Combustion- and friction-derived magnetic air pollution nanoparticles in human hearts

Lilian Calderón-Garcidueñas; Angélica González-Maciel; Partha S. Mukherjee; Rafael Reynoso-Robles; Beatriz Pérez-Guillé; Carlos Gayosso-Chávez; Ricardo Torres-Jardón; Janet V. Cross; Imad A.M. Ahmed; Vassil V. Karloukovski; Barbara A. Maher

doi:10.1016/j.envres.2019.108567

Combustion- and friction-derived magnetic air pollution nanoparticles in human hearts

Lilian Calderón-Garcidueñas
, Angélica González-Maciel
, Partha S. Mukherjee
, Rafael Reynoso-Robles
, Beatriz Pérez-Guillé
, Carlos Gayosso-Chávez
, Ricardo Torres-Jardón
, Janet V. Cross
, Imad A.M. Ahmed
, Vassil V. Karloukovski
, Barbara A. Maher

Biomedical and Pharmaceutical Sciences

Research output: Contribution to journal › Article › peer-review

158 Scopus citations

Abstract

Air pollution is a risk factor for cardiovascular and Alzheimer's disease (AD). Iron-rich, strongly magnetic, combustion- and friction-derived nanoparticles (CFDNPs) are abundant in particulate air pollution. Metropolitan Mexico City (MMC) young residents have abundant brain CFDNPs associated with AD pathology. We aimed to identify if magnetic CFDNPs are present in urbanites' hearts and associated with cell damage. We used magnetic analysis and transmission electron microscopy (TEM) to identify heart CFDNPs and measured oxidative stress (cellular prion protein, PrP^C), and endoplasmic reticulum (ER) stress (glucose regulated protein, GRP78) in 72 subjects age 23.8 ± 9.4y: 63 MMC residents, with Alzheimer Continuum vs 9 controls. Magnetite/maghemite nanoparticles displaying the typical rounded crystal morphologies and fused surface textures of CFDNPs were more abundant in MMC residents' hearts. NPs, ∼2–10 × more abundant in exposed vs controls, were present inside mitochondria in ventricular cardiomyocytes, in ER, at mitochondria-ER contact sites (MERCs), intercalated disks, endothelial and mast cells. Erythrocytes were identified transferring ‘hitchhiking’ NPs to activated endothelium. Magnetic CFDNP concentrations and particle numbers ranged from 0.2 to 1.7 μg/g and ∼2 to 22 × 10⁹/g, respectively. Co-occurring with cardiomyocyte NPs were abnormal mitochondria and MERCs, dilated ER, and lipofuscin. MMC residents had strong left ventricular PrP^C and bi-ventricular GRP78 up-regulation. The health impact of up to ∼22 billion magnetic NPs/g of ventricular tissue are likely reflecting the combination of surface charge, ferrimagnetism, and redox activity, and includes their potential for disruption of the heart's electrical impulse pathways, hyperthermia and alignment and/or rotation in response to magnetic fields. Exposure to solid NPs appears to be directly associated with early and significant cardiac damage. Identification of strongly magnetic CFDNPs in the hearts of children and young adults provides an important novel layer of information for understanding CVD pathogenesis emphasizing the urgent need for prioritization of particulate air pollution control.

Original language	English
Article number	108567
Journal	Environmental Research
Volume	176
DOIs	https://doi.org/10.1016/j.envres.2019.108567
State	Published - Sep 2019

Funding

Donald MacLaren (Physics Department, University of Glasgow) kindly assisted with the HRTEM analysis. Thanks to Jessica Hammond for assistance with tissue sampling. Work funded in part by SEP-CONACYT # 255956, Mexico. Funding source had no involvement in study design; collection, analysis and interpretation of data; in the writing of the report; and in the decision to submit the article for publication. Donald MacLaren (Physics Department, University of Glasgow) kindly assisted with the HRTEM analysis. Thanks to Jessica Hammond for assistance with tissue sampling. Work funded in part by SEP-CONACYT # 255956 , Mexico. Funding source had no involvement in study design; collection, analysis and interpretation of data; in the writing of the report; and in the decision to submit the article for publication.

Funders	Funder number
255956
Glasgow Caledonian University

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

SDG 3 Good Health and Well-being
SDG 11 Sustainable Cities and Communities

Keywords

Air pollution
Alzheimer's continuum
Cardiomyocytes
Cardiovascular disease
Cellular prion protein PrP
Children
Combustion/friction-derived nanoparticles (CFDNPs)
Endoplasmic reticulum stress
Glucose-regulated protein 78 (GRP78)
Heart
Mitochondrial myocardial damage
Oxidative stress
Particulate matter (PM)
Ultrafine PM

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10.1016/j.envres.2019.108567

Cite this

Calderón-Garcidueñas, L., González-Maciel, A., Mukherjee, P. S., Reynoso-Robles, R., Pérez-Guillé, B., Gayosso-Chávez, C., Torres-Jardón, R., Cross, J. V., Ahmed, I. A. M., Karloukovski, V. V., & Maher, B. A. (2019). Combustion- and friction-derived magnetic air pollution nanoparticles in human hearts. Environmental Research, 176, Article 108567. https://doi.org/10.1016/j.envres.2019.108567

@article{aedaa65571134185a3e9d69b70f82aa0,

title = "Combustion- and friction-derived magnetic air pollution nanoparticles in human hearts",

abstract = "Air pollution is a risk factor for cardiovascular and Alzheimer's disease (AD). Iron-rich, strongly magnetic, combustion- and friction-derived nanoparticles (CFDNPs) are abundant in particulate air pollution. Metropolitan Mexico City (MMC) young residents have abundant brain CFDNPs associated with AD pathology. We aimed to identify if magnetic CFDNPs are present in urbanites' hearts and associated with cell damage. We used magnetic analysis and transmission electron microscopy (TEM) to identify heart CFDNPs and measured oxidative stress (cellular prion protein, PrPC), and endoplasmic reticulum (ER) stress (glucose regulated protein, GRP78) in 72 subjects age 23.8 ± 9.4y: 63 MMC residents, with Alzheimer Continuum vs 9 controls. Magnetite/maghemite nanoparticles displaying the typical rounded crystal morphologies and fused surface textures of CFDNPs were more abundant in MMC residents' hearts. NPs, ∼2–10 × more abundant in exposed vs controls, were present inside mitochondria in ventricular cardiomyocytes, in ER, at mitochondria-ER contact sites (MERCs), intercalated disks, endothelial and mast cells. Erythrocytes were identified transferring {\textquoteleft}hitchhiking{\textquoteright} NPs to activated endothelium. Magnetic CFDNP concentrations and particle numbers ranged from 0.2 to 1.7 μg/g and ∼2 to 22 × 109/g, respectively. Co-occurring with cardiomyocyte NPs were abnormal mitochondria and MERCs, dilated ER, and lipofuscin. MMC residents had strong left ventricular PrPC and bi-ventricular GRP78 up-regulation. The health impact of up to ∼22 billion magnetic NPs/g of ventricular tissue are likely reflecting the combination of surface charge, ferrimagnetism, and redox activity, and includes their potential for disruption of the heart's electrical impulse pathways, hyperthermia and alignment and/or rotation in response to magnetic fields. Exposure to solid NPs appears to be directly associated with early and significant cardiac damage. Identification of strongly magnetic CFDNPs in the hearts of children and young adults provides an important novel layer of information for understanding CVD pathogenesis emphasizing the urgent need for prioritization of particulate air pollution control.",

keywords = "Air pollution, Alzheimer's continuum, Cardiomyocytes, Cardiovascular disease, Cellular prion protein PrP, Children, Combustion/friction-derived nanoparticles (CFDNPs), Endoplasmic reticulum stress, Glucose-regulated protein 78 (GRP78), Heart, Mitochondrial myocardial damage, Oxidative stress, Particulate matter (PM), Ultrafine PM",

author = "Lilian Calder{\'o}n-Garcidue{\~n}as and Ang{\'e}lica Gonz{\'a}lez-Maciel and Mukherjee, \{Partha S.\} and Rafael Reynoso-Robles and Beatriz P{\'e}rez-Guill{\'e} and Carlos Gayosso-Ch{\'a}vez and Ricardo Torres-Jard{\'o}n and Cross, \{Janet V.\} and Ahmed, \{Imad A.M.\} and Karloukovski, \{Vassil V.\} and Maher, \{Barbara A.\}",

note = "Publisher Copyright: {\textcopyright} 2019 Elsevier Inc.",

year = "2019",

month = sep,

doi = "10.1016/j.envres.2019.108567",

language = "English",

volume = "176",

journal = "Environmental Research",

issn = "0013-9351",

publisher = "Academic Press Inc.",

}

Calderón-Garcidueñas, L, González-Maciel, A, Mukherjee, PS, Reynoso-Robles, R, Pérez-Guillé, B, Gayosso-Chávez, C, Torres-Jardón, R, Cross, JV, Ahmed, IAM, Karloukovski, VV & Maher, BA 2019, 'Combustion- and friction-derived magnetic air pollution nanoparticles in human hearts', Environmental Research, vol. 176, 108567. https://doi.org/10.1016/j.envres.2019.108567

TY - JOUR

T1 - Combustion- and friction-derived magnetic air pollution nanoparticles in human hearts

AU - Calderón-Garcidueñas, Lilian

AU - González-Maciel, Angélica

AU - Mukherjee, Partha S.

AU - Reynoso-Robles, Rafael

AU - Pérez-Guillé, Beatriz

AU - Gayosso-Chávez, Carlos

AU - Torres-Jardón, Ricardo

AU - Cross, Janet V.

AU - Ahmed, Imad A.M.

AU - Karloukovski, Vassil V.

AU - Maher, Barbara A.

PY - 2019/9

Y1 - 2019/9

N2 - Air pollution is a risk factor for cardiovascular and Alzheimer's disease (AD). Iron-rich, strongly magnetic, combustion- and friction-derived nanoparticles (CFDNPs) are abundant in particulate air pollution. Metropolitan Mexico City (MMC) young residents have abundant brain CFDNPs associated with AD pathology. We aimed to identify if magnetic CFDNPs are present in urbanites' hearts and associated with cell damage. We used magnetic analysis and transmission electron microscopy (TEM) to identify heart CFDNPs and measured oxidative stress (cellular prion protein, PrPC), and endoplasmic reticulum (ER) stress (glucose regulated protein, GRP78) in 72 subjects age 23.8 ± 9.4y: 63 MMC residents, with Alzheimer Continuum vs 9 controls. Magnetite/maghemite nanoparticles displaying the typical rounded crystal morphologies and fused surface textures of CFDNPs were more abundant in MMC residents' hearts. NPs, ∼2–10 × more abundant in exposed vs controls, were present inside mitochondria in ventricular cardiomyocytes, in ER, at mitochondria-ER contact sites (MERCs), intercalated disks, endothelial and mast cells. Erythrocytes were identified transferring ‘hitchhiking’ NPs to activated endothelium. Magnetic CFDNP concentrations and particle numbers ranged from 0.2 to 1.7 μg/g and ∼2 to 22 × 109/g, respectively. Co-occurring with cardiomyocyte NPs were abnormal mitochondria and MERCs, dilated ER, and lipofuscin. MMC residents had strong left ventricular PrPC and bi-ventricular GRP78 up-regulation. The health impact of up to ∼22 billion magnetic NPs/g of ventricular tissue are likely reflecting the combination of surface charge, ferrimagnetism, and redox activity, and includes their potential for disruption of the heart's electrical impulse pathways, hyperthermia and alignment and/or rotation in response to magnetic fields. Exposure to solid NPs appears to be directly associated with early and significant cardiac damage. Identification of strongly magnetic CFDNPs in the hearts of children and young adults provides an important novel layer of information for understanding CVD pathogenesis emphasizing the urgent need for prioritization of particulate air pollution control.

AB - Air pollution is a risk factor for cardiovascular and Alzheimer's disease (AD). Iron-rich, strongly magnetic, combustion- and friction-derived nanoparticles (CFDNPs) are abundant in particulate air pollution. Metropolitan Mexico City (MMC) young residents have abundant brain CFDNPs associated with AD pathology. We aimed to identify if magnetic CFDNPs are present in urbanites' hearts and associated with cell damage. We used magnetic analysis and transmission electron microscopy (TEM) to identify heart CFDNPs and measured oxidative stress (cellular prion protein, PrPC), and endoplasmic reticulum (ER) stress (glucose regulated protein, GRP78) in 72 subjects age 23.8 ± 9.4y: 63 MMC residents, with Alzheimer Continuum vs 9 controls. Magnetite/maghemite nanoparticles displaying the typical rounded crystal morphologies and fused surface textures of CFDNPs were more abundant in MMC residents' hearts. NPs, ∼2–10 × more abundant in exposed vs controls, were present inside mitochondria in ventricular cardiomyocytes, in ER, at mitochondria-ER contact sites (MERCs), intercalated disks, endothelial and mast cells. Erythrocytes were identified transferring ‘hitchhiking’ NPs to activated endothelium. Magnetic CFDNP concentrations and particle numbers ranged from 0.2 to 1.7 μg/g and ∼2 to 22 × 109/g, respectively. Co-occurring with cardiomyocyte NPs were abnormal mitochondria and MERCs, dilated ER, and lipofuscin. MMC residents had strong left ventricular PrPC and bi-ventricular GRP78 up-regulation. The health impact of up to ∼22 billion magnetic NPs/g of ventricular tissue are likely reflecting the combination of surface charge, ferrimagnetism, and redox activity, and includes their potential for disruption of the heart's electrical impulse pathways, hyperthermia and alignment and/or rotation in response to magnetic fields. Exposure to solid NPs appears to be directly associated with early and significant cardiac damage. Identification of strongly magnetic CFDNPs in the hearts of children and young adults provides an important novel layer of information for understanding CVD pathogenesis emphasizing the urgent need for prioritization of particulate air pollution control.

KW - Air pollution

KW - Alzheimer's continuum

KW - Cardiomyocytes

KW - Cardiovascular disease

KW - Cellular prion protein PrP

KW - Children

KW - Combustion/friction-derived nanoparticles (CFDNPs)

KW - Endoplasmic reticulum stress

KW - Glucose-regulated protein 78 (GRP78)

KW - Heart

KW - Mitochondrial myocardial damage

KW - Oxidative stress

KW - Particulate matter (PM)

KW - Ultrafine PM

UR - https://www.scopus.com/pages/publications/85069687126

U2 - 10.1016/j.envres.2019.108567

DO - 10.1016/j.envres.2019.108567

M3 - Article

C2 - 31344533

AN - SCOPUS:85069687126

SN - 0013-9351

VL - 176

JO - Environmental Research

JF - Environmental Research

M1 - 108567

ER -

Combustion- and friction-derived magnetic air pollution nanoparticles in human hearts

Abstract

Funding

UN SDGs

Keywords

Access to Document

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