In vitro characterization of noradrenergic modulation of chemosensitive neurons in the retrotrapezoid nucleus

Journal of Neurophysiology

Volumn 116, Issue 3, 2016, Pages 1024-1035

  Kuo, Fu Shan ^a   Falquetto, Bárbara ^b   Chen, Dawei ^a   Oliveira, Luiz M ^b   Takakura, Ana C ^b   Mulkey, Daniel K ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Adrenergic receptors; Chemoreception; KCNQ channels; Neonatal brain slice; Norepinephrine

Indexed keywords

10,10 BIS(4 PYRIDINYLMETHYL) 9(10H) ANTHRACENONE; ADENOSINE TRIPHOSPHATE; ALPHA 1 ADRENERGIC RECEPTOR; ALPHA 1 ADRENERGIC RECEPTOR BLOCKING AGENT; CARBON DIOXIDE; HYDROGEN; NORADRENALIN; POTASSIUM CHANNEL KCNQ; SEROTONIN; ADRENERGIC RECEPTOR; ADRENERGIC RECEPTOR STIMULATING AGENT; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; SODIUM CHANNEL BLOCKING AGENT; TETRODOTOXIN;

ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN NUCLEUS; CHEMORECEPTOR; CHEMOSENSITIVITY; CONTROLLED STUDY; ELECTRIC POTENTIAL; IN VITRO STUDY; MEMBRANE CONDUCTANCE; MEMBRANE CURRENT; NERVE CELL; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE POTENTIAL; NEUROMODULATION; NEWBORN; NONHUMAN; NORADRENERGIC SYSTEM; PRIORITY JOURNAL; RAT; RETROTRAPEZOID NUCLEUS; VOLTAGE CLAMP TECHNIQUE; ACTION POTENTIAL; ANALYSIS OF VARIANCE; ANIMAL; CHEMORECEPTOR CELL; CYTOLOGY; DOSE RESPONSE; DRUG EFFECTS; METABOLISM; PATCH CLAMP TECHNIQUE; PHYSIOLOGY; RESPIRATION CENTER;

ACTION POTENTIALS; ADRENERGIC AGENTS; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; ASTROCYTES; CARBON DIOXIDE; CHEMORECEPTOR CELLS; DOSE-RESPONSE RELATIONSHIP, DRUG; IN VITRO TECHNIQUES; NEUROTRANSMITTER AGENTS; NOREPINEPHRINE; PATCH-CLAMP TECHNIQUES; RATS; RECEPTORS, ADRENERGIC; RESPIRATORY CENTER; SODIUM CHANNEL BLOCKERS; TETRODOTOXIN;

EID: 84986203176     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00022.2016     Document Type: Article

References (63)

1. + channels: form and function. Annu Rev Physiol 74: 245-269, 2012.
2. Arata A, Onimaru H, Homma I. The adrenergic modulation of firings of respiratory rhythm-generating neurons in medulla-spinal cord preparation from newborn rat. Exp Brain Res 119: 399-408, 1998.
3. + channel knock-out mice reveal the identity of calcium-dependent afterhyperpolarization currents. J Neurosci 24: 5301-5306, 2004.
4. Brown RE, Basheer R, McKenna JT, Strecker RE, McCarley RW. Control of sleep and wakefulness. Physiol Rev 92: 1087-1187, 2012.
5. Burton MD, Johnson DC, Kazemi H. Adrenergic and cholinergic interaction in central ventilatory control. J Appl Physiol (1985) 68: 2092-2099, 1990.
6. Cream C, Li A, Nattie E. The retrotrapezoid nucleus (RTN): local cytoarchitecture and afferent connections. Respir Physiol Neurobiol 130: 121-137, 2002.
7. Errchidi S, Monteau R, Hilaire G. Noradrenergic modulation of the medullary respiratory rhythm generator in the newborn rat: an in vitro study. J Physiol 443: 477-498, 1991.
8. Folgering H. Central beta-adrenergic effects on the control of ventilation in cats. Respiration 39: 131-138, 1980.
9. Funk GD, Smith JC, Feldman JL. Development of thyrotropin-releasing hormone and norepinephrine potentiation of inspiratory-related hypoglossal motoneuron discharge in neonatal and juvenile mice in vitro. J Neurophysiol 72: 2538-2541, 1994.
10. Funk GD, Zwicker JD, Selvaratnam R, Robinson DM. Noradrenergic modulation of hypoglossal motoneuron excitability: developmental and putative state-dependent mechanisms. Arch Ital Biol 149: 426-453, 2011.
11. Gourine AV, Kasymov V, Marina N, Tang F, Figueiredo MF, Lane S, Teschemacher AG, Spyer KM, Deisseroth K, Kasparov S. Astrocytes control breathing through pH-dependent release of ATP. Science 329: 571-575, 2010.
12. Guyenet PG, Mulkey DK. Retrotrapezoid nucleus and parafacial respiratory group. Respir Physiol Neurobiol 173: 244-255, 2010.
13. Guyenet PG, Mulkey DK, Stornetta RL, Bayliss DA. Regulation of ventral surface chemoreceptors by the central respiratory pattern generator. J Neurosci 25: 8938-8947, 2005.
14. Guyenet PG, Stornetta RL, Abbott SB, Depuy SD, Fortuna MG, Kanbar R. Central CO2 chemoreception and integrated neural mechanisms of cardiovascular and respiratory control. J Appl Physiol (1985) 108: 995-1002, 2010.
15. Happe HK, Coulter CL, Gerety ME, Sanders JD, O’Rourke M, Bylund DB, Murrin LC. Alpha-2 adrenergic receptor development in rat CNS: an autoradiographic study. Neuroscience 123: 167-178, 2004.
16. Hawkins VE, Hawryluk JM, Takakura AC, Tzingounis AV, Moreira TS, Mulkey DK. HCN channels contribute to serotonergic modulation of ventral surface chemosensitive neurons and respiratory activity. J Neurophysiol 113: 1195-1205, 2015.
17. Hawryluk JM, Moreira TS, Takakura AC, Wenker IC, Tzingounis AV, Mulkey DK. KCNQ channels determine serotonergic modulation of ventral surface chemoreceptors and respiratory drive. J Neurosci 32: 16943-16952, 2012.
18. Hilaire G, Viemari JC, Coulon P, Simonneau M, Bevengut M. Modulation of the respiratory rhythm generator by the pontine noradrenergic A5 and A6 groups in rodents. Respir Physiol Neurobiol 143: 187-197, 2004.
19. Hodges MR, Wehner M, Aungst J, Smith JC, Richerson GB. Transgenic mice lacking serotonin neurons have severe apnea and high mortality during development. J Neurosci 29: 10341-10349, 2009.
20. Horner RL. Emerging principles and neural substrates underlying tonic sleep-state-dependent influences on respiratory motor activity. Philos Trans R Soc Lond B Biol Sci 364: 2553-2564, 2009.
21. Huckstepp RT, Id BR, Eason R, Spyer KM, Dicke N, Willecke K, Marina N, Gourine AV, Dale N. Connexin hemichannel-mediated CO2-dependent release of ATP in the medulla oblongata contributes to central respiratory chemosensitivity. J Physiol 588: 3901-3920, 2010.
22. Katz DM, Dutschmann M, Ramirez JM, Hilaire G. Breathing disorders in Rett syndrome: progressive neurochemical dysfunction in the respiratory network after birth. Respir Physiol Neurobiol 168: 101-108, 2009.
23. Kumar NN, Velic A, Soliz J, Shi Y, Li K, Wang S, Weaver JL, Sen J, Abbott SB, Lazarenko RM, Ludwig MG, Perez-Reyes E, Mohebbi N, Bettoni C, Gassmann M, Suply T, Seuwen K, Guyenet PG, Wagner CA, Bayliss DA. Physiology. Regulation of breathing by CO2 requires the proton-activated receptor GPR4 in retrotrapezoid nucleus neurons. Science 348: 1255-1260, 2015.
24. Lazarenko RM, Milner TA, Depuy SD, Stornetta RL, West GH, Kievits JA, Bayliss DA, Guyenet PG. Acid sensitivity and ultrastructure of the retrotrapezoid nucleus in Phox2b-EGFP transgenic mice. J Comp Neurol 517: 69-86, 2009.
25. Leeb-Lundberg LM, Cotecchia S, DeBlasi A, Caron MG, Lefkowitz RJ. Regulation of adrenergic receptor function by phosphorylation. I. Agonistpromoted desensitization and phosphorylation of alpha 1-adrenergic receptors coupled to inositol phospholipid metabolism in DDT1 MF-2 smooth muscle cells. J Biol Chem 262: 3098-3105, 1987.
26. Li A, Nattie E. Catecholamine neurones in rats modulate sleep, breathing, central chemoreception and breathing variability. J Physiol 570: 385-396, 2006.
27. Li YW, Guyenet PG, Bayliss DA. Voltage-dependent calcium currents in bulbospinal neurons of neonatal rat rostral ventrolateral medulla: modulation by alpha2-adrenergic receptors. J Neurophysiol 79: 583-594, 1998.
28. Marzo A, Bai J, Otani S. Neuroplasticity regulation by noradrenaline in mammalian brain. Curr Neuropharmacol 7: 286-295, 2009.
29. Mulkey DK, Henderson RA III, Olson JE, Putnam RW, Dean JB. Oxygen measurements in brain stem slices exposed to normobaric hyperoxia and hyperbaric oxygen. J Appl Physiol 90: 1887-1899, 2001.
30. Mulkey DK, Stornetta RL, Weston MC, Simmons JR, Parker A, Bayliss DA, Guyenet PG. Respiratory control by ventral surface chemoreceptor neurons in rats. Nat Neurosci 7: 1360-1369, 2004.
31. + sensing by astrocytes in the retrotrapezoid nucleus and their possible contribution to respiratory drive. Exp Physiol 96: 400-406, 2011.
32. Murrin LC, Sanders JD, Bylund DB. Comparison of the maturation of the adrenergic and serotonergic neurotransmitter systems in the brain: implications for differential drug effects on juveniles and adults. Biochem Pharmacol 73: 1225-1236, 2007.
33. Nasse JS, Travers JB. Adrenoreceptor modulation of oromotor pathways in the rat medulla. J Neurophysiol 112: 580-593, 2014.
34. Nattie E, Li A. Central chemoreception is a complex system function that involves multiple brain stem sites. J Appl Physiol (1985) 106: 1464-1466, 2009.
35. Nattie E, Li A. Central chemoreceptors: locations and functions. Compr Physiol 2: 221-254, 2012.
36. O’Donnell J, Zeppenfeld D, McConnell E, Pena S, Nedergaard M. Norepinephrine: a neuromodulator that boosts the function of multiple cell types to optimize CNS performance. Neurochem Res 37: 2496-2512, 2012.
37. Oliveira LM, Moreira TS, Kuo F, Mulkey DK, Takakura AC. _1- and _2-Adernergic receptors in the retrotrapezoid nucleus differentially regulate breathing in anesthetized adult rats. J Neurophysiol. In press, 2016.
38. Parkis MA, Bayliss DA, Berger AJ. Actions of norepinephrine on rat hypoglossal motoneurons. J Neurophysiol 74: 1911-1919, 1995.
39. Patrick JM, Pearson SB. beta-Adrenoceptor blockade and ventilation in man. Br J Clin Pharmacol 10: 624-625, 1980.
40. Paukert M, Agarwal A, Cha J, Doze VA, Kang JU, Bergles DE. Norepinephrine controls astroglial responsiveness to local circuit activity. Neuron 82: 1263-1270, 2014.
41. Perkins KL. Cell-attached voltage-clamp and current-clamp recording and stimulation techniques in brain slices. J Neurosci Methods 154: 1-18, 2006.
42. Pineda J, Aghajanian GK. Carbon dioxide regulates the tonic activity of locus coeruleus neurons by modulating a proton- and polyamine-sensitive inward rectifier potassium current. Neuroscience 77: 723-743, 1997.
43. Ramirez JM, Ward CS, Neul JL. Breathing challenges in Rett syndrome: lessons learned from humans and animal models. Respir Physiol Neurobiol 189: 280-287, 2013.
44. Ray RS, Corcoran AE, Brust RD, Kim JC, Richerson GB, Nattie E, Dymecki SM. Impaired respiratory and body temperature control upon acute serotonergic neuron inhibition. Science 333: 637-642, 2011.
45. Rekling JC, Funk GD, Bayliss DA, Dong XW, Feldman JL. Synaptic control of motoneuronal excitability. Physiol Rev 80: 767-852, 2000.
46. Rosin DL, Chang DA, Guyenet PG. Afferent and efferent connections of the rat retrotrapezoid nucleus. J Comp Neurol 499: 64-89, 2006.
47. Schnell C, Negm M, Driehaus J, Scheller A, Hulsmann S. Norepinephrineinduced calcium signaling in astrocytes in the respiratory network of the ventrolateral medulla. Respir Physiol Neurobiol 226: 18-23, 2016.
48. Selvaratnam SR, Parkis MA, Funk GD. Developmental modulation of mouse hypoglossal nerve inspiratory output in vitro by noradrenergic receptor agonists. Brain Res 805: 104-115, 1998.
49. Silva JN, Lucena EV, Silva TM, Damasceno RS, Takakura AC, Moreira TS. Inhibition of the pontine Kölliker-Fuse nucleus reduces genioglossal activity elicited by stimulation of the retrotrapezoid chemoreceptor neurons. Neuroscience 328: 9-21, 2016.
50. Sobrinho CR, Kuo FS, Barna BF, Moreira TS, Mulkey DK. Cholinergic control of ventral surface chemoreceptors involves Gq/IP-mediated inhibition of KCNQ channels. J Physiol 594: 407-419, 2016.
51. + channel, is modulated by multiple neurotransmitters in motoneurons. Neuron 25: 399-410, 2000.
52. Tzingounis AV, Nicoll RA. Contribution of KCNQ2 and KCNQ3 to the medium and slow afterhyperpolarization currents. Proc Natl Acad Sci U S A 105: 19974-19979, 2008.
53. Viemari JC. Noradrenergic modulation of the respiratory neural network. Respir Physiol Neurobiol 164: 123-130, 2008.
54. Viemari JC, Garcia AJ III, Doi A, Elsen G, Ramirez JM. beta-Noradrenergic receptor activation specifically modulates the generation of sighs in vivo and in vitro. Front Neural Circuits 7: 179, 2013.
55. Viemari JC, Ramirez JM. Norepinephrine differentially modulates different types of respiratory pacemaker and nonpacemaker neurons. J Neurophysiol 95: 2070-2082, 2006.
56. Viemari JC, Roux JC, Tryba AK, Saywell V, Burnet H, Pena F, Zanella S, Bevengut M, Barthelemy-Requin M, Herzing LB, Moncla A, Mancini J, Ramirez JM, Villard L, Hilaire G. Mecp2 deficiency disrupts norepinephrine and respiratory systems in mice. J Neurosci 25: 11521-11530, 2005.
57. Viemari JC, Tryba AK. Bioaminergic neuromodulation of respiratory rhythm in vitro. Respir Physiol Neurobiol 168: 69-75, 2009.
58. Wakabayashi I, Hatake K, Kakishita E, Hishida S, Nagai K. Desensitization of alpha-1 adrenergic receptor mediated smooth muscle contraction in aorta from endotoxic rats. Life Sci 45: 509-515, 1989.
59. + and CO2. J Neurosci 33: 7756-7761, 2013.
60. + by inhibition of a Kir4.1-Kir51-like current and may contribute to chemoreception by a purinergic mechanism. J Neurophysiol 104: 3042-3052, 2010.
61. +-sensitive neurons by purinergic signaling. J Physiol 590: 2137-2150, 2012.
62. Zanella S, Doi A, Garcia AJ III, Elsen F, Kirsch S, Wei AD, Ramirez JM. When norepinephrine becomes a driver of breathing irregularities: how intermittent hypoxia fundamentally alters the modulatory response of the respiratory network. J Neurosci 34: 36-50, 2014.
63. Zanella S, Roux JC, Viemari JC, Hilaire G. Possible modulation of the mouse respiratory rhythm generator by A1/C1 neurones. Respir Physiol Neurobiol 153: 126-138, 2006.