Oral ingestion of Capsaicin, the pungent component of chili pepper, enhances a discreet population of macrophages and confers protection from autoimmune diabetes

Mucosal Immunology

Volumn 5, Issue 1, 2012, Pages 76-86

  Nevius, E ^a   Srivastava, P K ^a   Basu, S ^a  

^a UNIVERSITY OF CONNECTICUT SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSAICIN; CD11B ANTIGEN; INTERLEUKIN 10; PROGRAMMED DEATH 1 LIGAND 1; VANILLOID RECEPTOR 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNE DISEASE; CONTROLLED STUDY; DOSE RESPONSE; DRUG POTENCY; IMMUNOMODULATION; IN VIVO STUDY; INSULIN DEPENDENT DIABETES MELLITUS; LYMPH NODE; LYMPHOCYTE PROLIFERATION; MACROPHAGE; MOUSE; NONHUMAN; PANCREATIC LYMPH NODE; PRIORITY JOURNAL; PROTECTION; PROTEIN EXPRESSION; T LYMPHOCYTE ACTIVATION;

EID: 83655183018     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2011.50     Document Type: Article

References (45)

1. Tominaga, M., et al. The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron 21, 531-543 (1998). (Pubitemid 28475505)
2. Cesare, P., Moriondo, A., Vellani, V. & McNaughton, P. A. Ion channels gated by heat. Proc. Natl. Acad. Sci. USA 96, 7658-7663 (1999). (Pubitemid 29328336)
3. Caterina, M. J., et al. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288, 306-313 (2000). (Pubitemid 30226186)
4. Basu, S. & Srivastava, P. Immunological role of neuronal receptor vanilloid receptor 1 expressed on dendritic cells. Proc. Natl. Acad. Sci. USA 102, 5120-5125 (2005).
5. Bodo, E., et al. A hot new twist to hair biology: involvement of vanilloid receptor-1 (VR1/TRPV1) signaling in human hair growth control. Am. J. Pathol. 166, 985-998 (2005). (Pubitemid 40524424)
6. Lu, T., Newton, C., Perkins, I., Friedman, H. & Klein, T. W. Role of cannabinoid receptors in Delta-9-tetrahydrocannabinol suppression of IL-12p40 in mouse bone marrow-derived dendritic cells infected with Legionella pneumophila. Eur. J. Pharmacol. 532, 170-177 (2006).
7. Beltran, J., Ghosh, A. K. & Basu, S. Immunotherapy of tumors with neuroimmune ligand capsaicin. J. Immunol. 178, 3260-3264 (2007). (Pubitemid 46333209)
8. Flemming, A. Red chillies tackle tumours. Nat. Rev. Drug Discov. 6, 269 (2007).
9. Steinman, R. M., Hawiger, D. & Nussenzweig, M. C. Tolerogenic dendritic cells. Annu. Rev. Immunol. 21, 685-711 (2003). (Pubitemid 37174545)
10. Uematsu, S., et al. Regulation of humoraland cellular gut immunity by lamina propria dendritic cells expressing Toll-like receptor 5. Nat. Immunol. 9, 769-776 (2008). (Pubitemid 351859160)
11. Iwasaki, A. Mucosal dendritic cells. Annu. Rev. Immunol. 25, 381-418 (2007). (Pubitemid 46697912)
12. Denning, T. L., Wang, Y. C., Patel, S. R., Williams, I. R. & Pulendran, B. Lamina propria macrophages and dendritic cells differentially induce regulatory and interleukin 17-producing T cell responses. Nat. Immunol. 8, 1086-1094 (2007). (Pubitemid 47423756)
13. Sun, C. M., et al. Smallintestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid. J. Exp. Med. 204, 1775-1785 (2007).
14. Mowat, A. M. Anatomical basis of tolerance and immunity to intestinalantigens. Nat. Rev. Immunol. 3, 331-341 (2003). (Pubitemid 37328685)
15. Kelsall, B. L. & Strober, W. Distinct populations of dendritic cells are present in the subepithelial dome and T cell regions of the murine Peyers patch. J. Exp. Med. 183, 237-247 (1996). (Pubitemid 26028763)
16. Turley, S. J., Lee, J. W., Dutton-Swain, N., Mathis, D. & Benoist, C. Endocrine self and gut non-self intersect in the pancreatic lymph nodes. Proc. Natl. Acad. Sci. USA 102, 17729-17733 (2005). (Pubitemid 41803565)
17. Horwitz, M. S., et al. Diabetes induced by Coxsackie virus: initiation by bystander damage and not molecular mimicry. Nat. Med. 4, 781-785 (1998). (Pubitemid 28331018)
18. Schmid, S., et al. Delayed exposure to wheat and barley proteins reduces diabetes incidence in non-obese diabetic mice. Clin. Immunol. 111, 108-118 (2004). (Pubitemid 38482089)
19. Wen, L., et al. Innate immunity and intestinal microbiota in the development of Type 1 diabetes. Nature 455, 1109-1113 (2008).
20. Hartmann, B., Bellmann, K., Ghiea, I., Kleemann, R. & Kolb, H. Oralinsulin for diabetes prevention in NOD mice: potentiation by enhancing Th2 cytokine expression in the gut through bacterialadjuvant. Diabetologia 40, 902-909 (1997). (Pubitemid 27316570)
21. Chatenoud, L., Thervet, E., Primo, J. & Bach, J. F. Anti-CD3 antibody induces long-term remission of overt autoimmunity in nonobese diabetic mice. Proc. Natl. Acad. Sci USA 91, 123-127 (1994). (Pubitemid 24018655)
22. Kurts, C., et al. Constitutive class I-restricted exogenous presentation of self antigens in vivo. J. Exp. Med. 184, 923-930 (1996). (Pubitemid 26313550)
23. Clare-Salzler, M. J., Brooks, J., Chai, A., Van Herle, K. & Anderson, C. Prevention of diabetes in nonobese diabetic mice by dendritic cell transfer. J. Clin. Invest. 90, 741-748 (1992).
24. Feili-Hariri, M., et al. Immunotherapy of NOD mice with bone marrowderived dendritic cells. Diabetes 48, 2300-2308 (1999). (Pubitemid 30395420)
25. Zhou, Y., et al. Oral tolerance to food-induced systemic anaphylaxis mediated by the C-type lectin SIGNR1. Nat. Med. 16, 1128-1133 (2010).
26. Manicassamy, S., et al. Activation of beta-catenin in dendritic cells regulates immunity versus tolerance in the intestine. Science 329, 849-853 (2010).
27. Moore, K. W., de Waal Malefyt, R., Coffman, R. L. & OGarra, A. Interleukin-10 and the interleukin-10 receptor. Annu. Rev. Immunol. 19, 683-765 (2001). (Pubitemid 32368050)
28. Caterina, M. J., et al. The capsaicin receptor: a heat-activated ion channelin the pain pathway. Nature 389, 816-824 (1997). (Pubitemid 27462969)
29. Patterson, L. M., Zheng, H., Ward, S. M. & Berthoud, H. R. Vanilloid receptor (VR1) expression in vagalafferent neurons innervating the gastrointestinal tract. Cell Tissue Res. 311, 277-287 (2003). (Pubitemid 36459667)
30. Robinson, D. R., McNaughton, P. A., Evans, M. L. & Hicks, G. A. Characterization of the primary spinalafferent innervation of the mouse colon using retrograde labelling. Neurogastroenterol Motil. 16, 113-124 (2004). (Pubitemid 38253528)
31. Ward, S. M., Bayguinov, J., Won, K. J., Grundy, D. & Berthoud, H. R. Distribution of the vanilloid receptor (VR1) in the gastrointestinal tract. J. Comp. Neurol. 465, 121-135 (2003). (Pubitemid 37075684)
32. Zhang, L., Jones, S., Brody, K., Costa, M. & Brookes, S. J. Thermosensitive transient receptor potential channels in vagalafferent neurons of the mouse. Am. J. Physiol. Gastrointest. Liver Physiol. 286, G983-991 (2004). (Pubitemid 38715661)
33. Hirotani, T., et al. The nuclear IkappaB protein IkappaBNS selectively inhibits lipopolysaccharide-induced IL-6 production in macrophages of the colonic lamina propria. J. Immunol. 174, 3650-3657 (2005). (Pubitemid 40354075)
34. Kamada, N., et al. Abnormally differentiated subsets of intestinal macrophage play a key role in Th1-dominant chronic colitis through excess production of IL-12 and IL-23 in response to bacteria. J. Immunol. 175, 6900-6908 (2005). (Pubitemid 41598935)
35. Smythies, L. E., et al. Human intestinal macrophages display profound inflammatory anergy despite avid phagocytic and bacteriocidalactivity. J. Clin. Invest. 115, 66-75 (2005). (Pubitemid 40385506)
36. Kang, J. H., Kim, C. S., Han, I. S., Kawada, T. & Yu, R. Capsaicin, a spicy component of hot peppers, modulates adipokine gene expression and protein release from obese-mouse adipose tissues and isolated adipocytes, and suppresses the inflammatory responses of adipose tissue macrophages. FEBS Lett. 581, 4389-4396 (2007). (Pubitemid 47368195)
37. Kang, J. H., et al. Dietary capsaicin reduces obesity-induced insulin resistance and hepatic steatosis in obese mice fed a high-fat diet. Obesity (Silver Spring) 18, 780-787 (2010).
38. Kang, J. H., et al. Dietary capsaicin attenuates metabolic dysregulation in genetically obese diabetic mice. J. Med. Food 14, 310-315 (2011).
39. You, S., et al. Key role of the GITR/GITRLigand pathway in the development of murine autoimmune diabetes: a potential therapeutic target. PLoS One 4, e7848 (2009).
40. Eizirik, D. L., Sandler, S. & Palmer, J. P. Repair of pancreatic beta-cells. A relevant phenomenon in early IDDM? Diabetes 42, 1383-1391 (1993). (Pubitemid 23277193)
41. Levy, B. D., Clish, C. B., Schmidt, B., Gronert, K. & Serhan, C. N. Lipid mediator class switching during acute inflammation: signals in resolution. Nat. Immunol. 2, 612-619 (2001). (Pubitemid 32677628)
42. Serhan, C. N., Chiang, N. & Van Dyke, T. E. Resolving inflammation: dualanti-inflammatory and pro-resolution lipid mediators. Nat. Rev. Immunol. 8, 349-361 (2008). (Pubitemid 351595216)
43. Eizirik, D. L., Colli, M. L. & Ortis, F. The role of inflammation in insulitis and beta-cell loss in type 1 diabetes. Nat. Rev. Endocrinol. 5, 219-226 (2009).
44. Wick, E. C., et al. Transient receptor potential vanilloid 1, calcitonin generelated peptide, and substance P mediate nociception in acute pancreatitis. Am. J. Physiol. Gastrointest. Liver Physiol. 290, G959-969 (2006).
45. Razavi, R., et al. TRPV1+ sensory neurons control beta cell stress and islet inflammation in autoimmune diabetes. Cell 127, 1123-1135 (2006). (Pubitemid 44894522)