Neither serotonin nor adenosine-dependent mechanisms preserve ventilatory capacity in ALS rats

Respiratory Physiology and Neurobiology

Volumn 197, Issue 1, 2014, Pages 19-28

  Nichols, N L ^a   Johnson, R A ^a   Satriotomo, I ^a   Mitchell, G S ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Compensatory plasticity; Facilitation; Plethysmography; Respiration

Indexed keywords

ADENOSINE; ADENOSINE RECEPTOR; APOCYNIN; FENCLONINE; METHYSERGIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SEROTONIN; ACETOPHENONE DERIVATIVE; ADENOSINE A2 RECEPTOR ANTAGONIST; COPPER ZINC SUPEROXIDE DISMUTASE; ENZYME INHIBITOR; MSX 3 COMPOUND; SEROTONIN ANTAGONIST; SUPEROXIDE DISMUTASE; XANTHINE DERIVATIVE;

ADULT; AIR CONDITIONING; AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREATHING; CONTROLLED STUDY; ENZYME INHIBITION; LUNG CAPACITY; MALE; MOTONEURON; NONHUMAN; PHRENIC NERVE; PLASTICITY; PLETHYSMOGRAPHY; PRIORITY JOURNAL; RAT; SEROTONIN RELEASE; SHAM PROCEDURE; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; GENETICS; HUMAN; LUNG VENTILATION; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT; TIDAL VOLUME; TRANSGENIC RAT;

ACETOPHENONES; ADENOSINE; ADENOSINE A2 RECEPTOR ANTAGONISTS; AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; ENZYME INHIBITORS; HUMANS; MALE; METHYSERGIDE; MOTOR NEURONS; NADPH OXIDASE; PHRENIC NERVE; PLETHYSMOGRAPHY; PULMONARY VENTILATION; RATS, SPRAGUE-DAWLEY; RATS, TRANSGENIC; RESPIRATION; SEROTONIN; SEROTONIN ANTAGONISTS; SUPEROXIDE DISMUTASE; TIDAL VOLUME; XANTHINES;

EID: 84904290552     PISSN: 15699048     EISSN: 18781519     Source Type: Journal    
DOI: 10.1016/j.resp.2014.03.005     Document Type: Article

References (70)

1. Aghajanian G.K. Influence of drugs on the firing of serotonin-containing neurons in brain. Fed. Proc. 1972, 31:91-96.
2. Alexander G.J., Kopeloff L.M., Alexander R.B. Serotonin and norepinephrine, long-term decrease in rate of synthesis in brain of rats primed with p-chlorophenylalanine. Neurochem. Res. 1980, 5:879-883.
3. Bach K.B., Mitchell G.S. Hypoxia-induced long-term facilitation of respiratory activity is serotonin dependent. Respir. Physiol. 1996, 104:251-260.
4. Baker-Herman T.L., Fuller D.D., Bavis R.W., Zabka A.G., Golder F.J., Doperalski N.J., Johnson R.A., Watters J.J., Mitchell G.S. BDNF is necessary and sufficient for spinal respiratory plasticity following intermittent hypoxia. Nat. Neurosci. 2004, 7:48-55.
5. Boillée S., Vande Velde C., Cleveland D.W. ALS: a disease of motor neurons and their nonneuronal neighbors. Neuron 2006, 52:39-59.
6. Boulenguez P., Gestreau C., Vinit S., Stamegna J.C., Kastner A., Gauthier P. Specific and artifactual labeling in the rat spinal cord and medulla after injection of monosynaptic retrograde tracers into the diaphragm. Neurosci. Lett. 2007, 417(2):206-211.
7. Bourke S.C., Shaw P.J., Gibson G.J. Respiratory function vs. sleep-disordered breathing as predictors of QOL in ALS. Neurology 2001, 57:2040-2044.
8. Bruijn L., Becher I., Lee M.W., Anderson M.K., Jenkins K.L., Copeland N.A., Sisodia N.G., Rothstein S.S., Borchelt J.D., Price D.R., Cleveland D.L.D.W. ALS-linked SOD1 mutant G85R mediates damage to astrocytes and promotes rapidly progressive disease with SOD1-containing inclusions. Neuron 1997, 18(2):327-338.
9. Carlton S.M., Steinman J.L., Hillman G.R., Willis W.D. Differential effects of p-chlorophenylalanine on indoleamines in brainstem nuclei and spinal cord of rats. II. Identification of immunohistochemically stained structures using computer-assisted image enhancement techniques. Brain Res. 1987, 426:310-322.
10. Dale E.A., Satriotomo I., Mitchell G.S. Cervical spinal erythropoietin induces phrenic motor facilitation via extracellular signal-regulated protein kinase and Akt signaling. J. Neurosci. 2012, 32(17):5973-5983.
11. Dale-Nagle E.A., Hoffman M.S., MacFarlane P.M., Mitchell G.S. Multiple pathways to long-lasting phrenic motor facilitation. Adv. Exp. Med. Biol. 2010, 669:225-230.
12. Dale-Nagle E.A., Satriotomo I., Mitchell G.S. Spinal vascular endothelial growth factor induces phrenic motor facilitation via extracellular signal-regulated kinase and Akt signaling. J. Neurosci. 2011, 31(21):7682-7690.
13. Deguchi T., Sinha A.K., Barchas J.D. Biosynthesis of serotonin in raphe nuclei of rat brain: effect of p-chlorophenylalanine. J. Neurochem. 1973, 20:1329-1336.
14. Drorbaugh J.E., Fenn W.O. A barometric method for measuring ventilation in newborn infants. Pediatrics 1955, 16:81-87.
15. Eldridge F.L., Millhorn D.E. Oscillation, gating and memory in the respiratory control system. Handbook of Physiology, Section 3: The Respiratory System, Vol. II: Control of Breathing, Part 1 1986, 93-114. American Physiological Society, Bethesda, MD.
16. Feldman J.L., Mitchell G.S., Nattie E.E. Breathing: rhythmicity, plasticity chemosensitivity. Annu. Rev. Neurosci. 2003, 26:239-266.
17. Fuller D.D., Zabka A., Baker T.L., Mitchell G.S. Physiological and genomic consequences of intermittent hypoxia: selected contribution: phrenic long-term facilitation requires 5-HT receptor activation during but not following episodic hypoxia. J. Appl. Physiol. 2001, 90:2001-2006.
18. Glennon, R.A., Dukat, M., Westkaemper, R.B., 2000. Serotonin Receptor Subtypes and Ligands. In: F.E. Bloom, D.J. Kupfer (Eds.), Psychopharmacology: - The Fourth Generation of Progress. New York.
19. Golder F.J., Ranganathan L., Satriotomo I., Hoffman M., Lovett-Barr M.R., Watters J.J., Baker-Herman T.L., Mitchell G.S. Spinal adenosine A2a receptor activation elicits long-lasting phrenic motor facilitation. J. Neurosci. 2008, 28:2033-2042.
20. Gurney M.E., Pu H., Chiu A.Y., Dal Canto M.C., Polchow C.Y., Alexander D.D., Caliendo J., Hentati A., Kwon Y.W., Deng H.X., et al. Motor neuron degeneration in mice that express a human Cu, Zn superoxide dismutase mutation. Science 1994, 264(5166):1772-1775.
21. Hayashi F., Hinrichsen C.F., McCrimmon D.R. Short-term plasticity of descending synaptic input to phrenic motoneurons in rats. J. Physiol. 2003, 94(4):1421-1430.
22. Hoffman M.S., Mitchell G.S. Spinal 5-HT7 receptor activation induces long-lasting phrenic motor facilitation. J. Physiol. 2011, 589(6):1397-1407.
23. Hoffman M.S., Golder F.J., Mahamed S., Mitchell G.S. Spinal adenosine A2(A) receptor inhibition enhances phrenic long term facilitation following acute intermittent hypoxia. J. Physiol. 2010, 588(Pt 1):255-266.
24. Hougee S., Hartog A., Sanders A., Graus Y.M., Hoijer M.A., Garssen J., van den Berg W.B., van Beuningen H.M., Smit H.F. Oral administration of the NADPH-oxidase inhibitor apocynin partially restores diminished cartilage proteoglycan synthesis and reduces inflammation in mice. Eur. J. Pharmacol. 2006, 531(1-3):264-269.
25. Howland D.S., Liu J., She Y., Goad B., Maragakis N.J., Kim B., Erickson J., Kulik J., DeVito L., Psaltis G., DeGennaro L.J., Cleveland D.W., Rothstein J.D. Focal loss of the glutamate transporter EAAT2 in a transgenic rat model of SOD1 mutant-mediated amyotrophic lateral sclerosis (ALS). Proc. Natl. Acad. Sci. U. S. A. 2002, 99(3):1604-1609.
26. Hoyer D., Clarke D.E., Fozard J.R., Hartig P.R., Martin G.R., Mylecharane E.J., Saxena P.R., Humphrey P.P.A. International union of pharmacology classification of receptors for 5-hydroxytryptamine (serotonin). Pharmacol. Rev. 1994, 46:157-203.
27. Huxtable A.G., MacFarlane P.M., Vinit S., Nichols N.L., Dale E.A., Mitchell G.S. Adrenergic a1 receptor activation is sufficient, but not necessary for phrenic long-term facilitation. J. Appl. Physiol 2014, 10.1152/japplphysiol.00904.2013.
28. Jacky J.P. A plethysmograph for long-term measurements of ventilation in unrestrained animals. J. Appl. Physiol. 1978, 45(4):644-647.
29. Jacobs B.L., Azmitia E.C. Structure and function of the brain serotonin system. Physiol. Rev. 1992, 72:165-229.
30. Johnson R.A., Mitchell G.S. Common mechanisms of compensatory respiratory plasticity in spinal neurological disorders. Respir. Physiol. Neurobiol. 2013, 189(2):419-428.
31. Kinkead R., Mitchell G.S. Time-dependent hypoxic ventilatory responses in rats: effects of ketanserin and 5 carboxamidotryptamine. Am. J. Physiol. 1999, 277(2 Pt 2):R658-R666.
32. Kuhar M.J., Forth R.H., Aghajanian G.K. Selective reduction of tryptophan hydroxylase activity in rat forebrain after midbrain raphe lesions. Brain Res. 1971, 35:167-176.
33. Lechtzin N., Rothstein J., Clawson L., Diette G., Wiener C.M. Amyotrophic lateral sclerosis: evaluation and treatment of respiratory impairment. Amyotrophic Lateral Sclerosis 2002, 3:5-13.
34. Lee F.S., Chao M.V. Activation of Trk neurotrophin receptors in the absence of neurotrophins. Proc. Natl. Acad. Sci. U. S. A. 2001, 98(6):3555-3560.
35. Ling L. Serotonin and NMDA receptors in respiratory long-term facilitation. Respir. Physiol. Neurobiol. 2008, 164(1/2):233-241.
36. Lyall R.A., Donaldson N., Polkey M.I., Leigh P.N., Moxham J. Respiratory muscle strength and ventilatory failure in amyotrophic lateral sclerosis. Brain 2001, 124(10):110-118.
37. MacFarlane P.M., Mitchell G.S. Serotonin-induced phrenic long-term facilitation requires reactive oxygen species signaling via the NADPH oxidase complex. Soc. Neurosci. Abst. 2007, Program No. 520.15.
38. MacFarlane P.M., Mitchell G.S. NADPH oxidase activity is necessary for phrenic motor facilitation induced by 5HT2B receptor activation. FASEB J. 2008, 22:1232-1237.
39. MacFarlane P.M., Mitchell G.S. Respiratory long-term facilitation following intermittent hypoxia requires reactive oxygen species formation. Neuroscience 2008, 152:189-197.
40. MacFarlane P.M., Mitchell G.S. Episodic spinal serotonin receptor activation elicits long-lasting phrenic motor facilitation by an NADPH oxidase-dependent mechanism. J. Physiol. 2009, 587(Pt 22):5469-5481.
41. MacFarlane P.M., Wilkerson J.E., Lovett-Barr M.R., Mitchell G.S. Reactive oxygen species and respiratory plasticity following intermittent hypoxia. Respir. Physiol. Neurobiol. 2008, 164:263-271.
42. MacFarlane P.M., Satriotomo I., Windelborn J.A., Mitchell G.S. NADPH oxidase activity is necessary for acute intermittent hypoxia-induced phrenic long-term facilitation. J. Physiol. 2009, 587(Pt 9):1931-1942.
43. MacFarlane P.M., Vinit S., Mitchell G.S. Serotonin 2A and 2B receptor-induced phrenic motor facilitation: differential requirement for spinal NADPH oxidase activity. Neuroscience 2011, 178:45-55.
44. Mahamed S., Strey K.A., Mitchell G.S., Baker-Herman T.L. Reduced respiratory neural activity elicits phrenic motor facilitation. Respir. Physiol. Neurobiol. 2011, 175(3):303-309.
45. McCrimmon D.R., Mitchell G.S., Dekin M. Glutamate, GABA and Serotonin in Ventilatory Control 1995, 151-218. M. Dekker, New York.
46. McGuire M., Zhang Y., White D.P., Ling L. Serotonin receptor subtypes required for ventilatory long-term facilitation and its enhancement after chronic intermittent hypoxia in awake rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2004, 286:334-341.
47. Millhorn D.E., Eldridge F.L., Waldrop T.G. Prolonged stimulation of respiration by endogenous central serotonin. Respir. Physiol. 1980, 42:171-188.
48. Nagai M., Aoki M., Miyoshi I., Kato M., Pasinelli P., Kasai N., Brown R.H., Itoyama Y. Rats expressing human cytosolic copper-zinc superoxide dismutase trangenes with amyotrophic lateral sclerosis: associated mutations develop motor neuron disease. J. Neurosci. 2001, 21(23):9246-9254.
49. Nichols N.L., Johnson R.A., Satriotomo I., Nashold L.J., Mitchell G.S. Serotonin depletion does not impair ventilation in the SOD1G93A rat, a model of amyotrophic lateral sclerosis (ALS). FASEB J. 2009, 23:784-788.
50. Nichols N.L., Gowing G., Satriotomo I., Nashold L.J., Dale E.A., Suzuki M., Avalos P., Mulcrone P.L., McHugh J., Svendsen C.N., Mitchell G.S. Intermittent hypoxia and stem cell implants preserve breathing capacity in a rodent model of amyotrophic lateral sclerosis. Am. J. Respir. Crit. Care Med. 2013, 187(5):535-542.
51. Nichols N.L., Van Dyke J., Nashold L., Satriotomo I., Suzuki M., Mitchell G.S. Ventilatory control in ALS. Respir. Physiol. Neurobiol. 2013, 189(2):429-437.
52. Olson E.B., Dempsey J.A., McCrimmon D.R. Serotonin and the control of ventilation in awake rats. J. Clin. Invest. 1979, 64:689-693.
53. Peng Y.J., Nanduri J., Yuan G., Wang N., Deneris E., Pendyala S., Natarajan V., Kumar G.K., Prabhakar N.R. NADPH oxidase is required for the sensory plasticity of the carotid body by chronic intermittent hypoxia. J. Neurosci. 2009, 29(15):4903-4910.
54. Prabhakar N.R. Sensory plasticity of the carotid body: role of reactive oxygen species and physiological significance. Respir. Physiol. Neurobiol. 2011, 178(3):375-380.
55. Prabhakar N.R., Peng Y.J., Yuan G., Kumar G.K. Reactive oxygen species facilitate oxygen sensing. Novartis Found. Symp. 2006, 272:95-99.
56. Rosen D.R., Siddique T., Patterson D., Figlewicz D.A., Sapp P., Hentati A., Donaldson D., Goto J., O'Regan J.P., Deng H.X. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 1993, 362:59-62.
57. Schindler C.V., Karcz-Kubicha M., Thorndike E.B., Müller C.E., Tella S.R., Ferré S., Goldberg S.R. Role of central and peripheral adenosine receptors in the cardiovascular responses to intraperitoneal injections of adenosine A1 and A2A subtype receptor agonists. Br. J. Pharmacol. 2005, 144(5):642-650.
58. Silberstein S.D. Methysergide. Cephalalgia 1998, 18(7):421-435.
59. Sloviter R.S., Drust E.G., Connor J.D. Serotonin agonist actions of p-chlorophenylalanine. Neuropharmacology 1978, 17:1029-1033.
60. Steinman J.L., Carlton S.M., Haber B., Willis W.D. Differential effects of p-chlorophenylalanine on indoleamines in brainstem nuclei and spinal cord of rats. I. Biochemical and behavior analysis. Brain Res. 1987, 426:297-309.
61. Strey K.A., Nichols N.L., Baertsch N.A., Broytman O., Baker-Herman T.L. Spinal atypical protein kinase C activity is necessary to stabilize inactivity-induced phrenic motor facilitation. J. Neurosci. 2012, 32(46):16510-16520.
62. Tankersly C.G., Haenggeli C., Rothstein J.D. Respiratory impairment in a mouse model of amyotrophic lateral sclerosis. J. Appl. Physiol. 2007, 102:926-932.
63. Wang J., Slunt H., Gonzales V., Fromholt D., Coonfield M., Copeland N.G., Jenkins N.A., Borchelt D.R. Copper-binding-site-null SOD1 causes ALS in transgenic mice: aggregates of non-native SOD1 delineate a common feature. Hum. Mol. Genet. 2003, 12(21):2753-2764.
64. Wilkerson J.E., MacFarlane P.M., Hoffman M.S., Mitchell G.S. Respiratory plasticity following intermittent hypoxia: roles of protein phosphatases and reactive oxygen species. Biochem. Soc. Trans. 2007, 35(Pt 5):1269-1272.
65. Wilkerson J.E., Satriotomo I., Baker-Herman T.L., Watters J.J., Mitchell G.S. Okadaic acid-sensitive protein phosphatases constrain phrenic long-term facilitation after sustained hypoxia. J. Neurosci. 2008, 28:2458-2949.
66. Wong P.C., Pardo C.A., Borchelt D.R., Lee M.K., Copeland N.G., Jenkins N.A., Sisodia S.S., Cleveland D.W., Price D.L. An adverse property of a familial ALS-linked SOD1 mutation causes motor neuron disease characterized by vacuolar degeneration of mitochondria. Neuron 1995, 14:1105-1116.
67. Wong P.C., Cai H., Borchelt D.R., Price D.L. Genetically engineered mouse models of neurodegenerative diseases. Nat. Neurosci. 2002, 5:633-639.
68. Wu S.Y., Wang M.Y., Dun N.J. Serotonin via presynaptic 5-HT1 receptors attenuates synaptic transmission to immature rat motoneurones in vitro. Brain Res. 1991, 554:111-121.
69. Zhang Y., McGuire M., White D.P., Ling L. Serotonin receptor subtypes involved in vagus nerve stimulation-induced phrenic long-term facilitation in rats. Neurosci. Lett. 2004, 363(2):108-111.
70. Zifa E., Fillion G. 5-Hydroxytryptamine receptors. Pharmacol. Rev. 1992, 44:401-458.