Abstract
Plasma glutathione peroxidase (pGPx) is an extracellular antioxidative selenoenzyme which has been detected in various adult tissues, but little is known about the expression and distribution of pGPx during embryogenesis. To investigate the expression patterns of pGPx during embryogenesis, we performed quantitative real-time PCR, in situ hybridization, Western blot, and immunohistochemistry analyses in whole embryos or each developing organ of mice on embryonic days (E)7.5–18.5. In whole embryos of E7.5–8.5, pGPx mRNA was more typically expressed in extra-embryonic tissues including ectoplacental cone, trophectoderm, and decidual cells than in embryos. However, after E9.5, pGPx mRNA and protein levels were increased in the embryos with differentiation and growth, but trended to gradually decrease in the extra-embryonic tissues until E18.5. In sectioned embryonic tissues on E13.5–18.5, pGPx mRNA and protein were mainly expressed in the developing nervous tissues, the sensory organs, and the epithelia of lung, skin, and intestine, the heart and artery, and the kidney. In particular, pGPx immunoreactivity was very strong in the developing liver. These results indicate that pGPx is spatio-temporally expressed in various embryonic organs as well as extra-embryonic tissues, suggesting that pGPx may function to protect the embryos against endogenous and exogenous reactive oxygen species during organogenesis.
Similar content being viewed by others
References
Avissar N, Slemmon JR, Palmer IS, Cohen HJ (1991) Partial sequence of human plasma glutathione peroxidase and immunologic identification of milk glutathione peroxidase as the plasma enzyme. J Nutr 121:1243–1249
Avissar N, Eisenmann C, Breen JG, Horowitz S, Miller RK, Cohen HJ (1994) Human placenta makes extracellular glutathione peroxidase and secretes it into maternal circulation. Am J Physiol 267:E68–E76
Avissar N, Finkelstein JN, Horowitz S, Willey JC, Coy E, Frampton MW, Watkins RH, Khullar P, Xu YL, Cohen HJ (1996) Extracellular glutathione peroxidase in human lung epithelial lining fluid and in lung cells. Am J Physiol 270:L173–L182
Baek IJ, Yon JM, Lee BJ, Yun YW, Yu WJ, Hong JT, Ahn B, Kim YB, Kim DJ, Kang JK, Nam SY (2005) Expression pattern of cytosolic glutathione peroxidase (cGPx) mRNA during mouse embryogenesis. Anat Embryol 209:315–321
Baek IJ, Yon JM, Lee SR, Kim MR, Hong JT, Lee BJ, Yun YW, Nam SY (2011) Differential expression of gastrointestinal glutathione peroxidase (GI–GPx) gene during mouse organogenesis. Anat Histol Embryol 40:210–218
Behne D, Kyriakopoulos A (2001) Mammalian selenium-containing proteins. Annu Rev Nutr 21:453–473
Braissant O, Wahli W (1998) A simplified in situ hybridization protocol using non-radioactivity labeled probes to detect abundant and rare mRNAs on tissue sections. Biochemica 1:10–16
Brigelius-Flohe R (1999) Tissue-specific functions of individual glutathione peroxidases. Free Radic Biol Med 27:951–965
Burton GJ, Hempstock J, Jauniaux E (2003) Oxygen, early embryonic metabolism and free radical-mediated embryopathies. Reprod Biomed Online 6:84–96
Chabory E, Damon C, Lenoir A, Kauselmann G, Kern H, Zevnik B, Garrel C, Saez F, Cadet R, Henry-Berger J, Schoor M, Gottwald U, Habenicht U, Drevet JR, Vernet P (2009) Epididymis seleno-independent glutathione peroxidase 5 maintains sperm DNA integrity in mice. J Clin Invest 119(7):2074–2085
Chen Y, Whitney PL, Frank L (1994) Comparative responses of premature versus full-term newborn rats to prolonged hyperoxia. Pediatr Res 35:233–237
Chu FF, Doroshow JH, Esworthy RS (1993) Expression, characterization, and tissue-distribution of a new cellular selenium-dependent glutathione peroxidase, GSHPx–GI. J Biol Chem 268:2571–2576
Correia KM, Conlon RA (2001) Whole-mount in situ hybridization to mouse embryos. Methods 23:335–338
Fantel AG, Person RE (2002) Involvement of mitochondria and other free radical sources in normal and abnormal fetal development. Ann NY Acad Sci 959:424–433
Forstrom JW, Zakowski JJ, Tappel AL (1978) Identification of the catalytic site of rat liver glutathione peroxidase as selenocysteine. Biochemistry 17:2639–2644
Hernández-Escobar SA, Avila-Casado MC, Soto-Abraham V, López Escudero OL, Soto ME, Vega-Bravo ML, van der Goes TF, Reyes-Maldonado E (2009) Cytological damage of nasal epithelium associated with decreased glutathione peroxidase in residents from a heavily polluted city. Int Arch Occup Environ Health 82:603–612
Ishibashi M, Akazawa S, Sakamaki H, Matsumoto K, Yamasaki H, Yamaguchi Y, Goto S, Urata Y, Kondo T, Nagataki S (1997) Oxygen-induced embryopathy and the significance of glutathione-dependent antioxidant system in the rat embryo during early organogenesis. Free Radic Biol Med 22:447–454
Jauniaux E, Poston L, Burton GJ (2006) Placental-related diseases of pregnancy: involvement of oxidative stress and implications in human evolution. Hum Reprod Update 12(6):747–755
Jones ML, Mark PJ, Lewis JL, Mori TA, Keelan JA, Waddell BJ (2010) Antioxidant defenses in the rat placenta in late gestation: increased labyrinthine expression of superoxide dismutases, glutathione peroxidase 3, and uncoupling protein 2. Biol Reprod 83:254–260
Khan JY, Black SM (2003) Developmental changes in murine brain antioxidant enzymes. Pediatr Res 54:77–82
Kim WS, Wong J, Weickert CS, Webster MJ, Bahn S, Garner B (2009) Apolipoprotein-d expression is increased during development and maturation of the human prefrontal cortex. J Neurochem 109:1053–1066
Kingsley PD, Whitin JC, Cohen HJ, Palis J (1998) Developmental expression of extracellular glutathione peroxidase suggests antioxidant roles in deciduum, visceral yolk sac, and skin. Mol Reprod Dev 49:343–355
Kryukov GV, Castellano S, Novoselov SV, Lobanov AV, Zehtab O, Guigo R, Gladyshev VN (2003) Characterization of mammalian selenoproteomes. Science 300(5624):1439–1443
Le Prell CG, Dolan DF, Schacht J, Miller JM, Lomax MI, Altschuler RA (2003) Pathways for protection from noise induced hearing loss. Noise Health 5(20):1–17
Lubieniecka JM, Streijger F, Lee JH, Stoynov N, Liu J, Mottus R, Pfeifer T, Kwon BK, Coorssen JR, Foster LJ, Grigliatti TA, Tetzlaff W (2011) Biomarkers for severity of spinal cord injury in the cerebrospinal fluid of rats. PLoS One 6(4):e19247
Maser RL, Magenheimer BS, Calvet JP (1994) Mouse plasma glutathione peroxidase cDNA sequence analysis and renal proximal tubular expression and secretion. J Biol Chem 269:27066–27073
Mistry HD, Wilson V, Ramsay MM, Symonds ME, Broughton Pipkin F (2008) Reduced selenium concentrations and glutathione peroxidase activity in preeclamptic pregnancies. Hypertension 52:881–888
Mistry HD, Kurlak LO, Williams PJ, Ramsay MM, Symonds ME, Pipkin FB (2010) Differential expression and distribution of placental glutathione peroxidases 1, 3 and 4 in normal and preeclamptic pregnancy. Placenta 31:401–408
Nguyen VD, Saaranen MJ, Karala AR, Lappi AK, Wang L, Raykhel IB, Alanen HI, Salo KE, Wang CC, Ruddock LW (2011) Two endoplasmic reticulum PDI peroxidases increase the efficiency of the use of peroxide during disulfide bond formation. J Mol Biol 406(3):503–515
Ohlemiller KK, McFadden SL, Ding DL, Lear PM, Ho YS (2000) Targeted mutation of the gene for cellular glutathione peroxidase (Gpx1) increases noise-induced hearing loss in mice. J Assoc Res Otolaryngol 1:243–254
Olson GE, Whitin JC, Hill KE, Winfrey VP, Motley AK, Austin LM, Deal J, Cohen HJ, Burk RF (2010) Extracellular glutathione peroxidase (Gpx3) binds specifically to basement membranes of mouse renal cortex tubule cells. Am J Physiol Renal Physiol 298:F1244–F1253
Ravid BR, Rao KS (2006) Role of metals in neuronal apoptosis: challenges associated with neurodegeneration. Curr Alzheimer Res 3:311–326
Schneider M, Vogt Weisenhorn DM, Seiler A, Bornkamm GW, Brielmeier M, Conrad M (2006) Embryonic expression profile of phospholipid hydroperoxide glutathione peroxidase. Gene Exp Patterns 6(5):489–494
Sunde RA, Thompson KM, Evenson JK, Thompson BM (2009) Blood glutathione peroxidase-1 mRNA levels can be used as molecular biomarkers to determine dietary selenium requirements in rats. Exp Biol Med 234:1271–1279
Takahashi K, Avissar N, Whitin J, Cohen H (1987) Purification and characterization of human plasma glutathione peroxidase: a selenoglycoprotein distinct from the known cellular enzyme. Arch Biochem Biophys 256:677–686
Tham DM, Whitin JC, Kim KK, Zhu SX, Cohen HJ (1998) Expression of extracellular glutathione peroxidase in human and mouse gastrointestinal tract. Am J Physiol 275:G1463–G1471
Tham DM, Whitin JC, Cohen HJ (2002) Increased expression of extracellular glutathione peroxidase in mice with dextran sodium sulfate-induced experimental colitis. Pediatr Res 51(5):641–646
Ufer C, Wang CC, Borchert A, Heydeck D, Kuhn H (2010) Redox control in mammalian embryo development. Antioxid Redox Signal 13(6):833–875
Valenca SS, Silva Bezerra F, Lopes AA, Romana-Souza B, Marinho Cavalcante M, Lima AB, Goncalves Koatz VL, Porto LC (2008) Oxidative stress in mouse plasma and lungs induced by cigarette smoke and lipopolysaccharide. Environ Res 108:199–204
Whitin JC, Bhamre S, Tham DM, Cohen HJ (2002) Extracellular glutathione peroxidase is secreted basolaterally by human renal proximal tubule cells. Am J Physiol Renal Physiol 283:F20–F28
Yan J, Hales BF (2006) Depletion of glutathione induces 4-hydroxynonenal protein adducts and hydroxyurea teratogenicity in the organogenesis stage mouse embryo. J Phamacol Exp Ther 319:613–621
Yon JM, Baek IJ, Lee SR, Kim MR, Lee BJ, Yun YW, Nam SY (2008) Immunohistochemical identification and quantitative analysis of cytoplasmic Cu/Zn superoxide dismutase in mouse organogenesis. J Vet Sci 9(3):233–240
Acknowledgments
This work was supported by the Priority Research Centers Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education, Science and Technology (2010-0029709).
Author information
Authors and Affiliations
Corresponding author
Additional information
Ki Youn Jung and In-Jeoung Baek were contributed equally to this article.
Rights and permissions
About this article
Cite this article
Jung, K.Y., Baek, IJ., Yon, JM. et al. Developmental expression of plasma glutathione peroxidase during mouse organogenesis. J Mol Hist 42, 545–556 (2011). https://doi.org/10.1007/s10735-011-9362-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10735-011-9362-2