Journal of Applied Physiology Fuel your research with LabChart
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

J Appl Physiol 99: 995-998, 2005. First published May 12, 2005; doi:10.1152/japplphysiol.00319.2005
8750-7587/05 $8.00
This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF) Free
Right arrow All Versions of this Article:
99/3/995    most recent
00319.2005v1
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via ISI Web of Science (4)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Kluess, H. A.
Right arrow Articles by Clifford, P. S.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Kluess, H. A.
Right arrow Articles by Clifford, P. S.

Elevated temperature decreases sensitivity of P2X purinergic receptors in skeletal muscle arteries

Heidi A. Kluess, John B. Buckwalter, Jason J. Hamann, and Philip S. Clifford

Departments of Anesthesiology and Physiology, Medical College of Wisconsin, and Veterans Affairs Medical Center, Milwaukee, Wisconsin

Submitted 21 March 2005 ; accepted in final form 9 May 2005


   ABSTRACT
TOP
 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 
We hypothesized that elevated temperatures would attenuate but that reduced temperatures would potentiate the tension mediated by vascular P2X purinergic receptors. The femoral arteries of 24 rats were dissected out and placed in modified Krebs-Henseleit buffer. Arteries were cut into 2-mm sections and mounted in organ tissue baths. Maximal tension (g) was measured during a KCl and norepinephrine challenge. Tension was measured during doses of {alpha},{beta}-methylene ATP (10–7 to 10–3 M), phenylephrine (10–7 to 10–4 M), and acetylcholine (10–9 to 10–5 M), with tissue bath temperature adjusted to 35, 37, and 41°C. Dose-response curves were fit using nonlinear regression analysis to calculate the EC50 and slope. The peak tension was lower with {alpha},{beta}-methylene ATP during 41°C (1.49 ± 0.14 g) compared with 35°C (2.08 ± 0.09 g) and 37°C (1.94 ± 0.09 g; P < 0.05). Slope and EC50 were not affected by temperature. Tension produced by phenylephrine and relaxation to acetylcholine were not affected by temperature. These data indicate that the vasoconstrictor response to {alpha},{beta}-methylene ATP is sensitive to temperature. Moderate cooling does not potentiate P2X-mediated vasoconstriction, but elevated temperature attenuates the vasoconstrictor response to P2X purinergic receptors.

cold; adenosine 5'-triphosphate; femoral artery; sympatholysis

PURINERGIC RECEPTORS ARE PRESENT in most organ systems in the body, and there is accumulating evidence that they play an important role in vascular control in the tail, ear, mesenteric, and skeletal muscle vascular beds (1, 2, 4, 10, 11, 19, 25). In skeletal muscle, vasoconstriction is predominantly mediated by norepinephrine release from adrenergic neurons, which stimulates both {alpha}1- and {alpha}2-postjunctional receptors on vascular smooth muscle. However, recent evidence from our laboratory implicates P2X purinergic receptors on vascular smooth muscle in tonic vasoconstriction in skeletal muscle at rest and during exercise (2, 4). These receptors are activated by ATP, which is a cotransmitter released with norepinephrine from the sympathetic nerves (11, 12, 15, 24).

Our laboratory has previously shown that the responsiveness of vascular P2X receptors is attenuated with heavy exercise in dogs (2). A similar attenuation of sympathetic responsiveness also occurs with {alpha}2-receptors (3, 6, 28) and is termed "functional sympatholysis" (21). Although this phenomenon is well described, the mechanism by which sympatholysis occurs is not well understood. Heavy exercise causes a variety of chemical and environmental changes in the interstitium of exercising skeletal muscle. In particular, acidic pH and elevated temperature have the potential to influence vascular function (16, 18, 26). Previous research found that vasoconstriction via {alpha}2-receptors in skeletal muscle is enhanced by cold and attenuated by heat (7, 8, 14, 17, 22). The effect of temperature on P2X receptors in skeletal muscle is not known. However, heat is known to attenuate the response to activation of P2X receptors in smooth muscle of the bladder (32, 33).

Therefore, we wanted to explore whether P2X receptors in skeletal muscle arteries were sensitive to physiological temperature extremes equivalent to core body temperatures that would be seen during moderate hypothermia (35°C) and heavy exercise (41°C) (5). We hypothesized that cold would potentiate, whereas heat would attenuate, P2X receptor-mediated vasoconstriction in skeletal muscle conduit arteries.


   METHODS
TOP
 ABSTRACT
 METHODS
RESULTS
 DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 
Animals.   Experimental procedures described below were approved by the Institutional Animal Care and Use Committees of the Medical College of Wisconsin and Veterans Affairs Medical Center. Femoral artery ring segments (2 mm) were taken from male Sprague-Dawley rats (339.6 ± 10.5 g body wt) after anesthesia with pentobarbital sodium. The vessels were placed in a Krebs-Henseleit buffer solution (Sigma, St. Louis, MO) with HEPES (10 mM, Sigma), sodium bicarbonate (25 mM, ICN, Aurora, OH), and calcium chloride (0.95 mM, ICN) added. They were dissected free of connective tissue and cut into ring segments (2 mm). Segments were mounted on tungsten triangular holders, connected to a force transducer, and positioned in 15-ml organ baths containing modified Krebs-Henseleit buffer solution. Baths were continuously bubbled with a mixture of 5% CO2-95% O2. The tension of the vessel segments was set to 0.5 g and allowed to stabilize for 30 min at pH 7.4 and 37°C (31). Viability of the smooth muscle was assessed by contraction to phenylephrine (10–5 M, Baxter Healthcare, Irvine, CA), and the viability of the endothelium was assessed by at least 20% relaxation to acetylcholine (10–5 M, Sigma) (23). Maximal tension was measured during a potassium chloride (80 mM) and norepinephrine (10–6 M) challenge.

Protocols.   The response to the P2X agonist, {alpha},{beta}-methylene ATP (mATP; 10–7 to 10–3 M), was measured with tissue bath temperature adjusted to 35, 37, and 41°C with a Haake B3 Fisons circulating water bath (Karlsruhe, Germany) and monitored by a digital thermometer. After a change in temperature, the vessels were allowed to equilibrate for at least 3 min before agonists were added. The order of the temperatures was randomized with 35 and 37°C. Because of evidence that prior heating affects receptor-mediated vasoconstriction, the 41°C condition was always performed last (22).

Baths were rinsed five times over 15 min between each concentration to avoid P2X desensitization by mATP. The order of mATP concentrations was randomized within each temperature. Cumulative {alpha}1-agonist, phenylephrine, curves using bath concentrations of 10–7 to 10–4 M were performed in 12 rats at 35, 37, and 41°C. To assess the temperature sensitivity of the endothelium, the artery rings from six rats were preconstricted with phenylephrine (10–5 M), and then a cumulative acetylcholine curve (10–9 to 10–5 M) was performed with the organ baths at 35, 37, and 41°C.

Data analysis.   Results are expressed as means ± SE. Data are expressed in absolute tension in grams and as percentage of the maximal tension produced during the potassium chloride and norepinephrine challenge. Dose-response curves were fit using nonlinear regression analysis to calculate the concentration of the drug that produces 50% of the peak tension (EC50) and the slope. Percent maximal values were used for regression analysis. Statistical analysis of minimum tension, peak tension, EC50, and the slope for mATP, phenylephrine, and acetylcholine were assessed using a one-way analysis of variance followed by Tukey's post hoc test when appropriate.


   RESULTS
TOP
 ABSTRACT
 METHODS
 RESULTS
DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 
The average bath temperatures were 34.9 ± 0.6°C for 35°C, 37.1 ± 0.4°C for 37°C, and 40.9 ± 0.8°C for 41°C. Figure 1 is a summary of the tension produced at each mATP concentration with 35, 37, and 41°C. Peak tension produced by mATP with 35°C (2.08 ± 0.09 g) and 37°C (1.94 ± 0.09 g) was higher than peak tension produced with 41°C (1.49 ± 0.14 g; P < 0.05). EC50 and slope were not affected by temperature (P > 0.05; Table 1). The mean R values for the regression curve fits were 0.97 ± 0.02 for 35°C, 0.96 ± 0.04 for 37°C, and 0.96 ± 0.04 for 41°C.



View larger version (14K):
[in this window]
[in a new window]
  		Fig. 1. Dose-response curves for {alpha},{beta}-methylene ATP (mATP) with bath temperatures of 35, 37, and 41°C. Values are means ± SE for 6 rats. Heating attenuated relative tension produced by mATP. *P < 0.05 different from 35°C. +P < 0.05, different from 35 and 37°C.

 

View this table:
[in this window]
[in a new window]
  		Table 1. Mean EC50 and slope for temperatures of 35, 37, and 41°C

 
Figure 2 displays the tension produced at each phenylephrine concentration with 35, 37, and 41°C. The peak tension produced by phenylephrine (1.96 ± 0.13 g), the EC50, and the slope were not significantly affected by temperature (see Table 1 for the mean EC50 and slope at each temperature). The mean R values for the regression curve fits were 0.98 ± 0.05 for 35°C, 0.99 ± 0.01 for 37°C, and 0.98 ± 0.05 for 41°C.



View larger version (14K):
[in this window]
[in a new window]
  		Fig. 2. Dose-response curves for phenylephrine with bath temperatures of 35, 37, and 41°C. Values are means ± SE for 12 rats. There was no effect of temperature on relative tension produced by the {alpha}1-agonist, phenylephrine (P > 0.05).

 
The response at each acetylcholine concentration with 35, 37, and 41°C is shown in Fig. 3. Relaxation to acetylcholine was not affected by temperature (P > 0.05). There was no difference in EC50 or slope at temperatures of 35, 37, and 41°C (P > 0.05; Table 1). The mean R values for the regression curve fits were 0.94 ± 0.07 for 35°C, 0.98 ± 0.02 for 37°C, and 0.97 ± 0.04 for 41°C.



View larger version (15K):
[in this window]
[in a new window]
  		Fig. 3. Dose-response curves for acetylcholine with bath temperatures of 35, 37, and 41°C. Values are means ± SE for 6 rats. There was no effect of temperature on relative tension produced by the endothelium-dependent dilator acetylcholine (P > 0.05).

 

   DISCUSSION
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 
These data indicate that moderate cooling does not potentiate P2X-mediated vasoconstriction but that elevated temperature attenuates the vasoconstrictor response to P2X purinergic receptors. The effect of temperature was not nonspecific because tension produced by the {alpha}1-agonist, phenylephrine, was temperature insensitive. Furthermore, endothelium-dependent dilation with acetylcholine was not altered by temperature, suggesting that the endothelium was not responsible for the effect of temperature on vasoconstriction to mATP.

In agreement with Ziganshin et al. (32, 33), we found that heat attenuated P2X-mediated constriction. To our knowledge, there are no other studies that have looked at the effect of heat on P2X-mediated vasoconstriction in vascular smooth muscle. There are several mechanisms that should be considered as potential explanations for our findings, including alterations in calcium channels, the endothelium, ATP availability, or the P2X receptor.

A previous study suggested that changes in vasoconstriction with heat is caused by calcium channel activation. In vessels pretreated with phenylephrine or potassium chloride, calcium channels were sensitive to heat, resulting in an increase in tension (16). However, this effect appears to be specific to the heating protocol used because Massett et al. (16) also found no effect of heating on tension when phenylephrine was added after heating had occurred. In agreement with the latter observation, we found no effect of temperature on tension produced by the {alpha}1-agonist, phenylephrine. The heating protocol where the vessel is allowed to equilibrate at the temperature before addition of an agonist is the more traditional protocol for examining the effect of heating and has been used in numerous studies (14, 16, 17, 20, 22, 32, 33). On the basis of our results, it seems unlikely that calcium channels are involved in the effect of heat on P2X-mediated vasoconstriction.

The endothelium is also a potential source of temperature sensitivity in the femoral artery. There is some evidence that heat can increase endothelial nitric oxide release and intracellular calcium concentration in endothelial cells (9, 29). However, we found no effect of temperature on vascular smooth muscle relaxation to acetylcholine. This finding is in agreement with Ryan et al. (22), who found no effect of heat on dilation to acetylcholine until temperature exceeded 43°C. Additionally, Massett et al. (16) found that endothelium removal did not alter the effect of heating on vascular responses to phenylephrine and potassium chloride. Together with previous data, our acetylcholine curves suggest that endothelial modulation of vascular smooth muscle tone is not affected by temperature.

Although our data indicate that P2X receptors are sensitive to heat, the mechanism by which heat influences the bioavailability of ATP, ATP binding to the P2X receptor, or the P2X receptor itself is not well understood. It is conceivable that heat may cause an increase in the activity of ecto-ATPase and thus reduce the bioavailability of ATP. Although this mechanism may occur in vivo, it is unlikely in the present study because we used mATP, which is resistant to breakdown by ATPase (33).

In view of the above considerations, it appears that the mechanism of heat-induced decrease in tension with mATP application is most likely due to an intrinsic change in the P2X receptor. It should be noted that the increased tension produced by mATP is attributable solely to activation of P2X receptors such that the purinergic-2 antagonist, pyridoxal-phosphate-6-azophenyl-2'4'-disulfonic acid, totally abolishes the response (13). In agreement with Ziganshin et al. (33) we saw a significant decrease in maximal tension produced by mATP at the three highest doses with heat but no effect of heat on EC50 or slope of the dose-response curve. The lack of change in EC50 or the slope of the dose-response curve suggests that the sensitivity of the P2X receptor to ATP is unchanged by heat (27). Furthermore, Stoop et al. (27) suggested that a decrease in peak current to ATP application is an indicator of a reduction in ion pore permeability rather than a modification in the ligand or ligand binding. We speculate that this may be the mechanism whereby heat attenuates P2X-mediated vasoconstriction; however, this hypothesis would have to be confirmed by patch clamp experiments.

Our data indicate that moderate cooling did not potentiate vasoconstriction mediated by P2X receptors. Other studies that have shown significant cold potentiation in the bladder, cutaneous veins, and the mesenteric arterial bed employed temperatures of 30°C or lower, which indicates that there may be a threshold temperature for cold potentiation of P2X-mediated vasoconstriction (8, 30, 32). Although these very low temperatures may occur in the cutaneous circulation and during anesthetized surgery, we were specifically interested in temperatures that could occur in deep arteries under normal ambulatory conditions (8, 30). Therefore, we used a cold temperature of 35°C because deep arterial blood should be near core temperature with 35°C equivalent to moderate hypothermia (intense shivering and impaired coordination) (5). In summary, we did not observe cold potentiation of P2X-mediated vasoconstriction in skeletal muscle arteries. Although we cannot exclude the possibility that cold potentiation occurs, it happens at temperatures lower than would normally be encountered.

The physiological significance of these findings is that they provide a potential mechanism to explain observations regarding skeletal muscle vasculature during exercise (2, 4). Recently, our laboratory demonstrated that P2X receptors mediate tonic vasoconstriction in exercising skeletal muscle (4). However, the amount of vasoconstriction to exogenously administered mATP was attenuated during heavy exercise. We hypothesized that the mechanism of this attenuation may be related to changes in pH or temperature within the leg during exercise. Previously, we have shown that P2X receptors are sensitive to pH (13). These findings in conjunction with the present data suggest that acidosis and heat in the interstitium of exercising skeletal muscle provide a plausible mechanism for the observation of reduced sensitivity of vascular P2X receptors during dynamic exercise (2, 4).

In conclusion, P2X receptors on the femoral artery are not sensitive to moderate cooling, but they are sensitive to heating. Heating resulted in an attenuation of tension with mATP but did not affect tension produced by phenylephrine and relaxation with acetylcholine. It is unlikely that the effect of heating in femoral artery rings is a result of factors such as calcium channels or the endothelium. Further study using patch clamping of cloned receptors will be required to elucidate the mechanism by which P2X receptors are affected by heat.


   GRANTS
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 GRANTS
ACKNOWLEDGMENTS
 REFERENCES
 
This project was supported by the National Heart, Lung, and Blood Institute and the Medical Research Service of the Department of Veterans Affairs.


   ACKNOWLEDGMENTS
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
REFERENCES
 
The authors acknowledge the technical assistance of Kelly Allbee. We also thank Andrew Williams and Richard Rys for engineering and maintenance of our laboratory equipment.


   FOOTNOTES
 

Address for reprint requests and other correspondence: P. Clifford, 151 Anesthesia Research, VA Medical Center, Milwaukee, WI 53295 (E-mail: pcliff{at}mcw.edu)

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.


   REFERENCES
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 

  1. Bao JX and Stjarne L. Dual contractile effects of ATP released by field stimulation revealed by effects of {alpha},{beta}-methylene ATP and suramin in rat tail artery. Br J Pharmacol 110: 1421–1428, 1993.[ISI][Medline]
  2. Buckwalter JB, Hamann JJ, and Clifford PS. Vasoconstriction in active skeletal muscles: a potential role for P2X purinergic receptors? J Appl Physiol 95: 953–959, 2003.[Abstract/Free Full Text]
  3. Buckwalter JB, Naik JS, Valic Z, and Clifford PS. Exercise attenuates {alpha}-adrenergic-receptor responsiveness in skeletal muscle vasculature. J Appl Physiol 90: 172–178, 2001.[Abstract/Free Full Text]
  4. Buckwalter JB, Taylor JC, Hamann JJ, and Clifford PS. Do P2X purinergic receptors regulate skeletal muscle blood flow during exercise? Am J Physiol Heart Circ Physiol 286: H633–H639, 2004.[Abstract/Free Full Text]
  5. Brooks GA, Fahey TD, and White TP. Exercise in the heat and cold. In: Exercise Physiology: Human Bioenergetics and Its Application. Mountain View, CA: Mayfield, 1996, chapt. 22, p. 428–452.
  6. Dinneno FA and Joyner MJ. Blunted sympathetic vasoconstriction in contracting skeletal muscle of healthy humans: is nitric oxide obligatory? J Physiol 553: 281–292, 2003.[Abstract/Free Full Text]
  7. Flavahan NA and Vanhoutte PM. Effect of cooling on alpha-1 and alpha-2 adrenergic responses in canine saphenous and femoral veins. J Pharmacol Exp Ther 238: 139–147, 1986.[Abstract/Free Full Text]
  8. Flavahan NA and Vanhoutte PM. Sympathetic purinergic vasoconstriction and thermosensitivity in a canine cutaneous vein. J Pharmacol Exp Ther 239: 784–789, 1986.[Abstract/Free Full Text]
  9. Harris MB, Blackstone MA, Ju H, Venema VJ, and Venema RC. Heat-induced increases in endothelial NO synthase expression and activity and endothelial NO release. Am J Physiol Heart Circ Physiol 285: H333–H340, 2003.[Abstract/Free Full Text]
  10. Johnson CD, Coney AM, and Marshall JM. Roles of norepinephrine and ATP in sympathetically evoked vasoconstriction in rat tail and hindlimb in vivo. Am J Physiol Heart Circ Physiol 281: H2432–H2440, 2001.[Abstract/Free Full Text]
  11. Kennedy C, Saville VL, and Burnstock G. The contributions of noradrenaline and ATP to the responses of the rabbit central ear artery to sympathetic nerve stimulation depend on the parameters of stimulation. Eur J Pharmacol 122: 291–300, 1986.[CrossRef][ISI][Medline]
  12. King BF, Ziganshina LE, Pintor J, and Burnstock G. Full sensitivity of P2X2 purinoceptor to ATP revealed by changing extracellular pH. Br J Pharmacol 117: 1371–1373, 1996.[ISI][Medline]
  13. Kluess HA, Buckwalter JB, Hamann JJ, and Clifford PS. Acidosis attenuates P2X purinergic vasoconstriction in skeletal muscle arteries. Am J Physiol Heart Circ Physiol 288: H129–H132, 2005.[Abstract/Free Full Text]
  14. Kregel KC and Gisolfi CV. Circulatory responses to vasoconstrictor agents during passive heating in the rat. J Appl Physiol 68: 1220–1227, 1990.[Abstract/Free Full Text]
  15. Martin GN, Thom SAM, and Sever PS. The effects of adenosine triphosphate (ATP) and related purines on human subcutaneous and omental resistance arteries. Br J Pharmacol 102: 645–650, 1991.[ISI][Medline]
  16. Massett MP, Lewis SJ, Bates JN, and Kregel KC. Modulation of temperature-induced tone by vasoconstrictor agents. J Appl Physiol 86: 963–969, 1999.[Abstract/Free Full Text]
  17. Massett MP, Lewis SJ, and Kregel KC. Effect of heating on the hemodynamic responses to vasoactive agents. Am J Physiol Regul Integr Comp Physiol 275: R844–R853, 1998.[Abstract/Free Full Text]
  18. Medbo JI, Hanem S, Noddeland H, and Jebens E. Arterio-venous differences of blood acid-base status and plasma sodium caused by intense bicycling. Acta Physiol Scand 168: 311–326, 2000.[CrossRef][ISI][Medline]
  19. Morris JL. Cotransmission from sympathetic vasoconstrictor neurons to small cutaneous arteries in vivo. Am J Physiol Heart Circ Physiol 277: H58–H64, 1999.[Abstract/Free Full Text]
  20. Price JM and Wilmoth FR. Elevated body temperature and increased blood vessel sensitivity in spontaneously hypertensive rats. Am J Physiol Heart Circ Physiol 258: H946–H953, 1990.[Abstract/Free Full Text]
  21. Remensnyder JP, Mitchell JH, and Sarnoff SJ. Functional sympatholysis during muscular activity. Circ Res 11: 370–380, 1962.[Abstract/Free Full Text]
  22. Ryan AJ and Gisolfi CV. Responses of rat mesenteric arteries to norepinephrine during exposure to heat stress acidosis. J Appl Physiol 78: 38–45, 1995.[Abstract/Free Full Text]
  23. Schneider F, Bucher B, Schott C, Andre A, Julou-Schaeffer G, and Stoclet JC. Effect of bacterial liposaccharide on function of rat small femoral arteries. Am J Physiol Heart Circ Physiol 266: H191–H198, 1994.[Abstract/Free Full Text]
  24. Schwiebert EM and Zsembery A. Extracellular ATP as a signaling molecule for epithelial cells. Biochim Biophys Acta 1615: 7–32, 2003.[Medline]
  25. Sjoblom-Widfeldt N and Nilsson H. Sympathetic transmission in small mesenteric arteries: influence of impulse pattern. Acta Physiol Scand 138: 523–528, 1990.[ISI][Medline]
  26. Smith GL, Austin C, Crichton C, and Wray S. A review of the actions and control of intracellular pH in vascular smooth muscle. Cardiovasc Res 38: 316–331, 1998.[Abstract/Free Full Text]
  27. Stoop R, Suprenant A, and North A. Different sensitivities to pH of ATP-induced currents at four cloned P2X receptors. J Neurophysiol 78: 1937–1840, 1997.
  28. Thomas GD, Hansen J, and Victor RG. Inhibition of {alpha}2-adrenergic vasoconstriction during contraction of glycolytic, not oxidative, rat hindlimb muscle. Am J Physiol Heart Circ Physiol 266: H920–H929, 1994.[Abstract/Free Full Text]
  29. Watanabe H, Vriens J, Suh SH, Benham CD, Droogmans G, and Nilius B. Heat-evoked activation of TRPV4 channels in a HEK293 cell expression system and in native mouse aorta endothelial cells. J Biol Chem 277: 47044–47051, 2002.[Abstract/Free Full Text]
  30. Yamamoto R, Takasaki K, and Nickols GA. Purinergic vasoconstrictor component revealed by moderate cooling in the isolated mesenteric vasculature of Sprague-Dawley rats. J Pharmacol Exp Ther 262: 1133–1138, 1992.[Abstract/Free Full Text]
  31. Zhou Z, Price JM, Sutton ET, and Baker CH. Effect of muscle length on the in vitro comparison of femoral arteries before and after endotoxin shock. Am J Physiol Heart Circ Physiol 265: H1160–H1166, 1993.[Abstract/Free Full Text]
  32. Ziganshin AU, Rychkov AV, Ziganshina LE, and Burnstock G. Temperature dependency of P2 receptor-mediated responses. Eur J Pharmacol 456: 107–114, 2002.[CrossRef][ISI][Medline]
  33. Ziganshin AU, Rychkov AV, and Ziganshina LE. Effect of temperature on guinea pig urinary bladder contraction mediated via P2X-receptors. Bull Exp Biol Med 130: 961–963, 2000.[CrossRef][ISI][Medline]



This article has been cited by other articles:


Home page
 J. Appl. Physiol.Home page
Z. Gao, J. D. Li, L. I. Sinoway, and J. Li
Effect of muscle interstitial pH on P2X and TRPV1 receptor-mediated pressor response
J Appl Physiol, June 1, 2007; 102(6): 2288 - 2293.
[Abstract] [Full Text] [PDF]

Home page
 Am. J. Physiol. Heart Circ. Physiol.Home page
D. S. DeLorey, J. J. Hamann, Z. Valic, H. A. Kluess, P. S. Clifford, and J. B. Buckwalter
{alpha}-Adrenergic receptor responsiveness is preserved during prolonged exercise
Am J Physiol Heart Circ Physiol, January 1, 2007; 292(1): H392 - H398.
[Abstract] [Full Text] [PDF]

Home page
 Am. J. Physiol. Heart Circ. Physiol.Home page
Z. Gao, V. Kehoe, J. Xing, L. Sinoway, and J. Li
Temperature modulates P2X receptor-mediated cardiovascular responses to muscle afferent activation
Am J Physiol Heart Circ Physiol, September 1, 2006; 291(3): H1255 - H1261.
[Abstract] [Full Text] [PDF]

Home page
 J. Appl. Physiol.Home page
D. S. DeLorey, J. J. Hamann, H. A. Kluess, P. S. Clifford, and J. B. Buckwalter
{alpha}-Adrenergic receptor-mediated restraint of skeletal muscle blood flow during prolonged exercise
J Appl Physiol, May 1, 2006; 100(5): 1563 - 1568.
[Abstract] [Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF) Free
Right arrow All Versions of this Article:
99/3/995    most recent
00319.2005v1
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via ISI Web of Science (4)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Kluess, H. A.
Right arrow Articles by Clifford, P. S.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Kluess, H. A.
Right arrow Articles by Clifford, P. S.

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
Visit Other APS Journals Online
Copyright © 2005 by the American Physiological Society.