Skip to main content

Advertisement

Log in

Short-duration increases in intraluminal pressure improve vasoconstrictor responses in aged skeletal muscle feed arteries

  • Original Article
  • Published:
European Journal of Applied Physiology Aims and scope Submit manuscript

Abstract

Purpose

We tested the hypothesis that exposure to a short-duration (1 h) increase in intraluminal pressure, to mimic pressure associated with a bout of exercise, would attenuate age-induced impairments of vascular smooth muscle (VSM) constrictor responses in soleus muscle feed arteries (SFA) via the Rho pathway.

Methods

SFA from young (4 months) and old (24 months) Fischer 344 rats were cannulated and pressurized to 90 or 130 cmH2O for 1 h. Following the 1-h treatment, pressure in P130 arteries was lowered to 90 cmH2O for examination of vasoconstrictor responses to norepinephrine (NE), angiotensin II (Ang II), and phenylephrine (PE). To assess the role of the Rho pathway, vasoconstrictor responses were assessed in the absence or presence of a RhoA-kinase inhibitor (Y27632) or RhoA-kinase activator (LPA).

Results

Vasoconstrictor responses to NE, Ang II, and PE were impaired in old P90 SFA. Pretreatment of old SFA with increased pressure improved vasoconstrictor responses to NE, PE and Ang II. The beneficial effect of the pressure pretreatment in old SFA was eliminated in the presence of Y27632. In the presence of LPA, vasoconstrictor responses to Ang II were improved in old SFA such that responses were not different than young P90 SFA.

Conclusion

These results indicate that a short-duration exposure to increased intraluminal pressure, to mimic pressure associated with a bout of exercise, attenuates or reverses the age-related decrement in VSM constrictor responses in SFA and that the beneficial response is mediated through Rho kinase.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

Ang II:

Angiotensin II

PE:

Phenylephrine

NIA:

National Institute on Aging

NE:

Norepinephrine

PSS:

Physiological saline solution

ROCK:

Rho kinase

SFA:

Soleus muscle feed arteries

References

  • Amano M, Chihara K, Kimura K, Fukata Y, Nakamura N, Matsuura Y, Kaibuchi K (1997) Formation of actin stress fibers and focal adhesions enhanced by Rho-kinase. Science 275:1308–1311

    Article  CAS  PubMed  Google Scholar 

  • Celermajer D, Sorensen K, Spiegelhalter D, Georgakopoulos D, Robinson J, Deanfield J (1994) Aging is associated with endothelial dysfunction in healthy men years before the age-related decline in women. J Am Coll Cardiol 24:471–476

    Article  CAS  PubMed  Google Scholar 

  • Delp MD, Brown M, Laughlin MH, Hasser EM (1995) Rat aortic vasoreactivity is altered by old age and hindlimb unloading. J Appl Physiol 78:2079–2086

    CAS  PubMed  Google Scholar 

  • Delp MD, Behnke BJ, Spier SA, Wu G, Muller-Delp JM (2008) Ageing diminishes endothelium-dependent vasodilatation and tetrahydrobiopterin content in rat skeletal muscle arterioles. J Physiol 586:1161–1168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dinenno FA, Dietz NM, Joyner MJ (2002) Aging and forearm postjunctional α-adrenergic vasoconstriction in healthy men. Circulation 106:1349–1354

    Article  CAS  PubMed  Google Scholar 

  • Donato AJ, Lesniewski LA, Delp MD (2005) The effects of aging and exercise training on endothelin-1 vasoconstrictor responses in rat skeletal muscle arterioles. Cardiovasc Res 66:393–401

    Article  CAS  PubMed  Google Scholar 

  • Donato AJ, Lesniewski LA, Delp MD (2007) Ageing and exercise training alter adrenergic vasomotor responses of rat skeletal muscle arterioles. J Physiol 579:115–125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ghosh P, Solis FRM, Dominguez JM, Spier SA, Donato AJ, Delp MD, Muller-Delp JM (2015) Exercise training reverses aging-induced impairment of myogenic constriction in skeletal muscle arterioles. J Appl Physiol 118:904–911

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ishihata A, Katano Y, Morinobu S, Endoh M (1991) Influence of aging on the contractile response to endothelin of rat thoracic aorta. Eur J Pharmacol 200:199–201

    Article  CAS  PubMed  Google Scholar 

  • Kenney WL, Armstrong CG (1996) Reflex peripheral vasoconstriction is diminished in older men. J Appl Physiol 80:512–515

    CAS  PubMed  Google Scholar 

  • Kimura K, Ito M, Amano M, Chihara K, Fukata Y, Nakafuku M, Yamamori B, Feng J, Nakano T, Okawa K, Iwamatsu A, Kaibuchi K (1996) Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase). Science 273:245–248

    Article  CAS  PubMed  Google Scholar 

  • Lim S-M, Kreipe BA, Trzeciakowski J, Dangott L, Trache A (2010) Extracellular matrix effect on RhoA signaling modulation in vascular smooth muscle cells. Exp Cell Res 316:2833–2848

    Article  CAS  PubMed  Google Scholar 

  • Lim S-M, Trzeciakowski JP, Sreenivasappa H, Dangott LJ, Trache A (2012) RhoA-induced cytoskeletal tension controls adaptive cellular remodeling to mechanical signaling. Integr Biol 4:615–627

    Article  CAS  Google Scholar 

  • Loirand G, Guérin P, Pacaud P (2006) Rho kinases in cardiovascular physiology and pathophysiology. Circ Res 98:322–334

    Article  CAS  PubMed  Google Scholar 

  • Muller-Delp JM, Spier SA, Ramsey MW, Delp MD (2002) Aging impairs endothelium- dependent vasodilation in rat skeletal muscle arterioles. Am J Physiol Heart Circ Physiol 283:H1662–H1672

    Article  CAS  PubMed  Google Scholar 

  • Musch TI, Eklund KE, Hageman KS, Poole DC (2004) Altered regional blood flow responses to submaximal exercise in older rats. J Appl Physiol 96:81–88

    Article  PubMed  Google Scholar 

  • Park Y, Prisby RD, Behnke BJ, Dominguez JM, Lesniewski LA, Donato AJ, Muller-Delp J, Delp MD (2012) Effects of aging, TNF-α, and exercise training on angiotensin II- induced vasoconstriction of rat skeletal muscle arterioles. J Appl Physiol 113:1091–1100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qiu H, Zhu Y, Sun Z, Trzeciakowski JP, Gansner M, Depre C, Resuello RRG, Natividad FF, Hunter WC, Genin GM, Elson EL, Vatner DE, Meininger GA, Vatner SF (2010) Short communication: vascular smooth muscle cell stiffness as a mechanism for increased aortic stiffness with aging. Circ Res 107:615–619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Satoh K, Fukumoto Y, Shimokawa H (2011) Rho-kinase: important new therapeutic target in cardiovascular diseases. Am J Physiol Heart Circ Physiol 301:H287–H296

    Article  CAS  PubMed  Google Scholar 

  • Seawright J, Luttrell M, Woodman C (2014) Acute increases in intraluminal pressure improve vasodilator responses in aged soleus muscle feed arteries. Eur J Appl Physiol 114:1–9

    Article  Google Scholar 

  • Sindler AL, Delp MD, Reyes R, Wu G, Muller-Delp JM (2009) Effects of ageing and exercise training on eNOS uncoupling in skeletal muscle resistance arterioles. J Physiol 587:3885–3897

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Somlyo AP, Somlyo AV (2000) Signal transduction by G-proteins, Rho-kinase and protein phosphatase to smooth muscle and non-muscle myosin II. J Physiol 522:177–185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Spier SA, Delp MD, Meininger CJ, Donato AJ, Ramsey MW, Muller-Delp JM (2004) Effects of ageing and exercise training on endothelium-dependent vasodilatation and structure of rat skeletal muscle arterioles. J Physiol 556:947–958

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trott DW, Gunduz F, Laughlin MH, Woodman CR (2009) Exercise training reverses age-related decrements in endothelium-dependent dilation in skeletal muscle feed arteries. J Appl Physiol 106:1925–1934

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trott DW, Seawright JW, Luttrell MJ, Woodman CR (2011) NAD(P)H oxidase-derived reactive oxygen species contribute to age-related impairments of endothelium-dependent dilation in rat soleus feed arteries. J Appl Physiol 110:1171–1180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trott D, Luttrell M, Seawright J, Woodman C (2013) Aging impairs PI3K/Akt signaling and NO-mediated dilation in soleus muscle feed arteries. Eur J Appl Physiol 113:1–8

    Article  Google Scholar 

  • Williams D, Segal S (1993a) Feed artery role in blood flow control to rat hindlimb skeletal muscles. J Physiol 463:631–646

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Williams DA, Segal SS (1993b) Feed artery role in blood flow control to rat hindlimb skeletal muscles. J Physiol 463:631–646

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Woodman CR, Price EM, Laughlin MH (2002) Aging induces muscle-specific impairment of endothelium-dependent dilation in skeletal muscle feed arteries. J Appl Physiol 93:1685–1690

    Article  PubMed  Google Scholar 

  • Woodman CR, Trott DW, Laughlin MH (2007) Short-term increases in intraluminal pressure reverse age-related decrements in endothelium-dependent dilation in soleus muscle feed arteries. J Appl Physiol 103:1172–1179

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This work was supported by American Heart Association, South Central Affiliate Grants 0765043Y, 4150031 (C.R. Woodman), a Texas A&M University College of Education and Human Development Strategic Research Award (J.W. Seawright), and a Sydney and J.L. Huffines Institute of Sports Medicine and Human Performance Grant (J.W. Seawright). Additionally, the authors appreciate the Office for Biological Resources of NIA-NIH, for access to their Fisher 344 rat colony.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Christopher R. Woodman.

Ethics declarations

Conflict of interest

The authors have no conflicts of interest.

Additional information

Communicated by David C. Poole.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Seawright, J.W., Trache, A., Wilson, E. et al. Short-duration increases in intraluminal pressure improve vasoconstrictor responses in aged skeletal muscle feed arteries. Eur J Appl Physiol 116, 931–937 (2016). https://doi.org/10.1007/s00421-016-3350-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00421-016-3350-x

Keywords

Navigation