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| Identification of Sheep Endogenous Beta-Retroviruses with Uterus-Specific Expression in the Pregnant Mongolian Ewe |
| QI Jing-wei, XU Meng-jie, LIU Shu-ying, ZHANG Yu-fei, LIU Yue, ZHANG Ya-kun , CAO Gui-fang |
| College of Veterinary Medicine, Inner Mongolia Agricultural University, Huhhot 010018, P.R.China |
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摘要 The sheep genome harbours approximately 20 copies of endogenous beta-retroviruses (enJSRVs), and circumstantial evidence suggests that enJSRVs might play a role in mammalian reproduction, particularly placental morphogenesis. This study was aimed to assess the expression of mRNAs of an enJSRV and its receptor, HYAL2, in the uterus and conceptuses of Mongolian ewes throughout gestation, using real-time reverse transcription polymerase chain reaction and in situ hybridization analysis. The results showed that enJSRV and HYAL2 mRNAs were found to be expressed throughout gestation in the endometrium, chorion, placenta, and conceptus. The enJSRV mRNA was most abundant in the placenta on day 90 of pregnancy, in the endometrium on day 30 and 50, and in the chorion on day 70 and 110. However, HYAL2 mRNA was most abundant in the endometrium on day 30. These differences were all significantly different from each other (P<0.01). In situ hybridization showed that enJSRV and HYAL2 mRNAs were specifically expressed in endometrial luminal epithelium and glandular epithelium, trophoblastic giant binucleated cells (BNCs), endometrial caruncles, placental cotyledons, stroma, trophectoderm, as well as multinucleated syncytia of the placenta and blood vessel endothelial cells. Collectively, little is known about the molecular mechanisms by which trophoblastic differentiation and multinucleated syncytia formation are regulated by enJSRVs. However, the temporal and spatial distributions of enJSRV expression in the uterus and conceptus indicate that differentiation of BNCs and the formation of a multinucleated syncytiotrophoblast involve enJSRV and possibly its cellular receptor, HYAL2. Therefore, enJSRV and HYAL2 appear to play important roles in the female reproductive physiology in this breed of sheep.
Abstract The sheep genome harbours approximately 20 copies of endogenous beta-retroviruses (enJSRVs), and circumstantial evidence suggests that enJSRVs might play a role in mammalian reproduction, particularly placental morphogenesis. This study was aimed to assess the expression of mRNAs of an enJSRV and its receptor, HYAL2, in the uterus and conceptuses of Mongolian ewes throughout gestation, using real-time reverse transcription polymerase chain reaction and in situ hybridization analysis. The results showed that enJSRV and HYAL2 mRNAs were found to be expressed throughout gestation in the endometrium, chorion, placenta, and conceptus. The enJSRV mRNA was most abundant in the placenta on day 90 of pregnancy, in the endometrium on day 30 and 50, and in the chorion on day 70 and 110. However, HYAL2 mRNA was most abundant in the endometrium on day 30. These differences were all significantly different from each other (P<0.01). In situ hybridization showed that enJSRV and HYAL2 mRNAs were specifically expressed in endometrial luminal epithelium and glandular epithelium, trophoblastic giant binucleated cells (BNCs), endometrial caruncles, placental cotyledons, stroma, trophectoderm, as well as multinucleated syncytia of the placenta and blood vessel endothelial cells. Collectively, little is known about the molecular mechanisms by which trophoblastic differentiation and multinucleated syncytia formation are regulated by enJSRVs. However, the temporal and spatial distributions of enJSRV expression in the uterus and conceptus indicate that differentiation of BNCs and the formation of a multinucleated syncytiotrophoblast involve enJSRV and possibly its cellular receptor, HYAL2. Therefore, enJSRV and HYAL2 appear to play important roles in the female reproductive physiology in this breed of sheep.
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Received: 17 May 2012
Accepted:
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| Fund: This research was funded by the National Natural Science Foundation of China (30960271 and 31160493) and the doctor fund project of Ministry of Education of China (20111515110008). |
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Corresponding Authors:
Correspondence LIU Shu-ying, E-mail: liushuying_imau@126.com
E-mail: liushuying_imau@126.com
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| About author: QI Jing-wei, E-mail: qijingwei_66@126.com |
Cite this article:
QI Jing-wei, XU Meng-jie, LIU Shu-ying, ZHANG Yu-fei, LIU Yue, ZHANG Ya-kun , CAO Gui-fang.
2013.
Identification of Sheep Endogenous Beta-Retroviruses with Uterus-Specific Expression in the Pregnant Mongolian Ewe. Journal of Integrative Agriculture, 12(5): 884-891.
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| [1]Armezzani A, Arnaud F, Caporale M, Meo D G, lannuzzi L,Murqia C, Palmarini M. 2011. The signal peptide of arecently integrated endogenous sheep betaretrovirusenvelope plays a major role in eluding gag-mediatedlate restriction. Journal of General Virology, 85, 7118-7128[2]Arnaud F, Caporale M, Varela M, Biek R, Chessa B, AlbertiA, Golder M, Mura M, Zhang Y P, Li Y, et al. 2007. Aparadigm for virus-host coevolution: sequentialcounter-adaptations between endogenous andexogenous retroviruses. Plos Pathogens, 3, 1716-1729[3]Arnaud F, Varela M, Spencer T E, Palmarini M. 2008.Coevolution of endogenous betaretroviruses of sheepand their host. Cellular and Molecular Life Sciences,65, 3422-3432[4]Bieniasz P D. 2003. Restriction factors: a defense againstretroviral infection. Trends in Microbiology, 11, 286-291[5]Black S G, Arnaud F, Burghardt R C, Satterfield M C, FlemingT A, Long C R, Hanna C, Murphy L, Biek R, PalmariniM, et al. 2010. Viral particles of endogenous betaretroviruses are released in the sheep uterus andinfect the conceptus trophectoderm in a transspeciesembryo transfer model. Journal of General Virology,84, 9078-9085[6]Blond J L, Lavillette D, Cheynet V, Bouton O, Oriol G, SylvieC F, Mandrand B, Mallet F, Cosset F L. 2000. Anenvelope glycoprotein of the human endogenousretrovirus HERV-W is expressed in the human placentaand fuses cells expressing the type D mammalianretrovirus receptor. Journal of General Virology, 74,3321-3329[7]DeHaven J E, Schwartz D A, Dahm M W, Hazard E S,Trifiletti R, Lacy E R, Norris J S. 1998. Novel retroviralsequences are expressed in the epididymis and uterusof Syrian hamsters. Journal of General Virology, 79,2687-2694[8]DeMartini J C, Carlson J O, Leroux C, Spencer T, PalmariniM. 2003. Endogenous retroviruses related to Jaagsiektesheep retrovirus. Current Topics in Microbiology andImmunology, 275, 117-137[9]Dunlap K A, Palmarini M, Adelson D L, Spencer T E. 2005.Sheep endogenous betaretroviruses (enJSRVs) and thehyaluronidase 2 (HYAL2) receptor in the ovine uterusand conceptus. Biology of Reproduction, 73, 271-279[10]Dunlap K A, Palmarini M, Spencer T E. 2006a. Ovineendogenous betaretroviruses (enJSRVs) and placentalmorphogenesis. Placenta, 27, 135-140[11]Dunlap K A, Palmarini M, Varela M, Burghardt R C, HayashiK, Farmer J L, Spencer T E. 2006b. Endogenousretroviruses regulate periimplantation placental growthand differentiation. Proceedings of the NationalAcademy of Sciences of the United States of America,103, 14390-14395[12]Frendo J L, Olivier D, Cheynet V, Blond J L, Bouton O,Vidaud M, Rabreau M, Brion E D, Mallet F. 2003. Directinvolvement of HERV-W Env glycoprotein in humantrophoblast cell fusion and differentiation. Molecularand Cellular Biology, 23, 3566-3574[13]Gray C A, Bartol F F, Tarleton B J, Wiley A A, Johnson G A,Bazer F W, Spencer T E. 2001. Developmental biologyof uterine glands. Biology of Reproduction, 65, 1311-1323[14]Hofacre A, Fan H. 2010. Jaagsiekte sheep retrovirus biologyand oncogenesis. Viruses, 2, 2618-2648[15]Hofacre A, Nitta T, Fan H. 2009. Jaagsiekte sheep retrovirusencodes a regulatory factor, Rej, required for synthesisof Gag protein. Journal of General Virology, 83, 12483-12498[16]Lander E S, Linton L M, Birren B, Nusbaum C, Zody M C,Baldwin J, Devon K, Dewar K, Doyle M. 2001. Initialsequencing and analysis of the human genome. Nature,409, 860-921[17]Livak K J, Schmittgen T D. 2001. Analysis of relative geneexpression data using real-time quantitative PCR andthe 2-ΔΔCt method. Mechanisms and Methods Toxicol,25, 402-408[18]Mann G E, Lamming G E. 1999. The influence ofprogesterone during early pregnancy in cattle.Reproduction in Domestic Animals, 34, 269-274[19]Mi S, Lee X, Li X, Veldman G M, Finnerty H, Racie L, LaVallieE, Tang X Y, Edouard P, Howes S, et al. 2000. Syncytinis a captive retroviral envelope protein involved inhuman placental morphogenesis. Nature, 403, 785-789[20]Muir A, Lever A, Moffett A. 2004. Expression and functionsof human endogenous retroviruses in the placenta:anupdate. Placenta, 25, S16-S25.Mura M, Caporale P M, Spencer T E, Nagashima K, Rein A,Palmarini M. 2004. Late viral interference induced bytransdominant Gag of an endogenous retrovirus.Proceedings of the National Academy of Sciences ofthe United States of America, 101, 11117-11122[21]Paces J, Pavlícek A, Paces V. 2002. Database of humanendogenous retroviruses. Nucleic Acids Research, 30,205-206[22]Palmarini M, Gray A, Carpenter K, Fan H, Bazer F W, SpencerT E. 2001. Expression of endpgenous bataretrovirusesin the ovine uterus: effects of neonatal age,estrouscycle, pregnancy and progersterone. Journal ofGeneral Virology, 75, 11319-11327[23]Palmarini M, Mura M, Spencer T E. 2004. Endogenousbetaretroviruses of sheep: teaching new lessons inretroviral interference and adaptation. Journal ofGeneral Virology, 85, 1-13[24]Qi J W, Wu X L, Liu S Y, Cao G F. 2012. Expression ofenJSRV and Hyal-2 mRNA in immune organs of fetusesand lambs Virologica Sinica, 27, 83-92[25]Rote N S, Chakrabarti S, Stetzer B P. 2004. The role of humanendogenous retroviruses in trophoblast differentiationand placental development. Placenta, 25, 673-683[26]Roberts R M, Ealy A D, Alexenko A P, Alexenko, Han C S,Ezashi T. 1999. Trophoblast interferons. Placenta, 20,259-264[27]Spencer T E, Mura M, Gray C A, Griebel P J, Palmarini M.2003. Receptor usage and fetal expression of ovineendogenous beta-retroviruses: implications for coevolutionof endogenous and exogenous retrovirus.Journal of General Virology, 77, 749-753[28]Spencer T E, Ott T L, Bazer F W. 1998. Tau-Interferon:pregnancy recognition signal in ruminants.Proceedings of the Society for Experimental Biologyand Medicine, 213, 215-229[29]Stoye J P, Coffin J M. 2000. A provirus put to work. Nature,403, 715-717[30]Wang Y, Liu S Y, Li J Y, Han M, Wang Z L. 2008. Cloningand sequence analysis of complete genome from theinner mongolia strain of the endogenousbetaretroviruses (enJSRV). Virologica Sinica, 23, 15-24 |
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