Cyclic ADP-ribose requires CD38 to regulate the release of ATP in visceral smooth muscle

FEBS Journal

Volumn 278, Issue 17, 2011, Pages 3095-3108

  Durnin, Leonie ^a   Mutafova Yambolieva, Violeta N ^a  

^a UNIVERSITY OF NEVADA SCHOOL OF MEDICINE   (United States)

Author keywords

ATP; bladder; cADP ribose; CD38; NAD; purinergic neurotransmission

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CALCIUM ION; CD38 ANTIGEN; CYCLIC ADENOSINE DIPHOSPHATE RIBOSE;

ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CONTROLLED STUDY; CYTOSOL; DETRUSOR MUSCLE; ELECTRIC FIELD; ENZYME RELEASE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MOUSE; NEUROMODULATION; NONHUMAN; PRESYNAPTIC INHIBITION; PRIORITY JOURNAL; SARCOPLASMIC RETICULUM; SECOND MESSENGER; SIGNAL TRANSDUCTION; SMOOTH MUSCLE CONTRACTION; SYNAPTIC TRANSMISSION;

ADENOSINE TRIPHOSPHATE; ANIMALS; ANTIGENS, CD38; CALCIUM-TRANSPORTING ATPASES; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CYCLIC ADP-RIBOSE; ELECTRIC STIMULATION; ENZYME INHIBITORS; GUANINE NUCLEOTIDES; GUANOSINE DIPHOSPHATE SUGARS; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUSCLE CONTRACTION; MUSCLE, SMOOTH; NAD; RECEPTORS, CELL SURFACE; RYANODINE; SPECTROMETRY, FLUORESCENCE; URINARY BLADDER;

MAMMALIA; MUS;

EID: 84860395796     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2011.08233.x     Document Type: Article

References (53)

1. Meszaros LG, Bak J, &, Chu A, (1993) Cyclic ADP-ribose as an endogenous regulator of the non-skeletal type ryanodine receptor Ca2+ channel. Nature 364, 76-79. (Pubitemid 23233460)
2. Lee HC, (2001) Physiological functions of cyclic ADP-ribose and NAADP as calcium messengers. Annu Rev Pharmacol Toxicol 41, 317-345. (Pubitemid 32385891)
3. Higashida H, Salmina AB, Olovyannikova RY, Hashii M, Yokoyama S, Koizumi K, Jin D, Liu HX, Lopatina O, Amina S, et al. (2007) Cyclic ADP-ribose as a universal calcium signal molecule in the nervous system. Neurochem Int 51, 192-199. (Pubitemid 47176716)
4. Graeff RM, Franco L, De Flora A, &, Lee HC, (1998) Cyclic GMP-dependent and -independent effects on the synthesis of the calcium messengers cyclic ADP-ribose and nicotinic acid adenine dinucleotide phosphate. J Biol Chem 273, 118-125. (Pubitemid 28042184)
5. Graeff R, Liu Q, Kriksunov IA, Kotaka M, Oppenheimer N, Hao Q, &, Lee HC, (2009) Mechanism of cyclizing NAD to cyclic ADP-ribose by ADP-ribosyl cyclase and CD38. J Biol Chem 284, 27629-27636.
6. Lee HC, Zocchi E, Guida L, Franco L, Benatti U, &, De Flora A, (1993) Production and hydrolysis of cyclic ADP-ribose at the outer surface of human erythrocytes. Biochem Biophys Res Commun 191, 639-645. (Pubitemid 23222683)
7. Munshi C, Aarhus R, Graeff R, Walseth TF, Levitt D, &, Lee HC, (2000) Identification of the enzymatic active site of CD38 by site-directed mutagenesis. J Biol Chem 275, 21566-21571. (Pubitemid 30481862)
8. Billington RA, Bruzzone S, De Flora A, Genazzani AA, Koch-Nolte F, Ziegler M, &, Zocchi E, (2006) Emerging functions of extracellular pyridine nucleotides. Mol Med 12, 324-327. (Pubitemid 46489827)
9. Franco L, Guida L, Bruzzone S, Zocchi E, Usai C, &, Flora AD, (1998) The transmembrane glycoprotein CD38 is a catalytically active transporter responsible for generation and influx of the second messenger cyclic ADP-ribose across membranes. FASEB J 12, 1507-1520. (Pubitemid 28506720)
10. De Flora A, Zocchi E, Guidal L, Franco L, &, Bruzzone S, (2004) Autocrine and paracrine calcium signaling by the CD38/NAD+/cyclic ADP-ribose system. Ann NY Acad Sci 1028, 176-191. (Pubitemid 40372088)
11. Amina S, Hashii M, Ma WJ, Yokoyama S, Lopatina O, Liu HX, Islam MS, &, Higashida H, (2010) Intracellular calcium elevation induced by extracellular application of cyclic-ADP-ribose or oxytocin is temperature-sensitive in rodent NG108-15 neuronal cells with or without exogenous expression of human oxytocin receptors. J Neuroendocrinol 22, 460-466.
12. Smyth LM, Bobalova J, Mendoza MG, Lew C, &, Mutafova-Yambolieva VN, (2004) Release of {beta}-nicotinamide adenine dinucleotide upon stimulation of postganglionic nerve terminals in blood vessels and urinary bladder. J Biol Chem 279, 48893-48903. (Pubitemid 39625770)
13. Breen LT, Smyth LM, Yamboliev IA, &, Mutafova-Yambolieva VN, (2006) {beta}-NAD is a novel nucleotide released on stimulation of nerve terminals in human urinary bladder detrusor muscle. Am J Physiol Renal Physiol 290, F486-F495. (Pubitemid 43725002)
14. Smyth LM, Breen LT, &, Mutafova-Yambolieva VN, (2006) Nicotinamide adenine dinucleotide (NAD) is released from sympathetic nerve terminals via a botulinum neurotoxin A mediated mechanism in canine mesenteric artery. Am J Physiol Heart Circ Physiol 290, H1818-H1825.
15. Mutafova-Yambolieva VN, Hwang SJ, Hao X, Chen H, Zhu MX, Wood JD, Ward SM, &, Sanders KM, (2007) beta-Nicotinamide adenine dinucleotide is an inhibitory neurotransmitter in visceral smooth muscle. Proc Natl Acad Sci USA 104, 16359-16364. (Pubitemid 350099409)
16. Hwang SJ, Durnin L, Dwyer L, Rhee PL, Ward SM, Koh SD, Sanders KM, &, Mutafova-Yambolieva VN, (2011) beta-Nicotinamide adenine dinucleotide is an enteric inhibitory neurotransmitter in human and nonhuman primate colons. Gastroenterology 140, 608-617.
17. Andersson KE, &, Wein AJ, (2004) Pharmacology of the lower urinary tract: basis for current and future treatments of urinary incontinence. Pharmacol Rev 56, 581-631. (Pubitemid 40003785)
18. Burnstock G, (2009) Purinergic cotransmission. Exp Physiol 94, 20-24.
19. Evans WH, De VE, &, Leybaert L, (2006) The gap junction cellular internet: connexin hemichannels enter the signalling limelight. Biochem J 397, 1-14. (Pubitemid 44032830)
20. Stout CE, Costantin JL, Naus CC, &, Charles AC, (2002) Intercellular calcium signaling in astrocytes via ATP release through connexin hemichannels. J Biol Chem 277, 10482-10488. (Pubitemid 34968170)
21. Cotrina ML, Lin JH, Alves-Rodrigues A, Liu S, Li J, Azmi-Ghadimi H, Kang J, Naus CC, &, Nedergaard M, (1998) Connexins regulate calcium signaling by controlling ATP release. Proc Natl Acad Sci USA 95, 15735-15740. (Pubitemid 29018769)
22. Dahl G, &, Locovei S, (2006) Pannexin: to gap or not to gap, is that a question? IUBMB Life 58, 409-419. (Pubitemid 43995626)
23. Srinivas M, &, Spray DC, (2003) Closure of gap junction channels by arylaminobenzoates. Mol Pharmacol 63, 1389-1397. (Pubitemid 36627235)
24. Zimmermann H, (1996) Biochemistry, localization and functional roles of ecto-nucleotidases in the nervous system. Prog Neurobiol 49, 589-618. (Pubitemid 26343246)
25. Bollen M, Gijsbers R, Ceulemans H, Stalmans W, &, Stefan C, (2000) Nucleotide pyrophosphatases/phosphodiesterases on the move. Crit Rev Biochem Mol Biol 35, 393-432. (Pubitemid 32095990)
26. Zimmermann H, (2000) Extracellular metabolism of ATP and other nucleotides. Naunyn Schmiedebergs Arch Pharmacol 362, 299-309.
27. Yegutkin GG, (2008) Nucleotide- and nucleoside-converting ectoenzymes: important modulators of purinergic signalling cascade. Biochim Biophys Acta 1783, 673-694.
28. Yue J, Wei W, Lam CM, Zhao YJ, Dong M, Zhang LR, Zhang LH, &, Lee HC, (2009) CD38/cADPR/Ca2+ pathway promotes cell proliferation and delays nerve growth factor-induced differentiation in PC12 cells. J Biol Chem 284, 29335-29342.
29. de Groat WC, &, Yoshimura N, (2001) Pharmacology of the lower urinary tract. Annu Rev Pharmacol Toxicol 41, 691-721. (Pubitemid 32385903)
30. Gershon MD, (2005) Nerves, reflexes, and the enteric nervous system: pathogenesis of the irritable bowel syndrome. J Clin Gastroenterol 39, S184-S193. (Pubitemid 44638345)
31. Lecci A, Capriati A, Altamura M, &, Maggi CA, (2006) Tachykinins and tachykinin receptors in the gut, with special reference to NK2 receptors in human. Auton Neurosci 126-127, 232-249. (Pubitemid 43833351)
32. Burnstock G, (2008) The journey to establish purinergic signalling in the gut. Neurogastroenterol Motil 20 (Suppl 1), 8-19. (Pubitemid 351514536)
33. Starke K, von Kugelgen I, &, Bultmann R, (1992) Noradrenaline-ATP cotransmission: operation in blood vessels and cotransmitter release ratios. Jpn J Pharmacol 58 (Suppl 2), 166P-173P.
34. Yamboliev IA, Smyth LM, Durnin L, Dai Y, &, Mutafova-Yambolieva VN, (2009) Storage and secretion of beta-NAD, ATP and dopamine in NGF-differentiated rat pheochromocytoma PC12 cells. Eur J Neurosci 30, 756-768.
35. da Silva CP, Schweitzer K, Heyer P, Malavasi F, Mayr GW, &, Guse AH, (1998) Ectocellular CD38-catalyzed synthesis and intracellular Ca2+-signalling activity of cyclic ADP-ribose in T-lymphocytes are not functionally related. FEBS Lett 439, 291-296. (Pubitemid 28546662)
36. Catterall WA, &, Few AP, (2008) Calcium channel regulation and presynaptic plasticity. Neuron 59, 882-901.
37. Bouron A, (2001) Modulation of spontaneous quantal release of neurotransmitters in the hippocampus. Prog Neurobiol 63, 613-635. (Pubitemid 32119420)
38. Corriden R, &, Insel PA, (2010) Basal release of ATP: an autocrine-paracrine mechanism for cell regulation. Sci Signal 3, re1.
39. Kang J, Kang N, Lovatt D, Torres A, Zhao Z, Lin J, &, Nedergaard M, (2008) Connexin 43 hemichannels are permeable to ATP. J Neurosci 28, 4702-4711.
40. Huang YJ, Maruyama Y, Dvoryanchikov G, Pereira E, Chaudhari N, &, Roper SD, (2007) The role of pannexin 1 hemichannels in ATP release and cell-cell communication in mouse taste buds. Proc Natl Acad Sci USA 104, 6436-6441. (Pubitemid 47186112)
41. Bell PD, Lapointe JY, Sabirov R, Hayashi S, Peti-Peterdi J, Manabe K, Kovacs G, &, Okada Y, (2003) Macula densa cell signaling involves ATP release through a maxi anion channel. Proc Natl Acad Sci USA 100, 4322-4327. (Pubitemid 36418201)
42. Hisadome K, Koyama T, Kimura C, Droogmans G, Ito Y, &, Oike M, (2002) Volume-regulated anion channels serve as an auto/paracrine nucleotide release pathway in aortic endothelial cells. J Gen Physiol 119, 511-520. (Pubitemid 34615096)
43. Suadicani SO, Brosnan CF, &, Scemes E, (2006) P2X7 receptors mediate ATP release and amplification of astrocytic intercellular Ca2+ signaling. J Neurosci 26, 1378-1385. (Pubitemid 43237008)
44. Cantiello HF, (2001) Electrodiffusional ATP movement through CFTR and other ABC transporters. Pflugers Arch 443 (Suppl 1), S22-S27.
45. Gatof D, Kilic G, &, Fitz JG, (2004) Vesicular exocytosis contributes to volume-sensitive ATP release in biliary cells. Am J Physiol Gastrointest Liver Physiol 286, G538-G546. (Pubitemid 38374972)
46. Lund FE, Moutin MJ, Muller-Steffner H, &, Schuber F, (2005) ADP-ribosyl cyclase and GDP-ribosyl cyclase activities are not always equivalent: impact on the study of the physiological role of cyclic ADP-ribose. Anal Biochem 346, 336-338. (Pubitemid 41550267)
47. Glitsch MD, (2008) Spontaneous neurotransmitter release and Ca2+-how spontaneous is spontaneous neurotransmitter release? Cell Calcium 43, 9-15.
48. Walseth TF, &, Lee HC, (1993) Synthesis and characterization of antagonists of cyclic-ADP-ribose-induced Ca2+ release. Biochim Biophys Acta 1178, 235-242. (Pubitemid 23276215)
49. Meissner G, (1986) Ryanodine activation and inhibition of the Ca2+ release channel of sarcoplasmic reticulum. J Biol Chem 261, 6300-6306. (Pubitemid 17204136)
50. Birder LA, Kanai AJ, Cruz F, Moore K, &, Fry CH, (2010) Is the urothelium intelligent? Neurourol Urodyn 29, 598-602.
51. Smyth LM, Breen LT, Yamboliev IA, &, Mutafova-Yambolieva VN, (2006) Novel localization of CD38 in perivascular sympathetic nerve terminals. Neuroscience 139, 1467-1477. (Pubitemid 44308115)
52. Levitt B, Head RJ, &, Westfall DP, (1984) High-pressure liquid chromatographic-fluorometric detection of adenosine and adenine nucleotides: application to endogenous content and electrically induced release of adenyl purines in guinea pig vas deferens. Anal Biochem 137, 93-100. (Pubitemid 14165431)
53. Bobalova J, Bobal P, &, Mutafova-Yambolieva VN, (2002) High-performance liquid chromatographic technique for detection of a fluorescent analogue of ADP-ribose in isolated blood vessel preparations. Anal Biochem 305, 269-276. (Pubitemid 34666800)