The therapeutic potential of renin angiotensin aldosterone system (RAAS) in chronic pain: from preclinical studies to clinical trials

References

• Brennan F, Carr DB, Cousins M. Pain management: a fundamental human right. Anesth Analg. 2007;105:205–221.
   PubMed Web of Science ®Google Scholar
• Dworkin RH, O’Connor AB, Audette J, et al. Recommendations for the pharmacological management of neuropathic pain: an overview and literature update. Mayo Clin Proc. 2010;85:3–14.
   PubMed Web of Science ®Google Scholar
• Tigerstedt R, Bergmann PG. Niere und Kreislauf. Skand Arch Physiol. 1898;8:223–271.
   Google Scholar
• Chakrabarty A, Blacklock A, Svojanovsky S, et al. Estrogen elicits dorsal root ganglion axon sprouting via a renin-angiotensin system. Endocrinology. 2008;149:3452–3460.
   PubMed Web of Science ®Google Scholar
• Kukkar A, Singh N, Jaggi AS. Neuropathic pain-attenuating potential of aliskiren in chronic constriction injury model in rats. J Renin Angiotensin Aldosterone Syst. 2012;14:116–123.
   PubMed Web of Science ®Google Scholar
• Rohit C, Rao US, Gopala Krishna HN. Effects of captopril and losartan on thermal and chemical induced pain in mice. Indian J Physiol Pharmacol. 2006;50:169–174.
   PubMedGoogle Scholar
• Patil J, Schwab A, Nussberger J, et al. Intraneuronal angiotensinergic system in rat and human dorsal root ganglia. Regul Pept. 2010;162:90–98.
   PubMedGoogle Scholar
• Pavel J, Tang H, Brimijoin S, et al. Expression and transport of angiotensin II AT1 receptors in spinal cord, dorsal root ganglia and sciatic nerve of the rat. Brain Res. 2008;1246:111–122.
   PubMed Web of Science ®Google Scholar
• De Gasparo M, Catt KJ, Inagami T, et al. International Union of Pharmacology. XXIII. Angiotensin II Receptors Pharmacol Rev. 2000;52:415–472.
   PubMed Web of Science ®Google Scholar
• Yu L, Shao C, Gao L. Developmental expression patterns for angiotensin receptors in mouse skin and brain. J Renin Angiotensin Aldosterone Syst. 2014;15:139–149.
   PubMed Web of Science ®Google Scholar
• Nemoto W, Nakagawasai O, Yaoita F, et al. Angiotensin II produces nociceptive behavior through spinal AT1 receptor-mediated p38 mitogen-activated protein kinase activation in mice. Mol Pain. 2013;9:38.
   PubMed Web of Science ®Google Scholar
• Jaggi AS, Singh N. Exploring the potential of telmisartan in chronic constriction injury-induced neuropathic pain in rats. Eur J Pharmacol. 2011;667:215–221.
   PubMed Web of Science ®Google Scholar
• Bottari SP, Taylor V, King IN, et al. Angiotensin II AT2 receptors do not interact with guanine nucleotide binding proteins. Eur J Pharmacol. 1991;207:157–163.
   PubMed Web of Science ®Google Scholar
• Kambayashi Y, Bardhan S, Takahashi K, et al. Molecular cloning of a novel angiotensin II receptor isoform involved in phosphotyrosine phosphatase inhibition. J Biol Chem. 1993;268:24543–24546.
   PubMed Web of Science ®Google Scholar
• Mukoyama M, Kakajima M, Horiuchi M, et al. Expression cloning of type angiotensin II receptor reveals a unique class of seven transmembrane receptors. J Biol Chem. 1993;268:24539–24542.
   PubMed Web of Science ®Google Scholar
• Plouffe B, Guimond MO, Beaudry H, et al. Role of tyrosine kinase receptors in angiotensin II AT2 receptor signaling: involvement in neurite outgrowth and in p42/p44mapk activation in NG108-15 cells. Endocrinology. 2006;147:4646–4654.
   PubMed Web of Science ®Google Scholar
• Beaudry H, Gendron L, Guimond M-O, et al. Involvement of protein kinase C alpha (PKC alpha) in the early action of angiotensin II type 2 (AT2) effects on neurite outgrowth in NG108-15 cells: AT2-receptor inhibits PKC alpha and p21ras activity. Endocrinology. 2006;147:4263–4272.
   PubMed Web of Science ®Google Scholar
• Anand U, Yiangou Y, Sinisi M, et al. Mechanisms underlying clinical efficacy of angiotensin II type 2 receptor (AT2R) antagonist EMA401 in neuropathic pain: clinical tissue and in vitro studies. Mol Pain. 2015;11:38.
   PubMed Web of Science ®Google Scholar
• Danser AH, Anand P. The angiotensin II type 2 receptor for pain control. Cell. 2014;157:1504–1506.
   PubMed Web of Science ®Google Scholar
• Marion E, Song OR, Christophe T, et al. Mycobacterial toxin induces analgesia in buruli ulcer by targeting the angiotensin pathways. Cell. 2014;157:1565–1576.
   PubMed Web of Science ®Google Scholar
• Guenin-Macé L, Baron L, Chany AC, et al. Shaping mycolactone for therapeutic use against inflammatory disorders. Sci Trans Med. 2015;7:289ra85.
   PubMed Web of Science ®Google Scholar
• Jackson TR, Blair LA, Marshall J, et al. The mas oncogene encodes an angiotensin receptor. Nature. 1988;335:437–440.
   PubMed Web of Science ®Google Scholar
• Costa ACO, Becker LK, Moraes ER, et al. Angiotensin-(1-7) induces peripheral antinociception through mas receptor activation in an opioid-independent pathway. Pharmacology. 2012;89:137–144.
   PubMed Web of Science ®Google Scholar
• Chen T, Cai Q, Hong Y. Intrathecal sensory neuron-specific receptor agonists bovine adrenal medulla 8-22 and (Tyr6)-gamma2-MSH-6-12 inhibit formalin-evoked nociception and neuronal Fos-like immunoreactivity in the spinal cord of the rat. Neuroscience. 2006;141:965–975.
   PubMed Web of Science ®Google Scholar
• Guan Y, Liu Q, Tang Z, et al. Mas-related G-protein-coupled receptors inhibit pathological pain in mice. Proc Natl Acad Sci U S A. 2010;107:15933–15938.
   PubMed Web of Science ®Google Scholar
• Gallinat S, Yu M, Dorst A, et al. Sciatic nerve transection evokes lasting up-regulation of angiotensin AT2 and AT1 receptor mRNA in adult rat dorsal root ganglia and sciatic nerves. Brain Res Mol Brain Res. 1998;57:111–122.
   PubMedGoogle Scholar
• Zhao Y, Qin Y, Liu T, et al. Chronic nerve injury-induced Mas receptor expression in dorsal root ganglion neurons alleviates neuropathic pain. Exp Ther Med. 2015;10:2384–2388.
   PubMed Web of Science ®Google Scholar
• Li J, Culman J, Hörtnagl H, et al. Angiotensin AT2 receptor protects against cerebral ischemia-induced neuronal injury. FASEB J. 2005;19:617–619.
   PubMed Web of Science ®Google Scholar
• Dong F, Xie W, Strong JA, et al. Mineralocorticoid receptor blocker eplerenone reduces pain behaviors in vivo and decreases excitability in small-diameter sensory neurons from local inflamed dorsal root ganglia in vitro. Anesthesiology. 2012;117:1102–1112.
   PubMed Web of Science ®Google Scholar
• Sønder SU, Mikkelsen M, Rieneck K, et al. Effects of spironolactone on human blood mononuclear cells: mineralocorticoid receptor independent effects on gene expression and late apoptosis induction. Br J Pharmacol. 2006;148:46–53.
   PubMed Web of Science ®Google Scholar
• Jaggi AS, Singh N. Differential effect of spironolactone in chronic constriction injury and vincristine-induced neuropathic pain in rats. Eur J Pharmacol. 2010;648:102–109.
   PubMed Web of Science ®Google Scholar
• Leung L, Cahill CM. TNF-α and neuropathic pain - a review. J Neuroinflammation. 2010;7–27.
   PubMedGoogle Scholar
• Sacerdote P, Franchi S, Trovato AE, et al. Transient early expression of TNF-alpha in sciatic nerve and dorsal root ganglia in a mouse model of painful peripheral neuropathy. Neurosci Lett. 2008;436:210–213.
   PubMed Web of Science ®Google Scholar
• Fujiyoshi T, Hayashi T, Ohishi S, et al. Kaolin-induced writhing in mice, a new model of possible bradykinin induced assessment of analgesic agents. Agents Actions. 1989;27:332–334.
   PubMedGoogle Scholar
• Takai S, Song K, Tanaka T, et al. Antinociceptive effects of angiotensin-converting enzyme inhibitors and an angiotensin II receptor antagonist in mice. Life Sci. 1996;59:331–336.
   PubMedGoogle Scholar
• Araiza-Saldaña CI, Pedraza-Priego EF, Torres-López JE, et al. Fosinopril prevents the development of tactile allodynia in a streptozotocin-induced diabetic rat model. Drug Dev Res. 2015;76:442–449.
   PubMed Web of Science ®Google Scholar
• Pavel J, Oroszova Z, Hricova L, et al. Effect of subpressor dose of angiotensin II on pain-related behavior in relation with neuronal injury and activation of satellite glial cells in the rat dorsal root ganglia. Cell Mol Neurobiol. 2013;33:681–688.
   PubMed Web of Science ®Google Scholar
• Takata H, Takeda Y, Zhu A, et al. Protective effects of mineralocorticoid receptor blockade against neuropathy in experimental diabetic rats. Diabetes Obes Metab. 2012;14:155–162.
   PubMed Web of Science ®Google Scholar
• Muralidharan A, Wyse BD, Smith MT. Analgesic efficacy and mode of action of a selective small molecule angiotensin II type 2 receptor antagonist in a rat model of prostate cancer-induced bone pain. Pain Med. 2014;15:93–110.
   PubMed Web of Science ®Google Scholar
• Smith MT, Wyse BD, Edwards SR. Small molecule angiotensin II type 2 receptor (AT₂R) antagonists as novel analgesics for neuropathic pain: comparative pharmacokinetics, radioligand binding, and efficacy in rats. Pain Med. 2013;14:692–705.
   PubMed Web of Science ®Google Scholar
• Smith MT, Woodruff TM, Wyse BD, et al. A small molecule angiotensin II type 2 receptor (AT 2 R) antagonist produces analgesia in a rat model of neuropathic pain by inhibition of p38 mitogen-activated protein kinase (MAPK) and p44/p42 MAPK activation in the dorsal root ganglia. Pain Med. 2014;14:1557–1568.
   Web of Science ®Google Scholar
• Chakrabarty A, Liao Z, Smith PG. Angiotensin II receptor type 2 activation is required for cutaneous sensory hyperinnervation and hypersensitivity in a rat hind paw model of inflammatory pain. J Pain. 2013;14:1053–1065.
   PubMed Web of Science ®Google Scholar
• Khan N, Bakshi KS, Jaggi AS, et al. Ameliorative potential of spironolactone in diabetes induced hyperalgesia in mice. Yakugaku Zasshi. 2009;129:593–599.
   PubMed Web of Science ®Google Scholar
• Abdel-salam OME, Baiuomy AR, Nada SA. Effect of spironolactone on pain responses in mice. Issn. 2010;9:46–57.
   Google Scholar
• Chau TT, Lewin AC, Walter TL, et al. Evidence for a role of bradykinin in experimental pain models. Agents Actions. 1991;34:235–238.
   PubMedGoogle Scholar
• Zamir N, Simantov R, Segal M. Pain sensitivity and opioid activity in genetically and experimentally hypertensive rats. Brain Res. 1980;184:299–310.
   PubMed Web of Science ®Google Scholar
• Thurston CL, Randich A. Acute increases in arterial blood pressure produced by occlusion of the abdominal aorta induces antinociception: peripheral and central substrates. Brain Res. 1990;519:12–22.
   PubMed Web of Science ®Google Scholar
• Sitsen J, de Jong W. Observations on pain perception and hypertension in spontaneously hypertensive rats. Clin Exp Hypertens A. 1984;6:1345–1356.
   PubMed Web of Science ®Google Scholar
• Barres C, Vincent M, Sassard J. Pain sensitivity and blood pressure in genetically hypertensive rats of the Lyon strain. J Hypertens. 1983;1:225–227.
   Google Scholar
• Irvine RJ, White JM, Head RJ. The renin angiotensin system and nociception in spontaneously hypertensive rats. Life Sci. 1995;56:1073–1078.
   PubMed Web of Science ®Google Scholar
• Wang JF, Sun XJ, Yang HF, et al. Mobilization of calcium from intracellular store as a possible mechanism underlying the anti-opioid effect of angiotensin II. Neuropeptides. 1992;22:219–222.
   PubMed Web of Science ®Google Scholar
• Kaneko S, Mori A, Tamura S, et al. Intracerebroventricular administration of angiotensin II attenuates morphine-induced analgesia in mice. Neuropharmacology. 1985;24:1131–1134.
   PubMed Web of Science ®Google Scholar
• King GL. The role of inflammatory cytokines in diabetes and its complications. J Periodontol. 2008;79:1527–1534.
   PubMed Web of Science ®Google Scholar
• Kaur G, Jaggi AS, Singh N. Exploring the potential effect of Ocimum sanctum in vincristine-induced neuropathic pain in rats. J Brachial Plex Peripher Nerve Inj. 2010;5:3–11.
   PubMedGoogle Scholar
• Muthuraman A, Jaggi AS, Singh N, et al. Ameliorative effects of amiloride and pralidoxime in chronic constriction injury and vincristine induced painful neuropathy in rats. Eur J Pharmacol. 2008;587:104–111.
   PubMed Web of Science ®Google Scholar
• De Mos M, Huygen FJ, Stricker BH, et al. The association between ACE inhibitors and the complex regional pain syndrome: suggestions for a neuro-inflammatory pathogenesis of CRPS. Pain. 2009;142:218–224.
   PubMed Web of Science ®Google Scholar
• Veldman PH, Reynen HM, Arntz IE, et al. Signs and symptoms of reflex sympathetic dystrophy: prospective study of 829 patients. Lancet. 1993;342:1012–1016.
   PubMed Web of Science ®Google Scholar
• Huygen FJ, De Bruijn AG, De Bruin MT, et al. Evidence for local inflammation in complex regional pain syndrome type 1. Mediators Inflamm. 2002;11:47–51.
   PubMed Web of Science ®Google Scholar
• Gradl G, Finke B, Schattner S, et al. Continuous intra-arterial application of substance P induces signs and symptoms of experimental complex regional pain syndrome (CRPS) such as edema, inflammation and mechanical pain but no thermal pain. Neuroscience. 2007;148:757–765.
   PubMed Web of Science ®Google Scholar
• Skidgel RA, Erdös EG. Angiotensin converting enzyme (ACE) and neprilysin hydrolyze neuropeptides: a brief history, the beginning and follow-ups to early studies. Peptides. 2004;25:521–525.
   PubMed Web of Science ®Google Scholar
• Dendorfer A, Wolfrum S, Wellhöner P, et al. Intravascular and interstitial degradation of bradykinin in isolated perfused rat heart. Br J Pharmacol. 1997;122:1179–1187.
   PubMed Web of Science ®Google Scholar
• Ghione S. Hypertension-associated hypalgesia: evidence in experimental animals and humans, pathophysiological mechanisms, and potential clinical consequences. Hypertension. 1996;28:494–504.
   PubMed Web of Science ®Google Scholar
• Sheps DS, Bragdon EE, Gray TF III, et al. Relation between systemic hypertension and pain perception. Am J Cardiol. 1992;70:3–5.
   PubMed Web of Science ®Google Scholar
• Ghione S, Rosa C, Mezzasalma L, et al. Arterial hypertension is associated with hypalgesia in humans. Hypertension. 1988;12:491–497.
   PubMed Web of Science ®Google Scholar
• Guasti L, Grimoldi P, Diolisi A, et al. Treatment with enalapril modifies the pain perception pattern in hypertensive patients. Hypertension. 1998;31:1146–1150.
   PubMed Web of Science ®Google Scholar
• Rice ASC, Dworkin RH, McCarthy TD, et al. EMA401, an orally administered highly selective angiotensin II type 2 receptor antagonist, as a novel treatment for postherpetic neuralgia: a randomised, double-blind, placebo-controlled phase 2 clinical trial. Lancet. 2014;383:1637–1647.
   PubMed Web of Science ®Google Scholar
• The Effect of Spironolactone on Pain in Older People with Osteoarthris. University of Dundee & NHS Tayside. 2013. [cited2015 Dec 3]. Available from: www.clinicaltrialsregister.eu/ctr-search/trial/2013-002638-19/GB
   Google Scholar