Improvement in blastocyst quality by neurotensin signaling via its receptors in bovine spermatozoa during in vitro fertilization
Previously, we reported that neurotensin (NT), which is expressed in the uterus and oviduct, enhanced bovine sperm capacitation and acrosome reactions. As NT mRNA expression in bovine oviducts increases dramatically in the follicular phase, we hypothesized that NT modulates fertilization and subsequ...
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| Published in | Journal of Reproduction and Development Vol. 65; no. 2; pp. 147 - 153 |
|---|---|
| Main Authors | , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Japan
THE SOCIETY FOR REPRODUCTION AND DEVELOPMENT
2019
Japan Science and Technology Agency The Society for Reproduction and Development |
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| Online Access | Get full text |
| ISSN | 0916-8818 1348-4400 |
| DOI | 10.1262/jrd.2018-147 |
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| Abstract | Previously, we reported that neurotensin (NT), which is expressed in the uterus and oviduct, enhanced bovine sperm capacitation and acrosome reactions. As NT mRNA expression in bovine oviducts increases dramatically in the follicular phase, we hypothesized that NT modulates fertilization and subsequent conception in cattle. The objective of this study was to evaluate the effect of NT on embryo development and blastocyst quality. The rate of embryo cleavage was significantly increased by the addition of NT to the fertilization medium. Furthermore, the total number of cells and numbers of cells in the inner cell mass of blastocysts were significantly increased by NT during in vitro fertilization (IVF). These results suggested that NT enhanced the efficiency of early bovine embryo development and blastocyst quality. The expression of NT receptors (NTRs) in sperm, testes, oocytes, and cumulus cells was evaluated to determine whether NT acted via NTRs in sperm alone or in both male and female reproductive cells during IVF. Immunocytochemistry and reverse transcription polymerase chain reaction revealed that NTR1 and NTR2 were expressed in sperm and testes, but not in oocytes and cumulus cells. We propose that NT selectively acts upon sperm via NTR1 and NTR2 during IVF to improve the cleavage rate and quality of blastocysts, which are important determinants of sperm quality for successful conception. This research supports our hypothesis that NT acts as a key modulator of fertilization and conception in cattle. Further studies are necessary to apply our findings to the industrial framework of bovine reproduction. |
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| AbstractList | Previously, we reported that neurotensin (NT), which is expressed in the uterus and oviduct, enhanced bovine sperm capacitation and acrosome reactions. As NT mRNA expression in bovine oviducts increases dramatically in the follicular phase, we hypothesized that NT modulates fertilization and subsequent conception in cattle. The objective of this study was to evaluate the effect of NT on embryo development and blastocyst quality. The rate of embryo cleavage was significantly increased by the addition of NT to the fertilization medium. Furthermore, the total number of cells and numbers of cells in the inner cell mass of blastocysts were significantly increased by NT during in vitro fertilization (IVF). These results suggested that NT enhanced the efficiency of early bovine embryo development and blastocyst quality. The expression of NT receptors (NTRs) in sperm, testes, oocytes, and cumulus cells was evaluated to determine whether NT acted via NTRs in sperm alone or in both male and female reproductive cells during IVF. Immunocytochemistry and reverse transcription polymerase chain reaction revealed that NTR1 and NTR2 were expressed in sperm and testes, but not in oocytes and cumulus cells. We propose that NT selectively acts upon sperm via NTR1 and NTR2 during IVF to improve the cleavage rate and quality of blastocysts, which are important determinants of sperm quality for successful conception. This research supports our hypothesis that NT acts as a key modulator of fertilization and conception in cattle. Further studies are necessary to apply our findings to the industrial framework of bovine reproduction. Previously, we reported that neurotensin (NT), which is expressed in the uterus and oviduct, enhanced bovine sperm capacitation and acrosome reactions. As NT mRNA expression in bovine oviducts increases dramatically in the follicular phase, we hypothesized that NT modulates fertilization and subsequent conception in cattle. The objective of this study was to evaluate the effect of NT on embryo development and blastocyst quality. The rate of embryo cleavage was significantly increased by the addition of NT to the fertilization medium. Furthermore, the total number of cells and numbers of cells in the inner cell mass of blastocysts were significantly increased by NT during in vitro fertilization (IVF). These results suggested that NT enhanced the efficiency of early bovine embryo development and blastocyst quality. The expression of NT receptors (NTRs) in sperm, testes, oocytes, and cumulus cells was evaluated to determine whether NT acted via NTRs in sperm alone or in both male and female reproductive cells during IVF. Immunocytochemistry and reverse transcription polymerase chain reaction revealed that NTR1 and NTR2 were expressed in sperm and testes, but not in oocytes and cumulus cells. We propose that NT selectively acts upon sperm via NTR1 and NTR2 during IVF to improve the cleavage rate and quality of blastocysts, which are important determinants of sperm quality for successful conception. This research supports our hypothesis that NT acts as a key modulator of fertilization and conception in cattle. Further studies are necessary to apply our findings to the industrial framework of bovine reproduction. |
| Author | NUMABE, Takashi OIKAWA, Toshinori TANEMURA, Kentaro YANAI, Rin YAJIMA, Risa HIRADATE, Yuuki UMEZU, Kohei HARA, Kenshiro |
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| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30662011$$D View this record in MEDLINE/PubMed |
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| Cites_doi | 10.1095/biolreprod.113.112789 10.1095/biolreprod65.5.1606 10.1073/pnas.1717974115 10.1016/j.pneurobio.2007.06.006 10.1262/jrd.2016-055 10.1002/jcp.26883 10.1262/jrd.2015-073 10.1016/S0165-6147(99)01357-7 10.1016/S1472-6483(10)61960-8 10.1530/jrf.0.1090153 10.1093/humrep/des417 10.1016/j.anireprosci.2011.07.001 10.1016/0093-691X(92)90096-A 10.1002/rmb2.12021 10.1073/pnas.1018202108 10.1038/s41598-018-21335-8 10.1186/s12958-015-0077-1 10.1002/ijc.22407 10.1016/j.theriogenology.2014.01.041 10.1262/jrd.2017-041 10.3168/jds.2017-13138 10.1262/jrd.1056S15 10.1016/S0021-9258(17)32938-1 10.1262/jrd.2015-067 10.1262/jrd.2014-140 10.1002/jez.1402260120 10.1002/j.1939-4640.1991.tb00262.x 10.1262/jrd.1056S61 10.1016/j.anireprosci.2013.01.010 10.1016/j.theriogenology.2015.12.001 10.1046/j.0022-202x.2001.01439.x 10.3168/jds.S0022-0302(01)70158-0 10.1111/j.1476-5381.1995.tb13371.x 10.1016/j.peptides.2006.04.027 10.1016/S0093-691X(99)00162-4 10.1016/j.biochi.2011.04.024 10.1016/j.peptides.2006.08.009 10.1262/jrd.19031 10.1371/journal.pone.0036627 10.1111/j.1439-0531.2004.00559.x 10.1095/biolreprod.114.127266 10.1095/biolreprod.108.070961 10.1016/j.peptides.2005.12.016 10.1242/jcs.100867 |
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| Keywords | In vitro fertilization Cumulus-oocyte complex Neurotensin Bovine sperm Blastocyst |
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| References_xml | – reference: 25. Oikawa T, Itahashi T, Numabe T. Improved embryo development in Japanese black cattle by in vitro fertilization using ovum pick-up plus intracytoplasmic sperm injection with dithiothreitol. J Reprod Dev 2016; 62: 11–16. – reference: 31. Takeda K, Uchiyama K, Kinukawa M, Tagami T, Kaneda M, Watanabe S. Evaluation of sperm DNA damage in bulls by TUNEL assay as a parameter of semen quality. J Reprod Dev 2015; 61: 185–190. – reference: 16. Miller LA, Cochrane DE, Carraway RE, Feldberg RS. Blockade of mast cell histamine secretion in response to neurotensin by SR 48692, a nonpeptide antagonist of the neurotensin brain receptor. Br J Pharmacol 1995; 114: 1466–1470. – reference: 26. Thouas GA, Korfiatis NA, French AJ, Jones GM, Trounson AO. Simplified technique for differential staining of inner cell mass and trophectoderm cells of mouse and bovine blastocysts. Reprod Biomed Online 2001; 3: 25–29. – reference: 9. 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| SubjectTerms | Acrosome Reaction - drug effects Acrosome Reaction - genetics Animals Blastocyst Blastocyst - cytology Blastocyst - drug effects Blastocyst - physiology Blastocysts Bovine sperm Capacitation Cattle - embryology Cells, Cultured Cumulus-oocyte complex Embryo Culture Techniques - methods Embryo Culture Techniques - veterinary Embryo, Mammalian Embryonic Development - drug effects Embryonic Development - genetics Female Fertilization - drug effects Fertilization - genetics Fertilization in Vitro - veterinary Gene expression Immunocytochemistry In vitro fertilization Male Neurotensin Neurotensin - metabolism Neurotensin - pharmacology Neurotensin - physiology Oocytes Original Oviduct Polymerase chain reaction Quality Receptors, Neurotensin - genetics Receptors, Neurotensin - metabolism Receptors, Neurotensin - physiology Reverse transcription Signal Transduction - drug effects Signal Transduction - genetics Sperm Sperm Capacitation - drug effects Sperm Capacitation - genetics Spermatozoa - drug effects Spermatozoa - physiology Testes Uterus |
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| Title | Improvement in blastocyst quality by neurotensin signaling via its receptors in bovine spermatozoa during in vitro fertilization |
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