Electron microscopic observations on sperm entry into eggs of the rose bitterling, <i>Rhodeus ocellatus</i>

Ohta, Tatsuo; Isobe, Takashi

doi:10.1002/jez.1402270115

Cited by 45 publications

(29 citation statements)

References 16 publications

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“…2), which is consistent with the previous biochemical study in mice (5). 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).…”

Section: Resultssupporting

confidence: 88%

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: Resultssupporting

confidence: 88%

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 the carp and the rose bitterling, a fertilizing spermatozoonattaches first to the membraneof the microvilli at the SES just beneath a micropyle (9,15). Membrane fusion between sperm heads and egg microvilli has begun within 10 sec postinsemination (14).…”

Section: Discussionmentioning

confidence: 99%

“…After membrane fusion, the SES transforms into a SMwhich during early stages contains the naked sperm fated to move into the cortex. The SMenlarges increasingly until it plugs the micropyle, blocking possible penetration of excess spermatozoa following the fertilizing spermatozoon (15). With the lapse of time, the naked spermatozoon movesto the cortex and then the inner cytoplasm, and its nucleus soon transforms into a sperm pronucleus.…”

Section: Discussionmentioning

confidence: 99%

“…The morphology of the SES just beneath the micropyle varies among different species of teleosts (2,6,8,9,10,15). In cyprinid fishes, the SES has many microvilli in a circle coinciding with the inside diameter of the micropylar aperture (6,10,15).…”

Section: Discussionmentioning

confidence: 99%

“…The SMthereafter remains, plugging the micropyle, and serves to block the penetration of spermatozoa after the first (14,15). Cytochalasin B (CB) acts on micro filament function by inhibiting actin polymerization.…”

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Electron Microscopic Observations on Sperm Penetration in Cytochalasin-treated Eggs of the Rose Bitterling.

Ohta

Yoshida

Kato

1998

Cell Struct. Funct.

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Key words: fish egg/cytochalasin B/spermentry site/fertilization/sperm penetration ABSTRACT. The effects of cytochalasin B (CB), which acts on micro filaments, on sperm penetration into eggs of a teleost fish were investigated ultrastructurally.Eggs from the rose bitterling, Rhodeus ocellatus ocellatus, were pre-treated in physiological saline containing CB and inseminated in water also containing CB. Microvilli at the sperm entry site (SES) under the micropyle disappeared or shortened in length following CB treatment. However, a spermatozoon attached to and fused with the SES of CB-treated eggs. The spermatozoon present in a swollen mass (SM) remained at the egg surface even after membranefusion and did not enter the cortex. It was unclear whether or not sperm movement from the cortex to the inner cytoplasm is CB-sensitive. The SMformed and plugged the micropyle. CB did not inhibit cortical alveolus breakdown. Based on the present experiments with fish eggs, it is concluded that CBinhibits sperm movementfrom the egg surface to the cortex, but not sperm attachment (binding), membrane fusion and SMformation during the process of sperm penetration.The spermatozoon of a teleost fish is devoid of acrosomal structures. On the other hand, the egg is enveloped by an egg membrane (chorion) which has a micropyle at the animal pole. The egg plasma membrane just beneath the micropyle, through which a spermatozoon penetrates, is exposed directly to the exterior. A fertilizing spermatozoon is therefore able to attach to the egg plasma membranewithout making a hole in the chorion. In eggs of the rose bitterling, attachment and subsequent fusion of a fertilizing spermatozoon with the egg plasma membraneresults in formation of a swollen mass (SM) containing the naked spermatozoon. The SMthereafter remains, plugging the micropyle, and serves to block the penetration of spermatozoa after the first (14, 15). Cytochalasin B (CB) acts on micro filament function by inhibiting actin polymerization. We previously investigated the effects of CB on SM formation (16) and found that SMformation was not inhibited by CBtreatment. These preliminary observations of CBtreated eggs showed that sperm penetration seemed to occur, but that penetration of the sperm flagellum was slow in contrast to that seen in non-treated eggs. However, superficial observations by scanning electron microscopy (SEM) cannot clarify the details of penetration. In manyanimals, sperm penetration into CBtreated eggs has been inhibited (3, 5, ll, 12, 17, 21).However, it is unclear which steps in the process of sperm penetration are CB-sensitive. The present report was conducted to investigate the CB-sensitive steps in the process of the sperm penetration of fish eggs, using scanning and transmission (TEM) electron microscopy, as well as fluorescence microscopy. MATERIALS AND METHODSAdult rose bitterlings (Rhodeus ocellatus ocellatus) were kept in aerated aquaria together with freshwater bivalves, Anodonta woodiana at 18-23°C (water temperature). During breeding seasons sp...

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Sperm penetration and transformation of sperm entry site in eggs of the freshwater teleostRhodeus ocellatus ocellatus

Ohta

Nashirozawa

1996

J. Morphol.

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Electron microscopic observations on sperm entry into eggs of the rose bitterling, Rhodeus ocellatus

Cited by 45 publications

References 16 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

Electron Microscopic Observations on Sperm Penetration in Cytochalasin-treated Eggs of the Rose Bitterling.

Sperm penetration and transformation of sperm entry site in eggs of the freshwater teleostRhodeus ocellatus ocellatus

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