Environmental epigenetics and asthma: Current concepts and call for studies

American Journal of Respiratory and Critical Care Medicine

Volumn 177, Issue 6, 2008, Pages 567-573

  Miller, Rachel L ^a   Ho, Shuk Mei ^b  

^a Columbia University College of Physicians and Surgeons ^*  (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

Asthma; DNA methylation; Epigenetics; Gene environment interactions

Indexed keywords

BETA 2 ADRENERGIC RECEPTOR; CD14 ANTIGEN; GLUTATHIONE TRANSFERASE M1; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 13; INTERLEUKIN 4; INTERLEUKIN 4 RECEPTOR ALPHA; TOLL LIKE RECEPTOR 2; TUMOR NECROSIS FACTOR; MICRORNA;

ASTHMA; CELL DIFFERENTIATION; DISEASE COURSE; DISEASE PREDISPOSITION; DISEASE TRANSMISSION; DNA METHYLATION; ENVIRONMENTAL EXPOSURE; EPIGENETICS; GENE CONTROL; GENE INTERACTION; HELPER CELL; HUMAN; PHENOTYPE; POLARIZATION; PRENATAL EXPOSURE; PRIORITY JOURNAL; REVIEW; RISK FACTOR; AIR POLLUTANT; FEMALE; GENETIC EPIGENESIS; GENETIC PREDISPOSITION; GENETICS; IMMUNOLOGY; PREGNANCY;

AIR POLLUTANTS; ASTHMA; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; GENETIC PREDISPOSITION TO DISEASE; HUMANS; MICRORNAS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS;

EID: 40949124369     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.200710-1511PP     Document Type: Review

References (91)

1. Los H, Postmus PE, Boomsma DI. Asthma genetics and intermediate phenotypes: a review from twin studies. Twin Res 2001;4:81-93.
2. Venn AJ, Lewis SA, Cooper M, Hubbard R, Britton J. Living near a main road and the risk of wheezing illness in children. Am J Respir Crit Care Med 2001;164:2177-2180.
3. Hoppin JA, Umbach DM, London SJ, Alavanja MCR, Sandler DP. Diesel exhaust, solvents, and other occupational exposures as risk factors for wheeze among farmers. Am J Respir Crit Care Med 2004;169:1308-1313.
4. Lau C, Rogers JM. Embryonic and fetal programming of physiological disorders in adulthood. Birth Defects Research C Embryo Today 2004;72:300-312.
5. Hales C, Barker D. The thrifty phenotype hypothesis. Br Med Bull 2001;60:5-20.
6. Hales C, Barker D, Clark P, Cox L, Fall C, Osmond C, Winter P. Fetal and infant growth and impaired glucose tolerance at age 64. BMJ 1991;303:1019-1022.
7. McKeever T, Lewis SA, Smith C, Hubbard R. The importance of prenatal exposures on the development of allergic disease: a birth cohort study using the West Midlands General Practice Database. Am J Respir Crit Care Med 2002;166:827-832.
8. Mone S, Gillman MW, Miller TL, Herman EH, Lipshultz SE. Effects of environmental exposures on the cardiovascular system: prenatal period through adolescence. Pediatrics 2004;113:1058-1069.
9. Dolinoy D, Weidman J, Jirtle R. Epigenetic gene regulation: linking early developmental environment to adult disease. Reprod Toxicol 2007;23:297-307.
10. Nightingale KP, O'Neill LP, Turner BM. Histone modifications: signalling receptors and potential elements of a heritable epigenetic code. Curr Opin Genet Dev 2006;16:125-136.
11. Krebs JE. Moving marks: dynamic histone modifications in yeast. Mol Biosyst 2007;3:590-597.
12. Callinan PA, Feinberg AP. The emerging science of epigenomics. Hum Mol Genet 2006;15:R95-R101.
13. Sarraf SA, Stancheva I. Methyl-CpG binding protein MBD1 couples histone H3 methylation at lysine 9 by SETDB1 to DNA replication and chromatin assembly. Mol Cell 2004;15:595-605.
14. Cooney CA, Dave AA, Wolff GL. Maternal methyl supplements in mice affect epigenetic variation and DNA methylation of offspring. J Nutr 2002;132:2393S-2400S.
15. Waterland RA, Jirtle RL. Transposable elements: targets for early nutritional effects on epigenetic gene regulation. Mol Cell Biol 2003;23:5293-5300.
16. Feinberg A, Tycko B. The history of cancer epigenetics. Nat Rev Cancer 2004;4:143-153.
17. Falls JG, Pulford DJ, Wylie AA, Jirtle RL. Genomic imprinting: implications for human disease. Am J Pathol 1999;154:635-647.
18. Tang W, Ho SM. Epigenetic reprogramming and imprinting in origins of disease. Rev Endocr Metab Disord 2007;8:173-182.
19. Gilliland FD, Berhane K, Li Y-F, Rappaport EB, Peters JM. Effects of early onset asthma and in utero exposure to maternal smoking on childhood lung function. Am J Respir Crit Care Med 2003;167:917-924.
20. Kurukulaaratchy RJ, Matthews S, Arshad SH. Does environment mediate earlier onset of the persistent childhood asthma phenotype? Pediatrics 2004;113:345-350.
21. Mandhane PJ, Greene JM, Cowan JO, Taylor DR, Sears MR. Sex differences in factors associated with childhood- and adolescent-onset wheeze. Am J Respir Crit Care Med 2005;172:45-54.
22. Weaver I, Meaney M, Szyf M. Maternal care effects on the hippocampal transcriptome and anxiety-mediated behaviors in the offspring that are reversible in adulthood. Proc Natl Acad Sci USA 2006;103:3480-3485.
23. Marco RD, Locatelli F, Cerveri I, Bugiani M, Marinoni A, Giammanco G. Incidence and remission of asthma: a retrospective study on the natural history of asthma in Italy. J Allergy Clin Immunol 2002;110:228-235.
24. Magnusson L, Olesen A, Wennborg H, Olsen J. Wheezing, asthma, hayfever, and atopic eczema in childhood following exposure to tobacco smoke in fetal life. Clin Exp Allergy 2005;35:1550-1556.
25. Alati R, Al-Mamun A, O'Callaghan M, Najman JM, Williams GM. In utero and postnatal maternal smoking and asthma in adolescence. Epidemiology 2006;17:138-144.
26. Elliot JG, Carroll NG, James AL, Robinson PJ. Airway alveolar attachment points and exposure to cigarette smoke in utero. Am J Respir Crit Care Med 2003;167:45-49.
27. Devereux G, Turner SW, Craig LC, McNeill G, Martindale S, Harbour PJ, Helms PJ, Seaton A. Low maternal vitamin E intake during pregnancy is associated with asthma in 5-year-old children. Am J Respir Crit Care Med 2006;174:499-507.
28. Jedrychowski W, Galas A, Whyatt R, Perera F. The prenatal use of antibiotics and the development of allergic disease in one year old infants: a preliminary study. Int J Occup Med Environ Health 2006;19:70-76.
29. Kukkonen K, Savilahti E, Haahtela T, Juntunen-Backman K, Korpela R, Poussa T, Tuure T, Kuitunen M. Probiotics and prebiotic galactooligosaccharides in the prevention of allergic diseases: a randomized, double-blind, placebo-controlled trial. J Allergy Clin Immunol 2007;119:192-198.
30. Fitzsimon N, Fallon U, O'Mahony D, Loftus BG, Bury G, Murphy AW, Kelleher CC. Mothers' dietary patterns during pregnancy and risk of asthma symptoms in children at 3 years. Ir Med J 2007;100(Suppl):27-32.
31. Miller RL, Garfinkel R, Horton M, Camann D, Perera F, Whyatt RM, Kinney PL. Polycyclic aromatic hydrocarbons, environmental tobacco smoke, and respiratory symptoms in an inner-city birth cohort. Chest 2004;126:1071-1078.
32. Hamada K, Suzaki Y, Leme A, Ito T, Miyamoto K, Kobzik L, Kimura H. Exposure of pregnant mice to an air pollutant aerosol increases asthma susceptibility in offspring. J Toxicol Environ Health 2007;70:688-695.
33. Blumer N, Herz U, Wegmann M, Renz H. Prenatal lipopolysaccharide-exposure prevents allergic sensitization and airway inflammation, but not airway responsiveness in a murine model of experimental asthma. Clin Exp Allergy 2005;35:397-402.
34. Blumer N, Sel S, Virna S, Patrascan C, Zimmermann S, Herz U, Renz H, Garn H. Perinatal maternal application of Lactobacillus rhamnosus GG suppresses allergic airway inflammation in mouse offspring. Clin Exp Allergy 2007;37:348-357.
35. Fedulov AV, Leme A, Yang Z, Dahl M, Lim R, Mariani TJ, Kobzik L. Pulmonary exposure to particles during pregnancy causes increased neonatal asthma susceptibility. Am J Respir Cell Mol Biol 2008;38:57-67.
36. Traherne JA, Hill MR, Hysi P, D'Amato M, Broxholme J, Mott R, Moffatt MF, Cookson WO. LD mapping of maternally and nonmaternally derived alleles and atopy in Fc epsilon RI-beta. Hum Mol Genet 2003;12:2577-2585.
37. Nicolae D, Cox NJ, Lester LA, Schneider D, Tan Z, Billstrand C, Kuldanek S, Donfack J, Kogut P, Patel NM, et al. Fine mapping and positional candidate studies identify HLA-G as an asthma susceptibility gene on chromosome 6p21. Am J Hum Genet 2005;763:349-357.
38. Carroll WD, Lenney W, Child F, Strange RC, Jones PW, Fryer AA. Maternal glutathione s-transferase gstp1 genotype is a specific predictor of phenotype in children with asthma. Pediatr Allergy Immunol 2005;16:32-39.
39. Litonjua A, Carey VJ, Burge HA, Weiss ST, Gold DR. Parental history and the risk for childhood asthma: does mother confer more risk than father? Am J Respir Crit Care Med 1998;158:176-181.
40. Liu CA, Wang CL, Chuang H, Ou CY, Hsu TY, Land KD. Prenatal prediction of infant atopy by maternal but not paternal total IgE levels. J Allergy Clin Immunol 2003;112:899-904.
41. Li Y-F, Langholz B, Salam MT, Gilliland FD. Maternal and grand-maternal smoking patterns are associated with early childhood asthma. Chest 2005;127:1232-1241.
42. Sporik R, Holgate ST, Platts-Mills TA, Cogswell JJ. Exposure to housedust mite allergen (Der p i) and the development of asthma in childhood: a prospective study. N Engl J Med 1990;323:502-507.
43. Remes ST, Castro-Rodriguez JA, Holberg CJ, Martinez FD, Wright AL. Dog exposure in infancy decreases the subsequent risk of frequent wheeze but not of atopy. J Allergy Clin Immunol 2001;108:509-515.
44. Lau S, Illi S, Platts-Mills TA, Riposo D, Nickel R, Grüber C, Niggemann B, Wahn U. Longitudinal study on the relationship between cat allergen and endotoxin exposure, sensitization, cat-specific IgG and development of asthma in childhood-report of the German Multicentre Allergy Study (MAS 90). Allergy 2005;60:766-773.
45. Ponsonby AL, Dwyer T, Kemp A, Couper D, Cochrane J, Carmichael A. Aprospective study of the association between home gas appliance use during infancy and subsequent dust mite sensitization and lung function in childhood. Clin Exp Allergy 2001;31:1544-1552.
46. Perera F, Rauh V, Tsai W-Y, Kinney P, Camann D, Barr D, Bernert T, Garfinkel R, Tu Y-h, Diaz D, et al. Effects of transplacental exposure to environmental pollutants on birth outcomes in a multiethnic population. Environ Health Perspect 2003;111:201-206.
47. Windham GC, Hopkins B, Fenster L, Swan SH. Prenatal active or passive tobacco smoke exposure and the risk of preterm delivery or low birth weight. Epidemiology 2000;11:427-433.
48. Anand D, Stevenson CJ, West CR, Pharoah PO. Lung function and respiratory health in adolescents of very low birth weight. Arch Dis Child 2003;88:135-138.
49. Barker DJP, Godfrey KM, Fall C, Osmond C, Winter PD, Shaheen SO. Relation of birth weight and childhood respiratory infection to adult lung function and death from chronic obstructive airways disease. BMJ 1991;303:671-675.
50. Shaheen SO, Barker DJ, Shiell AW, Crocker FJ, Wield GA, Holgat ST. The relationship between pneumonia in early childhood and impaired lung function in late adult life. Am J Respir Crit Care Med 1994;149:616-619.
51. Jiang Y-h, Bressler J, Beaudet AL. Epigenetics and human disease. Annu Rev Genomics Hum Genet 2004;5:479-510.
52. Finch CE, Crimmins EM. Inflammatory exposure and historical changes in human life-spans. Science 2004;305:1736-1739.
53. Rahman I. Oxidative stress, chromatin remodeling and gene transcription in inflammation and chronic lung diseases. J Biochem Mol Biol 2003;36:95-109.
54. Ito K, Caramori G, Lim S, Oates T, Chung K, Barnes P, Adcock I. Expression and activity of histone deacetylases in human asthmatic airway. Am J Respir Crit Care Med 2002;166:392-396.
55. Perzanowski MS, Miller RL, Thorne PS, Barr RG, Divjan A, Sheares BJ, Garfinkel RS, Perera FP, Goldstein IF, Chew GL. Endotoxin in inner-city homes and the association with atopy and wheeze in the first two years of life. J Allergy Clin Immunol 2006;117:1082-1089.
56. Braun-Fahrlander C, Riedler J, Herz U, Eder W, Waser M, Grize L, Maisch S, Carr D, Gerlach F, Bufe A, et al. Environmental exposure to endotoxin and its relation to asthma in school-age children. N Engl J Med 2002;347:869-877.
57. Chan C, Li L, McCall CE, Yoza BK. Endotoxin tolerance disrupts chromatin remodeling and NF-kappaB transactivation at the IL-1beta promoter. J Immunol 2005;175:461-468.
58. Lee DU, Agarwal S, Rao A. Th2 lineage commitment and efficient IL-4 production involves extended demethylation of the IL-4 gene. Immunity 2002;16:649-660.
59. Agarwal S, Rao A.Modulation of chromatin structure regulates cytokine gene expression during T cell differentiation. Immunity 1998;9:765-775.
60. Tykocinski LO, Hajkova P, Chang HD, Stamm T, Sozeri O, Lohning M, Hu-Li J, Niesner U, Kreher S, Friedrich B, et al. A critical control element for interleukin-4 memory expression in t helper lymphocytes. J Biol Chem 2005;280:28177-28185.
61. Jones B, Chen J. Inhibition of IFN-g transcription by site-specific methylation during T helper cell development. EMBO J 2006;25:2443-2452.
62. White GP, Watt PM, Holt BJ, Holt PG. Differential patterns of methylation of the IFN-g promoter at CPG and non-CPG sites underlie differences in IFN-g gene expression between human neonatal and adult CD45ro- T cells. J Immunol 2002;168:2820-2827.
63. Young H, Ghosh P, Ye J, Lederer J, Lichtman A, Gerard J, Penix L, Wilson C, Melvin A, McGurn M, et al. Differentiation of the T helper phenotypes by analysis of the methylation state of the IFN-gamma gene. J Immunol 1994;153:3603-3610.
64. Liu J, Ballaney M, Al-Alem U, Quan C, Jin X, Perera F, Chen LC, Miller RL. Combined inhaled diesel exhaust particles and allergen exposure alter methylation of T helper genes and IgE production in vivo. Toxicol Sci 2008;102:76-81.
65. Digel W, Lübbert M. DNA methylation disturbances as novel therapeutic target in lung cancer: preclinical and clinical results. Crit Rev Oncol Hematol 2005;55:1-11.
66. Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene LIN-4 encodes small RNAs with antisense complementarity to LIN-14. Cell 1993;75:843-854.
67. Krek A, Grün D, Poy MN, Wolf R, Rosenberg L, Epstein EJ, MacMenamin P, Piedade ID, Gunsalus KC, Stoffel M, et al. Combinatorial microRNA target predictions. Nat Genet 2005;37:495-500.
68. Yanaihara N, Caplen N, Bowman E, Seike M, Kumamoto K, Yi M, Stephens RM, Okamoto A, Yokota J, Tanaka T, et al. Unique microRNA molecular profiles in lung cancer diagnosis and prognosis. Cancer Cell 2006;9:189-198.
69. Hunt JS, Petroff MG, McIntire RH, Ober C. HLA-G and immune tolerance in pregnancy. FASEB J 2005;19:681-693.
70. Tan Z, Randall G, Fan J, Camoretti-Mercado B, Brockman-Schneider R, Pan L, Solway J, Gern JE, Lemanske RF, Nicolae D, et al. Allele-specific targeting of microRNAs to HLA-G and risk of asthma. Am J Hum Genet 2007;81:829-834.
71. Ho S-m, Tang W-y. Techniques used in studies of epigenome dysregulation due to aberrant DNA methylation: an emphasis on fetal-based adult diseases. Reprod Toxicol 2007;23:267-282.
72. Dizier M, Bouzigon E, Guilloud-Bataille M, Siroux V, Lemainque A, Boland A, Lathrop M, Demenais F. Evidence for gene X smoking exposure interactions in a genome-wide linkage screen of asthma and bronchial hyperresponsiveness in EGEA families. Eur J Hum Genet 2007;15:810-815.
73. Colilla S, Nicolae D, Pluzhnikov A, Blumenthal M, Beaty T, Bleecker E, Lange E, Rich S, Meyers D, Ober C, et al. Evidence for gene-environment interactions in a linkage study of asthma and smoking exposure. J Allergy Clin Immunol 2003;111:840-846.
74. Choudhry SP, Avila PC, Nazario S, Ung J, Kho J, Rodriguez-Santana R, Csal J, Tsai HJ, Torres A, Ziv E, et al. CD14 tobacco gene-environment interaction modifies asthma severity and immunoglobulin E levels in Latinos with asthma. Am J Respir Crit Care Med 2005;172:173-182.
75. 2-adrenergic receptor gene polymorphism and cigarette smoking. Am J Respir Crit Care Med 2001;163:1404-1449.
76. Meyers D, Postma D, Stine O, Koppelman G, Ampleford E, Jongepier H, Howard T, Bleecker E. Genome screen for asthma and bronchial hyperresponsiveness: interactions with passive smoke exposure. J Allergy Clin Immunol 2005;115:1169-1175.
77. Ramadas R, Sadeghnejad A, Karmaus W, Arshad S, Matthews S, Huebner M, Kim D, Ewart S. Interleukin-1R antagonist gene and pre-natal smoke exposure are associated with childhood asthma. Eur Respir J 2007;29:502-508.
78. Gilliland FD, Li Y-F, Dubeau L, Berhane K, Avol E, McConnell R, Gauderman WJ, Peters JM. Effects of glutathione S-transferase M1, maternal smoking during pregnancy, and environmental tobacco smoke on asthma and wheezing in children. Am J Respir Crit Care Med 2002;166:457-463.
79. Li YF, Gauderman WJ, Avol E, Dubeau L, Gilliland FD. Associations of tumor necrosis factor g-308a with childhood asthma and wheezing. Am J Respir Crit Care Med 2006;173:970-976.
80. Blumenthal M, Langefeld C, Barnes K, Ober C, Meyers D, King R, Beaty T, Beck S, Bleecker E, Rich S. A genome-wide search for quantitative trait loci contributing to variation in seasonal pollen reactivity. J Allergy Clin Immunol 2006;117:79-85.
81. Leynaert B, Guilloud-Bataille M, Soussan D, Benessiano J, Guenegou A, Pin I, Neukirch F. Association between farm exposure and atopy, according to the CD14 C-159t polymorphism. J Allergy Clin Immunol 2006;118:658-665.
82. Eder W, Klimecki W, Yu L, von Mutius E, Riedler J, Braun-Fahrlander C, Nowak D, Martinez FD. Opposite effects of CD 14/-260 on serum IgE levels in children raised in different environments. J Allergy Clin Immunol 2005;116:601-607.
83. LeVan T, Essen SV, Romberger D, Lambert G, Martinez F, Vasquez M, Merchant J. Polymorphisms in the CD14 gene associated with pulmonary function in farmers. Am J Respir Crit Care Med 2005;171:773-779.
84. Eder W, Klimecki W, Yu L, Mutius Ev, Riedler J, Braun-Fahrlander C, Nowak D, Martinez FD. Toll-like receptor 2 as a major gene for asthma in children of European farmers. J Allergy Clin Immunol 2004;113:482-488.
85. Ege MJ, Bieli C, Frei R, Strien RTv, Riedler J, Ublagger E, Schram-Bijkerk D, Brunekreef B, Hage Mv, Scheynius A, et al. Prenatal farm exposure is related to the expression of receptors of the innate immunity and to atopic sensitization in school-age children. J Allergy Clin Immunol 2006;117:817-823.
86. Simpson A, John S, Jury F, Niven R, Woodcock A, Ollier WE, Custovic A. Endotoxin exposure, CD14, and allergic disease: an interaction between genes and the environment. Am J Respir Crit Care Med 2006;174:386-392.
87. Zambelli-Weiner A, Ehrlich E, Stockton ML, Grant AV, Zhang S, Levett PN, Beaty TH, Barnes KC. Evaluation of the CD14/-260 polymorphism and house dust endotoxin exposure in the Barbados Asthma Genetics Study. J Allergy Clin Immunol 2005;115:1203-1209.
88. Williams L, McPhee R, Ownby D, Peterson E, James M, Zoratti E, Johnson C. Gene-environment interactions with CD14 c-260t and their relationship to total serum IgE levels in adults. J Allergy Clin Immunol 2006;118:851-857.
89. Barr RG, Cooper DM, Speizer FE, Drazen JM, Camargo CA. Beta(2)-adrenoceptor polymorphism and body mass index are associated with adult-onset asthma in sedentary but not active women. Chest 2001;120:1474-1479.
90. Bernstein D, Wang N, Campo P, Chakraborty R, Smith A, Cartier A, Boulet L, Malo J, Yucesoy B, Luster M, et al. Diisocyanate asthma and gene-environment interactions with IL4ra, CD-14, and IL-13 genes. Ann Allergy Asthma Immunol 2006;97:800-806.
91. Pessi T, Virta M, Adjers K, Karjalainen J, Rautelin H, Kosunen TU, Hurme M. Genetic and environmental factors in the immunopathogenesis of atopy: interaction of Helicobacter pylori infection and IL4 genetics. Int Arch Allergy Immunol 2005;137:282-288.