Effects of 1-week sacral nerve stimulation on the rectal intestinal epithelial barrier and neuromuscular transmission in a porcine model

Neurogastroenterology and Motility

Volumn 27, Issue 1, 2015, Pages 40-50

  Provost, M ^a   Bregeon J ^a   Aubert, P ^a   Duchalais Dassonneville, E ^a   D'Aldebert, E ^b   Vergnolle, N ^b   Neunlist, M ^a   Meurette, G ^a  

^a HÔTEL DIEU   (France)

^b CHU PURPAN   (France)

Author keywords

Intestinal epithelial barrier; Paracellular permeability; Porcine model; Sacral nerve stimulation

Indexed keywords

CYTOKINES; RNA, MESSENGER;

ANIMALS; ELECTRIC STIMULATION; EPITHELIUM; INNERVATION; INTESTINAL MUCOSA; MALE; METABOLISM; MODELS, ANIMAL; PERMEABILITY; PHYSIOLOGY; RECTUM; SACRUM; SWINE; SYNAPTIC TRANSMISSION; TIGHT JUNCTIONS; TIME FACTORS;

ANIMALS; CYTOKINES; ELECTRIC STIMULATION; EPITHELIUM; INTESTINAL MUCOSA; MALE; MODELS, ANIMAL; PERMEABILITY; RECTUM; RNA, MESSENGER; SACRUM; SWINE; SYNAPTIC TRANSMISSION; TIGHT JUNCTIONS; TIME FACTORS;

EID: 84920073099     PISSN: 13501925     EISSN: 13652982     Source Type: Journal    
DOI: 10.1111/nmo.12465     Document Type: Article

References (43)

1. Thin NN, Horrocks EJ, Hotouras A, Palit S, Thaha MA, Chan CLH, Matzel KE, Knowles CH. Systematic review of the clinical effectiveness of neuromodulation in the treatment of faecal incontinence. Br J Surg 2013; 100: 1430-47.
2. Thomas GP, Dudding TC, Rahbour G, Nicholls RJ, Vaizey CJ. Sacral nerve stimulation for constipation. Br J Surg 2013; 100: 174-81.
3. Falletto E, Masin A, Lolli P, Villani R, Ganio E, Ripetti V, Infantino A, Stazi A. Is sacral nerve stimulation an effective treatment for chronic idiopathic anal pain? Dis Colon Rectum 2009; 52: 456-62.
4. Lundby L, Krogh K, Buntzen S, Laurberg S. Temporary sacral nerve stimulation for treatment of irritable bowel syndrome: a pilot study. Dis Colon Rectum 2008; 51: 1074-8.
5. Vitton V, Gigout J, Grimaud J-C, Bouvier M, Desjeux A, Orsoni P. Sacral nerve stimulation can improve continence in patients with Crohn's disease with internal and external anal sphincter disruption. Dis Colon Rectum 2008; 51: 924-7.
6. Liu Z, Shi C, Yang J, Zhang P, Ma Y, Wang F, Qin H. Molecular regulation of the intestinal epithelial barrier: implication in human diseases. Front Biosci J Virtual Libr 2011; 16: 2903-9.
7. Keita AV, Söderholm JD. The intestinal barrier and its regulation by neuroimmune factors. Neurogastroenterol Motil 2010; 22: 718-33.
8. Shen L, Su L, Turner JR. Mechanisms and functional implications of intestinal barrier defects. Dig Dis Basel Switz 2009; 27: 443-9.
9. Turner JR. Intestinal mucosal barrier function in health and disease. Nat Rev Immunol 2009; 9: 799-809.
10. Flamant M, Aubert P, Rolli-Derkinderen M, Bourreille A, Neunlist MR, Mahé MM, Meurette G, Marteyn B et al. Enteric glia protect against Shigella flexneri invasion in intestinal epithelial cells: a role for S-nitrosoglutathione. Gut 2011; 60: 473-84.
11. Costantini TW, Bansal V, Krzyzaniak M, Putnam JG, Peterson CY, Loomis WH, Wolf P, Baird A et al. Vagal nerve stimulation protects against burn-induced intestinal injury through activation of enteric glia cells. Am J Physiol Gastrointest Liver Physiol 2010; 299: G1308-18.
12. Neunlist M, Van Landeghem L, Mahé MM, Derkinderen P, Bruley des Varannes SB, Rolli-Derkinderen M. The digestive neuronal-glial-epithelial unit: a new actor in gut health and disease. Nat Rev Gastroenterol Hepatol 2012; 10: 90-100.
13. Meurette G, Blanchard C, Duchalais-Dassonneville E, Coquenlorge S, Aubert P, Wong M, Lehur PA, Neunlist M. Sacral nerve stimulation enhances epithelial barrier of the rectum: results from a porcine model. Neurogastroenterol Motil 2012; 24: 267-73, e110.
14. Cenac N, Chin AC, Garcia-Villar R, Salvador-Cartier C, Ferrier L, Vergnolle N, Buret AG, Fioramonti J et al. PAR2 activation alters colonic paracellular permeability in mice via IFN-gamma-dependent and -independent pathways. J Physiol 2004; 558(Pt 3): 913-25.
15. Moriez R, Salvador-Cartier C, Theodorou V, Fioramonti J, Eutamene H, Bueno L. Myosin light chain kinase is involved in lipopolysaccharide-induced disruption of colonic epithelial barrier and bacterial translocation in rats. Am J Pathol 2005; 167: 1071-9.
16. Wong MTC, Meurette G, Rodat F, Regenet N, Wyart V, Lehur P-A. Outcome and management of patients in whom sacral nerve stimulation for fecal incontinence failed. Dis Colon Rectum 2011; 54: 425-32.
17. George AT, Kalmar K, Panarese A, Dudding TC, Nicholls RJ, Vaizey CJ. Long-term outcomes of sacral nerve stimulation for fecal incontinence. Dis Colon Rectum 2012; 55: 302-6.
18. Maeda Y, Laurberg S. Sacral nerve stimulation: time for critical appraisal. Ann Surg 2011; 254: 174-5; author reply 175-176.
19. Pidsudko Z, Kaleczyc J, Majewski M, Lakomy M, Scheuermann DW, Timmermans JP. Differences in the distribution and chemical coding between neurons in the inferior mesenteric ganglion supplying the colon and rectum in the pig. Cell Tissue Res 2001; 303: 147-58.
20. Zalecki M, Podlasz P, Pidsudko Z, Wojtkiewicz J, Kaleczyc J. Vagal projections to the pylorus in the domestic pig (Sus scrofa domestica). Auton Neurosci Basic Clin 2012; 171: 21-7.
21. Motta J-P, Magne L, Descamps D, Rolland C, Squarzoni-Dale C, Rousset P, Martin L, Cenac N et al. Modifying the protease, antiprotease pattern by elafin overexpression protects mice from colitis. Gastroenterology 2011; 140: 1272-82.
22. Motta J-P, Bermúdez-Humarán LG, Deraison C, Martin L, Rolland C, Rousset P, Boue J, Dietrich G et al. Food-grade bacteria expressing elafin protect against inflammation and restore colon homeostasis. Sci Transl Med 2012; 4: 158ra144.
23. Döring G. The role of neutrophil elastase in chronic inflammation. Am J Respir Crit Care Med 1994; 150(6 Pt 2): S114-7.
24. Leroi AM, Damon H, Faucheron JL, Lehur PA, Siproudhis L, Slim K, Barbieux JP, Barth X et al. Sacral nerve stimulation in faecal incontinence: position statement based on a collective experience. Colorectal Dis 2009; 11: 572-83.
25. Dudding TC, Parés D, Vaizey CJ, Kamm MA. Predictive factors for successful sacral nerve stimulation in the treatment of faecal incontinence: a 10-year cohort analysis. Colorectal Dis 2008; 10: 249-56.
26. Marcelissen TAT, Leong RK, Serroyen J, van Kerrebroeck PEV, De Wachter SGG. The use of bilateral sacral nerve stimulation in patients with loss of unilateral treatment efficacy. J Urol 2011; 185: 976-80.
27. Kaufmann S, Naumann CM, Hamann MF, Seif C, Braun PM, Jünemann KP, van der Horst C. Unilateral vs bilateral sacral neuromodulation in pigs with formalin-induced detrusor hyperactivity. BJU Int 2009; 103: 260-3.
28. Coelho A-M, Vergnolle N, Guiard B, Fioramonti J, Bueno L. Proteinases and proteinase-activated receptor 2: a possible role to promote visceral hyperalgesia in rats. Gastroenterology 2002; 122: 1035-47.
29. Cenac N, Garcia-Villar R, Ferrier L, Larauche M, Vergnolle N, Bunnett NW, Coelho AM, Fioramonti J et al. Proteinase-activated receptor-2-induced colonic inflammation in mice: possible involvement of afferent neurons, nitric oxide, and paracellular permeability. J Immunol 2003; 170: 4296-300.
30. Neunlist M, Toumi F, Oreschkova T, Denis M, Leborgne J, Laboisse CL, Galmiche JP, Jarry A. Human ENS regulates the intestinal epithelial barrier permeability and a tight junction-associated protein ZO-1 via VIPergic pathways. Am J Physiol Gastrointest Liver Physiol 2003; 285: G1028-36.
31. Söderholm JD, Yang P-C, Ceponis P, Vohra A, Riddell R, Sherman PM, Perdue M. Chronic stress induces mast cell-dependent bacterial adherence and initiates mucosal inflammation in rat intestine. Gastroenterology 2002; 123: 1099-108.
32. Savidge TC, Newman P, Pothoulakis C, Ruhl A, Neunlist M, Bourreille A, Hurst R, Sofroniew M. Enteric glia regulate intestinal barrier function and inflammation via release of S-nitrosoglutathione. Gastroenterology 2007; 132: 1344-58.
33. Conlin VS, Wu X, Nguyen C, Dai C, Vallance BA, Buchan AMJ, Boyer L, Jacobson K. Vasoactive intestinal peptide ameliorates intestinal barrier disruption associated with Citrobacter rodentium-induced colitis. Am J Physiol Gastrointest Liver Physiol 2009; 297: G735-50.
34. Camilleri M, Lasch K, Zhou W. Irritable bowel syndrome: methods, mechanisms, and pathophysiology. The confluence of increased permeability, inflammation, and pain in irritable bowel syndrome. Am J Physiol Gastrointest Liver Physiol 2012; 303: G775-85.
35. Bertiaux-Vandaële N, Youmba SB, Belmonte L, Lecleire S, Antonietti M, Gourcerol G, Leroi AM, Déchelotte P et al. The expression and the cellular distribution of the tight junction proteins are altered in irritable bowel syndrome patients with differences according to the disease subtype. Am J Gastroenterol 2011; 106: 2165-73.
36. Coëffier M, Gloro R, Boukhettala N, Aziz M, Lecleire S, Vandaele N, Antonietti M, Savoye G et al. Increased proteasome-mediated degradation of occludin in irritable bowel syndrome. Am J Gastroenterol 2010; 105: 1181-8.
37. Poritz LS, Garver KI, Green C, Fitzpatrick L, Ruggiero F, Koltun WA. Loss of the tight junction protein ZO-1 in dextran sulfate sodium induced colitis. J Surg Res 2007; 140: 12-9.
38. Watson AJM, Hughes KR. TNF-α-induced intestinal epithelial cell shedding: implications for intestinal barrier function. Ann N Y Acad Sci 2012; 1258: 1-8.
39. Nystedt S, Larsson AK, Aberg H, Sundelin J. The mouse proteinase-activated receptor-2 cDNA and gene. Molecular cloning and functional expression. J Biol Chem 1995; 270: 5950-5.
40. Cenac N, Coelho A-M, Nguyen C, Compton S, Andrade-Gordon P, MacNaughton WK, Wallace J, Hollenberg M et al. Induction of intestinal inflammation in mouse by activation of proteinase-activated receptor-2. Am J Pathol 2002; 161: 1903-15.
41. Reed DE, Barajas-Lopez C, Cottrell G, Velazquez-Rocha S, Dery O, Grady EF, Bunnett N, Vanner S. Mast cell tryptase and proteinase-activated receptor 2 induce hyperexcitability of guinea-pig submucosal neurons. J Physiol 2003; 547(Pt 2): 531-42.
42. Matsufuji H, Yokoyama J. Neural control of the internal anal sphincter motility. J Smooth Muscle Res 2003; 39: 11-20.
43. Hirabayashi T, Matsufuji H, Yokoyama J, Hagane K, Hoshino K, Morikawa Y, Kitajima M. Colorectal motility induction by sacral nerve electrostimulation in a canine model: implications for colonic pacing. Dis Colon Rectum 2003; 46: 809-17.