Abstract
Polycyclic aromatic hydrocarbons (PAHs) are the most persistent organic pollutants in worldwide aquatic environments. The extensive isolation of genes responsive to PAH pollution in soft coral (Scleronephthya gracillimum) is described herein. Soft coral colonies were exposed to 100 μg/L of a standard mixture of PAHs. Gene candidates with transcript levels that changed in response to PAH exposure were identified by differential display polymerase chain reaction (DD-PCR). There were 37 types of candidate genes identified, of which 20 were upregulated in expression and 17 were downregulated. The functions of the genes identified included oxidative stress response, ribosomal structure maintenance, molecular chaperone activity, protein kinase activation and tumorigenesis, defense mechanisms, transcription, and other biological responses. mRNA quantification was carried out using real-time quantitative PCR in eight selected genes: cytosolic malate dehydrogenase, protein disulfide isomerase, ribosomal protein L6, ral guanine nucleotide dissociation stimulator-like 1, poly(ADP-ribose) polymerase 4, peptidylglycine α-hydroxylating monooxygenase, a disintegrin and metalloproteinase (ADAM) metallopeptidase protein, and eukaryotic initiation factor 4 gamma 3. Changes in transcript levels were consistent with DD-PCR results. The gene candidates isolated in this study were differentially expressed and therefore have potential as molecular biomarkers for understanding coral responses to environmental stressors.
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.References
Akcha F, Izuel C, Venier P, Budzinski H, Burgeot T, Narbonne J (2000) Enzymatic biomarker measurement and study of DNA adduct formation in benzo. Aquat Toxicol 49:269–287
Alvarez J, Hamplova J, Hohaus A, Morano I, Haase H, Vassort G (2004) Calcium current in rat cardiomyocytes is modulated by the carboxyl-terminal ahnak domain. J Biol Chem 279:12456–12461
Arnold J, Grune T (2002) PARP-mediated proteasome activation: a co-ordination of DNA repair and protein degradation? Bioessays 24:1060–1065
Baird AH, Bhagooli R, Ralph PJ, Takahashi S (2009) Coral bleaching: the role of the host. Trends Ecol Evol 24:16–20
Balk L, Hylland K, Hansson T, Berntssen MH, Beyer J, Jonsson G, Melbye A, Grung M, Torstensen BE, Borseth JF, Skarphedinsdottir H, Klungsoyr J (2011) Biomarkers in natural fish populations indicate adverse biological effects of offshore oil production. PLoS One 6:e19735
Blobel CP (1997) Metalloprotease-disintegrins: links to cell adhesion and cleavage of TNF alpha and Notch. Cell 90:589–592
Bond JS, Beynon RJ (1995) The astacin family of metalloendopeptidases. Protein Sci 4:1247–1261
Butler JS, Lee JH, Skalnik DG (2008) CFP1 interacts with DNMT1 independently of association with the Setd1 histone H3K4 methyltransferase complexes. DNA Cell Biol 27:533–543
Carafoli E (2003) Historical review: mitochondria and calcium: ups and downs of an unusual relationship. Trends Biochem Sci 28:175–181
Cheikyula JO, Koyama J, Uno S (2008) Comparative study of bioconcentration and EROD activity induction in the Japanese flounder, red sea bream, and Java medaka exposed to polycyclic aromatic hydrocarbons. Environ Toxicol 23:354–362
Chin D, Means AR (2000) Calmodulin: a prototypical calcium sensor. Trends Cell Biol 10:322–328
Ciocca DR, Calderwood SK (2005) Heat shock proteins in cancer: diagnostic, prognostic, predictive, and treatment implications. Cell Stress Chaperones 10:86–103
Costanza R, d'Arge R, de Groot R, Farber S, Grasso M, Hannon B, Limburg K, Naeem S, O'Neill RV, Paruelo J, Raskin RG, Sutton P, van den Belt M (1997) The value of the world's ecosystem services and natural capital. Nature 387:253–260
Davila DR, Davis DP, Campbell K, Cambier JC, Zigmond LA, Burchiel SW (1995) Role of alterations in Ca(2+)-associated signaling pathways in the immunotoxicity of polycyclic aromatic hydrocarbons. J Toxic Environ Health 45:101–126
del Arco A, Satrustegui J (1998) Molecular cloning of Aralar, a new member of the mitochondrial carrier superfamily that binds calcium and is present in human muscle and brain. J Biol Chem 273:23327–23334
Downs CA, Fauth JE, Halas JC, Dustan P, Bemiss J, Woodley CM (2002) Oxidative stress and seasonal coral bleaching. Free Radic Biol Med 33:533–543
Duchen MR (2000) Mitochondria and calcium: from cell signalling to cell death. J Physiol 529(Pt 1):57–68
Finlin BS, Gau CL, Murphy GA, Shao H, Kimel T, Seitz RS, Chiu YF, Botstein D, Brown PO, Der CJ, Tamanoi F, Andres DA, Perou CM (2001) RERG is a novel ras-related, estrogen-regulated and growth-inhibitory gene in breast cancer. J Biol Chem 276:42259–42267
Gruber CW, Cemazar M, Heras B, Martin JL, Craik DJ (2006) Protein disulfide isomerase: the structure of oxidative folding. Trends Biochem Sci 31:455–464
Hershko A, Ciechanover A (1998) The ubiquitin system. Annu Rev Biochem 67:425–479
Hochstrasser M (1996) Ubiquitin-dependent protein degradation. Annu Rev Genet 30:405–439
Hoeflich KP, Ikura M (2002) Calmodulin in action: diversity in target recognition and activation mechanisms. Cell 108:739–742
Hohaus A, Person V, Behlke J, Schaper J, Morano I, Haase H (2002) The carboxyl-terminal region of ahnak provides a link between cardiac L-type Ca2+ channels and the actin-based cytoskeleton. FASEB J 16:1205–1216
Huang Y, Laval SH, van Remoortere A, Baudier J, Benaud C, Anderson LV, Straub V, Deelder A, Frants RR, den Dunnen JT, Bushby K, van der Maarel SM (2007) AHNAK, a novel component of the dysferlin protein complex, redistributes to the cytoplasm with dysferlin during skeletal muscle regeneration. FASEB J 21:732–742
Hubert RS, Vivanco I, Chen E, Rastegar S, Leong K, Mitchell SC, Madraswala R, Zhou Y, Kuo J, Raitano AB, Jakobovits A, Saffran DC, Afar DE (1999) STEAP: a prostate-specific cell-surface antigen highly expressed in human prostate tumors. Proc Natl Acad Sci U S A 96:14523–14528
Hwang IT, Kim YJ, Kim SH, Kwak CI, Gu YY, Chun JY (2003) Annealing control primer system for improving specificity of PCR amplification. Biotechniques 35:1180–1184
Key MD, Andres DA, Der CJ, Repasky GA (2006) Characterization of RERG: an estrogen-regulated tumor suppressor gene. Methods Enzymol 407:513–527
Kim YJ, Kwak CI, Gu YY, Hwang IT, Chun JY (2004) Annealing control primer system for identification of differentially expressed genes on agarose gels. Biotechniques 36:424–426, 428, 430 passim
Knigge T, Monsinjon T, Andersen OK (2004) Surface-enhanced laser desorption/ionization-time of flight-mass spectrometry approach to biomarker discovery in blue mussels (Mytilus edulis) exposed to polyaromatic hydrocarbons and heavy metals under field conditions. Proteomics 4:2722–2727
Kolhekar AS, Keutmann HT, Mains RE, Quon AS, Eipper BA (1997) Peptidylglycine alpha-hydroxylating monooxygenase: active site residues, disulfide linkages, and a two-domain model of the catalytic core. Biochemistry 36:10901–10909
Koljak R, Boutaud O, Shieh BH, Samel N, Brash AR (1997) Identification of a naturally occurring peroxidase-lipoxygenase fusion protein. Science 277:1994–1996
Lee IH, Lim HJ, Yoon S, Seong JK, Bae DS, Rhee SG, Bae YS (2008) Ahnak protein activates protein kinase C (PKC) through dissociation of the PKC-protein phosphatase 2A complex. J Biol Chem 283:6312–6320
Lee JH, Skalnik DG (2005) CpG-binding protein (CXXC finger protein 1) is a component of the mammalian Set1 histone H3-Lys4 methyltransferase complex, the analogue of the yeast Set1/COMPASS complex. J Biol Chem 280:41725–41731
Lesser MP (2006) Oxidative stress in marine environments: biochemistry and physiological ecology. Annu Rev Physiol 68:253–278
Liang P, Pardee AB (1992) Differential display of eukaryotic messenger RNA by means of the polymerase chain reaction. Science 257:967–971
Liang P, Averboukh L, Pardee AB (1993) Distribution and cloning of eukaryotic mRNAs by means of differential display: refinements and optimization. Nucleic Acids Res 21:3269–3275
Liang P, Zhu W, Zhang X, Guo Z, O'Connell RP, Averboukh L, Wang F, Pardee AB (1994) Differential display using one-base anchored oligo-dT primers. Nucleic Acids Res 22:5763–5764
Mentlein R (1999) Dipeptidyl-peptidase IV (CD26)—role in the inactivation of regulatory peptides. Regul Pept 85:9–24
Mohrlen F, Maniura M, Plickert G, Frohme M, Frank U (2006) Evolution of astacin-like metalloproteases in animals and their function in development. Evol Dev 8:223–231
Moreto J, Vidal-Quadras M, Pol A, Santos E, Grewal T, Enrich C, Tebar F (2009) Differential involvement of H- and K-Ras in Raf-1 activation determines the role of calmodulin in MAPK signaling. Cell Signal 21:1827–1836
Nii CM, Muscatine L (1997) Oxidative stress in the symbiotic sea anemone Aiptasia pulchella (Carigen, 1943): contribution of the animal to superoxide ion production at elevated temperature. Biol Bull 192:444–456
Ohgami RS, Campagna DR, McDonald A, Fleming MD (2006) The Steap proteins are metalloreductases. Blood 108:1388–1394
Pan JS, He SZ, Xu HZ, Zhan XJ, Yang XN, Xiao HM, Shi HX, Ren JL (2008) Oxidative stress disturbs energy metabolism of mitochondria in ethanol-induced gastric mucosa injury. World J Gastroenterol 14:5857–5867
Primakoff P, Myles DG (2000) The ADAM gene family: surface proteins with adhesion and protease activity. Trends Genet 16:83–87
Reynaud S, Deschaux P (2006) The effects of polycyclic aromatic hydrocarbons on the immune system of fish: a review. Aquat Toxicol 77:229–238
Robinson PA, Ardley HC (2004) Ubiquitin-protein ligases. J Cell Sci 117:5191–5194
Ryu CH, Kim SW, Lee KH, Lee JY, Kim H, Lee WK, Choi BH, Lim Y, Kim YH, Hwang TK, Jun TY, Rha HK (2005) The merlin tumor suppressor interacts with Ral guanine nucleotide dissociation stimulator and inhibits its activity. Oncogene 24:5355–5364
Schwarz JA, Mitchelmore CL, Jones R, O'Dea A, Seymour S (2013) Exposure to copper induces oxidative and stress responses and DNA damage in the coral Montastraea franksi. Comp Biochem Physiol C Toxicol Pharmacol 157:272–279
Sharrocks AD, Brown AL, Ling Y, Yates PR (1997) The ETS-domain transcription factor family. Int J Biochem Cell Biol 29:1371–1387
Sharrocks AD (2001) The ETS-domain transcription factor family. Nat Rev Mol Cell Biol 2:827–837
Simbulan-Rosenthal CM, Rosenthal DS, Iyer S, Boulares AH, Smulson ME (1998) Transient poly(ADP-ribosyl)ation of nuclear proteins and role of poly(ADP-ribose) polymerase in the early stages of apoptosis. J Biol Chem 273:13703–13712
Sivasankar S, Sheldrick B, Rothstein SJ (2000) Expression of allene oxide synthase determines defense gene activation in tomato. Plant Physiol 122:1335–1342
Song M-K Y-JK, Song M, Choi H-S, Ryu J-C (2011) Dose–response functional gene analysis by exposure to 3 different polycyclic aromatic hydrocarbons in human hepatocytes. Mol Cell Toxicol 7:221–232
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
Tate CM, Lee JH, Skalnik DG (2009) CXXC finger protein 1 contains redundant functional domains that support embryonic stem cell cytosine methylation, histone methylation, and differentiation. Mol Cell Biol 29:3817–3831
Turner MW (2003) The role of mannose-binding lectin in health and disease. Mol Immunol 40:423–429
Valenti MT, Dalle Carbonare L, Donatelli L, Bertoldo F, Giovanazzi B, Caliari F, Lo Cascio V (2009) STEAP mRNA detection in serum of patients with solid tumours. Cancer Lett 273:122–126
van der Oost R, Beyer J, Vermeulen NP (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13:57–149
Warshawsky D, Cody T, Radike M, Reilman R, Schumann B, LaDow K, Schneider J (1995) Biotransformation of benzo[a]pyrene and other polycyclic aromatic hydrocarbons and heterocyclic analogs by several green algae and other algal species under gold and white light. Chem Biol Interact 97:131–148
Wasylyk B, Hagman J, Gutierrez-Hartmann A (1998) Ets transcription factors: nuclear effectors of the Ras-MAP-kinase signaling pathway. Trends Biochem Sci 23:213–216
Weis VM (2008) Cellular mechanisms of cnidarian bleaching: stress causes the collapse of symbiosis. J Exp Biol 211:3059–3066
White MA, Vale T, Camonis JH, Schaefer E, Wigler MH (1996) A role for the Ral guanine nucleotide dissociation stimulator in mediating Ras-induced transformation. J Biol Chem 271:16439–16442
Wilkinson B, Gilbert HF (2004) Protein disulfide isomerase. Biochim Biophys Acta 1699:35–44
Woo S, Yum S, Yoon M, Kim SH, Lee J, Kim JH, Lee TK (2005) Efficient isolation of intact RNA from the soft coral Scleronephthya gracillimum (Kükenthal) for gene expression analyses. Integr Biosci 9:205–209
Woo S, Yum S, Park HS, Lee TK, Ryu JC (2009) Effects of heavy metals on antioxidants and stress-responsive gene expression in Javanese medaka (Oryzias javanicus). Comp Biochem Physiol C Toxicol Pharmacol 149:289–299
Woo S, Jeon H, Lee J, Song J-I, Park H-S, Yum S (2010) Isolation of hyperthermal stress responsive genes in soft coral (Scleronephthya gracillimum). Mol Cell Toxicol 4:387–393
Yahara I (1996) Stress-inducible cellular responses. Introduction. EXS 77:XI–XII
Acknowledgments
This subject was supported by “Marine and Extreme Genome Research Center Program” of the Ministry of Oceans and Fisheries, Republic of Korea to SY (KIOST project no. PM57372), and the Korea Institute of Ocean Science and Technology project (PE99152).
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Philippe Garrigues
Rights and permissions
About this article
Cite this article
Woo, S., Lee, A., Denis, V. et al. Transcript response of soft coral (Scleronephthya gracillimum) on exposure to polycyclic aromatic hydrocarbons. Environ Sci Pollut Res 21, 901–910 (2014). https://doi.org/10.1007/s11356-013-1958-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-013-1958-5