Protein oligomerization is the biochemical process highly up-regulated in porcine oocytes before in vitro maturation (IVM)

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Abstract

A wide variety of mechanisms controlling oligomerization are observed. The dynamic nature of protein oligomerization is important for bioactivity control. The oocyte must undergo a series of changes to become a mature form before it can fully participate in the processes associated with its function as a female gamete. The growth of oocytes in the follicular environment is accompanied by surrounding somatic cumulus (CCs) and granulosa cells (GCs). It has been shown that oocytes tested before and after in vitro maturation (IVM) differ significantly in the transcriptomic and proteomic profiles. The aim of this study was to determine new proteomic markers for the oligomerization of porcine oocyte proteins that are associated with cell maturation competence. The Affymetrix microarray assay was performed to examine the gene expression profile associated with protein oligomerization in oocytes before and after IVM. In total, 12258 different transcriptomes were analyzed, of which 419 genes with lower expression in oocytes after IVM. We found 9 genes: GJA1, VCP, JUP, MIF, MAP3K1, INSR, ANGPTL4, EIF2AK3, DECR1, which were significantly down-regulated in oocytes after IVM (in vitro group) compared to oocytes analyzed before IVM (in vivo group). The higher expression of genes involved in the oligomerization of the protein before IVM indicates that they can be recognized as important markers of biological activation of proteins necessary for the further growth and development of pig embryos.

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  • 1. Watson AJ. Oocyte cytoplasmic maturation: a key mediator of oocyte and embryo developmental competence. J Anim Sci 2007;85:E1-3; DOI:10.2527/jas.2006-432.

  • 2. Agung B Otoi T Fuchimoto D Senbon S Onishi A Nagai T. In vitro fertilization and development of porcine oocytes matured in follicular fluid. J Reprod Dev. 2013;59:103–6.

  • 3. Chang CL Wang H-S Soong Y-K Huang SY Pai SY Hsu SYT. Regulation of oocyte and cumulus cell interactions by intermedin/adrenomedullin 2. J Biol Chem. 2011;286:43193–203; DOI:10.1074/jbc.M111.297358.

  • 4. Palma GA Argañaraz ME Barrera AD Rodler D Mutto AÁ Sinowatz F. Biology and biotechnology of follicle development. ScientificWorldJournal. 2012;2012:938138; DOI:10.1100/2012/938138.

  • 5. Liu S. A review on protein oligomerization process. Int J Precis Eng Manuf. 2015;16:2731–60; DOI:10.1007/s12541-015-0349-x.

  • 6. Celichowski P Nawrocki MJ Dyszkiewicz-Konwińska M Jankowski M Budna J Bryja A Kranc W Borys S Knap S Ciesiółka S Jeseta M Piasecka- Stryczyńska K Khozmi R Bukowska D Antosik P Brüssow KP Bruska M Nowicki M Zabel M Kempisty B. “Positive Regulation of RNA Metabolic Process” Ontology Group Highly Regulated in Porcine Oocytes Matured In Vitro: A Microarray Approach. BioMed Res Int. 2018;2018:2863068; DOI:10.1155/2018/2863068.

  • 7. Marques E Nkrumah JD Sherman EL Moore SS. Polymorphisms in positional candidate genes on BTA14 and BTA26 affect carcass quality in beef cattle. J Anim Sci. 2009;87:2475–84; DOI:10.2527/jas.2008-1456.

  • 8. Davoli R Fontanesi L Braglia S Russo V. A missense mutation in the porcine mitochondrial 24-dienoyl CoA reductase 1 (DECR1) gene and linkage mapping of this locus to chromosome 4; Anim Genet. 2002;33:73–5.

  • 9. Wathes DC Clempson AM Pollott GE. Associations between lipid metabolism and fertility in the dairy cow. Reprod Fertil Dev. 2012;25:48–61; DOI:10.1071/RD12272.

  • 10. Biterova E Esmaeeli M Alanen HI Saaranen M Ruddock LW. Structures of Angptl3 and Angptl4 modulators of triglyceride levels and coronary artery disease. Sci Rep. 2018;8:6752; DOI:10.1038/s41598-018-25237-7.

  • 11. Al-Edani T Assou S Ferrières A Bringer Deutsch S Gala A Lecellier C-H Aït-Ahmed O Hamamah S. Female aging alters expression of human cumulus cells genes that are essential for oocyte quality. BioMed Res Int. 2014;2014:964614; DOI:10.1155/2014/964614.

  • 12. Groh KJ Schönenberger R Eggen RIL Segner H Suter MJ-F. Analysis of protein expression in zebrafish during gonad differentiation by targeted proteomics. Gen Comp Endocrinol. 2013;193:210–20; DOI:10.1016/j.ygcen.2013.07.020.

  • 13. Cooke G Armstrong ME Donnelly SC. Macrophage migration inhibitory factor (MIF) enzymatic activity and the inflammatory response. BioFactors Oxf Engl. 2009;35:165–8; DOI:10.1002/biof.27.

  • 14. Lopes F Vannoni A Sestini S Casciaro A Carducci A Bartolommei S Toschi P Ptak G Cintorino M Arcuri F. Sheep (Ovis aries) Macrophage Migration Inhibitory Factor: molecular cloning characterization tissue distribution and expression in the ewe reproductive tract and in the placenta. Cytokine. 2011;54:315–23; DOI:10.1016/j.cyto.2011.02.013.

  • 15. Franz A Ackermann L Hoppe T. Create and preserve: Proteostasis in development and aging is governed by Cdc48/p97/VCP. Biochim Biophys Acta BBA - Mol Cell Res. 2014;1843:205–15; DOI:10.1016/j.bbamcr.2013.03.031.

  • 16. Capkova J Kubatova A Ded L Tepla O Peknicova J. Evaluation of the expression of sperm proteins in normozoospermic and asthenozoospermic men using monoclonal antibodies. Asian J Androl 2016;18:108–13; DOI:10.4103/1008-682X.151400.

  • 17. Müller JMM Deinhardt K Rosewell I Warren G Shima DT. Targeted deletion of p97 (VCP/CDC48) in mouse results in early embryonic lethality. Biochem Biophys Res Commun. 2007;354:459–65; DOI:10.1016/j.bbrc.2006.12.206.

  • 18. Shi Y Vattem KM Sood R An J Liang J Stramm L Wek RC. Identification and characterization of pancreatic eukaryotic initiation factor 2 alpha-subunit kinase PEK involved in translational control. Mol Cell Biol. 1998;18:7499–509.

  • 19. Harding HP Zhang Y Bertolotti A Zeng H Ron D. Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol Cell. 2000;5:897–904.

  • 20. Lin JH Li H Yasumura D Cohen HR Zhang C Panning B Shokat KM Lavail MM Walter P. IRE1 signaling affects cell fate during the unfolded protein response. Science. 2007;318:944–9; DOI:10.1126/science.1146361.

  • 21. Basheer WA Fu Y Shimura D Xiao S Agvanian S Hernandez DM Hitzeman TC Hong T Shaw RM. Stress response protein GJA1-20k promotes mitochondrial biogenesis metabolic quiescence and cardioprotection against ischemia/reperfusion injury. JCI Insight. 2018;3; DOI:10.1172/jci.insight.121900.

  • 22. Kempisty B Ziółkowska A Ciesiółka S Piotrowska H Antosik P Bukowska D Nowicki M Brüssow KP Zabel M. Study on connexin gene and protein expression and cellular distribution in relation to real-time proliferation of porcine granulosa cells. J Biol Regul Homeost Agents. 2014;28:625–35.

  • 23. Wang H-X Tong D El-Gehani F Tekpetey FR Kidder GM. Connexin expression and gap junctional coupling in human cumulus cells: contribution to embryo quality. J Cell Mol Med. 2009;13:972–84; DOI:10.1111/j.1582-4934.2008.00373.x.

  • 24. Richard S Baltz JM. Prophase I arrest of mouse oocytes mediated by natriuretic peptide precursor C requires GJA1 (connexin-43) and GJA4 (connexin-37) gap junctions in the antral follicle and cumulus- oocyte complex. Biol Reprod. 2014;90:137; DOI:10.1095/biolreprod.114.118505.

  • 25. Moller DE Cohen O Yamaguchi Y Assiz R Grigorescu F Eberle A Morrow LA Moses AC Flier JS. Prevalence of mutations in the insulin receptor gene in subjects with features of the type A syndrome of insulin resistance. Diabetes. 1994;43:247–55.

  • 26. Chaves RN Duarte ABG Rodrigues GQ Celestino JJH Silva GM Lopes CAP Almeida AP Donato MAM Peixoto CA Moura AAA Lobo CH Locatelli Y Mermillod P Campello CC Figueiredo JR. The effects of insulin and follicle-simulating hormone (FSH) during in vitro development of ovarian goat preantral follicles and the relative mRNA expression for insulin and FSH receptors and cytochrome P450 aromatase in cultured follicles. Biol Reprod. 2012;87:69; DOI:10.1095/biolreprod.112.099010.

  • 27. Borys S Brązert M Jankowski M Kocherova I Ożegowska K Celichowski P Nawrocki MJ Kranc W Bryja A Kulus M Jeseta M Pieńkowski W Bręborowicz A Bukowska D Antosik P Pawelczyk L Skowroński MT Brüssow KP Bruska M Zabel M Nowicki M Kempisty B. Enzyme linked receptor protein signaling pathway is one of the ontology groups that are highly up-regulated in porcine oocytes before in vitro maturation. J Biol Regul Homeost Agents. 2018;32:1089–103.

  • 28. Procházková J Kabátková M Šmerdová L Pacherník J Sykorová D Kohoutek J Šimečková P Hrubá E Kozubík A Machala M Vondráček J. Aryl hydrocarbon receptor negatively regulates expression of the plakoglobin gene (jup). Toxicol Sci Off J Soc Toxicol. 2013;134:258–70; DOI:10.1093/toxsci/kft110.

  • 29. Swope D Li J Muller EJ Radice GL. Analysis of a Jup hypomorphic allele reveals a critical threshold for postnatal viability. Genes N Y N 2000. 2012;50:717–27; DOI:10.1002/dvg.22034.

  • 30. Fan H-Y Liu Z Shimada M Sterneck E Johnson PF Hedrick SM Richards JS. MAPK3/1 (ERK1/2) in ovarian granulosa cells are essential for female fertility. Science. 2009;324:938–41; DOI:10.1126/science.1171396.

  • 31. Ou X-H Li S Xu B-Z Chen L-N Jiang M-X Chen S-Q Chen N-Q. Mitogen-activated protein kinase-activated protein kinase 2 is a critical regulator of pig oocyte meiotic maturation. Reprod Fertil Dev. 2017;29:223–33; DOI:10.1071/RD15150.

  • 32. Cao R Wu W Zhou X Liu K Li B Huang X Zhang Y Liu H. Let-7g induces granulosa cell apoptosis by targeting MAP3K1 in the porcine ovary. Int J Biochem Cell Biol. 2015;68:148–57; DOI:10.1016/j.biocel.2015.08.011.

  • 33. Xia Y Karin M. The control of cell motility and epithelial morphogenesis by Jun kinases. Trends Cell Biol. 2004;14:94–101; DOI:10.1016/j.tcb.2003.12.005.

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