TPC1 Has Two Variant Isoforms, and Their Removal Has Different Effects on Endo-Lysosomal Functions Compared to Loss of TPC2

REFERENCES

• Zwang Y, Yarden Y. 2009. Systems biology of growth factor-induced receptor endocytosis. Traffic 10:349–363. http://dx.doi.org/10.1111/j.1600-0854.2008.00870.x.
   PubMedGoogle Scholar
• Blakely RD, Edwards RH. 2012. Vesicular and plasma membrane transporters for neurotransmitters. Cold Spring Harb. Perspect. Biol. 4:a005595. http://dx.doi.org/10.1101/cshperspect.a005595.
   PubMed Web of Science ®Google Scholar
• Bird PI, Trapani JA, Villadangos JA. 2009. Endolysosomal proteases and their inhibitors in immunity. Nat. Rev. Immunol. 9:871–882. http://dx.doi.org/10.1038/nri2671.
   PubMed Web of Science ®Google Scholar
• Kraft C, Martens S. 2012. Mechanisms and regulation of autophagosome formation. Curr. Opin. Cell Biol. 24:496–501. http://dx.doi.org/10.1016/j.ceb.2012.05.001.
   PubMed Web of Science ®Google Scholar
• Groves E, Dart AE, Covarelli V, Caron E. 2008. Molecular mechanisms of phagocytic uptake in mammalian cells. Cell. Mol. Life Sci. 65:1957–1976. http://dx.doi.org/10.1007/s00018-008-7578-4.
   PubMed Web of Science ®Google Scholar
• Morgan AJ, Platt FM, Lloyd-Evans E, Galione A. 2011. Molecular mechanisms of endolysosomal Ca2+ signalling in health and disease. Biochem. J. 439:349–374. http://dx.doi.org/10.1042/BJ20110949.
   PubMed Web of Science ®Google Scholar
• Lloyd-Evans E, Platt FM. 2011. Lysosomal Ca2+ homeostasis: role in pathogenesis of lysosomal storage diseases. Cell Calcium 50:200–205. http://dx.doi.org/10.1016/j.ceca.2011.03.010.
   PubMed Web of Science ®Google Scholar
• Abe K, Puertollano R. 2011. Role of TRP channels in the regulation of the endosomal pathway. Physiology 26:14–22. http://dx.doi.org/10.1152/physiol.00048.2010.
   PubMedGoogle Scholar
• Ishibashi K, Suzuki M, Imai M. 2000. Molecular cloning of a novel form (two-repeat) protein related to voltage-gated sodium and calcium channels. Biochem. Biophys. Res. Commun. 270:370–376. http://dx.doi.org/10.1006/bbrc.2000.2435.
   PubMedGoogle Scholar
• Calcraft PJ, Ruas M, Pan Z, Cheng X, Arredouani A, Hao X, Tang J, Rietdorf K, Teboul L, Chuang K-T, Lin P, Xiao R, Wang C, Zhu Y, Lin Y, Wyatt CN, Parrington J, Ma J, Evans AM, Galione A, Zhu MX. 2009. NAADP mobilizes calcium from acidic organelles through two-pore channels. Nature 459:596–600. http://dx.doi.org/10.1038/nature08030.
   PubMed Web of Science ®Google Scholar
• Zong X, Schieder M, Cuny H, Fenske S, Gruner C, Rötzer K, Griesbeck O, Harz H, Biel M, Wahl-Schott C. 2009. The two-pore channel TPCN2 mediates NAADP-dependent Ca2+-release from lysosomal stores. Pflugers Arch. 458:891–899. http://dx.doi.org/10.1007/s00424-009-0690-y.
   PubMed Web of Science ®Google Scholar
• Brailoiu E, Churamani D, Cai X, Schrlau MG, Brailoiu GC, Gao X, Hooper R, Boulware MJ, Dun NJ, Marchant JS, Patel S. 2009. Essential requirement for two-pore channel 1 in NAADP-mediated calcium signaling. J. Cell Biol. 186:201–209. http://dx.doi.org/10.1083/jcb.200904073.
   PubMed Web of Science ®Google Scholar
• Clapham DE, Garbers DL. 2005. International Union of Pharmacology. L. Nomenclature and structure-function relationships of CatSper and two-pore channels. Pharmacol. Rev. 57:451–454. http://dx.doi.org/10.1124/pr.57.4.7.
   PubMed Web of Science ®Google Scholar
• Galione A, Evans AM, Ma J, Parrington J, Arredouani A, Cheng X, Zhu MX. 2009. The acid test: the discovery of two-pore channels (TPCs) as NAADP-gated endolysosomal Ca2+ release channels. Pflugers Arch. 458:869–876. http://dx.doi.org/10.1007/s00424-009-0682-y.
   PubMed Web of Science ®Google Scholar
• Zhu MX, Ma J, Parrington J, Calcraft PJ, Galione A, Evans AM. 2010. Calcium signaling via two-pore channels: local or global, that is the question. Am. J. Physiol. Cell Physiol. 298:C430–C441. http://dx.doi.org/10.1152/ajpcell.00475.2009.
   PubMed Web of Science ®Google Scholar
• Ruas M, Rietdorf K, Arredouani A, Davis LC, Lloyd-Evans E, Koegel H, Funnell TM, Morgan AJ, Ward JA, Watanabe K, Cheng X, Churchill GC, Zhu MX, Platt FM, Wessel GM, Parrington J, Galione A. 2010. Purified TPC isoforms form NAADP receptors with distinct roles for Ca2+ signaling and endolysosomal trafficking. Curr. Biol. 20:703–709. http://dx.doi.org/10.1016/j.cub.2010.02.049.
   PubMed Web of Science ®Google Scholar
• Bonifacino JS, Traub LM. 2003. Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu. Rev. Biochem. 72:395–447. http://dx.doi.org/10.1146/annurev.biochem.72.121801.161800.
   PubMed Web of Science ®Google Scholar
• Brailoiu E, Rahman T, Churamani D, Prole DL, Brailoiu GC, Hooper R, Taylor CW, Patel S. 2010. An NAADP-gated two-pore channel targeted to the plasma membrane uncouples triggering from amplifying Ca2+ signals. J. Biol. Chem. 285:38511–38516. http://dx.doi.org/10.1074/jbc.M110.162073.
   PubMed Web of Science ®Google Scholar
• Morgan AJ, Galione A. 2014. Two-pore channels (TPCs): current controversies. Bioessays 36:173–183. http://dx.doi.org/10.1002/bies.201300118.
   PubMedGoogle Scholar
• Galione A, Morgan AJ, Arredouani A, Davis LC, Rietdorf K, Ruas M, Parrington J. 2010. NAADP as an intracellular messenger regulating lysosomal calcium-release channels. Biochem. Soc. Trans. 38:1424–1431. http://dx.doi.org/10.1042/BST0381424.
   PubMedGoogle Scholar
• Hooper R, Churamani D, Brailoiu E, Taylor CW, Patel S. 2011. Membrane topology of NAADP-sensitive two-pore channels and their regulation by N-linked glycosylation. J. Biol. Chem. 286:9141–9149. http://dx.doi.org/10.1074/jbc.M110.189985.
   PubMed Web of Science ®Google Scholar
• 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. 2010. TPC2 is a novel NAADP-sensitive Ca2+ release channel, operating as a dual sensor of luminal pH and Ca2+. J. Biol. Chem. 285:35039–35046. http://dx.doi.org/10.1074/jbc.M110.156927.
   PubMed Web of Science ®Google Scholar
• Schieder M, Rötzer K, Brüggemann A, Biel M, Wahl-Schott CA. 2010. Characterization of two-pore channel 2 (TPCN2)-mediated Ca2+ currents in isolated lysosomes. J. Biol. Chem. 285:21219–21222. http://dx.doi.org/10.1074/jbc.C110.143123.
   PubMed Web of Science ®Google Scholar
• Rybalchenko V, Ahuja M, Coblentz J, Churamani D, Patel S, Kiselyov K, Muallem S. 2012. Membrane potential regulates nicotinic acid adenine dinucleotide phosphate (NAADP) dependence of the pH- and Ca2+-sensitive organellar two-pore channel TPC1. J. Biol. Chem. 287:20407–20416. http://dx.doi.org/10.1074/jbc.M112.359612.
   PubMedGoogle Scholar
• Cang C, Bekele B, Ren D. 2014. The voltage-gated sodium channel TPC1 confers endolysosomal excitability. Nat. Chem. Biol. 10:463–469. http://dx.doi.org/10.1038/nchembio.1522.
   PubMed Web of Science ®Google Scholar
• Pitt SJ, Lam AKM, Rietdorf K, Galione A, Sitsapesan R. 2014. Reconstituted human TPC1 is a proton-permeable ion channel and is activated by NAADP or Ca2+. Sci. Signal. 7:ra46. http://dx.doi.org/10.1126/scisignal.2004854.
   PubMedGoogle Scholar
• Jha A, Ahuja M, Patel S, Brailoiu E, Muallem S. 2014. Convergent regulation of the lysosomal two-pore channel-2 by Mg2+, NAADP, PI(3,5)P2 and multiple protein kinases. EMBO J. 33:501–511. http://dx.doi.org/10.1002/embj.201387035.
   PubMedGoogle Scholar
• Cang C, Zhou Y, Navarro B, Seo Y, Aranda K, Shi L, Battaglia-Hsu S, Nissim I, Clapham DE, Ren D. 2013. mTOR regulates lysosomal ATP-sensitive two-pore Na+ channels to adapt to metabolic state. Cell 152:778–790. http://dx.doi.org/10.1016/j.cell.2013.01.023.
   PubMed Web of Science ®Google Scholar
• Wang X, Zhang X, Dong X, Samie M, Li X, Cheng X, Goschka A, Shen D, Zhou Y, Harlow J, Zhu MX, Clapham DE, Ren D, Xu H. 2012. TPC proteins are phosphoinositide-activated sodium-selective ion channels in endosomes and lysosomes. Cell 151:372–383. http://dx.doi.org/10.1016/j.cell.2012.08.036.
   PubMed Web of Science ®Google Scholar
• Aley PK, Mikolajczyk AM, Munz B, Churchill GC, Galione A, Berger F. 2010. Nicotinic acid adenine dinucleotide phosphate regulates skeletal muscle differentiation via action at two-pore channels. Proc. Natl. Acad. Sci. U. S. A. 107:19927–19932. http://dx.doi.org/10.1073/pnas.1007381107.
   PubMedGoogle Scholar
• Lu Y, Hao B-X, Graeff R, Wong CWM, Wu W-T, Yue J. 2013. Two pore channel 2 (TPC2) inhibits autophagosomal-lysosomal fusion by alkalinizing lysosomal pH. J. Biol. Chem. 288:24247–24263. http://dx.doi.org/10.1074/jbc.M113.484253.
   PubMed Web of Science ®Google Scholar
• Zhang Z-H, Lu Y-Y, Yue J. 2013. Two pore channel 2 differentially modulates neural differentiation of mouse embryonic stem cells. PLoS One 8:e66077. http://dx.doi.org/10.1371/journal.pone.0066077.
   PubMed Web of Science ®Google Scholar
• Notomi T, Ezura Y, Noda M. 2012. Identification of two-pore channel 2 as a novel regulator of osteoclastogenesis. J. Biol. Chem. 287:35057–35064. http://dx.doi.org/10.1074/jbc.M111.328930.
   PubMedGoogle Scholar
• Gómez-Suaga P, Luzón-Toro B, Churamani D, Zhang L, Bloor-Young D, Patel S, Woodman PG, Churchill GC, Hilfiker S. 2012. Leucine-rich repeat kinase 2 regulates autophagy through a calcium-dependent pathway involving NAADP. Hum. Mol. Genet. 21:511–525. http://dx.doi.org/10.1093/hmg/ddr481.
   PubMed Web of Science ®Google Scholar
• Garfield AS. 2010. Derivation of primary mouse embryonic fibroblast (PMEF) cultures, p 19–27. In Ward A, Tosh D (ed), Mouse cell culture. Humana Press, Totowa, NJ.
   Google Scholar
• Sarbassov DD, Guertin DA, Ali SM, Sabatini DM. 2005. Phosphorylation and regulation of Akt/PKB by the Rictor-mTOR complex. Science 307:1098–1101. http://dx.doi.org/10.1126/science.1106148.
   PubMed Web of Science ®Google Scholar
• Rottach A, Kremmer E, Nowak D, Leonhardt H, Cardoso MC. 2008. Generation and characterization of a rat monoclonal antibody specific for multiple red fluorescent proteins. Hybridoma 27:337–343. http://dx.doi.org/10.1089/hyb.2008.0031.
   PubMedGoogle Scholar
• Tugba Durlu-Kandilci N, Ruas M, Chuang K-T, Brading A, Parrington J, Galione A. 2010. TPC2 proteins mediate nicotinic acid adenine dinucleotide phosphate (NAADP)- and agonist-evoked contractions of smooth muscle. J. Biol. Chem. 285:24925–24932. http://dx.doi.org/10.1074/jbc.M110.129833.
   PubMedGoogle Scholar
• Brickman JM, Tsakiridis A, To C, Stanford WL. 2010. A wider context for gene trap mutagenesis. Methods Enzymol. 477:271–295. http://dx.doi.org/10.1016/S0076-6879(10)77014-2.
   PubMedGoogle Scholar
• Kawaji H, Kasukawa T, Fukuda S, Katayama S, Kai C, Kawai J, Carninci P, Hayashizaki Y. 2006. CAGE basic/analysis databases: the CAGE resource for comprehensive promoter analysis. Nucleic Acids Res. 34:D632–D636. http://dx.doi.org/10.1093/nar/gkj034.
   PubMedGoogle Scholar
• Sakabe NJ, Nobrega MA. 2010. Genome-wide maps of transcription regulatory elements. Wiley Interdiscip. Rev. Syst. Biol. Med. 2:422–437. http://dx.doi.org/10.1002/wsbm.70.
   PubMedGoogle Scholar
• Lin-Moshier Y, Walseth TF, Churamani D, Davidson SM, Slama JT, Hooper R, Brailoiu E, Patel S, Marchant JS. 2012. Photoaffinity labeling of nicotinic acid adenine dinucleotide phosphate (NAADP) targets in mammalian cells. J. Biol. Chem. 287:2296–2307. http://dx.doi.org/10.1074/jbc.M111.305813.
   PubMedGoogle Scholar
• Arndt L, Castonguay J, Arlt E, Meyer D, Hassan S, Borth H, Zierler S, Wennemuth G, Breit A, Biel M, Wahl-Schott C, Gudermann T, Klugbauer N, Boekhoff I. 2014. NAADP and the two-pore channel protein 1 participate in the acrosome reaction in mammalian spermatozoa. Mol. Biol. Cell 25:948–964. http://dx.doi.org/10.1091/mbc.E13-09-0523.
   PubMedGoogle Scholar
• Hebert DN, Garman SC, Molinari M. 2005. The glycan code of the endoplasmic reticulum: asparagine-linked carbohydrates as protein maturation and quality-control tags. Trends Cell Biol. 15:364–370. http://dx.doi.org/10.1016/j.tcb.2005.05.007.
   PubMed Web of Science ®Google Scholar
• Rietdorf K, Funnell TM, Ruas M, Heinemann J, Parrington J, Galione A. 2011. Two-pore channels form homo- and heterodimers. J. Biol. Chem. 286:37058–37062. http://dx.doi.org/10.1074/jbc.C111.289835.
   PubMedGoogle Scholar
• Mindell JA. 2012. Lysosomal acidification mechanisms. Annu. Rev. Physiol. 74:69–86. http://dx.doi.org/10.1146/annurev-physiol-012110-142317.
   PubMed Web of Science ®Google Scholar
• Goldberg B, Green H. 1964. An analysis of collagen secretion by established mouse fibroblast lines. J. Cell Biol. 22:227–258. http://dx.doi.org/10.1083/jcb.22.1.227.
   PubMed Web of Science ®Google Scholar
• Cornell R. 1970. Ultrastructural variants among peripheral vesicles and vacuoles of murine embryo cell strains. Exp. Cell Res. 59:177–185. http://dx.doi.org/10.1016/0014-4827(70)90589-6.
   PubMedGoogle Scholar
• Tuffery AA, Baker RSU. 1973. Alterations of mouse embryo cells during in vitro aging. Exp. Cell Res. 76:186–190. http://dx.doi.org/10.1016/0014-4827(73)90434-5.
   PubMedGoogle Scholar
• Wernick NLB, Chinnapen DJ-F, Cho JA, Lencer WI. 2010. Cholera toxin: an intracellular journey into the cytosol by way of the endoplasmic reticulum. Toxins 2:310–325. http://dx.doi.org/10.3390/toxins2030310.
   PubMed Web of Science ®Google Scholar
• Karlsson P, Droce A, Moser JM, Cuhlmann S, Padilla CO, Heimann P, Bartsch JW, Fuchtbauer A, Fuchtbauer E-M, Schmitt-John T. 2013. Loss of Vps54 function leads to vesicle traffic impairment, protein mis-sorting and embryonic lethality. Int. J. Mol. Sci. 14:10908–10925. http://dx.doi.org/10.3390/ijms140610908.
   PubMedGoogle Scholar
• Schmitt-John T, Drepper C, Mußmann A, Hahn P, Kuhlmann M, Thiel C, Hafner M, Lengeling A, Heimann P, Jones JM, Meisler MH, Jockusch H. 2005. Mutation of Vps54 causes motor neuron disease and defective spermiogenesis in the wobbler mouse. Nat. Genet. 37:1213–1215. http://dx.doi.org/10.1038/ng1661.
   PubMed Web of Science ®Google Scholar
• Hutagalung AH, Novick PJ. 2011. Role of Rab GTPases in membrane traffic and cell physiology. Physiol. Rev. 91:119–149. http://dx.doi.org/10.1152/physrev.00059.2009.
   PubMed Web of Science ®Google Scholar
• Yang M, Chen T, Han C, Li N, Wan T, Cao X. 2004. Rab7b, a novel lysosome-associated small GTPase, is involved in monocytic differentiation of human acute promyelocytic leukemia cells. Biochem. Biophys. Res. Commun. 318:792–799. http://dx.doi.org/10.1016/j.bbrc.2004.04.115.
   PubMedGoogle Scholar
• Progida C, Cogli L, Piro F, Luca AD, Bakke O, Bucci C. 2010. Rab7b controls trafficking from endosomes to the TGN. J. Cell Sci. 123:1480–1491. http://dx.doi.org/10.1242/jcs.051474.
   PubMed Web of Science ®Google Scholar
• Mukhopadhyay S, Linstedt AD. 2013. Retrograde trafficking of AB5 toxins: mechanisms to therapeutics. J. Mol. Med. 91:1131–1141. http://dx.doi.org/10.1007/s00109-013-1048-7.
   PubMedGoogle Scholar
• Goh LK, Sorkin A. 2013. Endocytosis of receptor tyrosine kinases. Cold Spring Harb. Perspect. Biol. 5:a017459.
   PubMed Web of Science ®Google Scholar
• Huang M, DuHadaway JB, Prendergast GC, Laury-Kleintop LD. 2007. RhoB regulates PDGFR-β trafficking and signaling in vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 27:2597–2605. http://dx.doi.org/10.1161/ATVBAHA.107.154211.
   PubMedGoogle Scholar