Gastroenterology
Volume 137, Issue 1 , Pages 53-61 , July 2009

Bioengineered Internal Anal Sphincter Derived From Isolated Human Internal Anal Sphincter Smooth Muscle Cells

  • Sita Somara

      Affiliations

    • Department of Pediatrics-Gastroenterology University of Michigan, Ann Arbor, Michigan
  • ,
  • Robert R. Gilmont

      Affiliations

    • Department of Pediatrics-Gastroenterology University of Michigan, Ann Arbor, Michigan
  • ,
  • Robert G. Dennis

      Affiliations

    • Department of Biomedical Engineering, University of North Carolina, Chapel Hill, North Carolina
  • ,
  • Khalil N. Bitar

      Affiliations

    • Department of Pediatrics-Gastroenterology University of Michigan, Ann Arbor, Michigan
    • Corresponding Author InformationReprint requests Address requests for reprints to: Khalil N. Bitar, PhD, AGAF, University of Michigan Medical School, 1150 W. Medical Center Dr., MSRB I, Room A520, Ann Arbor, Michigan 48109-0658. fax: (734) 647-9703

Received 20 August 2008 ,Accepted 17 March 2009.

References 

  1. Drossman DA, Li Z, Andruzzi E, et al. US householder survey of functional gastrointestinal disorders (Prevalence, sociodemography, and health impact). Dig Dis Sci. 1993;38:1569–1580
  2. Perry S, Shaw C, McGrother C, et al. Leicestershire MRC Incontinence Study Team Prevalence of faecal incontinence in adults aged 40 years or more living in the community. Gut. 2002;50:480–484
  3. Rao SSC, Kempf J, Stessman M. Anal seepage:sphincter dysfunction or incomplete evacuation (abstr)?. Gastroenterology. 1998;114:A824
  4. Bharucha AE. Fecal incontinence. Gastroenterology. 2003;124:1672–1685
  5. Frenckner B. Function of the anal sphincters in spinal man. Gut. 1975;16:638–644
  6. Sahai E, Olson MF, Marshall CJ. Cross-talk between Ras and Rho signalling pathways in transformation favours proliferation and increased motility. EMBO J. 2001;20:755–766
  7. Sun WM, Read NW, Donnelly TC. Impaired internal anal sphincter in a subgroup of patients with idiopathic fecal incontinence. Gastroenterology. 1989;97:130–135
  8. Delechenaut P, Leroi AM, Weber J, et al. Relationship between clinical symptoms of anal incontinence and the results of anorectal manometry. Dis Colon Rectum. 1992;35:847–849
  9. Sultan AH, Kamm MA, Hudson CN, et al. Third degree obstetric anal sphincter tears: risk factors and outcome of primary repair. Br Med J. 1994;308:887–891
  10. Laurberg S, Swash M. Effects of aging on the anorectal sphincters and their innervation. Dis Colon Rectum. 1989;32:737–742
  11. Jones OM, Brading AF, Mortensen NJ. The physiology, pharmacology and therapeutic manipulation of the internal anal sphincter. Can J Physiol Pharmacol. 2002;16:249–257
  12. Szymanski PT, Szymanska G, Goyal RK. Differences in calmodulin and calmodulin-binding proteins in phasic and tonic smooth muscles. Am J Physiol Cell Physiol. 2002;282:C94–C104
  13. Rattan S, Regan RF, Patel CA, et al. Nitric oxide not carbon monoxide mediates nonadrenergic noncholinergic relaxation in the murine internal anal sphincter. Gastroenterology. 2005;129:1954–1966
  14. Bitar KN, Hillemeier C, Biancani P, et al. Regulation of smooth muscle contraction in rabbit internal anal sphincter by protein kinase C and Ins(1,4,5)P3. Am J Physiol. 1991;260:G537–G542
  15. Chakder S, Rattan S. Involvement of cAMP and cGMP in relaxation of internal anal sphincter by neural stimulation, VIP, and NO. Am J Physiol. 1993;264:G702–G707
  16. Patil SB, Bitar KN. RhoA- and PKC-α-mediated phosphorylation of MYPT and its association with HSP27 in colonic smooth muscle cells. Am J Physiol Gastrointest Liver Physiol. 2006;290:G83–G95
  17. Li F, De Godoy M, Rattan S. Role of adenylate and guanylate cyclases in β1-, β2-, and β3-adrenoceptor-mediated relaxation of internal anal sphincter smooth muscle. J Pharmacol Exp Ther. 2004;308:1111–1120
  18. Dennis RG, Kosnik PE. Excitability and isometric contractile properties of mammalian skeletal muscle constructs engineered in vitro. In Vitro Cell Dev Biol Anim. 2000;36:327–335
  19. Dennis RG, Kosnik PE. Mesenchymal cell culture: instrumentation and methods for evaluating engineered muscle. In:  Atala A,  Lanza R editor. Methods in tissue engineering. 9:San Diego: Harcourt, Academic Press; 2002;
  20. Hecker L, Baar K, Dennis RG, et al. Development of a three-dimensional physiological model of the internal anal sphincter bioengineered in vitro from isolated smooth muscle cells. Am J Physiol Gastrointest Liver Physiol. 2005;289:G188–G196
  21. Macpherson PC, Dennis RG, Faulkner JA. Sarcomere dynamics and contraction-induced injury to maximally activated single muscle fibres from soleus muscles of rats. J Physiol. 1997;500:523–533
  22. Biancani P, Walsh J, Behar J. Vasoactive intestinal peptide: a neurotransmitter for relaxation of the rabbit internal anal sphincter. Gastroenterology. 1985;89:867–874
  23. Glavind EB, Forman A, Madsen G, et al. Effects of transmural field stimulation in isolated smooth muscle of human rectum and internal anal sphincter. Am J Physiol Gastrointest Liver Physiol. 1997;272:G1075–G1082
  24. Martens JR, Navarro-Polanco R, Coppock EA, et al. Differential targeting of Shaker-like potassium channels to lipid rafts. J Biol Chem. 2000;275:7443–7446
  25. Rattan S, De Godoy MA, Patel CA. Rho kinase as a novel molecular therapeutic target for hypertensive internal anal sphincter. Gastroenterology. 2006;131:108–116
  26. Freshney RI. Culture of animal cells. New York: Wiley-Liss Inc; 1994;
  27. Banwait KS, Rattan S. Role of nitric oxide in β3-adrenoceptor activation on basal tone of internal anal sphincter. Am J Physiol Gastrointest Liver Physiol. 2003;285:G547–G555
  28. Bitar KN, Hillemeier C, Biancani P. Differential regulation of smooth muscle contraction in rabbit internal anal sphincter by substance P and bombesin. Life Sci. 1990;47:2429–2434
  29. Glavind EB, Forman A, Madsen G, et al. Mechanical properties of isolated smooth muscle from human rectum and internal anal sphincter. Am J Physiol. 1993;265:G792–G798
  30. Knudsen MA, Glavind EB, Tottrup A. Transmitter interactions in rabbit internal anal sphincter. Am J Physiol. 1995;269:G232–G239
  31. Ross JJ, Tranquillo RT. ECM gene expression correlates with in vitro tissue growth and development in fibrin gel remodeled by neonatal smooth muscle cells. Matrix Biol. 2003;22:477–490
  32. Huang YC, Dennis RG, Baar K. Development of a novel method for engineering 3-dimensional muscle for long-term culture of skeletal muscle. (Abstract) Washington, DC: Experimental biology; 2004;
  33. Kanada K, Matsuda T. Mechanical stress-induced orientation and ultrastructural change of smooth muscle cells cultured in three-dimensional collagen lattices. Cell Transplant. 1994;3:481–492
  34. Kim BS, Mooney DJ. Scaffolds for engineering smooth muscle under cyclic mechanical strain conditions. J Biomech Eng. 2000;122:210–215
  35. Lee AA, Graham DA, Dela Cruz S, et al. Fluid shear stress-induced alignment of cultured vascular smooth muscle cells. J Biomech Eng. 2002;124:37–43
  36. Stegemann J, Nerem RM. Effect of mechanical stimulation on smooth muscle cell proliferation and phenotype. Bioeng Conference. 2001;50:609–610
  37. Rembold CM, Foster DB, Strauss JD, et al. cGMP-mediated phosphorylation of heat shock protein 20 may cause smooth muscle relaxation without myosin light chain dephosphorylation in swine carotid artery. J Physiol. 2000;524:865–878
  38. Grassl ED, Oegema TR, Tranquillo RT. A fibrin-based arterial media equivalent. J Biomed Mater Res. 2003;66A:550–561
  39. Janis RA, Diamond J. Relationship between cyclic nucleotide levels and drug-induced relaxation of smooth muscle. J Pharmacol Exp Ther. 1979;211:480–484
  40. Moummi C, Rattan S. Effect of methylene blue and N-ethylmaleimide on internal anal sphincter relaxation. Am J Physiol. 1988;255:G571–G578
  41. Napoli JL, Mellon WS, Fivizzani MA, et al. Direct chemical synthesis of 1 α25-dihydroxy[26,27-3H]vitamin D3 with high specific activity: its use in receptor studies. Biochemistry. 1980;19:2515–2521

 Conflicts of interest The authors disclose no conflicts.

 Funding Supported by National Institutes of Health Grant NIDDK R01-DK071614.

PII: S0016-5085(09)00464-8

doi: 10.1053/j.gastro.2009.03.036

Gastroenterology
Volume 137, Issue 1 , Pages 53-61 , July 2009