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A protein disulfide isomerase coordinates redox homeostasis and ER calcium regulation for optimal lytic cycle progression in Toxoplasma gondii
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Abstract
The endoplasmic reticulum (ER) maintains an oxidative environment that facilitates the formation of disulfide bonds, a critical process for proper protein folding. Protein disulfide isomerases (PDIs) are ER-resident enzymes that facilitate the formation, breakage, and rearrangement of disulfide bonds between cysteine residues, thereby stabilizing protein structures. Although PDIs are functionally diverse, they all contain at least 1 thioredoxin-like domain and most mediate disulfide exchange through their conserved CXXC motifs. The apicomplexan parasite, Toxoplasma gondii , infects approximately one-third of the world population, posing a significant risk to immunosuppressed individuals and unborn fetuses. The fast-replicating tachyzoite form engages in a lytic cycle, causing host tissue damage and contributing to pathogenesis. While approximately 26 PDIs are predicted to be present in T. gondii , their specific roles remain largely unexplored. In this study, we investigate TgPDIA3, a T. gondii PDI localized to the ER, along with several of its interacting protein substrates. We explore its role in ER redox activity and calcium sequestration and assess how these functions contribute to the parasite’s lytic cycle. IMPORTANCE: The lytic cycle of Toxoplasma gondii is critical for parasite dissemination and disease progression in the host. Calcium signaling plays a crucial role in driving these processes; however, the molecules that control calcium storage and release remain poorly understood. The endoplasmic reticulum, likely the largest calcium reservoir in T. gondii , has been understudied in the context of calcium signaling. Here, we uncover a direct link between ER redox regulation and calcium homeostasis, showing that ER redox activity can influence calcium signaling events that govern microneme protein maturation and secretion, parasite invasion, and replication. Our findings indicate that redox-dependent calcium regulation in the ER contributes to control of the parasite lytic cycle and reveals a previously unrecognized mechanism that may influence parasite virulence.
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Cites
Fiji: an open-source platform for biological-image analysis
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., et al. (2012) · Nature Methods · doi:10.1038/nmeth.2019 · Cited by 66,890
Highly accurate protein structure prediction with AlphaFold
Jumper, J., Evans, R., Pritzel, A., Green, T., Figurnov, M., Ronneberger, O., Tunyasuvunakool, K., Bates, R., Žídek, A., Potapenko, A., et al. (2021) · Nature · doi:10.1038/s41586-021-03819-2 · Cited by 43,764 · cited 1×
“Using AlphaFold predicted models (42, 43), we visualized the spatial orientation of TgPDIA3 catalytic motifs and found that both face inward toward each other (Fig.”
MEGA11: Molecular Evolutionary Genetics Analysis Version 11
Tamura, K., Stecher, G., & Kumar, S. (2021) · Molecular Biology and Evolution · doi:10.1093/molbev/msab120 · Cited by 22,403
Enzymatic assembly of DNA molecules up to several hundred kilobases
Gibson, D. G., Young, L., Chuang, R.-Y., Venter, J. C., Hutchison, C. A., & Smith, H. O. (2009) · Nature Methods · doi:10.1038/nmeth.1318 · Cited by 10,088
Ultrasensitive fluorescent proteins for imaging neuronal activity
Chen, T.-W., Wardill, T. J., Sun, Y., Pulver, S. R., Renninger, S. L., Baohan, A., Schreiter, E. R., Kerr, R. A., Orger, M. B., Jayaraman, V., et al. (2013) · Nature · doi:10.1038/nature12354 · Cited by 6,474
Clapham, D. E. (2007) · Cell · doi:10.1016/j.cell.2007.11.028 · Cited by 4,175
The PRIDE database at 20 years: 2025 update
Pérez‐Riverol, Y., Bandla, C., Kundu, D. J., Kamatchinathan, S., Bai, J., Hewapathirana, S., John, N. S., Prakash, A., Walzer, M., Wang, S., et al. (2024) · Nucleic Acids Research · doi:10.1093/nar/gkae1011 · Cited by 2,342
Varadi, M., Bertoni, D., Magana, P., Paramval, U., Pidruchna, I., Radhakrishnan, M., Tsenkov, M., Nair, S., Mirdita, M., Yeo, J., et al. (2024) · Nucleic Acids Research · doi:10.1093/nar/gkad1011 · Cited by 2,052 · cited 1×
“Using AlphaFold predicted models (42, 43), we visualized the spatial orientation of TgPDIA3 catalytic motifs and found that both face inward toward each other (Fig.”
Oxidized Redox State of Glutathione in the Endoplasmic Reticulum
Hwang, C., Sinskey, A. J., & Lodish, H. F. (1992) · Science · doi:10.1126/science.1523409 · Cited by 1,968
Endoplasmic Reticulum Stress and Oxidative Stress in Cell Fate Decision and Human Disease
Cao, S. S., & Kaufman, R. J. (2014) · Antioxidants and Redox Signaling · doi:10.1089/ars.2014.5851 · Cited by 1,412
Toxoplasmic Encephalitis in AIDS
Luft, B. J., & Remington, J. S. (1992) · Clinical Infectious Diseases · doi:10.1093/clinids/15.2.211 · Cited by 1,295
Toxoplasma gondii: transmission, diagnosis and prevention
Hill, D. E., & Dubey, J. P. (2002) · Clinical Microbiology and Infection · doi:10.1046/j.1469-0691.2002.00485.x · Cited by 1,212
Endoplasmic reticulum stress: molecular mechanism and therapeutic targets
Chen, X., Shi, C., He, M., Xiong, S., & Xia, X. (2023) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01570-w · Cited by 1,155
A Genome-wide CRISPR Screen in Toxoplasma Identifies Essential Apicomplexan Genes
Sidik, S. M., Huet, D., Ganesan, S. M., Huynh, M.-H., Wang, T., Nasamu, A. S., Thiru, P., Saeij, J. P. J., Carruthers, V. B., Niles, J. C., et al. (2016) · Cell · doi:10.1016/j.cell.2016.08.019 · Cited by 804
ER chaperones in mammalian development and human diseases
Ni, M., & Lee, A. S. (2007) · FEBS Letters · doi:10.1016/j.febslet.2007.04.045 · Cited by 751
Li, G., Mongillo, M., Chin, K., Harding, H. P., Ron, D., Marks, A. R., & Tabas, I. A. (2009) · The Journal of Cell Biology · doi:10.1083/jcb.200904060 · Cited by 622
Chapter 3: Molecular Tools for Genetic Dissection of the Protozoan Parasite Toxoplasma gondii
Roos, D. S., Donald, R. G. K., Morrissette, N. S., & Moulton, A. L. C. (1995) · Methods in cell biology · doi:10.1016/s0091-679x(08)61845-2 · Cited by 598
Lytic Cycle ofToxoplasma gondii
Black, M. W., & Boothroyd, J. C. (2000) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.64.3.607-623.2000 · Cited by 554
Proximity labeling in mammalian cells with TurboID and split-TurboID
Cho, K. F., Branon, T. C., Udeshi, N. D., Myers, S. A., Carr, S. A., & Ting, A. Y. (2020) · Nature Protocols · doi:10.1038/s41596-020-0399-0 · Cited by 534
The endoplasmic reticulum Ca2+ store: a view from the lumen
Meldolesi, J., & Pozzan, T. (1998) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(97)01143-2 · Cited by 525
Calcium microdomains: Organization and function
Berridge, M. J. (2006) · Cell Calcium · doi:10.1016/j.ceca.2006.09.002 · Cited by 525
Ca2+ signaling and calcium binding chaperones of the endoplasmic reticulum
Michalak, M., Parker, J. M. R., & Opas, M. (2002) · Cell Calcium · doi:10.1016/s0143416002001884 · Cited by 484
Kiss and spit: the dual roles of Toxoplasma rhoptries
Boothroyd, J. C., & Dubremetz, J. (2007) · Nature Reviews Microbiology · doi:10.1038/nrmicro1800 · Cited by 425
Higo, T., Hattori, M., Nakamura, T., Natsume, T., Michikawa, T., & Mikoshiba, K. (2005) · Cell · doi:10.1016/j.cell.2004.11.048 · Cited by 373
Mobilization of intracellular calcium stimulates microneme discharge in Toxoplasma gondii
Carruthers, V. B., & Sibley, L. D. (1999) · Molecular Microbiology · doi:10.1046/j.1365-2958.1999.01174.x · Cited by 359
Secretion of micronemal proteins is associated with toxoplasma invasion of host cells
Carruthers, V. B., Giddings, O. K., & Sibley, L. D. (1999) · Cellular Microbiology · doi:10.1046/j.1462-5822.1999.00023.x · Cited by 350
Fundamentals of Cellular Calcium Signaling: A PrimerPreprint
Bootman, M. D., & Bultynck, G. (2019) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a038802 · Cited by 343
Shedding light on disulfide bond formation: engineering a redox switch in green fluorescent protein
Østergaard, H., Henriksen, A., Hansen, F. G., & Winther, J. R. (2001) · The EMBO Journal · doi:10.1093/emboj/20.21.5853 · Cited by 333
Barylyuk, K., Kořený, L., Ke, H., Butterworth, S., Crook, O. M., Lassadi, I., Gupta, V., Tromer, E. C., Mourier, T., Stevens, T. J., et al. (2020) · Cell Host & Microbe · doi:10.1016/j.chom.2020.09.011 · Cited by 332
Lytic Cycle of Toxoplasma gondii: 15 Years Later
Blader, I. J., Coleman, B. I., Chen, C., & Gubbels, M. (2015) · Annual Review of Microbiology · doi:10.1146/annurev-micro-091014-104100 · Cited by 327
A critical role for extracellular protein disulfide isomerase during thrombus formation in mice
Cho, J., Furie, B. C., Coughlin, S. R., & Furie, B. (2008) · Journal of Clinical Investigation · doi:10.1172/jci34134 · Cited by 326
Shenton, D., & Grant, C. M. (2003) · Biochemical Journal · doi:10.1042/bj20030414 · Cited by 326
Dong, G., Wearsch, P. A., Peaper, D. R., Cresswell, P., & Reinisch, K. M. (2009) · Immunity · doi:10.1016/j.immuni.2008.10.018 · Cited by 294
Cai, H., Wang, C. C., & Tsou, C. L. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)31426-6 · Cited by 277
VEuPathDB: the eukaryotic pathogen, vector and host bioinformatics resource center in 2023
Álvarez-Jarreta, J., Amos, B., Aurrecoechea, C., Bah, S. Y., Barba, M., Barreto, A., Basenko, E. Y., Belnap, R., Blevins, A. S., Böhme, U., et al. (2023) · Nucleic Acids Research · doi:10.1093/nar/gkad1003 · Cited by 272
The development and biology of bradyzoites of toxoplasma gondii
Louis, M. W. (2000) · Frontiers in bioscience · doi:10.2741/weiss · Cited by 271
The human protein disulfide isomerase gene family
Galligan, J. J., & Petersen, D. R. (2012) · Human Genomics · doi:10.1186/1479-7364-6-6 · Cited by 270
Neglected Parasitic Infections in the United States: Toxoplasmosis
Jones, J. L., Parise, M. E., & Fiore, A. E. (2014) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.13-0722 · Cited by 268
Sheiner, L., Demerly, J. L., Poulsen, N., Beatty, W. L., Lucas, O., Behnke, M. S., White, M. W., & Striepen, B. (2011) · PLoS Pathogens · doi:10.1371/journal.ppat.1002392 · Cited by 252
Ca2+-dependent redox modulation of SERCA 2b by ERp57
Li, Y., & Camacho, P. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200307010 · Cited by 244
Protein disulfide isomerase a multifunctional protein with multiple physiological roles
Khan, H. A., & Mutus, B. (2014) · Frontiers in Chemistry · doi:10.3389/fchem.2014.00070 · Cited by 227
Palmitoylated TMX and calnexin target to the mitochondria‐associated membrane
Lynes, E. M., Bui, M., Yap, M. C., Benson, M. D., Schneider, B. L., Ellgaard, L., Berthiaume, L. G., & Simmen, T. (2011) · The EMBO Journal · doi:10.1038/emboj.2011.384 · Cited by 224
Differential Modulation of SERCA2 Isoforms by Calreticulin
John, L. M., Lechleiter, J. D., & Camacho, P. (1998) · The Journal of Cell Biology · doi:10.1083/jcb.142.4.963 · Cited by 215
Protein disulfide–isomerase, a folding catalyst and a redox-regulated chaperone
Wang, L., Wang, X., & Wang, C.-C. (2015) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2015.02.007 · Cited by 205
Genetic and Epigenetic Changes in Human Epithelial Cells Immortalized by Telomerase
Farwell, D. G., Shera, K. A., Koop, J. I., Bonnet, G. A., Matthews, C. P., Reuther, G. W., Coltrera, M. D., McDougall, J. K., & Klingelhutz, A. J. (2000) · The American Journal of Pathology · doi:10.1016/s0002-9440(10)65025-0 · Cited by 196
The Cdc48 machine in endoplasmic reticulum associated protein degradation
Wolf, D. H., & Stolz, A. (2011) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2011.09.002 · Cited by 190
Ramakrishnan, C., Maier, S., Walker, R. A., Rehrauer, H., Joekel, D. E., Winiger, R. R., Basso, W., Grigg, M. E., Hehl, A. B., Deplazes, P., et al. (2019) · Scientific Reports · doi:10.1038/s41598-018-37671-8 · Cited by 189
ER to Golgi-Dependent Protein Secretion: The Conventional Pathway
Viotti, C. (2016) · Methods in molecular biology · doi:10.1007/978-1-4939-3804-9_1 · Cited by 179
de Miranda, K. R., Pace, D. A., Cintrón, R., Rodrigues, J. C. F., Fang, J., Smith, A. N., Rohloff, P. J., Coelho, E., de Haas, F., de Souza, W., et al. (2010) · Molecular Microbiology · doi:10.1111/j.1365-2958.2010.07165.x · Cited by 174
Self-citationLovett, J. L., Marchesini, N., Moreno, S. N. J., & Sibley, L. D. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m202553200 · Cited by 171
Self-citationTMX1 determines cancer cell metabolism as a thiol-based modulator of ER–mitochondria Ca2+ flux
Raturi, A., Gutiérrez, T., Ortiz-Sandoval, C. G., Ruangkittisakul, A., Herrera-Cruz, M. S., Rockley, J. P., Gesson, K., Ourdev, D., Lou, P., Lucchinetti, E., et al. (2016) · The Journal of Cell Biology · doi:10.1083/jcb.201512077 · Cited by 154
Congenital Toxoplasmosis: A Review
Hampton, M. M. (2015) · Neonatal Network The Journal of Neonatal Nursing · doi:10.1891/0730-0832.34.5.274 · Cited by 153
The calcium signaling toolkit of the Apicomplexan parasites Toxoplasma gondii and Plasmodium spp
Lourido, S., & Moreno, S. N. J. (2015) · Cell Calcium · doi:10.1016/j.ceca.2014.12.010 · Cited by 152
Self-citationDistinct stress conditions result in aggregation of proteins with similar properties
Weids, A. J., Ibstedt, S., Tamás, M. J., & Grant, C. M. (2016) · Scientific Reports · doi:10.1038/srep24554 · Cited by 152
Crystal Structure of the bb′ Domains of the Protein Disulfide Isomerase ERp57
Kozlov, G., Määttänen, P., Schrag, J. D., Pollock, S., Cygler, M., Nagar, B., Thomas, D. Y., & Gehring, K. (2006) · Structure · doi:10.1016/j.str.2006.06.019 · Cited by 149
Palmitoylation is the Switch that Assigns Calnexin to Quality Control or ER Calcium Signaling
Lynes, E. M., Raturi, A., Shenkman, M., Sandoval, C. O., Yap, M. C., Wu, J., Janowicz, A., Myhill, N., Benson, M. D., Campbell, R. E., et al. (2013) · Journal of Cell Science · doi:10.1242/jcs.125856 · Cited by 147
Reconstitution of Human Ero1-Lα/Protein-Disulfide Isomerase Oxidative Folding Pathway in Vitro
Wang, L., Li, S., Sidhu, A., Zhu, L., Liang, Y., Freedman, R. B., & Wang, C.-C. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m806645200 · Cited by 140
Protein disulfide isomerases: Redox connections in and out of the endoplasmic reticulum
Soares Moretti, A. I., & Martins Laurindo, F. R. (2017) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2016.11.007 · Cited by 140
Artemisinin Induces Calcium-Dependent Protein Secretion in the Protozoan Parasite Toxoplasma gondii
Nagamune, K., Beatty, W. L., & Sibley, L. D. (2007) · Eukaryotic Cell · doi:10.1128/ec.00262-07 · Cited by 138
Haller, T., Dietl, P., Deetjen, P., & Völkl, H. (1996) · Cell Calcium · doi:10.1016/s0143-4160(96)90084-6 · Cited by 131
Määttänen, P., Kozlov, G., Gehring, K., & Thomas, D. Y. (2006) · Biochemistry and Cell Biology · doi:10.1139/o06-186 · Cited by 127
Marino, M., Stoilova, T., Giorgi, C., Bachi, A., Cattaneo, A., Auricchio, A., Pinton, P., & Zito, E. (2014) · Human Molecular Genetics · doi:10.1093/hmg/ddu602 · Cited by 126
Pino, P., Foth, B. J., Kwok, L. Y., Sheiner, L., Schepers, R., Soldati, T., & Soldati‐Favre, D. (2007) · PLoS Pathogens · doi:10.1371/journal.ppat.0030115 · Cited by 120
Development of CRISPR/Cas9 for Efficient Genome Editing in Toxoplasma gondii
Shen, B., Brown, K. M., Long, S., & Sibley, L. D. (2016) · Methods in molecular biology · doi:10.1007/978-1-4939-6472-7_6 · Cited by 118
BiP and PDI Cooperate in the Oxidative Folding of Antibodiesin Vitro
Mayer, M., Kies, U., Kammermeier, R., & Büchner, J. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m002655200 · Cited by 116
Peters, L. R., & Raghavan, M. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1100690 · Cited by 114
Ushioda, R., Miyamoto, A., Inoue, M., Watanabe, S. P., Okumura, M., Maegawa, K.-I., Uegaki, K., Fujii, S., Fukuda, Y., Umitsu, M., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1605818113 · Cited by 101
ER stress as a sentinel mechanism for ER Ca2+ homeostasis
Makio, T., Chen, J., & Simmen, T. (2024) · Cell Calcium · doi:10.1016/j.ceca.2024.102961 · Cited by 90
Mitochondrial behaviour throughout the lytic cycle of Toxoplasma gondii
Ovciarikova, J., Lemgruber, L., Stilger, K. L., Sullivan, W. J., & Sheiner, L. (2017) · Scientific Reports · doi:10.1038/srep42746 · Cited by 88
Li, Z., Ramakrishnan, S., Striepen, B., & Moreno, S. N. J. (2013) · PLoS Pathogens · doi:10.1371/journal.ppat.1003665 · Cited by 82
Self-citationCarruthers, V. B. (1999) · Parasitology International · doi:10.1016/s1383-5769(98)00042-7 · Cited by 78
Identification of cryptic subunits from an apicomplexan ATP synthase
Huet, D., Rajendran, E., van Dooren, G. G., & Lourido, S. (2018) · eLife · doi:10.7554/elife.38097 · Cited by 78
Liffner, B., & Absalon, S. (2021) · Microorganisms · doi:10.3390/microorganisms9112306 · Cited by 78
Sharda, A. V., Kim, S. H., Jasuja, R., Gopal, S., Flaumenhaft, R. C., Furie, B. C., & Furie, B. (2015) · Blood · doi:10.1182/blood-2014-08-597419 · Cited by 77
Functional principles and regulation of molecular chaperones
Dahiya, V., & Büchner, J. (2018) · Advances in protein chemistry and structural biology · doi:10.1016/bs.apcsb.2018.10.001 · Cited by 77
Synchronous invasion of host cells by Toxoplasma gondii
Kafsack, B. F. C., Beckers, C. J., & Carruthers, V. B. (2004) · Molecular and Biochemical Parasitology · doi:10.1016/s0166-6851(04)00112-4 · Cited by 75
Calcium Signaling throughout the Toxoplasma gondii Lytic Cycle
Borges‐Pereira, L., Budu, A., McKnight, C. A., Moore, C. A., Vella, S. A., Triana, M. A. H., Liu, J., Garcia, C. R. S., Pace, D. A., & Moreno, S. N. J. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.652511 · Cited by 69
Self-citationChichiarelli, S., Fabio Altieri, F., Paglia, G., Rubini, E., Minacori, M., & Eufemi, M. (2022) · Cellular & Molecular Biology Letters · doi:10.1186/s11658-022-00315-x · Cited by 69
Zhang, L., Niu, Y., Zhu, L., Fang, J., Xie, W., Wang, L., & Wang, C.-C. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.602961 · Cited by 68
Protein Trafficking insideToxoplasma gondii
Sheiner, L., & Soldati‐Favre, D. (2008) · Traffic · doi:10.1111/j.1600-0854.2008.00713.x · Cited by 65
Reliable measurement of free Ca2+ concentrations in the ER lumen using Mag-Fluo-4
Rossi, A. M., & Taylor, C. W. (2020) · Cell Calcium · doi:10.1016/j.ceca.2020.102188 · Cited by 64
Noninvasive monitoring of chronic kidney disease using pH and perfusion imaging
Pavuluri, K., Manoli, I., Pass, A. R., Li, Y., Vernon, H. J., Venditti, C. P., & McMahon, M. T. (2019) · Science Advances · doi:10.1126/sciadv.aaw8357 · Cited by 63
Calcium signaling and the lytic cycle of the Apicomplexan parasite Toxoplasma gondii
Triana, M. A. H., Márquez‐Nogueras, K. M., Vella, S. A., & Moreno, S. N. J. (2018) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2018.08.004 · Cited by 61
Self-citationLiu, J., Pace, D. A., Dou, Z., King, T., Guidot, D. M., Li, Z., Carruthers, V. B., & Moreno, S. N. J. (2014) · Molecular Microbiology · doi:10.1111/mmi.12685 · Cited by 59
Self-citationHajagos, B. E., Turetzky, J. M., Peng, E. D., Cheng, S. J., Ryan, C. M., Souda, P., Whitelegge, J. P., Lebrun, M., Dubremetz, J., & Bradley, P. J. (2011) · Traffic · doi:10.1111/j.1600-0854.2011.01308.x · Cited by 57
Secretory organelle trafficking in Toxoplasma gondii: A long story for a short travel
Venugopal, K., & Marion, S. (2018) · International Journal of Medical Microbiology · doi:10.1016/j.ijmm.2018.07.007 · Cited by 57
Alanen, H. I., Williamson, R. A., Howard, M. J., Hatahet, F., Salo, K. E. H., Kauppila, A., Kellokumpu, S., & Ruddock, L. W. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m604314200 · Cited by 56
The endoplasmic reticulum is a focal point for co-ordination of cellular activity
Bootman, M. D., Petersen, O. H., & Verkhratsky, A. (2002) · Cell Calcium · doi:10.1016/s0143-4160(02)00200-2 · Cited by 54
Stasic, A. J., Chasen, N. M., Dykes, E. J., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.04.038 · Cited by 53
Novel Thioredoxin-related Transmembrane Protein TMX4 Has Reductase Activity
Sugiura, Y., Araki, K., Iemura, S., Natsume, T., Hoseki, J., & Nagata, K. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.082545 · Cited by 52
ER Stress-Induced Secretion of Proteins and Their Extracellular Functions in the Heart
Meyer, B. A., & Doroudgar, S. (2020) · Cells · doi:10.3390/cells9092066 · Cited by 51
Retarded PDI diffusion and a reductive shift in poise of the calcium depleted endoplasmic reticulum
Avezov, E., Konno, T., Zyryanova, A. F., Chen, W., Laine, R. F., Crespillo-Casado, A., Melo, E. P., Ushioda, R., Nagata, K., Kaminski, C. F., et al. (2015) · BMC Biology · doi:10.1186/s12915-014-0112-2 · Cited by 48
Laliberté, J., & Carruthers, V. B. (2011) · Molecular and Biochemical Parasitology · doi:10.1016/j.molbiopara.2011.01.009 · Cited by 45
Fani, G., Torre, C. E. L., Cascella, R., Cecchi, C., Vendruscolo, M., & Chiti, F. (2022) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-022-04513-w · Cited by 44
Structures of the Toxoplasma gliding motility adhesin
Song, G., & Springer, T. A. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1403059111 · Cited by 42
Calcium Uptake and Proton Transport by Acidocalcisomes of Toxoplasma gondii
Rohloff, P. J., de Miranda, K. R., Rodrigues, J. C. F., Fang, J., Galizzi, M., Plattner, H., Hentschel, J., & Moreno, S. N. J. (2011) · PLoS ONE · doi:10.1371/journal.pone.0018390 · Cited by 40
Self-citationStructure of an MHC I–tapasin–ERp57 editing complex defines chaperone promiscuity
Müller, I. K., Winter, C., Thomas, C., Spaapen, R. M., Trowitzsch, S., & Tampé, R. (2022) · Nature Communications · doi:10.1038/s41467-022-32841-9 · Cited by 39
Protein disulfide isomerase of Toxoplasma gondii is targeted by mucosal IgA antibodies in humans
Meek, B., Back, J. W., Klaren, V. N. A., Speijer, D., & Peek, R. (2002) · FEBS Letters · doi:10.1016/s0014-5793(02)02911-3 · Cited by 35
Chasen, N. M., Asady, B., Lemgruber, L., Vommaro, R. C., Kissinger, J. C., Coppens, I., & Moreno, S. N. J. (2017) · mSphere · doi:10.1128/msphere.00027-17 · Cited by 32
Self-citationSignaling through Ca2+Microdomains from Store-Operated CRAC ChannelsPreprint
Barak, P., & Parekh, A. B. (2019) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a035097 · Cited by 32
The role of potassium and host calcium signaling in Toxoplasma gondii egress
Vella, S. A., Moore, C. A., Li, Z., Triana, M. A. H., Potapenko, E. S., & Moreno, S. N. J. (2021) · Cell Calcium · doi:10.1016/j.ceca.2020.102337 · Cited by 31
Self-citationThe Toxoplasma plant‐like vacuolar compartment ( PLVAC )
Stasic, A. J., Moreno, S. N. J., Carruthers, V. B., & Dou, Z. (2022) · Journal of Eukaryotic Microbiology · doi:10.1111/jeu.12951 · Cited by 30
Self-citationWang, L., Zhou, J., Wang, L., Wang, C., & Essex, D. W. (2018) · Journal of Thrombosis and Haemostasis · doi:10.1111/jth.14366 · Cited by 27
Metallopeptidases of Toxoplasma gondii : in silico identification and gene expression
Escotte‐Binet, S., Huguenin, A., Aubert, D., Martin, A.-P., Kaltenbach, M. L., Florent, I., & Villena, I. (2018) · Parasite · doi:10.1051/parasite/2018025 · Cited by 24
Mares, R. E., Meléndez-López, S. G., & Ramos, M. A. (2011) · International Journal of Molecular Sciences · doi:10.3390/ijms12074625 · Cited by 23
Trapping redox partnerships in oxidant-sensitive proteins with a small, thiol-reactive cross-linker
Allan, K. M., Loberg, M. A., Chepngeno, J., Hurtig, J. E., Tripathi, S., Kang, M. G., Allotey, J. K., Widdershins, A., Pilat, J. M., Sizek, H., et al. (2016) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2016.10.506 · Cited by 23
Bifunctional Electrophiles Cross-Link Thioredoxins with Redox Relay Partners in Cells
Naticchia, M. R., Brown, H. A., García, F., Lamade, A. M., Justice, S. L., Herrin, R. P., Morano, K. A., & West, J. D. (2013) · Chemical Research in Toxicology · doi:10.1021/tx4000123 · Cited by 21
Genetic Indicators for Calcium Signaling Studies in Toxoplasma gondii
Vella, S. A., Calixto, A., Asady, B., Li, Z., & Moreno, S. N. J. (2019) · Methods in molecular biology · doi:10.1007/978-1-4939-9857-9_11 · Cited by 21
Self-citationCobb, D. W., Kudyba, H. M., Villegas, A., Hoopmann, M. R., Baptista, R. P., Bruton, B., Krakowiak, M., Moritz, R. L., & Muralidharan, V. (2021) · PLoS Pathogens · doi:10.1371/journal.ppat.1009293 · Cited by 20
Ramírez‐Flores, C. J., Cruz‐Mirón, R., Arroyo, R., Mondragón-Castelán, M. E., Nopal-Guerrero, T., González‐Pozos, S., Ríos‐Castro, E., & Mondragón‐Flores, R. (2018) · Parasitology Research · doi:10.1007/s00436-018-6163-5 · Cited by 19
A crosslinker-based identification of redox relay targets
Araki, K., Ushioda, R., Kusano, H., Tanaka, R., Hatta, T., Fukui, K., Nagata, K., & Natsume, T. (2017) · Analytical Biochemistry · doi:10.1016/j.ab.2016.12.025 · Cited by 11
Pinto, R. D., Moreira, A. R. S., Pereira, P. J. B., & dos Santos, N. M. S. (2013) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2013.07.024 · Cited by 10
Giraldo, D. M., Arenas, A. F., Dávila, J. A. A., Molina, D. A., Hernández, A., Cardona, N., Gomez-Yepes, M., & Gómez‐Marín, J. E. (2016) · Experimental Parasitology · doi:10.1016/j.exppara.2016.02.005 · Cited by 10
Oxygen-dependent regulation of F-box proteins in Toxoplasma gondii is mediated by Skp1 glycosylation
Mandalasi, M., Gas‐Pascual, E., Baptista, C. G., Deng, B., van der Wel, H., Kruijtzer, J. A. W., Boons, G., Blader, I. J., & West, C. M. (2024) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2024.107801 · Cited by 10
Yavuz, U., Alaylıoğlu, M., Şengül, B., Karras, S. Ν., Gezen‐Ak, D., & Dursun, E. (2021) · In Vitro Cellular & Developmental Biology - Animal · doi:10.1007/s11626-021-00602-5 · Cited by 7
Rinkenberger, N., Rosenberg, A., Radke, J. B., Bhushan, J., Tomita, T., Weiss, L. M., & Sibley, L. D. (2023) · mBio · doi:10.1128/mbio.02595-23 · Cited by 7
Wang, C., Sun, P., Jia, Y., Tang, X., Liu, X., Suo, X., & Peng, H. (2024) · mBio · doi:10.1128/mbio.02051-24 · Cited by 6
Bastos‐Aristizabal, S., Kozlov, G., & Gehring, K. (2014) · Scientific Reports · doi:10.1038/srep04464 · Cited by 5
Usey, M. M., Ruberto, A. A., Parker, K. V., & Huet, D. (2024) · Molecular Biology of the Cell · doi:10.1091/mbc.e24-08-0344 · Cited by 5
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Li, Z., Asady, B., Chang, L., Triana, M. A. H., Li, C., Coppens, I., & Moreno, S. N. J. (2025) · eLife · doi:10.1101/2024.08.15.608087 · Cited by 4
Self-citationCalcium transfer from the ER to other organelles for optimal signaling in Toxoplasma gondiiPreprint
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Self-citationNowak, J. I., Olszewska, A., Król, O., & Zmijewski, M. A. (2023) · Nutrients · doi:10.3390/nu15214529 · Cited by 3
Calixto, A., Moen, K. E., & Moreno, S. N. J. (2025) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2025.108372 · Cited by 3
Self-citation
Metadata
- Authors
- Moen, K. E., & Moreno, S. N. J.
- Affiliations
- University of Georgia (US)
- Corresponding author
- Moreno, Silvia N. J.
- ORCID
- Moreno, Silvia N. J.
- Venue
- mBio
- Publisher
- American Society for Microbiology
- Published
- 2026-05-13
- Volume
- 17
- Issue
- 5
- Pages
- e0312425-e0312425
- ISSN
- 2150-7511 (ISSN-L)
- PMC
- PMC12132493
- OpenAlex
- W7147608578
- Cited by
- 0
- References
- 123
- FWCI
- 0.00
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- mBio (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- PubMed (publishedVersion)
- PubMed Central (publishedVersion, cc-by)
- PubMed Central (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Institutes of Health (R01AI174600, R21AI154931, T32AI060546)
- Topics
- Life Sciences › Immunology and Microbiology › Parasitology › Toxoplasma gondii Research Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Endoplasmic Reticulum Stress and Disease
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
- Keywords
- Toxoplasma gondii, protein disulfide isomerase, endoplasmic reticulum, redox homeostasis, calcium signaling, lytic cycle, tachyzoites, disulfide bond formation, thioredoxin-like domain, CXXC motif, parasite invasion, parasite virulence, Apicomplexa
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Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.
