Signal processing at mammalian carotid body chemoreceptors

Seminars in Cell and Developmental Biology

Volumn 24, Issue 1, 2013, Pages 22-30

  Nurse, Colin A ^a   Piskuric, Nikol A ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

ATP; Autocrine paracrine transmitters; Neuromodulators; Pannexin 1; Type I cell; Type II cell

Indexed keywords

4 AMINOBUTYRIC ACID; ACETYLCHOLINE; ADENOSINE; ADENOSINE TRIPHOSPHATE; DOPAMINE; HISTAMINE; NEUROTRANSMITTER; NITRIC OXIDE; PURINERGIC P2Y RECEPTOR; SEROTONIN;

AUTOCRINE EFFECT; BLOOD VESSEL; CAROTID BODY CHEMORECEPTOR; CELL TYPE; GANGLION; GLOMUS (FUNGUS); GLOSSOPHARYNGEAL NERVE; HYPERCAPNIA; HYPOXIA; INFORMATION PROCESSING; MAMMAL; NEUROMODULATION; NONHUMAN; PARACRINE SIGNALING; PARASYMPATHETIC NERVE CELL; POSTSYNAPTIC INHIBITION; POSTSYNAPTIC POTENTIAL; REVIEW; SENSORY NERVE; SENSORY NERVE CELL; SIGNAL PROCESSING; SYNAPSE; SYNAPTIC TRANSMISSION;

GLOMUS; MAMMALIA;

EID: 84873418941     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2012.09.006     Document Type: Review

References (82)

1. Gonzalez C., Almaraz L., Obeso A., Rigual R. Carotid body chemoreceptors: from natural stimuli to sensory discharges. Physiological Reviews 1994, 74:829-898.
2. Teppema L.J., Dahan A. The ventilatory response to hypoxia in mammals: mechanisms, measurement, and analysis. Physiological Reviews 2010, 90:675-754.
3. Iturriaga R., Alcayaga J. Neurotransmission in the carotid body: transmitters and modulators between glomus cells and petrosal ganglion nerve terminals. Brain Research. Brain Research Reviews 2004, 47:46-53.
4. Nurse C.A. Neurotransmission and neuromodulation in the chemosensory carotid body. Autonomic Neuroscience 2005, 120:1-9.
5. Nurse C.A. Neurotransmitter and neuromodulatory mechanisms at peripheral arterial chemoreceptors. Experimental Physiology 2010, 95:657-667.
6. 2 sensors and multiple transmitters?. Experimental Physiology 2006, 91:17-23.
7. McDonald D.M. Peripheral chemoreceptors: structure-function relationships of the carotid body. Regulation of Breathing Lung Biol Health Dis 1981, 105-320. Marcel Dekker, New York. T.F. Hornbein (Ed.).
8. Leung P.S., Fung M.L., Tam M.S. Renin-angiotensin system in the carotid body. International Journal of Biochemistry and Cell Biology 2003, 35:847-854.
9. Rey S., Corthorn J., Chacon C., Iturriaga R. Expression and immunolocalization of endothelin peptides and its receptors, ETA and ETB, in the carotid body exposed to chronic intermittent hypoxia. Journal of Histochemistry and Cytochemistry 2007, 55:167-174.
10. Wilson R.J., Cumming K.J. Pituitary adenylate cyclase-activating polypeptide is vital for neonatal survival and the neuronal control of breathing. Respiratory Physiology and Neurobiology 2008, 164:168-178.
11. 2-sensing mechanisms in efferent neurons to the rat carotid body. Advances in Experimental Medicine and Biology 2003, 536:179-185.
12. Hohler B., Mayer B., Kummer W. Nitric oxide synthase in the rat carotid body and carotid sinus. Cell and Tissue Research 1994, 276:559-564.
13. Wang Z.Z., Bredt D.S., Fidone S.J., Stensaas L.J. Neurons synthesizing nitric oxide innervate the mammalian carotid body. Journal of Comparative Neurology 1993, 336:419-432.
14. Prabhakar N.R. NO and CO as second messengers in oxygen sensing in the carotid body. Respiration Physiology 1999, 115:161-168.
15. Abudara V., Garces G., Saez J.C. Cells of the carotid body express connexin43 which is up-regulated by cAMP. Brain Research 1999, 849:25-33.
16. Eyzaguirre C. Electric synapses in the carotid body-nerve complex. Respiratory Physiology and Neurobiology 2007, 157:116-122.
17. Jiang R.G., Eyzaguirre C. Dye and electric coupling between carotid nerve terminals and glomus cells. Advances in Experimental Medicine and Biology 2003, 536:247-253.
18. Pardal R., Ortega-Saenz P., Duran R., Lopez-Barneo J. Glia-like stem cells sustain physiologic neurogenesis in the adult mammalian carotid body. Cell 2007, 131:364-377.
19. McDonald D.M., Larue D.T. The ultrastructure and connections of blood vessels supplying the rat carotid body and carotid sinus. Journal of Neurocytology 1983, 12:117-153.
20. Heymans C., Bouckaert J.J., Dautrebande L. Sinus carotidienetréflexesrespiratoires. II Influences respiratoires reflexes de l" acidose, de l" alcalose, de l" anhydridecarbonique, de l" ionhydrogeneet de l" anoxémie: sinus carotidiens et échangesrespiratoiresdans les poumons et au dela des poumons. Archives of Internal Pharmacodynamics 1930, 39:400-408.
21. De Castro F. Sur la structure etl" innervation du sinus carotidien de l" homme et des mammifêres: nouveaux faitssurl" innervation et la fonction du glomuscaroticum. Trabajos del Laboratorio de Investigaciones biologicas de la Universidad de Madrid 1928, 25:330-380.
22. Kumar P., Bin-Jaliah I. Adequate stimuli of the carotid body: more than an oxygen sensor?. Respiratory Physiology and Neurobiology 2007, 157:12-21.
23. Lopez-Barneo J. Oxygen and glucose sensing by carotid body glomus cells. Current Opinion in Neurobiology 2003, 13:493-499.
24. 2 in cat carotid body. Journal of Applied Physiology 1998, 85:1719-1726.
25. Koyama Y., Coker R.H., Stone E.E., Lacy D.B., Jabbour K., Williams P.E., et al. Evidence that carotid bodies play an important role in glucoregulation in vivo. Diabetes 2000, 49:1434-1442.
26. Zhang M., Buttigieg J., Nurse C.A. Neurotransmitter mechanisms mediating low-glucose signalling in cocultures and fresh tissue slices of rat carotid body. Journal of Physiology 2007, 578:735-750.
27. Buckler K.J. TASK-like potassium channels and oxygen sensing in the carotid body. Respiratory Physiology and Neurobiology 2007, 157:55-64.
28. Lopez-Barneo J., Ortega-Saenz P., Pardal R., Pascual A., Piruat J.I., Duran R., et al. Oxygen sensing in the carotid body. Annals of the New York Academy of Sciences 2009, 1177:119-131.
29. Peers C., Wyatt C.N., Evans A.M. Mechanisms for acute oxygen sensing in the carotid body. Respiratory Physiology and Neurobiology 2010, 174:292-298.
30. Fitzgerald R.S. Oxygen and carotid body chemotransduction: the cholinergic hypothesis - a brief history and new evaluation. Respiration Physiology 2000, 120:89-104.
31. Nurse C.A., Zhang M. Acetylcholine contributes to hypoxic chemotransmission in co cultures of rat type 1 cells and petrosal neurons. Respiration Physiology 1999, 115:189-199.
32. Shirahata M., Balbir A., Otsubo T., Fitzgerald R.S. Role of acetylcholine in neurotransmission of the carotid body. Respiratory Physiology and Neurobiology 2007, 157:93-105.
33. Donnelly D.F. Chemoreceptor nerve excitation may not be proportional to catecholamine secretion. Journal of Applied Physiology 1996, 81:657-664.
34. Iturriaga R., Alcayaga J., Zapata P. Dissociation of hypoxia-induced chemosensory responses and catecholamine efflux in cat carotid body superfused in vitro. Journal of Physiology 1996, 497(Pt 2):551-564.
35. Zhang M., Zhong H., Vollmer C., Nurse C.A. Co-release of ATP and ACh mediates hypoxic signalling at rat carotid body chemoreceptors. Journal of Physiology 2000, 525(Pt 1):143-158.
36. Zhong H., Zhang M., Nurse C.A. Synapse formation and hypoxic signalling in co-cultures of rat petrosal neurones and carotid body type 1 cells. Journal of Physiology 1997, 503(Pt 3):599-612.
37. Prasad M., Fearon I.M., Zhang M., Laing M., Vollmer C., Nurse C.A. Expression of P2X2 and P2X3 receptor subunits in rat carotid body afferent neurones: role in chemosensory signalling. Journal of Physiology 2001, 537:667-677.
38. 2/pH chemosensory signaling in co-cultures of rat carotid body receptors and petrosal neurons: role of ATP and ACh. Journal of Neurophysiology 2004, 92:3433-3445.
39. Buttigieg J., Nurse C.A. Detection of hypoxia-evoked ATP release from chemoreceptor cells of the rat carotid body. Biochemical and Biophysical Research Communications 2004, 322:82-87.
40. Rong W., Gourine A.V., Cockayne D.A., Xiang Z., Ford A.P., Spyer K.M., et al. Pivotal role of nucleotide P2X2 receptor subunit of the ATP-gated ion channel mediating ventilatory responses to hypoxia. Journal of Neuroscience 2003, 23:11315-11321.
41. Niane L.M., Donnelly D.F., Joseph V., Bairam A. Ventilatory and carotid body chemoreceptor responses to purinergic P2X receptor antagonists in newborn rats. Journal of Applied Physiology 2011, 110:83-94.
42. Fitzgerald R.S., Shirahata M., Chang I., Kostuk E. The impact of hypoxia and low glucose on the release of acetylcholine and ATP from the incubated cat carotid body. Brain Research 2009, 1270:39-44.
43. He L., Dinger B., Fidone S. Effect of chronic hypoxia on cholinergic chemotransmission in rat carotid body. Journal of Applied Physiology 2005, 98:614-619.
44. Niane L., Joseph V., Bairam A. Role of cholinergic-nicotinic receptors on hypoxic chemoreflex during postnatal development in rats. Respiratory Physiology and Neurobiology 2009, 169:323-332.
45. Donnelly D.F. Nicotinic acetylcholine receptors do not mediate excitatory transmission in young rat carotid body. Journal of Applied Physiology 2009, 107:1806-1816.
46. Zhong H., Nurse C.A. Nicotinic acetylcholine sensitivity of rat petrosal sensory neurons in dissociated cell culture. Brain Research 1997, 766:153-161.
47. Gauda E.B., Cooper R., Johnson S.M., McLemore G.L., Marshall C. Autonomic microganglion cells: a source of acetylcholine in the rat carotid body. Journal of Applied Physiology 2004, 96:384-391.
48. Kim D.K., Prabhakar N.R., Kumar G.K. Acetylcholine release from the carotid body by hypoxia: evidence for the involvement of autoinhibitory receptors. Journal of Applied Physiology 2004, 96:376-383.
49. Conde S.V., Monteiro E.C. Activation of nicotinic ACh receptors with alpha4 subunits induces adenosine release at the rat carotid body. British Journal of Pharmacology 2006, 147:783-789.
50. Fearon I.M., Zhang M., Vollmer C., Nurse C.A. GABA mediates autoreceptor feedback inhibition in the rat carotid body via presynaptic GABAB receptors and TASK-1. Journal of Physiology 2003, 553:83-94.
51. Oomori Y., Nakaya K., Tanaka H., Iuchi H., Ishikawa K., Satoh Y., et al. Immunohistochemical and histochemical evidence for the presence of noradrenaline, serotonin and gamma aminobutyric acid in chief cells of the mouse carotid body. Cell and Tissue Research 1994, 278:249-254.
52. Kim C., Shvarev Y., Takeda S., Sakamoto A., Lindahl S.G., Eriksson L.I. Midazolam depresses carotid body chemoreceptor activity. Acta Anaesthesiologica Scandinavica 2006, 50:144-149.
53. Shirahata M. Neurotransmission in the carotid body and anesthesia. Journal of Anesthesiology 2002, 16:298-309.
54. Zhang M., Clarke K., Zhong H., Vollmer C., Nurse C.A. Postsynaptic action of GABA in modulating sensory transmission in co-cultures of rat carotid body via GABA(A) receptors. Journal of Physiology 2009, 587:329-344.
55. Conde S.V., Monteiro E.C., Obeso A., Gonzalez C. Adenosine in peripheral chemoreception: new insights into a historically overlooked molecule-invited article. Advances in Experimental Medicine and Biology 2009, 648:145-159.
56. Conde S.V., Obeso A., Monteiro E.C., Gonzalez C. The A(2B)-D(2) receptor interaction that controls carotid body catecholamines release locates between the last two steps of hypoxic transduction cascade. Advances in Experimental Medicine and Biology 2009, 648:161-168.
57. Gauda E.B. Gene expression in peripheral arterial chemoreceptors. Microscopy Research and Technique 2002, 59:153-167.
58. Kobayashi S., Conforti L., Millhorn D.E. Gene expression and function of adenosine A(2A) receptor in the rat carotid body. American Journal of Physiology Lung Cellular and Molecular Physiology 2000, 279:L273-L282.
59. Conde S.V., Gonzalez C., Batuca J.R., Monteiro E.C., Obeso A. An antagonistic interaction between A2B adenosine and D2 dopamine receptors modulates the function of rat carotid body chemoreceptor cells. Journal of Neurochemistry 2008, 107:1369-1381.
60. 2+] in type I cells of rat carotid bodies. American Journal of Cell Physiology 2006, 290:C1592-C1598.
61. + channel inhibition via protein kinase C. Journal of Physiology 2003, 551:825-842.
62. Jacono F.J., Peng Y.J., Kumar G.K., Prabhakar N.R. Modulation of the hypoxic sensory response of the carotid body by 5-hydroxytryptamine: role of the 5-HT2 receptor. Respiratory Physiology and Neurobiology 2005, 145:135-142.
63. Peng Y.J., Nanduri J., Yuan G., Wang N., Deneris E., Pendyala S., et al. NADPH oxidase is required for the sensory plasticity of the carotid body by chronic intermittent hypoxia. Journal of Neuroscience 2009, 29:4903-4910.
64. Jackson A., Nurse C.A. Role of acetylcholine receptors and dopamine transporter in regulation of extracellular dopamine in rat carotid body cultures grown in chronic hypoxia or nicotine. Journal of Neurochemistry 1998, 70:653-662.
65. 2+ currents by dopamine in glomus cells of the carotid body. European Journal of Neuroscience 1990, 2:809-812.
66. Koerner P., Hesslinger C., Schaefermeyer A., Prinz C., Gratzl M. Evidence for histamine as a transmitter in rat carotid body sensor cells. Journal of Neurochemistry 2004, 91:493-500.
67. Del Rio R., Moya E.A., Koenig C.S., Fujiwara K., Alcayaga J., Iturriaga R. Modulatory effects of histamine on cat carotid body chemoreception. Respiratory Physiology and Neurobiology 2008, 164:401-410.
68. Lazarov N., Rozloznik M., Reindl S., Rey-Ares V., Dutschmann M., Gratzl M. Expression of histamine receptors and effect of histamine in the rat carotid body chemoafferent pathway. European Journal of Neuroscience 2006, 24:3431-3444.
69. Campanucci V.A., Nurse C.A. Autonomic innervation of the carotid body: role in efferent inhibition. Respiratory Physiology and Neurobiology 2007, 157:83-92.
70. Fung M.L., Ye J.S., Fung P.C. Acute hypoxia elevates nitric oxide generation in rat carotid body in vitro. Pflugers Archiv 2001, 442:903-909.
71. Alcayaga J., Barrios M., Bustos F., Miranda G., Molina M.J., Iturriaga R. Modulatory effect of nitric oxide on acetylcholine-induced activation of cat petrosal ganglion neurons in vitro. Brain Research 1999, 825:194-198.
72. Kline D.D., Yang T., Huang P.L., Prabhakar N.R. Altered respiratory responses to hypoxia in mutant mice deficient in neuronal nitric oxide synthase. Journal of Physiology 1998, 511(Pt 1):273-287.
73. 2-chemoreceptors: role in nitric oxide-mediated efferent inhibition. Journal of Neuroscience 2006, 26:9482-9493.
74. 2+ current in glomus cells of the rabbit carotid body via a cGMP-independent mechanism. Journal of Neurophysiology 1999, 81:1449-1457.
75. 2+ release in type II cells of the rat carotid body. Journal of Physiology 2003, 549:739-747.
76. Xu J., Xu F., Tse F.W., Tse A. ATP inhibits the hypoxia response in type I cells of rat carotid bodies. Journal of Neurochemistry 2005, 92:1419-1430.
77. 2+]c increase without corresponding increases in CSN activity. Respiratory Physiology and Neurobiology 2003, 138:1-18.
78. Dubyak G.R. Both sides now: multiple interactions of ATP with pannexin-1 hemichannels. Focus on " A permeant regulating its permeation pore: inhibition of pannexin 1 channels by ATP" . American Journal of Cell Physiology 2009, 296:C235-C241.
79. Iglesias R., Dahl G., Qiu F., Spray D.C., Scemes E. Pannexin 1: the molecular substrate of astrocyte " hemichannels" . Journal of Neuroscience 2009, 29:7092-7097.
80. MacVicar B.A., Thompson R.J. Non-junction functions of pannexin-1 channels. Trends in Neurosciences 2010, 33:93-102.
81. Zhang M., Piskuric N.A., Vollmer C., Nurse C.A. P2Y2 receptor activation opens pannexin-1 channels in rat carotid body type II cells: Potential role in amplifying the neurotransmitter ATP. Journal of Physiology 2012, 590:4335-4350.
82. Huang Y.J., Maruyama Y., Dvoryanchikov G., Pereira E., Chaudhari N., Roper S.D. The role of pannexin 1 hemichannels in ATP release and cell-cell communication in mouse taste buds. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:6436-6441.