The Two-pore channel (TPC) interactome unmasks isoform-specific roles for TPCs in endolysosomal morphology and cell pigmentation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 36, 2014, Pages 13087-13092

  Lin Moshier, Yaping ^a   Keebler, Michael V ^a   Hooper, Robert ^b   Boulware, Michael J ^a   Liu, Xiaolong ^a   Churamani, Dev ^b   Abood, Mary E ^c   Walseth, Timothy F ^a   Brailoiu, Eugen ^c   Patel, Sandip ^b   Marchant, Jonathan S ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Ca2+signaling; Lysosome; Xenopus

Indexed keywords

CALCIUM CHANNEL; ISOPROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; NICOTINIC ACID ADENINE DINUCLEOTIDE PHOSPHATE; PROTEIN BINDING; RAB PROTEIN; TPCN1 PROTEIN, HUMAN; TPCN2 PROTEIN, HUMAN;

AFFINITY CHROMATOGRAPHY; ANALOGS AND DERIVATIVES; ANIMAL; CALCIUM SIGNALING; CELL PROLIFERATION; ENDOSOME; HEK293 CELL LINE; HUMAN; LYSOSOME; METABOLISM; PIGMENTATION; REPRODUCIBILITY; XENOPUS;

ANIMALS; CALCIUM CHANNELS; CALCIUM SIGNALING; CELL PROLIFERATION; CHROMATOGRAPHY, AFFINITY; ENDOSOMES; HEK293 CELLS; HUMANS; LYSOSOMES; NADP; PIGMENTATION; PROTEIN BINDING; PROTEIN ISOFORMS; RAB GTP-BINDING PROTEINS; REPRODUCIBILITY OF RESULTS; XENOPUS;

EID: 84907001175     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1407004111     Document Type: Article

References (57)

1. Zakon HH (2012) Adaptive evolution of voltage-gated sodium channels: The first 800 million years. Proc Natl Acad Sci USA 109(Suppl 1):10619-10625.
2. Brailoiu E, et al. (2009) Essential requirement for two-pore channel 1 in NAADP-mediated calcium signaling. J Cell Biol 186(2):201- 209.
3. Calcraft PJ, et al. (2009) NAADP mobilizes calcium from acidic organelles through two-pore channels. Nature 459(7246):596-600.
4. 2+. J Biol Chem 285(45):35039-35046.
5. 2+signals. J Biol Chem 285(49): 38511-38516.
6. 2+currents in isolated lysosomes. J Biol Chem 285(28):21219-21222.
7. 2+) signaling and endolysosomal trafficking. Curr Biol 20(8):703-709.
8. Lee HC (2005) Nicotinic acid adenine dinucleotide phosphate (NAADP)-mediated calcium signaling. J Biol Chem 280(40):33693-33696.
9. 2+signalling in health and disease. Biochem J 439(3):349-374.
10. Wang X, et al. (2012) TPC proteins are phosphoinositide- activated sodium-selective ion channels in endosomes and lysosomes. Cell 151(2):372-383.
11. Cang C, et al. (2013) mTOR regulates lysosomal ATP-sensitive two-pore Na(+) channels to adapt to metabolic state. Cell 152(4):778-790.
12. Morgan AJ, Galione A (2014) Two-pore channels (TPCs): Current controversies. Bio-Essays 36(2):173-183.
13. Marchant JS, Patel S (2013) Questioning regulation of two-pore channels by NAADP. Messenger (Los Angel) 2(2):113-119.
14. 2+signaling upon lysosome proliferation. J Biol Chem 285(18):13321-13325.
15. Schmidt TG, Skerra A (2007) The Strep-tag system for one-step purification and high-affinity detection or capturing of proteins. Nat Protoc 2(6):1528-1535.
16. Lam AK, Galione A, Lai FA, Zissimopoulos S (2013) Hax-1 identified as a two-pore channel (TPC)-binding protein. FEBS Lett 587(23):3782-3786.
17. Demaegd D, et al. (2013) Newly characterized Golgi-localized family of proteins is involved in calcium and pH homeostasis in yeast and human cells. Proc Natl Acad Sci USA 110(17):6859-6864.
18. Fujii Y, et al. (2012) Surf4 modulates STIM1-dependent calcium entry. Biochem Biophys Res Commun 422(4):615-620.
19. Zhang S, et al. (2006) Distinct role of the N-terminal tail of the Na,K-ATPase catalytic subunit as a signal transducer. J Biol Chem 281(31):21954-21962.
20. 3) signaling in C. elegans. Curr Biol 12(11): 951-956.
21. Zerial M, McBride H (2001) Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2(2):107-117.
22. Hutagalung AH, Novick PJ (2011) Role of Rab GTPases in membrane traffic and cell physiology. Physiol Rev 91(1):119-149.
23. Rink J, Ghigo E, Kalaidzidis Y, Zerial M (2005) Rab conversion as a mechanism of progression from early to late endosomes. Cell 122(5):735-749.
24. Bucci C, Thomsen P, Nicoziani P, McCarthy J, van Deurs B (2000) Rab7: A key to lysosome biogenesis. Mol Biol Cell 11(2):467- 480.
25. Saxena SK, Kaur S (2006) Regulation of epithelial ion channels by Rab GTPases. Biochem Biophys Res Commun 351(3):582-587.
26. v2 channel nano-environments in the mammalian brain. Proc Natl Acad Sci USA 107(34):14950-14957.
27. Zhang H, Cuevas J (2002) Sigma receptors inhibit high-voltage-activated calcium channels in rat sympathetic and parasympathetic neurons. J Neurophysiol 87(6):2867-2879.
28. Su TP, Hayashi T, Maurice T, Buch S, Ruoho AE (2010) The sigma-1 receptor chaperone as an inter-organelle signaling modulator. Trends Pharmacol Sci 31(12):557- 566.
29. Xu J, et al. (2011) Identification of the PGRMC1 protein complex as the putative sigma-2 receptor binding site. Nat Commun 2:380.
30. Zeng C, et al. (2007) Subcellular localization of sigma-2 receptors in breast cancer cells using two-photon and confocal microscopy. Cancer Res 67(14):6708-6716.
31. Ostenfeld MS, et al. (2005) Effective tumor cell death by sigma-2 receptor ligand siramesine involves lysosomal leakage and oxidative stress. Cancer Res 65(19):8975-8983.
32. Vilner BJ, Bowen WD (2000) Modulation of cellular calcium by sigma-2 receptors: Release from intracellular stores in human SK-N-SH neuroblastoma cells. J Pharmacol Exp Ther 292(3):900-911.
33. He P, et al. (2009) High-throughput functional screening for autophagy-related genes and identification of TM9SF1 as an autophagosome-inducing gene. Autophagy 5(1):52-60.
34. Tang HW, et al. (2011) Atg1-mediated myosin II activation regulates autophagosome formation during starvation-induced autophagy. EMBO J 30(4):636-651.
35. Ghislat G, Knecht E (2012) New Ca(2+)-dependent regulators of autophagosome maturation. Commun Integr Biol 5(4):308-311.
36. BasuRay S, Mukherjee S, Romero E, Wilson MC, Wandinger-Ness A (2010) Rab7 mutants associated with Charcot-Marie-Tooth disease exhibit enhanced NGF-stimulated signaling. PLoS ONE 5(12):e15351.
37. Brailoiu E, et al. (2005) Nicotinic acid adenine dinucleotide phosphate potentiates neurite outgrowth. J Biol Chem 280(7):5646-5650.
38. Gutierrez MG, Munafó DB, Berón W, Colombo MI (2004) Rab7 is required for the normal progression of the autophagic pathway in mammalian cells. J Cell Sci 117(Pt 13):2687-2697.
39. Pereira GJ, et al. (2011) Nicotinic acid adenine dinucleotide phosphate (NAADP) regulates autophagy in cultured astrocytes. J Biol Chem 286(32):27875-27881.
40. Ohbayashi N, Fukuda M (2012) Role of Rab family GTPases and their effectors in melanosomal logistics. J Biochem 151(4):343-351.
41. Sulem P, et al. (2008) Two newly identified genetic determinants of pigmentation in Europeans. Nat Genet 40(7):835-837.
42. Fukuda M, Kanno E, Ishibashi K, Itoh T (2008) Large scale screening for novel rab effectors reveals unexpected broad Rab binding specificity. Mol Cell Proteomics 7(6):1031-1042.
43. Subramanian VS, Marchant JS, Parker I, Said HM (2001) Intracellular trafficking/membrane targeting of human reduced folate carrier expressed in Xenopus oocytes. Am J Physiol Gastrointest Liver Physiol 281(6):G1477-G1486.
44. Agola JO, et al. (2012) A competitive nucleotide binding inhibitor: In vitro characterization of Rab7 GTPase inhibition. ACS Chem Biol 7(6):1095-1108.
45. 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(11):9141-9149.
46. Ward HH, et al. (2011) A conserved signal and GTPase complex are required for the ciliary transport of polycystin-1. Mol Biol Cell 22(18):3289-3305.
47. Hider JL, et al. (2013) Exploring signatures of positive selection in pigmentation candidate genes in populations of East Asian ancestry. BMC Evol Biol 13:150.
48. Mukhopadhyay A, Funato K, Stahl PD (1997) Rab7 regulates transport from early to late endocytic compartments in Xenopus oocytes. J Biol Chem 272(20):13055-13059.
49. Dong XP, et al. (2010) PI(3,5)P(2) controls membrane trafficking by direct activation of mucolipin Ca(2+) release channels in the endolysosome. Nat Commun 1:38.
50. 2and multiple protein kinases. EMBO J 33(5):501-511.
51. Pryor PR, Mullock BM, Bright NA, Gray SR, Luzio JP (2000) The role of intraorganellar Ca(2+) in late endosome-lysosome heterotypic fusion and in the reformation of lysosomes from hybrid organelles. J Cell Biol 149(5):1053- 1062.
52. Parkinson K, et al. (2014) Calcium-dependent regulation of Rab activation and vesicle fusion by an intracellular P2X ion channel. Nat Cell Biol 16(1):87-98.
53. Lesnick TG, et al. (2007) A genomic pathway approach to a complex disease: Axon guidance and Parkinson disease. PLoS Genet 3(6):e98.
54. Kim JM, et al. (2011) SNPs in axon guidance pathway genes and susceptibility for Parkinson's disease in the Korean population. J Hum Genet 56(2):125-129.
55. Gómez-Suaga P, Hilfiker S (2012) LRRK2 as a modulator of lysosomal calcium homeostasis with downstream effects on autophagy. Autophagy 8(4):692-693.
56. Lin-Moshier Y, Marchant JS (2013) Nuclear microinjection to assess how heterologously expressed proteins impact Ca2+ signals in Xenopus oocytes. Cold Spring Harb Protoc, 10.1101/pdb.prot072785.
57. Brailoiu GC, Oprea TI, Zhao P, Abood ME, Brailoiu E (2011) Intracellular cannabinoid type 1 (CB1) receptors are activated by anandamide. J Biol Chem 286(33):29166-29174.