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http://dx.doi.org/10.5657/KFAS.2013.0070

Changes in Stanniocalcin-2 and Hypoxia-Inducible Factor-1α mRNA Expression in Medaka Oryzias dancena Exposed to Acute Hypoxia  

Shin, Ji Hye (Department of Marine Molecular Biotechnology, Gangneung-Wonju National University)
Sohn, Young Chang (Department of Marine Molecular Biotechnology, Gangneung-Wonju National University)
Publication Information
Korean Journal of Fisheries and Aquatic Sciences / v.46, no.1, 2013 , pp. 70-76 More about this Journal
Abstract
Some fish live in aquatic environments with low or temporally changing $O_2$ availability. Variation in dissolved oxygen (DO) levels requires behavioral, physiological, and biochemical adaptations to ensure the uptake of sufficient $O_2$. Several species are relatively well adapted to tolerate low $O_2$ partial pressures (hypoxia). The medaka (Oryzias dancena ) is an important model organism for biomedical research that shows remarkable tolerance to hypoxia. We investigated the regulation and role of hypoxia-inducible factor-1 (HIF-$1{\alpha}$) as a general hypoxia-response gene and stanniocalcin-2 (STC2), which is one of the genes regulated by HIF-$1{\alpha}$ in mammals under hypoxia. We subjected adult male medaka to the following three acute hypoxia regimes: 1, 24, and 72 h at DO = $1.8{\pm}0.5$ ppm. The changes in STC2 and HIF-$1{\alpha}$ mRNA were monitored using quantitative real-time reverse-transcription PCR. We found strong upregulation of HIF-$1{\alpha}$ mRNA in the livers of fish exposed to hypoxia. Hypoxia rapidly upregulated STC-2 mRNA expression in muscle, but not in the brain, gills, liver, or intestine. Therefore, unlike in mammals, hypoxia might regulate O. dancena STC-2 expression in an HIF-$1{\alpha}$-independent manner.
Keywords
Oryzias dancera; Hypoxia; Hypoxia-inducible factor; Medaka; Real-time PCR; Stanniocalcin;
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1 Wang GL, Jiang BH, Rue EA and Semenza GL. 1995. Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc Natl Acad Sci U S A 92, 5510-5514.   DOI   ScienceOn
2 Wang GL and Semenza GL. 1995. Purification and characterization of hypoxia-inducible factor 1. J Biol Chem 270, 1230-1237.   DOI   ScienceOn
3 Wawrowski A, Gerlach F, Hankeln T and Burmester T. 2011. Changes of globin expression in the Japanese medaka (Oryzias latipes) in response to acute and chronic hypoxia. J Comp Physiol B 181, 199-208. http://dx.doi.org/10.1007/s00360-010-0518-2   DOI
4 Weber RE. 1982. Intraspecific adaptation of hemoglobin function in fish to oxygen availability. In: Exogenous and Endogenous Influences on Metabolic and Neural Control. Addink ADF and Spronk N, eds. Pergamon Press, Oxford, U.K., 87-102.
5 Yeung BH, Law AY and Wong CK. 2012. Evolution and roles of stanniocalcin. Mol Cell Endocrinol 349, 272-280. http://dx.doi.org/10.1016/j.mce.2011.11.007   DOI   ScienceOn
6 Yeung HY, Lai KP, Chan HY, Mak NK, Wagner GF and Wong CK. 2005. Hypoxia-inducible factor-1-mediated activation of stanniocalcin-1 in human cancer cells. Endocrinology 146, 4951-4960. http://dx.doi.org/10.1210/en.2005-0365   DOI   ScienceOn
7 Yu RM, Chen EX, Kong RY, Ng PK, Mok HO and Au DW. 2006. Hypoxia induces telomerase reverse transcriptase (TERT) gene expression in non-tumor fish tissues in vivo: the marine medaka (Oryzias melastigma) model. BMC Mol Biol 7, 27. http://dx.doi.org/10.1186/1471-2199-7-27   DOI
8 Law AY and Wong CK. 2010. Stanniocalcin-2 promotes epithelial-mesenchymal transition and invasiveness in hypoxic human ovarian cancer cells. Exp Cell Res 316, 3425-3434. http://dx.doi.org/10.1016/j.yexcr.2010.06.026   DOI   ScienceOn
9 Liu G, Yang G, Chang B, Mercado-Uribe I, Huang M, Zheng J, Bast RC, Lin SH and Liu J. 2010. Stanniocalcin 1 and ovarian tumorigenesis. J Natl Cancer Inst 102, 812-827. http://dx.doi.org/10.1093/jnci/djq127   DOI   ScienceOn
10 Luo CW, Kawamura K, Klein C and Hsueh AJ. 2004. Paracrine regulation of ovarian granulosa cell differentiation by stanniocalcin (STC) 1: mediation through specific STC1 receptors. Molecular Endocrinology 18, 2085-2096.   DOI   ScienceOn
11 Luo CW, Pisarska MD and Hsueh AJ. 2005. Identification of a stanniocalcin paralog, stanniocalcin-2, in fish and the paracrine actions of stanniocalcin-2 in the mammalian ovary. Endocrinology 146, 469-476. http://dx.doi.org/10.1210/en.2004-1197   DOI   ScienceOn
12 Meyer HA, Tolle A, Jung M, Fritzsche FR, Haendler B, Kristiansen I, Gaspert A, Johannsen M, Jung K and Kristiansen G. 2009. Identification of stanniocalcin 2 as prognostic marker in renal cell carcinoma. Eur Urol 55, 669-678. http://dx.doi.org/10.1016/j.eururo.2008.04.001   DOI   ScienceOn
13 Rahman MS and Thomas P. 2007. Molecular cloning, characterization and expression of two hypoxia-inducible factor alpha subunits, HIF-1alpha and HIF-2alpha, in a hypoxia-tolerant marine teleost, Atlantic croaker (Micropogonias undulatus). Gene 396, 273-282. http://dx.doi.org/10.1016/j.gene.2007.03.009   DOI   ScienceOn
14 Soitamo AJ, Rabergh CM, Gassmann M, Sistonen L and Nikinmaa M. 2001. Characterization of a hypoxia-inducible factor (HIF-1alpha) from rainbow trout. Accumulation of protein occurs at normal venous oxygen tension. J Biol Chem 276, 19699-19705.   DOI   ScienceOn
15 Salceda S and Caro J. 1997. Hypoxia-inducible factor 1alpha (HIF-1alpha) protein is rapidly degraded by the ubiquitin-proteasome system under normoxic conditions. Its stabilization by hypoxia depends on redox-induced changes. J Biol Chem 272, 22642-22647.   DOI   ScienceOn
16 Semenza GL. 1999. Regulation of mammalian O2 homeostasis by hypoxia-inducible factor 1. Annu Rev Cell Dev Biol 15, 551-578.   DOI   ScienceOn
17 Shin J and Sohn YC. 2009. cDNA cloning of Japanese flounder stanniocalcin 2 and its mRNA expression in a variety of tissues. Comp Biochem Physiol A Mol Integr Physiol 153, 24-29. http://dx.doi.org/10.1016/j.cbpa.2008.11.014   DOI   ScienceOn
18 Sundell K., Bjornsson BT, Itoh H and Kawauchi H. 1992. Chum Salmon (Oncorhynchus-Keta) Stanniocalcin Inhibits Invitro Intestinal Calcium-Uptake in Atlantic Cod (Gadus-Morhua). Journal of Comparative Physiology B-Biochemical Systemic and Environmental Physiology 162, 489-495.
19 Virani NA and Rees BB. 2000. Oxygen consumption, blood lactate and inter-individual variation in the gulf killifish, Fundulus grandis, during hypoxia and recovery. Comp Biochem Physiol A Mol Integr Physiol 126:397-405.   DOI   ScienceOn
20 Wagner GF, Hampong M, Park CM and Copp DH. 1986. Purification, characterization, and bioassay of teleocalcin, a glycoprotein from salmon corpuscles of Stannius. Gen Comp Endocrinol 63, 481-491.   DOI   ScienceOn
21 Gagliardi AD, Kuo EY, Raulic S, Wagner GF and DiMattia GE. 2005. Human stanniocalcin-2 exhibits potent growth-suppressive properties in transgenic mice independently of growth hormone and IGFs. Am J Physiol Endocrinol Metab 288, 92-105. http://dx.doi.org/10.1152/ajpendo.00268.2004   DOI   ScienceOn
22 Ieta K, Tanaka F, Yokobori T, Kita Y, Haraguchi N, Mimori K, Kato H, Asao T, Inoue H, Kuwano H and Mori M. 2009. Clinicopathological significance of stanniocalcin 2 gene expression in colorectal cancer. Int J Cancer 125, 926-931. http://dx.doi.org/10.1002/ijc.24453   DOI   ScienceOn
23 He LF, Wang TT, Gao QY, Zhao GF, Huang YH, Yu LK and Hou YY. 2011. Stanniocalcin-1 promotes tumor angiogenesis through up-regulation of VEGF in gastric cancer cells. J Biomed Sci 18, 39. http://dx.doi.org/10.1186/1423-0127-18-39   DOI
24 Huang LE, Arany Z, Livingston DM and Bunn HF. 1996. Activation of hypoxia-inducible transcription factor depends primarily upon redox-sensitive stabilization of its alpha subunit. J Biol Chem 271, 32253-32259.   DOI   ScienceOn
25 Huang LE, Gu J, Schau M and Bunn HF. 1998. Regulation of hypoxia-inducible factor 1alpha is mediated by an $O_2$-dependent degradation domain via the ubiquitin-proteasome pathway. Proc Natl Acad Sci U S A 95, 7987-7992.   DOI   ScienceOn
26 Ishibashi K, Miyamoto K, Taketani Y, Morita K, Takeda E, Sasaki S and Imai M. 1998. Molecular cloning of a second human stanniocalcin homologue (STC2). Biochem Biophys Res Commun 250, 252-258.   DOI   ScienceOn
27 Jensen K, Freundlich M, Bunemann L, Therkelsen K, Hansen H and Cold GE. 1993. The effect of indomethacin upon cerebral blood flow in healthy volunteers. The influence of moderate hypoxia and hypercapnia. Acta Neurochir (Wien) 124, 114-119.   DOI
28 Ju Z, Wells MC, Heater SJ and Walter RB. 2007. Multiple tissue gene expression analyses in Japanese medaka (Oryzias latipes) exposed to hypoxia. Comp Biochem Physiol C Toxicol Pharmacol 145, 134-144. http://dx.doi.org/10.1016/j.cbpc.2006.06.012   DOI   ScienceOn
29 Kallio PJ, Pongratz I, Gradin K, McGuire J and Poellinger L. 1997. Activation of hypoxia-inducible factor 1alpha: post-transcriptional regulation and conformational change by recruitment of the Arnt transcription factor. Proc Natl Acad Sci U S A 94, 5667-5672.   DOI   ScienceOn
30 Kang CK, Tsai SC, Lee TH and Hwang PP. 2008. Differen tial expression of branchial Na+/K(+)-ATPase of two medaka species, Oryzias latipes and Oryzias dancena, with different salinity tolerances acclimated to fresh water, brackish water and seawater. Comp Biochem Physiol A Mol Integr Physiol 151, 566-575. http://dx.doi.org/10.1016/j.cbpa.2008.07.020   DOI   ScienceOn
31 Koumenis C, Naczki C, Koritzinsky M, Rastani S, Diehl A, Sonenberg N, Koromilas A and Wouters BG. 2002. Regulation of protein synthesis by hypoxia via activation of the endoplasmic reticulum kinase PERK and phosphorylation of the translation initiation factor eIF2alpha. Mol Cell Biol 22, 7405-7416.   DOI
32 Koumenis C and Wouters BG. 2006. "Translating" tumor hypoxia: unfolded protein response (UPR)-dependent and UPR-independent pathways. Mol Cancer Res 4, 423-436. doi: 10.1158/1541-7786.MCR-06-0150   DOI   ScienceOn
33 Bouras T, Southey MC, Chang AC, Reddel RR, Willhite D, Glynne R, Henderson MA, Armes JE and Venter DJ. 2002. Stanniocalcin 2 is an estrogen-responsive gene coexpressed with the estrogen receptor in human breast cancer. Cancer Res 62, 1289-1295.
34 Butkus A, Roche PJ, Fernley RT, Haralambidis J, Penschow JD, Ryan GB, Trahair JF, Tregear GW and Coghlan JP. 1987. Purification and cloning of a corpuscles of Stannius protein from Anguilla australis. Mol Cell Endocrinol 54, 123-133.   DOI   ScienceOn
35 Chang AC and Reddel RR. 1998. Identification of a second stanniocalcin cDNA in mouse and human: stanniocalcin 2. Mol Cell Endocrinol 141, 95-99.   DOI   ScienceOn
36 Chen N, Chen LP, Zhang J, Chen C, Wei XL, Gul Y, Wang WM and Wang HL. 2012. Molecular characterization and expression analysis of three hypoxia-inducible factor alpha subunits, HIF-1alpha/2alpha/3alpha of the hypoxiasensitive freshwater species, Chinese sucker. Gene 498, 81-90. http://dx.doi.org/10.1016/j.gene.2011.12.058   DOI   ScienceOn
37 Ellard JP, McCudden CR, Tanega C, James KA, Ratkovic S, Staples JF and Wagner GF. 2007. The respiratory effects of stanniocalcin-1 (STC-1) on intact mitochondria and cells: STC-1 uncouples oxidative phosphorylation and its actions are modulated by nucleotide triphosphates. Mol Cell Endocrinol 264, 90-101. http://dx.doi.org/10.1016/j.mce.2006.10.008   DOI   ScienceOn
38 DiMattia GE, Varghese R and Wagner GF. 1998. Molecular cloning and characterization of stanniocalcin-related protein. Mol Cell Endocrinol 146, 137-140.   DOI   ScienceOn