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Neurotransmitters in the Carotid Body

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Arterial Chemoreceptors

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 360))

Abstract

One of the most fundamental physiological stimuli is oxygen, or more appropriately the lack of oxygen, i.e., hypoxia. The discovery that the carotid bodies are the principal sensory organs for monitoring the arterial oxygen opened new perspectives in respiratory physiology. The chemoreceptor organ morphologically resembles a miniaturized brain. It is comprised of type I (also called glomus) cells that are of neural crest origin and contain neurotransmitters. Glomus cells are in functional contact with afferent nerve endings; whereas the type II (or sustentacular) cells resemble glia. Currently, it is believed that the type I cells are the initial transducers of the hypoxic stimuli. Transduction mechanism(s) may involve biochemical or biophysical processes (Acker, 1989; Biscoe & Duchen, 1990; Fidone & Gonzalez, 1986). Neurochemical(s), on the other hand, are essential for sensory transmission in the carotid body (Fidone & Gonzalez, 1986; Prabhakar, 1992). The general consensus is that in response to low O2 glomus cells release neurochemical(s), which act on the nearby afferent nerve ending to increase the sensory discharge (Biscoe & Duchen, 1990; Fidone & Gonzalez, 1986; Prabhakar, 1992). Glomus cells are endowed with several types of chemicals that function as transmitters or modulators else where in the nervous system. These include biogenic amines, neuropeptides and nitric oxide (NO) and carbon monoxide (CO). Some of these neurochemicals co-exist within the same glomus cell (Wang et al., 1992b), and perhaps co-released during hypoxia. In view of this, the notion that hypoxia releases a “single” neurochemical, perhaps is no longer tenable.

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References

  • Acker, H. (1989) PO2 chemoreception in arterial chemoreceptors. Annu. Rev. Physiol. 51:835–844

    Article  PubMed  CAS  Google Scholar 

  • Biscoe, T.J. &M.R. Duchen (1990) Monitoring PO2 by the carotid chemoreceptor. News in Physiol. Sci. 5:229–233

    Google Scholar 

  • Bisgard, G.E., R.A. Mitchell, &D.A. Herbert (1979) Effects of dopamine, norepinephrine, and 5-hydroxytryptamine on the carotid body of the dog. Respir. Physiol. 37:61–80

    Article  PubMed  CAS  Google Scholar 

  • Buerk, D.G. &S. Lahiri (1993) Detecting dopamine release in cat carotid body in response to hypoxia using nation, thin-film coated recessed microelectrodes. FASEB J. 7:3661 .

    Google Scholar 

  • Chen, I.V., R.D. Yates, &J.T. Hansen (1986) Substance P-like immunoreactivity in rat and cat carotid bodies: Light and electron microscopic studies. Histol. Histopathol. 1:203–212 .

    PubMed  CAS  Google Scholar 

  • Cragg, P.A., M. Runold, Y.R. Kou &N.R. Prabhakar (1994) Tachykinin antagonists in carotid body responses to hypoxia and substance P in the rat. Respir. Physiol. In press

    Google Scholar 

  • De Sanctis, G.T., F.H.Y. Green &J.E. Remmers. (1991) Ventilatory responses to hypoxia and hypercapnia in awake rats pretreated with capsaicin. J. Appl. Physiol. 70:1168–1174

    Article  PubMed  Google Scholar 

  • Dev, N.B. &H.H. Loescheke (1979) A cholinergic mechanism involved in the respiratory chemosensitivity of the medulla oblongata in the cat. Pflüg. Arch. 379:29–36

    Article  CAS  Google Scholar 

  • Dinger, B., C. Gonzalez, K. Yoshizaki &S. Fidone (1981) [3-H]-spiroperidol binding in normal and denervated carotid bodies. Neurosci. Lett. 21:51–55

    Article  PubMed  CAS  Google Scholar 

  • Dinger, B., C. Gonzalez, K. Yoshizaki &S. Fidone (1985) Localization and function of cat carotid body nicotinic receptors. Brain Res. 339:295–304

    Article  PubMed  CAS  Google Scholar 

  • Dinger,B.G., T. Hirano &S.J. Fidone. (1986) Autoradiographic localization of muscarinic receptors in rabbit carotid body. Brain Res. 367:328–331

    Article  PubMed  CAS  Google Scholar 

  • Donnelly, D.F. &T.P. Doyle (1993) Free tissue catecholamines of rat carotid body, in vitro, during maturation and following chronic hypoxia. Soc. Neuro. Abstract 19:574.1

    Google Scholar 

  • Fidone, S.J. &C. Gonzalez (1986) Initiation and control of chemoreceptor activity in the carotid body, in: “Handbook of Physiology - Section 3: The Respiratory System,” N.S. Cherniack &J.G. Widdicombe, eds., Am. Physiol. Soc., Bethseda, MD

    Google Scholar 

  • Fidone, S.J., C. Gonzalez &K. Yoshizaki (1982) Effects of low oxygen on the release of dopamine from the rabbit carotid body in vitro. J. Physiol. (London), 333:81–91

    CAS  Google Scholar 

  • Fishman, M.C., W.L. Greene, &D. Platika (1985) Oxygen chemoreception by carotid body cells in culture. Proc. Natl. Acad. Sci. (USA) 82:1448–1450

    Article  CAS  Google Scholar 

  • Fitzgerald, R.S. &M. Shirahata, (1992) Carotid body chemotransduction, in: “Control of Breathing and Its Modelling Perspective,” Y. Honda, Y. Miyamoto, K. Konno &J.G. Widdicombe, eds., Plenum Press, New York

    Google Scholar 

  • Folgering, H., J. Ponte &T. Sadig (1982) Adrenergic mechanisms and chemoreception in the carotid body of the cat and rabbit. J. Physiol. (London) 325:1–21

    CAS  Google Scholar 

  • Gallagher, P.J., G. Paxinos &S.W. White (1985) The role of substance P in arterial chemoreflex control of ventilation. J. Auton. Nerv. System. 12:195–210

    Article  CAS  Google Scholar 

  • Gonzalez, C., L. Almaraz, A. Obeso &R. Rigual (1992) Oxygen and acid chemoreception in the carotid body chemoreceptors. TINS 15:146–153

    PubMed  CAS  Google Scholar 

  • Hansen, G., L. Jones &S. Fidone (1986) Physiological chemoreceptor stimulation decreases enkephalin and substance P in the cat carotid body. Peptides 7:767–769

    Article  Google Scholar 

  • Ichikawa, H. &C.J. Helke, (1993) Distribution, origin and plasticity of galanin immunoreactivity in the rat carotid body. Neurosci. 52:757–767

    Article  CAS  Google Scholar 

  • Kou, Y.R., G.K. Kumar &N.R. Prabhakar (1991a) Importance of substance P in the chemoreception of the carotid body in vitro. FASEB J. 5: A1118

    Google Scholar 

  • Kou, Y.R., P. Ernsberger, P.A. Cragg, N.S. Cherniack N.R. Prabhakar, (1991b) Role of a2-adrenergic receptors in the carotid body response to isocapnic hypoxia. Respir. Physiol. 83:353–364

    Article  PubMed  CAS  Google Scholar 

  • Kumar, G.K., M. Runold, R.D. Ghai, N.S. Cherniack &N.R. Prabhakar (1990) Occurrence of neutral endopeptidase activity in the cat carotid body and its significance in chemoreception. Brain Res. 517:341–343

    Article  PubMed  CAS  Google Scholar 

  • Kummer, W., K. Addicks, M. Henkel &C. Heym (1985) Cholecystokinin-like immunoreactivity in cat extra-adrenal paraganglia. Neurosci. Lett. 55:207–210

    Article  PubMed  CAS  Google Scholar 

  • Lahiri, S., T. Nishino, A. Mokashi &E. Mulligan (1980) Interaction of dopamine and haloperidol with O2 and CO2 chemoreception in carotid body. J. Appl. Physiol. 49:45–51

    PubMed  CAS  Google Scholar 

  • Lahiri, S., M. Pokorski &R.O. Davies (1981) Augmentation of carotid body chemoreceptor responses by isoproterenol in the cat. Respir. Physiol. 44:351–364

    Article  PubMed  CAS  Google Scholar 

  • Lahiri, S., N. Smatresk, M. Pokorski, P. Barnard, A. Mokashi &K.H. McGregor (1984) Dopaminergic efferent inhibition of carotid body chemoreceptors in chronically hypoxic cats. Am. J. Physiol. 247:R24–R28

    PubMed  CAS  Google Scholar 

  • Lahiri, S., R. Iturriaga, A. Mokashi, D.K. Ray &D. Chugh (1993) CO-binding heme pigments participate in O2 chemoreception in the carotid body. FASEB J. 7:2649

    Google Scholar 

  • Lever, J.D. &J.D. Boyd (1957) Osmiophilic granules in glomus cells of the rabbitcarotid body. Nature 179:1082–1083

    Article  PubMed  CAS  Google Scholar 

  • Lever, J.D., P.R. Lewis &J.D. Boyd (1959) Observations on the fine structure and histochemistry of the carotid body in the cat and rabbit. J. Anat. 93:478–490

    PubMed  CAS  Google Scholar 

  • Maxwell, D.L., R.W. Fuller, C.M.S. Dixon, F.M.C. Cuss, &P.J. Barnes (1990) Ventilatory effects of substance P, vasoactive intestinal peptide, and nitroprusside in humans. J. Appl. Physiol. 68:295–301.

    PubMed  CAS  Google Scholar 

  • McQueen, D. S. (1980) Effects of substance P on carotid chemoreceptor activity in cats, J. Physiol. (London) 302:31–47

    CAS  Google Scholar 

  • McQueen, D.S., &J.A. Ribeiro, (1980) Inhibitory actions of methionine-enkephalin and morphine on the cat carotid chemoreceptors. Br. J. Pharmacol. 71:297–305

    PubMed  CAS  Google Scholar 

  • McQueen, D.S. &J.A. Ribeiro, (1983) On the specificity and type of receptor involved in carotid body chemoreceptor activation by adenosine in the cat. Br. J. Pharmacol. 80:347–354

    Article  PubMed  CAS  Google Scholar 

  • Milsom, W. K. &T. Sadig (1983) Interaction between norepinephrine and hypoxia on carotid body chemoreception in rabbits. J. Appl. Physiol. 55:1893–1898

    PubMed  CAS  Google Scholar 

  • Mir, A.K., D.J. Pallot &S.R. Nahorski (1983) Biogenic amine stimulated cyclic adenosine-3’, 5’-monophosphate formation in the rat carotid body. J. Neurochem. 41:663–669

    Article  PubMed  CAS  Google Scholar 

  • Mir, A.K, D.S. McQueen, D.J. Pallot &S.R. Nahorski (1984) Direct biochemical and neuropharmacological identification of dopamine D-2 receptors in the rabbit carotid body Brain Res. 291:273–283

    Article  PubMed  CAS  Google Scholar 

  • Monti-Bloch, L. &C. Eyzaguirre (1980) A comparative physiological and pharmacological study of cat and rabbit carotid body chemoreceptors. Brain Res. 193:449–470

    Article  PubMed  CAS  Google Scholar 

  • Monti-Bloch, L. &C. Eyzaguirre (1985) Effects of methionine-enkephalin and substance P on the chemosensory discharge of the cat carotid body. Brain Res. 338:297–307

    Article  PubMed  CAS  Google Scholar 

  • Nishi, K. (1975) The action of 5-hydroxytryptamine on chemoreceptor discharges of the cat’s carotid body. Br. J. Pharmacol. 55:27–40

    Article  PubMed  CAS  Google Scholar 

  • O’Regan, R.G. (1981) Responses of carotid body chemosensory activity and blood flow to stimulation of sympathetic nerves in the cat. J. Physiol. (London) 315:81–88

    Google Scholar 

  • Pearse, A.G.E. (1969) The cytochemistry and ultrastructure of polypeptide hormone-producing cells of the APUD series and the embryologic, physiologic and pathologic implications of the concept. J. Histochem. Cytochem. 17:303–313

    Article  PubMed  CAS  Google Scholar 

  • Pokorski, M., &S. Lahiri (1981) Effects of naloxone on carotid body chemoreception and ventilation in the cat. J. Appl. Physiol. 51:1533–1538

    PubMed  CAS  Google Scholar 

  • Ponte, J. &C.L. Sadler (1989) Interactions between hypoxia, acetylcholine and dopamine in the carotid body of rabbit and cat. J. Physiol. (London) 410:595–610

    Google Scholar 

  • Prabhakar, N.R., M. Runold, G.K. Kumar, N.S. Cherniack, &A. Scarpa (1989a) Substance P and mitochondrial oxygen consumption: Evidence for a direct intracellular role for the peptide. Peptides. 10:1003–1006

    Article  PubMed  CAS  Google Scholar 

  • Prabhakar, N.R., S.C. Landis, G.K. Kumar, D.M. Kilpatrick, N.S. Cherniack &S.E. Leeman (1989b) Substance P and neurokinin-A in the cat carotid body: Localization, exogenous effects and changes in content in response to arterial PO2. Brain Res. 481:205–214.

    Article  PubMed  CAS  Google Scholar 

  • Prabhakar, N.R. (1992) Significance of excitatory and inhibitory neurochemicals in hypoxic chemotransmission of the carotid body. In: “Control of Breathing and Its Modelling Perspective.” Y. Honda, Y. Miyamoto, K. Konno &J.G. Widdicombe. eds., Plenum Press, New York.

    Google Scholar 

  • Prabhakar, N.R.. Y-R. Kou, P.A. Cragg &N.S. Cherniack (1992) Effect of arterial chemoreceptor stimulation: Role of norepinephrine in hypoxic chemotransmission. in: “Neurobiology and Cell Physiology of Chemoreception,” P.G. Data, S. Lahiri &H. Acker, eds., Plenum Press, New York, In press .

    Google Scholar 

  • Prabhakar, N.R., R. Sharma, F. Agani &M. Gratzl (1993a) Detection ofneurochemical release induced by chemical stimulants and hypoxia from PC-12 and carotid body cells with microvoltammetry. FASEB J.7:2302

    Google Scholar 

  • Prabhakar, N.R., G.K. Kumar, C.H. Chang, F.H. Agani &M.A. Haxhiu (1993b) Nitric oxide in the sensory function of the carotid body. Brain Res. 625:16–22

    Article  PubMed  CAS  Google Scholar 

  • Prabhakar, N.R., F.H. Agani, J.L. Dinerman &S.H. Snyder (1993c) Endogenous carbon monoxide (CO) and carotid body sensory activity. Soc. Neurosci. 19:574.3

    Google Scholar 

  • Prabhakar, N.R., H. Cao, J.A. Lowe, III &R.M. Snider (1993d) Selective inhibition of the carotid body sensory response to hypoxia by the substance P receptor antagonist CP-96,345. Proc. Natl. Acad. Sci. (USA) In press

    Google Scholar 

  • Prabhakar, N.R. &Y.R. Kou, (1994) Inhibitory sympathetic action on the carotid body responses to sustained hypoxia. Respir. Physiol., In press

    Google Scholar 

  • Runold, M., N.S. Cherniack &N.R. Prabhakar (1990a) Effect of adenosine on chemosensory activity of the cat aortic body. Res. Physiol. 80:299–306

    Article  CAS  Google Scholar 

  • Runold, M., N.S. Cherniack &N.R. Prabhakar (1990b) Effect of adenosine on isolated and superfused cat carotid body activity. Neurosci. Lett. 113:111–114.

    Article  PubMed  CAS  Google Scholar 

  • Schweitzer A. &S. Wright (1938) Action of prostigmin and acetylcholine on respiration. Q. J. Exp. Physiol. 28:33–47

    CAS  Google Scholar 

  • Snyder, S.H. (1992) Nitric oxide: First in a new class of neurotransmitters. Science 257:494–496

    Article  PubMed  CAS  Google Scholar 

  • Torrance, R.W. (1968) Prolegomena. In: “Arterial Chemoreceptors,” R,W.Torrance, ed.. Blackwell, Oxford

    Google Scholar 

  • Wang, Z.-Z., L. He, L.J. Stensaas, B.G. Dinger &S.J. Fidone (1991) Localization and in vitro action of atrial natriuretic peptide in the cat carotid body. J. Appl. Physiol. 70:942–946

    PubMed  CAS  Google Scholar 

  • Wang, Z.-Z., D.S. Berdt, S.H. Snyder, S.J. Fidone &L.J. Stensaas (1992a) Nitric oxide synthase in the carotid body. Soc. Neurosci. 18:1197

    Google Scholar 

  • Wang, Z.-Z., L.J. Stensaas, B. Dinger &SJ. Fidone (1992b) Coexistence of biogenic amines and neuropeptide in type I cells of the cat carotid body. Neurosci. 47:473–480

    Article  CAS  Google Scholar 

  • Ward, D.S. &M. Nino (1992) The effects of dopamine on the ventilatory response to sustained hypoxia in humans. In: “Control of Breathing and its Modelling Perspectives,” Y. Honda, Y. Miyamoto, K. Konno &J.G. Widdicombe, eds., Plenum Press, New York

    Google Scholar 

  • Zapata, P. (1975) Effects of dopamine on carotid chemo-and baroreceptors in vitro. J. Physiol. (Lond) 244:235–251

    CAS  Google Scholar 

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Prabhakar, N.R. (1994). Neurotransmitters in the Carotid Body. In: O’Regan, R.G., Nolan, P., McQueen, D.S., Paterson, D.J. (eds) Arterial Chemoreceptors. Advances in Experimental Medicine and Biology, vol 360. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-2572-1_6

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  • DOI: https://doi.org/10.1007/978-1-4615-2572-1_6

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