Efferent-like roles of afferent neurons in the gut: Blood flow regulation and tissue protection

Autonomic Neuroscience: Basic and Clinical

Volumn 125, Issue 1-2, 2006, Pages 70-75

  Holzer, Peter ^a  

^a MEDICAL UNIVERSITY OF GRAZ   (Austria)

Author keywords

Afferent neurons; Brainstem; c Fos; Calcitonin gene related peptide; Capsaicin; Chemonociception; Cytokines; Efferent like function of afferent neurons; Gastric mucosal protection; Gut brain axis; Hypersensitivity; Mucosal blood flow; Neurogenic inflammation; TRPV1; Vagus nerve

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; CAPSAICIN; CYTOKINE; NEUROTRANSMITTER; NITRIC OXIDE; VANILLOID RECEPTOR 1;

AUTONOMIC NERVOUS SYSTEM; BLOOD FLOW; CENTRAL NERVOUS SYSTEM; CHEMORECEPTOR; DIFFUSION; DIGESTIVE SYSTEM INFLAMMATION; DIGESTIVE SYSTEM INJURY; DRUG TARGETING; DUODENUM MUCOSA; DYSPEPSIA; EFFERENT NERVE; EMOTIONALITY; ESOPHAGUS MUCOSA; FUNCTIONAL ASSESSMENT; GASTROINTESTINAL MUCOSA; GASTROINTESTINAL PAIN; HOMEOSTASIS; HYPERALGESIA; HYPEREMIA; INNERVATION; INTESTINE; INTESTINE BLOOD FLOW; IRRITABLE COLON; NERVE ENDING; NERVE FUNCTION; NERVE STIMULATION; NEUROENDOCRINOLOGY; NOCICEPTION; NOCICEPTIVE STIMULATION; NONHUMAN; PATHOPHYSIOLOGY; PERIPHERAL NERVE; PRIORITY JOURNAL; PROTECTION; REGULATORY MECHANISM; REVIEW; RODENT; SENSITIZATION; SENSORY NERVE; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; SPINAL NERVE; STOMACH ACID; STOMACH MUCOSA; TISSUE REPAIR; VAGUS NERVE; WOUND HEALING;

ANIMALS; GASTROINTESTINAL TRACT; HUMANS; NEURONS, AFFERENT; REGIONAL BLOOD FLOW;

EID: 33646126930     PISSN: 15660702     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.autneu.2006.01.004     Document Type: Review

References (45)

1. Akiba Y., Guth P.H., Engel E., Nastaskin I., and Kaunitz J.D. Acid-sensing pathways of rat duodenum. Am. J. Physiol. 277 (1999) G268-G274
2. Akiba Y., Nakamura M., Nagata H., Kaunitz J.D., and Ishii H. Acid-sensing pathways in rat gastrointestinal mucosa. J. Gastroenterol. 37 Suppl. 14 (2002) 133-138
3. Berthoud H.-R., and Neuhuber W.L. Functional and chemical anatomy of the afferent vagal system. Auton. Neurosci. 85 (2000) 1-17
4. Bielefeldt K., Ozaki N., and Gebhart G.F. Experimental ulcers alter voltage-sensitive sodium currents in rat gastric sensory neurons. Gastroenterology 122 (2002) 394-405
5. Caterina M.J., Schumacher M.A., Tominaga M., Rosen T.A., Levine J.D., and Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389 (1997) 816-824
6. Cervero F. Sensory innervation of the viscera: peripheral basis of visceral pain. Physiol. Rev. 74 (1994) 95-138
7. Chen R.Y.Z., Li D.S., and Guth P.H. Role of calcitonin gene-related peptide in capsaicin-induced gastric submucosal arteriolar dilation. Am. J. Physiol. 262 (1992) H1350-H1355
8. Danzer M., Jocic M., Samberger C., Painsipp E., Bock E., Pabst M.-A., Crailsheim K., Schicho R., Lippe I.T., and Holzer P. Stomach-brain communication by vagal afferents in response to luminal acid backdiffusion, gastrin, and gastric acid secretion. Am. J. Physiol. 286 (2004) G403-G411
9. In: Drossman D.A., Corazziari E., Talley N.J., Thompson W.G., and Whitehead W.E. (Eds). Rome II. The Functional Gastrointestinal Disorders. Second edition (2000), Degnon Associates, McLean
10. Gebhart G.F. Pathobiology of visceral pain: molecular mechanisms and therapeutic implications: IV. Visceral afferent contributions to the pathobiology of visceral pain. Am. J. Physiol. 278 (2000) G834-G838
11. Goehler L.E., Gaykema R.P.A., Hansen M.K., Anderson K., Maier S.F., and Watkins L.R. Vagal immune-to-brain communication: a visceral chemosensory pathway. Auton. Neurosci. 85 (2000) 49-59
12. Grundy D. Neuroanatomy of visceral nociception: vagal and splanchnic afferent. Gut 51 Suppl. 1 (2002) i2-i5
13. Heinemann A., Jocic M., Herzeg G., and Holzer P. Tachykinin inhibition of acid-induced gastric hyperaemia in the rat. Br. J. Pharmacol. 119 (1996) 1525-1532
14. Holzer P. Local effector functions of capsaicin-sensitive sensory nerve endings: involvement of tachykinins, calcitonin gene-related peptide and other neuropeptides. Neuroscience 24 (1988) 739-768
15. Holzer P. Capsaicin: cellular targets, mechanisms of action, and selectivity for thin sensory neurons. Pharmacol. Rev. 43 (1991) 143-201
16. Holzer P. Neural emergency system in the stomach. Gastroenterology 114 (1998) 823-839
17. Holzer P. Neurogenic vasodilatation and plasma leakage in the skin. Gen. Pharmacol. 30 (1998) 5-11
18. Holzer P. Sensory neurone responses to mucosal noxae in the upper gut: relevance to mucosal integrity and gastrointestinal pain. Neurogastroenterol. Motil. 14 (2002) 459-475
19. Holzer P. Role of sensory neurons in mucosal protection from acid-induced lesions in the foregut. In: Dal Negro R.W., Geppetti P., and Morice A.H. (Eds). Experimental and Clinical Pharmacology of Gastroesophageal Reflux-Induced Asthma (2002), Pacini, Pisa 25-33
20. Holzer P. Gastrointestinal pain in functional bowel disorders: sensory neurons as novel drug targets. Expert Opin. Ther. Targets 8 (2004) 107-123
21. Holzer P., and Barthó L. Sensory neurons in the intestine. In: Geppetti P., and Holzer P. (Eds). Neurogenic Inflammation (1996), CRC Press, Boca Raton 153-167
22. Holzer P., and Lippe I.T. Stimulation of afferent nerve endings by intragastric capsaicin protects against ethanol-induced damage of gastric mucosa. Neuroscience 27 (1988) 981-987
23. Holzer P., and Maggi C.A. Dissociation of dorsal root ganglion neurons into afferent and efferent-like neurons. Neuroscience 86 (1998) 389-398
24. Holzer P., and Sametz W. Gastric mucosal protection against ulcerogenic factors in the rat mediated by capsaicin-sensitive afferent neurons. Gastroenterology 91 (1986) 975-981
25. Holzer P., Pabst M.-A., Lippe I.T., Peskar B.M., Peskar B.A., Livingston E.H., and Guth P.H. Afferent nerve-mediated protection against deep mucosal damage in the rat stomach. Gastroenterology 98 (1990) 838-848
26. Holzer P., Livingston E.H., and Guth P.H. Sensory neurons signal for an increase in rat gastric mucosal blood flow in the face of pending acid injury. Gastroenterology 101 (1991) 416-423
27. Holzer P., Wachter C., Jocic M., and Heinemann A. Vascular bed-dependent roles of the peptide CGRP and nitric oxide in acid-evoked hyperaemia of the rat stomach. J. Physiol. (Lond.) 480 (1994) 575-585
28. Holzer P., Danzer M., Schicho R., Samberger C., Painsipp E., and Lippe I.T. Vagal afferent input from the acid-challenged rat stomach to the brainstem: enhancement by interleukin-1beta. Neuroscience 129 (2004) 439-445
29. Jancsó N. Role of the nerve terminals in the mechanism of inflammatory reactions. Bull. Millard Fillmore Hosp. 7 (1960) 53-77
30. Konsman J.P., Parnet P., and Dantzer R. Cytokine-induced sickness behaviour: mechanisms and implications. Trends Neurosci. 25 (2002) 154-159
31. Lamb K., Kang Y.M., Gebhart G.F., and Bielefeldt K. Gastric inflammation triggers hypersensitivity to acid in awake rats. Gastroenterology 125 (2003) 1410-1418
32. Lembeck F., and Giere W. Otto Loewi (1968), Springer, Berlin
33. Li D.S., Raybould H.E., Quintero E., and Guth P.H. Calcitonin gene-related peptide mediates the gastric hyperemic response to acid back-diffusion. Gastroenterology 102 (1992) 1124-1128
34. Lippe I.T., and Holzer P. Participation of endothelium-derived nitric oxide but not prostacyclin in the gastric mucosal hyperaemia due to acid back-diffusion. Br. J. Pharmacol. 105 (1992) 708-714
35. Maggi C.A. Tachykinins and calcitonin gene-related peptide (CGRP) as co-transmitters released from peripheral endings of sensory nerves. Prog. Neurobiol. 45 (1995) 1-98
36. Michl T., Jocic M., Heinemann A., Schuligoi R., and Holzer P. Vagal afferent signaling of a gastric mucosal acid insult to medullary, pontine, thalamic, hypothalamic and limbic, but not cortical, nuclei of the rat brain. Pain 92 (2001) 19-27
37. Raybould H.E., Sternini C., Eysselein V.E., Yoneda M., and Holzer P. Selective ablation of spinal afferent neurons containing CGRP attenuates gastric hyperemic response to acid. Peptides 13 (1992) 249-254
38. Schicho R., Schemann M., Holzer P., and Lippe I.T. Mucosal acid challenge activates nitrergic neurons in the myenteric plexus of the rat stomach. Am. J. Physiol. 281 (2001) G1316-G1321
39. Schicho R., Schemann M., Pabst M.-A., Holzer P., and Lippe I.T. Capsaicin-sensitive extrinsic afferents are involved in acid-induced activation of distinct myenteric neurons in the rat stomach. Neurogastroenterol. Motil. 15 (2003) 33-44
40. Schicho R., Florian W., Liebmann I., Holzer P., and Lippe I.T. Increased expression of TRPV1 receptor in dorsal root ganglia by acid insult of the rat gastric mucosa. Eur. J. Neurosci. 19 (2004) 1811-1818
41. Schuligoi R., Jocic M., Heinemann A., Schöninkle E., Pabst M.A., and Holzer P. Gastric acid-evoked c-fos messenger RNA expression in rat brainstem is signaled by capsaicin-resistant vagal afferents. Gastroenterology 115 (1998) 649-660
42. Stroff T., Plate S., Seyed Ebrahim J., Ehrlich K.-H., Respondek M., and Peskar B.M. Tachykinin-induced increase in gastric mucosal resistance: role of primary afferent neurons, CGRP, and NO. Am. J. Physiol. 271 (1996) G1017-G1027
43. Szolcsányi J., and Barthó L. Impaired defense mechanism to peptic ulcer in the capsaicin-desensitized rat. In: Mózsik G., Hänninen O., and Jávor T. (Eds). Gastrointestinal Defense Mechanisms (1981), Akadémiai Kiadó, Budapest 39-51
44. Traub R.J., Sengupta J.N., and Gebhart G.F. Differential c-fos expression in the nucleus of the solitary tract and spinal cord following noxious gastric distention in the rat. Neuroscience 74 (1996) 873-884
45. Yeoh K.G., Kang J.Y., Yap I., Guan R., Tan C.C., Wee A., and Teng C.H. Chili protects against aspirin-induced gastroduodenal mucosal injury in humans. Dig. Dis. Sci. 40 (1995) 580-583