Mechanisms of constitutive and ATP-evoked ATP release in neonatal mouse olfactory epithelium

BMC Neuroscience

Volumn 13, Issue 1, 2012, Pages

  Hayoz, Sébastien ^a   Jia, Cuihong ^a   Hegg, CC ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ADENOSINE TRIPHOSPHATE; CALCIUM; CARBENOXOLONE; CLOSTRIDIUM DIFFICILE TOXIN A; CYCLIC AMP; PROBENECID; PURINERGIC P2X1 RECEPTOR; PURINERGIC P2X7 RECEPTOR; PURINERGIC P2Y RECEPTOR; PURINERGIC P2Y RECEPTOR AGONIST; PYRIDOXAL PHOSPHATE 6 AZOPHENYL 2',4' DISULFONIC ACID;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOSENSOR; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL REGENERATION; CONTROLLED STUDY; EVOKED RESPONSE; EXOCYTOSIS; HOMEOSTASIS; HUMAN; HUMAN CELL; IMAGING; IN VIVO STUDY; MOUSE; NERVE CELL; NERVE REGENERATION; NERVOUS SYSTEM INJURY; NONHUMAN; OLFACTORY EPITHELIUM; REGULATORY MECHANISM; SENSITIVITY ANALYSIS; STEM CELL;

ADENOSINE TRIPHOSPHATE; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; BACTERIAL TOXINS; BROMODEOXYURIDINE; CALCIUM; CARBENOXOLONE; CELLS, CULTURED; CYTIDINE TRIPHOSPHATE; DRUG INTERACTIONS; ENTEROTOXINS; ENZYME INHIBITORS; ETHYLMALEIMIDE; EXOCYTOSIS; GADOLINIUM; HUMANS; MICE; MICROSCOPY, CONFOCAL; MOLECULAR SEQUENCE DATA; OLFACTORY MUCOSA; ORGAN CULTURE TECHNIQUES; PHOSPHOPYRUVATE HYDRATASE; PURINERGIC AGENTS; PYRIDOXAL PHOSPHATE; QB-SNARE PROTEINS; QC-SNARE PROTEINS; QUINACRINE; RECEPTORS, PURINERGIC P2X2; SENSORY RECEPTOR CELLS; TIME FACTORS; TRANSFECTION; URIDINE TRIPHOSPHATE;

EID: 84861432823     PISSN: None     EISSN: 14712202     Source Type: Journal    
DOI: 10.1186/1471-2202-13-53     Document Type: Article

References (44)

1. Burnstock G. Physiology and pathophysiology of purinergic neurotransmission. Physiol Rev 2007, 87(2):659-797. 10.1152/physrev.00043.2006, 17429044.
2. Huang Y, Maruyama Y, Dvoryanchikov G, Pereira E, Chaudhari N, Roper S. The role of pannexin 1 hemichannels in ATP release and cell-cell communication in mouse taste buds. Proc Natl Acad Sci USA 2007, 104(15):6436-6441. 10.1073/pnas.0611280104, 1851090, 17389364.
3. Romanov RA, Rogachevskaja OA, Bystrova MF, Jiang P, Margolskee RF, Kolesnikov SS. Afferent neurotransmission mediated by hemichannels in mammalian taste cells. EMBO J 2007, 26(3):657-667. 10.1038/sj.emboj.7601526, 1794384, 17235286.
4. Sabirov RZ, Dutta AK, Okada Y. Volume-dependent ATP-conductive large-conductance anion channel as a pathway for swelling-induced ATP release. J Gen Physiol 2001, 118(3):251-266. 10.1085/jgp.118.3.251, 2229507, 11524456.
5. Tritsch NX, Yi E, Gale JE, Glowatzki E, Bergles DE. The origin of spontaneous activity in the developing auditory system. Nature 2007, 450(7166):50-55. 10.1038/nature06233, 17972875.
6. Anselmi F, Hernandez VH, Crispino G, Seydel A, Ortolano S, Roper SD, Kessaris N, Richardson W, Rickheit G, Filippov MA, et al. ATP release through connexin hemichannels and gap junction transfer of second messengers propagate Ca2+ signals across the inner ear. Proc Natl Acad Sci USA 2008, 105(48):18770-18775. 10.1073/pnas.0800793105, 2596208, 19047635.
7. Lahne M, Gale JE. Damage-induced cell-cell communication in different cochlear cell types via two distinct ATP-dependent Ca waves. Purinergic Signal 2010, 6(2):189-200. 10.1007/s11302-010-9193-8, 2912991, 20806011.
8. Kurth-Nelson ZL, Mishra A, Newman EA. Spontaneous glial calcium waves in the retina develop over early adulthood. J Neurosci 2009, 29(36):11339-11346. 10.1523/JNEUROSCI.2493-09.2009, 3148946, 19741140.
9. Jia C, Doherty JD, Crudgington S, Hegg CC. Activation of purinergic receptors induces proliferation and neuronal differentiation in Swiss Webster mouse olfactory epithelium. Neuroscience 2009, 163(1):120-128. 10.1016/j.neuroscience.2009.06.040, 2728178, 19555741.
10. Jia C, Roman C, Hegg CC. Nickel sulfate induces location-dependent atrophy of mouse olfactory epithelium: protective and proliferative role of purinergic receptor activation. Toxicol Sci 2010, 115(2):547-556. 10.1093/toxsci/kfq071, 2871758, 20200219.
11. Jia C, Sangsiri S, Belock B, Iqbal T, Pestka JJ, Hegg CC. ATP mediates neuroprotective and neuroproliferative effects in mouse olfactory epithelium following exposure to satratoxin G in vitro and in vivo. Toxicol Sci 2011, 124(1):169-178. 10.1093/toxsci/kfr213, 21865290.
12. Jia C, Cussen AR, Hegg CC. ATP differentially upregulates fibroblast growth factor 2 and transforming growth factor alpha in neonatal and adult mice: effect on neuroproliferation. Neuroscience 2011, 177:335-346. 3049987, 21187124.
13. Jia C, Hegg CC. NPY mediates ATP-induced neuroproliferation in adult mouse olfactory epithelium. Neurobiol Dis 2010, 38(3):405-413. 10.1016/j.nbd.2010.02.013, 2862820, 20211262.
14. Kanekar S, Jia C, Hegg CC. Purinergic receptor activation evokes neurotrophic factor neuropeptide Y release from neonatal mouse olfactory epithelial slices. J Neurosci Res 2009, 87(6):1424-1434. 10.1002/jnr.21954, 3097387, 19115410.
15. Abraham EH, Prat AG, Gerweck L, Seneveratne T, Arceci RJ, Kramer R, Guidotti G, Cantiello HF. The multidrug resistance (mdr1) gene product functions as an ATP channel. Proc Natl Acad Sci USA 1993, 90(1):312-316. 10.1073/pnas.90.1.312, 45650, 7678345.
16. Schwiebert EM. ABC transporter-facilitated ATP conductive transport. Am J Physiol 1999, 276(1 Pt 1):C1-C8.
17. Manzini I, Schild D. Multidrug resistance transporters in the olfactory receptor neurons of Xenopus laevis tadpoles. JPhysiol 2003, 546(Pt 2):375-385.
18. Delay RJ, Dionne VE. Coupling between sensory neurons in the olfactory epithelium. Chem Senses 2003, 28(9):807-815. 10.1093/chemse/bjg074, 14654449.
19. Miragall F, Hwang TK, Traub O, Hertzberg EL, Dermietzel R. Expression of connexins in the developing olfactory system of the mouse. J Comp Neurol 1992, 325(3):359-378. 10.1002/cne.903250304, 1332989.
20. Zhang C, Finger TE, Restrepo D. Mature olfactory receptor neurons express connexin 43. J Comp Neurol 2000, 426(1):1-12. 10.1002/1096-9861(20001009)426:1<1::AID-CNE1>3.0.CO;2-Y, 10980480.
21. Zhang C, Restrepo D. Expression of connexin 45 in the olfactory system. Brain Res 2002, 929(1):37-47. 10.1016/S0006-8993(01)03372-8, 11852029.
22. Zhang C, Restrepo D. Heterogeneous expression of connexin 36 in the olfactory epithelium and glomerular layer of the olfactory bulb. J Comp Neurol 2003, 459(4):426-439. 10.1002/cne.10617, 12687708.
23. Bruzzone R, Hormuzdi SG, Barbe MT, Herb A, Monyer H. Pannexins, a family of gap junction proteins expressed in brain. Proc Natl Acad Sci USA 2003, 100(23):13644-13649. 10.1073/pnas.2233464100, 263867, 14597722.
24. Gayle S, Burnstock G. Immunolocalisation of P2X and P2Y nucleotide receptors in the rat nasal mucosa. Cell Tissue Res 2005, 319(1):27-36. 10.1007/s00441-004-0979-2, 15558320.
25. Hassenklover T, Kurtanska S, Bartoszek I, Junek S, Schild D, Manzini I. Nucleotide-induced Ca(2+) signaling in sustentacular supporting cells of the olfactory epithelium. Glia 2008, 56(15):1614-1624. 10.1002/glia.20714, 18551628.
26. Hegg CC, Greenwood D, Huang W, Han P, Lucero MT. Activation of purinergic receptor subtypes modulates odor sensitivity. J Neurosci 2003, 23(23):8291-8301. 2976511, 12967991.
27. Sorensen CE, Novak I. Visualization of ATP release in pancreatic acini in response to cholinergic stimulus. Use of fluorescent probes and confocal microscopy. J Biol Chem 2001, 276(35):32925-32932. 10.1074/jbc.M103313200, 11387334.
28. Sudhof TC. The synaptic vesicle cycle. Annu Rev Neurosci 2004, 27:509-547. 10.1146/annurev.neuro.26.041002.131412, 15217342.
29. Ralevic V, Burnstock G. Receptors for purines and pyrimidines. Pharmacol Rev 1998, 50(3):413-492.
30. Pelegrin P, Surprenant A. Pannexin-1 mediates large pore formation and interleukin-1beta release by the ATP-gated P2X7 receptor. EMBO J 2006, 25(21):5071-5082. 10.1038/sj.emboj.7601378, 1630421, 17036048.
31. Ma W, Hui H, Pelegrin P, Surprenant A. Pharmacological characterization of pannexin-1 currents expressed in mammalian cells. J Pharmacol Exp Ther 2009, 328(2):409-418. 10.1124/jpet.108.146365, 2682283, 19023039.
32. Suadicani SO, Brosnan CF, Scemes E. P2X7 receptors mediate ATP release and amplification of astrocytic intercellular Ca2+ signaling. J Neurosci 2006, 26(5):1378-1385. 10.1523/JNEUROSCI.3902-05.2006, 2586295, 16452661.
33. Silverman W, Locovei S, Dahl G. Probenecid, a gout remedy, inhibits pannexin 1 channels. Am J Physiol Cell Physiol 2008, 295(3):C761-C767. 10.1152/ajpcell.00227.2008, 2544448, 18596212.
34. Waseem TV, Lapatsina LP, Fedorovich SV. Influence of integrin-blocking peptide on gadolinium- and hypertonic shrinking-induced neurotransmitter release in rat brain synaptosomes. Neurochem Res 2008, 33(7):1316-1324. 10.1007/s11064-007-9585-5, 18270818.
35. Spray DC, Ye ZC, Ransom BR. Functional connexin "hemichannels": a critical appraisal. Glia 2006, 54(7):758-773. 10.1002/glia.20429, 17006904.
36. De Lorenzo S. Presynaptic inhibition of spontaneous acetylcholine release mediated by P2Y receptors at the mouse neuromuscular junction. Neuroscience 2006, 142(1):71-85. 10.1016/j.neuroscience.2006.05.062, 16843602.
37. Hegg CC, Lucero MT. Purinergic receptor antagonists inhibit odorant-induced heat shock protein 25 induction in mouse olfactory epithelium. Glia 2006, 53(2):182-190. 10.1002/glia.20258, 2966283, 16206165.
38. Hassenklöver T, Schwartz P, Schild D, Manzini I. Purinergic signaling regulates cell proliferation of olfactory epithelium progenitors. Stem Cells 2009, 27(8):2022-2031. 10.1002/stem.126, 19544419.
39. Simpson SA, Alexander DJ, Reed CJ. Induction of heat shock protein 70 in rat olfactory epithelium by toxic chemicals: in vitro and in vivo studies. ArchToxicol 2005, 79(4):224-230.
40. Veggetti M, Muchnik S, Losavio A. Effect of purines on calcium-independent acetylcholine release at the mouse neuromuscular junction. Neuroscience 2008, 154(4):1324-1336. 10.1016/j.neuroscience.2008.04.056, 18534762.
41. Braun N, Zimmermann H. Association of ecto-5'-nucleotidase with specific cell types in the adult and developing rat olfactory organ. J Comp Neurol 1998, 393(4):528-537. 10.1002/(SICI)1096-9861(19980420)393:4<528::AID-CNE10>3.0.CO;2-L, 9550156.
42. Di VF, Steinberg TH, Silverstein SC. Inhibition of Fura-2 sequestration and secretion with organic anion transport blockers. Cell Calcium 1990, 11(2-3):57-62.
43. Decker DA, Galligan JJ. Cross-inhibition between nicotinic acetylcholine receptors and P2X receptors in myenteric neurons and HEK-293 cells. Am J Physiol Gastrointest Liver Physiol 2009, 296(6):G1267-G1276. 10.1152/ajpgi.00048.2009, 2697951, 19342512.
44. Hegg CC, Irwin M, Lucero MT. Calcium store-mediated signaling in sustentacular cells of the mouse olfactory epithelium. Glia 2009, 57(6):634-644. 10.1002/glia.20792, 2657191, 18942758.