobacteria and their removal during drinking water treatment. Water Res. 2002, 36, 2627-2635.
59. Jakubowska, N.; Szelag-Wasielewska, E. Toxic picoplanktonic cyanobacteria-Review. Mar. Drugs 2015, 13, 1497-1518.
60. Best, J. H.; Pflugmacher, S.; Wiegand, C.; Eddy, F. B.; Metcalf, J. S.; Codd, G. A. Effects of enteric bacterial and cyanobacterial lipopolysaccharides, and of microcystin-LR, on glutathione S-transferase activities in zebra fish (Danio rerio). Aquat. Toxicol. 2002, 60, 223-231.
61. Jaja-Chimedza, A.; Gantar, M.; Mayer, G. D.; Gibbs, P. D.; Berry, J. P. Effects of cyanobacterial lipopolysaccharides from microcystis on glutathione-based detoxification pathways in the zebrafish (Danio rerio) embryo. Toxins (Basel) 2012, 4, 390-404.
62. Notch, E. G.; Miniutti, D. M.; Berry, J. P.; Mayer, G. D. Cyanobacterial LPS potentiates cadmium toxicity in zebrafish (Danio rerio) embryos. Environ. Toxicol. 2011, 26, 498-505.
63. Ferrao-Filho Ada, S.; Kozlowsky-Suzuki, B. Cyanotoxins: Bioaccumulation and effects on aquatic animals. Mar. Drugs 2011, 9, 2729-2772.