Top

Published in:

01-06-2019 | Neuropathic Pain | Original Article

The kinin B₁ and B₂ receptors and TNFR1/p55 axis on neuropathic pain in the mouse brachial plexus

Authors: Nara L. M. Quintão, Lilian W. Rocha, Gislaine F. da Silva, Ana F. Paszcuk, Marianne N. Manjavachi, Allisson F. Bento, Kathryn Ana B. S. da Silva, Maria M. Campos, João B. Calixto

Published in: Inflammopharmacology | Issue 3/2019

Abstract

Tumour necrosis factor (TNF) and kinins have been associated with neuropathic pain-like behaviour in numerous animal models. However, the way that they interact to cause neuron sensitisation remains unclear. This study assessed the interaction of kinin receptors and TNF receptor TNFR1/p55 in mechanical hypersensitivity induced by an intraneural (i.n.) injection of rm-TNF into the lower trunk of brachial plexus in mice. The i.n. injection of rm-TNF reduced the mechanical withdrawal threshold of the right forepaw from the 3rd to the 10th day after the injection, indicating that TNF1/p55 displays a critical role in the onset of TNF-elicited neuropathic pain. The connection between TNF1/p55 and kinin B₁ and B₂ receptors (B₁R and B₂R) was confirmed using both knockout mice and mRNAs quantification in the injected nerve, DRG and spinal cord. The treatment with the B₂R antagonist HOE 140 or with B₁R antagonist des-Arg⁹-Leu⁸-BK reduced both BK- and DABK-induced hypersensitivity. The experiments using kinin receptor antagonists and CPM inhibitor (thiorphan) suggest that BK does not only activate B₂R as an orthosteric agonist, but also seems to be converted into DABK that consequently activates B₁R. These results indicate a connection between TNF and the kinin system, suggesting a relevant role for B₁R and B₂R in the process of sensitisation of the central nervous systems by the cross talk between the receptor and CPM after i.n. injection of rm-TNF.

Aggarwal BB, Gupta SC, Kim JH (2012) Historical perspectives on tumor necrosis factor and its superfamily: 25 years later, a golden journey. Blood 119(3):651–665. https://doi.org/10.1182/blood-2011-04-325225 CrossRefPubMedPubMedCentral

Akita K, Okuno M, Enya M, Imai S, Moriwaki H, Kawada N, Suzuki Y, Kojima S (2002) Impaired liver regeneration in mice by lipopolysaccharide via TNF-alpha/kallikrein-mediated activation of latent TGF-beta. Gastroenterology 123(1):352–364. https://doi.org/10.1053/gast.2002.34234 CrossRefPubMed

Andrade P, Visser-Vandewalle V, Hoffmann C, Steinbusch HW, Daemen MA, Hoogland G (2011) Role of TNF-alpha during central sensitization in preclinical studies. Neurol Sci 32(5):757–771. https://doi.org/10.1007/s10072-011-0599-z CrossRefPubMedPubMedCentral

Bastien D, Lacroix S (2014) Cytokine pathways regulating glial and leukocyte function after spinal cord and peripheral nerve injury. Exp Neurol 258:62–77. https://doi.org/10.1016/j.expneurol.2014.04.006 CrossRefPubMed

Calixto JB, Cabrini DA, Ferreira J, Campos MM (2000) Kinins in pain and inflammation. Pain 87(1):1–5. https://doi.org/10.1016/S0304-3959(00)00335-3 CrossRefPubMed

Calixto JB, Cabrini DA, Ferreira J, Campos MM (2001) Inflammatory pain: kinins and antagonists. Curr Opin Anaesthesiol 14(5):519–526CrossRefPubMed

Calixto JB, Medeiros R, Fernandes ES, Ferreira J, Cabrini DA, Campos MM (2004) Kinin B₁ receptors: key G-protein-coupled receptors and their role in inflammatory and painful processes. Br J Pharmacol 143(7):803–818. https://doi.org/10.1038/sj.bjp.0706012 CrossRefPubMedPubMedCentral

Campos AH, Calixto JB, Schor N (1999) Effects of kinins upon cytosolic calcium concentrations in mouse mesangial cells. Immunopharmacology 45(1–3):39–49CrossRefPubMed

Campos MM, Leal PC, Yunes RA, Calixto JB (2006) Non-peptide antagonists for kinin B₁ receptors: new insights into their therapeutic potential for the management of inflammation and pain. Trends Pharmacol Sci 27(12):646–651. https://doi.org/10.1016/j.tips.2006.10.007 CrossRefPubMed

Compston A, Zajicek J, Sussman J, Webb A, Hall G, Muir D, Shaw C, Wood A, Scolding N (1997) Glial lineages and myelination in the central nervous system. J Anat 190:161–200. https://doi.org/10.1046/j.1469-7580.1997.19020161.x CrossRefPubMedPubMedCentral

Couture R, Harrisson M, Vianna RM, Cloutier F (2001) Kinin receptors in pain and inflammation. Eur J Pharmacol 429(1–3):161–176. https://doi.org/10.1016/S0014-2999(01)01318-8 CrossRefPubMed

Cunha TM, Verri WA Jr, Fukada SY, Guerrero AT, Santodomingo-Garzón T, Poole S, Parada CA, Ferreira SH, Cunha FQ (2007) TNF-alpha and IL-1beta mediate inflammatory hypernociception in mice triggered by B₁ but not B₂ kinin receptor. Eur J Pharmacol 573(1–3):221–229. https://doi.org/10.1016/j.ejphar.2007.07.007 CrossRefPubMed

Deiteren K, Hendriks D, Scharpé S, Lambeir AM (2009) Carboxypeptidase M: multiple alliances and unknown partners. Clin Chim Acta 399(1–2):24–39. https://doi.org/10.1016/j.cca.2008.10.003 CrossRefPubMed

Fernandes ES, Passos GF, Campos MM, Araújo JG, Pesquero JL, Avelllar MC, Teixeira MM, Calixto JB (2003) Mechanisms underlying the modulatory action of platelet activating factor (PAF) on the upregulation of kinin B₁ receptors in the rat paw. Br J Pharmacol 139(5):973–981. https://doi.org/10.1038/sj.bjp.0705314 CrossRefPubMedPubMedCentral

Ferreira J, Campos MM, Araújo R, Bader M, Pesquero JB, Calixto JB (2002) The use of kinin B₁ and B₂ receptor knockout mice and selective antagonists to characterize the nociceptive responses caused by kinins at the spinal level. Neuropharmacology 43(7):1188–1197. https://doi.org/10.1016/S0028-3908(02)00311-8 CrossRefPubMed

Ferreira J, da Silva GL, Calixto JB (2004) Contribution of vanilloid receptors to the overt nociception induced by B₂ kinin receptor activation in mice. Br J Pharmacol 141(5):787–794. https://doi.org/10.1038/sj.bjp.0705546 CrossRefPubMedPubMedCentral

Ferreira J, Trichês KM, Medeiros R, Calixto JB (2005) Mechanisms involved in the nociception produced by peripheral protein kinase C activation in mice. Pain 117(1–2):171–181. https://doi.org/10.1016/j.pain.2005.06.001 CrossRefPubMed

George A, Buehl A, Sommer C (2004) Tumor necrosis factor receptor 1 and 2 proteins are differentially regulated during Wallerian degeneration of mouse sciatic nerve. Exp Neurol 192(1):163–166. https://doi.org/10.1016/j.expneurol.2004.11.002 CrossRef

Jin X, Gereau RW (2004) Acute p38-mediated modulation of tetrodotoxin-resistant sodium channels in mouse sensory neurons by tumor necrosis factor-alpha. J Neurosci 26:246–255. https://doi.org/10.1523/JNEUROSCI.3858-05.2006 CrossRef

Joedicke L, Mao J, Kuenze G, Reinhart C, Kalavacherla T, Jonker HRA, Richter C, Schwalbe H, Meiler J, Preu J, Michel H, Glaubitz C (2018) The molecular basis of subtype selectivity of human kinin G-protein-coupled receptors. Nat Chem Biol 14(3):284–290. https://doi.org/10.1038/nchembio.2551 CrossRefPubMedPubMedCentral

Kato K, Kikuchi S, Shubayev VI, Myers RR (2009) Distribution and tumor necrosis factor-alpha isoform binding specificity of locally administered etanercept into injured and uninjured rat sciatic nerve. Neuroscience 160(2):492–500. https://doi.org/10.1016/j.neuroscience.2009.02.038 CrossRefPubMed

Kuduk SD, Bock MG (2008) Bradykinin B₁ receptor antagonists as novel analgesics: a retrospective of selected medicinal chemistry developments. Curr Top Med Chem 8(16):1420–1430CrossRefPubMed

Leeb-Lundberg LM, Marceau F, Müller-Esterl W, Pettibone DJ, Zuraw BL (2005) International union of pharmacology. XLV. Classification of the kinin receptor family: from molecular mechanisms to pathophysiological consequences. Pharmacol Rev 57(1):27–77. https://doi.org/10.1124/pr.57.1.2 CrossRefPubMed

Levy D, Zochodne DW (2000) Increased mRNA expression of the B₁ and B₂ bradykinin receptors and antinociceptive effects of their antagonists in an animal model of neuropathic pain. Pain 86(3):265–271. https://doi.org/10.1016/S0304-3959(00)00256-6 CrossRefPubMed

Marceau F, Bawolak MT, Fortin JP, Morissette G, Roy C, Bachelard H, Gera L, Charest-Morin X (2018) Bifunctional ligands of the bradykinin B(2) and B(1) receptors: an exercise in peptide hormone plasticity. Peptides 105:37–50. https://doi.org/10.1016/j.peptides.2018.05.007 CrossRefPubMed

Medeiros R, Cabrini DA, Ferreira J, Fernandes ES, Mori MA, Pesquero JB, Bader M, Avellar MC, Campos MM, Calixto JB (2004) Bradykinin B₁ receptor expression induced by tissue damage in the rat portal vein: a critical role for mitogen-activated protein kinase and nuclear factor-kappaB signaling pathways. Circ Res 94(10):1375–1382. https://doi.org/10.1161/01.RES.0000128404.65887.08 CrossRefPubMed

Meotti FC, Campos R, da Silva K, Paszcuk AF, Costa R, Calixto JB (2012) Inflammatory muscle pain is dependent on the activation of kinin B₁ and B₂ receptors and intracellular kinase pathways. Br J Pharmacol 166(3):1127–1139. https://doi.org/10.1111/j.1476-5381.2012.01830.x CrossRefPubMedPubMedCentral

Mitchell S, Vargas J, Hoffmann A (2016) Signaling via the NFκB system. Wiley Interdiscip Rev Syst Biol Med 8(3):227–241. https://doi.org/10.1002/wsbm.1331 CrossRefPubMedPubMedCentral

Mogil JS, Chanda ML (2005) The case for the inclusion of female subjects in basic science studies of pain. Pain 117(1–2):1–5CrossRefPubMed

Olmos G, Lladó J (2014) Tumor necrosis factor alpha: a link between neuroinflammation and excitotoxicity. Mediators Inflamm 2014:861231. https://doi.org/10.1155/2014/861231 CrossRefPubMedPubMedCentral

Passos GF, Fernandes ES, Campos MM, Araújo JG, Pesquero JL, Souza GE, Avellar MC, Teixeira MM, Calixto JB (2004) Kinin B₁ receptor up-regulation after lipopolysaccharide administration: role of proinflammatory cytokines and neutrophil influx. J Immunol 172(3):1839–1847. https://doi.org/10.4049/jimmunol.172.3.1839 CrossRefPubMed

Paul AT, Gohil VM, Bhutani KK (2006) Modulating TNF-alpha signaling with natural products. Drug Discov Today 11(15–16):725–732. https://doi.org/10.1016/j.drudis.2006.06.002 CrossRefPubMed

Perkins NM, Tracey DJ (2000) Hyperalgesia due to nerve injury: role of neutrophils. Neuroscience 101(3):745–757. https://doi.org/10.1016/S0306-4522(00)00396-1 CrossRefPubMed

Petersen M, Eckert AS, Segond von Banchet G, Heppelmann B, Klusch A, Kniffki KD (1998) Plasticity in the expression of bradykinin binding sites in sensory neurons after mechanical nerve injury. Neuroscience 83(3):949–959. https://doi.org/10.1016/S0306-4522(97)00465-X CrossRefPubMed

Phagoo SB, Reddi K, Anderson KD, Leeb-Lundberg LM, Warburton D (2001) Bradykinin B₁ receptor up-regulation by interleukin-1beta and B₁ agonist occurs through independent and synergistic intracellular signaling mechanisms in human lung fibroblasts. J Pharmacol Exp Ther 298(1):77–85PubMed

Podsiadło K, Sulkowski G, Dąbrowska-Bouta B, Strużyńska L (2017) Blockade of the kinin B₁ receptor affects the cytokine/chemokine profile in rat brain subjected to autoimmune encephalomyelitis. Inflammopharmacology 25(4):459–469CrossRefPubMed

Poole S, Lorenzetti BB, Cunha JM, Cunha FQ, Ferreira SH (1999) Bradykinin B₁ and B₂ receptors, tumour necrosis factor alpha and inflammatory hyperalgesia. Br J Pharmacol 126(3):649–656. Erratum in: Br J Pharmacol 127(1):314. https://doi.org/10.1038/sj.bjp.0702347

Quintão NL, Balz D, Santos AR, Campos MM, Calixto JB (2006) Long-lasting neuropathic pain induced by brachial plexus injury in mice: role triggered by the pro-inflammatory cytokine, tumour necrosis factor alpha. Neuropharmacology 50(5):614–620. https://doi.org/10.1016/j.neuropharm.2005.11.007 CrossRefPubMed

Quintão NL, Passos GF, Medeiros R, Paszcuk AF, Motta FL, Pesquero JB, Campos MM, Calixto JB (2008) Neuropathic pain-like behavior after brachial plexus avulsion in mice: the relevance of kinin B₁ and B₂ receptors. J Neurosci 28(11):2856–2863. https://doi.org/10.1523/JNEUROSCI.4389-07.2008 CrossRefPubMedPubMedCentral

Rashid MH, Inoue M, Matsumoto M, Ueda H (2004) Switching of bradykinin-mediated nociception following partial sciatic nerve injury in mice. J Pharmacol Exp Ther 308(3):1158–1164. https://doi.org/10.1124/jpet.103.060335 CrossRefPubMed

Sabourin T, Morissette G, Bouthillier J, Levesque L, Marceau F (2002) Expression of kinin B(1) receptor in fresh or cultured rabbit aortic smooth muscle: role of NF-kappa B. Am J Physiol Heart Circ Physiol 283(1):H227–H237. https://doi.org/10.1152/ajpheart.00978.2001 CrossRefPubMed

Sacerdote P, Franchi S, Trovato AE, Valsecchi AE, Panerai AE (2008) Colleoni M.: Transient early expression of TNF-alpha in sciatic nerve and dorsal root ganglia in a mouse model of painful peripheral neuropathy. Neurosci Lett 436(2):210–213. https://doi.org/10.1016/j.neulet.2008.03.023 CrossRefPubMed

Schäfers M, Geis C, Svensson CI, Luo ZD, Sommer C (2003) Selective increase of tumour necrosis factor-alpha in injured and spared myelinated primary afferents after chronic constrictive injury of rat sciatic nerve. Eur J Neurosci 17(4):791–804. https://doi.org/10.1046/j.1460-9568.2003.02504.x CrossRefPubMed

Shamash S, Reichert F, Rotshenker S (2002) The cytokine network of Wallerian degeneration: tumor necrosis factor-alpha, interleukin-1alpha, and interleukin-1beta. J Neurosci 22(8):3052–3060CrossRefPubMedPubMedCentral

Shubayev VI, Myers RR (2000) Upregulation and interaction of TNFalpha and gelatinases A and B in painful peripheral nerve injury. Brain Res 855(1):83–89. https://doi.org/10.1016/S0006-8993(99)02321-5 CrossRefPubMed

Shubayev VI, Myers RR (2001) Axonal transport of TNF-alpha in painful neuropathy: distribution of ligand tracer and TNF receptors. J Neuroimmunol 114(1–2):48–56CrossRefPubMed

Simard E, Jin D, Takai S, Miyazaki M, Brochu I, D’Orléans-Juste P (2009) Chymase-dependent conversion of Big endothelin-1 in the mouse in vivo. J Pharmacol Exp Ther 328(2):540–548. https://doi.org/10.1124/jpet.108.142992 CrossRefPubMed

Takano M, Satoh C, Kunimatsu N, Otani M, Hamada-Kanazawa M, Miyake M, Ming K, Yayama K, Okamoto H (2008) Lipopolysaccharide activates the kallikrein-kinin system in mouse choroid plexus cell line ECPC4. Neurosci Lett 434(3):310–314. https://doi.org/10.1016/j.neulet.2008.01.072 CrossRefPubMed

Wang H, Kohno T, Amaya F, Brenner GJ, Ito N, Allchorne A, Ji RR, Woolf CJ (2005) Bradykinin produces pain hypersensitivity by potentiating spinal cord glutamatergic synaptic transmission. J Neurosci 25(35):7986–7992. https://doi.org/10.1523/JNEUROSCI.2393-05.2005 CrossRefPubMedPubMedCentral

Zelenka M, Schäfers M, Sommer C (2005) Intraneural injection of interleukin-1beta and tumor necrosis factor-alpha into rat sciatic nerve at physiological doses induces signs of neuropathic pain. Pain 116(3):257–263. https://doi.org/10.1016/j.pain.2005.04.018 CrossRefPubMed

Zeng XY, Zhang Q, Wang J, Yu J, Han SP, Wang JY (2014) Distinct role of tumor necrosis factor receptor subtypes 1 and 2 in the red nucleus in the development of neuropathic pain. Neurosci Lett 569:43–48. https://doi.org/10.1016/j.neulet.2014.03.048 CrossRefPubMed

Zhang X, Tan F, Zhang Y, Skidgel RA (2008) Carboxypeptidase M and kinin B₁ receptors interact to facilitate efficient B₁ signaling from B₂ agonists. J Biol Chem 283(12):7994–8004. https://doi.org/10.1074/jbc.M709837200 CrossRefPubMed

Zhang X, Tan F, Brovkovych V, Zhang Y, Skidgel RA (2011) Cross-talk between carboxypeptidase M and the kinin B₁ receptor mediates a new mode of G protein-coupled receptor signaling. J Biol Chem 286(21):18547–18561. https://doi.org/10.1074/jbc.M110.214940 CrossRefPubMedPubMedCentral

Zhang X, Tan F, Skidgel RA (2013) Carboxypeptidase M is a positive allosteric modulator of the kinin B₁ receptor. J Biol Chem 288(46):33226–33240. https://doi.org/10.1074/jbc.M113.520791 CrossRefPubMedPubMedCentral

Title: The kinin B1 and B2 receptors and TNFR1/p55 axis on neuropathic pain in the mouse brachial plexus
Authors: Nara L. M. Quintão
Lilian W. Rocha
Gislaine F. da Silva
Ana F. Paszcuk
Marianne N. Manjavachi
Allisson F. Bento
Kathryn Ana B. S. da Silva
Maria M. Campos
João B. Calixto
Publication date: 01-06-2019
Publisher: Springer International Publishing
Keywords: Neuropathic Pain
Cytokines
Published in: Inflammopharmacology / Issue 3/2019
Print ISSN: 0925-4692
Electronic ISSN: 1568-5608
DOI: https://doi.org/10.1007/s10787-019-00578-5

Keynote webinar | Spotlight on medication adherence

Springer Medicine

The kinin B₁ and B₂ receptors and TNFR1/p55 axis on neuropathic pain in the mouse brachial plexus

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 3/2019

Immunomodulatory properties of captopril, an ACE inhibitor, on LPS-induced lung inflammation and fibrosis as well as oxidative stress

Evaluation of the effects of extracts of Maytenus imbricata (Celastraceae) on the treatment of inflammatory and metabolic dysfunction induced by high-refined carbohydrate diet

Ponicidin inhibits pro-inflammatory cytokine TNF-α-induced epithelial–mesenchymal transition and metastasis of colorectal cancer cells via suppressing the AKT/GSK-3β/Snail pathway

Anti-inflammatory properties of Liposome-encapsulated clodronate or Anti-Ly6G can be modulated by peripheral or central inflammatory markers in carrageenan-induced inflammation model

Effect of Synadenium grantii and its isolated compound on dysmenorrhea behavior model in mice

Are peptides a solution for the treatment of hyperactivated JAK3 pathways?