Transcriptional profile of cumulus associated GJA1, PTX3, PRSS35, and SERPINE2 genes with oocytes and embryonic development in water buffalo.

Publisher: Reidel Country of Publication: Netherlands NLM ID: 0403234 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1573-4978 (Electronic) Linking ISSN: 03014851 NLM ISO Abbreviation: Mol Biol Rep Subsets: MEDLINE

Original Publication: Dordrecht, Boston, Reidel.

Buffaloes*/genetics ; Serpin E2*/metabolism; Animals ; Cumulus Cells/metabolism ; Embryonic Development/genetics ; Female ; Male ; Oocytes/metabolism ; Pregnancy

Background: In the present study, the potential of different groups of cumulus-oocyte complexes (COC's) for in vitro maturation (IVM) and embryonic development was assessed in two groups of COC's of water buffalo. Further, the expression pattern of cumulus-associated GJA1, PTX3, PRSS35, and SERPINE2 genes and their effects on embryonic development was analyzed. Slaughterhouse-derived buffalo COC's were graded into groups A and B. An equal number of 410 COC's were taken in both groups. IVM was carried out using Slaughterhouse-derived buffalo epididymis. A remarkable degree of cumulus expansion was noticed in group A (92.68%) as compared to group B (81.25%) oocytes. On in vitro fertilization (IVF) and embryo culture, group A produced a significantly higher rate of cleavage and blastocyst (92.682 ± 0.7179% and 42.682 ± 0.9683%) as compared to group B (85.365 ± 0.7608% and 31.707 ± 0.9688%). Also, the transcriptional analysis of cumulus-associated genes revealed significantly higher expression in group A as compared to group B.
Results: It was revealed that oocytes having good cumulus mass had a higher developmental potential. Based on differential gene expression of cumulus-associated genes, different quality of COC's, and the resultant embryos after IVF, it was concluded that these genes could be used as a marker for predicting the developmental competence of the oocytes.
Conclusion: We concluded that morphologically good quality of COC's had a higher developmental competence, and also the differential expressions of cumulus-associated genes in cumulus cells and embryos. So, we can conclude that these genes could be used as marker genes for predicting the developmental competence of buffalo's oocytes.
(© 2022. The Author(s), under exclusive licence to Springer Nature B.V.)

Hansen PJ (2006) Realizing the promise of IVF in cattle—an overview. Theriogenology 65:119–125. (PMID: 10.1016/j.theriogenology.2005.09.019)
Sadeesh EM (2015) In vitro embryo production in buffalo: effects of culture system on pre-implantation development and gene expression pattern. Curr Sci 109(3):603–607.
Kumar D, Shukla MK, Jeena LM, Rahangdale S, Kumari D, Singh A, Sarkhel BC (2016) Assessment of in vitro maturation of oocytes derived from slaughterhouse goat ovaries. Ruminant Sci 5(1):17–20.
Huang RH, Zhou WH (2021) Granulosa cell biomarkers to predict oocyte and embryo quality in assisted reproductive technology. Reprod Dev Med 5(1):30–77. (PMID: 10.4103/2096-2924.313684)
Turathum B, Gao EM, Chian RC (2021) The function of cumulus cells in oocyte growth and maturation and in subsequent ovulation and fertilization. Cells 10(9):2292. (PMID: 10.3390/cells10092292)
Nivet AL, Vigneault C, Blondin P, Sirard MA (2013) Changes in granulosa cells gene expression associated with increased oocyte competence in bovine. Reproduction 145(6):555–565. (PMID: 10.1530/REP-13-0032)
Pengfei L, Jinzhu M, Wenzhong L, George WS, Jianbo Y, Lihua L (2016) Transcriptome analysis of bovine ovarian follicles at pre deviation and onset of deviation stages of a follicular wave. Int J Genom 3472748:1–9.
Da Broi MG, Giorgi VSI, Wang F, Keefe DL, Albertini D, Navarro PA (2018) Influence of follicular fluid and cumulus cells on oocyte quality: clinical implications. J Assist Reprod Genet 35(5):735–751. (PMID: 10.1007/s10815-018-1143-3)
Ferre LB, Bogliotti Y, Chitwood JL, Fresno C, Ortega HH, Kjelland ME, Ross RJ (2016) Effect of spermatozoa motility hyperactivation factors and gamete co-incubation duration on in vitro bovine embryo development using flow cytometrically sorted spermatozoa. Reprod Fertil Dev 29(4):805–814. (PMID: 10.1071/RD15289)
Uhde K, van Tol HTA, Stout TAE, Bernard AJR (2018) Metabolomic profiles of bovine cumulus cells and cumulus-oocyte-complex-conditioned medium during maturation in vitro. Sci Rep 8:9477. (PMID: 10.1038/s41598-018-27829-9)
Anderson RA, Sciorio R, Kinnell H, Bayne RA, Thong KJ, De-Sousa PA (2009) Cumulus gene expression as a predictor of human oocyte fertilization, embryo development and competence to establish a pregnancy. Reproduction 138(4):629–637. (PMID: 10.1530/REP-09-0144)
Hasegawa J, Yanaihara A, Iwasaki S, Mitsukawa K, Negishi M, Okai T (2007) Reduction of connexin 43 in human cumulus cells yields good embryo competence during ICSI. J Assist Reprod Genet 24:463–466. (PMID: 10.1007/s10815-007-9155-4)
Ortiz-Escribano N, Smits K, Piepers S, Vanden-Abbeel E, Woelders H, Van-Soom A (2016) Role of cumulus cells during vitrification and fertilization of mature bovineoocytes: effects on survival, fertilization, and blastocyst development. Theriogenology 86(2):635–641. (PMID: 10.1016/j.theriogenology.2016.02.015)
Downs SM (2001) A gap-junction-mediated signal, rather than an external paracrine factor, predominates during meiotic induction in isolated mouse oocytes. Zygote 9(1):71–82. (PMID: 10.1017/S0967199401001071)
Li HS, Lin MH, Hwu MY, Lu HC, Yeh YL, Chen JY, Lee KKR (2015) Correlation of cumulus gene expression of GJA1, PRSS35, PTX3, and SERPINE2 with oocyte maturation, fertilization, and embryo development in human. Reprod Biol Endocrinol 13:93. (PMID: 10.1186/s12958-015-0091-3)
Xia GL, Kikuchi K, Noguchi J, Izaike Y (2000) Short time priming of pig cumulus-oocyte complexes with FSH and forskolin in the presence of hypoxanthine stimulates cumulus cells to secrete a meiosis-activating substance. Theriogenology 53(9):1807–1815. (PMID: 10.1016/S0093-691X(00)00316-2)
Ebner T, Moser M, Sommergruber M, Tews G (2003) Selection based on morphological assessment of oocytes and embryos at different stages of pre-implantation development: a review. Hum Reprod Update 9(3):251–262. (PMID: 10.1093/humupd/dmg021)
Wang HX, Tong D, El-Gehani F, Tekpetey FR, Kidder GM (2008) Connexin expression and gap junctional coupling in human cumulus cells: contribution to embryo quality. J Cell Mol Med 13(5):972–984. (PMID: 10.1111/j.1582-4934.2008.00373.x)
Wahlberg P, Nylander A, Ahlskog N, Liu K, Ny T (2008) Expression and localization of the serine proteases high-temperature requirement factor A1, serine protease 23, and serine protease 35 in the mouse ovary. Endocrinology 149(10):5070–5077. (PMID: 10.1210/en.2007-1736)
Zhang X, Jafari N, Barnes RB, Confino E, Milad M, Kazer RR (2005) Studies of gene expression in human cumulus cells indicate pentraxin 3 as a possible marker for oocyte quality. Fertil Steril 83(1):1169–1179. (PMID: 10.1016/j.fertnstert.2004.11.030)
Hamel M, Dufort I, Robert C, Gravel C, Leveille MC, Leader A (2008) Identification of differentially expressed markers in human follicular cells associated with competent oocytes. Mol Hum Reprod 23(5):1118–1127. (PMID: 10.1093/humrep/den048)
Bedard J, Brule S, Price CA, Silversides DW, Lussier JG (2003) Serine protease inhibitor-E2 (SERPINE2) is differentially expressed in granulosa cells of dominant follicle in cattle. Mol Reprod Dev 64(2):52–65. (PMID: 10.1002/mrd.10239)
Chern SR, Li SH, Chiu CL, Chang HH, Chen CP, Chen EIT (2011) Spatiotemporal expression of SERPINE2 in the human placenta and its role in extra villous trophoblast migration and invasion. Reprod Biol Endocrinol 9:106. (PMID: 10.1186/1477-7827-9-106)
Lee RK, Fan CC, Hwu YM, Lu CH, Lin MH (2011) SERPINE2, an inhibitor of plasminogen activators, is highly expressed in the human endometrium during the secretory phase. Reprod Biol Endocrinol 23:9–38.
Jeena LM, Kumar D, Rahangdale S, Singh AP, Sarkhel BC (2019) Effect of cumulus cells of cumulus-oocyte complexes on in vitro maturation, embryonic developmental and expression pattern of apoptotic genes after in vitro fertilization in water buffalo (Bubalus bubalis). Anim Biotechnol 31(2):135–141. (PMID: 10.1080/10495398.2018.1554580)
Jeena L, Kumar D, Rahangdale S, Singh A, Sarkhel BC (2018) In vitro development competence of buffalo oocytes- effect of oocytes quality on maturation, embryonic developments and apoptosis. Int J Livestock Res 8(11):73–80.
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2ˉ ^ΔΔCt method. Methods 25(4):402–408. (PMID: 10.1006/meth.2001.1262)
Edry I, Sela-Abramovich S, Dekel N (2006) Meiotic arrest of oocytes depends on cell-to-cell communication in the ovarian follicle. Mol Cell Endocrinol 252(1–2):102–106. (PMID: 10.1016/j.mce.2006.03.009)
Feuerstein P, Cadoret V, Dalbies-Tran R, Guerif F, Bidault R, Royere D (2007) Gene expression in human cumulus cells: one approach to oocyte competence. Hum Reprod 22(12):3069–3077. (PMID: 10.1093/humrep/dem336)
Mishra A, Sharma GT, Kumar GS (2010) Expression profile of connexin 43 and poly A polymerase genes in buffalo (Bubalus bubalis) oocytes and developing embryos produced in vitro. J Appl Res 38(1):29–33.
Diao H, Xiao S, Li R, Zhao F, Ye X (2013) Distinct spatiotemporal expression of serine proteases Prss23 and Prss35 in periimplantation mouse uterus and dispensable function of Prss35 in fertility. PLoS ONE 8(2):e56757. (PMID: 10.1371/journal.pone.0056757)
Huang X, Hao C, Shen X, Zhang Y, Liu X (2013) RUNX2, GPX3 and PTX3 gene expression profiling in cumulus cells are reflective oocyte/embryo competence and potentially reliable predictors of embryo developmental competence in PCOS patients. Reprod Biol Endocrinol 11:109. (PMID: 10.1186/1477-7827-11-109)
Varani S, Elvin JA, Yan C, DeMayo J, DeMayo FJ, Horton HF, Byrne MC, Matzuk MM (2002) Knockout of pentraxin 3, a downstream target of growth differentiation factor-9, causes female subfertility. Mol Endocrinol 16(6):1154–1167. (PMID: 10.1210/mend.16.6.0859)
Salustri A, Garlanda C, Hirsch E, De-Acetis M, Maccagno A, Bottazzi B, Doni A, Bastone A, Mantovani G, Beck-Peccoz P, Salvatori G, Mahoney DJ, Day AJ, Siracusa G, Romani L, Mantovani A (2004) PTX3 plays a key role in the organization of the cumulus oophorus extracellular matrix and in in vivo fertilization. Development 131:1577–1586. (PMID: 10.1242/dev.01056)
Scarchilli L, Camaioni A, Bottazzi B, Negri V, Doni A, Deban L, Bastone A, Salvatori GA, Mantovani GS, Salustri A (2007) PTX3 interacts with inter-alpha-trypsin inhibitor: implications for hyaluronan organization and cumulus oophorus expansion. J Biol Chem 282(41):30161–30170. (PMID: 10.1074/jbc.M703738200)
Miyakoshi K, Murphy MJ, Yeoman RR, Mitra S, Dubay CJ, Hennebold JD (2006) The identification of novel ovarian proteases through the use of genomic and bioin-formatic methodologies. Biol Reprod 75(6):823–835. (PMID: 10.1095/biolreprod.106.052290)
Lu CH, Lee RK, Hwu YM, Lin MH, Yeh LY, Chen YJ, Lin SP, Li SH (2013) Involvement of the serine protease inhibitor, SERPINE2, and the urokinase plasminogen activator in cumulus expansion and oocyte maturation. PLoS ONE 8(8):e74602. (PMID: 10.1371/journal.pone.0074602)
Devjak R, Fon Tacer K, Juvan P, Virant Klun I, Rozman D, Vrtacnik Bokal E (2012) Cumulus cells gene expression profiling in terms of oocyte maturity in controlled ovarian hyperstimulation using GnRH agonist or GnRH antagonist. PLoS ONE 7(10):e47106. (PMID: 10.1371/journal.pone.0047106)
Lonergan P, Rizos D, Gutierrez-Adan A, Moreira PM, Pintado B, de la Fuente J, Boland MP (2003) Temporal divergence in the pattern of messenger RNA expression in bovine embryos cultured from the zygote to blastocyst stage in vitro or in vivo. Biol Reprod 69(4):1424–1431. (PMID: 10.1095/biolreprod.103.018168)
Sadeesh EM, Sikka P, Balhara AK, Balhara S (2016) Developmental competence and expression profile of genes in buffalo (Bubalus bubalis) oocytes and embryos collected under different environmental stress. Cytotechnology 68:2271–2285. (PMID: 10.1007/s10616-016-0022-y)

Keywords: Buffalo; Cumulus-oocyte complexes (COC’s); Embryo; Gene expression; In vitro fertilization (IVF); In vitro maturation (IVM)

0 (Serpin E2)

Date Created: 20220423 Date Completed: 20220713 Latest Revision: 20220713

20250114

10.1007/s11033-022-07435-9

35460443