Annals of Biomedical Engineering

, Volume 38, Issue 8, pp 2594–2605 | Cite as

Length Adaptation of the Passive-to-Active Tension Ratio in Rabbit Detrusor

  • Atheer M. Almasri
  • Paul H. Ratz
  • John E. Speich
Article
First Online:
Received:
Accepted:

Abstract

The passive and active length–tension (L–T p and L–T a) relationships in airway, vascular, and detrusor smooth muscles can adapt with length changes and/or multiple contractions. The present objectives were to (1) determine whether short-term adaptation at one muscle length shifts the entire L–T a curve in detrusor smooth muscle (DSM), (2) compare adaptation at shorter versus longer lengths, and (3) determine the effect of adaptation on the T p/T a ratio. Results showed that multiple KCl-induced contractions on the descending limb of the original L–T a curve adapted DSM strips to that length and shifted the L–T a curve rightward. Peak T a at the new length was not different from the original peak T a, and the L–T p curve shifted rightward with the L–T a curve. Multiple contractions on the ascending limb increased both T a and T p. In contrast, multiple contractions on the descending limb increased T a but decreased T p. The T p/T a ratio on the original descending limb adapted from 0.540 ± 0.084 to 0.223 ± 0.033 (mean ± SE, n = 7), such that it was not different from the ratio of 0.208 ± 0.033 at the original peak T a length, suggesting a role of length adaptation may be to maintain a desirable T p/T a ratio as the bladder fills and voids over a broad DSM length range.

Keywords

Bladder Lower urinary tract Smooth muscle contraction Adjustable passive stiffness Length–tension curve 

Abbreviations

0-Ca

Nominally Ca2+-free solution consisting of PSS without CaCl2

APS

Adjustable passive stiffness

ASM

Airway smooth muscle

DSM

Detrusor smooth muscle

KPSS

PSS modified to include 110 mM KCl substituted isosmotically for NaCl

L–T

Length–tension

L–Ta

Length–active tension

Lo

Optimal length for active tension generation

L–Tp

Length–passive tension

PSS

Physiological salt solution

Ta

Active tension

To

Peak, optimal T a

Tp

Passive tension

Tt

Total tension

VSM

Vascular smooth muscle

This is a preview of subscription content, log in to check access.

Notes

Acknowledgments

We gratefully acknowledge the expert technical assistance of Amy S. Miner and the support and guidance of Dr. Harry P. Koo. This study was supported by a grant from the Edwin Beer Research Program in Urology and Urology Related Fields from the New York Academy of Medicine (to J.E.S.). Some bladders used for these studies were from rabbits used for vascular smooth muscles studies supported by National Heart, Lung and Blood Institute Grant No. R01-HL61320 (to P.H.R.).

References

  1. 1.
    Almasri, A. M., P. H. Ratz, H. Bhatia, A. P. Klausner, and J. E. Speich. Rhythmic contraction generates adjustable passive stiffness in rabbit detrusor. J. Appl. Physiol. 108(3):544–553, 2010.CrossRefPubMedGoogle Scholar
  2. 2.
    Bai, T. R., J. H. Bates, V. Brusasco, B. Camoretti-Mercado, P. Chitano, L. H. Deng, M. Dowell, B. Fabry, L. E. Ford, J. J. Fredberg, W. T. Gerthoffer, S. H. Gilbert, S. J. Gunst, C. M. Hai, A. J. Halayko, S. J. Hirst, A. L. James, L. J. Janssen, K. A. Jones, G. G. King, O. J. Lakser, R. K. Lambert, A. M. Lauzon, K. R. Lutchen, G. N. Maksym, R. A. Meiss, S. M. Mijailovich, H. W. Mitchell, R. W. Mitchell, W. Mitzner, T. M. Murphy, P. D. Pare, R. R. Schellenberg, C. Y. Seow, G. C. Sieck, P. G. Smith, A. V. Smolensky, J. Solway, N. L. Stephens, A. G. Stewart, D. D. Tang, and L. Wang. On the terminology for describing the length-force relationship and its changes in airway smooth muscle. J. Appl. Physiol. 97(6):2029–2034, 2004.CrossRefPubMedGoogle Scholar
  3. 3.
    Bosse, Y., A. Sobieszek, P. D. Pare, and C. Y. Seow. Length adaptation of airway smooth muscle. Proc. Am. Thorac. Soc. 5(1):62–67, 2008.CrossRefPubMedGoogle Scholar
  4. 4.
    Brocklehurst, R. J. Studies on the physiology of plain muscle: The effect of alteration of initial length on the tension produced on contraction. J. Physiol. 61(2):275–281, 1926.PubMedGoogle Scholar
  5. 5.
    de Groat, W. C. A neurological basis for the overactive bladder. Urology 50:36–52, 1997.CrossRefPubMedGoogle Scholar
  6. 6.
    Dulin, N. O., D. J. Fernandes, M. Dowell, S. Bellam, J. McConville, O. Lakser, R. Mitchell, B. Camoretti-Mercado, P. Kogut, and J. Solway. What evidence implicates airway smooth muscle in the cause of BHR? Clin. Rev. Allergy Immunol. 24(1):73–84, 2003.CrossRefPubMedGoogle Scholar
  7. 7.
    Ford, L. E. Plasticity in airway smooth muscle: an update. Can. J. Physiol. Pharmacol. 83(10):841–850, 2005.CrossRefPubMedGoogle Scholar
  8. 8.
    Ford, L. E., C. Y. Seow, and V. R. Pratusevich. Plasticity in smooth muscle, a hypothesis. Can. J. Physiol. Pharmacol. 72(11):1320–1324, 1994.PubMedGoogle Scholar
  9. 9.
    Gordon, A. M., A. F. Huxley, and F. J. Julian. The variation in isometric tension with sarcomere length in vertebrate muscle fibres. J. Physiol. 184(1):170–192, 1966.PubMedGoogle Scholar
  10. 10.
    Gordon, A. R., and M. J. Siegman. Mechanical properties of smooth muscle. I. Length-tension and force-velocity relations. Am. J. Physiol. 221(5):1243–1249, 1971.PubMedGoogle Scholar
  11. 11.
    Gregersen, H., J. L. Emery, and A. D. McCulloch. History-dependent mechanical behavior of guinea-pig small intestine. Ann. Biomed. Eng. 26(5):850–858, 1998.CrossRefPubMedGoogle Scholar
  12. 12.
    Gunst, S. J., R. A. Meiss, M. F. Wu, and M. Rowe. Mechanisms for the mechanical plasticity of tracheal smooth muscle. Am. J. Physiol. 268(5 Pt 1):C1267–1276, 1995.PubMedGoogle Scholar
  13. 13.
    Gunst, S. J., and W. Zhang. Actin cytoskeletal dynamics in smooth muscle: A new paradigm for the regulation of smooth muscle contraction. Am. J. Physiol. Cell Physiol. 295(3):C576–587, 2008.CrossRefPubMedGoogle Scholar
  14. 14.
    Herlihy, J. T., and R. A. Murphy. Length-tension relationship of smooth muscle of the hog carotid artery. Circ. Res. 33(3):257–283, 1973.Google Scholar
  15. 15.
    Jezior, J. R., J. D. Brady, D. I. Rosenstein, K. A. McCammon, A. S. Miner, and P. H. Ratz. Dependency of detrusor contractions on calcium sensitization and calcium entry through LOE-908-sensitive channels. Br. J. Pharmacol. 134:78–87, 2001.CrossRefPubMedGoogle Scholar
  16. 16.
    Longhurst, P. A., J. S. Kang, A. J. Wein, and R. M. Levin. Comparative length-tension relationship of urinary bladder strips from hamsters, rats, guinea-pigs, rabbits and cats. Comp. Biochem. Physiol. A 96(1):221–225, 1990.CrossRefPubMedGoogle Scholar
  17. 17.
    Murphy, R. A., and C. M. Rembold. The latch-bridge hypothesis of smooth muscle contraction. Can. J. Physiol. Pharmacol. 83(10):857–864, 2005.CrossRefPubMedGoogle Scholar
  18. 18.
    Poley, R. N., C. R. Dosier, J. E. Speich, A. S. Miner, and P. H. Ratz. Stimulated calcium entry and constitutive RhoA kinase activity cause stretch-induced detrusor contraction. Eur. J. Pharmacol. 599:137–145, 2008.CrossRefPubMedGoogle Scholar
  19. 19.
    Pratusevich, V. R., C. Y. Seow, and L. E. Ford. Plasticity in canine airway smooth muscle. J. Gen. Physiol. 105(1):73–94, 1995.CrossRefPubMedGoogle Scholar
  20. 20.
    Seow, C. Y. Response of arterial smooth muscle to length perturbation. J. Appl. Physiol. 89(5):2065–2072, 2000.PubMedGoogle Scholar
  21. 21.
    Seow, C. Y., V. R. Pratusevich, and L. E. Ford. Series-to-parallel transition in the filament lattice of airway smooth muscle. J. Appl. Physiol. 89(3):869–876, 2000.PubMedGoogle Scholar
  22. 22.
    Silveira, P. S., J. P. Butler, and J. J. Fredberg. Length adaptation of airway smooth muscle: A stochastic model of cytoskeletal dynamics. J. Appl. Physiol. 99(6):2087–2098, 2005.CrossRefPubMedGoogle Scholar
  23. 23.
    Speden, R. N. The effect of initial strip length on the noradrenaline-induced contraction of arterial strips. J. Physiol. 154(1):15–25, 1960.PubMedGoogle Scholar
  24. 24.
    Speich, J. E., A. M. Almasri, H. Bhatia, A. P. Klausner, and P. H. Ratz. Adaptation of the length-active tension relationship in rabbit detrusor. Am. J. Physiol. Renal Physiol. 297(4):F1119–1128, 2009.CrossRefPubMedGoogle Scholar
  25. 25.
    Speich, J. E., L. Borgsmiller, C. Call, R. Mohr, and P. H. Ratz. ROK-induced cross-link formation stiffens passive muscle: Reversible strain-induced stress softening in rabbit detrusor. Am. J. Physiol. Cell Physiol. 289(1):C12–21, 2005.CrossRefPubMedGoogle Scholar
  26. 26.
    Speich, J. E., C. Dosier, L. Borgsmiller, K. Quintero, H. P. Koo, and P. H. Ratz. Adjustable passive length-tension curve in rabbit detrusor smooth muscle. J. Appl. Physiol. 102(5):1746–1755, 2007.CrossRefPubMedGoogle Scholar
  27. 27.
    Speich, J. E., K. Quintero, C. Dosier, L. Borgsmiller, H. P. Koo, and P. H. Ratz. A mechanical model for adjustable passive stiffness in rabbit detrusor. J. Appl. Physiol. 101(4):1189–1198, 2006.CrossRefPubMedGoogle Scholar
  28. 28.
    Syyong, H., C. Cheung, D. Solomon, C. Y. Seow, and K. H. Kuo. Adaptive response of pulmonary arterial smooth muscle to length change. J. Appl. Physiol. 104(4):1014–1020, 2008.CrossRefPubMedGoogle Scholar
  29. 29.
    Uvelius, B. Isometric and isotonic length-tension relations and variations in longitudinal smooth muscle from rabbit urinary bladder. Acta Physiol. Scand. 97(1):1–12, 1976.CrossRefPubMedGoogle Scholar
  30. 30.
    Uvelius, B. Length-tension relations of in vitro urinary bladder smooth muscle strips. J. Pharmacol. Toxicol. Methods 45(2):87–90, 2001.CrossRefPubMedGoogle Scholar
  31. 31.
    Wang, L., P. D. Pare, and C. Y. Seow. Plasticity in skeletal, cardiac, and smooth muscle: Selected contribution: Effect of chronic passive length change on airway smooth muscle length-tension relationship. J. Appl. Physiol. 90(2):734–740, 2001.PubMedGoogle Scholar

Copyright information

© Biomedical Engineering Society 2010

Authors and Affiliations

  • Atheer M. Almasri
    • 1
  • Paul H. Ratz
    • 2
  • John E. Speich
    • 1
  1. 1.Department of Mechanical EngineeringVirginia Commonwealth UniversityRichmondUSA
  2. 2.Departments of Biochemistry & Molecular Biology and PediatricsVirginia Commonwealth UniversityRichmondUSA

Personalised recommendations