Mechanosensitive duodenal afferents contribute to vagal modulation of inflammation in the rat

Journal of Physiology

Volumn 554, Issue 1, 2004, Pages 227-235

  Miao, Frederick Jia Pei ^a,b   Green, Paul G ^a,b   Levine, Jon D ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRADYKININ; CAPSAICIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; BALLOON DILATATION; CELIAC PLEXUS; CONTROLLED STUDY; DIET RESTRICTION; DOSE RESPONSE; DUODENUM; EXTRAVASATION; HYPOTHESIS; INFLAMMATION; INTESTINE INNERVATION; INTESTINE SURGERY; KNEE; MALE; NERVE CONDUCTION; NEUROENDOCRINE SYSTEM; NONHUMAN; POSTOPERATIVE PERIOD; PRIORITY JOURNAL; RAT; REVIEW; SENSORY NERVE CONDUCTION; STOMACH; SYNOVIAL FLUID; UPPER GASTROINTESTINAL TRACT; VAGOTOMY; VAGUS NERVE STIMULATION; ARTICLE; ELECTROSTIMULATION; GASTRECTOMY; NEUROMODULATION; SMALL INTESTINE RESECTION; VAGUS NERVE;

ANIMALS; BALLOON DILATATION; BRADYKININ; CAPSAICIN; DUODENUM; ELECTRIC STIMULATION; FASTING; INFLAMMATION; KNEE JOINT; MALE; MECHANORECEPTORS; NEURONS, AFFERENT; RATS; RATS, SPRAGUE-DAWLEY; VAGOTOMY; VAGUS NERVE;

EID: 0347126390     PISSN: 00223751     EISSN: None     Source Type: Journal    
DOI: 10.1113/jphysiol.2003.056804     Document Type: Review

References (58)

1. Andrews PL (1986). Vagal afferent innervation of the gastrointestinal tract. Prog Brain Res 67, 65-86.
2. Berthoud HR, Carlson NR & Powley TL (1991). Topography of efferent vagal innervation of the rat gastrointestinal tract. Am J Physiol 260, R200-207.
3. Berthoud HR, Kressel M & Neuhuber WL (1992). An anterograde tracing study of the vagal innervation of rat liver, portal vein and biliary system. Anat Embryol 186, 431-442.
4. Blackshaw LA & Grundy D (1990). Effects of cholecystokinin (cck-8) on two classes of gastroduodenal vagal afferent fibre. J Auton Nerv Syst 31, 191-201.
5. Bluthe RM, Walter V, Parnet P, Laye S, Lestage J, Verrier D, Poole S, Stenning BE, Kelley KW & Dantzer R (1994). Lipopolysaccharide induces sickness behaviour in rats by a vagal mediated mechanism. C R Acad Sci III 317, 499-503.
6. Carpenter DO (1990). Neural mechanisms of emesis. Can J Physiol Pharmacol 68, 230-236.
7. Carr J & Wilhelm DL (1964). The evaluation of increased vascular permeability in the skin of guinea pigs. Aust J Exp Biol Med Sci 42, 511-522.
8. Coderre TJ, Basbaum AI & Levine JD (1989). Neural control of vascular permeability: Interactions between primary afferents, mast cells, and sympathetic efferents. J Neurophysiol 62, 48-58.
9. Cottrell DF & Iggo A (1984). Tension receptors with vagal afferent fibres in the proximal duodenum and pyloric sphincter of sheep. J Physiol 354, 457-475.
10. Cullen JJ, Ephgrave KS & Caropreso DK (1996). Gastrointestinal myoelectric activity during endotoxemia. Am J Surg 171, 596-599.
11. Elenkov IJ, Wilder RL, Chrousos GP & Vizi ES (2000). The sympathetic nerve - an integrative interface between two supersystems: the brain and the immune system. Pharmacol Rev 52, 595-638.
12. Fujimiya M, Okumiya K & Kuwahara A (1997). Immunoelectron microscopic study of the luminal release of serotonin from rat enterochromaffin cells induced by high intraluminal pressure. Histochem Cell Biol 108, 105-113.
13. Gaykema RP, Goehler LE, Hansen MK, Maier SF & Watkins LR (2000). Subdiaphragmatic vagotomy blocks interleukin-1beta-induced fever but does not reduce il-1beta levels in the circulation. Auton Neurosci 85, 72-77.
14. Goehler LE, Gaykema RP, Hansen MK, Anderson K, Maier SF & Watkins LR (2000). Vagal immune-to-brain communication: a visceral chemosensory pathway. Auton Neurosci 85, 49-59.
15. Green PG, Miao FJ, Janig W & Levine JD (1995). Negative feedback neuroendocrine control of the inflammatory response in rats. J Neurosci 15, 4678-4686.
16. Grundy D (1988). Speculations on the structure/function relationship for vagal and splanchnic afferent endings supplying the gastrointestinal tract. J Auton Nerv Syst 22, 175-180.
17. Grundy D (1993). Mechanoreceptors in the gastrointestinal tract. J Smooth Muscle Res 29, 37-46.
18. Grundy D & Scratchard T (1989). Sensory afferents from the gastrointestinal tract. In Handbook of physiology The Gastrointestinal System, ed Schultz SG, Wood JD, & Rauner BB, Vol 1, pp. 593-620. American Physiological Society, Bethesda, MD.
19. Hansen MK, O'Connor KA, Goehler LE, Watkins LR & Maier SF (2001). The contribution of the vagus nerve in interleukin-1beta-induced fever is dependent on dose. Am J Physiol Regul Integr Comp Physiol 280, R929-934.
20. Hargreaves KM, Roszkowski MT & Swift JQ (1993). Bradykinin and inflammatory pain. Agents Actions (suppl.) 41, 65-73.
21. Hebel R & Stromberg MW (1976). Anatomy of the Laboratory Rat. Williams & Wilkins, Baltimore.
22. Hermann GE, Tovar CA & Rogers RC (2003). Tnfalpha-stimulation of cfos-activation of neurons in the solitary nucleus is suppressed by tnfr: Fc adsorbant construct in the dorsal vagal complex. Brain Res 976, 69-74.
23. Jänig W, Khasar SG, Levine JD & Miao FJ (2000). The role of vagal visceral afferents in the control of nociception. Prog Brain Res 122, 273-287.
24. Khasar SG, Reichling DB, Green PG, Isenberg WM & Levine JD (2003). Fasting is a physiological stimulus of vagus-mediated enhancement of nociception in the female rat. Neuroscience 119, 215-221.
25. Kirchner A, Birklein F, Stefan H & Handwerker HO (2000). Left vagus nerve stimulation suppresses experimentally induced pain. Neurology 55, 1167-1171.
26. Krolczyk G, Zurowski D, Sobocki J, Slowiaczek MP, Laskiewicz J, Matyja A, Zaraska K, Zaraska W & Thor PJ (2001). Effects of continuous microchip (mc) vagal neuromodulation on gastrointestinal function in rats. J Physiol Pharmacol 52, 705-715.
27. Kumagai S (1989). Intestinal absorption and excretion of aflatoxin in rats. Toxicol Appl Pharmacol 97, 88-97.
28. Mei N (1983). Recent studies on intestinal vagal afferent innervation. Functional implications. J Auton Nerv Syst 9, 199-206.
29. Miao FJ, Benowitz NL & Levine JD (2001a). Endogenous opioids suppress activation of nociceptors by sub-nanomolar nicotine. Br J Pharmacol 133, 23-28.
30. Miao FJ, Dallman MF, Benowitz NL, Basbaum AI & Levine JD (1993). Adrenal medullary modulation of the inhibition of bradykinin-induced plasma extravasation by intrathecal nicotine. J Pharmacol Exp Ther 264, 839-844.
31. Miao FJ, Green PG, Benowitz N & Levine JD (2003). Vagal modulation of spinal nicotine-induced inhibition of the inflammatory response mediated by descending antinociceptive controls. Neuropharmacology 45, 605-611.
32. Miao FJ, Janig W, Dallman MF, Benowitz NL, Heller PH, Basbaum AI & Levine JD (1994). Role of vagal afferents and spinal pathways modulating inhibition of bradykinin-induced plasma extravasation by intrathecal nicotine. J Neurophysiol 72, 1199-1207.
33. Miao FJ, Janig W, Green PG & Levine JD (1996). Inhibition of bradykinin-induced synovial plasma extravasation produced by intrathecal nicotine is mediated by the hypothalamopituitary adrenal axis. J Neurophysiol 76, 2813-2821.
34. Miao FJ, Janig W, Green PG & Levine JD (1997a). Inhibition of bradykinin-induced plasma extravasation produced by noxious cutaneous and visceral stimuli and its modulation by vagal activity. J Neurophysiol 78, 1285-1292.
35. Miao FJ, Janig W, Jasmin L & Levine JD (2001b). Spino-bulbo-spinal pathway mediating vagal modulation of nociceptive-neuroendocrine control of inflammation in the rat. J Physiol 532, 811-822.
36. Miao FJ, Janig W & Levine JD (1997b). Vagal branches involved in inhibition of bradykinin-induced synovial plasma extravasation by intrathecal nicotine and noxious stimulation in the rat. J Physiol (Lond) 498 (2), 473-481.
37. Miao FJ, Janig W & Levine JD (2000). Nociceptive neuroendocrine negative feedback control of neurogenic inflammation activated by capsaicin in the rat paw: Role of the adrenal medulla. J Physiol 527, 601-610.
38. Miao FJ & Lee TJ (1989). Effects of bilirubin on cerebral arterial tone in vitro. J Cereb Blood Flow Metab 9, 666-674.
39. Miao FJ & Levine JD (1999). Neural and endocrine mechanisms mediating noxious stimulus-induced inhibition of bradykinin plasma extravasation in the rat. J Pharmacol Exp Ther 291, 1028-1037.
40. Moss HE & Sanger GJ (1990). The effects of granisetron, ics 205-930 and ondansetron on the visceral pain reflex induced by duodenal distension. Br J Pharmacol 100, 497-501.
41. Ness TJ, Randich A, Fillingim R, Faught RE & Backensto EM (2001). Left vagus nerve stimulation suppresses experimentally induced pain. Neurology 56, 985-986.
42. Niijima A (1983). Glucose-sensitive afferent nerve fibers in the liver and their role in food intake and blood glucose regulation. J Auton Nerv Syst 9, 207-220.
43. Niijima A (1984). The effect of d-glucose on the firing rate of glucose-sensitive vagal afferents in the liver in comparison with the effect of 2-deoxy-d-glucose. J Auton Nerv Syst 10, 255-260.
44. Phillips RJ, Baronowsky EA & Powley TL (1997). Afferent innervation of gastrointestinal tract smooth muscle by the hepatic branch of the vagus. J Comp Neurol 384, 248-270.
45. Phillips RJ & Powley TL (1998). Gastric Volume detection after selective vagotomies in rats. Am J Physiol 274, R1626-R1638.
46. Phillips RJ & Powley TL (2000). Tension and stretch receptors in gastrointestinal smooth muscle: Re-evaluating vagal mechanoreceptor electrophysiology. Brain Res Brain Res Rev 34, 1-26.
47. Raybould H (2001). Primary afferent response to signals in the intestinal lumen. J Physiol 530, 343.
48. Regoli D & Barabe J (1980). Pharmacology of bradykinin and related kinins. Pharmacol Rev 32, 1-46.
49. Schwartz GJ & Moran TH (1998). Duodenal nutrient exposure elicits nutrient-specific gut motility and vagal afferent signals in rat. Am J Physiol 274, R1236-1242.
50. Schwartz GJ, Tougas G & Moran TH (1995). Integration of vagal afferent responses to duodenal loads and exogenous CCK in rats. Peptides 16, 707-711.
51. Simons CT, Kulchitsky VA, Sugimoto N, Homer LD, Szekely M & Romanovsky AA (1998). Signaling the brain in systemic inflammation: which vagal branch is involved in fever genesis? Am J Physiol 275, R63-R68.
52. Sun FJ, Kaur S, Ziemer D, Banerjee S, Samuelson LC & De Lisle RC (2003). Decreased gastric bacterial killing and up-regulation of protective genes in small intestine in gastrin-deficient mouse. Dig Dis Sci 48, 976-985.
53. Swift JQ, Garry MG, Roszkowski MT & Hargreaves KM (1993). Effect of flurbiprofen on tissue levels of immunoreactive bradykinin and acute postoperative pain. J Oral Maxillofac Surg 51, 112-116; discussion 116-117.
54. Watkins LR, Wiertelak EP, Goehler LE, Mooney-Heiberger K, Martinez J, Furness L, Smith KP & Maier SF (1994a). Neurocircuitry of illness-induced hyperalgesia. Brain Res 639, 283-299.
55. Watkins LR, Wiertelak EP, Goehler LE, Smith KP, Martin D & Maier SF (1994b). Characterization of cytokine-induced hyperalgesia. Brain Res 654, 15-26.
56. Webster JI, Tonelli L & Sternberg EM (2002). Neuroendocrine regulation of immunity. Annu Rev Immunol 20, 125-163.
57. Wei JY & Wang YH (2000). Effect of cck pretreatment on the cck sensitivity of rat polymodal gastric vagal afferent in vitro. Am J Physiol Endocrinol Metab 279, E695-706.
58. Zhu JX, Zhu XY, Owyang C & Li Y (2001). Intestinal serotonin acts as a paracrine substance to mediate vagal signal transmission evoked by luminal factors in the rat. J Physiol 530, 431-442.