Молекулярные механизмы секреции инсулина β-клетками островков Лангерганса и перспективные мишени фармакологического воздействия для лечения сахарного диабета
Аннотация
Информация о молекулярных механизмах секреции инсулина β-клетками островков Лангерганса имеет первостепенное значение в понимании молекулярного патогенеза сахарного диабета и является фундаментальной основой для разработки современных фармацевтических средств патогенетической терапии сахарного диабета и его осложнений. В обзоре представлены современные данные в области изучения молекулярно-биологических аспектов регуляции секреции инсулина и обсуждаются перспективные мишени для фармакотерапии сахарного диабета.
Ключевые слова
Об авторах
Владимир Владимирович ШаройкоРоссия
ШАРОЙКО Владимир Владимирович – д.б.н., в.н.с.;
Татьяна Борисовна Тенникова
Россия
ТЕННИКОВА Татьяна Борисовна – д.х.н., проф., г.н.с.
Список литературы
1. Zimmet P., Alberti K. G.,Shaw J. (2001). Global and societal implications of the diabetes epidemic. Nature. 414, 782 – 787.
2. IDF Diabetes Atlas, 6th edition, 2014.
3. Государственный регистр больных сахарным диабетом, 2009.
4. Suckale J.,Solimena M. (2008). Pancreas islets in metabolic signaling-focus on the beta-cell. Front Biosci. 13, 7156 – 7171.
5. Elayat A.A., el-Nagga M.M., Tahir M. (1995). Animmunocytochemical and morphometric study of the rat pancreatic islets. J Anat. 186 ( Pt 3), 629 – 637.
6. Raphaël Scharfmann, Xiangwei Xiao, Harry Heimberg et al. (2008). Beta cells within single human islets originate from multiple progenitors. PLoS ONE, 3(10).
7. De Vos A., H. Heimberg et al. (1995). Human and rat beta cells differ in glucose transporter but not in glucokinase gene expression. The Journal of Clinical Investigation 96(5): 2489 – 2495.
8. Henquin J. C. (2009). Regulation of insulin secretion: a matter of phase control and amplitude modulation. Diabetologia. 52, 739 – 751.
9. LeRoith D. (2002). Beta-cell dysfunction and insulin resistance in type 2 diabetes: role of metabolic and genetic abnormalities. Am J Med. 113 Suppl 6A, 3S – 11S.
10. Hedeskov C. J. (1980). Mechanism of glucoseinduced insulin secretion. Physiol Rev. 60, 442 – 509.
11. Hedeskov C. J., Capito K. (1980). Pancreatic islet metabolism of pyruvate and other potentiators of insulin release. Effects of starvation. HormMetab Res Suppl. Suppl 10, 8 – 13.
12. Ashcroft F. M., Harrison D. E., Ashcroft S. J. (1984). Glucose induces closure of single potassium channels in isolated rat pancreatic beta-cells. Nature. 312, 446 – 448.
13. Arkhammar P., Nilsson T., Rorsman P. et al. (1987). Inhibition of ATP-regulated K+ channels precedes depolarization-induced increase in cytoplasmic free Ca2+ concentration in pancreatic beta-cells. The Journal of biological chemistry. 262, 5448–5454.
14. Gembal M., Detimary P., Gilon P. et al. (1993). Mechanisms by which glucose can control insulin release independently from its action on adenosine triphosphate-sensitive K+ channels in mouse B cells. J Clin Invest. 91, 871–880.
15. Steiner D.F., Spigelman L., Aten B. Insulin Biosynthesis: Evidence for a Precursor. Science. 1967; 157: 697–700.
16. The clinical potential of C-peptide replacement in type 1 diabetes.Wahren J., Kallas A., Sima A.A. Diabetes. 2012 Apr; 61(4): 761–772.
17. C-peptide preserves the renal microvascular architecture in the streptozotocin-induced diabeticrat. Flynn E.R., Lee J., Hutchens Z.M. Jr, et al. Diabetes Complications. 2013 Nov-Dec; 27(6): 538–547.
18. Impact of C-peptide preservation on metabolic and clinical outcomes in the Diabetes Control and Complications Trial. Lachin J.M., McGee P., Palmer J.P.; DCCT/EDIC Research Group. Diabetes. 2014 Feb; 63(2): 739–748.
19. Luppi P., Cifarelli V., Tse H. et al. Human Cpeptide antagonises high glucose-induced endothelial dysfunction through the nuclear factor-kappaB pat way. Diabetologia. 2008 Aug;51(8):1534–1543.
20. Mughal R..S, Scragg J.L., Lister P. et al. Cellular mechanisms by which proinsulin C-peptide prevents insulin-induced neointima formation in human saphenous vein. Diabetologia. 2010 Aug; 53(8): 1761–1771.
21. Haidet J., Cifarelli V., Trucco M., Luppi P. (2012). C-peptide reduces pro-inflammatory cytokine secretion in LPS-stimulated U937 monocytes in condition of hyperglycemia. Inflamm. Res. 61: 27–35.
22. Detimary P., Jonas J. C., Henquin J. C. (1996). Stable and diffusible pools of nucleotides in pancreatic islet cells. Endocrinology. 137, 4671–4676.
23. Sato Y., Henquin J. C. (1998). The K+-ATP channel-independent pathway of regulation of insulin secretion by glucose: in search of the underlying mechanism. Diabetes. 47, 1713–1721.
24. Seino S., Takahashi H., Fujimoto W., Shibasaki
25. T. (2009). Roles of cAMPsignalling in insulin granule exocytosis. Diabetes ObesMetab. 11 Suppl 4, 180–218.
26. Kashima Y., Miki T., Shibasaki T. et al. (2001). Critical role of cAMP-GEFII--Rim2 complex in incretinpotentiated insulin secretion. J Biol Chem. 276, 46046–4605.
27. Seino S., Shibasaki T. (2005). PKA-dependent and PKA-independent pathways for cAMP-regulated exocytosis. Physiol Rev. 85, 1303–1342.
28. Song K., Zhang X., Zhao C. et al. (2005). Inhibition of Ca2+-independent phospholipase A2 results in insufficient insulin secretion and impaired glucose tolerance. MolEndocrinol. 19, 504–515.
29. Thams P., Capito K., Hedeskov C. J. and Kofod
30. H. (1990). Phorbol-ester-induced down-regulation of protein kinase C in mouse pancreatic islets. Potentiation of phase 1 and inhibition of phase 2 of glucose-induced insulin secretion. Biochem J. 265, 777–787.
31. Prentki M. (1996). New insights into pancreatic beta-cell metabolic signaling in insulin secretion. Eur J Endocrinol. 134, 272–286.
32. Maechler P., Wollheim C. B. (1999). Mitochondrial glutamate acts as a messenger in glucose-induced insulin exocytosis. Nature. 402, 685–689.
33. Khan A., Ling Z. C. and Landau B. R. (1996). Quantifying the carboxylation of pyruvate in pancreatic islets. The Journal of biological chemistry. 271, 2539–2542.
34. MacDonald M. J. (1995). Feasibility of a mitochondrial pyruvate malate shuttle in pancreatic islets. Further implication of cytosolic NADPH in insulin secretion. J Biol Chem. 270, 20051–20058.
35. Brun T., Roche E., Assimacopoulos-Jeannet F. et al. (1996). Evidence for an anaplerotic/malonyl-CoA pathway in pancreatic beta-cell nutrient signaling. Diabetes. 45, 190–198.
36. Deeney J. T., Gromada J., Hoy M. et al. (2000). Acute stimulation with long chain acyl-CoA enhances exocytosis in insulin-secreting cells (HIT T-15 and NMRI beta-cells). J Biol Chem. 275, 9363–9368.
37. Yamada S., Komatsu M., Sato Y. et al. (2003). Nutrient modulation of palmitoylated 24-kilodalton protein in rat pancreatic islets. Endocrinology. 144, 5232–5241.
38. Chapman E. R., Blasi J., An S., Brose N. et al. (1996). Fatty acylation of synaptotagmin in PC12 cells and synaptosomes. BiochemBiophys Res Commun. 225, 326–332.
39. Gonzalo S., Greentree W. K. and Linder M. E. (1999). SNAP-25 is targeted to the plasma membrane through a novel membrane-binding domain. J Biol Chem. 274, 21313–21318.
40. Straub S. G. and Sharp G. W. (2007). Inhibition of insulin secretion by cerulenin might be due to impaired glucose metabolism. Diabetes Metab Res Rev. 23, 146–151.
41. Antinozzi P. A., Segall L., Prentki M. et al. (1998). Molecular or pharmacologic perturbation of the link between glucose and lipid metabolism is without effect on glucose-stimulated insulin secretion. A reevaluation of the long-chain acyl-CoA hypothesis. J Biol Chem. 273, 16146–16154.
42. Mulder H., Lu D., Finley J. T. et al. (2001). Overexpression of a modified human malonyl-CoA decarboxylase blocks the glucose-induced increase in malonyl-CoA level but has no impact on insulin secretion in INS-1-derived (832/13) beta-cells. J Biol Chem. 276, 6479–6484.
43. MacDonald P. E., El-Kholy W., Riedel M. J. et al. (2002). The multiple actions of GLP-1 on the process of glucose-stimulated insulin secretion. Diabetes. 51 Suppl 3, S434–442.
44. Zawalich W. S. and Rasmussen H. (1990). Control of insulin secretion: a model involving Ca2+, cAMP and diacylglycerol. Mol Cell Endocrinol. 70, 119–137.
45. Holz G. G. (2004). Epac: A new cAMP-binding protein in support of glucagon-like peptide-1 receptormediated signal transduction in the pancreatic beta-cell. Diabetes. 53, 5–13.
46. McClenaghan N. H., Flatt P. R. and Ball A. J. (2006). Actions of glucagon-like peptide-1 on KATP channel-dependent and -independent effects of glucose, sulphonylureas and nateglinide. J Endocrinol. 190, 889–896.
47. Holz G. G. (2004). New insights concerning the glucose-dependent insulin secretagogue action of glucagon-like peptide-1 in pancreatic beta-cells. HormMetab Res. 36, 787–794.
48. Akiba S. and Sato T. (2004). Cellular function of calcium-independent phospholipase A2. Biol Pharm Bull. 27, 1174–1178.
49. Ramanadham S., Song H., Bao S. et al. (2004). Islet complex lipids: involvement in the actions of group VIA calcium-independent phospholipase A(2) in betacells. Diabetes. 53 Suppl 1, S179–185.
50. Jenkins C.M., Cedars A., Gross R.W. Eicosanoid signalling pathways in the heart.Cardiovasc Res. 2009 May 1; 82(2): 240–249. Review.
51. Chakraborti S. (2003). Phospholipase A(2) isoforms: a perspective. Cell Signal. 15, 637–665.
52. Wolf B.A., Pasquale S.M. and Turk J. (1991). Free fatty acid accumulation in secretagogue-stimulated pancreatic islets and effects of arachidonate on depolarization-induced insulin secretion. Biochemistry. 30, 6372–6379.
53. Persaud S. J., Muller D., Belin V. D. et al. (2007). The role of arachidonic acid and its metabolites in insulin secretion from human islets of langerhans. Diabetes. 56, 197–203.
54. Sharoyko V.V., Zaitseva I.I., Leibiger B. et al. Arachidonic acid signaling is involved in the mechanism of imidazoline-induced KATP channel-independent stimulation of insulin secretion. Cell Mol Life Sci. 2007 Nov; 64(22): 2985–2993.
55. Krus U., Kotova O., Spégel P. et al. Pyruvate dehydrogenase kinase 1 controls mitochondrial metabolism and insulin secretion in INS-1 832/13 clonal beta-cells. Biochem J. 2010 Jul 1; 429(1): 205–213.
56. Malmgren S., Nicholls D. G., Taneera J. et al. (2009). Tight coupling between glucose and mitochondrial metabolism in clonal beta-cells is required for robust insulin secretion. The Journal of biological chemistry. 284, 32395–32404.
57. Schuit F., De Vos A., Farfari S. et al. (1997). Metabolic fate of glucose in purified islet cells. Glucoseregulated anaplerosis in beta cells. The Journal of biological chemistry. 272, 18572–18579.
58. Hasan N. M., Longacre M. J., Stoker S. W. et al. (2008). Impaired anaplerosis and insulin secretion in insulinoma cells caused by small interfering RNAmediated suppression of pyruvate carboxylase. The Journal of biological chemistry. 283, 28048–28059.
59. Sugden M. C. and Holness M. J. (2003). Recent advances in mechanisms regulating glucose oxidation at the level of the pyruvate dehydrogenase complex by PDKs. Am J PhysiolEndocrinolMetab. 284, E855–862.
60. Gudi R., Bowker-Kinley M. M., Kedishvili N. Y. et al. (1995). Diversity of the pyruvate dehydrogenase kinase gene family in humans. The Journal of biological chemistry. 270, 28989–28994.
61. Nicholls L. I., Ainscow E. K. and Rutter G. A. (2002). Glucose-stimulated insulin secretion does not require activation of pyruvate dehydrogenase: impact of adenovirus-mediated overexpression of PDH kinase and PDH phosphate phosphatase in pancreatic islets. Biochemical and biophysical research communications. 291, 1081–1088.
62. Xu J., Han J., Epstein P. N. and Liu Y. Q. (2006). Regulation of PDK mRNA by high fatty acid and glucose in pancreatic islets. Biochemical and biophysical research communications. 344, 827–833.
63. Cline G. W., Lepine R. L., Papas K. K. et al. (2004). 13C NMR isotopomer analysis of anaplerotic pathways in INS-1 cells. The Journal of biological chemistry. 279, 44370–44375.
64. Sugden M. C., Bulmer K., Augustine D. and Holness M. J. (2001). Selective modification of pyruvate dehydrogenase kinase isoform expression in rat pancreatic islets elicited by starvation and activation of peroxisome proliferator-activated receptor-alpha: implications for glucose-stimulated insulin secretion. Diabetes. 50, 2729–2736.
65. Goto Y., Nonaka I. and Horai S. (1990). A mutation in the tRNA(Leu)(UUR) gene associated with the MELAS subgroup of mitochondrial encephalomyopathies. Nature. 348, 651–653.
66. Reardon W., Ross R. J., Sweeney M. G. et al. (1992). Diabetes mellitus associated with a pathogenic point mutation in mitochondrial DNA. Lancet. 340, 1376–1379.
67. van den Ouweland J. M., Lemkes H. H., Ruitenbeek W. et al. (1992). Mutation in mitochondrial tRNA(Leu)(UUR) gene in a large pedigree with maternally transmitted type II diabetes mellitus and deafness. Nat Genet. 1, 368–371.
68. Silva J. P., Kohler M., Graff C. et al. (2000). Impaired insulin secretion and beta-cell loss in tissuespecific knockout mice with mitochondrial diabetes. Nat Genet. 26, 336–340.
69. Ronn T., Poulsen P., Tuomi T. et al. (2009). Genetic variation in ATP5O is associated with skeletal muscle ATP50 mRNA expression and glucose uptake in young twins. PLoS ONE. 4, e4793.
70. Scarpulla R. C. (2008). Transcriptional paradigms in mammalian mitochondrial biogenesis and function. Physiol Rev. 88, 611–638.
71. Metodiev M. D., Lesko N., Park C. B. et al. (2009). Methylation of 12S rRNA is necessary for in vivo stability of the small subunit of the mammalian mitochondrial ribosome. Cell Metab. 9, 386–397.
72. Koeck T., Olsson A.H., Nitert M.D. et al. A common variant in TFB1M is associated with reduced insulin secretion and increased future risk of type 2 diabetes. Cell Metab. 2011 Jan 5; 13(1): 80–91.
73. Sharoyko V.V., Abels M., Sun J. et al. Loss of TFB1M results in mitochondrial dysfunction that leads to impaired insulin secretion and diabetes. Hum Mol Genet. 2014 Nov 1; 23(21): 5733–5749.
Рецензия
Для цитирования:
Шаройко В.В., Тенникова Т.Б. Молекулярные механизмы секреции инсулина β-клетками островков Лангерганса и перспективные мишени фармакологического воздействия для лечения сахарного диабета. Природные ресурсы Арктики и Субарктики. 2015;20(2):90-97.
For citation:
Шаройко В.В., Тенникова Т.Б. Молекулярные механизмы секреции инсулина β-клетками островков Лангерганса и перспективные мишени фармакологического воздействия для лечения сахарного диабета. Arctic and Subarctic Natural Resources. 2015;20(2):90-97. (In Russ.)