Multifocal damage of the testis induced in rats by passive transfer of antibodies prepared against non-collagenous fraction of basement membrane

Denduchis, Berta; Satz, M. L.; Sztein, Marcelo B.; Puig, Raúl; Doncel, Gustavo F.; Lustig, Livia

doi:10.1016/0165-0378(85)90021-x

Cited by 23 publications

(11 citation statements)

References 15 publications

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“…Besides its presence at the apical ES, β1-integrin was also shown to be a component of the hemidesmosome, and we have recently co-localized β1-integrin with vimentin (an intermediate filament protein) and laminin α2 (a hemidesmosome protein) at the hemidesmosome in adult rat testes (Yan et al ., 2008d). However, the role of hemidesmosome and basement membrane in regulating spermatogenesis and BTB dynamics remains largely unknown, except that earlier studies have shown that antibodies against the basement membrane or its components (e.g., laminins) caused extensive damage to the seminiferous epithelium which mimicked orchitis (Denduchis et al ., 1985; Lustig et al ., 1978; Lustig et al ., 2000). …”

Section: The Apical Es–btb–basement Membrane Local Regulatory Axismentioning

confidence: 99%

An intracellular trafficking pathway in the seminiferous epithelium regulating spermatogenesis: a biochemical and molecular perspective

Cheng¹,

Mruk²

2009

Critical Reviews in Biochemistry and Molecular Biology

113

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During spermatogenesis, fully developed spermatids (i.e., spermatozoa) at the luminal edge of the seminiferous epithelium undergo 'spermiation' at stage VIII of the seminiferous epithelial cycle. This is manifested by the disruption of the apical ectoplasmic specialization (apical ES) so that spermatozoa can enter the tubule lumen and to complete their maturation in the epididymis. At the same time, the blood-testis barrier (BTB) located near the basement membrane undergoes extensive restructuring to allow transit of preleptotene spermatocytes so that post-meiotic germ cells complete their development behind the BTB. While spermiation and BTB restructuring take place concurrently at opposite ends of the Sertoli cell epithelium, the biochemical mechanism(s) by which they are coordinated were not known until recently. Studies have shown that fragments of laminin chains are generated from the laminin/integrin protein complex at the apical ES via the action of MMP-2 (matrix metalloprotease-2) at spermiation. These peptides serve as the local autocrine factors to 'destabilize' the BTB. These laminin peptides also exert their effects on hemidesmosome which, in turn, further potentiates BTB restructuring. Thus, a novel apical ES-BTB-hemidesmosome regulatory loop is operating in the seminiferous epithelium to coordinate these two crucial cellular events of spermatogenesis. This functional loop is further assisted by the Par3/Par6-based polarity protein complex in coordination with cytokines and testosterone at the BTB. Herein, we provide a critical review based on the latest findings in the field regarding the regulation of these cellular events. These recent findings also open up a new window for investigators studying blood-tissue barriers.

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Section: The Apical Es–btb–basement Membrane Local Regulatory Axismentioning

confidence: 99%

An intracellular trafficking pathway in the seminiferous epithelium regulating spermatogenesis: a biochemical and molecular perspective

Cheng¹,

Mruk²

2009

Critical Reviews in Biochemistry and Molecular Biology

113

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“…We have previously demonstrated that antibodies against a preparation enriched in basement membranes of seminiferous tubules (STBM) [18] or a noncollagenous fraction of STBM [19] passively transferred induced modifications to the basement membranes and focal sloughing of the seminiferous epithelium in the rat. In the present report, we tested the effect of passive immunization with anti-laminin IgG on the limiting membrane of the seminiferous tubules, on germ cell differentiation, and on the competence of the Sertoli cell junctions forming the blood-tissue barrier in the adult guinea pig.…”

Section: Introductionmentioning

confidence: 99%

Passive Immunization with Anti-Laminin Immunoglobulin G Modifies the Integrity of the Seminiferous Epithelium and Induces Arrest of Spermatogenesis in the Guinea Pig1

Lustig

Denduchis

Ponzio

et al. 2000

Biology of Reproduction

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In the testis, the base of the Sertoli cells is in contact with the basement membrane matrix, in which the laminins constitute the major noncollagenous components. We have previously demonstrated that antibodies against a preparation enriched in basement membranes of seminiferous tubules (STBM) or a noncollagenous fraction of STBM passively transferred induced modifications to the basement membranes and focal sloughing of the seminiferous epithelium in the rat. In the present report, we tested the effect of passive immunization with anti-laminin IgG on the limiting membrane of the seminiferous tubules, spermatogenesis, and maintenance of the blood-testis barrier in the adult guinea pig. Rabbit antibodies to laminin 1 (IgG fraction) were injected in adult male guinea pigs (GP). Nonimmunized GP and GP immunized with normal rabbit serum IgG were used as controls. Measurements of variations in the diameter and lumen of the tubules and in the size of individual components of the tubular limiting membrane showed that the highest percentage of tubules with reduced lumen occurred 30 days after passive immunization with anti-laminin, when the limiting membrane was thickest and lesions to the seminiferous epithelium were most severe. The lesions included thickening of the limiting membrane, infolding in the basal lamina, deposits of immune complexes coincident with sloughing of pachytene spermatocytes and spermatids, and vacuolization of the Sertoli cells. Mononuclear cell infiltration of the tubules was rare. Permeability tracer studies revealed that Sertoli cell tight junctions remained impermeable. Fifty and 80 days after treatment, the basement membrane of the tubules and the progression of the spermatogenesis were normal. Passive immunization with anti-laminin IgG provided a valuable experimental model for the in vivo study of the influence of the basement membrane on the issue of spermatogenesis and the integrity of the seminiferous epithelium.

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“…Indeed, studies in vitro have shown that BM modulates Sertoli cell differentiation, Sertoli cell barrier function, and germ cell development (6–8). Studies in rats have also shown that a disruption of the BM function—for instance, by passive transfer of Abs raised against seminiferous tubule BM—leads to focal sloughing of the seminiferous epithelium (9, 10), which illustrates that the BM is necessary to support spermatogenesis. Furthermore, exposure of Sertoli cells cultured in vitro with an established functional tight junction (TJ)‐permeability barrier to an Ab against type IV collagen (collagen IV) was found to perturb the TJ barrier function (11), which illustrates the role of collagen at the BM in Sertoli cell function.…”

mentioning

confidence: 99%

Regulation of spermatogenesis by a local functional axis in the testis: role of the basement membrane–derived noncollagenous 1 domain peptide

et al. 2017

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Spermatogenesis takes place in the epithelium of the seminiferous tubules of the testes, producing millions of spermatozoa per day in an adult male in rodents and humans. Thus, multiple cellular events that are regulated by an array of signaling molecules and pathways are tightly coordinated to support spermatogenesis. Here, we report findings of a local regulatory axis between the basement membrane (BM), the blood-testis barrier (BTB), and the apical ectoplasmic specialization (apical ES; a testis-specific, actin-rich adherens junction at the Sertoli cell-spermatid interface) to coordinate cellular events across the seminiferous epithelium during the epithelial cycle. In short, a biologically active fragment, noncollagenous 1 (NC1) domain that is derived from collagen chains in the BM, was found to modulate cell junction dynamics at the BTB and apical ES. NC1 domain from the collagen a3(IV) chain was cloned into a mammalian expression vector, pCI-neo, with and without a collagen signal peptide. We also prepared a specific Ab against the purified recombinant NC1 domain peptide. These reagents were used to examine whether overexpression of NC1 domain with high transfection efficacy would perturb spermatogenesis, in particular, spermatid adhesion (i.e., inducing apical ES degeneration) and BTB function (i.e., basal ES and tight junction disruption, making the barrier leaky), in the testis in vivo. We report our findings that NC1 domain derived from collagen a3(IV) chain-a major structural component of the BM-was capable of inducing BTB remodeling, making the BTB leaky in studies in vivo. Furthermore, NC1 domain peptide was transported across the epithelium via a microtubule-dependent mechanism and is capable of inducing apical ES degeneration, which leads to germ cell exfoliation from the seminiferous epithelium. Of more importance, we show that NC1 domain peptide exerted its regulatory effect by disorganizing actin microfilaments and microtubules in Sertoli cells so that they failed to support cell adhesion and transport of germ cells and organelles (e.g., residual bodies, phagosomes) across the seminiferous epithelium. This local regulatory axis between the BM, BTB, and the apical ES thus coordinates cellular events that take place across the seminiferous epithelium during the epithelial cycle of spermatogenesis.-Chen, H., Mruk, D. D., Lee, W. M., Cheng, C. Y. Regulation of spermatogenesis by a local functional axis in the testis: role of the basement membrane-derived noncollagenous 1 domain peptide. FASEB J. 31, 3587-3607 (2017). www.fasebj.orgIn the mammalian testis, basement membrane (BM), a modified form of the extracellular matrix and a product of Sertoli and peritubular myoid cells (1, 2), is mostly constituted by type IV collagen, laminins (e.g., laminin a1, a2, b1, b2, g1), heparin sulfate proteoglycan, and nidogen (formerly called entactin) (3-5). As BM is in direct contact with Sertoli cells in the seminiferous epithelium, it is likely that there are crosstalks between Sertoli cells and the B...

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Multifocal damage of the testis induced in rats by passive transfer of antibodies prepared against non-collagenous fraction of basement membrane

Cited by 23 publications

References 15 publications

An intracellular trafficking pathway in the seminiferous epithelium regulating spermatogenesis: a biochemical and molecular perspective

An intracellular trafficking pathway in the seminiferous epithelium regulating spermatogenesis: a biochemical and molecular perspective

Passive Immunization with Anti-Laminin Immunoglobulin G Modifies the Integrity of the Seminiferous Epithelium and Induces Arrest of Spermatogenesis in the Guinea Pig1

Regulation of spermatogenesis by a local functional axis in the testis: role of the basement membrane–derived noncollagenous 1 domain peptide

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