Signal transduction pathways for P2Y2 and P2X7 nucleotide receptors that mediate neuroinflammatory responses in astrocytes and microglial cells

Biomedical Research

Volumn 14, Issue 1, 2003, Pages 47-61

  Gendron, Fernand Pierre ^a   Newbold, Nathan L ^a   Vivas Mejia, Pablo E ^c   Wang, Min ^a   Neary, Joseph T ^b   Sun, Grace Y ^a   Gonzalez, Fernando A ^c   Weisman, Gary A ^a  

^a UNIVERSITY OF MISSOURI   (United States)

^b UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF PUERTO RICO   (Puerto Rico)

Author keywords

[No Author keywords available]

Indexed keywords

2 [1 (3 DIMETHYLAMINOPROPYL) 3 INDOLYL] 3 (3 INDOLYL)MALEIMIDE; 2 MORPHOLINO 8 PHENYLCHROMONE; ADENOSINE TRIPHOSPHATE; ARACHIDONIC ACID; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; G PROTEIN COUPLED RECEPTOR; ION CHANNEL; MITOGEN ACTIVATED PROTEIN KINASE; NUCLEOTIDE; PROTEIN TYROSINE KINASE; PURINE P2X RECEPTOR; PURINE P2Y RECEPTOR; STRESS ACTIVATED PROTEIN KINASE; TRANSFORMING GROWTH FACTOR BETA; URIDINE TRIPHOSPHATE;

ALZHEIMER DISEASE; ARTICLE; ASTROCYTE; BRAIN INJURY; CALCIUM TRANSPORT; CELL IMMORTALIZATION; ENCEPHALITIS; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; HUMAN; MICROGLIA; NERVE DEGENERATION; NONHUMAN; SIGNAL TRANSDUCTION;

EID: 0037599243     PISSN: 0970938X     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (135)

1. Burnstock G. Evolution of the autonomic innervation of visceral and cardiovascular systems in vertebrates. Pharmacol Rev 1969; 21: 247-324.
2. Burnstock G. Neural nomenclature. Nature 1971; 229: 282-283.
3. Burnstock G. Purinergic receptors. J Theor Biol 1976; 62: 491-503.
4. Burnstock G. A basis for distinguishing two types of purinergic receptor. In: Cell membrane receptors for drugs and hormones: A multidisciplinary approach. (Straub, R.W. and Bolis, L., Eds.), Raven Press, New York, pp. 1978; 108-118.
5. Su C, Bevan JA, Burnstock G. [3H]-adenosine triphosphate: release during stimulation of enteric nerves. Science 1971; 173: 336-338.
6. Langer SZ, Pinto EB. Possible involvement of a transmitter different from norepinephrine in the residual responses to nerve stimulation of the cat nictitating membrane after pretreatment with reserpine. J Pharmacol Exp Ther 1976; 196: 697-713.
7. Abbracchio MP, Burnstock G. Purinergic signalling: pathophysiological roles. Jap J Pharmacol 1998; 78: 113-145.
8. Williams M, Jarvis MF. Purinergic and pyrimidinergic receptors as potential drug targets. Biochem Pharmacol 2000; 59: 1173-1185.
9. Fredholm BB, Abbracchio MP, Burnstock G, Daly JW, Harden TK, Jacobson KA, Leff P, Williams M. Nomenclature and classification of purinoceptors. Pharmacol Rev 1994; 46: 143-156.
10. Fredholm BB, Ijzerman AP, Jacobson KA, Klotz KN, Linden J. International union of pharmacology. XXV. Nomenclature and classification of adenosine receptors. Pharmacol Rev 2001; 53: 527-552.
11. Burnstock G, Kennedy C. Is there a basis for distinguishing two types of P2 purinoreceptor? Gen Pharmacol 1985; 16: 433-440.
12. Abbracchio MP, Burnstock G. Purinoceptors: are there families of P2X and P2Y purinoceptors? Pharmacol Ther 1994; 64: 445-475.
13. von Kugelgen I, Wetter A. Molecular pharmacology of P2Y-receptors.Naunyn-Schmiedeberg's Arch Pharmacol 2000; 362: 310-323.
14. 1 purinoceptor. Gene 1996; 171: 295-297.
15. 1-purinoceptor. Br J Pharmacol 1996; 118: 167-173
16. Lustig KD, Shiau AK, Brake AJ, Julius D. Expression cloning of an ATP receptor from mouse neuroblastoma cells. Proc Natl Acad Sci USA 1993; 90: 5113-5117.
17. 2U nucleotide receptor: a target for cystic fibrosis pharmacotherapy. Proc Natl Acad Sci USA 1994; 91: 3275-3279
18. Nguyen T, Erb L, Weisman GA, Marchese A, Heng HHQ, Garrad RC, George SR, Turner JT, O'Dowd BF. 1995; Cloning, expression and chromosomal localization of a human uridine nucleotide receptor gene. J Biol Chem 1995; 270: 30845-30848.
19. Communi D, Pirotton S, Parmentier M, Boeynaems JM. Cloning and functional expression of a human uridine nucleotide receptor. J Biol Chem 1995; 270: 30849-30852.
20. 11 receptor. Br J Pharmacol 1999; 128: 1199-1206.
21. 6 receptor. Biochem Biophys Res Commun 1996; 222: 303-308.
22. Communi D, Govaerts C, Parmentier M, Boeynaems JM. Cloning of a human purinergic P2Y receptor coupled to phospholipase C and adenylyl cyclase. J Biol Chem 1997; 272: 31969-31973.
23. Hollopeter G, Jantzen HM, Vincent D, Li G, England L, Ramakrishnan V, Yang, RB, Nurden P, Nurden A, Julius D, Conley PB. Identification of the platelet ADP receptor targeted by antithrombotic drugs. Nature 2001; 409: 202-207.
24. Communi D, Gonzalez NS, Detheux M, Brezillon S, Lannoy V, Parmentier M, Boeynaems JM. Identification of a novel human ADP receptor coupled to Gi. J Biol Chem 2001; 44: 41479-41485.
25. αi-coupled ADP receptor from human and mouse. J Pharmacol Exp Ther 2002; 301: 705-713.
26. Chambers JK, MacDonald LE, Sarau HM, Ames RS, Freeman K, Foley JJ, Zhu Y, McLaughlin MM, Murdock P, McMillan L, Trill J, Swift A, Aiyar N, Taylor P, Vawter, L, Naheed S, Szekeres P, Hervieu G, Scott C, Watson JM, Murphy AJ, Duzic E, Klein C, Bergsma DJ, Wilson S, Livi GP. A G protein-coupled receptor for UDP-glucose. J Biol Chem 2000; 275: 10767-10771.
27. Erb L, Lustig KD, Sullivan DM, Turner JT, Weisman GA. Functional expression and photoaffinity labeling of a cloned P2U purinergic receptor. Proc Natl Acad Sci USA 1993; 90: 10449-10453.
28. Lin T-A, Lustig KD, Sportiello MG, Weisman GA, Sun GY. Signal transduction pathways in response to extracellular ATP and other nucleotides in NG108-15 cells. J Neurochem 1993; 60: 1115-1125.
29. Boarder MR, Weisman GA, Turner JT, Wilkinson GF. G protein-coupled P2 purinoceptors: from molecular biology to functional responses. TiPS 1995; 16: 133-139.
30. Harden TK, Boyer JL, Nicholas RA. P2-purinergic receptors: subtype-associated signaling responses and structure. Ann Rev Pharmacol Toxicol 1995; 35: 541-579.
31. Yang CM, Tsai Y-J, Pan S-L, Tsai C-T, Wu W-B, Chiu C-T, Luo S-F, Ou JT. Purinoceptor-stimulated phosphoinositide hydrolysis in Madin-Darby canine kidney (MDCK) cells. Naunyn-Schmiedeberg's Arch Pharmacol 1997; 356: 1-7.
32. Boyer JL, Delaney SM, Villanueva D, Harden TK. A molecularly identified P2Y receptor simultaneously activates phospholipase C and inhibits adenylyl cyclase and is nonselectively activated by all nucleoside triphosphates. Mol Pharmacol 2000; 57: 805-810.
33. 14 receptor) adds diversity to the P2Y receptor family. TiPS 2003; 24: 52-55.
34. Evans RJ, Lewis C, Virginio C, Lundstrom K, Buell G, Surprenant, A., and North, RA. Ionic permeability of, and divalent cation effects on, two ATP-gated cation channels (P2X receptors) expressed in mammalian cells. J Physiol 1996; 497: 413-422.
35. 4- receptor. J. Pharmacol Exp Ther 1990; 255: 46-51.
36. Nakazawa K, Fujimori K, Takanaka A, Inoue K. An ATP-activated conductance in pheochromocytoma cells and its suppression by extracellular calcium. J Physiol 1990; 428: 257-272.
37. Sela D, Ram E, Atlas D. ATP receptor. A putative receptor-operated channel in PC-12 cells. J Biol Chem 1991; 266: 17990-17994.
38. Dubyak GR, El-Moatassim C. Signal transduction via P2-purinergic receptors for extracellular ATP and other nucleotides. Am J Physiol 1993; 265: C577-C606
39. Berridge MJ, Irvine RF. Inositol phosphates and cell signalling. Nature 1989; 341: 197-205.
40. 4- receptor-mediated permeabilization of transformed mouse fibroblasts and its desensitization. J Cell Physiol 1989; 139: 109-115.
41. 2 purinoceptor in transformed mouse fibroblasts. J Biol Chem 1990; 265: 7424-7431.
42. Khakh BS, Burnstock G, Kennedy C, King BF, North RA, Séguéla P, Voigt M, Humphrey PPA. International union of pharmacology. XXIV. Current status of the nomenclature and properties of P2X receptors and their subunits. Pharmacol Rev 2001; 53: 107-118.
43. Weisman GA, Dé BK, Friedberg I, Pritchard RS, Heppel LA. Cellular responses to external ATP which precede an increase in nucleotide permeability in transformed cells. J Cell Physiol 1984; 119: 211-219.
44. Gordon JL. Extracellular ATP: Effects, sources and fate. Biochem J 1986; 233: 309-319.
45. 7). Science 1996; 272: 735-738.
46. Neary JT, Rathbone MP, Cattabeni F, Abbracchio MP, Burnstock G. Trophic actions of extracellular nucleotides and nucleosides on glial and neuronal cells. Trends Neurosci 1996; 19: 13-18.
47. 7-like receptor activation in astrocytes increases chemokine monocyte chemoattractant protein-1 expression via mitogen-activated protein kinase. J Neurosci 2001; 21: 7135-7142.
48. 7. J Leukoc Biol 2002; 72: 222-232.
49. Cserr HF, Knopf PM Cervical lymphatics, the blood-brain barrier and the immunoreactivity of the brain: A new view. Immunol Today 1992; 13: 507-512.
50. Bechmann I, Mor G, Nilsen J, Eliza M, Nitsch R, Naftolin F. FasL (CD95L, Apo1L) is expressed in the normal rat and human brain: evidence for the existence of an immunological brain barrier. GLIA 1999; 27: 62-74.
51. Flügel A, Schwiger FW, Neumann H, Medana I, Willem M, Wekerle H, Kreutzberg GW, Graeber MB. Neuronal FasL induces cell death of encephalitogenic T lymphocytes. Brain Pathol 2000; 10: 353-364.
52. Streit WJ, Graeber MB, Kreutzberg GW. Functional plasticity of microglia: A review. Glia 1988; 1: 301-307.
53. Thomas WE. Brain macrophages: evaluation of microglia and their functions. Brain Res Rev 1992; 17: 61-74.
54. Kreutzberg GW. Microglia: A sensor for pathological events in the CNS. Trends Neurosci 1996; 19: 312-318.
55. El Khoury J, Hickman SE, Thomas CA, Loike JD, Silverstein SC. Microglia, scavenger receptors, and the pathogenesis of Alzheimer's disease. Neurobiol Aging 1998; 19: S81-S84.
56. Aloisi F. Immune function of microglia. GLIA 2001; 36: 165-179.
57. McGeer PL, Itagaki S, Boyes BE, McGeer EG. Reactive microglia are positive for HLA-DR in the substania nigra of Parkinson's and Alzheimer's disease. Neurology 1988; 38: 1285-1291.
58. Rogers J, Luber-Nardo J, Styren SD, Civin WH. Expression of immune system-associated antigens by cells of the central nervous system: relationship to the pathology of Alzheimer's disease. Neurobiol Aging 1988; 9: 339-349.
59. Hofman A, Schulte W, Tanja TA, van Duijn CM, Haaxma R, Lameris AJ, Otten VM, Saan RJ. History of dementia and Parkinson's disease in 1st-degree relatives of patients with Alzheimer's disease. Neurology 1989; 39: 1589-1592.
60. Goodwin JL, Uemura E, Cunnick JE. Microglial release of nitric oxide by the synergistic action of beta-amyloid and IFN gamma. Brain Res 1999; 692: 207-214.
61. Dong Y, Benveniste EN. Immune function of astrocytes. Glia 2001; 36: 180-190.
62. Ralevic V, Burnstock G. Receptors for purines and pyrimidines. Pharmacol Rev 1998; 50: 413-492.
63. Padeh S, Cohen A, Roifman CM. ATP-induced activation of human B lymphocytes via P2-purinoceptors. J Immunol 1991; 146: 1626-1632.
64. Schmidt A, Ortaldo JR, Herberman RB. Inhibition of human natural killer cell reactivity by exogenous adenosine 5′-triphosphate. J Immunol 1984; 132: 146-150.
65. Krishnaraj R. Negative modulation of human NK cell activity by purinoceptors. 1. Effect of exogenous adenosine triphosphate. Cell Immunol 1992; 141: 306-322.
66. 2+ by adenine nucleotides in human T-leukaemia cells: evidence for ADP-specific and P2y-purinergic receptors. Biochem J 1994; 304: 769-774.
67. Baricordi OR, Ferrari D, Melchiorri L, Chiozzi P, Hanau S, Chiari E, Rubini M, Di Virgilio F. An ATP-activated channel is involved in mitogenic stimulation of human T lymphocytes. Blood 1996; 87: 682-690.
68. Chow SC, Kass GE, Orrenius S. Purines and their roles in apoptosis. Neuropharmacol 1997; 36: 1149-1156.
69. Burnstock G. Purinergic signaling and vascular cell proliferation and death. Arterioscler Thromb Vasc Biol 2002; 22: 364-373
70. Freyer DR, Boxer LA, Axtell RA, Todd RF. 3rd. Stimulation of human neutrophil adhesive properties by adenine nucleotides. J Immunol 1988; 141: 580-586.
71. Ventura MA, Thomopoulos P. ADP and ATP activate distinct signaling pathways in human promonocytic U-937 cells differentiated with 1,25-dihydroxy-vitamin D3. Mol Pharmacol 1995; 47: 104-114.
72. Parker AL, Likar LL, Dawicki DD, Rounds S. Mechanism of ATP-induced leukocyte adherence to cultured pulmonary artery endothelial cells. Am J Physiol 1996; 270: L695-L703.
73. Eng LF, Reier PJ, Houle JD. Astrocyte activation and fibrous gliosis: glial fibrillary acidic protein immunostaining of astrocytes following intraspinal cord grafting of fetal CNS tissue. Prog Brain Res 1987; 71: 439-455.
74. Norenberg MD. Astrocyte responses to CNS injury. J. Neuropath Exp Neurol 1994; 53: 213-220.
75. + conductance in cultured microglial cells from mouse brain. J Neurosci 1993; 13: 4403-4411.
76. Ferrari D, Villalba M, Chiozzoni P, Falzoni S, Ricciardi-Castagnoli P, Di Virgilio F. Mouse microglial cells express a plasma membrane pore gated by extracellular ATP. J Immunol 1996; 156: 1531-1539.
77. Haas S, Brockhaus J, Verkhratsky A, Kettenmann H. ATP-induced membrane currents in ameboid microglia acutely isolated from mouse brain slices. Neurosci 1996; 75: 257-261.
78. King BF, Neary JT, Zhu Q, Wang S, Norenberg MD, Burnstock G. P2 purinoceptors in rat cortical astrocytes: expression, calcium-imaging and signalling studies. Neuroscience 1996; 74: 1187-1196.
79. Neary JT, Kang Y, Bu YR, Yu E, Akong K, Peters CM. Mitogenic signaling by ATP/P2Y purinergic receptors in astrocytes: Involvement of a calcium-independent protein kinase C, extracellular signal-regulated protein kinase pathway distinct from the phosphatidylinositol-specific phospholipase C calcium pathway. J Neurosci 1999; 19: 4211-4220.
80. Rathbone MP, Middlemiss PJ, Gysbers JW, Andrew C, Herman MAR, Reed JK, Ciccarelli R, Di Iorio P, Caciagli F. Trophic effects of purines in neurons and glial cells. Prog Neurobiol 1999; 59: 663-690.
81. Lenz G, Gottfried C, Luo Z, Avruch J, Rodnight R, Nie WJ, Kang Y, Neary JT. P2Y purinoceptor subtypes recruit different mek activators in astrocytes. Br J Pharmacol 2000; 129: 927-936.
82. Franke H, Krügel U, Schmidt R, Grosche J, Reichenbach A, Illes P. P2 receptor-types involved in astrogliosis in vivo. Br J Pharmacol 2001; 134: 1180-1189.
83. --dependent mechanism. GLIA 2002; 37: 8-18.
84. Ferrari D, Chiozzi P, Falzoni S, Hanau S, Di Virgilio F. Purinergic modulation of interleukin-1 beta release from microglial cells stimulated with bacterial endotoxin. J Exp Med 1997; 185: 579-582.
85. 7) receptor activation of microglia induces cell death via an interleukin-1-independent mechanism. Mol Cell Neurosci 2002; 19: 272-280.
86. 7 receptor channels. J Neurosci 2002; 22: 3061-3069.
87. Hide I, Tanaka M, Inoue A, Nakajima K, Kohsaka S, Inoue K, Nakata Y. Extracellular ATP triggers tumor necrosis factor-alpha release from rat microglia. J Neurochem 2000; 75: 965-972.
88. 2+-dependent plasminogen release from cultured microglia. Br J Pharmacol 1998; 123: 1304-1310
89. Yamakuni H, Kawaguchi N, Ohtani Y, Nakamura J, Katayama T, Nakagawa T, Minami M, Satoh M. ATP induces leukemia inhibitory factor mRNA in cultured rat astrocytes. J Neuroimmunol 2002; 129: 43-50.
90. Marzella PL, Gillespie LN, Clark GM, Bartlett PF, Kilpatrick TJ. The neurotrophins act synergistically with LIF and members of the TGF-beta superfamily to promote the survival of spiral ganglia neurons in vitro. Hearing Res 1999; 138: 73-80.
91. Di Iorio P, Caciagli F, Giuliani P, Ballerini P, Ciccarelli R, Sperling O, Zoref-Shani E, Benowitz L, Traversa U, Bombi G, Florio T, Virgilio A, Andrew CM, Crocker CE, Werstiuk ES, Middlemiss PJ, Rathbone MP. Purine nucleosides protect injured neurons and stimulate neuronal regeneration by intracellular and membrane receptor-mediated mechanisms. Drug Dev Res 2001; 52: 303-315.
92. Brambilla R, Burnstock G, Bonazzi A, Ceruti S, Cattabeni, F, Abbracchio MP. Cyclo-oxygenase-2 mediates P2Y receptor-induced reactive astrogliosis. Br J Pharmacol 1999; 126: 563-567.
93. James G, Butt AM. Changes in P2Y and P2X purinoceptors in reactive glia following axonal degeneration in the rat optic nerve. Neurosci Lett 2001; 312: 33-36.
94. Honda S, Sasaki Y, Ohsawa K, Imai Y, Nakamura Y, Inoue K, Kohsaka S. Extracellular ATP or ADP induce chemotaxis of cultured microglia through Gi/o-coupled P2Y receptors. J Neurosci 2001; 21: 1975-1982.
95. Shigemoto-Mogami Y, Koizumi S, Tsuda M, Ohsawa K, Kohsaka S, Inoue K. Mechanisms underlying extracellular ATP-evoked interleukin-6 release in mouse microglial cell line, MG-5. J Neurochem 2001; 78: 1339-1349.
96. Neary JT, Zhu Q. Signaling by ATP receptors in astrocytes. NeuroReport 1994; 5: 1617-1620.
97. 7 nucleotide receptor. J Biol Chem 2000; 275: 26792-26798
98. 7 receptors activate protein kinase D and p42/p44 mitogen-activated protein kinase (MAPK) downstream of protein kinase C. Biochem J 2002; 366: 745-755.
99. 7 receptor-mediated ERK1/2 phosphorylation in human astrocytoma cells. Am J Physiol 2003; 284: C571-C581.
100. Bruner G, Murphy S. Purinergic P2Y receptors on astrocytes are directly coupled to phospholipase A2. Glia 1993; 7: 219-224.
101. Bandeira-Melo C, Hall JC, Penrose JF, Weller PF. Cysteinyl leukotrienes induce IL-4 release from cord blood-derived human eosinophils. J Aller Clin Immunol 2002; 109: 975-979.
102. 4 nucleotide receptor. Br J Pharmacol 1998; 124: 428-430.
103. Lagraoui M, Gagnon L. Enhancement of human neutrophil survival and activation by TGF-beta 1. Cell Mol Biol 1997; 43: 313-318.
104. Robinson MJ, Cobb MH. Mitogen-activated protein kinase pathways. Curr Opin Cell Biol 1997; 9: 180-186.
105. MAPK pathway. J Biol Chem 1996; 271: 20608-20616
106. Reszka AA, Seger R, Diltz CD, Krebs EG, Fisher EH. Association of mitogen-activated protein kinase with the microtubule cytoskeleton. Proc Natl Acad Sci USA 1995; 92: 8881-8885.
107. Marshall CJ. Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 1995; 80: 179-185.
108. Neary JT. MAPK cascades in cell growth and death. News Physiol Sci 1997; 12: 286-293.
109. Xu J, Weng YI, Simonyi A, Krugh B, Liao Z, Weisman GA, Sun G. Role of PKC and MAPK in cytosolic PLA2 phosphorylation and arachidonic acid release in primary murine astrocytes. J Neurochem 2002; 83: 259-270.
110. Neary JT, Whittemore SR, Zhu Q, Norenberg MD. Synergistic activation of DNA synthesis in astrocytes by fibroblast growth factor and extracellular ATP. J Neurochem 1994; 63: 490-494.
111. Neary JT. Trophic actions of extracellular ATP: gene expression profiling by DNA array analysis. J Auton Nerv Syst 2000; 81: 200-204.
112. Brambilla R, Abbracchio MP. Modulation of cyclooxygenase-2 and brain reactive astrogliosis by purinergic P2 receptors. Ann NY Acad Sci 2001; 939: 54-62.
113. Gehrmann J, Banati RB, Wiessner C, Hossmann KA, Kreutzberg GW. Reactive microglia in cerebral ischaemia: an early mediator of tissue damage? Neuropathol Appl Neurobiol 1995; 21: 277-289.
114. Zhang P, Miller BS, Rosenzweig SA, Bhat NR. Activation of C-jun N-terminal kinase/stressr-activated protein kinase in primary glial cultures. J Neurosci Res 1996; 46: 114-121.
115. Zhang P, Hogan EL, Bhat NR. Activation of JNK/SAPK in primary glial cultures: II. Differential activation of kinase isoforms correspond to their differential expression. Neurochem Res 1998; 23: 219-225.
116. Hidding U, Mielke K, Waetzig V, Brecht S, Hanisch U, Behrens A, Wagner E, Herdegen T. The c-Jun N-terminal kinases in cerebral microglia: immunological functions in the brain. Biochem Pharmacol 2002; 64: 781-788.
117. Whitmarsh AJ, Davis RJ. Transcription factor AP-1 regulation by mitogen-activated protein kinase signal transduction pathways. J Mol Med 1996; 74: 589-607.
118. Ip YT, Davis RJ. Signal transduction by the c-Jun N-terminal kinase (JNK)-from inflammation to development. Curr Opin Cell Biol 1998; 10: 205-219.
119. Dong C, Davis RJ, Flavell RA. MAP kinases in the immune response., Ann Rev Immunol 2002; 20: 55-72.
120. Chen BC, Lin WW. PKC- and ERK-dependent activation of 1 kappa B kinase by lipopolysaccharide in macrophages: enhancement by P2Y receptor-mediated CaMK activation. Br J Pharmacol 2001; 134: 1055-1065.
121. Chen BC, Lin WW. Involvement of protein kinases in the potentiation of lipopolysaccharide-induced inflammatory mediator formation by thapsigargin in peritoneal macrophages. J Leukoc Biol 2001; 69: 280-288.
122. Ishizuka T, Terada N, Gerwins P, Hamelmann E, Oshiba A, Fanger GR, Johnson GL, Gelfand EW. Mast cell tumor necrosis factor alpha production is regulated by MEK kinases. Proc Nat Acad Sci USA 1997; 94: 6358-6363.
123. 2 nucleotide receptor signaling in human monocytic cells: activation, desensitization and coupling to mitogen-activated protein kinases. J Cell Physiol 2001; 187: 196-208.
124. 2 receptors in U937 monocytes. Drug Dev Res 1998; 45: 222-228.
125. 0-mediated signal transduction. J Cell Biol 2001; 153: 491-501
126. 2 receptors regulate multiple signal transduction pathways in monocytic cells. Drug Dev Res 2001; 53: 186-192.
127. Neary JT, McCarthy M, Cornell-Bell A, Kang Y. Trophic signaling pathways activated by purinergic receptors in rat and human astroglia. Prog Brain Res 1999; 120: 323-332.
128. 2 purinoreceptors in PC12 cells. Difference in purinoreceptor sensitivity in two PC12 cell lines. J Biol Chem 1998; 273: 19965-19971.
129. Manser E, Leung T, Sailhuddin H, Zhao ZS, Lim L. A brain serine/threonine protein kinase activity by Cdc42 and Rac1. Nature 1994; 367: 40-46.
130. 2+ signalling in glial cell pathology in the central nervous system. Eur J Pharmacol 2002; 447: 247-260.
131. Di Virgilio F, Chiozzi P, Ferrari D, Falzoni S, Sanz JM, Morelli A, Torboli M, Bolognesi G, Baricordi OR. Nucleotide receptors: an emerging family of regulatory molecules in blood cells. Blood 2001; 97: 587-600.
132. 7 receptors in neurodegeneration. Eur J Pharmacol 2002; 447: 261-269.
133. 7 receptor signalling complex. Embo J 2001; 20: 6347-6358.
134. 2 nucleotide receptor expression in the duct-ligated rat submandibular gland. Am J Phys 2000; 279: C286-C294.
135. 2 nucleotide receptors mediate uridine 5′-triphosphate-induced intimal hyperplasia in collared rabbit carotid arteries. Circ 2002; 106: 2720-2726.