Molecular characterization and mRNA expression of HIF-prolyl hydroxylase-2 (phd2) in hypoxia-sensing pathways from Megalobrama amblycephala

Comparative Biochemistry and Physiology Part - B: Biochemistry and Molecular Biology

Volumn 186, Issue , 2015, Pages 28-35

  Wang, Huijuan ^a   Huang, Chunxiao ^a   Chen, Nan ^a   Zhu, Kecheng ^a   Chen, Boxiang ^a,b   Wang, Weimin ^a   Wang, Huanling ^a  

^a HUAZHONG AGRICULTURAL UNIVERSITY   (China)

^b Hubei BaiRong Improved Aquatic Seed Co   (China)

Author keywords

Expression; Hif 1 ; Hypoxia; Megalobrama amblycephala; Phd2

Indexed keywords

AMINO ACID; COMPLEMENTARY DNA; HYPOXIA INDUCIBLE FACTOR PROLINE DIOXYGENASE; MESSENGER RNA; OXYGENASE; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; FISH PROTEIN;

ALPHA CHAIN; AMINO ACID SEQUENCE; ARTICLE; CYPRINIFORMES; DEVELOPMENTAL STAGE; DNA SYNTHESIS; EMBRYO; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; GENE EXPRESSION; HYPOXIA; MEGALOBRAMA AMBLYCEPHALA; MOLECULAR CLONING; NONHUMAN; OPEN READING FRAME; PHYLOGENETIC TREE; PHYLOGENY; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; RNA ISOLATION; SIGNAL TRANSDUCTION; ZINC FINGER MOTIF; ANIMAL; ANOXIA; CHEMISTRY; EMBRYOLOGY; FISH DISEASE; GROWTH, DEVELOPMENT AND AGING; LARVA; METABOLISM; MOLECULAR GENETICS; SEA BREAM; VETERINARY;

HYPEROGLYPHE POROSA; MEGALOBRAMA AMBLYCEPHALA;

AMINO ACID SEQUENCE; ANIMALS; ANOXIA; FISH DISEASES; FISH PROTEINS; HYPOXIA-INDUCIBLE FACTOR-PROLINE DIOXYGENASES; LARVA; METABOLIC NETWORKS AND PATHWAYS; MOLECULAR SEQUENCE DATA; PHYLOGENY; RNA, MESSENGER; SEA BREAM;

EID: 84928574626     PISSN: 10964959     EISSN: 18791107     Source Type: Journal    
DOI: 10.1016/j.cbpb.2015.04.001     Document Type: Article

References (64)

1. Almeida D.V., Bianchini A., Marins L.F. Growth hormone overexpression generates an unfavorable phenotype in juvenile transgenic zebrafish under hypoxic conditions. Gen. Comp. Endocrinol. 2013, 194:102-109.
2. Aprelikova O., Chandramouli G.V., Wood M., Vasselli J.R., Riss J., Maranchie J.K., Linehan W.M., Barrett J.C. Regulation of HIF prolyl hydroxylases by hypoxia-inducible factors. J. Cell. Biochem. 2004, 92:491-501.
3. Aravind L., Koonin E. The DNA-repair protein AlkB, EGL-9, and leprecan define new. Genome Biol. 2001, 2:1-8.
4. Beers J.M., Borley K.A., Sidell B.D. Relationship among circulating hemoglobin, nitric oxide synthase activities and angiogenic poise in red- and white-blooded Antarctic notothenioid fishes. Comp. Biochem. Physiol. A 2010, 156:422-429.
5. Berra E., Richard D.E., Gothie E., Pouyssegur J. HIF-1-dependent transcriptional activity is required for oxygen-mediated HIF-1alpha degradation. FEBS Lett. 2001, 491:85-90.
6. Berra E., Benizri E., Ginouves A., Volmat V., Roux D., Pouyssegur J. HIF prolyl-hydroxylase 2 is the key oxygen sensor setting low steady-state levels of HIF-1alpha in normoxia. EMBO J. 2003, 22:4082-4090.
7. Borley K.A., Beers J.M., Sidell B.D. Phenylhydrazine-induced anemia causes nitric-oxide-mediated upregulation of the angiogenic pathway in Notothenia coriiceps. J. Exp. Biol. 2010, 213:2865-2872.
8. Bruick R.K., McKnight S.L. A conserved family of prolyl-4-hydroxylases that modify HIF. Science 2001, 294:1337-1340.
9. Brunelle J.K., Bell E.L., Quesada N.M., Vercauteren K., Tiranti V., Zeviani M., Scarpulla R.C., Chandel N.S. Oxygen sensing requires mitochondrial ROS but not oxidative phosphorylation. Cell Metab. 2005, 1:409-414.
10. Centanin L., Ratcliffe P.J., Wappner P. Reversion of lethality and growth defects in Fatiga oxygen-sensor mutant flies by loss of hypoxia-inducible factor-alpha/Sima. EMBO Rep. 2005, 6:1070-1075.
11. Chen N., Chen L.P., Zhang J., Chen C., Wei X.L., Gul Y., Wang W.M., Wang H.L. Molecular characterization and expression analysis of three hypoxia-inducible factor alpha subunits, HIF-1alpha/2alpha/3alpha of the hypoxia-sensitive freshwater species, Chinese sucker. Gene 2012, 498:81-90.
12. Cioffi C.L., Qin Liu X., Kosinski P.A., Garay M., Bowen B.R. Differential regulation of HIF-1α prolyl-4-hydroxylase genes by hypoxia in human cardiovascular cells. BBRC 2003, 303:947-953.
13. Ding Z., Wu J., Su L., Zhou F., Zhao X., Deng W., Zhang J., Liu S., Wang W., Liu H. Expression of heat shock protein 90 genes during early development and infection in Megalobrama amblycephala and evidence for adaptive evolution in teleost. Dev. Comp. Immunol. 2013, 41:683-693.
14. Donald A.K., Charles B.K. The zebrafish midblastula transition. Development 1993, 119:447-456.
15. Duan L.J., Takeda K., Fong G.H. Prolyl hydroxylase domain protein 2 (PHD2) mediates oxygen-induced retinopathy in neonatal mice. Am. J. Pathol. 2011, 178:1881-1890.
16. Epstein A.C., Gleadle J., McNeill,Hewitson K.S., O'Rourke J., Mole D.R. C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 2001, 107:1-12.
17. Flashman E., Bagg E.A., Chowdhury R., Mecinovic J., Loenarz C., McDonough M.A., Hewitson K.S., Schofield C.J. Kinetic rationale for selectivity toward N- and C-terminal oxygen-dependent degradation domain substrates mediated by a loop region of hypoxia-inducible factor prolyl hydroxylases. J. Biol. Chem. 2008, 283:3808-3815.
18. Freedman S.J., Sun Z.Y., Poy F., Kung A.L., Livingston D.M., Wagner G., Eck M.J. Structural basis for recruitment of CBP/p300 by hypoxia-inducible factor-1 alpha. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:5367-5372.
19. Freeman R.S., Hasbani D.M., Lipscomb E.A., Straub J.A., Xie L. SM-20, EGL-9, and the EGLN family of hypoxia-inducible factor prolyl hydroxylases. Mol. Cells 2003, 16:1-12.
20. Geng X., Feng J., Liu S., Wang Y., Arias C., Liu Z. Transcriptional regulation of hypoxia inducible factors alpha (HIF-α) and their inhibiting factor (FIH-1) of channel catfish (Ictalurus punctatus) under hypoxia. Comp. Biochem. Physiol. B 2014, 169:38-50.
21. Guzy R.D., Hoyos B., Robin E., Chen H., Liu L., Mansfield K.D. Mitochondrial complex III is required for hypoxia-induced ROS production and cellular oxygen sensing. Cell Metab. 2005, 1:401-408.
22. Han D., Wen L., Chen Y. Molecular cloning of phd1 and comparative analysis of phd1, 2, and 3 expression in Xenopus laevis. Sci. World J. 2012, 2012:287-689.
23. Han W.Q., Zhu Q., Hu J., Li P.L., Zhang F., Li N. Hypoxia-inducible factor prolyl-hydroxylase-2 mediates transforming growth factor beta 1-induced epithelial-mesenchymal transition in renal tubular cells. Biochim. Biophys. Acta 2013, 1833:1454-1462.
24. Harten S.K., Ashcroft M., Maxwell P.H. Prolyl hydroxylase domain inhibitors: a route to HIF activation and neuroprotection. Antioxid. Redox Signal. 2010, 12:459-480.
25. 2 sensing. Science 2001, 292:464-468.
26. 2-regulated prolyl hydroxylation. Science 2001, 292:468-472.
27. Janssen H.L., Haustermans K.M., Sprong D., Blommestijn G., Hofland I., Hoebers F.J., Blijweert E., Raleigh J.A., Semenza G.L., Varia M.A., Balm A.J., van Velthuysen M.L., Delaere P., Sciot R., Begg A.C. HIF-1A, pimonidazole, and iododeoxyuridine to estimate hypoxia and perfusion in human head-and-neck tumors. Int. J. Radiat. Oncol. Biol. Phys. 2002, 54:1537-1549.
28. Kaelin W.G., Ratcliffe P.J. Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol. Cell 2008, 30:393-402.
29. Kimmel C.B., Ballard W.W., Kimmel S.R., Ullmann B., Schilling T.F. Stages of embryonic development of the zebrafish. Dev. Dyn. 1995, 203:253-310.
30. Kivirikko K.I., Myllyla R., Pihlajaniemi T. Protein hydroxylation: prolyl 4-hydroxylase, an enzyme with four cosubstrates and a multifunctional subunit. FASEB J. 1989, 3:1609-1617.
31. Lahiri S., Roy A., Baby S.M., Hoshi T., Semenza G.L., Prabhakar N.R. Oxygen sensing in the body. Prog. Biophys. Mol. Biol. 2006, 91:249-286.
32. Law S.H., Wu R.S., Ng P.K., Yu R.M., Kong R.Y. Cloning and expression analysis of two distinct HIF-alpha isoforms-gcHIF-1alpha and gcHIF-4alpha-from the hypoxia tolerant grass carp Ctenopharyngodon idellus. BMC Mol. Biol. 2006, 7:15.
33. Layman C.A., Smith D.E., Herod J.D. Seasonally varying importance of abiotic and biotic factors in marsh-pond fish communities. Mar. Ecol. Prog. Ser. 2000, 207:155-169.
34. Lin Y.C., Tayag C.M., Huang C.L., Tsui W.C., Chen J.C. White shrimp Litopenaeus vannamei that had received the hot-water extract of Spirulina platensis showed earlier recovery in immunity and up-regulation of gene expressions after pH stress. Fish Shellfish Immunol. 2010, 29:1092-1098.
35. Liu Y.V., Semenza G.L. RACK1 vs. HSP90: competition for HIF-1 alpha degradation vs. stabilization. Cell Cycle 2007, 6:656-659.
36. Mansfield K.D., Guzy R.D., Pan Yi, Young R.M., Cash T.P., Paul, Schumacker.T., Celeste Simon M. Mitochondrial dysfunction resulting from loss of cyto chrome c impairs cellular oxygen sensing and hypoxic HIF-alpha activation. Cell Metab. 2005, 1:393-399.
37. McCulloch D.L. Metabolic response of the grass shrimp Palaemonetes kadiakensis Rathbun, to acute exposure of sublethal changes in pH. Aquat. Toxicol. 1990, 17:263-274.
38. McMahon S., Charbonneau M., Grandmont S., Richard D.E., Dubois C.M. Transforming growth factor beta1 induces hypoxia-inducible factor-1 stabilization through selective inhibition of PHD2 expression. J. Biol. Chem. 2006, 281:24171-24181.
39. Minamishima Y.A., Kaelin W.G. Reactivation of hepatic EPO synthesis in mice after PHD loss. Science (New York, N.Y.) 2010, 329:407.
40. Minamishima Y.A., Moslehi J., Bardeesy N., Cullen D., Bronson R.T., Kaelin W.G. Somatic inactivation of the PHD2 prolyl hydroxylase causes polycythemia and congestive heart failure. Blood 2008, 111:3236-3244.
41. Minamishima Y.A., Moslehi J., Padera R.F., Bronson R.T., Liao R., Kaelin W.G. A feedback loop involving the Phd3 prolyl hydroxylase tunes the mammalian hypoxic response in vivo. Mol. Cell. Biol. 2009, 29:5729-5741.
42. Moslehi J., Minamishima Y.A., Shi J., Neuberg D., Charytan D.M., Padera R.F., Signoretti S., Liao R., Kaelin W.G. Loss of hypoxia-inducible factor prolyl hydroxylase activity in cardiomyocytes phenocopies ischemic cardiomyopathy. Circulation 2010, 122:1004-1016.
43. Myllyharju J. Prolyl 4-hydroxylases, key enzymes in the synthesis of collagens and regulation of the response to hypoxia, and their roles as treatment targets. Ann. Med. 2008, 40:402-417.
44. Myllyharju J. HIF prolyl 4-hydroxylases and their potential as drug targets. Curr. Pharm. Des. 2009, 15:3878-3885.
45. Myllyharju J. Prolyl 4-hydroxylases, master regulators of the hypoxia response. Acta Physiol. 2013, 208:148-165.
46. Myllyharju J., Kivirikko K.I. Collagens, modifying enzymes and their mutations in humans, flies and worms. Trends Genet. 2004, 20:33-43.
47. Pektas S., Knapp M.J. Substrate preference of the HIF-prolyl hydroxylase-2 (PHD2) and substrate-induced conformational change. J. Inorg. Biochem. 2013, 126:55-60.
48. Piontkivska H., Chung J.S., Ivanina A.V., Sokolov E.P., Techa S., Sokolova I.M. Molecular characterization and mRNA expression of two key enzymes of hypoxia-sensing pathways in eastern oysters Crassostrea virginica (Gmelin): hypoxia-inducible factor alpha (HIF-alpha) and HIF-prolyl hydroxylase (PHD). Comp. Biochem. Physiol. D 2011, 6:103-114.
49. Pollock M.S., Clarke L.M.J., Dubé M.G. The effects of hypoxia on fishes: from ecological relevance to physiological effects. Environ. Rev. 2007, 15:1-14.
50. Ricard-Blum S. The collagen family. Cold Spring Harb. Perspect. Biol. 2011, 3:a004978.
51. Rojas D.A., Perez-Munizaga D.A., Centanin L., Antonelli M., Wappner P., Allende M.L., Reyes A.E. Cloning of hif-1alpha and hif-2alpha and mRNA expression pattern during development in zebrafish. Gene Expr. Patterns 2007, 7:339-345.
52. Rytkönen K.T., Williams T.A., Renshaw G.M., Primmer C.R., Nikinmaa M. Molecular evolution of the metazoan PHD-HIF oxygen-sensing system. Mol. Biol. Evol. 2011, 28:1913-1926.
53. Semenza G.L. Oxygen sensing, homeostasis, and disease. N. Engl. J. Med. 2011, 365:537-547.
54. Shen R.J., Jiang X.Y., Pu J.W., Zou S.M. HIF-1alpha and -2alpha genes in a hypoxia-sensitive teleost species Megalobrama amblycephala: cDNA cloning, expression and different responses to hypoxia. Comp. Biochem. Physiol. B 2010, 157:273-280.
55. Takeda K., Ho V.C., Takeda H., Duan L.J., Nagy A., Fong G.H. Placental but not heart defects are associated with elevated hypoxia-inducible factor α levels in mice lacking prolyl hydroxylase domain protein 2. Mol. Cell. Biol. 2006, 26:8336-8346.
56. Takeda K., Cowan A., Fong G.H. Essential role for prolyl hydroxylase domain protein 2 in oxygen homeostasis of the adult vascular system. Circulation 2007, 116:774-781.
57. Takeda K., Aguila H.L., Parikh N.S., Li X., Lamothe K., Duan L.J., Takeda H., Lee F.S., Fong G.H. Regulation of adult erythropoiesis by prolyl hydroxylase domain proteins. Blood 2008, 111:3229-3235.
58. Taylor M.S. Characterization and comparative analysis of the EGLN gene family. Gene 2001, 275:125-132.
59. Taylor C.T., Pouyssegur J. Oxygen, hypoxia, and stress. Ann. N. Y. Acad. Sci. 2007, 1113:87-94.
60. Welker T.L., Mcnulty S.T., Klesius P.H. Effect of sublethal hypoxia on the immune response and susceptibility of channel catfish, Ictalurus punctatus, to enteric septicemia. J. World Aquacult. Soc. 2007, 38:12-23.
61. Xiao W. The hypoxia signaling pathway and hypoxic adaptation in fishes. Sci. China Life Sci. 2015, 58(2):148-155.
62. Yu F., White S.B., Zhao Q., Lee F.S. HIF-1alpha binding to VHL is regulated by stimulus-sensitive proline hydroxylation. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:9630-9635.
63. Zhang J., Wei X.L., Chen L.P., Chen N., Li Y.H., Wang W.M., Wang H.L. Sequence analysis and expression differentiation of chemokine receptor CXCR4b among three populations of Megalobrama amblycephala. Dev. Comp. Immunol. 2013, 40:195-201.
64. Zhu C.D., Wang Z.H., Yan B. Strategies for hypoxia adaptation in fish species: a review. J. Comp. Physiol. B. 2013, 183:1005-1013.