Capsaicin-sensitive vagal afferent neurons contribute to the detection of pathogenic bacterial colonization in the gut

Journal of Neuroimmunology

Volumn 257, Issue 1-2, 2013, Pages 36-45

  Riley, T P ^a   Neal McKinney, J M ^a   Buelow, D R ^a   Konkel, M E ^a   Simasko, S M ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Campylobacter; Cholinergic anti inflammatory pathway; LPS; Salmonella; TNF ; Vagus

Indexed keywords

CAPSAICIN; LIPOPOLYSACCHARIDE; PROTEIN C FOS; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTONOMIC INNERVATION; BACTERIAL COLONIZATION; BACTERIUM DETECTION; CAMPYLOBACTER ENTERITIS; CELL ACTIVATION; CELL FUNCTION; CONTROLLED STUDY; HOST PATHOGEN INTERACTION; INTRACELLULAR SIGNALING; MOUSE; NERVE CELL CULTURE; NERVE CELL STIMULATION; NEUROANATOMY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SALMONELLOSIS; SENSITIVITY ANALYSIS; SENSORY NERVE CELL; SOLITARY TRACT NUCLEUS; UPREGULATION; VAGAL AFFERENT NEURON;

ANIMALS; CAMPYLOBACTER INFECTIONS; CAPSAICIN; COLONY COUNT, MICROBIAL; GASTROINTESTINAL TRACT; HUMANS; INFLAMMATION; MALE; MICE; MICE, INBRED BALB C; NEURONS, AFFERENT; RATS; RATS, SPRAGUE-DAWLEY; SALMONELLA INFECTIONS; VAGUS NERVE;

EID: 84875811944     PISSN: 01655728     EISSN: 18728421     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2013.01.009     Document Type: Article

References (58)

1. Andersson U., Tracey K.J. Reflex principles of immunological homeostasis. Annu. Rev. Immunol. 2012, 30:313-335.
2. Artis D. Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut. Nat. Rev. Immunol. 2008, 8:411-420.
3. Bell J.A., St Charles J.L., Murphy A.J., Rathinam V.A., Plovanich-Jones A.E., Stanley E.L., Wolf J.E., Gettings J.R., Whittam T.S., Manfield L.S. Multiple factors interact to produce responses resembling spectrum of human disease in Campylobacter jejuni infected C57BL/6 IL-10-/- mice. BMC Microbiol. 2009, 9:57.
4. Berthoud H.R., Patterson L.M., Willing A.E., Mueller K., Neuhuber W.L. Capsaicin-resistant vagal afferent fibers in the rat gastrointestinal tract: anatomical identification and functional integrity. Brain Res. 1997, 746:195-206.
5. Bluthe R.M., Michaud B., Kelley K.W., Dantzer R. Vagotomy blocks behavioural effects of interleukin-1 injected via the intraperitoneal route but not via other systemic routes. Neuroreport 1996, 7:2823-2827.
6. Borovikova L.V., Ivanova S., Zhang M., Yang H., Botchkina G.I., Watkins L.R., Wang H., Abumrad N., Eaton J.W., Tracey K.J. Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature 2000, 405:458-462.
7. Bratton B.O., Martelli D., McKinley M.J., Trevaks D., Anderson C.R., Mcallen R.M. Neural regulation of inflammation: no neural connection from vagus to splenic sympathetic neurons. Exp. Physiol. 2012, 45:1080-1085.
8. Bret-Dibat J.L., Bluthe R.M., Kent S., Kelley K.W., Dantzer R. Lipopolysaccharide and interleukin-1 depress food-motivated behavior in mice by a vagal-mediated mechanism. Brain Behav. Immun. 1995, 9:242-246.
9. Caterina M.J., Schumacher M.A., Tominaga M., Rosen T.A., Levine J.D., Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 1997, 389:816-824.
10. Danese S., Sans M., Fiocchi C. Inflammatory bowel disease: the role of environmental factors. Autoimmun. Rev. 2004, 3:394-400.
11. De A., Krueger J.M., Simasko S.M. Tumor necrosis factor alpha increases cytosolic calcium responses to AMPA and KCl in primary cultures of rat hippocampal neurons. Brain Res. 2003, 981:133-142.
12. Diogenes A., Ferraz C.C., Akopian A.N., Henry M.A., Hargreaves K.M. LPS sensitizes TRPV1 via activation of TLR4 in trigeminal sensory neurons. J. Dent. Res. 2011, 90:759-764.
13. Dorrell N., Wren B.W. The second century of Campylobacter research: recent advances, new opportunities and old problems. Curr. Opin. Infect. Dis. 2007, 20:514-518.
14. Ek M., Kurosawa M., Lundeberg T., Ericsson A. Activation of vagal afferents after intravenous injection of interleukin-1beta: role of endogenous prostaglandins. J. Neurosci. 1998, 18:9471-9479.
15. Elmquist J.K., Scammell T.E., Jacobson C.D., Saper C.B. Distribution of Fos-like immunoreactivity in the rat brain following intravenous lipopolysaccharide administration. J. Comp. Neurol. 1996, 371:85-103.
16. Emch G.S., Hermann G.E., Rogers R.C. TNF-alpha-induced c-Fos generation in the nucleus of the solitary tract is blocked by NBQX and MK-801. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2001, 281:R1394-R1400.
17. Fleshner M., Goehler L.E., Hermann J., Relton J.K., Maier S.F., Watkins L.R. Interleukin-1 beta induced corticosterone elevation and hypothalamic NE depletion is vagally mediated. Brain Res. Bull. 1995, 37:605-610.
18. Fleshner M., Silbert L., Deak T., Goehler L.E., Martin D., Watkins L.R., Maier S.F. TNF-alpha-induced corticosterone elevation but not serum protein or corticosteroid binding globulin reduction is vagally mediated. Brain Res. Bull. 1997, 44:701-706.
19. Fleshner M., Goehler L.E., Schwartz B.A., Mcgorry M., Martin D., Maier S.F., Watkins L.R. Thermogenic and corticosterone responses to intravenous cytokines (IL-1beta and TNF-alpha) are attenuated by subdiaphragmatic vagotomy. J. Neuroimmunol. 1998, 86:134-141.
20. Gaykema R.P., Goehler L.E., Lyte M. Brain response to cecal infection with Campylobacter jejuni: analysis with Fos immunohistochemistry. Brain Behav. Immun. 2004, 18:238-245.
21. Goehler L.E., Busch C.R., Tartaglia N., Relton J., Sisk D., Maier S.F., Watkins L.R. Blockade of cytokine induced conditioned taste aversion by subdiaphragmatic vagotomy: further evidence for vagal mediation of immune-brain communication. Neurosci. Lett. 1995, 185:163-166.
22. Goehler L.E., Relton J.K., Dripps D., Kiechle R., Tartaglia N., Maier S.F., Watkins L.R. Vagal paraganglia bind biotinylated interleukin-1 receptor antagonist: a possible mechanism for immune-to-brain communication. Brain Res. Bull. 1997, 43:357-364.
23. Goehler L.E., Gaykema R.P., Hammack S.E., Maier S.F., Watkins L.R. Interleukin-1 induces c-Fos immunoreactivity in primary afferent neurons of the vagus nerve. Brain Res. 1998, 804:306-310.
24. Goehler L.E., Gaykema R.P., Opitz N., Reddaway R., Badr N., Lyte M. Activation in vagal afferents and central autonomic pathways: early responses to intestinal infection with Campylobacter jejuni. Brain Behav. Immun. 2005, 19:334-344.
25. Hansen M.K., Krueger J.M. Subdiaphragmatic vagotomy blocks the sleep- and fever-promoting effects of interleukin-1beta. Am. J. Physiol. 1997, 273:R1246-R1253.
26. Hansen M.K., O'Connor K.A., Goehler L.E., Watkins L.R., Maier S.F. The contribution of the vagus nerve in interleukin-1beta-induced fever is dependent on dose. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2001, 280:R929-R934.
27. Hermann G.E., Rogers R.C. TNFalpha: a trigger of autonomic dysfunction. Neuroscientist 2008, 14:53-67.
28. Hermann G.E., Emch G.S., Tovar C.A., Rogers R.C. c-Fos generation in the dorsal vagal complex after systemic endotoxin is not dependent on the vagus nerve. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2001, 280:R289-R299.
29. Holzer P. Capsaicin as a tool for studying sensory neuron functions. Adv. Exp. Med. Biol. 1991, 298:3-16.
30. Hooper L.V., Macpherson A.J. Immune adaptations that maintain homeostasis with the intestinal microbiota. Nat. Rev. Immunol. 2010, 10:159-169.
31. Hosoi T., Okuma Y., Matsuda T., Nomura Y. Novel pathway for LPS-induced afferent vagus nerve activation: possible role of nodose ganglion. Auton. Neurosci. 2005, 120:104-107.
32. Hulisz D. The burden of illness of irritable bowel syndrome: current challenges and hope for the future. J. Manag. Care Pharm. 2004, 10:299-309.
33. Jesudason M.V., Hentges D.J., Pongpech P. Colonization of mice by Campylobacter jejuni. Infect. Immun. 1989, 57:2279-2282.
34. Jotwani R., Tanaka Y., Watanabe K., Tanaka K., Kato N., Ueno K. Cytokine stimulation during Salmonella typhimurium sepsis in Itys mice. J. Med. Microbiol. 1995, 42:348-352.
35. Koller H., Thiem K., Siebler M. Tumour necrosis factor-alpha increases intracellular Ca2+ and induces a depolarization in cultured astroglial cells. Brain 1996, 119(Pt 6):2021-2027.
36. Konsman J.P., Kelley K., Dantzer R. Temporal and spatial relationships between lipopolysaccharide-induced expression of Fos, interleukin-1beta and inducible nitric oxide synthase in rat brain. Neuroscience 1999, 89:535-548.
37. Li B.Y., Schild J.H. Electrophysiological and pharmacological validation of vagal afferent fiber type of neurons enzymatically isolated from rat nodose ganglia. J. Neurosci. Methods 2007, 164:75-85.
38. Liu C.Y., Mueller M.H., Grundy D., Kreis M.E. Vagal modulation of intestinal afferent sensitivity to systemic LPS in the rat. Am. J. Physiol. Gastrointest. Liver Physiol. 2007, 292:G1213-G1220.
39. Maloy K.J., Powrie F. Intestinal homeostasis and its breakdown in inflammatory bowel disease. Nature 2011, 474:298-306.
40. Mascarucci P., Perego C., Terrazzino S., De Simoni M.G. Glutamate release in the nucleus tractus solitarius induced by peripheral lipopolysaccharide and interleukin-1 beta. Neuroscience 1998, 86:1285-1290.
41. Mueller M.H., Kampitoglou D., Glatzle J., Hahn J., Kreis M.E. Systemic capsaicin inhibits neuronal activation in the brainstem during postoperative ileus in the mouse. Langenbecks Arch. Surg. 2006, 391:88-95.
42. Nevola J.J., Stocker B.A., Laux D.C., Cohen P.S. Colonization of the mouse intestine by an avirulent Salmonella typhimurium strain and its lipopolysaccharide-defective mutants. Infect. Immun. 1985, 50:152-159.
43. Niijima A. The afferent discharges from sensors for interleukin 1 beta in the hepatoportal system in the anesthetized rat. J. Auton. Nerv. Syst. 1996, 61:287-291.
44. Pollock J., McFarlane S.M., Connell M.C., Zehavi U., Vandenabeele P., MacEwan D.J., Scott R.H. TNF-alpha receptors simultaneously activate Ca2+ mobilisation and stress kinases in cultured sensory neurones. Neuropharmacology 2002, 42:93-106.
45. Rogers R.C., Van Meter M.J., Hermann G.E. Tumor necrosis factor potentiates central vagal afferent signaling by modulating ryanodine channels. J. Neurosci. 2006, 26:12642-12646.
46. Rosas-Ballina M., Ochani M., Parrish W.R., Ochani K., Harris Y.T., Huston J.M., Chavan S., Tracey K.J. Splenic nerve is required for cholinergic antiinflammatory pathway control of TNF in endotoxemia. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:11008-11013.
47. Rosas-Ballina M., Olofsson P.S., Ochani M., Valdes-Ferrer S.I., Levine Y.A., Reardon C., Tusche M.W., Pavlov V.A., Andersson U., Chavan S., Mak T.W., Tracey K.J. Acetylcholine-synthesizing T cells relay neural signals in a vagus nerve circuit. Science 2011, 334:98-101.
48. Sagar S.M., Price K.J., Kasting N.W., Sharp F.R. Anatomic patterns of Fos immunostaining in rat brain following systemic endotoxin administration. Brain Res. Bull. 1995, 36:381-392.
49. Simasko S.M., Wiens J., Karpiel A., Covasa M., Ritter R.C. Cholecystokinin increases cytosolic calcium in a subpopulation of cultured vagal afferent neurons. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2002, 283:R1303-R1313.
50. Tracey K.J. The inflammatory reflex. Nature 2002, 420:853-859.
51. Tracey K.J. Physiology and immunology of the cholinergic antiinflammatory pathway. J. Clin. Invest. 2007, 117:289-296.
52. Tracey K.J. Reflex control of immunity. Nat. Rev. Immunol. 2009, 9:418-428.
53. Van Der Zanden E.P., Snoek S.A., Heinsbroek S.E., Stanisor O.I., Verseijden C., Boeckxstaens G.E., Peppelenbosch M.P., Greaves D.R., Gordon S., De Jonge W.J. Vagus nerve activity augments intestinal macrophage phagocytosis via nicotinic acetylcholine receptor alpha4beta2. Gastroenterology 2009, 137:1029-1039. (1039 e1-4).
54. Vuckovic D., Abram M., Doric M. Primary Campylobacter jejuni infection in different mice strains. Microb. Pathog. 1998, 24:263-268.
55. Wang X., Wang B.R., Zhang X.J., Xu Z., Ding Y.Q., Ju G. Evidences for vagus nerve in maintenance of immune balance and transmission of immune information from gut to brain in STM-infected rats. World J. Gastroenterol. 2002, 8:540-545.
56. Wang H., Yu M., Ochani M., Amella C.A., Tanovic M., Susarla S., Li J.H., Wang H., Yang H., Ulloa L., Al-Abed Y., Czura C.J., Tracey K.J. Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation. Nature 2003, 421:384-388.
57. Watkins L.R., Goehler L.E., Relton J.K., Tartaglia N., Silbert L., Martin D., Maier S.F. Blockade of interleukin-1 induced hyperthermia by subdiaphragmatic vagotomy: evidence for vagal mediation of immune-brain communication. Neurosci. Lett. 1995, 183:27-31.
58. Young V.B., Schauer D.B., Fox J.G. Animal models of Campylobacter infection. Campylobacter 2000, ASM Press, Washington, D.C. 2nd ed. M.J. Blaser (Ed.).