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Gasotransmitters in Regulation of Neuromuscular Transmission

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Gasotransmitters: Physiology and Pathophysiology

Abstract

Nitric oxide (NO), carbon monoxide (CO), and hydrogen sulfide (H2S) are endogenously synthesized and serve as signaling molecules of autocrine and paracrine regulation in many systems. All three gases are produced in central nervous systems in response to neural excitation and regulate neurotransmitter release and are involved in the regulation of synaptic plasticity acting on pre- or postsynaptic levels. The modulatory mechanisms of these gases are different. In this chapter, we present the literature and our own data concerning the effects and mechanisms of these gases in the peripheral nervous system focusing on neuromuscular synapses. In motor nerve endings it was shown that NO decreased transmitter release while CO had the opposite effect. It was further shown that the main result of NO and CO action is a change of the cyclic adenosine monophosphate (cAMP) level which increased or decreased by cyclic guanosine monophosphate (cGMP) -dependent phosphodiesterases (PDEs) (2 or 3). H2S induced an increase of acetylcholine release and whose effect was mediated by cAMP and Ca2+. It is suggested that all three gases are produced at the neuromuscular junction and regulate transmitter release from motor nerve ending.

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Abbreviations

AC:

Adenylyl cyclase

Ach:

Acetylcholine

AMPA:

Amino-3-hydroxy-5-methyl-4-isoxasolepropionic acid

cAMP:

Cyclic adenosine monophosphate

CAT:

Cysteine aminotransferase

CBS:

Cystathionine β-synthase

cGMP:

Cyclic guanosine monophosphate

CNS:

Central nervous system

CO:

Carbon monoxide

CSE:

Cystathionine γ-lyase

EDRF:

Endothelial-derived relaxing factor

eNOS:

Endothelial-type NOS

EPPs:

Endplate potentials

GABA:

Gamma-amino-biturate acid

HO:

Heme oxygenases

H2S:

Hydrogen sulfide

iNOS:

Inducible-type NOS I

LTD:

Long-term depression

LTP:

Long-term potentiation

3MST:

3-mercaptopyruvate sulfurtransferase

NMDA:

N-methyl-D-aspartate

NMJ:

Neuromuscular junction

nNOS:

Neural-type NOS

NO:

Nitric oxide,

NOS:

NO synthase

PKA:

Protein kinase A

PKC:

Protein kinase C

PDE:

Phosphodiesterase

PKG:

Protein kinase G

sGC:

Soluble guanylyl cyclase

SNAP:

S-nitroso-N-acetylpenicillamine

SNP:

Sodium nitroprusside

References

  • Abe K, Kimura H (1996) The possible role of hydrogen sulfide as an endogenous neuromodulator. J Neurosci 16:1066–1071

    CAS  PubMed  Google Scholar 

  • Abramochkin DV, Haertdinov NN, Porokhnya MV, Zefirov AL, Sitdikova GF (2011) Carbon monoxide affects electrical and contractile activity of rat myocardium. J Biomed Sci 18(1):40. doi:10.1186/1423-0127-18-40

    CAS  PubMed  Google Scholar 

  • Alkadhi KA, Al-Hijailan RS, Malik K, Hogan YH (2001) Retrograde carbon monoxide is required for induction of long-term potentiation in rat superior cervical ganglion. J Neurosci 21(10):3515–3520

    CAS  PubMed  Google Scholar 

  • Ambiel CR, Alves-Do-Prado W (1997) Neuromuscular facilitation and blockade induced by L-arginine and nitric oxide in the rat isolated diaphragm. Gen Pharmacol 28:789–794

    CAS  PubMed  Google Scholar 

  • Ambiel CR, Alves-Do-Prado W (2001) Antagonism by hemoglobin of effects induced by L-arginine in neuromuscular preparations from rats. Braz J Med Biol Res 34:549–552

    CAS  PubMed  Google Scholar 

  • Artinian LR, Ding JM, Gillette MU (2001) Carbon monoxide and nitric oxide: interacting messengers in muscarinic signaling to the brain’s circadian clock. Exp Neurol 171:293–300

    CAS  PubMed  Google Scholar 

  • Baranano DE, Ferris CD, Snyder SH (2001) Atypical neural messengers. Trends Neurosci 24:99–106

    CAS  PubMed  Google Scholar 

  • Barroso A, Oliveira L, Campesatto-Mella E, Silva C, Timóteo MA, Magalhães-Cardoso MT, Alves-do-Prado W, Correia-de-Sá P (2007) L-Citrulline inhibits [3H]acetylcholine release from rat motor nerve terminals by increasing adenosine outflow and activation of A1 receptors. Br J Pharmacol 151:541–550

    CAS  PubMed  Google Scholar 

  • Baum O, Feussner M, Richter H, Gossrau R (2000) Heme oxygenase-2 is present in the sarcolemma region of skeletal muscle fibers and is non-continuously co-localized with nitric oxide synthase-1. Acta Histochem 102:281–298

    CAS  PubMed  Google Scholar 

  • Beaumont V, Zucker RS (2000) Enhancement of synaptic transmission by cyclic AMP modulation of presynaptic Ih channels. Nat Neurosci 3:133–141

    CAS  PubMed  Google Scholar 

  • Beavo JA (1995) Cyclic nucleotide phosphodiesterases: functional implications of multiple isoforms. Physiol Rev 75(4):725–748

    CAS  PubMed  Google Scholar 

  • Bilban M, Haschemi A, Wegiel B, Chin BY, Wagner O, Otterbein LE (2008) Heme oxygenase and carbon monoxide initiate homeostatic signaling. J Mol Med (Berl) 86(3):267–279

    CAS  Google Scholar 

  • Boehning D, Moon C, Sharma S, Hurt KJ, Hester LD, Ronnett GV, Shugar D, Snyder SH (2003) Carbon monoxide neurotransmission activated by CK2 phosphorylation of heme oxygenase-2. Neuron 40:129–137

    CAS  PubMed  Google Scholar 

  • Boehning D, Snyder SH (2003) Novel neural modulators. Annu Rev Neurosci 26:105–131

    CAS  PubMed  Google Scholar 

  • Bredt DS (2003) Nitric oxide signaling specificity—the heart of the problem. J Cell Sci 116(Pt 1):9–15

    CAS  PubMed  Google Scholar 

  • Bredt DS, Snyder SH (1992a) Isolation of nitric oxide synthetase, a calmodulin-requiring enzyme. Proc Natl Acad Sci U S A 87:682–685

    Google Scholar 

  • Bredt DS, Snyder SH (1992b) Nitric oxide, a novel neuronal messenger. Neuron 8:3–11

    CAS  PubMed  Google Scholar 

  • Brenman JE, Chao DS, Xia H, Aldape K, Bredt DS (1995) Nitric oxide synthase complexed with dystrophin and absent from skeletal muscle sarcolemma in Duchenne muscular dystrophy. Cell 82:743–752

    CAS  PubMed  Google Scholar 

  • Bukharaeva EA, Samigullin D, Nikolsky E, Vyskocil F (2002) Protein kinase a cascade regulates quantal release dispersion at frog muscle endplate. J Physiol 538:837–848

    CAS  PubMed  Google Scholar 

  • Burette A, Zabel U, Weinberg R, Schmidt H, Valtschanoff J (2002) Synaptic localization of nitric oxide synthase and soluble guanylyl cyclase in the hippocampus. J Neurosci 22(20):8961–8970

    CAS  PubMed  Google Scholar 

  • Byrne JH, Kandel ER (1996) Presynaptic facilitation revisited: state and time dependence. J Neurosci 16:425–435

    CAS  PubMed  Google Scholar 

  • Calabresi P, Gubellini P, Centonze D, Sancesario G, Morello M, Giorgi M, Pisani A, Bernardi G (1999) A critical role of the nitric oxide/cGMP pathway in corticostriatal long-term depression. J Neurosci 19:2489–2499

    CAS  PubMed  Google Scholar 

  • Capogna M, Gahwiler BH, Thompson SM (1995) Presynaptic enhancement of inhibitory synaptic transmission by protein kinases A and C in the rat hippocampus in vitro. J Neurosci 15:1249–1260

    CAS  PubMed  Google Scholar 

  • Castellano MA, Rojas-Díaz D, Martín F, Quintero M, Alonso J, Navarro E, González-Mora JL (2001) Opposite effects of low and high doses of arginine on glutamate-induced nitric oxide formation in rat substantia nigra. Neurosci Lett 314:127–130

    CAS  PubMed  Google Scholar 

  • Chao DS, Silvagno F, Xia H, Cornwell TL, Lincoln TM, Bredt DS (1997) Nitric oxide synthase and cyclic GMP-dependent protein kinase concentrated at the neuromuscular endplate. Neuroscience 76:665–672

    CAS  PubMed  Google Scholar 

  • Chaudhari K, Wisniewski NH, Bearden SE (2007) Role of sex and eNOS in cystathionine-γ-lyase expression in mouse heart, brain and skeletal muscle. FASEB J 21:577b

    Google Scholar 

  • Chen C, Regehr WG (1997) The mechanism of cAMP-mediated enhancement at a cerebellar synapse. J Neurosci 17:8687–8694

    CAS  PubMed  Google Scholar 

  • Cutajar MC, Edwards TM (2007) Evidence for the role of endogenous carbon monoxide in memory processing. J Cogn Neurosci 19(4):557–562

    CAS  PubMed  Google Scholar 

  • Dawson TM, Dawson VL (1996) Nitric oxide synthase: role as a transmitter/mediator in the brain and endocrine system. Annu Rev Med 47:219–227

    CAS  PubMed  Google Scholar 

  • Dello Russo C, Tringali G, Ragazzoni E, Maggiano N, Menini E, Vairano M, Preziosi P, Navarra P (2000) Evidence that hydrogen sulphide can modulate hypothalamo-pituitary-adrenal axis function: in vitro and in vivo studies in the rat. J Neuroendocrinol 12:225–233

    CAS  PubMed  Google Scholar 

  • Denninger JW, Marletta MA (1999) Guanylate cyclase and the. NO/cGMP signaling pathway. Biochim Biophys Acta 1411(2–3):334–350

    CAS  PubMed  Google Scholar 

  • Descarries LM, Cai S, Robitaille R, Josephson EM, Morest DK (1998) Localization and characterization of nitric oxide synthase at the frog neuromuscular junction. J Neurocytol 27(11):829–840

    CAS  PubMed  Google Scholar 

  • Doeller JE, Isbell TS, Benavides G, Koenitzer J, Patel H, Patel RP, Lancaster JR Jr, Darley-Usmar VM, Kraus DW (2005) Polarographic measurement of hydrogen sulfide production and consumption by mammalian tissues. Anal Biochem 341:40–51

    CAS  PubMed  Google Scholar 

  • Domek-Lopacinska K, Strosznajder JB (2005) Cyclic GMP metabolism and its role in brain physiology. J Physiol Pharmacol 56:15–34

    PubMed  Google Scholar 

  • Dore S, Takahashi M, Ferris CD, Zakhary R, Hester LD, Guastella D, Snyder SH (1999) Bilirubin, formed by activation of heme oxygenase-2, protects neurons against oxidative stress injury. Proc Natl Acad Sci U S A 96(5):2445–2450

    CAS  PubMed  Google Scholar 

  • Dryden WF, Singh YN, Gordon T, Lazarenko G (1988) Pharmacological elevation of cyclic AMP and transmitter release at the mouse neuromuscular junction. Can J Physiol Pharmacol 66(3):207–212

    CAS  PubMed  Google Scholar 

  • Duman JG, Forte JG (2003) What is the role of SNARE proteins in membrane fusion? Am J Physiol Cell Physiol 285:237–249

    Google Scholar 

  • Dwyer BE, Nishimura RN, Lu SY (1995) Differential localization of heme oxygenase and NADPH-diaphorase in spinal cord neurons. NeuroReport 6(7):973–976

    CAS  PubMed  Google Scholar 

  • Eliasson L, Ma X, Renstrom E, Barg S, Berggren PO, Galvanovskis J, Gromada J, Jing X, Lundquist I, Salehi A, Sewing S, Rorsman P (2003) SUR1 regulates PKA-independent cAMP-induced granule priming in mouse pancreatic B-cells. J Gen Physiol 121:181–197

    CAS  PubMed  Google Scholar 

  • Enokido Y, Suzuki E, Iwasawa K, Namekata K, Okazawa H, Kimura H (2005) Cystathionine beta-synthase, a key enzyme for homocysteine metabolism, is preferentially expressed in the radial glia/astrocyte lineage of developing mouse CNS. Faseb J 19:1854–1856

    CAS  PubMed  Google Scholar 

  • Esplugues JV (2002) NO as a signalling molecule in the nervous system. Br J Pharmacol 135:1079–1095

    CAS  PubMed  Google Scholar 

  • Etherington SJ, Everett AW (2004) Postsynaptic production of nitric oxide implicated in long-term depression at the mature amphibian (Bufo marinus) neuromuscular junction. J Physiol 559(2):507–517

    CAS  PubMed  Google Scholar 

  • Eto K, Ogasawara M, Umemura K, Nagai Y, Kimura H (2002) Hydrogen sulfide is produced in response to neuronal excitation. J Neurosci 22:3386–3391

    CAS  PubMed  Google Scholar 

  • Fan W, Dong W, Leng S, Li D, Cheng S, Li C, Qu H, He H (2008) Expression and colocalization of NADPH-diaphorase and heme oxygenase-2 in trigeminal ganglion and mesencephalic trigeminal nucleus of the rat. J Mol Histol 39:427–433

    CAS  PubMed  Google Scholar 

  • Fan W, Huang F, Dong W, Gao Z, Li C, Zhu X, Li D, He H (2009) Distribution of heme oxygenase-2 and NADPH-diaphorase in the spinal trigeminal nucleus of the rat. J Mol Histol 40(3):209–215

    CAS  PubMed  Google Scholar 

  • Fan W, Huang F, Wu Z, Zhu X, Li D, He H (2011) Carbon monoxide: a gas that modulates nociception. J Neurosci Res 89(6):802–807. doi:10.1002/jnr.22613

    CAS  PubMed  Google Scholar 

  • Feil R, Kleppisch T (2008) NO/cGMP-dependent modulation of synaptic transmission. Handb Exp Pharmacol 184:529–560

    CAS  PubMed  Google Scholar 

  • Fernhoff NB, Derbyshire ER, Marletta MA (2009) A nitric oxide/cysteine interaction mediates the activation of soluble guanylate cyclase. Proc Natl Acad Sci U S A 106(51):21602–21607

    CAS  PubMed  Google Scholar 

  • Forstermann U, Schmidt HH, Pollock JS, Sheng H, Mitchell JA, Warner TD, Nakane M, Murad F (1991) Isoforms of nitric oxide synthase. Characterization and purification from different cell types. Biochem Pharmacol 42:1849–1857

    CAS  PubMed  Google Scholar 

  • Förstermann U, Sessa WC (2011) Nitric oxide synthases: regulation and function. Eur Heart J Sep 1. [Epub ahead of print]

    Google Scholar 

  • Gadalla M, Snyder S (2010) Hydrogen sulfide as gasotransmitter. J Neurochem 113:14–26

    CAS  PubMed  Google Scholar 

  • Garcia-Bereguiain MA, Samhan-Arias AK, Martin-Romero FJ, Gutierrez-Merino C (2008) Clustering of plasma membrane-bound cytochrome b5 reductase within ‘lipid raft’ microdomains of the neuronal plasma membrane. Antioxid Redox Signal 10:31–41

    CAS  PubMed  Google Scholar 

  • Garthwaite J (2008) Concepts of neural nitric oxide-mediated transmission. Eur J Neurosci 27:2783–2802

    PubMed  Google Scholar 

  • Garthwaite J, Charles SL, Chess-Williams R (1988) Endothelium-derived relaxing factor release on activation of NMDA receptors suggests role as intercellular messenger in the brain. Nature 336(6197):385–388

    CAS  PubMed  Google Scholar 

  • Gekel I, Neher E (2008) Application of an Epac activator enhances neurotransmitter release at excitatory central synapses. J Neurosci 28(32):7991–8002

    CAS  PubMed  Google Scholar 

  • Gerasimova EV, Sitdikova GF, Zefirov AL (2008) Hydrogen sulfide as an endogenous modulator of mediator release in the frog neuromuscular synapse. Neurochem J 2(1–2):120–126

    Google Scholar 

  • Gibbons SJ, Farrugia G (2004) The role of carbon monoxide in the gastrointestinal tract. J Physiol 556:325–336

    CAS  PubMed  Google Scholar 

  • Goldstein J, Silberstein C, Ibarra C (2002) Adenylyl cyclase types I and VI but not II and V are selectively inhibited by nitric oxide. Braz J Med Biol Res 35(2):145–151

    CAS  PubMed  Google Scholar 

  • Gomes DA, Giusti-Paiva A, Ventura RR, Elias LL, Cunha FQ, Antunes-Rodrigues J (2010) Carbon monoxide and nitric oxide modulate hyperosmolality-induced oxytocin secretion by the hypothalamus in vitro. Biosci Rep 30(5):351–357

    CAS  PubMed  Google Scholar 

  • Graves AR, Lewin KA, A Lindgren C (2004) Nitric oxide, cAMP and the biphasic muscarinic modulation of ACh release at the lizard neuromuscular junction. J Physiol 559(Pt 2):423–432

    CAS  PubMed  Google Scholar 

  • Hanbauer I, Wink D, Osawa Y, Edelman GM, Gally JA (1992) Role of nitric oxide in NMDA-evoked release of [3H]-dopamine from striatal slices. NeuroReport 3(5):409–412

    CAS  PubMed  Google Scholar 

  • Hawkins RD, Zhuo M, Arancio O (1994) Nitric oxide and carbon monoxide as possible retrograde messengers in hippocampal long-term potentiation. J Neurobiol 25:652–665

    CAS  PubMed  Google Scholar 

  • Hawkins RD, Abrams TW, Carew TJ, Kandel ER (1983) A cellular mechanism of classical conditioning in Aplysia: activity-dependent amplification of presynaptic facilitation. Science 219(4583):400–405

    CAS  PubMed  Google Scholar 

  • Herring N, Paterson DJ (2001) Nitric oxide–cGMP pathway facilitates acetylcholine release and bradycardia during vagal nerve stimulation in the guinea-pig in vitro. J Physiol 535:507–518

    CAS  PubMed  Google Scholar 

  • Hill J, Howlett A, Klein C (2000) Nitric oxide selectively inhibits adenylyl cyclase isoforms 5 and 6. Cell Signal 12(4):233–237

    CAS  PubMed  Google Scholar 

  • Hille B (1992) Ionic channels of excitable membranes sunderland. Sinauer, MA

    Google Scholar 

  • Hofmann F, Bernhard D, Lukowski R, Weinmeister P (2009) cGMP regulated protein kinases (cGK). Handb Exp Pharmacol 191:137–162

    CAS  PubMed  Google Scholar 

  • Hopper RA, Garthwaite J (2006) Tonic and phasic nitric oxide signals in hippocampal long-term potentiation. J Neurosci 26:11513–11521

    CAS  PubMed  Google Scholar 

  • Hu LF, Lu M, Hon Wong PT, Bian JS (2011) Hydrogen sulfide: neurophysiology and neuropathology. Antioxid Redox Signal 15(2):405–419

    CAS  PubMed  Google Scholar 

  • Hughes B, Moro De Casillas ML, Kaminski HJ (2004) Pathophysiology of myasthenia gravis. Semin Neurol 24:21–30

    PubMed  Google Scholar 

  • Hung SY, Liou HC, Kang KH, Wu RM, Wen CC, Fu WM (2008) Overexpression of heme oxygenase-1 protects dopaminergic neurons against 1-methyl-4-phenylpyridinium-induced neurotoxicity. Mol Pharmacol 74:1564–1575

    CAS  PubMed  Google Scholar 

  • Ignarro LJ, Buga GM, Wood KS, Byrns RE, Chaudhuri G (1987) Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc Natl Acad Sci U S A 84(24):9265–9269

    CAS  PubMed  Google Scholar 

  • Ikegaya Y, Saito H, Matsuki N (1994) Involvement of carbon monoxide in long-term potentiation in the dentate gyrus of anesthetized rats. Jpn J Pharmacol 64:225–227

    CAS  PubMed  Google Scholar 

  • Ingi T, Cheng J, Ronnett GV (1996) Carbon monoxide: an endogenous modulator of the nitric oxide-cyclic GMP signaling system. Neuron 16:835–842

    CAS  PubMed  Google Scholar 

  • Ishigami M, Hiraki K, Umemura K, Ogasawara Y, Ishii K, Kimura H (2009) A source of hydrogen sulfide and a mechanism of its release in the brain. Antioxid Redox Signal 11:205–214

    CAS  PubMed  Google Scholar 

  • Izumi Y, Zorumski CF (1997) Involvement of nitric oxide in low glucose-mediated inhibition of hippocampal long-term potentiation. Synapse 25:258–262

    CAS  PubMed  Google Scholar 

  • Jaffrey SR, Erdjument-Bromage H, Ferris CD, Tempst P, Snyder SH (2001) Protein S-nitrosylation: a physiological signal for neuronal nitric oxide. Nat Cell Biol 3(2):193–197

    CAS  PubMed  Google Scholar 

  • Jaggar JH, Li A, Parfenova H, Liu J, Umstot ES, Dopico AM, Leffler CW (2005) Heme is a carbon monoxide receptor for large-conductance Ca2+-activated K+ channels. Circ Res 97:805–812

    CAS  PubMed  Google Scholar 

  • Jaggar JH, Leffler CW, Cheranov SY, Tcheranova D, Cheng X (2002) Carbon monoxide dilates cerebral arterioles by enhancing the coupling of Ca2+ sparks to Ca2+-activated K+ channels. Circ Res 91(7):610–617

    CAS  PubMed  Google Scholar 

  • Jin XG, Chen SR, Cao XH, Li L, Pan HL (2011) Nitric oxide inhibits nociceptive transmission by differentially regulating glutamate and glycine release to spinal dorsal horn neurons. J Biol Chem 286(38):33190–33202

    CAS  PubMed  Google Scholar 

  • Johnson FK, Johnson RA (2003) Carbon monoxide promotes endothelium- dependent constriction of isolated gracilis muscle arterioles. Am J Physiol Regul Integr Comp Physiol 285:R536–R541

    PubMed  Google Scholar 

  • Johnson RA, Colombari E, Colombari DS, Lavesa M, Talman WT, Nasjletti A (1997) Role of endogenous carbon monoxide in central regulation of arterial pressure. Hypertension 30:962–967

    CAS  PubMed  Google Scholar 

  • Kaneko M, Takahashi T (2004) Presynaptic mechanism underlying cAMP-dependent synaptic potentiation. J Neurosci 24(22):5202–5208

    CAS  PubMed  Google Scholar 

  • Kaneko S, Akaike A, Satoh M (1998) Differential regulation of N- and Q-type Ca2+ channels by cyclic nucleotides and G-proteins. Life Sci 62(17):1543–1547

    CAS  PubMed  Google Scholar 

  • Kim YM, Pae HO, Park JE, Lee YC, Woo JM, Kim NH, Choi YK, Lee BS, Kim SR, Chung HT (2010) Heme oxygenase in the regulation of vascular biology: from molecular mechanisms to therapeutic opportunities. Antioxid Redox Signal 14(1):137–167

    PubMed  Google Scholar 

  • Kim HP, Ryter SW, Choi AM (2006) CO as a cellular signaling molecule. Annu Rev Pharmacol Toxicol 46:411–449

    CAS  PubMed  Google Scholar 

  • Kimura H (2000) Hydrogen sulfide induces cyclic amp and modulates the nmda receptor. Biochem Biophys Res Commun 267:129–133

    CAS  PubMed  Google Scholar 

  • Kimura H (2010) Hydrogen sulfide: from brain to gut. Antioxid Redox Signal 12:1111–1123

    CAS  PubMed  Google Scholar 

  • Kimura H (2011) Hydrogen sulfide: its production, release and functions. Amino Acids 41(1):113–121

    CAS  PubMed  Google Scholar 

  • Kinobe RT, Dercho RA, Nakatsu K (2008) Inhibitors of the heme oxygenase—carbon monoxide system: on the doorstep of the clinic? Can J Physiol Pharmacol 86(9):577–599

    CAS  PubMed  Google Scholar 

  • Kleppisch T (2009) Phosphodiesterases in the central nervous system. Handb Exp Pharmacol 191:71–92

    CAS  PubMed  Google Scholar 

  • Kleppisch T, Feil R (2009) cGMP signalling in the mammalian brain: role in synaptic plasticity and behaviour. Handb Exp Pharmacol 191:549–579

    CAS  PubMed  Google Scholar 

  • Knecht KR, Milam S, Wilkinson DA, Fedinec AL, Leffler CW (2010) Time-dependent action of carbon monoxide on the newborn cerebrovascular circulation. Am J Physiol Heart Circ Physiol 299:H70–H75

    CAS  PubMed  Google Scholar 

  • Kuromi H, Kidokoro Y (2000) Tetanic stimulation recruits vesicles from reserve pool via a cAMP-mediated process in Drosophila synapses. Neuron 27:133–143

    CAS  PubMed  Google Scholar 

  • Kusner LL, Kaminski HJ (1996) Nitric oxide synthase is concentrated at the skeletal muscle endplate. Brain Res 730(1–2):238–242

    CAS  PubMed  Google Scholar 

  • Kusner L, Kima E, Kaminski HJ (1999) Heme oxygenase-2 expression at rat neuromuscular junctions. Neurosci Lett 273:143–146

    CAS  PubMed  Google Scholar 

  • Lange MD, Doengi M, Lesting J, Pape HC, Jüngling K (2012) Heterosynaptic long-term potentiation at interneuron-principal neuron synapses in the amygdala requires nitric oxide signalling. J Physiol 590(Pt 1):131–143

    CAS  PubMed  Google Scholar 

  • Lee JJ (2009) Nitric oxide modulation of GABAergic synaptic transmission in mechanically isolated rat auditory cortical neurons. Korean J Physiol Pharmacol 13(6):461–467

    CAS  PubMed  Google Scholar 

  • Lee M, Schwab C, Yu S, McGeer E, McGeer PL (2009) Astrocytes produce the antiinflammatory and neuroprotective agent hydrogen sulfide. Neurobiol Aging 30:1523–1534

    CAS  PubMed  Google Scholar 

  • Leffler CW, Parfenova H, Jaggar JH, Wang R (2006) Carbon monoxide and hydrogen sulfide: gaseous messengers in cerebrovascular circulation. J Appl Physiol 100:1065–1076

    CAS  PubMed  Google Scholar 

  • Lev-Ram V, Jiang T, Wood J, Lawrence DS, Tsien RY (1997) Synergies and coincidence requirements between NO, cGMP, and Ca21 in the induction of cerebellar long-term depression. Neuron 18:1025–1038

    CAS  PubMed  Google Scholar 

  • Li A, Xi Q, Umstot ES, Bellner L, Schwartzman ML, Jaggar JH, Leffler CW (2008) Astrocyte-derived CO is a diffusible messenger that mediates glutamate-induced cerebral arteriolar dilation by activating smooth muscle cell KCa channels. Circ Res 102:234–241

    CAS  PubMed  Google Scholar 

  • Li L, Hsu A, Moore PK (2009) Actions and interactions of nitric oxide, carbon monoxide and hydrogen sulphide in the cardiovascular system and in inflammation—a tale of three gases! Pharmacol Ther 123(3):386–400

    CAS  PubMed  Google Scholar 

  • Li Q, Yun JX, He RR (2002) Effect of agmatine on L-type calcium current in rat ventricular myocytes. Acta Pharmacol Sin 23(3):219–224

    CAS  PubMed  Google Scholar 

  • Lim I, Gibbons SJ, Lyford GL, Miller SM, Strege PR, Sarr MG, Chatterjee Szursewski JH, Shah VH, Farrugia G (2005) Carbon monoxide activates human intestinal smooth muscle L-type Ca2+-channels through a nitric oxide-dependent mechanism. Am J Gastrointest Liver Physiol 288:G7–G14

    CAS  Google Scholar 

  • Lin DT, Fretier P, Jiang C, Vincent SR (2010) Nitric oxide signaling via cGMP-stimulated phosphodiesterase in striatal neurons. Synapse 64(6):460–466

    CAS  PubMed  Google Scholar 

  • Linden DR, Sha L, Mazzone A, Stoltz GJ, Bernard CE, Furne JK, Levitt MD, Farrugia G, Szurszewski JH (2008) Production of the gaseous signal molecule hydrogen sulfide in mouse tissues. J Neurochem 106:1577–1585

    CAS  PubMed  Google Scholar 

  • Lindgren C, Laird MV (1994) Nitroprusside inhibits neurotransmitter release at the frog neuromuscular junction. NeuroReport 5:2205–2208

    CAS  PubMed  Google Scholar 

  • Liu H, Mount DB, Nasjletti A, Wang W (1999) Carbon monoxide stimulates the apical 70-pS K+ channel of the rat thick ascending limb. J Clin Invest 103: 963–970

    CAS  PubMed  Google Scholar 

  • Lonart G, Wang J, Johnson KM (1992) Nitric oxide induces neurotransmitter release from hippocampal slices. Eur J Pharmacol 220(2–3):271–272

    CAS  PubMed  Google Scholar 

  • Lu J, Katano T, Okuda-Ashitaka E, Oishi Y, Urade Y, Ito S (2009) Involvement of S-nitrosylation of actin in inhibition of neurotransmitter release by nitric oxide. Molecular Pain 5:58

    PubMed  Google Scholar 

  • Lugnier C (2006) Cyclic nucleotide phosphodiesterase (PDE) superfamily: a new target for the development of specific therapeutic agents. Pharmacol Ther 109:366–398

    CAS  PubMed  Google Scholar 

  • Maines MD (1997) The heme oxygenase system: a regulator of second messenger gases. Ann Rev Pharmacol Toxicol 37:517–554

    CAS  Google Scholar 

  • Maines MD (2004) The heme oxygenase system: past, present, and future. Antioxid Redox Signal 6(5):797–801

    CAS  PubMed  Google Scholar 

  • Maines MD (1993) Carbon monoxide—an emerging regulator of cGMP in the brain. Mol Cell Neurosci 4:389–397

    CAS  PubMed  Google Scholar 

  • Malen PL, Chapman PF (1997) Nitric oxide facilitates long-term potentiation, but not long-term depression. J Neurosci 17:2645–2651

    CAS  PubMed  Google Scholar 

  • Malomouzh AI, Nikolsky EE, Lieberman EM, Sherman JA, Lubischer JL, Grossfeld RM, Urazaev AKh (2005) Effect of N-acetylaspartylglutamate (NAAG) on non-quantal and spontaneous quantal release of acetylcholine at the neuromuscular synapse of rat. J Neurochem 94:257–267

    CAS  PubMed  Google Scholar 

  • Mancuso C (2004) Heme oxygenase and its products in the nervous system. Antiox Redox Signal 6:878–887

    CAS  Google Scholar 

  • McBain C, Kauer J (2009) Presynaptic plasticity: targeted control of inhibitory networks. Curr Opin Neurobiol 19:254–262

    CAS  PubMed  Google Scholar 

  • McCoubrey WK, Maines MD (1993) Domains of rat heme oxygenase-2: the amino terminus and histidine 151 are required for heme oxidation. Arch Biochem Biophys 302(2):402–408

    CAS  PubMed  Google Scholar 

  • McVey M, Hill J, Howlett A, Klein C (1999) Adenylate cyclase a coincidence detector for nitrric oxide. J Biol Chem 274(27):18887–18892

    CAS  PubMed  Google Scholar 

  • Morita T, Perrella MA, Lee ME, Kourembanas S (1995) Smooth muscle cell derived carbon monoxide is a regulator of vascular cGMP. Proc Natl Acad Sci U S A 92:1475–1479

    CAS  PubMed  Google Scholar 

  • Mukhtarov MR, Urazaev AK, Nikolsky EE, Vyskocil F (2000) Effect of nitric oxide and NO synthase inhibition on nonquantal acetylcholine release in the rat diaphragm. Eur J Neurosci 12:980–986

    CAS  PubMed  Google Scholar 

  • Murad F, Mittal CK, Arnold WP, Katsuki S, Kimura H (1978) Guanylate cyclase: activation by azide, nitro compounds, nitric oxide, and hydroxyl radical and inhibition by hemoglobin and yoglobin. Adv Cyclic Nucleotide Res 9:145–158

    CAS  PubMed  Google Scholar 

  • Nagai Y, Tsugane M, Oka J, Kimura H (2004) Hydrogen sulfide induces calcium waves in astrocytes. FASEB J 18:557–559

    CAS  PubMed  Google Scholar 

  • Neitz A, Mergia E, Eysel UT, Koesling D, Mittmann T (2011) Presynaptic nitric oxide/cGMP facilitates glutamate release via hyperpolarization-activated cyclic nucleotide-gated channels in the hippocampus. Eur J Neurosci 33(9):1611–1621. doi:10.1111/j.1460-9568.2011.07654.x

    PubMed  Google Scholar 

  • Nickels TJ, Reed GW, Drummond JT, Blevins DE, Lutz MC, Wilson DF (2007) Does nitric oxide modulate transmitter release at the mammalian neuromuscular junction? Clin Exp Pharmacol Physiol 34(4):318–326

    CAS  PubMed  Google Scholar 

  • Ogasawara Y, Isoda S, Tanabe S (1994) Tissue and subcellular distribution of bound and acid-labile sulfur, and the enzymic capacity for sulfide production in the rat. Biol Pharm Bull 17:1535–1542

    CAS  PubMed  Google Scholar 

  • Olson K (2005) Vascular actions of hydrogen sulfide in nonmammalian vertebrates. Antioxid Redox Signal 7:804–812

    CAS  PubMed  Google Scholar 

  • Ostrom RS, Bundey RA, Insel PA (2004) Nitric oxide inhibition of adenylyl cyclase type 6 activity is dependent upon lipid rafts and caveolin signaling complexes. J Biol Chem 279(19):19846–19853

    CAS  PubMed  Google Scholar 

  • Palmer RM, Ferrige AG, Moncada S (1987) Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 327(6122):524–526

    CAS  PubMed  Google Scholar 

  • Parkes D, Kasckow J, Vale W (1994) Carbon monoxide modulates secretion of corticotropin-releasing factor from rat hypothalamic cell cultures. Brain Res 646:315–318

    CAS  PubMed  Google Scholar 

  • Patacchini R, Santicioli P, Giuliani S, Maggi CA (2004) Hydrogen sulfide (H2S) stimulates capsaicin-sensitive primary afferent neurons in the rat urinary bladder. Br J Pharmacol 142:31–34

    CAS  PubMed  Google Scholar 

  • Patacchini R, Santicioli P, Giuliani S, Maggi CA (2005) Pharmacological investigation of hydrogen sulfide (H2S) contractile activity in rat detrusor muscle. Eur J Pharmacol 509(2–3):171–177

    CAS  PubMed  Google Scholar 

  • Peers C (2011) Ion channels as target effectors for carbon monoxide. Exp Physiol 96(9):836–839

    CAS  PubMed  Google Scholar 

  • Peers C, Dallas ML, Scragg JL (2009) Ion channels as effectors in carbon monoxide signaling. Commun Integr Biol 2(3):241–242

    CAS  PubMed  Google Scholar 

  • Petrov AM, Giniatullin AR, Sitdikova GF, Zefirov AL (2008) The role of cGMP-dependent signaling pathway in synaptic vesicle cycle at the frog motor nerve terminals. J Neurosci 28(49):13216–13222

    CAS  PubMed  Google Scholar 

  • Pinard A, Robitaille R (2008) Nitric oxide dependence of glutamate-mediated modulation at a vertebrate neuromuscular junction. Eur J Neurosci 28(3):577–587

    PubMed  Google Scholar 

  • Prast H, Philippu A (1992) Nitric oxide releases acetylcholine in the basal forebrain. Eur J Pharmacol 216(1):139–140

    CAS  PubMed  Google Scholar 

  • Prast H, Philippu A (2001) Nitric oxide as modulator of neuronal function. Prog Neurobiol 64:51–68

    CAS  PubMed  Google Scholar 

  • Que LG, George SE, Gotoh T, Mori M, Huang Y-CT (2002) Effects of arginase isoforms on NO production by nNOS. Nitric Oxide—Biol Chem 6(1):1–8

    CAS  Google Scholar 

  • Queiroga CS, Almeida AS, Martel C, Brenner C, Alves PM, Vieira HL (2010) Glutathionylation of adenine nucleotide translocase induced by carbon monoxide prevents mitochondrial membrane permeabilization and apoptosis. J Biol Chem 285(22):17077–17088

    CAS  PubMed  Google Scholar 

  • Queiroz RN, Ramos ERP, Alves-Do-Prado W (2003) 4-Aminopyridine and neuromuscular effects of NO and 8-Br-cGMP. Braz J Med Biol Res 2036:937–941

    Google Scholar 

  • Raju VS, McCoubrey WK, Maines MD (1997) Regulation of heme oxygenase-2 by glucocorticoids in neonatal rat brain: characterization of a functional glucocorticoid response element. Biochim Biophys Acta 1351(1–2):89–104

    CAS  PubMed  Google Scholar 

  • Rattan S, Chakder S (1993) Inhibitory effect of CO on internal anal sphincter. Heme oxygenase inhibitor inhibits NANC relaxation. Am J Physiol Gastrointest Liver Physiol 265:G799–G804

    CAS  Google Scholar 

  • Reis DJ, Regunathan S (2000) Is agmatine a novel neurotransmitter in brain? Trends Pharmacol Sci 21(5):187–193

    CAS  PubMed  Google Scholar 

  • Reyes-Harde M, Potter BV, Galione A, Stanton PK (1999) Induction of hippocampal LTD requires nitric-oxide-stimulated PKG activity and Ca2+ release from cyclic ADP-ribose-sensitive stores. J Neurophysiol 82(3):1569–1576

    CAS  PubMed  Google Scholar 

  • Ribera J, Marsal J, Casanovas A, Hukkanen M, Tarabal O, Esquerda JE (1998) Nitric oxide synthase in rat neuromuscular junctions and in nerve terminals of torpedo electric organ: its role as regulator of acetylcholine release. J Neurosci Res 51(1):90–102

    CAS  PubMed  Google Scholar 

  • Rocchitta G, Migheli R, Mura MP, Esposito G, Desole MS, Miele E, Miele M (2004) Signalling pathways in the nitric oxide donor-induced dopamine release in the striatum of freely moving rats: evidence that exogenous nitric oxide promotes Ca2+ entry through store-operated channels. Brain Res 1023(2):243–252

    CAS  PubMed  Google Scholar 

  • Rothe F, Langnaese K, Wolf G (2005) New aspects of the location of neuronal nitric oxide synthase in the skeletal muscle: a light and electron microscopic study. Nitric Oxide 13:21–35

    CAS  PubMed  Google Scholar 

  • Ruehr ML, Russell MA, Ferguson DG, Bhat M, Ma J, Damron DS, Scott JD, Bond M (2003) Targeting of protein kinase a by muscle a kinase-anchoring protein (makap) regulates phosphorylation and function of the skeletal muscle ryanodine receptor. J Biol Chem 278:24831–24836

    CAS  PubMed  Google Scholar 

  • Ryter SW, Alam J, Choi AM (2006) Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol Rev 86:583–650

    CAS  PubMed  Google Scholar 

  • Santafé MM, Garcia N, Lanuza MA, Tomàs M, Tomàs J (2009) Interaction between protein kinase C and protein kinase A can modulate transmitter release at the rat neuromuscular synapse. J Neurosci Res 87(3):683–690

    PubMed  Google Scholar 

  • Schipper HM (2004) Heme oxygenase expression in human central nervous system disorders. Free Radic Biol Med 37(12):1995–2011

    CAS  PubMed  Google Scholar 

  • Schmidt HH, Lohmann SM, Walter U (1993) The nitric oxide and cGMP signal transduction system: regulation and mechanism of action. Biochim Biophys Acta 1178(2):153–175

    CAS  PubMed  Google Scholar 

  • Schwartz A, Whitacre C, Lin Y, Wilson DF (2003) Adenosine inhibits N-type calcium channels at the rat neuromuscular junction. Clin Exp Pharmacol Physiol 30:174–177

    CAS  PubMed  Google Scholar 

  • Scragg JL, Dallas ML, Wilkinson JA, Varadi G, Peers C (2008) Carbon monoxide inhibits L-type Ca2+ channels via redox modulation of key cysteine residues by mitochondrial reactive oxygen species. J Biol Chem 283(36):24412–24419

    CAS  PubMed  Google Scholar 

  • Seino S, Shibasaki T (2005) PKA-Dependent and PKA-Independent Pathways for cAMP-Regulated Exocytosis. Physiol Rev 85:1303–1342

    CAS  PubMed  Google Scholar 

  • Sequeira SM, Ambrósio AF, Malva JO, Carvalho AP, Carvalho CM (1997) Modulation of glutamate release from rat hippocampal synaptosomes by nitric oxide. Nitric Oxide 1(4):315–329

    CAS  PubMed  Google Scholar 

  • Shibuya N, Tanaka M, Yoshida M, Ogasawara Y, Togawa T, Ishii K, Kimura H (2009) 3-Mercaptopyruvate sulfurtransferase produces hydrogen sulfide and bound sulfane sulfur in the brain. Antioxid Redox Signal 11:703–714

    CAS  PubMed  Google Scholar 

  • Shinomura T, Nakao SI, Mori K (1994) Reduction of depolarization-induced glutamate released by heme oxygenase inhibitor: possible role of carbon monoxide in synaptic transmission. Neurosci Lett 166:131–134

    CAS  PubMed  Google Scholar 

  • Silva HMV, Ambiel CR, Alves-do-Prado W (1999) The neuromuscular transmission fade (Wedensky inhibition) induced by l-arginine in neuromuscular preparations from rats. Gen Pharmacol 32:705–712

    CAS  PubMed  Google Scholar 

  • Silvagno F, Xia H, Bredt DS (1996) Neuronal nitric-oxide synthase-mu, an alternatively spliced isoform expressed in differentiated skeletal muscle. J Biol Chem 271(19):11204–11208

    CAS  PubMed  Google Scholar 

  • Sitdikova GF, Yakovlev AV, Zefirov AL, Arkhipova OV (2003) The effects of L- and D-stereoisomers on the transmitter secretion and ionic currents in the motor nerve ending. Dokl Biol Sci 393(1-6):523–526. doi:10.1023/b:dobs.0000010313.65536.1f

    CAS  PubMed  Google Scholar 

  • Sitdikova GF, Gerasimova EV, Khaertdinov NN, Zefirov AL (2009) Role of Cyclic Nucleotides in Effects of Hydrogen Sulfide on the Mediator Release in Frog Neuromuscular Junction. Neurochem J 3(4):282–287

    Google Scholar 

  • Sitdikova GF, Grishin SN, Zefirov AL (2005) Presynaptic effects of carbon monoxide in the myoneural synapse of the frog. Dokl Biol Sci 403:233–236

    CAS  PubMed  Google Scholar 

  • Sitdikova GF, Islamov RR, Mukhamedyarov MA, Permyakova VV, Zefirov AL, Palotás A (2007) Modulation of neurotransmitter release by carbon monoxide at the frog neuro-muscular junction. Curr Drug Metab 8(2):177–184

    CAS  PubMed  Google Scholar 

  • Sitdikova GF, Yakovlev AV, Odnoshivkina YG, Zefirov AL (2011) Effects of hydrogen sulfide on the exo- and endocytosis of synaptic vesicles in frog motor nerve endings. Neurochem J 5(4):245–250

    CAS  Google Scholar 

  • Snyder SH, Bredt DS (1991) Nitric oxide as a neuronal messenger. Trends Pharmacol Sci 12(4):125–128

    CAS  PubMed  Google Scholar 

  • Stamler JS, Meissner G (2001) Physiology of nitric oxide in skeletal muscle. Physiol Rev 81:209–237

    CAS  PubMed  Google Scholar 

  • Stanarius A, Topel I, Schulz S, Noack H, Wolf G (1997) Immunocytochemistry of endothelial nitric oxide synthase in the rat brain: a light and electron microscopical study using the tyramide signal amplification technique. Acta Histochem 99:411–429

    CAS  PubMed  Google Scholar 

  • Steinert JR, Chernova T, Forsythe ID (2010) Nitric oxide signaling in brain function, dysfunction, and dementia. Neuroscientist 16(4):435–452

    CAS  PubMed  Google Scholar 

  • Stevens CF, Wang Y (1993) Reversal of long term potentiation by inhibitors of heme oxygenase. Nature 364:147–149

    CAS  PubMed  Google Scholar 

  • Stone JR, Marletta MA (1994) Soluble guanylate cyclase from bovine lung: activation with nitric oxide and carbon monoxide and spectral characterization of the ferrous and ferric states. Biochemistry 33:5636–5640

    CAS  PubMed  Google Scholar 

  • Swaroop M, Bradley K, Ohura T, Tahara T, Roper MD, Rosenberg LE, Kraus JP (1992) Rat cystathionine beta- synthase. Gene organization and alternative splicing. J Biol Chem 267:11455–11461

    CAS  PubMed  Google Scholar 

  • Szabadits E, Cserép C, Ludányi A, Katona I, Gracia-Llanes J, Freund T, Nyíri G (2007) Hippocampal GABAergic synapses possess the molecular machinery for retrograde nitric oxide signaling. J Neurosci 27:8101–8111

    CAS  PubMed  Google Scholar 

  • Szabadits E, Cserép C, Szonyi A, Fukazawa Y, Shigemoto R, Watanabe M, Itohara S, Freund TF, Nyiri G (2011) NMDA receptors in hippocampal GABAergic synapses and their role in nitric oxide signaling. J Neurosci 31(16):5893–5904

    CAS  PubMed  Google Scholar 

  • Tan BH, Wong PT, Bian JS (2010) Hydrogen sulfide: a novel signaling molecule in the central nervous system. Neurochem Int 56:3–10

    CAS  PubMed  Google Scholar 

  • Thomas S, Robitaille R (2001) Differential frequency-dependent regulation of transmitter release by endogenous nitric oxide at the amphibian neuromuscular synapse. J Neurosci 21:1087–1095

    CAS  PubMed  Google Scholar 

  • Trudeau LE, Emery DG, Haydon PG (1996) Direct modulation of the secretory machinery underlies PKA-dependent synaptic facilitation in hippocampal neurons. Neuron 17(4):789–797

    CAS  PubMed  Google Scholar 

  • Velardez MO, De Laurentiis A, del Carmen Diaz MC, Lasaga M, Pisera D, Seilicovich A, Duvilanski BH (2000) Role of phosphodiesterase and protein kinase G on nitric oxide-induced inhibition of prolactin release from the rat anterior pituitary. Eur J Endocrinol 143:279–284

    CAS  PubMed  Google Scholar 

  • Verma A, Hirsch DJ, Glatt CE, Ronnett GV, Snyder SH (1993) Carbon monoxide: a putative neural messenger. Science 259:381–384

    CAS  PubMed  Google Scholar 

  • Vincent SR (2010) Nitric oxide neurons and neurotransmission. Prog Neurobiol 90(2):246–255

    CAS  PubMed  Google Scholar 

  • Vincent SR, Maines MD (1994) Brain heme oxygenase isoenzymes and nitric oxide synthase are co-localized in select neurons. Neuro Sci 63:223–231

    CAS  Google Scholar 

  • Wang R (2004) Signal transduction and the gasotransmitters. NO, CO and H2S in biology and medicine. Humana Press, Totowa

    Google Scholar 

  • Wang CY, Chau LY (2010) Heme oxygenase-1 in cardiovascular diseases: molecular mechanisms and clinical perspectives. Chang Gung Med J 33(1):13–24

    CAS  PubMed  Google Scholar 

  • Wang R, Wu L (1997) The chemical modification of K(Ca) channels by carbon monoxide in vascular smooth muscle cells. J Biol Chem 272:8222–8226

    CAS  PubMed  Google Scholar 

  • Wang T, Xie Z, Lu B (1995) Nitric oxide mediates activity dependent synaptic suppression at developing neuromuscular synapses. Nature 374:262–266

    CAS  PubMed  Google Scholar 

  • Wei JY, Jin X, Cohen ED, Daw NW, Barnstable CJ (2002) cGMP-induced presynaptic depression and postsynaptic facilitation at glutamatergic synapses in visual cortex. Brain Res 927(1):42–54

    CAS  PubMed  Google Scholar 

  • Williams SE, Wootton P, Mason HS, Bould J, Iles DE, Riccardi D, Peers C, Kemp PJ (2004) Hemoxygenase-2 is an oxygen sensor for a calcium-sensitive potassium channel. Science 306:2093–2097

    CAS  PubMed  Google Scholar 

  • Wood KC, Batchelor AM, Bartus K, Harris KL, Garthwaite G, Vernon J, Garthwaite J (2011) Picomolar nitric oxide signals from central neurons recorded using ultrasensitive detector cells. J Biol Chem 286(50):43172–43181

    CAS  PubMed  Google Scholar 

  • Wu L, Cao K, Lu Y, Wang R (2002) Different mechanisms underlying the stimulation of KCa channels by nitric oxide and carbon monoxide. J Clin Invest 110(5):691–700

    CAS  PubMed  Google Scholar 

  • Wu L, Wang R (2005) Carbon monoxide: endogenous production, physiological functions, and pharmacological applications. Pharmacol Rev 57:585–630

    CAS  PubMed  Google Scholar 

  • Xi Q, Tcheranova D, Parfenova H, Horowitz B, Leffler CW, Jaggar JH (2004) Carbon monoxide activates KCa channels in newborn arteriole smooth muscle cells by increasing apparent Ca2+ sensitivity of alpha-subunits. Am J Physiol Heart Circ Physiol 286:H610–H618

    CAS  PubMed  Google Scholar 

  • Yakovlev AV, Sitdikova GF, Zefirov AL (2002) Role of cyclic nucleotides in mediating the nitric oxide (II) effects on transmitter release and the electrogenesis of motor nerve endings. Dokl Biol Sci 382:11–14

    CAS  PubMed  Google Scholar 

  • Yakovlev AV, Sitdikova GF, Zefirov AL (2005) Intracellular presynaptic mechanisms of nitric oxide (II) action in frog neuromuscular junction. Neirokhimiia 22(1):81–87

    Google Scholar 

  • Yang G, Wu L, Jiang B, Yang W, Qi J, Cao K, Meng Q, Mustafa AK, Mu W, Zhang S, Snyder SH, Wang R (2008) H2S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine gamma-lyase. Science 322:587–590

    CAS  PubMed  Google Scholar 

  • Yao L, Sakaba T (2010) cAMP modulates intracellular Ca2+ sensitivity of fast-releasing synaptic vesicles at the calyx of held synapse. J Neurophysiol 104(6):3250–3260

    CAS  PubMed  Google Scholar 

  • Yoshihara M, Suzuki K, Kidokoro Y (2000) Two independent pathways mediated by cAMP and protein kinase A enhance spontaneous transmitter release at Drosophila neuromuscular junctions. J Neurosci 20(22):8315–8322

    CAS  PubMed  Google Scholar 

  • Zakhary R, Poss KD, Jaffrey SR, Ferris CD, Tonegawa S, Synder SH (1997) Targeted gene deletion of heme oxygenase 2 reveals neural role for carbon monoxide. Proc Natl Acad Sci U S A 94:14848–14853

    CAS  PubMed  Google Scholar 

  • Zefirov AL, Khaliullina RR, Anuchin AA, Yakovlev AV (2002) The effects of exogenous nitric oxide on the function of neuromuscular synapses. Neurosci Behav Physiol 32:583–588

    CAS  PubMed  Google Scholar 

  • Zhong N, Zucker RS (2005) cAMP acts on exchange protein activated by cAMP/cAMP-regulated guanine nucleotide exchange protein to regulate transmitter release at the crayfish neuromuscular junction. J Neurosci 25(1):208–214

    CAS  PubMed  Google Scholar 

  • Zhou L, Zhu DY (2009) Neuronal nitric oxide synthase: structure, subcellular localization, regulation,and clinical implications nitric oxide. Nitric Oxide 20:223–230

    CAS  PubMed  Google Scholar 

  • Zhuo M, Laitinen JT, Li XC, Hawkins RD (1999) On the respective roles of nitric oxide and carbon monoxide in long-term potentiation in the hippocampus. Learn Mem 6(1):63–76

    CAS  PubMed  Google Scholar 

  • Zhuo M, Small SA, Kandel ER, Hawkins RD (1993) Nitric oxide and carbon monoxide produce activity-dependent long-term synaptic enhancement in hippocampus. Science 260:1946–1950

    CAS  PubMed  Google Scholar 

  • Zufall F, Leinders-Zufall T (1997) Identification of a long-lasting form of odor adaptation that depends on the carbon monoxide/cGMP second-messenger system. J Neurosci 17(8):2703–2712

    CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Anton Hermann and Thomas M. Weiger for invaluable help during the preparation of this paper. The study was supported from the Russian Foundation of Basic Research and from the Russian Ministry of Education (grant to Leading Scientific schools of Russian Federation).

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Authors and Affiliations

  1. Department of Human and Animal Physiology, Kazan Federal University, Kremlevskii str., 18, Kazan, Russia

    Guzel F. Sitdikova

  2. Department of Physiology, Kazan Medical University, Butlerova str., 42, Kazan, Russia

    Andrey L. Zefirov

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  1. Guzel F. Sitdikova
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  2. Andrey L. Zefirov
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Correspondence to Guzel F. Sitdikova .

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Editors and Affiliations

  1. , Department of Cell Biology, University of Salzburg, Heilbrunnerstr. 34, Salzburg, 5020, Austria

    Anton Hermann

  2. , Department of Human and Animal Physiolog, Kazan Federal University, ul. Kremlevskaya 18, Kazan, 420008, Russia

    Guzel F. Sitdikova

  3. , Department of Cell Biology, University of Salzburg, Hellbrunnerstr. 34, Salzburg, 5020, Austria

    Thomas M. Weiger

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Sitdikova, G.F., Zefirov, A.L. (2012). Gasotransmitters in Regulation of Neuromuscular Transmission. In: Hermann, A., Sitdikova, G., Weiger, T. (eds) Gasotransmitters: Physiology and Pathophysiology. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-30338-8_5

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