TNF-α/TNFR1 Signaling Is Required for the Development and Function of Primary Nociceptors

Neuron

Volumn 82, Issue 3, 2014, Pages 587-602

  Wheeler, Michael A ^a   Heffner, Danielle L ^a   Kim, Suemin ^a   Espy, Sarah M ^a   Spano, Anthony J ^a   Cleland, Corey L ^b   Deppmann, Christopher D ^a,c,d  

^a UNIVERSITY OF VIRGINIA   (United States)

^b JAMES MADISON UNIVERSITY   (United States)

^c UNIVERSITY OF VIRGINIA   (United States)

^d University of Virginia   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; NERVE GROWTH FACTOR; PERIPHERIN; PROTEIN RET; PROTEIN TYROSINE KINASE A; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL SURVIVAL; CELLULAR DISTRIBUTION; CONNECTOME; CONTROLLED STUDY; DOWN REGULATION; GENE DELETION; GENE INACTIVATION; GENETIC ASSOCIATION; HETEROZYGOSITY; INTRACELLULAR SIGNALING; MECHANICAL STIMULATION; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MOUSE; NERVE CELL DIFFERENTIATION; NERVE EXCITABILITY; NERVE FIBER GROWTH; NERVE PROJECTION; NERVOUS SYSTEM DEVELOPMENT; NEUROMODULATION; NGF GENE; NOCIRECEPTOR FORMATION; NONHUMAN; NONPEPTIDERGIC NOCICEPTOR; PAIN RECEPTOR; PAIN THRESHOLD; PEPTIDERGIC NOCICEPTOR; PHENOTYPE; PHYSICAL SENSITIVITY; PRIMARY NOCIRECEPTOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SKIN NERVE; SPINAL CORD DORSAL HORN; SPINAL GANGLION; THERMAL STIMULATION; TNFR1 GENE; UPREGULATION;

ANIMALS; CELL SURVIVAL; CELLS, CULTURED; DOWN-REGULATION; MICE; MICE, 129 STRAIN; MICE, KNOCKOUT; NEURONS; NOCICEPTORS; PAIN MEASUREMENT; PROTO-ONCOGENE PROTEINS C-RET; RECEPTOR, TRKA; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE I; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION;

EID: 84899797895     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2014.04.009     Document Type: Article

References (73)

1. Abraira V.E., Ginty D.D. The sensory neurons of touch. Neuron 2013, 79:618-639.
2. Airaksinen M.S., Saarma M. The GDNF family: signalling, biological functions and therapeutic value. Nat. Rev. Neurosci. 2002, 3:383-394.
3. Aloe L., Mugnaini E., Levi-Montalcini R. Light and electron microscopic studies on the excessive growth of sympathetic ganglia in rats injected daily from birth with 6-OHDA and NGF. Arch. Ital. Biol. 1975, 113:326-353.
4. Bandell M., Story G.M., Hwang S.W., Viswanath V., Eid S.R., Petrus M.J., Earley T.J., Patapoutian A. Noxious cold ion channel TRPA1 is activated by pungent compounds and bradykinin. Neuron 2004, 41:849-857.
5. Barker V., Middleton G., Davey F., Davies A.M. TNFalpha contributes to the death of NGF-dependent neurons during development. Nat. Neurosci. 2001, 4:1194-1198.
6. Basbaum A.I., Bautista D.M., Scherrer G., Julius D. Cellular and molecular mechanisms of pain. Cell 2009, 139:267-284.
7. Bergmann I., Priestley J.V., McMahon S.B., Bröcker E.B., Toyka K.V., Koltzenburg M. Analysis of cutaneous sensory neurons in transgenic mice lacking the low affinity neurotrophin receptor p75. Eur. J. Neurosci. 1997, 9:18-28.
8. Brennan C., Rivas-Plata K., Landis S.C. The p75 neurotrophin receptor influences NT-3 responsiveness of sympathetic neurons invivo. Nat. Neurosci. 1999, 2:699-705.
9. Caterina M.J., Schumacher M.A., Tominaga M., Rosen T.A., Levine J.D., Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 1997, 389:816-824.
10. Chen A.I., de Nooij J.C., Jessell T.M. Graded activity of transcription factor Runx3 specifies the laminar termination pattern of sensory axons in the developing spinal cord. Neuron 2006, 49:395-408.
11. Chen C.L., Broom D.C., Liu Y., de Nooij J.C., Li Z., Cen C., Samad O.A., Jessell T.M., Woolf C.J., Ma Q. Runx1 determines nociceptive sensory neuron phenotype and is required for thermal and neuropathic pain. Neuron 2006, 49:365-377.
12. 2-mediated inhibition. Nature 2001, 411:957-962.
13. Clapham D.E. TRP channels as cellular sensors. Nature 2003, 426:517-524.
14. Costigan M., Scholz J., Woolf C.J. Neuropathic pain: a maladaptive response of the nervous system to damage. Annu. Rev. Neurosci. 2009, 32:1-32.
15. Craig A.D.B. Pain mechanisms: labeled lines versus convergence in central processing. Annu. Rev. Neurosci. 2003, 26:1-30.
16. Crowley C., Spencer S.D., Nishimura M.C., Chen K.S., Pitts-Meek S., Armanini M.P., Ling L.H., McMahon S.B., Shelton D.L., Levinson A.D., et al. Mice lacking nerve growth factor display perinatal loss of sensory and sympathetic neurons yet develop basal forebrain cholinergic neurons. Cell 1994, 76:1001-1011.
17. Davies A.M., Lee K.F., Jaenisch R. p75-deficient trigeminal sensory neurons have an altered response to NGF but not to other neurotrophins. Neuron 1993, 11:565-574.
18. Deppmann C.D., Janes K. Cytokine-cytokine crosstalk and cell-death decisions. Systems Biology of Apoptosis 2013, 163-180. Springer Publishers, New York. I.N. Lavrik (Ed.).
19. Deppmann C.D., Mihalas S., Sharma N., Lonze B.E., Niebur E., Ginty D.D. A model for neuronal competition during development. Science 2008, 320:369-373.
20. Dong X., Han S., Zylka M.J., Simon M.I., Anderson D.J. A diverse family of GPCRs expressed in specific subsets of nociceptive sensory neurons. Cell 2001, 106:619-632.
21. Gascon E., Gaillard S., Malapert P., Liu Y., Rodat-Despoix L., Samokhvalov I.M., Delmas P., Helmbacher F., Maina F., Moqrich A. Hepatocyte growth factor-Met signaling is required for Runx1 extinction and peptidergic differentiation in primary nociceptive neurons. J.Neurosci. 2010, 30:12414-12423.
22. Gerevich Z., Borvendeg S.J., Schröder W., Franke H., Wirkner K., Nörenberg W., Fürst S., Gillen C., Illes P. Inhibition of N-type voltage-activated calcium channels in rat dorsal root ganglion neurons by P2Y receptors is a possible mechanism of ADP-induced analgesia. J.Neurosci. 2004, 24:797-807.
23. Glebova N.O., Ginty D.D. Heterogeneous requirement of NGF for sympathetic target innervation invivo. J.Neurosci. 2004, 24:743-751.
24. Guo T., Mandai K., Condie B.G., Wickramasinghe S.R., Capecchi M.R., Ginty D.D. An evolving NGF-Hoxd1 signaling pathway mediates development of divergent neural circuits in vertebrates. Nat. Neurosci. 2011, 14:31-36.
25. Hefti F.F., Rosenthal A., Walicke P.A., Wyatt S., Vergara G., Shelton D.L., Davies A.M. Novel class of pain drugs based on antagonism of NGF. Trends Pharmacol. Sci. 2006, 27:85-91.
26. Hunt S.P., Mantyh P.W. The molecular dynamics of pain control. Nat. Rev. Neurosci. 2001, 2:83-91.
27. Indo Y., Tsuruta M., Hayashida Y., Karim M.A., Ohta K., Kawano T., Mitsubuchi H., Tonoki H., Awaya Y., Matsuda I. Mutations in the TRKA/NGF receptor gene in patients with congenital insensitivity to pain with anhidrosis. Nat. Genet. 1996, 13:485-488.
28. Ji R.R., Samad T.A., Jin S.X., Schmoll R., Woolf C.J. p38 MAPK activation by NGF in primary sensory neurons after inflammation increases TRPV1 levels and maintains heat hyperalgesia. Neuron 2002, 36:57-68.
29. Julius D., Basbaum A.I. Molecular mechanisms of nociception. Nature 2001, 413:203-210.
30. Kaplan D.R., Miller F.D. Neurotrophin signal transduction in the nervous system. Curr. Opin. Neurobiol. 2000, 10:381-391.
31. Kisiswa L., Osório C., Erice C., Vizard T., Wyatt S., Davies A.M. TNFα reverse signaling promotes sympathetic axon growth and target innervation. Nat. Neurosci. 2013, 16:865-873.
32. Kommaddi R.P., Thomas R., Ceni C., Daigneault K., Barker P.A. Trk-dependent ADAM17 activation facilitates neurotrophin survival signaling. FASEB J. 2011, 25:2061-2070.
33. Lallemend F., Ernfors P. Molecular interactions underlying the specification of sensory neurons. Trends Neurosci. 2012, 35:373-381.
34. Lane N.E., Schnitzer T.J., Birbara C.A., Mokhtarani M., Shelton D.L., Smith M.D., Brown M.T. Tanezumab for the treatment of pain from osteoarthritis of the knee. N.Engl. J. Med. 2010, 363:1521-1531.
35. Lee K.F., Li E., Huber L.J., Landis S.C., Sharpe A.H., Chao M.V., Jaenisch R. Targeted mutation of the gene encoding the low affinity NGF receptor p75 leads to deficits in the peripheral sensory nervous system. Cell 1992, 69:737-749.
36. Lee K.F., Davies A.M., Jaenisch R. p75-deficient embryonic dorsal root sensory and neonatal sympathetic neurons display a decreased sensitivity to NGF. Development 1994, 120:1027-1033.
37. Lewin G.R., Ritter A.M., Mendell L.M. Nerve growth factor-induced hyperalgesia in the neonatal and adult rat. J.Neurosci. 1993, 13:2136-2148.
38. Li L., Rutlin M., Abraira V.E., Cassidy C., Kus L., Gong S., Jankowski M.P., Luo W., Heintz N., Koerber H.R., et al. The functional organization of cutaneous low-threshold mechanosensory neurons. Cell 2011, 147:1615-1627.
39. Lindfors P.H., Võikar V., Rossi J., Airaksinen M.S. Deficient nonpeptidergic epidermis innervation and reduced inflammatory pain in glial cell line-derived neurotrophic factor family receptor α2 knock-out mice. J.Neurosci. 2006, 26:1953-1960.
40. Liu Y., Ma Q. Generation of somatic sensory neuron diversity and implications on sensory coding. Curr. Opin. Neurobiol. 2011, 21:52-60.
41. Liu Q., Tang Z., Surdenikova L., Kim S., Patel K.N., Kim A., Ru F., Guan Y., Weng H.J., Geng Y., et al. Sensory neuron-specific GPCR Mrgprs are itch receptors mediating chloroquine-induced pruritus. Cell 2009, 139:1353-1365.
42. Locksley R.M., Killeen N., Lenardo M.J. The TNF and TNF receptor superfamilies: integrating mammalian biology. Cell 2001, 104:487-501.
43. Luo W., Wickramasinghe S.R., Savitt J.M., Griffin J.W., Dawson T.M., Ginty D.D. A hierarchical NGF signaling cascade controls Ret-dependent and Ret-independent events during development of nonpeptidergic DRG neurons. Neuron 2007, 54:739-754.
44. Luther J.A., Birren S.J. p75 and TrkA signaling regulates sympathetic neuronal firing patterns via differential modulation of voltage-gated currents. J.Neurosci. 2009, 29:5411-5424.
45. Mantyh P.W., Koltzenburg M., Mendell L.M., Tive L., Shelton D.L. Antagonism of nerve growth factor-TrkA signaling and the relief of pain. Anesthesiology 2011, 115:189-204.
46. Maricich S.M., Wellnitz S.A., Nelson A.M., Lesniak D.R., Gerling G.J., Lumpkin E.A., Zoghbi H.Y. Merkel cells are essential for light-touch responses. Science 2009, 324:1580-1582.
47. Marmigère F., Ernfors P. Specification and connectivity of neuronal subtypes in the sensory lineage. Nat. Rev. Neurosci. 2007, 8:114-127.
48. Molliver D.C., Wright D.E., Leitner M.L., Parsadanian A.S., Doster K., Wen D., Yan Q., Snider W.D. IB4-binding DRG neurons switch from NGF to GDNF dependence in early postnatal life. Neuron 1997, 19:849-861.
49. Moran M.M., McAlexander M.A., Bíró T., Szallasi A. Transient receptor potential channels as therapeutic targets. Nat. Rev. Drug Discov. 2011, 10:601-620.
50. Newbern J.M., Li X., Shoemaker S.E., Zhou J., Zhong J., Wu Y., Bonder D., Hollenback S., Coppola G., Geschwind D.H., et al. Specific functions for ERK/MAPK signaling during PNS development. Neuron 2011, 69:91-105.
51. Nikolaev A., McLaughlin T., O'Leary D.D., Tessier-Lavigne M. APP binds DR6 to trigger axon pruning and neuron death via distinct caspases. Nature 2009, 457:981-989.
52. Ozen S., Bilginer Y. A clinical guide to autoinflammatory diseases: familial Mediterranean fever and next-of-kin. Nat. Rev. Rheumatol. 2014, 10:135-147.
53. Patel T.D., Jackman A., Rice F.L., Kucera J., Snider W.D. Development of sensory neurons in the absence of NGF/TrkA signaling invivo. Neuron 2000, 25:345-357.
54. Peier A.M., Moqrich A., Hergarden A.C., Reeve A.J., Andersson D.A., Story G.M., Earley T.J., Dragoni I., McIntyre P., Bevan S., Patapoutian A. A TRP channel that senses cold stimuli and menthol. Cell 2002, 108:705-715.
55. Pezet S., McMahon S.B. Neurotrophins: mediators and modulators of pain. Annu. Rev. Neurosci. 2006, 29:507-538.
56. Sandkühler J. Models and mechanisms of hyperalgesia and allodynia. Physiol. Rev. 2009, 89:707-758.
57. Sharma N., Deppmann C.D., Harrington A.W., St Hillaire C., Chen Z.Y., Lee F.S., Ginty D.D. Long-distance control of synapse assembly by target-derived NGF. Neuron 2010, 67:422-434.
58. Silos-Santiago I., Molliver D.C., Ozaki S., Smeyne R.J., Fagan A.M., Barbacid M., Snider W.D. Non-TrkA-expressing small DRG neurons are lost in TrkA deficient mice. J.Neurosci. 1995, 15:5929-5942.
59. Singh K.K., Park K.J., Hong E.J., Kramer B.M., Greenberg M.E., Kaplan D.R., Miller F.D. Developmental axon pruning mediated by BDNF-p75NTR-dependent axon degeneration. Nat. Neurosci. 2008, 11:649-658.
60. Smelter E., Hochberg M.C. New treatments for osteoarthritis. Curr. Opin. Rheumatol. 2013, 25:310-316.
61. Steinberg G.R., Michell B.J., van Denderen B.J., Watt M.J., Carey A.L., Fam B.C., Andrikopoulos S., Proietto J., Görgün C.Z., Carling D., et al. Tumor necrosis factor alpha-induced skeletal muscle insulin resistance involves suppression of AMP-kinase signaling. Cell Metab. 2006, 4:465-474.
62. 4)-positive and -negative nociceptors are functionally distinct. J.Neurosci. 1999, 19:6497-6505.
63. Sun M., Fink P.J. A new class of reverse signaling costimulators belongs to the TNF family. J.Immunol. 2007, 179:4307-4312.
64. Suo D., Park J., Harrington A.W., Zweifel L.S., Mihalas S., Deppmann C.D. Coronin-1 is a neurotrophin endosomal effector that is required for developmental competition for survival. Nat. Neurosci. 2014, 17:36-45.
65. Verhoeven K., Timmerman V., Mauko B., Pieber T.R., De Jonghe P., Auer-Grumbach M. Recent advances in hereditary sensory and autonomic neuropathies. Curr. Opin. Neurol. 2006, 19:474-480.
66. Vrontou S., Wong A.M., Rau K.K., Koerber H.R., Anderson D.J. Genetic identification of C fibres that detect massage-like stroking of hairy skin invivo. Nature 2013, 493:669-673.
67. Wang T., Jing X., DeBerry J.J., Schwartz E.S., Molliver D.C., Albers K.M., Davis B.M. Neurturin overexpression in skin enhances expression of TRPM8 in cutaneous sensory neurons and leads to behavioral sensitivity to cool and menthol. J.Neurosci. 2013, 33:2060-2070.
68. Wende H., Lechner S.G., Cheret C., Bourane S., Kolanczyk M.E., Pattyn A., Reuter K., Munier F.L., Carroll P., Lewin G.R., Birchmeier C. The transcription factor c-Maf controls touch receptor development and function. Science 2012, 335:1373-1376.
69. Woolf C.J., Salter M.W. Neuronal plasticity: increasing the gain in pain. Science 2000, 288:1765-1769.
70. Yeo T.T., Chua-Couzens J., Butcher L.L., Bredesen D.E., Cooper J.D., Valletta J.S., Mobley W.C., Longo F.M. Absence of p75NTR causes increased basal forebrain cholinergic neuron size, choline acetyltransferase activity, and target innervation. J.Neurosci. 1997, 17:7594-7605.
71. Zhang X., Huang J., McNaughton P.A. NGF rapidly increases membrane expression of TRPV1 heat-gated ion channels. EMBO J. 2005, 24:4211-4223.
72. Zhong J., Li X., McNamee C., Chen A.P., Baccarini M., Snider W.D. Raf kinase signaling functions in sensory neuron differentiation and axon growth invivo. Nat. Neurosci. 2007, 10:598-607.
73. Zylka M.J., Rice F.L., Anderson D.J. Topographically distinct epidermal nociceptive circuits revealed by axonal tracers targeted to Mrgprd. Neuron 2005, 45:17-25.