期刊论文详细信息
BMC Cell Biology
Unlaid Xenopus eggs degrade by apoptosis in the genital tract
Alexander A Tokmakov1  Yasuo Fukami2  Tetsushi Iwasaki1  Sho Iguchi2 
[1] Research Center for Environmental Genomics, Kobe University, Rokko dai 1-1, Nada, Kobe, 657-8501, Japan;Graduate School of Science, Rokko dai 1-1, Nada, Kobe, 657-8501, Japan
关键词: Genital tract;    Xenopus laevis;    Meiotic exit;    Ovulation;    Maturation;    Unlaid eggs;    Apoptosis;   
Others  :  855475
DOI  :  10.1186/1471-2121-14-11
 received in 2012-08-13, accepted in 2013-02-28,  发布年份 2013
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【 摘 要 】

Background

In several species with external fertilization, including frogs, laid unfertilized eggs were found to die by apoptosis outside of the animal body. However, there is no apparent reason for the externally laid eggs to degrade by this process, considering that apoptosis developed as a mechanism to reduce the damaging effect of individual cell death to the whole organism.

Results

Here, we demonstrate that a number of eggs are retained in the genital tract of the African clawed frog Xenopus laevis after gonadotropin-induced ovulation. The majority of these eggs exit meiotic arrest within 24 hours of hormone administration. Subsequently, post-meiotic eggs die in the frog genital tract by a well-defined apoptotic process. The hallmarks of egg degradation include prominent morphological changes, cytochrome c release, caspase activation, increase in ADP/ATP ratio, progressive intracellular acidification, egg swelling and all-out proteolysis of egg proteins. The sustained presence of post-apoptotic eggs in the genital tract of ageing frogs evidenced age-associated worsening of apoptotic clearance.

Conclusions

The direct observation of egg degradation in the Xenopus genital tract provides a clue to the physiological relevance of frog egg apoptosis. It works to eliminate the mature unlaid eggs retained in the animal body after ovulation. Our findings establish egg apoptosis as a major physiological process accompanying ovulation in frogs.

【 授权许可】

   
2013 Iguchi et al; licensee BioMed Central Ltd.

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【 参考文献 】
  • [1]Masui Y, Markert CL: Cytoplasmic control of nuclear behavior during meiotic maturation of frog oocytes. J Exp Zool 1971, 177:129-145.
  • [2]Masui Y: The elusive cytostatic factor in the animal egg. Nat Rev Mol Cell Biol 2000, 1:228-232.
  • [3]Tunquist BJ, Maller JL: Under arrest: cytostatic factor (CSF)-mediated metaphase arrest in vertebrate eggs. Gene Dev 2003, 17:683-710.
  • [4]Dupre A, Haccard O, Jesus C: Mos in the oocyte: how to use MAPK independently of growth factors and transcription to control meiotic divisions. J Signal Transduct 2011.
  • [5]Austin CR: Ageing and reproduction: Post-ovulatory deterioration of the egg. J Reprod Fertil 1970, 12(Suppl):39-53.
  • [6]Miao YL, Kikuchi K, Sun QY, Shatten H: Oocyte aging: cellular and molecular changes, developmental potential and reversal possibility. Hum Reprod Update 2009, 15:573-585.
  • [7]Witschi E: Overripeness of the egg as a cause of twinning and teratogenesis. Cancer Res 1952, 12:763-786.
  • [8]Kjorsvik E, Mangor-jensen A, Homefiord I: Egg quality in fishes. Adv Mar Biol 1990, 26:71-113.
  • [9]Wilcox AJ, Weinberg CR, Baird DD: Post-ovulatory ageing of the human oocyte and embryo failure. Hum Reprod Update 1998, 13:394-397.
  • [10]Lacham-Kaplan O, Trounson A: Reduced developmental competence of immature in-vitro matured and postovulatory aged mouse oocytes following IVF and ICSI. Reprod Biol Endocrinol 2008, 6:58. BioMed Central Full Text
  • [11]Xu Z, Abbott A, Kopf GS, Schultz RM, Ducibella T: Spontaneous activation of ovulated mouse eggs: time-dependent effects on M-phase exit, cortical granule exocytosis, maternal messenger ribonucleic acid recruitment, and inositol 1,4,5-trisphosphate sensitivity. Biol Reprod 1997, 57:743-750.
  • [12]Chebotareva T, Taylor J, Mullins JJ, Wilmut I: Rat eggs cannot wait: spontaneous exit from meiotic metaphase II arrest. Mol Reprod Dev 2011, 78:795-807.
  • [13]Fujino Y, Ozaki K, Yamamasu S, Ito F, Matsuoka I, Hayashi E, Nakamura H, Ogita S, Sato E, Inoue M: DNA fragmentation of oocytes in aged mice. Hum Reprod 1996, 11:1480-1483.
  • [14]Tilly JL, Kowalski KI, Johnson AL, Hsueh AJ: Involvement of apoptosis in ovarian follicular atresia and postovulatory regression. Endocrinology 1991, 129:2799-2810.
  • [15]Hsueh AJ, Billig H, Tsafriri A: Ovarian follicle atresia: a hormonally controlled apoptotic process. Endocr Rev 1994, 15:707-724.
  • [16]Sasaki K, Chiba K: Fertilization blocks apoptosis of starfish eggs by inactivation of the MAP kinase pathway. Dev Biol 2001, 237:18-28.
  • [17]Yuce O, Sadler KC: Postmeiotic unfertilized starfish eggs die by apoptosis. Dev Biol 2001, 237:29-44.
  • [18]Sasaki K, Chiba K: Induction of apoptosis in starfish eggs requires spontaneous inactivation of MAPK (extracellular signal-regulated kinase) followed by activation of p38MAPK. Mol Biol Cell 2004, 15:1387-1396.
  • [19]Sadler KC, Yuce O, Hamaratoglu F, Verge V, Peaucellier G, Picard A: MAP kinases regulate unfertilized egg apoptosis and fertilization suppress death via Ca+2 signaling. Mol Reprod Dev 2004, 67:366-383.
  • [20]Pasquier DD, Dupre A, Jessus C: Unfertilized Xenopus eggs die by Bad-dependent apoptosis under the control of Cdk1 and JNK. PLoS One 2011, 6(8):e23672.
  • [21]Tokmakov AA, Iguchi S, Iwasaki T, Fukami Y: Unfertilized frog eggs die by apoptosis following meiotic exit. BMC Cell Biol 2011, 12:56. BioMed Central Full Text
  • [22]Morgan TH: The development of the frog’s egg: an introduction to experimental embryology. : New York Macmillan; 1897.
  • [23]Smith LD, Ecker RE: Uterine suppression of biochemical and morphogenetic events in Rana pipiens. Dev Biol 1970, 22:622-637.
  • [24]Diakow C, Scharff C, Aronow L: Egg-oviduct interaction initiates reproductive behavior. Horm Behav 1988, 22:131-138.
  • [25]Bakos MA, Kurosky A, Hedrick JL: Physicochemical characterization of progressive changes in the Xenopus laevis egg envelope following oviducal transport and fertilization. Biochemistry 1990, 29:609-615.
  • [26]Hedrick JL: Anuran and pig egg zona pellucida glycoproteins in fertilization and early development. Int J Dev Biol 2008, 52:683-701.
  • [27]Green SL, Parker J, Davis C, Bouley DM: Ovarian hyperstimulation syndrome in gonadotropin-treated laboratory South African Clawed Frogs (Xenopus laevis). J Am Assoc Lab Anim Sci 2007, 46:64-67.
  • [28]Faure S, Vigneron S, Doree M, Morin N: A member of the Ste20/PAK family of protein kinases is involved in both arrest of Xenopus oocytes at G2/prophase of the first meiotic cell cycle and in prevention of apoptosis. EMBO J 1997, 16:589-597.
  • [29]Tashker JS, Olson M, Kornbluth S: Post-cytochrome c protection from apoptosis conferred by a MAPK pathway in Xenopus egg extracts. Mol Biol Cell 2002, 13:393-401.
  • [30]Allan LA, Clarke PR: Phosphorylation of caspase-9 by CDK1/cyclin B1 protects mitotic cells against apoptosis. Mol Cell 2007, 26:301-310.
  • [31]Andersen JL, Johnson CE, Freel CD, Parrish AB, Day JL, Buchakjian MR, Nutt LK, Thompson JW, Moseley MA, Kornbluth S: Restraint of apoptosis during mitosis through interdomain phopshorylation of caspase-2. EMBO J 2009, 28:3216-3227.
  • [32]Jorgensen CB: Growth and reproduction. In Environmental physiology of the amphibians. Edited by Feder ME, Burggren WW. Chicago: University of Chicago Press; 1992:439-466.
  • [33]Henson PM, Hume DA: Apoptotic cell removal in development and tissue homeostasis. Trends Immunol 2006, 27:244-250.
  • [34]Elliott MR, Ravichandran KS: Clearance of apoptotic cells: implications in health and disease. J Cell Biol 2010, 189:1059-1070.
  • [35]Tokmakov AA, Iwasaki T, Sato K-I, Fukami Y: Analysis of signal transduction in cell-free extracts and rafts of Xenopus eggs. Methods 2010, 51:177-182.
  • [36]Laemmli UK: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
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