Ion channel regulation by the LKB1-AMPK signalling pathway: The key to carotid body activation by hypoxia and metabolic homeostasis at the whole body level

Advances in Experimental Medicine and Biology

Volumn 758, Issue , 2012, Pages 81-90

  Evans, A Mark ^a   Peers, Chris ^b   Wyatt, Christopher N ^c   Kumar, Prem ^d   Hardie, D Grahame ^e  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF LEEDS   (United Kingdom)

^c WRIGHT STATE UNIVERSITY   (United States)

^d UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^e UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

Afferent discharge; AMPK; Carotid body; Hypoxia; LKB1; TASK; Ventilation

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; POTASSIUM CHANNEL; PROTEIN KINASE LKB1;

CAROTID BODY; CELL ACTIVATION; CONFERENCE PAPER; DOWN REGULATION; ENZYME ACTIVATION; EVOKED RESPONSE; HUMAN; HYPOXIA; METABOLIC REGULATION; MITOCHONDRION; NERVE FUNCTION; NONHUMAN; OXYGEN AFFINITY; OXYGEN SENSING; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SENSORY NERVE CONDUCTION; SIGNAL TRANSDUCTION; UPREGULATION;

EID: 84870446015     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-94-007-4584-1_11     Document Type: Conference Paper

References (53)

1. Biscoe TJ, Pallot DJ (1982) The carotid body chemoreceptor: An investigation in the mouse. Q J Exp Physiol 67(4):557-576 (Cambridge, England
2. Brown GC (1992) Control of respiration and ATP synthesis in mammalian mitochondria and cells. Biochem J 284(Pt 1):1-13
3. Buckler KJ (1997) A novel oxygen-sensitive potassium current in rat carotid body type I cells. J Physiol (Pt 3):649-662
4. Buckler KJ (2007) TASK-like potassium channels and oxygen sensing in the carotid body. Respir Physiol Neurobiol 157(1):55-64
5. Buttigieg J, Brown ST, Lowe M, Zhang M, Nurse CA (2008) Functional mitochondria are required for O2 but not CO2 sensing in immortalized adrenomedullary chromaf fi n cells. Am J Physiol Cell Physiol 294(4):C945-956
6. Chandel NS (2010) Mitochondrial complex III: An essential component of universal oxygen sensing machinery? Respir Physiol Neurobiol 174(3):175-181
7. Cooper CE, Brown GC (2008) The inhibition of mitochondrial cytochrome oxidase by the gases carbon monoxide, nitric oxide, hydrogen cyanide and hydrogen sul fi de: Chemical mechanism and physiological significance. J Bioenerg Biomembr 40(5):533-539
8. De Castro F (1928) Sur la structure et l'innervation du sinus carotidien de l'homme et des mammiferes: Nouveau faits sur l'innervation et la fonction du glomus caroticum. Trab Lab Invest Biol Univ Madrid 24:330-380
9. Delpiano MA, Hescheler J (1989) Evidence for a PO2-sensitive K + channel in the type-I cell of the rabbit carotid body. FEBS Lett 249(2):195-198
10. Dipp M, Evans AM (2001) Cyclic ADP-ribose is the primary trigger for hypoxic pulmonary vasoconstriction in the rat lung in situ. Circ Res 89(1):77-83
11. Duchen MR, Biscoe TJ (1992a) Relative mitochondrial membrane potential and [Ca2+]i in type I cells isolated from the rabbit carotid body. J Physiol 450:33-61
12. Duchen MR, Biscoe TJ (1992b) Mitochondrial function in type I cells isolated from rabbit arterial chemoreceptors. J Physiol 450:13-31
13. Evans AM (2006) AMP-activated protein kinase and the regulation of Ca2+ signalling in O2-sensing cells. J Physiol (Pt 1):113-123
14. Evans AM, Mustard KJ, Wyatt CN, Peers C, Dipp M, Kumar P, Kinnear NP, Hardie DG (2005) Does AMP-activated protein kinase couple inhibition of mitochondrial oxidative phosphorylation by hypoxia to calcium signaling in O2-sensing cells? J Biol Chem 280(50):41504-41511
15. Evans AM, Hardie DG, Peers C, Wyatt CN, Viollet B, Kumar P, Dallas ML, Ross F, Ikematsu N, Jordan HL, Barr BL, Rafferty JN, Ogunbayo O (2009) Ion channel regulation by AMPK: The route of hypoxia-response coupling in the carotid body and pulmonary artery. Ann N Y Acad Sci 1177:89-100
16. Evans AM, Hardie DG, Peers C, Mahmoud A (2011) Hypoxic pulmonary vasoconstriction: Mechanisms of oxygensensing. Curr Opin Anaesthesiol 24(1):13-20
17. Eyzaguirre C, Koyano H (1965a) Effects of hypoxia, hypercapnia, and pH on the chemoreceptor activity of the carotid body in vitro. J Physiol 178(3):385-409
18. Eyzaguirre C, Koyano H (1965b) Effects of some pharmacological agents on chemoreceptor discharges. J Physiol 178(3):410-437
19. Gadalla AE, Pearson T, Currie AJ, Dale N, Hawley SA, Sheehan M, Hirst W, Michel AD, Randall A, Hardie DG, Frenguelli BG (2004) AICA riboside both activates AMP-activated protein kinase and competes with adenosine for the nucleoside transporter in the CA1 region of the rat hippocampus. J Neurochem 88(5):1272-1282
20. Gnaiger E, Lassnig B, Kuznetsov A, Rieger G, Margreiter R (1998) Mitochondrial oxygen af fi nity, respiratory fl ux control and excess capacity of cytochrome c oxidase. J Exp Biol 201(Pt 8):1129-1139
21. Gonzalez C, Almaraz L, Obeso A, Rigual R (1994) Carotid body chemoreceptors: From natural stimuli to sensory discharges. Physiol Rev 74(4):829-898
22. Gonzalez C, Vicario I, Almaraz L, Rigual R (1995a) Oxygen sensing in the carotid body. Biol Signal 4(5):245-256
23. Gonzalez C, Lopez-Lopez JR, Obeso A, Perez-Garcia MT, Rocher A (1995b) Cellular mechanisms of oxygen chemoreception in the carotid body. Respir Physiol 102(2-3):137-147
24. Hardie DG (2007) AMP-activated/SNF1 protein kinases: Conserved guardians of cellular energy. Nat Rev (10):774-785
25. Hardie DG, Carling D, Gamblin SJ (2011) AMP-activated protein kinase: Also regulated by ADP? Trends Biochem Sci 29:18-24
26. Hatton CJ, Carpenter E, Pepper DR, Kumar P, Peers C (1997) Developmental changes in isolated rat type I carotid body cell K + currents and their modulation by hypoxia. J Physiol 501(Pt 1):49-58
27. Hescheler J, Delpiano MA, Acker H, Pietruschka F (1989) Ionic currents on type-I cells of the rabbit carotid body measured by voltage-clamp experiments and the effect of hypoxia. Brain Res 486(1):79-88
28. Heymans C, Bouckaert JJ, Dautrebande L (1930) Sinus carotidien et re fl exes respiratoires. II. Influences respiratoires re fl exes de l'acidose, de l'alcalose, de l'anhydride carbonique, de l'ion hydrogene et de l'anoxemie: Sinus carotidiens et echanges respiratoires dans les poumons et au dela poumons. Arch Int Pharmacodyn Ther 39(2)):400-408
29. Hill AA, Garcia AJ 3rd, Zanella S, Upadhyaya R, Ramirez JM (2011) Graded reductions in oxygenation evoke graded recon fi guration of the isolated respiratory network. J Neurophysiol 105(2):625-639
30. Ikematsu N, Dallas ML, Ross FA, Lewis RW, Rafferty JN, David JA, Suman R, Peers C, Hardie DG, Evans AM (2011 Phosphorylation of the voltage-gated potassium channel Kv2.1 by AMP-activated protein kinase regulates membrane excitability. Proc Natl Acad Sci U S A 44:18132-18137
31. Iturriaga R, Alcayaga J (2004) Neurotransmission in the carotid body: Transmitters and modulators between glomus cells and petrosal ganglion nerve terminals. Brain Res Rev 47(1-3):46-53
32. Jones DP (1986) Intracellular diffusion gradients of O2 and ATP. Am J Physiol 250(5 Pt 1):C663-675
33. Kim D, Cavanaugh EJ, Kim I, Carroll JL (2009) Heteromeric TASK-1/TASK-3 is the major oxygen-sensitive background K + channel in rat carotid body glomus cells. J Physiol 587(Pt 12):2963-2975
34. Kumar P, Prabhakar N (2007) Sensing hypoxia: Carotid body mechanisms and re fl exes in health and disease. Respir Physiol Neurobiol 157(1):1-3
35. Lopez-Barneo J, Lopez-Lopez JR, Urena J, Gonzalez C (1988) Chemotransduction in the carotid body: K+ current modulated by PO2 in type I chemoreceptor cells. Science 241(4865):580-582
36. New York, NY Lopez-Lopez JR, De Luis DA, Gonzalez C (1993) Properties of a transient K+ current in chemoreceptor cells of rabbit carotid body. J Physiol 460:15-32
37. Mills E, Jobsis FF (1972) Mitochondrial respiratory chain of carotid body and chemoreceptor response to changes in oxygen tension. J Neurophysiol 35(4):405-428
38. Nurse CA (2010) Neurotransmitter and neuromodulatory mechanisms at peripheral arterial chemoreceptors. Exp Physiol 95(6):657-667
39. Ortega-Saenz P, Levitsky KL, Marcos-Almaraz MT, Bonilla-Henao V, Pascual A, Lopez-Barneo J (2010) Carotid body chemosensory responses in mice de fi cient of TASK channels. J Gen Physiol 135(4):379-392
40. Peers C (1990) Hypoxic suppression of K+ currents in type I carotid body cells: Selective effect on the Ca2(+)-activated K+ current. Neurosci Lett 119(2):253-256
41. Peers C, Wyatt CN, Evans AM (2010) Mechanisms for acute oxygen sensing in the carotid body. Respir Physiol Neurobiol 174(3):292-298
42. Peng YJ, Nanduri J, Raghuraman G, Souvannakitti D, Gadalla MM, Kumar GK, Snyder SH, Prabhakar NR (2010) H2S mediates O2 sensing in the carotid body. Proc Natl Acad Sci U S A 107(23):10719-10724
43. Perez-Garcia MT, Colinas O, Miguel-Velado E, Moreno-Dominguez A, Lopez-Lopez JR (2004) Characterization of the Kv channels of mouse carotid body chemoreceptor cells and their role in oxygen sensing. J Physiol (Pt 2):457-471
44. Ross FA, Rafferty JN, Dallas ML, Ogunbayo O, Ikematsu N, McClafferty H, Tian L, Widmer H, Rowe IC, Wyatt CN, Shipston MJ, Peers C, Hardie DG, Evans AM (2011) Selective expression in carotid body type I cells of a single splice variant of the large conductance calcium- and voltage-activated potassium channel confers regulation by AMP-activated protein kinase. J Biol Chem 286(14):11929-11936
45. Stea A, Nurse CA (1991) Whole-cell and perforated-patch recordings from O2-sensitive rat carotid body cells grown in short- and long-term culture. P fl ugers Archiv 418(1-2):93-101
46. Tamas P, Hawley SA, Clarke RG, Mustard KJ, Green K, Hardie DG, Cantrell DA (2006) Regulation of the energy sensor AMP-activated protein kinase by antigen receptor and Ca2+ in T lymphocytes. J Exp Med 203(7):1665-1670
47. Thompson RJ, Jackson A, Nurse CA (1997) Developmental loss of hypoxic chemosensitivity in rat adrenomedullary chromaf fi n cells. J Physiol 498(Pt 2):503-510
48. Verna A, Roumy M, Leitner LM (1975) Loss of chemoreceptive properties of the rabbit carotid body after destruction of the glomus cells. Brain Res 100(1):13-23
49. Wasicko MJ, Breitwieser GE, Kim I, Carroll JL (2006) Postnatal development of carotid body glomus cell response to hypoxia. Respir Physiol Neurobiol 154(3):356-371
50. Wyatt CN, Evans AM (2007) AMP-activated protein kinase and chemotransduction in the carotid body. Respir Physiol Neurobiol 157(1):22-29
51. Wyatt CN, Mustard KJ, Pearson SA, Dallas ML, Atkinson L, Kumar P, Peers C, Hardie DG, Evans AM (2007) AMPactivated protein kinase mediates carotid body excitation by hypoxia. J Biol Chem 282(11):8092-8098
52. Xiao B, Sanders MJ, Underwood E, Heath R, Mayer FV, Carmena D, Jing C, Walker PA, Eccleston JF, Haire LF, Saiu P, Howell SA, Aasland R, Martin SR, Carling D, Gamblin SJ (2011) Structure of mammalian AMPK and its regulation by ADP. Nature 472(7342):230-233
53. Zhang M, Zhong H, Vollmer C, Nurse CA (2000) Co-release of ATP and ACh mediates hypoxic signalling at rat carotid body chemoreceptors. J Physiol 525(Pt 1):143-158