Nogo receptor homolog NgR2 expressed in sensory DRG neurons controls epidermal innervation by interaction with Versican

Journal of Neuroscience

Volumn 34, Issue 5, 2014, Pages 1633-1646

  Bäumer, Bastian E ^a   Kurz, Antje ^a   Borrie, Sarah C ^a   Sickinger, Stephan ^a   Dours Zimmermann, María T ^b   Zimmermann, Dieter R ^b   Bandtlow, Christine E ^a  

^a INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^b UNIVERSITY HOSPITAL ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

NOGO 66 RECEPTOR; NOGO RECEPTOR 2; UNCLASSIFIED DRUG; VERSICAN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COLD PLATE TEST; CONFOCAL MICROSCOPY; CONTROLLED STUDY; EPIFLUORESCENCE MICROSCOPY; HOT PLATE TEST; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; IN SITU HYBRIDIZATION; MALE; MOUSE; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; RANDALL-SELITTO TEST; REAL TIME POLYMERASE CHAIN REACTION; SKIN NERVE; SPECTROPHOTOMETRY; SPINAL GANGLION; WESTERN BLOTTING;

ANIMALS; ANIMALS, NEWBORN; CALCITONIN GENE-RELATED PEPTIDE; CHO CELLS; CRICETULUS; EPIDERMIS; F-BOX PROTEINS; GANGLIA, SPINAL; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLYCOPROTEINS; HYPERALGESIA; MICE; MICE, KNOCKOUT; NEUROFILAMENT PROTEINS; NOCICEPTORS; PAIN THRESHOLD; PHYSICAL STIMULATION; PROTEIN BINDING; RECEPTORS, CELL SURFACE; RECEPTORS, PURINERGIC P2X; SENSORY RECEPTOR CELLS; TRPV CATION CHANNELS; TUBULIN; VERSICANS;

EID: 84893108349     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3094-13.2014     Document Type: Article

References (64)

1. Albers KM, Woodbury CJ, Ritter AM, Davis BM, Koerber HR (2006) Glial cell-line-derived neurotrophic factor expression in skin alters the mechanical sensitivity of cutaneous nociceptors. J Neurosci 26: 2981-2990. CrossRef Medline
2. Bandtlow CE, Zimmermann DR (2000) Proteoglycans in the developing brain: new conceptual insights for old proteins. Physiol Rev 80: 1267-1290. Medline
3. Banerjee B, Medda BK, Schmidt J, Zheng Y, Zhang Z, Shaker R, Sengupta JN (2009) Altered expression of P2X3 in vagal and spinal afferents following esophagitis in rats. Histochem Cell Biol 132: 585-597. CrossRef Medline
4. Basbaum AI, Bautista DM, Scherrer G, Julius D (2009) Cellular and molecular mechanisms of pain. Cell 139: 267-284. CrossRef Medline
5. Bautista DM, Siemens J, Glazer JM, Tsuruda PR, Basbaum AI, Stucky CL, Jordt SE, Julius D (2007) The menthol receptor TRPM8 is the principal detector of environmental cold. Nature 448: 204-208. CrossRef Medline
6. Bogen O, Joseph EK, Chen X, Levine JD (2008) GDNF hyperalgesia is mediated by PLCgamma, MAPK/ERK, PI3K, CDK5 and Src family kinase signaling and dependent on the IB4-binding protein versican. Eur J Neurosci 28: 12-19. CrossRef Medline
7. Borisoff JF, Chan CC, Hiebert GW, Oschipok L, Robertson GS, Zamboni R, Steeves JD, Tetzlaff W (2003) Suppression of Rho-kinase activity promotes axonal growth on inhibitory CNS substrates. Mol Cell Neurosci 22: 405-416. CrossRef Medline
8. Bourane S, Méchaly I, Venteo S, Garces A, Fichard A, Valmier J, Carroll P (2007) A SAGE-based screen for genes expressed in sub-populations of neurons in the mouse dorsal root ganglion. BMCNeurosci 8: 97. CrossRef Medline
9. Chiang LY, Poole K, Oliveira BE, Duarte N, Sierra YA, Bruckner-Tuderman L, Koch M, Hu J, Lewin GR (2011) Laminin-332 coordinates mechanotransduction and growth cone bifurcation in sensory neurons. Nat Neurosci 14: 993-1000. CrossRef Medline
10. Colburn RW, Lubin ML, Stone DJ Jr, Wang Y, Lawrence D, D'Andrea MR, Brandt MR, Liu Y, Flores CM, Qin N (2007) Attenuated cold sensitivity in TRPM8 null mice. Neuron 54: 379-386. CrossRef Medline
11. da Costa DS, Meotti FC, Andrade EL, Leal PC, Motta EM, Calixto JB (2010) The involvement of the transient receptor potential A1 (TRPA1) in the maintenance of mechanical and cold hyperalgesia in persistent inflammation. Pain 148: 431-437. CrossRef Medline
12. Dickendesher TL, Baldwin KT, Mironova YA, Koriyama Y, Raiker SJ, Askew KL, Wood A, Geoffroy CG, Zheng B, Liepmann CD, Katagiri Y, Benowitz LI, Geller HM, Giger RJ (2012) NgR1 and NgR3 are receptors for chondroitin sulfate proteoglycans. Nat Neurosci 15: 703-712. CrossRef Medline
13. Dours-Zimmermann MT, Zimmermann DR (1994) A novel glycosaminoglycan attachment domain identified in two alternative splice variants of human versican. J Biol Chem 269: 32992-32998. Medline
14. Dours-Zimmermann MT, Maurer K, Rauch U, Stoffel W, Fässler R, Zimmermann DR (2009) Versican V2 assembles the extracellular matrix surrounding the nodes of ranvier in the CNS. J Neurosci 29: 7731-7742. CrossRef Medline
15. Duggan A, Garcia-Anoveros J, Corey DP (2002) The PDZ domain protein PICK1 and the sodium channel BNaC1 interact and localize at mechanosensory terminals of dorsal root ganglion neurons and dendrites of central neurons. J Biol Chem 277: 5203-5208. CrossRef Medline
16. Dutt S, Kléber M, Matasci M, Sommer L, Zimmermann DR (2006) Versican V0 and V1 guide migratory neural crest cells. J Biol Chem 281: 12123-12131. CrossRef Medline
17. Dutt S, Cassoly E, Dours-Zimmermann MT, Matasci M, Stoeckli ET, Zimmermann DR (2011) Versican V0 and V1 direct the growth of peripheral axons in the developing chick hindlimb. J Neurosci 31: 5262-5270. CrossRef Medline
18. Fisher D, Xing B, Dill J, Li H, Hoang HH, Zhao Z, Yang XL, Bachoo R, Cannon S, Longo FM, Sheng M, Silver J, Li S (2011) Leukocyte common antigen-related phosphatase is a functional receptor for chondroitin sulfate proteoglycan axon growth inhibitors. J Neurosci 31: 14051-14066. CrossRef Medline
19. Fournier AE, GrandPre T, Strittmatter SM (2001) Identification of a receptor mediating Nogo-66 inhibition of axonal regeneration. Nature 409: 341-346. CrossRef Medline
20. Franck MC, Stenqvist A, Li L, Hao J, Usoskin D, Xu X, Wiesenfeld-Hallin Z, Ernfors P (2011) Essential role of Ret for defining nonpeptidergic nociceptor phenotypes and functions in the adult mouse. Eur J Neurosci 33: 1385-1400. CrossRef Medline
21. García-Añoveros J, Samad TA, Zuvela-Jelaska L, Woolf CJ, Corey DP (2001) Transport and localization of the DEG/ENaC ion channel BNaC1alpha to peripheral mechanosensory terminals of dorsal root ganglia neurons. J Neurosci 21: 2678-2686. Medline
22. Golden JP, Hoshi M, Nassar MA, Enomoto H, Wood JN, Milbrandt J, Gereau RW 4th, Johnson EM Jr, Jain S (2010) RET signaling is required for survival and normal function of nonpeptidergic nociceptors. J Neurosci 30: 3983-3994. CrossRef Medline
23. Hattori T, Chen J, Harding AM, Price MP, Lu Y, Abboud FM, Benson CJ (2009) ASIC2a and ASIC3 heteromultimerize to form pH-sensitive channels in mouse cardiac dorsal root ganglia neurons. Circ Res 105: 279-286. CrossRef Medline
24. Hsieh YL, Chiang H, Lue JH, Hsieh ST (2012) P2X3-mediated peripheral sensitization of neuropathic pain in resiniferatoxin-induced neuropathy. Exp Neurol 235: 316-325. CrossRef Medline
25. Jankowski MP, Lawson JJ, McIlwrath SL, Rau KK, Anderson CE, Albers KM, Koerber HR (2009) Sensitization of cutaneous nociceptors after nerve transection and regeneration: possible role of target-derived neurotrophic factor signaling. J Neurosci 29: 1636-1647. CrossRef Medline
26. Jankowski MP, Soneji DJ, Ekmann KM, Anderson CE, Koerber HR (2012) Dynamic changes in heat transducing channel TRPV1 expression regulate mechanically insensitive, heat sensitive C-fiber recruitment after axotomy and regeneration. J Neurosci 32: 17869-17873. CrossRef Medline
27. Kojima N, Saito H, Nishikawa M, Yuri S, Jo OD, Pham PC, Yanagawa N (2011) Lithium induces c-Ret expression in mouse inner medullary collecting duct cells. Cell Signal 23: 371-379. CrossRef Medline
28. Krylova O, Herreros J, Cleverley KE, Ehler E, Henriquez JP, Hughes SM, Salinas PC (2002) WNT-3, expressed by motoneurons, regulates terminal arborization of neurotrophin-3-responsive spinal sensory neurons. Neuron 35: 1043-1056. CrossRef Medline
29. Lagerström MC, Rogoz K, Abrahamsen B, Lind AL, Olund C, Smith C, Mendez JA, Wallén-Mackenzie A, Wood JN, Kullander K (2011) A sensory subpopulation depends on vesicular glutamate transporter 2 for mechanical pain, and together with substance P, inflammatory pain. Proc Natl Acad Sci U S A 108: 5789-5794. CrossRef Medline
30. Landolt RM, Vaughan L, Winterhalter KH, Zimmermann DR (1995) Versican is selectively expressed in embryonic tissues that act as barriers to neural crest cell migration and axon outgrowth. Development 121: 2303-2312. Medline
31. Laurén J, Airaksinen MS, Saarma M, Timmusk T (2003) Two novel mammalian nogo receptor homologs differentially expressed in the central and peripheral nervous systems. Mol Cell Neurosci 24: 581-594. CrossRef Medline
32. Lindfors PH, Vöikar V, Rossi J, Airaksinen MS (2006) Deficient nonpeptidergic epidermis innervation and reduced inflammatory pain in glial cell line-derived neurotrophic factor family receptor alpha2 knock-out mice. J Neurosci 26: 1953-1960. CrossRef Medline
33. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 (-Delta Delta C (T) Method. Methods 25: 402-408. CrossRef Medline
34. Luo W, Wickramasinghe SR, Savitt JM, Griffin JW, Dawson TM, Ginty DD (2007) AhierarchicalNGFsignaling cascade controls Ret-dependent and Ret-independent events during development of nonpeptidergic DRG neurons. Neuron 54: 739-754. CrossRef Medline
35. Ma L, Tessier-Lavigne M (2007) Dual branch-promoting and branchrepelling actions of Slit/Robo signaling on peripheral and central branches of developing sensory axons. J Neurosci 27: 6843-6851. CrossRef Medline
36. Malgouries S, Thibaut S, Bernard BA (2008) Proteoglycan expression patterns in human hair follicle. Br J Dermatol 158: 234-242. Medline
37. Marthiens V, Gavard J, Padilla F, Monnet C, Castellani V, Lambert M, Mège RM (2005) A novel function for cadherin-11 in the regulation of motor axon elongation and fasciculation. Mol Cell Neurosci 28: 715-726. CrossRef Medline
38. Mironova YA, Giger RJ (2013) Where no synapses go: gatekeepers of circuit remodeling and synaptic strength. Trends Neurosci 36: 363-373. CrossRef Medline
39. Molliver DC, Snider WD (1997) Nerve growth factor receptor TrkA is down-regulated during postnatal development by a subset of dorsal root ganglion neurons. J Comp Neurol 381: 428-438. CrossRef Medline
40. Molliver DC, Radeke MJ, Feinstein SC, Snider WD (1995) Presence or absence of TrkA protein distinguishes subsets of small sensory neurons with unique cytochemical characteristics and dorsal horn projections. J Comp Neurol 361: 404-416. CrossRef Medline
41. Moss A, Alvares D, Meredith-Middleton J, Robinson M, Slater R, Hunt SP, Fitzgerald M (2005) Ephrin-A4 inhibits sensory neurite outgrowth and is regulated by neonatal skin wounding. Eur J Neurosci 22: 2413-2421. CrossRef Medline
42. Niederöst B, Oertle T, Fritsche J, McKinney RA, Bandtlow CE (2002) Nogo-A and myelin-associated glycoprotein mediate neurite growth inhibition by antagonistic regulation of RhoA and Rac1. J Neurosci 22: 10368-10376. Medline
43. Oertle T, van der Haar ME, Bandtlow CE, Robeva A, Burfeind P, Buss A, Huber AB, Simonen M, Schnell L, Brösamle C, Kaupmann K, Vallon R, Schwab ME (2003) Nogo-A inhibits neurite outgrowth and cell spreading with three discrete regions. J Neurosci 23: 5393-5406. Medline
44. Park JB, Yiu G, Kaneko S, Wang J, Chang J, He XL, Garcia KC, He Z (2005) A TNF receptor family member, TROY, is a coreceptor with Nogo receptor in mediating the inhibitory activity of myelin inhibitors. Neuron 45: 345-351. CrossRef Medline
45. Peters EM, Botchkarev VA, Müller-Röver S, Moll I, Rice FL, Paus R (2002) Developmental timing of hair follicle and dorsal skin innervation in mice. J Comp Neurol 448: 28-52. CrossRef Medline
46. Price MP, Lewin GR, McIlwrath SL, Cheng C, Xie J, Heppenstall PA, Stucky CL, Mannsfeldt AG, Brennan TJ, Drummond HA, Qiao J, Benson CJ, Tarr DE, Hrstka RF, Yang B, Williamson RA, Welsh MJ (2000) The mammalian sodium channel BNC1 is required for normal touch sensation. Nature 407: 1007-1011. CrossRef Medline
47. Price MP, McIlwrath SL, Xie J, Cheng C, Qiao J, Tarr DE, Sluka KA, Brennan TJ, Lewin GR, Welsh MJ (2001) The DRASIC cation channel contributes to the detection of cutaneous touch and acid stimuli in mice. Neuron 32: 1071-1083. CrossRef Medline
48. Priestley JV, Michael GJ, Averill S, Liu M, Willmott N (2002) Regulation of nociceptive neurons by nerve growth factor and glial cell line derived neurotrophic factor. Can J Physiol Pharmacol 80: 495-505. CrossRef Medline
49. Schweigreiter R, Walmsley AR, Niederöst B, Zimmermann DR, Oertle T, Casademunt E, Frentzel S, Dechant G, Mir A, Bandtlow CE (2004) Versican V2 and the central inhibitory domain of Nogo-A inhibit neurite growth via p75NTR/NgR-independent pathways that converge at RhoA. Mol Cell Neurosci 27: 163-174. CrossRef Medline
50. Shen Y, Tenney AP, Busch SA, Horn KP, Cuascut FX, Liu K, He Z, Silver J, Flanagan JG (2009) PTPsigma is a receptor for chondroitin sulfate proteoglycan, an inhibitor of neural regeneration. Science 326: 592-596. CrossRef Medline
51. Sherwood TW, Lee KG, Gormley MG, Askwith CC (2011) Heteromeric acid-sensing ion channels (ASICs) composed of ASIC2b and ASIC1a display novel channel properties and contribute to acidosis-induced neuronal death. J Neurosci 31: 9723-9734. CrossRef Medline
52. Tan CL, Kwok JC, Patani R, Ffrench-Constant C, Chandran S, Fawcett JW (2011) Integrin activation promotes axon growth on inhibitory chondroitin sulfate proteoglycans by enhancing integrin signaling. J Neurosci 31: 6289-6295. CrossRef Medline
53. Tominaga M, Ogawa H, Takamori K (2008) Decreased production of semaphorin 3A in the lesional skin of atopic dermatitis. Br J Dermatol 158: 842-844. CrossRef Medline
54. Venkatesh K, Chivatakarn O, Lee H, Joshi PS, Kantor DB, Newman BA, Mage R, Rader C, Giger RJ (2005) The Nogo-66 receptor homolog NgR2 is a sialic acid-dependent receptor selective for myelin-associated glycoprotein. J Neurosci 25: 808-822. CrossRef Medline
55. Wang KC, Koprivica V, Kim JA, Sivasankaran R, Guo Y, Neve RL, He Z (2002) Oligodendrocyte-myelin glycoprotein is a Nogo receptor ligand that inhibits neurite outgrowth. Nature 417: 941-944. CrossRef Medline
56. Wang T, Jing X, DeBerry JJ, Schwartz ES, Molliver DC, Albers KM, Davis BM (2013) Neurturin overexpression in skin enhances expression of TRPM8 in cutaneous sensory neurons and leads to behavioral sensitivity to cool and menthol. J Neurosci 33: 2060-2070. CrossRef Medline
57. Wills ZP, Mandel-Brehm C, Mardinly AR, McCord AE, Giger RJ, Greenberg ME (2012) The nogo receptor family restricts synapse number in the developing hippocampus. Neuron 73: 466-481. CrossRef Medline
58. Wörter V, Schweigreiter R, Kinzel B, Mueller M, Barske C, Böck G, Frentzel S, Bandtlow CE (2009) Inhibitory activity of myelin-associated glycoprotein on sensory neurons is largely independent of NgR1 and NgR2 and resides within Ig-Like domains 4 and 5. PLoS One 4: e5218. CrossRef Medline
59. Xu GY, Shenoy M, Winston JH, Mittal S, Pasricha PJ (2008) P2X receptormediated visceral hyperalgesia in a rat model of chronic visceral hypersensitivity. Gut 57: 1230-1237. CrossRef Medline
60. Zako M, Shinomura T, Ujita M, Ito K, Kimata K (1995) Expression of PGM (V3), an alternatively spliced form of PG-M without a chondroitin sulfate attachment in region in mouse and human tissues. J Biol Chem 270: 3914-3918. CrossRef Medline
61. Zimmermann DR, Ruoslahti E (1989) Multiple domains of the large fibroblast proteoglycan, versican. EMBO J 8: 2975-2981. Medline
62. Zimmermann DR, Dours-Zimmermann MT, Schubert M, Bruckner-Tuderman L (1994) Versican is expressed in the proliferating zone in the epidermis and in association with the elastic network of the dermis. J Cell Biol 124: 817-825. CrossRef Medline
63. Zwick M, Davis BM, Woodbury CJ, Burkett JN, Koerber HR, Simpson JF, Albers KM (2002) Glial cell line-derived neurotrophic factor is a survival factor for isolectin B4-positive, but not vanilloid receptor 1-positive, neurons in the mouse. J Neurosci 22: 4057-4065. Medline
64. Zylka MJ, Rice FL, Anderson DJ (2005) Topographically distinct epidermal nociceptive circuits revealed by axonal tracers targeted to Mrgprd. Neuron 45: 17-25. CrossRef Medline