Vagal control of pancreatic β-cell proliferation

American Journal of Physiology - Endocrinology and Metabolism

Volumn 299, Issue 5, 2010, Pages

  Lausier, James ^a   Diaz, William C ^a   Roskens, Violet ^a   LaRock, Kyla ^a   Herzer, Kristi ^a   Fong, Christopher G ^a   Latour, Martin G ^b   Peshavaria, Mina ^a   Jetton, Thomas L ^a  

^a UNIVERSITY OF VERMONT   (United States)

^b Montreal Diabetes Research Center   (Canada)

Author keywords

cell mass; Celiac vagotomy

Indexed keywords

GLUCAGON LIKE PEPTIDE 1; PROTEIN KINASE B; INSULIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CELL PROLIFERATION; CONTROLLED STUDY; FOOD INTAKE; GLUCOSE TOLERANCE; IN VITRO STUDY; INSULIN RELEASE; MALE; METABOLIC PARAMETERS; MORPHOMETRICS; NONHUMAN; PANCREAS ISLET BETA CELL; PARASYMPATHETIC NERVE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; RAT; VAGUS NERVE; ANIMAL; APOPTOSIS; BLOOD; BODY WEIGHT; CELL GROWTH; CONFOCAL MICROSCOPY; DRINKING; EATING; GLUCOSE BLOOD LEVEL; GLUCOSE TOLERANCE TEST; PHYSIOLOGY; SPRAGUE DAWLEY RAT; ULTRASTRUCTURE;

ANIMALS; APOPTOSIS; BLOOD GLUCOSE; BODY WEIGHT; CELL GROWTH PROCESSES; DRINKING; EATING; GLUCAGON-LIKE PEPTIDE 1; GLUCOSE TOLERANCE TEST; INSULIN; INSULIN-SECRETING CELLS; MALE; MICROSCOPY, CONFOCAL; RATS; RATS, SPRAGUE-DAWLEY; VAGUS NERVE;

EID: 78349297587     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00202.2010     Document Type: Article

References (48)

1. Avellar MC, Lázari MF, Porto CS. Expression and function of Gprotein- coupled receptors in the male reproductive tract. An Acad Bras Cienc 81: 321-344, 2009.
2. Balcazar N, Sathyamurthy A, Elghazi L, Gould A, Weiss A, Shiojima I, Walsh K, Bernal-Mizrachi E. mTORC1 activation regulates beta-cell mass and proliferation by modulation of cyclin D2 synthesis and stability. J Biol Chem 284: 7832-7842, 2009.
3. Bereiter DA, Rohner-Jeanrenaud F, Berthoud HR, Jeanrenaud B. CNS modulation of pancreatic endocrine function. Multiple modes of expression. Diabetologia 20 Suppl: 417-425, 1981.
4. Bloom SR, Edwards AV, Hardy RN. The role of the autonomic nervous system in the control of glucagon, insulin and pancreatic polypeptide release from the pancreas. J Physiol 280: 9-23, 1978. (Pubitemid 8398555)
5. Bonner-Weir S. Islet growth and development in the adult. J Mol Endocrinol 24: 297-302, 2000.
6. Buijs RM, Chun SJ, Niijima A, Romijn HJ, Nagai K. Parasympathetic and sympathetic control of the pancreas: a role for the suprachiasmatic nucleus and other hypothalamic centers that are involved in the regulation of food intake. J Comp Neurol 431: 405-423, 2001. (Pubitemid 32178945)
7. Burris RE, Hebrok M. Pancreatic innervation in mouse development and beta-cell regeneration. Neuroscience 150: 592-602, 2007. (Pubitemid 350198741)
8. Das VA, Robinson R, Paulose CS. Enhanced β-adrenergic receptors in the brain and pancreas during pancreatic regeneration in weanling rats. Mol Cell Biochem 289: 11-19, 2006. (Pubitemid 44322470)
9. Dixon KD, Williams FE, Wiggins RL, Pavelka J, Lucente J, Bellinger LL, Gietzen DW. Differential effects of selective vagotomy and tropisetron in aminoprivic feeding. Am J Physiol Regul Integr Comp Physiol 279: R997-R1009, 2000.
10. Dor Y, Brown J, Martinez OI, Melton DA. Adult pancreatic beta-cells are formed by self-duplication rather than stem-cell differentiation. Nature 429: 41-46, 2004. (Pubitemid 38620543)
11. Dor Y. beta-Cell proliferation is the major source of new pancreatic beta cells. Nat Clin Pract Endocrinol Metab 2: 242-243, 2006.
12. Duttaroy A, Zimliki CL, Gautam D, Cui Y, Mears D, Wess J. Muscarinic stimulation of pancreatic insulin and glucagon release is abolished in m3 muscarinic acetylcholine receptor-deficient mice. Diabetes 53: 1714-1720, 2004. (Pubitemid 38857029)
13. Edvell A, Lindstrom P. Vagotomy in young hyperglycemic mice: effects on syndrome development and islet proliferation. Am J Physiol Endocrinol Metab 274: E1034-E1039, 1998. (Pubitemid 28308789)
14. Finegood DT, Scaglia L, Bonner-Weir S. Dynamics of beta-cell mass in the growing rat pancreas. Estimation with a simple mathematical model. Diabetes 44: 249-256, 1995.
15. Gautam D, Han SJ, Hamdan FF, Jeon J, Li B, Li JH, Cui Y, Mears D, Lu H, Deng C, Heard T, Wess J. A critical role for beta cell M3 muscarinic acetylcholine receptors in regulating insulin release and blood glucose homeostasis in vivo. Cell Metab 3: 449-461, 2006. (Pubitemid 43811775)
16. Gautam D, Jeon J, Li JH, Han SJ, Hamdan FF, Cui Y, Lu H, Deng C, Gavrilova O, Wess J. Metabolic roles of the M3 muscarinic acetylcholine receptor studied with M3 receptor mutant mice: a review. J Recept Signal Transduct Res 28: 93-108, 2008. (Pubitemid 351588080)
17. Georgia S, Bhushan A. p27 Regulates the transition of beta-cells from quiescence to proliferation. Diabetes 55: 2950-2956, 2006.
18. Imai J, Katagiri H, Yamada T, Ishigaki Y, Suzuki T, Kudo H, Uno K, Hasegawa Y, Gao J, Kaneko K, Ishihara H, Niijima A, Nakazato M, Asano T, Minokoshi Y, Oka Y. Regulation of pancreatic beta cell mass by neuronal signals from the liver. Science 322: 1250-1254, 2008.
19. Jansson L, Hellerström C. Glucose-induced changes in pancreatic islet blood flow mediated by central nervous system. Am J Physiol Endocrinol Metab 251: E644-E647, 1986.
20. Jetton TL, Lausier J, LaRock K, Trotman WE, Larmie B, Habibovic A, Peshavaria M, Leahy JL. Mechanisms of compensatory beta-cell growth in insulin-resistant rats: roles of Akt kinase. Diabetes 54: 2294-2304, 2005.
21. 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 50: 1377-1384, 2001.
22. Jetton TL, Liu YQ, Trotman WE, Nevin PW, Sun XJ, Leahy JL. Enhanced expression of insulin receptor substrate-2 and activation of protein kinase B/Akt in regenerating pancreatic duct epithelium of 60%- partial pancreatectomy rats. Diabetologia 44: 2056-2065, 2001.
23. Jetton TL, Everill B, Lausier J, Roskens V, Habibovic A, LaRock K, Gokin A, Peshavaria M, Leahy JL. Enhanced β-cell mass without increased proliferation following chronic mild glucose infusion. Am J Physiol Endocrinol Metab 294: E679-E687, 2008.
24. Jhala US, Canettieri G, Screaton RA, Kulkarni RN, Krajewski S, Reed J, Walker J, Lin X, White M, Montminy M. cAMP promotes pancreatic beta-cell survival via CREB-mediated induction of IRS2. Genes Dev 17: 1575-1580, 2003.
25. Kaneto H, Miyatsuka T, Kawamori D, Yamamoto K, Kato K, Shiraiwa T, Katakami N, Yamasaki Y, Matsuhisa M, Matsuoka TA. PDX-1 and MafA play a crucial role in pancreatic beta-cell differentiation and maintenance of mature beta-cell function. Endocr J 55: 235-252, 2007.
26. Kiba T, Tanaka K, Inoue S, Endo O, Takamura Y. Comparison of DNA contents of visceral organs in rats with ventromedial hypothalamic lesions and fed a high fat diet. Neurosci Lett 126: 127-130, 1991.
27. Kiba T, Tanaka K, Numata K, Hoshino M, Misugi K, Inoue S. Ventromedial hypothalamic lesion-induced vagal hyperactivity stimulates rat pancreatic cell proliferation. Gastroenterology 110: 885-893, 1996.
28. Kiba T. Relationships between the autonomic nervous system and the pancreas including regulation of regeneration and apoptosis: recent developments. Pancreas 29: e51-e58, 2004.
29. Kulkarni RN, Jhala US, Winnay JN, Krajewski S, Montminy M, Kahn CR. PDX-1 haploinsufficiency limits the compensatory islet hyperplasia that occurs in response to insulin resistance. J Clin Invest 114: 828-836, 2004.
30. Kushner JA, Ciemerych MA, Sicinska E, Wartschow LM, Teta M, Long SY, Sicinski P, White MF. Cyclins D2 and D1 are essential for postnatal pancreatic beta-cell growth. Mol Cell Biol 25: 3752-3762, 2005.
31. Li Y, Owyang C. Musings on the Wanderer: What's New in Our Understanding of Vago-Vagal Reflexes? V. Remodeling of vagus and enteric neural circuitry after vagal injury. Am J Physiol Gastrointest Liver Physiol 285: G461-G469, 2003.
32. Mayerhofer A, Kunz L. A non-neuronal cholinergic system of the ovarian follicle. Ann Anat 187: 521-528, 2005.
33. McKinnon CM, Docherty K. Pancreatic duodenal homeobox-1, PDX-1, a major regulator of beta cell identity and function. Diabetologia 44: 1203-1214, 2001.
34. Nekrep N, Wang J, Miyatsuka T, German MS. Signals from the neural crest regulate beta-cell mass in the pancreas. Development 135: 2151-2160, 2008.
35. Okamoto H, Hribal ML, Lin HV, Bennett WR, Ward A, Accili D. Role of the forkhead protein FoxO1 in beta cell compensation to insulin resistance. J Clin Invest 116: 775-782, 2006.
36. Park S, Dong X, Fisher TL, Dunn S, Omer AK, Weir G, White MF. Exendin-4 uses Irs2 signaling to mediate pancreatic beta cell growth and function. J Biol Chem 281: 1159-1168, 2006.
37. Peshavaria M, Larmie BL, Lausier J, Satish B, Habibovic A, Roskens V, Larock K, Everill B, Leahy JL, Jetton TL. Regulation of pancreatic beta-cell regeneration in the normoglycemic 60% partial-pancreatectomy mouse. Diabetes 55: 3289-3298, 2006.
38. Renuka TR, Savitha B, Paulose CS. Muscarinic M1 and M3 receptor binding alterations in pancreas during pancreatic regeneration of young rats. Endocr Res 31: 259-270, 2005.
39. Resende RR, Adhikari A. Cholinergic receptor pathways involved in apoptosis, cell proliferation and neuronal differentiation. Cell Commun Signal 7: 20, 2009.
40. Rocca AS, Brubaker PL. Role of the vagus nerve in mediating proximal nutrient-induced glucagon-like peptide-1 secretion. Endocrinology 40: 1687-1694, 1999.
41. Sangiorgi E, Capecchi MR. Bmi1 lineage tracing identifies a self-renewing pancreatic acinar cell subpopulation capable of maintaining pancreatic organ homeostasis. Proc Natl Acad Sci USA 106: 7101-7106, 2009.
42. Scaglia L, Smith FE, Bonner-Weir S. Apoptosis contributes to the involution of beta cell mass in the post partum rat pancreas. Endocrinology 136: 5461-5468, 1995.
43. Tanaka K, Inoue S, Nagase H, Takamura Y. Modulation of arginine-induced insulin and glucagon secretion by the hepatic vagus nerve in the rat: effects of celiac vagotomy and administration of atropine. Endocrinology 127: 2017-2023, 1990.
44. Tobin G, Giglio D, Lundgren O. Muscarinic receptor subtypes in the alimentary tract. J Physiol Pharmacol 60: 3-21, 2009.
45. Uchida T, Nakamura T, Hashimoto N, Matsuda T, Kotani K, Sakaue H, Kido Y, Hayashi Y, Nakayama KI, White MF, Kasuga M. Deletion of Cdkn1b ameliorates hyperglycemia by maintaining compensatory hyperinsulinemia in diabetic mice. Nat Med 11: 175-182, 2005.
46. Westmoreland JJ, Wang Q, Bouzaffour M, Baker SJ, Sosa-Pineda B. Pdk1 activity controls proliferation, survival, and growth of developing pancreatic cells. Dev Biol 334: 285-298, 2009.
47. Woods SC, Porte D Jr. Neural control of the endocrine pancreas. Physiol Rev 54: 596-619, 1974.
48. Yoshimura R, Omori H, Somekawa S, Osaka T, Ito R, Inoue S, Endo Y. Continuous carbachol infusion promotes peripheral cell proliferation and mimics vagus hyperactivity in a rat model of hypothalamic obesity. Biomed Res 27: 81-88, 2006.