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Psychiatric Times. Vol. 25 No. 5
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The Muscarinic Hypothesis of Schizophrenia

Implications for Pharmacological Treatment

By Thomas J. Raedler, MD | April 15, 2008


Several M1 muscarinic agonists were developed for potential treatment of patients with dementia. Alvameline, milameline, sabcomeline, SDZ 210-086, and xanomeline were all discontinued for lack of effectiveness or because of their adverse-effect profiles.3 Some of these agents lacked true specificity for the M1 receptor subtype, which resulted in limitations in dosage. With the exception of xanomeline, no M1 muscarinic agonist has been assessed in schizophrenia. Several novel M1 muscarinic agonists are currently under development, which should overcome the shortcomings of these older agents.24 In addition, M4 muscarinic agonists are in the early stages of development for use in schizophrenia.

N-desmethylclozapine as the first partial M1 muscarinic agonist
Clozapine remains the antipsychotic of choice in patients with treatment-refractory schizophrenia. Recent studies have confirmed the superiority of clozapine(Drug information on clozapine) for this patient group.25,26 The mechanism of clozapine remains poorly understood. Clozapine has strong in vivoeffects on muscarinic receptors.16 While it is traditionally associated with muscarinic antagonism, some of its adverse effects (eg, hypersalivation) actually improve under treatment with anticholinergics, suggesting possible muscarinic agonist effects.

Because of its unique pharmacological properties, N-desmethylclozapine (norclozapine; NDMC), the main active metabolite of clozapine, has been the focus of attention. In addition to being a partial agonist at dopamine(Drug information on dopamine) D2 and D3 receptors, NDMC is also a partial agonist at M1 muscarinic receptors.27 NDMC (ACP-104) is currently undergoing a phase 2 study in patients with schizophrenia. The results of this study will help further assess the usefulness of M1 muscarinic agonists in schizophrenia.

Summary
The muscarinic hypothesis of schizophrenia postulates an alteration of the muscarinic cholinergic system as part of the underlying pathophysiology of this disorder and is supported by data from neuropathology, brain imaging, preclinical and clinical pharmacology, and clinical studies. The muscarinic hypothesis should be seen as an addition to existing theories on schizophrenia and offers a potential new approach for the pharmacological treatment of schizophrenia.

All currently available antipsychotics focus on the dopaminergic system. The interactions between the muscarinic and the dopaminergic systems are complex and occur at different levels in the brain. It remains unclear if beneficial effects of muscarinic agonists in schizophrenia are primarily caused by direct muscarinic effects or are secondary to a modulatory effect on the dopaminergic system. These 2 mechanisms are not mutually exclusive and can combine for additional efficacy.

Some currently available pharmacological agents affect the muscarinic cholinergic system. Several older and newer antipsychotics interact with muscarinic receptors in vitro and in vivo. While muscarinic antagonism may help lower the risk of treatment-emergent motor adverse effects, muscarinic antagonism also carries the potential of worsening cognitive function. The effects of the adjunctive use of cholinesterase inhibitors on cognitive function in schizophrenia have been modest at best.

Positive and negative symptoms as well as cognitive symptoms are potential target symptoms for muscarinic agonists in schizophrenia. Different muscarinic agonists were developed primarily for the treatment of dementia. These agents were abandoned because of problems with dosing and tolerability. New muscarinic agonists are under development with the potential for better specificity and tolerability. For the treatment of schizophrenia, M1 muscarinic agonists seem the most promising new approach.

Experimental data and first clinical data suggest that M1 muscarinic agonists are effective against psychotic and cognitive symptoms. However, there are limited clinical data. NDMC, the active metabolite of clozapine, is a partial M1 muscarinic agonist. The results of first clinical trials with NDMC will shed additional light on the effects of M1 muscarinic agonists in schizophrenia.

The muscarinic cholinergic system is a promising new target for the pharmacological treatment of schizophrenia. However, large studies with newly developed agents are needed to determine the clinical usefulness of this approach. Tables 1 and 2 present brief summaries of muscarinic treatment strategies for schizophrenia and the effects of psychotropic medications on muscarinic receptors, respectively.

 

   
TABLE 1
Effects of currently available psychotropic agents on muscarinic receptors
   
 
 • Muscarinic antagonists (anticholinergics) are beneficial against antipsychoticinduced motor adverse effects
 • Anticholinergics impair cognition
 • Different antipsychotics (eg, clozapine and olanzapine(Drug information on olanzapine)) as well as tricyclic antidepressants antagonize muscarinic receptors in vitro and in vivo
 • The effects of cholinesterase inhibitors on cognition in schizophrenia are modest at best
 • N-desmethylclozapine, the active metabolite of clozapine, is a partial agonist at M1 muscarinic receptors and may explain the superior clinical efficacy of clozapine



 

   
TABLE 2
Novel muscarinic treatment strategies in schizophrenia
   
 
 • Preclinical and small clinical studies suggest that muscarinic agonists may be beneficial for the treatment of positive and cognitive symptoms of schizophrenia
 • All previously developed M1 muscarinic agonists had to be abandoned because of their lack of specificity and adverse-effect profiles
 • Several M1 muscarinic agonists are currently in development that promise better selectivity and tolerability
 • Future clinical studies will show whether muscarinic agonism emerges as a new treatment option in schizophrenia
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References
1. Raedler TJ, Bymaster FP, Tandon R, et al. Towards a muscarinic hypothesis of schizophrenia. Mol Psychiatry. 2007;12:232-246.
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9. Ellis JR, Ellis KA, Bartholomeusz CF, et al. Muscarinic and nicotinic receptors synergistically modulate working memory and attention in humans. Int J Neuropsychopharmacol. 2006;9:175-189.
10. Minzenberg MJ, Poole JH, Benton C, Vinogradov S. Association of anticholinergic load with impairment of complex attention and memory in schizophrenia. Am J Psychiatry. 2004;161:116-124.
11. Tandon R, DeQuardo JR, Goodson J, et al. Effect of anticholinergics on positive and negative symptoms in schizophrenia. Psychopharmacol Bull. 1992; 28:297-302.
12. Zemishlany Z, Aizenberg D, Weiner Z, Weizman A. Trihexyphenidyl (Artane) abuse in schizophrenic patients. Int Clin Psychopharmacol. 1996;11:199-202.
13. Furey ML, Drevets WC. Antidepressant efficacy of the antimuscarinic drug scopolamine: a randomized, placebo-controlled clinical trial. Arch Gen Psychiatry. 2006;63:1121-1129.
14. Schotte A, Janssen PF, Gommeren W, et al. Risperidone compared with new and reference antipsychotic drugs: in vitro and in vivo receptor binding. Psychopharmacology. 1996;124:57-73.
15. Chew ML, Mulsant BH, Pollock BG, et al. A model of anticholinergic activity of atypical antipsychotic medications. Schizophr Res. 2006;88:63-72.
16. Raedler TJ, Knable MB, Jones DW, et al. Central muscarinic acetylcholine receptor availability in patients treated with clozapine. Neuropsychopharmacology. 2003;28:1531-1537.
17. Raedler TJ, Knable MB, Jones DW, et al. In vivo olanzapine occupancy of muscarinic acetylcholine receptors in patients with schizophrenia. Neuropsychopharmacology. 2000;23:56-68.
18. Raedler TJ. Comparison of the in vivo muscarinic cholinergic receptor availability in patients treated with clozapine and olanzapine. Int J Neuropsychopharmacol. 2007;10:275-280.
19. Gautam D, Han SJ, Duttaroy A, et al. Role of the M3 muscarinic acetylcholine receptor in beta-cell function and glucose homeostasis. Diabetes Obes Metab. 2007;9(suppl 2):158-169.
20. Jindal RD, Keshavan MS. Critical role of M3 muscarinic receptor in insulin secretion: implications for psychopharmacology. J Clin Psychopharmacol. 2006; 26:449-450.
21. Sullivan RJ, Andres S, Otto C, et al. The effects of an indigenous muscarinic drug, Betel nut (Areca catechu), on the symptoms of schizophrenia: a longitudinal study in Palau, Micronesia. Am J Psychiatry. 2007;164:670-673.
22. Bodick NC, Offen WW, Levey AI, et al. Effects of xanomeline, a selective muscarinic receptor agonist, on cognitive function and behavioral symptoms in Alzheimer disease. Arch Neurol. 1997;54:465-473.
23. Shekhar A, Potter WZ, Lienemann J, et al. Efficacy of xanomeline, a selective muscarinic agonist, in treating schizophrenia: a double-blind, placebo controlled study. Presented at: the 40th Annual Meeting of the American College of Neuropsychopharmacology; December 9-13, 2001; Hawaii.
24. Li Z, Bonhaus DW, Huang M, et al. AC260584 (4-[3-(4-butylpiperidin-1-yl)-propyl]-7-fluoro-4H-benzo[1,4]oxazin-3-one), a selective muscarinic M1 receptor agonist, increases acetylcholine and dopamine release in rat medial prefrontal cortex and hippocampus. Eur J Pharmacol. 2007;572:129-137.
25. Lewis SW, Barnes TR, Davies L, et al. Randomized controlled trial of effect of prescription of clozapine versus other second-generation antipsychotic drugs in resistant schizophrenia. Schizophr Bull. 2006;32: 715-723.
26. McEvoy JP, Lieberman JA, Stroup TS, et al. Effectiveness of clozapine versus olanzapine, quetiapine, and risperidone in patients with chronic schizophrenia who did not respond to prior atypical antipsychotic treatment. Am J Psychiatry. 2006;163:600-610.
27. Lameh J, Burstein ES, Taylor E, et al. Pharmacology of N-desmethylclozapine. Pharmacol Ther. 2007; 115:223-231.


 
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