DOI: 10.1146/annurev.pharmtox.41.1.317. Physiological Functions of Cyclic ADP-Ribose and NAADP as Calcium Messengers

Physiological Functions of Cyclic ADP-Ribose and NAADP as Calcium Messengers

10.1146/annurev.pharmtox.41.1.317

Crossref journal-article

Annual Reviews

Annual Review of Pharmacology and Toxicology (22)

Abstract

Cyclic ADP-ribose (cADPR) and nicotinic acid adenine dinucleotide phosphate (NAADP) are two Ca2+messengers derived from NAD and NADP, respectively. Although NAADP is a linear molecule, structurally distinct from the cyclic cADPR, it is synthesized by similar enzymes, ADP-ribosyl cyclase and its homolog, CD38. The crystal structure of the cyclase has been solved and its active site identified. These two novel nucleotides have now been shown to be involved in a wide range of cellular functions including: cell cycle regulation in Euglena, a protist; gene expression in plants; and in animal systems, from fertilization to neurotransmitter release and long-term depression in brain. A battery of pharmacological reagents have been developed, providing valuable tools for elucidating the physiological functions of these two novel Ca2+messengers. This article reviews these recent results and explores the implications of the existence of multiple Ca2+messengers and Ca2+stores in cells.

Bibliography

Lee, H. C. (2001). Physiological Functions of Cyclic ADP-Ribose and NAADP as Calcium Messengers. Annual Review of Pharmacology and Toxicology, 41(1), 317â345.

Authors 1

Hon Cheung Lee (first)

References 178 Referenced 310

10.1016/S0021-9258(18)47970-7 / J. Biol. Chem. by Clapper DL (1987)
10.1016/S0021-9258(18)94230-4 / J. Biol. Chem. by Lee HC (1989)
10.1038/nsb0394-143
10.1074/jbc.270.5.2152
10.1152/physrev.1997.77.4.1133
10.1007/s002320001001
10.1074/jbc.270.51.30327
10.1074/jbc.274.43.30770
10.1074/jbc.M909365199
10.1152/ajpcell.1998.274.2.C430
10.1111/j.1469-7793.1998.155bz.x
10.1016/S0014-5793(97)00168-3
10.1126/science.278.5346.2126
10.1038/18024
10.1016/S0021-9258(18)80125-9 / J. Biol. Chem. by Rusinko N (1989)
10.1016/0167-4838(93)90113-6
10.1016/S0083-6729(08)60499-9
10.1007/BF00928466
10.1091/mbc.2.3.203
10.4049/jimmunol.144.7.2811 / J. Immunol. by Jackson DG (1990)
10.1016/0968-0004(92)90337-9
10.1006/bbrc.1994.2325
10.1126/science.8395705
10.1006/bbrc.1993.1265
10.1126/science.8235624
10.1016/S0021-9258(19)74275-6 / J. Biol. Chem. by Takasawa S (1993)
10.1016/S0006-8993(98)01347-X
{'key': 'b28', 'first-page': '81', 'volume': '12', 'author': 'Fernandez JE', 'year': '1998', 'journal-title': 'J. Biol. Regul. Homeostatic Agents'} / J. Biol. Regul. Homeostatic Agents by Fernandez JE (1998)
10.1023/A:1006916311348
10.1515/BC.1999.098
10.1159/000058774
10.1016/0006-8993(95)00885-T
10.1038/15640
10.1006/abbi.1999.1526
10.1074/jbc.M908231199
10.1006/bbrc.1998.9752
10.1093/oxfordjournals.jbchem.a022307
10.1016/S0167-4838(98)00204-0
10.1038/nsb1196-957
10.1002/(SICI)1097-0134(199601)24:1<138::AID-PROT10>3.3.CO;2-K
10.1006/bbrc.1994.2601
10.1021/bi9520848
10.1021/bi951898l
10.1074/jbc.273.45.29506
10.1021/ja001139c
10.1021/bi981248s
10.1126/science.1909457
10.1016/S0021-9258(18)54148-X / J. Biol. Chem. by Lee HC (1993)
10.1074/jbc.270.16.9060
10.1006/bbrc.1995.1111
10.1016/0896-6273(94)90315-8
10.1002/j.1460-2075.1994.tb06478.x
10.1146/annurev.ph.56.030194.002413
10.1016/0167-4889(93)90199-Y
10.1074/jbc.272.26.16358
10.1152/jn.1999.82.3.1569
10.1016/S0021-9258(19)74367-1 / J. Biol. Chem. by Walseth TF (1993)
10.1016/S0304-4165(99)00161-0
10.1074/jbc.272.33.20378
10.1016/S0304-4165(98)00079-8
10.1074/jbc.271.15.8513
10.1074/jbc.271.20.11599
10.1038/sj.bjp.0701295
10.1093/oxfordjournals.jbchem.a124698
10.1042/bj3190613
10.1038/370307a0
10.1074/jbc.270.51.30257
10.1073/pnas.92.8.3244
10.1074/jbc.272.34.21002
10.1016/S0006-3495(95)79880-0
10.1113/jphysiol.1995.sp020901
10.1038/364076a0
10.1161/01.RES.75.3.596
10.1152/ajpcell.1995.268.5.C1235
10.1093/emboj/17.10.2790
10.1016/0014-5793(94)00931-7
10.1074/jbc.272.39.24234
10.1074/jbc.271.30.17739
10.1126/science.8235594
10.1042/0264-6021:3420269
10.1111/j.1469-7793.1999.00575.x
10.1042/0264-6021:3400519
10.1091/mbc.1.3.279
10.1016/0167-4889(91)90032-S
10.1016/S0076-6879(97)80120-6
10.1016/S0021-9258(18)52240-7 / J. Biol. Chem. by Lee HC (1991)
10.1016/0014-5793(95)00914-U
10.1016/S0076-6879(97)80114-0
10.1073/pnas.96.7.4061
10.1074/jbc.273.5.2497
10.1023/A:1006980630912
10.1074/jbc.270.43.25488
10.1074/jbc.272.50.31272
10.1074/jbc.274.47.33348
10.1038/365456a0
{'key': 'b96', 'first-page': '134', 'volume': '9', 'author': 'Lee HC', 'year': '1994', 'journal-title': 'News Physiol. Sci.'} / News Physiol. Sci. by Lee HC (1994)
10.1074/jbc.273.1.118
10.1074/jbc.271.13.7297
10.1016/S0165-6147(97)90641-6
10.1091/mbc.3.12.1415
10.1054/ceca.1999.0064
10.1523/JNEUROSCI.15-07-05098.1995
10.1016/S0742-8413(97)00173-4
10.1074/jbc.273.14.8017
10.1126/science.7732384
10.1016/S1360-1385(98)01219-9
10.1016/0014-5793(96)01000-9
10.1073/pnas.96.4.1779
10.1006/excr.1998.4070
10.1242/jcs.111.9.1217 / J. Cell Sci. by Churchill GC (1998)
10.1073/pnas.95.26.15837
10.1073/pnas.95.17.10328
10.1074/jbc.270.13.7745
10.1074/jbc.272.7.4172
10.1126/science.8392749
10.1126/science.8392748
10.1006/dbio.1997.8674
10.1074/jbc.273.23.14566
10.1006/bbrc.1998.9583
10.1016/S0143-4160(97)90085-3
10.1074/jbc.275.12.8301
10.1242/dev.121.7.2233 / Development by Ayabe T (1995)
10.1242/dev.121.8.2645 / Development by Yue C (1995)
10.1095/biolreprod56.4.921
10.1016/0014-5793(93)80524-X
10.1126/science.8420005
10.1016/S0960-9822(99)80335-2
10.1038/18032
10.1007/s004240050578
10.1016/S0021-9258(19)39317-2 / J. Biol. Chem. by Matozaki T (1990)
10.1016/S0092-8674(00)81292-1
10.1016/S0960-9822(07)00347-8
10.1161/01.RES.79.1.147
10.1016/S0960-9822(02)00643-7
10.1074/jbc.274.25.17820
10.1161/01.RES.81.5.879
10.1152/ajpcell.1998.274.6.C1653
{'key': 'b138', 'first-page': 'H', 'volume': '39', 'author': 'Kannan MS', 'year': '1996', 'journal-title': 'Am. J. Physiol.'} / Am. J. Physiol. by Kannan MS (1996)
10.1074/jbc.272.25.16023
10.1006/bbrc.1999.1234
10.1074/jbc.270.30.17917
10.4049/jimmunol.155.7.3353 / J. Immunol. by Guse AH (1995)
10.1074/jbc.271.39.23946
10.1074/jbc.272.13.8546
10.1096/fasebj.14.5.680
10.1016/S0898-6568(99)00004-2
10.1016/0143-4160(86)90026-6
10.1042/bj3190393
10.1074/jbc.274.4.1869
10.1074/jbc.270.50.30045
10.1172/JCI1656
10.2337/diabetes.48.12.2309
10.1126/science.8211188
10.1016/0143-4160(94)90002-7
10.1074/jbc.271.32.19074
10.1126/science.262.5133.585
10.1074/jbc.272.6.3133
{'key': 'b158', 'first-page': '355', 'volume': '51', 'author': 'Lee HC', 'year': '1996', 'journal-title': 'Re. Prog. Horm. Res.'} / Re. Prog. Horm. Res. by Lee HC (1996)
10.1113/jphysiol.1995.sp020520
10.1074/jbc.272.34.20967
10.1016/S0306-4522(99)00509-6
10.1111/j.1469-7793.1998.405bt.x
10.1007/s002329900203
10.1152/ajpcell.1997.273.4.C1306
10.1177/00220345980770100801
Lee HC. 1995.Cyclic ADP-ribose: A mediator of a calcium signaling pathway.InRyanodine Receptors, ed. V. Sorrentino, pp. 31–50. Boca Raton, Fl.: CRC
10.1074/jbc.272.25.15771
10.1007/BF00374798
10.1016/0014-5793(95)00131-R
10.1152/ajpcell.1999.276.2.C426
10.1096/fasebj.12.14.1507
10.1096/fasebj.13.2.273
10.1016/S1357-2725(97)00062-9
10.1016/0092-8674(95)90494-8
10.1042/bj3150721
10.1021/bi9705671
10.1016/0014-5793(95)01515-9
10.1016/0263-7855(96)00009-4

Dates

Type	When
Created	23 years, 1 month ago (July 27, 2002, 7:46 a.m.)
Deposited	2 years, 4 months ago (April 23, 2023, 2:59 p.m.)
Indexed	2 weeks, 1 day ago (Aug. 12, 2025, 5:35 p.m.)
Issued	24 years, 4 months ago (April 1, 2001)
Published	24 years, 4 months ago (April 1, 2001)
Published Print	24 years, 4 months ago (April 1, 2001)

Funders 0

None

BibTeX

@article{Lee_2001, title={Physiological Functions of Cyclic ADP-Ribose and NAADP as Calcium Messengers}, volume={41}, ISSN={1545-4304}, url={http://dx.doi.org/10.1146/annurev.pharmtox.41.1.317}, DOI={10.1146/annurev.pharmtox.41.1.317}, number={1}, journal={Annual Review of Pharmacology and Toxicology}, publisher={Annual Reviews}, author={Lee, Hon Cheung}, year={2001}, month=apr, pages={317–345} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        8,
        12
      ]
    ],
    "date-time": "2025-08-12T21:35:10Z",
    "timestamp": 1755034510141
  },
  "reference-count": 178,
  "publisher": "Annual Reviews",
  "issue": "1",
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        2001,
        4
      ]
    ]
  },
  "abstract": "<jats:p>Cyclic ADP-ribose (cADPR) and nicotinic acid adenine dinucleotide phosphate (NAADP) are two Ca<jats:sup>2+</jats:sup>messengers derived from NAD and NADP, respectively. Although NAADP is a linear molecule, structurally distinct from the cyclic cADPR, it is synthesized by similar enzymes, ADP-ribosyl cyclase and its homolog, CD38. The crystal structure of the cyclase has been solved and its active site identified. These two novel nucleotides have now been shown to be involved in a wide range of cellular functions including: cell cycle regulation in Euglena, a protist; gene expression in plants; and in animal systems, from fertilization to neurotransmitter release and long-term depression in brain. A battery of pharmacological reagents have been developed, providing valuable tools for elucidating the physiological functions of these two novel Ca<jats:sup>2+</jats:sup>messengers. This article reviews these recent results and explores the implications of the existence of multiple Ca<jats:sup>2+</jats:sup>messengers and Ca<jats:sup>2+</jats:sup>stores in cells.</jats:p>",
  "DOI": "10.1146/annurev.pharmtox.41.1.317",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2002,
        7,
        27
      ]
    ],
    "date-time": "2002-07-27T11:46:15Z",
    "timestamp": 1027770375000
  },
  "page": "317-345",
  "source": "Crossref",
  "is-referenced-by-count": 310,
  "title": "Physiological Functions of Cyclic ADP-Ribose and NAADP as Calcium Messengers",
  "prefix": "10.1146",
  "volume": "41",
  "author": [
    {
      "given": "Hon Cheung",
      "family": "Lee",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Department of Pharmacology, University of Minnesota, Minneapolis, Minnesota 55455;"
        }
      ]
    }
  ],
  "member": "22",
  "reference": [
    {
      "key": "b1",
      "doi-asserted-by": "crossref",
      "first-page": "9561",
      "DOI": "10.1016/S0021-9258(18)47970-7",
      "volume": "262",
      "author": "Clapper DL",
      "year": "1987",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "b2",
      "doi-asserted-by": "crossref",
      "first-page": "1608",
      "DOI": "10.1016/S0021-9258(18)94230-4",
      "volume": "264",
      "author": "Lee HC",
      "year": "1989",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "b3",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/nsb0394-143"
    },
    {
      "key": "b4",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.270.5.2152"
    },
    {
      "key": "b5",
      "doi-asserted-by": "publisher",
      "DOI": "10.1152/physrev.1997.77.4.1133"
    },
    {
      "key": "b6",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/s002320001001"
    },
    {
      "key": "b7",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.270.51.30327"
    },
    {
      "key": "b8",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.274.43.30770"
    },
    {
      "key": "b9",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.M909365199"
    },
    {
      "key": "b10",
      "doi-asserted-by": "publisher",
      "DOI": "10.1152/ajpcell.1998.274.2.C430"
    },
    {
      "key": "b11",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1469-7793.1998.155bz.x"
    },
    {
      "key": "b12",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0014-5793(97)00168-3"
    },
    {
      "key": "b13",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.278.5346.2126"
    },
    {
      "key": "b14",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/18024"
    },
    {
      "key": "b15",
      "doi-asserted-by": "crossref",
      "first-page": "11725",
      "DOI": "10.1016/S0021-9258(18)80125-9",
      "volume": "264",
      "author": "Rusinko N",
      "year": "1989",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "b16",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0167-4838(93)90113-6"
    },
    {
      "key": "b17",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0083-6729(08)60499-9"
    },
    {
      "key": "b18",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF00928466"
    },
    {
      "key": "b19",
      "doi-asserted-by": "publisher",
      "DOI": "10.1091/mbc.2.3.203"
    },
    {
      "key": "b20",
      "doi-asserted-by": "crossref",
      "first-page": "2811",
      "DOI": "10.4049/jimmunol.144.7.2811",
      "volume": "144",
      "author": "Jackson DG",
      "year": "1990",
      "journal-title": "J. Immunol."
    },
    {
      "key": "b21",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0968-0004(92)90337-9"
    },
    {
      "key": "b22",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/bbrc.1994.2325"
    },
    {
      "key": "b23",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.8395705"
    },
    {
      "key": "b24",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/bbrc.1993.1265"
    },
    {
      "key": "b25",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.8235624"
    },
    {
      "key": "b26",
      "doi-asserted-by": "crossref",
      "first-page": "26052",
      "DOI": "10.1016/S0021-9258(19)74275-6",
      "volume": "268",
      "author": "Takasawa S",
      "year": "1993",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "b27",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0006-8993(98)01347-X"
    },
    {
      "key": "b28",
      "first-page": "81",
      "volume": "12",
      "author": "Fernandez JE",
      "year": "1998",
      "journal-title": "J. Biol. Regul. Homeostatic Agents"
    },
    {
      "key": "b29",
      "doi-asserted-by": "publisher",
      "DOI": "10.1023/A:1006916311348"
    },
    {
      "key": "b30",
      "doi-asserted-by": "publisher",
      "DOI": "10.1515/BC.1999.098"
    },
    {
      "key": "b31",
      "doi-asserted-by": "publisher",
      "DOI": "10.1159/000058774"
    },
    {
      "key": "b32",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0006-8993(95)00885-T"
    },
    {
      "key": "b33",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/15640"
    },
    {
      "key": "b34",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/abbi.1999.1526"
    },
    {
      "key": "b35",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.M908231199"
    },
    {
      "key": "b36",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/bbrc.1998.9752"
    },
    {
      "key": "b37",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/oxfordjournals.jbchem.a022307"
    },
    {
      "key": "b38",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0167-4838(98)00204-0"
    },
    {
      "key": "b39",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/nsb1196-957"
    },
    {
      "key": "b40",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/(SICI)1097-0134(199601)24:1<138::AID-PROT10>3.3.CO;2-K"
    },
    {
      "key": "b41",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/bbrc.1994.2601"
    },
    {
      "key": "b42",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/bi9520848"
    },
    {
      "key": "b43",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/bi951898l"
    },
    {
      "key": "b44",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.273.45.29506"
    },
    {
      "key": "b45",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/ja001139c"
    },
    {
      "key": "b46",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/bi981248s"
    },
    {
      "key": "b47",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.1909457"
    },
    {
      "key": "b48",
      "doi-asserted-by": "crossref",
      "first-page": "293",
      "DOI": "10.1016/S0021-9258(18)54148-X",
      "volume": "268",
      "author": "Lee HC",
      "year": "1993",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "b49",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.270.16.9060"
    },
    {
      "key": "b50",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/bbrc.1995.1111"
    },
    {
      "key": "b51",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0896-6273(94)90315-8"
    },
    {
      "key": "b52",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/j.1460-2075.1994.tb06478.x"
    },
    {
      "key": "b53",
      "doi-asserted-by": "publisher",
      "DOI": "10.1146/annurev.ph.56.030194.002413"
    },
    {
      "key": "b54",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0167-4889(93)90199-Y"
    },
    {
      "key": "b55",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.272.26.16358"
    },
    {
      "key": "b56",
      "doi-asserted-by": "publisher",
      "DOI": "10.1152/jn.1999.82.3.1569"
    },
    {
      "key": "b57",
      "doi-asserted-by": "crossref",
      "first-page": "26686",
      "DOI": "10.1016/S0021-9258(19)74367-1",
      "volume": "268",
      "author": "Walseth TF",
      "year": "1993",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "b58",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0304-4165(99)00161-0"
    },
    {
      "key": "b59",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.272.33.20378"
    },
    {
      "key": "b60",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0304-4165(98)00079-8"
    },
    {
      "key": "b61",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.271.15.8513"
    },
    {
      "key": "b62",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.271.20.11599"
    },
    {
      "key": "b63",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/sj.bjp.0701295"
    },
    {
      "key": "b64",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/oxfordjournals.jbchem.a124698"
    },
    {
      "key": "b65",
      "doi-asserted-by": "publisher",
      "DOI": "10.1042/bj3190613"
    },
    {
      "key": "b66",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/370307a0"
    },
    {
      "key": "b67",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.270.51.30257"
    },
    {
      "key": "b68",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.92.8.3244"
    },
    {
      "key": "b69",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.272.34.21002"
    },
    {
      "key": "b70",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0006-3495(95)79880-0"
    },
    {
      "key": "b71",
      "doi-asserted-by": "publisher",
      "DOI": "10.1113/jphysiol.1995.sp020901"
    },
    {
      "key": "b72",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/364076a0"
    },
    {
      "key": "b73",
      "doi-asserted-by": "publisher",
      "DOI": "10.1161/01.RES.75.3.596"
    },
    {
      "key": "b74",
      "doi-asserted-by": "publisher",
      "DOI": "10.1152/ajpcell.1995.268.5.C1235"
    },
    {
      "key": "b75",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/emboj/17.10.2790"
    },
    {
      "key": "b76",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0014-5793(94)00931-7"
    },
    {
      "key": "b77",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.272.39.24234"
    },
    {
      "key": "b78",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.271.30.17739"
    },
    {
      "key": "b79",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.8235594"
    },
    {
      "key": "b80",
      "doi-asserted-by": "publisher",
      "DOI": "10.1042/0264-6021:3420269"
    },
    {
      "key": "b81",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1469-7793.1999.00575.x"
    },
    {
      "key": "b82",
      "doi-asserted-by": "publisher",
      "DOI": "10.1042/0264-6021:3400519"
    },
    {
      "key": "b83",
      "doi-asserted-by": "publisher",
      "DOI": "10.1091/mbc.1.3.279"
    },
    {
      "key": "b84",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0167-4889(91)90032-S"
    },
    {
      "key": "b85",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0076-6879(97)80120-6"
    },
    {
      "key": "b86",
      "doi-asserted-by": "crossref",
      "first-page": "2276",
      "DOI": "10.1016/S0021-9258(18)52240-7",
      "volume": "266",
      "author": "Lee HC",
      "year": "1991",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "b87",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0014-5793(95)00914-U"
    },
    {
      "key": "b88",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0076-6879(97)80114-0"
    },
    {
      "key": "b89",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.96.7.4061"
    },
    {
      "key": "b90",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.273.5.2497"
    },
    {
      "key": "b91",
      "doi-asserted-by": "publisher",
      "DOI": "10.1023/A:1006980630912"
    },
    {
      "key": "b92",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.270.43.25488"
    },
    {
      "key": "b93",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.272.50.31272"
    },
    {
      "key": "b94",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.274.47.33348"
    },
    {
      "key": "b95",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/365456a0"
    },
    {
      "key": "b96",
      "first-page": "134",
      "volume": "9",
      "author": "Lee HC",
      "year": "1994",
      "journal-title": "News Physiol. Sci."
    },
    {
      "key": "b97",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.273.1.118"
    },
    {
      "key": "b98",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.271.13.7297"
    },
    {
      "key": "b99",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0165-6147(97)90641-6"
    },
    {
      "key": "b100",
      "doi-asserted-by": "publisher",
      "DOI": "10.1091/mbc.3.12.1415"
    },
    {
      "key": "b101",
      "doi-asserted-by": "publisher",
      "DOI": "10.1054/ceca.1999.0064"
    },
    {
      "key": "b102",
      "doi-asserted-by": "publisher",
      "DOI": "10.1523/JNEUROSCI.15-07-05098.1995"
    },
    {
      "key": "b103",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0742-8413(97)00173-4"
    },
    {
      "key": "b104",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.273.14.8017"
    },
    {
      "key": "b105",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.7732384"
    },
    {
      "key": "b106",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S1360-1385(98)01219-9"
    },
    {
      "key": "b107",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0014-5793(96)01000-9"
    },
    {
      "key": "b108",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.96.4.1779"
    },
    {
      "key": "b109",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/excr.1998.4070"
    },
    {
      "key": "b110",
      "doi-asserted-by": "crossref",
      "first-page": "1217",
      "DOI": "10.1242/jcs.111.9.1217",
      "volume": "111",
      "author": "Churchill GC",
      "year": "1998",
      "journal-title": "J. Cell Sci."
    },
    {
      "key": "b111",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.95.26.15837"
    },
    {
      "key": "b112",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.95.17.10328"
    },
    {
      "key": "b113",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.270.13.7745"
    },
    {
      "key": "b114",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.272.7.4172"
    },
    {
      "key": "b115",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.8392749"
    },
    {
      "key": "b116",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.8392748"
    },
    {
      "key": "b117",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/dbio.1997.8674"
    },
    {
      "key": "b118",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.273.23.14566"
    },
    {
      "key": "b119",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/bbrc.1998.9583"
    },
    {
      "key": "b120",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0143-4160(97)90085-3"
    },
    {
      "key": "b121",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.275.12.8301"
    },
    {
      "key": "b122",
      "doi-asserted-by": "crossref",
      "first-page": "2233",
      "DOI": "10.1242/dev.121.7.2233",
      "volume": "121",
      "author": "Ayabe T",
      "year": "1995",
      "journal-title": "Development"
    },
    {
      "key": "b123",
      "doi-asserted-by": "crossref",
      "first-page": "2645",
      "DOI": "10.1242/dev.121.8.2645",
      "volume": "121",
      "author": "Yue C",
      "year": "1995",
      "journal-title": "Development"
    },
    {
      "key": "b124",
      "doi-asserted-by": "publisher",
      "DOI": "10.1095/biolreprod56.4.921"
    },
    {
      "key": "b125",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0014-5793(93)80524-X"
    },
    {
      "key": "b126",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.8420005"
    },
    {
      "key": "b127",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0960-9822(99)80335-2"
    },
    {
      "key": "b128",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/18032"
    },
    {
      "key": "b129",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/s004240050578"
    },
    {
      "key": "b130",
      "doi-asserted-by": "crossref",
      "first-page": "6247",
      "DOI": "10.1016/S0021-9258(19)39317-2",
      "volume": "265",
      "author": "Matozaki T",
      "year": "1990",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "b131",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0092-8674(00)81292-1"
    },
    {
      "key": "b132",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0960-9822(07)00347-8"
    },
    {
      "key": "b133",
      "doi-asserted-by": "publisher",
      "DOI": "10.1161/01.RES.79.1.147"
    },
    {
      "key": "b134",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0960-9822(02)00643-7"
    },
    {
      "key": "b135",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.274.25.17820"
    },
    {
      "key": "b136",
      "doi-asserted-by": "publisher",
      "DOI": "10.1161/01.RES.81.5.879"
    },
    {
      "key": "b137",
      "doi-asserted-by": "publisher",
      "DOI": "10.1152/ajpcell.1998.274.6.C1653"
    },
    {
      "key": "b138",
      "first-page": "H",
      "volume": "39",
      "author": "Kannan MS",
      "year": "1996",
      "journal-title": "Am. J. Physiol."
    },
    {
      "key": "b139",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.272.25.16023"
    },
    {
      "key": "b140",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/bbrc.1999.1234"
    },
    {
      "key": "b141",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.270.30.17917"
    },
    {
      "key": "b142",
      "doi-asserted-by": "crossref",
      "first-page": "3353",
      "DOI": "10.4049/jimmunol.155.7.3353",
      "volume": "155",
      "author": "Guse AH",
      "year": "1995",
      "journal-title": "J. Immunol."
    },
    {
      "key": "b143",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.271.39.23946"
    },
    {
      "key": "b144",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.272.13.8546"
    },
    {
      "key": "b145",
      "doi-asserted-by": "publisher",
      "DOI": "10.1096/fasebj.14.5.680"
    },
    {
      "key": "b146",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0898-6568(99)00004-2"
    },
    {
      "key": "b147",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0143-4160(86)90026-6"
    },
    {
      "key": "b148",
      "doi-asserted-by": "publisher",
      "DOI": "10.1042/bj3190393"
    },
    {
      "key": "b149",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.274.4.1869"
    },
    {
      "key": "b150",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.270.50.30045"
    },
    {
      "key": "b151",
      "doi-asserted-by": "publisher",
      "DOI": "10.1172/JCI1656"
    },
    {
      "key": "b152",
      "doi-asserted-by": "publisher",
      "DOI": "10.2337/diabetes.48.12.2309"
    },
    {
      "key": "b153",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.8211188"
    },
    {
      "key": "b154",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0143-4160(94)90002-7"
    },
    {
      "key": "b155",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.271.32.19074"
    },
    {
      "key": "b156",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.262.5133.585"
    },
    {
      "key": "b157",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.272.6.3133"
    },
    {
      "key": "b158",
      "first-page": "355",
      "volume": "51",
      "author": "Lee HC",
      "year": "1996",
      "journal-title": "Re. Prog. Horm. Res."
    },
    {
      "key": "b159",
      "doi-asserted-by": "publisher",
      "DOI": "10.1113/jphysiol.1995.sp020520"
    },
    {
      "key": "b160",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.272.34.20967"
    },
    {
      "key": "b161",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0306-4522(99)00509-6"
    },
    {
      "key": "b162",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1469-7793.1998.405bt.x"
    },
    {
      "key": "b163",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/s002329900203"
    },
    {
      "key": "b164",
      "doi-asserted-by": "publisher",
      "DOI": "10.1152/ajpcell.1997.273.4.C1306"
    },
    {
      "key": "b165",
      "doi-asserted-by": "publisher",
      "DOI": "10.1177/00220345980770100801"
    },
    {
      "key": "b166",
      "unstructured": "Lee HC. 1995.Cyclic ADP-ribose: A mediator of a calcium signaling pathway.InRyanodine Receptors, ed. V. Sorrentino, pp. 31\u201350. Boca Raton, Fl.: CRC"
    },
    {
      "key": "b167",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.272.25.15771"
    },
    {
      "key": "b168",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF00374798"
    },
    {
      "key": "b169",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0014-5793(95)00131-R"
    },
    {
      "key": "b170",
      "doi-asserted-by": "publisher",
      "DOI": "10.1152/ajpcell.1999.276.2.C426"
    },
    {
      "key": "b171",
      "doi-asserted-by": "publisher",
      "DOI": "10.1096/fasebj.12.14.1507"
    },
    {
      "key": "b172",
      "doi-asserted-by": "publisher",
      "DOI": "10.1096/fasebj.13.2.273"
    },
    {
      "key": "b173",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S1357-2725(97)00062-9"
    },
    {
      "key": "b174",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(95)90494-8"
    },
    {
      "key": "b175",
      "doi-asserted-by": "publisher",
      "DOI": "10.1042/bj3150721"
    },
    {
      "key": "b176",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/bi9705671"
    },
    {
      "key": "b177",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0014-5793(95)01515-9"
    },
    {
      "key": "b178",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0263-7855(96)00009-4"
    }
  ],
  "container-title": "Annual Review of Pharmacology and Toxicology",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://www.annualreviews.org/doi/pdf/10.1146/annurev.pharmtox.41.1.317",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        4,
        23
      ]
    ],
    "date-time": "2023-04-23T18:59:06Z",
    "timestamp": 1682276346000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://www.annualreviews.org/doi/10.1146/annurev.pharmtox.41.1.317"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2001,
        4
      ]
    ]
  },
  "references-count": 178,
  "journal-issue": {
    "issue": "1",
    "published-print": {
      "date-parts": [
        [
          2001,
          4
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1146/annurev.pharmtox.41.1.317"
  ],
  "URL": "http://dx.doi.org/10.1146/annurev.pharmtox.41.1.317",
  "relation": {},
  "ISSN": [
    "0362-1642",
    "1545-4304"
  ],
  "subject": [],
  "container-title-short": "Annu. Rev. Pharmacol. Toxicol.",
  "published": {
    "date-parts": [
      [
        2001,
        4
      ]
    ]
  }
}