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Endolysosomal Ca2+ Signaling in Cancer: The Role of TPC2, From Tumorigenesis to Metastasis.

Alharbi AF, Parrington J.

Front Cell Dev Biol. 2019 Dec 4;7:302. doi: 10.3389/fcell.2019.00302. eCollection 2019. Review.


The eggstraordinary story of how life begins.

Parrington J, Arnoult C, Fissore RA.

Mol Reprod Dev. 2019 Jan;86(1):4-19. doi: 10.1002/mrd.23083. Epub 2018 Nov 30. Review.


Tpcn2 knockout mice have improved insulin sensitivity and are protected against high-fat diet-induced weight gain.

He H, Holl K, DeBehnke S, Yeo CT, Hansen P, Gebre AK, Leone-Kabler S, Ruas M, Parks JS, Parrington J, Solberg Woods LC.

Physiol Genomics. 2018 Aug 1;50(8):605-614. doi: 10.1152/physiolgenomics.00135.2017. Epub 2018 May 11.


PLCζ is the physiological trigger of the Ca2+ oscillations that induce embryogenesis in mammals but conception can occur in its absence.

Hachem A, Godwin J, Ruas M, Lee HC, Ferrer Buitrago M, Ardestani G, Bassett A, Fox S, Navarrete F, de Sutter P, Heindryckx B, Fissore R, Parrington J.

Development. 2017 Aug 15;144(16):2914-2924. doi: 10.1242/dev.150227. Epub 2017 Jul 10.


Synthesis of the Ca2+-mobilizing messengers NAADP and cADPR by intracellular CD38 enzyme in the mouse heart: Role in β-adrenoceptor signaling.

Lin WK, Bolton EL, Cortopassi WA, Wang Y, O'Brien F, Maciejewska M, Jacobson MP, Garnham C, Ruas M, Parrington J, Lei M, Sitsapesan R, Galione A, Terrar DA.

J Biol Chem. 2017 Aug 11;292(32):13243-13257. doi: 10.1074/jbc.M117.789347. Epub 2017 May 24.


Ca2+ release via two-pore channel type 2 (TPC2) is required for slow muscle cell myofibrillogenesis and myotomal patterning in intact zebrafish embryos.

Kelu JJ, Webb SE, Parrington J, Galione A, Miller AL.

Dev Biol. 2017 May 15;425(2):109-129. doi: 10.1016/j.ydbio.2017.03.031. Epub 2017 Apr 6.


Metabolic alterations derived from absence of Two-Pore Channel 1 at cardiac level.

Garcia-Rua V, Feijoo-Bandin S, Garcia-Vence M, Aragon-Herrera A, Bravo SB, Rodriguez-Penas D, Mosquera-Leal A, Lear PV, Parrington J, Alonso J, Rosello-Lleti E, Portoles M, Rivera M, Gonzalez-Juanatey JR, Lago F.

J Biosci. 2016 Dec;41(4):643-658.


Two-Pore Channels: Lessons from Mutant Mouse Models.

Ruas M, Galione A, Parrington J.

Messenger (Los Angel). 2015 Jun;4(1):4-22.


The two pore channel TPC2 is dispensable in pancreatic β-cells for normal Ca²⁺ dynamics and insulin secretion.

Cane MC, Parrington J, Rorsman P, Galione A, Rutter GA.

Cell Calcium. 2016 Jan;59(1):32-40. doi: 10.1016/j.ceca.2015.12.004. Epub 2015 Dec 23.


Endolysosomal two-pore channels regulate autophagy in cardiomyocytes.

García-Rúa V, Feijóo-Bandín S, Rodríguez-Penas D, Mosquera-Leal A, Abu-Assi E, Beiras A, María Seoane L, Lear P, Parrington J, Portolés M, Roselló-Lletí E, Rivera M, Gualillo O, Parra V, Hill JA, Rothermel B, González-Juanatey JR, Lago F.

J Physiol. 2016 Jun 1;594(11):3061-77. doi: 10.1113/JP271332. Epub 2016 Feb 4.


Calcium signals regulated by NAADP and two-pore channels--their role in development, differentiation and cancer.

Parrington J, Lear P, Hachem A.

Int J Dev Biol. 2015;59(7-9):341-55. doi: 10.1387/ijdb.150211jp. Review.


Two-Pore Channel 2 activity is required for slow muscle cell-generated Ca(2+) signaling during myogenesis in intact zebrafish.

Kelu JJ, Chan HL, Webb SE, Cheng AH, Ruas M, Parrington J, Galione A, Miller AL.

Int J Dev Biol. 2015;59(7-9):313-25. doi: 10.1387/ijdb.150206am.


Two-pore Channels (TPC2s) and Nicotinic Acid Adenine Dinucleotide Phosphate (NAADP) at Lysosomal-Sarcoplasmic Reticular Junctions Contribute to Acute and Chronic β-Adrenoceptor Signaling in the Heart.

Capel RA, Bolton EL, Lin WK, Aston D, Wang Y, Liu W, Wang X, Burton RA, Bloor-Young D, Shade KT, Ruas M, Parrington J, Churchill GC, Lei M, Galione A, Terrar DA.

J Biol Chem. 2015 Dec 11;290(50):30087-98. doi: 10.1074/jbc.M115.684076. Epub 2015 Oct 5.


Nicotinic Acid Adenine Dinucleotide Phosphate (NAADP) and Endolysosomal Two-pore Channels Modulate Membrane Excitability and Stimulus-Secretion Coupling in Mouse Pancreatic β Cells.

Arredouani A, Ruas M, Collins SC, Parkesh R, Clough F, Pillinger T, Coltart G, Rietdorf K, Royle A, Johnson P, Braun M, Zhang Q, Sones W, Shimomura K, Morgan AJ, Lewis AM, Chuang KT, Tunn R, Gadea J, Teboul L, Heister PM, Tynan PW, Bellomo EA, Rutter GA, Rorsman P, Churchill GC, Parrington J, Galione A.

J Biol Chem. 2015 Aug 28;290(35):21376-92. doi: 10.1074/jbc.M115.671248. Epub 2015 Jul 7.


Both RyRs and TPCs are required for NAADP-induced intracellular Ca²⁺ release.

Gerasimenko JV, Charlesworth RM, Sherwood MW, Ferdek PE, Mikoshiba K, Parrington J, Petersen OH, Gerasimenko OV.

Cell Calcium. 2015 Sep;58(3):237-45. doi: 10.1016/j.ceca.2015.05.005. Epub 2015 Jun 10.


Reply to "TPC1 Knockout Knocks Out TPC1".

Ruas M, Galione A, Parrington J.

Mol Cell Biol. 2015 May;35(10):1884. doi: 10.1128/MCB.00083-15. No abstract available.


Expression of Ca²⁺-permeable two-pore channels rescues NAADP signalling in TPC-deficient cells.

Ruas M, Davis LC, Chen CC, Morgan AJ, Chuang KT, Walseth TF, Grimm C, Garnham C, Powell T, Platt N, Platt FM, Biel M, Wahl-Schott C, Parrington J, Galione A.

EMBO J. 2015 Jul 2;34(13):1743-58. doi: 10.15252/embj.201490009. Epub 2015 Apr 14.


Absence of intracellular ion channels TPC1 and TPC2 leads to mature-onset obesity in male mice, due to impaired lipid availability for thermogenesis in brown adipose tissue.

Lear PV, González-Touceda D, Porteiro Couto B, Viaño P, Guymer V, Remzova E, Tunn R, Chalasani A, García-Caballero T, Hargreaves IP, Tynan PW, Christian HC, Nogueiras R, Parrington J, Diéguez C.

Endocrinology. 2015 Mar;156(3):975-86. doi: 10.1210/en.2014-1766. Epub 2014 Dec 29.


Lysosomal two-pore channel subtype 2 (TPC2) regulates skeletal muscle autophagic signaling.

Lin PH, Duann P, Komazaki S, Park KH, Li H, Sun M, Sermersheim M, Gumpper K, Parrington J, Galione A, Evans AM, Zhu MX, Ma J.

J Biol Chem. 2015 Feb 6;290(6):3377-89. doi: 10.1074/jbc.M114.608471. Epub 2014 Dec 5.


VEGF-induced neoangiogenesis is mediated by NAADP and two-pore channel-2-dependent Ca2+ signaling.

Favia A, Desideri M, Gambara G, D'Alessio A, Ruas M, Esposito B, Del Bufalo D, Parrington J, Ziparo E, Palombi F, Galione A, Filippini A.

Proc Natl Acad Sci U S A. 2014 Nov 4;111(44):E4706-15. doi: 10.1073/pnas.1406029111. Epub 2014 Oct 20.


Synthesis of caged NAADP.

Galione A, Chuang KT, Funnell TM, Davis LC, Morgan AJ, Ruas M, Parrington J, Churchill GC.

Cold Spring Harb Protoc. 2014 Oct 1;2014(10):pdb.prot076943. doi: 10.1101/pdb.prot076943.


Measurement of luminal pH of acidic stores as a readout for NAADP action.

Galione A, Chuang KT, Funnell TM, Davis LC, Morgan AJ, Ruas M, Parrington J, Churchill GC.

Cold Spring Harb Protoc. 2014 Oct 1;2014(10):pdb.prot076935. doi: 10.1101/pdb.prot076935.


Synthesis of NAADP-AM as a membrane-permeant NAADP analog.

Galione A, Chuang KT, Funnell TM, Davis LC, Morgan AJ, Ruas M, Parrington J, Churchill GC.

Cold Spring Harb Protoc. 2014 Oct 1;2014(10):pdb.prot076927. doi: 10.1101/pdb.prot076927.


Identification of a novel gene for diabetic traits in rats, mice, and humans.

Tsaih SW, Holl K, Jia S, Kaldunski M, Tschannen M, He H, Andrae JW, Li SH, Stoddard A, Wiederhold A, Parrington J, Ruas da Silva M, Galione A, Meigs J; Meta-Analyses of Glucose and Insulin-Related Traits Consortium (MAGIC) Investigators, Hoffmann RG, Simpson P, Jacob H, Hessner M, Solberg Woods LC.

Genetics. 2014 Sep;198(1):17-29. doi: 10.1534/genetics.114.162982.


Synthesis of [³²P]NAADP for the radioreceptor binding assay.

Galione A, Chuang KT, Funnell TM, Davis LC, Morgan AJ, Ruas M, Parrington J, Churchill GC.

Cold Spring Harb Protoc. 2014 Sep 2;2014(9):993-5. doi: 10.1101/pdb.prot076919.


Preparation and use of sea urchin egg homogenates for studying NAADP-mediated Ca²⁺ release.

Galione A, Chuang KT, Funnell TM, Davis LC, Morgan AJ, Ruas M, Parrington J, Churchill GC.

Cold Spring Harb Protoc. 2014 Sep 2;2014(9):988-92. doi: 10.1101/pdb.prot076901.


TPC1 has two variant isoforms, and their removal has different effects on endo-lysosomal functions compared to loss of TPC2.

Ruas M, Chuang KT, Davis LC, Al-Douri A, Tynan PW, Tunn R, Teboul L, Galione A, Parrington J.

Mol Cell Biol. 2014 Nov;34(21):3981-92. doi: 10.1128/MCB.00113-14. Epub 2014 Aug 18.


Ca(2+) signals, NAADP and two-pore channels: role in cellular differentiation.

Parrington J, Tunn R.

Acta Physiol (Oxf). 2014 Jun;211(2):285-96. doi: 10.1111/apha.12298. Review.


Bidirectional Ca²⁺ signaling occurs between the endoplasmic reticulum and acidic organelles.

Morgan AJ, Davis LC, Wagner SK, Lewis AM, Parrington J, Churchill GC, Galione A.

J Cell Biol. 2013 Mar 18;200(6):789-805. doi: 10.1083/jcb.201204078. Epub 2013 Mar 11.


NAADP activates two-pore channels on T cell cytolytic granules to stimulate exocytosis and killing.

Davis LC, Morgan AJ, Chen JL, Snead CM, Bloor-Young D, Shenderov E, Stanton-Humphreys MN, Conway SJ, Churchill GC, Parrington J, Cerundolo V, Galione A.

Curr Biol. 2012 Dec 18;22(24):2331-7. doi: 10.1016/j.cub.2012.10.035. Epub 2012 Nov 21.


The luminal Ca(2+) chelator, TPEN, inhibits NAADP-induced Ca(2+) release.

Morgan AJ, Parrington J, Galione A.

Cell Calcium. 2012 Dec;52(6):481-7. doi: 10.1016/j.ceca.2012.09.001. Epub 2012 Oct 23.


Variance in total levels of phospholipase C zeta (PLC-ζ) in human sperm may limit the applicability of quantitative immunofluorescent analysis as a diagnostic indicator of oocyte activation capability.

Kashir J, Jones C, Mounce G, Ramadan WM, Lemmon B, Heindryckx B, de Sutter P, Parrington J, Turner K, Child T, McVeigh E, Coward K.

Fertil Steril. 2013 Jan;99(1):107-17. doi: 10.1016/j.fertnstert.2012.09.001. Epub 2012 Oct 3.


Increased expression of fatty-acid and calcium metabolism genes in failing human heart.

García-Rúa V, Otero MF, Lear PV, Rodríguez-Penas D, Feijóo-Bandín S, Noguera-Moreno T, Calaza M, Álvarez-Barredo M, Mosquera-Leal A, Parrington J, Brugada J, Portolés M, Rivera M, González-Juanatey JR, Lago F.

PLoS One. 2012;7(6):e37505. doi: 10.1371/journal.pone.0037505. Epub 2012 Jun 6.


Characterization of two heterozygous mutations of the oocyte activation factor phospholipase C zeta (PLCζ) from an infertile man by use of minisequencing of individual sperm and expression in somatic cells.

Kashir J, Konstantinidis M, Jones C, Heindryckx B, De Sutter P, Parrington J, Wells D, Coward K.

Fertil Steril. 2012 Aug;98(2):423-31. doi: 10.1016/j.fertnstert.2012.05.002. Epub 2012 May 24.


A sperm's tail: the need to consider temporal aspects of specific physiological mechanisms during and following gamete fusion.

Kashir J, Heindryckx B, Jones C, De Sutter P, Parrington J, Coward K.

Hum Reprod. 2012 Feb;27(2):625-6. doi: 10.1093/humrep/der411. Epub 2011 Nov 28. No abstract available.


Photoaffinity labeling of high affinity nicotinic acid adenine dinucleotide phosphate (NAADP)-binding proteins in sea urchin egg.

Walseth TF, Lin-Moshier Y, Jain P, Ruas M, Parrington J, Galione A, Marchant JS, Slama JT.

J Biol Chem. 2012 Jan 20;287(4):2308-15. doi: 10.1074/jbc.M111.306563. Epub 2011 Nov 23.


A maternally inherited autosomal point mutation in human phospholipase C zeta (PLCζ) leads to male infertility.

Kashir J, Konstantinidis M, Jones C, Lemmon B, Lee HC, Hamer R, Heindryckx B, Deane CM, De Sutter P, Fissore RA, Parrington J, Wells D, Coward K.

Hum Reprod. 2012 Jan;27(1):222-31. doi: 10.1093/humrep/der384. Epub 2011 Nov 16.


Loss of activity mutations in phospholipase C zeta (PLCζ) abolishes calcium oscillatory ability of human recombinant protein in mouse oocytes.

Kashir J, Jones C, Lee HC, Rietdorf K, Nikiforaki D, Durrans C, Ruas M, Tee ST, Heindryckx B, Galione A, De Sutter P, Fissore RA, Parrington J, Coward K.

Hum Reprod. 2011 Dec;26(12):3372-87. doi: 10.1093/humrep/der336. Epub 2011 Oct 18.


Two-pore channels form homo- and heterodimers.

Rietdorf K, Funnell TM, Ruas M, Heinemann J, Parrington J, Galione A.

J Biol Chem. 2011 Oct 28;286(43):37058-62. doi: 10.1074/jbc.C111.289835. Epub 2011 Sep 8.


Quantitative expression of phospholipase C zeta, as an index to assess fertilization potential of a semen sample.

Aghajanpour S, Ghaedi K, Salamian A, Deemeh MR, Tavalaee M, Moshtaghian J, Parrington J, Nasr-Esfahani MH.

Hum Reprod. 2011 Nov;26(11):2950-6. doi: 10.1093/humrep/der285. Epub 2011 Sep 6.


PLCζ and its role as a trigger of development in vertebrates.

Ito J, Parrington J, Fissore RA.

Mol Reprod Dev. 2011 Oct-Nov;78(10-11):846-53. doi: 10.1002/mrd.21359. Epub 2011 Aug 5. Review.


Physiological roles of NAADP-mediated Ca2+ signaling.

Galione A, Parrington J, Funnell T.

Sci China Life Sci. 2011 Aug;54(8):725-32. doi: 10.1007/s11427-011-4207-5. Epub 2011 Jul 24. Review.


Effects of cryopreservation and density-gradient washing on phospholipase C zeta concentrations in human spermatozoa.

Kashir J, Heynen A, Jones C, Durrans C, Craig J, Gadea J, Turner K, Parrington J, Coward K.

Reprod Biomed Online. 2011 Aug;23(2):263-7. doi: 10.1016/j.rbmo.2011.04.006. Epub 2011 May 7.


Identification and functional analysis of an ovarian form of the egg activation factor phospholipase C zeta (PLCζ) in pufferfish.

Coward K, Ponting CP, Zhang N, Young C, Huang CJ, Chou CM, Kashir J, Fissore RA, Parrington J.

Mol Reprod Dev. 2011 Jan;78(1):48-56. doi: 10.1002/mrd.21262. Epub 2011 Jan 14.


Sperm and testis mediated DNA transfer as a means of gene therapy.

Parrington J, Coward K, Gadea J.

Syst Biol Reprod Med. 2011 Feb;57(1-2):35-42. doi: 10.3109/19396368.2010.514022. Review.


NAADP as an intracellular messenger regulating lysosomal calcium-release channels.

Galione A, Morgan AJ, Arredouani A, Davis LC, Rietdorf K, Ruas M, Parrington J.

Biochem Soc Trans. 2010 Dec;38(6):1424-31. doi: 10.1042/BST0381424.


An emerging role for NAADP-mediated Ca2+ signaling in the pancreatic β-cell.

Arredouani A, Evans AM, Ma J, Parrington J, Zhu MX, Galione A.

Islets. 2010 Sep-Oct;2(5):323-30. Epub 2010 Sep 1.


Reduced fertilization after ICSI and abnormal phospholipase C zeta presence in spermatozoa from the wobbler mouse.

Heytens E, Schmitt-John T, Moser JM, Jensen NM, Soleimani R, Young C, Coward K, Parrington J, De Sutter P.

Reprod Biomed Online. 2010 Dec;21(6):742-9. doi: 10.1016/j.rbmo.2010.07.006. Epub 2010 Jul 18.


TPC2 is a novel NAADP-sensitive Ca2+ release channel, operating as a dual sensor of luminal pH and Ca2+.

Pitt SJ, Funnell TM, Sitsapesan M, Venturi E, Rietdorf K, Ruas M, Ganesan A, Gosain R, Churchill GC, Zhu MX, Parrington J, Galione A, Sitsapesan R.

J Biol Chem. 2010 Nov 5;285(45):35039-46. doi: 10.1074/jbc.M110.156927. Epub 2010 Aug 18.


Oocyte activation, phospholipase C zeta and human infertility.

Kashir J, Heindryckx B, Jones C, De Sutter P, Parrington J, Coward K.

Hum Reprod Update. 2010 Nov-Dec;16(6):690-703. doi: 10.1093/humupd/dmq018. Epub 2010 Jun 23. Review.


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