Aging-associated oxidative stress leads to decrease in IAS tone via RhoA/ROCK downregulation

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 306, Issue 11, 2014, Pages

  Singh, Jagmohan ^a   Kumar, Sumit ^a   Krishna, Chadalavada Vijay ^a   Rattan, Satish ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

Aging; Internal anal sphincter; Oxidative stress; Rectoanal incontinence; RhoA ROCK

Indexed keywords

15 HYDROXY 11ALPHA,9ALPHA EPOXYMETHANOPROSTA 5,13 DIENOIC ACID; 4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; 6 ANILINO 5,8 QUINOLINEQUINONE; COMPLEMENTARY DNA; MESSENGER RNA; PROTEIN KINASE; REACTIVE OXYGEN METABOLITE; RHOA ASSOCIATED KINASE; SUPEROXIDE; UNCLASSIFIED DRUG;

ADULT; AGED; AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANUS SPHINCTER; ARTICLE; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; FECES INCONTINENCE; GENE SEQUENCE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; WESTERN BLOTTING;

AGING; INTERNAL ANAL SPHINCTER; OXIDATIVE STRESS; RECTOANAL INCONTINENCE; RHOA/ROCK;

AGING; AMINOQUINOLINES; ANAL CANAL; ANIMALS; CELL CULTURE TECHNIQUES; GENE EXPRESSION REGULATION; MUSCLE TONUS; MYOCYTES, SMOOTH MUSCLE; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY; RHO-ASSOCIATED KINASES; RHOA GTP-BINDING PROTEIN;

EID: 84901719840     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00087.2014     Document Type: Article

References (52)

1. Barja G. Updating the mitochondrial free radical theory of aging: an integrated view, key aspects, and confounding concepts. Antioxid Redox Signal 19: 1420-1445, 2013.
2. Berrougui H, Martin-Cordero C, Khalil A, Hmamouchi M, Ettaib A, Mahuenda E, Herrera MD. Vasorelaxant effects of harmine and harmaline extracted from Peganum harmala L. seeds in isolated rat aorta. Pharmacol Res 54: 150-157, 2006.
3. Bharucha AE. Outcome measures for fecal incontinence: anorectal structure and function. Gastroenterology 126: S90-S98, 2004.
4. Bharucha AE, Rao SS. An update on anorectal disorders for gastroenterologists. Gastroenterology 146: 37-45, 2014.
5. Bi D, Nishimura J, Niiro N, Hirano K, Kanaide H. Contractile properties of the cultured vascular smooth muscle cells: the crucial role played by RhoA in the regulation of contractility. Circ Res 96: 890-897, 2005.
6. Bitar KN, Greenwood-Van Meerveld B, Saad R, Wiley JW. Aging and gastrointestinal neuromuscular function: insights from within and outside the gut. Neurogastroenterol Motil 23: 490-501, 2011.
7. 2+ sensitization in pulmonary vascular smooth muscle through superoxide-dependent stimulation of RhoA. Am J Physiol Lung Cell Mol Physiol 298: L232-L242, 2010.
8. Cheng JC, Cheng HP, Tsai IC, Jiang MJ. ROS-mediated downregulation of MYPT1 in smooth muscle cells: a potential mechanism for the aberrant contractility in atherosclerosis. Lab Invest 93: 422-433, 2013.
9. Choi K, Chen J, Mitra S, Sarna SK. Impaired integrity of DNA after recovery from inflammation causes persistent dysfunction of colonic smooth muscle. Gastroenterology 141: 1293-1301, 2011.
10. Culver PJ, Rattan S. Genesis of anal canal pressures in the opossum. Am J Physiol Gastrointest Liver Physiol 251: G765-G771, 1986.
11. De Godoy MA, Rattan N, Rattan S. Arachidonic acid metabolites follow the preferential course of cyclooxygenase pathway for the basal tone in the internal anal sphincter. Am J Physiol Gastrointest Liver Physiol 296: G727-G734, 2009.
12. Demel SL, Dong H, Swain GM, Wang X, Kreulin DL, Galligan JJ. Antioxidant treatment restores prejunctional regulation of purinergic transmission in mesenteric arteries of deoxycorticosterone acetate-salt hypertensive rats. Neuroscience 168: 335-345, 2010.
13. Firth M, Prather CM. Gastrointestinal motility problems in the elderly patient. Gastroenterology 122: 1688-1700, 2002.
14. Freeman BA, Crapo JD. Biology of disease: free radicals and tissue injury. Lab Invest 47: 412-426, 1982.
15. Fridovich I. Superoxide radical and superoxide dismutases. Annu Rev Biochem 64: 97-112, 1995.
16. Gemma C, Vila J, Bachstetter A, Bickford PC. Oxidative stress and the aging brain: from theory to prevention. In: Brain Aging, edited by Riddle DR. Boca Raton, FL: CRC, 2007.
17. Halliwell B, Gutteridge JM, Cross CE. Free radicals, antioxidants, and human disease: where are we now? J Lab Clin Med 119: 598-620, 1992.
18. Hernandez L, Grasa L, Fagundes DS, Gonzalo MP, Arruebo MP, Plaza MA, Murillo MD. Role of potassium channels in rabbit intestinal motility disorders induced by 2,2′-azobis (2-amidinopropane) dihydrochloride (AAPH). J Physiol Pharmacol 61: 279-286, 2010.
19. Hillemeier C, Bitar KN, Sohn U, Biancani P. Protein kinase C mediates spontaneous tone in the cat lower esophageal sphincter. J Pharmacol Exp Ther 277: 144-149, 1996.
20. Jiang F, Zhang Y, Dusting GJ. NADPH oxidase-mediated redox signaling: roles in cellular stress response, stress tolerance, and tissue repair. Pharmacol Rev 63: 218-242, 2011.
21. Jones OM, Moore JA, Brading AF, Mortensen NJ. Botulinum toxin injection inhibits myogenic tone and sympathetic nerve function in the porcine internal anal sphincter. Colorectal Dis 5: 552-557, 2003.
22. Khaikin M, Bashankaev B, Sands D, Weiss EG, Zbar A, Wexner SD. The effect of topical anal captopril on resting anal pressure in healthy volunteers: the first human pilot study. Tech Coloproctol 18: 139-143, 2013.
23. 2+ sensitization. Free Radic Biol Med 46: 633-642, 2009.
24. Koughnett JA, Wexner SD. Current management of fecal incontinence: choosing amongst treatment options to optimize outcomes. World J Gastroenterol 19: 9216-9230, 2013.
25. Kumagai Y, Midorikawa K, Nakai Y, Yoshikawa T, Kushida K, Homma-Takeda S, Shimojo N. Inhibition of nitric oxide formation and superoxide generation during reduction of LY83583 by neuronal nitric oxide synthase. Eur J Pharmacol 360: 213-218, 1998.
26. Lazarescue A, Turnbull GK, Vanner S. Investigating and treating fecal incontinence: when and how. Can J Gastroenterol 23: 301-308, 2009.
27. 2+ sensitization pathways in gallbladder smooth muscle. Age 34: 881-893, 2012.
28. Patel CA, 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.
29. Patel CA, 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.
30. Peluso I, Campolongo P, Valeri P, Romanelli L, Palmery M. Intestinal motility disorder induced by free radicals: a new model mimicking oxidative stress in gut. Pharmacol Res 46: 533-538, 2002.
31. Rao SS. Pathophysiology of adult fecal incontinence. Gastroenterology 126: S14-S22, 2004.
32. Rattan S, Benjamin P, Maxwell IV. RhoA/ROCK-kinase: pathophysiologic and therapeutic implications in gastrointestinal smooth muscle tone and relaxation. Gastroenterology 138: 13-18, 2010.
33. Rattan S, De Godoy MA, Patel CA. Rho kinase as a novel molecular therapeutic target for hypertensive internal anal sphincter. Gastroenterology 131: 108-116, 2006.
34. Rattan S, Singh J. Basal internal anal sphincter tone, inhibitory neurotransmission, and other factors contributing to the maintenance of high pressures in the anal canal. Neurogastroenterol Motil 23: 3-7, 2011.
35. 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.
36. Roberts JA, Durnin L, Sharkey KA, Mutafova-Yambolieva VN, Mawe GM. Oxidative stress disrupts purinergic neuromuscular transmission in the inflamed colon. J Physiol 591: 3725-3737, 2013.
37. Shi XZ, Lindholm PF, Sarna SK. NF-αB activation by oxidative stress and inflammation suppresses contractility in colonic circular smooth muscle cells. Gastroenterology 124: 1369-1380, 2003.
38. Singh J, Maxwell IV, Rattan S. Immunocytochemical evidence for PDBu-induced activation of RhoA/ROCK in human internal anal sphincter smooth muscle cells. Am J Physiol Gastrointest Liver Physiol 301: G317-G325, 2011.
39. Snetkov VA, Smirnov SV, Kua J, Aaronson PI, Ward JP, Knock GA. Superoxide differentially controls pulmonary and systemic vascular tone through multiple signalling pathways. Cardiovasc Res 89: 214-224, 2011.
40. Somara S, Bashllari D, Gilmont RR, Bitar KN. Real-time dynamic movement of caveolin-1 during smooth muscle contraction of human colon and aged rat colon transfected with caveolin-1 cDNA. Am J Physiol Gastrointest Liver Physiol 300: G1022-G1032, 2011.
41. Somara S, Gilmont RR, Martens JR, Bitar KN. Ectopic expression of caveolin-1 restores physiological contractile response of aged colonic smooth muscle. Am J Physiol Gastrointest Liver Physiol 293: G240-G249, 2007.
42. Speakman CT, Hoyle CH, Kamm MA, Swash M, Henry MM, Nicholls RJ, Chir M, Burnstock G. Abnormal internal anal sphincter fibrosis and elasticity in fecal incontinence. Dis Colon Rectum 38: 407-410, 1995.
43. Strittmatter F, Gratzke C, Weinhold P, Steib CJ, Hartmann AC, Schlenker B, Andersson KE, Hedlund P, Stief CG, Hennenberg M. Thromboxane A2 induces contraction of human prostate smooth muscle by Rho kinase-and calmodulin-dependent mechanisms. Eur J Pharmacol 650: 650-655, 2011.
44. Thannickal VJ, Fanburg BL. Reactive oxygen species in cell signaling. Am J Physiol Lung Cell Mol Physiol 279: L1005-L1028, 2000.
45. Van der Vliet A, Tunistra TJ, Bast A. Modulation of oxidative stress in the gastrointestinal tract and effect on rat intestinal motility. Biochem Pharmacol 38: 2807-2818, 1989.
46. Voukali E, Shotton HR, Lincoln J. Selective responses of myenteric neurons to oxidative stress in diabetic stimuli. Neurogastroenterol Motil 23: 964-e411, 2011.
47. Wade PR. Aging and neural control of GI tract. I. Age-related changes in enteric nervous system. Am J Physiol Gastrointest Liver Physiol 283: G489-G495, 2002.
48. Wald A. Faecal incontinence in the elderly: epidemiology and management. Drugs Aging 22: 131-139, 2005.
49. Wang C, Houghton MJ, Gamage PP, Collins HE, Patel BA, Yeoman MS, Ranson RN, Saffrey MJ. Changes in the innervation of the mouse internal anal sphincter during aging. Neurogastroenterol Motil 25: e469-e477, 2013.
50. Whitehead WE, Borrud L, Goode PS, Meikle S, Mueller ER, Tuteja A, Weidner A, Weinstein M, Ye W. Fecal incontinence in US adults: epidemiology and risk factors. Gastroenterology 137: 512-517, 2009.
51. Wiley JW. Aging and neural control of the GI tract. III. Senescent enteric nervous system: lessons from extraintestinal sites and nonmammalian species. Am J Physiol Gastrointest Liver Physiol 283: G1020-G1026, 2002.
52. Winston JH, Li Q, Sarna SK. Paradoxical regulation of ChAT and nNOS expression in animal models of Crohn's colitis and ulcerative colitis. Am J Physiol Gastrointest Liver Physiol 305: G295-G302, 2013.