Targeted deletion of LPA5 identifies novel roles for lysophosphatidic acid signaling in development of neuropathic pain

Journal of Biological Chemistry

Volumn 287, Issue 21, 2012, Pages 17608-17617

  Lin, Mu En ^a,b   Rivera, Richard R ^a   Chun, Jerold ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOACTIVE LIPIDS; COUPLED RECEPTORS; DORSAL ROOT GANGLION NEURONS; ELEMENT-BINDING PROTEINS; EXTRACELLULAR; G PROTEIN COUPLED RECEPTORS; GLIAL FIBRILLARY ACIDIC PROTEINS; LYSOPHOSPHATIDIC ACID; MOUSE MODELS; NEUROPATHIC PAIN; NULL MUTANT; PATHOLOGICAL EFFECTS; SCIATIC NERVES; SIGNALING MOLECULES; SIGNALING PATHWAYS; SPINAL CORDS; UP-REGULATION;

GENE EXPRESSION; MAMMALS; PHOSPHOLIPIDS; PHOSPHORYLATION; PROTEINS;

HEALTH;

BIOLOGICAL MARKER; CALCIUM CHANNEL ALPHA 2 DELTA 1; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; GLIAL FIBRILLARY ACIDIC PROTEIN; LYSOPHOSPHATIDIC ACID RECEPTOR; MESSENGER RNA; UNCLASSIFIED DRUG; CYCLIC AMP; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; LYSOPHOSPHATIDIC ACID; LYSOPHOSPHOLIPID; NERVE PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DELETION MUTANT; DISEASE MARKER; FEMALE; GENE; GENE DELETION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE TARGETING; GENETIC ASSOCIATION; LYSOPHOSPHATIDIC ACID RECEPTOR 5 GENE; MOUSE; NEUROPATHIC PAIN; NONHUMAN; NULL ALLELE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SPINAL CORD DORSAL HORN; UPREGULATION; WILD TYPE; ANIMAL; DNA RESPONSIVE ELEMENT; GENETICS; METABOLISM; MOUSE MUTANT; NEURALGIA; PATHOLOGY; SPINAL GANGLION;

MUS;

ANIMALS; CYCLIC AMP; GANGLIA, SPINAL; GENE DELETION; GTP-BINDING PROTEIN ALPHA SUBUNITS, G12-G13; LYSOPHOSPHOLIPIDS; MICE; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; NEURALGIA; RECEPTORS, LYSOPHOSPHATIDIC ACID; RESPONSE ELEMENTS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84861218222     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.330183     Document Type: Article

References (47)

1. Bouhassira, D., Lantéri-Minet, M., Attal, N., Laurent, B., and Touboul, C. (2008) Prevalence of chronic pain with neuropathic characteristics in the general population. Pain 136, 380-387 (Pubitemid 351680253)
2. Torrance, N., Smith, B. H., Bennett, M. I., and Lee, A. J. (2006) The epidemiology of chronic pain of predominantly neuropathic origin. Results from a general population survey. J. Pain 7, 281-289
3. Seltzer, Z., Dubner, R., and Shir, Y. (1990) A novel behavioral model of neuropathic pain disorders produced in rats by partial sciatic nerve injury. Pain 43, 205-218 (Pubitemid 20385185)
4. Gao, X., Kim, H. K., Chung, J. M., and Chung, K. (2005) Enhancement of NMDA receptor phosphorylation of the spinal dorsal horn and nucleus gracilis neurons in neuropathic rats. Pain 116, 62-72 (Pubitemid 40828501)
5. Miletic, G., Pankratz, M. T., and Miletic, V. (2002) Increases in the phosphorylation of cyclic AMP response element binding protein (CREB) and decreases in the content of calcineurin accompany thermal hyperalgesia following chronic constriction injury in rats. Pain 99, 493-500 (Pubitemid 35284281)
6. Sorkin, L. S., and Yaksh, T. L. (2009) Behavioral models of pain states evoked by physical injury to the peripheral nerve. Neurotherapeutics 6, 609-619
7. Inoue, M., Rashid, M. H., Fujita, R., Contos, J. J., Chun, J., and Ueda, H. (2004) Initiation of neuropathic pain requires lysophosphatidic acid receptor signaling. Nat. Med. 10, 712-718 (Pubitemid 38937636)
8. Karliner, J. S. (2004) Mechanisms of cardioprotection by lysophospholipids. J. Cell Biochem. 92, 1095-1103
9. Swaney, J. S., Chapman, C., Correa, L. D., Stebbins, K. J., Bundey, R. A., Prodanovich, P. C., Fagan, P., Baccei, C. S., Santini, A. M., Hutchinson, J. H., Seiders, T. J., Parr, T. A., Prasit, P., Evans, J. F., and Lorrain, D. S. (2010) A novel, orally active LPA1 receptor antagonist inhibits lung fibrosis in the mouse bleomycin model. Br. J. Pharmacol. 160, 1699-1713
10. Panupinthu, N., Lee, H. Y., and Mills, G. B. (2010) Lysophosphatidic acid production and action. Critical new players in breast cancer initiation and progression. Br. J. Cancer 102, 941-946
11. Ye, X., Hama, K., Contos, J. J., Anliker, B., Inoue, A., Skinner, M. K., Suzuki, H., Amano, T., Kennedy, G., Arai, H., Aoki, J., and Chun, J. (2005) LPA3- mediated lysophosphatidic acid signalling in embryo implantation and spacing. Nature 435, 104-108 (Pubitemid 40655916)
12. Yung, Y. C., Mutoh, T., Lin, M. E., Noguchi, K., Rivera, R. R., Choi, J. W., Kingsbury, M. A., and Chun, J. (2011) Lysophosphatidic acid signaling may initiate fetal hydrocephalus. Sci. Transl Med. 3, 99ra87
13. Lin, M. E., Herr, D. R., and Chun, J. (2010) Lysophosphatidic acid (LPA) receptors. Signaling properties and disease relevance. Prostaglandins Other Lipid Mediat. 91, 130-138
14. Noguchi, K., Herr, D., Mutoh, T., and Chun, J. (2009) Lysophosphatidic acid (LPA) and its receptors. Curr. Opin Pharmacol. 9, 15-23
15. Contos, J. J., Fukushima, N., Weiner, J. A., Kaushal, D., and Chun, J. (2000) Requirement for the lpA1 lysophosphatidic acid receptor gene in normal suckling behavior. Proc. Natl. Acad. Sci. U.S.A. 97, 13384-13389
16. 2 (Edg2/Edg4) lysophosphatidic acid receptor knockout mice. Signaling deficits without obvious phenotypic abnormality attributable to lpa2. Mol. Cell Biol. 22, 6921-6929
17. Sumida, H., Noguchi, K., Kihara, Y., Abe, M., Yanagida, K., Hamano, F., Sato, S., Tamaki, K., Morishita, Y., Kano, M. R., Iwata, C., Miyazono, K., Sakimura, K., Shimizu, T., and Ishii, S. (2010) LPA4 regulates blood and lymphatic vessel formation during mouse embryogenesis. Blood 116, 5060-5070
18. Choi, J. W., Herr, D. R., Noguchi, K., Yung, Y. C., Lee, C. W., Mutoh, T., Lin, M. E., Teo, S. T., Park, K. E., Mosley, A. N., and Chun, J. (2010) LPA receptors. Subtypes and biological actions. Annu. Rev. Pharmacol. Toxicol. 50, 157-186
19. Cohen, A., Sagron, R., Somech, E., Segal-Hayoun, Y., and Zilberberg, N. (2009) Pain-associated signals, acidosis and lysophosphatidic acid, modulate the neuronal K(2P)2.1 channel. Mol. Cell Neurosci. 40, 382-389
20. Xie, W., Matsumoto, M., Chun, J., and Ueda, H. (2008) Involvement of LPA1 receptor signaling in the reorganization of spinal input through Aβ-fibers in mice with partial sciatic nerve injury. Mol. Pain 4, 46
21. Lee, C. W., Rivera, R., Gardell, S., Dubin, A. E., and Chun, J. (2006) GPR92 as a new G12/13- and Gq-coupled lysophosphatidic acid receptor that increases cAMP, LPA5. J. Biol. Chem. 281, 23589-23597 (Pubitemid 44274133)
22. Kotarsky, K., Boketoft, A., Bristulf, J., Nilsson, N. E., Norberg, A., Hansson, S., Owman, C., Sillard, R., Leeb-Lundberg, L. M., and Olde, B. (2006) Lysophosphatidic acid binds to and activates GPR92, a G protein-coupled receptor highly expressed in gastrointestinal lymphocytes. J. Pharmacol. Exp. Ther. 318, 619-628 (Pubitemid 44061237)
23. Amisten, S., Braun, O. O., Bengtsson, A., and Erlinge, D. (2008) Gene expression profiling for the identification of G-protein coupled receptors in human platelets. Thromb. Res. 122, 47-57 (Pubitemid 351601841)
24. Ohuchi, H., Hamada, A., Matsuda, H., Takagi, A., Tanaka, M., Aoki, J., Arai, H., and Noji, S. (2008) Expression patterns of the lysophospholipid receptor genes during mouse early development. Dev. Dyn. 237, 3280-3294
25. Braissant, O., and Wahli, W. (1998) A simplified in situ hybridization protocol using non-radioactively labeled probes to detect abundant and rare mRNAs on tissue sections. Biochemica 1, 10-16
26. Plenz, G., Weissen, B., and Steffen, I. (2003) Detection of mRNAs on cryosections of the cardiovascular system using DIG-labeled RNA probes. Biochemica 1, 19-21 (Pubitemid 36270167)
27. Smith, K. J., and McDonald, W. I. (1982) Spontaneous and evoked electrical discharges from a central demyelinating lesion. J. Neurol. Sci. 55, 39-47
28. Rasminsky, M. (1978) Ectopic generation of impulses and cross-talk in spinal nerve roots of "dystrophic" mice. Ann. Neurol. 3, 351-357
29. Luo, Z. D., Calcutt, N. A., Higuera, E. S., Valder, C. R., Song, Y. H., Svensson, C. I., and Myers, R. R. (2002) Injury type-specific calcium channel α2 δ-1 subunit up-regulation in rat neuropathic pain models correlates with antiallodynic effects of gabapentin. J. Pharmacol. Exp. Ther. 303, 1199-1205 (Pubitemid 35424406)
30. Luo, Z. D., Chaplan, S. R., Higuera, E. S., Sorkin, L. S., Stauderman, K. A., Williams, M. E., and Yaksh, T. L. (2001) Upregulation of dorsal root ganglion α2δ calcium channel subunit and its correlation with allodynia in spinal nerve-injured rats. J. Neurosci. 21, 1868-1875 (Pubitemid 32221370)
31. Malmberg, A. B., Chen, C., Tonegawa, S., and Basbaum, A. I. (1997) Preserved acute pain and reduced neuropathic pain in mice lacking PKCγ. Science 278, 279-283 (Pubitemid 27450873)
32. Coyle, D. E. (1998) Partial peripheral nerve injury leads to activation of astroglia and microglia which parallels the development of allodynic behavior. Glia 23, 75-83
33. Ma, W., and Quirion, R. (2001) Increased phosphorylation of cyclic AMP response element-binding protein (CREB) in the superficial dorsal horn neurons following partial sciatic nerve ligation. Pain 93, 295-301 (Pubitemid 32763186)
34. Song, X. S., Cao, J. L., Xu, Y. B., He, J. H., Zhang, L. C., and Zeng, Y. M. (2005) Activation of ERK/CREB pathway in spinal cord contributes to chronic constrictive injury-induced neuropathic pain in rats. Acta Pharmacol. Sin. 26, 789-798
35. Liou, J. T., Liu, F. C., Hsin, S. T., Yang, C. Y., and Lui, P. W. (2007) Inhibition of the cyclic adenosine monophosphate pathway attenuates neuropathic pain and reduces phosphorylation of cyclic adenosine monophosphate response element-binding in the spinal cord after partial sciatic nerve ligation in rats. Anesth. Analg. 105, 1830-1837
36. Wang, Y., Cheng, X., Xu, J., Liu, Z., Wan, Y., and Ma, D. (2011) Antihyperalgesic effect of CaMKII inhibitor is associated with downregulation of phosphorylated CREB in rat spinal cord. J. Anesth. 25, 87-92
37. Ma, L., Uchida, H., Nagai, J., Inoue, M., Aoki, J., and Ueda, H. (2010) Evidence for de novo synthesis of lysophosphatidic acid in the spinal cord through phospholipase A2 and autotaxin in nerve injury-induced neuropathic pain. J. Pharmacol. Exp. Ther. 333, 540-546
38. Nagai, J., Uchida, H., Matsushita, Y., Yano, R., Ueda, M., Niwa, M., Aoki, J., Chun, J., and Ueda, H. (2010) Autotaxin and lysophosphatidic acid 1 receptor-mediated demyelination of dorsal root fibers by sciatic nerve injury and intrathecal lysophosphatidylcholine. Mol. Pain 6, 78
39. Gao, Y. J., and Ji, R. R. (2010) Targeting astrocyte signaling for chronic pain. Neurotherapeutics 7, 482-493
40. Milligan, E. D., and Watkins, L. R. (2009) Pathological and protective roles of glia in chronic pain. Nat. Rev. Neurosci. 10, 23-36
41. Bezzi, P., Domercq, M., Vesce, S., and Volterra, A. (2001) Neuron-astrocyte cross-talk during synaptic transmission. Physiological and neuropathological implications. in Progress in Brain Research (Castellano Lopez, M. N.-S. B., ed) pp. 255-265, Elsevier Science Publishing Co., Inc., New York
42. Hoeger-Bement, M. K., and Sluka, K. A. (2003) Phosphorylation of CREB and mechanical hyperalgesia is reversed by blockade of the cAMP pathway in a time-dependent manner after repeated intramuscular acid injections. J. Neurosci. 23, 5437-5445 (Pubitemid 36807817)
43. Kawasaki, Y., Kohno, T., Zhuang, Z. Y., Brenner, G. J., Wang, H., Van Der Meer, C., Befort, K., Woolf, C. J., and Ji, R. R. (2004) Ionotropic and metabotropic receptors, protein kinase A, protein kinase C, and Src contribute to C-fiber-induced ERK activation and cAMP response elementbinding protein phosphorylation in dorsal horn neurons, leading to central sensitization. J. Neurosci. 24, 8310-8321 (Pubitemid 39280810)
44. Ji, R. R., and Rupp, F. (1997) Phosphorylation of transcription factor CREB in rat spinal cord after formalin-induced hyperalgesia. Relationship to c-fos induction. J. Neurosci. 17, 1776-1785
45. Williams, J. R., Khandoga, A. L., Goyal, P., Fells, J. I., Perygin, D. H., Siess, W., Parrill, A. L., Tigyi, G., and Fujiwara, Y. (2009) Unique ligand selectivity of the GPR92/LPA5 lysophosphatidate receptor indicates role in human platelet activation. J. Biol. Chem. 284, 17304-17319
46. Fujiwara, Y., Sardar, V., Tokumura, A., Baker, D., Murakami-Murofushi, K., Parrill, A., and Tigyi, G. (2005) Identification of residues responsible for ligand recognition and regioisomeric selectivity of lysophosphatidic acid receptors expressed in mammalian cells. J. Biol. Chem. 280, 35038 -35050
47. Ma, L., Uchida, H., Nagai, J., Inoue, M., Chun, J., Aoki, J., and Ueda, H. (2009) Lysophosphatidic acid-3 receptor-mediated feed-forward production of lysophosphatidic acid. An initiator of nerve injury-induced neuropathic pain. Mol. Pain 5, 64