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      Development of heterotopic transplantation of the testis with the epididymis to evaluate an aspect of testicular immunology in rats

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          Abstract

          Transplantation of testicular cells and tissues has been studied for the investigation of immunology of the testis, which is an immunologically privileged organ. However, reports of transplant of the testis at organ level have been extremely limited because of technical difficulties of the orthotopic testis transplantation (OTT) in experimental animals. In the present study, we developed a new and simple model of the heterotopic testis transplantation (HTT), which is donor testis transplantation into the cervical region of recipients, in a syngeneic model in rats [donor Lewis (LEW) graft to LEW recipient]. The duration of HTT was significantly shorter and success rate higher than that of OTT. To histologically evaluate HTT, the local immune responses were compared among the syngeneic model, an acute rejection allogeneic model [donor Augustus Copenhagen Irish (ACI) graft to LEW recipient] and a chronic rejection allogeneic model (donor F344 graft to LEW recipient) at postoperative day 3. We found that allogeneic ACI grafts resulted in mild and not severe orchitic lesions, whereas immune responses of allogeneic F344 grafts seemed intact and were not significantly different from those of syngeneic LEW grafts. These results suggest that our new operative procedure will be useful in future for the investigation of the testicular immunology.

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          Most cited references 38

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          Sperm from neonatal mammalian testes grafted in mice.

          Spermatogenesis is a productive and highly organized process that generates virtually unlimited numbers of sperm during adulthood. Continuous proliferation and differentiation of germ cells occur in a delicate balance with other testicular compartments, especially the supporting Sertoli cells. Many complex aspects of testis function in humans and large animals have remained elusive because of a lack of suitable in vitro or in vivo models. Germ cell transplantation has produced complete donor-derived spermatogenesis in rodents but not in other mammalian species. Production of sperm in grafted tissue from immature mammalian testes and across species has not yet been accomplished. Here we report the establishment of complete spermatogenesis by grafting testis tissue from newborn mice, pigs or goats into mouse hosts. This approach maintains structural integrity and provides the accessibility that is essential for studying and manipulating the function of testes and for preserving the male germ line. Our results indicate that this approach is applicable to diverse mammalian species.
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            Spermatogenesis and steroidogenesis in mouse, hamster and monkey testicular tissue after cryopreservation and heterotopic grafting to castrated hosts.

            Retrieval, extracorporal storage and autotransplantation of testicular tissue could become an important strategy for preserving male gonadal function. The present study used syngeneic and immunodeficient nude mice as hosts, and immature and adult mice, neonatal and adult photoregressed Djungarian hamsters and neonatal marmosets to identify the potential of testicular tissue grafting to maintain the morphological and functional integrity of the testis. Testicular tissue was grafted s.c. either as fresh tissue or after cryopreservation into adult, orchidectomized hosts. The mice that received rodent testis tissue were autopsied 50 days later, and blood samples were collected. Sixty-five per cent of mouse isografts contained morphologically normal testicular tissue and seminiferous tubules with some degree of spermatogenic recovery. Mature spermatozoa were recovered after enzymatic disaggregation. Although the recovery of spermatogenesis was limited in adult mouse and hamster tissue, complete spermatogenesis was observed in grafts from immature rodents. Testicular tissue from neonatal marmosets developed up to the stage of spermatocytes at day 135 after xenografting. Androgen concentrations were comparable in intact control mice and in mice receiving fresh mouse and hamster grafts, slightly lower in mice receiving cryopreserved grafts and adult photoregressed hamster tissue, and low in castrated control mice and in mice receiving marmoset tissue. These results show that isografts and xenografts of immature and adult testicular tissue become functionally active as a s.c. graft in the mouse and that this approach might be useful in combination with cryopreservation as a tool for storage and activation of the male germ line and androgen replacement therapy in patients.
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              Rat resident testicular macrophages have an alternatively activated phenotype and constitutively produce interleukin-10 in vitro.

              The ability of the rodent testis to tolerate graft alloantigens and spermatogenic cell autoantigens is well known. The mechanisms underlying this "immune privilege" are poorly understood, but the numerous resident TMs have been implicated. Although it has been assumed that TMs display a phenotype consistent with immune privilege, this has not been formally established. Consequently, TMs were isolated from adult rats and cultured under basal conditions and following stimulation with LPS and IFN-γ (classical activation) or IL-4 (alternative activation). BMMs matured in vitro were used as control. Expression of the classical (proinflammatory) activation markers TNF-α, IL-1β, iNOS, IL-6, RANTES, IL-12p40, and SOCS3 and alternative (immunoregulatory) activation markers IL-10, TGF-β1, CXCL2, and SOCS1 was measured by QPCR or ELISA. In culture, TMs were characterized by poor expression of classical activation genes and TGF-β1 but constitutively high IL-10 production and reduced costimulatory activity in a polyclonal T cell activation assay. This pattern of gene expression was associated with TMs expressing the scavenger receptor CD163, which is characteristic of tissue resident macrophages and alternative activation. By contrast, CD163-negative TMs displayed reduced inflammatory gene expression but did not constitutively produce IL-10. These data indicate that under the influence of the testicular environment, macrophages adopt an alternatively activated phenotype, involving reduced capacity for proinflammatory gene expression, constitutive IL-10 production, and impaired ability to support T cell activation, consistent with a role in maintaining testicular immune privilege.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                5 May 2017
                2017
                : 12
                : 5
                Affiliations
                [1 ]Department of Anatomy, Tokyo Medical University, Tokyo, Japan
                [2 ]Department of Anatomy, Aichi Medical University, Aichi, Japan
                University of Hyderabad, INDIA
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                • Conceptualization: MN MI.

                • Data curation: KY NH Shuichi Hirai NQ Shogo Hayashi SK KN.

                • Formal analysis: NH Shuichi Hirai.

                • Funding acquisition: MN MI.

                • Investigation: KY NH Shuichi Hirai MN MI.

                • Methodology: NH MN MI.

                • Resources: MN MI.

                • Supervision: Shuichi Hirai MN MI.

                • Validation: KY NH Shuichi Hirai.

                • Visualization: NH.

                • Writing – original draft: KY NH Shuichi Hirai MN MI.

                • Writing – review & editing: NH Shuichi Hirai MN MI.

                Article
                PONE-D-17-04282
                10.1371/journal.pone.0177067
                5419600
                28475594
                © 2017 Yi et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                Page count
                Figures: 9, Tables: 1, Pages: 17
                Product
                Funding
                Funded by: JSPS KAKENHI
                Award ID: 15K08159
                Award Recipient :
                Author Mashahiro Itoh received funding from JSPS KAKENHI (15K08159). The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Medicine and Health Sciences
                Surgical and Invasive Medical Procedures
                Transplantation
                Organ Transplantation
                Testicular Transplantation
                Medicine and Health Sciences
                Surgical and Invasive Medical Procedures
                Reproductive System Procedures
                Testicular Transplantation
                Biology and Life Sciences
                Anatomy
                Reproductive System
                Genital Anatomy
                Testes
                Medicine and Health Sciences
                Anatomy
                Reproductive System
                Genital Anatomy
                Testes
                Biology and Life Sciences
                Anatomy
                Reproductive System
                Genital Anatomy
                Seminiferous Tubules
                Medicine and Health Sciences
                Anatomy
                Reproductive System
                Genital Anatomy
                Seminiferous Tubules
                Medicine and Health Sciences
                Clinical Medicine
                Clinical Immunology
                Transplantation Immunology
                Biology and Life Sciences
                Immunology
                Clinical Immunology
                Transplantation Immunology
                Medicine and Health Sciences
                Immunology
                Clinical Immunology
                Transplantation Immunology
                Biology and Life Sciences
                Anatomy
                Histology
                Medicine and Health Sciences
                Anatomy
                Histology
                Medicine and Health Sciences
                Clinical Medicine
                Clinical Immunology
                Transplantation Immunology
                Transplant Rejection
                Biology and Life Sciences
                Immunology
                Clinical Immunology
                Transplantation Immunology
                Transplant Rejection
                Medicine and Health Sciences
                Immunology
                Clinical Immunology
                Transplantation Immunology
                Transplant Rejection
                Biology and Life Sciences
                Cell Biology
                Cellular Types
                Animal Cells
                Germ Cells
                Sperm
                Medicine and Health Sciences
                Surgical and Invasive Medical Procedures
                Cardiovascular Procedures
                Cardiac Transplantation
                Medicine and Health Sciences
                Surgical and Invasive Medical Procedures
                Transplantation
                Organ Transplantation
                Cardiac Transplantation
                Custom metadata
                All relevant data are within the paper and its Supporting Information files.

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