Toll-like receptor 4 modulates small intestine neuromuscular function through nitrergic and purinergic pathways

Frontiers in Pharmacology

Volumn 8, Issue JUN, 2017, Pages

  Caputi, Valentina ^a   Marsilio, Ilaria ^a   Cerantola, Silvia ^a,b   Roozfarakh, Mona ^c   Lante, Isabella ^b   Galuppini, Francesca ^a   Rugge, Massimo ^a   Napoli, Eleonora ^d   Giulivi, Cecilia ^d,e   Orso, Genny ^f   Giron, Maria Cecilia ^a  

^a UNIVERSITY OF PADOVA   (Italy)

^b SAN CAMILLO HOSPITAL   (Italy)

^c MEDWAY SCHOOL OF PHARMACY   (United Kingdom)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f SCIENTIFIC INSTITUTE   (Italy)

Author keywords

Enteric nervous system; Gut microbiota; Innate immunity; Intestinal motility; Intestinal transit; Knockout mice; Small bowel; Toll like receptor 4

Indexed keywords

ADENOSINE TRIPHOSPHATE; INDUCIBLE NITRIC OXIDE SYNTHASE; NEURONAL NITRIC OXIDE SYNTHASE; PURINERGIC P2X7 RECEPTOR; PURINERGIC P2Y1 RECEPTOR; PURINERGIC RECEPTOR; TOLL LIKE RECEPTOR 4;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL MEMBRANE PERMEABILITY; CELL SURVIVAL; CELLULAR DISTRIBUTION; CHOLINERGIC ACTIVITY; CONTROLLED STUDY; GASTROINTESTINAL TRANSIT; GLIOSIS; IMMUNOHISTOCHEMISTRY; INTESTINE FUNCTION; INTESTINE INNERVATION; INTESTINE MOTILITY; MALE; MOLECULAR INTERACTION; MOUSE; NEUROMUSCULAR FUNCTION; NEUROTRANSMISSION; NITRERGIC NERVE CELL; NONHUMAN; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

EID: 85020787675     PISSN: None     EISSN: 16639812     Source Type: Journal    
DOI: 10.3389/fphar.2017.00350     Document Type: Article

References (56)

1. Anitha, M., Gondha, C., Sutliff, R., Parsadanian, A., Mwangi, S., Sitaraman, S. V., et al. (2006). GDNF rescues hyperglycemia-induced diabetic enteric neuropathy through activation of the PI3K/Akt pathway. J. Clin. Invest. 116, 344-356. doi: 10.1172/JCI26295
2. Anitha, M., Vijay-Kumar, M., Sitaraman, S. V., Gewirtz, A. T., and Srinivasan, S. (2012). Gut microbial products regulate murine gastrointestinal motility via Toll-like receptor 4 signaling. Gastroenterology 143, 1006.e4-1016.e4. doi: 10.1053/j.gastro.2012.06.034
3. Antonioli, L., Giron, M. C., Colucci, R., Pellegrini, C., Sacco, D., Caputi, V., et al. (2014). Involvement of the P2X7 purinergic receptor in colonic motor dysfunction associated with bowel inflammation in rats. PLoS ONE 9:e116253. doi: 10.1371/journal.pone.0116253
4. Aravalli, R. N., Peterson, P. K., and Lokensgard, J. R. (2007). Toll-like receptors in defense and damage of the central nervous system. J. Neuroimmune Pharmacol. 2, 297-312. doi: 10.1007/s11481-007-9071-5
5. Arqués, O., Chicote, I., Tenbaum, S., Puig, I., and Palmer, H. G. (2014). Quantitative procedure to analyze nuclear β-catenin using immunofluorescence tissue staining. Protoc. Exchange doi: 10.1038/protex.2012.008
6. Aubé, A.-C., Cabarrocas, J., Bauer, J., Philippe, D., Aubert, P., Doulay, F., et al. (2006). Changes in enteric neurone phenotype and intestinal functions in a transgenic mouse model of enteric glia disruption. Gut 55, 630-637. doi: 10.1136/gut.2005.067595
7. Barajon, I., Serrao, G., Arnaboldi, F., Opizzi, E., Ripamonti, G., Balsari, A., et al. (2009). Toll-like receptors 3, 4, and 7 are expressed in the enteric nervous system and dorsal root ganglia. J. Histochem. Cytochem. 57, 1013-1023. doi: 10.1369/jhc.2009.953539
8. Barbara, G., Feinle-Bisset, C., Ghoshal, U. C., Quigley, E. M., Santos, J., Vanner, S., et al. (2016). The intestinal microenvironment and functional gastrointestinal disorders. Gastroenterology 150, doi: 10.1053/j.gastro.2016.02.028 [Epub head of print]
9. Bashashati, M., Storr, M. A., Nikas, S. P., Wood, J. T., Godlewski, G., Liu, J., et al. (2012). Inhibiting fatty acid amide hydrolase normalizes endotoxin-induced enhanced gastrointestinal motility in mice. Br. J. Pharmacol. 165, 1556-1571. doi: 10.1111/j.1476-5381.2011.01644.x
10. Becattini, S., Taur, Y., and Pamer, E. G. (2016). Antibiotic-induced changes in the intestinal microbiota and disease. Trends Mol. Med. 22, 458-478. doi: 10.1016/j.molmed.2016.04.003
11. Bischoff, S. C., Barbara, G., Buurman, W., Ockhuizen, T., Schulzke, J.-D., Serino, M., et al. (2014). Intestinal permeability-a new target for disease prevention and therapy. BMC Gastroenterol. 14:189. doi: 10.1186/s12876-014-0189-7
12. Brown, I. A. M., McClain, J. L., Watson, R. E., Patel, B. A., and Gulbransen, B. D. (2015). Enteric glia mediate neuron death in colitis through purinergic pathways that require connexin-43 and nitric oxide. Cell. Mol. Gastroenterol. Hepatol. 57, 742-768. doi: 10.1002/dev.21214
13. Brun, P., Giron, M. C., Qesari, M., Porzionato, A., Caputi, V., Zoppellaro, C., et al. (2013). Toll-like receptor 2 regulates intestinal inflammation by controlling integrity of the enteric nervous system. Gastroenterology 145, 1323-1333. doi: 10.1053/j.gastro.2013.08.047
14. Brun, P., Gobbo, S., Caputi, V., Spagnol, L., Schirato, G., Pasqualin, M., et al. (2015). Toll like receptor-2 regulates production of glial-derived neurotrophic factors in murine intestinal smooth muscle cells. Mol. Cell. Neurosci. 68, 24-35. doi: 10.1016/j.mcn.2015.03.018
15. Burnstock, G. (2014). Purinergic signalling in the gastrointestinal tract and related organs in health and disease. Purinergic Signal. 10, 3-50. doi: 10.1007/s11302-013-9397-9
16. Cario, E. (2010). Toll-like receptors in inflammatory bowel diseases: a decade later. Inflamm. Bowel Dis. 16, 1583-1597. doi: 10.1002/ibd.21282
17. Coquenlorge, S., Duchalais, E., Chevalier, J., Cossais, F., Rolli-Derkinderen, M., and Neunlist, M. (2014). Modulation of lipopolysaccharide-induced neuronal response by activation of the enteric nervous system. J. Neuroinflammation 11:202. doi: 10.1186/s12974-014-0202-7
18. Corsetti, M., Akyuz, F., and Tack, J. (2015). Targeting tachykinin receptors for the treatment of functional gastrointestinal disorders with a focus on irritable bowel syndrome. Neurogastroenterol. Motil. 27, 1354-1370. doi: 10.1111/nmo.12616
19. Dall'Olmo, L., Fassan, M., Dassie, E., Scarpa, M., Realdon, S., Cavallin, F., et al. (2014). Role of proton pump inhibitor on esophageal carcinogenesis and pancreatic acinar cell metaplasia development: an experimental in vivo study. PLoS ONE 9:e112862. doi: 10.1371/journal.pone.0112862
20. De Mello, S. T., De Miranda Neto, M. H., Zanoni, J. N., and Furlan, M. M. D. P. (2009). Effects of insulin treatment on HuC/HuD, NADH diaphorase, and nNOS-positive myoenteric neurons of the duodenum of adult rats with acute diabetes. Dig. Dis. Sci. 54, 731-737. doi: 10.1007/s10620-008-0430-8
21. Devaraj, S., Tobias, P., and Jialal, I. (2011). Knockout of toll-like receptor-4 attenuates the pro-inflammatory state of diabetes. Cytokine 55, 441-445. doi: 10.1016/j.cyto.2011.03.023
22. Ekblad, E., and Bauer, A. J. (2004). Role of vasoactive intestinal peptide and inflammatory mediators in enteric neuronal plasticity. Neurogastroenterol. Motil. 16, 123-128. doi: 10.1111/j.1743-3150.2004.00487.x
23. Eskandari, M. K., Kalff, J. C., Billiar, T. R., Lee, K. K. W., and Bauer, A. J. (1999). LPS-induced muscularis macrophage nitric oxide suppresses rat jejunal circular muscle activity. Am. J. Physiol. Gastrointest. Liver Physiol. 277, G478-G486
24. Gallego, D., Malagelada, C., Accarino, A., De Giorgio, R., Malagelada, J. R., Azpiroz, F., et al. (2014). Nitrergic and purinergic mechanisms evoke inhibitory neuromuscular transmission in the human small intestine. Neurogastroenterol. Motil. 26, 419-429. doi: 10.1111/nmo.12293
25. Giaroni, C. (2002). P2 receptors in the murine gastrointestinal tract. Neuropharmacology 43, 1313-1323. doi: 10.1016/S0028-3908(02)00294-0
26. Giron, M. C., Bin, A., Brun, P., Etteri, S., Bolego, C., Florio, C., et al. (2008). Cyclic AMP in rat ileum: evidence for the presence of an extracellular cyclic AMP-adenosine pathway. Gastroenterology 134, 1116-1126. doi: 10.1053/j.gastro.2008.01.030
27. Gulbransen, B. D., and Sharkey, K. A. (2012). Novel functional roles for enteric glia in the gastrointestinal tract. Nat. Rev. Gastroenterol. Hepatol. 9, 625-632. doi: 10.1038/nrgastro.2012.138
28. Hritz, I., Mandrekar, P., Velayudham, A., Catalano, D., Dolganiuc, A., Kodys, K., et al. (2008). The critical role of toll-like receptor (TLR) 4 in alcoholic liver disease is independent of the common TLR adapter MyD88. Hepatology 48, 1224-1231. doi: 10.1002/hep.22470
29. Hu, H. Z., Gao, N., Lin, Z., Gao, C., Liu, S., Ren, J., et al. (2001). P2X(7) receptors in the enteric nervous system of guinea-pig small intestine. J. Comp. Neurol. 440, 299-310. doi: 10.1002/cne.1387
30. Kabouridis, P. S., and Pachnis, V. (2015). Emerging roles of gut microbiota and the immune system in the development of the enteric nervous system. J. Clin. Invest. 125, 956-964. doi: 10.1172/JCI76308
31. Kamada, N., Chen, G. Y., Inohara, N., and Núñez, G. (2013). Control of pathogens and pathobionts by the gut microbiota. Nat. Immunol. 14, 685-690. doi: 10.1038/ni.2608
32. Lecci, A. (2002). Pharmacology of transmission to gastrointestinal muscle. Curr. Opin. Pharmacol. 2, 630-641. doi: 10.1016/S1471-4892(02)00225-4
33. Lee, K. N., and Lee, O. Y. (2014). Intestinal microbiota in pathophysiology and management of irritable bowel syndrome. World J. Gastroenterol. 20, 8886-8897. doi: 10.3748/wjg.v20.i27.8886
34. Lomax, A. E., Sharkey, K. A., and Furness, J. B. (2010). The participation of the sympathetic innervation of the gastrointestinal tract in disease states. Neurogastroenterol. Motil. 22, 7-18. doi: 10.1111/j.1365-2982.2009.01381.x
35. Lu, H., Zhu, B., and Xue, X.-D. (2006). Role of neuronal nitric oxide synthase and inducible nitric oxide synthase in intestinal injury in neonatal rats. World J. Gastroenterol. 12, 4364-4368. doi: 10.3748/wjg.v12.i27.4364
36. Margolis, K. G., and Gershon, M. D. (2009). Neuropeptides and inflammatory bowel disease. Curr. Opin. Gastroenterol. 25, 503-511. doi: 10.1097/MOG.0b013e328331b69e
37. McGrath, J. C., and Lilley, E. (2015). Implementing guidelines on reporting research using animals (ARRIVE etc.): new requirements for publication in BJP. Br. J. Pharmacol. 172, 3189-3193. doi: 10.1111/bph.12955
38. McQuade, R. M., Carbone, S. E., Stojanovska, V., Rahman, A., Gwynne, R. M., Robinson, A. M., et al. (2016). Role of oxidative stress in oxaliplatin-induced enteric neuropathy and colonic dysmotility in mice. Br. J. Pharmacol. 173, 3502-3521. doi: 10.1111/bph.13646
39. Morrison, H. W., Filosa, J. A., Roger, V., Go, A., Lloyd-Jones, D., Benjamin, E., et al. (2013). A quantitative spatiotemporal analysis of microglia morphology during ischemic stroke and reperfusion. J. Neuroinflammation 10:4. doi: 10.1186/1742-2094-10-4
40. Neunlist, M., Rolli-Derkinderen, M., Latorre, R., Van Landeghem, L., Coron, E., Derkinderen, P., et al. (2014). Enteric glial cells: recent developments and future directions. Gastroenterology 147, 1230-1237. doi: 10.1053/j.gastro.2014.09.040
41. Ochoa-Cortes, F., Turco, F., Linan-Rico, A., Soghomonyan, S., Whitaker, E., Wehner, S., et al. (2016). Enteric glial cells. Inflamm. Bowel Dis. 22, 433-449. doi: 10.1097/MIB.0000000000000667
42. Okun, E., Griffioen, K. J., and Mattson, M. P. (2011). Toll-like receptor signaling in neural plasticity and disease. Trends Neurosci. 34, 269-281. doi: 10.1016/j.tins.2011.02.005
43. Orso, G., Martinuzzi, A., Rossetto, M. G., Sartori, E., Feany, M., and Daga, A. (2005). Disease-related phenotypes in a Drosophila model of hereditary spastic paraplegia are ameliorated by treatment with vinblastine. J. Clin. Invest. 115, 3026-3034. doi: 10.1172/JCI24694
44. Peterson, C. Y., Costantini, T. W., Loomis, W. H., Putnam, J. G., Wolf, P., Bansal, V., et al. (2010). Toll-like receptor-4 mediates intestinal barrier breakdown after thermal injury. Surg. Infect. (Larchmt). 11, 137-144. doi: 10.1089/sur.2009.053
45. Rakoff-Nahoum, S., Paglino, J., Eslami-Varzaneh, F., Edberg, S., and Medzhitov, R. (2004). Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118, 229-241. doi: 10.1016/j.cell.2004.07.002
46. Ratz, P. H., Berg, K. M., Urban, N. H., and Miner, A. S. (2005). Regulation of smooth muscle calcium sensitivity: KCl as a calcium-sensitizing stimulus. Am. J. Physiol. Cell Physiol. 288, C769-C783. doi: 10.1152/ajpcell.00529.2004
47. Riehl, T. E., Santhanam, S., Foster, L., Ciorba, M., and Stenson, W. F. (2015). CD44 and TLR4 mediate hyaluronic acid regulation of Lgr5+ stem cell proliferation, crypt fission, and intestinal growth in postnatal and adult mice. Am. J. Physiol. Gastrointest. Liver Physiol. 309, G874-G887. doi: 10.1152/ajpgi.00123.2015
48. Rühl, A. (2005). Glial cells in the gut. Neurogastroenterol. Motil. 17, 777-790. doi: 10.1111/j.1365-2982.2005.00687.x
49. Rumio, C., Besusso, D., Arnaboldi, F., Palazzo, M., Selleri, S., Gariboldi, S., et al. (2006). Activation of smooth muscle and myenteric plexus cells of jejunum via Toll-like receptor 4. J. Cell. Physiol. 208, 47-54. doi: 10.1002/jcp.20632
50. Schuster, A., Klotz, M., Schwab, T., Di Liddo, R., Bertalot, T., Schrenk, S., et al. (2014). Maintenance of the enteric stem cell niche by bacterial lipopolysaccharides? Evidence and perspectives. J. Cell. Mol. Med. 18, 1429-1443. doi: 10.1111/jcmm.12292
51. Sharkey, K. A., and Savidge, T. C. (2014). Role of enteric neurotransmission in host defense and protection of the gastrointestinal tract. Auton Neurosci. 181, 94-106. doi: 10.1016/j.autneu.2013.12.006
52. Voukali, E., Shotton, H. R., and Lincoln, J. (2011). Selective responses of myenteric neurons to oxidative stress and diabetic stimuli. Neurogastroenterol. Motil. 23, 964-e411. doi: 10.1111/j.1365-2982.2011.01778.x
53. Zhang, B., Ramesh, G., Uematsu, S., Akira, S., and Reeves, W. B. (2008). TLR4 signaling mediates inflammation and tissue injury in nephrotoxicity. J. Am. Soc. Nephrol. 19, 923-932. doi: 10.1681/ASN.2007090982
54. Zizzo, M. G., Mule, F., and Serio, R. (2003). Duodenal contractile activity in dystrophic (mdx) mice: reduction of nitric oxide influence. Neurogastroenterol. Motil. 15, 559-565. doi: 10.1046/j.1365-2982.2003.00438.x
55. Zizzo, M. G., Mulè, F., and Serio, R. (2004). Interplay between PACAP and NO in mouse ileum. Neuropharmacology 46, 449-455. doi: 10.1016/j.neuropharm.2003.09.011
56. Zoppellaro, C., Bin, A., Brun, P., Banzato, S., Macchi, V., Castagliuolo, I., et al. (2013). Adenosine-mediated enteric neuromuscular function is affected during herpes simplex virus type 1 infection of rat enteric nervous system. PLoS ONE 8:e72648. doi: 10.1371/journal.pone.0072648