Arresting inflammation: Contributions of plasma membrane and endosomal signalling to neuropeptide-driven inflammatory disease

Biochemical Society Transactions

Volumn 41, Issue 1, 2013, Pages 137-143

  Cattaruzza, Fiore ^a   Poole, Daniel P ^b   Bunnett, Nigel W ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b MONASH UNIVERSITY   (Australia)

Author keywords

Arrestin; Endosome; G protein coupled receptor (GPCR); Neuropeptide; Protease; Trafficking

Indexed keywords

ANGIOTENSIN 1A RECEPTOR; BETA ARRESTIN; BETA ARRESTIN 1; BETA ARRESTIN 2; BRADYKININ B2 RECEPTOR; CHEMOKINE RECEPTOR CXCR2; CLATHRIN; ENDOTHELIN CONVERTING ENZYME; GLYCOGEN SYNTHASE KINASE 3; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 8; MEMBRANE METALLOENDOPEPTIDASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MU OPIATE RECEPTOR; NEUROKININ 1 RECEPTOR; NEUROKININ 3 RECEPTOR; NEUROTENSIN RECEPTOR; SOMATOSTATIN 14; STRESS ACTIVATED PROTEIN KINASE; SUBSTANCE P; VANILLOID RECEPTOR 4; VASOPRESSIN V2 RECEPTOR;

APOPTOSIS; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; CELL MIGRATION; CELL PROLIFERATION; CELL SURFACE; CELL SURVIVAL; CELLULAR DISTRIBUTION; CONFERENCE PAPER; CYTOKINE PRODUCTION; DISEASE EXACERBATION; ENDOCYTOSIS; ENDOSOME; ENDOTHELIUM CELL; ENZYME ACTIVATION; GENE DELETION; IN VIVO STUDY; INFLAMMATORY CELL; NEUROGENIC INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RECEPTOR DOWN REGULATION; SIGNAL TRANSDUCTION; TIGHT JUNCTION; UBIQUITINATION;

CELL MEMBRANE; ENDOSOMES; HUMANS; INFLAMMATION; NEUROPEPTIDES; SIGNAL TRANSDUCTION;

EID: 84873203576     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST20120343     Document Type: Conference Paper

References (50)

1. Murphy, J. E., Padilla, B. E., Hasdemir, B., Cottrell, G. S. and Bunnett, N. W. (2009) Endosomes: a legitimate platform for the signaling train. Proc. Natl. Acad. Sci. U. S. A. 106, 17615-17622
2. Bowden, J. J., Garland, A. M., Baluk, P., Lefevre, P., Grady, E. F., Vigna, S. R., Bunnett, N. W. and McDonald, D. M. (1994) Direct observation of substance P-induced internalization of neurokinin 1 (NK1) receptors at sites of inflammation. Proc. Natl. Acad. Sci. U. S. A. 91, 8964-8968
3. Grady, E. F., Gamp, P. D., Jones, E., Baluk, P., McDonald, D. M., Payan, D. G. and Bunnett, N. W. (1996) Endocytosis and recycling of neurokinin 1 receptors in enteric neurons. Neuroscience 75, 1239-1254 (Pubitemid 26377109)
4. Mantyh, P. W., DeMaster, E., Malhotra, A., Ghilardi, J. R., Rogers, S. D., Mantyh, C. R., Liu, H., Basbaum, A. I., Vigna, S. R., Maggio, J. E. et al. (1995) Receptor endocytosis and dendrite reshaping in spinal neurons after somatosensory stimulation. Science 268, 1629-1632
5. Marvizon, J. C., Martinez, V., Grady, E. F., Bunnett, N. W. and Mayer, E. A. (1997) Neurokinin 1 receptor internalization in spinal cord slices induced by dorsal root stimulation is mediated by NMDA receptors. J. Neurosci. 17, 8129-8136 (Pubitemid 27461037)
6. Southwell, B. R., Woodman, H. L., Royal, S. J. and Furness, J. B. (1998) Movement of villi induces endocytosis of NK1 receptors in myenteric neurons from guinea-pig ileum. Cell Tissue Res. 292, 37-45 (Pubitemid 28143874)
7. Mantyh, C. R., Pappas, T. N., Lapp, J. A., Washington, M. K., Neville, L. M., Ghilardi, J. R., Rogers, S. D., Mantyh, P. W. and Vigna, S. R. (1996) Substance P activation of enteric neurons in response to intraluminal Clostridium difficile toxin A in the rat ileum. Gastroenterology 111, 1272-1280 (Pubitemid 26362252)
8. Mantyh, P. W., Rogers, S. D., Honore, P., Allen, B. J., Ghilardi, J. R., Li, J., Daughters, R. S., Lappi, D. A., Wiley, R. G. and Simone, D. A. (1997) Inhibition of hyperalgesia by ablation of lamina I spinal neurons expressing the substance P receptor. Science 278, 275-279 (Pubitemid 27450872)
9. Sternini, C, Spann, M., Anton, B., Keith, Jr, D. E., Bunnett, N. W., von Zastrow, M., Evans, C. and Brecha, N. C. (1996) Agonist-selective endocytosis of μ opioid receptor by neurons in vivo. Proc. Natl. Acad. Sci. U. S. A. 93, 9241-9246 (Pubitemid 26282048)
10. Trafton, J. A., Abbadie, C, Marek, K. and Basbaum, A. I. (2000) Postsynaptic signaling via the μ-opioid receptor: responses of dorsal horn neurons to exogenous opioids and noxious stimulation. J. Neurosci. 20, 8578-8584
11. Poole, D. P., Pelayo, J. C., Scherrer, G., Evans, C. J., Kieffer, B. L. and Bunnett, N. W. (2011) Localization and regulation of fluorescently labeled S opioid receptor, expressed in enteric neurons of mice. Gastroenterology 141, 982-991 e981-e988
12. Scherrer, G., Tryoen-Toth, P., Filliol, D., Matifas, A., Laustriat, D., Cao, Y. Q., Basbaum, A. I., Dierich, A., Vonesh, J. L., Gaveriaux-Ruff, C. and Kieffer, B. L. (2006) Knockin mice expressing fluorescent δ-opioid receptors uncover G protein-coupled receptor dynamics in vivo. Proc. Natl. Acad. Sci. U. S. A. 103, 9691-9696 (Pubitemid 43955886)
13. Shenoy, S. K. and Lefkowitz, R. J. (2011) β-Arrestin-mediated receptor trafficking and signal transduction. Trends Pharmacol. Sci. 32, 521-533
14. DeFea, K. A., Vaughn, Z. D., O'Bryan, E. M., Nishijima, D., Dery, O. and Bunnett, N. W. (2000) The proliferative and antiapoptotic effects of substance P are facilitated by formation of a β-arrestin-dependent scaffolding complex. Proc. Natl. Acad. Sci. U. S. A. 97, 11086-11091
15. McConalogue, K., Dery, O., Lovett, M., Wong, H., Walsh, J. H., Grady, E. F. and Bunnett, N. W. (1999) Substance P-induced trafficking of β-arrestins: the role of β-arrestins in endocytosis of the neurokinin-1 receptor. J. Biol. Chem. 274, 16257-16268
16. Schmidlin, F., Roosterman, D. and Bunnett, N. W. (2003) The third intracellular loop and carboxyl tail of neurokinin 1 and 3 receptors determine interactions with β-arrestins. Am. J. Physiol. Cell Physiol. 285, C945-C958 (Pubitemid 37158819)
17. Schmidlin, F., Dery, O., Bunnett, N. W. and Grady, E. F. (2002) Heterologous regulation of trafficking and signaling of G protein-coupled receptors: β-arrestin-dependent interactions between neurokinin receptors. Proc. Natl. Acad. Sci. U. S. A. 99, 3324-3329 (Pubitemid 34240630)
18. Yu, Y. J., Arttamangkul, S., Evans, C. J., Williams, J. T. and von Zastrow, M. (2009) Neurokinin 1 receptors regulate morphine-induced endocytosis and desensitization of μ-opioid receptors in CNS neurons. J. Neurosci. 29, 222-233
19. Murphy, J. E., Roosterman, D., Cottrell, G. S., Padilla, B. E., Feld, M., Brand, E., Cedron, W. J., Bunnett, N. W. and Steinhoff, M. (2011) Protein phosphatase 2A mediates resensitization of the neurokinin 1 receptor. Am. J. Physiol. Cell Physiol. 301, C780-C791
20. Ahn, S., Kim, J., Hara, M. R., Ren, X. R. and Lefkowitz, R. J. (2009) β-Arrestin-2 mediates anti-apoptotic signaling through regulation of BAD phosphorylation. J. Biol. Chem. 284, 8855-8865
21. DeFea, K. A., Zalevsky, J., Thoma, M. S., Dery, O., Mullins, R. D. and Bunnett, N. W. (2000) β-Arrestin-dependent endocytosis of proteinase-activated receptor 2 is required for intracellular targeting of activated ERK1/2. J. Cell Biol. 148, 1267-1281
22. DeWire, S. M., Kim, J., Whalen, E. J., Ahn, S., Chen, M. and Lefkowitz, R. J. (2008) β-Arrestin-mediated signaling regulates protein synthesis. J. Biol. Chem. 283, 10611-10620
23. Beaulieu, J. M., Sotnikova, T. D., Marion, S., Lefkowitz, R. J., Gainetdinov, R. R. and Caron, M. G. (2005) An Akt/β-arrestin 2/PP2A signaling complex mediates dopaminergic neurotransmission and behavior. Cell 122, 261-273 (Pubitemid 41032989)
24. Walters, R. W., Shukla, A. K., Kovacs, J. J., Violin, J. D., DeWire, S. M., Lam, C. M., Chen, J. R., Muehlbauer, M. J., Whalen, E. J. and Lefkowitz, R. J. (2009) β-Arrestin1 mediates nicotinic acid-induced flushing, but not its antilipolytic effect, in mice. J. Clin. Invest. 119, 1312-1321
25. Gao, H., Sun, Y., Wu, Y., Luan, B., Wang, Y., Qu, B. and Pei, G. (2004) Identification of β-arrestin2 as a G protein-coupled receptor-stimulated regulator of NF-κB pathways. Mol. Cell 14, 303-317 (Pubitemid 38591402)
26. Shukla, A. K., Kim, J., Ahn, S., Xiao, K., Shenoy, S. K., Liedtke, W. and Lefkowitz, R. J. (2010) Arresting a transient receptor potential (TRP) channel: β-arrestin 1 mediates ubiquitination and functional down-regulation of TRPV4. J. Biol. Chem. 285, 30115-30125
27. Barlic, J., Andrews, J. D., Kelvin, A. A., Bosinger, S. E., DeVries, M. E., Xu, L., Dobransky, T., Feldman, R. D., Ferguson, S. S. and Kelvin, D. J. (2000) Regulation of tyrosine kinase activation and granule release through β-arrestin by CXCRI. Nat. Immunol. 1, 227-233
28. Su, Y., Raghuwanshi, S. K., Yu, Y., Nanney, L. B., Richardson, R. M. and Richmond, A. (2005) Altered CXCR2 signaling in β-arrestin-2-deficient mouse models. J. Immunol. 175, 5396-5402 (Pubitemid 41456426)
29. Nichols, H. L., Saffeddine, M., Theriot, B. S., Hegde, A., Polley, D., El-Mays, T., Vliagoftis, H., Hollenberg, M. D., Wilson, E. H., Walker, J. K. and Defea, K. A. (2012) β-Arrestin-2 mediates the proinflammatory effects of proteinase-activated receptor-2 in the airway. Proc. Natl. Acad. Sci. U. S. A. 109, 16660-16665
30. Walker, J. K., Fong, A. M., Lawson, B. L., Savov, J. D., Patel, D. D., Schwartz, D. A. and Lefkowitz, R. J. (2003) β-Arrestin-2 regulates the development of allergic asthma. J. Clin. Invest. 112, 566-574 (Pubitemid 38056341)
31. Jacob, C., Yang, P. C., Darmoul, D., Amadesi, S., Saito, T., Cottrell, G. S., Coelho, A. M., Singh, P., Grady, E. F., Perdue, M. and Bunnett, N. W. (2005) Mast cell tryptase controls paracellular permeability of the intestine: role of protease-activated receptor 2 and β-arrestins. J. Biol. Chem. 280, 31936-31948 (Pubitemid 41291944)
32. Fan, H., Bitto, A., Zingarelli, B., Luttrell, L. M., Borg, K., Halushka, P. V. and Cook, J. A. (2010) β-Arrestin 2 negatively regulates sepsis-induced inflammation. Immunology 130, 344-351
33. Li, P., Cook, J. A., Gilkeson, G. S., Luttrell, L. M., Wang, L., Borg, K. T., Halushka, P. V. and Fan, H. (2011) Increased expression of β-arrestin 1 and 2 in murine models of rheumatoid arthritis: isoform specific regulation of inflammation. Mol. Immunol. 49, 64-74
34. Ge, L., Shenoy, S. K., Lefkowitz, R. J. and DeFea, K. (2004) Constitutive protease-activated receptor-2-mediated migration of MDA MB-231 breast cancer cells requires both β-arrestin-1 and -2. J. Biol. Chem. 279, 55419-55424 (Pubitemid 40066542)
35. Raghuwanshi, S. K., Nasser, M. W., Chen, X., Strieter, R. M. and Richardson, R. M. (2008) Depletion of β-arrestin-2 promotes tumor growth and angiogenesis in a murine model of lung cancer. J. Immunol. 180, 5699-5706
36. Porter, K. J., Gonipeta, B., Parvataneni, S., Appledorn, D. M., Patial, S., Sharma, D., Gangur, V., Amalfitano, A. and Parameswaran, N. (2010) Regulation of lipopolysaccharide-induced inflammatory response and endotoxemia by β-arrestins. J. Cell. Physiol. 225, 406-416
37. Okamoto, A., Lovett, M., Payan, D. G. and Bunnett, N. W. (1994) Interactions between neutral endopeptidase (EC 3.4.24.11) and the substance P (NK1) receptor expressed in mammalian cells. Biochem. J. 299, 683-693 (Pubitemid 24138535)
38. Johnson, G. D., Stevenson, T. and Ahn, K. (1999) Hydrolysis of peptide hormones by endothelin-converting enzyme-1: a comparison with neprilysin. J. Biol. Chem. 274, 4053-4058
39. Cottrell, G. S., Padilla, B. E., Amadesi, S., Poole, D. P., Murphy, J. E., Hardt, M., Roosterman, D., Steinhoff, M. and Bunnett, N. W. (2009) Endosomal endothelin-converting enzyme-1: a regulator of β-arrestin-dependent ERK signaling. J. Biol. Chem. 284, 22411-22425
40. Law, I. K., Murphy, J. E., Bakirtzi, K., Bunnett, N. W. and Pothoulakis, C. (2012) Neurotensin-induced proinflammatory signaling in human colonocytes is regulated by β-arrestins and endothelin-converting enzyme-1-dependent endocytosis and resensitization of neurotensin receptor 1. J. Biol. Chem. 287, 15066-15075
41. Padilla, B. E., Cottrell, G. S., Roosterman, D., Pikios, S., Muller, L., Steinhoff, M. and Bunnett, N. W. (2007) Endothelin-converting enzyme-1 regulates endosomal sorting of calcitonin receptor-like receptor and β-arrestins. J. Cell Biol. 179, 981-997 (Pubitemid 350223493)
42. Roosterman, D., Cottrell, G. S., Padilla, B. E., Muller, L., Eckman, C. B., Bunnett, N. W. and Steinhoff, M. (2007) Endothelin-converting enzyme 1 degrades neuropeptides in endosomes to control receptor recycling. Proc. Natl. Acad. Sci. U. S. A. 104, 11838-11843 (Pubitemid 47175099)
43. Roosterman, D., Kempkes, C., Cottrell, G. S., Padilla, B. E., Bunnett, N. W., Turck, C. W. and Steinhoff, M. (2008) Endothelin-converting enzyme-1 degrades internalized somatostatin-14. Endocrinology 149, 2200-2207 (Pubitemid 351574502)
44. Cattaruzza, F., Cottrell, G. S., Vaksman, N. and Bunnett, N. W. (2009) Endothelin-converting enzyme 1 promotes re-sensitization of neurokinin 1 receptor-dependent neurogenic inflammation. Br. J. Pharmacol. 156, 730-739
45. Pelayo, J. C., Poole, D. P., Steinhoff, M., Cottrell, G. S. and Bunnett, N. W. (2011) Endothelin-converting enzyme-1 regulates trafficking and signalling of the neurokinin 1 receptor in endosomes of myenteric neurones. J. Physiol. 589, 5213-5230
46. Lu, B., Figini, M., Emanueli, C., Geppetti, P., Grady, E. F., Gerard, N. P., Ansell, J., Payan, D. G., Gerard, C. and Bunnett, N. (1997) The control of microvascular permeability and blood pressure by neutral endopeptidase. Nat. Med. 3, 904-907 (Pubitemid 27353452)
47. Sturiale, S., Barbara, G., Qiu, B., Figini, M., Geppetti, P., Gerard, N., Gerard, C., Grady, E. F., Bunnett, N. W. and Collins, S. M. (1999) Neutral endopeptidase (EC 3.4.24.11) terminates colitis by degrading substance P. Proc. Natl. Acad. Sci. U. S. A. 96, 11653-11658 (Pubitemid 29487436)
48. Kirkwood, K. S., Bunnett, N. W., Maa, J., Castagliolo, I., Liu, B., Gerard, N., Zacks, J., Pothoulakis, C. and Grady, E. F. (2001) Deletion of neutral endopeptidase exacerbates intestinal inflammation induced by Clostridium difficile toxin A. Am. J. Physiol. Gastroinstest. Liver Physiol. 281, G544-G551
49. Scholzen, T. E., Steinhoff, M., Bonaccorsi, P., Klein, R., Amadesi, S., Geppetti, P., Lu, B., Gerard, N. P., Olerud, J. E., Luger, T. A. et al. (2001) Neutral endopeptidase terminates substance P-induced inflammation in allergic contact dermatitis. J. Immunol. 166, 1285-1291 (Pubitemid 32060289)
50. Lee, S., Carter, P. R., Watts, M. N., Bao, J. R. and Harris, N. R. (2009) Effects of the endothelin-converting enzyme inhibitor SM-19712 in a mouse model of dextran sodium sulfate-induced colitis. Inflamm. Bowel Dis. 15, 1007-1013