Ultrafine particulate matter pollution and dysfunction of endoplasmic reticulum Ca2+ store: A pathomechanism shared with amyotrophic lateral sclerosis motor neurons?
Increased risk of neurodegenerative diseases has been envisaged for air pollution exposure. On the other hand, environmental risk factors, including air pollution, have been suggested for Amyotrophic Lateral Sclerosis (ALS) pathomechanism. Therefore, the neurotoxicity of ultrafine particulate matter...
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| Format: | Article |
| Language: | English |
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Elsevier
2024-03-01
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| Series: | Ecotoxicology and Environmental Safety |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S0147651324001799 |
| _version_ | 1797261867269226496 |
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| author | Silvia Sapienza Valentina Tedeschi Barbara Apicella Anna Pannaccione Carmela Russo Maria Josè Sisalli Giorgia Magliocca Stefania Loffredo Agnese Secondo |
| author_facet | Silvia Sapienza Valentina Tedeschi Barbara Apicella Anna Pannaccione Carmela Russo Maria Josè Sisalli Giorgia Magliocca Stefania Loffredo Agnese Secondo |
| author_sort | Silvia Sapienza |
| collection | DOAJ |
| description | Increased risk of neurodegenerative diseases has been envisaged for air pollution exposure. On the other hand, environmental risk factors, including air pollution, have been suggested for Amyotrophic Lateral Sclerosis (ALS) pathomechanism. Therefore, the neurotoxicity of ultrafine particulate matter (PM0.1) (PM < 0.1 μm size) and its sub-20 nm nanoparticle fraction (NP20) has been investigated in motor neuronal-like cells and primary cortical neurons, mainly affected in ALS. The present data showed that PM0.1 and NP20 exposure induced endoplasmic reticulum (ER) stress, as occurred in cortex and spinal cord of ALS mice carrying G93A mutation in SOD1 gene. Furthermore, NSC-34 motor neuronal-like cells exposed to PM0.1 and NP20 shared the same proteomic profile on some apoptotic factors with motor neurons treated with the L-BMAA, a neurotoxin inducing Amyotrophic Lateral Sclerosis/Parkinson–Dementia Complex (ALS/PDC). Of note ER stress induced by PM0.1 and NP20 in motor neurons was associated to pathological changes in ER morphology and dramatic reduction of organellar Ca2+ level through the dysregulation of the Ca2+-pumps SERCA2 and SERCA3, the Ca2+-sensor STIM1, and the Ca2+-release channels RyR3 and IP3R3. Furthermore, the mechanism deputed to ER Ca2+ refilling (e.g. the so called store operated calcium entry-SOCE) and the relative currents ICRAC were also altered by PM0.1 and NP20 exposure. Additionally, these carbonaceous particles caused the exacerbation of L-BMAA-induced ER stress and Caspase-9 activation. In conclusion, this study shows that PM0.1 and NP20 induced the aberrant expression of ER proteins leading to dysmorphic ER, organellar Ca2+ dysfunction, ER stress and neurotoxicity, providing putative correlations with the neurodegenerative process occurring in ALS. |
| first_indexed | 2024-03-07T23:39:44Z |
| format | Article |
| id | doaj.art-ce4221280da74e40b4b7ca7de9632e54 |
| institution | Directory Open Access Journal |
| issn | 0147-6513 |
| language | English |
| last_indexed | 2024-04-24T23:48:02Z |
| publishDate | 2024-03-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Ecotoxicology and Environmental Safety |
| spelling | doaj.art-ce4221280da74e40b4b7ca7de9632e542024-03-15T04:42:43ZengElsevierEcotoxicology and Environmental Safety0147-65132024-03-01273116104Ultrafine particulate matter pollution and dysfunction of endoplasmic reticulum Ca2+ store: A pathomechanism shared with amyotrophic lateral sclerosis motor neurons?Silvia Sapienza0Valentina Tedeschi1Barbara Apicella2Anna Pannaccione3Carmela Russo4Maria Josè Sisalli5Giorgia Magliocca6Stefania Loffredo7Agnese Secondo8Department of Neuroscience, Reproductive and Odontostomatological Sciences, University of Naples Federico II, Naples 80131, ItalyDepartment of Neuroscience, Reproductive and Odontostomatological Sciences, University of Naples Federico II, Naples 80131, ItalyIstituto di Scienze e Tecnologie per l′Energia e la Mobilità Sostenibili (STEMS)-CNR, Naples 80125, ItalyDepartment of Neuroscience, Reproductive and Odontostomatological Sciences, University of Naples Federico II, Naples 80131, ItalyIstituto di Scienze e Tecnologie per l′Energia e la Mobilità Sostenibili (STEMS)-CNR, Naples 80125, ItalyDepartment of Translational Medical Sciences, University of Naples Federico II, Naples 80131, ItalyDepartment of Neuroscience, Reproductive and Odontostomatological Sciences, University of Naples Federico II, Naples 80131, ItalyDepartment of Translational Medical Sciences, University of Naples Federico II, Naples 80131, Italy; Center for Basic and Clinical Immunology Research (CISI), University of Naples Federico II, WAO Center of Excellence, Naples 80131, ItalyDepartment of Neuroscience, Reproductive and Odontostomatological Sciences, University of Naples Federico II, Naples 80131, Italy; Corresponding author.Increased risk of neurodegenerative diseases has been envisaged for air pollution exposure. On the other hand, environmental risk factors, including air pollution, have been suggested for Amyotrophic Lateral Sclerosis (ALS) pathomechanism. Therefore, the neurotoxicity of ultrafine particulate matter (PM0.1) (PM < 0.1 μm size) and its sub-20 nm nanoparticle fraction (NP20) has been investigated in motor neuronal-like cells and primary cortical neurons, mainly affected in ALS. The present data showed that PM0.1 and NP20 exposure induced endoplasmic reticulum (ER) stress, as occurred in cortex and spinal cord of ALS mice carrying G93A mutation in SOD1 gene. Furthermore, NSC-34 motor neuronal-like cells exposed to PM0.1 and NP20 shared the same proteomic profile on some apoptotic factors with motor neurons treated with the L-BMAA, a neurotoxin inducing Amyotrophic Lateral Sclerosis/Parkinson–Dementia Complex (ALS/PDC). Of note ER stress induced by PM0.1 and NP20 in motor neurons was associated to pathological changes in ER morphology and dramatic reduction of organellar Ca2+ level through the dysregulation of the Ca2+-pumps SERCA2 and SERCA3, the Ca2+-sensor STIM1, and the Ca2+-release channels RyR3 and IP3R3. Furthermore, the mechanism deputed to ER Ca2+ refilling (e.g. the so called store operated calcium entry-SOCE) and the relative currents ICRAC were also altered by PM0.1 and NP20 exposure. Additionally, these carbonaceous particles caused the exacerbation of L-BMAA-induced ER stress and Caspase-9 activation. In conclusion, this study shows that PM0.1 and NP20 induced the aberrant expression of ER proteins leading to dysmorphic ER, organellar Ca2+ dysfunction, ER stress and neurotoxicity, providing putative correlations with the neurodegenerative process occurring in ALS.http://www.sciencedirect.com/science/article/pii/S0147651324001799Air pollutionCarbon PM[Ca2+]i homeostasisER-stressNeurotoxicitySOCE |
| spellingShingle | Silvia Sapienza Valentina Tedeschi Barbara Apicella Anna Pannaccione Carmela Russo Maria Josè Sisalli Giorgia Magliocca Stefania Loffredo Agnese Secondo Ultrafine particulate matter pollution and dysfunction of endoplasmic reticulum Ca2+ store: A pathomechanism shared with amyotrophic lateral sclerosis motor neurons? Ecotoxicology and Environmental Safety Air pollution Carbon PM [Ca2+]i homeostasis ER-stress Neurotoxicity SOCE |
| title | Ultrafine particulate matter pollution and dysfunction of endoplasmic reticulum Ca2+ store: A pathomechanism shared with amyotrophic lateral sclerosis motor neurons? |
| title_full | Ultrafine particulate matter pollution and dysfunction of endoplasmic reticulum Ca2+ store: A pathomechanism shared with amyotrophic lateral sclerosis motor neurons? |
| title_fullStr | Ultrafine particulate matter pollution and dysfunction of endoplasmic reticulum Ca2+ store: A pathomechanism shared with amyotrophic lateral sclerosis motor neurons? |
| title_full_unstemmed | Ultrafine particulate matter pollution and dysfunction of endoplasmic reticulum Ca2+ store: A pathomechanism shared with amyotrophic lateral sclerosis motor neurons? |
| title_short | Ultrafine particulate matter pollution and dysfunction of endoplasmic reticulum Ca2+ store: A pathomechanism shared with amyotrophic lateral sclerosis motor neurons? |
| title_sort | ultrafine particulate matter pollution and dysfunction of endoplasmic reticulum ca2 store a pathomechanism shared with amyotrophic lateral sclerosis motor neurons |
| topic | Air pollution Carbon PM [Ca2+]i homeostasis ER-stress Neurotoxicity SOCE |
| url | http://www.sciencedirect.com/science/article/pii/S0147651324001799 |
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