Effects of olanzapine on muscarinic M3 receptor binding density in the brain relates to weight gain, plasma insulin and metabolic hormone levels

European Neuropsychopharmacology

Volumn 22, Issue 5, 2012, Pages 364-373

  Weston Green, Katrina ^a,b   Huang, Xu Feng ^a,b   Lian, Jiamei ^a   Deng, Chao ^a,b  

^a UNIVERSITY OF WOLLONGONG   (Australia)

^b SCHIZOPHRENIA RESEARCH INSTITUTE   (Australia)

Author keywords

Antipsychotic agents; Diabetes mellitus; Metabolism; Muscarinic M3 receptor; Obesity

Indexed keywords

4 DIPHENYLACETOXY 1 METHYLPIPERIDINE; ACETYLCHOLINE; CHOLECYSTOKININ; GHRELIN; GLUCOSE; INSULIN; MUSCARINIC M3 RECEPTOR; OLANZAPINE; OTENZEPAD; PIRENZEPINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARCUATE NUCLEUS; ARTICLE; BODY WEIGHT; BRAIN STEM; CONTROLLED STUDY; DIABETOGENESIS; DRUG EFFECT; DRUG RECEPTOR BINDING; FEMALE; FOOD INTAKE; GLUCOSE BLOOD LEVEL; HORMONE BLOOD LEVEL; HYPOTHALAMUS VENTROMEDIAL NUCLEUS; INSULIN BLOOD LEVEL; INSULIN RELEASE; NONHUMAN; PRIORITY JOURNAL; RAT; RECEPTOR DENSITY; UPREGULATION; VAGUS NERVE; VAGUS NERVE DORSAL NUCLEUS; WEIGHT GAIN;

ANIMALS; BENZODIAZEPINES; BRAIN; CHOLECYSTOKININ; EATING; FEMALE; GHRELIN; INSULIN; METABOLIC NETWORKS AND PATHWAYS; PROTEIN BINDING; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, MUSCARINIC M3; TREATMENT OUTCOME; WEIGHT GAIN;

EID: 84859211563     PISSN: 0924977X     EISSN: 18737862     Source Type: Journal    
DOI: 10.1016/j.euroneuro.2011.09.003     Document Type: Article

References (63)

1. Albaugh V., Henry C., Bello N., Hajnal A., Lynch S., Halle B., Lynch C. Hormonal and metabolic effects of olanzapine and clozapine related to body weight in rodents. Obesity 2006, 14:36-50.
2. American Diabetes Association, American Psychiatric Association, American Association of Clinical Endocrinologists, Obesity, N.A.A.f.t.S.o. Consensus development conference on antipsychotic drugs and obesity and diabetes. Diab. Care 2004, 27:596-601.
3. Australian Government National Health and Medical Research Council Australian Code of Practice for the Care and Use of Animals for Scientific Purposes 2004, Australian Government, Canberra. seventh ed.
4. Aravagiri M., Teper Y., Marder S.R. Pharmacokinetics and tissue distribution of olanzapine in rats. Biopharm. Drug Dispos. 1999, 20:369-377.
5. Balakrishnan S., Mathew J., Antony S., Paulose C.S. Muscarinic M1, M3 receptors function in the brainstem of streptozotocin induced diabetic rats: their role in insulin secretion from the pancreatic islets as a function of age. Eur. J. Pharmacol. 2009, 608:14-22.
6. Berthoud H.-R. The vagus nerve, food intake and obesity. Regul. Pept. 2008, 149:15-25.
7. Bouche C., Serdy S., Kahn C.R., Goldfine A.B. The cellular fate of glucose and its relevance in Type 2 diabetes. Endocr. Rev. 2004, 25:807-830.
8. Buijs R., Chun S., Niijima A., Romijn H., 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. 2001, 431:405-423.
9. Chintoh A.F., Mann S.W., Lam L., Giacca A., Fletcher P., Nobrega J., Remington G. Insulin resistance and secretion in vivo: effects of different antipsychotics in an animal model. Schizophr. Res. 2009, 108:127-133.
10. Chintoh A.F., Mann S.W., Lam L., Lam C., Cohn T.A., Fletcher P.J., Nobrega J.N., Giacca A., Remington G. Insulin resistance and decreased glucose-stimulated insulin secretion after acute olanzapine administration. J. Clin. Psychopharmacol. 2008, 28:494-499.
11. Chintoh A.F., Mann S.W., Lam T.K.T., Giacca A., Remington G. Insulin resistance following continuous, chronic olanzapine treatment: an animal model. Schizophr. Res. 2008, 104:23-30.
12. Chiu C.-C., Chen C.-H., Chen B.-Y., Yu S.-H., Lu M.-L. The time-dependent change of insulin secretion in schizophrenic patients treated with olanzapine. Prog. Neuropsychopharmacol. Biol. Psychiatry 2010, 34:866-870.
13. Chiu C., Chen K., Liu H., Lu M. The early effect of olanzapine and risperidone on insulin secretion in atypical-naive schizophrenic patients. J. Clin. Psychopharmacol. 2006, 26:504-507.
14. Coccurello R., Brina D., Caprioli A., Conti R., Ghirardi O., Schepis F., Moles A. 30 days of continuous olanzapine infusion determines energy imbalance, glucose intolerance, insulin resistance, and dyslipidemia in mice. J. Clin. Psychopharmacol. 2009, 29:576-583.
15. Coccurello R., Moles A. Potential mechanisms of atypical antipsychotic-induced metabolic derangement: clues for understanding obesity and novel drug design. Pharmacol. Ther. 2010, 127:210-251.
16. Cone R.D., Cowley M.A., Butler A.A., Fan W., Marks D.L., Low M.J. The arcuate nucleus as a conduit for diverse signals relevant to energy homeostasis. Int. J. Obes. Relat. Disord. 2001, 25:S63.
17. Crook J.M., Tomaskovic-Crook E., Copolov D.L., Dean B. Low muscarinic receptor binding in prefrontal cortex from subjects with schizophrenia: a study of Brodmann's areas 8, 9, 10, and 46 and the effects of neuroleptic drug treatment. Am. J. Psychiatry 2001, 158:918-925.
18. Das U.N. Vagus nerve stimulation as a strategy to prevent and manage metabolic syndrome. Med. Hypotheses 2010, 76:429-433.
19. Deng C., Weston-Green K.L., Han M., Huang X.-F. Olanzapine treatment decreases the density of muscarinic M2 receptors in the dorsal vagal complex of rats. Prog. Neuropsychopharmacol. Biol. Psychiatry 2007, 31:915-920.
20. Dockray G.J. The versatility of the vagus. Physiol. Behav. 2009, 97:531-536.
21. Duttaroy A., Zimliki C.L., Gautam D., Cui Y., Mears D., Wess J. Muscarinic stimulation of pancreatic insulin and glucagon release is abolished in [M.sub.3] muscarinic acetylcholine receptor-deficient mice. (Islet studies). Diabetes 2004, 53:1714-1717.
22. Gautam D., de Azua I.R., Li J.H., Guettier J.-M., Heard T., Cui Y., Lu H., Jou W., Gavrilova O., Zawalich W.S., Wess J. Beneficial metabolic effects caused by persistent activation of {beta}-cell M3 muscarinic acetylcholine receptors in transgenic mice. Endocrinology 2010, 151:5185-5194.
23. Gautam D., Gavrilova O., Jeon J., Pack S., Jou W., Cui Y., Li J.H., Wess J. Beneficial metabolic effects of M3 muscarinic acetylcholine receptor deficiency. Cell Metab. 2006, 4:363-375.
24. Gautam D., Han S.-J., Hamdan F.F., Jeon J., Li B., Li J.H., 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. 2006, 3:449-461.
25. Gibbons A.S., Scarr E., McLean C., Sundram S., Dean B. Decreased muscarinic receptor binding in the frontal cortex of bipolar disorder and major depressive disorder subjects. J. Affect. Disord. 2009, 116:184-191.
26. Gilon P., Henquin J.-C. Mechanisms and physiological significance of the cholinergic control of pancreatic {beta}-cell function. Endocr. Rev. 2001, 22:565-604.
27. Han M., Newell K., Zavitsanou K., Deng C., Huang X.-F. Effects of antipsychotic medication on muscarinic M1 receptor mRNA expression in the rat brain. J. Neurosci. Res. 2008, 86:457-464.
28. Haro J.M., Novick D., Suarez D., Roca M. Antipsychotic treatment discontinuation in previously untreated patients with schizophrenia: 36-month results from the SOHO study. J. Psychiatr. Res. 2009, 43:265-273.
29. Johnson D.E., Yamazaki H., Ward K.M., Schmidt A.W., Lebel W.S., Treadway J.L., Gibbs E.M., Zawalich W.S., Rollema H. Inhibitory effects of antipsychotics on carbachol-enhanced insulin secretion from perifused rat islets: role of muscarinic antagonism in antipsychotic-induced diabetes and hyperglycemia. Diabetes 2005, 54:1552-1558.
30. Kapur S., VanderSpek S.C., Brownlee B.A., Nobrega J. Antipsychotic dosing in preclinical models is often unrepresentative of the clinical condition: a suggested solution based on in vivo occupancy. J. Pharmacol. Exp. Ther. 2003, 305:625-631.
31. Kroeze W.K., Hufeisen S.J., Popadak B.A., Renock S.M., Steinberg S., Ernsberger P., Jayathilake K., Meltzer H.Y., Roth B.L. H1-histamine receptor affinity predicts short-term weight gain for typical and atypical antipsychotic drugs. Neuropsychopharmacology 2003, 28:519-526.
32. Lee H.-M., Wang G., Englander E.W., Kojima M., Greeley G.H. Ghrelin, a new gastrointestinal endocrine peptide that stimulates insulin secretion: enteric distribution, ontogeny, influence of endocrine, and dietary manipulations. Endocrinology 2002, 143:185-190.
33. Levey A.I., Edmunds S.M., Heilman C.J., Desmond T.J., Frey K.A. Localization of muscarinic M3 receptor protein and M3 receptor binding in rat brain. Neuroscience 1994, 63:207-221.
34. Li J., Gautam D., Han S., Guettier J., Cui Y., Lu H., Deng C., O'Hare J., Jou W., Gavrilova O., Buettner C., Wess J. Hepatic muscarinic acetylcholine receptors are not critically involved in maintaining glucose homeostasis in mice. Diabetes 2009, 58:2776.
35. Li Y., Wu X., Zhu J., Yan J., Owyang C. Hypothalamic regulation of pancreatic secretion is mediated by central cholinergic pathways in the rat. J. Physiol. 2003, 552:571-587.
36. Liddle R.A. Regulation of cholecystokinin secretion in humans. J. Gastroenterol. 2000, 35:181-187.
37. Lieberman J.A., Stroup T.S., McEvoy J.P., Swartz M.S., Rosenheck R.A., Perkins D.O., Keefe R.S.E., Davis S.M., Davis C.E., Lebowitz B.D., Severe J., Hsiao J.K. Effectiveness of antipsychotic drugs in patients with chronic schizophrenia. N. Engl. J. Med. 2005, 353:1209-1223.
38. Matsui-Sakata A., Ohtani H., Sawada Y. Receptor occupancy-based analysis of the contributions of various receptors to antipsychotics-induced weight gain and diabetes mellitus. Drug Metab. Pharmacokinet. 2005, 20:368-378.
39. Michel A.D., Stefanich E., Whiting R.L. Direct labeling of rat M3-muscarinic receptors by [3H]4DAMP. Eur. J. Pharmacol. 1989, 166:459-466.
40. Newcomer J. Second-generation atypical antipsychotics and metabolic effects. A comprehensive literature review. CNS Drugs 2005, 19:1-93.
41. Ochi Y., Horie S., Maruyama T., Watanabe K., Yano S. Necessity of intracellular cyclic AMP in inducing gastric acid secretion via muscarinic M3 and cholecystokinin2 receptors on parietal cells in isolated mouse stomach. Life Sci. 2005, 77:2040-2050.
42. Oriot P., Feys J., Mertens de Wilmars S., Misson S., Ayache A., Fagnart O., Gruson D., Luts A., Jamart J., Hermans M.-P., Buysschaert M. Insulin sensitivity, adjusted beta-cell function and adiponectinaemia among lean drug-naive schizophrenic patients treated with atypical antipsychotic drugs: a nine-month prospective study. Diab. Metab. 2008, 34:490-496.
43. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 2007, Elselvier Academic Press Inc., CA, USA. 6th ed.
44. Perez-Iglesias R., Vazquez-Barquero J.L., Amado J.A., Berja A., Garcia-Unzueta M.T., Pelayo-Teran J.M., Carrasco-Marin E., Mata I., Crespo-Facorro B. Effect of antipsychotics on peptides involved in energy balance in drug-naive psychotic patients after 1 year of treatment. J. Clin. Psychopharmacol. 2008, 28:289-295.
45. Ramankutty G. Olanzapine-induced destabilization of diabetes in the absence of weight gain. Acta Psychiatr. Scand. 2002, 105:235-236.
46. Reagan-Shaw S., Nihal M., Ahmad N. Dose translation from animal to human studies revisited. FASEB J. 2007, 22:659-661.
47. Renuka T.R., Ani D.V., Paulose C.S. Alterations in the muscarinic M1 and M3 receptor gene expression in the brain stem during pancreatic regeneration and insulin secretion in weanling rats. Life Sci. 2004, 75:2269-2280.
48. Reynolds G.P., Kirk S.L. Metabolic side effects of antipsychotic drug treatment - pharmacological mechanisms. Pharmacol. Ther. 2010, 125:169-179.
49. Rohner-Jeanrenaud F., Jeanrenaud B. Consequences of ventromedial hypothalamic lesions upon insulin and glucagon secretion by subsequently isolated perfused pancreases in the rat. J. Clin. Investig. 1980, 65:902-910.
50. Ruiz de Azua I., Gautam D., Guettier J.-M., Wess J. Novel insights into the function of [beta]-cell M3 muscarinic acetylcholine receptors: therapeutic implications. Trends Endocrinol. Metab. 2011, 22:74-80.
51. Shen K.-Z., Johnson S.W. Presynaptic dopamine D2 and muscarine M3 receptors inhibit excitatory and inhibitory transmission to rat subthalamic neurones in vitro. J. Physiol. 2000, 525:331-341.
52. Silvestre J., Prous J. Research on adverse drug events. I. Muscarinic M3 receptor binding affinity could predict the risk of antipsychotics to induce type 2 diabetes. Methods Find. Exp. Clin. Pharmacol. 2005, 27:289-304.
53. Smith G.P., Jerome C., Cushin B.J., Eterno R., Simansky K.J. Abdominal vagotomy blocks the satiety effect of cholecystokinin in the rat. Science 1981, 213:1036-1037.
54. Starrenburg F.C.J., Bogers J.P.A.M. How can antipsychotics cause diabetes mellitus? Insights based on receptor-binding profiles, humoral factors and transporter proteins. Eur. Psychiatry 2009, 24:164-170.
55. Tebbe J.J., Dietze T., Grote C., Mönnikes H. Excitatory stimulation of neurons in the arcuate nucleus inhibits gastric acid secretion via vagal pathways in anesthetized rats. Brain Res. 2001, 913:10-17.
56. Terry A.V., Gearhart D.A., Mahadik S.P., Warsi S., Waller J.L. Chronic treatment with first or second generation antipsychotics in rodents: effects on high affinity nicotinic and muscarinic acetylcholine receptors in the brain. Neuroscience 2006, 140:1277-1287.
57. Toshinai K., Mondal M.S., Nakazato M., Date Y., Murakami N., Kojima M., Kangawa K., Matsukura S. Upregulation of ghrelin expression in the stomach upon fasting, insulin-induced hypoglycemia, and leptin administration. Biochem. Biophys. Res. Commun. 2001, 281:1220-1225.
58. Weston-Green K., Huang X.-F., Deng C. Olanzapine treatment and metabolic dysfunction: a dose response study in female Sprague Dawley rats. Behav. Brain Res. 2011, 217:337-346.
59. White J., Olchovsky D., Kershaw M., Berelowitz M. Increased hypothalamic content of preproneuropeptide-Y messenger ribonucleic acid in streptozotocin-diabetic rats. Endocrinology 1990, 126:765-772.
60. Yamada M., Miyakawa T., Duttaroy A., Yamanaka A., Moriguchi T., Makita R., Ogawa M., Chou C.J., Xia B., Crawley J.N., Felder C.C., Deng C.-X., Wess J. Mice lacking the M3 muscarinic acetylcholine receptor are hypophagic and lean. Nature 2001, 410:207-212.
61. Yang T.-T., Chang C.-K., Tsao C.-W., Hsu Y.-M., Hsu C.-T., Cheng J.-T. Activation of muscarinic M-3 receptor may decrease glucose uptake and lipolysis in adipose tissue of rats. Neurosci. Lett. 2009, 451:57-59.
62. Zavitsanou K., Nguyen V., Han M., Huang X. Effects of typical and atypical antipsychotic drugs on rat brain muscarinic receptors. Neurochem. Res. 2007, 32:525-532.
63. Zubieta J.K., Frey K.A. Autoradiographic mapping of M3 muscarinic receptors in the rat brain. J. Pharmacol. Exp. Ther. 1993, 264:415-422.