Cited by 37Pancreatic function and diabetesBirth, Development, and HealthAir Quality and Health Impacts

Prenatal exposure to diesel exhaust PM2.5 causes offspring β cell dysfunction in adulthood

Open access
Chen, Minjie, Liang, Shuai, Qin, Xiaobo, Zhang, Li, Qiu, Lianglin, Chen, Sufang, Hu, Ziying, Xu, Yanyi +4 more·2018·American Journal of Physiology-Endocrinology and Metabolism

Abstract

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.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1152/ajpendo.00336.2017

Cites

2 of 2 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 24

  1. 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
  2. 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
  3. 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
  4. 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.
  5. 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
  6. 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
  7. 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
  8. 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
  9. Hales CN, Barker DJ. The thrifty phenotype hypothesis. Br Med Bull 60: 5-20, 2001. doi:10.1093/bmb/60.1.5. · DOI
  10. 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
  11. 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
  12. 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
  13. 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
  14. 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
  15. 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
  16. 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
  17. 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
  18. 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
  19. 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
  20. 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
  21. 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
  22. 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
  23. 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
  24. 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

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
Published
2018-07-01
Volume
315
Issue
1
Pages
E72-E80
ISSN
  • 0193-1849 (ISSN-L)
  • 1522-1555
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
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

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review