CO2 -Induced ATP-Dependent release of acetylcholine on the ventral surface of the medulla oblongata

PLoS ONE

Volumn 11, Issue 12, 2016, Pages

  Huckstepp, Robert T R ^a,b   Llaudet, Enrique ^b   Gourine, Alexander V ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINE; ADENOSINE TRIPHOSPHATE; CARBON DIOXIDE;

ACETYLCHOLINE RELEASE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BREATHING; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; HYPERCAPNIA; IN VITRO STUDY; IN VIVO STUDY; MALE; MEDULLA OBLONGATA; NONHUMAN; RAT; SIGNAL TRANSDUCTION; ANIMAL; GENETIC PROCEDURES; METABOLISM; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ACETYLCHOLINE; ADENOSINE TRIPHOSPHATE; ANIMALS; BIOSENSING TECHNIQUES; CARBON DIOXIDE; IN VITRO TECHNIQUES; MALE; MEDULLA OBLONGATA; RATS; RATS, SPRAGUE-DAWLEY;

EID: 85003952204     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0167861     Document Type: Article

References (42)

1. Daly M. Peripheral arterial chemoreception and respiratory-cardiovascular integration. Monograph for the Physiological Society. Oxford: Oxford University Press.1997.
2. Gonzalez C, Almaraz L, Obeso A, Rigual R. Carotid body chemoreceptors: from natural stimuli to sensory discharges. Physiol Rev. 1994; 74(4):829-98 PMID: 7938227
3. Spyer KM, Gourine AV. Chemosensory pathways in the brainstem controlling cardiorespiratory activity. Phil Trans R Soc B. 2009; 364(1529):2603-10 doi: 10.1098/rstb.2009.0082 PMID: 19651660
4. Nattie E. Julius H. Comroe, Jr., distinguished lecture: central chemoreception: then . . . and now. J Appl Physiol. 2011; 110(1):1-8 doi: 10.1152/japplphysiol.01061.2010 PMID: 21071595
5. 2 during hyperoxia. Resp Physiol. 1979; 37(3):365-79
6. Ballantyne D, Scheid P. Mammalian brainstem chemosensitive neurones: linking them to respiration in vitro. J Physiol. 2000; 525(3):567-77
7. Loeschcke HH. Central chemosensitivity and the reaction theory. J Physiol. 1982; 332:1-24 PMID: 6818338
8. 2 sensitivity in rats. Respir Physiol. 1994; 97(1):63-77 PMID: 8091025
9. Gourine AV, Llaudet E, Dale N, Spyer KM. ATP is a mediator of chemosensory transduction in the central nervous system. Nature. 2005; 436:108-11 doi: 10.1038/nature03690 PMID: 16001070
10. 2 chemosensitivity-towards a better understanding of mechanism. J Physiol. 2011; 589(23):5561-79
11. 2 chemosensitivity, fatal central apnea, and specific loss of parafacial neurons. PNAS. 2008; 105(3):1067-72 doi: 10.1073/pnas.0709115105 PMID: 18198276
12. 2 chemosensitivity in conditional Phox2b mutants. J Neurosci. 2011; 31(36):12880-8 doi: 10. 1523/JNEUROSCI.1721-11.2011 PMID: 21900566
13. Marina N, Abdala AP, Trapp S, Li A, Nattie EE, Hewinson J, et al. Essential role of Phox2b-expressing ventrolateral brainstem neurons in the chemosensory control of inspiration and expiration. J Neurosci. 2010; 30(37):12466-73 doi: 10.1523/JNEUROSCI.3141-10.2010 PMID: 20844141
14. Dev NB, Loeschcke HH. Topography of the respiratory and circulatory responses to acetylcholine and nicotine on the ventral surface of the medulla oblongata. Pflugers Arch. 1979; 379:19-27 PMID: 571101
15. Fukuda Y, Loeschcke H. A cholinergic mechanism involved in the neuronal excitation by H+ in the respiratory chemosensitive structures of the ventral medulla oblongata of rats in vitro. Pflugers Arch. 1979; 379(2):125-35 PMID: 34826
16. Sobrinho CR, Kuo F-S, Barna BF, Moreira TS, Mulkey DK. Cholinergic control of ventral surface chemoreceptors involves Gq/inositol 1,4,5-trisphosphate-mediated inhibition of KCNQ channels. J Physiol. 2016; 594(2):407-19 doi: 10.1113/JP271761 PMID: 26572090
17. 2 -dependent release of ATP in the medulla oblongata contributes to central respiratory chemosensitivity. J Physiol. 2010; 588(20):3901-20
18. Gourine AV, Kasymov V, Marina N, Tang F, Figueiredo MF, Lane S, et al. Astrocytes control breathing through pH-dependent elease of ATP. Science. 2010; 329(5991):571-5 doi: 10.1126/science.1190721 PMID: 20647426
19. 2 chemoreception. J Physiol. 2000; 523(2):441-7
20. 2 receptor subunit. J Physiol. 2003; 552(1):197-211
21. Huckstepp RTR, Cardoza KP, Henderson LE, Feldman JL. Role of parafacial nuclei in control of breathing in adult rats. J Neurosci. 2015; 35:1052-67 doi: 10.1523/JNEUROSCI.2953-14.2015 PMID: 25609622
22. Zhang M, Zhong H, Vollmer C, Nurse CA. Co-release of ATP and ACh mediates hypoxic signalling at rat carotid body chemoreceptors. J Physiol. 2000; 525(1):143-58
23. Gourine AV, Wood JD, Burnstock G. Purinergic signalling in autonomic control. Trends Neurosci. 2009; 32(5):241-8 doi: 10.1016/j.tins.2009.03.002 PMID: 19359051
24. Gourine AV. On the peripheral and central chemoreception and control of breathing: an emerging role of ATP. J Physiol. 2005; 568(3):715-24
25. Llaudet E, Hatz S, Droniou M, Dale N. Microelectrode biosensor for real-time measurement of ATP in biological tissue. Anal Chem. 2005; 77(10):3267-73 doi: 10.1021/ac048106q PMID: 15889918
26. Llaudet E, Botting NP, Crayston JA, Dale N. A three-enzyme microelectrode sensor for detecting purine release from central nervous system. Biosens Bioelectron. 2003; 18(1):43-52 PMID: 12445443
27. Gourine AV, Llaudet E, Dale N, Spyer KM. Release of ATP in the ventral medulla during hypoxia in rats: role in hypoxic ventilatory response. J Neurosci. 2005; 25(5):1211-8 doi: 10.1523/JNEUROSCI.3763-04.2005 PMID: 15689558
28. + -sensitive neurons by purinergic signalling. J Physiol. 2012; 590(9):2137-50 doi: 10.1113/jphysiol.2012. 229666 PMID: 22411009
29. 2 -dependent opening of connexin 26 and related β connexins. J Physiol. 2010; 588(Pt 20):3921-31 doi: 10.1113/jphysiol.2010.192096 PMID: 20736419
30. 2 directly modulates connexin 26 by formation of carbamate bridges between subunits. eLife. 2013; 2:e01213 doi: 10.7554/eLife. 01213 PMID: 24220509
31. Stornetta RL, Macon CJ, Nguyen TM, Coates MB, Guyenet PG. Cholinergic neurons in the mouse rostral ventrolateral medulla target sensory afferent areas. Brain Struct Func. 2013; 218(2):455-75
32. Kasymov V, Larina O, Castaldo C, Marina N, Patrushev M, Kasparov S, et al. Differential sensitivity of brainstem versus cortical astrocytes to changes in pH reveals functional regional specialization of astroglia. J Neurosci. 2013; 33(2):435-41 doi: 10.1523/JNEUROSCI.2813-12.2013 PMID: 23303924
33. Woolf NJ. Cholinergic systems in mammalian brain and spinal cord. Prog Neurobiol. 1991; 37(6):475-524 PMID: 1763188
34. Woolf NJ, Butcher LL. Cholinergic systems in the rat brain: IV. descending projections of the pontomesencephalic tegmentum. Brain Res Bull. 1989; 23(6):519-40 PMID: 2611694
35. 2 requires the proton-activated receptor GPR4 in retrotrapezoid nucleus neurons. Science. 2015; 348(6240):1255-60 doi: 10.1126/science.aaa0922 PMID: 26068853
36. Guyenet PG, Bayliss DA, Stornetta RL, Ludwig M-G, Kumar NN, Shi Y, et al. Proton detection and breathing regulation by the retrotrapezoid nucleus. J Physiol. 2016; 594(6):1529-51 doi: 10.1113/ JP271480 PMID: 26748771
37. 2 sensitivity of astrocytes in a mouse model of Rett syndrome. J Physiol. 2015; 593(14):3159-68 doi: 10.1113/JP270369 PMID: 25981852
38. Garg SK, Lioy DT, Knopp SJ, Bissonnette JM. Conditional depletion of methyl-CpG-binding protein 2 (MeCP2) in astrocytes depresses the hypercapnic ventilatory response (HCVR) in mice. J Appl Physiol. 2015; 119(6):670-6 doi: 10.1152/japplphysiol.00411.2015 PMID: 26205541
39. Hawkins V, Kuo F, Bellemare L, Perez D, Dubreuil T, Mulkey D. Conditional knockdown of Kir4.1 in astrocytes blunts the hypercapnic respiratory response in awake mice (872.7). FASEB J. 2014; 28(1 Supplement)
40. 2 sensitivity of astrocytes. J Neurosci. 2016; 36(42):10750 doi: 10.1523/JNEUROSCI.1281-16. 2016 PMID: 27798130
41. 2 chemoreception: a mechanism involving P2 purinoreceptors localized in the ventrolateral medulla of the anaesthetized rat. J Physiol. 1999; 517 (3):899-905
42. Wenker IC, Kréneisz O, Nishiyama A, Mulkey DK. Astrocytes in the retrotrapezoid nucleus sense H+ by Inhibition Of a Kir4.1-Kir5.1-like current and may contribute to chemoreception by a purinergic mechanism. J Neurophysiol. 2010; 104(6):3042-52 doi: 10.1152/jn.00544.2010 PMID: 20926613