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This review focuses on the striking differences in the patterns of transcription and translation in somatic and spermatogenic cells in mammals. In early haploid cells, mRNA translation evidently functions to restrict the synthesis of certain proteins, notably protamines, to transcriptionally inert late haploid cells. However, this does not explain why a substantial proportion of virtually all mRNA species are sequestered in translationally inactive free-messenger ribonucleoprotein particles (free-mRNPs) in meiotic cells, since most mRNAs undergo little or no increase in translational activity in transcriptionally active early haploid cells. In addition, most mRNAs in meiotic cells appear to be overexpressed because they are never fully loaded on polysomes and the levels of the corresponding protein are often much lower than the mRNA and are sometimes undetectable. A large number of genes are expressed at grossly higher levels in meiotic and/or early haploid spermatogenic cells than in somatic cells, yet they too are translated inefficiently. Many genes utilize alternative promoters in somatic and spermatogenic cells. Some of the resulting spermatogenic cell-altered transcripts (SCATs) encode proteins with novel functions, while others contain features in their 5'-UTRs, secondary structure or upstream reading frames, that are predicted to inhibit translation. This review proposes that the transcriptional machinery is modified to provide access to specific DNA sequences during meiosis, which leads to mRNA overexpression and creates a need for translational fine-tuning to prevent deleterious consequences of overproducing proteins.

The translational activity of more than 40 different mRNAs in rodent testes has been analyzed by determining the proportions of inactive free‐mRNPs and active polysomal mRNAs in sucrose gradients. These mRNAs can be sorted into several groups comprising mRNAs with similar patterns of translational activity in particular cell types. mRNAs in testicular somatic cells sediment primarily with polysomes, indicating that they are translated efficiently, whereas the vast majority of mRNAs in late meiotic and haploid spermatogenic cells display high levels of free‐mRNPs, indicative of a block to the initiation of translation. Protamine mRNAs exemplify a group of mRNAs that is transcribed in round spermatids, stored as free‐mRNPs for several days, and translated in elongated spermatids after the cessation of transcription. The extent to which the free‐mRNPs in primary spermatocytes and round spermatids are due to developmental changes in translational activity is unclear. mRNAs at these stages can often be detected earlier than the corresponding protein, implicating either a delay in translational activation or difficulties in detecting the protein. In contrast, sucrose gradients consistently indicate little difference in the proportions of various mRNAs in free‐mRNPs in primary spermatocytes and round spermatids, implying that the proportions of translationally active mRNAs remain essentially constant. Since the levels of some mRNAs appear to greatly exceed the amount that is translated, the biological significance of some free‐mRNPs in meiotic and early haploid cells in unclear. There are numerous examples of controls over the translation of individual mRNAs in meiotic and haploid cells; the proportions of various mRNAs in free‐mRNPs range from virtually none to virtually all, and individual mRNAs are activated at specific stages in elongated spermatids. Existing evidence is contradictory whether the mRNAs in the protamine/transition protein gene family are repressed by mRNP proteins of sequestration. © 1996 Wiley‐Liss, Inc.

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This review proposes that the peculiar patterns of gene expression in spermatogenic cells are the consequence of powerful evolutionary forces known as sexual selection. Sexual selection is generally characterized by intense competition of males for females, an enormous variety of the strategies to maximize male reproductive success, exaggerated male traits at all levels of biological organization, co-evolution of sexual traits in males and females, and conflict between the sexual advantage of the male trait and the reproductive fitness of females and the individual fitness of both sexes. In addition, spermatogenesis is afflicted by selfish genes that promote their transmission to progeny while causing deleterious effects. Sexual selection, selfish genes, and genetic conflict provide compelling explanations for many atypical features of gene expression in spermatogenic cells including the gross overexpression of certain mRNAs, transcripts encoding truncated proteins that cannot carry out basic functions of the proteins encoded by the same genes in somatic cells, the large number of gene families containing paralogous genes encoding spermatogenic cell-specific isoforms, the large number of testis-cancer-associated genes that are expressed only in spermatogenic cells and malignant cells, and the overbearing role of Sertoli cells in regulating the number and quality of spermatozoa.

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The sperm mitochondria-associated cysteine-rich protein (SMCP) is a cysteine-and proline-rich structural protein that is closely associated with the keratinous capsules of sperm mitochondria in the mitochondrial sheath surrounding the outer dense fibers and axoneme. To investigate the function of SMCP, we generated mice with a targeted disruption of the gene Smcp by homologous recombination. Homozygous mutant males on a mixed genetic background (C57BL/6J ؋ 129/Sv) are fully fertile, while they are infertile on the 129/Sv background, although spermatogenesis and mating are normal. Homozygous Smcp ؊/؊ female mice are fertile on both genetic backgrounds. Electron microscopical examination demonstrated normal structures of sperm head, mitochondria, and tail. In vivo experiments with sperm of Smcp ؊/؊ 129/Sv mice revealed that the migration of spermatozoa from the uterus into the oviduct is reduced. This result is supported by the observation that sperm motility as determined by the computer-assisted semen analysis system (CASA) is significantly affected as compared to wild-type spermatozoa. In vitro fertilization assays showed that Smcpdeficient spermatozoa are able to bind to the oocyte but that the number of fertilized eggs is reduced by more than threefold relative to the wild-type control. However, removal of the zona pellucida resulted in an unaffected sperm-egg fusion which was monitored by the presence of pronuclei and generation of blastocyts. These results indicate that the infertility of the male Smcp ؊/؊ mice on the 129/Sv background is due to reduced motility of the spermatozoa and decreased capability of the spermatozoa to penetrate oocytes.Mitochondria are confined to a structure known as the mitochondrial sheath in the midpiece of mammalian spermatozoa. The mitochondria in the sheath are elongated, crescent shaped, and aligned end-to-end in helices wrapped around the outer dense fibers which in turn surround the flagellar axoneme (21). Pallini et al. (22) purified sonication-and sodium dodecyl sulfate (SDS)-resistant structures from sperm mitochondria, known as capsules, that retain the size and shape of the outer membranes of sperm mitochondria. The integrity of capsules is maintained by disulfide bridges, and purified capsules from bull sperm contain three proteins, including a peculiar hydrophilic protein containing a large amount of proline (26%) and cysteine (18%), the sperm mitochondria-associated cysteine-rich protein (SMCP). For many years, SMCP was thought to be a 20-kDa selenoprotein and the predominant capsular protein (7), but recent work demonstrates that those attributes belong to phospholipid hydroxide glutathione peroxidase, which functions as a cytosolic enzyme in somatic cells and an enzymatically inactive structural protein in the mitochondrial capsule (33). Electron microscope immunocytochemistry localizes mouse SMCP to the outer mitochondrial membranes and intermitochondrial spaces of the mitochondrial sheath (8). Since SMCP is neither a selenoprotein nor the major capsule protein...