Purinergic signalling and diabetes

Purinergic Signalling

Volumn 9, Issue 3, 2013, Pages 307-324

  Burnstock, Geoffrey ^a,b   Novak, Ivana ^c  

^a ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

cells; Adenosine 5 triphosphate; Cardiovascular disease; Exocrine pancreas; Insulin; Nephropathy; Obesity; Pain

Indexed keywords

6 N CYCLOHEXYL 2' O METHYLADENOSINE; ADENOSINE; ADENOSINE A1 RECEPTOR AGONIST; ADENOSINE DIPHOSPHATE; ADENOSINE RECEPTOR; ADENOSINE RECEPTOR BLOCKING AGENT; ADENOSINE TRIPHOSPHATE; ATL 844; BVT 115959; GLUCAGON; GS 6201; GS 9667; INSULIN; NUCLEOTIDE; PURINERGIC P2X RECEPTOR; PURINERGIC P2Y RECEPTOR; PURINERGIC RECEPTOR; UNCLASSIFIED DRUG;

APOPTOSIS; CARDIOVASCULAR SYSTEM; CELL PROLIFERATION; CELL PROTECTION; DIABETES MELLITUS; DIABETIC NEUROPATHY; DIABETIC RETINOPATHY; GASTROINTESTINAL TRACT; HUMAN; HYPERTRIGLYCERIDEMIA; INSULIN RELEASE; KIDNEY DISEASE; NONHUMAN; PANCREAS; PANCREAS ISLET BETA CELL; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PREGNANCY DIABETES MELLITUS; REVIEW; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; SKIN; UROGENITAL SYSTEM;

ANIMALS; DIABETES MELLITUS; HUMANS; PURINES; RECEPTORS, PURINERGIC; SIGNAL TRANSDUCTION;

EID: 84883465174     PISSN: 15739538     EISSN: 15739546     Source Type: Journal    
DOI: 10.1007/s11302-013-9359-2     Document Type: Review

References (236)

1. van Belle TL, Coppieters KT, von Herrath MG (2011) Type 1 diabetes: etiology, immunology, and therapeutic strategies. Physiol Rev 91: 79-118.
2. Stumvoll M, Goldstein BJ, van Haeften TW (2005) Type 2 diabetes: principles of pathogenesis and therapy. Lancet 365: 1333-1346.
3. Dinarello CA, Donath MY, Mandrup-Poulsen T (2010) Role of IL-1 β in type 2 diabetes. Curr Opin Endocrinol Diabetes Obes 17: 314-321.
4. Kalupahana NS, Moustaid-Moussa N, Claycombe KJ (2012) Immunity as a link between obesity and insulin resistance. Mol Aspects Med 33: 26-34.
5. Osborn O, Olefsky JM (2012) The cellular and signaling networks linking the immune system and metabolism in disease. Nat Med 18: 363-374.
6. Johansson BB, Torsvik J, Bjorkhaug L, Vesterhus M, Ragvin A, Tjora E, Fjeld K, Hoem D, Johansson S, Raeder H, Lindquist S, Hernell O, Cnop M, Saraste J, Flatmark T, Molven A, Njolstad PR (2011) Diabetes and pancreatic exocrine dysfunction due to mutations in the carboxyl ester lipase gene-maturity onset diabetes of the young (CEL-MODY): a protein misfolding disease. J Biol Chem 286: 34593-34605.
7. Leeds JS, Oppong K, Sanders DS (2011) The role of fecal elastase-1 in detecting exocrine pancreatic disease. Nat Rev Gastroenterol Hepatol 8: 405-415.
8. Andersen DK (2012) The practical importance of recognizing pancreatogenic or type 3c diabetes. Diabetes Metab Res Rev 28: 326-328.
9. Cui Y, Andersen DK (2011) Pancreatogenic diabetes: special considerations for management. Pancreatology 11: 279-294.
10. Bertelli E, Bendayan M (2005) Association between endocrine pancreas and ductal system. More than an epiphenomenon of endocrine differentiation and development? J Histochem Cytochem 53: 1071-1086.
11. Movahedi B, van de Casteele M, Caluwe N, Stange G, Breckpot K, Thielemans K, Vreugdenhil G, Mathieu C, Pipeleers D (2004) Human pancreatic duct cells can produce tumour necrosis factor-α that damages neighbouring beta cells and activates dendritic cells. Diabetologia 47: 998-1008.
12. Movahedi B, Gysemans C, Jacobs-Tulleneers-Thevissen D, Mathieu C, Pipeleers D (2008) Pancreatic duct cells in human islet cell preparations are a source of angiogenic cytokines interleukin-8 and vascular endothelial growth factor. Diabetes 57: 2128-2136.
13. Ewald N, Raspe A, Kaufmann C, Bretzel RG, Kloer HU, Hardt PD (2009) Determinants of exocrine pancreatic function as measured by fecal elastase-1 concentrations (FEC) in patients with diabetes mellitus. Eur J Med Res 14: 118-122.
14. Ewald N, Kaufmann C, Raspe A, Kloer HU, Bretzel RG, Hardt PD (2012) Prevalence of diabetes mellitus secondary to pancreatic diseases (type 3c). Diabetes Metab Res Rev 28: 338-342.
15. Rees DA, Alcolado JC (2005) Animal models of diabetes mellitus. Diabet Med 22: 359-370.
16. Chatzigeorgiou A, Halapas A, Kalafatakis K, Kamper E (2009) The use of animal models in the study of diabetes mellitus. In Vivo 23: 245-258.
17. Rakieten N, Rakieten ML, Nadkarni MV (1963) Studies on the diabetogenic action of streptozotocin (Nsc-37917). Cancer Chemother Reports 29: 91-98.
18. Jacobs HR (1937) Hyperglycemic actions of alloxan. Proc Soc Exp Biol Med 37: 404-409.
19. Rerup CC (1970) Drugs producing diabetes through damage of the insulin secreting cells. Pharmacol Rev 22: 485-518.
20. Nakhooda AF, Like AA, Chappel CI, Murray FT, Marliss EB (1977) The spontaneously diabetic Wistar rat. Metabolic and morphologic studies. Diabetes 26: 100-112.
21. Makino S, Kunimoto K, Muraoka Y, Mizushima Y, Katagiri K, Tochino Y (1980) Breeding of a non-obese, diabetic strain of mice. Jikken Dobutsu 29: 1-13.
22. Domènech A, Pasquinelli G, De Giorgio R, Gori A, Bosch F, Pumarola M, Jiménez M (2011) Morphofunctional changes underlying intestinal dysmotility in diabetic RIP-I/hIFNβ transgenic mice. Int J Exp Pathol 92: 400-412.
23. Clark JB, Palmer CJ, Shaw WN (1983) The diabetic Zucker fatty rat. Proc Soc Exp Biol Med 173: 68-75.
24. Burnstock G (1972) Purinergic nerves. Pharmacol Rev 24: 509-581.
25. Yegutkin GG (2008) Nucleotide- and nucleoside-converting ectoenzymes: important modulators of purinergic signalling cascade. Biochim Biophys Acta 1783: 673-694.
26. Burnstock G (1978) A basis for distinguishing two types of purinergic receptor. In: Straub RW, Bolis L (eds) Cell membrane receptors for drugs and hormones: a multidisciplinary approach. Raven Press, New York, pp 107-118.
27. 2-purinoceptor? Gen Pharmacol 16: 433-440.
28. Ralevic V, Burnstock G (1998) Receptors for purines and pyrimidines. Pharmacol Rev 50: 413-492.
29. Burnstock G (2007) Purine and pyrimidine receptors. Cell Mol Life Sci 64: 1471-1483.
30. Abbracchio MP, Burnstock G, Boeynaems J-M, Barnard EA, Boyer JL, Kennedy C, Knight GE, Fumagalli M, Gachet C, Jacobson KA, Weisman GA (2006) International Union of Pharmacology. Update on the P2Y G protein-coupled nucleotide receptors: from molecular mechanisms and pathophysiology to therapy. Pharmacol Rev 58: 281-341.
31. Burnstock G, Knight GE (2004) Cellular distribution and functions of P2 receptor subtypes in different systems. Int Rev Cytol 240: 31-304.
32. Hattori M, Gouaux E (2012) Molecular mechanism of ATP binding and ion channel activation in P2X receptors. Nature 485: 207-212.
33. Xu F, Wu H, Katritch V, Han GW, Jacobson KA, Gao ZG, Cherezov V, Stevens RC (2011) Structure of an agonist-bound human A2A adenosine receptor. Science 332: 322-327.
34. Zimmermann H, Zebisch M, Strater N (2012) Cellular function and molecular structure of ecto-nucleotidases. Purinergic Signal 8: 437-502.
35. Novak I (2008) Purinergic receptors in the endocrine and exocrine pancreas. Purinergic Signal 4: 237-253.
36. Novak I (2011) Purinergic signalling in epithelial ion transport-regulation of secretion and absorption. Acta Physiologica 202: 501-522.
37. Hellman B (2009) Pulsatility of insulin release-a clinically important phenomenon. Ups J Med Sci 114: 193-205.
38. Petit P, Lajoix AD, Gross R (2009) P2 purinergic signalling in the pancreatic beta-cell: control of insulin secretion and pharmacology. Eur J Pharm Sci 37: 67-75.
39. Burnstock G, Novak I (2012) Purinergic signalling in the pancreas in health and disease. J Endocrinol 213: 123-141.
40. Karanauskaite J, Hoppa MB, Braun M, Galvanovskis J, Rorsman P (2009) Quantal ATP release in rat beta-cells by exocytosis of insulin-containing LDCVs. Pflugers Arch 458: 389-401.
41. Haanes KA, Novak I (2010) ATP storage and uptake by isolated pancreatic zymogen granules. Biochem J 429: 303-311.
42. Lazarowski ER (2012) Vesicular and conductive mechanisms of nucleotide release. Purinergic Signal 8: 359-373.
43. Lavoie EG, Fausther M, Kauffenstein G, Kukulski F, Kunzli BM, Friess H, Sevigny J (2010) Identification of the ectonucleotidases expressed in mouse, rat, and human Langerhans islets: potential role of NTPDase3 in insulin secretion. Am J Physiol Endocrinol Metab 299: E647-E656.
44. Yegutkin GG, Samburski SS, Jalkalen S, Novak I (2006) ATP-consuming and ATP-generating enzymes secreted by pancreas. J Biol Chem 281: 29441-29447.
45. 2B receptors on glucose homoeostasis. J Pharm Pharmacol 58: 1639-1645.
46. Figler RA, Wang G, Srinivasan S, Jung DY, Zhang Z, Pankow JS, Ravid K, Fredholm B, Hedrick CC, Rich SS, Kim JK, LaNoue KF, Linden J (2011) Links between insulin resistance, adenosine A2B receptors, and inflammatory markers in mice and humans. Diabetes 60: 669-679.
47. Andersson O, Adams BA, Yoo D, Ellis GC, Gut P, Anderson RM, German MS, Stainier DY (2012) Adenosine signaling promotes regeneration of pancreatic β cells in vivo. Cell Metab 15: 885-894.
48. Salehi A, Qader SS, Grapengiesser E, Hellman B (2005) Inhibition of purinoceptors amplifies glucose-stimulated insulin release with removal of its pulsatility. Diabetes 54: 2126-2131.
49. Coutinho-Silva R, Parsons M, Robson T, Burnstock G (2001) Changes in expression of P2 receptors in rat and mouse pancreas during development and aging. Cell Tissue Res 306: 373-383.
50. Salehi A, Qader SS, Grapengiesser E, Hellman B (2007) Pulses of somatostatin release are slightly delayed compared with insulin and antisynchronous to glucagon. Regul Pept 144: 43-49.
51. + channels in human pancreatic duct epithelium. Am J Physiol Cell Physiol. doi: 10. 1152/ajpcell. 00196. 2012.
52. Ko T, An HJ, Ji YG, Kim OJ, Lee DH (2012) P2Y receptors regulate proliferation of human pancreatic duct epithelial cells. Pancreas 41: 797-803.
53. 2+ signaling events following activation in culture and in a disease model of pancreatitis. Mol Biol Cell 22: 421-436.
54. Haanes KA, Schwab A, Novak I (2012) The P2X7 receptor supports both life and death in the fibrogenic pancreatic stellate cells. PLoS One 7(12): e51164.
55. Yabe D, Seino Y (2011) Two incretin hormones GLP-1 and GIP: comparison of their actions in insulin secretion and beta cell preservation. Prog Biophys Mol Biol 107: 248-256.
56. 2+-stimulated degradation of polyphosphoinositides in pancreatic islets from neonatally streptozotocin-diabetic rats. Biochem Biophys Res Commun 228: 573-578.
57. Nukatsuka M, Yoshimura Y, Nishida M, Kawada J (1990) Importance of the concentration of ATP in rat pancreatic beta cells in the mechanism of streptozotocin-induced cytotoxicity. J Endocrinol 127: 161-165.
58. Grill V, Radtke M, Qvigstad E, Kollind M, Björklund A (2009) Beneficial effects of K-ATP channel openers in diabetes: an update on mechanisms and clinical experiences. Diabetes Obes Metab 11: 143-148.
59. de Wet H, Proks P, Lafond M, Aittoniemi J, Sansom MS, Flanagan SE, Pearson ER, Hattersley AT, Ashcroft FM (2008) A mutation (R826W) in nucleotide-binding domain 1 of ABCC8 reduces ATPase activity and causes transient neonatal diabetes. EMBO Rep 9: 648-654.
60. Detimary P, Jonas J-C, Henquin J-C (1995) Possible links between glucose-induced changes in the energy state of pancreatic B cells and insulin release. J Clin Invest 96: 1738-1745.
61. Zhao Z, Zhao C, Zhang XH, Zheng F, Cai W, Vlassara H, Ma ZA (2009) Advanced glycation end products inhibit glucose-stimulated insulin secretion through nitric oxide-dependent inhibition of cytochrome c oxidase and adenosine triphosphate synthesis. Endocrinology 150: 2569-2576.
62. Mikhail TH, Awadallah R (1977) The effect of ATP and certain trace elements on the induction of experimental diabetes. Z Ernährungswiss 16: 176-183.
63. Awadallah R, Tahani HM, El-Dessoukey EA (1979) Serum mineral changes due to exogenous ATP and certain trace elements in experimental diabetes. Z Ernährungswiss 18: 1-7.
64. Tahani HM (1979) The purinergic nerve hypothesis and insulin secretion. Z Ernährungswiss 18: 128-138.
65. Hillaire-Buys D, Gross R, Chapal J, Ribes G, Loubatieres-Mariani MM (1992) P2y purinoceptor responses of β cells and vascular bed are preserved in diabetic rat pancreas. Br J Pharmacol 106: 610-615.
66. 2 purinoceptor agonists in Zucker diabetic fatty rats. Am J Physiol 270: E504-E512.
67. Fischer B, Chulkin A, Boyer JL, Harden KT, Gendron FP, Beaudoin AR, Chapal J, Hillaire-Buys D, Petit P (1999) 2-thioether 5′-O-(1-thiotriphosphate)adenosine derivatives as new insulin secretagogues acting through P2Y-Receptors. J Med Chem 42: 3636-3646.
68. Fischer B et al (2000) 2-Thioether-5'-O-(1-thiotriphosphate)-adenosine derivatives: new insulin secretagogues acting through P2Y-receptors. Isr Med Assoc J 2(92-8): 92-98.
69. Farret A, Vignaud M, Dietz S, Vignon J, Petit P, Gross R (2004) P2Y purinergic potentiation of glucose-induced insulin secretion and pancreatic beta-cell metabolism. Diabetes 53(Suppl 3): S63-S66, S63-S66.
70. Eliahu S, Barr HM, Camden J, Weisman GA, Fischer B (2010) A novel insulin secretagogue based on a dinucleoside polyphosphate scaffold. J Med Chem 53: 2472-2481.
71. 1 receptor is involved in the maintenance of glucose homeostasis and in insulin secretion in mice. Purinergic Signal 1: 145-151.
72. Coutinho-Silva R, Parsons M, Robson T, Lincoln J, Burnstock G (2003) P2X and P2Y purinoceptor expression in pancreas from streptozotocin-diabetic rats. Mol Cell Endocrinol 204: 141-154.
73. 7 receptors in NOD mouse pancreas during the development of diabetes. Autoimmunity 40: 108-116.
74. 7 receptors regulate secretion of interleukin-1 receptor antagonist and beta cell function and survival. Diabetologia 52: 1579-1588.
75. Gross R, Hillaire-Buys D, Bertrand G, Ribes G, Loubatières-Mariani MM (1989) Diabetes and impaired response of glucagon cells and vascular bed to adenosine in rat pancreas. Diabetes 38: 1291-1295.
76. Laurent F, Hillaire-Buys D, Chapal J, Dietz S, Portet K, Cros G, Petit P, Michel A (1999) Contrasting effects of streptozotocin-induced diabetes on the in vitro relaxant properties of adenosine in rat pancreatic vascular bed and thoracic aorta. Naunyn Schmiedebergs Arch Pharmacol 360: 309-316.
77. Gross R, Hillaire-Buys D, Ribes G, Loubatières-Mariani MM (1991) Diabetes alters the responses of glucagon secreting cells and vascular bed to isoprenaline and forskolin in vitro in rat pancreas. Life Sci 48: 2349-2358.
78. Johansson SM, Salehi A, Sandstrom ME, Westerblad H, Lundquist I, Carlsson PO, Fredholm BB, Katz A (2007) A1 receptor deficiency causes increased insulin and glucagon secretion in mice. Biochem Pharmacol 74: 1628-1635.
79. Faulhaber-Walter R, Jou W, Mizel D, Li L, Zhang J, Kim SM, Huang Y, Chen M, Briggs JP, Gavrilova O, Schnermann JB (2011) Impaired glucose tolerance in the absence of adenosine A1 receptor signaling. Diabetes 60: 2578-2587.
80. Németh ZH, Bleich D, Csóka B, Pacher P, Mabley JG, Himer L, Vizi ES, Deitch EA, Szabo C, Cronstein BN, Hasko G (2007) Adenosine receptor activation ameliorates type 1 diabetes. FASEB J 21: 2379-2388.
81. Maedler K, Dharmadhikari G, Schumann DM, Storling J (2009) Interleukin-1β targeted therapy for type 2 diabetes. Expert Opin Biol Ther 9: 1177-1188.
82. Elliott JI, Higgins CF (2004) Major histocompatibility complex class I shedding and programmed cell death stimulated through the proinflammatory P2X7 receptor: a candidate susceptibility gene for NOD diabetes. Diabetes 53: 2012-2017.
83. Lenertz LY, Gavala ML, Zhu Y, Bertics PJ (2011) Transcriptional control mechanisms associated with the nucleotide receptor P2X7, a critical regulator of immunologic, osteogenic, and neurologic functions. Immunol Res 50: 22-38.
84. Balasubramanian R, Ruiz de Azua I, Wess J, Jacobson KA (2010) Activation of distinct P2Y receptor subtypes stimulates insulin secretion in MIN6 mouse pancreatic beta cells. Biochem Pharmacol 79: 1317-1326.
85. 13 induce apoptosis in pancreatic beta-cells. Cell Mol Life Sci 67: 445-453.
86. 13 receptor. Purinergic Signal 2012 [Epub ahead of print 1/9/12].
87. Ohtani M, Ohura K, Oka T (2011) Involvement of P2X receptors in the regulation of insulin secretion, proliferation and survival in mouse pancreatic β-cells. Cell Physiol Biochem 28: 355-366.
88. Annes JP, Ryu JH, Lam K, Carolan PJ, Utz K, Hollister-Lock J, Arvanites AC, Rubin LL, Weir G, Melton DA (2012) Adenosine kinase inhibition selectively promotes rodent and porcine islet beta-cell replication. Proc Natl Acad Sci U S A 109: 3915-3920.
89. Loubatières-Mariani MM, Hillaire-Buys D, Chapal J, Bertrand G, Petit P (1997) P2 purinoceptor agonists: new insulin secretagogues potentially useful in the treatment of non-insulin-dependent diabetes mellitus. In: Jacobson KA, Jarvis MF (eds) Purinergic approaches in experimental therapeutics. Wiley-Liss, New York, pp 253-260.
90. Petit P, Hillaire-Buys D, Loubatières-Mariani MM, Chapal J (2001) Purinergic receptors and the pharmacology of type 2 diabetes. In: Abbracchio MP, Williams M (eds) Handbook of experimental pharmacology. Purinergic and pyrimidinergic signalling II-cardiovascular, respiratory, immune, metabolic and gastrointestinal tract function. Springer, Berlin, pp 337-391.
91. Farret A, Lugo-Garcia L, Galtier F, Gross R, Petit P (2005) Pharmacological interventions that directly stimulate or modulate insulin secretion from pancreatic beta-cell: implications for the treatment of type 2 diabetes. Fund Clin Pharmacol 19: 647-656.
92. McIntosh VJ, Lasley RD (2012) Adenosine receptor-mediated cardioprotection: are all 4 subtypes required or redundant? J Cardiovasc Pharmacol Ther 17: 21-33.
93. Headrick JP, Peart JN, Reichelt ME, Haseler LJ (2011) Adenosine and its receptors in the heart: regulation, retaliation and adaptation. Biochim Biophy Acta Biomembranes 1808: 1413-1428.
94. Mueller SM, Mueller TM, Ertel PJ (1982) Sympathetic and vascular dysfunction in early experimental juvenile diabetes mellitus. Am J Physiol 243: H139-H144.
95. Ralevic V, Belai A, Burnstock G (1995) Effects of streptozotocin-diabetes on sympathetic nerve, endothelial and smooth muscle function in the rat mesenteric arterial bed. Eur J Pharmacol 286: 193-199.
96. Ralevic V, Belai A, Burnstock G (1993) Impaired sensory-motor nerve function in the isolated mesenteric arterial bed of streptozotocin-diabetic and ganglioside-treated streptozotocin-diabetic rats. Br J Pharmacol 110: 1105-1111.
97. Ishida K, Matsumoto T, Taguchi K, Kamata K, Kobayashi T (2011) Mechanisms underlying altered extracellular nucleotide-induced contractions in mesenteric arteries from rats in later-stage type 2 diabetes: effect of ANG II type 1 receptor antagonism. Am J Physiol Heart Circ Physiol 301: H1850-H1861.
98. Speier S, Rupnik M (2003) A novel approach to in situ characterization of pancreatic beta-cells. Pflugers Arch 446: 553-558.
99. Onodera H, Hirata T, Sugawara H, Sugai K, Yoda B, Toyota T, Goto Y (1982) Platelet sensitivity to adenosine diphosphate and to prostacyclin in diabetic patients. Tohoku J Exp Med 137: 423-428.
100. Guo X, Wu J, Du J, Ran J, Xu J (2009) Platelets of type 2 diabetic patients are characterized by high ATP content and low mitochondrial membrane potential. Platelets 20: 588-593.
101. Lunkes GI, Lunkes DS, Morsch VM, Mazzanti CM, Morsch AL, Miron VR, Schetinger MR (2004) NTPDase and 5′-nucleotidase activities in rats with alloxan-induced diabetes. Diabetes Res Clin Pract 65: 1-6.
102. Miron VR, Bauermann L, Morsch AL, Zanin RF, Correa M, da Silva AC, Mazzanti C, Morsch VM, Lunkes GI, Schetinger MR (2007) Enhanced NTPDase and 5′-nucleotidase activities in diabetes mellitus and iron-overload model. Mol Cell Biochem 298: 101-107.
103. De Bona KS, Belle LP, Sari MH, Thome G, Schetinger MR, Morsch VM, Boligon A, Athayde ML, Pigatto AS, Moretto MB (2010) Syzygium cumini extract decrease adenosine deaminase, 5′nucleotidase activities and oxidative damage in platelets of diabetic patients. Cell Physiol Biochem 26: 729-738.
104. Aursnes I, Dahl-Jørgensen K, Hanssen KF (1986) ATP-concentrations in erythrocytes influenced by insulin levels in plasma. Clin Hemorheol 6: 429-433.
105. Sprague R, Stephenson A, Bowles E, Stumpf M, Ricketts G, Lonigro A (2012) Expression of the heterotrimeric G protein Gi and ATP release are impaired in erythrocytes of humans with diabetes mellitus. Adv Exp Med Biol 588: 207-216.
106. Moritz CE, Abreu-Vieira G, Piroli C, De Senna PN, Cardoso VV, Wink MR, Harthmann AD, Rucker B, Casali EA (2012) Physical training normalizes nucleotide hydrolysis and biochemical parameters in blood serum from streptozotocin-diabetic rats. Arch Physiol Biochem 118: 253-259.
107. Thaning P, Bune LT, Hellsten Y, Pilegaard H, Saltin B, Rosenmeier JB (2010) Attenuated purinergic receptor function in patients with type 2 diabetes. Diabetes 59: 182-189.
108. 7 receptor activation on the retinal blood velocity of diabetic rabbits. Arch Ophthalmol 124: 1143-1149.
109. Nakazawa T, Mori A, Saito M, Sakamoto K, Nakahara T, Ishii K (2008) Vasodilator effects of adenosine on retinal arterioles in streptozotocin-induced diabetic rats. Naunyn Schmiedebergs Arch Pharmacol 376: 423-430.
110. Malorgio F, Cignarella A, Pelosi V, Bolego C, Gaion RM (2010) Alterations of adenosine-related inflammatory pathways in vascular smooth muscle cells from diabetic rats. Purinergic Signal 6: 96.
111. Fahim M, Hussain T, Mustafa SJ (2001) Relaxation of rat aorta by adenosine in diabetes with and without hypertension: role of endothelium. Eur J Pharmacol 412: 51-59.
112. Pieper GM, Mei DA, Langenstroer P, O'Rourke ST (1992) Bioassay of endothelium-derived relaxing factor in diabetic rat aorta. Am J Physiol 263: H676-H680.
113. Guzman-Gutierrez E, Abarzua F, Belmar C, Nien JK, Ramirez MA, Arroyo P, Salomon C, Westermeier F, Puebla C, Leiva A, Casanello P, Sobrevia L (2011) Functional link between adenosine and insulin: a hypothesis for fetoplacental vascular endothelial dysfunction in gestational diabetes. Curr Vasc Pharmacol 9: 750-762.
114. Parés-Herbuté N, Hillaire-Buys D, Etienne P, Gross R, Loubatières-Mariani MM, Monnier L (1996) Adenosine inhibitory effect on enhanced growth of aortic smooth muscle cells from streptozotocin-induced diabetic rats. Br J Pharmacol 118: 783-789.
115. Usta CK, Adan G, Özdem SS (2001) The effects of adenosine on isolated right atrial preparations from streptozotocin-diabetic rats. J Auton Pharmacol 21: 191-195.
116. Podgorska M, Kocbuch K, Grden M, Szutowicz A, Pawelczyk T (2006) Reduced ability to release adenosine by diabetic rat cardiac fibroblasts due to altered expression of nucleoside transporters. J Physiol 576: 179-189.
117. Wang Y, Ebermann L, Sterner-Kock A, Wika S, Schultheiss HP, Dörner A, Walther T (2009) Myocardial overexpression of adenine nucleotide translocase 1 ameliorates diabetic cardiomyopathy in mice. Exp Physiol 94: 220-227.
118. Alfarano C, Suffredini S, Fantappie O, Mugelli A, Cerbai E, Manni ME, Raimondi L (2011) The effect of losartan treatment on the response of diabetic cardiomyocytes to ATP depletion. Pharmacol Res 63: 225-232.
119. Grden M, Podgórska M, Szutowicz A, Pawelczyk T (2005) Altered expression of adenosine receptors in heart of diabetic rat. J Physiol Pharmacol 56: 587-597.
120. Bravo PE, Hage FG, Woodham RM, Heo J, Editor IA (2008) Heart rate response to adenosine in patients with diabetes mellitus and normal myocardial perfusion imaging. Am J Cardiol 102: 1103-1106.
121. Hage FG, Heo J, Franks B, Belardinelli L, Blackburn B, Wang W, Iskandrian AE (2009) Differences in heart rate response to adenosine and regadenoson in patients with and without diabetes mellitus. Am Heart J 157: 771-776.
122. Fürstenau CR, Rücker B, Pochmann D, Vieira G, Bischoff LB, Sarkis JJ, Zerbini LF, Casali EA, Wink MR (2010) Streptozotocin-induced diabetes alters ATP and ADP hydrolysid in rat heart left ventricle. Purinergic Signalling 6: S114.
123. 7 receptor-mediated function in human primary fibroblasts. Diabetologia 43: 1248-1256.
124. Solini A, Chiozzi P, Morelli A, Adinolfi E, Rizzo R, Baricordi OR, Di Virgilio F (2004) Enhanced P2X7 activity in human fibroblasts from diabetic patients: a possible pathogenetic mechanism for vascular damage in diabetes. Arterioscler Thromb Vasc Biol 24: 1240-1245.
125. Solini A, Chiozzi P, Morelli A, Passaro A, Fellin R, Di Virgilio F (2003) Defective P2Y purinergic receptor function: A possible novel mechanism for impaired glucose transport. J Cell Physiol 197: 435-444.
126. Sobrevia L, Jarvis SM, Yudilevich DL (1994) Adenosine transport in cultured human umbilical vein endothelial cells is reduced in diabetes. Am J Physiol 267: C39-C47.
127. San Martín R, Sobrevia L (2006) Gestational diabetes and the adenosine/L-arginine/nitric oxide (ALANO) pathway in human umbilical vein endothelium. Placenta 27: 1-10.
128. Farías M, Puebla C, Westermeier F, Jo MJ, Pastor-Anglada M, Casanello P, Sobrevia L (2010) Nitric oxide reduces SLC29A1 promoter activity and adenosine transport involving transcription factor complex hCHOP-C/EBPα in human umbilical vein endothelial cells from gestational diabetes. Cardiovasc Res 86: 45-54.
129. Westermeier F, Salomon C, Gonzalez M, Puebla C, Guzman-Gutierrez E, Cifuentes F, Leiva A, Casanello P, Sobrevia L (2011) Insulin restores gestational diabetes mellitus-reduced adenosine transport involving differential expression of insulin receptor isoforms in human umbilical vein endothelium. Diabetes 60: 1677-1687.
130. Thomas PK, Tomlinson DR (1993) Diabetic and hypoglycaemic neuropathy. In: Dyck PI, Thomas PK, Griffin JW, Low PA, Poduslo JF (eds) Peripheral neuropathy. W. B. Saunders, Philadelphia, pp 1219-1250.
131. Yasuda H, Terada M, Maeda K, Kogawa S, Sanada M, Haneda M, Kashiwagi A, Kikkawa R (2003) Diabetic neuropathy and nerve regeneration. Prog Neurobiol 69: 229-285.
132. Anand P (1996) Neurotrophins and peripheral neuropathy. Philos Trans R Soc Lond B Biol Sci 351: 449-454.
133. Low PA (2009) Experimental diabetic autonomic neuropathy. In: Veves A, Malik R (eds) Contemporary diabetes: diabetic neuropathy. Clinical management. Humana, Totowa, pp 153-164.
134. Giachetti A (1978) The functional state of sympathetic nerves in spontaneously diabetic mice. Diabetes 27: 969-974.
135. Mundinger TO, Mei Q, Figlewicz DP, Lernmark A, Taborsky GJ Jr (2003) Impaired glucagon response to sympathetic nerve stimulation in the BB diabetic rat: effect of early sympathetic islet neuropathy. Am J Physiol Endocrinol Metab 285: E1047-E1054.
136. Christianson JA, Riekhof JT, Wright DE (2003) Restorative effects of neurotrophin treatment on diabetes-induced cutaneous axon loss in mice. Exp Neurol 179: 188-199.
137. Archer AG, Watkins PJ, Thomas PK, Sharma AK, Payan J (1983) The natural history of acute painful neuropathy in diabetes mellitus. J Neurol Neurosurg Psychiatry 46: 491-499.
138. Sato J, Kumazawa T (1996) Sympathetic modulation of cutaneous polymodal receptors in chronically inflamed and diabetic rats. Prog Brain Res 113: 153-159.
139. Lynch JJ III, Jarvis MF, Kowaluk EA (1999) An adenosine kinase inhibitor attenuates tactile allodynia in a rat model of diabetic neuropathic pain. Eur J Pharmacol 364: 141-146.
140. Kiesman WF, Elzein E, Zablocki J (2009) A1 adenosine receptor antagonists, agonists, and allosteric enhancers. Handb Exp Pharmacol 193: 25-58.
141. Valls MD, Cronstein BN, Montesinos MC (2009) Adenosine receptor agonists for promotion of dermal wound healing. Biochem Pharmacol 77: 1117-1124.
142. Tsuda M, Tozaki-Saitoh H, Inoue K (2010) Pain and purinergic signaling. Brain Res Rev 63: 222-232.
143. Migita K, Moriyama T, Koguchi M, Honda K, Katsuragi T, Takano Y, Ueno S (2009) Modulation of P2X receptors in dorsal root ganglion neurons of streptozotocin-induced diabetic neuropathy. Neurosci Lett 452: 200-203.
144. Xu GY, Li G, Liu N, Huang LY (2011) Mechanisms underlying purinergic P2X3 receptor-mediated mechanical allodynia induced in diabetic rats. Mol Pain 7: 60.
145. Balasubramanyan S, Sharma SS (2008) Protective effect of adenosine in diabetic neuropathic pain is mediated through adenosine A1-receptors. Indian J Physiol Pharmacol 52: 233-242.
146. Finco C, Abbracchio MP, Malosio ML, Cattabeni F, Di Giulio AM, Paternieri B, Mantegazza P, Gorio A (1992) Diabetes-induced alterations of central nervous system G proteins. ADP-ribosylation, immunoreactivity, and gene-expression studies in rat striatum. Mol Chem Neuropathol 17: 259-272.
147. Duarte JM, Oses JP, Rodrigues RJ, Cunha RA (2007) Modification of purinergic signaling in the hippocampus of streptozotocin-induced diabetic rats. Neuroscience 149: 382-391.
148. Morrison PD, Mackinnon MW, Bartrup JT, Skett PG, Stone TW (1992) Changes in adenosine sensitivity in the hippocampus of rats with streptozotocin-induced diabetes. Br J Pharmacol 105: 1004-1008.
149. Cassar M, Jones MG, Szatkowski M (1998) Reduced adenosine uptake accelerates ischaemic block of population spikes in hippocampal slices from streptozotocin-treated diabetic rats. Eur J Neurosci 10: 239-245.
150. 2A receptor density in the hippocampus of streptozotocin-induced diabetic rats. Neurochem Int 48: 144-150.
151. 2+-ATPase activity and ionized calcium in type 2 diabetic patients with neuropathy. Diabetes Res Clin Pract 49: 113-118.
152. Shah CA (2008) Diabetic retinopathy: a comprehensive review. Indian J Med Sci 62: 500-519.
153. Steinle JJ, Kern TS, Thomas SA, McFadyen-Ketchum LS, Smith CP (2009) Increased basement membrane thickness, pericyte ghosts, and loss of retinal thickness and cells in dopamine beta hydroxylase knockout mice. Exp Eye Res 88: 1014-1019.
154. Costa G, Pereira T, Neto AM, Cristóvão AJ, Ambrosio AF, Santos PF (2009) High glucose changes extracellular adenosine triphosphate levels in rat retinal cultures. J Neurosci Res 87: 1375-1380.
155. 2+ responses triggered by purinergic stimulation in retinal neurons and microglia. Brain Res 1316: 129-138.
156. Robertson PL, Ar D, Goldstein GW (1990) Phosphoinositide metabolism and prostacyclin formation in retinal microvascular endothelium: stimulation by adenine nucleotides. Exp Eye Res 50: 37-44.
157. 7-induced pore formation and apoptosis: an early effect of diabetes on the retinal microvasculature. Invest Ophthalmol Vis Sci 45: 1026-1032.
158. Sugiyama T, Kawamura H, Yamanishi S, Kobayashi M, Katsumura K, Puro DG (2008) Regulation of P2X7-induced pore formation and cell death in pericyte-containing retinal microvessels. Am J Physiol Cell Physiol 288: C568-C576.
159. Wurm A, Iandiev I, Hollborn M, Wiedemann P, Reichenbach A, Zimmermann H, Bringmann A, Pannicke T (2008) Purinergic receptor activation inhibits osmotic glial cell swelling in the diabetic rat retina. Exp Eye Res 87: 385-393.
160. Pflueger AC, Schenk F, Osswald H (1995) Increased sensitivity of the renal vasculature to adenosine in streptozotocin-induced diabetes mellitus rats. Am J Physiol 269: F529-F535.
161. Pflueger AC, Osswald H, Knox FG (1999) Adenosine-induced renal vasoconstriction in diabetes mellitus rats: role of nitric oxide. Am J Physiol 276: F340-F346.
162. 1-receptor deficient mice lacking the tubuloglomerular feedback mechanism. Acta Physiol (Oxf) 190: 253-259.
163. 1 receptors determine glomerular hyperfiltration and the salt paradox in early streptozotocin diabetes mellitus. Nephron Physiol 111: 30-38.
164. Oppermann M, Qin Y, Lai EY, Eisner C, Li L, Huang Y, Mizel D, Fryc J, Wilcox CS, Briggs J, Schnermann J, Castrop H (2009) Enhanced tubuloglomerular feedback in mice with vascular overexpression of A1 adenosine receptors. Am J Physiol Renal Physiol 297: F1256-F1264.
165. Castrop H (2007) Mediators of tubuloglomerular feedback regulation of glomerular filtration: ATP and adenosine. Acta Physiol (Oxf) 189: 3-14.
166. Guan Z, Inscho EW (2011) Role of adenosine 5′-triphosphate in regulating renal microvascular function and in hypertension. Hypertension 58: 333-340.
167. San Martin R, Valladares D, Roa H, Troncoso E, Sobrevia L (2009) Do adenosine receptors offer new therapeutic options for diabetic nephropathy? Curr Vasc Pharmacol 7: 450-459.
168. Vallon V, Osswald H (1994) Dipyridamole prevents diabetes-induced alterations of kidney function in rats. Naunyn Schmiedebergs Arch Pharmacol 349: 217-222.
169. Morato M, Patinha D, Afonso J, Correia C, Albino-Teixeira A (2010) Endogenous and exogenous adenosine and structural alterations in diabetic nephropathy: a possible role of the renin-angiotensin system? Purinergic Signal 6: 100.
170. Morato M, Patinha D, Afonso J, Sousa T, Albino-Teixeira A (2010) Renal effects of adenosine on diabetic Wistar and SHR rats. Purinergic Signal 6: 140.
171. Xia JF, Liang QL, Hu P, Wang YM, Li P, Luo GA (2009) Correlations of six related purine metabolites and diabetic nephropathy in Chinese type 2 diabetic patients. Clin Biochem 42: 215-220.
172. Roa H, Gajardo C, Troncoso E, Fuentealba V, Escudero C, Yáñez A, Sobrevia L, Pastor-Anglada M, Quezada C, San MR (2009) Adenosine mediates transforming growth factor-beta 1 release in kidney glomeruli of diabetic rats. FEBS Lett 583: 3192-3198.
173. 2A receptor activation attenuates inflammation and injury in diabetic nephropathy. Am J Physiol Renal Physiol 290: F828-F837.
174. Pawelczyk T, Grden M, Rzepko R, Sakowicz M, Szutowicz A (2005) Region-specific alterations of adenosine receptors expression level in kidney of diabetic rat. Am J Pathol 167: 315-325.
175. Pflueger AC, Berndt TJ, Knox FG (1998) Effect of renal interstitial adenosine infusion on phosphate excretion in diabetes mellitus rats. Am J Physiol 274: R1228-R1235.
176. Leipziger J (2011) Luminal nucleotides are tonic inhibitors of renal tubular transport. Curr Opin Nephrol Hypertens 20: 518-522.
177. Friedman DJ, Rennke HG, Csizmadia E, Enjyoji K, Robson SC (2007) The vascular ectonucleotidase ENTPD1 is a novel renoprotective factor in diabetic nephropathy. Diabetes 56: 2371-2379.
178. Ellenberg M (1980) Development of urinary bladder dysfunction in diabetes mellitus. Ann Intern Med 92: 321-323.
179. Longhurst PA, Belis JA (1986) Abnormalities of rat bladder contractility in streptozotocin-induced diabetes mellitus. J Pharmacol Exp Ther 238: 773-777.
180. Luheshi GN, Zar MA (1990) Inhibitory effect of streptozotocin-induced diabetes on non-cholinergic motor transmission in rat detrusor and its prevention by sorbinil. Br J Pharmacol 101: 411-417.
181. 2-muscarinic receptor inhibits the development of streptozotocin-induced neuropathy in mouse urinary bladder. J Pharmacol Exp Ther 335: 239-248.
182. Liu G, Daneshgari F (2005) Alterations in neurogenically mediated contractile responses of urinary bladder in rats with diabetes. Am J Physiol Renal Physiol 288: F1220-F1226.
183. Liu G, Daneshgari F (2008) Temporal expression of muscarinic and purinergic receptors in diabetic rat bladder. Neurourol Urodyn 27: 594-595.
184. Suadicani SO, Urban-Maldonado M, Tar MT, Melman A, Spray DC (2009) Effects of ageing and streptozotocin-induced diabetes on connexin43 and P2 purinoceptor expression in the rat corpora cavernosa and urinary bladder. BJU Int 103: 1686-1693.
185. Mumtaz FH, Lau DH, Siddiqui EJ, Morgan RJ, Thompson CS, Mikhailidis DP (2006) Changes in cholinergic and purinergic neurotransmission in the diabetic rabbit bladder. In Vivo 20: 1-4.
186. Benkó R, Lázár Z, Pórszasz R, Somogyi GT, Barthó L (2003) Effect of experimental diabetes on cholinergic, purinergic and peptidergic motor responses of the isolated rat bladder to electrical field stimulation or capsaicin. Eur J Pharmacol 478: 73-80.
187. Lee WC, Wu HP, Tai TY, Yu HJ, Chiang PH (2009) Investigation of urodynamic characteristics and bladder sensory function in the early stages of diabetic bladder dysfunction in women with type 2 diabetes. J Urol 181: 198-203.
188. Munoz A, Romain Z, Munch E, Gangitano D, Boone T, Smith C, Somogyi G (2009) Changes in purinergic and nitrergic sensory signals in female rats during early diabetes. Neurol Urodyn 28: 110-111.
189. Pinna C, Zanardo R, Puglisi L (2000) Prostaglandin-release impairment in the bladder epithelium of streptozotocin-induced diabetic rats. Eur J Pharmacol 388: 267-273.
190. Vlaskovska M, Kasakov L, Rong W, Bodin P, Bardini M, Cockayne DA, Ford AP, Burnstock G (2001) P2X3 knock-out mice reveal a major sensory role for urothelially released ATP. J Neurosci 21: 5670-5677.
191. Munoz A, Smith CP, Boone TB, Somogyi GT (2011) Overactive and underactive bladder dysfunction is reflected by alterations in urothelial ATP and NO release. Neurochem Int 58: 295-300.
192. Ayan S, Yildirim S, Ucar C, Sarioglu Y, Gültekin Y, Bütüner C (1999) Corporal reactivity to adenosine and prostaglandin E1 in alloxan-induced diabetic rabbit corpus cavernosum, and the effect of insulin therapy. BJU Int 83: 108-112.
193. Carneiro FS, Giachini FR, Lima VV, Carneiro ZN, Leite R, Inscho EW, Tostes RC, Webb RC (2008) Adenosine actions are preserved in corpus cavernosum from obese and type II diabetic db/db mouse. J Sex Med 5: 1156-1166.
194. Gür S, Öztürk B (2000) Altered relaxant responses to adenosine and adenosine 5′-triphosphate in the corpus cavernosum from men and rats with diabetes. Pharmacology 60: 105-112.
195. Calvert RC, Khan MA, Thompson CS, Mikhailidis DP, Burnstock G (2008) A functional study of purinergic signalling in the normal and pathological rabbit corpus cavernosum. BJU Int 101: 1043-1047.
196. Gür S, Kadowitz PJ, Abdel-Mageed AS, Kendirci M, Sikka SC, Burnstock G, Hellstrom WJG (2009) Management of erectile function by purinergic P2 receptors in diabetic rat. J Urol 181: 2382.
197. D'Amato M, Currò D (1990) Non-adrenergic non-cholinergic inhibitory innervation of the gastric fundus in streptozotocin-diabetic rats. Acta Physiol Hung 75(Suppl): 77-78.
198. Jenkinson KM, Reid JJ (2000) Altered non-adrenergic non-cholinergic neurotransmission in gastric fundus from streptozotocin-diabetic rats. Eur J Pharmacol 401: 251-258.
199. Belai A, Lefebvre RA, Burnstock G (1991) Motor activity and neurotransmitter release in the gastric fundus of streptozotocin-diabetic rats. Eur J Pharmacol 194: 225-234.
200. Jenkinson KM, Reid JJ (1995) Effect of diabetes on relaxations to non-adrenergic, non-cholinergic nerve stimulation in longitudinal muscle of the rat gastric fundus. Br J Pharmacol 116: 1551-1556.
201. Martinez-Cuesta MA, Massuda H, Whittle BJ, Moncada S (1995) Impairment of nitrergic-mediated relaxation of rat isolated duodenum by experimental diabetes. Br J Pharmacol 114: 919-924.
202. Hoyle CHV, Reilly WM, Lincoln J, Burnstock G (1988) Adrenergic, but not cholinergic or purinergic, responses are potentiated in the cecum of diabetic rats. Gastroenterology 94: 1357-1367.
203. Tahani H, Samia M, Rizk S, Habib YA, Tallaat M (1977) Effect of repeated doses of ATP on serum protein pattern and fat content of the liver in experimental diabetes. Z Ernährungswiss 16: 120-127.
204. Grden M, Podgorska M, Szutowicz A, Pawelczyk T (2007) Diabetes-induced alterations of adenosine receptors expression level in rat liver. Exp Mol Pathol 83: 392-398.
205. 2B receptor. J Med Chem 44: 170-179.
206. Liu IM, Tzeng TF, Tsai CC, Lai TY, Chang CT, Cheng JT (2003) Increase in adenosine A1 receptor gene expression in the liver of streptozotocin-induced diabetic rats. Diabetes Metab Res Rev 19: 209-215.
207. Hashimoto N, Robinson FW, Shibata Y, Flanagan JE, Kono T (1987) Diversity in the effects of extracellular ATP and adenosine on the cellular processing and physiologic actions of insulin in rat adipocytes. J Biol Chem 262: 15026-15032.
208. Camberos MC, Perez AA, Udrisar DP, Wanderley MI, Cresto JC (2001) ATP inhibits insulin-degrading enzyme activity. Exp Biol Med (Maywood) 226: 334-341.
209. Song ES, Juliano MA, Juliano L, Fried MG, Wagner SL, Hersh LB (2004) ATP effects on insulin-degrading enzyme are mediated primarily through its triphosphate moiety. J Biol Chem 279: 54216-54220.
210. Foley JE (1992) Rationale and application of fatty acid oxidation inhibitors in treatment of diabetes mellitus. Diabetes Care 15: 773-784.
211. Dong Q, Ginsberg HN, Erlanger BF (2001) Overexpression of the A1 adenosine receptor in adipose tissue protects mice from obesity-related insulin resistance. Diabetes Obes Metab 3: 360-366.
212. Cox BF, Clark KL, Perrone MH, Welzel GE, Greenland BD, Colussi DJ, Merkel LA (1997) Cardiovascular and metabolic effects of adenosine A1-receptor agonists in streptozotocin-treated rats. J Cardiovasc Pharmacol 29: 417-426.
213. Dhalla AK, Chisholm JW, Reaven GM, Belardinelli L (2009) A1 adenosine receptor: role in diabetes and obesity. Handb Exp Pharmacol 193: 271-295.
214. 1 adenosine receptors in diabetes treatment. Curr Pharm Des 16: 4237-4242.
215. Gharibi B, Abraham AA, Ham J, Evans BA (2012) Contrasting effects of A1 and A2b adenosine receptors on adipogenesis. Int J Obes (Lond) 36: 397-406.
216. Lee H, Jun DJ, Suh BC, Choi BH, Lee JH, Do MS, Suh BS, Ha H, Kim KT (2005) Dual roles of P2 purinergic receptors in insulin-stimulated leptin production and lipolysis in differentiated rat white adipocytes. J Biol Chem 280: 28556-28563.
217. 1 receptor supports leptin secretion in adipose tissue. Endocrinology 151: 2060-2070.
218. Yu Z, Jin T (2010) Extracellular high dosages of adenosine triphosphate induce inflammatory response and insulin resistance in rat adipocytes. Biochem Biophys Res Commun 402: 455-460.
219. Madec S, Rossi C, Chiarugi M, Santini E, Salvati A, Ferrannini E, Solini A (2011) Adipocyte P2X7 receptors expression: a role in modulating inflammatory response in subjects with metabolic syndrome? Atherosclerosis 219: 552-558.
220. 2+ signaling and membrane trafficking by multiple p2 receptors in brown adipocytes. J Membr Biol 207: 131-142.
221. Schmid AI, Szendroedi J, Chmelik M, Krssak M, Moser E, Roden M (2011) Liver ATP synthesis is lower and relates to insulin sensitivity in patients with type 2 diabetes. Diabetes Care 34: 448-453.
222. Minet AD, Gaster M (2010) ATP synthesis is impaired in isolated mitochondria from myotubes established from type 2 diabetic subjects. Biochem Biophys Res Commun 402: 70-74.
223. Thong FS, Lally JS, Dyck DJ, Greer F, Bonen A, Graham TE (2007) Activation of the A1 adenosine receptor increases insulin-stimulated glucose transport in isolated rat soleus muscle. Appl Physiol Nutr Metab 32: 701-710.
224. Challis RA, Budohoski L, McManus B, Newsholme EA (1984) Effects of an adenosine-receptor antagonist on insulin-resistance in soleus muscle from obese Zucker rats. Biochem J 221: 915-917.
225. 12 skeletal muscle cells. Arch Biochem Biophys 401: 205-214.
226. Mortensen SP, Gonzalez-Alonso J, Nielsen JJ, Saltin B, Hellsten Y (2009) Muscle interstitial ATP and norepinephrine concentrations in the human leg during exercise and ATP infusion. J Appl Physiol 107: 1757-1762.
227. Borno A, Ploug T, Bune LT, Rosenmeier JB, Thaning P (2012) Purinergic receptors expressed in human skeletal muscle fibres. Purinergic Signal 8: 255-264.
228. Ellis CG, Goldman D, Hanson M, Stephenson AH, Milkovich S, Benlamri A, Ellsworth ML, Sprague RS (2010) Defects in oxygen supply to skeletal muscle of prediabetic ZDF rats. Am J Physiol Heart Circ Physiol 298: H1661-H1670.
229. Sprague RS, Bowles EA, Achilleus D, Ellsworth ML (2011) Erythrocytes as controllers of perfusion distribution in the microvasculature of skeletal muscle. Acta Physiol (Oxf) 202: 285-292.
230. Bienso RS et al (2012) GLUT4 and glycogen synthase are key players in bed rest-induced insulin resistance. Diabetes 61: 1090-1099.
231. 2A receptors restores the altered cell-cycle machinery during impaired wound healing in genetically diabetic mice. Surgery 149: 253-261.
232. Wang J, Wan R, Mo Y, Li M, Zhang Q, Chien S (2010) Intracellular delivery of adenosine triphosphate enhanced healing process in full-thickness skin wounds in diabetic rabbits. Am J Surg 199: 823-832.
233. Yamauchi R, Kobayashi M, Matsuda Y, Ojika M, Shigeoka S, Yamamoto Y, Tou Y, Inoue T, Katagiri T, Murai A, Horio F (2010) Coffee and caffeine ameliorate hyperglycemia, fatty liver, and inflammatory adipocytokine expression in spontaneously diabetic KK-Ay mice. J Agric Food Chem 58: 5597-5603.
234. Fredholm BB, IJzerman AP, Jacobson KA, Linden J, Muller CE (2011) International Union of Basic and Clinical Pharmacology. LXXXI. Nomenclature and classification of adenosine receptors-an update. Pharmacol Rev 63: 1-34.
235. Muller CE, Jacobson KA (2011) Recent developments in adenosine receptor ligands and their potential as novel drugs. Biochim Biophys Acta 1808: 1290-1308.
236. Sone H, Sasaki Y, Komai M, Toyomizu M, Kagawa Y, Furukawa Y (2004) Biotin enhances ATP synthesis in pancreatic islets of the rat, resulting in reinforcement of glucose-induced insulin secretion. Biochem Biophys Res Commun 314: 824-829.