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BioMed Research International
Volume 2016 (2016), Article ID 9704607, 14 pages
http://dx.doi.org/10.1155/2016/9704607
Research Article

Animal Model of Gestational Diabetes Mellitus with Pathophysiological Resemblance to the Human Condition Induced by Multiple Factors (Nutritional, Pharmacological, and Stress) in Rats

1Department of Pharmacology and Chemistry, Faculty of Pharmacy, Universiti Teknologi MARA, 42300 Bandar Puncak Alam, Selangor Darul Ehsan, Malaysia
2Department of Physiology and Pharmacology, Faculty of Medicine, University of Calgary, 3330 Hospital Drive NW, Calgary, AB, Canada T2N 4N1
3Department of Pharmaceutical and Life Sciences, Faculty of Pharmacy, Universiti Teknologi MARA, 42300 Bandar Puncak Alam, Selangor Darul Ehsan, Malaysia
4Immunology Unit, Department of Pathology, Faculty of Medicine and Health Sciences, Universiti Putra Malaysia (UPM), 43400 Serdang, Selangor Darul Ehsan, Malaysia

Received 16 March 2016; Accepted 8 May 2016

Academic Editor: Monica Fedele

Copyright © 2016 Siti Hajar Abdul Aziz 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 Diabete Association, “2. Classification and Diagnosis of Diabetes,” Diabetes Care, vol. 38, supplement 1, pp. S8–S16, 2015. View at Publisher · View at Google Scholar
  2. L. A. Barbour, C. E. McCurdy, T. L. Hernandez, J. P. Kirwan, P. M. Catalano, and J. E. Friedman, “Cellular mechanisms for insulin resistance in normal pregnancy and gestational diabetes,” Diabetes Care, vol. 30, supplement 2, pp. S112–S119, 2007. View at Publisher · View at Google Scholar · View at Scopus
  3. T. A. Buchanan, A. H. Xiang, and K. A. Page, “Gestational diabetes mellitus: risks and management during and after pregnancy,” Nature Reviews Endocrinology, vol. 8, no. 11, pp. 639–649, 2012. View at Publisher · View at Google Scholar · View at Scopus
  4. C. Capula, E. Chiefari, A. Vero et al., “Gestational diabetes mellitus: screening and outcomes in southern Italian pregnant women,” ISRN Endocrinology, vol. 2013, Article ID 387495, 8 pages, 2013. View at Publisher · View at Google Scholar
  5. R. á Rogvi, J. L. Forman, P. Damm, and G. Greisen, “Women born preterm or with inappropriate weight for gestational age are at risk of subsequent gestational diabetes and pre-eclampsia,” PLoS ONE, vol. 7, no. 3, Article ID e34001, 2012. View at Publisher · View at Google Scholar · View at Scopus
  6. B. He, D. Piao, C. Yu, Y. Wang, and P. Han, “Amelioration in hepatic insulin sensitivity by reduced hepatic lipid accumulation at short-term after Roux-en-Y gastric bypass surgery in type 2 diabetic rats,” Obesity Surgery, vol. 23, no. 12, pp. 2033–2041, 2013. View at Publisher · View at Google Scholar · View at Scopus
  7. C. Kühl, P. J. Hornnes, and O. Andersen, “Review: etiology and pathophysiology of gestational diabetes mellitus,” Diabetes, vol. 34, no. 2, pp. 66–70, 1985. View at Publisher · View at Google Scholar · View at Scopus
  8. L. Bellamy, J.-P. Casas, A. D. Hingorani, and D. Williams, “Type 2 diabetes mellitus after gestational diabetes: a systematic review and meta-analysis,” The Lancet, vol. 373, no. 9677, pp. 1773–1779, 2009. View at Publisher · View at Google Scholar · View at Scopus
  9. B. E. Metzger, T. A. Buchanan, D. R. Coustan et al., “Summary and recommendations of the fifth international workshop-conference on gestational diabetes mellitus,” Diabetes Care, vol. 30, supplement 2, pp. S251–S260, 2007. View at Publisher · View at Google Scholar · View at Scopus
  10. M. Koulmanda, A. Qipo, S. Chebrolu, J. O'Neil, H. Auchincloss Jr., and R. N. Smith, “The effect of low versus high dose of streptozotocin in cynomolgus monkeys (Macaca fascilularis),” American Journal of Transplantation, vol. 3, no. 3, pp. 267–272, 2003. View at Publisher · View at Google Scholar · View at Scopus
  11. F. A. Van Assche, L. Aerts, and K. Holemans, “Metabolic alterations in adulthood after intrauterine development in mothers with mild diabetes,” Diabetes, vol. 40, supplement 2, pp. 106–108, 1991. View at Publisher · View at Google Scholar · View at Scopus
  12. E. Shafrir and G. Desoye, “Pregnancy in diabetic animals,” in Textbook of Diabetes and Pregnancy, M. Hod, L. Jovanovic, G. C. Di Renzo, A. Leiva, and O. Langer, Eds., pp. 96–97, Informa, London, UK, 2003. View at Google Scholar
  13. S. Caluwaerts, K. Holemans, R. Van Bree, J. Verhaeghe, and F. A. Van Assche, “Is low-dose streptozotocin in rats an adequate model for gestational diabetes mellitus?” Journal of the Society for Gynecologic Investigation, vol. 10, no. 4, pp. 216–221, 2003. View at Publisher · View at Google Scholar · View at Scopus
  14. K. Holemans, S. Caluwaerts, L. Poston, and F. A. Van Assche, “Diet-induced obesity in the rat: a model for gestational diabetes mellitus,” American Journal of Obstetrics and Gynecology, vol. 190, no. 3, pp. 858–865, 2004. View at Publisher · View at Google Scholar · View at Scopus
  15. I. López-Soldado and E. Herrera, “Different diabetogenic response to moderate doses of streptozotocin in pregnant rats, and its long-term consequences in the offspring,” Experimental Diabesity Research, vol. 4, no. 2, pp. 107–118, 2003. View at Publisher · View at Google Scholar · View at Scopus
  16. J. Yoshino, K. F. Mills, M. J. Yoon, and S.-I. Imai, “Nicotinamide mononucleotide, a key NAD+ intermediate, treats the pathophysiology of diet- and age-induced diabetes in mice,” Cell Metabolism, vol. 14, no. 4, pp. 528–536, 2011. View at Publisher · View at Google Scholar · View at Scopus
  17. P. Masiello, C. Broca, R. Gross et al., “Experimental NIDDM: development of a new model in adult rats administered streptozotocin and nicotinamide,” Diabetes, vol. 47, no. 2, pp. 224–229, 1998. View at Publisher · View at Google Scholar · View at Scopus
  18. L. H. Storlien, A. B. Jenkins, D. J. Chisholm, W. S. Pascoe, S. Khouri, and E. W. Kraegen, “Influence of dietary fat composition on development of insulin resistance in rats: relationship to muscle triglyceride and ω-3 fatty acids in muscle phospholipid,” Diabetes, vol. 40, no. 2, pp. 280–289, 1991. View at Publisher · View at Google Scholar · View at Scopus
  19. K. Srinivasan, P. S. Patole, C. L. Kaul, and P. Ramarao, “Reversal of glucose intolerance by pioglitazone in high fat diet-fed rats,” Methods and Findings in Experimental and Clinical Pharmacology, vol. 26, no. 5, pp. 327–333, 2004. View at Publisher · View at Google Scholar · View at Scopus
  20. Z.-H. Yang, H. Miyahara, J. Takeo, and M. Katayama, “Diet high in fat and sucrose induces rapid onset of obesity-related metabolic syndrome partly through rapid response of genes involved in lipogenesis, insulin signalling and inflammation in mice,” Diabetology and Metabolic Syndrome, vol. 4, article 32, 2012. View at Publisher · View at Google Scholar · View at Scopus
  21. C. L. Ogden, S. Z. Yanovski, M. D. Carroll, and K. M. Flegal, “The epidemiology of obesity,” Gastroenterology, vol. 132, no. 6, pp. 2087–2102, 2007. View at Publisher · View at Google Scholar · View at Scopus
  22. R. T. Hurt, C. Kulisek, L. A. Buchanan, and S. A. McClave, “The obesity epidemic: challenges, health initiatives, and implications for gastroenterologists,” Gastroenterology and Hepatology, vol. 6, no. 12, pp. 780–792, 2010. View at Google Scholar · View at Scopus
  23. L. S. Aucott, “Influences of weight loss on long-term diabetes outcomes,” Proceedings of the Nutrition Society, vol. 67, no. 1, pp. 54–59, 2008. View at Publisher · View at Google Scholar · View at Scopus
  24. E. S. Abdel-Reheim, A. A. Abd-Elmoneim, and A. A. Hosni, “Fatty-sucrosed diet/minimal dose of streptozotocin-treated rat: a novel model of gestational diabetes mellitus, metabolic and inflammatory insight,” Journal of Diabetes & Metabolism, vol. 5, p. 430, 2014. View at Publisher · View at Google Scholar
  25. K. Srinivasan, B. Viswanad, L. Asrat, C. L. Kaul, and P. Ramarao, “Combination of high-fat diet-fed and low-dose streptozotocin-treated rat: a model for type 2 diabetes and pharmacological screening,” Pharmacological Research, vol. 52, no. 4, pp. 313–320, 2005. View at Publisher · View at Google Scholar · View at Scopus
  26. C. M. John, R. Ramasamy, G. Al Naqeeb, A. H. Dhiab Al-Nuaimi, and A. Adam, “Enhanced CD4+CD25+ regulatory T cells with splenic proliferation and protection against oxidative stress by nicotinamide in gestational diabetes,” Current Medicinal Chemistry, In press.
  27. C. M. John, R. Ramasamy, G. Al Naqeeb, A. H. D. Al-Nuaimi, and A. Adam, “Nicotinamide supplementation protects gestational diabetic rats by reducing oxidative stress and enhancing immune responses,” Current Medicinal Chemistry, vol. 19, no. 30, pp. 5181–5186, 2012. View at Publisher · View at Google Scholar · View at Scopus
  28. A. Gumieniczek, H. Hopkała, Z. Wójtowicz, and J. Nikołajuk, “Changes in antioxidant status of heart muscle tissue in experimental diabetes in rabbits,” Acta Biochimica Polonica, vol. 49, no. 2, pp. 529–535, 2002. View at Google Scholar · View at Scopus
  29. Y. J. Suzuki, V. Jain, A.-M. Park, and R. M. Day, “Oxidative stress and oxidant signaling in obstructive sleep apnea and associated cardiovascular diseases,” Free Radical Biology and Medicine, vol. 40, no. 10, pp. 1683–1692, 2006. View at Publisher · View at Google Scholar · View at Scopus
  30. F. K. Marcondes, F. J. Bianchi, and A. P. Tanno, “Determination of the estrous cycle phases of rats: some helpful considerations,” Brazilian Journal of Biology, vol. 62, no. 4, pp. 609–614, 2002. View at Publisher · View at Google Scholar · View at Scopus
  31. R. Kopf, D. Lorenz, and E. Salewski, “Procedure for staining implantation sites of fresh rat uteri,” Naunyn-Schmiedebergs Archiv für experimentelle Pathologie und Pharmakologie, vol. 247, no. 2, pp. 121–135, 1964. View at Publisher · View at Google Scholar
  32. D. A. Benson, I. Karsch-Mizrachi, D. J. Lipman, J. Ostell, B. A. Rapp, and D. L. Wheeler, “GenBank,” Nucleic Acids Research, vol. 30, no. 1, pp. 17–20, 2002. View at Publisher · View at Google Scholar · View at Scopus
  33. I. M. B. Francischetti, E. Gordon, B. Bizzarro et al., “Tempol, an intracellular antioxidant, inhibits tissue factor expression, attenuates dendritic cell function, and is partially protective in a murine model of cerebral malaria,” PLoS ONE, vol. 9, no. 2, Article ID e87140, 2014. View at Publisher · View at Google Scholar · View at Scopus
  34. C. Liang, K. DeCourcy, and M. R. Prater, “High-saturated-fat diet induces gestational diabetes and placental vasculopathy in C57BL/6 mice,” Metabolism: Clinical and Experimental, vol. 59, no. 7, pp. 943–950, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. T. Szkudelski, “The mechanism of alloxan and streptozotocin action in B cells of the rat pancreas,” Physiological Research, vol. 50, no. 6, pp. 537–546, 2001. View at Google Scholar · View at Scopus
  36. M. Chatterjea and R. Shinde, Textbook of Medical Biochemistry, 2011.
  37. C. Homko, E. Sivan, X. Chen, E. A. Reece, and G. Boden, “Insulin secretion during and after pregnancy in patients with gestational diabetes mellitus,” The Journal of Clinical Endocrinology & Metabolism, vol. 86, no. 2, pp. 568–573, 2001. View at Publisher · View at Google Scholar · View at Scopus
  38. E. Herrera and H. Ortega-Senovilla, “Disturbances in lipid metabolism in diabetic pregnancy—are these the cause of the problem?” Best Practice and Research: Clinical Endocrinology and Metabolism, vol. 24, no. 4, pp. 515–525, 2010. View at Publisher · View at Google Scholar · View at Scopus
  39. J. Ghalami, H. Zardooz, F. Rostamkhani, B. Farrokhi, and M. Hedayati, “High-fat diet did not change metabolic response to acute stress in rats,” EXCLI Journal, vol. 10, pp. 205–217, 2011. View at Google Scholar · View at Scopus
  40. A. Dresner, D. Laurent, M. Marcucci et al., “Effects of free fatty acids on glucose transport and IRS-1-associated phosphatidylinositol 3-kinase activity,” The Journal of Clinical Investigation, vol. 103, no. 2, pp. 253–259, 1999. View at Publisher · View at Google Scholar · View at Scopus
  41. H. Bays, L. Mandarino, and R. A. Defronzo, “Role of the adipocyte, free fatty acids, and ectopic fat in pathogenesis of type 2 diabetes mellitus: peroxisomal proliferator-activated receptor agonists provide a rational therapeutic approach,” The Journal of Clinical Endocrinology & Metabolism, vol. 89, no. 2, pp. 463–478, 2004. View at Publisher · View at Google Scholar · View at Scopus
  42. E. M. Sternberg, G. P. Chrousos, R. L. Wilder, and P. W. Gold, “The stress response and the regulation of inflammatory disease,” Annals of Internal Medicine, vol. 117, no. 10, pp. 854–866, 1992. View at Publisher · View at Google Scholar
  43. M. Lappas, A. Mittion, and M. Permezel, “In response to oxidative stress, the expression of inflammatory cytokines and antioxidant enzymes are impaired in placenta, but not adipose tissue, of women with gestational diabetes,” Journal of Endocrinology, vol. 204, no. 1, pp. 75–84, 2010. View at Publisher · View at Google Scholar · View at Scopus
  44. L. Rui, V. Aguirre, J. K. Kim et al., “Insulin/IGF-1 and TNF-α stimulate phosphorylation of IRS-1 at inhibitory Ser307 via distinct pathways,” The Journal of Clinical Investigation, vol. 107, no. 2, pp. 181–189, 2001. View at Publisher · View at Google Scholar · View at Scopus
  45. J.-P. Bastard, M. Maachi, J. T. Van Nhieu et al., “Adipose tissue IL-6 content correlates with resistance to insulin activation of glucose uptake both in vivo and in vitro,” Journal of Clinical Endocrinology & Metabolism, vol. 87, no. 5, pp. 2084–2089, 2002. View at Publisher · View at Google Scholar · View at Scopus
  46. A. Dehghan, I. Kardys, M. P. M. De Maat et al., “Genetic variation, C-reactive protein levels, and incidence of diabetes,” Diabetes, vol. 56, no. 3, pp. 872–878, 2007. View at Publisher · View at Google Scholar · View at Scopus
  47. B. Vozarova, C. Weyer, K. Hanson, P. A. Tataranni, C. Bogardus, and R. E. Pratley, “Circulating interleukin-6 in relation to adiposity, insulin action, and insulin secretion,” Obesity Research, vol. 9, no. 7, pp. 414–417, 2001. View at Publisher · View at Google Scholar · View at Scopus
  48. P. A. Kern, S. Ranganathan, C. Li, L. Wood, and G. Ranganathan, “Adipose tissue tumor necrosis factor and interleukin-6 expression in human obesity and insulin resistance,” American Journal of Physiology—Endocrinology and Metabolism, vol. 280, no. 5, pp. E745–E751, 2001. View at Google Scholar · View at Scopus
  49. P. Bevan, “Insulin signalling,” Journal of Cell Science, vol. 114, no. 8, pp. 1429–1430, 2001. View at Google Scholar · View at Scopus
  50. A. D. Kohn, F. Takeuchi, and R. A. Roth, “Akt, a pleckstrin homology domain containing kinase, is activated primarily by phosphorylation,” The Journal of Biological Chemistry, vol. 271, no. 36, pp. 21920–21926, 1996. View at Publisher · View at Google Scholar · View at Scopus
  51. M. R. Calera, C. Martinez, H. Liu, A. K. El Jack, M. J. Birnbaum, and P. F. Pilch, “Insulin increases the association of Akt-2 with Glut4-containing vesicles,” The Journal of Biological Chemistry, vol. 273, no. 13, pp. 7201–7204, 1998. View at Publisher · View at Google Scholar · View at Scopus
  52. L.-N. Cong, H. Chen, Y. Li et al., “Physiological role of AKT in insulin-stimulated translocation of GLUT4 in transfected rat adipose cells,” Molecular Endocrinology, vol. 11, no. 13, pp. 1881–1890, 1997. View at Publisher · View at Google Scholar · View at Scopus
  53. C. Kim and A. Ferrara, Gestational Diabetes during and after Pregnancy, Springer, New York, NY, USA, 2010.
  54. T. Holyoak, S. M. Sullivan, and T. Nowak, “Structural insights into the mechanism of PEPCK catalysis,” Biochemistry, vol. 45, no. 27, pp. 8254–8263, 2006. View at Publisher · View at Google Scholar · View at Scopus
  55. A. Méndez-Lucas, J. A. G. Duarte, N. E. Sunny et al., “PEPCK-M expression in mouse liver potentiates, not replaces, PEPCK-C mediated gluconeogenesis,” Journal of Hepatology, vol. 59, no. 1, pp. 105–113, 2013. View at Publisher · View at Google Scholar · View at Scopus
  56. A. Ornoy, “Embryonic oxidative stress as a mechanism of teratogenesis with special emphasis on diabetic embryopathy,” Reproductive Toxicology, vol. 24, no. 1, pp. 31–41, 2007. View at Publisher · View at Google Scholar · View at Scopus
  57. M. Valko, C. J. Rhodes, J. Moncol, M. Izakovic, and M. Mazur, “Free radicals, metals and antioxidants in oxidative stress-induced cancer,” Chemico-Biological Interactions, vol. 160, no. 1, pp. 1–40, 2006. View at Publisher · View at Google Scholar · View at Scopus
  58. D. Vara and G. Pula, “Reactive oxygen species: physiological roles in the regulation of vascular cells,” Current Molecular Medicine, vol. 14, no. 9, pp. 1103–1125, 2014. View at Publisher · View at Google Scholar · View at Scopus
  59. U. Asmat, K. Abad, and K. Ismail, “Diabetes mellitus and oxidative stress—a concise review,” Saudi Pharmaceutical Journal, 2015. View at Publisher · View at Google Scholar · View at Scopus
  60. H. Zardooz, S. Z. Asl, and M. G. Naseri, “Effect of chronic psychological stress on insulin release from rat isolated pancreatic islets,” Life Sciences, vol. 79, no. 1, pp. 57–62, 2006. View at Publisher · View at Google Scholar · View at Scopus
  61. K. Sakai, K. Matsumoto, T. Nishikawa et al., “Mitochondrial reactive oxygen species reduce insulin secretion by pancreatic β-cells,” Biochemical and Biophysical Research Communications, vol. 300, no. 1, pp. 216–222, 2003. View at Publisher · View at Google Scholar · View at Scopus
  62. S. Lenzen, “The mechanisms of alloxan- and streptozotocin-induced diabetes,” Diabetologia, vol. 51, no. 2, pp. 216–226, 2008. View at Publisher · View at Google Scholar · View at Scopus
  63. L. I. Rachek, N. P. Thornley, V. I. Grishko, S. P. LeDoux, and G. L. Wilson, “Protection of INS-1 cells from free fatty acid-induced apoptosis by targeting hOGG1 to mitochondria,” Diabetes, vol. 55, no. 4, pp. 1022–1028, 2006. View at Publisher · View at Google Scholar · View at Scopus
  64. R. Schwartz, P. A. Gruppuso, K. Petzold, D. Brambilla, V. Hiilesmaa, and K. A. Teramo, “Hyperinsulinemia and macrosomia in the fetus of the diabetic mother,” Diabetes Care, vol. 17, no. 7, pp. 640–648, 1994. View at Publisher · View at Google Scholar · View at Scopus
  65. H. H. Günter, I. Tzialidou, A. Scharf, P. Wenzlaff, H. Maul, and P. Hillemanns, “Intrauterine fetal death in pregnancies of women with preconceptional and gestational diabetes mellitus and of women without glucose tolerance disorders. Results of the Perinatal Registry of Lower Saxony, Germany,” Zeitschrift fur Geburtshilfe und Neonatologie, vol. 210, no. 6, pp. 193–199, 2006. View at Publisher · View at Google Scholar · View at Scopus