Advanced search
Publication Cover
Critical Reviews in Toxicology Volume 53, 2023 - Issue 8
Submit an article Journal homepage
1,812
Views
0
CrossRef citations to date
0
Altmetric
Review Article

A review of pulmonary neutrophilia and insights into the key role of neutrophils in particle-induced pathogenesis in the lung from animal studies of lunar dusts and other poorly soluble dust particles

Chiu-wing Lama Biomedical Research and Environmental Sciences Division, NASA Johnson Space Center, Houston, TX, USA;b Biomedical & Environmental Research Department, KBR Toxicology & Environmental Chemistry, Houston, TX, USA;c Department of Pathology and Laboratory Medicine, University of Texas Medical School at Houston, Houston, TX, USACorrespondence[email protected] [email protected]
,
Vincent Castranovad Health Effects Laboratory Division, National Institute for Occupational Safety and Health, Morgantown, WV, USACorrespondence[email protected]
,
Kevin Driscolle Ernest Mario School of Pharmacy, Rutgers University, Piscataway, NJ, USA
,
David Warheitf Warheit Scientific LLC, Wilmington, DE, USA
,
Valerie Rydera Biomedical Research and Environmental Sciences Division, NASA Johnson Space Center, Houston, TX, USA
,
Ye Zhanga Biomedical Research and Environmental Sciences Division, NASA Johnson Space Center, Houston, TX, USA;g Utilization and Life Sciences Office, Kennedy Space Center, Merritt Island, FL, USA
,
Patti Zeidler-Erdelyd Health Effects Laboratory Division, National Institute for Occupational Safety and Health, Morgantown, WV, USA
,
Robert Hunterc Department of Pathology and Laboratory Medicine, University of Texas Medical School at Houston, Houston, TX, USA
,
Robert Scullya Biomedical Research and Environmental Sciences Division, NASA Johnson Space Center, Houston, TX, USA;b Biomedical & Environmental Research Department, KBR Toxicology & Environmental Chemistry, Houston, TX, USA
,
William Wallacea Biomedical Research and Environmental Sciences Division, NASA Johnson Space Center, Houston, TX, USA;b Biomedical & Environmental Research Department, KBR Toxicology & Environmental Chemistry, Houston, TX, USA
,
John Jamesa Biomedical Research and Environmental Sciences Division, NASA Johnson Space Center, Houston, TX, USA
,
Brian Cruciana Biomedical Research and Environmental Sciences Division, NASA Johnson Space Center, Houston, TX, USA
,
Mayra Nelmana Biomedical Research and Environmental Sciences Division, NASA Johnson Space Center, Houston, TX, USA;b Biomedical & Environmental Research Department, KBR Toxicology & Environmental Chemistry, Houston, TX, USA
,
Richard McCluskeyh FAA Civil Aerospace Medical Institute, Oklahoma City, OK, USA
,
Donald Gardneri Inhalation Toxicology Associates, Savannah, GA, USA
,
Roger Rennej Roger Renne ToxPath Consulting Inc., Sumner, WA, USA
&
Roger McClellank Toxicology and Human Health Risk Analysis, Albuquerque, NM, USA
 show all
Pages 441-479 | Received 09 Mar 2023, Accepted 27 Aug 2023, Published online: 18 Oct 2023

References

  • Albrecht C, Knaapen AM, Becker A, Höhr D, Haberzettl P, van Schooten FJ, Borm PJ, Schins RP. 2005. The crucial role of particle surface reactivity in respirable quartz-induced reactive oxygen/nitrogen species formation and APE/Ref-1 induction in rat lung. Respir Res. 6(1):129–137. doi: 10.1186/1465-9921-6-129.
  • Allen RC. 1977. Evaluation of serum opsonic capacity by quantitating the initial chemiluminescent response from phagocytizing polymorphonuclear leukocytes. Infect Immun. 15(3):828–833. doi: 10.1128/iai.15.3.828-833.1977.
  • Alon R, Sportiello M, Kozlovski S, Kumar A, Reilly EC, Zarbock A, Garbi N, Topham DJ. 2021. Leukocyte trafficking to the lungs and beyond: lessons from influenza for COVID-19. Nat Rev Immunol. 21(1):49–64. doi: 10.1038/s41577-020-00470-2.
  • Amdur MO, Chen LC. 1989. Furnace-generated acid aerosols: speciation and pulmonary effects. Environ Health Perspect. 79:147–150. doi: 10.1289/ehp.8979147.
  • Antonini JM, Van Dyke K, Ye Z, DiMatteo M, Reasor MJ. 1994. Introduction of luminol-dependent chemiluminescence as a method to study silica inflammation in the tissue and phagocytic cells of rat lung. Environ Health Perspect. 102(Suppl. 10):37–42. doi: 10.1289/ehp.94102s1037.
  • Arandjelovic S, Ravichandran KS. 2015. Phagocytosis of apoptotic cells in homeostasis. Nat Immunol. 16(9):907–917. doi: 10.1038/ni.3253.
  • Aris RM, Christian D, Hearne PQ, Kerr K, Finkbeiner WE, Balmes JR. 1993. Ozone-induced airway inflammation in human subjects as determined by airway lavage and biopsy. Am Rev Respir Dis. 148(5):1363–1372. doi: 10.1164/ajrccm/148.5.1363.
  • Auten RL, Whorton MH, Mason NS. 2002. Blocking neutrophil influx reduces DNA damage in hyperoxia-exposed newborn rat lung. Am J Respir Cell Mol Biol. 26(4):391–397. doi: 10.1165/ajrcmb.26.4.4708.
  • Baggiolini M, Walz A, Kunkel SL. 1989. Neutrophil-activating peptide-1/interleukin 8, a novel cytokine that activates neutrophils. J Clin Invest. 84(4):1045–1049. doi: 10.1172/JCI114265.
  • Bello-Irizarry SN, Wang J, Olsen K, Gigliotti F, Wright TW. 2012. The alveolar epithelial cell chemokine response to pneumocystis requires adaptor molecule MyD88 and interleukin-1 receptor but not toll-like receptor 2 or 4. Infect Immun. 80(11):3912–3920. doi: 10.1128/IAI.00708-12.
  • Bermudez E, Mangum JB, Asgharian B, Wong BA, Reverdy EE, Janszen DB, Hext PM, Warheit DB, Everitt JI. 2002. Long-term pulmonary responses of three laboratory rodent species to subchronic inhalation of pigmentary titanium dioxide particles. Toxicol Sci. 70(1):86–97. doi: 10.1093/toxsci/70.1.86.
  • Bermudez E, Mangum JB, Wong BA, Asgharian B, Hext PM, Warheit DB, Everitt JI. 2004. Pulmonary responses of rats, mice, and hamsters to subchronic inhalation of ultrafine titanium dioxide particles. Toxicol Sci. 77(2):347–357. doi: 10.1093/toxsci/kfh019.
  • Bodas M, Vij N. 2010. The NF-kappaB signaling in cystic fibrosis lung disease: pathophysiology and therapeutic potential. Discov Med. 9(47):346–356.
  • Borm PJ, Driscoll KE. 2019. The hazards and risks of inhaled poorly soluble particles—where do we stand after 30 years of research? Part Fibre Toxicol. 16(1):11. doi: 10.1186/s12989-019-0294-4.
  • Borm PJ, Schins RP, Albrecht C. 2004. Inhaled particles and lung cancer, Part B: paradigms and risk assessment. Int J Cancer. 110(1):3–14. doi: 10.1002/ijc.20064.
  • Bosson J, Pourazar J, Forsberg B, Adelroth E, Sandström T, Blomberg A. 2007. Ozone enhances the airway inflammation initiated by diesel exhaust. Respir Med. 101(6):1140–1146. doi: 10.1016/j.rmed.2006.11.010.
  • Botto M, Lissandrini D, Sorio C, Walport MJ. 1992. Biosynthesis and secretion of complement component (C3) by activated human polymorphonuclear leukocytes. J Immunol. 149(4):1348–1355.
  • Boyle JJ. 2005. Macrophage activation in atherosclerosis: pathogenesis and pharmacology of plaque rupture. Curr Vasc Pharmacol. 3(1):63–68. doi: 10.2174/1570161052773861.
  • Brain JD. 1980. Macrophage damage in relation to the pathogenesis of lung diseases. Environ Health Perspect. 35:21–28. doi: 10.1289/ehp.803521.
  • Camous L, Roumenina L, Bigot S, Brachemi S, Frémeaux-Bacchi V, Lesavre P, Halbwachs-Mecarelli L. 2011. Complement alternative pathway acts as a positive feedback amplification of neutrophil activation. Blood. 117(4):1340–1349. doi: 10.1182/blood-2010-05-283564.
  • CARB. 2022. Overview: diesel exhaust & health. The California Air Resources Board; [assessed 2022 Dec]. https://ww2.arb.ca.gov/resources/overview-diesel-exhaust-and-health.
  • Carter JM, Driscoll KE. 2001. The role of inflammation, oxidative stress, and proliferation in silica-induced lung disease: a species comparison. J Environ Pathol Toxicol Oncol. 20(Suppl. 1):12. doi: 10.1615/JEnvironPatholToxicolOncol.v20.iSuppl.1.30.
  • Caston R, Luc K, Hendrix D, Hurowitz JA, Demple B. 2018. Assessing toxicity and nuclear and mitochondrial DNA damage caused by exposure of mammalian cells to lunar regolith simulants. Geohealth. 2(4):139–148. doi: 10.1002/2017GH000125.
  • Castranova V, Bowman L, Reasor MJ, Lewis T, Tucker J, Miles PR. 1985. The response of rat alveolar macrophages to chronic inhalation of coal dust and/or diesel exhaust. Environ Res. 36(2):405–419. doi: 10.1016/0013-9351(85)90034-9.
  • Castranova V, Jones T, Barger M, Afshari A, Frazer DG. 1990. Pulmonary responses of guinea pigs to consecutive exposures to cotton dust. In: Jacobs R, Wakelyn P, Domelsmith L, editors. Proceedings of the 14th Cotton Dust Research Conference; Jan 10–13; Las Vegas (NV): National Cotton Council; p. 131–135.
  • Castranova V, Porter D, Millecchia L, Ma JY, Hubbs AF, Teass A. 2002. Effect of inhaled crystalline silica in a rat model: time course of pulmonary reactions. Mol Cell Biochem. 234–235 (1–2):177–184.
  • Castranova V, Rabovsky J, Tucker JH, Miles PR. 1988. The alveolar type II epithelial cell: a multifunctional pneumocyte. Toxicol Appl Pharmacol. 93(3):472–483. doi: 10.1016/0041-008x(88)90051-8.
  • Castranova V. 1998. Particles and the airways: basic biological mechanisms of pulmonary pathogenicity. Appl Occup Environ Hyg. 13(8):613–616. doi: 10.1080/1047322X.1998.10390122.
  • Chang YS, Kim YJ, Yoo HS, Sung DK, Kim SY, Kang S, Park WS. 2009. Alpha-phenyl-N-tert-butylnitrone attenuates hyperoxia-induced lung injury by down-modulating inflammation in neonatal rats. Exp Lung Res. 35(3):234–249. doi: 10.1080/01902140802573007.
  • Chong S, Lee KS, Chung MJ, Han J, Kwon OJ, Kim TS. 2006. Pneumoconiosis: comparison of imaging and pathologic findings. Radiographics. 26(1):59–77. doi: 10.1148/rg.261055070.
  • Creutzenberg O, Bellmann B, Muhle H, Dasenbrock C, Morrow P, Mermelstein R. 1998. Lung clearance and retention of toner, TiO2, and crystalline silica, utilizing a tracer technique during chronic inhalation exposure in Syrian golden hamsters. Inhal Toxicol. 10:731–751.
  • Crucian B, Quiriarte H, Nelman M, Lam C-W, James JT, Sams C. 2014. Pulmonary and systemic immune response to chronic lunar dust inhalation. NASA Technical Report Server. [accessed 2019 May]. http://ntrs.nasa.gov/search.jsp?R=20140013073.
  • Dockery DW, Pope CA, Xu X, Spengler JD, Ware JH, Fay ME, Ferris BG, Speizer FE. 1993. An association between air pollution and mortality in six US cities. N Engl J Med. 329(24):1753–1759. doi: 10.1056/NEJM199312093292401.
  • Domínguez-Rodríguez A, Báez-Ferrer N, Abreu-González P, Rodríguez S, Díaz R, Avanzas P, Hernández-Vaquero D. 2021. Impact of desert dust events on the cardiovascular disease: a systematic review and meta-analysis. J Clin Med. 10(4):727. doi: 10.3390/jcm10040727.
  • Donaldson K, Beswick PH, Gilmour PS. 1996. Free radical activity associated with the surface of particles: a unifying factor in determining biological activity? Toxicol Lett. 88(1–3):293–298. doi: 10.1016/0378-4274(96)03752-6.
  • Driscoll KE, Borm PJA. 2020. Expert workshop on the hazards and risks of poorly soluble low toxicity particles. Inhal Toxicol. 32(2):53–62. doi: 10.1080/08958378.2020.1735581.
  • Driscoll KE, Carter JM, Hassenbein DG, Howard B. 1997. Cytokines and particle-induced inflammatory cell recruitment. Environ Health Perspect. 105(Suppl. 5):1159–1164. doi: 10.1289/ehp.97105s51159.
  • Driscoll KE, Deyo LC, Carter JM, Howard BW, Hassenbein DG, Bertram TA. 1997. Effects of particle exposure and particle-elicited inflammatory cells on mutation in rat alveolar epithelial cells. Carcinogenesis. 18(2):423–430. doi: 10.1093/carcin/18.2.423.
  • Driscoll KE, Howard BW, Carter JM, Asquith T, Johnston C, Detilleux P, Kunkel SL, Isfort RJ. 1996. Alpha-quartz-induced chemokine expression by rat lung epithelial cells: effects of in vivo and in vitro particle exposure. Am J Pathol. 149(5):1627–1637.
  • Driscoll KE. 1996. The role of inflammation in the development of rat lung tumors in response to chronic particle exposure. Inhal Toxicol. 8:139–153.
  • Driscoll KE. 2022. Review of lung particle overload, rat lung cancer, and the conclusions of the Edinburgh Expert Panel—it’s time to revisit cancer hazard classifications for titanium dioxide and carbon black. Front Public Health. 10:907318. doi: 10.3389/fpubh.2022.907318.
  • Egger G, Spendel S, Porta S. 1988. Characteristics of ingress and life span of neutrophils at a site of acute inflammation, determined with the Sephadex model in rats. Exp Pathol. 35(4):209–218. doi: 10.1016/s0232-1513(88)80090-2.
  • Eidelman O, Srivastava M, Zhang J, Leighton X, Murtie J, Jozwik C, Jacobson K, Weinstein DL, Metcalf EL, Pollard HB. 2001. Control of the proinflammatory state in cystic fibrosis lung epithelial cells by genes from the TNF-alphaR/NFkappaB pathway. Mol Med. 7(8):523–534. doi: 10.1007/BF03401858.
  • Elder A, Gelein R, Finkelstein JN, Driscoll KE, Harkema J, Oberdörster G. 2005. Effects of subchronically inhaled carbon black in three species. I. Retention kinetics, lung inflammation, and histopathology. Toxicol Sci. 88(2):614–629. doi: 10.1093/toxsci/kfi327.
  • EPA. 2021. New approach methods work plan. Washington (DC): Office of Chemical Safety and Pollution Prevention, Office of Research and Development, U.S. Environmental Protection Agency. https://www.epa.gov/system/files/documents/2021-11/nams-work-plan_11_15_21_508-tagged.pdf.
  • Ezekowitz RA, Sim RB, MacPherson GG, Gordon S. 1985. Interaction of human monocytes, macrophages, and polymorphonuclear leukocytes with zymosan in vitro. Role of type 3 complement receptors and macrophage-derived complement. J Clin Invest. 76(6):2368–2376. doi: 10.1172/JCI112249.
  • Ferrante A. 1992. Activation of neutrophils by interleukins-1 and -2 and tumor necrosis factors. Immunol Ser. 57:417–436.
  • Finkelstein JN, Johnston C, Barrett T, Oberdörster G. 1997. Particulate–cell interactions and pulmonary cytokine expression. Environ Health Perspect. 105(Suppl. 5):1179–1182. doi: 10.1289/ehp.97105s51179.
  • Fritsch P, Masse R. 1992. Overview of pulmonary alveolar macrophage renewal in normal rats and during different pathological processes. Environ Health Perspect. 97:59–67. doi: 10.1289/ehp.929759.
  • Fubini B, Bolis V, Giamello E, Pugliese L, Volante M. 1989. The formation of oxygen reactive radicals at the surface of the crushed quartz dusts as a possible cause of silica pathogenicity. In: Mossman BT, Bégin RO, editors. Effects of mineral dusts on cells. NATO ASI series. Vol. 30. Berlin, Heidelberg: Springer; p. 205–214.
  • Fubini B, Bolis V, Giamello E. 1987. The surface chemistry of crushed quartz dust in relation to its pathogenesis. Inorg Chim Acta. 138(3):193–197. doi: 10.1016/S0020-1693(00)81222-0.
  • Fubini B, Giamello E, Volante M, Bolis V. 1990. Chemical functionalities at the silica surface determining its reactivity when inhaled. Formation and reactivity of surface radicals. Toxicol Ind Health. 6(6):571–598.
  • Fubini B, Hubbard A. 2003. Reactive oxygen species (ROS) and reactive nitrogen species (RNS) generation by silica in inflammation and fibrosis. Free Radic Biol Med. 34(12):1507–1516. doi: 10.1016/s0891-5849(03)00149-7.
  • Fubini B, Mollo L, Giamello E. 1995. Free radical generation at the solid/liquid interface in iron containing minerals. Free Radic Res. 23(6):593–614. doi: 10.3109/10715769509065280.
  • Fubini B. 1998. Surface chemistry and quartz hazard. Ann Occup Hyg. 42(8):521–530. doi: 10.1016/s0003-4878(98)00066-0.
  • Ghio AJ, Kim C, Devlin RB. 2000. Concentrated ambient air particles induce mild pulmonary inflammation in healthy human volunteers. Am J Respir Crit Care Med. 162(3 Pt 1):981–988. doi: 10.1164/ajrccm.162.3.9911115.
  • Giannadaki D, Pozzer A, Lelieveld J. 2014. Modeled global effects of airborne desert dust on air quality and premature mortality. Atmos Chem Phys. 14(2):957–968. doi: 10.5194/acp-14-957-2014.
  • Gupta-Wright A, Tembo D, Jambo KC, Chimbayo E, Mvaya L, Caldwell S, Russell DG, Mwandumba HC. 2017. Functional analysis of phagocyte activity in whole blood from HIV/tuberculosis-infected individuals using a novel flow cytometry-based assay. Front Immunol. 8:1222. doi: 10.3389/fimmu.2017.01222.
  • Hamilton RF Jr, Thakur SA, Holian A. 2008. Silica binding and toxicity in alveolar macrophages. Free Radic Biol Med. 44(7):1246–1258. doi: 10.1016/j.freeradbiomed.2007.12.027.
  • Harrington AD, McCubbin FM, Kaur J, Smirnov A, Galdanes K, Schoonen MAA, Chen LC, Tsirka SE, Gordon T. 2017. Pulmonary inflammatory responses to acute meteorite dust exposures—implications for human space exploration. Lunar Planet Sci. XLVIII:2922.
  • Harrington AD, Schmidt MP, Szema AM, Galdanes K, Tsirka SE, Gordon T, Schoonen MAA. 2017. The role of Iraqi dust in inducing lung injury in United States soldiers—an interdisciplinary study: Iraqi dust and U.S. soldiers’ lung injury. Geohealth. 1(5):237–246. doi: 10.1002/2017GH000071.
  • Haslam PL, Turton CW, Heard B, Lukoszek A, Collins JV, Salsbury AJ, Turner-Warwick M. 1980. Bronchoalveolar lavage in pulmonary fibrosis: comparison of cells obtained with lung biopsy and clinical features. Thorax. 35(1):9–18. doi: 10.1136/thx.35.1.9.
  • Hector A, Griese M, Hartl D. 2014. Oxidative stress in cystic fibrosis lung disease: an early event, but worth targeting? Eur Respir J. 44(1):17–19. doi: 10.1183/09031936.00038114.
  • Heinrich U, Fuhst R, Rittinghausen S, Creutzenberg O, Bellmann B, Koch W, Levsen K. 1995. Chronic inhalation exposure of Wistar rats and two different strains of mice to diesel engine exhaust, carbon black, and titanium dioxide. Inhal Toxicol. 7(4):533–556. doi: 10.3109/08958379509015211.
  • Helleday R, Sandström T, Stjernberg N. 1994. Differences in bronchoalveolar cell response to nitrogen dioxide exposure between smokers and nonsmokers. Eur Respir J. 7(7):1213–1220. doi: 10.1183/09031936.94.07071213.
  • Herrero-Cervera A, Soehnlein O, Kenne E. 2022. Neutrophils in chronic inflammatory diseases. Cell Mol Immunol. 19(2):177–191. doi: 10.1038/s41423-021-00832-3.
  • Hetland RB, Schwarze PE, Johansen BV, Myran T, Uthus N, Refsnes M. 2001. Silica-induced cytokine release from A549 cells: importance of surface area versus size. Hum Exp Toxicol. 20(1):46–55. doi: 10.1191/096032701676225130.
  • Hext PM. 1994. Current perspectives on particulate induced pulmonary tumours. Hum Exp Toxicol. 13(10):700–715. doi: 10.1177/096032719401301009.
  • Hill HR, Hogan NA, Bale JF, Hemming VG. 1977. Evaluation of nonspecific (alternative pathway) opsonic activity by neutrophil chemiluminescence. Int Arch Allergy Appl Immunol. 53(6):490–497. doi: 10.1159/000231790.
  • [IARC] International Agency for Research on Cancer. 1989. Diesel and gasoline engine exhausts and some nitroarenes. IARC monographs on the evaluation of carcinogenic risks to humans. Vol. 46. Lyon; Lyon, France: International Agency for Research on Cancer; World Health Organization.
  • [IARC] International Agency for Research on Cancer. 2013. IARC: outdoor air pollution a leading environmental cause of cancer deaths. Press release (17 October 2013); [accessed 2019 May]. Lyon, France: International Agency for Research on Cancer, World Health Organization. https://www.iarc.fr/wp-content/uploads/2018/07/pr221_E.pdf.
  • Iba T, Hashiguchi N, Nagaoka I, Tabe Y, Murai M. 2013. Neutrophil cell death in response to infection and its relation to coagulation. J Intensive Care. 1(1):13. doi: 10.1186/2052-0492-1-13.
  • Jacquot J, Tabary O, Le Rouzic P, Clement A. 2008. Airway epithelial cell inflammatory signalling in cystic fibrosis. Int J Biochem Cell Biol. 40(9):1703–1715. doi: 10.1016/j.biocel.2008.02.002.
  • Jeon NL, Baskaran H, Dertinger SK, Whitesides GM, Van de Water L, Toner M. 2002. Neutrophil chemotaxis in linear and complex gradients of interleukin-8 formed in a microfabricated device. Nat Biotechnol. 20(8):826–830. doi: 10.1038/nbt712.
  • Johnston CJ, Driscoll KE, Finkelstein JN, Baggs R, O'Reilly MA, Carter J, Gelein R, Oberdörster G. 2000. Pulmonary chemokine and mutagenic responses in rats after subchronic inhalation of amorphous and crystalline silica. Toxicol Sci. 56(2):405–413. doi: 10.1093/toxsci/56.2.405.
  • Khan TZ, Wagener JS, Bost T, Martinez J, Accurso FJ, Riches DW. 1995. Early pulmonary inflammation in infants with cystic fibrosis. Am J Respir Crit Care Med. 151(4):1075–1082. doi: 10.1164/ajrccm/151.4.1075.
  • Knaapen AM, Seiler F, Schilderman PA, Nehls P, Bruch J, Schins RP, Borm PJ. 1999. Neutrophils cause oxidative DNA damage in alveolar epithelial cells. Free Radic Biol Med. 27(1–2):234–240. doi: 10.1016/s0891-5849(98)00285-8.
  • Knudsen E, Benestad HB, Seierstad T, Iversen PO. 2004. Macrophages in spleen and liver direct the migration pattern of rat neutrophils during inflammation. Eur J Haematol. 73(2):109–122. doi: 10.1111/j.1600-0609.2004.00263.x.
  • Kolling A, Ernst H, Rittinghausen S, Heinrich U. 2011. Relationship of pulmonary toxicity and carcinogenicity of fine and ultrafine granular dusts in a rat bioassay. Inhal Toxicol. 23(9):544–554. doi: 10.3109/08958378.2011.594458.
  • Koto H, Salmon M, Haddad el-B, Huang TJ, Zagorski J, Chung KF. 1997. Role of cytokine-induced neutrophil chemoattractant (CINC) in ozone-induced airway inflammation and hyperresponsiveness. Am J Respir Crit Care Med. 156(1):234–239. doi: 10.1164/ajrccm.156.1.9606095.
  • Krewski D, Burnett RT, Goldberg MS, Hoover BK, Siemiatycki J, Jerrett M, Abrahamowicz M, White WH. 2003. Overview of the reanalysis of the Harvard Six Cities Study and American Cancer Society Study of particulate air pollution and mortality. J Toxicol Environ Health A. 66(16–19):1507–1551. doi: 10.1080/15287390306424.
  • Laden F. 2019. A tale of six cities: the Landmark Harvard Six Cities Study. Environ Epidemiol. 3:221. doi: 10.1097/01.EE9.0000608272.94008.7b.
  • Lam C-W, Castranova V, Zeidler-Erdely PC, Renne R, Hunter R, McCluskey R, Scully RR, Wallace WT, Zhang Y, Ryder VE, et al. 2022. Comparative pulmonary toxicities of lunar dusts and terrestrial dusts (TiO2 & SiO2) in rats and an assessment of the impact of particle-generated oxidants on the dusts’ toxicities. Inhal Toxicol. 34(3–4):51–67. doi: 10.1080/08958378.2022.2038736.
  • Lam C-w, Scully RR, Zhang Y, Renne RA, Hunter RL, McCluskey RA, Chen BT, Castranova V, Driscoll KE, Gardner DE, et al. 2013. Toxicity of lunar dust assessed in inhalation-exposed rats. Inhal Toxicol. 25(12):661–678. doi: 10.3109/08958378.2013.833660.
  • Lapp NL, Castranova V. 1993. How silicosis and coal workers’ pneumoconiosis develop—a cellular assessment. Occup Med. 8(1):35–56.
  • Laskin DL, Malaviya R, Laskin JD. 2019. Role of macrophages in acute lung injury and chronic fibrosis induced by pulmonary toxicants. Toxicol Sci. 168(2):287–301. doi: 10.1093/toxsci/kfy309.
  • Laskin DL, Sunil VR, Gardner CR, Laskin JD. 2011. Macrophages and tissue injury: agents of defense or destruction? Annu Rev Pharmacol Toxicol. 51(1):267–288. doi: 10.1146/annurev.pharmtox.010909.105812.
  • Last JA, Sun WM, Witschi H. 1994. Ozone, NO, and NO2: oxidant air pollutants and more. Environ Health Perspect. 102(10):179–184.
  • Le Jeune I, Gribbin J, West J, Smith C, Cullinan P, Hubbard R. 2007. The incidence of cancer in patients with idiopathic pulmonary fibrosis and sarcoidosis in the UK. Respir Med. 101(12):2534–2540. doi: 10.1016/j.rmed.2007.07.012.
  • Lee KP, Trochimowicz HJ, Reinhardt CF. 1985. Pulmonary response of rats exposed to titanium dioxide (TiO2) by inhalation for two years. Toxicol Appl Pharmacol. 79(2):179–192. doi: 10.1016/0041-008x(85)90339-4.
  • Liu CY, Liu YH, Lin SM, Yu CT, Wang CH, Lin HC, Lin CH, Kuo HP. 2003. Apoptotic neutrophils undergoing secondary necrosis induce human lung epithelial cell detachment. J Biomed Sci. 10(6):746–756. doi: 10.1007/BF02256327.
  • Liu J, Pang Z, Wang G, Guan X, Fang K, Wang Z, Wang F. 2017. Advanced role of neutrophils in common respiratory diseases. J Immunol Res. 2017:6710278. doi: 10.1155/2017/6710278.
  • Lorant DE, Albertine K, Bohnsack JF. 1999. Chronic lung disease of early infancy: role of neutrophils. In Bland RD, Coalson J, editors. Chronic lung disease in early infancy, lung biology in health and disease. New York: Marcel Dekker; p. 793–812.
  • Makni-Maalej K, Chiandotto M, Hurtado-Nedelec M, Bedouhene S, Gougerot-Pocidalo MA, Dang PM, El-Benna J. 2013. Zymosan induces NADPH oxidase activation in human neutrophils by inducing the phosphorylation of p47phox and the activation of Rac2: involvement of protein tyrosine kinases. Biochem Pharmacol. 85(1):92–100. doi: 10.1016/j.bcp.2012.10.010.
  • Mauderly JL, Jones RK, Griffith WC, Henderson RF, McClellan RO. 1987. Diesel exhaust is a pulmonary carcinogen in rats exposed chronically by inhalation. Fundam Appl Toxicol. 9(2):208–221. doi: 10.1093/toxsci/9.2.208.
  • Mauderly JL, Snipes MB, Barr EB, Belinsky SA, Bond JA, Brooks AL, Chang IY, Cheng YS, Gillett NA, Griffith WC, et al. 1994. Pulmonary toxicity of inhaled diesel exhaust and carbon black in chronically exposed rats. Part I: neoplastic and nonneoplastic lung lesions. Res Rep Health Eff Inst. 68(Pt 1):1–97.
  • Mauderly JL. 1997. Relevance of particle-induced rat lung tumors for assessing lung carcinogenic hazard and human lung cancer risk. Environ Health Perspect. 105(Suppl. 5):1337–1346. doi: 10.1289/ehp.97105s51337.
  • McKay DS, Cooper BL, Taylor LA, James JT, Thomas-Keprta K, Pieters CM, Wentworth SJ, Wallace WT, Lee TS. 2015. Properties of potentially toxic, respirable-size lunar dust. Acta Astronaut. 107:163–176. doi: 10.1016/j.actaastro.2014.10.032.
  • Michaudel C, Mackowiak C, Maillet I, Fauconnier L, Akdis CA, Sokolowska M, Dreher A, Tan HT, Quesniaux VF, Ryffel B, et al. 2018. Ozone exposure induces respiratory barrier biphasic injury and inflammation controlled by IL-33. J Allergy Clin Immunol. 142(3):942–958. doi: 10.1016/j.jaci.2017.11.044.
  • Miedel EL, Hankenson FC. 2015. Biology and diseases of hamsters. Lab Anim Med. Published online 2015 Jul 10:209–245. doi: 10.1016/B978-0-12-409527-4.00005-5.
  • Mitsuhashi H, Hata J, Asano S, Kishimoto T. 1999. Appearance of cytokine-induced neutrophil chemoattractant isoforms and immunolocalization of them in lipopolysaccharide-induced acute lung inflammation in rats. Inflamm Res. 48(11):588–593. doi: 10.1007/s000110050508.
  • Monteiller C, Tran L, MacNee W, Faux S, Jones A, Miller B, Donaldson K. 2007. The pro-inflammatory effects of low-toxicity low-solubility particles, nanoparticles and fine particles, on epithelial cells in vitro: the role of surface area. Occup Environ Med. 64(9):609–615. doi: 10.1136/oem.2005.024802.
  • Morrow PE, Haseman JK, Hobbs CH, Driscoll KE, Vu V, Oberdörster G. 1996. The maximum tolerated dose for inhalation bioassays: toxicity vs overload. Fundam Appl Toxicol. 29(2):155–167. doi: 10.1093/toxsci/29.2.155.
  • Morrow PE. 1988. Possible mechanisms to explain dust overloading of the lungs. Fundam Appl Toxicol. 10(3):369–384. doi: 10.1016/0272-0590(88)90284-9.
  • Mossman BT, Borm PJ, Castranova V, Costa DL, Donaldson K, Kleeberger SR. 2007. Mechanisms of action of inhaled fibers, particles and nanoparticles in lung and cardiovascular diseases. Part Fibre Toxicol. 4(1):4–14. doi: 10.1186/1743-8977-4-4.
  • Muhle H, Takenaka S, Mohr U, Dasenbrock C, Mermelstein R. 1989. Lung tumor induction upon long-term low-level inhalation of crystalline silica. Am J Ind Med. 15(3):343–346. doi: 10.1002/ajim.4700150309.
  • Murphy J, Summer R, Wilson AA, Kotton DN, Fine A. 2008. The prolonged life-span of alveolar macrophages. Am J Respir Cell Mol Biol. 38(4):380–385. doi: 10.1165/rcmb.2007-0224RC.
  • Nightingale JA, Maggs R, Cullinan P, Donnelly LE, Rogers DF, Kinnersley R, Chung KF, Barnes PJ, Ashmore M, Newman-Taylor A. 2000. Airway inflammation after controlled exposure to diesel exhaust particulates. Am J Respir Crit Care Med. 162(1):161–166. doi: 10.1164/ajrccm.162.1.9908092.
  • Nordenhäll C, Pourazar J, Blomberg A, Levin JO, Sandström T, Adelroth E. 2000. Airway inflammation following exposure to diesel exhaust: a study of time kinetics using induced sputum. Eur Respir J. 15(6):1046–1051. doi: 10.1034/j.1399-3003.2000.01512.x.
  • [NTP] National Toxicology Program. 1993. Toxicology and carcinogenesis studies of talc (CAS No. 14807-96-6) (non-asbestiform) in F344/N rats and B6C3F1 mice (inhalation studies). National Toxicology Program Tech. Rept. No. 507. Bethesda (MD): National Institutes of Health.
  • [NTP] National Toxicology Program. 2000. 13th report on carcinogens. USA: National Toxicology Program, U.S. Department of Health and Human Services; [accessed 2019 May]. https://ntp.niehs.nih.gov/ntp/roc/content/profiles/dieselexhaustparticulates.pdf.
  • Oberdörster G, Ferin J, Gelein R, Soderholm SC, Finkelstein J. 1992. Role of the alveolar macrophage in lung injury: studies with ultrafine particles. Environ Health Perspect. 97:193–199. doi: 10.2307/3431353.
  • Oberdörster G, Oberdörster E, Oberdörster J. 2005. Nanotoxicology: an emerging discipline evolving from studies of ultrafine particles. Environ Health Perspect. 113(7):823–839. doi: 10.1289/ehp.7339.
  • Pohlen M, Carroll D, Prisk GK, Sawyer AJ. 2022. Overview of lunar dust toxicity risk. NPJ Microgravity. 8(1):55. doi: 10.1038/s41526-022-00244-1.
  • Pope CA 3rd, Burnett RT, Thun MJ, Calle EE, Krewski D, Ito K, Thurston GD. 2002. Lung cancer, cardiopulmonary mortality, and long-term exposure to fine particulate air pollution. JAMA. 287(9):1132–1141.
  • Porter DW, Hubbs AF, Mercer R, Robinson VA, Ramsey D, McLaurin J, Khan A, Battelli L, Brumbaugh K, Teass A, et al. 2004. Progression of lung inflammation and damage in rats after cessation of silica inhalation. Toxicol Sci. 79(2):370–380. doi: 10.1093/toxsci/kfh110.
  • Porter DW, Millecchia L, Robinson VA, Hubbs A, Willard P, Pack D, Ramsey D, McLaurin J, Khan A, Landsittel D, et al. 2002. Enhanced nitric oxide and reactive oxygen species production and damage after inhalation of silica. Am J Physiol Lung Cell Mol Physiol. 283(2):L485–L493. doi: 10.1152/ajplung.00427.2001.
  • Quint JK, Wedzicha JA. 2007. The neutrophil in chronic obstructive pulmonary disease. J Allergy Clin Immunol. 119(5):1065–1071. doi: 10.1016/j.jaci.2006.12.640.
  • Riley PA. 1994. Free radicals in biology: oxidative stress and the effects of ionizing radiation. Int J Radiat Biol. 65(1):27–33. doi: 10.1080/09553009414550041.
  • Roberts JR, Mercer RR, Chapman RS, Cohen GM, Bangsaruntip S, Schwegler-Berry D, Scabilloni JF, Castranova V, Antonini JM, Leonard SS. 2012. Pulmonary toxicity, distribution, and clearance of intratracheally instilled silicon nanowires in rats. J Nanomater. 2012:398302–398317. doi: 10.1155/2012/398302.
  • Roberts JR, Young SH, Castranova V, Antonini JM. 2007. Soluble metals in residual oil fly ash alter innate and adaptive pulmonary immune responses to bacterial infection in rats. Toxicol Appl Pharmacol. 221(3):306–319. doi: 10.1016/j.taap.2007.03.022.
  • Robinson JP. 1998. Oxygen and nitrogen reactive metabolites and phagocytic cells. In: Robinson JP, Babcock GF, editors. Phagocyte function: a guide for research and clinical evaluation. New York (NY): Wiley-Liss; p. 217–252.
  • Rosenthal GJ, Germolec DR, Blazka ME, Corsini E, Simeonova P, Pollock P, Kong LY, Kwon J, Luster MI. 1994. Asbestos stimulates IL-8 production from human lung epithelial cells. J Immunol. 153(7):3237–3244.
  • Ross GD, Thompson RA, Walport MJ, Springer TA, Watson JV, Ward RH, Lida J, Newman SL, Harrison RA, Lachmann PJ. 1985. Characterization of patients with an increased susceptibility to bacterial infections and a genetic deficiency of leukocyte membrane complement receptor type 3 and the related membrane antigen LFA-1. Blood. 66(4):882–890. doi: 10.1182/blood.V66.4.882.882.
  • Rousset-Jablonski C, Dalon F, Reynaud Q, Lemonnier L, Dehillotte C, Jacoud F, Berard M, Viprey M, Van Ganse E, Durieu I, et al. 2022. Cancer incidence and prevalence in cystic fibrosis patients with and without a lung transplant in France. Front Public Health. 10:1043691. doi: 10.3389/fpubh.2022.1043691.
  • Rudloff I, Cho SX, Bui CB, McLean C, Veldman A, Berger PJ, Nold MF, Nold-Petry CA. 2017. Refining anti-inflammatory therapy strategies for bronchopulmonary dysplasia. J Cell Mol Med. 21(6):1128–1138. doi: 10.1111/jcmm.13044.
  • Rydell-Törmänen K, Uller L, Erjefält JS. 2006. Direct evidence of secondary necrosis of neutrophils during intense lung inflammation. Eur Respir J. 28(2):268–274.
  • Saffiotti U. 1992. Lung cancer induction by crystalline silica. In: d’Amato R, Slaga TG, Farland W, Henry C, editors. Relevance of animal studies to the evaluation of human cancer risk. New York (NY): Wiley-Liss, Inc.; p. 51–59.
  • Salvi SS, Nordenhall C, Blomberg A, Rudell B, Pourazar J, Kelly FJ, Wilson S, Sandström T, Holgate ST, Frew AJ. 2000. Acute exposure to diesel exhaust increases IL-8 and GRO-alpha production in healthy human airways. Am J Respir Crit Care Med. 161(2 Pt 1):550–557. doi: 10.1164/ajrccm.161.2.9905052.
  • Saran M, Summer KH. 1999. Assaying for hydroxyl radicals: hydroxylated terephthalate is a superior fluorescence marker than hydroxylated benzoate. Free Radic Res. 31(5):429–436. doi: 10.1080/10715769900300991.
  • Sayes CM, Reed KL, Warheit DB. 2007. Assessing toxicity of fine and nanoparticles: comparing in vitro measurements to in vivo pulmonary toxicity profiles. Toxicol Sci. 97(1):163–180. doi: 10.1093/toxsci/kfm018.
  • Scheel-Toellner D, Wang K, Craddock R, Webb PR, McGettrick HM, Assi LK, Parkes N, Clough LE, Gulbins E, Salmon M, et al. 2004. Reactive oxygen species limit neutrophil life span by activating death receptor signaling. Blood. 104(8):2557–2564. doi: 10.1182/blood-2004-01-0191.
  • Seagrave J, Mauderly JL, Seilkop SK. 2003. In vitro relative toxicity screening of combined particulate and semivolatile organic fractions of gasoline and diesel engine emissions. J Toxicol Environ Health A. 66(12):1113–1132. doi: 10.1080/15287390390213881.
  • Seaton A. 1983. Coal and the lung. Thorax. 38(4):241–243. doi: 10.1136/thx.38.4.241.
  • Seiler F, Rehn B, Rehn S, Bruchs J. 2001. Significant differences in the cellular and molecular reactions of rat and hamster lung after quartz exposure. Toxicol Lett. 119(1):11–19. doi: 10.1016/s0378-4274(00)00289-7.
  • Sellamuthu R, Umbright C, Roberts JR, Cumpston A, McKinney W, Chen BT, Frazer D, Li S, Kashon M, Joseph P. 2013. Molecular insights into the progression of crystalline silica-induced pulmonary toxicity in rats. J Appl Toxicol. 33(4):301–312. doi: 10.1002/jat.2733.
  • Selley L, Phillips DH, Mudway I. 2019. The potential of omics approaches to elucidate mechanisms of biodiesel-induced pulmonary toxicity. Part Fibre Toxicol. 16(1):4. doi: 10.1186/s12989-018-0284-y.
  • Silva MT, do Vale A, dos Santos NM. 2008. Secondary necrosis in multicellular animals: an outcome of apoptosis with pathogenic implications. Apoptosis. 13(4):463–482. doi: 10.1007/s10495-008-0187-8.
  • Smith D. 1962. Free radical in irradiated biology material and systems. Annu Rev Nucl Sci. 12(1):577–602. doi: 10.1146/annurev.ns.12.120162.003045.
  • Specktor B. 2018. Moon dust is super toxic to human cells; [accessed 2023 Jan]. Live Science; [accessed 2018 Mar 17]. https://www.livescience.com/62590-moon-dust-bad-lungs-brain.html.
  • Strzyz P. 2017. Cell death: pulling the apoptotic trigger for necrosis. Nat Rev Mol Cell Biol. 18(2):72–72. doi: 10.1038/nrm.2017.1.
  • Summers C, Rankin SM, Condliffe AM, Singh N, Peters AM, Chilvers ER. 2010. Neutrophil kinetics in health and disease. Trends Immunol. 31(8):318–324. doi: 10.1016/j.it.2010.05.006.
  • Turci F, Corazzari I, Alberto G, Martra G, Fubini B. 2015. Free-radical chemistry as a means to evaluate lunar dust health hazard in view of future missions to the moon. Astrobiology. 15(5):371–380. doi: 10.1089/ast.2014.1216.
  • Valderrama A, Zapata MI, Hernandez JC, Cardona-Arias JA. 2022. Systematic review of preclinical studies on the neutrophil-mediated immune response to air pollutants, 1980–2020. Heliyon. 8(1):e08778. doi: 10.1016/j.heliyon.2022.e08778.
  • Vallyathan V, Shi X. 1997. The role of oxygen free radicals in occupational and environmental lung diseases. Environ Health Perspect. 105(1):165–177.
  • Vallyathan V, Shi XL, Dalal NS, Irr W, Castranova V. 1988. Generation of free radicals from freshly fractured silica dust. Potential role in acute silica-induced lung injury. Am Rev Respir Dis. 138(5):1213–1219. doi: 10.1164/ajrccm/138.5.1213.
  • Vandette K. 2018. Moon dust is extremely toxic and poses health hazards for astronauts. Nature.Science.Life; [accessed 2023 Jan]. Earth.com; [accessed 2018 Dec 19]. https://www.earth.com/news/moon-dust-toxic-health/.
  • Wallace WT, Taylor LA, Liu Y, Cooper BL, McKay D, Chen B, Jeevarajan AS. 2009. Lunar dust and lunar simulant activation and monitoring. Meteorit Planet Sci. 44(7):961–970. doi: 10.1111/j.1945-5100.2009.tb00781.x.
  • Wardman P. 1989. Reduction potentials of one-electron couples involving free-radicals in aqueous-solution. J Phys Chem Ref Data. 18(4):1637–1755. doi: 10.1063/1.555843.
  • Watanabe K, Koizumi F, Kurashige Y, Tsurufuji S, Nakagawa H. 1991. Rat CINC, a member of the interleukin-8 family, is a neutrophil-specific chemoattractant in vivo. Exp Mol Pathol. 55(1):30–37. doi: 10.1016/0014-4800(91)90016-q.
  • [WHO] WHO Regional Office for Europe. 2012. Health effects of black carbon. Copenhagen: WHO Regional Office for Europe; [accessed 2022 Dec]. http://www.euro.who.int/__data/assets/pdf_file/0004/162535/e96541.pdf.
  • Wynn TA. 2011. Integrating mechanisms of pulmonary fibrosis. J Exp Med. 208(7):1339–1350. doi: 10.1084/jem.20110551.
  • Yanagisawa R, Takano H, Ichinose T, Mizushima K, Nishikawa M, Mori I, Inoue K-I, Sadakane K, Yoshikawa T. 2007. Gene expression analysis of murine lungs following pulmonary exposure to Asian sand dust particles. Exp Biol Med. 232(8):1109–1118. doi: 10.3181/0612-RM-311.
  • Yuen J, Pluthero FG, Douda DN, Riedl M, Cherry A, Ulanova M, Kahr WH, Palaniyar N, Licht C. 2016. NETosing neutrophils activate complement both on their own nets and bacteria via alternative and non-alternative pathways. Front Immunol. 7:137. doi: 10.3389/fimmu.2016.00137.
  • Zhang DD, Hartsky MA, Warheit DB. 2002. Time course of quartz and TiO2 particle-induced pulmonary inflammation and neutrophil apoptotic responses in rats. Exp Lung Res. 28(8):641–670.
  • Zhang Y, Story M, Yeshitla S, Wang X, Scully RR, Theriot C, Wu HL, Ryder VE, Lam CW. 2023. Persistent changes in expression of genes involved in inflammation and fibrosis in the lungs of rats exposed to airborne lunar dust. Inhal Toxicol. 35(5–6):139–156. doi: 10.1080/08958378.2023.2172485.

Related research

People also read lists articles that other readers of this article have read.

Recommended articles lists articles that we recommend and is powered by our AI driven recommendation engine.

Cited by lists all citing articles based on Crossref citations.
Articles with the Crossref icon will open in a new tab.