Peripheral δ-opioid receptors attenuate the exercise pressor reflex

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 305, Issue 8, 2013, Pages

  Leal, Anna K ^a   Yamauchi, Katsuya ^a   Kim, Joyce ^a   Ruiz Velasco, Victor ^a   Kaufman, Marc P ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

Decerebrate rats; Neural control of the circulation; Peripheral artery disease; Thin fiber muscle afferents

Indexed keywords

CAPSAICIN; DELTA OPIATE RECEPTOR; ENKEPHALIN[2,5 DEXTRO PENICILLAMINE]; NARCOTIC ANALGESIC AGENT;

ANIMAL EXPERIMENT; ARTERY LIGATION; ARTICLE; CONTROLLED STUDY; EXERCISE; FEMORAL ARTERY; HINDLIMB; INNERVATION; MALE; MUSCLE CONTRACTION; NONHUMAN; PRESSOR RESPONSE; PRESSORECEPTOR REFLEX; PRIORITY JOURNAL; RAT; SPINAL GANGLION; WESTERN BLOTTING; AGONISTS; ANIMAL; BLOOD PRESSURE; DRUG EFFECTS; HEART RATE; HEMODYNAMICS; LIGATION; MECHANORECEPTOR; PHYSIOLOGY; REFLEX; SKELETAL MUSCLE; SPRAGUE DAWLEY RAT; SURGERY;

ANALGESICS, OPIOID; ANIMALS; BLOOD PRESSURE; ENKEPHALIN, D-PENICILLAMINE (2,5)-; FEMORAL ARTERY; HEART RATE; HEMODYNAMICS; LIGATION; MALE; MECHANORECEPTORS; MUSCLE, SKELETAL; PHYSICAL CONDITIONING, ANIMAL; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, OPIOID, DELTA; REFLEX;

EID: 84885663773     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00116.2013     Document Type: Article

References (52)

1. Alain M, Smirk FH. Observation in man upon a blood pressure raising reflex arising from the voluntary muscles. J Physiol 89: 372-383, 1937.
2. Amann M, Blain GM, Proctor LT, Sebranek JJ, Pegelow DF, Demp-sey JA. Group III and IV muscle afferents contribute to ventilatory and cardiovascular response to rhythmic exercise in humans. J Appl Physiol 109: 966-976, 2010.
3. Amann M, Runnels S, Morgan DE, Trinity JD, Fjeldstad AS, Wray DW, Reese VR, Richardson RS. On the contribution of group III and IV muscle afferents to the circulatory response to rhythmic exercise in humans. J Physiol 589: 3855-3866, 2011.
4. Beaudry H, Dubois D, Gendron L. Activation of spinal muand delta-opioid receptors potently inhibits substance P release induced by peripheral noxious stimuli. J Neurosci 31: 13068-13077, 2011.
5. Cahill CM, McClellan KA, Morinville A, Hoffert C, Hubatsch D, O'Donnell D, Beaudet A. Immunohistochemical distribution of delta opioid receptors in the rat central nervous system: evidence for somato-dendritic labeling and antigen-specific cellular compartmentalization. J Comp Neurol 440: 65-84, 2001.
6. Cahill CM, Morinville A, Hoffert C, O'Donnell D, Beaudet A. Up-regulation and trafficking of delta opioid receptor in a model of chronic inflammation: implications for pain control. Pain 101: 199-208, 2003.
7. Cahill CM, Morinville A, Lee MC, Vincent JP, Collier B, Beaudet A. Prolonged morphine treatment targets delta opioid receptors to neuronal plasma membranes and enhances delta-mediated antinociception. J Neurosci 21: 7598-7607, 2001.
8. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389: 816-824, 1997.
9. Coote JH, Hilton SM, Perez-Gonzalez JF. The reflex nature of the pressor response to muscular exercise. J Physiol 215: 789-804, 1971.
10. Craig AD. Distribution of brainstem projections from spinal lamina I neurons in the cat and the monkey. J Comp Neurol 361: 225-248, 1995.
11. Craig AD, Heppelmann B, Schaible HG. The projection of the medial and posterior articular nerves of the cat's knee to the spinal cord. J Comp Neurol 276: 279-288, 1988.
12. Craig AD, Mense S. The distribution of afferent fibers from the gastroc-nemius-soleus muscle in the dorsal horn of the cat as revealed by the transport of horseradish peroxidase. Neurosci Lett 41: 233-238, 1983.
13. Gendron L, Pintar JE, Chavkin C. Essential role of mu opioid receptor in the regulation of delta opioid receptor-mediated antihyperalgesia. Neu-roscience 150: 807-817, 2007.
14. Gomes I, Gupta A, Filipovska J, Szeto HH, Pintar JE, Devi LA. A role for heterodimerization of mu and delta opiate receptors in enhancing morphine analgesia. Proc Natl Acad Sci USA 101: 5135-5139, 2004.
15. Hayes SG, Kindig AE, Kaufman MP. Comparison between the effect of static contraction and tendon stretch on the discharge of group III and IV muscle afferents. J Appl Physiol 99: 1891-1896, 2005.
16. Hill JM, Kaufman MP. Attenuation of reflex pressor and ventilatory responses to static muscular contraction by intrathecal opioids. J Appl Physiol 68: 2466-2472, 1990.
17. Immke DC, McCleskey EW. Lactate enhances the acid-sensing Na+ channel on ischemia-sensing neurons. Nat Neurosci 4: 869-870, 2001.
18. Iwamoto GA, Parnaveles JG, Kaufman MP, Botterman BR, Mitchell JH. Activation of caudal brainstem cell groups during the exercise pressor reflex as elucidated by 2-[14C]deoxyglucose. Brain Res 304: 178-182, 1984.
19. Iwamoto GA, Waldrop TG, Bauer RM, Mitchell JH. Pressor responses to muscular contraction in the cat: contributions by caudal and rostral ventrolateral medulla. Prog Brain Res 81: 253-263, 1989.
20. Iwamoto GA, Waldrop TG, Kaufman MP, Botterman BR, Rybicki KJ, Mitchell JH. Pressor reflex evoked by muscular contraction: contributions by neuraxis levels. J Appl Physiol 59: 459-467, 1985.
21. Kaufman MP, Forster HV. Reflexes controlling circulatory, ventilatory and airway responses to exercise. In: Handbook of Physiology. Exercise: Regulation and Integration of Multiple Systems. II. Control of Respiratory and Cardiovascular Systems. Bethesda, MD: Am. Physiol. Soc., 1996, sect. 12, p. 381-447.
22. Kaufman MP, Iwamoto GA, Longhurst JC, Mitchell JH. Effects of capsaicin and bradykinin on afferent fibers with endings in skeletal muscle. Circ Res 50: 133-139, 1982.
23. 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.
24. Kaufman MP, Rybicki KJ, Waldrop TG, Ordway GA. Effect of ischemia on responses of group III and IV afferents to contraction. J Appl Physiol 57: 644-650, 1984.
25. Law PY, Erickson-Herbrandson LJ, Zha QQ, Solberg J, Chu J, Sarre A, Loh HH. Heterodimerization of muand delta-opioid receptors occurs at the cell surface only and requires receptor-G protein interactions. J Biol Chem 280: 11152-11164, 2005.
26. Machelska H, Stein C. Leukocyte-derived opioid peptides and inhibition of pain. J Neuroimmune Pharmacol 1: 90-97, 2006.
27. McCloskey DI, Mitchell JH. Reflex cardiovascular and respiratory responses originating in exercising muscle. J Physiol 224: 173-186, 1972.
28. Mennicken F, Zhang J, Hoffert C, Ahmad S, Beaudet A, O'Donnell D. Phylogenetic changes in the expression of delta opioid receptors in spinal cord and dorsal root ganglia. J Comp Neurol 465: 349-360, 2003.
29. Minami M, Maekawa K, Yabuuchi K, Satoh M. Double in situ hybridization study on coexistence of mudeltaand kappa-opioid receptor mRNAs with preprotachykinin A mRNA in the rat dorsal root ganglia. Brain Res Mol Brain Res 30: 203-210, 1995.
30. Mitchell JH, Kaufman MP, Iwamoto GA. The exercise pressor reflex: Its cardiovascular effects, afferent mechanisms, and central pathways. Ann Rev Physiol 45: 229-242, 1983.
31. Morinville A, Cahill CM, Aibak H, Rymar VV, Pradhan A, Hoffert C, Mennicken F, Stroh T, Sadikot AF, O'Donnell D, Clarke PB, Collier B, Henry JL, Vincent JP, Beaudet A. Morphine-induced changes in delta opioid receptor trafficking are linked to somatosensory processing in the rat spinal cord. J Neurosci 24: 5549-5559, 2004.
32. Morinville A, Cahill CM, Esdaile MJ, Aibak H, Collier B, Kieffer BL, Beaudet A. Regulation of delta-opioid receptor trafficking via mu-opioid receptor stimulation: evidence from mu-opioid receptor knock-out mice. J Neurosci 23: 4888-4898, 2003.
33. Morinville A, Cahill CM, Kieffer B, Collier B, Beaudet A. Mu-opioid receptor knockout prevents changes in delta-opioid receptor trafficking induced by chronic inflammatory pain. Pain 109: 266-273, 2004.
34. Mosberg HI, Hurst R, Hruby VJ, Gee K, Yamamura HI, Galligan JJ, Burks TF. Bis-penicillamine enkephalins possess highly improved specificity toward delta opioid receptors. Proc Natl Acad Sci USA 80: 5871-5874, 1983.
35. O'Leary DS, Augustyniak RA, Ansorge EJ, Collins HL. Muscle metaboreflex improves O2 delivery to ischemic active skeletal muscle. Am J Physiol Heart Circ Physiol 276: H1399-H1403, 1999.
36. Portoghese PS, Sultana M, Takemori AE. Naltrindole, a highly selective and potent non-peptide delta opioid receptor antagonist. Eur J Pharmacol 146: 185-186, 1988.
37. Prior BM, Lloyd PG, Ren J, Li H, Yang HT, Laughlin MH, Terjung RL. Time course of changes in collateral blood flow and isolated vessel size and gene expression after femoral artery occlusion in rats. Am J Physiol Heart Circ Physiol 287: H2434-H2447, 2004.
38. Puehler W, Zollner C, Brack A, Shaqura MA, Krause H, Schafer M, Stein C. Rapid upregulation of mu opioid receptor mRNA in dorsal root ganglia in response to peripheral inflammation depends on neuronal conduction. Neuroscience 129: 473-479, 2004.
39. Rotto DM, Kaufman MP. Effects of metabolic products of muscular contraction on the discharge of group III and IV afferents. J Appl Physiol 64: 2306-2313, 1988.
40. Scherrer G, Imamachi N, Cao YQ, Contet C, Mennicken F, O'Donnell D, Kieffer BL, Basbaum AI. Dissociation of the opioid receptor mechanisms that control mechanical and heat pain. Cell 137: 1148-1159, 2009.
41. Sinoway LI, Hill JM, Pickar JG, Kaufman MP. Effects of contraction and lactic acid on the discharge of group III muscle afferents in cats. J Neurophysiol 69: 1053-1059, 1993.
42. Smith SA, Mitchell GS, Garry MG. Electrically induced static exercise elicits a pressor response in the decerebrate rat. J Physiol 537: 961-970, 2001.
43. Stebbins CL, Brown B, Levin D, Longhurst JC. Reflex effect of skeletal muscle mechanoreceptor stimulation on the cardiovascular system. J Appl Physiol 65: 1539-1547, 1988.
44. 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.
45. Tsuchimochi H, McCord JL, Kaufman MP. Peripheral mu-opioid receptors attenuate the augmented exercise pressor reflex in rats with chronic femoral artery occlusion. Am J Physiol Heart Circ Physiol 299: H557-H565, 2010.
46. van Rijn RM, Whistler JL, Waldhoer M. Opioid-receptor-heteromer-specific trafficking and pharmacology. Curr Opin Pharmacol 10: 73-79, 2010.
47. Wang HB, Zhao B, Zhong YQ, Li KC, Li ZY, Wang Q, Lu YJ, Zhang ZN, He SQ, Zheng HC, Wu SX, Hokfelt TG, Bao L, Zhang X. Coexpression of deltaand mu-opioid receptors in nociceptive sensory neurons. Proc Natl Acad Sci USA 107: 13117-13122, 2010.
48. Weng X, Smith T, Sathish J, Djouhri L. Chronic inflammatory pain is associated with increased excitability and hyperpolarization-activated current (Ih) in Cbut not Adelta-nociceptors. Pain 153: 900-914, 2012.
49. Wilson LB, Andrew D, Craig AD. Activation of spinobulbar lamina I neuron by static contraction. J Neurophysiol 87: 1641-1645, 2002.
50. Wilson LB, Wall PT, Pawelczyk JA, Matsukawa K. Cardiorespiratory and phrenic nerve responses to graded muscle stretch in anesthetized cats. Respir Physiol 98: 251-266, 1994.
51. Xing J, Lu J, Li J. Acid-sensing ion channel subtype 3 function and immunolabelling increases in skeletal muscle sensory neurons following femoral artery occlusion. J Physiol 590: 1261-1272, 2012.
52. Yang HT, Feng Y, Allen LA, Protter A, Terjung RL. Efficacy and specificity of bFGF increased collateral flow in experimental peripheral arterial insufficiency. Am J Physiol Heart Circ Physiol 278: H1966-H1973, 2000.