Chemical oxidative potential and cellular oxidative stress from open

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Ecotoxicology and Human Environmental Health

Chemical oxidative potential and cellular oxidative stress from open biomass burning aerosol Wing Y Tuet, Fobang Liu, Nilmara de Oliveira Alves, Shierly Fok, Paulo Artaxo, Perola C Vasconcellos, Julie Champion, and Nga Lee Ng Environ. Sci. Technol. Lett., Just Accepted Manuscript • DOI: 10.1021/acs.estlett.9b00060 • Publication Date (Web): 15 Feb 2019 Downloaded from http://pubs.acs.org on February 17, 2019

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Environmental Science & Technology Letters

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Chemical oxidative potential and cellular oxidative stress from open biomass burning

2

aerosol

3

Wing Y. Tuet1, Fobang Liu1, Nilmara de Oliveira Alves2, Shierly Fok1, Paulo Artaxo3, Pérola

4

Vasconcellos4, Julie A. Champion1, Nga L. Ng1,5*

5

1School

6

GA 30332, USA

7

2School

8

3Institute

of Physics, University of São Paulo, São Paulo, 05508, Brazil

9

4Institute

of Chemistry, University of São Paulo, São Paulo, 05508, Brazil

of Chemical and Biomolecular Engineering, Georgia Institute of Technology, Atlanta,

of Medicine, University of São Paulo, São Paulo, 03178, Brazil

10

5School

11

30332, USA

12

Corresponding Author

13

*email:

of Earth and Atmospheric Sciences, Georgia Institute of Technology, Atlanta, GA

[email protected]

ACS Paragon Plus Environment

1


14

Keywords: oxidative potential, reactive oxygen/nitrogen species, biomass burning, particulate

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matter

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Abstract

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Particulate matter (PM) exposure is a leading global human health risk. In this

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study, water-soluble oxidative potential (OP) and intracellular reactive oxygen and

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nitrogen species (ROS/RNS) production were measured for open biomass burning

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aerosol collected from the Brazilian Amazon. Compared to ambient samples collected

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from Atlanta and laboratory-generated secondary organic aerosol (SOA), biomass

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burning aerosol had comparable OP and induced higher levels of ROS/RNS. Compared

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to regressed OP ranges for biomass burning factors resolved using source apportionment

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in prior studies, the samples investigated in this study spanned a wider OP range,

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suggesting that concentration addition may not be applicable for OP measurements. The

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discrepancy between ROS/RNS estimated using laboratory polycyclic aromatic

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hydrocarbons (PAHs) solution mixtures and ROS/RNS measured for the water-soluble

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hydrophobic fraction of Amazon filter samples further supports this conclusion. These

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results have important implications as many previous studies are based on linear

30

regressions that assume concentration addition. Finally, a significant correlation was

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observed between ROS/RNS and levoglucosan concentrations although exposure to

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pure solutions of levoglucosan induced negligible ROS/RNS. These results demonstrate

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that levoglucosan may be considered as predictors for ROS/RNS even though

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concentration addition may not be an applicable mixture effect model.


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Introduction

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Exposure to inhalable particulate matter (PM) is a leading cause of premature

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death worldwide.1, 2 According to recent data from the World Health Organization (WHO),

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an estimated 7 million premature deaths each year may be attributed to PM inhalation,

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and 9 out of 10 individuals worldwide breathe air containing high levels of pollutants.3

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Over the past few decades, multiple epidemiological studies have reported associations

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between elevated PM concentrations and increased incidences of cardiopulmonary

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morbidity and mortality.2, 4-9 The specific mechanism by which PM exposure results in

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adverse health outcomes is still unclear. Nevertheless, toxicological studies have

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suggested a possible mechanism whereby oxidative stress is induced through PM-

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initiated oxidant production,10-13 and multiple assays14-17 have been developed to

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measure the production of these oxidants.

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Recently, several studies on the relative toxicities of different aerosol subtypes

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resolved using various source apportionment methods reported a high oxidative potential

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(OP) for biomass burning aerosol (BURN18 and biomass burning organic aerosol,

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BBOA19). However, direct measures of biomass burning aerosol toxicity are scarce20, 21

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or include measures that cannot be readily compared to the toxicity of other aerosol

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subtypes.22-25 Furthermore, the BURN18 and BBOA19 factors were resolved assuming a

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concentration addition model for oxidative potentials, which may not be applicable

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according to recent studies.26-28


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The Brazilian Amazon presents an ideal environment for studying the toxicity of

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biomass burning aerosol with minimal influence from industrial emissions or other

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sources.29, 30 The region contains about 40% of the world’s remaining tropical rainforests

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and has been severely affected by deforestation and open biomass burning emissions in

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recent years.31 These activities represent a major source of inhalable PM,32 especially

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during the dry season, and the increased PM has been shown to have a significant health

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impact on the surrounding population (e.g., increased incidence of respiratory

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diseases).22, 29, 33

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In the present study, OP and reactive oxygen and nitrogen species (ROS/RNS)

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production were measured for ambient PM samples collected in the southwestern region

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of the Brazilian Amazon during dry and wet seasons. The dithiothreitol (DTT) assay was

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utilized to measure OP, which may represent the concentration of redox-active species

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present in the PM sample.34 A cellular assay involving murine alveolar macrophages was

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employed to measure intracellular ROS/RNS produced as a result of PM exposure.16, 28,

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35

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composition were explored to identify and elucidate components associated with biomass

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burning aerosol toxicity.

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Methods

Correlations between aerosol toxicity measures (OP or ROS/RNS levels) and chemical


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PM collection and extraction. Ambient PM10 samples were collected from a site

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(8.69⁰ S, 63.87⁰ W) located in the southwestern region of the Brazilian Amazon, about 5

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km north of Porto Velho,36 during the dry (28 July 2011 – 10 October 2011) and wet (10

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October 2011 – 15 March 2012) seasons. High-volume samplers with a flow rate of 1.3

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m3 min-1 were used to collect particles onto pre-baked quartz filters. Concentrations of

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organic carbon (OC) and elemental carbon (EC) were determined using thermal-optical

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transmittance (TOT, Sunset Laboratory Inc.), while concentrations of monosaccharide

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anhydrides (levoglucosan, mannosan, and galactosan) were measured using high-

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performance anion-exchange chromatography coupled to electrospray ionization mass

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spectrometry (HPAEC/ESI-MS).37 Concentrations of various polycyclic aromatic

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hydrocarbons (PAHs) and their derivatives (fluorene, phenanthrene, anthracene,

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luoranthene, pyrene, retene, benzo(a)anthracene, chrysene, benzo(b)fluoranthene,

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benzo(k)fluoranthene,

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dibenzo(a,h)anthracene, and benzo(g,h,i)perylene), oxygenated-PAHs (oxy-PAHs; 9-

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fluorenone, 9,10-anthraquinone, 2-methylanthraquinone, and benzo(a)anthracene-7,12-

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dione), and nitrogenated-PAHs (nitro-PAHs; 9-nitrophenanthrene, 3-nitrophenanthrene,

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2-nitrophenanthrene, 2-nitroanthracene, 3-nitrofluoranthene, 2-nitrofluoranthene, 1-

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nitropyrene,

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nitrobenzo(a)pyrene) were determined using gas chromatography-mass spectrometry

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(GC-MS, Agilent 7820A).37,

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these samples can be found in Oliveira Alves et al. 37, 38

benzo(e)pyrene,

4-nitropyrene,

benzo(a)pyrene,

7-nitrobenzo(a)anthracene,

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indenol(1,2,3-c,d)pyrene,

6-nitrochrysene,

and

6-

Mass concentrations and detailed chemical analysis of


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Collected samples were extracted following pre-established procedures for OP

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determination39 and intracellular ROS/RNS measurement.16 Briefly, filters were

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submerged in extraction media (DI water for OP and cell culture media (RPMI-1640) for

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ROS/RNS) and sonicated for 30 min using an Ultrasonic Cleanser (VWR International).

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Extracts were filtered using a 0.45 µm polytetrafluoroethylene (PTFE) syringe filter

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(Fisherbrand™) to remove insoluble material post-sonication34 and extracts for cellular

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exposure were supplemented with 10% fetal bovine serum (FBS).16

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Polycyclic aromatic hydrocarbon solutions. Laboratory solutions of pure oxy- and

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nitro-PAHs were prepared to final concentrations of 1 ng µL-1 (9-fluorenone), 2 ng µL-1 (1-

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nitropyrene, 6-nitrochrysene), and 4 ng µL-1 (2-methylanthraquinone) and diluted 1000x

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prior to cellular exposure. Concentrations were chosen to span the range observed for

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these species in the collected samples.38

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Oxidative potential. Intrinsic water-soluble OP as measured by DTT was measured

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using a semi-automated DTT system.34 Briefly, the method consisted of three major

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steps: (1) oxidation of DTT by redox-active species, (2) reaction of unoxidized DTT with

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5,5-dithio-bis-(2-nitrobenzoic acid) (DTNB) to form 2-nitro-5-mercaptobenoic acid (TNB),

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and (3) measurement of TNB at 412 nm using an online spectrophotometer (Ocean

111

Optics, Inc., Dunedin, USA).

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Intracellular ROS/RNS measurement. Murine alveolar macrophages (MH-S,

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ATCC®CRL-2019™), maintained in RPMI-1640 media supplemented with 10% FBS, 1%


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penicillin-streptomycin, and 50 µM β-mercaptoethanol at 37°C and 5% CO2, were

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exposed to PM extracts or laboratory-prepared solutions of pure oxy- and nitro-PAHs for

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24 hrs. Intracellular ROS/RNS levels were measured post-exposure following the

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methodology described in Tuet et al.16 (cell density: 2 x 104 cells well-1; ROS/RNS probe:

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carboxy-H2DCFDA, Molecular Probes C-400, 10 µM). A detailed description of ROS/RNS

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measurement is provided in supporting information and have been described in Tuet et

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al.16, 28, 35

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Cellular

metabolic

activity.

MTT

(3-(4,5-dimethylthiazol-2-yl)-2,5-

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diphenyltetrazolium bromide) was used to assess cellular metabolic activity post PM

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exposure following manufacturer’s instruments (Biotium). No decrease of metabolic

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activity was observed upon exposure to filter extract.

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Statistical analysis. Linear regressions were evaluated using Pearson’s correlation

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coefficient with the significance determined using multiple imputation40 and a 95%

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confidence level.

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Results and Discussion

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Ambient and chamber context. Open biomass burning aerosol collected from the

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Brazilian Amazon during both dry (intense biomass burning)37, 38 and wet (low to moderate

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biomass burning)37,

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manner (Fig. S1). Over the same dose range, Amazon aerosol generally induced higher

38

seasons induced ROS/RNS production in a dose-dependent


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ROS/RNS levels (AUC per µg of PM) than ambient samples collected around the Greater

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Atlanta region16 and secondary organic aerosol (SOA) generated from a variety of

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biogenic and anthropogenic precursors28,

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during the dry season. The high ROS/RNS production observed for biomass burning

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aerosol suggests that oxidative stress may be a likely mechanism by which biomass

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burning aerosol exposure results in the adverse health endpoints reported in prior

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studies.41, 42 In particular, de Oliveira Alves et al.22 showed that biomass burning aerosol

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(the same samples used in this work) induced oxidative stress in human lung cells.

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Furthermore, previous studies have shown that exposure to biomass burning aerosol was

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associated with increased phlegm production in humans.42 A well-established link exists

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between oxidative stress, characterized by increased oxidant production such as

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ROS/RNS, and mucus hypersecretion,43-46 further supporting oxidative stress as a

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possible mechanism for the health effects of biomass burning aerosol. Increased oxidant

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production may also result in other cellular damages, including DNA/RNA damage,

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protein oxidation, and lipid peroxidation.47, 48 A higher occurrence of DNA damage have

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been found in a prior study23 from exposure to biomass burning aerosol collected from

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the Brazilian Amazon. These results are in agreement with the ROS/RNS measurements

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obtained in this study, where higher ROS/RNS levels were observed for samples

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collected during the dry season (Fig. S2).

35

(Fig. 1), especially for aerosol collected


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In terms of OP, biomass burning aerosol had redox activities comparable to that

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observed for ambient samples collected from multiple sites in Atlanta19, 39, 49 and chamber

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SOA generated from different precursors50 (Fig.1). Additionally, higher DTT activities

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were observed for samples collected during the dry season compared to the wet season

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(Fig.S2). Previous studies using factor analysis and linear regression reported that BBOA

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resolved from ambient high resolution time-of-flight aerosol mass spectrometer (AMS)

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data was the most redox-active among different aerosol subtypes.19 The higher redox

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activity observed during the dry season is therefore consistent with the more intense open

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biomass burning that is characteristic of the dry season. It is also interesting to note that

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many DTT activities measured for open biomass burning aerosol collected from the

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Amazon region overlap the ranges in between two biomass burning aerosol factors

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(BBOA and BURN) resolved using different source apportionment methods.18, 19 Note that

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aerosol samples collected in this study were PM10 while PM2.5 samples were analyzed in

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the BBOA and BURN studies.18,

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accounted for ~80% mass concentration of PM10 during the dry season at the same

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sampling site of this study.32 To our knowledge, the measurements acquired in this study

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represent the first direct measures of aerosol oxidative potential during intense open

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biomass burning from the Amazon region. It is promising that there exists some overlap

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between direct measures and regressed values. However, it should be noted that the

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direct measurements of open biomass burning OP span a range that extends lower than

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that predicted by either regression study,18, 19 although components from other types of

19

However, a previous study showed that PM2.5


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aerosol might contribute to the lower range in this study. Additionally, this study confirms

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our previous conclusion16, 35 that there is not one simple correlation between oxidative

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potential and cellular ROS/RNS levels for different PM samples, while low DTT activity

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will likely correspond to a low cellular response (Fig.1).

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PM constituents associated with ROS/RNS production. PM-induced ROS/RNS

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production (AUC per m3 of air) was significantly correlated with concentrations of various

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monosaccharide anhydrides (levoglucosan, mannosan, and galactosan) (Fig. 2). These

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monosaccharides are known tracers for biomass burning and ratios of different

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monosaccharides may be used to infer the source of biomass burning.51 For wet season

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samples, low but appreciable levels of ROS/RNS were induced despite negligible

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amounts of all three monosaccharides. These results suggest that monosaccharide

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concentrations may serve not only as a tracer for biomass burning, but also as a good

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predictor for ROS/RNS produced as a result of exposure to biomass burning aerosol.

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Note that exposure to pure levoglucosan solutions (prepared in the laboratory) induced

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negligible ROS/RNS production over the range observed in the collected samples (Fig.

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S3).

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ROS/RNS levels were also significantly correlated with concentrations of OC and

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EC (Fig. S4). Prior studies involving both cellular and acellular assays have highlighted

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the importance of organic species in terms of aerosol toxicity.28,

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correlations between ROS/RNS production and organic species (water-soluble organic

35, 52-55

For instance,


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carbon and brown carbon) have been previously reported using the same cellular assay

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used in this study.16 Another study using a different cellular assay reported significant

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correlations between the biomass burning fraction of water-soluble organic carbon and

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ROS activity as well.54 Additionally, a meta-analysis performed using data from multiple

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epidemiological studies found that the relative health risk per mass of EC was about an

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order of magnitude greater than that of PM2.5.56 This indicates that EC was a tracer for

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many chemical species co-emitted during biomass burning.

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To gain further insight into the organic species associated with biomass burning

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aerosol toxicity, correlations between the concentrations of multiple PAHs and ROS/RNS

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levels were evaluated. The sum of all PAHs detected in the biomass burning samples

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was not significantly correlated with ROS/RNS production (Fig. S5a). For samples

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collected during the wet season, a low level of ROS/RNS was induced regardless of total

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PAH concentration (blue markers in Fig. S5a). A larger range of ROS/RNS was observed

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for samples collected during the dry season, although no significant correlation was

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found. Similar relationships were observed for individual PAHs detected. Previous studies

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have shown that oxy-PAHs are more redox active and induce the formation of more

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ROS/RNS upon cellular exposure.35, 50, 57, 58 Correlations between oxy- and nitro-PAHs

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and ROS/RNS, however, were also not significant for the majority of individual oxy- and

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nitro-PAHs as well as the sum of oxy- and nitro-PAHs (Fig. S5). The lack of correlation

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did not necessarily indicate a lack of response. As in laboratory experiments, exposure


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to pure solutions of four oxy- and nitro-PAHs (1-nitropyrene, 6-nitrochrysene, 9-

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fluorenone, and 2-methylanthraquinone) induced considerable levels of ROS/RNS

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production (Fig. S6). These specific compounds were chosen due to their demonstrated

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toxicity, including DNA adduct formation, carcinogenicity, and cytotoxicity.58-62 In

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particular, 9-fluorenone has been shown to induce ROS production61 and a significant

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correlation between concentrations of 9-fluorenone and ROS/RNS was observed for the

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biomass burning samples (Fig. S7). Together with the results obtained for levoglucosan,

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these results suggest that there is not a simple relationship between correlation and

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causation, and caution must be exercised when interpreting correlation results.

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Compared to the Pearson correlation, it is suggested to use non-parameter methods in

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statistical analysis. It should however be noted that ambient samples contain other

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compounds that were not identified in this study. These compounds may induce

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ROS/RNS production, which may potentially affect correlation results.

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To gauge the relative contribution of oxy- and nitro-PAHs to ROS/RNS production

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and to evaluate the applicability of concentration addition as an effect model, an estimated

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ROS/RNS level was calculated using individual dose-response curves (Fig. S6) and

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concentrations for the four oxy- and nitro-PAHs (Fig. 3, aqua bars). ROS/RNS produced

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as a result of exposure to the water-soluble hydrophobic fraction of biomass burning

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aerosol collected from the Brazilian Amazon, obtained by passing the water-soluble

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extract through a C-18 column,63 was also measured for comparison (Fig. 3, pink bars).


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For the eight samples investigated, the ROS/RNS estimated using oxy- and nitro-PAHs

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was lower than that measured for the water-soluble hydrophobic fraction for six samples

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and higher for two samples. These results directly demonstrate that concentration

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addition is not an accurate effect model for estimating cellular responses induced as a

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result of aerosol exposure, in agreement with recent findings regarding the non-additivity

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of redox activities.26-28

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Implications. Results from this study represent the first direct measurements for

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OP and ROS/RNS of open biomass burning aerosol from the Amazon region. The

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perspective gained on the relative toxicity of biomass burning aerosol in the context of

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other aerosol subtypes as well as the information obtained from the differences observed

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between samples collected during dry and wet seasons can guide future studies to focus

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more on biomass burning emissions due to its high relative toxicity. Furthermore, the

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discrepancies between OP measured in this study and biomass burning factors resolved

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from source apportionment methods (BURN and BBOA) and between ROS/RNS

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estimated using oxy- and nitro-PAHs and ROS/RNS measured demonstrates that

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concentration addition may not be an applicable mixture effect model for both OP and

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ROS/RNS measurements. These results have important implications as many previous

250

studies are based on linear regressions that assume concentration addition.18, 19, 64

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Supporting Information

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The supporting material consists of a detailed description of ROS/RNS measurement

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and seven figures.

255 256

AUTHOR INFORMATION

257

Corresponding author

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Nga Lee Ng: Phone: (404) 385 2148; Email: [email protected]

259 260

Notes

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The authors declare no competing financial interest.

262 263

ACKNOWLEDGMENT

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This work was supported by the Health Effects Institute under research agreement No.

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4943-RFA13-2/14-4. W. Y. Tuet acknowledges support by the National Science

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Foundation Graduate Research Fellowship under Grant No. DGE-1650044. P. Artaxo

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acknowledges support from FAPESP under Grants 2013/05014-0 and 2017/17047-0 and

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CNPq. The authors thank Fernando Morais and Fábio Jorge for assisting with sample

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collection in the Amazon and acknowledge support from the LBA Central office at INPA,

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Manaus. The authors also thank Rodney J. Weber for use of the DTT assay setup.


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ABBREVIATIONS

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PM: particulate matter; ROS/RNS: reactive oxygen and nitrogen species; DTT:

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dithiothreitol; OP: oxidative potential

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30. Marle, M. J.; Field, R. D.; Werf, G. R.; Estrada de Wagt, I. A.; Houghton, R. A.; Rizzo, L. V.; Artaxo, P.; Tsigaridis, K., Fire and deforestation dynamics in Amazonia (1973–2014). Global. Biogeochem. Cy. 2017, 31 (1), 24-38. 31. Laurance, W. F.; Cochrane, M. A.; Bergen, S.; Fearnside, P. M.; Delamônica, P.; Barber, C.; D'Angelo, S.; Fernandes, T., The Future of the Brazilian Amazon. Science 2001, 291 (5503), 438-439. 32. Artaxo, P.; Rizzo, L. V.; Brito, J. F.; Barbosa, H. M.; Arana, A.; Sena, E. T.; Cirino, G. G.; Bastos, W.; Martin, S. T.; Andreae, M. O., Atmospheric aerosols in Amazonia and land use change: from natural biogenic to biomass burning conditions. Faraday. Discuss. 2013, 165, 203235. 33. Jacobson, L. d. S. V.; de Souza Hacon, S.; de Castro, H. A.; Ignotti, E.; Artaxo, P.; Saldiva, P. H. N.; de Leon, A. C. M. P., Acute effects of particulate matter and black carbon from seasonal fires on peak expiratory flow of schoolchildren in the Brazilian Amazon. PloS one 2014, 9 (8), e104177. 34. Fang, T.; Verma, V.; Guo, H.; King, L.; Edgerton, E.; Weber, R., A semi-automated system for quantifying the oxidative potential of ambient particles in aqueous extracts using the dithiothreitol (DTT) assay: results from the Southeastern Center for Air Pollution and Epidemiology (SCAPE). Atmos. Meas. Tech. 2015, 8 (1), 471-482. 35. Tuet, W. Y.; Chen, Y.; Fok, S.; Champion, J. A.; Ng, N. L., Inflammatory responses to secondary organic aerosols (SOA) generated from biogenic and anthropogenic precursors. Atmos. Chem. Phys. 2017, 17 (18), 11423-11440. 36. Brito, J.; Rizzo, L. V.; Morgan, W. T.; Coe, H.; Johnson, B.; Haywood, J.; Longo, K.; Freitas, S.; Andreae, M. O.; Artaxo, P., Ground-based aerosol characterization during the South American Biomass Burning Analysis (SAMBBA) field experiment. Atmos. Chem. Phys. 2014, 14 (22), 12069-12083. 37. de Oliveira Alves, N.; Brito, J.; Caumo, S.; Arana, A.; de Souza Hacon, S.; Artaxo, P.; Hillamo, R.; Teinilä, K.; de Medeiros, S. R. B.; de Castro Vasconcellos, P., Biomass burning in the Amazon region: Aerosol source apportionment and associated health risk assessment. Atmos. Environ. 2015, 120, 277-285. 38. de Oliveira Galvão, M. F.; de Oliveira Alves, N.; Ferreira, P. A.; Caumo, S.; de Castro Vasconcellos, P.; Artaxo, P.; de Souza Hacon, S.; Roubicek, D. A.; de Medeiros, S. R. B., Biomass burning particles in the Brazilian Amazon region: Mutagenic effects of nitro and oxyPAHs and assessment of health risks. Environ. Pollut. 2018, 233, 960-970. 39. Fang, T.; Guo, H.; Verma, V.; Peltier, R. E.; Weber, R. J., PM2.5 water-soluble elements in the southeastern United States: automated analytical method development, spatiotemporal distributions, source apportionment, and implications for heath studies. Atmos. Chem. Phys. 2015, 15 (20), 11667-11682. 40. Pan, Q.; Shimizu, I. In Imputation Variance Estimation by Multiple Imputation Method for the National Hospital Discharge Survey, JSM Proceedings, 2009; 2009; pp 1106-1114. 41. Arbex, M. A.; Martins, L. C.; de Oliveira, R. C.; Pereira, L. A. A.; Arbex, F. F.; Cançado, J. E. D.; Saldiva, P. H. N.; Braga, A. L. F., Air pollution from biomass burning and asthma hospital admissions in a sugar cane plantation area in Brazil. J. Epidemiol. Community. Health. 2007, 61 (5), 395-400. 42. Regalado, J.; Pérez-Padilla, R.; Sansores, R.; Paramo Ramirez, J. I.; Brauer, M.; Paré, P.; Vedal, S., The effect of biomass burning on respiratory symptoms and lung function in rural Mexican women. Am. J. Respir. Crit. Care. Med. 2006, 174 (8), 901-905.


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43. MacNee, W.; Rahman, I., Is oxidative stress central to the pathogenesis of chronic obstructive pulmonary disease? Trends. Mol. Med. 2001, 7 (2), 55-62. 44. McGuinness, A. J. A.; Sapey, E., Oxidative stress in COPD: sources, markers, and potential mechanisms. J. Clin. Med. 2017, 6 (2), 21. 45. Santus, P.; Corsico, A.; Solidoro, P.; Braido, F.; Di Marco, F.; Scichilone, N., Oxidative stress and respiratory system: pharmacological and clinical reappraisal of N-acetylcysteine. COPD 2014, 11 (6), 705-717. 46. Repine, J. E.; Bast, A.; Lankhorst, I.; Group, O. S. S., Oxidative stress in chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care. Med. 1997, 156 (2), 341-357. 47. Wiseman, H.; Halliwell, B., Damage to DNA by reactive oxygen and nitrogen species: role in inflammatory disease and progression to cancer. Biochem. J. 1996, 313 (Pt 1), 17-29. 48. Hensley, K.; Robinson, K. A.; Gabbita, S. P.; Salsman, S.; Floyd, R. A., Reactive oxygen species, cell signaling, and cell injury. Free. Radic. Biol. Med. 2000, 28 (10), 1456-1462. 49. Verma, V.; Fang, T.; Guo, H.; King, L.; Bates, J.; Peltier, R.; Edgerton, E.; Russell, A.; Weber, R., Reactive oxygen species associated with water-soluble PM2.5 in the southeastern United States: spatiotemporal trends and source apportionment. Atmos. Chem. Phys. 2014, 14 (23), 12915-12930. 50. Tuet, W. Y.; Chen, Y.; Xu, L.; Fok, S.; Gao, D.; Weber, R. J.; Ng, N. L., Chemical oxidative potential of secondary organic aerosol (SOA) generated from the photooxidation of biogenic and anthropogenic volatile organic compounds. Atmos. Chem. Phys. 2017, 17 (2), 839853. 51. Simoneit, B. R., Biomass burning—a review of organic tracers for smoke from incomplete combustion. Appl. Geochem. 2002, 17 (3), 129-162. 52. Li, N.; Sioutas, C.; Cho, A.; Schmitz, D.; Misra, C.; Sempf, J.; Wang, M.; Oberley, T.; Froines, J.; Nel, A., Ultrafine particulate pollutants induce oxidative stress and mitochondrial damage. Environ. Health Perspect. 2003, 111 (4), 455. 53. Kleinman, M. T.; Hamade, A.; Meacher, D.; Oldham, M.; Sioutas, C.; Chakrabarti, B.; Stram, D.; Froines, J. R.; Cho, A. K., Inhalation of concentrated ambient particulate matter near a heavily trafficked road stimulates antigen-induced airway responses in mice. J. Air. Waste. Manag. Assoc. 2005, 55 (9), 1277-1288. 54. Hamad, S. H.; Shafer, M. M.; Kadhim, A. K. H.; Al-Omran, S. M.; Schauer, J. J., Seasonal trends in the composition and ROS activity of fine particulate matter in Baghdad, Iraq. Atmos. Environ. 2015, 100, 102-110. 55. Verma, V.; Wang, Y.; El-Afifi, R.; Fang, T.; Rowland, J.; Russell, A. G.; Weber, R. J., Fractionating ambient humic-like substances (HULIS) for their reactive oxygen species activity – Assessing the importance of quinones and atmospheric aging. Atmos. Environ. 2015, 120, 351359. 56. Janssen, N. A.; Hoek, G.; Simic-Lawson, M.; Fischer, P.; Van Bree, L.; Ten Brink, H.; Keuken, M.; Atkinson, R. W.; Anderson, H. R.; Brunekreef, B., Black carbon as an additional indicator of the adverse health effects of airborne particles compared with PM10 and PM2.5. Environ. Health Perspect. 2011, 119 (12), 1691-1699. 57. Charrier, J. G.; Anastasio, C., On dithiothreitol (DTT) as a measure of oxidative potential for ambient particles: evidence for the importance of soluble transition metals. Atmos. Chem. Phys. 2012, 12 (19), 9321-9333.


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452 453 454 455 456 457 458 459 460 461 462 463 464 465 466 467 468 469 470 471 472


58. Doroshow, J. H., Role of hydrogen peroxide and hydroxyl radical formation in the killing of Ehrlich tumor cells by anticancer quinones. Proc. Natl. Acad. Sci. U. S. A. 1986, 83 (12), 4514-4518. 59. Stanton, C. A.; Chow, F. L.; Phillips, D. H.; Grover, P. L.; Garner, R. C.; Martin, C. N., Evidence for N-(deoxyguanosin-8-yl)-1-aminopyrene as a major DNA adduct in female rats treated with 1-nitropyrene. Carcinogenesis 1985, 6 (4), 535-538. 60. Busby, J. W. F.; Garner, R. C.; Chow, F. L.; Martin, C. N.; Stevens, E. K.; Newberne, P. M.; Wogan, G. N., 6-Nitrochrysene is a potent tumorigen in newborn mice. Carcinogenesis 1985, 6 (5), 801-803. 61. Atsumi, T.; Ishihara, M.; Kadoma, Y.; Tonosaki, K.; Fujisawa, S., Comparative radical production and cytotoxicity induced by camphorquinone and 9‐fluorenone against human pulp fibroblasts. J. Oral. Rehabil. 2004, 31 (12), 1155-1164. 62. Lin, T.-S.; Tiecher, B. A.; Sartorelli, A. C., 2-Methylanthraquinone derivatives as potential bioreductive alkylating agents. J. Med. Chem. 1980, 23 (11), 1237-1242. 63. Verma, V.; Rico-Martinez, R.; Kotra, N.; King, L.; Liu, J.; Snell, T. W.; Weber, R. J., Contribution of water-soluble and insoluble components and their hydrophobic/hydrophilic subfractions to the reactive oxygen species-generating potential of fine ambient aerosols. Environ. Sci. Technol. 2012, 46 (20), 11384-11392. 64. Verma, V.; Shafer, M. M.; Schauer, J. J.; Sioutas, C., Contribution of transition metals in the reactive oxygen species activity of PM emissions from retrofitted heavy-duty vehicles. Atmos. Environ. 2010, 44 (39), 5165-5173.

473


21


Dry season Wet season Ambient samples (Tuet et al., 2016) Chamber SOA (Tuet el al., 2017) BURN (Bates et al. 2015) BBOA (Verma et al. 2015)

1.4

ROS/RNS (per μg of PM)

Page 22 of 27

1.2 1.0 0.8 0.6 0.4 0.2 0.0 0.00

0.05

0.10

0.15 -1

474

0.20

-1

DTT activity (nmol min μg )

475

Figure 1. ROS/RNS production and DTT activities for biomass burning aerosol collected

476

from the Brazilian Amazon, ambient samples collected from around the greater Atlanta

477

area,16 and chamber SOA generated from a variety of biogenic (isoprene, α-pinene, β-

478

caryophyllene) and anthropogenic (pentadecane, m-xylene, naphthalene) precursors

479

under different formation conditions.35, 50 Biomass burning samples are colored based on

480

season (dry in red and wet in blue). All samples were analyzed following the methology

481

outlined in Fang et al.34 and Tuet et al.16 Biomass burning factors obtained from source

482

apportionment (BURN18 and BBOA19) and their respective DTT activities estimated using

483

multiple linear regression are shown as shaded regions for comparison. BURN was

484

derived from offline chemical analysis and chemical mass balance (CMB) model.18 BBOA


22

Page 23 of 27


485

was derived from high-resolution aerosol mass spectrometer (AMS) measurements and

486

positive matrix factorization (PMF) analysis.19

487


23

50 40

Page 24 of 27

Dry season Wet season

3

A ROS/RNS (per m of air)


30

R = 0.89**

20 10 0 0

1000

2000

3000

4000

-3

Levoglucosan (ng m ) 50 40

3

ROS/RNS (per m of air)

B

R = 0.90**

30 20 10 0 0

50

100

150

200

250

-3

Galactosan (ng m ) 50 40

3

ROS/RNS (per m of air)

C

30

R = 0.89**

20 10 0 0

488

50

100

150

200

250

300

350

-3

Mannosan (ng m )

489

Figure 2. Correlations between ROS/RNS levels and concentrations of three

490

monosaccharide anhydrides, i.e., levoglucosan (R=0.89**), galactosan (R=0.90**), and

491

mannosan (R=0.89**). Pearson’s correlation coefficients for dry and wet season


24

Page 25 of 27


492

separately were: Rdry=0.88** and Rwet=-0.07 for levoglucosan, Rdry=0.91** and Rwet=0.33

493

for galactosan, and Rdry=0.87** and Rwet=0.25 for mannosan. ** indicates significance of p

494

< 0.01.


25


ROS/RNS (per µg of PM)

20

Page 26 of 27

Amazon samples Laboratory prepared oxy- and nitro-PAHs

15

10

5

0 4 495

5

6

17

21

28

32

45

Sample ID

496

Figure 3. ROS/RNS estimated from four oxy- and nitro-PAHs (1-nitropyrene, 6-nitrochrysene, 9-

497

fluorenone, and 2-methylanthraquinone) (aqua bars) prepared in the laboratory and ROS/RNS

498

measured for the water-soluble hydrophobic fraction of biomass burning aerosol samples collected

499

from the Brazilian Amazon (pink bars). Estimations were obtained using dose-response

500

relationships for individual oxy- and nitro-PAHs (Fig. S7) and concentrations of oxy- and nitro-

501

PAHs assuming concentration addition as the mixture model. The water-soluble hydrophobic

502

fraction was obtained by passing the water-soluble extract through a C-18 column. The sample ID

503

is the numbering of collected filter samples. Samples 4, 5, 6, 17 and 21 were collected in dry season

504

and samples 28, 32 and 45 were collected in wet season.

505


26

Page 27 of 27

506


For Table of Contents Use Only

507

508


27

Chemical oxidative potential and cellular oxidative stress from open

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