Role for NGF in augmented sympathetic nerve response to activation of mechanically and metabolically sensitive muscle afferents in rats with femoral artery occlusion

Journal of Applied Physiology

Volumn 113, Issue 8, 2012, Pages 1311-1322

  Lu, Jian ^a   Xing, Jihong ^a   Li, Jianhua ^a  

^a PENN STATE MILTON S HERSHEY MEDICAL CENTER   (United States)

Author keywords

ASIC3; Hindlimb ischemia; Muscle pressor reflex; Nerve growth factor; Peripheral arterial disease

Indexed keywords

ACCN3 PROTEIN, RAT; ACID SENSING ION CHANNEL; LACTIC ACID; NERVE GROWTH FACTOR;

ADRENERGIC SYSTEM; ANIMAL; ANOXIA; ARTERY; ARTICLE; BLOOD PRESSURE; FEMORAL ARTERY; HINDLIMB; INNERVATION; MALE; METABOLISM; MUSCLE CONTRACTION; MYELINATED NERVE; NONMYELINATED NERVE; PATHOPHYSIOLOGY; PHYSIOLOGY; PRESSORECEPTOR; RAT; REFLEX; SENSORY NERVE CELL; SENSORY RECEPTOR; SKELETAL MUSCLE; SPINAL GANGLION; SPRAGUE DAWLEY RAT; TENDON;

ACID SENSING ION CHANNELS; ANIMALS; ANOXIA; ARTERIES; BLOOD PRESSURE; FEMORAL ARTERY; GANGLIA, SPINAL; HINDLIMB; LACTIC ACID; MALE; MUSCLE CONTRACTION; MUSCLE, SKELETAL; NERVE FIBERS, MYELINATED; NERVE FIBERS, UNMYELINATED; NERVE GROWTH FACTOR; NEURONS, AFFERENT; PRESSORECEPTORS; RATS; RATS, SPRAGUE-DAWLEY; REFLEX; SENSORY RECEPTOR CELLS; SYMPATHETIC NERVOUS SYSTEM; TENDONS;

EID: 84867566630     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00617.2012     Document Type: Article

References (63)

1. Baccelli G, Reggiani P, Mattioli A, Corbellini E, Garducci S, Catalano M. The exercise pressor reflex and changes in radial arterial pressure and heart rate during walking in patients with arteriosclerosis obliterans. Angiology 50: 361-374, 1999.
2. Bakke EF, Hisdal J, Jorgensen JJ, Kroese A, Stranden E. Blood pressure in patients with intermittent claudication increases continuously during walking. Eur J Vasc Endovasc Surg 33: 20-25, 2007.
3. Campenot RB, MacInnis BL. Retrograde transport of neurotrophins: fact and function. J Neurobiol 58: 217-229, 2004.
4. Coote JH, Hilton SM, Pérez-González JF. The reflex nature of the pressor response to muscular exercise. J Physiol 215: 789-804, 1971.
5. Critchley JA, Capewell S. Mortality risk reduction associated with smoking cessation in patients with coronary heart disease: a systematic review. JAMA 290: 86-97, 2003.
6. Deval E, Noël J, Gasull X, Delaunay A, Alloui A, Friend V, Eschalier A, Lazdunski M, Lingueglia E. Acid-sensing ion channels in postoperative pain. J Neurosci 31: 6059-6066, 2011.
7. Deval E, Noël J, Lay N, Alloui A, Diochot S, Friend V, Jodar M, Lazdunski M, Lingueglia E. ASIC3, a sensor of acidic and primary inflammatory pain. EMBO J 19: 3047-3055, 2008.
8. Emanueli C, Salis MB, Pinna A, Graiani G, Manni L, Madeddu P. Nerve growth factor promotes angiogenesis and arteriogenesis in ischemic hindlimbs. Circulation 106: 2257-2262, 2002.
9. Fadel PJ, Ogoh S, Watenpaugh DE, Wasmund W, Olivencia-Yurvati A, Smith ML, Raven PB. Carotid baroreflex regulation of sympathetic nerve activity during dynamic exercise in humans. Am J Physiol Heart Circ Physiol 280: H1383-H1390, 2001.
10. Gao Z, Xing J, Sinoway L, Li J. P2X receptor-mediated muscle pressor reflex in myocardial infarction. Am J Physiol Heart Circ Physiol 292: H939-H945, 2007.
11. Giniatullin R, Nistri A, Fabbretti E. Molecular mechanisms of sensitization of pain-transducing P2X3 receptors by the migraine mediators CGRP and NGF. Mol Neurobiol 37: 83-90, 2008.
12. Goodwin GM, McCloskey DI, Mitchell JH. Cardiovascular and respiratory responses to changes in central command during isometric exercise at constant muscle tension. J Physiol 226: 173-190, 1972.
13. Hanna RL, Hayes SG, Kaufman M. ab-Methylene ATP elicits a reflex pressor response arising from muscle in decerebrate cats. J Appl Physiol 93: 834-841, 2002.
14. Hayes SG, Kindig AE, Kaufman MP. Blockade of acid sensing ion channels attenuates the exercise pressor reflex in cats. J Physiol 581: 1271-1282, 2007.
15. Hayes SG, McCord JL, Kaufman MP. Role played by P2X and P2Y receptors in evoking the muscle chemoreflex. J Appl Physiol 104: 538- 541, 2008.
16. Hayes SG, McCord JL, Rainier J, Liu Z, Kaufman MP. Role played by acid-sensitive ion channels in evoking the exercise pressor reflex. Am J Physiol Heart Circ Physiol 295: H1720-H1725, 2008.
17. Hunter DD, Myers AC, Undem BJ. Nerve growth factor-induced phenotypic switch in guinea pig airway sensory neurons. Am J Respir Crit Care Med 161: 1985-1990, 2000.
18. Kaufman MP, Forster HV. Reflexes controlling circulatory, ventilatory and airway responses to exercise. In: Handbook of Physiology. Exercise: Regulation and Integration of Multiple Systems, edited by Rowell LB, Shepherd JT. New York: Oxford University Press, 1996, sect. 12, chapt. 10, p. 381-447.
19. Kaufman MP, Longhurst JC, Rybicki KJ, Wallach JH, Mitchell JH. Effects of static muscular contraction on impulse activity of groups III and IV afferents in cats. J Appl Physiol 55: 105-112, 1983.
20. Kaufman MP, Waldrop TG, Rybicki KJ, Ordway GA, Mitchell JH. Effects of static and rhythmic twitch contractions on the discharge of group III and IV muscle afferents. Cardiovasc Res 18: 663-668, 1984.
21. Li J, Maile MD, Sinoway AN, Sinoway LI. Muscle pressor reflex: potential role of vanilloid type 1 receptor and acid-sensing ion channel. J Appl Physiol 97: 1709-1714, 2004.
22. Li J, Sinoway AN, Gao Z, Maile MD, Pu M, Sinoway LI. Muscle mechanoreflex and metaboreflex responses after myocardial infarction in rats. Circulation 110: 3049-3054, 2004.
23. Li J, Sinoway LI. ATP stimulates chemically sensitive and sensitizes mechanically sensitive afferents. Am J Physiol Heart Circ Physiol 283: H2636-H2643, 2002.
24. Light AR, Hughen RW, Zhang J, Rainier J, Liu Z, Lee J. Dorsal root ganglion neurons innervating skeletal muscle respond to physiological combinations of protons, ATP, and lactate mediated by ASIC, P2X, and TROVE. J Neurophysiol 100: 1184-1201, 2008.
25. Liu J, Gao Z, Li J. Femoral artery occlusion increases expression of ASIC3 in dorsal root ganglion neurons. Am J Physiol Heart Circ Physiol 299: H1357-H1364, 2010.
26. Liu J, Li J, Lu J, Xing J, Li J. Contribution of nerve growth factor to upregulation of P2X3 expression in DRG neurons of rats with femoral artery occlusion. Am J Physiol Heart Circ Physiol 301: H1070-H1079, 2011.
27. Liu J, Mao W, Ding B, Liang CS. ERKs/p53 signal transduction pathway is involved in doxorubicin-induced apoptosis in H9c2 cells and cardiomytes. Am J Physiol Heart Circ Physiol 295: H1956-H1965, 2008.
28. +, lactate and phosphate determined with MSNA during exercise in humans. Am J Physiol Regul Integr Comp Physiol 278: R563-R571, 2000.
29. MacLean DA, LaNoue KF, Gray KS, Sinoway LI. Effects of hindlimb contraction on pressor and muscle interstitial metabolite responses in the cat. J Appl Physiol 85: 1583-1592, 1998.
30. Mamet J, Baron A, Lazdunski M, Voilley N. Proinflammatory mediators, stimulators of sensory neuron excitability via the expression of acid-sensing ion channels. J Neurosci 22: 10662-10670, 2002.
31. Mamet J, Lazdunski M, Voilley N. How nerve growth factor drives physiological and inflammatory expressions of acid-sensing ion channel 3 in sensory neurons. J Biol Chem 278: 48907-48913, 2003.
32. McCloskey DI, Mitchell JH. Reflex cardiovascular and respiratory responses originating in exercising muscle. J Physiol 224: 173-186, 1972.
33. McCord JL, Hayes SG, Kaufman MP. Acid-sensing ion and epithelial sodium channels do not contribute to the mechanoreceptor component of the exercise pressor reflex. Am J Physiol Heart Circ Physiol 295: H1017- H1024, 2008.
34. McCord JL, Tsuchimochi H, Kaufman MP. Acid-sensing ion channels contribute to the metaboreceptor component of the exercise pressor reflex. Am J Physiol Heart Circ Physiol 297: H443-H449, 2009.
35. Mitchell JH, Kaufman MP, Iwamoto GA. The exercise pressor reflex: Its cardiovascular effects, afferent mechanism, and central pathways. Annu Rev Physiol 45: 229-242, 1983.
36. Mitchell JH, Reardon WC, McCloskey DI. Reflex effects on circulation and respiration from contracting skeletal muscle. Am J Physiol Heart Circ Physiol 233: H374-H378, 1977.
37. Muir RL. Peripheral arterial disease: Pathophysiology, risk factors, diagnosis, treatment, and prevention. J Vasc Nurs 27: 26-30, 2009.
38. Ouriel K. Peripheral arterial disease. Lancet 358: 1257-1264, 2001.
39. Pan HL, Stebbins CL, Longhurst JC. Bradykinin contributes to the exercise pressor reflex: mechanism of action. J Appl Physiol 75: 2061- 2068, 1993.
40. Pezet S, McMahon SB. Neurotrophins: mediators and modulators of pain. Annu Rev Neurosci 29: 507-538, 2006.
41. Potts JT, Li J. Interaction between carotid baroreflex and exercise pressor reflex depends on baroreceptor afferent input. Am J Physiol Heart Circ Physiol 274: H1841-H1847, 1998.
42. Ramer MS, Bradbury EJ, McMahon SB. Nerve growth factor induces P2X(3) expression in sensory neurons. J Neurochem 77: 864-875, 2001.
43. Rejeski WJ, Tian L, Liao Y, McDermott MM. Social cognitive constructs and the promotion of physical activity in patients with peripheral artery disease. J Cardiopulm Rehabil Prev 28: 65-72, 2008.
44. Rotto DM, Kaufman MP. Effect of metabolic products of muscular contraction on discharge of group III and IV afferents. J Appl Physiol 64: 2306-2313, 1988.
45. Rotto DM, Stebbins CL, Kaufman MP. Reflex cardiovascular and ventilatory responses to increasing H+ activity in cat hindlimb muscle. J Appl Physiol 67: 256-263, 1989.
46. Sinoway L, Prophet S, Gorman I, Mosher T, Shenberger J, Dolecki M, Briggs R, Zelis R. Muscle acidosis during static exercise is associated with calf vasoconstriction. J Appl Physiol 66: 429-436, 1989.
47. Sinoway LI, Li J. A perspective on the muscle reflex: implications for congestive heart failure. J Appl Physiol 99: 5-22, 2005.
48. Skoff AM, Adler JE. Nerve growth factor regulates substance P in adult sensory neurons through both TrkA and p75 receptors. Exp Neurol 197: 430-436, 2006.
49. Smith SA, Mitchell JH, Garry MG. The mammalian exercise pressor reflex in health and disease. Exp Physiol 91: 89-102, 2006.
50. Sugiura A, Ohtori S, Yamashita M, Inoue G, Yamauchi K, Koshi T, Suzuki M, Norimoto M, Orita S, Eguchi Y, Takahashi Y, Watanabe TS, Ochiai N, Takaso M, Takahashi K. Existence of nerve growth factor receptors, tyrosine kinase a and p75 neurotrophin receptors in intervertebral discs and on dorsal root ganglion neurons innervating intervertebral discs in rats. Spine (Phila Pa 1976) 33: 2047-2051, 2008.
51. Tsuchimochi H, McCord JL, Hayes SG, Koba S, Kaufman MP. Chronic femoral artery occlusion augments exercise pressor reflex in decerebrated rats. Am J Physiol Heart Circ Physiol 299: H106-H113, 2010.
52. Tsuchimochi H, Yamauchi K, McCord JL, Kaufman MP. Blockade of acid sensing ion channels attenuates the augmented exercise pressor reflex in rats with chronic femoral artery occlusion. J Physiol 589: 6173-6189, 2011.
53. Victor RG, Bertocci L, Pryor S, Nunnally R. Sympathetic nerve discharge is coupled to muscle cell pH during exercise in humans. J Clin Invest 82: 1301-1305, 1988.
54. Waldmann R, Bassilana F, de Weille J, Champigny G, Heurteaux C, Lazdunski M. Molecular cloning of a non-inactivating proton-gated Na+ channel specific for sensory neurons. J Biol Chem 272: 20975-20978, 1997.
55. Waldmann R, Champigny G, Bassilana F, Heurteaux C, Lazdunski M. A proton-gated cation channel involved in acid-sensing. Nature 386: 173-177, 1997.
56. Waldmann R, Champigny G, Lingueglia E, De Weille JR, Heurteaux C, Lazdunski M. H(+)-gated cation channels. Ann NY Acad Sci 868: 67-76, 1999.
57. Waldrop TG, Eldridge FL, Iwamoto GA, Mitchell JH. Central neural control of respiration and circulation during exercise. In: Handbook of Physiology. Exercise: Regulation and Integration of Multiple Systems, edited by Rowell LB, Shepherd JT. New York: Oxford University Press, 1996, sect. 12, chapt. 9, p. 333-380.
58. Waters RE, Terjung RL, Peters KG, Annex BH. Preclinical models of human peripheral arterial occlusive disease: implications for investigation of therapeutic agents. J Appl Physiol 97: 773-780, 2004.
59. Wu C, Erickson MA, Xu J, Wild KD, Brennan TJ. Expression profile of nerve growth factor after muscle incision in the rat. Anesthesiology 110: 140-149, 2009.
60. Xing J, Gao Z, Lu J, Sinoway LI, Li J. Femoral artery occlusion augments TROVE-mediated sympathetic responsiveness. Am J Physiol Heart Circ Physiol 295: H1262-H1269, 2008.
61. Xing J, Lu J, Li J. ASIC3 function and immunolabeling increases in skeletal muscle sensory neurons following femoral artery occlusion. J Physiol 590: 1261-1272, 2012.
62. Xing J, Lu J, Li J. Contribution of nerve growth factor to augmented TROVE responses of muscle sensory neurons by femoral artery occlusion. Am J Physiol Heart Circ Physiol 296: H1380-H1387, 2009.
63. Yagi J, Wenk HN, Naves LA, McCleskey EW. Sustained currents through ASIC3 ion channels at the modest pH changes that occur during myocardial ischemia. Circ Res 99: 501-509, 2006.