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Elevated intracellular pH appears in aged oocytes and causes oocyte aneuploidy associated with the loss of cohesion in mice

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Pages 2454-2463 | Received 08 Apr 2016, Accepted 08 Jun 2016, Published online: 19 Aug 2016

References

  • Pan H, Ma P, Zhu W, Schultz RM. Age-associated increase in aneuploidy and changes in gene expression in mouse eggs. Dev Biol 2008; 316:397-407; PMID:18342300; http://dx.doi.org/10.1016/j.ydbio.2008.01.048
  • Nagaoka SI, Hassold TJ, Hunt PA. Human aneuploidy: mechanisms and new insights into an age-old problem. Nat Rev Genet 2012; 13:493-504; PMID:22705668; http://dx.doi.org/10.1038/nrg3245
  • Chiang T, Duncan FE, Schindler K, Schultz RM, Lampson MA. Evidence that weakened centromere cohesion is a leading cause of age-related aneuploidy in oocytes. Curr Biol 2010; 20:1522-8; PMID:20817534; http://dx.doi.org/10.1016/j.cub.2010.06.069
  • Chiang T, Schultz RM, Lampson MA. Meiotic origins of maternal age-related aneuploidy. Biol Reprod 2012; 86:1-7; PMID:21957193; http://dx.doi.org/10.1095/biolreprod.111.094367
  • Jessberger R. Age-related aneuploidy through cohesion exhaustion. EMBO Rep 2012; 13:539-46; PMID:22565322
  • Jones KT, Lane SI. Molecular causes of aneuploidy in mammalian eggs. Development 2013; 140:3719-30; PMID:23981655; http://dx.doi.org/10.1242/dev.090589
  • Fu X, Cheng J, Hou Y, Zhu S. The association between the oocyte pool and aneuploidy: a comparative study of the reproductive potential of young and aged mice. J Assist Reprod Genet 2014; 31:323-31; PMID:24362910; http://dx.doi.org/10.1007/s10815-013-0160-5
  • Sakakibara Y, Hashimoto S, Nakaoka Y, Kouznetsova A, Hoog C, Kitajima TS. Bivalent sep -aration into univalents precedes age-related meiosis I errors in oocytes. Nat Commun 2015; 6:7550; PMID:26130582
  • Brieno-Enriquez MA, Cohen PE. Double trouble in human aneuploidy. Nat Genet 2015; 47:696-8; PMID:26111508; http://dx.doi.org/10.1038/ng.3344
  • Brar GA, Amon A. Emerging roles for centromeres in meiosis I chromosome segregation. Nat Rev Genet 2008; 9:899-910; PMID:18981989; http://dx.doi.org/10.1038/nrg2454
  • Hauf S, Watanabe Y. Kinetochore orientation in mitosis and meiosis. Cell 2004; 119:317-27; PMID:15507205; http://dx.doi.org/10.1016/j.cell.2004.10.014
  • Garcia-Cruz R, Brieno MA, Roig I, Grossmann M, Velilla E, Pujol A, Cabero L, Pessarrodona A, Barbero JL, Garcia Caldes M. Dynamics of cohesin proteins REC8, STAG3, SMC1 beta and SMC3 are consistent with a role in sister chromatid cohesion during meiosis in human oocytes. Hum Reprod 2010; 25:2316-27; PMID:20634189; http://dx.doi.org/10.1093/humrep/deq180
  • Wood AJ, Severson AF, Meyer BJ. Condensin and cohesin complexity: the expanding repertoire of functions. Nat Rev Genet 2010; 11:391-404; PMID:20442714; http://dx.doi.org/10.1038/nrg2794
  • Takahashi T, Saito H, Hiroi M, Doi K, Takahashi E. Effects of aging on inositol 1,4,5-triphosphate-induced Ca2+ release in unfertilized mouse oocytes. Mol Reprod Dev 2000; 55:299-306; PMID:10657049; http://dx.doi.org/10.1002/(SICI)1098-2795(200003)55:3%3c299::AID-MRD8%3e3.0.CO;2-G
  • Takahashi T, Takahashi E, Igarashi H, Tezuka N, Kurachi H. Impact of oxidative stress in aged mouse oocytes on calcium oscillations at fertilization. Mol Reprod Dev 2003; 66:143-52; PMID:12950101; http://dx.doi.org/10.1002/mrd.10341
  • Miao YL, Kikuchi K, Sun QY, Schatten H. Oocyte aging: cellular and molecular changes, developmental potential and reversal possibility. Hum Reprod Update 2009; 15:573-85; PMID:19429634; http://dx.doi.org/10.1093/humupd/dmp014
  • Simsek-Duran F, Li F, Ford W, Swanson RJ, Jones HW Jr, Castora FJ. Age-associated metabolic and morphologic changes in mitochondria of individual mouse and hamster oocytes. PLoS One 2013; 8:e64955; PMID:23741435; http://dx.doi.org/10.1371/journal.pone.0064955
  • Alper SL. The band 3-related AE anion exchanger gene family. Annu Rev Physiol 1991; 53:549-64; PMID:2042971; http://dx.doi.org/10.1146/annurev.ph.53.030191.003001
  • Orlowski J, Grinstein S. Na+/H+ exchangers of mammalian cells. J Biol Chem 1997; 272:22373-6; PMID:9278382; http://dx.doi.org/10.1074/jbc.272.36.22373
  • Roos A, Boron WF. Intracellular pH. Physiol Rev 1981; 61:296-434; PMID:7012859
  • Alper SL. Molecular physiology of SLC4 anion exchangers. Exp Physiol 2006 ;91:153-61; PMID:16239253; http://dx.doi.org/10.1113/expphysiol.2005.031765
  • Romero MF, Fulton CM, Boron WF. The SLC4 family of HCO3− transporters. Pflugers Arch 2004; 447:495-509; PMID:14722772; http://dx.doi.org/10.1007/s00424-003-1180-2
  • Romero MF, Chen AP, Parker MD, Boron WF. The SLC4 family of bicarbonate (HCO3−/Cl−) transporters. Mol Aspects Med 2013; 34:159-82; PMID:23506864; http://dx.doi.org/10.1016/j.mam.2012.10.008
  • Phillips KP, Baltz JM. Intracellular pH regulation by HCO3−/Cl− exchange is activated during early mouse zygote development. Dev Biol 1999; 208:392-405; PMID:10191053; http://dx.doi.org/10.1006/dbio.1999.9199
  • Zhao Y, Chauvet PJ, Alper SL, Baltz JM. Expression and function of bicarbonate/chloride exchangers in the preimplantation mouse embryo. J Biol Chem 1995; 270:24428-34; PMID:7592657; http://dx.doi.org/10.1074/jbc.270.41.24428
  • Erdogan S, FitzHarris G, Tartia AP, Baltz JM. Mechanisms regulating intracellular pH are activated during growth of the mouse oocyte coincident with acquisition of meiotic competence. Dev Biol 2005; 286:352-60; PMID:16150436; http://dx.doi.org/10.1016/j.ydbio.2005.08.009
  • Fitzharris G, Baltz JM. Granulosa cells regulate intracellular pH of the murine growing oocyte via gap junctions: development of independent homeostasis during oocyte growth. Development 2006; 133:591-9; PMID:16407396; http://dx.doi.org/10.1242/dev.02246
  • FitzHarris G, Siyanov V, Baltz JM. Granulosa cells regulate oocyte intracellular pH against acidosis in preantral follicles by multiple mechanisms. Development 2007; 134:4283-95; PMID:17978006; http://dx.doi.org/10.1242/dev.005272
  • Phillips KP, Petrunewich MA, Collins JL, Baltz JM. The intracellular pH-regulatory HCO3−/Cl− exchanger in the mouse oocyte is inactivated during first meiotic metaphase and reactivated after egg activation via the MAP kinase pathway. Mol Biol Cell 2002; 13:3800-10; PMID:12429825; http://dx.doi.org/10.1091/mbc.E02-04-0242
  • Zhou C, Tiberi M, Liang B, Alper SL, Baltz JM. HCO3−/Cl− exchange inactivation and reactivation during mouse oocyte meiosis correlates with MEK/MAPK -regulated Ae2 plasma membrane localization. PLoS One 2009; 4:e7417; PMID:19823673; http://dx.doi.org/10.1371/journal.pone.0007417
  • FitzHarris G, Baltz JM. Regulation of intracellular pH during oocyte growth and maturation in mammals. Reproduction 2009; 138:619-27; PMID:19520797; http://dx.doi.org/10.1530/REP-09-0112
  • Merriman JA, Jennings PC, McLaughlin EA, Jones KT. Effect of aging on superovulation efficiency, aneuploidy rates, and sister chromatid cohesion in mice aged up to 15 months. Biol Reprod 2012; 86:49; PMID:22053097; http://dx.doi.org/10.1095/biolreprod.111.095711
  • Shomper M, Lappa C, FitzHarris G. Kinetochore microtubule establishment is defective in oocytes from aged mice. Cell Cycle 2014; 13:1171-9; PMID:24553117; http://dx.doi.org/10.4161/cc.28046
  • Damaghi M, Wojtkowiak JW, Gillies RJ. pH sensing and regulation in cancer. Front Physiol 2013; 4:370; PMID:24381558; http://dx.doi.org/10.3389/fphys.2013.00370
  • Steuerwald N, Cohen J, Herrera RJ, Sandalinas M, Brenner CA. Association between spindle assembly chechpoint expression and maternal age in human oocytes. Mol Hum Reprod 2001; 7:49-55; PMID:11134360; http://dx.doi.org/10.1093/molehr/7.1.49
  • Bavister B. Culture of preimpantation embryos: facts and artifacts. Hum Reprod Update 1995; 1:91-148; PMID:15726768; http://dx.doi.org/10.1093/humupd/1.2.91
  • Grinstein S, Rotin D, Mason MJ. Na+/H+ exchange and growth factor-induced cytosolic pH changes. Role in cellular proliferation. Biochim Biophys Acta 1989; 988:73-97; PMID:2535787; http://dx.doi.org/10.1016/0304-4157(89)90004-X
  • Kapus A, Grinstein S, Wasan S, Kandasamy R, Orlowski J. Functional characterization of three isoforms of the Na+/H+ exchanger stably expressed in Chinese hamster ovary cells. ATP dependence, osmotic sensitivity, and role in cell proliferation. J Biol Chem 1994; 269:23544-52; PMID:8089122
  • Schonichen A, Webb BA, Jacobson MP, Barber DL. Considering protonation as a posttranslational modification regulating protein structure and function. Annu Rev Biophys 2013; 42:289-314; PMID:23451893; http://dx.doi.org/10.1146/annurev-biophys-050511-102349
  • Tachibana-Konwalski K, Godwin J, van der Weyden L, Champion L, Kudo NR, Adams DJ, Nasmyth K. Rec8-containing cohesin maintains bivalents without turnover during the growing phase of mouse oocytes. Genes Dev 2010; 24:2505-16; PMID:20971813; http://dx.doi.org/10.1101/gad.605910
  • Lister LM, Kouznetsova A, Hyslop LA, Kalleas D, Pace SL, Barel JC, Nathan A, Floros V, Adelfalk C, Watanabe Y, et al. Age-related meiotic segregation errors in mammalian oocytes are preceded by depletion of cohesin and Sgo2. Curr Biol 2010; 20:1511-21; PMID:20817533; http://dx.doi.org/10.1016/j.cub.2010.08.023
  • Hodges CA, Revenkova E, Jessberger R, Hassold TJ, Hunt PA. SMC1beta-deficient female mice provide evidence that cohesins are a missing link in age-related nondisjunction. Nat Genet 2005; 37:1351-55; PMID:16258540; http://dx.doi.org/10.1038/ng1672
  • Lundback T, van Den Berg S, Hard T. Sequence-specific DNA binding by the glucocorticoid receptor DNA-binding domain is linked to a salt-dependent histidine protonation. Biochemistry 2000; 39:8909-16; PMID:10913303; http://dx.doi.org/10.1021/bi000231i
  • Lawitts JA, Biggers JD. Culture of preimplantation embryos. Methods Enzymol 1993; 225:153-64; PMID:8231853; http://dx.doi.org/10.1016/0076-6879(93)25012-Q
  • Dale B, Menezo Y, Cohen J, DiMatteo L, Wilding M. Intracellular PH regulation in the human oocyte. Hum Reprod 1998; 13:964-70; PMID:9619555; http://dx.doi.org/10.1093/humrep/13.4.964
  • Baltz JM, Biggers JD, Lechene C. Apparent absence of Na+/H+ antiport activity in the two- cell mouse embryo. Dev Biol 1990; 138:421-9; PMID:2156738; http://dx.doi.org/10.1016/0012-1606(90)90208-Z
  • Nord EP, Brown SE, Crandall ED. Cl−/HCO3− exchange modulates intracellular pH in rat type II alveolar epithelial cells. J Biol Chem 1988; 263:5599-606; PMID:3356700
  • Cheng JM, Jia BY, Wu TY, Zhou GB, Hou YP, Fu XW, Zhu SE. Effects of vitrification for germinal vesicle and metaphase II oocytes on subsequent centromere cohesion and chromosome aneuploidy in mice. Theriogenology 2014; 82:495-500; PMID:24930605; http://dx.doi.org/10.1016/j.theriogenology.2014.05.009
  • Hodges CA, Hunt PA. Simultaneous analysis of chromosomes and chromosome-associated proteins in mammalian oocytes and embryos. Chromosoma 2002; 111:165-9; PMID:12355205; http://dx.doi.org/10.1007/s00412-002-0195-3
  • Su YQ, Sugiura K, Woo Y, Wigglesworth K, Kamdar S, Affourtit J, Eppig JJ. Selective degradation of transcripts during meiotic maturation of mouse oocytes. Dev Biol 2007; 302:104-17; PMID:17022963; http://dx.doi.org/10.1016/j.ydbio.2006.09.008

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