Prenatal exposure to diesel exhaust PM2.5 causes offspring β cell dysfunction in adulthood
Open accessAbstract
Environmental stressors that encounter in early-life and cause abnormal fetal and/or neonatal development may increase susceptibility to non-communicable diseases such as diabetes. Maternal exposure to ambient fine particulate matter (PM 2.5) is associated with various fetal abnormalities, suggesting that it may program offspring’s susceptibility to diabetes. In the present study, we therefore examined whether maternal exposure to diesel exhaust PM 2.5 (DEP), one of the major sources of ambient PM 2.5 in urban areas, programs adult offspring’s glucose metabolism. Female C57Bl/6J mice were intratracheally instilled with DEP or vehicle throughout a 7-wk preconceptional period, gestation, and lactation, and the glucose homeostasis of their adult male offspring was assessed. Intraperitoneal glucose tolerance test (IPGTT) revealed that the maternal exposure to DEP significantly impaired adult male offspring’s glucose tolerance. Unexpectedly, it did not influence their insulin sensitivity, whereas it significantly decreased their glucose-induced insulin secretion (GIIS). This deficit in insulin secretion was corroborated by their significant decrease in arginine-induced insulin secretion. Histological analysis demonstrated that the deficit in insulin secretion was accompanied by the decrease in pancreatic islet and β cell sizes. To differentiate the effects of maternal exposure to DEP before birth and during lactation, some offspring were cross-fostered once born. We did not observe any significant effect of cross-fostering on the glucose homeostasis of adult male offspring and the function and morphology of their β cells. Prenatal exposure to DEP programs the morphology and function of β cells and thus homeostatic regulation of glucose metabolism in adult male offspring.
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Prenatal exposure to diesel exhaust PM2.5 in C57Bl/6 mice altered the morphology and function of male offspring pancreatic β cells, correlating with decreased pancreatic islet cell and β cell sizes.
“Chen et al. [86] demonstrated prenatal exposure to DE PM2.5 in C57Bl/6 mice altered the morphology and function of male offspring pancreatic β cells, which are responsible for producing insulin, thus altering glucose metabolism. This deficiency correlated with decreased pancreatic islet cell and β cell sizes.”
From Air pollution and children’s health—a review of adverse effects associated with prenatal exposure from fine to ultrafine particulate matter (2021) · cites this paper as [86]
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Rich, D. Q., Liu, K., Zhang, J., Thurston, S. W., Stevens, T. P., Pan, Y., Kane, C., Weinberger, B., Ohman-Strickland, P., Woodruff, T. J., et al. (2015) · Environmental Health Perspectives · doi:10.1289/ehp.1408795 · Cited by 174 · see citing works
Fleisch, A. F., Rifas-Shiman, S. L., Koutrakis, P., Schwartz, J. D., Kloog, I., Melly, S., Coull, B. A., Zanobetti, A., Gillman, M. W., Gold, D. R., et al. (2015) · Epidemiology · doi:10.1097/ede.0000000000000203 · Cited by 140 · see citing works
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Research works printed but not linked: 24
- Abdelaal M, le Roux CW, Docherty NG. Morbidity and mortality associated with obesity. Ann Transl Med 5: 161, 2017. doi:10.21037/atm. 2017.03.107. · DOI · Paper page
- Bolton JL, Auten RL, Bilbo SD. Prenatal air pollution exposure induces sexually dimorphic fetal programming of metabolic and neuroinflamma- tory outcomes in adult offspring. Brain Behav Immun 37: 30 -44, 2014. doi:10.1016/j.bbi.2013.10.029. · DOI
- Bolton JL, Smith SH, Huff NC, Gilmour MI, Foster WM, Auten RL, Bilbo SD. Prenatal air pollution exposure induces neuroinflammation and predisposes offspring to weight gain in adulthood in a sex-specific manner. FASEB J 26: 4743-4754, 2012. doi:10.1096/fj.12-210989. · DOI
- Bonzini M, Carugno M, Grillo P, Mensi C, Bertazzi PA, Pesatori AC. Impact of ambient air pollution on birth outcomes: systematic review of the current evidences. Med Lav 101: 341-363, 2010.
- Chen M, Liang S, Zhou H, Xu Y, Qin X, Hu Z, Wang X, Qiu L, Wang W, Zhang Y, Ying Z. Prenatal and postnatal mothering by diesel exhaust PM2.5-exposed dams differentially program mouse energy metabolism. Part Fibre Toxicol 14: 3, 2017. doi:10.1186/s12989-017-0183-7. · DOI · Paper page
- Chen M, Wang X, Hu Z, Zhou H, Xu Y, Qiu L, Qin X, Zhang Y, Ying Z. Programming of mouse obesity by maternal exposure to concentrated ambient fine particles. Part Fibre Toxicol 14: 20, 2017. doi:10.1186/ s12989-017-0201-9. · DOI · Paper page
- Dadvand P, Parker J, Bell ML, Bonzini M, Brauer M, Darrow LA, Gehring U, Glinianaia SV, Gouveia N, Ha EH, Leem JH, van den Hooven EH, Jalaludin B, Jesdale BM, Lepeule J, Morello-Frosch R, Morgan GG, Pesatori AC, Pierik FH, Pless-Mulloli T, Rich DQ, Sathyanarayana S, Seo J, Slama R, Strickland M, Tamburic L, Wartenberg D, Nieuwenhuijsen MJ, Woodruff TJ. Maternal exposure to particulate air pollution and term birth weight: a multi-country evalu- ation of effect and heterogeneity. Environ Health Perspect 121: 267-373, 2013. doi:10.1289/ehp.1205575. · DOI
- Grandjean P, Barouki R, Bellinger DC, Casteleyn L, Chadwick LH, Cordier S, Etzel RA, Gray KA, Ha EH, Junien C, Karagas M, Kawamoto T, Paige Lawrence B, Perera FP, Prins GS, Puga A, Rosenfeld CS, Sherr DH, Sly PD, Suk W, Sun Q, Toppari J, van den Hazel P, Walker CL, Heindel JJ. Life-long implications of developmen- tal exposure to environmental stressors: new perspectives. Endocrinology 156: 3408 -3415, 2015. doi:10.1210/EN.2015-1350. · DOI
- Hales CN, Barker DJ. The thrifty phenotype hypothesis. Br Med Bull 60: 5-20, 2001. doi:10.1093/bmb/60.1.5. · DOI
- Hyder A, Lee HJ, Ebisu K, Koutrakis P, Belanger K, Bell ML. PM2.5 exposure and birth outcomes: use of satellite-and monitor-based data. Epidemiology 25: 58 -67, 2014. doi:10.1097/EDE.0000000000000027. · DOI
- Kammoun HL, Kraakman MJ, Febbraio MA. Adipose tissue inflam- mation in glucose metabolism. Rev Endocr Metab Disord 15: 31-44, 2014. doi:10.1007/s11154-013-9274-4. · DOI
- Kyjovska ZO, Jacobsen NR, Saber AT, Bengtson S, Jackson P, Wallin H, Vogel U. DNA strand breaks, acute phase response and inflammation following pulmonary exposure by instillation to the diesel exhaust particle NIST1650b in mice. Mutagenesis 30: 499 -507, 2015. doi:10.1093/ mutage/gev009. · DOI
- Lawlor N, Khetan S, Ucar D, Stitzel ML. Genomics of islet (dys)func- tion and Type 2 diabetes. Trends Genet 33: 244 -255, 2017. doi:10.1016/ j.tig.2017.01.010. · DOI
- Lim SS, Vos T, Flaxman AD, Danaei G, Shibuya K, Adair-Rohani H, Amann M, Anderson HR, Andrews KG, Aryee M, Atkinson C, Bacchus LJ, Bahalim AN, Balakrishnan K, Balmes J, Barker-Collo S, Baxter A, Bell ML, Blore JD, Blyth F, Bonner C, Borges G, Bourne R, Boussinesq M, Brauer M, Brooks P, Bruce NG, Brunekreef B, Bryan- Hancock C, Bucello C, Buchbinder R, Bull F, Burnett RT, Byers TE, Calabria B, Carapetis J, Carnahan E, Chafe Z, Charlson F, Chen H, Chen JS, Cheng AT, Child JC, Cohen A, Colson KE, Cowie BC, Darby S, Darling S, Davis A, Degenhardt L, Dentener F, Des Jarlais DC, Devries K, Dherani M, Ding EL, Dorsey ER, Driscoll T, Edmond K, Ali SE, Engell RE, Erwin PJ, Fahimi S, Falder G, Farzadfar F, Ferrari A, Finucane MM, Flaxman S, Fowkes FG, Freedman G, Freeman MK, Gakidou E, Ghosh S, Giovannucci E, Gmel G, Graham K, Grainger R, Grant B, Gunnell D, Gutierrez HR, Hall W, Hoek HW, Hogan A, Hosgood HD III, Hoy D, Hu H, Hubbell BJ, Hutchings SJ, Ibeanusi SE, Jacklyn GL, Jasrasaria R, Jonas JB, Kan H, Kanis JA, Kassebaum N, Kawakami N, Khang YH, Khatibzadeh S, Khoo JP, Kok C, Laden F, Lalloo R, Lan Q, Lathlean T, Leasher JL, Leigh J, Li Y, Lin JK, Lipshultz SE, London S, Lozano R, Lu Y, Mak J, Malekzadeh R, Mallinger L, Marcenes W, March L, Marks R, Martin R, McGale P, McGrath J, Mehta S, Mensah GA, Merriman TR, Micha R, Michaud C, Mishra V, Mohd Hanafiah K, Mokdad AA, Morawska L, Mozaffarian D, Murphy T, Naghavi M, Neal B, Nelson PK, Nolla JM, Norman R, Olives C, Omer SB, Orchard J, Osborne R, Ostro B, Page A, Pandey KD, Parry CD, Passmore E, Patra J, Pearce N, Pelizzari PM, Petzold M, Phillips MR, Pope D, Pope CA III, Powles E79 PM2.5 EXPOSURE AND OFFSPRING  CELL FUNCTION AJP-Endocrinol Metab • doi:10.1152/ajpendo.00336.2017 • www.ajpendo.org Downloaded from journals.physiology.org/journal/ajpendo (173.232.020.223) on September 1, 2023. · DOI
- J, Rao M, Razavi H, Rehfuess EA, Rehm JT, Ritz B, Rivara FP, Roberts T, Robinson C, Rodriguez-Portales JA, Romieu I, Room R, Rosenfeld LC, Roy A, Rushton L, Salomon JA, Sampson U, Sanchez- Riera L, Sanman E, Sapkota A, Seedat S, Shi P, Shield K, Shivakoti R, Singh GM, Sleet DA, Smith E, Smith KR, Stapelberg NJ, Steenland K, Stöckl H, Stovner LJ, Straif K, Straney L, Thurston GD, Tran JH, Van Dingenen R, van Donkelaar A, Veerman JL, Vijayakumar L, Weintraub R, Weissman MM, White RA, Whiteford H, Wiersma ST, Wilkinson JD, Williams HC, Williams W, Wilson N, Woolf AD, Yip P, Zielinski JM, Lopez AD, Murray CJ, Ezzati M, AlMazroa MA, Memish ZA. A comparative risk assessment of burden of disease and injury attributable to 67 risk factors and risk factor clusters in 21 regi- ons, 1990-2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 380: 2224 -2260, 2012. doi:10.1016/S0140-6736(12) 61766-8. · DOI · Paper page
- Paul R, Choudhury A, Choudhury S, Mazumder MK, Borah A. Cholesterol in pancreatic -cell death and dysfunction: underlying mech- anisms and pathological implications. Pancreas 45: 317-324, 2016. doi: 10.1097/MPA.0000000000000486. · DOI
- Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45, 2001. doi:10.1093/nar/29. 9.e45. · DOI · Paper page
- Savitz DA, Bobb JF, Carr JL, Clougherty JE, Dominici F, Elston B, Ito K, Ross Z, Yee M, Matte TD. Ambient fine particulate matter, nitrogen dioxide, and term birth weight in New York, New York. Am J Epidemiol 179: 457-466, 2014. doi:10.1093/aje/kwt268. · DOI
- Schembari A, de Hoogh K, Pedersen M, Dadvand P, Martinez D, Hoek G, Petherick ES, Wright J, Nieuwenhuijsen MJ. Ambient air pollution and newborn size and adiposity at birth: differences by maternal ethnicity (the Born in Bradford Study Cohort). Environ Health Perspect 123: 1208 -1215, 2015. doi:10.1289/ehp.1408675. · DOI
- Sun X, Luo X, Zhao C, Chung Ng RW, Lim CE, Zhang B, Liu T. The association between fine particulate matter exposure during pregnancy and preterm birth: a meta-analysis. BMC Pregnancy Childbirth 15: 300, 2015. doi:10.1186/s12884-015-0738-2. · DOI
- Talchai C, Xuan S, Lin HV, Sussel L, Accili D. Pancreatic  cell dedifferentiation as a mechanism of diabetic  cell failure. Cell 150: 1223-1234, 2012. doi:10.1016/j.cell.2012.07.029. · DOI · Paper page
- Thams P, Capito K. L-Arginine stimulation of glucose-induced insulin secretion through membrane depolarization and independent of nitric oxide. Eur J Endocrinol 140: 87-93, 1999. doi:10.1530/eje.0.1400087. · DOI
- Valdiglesias V, Pásaro E, Méndez J, Laffon B. In vitro evaluation of selenium genotoxic, cytotoxic, and protective effects: a review. Arch Toxicol 84: 337-351, 2010. doi:10.1007/s00204-009-0505-0. · DOI
- Vasavada RC, Cavaliere C, D'Ercole AJ, Dann P, Burtis WJ, Madlener AL, Zawalich K, Zawalich W, Philbrick W, Stewart AF. Overexpression of parathyroid hormone-related protein in the pancre- atic islets of transgenic mice causes islet hyperplasia, hyperinsulin- emia, and hypoglycemia. J Biol Chem 271: 1200 -1208, 1996. doi:10. 1074/jbc.271.2.1200. · DOI
Cited by
Sorted by citations
Johnson, N. M., Hoffmann, A. R., Behlen, J. C., Lau, C., Pendleton, D., Harvey, N., Shore, R., Li, Y., Chen, J., Tian, Y., et al. (2021) · Environmental Health and Preventive Medicine · doi:10.1186/s12199-021-00995-5 · Cited by 339 · see citing works
- Authors
- Chen, M., Liang, S., Qin, X., Zhang, L., Qiu, L., Chen, S., Hu, Z., Xu, Y., Wang, W., Zhang, Y., Cao, Q., & Ying, Z.
- Affiliations
- University of Maryland, Baltimore (US)
- Fudan University (CN)
- Corresponding author
- Ying, Zhekang
- Venue
- American Journal of Physiology-Endocrinology and Metabolism
- Publisher
- American Physiological Society
- Published
- 2018-07-01
- Volume
- 315
- Issue
- 1
- Pages
- E72-E80
- ISSN
- 0193-1849 (ISSN-L)
- 1522-1555
- PMC
- PMC6087722
- OpenAlex
- W2775860725
- Cited by
- 37
- References
- 2
- Citations by year
- 2026: 3 · 2025: 4 · 2024: 7 · 2023: 8 · 2022: 3 · 2021: 5 · 2020: 3 · 2019: 2 · 2018: 2
- FWCI
- 1.96
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- American Journal of Physiology-Endocrinology and Metabolism (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- HHS | NIH | National Institute of Environmental Health Sciences (NIEHS) (R01ES024516)
- National Natural Science Foundation of China (NSFC) (81500216, 81770805)
- Topics
- Health Sciences › Medicine › Surgery › Pancreatic function and diabetes
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Air Quality and Health Impacts
- Keywords
- diesel exhaust, PM2.5, prenatal exposure, beta-cell dysfunction, glucose tolerance, insulin secretion, glucose-stimulated insulin secretion, pancreatic islets, developmental programming, diabetes susceptibility, cross-fostering, glucose homeostasis, insulin sensitivity
- MeSH terms
- Insulin Secretion, Air Pollutants, Animals, Vehicle Emissions, Female, Glucose, Glucose Tolerance Test, Insulin Resistance, Male, Mice, Inbred C57BL, Pregnancy, Prenatal Exposure Delayed Effects, Maternal Exposure, Cell Size, Insulin-Secreting Cells, Mice, Particulate Matter
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