Molecular characterization and mRNA expression of two key enzymes of hypoxia-sensing pathways in eastern oysters Crassostrea virginica (Gmelin): Hypoxia-inducible factor α (HIF-α) and HIF-prolyl hydroxylase (PHD)

Comparative Biochemistry and Physiology - Part D: Genomics and Proteomics

Volumn 6, Issue 2, 2011, Pages 103-114

  Piontkivska, Helen ^c   Chung, J Sook ^b   Ivanina, Anna V ^a   Sokolov, Eugene P ^d   Techa, Sirinart ^b   Sokolova, Inna M ^a  

^a UNIVERSITY OF NORTH CAROLINA AT CHARLOTTE   (United States)

^b UNIVERSITY OF MARYLAND   (United States)

^c KENT STATE UNIVERSITY   (United States)

^d CAROLINAS MEDICAL CENTER   (United States)

Author keywords

Evolution; Expression; Hypoxia inducible factor; Intertidal mollusk; Oxygen sensing

Indexed keywords

CADMIUM; HYPOXIA INDUCIBLE FACTOR; HYPOXIA INDUCIBLE FACTOR ALPHA; HYPOXIA INDUCIBLE FACTOR PROLYLHYDROXYLASE; MESSENGER RNA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANOXIA; ARTICLE; CHEMICAL STRUCTURE; CRASSOSTREA VIRGINICA; GENETIC VARIABILITY; HOMOLOGOUS RECOMBINATION; HYPOXIA; MOLECULAR DYNAMICS; NONHUMAN; NUCLEOTIDE SEQUENCE; OXYGEN SENSING; OYSTER; PHYLOGENY; PRIORITY JOURNAL;

ANIMALIA; CRASSOSTREA VIRGINICA; INVERTEBRATA; METAZOA; MOLLUSCA; OSTREIDAE; VERTEBRATA;

EID: 79956369500     PISSN: 1744117X     EISSN: 18780407     Source Type: Journal    
DOI: 10.1016/j.cbd.2010.10.003     Document Type: Article

References (77)

1. Anisimova, M., Gascuel, O., 2006. Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Syst. Biol. 55, 539-552.
2. Appelhoff, R.J., Tian, Y.M., Raval, R.R., Turley, H., Harris, A.L., Pugh, C.W., Ratcliffe, P.J., Gleadle, J.M., 2004. Differential function of the prolyl hydroxylases PHD1, PHD2, and PHD3 in the regulation of hypoxia-inducible factor. J. Biol. Chem. 279, 38458-38465.
3. Aprelikova, O., Chandramouli, G.V.R., Wood, M., Vasselli, J.R., Riss, J., Maranchie, J.K., Linehan, W.M., Barrett, J.C., 2004. Regulation of HIF prolyl hydroxylases by hypoxia-inducible factors. J. Cell. Biochem. 92, 491-501.
4. Aragones, J., Fraisl, P., Baes, M., Carmeliet, P., 2009. Oxygen sensors at the crossroad of metabolism. Cell Metab. 9, 11-22.
5. Aravind, L., Koonin, E.V., 2001. The DNA-repair protein AlkB, EGL-9, and leprecan define new families of 2-oxoglutarate- and iron-dependent dioxygenases. Genome Biol. 2 RESEARCH0007.
6. Belaidi, E., Beguin, P.C., Levy, P., Ribuot, C., Godin, G.-R., 2008. Prevention of HIF-1 activation and iNOS gene targeting by low-dose cadmium results in loss of myocardial hypoxic preconditioning in the rat. Am. J. Physiol. Heart Circ. Physiol. 294, H901-H908.
7. Benizri, E., Ginouvès, A., Berra, E., 2008. The magic of the hypoxia-signaling cascade. Cell. Mol. Life Sci. 65, 1133-1149.
8. Benson, D.A., Karsch-Mizrachi, I., Lipman, D.J., Ostell, J., Wheeler, D.L., 2007. GenBank. Nucleic Acids Res. 35, D21-D25. (Pubitemid 46056163)
9. Berra, E., Benizri, E., Ginouvès, A., Volmat, V., Roux, D., Pouysségur, J., 2003. HIF prolylhydroxylase 2 is the key oxygen sensor setting low steady-state levels of HIF-1alpha in normoxia. EMBO J. 22, 4082-4090. (Pubitemid 37021737)
10. Brinkhoff, W., Stockmann, K., Grieshaber, M., 1983. Natural occurrence of anaerobiosis in molluscs from intertidal habitats. Oecologia 57, 151-155. (Pubitemid 15274172)
11. Bruick, R.K., McKnight, S.L., 2002. Transcription. Oxygen sensing gets a second wind. Science 295, 807-808.
12. Cao, Y.B., Chen, X.Q., Wang, S., Wang, Y.X., Du, J.Z., 2008. Evolution and regulation of the downstream gene of hypoxia-inducible factor-1alpha in naked carp (Gymnocypris przewalskii) from Lake Qinghai, China. J. Mol. Evol. 67, 570-580.
13. Cherkasov, A.S., Ringwood, A.H., Sokolova, I.M., 2006. Effects of cadmium exposure on mitochondrial function are modulated by acclimation temperature in eastern oysters Crassostrea virginica Gmelin (Bivalvia: Ostreidae). Environ. Toxicol. Chem. 25, 2461-2469.
14. Chun, Y.-S., Choi, E., Kim, G.-T., Choi, H., Kim, C.-H., Lee, M.-J., Kim, M.-S., Park, J.-W., 2000. Cadmium blocks hypoxia-inducible factor (HIF)-1-mediated response to hypoxia by stimulating the proteasome-dependent degradation of HIF-1α. Eur. J. Biochem. 267, 4198-4204.
15. Crompton T.R. (1997) Toxicants in aqueous ecosystem John Wiley and Sons, Chichester, New York, Weinheim, Brisbane, Singapore, Toronto
16. D'Angelo, G., Duplan, E., Boyer, N., Vigne, P., Frelin, C., 2003. Hypoxia up-regulates prolyl hydroxylase activity. J. Biol. Chem. 278, 38183-38187.
17. Dayhoff, M., Schwartz, R., Orcutt, B., 1978. A model of evolutionary change in proteins. In: Dayhoff, M. (Ed.), Atlas of Protein Sequence and Structure. Volume 5., Washington, DC., Natl. Biomed. Res. Found, pp. 345-352.
18. Edgar, R.C., 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797. (Pubitemid 38832724)
19. Felsenstein, J., 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783-791.
20. Finn, R.D., Tate, J., Mistry, J., Coggill, P.C., Sammut, J.S., Hotz, H.R., Ceric, G., Forslund, K., Eddy, S.R., Sonnhammer, E.L., Bateman, A., 2008. The Pfam protein families database. Nucleic Acids Res. 36, D281-D288. (Pubitemid 351149737)
21. Frew, R.D., Hunter, K.A., Beyer, R., 1997. Cadmium in oysters and sediments from Foveaux Strait, New Zealand. In: Macaskill, R.B. (Ed.), Proceedings of the Trace Element Group of New Zealand. Waikato University Press, pp. 1-23.
22. GESAMP, 1987. Land-sea boundary flux of contaminants: contributions from rivers. Group of experts on the scientific aspects of marine environmental protection (GESAMP). Reports and Studies 32, 1-172.
23. Ginouvès, A., Ilc, K., Macías, N., Pouysségur, J., Berra, E., 2008. PHDs overactivation during chronic hypoxia " desensitizes" HIFα and protects cells from necrosis. Proc. Nat. Acad. Sci. 105, 4745-4750. doi:10.1073/pnas.0705680105.
24. Gorr, T.A., Gassmann, M., Wappner, P., 2006. Sensing and responding to hypoxia via HIF in model invertebrates. J. Insect Physiol. 52, 349-364.
25. Gu, Y.Z., Moran, S.M., Hogenesch, J.B., Wartman, L., Bradfield, C.A., 1998. Molecular characterization and chromosomal localization of a third alpha-class hypoxia inducible factor subunit, HIF3alpha. Gene Expr. 7, 205-213. (Pubitemid 28527216)
26. Gu, Y.Z., Hogenesch, J.B., Bradfield, C.A., 2000. The PAS superfamily: sensors of environmental and developmental signals. Annu. Rev. Pharmacol. Toxicol. 40, 519-561.
27. Guindon, S., Gascuel, O., 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52, 696-704.
28. Hackney, C.T., Grimley, J., Posey, M., Alphin, T., Hyland, J., 1998. Sediment contamination in North Carolina's estuaries. Publication # 198 of the Center For Marine Science Research, University of North Carolina at Wilmington. 2-59.
29. Hedges, B.S., Kumar, S., 2003. Genomic clocks and evolutionary timescales. Trends Genet. 19, 200-206. (Pubitemid 36398422)
30. Heerden, D.v., Vosloo, A., Nikinmaa, M., 2004. Effects of short-term copper exposure on gill structure, metallothionein and hypoxia-inducible factor-1[alpha] (HIF-1 [alpha]) levels in rainbow trout (Oncorhynchus mykiss). Aquat. Toxicol. 69, 271-280.
31. Heidbreder, M., Frohlich, F., Johren, O., Dendorfer, A., Qadri, F., Dominiak, P., 2003. Hypoxia rapidly activates HIF-3α mRNA expression. The FASEB Journal express article. doi:10.1096/fj.02-0963fje.
32. Heise, K., Puntarulo, S., Nikinmaa, M., Abele, D., Portner, H.-O., 2006a. Oxidative stress during stressful heat exposure and recovery in the North Sea eelpout Zoarces viviparus L. J. Exp. Biol. 209, 353-363. doi:10.1242/jeb.01977.
33. Heise, K., Puntarulo, S., Nikinmaa, M., Lucassen, M., Pörtner, H.-O., Abele, D., 2006b. Oxidative stress and HIF-1 DNA binding during stressful cold exposure and recovery in the North Sea eelpout (Zoarces viviparus). Comp. Biochem. Physiol. A 143, 494-503.
34. Heise, K., Estevez, M., Puntarulo, S., Galleano, M., Nikinmaa, M., Pörtner, H., Abele, D., 2007. Effects of seasonal and latitudinal cold on oxidative stress parameters and activation of hypoxia inducible factor (HIF-1) in zoarcid fish. J. Comp. Physiol. B 177, 765-777.
35. Hochachka, P.W., Rupert, J.L., Goldenberg, L., Gleave, M., Kozlowski, P., 2002. Going malignant: the hypoxia-cancer connection in the prostate. BioEssays 24, 749-757. (Pubitemid 34850332)
36. Hoogewijs, D., Terwilliger, N.B., Webster, K.A., Powell-Coffman, J.A., Tokishita, S., Yamagata, H., Hankein, T., Burmester, T., Rytkönen, K.T., Nikinmaa, M., Abele, D., Heise, K., Lucassen, M., Fandrey, J., Maxwell, P.H., Påhlman, S., Gorr, T.A., 2007. From critters to cancers: bridging comparative and clinical research on oxygen sensing, HIF signaling, and adaptations towards hypoxia. Integr CompBiol 1-26.
37. Horiguchi, H., Kayama, F., Oguma, E., Willmore, W.G., Hradecky, P., Bunn, H.F., 2000. Cadmium and platinum suppression of erythropoietin production in cell culture: clinical implications. Blood 96, 3743-3747.
38. Hubbard, T.J., Aken, B.L., Beal, K., Ballester, B., Caccamo, M., Chen, Y., Clarke, L., Coates, G., Cunningham, F., Cutts, T., Down, T., Dyer, S.C., Fitzgerald, S., Fernandez-Banet, J., Graf, S., Haider, S., Hammond, M., Herrero, J., Holland, R., Howe, K., Johnson, N., Kahari, A., Keefe, D., Kokocinski, F., Kulesha, E., Lawson, D., Longden, I., Melsopp, C., Megy, K., Meidl, P., Ouverdin, B., Parker, A., Prlic, A., Rice, S., Rios, D., Schuster, M., Sealy, I., Severin, J., Slater, G., Smedley, D., Spudich, G., Trevanion, S., Vilella, A., Vogel, J., White, S., Wood, M., Cox, T., Curwen, V., Durbin, R., Fernandez-Suarez, X.M., Flicek, P., Kasprzyk, A., Proctor, G., Searle, S., Smith, J., Ureta-Vidal, A., Birney, E., 2007. Ensembl 2007. Nucleic Acids Res. 35, D610-D617. (Pubitemid 46056279)
39. Ivanina, A.V., Eilers, S., Kurochkin, I.O., Chung, J.S., Techa, S., Piontkivska, H., Sokolov, E.P., Sokolova, I.M., 2010. Effects of cadmium exposure and intermittent anoxia on nitric oxide metabolism in eastern oysters, Crassostrea virginica. J. Exp. Biol. 213, 433-444. doi:10.1242/jeb.038059.
40. Jiang, H., Guo, R., Powell-Coffman, J.A., 2001. The Caenorhabditis elegans hif-1 gene encodes a bHLH-PAS protein that is required for adaptation to hypoxia. Proc. Natl Acad. Sci. USA 98, 7916-7921.
41. Ke, Q., Costa, M., 2006. Hypoxia-Inducible Factor-1 (HIF-1). Mol. Pharmacol. 70, 1469-1480.
42. Kurochkin, I.O., Ivanina, A.V., Eilers, S., Downs, C.A., May, L.A., Sokolova, I.M., 2009. Cadmium affects metabolic responses to prolonged anoxia and reoxygenation in eastern oysters Crassostrea virginica. Am. J. Physiol. Regul. Integr. Comp. Physiol. 297, R1262-R1272.
43. Lahiri, S., Roy, A., Baby, S.M., Hoshi, T., Semenza, G.L., Prabhakar, N.R., 2006. Oxygen sensing in the body. Progress In Biophysics & Molecular Biology 91, 249-286.
44. Lannig, G., Flores, J.F., Sokolova, I.M., 2006. Temperature-dependent stress response in oysters, Crassostrea virginica: pollution reduces temperature tolerance in oysters. Aquat. Toxicol. 79, 278-287.
45. Li, T., Brouwer, M., 2007. Hypoxia-inducible factor, gsHIF, of the grass shrimp Palaemonetes pugio: molecular characterization and response to hypoxia. Comp Biochem Physiol B 147, 11-19. (Pubitemid 46484418)
46. Li, T., Brouwer, M., 2009. Gene expression profile of grass shrimp Palaemonetes pugio exposed to chronic hypoxia. Comp Biochem Physiol D 4, 196-208.
47. Liu, Y.V., Semenza, G.L., 2007. Perspective RACK1 vs. HSP90. Competition for HIF-1α degradation vs. stabilization. Cell Cycle 6, 656-659.
48. Morin, P., McMullen, D., Storey, K., 2005. HIF-1α involvement in low temperature and anoxia survival by a freeze tolerant insect. Mol. Cell. Biochem. 280, 99-106.
49. Nei, M., Kumar, S., 2000. Molecular evolution and phylogenetics. Oxford University Press, Oxford.
50. Newell, R.C., 1976. Adaptations to intertidal life. In: Newell, R.C. (Ed.), Adaptations to Environment: Essays on the Physiology of Marine Animals. Butterworths, Boston, Massachusets, pp. 1-82.
51. Nikinmaa, M., Leveelahti, L., Dahl, E., Rissanen, E., Rytkönen, K.T., Laurila, A., 2008. Population origin, development and temperature of development affect the amounts of HSP70, HSP90 and the putative hypoxia-inducible factor in the tadpoles of the common frog Rana temporaria. J. Exp. Biol. 211, 1999-2004.
52. Pfaffl, M.W., 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, 2002-2007.
53. Ratcliffe, P.J., 2007. HIF-1 and HIF-2: working alone or together in hypoxia? J. Clin. Investig. 117, 862-865.
54. Rissanen, E., Tranberg, H.K., Nikinmaa, M., 2006a. Oxygen availability regulates metabolism and gene expression in trout hepatocyte cultures. Am. J. Physiol. Regul. Integr. Comp. Physiol. 291, R1507-R1515.
55. Rissanen, E., Tranberg, H.K., Sollid, J., Nilsson, G.E., Nikinmaa, M., 2006b. Temperature regulates hypoxia-inducible factor-1 (HIF-1) in a poikilothermic vertebrate, crucian carp (Carassius carassius). J. Exp. Biol. 209, 994-1003.
56. Rytkönen, K.T., Vuori, K.A.M., Primmer, C.R., Nikinmaa, M., 2007. Comparison of hypoxia-inducible factor-1 alpha in hypoxia-sensitive and hypoxia-tolerant fish species. Comp. Biochem. Physiol., D: Genomics Proteomics 2, 177-186. (Pubitemid 46648164)
57. Rytkönen, K.T., Ryynanen, H.J., Nikinmaa, M., Primmer, C.R., 2008. Variable patterns in the molecular evolution of the hypoxia-inducible factor-1 alpha (HIF-1α) gene in teleost fishes and mammals. Gene 420, 1-10.
58. Rzhetsky, A., Nei, M., 1992. A simple method for estimating and testing minimum-evolution trees. Mol. Biol. Evol. 9, 945-967.
59. Sanni, B., Williams, K., Sokolov, E.P., Sokolova, I.M., 2008. Effects of acclimation temperature and cadmium exposure on mitochondrial aconitase and LON protease from a model marine ectotherm, Crassostrea virginica. Comp Biochem Physiol C 147, 101-112. (Pubitemid 350218278)
60. Semenza, G.L., 2004. Hydroxylation of HIF-1: oxygen sensing at the molecular level. Physiology 19, 176-182. (Pubitemid 39481932)
61. Shen, Chuan, Powell-Coffman, J.A., 2003. Genetic analysis of hypoxia signaling and response in C. elegans. Ann. NY Acad. Sci. 995, 191-199.
62. Shen, C., Nettleton, D., Jiang, M., Kim, S.K., Powell-Coffman, J.A., 2005. Roles of the HIF-1 hypoxia-inducible factor during hypoxia response in Caenorhabditis elegans. J. Biol. Chem. 280, 20580-20588.
63. Simionato, E., Ledent, V., Richards, G., Thomas-Chollier, M., Kerner, P., Coornaert, D., Degnan, B., Vervoort, M., 2007. Origin and diversification of the basic helix-loop-helix gene family in metazoans: insights from comparative genomics. BMC Evol. Biol. 7, 33.
64. Sogawa, K., Fujii-Kuriyama, Y., 1997. Ah receptor, a novel ligand-activated transcription factor. J. Biochem. 122, 1075-1079. (Pubitemid 28019968)
65. Sokolova, I.M., Sokolov, E.P., 2005. Evolution of mitochondrial uncoupling proteins: novel invertebrate UCP homologues suggest early evolutionary divergence of the UCP family. FEBS Lett. 579, 313-317. (Pubitemid 40092405)
66. Sokolova, I.M., Ringwood, A.H., Johnson, C., 2005. Tissue-specific accumulation of cadmium in subcellular compartments of eastern oysters Crassostrea virginica Gmelin (Bivalvia: Ostreidae). Aquat. Toxicol. 74, 218-228. (Pubitemid 41138065)
67. Sollid, J., Rissanen, E., Tranberg, H., Thorstensen, T., Vuori, K., Nikinmaa, M., Nilsson, G., 2006. HIF-1α and iNOS levels in crucian carp gills during hypoxia-induced transformation. J. Comp. Physiol. B 176, 359-369.
68. Soñanez-Organis, J.G., Peregrino-Uriarte, A.B., Gómez-Jiménez, S., López-Zavala, A., Forman, H.J., Yepiz-Plascencia, G., 2009. Molecular characterization of hypoxia inducible factor-1 (HIF-1) from the white shrimp Litopenaeus vannamei and tissue-specific expression under hypoxia. Comp Biochem Physiol C 150, 395-405.
69. Stroka, D.M., Burkhardt, T., Desbaillets, I., Wenger, R.H., Neil, D.A.H., Bauer, C., Gassmann, M., Candinas, D., 2001. HIF-1 is expressed in normoxic tissue and displays an organ-specific regulation under systemic hypoxia. FASEB J. 15, 2445-2453. (Pubitemid 33063172)
70. Tamura, K., Dudley, J., Nei, M., Kumar, S., 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24, 1596-1599.
71. Taylor, M.S., 2001. Characterization and comparative analysis of the EGLN gene family. Gene 275, 125-132. (Pubitemid 32907334)
72. Taylor, C.T., Pouyssegur, J., 2007. Oxygen, hypoxia, and stress. Ann. NY Acad. Sci. 1113, 87-94.
73. Tian, H., McKnight, S.L., Russell, D.W., 1997. Endothelial PAS domain protein 1 (EPAS1), a transcription factor selectively expressed in endothelial cells. Genes Dev. 11, 72-82. (Pubitemid 27043825)
74. Vuori, K.A.M., Soitamo, A., Vuorinen, P.J., Nikinmaa, M., 2004. Baltic salmon (Salmo salar) yolk-sac fry mortality is associated with disturbances in the function of hypoxia-inducible transcription factor (HIF-1α) and consecutive gene expression. Aquat. Toxicol. 68, 301-313.
75. Wang, C.-D., Zhang, F.-S., 1995. Effect of enviromental oxygen deficiency on embryos and larvae of bay scallop Argopecten irradians irradians. Chinese J Oceanol Limnol 13, 362-369. (Pubitemid 126047363)
76. Webster, K.A., 2003. Evolution of the coordinate regulation of glycolytic enzyme genes by hypoxia. J. Exp. Biol. 206, 2911-2922.
77. Whelan, S., Goldman, N., 2001. A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol. Biol. Evol. 18, 691-699.