Spinal expression of Hippo signaling components YAP and TAZ following peripheral nerve injury in rats

Brain Research

Volumn 1535, Issue , 2013, Pages 137-147

  Li, Na ^a,b   Lim, Grewo ^a   Chen, Lucy ^a   McCabe, Michael F ^a   Kim, Hyangin ^a   Zhang, Shuzhuo ^a,c   Mao, Jianren ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b KUNMING GENERAL HOSPITAL   (China)

^c BEIJING INSTITUTE OF PHARMACOLOGY AND TOXICOLOGY   (China)

Author keywords

Dendrite; Dorsal horn; Hippo signaling pathway; Neuropathic pain; Proliferation; Spinal cord; Structural plasticity; Synaptic plasticity

Indexed keywords

NERVE PROTEIN; PROTEIN HIPPO; PROTEIN TAZ; PROTEIN YAP; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHRONIC CONSTRICTION SCIATIC NERVE INJURY; GLIA CELL; INFLAMMATION; MALE; NONHUMAN; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPINAL CORD DORSAL HORN; TOPOGRAPHY; UPREGULATION;

RATTUS;

DENDRITE; DORSAL HORN; HIPPO SIGNALING PATHWAY; NEUROPATHIC PAIN; PROLIFERATION; SPINAL CORD; STRUCTURAL PLASTICITY; SYNAPTIC PLASTICITY;

ANIMALS; APOPTOSIS REGULATORY PROTEINS; CALCITONIN GENE-RELATED PEPTIDE; HYPERALGESIA; LECTINS; MALE; NEURALGIA; NEURONS; PAIN MEASUREMENT; PERIPHERAL NERVE INJURIES; PROTEIN-SERINE-THREONINE KINASES; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; SPINAL CORD; TIME FACTORS; TRANSCRIPTION FACTORS; UP-REGULATION;

EID: 84884699847     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2013.08.049     Document Type: Article

References (61)

1. J.K. Alexander, G.M. Cox, J.B. Tian, A.M. Zha, P. Wei, K.A. Kigerl, M.K. Reddy, N.M. Dagia, T. Sielecki, M.X. Zhu, A.R. Satoskar, D.M. McTigue, C.C. Whitacre, and P.G. Popovich Macrophage migration inhibitory factor (MIF) is essential for inflammatory and neuropathic pain and enhances pain in response to stress Exp. Neurol. 236 2012 351 362
2. S. Averill, S.B. McMahon, D.O. Clary, L.F. Reichardt, and J.V. Priestley Immunocytochemical localization of trkA receptors in chemically identified subgroups of adult rat sensory neurons Eur. J. Neurosci. 7 1995 1484 1494
3. M. Belkouch, M.A. Dansereau, A. Reaux-Le Goazigo, J. Van Steenwinckel, N. Beaudet, A. Chraibi, S. Melik-Parsadaniantz, and P. Sarret The chemokine CCL2 increases Nav1.8 sodium channel activity in primary sensory neurons through a Gbetagamma-dependent mechanism J. Neurosci. 31 2011 18381 18390
4. G.J. Bennett, and Y.K. Xie A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man Pain 33 1988 87 107
5. J.V. Berger, L. Knaepen, S.P. Janssen, R.J. Jaken, M.A. Marcus, E.A. Joosten, and R. Deumens Cellular and molecular insights into neuropathy-induced pain hypersensitivity for mechanism-based treatment approaches Brain Res. Rev. 67 2011 282 310
6. J.C. Boggiano, and R.G. Fehon Growth control by committee: intercellular junctions, cell polarity, and the cytoskeleton regulate Hippo signaling Dev. Cell. 22 2012 695 702
7. M.J. Caterina, A. Leffler, A.B. Malmberg, W.J. Martin, J. Trafton, K.R. Petersen-Zeitz, M. Koltzenburg, A.I. Basbaum, and D. Julius Impaired nociception and pain sensation in mice lacking the capsaicin receptor Science 288 2000 306 313
8. L. Chen, P.G. Loh, and H. Song Structural and functional insights into the TEAD-YAP complex in the Hippo signaling pathway Protein and Cell 1 2010 1073 1083
9. L.J. Chen, F.G. Zhang, J. Li, H.X. Song, L.B. Zhou, B.C. Yao, F. Li, and W.C. Li Expression of calcitonin gene-related peptide in anterior and posterior horns of the spinal cord after brachial plexus injury J. Clin. Neurosci. 17 2010 87 91
10. R.E. Coggeshall, H.A. Lekan, F.A. White, and C.J. Woolf A-fiber sensory input induces neuronal cell death in the dorsal horn of the adult rat spinal cord J. Comp. Neurol. 435 2001 276 282
11. G. Cruccu, C. Sommer, P. Anand, N. Attal, R. Baron, L. Garcia-Larrea, M. Haanpaa, T.S. Jensen, J. Serra, and R.D. Treede EFNS guidelines on neuropathic pain assessment: revised 2009 Eur. J. Neurol 17 2010 1010 1018
12. M. Devor Ectopic discharge in Abeta afferents as a source of neuropathic pain Exp. Brain Res 196 2009 115 128
13. S. Echeverry, X.Q. Shi, and J. Zhang Characterization of cell proliferation in rat spinal cord following peripheral nerve injury and the relationship with neuropathic pain Pain 135 2008 37 47
14. N. Eijkelkamp, C.J. Heijnen, H.L. Willemen, R. Deumens, E.A. Joosten, W. Kleibeuker, I.J. den Hartog, C.T. van Velthoven, C. Nijboer, M.A. Nassar, G.W. Dorn 2nd, J.N. Wood, and A. Kavelaars GRK2: a novel cell-specific regulator of severity and duration of inflammatory pain J. Neurosci. 30 2010 2138 2149
15. K. Emoto, Y. He, B. Ye, W.B. Grueber, P.N. Adler, L.Y. Jan, and Y.N. Jan Control of dendritic branching and tiling by the Tricornered-kinase/Furry signaling pathway in Drosophila sensory neurons Cell 119 2004 245 256
16. K. Emoto, J.Z. Parrish, L.Y. Jan, and Y.N. Jan The tumour suppressor Hippo acts with the NDR kinases in dendritic tiling and maintenance Nature 443 2006 210 213
17. K. Emoto The growing role of the Hippo-NDR kinase signalling in neuronal development and disease J. Biochem 150 2011 133 141
18. L.A. Fernandez, P.A. Northcott, J. Dalton, C. Fraga, D. Ellison, S. Angers, M.D. Taylor, and A.M. Kenney YAP1 is amplified and up-regulated in hedgehog-associated medulloblastomas and mediates Sonic hedgehog-driven neural precursor proliferation Genes Dev. 23 2009 2729 2741
19. N.B. Finnerup, S.H. Sindrup, and T.S. Jensen The evidence for pharmacological treatment of neuropathic pain Pain 150 2010 573 581
20. C.J. Garrison, P.M. Dougherty, K.C. Kajander, and S.M. Carlton Staining of glial fibrillary acidic protein (GFAP) in lumbar spinal cord increases following a sciatic nerve constriction injury Brain Res. 565 1991 1 7
21. S.J. Gibson, J.M. Polak, S.R. Bloom, I.M. Sabate, P.M. Mulderry, M.A. Ghatei, G.P. McGregor, J.F. Morrison, J.S. Kelly, and R.M. Evans Calcitonin gene-related peptide immunoreactivity in the spinal cord of man and of eight other species J. Neurosci. 4 1984 3101 3111
22. Y. Guan, Q. Liu, Z. Tang, S.N. Raja, D.J. Anderson, and X. Dong Mas-related G-protein-coupled receptors inhibit pathological pain in mice Proc. Nat. Acad. Sci. U.S.A 107 2010 15933 15938
23. T.Z. Guo, T. Wei, X. Shi, W.W. Li, S. Hou, L. Wang, K. Tsujikawa, K.C. Rice, K. Cheng, D.J. Clark, and W.S. Kingery Neuropeptide deficient mice have attenuated nociceptive, vascular, and inflammatory changes in a tibia fracture model of complex regional pain syndrome Mol. Pain 8 2012 85
24. Y. Hao, A. Chun, K. Cheung, B. Rashidi, and X. Yang Tumor suppressor LATS1 is a negative regulator of oncogene YAP J. Biol. Chem. 283 2008 5496 5509
25. D.R. Hipfner, and S.M. Cohen Connecting proliferation and apoptosis in development and disease Nat. Rev. Mol. Cell Biol. 5 2004 805 815
26. D.I. Hughes, D.T. Scott, J.S. Riddell, and A.J. Todd Upregulation of substance P in low-threshold myelinated afferents is not required for tactile allodynia in the chronic constriction injury and spinal nerve ligation models J. Neurosci 27 2007 2035 2044
27. S.P. Hunt, and J. Rossi Peptide- and non-peptide-containing unmyelinated primary afferents: the parallel processing of nociceptive information Philos. Trans. R. Soc. London B Biol. Sci 308 1985 283 289
28. H. Ikeda, T. Kiritoshi, and K. Murase Contribution of microglia and astrocytes to the central sensitization, inflammatory and neuropathic pain in the juvenile rat Mol. Pain 8 2012 43
29. R.W. Justice, O. Zilian, D.F. Woods, M. Noll, and P.J. Bryant The Drosophila tumor suppressor gene warts encodes a homolog of human myotonic dystrophy kinase and is required for the control of cell shape and proliferation Genes Dev 9 1995 534 546
30. N. Kumar, A. Laferriere, J.S. Yu, T. Poon, and T.J. Coderre Metabotropic glutamate receptors (mGluRs) regulate noxious stimulus-induced glutamate release in the spinal cord dorsal horn of rats with neuropathic and inflammatory pain J. Neurochem 114 2010 281 290
31. J.W. Leem, Y.S. Gwak, E.H. Lee, S.S. Chung, Y.S. Kim, and T.S. Nam Effects of iontophoretically applied substance P, calcitonin gene-related peptide on excitability of dorsal horn neurones in rats Yonsei Med. J. 42 2001 74 83
32. Y.T. Lin, J.Y. Ding, M.Y. Li, T.S. Yeh, T.W. Wang, and J.Y. Yu YAP regulates neuronal differentiation through Sonic hedgehog signaling pathway Exp. Cell Res. 318 2012 1877 1888
33. L. Liu, M. Rudin, and E.N. Kozlova Glial cell proliferation in the spinal cord after dorsal rhizotomy or sciatic nerve transection in the adult rat Exp. Brain Res 131 2000 64 73
34. W. Liu, J. Wu, L. Xiao, Y. Bai, A. Qu, Z. Zheng, and Z. Yuan Regulation of neuronal cell death by c-Abl-Hippo/MST2 signaling pathway PLoS One 7 2012 e36562
35. W.M. Mahoney Jr., J.H. Hong, M.B. Yaffe, and I.K. Farrance The transcriptional co-activator TAZ interacts differentially with transcriptional enhancer factor-1 (TEF-1) family members Biochem. J. 388 2005 217 225
36. J. Mao, B. Sung, R.R. Ji, and G. Lim Neuronal apoptosis associated with morphine tolerance: evidence for an opioid-induced neurotoxic mechanism J. Neurosci. 22 2002 7650 7661
37. S.B. McMahon, and M. Malcangio Current challenges in glia-pain biology Neuron 64 2009 46 54
38. E.D. Milligan, and L.R. Watkins Pathological and protective roles of glia in chronic pain Nat. Rev. Neurosci. 10 2009 23 36
39. D.C. Molliver, D.E. Wright, M.L. Leitner, A.S. Parsadanian, K. Doster, D. Wen, Q. Yan, and W.D. Snider IB4-binding DRG neurons switch from NGF to GDNF dependence in early postnatal life Neuron 19 1997 849 861
40. T. Oka, V. Mazack, and M. Sudol Mst2 and Lats kinases regulate apoptotic function of Yes kinase-associated protein (YAP) J. Biol. Chem 283 2008 27534 27546
41. K. Ren, and R. Dubner Interactions between the immune and nervous systems in pain Nat. Med 16 2010 1267 1276
42. A. Ribeiro-da-Silva The substantia gelatinosa of the rat spinal cord G. Paxinos, The Rat Nervous System third ed. 2004 Academic Press Sydney 129 148
43. N. Rochefort, N. Quenech′du, L. Watroba, M. Mallat, C. Giaume, and C. Milleret Microglia and astrocytes may participate in the shaping of visual callosal projections during postnatal development J. Physiol. Paris 96 2002 183 192
44. L. Saur, P.P. Baptista, P.N. de Senna, M.F. Paim, P.D. Nascimento, J. Ilha, P.B. Bagatini, M. Achaval, and L.L. Xavier Physical exercise increases GFAP expression and induces morphological changes in hippocampal astrocytes Brain Struct. Funct. 2013
45. J. Scholz, D.C. Broom, D.H. Youn, C.D. Mills, T. Kohno, M.R. Suter, K.A. Moore, I. Decosterd, R.E. Coggeshall, and C.J. Woolf Blocking caspase activity prevents transsynaptic neuronal apoptosis and the loss of inhibition in lamina II of the dorsal horn after peripheral nerve injury J. Neurosci. 25 2005 7317 7323
46. Y. Shi, B.B. Gelman, J.G. Lisinicchia, and S.J. Tang Chronic-pain- associated astrocytic reaction in the spinal cord dorsal horn of human immunodeficiency virus-infected patients J. Neurosci. 32 2012 10833 10840
47. C.L. Stucky, and G.R. Lewin Isolectin B(4)-positive and -negative nociceptors are functionally distinct J. Neurosci. 19 1999 6497 6505
48. R.Q. Sun, Y.J. Tu, N.B. Lawand, J.Y. Yan, Q. Lin, and W.D. Willis Calcitonin gene-related peptide receptor activation produces PKA- and PKC-dependent mechanical hyperalgesia and central sensitization J. Neurophysiol. 92 2004 2859 2866
49. F.Y. Tanga, V. Raghavendra, and J.A. DeLeo Quantitative real-time RT-PCR assessment of spinal microglial and astrocytic activation markers in a rat model of neuropathic pain Neurochem. Int 45 2004 397 407
50. A.J. Todd Neuronal circuitry for pain processing in the dorsal horn Nat. Rev. Neurosci 11 2010 823 836
51. R.S. Udan, M. Kango-Singh, R. Nolo, C. Tao, and G. Halder Hippo promotes proliferation arrest and apoptosis in the Salvador/Warts pathway Nat. Cell Biol. 5 2003 914 920
52. F. Wei, R. Dubner, S. Zou, K. Ren, G. Bai, D. Wei, and W. Guo Molecular depletion of descending serotonin unmasks its novel facilitatory role in the development of persistent pain J. Neurosci. 30 2010 8624 8636
53. L.C. Yu, J.F. Hou, F.H. Fu, and Y.X. Zhang Roles of calcitonin gene-related peptide and its receptors in pain-related behavioral responses in the central nervous system Neurosci. Biobehav. Rev 33 2009 1185 1191
54. Y. Yu, T. Lundeberg, and L.C. Yu Role of calcitonin gene-related peptide and its antagonist on the evoked discharge frequency of wide dynamic range neurons in the dorsal horn of the spinal cord in rats Regul. Pept 103 2002 23 27
55. H. Zhang, H. Nei, and P.M. Dougherty A p38 mitogen-activated protein kinase-dependent mechanism of disinhibition in spinal synaptic transmission induced by tumor necrosis factor-alpha J. Neurosci 30 2010 12844 12855
56. H. Zhang, M. Deo, R.C. Thompson, M.D. Uhler, and D.L. Turner Negative regulation of Yap during neuronal differentiation Dev. Biol. 361 2012 103 115
57. J. Zhang, and Y. De Koninck Spatial and temporal relationship between monocyte chemoattractant protein-1 expression and spinal glial activation following peripheral nerve injury J. Neurochem 97 2006 772 783
58. J. Zhang, G.A. Smolen, and D.A. Haber Negative regulation of YAP by LATS1 underscores evolutionary conservation of the Drosophila Hippo pathway Cancer Res. 68 2008 2789 2794
59. X. Zhang, F.A. Grusche, and K.F. Harvey Control of tissue growth and cell transformation by the Salvador/Warts/Hippo pathway PLoS One 7 2012 e31994
60. B. Zhao, X. Wei, W. Li, R.S. Udan, Q. Yang, J. Kim, J. Xie, T. Ikenoue, J. Yu, L. Li, P. Zheng, K. Ye, A. Chinnaiyan, G. Halder, Z.C. Lai, and K.L. Guan Inactivation of YAP oncoprotein by the Hippo pathway is involved in cell contact inhibition and tissue growth control Genes Dev. 21 2007 2747 2761
61. B. Zhao, Q.Y. Lei, and K.L. Guan The Hippo-YAP pathway: new connections between regulation of organ size and cancer Curr. Opin. Cell Biol. 20 2008 638 646