全部 标题 作者
关键词 摘要

OALib Journal期刊
ISSN: 2333-9721
费用:99美元

查看量下载量

相关文章

更多...
PLOS ONE  2014 

Up-Regulated Expression of AOS-LOXa and Increased Eicosanoid Synthesis in Response to Coral Wounding

DOI: 10.1371/journal.pone.0089215

Full-Text   Cite this paper   Add to My Lib

Abstract:

In octocorals, a catalase–like allene oxide synthase (AOS) and an 8R-lipoxygenase (LOX) gene are fused together encoding for a single AOS-LOX fusion protein. Although the AOS-LOX pathway is central to the arachidonate metabolism in corals, its biological function in coral homeostasis is unclear. Using an acute incision wound model in the soft coral Capnella imbricata, we here test whether LOX pathway, similar to its role in plants, can contribute to the coral damage response and regeneration. Analysis of metabolites formed from exogenous arachidonate before and after fixed time intervals following wounding indicated a significant increase in AOS-LOX activity in response to mechanical injury. Two AOS-LOX isoforms, AOS-LOXa and AOS-LOXb, were cloned and expressed in bacterial expression system as active fusion proteins. Transcription levels of corresponding genes were measured in normal and stressed coral by qPCR. After wounding, AOS-LOXa was markedly up-regulated in both, the tissue adjacent to the incision and distal parts of a coral colony (with the maximum reached at 1 h and 6 h post wounding, respectively), while AOS-LOXb was stable. According to mRNA expression analysis, combined with detection of eicosanoid product formation for the first time, the AOS-LOX was identified as an early stress response gene which is induced by mechanical injury in coral.

References

[1]  Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, et al. (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301: 929–933. doi: 10.1126/science.1085046
[2]  Rotjan RD, Lewis SM (2008) Impact of coral predators on tropical reefs. Marine Ecology Progress Series 367: 73–91. doi: 10.3354/meps07531
[3]  Kultz D (2005) Molecular and evolutionary basis of the cellular stress response. Annu Rev Physiol 67: 225–257. doi: 10.1146/annurev.physiol.67.040403.103635
[4]  Fang LS, Huang SP, Lin KL (1997) High temperature induces the synthesis of heat-shock proteins and the elevation of intracellular calcium in the coral Acropora grandis. Coral Reefs 16: 127–131. doi: 10.1007/s003380050066
[5]  DeSalvo MK, Voolstra CR, Sunagawa S, Schwarz JA, Stillman JH, et al. (2008) Differential gene expression during thermal stress and bleaching in the Caribbean coral Montastraea faveolata. Mol Ecol 17: 3952–3971. doi: 10.1111/j.1365-294x.2008.03879.x
[6]  Souter P, Bay LK, Andreakis N, Csaszar N, Seneca FO, et al. (2011) A multilocus, temperature stress-related gene expression profile assay in Acropora millepora, a dominant reef-building coral. Mol Ecol Resour 11: 328–334. doi: 10.1111/j.1755-0998.2010.02923.x
[7]  Seneca FO, Forêt S, Ball EE, Smith-Keune C, Miller DJ, et al. (2009) Patterns of Gene Expression in a Scleractinian Coral Undergoing Natural Bleaching. Marine Biotechnology 12: 594–604. doi: 10.1007/s10126-009-9247-5
[8]  Woo S, Jeon H-y, Lee J, Song J-I, Park H-S, et al. (2010) Isolation of hyperthermal stress responsive genes in soft coral (Scleronephthya gracillimum). Molecular & Cellular Toxicology 6: 384–390. doi: 10.1007/s13273-010-0051-0
[9]  Singer AJ, Clark RA (1999) Cutaneous wound healing. N Engl J Med 341: 738–746. doi: 10.1056/nejm199909023411006
[10]  Palmer CV, Traylor-Knowles NG, Willis BL, Bythell JC (2011) Corals use similar immune cells and wound-healing processes as those of higher organisms. PLoS One 6: e23992. doi: 10.1371/journal.pone.0023992
[11]  Reitzel AM, Sullivan JC, Traylor-Knowles N, Finnerty JR (2008) Genomic survey of candidate stress-response genes in the estuarine anemone Nematostella vectensis. Biol Bull 214: 233–254. doi: 10.2307/25470666
[12]  Meszaros A, Bigger C (1999) Qualitative and quantitative study of wound healing processes in the coelenterate, Plexaurella fusifera: spatial, temporal, and environmental (light attenuation) influences. J Invertebr Pathol 73: 321–331. doi: 10.1006/jipa.1999.4851
[13]  Work TM, Aeby GS (2010) Wound repair in Montipora capitata. Journal of Invertebrate Pathology 105: 116–119. doi: 10.1016/j.jip.2010.05.009
[14]  Palmer CV, Mydlarz LD, Willis BL (2008) Evidence of an inflammatory-like response in non-normally pigmented tissues of two scleractinian corals. Proc Biol Sci 275: 2687–2693. doi: 10.1098/rspb.2008.0335
[15]  Mydlarz LD, Holthouse SF, Peters EC, Harvell CD (2008) Cellular responses in sea fan corals: granular amoebocytes react to pathogen and climate stressors. PLoS One 3: e1811. doi: 10.1371/journal.pone.0001811
[16]  Mydlarz LD, Harvell CD (2007) Peroxidase activity and inducibility in the sea fan coral exposed to a fungal pathogen. Comp Biochem Physiol A Mol Integr Physiol 146: 54–62. doi: 10.1016/j.cbpa.2006.09.005
[17]  Serhan CN, Chiang N, Van Dyke TE (2008) Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators. Nat Rev Immunol 8: 349–361. doi: 10.1038/nri2294
[18]  Schneider C, Pratt DA, Porter NA, Brash AR (2007) Control of oxygenation in lipoxygenase and cyclooxygenase catalysis. Chem Biol 14: 473–488. doi: 10.1016/j.chembiol.2007.04.007
[19]  Kuhn H, O'Donnell VB (2006) Inflammation and immune regulation by 12/15-lipoxygenases. Prog Lipid Res 45: 334–356. doi: 10.1016/j.plipres.2006.02.003
[20]  Kalish BT, Kieran MW, Puder M, Panigrahy D (2013) The growing role of eicosanoids in tissue regeneration, repair, and wound healing. Prostaglandins Other Lipid Mediat 104–105: 130–138. doi: 10.1016/j.prostaglandins.2013.05.002
[21]  Mauch F, Kmecl A, Schaffrath U, Volrath S, Gorlach J, et al. (1997) Mechanosensitive expression of a lipoxygenase gene in wheat. Plant Physiol 114: 1561–1566. doi: 10.1104/pp.114.4.1561
[22]  Sivasankar S, Sheldrick B, Rothstein SJ (2000) Expression of allene oxide synthase determines defense gene activation in tomato. Plant Physiol 122: 1335–1342. doi: 10.1104/pp.122.4.1335
[23]  Andreou A, Brodhun F, Feussner I (2009) Biosynthesis of oxylipins in non-mammals. Prog Lipid Res 48: 148–170. doi: 10.1016/j.plipres.2009.02.002
[24]  Gfeller A, Baerenfaller K, Loscos J, Chetelat A, Baginsky S, et al. (2011) Jasmonate Controls Polypeptide Patterning in Undamaged Tissue in Wounded Arabidopsis Leaves. Plant Physiology 156: 1797–1807. doi: 10.1104/pp.111.181008
[25]  Bundy GL, Nidy EG, Epps DE, Mizsak SA, Wnuk RJ (1986) Discovery of an arachidonic acid C-8 lipoxygenase in the gorgonian coral Pseudoplexaura porosa. J Biol Chem 261: 747–751.
[26]  Brash AR, Baertschi SW, Ingram CD, Harris TM (1987) On non-cyclooxygenase prostaglandin synthesis in the sea whip coral, Plexaura homomalla: an 8(R)-lipoxygenase pathway leads to formation of an alpha-ketol and a Racemic prostanoid. J Biol Chem 262: 15829–15839.
[27]  Varvas K, Koljak R, Jarving I, Pehk T, Samel N (1994) Endoperoxide Pathway in Prostaglandin Biosynthesis in the Soft Coral Gersemia-Fruticosa. Tetrahedron Lett 35: 8267–8270. doi: 10.1016/0040-4039(94)88299-1
[28]  Koljak R, Boutaud O, Shieh BH, Samel N, Brash AR (1997) Identification of a naturally occurring peroxidase-lipoxygenase fusion protein. Science 277: 1994–1996. doi: 10.1126/science.277.5334.1994
[29]  Koljak R, Jarving I, Kurg R, Boeglin WE, Varvas K, et al. (2001) The basis of prostaglandin synthesis in coral: molecular cloning and expression of a cyclooxygenase from the Arctic soft coral Gersemia fruticosa. J Biol Chem 276: 7033–7040. doi: 10.1074/jbc.m009803200
[30]  Valmsen K, Boeglin WE, Jarving I, Schneider C, Varvas K, et al. (2004) Structural and functional comparison of 15S- and 15R-specific cyclooxygenases from the coral Plexaura homomalla. European Journal of Biochemistry 271: 3533–3538. doi: 10.1111/j.0014-2956.2004.04289.x
[31]  Mortimer M, Jarving R, Brash AR, Samel N, Jarving I (2006) Identification and characterization of an arachidonate 11R-lipoxygenase. Arch Biochem Biophys 445: 147–155. doi: 10.1016/j.abb.2005.10.023
[32]  Lohelaid H, Jarving R, Valmsen K, Varvas K, Kreen M, et al. (2008) Identification of a functional allene oxide synthase-lipoxygenase fusion protein in the soft coral Gersemia fruticosa suggests the generality of this pathway in octocorals. Biochim Biophys Acta 1780: 315–321. doi: 10.1016/j.bbagen.2007.10.010
[33]  Lee DS, Nioche P, Hamberg M, Raman CS (2008) Structural insights into the evolutionary paths of oxylipin biosynthetic enzymes. Nature 455: 363–368. doi: 10.1038/nature07307
[34]  Corey EJ, Washburn WN, Chen JC (1973) Studies on the prostaglandin A 2 synthetase complex from Plexaura homomalla. J Am Chem Soc 95: 2054–2055. doi: 10.1021/ja00787a079
[35]  Corey EJ, Lansbury PT, Yamada Y (1985) Identification of a New Eicosanoid from Invitro Biosynthetic Experiments with Clavularia-Viridis - Implications for the Biosynthesis of Clavulones. Tetrahedron Letters 26: 4171–4174. doi: 10.1016/s0040-4039(00)98982-2
[36]  Varvas K, Jarving I, Koljak R, Vahemets A, Pehk T, et al. (1993) Invitro Biosynthesis of Prostaglandins in the White Sea Soft Coral Gersemia-Fruticosa - Formation of Optically-Active Pgd2, Pge2, Pgf2-Alpha and 15-Keto-Pgf2-Alpha from Arachidonic-Acid. Tetrahedron Letters 34: 3643–3646. doi: 10.1016/s0040-4039(00)73658-6
[37]  Corey EJ, Dalarcao M, Matsuda SPT, Lansbury PT, Yamada Y (1987) Intermediacy of 8-(R)-Hpete in the Conversion of Arachidonic-Acid to Pre-Clavulone-a by Clavularia-Viridis - Implications for the Biosynthesis of Marine Prostanoids. J Am Chem Soc 109: 289–290. doi: 10.1021/ja00235a053
[38]  Varvas K, Jarving I, Koljak R, Valmsen K, Brash AR, et al. (1999) Evidence of a cyclooxygenase-related prostaglandin synthesis in coral. The allene oxide pathway is not involved in prostaglandin biosynthesis. J Biol Chem 274: 9923–9929. doi: 10.1074/jbc.274.15.9923
[39]  Hashimoto N, Fujiwara S, Watanabe K, Iguchi K, Tsuzuki M (2003) Localization of clavulones, prostanoids with antitumor activity, within the Okinawan soft coral Clavularia viridis (Alcyonacea, Clavulariidae): Preparation of a high-purity Symbiodinium fraction using a protease and a detergent. Lipids 38: 991–997. doi: 10.1007/s11745-003-1153-2
[40]  Pawlik JR, Burch MT, Fenical W (1987) Patterns of Chemical Defense among Caribbean Gorgonian Corals - a Preliminary Survey. Journal of Experimental Marine Biology and Ecology 108: 55–66. doi: 10.1016/0022-0981(87)90130-4
[41]  Gerhart DJ (1991) Emesis, Learned Aversion, and Chemical Defense in Octocorals - a Central Role for Prostaglandins. American Journal of Physiology 260: R839–R843.
[42]  O'Neal W, Pawlik JR (2002) A reappraisal of the chemical and physical defenses of Caribbean gorgonian corals against predatory fishes. Marine Ecology Progress Series 240: 117–126. doi: 10.3354/meps240117
[43]  Whalen KE, Starczak VR, Nelson DR, Goldstone JV, Hahn ME (2010) Cytochrome P450 diversity and induction by gorgonian allelochemicals in the marine gastropod Cyphoma gibbosum. BMC Ecol 10: 24. doi: 10.1186/1472-6785-10-24
[44]  Su X, Gibor A (1988) A method for RNA isolation from marine macro-algae. Anal Biochem 174: 650–657. doi: 10.1016/0003-2697(88)90068-1
[45]  Rodriguez-Lanetty M, Phillips WS, Dove S, Hoegh-Guldberg O, Weis VM (2008) Analytical approach for selecting normalizing genes from a cDNA microarray platform to be used in q-RT-PCR assays: a cnidarian case study. J Biochem Biophys Methods 70: 985–991. doi: 10.1016/j.jbbm.2007.08.005
[46]  Livak KJ, Schmittgen TD (2001) Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2?ΔΔCT Method. Methods 25: 402–408. doi: 10.1006/meth.2001.1262
[47]  Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30: e36. doi: 10.1093/nar/30.9.e36
[48]  Coffa G, Schneider C, Brash AR (2005) A comprehensive model of positional and stereo control in lipoxygenases. Biochem Biophys Res Commun 338: 87–92. doi: 10.1016/j.bbrc.2005.07.185
[49]  Proksch E, Brandner JM, Jensen J-M (2008) The skin: an indispensable barrier. Experimental Dermatology 17: 1063–1072. doi: 10.1111/j.1600-0625.2008.00786.x
[50]  Rodriguez PG, Felix FN, Woodley DT, Shim EK (2008) The role of oxygen in wound healing: a review of the literature. Dermatol Surg 34: 1159–1169. doi: 10.1111/j.1524-4725.2008.34254.x
[51]  Ariel A, Timor O (2013) Hanging in the balance: endogenous anti-inflammatory mechanisms in tissue repair and fibrosis. The Journal of Pathology 229: 250–263. doi: 10.1002/path.4108
[52]  Cordeiro JV, Jacinto A (2013) The role of transcription-independent damage signals in the initiation of epithelial wound healing. Nature Reviews Molecular Cell Biology 14: 249–262. doi: 10.1038/nrm3541
[53]  Wenemoser D, Lapan SW, Wilkinson AW, Bell GW, Reddien PW (2012) A molecular wound response program associated with regeneration initiation in planarians. Genes Dev 26: 988–1002. doi: 10.1101/gad.187377.112
[54]  Leon J, Rojo E, Sanchez-Serrano JJ (2001) Wound signalling in plants. J Exp Bot 52: 1–9.
[55]  Maffei ME, Mith?fer A, Boland W (2007) Before gene expression: early events in plant–insect interaction. Trends in Plant Science 12: 310–316. doi: 10.1016/j.tplants.2007.06.001
[56]  Kombrink E (2012) Chemical and genetic exploration of jasmonate biosynthesis and signaling paths. Planta 236: 1351–1366. doi: 10.1007/s00425-012-1705-z
[57]  Wasternack C, Hause B (2013) Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Annals of Botany 111: 1021–1058.
[58]  Bell E, Creelman RA, Mullet JE (1995) A chloroplast lipoxygenase is required for wound-induced jasmonic acid accumulation in Arabidopsis. Proc Natl Acad Sci U S A 92: 8675–8679. doi: 10.1073/pnas.92.19.8675
[59]  Glauser G, Dubugnon L, Mousavi SAR, Rudaz S, Wolfender JL, et al. (2009) Velocity Estimates for Signal Propagation Leading to Systemic Jasmonic Acid Accumulation in Wounded Arabidopsis. Journal of Biological Chemistry 284: 34506–34513. doi: 10.1074/jbc.m109.061432
[60]  Schommer C, Palatnik JF, Aggarwal P, Chetelat A, Cubas P, et al. (2008) Control of jasmonate biosynthesis and senescence by miR319 targets. Plos Biology 6: 1991–2001. doi: 10.1371/journal.pbio.0060230
[61]  Laudert D, Pfannschmidt U, Lottspeich F, Hollander-Czytko H, Weiler EW (1996) Cloning, molecular and functional characterization of Arabidopsis thaliana allene oxide synthase (CYP 74), the first enzyme of the octadecanoid pathway to jasmonates. Plant Mol Biol 31: 323–335. doi: 10.1007/bf00021793
[62]  Bate NJ, Sivasankar S, Moxon C, Riley JM, Thompson JE, et al. (1998) Molecular characterization of an Arabidopsis gene encoding hydroperoxide lyase, a cytochrome P-450 that is wound inducible. Plant Physiol 117: 1393–1400. doi: 10.1104/pp.117.4.1393
[63]  Song WC, Funk CD, Brash AR (1993) Molecular cloning of an allene oxide synthase: a cytochrome P450 specialized for the metabolism of fatty acid hydroperoxides. Proc Natl Acad Sci U S A 90: 8519–8523. doi: 10.1073/pnas.90.18.8519
[64]  Howe GA, Lee GI, Itoh A, Li L, DeRocher AE (2000) Cytochrome P450-dependent metabolism of oxylipins in tomato. Cloning and expression of allene oxide synthase and fatty acid hydroperoxide lyase. Plant Physiol 123: 711–724. doi: 10.1104/pp.123.2.711
[65]  Vick BA, Zimmerman DC (1987) Pathways of Fatty-Acid Hydroperoxide Metabolism in Spinach Leaf Chloroplasts. Plant Physiology 85: 1073–1078. doi: 10.1104/pp.85.4.1073
[66]  Grechkin AN, Hamberg M (2004) The “heterolytic hydroperoxide lyase” is an isomerase producing a short-lived fatty acid hemiacetal. Biochimica Et Biophysica Acta-Molecular and Cell Biology of Lipids 1636: 47–58. doi: 10.1016/j.bbalip.2003.12.003
[67]  Halitschke R, Ziegler J, Kein?nen M, Baldwin IT (2004) Silencing of hydroperoxide lyase and allene oxide synthase reveals substrate and defense signaling crosstalk in Nicotiana attenuata. The Plant Journal 40: 35–46. doi: 10.1111/j.1365-313x.2004.02185.x
[68]  Boutaud O, Brash AR (1999) Purification and catalytic activities of the two domains of the allene oxide synthase-lipoxygenase fusion protein of the coral Plexaura homomalla. J Biol Chem 274: 33764–33770. doi: 10.1074/jbc.274.47.33764

Full-Text

Contact Us

service@oalib.com

QQ:3279437679

WhatsApp +8615387084133