P2X7 receptor activation induces inflammatory responses in salivary gland epithelium

American Journal of Physiology - Cell Physiology

Volumn 303, Issue 7, 2012, Pages

  Woods, Lucas T ^a,b   Camden, Jean M ^a,b   Batek, Josef M ^a   Petris, Michael J ^a,b   Erb, Laurie ^a,b   Weisman, Gary A ^a,b  

^a University of Missouri   (United States)

^b UNIVERSITY OF MISSOURI   (United States)

Author keywords

Apoptosis; Proinflammatory response; Salivary gland degeneration; Sjogren's syndrome

Indexed keywords

3' O (4 BENZOYL)BENZOYL ADENOSINE TRIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ALPHA FODRIN; CASPASE 3; CYTOSKELETON PROTEIN; INTERLEUKIN 1BETA CONVERTING ENZYME; PURINERGIC P2X7 RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; C57BL 6 MOUSE; CELL INFILTRATION; CONTROLLED STUDY; ENZYME ACTIVITY; EPITHELIUM; EPITHELIUM CELL; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN SECRETION; SALIVARY GLAND; SJOEGREN SYNDROME; SUBMANDIBULAR GLAND;

ADENOSINE TRIPHOSPHATE; ANIMALS; EPITHELIUM; INFLAMMATION MEDIATORS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, PURINERGIC P2X7; SALIVARY GLANDS; SUBMANDIBULAR GLAND;

MUS;

EID: 84867095238     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00072.2012     Document Type: Article

References (108)

1. Adinolfi E, Pizzirani C, Idzko M, Panther E, Norgauer J, Di Virgilio F, Ferrari D. P2X7 receptor: death or life? Purinergic Signal 1: 219-227, 2005.
2. Ahn JS, Camden JM, Schrader AM, Redman RS, Turner JT. Reversible regulation of P2Y2 nucleotide receptor expression in the duct-ligated rat submandibular gland. Am J Physiol Cell Physiol 279: C286-C294, 2000.
3. Arulkumaran N, Unwin RJ, Tam FW. A potential therapeutic role for P2X7 receptor (P2X7R) antagonists in the treatment of inflammatory diseases. Expert Opin Investig Drugs 20: 897-915, 2011.
4. Atkinson JC, Grisius M, Massey W. Salivary hypofunction and xerostomia: diagnosis and treatment. Dent Clin North Am 49: 309-326, 2005.
5. Avila JL, Grundmann O, Burd R, Limesand KH. Radiation-induced salivary gland dysfunction results from p53-dependent apoptosis. Int J Radiat Oncol Biol Phys 73: 523-529, 2009.
6. Baker OJ, Camden JM, Rome DE, Seye CI, Weisman GA. P2Y2 nucleotide receptor activation up-regulates vascular cell adhesion molecule-1 [corrected] expression and enhances lymphocyte adherence to a human submandibular gland cell line. Mol Immunol 45: 65-75, 2008.
7. Bortner CD, Oldenburg NB, Cidlowski JA. The role of DNA fragmentation in apoptosis. Trends Cell Biol 5: 21-26, 1995.
8. Bours MJ, Dagnelie PC, Giuliani AL, Wesselius A, Di Virgilio F. P2 receptors and extracellular ATP: a novel homeostatic pathway in inflam-mation. Front Biosci 3: 1443-1456, 2011.
9. Broderick MJ, Winder SJ. Towards a complete atomic structure of spectrin family proteins. J Struct Biol 137: 184-193, 2002.
10. Carpenter GH, Osailan SM, Correia P, Paterson KP, Proctor GB. Rat salivary gland ligation causes reversible secretory hypofunction. Acta Physiol (Oxf) 189: 241-249, 2007.
11. Chessell IP, Hatcher JP, Bountra C, Michel AD, Hughes JP, Green P, Egerton J, Murfin M, Richardson J, Peck WL, Grahames CB, Casula MA, Yiangou Y, Birch R, Anand P, Buell GN. Disruption of the P2X7 purinoceptor gene abolishes chronic inflammatory and neuropathic pain. Pain 114: 386-396, 2005.
12. Cohen GM. Caspases: the executioners of apoptosis. Biochem J 326: 1-16, 1997.
13. Coleman ML, Sahai EA, Yeo M, Bosch M, Dewar A, Olson MF. Membrane blebbing during apoptosis results from caspase-mediated activation of ROCK I. Nat Cell Biol 3: 339-345, 2001.
14. Collo G, Neidhart S, Kawashima E, Kosco-Vilbois M, North RA, Buell G. Tissue distribution of the P2X7 receptor. Neuropharmacology 36: 1277-1283, 1997.
15. Correia PN, Carpenter GH, Osailan SM, Paterson KL, Proctor GB. Acute salivary gland hypofunction in the duct ligation model in the absence of inflammation. Oral Dis 14: 520-528, 2008.
16. Deaglio S, Robson SC. Ectonucleotidases as regulators of purinergic signaling in thrombosis, inflammation, and immunity. Adv Pharmacol 61: 301-332, 2011.
17. Dehaye JP, Moran A, Marino A. Purines, a new class of agonists in salivary glands? Arch Oral Biol 44, Suppl 1: S39-43, 1999.
18. Di Virgilio F. ATP as a death factor. Biofactors 8: 301-303, 1998.
19. Di Virgilio F. Liaisons dangereuses: P2X7 and the inflammasome. Trends Pharmacol Sci 28: 465-472, 2007.
20. Dinarello CA. A clinical perspective of IL-1as the gatekeeper of inflammation. Eur J Immunol 41: 1203-1217, 2011.
21. Elliott MR, Chekeni FB, Trampont PC, Lazarowski ER, Kadl A, Walk SF, Park D, Woodson RI, Ostankovich M, Sharma P, Lysiak JJ, Harden TK, Leitinger N, Ravichandran KS. Nucleotides released by apoptotic cells act as a find-me signal to promote phagocytic clearance. Nature 461: 282-286, 2009.
22. Elmore S. Apoptosis: a review of programmed cell death. Toxicol Pathol 35: 495-516, 2007.
23. Erb L, Lustig KD, Ahmed AH, Gonzalez FA, Weisman GA. Covalent incorporation of 3′=-O-(4-benzoyl)benzoyl-ATP into a P2 purinoceptor in transformed mouse fibroblasts. J Biol Chem 265: 7424-7431, 1990.
24. Fan TJ, Han LH, Cong RS, Liang J. Caspase family proteases and apoptosis. Acta Biochim Biophys Sin (Shanghai) 37: 719-727, 2005.
25. Ferrari D, Pizzirani C, Adinolfi E, Lemoli RM, Curti A, Idzko M, Panther E, Di Virgilio F. The P2X7 receptor: a key player in IL-1 processing and release. J Immunol 176: 3877-3883, 2006.
26. Fitz JG. Regulation of cellular ATP release. Trans Am Clin Climatol Assoc 118: 199-208, 2007.
27. Fox PC. Acquired salivary dysfunction. Drugs and radiation. Ann NY Acad Sci 842: 132-137, 1998.
28. Fox RI, Kang HI. Pathogenesis of Sjogren's syndrome. Rheum Dis Clin North Am 18: 517-538, 1992.
29. Fox RI, Maruyama T. Pathogenesis and treatment of Sjogren's syndrome. Curr Opin Rheumatol 9: 393-399, 1997.
30. Friedle SA, Curet MA, Watters JJ. Recent patents on novel P2X7 receptor antagonists and their potential for reducing central nervous system inflammation. Recent Pat CNS Drug Discov 5: 35-45, 2010.
31. Garrett JR, Parsons PA. Changes in the main submandibular salivary duct of rabbits resulting from ductal ligation. Z Mikrosk Anat Forsch 93: 593-608, 1979.
32. Gonzalez FA, Ahmed AH, Lustig KD, Erb L, Weisman GA. Permeabilization of transformed mouse fibroblasts by 3′=-O-(4-benzoyl)benzoyl adenosine 5′=-triphosphate and the desensitization of the process. J Cell Physiol 139: 109-115, 1989.
33. Grundmann O, Fillinger JL, Victory KR, Burd R, Limesand KH. Restoration of radiation therapy-induced salivary gland dysfunction in mice by post therapy IGF-1 administration. BMC Cancer 10: 417, 2010.
34. Grundmann O, Mitchell GC, Limesand KH. Sensitivity of salivary glands to radiation: from animal models to therapies. J Dent Res 88: 894-903, 2009.
35. Hwang SM, Koo NY, Choi SY, Chun GS, Kim JS, Park K. P2X7 receptor-mediated membrane blebbing in salivary epithelial cells. Korean J Physiol Pharmacol 13: 175-179, 2009.
36. Hwang SM, Li J, Koo NY, Choi SY, Lee SJ, Oh SB, Castro R, Kim JS, Park K. Role of purinergic receptor in-fodrin degradation in Par C5 cells. J Dent Res 88: 927-932, 2009.
37. Janicke RU, Ng P, Sprengart ML, Porter AG. Caspase-3 is required for-fodrin cleavage but dispensable for cleavage of other death sub-strates in apoptosis. J Biol Chem 273: 15540-15545, 1998.
38. Jin C, Flavell RA. Molecular mechanism of NLRP3 inflammasome activation. J Clin Immunol 30: 628-631, 2010.
39. Khakh BS, North RA. P2X receptors as cell-surface ATP sensors in health and disease. Nature 442: 527-532, 2006.
40. Kong L, Ogawa N, McGuff HS, Nakabayashi T, Sakata KM, Masago R, Vela-Roch N, Talal N, Dang H. Bcl-2 family expression in salivary glands from patients with primary Sjogren's syndrome: involvement of Bax in salivary gland destruction. Clin Immunol Immunopathol 88: 133-141, 1998.
41. Kong Q, Wang M, Liao Z, Camden JM, Yu S, Simonyi A, Sun GY, Gonzalez FA, Erb L, Seye CI, Weisman GA. P2X7 nucleotide receptors mediate caspase-8/9/3-dependent apoptosis in rat primary cortical neurons. Purinergic Signal 1: 337-347, 2005.
42. Labasi JM, Petrushova N, Donovan C, McCurdy S, Lira P, Payette MM, Brissette W, Wicks JR, Audoly L, Gabel CA. Absence of the P2X7 receptor alters leukocyte function and attenuates an inflammatory response. J Immunol 168: 6436-6445, 2002.
43. Leybaert L, Braet K, Vandamme W, Cabooter L, Martin PE, Evans WH. Connexin channels, connexin mimetic peptides and ATP release. Cell Commun Adhes 10: 251-257, 2003.
44. Limesand KH, Said S, Anderson SM. Suppression of radiation-induced salivary gland dysfunction by IGF-1. PLos One 4: e4663, 2009.
45. Limesand KH, Schwertfeger KL, Anderson SM. MDM2 is required for suppression of apoptosis by activated Akt1 in salivary acinar cells. Mol Cell Biol 26: 8840-8856, 2006.
46. Lister MF, Sharkey J, Sawatzky DA, Hodgkiss JP, Davidson DJ, Rossi AG, Finlayson K. The role of the purinergic P2X7 receptor in inflammation. J Inflamm 4: 5, 2007.
47. Lucattelli M, Cicko S, Muller T, Lommatzsch M, De Cunto G, Cardini S, Sundas W, Grimm M, Zeiser R, Durk T, Zissel G, Sorichter S, Ferrari D, Di Virgilio F, Virchow JC, Lungarella G, Idzko M. P2X7 receptor signaling in the pathogenesis of smoke-induced lung inflammation and emphysema. Am J Respir Cell Mol Biol 44: 423-429, 2011.
48. Luttikhuizen DT, Harmsen MC, de Leij LF, van Luyn MJ. Expression of P2 receptors at sites of chronic inflammation. Cell Tissue Res 317: 289-298, 2004.
49. Martinez JR, Bylund DB, Cassity N. Progressive secretory dysfunction in the rat submandibular gland after excretory duct ligation. Arch Oral Biol 27: 443-450, 1982.
50. Matsuzaki T, Suzuki T, Koyama H, Tanaka S, Takata K. Aquaporin-5 (AQP5), a water channel protein, in the rat salivary and lacrimal glands: immunolocalization and effect of secretory stimulation. Cell Tissue Res 295: 513-521, 1999.
51. McGaraughty S, Chu KL, Namovic MT, Donnelly-Roberts DL, Harris RR, Zhang XF, Shieh CC, Wismer CT, Zhu CZ, Gauvin DM, Fabiyi AC, Honore P, Gregg RJ, Kort ME, Nelson DW, Carroll WA, Marsh K, Faltynek CR, Jarvis MF. P2X7-related modulation of pathological nociception in rats. Neuroscience 146: 1817-1828, 2007.
52. Melani A, Corti F, Stephan H, Muller CE, Donati C, Bruni P, Vannucchi MG, Pedata F. Ecto-ATPase inhibition: ATP and adenosine release under physiological and ischemic in vivo conditions in the rat striatum. Exp Neurol 233: 193-204, 2012.
53. Melvin JE, Yule D, Shuttleworth T, Begenisich T. Regulation of fluid and electrolyte secretion in salivary gland acinar cells. Annu Rev Physiol 67: 445-469, 2005.
54. Miyazaki K, Takeda N, Ishimaru N, Omotehara F, Arakaki R, Hayashi Y. Analysis of in vivo role of-fodrin autoantigen in primary Sjogren's syndrome. Am J Pathol 167: 1051-1059, 2005.
55. Montalbetti N, Leal Denis MF, Pignataro OP, Kobatake E, Lazarowski ER, Schwarzbaum PJ. Homeostasis of extracellular ATP in human erythrocytes. J Biol Chem 286: 38397-38407, 2011.
56. Morel O, Morel N, Jesel L, Freyssinet JM, Toti F. Microparticles: a critical component in the nexus between inflammation, immunity, and thrombosis. Semin Immunopathol 33: 469-486, 2011.
57. Morelli A, Chiozzi P, Chiesa A, Ferrari D, Sanz JM, Falzoni S, Pinton P, Rizzuto R, Olson MF, Di Virgilio F. Extracellular ATP causes ROCK I-dependent bleb formation in P2X7-transfected HEK293 cells. Mol Biol Cell 14: 2655-2664, 2003.
58. Nakamoto T, Brown DA, Catalan MA, Gonzalez-Begne M, Romanenko VG, Melvin JE. Purinergic P2X7 receptors mediate ATP-induced saliva secretion by the mouse submandibular gland. J Biol Chem 284: 4815-4822, 2009.
59. Novak I. Purinergic receptors in the endocrine and exocrine pancreas. Purinergic Signal 4: 237-253, 2008.
60. Novak I, Jans IM, Wohlfahrt L. Effect of P2X7 receptor knockout on exocrine secretion of pancreas, salivary glands and lacrimal glands. J Physiol 588: 3615-3627, 2010.
61. Ohshima Y, Tsukimoto M, Takenouchi T, Harada H, Suzuki A, Sato M, Kitani H, Kojima S. γ-Irradiation induces P2X7 receptor-dependent ATP release from B16 melanoma cells. Biochim Biophys Acta 1800: 40-46, 2009.
62. Oxholm P, Daniels TE, Bendtzen K. Cytokine expression in labial salivary glands from patients with primary Sjogren's syndrome. Autoimmunity 12: 185-191, 1992.
63. Panupinthu N, Zhao L, Possmayer F, Ke HZ, Sims SM, Dixon SJ. P2X7 nucleotide receptors mediate blebbing in osteoblasts through a pathway involving lysophosphatidic acid. J Biol Chem 282: 3403-3412, 2007.
64. Pelegrin P, Surprenant A. Pannexin-1 mediates large pore formation and interleukin-1 release by the ATP-gated P2X7 receptor. EMBO J 25: 5071-5082, 2006.
65. Pellegatti P, Raffaghello L, Bianchi G, Piccardi F, Pistoia V, Di Virgilio F. Increased level of extracellular ATP at tumor sites: in vivo imaging with plasma membrane luciferase. PLos One 3: e2599, 2008.
66. Pfeiffer ZA, Aga M, Prabhu U, Watters JJ, Hall DJ, Bertics PJ. The nucleotide receptor P2X7 mediates actin reorganization and membrane blebbing in RAW 264.7 macrophages via p38 MAP kinase and Rho. J Leukoc Biol 75: 1173-1182, 2004.
67. Pizzirani C, Ferrari D, Chiozzi P, Adinolfi E, Sandona D, Savaglio E, Di Virgilio F. Stimulation of P2 receptors causes release of IL-1 -loaded microvesicles from human dendritic cells. Blood 109: 3856-3864, 2007.
68. Pochet S, Garcia-Marcos M, Seil M, Otto A, Marino A, Dehaye JP. Contribution of two ionotropic purinergic receptors to ATP responses in submandibular gland ductal cells. Cell Signal 19: 2155-2164, 2007.
69. Qu Y, Dubyak GR. P2X7 receptors regulate multiple types of membrane trafficking responses and non-classical secretion pathways. Purinergic Signal 5: 163-173, 2009.
70. Qu Y, Franchi L, Nunez G, Dubyak GR. Nonclassical IL-1 secretion stimulated by P2X7 receptors is dependent on inflammasome activation and correlated with exosome release in murine macrophages. J Immunol 179: 1913-1925, 2007.
71. Qu Y, Misaghi S, Newton K, Gilmour LL, Louie S, Cupp JE, Dubyak GR, Hackos D, Dixit VM. Pannexin-1 is required for ATP release during apoptosis but not for inflammasome activation. J Immunol 186: 6553-6561, 2011.
72. Ramachandra L, Qu Y, Wang Y, Lewis CJ, Cobb BA, Takatsu K, Boom WH, Dubyak GR, Harding CV. Mycobacterium tuberculosis synergizes with ATP to induce release of microvesicles and exosomes containing major histocompatibility complex class II molecules capable of antigen presentation. Infect Immun 78: 5116-5125, 2010.
73. Ratchford AM, Baker OJ, Camden JM, Rikka S, Petris MJ, Seye CI, Erb L, Weisman GA. P2Y2 nucleotide receptors mediate metalloprotease-dependent phosphorylation of epidermal growth factor receptor and ErbB3 in human salivary gland cells. J Biol Chem 285: 7545-7555, 2010.
74. Riteau N, Gasse P, Fauconnier L, Gombault A, Couegnat M, Fick L, Kanellopoulos J, Quesniaux VF, Marchand-Adam S, Crestani B, Ryffel B, Couillin I. Extracellular ATP is a danger signal activating P2X7 receptor in lung inflammation and fibrosis. Am J Respir Crit Care Med 182: 774-783, 2010.
75. Roescher N, Tak PP, Illei GG. Cytokines in Sjogren's syndrome. Oral Dis 15: 519-526, 2009.
76. Roger S, Pelegrin P, Surprenant A. Facilitation of P2X7 receptor currents and membrane blebbing via constitutive and dynamic calmodulin binding. J Neurosci 28: 6393-6401, 2008.
77. Saribas AS, Lustig KD, Zhang X, Weisman GA. Extracellular ATP reversibly increases the plasma membrane permeability of transformed mouse fibroblasts to large macromolecules. Anal Biochem 209: 45-52, 1993.
78. Schrader AM, Camden JM, Weisman GA. P2Y2 nucleotide receptor up-regulation in submandibular gland cells from the NOD. B10 mouse model of Sjogren's syndrome. Arch Oral Biol 50: 533-540, 2005.
79. Schulze-Lohoff E, Hugo C, Rost S, Arnold S, Gruber A, Brune B, Sterzel RB. Extracellular ATP causes apoptosis and necrosis of cultured mesangial cells via P2Z/P2X7 receptors. Am J Physiol Renal Physiol 275: F962-F971, 1998.
80. Seil M, Fontanils U, Etxebarria IG, Pochet S, Garcia-Marcos M, Marino A, Dehaye JP. Pharmacological evidence for the stimulation of NADPH oxidase by P2X7 receptors in mouse submandibular glands. Purinergic Signal 4: 347-355, 2008.
81. Shiba R, Hamada T, Kawakatsu K. Histochemical and electron microscopical studies on the effect of duct ligation of rat salivary glands. Arch Oral Biol 17: 299-309, 1972.
82. Shibata Y, Hishikawa Y, Izumi S, Fujita S, Yamaguchi A, Koji T. Involvement of Fas/Fas ligand in the induction of apoptosis in chronic sialadenitis of minor salivary glands including Sjogren's syndrome. Hum Cell 15: 52-60, 2002.
83. Skaper SD, Debetto P, Giusti P. The P2X7 purinergic receptor: from physiology to neurological disorders. FASEB J 24: 337-345, 2009.
84. Sperlagh B, Vizi ES, Wirkner K, Illes P. P2X7 receptors in the nervous system. Prog Neurobiol 78: 327-346, 2006.
85. Stagg J, Smyth MJ. Extracellular adenosine triphosphate and adenosine in cancer. Oncogene 29: 5346-5358, 2010.
86. Sugiyama T, Oku H, Shibata M, Fukuhara M, Yoshida H, Ikeda T. Involvement of P2X7 receptors in the hypoxia-induced death of rat retinal neurons. Invest Ophthalmol Vis Sci 51: 3236-3243, 2010.
87. Sumida T, Matsumoto I, Murata H, Namekawa T, Matsumura R, Tomioka H, Iwamoto I, Saito Y, Mizushima Y, Hasunuma T, Maeda T, Nishioka K. TCR in Fas-sensitive T cells from labial salivary glands of patients with Sjogren's syndrome. J Immunol 158: 1020-1025, 1997.
88. Takenouchi T, Sugama S, Iwamaru Y, Hashimoto M, Kitani H. Modulation of the ATP-lnduced release and processing of IL-1. in microglial cells. Crit Rev Immunol 29: 335-345, 2009.
89. Tamarin A. The leukocytic response in ligated rat submandibular glands. J Oral Pathol Med 8: 293-304, 1979.
90. Taylor SR, Gonzalez-Begne M, Dewhurst S, Chimini G, Higgins CF, Melvin JE, Elliott JI. Sequential shrinkage and swelling underlie P2X7-stimulated lymphocyte phosphatidylserine exposure and death. J Immunol 180: 300-308, 2008.
91. Thery C. Exosomes: secreted vesicles and intercellular communications. F1000 Biol Rep 3: 15, 2011.
92. Trautmann A. Extracellular ATP in the immune system: more than just a "danger signal". Sci Signal 2: pe6, 2009.
93. Tripathi A, Chaube SK. High cytosolic free calcium level signals apoptosis through mitochondria-caspase mediated pathway in rat eggs cultured in vitro. Apoptosis 17: 439-448, 2012.
94. Tschopp J, Schroder K. NLRP3 inflammasome activation: The convergence of multiple signalling pathways on ROS production? Nat Rev Immunol 10: 210-215, 2010.
95. Tsuda M, Tozaki-Saitoh H, Inoue K. Pain and purinergic signaling. Brain Res Rev 63: 222-232, 2009.
96. Turner CM, Tam FW, Lai PC, Tarzi RM, Burnstock G, Pusey CD, Cook HT, Unwin RJ. Increased expression of the pro-apoptotic ATP-sensitive P2X7 receptor in experimental and human glomerulonephritis. Nephrol Dial Transplant 22: 386-395, 2007.
97. Turne JT, Landon LA, Gibbons SJ, Talamo BR. Salivary gland P2 nucleotide receptors. Crit Rev Oral Biol Med 10: 210-224, 1999.
98. Turner JT, Weisman GA, Camden JM. Upregulation of P2Y2 nucleotide receptors in rat salivary gland cells during short-term culture. Am J Physiol Cell Physiol 273: C1100-C1107, 1997.
99. Ulukaya E, Acilan C, Yilmaz Y. Apoptosis: why and how does it occur in biology? Cell Biochem Funct 29: 468-480, 2011.
100. Uratsuji H, Tada Y, Kawashima T, Kamata M, Hau CS, Asano Y, Sugaya M, Kadono T, Asahina A, Sato S, Tamaki K. P2Y6 receptor signaling pathway mediates inflammatory responses induced by monosodium urate crystals. J Immunol 188: 436-444, 2012.
101. Varani K, De Mattei M, Vincenzi F, Tosi A, Targa M, Masieri FF, Pellati A, Massari L, Borea PA. P2X1 and P2X3 purinergic receptors differentially modulate the inflammatory response in human osteoar. thritic synovial fibroblasts. Cell Physiol Biochem 25: 325-336, 2010.
102. Verderio C, Matteoli M. ATP mediates calcium signaling between astrocytes and microglial cells: modulation by IFN-γ. J Immunol 166: 6383-6391, 2001.
103. Verhoef PA, Estacion M, Schilling W, Dubyak GR. P2X7 receptor. dependent blebbing and the activation of Rho-effector kinases, caspases, and IL-1 release. J Immunol 170: 5728-5738, 2003.
104. Wang Q, Wang L, Feng YH, Li X, Zeng R, Gorodeski GI. P2X7 . receptor-mediated apoptosis of human cervical epithelial cells. Am J Physiol Cell Physiol 287: C1349-C1358, 2004.
105. Weisman GA, De BK, Pritchard RS. Ionic dependence of the extra. cellular ATP-induced permeabilization of transformed mouse fibroblasts: role of plasma membrane activities that regulate cell volume. J Cell Physiol 138: 375-383, 1989.
106. Weisman GA, Dunn SD, De BK, Kitagawa T, Friedberg I. On the role . of protein phosphorylation in the ATP-dependent permeabilization of transformed cells. J Cell Physiol 118: 124-132, 1984.
107. Wiley JS, Sluyter R, Gu BJ, Stokes L, Fuller SJ. The human P2X7 . receptor and its role in innate immunity. Tissue Antigens 78: 321-332, 2011.
108. Wilson HL, Wilson SA, Surprenant A, North RA. Epithelial . membrane proteins induce membrane blebbing and interact with the P2X7 receptor C terminus. J Biol Chem 277: 34017-34023, 2002.