The RhoA GTPase-activating protein DLC2 modulates RhoA activity and hyperalgesia to noxious thermal and inflammatory stimuli

NeuroSignals

Volumn 20, Issue 2, 2012, Pages 112-126

  Chan, Fred K C ^a   Chung, Stephen S M ^a,b   Ng, Irene O ^a   Chung, Sookja K ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b BNU HKBU UNITED INTERNATIONAL COLLEGE   (China)

Author keywords

Deleted in liver cancer 2; ERK; Hyperalgesia; Inflammation; Nerve conduction velocity; Pain; RhoA

Indexed keywords

DELETED IN LIVER CANCER 2; ENZYME ACTIVATOR; FORMALDEHYDE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN; ENZYME PHOSPHORYLATION; HYPERALGESIA; INFLAMMATION; MALE; MOUSE; NERVE CONDUCTION; NOCICEPTIVE STIMULATION; NONHUMAN; SCIATIC NERVE; SKIN NERVE; SPINAL CORD DORSAL HORN; SURAL NERVE; THERMAL STIMULATION;

ANIMALS; BRAIN; GTPASE-ACTIVATING PROTEINS; HYPERALGESIA; INFLAMMATION; MALE; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RHOA GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION; SPINAL CORD; SURAL NERVE; TUMOR SUPPRESSOR PROTEINS;

EID: 84858998423     PISSN: 1424862X     EISSN: 14248638     Source Type: Journal    
DOI: 10.1159/000331240     Document Type: Article

References (63)

1. Ching YP, Wong CM, Chan SF, Leung TH, Ng DC, Jin DY, Ng IO: Deleted in liver cancer (DLC) 2 encodes a RhoGAP protein with growth suppressor function and is underexpressed in hepatocellular carcinoma. J Biol Chem 2003; 278: 10824-10830. (Pubitemid 36800356)
2. Laurent-Puig P, Legoix P, Bluteau O, Belghiti J, Franco D, Binot F, Monges G, Thomas G, Bioulac-Sage P, Zucman-Rossi J: Genetic alterations associated with hepatocellular carcinomas define distinct pathways of hepatocarcinogenesis. Gastroenterology 2001; 120: 1763-1773. (Pubitemid 32523494)
3. Piao Z, Park C, Park JH, Kim H: Allelotype analysis of hepatocellular carcinoma. Int J Cancer 1998; 75: 29-33. (Pubitemid 28113973)
4. Kuroki T, Fujiwara Y, Nakamori S, Imaoka S, Kanematsu T, Nakamura Y: Evidence for the presence of two tumour-suppressor genes for hepatocellular carcinoma on chromosome 13q. Br J Cancer 1995; 72: 383-385.
5. Nagai H, Pineau P, Tiollais P, Buendia MA, Dejean A: Comprehensive allelotyping of human hepatocellular carcinoma. Oncogene 1997; 14: 2927-2933. (Pubitemid 27315661)
6. Lin YW, Sheu JC, Huang GT, Lee HS, Chen CH, Wang JT, Lee PH, Lu FJ: Chromosomal abnormality in hepatocellular carcinoma by comparative genomic hybridisation in Taiwan. Eur J Cancer 1999; 35: 652-658.
7. Zondervan PE, Wink J, Alers JC, Ijzermans JN, Schalm SW, de Man RA, van Dekken H: Molecular cytogenetic evaluation of virusassociated and non-viral hepatocellular carcinoma: analysis of 26 carcinomas and 12 concurrent dysplasias. J Pathol 2000; 192: 207-215.
8. Wong N, Lai P, Pang E, Leung TW, Lau JW, Johnson PJ: A comprehensive karyotypic study on human hepatocellular carcinoma by spectral karyotyping. Hepatology 2000; 32: 1060-1068.
9. Wang G, Zhao Y, Liu X, Wang L, Wu C, Zhang W, Liu W, Zhang P, Cong W, Zhu Y, Zhang L, Chen S, Wan D, Zhao X, Huang W, Gu J: Allelic loss and gain, but not genomic instability, as the major somatic mutation in primary hepatocellular carcinoma. Genes Chromosomes Cancer 2001; 31: 221-227. (Pubitemid 32521752)
10. Nagaraja GM, Kandpal RP: Chromosome 13q12 encoded Rho GTPase activating protein suppresses growth of breast carcinoma cells, and yeast two-hybrid screen shows its interaction with several proteins. Biochem Biophys Res Commun 2004; 313: 654-665. (Pubitemid 38021881)
11. Leung TH, Ching YP, Yam JW, Wong CM, Yau TO, Jin DY, Ng IO: Deleted in liver cancer (DLC2) suppresses cell transformation by means of inhibition of RhoA activity. Proc Natl Acad Sci USA 2005; 102: 15207-15212. (Pubitemid 41513360)
12. Yau TO, Leung THY, Lam SGS, Cheung OF, Khong PL, Lam AKM, Chung SK, Ng IOL: Deleted in liver cancer 2 (DLC2) was dispensable for development and its deficiency did not aggravate hepatocarcinogenesis. PLoS One 2009; 4:e6566.
13. Inoue M, Rashid MH, Fujita R, Contos JJ, Chun J, Ueda H: Initiation of neuropathic pain requires lysophosphatidic acid receptor signaling. Nat Med 2004; 10: 712-718. (Pubitemid 38937636)
14. Tatsumi S, Mabuchi T, Katano T, Matsumura S, Abe T, Hidaka H, Suzuki M, Sasaki Y, Minami T, Ito S: Involvement of Rho-kinase in inflammatory and neuropathic pain through phosphorylation of myristoylated alanine-rich C-kinase substrate (MARCKS). Neuroscience 2005; 131: 491-498. (Pubitemid 40222456)
15. Büyükafa K, Yalçn I, Kurt AH, Tiftik RN, Sahan-Firat S, Aksu F: Rho-kinase inhibitor, Y-27632, has an antinociceptive effect in mice. Eur J Pharmacol 2006; 541: 49-52. (Pubitemid 43922439)
16. Büyükafa K, Levent A: Involvement of Rho/ Rho-kinase signalling in the contractile activity and acetylcholine release in the mouse gastric fundus. Biochem Biophys Res Commun 2003 303 777-781. (Pubitemid 36384922)
17. Sasaki Y: New aspects of neurotransmitter release and exocytosis: Rho-kinase-dependent myristoylated alanine-rich C-kinase substrate phosphorylation and regulation of neurofilament structure in neuronal cells. J Pharmacol Sci 2003; 93: 35-40. (Pubitemid 37254264)
18. McMullan R, Hiley E, Morrison P, Nurrish SJ: Rho is a presynaptic activator of neurotransmitter release at pre-existing synapses in C. elegans . Genes Dev 2006; 20: 65-76. (Pubitemid 43042668)
19. Crawley JN: What's Wrong with My Mouse? Behavioral Phenotyping of Transgenic and Knockout Mice. New York, Wiley-Liss, 2000.
20. Song Z, Fu DT, Chan YS, Leung S, Chung SS, Chung SK: Transgenic mice overexpressing aldose reductase in Schwann cells show more severe nerve conduction velocity deficit and oxidative stress under hyperglycemic stress. Mol Cell Neurosci 2003; 23: 638-647. (Pubitemid 36970224)
21. Ho EC, Lam KS, Chen YS, Yip JC, Arvindakshan M, Yamagishi S, Yagihashi S, Oates PJ, Ellery CA, Chung SS, Chung SK: Aldose reductase- deficient mice are protected from delayed motor nerve conduction velocity, increased c-Jun NH2-terminal kinase activation, depletion of reduced glutathione, increased superoxide accumulation, and DNA damage. Diabetes 2006; 55: 1946-1953. (Pubitemid 44509966)
22. De Koning P, Gispen WH: Org.2766 improves functional and electrophysiological aspects of regenerating sciatic nerve in the rat. Peptides 1987; 8: 415-422. (Pubitemid 17119173)
23. Chen YS, Chung SS, Chung SK: Noninvasive monitoring of diabetes-induced cutaneous nerve fiber loss and hypoalgesia in thy1-YFP transgenic mice. Diabetes 2005; 54: 3112-3118. (Pubitemid 43334363)
24. Lauria G, Cornblath DR, Johansson O, McArthur JC, Mellgren SI, Nolano M, Rosenberg N, Sommer C: EFNS guidelines on the use of skin biopsy in the diagnosis of peripheral neuropathy. Eur J Neurol 2005; 12: 747-758. (Pubitemid 41495131)
25. Ji RR, Baba H, Brenner GJ, Woolf CJ: Nociceptive- specific activation of ERK in spinal neurons contributes to pain hypersensitivity. Nat Neurosci 1999; 2: 1114-1119. (Pubitemid 30126370)
26. Ji RR, Befort K, Brenner GJ, Woolf CJ: ERK MAP kinase activation in superficial spinal cord neurons induces prodynorphin and NK-1 upregulation and contributes to persistent inflammatory pain hypersensitivity. J Neurosci 2002; 22: 478-485. (Pubitemid 34049086)
27. Leung TH, Yam JW, Chan LK, Ching YP, Ng IO: Deleted in liver cancer 2 suppresses cell growth via the regulation of the Raf-1- ERK1/2-p70S6K signalling pathway. Liver Int 2010; 30: 1315-1323.
28. Tanaka H, Yoshida T, Miyamoto N, Motoike T, Kurosu H, Shibata K, Yamanaka A, Williams SC, Richardson JA, Tsujino N, Garry MG, Lerner MR, King DS, O'Dowd BF, Sakurai T, Yanagisawa M: Characterization of a family of endogenous neuropeptide ligands for the G protein-coupled receptors GPR7 and GPR8. Proc Natl Acad Sci USA 2003; 100: 6251-6256. (Pubitemid 36576962)
29. Lee DK, Nguyen T, Porter CA, Cheng R, George SR, O'Dowd BF: Two related G protein- coupled receptors: the distribution of GPR7 in rat brain and the absence of GPR8 in rodents. Brain Res Mol Brain Res 1999; 71: 96-103. (Pubitemid 29320060)
30. Neugebauer V, Li W, Bird GC, Han JS: The amygdala and persistent pain. Neuroscientist 2004; 10: 221-234. (Pubitemid 38678530)
31. Khanna S, Chang LS, Jiang F, Koh HC: Nociception- driven decreased induction of Fos protein in ventral hippocampus field CA1 of the rat. Brain Res 2004; 1004: 167-176. (Pubitemid 38368073)
32. Lanteri-Minet M, Isnardon P, de Pommery J, Menetrey D: Spinal and hindbrain structures involved in visceroception and visceronociception as revealed by the expression of Fos, Jun and Krox-24 proteins. Neuroscience 1993; 55: 737-753. (Pubitemid 23226119)
33. Mogil JS, Wilson SG, Bon K, Lee SE, Chung K, Raber P, Pieper JO, Hain HS, Belknap JK, Hubert L, Elmer GI, Chung JM, Devor M: Heritability of nociception II. Types' of nociception revealed by genetic correlation analysis. Pain 1999; 80: 83-93. (Pubitemid 29151692)
34. Kelly MA, Beuckmann CT, Williams SC, Sinton CM, Motoike T, Richardson JA, Hammer RE, Garry MG, Yanagisawa M: Neuropeptide B-deficient mice demonstrate hyperalgesia in response to inflammatory pain. Proc Natl Acad Sci USA 2005; 102: 9942-9947. (Pubitemid 40993672)
35. Gyires K, Torma Z: The use of the writhing test in mice for screening different types of analgesics. Arch Int Pharmacodyn Ther 1984; 267: 131-140. (Pubitemid 14193943)
36. Karim F, Hu HJ, Adwanikar H, Kaplan D, Gereau RWt: Impaired inflammatory pain and thermal hyperalgesia in mice expressing neuron-specific dominant negative mitogen activated protein kinase kinase (MEK). Mol Pain 2006; 2: 2.
37. Ramakers GJ: Rho proteins and the cellular mechanisms of mental retardation. Am J Med Genet 2000; 94: 367-371.
38. Nakazawa T, Watabe AM, Tezuka T, Yoshida Y, Yokoyama K, Umemori H, Inoue A, Okabe S, Manabe T, Yamamoto T: p250GAP, a novel brain-enriched GTPase-activating protein for Rho family GTPases, is involved in the N-methyl-d-aspartate receptor signaling. Mol Biol Cell 2003; 14: 2921-2934. (Pubitemid 36871531)
39. Wong CM, Lee JM, Ching YP, Jin DY, Ng IO: Genetic and epigenetic alterations of DLC-1 gene in hepatocellular carcinoma. Cancer Res 2003; 63: 7646-7651. (Pubitemid 37466690)
40. Durkin ME, Avner MR, Huh CG, Yuan BZ, Thorgeirsson SS, Popescu NC: DLC-1, a Rho GTPase-activating protein with tumor suppressor function, is essential for embryonic development. FEBS Lett 2005; 579: 1191-1196. (Pubitemid 40248686)
41. Brouns MR, Matheson SF, Settleman J: p190 RhoGAP is the principal Src substrate in brain and regulates axon outgrowth, guidance and fasciculation. Nat Cell Biol 2001; 3: 361-367. (Pubitemid 32288443)
42. Soleimannejad E, Semnanian S, Fathollahi Y, Naghdi N: Microinjection of ritanserin into the dorsal hippocampal CA1 and dentate gyrus decrease nociceptive behavior in adult male rat. Behav Brain Res 2006; 168: 221-225. (Pubitemid 43201938)
43. Masri R, Quiton RL, Lucas JM, Murray PD, Thompson SM, Keller A: Zona incerta: a role in central pain. J Neurophysiol 2009; 102: 181-191.
44. Tucker KJ, Tuncer M, Türker KS: A review of the H-reflex and M-wave in the human triceps surae. Hum Mov Sci 2005; 24: 667-688. (Pubitemid 43124619)
45. Gally JA, Montague PR, Reeke GN Jr, Edelman GM: The NO hypothesis: possible effects of a short-lived, rapidly diffusible signal in the development and function of the nervous system. Proc Natl Acad Sci USA 1990; 87: 3547-3551.
46. Matsumura S, Abe T, Mabuchi T, Katano T, Takagi K, Okuda-Ashitaka E, Tatsumi S, Nakai Y, Hidaka H, Suzuki M, Sasaki Y, Minami T, Ito S: Rho-kinase mediates spinal nitric oxide formation by prostaglandin E2 via EP3 subtype. Biochem Biophys Res Commun 2005; 338: 550-557. (Pubitemid 41540602)
47. Ye X, Inoue M, Ueda H: Botulinum toxin C3 inhibits hyperalgesia in mice with partial sciatic nerve injury. Jpn J Pharmacol 2000; 83: 161-163. (Pubitemid 30449747)
48. Ohsawa M, Mutoh J, Hisa H: Mevalonate sensitizes the nociceptive transmission in the mouse spinal cord. Pain 2008; 134: 285-292.
49. Ohsawa M, Aasato M, Hayashi SS, Kamei J: RhoA/Rho kinase pathway contributes to the pathogenesis of thermal hyperalgesia in diabetic mice. Pain 2011; 152: 114-122.
50. Kawai K, Kiyota M, Seike J, Deki Y, Yagisawa H: START-GAP3/DLC3 is a GAP for RhoA and Cdc42 and is localized in focal adhesions regulating cell morphology. Biochem Biophys Res Commun 2007; 364: 783-789. (Pubitemid 350087871)
51. Ji RR: Peripheral and central mechanisms of inflammatory pain, with emphasis on MAP kinases. Curr Drug Targets Inflamm Allergy 2004; 3: 299-303.
52. Sasagawa S, Ozaki Y, Fujita K, Kuroda S: Prediction and validation of the distinct dynamics of transient and sustained ERK activation. Nat Cell Biol 2005; 7: 365-373. (Pubitemid 40533125)
53. Morozov A, Muzzio IA, Bourtchouladze R, Van-Strien N, Lapidus K, Yin D, Winder DG, Adams JP, Sweatt JD, Kandel ER: Rap1 couples cAMP signaling to a distinct pool of p42/44MAPK regulating excitability, synaptic plasticity, learning, and memory. Neuron 2003; 39: 309-325. (Pubitemid 36897552)
54. Impey S, Obrietan K, Wong ST, Poser S, Yano S, Wayman G, Deloulme JC, Chan G, Storm DR: Cross talk between ERK and PKA is required for Ca2+ stimulation of CREB-dependent transcription and ERK nuclear translocation. Neuron 1998; 21: 869-883. (Pubitemid 28498794)
55. Obrietan K, Impey S, Smith D, Athos J, Storm DR: Circadian regulation of cAMP response element-mediated gene expression in the suprachiasmatic nuclei. J Biol Chem 1999; 274: 17748-17756.
56. Xing J, Ginty DD, Greenberg ME: Coupling of the RAS-MAPK pathway to gene activation by RSK2, a growth factor-regulated CREB kinase. Science 1996; 273: 959-963. (Pubitemid 26275173)
57. Abbadie C, Trafton J, Liu H, Mantyh PW, Basbaum AI: Inflammation increases the distribution of dorsal horn neurons that internalize the neurokinin-1 receptor in response to noxious and non-noxious stimulation. J Neurosci 1997; 17: 8049-8060. (Pubitemid 27426240)
58. McCarson KE, Krause JE: NK-1 and NK-3 type tachykinin receptor mRNA expression in the rat spinal cord dorsal horn is increased during adjuvant or formalin-induced nociception. J Neurosci 1994; 14: 712-720. (Pubitemid 24043925)
59. Dubner R, Ruda MA: Activity-dependent neuronal plasticity following tissue injury and inflammation. Trends Neurosci 1992; 15: 96-103.
60. Hylden JL, Nahin RL, Traub RJ, Dubner R: Effects of spinal kappa-opioid receptor agonists on the responsiveness of nociceptive superficial dorsal horn neurons. Pain 1991; 44: 187-193.
61. Stahle M, Veit C, Bachfischer U, Schierling K, Skripczynski B, Hall A, Gierschik P, Giehl K: Mechanisms in LPA-induced tumor cell migration: critical role of phosphorylated ERK. J Cell Sci 2003; 116: 3835-3846. (Pubitemid 37185312)
62. Zhu S, Korzh V, Gong Z, Low BC: RhoA prevents apoptosis during zebrafish embryogenesis through activation of Mek/Erk pathway. Oncogene 2008; 27: 1580-1589. (Pubitemid 351347874)
63. Li H, Ung CY, Ma XH, Li BW, Low BC, Cao ZW, Chen YZ: Simulation of crosstalk between small GTPase RhoA and EGFR-ERK signaling pathway via MEKK1. Bioinformatics 2009; 25: 358-364.