385
Views
1
CrossRef citations to date
0
Altmetric
Research Articles

Aging influence on pulmonary and systemic inflammation and neural metabolomics arising from pulmonary multi-walled carbon nanotube exposure in apolipoprotein E-deficient and C57BL/6 female mice

, , , , , ORCID Icon, , , , , & ORCID Icon show all
Pages 86-100 | Received 28 Sep 2021, Accepted 03 Jan 2022, Published online: 17 Jan 2022

References

  • Achariyar TM, Li B, Peng W, Verghese PB, Shi Y, McConnell E, Benraiss A, Kasper T, Song W, Takano T, et al. 2016. Glymphatic distribution of CSF-derived apoE into brain is isoform specific and suppressed during sleep deprivation. Mol Neurodegener. 11(1):74.
  • Andreau K, Leroux M, Bouharrour A. 2012. Health and cellular impacts of air pollutants: from cytoprotection to cytotoxicity. Biochem Res Int. 2012:493894.
  • Aragon M, Erdely A, Bishop L, Salmen R, Weaver J, Liu J, Hall P, Eye T, Kodali V, Zeidler-Erdely P, et al. 2016. MMP-9-dependent serum-borne bioactivity caused by multiwalled carbon nanotube exposure induces vascular dysfunction via the CD36 scavenger receptor. Toxicol Sci. 150(2):488–498.
  • Aragon MJ, Chrobak I, Brower J, Roldan L, Fredenburgh LE, McDonald JD, Campen MJ. 2016. Inflammatory and vasoactive effects of serum following inhalation of varied complex mixtures. Cardiovasc Toxicol. 16(2):163–171.
  • Aragon MJ, Topper L, Tyler CR, Sanchez B, Zychowski K, Young T, Herbert G, Hall P, Erdely A, Eye T, et al. 2017. Serum-borne bioactivity caused by pulmonary multiwalled carbon nanotubes induces neuroinflammation via blood-brain barrier impairment. Proc Natl Acad Sci USA. 114(10):E1968–E1976.
  • Balamayooran G, Batra S, Balamayooran T, Cai S, Jeyaseelan S. 2011. Monocyte chemoattractant protein 1 regulates pulmonary host defense via neutrophil recruitment during Escherichia coli infection. Infect Immun. 79(7):2567–2577.
  • Bektas A, Schurman SH, Sen R, Ferrucci L. 2018. Aging, inflammation and the environment. Exp Gerontol. 105:10–18. Epub 2017/12/25. PubMed PMID: 29275161; PMCID: PMC5909704.
  • Bratic A, Larsson NG. 2013. The role of mitochondria in aging. J Clin Invest. 123(3):951–957.
  • Brook RD, Rajagopalan S, Pope CA, 3rd, Brook JR, Bhatnagar A, Diez-Roux AV, Holguin F, Hong Y, Luepker RV, Mittleman MA, et al. 2010. Particulate matter air pollution and cardiovascular disease: an update to the scientific statement from the American Heart Association. Circulation. 121(21):2331–2378.
  • Byun J, Song B, Lee K, Kim B, Hwang HW, Ok MR, Jeon H, Lee K, Baek SK, Kim SH, et al. 2019. Identification of urban particulate matter-induced disruption of human respiratory mucosa integrity using whole transcriptome analysis and organ-on-a chip. J Biol Eng. 13:88.
  • Campen M, Robertson S, Lund A, Lucero J, McDonald J. 2014. Engine exhaust particulate and gas phase contributions to vascular toxicity. Inhal Toxicol. 26(6):353–360.
  • Cao Y, Jacobsen NR, Danielsen PH, Lenz AG, Stoeger T, Loft S, Wallin H, Roursgaard M, Mikkelsen L, Moller P. 2014. Vascular effects of multiwalled carbon nanotubes in dyslipidemic ApoE−/− mice and cultured endothelial cells. Toxicol Sci. 138(1):104–116.
  • Caraballo JC, Yshii C, Westphal W, Moninger T, Comellas AP. 2011. Ambient particulate matter affects occludin distribution and increases alveolar transepithelial electrical conductance. Respirology. 16(2):340–349.
  • Carroll PA, Diolaiti D, McFerrin L, Gu H, Djukovic D, Du J, Cheng PF, Anderson S, Ulrich M, Hurley JB, et al. 2015. Deregulated Myc requires MondoA/Mlx for metabolic reprogramming and tumorigenesis. Cancer Cell. 27(2):271–285.
  • Cung H, Aragon MJ, Zychowski K, Anderson JR, Nawarskas J, Roldan C, Sood A, Qualls C, Campen MJ. 2015. Characterization of a novel endothelial biosensor assay reveals increased cumulative serum inflammatory potential in stabilized coronary artery disease patients. J Transl Med. 13:99.
  • Devi G. 2018. Menopause-related cognitive impairment. Obstet Gynecol. 132(6):1325–1327.
  • Ding J, Ji J, Rabow Z, Shen T, Folz J, Brydges CR, Fan S, Lu X, Mehta S, Showalter MR, et al. 2021. A metabolome atlas of the aging mouse brain. Nat Commun. 12(1):6021.
  • Dockery DW, Pope CA, 3rd, Kanner RE, Martin Villegas G, Schwartz J. 1999. Daily changes in oxygen saturation and pulse rate associated with particulate air pollution and barometric pressure. Res Rep Health Eff Inst. 83:1–19.
  • Eghlimi R, Shi XJ, Hrovat J, Xi BW, Gu HW. 2020. Triple negative breast cancer detection using LC-MS/MS lipidomic profiling. J Proteome Res. 19(6):2367–2378.
  • Erdely A, Dahm M, Chen BT, Zeidler-Erdely PC, Fernback JE, Birch ME, Evans DE, Kashon ML, Deddens JA, Hulderman T, et al. 2013. Carbon nanotube dosimetry: from workplace exposure assessment to inhalation toxicology. Part Fibre Toxicol. 10(1):53.
  • Fang EF, Kassahun H, Croteau DL, Scheibye-Knudsen M, Marosi K, Lu H, Shamanna RA, Kalyanasundaram S, Bollineni RC, Wilson MA, et al. 2016. NAD + replenishment improves lifespan and healthspan in ataxia telangiectasia models via mitophagy and DNA repair. Cell Metab. 24(4):566–581.
  • Fraser K, Kodali V, Yanamala N, Birch ME, Cena L, Casuccio G, Bunker K, Lersch TL, Evans DE, Stefaniak A, et al. 2020. Physicochemical characterization and genotoxicity of the broad class of carbon nanotubes and nanofibers used or produced in U.S. facilities. Part Fibre Toxicol. 17(1):62.
  • Grande G, Ljungman PLS, Eneroth K, Bellander T, Rizzuto D. 2020. Association between cardiovascular disease and long-term exposure to air pollution with the risk of dementia. JAMA Neurol. 77(7):801–809.
  • Gu H, Carroll PA, Du J, Zhu J, Neto FC, Eisenman RN, Raftery D. 2016. Quantitative method to investigate the balance between metabolism and proteome biomass: starting from glycine. Angew Chem Int Ed Engl. 55(50):15646–15650.
  • Gu H, Zhang P, Zhu J, Raftery D. 2015. Globally optimized targeted mass spectrometry: reliable metabolomics analysis with broad coverage. Anal Chem. 87(24):12355–12362.
  • Han SG, Howatt D, Daugherty A, Gairola G. 2015. Pulmonary and atherogenic effects of multi-walled carbon nanotubes (MWCNT) in apolipoprotein-E-deficient mice. J Toxicol Environ Health A. 78(4):244–253.
  • He J, Zhu Z, Bundy JD, Dorans KS, Chen J, Hamm LL. 2021. Trends in cardiovascular risk factors in US adults by race and ethnicity and socioeconomic status, 1999-2018. JAMA. 326(13):1286–1298.
  • Henderson VW, Brinton RD. 2010. Menopause and mitochondria: windows into estrogen effects on Alzheimer’s disease risk and therapy. Prog Brain Res. 182:77–96.
  • Heneka MT, Carson MJ, El Khoury J, Landreth GE, Brosseron F, Feinstein DL, Jacobs AH, Wyss-Coray T, Vitorica J, Ransohoff RM, et al. 2015. Neuroinflammation in Alzheimer’s disease. Lancet Neurol. 14(4):388–405.
  • Hou Y, Lautrup S, Cordonnier S, Wang Y, Croteau DL, Zavala E, Zhang Y, Moritoh K, O’Connell JF, Baptiste BA, et al. 2018. NAD + supplementation normalizes key Alzheimer’s features and DNA damage responses in a new AD mouse model with introduced DNA repair deficiency. Proc Natl Acad Sci USA. 115(8):E1876–E1885.
  • Ivanisevic J, Stauch KL, Petrascheck M, Benton HP, Epstein AA, Fang M, Gorantla S, Tran M, Hoang L, Kurczy ME, et al. 2016. Metabolic drift in the aging brain. Aging. 8(5):1000–1020.
  • Jacobsen NR, Moller P, Jensen KA, Vogel U, Ladefoged O, Loft S, Wallin H. 2009. Lung inflammation and genotoxicity following pulmonary exposure to nanoparticles in ApoE-/- mice. Part Fibre Toxicol. 6:2.
  • Jasbi P, Mitchell NM, Shi XJ, Grys TE, Wei YP, Liu L, Lake DF, Gu HW. 2019. Coccidioidomycosis detection using targeted plasma and urine metabolic profiling. J Proteome Res. 18(7):2791–2802.
  • Jin L, Ghimire L, Paudel S, Cai S, Rangasamy T, Jeyaseelan S. 2018. MCP-1 plays a critical role in neutrophil function and pyroptosis during carbapenemf-resistant Klebsiella pneumoniae. J Immunol. 200(1):46.17.
  • Krouwer VJ, Hekking LH, Langelaar-Makkinje M, Regan-Klapisz E, Post JA. 2012. Endothelial cell senescence is associated with disrupted cell-cell junctions and increased monolayer permeability. Vasc Cell. 4(1):12.
  • Kulminski AM, Barochia AV, Loika Y, Raghavachari N, Arbeev KG, Wojczynski MK, Thyagarajan B, Vardarajan BN, Christensen K, Yashin AI, et al. 2018. The APOE ε4 allele is associated with a reduction in FEV1/FVC in women: a cross-sectional analysis of the long life family study. PLoS One. 13(11):e0206873.
  • Leng F, Edison P. 2021. Neuroinflammation and microglial activation in Alzheimer disease: where do we go from here? Nat Rev Neurol. 17(3):157–172.
  • Liu CC, Liu CC, Kanekiyo T, Xu H, Bu G. 2013. Apolipoprotein E and Alzheimer disease: risk, mechanisms and therapy. Nat Rev Neurol. 9(2):106–118.
  • Liu J, Chen X, Dou M, He H, Ju M, Ji S, Zhou J, Chen C, Zhang D, Miao C, et al. 2019. Particulate matter disrupts airway epithelial barrier via oxidative stress to promote Pseudomonas aeruginosa infection. J Thorac Dis. 11(6):2617–2627.
  • Lo Sasso G, Schlage WK, Boue S, Veljkovic E, Peitsch MC, Hoeng J. 2016. The Apoe(-/-) mouse model: a suitable model to study cardiovascular and respiratory diseases in the context of cigarette smoke exposure and harm reduction. J Transl Med. 14(1):146.
  • Long J, Ma W, Yu Z, Liu H, Cao Y. 2019. Multi-walled carbon nanotubes (MWCNTs) promoted lipid accumulation in THP-1 macrophages through modulation of endoplasmic reticulum (ER) stress. Nanotoxicology. 13(7):938.
  • Long J, Xiao Y, Liu L, Cao Y. 2017. The adverse vascular effects of multi-walled carbon nanotubes (MWCNTs) to human vein endothelial cells (HUVECs) in vitro: role of length of MWCNTs. J Nanobiotechnology. 15(1):80.
  • Meyer KC. 2001. The role of immunity in susceptibility to respiratory infection in the aging lung. Respir Physiol. 128(1):23–31.
  • Mostovenko E, Saunders S, Muldoon PP, Bishop L, Campen MJ, Erdely A, Ottens AK. 2021. Carbon nanotube exposure triggers a cerebral peptidomic response: barrier compromise, neuroinflammation, and a hyperexcited state. Toxicol Sci. 182(1):107–119.
  • Mostovenko E, Young T, Muldoon PP, Bishop L, Canal CG, Vucetic A, Zeidler-Erdely PC, Erdely A, Campen MJ, Ottens AK. 2019. Nanoparticle exposure driven circulating bioactive peptidome causes systemic inflammation and vascular dysfunction. Part Fibre Toxicol. 16(1):20.
  • Mulder M. 2009. Sterols in the central nervous system. Curr Opin Clin Nutr Metab Care. 12(2):152–158.
  • Mumaw CL, Levesque S, McGraw C, Robertson S, Lucas S, Stafflinger JE, Campen MJ, Hall P, Norenberg JP, Anderson T, et al. 2016. Microglial priming through the lung-brain axis: the role of air pollution-induced circulating factors. FASEB J. 30(5):1880–1891.
  • Nacarelli T, Lau L, Fukumoto T, Zundell J, Fatkhutdinov N, Wu S, Aird KM, Iwasaki O, Kossenkov AV, Schultz D, et al. 2019. NAD + metabolism governs the proinflammatory senescence-associated secretome. Nat Cell Biol. 21(3):397–407.
  • Nation DA, Sweeney MD, Montagne A, Sagare AP, D’Orazio LM, Pachicano M, Sepehrband F, Nelson AR, Buennagel DP, Harrington MG, et al. 2019. Blood-brain barrier breakdown is an early biomarker of human cognitive dysfunction. Nat Med. 25(2):270–276.
  • Poole JA, Romberger DJ, Wyatt TA, Staab E, VanDeGraaff J, Thiele GM, Dusad A, Klassen LW, Duryee MJ, Mikuls TR, et al. 2015. Age impacts pulmonary inflammation and systemic bone response to inhaled organic dust exposure. J Toxicol Environ Health A. 78(19):1201–1216.
  • Pope CA, 3rd, Burnett RT, Thurston GD, Thun MJ, Calle EE, Krewski D, Godleski JJ. 2004. Cardiovascular mortality and long-term exposure to particulate air pollution: epidemiological evidence of general pathophysiological pathways of disease. Circulation. 109(1):71–77.
  • Pope CA, 3rd, Ezzati M, Dockery DW. 2009. Fine-particulate air pollution and life expectancy in the United States. N Engl J Med. 360(4):376–386.
  • Porter DW, Hubbs AF, Chen BT, McKinney W, Mercer RR, Wolfarth MG, Battelli L, Wu N, Sriram K, Leonard S, et al. 2013. Acute pulmonary dose-responses to inhaled multi-walled carbon nanotubes. Nanotoxicology. 7(7):1179–1194.
  • Porter DW, Hubbs AF, Mercer RR, Wu N, Wolfarth MG, Sriram K, Leonard S, Battelli L, Schwegler-Berry D, Friend S, et al. 2010. Mouse pulmonary dose- and time course-responses induced by exposure to multi-walled carbon nanotubes. Toxicology. 269(2–3):136–147.
  • Sawant KV, Poluri KM, Dutta AK, Sepuru KM, Troshkina A, Garofalo RP, Rajarathnam K. 2016. Chemokine CXCL1 mediated neutrophil recruitment: role of glycosaminoglycan interactions. Sci Rep. 6(1):33123.
  • Schubauer-Berigan MK, Dahm MM, Erdely A, Beard JD, Eileen Birch M, Evans DE, Fernback JE, Mercer RR, Bertke SJ, Eye T, et al. 2018. Association of pulmonary, cardiovascular, and hematologic metrics with carbon nanotube and nanofiber exposure among U.S. workers: a cross-sectional study. Part Fibre Toxicol. 15(1):22.
  • Seynhaeve ALB, Vermeulen CE, Eggermont AMM, ten Hagen TLM. 2006. Cytokines and vascular permeability: an in vitro study on human endothelial cells in relation to tumor necrosis factor-alpha-primed peripheral blood mononuclear cells. CBB. 44(1):157–169.
  • Shi XJ, Wang S, Jasbi P, Turner C, Hrovat J, Wei YP, Liu JP, Gu HW. 2019. Database-assisted globally optimized targeted mass spectrometry (dGOT-MS): broad and reliable metabolomics analysis with enhanced identification. Anal Chem. 91(21):13737–13745.
  • Shvedova AA, Kisin E, Murray AR, Johnson VJ, Gorelik O, Arepalli S, Hubbs AF, Mercer RR, Keohavong P, Sussman N, et al. 2008. Inhalation vs. aspiration of single-walled carbon nanotubes in C57BL/6 mice: inflammation, fibrosis, oxidative stress, and mutagenesis. Am J Physiol Lung Cell Mol Physiol. 295(4):L552–L565.
  • Smith TR, Bhatnagar A. 2018. Enviromics: understanding aging. Aging. 11(1):9–10.
  • Sokolowska M, Quesniaux VFJ, Akdis CA, Chung KF, Ryffel B, Togbe D. 2019. Acute respiratory barrier disruption by ozone exposure in mice. Front Immunol. 10:2169.
  • Stapleton PA, Minarchick VC, Cumpston AM, McKinney W, Chen BT, Sager TM, Frazer DG, Mercer RR, Scabilloni J, Andrew ME, et al. 2012. Impairment of coronary arteriolar endothelium-dependent dilation after multi-walled carbon nanotube inhalation: a time-course study. Int J Mol Sci. 13(11):13781–13803.
  • Tyler CR, Noor S, Young TL, Rivero V, Sanchez B, Lucas S, Caldwell KK, Milligan ED, Campen MJ. 2018. Aging exacerbates neuroinflammatory outcomes induced by acute ozone exposure. Toxicol Sci. 163(1):123–139.
  • Tyler CR, Zychowski KE, Sanchez BN, Rivero V, Lucas S, Herbert G, Liu J, Irshad H, McDonald JD, Bleske BE, et al. 2016. Surface area-dependence of gas-particle interactions influences pulmonary and neuroinflammatory outcomes. Part Fibre Toxicol. 13(1):64.
  • Vega JN, Zurkovsky L, Albert K, Melo A, Boyd B, Dumas J, Woodward N, McDonald BC, Saykin AJ, Park JH, et al. 2016. Altered brain connectivity in early postmenopausal women with subjective cognitive impairment. Front Neurosci. 10:433.
  • Vesterdal LK, Folkmann JK, Jacobsen NR, Sheykhzade M, Wallin H, Loft S, Moller P. 2010. Pulmonary exposure to carbon black nanoparticles and vascular effects. Part Fibre Toxicol. 7:33.
  • Wagner KH, Cameron-Smith D, Wessner B, Franzke B. 2016. Biomarkers of aging: from function to molecular biology. Nutrients. 8(6):338.
  • Wang L, Green FH, Smiley-Jewell SM, Pinkerton KE. 2010. Susceptibility of the aging lung to environmental injury. Semin Respir Crit Care Med. 31(5):539–553.
  • World Health Organization. 2018. Fact sheet: Ambient (outdoor) air pollution Geneva (Switzerland): WHO.
  • Wyss-Coray T. 2016. Ageing, neurodegeneration and brain rejuvenation. Nature. 539(7628):180–186.
  • Yamashita CM, Fessler MB, Vasanthamohan L, Lac J, Madenspacher J, McCaig L, Yao L, Wang L, Puntorieri V, Mehta S, et al. 2014. Apolipoprotein E-deficient mice are susceptible to the development of acute lung injury. Respiration. 87(5):416–427.
  • Yao X, Gordon EM, Figueroa DM, Barochia AV, Levine SJ. 2016. Emerging roles of apolipoprotein E and apolipoprotein A-I in the pathogenesis and treatment of lung disease. Am J Respir Cell Mol Biol. 55(2):159–169.
  • Yin Y, Wang Z. 2018. ApoE and neurodegenerative diseases in aging. Adv Exp Med Biol. 1086:77–92.
  • Zhang SH, Reddick RL, Piedrahita JA, Maeda N. 1992. Spontaneous hypercholesterolemia and arterial lesions in mice lacking apolipoprotein E. Science. 258(5081):468–471.
  • Zhao N, Liu CC, Qiao W, Bu G. 2018. Apolipoprotein E, receptors, and modulation of Alzheimer’s disease. Biol Psychiatry. 83(4):347–357.
  • Zychowski KE, Sanchez B, Pedrosa RP, Lorenzi-Filho G, Drager LF, Polotsky VY, Campen MJ. 2016. Serum from obstructive sleep apnea patients induces inflammatory responses in coronary artery endothelial cells. Atherosclerosis. 254:59–66.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.