Mitochondrial regulation of [Ca²⁺]i oscillations during cell cycle resumption of the second meiosis of oocyte

References

• Chow KM, Cheung MC, Cheung IK. Psychosocial interventions for infertile couples: a critical review. J Clin Nurs. 2016 Aug;25(15–16):2101–2113. PubMed PMID: 27278496.
   PubMed Web of Science ®Google Scholar
• Schatten H, Sun QY, Prather R. The impact of mitochondrial function/dysfunction on IVF and new treatment possibilities for infertility. Reprod Biol Endocrinol. 2014 Nov 24;12:111. PubMed PMID: 25421171; PubMed Central PMCID: PMCPMC4297407.
   PubMed Web of Science ®Google Scholar
• Stricker SA. Comparative biology of calcium signaling during fertilization and egg activation in animals. Dev Biol. 1999 Jul 15;211(2):157–176. PubMed PMID: 10395780.
   PubMed Web of Science ®Google Scholar
• Wakai T, Zhang N, Vangheluwe P, et al. Regulation of endoplasmic reticulum Ca(2+) oscillations in mammalian eggs. J Cell Sci. 2013 Dec 15;126(Pt 24):5714–5724. PubMed PMID: 24101727; PubMed Central PMCID: PMCPMC3860313.
   PubMed Web of Science ®Google Scholar
• Yazawa H, Yanagida K, Sato A. Human round spermatids from azoospermic men exhibit oocyte-activation and Ca2+ oscillation-inducing activities. Zygote. 2007 Nov;15(4):337–346. PubMed PMID: 17967213.
   PubMed Web of Science ®Google Scholar
• Morrill GA, Kostellow AB, Mahajan S, et al. Role of calcium in regulating intracellular pH following the stepwise release of the metabolic blocks at first-meiotic prophase and second-meiotic metaphase in amphibian oocytes. Biochim Biophys Acta. 1984 May 22;804(1):107–117. PubMed PMID: 6609721.
   PubMedGoogle Scholar
• Deng MQ, Fan BQ. Intracellular Ca2+ during fertilization and artificial activation in mouse oocytes. Zhongguo Yao Li Xue Bao. 1996 Jul;17(4):357–360. PubMed PMID: 9812724.
   PubMed Web of Science ®Google Scholar
• Jungheim ES, Travieso JL, Hopeman MM. Weighing the impact of obesity on female reproductive function and fertility. Nutr Rev. 2013 Oct;71 Suppl 1:S3–8. PubMed PMID: 24147921; PubMed Central PMCID: PMCPMC3813308.
   PubMed Web of Science ®Google Scholar
• Bustos G, Cruz P, Lovy A, et al. Endoplasmic reticulum-mitochondria calcium communication and the regulation of mitochondrial metabolism in cancer: a novel potential target. Front Oncol. 2017;7:199. PubMed PMID: 28944215; PubMed Central PMCID: PMCPMC5596064.
   PubMed Web of Science ®Google Scholar
• Hajnoczky G, Robb-Gaspers LD, Seitz MB, et al. Decoding of cytosolic calcium oscillations in the mitochondria. Cell. 1995 Aug 11;82(3):415–424. PubMed PMID: 7634331.
   PubMed Web of Science ®Google Scholar
• Boulais M, Soudant P, Le Goic N, et al. Involvement of mitochondrial activity and OXPHOS in ATP synthesis during the motility phase of spermatozoa in the pacific oyster, crassostrea gigas. Biol Reprod. 2015 Nov;93(5):118. PubMed PMID: 26423125.
   PubMed Web of Science ®Google Scholar
• Pedriali G, Rimessi A, Sbano L, et al. Regulation of endoplasmic reticulum-mitochondria Ca(2+) transfer and its importance for anti-cancer therapies. Front Oncol. 2017;7:180. PubMed PMID: 28913175; PubMed Central PMCID: PMCPMC5583168.
   PubMed Web of Science ®Google Scholar
• Van Blerkom J. Mitochondrial function in the human oocyte and embryo and their role in developmental competence. Mitochondrion. 2011 Sep;11(5):797–813. PubMed PMID: 20933103.
   PubMed Web of Science ®Google Scholar
• Adeva-Andany MM, Calvo-Castro I, Fernandez-Fernandez C, et al. Significance of l-carnitine for human health. IUBMB Life. 2017 Aug;69(8):578–594. PubMed PMID: 28653367.
   PubMed Web of Science ®Google Scholar
• Chung J, Nguyen AK, Henstridge DC, et al. HSP72 protects against obesity-induced insulin resistance. Proc Natl Acad Sci U S A. 2008 Feb 5;105(5):1739–1744. PubMed PMID: 18223156; PubMed Central PMCID: PMCPMC2234214.
   PubMed Web of Science ®Google Scholar
• Gehrig SM, van der Poel C, Sayer TA, et al. Hsp72 preserves muscle function and slows progression of severe muscular dystrophy. Nature. 2012 Apr 4;484(7394):394–398. PubMed PMID: 22495301.
   PubMed Web of Science ®Google Scholar
• Literati-Nagy B, Kulcsar E, Literati-Nagy Z, et al. Improvement of insulin sensitivity by a novel drug, BGP-15, in insulin-resistant patients: a proof of concept randomized double-blind clinical trial. Horm Metab Res. 2009 May;41(5):374–380. PubMed PMID: 19214941.
   PubMed Web of Science ®Google Scholar
• Nagy G, Szarka A, Lotz G, et al. BGP-15 inhibits caspase-independent programmed cell death in acetaminophen-induced liver injury. Toxicol Appl Pharmacol. 2010 Feb 15;243(1):96–103. PubMed PMID: 19931551.
   PubMed Web of Science ®Google Scholar
• Wu LL, Russell DL, Wong SL, et al. Mitochondrial dysfunction in oocytes of obese mothers: transmission to offspring and reversal by pharmacological endoplasmic reticulum stress inhibitors. Development. 2015 Feb 15;142(4):681–691. PubMed PMID: 25670793.
   PubMed Web of Science ®Google Scholar
• Fathi M, El-Shahat KH. L-carnitine enhances oocyte maturation and improves in vitro development of embryos in dromedary camels (Camelus dromedaries). Theriogenology. 2017 Aug 04;104:18–22. PubMed PMID: 28802113.
   PubMed Web of Science ®Google Scholar
• Ohlen SB, Russell ML, Brownstein MJ, et al. BGP-15 prevents the death of neurons in a mouse model of familial dysautonomia. Proc Natl Acad Sci U S A. 2017 May 9;114(19):5035–5040. PubMed PMID: 28439028; PubMed Central PMCID: PMCPMC5441694.
   PubMed Web of Science ®Google Scholar
• Minge CE, Bennett BD, Norman RJ, et al. Peroxisome proliferator-activated receptor-gamma agonist rosiglitazone reverses the adverse effects of diet-induced obesity on oocyte quality. Endocrinology. 2008 May;149(5):2646–2656. PubMed PMID: 18276752.
   PubMed Web of Science ®Google Scholar
• Igosheva N, Abramov AY, Poston L, et al. Maternal diet-induced obesity alters mitochondrial activity and redox status in mouse oocytes and zygotes. PLoS One. 2010 Apr 9;5(4):e10074. PubMed PMID: 20404917; PubMed Central PMCID: PMCPMC2852405.
   PubMed Web of Science ®Google Scholar
• Jungheim ES, Schoeller EL, Marquard KL, et al. Diet-induced obesity model: abnormal oocytes and persistent growth abnormalities in the offspring. Endocrinology. 2010 Aug;151(8):4039–4046. PubMed PMID: 20573727; PubMed Central PMCID: PMCPMC2940512.
   PubMed Web of Science ®Google Scholar
• Shankar K, Zhong Y, Kang P, et al. Maternal obesity promotes a proinflammatory signature in rat uterus and blastocyst. Endocrinology. 2011 Nov;152(11):4158–4170. PubMed PMID: 21862610; PubMed Central PMCID: PMCPMC3199010.
   PubMed Web of Science ®Google Scholar
• Luzzo KM, Wang Q, Purcell SH, et al. High fat diet induced developmental defects in the mouse: oocyte meiotic aneuploidy and fetal growth retardation/brain defects. PLoS One. 2012;7(11):e49217. PubMed PMID: 23152876; PubMed Central PMCID: PMCPMC3495769.
   PubMed Web of Science ®Google Scholar
• Gesink Law DC, Maclehose RF, Longnecker MP. Obesity and time to pregnancy. Hum Reprod. 2007 Feb;22(2):414–420. PubMed PMID: 17095518; PubMed Central PMCID: PMCPMC1924918.
   PubMed Web of Science ®Google Scholar
• Rittenberg V, Sobaleva S, Ahmad A, et al. Influence of BMI on risk of miscarriage after single blastocyst transfer. Hum Reprod. 2011 Oct;26(10):2642–2650. PubMed PMID: 21813669.
   PubMed Web of Science ®Google Scholar
• Ou XH, Sun QY. Mitochondrial replacement techniques or therapies (MRTs) to improve embryo development and to prevent mitochondrial disease transmission. J Genet Genomics. 2017 Aug 20;44(8):371–374. PubMed PMID: 28847473.
   PubMed Web of Science ®Google Scholar
• Ozil JP, Banrezes B, Toth S, et al. Ca2+ oscillatory pattern in fertilized mouse eggs affects gene expression and development to term. Dev Biol. 2006 Dec 15;300(2):534–544. PubMed PMID: 16996050.
   PubMed Web of Science ®Google Scholar
• Ducibella T, Huneau D, Angelichio E, et al. Egg-to-embryo transition is driven by differential responses to Ca(2+) oscillation number. Dev Biol. 2002 Oct 15;250(2):280–291. PubMed PMID: 12376103.
   PubMed Web of Science ®Google Scholar
• Bengtson CP, Bading H. Nuclear calcium signaling. Adv Exp Med Biol. 2012;970:377–405. PubMed PMID: 22351065.
   PubMed Web of Science ®Google Scholar
• Griffiths EJ, Rutter GA. Mitochondrial calcium as a key regulator of mitochondrial ATP production in mammalian cells. Biochim Biophys Acta. 2009 Nov;1787(11):1324–1333. PubMed PMID: 19366607.
   PubMed Web of Science ®Google Scholar
• Marchant JS, Ramos V, Parker I. Structural and functional relationships between Ca2+ puffs and mitochondria in Xenopus oocytes. Am J Physiol Cell Physiol. 2002 Jun;282(6):C1374–86. PubMed PMID: 11997252.
   PubMed Web of Science ®Google Scholar
• Gordo AC, Rodrigues P, Kurokawa M, et al. Intracellular calcium oscillations signal apoptosis rather than activation in in vitro aged mouse eggs. Biol Reprod. 2002 Jun;66(6):1828–1837. PubMed PMID: 12021069.
   PubMed Web of Science ®Google Scholar
• Ozil JP, Markoulaki S, Toth S, et al. Egg activation events are regulated by the duration of a sustained [Ca2+]cyt signal in the mouse. Dev Biol. 2005 Jun 1;282(1):39–54. PubMed PMID: 15936328.
   PubMed Web of Science ®Google Scholar
• Berridge MJ, Lipp P, Bootman MD. The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol. 2000 Oct;1(1):11–21. PubMed PMID: 11413485.
   PubMed Web of Science ®Google Scholar
• Bootman MD, Lipp P, Berridge MJ. The organisation and functions of local Ca(2+) signals. J Cell Sci. 2001 Jun;114(Pt 12):2213–2222. PubMed PMID: 11493661.
   PubMed Web of Science ®Google Scholar
• Hagen BM, Boyman L, Kao JP, et al. A comparative assessment of fluo Ca2+ indicators in rat ventricular myocytes. Cell Calcium. 2012 Aug;52(2):170–181. PubMed PMID: 22721780; PubMed Central PMCID: PMCPMC3393790.
   PubMed Web of Science ®Google Scholar
• Jones DP. Mitochondrial dysfunction during anoxia and acute cell injury. Biochim Biophys Acta. 1995 May 24;1271(1):29–33. PubMed PMID: 7599222.
   PubMed Web of Science ®Google Scholar
• Mehlmann LM, Kline D. Regulation of intracellular calcium in the mouse egg: calcium release in response to sperm or inositol trisphosphate is enhanced after meiotic maturation. Biol Reprod. 1994 Dec;51(6):1088–1098. PubMed PMID: 7888488.
   PubMed Web of Science ®Google Scholar
• Wakai T, Fissore RA. Ca(2+) homeostasis and regulation of ER Ca(2+) in mammalian oocytes/eggs. Cell Calcium. 2013 Jan;53(1):63–67. PubMed PMID: 23260016; PubMed Central PMCID: PMCPMC4120948.
   PubMed Web of Science ®Google Scholar
• Malhotra JD, Kaufman RJ. The endoplasmic reticulum and the unfolded protein response. Semin Cell Dev Biol. 2007 Dec;18(6):716–731. PubMed PMID: 18023214; PubMed Central PMCID: PMCPMC2706143.
   PubMed Web of Science ®Google Scholar
• Vannuvel K, Renard P, Raes M, et al. Functional and morphological impact of ER stress on mitochondria. J Cell Physiol. 2013 Sep;228(9):1802–1818. PubMed PMID: 23629871.
   PubMed Web of Science ®Google Scholar
• Dumollard R, Marangos P, Fitzharris G, et al. Sperm-triggered [Ca2+] oscillations and Ca2+ homeostasis in the mouse egg have an absolute requirement for mitochondrial ATP production. Development. 2004 Jul;131(13):3057–3067. PubMed PMID: 15163630.
   PubMed Web of Science ®Google Scholar
• Van Blerkom J, Davis PW, Lee J. ATP content of human oocytes and developmental potential and outcome after in-vitro fertilization and embryo transfer. Hum Reprod. 1995 Feb;10(2):415–424. PubMed PMID: 7769073.
   PubMed Web of Science ®Google Scholar
• Dumollard R, Duchen M, Carroll J. The role of mitochondrial function in the oocyte and embryo. Curr Top Dev Biol. 2007;77:21–49. PubMed PMID: 17222699.
   PubMed Web of Science ®Google Scholar
• Zhou X, Liu F, Zhai S. Effect of L-carnitine and/or L-acetyl-carnitine in nutrition treatment for male infertility: a systematic review. Asia Pac J Clin Nutr. 2007;16 Suppl 1:383–390. PubMed PMID: 17392136.
   PubMed Web of Science ®Google Scholar
• Vanella A, Russo A, Acquaviva R, et al. L -propionyl-carnitine as superoxide scavenger, antioxidant, and DNA cleavage protector. Cell Biol Toxicol. 2000;16(2):99–104. PubMed PMID: 10917565.
   PubMed Web of Science ®Google Scholar
• Gulcin I. Antioxidant and antiradical activities of L-carnitine. Life Sci. 2006 Jan 18;78(8):803–811. PubMed PMID: 16253281.
   PubMed Web of Science ®Google Scholar
• Pillich RT, Scarsella G, Risuleo G. Reduction of apoptosis through the mitochondrial pathway by the administration of acetyl-L-carnitine to mouse fibroblasts in culture. Exp Cell Res. 2005 May 15;306(1):1–8. PubMed PMID: 15878327.
   PubMed Web of Science ®Google Scholar
• Sharma S, Black SM. Carnitine homeostasis, mitochondrial function, and cardiovascular disease. Drug Discov Today Dis Mech. 2009;6(1–4):e31–e39. PubMed PMID: 20648231; PubMed Central PMCID: PMCPMC2905823.
   PubMedGoogle Scholar
• Nelson HK, Lauber RP, Sheard NF. Effect of various levels of supplementation with sodium pivalate on tissue carnitine concentrations and urinary excretion of carnitine in the rat. J Nutr Biochem. 2001 Apr;12(4):242–250. PubMed PMID: 11287220.
   PubMed Web of Science ®Google Scholar
• Jones LL, McDonald DA, Borum PR. Acylcarnitines: role in brain. Prog Lipid Res. 2010 Jan;49(1):61–75. PubMed PMID: 19720082.
   PubMed Web of Science ®Google Scholar
• Isidori AM, Pozza C, Gianfrilli D, et al. Medical treatment to improve sperm quality. Reprod Biomed Online. 2006 Jun;12(6):704–714. PubMed PMID: 16792845.
   PubMed Web of Science ®Google Scholar
• Mansour G, Abdelrazik H, Sharma RK, et al. L-carnitine supplementation reduces oocyte cytoskeleton damage and embryo apoptosis induced by incubation in peritoneal fluid from patients with endometriosis. Fertil Steril. 2009 May;91(5 Suppl):2079–2086. PubMed PMID: 18394615.
   PubMed Web of Science ®Google Scholar
• Jamilian H, Jamilian M, Samimi M, et al. Oral carnitine supplementation influences mental health parameters and biomarkers of oxidative stress in women with polycystic ovary syndrome: a randomized, double-blind, placebo-controlled trial. Gynecol Endocrinol. 2017 Jun;33(6):442–447. PubMed PMID: 28277138.
   PubMed Web of Science ®Google Scholar
• Hashimoto S. Application of in vitro maturation to assisted reproductive technology. J Reprod Dev. 2009 Feb;55(1):1–10. PubMed PMID: 19276618.
   PubMed Web of Science ®Google Scholar
• Gombos I, Crul T, Piotto S, et al. Membrane-lipid therapy in operation: the HSP co-inducer BGP-15 activates stress signal transduction pathways by remodeling plasma membrane rafts. PLoS One. 2011;6(12):e28818. PubMed PMID: 22174906; PubMed Central PMCID: PMCPMC3236211.
   PubMed Web of Science ®Google Scholar
• Henstridge DC, Bruce CR, Drew BG, et al. Activating HSP72 in rodent skeletal muscle increases mitochondrial number and oxidative capacity and decreases insulin resistance. Diabetes. 2014 Jun;63(6):1881–1894. PubMed PMID: 24430435; PubMed Central PMCID: PMCPMC4030108.
   PubMed Web of Science ®Google Scholar
• Sumegi K, Fekete K, Antus C, et al. BGP-15 protects against oxidative stress- or lipopolysaccharide-induced mitochondrial destabilization and reduces mitochondrial production of reactive oxygen species. PLoS One. 2017;12(1):e0169372. PubMed PMID: 28046125; PubMed Central PMCID: PMCPMC5207682.
   PubMed Web of Science ®Google Scholar
• Crul T, Toth N, Piotto S, et al. Hydroximic acid derivatives: pleiotropic HSP co-inducers restoring homeostasis and robustness. Curr Pharm Des. 2013;19(3):309–346. PubMed PMID: 22920902.
   PubMed Web of Science ®Google Scholar
• Literati-Nagy B, Tory K, Peitl B, et al. Improvement of insulin sensitivity by a novel drug candidate, BGP-15, in different animal studies. Metab Syndr Relat Disord. 2014 Mar;12(2):125–131. PubMed PMID: 24386957.
   PubMed Web of Science ®Google Scholar
• Salah H, Li M, Cacciani N, et al. The chaperone co-inducer BGP-15 alleviates ventilation-induced diaphragm dysfunction. Sci Transl Med. 2016 Aug 3;8(350):350ra103. PubMed PMID: 27488897.
   PubMed Web of Science ®Google Scholar
• Moawad AR, Xu B, Tan SL, et al. l-carnitine supplementation during vitrification of mouse germinal vesicle stage-oocytes and their subsequent in vitro maturation improves meiotic spindle configuration and mitochondrial distribution in metaphase II oocytes. Hum Reprod. 2014 Oct 10;29(10):2256–2268. PubMed PMID: 25113843.
   PubMed Web of Science ®Google Scholar
• Moawad AR, Tan SL, Xu B, et al. L-carnitine supplementation during vitrification of mouse oocytes at the germinal vesicle stage improves preimplantation development following maturation and fertilization in vitro. Biol Reprod. 2013 Apr;88(4):104. PubMed PMID: 23446455.
   PubMed Web of Science ®Google Scholar
• Greenfield A, Braude P, Flinter F, et al. Assisted reproductive technologies to prevent human mitochondrial disease transmission. Nat Biotechnol. 2017 Nov 9;35(11):1059–1068. PubMed PMID: 29121011.
   PubMed Web of Science ®Google Scholar
• Igarashi H, Takahashi T, Abe H, et al. Poor embryo development in post-ovulatory in vivo-aged mouse oocytes is associated with mitochondrial dysfunction, but mitochondrial transfer from somatic cells is not sufficient for rejuvenation. Hum Reprod. 2016 Oct;31(10):2331–2338. PubMed PMID: 27591230.
   PubMed Web of Science ®Google Scholar
• Meng TG, Hu MW, Ma XS, et al. Oocyte-specific deletion of furin leads to female infertility by causing early secondary follicle arrest in mice. Cell Death Dis. 2017 Jun 1;8(6):e2846. PubMed PMID: 28569793; PubMed Central PMCID: PMCPMC5520891.
   PubMedGoogle Scholar
• Liu Y, Han M, Li X, et al. Age-related changes in the mitochondria of human mural granulosa cells. Hum Reprod. 2017 Dec 1;32(12):2465–2473. PubMed PMID: 29045673.
   PubMed Web of Science ®Google Scholar
• Yoon SY, Eum JH, Lee JE, et al. Recombinant human phospholipase C zeta 1 induces intracellular calcium oscillations and oocyte activation in mouse and human oocytes. Hum Reprod. 2012 Jun;27(6):1768–1780. PubMed PMID: 22456923.
   PubMed Web of Science ®Google Scholar