Air Pollution Stress and the Aging Phenotype: The Telomere Connection

Current environmental health reports

Volumn 3, Issue 3, 2016, Pages 258-269

  Martens, Dries S ^a   Nawrot, Tim S ^a,b  

^a HASSELT UNIVERSITY   (Belgium)

^b UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Aging; Air pollution; Exposome; Telomere

Indexed keywords

AGING; AIR POLLUTANT; ENVIRONMENTAL EXPOSURE; HUMAN; PARTICULATE MATTER; PHENOTYPE; RISK FACTOR; TELOMERE;

AGING; AIR POLLUTANTS; ENVIRONMENTAL EXPOSURE; HUMANS; PARTICULATE MATTER; PHENOTYPE; RISK FACTORS; TELOMERE;

EID: 84992107384     PISSN: None     EISSN: 21965412     Source Type: Journal    
DOI: 10.1007/s40572-016-0098-8     Document Type: Article

References (142)

1. Levy JI, Hammitt JK, Spengler JD. Estimating the mortality impacts of particulate matter: what can be learned from between-study variability? Environ Health Perspect. 2000;108(2):109–17.
2. Nawrot TS, Perez L, Kunzli N, et al. Public health importance of triggers of myocardial infarction: a comparative risk assessment. Lancet. 2011;377(9767):732–40.
3. Provost EB, Louwies T, Cox B, et al. Short-term fluctuations in personal black carbon exposure are associated with rapid changes in carotid arterial stiffening. Environ Int. 2016;88:228–34.
4. Beelen R, Raaschou-Nielsen O, Stafoggia M, et al. Effects of long-term exposure to air pollution on natural-cause mortality: an analysis of 22 European cohorts within the multicentre ESCAPE project. Lancet. 2014;383(9919):785–95.
5. Beelen R, Stafoggia M, Raaschou-Nielsen O, et al. Long-term exposure to air pollution and cardiovascular mortality: an analysis of 22 European cohorts. Epidemiology. 2014;25(3):368–78.
6. Hamra GB, Guha N, Cohen A, et al. Outdoor particulate matter exposure and lung cancer: a systematic review and meta-analysis. Environ Health Perspect. 2014;122(9):906–11.
7. Laden F, Schwartz J, Speizer FE, et al. Reduction in fine particulate air pollution and mortality: Extended follow-up of the Harvard Six Cities study. Am J Respir Crit Care Med. 2006;173(6):667–72.
8. Provost EB, Madhloum N, Int Panis L, et al. Carotid intima-media thickness, a marker of subclinical atherosclerosis, and particulate air pollution exposure: the meta-analytical evidence. PLoS One. 2015;10(5):e0127014.
9. WHO. Health Risks of Particulate Matter from Long-range Transboundary Air Pollution (World Health Organization). 2006. http://www.euro.who.int/__data/assets/pdf_file/0006/78657/E88189.pdf.
10. Pope 3rd CA, Ezzati M, Dockery DW. Fine-particulate air pollution and life expectancy in the United States. N Engl J Med. 2009;360(4):376–86.
11. Hanninen O, Knol AB, Jantunen M, et al. Environmental burden of disease in Europe: assessing nine risk factors in six countries. Environ Health Perspect. 2014;122(5):439–46.
12. Collaborators GBDRF, Forouzanfar MH, Alexander L, et al. Global, regional, and national comparative risk assessment of 79 behavioural, environmental and occupational, and metabolic risks or clusters of risks in 188 countries, 1990-2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet. 2015;386(10010):2287–323.
13. Barker DJ. Fetal origins of coronary heart disease. BMJ. 1995;311(6998):171–4.
14. Dietert RR, DeWitt JC, Germolec DR, et al. Breaking patterns of environmentally influenced disease for health risk reduction: immune perspectives. Environ Health Perspect. 2010;118(8):1091–9.
15. Arbeev KG, Ukraintseva SV, Akushevich I, et al. Age trajectories of physiological indices in relation to healthy life course. Mech Ageing Dev. 2011;132(3):93–102.
16. Belsky DW, Caspi A, Houts R, et al. Quantification of biological aging in young adults. Proc Natl Acad Sci U S A. 2015;112(30):E4104–10.
17. Jacobs L, Buczynska A, Walgraeve C, et al. Acute changes in pulse pressure in relation to constituents of particulate air pollution in elderly persons. Environ Res. 2012;117:60–7.
18. Liang R, Zhang B, Zhao X, et al. Effect of exposure to PM2.5 on blood pressure: a systematic review and meta-analysis. J Hypertens. 2014;32(11):2130–40. discussion 41.
19. Pieters N, Koppen G, Van Poppel M, et al. Blood pressure and same-day exposure to air pollution at school: associations with nano-sized to coarse PM in children. Environ Health Perspect. 2015;123(7):737–42.
20. Calderon-Garciduenas L, Franco-Lira M, D'Angiulli A, et al. Mexico city normal weight children exposed to high concentrations of ambient PM2.5 show high blood leptin and endothelin-1, vitamin D deficiency, and food reward hormone dysregulation versus low pollution controls. Relevance for obesity and Alzheimer disease. Environ Res. 2015;140:579–92.
21. Eze IC, Schaffner E, Fischer E, et al. Long-term air pollution exposure and diabetes in a population-based Swiss cohort. Environ Int. 2014;70:95–105.
22. Struijker-Boudier HA, Heijnen BF, Liu YP, et al. Phenotyping the microcirculation. Hypertension. 2012;60(2):523–7.
23. Adar SD, Klein R, Klein BE, et al. Air Pollution and the microvasculature: a cross-sectional assessment of in vivo retinal images in the population-based multi-ethnic study of atherosclerosis (MESA). PLoS Med. 2010;7(11):e1000372.
24. Louwies T, Panis LI, Kicinski M, et al. Retinal microvascular responses to short-term changes in particulate air pollution in healthy adults. Environ Health Perspect. 2013;121(9):1011–6.
25. Wild CP, Kleinjans J. Children and increased susceptibility to environmental carcinogens: evidence or empathy? Cancer Epidemiol Biomarkers Prev. 2003;12(12):1389–94.
26. Blackburn EH. Structure and function of telomeres. Nature. 1991;350(6319):569–73.
27. Wright WE, Tesmer VM, Huffman KE, et al. Normal human chromosomes have long G-rich telomeric overhangs at one end. Genes Dev. 1997;11(21):2801–9.
28. Levy MZ, Allsopp RC, Futcher AB, et al. Telomere end-replication problem and cell aging. J Mol Biol. 1992;225(4):951–60.
29. Hayflick L. The limited in vitro lifetime of human diploid cell strains. Exp Cell Res. 1965;37:614–36.
30. Shay JW, Wright WE. Hayflick, his limit, and cellular ageing. Nat Rev Mol Cell Biol. 2000;1(1):72–6.
31. Campisi J, d'Adda di Fagagna F. Cellular senescence: when bad things happen to good cells. Nat Rev Mol Cell Biol. 2007;8(9):729–40.
32. Shay JW, Wright WE. Senescence and immortalization: role of telomeres and telomerase. Carcinogenesis. 2005;26(5):867–74.
33. Shay JW, Wright WE, Werbin H. Defining the molecular mechanisms of human cell immortalization. Biochim Biophys Acta. 1991;1072(1):1–7.
34. Blackburn EH, Epel ES, Lin J. Human telomere biology: A contributory and interactive factor in aging, disease risks, and protection. Science. 2015;350(6265):1193–8.
35. Kim NW, Piatyszek MA, Prowse KR, et al. Specific association of human telomerase activity with immortal cells and cancer. Science. 1994;266(5193):2011–5.
36. Hiyama K, Hirai Y, Kyoizumi S, et al. Activation of telomerase in human lymphocytes and hematopoietic progenitor cells. J Immunol. 1995;155(8):3711–5.
37. de Lange T. Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev. 2005;19(18):2100–10.
38. O'Sullivan RJ, Karlseder J. Telomeres: protecting chromosomes against genome instability. Nat Rev Mol Cell Biol. 2010;11(3):171–81.
39. Griffith JD, Comeau L, Rosenfield S, et al. Mammalian telomeres end in a large duplex loop. Cell. 1999;97(4):503–14.
40. Greider CW. Telomeres do D-loop-T-loop. Cell. 1999;97(4):419–22.
41. Aviv A, Valdes AM, Spector TD. Human telomere biology: pitfalls of moving from the laboratory to epidemiology. Int J Epidemiol. 2006;35(6):1424–9.
42. Sanders JL, Newman AB. Telomere length in epidemiology: a biomarker of aging, age-related disease, both, or neither? Epidemiol Rev. 2013;35:112–31.
43. Daniali L, Benetos A, Susser E, et al. Telomeres shorten at equivalent rates in somatic tissues of adults. Nat Commun. 2013;4:1597.
44. Mather KA, Jorm AF, Parslow RA, et al. Is telomere length a biomarker of aging? a review. J Gerontol A Biol Sci Med Sci. 2011;66(2):202–13.
45. Benetos A, Okuda K, Lajemi M, et al. Telomere length as an indicator of biological aging: the gender effect and relation with pulse pressure and pulse wave velocity. Hypertension. 2001;37(2 Pt 2):381–5.
46. Cawthon RM, Smith KR, O'Brien E, et al. Association between telomere length in blood and mortality in people aged 60 years or older. Lancet. 2003;361(9355):393–5.
47. Fitzpatrick AL, Kronmal RA, Gardner JP, et al. Leukocyte telomere length and cardiovascular disease in the cardiovascular health study. Am J Epidemiol. 2007;165(1):14–21.
48. Nawrot TS, Staessen JA, Holvoet P, et al. Telomere length and its associations with oxidized-LDL, carotid artery distensibility and smoking. Front Biosci (Elite Ed). 2010;2:1164–8.
49. Samani NJ, Boultby R, Butler R, et al. Telomere shortening in atherosclerosis. Lancet. 2001;358(9280):472–3.
50. Haycock PC, Heydon EE, Kaptoge S, et al. Leucocyte telomere length and risk of cardiovascular disease: systematic review and meta-analysis. BMJ. 2014;349:g4227.
51. Demissie S, Levy D, Benjamin EJ, et al. Insulin resistance, oxidative stress, hypertension, and leukocyte telomere length in men from the Framingham heart study. Aging Cell. 2006;5(4):325–30.
52. Valdes AM, Andrew T, Gardner JP, et al. Obesity, cigarette smoking, and telomere length in women. Lancet. 2005;366(9486):662–4.
53. Kuznetsova T, Codd V, Brouilette S, et al. Association between left ventricular mass and telomere length in a population study. Am J Epidemiol. 2010;172(4):440–50.
54. Bischoff C, Petersen HC, Graakjaer J, et al. No association between telomere length and survival among the elderly and oldest old. Epidemiology. 2006;17(2):190–4.
55. Martin-Ruiz CM, Gussekloo J, van Heemst D, et al. Telomere length in white blood cells is not associated with morbidity or mortality in the oldest old: a population-based study. Aging Cell. 2005;4(6):287–90.
56. Hjelmborg JB, Dalgard C, Moller S, et al. The heritability of leucocyte telomere length dynamics. J Med Genet. 2015;52(5):297–302.
57. Slagboom PE, Droog S, Boomsma DI. Genetic determination of telomere size in humans: a twin study of three age groups. Am J Hum Genet. 1994;55(5):876–82.
58. Vasa-Nicotera M, Brouilette S, Mangino M, et al. Mapping of a major locus that determines telomere length in humans. Am J Hum Genet. 2005;76(1):147–51.
59. Nawrot TS, Staessen JA, Gardner JP, et al. Telomere length and possible link to X chromosome. Lancet. 2004;363(9408):507–10.
60. Andrew T, Aviv A, Falchi M, et al. Mapping genetic loci that determine leukocyte telomere length in a large sample of unselected female sibling pairs. Am J Hum Genet. 2006;78(3):480–6.
61. Gardner M, Bann D, Wiley L, et al. Gender and telomere length: systematic review and meta-analysis. Exp Gerontol. 2014;51:15–27.
62. Kimura M, Cherkas LF, Kato BS, et al. Offspring's leukocyte telomere length, paternal age, and telomere elongation in sperm. PLoS Genet. 2008;4(2):e37.
63. Okuda K, Bardeguez A, Gardner JP, et al. Telomere length in the newborn. Pediatr Res. 2002;52(3):377–81.
64. Kimura M, Gazitt Y, Cao X, et al. Synchrony of telomere length among hematopoietic cells. Exp Hematol. 2010;38(10):854–9.
65. Youngren K, Jeanclos E, Aviv H, et al. Synchrony in telomere length of the human fetus. Hum Genet. 1998;102(6):640–3.
66. Heidinger BJ, Blount JD, Boner W, et al. Telomere length in early life predicts lifespan. Proc Natl Acad Sci U S A. 2012;109(5):1743–8.
67. Aubert G, Baerlocher GM, Vulto I, et al. Collapse of telomere homeostasis in hematopoietic cells caused by heterozygous mutations in telomerase genes. PLoS Genet. 2012;8(5):e1002696.
68. Frenck Jr RW, Blackburn EH, Shannon KM. The rate of telomere sequence loss in human leukocytes varies with age. Proc Natl Acad Sci U S A. 1998;95(10):5607–10.
69. Mitchell C, Hobcraft J, McLanahan SS, et al. Social disadvantage, genetic sensitivity, and children's telomere length. Proc Natl Acad Sci U S A. 2014;111(16):5944–9.
70. von Zglinicki T. Oxidative stress shortens telomeres. Trends Biochem Sci. 2002;27(7):339–44.
71. Sahin E, DePinho RA. Axis of ageing: telomeres, p53 and mitochondria. Nat Rev Mol Cell Biol. 2012;13(6):397–404.
72. Liu P, Demple B. DNA repair in mammalian mitochondria: much more than we thought? Environ Mol Mutagen. 2010;51(5):417–26.
73. Singh KK. Mitochondria damage checkpoint, aging, and cancer. Ann N Y Acad Sci. 2006;1067:182–90.
74. Kim HS, Patel K, Muldoon-Jacobs K, et al. SIRT3 is a mitochondria-localized tumor suppressor required for maintenance of mitochondrial integrity and metabolism during stress. Cancer Cell. 2010;17(1):41–52.
75. Park SH, Ozden O, Jiang H, et al. Sirt3, mitochondrial ROS, ageing, and carcinogenesis. Int J Mol Sci. 2011;12(9):6226–39.
76. Hochhauser D. Relevance of mitochondrial DNA in cancer. Lancet. 2000;356(9225):181–2.
77. Kuo JH, Chu YL, Yang JS, et al. Cantharidin induces apoptosis in human bladder cancer TSGH 8301 cells through mitochondria-dependent signal pathways. Int J Oncol. 2010;37(5):1243–50.
78. Cree LM, Patel SK, Pyle A, et al. Age-related decline in mitochondrial DNA copy number in isolated human pancreatic islets. Diabetologia. 2008;51(8):1440–3.
79. Gianotti TF, Sookoian S, Dieuzeide G, et al. A decreased mitochondrial DNA content is related to insulin resistance in adolescents. Obesity (Silver Spring). 2008;16(7):1591–5.
80. Ballinger SW, Patterson C, Knight-Lozano CA, et al. Mitochondrial integrity and function in atherogenesis. Circulation. 2002;106(5):544–9.
81. Roy Chowdhury SK, Sangle GV, Xie X, et al. Effects of extensively oxidized low-density lipoprotein on mitochondrial function and reactive oxygen species in porcine aortic endothelial cells. Am J Physiol Endocrinol Metab. 2010;298(1):E89–98.
82. Harrison CM, Pompilius M, Pinkerton KE, et al. Mitochondrial oxidative stress significantly influences atherogenic risk and cytokine-induced oxidant production. Environ Health Perspect. 2011;119(5):676–81.
83. Knight-Lozano CA, Young CG, Burow DL, et al. Cigarette smoke exposure and hypercholesterolemia increase mitochondrial damage in cardiovascular tissues. Circulation. 2002;105(7):849–54.
84. Hou L, Zhu ZZ, Zhang X, et al. Airborne particulate matter and mitochondrial damage: a cross-sectional study. Environ Health. 2010;9:48.
85. Halvorsen CP, Andolf E, Hu J, et al. Discordant twin growth in utero and differences in blood pressure and endothelial function at 8 years of age. J Intern Med. 2006;259(2):155–63.
86. Leeson CP, Kattenhorn M, Morley R, et al. Impact of low birth weight and cardiovascular risk factors on endothelial function in early adult life. Circulation. 2001;103(9):1264–8.
87. Aubert G, Hills M, Lansdorp PM. Telomere length measurement-caveats and a critical assessment of the available technologies and tools. Mutat Res. 2012;730(1-2):59–67.
88. Montpetit AJ, Alhareeri AA, Montpetit M, et al. Telomere length: a review of methods for measurement. Nurs Res. 2014;63(4):289–99.
89. Vera E, Blasco MA. Beyond average: potential for measurement of short telomeres. Aging (Albany NY). 2012;4(6):379–92.
90. Kimura M, Stone RC, Hunt SC, et al. Measurement of telomere length by the Southern blot analysis of terminal restriction fragment lengths. Nat Protoc. 2010;5(9):1596–607.
91. Cawthon RM. Telomere measurement by quantitative PCR. Nucleic Acids Res. 2002;30(10):e47.
92. Cawthon RM. Telomere length measurement by a novel monochrome multiplex quantitative PCR method. Nucleic Acids Res. 2009;37(3):e21.
93. Aviv A, Hunt SC, Lin J, et al. Impartial comparative analysis of measurement of leukocyte telomere length/DNA content by Southern blots and qPCR. Nucleic Acids Res. 2011;39(20):e134.
94. Elbers CC, Garcia ME, Kimura M, et al. Comparison between southern blots and qPCR analysis of leukocyte telomere length in the health ABC study. J Gerontol A Biol Sci Med Sci. 2014;69(5):527–31.
95. Baird DM, Rowson J, Wynford-Thomas D, et al. Extensive allelic variation and ultrashort telomeres in senescent human cells. Nat Genet. 2003;33(2):203–7.
96. Canela A, Vera E, Klatt P, et al. High-throughput telomere length quantification by FISH and its application to human population studies. Proc Natl Acad Sci U S A. 2007;104(13):5300–5.
97. Rufer N, Dragowska W, Thornbury G, et al. Telomere length dynamics in human lymphocyte subpopulations measured by flow cytometry. Nat Biotechnol. 1998;16(8):743–7.
98. Miller FJ, Rosenfeldt FL, Zhang C, et al. Precise determination of mitochondrial DNA copy number in human skeletal and cardiac muscle by a PCR-based assay: lack of change of copy number with age. Nucleic Acids Res. 2003;31(11):e61.
99. Hou L, Zhang X, Dioni L, et al. Inhalable particulate matter and mitochondrial DNA copy number in highly exposed individuals in Beijing, China: a repeated-measure study. Part Fibre Toxicol. 2013;10:17.
100. Janssen BG, Munters E, Pieters N, et al. Placental mitochondrial DNA content and particulate air pollution during in utero life. Environ Health Perspect. 2012;120(9):1346–52.
101. Perry VH, Cunningham C, Holmes C. Systemic infections and inflammation affect chronic neurodegeneration. Nat Rev Immunol. 2007;7(2):161–7.
102. Deeks SG. HIV infection, inflammation, immunosenescence, and aging. Annu Rev Med. 2011;62:141–55.
103. Risom L, Moller P, Loft S. Oxidative stress-induced DNA damage by particulate air pollution. Mutat Res. 2005;592(1-2):119–37.
104. Ghio AJ, Carraway MS, Madden MC. Composition of air pollution particles and oxidative stress in cells, tissues, and living systems. J Toxicol Environ Health B Crit Rev. 2012;15(1):1–21.
105. Soberanes S, Urich D, Baker CM, et al. Mitochondrial complex III-generated oxidants activate ASK1 and JNK to induce alveolar epithelial cell death following exposure to particulate matter air pollution. J Biol Chem. 2009;284(4):2176–86.
106. von Zglinicki T, Saretzki G, Docke W, et al. Mild hyperoxia shortens telomeres and inhibits proliferation of fibroblasts: a model for senescence? Exp Cell Res. 1995;220(1):186–93.
107. Petersen S, Saretzki G, von Zglinicki T. Preferential accumulation of single-stranded regions in telomeres of human fibroblasts. Exp Cell Res. 1998;239(1):152–60.
108. Kawanishi S, Oikawa S. Mechanism of telomere shortening by oxidative stress. Ann N Y Acad Sci. 2004;1019:278–84.
109. von Zglinicki T, Pilger R, Sitte N. Accumulation of single-strand breaks is the major cause of telomere shortening in human fibroblasts. Free Radic Biol Med. 2000;28(1):64–74.
110. Sahin E, Colla S, Liesa M, et al. Telomere dysfunction induces metabolic and mitochondrial compromise. Nature. 2011;470(7334):359–65. These authors made a substantial contribution in unravelling the link between telomeres, mitochondria and aging.
111. Yamamoto H, Schoonjans K, Auwerx J. Sirtuin functions in health and disease. Mol Endocrinol. 2007;21(8):1745–55.
112. Lagouge M, Argmann C, Gerhart-Hines Z, et al. Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha. Cell. 2006;127(6):1109–22.
113. Nemoto S, Fergusson MM, Finkel T. SIRT1 functionally interacts with the metabolic regulator and transcriptional coactivator PGC-1{alpha}. J Biol Chem. 2005;280(16):16456–60.
114. Narala SR, Allsopp RC, Wells TB, et al. SIRT1 acts as a nutrient-sensitive growth suppressor and its loss is associated with increased AMPK and telomerase activity. Mol Biol Cell. 2008;19(3):1210–9.
115. Vaziri H, Dessain SK, Ng Eaton E, et al. hSIR2(SIRT1) functions as an NAD-dependent p53 deacetylase. Cell. 2001;107(2):149–59.
116. Aquilano K, Vigilanza P, Baldelli S, et al. Peroxisome proliferator-activated receptor gamma co-activator 1alpha (PGC-1alpha) and sirtuin 1 (SIRT1) reside in mitochondria: possible direct function in mitochondrial biogenesis. J Biol Chem. 2010;285(28):21590–9.
117. Donmez G, Guarente L. Aging and disease: connections to sirtuins. Aging Cell. 2010;9(2):285–90.
118. Sahin E, Depinho RA. Linking functional decline of telomeres, mitochondria and stem cells during ageing. Nature. 2010;464(7288):520–8.
119. Pieters N, Janssen BG, Dewitte H, et al. Biomolecular markers within the core axis of aging and particulate air pollution exposure in the elderly: a cross-sectional study. Environ Health Perspect. 2015. This study integrates different aging related molecular markers in elderly in association with long-term air pollution exposure.
120. Wong JY, De Vivo I, Lin X, et al. Cumulative PM(2.5) exposure and telomere length in workers exposed to welding fumes. J Toxicol Environ Health A. 2014;77(8):441–55.
121. Hou L, Wang S, Dou C, et al. Air pollution exposure and telomere length in highly exposed subjects in Beijing, China: a repeated-measure study. Environ Int. 2012;48:71–7.
122. Dioni L, Hoxha M, Nordio F, et al. Effects of short-term exposure to inhalable particulate matter on telomere length, telomerase expression, and telomerase methylation in steel workers. Environ Health Perspect. 2011;119(5):622–7.
123. Hoxha M, Dioni L, Bonzini M, et al. Association between leukocyte telomere shortening and exposure to traffic pollution: a cross-sectional study on traffic officers and indoor office workers. Environ Health. 2009;8:41.
124. Xia Y, Chen R, Wang C, et al. Ambient air pollution, blood mitochondrial DNA copy number and telomere length in a panel of diabetes patients. Inhal Toxicol. 2015;27(10):481–7.
125. Shan M, Yang X, Ezzati M, et al. A feasibility study of the association of exposure to biomass smoke with vascular function, inflammation, and cellular aging. Environ Res. 2014;135:165–72.
126. McCracken J, Baccarelli A, Hoxha M, et al. Annual ambient black carbon associated with shorter telomeres in elderly men: Veterans Affairs Normative Aging Study. Environ Health Perspect. 2010;118(11):1564–70. First study on telomere attrition and long-term air pollution exposure in elderly.
127. Weng NP, Granger L, Hodes RJ. Telomere lengthening and telomerase activation during human B cell differentiation. Proc Natl Acad Sci U S A. 1997;94(20):10827–32.
128. Bijnens E, Zeegers MP, Gielen M, et al. Lower placental telomere length may be attributed to maternal residential traffic exposure; a twin study. Environ Int. 2015;79:1–7. This study provides evidence that maternal traffic exposure is linked with telomere length in early life.
129. Zhong J, Cayir A, Trevisi L, et al. Traffic-related air pollution, blood pressure, and adaptive response of mitochondrial abundance. Circulation. 2016;133(4):378–87.
130. Rappaport SM, Smith MT. Epidemiology. Environment and disease risks. Science. 2010;330(6003):460–1.
131. Wild CP. The exposome: from concept to utility. Int J Epidemiol. 2012;41(1):24–32.
132. Epel ES, Blackburn EH, Lin J, et al. Accelerated telomere shortening in response to life stress. Proc Natl Acad Sci U S A. 2004;101(49):17312–5.
133. Crous-Bou M, Fung TT, Prescott J, et al. Mediterranean diet and telomere length in nurses' health study: population based cohort study. BMJ. 2014;349:g6674.
134. Steptoe A, Hamer M, Butcher L, et al. Educational attainment but not measures of current socioeconomic circumstances are associated with leukocyte telomere length in healthy older men and women. Brain Behav Immun. 2011;25(7):1292–8.
135. Adler N, Pantell MS, O'Donovan A, et al. Educational attainment and late life telomere length in the health, aging and body composition study. Brain Behav Immun. 2013;27(1):15–21.
136. Muezzinler A, Zaineddin AK, Brenner H. Body mass index and leukocyte telomere length in adults: a systematic review and meta-analysis. Obes Rev. 2014;15(3):192–201.
137. Liang G, Schernhammer E, Qi L, et al. Associations between rotating night shifts, sleep duration, and telomere length in women. PLoS One. 2011;6(8):e23462.
138. Surtees PG, Wainwright NW, Pooley KA, et al. Life stress, emotional health, and mean telomere length in the European Prospective Investigation into cancer (EPIC)-Norfolk population study. J Gerontol A Biol Sci Med Sci. 2011;66(11):1152–62.
139. Entringer S, Epel ES, Lin J, et al. Maternal psychosocial stress during pregnancy is associated with newborn leukocyte telomere length. Am J Obstet Gynecol. 2013;208(2):134 e1–7.
140. Marchetto NM, Glynn RA, Ferry ML, et al. Prenatal stress and newborn telomere length. Am J Obstet Gynecol. 2016.
141. Salihu HM, Pradhan A, King L, et al. Impact of intrauterine tobacco exposure on fetal telomere length. Am J Obstet Gynecol. 2015;212(2):205 e1–8.
142. Lin S, Huo X, Zhang Q, et al. Short placental telomere was associated with cadmium pollution in an electronic waste recycling town in China. PLoS One. 2013;8(4):e60815.