Mycobacterial toxin induces analgesia in Buruli ulcer by targeting the angiotensin pathways

Cell

Volumn 157, Issue 7, 2014, Pages 1565-1576

  Marion, Estelle ^a,b   Song, Ok Ryul ^a,b,c   Christophe, Thierry ^b   Babonneau, Jérémie ^b   Fenistein, Denis ^b   Eyer, Joël ^d   Letournel, Frank ^d   Henrion, Daniel ^e   Clere, Nicolas ^f   Paille, Vincent ^e   Guérineau, Nathalie C ^e   Saint André, Jean Paul ^g   Gersbach, Philipp ^h   Altmann, Karl Heinz ^h   Stinear, Timothy Paul ⁱ   Comoglio, Yannick ^j   Sandoz, Guillaume ^j   Preisser, Laurence ^k   Delneste, Yves ^k   Yeramian, Edouard ^l   Marsollier, Laurent ^a,b,k   Brodin, Priscille ^b,c   more..

^a INSERM   (France)

^b Institut Pasteur Korea   (South Korea)

^c INSERM U1019   (France)

^d UNIVERSITÉ D'ANGERS   (France)

^e UNIVERSITÉ D'ANGERS   (France)

^f UNIVERSITÉ D'ANGERS   (France)

^g Laboratoire d'anatomie pathologique   (France)

^h ETH ZURICH   (Switzerland)

ⁱ UNIVERSITY OF MELBOURNE   (Australia)

^j Laboratory of Excellence in Ion Channel Science and Therapeutics   (France)

^k Team 12   (France)

^l INSTITUT PASTEUR   (France)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN RECEPTOR; BACTERIAL TOXIN; MYCOLACTONE; POLYKETIDE; POTASSIUM CHANNEL; PROSTAGLANDIN SYNTHASE; TYPE 2 ANGIOTENSIN II RECEPTOR; UNCLASSIFIED DRUG; ANGIOTENSIN 2 RECEPTOR; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; INTERLEUKIN 23 RECEPTOR; PHOSPHOLIPASE A2; PROSTAGLANDIN E SYNTHASE; PROSTAGLANDIN E2; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1;

ANALGESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BURULI ULCER; CONTROLLED STUDY; EDEMA; FEMALE; HYPERPOLARIZATION; HYPESTHESIA; IN VIVO STUDY; MOUSE; MYCOBACTERIUM ULCERANS; NERVE CELL; NOCICEPTION; NONHUMAN; PHYSIOLOGICAL PROCESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; SIGNAL TRANSDUCTION; VALIDATION PROCESS; ANIMAL TISSUE; BINDING AFFINITY; MEMBRANE STEADY POTENTIAL; NERVE DEGENERATION; NEUROTRANSMISSION; PROTEIN TARGETING;

ANALGESICS; ANGIOTENSINS; ANIMALS; BURULI ULCER; DISEASE MODELS, ANIMAL; EDEMA; HUMANS; HYPESTHESIA; MACROLIDES; MICE; MYCOBACTERIUM ULCERANS; NEURONS; POTASSIUM CHANNELS; PROSTAGLANDIN-ENDOPEROXIDE SYNTHASES; RECEPTOR, ANGIOTENSIN, TYPE 2; SIGNAL TRANSDUCTION;

EID: 84903151764     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2014.04.040     Document Type: Article

References (46)

1. U. Anand, P. Facer, Y. Yiangou, M. Sinisi, M. Fox, T. McCarthy, C. Bountra, Y.E. Korchev, and P. Anand Angiotensin II type 2 receptor (AT2 R) localization and antagonist-mediated inhibition of capsaicin responses and neurite outgrowth in human and rat sensory neurons Eur. J. Pain 17 2013 1012 1026
2. Asiedu, K., Sherpbier, R., and Raviglione, M.C. (2000). Buruli Ulcer Mycobacterium ulcerans infection. W.H.O. Global Buruli Ulcer Initiative. Report 2000 World Health Organisation (Geneva: WHO).
3. G.A. Banker, and W.M. Cowan Rat hippocampal neurons in dispersed cell culture Brain Res. 126 1977 397-42
4. K. Bedecs, N. Elbaz, M. Sutren, M. Masson, C. Susini, A.D. Strosberg, and C. Nahmias Angiotensin II type 2 receptors mediate inhibition of mitogen-activated protein kinase cascade and functional activation of SHP-1 tyrosine phosphatase Biochem. J. 325 1997 449 454
5. J.M. Besson The neurobiology of pain Lancet 353 1999 1610 1615
6. J.P. Carralot, T.K. Kim, B. Lenseigne, A.S. Boese, P. Sommer, A. Genovesio, and P. Brodin Automated high-throughput siRNA transfection in raw 264.7 macrophages: a case study for optimization procedure J. Biomol. Screen. 14 2009 151 160
7. N. Clere, I. Corre, S. Faure, A.L. Guihot, E. Vessières, M. Chalopin, A. Morel, O. Coqueret, L. Hein, and Y. Delneste et al. Deficiency or blockade of angiotensin II type 2 receptor delays tumorigenesis by inhibiting malignant cell proliferation and angiogenesis Int. J. Cancer 127 2010 2279 2291
8. E. Coutanceau, L. Marsollier, R. Brosch, E. Perret, P. Goossens, M. Tanguy, S.T. Cole, P.L. Small, and C. Demangel Modulation of the host immune response by a transient intracellular stage of Mycobacterium ulcerans: the contribution of endogenous mycolactone toxin Cell. Microbiol. 7 2005 1187 1196
9. V. Dall'Asta, R. Gatti, G. Orlandini, P.A. Rossi, B.M. Rotoli, R. Sala, O. Bussolati, and G.C. Gazzola Membrane potential changes visualized in complete growth media through confocal laser scanning microscopy of bis-oxonol-loaded cells Exp. Cell Res. 231 1997 260 268
10. J. En, M. Goto, K. Nakanaga, M. Higashi, N. Ishii, H. Saito, S. Yonezawa, H. Hamada, and P.L. Small Mycolactone is responsible for the painlessness of Mycobacterium ulcerans infection (buruli ulcer) in a murine study Infect. Immun. 76 2008 2002 2007
11. D. Fenistein, B. Lenseigne, T. Christophe, P. Brodin, and A. Genovesio A fast, fully automated cell segmentation algorithm for high-throughput and high-content screening Cytometry A 73 2008 958 964
12. J.I. Fletcher, M. Haber, M.J. Henderson, and M.D. Norris ABC transporters in cancer: more than just drug efflux pumps Nat. Rev. Cancer 10 2010 147 156
13. K.M. George, D. Chatterjee, G. Gunawardana, D. Welty, J. Hayman, R. Lee, and P.L. Small Mycolactone: a polyketide toxin from Mycobacterium ulcerans required for virulence Science 283 1999 854 857
14. P. Gersbach, A. Jantsch, F. Feyen, N. Scherr, J.P. Dangy, G. Pluschke, and K.H. Altmann A ring-closing metathesis (RCM)-based approach to mycolactones A/B Chemistry 17 2011 13017 13031
15. M. Goto, K. Nakanaga, T. Aung, T. Hamada, N. Yamada, M. Nomoto, S. Kitajima, N. Ishii, S. Yonezawa, and H. Saito Nerve damage in Mycobacterium ulcerans-infected mice: probable cause of painlessness in buruli ulcer Am. J. Pathol. 168 2006 805 811
16. J.W. Griffin, and W.J. Thompson Biology and pathology of nonmyelinating Schwann cells Glia 56 2008 1518 1531
17. L. Guenin-Macé, F. Carrette, F. Asperti-Boursin, A. Le Bon, L. Caleechurn, V. Di Bartolo, A. Fontanet, G. Bismuth, and C. Demangel Mycolactone impairs T cell homing by suppressing microRNA control of L-selectin expression Proc. Natl. Acad. Sci. USA 108 2011 12833 12838
18. L. Guenin-Macé, R. Veyron-Churlet, M.I. Thoulouze, G. Romet-Lemonne, H. Hong, P.F. Leadlay, A. Danckaert, M.T. Ruf, S. Mostowy, and C. Zurzolo et al. Mycolactone activation of Wiskott-Aldrich syndrome proteins underpins Buruli ulcer formation J. Clin. Invest. 123 2013 1501 1512
19. L. Hein, G.S. Barsh, R.E. Pratt, V.J. Dzau, and B.K. Kobilka Behavioural and cardiovascular effects of disrupting the angiotensin II type-2 receptor in mice Nature 377 1995 744 747
20. J.G. Hoeijmakers, C.G. Faber, G. Lauria, I.S. Merkies, and S.G. Waxman Small-fibre neuropathies - advances in diagnosis, pathophysiology and management Nat Rev Neurol 8 2012 369 379
21. P.D. Johnson, T. Stinear, P.L. Small, G. Pluschke, R.W. Merritt, F. Portaels, K. Huygen, J.A. Hayman, and K. Asiedu Buruli ulcer (M. ulcerans infection): new insights, new hope for disease control PLoS Med. 2 2005 e108
22. J. Kang, P. Posner, and C. Sumners Angiotensin II type 2 receptor stimulation of neuronal K+ currents involves an inhibitory GTP binding protein Am. J. Physiol. 267 1994 C1389 C1397
23. I. Lauritzen, N. Blondeau, C. Heurteaux, C. Widmann, G. Romey, and M. Lazdunski Polyunsaturated fatty acids are potent neuroprotectors EMBO J. 19 2000 1784 1793
24. L. Marsollier, J. Aubry, E. Coutanceau, J.P. André, P.L. Small, G. Milon, P. Legras, S. Guadagnini, B. Carbonnelle, and S.T. Cole Colonization of the salivary glands of Naucoris cimicoides by Mycobacterium ulcerans requires host plasmatocytes and a macrolide toxin, mycolactone Cell. Microbiol. 7 2005 935 943
25. L. Marsollier, P. Brodin, M. Jackson, J. Korduláková, P. Tafelmeyer, E. Carbonnelle, J. Aubry, G. Milon, P. Legras, and J.P. André et al. Impact of Mycobacterium ulcerans biofilm on transmissibility to ecological niches and Buruli ulcer pathogenesis PLoS Pathog. 3 2007 e62
26. A. Muralidharan, B.D. Wyse, and M.T. Smith 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. 15 2014 93 110
27. J. Noël, G. Sandoz, and F. Lesage Molecular regulations governing TREK and TRAAK channel functions Channels (Austin) 5 2011 402 409
28. S. Nouet, and C. Nahmias Signal transduction from the angiotensin II AT2 receptor Trends Endocrinol. Metab. 11 2000 1 6
29. A. Pelegrini-da-Silva, A.R. Martins, and W.A. Prado A new role for the renin-angiotensin system in the rat periaqueductal gray matter: angiotensin receptor-mediated modulation of nociception Neuroscience 132 2005 453 463
30. A.S. Rice, R.H. Dworkin, T.D. McCarthy, P. Anand, C. Bountra, P.I. McCloud, J. Hill, G. Cutter, G. Kitson, N. Desem, M. Raff EMA401-003 study group 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 383 2014 1637 1647
31. G. Sandoz, J. Levitz, R.H. Kramer, and E.Y. Isacoff Optical control of endogenous proteins with a photoswitchable conditional subunit reveals a role for TREK1 in GABA(B) signaling Neuron 74 2012 1005 1014
32. F.S. Sarfo, P.J. Converse, D.V. Almeida, J. Zhang, C. Robinson, M. Wansbrough-Jones, and J.H. Grosset Microbiological, histological, immunological, and toxin response to antibiotic treatment in the mouse model of Mycobacterium ulcerans disease PLoS Negl. Trop. Dis. 7 2013 e2101
33. N. Scherr, P. Gersbach, J.P. Dangy, C. Bomio, J. Li, K.H. Altmann, and G. Pluschke Structure-activity relationship studies on the macrolide exotoxin mycolactone of Mycobacterium ulcerans PLoS Negl. Trop. Dis. 7 2013 e2143
34. R.E. Simmonds, F.V. Lali, T. Smallie, P.L. Small, and B.M. Foxwell Mycolactone inhibits monocyte cytokine production by a posttranscriptional mechanism J. Immunol. 182 2009 2194 2202
35. V. Sizaire, F. Nackers, E. Comte, and F. Portaels Mycobacterium ulcerans infection: control, diagnosis, and treatment Lancet Infect. Dis. 6 2006 288 296
36. 2R) antagonists as novel analgesics for neuropathic pain: comparative pharmacokinetics, radioligand binding, and efficacy in rats Pain Med. 14 2013 692 705
37. C. Sumners, and C.H. Gelband Neuronal ion channel signalling pathways: modulation by angiotensin II Cell. Signal. 10 1998 303 311
38. I. Szelenyi Flupirtine, a re-discovered drug, revisited Inflamm. Res. 62 2013 251 258
39. N.J. Tobias, T. Seemann, S.J. Pidot, J.L. Porter, L. Marsollier, E. Marion, F. Letournel, T. Zakir, J. Azuolas, and J.R. Wallace et al. Mycolactone gene expression is controlled by strong SigA-like promoters with utility in studies of Mycobacterium ulcerans and buruli ulcer PLoS Negl. Trop. Dis. 3 2009 e553
40. E. Torrado, A.G. Fraga, E. Logarinho, T.G. Martins, J.A. Carmona, J.B. Gama, M.A. Carvalho, F. Proença, A.G. Castro, and J. Pedrosa IFN-gamma-dependent activation of macrophages during experimental infections by Mycobacterium ulcerans is impaired by the toxin mycolactone J. Immunol. 184 2010 947 955
41. M. Wansbrough-Jones, and R. Phillips Buruli ulcer: emerging from obscurity Lancet 367 2006 1849 1858
42. F.M. Williams, S. Scollen, D. Cao, Y. Memari, C.L. Hyde, B. Zhang, B. Sidders, D. Ziemek, Y. Shi, and J. Harris et al. Genes contributing to pain sensitivity in the normal population: an exome sequencing study PLoS Genet. 8 2012 e1003095
43. E.D. Foucher, S. Blanchard, L. Preisser, E. Garo, N. Ifrah, P. Guardiola, Y. Delneste, and P. Jeannin IL-34 induces the differentiation of human monocytes into immunosuppressive macrophages. antagonistic effects of GM-CSF and IFNγ PLoS ONE 8 2013 e56045
44. 2 receptor antibodies are nonspecific PLoS ONE 8 2013 e69234
45. E. Marion, S. Prado, C. Cano, J. Babonneau, S. Ghamrawi, and L. Marsollier Photodegradation of the Mycobacterium ulcerans toxin, mycolactones: considerations for handling and storage PLoS ONE 7 2012 e33600
46. C.C. Shepard, and D.H. McRae A method for counting acid-fast bacteria Int. J. Lepr. Other Mycobact. Dis. 36 1968 78 82