Fertilization and early development in the Chinese hamster, <i>Cricetulus griseus</i>

Pickworth, Stella; Yerganian, George; Chang, M. C.

doi:10.1002/ar.1091620207

Cited by 21 publications

(10 citation statements)

References 12 publications

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“…In most vertebrates, intact mitochondrial sheath and tail enter oocyte cytoplasm during fertilization; this is also the case in O. latipes (30). The only exception is Chinese hamster (Cricetulus griseus), in which the mitochondria remain outside of the egg (31). Therefore, we next turned our attention to the fate of mtDNA in matured sperm after fertilization.…”

Section: Resultsmentioning

confidence: 99%

Active digestion of sperm mitochondrial DNA in single living sperm revealed by optical tweezers

Nishimura

Yoshinari

Naruse

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

145

104

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In almost all eukaryotes, mitochondrial (mt) genes are transmitted to progeny mainly from the maternal parent. The most popular explanation for this phenomenon is simple dilution of paternal mtDNA, because the paternal gametes (sperm) are much smaller than maternal gametes (egg) and contribute a limited amount of mitochondria to the progeny. Recently, this simple explanation has been challenged in several reports that describe the active digestion of sperm mtDNA, down-regulation of mtDNA replication in sperm, and proteolysis of mitochondria triggered by ubiquitination. In this investigation, we visualized mt nucleoids in living sperm by using highly sensitive SYBR green I vital staining. The ability to visualize mt nucleoids allowed us to clarify that the elimination of sperm mtDNA upon fertilization is achieved through two steps: (i) gradual decrease of mt nucleoid numbers during spermatogenesis and (ii) rapid digestion of sperm mtDNA just after fertilization. One notable point is that the digestion of mtDNA is achieved before the complete destruction of mitochondrial structures, which may be necessary to avoid the diffusion and transmission of potentially deleterious sperm mtDNA to the progeny. maternal inheritance ͉ medaka ͉ mtDNA M itochondria and chloroplasts contain their own genomes, which are believed to be vestiges of their bacterial ancestors (1). Mitochondrial (mt) and chloroplast (cp) genes are inherited in non-Mendelian fashion. A variety of patterns and mechanisms have been observed for the transmission of these genes, but in almost all eukaryotes, they are inherited mainly from the maternal parent (2-4).Generally, the maternal inheritance of mt (cp) DNA is thought to be a result of the dilution of the paternal contribution, because the paternal gametes (sperm) are much smaller than maternal gametes (egg) and contribute only a limited amount of cytoplasm to the progeny. In animals, a mature sperm carries Ϸ100 copies of mtDNA, which might be necessary to maintain the integrity of mitochondrial activity (5). In contrast, the animal oocyte contains Ϸ10 5 to 10 8 copies of mtDNA, exceeding that of sperm by a factor of at least 10 3 (3, 6). Therefore, the paternal contribution of mtDNA or cpDNA would be diluted beyond the limits of detection by using conventional restriction enzyme analysis (7).This simple explanation, however, has been challenged by many findings (8). For example, there have been several fairly unsuccessful attempts to detect leaky transmission of paternal mtDNA by repetitive backcross experiments using lepidopteran insects (9). On the contrary, in mussels (Mtylus), paternal mtDNA can be transmitted to male progeny at a remarkably high frequency, even though paternal mtDNAs are transmitted by sperm (10-12). A more striking example was found in the unicellular alga Chlamydomonas reinhardtii. In C. reinhardtii, despite the fact that mtϩ (female) and mtϪ (male) gametes contribute equal amounts of cytoplasm to the progeny, cpDNA is transmitted only from the mtϩ parent. One biochemical stud...

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Section: Resultsmentioning

confidence: 99%

Active digestion of sperm mitochondrial DNA in single living sperm revealed by optical tweezers

Nishimura

Yoshinari

Naruse

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

145

104

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“…On the other hand, it seems that zygotic selection between the two species may vary on account of their different embryogenesis. Chi nese hamster embryos develop slower than mouse embryos during the early cleavage period (Pickworth et al, 1968;Rugh, 1968) and, therefore, may have a greater opportunity for gene expression in the early stages.…”

Section: Discussionmentioning

confidence: 99%

Selective elimination of chromosomally unbalanced zygotes at the two-cell stage in the Chinese hamster

Sonta

Fukui

Yamamura

1984

Cytogenet Genome Res

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The gametic and zygotic selection of genome imbalance was investigated in the Chinese hamster by direct chromosome analyses of spermatocytes and preimplantation embryos from crosses between chromosomally normal females and males heterozygous for a reciprocal translocation, T(2;10)3Idr, abbreviated here as T3. The karyotypes and the frequencies of embryos observed at the first cleavage in the cross + / + ♀ × T3/ + ♂ were consistent with those expected from Mil scoring in male T3 heterozygotes. Therefore, it was concluded that there was neither gametic selection against genome imbalance nor zygotic selection from fertilization until the first cleavage metaphase. However, 9.1–10.8% of embryos were arrested at the two-cell stage, and karyotypes of these embryos were confirmed as 22(2,10,10,10²), 21(2,10,10), and 21(2,10,10²). The common abnormality of these embryos was partial monosomy of chromosome 2. Among day 4 embryos, some chromosomally unbalanced embryos, mainly with a deficiency of other segments of chromosomes 2 and 10, had fewer blastomeres than chromosomally balanced embryos. This finding suggests that cleavage of these embryos had been retarded by day 4 of gestation.

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“…Austin and Walton (1960) concluded that it was analogous to the entrance cone (also termed fertilization, or incorporation, cone) of invertebrate eggs. A similar phenomenon was described in the Chinese hamster (Pickworth et al, 1968). Later electron microscopic studies of mouse eggs also revealed an "incorporation cone" over the sperm head (Stefanini et al, 1969a;Anderson et al, 1975).…”

Section: Sperm Fusion With Oocytementioning

confidence: 52%

“…(Some instances of incomplete incorporation have been noted during in vitro fertilization in the mouse and hamster [Gaddum-Rosse et al, 1982;Yang et al, 1972;Yanagimachi, 19811. ) Only two of the mammalian species studied so far are exceptions to this generalization: the Chinese hamster and the field vole (Austin and Walton, 1960;Pickworth et al, 1968;Yanagimachi et al, 1983). The Chinese hamster sperm tail may enter the perivitelline space or even become partially incorporated into the vitellus, but it is normally expelled sooner or later by the fertilized egg or embryo.…”

Section: Incorporation Of the Sperm Flagellummentioning

confidence: 99%

Mammalian gamete interactions: What can be gained from observations on living eggs?

Gaddum-Rosse

1985

Am. J. Anat.

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Studies on fertilization have involved a variety of investigational techniques from the simple to the very complex. Perhaps the most direct approach has been the observation and photographic recording of the interactions of living gametes in vitro. The purpose of this paper is to review the major contributions that have been made, by means of this technique, to our knowledge of mammalian fertilization, and to examine its advantages and limitations. Some of the events of mammalian fertilization that have been observed in living eggs and are reviewed herein include sperm penetration through the zona pellucida, contact of the fertilizing spermatozoon with the oocyte surface and the subsequent incorporation of the sperm head into the oocyte cytoplasm, the formation and disappearance of the incorporation cone, the gradual incorporation of the sperm flagellum, surface movements of the oocyte after activation, and the formation of the second polar body. One advantage of studying living eggs is the opportunity it affords to witness events as they actually occur and, under favorable circumstances, to observe the whole series of events in individual eggs. Only by this mechanism can certain features of the process be fully appreciated and accurate data obtained on the timing of events. With the addition of time-lapse photographic methods, some of the more subtle changes become more amenable to study. Among the limitations of the technique are its limited resolution and the necessity for examining the gametes outside their normal in vivo environment.

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Fertilization and early development in the Chinese hamster, Cricetulus griseus

Cited by 21 publications

References 12 publications

Active digestion of sperm mitochondrial DNA in single living sperm revealed by optical tweezers

Active digestion of sperm mitochondrial DNA in single living sperm revealed by optical tweezers

Selective elimination of chromosomally unbalanced zygotes at the two-cell stage in the Chinese hamster

Mammalian gamete interactions: What can be gained from observations on living eggs?

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