Abstract
Unlike the intermediate filament- and septin-based cytoskeletons which are apolar structures, the microtubule (MT) and actin cytoskeletons are polarized structures in mammalian cells and tissues including the testis, most notable in Sertoli cells. In the testis, these cytoskeletons that stretch across the epithelium of seminiferous tubules and lay perpendicular to the basement membrane of tunica propria serve as tracks for corresponding motor proteins to support cellular cargo transport. These cargoes include residual bodies, phagosomes, endocytic vesicles and most notably developing spermatocytes and haploid spermatids which lack the ultrastructures of motile cells (e.g., lamellipodia, filopodia). As such, these developing germ cells require the corresponding motor proteins to facilitate their transport across the seminiferous epithelium during the epithelial cycle of spermatogenesis. Due to the polarized natures of these cytoskeletons with distinctive plus (+) and minus (−) end, directional cargo transport can take place based on the use of corresponding actin- or MT-based motor proteins. These include the MT-based minus (−) end directed motor proteins: dyneins, and the plus (+) end directed motor proteins: kinesins, as well as the actin-based motor proteins: myosins, many of which are plus (+) end directed but a few are also minus (−) end directed motor proteins. Recent studies have shown that these motor proteins are essential to support spermatogenesis. In this review, we briefly summarize and evaluate these recent findings so that this information will serve as a helpful guide for future studies and for planning functional experiments to better understand their role mechanistically in supporting spermatogenesis.
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Introduction
The blood-testis barrier (BTB) in the adult mammalian testis is a unique blood-tissue barrier which restricts paracellular (between cells; i.e., gate-keeper function of the BTB) and transcellular (across cells; i.e., fence function of the BTB) transport (or diffusion) of water, electrolytes, nutrients, cytokines and biomolecules including paracrine and autocrine factors between adjacent Sertoli cells at the base of the seminiferous tubules, also known as the Sertoli cell barrier [1,2,3,4,5,6] (Fig. 1). Interestingly, microvessels found in the interstitial space between seminiferous tubules contribute relatively little barrier function to the BTB in the testis of rodents, primates and humans (Fig. 1) [5, 9]. The BTB also divides the seminiferous epithelium into the basal and the adluminal (apical) compartments as noted in Fig. 1. As such, meiosis I/II and all the cellular events pertinent to post-meiotic development take place behind the BTB in a specialized microenvironment (Fig. 1), whereas mitotic proliferation of spermatogonia and differentiation/transformation of type A and type B spermatogonia to earlier spermatocytes take place in the basal compartment [10,11,12]. The BTB is a highly dynamic blood-tissue barrier since preleptotene spermatocytes, once derived from type B spermatogonia in the basal compartment rodents, are to be transported across the BTB in late Stage VII through early Stage IX of the epithelial cycle while differentiating into leptotene spermatocytes, which can be transformed into zygotene and pachytene spermatocytes to prepare for meiosis. Studies have shown that the BTB in the rodent testis is constituted by the actin-based tight junction (TJ) between adjacent Sertoli cells, reinforced by a testis-specific actin-rich adherens junction (AJ) type called basal ectoplasmic specialization (ES), and supported by the actin-based gap junction, but also intermediate filament-based desmosome [13,14,15,16,17,18,19]. Once haploid spermatids are formed through meiosis, they are also being transported across the seminiferous epithelium in the adluminal compartment before fully developed step 19, 16, and 12 spermatids in the testis of rats, mice, and humans, respectively, are transformed to spermatozoa via spermiogenesis [12, 14, 20] as these cells are lacking the ultrastructures found in motile cells, namely the lamellipodia and filopodia [21]. Spermatozoa are then line-up at the edge of the seminiferous tubule lumen to undergo spermiation in Stage VIII of the epithelial cycle in rodents versus VI in humans, respectively, which is composed of a tightly regulated series of biochemical and cellular events involving multiple signal and regulatory proteins [13, 22,23,24]. The testicular sperm emptied into the epididymis are then undergo another series of maturation processes, rendering them capable of fertilizing the egg.
Studies have shown that BTB dynamics that support preleptotene spermatocyte transport across the immunological barrier, and the subsequent haploid spermatid transport across the seminiferous epithelium, are tightly regulated cellular events. These involve several biologically active peptides released at the basement membrane but also at the Sertoli-spermatid adhesion site known as the apical ES via proteolytic cleavage of the structural proteins at these two sites, namely the F5-, the NC1- and the LG3/4/5-peptide [9, 25,26,27]. These bioactive peptides, in turn, are working in concert with a number of signaling proteins such as mTORC1/rpS6/Akt1/2 and FAK-Y407, and cytoskeletal regulatory proteins such as Arp3, Eps8, +TIPs and −TIPs to modulate BTB and ES dynamics [9, 27, 28]. The ultrastructures and the biomolecules that support germ cell transport are the actin- and MT-based cytoskeletons, as well as the corresponding actin- and MT-based motor proteins. In brief, motor proteins are the “vehicles” that carry the “cargoes”, namely preleptotene spermatocytes and spermatids, utilizing the corresponding actin or microtubule (MT)-based cytoskeletons as tracks to transport developing germ cells and other organelles (e.g., residual bodies, phagosomes, cell vacuoles, endocytic vesicles) to their corresponding “destination” across the seminiferous epithelium (Fig. 1). Furthermore, this requires intricate involvement of both actin- and MT-based cytoskeletons to support cargo transport across the seminiferous epithelium. However, much of this information remains unknown. In this review, we provide a timely discussion on latest findings in this area of research regarding the role of motor proteins in supporting cargo transport across the seminiferous epithelium using the rat testis as a study model. We also highlight some of the specific research areas that deserve attentions in future studies, which should be helpful to understand the underlying mechanism(s) of idiopathic male infertility.
Sertoli Cell Cytoskeletons in the Testis
In the seminiferous epithelium of adult rodent testes, similar to other mammalian organs, the two prominent cytoskeletons are the intrinsically polarized actin- and microtubule (MT)-based cytoskeletons which are composed of globular subunits of actin and α-tubulin/β-tubulin oligomers, respectively (Fig. 1) [29,30,31,32,33]. These polarized structures also serve as tracks to support specific motor proteins for directional transport of cargoes across the seminiferous epithelium. On the other hand, the intermediate filament-based cytoskeleton constituted by vimentin [16, 34] and the septin-based cytoskeleton [35] are both apolar structures, thus, they do not support motor proteins for directional cargo transport along their filaments.
Actin-Based Cytoskeleton
A functional actin-based track is composed of linear actin filaments (i.e., filamentous actin, F-actin) derived from polymerized globulin (G)-actin subunits, with the fast-growing barbed (+) end near the base of the seminiferous epithelium, closest to the basement membrane, and the slow-growing pointed (−) end near the seminiferous tubule lumen (Fig. 1) [36, 37]. In brief, polymerization of a linear actin filament occurs by incoming ATP-bound G-actin subunits at the fast-growing barbed (+) end involving actin nucleation proteins (e.g., formin 1, spire 1). The ATP-bound G-actin subunits are rapidly dephosphorylated to ADP-bound G-actin and are all found at the slow-growing pointed (−) end near the tubule lumen (Fig. 1) [37, 38]. The actin-based tracks are most notable in late Stage VIII of the epithelial cycle that stretch across the seminiferous epithelium and align perpendicular to the basement membrane [38] (Fig. 1). However, F-actin are also prominently noted at the apical ES and basal ES/BTB wherein the actin filaments are aligned parallel to the Sertoli cell plasma membrane and appear as bundled structures in cross-sections of the tubules. As such, these actin filaments appear as “rod-like” structures in cross-sections of the tubules at the apical ES and basal ES/BTB sites, thereby reinforcing cell adhesion (Fig. 1). ES in the testis also plays a crucial role to support germ cell transport as preleptotene spermatocytes (at the basal ES) and developing spermatids (at the apical ES) tightly anchored onto the actin filament bundles at the ES, and with the MTs located nearby [18, 33], which are located in close proximity to the plasma membrane of the Sertoli cell. Thus, these cells are separated only by their apposing Sertoli cell-cell or Sertoli-germ cell plasma membranes [3, 39]. Thus, even though these germ cells, namely preleptotene spermatocytes or haploid elongate spermatids, are located “outside” the Sertoli actin filament and MT networks, they are anchor onto these cytoskeletons through the unusual adhesion of ES between these adjacent cells, which are considered as cargoes to the Sertoli cell at the site. Due to this intrinsic polarized nature of the actin filaments, the actin-based plus (+) end-directed motor protein myosin VIIa, and the actin-based minus (−) end-directed myosin VI are capable of moving cargoes either to the base or to the tubule lumen across the epithelium, respectively (Fig. 1).
MT-Based Cytoskeleton
Microtubules (MTs) are also polarized ultrastructures in which a microtubule is composed of 13 laterally associated protofilaments of α- and β-tubulin heterodimers, with a hollow lumen wherein the plus (+) fast growing end is near the basement membrane and the minus (−) slow growing end near the tubule lumen (Fig. 1) [40,41,42,43]. Due to the intrinsic polarized nature of MTs, the MT-based minus (−) end-directed motor protein dynein 1 and the plus (+) end-directed motor protein kinesins (e.g., kinesin 15) can move cargoes to the corresponding minus or plus end of MTs, respectively [44,45,46,47].
Motor Proteins
Motor proteins are a class of molecular motors that bind to either microtubule (MT)- or actin-based tracks. They are capable of converting chemical energy through the hydrolysis of ATP to generate the mechanical force necessary to transport cargoes along the track across cell cytoplasm. Herein, we discuss several motor proteins that have been studied in the testis pertinent to support spermatogenesis. Besides serving as an update, this summary also provides the basis for future studies regarding the role of motor proteins in supporting germ cell and cargo transport across the seminiferous epithelium.
MT-Based Motor Proteins: Dynein and Kinesin
Dynein
Dynein is a family of motor proteins that use MT-based track in retrograde sliding movement towards the minus (−) ends of microtubules [47, 48]. In brief, a dynein motor protein transports cargoes towards the center of the cell or seminiferous tubule lumen in the testis. There are two major classes of dyneins, cytoplasmic and axonemal dyneins, which are classified according to their function and structure differences. Dynein 1 is a cytoplasmic dynein of about 1.5 megadaltons (MDa) (Fig. 2; Fig. 3A), involved in intracellular transport, mitosis, cell polarization and directional cargo transport. For instance, dynein 1 carries the cargo (e.g., spermatid) by “walking” along the MT-track in the Sertoli cell. Even though spermatids locate outside the Sertoli cell, but they are tightly anchored onto the MT-track in the Sertoli cell at the apical ES (or preleptotene spermatocyte anchored onto the MT-track in the Sertoli cell at the basal ES), which is a known adhesion ultrastructure that supports spermatid or preleptotene spermatocyte transport [3, 17]. There are 15 types of axonemal dyneins to support ciliary (e.g., dynein 2) and flagellar movement [48,49,50,51] such as sperm flagella that confers sperm progressive motility. Axonemal dyneins support the beating of flagella and cilia through rapid and efficient sliding movements of MTs [52]. In this context, it is of interest to note that mechanical movement of hair cells in cochlea is supported by the motor protein prestin [53, 54] which is different from the dynein family motor proteins. A functional dynein motor protein is considerably larger and more complex than kinesin or myosin motors, and it is composed of two heavy chains and a variable number of associated intermediate chains, light intermediate chains and light chains (Fig. 3A). For instance, dynein 1 is a dimeric protein composed of two identical heavy chains with a large molecular mass (Mr) of 500 kDa each. Each HC, in turn, binds to a light intermediate chain (LIC), an intermediate chain (IC), and three light chains (LCs) of LC7, LC8, and Tctex 1 (Fig. 3A). Thus, dynein 1 is a dimer of dimers. Each heavy chain is composed of three functional domains: a coiled-coil stalk with MT binding domain (MTBD) containing a globular motor head at the C-terminus, an AAA+ ring containing six AAA+ modules that organized into a doughnut-like structure, and a cargo-binding tail at by N-terminus (Figure 3A). The AAA+ ring can hydrolyze ATP hence converting chemical energy into mechanical force to support cargo transport [59]. In the testis, dynein 1 interacts with a protein complex called dynactin and cargo adaptor to form a functional motor protein called the dynein-dynactin-adaptor complex that supports spermatid transport on MT-based cytoskeleton. Dynein I also transports various cellular cargoes along MT towards the minus (−) end of MT tracks [60]. Cargoes transported by cytoplasmic dynein include endosomes [61], lysosomes [62], phagosomes [63], melanosomes [64], peroxisomes [65], lipid droplets [66], mitochondria [67] and vesicles from the endoplasmic reticulum (ER) destined for the Golgi [68]. These cargo transports hence regulate the intracellular function of cells and tissues through different cell signaling pathways. In the rat testis, dynein 1 is necessary to confer Sertoli cell TJ-permeability barrier function since its knockdown by RNAi perturbs the TJ-barrier function due to gross defects of F-actin and microtubules (MTs) across the Sertoli cell cytosol wherein both cytoskeletons become extensively truncated [69]. These defects, in turn, perturb the distribution of BTB-associated proteins at the site, including the cell adhesion complexes CAR/ZO-1 and N-cadherin/β-catenin [69]. Furthermore, dynein 1 knockdown also perturbs the polymerization activities of F-actin and MTs [69], possibly due to defects in transporting machineries (e.g., actin or MT polymerization proteins) necessary to support cytoskeletal nucleation. More important, the loss of dynein 1 function by RNAi also perturbs the BTB function in vivo since the barrier no longer restricts the diffusion of small molecular biotin across the immunological barrier [69]. Multiple defective sperms are also noted in the epididymis including extensive defects in spermatid heads, tail, and sperm morphology due to defects of intracellular trafficking to support the assembly of essential cellular components during spermiogenesis [69]. The importance of dynein-based motor proteins is also noted in Table 1 since its KO in mice led to embryonic lethality.
Kinesin
Kinesin is a group of related motor proteins that use MT track in anterograde movement, to transport cargoes towards the plus (+) ends of MTs [96,97,98] (Fig. 2). In brief, a kinesin motor protein transports cargoes away from the center of the cell, usually to cell peripheries to support cell homeostasis, or to the base of the seminiferous epithelium in the testis (Fig. 1). Kinesin superfamily members in humans and rodents are organized into 14 families [99, 100]. A functional kinesin motor protein is a tetrameric protein, comprised of two heavy chains and two light chains (Fig. 3A). Each heavy chain has a globular motor head where microtubule binding and ATP hydrolysis take place at its N-terminal region, which in turn generate the energy via ATPase that converts chemical energy into mechanical force to elicit cargo transport. The head region is connected by a short neck linker to a long intertwined coiled-coil stalk, to be followed by the tail at its C-terminal region (Fig. 3A). A light chain associates with a tail which serve as the adapter for binding to a cargo while moving along the MT track towards the MT plus (+) end to facilitate cargo (e.g., spermatid, residual body, phagosome) transport [49, 97, 101] (Table 1). Kinesins typically move cargoes in the direction of MT plus (+) end on MT tracks, such that cargo is transported from the center of the cell to its periphery (i.e., anterograde movement). However, some kinesins (members of the kinesin-5 family), such as kinesin-14, move cargoes to the MT minus (−) end along the MT tracks wherein the motor region is located at the C-terminal region of the heavy chain [102]. On the other hand, kinesin-5 Cin8 (members of the kinesin-5 family) is a bidirectional kinesin which can move a cargo towards the microtubule minus (−) end when works alone but to the plus (+) end in an ensemble with a team of motors [103]. Emerging evidence has shown that kinesins are crucial to support tumorigenesis. For instance, KIF18A promotes invasion and metastasis by activating Akt and MMP-7/MMP-9-related signaling pathways [104] whereas kinesins also support proliferation, cell differentiation, aggressiveness and epithelial-mesenchymal transition of tumor cells [105,106,107,108,109]. A recent report has demonstrated the importance of kinesin-9 in conferring progressive motility in mouse spermatozoa since a deletion of 16 bp nucleotides of the Kif9 gene in mice (Kif9−16/−16) using CRISPR/Cas9 led to defects in flagellar movement of sperm tails [110]. Studies have also shown that kinesin-7 CENP-E is crucial to support chromosome alignment and genome stability of spermatogenic cells (e.g., spermatogonia and spermatocytes) during mitosis and meiosis [111], whereas kinesin-5 Eg5 supports spindle assembly and chromosome alignment of mouse spermatocytes [112]. Nonetheless, much work is needed to better understand the role of kinesins in supporting spermatogenesis in the testis. However, as noted in Table 1, deletion of one of the several kinesins in mice led to embryonic lethality, illustrating the physiological significance of kinesin-based motor proteins in supporting cellular function.
F-actin-Based Motor Proteins: Myosins
Myosins
Myosins are the only known actin-based motor proteins in mammalian cells and tissues including the testis [47, 113]. There are 18 classes of myosin superfamily members known to date based on phylogenetic analysis of their motor domain, and at least 40 myosin genes have been identified [57, 114]. By converting chemical energy via hydrolysis of ATP at the myosin motor head to mechanical energy, which in turn is used to propel cargo to be transported along the actin-based tracks, which are most notable in late Stage VIII tubules across the seminiferous epithelium in the testis [38]. Besides the regular myosins noted in mammalian cells, there is an emerging long-tailed unconventional class of myosins, namely myosin 1E and myosin 1F [115]. In general, each myosin has a Mr of 520 kDa, consisting of six subunits: two 220 kDa heavy chains, and two pairs of light chains (20 kDa for each light chain) (Fig. 3) [116]. Thus, there are two monomers in a functional myosin motor protein, with each monomer consists of a heavy chain and a pair of light chains to a total of three subunits. Each heavy chain, in turn, can be divided into distinctive head, neck and tail domains (Fig. 3B). The globular head domain interacts with actin filaments (i.e., actin-based track) though its actin binding site at the N-terminal region which also contains the ATPase site, capable of hydrolyzing ATP to convert the chemical energy to mechanical energy to propel cargo transport. The neck region of each heavy chain serves as a linker, which also transduces force generated by the catalytic motor domain at the head region. The neck region also provides the binding site for a pair of light chains, which are distinct protein subunits that interact with the neck region (Fig. 3B). The C-terminal tail contains a relatively long α-helical coiled-coil domain and at its C-terminal region, it contains the sequential SH3 (SRC homology 3), MyTH4 (myosin tail homology 4), FERM (F, 4.1 protein; E, ezrin; R, radixin; M, moesin) domains and the globular tail domain (GTD) at its C-terminus. GTD domain is supported by the FERM, MyTH4 and SH3 domains, and GTD also recognizes different cargoes through direct interactions or mediated through adaptor proteins, such as vezatin in the testis [117] (Fig. 3B). Most myosins (e.g., myosin VIIa) walk along actin filaments to the actin plus (+) end, but Myosin VI moves cargoes to the minus (−) end of actin tracks [113]. Myosin VIIa is a member of the myosin superfamily found in testis and other tissues [118] In testes, actin filament bundles constitute the ectoplasmic specialization, which also serve as the attachment site for cell adhesion protein complexes (e.g., N-cadherin-β-catenin, occludin-ZO-1, nectin-afadin). It also supports the transport of spermatids or organelles (i.e., cargoes) by serving as the track [12, 18]. Studies of myosin VIIa in the testis have shown that the knockdown of myosin VIIa in the testis in vivo by RNAi perturbs the organization of F-actin, but also MT tracks, across the seminiferous epithelium wherein these cytoskeletal tracks are extensively truncated [119]. These disruptive changes are likely the results of a considerably reduction in actin and MT polymerization activity in Sertoli cells [119] due to defects in intracellular protein trafficking. These defects also lead to formation of multiple defective sperms with gross changes in their morphology including round-shaped epididymal sperm heads, consistent presence of cytoplasmic droplets in the head region, and structural defects of sperm necks [119]. These findings are also consistent with earlier reports which have shown that KO of myosin motor proteins lead to embryonic fatality in mice (Table 1), and its mutation or genetic variations in humans also lead to defects in brain and heart development due to defects in intracellular protein trafficking.
Concluding Remarks and Future Perspectives
Herein, we summarize findings regarding the role of MT- and actin-based motor proteins in supporting mammalian spermatogenesis. As seen in studies using genetic models through gene deletion in mice (Table 1), and genetic mutations or gene variants in humans (Table 2), embryonic lethality (in mice) and serious pathological conditions (in humans) are noted in Tables 1 and 2, illustrating the significance of these motor proteins in cells and tissues, besides the testis. However, there are main questions remain. For instance, what are the biomolecules that trigger the use of specific plus (+) end or minus (−) directed motor proteins to initiate cargo transport of germ cells or other organelles to support spermatogenesis through different epithelial cycles? What is the mechanism(s) in place that selects the use of actin- or MT-based tracks or both? How does actin- and MT-based cytoskeletons coordinate with each other to streamline the transport of cargoes using their tracks to support spermatogenesis? It is now known that the several locally produced biomolecules, namely the F5-, NC1- and LG3/4/5-peptide, that regulate spermatogenesis exert their regulatory effects through their corresponding downstream signaling molecules on cytoskeletal organization. What is the mechanism(s) by which these biomolecules select the appropriate cytoskeleton, namely the F-actin or MT cytoskeleton, to execute their function? The answers to many of these questions will be helpful to understand and better manage unexplained male infertility. In brief, an intensive race is on to search for answers to some of these questions in the years to come, such as the role of many genes known to regulaste spermatogenesis to support motor protein function [191]. It is likely that the use of scRNA-seq and scATAC-seq coupled with transcriptome profiling and bioinformatics analyses will provide many of the missing information in this race to tackle male infertility (or fertility) in the years to come.
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Wu, S. et al. (2021). Motor Proteins and Spermatogenesis. In: Cheng, C., Sun, F. (eds) Molecular Mechanisms in Spermatogenesis. Advances in Experimental Medicine and Biology, vol 1381. Springer, Cham. https://doi.org/10.1007/978-3-030-77779-1_7
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