Transcriptomic Pattern of Genes Regulating Protein Response and Status of Mitochondrial Activity Are Related to Oocyte Maturational Competence-A Transcriptomic Study

. 2019 May 07 ; 20 (9) : . [epub] 20190507

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid31067669

Grantová podpora
UMO-2016/21/B/NZ9/03535 Narodowe Centrum Nauki

This paper aims to identify and describe new genetic markers involved in the processes of protein expression and modification reflected in the change of mitochondrial activity before and after in vitro maturation of the oocyte. Porcine oocytes collected from the ovaries of slaughtered landrace gilts were subjected to the process of in vitro maturation. Transcriptomic changes in the expression profile of oocyte genes involved in response to hypoxia, the transmembrane protein receptor serine threonine kinase signaling pathway, the "transforming growth factor β receptor signaling pathway", "response to protein stimulus", and "response to organic substance" were investigated using microarrays. The expression values of these genes in oocytes was analyzed before (immature) and after (mature) in vitro maturation, with significant differences found. All the significantly altered genes showed downregulation after the maturation process. The most changed genes from these gene ontologies, FOS, ID2, VEGFA, BTG2, CYR61, ESR1, AR, TACR3, CCND2, CHRDL1, were chosen to be further validated, described and related to the literature. Additionally, the mitochondrial activity of the analyzed oocytes was measured using specific dyes. We found that the mitochondrial activity was higher before the maturation process. The analysis of these results and the available literature provides a novel insight on the processes that occur during in vitro oocyte maturation. While this knowledge may prove to be useful in further research of the procedures commonly associated with in vitro fertilization procedures, it serves mostly as a basic reference for further proteomic, in vivo, and clinical studies that are necessary to translate it into practical applications.

Zobrazit více v PubMed

Suresh K.P., Nandi S., Mondal S. Factors affecting laboratory production of buffalo embryos: A meta-analysis. Theriogenology. 2009;72:978–985. doi: 10.1016/j.theriogenology.2009.06.017. PubMed DOI

Rybska M., Knap S., Jankowski M., Jeseta M., Bukowska D., Antosik P., Nowicki M., Zabel M., Kempisty B., Jaśkowski J.M. Cytoplasmic and nuclear maturation of oocytes in mammals—Living in the shadow of cells developmental capability. Med. J. Cell Biol. 2018;6:13–17. doi: 10.2478/acb-2018-0003. DOI

Chermuła B., Brązert M., Jeseta M., Ożegowska K., Sujka-Kordowska P., Konwerska A., Bryja A., Kranc W., Jankowski M., Nawrocki M.J., et al. The Unique Mechanisms of Cellular Proliferation, Migration and Apoptosis are Regulated through Oocyte Maturational Development—A Complete Transcriptomic and Histochemical Study. Int. J. Mol. Sci. 2018;20:84. doi: 10.3390/ijms20010084. PubMed DOI PMC

Ożegowska K., Dyszkiewicz-Konwińska M., Celichowski P., Nawrocki M.J., Bryja A., Jankowski M., Kranc W., Brązert M., Knap S., Jeseta M., et al. Expression pattern of new genes regulating female sex differentiation and in vitro maturational status of oocytes in pigs. Theriogenology. 2018;121:122–133. doi: 10.1016/j.theriogenology.2018.08.019. PubMed DOI

Celichowski P., Nawrocki M.J., Dyszkiewicz-Konwińska M., Jankowski M., Budna J., Bryja A., Kranc W., Borys S., Knap S., Ciesiółka S., et al. “Positive Regulation of RNA Metabolic Process” Ontology Group Highly Regulated in Porcine Oocytes Matured In Vitro: A Microarray Approach. BioMed Res. Int. 2018;2018:1–10. doi: 10.1155/2018/2863068. PubMed DOI PMC

El Shourbagy S.H., Spikings E.C., Freitas M., John J.C.S. Mitochondria directly influence fertilisation outcome in the pig. Reproduction. 2006;131:233–245. doi: 10.1530/rep.1.00551. PubMed DOI

Moyes C.D., Battersby B.J., Leary S.C. Regulation of muscle mitochondrial design. J. Exp. Biol. 1998;201:299–307. PubMed

Liu H., Shi W., Wang D., Zhao X. Association analysis of mitochondrial DNA polymorphisms with oocyte number in pigs. Reprod. Fertil. Dev. 2019;31:805. doi: 10.1071/RD18219. PubMed DOI

Zand E., Fathi R., Nasrabadi M.H., Atrabi M.J., Spears N., Akbarinejad V. Maturational gene upregulation and mitochondrial activity enhancement in mouse in vitro matured oocytes and using granulosa cell conditioned medium. Zygote. 2018;26:366–371. doi: 10.1017/S0967199418000333. PubMed DOI

Kang E., Wu J., Gutierrez N.M., Koski A., Tippner-Hedges R., Agaronyan K., Platero-Luengo A., Martinez-Redondo P., Ma H., Lee Y., et al. Mitochondrial replacement in human oocytes carrying pathogenic mitochondrial DNA mutations. Nat. Cell Biol. 2016;540:270–275. doi: 10.1038/nature20592. PubMed DOI

Budna J., Celichowski P., Karimi P., Kranc W., Bryja A., Ciesiółka S., Rybska M., Borys S., Jeseta M., Bukowska D., et al. Does Porcine Oocytes Maturation in Vitro is Regulated by Genes Involved in “transforming growth factor β receptor signaling pathway”? Adv. Cell Biol. 2017;5:1–14. doi: 10.1515/acb-2017-0001. DOI

Kranc W., Budna J., Chachuła A., Borys S., Bryja A., Rybska M., Ciesiółka S., Sumelka E., Jeseta M., Brüssow K.P., et al. Cell Migration’ Is the Ontology Group Differentially Expressed in Porcine Oocytes Before and After In Vitro Maturation: A Microarray Approach. DNA Cell Biol. 2017;36:273–282. doi: 10.1089/dna.2016.3425. PubMed DOI

Budna J., Bryja A., Celichowski P., Kranc W., Ciesiółka S., Borys S., Rybska M., Kolecka-Bednarczyk A., Jeseta M., Bukowska D., et al. ‘Bone Development’ Is an Ontology Group Upregulated in Porcine Oocytes Before In Vitro Maturation: A Microarray Approach. DNA Cell Biol. 2017;36:638–646. doi: 10.1089/dna.2017.3677. PubMed DOI

Krishna A., Bhatt M.L.B., Singh V., Singh S., Gangwar P.K., Singh U.S., Kumar V., Mehrotra D. Differential Expression of c-fos Proto-Oncogene in Normal Oral Mucosa versus Squamous Cell Carcinoma. Asian Pac. J. Cancer Prev. 2018;19:867–874. PubMed PMC

Li X., Liu C., Jin M., Lu B. Oocyte-Specific Expression of Mouse MEX3C652AA in the Ovary and Its Potential Role in Regulating Maternal Fos mRNA. Biol. Reprod. 2016;94:115. doi: 10.1095/biolreprod.115.136630. PubMed DOI

Fakruzzaman M., Ghanem N., Bang J.-I., Ha A.-N., Lee K.-L., Sohn S.-H., Wang Z., Lee D.-S., Kong I.-K. Effect of peroxiredoxin II on the quality and mitochondrial activity of pre-implantation bovine embryos. Reprod. Sci. 2015;159:172–183. doi: 10.1016/j.anireprosci.2015.06.015. PubMed DOI

Guo L., Lan J., Lin Y., Guo P., Nie Q., Mao Q., Ren L., Qiu Y. Hypoxia/ischemia up-regulates Id2 expression in neuronal cells in vivo and in vitro. Neurosci. Lett. 2013;554:88–93. doi: 10.1016/j.neulet.2013.08.044. PubMed DOI

Zhong W., Xie Y., Abdallah M., Awonuga A.O., Slater J.A., Sipahi L., Puscheck E.E., Rappolee D.A. Cellular stress causes reversible, PRKAA1/2-, and proteasome-dependent ID2 protein loss in trophoblast stem cells. Reproduction. 2010;140:921–930. doi: 10.1530/REP-10-0268. PubMed DOI PMC

Murre C., Massari M.E. Helix-Loop-Helix Proteins: Regulators of Transcription in Eucaryotic Organisms. Mol. Cell. Biol. 2000;20:429–440. PubMed PMC

Budna J., Chachuła A., Kaźmierczak D., Rybska M., Ciesiółka S., Bryja A., Kranc W., Borys S., Żok A., Bukowska D., et al. Morphogenesis-related gene-expression profile in porcine oocytes before and after in vitro maturation. Zygote. 2017;25:331–340. doi: 10.1017/S096719941700020X. PubMed DOI

Verbraak E.J.C., van ’t Veld E.M., Groot Koerkamp M., Roelen B.A.J., van Haeften T., Stoorvogel W., Zijlstra C. Identification of genes targeted by FSH and oocytes in porcine granulosa cells. Theriogenology. 2011;75:362–376. doi: 10.1016/j.theriogenology.2010.09.008. PubMed DOI

Kaune H., Peyrache E., Williams S.A. Oocyte-derived Smad4 is not required for development of the oocyte or the preimplantation embryo. Theriogenology. 2015;83:897–903. doi: 10.1016/j.theriogenology.2014.11.024. PubMed DOI

Zhang L., Du X., Wei S., Li D., Li Q. A comprehensive transcriptomic view on the role of SMAD4 gene by RNAi-mediated knockdown in porcine follicular granulosa cells. Reproduction. 2016;152:81–89. doi: 10.1530/REP-16-0034. PubMed DOI

Trau H.A., Brännström M., Curry T.E., Duffy D.M. Prostaglandin E2 and vascular endothelial growth factor A mediate angiogenesis of human ovarian follicular endothelial cells. Hum. Reprod. 2016;31:436–444. doi: 10.1093/humrep/dev320. PubMed DOI PMC

Konwerska A., Janik B., Malińska A., Witkiewicz W., Zabel M. The Contribution of Endothelial Marker Proteins in the Determination of Vascular Angiogenic Potential, in Normal Physiological Conditions and in Neoplasia. Adv. Cell Biol. 2011;3:69–83. doi: 10.2478/v10052-011-0005-2. DOI

Douglas L.M., Alvarez F.J., McCreary C., Konopka J.B. Septin Function in Yeast Model Systems and Pathogenic Fungi. Eukaryot. Cell. 2005;4:1503–1512. doi: 10.1128/EC.4.9.1503-1512.2005. PubMed DOI PMC

Behbahanian A., Eimani H., Zeinali B., Valojerdi M.R., Yazdi P.E., Shahverdi A., Gourabi H., Golkar-Narenji A. In Vitro Maturation, Fertilization and Embryo Culture of Oocytes Obtained from Vitrified Auto-Transplanted Mouse Ovary. Int. J. Fertil. Steril. 2013;6:278–285. PubMed PMC

Zand-Vakili M., Golkar-Narenji A., E Mozdziak P., Eimani H. An in vitro study on oocyte and follicles of transplanted ovaries treated with vascular endothelial growth factor. J. Turk. Gynecol. Assoc. 2017;18:167–173. doi: 10.4274/jtgga.2017.0026. PubMed DOI PMC

Wright G.L., Maroulakou I.G., Eldridge J., Liby T.L., Sridharan V., Tsichlis P.N., Muise-Helmericks R.C. VEGF stimulation of mitochondrial biogenesis: requirement of AKT3 kinase. FASEB J. 2008;22:3264–3275. doi: 10.1096/fj.08-106468. PubMed DOI PMC

Tirone F. The gene PC3TIS21/BTG2, prototype member of the PC3/BTG/TOB family: Regulator in control of cell growth, differentiation, and DNA repair? J. Cell. Physiol. 2001;187:155–165. doi: 10.1002/jcp.1062. PubMed DOI

Hu X., Xing L., Jiao Y., Xu J., Wang X., Han A., Yu J. BTG2 overexpression increases the radiosensitivity of breast cancer cells in vitro and in vivo. Oncol. Res. 2013;20:457–465. doi: 10.3727/096504013X13685487925211. PubMed DOI

Zhang Y.-J., Wei L., Liu M., Li J., Zheng Y.-Q., Gao Y., Li X.-R. BTG2 inhibits the proliferation, invasion, and apoptosis of MDA-MB-231 triple-negative breast cancer cells. Tumor Biol. 2013;34:1605–1613. doi: 10.1007/s13277-013-0691-5. PubMed DOI

Fiori M.E., Villanova L., Barbini C., de Angelis M.L., De Maria R. miR-663 sustains NSCLC by inhibiting mitochondrial outer membrane permeabilization (MOMP) through PUMA/BBC3 and BTG2. Cell Death. 2018;9:49. doi: 10.1038/s41419-017-0080-x. PubMed DOI PMC

Borys S., Khozmi R., Kranc W., Bryja A., Dyszkiewicz-Konwinska M., Jeseta M., Kempisty B. Recent Findings of the Types of Programmed Cell Death. Adv. Cell Biol. 2017;5:43–49. doi: 10.1515/acb-2017-0004. DOI

Huang Y., Zhang J., Shao H., Liu J., Jin M., Chen J., Zhao H. miR-33a Mediates the Anti-Tumor Effect of Lovastatin in Osteosarcoma by Targeting CYR61. Cell. Physiol. Biochem. 2018;51:938–948. doi: 10.1159/000495396. PubMed DOI

Chien W., Kumagai T., Miller C.W., Desmond J.C., Frank J.M., Said J.W., Koeffler H.P. Cyr61 Suppresses Growth of Human Endometrial Cancer Cells. J. Biol. Chem. 2004;279:53087–53096. doi: 10.1074/jbc.M410254200. PubMed DOI

Chen Y., Breen K., E Pepling M. Estrogen can signal through multiple pathways to regulate oocyte cyst breakdown and primordial follicle assembly in the neonatal mouse ovary. J. Endocrinol. 2009;202:407–417. doi: 10.1677/JOE-09-0109. PubMed DOI

Ribas V., Drew B.G., Zhou Z., Phun J., Kalajian N.Y., Soleymani T., Daraei P., Widjaja K., Wanagat J., Vallim T.Q.D.A., et al. Skeletal muscle action of estrogen receptor α is critical for the maintenance of mitochondrial function and metabolic homeostasis in females. Sci. Transl. Med. 2016;8:334ra54. doi: 10.1126/scitranslmed.aad3815. PubMed DOI PMC

McElroy S.L., Byrne J.A., Chavez S.L., Behr B., Hsueh A.J., Westphal L.M., Pera R.A.R. Parthenogenic Blastocysts Derived from Cumulus-Free In Vitro Matured Human Oocytes. PLoS ONE. 2010;5:e10979. doi: 10.1371/journal.pone.0010979. PubMed DOI PMC

Walters K.A., Middleton L.J., Joseph S.R., Hazra R., Jimenez M., Simanainen U., Allan C.M., Handelsman D.J. Targeted Loss of Androgen Receptor Signaling in Murine Granulosa Cells of Preantral and Antral Follicles Causes Female Subfertility. Biol. Reprod. 2012;87:151. doi: 10.1095/biolreprod.112.102012. PubMed DOI

Wang X., Deng H., Basu I., Zhu L. Induction of Androgen Receptor-Dependent Apoptosis in Prostate Cancer Cells by the Retinoblastoma Protein. Cancer Res. 2004;64:1377–1385. doi: 10.1158/0008-5472.CAN-03-2428. PubMed DOI

Van Montfoort A.P., Geraedts J.P., Dumoulin J.C., Stassen A.P., Evers J., Ayoubi T.A. Differential gene expression in cumulus cells as a prognostic indicator of embryo viability: A microarray analysis. Mol. Hum. Reprod. 2008;14:157–168. doi: 10.1093/molehr/gam088. PubMed DOI

Budna J., Rybska M., Ciesiółka S., Bryja A., Borys S., Kranc W., Wojtanowicz-Markiewicz K., Jeseta M., Sumelka E., Bukowska D., et al. Expression of genes associated with BMP signaling pathway in porcine oocytes before and after IVM—A microarray approach. Reprod. Biol. Endocrinol. 2017;15:43. doi: 10.1186/s12958-017-0261-6. PubMed DOI PMC

Lin J., Patel S.R., Cheng X., Cho E.A., Levitan I., Ullenbruch M., Phan S.H., Park J.M., Dressler G.R. Kielin/chordin-like protein, a novel enhancer of BMP signaling, attenuates renal fibrotic disease. Nat. Med. 2005;11:387–393. doi: 10.1038/nm1217. PubMed DOI

Bentov Y., Casper R.F. The aging oocyte—Can mitochondrial function be improved? Fertil. Steril. 2013;99:18–22. doi: 10.1016/j.fertnstert.2012.11.031. PubMed DOI

Egerszegi I., Alm H., Ratky J., Heleil B., Brüssow K.-P., Torner H. Meiotic progression, mitochondrial features and fertilisation characteristics of porcine oocytes with different G6PDH activities. Reprod. Fertil. Dev. 2010;22:830–838. doi: 10.1071/RD09140. PubMed DOI

Roca J., Martínez E., Vazquez J.M., Lucas X. Selection of immature pig oocytes for homologous in vitro penetration assays with the brilliant cresyl blue test. Reprod. Fertil. Dev. 1998;10:479–486. doi: 10.1071/RD98060. PubMed DOI

Kranc W., Jankowski M., Budna J., Celichowski P., Khozmi R., Bryja A., Borys S., Dyszkiewicz-Konwińska M., Jeseta M., Magas M., et al. Amino acids metabolism and degradation is regulated during porcine oviductal epithelial cells (OECs) primary culture in vitro—A signaling pathways activation approach. Med. J. Cell Biol. 2018;6:18–26. doi: 10.2478/acb-2018-0004. DOI

Chamier-Gliszczyńska A., Brązert M., Sujka-Kordowska P., Popis M., Ożegowska K., Stefańska K., Kocherova I., Celichowski P., Kulus M., Bukowska D., et al. Genes involved in angiogenesis and circulatory system development are differentially expressed in porcine epithelial oviductal cells during long-term primary in vitro culture—A transcriptomic study. Med. J. Cell Biol. 2018;6:163–173. doi: 10.2478/acb-2018-0026. DOI

Bryja A., Dyszkiewicz-Konwińska M., Jankowski M., Celichowski P., Stefańska K., Chamier-Gliszczyńska A., Popis M., Mehr K., Bukowska D., Antosik P., et al. Ion homeostasis and transport are regulated by genes differentially expressed in porcine buccal pouch mucosal cells during long-term culture in vitro—A microarray approach. Med. J. Cell Biol. 2018;6:75–82. doi: 10.2478/acb-2018-0013. DOI

Nawrocki M.J., Celichowski P., Jankowski M., Kranc W., Bryja A., Borys-Wójcik S., Jeseta M., Antosik P., Bukowska D., Bruska M., et al. Ontology groups representing angiogenesis and blood vessels development are highly up-regulated during porcine oviductal epithelial cells long-term real-time proliferation—A primary cell culture approach. Med. J. Cell Biol. 2018;6:186–194. doi: 10.2478/acb-2018-0029. DOI

Stefańska K., Chamier-Gliszczyńska A., Jankowski M., Celichowski P., Kulus M., Rojewska M., Antosik P., Bukowska D., Bruska M., Nowicki M., et al. Epithelium morphogenesis and oviduct development are regulated by significant increase of expression of genes after long-term in vitro primary culture—A microarray assays. Med. J. Cell Biol. 2018;6:195–204. doi: 10.2478/acb-2018-0030. DOI

Walter W., Sánchez-Cabo F., Ricote M. GOplot: An R package for visually combining expression data with functional analysis: Fig. 1. Bioinformatics. 2015;31:2912–2914. doi: 10.1093/bioinformatics/btv300. PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...