Nicotinic Acid Adenine Dinucleotide Phosphate (NAADP) Induces Intracellular Ca2+ Release through the Two-Pore Channel TPC1 in Metastatic Colorectal Cancer Cells

Cancers - Tập 11 Số 4 - Trang 542
Pawan Faris1,2, Giorgia Pellavio3, Federica Ferulli4, Francesca Di Nezza5, Mudhir Sabir Shekha6,2, Dmitry Lim7, Marcello Maestri8,9, Germano Guerra5, Luigi Ambrosone5, Paolo Pedrazzoli10, Umberto Laforenza3, Daniela Montagna8,4, Francesco Moccia1
1Laboratory of General Physiology, Department of Biology and Biotechnology “L. Spallanzani”, University of Pavia, 27100 Pavia, Italy
2Research Centre, Salahaddin University-Erbil, 44001 Erbil, Kurdistan-Region of Iraq, Iraq
3Human Physiology Unit, via Forlanini 6, Department of Molecular Medicine, University of Pavia, 27100 Pavia, Italy
4Laboratory of Immunology Transplantation, Foundation IRCCS Policlinico San Matteo, 27100 Pavia, Italy
5Department of Medicine and Health Sciences ”Vincenzo Tiberio”, University of Molise, 86100, Campobasso, Italy
6Department of Pathological Analysis, College of Science, Knowledge University, 074016 Erbil, Kurdistan-Region of Iraq, Iraq
7Department of Pharmaceutical Sciences, Università del Piemonte Orientale, 28100 Novara, Italy
8Department of Sciences Clinic-Surgical, Diagnostic and Pediatric, University of Pavia, 27100 Pavia, Italy
9Unit of General Surgery, Foundation IRCCS Policlinico San Matteo, 27100 Pavia, Italy
10Medical Oncology, oundation IRCCS Policlinico San Matteo, 27100 Pavia, Italy

Tóm tắt

Nicotinic acid adenine dinucleotide phosphate (NAADP) gates two-pore channels 1 and 2 (TPC1 and TPC2) to elicit endo-lysosomal (EL) Ca2+ release. NAADP-induced EL Ca2+ signals may be amplified by the endoplasmic reticulum (ER) through the Ca2+-induced Ca2+ release mechanism (CICR). Herein, we aimed at assessing for the first time the role of EL Ca2+ signaling in primary cultures of human metastatic colorectal carcinoma (mCRC) by exploiting Ca2+ imaging and molecular biology techniques. The lysosomotropic agent, Gly-Phe β-naphthylamide (GPN), and nigericin, which dissipates the ΔpH which drives Ca2+ refilling of acidic organelles, caused massive Ca2+ release in the presence of a functional inositol-1,4,5-trisphosphate (InsP3)-sensitive ER Ca2+ store. Liposomal delivery of NAADP induced a transient Ca2+ release that was reduced by GPN and NED-19, a selective TPC antagonist. Pharmacological and genetic manipulations revealed that the Ca2+ response to NAADP was triggered by TPC1, the most expressed TPC isoform in mCRC cells, and required ER-embedded InsP3 receptors. Finally, NED-19 and genetic silencing of TPC1 reduced fetal calf serum-induced Ca2+ signals, proliferation, and extracellular signal-regulated kinase and Akt phoshorylation in mCRC cells. These data demonstrate that NAADP-gated TPC1 could be regarded as a novel target for alternative therapies to treat mCRC.

Từ khóa


Tài liệu tham khảo

Berridge, 2003, Calcium signalling: Dynamics, homeostasis and remodelling, Nat. Rev. Mol. Cell Biol., 4, 517, 10.1038/nrm1155

Samanta, 2017, Spatial Ca(2+) profiling: Decrypting the universal cytosolic Ca(2+) oscillation, J. Physiol., 595, 3053, 10.1113/JP272860

Zuccolo, 2018, Stromal cell-derived factor-1alpha promotes endothelial colony-forming cell migration through the Ca(2+)-dependent activation of the extracellular signal-regulated kinase 1/2 and phosphoinositide 3-kinase/AKT pathways, Stem Cells Dev., 27, 23, 10.1089/scd.2017.0114

Cardenas, 2016, Selective vulnerability of cancer cells by inhibition of Ca(2+) transfer from endoplasmic reticulum to mitochondria, Cell Rep., 15, 219, 10.1016/j.celrep.2016.03.045

Prevarskaya, 2018, Ion channels in cancer: Are cancer hallmarks oncochannelopathies?, Physiol. Rev., 98, 559, 10.1152/physrev.00044.2016

Lam, 2013, The endoplasmic reticulum and junctional membrane communication during calcium signaling, Biochim. Biophys. Acta, 1833, 2542, 10.1016/j.bbamcr.2013.06.004

Patel, 2010, Acidic calcium stores open for business: Expanding the potential for intracellular Ca2+ signaling, Trends Cell Biol., 20, 277, 10.1016/j.tcb.2010.02.003

Missiaen, 2007, Calcium in the Golgi apparatus, Cell Calcium, 41, 405, 10.1016/j.ceca.2006.11.001

Berridge, 2002, The endoplasmic reticulum: A multifunctional signaling organelle, Cell Calcium, 32, 235, 10.1016/S0143416002001823

Morgan, 2011, Molecular mechanisms of endolysosomal Ca2+ signalling in health and disease, Biochem. J., 439, 349, 10.1042/BJ20110949

Galione, 2015, A primer of NAADP-mediated Ca(2+) signalling: From sea urchin eggs to mammalian cells, Cell Calcium, 58, 27, 10.1016/j.ceca.2014.09.010

Morgan, 2016, Ca2+ dialogue between acidic vesicles and ER, Biochem. Soc. Trans., 44, 546, 10.1042/BST20150290

Melchionda, 2016, Ca2+/H+ exchange by acidic organelles regulates cell migration in vivo, J. Cell Biol., 212, 803, 10.1083/jcb.201510019

Ronco, 2015, A novel Ca(2)(+)-mediated cross-talk between endoplasmic reticulum and acidic organelles: Implications for NAADP-dependent Ca(2)(+) signalling, Cell Calcium, 57, 89, 10.1016/j.ceca.2015.01.001

Yang, 2019, Release and uptake mechanisms of vesicular Ca(2+) stores, Protein Cell, 10, 8, 10.1007/s13238-018-0523-x

Zong, 2009, The two-pore channel TPCN2 mediates NAADP-dependent Ca(2+)-release from lysosomal stores, Pflug. Arch., 458, 891, 10.1007/s00424-009-0690-y

Ruas, 2015, Expression of Ca(2)(+)-permeable two-pore channels rescues NAADP signalling in TPC-deficient cells, EMBO J., 34, 1743, 10.15252/embj.201490009

Brailoiu, 2009, Essential requirement for two-pore channel 1 in NAADP-mediated calcium signaling, J. Cell Biol., 186, 201, 10.1083/jcb.200904073

Calcraft, 2009, NAADP mobilizes calcium from acidic organelles through two-pore channels, Nature, 459, 596, 10.1038/nature08030

Guse, 2012, Linking NAADP to ion channel activity: A unifying hypothesis, Sci. Signal., 5, pe18, 10.1126/scisignal.2002890

Wolf, 2015, Frontrunners of T cell activation: Initial, localized Ca2+ signals mediated by NAADP and the type 1 ryanodine receptor, Sci. Signal., 8, ra102, 10.1126/scisignal.aab0863

Penny, 2015, Coupling acidic organelles with the ER through Ca(2)(+) microdomains at membrane contact sites, Cell Calcium, 58, 387, 10.1016/j.ceca.2015.03.006

Ruas, 2010, Purified TPC isoforms form NAADP receptors with distinct roles for Ca(2+) signaling and endolysosomal trafficking, Curr. Biol., 20, 703, 10.1016/j.cub.2010.02.049

Moccia, 2006, NAADP and InsP3 play distinct roles at fertilization in starfish oocytes, Dev. Biol., 294, 24, 10.1016/j.ydbio.2006.02.011

Favia, 2014, VEGF-induced neoangiogenesis is mediated by NAADP and two-pore channel-2-dependent Ca2+ signaling, Proc. Natl. Acad. Sci. USA, 111, E4706, 10.1073/pnas.1406029111

Zuccolo, 2016, Arachidonic acid-evoked Ca2+ signals promote nitric oxide release and proliferation in human endothelial colony forming cells, Vascul. Pharmacol., 87, 159, 10.1016/j.vph.2016.09.005

Zuccolo, 2019, Muscarinic M5 receptors trigger acetylcholine-induced Ca(2+) signals and nitric oxide release in human brain microvascular endothelial cells, J. Cell. Physiol., 234, 4540, 10.1002/jcp.27234

Brailoiu, 2005, Nicotinic acid adenine dinucleotide phosphate potentiates neurite outgrowth, J. Biol. Chem., 280, 5646, 10.1074/jbc.M408746200

Pereira, 2017, Glutamate induces autophagy via the two-pore channels in neural cells, Oncotarget, 8, 12730, 10.18632/oncotarget.14404

Arredouani, 2015, Nicotinic acid adenine dinucleotide phosphate (NAADP) and endolysosomal two-pore channels modulate membrane excitability and stimulus-secretion coupling in mouse pancreatic beta cells, J. Biol. Chem., 290, 21376, 10.1074/jbc.M115.671248

Zuccolo, 2019, Glutamate triggers intracellular Ca(2+) oscillations and nitric oxide release by inducing NAADP-and InsP3-dependent Ca(2+) release in mouse brain endothelial cells, J. Cell. Physiol., 234, 3538, 10.1002/jcp.26953

Patel, 2018, Two-pore channels and disease, Biochim. Biophys. Acta Mol. Cell Res., 1865, 1678, 10.1016/j.bbamcr.2018.05.004

Sterea, 2018, The hidden potential of lysosomal ion channels: A new era of oncogenes, Cell Calcium, 72, 91, 10.1016/j.ceca.2018.02.006

Grimm, C., Bartel, K., Vollmar, A.M., and Biel, M. (2018). Endolysosomal cation channels and cancer-a link with great potential. Pharmaceuticals (Basel), 11.

Jahidin, 2016, Differential effects of two-pore channel protein 1 and 2 silencing in MDA-MB-468 breast cancer cells, Biochem. Biophys. Res. Commun., 477, 731, 10.1016/j.bbrc.2016.06.127

Nguyen, 2017, Two-pore channel function is crucial for the migration of invasive cancer cells, Cancer Res., 77, 1427, 10.1158/0008-5472.CAN-16-0852

Favia, 2016, NAADP-dependent Ca(2+) signaling controls melanoma progression, metastatic dissemination and neoangiogenesis, Sci. Rep., 6, 18925, 10.1038/srep18925

Turin, 2014, In vitro efficient expansion of tumor cells deriving from different types of human tumor samples, Med. Sci., 2, 70

Zuccolo, 2018, Stim and Orai mediate constitutive Ca(2+) entry and control endoplasmic reticulum Ca(2+) refilling in primary cultures of colorectal carcinoma cells, Oncotarget, 9, 31098, 10.18632/oncotarget.25785

Morgan, 2013, Bidirectional Ca(2)(+) signaling occurs between the endoplasmic reticulum and acidic organelles, J. Cell Biol., 200, 789, 10.1083/jcb.201204078

Kilpatrick, 2013, Direct mobilisation of lysosomal Ca2+ triggers complex Ca2+ signals, J. Cell Sci., 126, 60, 10.1242/jcs.118836

McGuinness, 2007, The lysosome or lysosome-related organelle may serve as a Ca2+ store in the boutons of hippocampal pyramidal cells, Neuropharmacology, 52, 126, 10.1016/j.neuropharm.2006.07.029

Pandey, 2009, Recruitment of NAADP-sensitive acidic Ca2+ stores by glutamate, Biochem. J., 422, 503, 10.1042/BJ20090194

Cancela, 2002, Transformation of local Ca2+ spikes to global Ca2+ transients: The combinatorial roles of multiple Ca2+ releasing messengers, EMBO J., 21, 909, 10.1093/emboj/21.5.909

Penny, 2014, A computational model of lysosome-ER Ca2+ microdomains, J. Cell Sci., 127, 2934

Moccia, 2016, Targeting Stim and Orai proteins as an alternative approach in anticancer therapy, Curr. Med. Chem., 23, 3450, 10.2174/0929867323666160607111220

Dragoni, 2011, Vascular endothelial growth factor stimulates endothelial colony forming cells proliferation and tubulogenesis by inducing oscillations in intracellular Ca2+ concentration, Stem Cells, 29, 1898, 10.1002/stem.734

Zuccolo, 2017, Liposomes as a putative tool to investigate NAADP signaling in vasculogenesis, J. Cell. Biochem., 118, 3722, 10.1002/jcb.26019

Azimi, 2018, Pharmacological inhibition of store-operated calcium entry in MDA-MB-468 basal A breast cancer cells: Consequences on calcium signalling, cell migration and proliferation, Cell. Mol. Life Sci., 75, 4525, 10.1007/s00018-018-2904-y

Yang, 2009, Orai1 and STIM1 are critical for breast tumor cell migration and metastasis, Cancer Cell, 15, 124, 10.1016/j.ccr.2008.12.019

Zhu, 2014, Elevated Orai1 expression mediates tumor-promoting intracellular Ca2+ oscillations in human esophageal squamous cell carcinoma, Oncotarget, 5, 3455, 10.18632/oncotarget.1903

Kinnear, 2008, Lysosomes co-localize with ryanodine receptor subtype 3 to form a trigger zone for calcium signalling by NAADP in rat pulmonary arterial smooth muscle, Cell Calcium, 44, 190, 10.1016/j.ceca.2007.11.003

Kelu, 2015, Two-pore channel 2 activity is required for slow muscle cell-generated Ca(2+) signaling during myogenesis in intact zebrafish, Int. J. Dev. Biol., 59, 313, 10.1387/ijdb.150206am

Pitt, 2016, Exploring the biophysical evidence that mammalian two-pore channels are NAADP-activated calcium-permeable channels, J. Physiol., 594, 4171, 10.1113/JP270936

Davis, 2012, NAADP activates two-pore channels on T cell cytolytic granules to stimulate exocytosis and killing, Curr. Biol., 22, 2331, 10.1016/j.cub.2012.10.035

Jiang, 2013, Nicotinic acid adenine dinucleotide phosphate (NAADP) activates global and heterogeneous local Ca2+ signals from NAADP-and ryanodine receptor-gated Ca2+ stores in pulmonary arterial myocytes, J. Biol. Chem., 288, 10381, 10.1074/jbc.M112.423053

Monteith, 2017, The calcium-cancer signalling nexus, Nat. Rev. Cancer, 17, 367, 10.1038/nrc.2017.18

Moccia, F. (2018). Endothelial Ca(2+) Signaling and the Resistance to Anticancer Treatments: Partners in Crime. Int. J. Mol. Sci., 19.

Moccia, 2015, May the remodeling of the Ca(2)(+) toolkit in endothelial progenitor cells derived from cancer patients suggest alternative targets for anti-angiogenic treatment?, Biochim. Biophys. Acta, 1853, 1958, 10.1016/j.bbamcr.2014.10.024

Pinto, 2015, Calcium signaling and cell proliferation, Cell Signal., 27, 2139, 10.1016/j.cellsig.2015.08.006

Chalmers, 2018, ORAI channels and cancer, Cell Calcium, 74, 160, 10.1016/j.ceca.2018.07.011

Carrato, 2008, Adjuvant treatment of colorectal cancer, Gastrointest. Cancer Res., 2, S42

Turin, 2018, In vitro killing of colorectal carcinoma cells by autologous activated NK cells is boosted by anti-epidermal growth factor receptor-induced ADCC regardless of RAS mutation status, J. Immunother., 41, 190, 10.1097/CJI.0000000000000205

Bufalo, 2017, Physicochemical investigation of ultrasound effects on some steps of mink fur processing. A suggestion for improving the worker health and reducing the environmental impact, J. Clean. Prod., 143, 10, 10.1016/j.jclepro.2016.12.160

Laemmli, 1970, Cleavage of structural proteins during the assembly of the head of bacteriophage T4, Nature, 227, 680, 10.1038/227680a0

Bradford, 1976, A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding, Anal. Biochem., 72, 248, 10.1016/0003-2697(76)90527-3

Spano, 2013, Changes on lysosomal compartment during PMA-induced differentiation of THP-1 monocytic cells: Influence of type I and type IV collagens, Adv. Biosci. Biotechnol., 4, 8, 10.4236/abb.2013.48A3002