The molecular basis of the genesis of basal tone in internal anal sphincter

Nature Communications

Volumn 7, Issue , 2016, Pages

  Zhang, Cheng Hai ^a,b   Wang, Pei ^a   Liu, Dong Hai ^b   Chen, Cai Ping ^a   Zhao, Wei ^a   Chen, Xin ^a   Chen, Chen ^a   He, Wei Qi ^a,c   Qiao, Yan Ning ^a   Tao, Tao ^a   Sun, Jie ^a   Peng, Ya Jing ^a   Lu, Ping ^b   Zheng, Kaizhi ^b   Craige, Siobhan M ^b   Lifshitz, Lawrence M ^b   Keaney, John F ^b   Fogarty, Kevin E ^b   Ge, Ronghua Zhu ^b   Zhu, Min Sheng ^a,d  

^a NANJING UNIVERSITY   (China)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^c SOOCHOW UNIVERSITY   (China)

^d Key Laboratory of Remodeling Related Cardiovascular Diseases   (China)

Author keywords

[No Author keywords available]

Indexed keywords

4 (2 BENZYLBENZOYL) 2,5 DIMETHYL 1H PYRROLE 3 CARBOXYLIC ACID METHYL ESTER; ANOCTAMIN 1; BETHANECHOL; CAFFEINE; CALCIUM; CALCIUM ACTIVATED CHLORIDE CHANNEL; CALCIUM CHANNEL L TYPE; MYOSIN LIGHT CHAIN KINASE; NIFEDIPINE; NIFLUMIC ACID; POTASSIUM CHLORIDE; RYANODINE; RYANODINE RECEPTOR; UNCLASSIFIED DRUG; CHLORIDE CHANNEL; TMEM16A PROTEIN, MOUSE;

ANATOMY; CALCIUM; CELLS AND CELL COMPONENTS; ENZYME ACTIVITY; MUSCLE; PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ANUS SPHINCTER; ARTICLE; BASAL TONE; CALCIUM SIGNALING; CALCIUM TRANSPORT; CONTROLLED STUDY; DEFECATION; FECES INCONTINENCE; FEMALE; GENE DELETION; GENE INACTIVATION; MALE; MOLECULAR BIOLOGY; MOUSE; NONHUMAN; SMOOTH MUSCLE CELL; SMOOTH MUSCLE CONTRACTILITY; SMOOTH MUSCLE CONTRACTION; SMOOTH MUSCLE TONE; ANAL CANAL; ANIMAL; C57BL MOUSE; DEFICIENCY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HUMAN; MEMBRANE POTENTIAL; METABOLISM; MUSCLE CONTRACTION; MUSCLE HYPOTONIA; PATCH CLAMP TECHNIQUE; PATHOPHYSIOLOGY; PHYSIOLOGY; SMOOTH MUSCLE; TRANSGENIC MOUSE;

ANAL CANAL; ANIMALS; BETHANECHOL; CAFFEINE; CALCIUM; CALCIUM CHANNELS, L-TYPE; CALCIUM SIGNALING; CHLORIDE CHANNELS; DEFECATION; FECAL INCONTINENCE; FEMALE; GENE EXPRESSION REGULATION; HUMANS; MALE; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUSCLE CONTRACTION; MUSCLE HYPOTONIA; MUSCLE, SMOOTH; MYOSIN-LIGHT-CHAIN KINASE; NIFEDIPINE; NIFLUMIC ACID; PATCH-CLAMP TECHNIQUES; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL;

EID: 84966320684     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms11358     Document Type: Article

References (57)

1. Vander, A., Sherman, J., & Luciano, D. Human Physiology: The Mechanisms of Body Function 6th edn, International Edition (McGraw-Hill international editions, 1994).
2. Rattan, S. The internal anal sphincter: regulation of smooth muscle tone and relaxation. Neurogastroenterol. Motil. 17, 50-59 (2005).
3. Murthy, K. S. Signaling for contraction and relaxation in smooth muscle of the gut. Annu. Rev. Physiol. 68, 345-374 (2006).
4. 2+ sensitivity of smooth muscle and nonmuscle myosin II: modulated by G proteins, kinases, and myosin phosphatase. Physiol. Rev. 83, 1325-1358 (2003).
5. Rattan, S., & Singh, J. RhoA/ROCK pathway is the major molecular determinant of basal tone in intact human internal anal sphincter. Am. J. Physiol. Gastrointest. Liver Physiol. 302, G664-G675 (2012).
6. Patel, C. A., & Rattan, S. Cellular regulation of basal tone in internal anal sphincter smooth muscle by RhoA/ROCK. Am. J. Physiol. Gastrointest. Liver Physiol. 292, G1747-G1756 (2007).
7. Patel, C. A., & Rattan, S. Spontaneously tonic smooth muscle has characteristically higher levels of RhoA/ROK compared with the phasic smooth muscle. Am. J. Physiol. Gastrointest. Liver Physiol. 291, G830-G837 (2006).
8. Mcdonnell, B., Hamilton, R., Fong, M., Ward, S. M., & Keef, K. D. Functional evidence for purinergic inhibitory neuromuscular transmission in the mouse internal anal sphincter. Am. J. Physiol. Gastrointest. Liver Physiol. 294, G1041-G1051 (2008).
9. Chakder, S., Mchugh, K. M., & Rattan, S. Inhibitory neurotransmission in lethal spotted mutant mice: a model for Hirschsprung?s disease. Gastroenterology 112, 1575-1585 (1997).
10. Hall, K. A., Ward, S. M., Cobine, C. A., & Keef, K. D. Spatial organization and coordination of slow waves in the mouse anorectum. J. Physiol. 592, 3813-3829 (2014).
11. Cobine, C. A., et al. Interstitial cells of Cajal in the cynomolgus monkey rectoanal region and their relationship to sympathetic and nitrergic nerves. Am. J. Physiol. Gastrointest. Liver Physiol. 298, G643-G656 (2010).
12. He, W. Q., et al. Altered contractile phenotypes of intestinal smooth muscle in mice deficient in myosin phosphatase target subunit 1. Gastroenterology 144, 1456-1465 (2013).
13. He, W. Q., et al. Myosin light chain kinase is central to smooth muscle contraction and required for gastrointestinal motility in mice. Gastroenterology 135, 610-620 (2008).
14. Zhang, W. C., et al. Myosin light chain kinase is necessary for tonic airway smooth muscle contraction. J. Biol. Chem. 285, 17-19 (2010).
15. Rao, S., Kempf, J., & Stessman, M. Anal seepage: sphincter dysfunction or incomplete evaluation?. Gastroenterology 114, A824 (1998).
16. Rao, S. S. Pathophysiology of adult fecal incontinence. Gastroenterology 126, S14-S22 (2004).
17. Cobine, C. A., Fong, M., Hamilton, R., & Keef, K. D. Species dependent differences in the actions of sympathetic nerves and noradrenaline in the internal anal sphincter. Neurogastroenterol. Motil. 19, 937-945 (2007).
18. 2+ channel activator, in cardiac and vascular preparations. Mol. Pharmacol. 40, 734-741 (1991).
19. McDonough, S. I., Mori, Y., & Bean, B. P. FPL 64176 modification of CaV1.2L-Type calcium channels: dissociation of effects on ionic current and gating current. Biophys. J. 88, 211-223 (2005).
20. 2+ sparks act as potent regulators of excitation-contraction coupling in airway smooth muscle. J. Biol. Chem. 285, 2203-2210 (2010).
21. Bulley, S., & Jaggar, J. H. Cl channels in smooth muscle cells. Pflug. Arch. 466, 861-872 (2013).
22. Saha, J. K., Sengupta, J. N., & Goyal, R. K. Role of chloride ions in lower esophageal sphincter tone and relaxation. Am. J. Physiol. Gastrointest. Liver Physiol. 263, G115-G126 (1992).
23. Namkung, W., Phuan, P. W., & Verkman, A. S. TMEM16A inhibitors reveal TMEM16A as a minor component of calcium-Activated chloride channel conductance in airway and intestinal epithelial cells. J. Biol. Chem. 286, 2365-2374 (2011).
24. 2+-Activated Cl-channels in Xenopus oocytes. Mol. Pharmacol. 37, 720-724 (1990).
25. Namkung, W., Yao, Z., Finkbeiner, W. E., & Verkman, A. S. Small-molecule activators of TMEM16A, a calcium-Activated chloride channel, stimulate epithelial chloride secretion and intestinal contraction. FASEB J. 25, 4048-4062 (2011).
26. Nelson, M. T., et al. Relaxation of arterial smooth muscle by calcium sparks. Science 270, 633-637 (1995).
27. + channels, and coupling ratio between them. Am. J. Physiol. Cell Physiol. 287, C1577-C1588 (2004).
28. 2+ sparks and spontaneous transient outward currents in single smooth muscle cells. J. Gen. Physiol. 113, 215-228 (1999).
29. 2+ sparks activate K? and Cl-channels, resulting in spontaneous transient currents in guinea-pig tracheal myocytes. J. Physiol. 513, 711-718 (1998).
30. Huang, F., et al. Studies on expression and function of the TMEM16A calcium-Activated chloride channel. Proc. Natl Acad. Sci. USA 106, 21413-21418 (2009).
31. Yang, Y. D., et al. TMEM16A confers receptor-Activated calcium-dependent chloride conductance. Nature 455, 1210-1215 (2008).
32. Schroeder, B. C., Cheng, T., Jan, Y. N., & Jan, L. Y. Expression cloning of TMEM16A as a calcium-Activated chloride channel subunit. Cell 134, 1019-1029 (2008).
33. Caputo, A., et al. TMEM16A, a membrane protein associated with calcium-dependent chloride channel activity. Science 322, 590-594 (2008).
34. Manoury, B., Tamuleviciute, A., & Tammaro, P. TMEM16A/anoctamin 1 protein mediates calcium-Activated chloride currents in pulmonary arterial smooth muscle cells. J. Physiol. 588, 2305-2314 (2010).
35. Stohr, H., et al. TMEM16B, a novel protein with calcium-dependent chloride channel activity, associates with a presynaptic protein complex in photoreceptor terminals. J. Neurosci. 29, 6809-6818 (2009).
36. Rock, J. R., Futtner, C. R., & Harfe, B. D. The transmembrane protein TMEM16A is required for normal development of the murine trachea. Dev. Biol. 321, 141-149 (2008).
37. 2+-Activated Clchannel in airway smooth muscle contributes to airway hyperresponsiveness. Am. J. Respir. Crit. Care Med. 187, 374-381 (2013).
38. 2+-Activated chloride currents lowers blood pressure. J. Clin. Invest. 124, 675-686 (2014).
39. 2+-Activated Cl currents and contractility of smooth muscle in rat mesenteric small arteries. Pflug. Arch. 466, 1391-1409 (2014).
40. Bulley, S., et al. TMEM16A/ANO1 channels contribute to the myogenic response in cerebral arteries. Circ. Res. 111, 1027-1036 (2012).
41. 2+-Activated chloride channel stoichiometrically interacts with an ezrin-radixin-moesin network. Proc. Natl Acad. Sci. USA 109, 10376-10381 (2012).
42. 2+-Activated Cl-currents by phosphorylation in pulmonary arterial smooth muscle cells. J. Gen. Physiol. 128, 73-87 (2006).
43. 2+-dependent Cl-channels in undifferentiated human colonic cells (HT-29). II. Regulation and rundown. Am. J. Physiol. Cell Physiol. 264, C977-C985 (1993).
44. 2+ sparks in mouse airway smooth muscle. J. Gen. Physiol. 132, 145-160 (2008).
45. Morita, H., et al. Membrane stretch-induced activation of a TRPM4-like nonselective cation channel in cerebral artery myocytes. J. Pharmacol. Sci. 103, 417-426 (2007).
46. Collier, M., Ji, G., Wang, Y. X., & Kotlikoff, M. Calcium-induced calcium release in smooth muscle loose coupling between the action potential and calcium release. J. Gen. Physiol. 115, 653-662 (2000).
47. 2+ sparks in murine arterial smooth muscle cells. J. Physiol. 584, 205-219 (2007).
48. Carl, A., Lee, H. K., & Sanders, K. M. Regulation of ion channels in smooth muscles by calcium. Am. J. Physiol. Cell Physiol. 271, C9-C34 (1996).
49. 2+-Activated Cl-channels in rabbit pulmonary artery smooth muscle cells. J. Physiol. 547, 181-196 (2003).
50. Sanders, K. M., Ward, S. M., & Koh, S. D. Interstitial cells: regulators of smooth muscle function. Physiol. Rev. 94, 859-907 (2014).
51. Duffy, A. M., Cobine, C. A., & Keef, K. D. Changes in neuromuscular transmission in the W/WV mouse internal anal sphincter. Neurogastroenterol. Motil. 24, e41-e55 (2012).
52. de Lorijn, F., et al. Interstitial cells of Cajal are involved in the afferent limb of the rectoanal inhibitory reflex. Gut 54, 1107-1113 (2005).
53. 2+ activated Cl-conductance via the interaction with actin cytoskeleton in murine portal vein. J. Pharmacol. Sci. 125, 107-111 (2014).
54. Wang, Y. F., & Daniel, E. E. Gap junctions in gastrointestinal muscle contain multiple connexins. Am. J. Physiol. Gastrointest. Liver Physiol. 281, G533-G543 (2001).
55. Samuel, U., Lutjen-Drecoll, E., & Tamm, E. R. Gap junctions are found between iris sphincter smooth muscle cells but not in the ciliary muscle of human and monkey eyes. Exp. Eye Res. 63, 187-192 (1996).
56. Liu, P., Jenkins, N. A., & Copeland, N. G. A highly efficient recombineeringbased method for generating conditional knockout mutations. Genome Res. 13, 476-484 (2003).
57. 2+ current. J. Gen. Physiol. 116, 845-864 (2000).