Abstract
Myosin heavy chain 11 (MYH11), a member of the myosin family, is an actin-based cytoskeletal motor protein. Limited previous studies have revealed that the Myh11 gene is expressed in cumulus cells, cumulus-oocyte complexes, and ovarian theca cells. However, its expression profiles in mouse tissues, oocytes and preimplantation embryos are largely unknown. Here, we found that the MYH11 protein was expressed in multiple mouse tissues. In the ovary, the MYH11 protein was highly expressed in oocytes and smooth muscle fiber cells. After ovulation and fertilization, Myh11 mRNA expression had sharply declined in zygotes and could not be detected from 8-cell to blastocyst stages, while the protein persisted until the blastocyst stage. Furthermore, the MYH11 protein was localized in the cytoplasm of oocytes and preimplantation embryos. These results provide the first evidence that MYH11 is enriched in oocytes and early embryos and might play a key role in oogenesis and early embryogenesis of mice.
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An Q, Peng W, Cheng Y, Lu Z, Zhou C, Zhang Y, Su J (2019) Melatonin supplementation during in vitro maturation of oocyte enhances subsequent development of bovine cloned embryos. J Cell Physiol 234:1–12. https://doi.org/10.1002/jcp.28357
Babu GJ, Warshaw DM, Periasamy M (2000) Smooth muscle myosin heavy chain isoforms and their role in muscle physiology. Microsc Res Techn 50:532–540. https://doi.org/10.1002/1097-0029(20000915)50:6<532::AID-JEMT10>3.0.CO;2-E
Babu GJ, Pyne GJ, Zhou Y et al (2004) Isoform switching from SM-B to SM-A myosin results in decreased contractility and altered expression of thin filament regulatory proteins. Am J Physiol Cell Physiol 287:C723–C729. https://doi.org/10.1152/ajpcell.00029.2004
Barfeld SJ, East P, Zuber V, Mills IG (2014) Meta-analysis of prostate cancer gene expression data identifies a novel discriminatory signature enriched for glycosylating enzymes. BMC Med Genom 7:513. https://doi.org/10.1186/s12920-014-0074-9
Deng Z, Liu P, Marlton P et al (1993) Smooth muscle myosin heavy chain locus (MYH11) maps to 16p13.13-p13.12 and establishes a new region of conserved synteny between human 16p and mouse 16. Genomics 18:156–159. https://doi.org/10.1006/geno.1993.1443
Foth BJ, Goedecke MC, Soldati D (2006) New insights into myosin evolution and classification. Proc Natl Acad Sci U S A 103:3681–3686. https://doi.org/10.1073/pnas.0506307103
García-Láez V, Beltrán D, De los Santos JM, Esteban FJ, Martínez-Conejero JA, De los Santos MJ (2011) Identification of gene expression of MYH11 and PF4V1 in cumulus cells (CC) after ovarian stimulation by microarrays technology: possible implications on oocyte maturation. Fertil Steril 96:S240. https://doi.org/10.1016/j.fertnstert.2011.07.921
Hao Y, Cui Y, Gu X (2016) Genome-wide DNA methylation profiles changes associated with constant heat stress in pigs as measured by bisulfite sequencing. Sci Rep 6:27507. https://doi.org/10.1038/srep27507
Itami N, Kawahara-Miki R, Kawana H, Endo M, Kuwayama T, Iwata H (2014) Age-associated changes in bovine oocytes and granulosa cell complexes collected from early antral follicles. J Assist Repr Genet 31:1079–1088. https://doi.org/10.1007/s10815-014-0251-y
Korn ED (2000) Coevolution of head, neck, and tail domains of myosin heavy chains. Proc Natl Acad Sci U S A 97:12559–12564. https://doi.org/10.1073/pnas.230441597
Landreh L, Stukenborg JB, Soder O, Svechnikov K (2013) Phenotype and steroidogenic potential of PDGFRα-positive rat neonatal peritubular cells. Mol Cell Endocrinol 372:96–104. https://doi.org/10.1016/j.mce.2013.03.019
Li L, Baibakov B, Dean J (2008) A subcortical maternal complex essential for preimplantation mouse embryogenesis. Dev Cell 15:416–425. https://doi.org/10.1016/j.devcel.2008.07.010
Masters TA, Kendrick-Jones J, Buss F (2017) Myosins: domain organisation, motor properties, physiological roles and cellular functions. In: Jockusch BM (ed) The actin cytoskeleton. Springer International Publishing, Cham, pp 77–122. https://doi.org/10.1007/164_2016_29
McGuire MM, Bowden W, Engel NJ, Ahn HW, Kovanci E, Rajkovic A (2011) Genomic analysis using high-resolution single-nucleotide polymorphism arrays reveals novel microdeletions associated with premature ovarian failure. Fertil Steril 95:1595–1600. https://doi.org/10.1016/j.fertnstert.2010.12.052
Miano JM, Cserjesi P, Ligon KL, Periasamy M, Olson EN (1994) Smooth muscle myosin heavy chain exclusively marks the smooth muscle lineage during mouse embryogenesis. Circ Res 75:803–812. https://doi.org/10.1161/01.RES.75.5.803
Okumu LA, Bruinton S, Braden TD, Simon L, Goyal HO (2012) Estrogen-induced maldevelopment of the penis involves down-regulation of myosin heavy chain 11 (MYH11) expression, a biomarker for smooth muscle cell differentiation. Biol Reprod 87:109. https://doi.org/10.1095/biolreprod.112.103556
Pannu H, Tran-Fadulu V, Papke CL et al (2007) MYH11 mutations result in a distinct vascular pathology driven by insulin-like growth factor 1 and angiotensin II. Hum Mol Genet 16:2453–2462. https://doi.org/10.1093/hmg/ddm201
Peng H, Chang B, Lu C et al (2012) Nlrp2, a maternal effect gene required for early embryonic development in the mouse. PLoS One 7:e30344. https://doi.org/10.1371/journal.pone.0030344
Peng H, Lin X, Liu F, Wang C, Zhang W (2015) NLRP9B protein is dispensable for oocyte maturation and early embryonic development in the mouse. J Reprod Develop 61:559–564. https://doi.org/10.1262/jrd.2015-050
Roussis IM, Guille M, Myers FA, Scarlett GP (2016) RNA whole-mount in situ hybridisation proximity ligation assay (rISH-PLA), an assay for detecting RNA-protein complexes in intact cells. PLoS One 11:e0147967. https://doi.org/10.1371/journal.pone.0147967
Schutz LF, Hurst RE, Schreiber NB, Spicer LJ (2018) Transcriptome profiling of bovine ovarian theca cells treated with fibroblast growth factor 9. Domest Anim Endocrin 63:48–58. https://doi.org/10.1016/j.domaniend.2017.12.002
Tong ZB, Gold L, De Pol A et al (2004) Developmental expression and subcellular localization of mouse MATER, an oocyte-specific protein essential for early development. Endocrinology 145:1427–1434. https://doi.org/10.1210/en.2003-1160
Wen Q, Wang Y, Tang J, Cheng CY, Liu YX (2016) Sertoli cell Wt1 regulates peritubular Myoid cell and fetal Leydig cell differentiation during fetal testis development. PLoS One 11:e0167920. https://doi.org/10.1371/journal.pone.0167920
Yan J, Zhang L, Xu J et al (2014) Smad4 regulates ureteral smooth muscle cell differentiation during mouse embryogenesis. PLoS One 9:e104503. https://doi.org/10.1371/journal.pone.0104503
Yang F, Wei Q, Adelstein RS, Wang PJ (2012) Non-muscle myosin IIB is essential for cytokinesis during male meiotic cell divisions. Dev Biol 369:356–361. https://doi.org/10.1016/j.ydbio.2012.07.011
Zhang W, Cheng Z, Qu X, Dai H, Ke X, Chen Z (2014) Overexpression of myosin is associated with the development of uterine myoma. J Obstet Gynaecol Re 40:2051–2057. https://doi.org/10.1111/jog.12461
Acknowledgments
The authors thank Professor Wenchang Zhang for helpful discussions. This work was supported by grants from the National Natural Science Foundation of China (grant number 31672415), Fujian Provincial Natural Science Foundation (grant number 2018 J01594), and FAFU Program for Distinguished Young Scholars (grant number XJQ201509).
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Fang, J., Meng, D., Huo, J. et al. Expression and localization of MYH11 in mouse tissues, oocytes and preimplantation embryos. Biologia 75, 961–967 (2020). https://doi.org/10.2478/s11756-019-00353-5
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DOI: https://doi.org/10.2478/s11756-019-00353-5