Immunohistochemical characterization of the innervation of human colonic mesenteric and submucosal blood vessels

Neurogastroenterology and Motility

Volumn 20, Issue 11, 2008, Pages 1212-1226

  De Fontgalland, D ^a   Wattchow, D A ^b   Costa, M ^a   Brookes, S J H ^a  

^a FLINDERS UNIVERSITY   (Australia)

^b FLINDERS MEDICAL CENTRE   (Australia)

Author keywords

Artery; Enteric; Human; Intestinal vessels; Mesentery; Perivascular nerves; Sensory; Submucosa; Sympathetic; Vein

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; ENKEPHALIN; GENE PRODUCT; NEUROPEPTIDE Y; NITRIC OXIDE SYNTHASE; PROTEIN GENE PRODUCT 9 5; SOMATOSTATIN; SUBSTANCE P; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG; VASOACTIVE INTESTINAL POLYPEPTIDE; VESICULAR ACETYLCHOLINE TRANSPORTER;

ADULT; AGED; ARTICLE; BLOOD FLOW; BLOOD VESSEL INNERVATION; CONTROLLED STUDY; ENZYME LOCALIZATION; FEMALE; HUMAN; HUMAN TISSUE; HUMAN VERSUS ANIMAL COMPARISON; INTESTINE INNERVATION; MALE; MESENTERIC ARTERY; MESENTERIC VEIN; NERVE FIBER; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SENSORY NERVE CELL; SYMPATHETIC NERVE CELL; TISSUE DISTRIBUTION;

ADULT; AGED; AGED, 80 AND OVER; BLOOD VESSELS; COLON; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MIDDLE AGED; NEURONS;

EID: 53949115937     PISSN: 13501925     EISSN: 13652982     Source Type: Journal    
DOI: 10.1111/j.1365-2982.2008.01150.x     Document Type: Article

References (51)

1. Williams LR, Leggett RW. Reference values for resting blood flow to organs of man. Clin Phys Physiol Meas 1989 10 : 187 217.
2. Mulvany MJ, Aalkjaer C. Structure and function of small arteries. Physiol Rev 1990 70 : 921 61.
3. Kotecha N. Mechanisms underlying ACh induced modulation of neurogenic and applied ATP constrictions in the submucosal arterioles of the guinea-pig small intestine. Br J Pharmacol 1999 126 : 1625 33.
4. Keast JR. Visualization and immunohistochemical characterization of sympathetic and parasympathetic neurons in the male rat major pelvic ganglion. Neuroscience 1995 66 : 655 62.
5. Ekblad E, Edvinsson L, Wahlestedt C, Uddman R, Hakanson R, Sundler F. Neuropeptide Y co-exists and co-operates with noradrenaline in perivascular nerve fibers. Regul Pept 1984 8 : 225 35.
6. Smyth L, Bobalova J, Ward SM, Keef KD, Mutafova-Yambolieva VN. Cotransmission from sympathetic vasoconstrictor neurons: differences in guinea-pig mesenteric artery and vein. Auton Neurosci Basic Clin 2000 86 : 18 29.
7. Kreulen DL. Activation of mesenteric arteries and veins by preganglionic and postganglionic nerves. Am J Physiol 1986 251 : H1267 75.
8. Evans RJ, Surprenant A. Vasoconstriction of guinea-pig submucosal arterioles following sympathetic nerve stimulation is mediated by the release of ATP. Br J Pharmacol 1992 106 : 242 9.
9. Ralevic V. Mechanism of prolonged vasorelaxation to ATP in the rat isolated mesenteric arterial bed. Br J Pharmacol 2001 132 : 685 92.
10. Gibbins IL, Furness JB, Costa M, MacIntyre I, Hillyard CJ, Girgis S. Co-localization of calcitonin gene-related peptide-like immunoreactivity with substance P in cutaneous, vascular and visceral sensory neurons of guinea pigs. Neurosci Lett 1985 57 : 125 30.
11. Brain SD, Williams TJ, Tippins JR, Morris HR, MacIntyre I. Calcitonin gene-related peptide is a potent vasodilator. Nature 1985 313 : 54 6.
12. Galligan JJ, Jiang MM, Shen KZ, Surprenant A. Substance P mediates neurogenic vasodilatation in extrinsically denervated guinea-pig submucosal arterioles. J Physiol 1990 420 : 267 80.
13. Lembeck F, Holzer P. Substance P as neurogenic mediator of antidromic vasodilation and neurogenic plasma extravasation. Naunyn Schmiedebergs Arch Pharmacol 1979 310 : 175 83.
14. Vanner S. Myenteric neurons activate submucosal vasodilator neurons in guinea pig ileum. Am J Physiol Gastrointest Liver Physiol 2000 279 : G380 7.
15. Vanner S, Surprenant A. Neural reflexes controlling intestinal microcirculation. Am J Physiol 1996 271 : G223 30.
16. Costa M, Furness JB, Yanaihara N, Yanaihara C, Moody TW. Distribution and projections of neurons with immunoreactivity for both gastrin-releasing peptide and bombesin in the guinea-pig small intestine. Cell Tissue Res 1984 235 : 285 93.
17. Li ZS, Fox-Threlkeld JE, Furness JB. Innervation of intestinal arteries by axons with immunoreactivity for the vesicular acetylcholine transporter (VAChT). J Anat 1998 192 : 107 17.
18. Li Q, Johansson H, Grimelius L. Innervation of human adrenal gland and adrenal cortical lesions. Virchows Arch 1999 435 : 580 9.
19. Tassicker BC, Hennig GW, Costa M, Brookes SJ. Rapid anterograde and retrograde tracing from mesenteric nerve trunks to the guinea-pig small intestine in vitro. Cell Tissue Res 1999 295 : 437 52.
20. Morris JL, Gibbins IL, Kadowitz PJ et al. Roles of peptides and other substances in cotransmission from vascular autonomic and sensory neurons. Can J Physiol Pharmacol 1995 73 : 521 32.
21. Gerke DC, Frewin DB, Soltys JS. Adrenergic innervation of human mesenteric blood vessels. Aust J Exp Biol Med Sci 1975 53 : 241 3.
22. Lundberg JM, Terenius L, Hokfelt T, Goldstein M. High levels of neuropeptide Y in peripheral noradrenergic neurons in various mammals including man. Neurosci Lett 1983 42 : 167 72.
23. Akiyoshi H, Gonda T, Terada T. A comparative histochemical and immunohistochemical study of aminergic, cholinergic and peptidergic innervation in rat, hamster, guinea pig, dog and human livers. Liver 1998 18 : 352 9.
24. Donoso MV, Brown N, Carrasco C, Cortes V, Fournier A, Huidobro-Toro JP. Stimulation of the sympathetic perimesenteric arterial nerves releases neuropeptide Y potentiating the vasomotor activity of noradrenaline: involvement of neuropeptide Y-Y1 receptors. J Neurochem 1997 69 : 1048 59.
25. Macrae IM, Furness JB, Costa M. Distribution of subgroups of noradrenaline neurons in the coeliac ganglion of the guinea-pig. Cell Tissue Res 1986 244 : 173 80.
26. Browning KN, Zheng Z, Kreulen DL, Travagli RA. Two populations of sympathetic neurons project selectively to mesenteric artery or vein. Am J Physiol 1999 276 : H1263 72.
27. De Backer D, Creteur J, Preiser JC, Dubois MJ, Vincent JL. Microvascular blood flow is altered in patients with sepsis [see comment]. Am J Respir Crit Care Med 2002 166 : 98 104.
28. Van der Graaf PH, Shankley NP, Black JW. Analysis of the effects of alpha 1-adrenoceptor antagonists on noradrenaline-mediated contraction of rat small mesenteric artery. Br J Pharmacol 1996 118 : 1308 16.
29. Han S, Yang CL, Chen X, Naes L, Cox BF, Westfall T. Direct evidence for the role of neuropeptide Y in sympathetic nerve stimulation-induced vasoconstriction. Am J Physiol 1998 274 : H290 4.
30. Gitterman DP, Evans RJ. Properties of P2X and P2Y receptors are dependent on artery diameter in the rat mesenteric bed. Br J Pharmacol 2000 131 : 1561 8.
31. Holzer P. Local effector functions of capsaicin-sensitive sensory nerve endings: involvement of tachykinins, calcitonin gene-related peptide and other neuropeptides. Neuroscience 1988 24 : 739 68.
32. Holzer P, Lippe IT, Jocic M, Wachter C, Erb R, Heinemann A. Nitric oxide-dependent and -independent hyperaemia due to calcitonin gene-related peptide in the rat stomach. Br J Pharmacol 1993 110 : 404 10.
33. Mayer EA, Raybould H, Koelbel C. Neuropeptides, inflammation, and motility. Dig Dis Sci 1988 33 (3 Suppl. 71S 7S.
34. Reinshagen M, Flamig G, Ernst S et al. Calcitonin gene-related peptide mediates the protective effect of sensory nerves in a model of colonic injury. J Pharmacol Exp Ther 1998 286 : 657 61.
35. Tornebrandt K, Nobin A, Owman C. Contractile and dilatory action of neuropeptides on isolated human mesenteric blood vessels. Peptides 1987 8 : 251 6.
36. Holzer P. Local microcirculatory reflexes and afferent signalling in response to gastric acid challenge. Gut 2000 47 (Suppl. 4 iv46 8 Discussion iv52.
37. Hobara N, Nakamura A, Ohtsuka A et al. Distribution of adrenomedullin-containing perivascular nerves in the rat mesenteric artery. Peptides 2004 25 : 589 99.
38. Birch D, Knight GE, Boulos PB, Burnstock G. Analysis of innervation of human mesenteric vessels in non-inflamed and inflamed bowel - a confocal and functional study. Neurogastroenterol Motil 2008 20 : 660 70.
39. Vanner S, Bolton M. Neural circuitry of capsaicin-sensitive afferents innervating submucosal arterioles in guinea pig ileum. Am J Physiol 1996 270 : G948 55.
40. Hulten L, Jodal M, Lundgren O. The effects of graded electrical stimulation or reflex activation of the sympathetic and the parasympathetic nerve supply on the regional blood flow in cat colon. Bibl Anat 1969 10 : 312 5.
41. Chiocchetti R, Poole DP, Kimura H et al. Evidence that two forms of choline acetyltransferase are differentially expressed in subclasses of enteric neurons. Cell Tissue Res 2003 311 : 11 22.
42. Milner P, Ralevic V, Hopwood AM et al. Ultrastructural localisation of substance P and choline acetyltransferase in endothelial cells of rat coronary artery and release of substance P and acetylcholine during hypoxia. Experientia 1989 45 : 121 5.
43. Steele PA, Brookes SJ, Costa M. Immunohistochemical identification of cholinergic neurons in the myenteric plexus of guinea-pig small intestine. Neuroscience 1991 45 : 227 39.
44. Vanner S, Surprenant A. Cholinergic and noncholinergic submucosal neurons dilate arterioles in guinea pig colon. Am J Physiol 1991 261 : G136 44.
45. Christensen J, Rick GA. Distribution of myelinated nerves in ascending nerves and myenteric plexus of cat colon. Am J Anat 1987 178 : 250 8.
46. Andersson PO. Vascular control in the colon and rectum. Scand J Gastroenterol Suppl 1984 93 : 65 78.
47. Song ZM, Brookes SJ, Neild TO, Costa M. Immunohistochemical and electrophysiological characterization of submucous neurons from the guinea-pig small intestine in organ culture. J Auton Nerv Syst 1997 63 : 161 71.
48. Hatoum OA, Binion DG. The vasculature and inflammatory bowel disease: contribution to pathogenesis and clinical pathology. Inflamm Bowel Dis 2005 11 : 304 13.
49. Porter AJ, Wattchow DA, Hunter A, Costa M. Abnormalities of nerve fibers in the circular muscle of patients with slow transit constipation. Int J Colorectal Dis 1998 13 : 208 16.
50. Wattchow DA, Furness JB, Costa M. Distribution and coexistence of peptides in nerve fibers of the external muscle of the human gastrointestinal tract. Gastroenterology 1988 95 : 32 41.
51. Gibbins IL, Wattchow D, Coventry B. Two immunohistochemically identified populations of calcitonin gene-related peptide (CGRP)-immunoreactive axons in human skin. Brain Res 1987 414 : 143 8.