Wnt-fzd signaling sensitizes peripheral sensory neurons via distinct noncanonical pathways

Neuron

Volumn 83, Issue 1, 2014, Pages 104-121

  Simonetti, Manuela ^a,f   Agarwal, Nitin ^a   Stösser, Sebastian ^a   Bali, Kiran Kumar ^a,f   Karaulanov, Emil ^b   Kamble, Rashmi ^a   Pospisilova, Blanka ^a   Kurejova, Martina ^a   Birchmeier, Walter ^c   Niehrs, Christof ^b,d   Heppenstall, Paul ^e,f   Kuner, Rohini ^a,f  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b INSTITUTE OF MOLECULAR BIOLOGY IMB   (Germany)

^c MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^d GERMAN CANCER RESEARCH CENTER   (Germany)

^e EUROPEAN MOLECULAR BIOLOGY LABORATORY EMBL   (Italy)

^f Otto Meyerhof Centre   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; CALCIUM; FRIZZLED PROTEIN; PURINERGIC P2X3 RECEPTOR; TRANSIENT RECEPTOR POTENTIAL CHANNEL A1; WNT3A PROTEIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CALCIUM SIGNALING; CANCER PAIN; CELL FATE; CELL POLARITY; CONTROLLED STUDY; FZD SIGNALING PATHWAY; HYPERALGESIA; HYPERSENSITIVITY; IN VIVO STUDY; INTRACELLULAR SIGNALING; MEMBRANE TRANSPORT; MOUSE; NEUROMODULATION; NOCICEPTION; NONCANONICAL PATHWAY; NONHUMAN; PATHOPHYSIOLOGY; PERIPHERAL NERVE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; REGULATOR GENE; SENSITIZATION; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; SPINAL GANGLION; THERMOREGULATION; WNT SIGNALING PATHWAY;

ANIMALS; CELLS, CULTURED; FRIZZLED RECEPTORS; GANGLIA, SPINAL; HEK293 CELLS; HUMANS; HYPERALGESIA; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; PERIPHERAL NERVES; SENSORY RECEPTOR CELLS; WNT SIGNALING PATHWAY; WNT3A PROTEIN;

EID: 84903596753     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2014.05.037     Document Type: Article

References (32)

1. Agarwal N., Offermanns S., Kuner R. Conditional gene deletion in primary nociceptive neurons of trigeminal ganglia and dorsal root ganglia. Genesis 2004, 38:122-129.
2. Alfaro M.P., Pagni M., Vincent A., Atkinson J., Hill M.F., Cates J., Davidson J.M., Rottman J., Lee E., Young P.P. The Wnt modulator sFRP2 enhances mesenchymal stem cell engraftment, granulation tissue formation and myocardial repair. Proc. Natl. Acad. Sci. USA 2008, 105:18366-18371.
3. Basbaum A.I., Bautista D.M., Scherrer G., Julius D. Cellular and molecular mechanisms of pain. Cell 2009, 139:267-284.
4. Budnik V., Salinas P.C. Wnt signaling during synaptic development and plasticity. Curr. Opin. Neurobiol. 2011, 21:151-159.
5. Cain D.M., Wacnik P.W., Turner M., Wendelschafer-Crabb G., Kennedy W.R., Wilcox G.L., Simone D.A. Functional interactions between tumor and peripheral nerve: changes in excitability and morphology of primary afferent fibers in a murine model of cancer pain. J.Neurosci. 2001, 21:9367-9376.
6. Cavanaugh D.J., Lee H., Lo L., Shields S.D., Zylka M.J., Basbaum A.I., Anderson D.J. Distinct subsets of unmyelinated primary sensory fibers mediate behavioral responses to noxious thermal and mechanical stimuli. Proc. Natl. Acad. Sci. USA 2009, 106:9075-9080.
7. Durand J., Lampron A., Mazzuco T.L., Chapman A., Bourdeau I. Characterization of differential gene expression in adrenocortical tumors harboring beta-catenin (CTNNB1) mutations. J.Clin. Endocrinol. Metab. 2011, 96:E1206-E1211.
8. Fodde R., Brabletz T. Wnt/beta-catenin signaling in cancer stemness and malignant behavior. Curr. Opin. Cell Biol. 2007, 19:150-158.
9. Glinka A., Wu W., Delius H., Monaghan A.P., Blumenstock C., Niehrs C. Dickkopf-1 is a member of a new family of secreted proteins and functions in head induction. Nature 1998, 391:357-362.
10. Grigoryan T., Wend P., Klaus A., Birchmeier W. Deciphering the function of canonical Wnt signals in development and disease: conditional loss- and gain-of-function mutations of beta-catenin in mice. Genes Dev. 2008, 22:2308-2341.
11. Hartmann B., Ahmadi S., Heppenstall P.A., Lewin G.R., Schott C., Borchardt T., Seeburg P.H., Zeilhofer H.U., Sprengel R., Kuner R. The AMPA receptor subunits GluR-A and GluR-B reciprocally modulate spinal synaptic plasticity and inflammatory pain. Neuron 2004, 44:637-650.
12. Huelsken J., Vogel R., Erdmann B., Cotsarelis G., Birchmeier W. beta-Catenin controls hair follicle morphogenesis and stem cell differentiation in the skin. Cell 2001, 105:533-545.
13. Ishitani T., Kishida S., Hyodo-Miura J., Ueno N., Yasuda J., Waterman M., Shibuya H., Moon R.T., Ninomiya-Tsuji J., Matsumoto K. The TAK1-NLK mitogen-activated protein kinase cascade functions in the Wnt-5a/Ca(2+) pathway to antagonize Wnt/beta-catenin signaling. Mol. Cell. Biol. 2003, 23:131-139.
14. Kaan T.K., Yip P.K., Patel S., Davies M., Marchand F., Cockayne D.A., Nunn P.A., Dickenson A.H., Ford A.P., Zhong Y., et al. Systemic blockade of P2X3 and P2X2/3 receptors attenuates bone cancer pain behaviour in rats. Brain 2010, 133:2549-2564.
15. Kawano Y., Kypta R. Secreted antagonists of the Wnt signalling pathway. J.Cell Sci. 2003, 116:2627-2634.
16. Koltzenburg M., Stucky C.L., Lewin G.R. Receptive properties of mouse sensory neurons innervating hairy skin. J.Neurophysiol. 1997, 78:1841-1850.
17. Komekado H., Yamamoto H., Chiba T., Kikuchi A. Glycosylation and palmitoylation of Wnt-3a are coupled to produce an active form of Wnt-3a. Genes Cells 2007, 12:521-534.
18. Komiya Y., Habas R. Wnt signal transduction pathways. Organogenesis 2008, 4:68-75.
19. MacDonald B.T., Tamai K., He X. Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev. Cell 2009, 17:9-26.
20. Maretto S., Cordenonsi M., Dupont S., Braghetta P., Broccoli V., Hassan A.B., Volpin D., Bressan G.M., Piccolo S. Mapping Wnt/beta-catenin signaling during mouse development and in colorectal tumors. Proc. Natl. Acad. Sci. USA 2003, 100:3299-3304.
21. Mikels A.J., Nusse R. Purified Wnt5a protein activates or inhibitsbeta-catenin-TCF signaling depending on receptor context. PLoS Biol. 2006, 4:e115.
22. Niehrs C. Function and biological roles of the Dickkopf family of Wnt modulators. Oncogene 2006, 25:7469-7481.
23. Patapoutian A., Reichardt L.F. Roles of Wnt proteins in neural development and maintenance. Curr. Opin. Neurobiol. 2000, 10:392-399.
24. Petrus M., Peier A.M., Bandell M., Hwang S.W., Huynh T., Olney N., Jegla T., Patapoutian A. A role of TRPA1 in mechanical hyperalgesia is revealed by pharmacological inhibition. Mol. Pain 2007, 3:40.
25. Schweizerhof M., Stösser S., Kurejova M., Njoo C., Gangadharan V., Agarwal N., Schmelz M., Bali K.K., Michalski C.W., Brugger S., et al. Hematopoietic colony-stimulating factors mediate tumor-nerve interactions and bone cancer pain. Nat. Med. 2009, 15:802-807.
26. Shan J., Shi D.L., Wang J., Zheng J. Identification of a specific inhibitor of the dishevelled PDZ domain. Biochemistry 2005, 44:15495-15503.
27. Stösser S., Agarwal N., Tappe-Theodor A., Yanagisawa M., Kuner R. Dissecting the functional significance of endothelin A receptors in peripheral nociceptors invivo via conditional gene deletion. Pain 2010, 148:206-214.
28. Tsuda M., Koizumi S., Kita A., Shigemoto Y., Ueno S., Inoue K. Mechanical allodynia caused by intraplantar injection of P2X receptor agonist in rats: involvement of heteromeric P2X2/3 receptor signaling in capsaicin-insensitive primary afferent neurons. J.Neurosci. 2000, 20:RC90.
29. Yuan S., Shi Y., Tang S.J. Wnt signaling in the pathogenesis of multiple sclerosis-associated chronic pain. J.Neuroimmune Pharmacol. 2012, 7:904-913. 10.1007/s11481-012-9370-3.
30. Zhang X., Huang J., McNaughton P.A. NGF rapidly increases membrane expression of TRPV1 heat-gated ion channels. EMBO J. 2005, 24:4211-4223.
31. Zhang Y.K., Huang Z.J., Liu S., Liu Y.P., Song A.A., Song X.J. WNT signaling underlies the pathogenesis of neuropathic pain in rodents. J.Clin. Invest. 2013, 123:2268-2286.
32. Zurborg S., Piszczek A., Martínez C., Hublitz P., Al Banchaabouchi M., Moreira P., Perlas E., Heppenstall P.A. Generation and characterization of an Advillin-Cre driver mouse line. Mol. Pain 2011, 7:66.