A new role for P2X4 receptors as modulators of lung surfactant secretion

Frontiers in Cellular Neuroscience

Volumn , Issue OCT, 2013, Pages

  Miklavc, Pika ^a   Thompson, Kristin E ^a   Frick, Manfred ^a  

^a UNIVERSITY OF ULM   (Germany)

Author keywords

Alveolar epithelial cell; Calcium; Cellular secretion; Exocytosis; Lamellar body; P2X4 receptor; Pulmonary surfactant

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM; LUNG SURFACTANT; PURINERGIC P2X RECEPTOR; PURINERGIC P2X4 RECEPTOR;

CALCIUM TRANSPORT; CELL MEMBRANE; CELL ORGANELLE; CELL TYPE; CELLULAR SECRETION; EXOCYTOSIS; HUMAN; LAMELLAR BODY; LUNG ALVEOLITIS; LUNG ALVEOLUS CELL TYPE 2; NEUROMODULATION; REVIEW;

EID: 84886821958     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2013.00171     Document Type: Review

References (93)

1. Adriaensen, D., and Timmermans, J. P. (2004). Purinergic signalling in the lung: important in asthma and COPD? Curr. Opin. Pharmacol. 4, 207-214. doi: 10.1016/j.coph.2004.01.010
2. Andreeva, A. V., Kutuzov, M. A., and Voyno-Yasenetskaya, T. A. (2007). Regulation of surfactant secretion in alveolar type II cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 293, L259-L271. doi: 10.1152/ajplung.00112.2007
3. Belete, H. A., Hubmayr, R. D., Wang, S., and Singh, R. D. (2011). The role of purinergic signaling on deformation induced injury and repair responses of alveolar epithelial cells. PLoS ONE 6:e27469. doi: 10.1371/journal.pone.0027469
4. Bhattacharya, S., Verrill, D. S., Carbone, K. M., Brown, S., Yule, D. I., and Giovannucci, D. R. (2012). Distinct contributions by ionotropic purinoceptor subtypes to ATP-evoked calcium signals in mouse parotid acinar cells. J. Physiol. 590, 2721-2737. doi: 10.1113/jphysiol.2012.228148
5. Blott, E. J., and Griffiths, G. M. (2002). Secretory lysosomes. Nat. Rev. Mol. Cell Biol.3, 122-131. doi: 10.1038/nrm732
6. Bodin, P., and Burnstock, G. (2001). Purinergic signalling: ATP release. Neurochem. Res. 26, 959-969. doi: 10.1023/A:1012388618693
7. Bove, P. F., Grubb, B. R., Okada, S. F., Ribeiro, C. M., Rogers, T. D., Randell, S. H., et al. (2010). Human alveolar type II cells secrete and absorb liquid in response to local nucleotide signaling. J. Biol. Chem. 285, 34939-34949. doi: 10.1074/jbc.M110.162933
8. Brake, A. J., Wagenbach, M. J., and Julius, D. (1994). New structural motif for ligand-gated ion channels defined by an ionotropic ATP receptor. Nature 371, 519-523. doi: 10.1038/371519a0
9. Brunschweiger, A., and Muller, C. E. (2006). P2 receptors activated by uracil nucleotides-an update. Curr. Med. Chem. 13, 289-312. doi: 10.2174/092986706775476052
10. Burgoyne, R. D., and Morgan, A. (1998). Calcium sensors in regulated exocytosis. Cell Calcium 24, 367-376. doi: 10.1016/S0143-4160(98)90060-4
11. Burnstock, G., Brouns, I., Adriaensen, D., and Timmermans, J. P. (2012). Purinergic signaling in the airways. Pharmacol. Rev. 64, 834-868. doi: 10.1124/pr.111.005389
12. Burnstock, G., and Kennedy, C. (2011). P2X receptors in health and disease. Adv. Pharmacol. 61, 333-372. doi: 10.1016/B978-0-12-385526-8.00011-4
13. Chander, A., Johnson, R. G., Reicherter, J., and Fisher, A. B. (1986). Lung lamellar bodies maintain an acidic internal pH. J. Biol. Chem. 261, 6126-6131.
14. 4 purinoceptor removes extracellular pH sensitivity. J. Physiol. 523(Pt 3), 697-703. doi: 10.1111/j.1469-7793.2000.00697.x
15. Cockcroft, S., and Gomperts, B. D. (1979a). Activation and inhibition of calcium-dependent histamine secretion by ATP ions applied to rat mast cells. J. Physiol. 296, 229-243.
16. Cockcroft, S., and Gomperts, B. D. (1979b). ATP induces nucleotide permeability in rat mast cells. Nature 279, 541-542. doi: 10.1038/279541a0
17. Cockcroft, S., and Gomperts, B. D. (1980). The ATP4-receptor of rat mast cells. Biochem. J. 188, 789-798.
18. Coddou, C., Yan, Z., Obsil, T., Huidobro-Toro, J. P., and Stojilkovic, S. S. (2011). Activation and regulation of purinergic P2X receptor channels. Pharmacol. Rev. 63, 641-683. doi: 10.1124/pr.110.003129
19. Dell'Angelica, E. C., Mullins, C., Caplan, S., and Bonifacino, J. S. (2000). Lysosome-related organelles. FASEB J. 14, 1265-1278. doi: 10.1096/fj.14.10.1265
20. Diamant, B., and Kruger, P. G. (1967). Histamine release from isolated rat peritoneal mast cells induced by adenosine-5′-triphosphate. Acta Physiol. Scand. 71, 291-302. doi: 10.1111/j.1748-1716.1967.tb03736.x
21. Dietl, P., Frick, M., Mair, N., Bertocchi, C., and Haller, T. (2004). Pulmonary consequences of a deep breath revisited. Biol. Neonate 85, 299-304. doi: 10.1159/000078176
22. Dietl, P., and Haller, T. (2005). Exocytosis of lung surfactant: from the secretory vesicle to the air-liquid interface. Annu. Rev. Physiol. 67, 595-621. doi: 10.1146/annurev.physiol.67.040403.102553
23. 2+) in surfactant secreting pulmonary alveolar type II pneumocytes. Cell Calcium 52, 296-302. doi: 10.1016/j.ceca.2012.04.010
24. Dietl, P., Haller, T., Mair, N., and Frick, M. (2001). Mechanisms of surfactant exocytosis in alveolar type II cells in vitro and in vivo. News Physiol. Sci. 16, 239-243.
25. Dietl, P., Liss, B., Felder, E., Miklavc, P., and Wirtz, H. (2010). Lamellar body exocytosis by cell stretch or purinergic stimulation: possible physiological roles, messengers and mechanisms. Cell. Physiol. Biochem. 25, 1-12. doi: 10.1159/000272046
26. Dolensek, J., Skelin, M., and Rupnik, M. S. (2011). Calcium dependencies of regulated exocytosis in different endocrine cells. Physiol. Res. 60(Suppl. 1), S29-S38.
27. Egan, T. M., and Khakh, B. S. (2004). Contribution of calcium ions to P2X channel responses. J. Neurosci. 24, 3413-3420. doi: 10.1523/JNEUROSCI.5429-03.2004
28. Folkesson, H. G., and Matthay, M. A. (2006). Alveolar epithelial ion and fluid transport: recent progress. Am. J. Respir. Cell Mol. Biol. 35, 10-19. doi: 10.1165/rcmb.2006-0080SF
29. 2+ entry is essential for cell strain-induced lamellar body fusion in isolated rat type II pneumocytes. Am. J. Physiol. Lung Cell. Mol. Physiol. 286, L210-L220. doi: 10.1152/ajplung.00332.2003
30. Frick, M., Eschertzhuber, S., Haller, T., Mair, N., and Dietl, P. (2001). Secretion in alveolar type II cells at the interface of constitutive and regulated exocytosis. Am. J. Respir. Cell Mol. Biol. 25, 306-315. doi: 10.1165/ajrcmb.25.3.4493
31. 4 receptor reveals pharmacological differences to the rat homologue. Mol. Pharmacol. 51, 109-118.
32. Garcia-Verdugo, I., Ravasio, A., De Paco, E. G., Synguelakis, M., Ivanova, N., Kanellopoulos, J., et al. (2008). Long-term exposure to LPS enhances the rate of stimulated exocytosis and surfactant secretion in alveolar type II cells and upregulates P2Y2 receptor expression. Am. J. Physiol. Lung Cell. Mol. Physiol. 295, L708-L717. doi: 10.1152/ajplung.00536.2007
33. Geisler, J. C., Corbin, K. L., Li, Q., Feranchak, A. P., Nunemaker, C. S., and Li, C. (2013). Vesicular nucleotide transporter-mediated ATP release regulates insulin secretion. Endocrinology 154, 675-684. doi: 10.1210/en.2012-1818
34. Gu, J. G., and MacDermott, A. B. (1997). Activation of ATP P2X receptors elicits glutamate release from sensory neuron synapses. Nature 389, 749-753. doi: 10.1038/39639
35. Gutierrez-Martin, Y., Bustillo, D., Gomez-Villafuertes, R., Sanchez-Nogueiro, J., Torregrosa-Hetland, C., Binz, T., et al. (2011). P2X7 receptors trigger ATP exocytosis and modify secretory vesicle dynamics in neuroblastoma cells. J. Biol. Chem. 286, 11370-11381. doi: 10.1074/jbc.M110.139410
36. 2+-dependent process regulating secretion from alveolar type II cells. J. Cell Biol. 155, 279-289. doi: 10.1083/jcb.200102106
37. Haller, T., Dietl, P., Stockner, H., Frick, M., Mair, N., Tinhofer, I., et al. (2004). Tracing surfactant transformation from cellular release to insertion into an air-liquid interface. Am. J. Physiol. Lung Cell. Mol. Physiol. 286, L1009-L1015. doi: 10.1152/ajplung.00342.2003
38. Hayoz, S., Jia, C., and Hegg, C. (2012). Mechanisms of constitutive and ATP-evoked ATP release in neonatal mouse olfactory epithelium. BMC Neurosci. 13:53. doi: 10.1186/1471-2202-13-53
39. Huang, Y. A., Stone, L. M., Pereira, E., Yang, R., Kinnamon, J. C., Dvoryanchikov, G., et al. (2011). Knocking out P2X receptors reduces transmitter secretion in taste buds.J. Neurosci. 31, 13654-13661. doi: 10.1523/JNEUROSCI.3356-11.2011
40. Jacques-Silva, M. C., Correa-Medina, M., Cabrera, O., Rodriguez-Diaz, R., Makeeva, N., Fachado, A., et al. (2010). ATP-gated P2X3 receptors constitute a positive autocrine signal for insulin release in the human pancreatic beta cell. Proc. Natl. Acad. Sci. U.S.A. 107, 6465-6470. doi: 10.1073/pnas.0908935107
41. Kaczmarek-Hajek, K., Lorinczi, E., Hausmann, R., and Nicke, A. (2012). Molecular and functional properties of P2X receptors-recent progress and persisting challenges. Purinergic Signal. 8, 375-417. doi: 10.1007/s11302-012-9314-7
42. Khakh, B. S., and North, R. A. (2006). P2X receptors as cell-surface ATP sensors in health and disease. Nature 442, 527-532. doi: 10.1038/nature04886
43. 4) receptor channels. J. Neurosci. 19, 7289-7299.
44. 2+ signals and exocytosis in rat prostate neuroendocrine cells. J. Biol. Chem. 279, 27345-27356. doi: 10.1074/jbc.M313575200
45. Kreda, S. M., Seminario-Vidal, L., Van Heusden, C. A., O'Neal, W., Jones, L., Boucher, R. C., et al. (2010). Receptor-promoted exocytosis of airway epithelial mucin granules containing a spectrum of adenine nucleotides. J. Physiol. 588, 2255-2267. doi: 10.1113/jphysiol.2009.186643
46. Lazarowski, E. R., Sesma, J. I., Seminario-Vidal, L., and Kreda, S. M. (2011). Molecular mechanisms of purine and pyrimidine nucleotide release. Adv. Pharmacol. 61, 221-261. doi: 10.1016/B978-0-12-385526-8.00008-4
47. Lazarowski, E. R., Watt, W. C., Stutts, M. J., Boucher, R. C., and Harden, T. K. (1995). Pharmacological selectivity of the cloned human P2U-purinoceptor: potent activation by diadenosine tetraphosphate. Br. J. Pharmacol. 116, 1619-1627. doi: 10.1111/j.1476-5381.1995.tb16382.x
48. Lommatzsch, M., Cicko, S., Muller, T., Lucattelli, M., Bratke, K., Stoll, P., et al. (2010). Extracellular adenosine triphosphate and chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 181, 928-934. doi: 10.1164/rccm.200910-1506OC
49. Lucattelli, M., Cicko, S., Muller, T., Lommatzsch, M., De Cunto, G., Cardini, S., et al. (2011). P2X7 receptor signaling in the pathogenesis of smoke-induced lung inflammation and emphysema. Am. J. Respir. Cell Mol. Biol. 44, 423-429. doi: 10.1165/rcmb.2010-0038OC
50. Luzio, J. P., Pryor, P. R., and Bright, N. A. (2007). Lysosomes: fusion and function. Nat. Rev. Mol. Cell Biol. 8, 622-632. doi: 10.1038/nrm2217
51. MacKenzie, A., Wilson, H. L., Kiss-Toth, E., Dower, S. K., North, R. A., and Surprenant, A. (2001). Rapid secretion of interleukin-1beta by microvesicle shedding. Immunity15, 825-835. doi: 10.1016/S1074-7613(01)00229-1
52. Miklavc, P., Albrecht, S., Wittekindt, O. H., Schullian, P., Haller, T., and Dietl, P. (2009). Existence of exocytotic hemifusion intermediates with a lifetime of up to seconds in type II pneumocytes. Biochem. J. 424, 7-14. doi: 10.1042/BJ20091094
53. Miklavc, P., and Frick, M. (2011). Vesicular calcium channels as regulators of the exocytotic post-fusion phase. Commun. Integr. Biol. 4, 796-798.
54. 2+) during the post-fusion stage of lamellar body exocytosis in rat type II pneumocytes. PLoS ONE 5:e10982. doi: 10.1371/journal.pone.0010982
55. Miklavc, P., Hecht, E., Hobi, N., Wittekindt, O. H., Dietl, P., Kranz, C., et al. (2012). Actin coating and compression of fused secretory vesicles are essential for surfactant secretion-a role for Rho, formins and myosin II. J. Cell Sci. 125, 2765-2774. doi: 10.1242/jcs.105262
56. 4 receptors promotes fusion pore opening and exocytotic content release in pneumocytes. Proc. Natl. Acad. Sci. U.S.A.108, 14503-14508. doi: 10.1073/pnas.1101039108
57. Mishra, A., Chintagari, N. R., Guo, Y., Weng, T., Su, L., and Liu, L. (2011). Purinergic P2X7 receptor regulates lung surfactant secretion in a paracrine manner. J. Cell Sci.124, 657-668. doi: 10.1242/jcs.066977
58. Neher, E., and Sakaba, T. (2008). Multiple roles of calcium ions in the regulation of neurotransmitter release. Neuron 59, 861-872. doi: 10.1016/j.neuron.2008.08.019
59. North, R. A. (2002). Molecular physiology of P2X receptors. Physiol. Rev. 82, 1013-1067.
60. Novak, I. (2011). Purinergic signalling in epithelial ion transport: regulation of secretion and absorption. Acta Physiol. (Oxf.) 202, 501-522. doi: 10.1111/j.1748-1716.2010.02225.x
61. Ohtani, M., Ohura, K., and Oka, T. (2011). Involvement of P2X receptors in the regulation of insulin secretion, proliferation and survival in mouse pancreatic beta-cells. Cell. Physiol. Biochem. 28, 355-366. doi: 10.1159/000331752
62. Okada, S. F., Zhang, L., Kreda, S. M., Abdullah, L. H., Davis, C. W., Pickles, R. J., et al. (2011). Coupled nucleotide and mucin hypersecretion from goblet-cell metaplastic human airway epithelium. Am. J. Respir. Cell Mol. Biol. 45, 253-260. doi: 10.1165/rcmb.2010-0253OC
63. Patel, A. S., Reigada, D., Mitchell, C. H., Bates, S. R., Margulies, S. S., and Koval, M. (2005). Paracrine stimulation of surfactant secretion by extracellular ATP in response to mechanical deformation. Am. J. Physiol. Lung Cell. Mol. Physiol. 289, L489-L496. doi: 10.1152/ajplung.00074.2005
64. Praetorius, H. A., and Leipziger, J. (2009). ATP release from non-excitable cells. Purinergic Signal. 5, 433-446. doi: 10.1007/s11302-009-9146-2
65. Qu, Y., and Dubyak, G. R. (2009). P2X7 receptors regulate multiple types of membrane trafficking responses and non-classical secretion pathways. Purinergic Signal. 5, 163-173. doi: 10.1007/s11302-009-9132-8
66. Qu, Y., Franchi, L., Nunez, G., and Dubyak, G. R. (2007). Nonclassical IL-1 beta secretion stimulated by P2X7 receptors is dependent on inflammasome activation and correlated with exosome release in murine macrophages. J. Immunol. 179, 1913-1925.
67. 4 receptors by lysosomal targeting, glycan protection and exocytosis. J. Cell Sci. 120, 3838-3849. doi: 10.1242/jcs.010348
68. 2+-dependent ATP release from lung epithelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 300, L587-L595. doi: 10.1152/ajplung.00345.2010
69. Ransford, G. A., Fregien, N., Qiu, F., Dahl, G., Conner, G. E., and Salathe, M. (2009). Pannexin 1 contributes to ATP release in airway epithelia. Am. J. Respir. Cell Mol. Biol. 41, 525-534. doi: 10.1165/rcmb.2008-0367OC
70. Rice, W. R., and Singleton, F. M. (1987). P2Y-purinoceptor regulation of surfactant secretion from rat isolated alveolar type II cells is associated with mobilization of intracellular calcium. Br. J. Pharmacol. 91, 833-838. doi: 10.1111/j.1476-5381.1987.tb11282.x
71. Riteau, N., Gasse, P., Fauconnier, L., Gombault, A., Couegnat, M., Fick, L., et al. (2010). Extracellular ATP is a danger signal activating P2X7 receptor in lung inflammation and fibrosis. Am. J. Respir. Crit. Care Med. 182, 774-783. doi: 10.1164/rccm.201003-0359OC
72. Rodriguez Candela, J. L., and Garcia-Fernandez, M. C. (1963). Stimulation of secretion of insulin by adenosine-triphosphate. Nature 197, 1210. doi: 10.1038/1971210a0
73. Seminario-Vidal, L., Okada, S. F., Sesma, J. I., Kreda, S. M., Van Heusden, C. A., Zhu, Y., et al. (2011). Rho signaling regulates pannexin 1-mediated ATP release from airway epithelia. J. Biol. Chem. 286, 26277-26286. doi: 10.1074/jbc.M111.260562
74. 2+ entry through presynaptic P2X receptors elicits postsynaptic firing in the brainstem autonomic network. J. Neurosci. 24, 3125-3135. doi: 10.1523/JNEUROSCI.0090-04.2004
75. Singer, W., Frick, M., Haller, T., Bernet, S., Ritsch-Marte, M., and Dietl, P. (2003). Mechanical forces impeding exocytotic surfactant release revealed by optical tweezers. Biophys. J. 84, 1344-1351. doi: 10.1016/S0006-3495(03)74950-9
76. Smith, R. M., Baibakov, B., Ikebuchi, Y., White, B. H., Lambert, N. A., Kaczmarek, L. K., et al. (2000). Exocytotic insertion of calcium channels constrains compensatory endocytosis to sites of exocytosis. J. Cell Biol. 148, 755-767. doi: 10.1083/jcb.148.4.755
77. Solini, A., Chiozzi, P., Morelli, A., Fellin, R., and Di Virgilio, F. (1999). Human primary fibroblasts in vitro express a purinergic P2X7 receptor coupled to ion fluxes, microvesicle formation and IL-6 release. J. Cell Sci. 112(Pt 3), 297-305.
78. Sudhof, T. C. (2004). The synaptic vesicle cycle. Annu. Rev. Neurosci. 27, 509-547. doi: 10.1146/annurev.neuro.26.041002.131412
79. Surprenant, A. (1996). Functional properties of native and cloned P2X receptors. Ciba Found. Symp. 198, 208-219; discussion 219-222.
80. Surprenant, A., Rassendren, F., Kawashima, E., North, R. A., and Buell, G. (1996). The cytolytic P2Z receptor for extracellular ATP identified as a P2X receptor (P2X7). Science 272, 735-738. doi: 10.1126/science.272.5262.735
81. Tatur, S., Kreda, S., Lazarowski, E., and Grygorczyk, R. (2008). Calcium-dependent release of adenosine and uridine nucleotides from A549 cells. Purinergic Signal. 4, 139-146. doi: 10.1007/s11302-007-9059-x
82. 4) couples surfactant secretion and alveolar fluid transport. FASEB J. 27, 1772-1783. doi: 10.1096/fj.12-220533
83. Thorn, P. (2009). New insights into the control of secretion. Commun. Integr. Biol. 2, 315-317. doi: 10.4161/cib.2.4.8262
84. 4 receptor trafficking to the cell surface of microglia. Purinergic Signal. 8, 301-310. doi: 10.1007/s11302-011-9288-x
85. 4-receptor-mediated synthesis and release of brain-derived neurotrophic factor in microglia is dependent on calcium and p38-mitogen-activated protein kinase activation. J. Neurosci. 29, 3518-3528. doi: 10.1523/JNEUROSCI.5714-08.2009
86. 4 receptors in spinal microglia after peripheral nerve injury mediates BDNF release and neuropathic pain. J. Neurosci. 28, 11263-11268. doi: 10.1523/JNEUROSCI.2308-08.2008
87. Valera, S., Hussy, N., Evans, R. J., Adami, N., North, R. A., Surprenant, A., et al. (1994). A new class of ligand-gated ion channel defined by P2x receptor for extracellular ATP. Nature 371, 516-519. doi: 10.1038/371516a0
88. Vavra, V., Bhattacharya, A., and Zemkova, H. (2011). Facilitation of glutamate and GABA release by P2X receptor activation in supraoptic neurons from freshly isolated rat brain slices. Neuroscience 188, 1-12. doi: 10.1016/j.neuroscience.2011.04.067
89. Wang, C. Z., Namba, N., Gonoi, T., Inagaki, N., and Seino, S. (1996). Cloning and pharmacological characterization of a fourth P2X receptor subtype widely expressed in brain and peripheral tissues including various endocrine tissues. Biochem. Biophys. Res. Commun. 220, 196-202. doi: 10.1006/bbrc.1996.0380
90. 4 receptor complexes in mouse lung epithelial cells. Cell. Mol. Life Sci. 67, 2631-2642. doi: 10.1007/s00018-010-0355-1
91. Wirtz, H. R., and Dobbs, L. G. (2000). The effects of mechanical forces on lung functions. Respir. Physiol. 119, 1-17. doi: 10.1016/S0034-5687(99)00092-4
92. 2+ channel promotes endocytosis and couples exocytosis to endocytosis. Cell 138, 947-960. doi: 10.1016/j.cell.2009.06.033
93. Zsembery, A., Boyce, A. T., Liang, L., Peti-Peterdi, J., Bell, P. D., and Schwiebert, E. M. (2003). Sustained calcium entry through P2X nucleotide receptor channels in human airway epithelial cells. J. Biol. Chem. 278, 13398-13408. doi: 10.1074/jbc.M212277200