Mechanisms of CO2 sensing in avian intrapulmonary chemoreceptors

Airway Chemoreceptors in Vertebrates

Volumn , Issue , 2019, Pages 213-234

  Hempleman, Steven C ^a   Pilarski, Jason Q ^a  

^a NORTHERN ARIZONA UNIVERSITY   (United States)

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EID: 79960699163     PISSN: None     EISSN: None     Source Type: Book    
DOI: None     Document Type: Chapter

References (88)

1. Abramovici, A., 1967. Levolution du pH du plasma et des liquides extra embryonnaires de lembryon de poulet au cours du development normal. C. R. Acad. Sci. (Paris) 265:336-339.
2. Adamson, T.P., and Burger, R.E. 1986. Sodium bicarbonate infusion increases discharge frequency of intrapulmonary chemoreceptors only at high CO2. Respir. Physiol. 66(1):83-93.
3. Adriaensen, D., Brouns, I., Pinteion, I., De Proost, I., and Timmermans, J.-P. 2006. Evidence for a role of neuroepithelial bodies as complex airway sensors: comparison with smooth muscle-associated airway receptors. J. Appi Physiol. 101:960-970.
4. Bayliss, D.A., Talley, E.M., Sirois, J.E., and Lei, Q. 2001. Task-1 is a highly modulated pH-sensitive 'leak' K channel expressed in brainstem respiratory neurons. Respir. Physiol. 129:159-174.
5. Bebout, D.E., and Hempleman, S.C. 1999. Chronic hypercapnia resets CO2 sensitivity of avian intrapulmonary chemoreceptors. Am. J. Physiol. 276 (Reg. Int. Comp. Physiol. 45): R317-R322.
6. Berger, P.J., Tallman Jr., R.D., and Kunz, A.L.. 1980. Discharge of intrapulmonary chemoreceptors and its modulation by rapid FICO2 changes in decerebrate ducks. Respir. Physiol. 42:123-130.
7. Bina, R.W., and Hempleman, S.C. 2007. Evidence for TREK-like tandem-pore domain channels in intrapulmonary chemoreceptor chemotransduction. Evidence for TREK-like tandem pore domain leak channels in intrapulmonary CO2 chemoreception. Respir. Physiol. Neurobiol. 14;156(2):120-31.
8. Buckler, K.J., Williams, B.A., and Honore, E. 2000. An oxygen-, acid- and anesthetic sensitive TASK-like background potassium channel in rate arterial chemoreceptor cells. J. Physiol. (London). 525:135-142.
9. Burger, R.E. 1968. Pulmonary chemosensitivity in the domestic fowl. Fed. Proc. 27:328.
10. Burger, R.E., Osborne, J.L., and Banzett, R.B. 1974. Intrapulmonary chemoreceptors in Gallus domesticus: adequate stimulus and functional localization. Respir. Physiol. 22:87-97.
11. Chiang, M.J., Berger, P.J., and Kunz, A.L. 1978. A study of the effect of SO2 on pacing and intrapulmonary chemoreceptor discharge in the domestic fowl. Respir. Physiol. 33(2):229-239.
12. Coates, E.L., Knuth, S.L., and Bartlett Jr., D. 1996. Laryngeal CO2 receptors: influence of systemic PCO2 and carbonic anhydrase inhibition. Respir. Physiol. 104(1):53-61.
13. Cook, R., Vailland, C., and King, A. 1986. The abdominal air sac ostium of the domestic fowl: a sphincter regulated by neuroepithelial cells?;. Anat. 149:101-111.
14. Dawes, C., and Simkiss, K. 1969. The acid-base status of the blood of the developing chick embryo. J. Exp. Biol. 50:70-86.
15. Dean, J.B., Lawing, W.L., and Millhorn, D.E. 1989. CO2 decreases membrane conductance and depolarizes neurons in the nucleus tractus solitarii. Exp. Brain Res. 76(3):656-661.
16. Duncker, H.-R. 1971. The lung air sac system of birds. Adv. Anat. Embryol. Cell Biol. 45:7-171.
17. Duncker, H.-R. 2004. Vertebrate lungs: structure, topography and mechanics. A comparative perspective of the progressive integration of respiratory system, locomotor apparatus and ontogenetic development. Respir. Physiol. Neurobiol. 144(2-3):111-124.
18. Erasmus, Bde. W., Howell, B.J., and Rahn, H. 1970/71. Ontogeny of acid-base balance in the bullfrog and chicken. Respir. Physiol. 11:46-53.
19. Erlichman, J.S., and Leiter, J.C. 1997. Comparative aspects of central CO2 chemoreception. Respir. Physiol. 110:177-185.
20. Fedde, M.R., and Peterson, D.F. 1970. Intrapulmonary receptor response to changes in airway-gas composition in Gallus domesticus. J. Physiol. (London). 209(3):609-625.
21. Fedde, M.R., and Scheid, P. 1976. Intrapulmonary CO2 receptors in the duck: IV. Discharge pattern of the population during a respiratory cycle. Respir. Physiol. 26:223-227.
22. Fitzgerald, R.S., Shirihata, M., and Lahiri, S. 1990. Amiloride and carotid body chemoreception of hypercapnia and hypoxia. Respir. Physiol. 81(3):337-347.
23. Frappell, P.B., Hinds, D.S., and Boggs, D.F. 2001. Scaling of respiratory variables and the breathing pattern in birds: an allometric and phylogenetic approach. Physiol Biochem. Zool. 74(1):75-89.
24. Freeman, B.M., and Misson, B.H. 1970. pH, Po2, and Pco2 of blood from the foetus and neonate of Gallus domesticus. Comp. Biochem. Physiol. 33:763-772.
25. Furilla, R.A., and Bernstein, M.H. 1995. Intrapulmonary CO2 rise time and ventilation in ducks. J. Appl. Physiol. 79(5):1397-1404.
26. Gonzalez, C., Almaraz, L, Obeso, A., and Riguai, R. 1994. Carotid body chemoreceptors: from natural stimuli to sensory discharges. Physiol. Rev. 74:829-898.
27. Hempleman, S.C., and Burger, R.E. 1984. Receptive fields of intrapulmonary chemoreceptors in the pekin duck. Respir. Physiol. 57:317-330.
28. Hempleman, S.C., and Bebout, D.E. 1994. Increased venous PCO2 enhances dynamic responses of avian intrapulmonary chemoreceptors. Am. J. Physiol. (Reg. Int. Comp. Physiol.): 266: R15-R19.
29. Hempleman, S.C., and Posner, R.G. 2004. CO2 transduction mechanisms in avian intrapulmonary chemoreceptors: experiments and models. Respir. Physiol. Neurohiol. 144(2-3):203-214.
30. Hempleman, S.C., Powell, F.L., and Prisk, G.K. 1992. Avian arterial chemoreceptor responses to steps of CO2 and O2. Respir: Physiol. 90: 325-340.
31. Hempleman, S.C., Rodriguez, T.A., Bhagat, Y., and Begay, R.S. 2000. Benzolamide, acetazolamide and signal transduction in avian intrapulmonary chemoreceptors. Am. J. Physiol. (Reg. Int. Comp. Physiol): 279:R1988-R1995.
32. Hempleman, S.C., Adamson, T.P., Begay, R.S., and Solomon, I.C. 2003. CO2 transduction in avian intrapulmonary chemoreceptors is critically dependent on transmembrane Na+/H+ exchange. Am. J. Physiol. (Reg. Int. Comp. Physiol.) 284(6):R1551-R1559.
33. Hempleman, S.C., Kilgore, Jr., D.L., Colby, C. Bavis, R.W, and Powell, F.L. 2005. Spike firing allometry in avian intrapulmonary chemoreceptors: matching neural code to body size. J. Exp. Biol. 208(Pt16):3065-73.
34. Hempleman, S.C., Egan, S.X., Pilarski, J.P., Adamson, T.P., and Solomon, I.C. 2006. Calcium and avian intrapulmonary chemoreceptor response to CO2. J. Appl. Physiol. 101(6):1565-1575.
35. Hille, A. 1992a. In: Ionic Channels of Excitable Membranes, 2nd ed. Sinauer Associates, Sunderland, MA. pp. 79-81.
36. Hille, A. 1992b. In: Ionic Channels of Excitable Membranes, 2nd ed. Sinauer Associates, Sunderland, MA. pp. 525-544.
37. Iturriaga, R., Mokashi, A., and Lahiri, S. 1991. Carbonic anhydrase and chemoreception in the cat carotid body. Am. J. Physiol. (Cell Physiol.) 261(30):C565-C573.
38. Iturriaga, R., Mokashi, A., and Lahiri, S. 1998. Anion exchanger and chloride channel in cat carotid body chemotransduction. J. Auton. Nerv. Syst. 70(1-2):23-31.
39. Jiang, C., Rojas, A., Wang, R., and Wang, X. 2005. CO2 central chemosensitivity: why are there so many sensing molecules? Respir. Physiol. Neurobiol. 145(2-3):115-126.
40. Kemp, P.J., Lewis, A., Hartness, M., E., Searle, G.J., Miller, P., O'Kelly, I., and Peers, C. 2002. Airway chemotransduction: from oxygen sensor to cellular effector. Am. J. Respir: Crit. Care Med. 166(12 Pt2):S17-S24.
41. Kennedy, M.B., Beale, H.C., Carlisle, H.J., and Washburn, L.R. 2005. Integration of biochemical signaling in spines. Nature Rev. Neurosci. 6(6):423-434.
42. Krause, W.L., Kazemi, H., and Burton, M.D. 1998. Potential role for imidazole in the rhythmic respiratory activity of the in vitro neonatal rat brainstem. Neurosci. Lett. 251(3):153-160.
43. Kubke, M.F., Ross, J.M., and Wild, J.M. 2004. Vagal innervation of the airsacs in a songbird, Taenopygia guttata. J. Anat. 204:283-292.
44. Kumaraswamy, M., Solomon, I.C., and Hempleman, S.C. 2004. Ammonia, pH, and signal transduction in avian intrapulmonary chemoreceptors. FASEBJ. 18(5): A1060-A1061.
45. Lopes, CM., Rohacs, T., Czirjak, G., Balia, X, Enyedi, P., and Logothetis, D.E. 2005. PIP2 hydrolysis underlies agonist-induced inhibition and regulates voltage gating of two-pore domain K+ channell.;. Physiol. 564(Pt 1):117-29.
46. Lu, D.C., Erlichman, J.S., and LeitnerJ.C. 1998. Diethyl pyrocarbonate (DEPC) inhibits CO2 chemosensitivity in Helix aspersa. Respir. Physiol. 111(1):65-78.
47. Maren, T.H. 1977. Use of inhibitors in physiological studies of carbonic anhydrase. Am. J. Physiol. 232(4):F291-F297.
48. McLelland, J., and Macfarlane, C. 1986. Solitary granular endocrine cells and neuroepithelial bodies in the lungs of Ringed Turtle Dove (Streptopelia risoria). J. Anat. 147:83-93.
49. Milsom, W.K. 2002. Phylogeny of CO2/H+ chemoreception in vertebrates. Respir. Physiol. Neurohiol. 131(1-2): 29-41.
50. Milsom, W.K., Abe, A.S., Andrade, D.V., and Tattersall, G.J. 2004. Evolutionary trends in airway CO2/H+ chemoreception. Respir. Physiol. Neurohiol. 144(2-3):191-202.
51. Name, E.E. 1986a. Diethyl pyrocarbonate (an imidazole binding substance) inhibits rostral VLM CO2 sensitivity. J. Appl. Physiol. 61:843-850.
52. Nattie, E.E. 1986b. Intracisternal diethylpyrocarbonate inhibits central chemoreception in conscious rabbits. Respir. Physiol. 64:161-176.
53. Nattie, E.E. 1988. Diethyl pyrocarbonate inhibits rostral ventrolateral medullary H+ sensitivity. J. Appl. Physiol. 64:1600-1609.
54. Neubauer, J.A. 1991. Carbonic anhydrase and sensory function in the central nervous system. In: The Carbonic Anhydrases. S. Dodgson, R. Tashian, G. Gros, and N. Carter (Eds.), Plenum Press, New York. pp. 49-70.
55. Ovadi, J., and Saks, V. 2004. On the origin of intracellular compartmentation and organized metabolic systems. Mol. Cell. Biochem. 256/257:5-12.
56. Patel, A.J., and Honore, E. 2001. Anesthetic-sensitive 2P domain K+ channels. Anesthes. 95(4):1013-1021.
57. Patel, A.J., Honore, E., Lesage, E, Fink, M., Romey, G., and Lazdunski, M. 1999. Inhalational anesthetics activate two-pore-domain background K+ channels. Nature Neurosci. 2(5):422-426.
58. Peers, C., and Green, F.K. 1991. Inhibition of Ca-activated K currents by intracellular acidosis in isolated type I cells of neonatal rat carotid body. J. Physiol. (London). 437:589-602.
59. Peterson, D.E, and Fedde, M.R. 1968. Receptors sensitive to carbon dioxide in lungs of chicken. Science. 162:1499-1501.
60. Petheo, G.L., Molnar, Z., Roka, A., Makara, J.K., and Spat, A. 2001. A pH-sensitive chloride current in the chemoreceptor cell of rat carotid bodyj. Physiol. 535(Pt 1):95-106.
61. Pilarski, J.Q., and Hempleman, S.C. 2006. Imidazole binding reagent diethyl pyrocarbonate (DEPC) inhibits avian intrapulmonary chemoreceptor discharge in vivo. Respir. Physiol. Neurohiol. 150(2-3):144-154.
62. Pilarski, J.Q., and Hempleman, S.C. 2007. Development of intrapulmonary chemoreceptors. Respir. Physiol. Neurohiol. 157(2-3):393-402.
63. Powell, F.L. 2000. Respiration. In: Sturkies Avian Physiology, 5th Ed, G.C. Whittow (Ed.), Academic Press, San Diego, CA, pp. 233-264.
64. Powell, F.L., Fedde, M.R., Gratz, G.K., and Scheid, P. 1978. Role of avian intrapulmonary chemoreceptors in the ventilatory response to inhaled CO2: effects of acetazolamide in the duck. In: Respiratory Function in Birds, Adult and Embryonic J. Piiper (Ed.), Berlin, Springer-Verlag, pp. 164-167.
65. Powell, F.L., Geiser, J., Gratz, R.K., and Scheid, P. 1981. Airflow in the avian respiratory tract: variations of O2 and CO2 concentrations in the bronchi of the duck. Respir. Physiol. 44:195-213.
66. Putnam, R.W., Filosa, J.A., and Ritucci, N.A. 2004. Cellular mechanisms involved in CO2 and acid signaling in chemosensitive neurons. Am. J. Physiol. Cell Physiol. 287(6):C1493-C1526.
67. Reeves, R.B. 1972. An imidazole alphastat hypothesis for vertebrate acid-base regulation: tissue carbon dioxide content and body temperature in bullfrogs. Respir. Physiol. 14:219-236.
68. Richerson, G.B. 1995. Response to CO2 of neurons in the rostral ventral medulla in vitro. J. Neurophysiol. 73(3):933-944.
69. Scheid, P., and Piiper, J. 1972. Cross-current gas exchange in avian lungs: effects of reversed parabronchial air flow in ducks. Respir. Physiol. 16(3):304-312.
70. Scheid, P., and Piiper, J. 1986. Control of breathing in birds. In: Handbook of Physiology, Sec. 3: The Respiratory System, Voi II, Part 2, A.P. Fishman, N.S. Cherniack, J.G. Widdicombe, and S.R. Geiger (Eds.), American Physiological Society, Bethesda, pp. 815-832.
71. Scheid, P., Kuhlmann, W.D., and Fedde, M.R. 1977. Intrapulmonary receptors in the tegu lizard: II. Functional characteristics and localization. Respir. Physiol. 29:49-62.
72. Scheid, P., Gratz, R.K., Powell, F.L., and Fedde, M.R. 1978. Ventilatory response to CO2 in birds. II. Contribution by intrapulmonary chemoreceptors. Respir. Physiol. 35:361-372.
73. Schmidt-Nielsen, K. 1984. In: Scaling: Why is Animal Size so Important? Cambridge University Press, New York.
74. Shoemaker, J.S., and Hempleman, S.C. 2001. Avian intrapulmonary chemoreceptor discharge rate is increased by anion exchange blocker"DIDS". Respir. Physiol. 128:195-204.
75. Sterling, D., Reithmeier, R.A.F., and Casey, J.R. 2001. A transport metabolon. Functional interation of carbonic anhydrase II and chloride/bicarbonate exchangers. J. Biol. Chem. 276(51):47886-47894.
76. Tallman, R.D., Jr., and Grodins, F.S. 1982. Intrapulmonary CO2 receptor discharge at different levels of venous PCO2 J. Appl. Physiol. 53(6):1386-1391.
77. Tallman, R.D., Jr., Ghazanshahi, S.D., and Khoo, M.C.K. 1996. Transduction dynamics of intrapulmonary CO2 chemoreceptors. Respir; Physiol. 106(2):115-125.
78. Tazawa, H. 1981. Compensation of diffusive respiratory disturbances of the acid-base balance in the chick embryo. Comp. Biochem. Physiol. A 69:333-336.
79. Tazawa, H. 1982. Regulatory process of metabolic and respiratory acid-base disturbances in embryos. J. Appl. Physiol. 53:1449-1454.
80. Tazawa, H. 1986. Acid-base equilibrium in birds and eggs. In: Acid-Base Regulation in Animals, N. Heisler rEd.), Elsevier, Amsterdam, pp. 220-2233.
81. Tazawa, H. 1987. Embryonic respiration. In: Bird Respiration Vol. II, T.J. Seller (Ed.), CRC Press, Boca Raton, FL, pp. 3-41.
82. Tazawa, H., Mikami, T., and Yoshimoto, C. 1971. Respiratory properties of chicken embryonic blood during development. Respir. Physiol. 13:160-170.
83. Vince, M. A., and Tolhurst, B.E. 1975. The establishment of lung ventilation in the avian embryo: the rate at which lungs become aerated. Comp. Biochem. Physiol. A 52(2):331-337.
84. Visschedijk, A.H.J. 1968a. The air space and embryonic respiration. 1. The pattern of gaseous exchange in the fertile egg during the closing stages of incubation. Brit. Poul. Sci. 9:173-184.
85. Visschedijk, A.H.J. 1968b. The air space and embryonic respiration. 3. The balance between oxygen and carbon dioxide in the air space of the incubating chicken egg and its role in stimulating pipping. Brit. Poul. Sci. 9:197-210.
86. Vivoni, M., Castro, M.I., Lojo, L., and Furilla, R.A. 2001. Airway ammonia negates the normal ventilatory response to airway CO2 in garter snakes. Respir. Physiol. 127(1):13-22.
87. Wellner-Kienitz, M.-C., and Shams, H. 1998a. Hyperpolarization-activated inward currents contribute to spontaneous electrical activity and CO2/H+ sensitivity of cultivated neurons of fetal rat medulla. Neuroscience. 87(1):109-121.
88. Wellner-Kienitz, M.-C., Shams, H., and Scheid, P. 1998b. Contribution of Ca++-activated K+ channels to central chemosensitivity in cultivated neurons of fetal rat medulla. J. Neurophysiol. 70:2885-2894.