Antagonism of the TRPv1 receptor partially corrects muscle metaboreflex overactivity in spontaneously hypertensive rats

Journal of Physiology

Volumn 589, Issue 24, 2011, Pages 6191-6204

  Mizuno, Masaki ^a   Murphy, Megan N ^a   Mitchell, Jere H ^a   Smith, Scott A ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSAICIN; CAPSAZEPINE; VANILLOID RECEPTOR 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; HYPERTENSION; MALE; MEAN ARTERIAL PRESSURE; MUSCLE CONTRACTION; MUSCLE EXCITATION; MUSCLE ISCHEMIA; MUSCLE METABOREFLEX; MUSCLE REFLEX; NERVOUS SYSTEM FUNCTION; NONHUMAN; PRESSORECEPTOR REFLEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; RENAL SYMPATHETIC NERVE ACTIVITY; SKELETAL MUSCLE; SPINAL GANGLION; SPONTANEOUSLY HYPERTENSIVE RAT; SYMPATHETIC REFLEX; WISTAR KYOTO RAT;

ANIMALS; BAROREFLEX; BLOOD PRESSURE; CAPSAICIN; ELECTRIC STIMULATION; HINDLIMB; HYPERTENSION; ISCHEMIA; KIDNEY; MALE; MUSCLE CONTRACTION; MUSCLE, SKELETAL; RATS; RATS, INBRED SHR; RATS, INBRED WKY; SCIATIC NERVE; SYMPATHETIC NERVOUS SYSTEM; TRPV CATION CHANNELS;

EID: 83455220023     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2011.214429     Document Type: Article

References (55)

1. Aoki K, Sato K, Kondo S, Pyon CB & Yamamoto M (1983). Increased response of blood pressure to rest and handgrip in subjects with essential hypertension. Jpn Circ J 47, 802-809.
2. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD & Julius D (1997). The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389, 816-824.
3. Dang K, Bielefeldt K & Gebhart GF (2005). Differential responses of bladder lumbosacral and thoracolumbar dorsal root ganglion neurons to purinergic agonists, protons, and capsaicin. J Neurosci 25, 3973-3984.
4. Delaney EP, Greaney JL, Edwards DG, Rose WC, Fadel PJ & Farquhar WB (2010). Exaggerated sympathetic and pressor responses to handgrip exercise in older hypertensive humans: Role of the muscle metaboreflex. Am J Physiol Heart Circ Physiol 299, H1318-1327.
5. Dengel D, Hagberg J, Pratley R, Rogus E & Goldberg A (1998). Improvements in blood pressure, glucose metabolism and lipoprotein lipids after aerobic exercise plus weight loss in obese hypertensive middle-aged men. Metabolism 47, 1075-1082.
6. Fox AJ, Urban L, Barnes PJ & Dray A (1995). Effects of capsazepine against capsaicin- and proton-evoked excitation of single airway C-fibres and vagus nerve from the guinea-pig. Neuroscience 67, 741-752.
7. Gao Z, Koba S, Sinoway L & Li J (2008). 20-HETE increases renal sympathetic nerve activity via activation of chemically and mechanically sensitive muscle afferents. J Physiol 586, 2581-2591.
8. Giannesini B, Izquierdo M, Dalmasso C, Le Fur Y, Cozzone PJ, Verleye M, Le Guern ME, Gillardin JM & Bendahan D (2007). Endotoxemia causes a paradoxical intracellular pH recovery in exercising rat skeletal muscle. Muscle Nerve 36, 505-514.
9. Gonzalez-Alonso J, Quistorff B, Krustrup P, Bangsbo J & Saltin B (2000). Heat production in human skeletal muscle at the onset of intense dynamic exercise. J Physiol 524, 603-615.
10. Goodwin GM, McCloskey DI & Mitchell JH (1972). Cardiovascular and respiratory responses to changes in central command during isometric exercise at constant muscle tension. J Physiol 226, 173-190.
11. Habelt C, Kessler F, Distler C, Kress M & Reeh PW (2000). Interactions of inflammatory mediators and low pH not influenced by capsazepine in rat cutaneous nociceptors. Neuroreport 11, 973-976.
12. Hansen AH, Nielsen JJ, Saltin B & Hellsten Y (2010). Exercise training normalizes skeletal muscle vascular endothelial growth factor levels in patients with essential hypertension. J Hypertens 28, 1176-1185.
13. Hayes SG, Kindig AE & Kaufman MP (2007). Blockade of acid sensing ion channels attenuates the exercise pressor reflex in cats. J Physiol 581, 1271-1282.
14. Hoberg E, Schuler G, Kunze B, Obermoser AL, Hauer K, Mautner HP, Schlierf G & Kubler W (1990). Silent myocardial ischemia as a potential link between lack of premonitoring symptoms and increased risk of cardiac arrest during physical stress. Am J Cardiol 65, 583-589.
15. Hoheisel U, Reinohl J, Unger T & Mense S (2004). Acidic pH and capsaicin activate mechanosensitive group IV muscle receptors in the rat. Pain 110, 149-157.
16. Hong S & Wiley JW (2005). Early painful diabetic neuropathy is associated with differential changes in the expression and function of vanilloid receptor 1. J Biol Chem 280, 618-627.
17. Hwang SW, Cho H, Kwak J, Lee SY, Kang CJ, Jung J, Cho S, Min KH, Suh YG, Kim D & Oh U (2000). Direct activation of capsaicin receptors by products of lipoxygenases: endogenous capsaicin-like substances. Proc Natl Acad Sci U S A 97, 6155-6160.
18. Jansco G, Kiraly E & Jansco-Gabor A (1977). Pharmacologically induced selective degeneration of chemosensitive primary sensory neurones. Nature 270, 741-743.
19. Kaufman MP, Iwamoto GA, Longhurst JC & Mitchell JH (1982). Effects of capsaicin and bradykinin on afferent fibers with endings in skeletal muscle. Circ Res 50, 133-139.
20. Kaufman MP, Waldrop TG, Rybicki KJ, Ordway GA & Mitchell JH (1984). Effects of static and rhythmic twitch contractions on the discharge of group III and IV muscle afferents. Cardiovasc Res 18, 663-668.
21. Lanfranchi PA & Somers VK (2002). Arterial baroreflex function and cardiovascular variability: interactions and implications. Am J Physiol Regul Integr Comp Physiol 283, R815-R826.
22. Leal AK, Williams MA, Garry MG, Mitchell JH & Smith SA (2008). Evidence for functional alterations in the skeletal muscle mechanoreflex and metaboreflex in hypertensive rats. Am J Physiol Heart Circ Physiol 295, H1429-H1438.
23. Li J, Sinoway AN, Gau Z, Maile MD, Pu M & Sinoway LI (2004). Muscle mechanoreflex and metaboreflex responses after myocardial infarction in rats. Circulation 110, 3049-3054.
24. Liu M, Willmott NJ, Michael GJ & Priestley JV (2004). Differential pH and capsaicin responses of Griffonia simplicifolia IB4 (IB4)-positive and IB4-negative small sensory neurons. Neuroscience 127, 659-672.
25. Mandadi S, Tominaga T, Numazaki M, Murayama N, Saito N, Armati PJ, Roufogalis BD & Tominaga M (2006). Increased sensitivity of desensitized TRPV1 by PMA occurs through PKCe{open}-mediated phosphorylation at S800. Pain 123, 106-116.
26. McCloskey DI & Mitchell JH (1972). Reflex cardiovascular and respiratory responses originating in exercising muscle. J Physiol 224, 173-186.
27. McCord JL, Tsuchimochi H & Kaufman MP (2009). Acid-sensing ion channels contribute to the metaboreceptor component of the exercise pressor reflex. Am J Physiol Heart Circ Physiol 297, H443-H449.
28. McCord JL, Tsuchimochi H & Kaufman MP (2010). P2X2/3 and P2X3 receptors contribute to the metaboreceptor component of the exercise pressor reflex. J Appl Physiol 109, 1416-1423.
29. Minami N, Yoshikawa T, Kataoka H, Mori N, Nagasaka M, Kurosawa H, Kanazawa M & Kohzuki M (2003). Effects of exercise and beta-blocker on blood pressure and baroreflexes in spontaneously hypertensive rats. Am J Hypertens 16, 966-972.
30. Mitchell JH, Kaufman MP & Iwamoto GA (1983). The exercise pressor reflex: its cardiovascular effects, afferent mechanisms, and central pathways. Annu Rev Physiol 45, 229-242.
31. Mittleman MA, Maclure M, Tofler GH, Sherwood JB, Goldberg RJ & Muller JE (1993). Triggering of acute myocardial infarction by heavy physical exertion. Protection against triggering by regular exertion. Determinants of Myocardial Infarction Onset Study Investigators. N Engl J Med 329, 1677-1683.
32. Mittleman MA & Siscovick DS (1996). Physical exertion as a trigger of myocardial infarction and sudden cardiac death. Cardiol Clin 14, 263-270.
33. Mizuno M, Murphy MN, Mitchell JH & Smith SA (2011). Skeletal muscle reflex-mediated changes in sympathetic nerve activity are abnormal in spontaneously hypertensive rats. Am J Physiol Heart Circ Physiol 300, H968-H977.
34. Moreira ED, Ida F, Oliveira VL & Krieger EM (1992). Early depression of the baroreceptor sensitivity during onset of hypertension. Hypertension 19, II198-II201.
35. Pan HL, Stebbins CL & Longhurst JC (1993). Bradykinin contributes to the exercise pressor reflex: mechanism of action. J Appl Physiol 75, 2061-2068.
36. 1H NMR. Proc Natl Acad Sci U S A 85, 7836-7839.
37. Pickering TG (1987). Pathophysiology of exercise hypertension. Herz 12, 119-124.
38. Potts JT, Shi XR & Raven PB (1993). Carotid baroreflex responsiveness during dynamic exercise in humans. Am J Physiol Heart Circ Physiol 265, H1928-H1938.
39. Remensnyder JP, Mitchell JH & Sarnoff SJ (1962). Functional sympatholysis during muscular activity. Observations on influence of carotid sinus on oxygen uptake. Circ Res 11, 370-380.
40. Rondon MU, Laterza MC, de Matos LD, Trombetta IC, Braga AM, Roveda F, Alves MJ, Krieger EM & Negrao CE (2006). Abnormal muscle metaboreflex control of sympathetic activity in never-treated hypertensive subjects. Am J Hypertens 19, 951-957.
41. Rotto DM, Schultz HD, Longhurst JC & Kaufman MP (1990). Sensitization of group III muscle afferents to static contraction by arachidonic acid. J Appl Physiol 68, 861-867.
42. Sausen MT, Delaney EP, Stillabower ME & Farquhar WB (2009). Enhanced metaboreflex sensitivity in hypertensive humans. Eur J Appl Physiol 105, 351-356.
43. Seguro C, Sau F, Zedda N, Scano G & Cherchi A (1991). Arterial blood pressure behavior during progressive muscular exercise in subjects with stable arterial hypertension. Cardiologia 36, 867-877.
44. Smith SA, Leal AK, Williams MA, Murphy MN, Mitchell JH & Garry MG (2010). The TRPv1 receptor is a mediator of the exercise pressor reflex in rats. J Physiol 588, 1179-1189.
45. Smith SA, Mitchell JH & Garry MG (2001). Electrically induced static exercise elicits a pressor response in the decerebrate rat. J Physiol 537, 961-970.
46. Smith SA, Williams MA, Leal AK, Mitchell JH & Garry MG (2006). Exercise pressor reflex function is altered in spontaneously hypertensive rats. J Physiol 577, 1009-1020.
47. Smith SA, Williams MA, Mitchell JH, Mammen PP & Garry MG (2005). The capsaicin-sensitive afferent neuron in skeletal muscle is abnormal in heart failure. Circulation 111, 2056-2065.
48. Tominaga M, Caterina MJ, Malmberg AB, Rosen TA, Gilbert H, Skinner K, Raumann BE, Basbaum AI & Julius D (1998). The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron 21, 531-543.
49. Tsuchimochi H, McCord JL, Leal AK & Kaufman MP (2011). Dorsal root tetrodotoxin-resistant sodium channels do not contribute to the augmented exercise pressor reflex in rats with chronic femoral artery occlusion. Am J Physiol Heart Circ Physiol 300, H652-663.
50. Ugawa S, Ueda T, Ishida Y, Nishigaki M, Shibata Y & Shimada S (2002). Amiloride-blockable acid-sensing ion channels are leading acid sensors expressed in human nociceptors. J Clin Invest 110, 1185-1190.
51. Vongpatanasin W, Wang Z, Arbique D, Arbique G, Admas-Huet B, Mitchell J, Victor RG & Thomas GD (2011). Functional sympatholysis is impaired in hypertensive humans. J Physiol 589, 1209-1220.
52. Vyklicky L, Knotkova-Urbancova H, Vitaskova Z, Vlachova V, Kress M & Reeh PW (1998). Inflammatory mediators at acidic pH activate capsaicin receptors in cultured sensory neurons from newborn rats. J Neurophysiol 79, 670-676.
53. Wang HJ, Li YL, Gao L, Zucker IH & Wang W (2010). Alteration in skeletal muscle afferents in rats with chronic heart failure. J Physiol 588, 5033-5047.
54. Weiss SA, Blumenthal RS, Sharrett AR, Redberg RF & Mora S (2010). Exercise blood pressure and future cardiovascular death in asymptomatic individuals. Circulation 121, 2109-2116.
55. Williams MA, Smith SA, O'Brien DE, Mitchell JH & Garry MG (2008). The group IV afferent neuron expresses multiple receptor alterations in cardiomyopathyic rats: evidence at the cannabinoid CB1 receptor. J Physiol 586, 835-845.