High glucose levels affect spermatogenesis: an in vitro approach
Renata S. Tavares A B , Joana M. D. Portela A , Maria I. Sousa A , Paula C. Mota A B , João Ramalho-Santos A C and Sandra Amaral A B D
+ Author Affiliations
- Author Affiliations
A Biology of Reproduction and Stem Cell Group, Center for Neuroscience and Cell Biology (CNC), University of Coimbra, Rua Larga, Faculty of Medicine, Pólo I, 3004-504 Coimbra, Portugal.
B Institute for Interdisciplinary Research, University of Coimbra, Casa Costa Alemão, Pólo II, Rua Dom Francisco Lemos, 3030-789 Coimbra, Portugal.
C Department of Life Sciences, University of Coimbra, Calçada Martim de Freitas, 3001-456 Coimbra, Portugal.
D Corresponding author. Email: scgamaral@gmail.com
Reproduction, Fertility and Development 29(7) 1369-1378 https://doi.org/10.1071/RD15475
Submitted: 14 November 2015 Accepted: 4 May 2016 Published: 6 June 2016
Abstract
Besides known factors that may cause male infertility, systemic diseases such as diabetes mellitus may further exacerbate a decline in male fertility. This metabolic disease, clinically characterised by a hyperglycaemic phenotype, has devastating consequences in terms of human health, with reproductive dysfunction being one of the associated clinical complications. Nonetheless, the mechanisms responsible for such alterations are still poorly understood due to the multiplicity of factors involved in the induced pathophysiological changes. With this in mind, we focused on the main mediator of diabetes-associated alterations and performed an in vitro approach to address the effects of high glucose conditions on spermatogenesis, avoiding other confounding in vivo factors. Mouse (5 days post partum) testis fragments were cultured on agar gel stands at a gas–liquid interface with either 5, 25 or 50 mM D-glucose for 3 weeks. Stereological analysis revealed that high D-glucose levels increased Sertoli cell number (P < 0.05) and decreased tubular luminal area (P < 0.01), suggesting an impairment of this somatic cell type. Moreover, higher proliferative activity in a TM4 Sertoli cell line exposed to high D-glucose was found (P < 0.05) without compromising cell viability (P > 0.05), further suggesting altered Sertoli cell maturation. Overall, high D-glucose concentrations may lead to impairment of Sertoli cell function, which, given their significant role in spermatogenic control, may compromise male fertility.
Additional keywords: diabetes mellitus, hyperglycaemia, organ culture, Sertoli cells.
References
Agbaje, I. M., Rogers, D. A., McVicar, C. M., McClure, N., Atkinson, A. B., Mallidis, C., and Lewis, S. E. (2007). Insulin dependant diabetes mellitus: implications for male reproductive function. Hum. Reprod. 22, 1871–1877.| Insulin dependant diabetes mellitus: implications for male reproductive function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXptFOrsLk%3D&md5=deb29046285e513bd2ea36cfdefafd7cCAS | 17478459PubMed |
Alves, M. G., Martins, A. D., Cavaco, J. E., Socorro, S., and Oliveira, P. F. (2013). Diabetes, insulin-mediated glucose metabolism and Sertoli/blood-testis barrier function. Tissue Barriers 1, e23992.
| Diabetes, insulin-mediated glucose metabolism and Sertoli/blood-testis barrier function.Crossref | GoogleScholarGoogle Scholar | 24665384PubMed |
Amaral, S., and Ramalho-Santos, J. (2014). Free radical biology and reproductive health in diabetes. In ‘Systems Biology of Free Radicals and Anti-Oxidants’. (Ed. I. Laher.) pp. 1–24. (Springer–Verlag: Berlin.)
Amaral, S., Moreno, A. J., Santos, M. S., Seiça, R., and Ramalho-Santos, J. (2006). Effects of hyperglycemia on sperm and testicular cells of Goto-Kakizaki and streptozotocin-treated rat models for diabetes. Theriogenology 66, 2056–2067.
| Effects of hyperglycemia on sperm and testicular cells of Goto-Kakizaki and streptozotocin-treated rat models for diabetes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1SmsLnP&md5=fe10caa5cff688c186b9a07151e347e1CAS | 16860381PubMed |
Amaral, S., Mota, P., Lacerda, B., Alves, M., de Lourdes Pereira, M., Oliveira, P. J., and Ramalho-Santos, J. (2009). Testicular mitochondrial alterations in untreated streptozotocin-induced diabetic rats. Mitochondrion 9, 41–50.
| Testicular mitochondrial alterations in untreated streptozotocin-induced diabetic rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXktlegur0%3D&md5=0aa2e46082db8a767d83441bf962bb72CAS | 19100345PubMed |
American Diabetes Association (2013). Diagnosis and classification of diabetes mellitus. Diabetes Care 36, S67–S74.
| Diagnosis and classification of diabetes mellitus.Crossref | GoogleScholarGoogle Scholar | 23264425PubMed |
Arikawe, A. P., Daramola, A. O., Odofin, A. O., and Obika, L. F. (2006). Alloxan-induced and insulin-resistant diabetes mellitus affect semen parameters and impair spermatogenesis in male rats. Afr. J. Reprod. Health 10, 106–113.
| Alloxan-induced and insulin-resistant diabetes mellitus affect semen parameters and impair spermatogenesis in male rats.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2szgslaltg%3D%3D&md5=e4c3c7bddddb6d1012bdcbd9875da384CAS | 17518137PubMed |
Auharek, S. A., and de França, L. R. (2010). Postnatal testis development, Sertoli cell proliferation and number of different spermatogonial types in C57BL/6J mice made transiently hypo- and hyperthyroidic during the neonatal period. J. Anat. 216, 577–588.
| Postnatal testis development, Sertoli cell proliferation and number of different spermatogonial types in C57BL/6J mice made transiently hypo- and hyperthyroidic during the neonatal period.Crossref | GoogleScholarGoogle Scholar | 20525087PubMed |
Baccetti, B., La Marca, A., Piomboni, P., Capitani, S., Bruni, E., Petraglia, F., and De Leo, V. (2002). Insulin dependent diabetes in men is associated with hypothalamo-pituitary derangement and with impairment in semen quality. Hum. Reprod. 17, 2673–2677.
| Insulin dependent diabetes in men is associated with hypothalamo-pituitary derangement and with impairment in semen quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xns1GgtLw%3D&md5=de99b848a2aaece0f975d0d51e733ddcCAS | 12351547PubMed |
Barták, V., Josífko, M., and Horácková, M. (1975). Juvenile diabetes and human sperm quality. Int. J. Fertil. 20, 30–32.
Bayram, S., Kizilay, G., and Topcu-Tarladacalisir, Y. (2016). Evaluation of the Fas/FasL signalling pathway in diabetic rat testis. Biotech. Histochem. 91, 204–211.
| Evaluation of the Fas/FasL signalling pathway in diabetic rat testis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XktlGqtb0%3D&md5=c1221a1bd776c6073346e83e898b59adCAS | 26960002PubMed |
Bellvé, A. R., Cavicchia, J. C., Millette, C. F., O’Brien, D. A., Bhatnagar, Y. M., and Dym, M. (1977). Spermatogenic cells of the prepuberal mouse. Isolation and morphological characterisation. J. Cell Biol. 74, 68–85.
| Spermatogenic cells of the prepuberal mouse. Isolation and morphological characterisation.Crossref | GoogleScholarGoogle Scholar | 874003PubMed |
Brehm, R., Zeiler, M., Rüttinger, C., Herde, K., Kibschull, M., Winterhager, E., Willecke, K., Guillou, F., Lécureuil, C., Steger, K., Konrad, L., Biermann, K., Failing, K., and Bergmann, M. (2007). A Sertoli cell-specific knockout of connexin43 prevents initiation of spermatogenesis. Am. J. Pathol. 171, 19–31.
| A Sertoli cell-specific knockout of connexin43 prevents initiation of spermatogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXosValsrw%3D&md5=ac6c8a260e5d67407f3e107b9c33ff56CAS | 17591950PubMed |
Burant, C. F., and Davidson, N. O. (1994). GLUT3 glucose transporter isoform in rat testis: localisation, effect of diabetes mellitus and comparison to human testis. Am. J. Physiol. 267, R1488–R1495.
| 1:CAS:528:DyaK2MXivFGksLY%3D&md5=435425f5d4801a351d64ff3f452475c6CAS | 7810757PubMed |
Cameron, D. F., Murray, F. T., and Drylie, D. D. (1985). Interstitial compartment pathology and spermatogenic disruption in testes from impotent diabetic men. Anat. Rec. 213, 53–62.
| Interstitial compartment pathology and spermatogenic disruption in testes from impotent diabetic men.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL28%2FnsFWiuw%3D%3D&md5=c47809a8a78bea78fe59df16bcf14cb0CAS | 4073561PubMed |
Cameron, D. F., Rountree, J., Schultz, R. E., Repetta, D., and Murray, F. T. (1990). Sustained hyperglycemia results in testicular dysfunction and reduced fertility potential in BBWOR diabetic rats. Am. J. Physiol. 259, E881–E889.
| 1:CAS:528:DyaK3MXnvFGltQ%3D%3D&md5=bd9bfa1ae83bfbd033aa63b1f5416c91CAS | 2260654PubMed |
De Kretser, D. M., and Kerr, J. B. (1994). The cytology of the testis. In ‘The Physiology of Reproduction’. (Eds E. Knobil and J. D. Neill.) pp. 1177–1290. (Raven Press Ltd: New York.)
Delfino, M., Imbrogno, N., Elia, J., Capogreco, F., and Mazzilli, F. (2007). Prevalence of diabetes mellitus in male partners of infertile couples. Minerva Urol. Nefrol. 59, 131–135.
| 1:STN:280:DC%2BD2szlvVamtA%3D%3D&md5=121747dc38b888de92b8e53b78a54df4CAS | 17571048PubMed |
Dohle, G. R., Colpi, G. M., Hargreave, T. B., Papp, G. K., Jungwirth, A., and Weidner, W. (2005). EAU guidelines on male infertility. Eur. Urol. 48, 703–711.
| EAU guidelines on male infertility.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2Mrltl2jsQ%3D%3D&md5=34d8a95f049be95905a725bd4c17deb1CAS | 16005562PubMed |
Emilien, G., Maloteaux, J. M., and Ponchon, M. (1999). Pharmacological management of diabetes: recent progress and future perspective of daily drug treatment. Pharmacol. Ther. 81, 37–51.
| Pharmacological management of diabetes: recent progress and future perspective of daily drug treatment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhtFensg%3D%3D&md5=6ad7aded3db3e1aa2494c88f95a8cc22CAS | 10051177PubMed |
Gondos, B., and Bevier, W. (1995). Effect of insulin on testicular alterations in the nonobese diabetic mouse. Ann. Clin. Lab. Sci. 25, 272–277.
| 1:CAS:528:DyaK2MXmtlGjsrg%3D&md5=95b1ec2e4f72f71d5de0b555aaa114b2CAS | 7605110PubMed |
Gondos, B., Rivkind, Y., and Jovanovic, L. (1998). Effect of increasing glucose concentrations on Sertoli cell viability in the nonobese diabetic mouse. Ann. Clin. Lab. Sci. 28, 236–241.
| 1:CAS:528:DyaK1MXhvVOmsb0%3D&md5=1e27feaabc2a8c10e3a62f9d0e37232aCAS | 9715350PubMed |
Griswold, M. D. (2012). Making male gametes in culture. Proc. Natl. Acad. Sci. USA 109, 16762–16763.
| Making male gametes in culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1Wks7bJ&md5=ee4ba23b9e46f4a65801d7bbd8013486CAS | 23047695PubMed |
Griswold, M. D., Morales, C., and Sylvester, S. R. (1988). Molecular biology of the Sertoli cell. Oxf. Rev. Reprod. Biol. 10, 124–161.
| 1:STN:280:DyaL1M3itVSltw%3D%3D&md5=fb4fcd32389cdf442c837bb1fe29c6efCAS | 3072501PubMed |
Handelsman, D. J., Conway, A. J., Boylan, L. M., Yue, D. K., and Turtle, J. R. (1985). Testicular function and glycemic control in diabetic men. A controlled study. Andrologia 17, 488–496.
| Testicular function and glycemic control in diabetic men. A controlled study.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL28%2FkvVKgsA%3D%3D&md5=192505b17a694449a6633d0e06838328CAS | 3933383PubMed |
Hassan, A. A., Hassouna, M. M., Taketo, T., Gagnon, C., and Elhilai, M. M. (1993). The effect of diabetes on sexual behavior and reproductive tract function in male rats. J. Urol. 149, 148–154.
| 1:STN:280:DyaK3s7gvVGhtA%3D%3D&md5=593de888422655ad2b6b9666cfebad52CAS | 8417201PubMed |
Hermo, L., Pelletier, R. M., Cyr, D. G., and Smith, C. E. (2010). Surfing the wave, cycle, life history, and genes/proteins expressed by testicular germ cells. Part 1: background to spermatogenesis, spermatogonia, and spermatocytes. Microsc. Res. Tech. 73, 241–278.
| Surfing the wave, cycle, life history, and genes/proteins expressed by testicular germ cells. Part 1: background to spermatogenesis, spermatogonia, and spermatocytes.Crossref | GoogleScholarGoogle Scholar | 19941293PubMed |
Holstein, A. F., Schulze, W., and Davidoff, M. (2003). Understanding spermatogenesis is a prerequisite for treatment. Reprod. Biol. Endocrinol. 1, 107.
| Understanding spermatogenesis is a prerequisite for treatment.Crossref | GoogleScholarGoogle Scholar | 14617369PubMed |
Hutson, J. C. (1984). Altered biochemical responses by rat Sertoli cells and peritubular cells cultured under simulated diabetic conditions. Diabetologia 26, 155–158.
| Altered biochemical responses by rat Sertoli cells and peritubular cells cultured under simulated diabetic conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXhslalsL8%3D&md5=1a7c12282a7f62eb95f9091b7da7147eCAS | 6325283PubMed |
Irvine, D. S. (1998). Epidemiology and aetiology of male infertility. Hum. Reprod. 13, 33–44.
| Epidemiology and aetiology of male infertility.Crossref | GoogleScholarGoogle Scholar | 9663768PubMed |
Jangir, R. N., and Jain, G. C. (2014). Diabetes mellitus induced impairment of male reproductive functions: a review. Curr. Diabetes Rev. 10, 147–157.
| Diabetes mellitus induced impairment of male reproductive functions: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtFOjsrjI&md5=f025ac1dd50052a1d0d9a46ecd8b9293CAS | 24919656PubMed |
Jørgensen, A., Nielsen, J. E., Perlman, S., Lundvall, L., Mitchell, R. T., Juul, A., and Rajpert-De Meyts, E. (2015). Ex vivo culture of human fetal gonads: manipulation of meiosis signalling by retinoic acid treatment disrupts testis development. Hum. Reprod. 30, 2351–2363.
| Ex vivo culture of human fetal gonads: manipulation of meiosis signalling by retinoic acid treatment disrupts testis development.Crossref | GoogleScholarGoogle Scholar | 26251460PubMed |
Kianifard, D., Sadrkhanlou, R. A., and Hasanzadeh, S. (2012). The ultrastructural changes of the Sertoli and Leydig cells following streptozotocin induced diabetes. Iran. J. Basic Med. Sci. 15, 623–635.
| 23493249PubMed |
Kim, S. T., and Moley, K. H. (2008). Paternal effect on embryo quality in diabetic mice is related to poor sperm quality and associated with decreased glucose transporter expression. Reproduction 136, 313–322.
| Paternal effect on embryo quality in diabetic mice is related to poor sperm quality and associated with decreased glucose transporter expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1GmtLzF&md5=adac470197d38ba0af4e200bb66ccde5CAS | 18558660PubMed |
Klip, A., Tsakiridis, T., Marette, A., and Ortiz, P. A. (1994). Regulation of expression of glucose transporters by glucose: a review of studies in vivo and in cell cultures. FASEB J. 8, 43–53.
| 1:CAS:528:DyaK2cXhvVOkt7o%3D&md5=216520cfae0a23ecc89f9e0709865e35CAS | 8299889PubMed |
Kühn-Velten, N., Shermer, R., and Staib, W. (1984). Effect of streptozotocin-induced hyperglycaemia on androgen-binding protein in the testis and epididymis. Diabetologia 26, 300–303.
| Effect of streptozotocin-induced hyperglycaemia on androgen-binding protein in the testis and epididymis.Crossref | GoogleScholarGoogle Scholar | 6539717PubMed |
Kumi-Diaka, J., and Butler, A. (2000). Caspase-3 protease activation during the process of genistein-induced apoptosis in TM4 testicular cells. Biol. Cell 92, 115–124.
| Caspase-3 protease activation during the process of genistein-induced apoptosis in TM4 testicular cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXksVGiur8%3D&md5=bd8384dae8fc140b0908bab5e5482b74CAS | 10879632PubMed |
Kyathanahalli, C., Bangalore, S., Hanumanthappa, K., and Muralidhara, (2014). Experimental diabetes-induced testicular damage in prepubertal rats. J. Diabetes 6, 48–59.
| Experimental diabetes-induced testicular damage in prepubertal rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvV2mtLvL&md5=70e0aa30c79b02409dfe1f9c945400a6CAS | 23773549PubMed |
La Vignera, S., Condorelli, R., Vicari, E., D’Agata, R., and Calogero, A. E. (2012). Diabetes mellitus and sperm parameters. J. Androl. 33, 145–153.
| Diabetes mellitus and sperm parameters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XktVyrs70%3D&md5=f8c7b3cde3082ccd0eff43fa5d4927c9CAS | 21474785PubMed |
Lo, K. C., and Domes, T. (2011). Can we grow sperm? A translational perspective on the current animal and human spermatogenesis models. Asian J. Androl. 13, 677–682.
| Can we grow sperm? A translational perspective on the current animal and human spermatogenesis models.Crossref | GoogleScholarGoogle Scholar | 21765440PubMed |
Lucas, M. J., Leveno, K. J., Williams, M. L., Raskin, P., and Whalley, P. J. (1989). Early pregnancy glycosylated hemoglobin, severity of diabetes, and fetal malformations. Am. J. Obstet. Gynecol. 161, 426–431.
| Early pregnancy glycosylated hemoglobin, severity of diabetes, and fetal malformations.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1MzkvFaktA%3D%3D&md5=0aad30d6f5c565930fbbdd4f1d961268CAS | 2669494PubMed |
Mangoli, E., Talebi, A. R., Anvari, M., and Pourentezari, M. (2013). Effects of experimentally-induced diabetes on sperm parameters and chromatin quality in mice. Iran. J. Reprod. Med. 11, 53–60.
| 1:CAS:528:DC%2BC3sXpsFCns78%3D&md5=239073ed6cb84c874e88dc9ff140652fCAS | 24639693PubMed |
Marx, J. (2002). Unravelling the causes of diabetes. Science 296, 686–689.
| Unravelling the causes of diabetes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjtlOhtbw%3D&md5=1ba126aafdede91137715bd8769db10fCAS | 11976439PubMed |
Miller, E., Hare, J. W., Cloherty, J. P., Dunn, P. J., Gleason, R. E., Soeldner, J. S., and Kitzmiller, J. L. (1981). Elevated maternal hemoglobin A1c in early pregnancy and major congenital anomalies in infants of diabetic mothers. N. Engl. J. Med. 304, 1331–1334.
| Elevated maternal hemoglobin A1c in early pregnancy and major congenital anomalies in infants of diabetic mothers.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3M7nt12itA%3D%3D&md5=0406dd658d108c69ff0250a62bfd76e0CAS | 7012627PubMed |
Mota, P. C., Ehmcke, J., Westernströer, B., Gassei, K., Ramalho-Santos, J., and Schlatt, S. (2012). Effects of different storage protocols on cat testis tissue potential for xenografting and recovery of spermatogenesis. Theriogenology 77, 299–310.
| Effects of different storage protocols on cat testis tissue potential for xenografting and recovery of spermatogenesis.Crossref | GoogleScholarGoogle Scholar | 21958640PubMed |
Mulholland, J., Mallidis, C., Agbaje, I., and McClure, N. (2011). Male diabetes mellitus and assisted reproduction treatment outcome. Reprod. Biomed. Online 22, 215–219.
| Male diabetes mellitus and assisted reproduction treatment outcome.Crossref | GoogleScholarGoogle Scholar | 21227754PubMed |
Navarro-Casado, L., Juncos-Tobarra, M. A., Cháfer-Rudilla, M., de Onzono, L. I., Blázquez-Cabrera, J. A., and Miralles-García, J. M. (2010). Effect of experimental diabetes and STZ on male fertility capacity. Study in rats. J. Androl. 31, 584–592.
| Effect of experimental diabetes and STZ on male fertility capacity. Study in rats.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cbms1aktg%3D%3D&md5=544c825126822134cf118a669cab610dCAS | 20203339PubMed |
Oliveira, P. F., Alves, M. G., Rato, L., Laurentino, S., Silva, J., Sá, R., Barros, A., Sousa, M., Carvalho, R. A., Cavaco, J. E., and Socorro, S. (2012). Effect of insulin deprivation on metabolism and metabolism-associated gene transcript levels of in vitro cultured human Sertoli cells. Biochim. Biophys. Acta 1820, 84–89.
| Effect of insulin deprivation on metabolism and metabolism-associated gene transcript levels of in vitro cultured human Sertoli cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xos1yguw%3D%3D&md5=c3ef12821b5ed460b80b42f9452c0a7aCAS | 22146232PubMed |
Oonk, R. B., and Grootegoed, J. A. (1987). Identification of insulin receptors on rat Sertoli cells. Mol. Cell. Endocrinol. 49, 51–62.
| Identification of insulin receptors on rat Sertoli cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXnvFWnsQ%3D%3D&md5=e77ce6558ac0d22d895b81e16f6074a9CAS | 3549388PubMed |
Oonk, R. B., Grootegoed, J. A., and van der Molen, H. J. (1985). Comparison of the effects of insulin and follitropin on glucose metabolism by Sertoli cells from immature rats. Mol. Cell. Endocrinol. 42, 39–48.
| Comparison of the effects of insulin and follitropin on glucose metabolism by Sertoli cells from immature rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXltFKlt7s%3D&md5=1002a1a88699133a362d7566875ed6c7CAS | 3928417PubMed |
Padrón, R. S., Dambay, A., Suárez, R., and Más, J. (1984). Semen analyses in adolescent diabetic patients. Acta Diabetol. Lat. 21, 115–121.
| Semen analyses in adolescent diabetic patients.Crossref | GoogleScholarGoogle Scholar | 6475450PubMed |
Portela, J. M. D., Tavares, R. S., Mota, P. C., Ramalho-Santos, J., and Amaral, S. (2015). High glucose concentrations per se do not adversely affect human sperm function in vitro. Reproduction 150, 77–84.
| High glucose concentrations per se do not adversely affect human sperm function in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhsV2ktLzF&md5=04169bd9e8658e65954fc2455abaa74fCAS |
Riera, M. F., Meroni, S. B., Schteingart, H. F., Pellizzari, E. H., and Cigorraga, S. B. (2002). Regulation of lactate production and glucose transport as well as of glucose transporter 1 and lactate dehydrogenase A mRNA levels by basic fibroblast growth factor in rat Sertoli cells. J. Endocrinol. 173, 335–343.
| Regulation of lactate production and glucose transport as well as of glucose transporter 1 and lactate dehydrogenase A mRNA levels by basic fibroblast growth factor in rat Sertoli cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xkt1Slsb0%3D&md5=3f8b2b6330e2623b960b36a1eed2204dCAS | 12010641PubMed |
Riera, M. F., Galardo, M. N., Pellizzari, E. H., Meroni, S. B., and Cigorraga, S. B. (2009). Molecular mechanisms involved in Sertoli cell adaptation to glucose deprivation. Am. J. Physiol. Endocrinol. Metab. 297, E907–E914.
| Molecular mechanisms involved in Sertoli cell adaptation to glucose deprivation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlensbbL&md5=dd3b41813bcd38ec896281b3d293f5f7CAS | 19638510PubMed |
Rodriguez, I., Ody, C., Araki, K., Garcia, I., and Vassalli, P. (1997). An early and massive wave of germinal cell apoptosis is required for the development of functional spermatogenesis. EMBO J. 16, 2262–2270.
| An early and massive wave of germinal cell apoptosis is required for the development of functional spermatogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjsV2nu7Y%3D&md5=40d118ba11972ac31d1c74c612366f81CAS | 9171341PubMed |
Ruwanpura, S. M., McLachlan, R. I., and Meachem, S. J. (2010). Hormonal regulation of male germ cell development. J. Endocrinol. 205, 117–131.
| Hormonal regulation of male germ cell development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmvVCgs7s%3D&md5=6b3f175907ae32352757b9f76cc1e30dCAS | 20144980PubMed |
Sato, T., Katagiri, K., Gohbara, A., Inoue, K., Ogonuki, N., Ogura, A., Kubota, Y., and Ogawa, T. (2011). In vitro production of functional sperm in cultured neonatal mouse testes. Nature 471, 504–507.
| In vitro production of functional sperm in cultured neonatal mouse testes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjvVOiu74%3D&md5=0ebb561720547327af771b6f3b71ac5fCAS | 21430778PubMed |
Sato, T., Katagiri, K., Kubota, Y., and Ogawa, T. (2013). In vitro sperm production from mouse spermatogonial stem cell lines using an organ culture method. Nat. Protoc. 8, 2098–2104.
| In vitro sperm production from mouse spermatogonial stem cell lines using an organ culture method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsFGqt7fE&md5=031f4049fd6525c239a2bda84eb1df22CAS | 24091557PubMed |
Scarano, W. R., Messias, A. G., Oliva, S. U., Klinefelter, G. R., and Kempinas, W. G. (2006). Sexual behaviour, sperm quantity and quality after short-term streptozotocin-induced hyperglycaemia in rats. Int. J. Androl. 29, 482–488.
| Sexual behaviour, sperm quantity and quality after short-term streptozotocin-induced hyperglycaemia in rats.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28vntVemtw%3D%3D&md5=a76d6225d08f921d9a16990b7b6db4acCAS | 16524366PubMed |
Schoeller, E. L., Schon, S., and Moley, K. H. (2012a). The effects of type 1 diabetes on the hypothalamic, pituitary and testes axis. Cell Tissue Res. 349, 839–847.
| The effects of type 1 diabetes on the hypothalamic, pituitary and testes axis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1yltbrL&md5=6c8bb8fd3d753d19da41654eacc49239CAS | 22526620PubMed |
Schoeller, E. L., Albanna, G., Frolova, A. I., and Moley, K. H. (2012b). Insulin rescues impaired spermatogenesis via the hypothalamic-pituitary-gonadal axis in Akita diabetic mice and restores male fertility. Diabetes 61, 1869–1878.
| Insulin rescues impaired spermatogenesis via the hypothalamic-pituitary-gonadal axis in Akita diabetic mice and restores male fertility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVCrs7nM&md5=897802222b482edb495d349a21bd456bCAS | 22522616PubMed |
Seethalakshmi, L., Menon, M., and Diamond, D. (1987). The effect of streptozotocin-induced diabetes on the neuroendocrine-male reproductive tract axis of the adult rat. J. Urol. 138, 190–194.
| 1:STN:280:DyaL2s3lsVCrtA%3D%3D&md5=0cc6f07592dbc3b7e9e7a840731fdaf1CAS | 3599211PubMed |
Sharpe, R. M., McKinnell, C., Kivlin, C., and Fisher, J. S. (2003). Proliferation and functional maturation of Sertoli cells, and their relevance to disorders of testis function in adulthood. Reproduction 125, 769–784.
| Proliferation and functional maturation of Sertoli cells, and their relevance to disorders of testis function in adulthood.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXltFelt7c%3D&md5=10cf4b0261e962d361c84957f26be906CAS | 12773099PubMed |
Shrilatha, B., and Muralidhara, (2007). Early oxidative stress in testis and epididymal sperm in streptozotocin-induced diabetic mice: its progression and genotoxic consequences. Reprod. Toxicol. 23, 578–587.
| Early oxidative stress in testis and epididymal sperm in streptozotocin-induced diabetic mice: its progression and genotoxic consequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlsFKlt74%3D&md5=cad700caa11b37c005bcaac20adbbb48CAS | 17360155PubMed |
Soudamani, S., Malini, T., and Balasubramanian, K. (2005). Effects of streptozotocin-diabetes and insulin replacement on the epididymis of prepubertal rats: histological and histomorphometric studies. Endocr. Res. 31, 81–98.
| Effects of streptozotocin-diabetes and insulin replacement on the epididymis of prepubertal rats: histological and histomorphometric studies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1Gltb3E&md5=479759b2da7809ed38099cc775721d65CAS | 16353669PubMed |
Staub, C. (2001). A century of research on mammalian male germ cell meiotic differentiation in vitro. J. Androl. 22, 911–926.
| A century of research on mammalian male germ cell meiotic differentiation in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXotlygu7w%3D&md5=5f645b8a0717a8d47ef86ffac0a5444bCAS | 11700854PubMed |
Taylor, C. R. (2009). Immunohistochemical standardisation and ready-to-use antibodies methods. In ‘Immunohistochemical Staining Methods’. (Eds G. L. Kumar and L. Rudbeck.) pp. 21–28. (Dako: North America.)
Tremellen, K. (2008). Oxidative stress and male infertility – a clinical perspective. Hum. Reprod. Update 14, 243–258.
| Oxidative stress and male infertility – a clinical perspective.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXkvFOqtbc%3D&md5=0c549fa3dd4a4932c4975182d5a4f1daCAS | 18281241PubMed |
Vignon, F., Le Faou, A., Montagnon, D., Pradignac, A., Cranz, C., Winiszewsky, P., and Pinget, M. (1991). Comparative study of semen in diabetic and healthy men. Diabete Metab. 17, 350–354.
| 1:STN:280:DyaK3Mzlslamsg%3D%3D&md5=9da29971f3eaa36d45dd7d8e4e56c647CAS | 1884879PubMed |
Wankeu-Nya, M., Florea, A., Bâlici, S., Watcho, P., Matei, H., and Kamanyi, A. (2013). Dracaena arborea alleviates ultra-structural spermatogenic alterations in streptozotocin-induced diabetic rats. BMC Complement. Altern. Med. 13, 71–80.
| Dracaena arborea alleviates ultra-structural spermatogenic alterations in streptozotocin-induced diabetic rats.Crossref | GoogleScholarGoogle Scholar | 23548080PubMed |
Weinbauer, G. F., Luetjens, C. M., Simoni, M., and Nieschlag, E. (2010). Physiology of testicular function. In ‘Andrology: Male Reproductive Health and Dysfunction’. (Eds E. Nieschlag, H. Behre, and S. Nieschlag.) pp. 11–59. (Springer Berlin Heidelberg: Berlin.)
Wild, S., Roglic, G., Green, A., Sicree, R., and King, H. (2004). Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care 27, 1047–1053.
| Global prevalence of diabetes: estimates for the year 2000 and projections for 2030.Crossref | GoogleScholarGoogle Scholar | 15111519PubMed |
Wistuba, J., Schrod, A., Greve, B., Hodges, J. K., Aslam, H., Weinbauer, G. F., and Luetjens, C. M. (2003). Organisation of seminiferous epithelium in primates: relationship to spermatogenic efficiency, phylogeny, and mating system. Biol. Reprod. 69, 582–591.
| Organisation of seminiferous epithelium in primates: relationship to spermatogenic efficiency, phylogeny, and mating system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlvVerurg%3D&md5=08a8b1af29898fcd6ba37df32a2c7a26CAS | 12700190PubMed |
