Dopamine modulates insulin release and is involved in the survival of rat pancreatic beta cells

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Barrado, Maria Jose Garcia ^a,b   Osma, Maria Carmen Iglesias ^a,b   Blanco, Enrique J ^a,b   Hernández, Marta Carretero ^a   Robledo, Virginia Sánchez ^a   Iniesta, Leonardo Catalano ^a   Carrero, Sixto ^b   Carretero, Jose ^a,b  

^a UNIVERSITY OF SALAMANCA   (Spain)

^b INSTITUTO DE INVESTIGACIÓN BIOMÉDICA DE SALAMANCA IBSAL   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CYCLINE; DOPAMINE; GLUCOSE; INSULIN;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL LABELING; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DOPAMINE METABOLISM; DOPAMINERGIC ACTIVITY; IMMUNOCYTOCHEMISTRY; INSULIN RELEASE; MALE; METABOLIC REGULATION; NONHUMAN; PANCREAS ISLET BETA CELL; RAT; ANIMAL; DRUG EFFECTS; PANCREAS ISLET; SECRETION (PROCESS); WISTAR RAT;

RATTUS; RATTUS NORVEGICUS;

ANIMALS; APOPTOSIS; CELL PROLIFERATION; CELL SURVIVAL; DOPAMINE; GLUCOSE; INSULIN; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS; MALE; RATS; RATS, WISTAR;

EID: 84928815070     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0123197     Document Type: Article

References (49)

1. Callier S, Snapyan M, Le Crom S, Prou D, Vincent JD, Vernier P. Evolution and cell biology of dopamine receptors in vertebrates. Biol Cell. 2003; 95(7):489-502. Epub 2003/11/05. PMID: 14597267.
2. Kitamura T, Kitamura Y, Kuroda S, Hino Y, Ando M, Kotani K, et al. Insulin-induced phosphorylation and activation of cyclic nucleotide phosphodiesterase 3B by the serine-threonine kinase Akt. Mol Cell Biol. 1999; 19(9):6286-96. Epub 1999/08/24. PMID: 10454575; PubMed Central PMCID: PMC84592.
3. Ahren B, Lundquist I. Effects of L-dopa-induced dopamine accumulation on 45Ca2+ efflux and insulin secretion in isolated rat islets. Pharmacology. 1985; 30(2):71-82. Epub 1985/01/01. PMID: 3883370.
4. Kvist-Reimer M, Sundler F, Ahren B. Effects of chemical sympathectomy by means of 6-hydroxydopamine on insulin secretion and islet morphology in alloxan-diabetic mice. Cell and tissue research. 2002; 307(2):203-9. Epub 2002/02/15. doi: 10.1007/s00441-001-0496-5 PMID: 11845327.
5. Rosati G, Maioli M, Aiello I, Farris A, Agnetti V. Effects of long-term L-dopa therapy on carbohydrate metabolism in patients with Parkinson's disease. European neurology. 1976; 14(3):229-39. Epub 1976/01/01. PMID: 1278195.
6. Driver JA, Smith A, Buring JE, Gaziano JM, Kurth T, Logroscino G. Prospective cohort study of type 2 diabetes and the risk of Parkinson's disease. Diabetes Care. 2008; 31(10):2003-5. doi: 10.2337/dc08-0688 PMID: 18599528; PubMed Central PMCID: PMC2551644.
7. Ericson LE, Hakanson R, Lundquist I. Accumulation of dopamine in mouse pancreatic B-cells following injection of L-DOPA. Localization to secretory granules and inhibition of insulin secretion. Diabetologia. 1977; 13(2):117-24. Epub 1977/04/01. PMID: 404204.
8. Zern RT, Bird JL, Feldman JM. Effect of increased pancreatic islet norepinephrine, dopamine and serotonin concentration on insulin secretion in the golden hamster. Diabetologia. 1980; 18(4):341-6. Epub 1980/04/01. PMID: 6998806.
9. Arneric SP, Long JP, Williams M, Goodale DB, Mott J, Lakoski JM, et al. RDS-127 (2-di-n-propylamino-4,7-dimethoxyindane): central effects of a new dopamine receptor agonist. The Journal of pharmacology and experimental therapeutics. 1983; 224(1):161-70. Epub 1983/01/01. PMID: 6401334.
10. Shankar E, Santhosh KT, Paulose CS. Dopaminergic regulation of glucose-induced insulin secretion through dopamine D2 receptors in the pancreatic islets in vitro. IUBMB Life. 2006; 58(3):157-63. Epub 2006/06/13. doi: 10.1080/15216540600687993 PMID: 16766383.
11. Henquin JC. Triggering and amplifying pathways of regulation of insulin secretion by glucose. Diabetes. 2000; 49(11):1751-60. PMID: 11078440.
12. Simpson N, Maffei A, Freeby M, Burroughs S, Freyberg Z, Javitch J, et al. Dopamine-mediated autocrine inhibitory circuit regulating human insulin secretion in vitro. Mol Endocrinol. 2012; 26(10):1757-72. doi: 10.1210/me.2012-1101 PMID: 22915827; PubMed Central PMCID: PMC3458225.
13. Rubi B, Ljubicic S, Pournourmohammadi S, Carobbio S, Armanet M, Bartley C, et al. Dopamine D2-like receptors are expressed in pancreatic beta cells and mediate inhibition of insulin secretion. The Journal of biological chemistry. 2005; 280(44):36824-32. Epub 2005/09/01. doi: 10.1074/jbc.M505560200 PMID: 16129680.
14. Ustione A, Piston DW. Dopamine synthesis and D3 receptor activation in pancreatic beta-cells regulates insulin secretion and intracellular [Ca(2+)] oscillations. Molecular endocrinology. 2012; 26 (11):1928-40. Epub 2012/08/25. doi: 10.1210/me.2012-1226 PMID: 22918877; PubMed Central PMCID: PMC3487623.
15. Borelli MI, Gagliardino JJ. Possible modulatory effect of endogenous islet catecholamines on insulin secretion. BMC Endocr Disord. 2001; 1(1):1. Epub 2001/11/07. PMID: 11696250; PubMed Central PMCID: PMC59668.
16. Borelli MI, Rubio M, Garcia ME, Flores LE, Gagliardino JJ. Tyrosine hydroxylase activity in the endocrine pancreas: changes induced by short-term dietary manipulation. BMC Endocr Disord. 2003; 3 (1):2. Epub 2003/03/28. PMID: 12659644; PubMed Central PMCID: PMC153518.
17. Raffo A, Hancock K, Polito T, Xie Y, Andan G, Witkowski P, et al. Role of vesicular monoamine transporter type 2 in rodent insulin secretion and glucose metabolism revealed by its specific antagonist tetrabenazine. The Journal of endocrinology. 2008; 198(1):41-9. Epub 2008/06/26. doi: 10.1677/JOE-07-0632 PMID: 18577569; PubMed Central PMCID: PMC2712213.
18. Sakano D, Shiraki N, Kikawa K, Yamazoe T, Kataoka M, Umeda K, et al. VMAT2 identified as a regulator of late-stage beta-cell differentiation. Nature chemical biology. 2014; 10(2):141-8. Epub 2013/12/10. doi: 10.1038/nchembio.1410 PMID: 24316738.
19. de Leeuw van Weenen JE, Parlevliet ET, Maechler P, Havekes LM, Romijn JA, Ouwens DM, et al. The dopamine receptor D2 agonist bromocriptine inhibits glucose-stimulated insulin secretion by direct activation of the alpha2-adrenergic receptors in beta cells. Biochemical pharmacology. 2010; 79 (12):1827-36. Epub 2010/02/09. doi: 10.1016/j.bcp.2010.01.029 PMID: 20138024.
20. Garcia-Tornadu I, Ornstein AM, Chamson-Reig A, Wheeler MB, Hill DJ, Arany E, et al. Disruption of the dopamine d2 receptor impairs insulin secretion and causes glucose intolerance. Endocrinology. 2010; 151(4):1441-50. Epub 2010/02/12. doi: 10.1210/en.2009-0996 PMID: 20147524.
21. Garcia-Tornadu I, Perez-Millan MI, Recouvreux V, Ramirez MC, Luque G, Risso GS, et al. New insights into the endocrine and metabolic roles of dopamine D2 receptors gained from the Drd2 mouse. Neuroendocrinology. 2010; 92(4):207-14. Epub 2010/10/27. doi: 10.1159/000321395 PMID: 20975260.
22. Chen Y, Hong F, Chen H, Fan RF, Zhang XL, Zhang Y, et al. Distinctive expression and cellular distribution of dopamine receptors in the pancreatic islets of rats. Cell and tissue research. 2014. Epub 2014/05/16. doi: 10.1007/s00441-014-1894-9 PMID: 24825414.
23. Iwatsubo K, Suzuki S, Li C, Tsunematsu T, Nakamura F, Okumura S, et al. Dopamine induces apoptosis in young, but not in neonatal, neurons via Ca2+-dependent signal. American journal of physiology Cell physiology. 2007; 293(5):C1498-508. doi: 10.1152/ajpcell.00088.2007 PMID: 17804610.
24. Garcia-Barrado MJ, Ravier MA, Rolland JF, Gilon P, Nenquin M, Henquin JC. Inhibition of protein synthesis sequentially impairs distinct steps of stimulus-secretion coupling in pancreatic beta cells. Endocrinology. 2001; 142(1):299-307. doi: 10.1210/endo.142.1.7910 PMID: 11145593.
25. Carretero J, Angoso M, Rubio M, Blanco EJ, Sierra E, Herrero JJ, et al. In vitro immunoblockade of VIP inhibits the proliferation of pituitary prolactin cells. Anatomy and embryology. 2006; 211(1):11-8. doi: 10.1007/s00429-005-0058-9 PMID: 16328361.
26. Debuyser A, Drews G, Henquin JC. Adrenaline inhibition of insulin release: role of cyclic AMP. Molecular and cellular endocrinology. 1991; 78(3):179-86. PMID: 1663876.
27. Peterhoff M, Sieg A, Brede M, Chao CM, Hein L, Ullrich S. Inhibition of insulin secretion via distinct signaling pathways in alpha2-adrenoceptor knockout mice. European journal of endocrinology / European Federation of Endocrine Societies. 2003; 149(4):343-50. PMID: 14514350.
28. Ruffolo RR Jr., Nichols AJ, Hieble JP. Metabolic regulation by alpha 1- and alpha 2-adrenoceptors. Life sciences. 1991; 49(3):171-83. PMID: 1648157.
29. Szollosi A, Nenquin M, Henquin JC. Pharmacological stimulation and inhibition of insulin secretion in mouse islets lacking ATP-sensitive K+ channels. British journal of pharmacology. 2010; 159(3):669-77. Epub 2010/02/05. doi: 10.1111/j.1476-5381.2009.00588.x PMID: 20128805; PubMed Central PMCID: PMC2828030.
30. Bonner-Weir S. Life and death of the pancreatic beta cells. Trends in endocrinology and metabolism: TEM. 2000; 11(9):375-8. PMID: 11042468.
31. Butler AE, Janson J, Soeller WC, Butler PC. Increased beta-cell apoptosis prevents adaptive increase in beta-cell mass in mouse model of type 2 diabetes: evidence for role of islet amyloid formation rather than direct action of amyloid. Diabetes. 2003; 52(9):2304-14. PMID: 12941770.
32. Carretero J, Sanchez F, Rubio M, Francos CM, Blanco J, Vazquez R. In vitro and in vivo evidence for direct dopaminergic inhibition of VIP-immunoreactive pituitary cells. Neuropeptides. 1994; 27(1):1-6. PMID: 7969815.
33. Oliver-Krasinski JM, Stoffers DA. On the origin of the beta cell. Genes & development. 2008; 22 (15):1998-2021. doi: 10.1101/gad.1670808 PMID: 18676806; PubMed Central PMCID: PMC2735346.
34. Vazquez P, Robles AM, de Pablo F, Hernandez-Sanchez C. Non-neural tyrosine hydroxylase, via modulation of endocrine pancreatic precursors, is required for normal development of beta cells in the mouse pancreas. Diabetologia. 2014; 57(11):2339-47. doi: 10.1007/s00125-014-3341-6 PMID: 25082160; PubMed Central PMCID: PMC4181516.
35. Jetton TL, Liang Y, Cincotta AH. Systemic treatment with sympatholytic dopamine agonists improves aberrant beta-cell hyperplasia and GLUT2, glucokinase, and insulin immunoreactive levels in ob/ob mice. Metabolism: clinical and experimental. 2001; 50(11):1377-84. Epub 2001/11/08. doi: 10.1053/meta.2001.26741 PMID: 11699060.
36. Milburn JL Jr, Hirose H, Lee YH, Nagasawa Y, Ogawa A, Ohneda M, et al. Pancreatic beta-cells in obesity. Evidence for induction of functional, morphologic, and metabolic abnormalities by increased long chain fatty acids. The Journal of biological chemistry. 1995; 270(3):1295-9. PMID: 7836394.
37. Fleenor DE, Freemark M. Prolactin induction of insulin gene transcription: roles of glucose and signal transducer and activator of transcription 5. Endocrinology. 2001; 142(7):2805-10. doi: 10.1210/endo.142.7.8267 PMID: 11415999.
38. Los M, Wesselborg S, Schulze-Osthoff K. The role of caspases in development, immunity, and apoptotic signal transduction: lessons from knockout mice. Immunity. 1999; 10(6):629-39. PMID: 10403638.
39. Choi D, Woo M. Executioners of apoptosis in pancreatic {beta}-cells: not just for cell death. American journal of physiology Endocrinology and metabolism. 2010; 298(4):E735-41. Epub 2009/12/24. doi: 10.1152/ajpendo.00696.2009 PMID: 20028968.
40. Bensellam M, Laybutt DR, Jonas JC. The molecular mechanisms of pancreatic beta-cell glucotoxicity: recent findings and future research directions. Molecular and cellular endocrinology. 2012; 364(1-2):1-27. Epub 2012/08/14. doi: 10.1016/j.mce.2012.08.003 PMID: 22885162.
41. Cnop M, Welsh N, Jonas JC, Jorns A, Lenzen S, Eizirik DL. Mechanisms of pancreatic beta-cell death in type 1 and type 2 diabetes: many differences, few similarities. Diabetes. 2005; 54 Suppl 2:S97-107. Epub 2005/11/25. PMID: 16306347.
42. Van de Casteele M, Kefas BA, Cai Y, Heimberg H, Scott DK, Henquin JC, et al. Prolonged culture in low glucose induces apoptosis of rat pancreatic beta-cells through induction of c-myc. Biochemical and biophysical research communications. 2003; 312(4):937-44. Epub 2003/12/04. PMID: 14651961.
43. Butler AE, Janson J, Bonner-Weir S, Ritzel R, Rizza RA, Butler PC. Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes. 2003; 52(1):102-10. PMID: 12502499.
44. Weir GC, Marselli L, Marchetti P, Katsuta H, Jung MH, Bonner-Weir S. Towards better understanding of the contributions of overwork and glucotoxicity to the beta-cell inadequacy of type 2 diabetes. Diabetes, obesity & metabolism. 2009; 11 Suppl 4:82-90. doi: 10.1111/j.1463-1326.2009.01113.x PMID: 19817791.
45. Jonas JC, Sharma A, Hasenkamp W, Ilkova H, Patane G, Laybutt R, et al. Chronic hyperglycemia triggers loss of pancreatic beta cell differentiation in an animal model of diabetes. The Journal of biological chemistry. 1999; 274(20):14112-21. Epub 1999/05/13. PMID: 10318828.
46. Jiang JL, Peng YP, Qiu YH, Wang JJ. Effect of endogenous catecholamines on apoptosis of Con A-activated lymphocytes of rats. Journal of neuroimmunology. 2007; 192(1-2):79-88. doi: 10.1016/j.jneuroim.2007.09.012 PMID: 17920695.
47. Putinski C, Abdul-Ghani M, Stiles R, Brunette S, Dick SA, Fernando P, et al. Intrinsic-mediated caspase activation is essential for cardiomyocyte hypertrophy. Proc Natl Acad Sci U S A. 2013; 110(43):E4079-87. doi: 10.1073/pnas.1315587110 PMID: 24101493; PubMed Central PMCID: PMC3808644.
48. Radl DB, Ferraris J, Boti V, Seilicovich A, Sarkar DK, Pisera D. Dopamine-induced apoptosis of lactotropes is mediated by the short isoform of D2 receptor. PLoS One. 2011; 6(3):e18097. doi: 10.1371/journal.pone.0018097 PMID: 21464994; PubMed Central PMCID: PMC3064585.
49. Ustione A, Piston DW, Harris PE. Minireview: Dopaminergic regulation of insulin secretion from the pancreatic islet. Molecular endocrinology. 2013; 27(8):1198-207. Epub 2013/06/08. doi: 10.1210/me.2013-1083 PMID: 23744894; PubMed Central PMCID: PMC3725340.