Minding the calcium store: Ryanodine receptor activation as a convergent mechanism of PCB toxicity

Pessah, Isaac N.; Cherednichenko, Gennady; Lein, Pamela J.

doi:10.1016/j.pharmthera.2009.10.009

Cited by 231Toxic Organic Pollutants ImpactIon channel regulation and functionCardiac electrophysiology and arrhythmias

Minding the calcium store: Ryanodine receptor activation as a convergent mechanism of PCB toxicity

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Pessah, Isaac N., Cherednichenko, Gennady, Lein, Pamela J.·2010·Pharmacology & Therapeutics

DOI 10.1016/j.pharmthera.2009.10.009PMC PMC2823855

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Abstract

Chronic low-level polychlorinated biphenyl (PCB) exposures remain a significant public health concern since results from epidemiological studies indicate that PCB burden is associated with immune system dysfunction, cardiovascular disease, and impairment of the developing nervous system. Of these various adverse health effects, developmental neurotoxicity has emerged as a particularly vulnerable endpoint in PCB toxicity. Arguably the most pervasive biological effects of PCBs could be mediated by their ability to alter the spatial and temporal fidelity of Ca2+ signals through one or more receptor-mediated processes. This review will focus on our current knowledge of the structure and function of ryanodine receptors (RyRs) in muscle and nerve cells and how PCBs and related non-coplanar structures alter these functions. The molecular and cellular mechanisms by which non-coplanar PCBs and related structures alter local and global Ca2+ signaling properties and the possible short and long-term consequences of these perturbations on neurodevelopment and neurodegeneration are reviewed.

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Nanomolar concentrations of PCB 95 stabilize ryanodine receptors in the open configuration, increasing Ca2+ release from intracellular stores.
“Nanomolar concentrations of PCB 95 stabilize ryanodine receptors (RyRs) in the open configuration, increasing Ca 2ϩ release from intracellular stores (Pessah et al., 2010).”
From The Environmental Neurotoxicant PCB 95 Promotes Synaptogenesis via Ryanodine Receptor-Dependent miR132 Upregulation (2014) · cites this paper as Pessah et al., 2010
Section 2.2 says PCB 95 stabilizes RyR1 in its fully open state, and section 2.3 describes PCB 95–induced calcium release from intracellular ER stores. The copy does not establish that these effects occur at nanomolar PCB 95 concentrations; its concentration statement reports enhanced RyR activity at ≤1 μM. (LLM, conf=0.86)
Experimental — accuracy not yet measured
Because RyRs are functionally coupled to NMDA receptors, the findings suggest that RyRs are required for not only PCB-induced synaptogenesis, but also activity-dependent synaptogenesis, expanding the role for RyRs in neuronal plasticity.
“Because RyRs are functionally coupled to NMDA receptors (Berridge, 2006;Pessah et al., 2010), our findings suggest that RyRs are required for not only PCB-induced synaptogenesis, but also activity-dependent synaptogenesis, expanding the role for RyRs in neuronal plasticity.”
From The Environmental Neurotoxicant PCB 95 Promotes Synaptogenesis via Ryanodine Receptor-Dependent miR132 Upregulation (2014) · cites this paper as Pessah et al., 2010
NDL PCBs are thought to disrupt normal neurodevelopment via modulation of signaling by biogenic amines, thyroid hormone, and intracellular calcium during critical windows of brain development.
“NDL PCBs are thought to disrupt normal neurodevelopment via modulation of signaling by biogenic amines, thyroid hormone, and intracellular calcium during critical windows of brain development [ 105 ].”
From DNA methylation: a mechanism linking environmental chemical exposures to risk of autism spectrum disorders? (2016) · cites this paper as [105]
These pathways are also dysregulated in ASD.
“These are pathways that are also dysregulated in ASD [ 27 , 105 , 123 ].”
From DNA methylation: a mechanism linking environmental chemical exposures to risk of autism spectrum disorders? (2016) · cites this paper as [105]
PCBs are important endocrine disruptors that perturb intracellular Ca2+ signalling by promoting Ca2+ entry and enhancing Ca2+ release from endoplasmic reticulum through ryanodine receptors.
“PCBs are important endocrine disruptors which, among several other effects, perturb intracellular Ca2+ signalling by promoting Ca2+ entry and by enhancing Ca2+ release from the endoplasmic reticulum through ryanodine receptors [248].”
From Consensus Paper: Pathological Role of the Cerebellum in Autism (2012) · cites this paper as [248]

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Morita, H., Honda, A., Inoue, R., Ito, Y., Abe, K., Nelson, M. T., & Brayden, J. E. (2007) · Journal of Pharmacological Sciences · doi:10.1254/jphs.fp0061332 · Cited by 125 · see citing works
Ortho-substituted polychlorinated biphenyls Alter microsomal calcium transport by direct interaction with ryanodine receptors of mammalian brain*
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Polychlorinated Biphenyl Exposure and Neuropsychological Status among Older Residents of Upper Hudson River Communities
Fitzgerald, E. F., Belanger, E. E., Gómez, M. I., Cayo, M. R., McCaffrey, R. J., Seegal, R. F., Jansing, R. L., Hwang, S., & Hicks, H. E. (2007) · Environmental Health Perspectives · doi:10.1289/ehp.10432 · Cited by 124 · see citing works
Skeletal Muscle Ryanodine Receptor Is a Redox Sensor with a Well Defined Redox Potential That Is Sensitive to Channel Modulators
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Polychlorinated biphenyls in Spanish adults: Determinants of serum concentrations
Agudo, A., Goñi, F., Etxeandia, A., Vives, A., Millán, E., López, R., Amiano, P., Ardanáz, E., Barricarte, A., Chirlaque, M. D., et al. (2009) · Environmental Research · doi:10.1016/j.envres.2009.03.009 · Cited by 120 · see citing works
Timing is everything: Consequences of transient and sustained AhR activity
Mitchell, K. A., & Elferink, C. J. (2008) · Biochemical Pharmacology · doi:10.1016/j.bcp.2008.10.028 · Cited by 120 · see citing works
Polychlorinated Biphenyl–Induced Reduction of Dopamine Transporter Expression as a Precursor to Parkinson's Disease–Associated Dopamine Toxicity
Caudle, W. M., Richardson, J. R., Delea, K. C., Guillot, T. S., Wang, M., Pennell, K. D., & Miller, G. W. (2006) · Toxicological Sciences · doi:10.1093/toxsci/kfl018 · Cited by 120 · see citing works
Levels and chiral signatures of persistent organochlorine pollutants in human tissues from Belgium
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Fetal Mechanisms in Neurodevelopmental Disorders
Connors, S. L., Levitt, P. R., Matthews, S. G., Slotkin, T. A., Johnston, M. V., Kinney, H. C., Johnson, W. G., Dailey, R. M., & Zimmerman, A. W. (2008) · Pediatric Neurology · doi:10.1016/j.pediatrneurol.2007.10.009 · Cited by 119 · see citing works
The Ryanodine Receptor Calcium Channel of β-Cells
Islam, M. S. (2002) · Diabetes · doi:10.2337/diabetes.51.5.1299 · Cited by 119 · see citing works
Human health risk of polychlorinated biphenyls and organochlorine pesticides resulting from seafood consumption in South Korea, 2005–2007
Moon, H., Kim, H.-S., Choi, M., Yu, J., & Choi, H. (2009) · Food and Chemical Toxicology · doi:10.1016/j.fct.2009.04.028 · Cited by 118 · see citing works
A novel pathway regulating the mammalian target of rapamycin (mTOR) signaling
Chen, J., & Fang, Y. (2002) · Biochemical Pharmacology · doi:10.1016/s0006-2952(02)01263-7 · Cited by 116 · see citing works
Environmental Contaminants as Risk Factors for Developing Diabetes
Carpenter, D. O. (2008) · Reviews on Environmental Health · doi:10.1515/reveh.2008.23.1.59 · Cited by 116 · see citing works
Ortho-substituted polychlorinated biphenyls alter calcium regulation by a ryanodine receptor-mediated mechanism: structural specificity toward skeletal- and cardiac-type microsomal calcium release channels.
WONG, P. W. K., & Pessah, I. N. (1996) · Molecular Pharmacology · doi:10.1016/s0026-895x(25)08790-5 · Cited by 116 · see citing works
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Polychlorinated biphenyls, organochlorine pesticides and neurodevelopment
Korrick, S. A., & Sagiv, S. K. (2008) · Current Opinion in Pediatrics · doi:10.1097/mop.0b013e3282f6a4e9 · Cited by 115 · see citing works
The Skeletal L-type Ca2+ Current Is a Major Contributor to Excitation-coupled Ca2+ entry
Bannister, R. A., Pessah, I. N., & Beam, K. G. (2008) · The Journal of General Physiology · doi:10.1085/jgp.200810105 · Cited by 115 · see citing works
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Subnanometer-resolution electron cryomicroscopy-based domain models for the cytoplasmic region of skeletal muscle RyR channel
Serysheva, I. I., Ludtke, S. J., Baker, M. L., Cong, Y., Topf, M., Eramian, D., Šali, A., Hamilton, S. L., & Chiu, W. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0803189105 · Cited by 114 · see citing works
Long-term effects of developmental exposure to 2,2',3,5',6-pentachlorobiphenyl (PCB 95) on locomotor activity, spatial learning and memory and brain ryanodine binding.
Schantz, S. L., Seo, B. W., Wong, P. W., & Pessah, I. N. (1997) · PubMed · Cited by 114 · see citing works
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Visualization of the Domain Structure of an L-type Ca2+ Channel Using Electron Cryo-microscopy
Wolf, M., Eberhart, A., Glossmann, H. H., Striessnig, J., & Grigorieff, N. (2003) · Journal of Molecular Biology · doi:10.1016/s0022-2836(03)00899-4 · Cited by 114 · see citing works
Differential regulation of SK and BK channels by Ca2+ signals from Ca2+ channels and ryanodine receptors in guinea‐pig urinary bladder myocytes
Herrera, G. M., & Nelson, M. T. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2002.017707 · Cited by 114 · see citing works
Polychlorinated biphenyls induce caspase-dependent cell death in cultured embryonic rat hippocampal but not cortical neurons via activation of the ryanodine receptor
Howard, A. (2003) · Toxicology and Applied Pharmacology · doi:10.1016/s0041-008x(03)00156-x · Cited by 112 · see citing works
Induction of LTD in the Dentate Gyrus In Vitro Is NMDA Receptor Independent, but Dependent on Ca2+Influx via Low-Voltage–Activated Ca2+Channels and Release of Ca2+From Intracellular Stores
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THE DISTRIBUTION AND EXCRETION OF2,4,5,2', 5'-PENTACHLOROBIPHENYL IN THE RAT
Matthews, H. B., & ANDERSON, M. W. (1975) · Drug Metabolism and Disposition · doi:10.1016/s0090-9556(25)05715-0 · Cited by 112 · see citing works
A “Synaptoplasmic Cistern” Mediates Rapid Inhibition of Cochlear Hair Cells
Lioudyno, M., Hiel, H., Kong, J.-H., Katz, E., Waldman, E. H., Parameshwaran, S., Glowatzki, E., & Fuchs, P. A. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.3674-04.2004 · Cited by 111 · see citing works
Ontogeny of Local Sarcoplasmic Reticulum Ca2+Signals in Cerebral Arteries
Gollasch, M., Wellman, G. C., Knot, H. J., Jaggar, J. H., Damon, D. H., Bonev, A. D., & Nelson, M. T. (1998) · Circulation Research · doi:10.1161/01.res.83.11.1104 · Cited by 111 · see citing works
Presenilin 2 Interacts with Sorcin, a Modulator of the Ryanodine Receptor
Pack-Chung, E., Meyers, M. B., Pettingell, W. P., Moir, R. D., Brownawell, A. M., Cheng, I., Tanzi, R. E., & Kim, T. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m909882199 · Cited by 110 · see citing works
Conformational activation of Ca 2+ entry by depolarization of skeletal myotubes
Cherednichenko, G., Hurne, A. M., Fessenden, J. D., Lee, E. H., Allen, P. D., Beam, K. G., & Pessah, I. N. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0403485101 · Cited by 109 · see citing works
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Polychlorinated biphenyls (PCBs) in San Francisco Bay
Davis, J. A., Hetzel, F., Oram, J. J., & McKee, L. J. (2007) · Environmental Research · doi:10.1016/j.envres.2007.01.013 · Cited by 109 · see citing works
Molecular Mechanisms Involved in the Toxic Effects of Polychlorinated Biphenyls (PCBs) and Brominated Flame Retardants (BFRs)
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Mobilization of Calcium from Intracellular Stores Facilitates Somatodendritic Dopamine Release
Patel, J. C., Witkovsky, P., Avshalumov, M. V., & Rice, M. E. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.0181-09.2009 · Cited by 109 · see citing works

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Consensus Paper: Pathological Role of the Cerebellum in Autism
Fatemi, S. H., Aldinger, K. A., Ashwood, P., Bauman, M. L., Blaha, C. D., Blatt, G. J., Chauhan, A., Chauhan, V., Dager, S. R., Dickson, P. E., et al. (2012) · The Cerebellum · doi:10.1007/s12311-012-0355-9 · Cited by 723 · see citing works
Environmental pollution, a hidden culprit for health issues
Xu, H., Yang, J., Sun, Z., Su, J., Liu, Q. S., Zhou, Q., & Jiang, G. (2022) · Eco-Environment & Health · doi:10.1016/j.eehl.2022.04.003 · Cited by 334 · see citing works
Cytokine dysregulation in autism spectrum disorders (ASD): Possible role of the environment
Goines, P. E., & Ashwood, P. (2013) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2012.07.006 · Cited by 314 · see citing works
Polychlorinated Biphenyls (PCBs) in the Environment: Occupational and Exposure Events, Effects on Human Health and Fertility
Montano, L., Pironti, C., Pinto, G., Ricciardi, M., Buono, A., Brogna, C., Venier, M., Piscopo, M., Amoresano, A., & Motta, O. (2022) · Toxics · doi:10.3390/toxics10070365 · Cited by 272 · see citing works
A mechanistic view of polybrominated diphenyl ether (PBDE) developmental neurotoxicity
Costa, L. G., de Laat, R., Tagliaferri, S., & Pellacani, C. (2013) · Toxicology Letters · doi:10.1016/j.toxlet.2013.11.011 · Cited by 256 · see citing works
Neurotoxicity of polychlorinated biphenyls and related organohalogens
Pessah, I. N., Lein, P. J., Seegal, R. F., & Sagiv, S. K. (2019) · Acta Neuropathologica · doi:10.1007/s00401-019-01978-1 · Cited by 222 · see citing works
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Early environmental risk factors for neurodevelopmental disorders – a systematic review of twin and sibling studies
Carlsson, T., Molander, F., Taylor, M. J., Jonsson, U., & Bölte, S. (2020) · Development and Psychopathology · doi:10.1017/s0954579420000620 · Cited by 182 · see citing works
Levels of select PCB and PBDE congeners in human postmortem brain reveal possible environmental involvement in 15q11‐q13 duplication autism spectrum disorder
Mitchell, M. M., Woods, R., Chi, L., Schmidt, R. J., Pessah, I. N., Kostyniak, P. J., & LaSalle, J. M. (2012) · Environmental and Molecular Mutagenesis · doi:10.1002/em.21722 · Cited by 164 · see citing works
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Tipping the balance of autism risk: potential mechanisms linking pesticides and autism
Shelton, J. F., Hertz-Picciotto, I., & Pessah, I. N. (2012) · Environmental Health Perspectives · doi:10.1289/ehp.1104553 · Cited by 164 · see citing works
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DNA methylation: a mechanism linking environmental chemical exposures to risk of autism spectrum disorders?
Keil, K. P., & Lein, P. J. (2016) · Environmental Epigenetics · doi:10.1093/eep/dvv012 · Cited by 167 · see citing works
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PCB-95 Promotes Dendritic Growth via Ryanodine Receptor–Dependent Mechanisms
Wayman, G. A., Yang, D., Bose, D. D., Lesiak, A., Ledoux, V., Bruun, D., Pessah, I. N., & Lein, P. J. (2012) · Environmental Health Perspectives · doi:10.1289/ehp.1104832 · Cited by 136 · see citing works
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PCB-95 Modulates the Calcium-Dependent Signaling Pathway Responsible for Activity-Dependent Dendritic Growth
Wayman, G. A., Bose, D. D., Yang, D., Lesiak, A. J., Bruun, D. A., Impey, S., Ledoux, V. A., Pessah, I. N., & Lein, P. J. (2012) · Environmental Health Perspectives · doi:10.1289/ehp.1104833 · Cited by 136 · see citing works
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Evidence Implicating Non-Dioxin-Like Congeners as the Key Mediators of Polychlorinated Biphenyl (PCB) Developmental Neurotoxicity
Klocke, C. R., & Lein, P. J. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21031013 · Cited by 135 · see citing works
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Neuronal connectivity as a convergent target of gene × environment interactions that confer risk for Autism Spectrum Disorders
Stamou, M., Streifel, K. M., Goines, P. E., & Lein, P. J. (2013) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2012.12.001 · Cited by 128 · see citing works
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Is Triclosan a neurotoxic agent?
Ruszkiewicz, J. A., Li, S., Rodriguez, M. B., & Aschner, M. (2017) · Journal of Toxicology and Environmental Health Part B · doi:10.1080/10937404.2017.1281181 · Cited by 121 · see citing works
Advancing the science of developmental neurotoxicity (DNT): testing for better safety evaluation
Bal‐Price, A. (2012) · ALTEX · doi:10.14573/altex.2012.2.202 · Cited by 112 · see citing works
Developing and applying the adverse outcome pathway concept for understanding and predicting neurotoxicity
Bal‐Price, A., Lein, P. J., Keil, K. P., Sethi, S., Shafer, T. J., Barenys, M., Fritsche, E., Sachana, M., & Meek, M. E. (2016) · NeuroToxicology · doi:10.1016/j.neuro.2016.05.010 · Cited by 96 · see citing works
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PCBs and OH-PCBs in Serum from Children and Mothers in Urban and Rural U.S. Communities
Marek, R. F., Thorne, P. S., Wang, K., DeWall, J., & Hornbuckle, K. C. (2013) · Environmental Science & Technology · doi:10.1021/es304455k · Cited by 96 · see citing works
Endocrine-disrupting actions of PCBs on brain development and social and reproductive behaviors
Bell, M. R. (2014) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2014.09.020 · Cited by 94 · see citing works
Biotransformation of BDE-47 to Potentially Toxic Metabolites Is Predominantly Mediated by Human CYP2B6
Feo, M. L., Gross, M. S., McGarrigle, B. P., Eljarrat, E., Barceló, ‪., Aga, D. S., & Olson, J. R. (2012) · Environmental Health Perspectives · doi:10.1289/ehp.1205446 · Cited by 93 · see citing works
Comparative Analyses of the 12 Most Abundant PCB Congeners Detected in Human Maternal Serum for Activity at the Thyroid Hormone Receptor and Ryanodine Receptor
Sethi, S., Morgan, R. K., Feng, W., Lin, Y., Li, X., Luna, C., Koch, M., Bansal, R., Duffel, M. W., Puschner, B., et al. (2019) · Environmental Science & Technology · doi:10.1021/acs.est.9b00535 · Cited by 90 · see citing works
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Possible Mechanism of Perfluorooctane Sulfonate and Perfluorooctanoate on the Release of Calcium Ion from Calcium Stores in Primary Cultures of Rat Hippocampal Neurons
Liu, X., Jin, Y., Liu, W., Wang, F., & Hao, S. (2011) · Toxicology in Vitro · doi:10.1016/j.tiv.2011.04.016 · Cited by 91 · see citing works
The Environmental Neurotoxicant PCB 95 Promotes Synaptogenesis via Ryanodine Receptor-Dependent miR132 Upregulation
Lesiak, A., Zhu, M., Chen, H., Appleyard, S. M., Impey, S., Lein, P. J., & Wayman, G. A. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.2884-13.2014 · Cited by 85 · see citing works
“MeCP2 knock-out animals have significantly perturbed synthesis and release of BDNF, a neurotrophic factor that stimulates dendritic outgrowth and synaptogenesis (Jin et al., 2003; Wang et al., 2006; Rex et al., 2007).”
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Triclosan Impairs Swimming Behavior and Alters Expression of Excitation-Contraction Coupling Proteins in Fathead Minnow (Pimephales promelas)
Holland, E. B., Connon, R. E., Werner, I., Davies, R. E., Beggel, S., Feng, W., & Pessah, I. N. (2013) · Environmental Science & Technology · doi:10.1021/es303790b · Cited by 85 · see citing works
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Ryanodine receptor calcium channels and their partners as drug targets
Mackrill, J. J. (2010) · Biochemical Pharmacology · doi:10.1016/j.bcp.2010.01.014 · Cited by 84 · see citing works
The developmental neurotoxicity of legacy vs. contemporary polychlorinated biphenyls (PCBs): similarities and differences
Klocke, C. R., Sethi, S., & Lein, P. J. (2019) · Environmental Science and Pollution Research · doi:10.1007/s11356-019-06723-5 · Cited by 83 · see citing works
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Current Status of the Epidemiologic Evidence Linking Polychlorinated Biphenyls and Non-Hodgkin Lymphoma, and the Role of Immune Dysregulation
Kramer, S., Hikel, S. M., Adams, K., Hinds, D. R., & Moon, K. A. (2012) · Environmental Health Perspectives · doi:10.1289/ehp.1104652 · Cited by 82 · see citing works
Chiral polychlorinated biphenyls: absorption, metabolism and excretion—a review
Kania‐Korwel, I., & Lehmler, H. (2015) · Environmental Science and Pollution Research · doi:10.1007/s11356-015-4150-2 · Cited by 79 · see citing works
Para- and Ortho -Substitutions Are Key Determinants of Polybrominated Diphenyl Ether Activity toward Ryanodine Receptors and Neurotoxicity
Kim, K. H., Bose, D. D., Ghogha, A., Riehl, J., Zhang, R., Barnhart, C. D., Lein, P. J., & Pessah, I. N. (2010) · Environmental Health Perspectives · doi:10.1289/ehp.1002728 · Cited by 77 · see citing works
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Bioaccumulation and behavioral effects of 2,2′,4,4′-tetrabromodiphenyl ether (BDE-47) in perinatally exposed mice
Ta, T. A., Koenig, C. M., Golub, M. S., Pessah, I. N., Qi, L., Aronov, P. A., & Berman, R. F. (2011) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2011.02.003 · Cited by 73 · see citing works
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Placenta and fetal brain share a neurodevelopmental disorder DNA methylation profile in a mouse model of prenatal PCB exposure
Laufer, B. I., Neier, K. E., Valenzuela, A. E., Yasui, D. H., Schmidt, R. J., Lein, P. J., & LaSalle, J. M. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110442 · Cited by 72 · see citing works
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Prenatal exposure to common environmental factors affects brain lipids and increases risk of developing autism spectrum disorders
Wong, C. T., Wais, J., & Crawford, D. A. (2015) · European Journal of Neuroscience · doi:10.1111/ejn.13028 · Cited by 74 · see citing works
Cumulative Impact of Polychlorinated Biphenyl and Large Chromosomal Duplications on DNA Methylation, Chromatin, and Expression of Autism Candidate Genes
Dunaway, K. W., Islam, M. S., Coulson, R. L., Lopez, S. J., Ciernia, A. V., Chu, R. G., Yasui, D. H., Pessah, I. N., Lott, P. C., Mordaunt, C. E., et al. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.11.058 · Cited by 68 · see citing works
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Polychlorinated Biphenyls (PCBs): Risk Factors for Autism Spectrum Disorder?
Panesar, H. K., Kennedy, C., Keil, K. P., & Lein, P. J. (2020) · Toxics · doi:10.3390/toxics8030070 · Cited by 70 · see citing works
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PCB 136 Atropselectively Alters Morphometric and Functional Parameters of Neuronal Connectivity in Cultured Rat Hippocampal Neurons via Ryanodine Receptor-Dependent Mechanisms
Yang, D., Kania‐Korwel, I., Ghogha, A., Chen, H., Stamou, M., Bose, D. D., Pessah, I. N., Lehmler, H., & Lein, P. J. (2014) · Toxicological Sciences · doi:10.1093/toxsci/kft334 · Cited by 71 · see citing works
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The Mitochondrial Aspartate/Glutamate Carrier AGC1 and Calcium Homeostasis: Physiological Links and Abnormalities in Autism
Napolioni, V., Persico, A. M., Porcelli, V., & Palmieri, L. (2011) · Molecular Neurobiology · doi:10.1007/s12035-011-8192-2 · Cited by 70 · see citing works
Nonlegacy PCBs: Pigment Manufacturing By-Products Get a Second Look
Grossman, E. (2013) · Environmental Health Perspectives · doi:10.1289/ehp.121-a86 · Cited by 70 · see citing works
Developmental exposure to polychlorinated biphenyls (PCBs) in the maternal diet causes host-microbe defects in weanling offspring mice
Rude, K. M., Pusceddu, M. M., Keogh, C. E., Sladek, J. A., Rabasa, G., Miller, E. N., Sethi, S., Keil, K. P., Pessah, I. N., Lein, P. J., et al. (2019) · Environmental Pollution · doi:10.1016/j.envpol.2019.07.066 · Cited by 67 · see citing works
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2,2′,3,5′,6-Pentachlorobiphenyl (PCB 95) and Its Hydroxylated Metabolites Are Enantiomerically Enriched in Female Mice
Kania‐Korwel, I., Barnhart, C. D., Stamou, M., Truong, K. M., Elkomy, M. H., Lein, P. J., Veng‐Pedersen, P., & Lehmler, H. (2012) · Environmental Science & Technology · doi:10.1021/es302810t · Cited by 62 · see citing works
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Exposure to endocrine disrupting chemicals and neurodevelopmental alterations
Pinson, A., Bourguignon, J. P., & Parent, A. (2016) · Andrology · doi:10.1111/andr.12211 · Cited by 62 · see citing works
Neurodevelopmental and behavioral toxicity via lactational exposure to the sum of six indicator non-dioxin-like-polychlorinated biphenyls (∑6 NDL-PCBs) in mice
Elnar, A. A., Diesel, B., Desor, F., Feidt, C., Bouayed, J., Kiemer, A. K., & Soulimani, R. (2012) · Toxicology · doi:10.1016/j.tox.2012.05.004 · Cited by 61 · see citing works
Review of QSAR Models and Software Tools for predicting Acute and Chronic Systemic Toxicity
Lapenna, S., Gatnik, M. F., & Andrew, W. (2010) · Joint Research Centre (European Commission) · doi:10.2788/60766 · Cited by 55 · see citing works
Protective Role of Quercetin on PCBs-Induced Oxidative Stress and Apoptosis in Hippocampus of Adult Rats
Selvakumar, K., Bavithra, S., Suganthi, M., Selvanesan, B. C., Perumal, E., Arunkumar, R., Krishnamoorthy, G., Venkataraman, P., & Arunakaran, J. (2011) · Neurochemical Research · doi:10.1007/s11064-011-0661-5 · Cited by 56 · see citing works
Toxicity of the Flame-Retardant BDE-49 on Brain Mitochondria and Neuronal Progenitor Striatal Cells Enhanced by a PTEN-Deficient Background
Napoli, E., Hung, C., Wong, S., & Giulivi, C. (2013) · Toxicological Sciences · doi:10.1093/toxsci/kfs339 · Cited by 55 · see citing works
The Sarcoplasmic Reticulum of Skeletal Muscle Cells: A Labyrinth of Membrane Contact Sites
Rossi, D., Pierantozzi, E., Amadsun, D. O., Buonocore, S., Rubino, E. M., & Sorrentino, V. (2022) · Biomolecules · doi:10.3390/biom12040488 · Cited by 51 · see citing works
Molecular Advances Leading to Treatment Implications for Fragile X Premutation Carriers
Hagerman, R. J. (2014) · Brain Disorders & Therapy · doi:10.4172/2168-975x.1000119 · Cited by 52 · see citing works
Variability in PCB and OH-PCB Serum Levels in Children and Their Mothers in Urban and Rural U.S. Communities
Marek, R. F., Thorne, P. S., DeWall, J., & Hornbuckle, K. C. (2014) · Environmental Science & Technology · doi:10.1021/es502490w · Cited by 53 · see citing works
Quantification of Polychlorinated Biphenyls and Polybrominated Diphenyl Ethers in Commercial Cows’ Milk from California by Gas Chromatography–Triple Quadruple Mass Spectrometry
Chen, X., Lin, Y., Dang, K., & Puschner, B. (2017) · PLoS ONE · doi:10.1371/journal.pone.0170129 · Cited by 52 · see citing works
Developmental exposure to environmentally relevant concentrations of bifenthrin alters transcription of mTOR and ryanodine receptor-dependent signaling molecules and impairs predator avoidance behavior across early life stages in inland silversides (Menidia beryllina)
Frank, D. F., Brander, S. M., Hasenbein, S., Harvey, D. J., Lein, P. J., Geist, J. P., & Connon, R. E. (2018) · Aquatic Toxicology · doi:10.1016/j.aquatox.2018.10.014 · Cited by 52 · see citing works
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Cross-omics gene and protein expression profiling in juvenile female mice highlights disruption of calcium and zinc signalling in the brain following dietary exposure to CB-153, BDE-47, HBCD or TCDD
Rasinger, J. D., Carroll, T. S., Lundebye, A. K., & Högstrand, C. (2014) · Toxicology · doi:10.1016/j.tox.2014.03.006 · Cited by 51 · see citing works
Polychlorinated biphenyls influence on autism spectrum disorder risk in the MARBLES cohort
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Authors: Pessah, I. N., Cherednichenko, G., & Lein, P. J.
Affiliations: University of California, Davis (US)
Corresponding author: Pessah, Isaac N.
ORCID: Pessah, Isaac N.
Lein, Pamela J.
Venue: Pharmacology & Therapeutics
Publisher: Elsevier BV
Published: 2010-02
Volume: 125
Issue: 2
Pages: 260-285
ISSN: 0163-7258 (ISSN-L)
DOI: 10.1016/j.pharmthera.2009.10.009
PMC: PMC2823855
OpenAlex: W2171969201
Cited by: 231
References: 452
Citations by year: 2026: 2 · 2025: 8 · 2024: 4 · 2023: 12 · 2022: 12 · 2021: 9 · 2020: 18 · 2019: 15 · 2018: 19 · 2017: 22 · 2016: 14 · 2015: 15 · 2014: 19 · 2013: 15 · 2012: 27
FWCI: 1.72
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Pharmacology & Therapeutics (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute of Environmental Health Sciences (1 P01-ES11269, P42-ES-04699, P42ES004699, P01ES011269, R01ES014901)
Topics: Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Toxic Organic Pollutants Impact
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac electrophysiology and arrhythmias
Keywords: polychlorinated biphenyls, ryanodine receptor, calcium signaling, developmental neurotoxicity, neurodegeneration, intracellular calcium stores, immune dysfunction, cardiovascular disease
MeSH terms: Calcium, Environmental Pollutants, Humans, Polychlorinated Biphenyls, Structure-Activity Relationship, Ryanodine Receptor Calcium Release Channel

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Minding the calcium store: Ryanodine receptor activation as a convergent mechanism of PCB toxicity

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