Sirtuins在卵母细胞成熟过程中的作用
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摘要
卵母细胞成熟包括细胞核和细胞质成熟。核成熟主要涉及染色体的分离,细胞质成熟囊括了一系列复杂的过程。Sirtuins是NAD~+依赖的组蛋白去乙酰酶家族,其中,SIRT1、SIRT2、SIRT3、SIRT4、SIRT6、SIRT7均和减数分裂相关。现综述了卵母细胞成熟过程中细胞核成熟和细胞质成熟的变化及sirtuins在卵母细胞成熟过程中的作用,并总结了sirtuins与老龄鼠卵母细胞成熟异常的关系。
Oocyte maturation includes nuclear maturation and cytoplasmic maturation. Nuclear maturation mainly involves chromosome segregation, and cytoplasmic maturation encompasses a complex set of processes. Sirtuins are NAD~+-dependent histone deacetylase families, in which SIRT1, SIRT2, SIRT3, SIRT4, SIRT6 and SIRT7 are all associated with meiosis. This review summarized the changes in nuclear maturation and cytoplasmic maturation during oocyte maturation and the role of sirtuins in oocyte maturation. Finally, the defects of maturation oocytes from aged mice and the possibility of saving these problems through sirtuins were discussed.
Oocyte maturation includes nuclear maturation and cytoplasmic maturation. Nuclear maturation mainly involves chromosome segregation, and cytoplasmic maturation encompasses a complex set of processes. Sirtuins are NAD~+-dependent histone deacetylase families, in which SIRT1, SIRT2, SIRT3, SIRT4, SIRT6 and SIRT7 are all associated with meiosis. This review summarized the changes in nuclear maturation and cytoplasmic maturation during oocyte maturation and the role of sirtuins in oocyte maturation. Finally, the defects of maturation oocytes from aged mice and the possibility of saving these problems through sirtuins were discussed.
引文
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[2]Liang CG,Su YQ,Fan HY,et al.Mechanisms regulating oocyte meiotic resumption:roles of mitogen-activated protein kinase.Mol Endocrinol,2007,21:2037-55
[3]Houtkooper RH,Pirinen E,Auwerx J.Sirtuins as regulators of metabolism and healthspan.Nat Rev Mol Cell Biol,2012,13:225-38
[4]Tatone C,Di Emidio G,Vitti M,et al.Sirtuin functions in female fertility:possible role in oxidative stress and aging.Oxid Med Cell Longev,2015,2015:659687
[5]Pucci B,Villanova L,Sansone L,et al.Sirtuins:the molecular basis of beneficial effects of physical activity.Intern Emerg Med,2013,8:S23-5
[6]Imai S,Guarente L.Ten years of nad-dependent sir2family deacetylases:implications for metabolic diseases.Trends Pharmacol Sci,2010,31:212-20
[7]Zeng J,Jiang M,Wu X,et al.Sirt4 is essential for metabolic control and meiotic structure during mouse oocyte maturation.Aging Cell,2018,17:e12789
[8]Benkhalifa M,Ferreira YJ,Chahine H,et al.Mitochondria:participation to infertility as source of energy and cause of senescence.Int J Biochem Cell Biol,2014,55:60-4
[9]Zhang L,Han L,Ma R,et al.Sirt3 prevents maternal obesity-associated oxidative stress and meiotic defects in mouse oocytes.Cell Cycle,2015,14:2959-68
[10]Gao M,Li X,He Y,et al.Sirt7 functions in redox homeostasis and cytoskeletal organization during oocyte maturation.FASEB J,2018,[Epub ahead of print]
[11]Han L,Ge J,Zhang L,et al.Sirt6 depletion causes spindle defects and chromosome misalignment during meiosis of mouse oocyte.Sci Rep,2015,5:15366
[12]Zhang J,Fang L,Lu Z,et al.Are sirtuins markers of ovarian aging?Gene,2016,575:680-6
[13]Rodrigues P,Limback D,McGinnis LK,et al.Oogenesis:prospects and challenges for the future.J Cell Physiol,2008,216:355-65
[14]Moor RM,Dai Y,Lee C,et al.Oocyte maturation and embryonic failure.Hum Reprod Update,1998,4:223-36
[15]Kupker W,Diedrich K,Edwards RG.Principles of mammalian fertilization.Hum Reprod,1998,13:20-32
[16]Li R,Albertini DF.The road to maturation:somatic cell interaction and self-organization of the mammalian oocyte.Nat Rev Mol Cell Biol,2013,14:141-52
[17]Sun QY,Miao YL,Schatten H.Towards a new understanding on the regulation of mammalian oocyte meiosis resumption.Cell Cycle,2009,8:2741-7
[18]Reyes JM,Ross PJ.Cytoplasmic polyadenylation in mammalian oocyte maturation.Wiley Interdiscip Rev RNA,2016,7:71-89
[19]Gu L,Wang Q,Sun QY.Histone modifications during mammalian oocyte maturation:dynamics,regulation and functions.Cell Cycle,2010,9:1942-50
[20]Dehapiot B,Carriere V,Carroll J,et al.Polarized Cdc42activation promotes polar body protrusion and asymmetric division in mouse oocytes.Dev Biol,2013,377:202-12
[21]Stojkovic M,Machado SA,Stojkovic P,et al.Mitochondrial distribution and adenosine triphosphate content of bovine oocytes before and after in vitro maturation:correlation with morphological criteria and developmental capacity after in vitro fertilization and culture.Biol Reprod,2001,64:904-9
[22]Dumollard R,Duchen M,Sardet C.Calcium signals and mitochondria at fertilisation.Semin Cell Dev Biol,2006,17:314-23
[23]Moreno RD,Schatten G,Ramalho-Santos J.Golgi apparatus dynamics during mouse oocyte in vitro maturation:effect of the membrane trafficking inhibitor brefeldin A.Biol Reprod,2002,66:1259-66
[24]FitzHarris G,Marangos P,Carroll J.Changes in endoplasmic reticulum structure during mouse oocyte maturation are controlled by the cytoskeleton and cytoplasmic dynein.Dev Biol,2007,305:133-44
[25]Gumus E,Bulut HE,Kaloglu C.Cytoskeletal changes in oocytes and early embryos during in vitro fertilization process in mice.Anat Histol Embryol,2010,39:51-8
[26]Takeo S,Sato D,Kimura K,et al.Resveratrol improves the mitochondrial function and fertilization outcome of bovine oocytes.J Reprod Dev,2014,60:92-9
[27]Di Emidio G,Falone S,Vitti M,et al.Sirt1 signalling protects mouse oocytes against oxidative stress and is deregulated during aging.Hum Reprod,2014,29:2006-17
[28]Zhang L,Hou X,Ma R,et al.Sirt2 functions in spindle organization and chromosome alignment in mouse oocyte meiosis.FASEB J,2014,28:1435-45
[29]Tseng AH,Shieh SS,Wang DL.SIRT3 deacetylates FOXO3 to protect mitochondria against oxidative damage.Free Radic Biol Med,2013,63:222-34
[30]Liu B,Che W,Zheng C,et al.Sirt5:a safeguard against oxidative stress-induced apoptosis in cardiomyocytes.Cell Physiol Biochem,2013,32:1050-9
[31]Rogina B,Helfand SL.Sir2 mediates longevity in the fly through a pathway related to calorie restriction.Proc Natl Acad Sci USA,2004,101:15998-6003
[32]Caito S,Rajendrasozhan S,Cook S,et al.Sirt1 is a redoxsensitive deacetylase that is post-translationally modified by oxidants and carbonyl stress.FASEB J,2010,24:3145-59
[33]Zhong L,Mostoslavsky R.Fine tuning our cellular factories:sirtuins in mitochondrial biology.Cell Metab,2011,13:621-6
[34]Kottarathil VD,Antony MA,Nair IR,et al.Recent advances in granulosa cell tumor ovary:a review.Indian JSurg Oncol,2013,4:37-47
[35]Pavlova S,Klucska K,Vasicek D,et al.The involvement of sirt1 and transcription factor NF-κB(p50/p65)in regulation of porcine ovarian cell function.Anim Reprod Sci,2013,140:180-8
[36]North BJ,Verdin E.Interphase nucleo-cytoplasmic shuttling and localization of sirt2 during mitosis.PLoSOne,2007,2:e784
[37]Ma P,Schultz RM.Histone deacetylase 2(hdac2)regulates chromosome segregation and kinetochore function via H4K16 deacetylation during oocyte maturation in mouse.PLoS Genet,2013,9:e1003377
[38]Bause AS,Haigis MC.Sirt3 regulation of mitochondrial oxidative stress.Exp Gerontol,2013 48:634-9
[39]Rardin MJ,Newman JC,Held JM,et al.Label-free quantitative proteomics of the lysine acetylome in mitochondria identifies substrates of sirt3 in metabolic pathways.Proc Natl Acad Sci USA,2013,110:6601-6.
[40]Someya S,Yu W,Hallows WC,et al.Sirt3 mediates reduction of oxidative damage and prevention of agerelated hearing loss under caloric restriction.Cell,2010,143:802-12
[41]Chen Y,Zhang J,Lin Y,et al.Tumour suppressor SIRT3deacetylates and activates manganese superoxide dismutase to scavenge ROS.EMBO Rep,2011,12:534-41
[42]Zhao HC,Ding T,Ren Y,et al.Role of Sirt3 in mitochondrial biogenesis and developmental competence of human in vitro matured oocytes.Hum Reprod,2016,31:607-22
[43]Kawamura Y,Uchijima Y,Horike N,et al.Sirt3 protects in vitro-fertilized mouse preimplantation embryos against oxidative stress-induced p53-mediated developmental arrest.J Clin Invest,2010,120:2817-28
[44]Grabowska W,Sikora E,Bielak-Zmijewska A.Sirtuins,a promising target in slowing down the ageing process.Biogerontology,2017,18:447-76
[45]Anderson KA,Huynh FK,Fisher-Wellman K,et al.Sirt4is a lysine deacylase that controls leucine metabolism and insulin secretion.Cell Metab,2017,25:838-55
[46]Watroba M,Szukiewicz D.The role of sirtuins in aging and age-related diseases.Adv Med Sci,2016,61:52-62
[47]Luo YX,Tang X,An XZ,et al.Sirt4 accelerates ang iiinduced pathological cardiac hypertrophy by inhibiting manganese superoxide dismutase activity.Eur Heart J,2017,38:1389-98
[48]Mostoslavsky R,Chua KF,Lombard DB,et al.Genomic instability and aging-like phenotype in the absence of mammalian sirt6.Cell,2006,124:315-29
[49]Michishita E,McCord RA,Boxer LD,et al.Cell cycledependent deacetylation of telomeric histone H3 lysine K56 by human SIRT6.Cell Cycle,2009,8:2664-6
[50]Ford E,Voit R,Liszt G,et al.Mammalian Sir2 homolog SIRT7 is an activator of RNA polymerase I transcription.Genes Dev,2006,20:1075-80
[51]Ryu D,Jo YS,Lo Sasso G,et al.A SIRT7-dependent acetylation switch of GABPβ1 controls mitochondrial function.Cell Metab,2014,20:856-69
[52]Singh CK,Chhabra G,Ndiaye MA,et al.The role of sirtuins in antioxidant and redox signaling.Antioxid Redox Signal,2018,28:643-61
[53]Vakhrusheva O,Smolka C,Gajawada P,et al.Sirt7increases stress resistance of cardiomyocytes and prevents apoptosis and inflammatory cardiomyopathy in mice.Circ Res,2008,102:703-10
[54]Pellestor F,Andreo B,Arnal F,et al.Maternal aging and chromosomal abnormalities:new data drawn from in vitro unfertilized human oocytes.Hum Genet,2003,112:195-203
[55]Lee SE,Kim JH,Kim NH.Inactivation of mapk affects centrosome assembly,but not actin filament assembly,in mouse oocytes maturing in vitro.Mol Reprod Dev,2007,74:904-11
[56]Kansaku K,Takeo S,Itami N,et al.Maternal aging affects oocyte resilience to carbonyl cyanide-m-chlorophenylhydrazone-induced mitochondrial dysfunction in cows.PLoS One,2017,12:e0188099
[57]Jones KT,Lane SI.Molecular causes of aneuploidy in mammalian eggs.Development,2013,140:3719-30
[58]MacLennan M,Crichton JH,Playfoot CJ,et al.Oocyte development,meiosis and aneuploidy.Semin Cell Dev Biol,2015,45:68-76
[59]Yue MX,Fu XW,Zhou GB,et al.Abnormal DNAmethylation in oocytes could be associated with a decrease in reproductive potential in old mice.J Assist Reprod Genet,2012,29:643-50
[60]Suo L,Meng QG,Pei Y,et al.Changes in acetylation on lysine 12 of histone h4(acH4K12)of murine oocytes during maternal aging may affect fertilization and subsequent embryo development.Fertil Steril,2010,93:945-51
[61]Steuerwald NM,Bermudez MG,Wells D,et al.Maternal age-related differential global expression profiles observed in human oocytes.Reprod Biomed Online,2007,14:700-8
[62]Liu M,Yin Y,Ye X,et al.Resveratrol protects against ageassociated infertility in mice.Hum Reprod,2013,28:707-17
[2]Liang CG,Su YQ,Fan HY,et al.Mechanisms regulating oocyte meiotic resumption:roles of mitogen-activated protein kinase.Mol Endocrinol,2007,21:2037-55
[3]Houtkooper RH,Pirinen E,Auwerx J.Sirtuins as regulators of metabolism and healthspan.Nat Rev Mol Cell Biol,2012,13:225-38
[4]Tatone C,Di Emidio G,Vitti M,et al.Sirtuin functions in female fertility:possible role in oxidative stress and aging.Oxid Med Cell Longev,2015,2015:659687
[5]Pucci B,Villanova L,Sansone L,et al.Sirtuins:the molecular basis of beneficial effects of physical activity.Intern Emerg Med,2013,8:S23-5
[6]Imai S,Guarente L.Ten years of nad-dependent sir2family deacetylases:implications for metabolic diseases.Trends Pharmacol Sci,2010,31:212-20
[7]Zeng J,Jiang M,Wu X,et al.Sirt4 is essential for metabolic control and meiotic structure during mouse oocyte maturation.Aging Cell,2018,17:e12789
[8]Benkhalifa M,Ferreira YJ,Chahine H,et al.Mitochondria:participation to infertility as source of energy and cause of senescence.Int J Biochem Cell Biol,2014,55:60-4
[9]Zhang L,Han L,Ma R,et al.Sirt3 prevents maternal obesity-associated oxidative stress and meiotic defects in mouse oocytes.Cell Cycle,2015,14:2959-68
[10]Gao M,Li X,He Y,et al.Sirt7 functions in redox homeostasis and cytoskeletal organization during oocyte maturation.FASEB J,2018,[Epub ahead of print]
[11]Han L,Ge J,Zhang L,et al.Sirt6 depletion causes spindle defects and chromosome misalignment during meiosis of mouse oocyte.Sci Rep,2015,5:15366
[12]Zhang J,Fang L,Lu Z,et al.Are sirtuins markers of ovarian aging?Gene,2016,575:680-6
[13]Rodrigues P,Limback D,McGinnis LK,et al.Oogenesis:prospects and challenges for the future.J Cell Physiol,2008,216:355-65
[14]Moor RM,Dai Y,Lee C,et al.Oocyte maturation and embryonic failure.Hum Reprod Update,1998,4:223-36
[15]Kupker W,Diedrich K,Edwards RG.Principles of mammalian fertilization.Hum Reprod,1998,13:20-32
[16]Li R,Albertini DF.The road to maturation:somatic cell interaction and self-organization of the mammalian oocyte.Nat Rev Mol Cell Biol,2013,14:141-52
[17]Sun QY,Miao YL,Schatten H.Towards a new understanding on the regulation of mammalian oocyte meiosis resumption.Cell Cycle,2009,8:2741-7
[18]Reyes JM,Ross PJ.Cytoplasmic polyadenylation in mammalian oocyte maturation.Wiley Interdiscip Rev RNA,2016,7:71-89
[19]Gu L,Wang Q,Sun QY.Histone modifications during mammalian oocyte maturation:dynamics,regulation and functions.Cell Cycle,2010,9:1942-50
[20]Dehapiot B,Carriere V,Carroll J,et al.Polarized Cdc42activation promotes polar body protrusion and asymmetric division in mouse oocytes.Dev Biol,2013,377:202-12
[21]Stojkovic M,Machado SA,Stojkovic P,et al.Mitochondrial distribution and adenosine triphosphate content of bovine oocytes before and after in vitro maturation:correlation with morphological criteria and developmental capacity after in vitro fertilization and culture.Biol Reprod,2001,64:904-9
[22]Dumollard R,Duchen M,Sardet C.Calcium signals and mitochondria at fertilisation.Semin Cell Dev Biol,2006,17:314-23
[23]Moreno RD,Schatten G,Ramalho-Santos J.Golgi apparatus dynamics during mouse oocyte in vitro maturation:effect of the membrane trafficking inhibitor brefeldin A.Biol Reprod,2002,66:1259-66
[24]FitzHarris G,Marangos P,Carroll J.Changes in endoplasmic reticulum structure during mouse oocyte maturation are controlled by the cytoskeleton and cytoplasmic dynein.Dev Biol,2007,305:133-44
[25]Gumus E,Bulut HE,Kaloglu C.Cytoskeletal changes in oocytes and early embryos during in vitro fertilization process in mice.Anat Histol Embryol,2010,39:51-8
[26]Takeo S,Sato D,Kimura K,et al.Resveratrol improves the mitochondrial function and fertilization outcome of bovine oocytes.J Reprod Dev,2014,60:92-9
[27]Di Emidio G,Falone S,Vitti M,et al.Sirt1 signalling protects mouse oocytes against oxidative stress and is deregulated during aging.Hum Reprod,2014,29:2006-17
[28]Zhang L,Hou X,Ma R,et al.Sirt2 functions in spindle organization and chromosome alignment in mouse oocyte meiosis.FASEB J,2014,28:1435-45
[29]Tseng AH,Shieh SS,Wang DL.SIRT3 deacetylates FOXO3 to protect mitochondria against oxidative damage.Free Radic Biol Med,2013,63:222-34
[30]Liu B,Che W,Zheng C,et al.Sirt5:a safeguard against oxidative stress-induced apoptosis in cardiomyocytes.Cell Physiol Biochem,2013,32:1050-9
[31]Rogina B,Helfand SL.Sir2 mediates longevity in the fly through a pathway related to calorie restriction.Proc Natl Acad Sci USA,2004,101:15998-6003
[32]Caito S,Rajendrasozhan S,Cook S,et al.Sirt1 is a redoxsensitive deacetylase that is post-translationally modified by oxidants and carbonyl stress.FASEB J,2010,24:3145-59
[33]Zhong L,Mostoslavsky R.Fine tuning our cellular factories:sirtuins in mitochondrial biology.Cell Metab,2011,13:621-6
[34]Kottarathil VD,Antony MA,Nair IR,et al.Recent advances in granulosa cell tumor ovary:a review.Indian JSurg Oncol,2013,4:37-47
[35]Pavlova S,Klucska K,Vasicek D,et al.The involvement of sirt1 and transcription factor NF-κB(p50/p65)in regulation of porcine ovarian cell function.Anim Reprod Sci,2013,140:180-8
[36]North BJ,Verdin E.Interphase nucleo-cytoplasmic shuttling and localization of sirt2 during mitosis.PLoSOne,2007,2:e784
[37]Ma P,Schultz RM.Histone deacetylase 2(hdac2)regulates chromosome segregation and kinetochore function via H4K16 deacetylation during oocyte maturation in mouse.PLoS Genet,2013,9:e1003377
[38]Bause AS,Haigis MC.Sirt3 regulation of mitochondrial oxidative stress.Exp Gerontol,2013 48:634-9
[39]Rardin MJ,Newman JC,Held JM,et al.Label-free quantitative proteomics of the lysine acetylome in mitochondria identifies substrates of sirt3 in metabolic pathways.Proc Natl Acad Sci USA,2013,110:6601-6.
[40]Someya S,Yu W,Hallows WC,et al.Sirt3 mediates reduction of oxidative damage and prevention of agerelated hearing loss under caloric restriction.Cell,2010,143:802-12
[41]Chen Y,Zhang J,Lin Y,et al.Tumour suppressor SIRT3deacetylates and activates manganese superoxide dismutase to scavenge ROS.EMBO Rep,2011,12:534-41
[42]Zhao HC,Ding T,Ren Y,et al.Role of Sirt3 in mitochondrial biogenesis and developmental competence of human in vitro matured oocytes.Hum Reprod,2016,31:607-22
[43]Kawamura Y,Uchijima Y,Horike N,et al.Sirt3 protects in vitro-fertilized mouse preimplantation embryos against oxidative stress-induced p53-mediated developmental arrest.J Clin Invest,2010,120:2817-28
[44]Grabowska W,Sikora E,Bielak-Zmijewska A.Sirtuins,a promising target in slowing down the ageing process.Biogerontology,2017,18:447-76
[45]Anderson KA,Huynh FK,Fisher-Wellman K,et al.Sirt4is a lysine deacylase that controls leucine metabolism and insulin secretion.Cell Metab,2017,25:838-55
[46]Watroba M,Szukiewicz D.The role of sirtuins in aging and age-related diseases.Adv Med Sci,2016,61:52-62
[47]Luo YX,Tang X,An XZ,et al.Sirt4 accelerates ang iiinduced pathological cardiac hypertrophy by inhibiting manganese superoxide dismutase activity.Eur Heart J,2017,38:1389-98
[48]Mostoslavsky R,Chua KF,Lombard DB,et al.Genomic instability and aging-like phenotype in the absence of mammalian sirt6.Cell,2006,124:315-29
[49]Michishita E,McCord RA,Boxer LD,et al.Cell cycledependent deacetylation of telomeric histone H3 lysine K56 by human SIRT6.Cell Cycle,2009,8:2664-6
[50]Ford E,Voit R,Liszt G,et al.Mammalian Sir2 homolog SIRT7 is an activator of RNA polymerase I transcription.Genes Dev,2006,20:1075-80
[51]Ryu D,Jo YS,Lo Sasso G,et al.A SIRT7-dependent acetylation switch of GABPβ1 controls mitochondrial function.Cell Metab,2014,20:856-69
[52]Singh CK,Chhabra G,Ndiaye MA,et al.The role of sirtuins in antioxidant and redox signaling.Antioxid Redox Signal,2018,28:643-61
[53]Vakhrusheva O,Smolka C,Gajawada P,et al.Sirt7increases stress resistance of cardiomyocytes and prevents apoptosis and inflammatory cardiomyopathy in mice.Circ Res,2008,102:703-10
[54]Pellestor F,Andreo B,Arnal F,et al.Maternal aging and chromosomal abnormalities:new data drawn from in vitro unfertilized human oocytes.Hum Genet,2003,112:195-203
[55]Lee SE,Kim JH,Kim NH.Inactivation of mapk affects centrosome assembly,but not actin filament assembly,in mouse oocytes maturing in vitro.Mol Reprod Dev,2007,74:904-11
[56]Kansaku K,Takeo S,Itami N,et al.Maternal aging affects oocyte resilience to carbonyl cyanide-m-chlorophenylhydrazone-induced mitochondrial dysfunction in cows.PLoS One,2017,12:e0188099
[57]Jones KT,Lane SI.Molecular causes of aneuploidy in mammalian eggs.Development,2013,140:3719-30
[58]MacLennan M,Crichton JH,Playfoot CJ,et al.Oocyte development,meiosis and aneuploidy.Semin Cell Dev Biol,2015,45:68-76
[59]Yue MX,Fu XW,Zhou GB,et al.Abnormal DNAmethylation in oocytes could be associated with a decrease in reproductive potential in old mice.J Assist Reprod Genet,2012,29:643-50
[60]Suo L,Meng QG,Pei Y,et al.Changes in acetylation on lysine 12 of histone h4(acH4K12)of murine oocytes during maternal aging may affect fertilization and subsequent embryo development.Fertil Steril,2010,93:945-51
[61]Steuerwald NM,Bermudez MG,Wells D,et al.Maternal age-related differential global expression profiles observed in human oocytes.Reprod Biomed Online,2007,14:700-8
[62]Liu M,Yin Y,Ye X,et al.Resveratrol protects against ageassociated infertility in mice.Hum Reprod,2013,28:707-17