β- hydroxybutyrate modulates N-type calcium channels in rat sympathetic neurons by acting as an agonist for the G-protein-coupled receptor FFA3

Journal of Neuroscience

Volumn 33, Issue 49, 2013, Pages 19314-19325

  Won, Yu Jin ^a   Lu, Van B ^a   Puhl III, Henry L ^a   Ikeda, Stephen R ^a  

^a NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 HYDROXYBUTYRIC ACID; CALCIUM CHANNEL N TYPE; COMPLEMENTARY DNA; FREE FATTY ACID RECEPTOR 3; G PROTEIN COUPLED RECEPTOR; UNCLASSIFIED DRUG;

ADRENERGIC SYSTEM; ANIMAL CELL; ARTICLE; AUTONOMIC NERVOUS SYSTEM FUNCTION; BIOLUMINESCENCE RESONANCE ENERGY TRANSFER; CONTROLLED STUDY; DIABETIC KETOACIDOSIS; ELECTROPHYSIOLOGY; HUMAN CELL; IN SITU HYBRIDIZATION; KETOGENESIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; NUTRITIONAL STATUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STARVATION; SYMPATHETIC NERVE CELL;

3-HYDROXYBUTYRIC ACID; ANIMALS; CALCIUM CHANNELS, N-TYPE; DNA, COMPLEMENTARY; ELECTROPHYSIOLOGICAL PROCESSES; FLUORESCENCE RESONANCE ENERGY TRANSFER; GANGLIA, SYMPATHETIC; HELA CELLS; HUMANS; IN SITU HYBRIDIZATION; KETONE BODIES; LIGANDS; MALE; NEURONS; RATS; RATS, WISTAR; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, G-PROTEIN-COUPLED; SYMPATHETIC NERVOUS SYSTEM; TRANSFECTION;

EID: 84889078129     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3102-13.2013     Document Type: Article

References (46)

1. Brown AJ, Goldsworthy SM, Barnes AA, Eilert MM, Tcheang L, Daniels D, Muir AI, Wigglesworth MJ, Kinghorn I, Fraser NJ, Pike NB, Strum JC, Steplewski KM, Murdock PR, Holder JC, Marshall FH, Szekeres PG, Wilson S, Ignar DM, Foord SM, et al. (2003) The Orphan G proteincoupled receptors GPR41 and GPR43 are activated by propionate and other short chain carboxylic acids. J Biol Chem 278:11312-11319. CrossRef Medline
2. Brown AJ, Jupe S, Briscoe CP (2005) A family of fatty acid binding receptors. DNA Cell Biol 24:54-61. CrossRef Medline
3. Desch G, Oules R, Mion C, Descomps B, De Paulet AC (1978) Plasma acetate levels during hemodialysis. Clin Chim Acta 85:231-241. CrossRef Medline
4. Elmslie KS, Zhou W, Jones SW (1990) LHRH and GTP-_-S modify calcium current activation in bullfrog sympathetic neurons. Neuron 5:75-80. CrossRef Medline
5. Fulop M, Murthy V, Michilli A, Nalamati J, Qian Q, Saitowitz A (1999) Serum _-hydroxybutyrate measurement in patients with uncontrolled diabetes mellitus. Arch Intern Med 159:381-384. CrossRef Medline
6. Gilbert DL, Pyzik PL, Freeman JM (2000) The ketogenic diet: seizure control correlates better with serum _-hydroxybutyrate than with urine ketones. J Child Neurol 15:787-790. CrossRef Medline
7. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch 391:85-100. CrossRef Medline
8. Hirning LD, Fox AP, McCleskey EW, Olivera BM, Thayer SA, Miller RJ, Tsien RW (1988) Dominant role of N-type Ca2_ channels in evoked release of norepinephrine from sympathetic neurons. Science 239:57-61. CrossRef Medline
9. Hong YH, Nishimura Y, Hishikawa D, Tsuzuki H, Miyahara H, Gotoh C, Choi KC, Feng DD, Chen C, Lee HG, Katoh K, Roh SG, Sasaki S (2005) Acetate and propionate short chain fatty acids stimulate adipogenesis via GPCR43. Endocrinology 146:5092-5099. CrossRef Medline
10. Ikeda SR (1991) Double-pulse calcium channel current facilitation in adult rat sympathetic neurones. J Physiol 439:181-214. Medline
11. Ikeda SR (1996) Voltage-dependent modulation of N-type calcium channels by G-protein __ subunits. Nature 380:255-258. CrossRef Medline
12. Ikeda SR (2004) Expression of G-protein signaling components in adult mammalian neurons by microinjection. Methods Mol Biol 259:167-181. CrossRef Medline
13. Ikeda SR, Dunlap K (1999) Voltage-dependent modulation of N-type calcium channels: role of G protein subunits. Adv Second Messenger Phosphoprotein Res 33:131-151. CrossRef Medline
14. Ikeda SR, Jeong SW (2004) Use of RGS-insensitive G_ subunits to study endogenous RGS protein action on G-protein modulation of N-type calcium channels in sympathetic neurons. Methods Enzymol 389:170-189. CrossRef Medline
15. Ikeda SR, Schofield GG (1989) Somatostatin blocks a calcium current in rat sympathetic ganglion neurones. J Physiol 409:221-240. Medline
16. Jiang LI, Collins J, Davis R, Lin KM, DeCamp D, Roach T, Hsueh R, Rebres RA, Ross EM, Taussig R, Fraser I, Sternweis PC (2007) Use of a cAMP BRET sensor to characterize a novel regulation of cAMP by the sphingosine 1-phosphate/G13 pathway. J Biol Chem 282:10576-10584. CrossRef Medline
17. Karaki S, Tazoe H, Hayashi H, Kashiwabara H, Tooyama K, Suzuki Y, Kuwahara A (2008) Expression of the short-chain fatty acid receptor, GPR43, in the human colon. J Mol Histol 39:135-142. CrossRef Medline
18. Keast JR (1995) Visualization and immunohistochemical characterization of sympathetic and parasympathetic neurons in the male rat major pelvic ganglion. Neuroscience 66:655-662. CrossRef Medline
19. Kebede MA, Alquier T, Latour MG, Poitout V (2009) Lipid receptors and islet function: therapeutic implications? Diabetes Obes Metab 11 [Suppl 4]:10-20.
20. Kimura I, Inoue D, Maeda T, Hara T, Ichimura A, Miyauchi S, Kobayashi M, Hirasawa A, Tsujimoto G (2011) Short-chain fatty acids and ketones directly regulate sympathetic nervous system via G protein-coupled receptor 41 (GPR41). Proc Natl Acad Sci U S A 108:8030-8035. CrossRef Medline
21. Koh DS, Hille B (1997) Modulation by neurotransmitters of catecholamine secretion from sympathetic ganglion neurons detected by amperometry. Proc Natl Acad Sci U S A 94:1506-1511. CrossRef Medline
22. Landsberg L (2006) Feast or famine: the sympathetic nervous system response to nutrient intake. Cell Mol Neurobiol 26:497-508. CrossRef Medline
23. Layden BT, Angueira AR, Brodsky M, Durai V, Lowe WL Jr (2013) Short chain fatty acids and their receptors: new metabolic targets. Transl Res 161:131-140. CrossRef Medline
24. Lee JH, Kim EG, Park BG, Kim KH, Cha SK, Kong ID, Lee JW, Jeong SW (2002) Identification of T-type _1H Ca2_ channels (Ca(v)3.2) in major pelvic ganglion neurons. J Neurophysiol 87:2844-2850. Medline
25. Le Poul E, Loison C, Struyf S, Springael JY, Lannoy V, Decobecq ME, Brezillon S, Dupriez V, Vassart G, Van Damme J, Parmentier M, Detheux M (2003) Functional characterization of human receptors for short chain fatty acids and their role in polymorphonuclear cell activation. J Biol Chem 278:25481-25489. CrossRef Medline
26. Lu VB, Williams DJ, Won YJ, Ikeda SR (2009) Intranuclear microinjection of DNA into dissociated adult mammalian neurons. J Vis Exp 10:e1614. CrossRef Medline
27. Maxwell CR, Spangenberg RJ, Hoek JB, Silberstein SD, Oshinsky ML (2010) Acetate causes alcohol hangover headache in rats. PLoS One 5:e15963. CrossRef Medline
28. Nilsson NE, Kotarsky K, Owman C, Olde B (2003) Identification of a free fatty acid receptor, FFA2R, expressed on leukocytes and activated by short-chain fatty acids. Biochem Biophys Res Commun 303:1047-1052. CrossRef Medline
29. Pluznick JL, Protzko RJ, Gevorgyan H, Peterlin Z, Sipos A, Han J, Brunet I, Wan LX, Rey F, Wang T, Firestein SJ, Yanagisawa M, Gordon JI, Eichmann A, Peti-Peterdi J, Caplan MJ (2013) Olfactory receptor responding to gut microbiota-derived signals plays a role in renin secretion and blood pressure regulation. Proc Natl Acad Sci U S A 110:4410-4415. CrossRef Medline
30. Samuel BS, Shaito A, Motoike T, Rey FE, Backhed F, Manchester JK, Hammer RE, Williams SC, Crowley J, Yanagisawa M, Gordon JI (2008) Effects of the gut microbiota on host adiposity are modulated by the short-chain fatty-acid bindingGprotein-coupled receptor, Gpr41. Proc Natl Acad Sci U S A 105:16767-16772. CrossRef Medline
31. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3:1101-1108. CrossRef Medline
32. Schofield GG, Puhl HL 3rd, Ikeda SR (2008) Properties of wild-type and fluorescent protein-tagged mouse tetrodotoxin-resistant sodium channel (NaV1.8) heterologously expressed in rat sympathetic neurons. J Neurophysiol 99:1917-1927. CrossRef Medline
33. Sellin JH (1999) SCFAs: the enigma of weak electrolyte transport in the colon. News Physiol Sci 14:58-64. Medline
34. Taggart AK, Kero J, Gan X, Cai TQ, Cheng K, Ippolito M, Ren N, Kaplan R, Wu K, Wu TJ, Jin L, Liaw C, Chen R, Richman J, Connolly D, Offermanns S, Wright SD, Waters MG (2005) (D)-beta-Hydroxybutyrate inhibits adipocyte lipolysis via the nicotinic acid receptor PUMA-G. J Biol Chem 280:26649-26652. CrossRef Medline
35. Tazoe H, Otomo Y, Karaki S, Kato I, Fukami Y, Terasaki M, Kuwahara A (2009) Expression of short-chain fatty acid receptor GPR41 in the human colon. Biomed Res 30:149-156. CrossRef Medline
36. Topping DL, Clifton PM (2001) Short-chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides. Physiol Rev 81:1031-1064. Medline
37. Tunaru S, Kero J, Schaub A, Wufka C, Blaukat A, Pfeffer K, Offermanns S (2003) PUMA-G and HM74 are receptors for nicotinic acid and mediate its anti-lipolytic effect. Nat Med 9:352-355. CrossRef Medline
38. Vivaudou M, Chan KW, Sui JL, Jan LY, Reuveny E, Logothetis DE (1997) Probing the G-protein regulation of GIRK1 and GIRK4, the two subunits of the KACh channel, using functional homomeric mutants. J Biol Chem 272:31553-31560. CrossRef Medline
39. Weber M, Pehl U, Breer H, Strotmann J (2002) Olfactory receptor expressed in ganglia of the autonomic nervous system. J Neurosci Res 68:176-184. CrossRef Medline
40. Wise A, Foord SM, Fraser NJ, Barnes AA, Elshourbagy N, Eilert M, Ignar DM, Murdock PR, Steplewski K, Green A, Brown AJ, Dowell SJ, Szekeres PG, Hassall DG, Marshall FH, Wilson S, Pike NB (2003) Molecular identification of high and low affinity receptors for nicotinic acid. J Biol Chem 278:9869-9874. CrossRef Medline
41. Xiong Y, Miyamoto N, Shibata K, Valasek MA, Motoike T, Kedzierski RM, Yanagisawa M (2004) Short-chain fatty acids stimulate leptin production in adipocytes through the G protein-coupled receptor GPR41. Proc Natl Acad Sci U S A 101:1045-1050. CrossRef Medline
42. Young JB, Landsberg L (1977) Suppression of sympathetic nervous system during fasting. Science 196:1473-1475. CrossRef Medline
43. Zaibi MS, Stocker CJ, O'Dowd J, Davies A, Bellahcene M, Cawthorne MA, Brown AJ, Smith DM, Arch JR (2010) Roles of GPR41 and GPR43 in leptin secretory responses of murine adipocytes to short chain fatty acids. FEBS Lett 584:2381-2386. CrossRef Medline
44. Zhu Y, Ikeda SR (1993a) Adenosine modulates voltage-gated Ca2_ channels in adult rat sympathetic neurons. J Neurophysiol 70:610-620. Medline
45. Zhu Y, Ikeda SR (1993b) 2,3-Butanedione monoxime blockade of Ca2_ currents in adult rat sympathetic neurons does not involve "chemical phosphatase" activity. Neurosci Lett 155:24-28. CrossRef Medline
46. Zhu Y, Zboran EL, Ikeda SR (1995) Phenotype-specific expression of T-type calcium channels in neurons of the major pelvic ganglion of the adult male rat. J Physiol 489:363-375. Medline