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Journal of Diabetes Research
Volume 2015 (2015), Article ID 973142, 13 pages
http://dx.doi.org/10.1155/2015/973142
Research Article

Testicular Metabolic Reprogramming in Neonatal Streptozotocin-Induced Type 2 Diabetic Rats Impairs Glycolytic Flux and Promotes Glycogen Synthesis

1Health Sciences Research Centre (CICS), Faculty of Health Sciences, University of Beira Interior (UBI), Covilhã, Portugal
2Department of Life Sciences, Faculty of Sciences and Technology and Center for Neurosciences and Cell Biology (CNC), University of Coimbra, Portugal
3Department of Microscopy, Laboratory of Cell Biology, Abel Salazar Institute of Biomedical Sciences (ICBAS), University of Porto, Portugal
4Unit for Multidisciplinary Research in Biomedicine (UMIB), Abel Salazar Institute of Biomedical Sciences (ICBAS), University of Porto (UP), Portugal

Received 26 November 2014; Revised 22 April 2015; Accepted 23 April 2015

Academic Editor: Maria Pia Francescato

Copyright © 2015 L. Rato et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. American Diabetes Association, “Diagnosis and classification of diabetes mellitus,” Diabetes Care, vol. 36, supplement 1, pp. S67–S74, 2012. View at Publisher · View at Google Scholar
  2. L. Seethalakshmi, M. Menon, and D. Diamond, “The effect of streptozotocin-induced diabetes on the neuroendocrine-male reproductive tract axis of the adult rat,” Journal of Urology, vol. 138, no. 1, pp. 190–194, 1987. View at Google Scholar · View at Scopus
  3. V. Bartak, “Sperm quality in adult diabetic men,” International Journal of Fertility, vol. 24, no. 4, pp. 226–232, 1979. View at Google Scholar · View at Scopus
  4. R. S. Padrón, A. Dambay, R. Suárez, and J. Más, “Semen analyses in adolescent diabetic patients,” Acta Diabetologia Latina, vol. 21, no. 2, pp. 115–121, 1984. View at Publisher · View at Google Scholar · View at Scopus
  5. S. La Vignera, R. Condorelli, E. Vicari, R. D'Agata, and A. E. Calogero, “Diabetes mellitus and sperm parameters,” Journal of Andrology, vol. 33, no. 2, pp. 145–153, 2012. View at Publisher · View at Google Scholar · View at Scopus
  6. F. Vignon, A. le Faou, D. Montagnon et al., “Comparative study of semen in diabetic and healthy men,” Diabètes et Métabolisme, vol. 17, no. 3, pp. 350–354, 1991. View at Google Scholar · View at Scopus
  7. B. E. Hamilton, D. L. Hoyert, J. A. Martin, D. M. Strobino, and B. Guyer, “Annual summary of vital statistics: 2010-2011,” Pediatrics, vol. 131, no. 3, pp. 548–558, 2013. View at Publisher · View at Google Scholar · View at Scopus
  8. W. Lutz, H. Leridon, R. J. Aitken, and F. E. Von Eyben, “Fertility rates and future population trends: Will Europe's birth rate recover or continue to decline?” International Journal of Andrology, vol. 29, no. 1, pp. 25–33, 2006. View at Publisher · View at Google Scholar · View at Scopus
  9. L. Rato, M. G. Alves, T. R. Dias et al., “High-energy diets may induce a pre-diabetic state altering testicular glycolytic metabolic profile and male reproductive parameters,” Andrology, vol. 1, no. 3, pp. 495–504, 2013. View at Publisher · View at Google Scholar · View at Scopus
  10. R. L. Bernardino, T. T. Jesus, A. D. Martins et al., “Molecular basis of bicarbonate membrane transport in the male reproductive tract,” Current Medicinal Chemistry, vol. 20, no. 32, pp. 4037–4049, 2013. View at Publisher · View at Google Scholar · View at Scopus
  11. J. K. Beckman and J. G. Coniglio, “A comparative study of the lipid composition of isolated rat Sertoli and germinal cells,” Lipids, vol. 14, no. 3, pp. 262–267, 1979. View at Publisher · View at Google Scholar · View at Scopus
  12. I. Gillot, C. Jehl-Pietr, P. Gounon et al., “Germ cells and fatty acids induce translocation of CD36 scavenger receptor to the plasma membrane of Sertoli cells,” Journal of Cell Science, vol. 118, no. 14, pp. 3027–3035, 2005. View at Publisher · View at Google Scholar · View at Scopus
  13. P. F. Oliveira, A. D. Martins, A. C. Moreira, C. Y. Cheng, and M. G. Alves, “The Warburg effect revisited—lesson from the Sertoli cell,” Medicinal Research Reviews, vol. 35, no. 1, pp. 126–151, 2015. View at Publisher · View at Google Scholar
  14. N. H. P. M. Jutte, J. A. Grootegoed, F. F. G. Rommerts, and H. J. Van der Molen, “Exogenous lactate is essential for metabolic activities in isolated rat spermatocytes and spermatids,” Reproduction, vol. 62, no. 2, pp. 399–405, 1981. View at Publisher · View at Google Scholar · View at Scopus
  15. R. Robinson and I. B. Fritz, “Metabolism of glucose by Sertoli cells in culture,” Biology of Reproduction, vol. 24, no. 5, pp. 1032–1041, 1981. View at Publisher · View at Google Scholar · View at Scopus
  16. N. H. P. M. Jutte, R. Jansen, J. A. Grootegoed, F. F. Rommerts, O. P. Clausen, and H. J. van der Molen, “Regulation of survival of rat pachytene spermatocytes by lactate supply from Sertoli cells,” Journal of Reproduction and Fertility, vol. 65, no. 2, pp. 431–438, 1982. View at Publisher · View at Google Scholar · View at Scopus
  17. L. Rato, M. G. Alves, S. Socorro, R. A. Carvalho, J. E. Cavaco, and P. F. Oliveira, “Metabolic modulation induced by oestradiol and DHT in immature rat Sertoli cells cultured in vitro,” Bioscience Reports, vol. 32, no. 1, pp. 61–69, 2012. View at Publisher · View at Google Scholar · View at Scopus
  18. M. G. Alves, A. D. Martins, L. Rato, P. I. Moreira, S. Socorro, and P. F. Oliveira, “Molecular mechanisms beyond glucose transport in diabetes-related male infertility,” Biochimica et Biophysica Acta—Molecular Basis of Disease, vol. 1832, no. 5, pp. 626–635, 2013. View at Publisher · View at Google Scholar · View at Scopus
  19. L. Rato, M. G. Alves, S. Socorro, A. I. Duarte, J. E. Cavaco, and P. F. Oliveira, “Metabolic regulation is important for spermatogenesis,” Nature Reviews Urology, vol. 9, no. 6, pp. 330–338, 2012. View at Publisher · View at Google Scholar · View at Scopus
  20. L. Rato, A. I. Duarte, G. D. Tomás et al., “Pre-diabetes alters testicular PGC1-α/SIRT3 axis modulating mitochondrial bioenergetics and oxidative stress,” Biochimica et Biophysica Acta, vol. 1837, no. 3, pp. 335–344, 2014. View at Publisher · View at Google Scholar · View at Scopus
  21. L. Rato, M. G. Alves, J. E. Cavaco, and P. F. Oliveira, “High-energy diets: a threat for male fertility?” Obesity Reviews, vol. 15, no. 12, pp. 996–1007, 2014. View at Publisher · View at Google Scholar
  22. B. Leiderman and R. E. Mancini, “Glycogen content in the rat testis from postnatal to adult ages,” Endocrinology, vol. 85, no. 3, pp. 607–609, 1969. View at Publisher · View at Google Scholar · View at Scopus
  23. G. R. Slaughter and A. R. Means, “Follicle-stimulating hormone activation of glycogen phosphorylase in the Sertoli cell-enriched rat testis,” Endocrinology, vol. 113, no. 4, pp. 1476–1485, 1983. View at Publisher · View at Google Scholar · View at Scopus
  24. F. Villarroel-Espíndola, R. Maldonado, H. Mancilla et al., “Muscle glycogen synthase isoform is responsible for testicular glycogen synthesis: glycogen overproduction induces apoptosis in male germ cells,” Journal of Cellular Biochemistry, vol. 114, no. 7, pp. 1653–1664, 2013. View at Publisher · View at Google Scholar · View at Scopus
  25. M. J. Spiro, “Effects of diabetes on the sugar nucleotides in several tissues of the rat,” Diabetologia, vol. 26, no. 1, pp. 70–75, 1984. View at Google Scholar · View at Scopus
  26. M. Iwase, M. Kikuchi, K. Nunoi et al., “A new model of type 2 (non-insulin-dependent) diabetes mellitus in spontaneously hypertensive rats: diabetes induced by neonatal streptozotocin treatment,” Diabetologia, vol. 29, no. 11, pp. 808–811, 1986. View at Publisher · View at Google Scholar · View at Scopus
  27. A. G. Holmes, J. L. Mesa, B. A. Neill et al., “Prolonged interleukin-6 administration enhances glucose tolerance and increases skeletal muscle PPARalpha and UCP2 expression in rats,” Journal of Endocrinology, vol. 198, no. 2, pp. 367–374, 2008. View at Google Scholar
  28. M. W. Pfaffl, “A new mathematical model for relative quantification in real-time RT-PCR,” Nucleic Acids Research, vol. 29, no. 9, article e45, 2001. View at Publisher · View at Google Scholar · View at Scopus
  29. V. L. Simões, M. G. Alves, A. D. Martins et al., “Regulation of apoptotic signaling pathways by 5α-dihydrotestosterone and 17β-estradiol in immature rat Sertoli cells,” The Journal of Steroid Biochemistry and Molecular Biology, vol. 135, no. 1, pp. 15–23, 2013. View at Publisher · View at Google Scholar · View at Scopus
  30. M. G. Alves, A. D. Martins, C. V. Vaz et al., “Metformin and male reproduction: effects on Sertoli cell metabolism,” British Journal of Pharmacology, vol. 171, no. 4, pp. 1033–1042, 2014. View at Publisher · View at Google Scholar · View at Scopus
  31. A. F. Mohun and I. J. Cook, “Simple methods for measuring serum levels of the glutamic-oxalacetic and glutamic-pyruvic transaminases in routine laboratories,” Journal of Clinical Pathology, vol. 10, no. 4, pp. 394–399, 1957. View at Publisher · View at Google Scholar · View at Scopus
  32. T. R. Dias, M. G. Alves, G. D. Tomás, S. Socorro, B. M. Silva, and P. F. Oliveira, “White tea as a promising antioxidant medium additive for sperm storage at room temperature: a comparative study with green tea,” Journal of Agricultural and Food Chemistry, vol. 62, no. 3, pp. 608–617, 2014. View at Publisher · View at Google Scholar · View at Scopus
  33. G. Lopes, A. Simões, P. Ferreira, A. Martins-Bessa, and A. Rocha, “Differences in preservation of canine chilled semen using different transport containers,” Animal Reproduction Science, vol. 112, no. 1-2, pp. 158–163, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. A. J. F. King, “The use of animal models in diabetes research,” British Journal of Pharmacology, vol. 166, no. 3, pp. 877–894, 2012. View at Publisher · View at Google Scholar · View at Scopus
  35. A. Junod, A. E. Lambert, W. Stauffacher, and A. E. Renold, “Diabetogenic action of streptozotocin: relationship of dose to metabolic response,” Journal of Clinical Investigation, vol. 48, no. 11, pp. 2129–2139, 1969. View at Publisher · View at Google Scholar · View at Scopus
  36. Y. Ning, W. Zhen, Z. Fu et al., “Ranolazine increases β-cell survival and improves glucose homeostasis in low-dose streptozotocin-induced diabetes in mice,” Journal of Pharmacology and Experimental Therapeutics, vol. 337, no. 1, pp. 50–58, 2011. View at Publisher · View at Google Scholar · View at Scopus
  37. G. M. Steil, N. Trivedi, J.-C. Jonas et al., “Adaptation of β-cell mass to substrate oversupply: enhanced function with normal gene expression,” The American Journal of Physiology—Endocrinology and Metabolism, vol. 280, no. 5, pp. E788–E796, 2001. View at Google Scholar · View at Scopus
  38. M. Maneesh, H. Jayalakshmi, T. A. Singh, and A. Chakrabarti, “Impaired hypothalamic-pituitary-gonadal axis function in men with diabetes mellitus,” Indian Journal of Clinical Biochemistry, vol. 21, no. 1, pp. 165–168, 2006. View at Publisher · View at Google Scholar · View at Scopus
  39. N. Pitteloud, M. Hardin, A. A. Dwyer et al., “Increasing insulin resistance is associated with a decrease in Leydig cell testosterone secretion in men,” The Journal of Clinical Endocrinology & Metabolism, vol. 90, no. 5, pp. 2636–2641, 2005. View at Publisher · View at Google Scholar · View at Scopus
  40. P. M. Rao, D. M. Kelly, and T. H. Jones, “Testosterone and insulin resistance in the metabolic syndrome and T2DM in men,” Nature Reviews Endocrinology, vol. 9, no. 8, pp. 479–493, 2013. View at Publisher · View at Google Scholar · View at Scopus
  41. N. Burul-Bozkurt, C. Pekiner, and P. Kelicen, “Diabetes alters aromatase enzyme levels in gonadal tissues of rats,” Naunyn-Schmiedeberg's Archives of Pharmacology, vol. 382, no. 1, pp. 33–41, 2010. View at Publisher · View at Google Scholar · View at Scopus
  42. A. Prabhu, Q. Xu, M. B. Manigrasso et al., “Expression of aromatase, androgen and estrogen receptors in peripheral target tissues in diabetes,” Steroids, vol. 75, no. 11, pp. 779–787, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. C. Maric, C. Forsblom, L. Thorn, J. Wadén, and P.-H. Groop, “Association between testosterone, estradiol and sex hormone binding globulin levels in men with type 1 diabetes with nephropathy,” Steroids, vol. 75, no. 11, pp. 772–778, 2010. View at Publisher · View at Google Scholar · View at Scopus
  44. A. D. Martins, M. G. Alves, V. L. Simões et al., “Control of Sertoli cell metabolism by sex steroid hormones is mediated through modulation in glycolysis-related transporters and enzymes,” Cell and Tissue Research, vol. 354, no. 3, pp. 861–868, 2013. View at Publisher · View at Google Scholar · View at Scopus
  45. P. F. Oliveira, M. G. Alves, L. Rato et al., “Influence of 5α-dihydrotestosterone and 17β-estradiol on human Sertoli cells metabolism,” International Journal of Andrology, vol. 34, no. 6, pp. e612–e620, 2011. View at Publisher · View at Google Scholar · View at Scopus
  46. M. G. Alves, A. D. Martins, J. E. Cavaco, S. Socorro, and P. F. Oliveira, “Diabetes, insulin-mediated glucose metabolism and Sertoli/blood-testis barrier function,” Tissue Barriers, vol. 1, no. 2, Article ID e23992, 2013. View at Publisher · View at Google Scholar
  47. S. Amaral, A. J. Moreno, M. S. Santos, R. Seiça, and J. Ramalho-Santos, “Effects of hyperglycemia on sperm and testicular cells of Goto-Kakizaki and streptozotocin-treated rat models for diabetes,” Theriogenology, vol. 66, no. 9, pp. 2056–2067, 2006. View at Publisher · View at Google Scholar · View at Scopus
  48. F. M. Ferreira, C. M. Palmeira, R. Seiça, A. J. Moreno, and M. S. Santos, “Diabetes and mitochondrial bioenergetics: alterations with age,” Journal of Biochemical and Molecular Toxicology, vol. 17, no. 4, pp. 214–222, 2003. View at Publisher · View at Google Scholar · View at Scopus
  49. J. M. O'Donnell, R. K. Kudej, K. F. LaNoue, S. F. Vatner, and E. D. Lewandowski, “Limited transfer of cytosolic NADH into mitochondria at high cardiac workload,” The American Journal of Physiology: Heart and Circulatory Physiology, vol. 286, no. 6, pp. H2237–H2242, 2004. View at Publisher · View at Google Scholar · View at Scopus
  50. S. T. Kim and K. H. Moley, “Paternal effect on embryo quality in diabetic mice is related to poor sperm quality and associated with decreased glucose transporter expression,” Reproduction, vol. 136, no. 3, pp. 313–322, 2008. View at Publisher · View at Google Scholar · View at Scopus
  51. T. K. Sung and K. H. Moley, “The expression of GLUT8, GLUT9a, and GLUT9b in the mouse testis and sperm,” Reproductive Sciences, vol. 14, no. 5, pp. 445–455, 2007. View at Publisher · View at Google Scholar · View at Scopus
  52. T. R. Dias, M. G. Alves, B. M. Silva, and P. F. Oliveira, “Sperm glucose transport and metabolism in diabetic individuals,” Molecular and Cellular Endocrinology, vol. 396, no. 1, pp. 37–45, 2014. View at Google Scholar
  53. V. Douard and R. P. Ferraris, “Regulation of the fructose transporter GLUT5 in health and disease,” American Journal of Physiology—Endocrinology and Metabolism, vol. 295, no. 2, pp. E227–E237, 2008. View at Publisher · View at Google Scholar · View at Scopus
  54. C. Bouché, S. Serdy, C. R. Kahn, and A. B. Goldfine, “The cellular fate of glucose and its relevance in type 2 diabetes,” Endocrine Reviews, vol. 25, no. 5, pp. 807–830, 2004. View at Publisher · View at Google Scholar · View at Scopus
  55. C. Villar-Palasí and J. J. Guinovart, “The role of glucose 6-phosphate in the control of glycogen synthase,” The FASEB Journal, vol. 11, no. 7, pp. 544–558, 1997. View at Google Scholar · View at Scopus
  56. P. Dent, A. Lavoinne, S. Nakielny, F. B. Caudwell, P. Watt, and P. Cohen, “The molecular mechanism by which insulin stimulates glycogen synthesis in mammalian skeletal muscle,” Nature, vol. 348, no. 6299, pp. 302–308, 1990. View at Publisher · View at Google Scholar · View at Scopus
  57. R. Elkon, E. Zlotorynski, K. I. Zeller, and R. Agami, “Major role for mRNA stability in shaping the kinetics of gene induction,” BMC Genomics, vol. 11, no. 1, article 259, 2010. View at Publisher · View at Google Scholar · View at Scopus
  58. I. Das, “Studies on glycogen metabolism in normal and diabetic rat heart in vivo,” Canadian Journal of Biochemistry, vol. 51, no. 5, pp. 637–641, 1973. View at Google Scholar · View at Scopus
  59. V. Chen and C. D. Ianuzzo, “Dosage effects of streptozotocin on rat tissue enzyme activities and glycogen concentration,” Canadian Journal of Physiology and Pharmacology, vol. 60, no. 10, pp. 1251–1256, 1982. View at Publisher · View at Google Scholar · View at Scopus
  60. P. Puthanveetil, F. Wang, G. Kewalramani et al., “Cardiac glycogen accumulation after dexamethasone is regulated by AMPK,” The American Journal of Physiology—Heart and Circulatory Physiology, vol. 295, no. 4, pp. H1753–H1762, 2008. View at Publisher · View at Google Scholar · View at Scopus
  61. D. Qi, T. Pulinilkunnil, D. An et al., “Single-dose dexamethasone induces whole-body insulin resistance and alters both cardiac fatty acid and carbohydrate metabolism,” Diabetes, vol. 53, no. 7, pp. 1790–1797, 2004. View at Publisher · View at Google Scholar · View at Scopus
  62. A. Khaki, F. Fathiazad, M. Nouri, N. A. Maleki, H. J. Khamnei, and P. Ahmadi, “Beneficial effects of quercetin on sperm parameters in streptozotocin-induced diabetic male rats,” Phytotherapy Research, vol. 24, no. 9, pp. 1285–1291, 2010. View at Publisher · View at Google Scholar · View at Scopus
  63. D. Dinulovic and G. Radonjic, “Diabetes mellitus/male infertility,” Archives of Andrology, vol. 25, no. 3, pp. 277–293, 1990. View at Publisher · View at Google Scholar · View at Scopus