Gastroenterology
Volume 138, Issue 1 , Pages 98-107.e4 , January 2010

Neuropeptide S Receptor Induces Neuropeptide Expression and Associates With Intermediate Phenotypes of Functional Gastrointestinal Disorders

  • Michael Camilleri

      Affiliations

    • Clinical Enteric Neuroscience Translational and Epidemiological Research (CENTER), Division of Biostatistics, College of Medicine, Mayo Clinic, Rochester, Minnesota
    • Corresponding Author InformationReprint requests Address requests for reprints to: Michael Camilleri, MD, Mayo Clinic, Charlton 8-110, 200 First Street SW, Rochester, Minnesota 55905
  • ,
  • Paula Carlson

      Affiliations

    • Clinical Enteric Neuroscience Translational and Epidemiological Research (CENTER), Division of Biostatistics, College of Medicine, Mayo Clinic, Rochester, Minnesota
  • ,
  • Alan R. Zinsmeister

      Affiliations

    • Department of Health Sciences Research, Division of Biostatistics, College of Medicine, Mayo Clinic, Rochester, Minnesota
  • ,
  • Sanna McKinzie

      Affiliations

    • Clinical Enteric Neuroscience Translational and Epidemiological Research (CENTER), Division of Biostatistics, College of Medicine, Mayo Clinic, Rochester, Minnesota
  • ,
  • Irene Busciglio

      Affiliations

    • Clinical Enteric Neuroscience Translational and Epidemiological Research (CENTER), Division of Biostatistics, College of Medicine, Mayo Clinic, Rochester, Minnesota
  • ,
  • Duane Burton

      Affiliations

    • Clinical Enteric Neuroscience Translational and Epidemiological Research (CENTER), Division of Biostatistics, College of Medicine, Mayo Clinic, Rochester, Minnesota
  • ,
  • Marco Zucchelli

      Affiliations

    • Department of Biosciences and Nutrition, Karolinska Institutet, Stockholm, Sweden
  • ,
  • Mauro D'Amato

      Affiliations

    • Department of Biosciences and Nutrition, Karolinska Institutet, Stockholm, Sweden

Received 19 May 2009 ,Accepted 20 August 2009.

References 

  1. Camilleri M. Mechanisms in IBS: something old, something new, something borrowed. Neurogastroenterol Motil. 2005;17:311–316
  2. Camilleri M, McKinzie S, Busciglio I, et al. Prospective study of motor, sensory, psychological and autonomic functions in patients with irritable bowel syndrome. Clin Gastroenterol Hepatol. 2008;6:772–781
  3. Dorn SD, Palsson OS, Thiwan SI, et al. Increased colonic pain sensitivity in irritable bowel syndrome is the result of an increased tendency to report pain rather than increased neurosensory sensitivity. Gut. 2007;56:1202–1209
  4. Spiller RC, Jenkins D, Thornley JP, et al. Increased rectal mucosal enteroendocrine cells, T lymphocytes, and increased gut permeability following acute Campylobacter enteritis and in post-dysenteric irritable bowel syndrome. Gut. 2000;47:804–811
  5. Dunlop SP, Hebden J, Campbell E, et al. Abnormal intestinal permeability in subgroups of diarrhea-predominant irritable bowel syndromes. Am J Gastroenterol. 2006;101:1288–1294
  6. Xavier RJ, Podolsky DK. Unravelling the pathogenesis of inflammatory bowel disease. Nature. 2007;448:427–434
  7. Saito YA. Genes and irritable bowel syndrome: is there a link?. Curr Gastroenterol Rep. 2008;10:355–362
  8. Schreiber S, Rosenstiel P, Albrecht M, et al. Genetics of Crohn disease, an archetypal inflammatory barrier disease. Nat Rev Genet. 2005;6:376–388
  9. Xu YL, Reinscheid RK, Huitron-Resendiz S, et al. Neuropeptide S: a neuropeptide promoting arousal and anxiolytic-like effects. Neuron. 2004;43:487–497
  10. Okamura N, Reinscheid RK. Neuropeptide S: a novel modulator of stress and arousal. Stress. 2007;10:221–226
  11. Raiteri L, Luccini E, Romei C, et al. Neuropeptide S selectively inhibits the release of 5-HT and noradrenaline from mouse frontal cortex nerve endings. Br J Pharmacol. 2009 Apr 3;[Epub ahead of print]
  12. Jüngling K, Seidenbecher T, Sosulina L, et al. Neuropeptide S-mediated control of fear expression and extinction: role of intercalated GABAergic neurons in the amygdala. Neuron. 2008;59:298–310
  13. Xu YL, Gall CM, Jackson VR, et al. Distribution of neuropeptide S receptor mRNA and neurochemical characteristics of neuropeptide S-expressing neurons in the rat brain. J Comp Neurol. 2007;500:84–102
  14. Li W, Chang M, Peng YL, et al. Neuropeptide S produces antinociceptive effect at the supraspinal level in mice. Regul Pept. 2009 Apr 2;[Epub ahead of print]
  15. D'Amato M, Bruce S, Bresso F, et al. Neuropeptide S receptor 1 gene polymorphism is associated with susceptibility to inflammatory bowel disease. Gastroenterology. 2007;133:808–817
  16. Laitinen T, Polvi A, Rydman P, et al. Characterization of a common susceptibility locus for asthma-related traits. Science. 2004;304:300–304
  17. Swedish Human Proteome Resource Program. Human protein atlas. www.proteinatlas.orgAccessed May 14, 2009
  18. Kormann MS, Carr D, Klopp N, et al. G-protein-coupled receptor polymorphisms are associated with asthma in a large German population. Am J Respir Crit Care Med. 2005;171:1358–1362
  19. Melen E, Bruce S, Doekes G, et al. Haplotypes of G protein-coupled receptor 154 are associated with childhood allergy and asthma. Am J Respir Crit Care Med. 2005;171:1089–1095
  20. Malerba G, Lindgren CM, Xumerle L, et al. Chromosome 7p linkage and GPR154 gene association in Italian families with allergic asthma. Clin Exp Allergy. 2007;37:83–89
  21. Feng Y, Hong X, Wang L, et al. G protein-coupled receptor 154 gene polymorphism is associated with airway hyperresponsiveness to methacholine in a Chinese population. J Allergy Clin Immunol. 2006;117:612–617
  22. Hersh CP, Raby BA, Soto-Quirós ME, et al. Comprehensive testing of positionally cloned asthma genes in two populations. Am J Respir Crit Care Med. 2007;176:849–857
  23. Pulkkinen V, Majuri ML, Wang G, et al. Neuropeptide S and G protein-coupled receptor 154 modulate macrophage immune responses. Hum Mol Genet. 2006;15:1667–1679
  24. Vendelin J, Pulkkinen V, Rehn M, et al. Characterization of GPRA, a novel G protein-coupled receptor related to asthma. Am J Respir Cell Mol Biol. 2005;33:262–270
  25. Talley NJ, Phillips SF, Wiltgen CM, et al. Assessment of functional gastrointestinal disease: the bowel disease questionnaire. Mayo Clin Proc. 1990;65:1456–1479
  26. Camilleri M, Carlson P, Zinsmeister AR, et al. Mitochondrial DNA and gastrointestinal motor and sensory functions in health and functional gastro-intestinal disorders. Am J Physiol Gastrointest Liver Physiol. 2009;296:G510–G516
  27. Kim HJ, Camilleri M, Carlson PJ, et al. Association of distinct α2 adrenoceptor and serotonin-transporter polymorphisms associated with constipation and somatic symptoms in functional gastrointestinal disorders. Gut. 2004;53:829–837
  28. Andresen V, Camilleri M, Kim HJ, et al. Is there an association between GNβ3 C825T genotype and lower functional gastrointestinal disorders?. Gastroenterology. 2006;130:1985–1994
  29. Camilleri CE, Carlson PJ, Camilleri M, et al. A study of candidate genotypes associated with dyspepsia in a U.S. community. Am J Gastroenterol. 2006;101:581–592
  30. Castillo EJ, Camilleri M, Locke GR, et al. A community based, controlled study of the epidemiology and pathophysiology of dyspepsia. Clin Gastroenterol Hepatol. 2004;2:985–996
  31. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)). Methods. 2001;25:402–408
  32. Gonzalez JR, Armengol L, Sole X, et al. SNPassoc: an R package to perform whole genome association studies. Bioinformatics. 2007;23:644–645
  33. Delgado-Aros S, Camilleri M, Garcia MA, et al. High body mass alters colonic sensory-motor function and transit in humans. Am J Physiol Gastrointest Liver Physiol. 2008;295:G382–G388
  34. Yeo A, Boyd P, Lumsden S, et al. Association between a functional polymorphism in the serotonin transporter gene and diarrhoea predominant irritable bowel syndrome in women. Gut. 2004;53:1452–1458
  35. Van Kerkhoven LA, Laheij RJ, Jansen JB. Meta-analysis: a functional polymorphism in the gene encoding for activity of the serotonin transporter protein is not associated with the irritable bowel syndrome. Aliment Pharmacol Ther. 2007;26:979–986
  36. Camilleri M, Busciglio I, Carlson P, et al. Candidate genes and sensory functions in health and irritable bowel syndrome. Am J Physiol Gastrointest Liver Physiol. 2008;295:G219–G225
  37. Reinscheid RK, Xu YL, Okamura N, et al. Pharmacological characterization of human and murine neuropeptide S receptor variants. J Pharmacol Exp Ther. 2005;315:1338–1345
  38. Roth AL, Marzola E, Rizzi A, et al. Structure-activity studies on neuropeptide S: identification of the amino acid residues crucial for receptor activation. J Biol Chem. 2006;281:20809–20816
  39. Bernier V, Stocco R, Bogusky MJ, et al. Structure/function relationships in the neuropeptide s receptor: molecular consequences of the asthma-associated mutation N107I. J Biol Chem. 2006;281:24704–24712
  40. Vendelin J, Bruce S, Holopainen P, et al. Downstream target genes of the neuropeptide S-NPSR1 pathway. Hum Mol Genet. 2006;15:2923–2935
  41. Shimizu Y, Matsuyama H, Shiina T, et al. Tachykinins and their functions in the gastrointestinal tract. Cell Mol Life Sci. 2008;65:295–311
  42. Bornstein JC, Costa M, Grider JR. Enteric motor and interneuronal circuits controlling motility. Neurogastroenterol Motil. 2004;16(Suppl 1):34–38
  43. Olsson C, Holmgren S. The control of gut motility. Comp Biochem Physiol A Mol Integr Physiol. 2001;128:481–503
  44. Camilleri M, Grudell AB. Appetite and obesity: a gastroenterologist's perspective. Neurogastroenterol Motil. 2007;19:333–341
  45. Han RW, Chang M, Peng YL, et al. Central neuropeptide S inhibits distal colonic transit through activation of central neuropeptide S receptor in mice. Peptides. 2009;30:1313–1317
  46. Mayer EA. The challenge of studying the biology of complex, symptom-based GI disorders. Gastroenterology. 2008;134:1826–1827

 Conflict of interest The authors disclose no conflicts.

 Funding Dr Camilleri is supported in part by RO1 grant DK54681 from National Institutes of Health. Dr D'Amato is supported by the Groschinskys Minnesfond, the Ruth and Richard Juhlin's Foundation, and the Prof Nanna Svartz Fund.

PII: S0016-5085(09)01509-1

doi: 10.1053/j.gastro.2009.08.051

Gastroenterology
Volume 138, Issue 1 , Pages 98-107.e4 , January 2010