Pre-conceptional exposure to multiwalled carbon nanotubes suppresses antibody production in mouse offspring

References

• Barfod, K. K., K. Vrankx, H. C. Mirsepasi-Lauridsen, J. S. Hansen, K. S. Hougaard, S. T. Larsen, A. C. Ouwenhand, et al. 2015. “The Murine Lung Microbiome Changes During Lung Inflammation and Intranasal Vancomycin Treatment.” The Open Microbiology Journal 9 (1): 167–179. doi:10.2174/1874285801509010167.
   PubMedGoogle Scholar
• Blossom, S. J., S. B. Melnyk, M. Li, W. D. Wessinger, and C. A. Cooney. 2017. “Inflammatory and Oxidative Stress-Related Effects Associated with Neurotoxicity Are Maintained after Exclusively Prenatal Trichloroethylene Exposure.” Neurotoxicology 59: 164–174. doi:10.1016/j.neuro.2016.01.002.
   PubMed Web of Science ®Google Scholar
• Blumer, N., U. Herz, M. Wegmann, and H. Renz. 2005. “Prenatal Lipopolysaccharide-Exposure Prevents Allergic Sensitization and Airway Inflammation, but Not Airway Responsiveness in a Murine Model of Experimental Asthma.” Clinical and Experimental Allergy 35 (3): 397–402. doi:10.1111/j.1365-2222.2005.02184.x.
   PubMed Web of Science ®Google Scholar
• Blumer, N, et al. 2007. “Perinatal Maternal Application of Lactobacillus rhamnosus GG Suppresses Allergic Airway Inflammation in Mouse Offspring.” Clinical and Experimental Allergy 37: 348–357.
   PubMed Web of Science ®Google Scholar
• Canu, I. G, et al. 2016. “Human Exposure to Carbon-Based Fibrous Nanomaterials: A Review.” International Journal of Hygiene and Environmental Health. 219: 166–175.
   PubMed Web of Science ®Google Scholar
• Cao, L., J. Wang, Y. Zhu, I. Tseu, and M. Post. 2010. “Maternal Endotoxin Exposure Attenuates Allergic Airway Disease in Infant Rats.” American Journal of Physiology-Lung Cellular and Molecular Physiology 298 (5): L670–L677. doi:10.1152/ajplung.00399.2009.
   PubMed Web of Science ®Google Scholar
• Clausen, S. K., M. Bergqvist, L. K. Poulsen, O. M. Poulsen, and G. D. Nielsen. 2003. “Development of Sensitisation or Tolerance Following Repeated OVA Inhalation in BALB/cJ Mice. Dose-Dependency and Modulation by the Al(OH)3 Adjuvant.” Toxicology 184 (1): 51–68. doi:10.1016/S0300-483X(02)00583-8.
   PubMed Web of Science ®Google Scholar
• Conrad, M. L., R. Ferstl, R. Teich, S. Brand, N. Blümer, A. Ö. Yildirim, C. C. Patrascan, et al. 2009. “Maternal TLR Signaling Is Required for Prenatal Asthma Protection by the Nonpathogenic Microbe Acinetobacter lwoffii F78.” The Journal of Experimental Medicine 206 (13): 2869–2877., doi:10.1084/jem.20090845.
   PubMed Web of Science ®Google Scholar
• Corson, L., H. Zhu, C. Quan, G. Grunig, M. Ballaney, X. Jin, F. P. Perera, et al. 2010. “Prenatal Allergen and Diesel Exhaust Exposure and Their Effects on Allergy in Adult Offspring Mice.” Allergy, Asthma & Clinical Immunology 6 (1): 7. doi:10.1186/1710-1492-6-7.
   PubMedGoogle Scholar
• Dietert, R. R., and J. T. Zelikoff. 2008. “Early-Life Environment, Developmental Immunotoxicology, and the Risk of Pediatric Allergic Disease Including Asthma.” Birth Defects Research Part B: Developmental and Reproductive Toxicology 83 (6): 547–560. doi:10.1002/bdrb.20170.
   PubMedGoogle Scholar
• Dong, J., and Q. Ma. 2018. “Type 2 Immune Mechanisms in Carbon Nanotube-Induced Lung Fibrosis.” Frontiers in Immunology 9: 1120. doi:10.3389/fimmu.2018.01120.
   PubMed Web of Science ®Google Scholar
• El-Sayed, Y. S., R. Shimizu, A. Onoda, K. Takeda, and M. Umezawa. 2015. “Carbon Black Nanoparticle Exposure During Middle and Late Fetal Development Induces Immune Activation in Male Offspring Mice.” Toxicology 327: 53–61. doi:10.1016/j.tox.2014.11.005.
   PubMed Web of Science ®Google Scholar
• Fedulov, A. V., A. Leme, Z. Yang, M. Dahl, R. Lim, T. J. Mariani, L. Kobzik, et al. 2008. “Pulmonary Exposure to Particles During Pregnancy Causes Increased Neonatal Asthma Susceptibility.” American Journal of Respiratory Cell and Molecular Biology 38 (1): 57–67. doi:10.1165/rcmb.2007-0124OC.
   PubMed Web of Science ®Google Scholar
• Finkelman, F. D. 2014. “Diesel Exhaust Particle Exposure During Pregnancy Promotes Development of Asthma and Atopy.” Journal of Allergy and Clinical Immunology 134 (1): 73–74. doi:10.1016/j.jaci.2014.04.002.
   PubMed Web of Science ®Google Scholar
• Francis, A. P., and T. Devasena. 2018. “Toxicity of Carbon Nanotubes: A Review.” Toxicology and Industrial Health 34 (3): 200–210. doi:10.1177/0748233717747472.
   PubMed Web of Science ®Google Scholar
• Galli, S. J., M. Tsai, and A. M. Piliponsky. 2008. “The Development of Allergic Inflammation.” Nature 454 (7203): 445–454. doi:10.1038/nature07204.
   PubMed Web of Science ®Google Scholar
• Hansen, J. S, et al. 2007. “Does Lipophilicity per se Induce Adjuvant Effects? Methyl Palmitate as Model Substance Does Not Affect Ovalbumin Sensitization.” Journal of Toxicology & Environmental Health Part A: Current Issues. 70: 128–137.
   PubMed Web of Science ®Google Scholar
• Hansen, J. S., U. C. Nygaard, R. Lyle, and M. Lovik. 2012. “Early Life Interventions to Prevent Allergy in the Offspring: The Role of Maternal Immunization and Postnatal Mucosal Allergen Exposure.” International Archives of Allergy and Immunology 158 (3): 261–275. doi:10.1159/000332963.
   PubMed Web of Science ®Google Scholar
• Hansen, J. S., A. W. Nørgaard, I. K. Koponen, J. B. Sørli, M. D. Paidi, S. W. K. Hansen, P. A. Clausen, et al. 2016. “Limonene and Its Ozone-Initiated Reaction Products Attenuate Allergic Lung Inflammation in Mice.” Journal of Immunotoxicology 13 (6): 793–803., doi:10.1080/1547691X.2016.1195462.
   PubMed Web of Science ®Google Scholar
• He, J. -S., S. Narayanan, S. Subramaniam, W. Q. Ho, J. J. Lafaille, and M. A. Curotto de Lafaille. 2015. “Biology of IgE Production: IgE Cell Differentiation and the Memory of IgE responses.” Current Topics in Microbiology and Immunology 388: 1–19. doi:10.1007/978-3-319-13725-4_1.
   PubMed Web of Science ®Google Scholar
• He, J. -S., S. Subramaniam, V. Narang, K. Srinivasan, S. P. Saunders, D. Carbajo, T. Wen-Shan, et al. 2017. “IgG1 Memory B Cells Keep the Memory of IgE Responses.” Nature Communications 8 (1): 641., doi:10.1038/s41467-017-00723-0.
   PubMedGoogle Scholar
• Hiraku, Y., F. Guo, N. Ma, T. Yamada, S. Wang, S. Kawanishi, M. Murata, et al. 2016. “Multi-Walled Carbon Nanotube Induces Nitrative DNA Damage in Human Lung Epithelial Cells via HMGB1-RAGE Interaction and Toll-like Receptor 9 Activation.” Particle and Fibre Toxicology 13 (1): 16. doi:10.1186/s12989-016-0127-7.
   PubMed Web of Science ®Google Scholar
• Holt, P. G., A. H. Rose, J. E. Batty, and K. J. Turner. 1981. “Inhibition of Specific IgE Responses in Mice by Pre-Exposure to Inhaled Antigen.” International Archives of Allergy and Immunology 65 (1): 42–417. doi:10.1159/000232736.
   Google Scholar
• Hougaard, K. S., P. Jackson, Z. O. Kyjovska, R. K. Birkedal, P. -J. De Temmerman, A. Brunelli, E. Verleysen, et al. 2013. “Effects of Lung Exposure to Carbon Nanotubes on Female Fertility and Pregnancy. A Study in Mice.” Reproductive Toxicology. 41: 86–97. doi:10.1016/j.reprotox.2013.05.006.
   PubMed Web of Science ®Google Scholar
• Jackson, P., K. Kling, K. A. Jensen, P. A. Clausen, A. M. Madsen, H. Wallin, U. Vogel, et al. 2015. “Characterization of Genotoxic Response to 15 Multiwalled Carbon Nanotubes with Variable Physicochemical Properties Including Surface Functionalizations in the FE1-Muta(TM) Mouse Lung Epithelial Cell Line.” Environmental and Molecular Mutagenesis 56 (2): 183–203. doi:10.1002/em.21922.
   PubMed Web of Science ®Google Scholar
• Jedrychowski, W., F. P. Perera, U. Maugeri, D. Mrozek-Budzyn, E. Mroz, E. Flak, S. Edwards, et al. 2009. “Early Wheezing Phenotypes and Severity of Respiratory Illness in Very Early Childhood: Study on Intrauterine Exposure to Fine Particle Matter.” Environment International. 35 (6): 877–884. doi:10.1016/j.envint.2009.03.004.
   PubMed Web of Science ®Google Scholar
• Jedrychowski, W. A., F. P. Perera, U. Maugeri, E. Mroz, M. Klimaszewska-Rembiasz, E. Flak, S. Edwards, et al. 2010a. “Effect of Prenatal Exposure to Fine Particulate Matter on Ventilatory Lung Function of Preschool Children of Non-Smoking Mothers.” Paediatric and Perinatal Epidemiology 24 (5): 492–501. doi:10.1111/j.1365-3016.2010.01136.x.
   PubMed Web of Science ®Google Scholar
• Jedrychowski, W. A., F. P. Perera, U. Maugeri, D. Mrozek-Budzyn, E. Mroz, M. Klimaszewska-Rembiasz, E. Flak, et al. 2010b. “Intrauterine Exposure to Polycyclic Aromatic Hydrocarbons, Fine Particulate Matter and Early Wheeze. Prospective Birth Cohort Study in 4-Year Olds.” Pediatric Allergy and Immunology 21 (4p2): e723–32., doi:10.1111/j.1399-3038.2010.01034.x.
   PubMedGoogle Scholar
• Jedrychowski, W. A., F. P. Perera, J. D. Spengler, E. Mroz, L. Stigter, E. Flak, R. Majewska, et al. 2013. “Intrauterine Exposure to Fine Particulate Matter as a Risk Factor for Increased Susceptibility to Acute Broncho-Pulmonary Infections in Early Childhood.” International Journal of Hygiene and Environmental Health 216 (4): 395–401. doi:10.1016/j.ijheh.2012.12.014.
   PubMed Web of Science ®Google Scholar
• Johansson, H. K. L., J. S. Hansen, B. Elfving, S. P. Lund, Z. O. Kyjovska, S. Loft, K. K. Barfod, et al. 2017. “Airway Exposure to Multi-Walled Carbon Nanotubes Disrupts the Female Reproductive Cycle Without Affecting Pregnancy Outcomes in Mice.” Particle and Fibre Toxicology 14 (1): 17., doi:10.1186/s12989-017-0197-1.
   PubMedGoogle Scholar
• Kilkenny, C., W. J. Browne, I. C. Cuthill, M. Emerson, and D. G. Altman. 2010. “Improving Bioscience Research Reporting: The ARRIVE Guidelines for Reporting Animal Research.” PLoS Biology 8 (6): e1000412. doi:10.1371/journal.pbio.1000412.
   PubMed Web of Science ®Google Scholar
• Kolosnjaj-Tabi, J., J. Just, K. B. Hartman, Y. Laoudi, S. Boudjemaa, D. Alloyeau, H. Szwarc, et al. 2015. “Anthropogenic Carbon Nanotubes Found in the Airways of Parisian Children.” EBioMedicine 2 (11): 1697–1704. doi:10.1016/j.ebiom.2015.10.012.
   PubMed Web of Science ®Google Scholar
• Looney, T. J., J. -Y. Lee, K. M. Roskin, R. A. Hoh, J. King, J. Glanville, Y. Liu, et al. 2016. “Human B-Cell Isotype Switching Origins of IgE.” Journal of Allergy and Clinical Immunology 137 (2): 579–586.e7. doi:10.1016/j.jaci.2015.07.014.
   PubMed Web of Science ®Google Scholar
• Lowrey, J. A., N. D. L. Savage, D. Palliser, M. Corsin-Jimenez, L. M. G. Forsyth, G. Hall, S. Lindey, et al. 1998. “Induction of Tolerance via the Respiratory Mucosa.” International Archives of Allergy and Immunology 116 (2): 93–102., doi:10.1159/000023931.
   PubMed Web of Science ®Google Scholar
• Mackenzie, N. M. 1990. “Transport of Maternally Derived Immunoglobulins Across the Intestinal Epithelium.” In Ontogeny of the Immune System of the Gut, edited by T. T. MacDonald, 69–82. 1st ed. Boca Raton, FL: CRC Press.
   Google Scholar
• Manners, S., R. Alam, D. A. Schwartz, and M. M. Gorska. 2014. “A Mouse Model Links Asthma Susceptibility to Prenatal Exposure to Diesel Exhaust.” Journal of Allergy and Clinical Immunology 134 (1): 63–72. doi:10.1016/j.jaci.2013.10.047.
   PubMed Web of Science ®Google Scholar
• Mitchell, L. A., J. Gao, R. V. Wal, A. Gigliotti, S. W. Burchiel, and J. D. McDonald. 2007. “Pulmonary and Systemic Immune Response to Inhaled Multiwalled Carbon Nanotubes.” Toxicological Sciences 100 (1): 203–214. doi:10.1093/toxsci/kfm196.
   PubMed Web of Science ®Google Scholar
• Mitchell, L. A., F. T. Lauer, S. W. Burchiel, and J. D. McDonald. 2009. “Mechanisms for How Inhaled Multiwalled Carbon Nanotubes Suppress Systemic Immune Function in Mice.” Nature Nanotechnology 4 (7): 451–456. doi:10.1038/nnano.2009.151.
   PubMed Web of Science ®Google Scholar
• Mukherjee, S. P., O. Bondarenko, P. Kohonen, F. T. Andón, T. Brzicová, I. Gessner, S. Mathur, et al. 2018. “Macrophage Sensing of Single-Walled Carbon Nanotubes via Toll-like Receptors.” Scientific Reports 8 (1): 1115. doi:10.1038/s41598-018-19521-9.
   PubMedGoogle Scholar
• Nygaard, U. C., J. S. Hansen, M. Samuelsen, T. Alberg, C. D. Marioara, and M. Løvik. 2009. “Single-Walled and Multi-Walled Carbon Nanotubes Promote Allergic Immune Responses in Mice.” Toxicological Sciences 109 (1): 113–123. doi:10.1093/toxsci/kfp057.
   PubMed Web of Science ®Google Scholar
• Pandya, R. J., G. Solomon, A. Kinner, and J. R. Balmes. 2002. “Diesel Exhaust and Asthma: Hypotheses and Molecular Mechanisms of Action.” Environmental Health Perspectives. 110 (Suppl 1): 103–112. doi:10.1289/ehp.02110s1103.
   PubMed Web of Science ®Google Scholar
• Parnia, S., and A. J. Frew. 2001. “Is Diesel the Cause for the Increase in Allergic Disease?” Ann Allerg Asthma Immunol 87 (6): 18–23. doi:10.1016/S1081-1206(10)62335-6.
   PubMed Web of Science ®Google Scholar
• Pawankar R., S. T. Holgate, G. Walter Canonica, R. F. Lockey, M. S. Blaiss, eds. 2013. WAO White Book on Allergy: Update 2013. Milwaukee, WI: World Allergy Organization.
   Google Scholar
• Poulsen, S. S., A. T. Saber, A. Mortensen, J. Szarek, D. Wu, A. Williams, O. Andersen, et al. 2015a. “Changes in Cholesterol Homeostasis and Acute Phase Response Link Pulmonary Exposure to Multi-Walled Carbon Nanotubes to Risk of Cardiovascular Disease.” Toxicology and Applied Pharmacology. 283 (3): 210–222. doi:10.1016/j.taap.2015.01.011.
   PubMed Web of Science ®Google Scholar
• Poulsen, S. S., A. T. Saber, A. Williams, O. Andersen, C. Købler, R. Atluri, M. E. Pozzebon, et al. 2015b. “MWCNTs of Different Physicochemical Properties Cause Similar Inflammatory Responses, but Differences in Transcriptional and Histological Markers of Fibrosis in Mouse Lungs.” Toxicology and Applied Pharmacology. 284 (1): 16–32.
   PubMed Web of Science ®Google Scholar
• Rajasekaran, S., R. Anuradha, and R. Bethunaickan. 2017. “TLR Specific Immune Responses Against Helminth Infections.” Journal of Parasitology Research. 2017: 6865789. doi:10.1155/2017/6865789.
   PubMedGoogle Scholar
• Rychlik, K. A., J. R. Secrest, C. Lau, J. Pulczinski, M. L. Zamora, J. Leal, R. Langley, et al. 2019. “In Utero Ultrafine Particulate Matter Exposure Causes Offspring Pulmonary Immunosuppression.” Proceedings of the National Academy of Sciences 116 (9): 3443–3448. doi:10.1073/pnas.1816103116.
   PubMed Web of Science ®Google Scholar
• Saber, A. T., S. Halappanavar, J. K. Folkmann, J. Bornholdt, A. Boisen, P. Møller, A. Williams, et al. 2009. “Lack of Acute Phase Response in the Livers of Mice Exposed to Diesel Exhaust Particles or Carbon Black by Inhalation.” Particle and Fibre Toxicology 6 (1): 12., doi:10.1186/1743-8977-6-12.
   PubMedGoogle Scholar
• Saber, A., N. Jacobsen, A. Mortensen, J. Szarek, P. Jackson, A. Madsen, K. Jensen, et al. 2012. “Nanotitanium Dioxide Toxicity in Mouse Lung Is Reduced in Sanding Dust from Paint.” Particle and Fibre Toxicology 9 (1): 4. doi:10.1186/1743-8977-9-4.
   PubMedGoogle Scholar
• Shimizu, R., M. Umezawa, S. Okamoto, A. Onoda, M. Uchiyama, K. Tachibana, S. Watanabe, et al. 2014. “Effect of Maternal Exposure to Carbon Black Nanoparticle During Early Gestation on the Splenic Phenotype of Neonatal Mouse.” The Journal of Toxicological Sciences 39 (4): 571–578. doi:10.2131/jts.39.571.
   PubMed Web of Science ®Google Scholar
• Smole, U., I. Schabussova, W. F. Pickl, and U. Wiedermann. 2017. “Murine Models for Mucosal Tolerance in Allergy.” Seminars in Immunology. 30: 12–27. doi:10.1016/j.smim.2017.07.007.
   PubMed Web of Science ®Google Scholar
• Sudowe, S.,. A. Rademaekers, and E. Kolsch. 1997. “Antigen Dose-Dependent Predominance of Either Direct or Sequential Switch in IgE Antibody Responses.” Immunology 91 (3): 464–472. doi:10.1046/j.1365-2567.1997.00268.x.
   PubMed Web of Science ®Google Scholar
• Turabekova, M., B. Rasulev, M. Theodore, J. Jackman, D. Leszczynska, and J. Leszczynski. 2014. “Immunotoxicity of Nanoparticles: A Computational Study Suggests That CNTs and C60 Fullerenes Might Be Recognized as Pathogens by Toll-like Receptors.” Nanoscale 6 (7): 3488–3495. doi:10.1039/C3NR05772K.
   PubMed Web of Science ®Google Scholar
• Van Loveren, H., and A. Piersma. 2004. “Immunotoxicological Consequences of Perinatal Chemical Exposures.” Toxicology Letters. 149 (1-3): 141–145. doi:10.1016/j.toxlet.2003.12.028.
   PubMed Web of Science ®Google Scholar
• Vlaanderen, J., A. Pronk, N. Rothman, A. Hildesheim, D. Silverman, H. D. Hosgood, S. Spaan, et al. 2017. “A Cross-Sectional Study of Changes in Markers of Immunological Effects and Lung Health Due to Exposure to Multi-Walled Carbon Nanotubes.” Nanotoxicology 11 (3): 395–404., doi:10.1080/17435390.2017.1308031.
   PubMed Web of Science ®Google Scholar
• Wang, L., and K. E. Pinkerton. 2008. “Detrimental Effects of Tobacco Smoke Exposure During Development on Postnatal Lung Function and Asthma.” Birth Defects Research Part C: Embryo Today: Reviews 84 (1): 54–60. doi:10.1002/bdrc.20114.
   PubMedGoogle Scholar
• Weichenthal, S., A. Dufresne, and C. Infante-Rivard. 2007. “Indoor Ultrafine Particles and Childhood Asthma: Exploring a Potential Public Health Concern.” Indoor Air 17 (2): 81–91. doi:10.1111/j.1600-0668.2006.00446.x.
   PubMed Web of Science ®Google Scholar
• Whitten, W. K. 1959. “Occurrence of Anoestrus in Mice Caged in Groups.” Journal of Endocrinology 18 (1): 102–107. doi:10.1677/joe.0.0180102.
   PubMed Web of Science ®Google Scholar
• Xiong, H., J. Dolpady, M. Wabl, M. A. Curotto de Lafaille, and J. J. Lafaille. 2012. “Sequential Class Switching Is Required for the Generation of High Affinity IgE Antibodies.” The Journal of Experimental Medicine 209 (2): 353–364. doi:10.1084/jem.20111941.
   PubMed Web of Science ®Google Scholar
• Zhang, M. F., H. Zola, L. C. Read, and I. A. Penttila. 1999. “Localization of Transforming Growth Factor-Beta Receptor Types I, II, and III in the Postnatal Rat Small Intestine.” Pediatric Research 46 (6): 657–665. doi:10.1203/00006450-199912000-00017.
   PubMed Web of Science ®Google Scholar