Testis Expressed Actin-Like 7b (Actl7b) Is Required for Mouse Spermatid Morphogenesis and Male Fertility.
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During spermiogenesis round spermatids differentiate into elongated and then condensed spermatids followed by spermiation. Although the structural components and morphological changes in this complex process have been described in detail, relatively little is known about the mechanisms that drive these structural changes. The involvement of filamentous actin (F-actin) has been suggested for several aspects of spermatid differentiation, including acrosome formation and attachment to the nucleus, formation of tubulobulbar complexes and cytoplasmic removal, and spermiation. In addition, human male infertility is often associated with a high incidence of abnormally shaped sperm heads, suggesting that cytoskeletal regulation is important for male fertility. Actin-like 7b (Actl7b) is an intronless gene expressed in spermatids and conserved in mammals. Immunohistochemistry and indirect immunofluorescence were utilized to investigate the expression of ACTL7B. It is localized in the cytoplasm of round and elongating spermatids and co-localizes with phalloidin labeled F-actin) in or around the forming acrosome, suggesting a role in this process. To determine the functional relevance of (Actl7b), knockout mice were generated from targeted ES cells in which the (Actl7b) coding region was replaced with a LacZ reporter sequence, obtained from the KnockOut Mouse Project (KOMP) Repository. X-gal staining of tissues from heterozygous animals revealed that (Actl7b) is expressed in the testis and, unexpectedly, the brain. While (Actl7b) knockout mice develop to adulthood and appear normal, breeding studies revealed that (Actl7b) knockout males mate and produce vaginal plugs, but are infertile. Testis and epididymal weights and sperm counts are lower in knockout males than in wild type males. In addition, sperm heads are misshapen with a rounded appearance. Most of these sperm are immotile, with less than three percent showing minimal flagellar movement. These results indicate that ACTL7B is required for spermatid morphogenesis, sperm motility, and male fertility. They also suggest that ACTL7B is either the F-actin recognized by phalloidin or is required for F-actin assembly in spermatids. This research was supported by the Intramural Research Program of the NIH, National Institute of Environmental Health Sciences (EME).Keywords:
Spermatid
Spermiogenesis
Knockout mouse
Phalloidin
Abstract The elimination of the spermatid cytoplasm during spermiogenesis enables the sperm to acquire a streamlined architecture, which allows for unhindered swimming. While this process has been well described in vertebrates, it has rarely been reported in invertebrates. In this study, we observed the process of cytoplasm elimination during spermiogenesis in Octopus tankahkeei (Mollusca, Cephalopoda) using light microscopy, transmission electron microscopy, and immunofluorescence. In the early spermatid, the cell is circular, and the nucleus is centrally located. With spermatid development, the cell becomes polarized. The nucleus gradually elongates and moves toward the end of the cell where the tail is forming. As a result, the cytoplasm moves past the nucleus at the anterior region of the future sperm head (the foreside of the acrosome). Following this, during the late stage of spermiogenesis, the cytoplasm condenses and collects on the foreside of the acrosome until finally the residual body is discarded from the top of the sperm head. This represents a distinct directionality for the development of cytoplasmic polarity and discarding of residual body compared with that reported for vertebrates (in which the cytoplasm of the elongating spermatids is polarized toward the caudal region). The fact that the cytoplasm also becomes concentrated suggests that water pumps may be involved in the elimination of water from the cytoplasm before the residual body is discarded. Furthermore, we found that microtubules, forming a manchette‐like structure, are involved not only in reshaping of the nucleus but also in the transport of mitochondria and vesicles to the foreside of the acrosome, subsequently allowing them to be discarded with the residual body. This study broadens our understanding of the development of polarization and elimination of cytoplasm from spermatids in animals.
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Peroxiredoxins (Prx) are a recently identified family of proteins that have been shown to exhibit peroxidase activity, as well as other divergent functions. Of the six known members of the family, Prx4 is present as a secretable form in most tissues and as a membrane-bound form only in testes. We recently proposed that the unprocessed form may be involved in acrosome formation during spermiogenesis. In the present study, it was found that levels of the unprocessed Prx4 decreased during cryptorchidism and this decrease corresponded to the degree of the defect in spermiogenesis. In contrast, the levels of the secretable Prx4 remained virtually the same during cryptorchidism. These results were consistent with selective expression of the unprocessed form after the spermatid stage, suggesting the existence of a relationship with acrosome formation.
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The structure of early, intermediate and late spermatids as well as of the spermatozoon of the mite Erythraeus phaiangoides is described. The acrosome and the attached acrosomal filament are formed during early spermiogenesis. The nuclear material, undergoing gradual condensation, also adheres to the acrosome. At the same time, the nucleus strongly elongates and the nuclear envelope almost completely disappears. Peripherally distributed, flattened and tubular cisternae appear in the late spermatid. These cisternae develop as invaginations of the plasmalemma and their membranes communicate with the plasma membrane. Immediately before entering the lumen of the testis, the spermatozoa develop an additional outer membrane formed on the outside of the plasmalemma. During spermiogenesis mitochondria undergo a structural reorganization, with electron-dense granules appearing in their matrix
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The kinetic apparatus, the acrosome and associated structures, and the manchette of the spermatid of the domestic chicken have been studied with the electron microscope. The basic structural features of the two centrioles do not change during spermiogenesis, but there is a change in orientation and length. The proximal centriole is situated in a groove at the edge of the nucleus and oriented normal to the long axis of the nucleus and at right angles to the elongate distal centriole. The tail filaments appear to originate from the distal centriole. The plasma membrane is invaginated along the tail filaments. A dense structure which appears at the deep reflection of the plasma membrane is identified as the ring. The fine structure of the ring has no resemblance to that of a centriole and there is no evidence that it is derived from or related to the centrioles. The tail of the spermatid contains nine peripheral pairs and one central pair of tubular filaments. The two members of each pair of peripheral filaments differ in density and in shape: one is dense and circular, and the other is light and semilunar in cross-section. The dense filaments have processes. A manchette consisting of fine tubules appears in the cytoplasm of the older spermatid along the nucleus, neck region, and proximal segment of the tail. The acrosome is spherical in young spermatids and becomes crescentic and, finally, U-shaped as spermiogenesis proceeds. A dense granule is observed in the cytoplasm between acrosome and nucleus. This granule later becomes a dense rod which is interpreted as the perforatorium.
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Abstract A family of transgenic mice (OVE 219) was generated by microinjection of a tyrosinase minigene (Ty811C). The transgenic mice demonstrate an atypical and variable coat color pattern and the homozygous males show abnormalities of spermatogenesis that are variably expressed from animal to animal. Heterozygous mice proved to have normal spermatogenesis and along with non‐transgenic mice were used as controls to study the abnormalities in spermatogenesis in OVE 219 homozygous males. These abnormalities shed light on the features controlling normal spermatogenesis. In some homozygous males early spermiogenesis was disrupted as the flagellar microtubules became disorganized within the flagellar process. What appeared to be crystalline tubulin was noted within some of the rounded flagellar processes. Sperm with this defect did not develop a flagellum. In other homozygous males defects were apparent by step 6 or 7 of spermiogenesis when the acrosome did not grow and spread over the nucleus as noted in control animals. The modified nuclear envelope underlying the acrosome continued to develop and spread well beyond one margin of the acrosome. Since the modified nuclear envelope grew independently of the acrosome, the acrosome was not the controlling factor in determining the spread of the modified nuclear envelope. Micrographs revealed that Sertoli ectoplasmic specialization failed to form over most regions of the spermatid head lacking a normal acrosome. In homozygous males, the manchette took origin (proximally) in close relation to the modified nuclear envelope and never in relation to the edge of the spreading acrosome, a feature indicating that manchette placement was influenced by the position of the modified nuclear envelope and not the edge of the acrosome. Thus the modification in the nuclear envelope may be the primary event to signal acrosomal spread and manchette development. In spermatids where the manchette developed from an ectopic site, the result was abnormal caudal head shaping. In some spermatids a portion of the manchette was lacking. When this occurred the caudal head was rounded in the region of the missing manchette. In a minority of spermatids there was no evidence for a manchette. The entire caudal head was gently rounded. These data support the growing body of evidence that the caudal sperm head is shaped, in part, by the manchette. The OVE 219 family of mice provides a useful model to understand the processes involved in periods of spermiogenesis that are critical to development of a normally shaped sperm head. © 1994 Wiley‐Liss, Inc.
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The spermiogenesis of Crocidura shantungensis were studied by electron microscope. All process of spermiogenesis was divided into 11 phases 15 steps, based on the morphological features of the nucleus and cell organelles in cytoplasm of spermatids. The spermatids in Golgi and cap phases were a spherical shape. On the other hand, at the early acrosomal phase they changed into an oval shape, and the tail was created in this phase. In maturation phase, the shapes of spermatid head were thin and longish. Until step 7 the direction of spermatids head turned toward the lumen of the seminiferous tubule. From step 8 to step 15 their heads turned toward the basal lamina. In step 12, the nucleus and acrosome shown maximal elongation. From Step 13 the nucleus of spermatids became flat, simultaneously with flat expansion of the acrosome expanded, and the visible whole lengths of spermatids were tend to be shorten. Spermatid heading which arrived to step 14 was taken the final shape. The nucleus was doing the wedge shape, and the nuclear chromatins condensed completely and homogenized. In the spermiation phase, the spermatids were gradually disconnected from the cytoplasm of the Sertoli cell. In this phase, the acrosome of the spermatids were fully shorten and flat, and the spermatozoa completed the process of heading and the tailing. Considering all the results, the spermiogenesis may be useful information to analyze the differentiation of spermatogenic cells.
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Stereocilia (inner ear)
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Ultrastructural characteristics of spermiogenesis in the peanut worm, Phascolosoma esculenta (Phascolosomatidea), were observed by transmission electron microscopy (TEM). The spermiogenesis principally occurs in the coelom and can be divided into three stages (the early, middle and late stages) based on the chromatin morphology, acrosome development, spermatozoon midpiece and flagellum formation. Spermatids within a given spermatid mass develop synchronously. With the spermiogenesis proceeding, the spermatid masses become loosely structured, and later, adjacent spermatids are interconnected at one extremity of the cells. Gradually, condensation of the chromatin accelerates and is almost completed in late spermiogenesis, leaving the late spermatids with highly condensed homogeneous chromatin. In the spermatid head, the conical acrosome is generally composed of an acrosomal vesicle which is formed by the coalescence of small proacrosomal vesicles within the cytoplasm, a subacrosomal space that situates between the acrosomal vesicle and nucleus, and an acrosomal rod which develops from a bunch of filamentous material within the subacrosomal space. Certain mitochondria move posteriorly towards the nucleus, thus constituting the spermatozoon midpiece. The flagellum, originated from the distal centriole, appears in the early spermiogenesis. Ultimately, mature spermatidium dissociates into numerous spermatozoa, which are subsequently released as a single cell from the coelom into the nephridia. The spermatozoon has a prominent head, containing an acrosome and nucleus, a short midpiece and a slender tail. When compared with other sipunculans or invertebrates with external fertilization, the spermiogenesis of P. esculenta, presumably, is closely associated with its biological adaptations for the reproductive strategy.
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Summary The spermiogenesis of the brachiopod Rhynchonella psittacea was studied. The acrosome develops from cup-shaped acrosomal vesicles near the Golgi complex in the basal part of the spermatid. The acrosome vesicle then migrates to the apical region of the cell. The periacrosomal substance appears between the acrosomal vesicle and the nucleus. A ring-shaped mitochondrion is localized around the basal part of the nucleus. During spermiogenesis the proximal centriole is in contact with the nucleus via a single pericentriolar element. A distal centriole of the late spermatid has nine elements in a pericentriolar complex. The tail flagellum has a normal axonemal complex (9 + 2).
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Basal body
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