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

  • Nara L. M. QuintãoEmail author
  • 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
Original Article
  • 57 Downloads

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.

Keywords

Brachial plexus Cytokine TNF Neuropathic pain Kinin receptors Carboxypeptidase 

Notes

Acknowledgements

This work was supported by grants from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), the Fundação de Apoio a Pesquisa Científica e Tecnológica do Estado de Santa Catarina (FAPESC), and the Programa de Apoio aos Núcleos de Excelência (PRONEX), Brazil. A. F. P., M. N. M., and A. F. B. were Ph.D. students supported by grants from CNPq and CAPES (Financial Code 001). We are grateful to C. Scheidt for his help in the conception of Figs. 7 and 8 illustrations.

References

  1. 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 CrossRefGoogle Scholar
  2. 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 CrossRefGoogle Scholar
  3. 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 CrossRefGoogle Scholar
  4. 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 CrossRefGoogle Scholar
  5. 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 CrossRefGoogle Scholar
  6. Calixto JB, Cabrini DA, Ferreira J, Campos MM (2001) Inflammatory pain: kinins and antagonists. Curr Opin Anaesthesiol 14(5):519–526CrossRefGoogle Scholar
  7. 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 CrossRefGoogle Scholar
  8. Campos AH, Calixto JB, Schor N (1999) Effects of kinins upon cytosolic calcium concentrations in mouse mesangial cells. Immunopharmacology 45(1–3):39–49CrossRefGoogle Scholar
  9. 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 CrossRefGoogle Scholar
  10. 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 CrossRefGoogle Scholar
  11. 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 CrossRefGoogle Scholar
  12. 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 CrossRefGoogle Scholar
  13. 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 CrossRefGoogle Scholar
  14. 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 CrossRefGoogle Scholar
  15. 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 CrossRefGoogle Scholar
  16. 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 CrossRefGoogle Scholar
  17. 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 CrossRefGoogle Scholar
  18. 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 CrossRefGoogle Scholar
  19. 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 CrossRefGoogle Scholar
  20. 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 CrossRefGoogle Scholar
  21. 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 CrossRefGoogle Scholar
  22. 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):1420–1430CrossRefGoogle Scholar
  23. 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 CrossRefGoogle Scholar
  24. 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 CrossRefGoogle Scholar
  25. 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 CrossRefGoogle Scholar
  26. 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 CrossRefGoogle Scholar
  27. 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 CrossRefGoogle Scholar
  28. 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 CrossRefGoogle Scholar
  29. Mogil JS, Chanda ML (2005) The case for the inclusion of female subjects in basic science studies of pain. Pain 117(1–2):1–5CrossRefGoogle Scholar
  30. 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 CrossRefGoogle Scholar
  31. 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 CrossRefGoogle Scholar
  32. 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 CrossRefGoogle Scholar
  33. 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 CrossRefGoogle Scholar
  34. 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 CrossRefGoogle Scholar
  35. 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):77–85Google Scholar
  36. 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):459–469CrossRefGoogle Scholar
  37. 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
  38. 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 CrossRefGoogle Scholar
  39. 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 CrossRefGoogle Scholar
  40. 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 CrossRefGoogle Scholar
  41. 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 CrossRefGoogle Scholar
  42. 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 CrossRefGoogle Scholar
  43. 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 CrossRefGoogle Scholar
  44. 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):3052–3060CrossRefGoogle Scholar
  45. 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 CrossRefGoogle Scholar
  46. 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):48–56CrossRefGoogle Scholar
  47. 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 CrossRefGoogle Scholar
  48. 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 CrossRefGoogle Scholar
  49. 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 CrossRefGoogle Scholar
  50. 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 CrossRefGoogle Scholar
  51. 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 CrossRefGoogle Scholar
  52. 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 CrossRefGoogle Scholar
  53. 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 CrossRefGoogle Scholar
  54. 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 CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Nara L. M. Quintão
    • 1
    Email author
  • Lilian W. Rocha
    • 1
  • Gislaine F. da Silva
    • 1
  • Ana F. Paszcuk
    • 2
  • Marianne N. Manjavachi
    • 2
  • Allisson F. Bento
    • 2
  • Kathryn Ana B. S. da Silva
    • 1
  • Maria M. Campos
    • 3
  • João B. Calixto
    • 2
    • 4
  1. 1.Programa de Pós-graduação em Ciências Farmacêuticas, Centro de Ciências da SaúdeUniversidade do Vale do ItajaíItajaíBrazil
  2. 2.Departamento de Farmacologia, Centro de Ciências BiológicasUniversidade Federal de Santa CatarinaFlorianópolisBrazil
  3. 3.Centro de Pesquisa em Toxicologia e Farmacologia, Escola de Ciências da SaúdePontifícia Universidade Católica do Rio Grande do Sul (PUCRS)Porto AlegreBrazil
  4. 4.Centro de Inovação e Ensaios pré-clínicosFlorianópolisBrazil

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