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The removal of the sperm perinuclear theca and its association with the bovine oocyte surface during fertilization.: Dev Biol, Vol. 188, No. 1. (1 August 1997), pp. 75-84.The perinuclear theca (PT) is a unique cytoskeletal structure whose anterior part is intercalated between the inner acrosomal membrane and the nuclear envelope of the mammalian sperm head and is important for spermiogenesis and stabilization of sperm structures (Oko and Maravei, Biol. Reprod. 50, 1000-1014, 1994; Oko and Maravei, Microsc. Res. Tech. 32, 520-532, 1995). Using immunofluoresc ence labeling of inseminated bovine oocytes and serial sectioning-ult rastructural analysis, we demonstrate that the PT is removed from the sperm nucleus following the loss of the sperm plasma membrane and the interaction of oocyte cortex with the PT. These events precede the development of the male pronucleus. The removal of the PT involves the elongated oocyte microvilli, rich in actin microfilaments , since it can be blocked by the microfilament- disrupting drug cytochalasin B. Reduction of disulfide bonds, which is a major factor supporting the disassembly of the sperm nucleus and accessory structures during mammalian fertilization, seems to exert little effect on the PT in vitro, as evidenced by the treatment of isolated bull sperm with the disulfide bond-reducing agent dithiothreitol . In vivo, intact bull sperm microinjected into mature oocytes do not undergo disassembly of the PT. Consequently, the decondensation of the sperm nucleus does not occur. These data suggest that the binding of the PT to the oocyte microvillar region and its removal from the sperm nucleus constitute an early step in mammalian fertilization, which is required for the conversion of the sperm nucleus into a male pronucleus.P Sutovsky, R Oko, L Hewitson, G Schatten

Source: Dev Biol, Vol. 188, No. 1. (1 August 1997), pp. 75-84.
Assembly of nuclear pore complexes and annulate lamellae promotes normal pronuclear development in fertilized mammalian oocytes.: J Cell Sci, Vol. 111 ( Pt 19) (October 1998), pp. 2841-2854.In addition to functional nuclear pore complexes engaged in nucleo-cytopla smic transport, the cytoplasmic stacks of pore complexes, called annulate lamellae, exist in numerous cell types. Although both annulate lamellae and nuclear pore complexes are present in fertilized mammalian oocytes, their relative roles in the process of fertilization and preimplantatio n development are not known. Using epifluorescenc e and electron microscopy, we explored their fate during bovine fertilization. The assembly of annulate lamellae in bovine oocytes was triggered by sperm-oocyte binding and continued concomitantly with the incorporation of the nuclear pores in the nuclear envelopes of the developing male and female pronuclei. This process was also induced by the parthenogeneti c activation of metaphase-II-a rrested oocytes. Depletion of Ca2+, previously implicated in oocyte activation and in the insertion of pore complexes into the nuclear envelope, prevented the formation of nuclear pore complexes, but not the assembly of annulate lamellae in oocyte cytoplasm. Injection of the nuclear pore antagonist, wheat germ agglutinin, into the cytoplasm of mature oocytes that were subsequently fertilized caused the arrest of pronuclear development, indicating the requirement of nuclear pore complexes for normal pronuclear development. Treatment of the fertilized oocytes with the microtubule inhibitor, nocodazole, prevented gathering of annulate lamellae around the developing pronuclei, insertion of nuclear pores into their nuclear envelopes, and further pronuclear development. The formation of the male pronuclei was reconstituted in Xenopus egg extracts and reflected the behavior of nuclear pores during natural fertilization. These data suggest that nuclear pore complexes are required for normal pronuclear development from its beginning up until pronuclear apposition. Annulate lamellae may be involved in the turnover of nuclear pore complexes during fertilization, which is in turn facilitated by the reorganization of oocyte microtubules and influx of Ca2+ into oocyte cytoplasm.P Sutovsky, C Simerly, L Hewitson, G Schatten

Source: J Cell Sci, Vol. 111 ( Pt 19) (October 1998), pp. 2841-2854.
Expression of proto-oncogene s in mouse eggs and preimplantatio n embryos.: Mol Reprod Dev, Vol. 35, No. 1. (May 1993), pp. 8-15.The expression of several protooncogenes has been investigated in mouse eggs and preimplantatio n embryos using reverse transcription coupled to amplification of cDNAs by the polymerase chain reaction (RT-PCR). The genes chosen for analysis included both cytoplasmic (c-raf-1, rasH, rasK, and rasN) and nuclear (c-fos and c-myc) proto-oncogene s encoding proteins involved in the transduction of signals from protein-tyrosi ne kinase growth factor receptors. Transcripts of the cytoplasmic proto-oncogene s were detected both as maternal and embryonic mRNAs at levels (ca. 1,000 copies per egg or embryo) approximately comparable to their levels of transcription in somatic cells. Transcripts of c-fos and c-myc were also detected in both eggs and embryos, although at more variable levels: Maternal transcripts were present at very low levels (ca. 1-10 copies per egg) in growing oocytes and ovulated eggs; embryonic transcription of c-myc increased, reaching mRNA levels of approximately 100-1,000 copies per embryo in four-cell embryos, morula, and blastocysts; in contrast the transcription of c-fos remained at low, barely detectable levels throughout preimplantatio n development. Although the significance of the low levels of c-fos mRNA is unclear, these results indicate that preimplantatio n embryos possess the basic intracellular signaling apparatus required to respond to polypeptide growth factors.SK Pal, R Crowell, AA Kiessling, GM Cooper

Source: Mol Reprod Dev, Vol. 35, No. 1. (May 1993), pp. 8-15.
Chromatin remodelling and epigenetic features of germ cells: Nature, Vol. 434, No. 7033. (31 March 2005), pp. 583-589.Sarah Kimmins, Paolo Sassone-Corsi

Source: Nature, Vol. 434, No. 7033. (31 March 2005), pp. 583-589.
Topoisomerase II Mediated Breaks in Spermatozoa Cause the Specific Degradation of Paternal DNA in Fertilized Oocytes.: Biol Reprod (20 December 2006)We have demonstrated that mouse spermatozoa can cleave their DNA into 50 kb fragments when treated with TritonX-100, MnCl2, and CaCl2. This cleavage, termed "Sperm Chromatin Fragmentation" (SCF), is mediated by Topoisomerase IIB (TOP2B) when stimulated by a factor in the epididymal fluid, most likely a nuclease, and can be at least partially religated by EDTA. When the protamines are removed, this DNA breakage is followed by digestion of all the DNA by a nuclease(s). We tested whether the oocyte could repair TOP2B induced sperm DNA breaks, or whether partial religation by EDTA would allow spermatozoa to fertilize the oocytes normally. Oocytes injected with untreated spermatozoa developed normally. However, oocytes injected with spermatozoa treated with MnCl2 and CaCl2 to induce SCF, with or without subsequent EDTA treatment, failed to develop. In both of these treatment groups, the maternal pronuclei developed normally and replicated their DNA. However the paternal pronuclei did not replicate their DNA, and the DNA began to disappear at 6 hours after injection-- at about the same time that maternal DNA replication was initiated. These data suggest that when TOP2B is induced to cleave the sperm DNA before fertilization, the paternal DNA is subsequently degraded by a highly regulated mechanism that does not affect the maternal chromatin. Furthermore, partial religation of the TOP2B breaks by EDTA does not prevent either the inhibition of DNA synthesis or the DNA degradation.Ya suhiro Yamauchi, Jeffery A Shaman, W Steven Ward

Source: Biol Reprod (20 December 2006)
New insights into the molecular mechanisms of sperm-egg interaction.: Cell Mol Life Sci (20 April 2007)At the moment of insemination millions of mammalian sperm cells are released into the female reproductive tract in order to find a single cell - the oocyte. The spermatozoa subsequently ignore the thousands of cells they make contact with during their journey to the site of fertilisation, until they reach the surface of the oocyte. At this point, they bind tenaciously to the acellular coat, known as the zona pellucida, that surrounds the oocyte and initiate the chain of cellular interactions that will culminate in fertilization. These exquisitely cell- and species-specif ic recognition events are among the most strategically important cellular interactions in biology. Understanding the cellular and molecular mechanisms that underpin them has implications for diagnosis of the aetiology of human infertility and the development of novel targets for fertility regulation. Herein, we describe two models indicating the plethora of highly orchestrated molecular interactions underlying successful sperm zona binding and sperm oocyte fusion.B Nixon, R Aitken, E McLaughlin

Source: Cell Mol Life Sci (20 April 2007)
Paternal Pronuclear DNA Degradation Is Functionally Linked to DNA Replication in Mouse Oocytes.: Biol Reprod (9 May 2007)We recently demonstrated that mouse spermatozoa contain a mechanism to degrade their DNA into loop-sized fragments of about 50 kb, mediated by topoisomerase IIB, termed sperm chromatin fragmentation (SCF). SCF is often followed by a more complete digestion of the DNA with a sperm nuclease. When SCF-induced spermatozoa are injected into oocytes, the paternal pronuclei degrade their DNA after the initiation of DNA synthesis, but the maternal pronuclei are unaffected and replicate normally. Here, we tested whether the nuclease activity changes in spermatozoa of different maturation stages, and whether there is a functional relationship between the initiation of DNA synthesis and paternal DNA degradation induced by SCF in the zygote. We found that spermatozoa from the vas deferens have a much higher level of SCF activity than those from the cauda epididymis, suggesting that spermatozoa may acquire this activity in the vas deferens. Furthermore, paternal pronuclei formed in zygotes from injecting oocytes with SCF-induced vas deferens spermatozoa degraded their DNA, but this degradation could be inhibited by the DNA synthesis inhibitor, aphidicolin. Upon release from a 4 hour aphidicolin-in duced arrest, DNA synthesis was initiated in maternal pronuclei while the paternal pronuclei degraded their DNA. Longer aphidicolin arrest resulted in the paternal pronuclei replicating their DNA, suggesting that delaying the initiation of DNA synthesis allowed the paternal pronuclei to overcome the SCF-induced DNA degradation pathway. These results suggest that the paternal DNA degradation, in oocytes fertilized with SCF-induced spermatozoa, is coupled to the initiation of DNA synthesis in newly fertilized zygotes.Yasuhi ro Yamauchi, Jeffrey A Shaman, Segal M Boaz, W Steven Ward

Source: Biol Reprod (9 May 2007)
Interactions of sperm perinuclear theca with the oocyte: implications for oocyte activation, anti-polysperm y defense, and assisted reproduction.: Microsc Res Tech, Vol. 61, No. 4. (1 July 2003), pp. 362-378.Perinu clear theca (PT) is the cytoskeletal coat of mammalian sperm nucleus that is removed from the sperm head at fertilization. PT harbors the sperm borne, oocyte-activat ing factor (SOAF), a yet-to-be-char acterized substance responsible for triggering the signaling cascade of oocyte activation, thought to be dependent on intra-oocyte calcium release. The present article reviews the current knowledge on the biogenesis and molecular composition of sperm PT. Possible functions of sperm PT during natural and assisted fertilization, and in the initiation of embryonic development are discussed. Furthermore, evidence is provided that SOAF is transferred from the sperm PT to oocyte cytoplasm through the internalizatio n and rapid solubilization of the post-acrosomal PT. It is shown that during natural fertilization the sperm PT dissolves in the oocyte cytoplasm concomitantly with sperm nuclear decondensation and the initiation of pronuclear development. SOAF activity is preserved in the differentially extracted sperm heads only if the integrity of PT is maintained. After intracytoplasm ic sperm injection (ICSI), activation occurs only in those oocytes in which the injected spermatozoon displays complete or partial dissolution of PT. In the latter case, the residual PT of the sub-acrosomal and/or post-acrosomal sperm region may persist on the apical surface of the sperm nucleus/male pronucleus and may cause a delay or arrest of zygotic development. We propose that the sperm PT harbors SOAF in the post-acrosomal sheath, as this is the first part of the sperm cytosol to enter the oocyte cytoplasm and its disassembly appears sufficient to initiate the early events of oocyte activation. Dissolution of the sub-acrosomal part of the PT, on the other hand, appears necessary to insure complete DNA decondensation in the internalized sperm nucleus and initiate DNA synthesis of both pronuclei. The release of the SOAF from the sperm head into oocyte cytoplasm at fertilization ultimately leads to the activation of oocyte mechanism including the completion of the meiotic cell cycle, pronuclear development and anti-polysperm y defense.P Sutovsky, G Manandhar, A Wu, R Oko

Source: Microsc Res Tech, Vol. 61, No. 4. (1 July 2003), pp. 362-378.
Sperm nuclear halos can transform into normal chromosomes after injection into oocytes.: Mol Reprod Dev, Vol. 62, No. 3. (July 2002), pp. 416-420.Mouse sperm nuclei extracted with an ionic detergent and 2 M NaCl retain their overall morphology, but upon subsequent reduction of the protamine disulfides they lose all elements of chromatin structure except the organization of DNA into loop that are anchored to the nuclear matrix. These DNA loops appear as a halo surrounding the nuclear matrix, and nuclei extracted in this manner are, therefore, called nuclear halos. Here, we report that sperm nuclear halos injected into oocytes can form pronuclei, then transform into chromosomes with normal morphology. This suggests that sperm nuclear halos retain all the information necessary for normal chromosomal organization, and that micromanipulat ion of these extracted sperm nuclei can be accomplished without major DNA damage.I Mohar, MA Szczygiel, R Yanagimachi, WS Ward

Source: Mol Reprod Dev, Vol. 62, No. 3. (July 2002), pp. 416-420.
Potential role of protein tyrosine phosphatase nonreceptor type 13 in the control of oocyte meiotic maturation.: Development, Vol. 131, No. 20. (October 2004), pp. 4987-4998.Prot ein tyrosine phosphatase nonreceptor type 13 (PTPN13) is a tyrosine phosphatase with multiple interacting domains that has been implicated previously in the regulation of apoptosis. We provide evidence that PTPN13 plays an important role in the control of the meiotic cell cycle. A cDNA coding for PTPN13 was isolated during the screening for the substrate of protein kinase A expressed in mammalian oocytes. PTPN13 is expressed in both mouse and Xenopus oocytes and is a substrate for protein kinase A in vitro and in vivo. Expression of a truncated constitutively -active PTPN13 in Xenopus oocytes synergizes with progesterone in the induction of germinal vesicle breakdown, the translation of Mos, the phosphorylatio n of Erk and the dephosphorylat ion of Cdc2. The phosphatase activity of PTPN13 is required for this synergism. Oocyte injection with specific small interference RNA downregulates the expression of mRNA for PTPN13 and blocks oocyte maturation induced by progesterone, a blockade that can be overcome by Cdc25 overexpression . These findings indicate that PTPN13 is involved in the regulation of the meiotic cell cycle.T Nedachi, M Conti

Source: Development, Vol. 131, No. 20. (October 2004), pp. 4987-4998.

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