Vasoresponsiveness of collateral vessels in the rat hindlimb: influence of training.

Patrick N Colleran, Zeyi Li, Hsiao T Yang, M Harold Laughlin, Ronald L Terjung
Author Information
  1. Patrick N Colleran: Department of Biomedical Sciences, College of Veterinary Medicine, University of Missouri, Columbia, MO 65211, USA.

Abstract

Exercise training is known to be an effective means of improving functional capacity and quality of life in patients with peripheral arterial insufficiency (PAI). However, the specific training-induced physiological adaptations occurring within collateral vessels remain to be clearly defined. The purpose of this study was to determine the effect of exercise training on vasomotor properties of isolated peripheral collateral arteries. We hypothesized that daily treadmill exercise would improve the poor vasodilatory capacity of collateral arteries isolated from rats exposed to surgical occlusion of the femoral artery. Following femoral artery ligation, animals were either kept sedentary or exercise trained daily for a period of 3 weeks. Hindlimb collateral arteries were then isolated, cannulated and pressurized via hydrostatic reservoirs to an intravascular pressure of either 45 or 120 cmH(2)O. Non-occluded contralateral vessels of the sedentary animals served as normal Control. Vasodilatory responses to acetylcholine (ACh; 1 x 10(9)-1 x 10(5)m) and sodium nitroprusside (SNP; 1 x 10(9)-1 x 10(4)m), constrictor responses to phenylephrine (PE; 1 x 10(9)-1 x 10(4)m), and flow-induced vasodilatation were determined. Endothelium-mediated vasodilatation responses were significantly greater to either ACh (P < 0.02) or intravascular flow (P < 0.001) in collateral arteries of trained rats. Neither blockade of cyclooxygenase with indomethacin (Indo; 5 microm) nor blockade of endothelial nitric oxide synthase with N(G)-nitro-L-arginine methyl ester (L-NAME; 300 microm) eliminated this ACh- or flow-induced vasodilatation. The depressed vasodilatory response to SNP caused by vascular occlusion was reversed with training. These data indicate that exercise training improves endothelium-mediated vasodilatory capacity of hindlimb collateral arteries, apparently by enhanced production of the putative endothelium-derived hyperpolarizing factor(s). If these findings were applicable to patients with PAI, they could contribute to an improved collateral vessel function and enhance exercise tolerance during routine physical activity.

References

  1. Circ Res. 1991 Nov;69(5):1340-52 [PMID: 1934361]
  2. J Appl Physiol. 1971 Oct;31(4):550-5 [PMID: 5111000]
  3. Cochrane Database Syst Rev. 2000;(2):CD000990 [PMID: 10796572]
  4. Microvasc Res. 2002 Nov;64(3):491-6 [PMID: 12453444]
  5. Am J Pathol. 2002 Jul;161(1):145-53 [PMID: 12107099]
  6. N Engl J Med. 2002 Dec 12;347(24):1941-51 [PMID: 12477945]
  7. Circulation. 2004 Feb 10;109(5):664-70 [PMID: 14769688]
  8. Am J Physiol. 1992 Jun;262(6 Pt 2):H1669-75 [PMID: 1621827]
  9. Am J Physiol Heart Circ Physiol. 2000 Jun;278(6):H1984-92 [PMID: 10843897]
  10. Am J Physiol Heart Circ Physiol. 2004 Dec;287(6):H2434-47 [PMID: 15271665]
  11. J Appl Physiol (1985). 1994 May;76(5):2241-7 [PMID: 7520432]
  12. Am J Physiol. 1997 Dec;273(6):H2575-9 [PMID: 9435589]
  13. Proc Natl Acad Sci U S A. 1991 Mar 15;88(6):2166-70 [PMID: 1848694]
  14. Am J Physiol. 1990 Mar;258(3 Pt 2):H759-65 [PMID: 2316692]
  15. Am J Physiol. 1995 Mar;268(3 Pt 2):H1174-80 [PMID: 7900871]
  16. Am J Physiol. 1991 Dec;261(6 Pt 2):H1706-15 [PMID: 1750529]
  17. J Cell Biol. 2001 Oct 15;155(2):271-8 [PMID: 11604422]
  18. J Vasc Res. 1997 May-Jun;34(3):237-43 [PMID: 9226306]
  19. Am J Physiol Heart Circ Physiol. 2002 Jan;282(1):H165-74 [PMID: 11748060]
  20. Pflugers Arch. 2002 Oct;445(1):51-4 [PMID: 12397386]
  21. Am J Physiol. 1998 Jun;274(6):H2053-61 [PMID: 9841532]
  22. Circ Res. 1992 Mar;70(3):546-53 [PMID: 1537090]
  23. Am J Physiol Heart Circ Physiol. 2000 Aug;279(2):H459-65 [PMID: 10924042]
  24. Circulation. 2003 Sep 9;108(10):1253-8 [PMID: 12874194]
  25. Circ Res. 1998 Nov 2;83(9):960-5 [PMID: 9797346]
  26. Arterioscler Thromb Vasc Biol. 2001 Feb;21(2):233-7 [PMID: 11156858]
  27. J Appl Physiol (1985). 1997 May;82(5):1438-44 [PMID: 9134890]
  28. J Appl Physiol (1985). 1999 Nov;87(5):1948-56 [PMID: 10562641]
  29. Exerc Sport Sci Rev. 2003 Jan;31(1):26-33 [PMID: 12562167]
  30. Circulation. 1998 Oct 20;98(16):1675-83 [PMID: 9778334]
  31. Circulation. 2001 Jan 2;103(1):E1-6 [PMID: 11136704]
  32. Am J Physiol Heart Circ Physiol. 2000 Oct;279(4):H1890-7 [PMID: 11009477]
  33. Stroke. 1998 Jun;29(6):1194-200; discussion 1200-1 [PMID: 9626294]
  34. Am J Physiol Heart Circ Physiol. 2003 May;284(5):H1668-78 [PMID: 12543634]
  35. J Appl Physiol (1985). 2004 Jan;96(1):233-44 [PMID: 12923113]
  36. Circ Res. 1995 Mar;76(3):448-56 [PMID: 7859390]
  37. Am J Physiol. 1991 Dec;261(6 Pt 2):H1797-801 [PMID: 1750535]
  38. J Appl Physiol (1985). 1997 Feb;82(2):460-8 [PMID: 9049725]
  39. Am J Physiol Heart Circ Physiol. 2001 Jun;280(6):H2462-9 [PMID: 11356599]
  40. Am J Physiol Heart Circ Physiol. 2002 Jan;282(1):H301-10 [PMID: 11748075]
  41. J Vasc Surg. 2005 Mar;41(3):436-42 [PMID: 15838477]
  42. J Physiol. 2004 Dec 1;561(Pt 2):575-82 [PMID: 15579542]
  43. J Vasc Res. 1996 Nov-Dec;33(6):471-9 [PMID: 8998196]
  44. Am J Physiol Heart Circ Physiol. 2001 Dec;281(6):H2528-38 [PMID: 11709420]
  45. Circulation. 2001 Sep 18;104(12):1393-8 [PMID: 11560855]
  46. Vasc Med. 1997 Nov;2(4):286-91 [PMID: 9575600]
  47. Circ Res. 1996 Oct;79(4):857-63 [PMID: 8831511]
  48. Am J Physiol. 1988 Sep;255(3 Pt 2):H446-51 [PMID: 3137826]
  49. Circ Res. 1994 Feb;74(2):349-53 [PMID: 7507417]
  50. J Appl Physiol (1985). 1995 Jul;79(1):73-82 [PMID: 7559251]
  51. Vascul Pharmacol. 2003 Oct;40(3):161-5 [PMID: 13678648]
  52. Arterioscler Thromb Vasc Biol. 2007 Apr;27(4):791-8 [PMID: 17234725]
  53. Am J Physiol Heart Circ Physiol. 2001 Jun;280(6):H2456-61 [PMID: 11356598]
  54. Circ Res. 1996 Mar;78(3):415-23 [PMID: 8593700]
  55. Am J Physiol Heart Circ Physiol. 2003 Apr;284(4):H1378-87 [PMID: 12595293]
  56. Hypertension. 2000 Jan;35(1 Pt 2):231-6 [PMID: 10642303]
  57. Arterioscler Thromb Vasc Biol. 2002 Jan;22(1):28-33 [PMID: 11788457]
  58. Circ Res. 1968 Aug;23(2):239-48 [PMID: 5662576]
  59. Angiogenesis. 2001;4(4):247-57 [PMID: 12197469]
  60. Am J Cardiol. 2001 Feb 1;87(3):324-9 [PMID: 11165969]
  61. J Cardiovasc Pharmacol. 1996 Oct;28(4):488-93 [PMID: 8891871]
  62. Am J Physiol. 1997 Sep;273(3 Pt 2):H1255-65 [PMID: 9321814]
  63. Circ Res. 1996 Jul;79(1):62-9 [PMID: 8925570]
  64. Am J Physiol. 1995 Jan;268(1 Pt 2):H125-37 [PMID: 7840257]
  65. Med Sci Sports Exerc. 1995 Aug;27(8):1152-7 [PMID: 7476059]
  66. JAMA. 1995 Sep 27;274(12):975-80 [PMID: 7674529]
  67. J Physiol. 2008 Mar 15;586(6):1649-67 [PMID: 18218679]
  68. Circ Res. 1995 Apr;76(4):544-50 [PMID: 7534658]
  69. J Surg Res. 1996 Mar;61(2):463-8 [PMID: 8656626]
  70. Circulation. 1990 Jun;81(6):1938-47 [PMID: 2111743]
  71. J Am Geriatr Soc. 2001 Jun;49(6):755-62 [PMID: 11454114]
  72. Am J Physiol Heart Circ Physiol. 2001 Sep;281(3):H1380-9 [PMID: 11514310]
  73. J Appl Physiol (1985). 2005 Feb;98(2):753-61 [PMID: 15448126]
  74. Am J Physiol. 1997 Nov;273(5):H2423-7 [PMID: 9374780]
  75. Microvasc Res. 1998 Jul;56(1):54-61 [PMID: 9683563]
  76. J Appl Physiol (1985). 1990 Oct;69(4):1353-9 [PMID: 2262453]
  77. Am J Physiol Heart Circ Physiol. 2002 Nov;283(5):H2012-20 [PMID: 12384480]
  78. Eur J Vasc Endovasc Surg. 2001 Feb;21(2):118-22 [PMID: 11237783]
  79. J Vasc Res. 1995 Mar-Apr;32(2):79-92 [PMID: 7537544]
  80. Am J Physiol. 1994 Dec;267(6 Pt 2):H2523-30 [PMID: 7529001]
  81. Fundam Clin Pharmacol. 1997;11(3):252-9 [PMID: 9243257]

Grants

  1. R01 HL037387/NHLBI NIH HHS
  2. R01-HL37387/NHLBI NIH HHS
  3. T32-AR48523/NIAMS NIH HHS
  4. R01 HL036088/NHLBI NIH HHS
  5. R01-HL36088/NHLBI NIH HHS
  6. T32 AR048523/NIAMS NIH HHS

MeSH Term

Adaptation, Physiological
Animals
Collateral Circulation
Disease Models, Animal
Endothelium, Vascular
Hindlimb
Nitric Oxide
Peripheral Vascular Diseases
Physical Conditioning, Animal
Prostaglandin-Endoperoxide Synthases
Rats
Rats, Sprague-Dawley
Regional Blood Flow
Signal Transduction
Vasoconstriction
Vasoconstrictor Agents
Vasodilation
Vasodilator Agents
Vasomotor System

Chemicals

Vasoconstrictor Agents
Vasodilator Agents
Nitric Oxide
Prostaglandin-Endoperoxide Synthases

Word Cloud

Created with Highcharts 10.0.0collateralx10trainingexercisearteriescapacityvesselsisolatedvasodilatoryeitherresponses19-1mvasodilatationpatientsperipheralPAIdailyratsocclusionfemoralarteryanimalssedentarytrainedintravascularACh5SNP4flow-inducedP<0blockademicromExerciseknowneffectivemeansimprovingfunctionalqualitylifearterialinsufficiencyHoweverspecifictraining-inducedphysiologicaladaptationsoccurringwithinremainclearlydefinedpurposestudydetermineeffectvasomotorpropertieshypothesizedtreadmillimprovepoorexposedsurgicalFollowingligationkeptperiod3weeksHindlimbcannulatedpressurizedviahydrostaticreservoirspressure45120cmH2ONon-occludedcontralateralservednormalControlVasodilatoryacetylcholinesodiumnitroprussideconstrictorphenylephrinePEdeterminedEndothelium-mediatedsignificantlygreater02flow001NeithercyclooxygenaseindomethacinIndoendothelialnitricoxidesynthaseNG-nitro-L-argininemethylesterL-NAME300eliminatedACh-depressedresponsecausedvascularreverseddataindicateimprovesendothelium-mediatedhindlimbapparentlyenhancedproductionputativeendothelium-derivedhyperpolarizingfactorsfindingsapplicablecontributeimprovedvesselfunctionenhancetoleranceroutinephysicalactivityVasoresponsivenessrathindlimb:influence

Similar Articles

Cited By