Oxidized fatty acids as inter-kingdom signaling molecules

Molecules

Volumn 19, Issue 1, 2014, Pages 1273-1285

  Pohl, Carolina H ^a   Kock, Johan L F ^a  

^a UNIVERSITY OF THE FREE STATE   (South Africa)

Author keywords

Inter kingdom communication; Oxidized fatty acids; Signaling

Indexed keywords

OXYLIPIN;

ANIMAL; EVOLUTION; HOST PARASITE INTERACTION; HOST PATHOGEN INTERACTION; HUMAN; METABOLISM; MICROBIOLOGY; PARASITOLOGY; PLANT; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; BIOLOGICAL EVOLUTION; HOST-PARASITE INTERACTIONS; HOST-PATHOGEN INTERACTIONS; HUMANS; OXYLIPINS; PLANTS; SIGNAL TRANSDUCTION;

EID: 84893117139     PISSN: None     EISSN: 14203049     Source Type: Journal    
DOI: 10.3390/molecules19011273     Document Type: Review

References (67)

1. Schultz, J.C. Shared signals and the potential for phylogenetic espionage between plants and animals. Integr. Comp. Biol. 2002, 42, 454-462.
2. Schultz, J.C.; Appel, H.M. Cross-kingdom cross-talk: Hormones shared by plants and insects and their herbivores. Ecology 2004, 85, 70-77.
3. Savchenko, T.; Walley, J.W.; Chehab, E.W.; Xiao, Y.; Kaspi, R.; Pye, M.F.; Mohamed, M.E.; Lazarus, C.M.; Bostock, R.M.; Dehesh, K. Arachidonic acid: An evolutionary conserved signaling molecule modulates plant stress signaling networks. Plant Cell 2010, 22, 3193-3205.
4. Hernandez-Oñate, M.A.; Esquivel-Naranjo, E.U.; Mendoza-Mendoza, A.; Stewart, A.; Herrera-Estrella, A.H. An injury-response mechanism conserved across kingdoms determines entry of the fungus Trichoderma atroviride into development. Proc. Natl. Acad. Sci. USA 2012, 109, 14918-14923.
5. Haas-Stapleton, E.J.; Lu, Y.; Hong, S.; Arita, M.; Favoreto, S.; Nigam, S.; Serhan, C.N.; Agabian, N. Candida albicans modulates host defence by biosynthesizing the pro-resolving mediator resolvin E1. PLoS One 2007, 12, e1316.
6. Weber, H. Fatty acid-derived signals in plants. Trends Plant. Sci. 2002, 7, 217-224.
7. Li, X.; Schuler, M.A.; Berenbaum, M.R. Jasmonate and salicylate induce expression of herbivore cytochrome 450 genes. Nature 2002, 419, 712-715.
8. Parchmann, S.; Meuller, M.J. Evidence for the formation of dinor isoprostanes E1 from linolenic acid in plants. J. Biol. Chem. 1998, 273, 32650-32655.
9. Imbusch, R.; Meuller, M.J. Formation of isoprostane F2-like compounds (phytoprostanes F1) from a-linolenic acid in plants. Free Radic. Biol. Med. 2000, 28, 720-726.
10. Traidl-Hoffmann, C.; Mariani, V.; Hochrein, H.; Karg, K.; Wagner, H.; Ring, J.; Meuller, M.J.; Jakob, T.; Behrendt, H. Pollen-Associated phytoprostanes inhibit dendritic cell interleukin-12 production and augment T helper type 2 cell polarization. J. Exp. Med. 2005, 20, 627-636.
11. Gilles, S.; Mariani, V.; Bryce, M.; Meuller, M.J.; Ring, J.; Behrendt, H.; Jakob, T.; Traidl-Hoffmann, C. Pollen allergens do not come alone: Pollen associated lipid mediators (PALMS) shift the human immune systems towards a Th2-dominated response. Allergy Asthma Clin. Immunol. 2009, 5, 3.
12. Traidl-Hoffmann, C.; Kasche, A.; Jakob, T.; Huger, M.; Plötz, S.; Feussner, I.; Ring, J.; Behrendt, H. Lipid mediators from pollen act as chemoattractants and activators of polymorphonuclear granulocytes. J. Allergy Clin. Immunol. 2002, 109, 831-838.
13. Gilles, S.; Mariani, V.; Bryce, M.; Meuller, M.J.; Ring, J.; Jakob, T.; Pastore, S.; Behrendt, H.; Traidl-Hoffmann, C. Pollen derived E1 phytoprostanes signal via PPAR-? and NF-?B dependent mechanisms. J. Immunol. 2009, 182, 6653-6658.
14. Alborn, H.T.; Turlings, T.C.J.; Jones, T.H.; Stenhagen, G.; Loughrin, J.H.; Tumlinson, J.H. An elicitor of plant volatiles from beet armyworm oral secretion. Science 1997, 276, 945-949.
15. Turlings, T.C.J.; Alborn, H.T.; Loughrin, J.H.; Tumlinson, J.H. Volicitin, an elicitor of maize volatiles in oral secretions of Spodoptera exigua: Isolation and bioactivity. J. Chem. Ecol. 2000, 26, 189-202.
16. Mori, N.; Yoshinaga, N. Function and evolutionary diversity of fatty acid amino acid conjugates in insects. J. Plant Interact. 2011, 6, 103-107.
17. Häring, D.A.; Huber, M.J.; Suter, D.; Edwards, P.J.; Lüscher, A. Plant enemy-derived elicitors increase the foliar tannin concentration of Onobrychis viciifolia without a trade-off to growth. Ann. Bot. 2008, 102, 979-987.
18. Fontana, A.; d'Ippolito, G.; Cutignano, A.; Romano, G.; Lamari, N.; Massa Gallucci, A.; Cimino, A.; Miralto, G.; Ianora, A. A metabolic mechanism for the detrimental effect of marine diatoms on zooplankton grazers. ChemBioChem 2007, 8, 1810-1818.
19. Ianora, A.; Romano, G.; Carotenuto, Y.; Esposito, F.; Roncalli, V.; Buttino, I.; Miralto, A. Impact of the diatom oxylipin 15S-HEPE on the reproductive success of the copepod Temora stylifera. Hydrobiologia 2011, 666, 265-275.
20. Ianora, A.; Miralto, A. Toxigenic effects of diatoms on grazers, phytoplankton and other microbes: A review. Ecotoxicology 2010, 19, 493-511.
21. Smith, W.L. The eicosanoids and their biochemical mechanism of action. Biochem. J. 1989, 259, 315-324.
22. Zeldin, D.C. Epoxygenase pathways of arachidonic acid metabolism. J. Biol. Chem. 2001, 276, 36059-36062.
23. Murakami, M.; Kudo, I. Recent advances in molecular biology and physiology of the prostaglandin E2-biosynthetic pathway. Prog. Lipid Res. 2004, 43, 3-35.
24. Henderson, W.R. The role of leukotrienes in inflammation. Ann. Intern. Med. 1994, 121, 684-697.
25. Carroll, M.A.; McGiff, J.C. A new class of lipid mediators: Cytochrome P450 arachidonate metabolites. Thorax 2000, 55, S13-S16.
26. Buczynski, M.W.; Dumlao, D.S.; Dennis, E.D. Thematic review: An integrated omics analysis of eicosanoid biology. J. Lipid Res. 2009, 50, 1015-1038.
27. Serhan, C.N.; Arita, M.; Hong, S.; Gotlinger, K. Resolvins, docosatrienes, and neuroprotectins, novel omega-3-derived mediators, and their endogenous aspirin-triggered epimers. Lipids 2004, 39, 1125-1132.
28. Funk, C.D. Prostaglandins and leukotrienes: Advances in eicosanoid biology. Science 2001, 294, 1871-1875.
29. Hatae, N.; Sugimoto, Y.; Ichikawa, A. Prostaglandin receptors: Advances in the study of EP3 receptor signalling. J. Biochem. 2002, 131, 781-783.
30. Tsitsigiannis, D.I.; Keller, N.P. Oxylipins as developmental and host-fungal communication signals. Trends Microbiol. 2007, 15, 109-118.
31. Ells, R.; Kock, J.L.F.; Albertyn, J.; Pohl, C.H. Arachidonic acid metabolites of pathogenic yeasts. Lipids Health Dis. 2012, 11, doi:10.1186/1476-511X-11-100.
32. Noverr, M.C.; Phare, S.M.; Toews, G.B.; Coffey, M.J.; Huffnagle, G.B. Pathogenic yeasts Cryptococcus neoformans and Candida albicans produce immunomodulatory prostaglandins. Infect. Immun. 2001, 69, 2957-2963.
33. Shiraki, Y.; Ishbashi, Y.; Hiruma, M.; Nashikawa, A.; Ikeda, S. Candida albicans abrogates the expression of interferon-?-inducible protein-10 in human keratinocytes. FEMS Immunol. Med. Microbiol. 2008, 54, 122-128.
34. Ells, R.; Kock, J.L.F.; Albertyn, J.; Kemp, G.; Pohl, C.H. Effect of inhibitors of arachidonic acid metabolism on prostaglandin E2 production by Candida albicans and Candida dubliniensis. Med. Microbiol. Immunol. 2011, 200, 23-28.
35. Noverr, M.C.; Toews, G.B.; Huffnagle, G.B. Production of prostaglandins and leukotrienes by pathogenic fungi. Infect. Immun. 2002, 70, 400-402.
36. Bordon, A.P.; Dias-Melicio, L.A.; Acorci, M.J.; Calvi, S.A.; Peraçoli, M.T.S.; Soares, A.M.V.C. Prostalandin E2 inhibits Paracoccidioides brasiliensis killing by human monocytes. Microbes Infect. 2007, 9, 744-747.
37. Biondo, G.A.; Dias-Melicio, L.A.; Bordon-Graciani, A.P.; Acorci-Valério, M.J.; Soares, A.M.V.C. Paracoccidioides brasiliensis uses endogenous and exogenous arachidonic acid for PGEx production. Mycopathologia 2010, 170, 123-130.
38. Tsitsigiannis, D.I.; Bok, J.; Andes, D.; Nielsen, K.F.; Frisvad, J.C.; Keller, N.P. Aspergillus cyclooxygenase-like enzymes are associated with prostaglandin production and virulence. Infect. Immun. 2005, 73, 4548-4559.
39. Kupfahl, C.; Tsikas, D.; Niemann, J.; Geginat, G.; Hof, H. Production of prostaglandins, isoprostanes and thromboxane by Aspergillus fumigatus: Identification by gas chromatography-tandem mass spectrometry and quantification by enzyme immunoassay. Mol. Immunol. 2012, 49, 621-627.
40. Betz, M.; Fox, B.S. Prostaglandin E2 inhibits production of Th1 lymphokines but not of Th2 lymphokines. J. Immunol. 1991, 146, 108-113.
41. Soares, A.M.V.C.; Calvi, S.A.; Peraçoli, M.T.S.; Fernandez, A.C.; Dias, L.A.; Dos Anjos, A.R. Modulatory effect of prostaglandins on human monocyte activiation for killing of high-And low-virulence strains of Paracoccidioides brasiliensis. Immunology 2001, 102, 480-485.
42. Noverr, M.C.; Erb-Downward, J.R.; Huffnagle, G.B. Production of eicosanoids and other oxylipins by pathogenic eukaryotic microbes. Clin. Microbiol. Rev. 2003, 16, 517-533.
43. Shibata, Y.; Hendersen, R.A.; Honda, I.; Nakamura, R.M.; Myrvik, Q.N. Splenic PGE2-releasing macrophages regulate Th1 and Th2 immune responses in mice treated with heat-killed BCG. J. Leukoc. Biol. 2005, 78, 1281-1290.
44. Kalo-Klein, A.; Witkin, S.S. Prostaglandin E2 enhances and gamma-interferon inhibits germ tube formation in Candida albicans. Infect. Immun. 1990, 58, 260-262.
45. Noverr, M.C.; Huffnagle, G.B. Regulation of Candida albicans morphogenesis by fatty acid metabolites. Infect. Immun. 2004, 72, 6206-6210.
46. Yang, J.; Eiserich, J.P.; Cross, C.E.; Morrissey, B.M.; Hammock, B.D. Metabolomic profiling of regulatory lipid mediators in sputum from adult cystic fibrosis patients. Free Radic. Biol. Med. 2012, 53, 160-171.
47. Eiserich, J.P.; Yang, J.; Morrissey, B.M.; Hammock, B.D.; Cross, C.E. Omics approaches in cystic fibrosis research: A focus on oxylipin profiling in airway secretions. Ann. N. Y. Acad. Sci. 2012, 1259, 1-9.
48. Ciofu, O.; Hansen, C.R.; Høiby, N. Respiratory bacterial infections in cystic fibrosis. Curr. Opin. Pulm. Med. 2013, 19, 251-258.
49. Saliba, A.M.; Nascimento, D.O.; Silva, M.C.A.; Assis, M.C.; Gayer, C.R.M.; Raymond, B.; Coelho, M.G.P.; Marques, E.A.; Touqui, L.; Albano, R.M.; et al. Eicosanoid-mediated proinflammatory activity of Pseudomonas aeruginosa ExoU. Cell. Microbiol. 2005, 7, 1811-1822.
50. Vance, R.E.; Hong, S.; Gronert, K.; Serhan, C.N.; Mekalanos, J.J. The opportunistic pathogen Pseudomonas aeruginosa carries a secretable arachidonate 15-lipoxygenase. Proc. Natl. Acad. Sci. USA 2004, 101, 2135-2139.
51. Kühn, H.; O'Donnell, V.B. Inflammation and immune regulation by 12/15-lipoxygenases. Prog. Lipid Res. 2006, 45, 334-356.
52. Kühn, H.; Walther, M.; Kuban, R.J. Mammalian arachidonate 15-lipoxygenases, structure, function and biological implications. Prostaglandins Other Lipid Mediat. 2002, 68, 263-290.
53. Weil, K.; Gruber, P.; Heckel, F.; Harmsen, D.; Schreier, P. Selective (R)-3-hydroxylation of FA by Stenotrophomonas maltophilia. Lipids 2002, 37, 317-323.
54. Ciccoli, R.; Sahi, S.; Singh, S.; Prakash, H.; Zafiriou, M.-P.; Ishdorj, G.; Kock, J.L.F.; Nigam, S. Oxygenation by COX-2 (cyclo-oxygenase-2) of 3-HETE (3-hydroxyeicosatetraenoic acid), a fungal mimetic of arachidonic acid, produces a cascade of novel bioactive 3-hydroxyeicosanoids. Biochem. J. 2005, 390, 737-747.
55. Tirelli, A.S.; Colombo, C.; Torresani, E.; Fortunato, F.; Biffi, A.; Cariani, L.; Daccò, V.; Carbone, A.; Edefonti, A.; Paglialonga, F.; et al. Effects of treatment in the levels of circulating cytokines and growth factors in cystic fibrosis and dialyzed patients by multi-Analytical determination with a biochip array platform. Cytokine 2013, 62, 413-420.
56. Beiersdorf, N.; Schien, M.; Hentschel, J.; Pfister, W.; Markert, U.R.; Mainz, J.G. Soluble inflammation markers in nasal lavage from CF patients and healthy controls. J. Cystic Fibrosis 2013, 12, 249-257.
57. King, S.J.; Nyulasi, I.B.; Bailey, M.; Kotsimbos, T.; Wilson, J.W. Loss of fat-free mass over four years in adult cystic fibrosis is associated with high serum interleukin-6 levels but not tumour necrosis factor-Alpha. Clin. Nutrit. 2013, doi:10.1016/j.clnu.2013.04.012.
58. Christensen, S.A.; Kolomiets, M.V. The lipid language of plant-fungal interactions. Fungal Genet. Biol. 2011, 48, 4-14.
59. Calvo, A.; Hinze, L.; Gardner, H.; Keller, N.P. Sporogenic effect of polyunsaturated fatty acids on Aspergillus ssp. development. Appl. Environ. Microbiol. 1999, 65, 3668-3673.
60. Burow, G.B.; Nesbitt, T.C.; Dunlap, J.; Keller, N.P. Seed lipoxygenase products modulate Aspergillus mycotoxin biosynthesis. Mol. Plant. Microbe Interact. 1997, 10, 380-387.
61. Gao, X.Q.; Kolomiets, M.V. Host-derived lipids and oxylipins are crucial signals in modulating mycotoxin production by fungi. Toxin Rev. 2009, 28, 79-88.
62. Goodrich-Tanrikulu, M.; Mahoney, N.E.; Rodriques, S.B. The plant-growth regulator methyl jasmonate inhibits aflatoxin production by Aspergillus flavus. Microbiology 1995, 141, 2831-2837.
63. Vergopoulou, S.; Galanopoulou, D.; Markaki, P. Methyl jasmonate stimulates aflatoxin B-1 biosynthesis by Aspergillus parasiticus. J. Agric. Food Chem. 2001, 49, 3494-3498.
64. Brodhagen, M.; Tsitsigiannis, D.I.; Hornung, E.; Goebel, C.; Feussner, I.; Keller, N.P. Reciprocal oxylipin-mediated cross-talk in the Aspergillus-seed pathosystem. Mol. Microbiol. 2008, 67, 378-391.
65. Tsukada, K.; Takahashi, K.; Nabeta, K. Biosynthesis of jasmonic acid in a plant pathogenic fungus, Lasiodiplodia theobromae. Phytochemistry 2010, 71, 2019-2023.
66. Morcillo, R.J.L.; Ocampo, J.A.; García Garrido, J.M. Plant 9-lox oxylipin metabolism in response to arbuscular mycorrhiza. Plant. Signal. Behav. 2012, 7, 1-5.
67. Ding, L.; Peschel, G.; Hertwick, C. Biosynthesis of archetypal plant self-defensive oxylipins by an endophytic fungus in mangrove embryos. ChemBioChem 2012, 13, 2661-2664.