Impact of diabetes in blood-testis and blood-brain barriers: Resemblances and differences

Current Diabetes Reviews

Volumn 8, Issue 6, 2012, Pages 401-412

  Alves, Marco G ^a   Oliveira, Pedro F ^a   Socorro, Sílvia ^a   Moreira, Paula I ^b,c  

^a UNIVERSITY OF BEIRA INTERIOR   (Portugal)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c UNIVERSITY OF COIMBRA   (Portugal)

Author keywords

Blood brain barrier; Blood testis barrier; Brain; Diabetes; Glucose metabolism; Insulin; Sertoli cells

Indexed keywords

GLUCOSE; GLUCOSE TRANSPORTER 1; GLUCOSE TRANSPORTER 3; INSULIN; INTERLEUKIN 1;

ARTICLE; BLOOD BRAIN BARRIER; BLOOD TESTIS BARRIER; DIABETES MELLITUS; ENDOTHELIUM CELL; ENERGY METABOLISM; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; GLYCEMIC CONTROL; HEMODYNAMICS; HUMAN; HYPERGLYCEMIA; HYPERINSULINEMIA; HYPOGLYCEMIA; INSULIN TREATMENT; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SERTOLI CELL; SPERMATOGENESIS;

ANIMALS; BIOLOGICAL TRANSPORT; BLOOD-BRAIN BARRIER; BLOOD-TESTIS BARRIER; DIABETES COMPLICATIONS; DIABETES MELLITUS, EXPERIMENTAL; GLUCOSE TRANSPORTER TYPE 1; GLUCOSE TRANSPORTER TYPE 3; HUMANS; INFERTILITY, MALE; MALE; METABOLIC SYNDROME X; RATS; SEMINIFEROUS EPITHELIUM; TIGHT JUNCTIONS;

EID: 84870183874     PISSN: 15733998     EISSN: 18756417     Source Type: Journal    
DOI: 10.2174/157339912803529896     Document Type: Article

References (181)

1. Saunders NR, Habgood MD, Dziegielewska KM. Barrier mechanisms in the brain, I. Adult brain. Clin Exp Pharmacol Physiol 1999; 26: 11-9.
2. Spranger J, Verma S, Gohring I, et al. Adiponectin does not cross the blood-brain barrier but modifies cytokine expression of brain endothelial cells. Diabetes 2006; 55: 141-7.
3. Cardozo-Pelaez F, Brooks PJ, Stedeford T, Song S, Sanchez-Ramos J. DNA damage, repair, and antioxidant systems in brain regions: a correlative study. Free Radic Biol Med 2000; 28: 779-85.
4. Lovell MA, Markesbery WR. Oxidative DNA damage in mild cognitive impairment and late-stage Alzheimer's disease. Nucleic Acids Res 2007; 35: 7497-504.
5. Osawa A, Maeshima S, Shimamoto Y, et al. Relationship between cognitive function and regional cerebral blood flow in different types of dementia. Disabil Rehabil 2004; 26: 739-45.
6. Setchell BP, Scott TW, Voglmayr JK, Waites GM. Characteristics of testicular spermatozoa and the fluid which transports them into the epididymis. Biology of Reproduction 1969; 1: Suppl 1:40-66.
7. Meinhardt A, Hedger MP. Immunological, paracrine and endocrine aspects of testicular immune privilege. Mol Cell Endocrinol 2011; 335: 60-8.
8. Persidsky Y, Ramirez SH, Haorah J, Kanmogne GD. Blood-brain barrier: structural components and function under physiologic and pathologic conditions. J Neuroimmune Pharmacol 2006; 1: 223-36.
9. Belanger M, Allaman I, Magistretti PJ. Brain energy metabolism: focus on astrocyte-neuron metabolic cooperation. Cell Metab 2011; 14: 724-38.
10. Ritter AM, Robertson CS. Cerebral metabolism. Neurosurg Clin N Am 1994; 5: 633-45.
11. Leybaert L. Neurobarrier coupling in the brain: a partner of neurovascular and neurometabolic coupling? J Cereb Blood Flow Metab 2005; 25: 2-16.
12. Routh VH. Glucose-sensing neurons: are they physiologically relevant? Physiol Behav 2002; 76: 403-13.
13. McCall AL. Cerebral glucose metabolism in diabetes mellitus. Eur J Pharmacol 2004; 490: 147-58.
14. Cardoso S, Santos MS, Seica R, Moreira PI. Cortical and hippocampal mitochondria bioenergetics and oxidative status during hyperglycemia and/or insulin-induced hypoglycemia. Biochim Biophys Acta 2010; 1802: 942-51.
15. Cardoso S, Carvalho C, Santos R, et al. Impact of STZ-induced hyperglycemia and insulin-induced hypoglycemia in plasma amino acids and cortical synaptosomal neurotransmitters. Synapse 2011; 65: 457-66.
16. Sharpe RM, McKinnell C, Kivlin C, Fisher JS. Proliferation and functional maturation of Sertoli cells, and their relevance to disorders of testis function in adulthood. Reproduction 2003; 125: 769-84.
17. Walker WH, Cheng J. FSH and testosterone signaling in Sertoli cells. Reproduction 2005; 130: 15-28.
18. Oliveira PF, Sousa M, Barros A, Moura T, Rebelo da Costa A. Intracellular pH regulation in human Sertoli cells: role of membrane transporters. Reproduction 2009; 137: 353-9.
19. Oliveira PF, Sousa M, Barros A, Moura T, Rebelo da Costa A. Membrane transporters and cytoplasmatic pH regulation on bovine Sertoli cells. Journal of Membrane Biology 2009; 227: 49-55.
20. Rato L, Socorro S, Cavaco JE, Oliveira PF. Tubular fluid secretion in the seminiferous epithelium: ion transporters and aquaporins in Sertoli cells. Journal of Membrane Biology 2010; 236: 215-24.
21. Mita M, Hall PF. Metabolism of round spermatids from rats: lactate as the preferred substrate. Biology of Reproduction 1982; 26: 445-55.
22. Pellerin L, Bonvento G, Chatton JY, Pierre K, Magistretti PJ. Role of neuron-glia interaction in the regulation of brain glucose utilization. Diabetes Nutr Metab 2002; 15: 268-73.
23. Jutte NH, Jansen R, Grootegoed JA, Rommerts FF, Clausen OP, van der Molen HJ. Regulation of survival of rat pachytene spermatocytes by lactate supply from Sertoli cells. J Reprod Fertil 1982; 65: 431-8.
24. Klip A, Tsakiridis T, Marette A, Ortiz PA. Regulation of expression of glucose transporters by glucose: a review of studies in vivo and in cell cultures. FASEB J 1994; 8: 43-53.
25. Dick AP, Harik SI. Distribution of the glucose transporter in the mammalian brain. J Neurochem 1986; 46: 1406-11.
26. Dick AP, Harik SI, Klip A, Walker DM. Identification and characterization of the glucose transporter of the blood-brain barrier by cytochalasin B binding and immunological reactivity. Proc Natl Acad Sci U S A 1984; 81: 7233-7.
27. Carosa E, Radico C, Giansante N, et al. Ontogenetic profile and thyroid hormone regulation of type-1 and type-8 glucose transporters in rat Sertoli cells. Int J Androl 2005; 28: 99-106.
28. Galardo MN, Riera MF, Pellizzari EH, et al. Regulation of expression of Sertoli cell glucose transporters 1 and 3 by FSH, IL1 beta, and bFGF at two different time-points in pubertal development. Cell and Tissue Research 2008; 334: 295-304.
29. Lam TK, Gutierrez-Juarez R, Pocai A, Rossetti L. Regulation of blood glucose by hypothalamic pyruvate metabolism. Science 2005; 309: 943-7.
30. Gjedde A, Crone C. Blood-brain glucose transfer: repression in chronic hyperglycemia. Science 1981; 214: 456-7.
31. Hall PF, Mita M. Influence of follicle-stimulating hormone on glucose transport by cultured Sertoli cells. Biol Reprod 1984; 31: 863-9.
32. Riera MF, Galardo MN, Pellizzari EH, Meroni SB, Cigorraga SB. Molecular mechanisms involved in Sertoli cell adaptation to glucose deprivation. Am J Physiol Endocrinol Metab 2009; 297: E907-14.
33. Alves MG, Rato L, Carvalho RA, et al. Hormonal control of Sertoli cells metabolism regulates spermatogenesis. Cell Mol Life Sci 2012 DOI: 10.1007/s00018-012-1079-1.
34. Moreira PI, Oliveira CR. Mitochondria as potential targets in antidiabetic therapy. Handb Exp Pharmacol 2011: 331-56.
35. Sage JI, Van Uitert RL, Duffy TE. Early changes in blood brain barrier permeability to small molecules after transient cerebral ischemia. Stroke 1984; 15: 46-50.
36. Mueller SM, Luft FC. The blood-brain barrier in renovascular hypertension. Stroke 1982; 13: 229-34.
37. Arieff AI, Kleeman CR. Studies on mechanisms of cerebral edema in diabetic comas. Effects of hyperglycemia and rapid lowering of plasma glucose in normal rabbits. J Clin Invest 1973; 52: 571-83.
38. Gradman TJ, Laws A, Thompson LW, Reaven GM. Verbal learning and/or memory improves with glycemic control in older subjects with non-insulin-dependent diabetes mellitus. J Am Geriatr Soc 1993; 41: 1305-12.
39. Meneilly GS, Cheung E, Tessier D, Yakura C, Tuokko H. The effect of improved glycemic control on cognitive functions in the elderly patient with diabetes. J Gerontol 1993; 48: M117-21.
40. Stumvoll M, Goldstein BJ, van Haeften TW. Type 2 diabetes: principles of pathogenesis and therapy. Lancet 2005; 365: 1333-46.
41. Starr J, Wardlaw J, Ferguson K, MacLullich A, Deary I, Marshall I. Increased blood-brain barrier permeability in type II diabetes demonstrated by gadolinium magnetic resonance imaging. Journal of Neurology, Neurosurgery & Psychiatry 2003; 74: 70-6.
42. Vannucci SJ, Gibbs EM, Simpson IA. Glucose utilization and glucose transporter proteins GLUT-1 and GLUT-3 in brains of diabetic (db/db) mice. Am J Physiol 1997; 272: E267-74.
43. Pardridge WM, Triguero D, Farrell CR. Downregulation of bloodbrain barrier glucose transporter in experimental diabetes. Diabetes 1990; 39: 1040-4.
44. Pennathur S, Heinecke JW. Oxidative stress and endothelial dysfunction in vascular disease. Curr Diab Rep 2007; 7: 257-64.
45. Schrauwen-Hinderling VB, Roden M, Kooi ME, Hesselink MK, Schrauwen P. Muscular mitochondrial dysfunction and type 2 diabetes mellitus. Curr Opin Clin Nutr Metab Care 2007; 10: 698-703.
46. McCall AL, Fixman LB, Fleming N, Tornheim K, Chick W, Ruderman NB. Chronic hypoglycemia increases brain glucose transport. Am J Physiol 1986; 251: E442-7.
47. Pelligrino DA, Segil LJ, Albrecht RF. Brain glucose utilization and transport and cortical function in chronic vs. acute hypoglycemia. Am J Physiol 1990; 259: E729-35.
48. Kumagai AK, Kang YS, Boado RJ, Pardridge WM. Upregulation of blood-brain barrier GLUT1 glucose transporter protein and mRNA in experimental chronic hypoglycemia. Diabetes 1995; 44: 1399-404.
49. Russo VC, Kobayashi K, Najdovska S, Baker NL, Werther GA. Neuronal protection from glucose deprivation via modulation of glucose transport and inhibition of apoptosis: a role for the insulinlike growth factor system. Brain Res 2004; 1009: 40-53.
50. Simpson IA, Appel NM, Hokari M, et al. Blood-brain barrier glucose transporter: effects of hypo-and hyperglycemia revisited. J Neurochem 1999; 72: 238-47.
51. Lorenzi M, Healy DP, Hawkins R, Printz JM, Printz MP. Studies on the permeability of the blood-brain barrier in experimental diabetes. Diabetologia 1986; 29: 58-62.
52. Dai J, Vrensen GF, Schlingemann RO. Blood-brain barrier integrity is unaltered in human brain cortex with diabetes mellitus. Brain Res 2002; 954: 311-6.
53. Starr JM, Wardlaw J, Ferguson K, MacLullich A, Deary IJ, Marshall I. Increased blood-brain barrier permeability in type II diabetes demonstrated by gadolinium magnetic resonance imaging. J Neurol Neurosurg Psychiatry 2003; 74: 70-6.
54. Ciudin A, Hernandez C, Simo R. Non-invasive methods of glucose measurement: current status and future perspectives. Curr Diabetes Rev 2012; 8: 48-54.
55. Fouyas IP, Kelly PA, Ritchie IM, Lammie GA, Whittle IR. Cerebrovascular responses to pathophysiological insult in diabetic rats. J Clin Neurosci 2003; 10: 88-91.
56. Kusuhara H, Sugiyama Y. Efflux transport systems for drugs at the blood-brain barrier and blood-cerebrospinal fluid barrier (Part 1). Drug Discov Today 2001; 6: 150-6.
57. Liu H, Xu X, Yang Z, Deng Y, Liu X, Xie L. Impaired function and expression of P-glycoprotein in blood-brain barrier of streptozotocin-induced diabetic rats. Brain Res 2006; 1123: 245-52.
58. Kamei J, Hirano S, Miyata S, Saitoh A, Onodera K. Effects of firstand second-generation histamine-H1-receptor antagonists on the pentobarbital-induced loss of the righting reflex in streptozotocininduced diabetic mice. J Pharmacol Sci 2005; 97: 266-72.
59. Pinhas-Hamiel O, Zeitler P. The global spread of type 2 diabetes mellitus in children and adolescents. J Pediatr 2005; 146: 693-700.
60. Murray FT, Cameron DF, Orth JM. Gonadal dysfunction in the spontaneously diabetic BB rat. Metabolism 1983; 32: 141-7.
61. Agbaje IM, Rogers DA, McVicar CM, et al. Insulin dependant diabetes mellitus: implications for male reproductive function. Hum Reprod 2007; 22: 1871-7.
62. Gazzaruso C, Coppola A, Giustina A. Erectile dysfunction and coronary artery disease in patients with diabetes. Curr Diabetes Rev 2011; 7: 143-7.
63. Kuhn-Velten N, Schermer R, Staib W. Effect of streptozotocininduced hyperglycaemia on androgen-binding protein in rat testis and epididymis. Diabetologia 1984; 26: 300-3.
64. Seethalakshmi L, Menon M, Diamond D. The effect of streptozotocin-induced diabetes on the neuroendocrine-male reproductive tract axis of the adult rat. J Urol 1987; 138: 190-4.
65. Scarano WR, Messias AG, Oliva SU, Klinefelter GR, Kempinas WG. Sexual behaviour, sperm quantity and quality after short-term streptozotocin-induced hyperglycaemia in rats. Int J Androl 2006; 29: 482-8.
66. Ricci G, Catizone A, Esposito R, Pisanti FA, Vietri MT, Galdieri M. Diabetic rat testes: morphological and functional alterations. Andrologia 2009; 41: 361-8.
67. Cameron DF, Murray FT, Drylie DD. Interstitial compartment pathology and spermatogenic disruption in testes from impotent diabetic men. Anat Rec 1985; 213: 53-62.
68. Sexton WJ, Jarow JP. Effect of diabetes mellitus upon male reproductive function. Urology 1997; 49: 508-13.
69. Ulisse S, Jannini EA, Pepe M, De Matteis S, D'Armiento M. Thyroid hormone stimulates glucose transport and GLUT1 mRNA in rat Sertoli cells. Molecular and Cellular Endocrinology 1992; 87: 131-7.
70. Piroli GG, Grillo CA, Hoskin EK, et al. Peripheral glucose administration stimulates the translocation of GLUT8 glucose transporter to the endoplasmic reticulum in the rat hippocampus. Journal of Comparative Neurology 2002; 452: 103-14.
71. Reagan LP, Gorovits N, Hoskin EK, et al. Localization and regulation of GLUTx1 glucose transporter in the hippocampus of streptozotocin diabetic rats. Proc Natl Acad Sci U S A 2001; 98: 2820-5.
72. Gomez O, Romero A, Terrado J, Mesonero JE. Differential expression of glucose transporter GLUT8 during mouse spermatogenesis. Reproduction 2006; 131: 63-70.
73. Schurmann A, Axer H, Scheepers A, Doege H, Joost HG. The glucose transport facilitator GLUT8 is predominantly associated with the acrosomal region of mature spermatozoa. Cell Tissue Res 2002; 307: 237-42.
74. Carayannopoulos MO, Chi MM, Cui Y, et al. GLUT8 is a glucose transporter responsible for insulin-stimulated glucose uptake in the blastocyst. Proc Natl Acad Sci U S A 2000; 97: 7313-8.
75. Adastra KL, Frolova AI, Chi MM, et al. Slc2a8 Deficiency in Mice Results in Reproductive and Growth Impairments. Biol Reprod 2012; 87: 1-11.
76. Robinson R, Fritz IB. Metabolism of glucose by Sertoli cells in culture. Biology of Reproduction 1981; 24: 1032-41.
77. Jutte NH, Grootegoed JA, Rommerts FF, van der Molen HJ. Exogenous lactate is essential for metabolic activities in isolated rat spermatocytes and spermatids. J Reprod Fertil 1981; 62: 399-405.
78. Rato L, Alves MG, Socorro S, Carvalho RA, Cavaco JE, Oliveira PF. Metabolic modulation induced by oestradiol and DHT in immature rat Sertoli cells cultured in vitro. Biosci Rep 2012; 32: 61-9.
79. Oliveira PF, Alves MG, Rato L, et al. Influence of 5a-dihydrotestosterone and 17b-estradiol on human Sertoli cells metabolism. Int J Androl 2011; 34: e612-e20.
80. Nakamura M, Okinaga S, Arai K. Metabolism of round spermatids: evidence that lactate is preferred substrate. Am J Physiol 1984; 247: E234-42.
81. Oliveira PF, Alves MG, Rato L, et al. Effect of insulin deprivation on metabolism and metabolism-associated gene transcript levels of in vitro cultured human Sertoli cells. Biochim Biophys Acta 2012; 1820: 84-9.
82. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. The Diabetes Control and Complications Trial Research Group. N Engl J Med 1993; 329: 977-86.
83. Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33). UK Prospective Diabetes Study (UKPDS) Group. Lancet 1998; 352: 837-53.
84. Cryer PE. The barrier of hypoglycemia in diabetes. Diabetes 2008; 57: 3169-76.
85. Cryer PE. Hypoglycemia: still the limiting factor in the glycemic management of diabetes. Endocr Pract 2008; 14: 750-6.
86. Risk of hypoglycaemia in types 1 and 2 diabetes: effects of treatment modalities and their duration. Diabetologia 2007; 50: 1140-7.
87. Dagogo-Jack SE, Craft S, Cryer PE. Hypoglycemia-associated autonomic failure in insulin-dependent diabetes mellitus. Recent antecedent hypoglycemia reduces autonomic responses to, symptoms of, and defense against subsequent hypoglycemia. J Clin Invest 1993; 91: 819-28.
88. Segel SA, Paramore DS, Cryer PE. Hypoglycemia-associated autonomic failure in advanced type 2 diabetes. Diabetes 2002; 51: 724-33.
89. El-Kaissi S, Sherbeeni S. Pharmacological management of type 2 diabetes mellitus: an update. Curr Diabetes Rev 2011; 7: 392-405.
90. Simonson DC, Tamborlane WV, DeFronzo RA, Sherwin RS. Intensive insulin therapy reduces counterregulatory hormone responses to hypoglycemia in patients with type I diabetes. Ann Intern Med 1985; 103: 184-90.
91. Amiel SA, Sherwin RS, Simonson DC, Tamborlane WV. Effect of intensive insulin therapy on glycemic thresholds for counterregulatory hormone release. Diabetes 1988; 37: 901-7.
92. Huber JD, VanGilder RL, Houser KA. Streptozotocin-induced diabetes progressively increases blood-brain barrier permeability in specific brain regions in rats. Am J Physiol Heart Circ Physiol 2006; 291: H2660-8.
93. Moreira PI, Rolo AP, Sena C, Seica R, Oliveira CR, Santos MS. Insulin attenuates diabetes-related mitochondrial alterations: a comparative study. Med Chem 2006; 2: 299-308.
94. Sherwin RS. Bringing light to the dark side of insulin: a journey across the blood-brain barrier. Diabetes 2008; 57: 2259-68.
95. Boyle PJ, Kempers SF, O'Connor AM, Nagy RJ. Brain glucose uptake and unawareness of hypoglycemia in patients with insulindependent diabetes mellitus. N Engl J Med 1995; 333: 1726-31.
96. Boyle PJ, Nagy RJ, O'Connor AM, Kempers SF, Yeo RA, Qualls C. Adaptation in brain glucose uptake following recurrent hypoglycemia. Proc Natl Acad Sci U S A 1994; 91: 9352-6.
97. Hasselbalch SG, Knudsen GM, Capaldo B, Postiglione A, Paulson OB. Blood-brain barrier transport and brain metabolism of glucose during acute hyperglycemia in humans. J Clin Endocrinol Metab 2001; 86: 1986-90.
98. Blomqvist G, Gjedde A, Gutniak M, et al. Facilitated transport of glucose from blood to brain in man and the effect of moderate hypoglycaemia on cerebral glucose utilization. Eur J Nucl Med 1991; 18: 834-7.
99. Hasselbalch SG, Knudsen GM, Videbaek C, et al. No effect of insulin on glucose blood-brain barrier transport and cerebral metabolism in humans. Diabetes 1999; 48: 1915-21.
100. Knudsen GM, Hasselbalch SG, Hertz MM, Paulson OB. High dose insulin does not increase glucose transfer across the blood-brain barrier in humans: a re-evaluation. Eur J Clin Invest 1999; 29: 687-91.
101. Kar S, Chabot JG, Quirion R. Quantitative autoradiographic localization of [125I]insulin-like growth factor I, [125I]insulin-like growth factor II, and [125I]insulin receptor binding sites in developing and adult rat brain. J Comp Neurol 1993; 333: 375-97.
102. Duarte AI, Moreira PI, Oliveira CR. Insulin in central nervous system: more than just a peripheral hormone. J Aging Res 2012; 2012: 384017: 1-21.
103. Kondo T, Hafezi-Moghadam A, Thomas K, Wagner DD, Kahn CR. Mice lacking insulin or insulin-like growth factor 1 receptors in vascular endothelial cells maintain normal blood-brain barrier. Biochem Biophys Res Commun 2004; 317: 315-20.
104. McCall AL, Gould JB, Ruderman NB. Diabetes-induced alterations of glucose metabolism in rat cerebral microvessels. Am J Physiol 1984; 247: E462-7.
105. Mooradian AD, Morin AM. Brain uptake of glucose in diabetes mellitus: the role of glucose transporters. Am J Med Sci 1991; 301: 173-7.
106. McCall AL, Millington WR, Wurtman RJ. Metabolic fuel and amino acid transport into the brain in experimental diabetes mellitus. Proc Natl Acad Sci U S A 1982; 79: 5406-10.
107. Hutson JC. Altered biochemical responses by rat Sertoli cells and peritubular cells cultured under simulated diabetic conditions. Diabetologia 1984; 26: 155-8.
108. Oonk RB, Grootegoed JA, van der Molen HJ. Comparison of the effects of insulin and follitropin on glucose metabolism by Sertoli cells from immature rats. Molecular and Cellular Endocrinology 1985; 42: 39-48.
109. Oonk RB, Grootegoed JA. Identification of insulin receptors on rat Sertoli cells. Molecular and Cellular Endocrinology 1987; 49: 51-62.
110. Mason GF, Petersen KF, Lebon V, Rothman DL, Shulman GI. Increased brain monocarboxylic acid transport and utilization in type 1 diabetes. Diabetes 2006; 55: 929-34.
111. Ebert D, Haller RG, Walton ME. Energy contribution of octanoate to intact rat brain metabolism measured by 13C nuclear magnetic resonance spectroscopy. J Neurosci 2003; 23: 5928-35.
112. Ruderman NB, Ross PS, Berger M, Goodman MN. Regulation of glucose and ketone-body metabolism in brain of anaesthetized rats. Biochem J 1974; 138: 1-10.
113. Deelchand DK, Shestov AA, Koski DM, Ugurbil K, Henry PG. Acetate transport and utilization in the rat brain. J Neurochem 2009; 109 Suppl 1: 46-54.
114. Cremer JE, Heath DF. The estimation of rates of utilization of glucose and ketone bodies in the brain of the suckling rat using compartmental analysis of isotopic data. Biochem J 1974; 142: 527-44.
115. Owen OE, Morgan AP, Kemp HG, Sullivan JM, Herrera MG, Cahill GF, Jr. Brain metabolism during fasting. J Clin Invest 1967; 46: 1589-95.
116. Mooradian AD. Blood-brain barrier choline transport is reduced in diabetic rats. Diabetes 1987; 36: 1094-7.
117. Mooradian AD. Effect of ascorbate and dehydroascorbate on tissue uptake of glucose. Diabetes 1987; 36: 1001-4.
118. Mooradian AD, Smith TL. The effect of experimentally induced diabetes mellitus on the lipid order and composition of rat cerebral microvessels. Neurosci Lett 1992; 145: 145-8.
119. Mayhan WG, Didion SP. Glutamate-induced disruption of the blood-brain barrier in rats. Role of nitric oxide. Stroke 1996; 27: 965-9.
120. Hawkins RA, Peterson DR, Vina JR. The complementary membranes forming the blood-brain barrier. IUBMB Life 2002; 54: 101-7.
121. Hawkins RA, O'Kane RL, Simpson IA, Vina JR. Structure of the blood-brain barrier and its role in the transport of amino acids. J Nutr 2006; 136: 218S-26S.
122. Castell LM, Yamamoto T, Phoenix J, Newsholme EA. The role of tryptophan in fatigue in different conditions of stress. Adv Exp Med Biol 1999; 467: 697-704.
123. Fernstrom JD. Branched-chain amino acids and brain function. J Nutr 2005; 135: 1539S-46S.
124. Gregg EW, Yaffe K, Cauley JA, et al. Is diabetes associated with cognitive impairment and cognitive decline among older women? Study of Osteoporotic Fractures Research Group. Arch Intern Med 2000; 160: 174-80.
125. Siesjo BK. Hypoglycemia, brain metabolism, and brain damage. Diabetes Metab Rev 1988; 4: 113-44.
126. Dienel GA, Cruz NF. Neighborly interactions of metabolicallyactivated astrocytes in vivo. Neurochem Int 2003; 43: 339-54.
127. Dienel GA, Wang RY, Cruz NF. Generalized sensory stimulation of conscious rats increases labeling of oxidative pathways of glucose metabolism when the brain glucose-oxygen uptake ratio rises. J Cereb Blood Flow Metab 2002; 22: 1490-502.
128. Choi IY, Tkac I, Ugurbil K, Gruetter R. Noninvasive measurements of [1-(13)C]glycogen concentrations and metabolism in rat brain in vivo. J Neurochem 1999; 73: 1300-8.
129. Choi IY, Gruetter R. In vivo 13C NMR assessment of brain glycogen concentration and turnover in the awake rat. Neurochem Int 2003; 43: 317-22.
130. Gruetter R. Glycogen: the forgotten cerebral energy store. J Neurosci Res 2003; 74: 179-83.
131. Seaquist ER, Gruetter R. Brain glycogen: an insulin-sensitive carbohydrate store. Diabetes Nutr Metab 2002; 15: 285-90.
132. Sickmann HM, Waagepetersen HS, Schousboe A, Benie AJ, Bouman SD. Brain glycogen and its role in supporting glutamate and GABA homeostasis in a type 2 diabetes rat model. Neurochem Int 2012; 60: 267-75.
133. Plaschke K, Hoyer S. Action of the diabetogenic drug streptozotocin on glycolytic and glycogenolytic metabolism in adult rat brain cortex and hippocampus. Int J Dev Neurosci 1993; 11: 477-83.
134. Rato L, Alves MG, Socorro S, Duarte AI, Cavaco JE, Oliveira PF. Metabolic regulation is important for spermatogenesis. Nat Rev Urol 2012; 9: 330-8.
135. Mancine RE, Penhos JC, Izquierdo IA, Heinrich JJ. Effects of acute hypoglycemia on rat testis. Proceedings of the Society for Experimental Biology and Medicine 1960; 104: 699-702.
136. Zysk JR, Bushway AA, Whistler RL, Carlton WW. Temporary sterility produced in male mice by 5-thio-D-glucose. J Reprod Fertil 1975; 45: 69-72.
137. Xiong W, Wang H, Wu H, Chen Y, Han D. Apoptotic spermatogenic cells can be energy sources for Sertoli cells. Reproduction 2009; 137: 469-79.
138. Chung S, Wang SP, Pan L, Mitchell G, Trasler J, Hermo L. Infertility and testicular defects in hormone-sensitive lipasedeficient mice. Endocrinology 2001; 142: 4272-81.
139. Jutte NH, Eikvar L, Levy FO, Hansson V. Metabolism of palmitate in cultured rat Sertoli cells. J Reprod Fertil 1985; 73: 497-503.
140. Yount EA, Harris RA. Ketone body and acetate formation from oleate by isolated rat testicular cells. Arch Biochem Biophys 1982; 217: 503-11.
141. Kaiser GR, Monteiro SC, Gelain DP, Souza LF, Perry ML, Bernard EA. Metabolism of amino acids by cultured rat Sertoli cells. Metabolism 2005; 54: 515-21.
142. Leiderman B, Mancini RE. Glycogen content in the rat testis from postnatal to adult ages. Endocrinology 1969; 85: 607-9.
143. Slaughter GR, Means AR. Follicle-stimulating hormone activation of glycogen phosphorylase in the Sertoli cell-enriched rat testis. Endocrinology 1983; 113: 1476-85.
144. Alves MG, Socorro S, Silva J, et al. In vitro cultured human Sertoli cells secrete high amounts of acetate that is stimulated by 17betaestradiol and suppressed by insulin deprivation. Biochim Biophys Acta 2012; 1823: 1389-94.
145. Desjardins M, Bendayan M. Ultrastructural distribution of glomerular basement membrane components in experimental diabetes. Diabetes Res 1990; 14: 65-73.
146. Hirose K, Osterby R, Nozawa M, Gundersen HJ. Development of glomerular lesions in experimental long-term diabetes in the rat. Kidney Int 1982; 21: 689-95.
147. Ditzel J, Junker K. Abnormal glomerular filtration rate, renal plasma flow, and renal protein excretion in recent and short-term diabetics. Br Med J 1972; 2: 13-9.
148. Fawcett DW, Leak LV, Heidger PM, Jr. Electron microscopic observations on the structural components of the blood-testis barrier. J Reprod Fertil Suppl 1970; 10: 105-22.
149. Holash JA, Harik SI, Perry G, Stewart PA. Barrier properties of testis microvessels. Proc Natl Acad Sci U S A 1993; 90: 11069-73.
150. Bustamante JC, Setchell BP. The uptake of amino acids, in particular leucine, by isolated perfused testes of rats. J Androl 2000; 21: 452-63.
151. Ghabriel MN, Lu JJ, Hermanis G, Zhu C, Setchell BP. Expression of a blood-brain barrier-specific antigen in the reproductive tract of the male rat. Reproduction 2002; 123: 389-97.
152. Risau W. Induction of blood-brain barrier endothelial cell differentiation. Ann N Y Acad Sci 1991; 633: 405-19.
153. Stewart PA. Endothelial vesicles in the blood-brain barrier: are they related to permeability? Cell Mol Neurobiol 2000; 20: 149-63.
154. Weihe E, Nimmrich H, Metz J, Forssmann WG. Horseradish peroxidase as a tracer for capillary permeability studies. J Histochem Cytochem 1979; 27: 1357-9.
155. Brightman MW, Reese TS. Junctions between intimately apposed cell membranes in the vertebrate brain. J Cell Biol 1969; 40: 648-77.
156. Liu H, Liu X, Jia L, et al. Insulin therapy restores impaired function and expression of P-glycoprotein in blood-brain barrier of experimental diabetes. Biochem Pharmacol 2008; 75: 1649-58.
157. Hawkins BT, Lundeen TF, Norwood KM, Brooks HL, Egleton RD. Increased blood-brain barrier permeability and altered tight junctions in experimental diabetes in the rat: contribution of hyperglycaemia and matrix metalloproteinases. Diabetologia 2007; 50: 202-11.
158. Bakker W, Eringa EC, Sipkema P, van Hinsbergh VW. Endothelial dysfunction and diabetes: roles of hyperglycemia, impaired insulin signaling and obesity. Cell Tissue Res 2009; 335: 165-89.
159. Huber JD. Diabetes, cognitive function, and the blood-brain barrier. Curr Pharm Des 2008; 14: 1594-600.
160. Li Q, Liu H, Du J, et al. Advanced glycation end products induce moesin phosphorylation in murine brain endothelium. Brain Res 2011; 1373: 1-10.
161. Mallidis C, Agbaje I, Rogers D, et al. Distribution of the receptor for advanced glycation end products in the human male reproductive tract: prevalence in men with diabetes mellitus. Hum Reprod 2007; 22: 2169-77.
162. Mallidis C, Agbaje IM, Rogers DA, et al. Advanced glycation end products accumulate in the reproductive tract of men with diabetes. Int J Androl 2009; 32: 295-305.
163. Donath MY, Storling J, Berchtold LA, Billestrup N, Mandrup-Poulsen T. Cytokines and beta-cell biology: from concept to clinical translation. Endocr Rev 2008; 29: 334-50.
164. Garcia MC, Wernstedt I, Berndtsson A, et al. Mature-onset obesity in interleukin-1 receptor I knockout mice. Diabetes 2006; 55: 1205-13.
165. Chida D, Hashimoto O, Kuwahara M, et al. Increased fat:carbohydrate oxidation ratio in Il1ra (-/-) mice on a high-fat diet is associated with increased sympathetic tone. Diabetologia 2008; 51: 1698-706.
166. Larsen CM, Faulenbach M, Vaag A, et al. Interleukin-1-receptor antagonist in type 2 diabetes mellitus. N Engl J Med 2007; 356: 1517-26.
167. Ehses JA, Lacraz G, Giroix MH, et al. IL-1 antagonism reduces hyperglycemia and tissue inflammation in the type 2 diabetic GK rat. Proc Natl Acad Sci U S A 2009; 106: 13998-4003.
168. Dinarello CA. Biology of interleukin 1. FASEB J 1988; 2: 108-15.
169. Banks WA, Kastin AJ. Human interleukin-1 alpha crosses the blood-testis barriers of the mouse. J Androl 1992; 13: 254-9.
170. Ban E, Milon G, Prudhomme N, Fillion G, Haour F. Receptors for interleukin-1 (alpha and beta) in mouse brain: mapping and neuronal localization in hippocampus. Neuroscience 1991; 43: 21-30.
171. Takao T, Mitchell WM, Tracey DE, De Souza EB. Identification of interleukin-1 receptors in mouse testis. Endocrinology 1990; 127: 251-8.
172. Katsuura G, Gottschall PE, Arimura A. Identification of a highaffinity receptor for interleukin-1 beta in rat brain. Biochem Biophys Res Commun 1988; 156: 61-7.
173. Wong ML, Licinio J. Localization of interleukin 1 type I receptor mRNA in rat brain. Neuroimmunomodulation 1994; 1: 110-5.
174. Plotkin SR, Banks WA, Maness LM, Kastin AJ. Differential transport of rat and human interleukin-1alpha across the bloodbrain barrier and blood-testis barrier in rats. Brain Res 2000; 881: 57-61.
175. del Rey A, Monge-Arditi G, Besedovsky HO. Central and peripheral mechanisms contribute to the hypoglycemia induced by interleukin-1. Ann N Y Acad Sci 1998; 840: 153-61.
176. Vega C, Pellerin L, Dantzer R, Magistretti PJ. Long-term modulation of glucose utilization by IL-1 alpha and TNF-alpha in astrocytes: Na+ pump activity as a potential target via distinct signaling mechanisms. Glia 2002; 39: 10-8.
177. Khan SA, Nieschlag E. Interleukin-1 inhibits follitropin-induced aromatase activity in immature rat Sertoli cells in vitro. Molecular and Cellular Endocrinology 1991; 75: 1-7.
178. Syed V, Stephan JP, Gerard N, et al. Residual bodies activate Sertoli cell interleukin-1 alpha (IL-1 alpha) release, which triggers IL-6 production by an autocrine mechanism, through the lipoxygenase pathway. Endocrinology 1995; 136: 3070-8.
179. Pollanen P, Soder O, Parvinen M. Interleukin-1 alpha stimulation of spermatogonial proliferation in vivo. Reproduction, Fertility and Development 1989; 1: 85-7.
180. Parvinen M, Soder O, Mali P, Froysa B, Ritzen EM. In vitro stimulation of stage-specific deoxyribonucleic acid synthesis in rat seminiferous tubule segments by interleukin-1 alpha. Endocrinology 1991; 129: 1614-20.
181. Nehar D, Mauduit C, Boussouar F, Benahmed M. Interleukin 1alpha stimulates lactate dehydrogenase A expression and lactate production in cultured porcine sertoli cells. Biology of Reproduction 1998; 59: 1425-32.