Epigenetics and the maintenance of developmental plasticity: extending the signalling theory framework
dc.contributor.author | Laubach, Zachary M. | |
dc.contributor.author | Perng, Wei | |
dc.contributor.author | Dolinoy, Dana C. | |
dc.contributor.author | Faulk, Christopher D. | |
dc.contributor.author | Holekamp, Kay E. | |
dc.contributor.author | Getty, Thomas | |
dc.date.accessioned | 2018-08-13T18:48:05Z | |
dc.date.available | 2019-10-01T16:02:10Z | en |
dc.date.issued | 2018-08 | |
dc.identifier.citation | Laubach, Zachary M.; Perng, Wei; Dolinoy, Dana C.; Faulk, Christopher D.; Holekamp, Kay E.; Getty, Thomas (2018). "Epigenetics and the maintenance of developmental plasticity: extending the signalling theory framework." Biological Reviews 93(3): 1323-1338. | |
dc.identifier.issn | 1464-7931 | |
dc.identifier.issn | 1469-185X | |
dc.identifier.uri | https://hdl.handle.net/2027.42/145204 | |
dc.description.abstract | Developmental plasticity, a phenomenon of importance in both evolutionary biology and human studies of the developmental origins of health and disease (DOHaD), enables organisms to respond to their environment based on previous experience without changes to the underlying nucleotide sequence. Although such phenotypic responses should theoretically improve an organism’s fitness and performance in its future environment, this is not always the case. Herein, we first discuss epigenetics as an adaptive mechanism of developmental plasticity and use signaling theory to provide an evolutionary context for DOHaD phenomena within a generation. Next, we utilize signalling theory to identify determinants of adaptive developmental plasticity, detect sources of random variability – also known as process errors that affect maintenance of an epigenetic signal (DNA methylation) over time, and discuss implications of these errors for an organism’s health and fitness. Finally, we apply life‐course epidemiology conceptual models to inform study design and analytical strategies that are capable of parsing out the potential effects of process errors in the relationships among an organism’s early environment, DNA methylation, and phenotype in a future environment. Ultimately, we hope to foster cross‐talk and interdisciplinary collaboration between evolutionary biology and DOHaD epidemiology, which have historically remained separate despite a shared interest in developmental plasticity. | |
dc.publisher | Blackwell Publishing Ltd | |
dc.publisher | Wiley Periodicals, Inc. | |
dc.subject.other | predictive adaptive response (PAR) | |
dc.subject.other | thrifty phenotype | |
dc.subject.other | DNA methylation | |
dc.subject.other | signalling theory | |
dc.subject.other | developmental plasticity | |
dc.subject.other | epigenetics | |
dc.subject.other | developmental origins of health and disease (DOHaD) | |
dc.title | Epigenetics and the maintenance of developmental plasticity: extending the signalling theory framework | |
dc.type | Article | en_US |
dc.rights.robots | IndexNoFollow | |
dc.subject.hlbsecondlevel | Ecology and Evolutionary Biology | |
dc.subject.hlbtoplevel | Science | |
dc.description.peerreviewed | Peer Reviewed | |
dc.description.bitstreamurl | https://deepblue.lib.umich.edu/bitstream/2027.42/145204/1/brv12396_am.pdf | |
dc.description.bitstreamurl | https://deepblue.lib.umich.edu/bitstream/2027.42/145204/2/brv12396.pdf | |
dc.identifier.doi | 10.1111/brv.12396 | |
dc.identifier.source | Biological Reviews | |
dc.identifier.citedreference | Pike, R. K., McNamara, J. M. & Houston, A. I. ( 2016 ). A general expression for the reproductive value of information. Behavioral Ecology 27, 1296 – 1303. | |
dc.identifier.citedreference | Roseboom, T. J., van der Meulen, J. H. P., Ravelli, A. C., Osmond, C., Barker, D. J. P. & Bleker, O. P. ( 2001 ). Effects of prenatal expossure to the Dutch famine on adult disease in later life: an overview. Molecular and Cellular Endocrinology 185, 93 – 98. | |
dc.identifier.citedreference | Rothman, K. J., Greenland, S. & Lash, T. L. ( 2008 ). Clinical Epidemiology. In Modern Epidemiology, 3rd Edition, pp. 641 – 651. Lippincott Williams & Wilkins, Philadelphia. | |
dc.identifier.citedreference | Schneider, T. D. ( 2014 ). Information theory primer with an appendix on logarithms. National Cancer Institute 1 – 9. https://scneider.ncifcrf.gov/paper/primer/primer.pdf | |
dc.identifier.citedreference | Shannon, C. E. ( 1948 ). A mathematical theory of communication. The Bell System Technical Journal 27, 379 – 423, 656. | |
dc.identifier.citedreference | Shannon, C. E. ( 1949 ). Communication in the presence of noise. Proceedings of the Institute of Radio Engineers 37, 10 – 21. | |
dc.identifier.citedreference | Shapiro, J. A. ( 2017 ). Exploring the read‐write genome: mobile DNA and mammalian adaptation. Critical Reviews in Biochemistry and Molecular Biology 52, 1 – 17. | |
dc.identifier.citedreference | Shibata, D. ( 2009 ). Inferring human stem cell behaviour from epigenetic drift. Journal of Pathology 217, 199 – 205. | |
dc.identifier.citedreference | Siegfried, Z. & Simon, I. ( 2010 ). DNA methylation and gene expression. Wiley Interdisciplinary Reviews: Systems Biology and Medicine 2, 362 – 371. | |
dc.identifier.citedreference | Simmen, M. W. ( 2008 ). Genome‐scale relationships between cytosine methylation and dinucleotide abundances in animals. Genomics 92, 33 – 40. | |
dc.identifier.citedreference | Simpson, S. J., Despland, E., Hägele, B. F. & Dodgson, T. ( 2001 ). Gregarious behavior in desert locusts is evoked by touching their back legs. Proceedings of the National Academy of Sciences of the United States of America 98, 3895 – 3897. | |
dc.identifier.citedreference | Simpson, S. J., Sword, G. A. & Lo, N. ( 2011 ). Polyphenism in insects. Current Biology 21, R738 – R749. | |
dc.identifier.citedreference | Sinclair, K. D., Allegrucci, C., Singh, R., Gardner, D. S., Sebastian, S., Bispham, J., Thurston, A., Huntley, J. F., Rees, W. D., Maloney, C. A., Lea, R. G., Craigon, J., McEvoy, T. G. & Young, L. E. ( 2007 ). DNA methylation, insulin resistance, and blood pressure in offspring determined by maternal periconceptional B vitamin and methionine status. Proceedings of the National Academy of Sciences of the United States of America 104, 19351 – 19356. | |
dc.identifier.citedreference | Slotkin, R. K. & Martienssen, R. ( 2007 ). Transposable elements and the epigenetic regulation of the genome. Nature Reviews Genetics 8, 272 – 285. | |
dc.identifier.citedreference | Stamps, J. A. ( 2016 ). Individual differences in behavioural plasticities. Biological Reviews 91, 534 – 567. | |
dc.identifier.citedreference | Stamps, J. A. & Frankenhuis, W. E. ( 2016 ). Bayesian models of development. Trends in Ecology & Evolution 31, 260 – 268. | |
dc.identifier.citedreference | Stearns, S. C. ( 1989 ). The evolutionary significance of phenotypic plasticity. BioScience 39, 436 – 445. | |
dc.identifier.citedreference | Stockton, F.R. ( 1882 ). ‘The lady, or the tiger?’ The Century, pp. 83 – 86. | |
dc.identifier.citedreference | Tahiliani, M., Koh, K. P., Shen, Y., Pastor, W. A., Bandukwala, H., Brudno, Y., Agarwal, S., Iyer, L. M., Liu, D. R., Aravind, L. & Rao, A. ( 2009 ). Conversion of 5‐methylcytosine to 5‐hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324, 930 – 935. | |
dc.identifier.citedreference | Tobi, E. W., Lumey, L. H., Talens, R. P., Kremer, D., Putter, H., Stein, A. D., Slagboom, P. E. & Heijmans, B. T. ( 2009 ). DNA methylation differences after exposure to prenatal famine are common and timing‐ and sex‐specific. Human Molecular Genetics 18, 4046 – 4053. | |
dc.identifier.citedreference | Wang, X., Fang, X., Yang, P., Jiang, X., Jiang, F., Zhao, D., Li, B., Cui, F., Wei, J., Ma, C., Wang, Y., He, J., Lui, Y., Wang, Z., Guo, X., et al. ( 2014 ). The locust genome provides insight into swarm formation and long‐distance flight. Nature Communications 5, 2957. | |
dc.identifier.citedreference | Waterland, R. A., Dolinoy, D. C., Lin, J. R., Smith, C. A., Shi, X. & Tahiliani, K. G. ( 2006 ). Maternal methyl supplements increase offspring DNA methylation at Axin fused. Genesis 44, 401 – 406. | |
dc.identifier.citedreference | Watt, F. & Molloy, P. L. ( 1988 ). Cytosine methylation prevents binding to DNA of a HeLa cell transcription factor required for optimal expression of the adenovirus major late promoter. Genes & Development 2, 1136 – 1143. | |
dc.identifier.citedreference | Weaver, I. C. G., Hellstrom, I. C., Brown, S. E., Andrews, S. D., Dymov, S., Diorio, J., Zhang, T., Szyf, M. & Meaney, M. J. ( 2014 ). The methylated‐DNA binding protein MBD2 enhances NFGI‐A (egr‐1)‐mediated transcriptional activation of the glucocorticoid receptor. Philosophical Transactions of the Royal Society of London B 19, 1 – 11. | |
dc.identifier.citedreference | West‐Eberhard, M. J. ( 1989 ). Phenotypic plasticity and the origins of diversity. Annual Review of Ecology and Systematics 20, 249 – 278. | |
dc.identifier.citedreference | Wiley, R. H. ( 2006 ). Signal detection and animal communication. Advances in the Study of Behavior 36, 217 – 247. | |
dc.identifier.citedreference | Wong, A. H. C., Gottesman, I. I. & Petronis, A. ( 2005 ). Phenotypic differences in genetically identical organisms: the epigenetic perspective. Human Molecular Genetics 14, 11 – 18. | |
dc.identifier.citedreference | Yu, M., Hon, G. C., Szulwach, K. E., Song, C. X., Zhang, L., Kim, A., Li, X., Dai, Q., Shen, Y., Park, B., Min, J. H., Jin, P., Ren, B. & He, C. ( 2012 ). Base‐resolution analysis of 5‐hydroxymethylcytosine in the mammalian genome. Cell 149, 1368 – 1380. | |
dc.identifier.citedreference | Adami, C. ( 2004 ). Use of information theory in molecular biology. arXiv 1, 30. | |
dc.identifier.citedreference | Allis, C. D., Jenuwein, T. & Reinberg, D. ( 2007 ). Epigenetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor. | |
dc.identifier.citedreference | Anderson, N. D. ( 2015 ). Teaching signal detection theory with pseudoscience. Frontiers in Psychology 6, 1 – 4. | |
dc.identifier.citedreference | Anderson, O. S., Sant, K. E. & Dolinoy, D. C. ( 2012 ). Nutrition and epigenetics: an interplay of dietary methyl donors, one‐carbon metabolism, and DNA methylation. Journal of Nutritional Biochemistry 23, 853 – 859. | |
dc.identifier.citedreference | Applebaum, S. W. & Heifetz, Y. ( 1999 ). Density‐dependent physiological phase in insects. Annual Review of Entomology 44, 317 – 341. | |
dc.identifier.citedreference | Barker, D. J. P., Osmond, C., Winter, P. D., Margetts, B. & Simmonds, S. J. ( 1989 ). Weight in infancy and death from ischaemic heart disease. The Lancet 334, 577 – 580. | |
dc.identifier.citedreference | Barlow, D. P. & Bartolomei, M. S. ( 2007 ). Genomic imprinting in mammals. In Epigenetics (eds C. D. Allis, T. Jenuwein, D. Reinberg and M.‐L. Caparros ), pp. 357 – 375. Cold Spring Harbor Laboratory Press, Cold Spring Harbor. | |
dc.identifier.citedreference | Barouki, R., Gluckman, P. D., Grandjean, P., Hanson, M. & Heindel, J. J. ( 2012 ). Developmental origins of non‐communicable disease: implications for research and public health. Environmental Health 11 ( 42 ). https://doi.org/10.1186/1476‐069X‐11‐42 | |
dc.identifier.citedreference | Bateson, P., Barker, D., Clutton‐Brock, T., Deb, D., D’Udine, B., Foley, R. A., Gluckman, P., Godfrey, K., Kirkwood, T., Lahr, M. M., McNamara, J., Metcalfe, N. B., Monaghan, P., Spencer, H. G. & Sultan, S. E. ( 2004 ). Developmental plasticity and human health. Nature 430, 419 – 421. | |
dc.identifier.citedreference | Bateson, P., Gluckman, P. & Hanson, M. ( 2014 ). The biology of developmental plasticity and the predictive adaptive response hypothesis. The Journal of Physiology 592, 2357 – 2368. | |
dc.identifier.citedreference | Beal, J. ( 2015 ). Signal‐to‐noise ratio measures efficacy of biological computing devices and circuits. Frontiers in Bioengineering and Biotechnology 3, 93. | |
dc.identifier.citedreference | Berger, S. L., Kouzarides, T., Shiekhattar, R. & Shilatifard, A. ( 2009 ). An operational definition of epigenetics. Genes & Development 23, 781 – 783. | |
dc.identifier.citedreference | Bestor, T. H. & Tycko, B. ( 1996 ). Creation of genomic methylation patterns. Nature Genetics 12, 363 – 367. | |
dc.identifier.citedreference | Bibikova, M., Barnes, B., Tsan, C., Ho, V., Klotzle, B., Le, J. M., Delano, D., Zhang, L., Schroth, G. P., Gunderson, K. L., Fan, J. B. & Shen, R. ( 2011 ). High density DNA methylation array with single CpG site resolution. Genomics 98, 288 – 295. | |
dc.identifier.citedreference | Bird, A. ( 2002 ). DNA methylation patterns and epigenetic memory. Genes and Development 16, 6 – 21. | |
dc.identifier.citedreference | Bird, A. ( 2007 ). Perceptions of epigenetics. Nature 447, 396 – 398. | |
dc.identifier.citedreference | Bird, A., Taggart, M., Frommer, M., Miller, O. J. & Macleod, D. ( 1985 ). A fraction of the mouse genome that is derived from islands of nonmethylated, CpG‐rich DNA. Cell 40, 91 – 99. | |
dc.identifier.citedreference | Bird, A. P. ( 1980 ). DNA methylation and the frequency of CpG in animal DNA. Nucleic Acids Research 8, 1499 – 1504. | |
dc.identifier.citedreference | Bird, A. P. ( 1986 ). CpG‐rich islands and the function of DNA methylation. Nature 321, 209 – 213. | |
dc.identifier.citedreference | Bjornsson, H., Fallin, M. D. & Feinberg, A. P. ( 2004 ). An integrated epigenetic and genetic approach to common human disease. Trends in Genetics 20, 350 – 358. | |
dc.identifier.citedreference | Bjornsson, T. H., Sigurdsson, M. I., Fallin, M. D., Irizarry, R. a., Aspelund, T., Cui, H., Yu, W., Rongione, M. a., Ekström, T. J., Harris, T. B., Launer, L. J., Eiriksdottir, G., Leppert, M. F., Sapienza, C., Gudnason, V. & Feinberg, A. P. ( 2008 ). Intra‐individual change over time in DNA methylation with familial clustering. Journal of American Medical Association 299, 2877 – 2883. | |
dc.identifier.citedreference | Boerjan, B., Sas, F., Ernst, U. R., Tobback, J., Lemiere, F., Vandegehuchte, M. B., Janssen, C. R., Badisco, L., Marchal, E., Verlinden, H., Schoofs, L. & De Loof, A. ( 2011 ). Locust phase polyphenism: does epigenetic precede endocrine regulation? General and Comparative Endocrinology 173, 120 – 128. | |
dc.identifier.citedreference | Bogdanović, O. & Veenstra, G. J. C. ( 2009 ). DNA methylation and methyl‐CpG binding proteins: developmental requirements and function. Chromosoma 118, 549 – 565. | |
dc.identifier.citedreference | Bolker, B. M. ( 2008 ). Ecological Models and Data in R. Princeton University Press, Princeton. | |
dc.identifier.citedreference | Bradbury, J. W. & Vehrencamp, S. L. ( 2011 ). Priciples of Animal Communication, Second Edition. Sinauer Associates, Sunderland. | |
dc.identifier.citedreference | Campanero, M. R., Armstrong, M. I. & Flemington, E. K. ( 2000 ). CpG methylation as a mechanism for the regulation of E2F activity. Proceedings of the National Academy of Sciences 97, 6481 – 6486. | |
dc.identifier.citedreference | Carlin, J. L., George, R. & Reyes, T. M. ( 2013 ). Methyl donor supplementation blocks the adverse effects of maternal high fat diet on offspring physiology. PLoS One 8, e63549. | |
dc.identifier.citedreference | Chen, Z. & Riggs, A. D. ( 2005 ). Maintenance and regulation of DNA methylation patterns in mammals. Biochemistry and Cell Biology 83, 438 – 448. | |
dc.identifier.citedreference | Cordero, P., Gomez‐Uriz, A. M., Campion, J., Milagro, F. I. & Martinez, J. A. ( 2013 ). Dietary supplementation with methyl donors reduces fatty liver and modifies the fatty acid synthase DNA methylation profile in rats fed an obesogenic diet. Genes and Nutrition 8, 105 – 113. | |
dc.identifier.citedreference | Crudo, A., Petropoulos, S., Moisiadis, V. G., Iqbal, M., Kostaki, A., Machnes, Z., Szyf, M. & Matthews, S. G. ( 2012 ). Prenatal synthetic glucocorticoid treatment changes DNA methylation states in male organ systems: multigenerational effects. Endocrinology 153, 3269 – 3283. | |
dc.identifier.citedreference | Dall, S. R. X., Giraldeau, L.‐A., Olsson, O., McNamar, J. M. & Stephens, D. W. ( 2005 ). Information and its use by animals in evolutionary ecology. Trends in Ecology & Evolution 20, 187 – 193. | |
dc.identifier.citedreference | Deaton, A. & Bird, A. ( 2011 ). CpG islands and the regulation of transcription. Genes & Development 25, 1010 – 1022. | |
dc.identifier.citedreference | Dolinoy, D. C., Das, R., Weidman, J. R. & Jirtle, R. L. ( 2007a ). Metastable epialleles, imprinting, and the fetal origins of adult diseases. Pediatric Research 61, 30 – 37. | |
dc.identifier.citedreference | Dolinoy, D. C., Huang, D. & Jirtle, R. L. ( 2007b ). Maternal nutrient supplementation counteracts bisphenol A‐induced DNA hypomethylation in early development. Proceedings of the National Academy of Sciences of the United States of America 104, 13056 – 13061. | |
dc.identifier.citedreference | Endler, J. A. ( 1992 ). Signals, signal conditions, and the direction of evolution. The American Naturalist 139, S125 – S153. | |
dc.identifier.citedreference | Falckenhayn, C., Boerjan, B., Raddatz, G., Frohme, M., Schoofs, L. & Lyko, F. ( 2013 ). Characterization of genome methylation patterns in the desert locust Schistocerca gregaria. The Journal of Experimental Biology 216, 1423 – 1429. | |
dc.identifier.citedreference | Faulk, C. & Dolinoy, D. C. ( 2011 ). Timing is everything. Epigenetics 6, 791 – 797. | |
dc.identifier.citedreference | Faulk, C., Liu, K., Barks, A., Goodrich, J. M. & Dolinoy, D. C. ( 2014 ). Longitudinal epigenetic drift in mice perinatally exposed to lead. Epigenetics 9, 934 – 941. | |
dc.identifier.citedreference | Feinberg, A. P. ( 2007 ). Phenotypic plasticity and the epigenetics of human disease. Nature 447, 433 – 440. | |
dc.identifier.citedreference | Finnegan, D. J. ( 1989 ). Eukaryotic transposable elements and genome evolution. Trends in Genetics 5, 103 – 107. | |
dc.identifier.citedreference | Fraga, M. F., Ballestar, E., Paz, M. F., Ropero, S., Setien, F., Ballestar, M. L., Heine‐Suner, D., Cigudosa, J. C., Urioste, M., Benitez, J., Boix‐Chornet, M., Sanchez‐Aguilera, A., Ling, C., Carlsson, E., Poulsen, P., Vaag, A., Stephan, Z., Spector, T. D., Wu, Y. Z., Plass, C. & Esteller, M. ( 2005 ). Epigenetic differences arise during the lifetime of monozygotic twins. Proceedings of the National Academy of Sciences of the United States of America 102, 10604 – 10609. | |
dc.identifier.citedreference | Fraga, M. F. & Esteller, M. ( 2007 ). Epigenetics and aging: the targets and the marks. Trends in Genetics 23, 413 – 418. | |
dc.identifier.citedreference | Frankenhuis, W. E. & Del Giudice, M. ( 2012 ). When do adaptive developmental mechanisms yield maladaptive outcomes? Developmental Psychology 48, 628 – 642. | |
dc.identifier.citedreference | Getty, T. ( 1996 ). The maintenance of phenotypic plasticity as a signal detection problem. The American Naturalist 148, 378 – 385. | |
dc.identifier.citedreference | Getty, T. ( 2014 ). GEIs when information transfer is uncertain or incomplete. In Genotype‐by‐Environment Interactions ans Sexual Selection (eds J. Hunt and D. J. Hosken ), pp. 19 – 38. Wiley Blackwell. Hoboken, NJ. | |
dc.identifier.citedreference | Ghalambor, C. K., McKay, J. K., Carroll, S. P. & Reznick, D. N. ( 2007 ). Adaptive versus non‐adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Functional Ecology 21, 394 – 407. | |
dc.identifier.citedreference | Gilbert, S. F. & Epel, D. ( 2015 ). Ecological Developmental Biology: The Environmental Regulation of Development, Health, and Evolution. Sinauer Associates. Sunderland, MA. | |
dc.identifier.citedreference | Gillman, M. W. ( 2005 ). Developmental origins of health and disease. New England Journal of Medicine 353, 1848 – 1850. | |
dc.identifier.citedreference | Gillman, M. W. ( 2010 ). Early infancy – a critical period for development of obesity. Journal of Developmental Origins of Health and Disease 1, 292 – 299. | |
dc.identifier.citedreference | Gluckman, P. D., Cutfield, W., Hofman, P. & Hanson, M. A. ( 2005a ). The fetal, neonatal, and infant environments – the long‐term consequences for disease risk. Early Human Development 81, 51 – 59. | |
dc.identifier.citedreference | Gluckman, P. D., Hanson, M. A. & Spencer, H. G. ( 2005b ). Predictive adaptive responses and human evolution. Trends in Ecology and Evolution 20, 527 – 533. | |
dc.identifier.citedreference | Gluckman, P. D. & Hanson, M. A. ( 2006 ). The developmental origins of health and disease: an overview. In Developmental Origins of Health and Disease (eds P. D. Gluckman and M. A Hanson ), pp. 1 – 5. Cambridge University Press, Cambridge. | |
dc.identifier.citedreference | Gluckman, P. D., Hanson, M. A. & Beedle, A. S. ( 2007 ). Early life events and their consequences for later disease: a life history and evolutionary perspective. American Journal of Human Biology 19, 1 – 19. | |
dc.identifier.citedreference | Godfrey, K. M., Gluckman, P. D. & Hanson, M. A. ( 2010 ). Developmental origins of metabolic disease: life course and intergenerational perspectives. Trends in Endocrinology and Metabolism 21, 199 – 205. | |
dc.identifier.citedreference | Godfrey, K. M., Lillycrop, K. A., Burdge, G. C., Gluckman, P. D. & Hanson, M. A. ( 2007 ). Epigenetic mechanisms and the mismatch concept of the developmental origins of health and disease. Pediatric Research 61, 31 – 36. | |
dc.identifier.citedreference | Goll, M. G. & Bestor, T. H. ( 2005 ). Eukaryotic cytosine methyltransferases. Annual Review Biochemestry 74, 481 – 514. | |
dc.identifier.citedreference | Guilford, T. & Dawkins, M. S. ( 1991 ). Receiver psychology and the evolution of animal signals. Animal Behaviour 42, 1 – 14. | |
dc.identifier.citedreference | Guilford, T. & Dawkins, M. S. ( 1993 ). Receiver psychology and the design of animal signals. Trends in Neurosciences 16, 430 – 436. | |
dc.identifier.citedreference | Hahn‐Townsend, C. K., Varde, P. A., MohanKumar, P. S. & MohanKumar, S. M. ( 2016 ). Metabolic dysfunction induced by prenatal exposure to bisphenol‐A and diethyl hexyl phthalate: exacerbation by high fat diet. The FASEB Journal 30, 1293.6 – 1293.6. | |
dc.identifier.citedreference | Hales, C. N. & Barker, D. J. P. ( 2001 ). The thrifty phenotype hypothesis: type 2 diabetes. British Medical Bulletin 60, 5 – 20. | |
dc.identifier.citedreference | Hartley, R. V. L. ( 1928 ). Transmission of information. Bell System Technical Journal 7, 535 – 563. | |
dc.identifier.citedreference | Hasson, O. ( 1994 ). Cheating signals. Journal of Theoretical Biology 167, 223 – 238. | |
dc.identifier.citedreference | Hasson, O. ( 1997 ). Towards a general theory of biological signaling. Journal of Theoretical Biology 185, 139 – 156. | |
dc.identifier.citedreference | Heijmans, B. T., Tobi, E. W., Stein, A. D., Putter, H., Blauw, G. J., Susser, E. S., Slagboom, P. E. & Lumey, L. H. ( 2008 ). Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proceedings of the National Academy of Sciences of the United States of America 105, 17046 – 17049. | |
dc.identifier.citedreference | Holliday, R. & Pugh, J. E. ( 1975 ). DNA modification mechanisms and gene activity during development. Science 187, 226 – 232. | |
dc.identifier.citedreference | Hunter, R. G., Gagnidze, K., McEwen, B. S. & Pfaff, D. W. ( 2014 ). Stress and the dynamic genome: steroids, epigenetics, and the transposome. Proceedings of the National Academy of Sciences of the United States of America 112, 6828 – 6833. | |
dc.identifier.citedreference | Hurd, P. L. & Enquist, M. ( 2005 ). A strategic taxonomy of biological communication. Animal Behaviour 70, 1155 – 1170. | |
dc.identifier.citedreference | Illingworth, R. S. & Bird, A. P. ( 2009 ). CpG islands – ‘A rough guide’. FEBS Letters 583, 1713 – 1720. | |
dc.identifier.citedreference | Irizarry, R. A., Ladd‐Acosta, C., Wen, B., Wu, Z., Montano, C., Onyango, P., Cui, H., Gabo, K., Rongione, M., Webster, M., Ji, H., Potash, J. B., Sabunciyan, S. & Feinberg, A. P. ( 2009 ). The human colon cancer methylome shows similar hypo‐ and hypermethylation at conserved tissue‐specific CpG island shores. Nature Genetics 41, 178 – 186. | |
dc.identifier.citedreference | Jaenisch, R. & Bird, A. ( 2003 ). Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nature Genetics 33, 245 – 254. | |
dc.identifier.citedreference | Jones, P. A. ( 2012 ). Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nature Reviews Genetics 13, 484 – 492. | |
dc.identifier.citedreference | Klose, R. J. & Bird, A. P. ( 2006 ). Genomic DNA methylation: the mark and its mediators. Trends in Biochemical Sciences 31, 89 – 97. | |
dc.identifier.citedreference | Kochmanski, J., Marchlewicz, E. H., Savidge, M., Montrose, L., Faulk, C. & Dolinoy, D. C. ( 2016 ). Longitudinal effects of developmental bisphenol A and variable diet exposures on epigenetic drift in mice. Reproductive Toxicology 68, 154 – 163. | |
dc.identifier.citedreference | Kochmanski, J., Montrose, L., Goodrich, J. M. & Dolinoy, D. C. ( 2017 ). Environmental deflection: the impact of toxicant exposures on the aging epigenome. Toxicological Sciences 156 ( 2 ), 1 – 11. | |
dc.identifier.citedreference | Kohli, R. M. & Zhang, Y. ( 2013 ). TET enzymes, TDG and the dynamics of DNA demethylation. Nature 502, 472 – 479. | |
dc.identifier.citedreference | Kuh, D., Ben‐Shlomo, Y., Lynch, J., Hallqvist, J. & Power, C. ( 2003 ). Life course epidemiology. Journal of Epidemiology and Community Health 57, 778 – 783. | |
dc.identifier.citedreference | Kundakovic, M., Gudsnuk, K., Franks, B., Madrid, J., Miller, R. L., Perera, F. P. & Champagne, F. A. ( 2013 ). Sex‐specific epigenetic disruption and behavioral changes following low‐dose in utero bisphenol A exposure. Proceedings of the National Academy of Sciences of the United States of America 110, 9956 – 9961. | |
dc.identifier.citedreference | Laird, C. D., Pleasant, N. D., Clark, A. D., Sneeden, J. L., Hassan, K. M. A., Manley, N. C., Vary, J. C. J., Morgan, T., Hansen, R. S. & Stöger, R. ( 2004 ). Hairpin‐bisulfite PCR: assessing epigenetic methylation patterns on complementary strands of individual DNA molecules. Proceedings of the National Academy of Sciences of the United States of America 101, 204 – 209. | |
dc.identifier.citedreference | Laubach, Z. M., Faulk, C. D., Cardenas, A. & Perng, W. ( 2017 ). Nutrition, DNA methylation, and developmental origins of cardiometabolic disease: a signal systems approach. In Handbook of Nutrition, Diet, and Epigenetics (eds V. R. Preedy and V. B. Patel ), pp. 1 – 18. Springer International Publishing. Gewerbestrasse 11, Switzerland. | |
dc.identifier.citedreference | Li, E. & Bird, A. ( 2007 ). DNA methylation in mammals. In Epigenetics (eds C. D. Allis, T. Jenuwein, D. Reinberg and M.‐L. Caparros ), pp. 343 – 356. Cold Spring Harbor Laboratory Press, Cold Spring Harbor. | |
dc.identifier.citedreference | Martin, G. M. ( 2005 ). Epigenetic drift in aging identical twins. Proceedings of the National Academy of Sciences of the United States of America 102, 10413 – 10414. | |
dc.identifier.citedreference | Maynard Smith, J. & Harper, D. ( 2003 ). Animal Signals. Oxford University Press, Oxford. | |
dc.identifier.citedreference | McClintock, B. ( 1984 ). The significance of responses of the genome to challenge. Science 226, 792 – 801. | |
dc.identifier.citedreference | McNamara, J. M., Dall, S. R. X., Hammerstein, P. & Leimar, O. ( 2016 ). Detection vs. selection: integration of genetic, epigenetic and environmental cues in fluctuating environments. Ecology Letters 19, 1267 – 1276. | |
dc.identifier.citedreference | Miura, T. ( 2005 ). Developmental regulation of caste‐specific characters in social‐insect polyphenism. Evolution and Development 7, 122 – 129. | |
dc.identifier.citedreference | Nan, X., Ng, H. H., Johnson, C. A., Laherty, C. D., Turner, B. M., Eisenman, R. N. & Bird, A. ( 1998 ). Transcriptional repression by the methyl‐CpG‐binding protein MeCP2 involves a histone deacetylase complex. Nature 393, 386 – 389. | |
dc.identifier.citedreference | Nettle, D. & Bateson, M. ( 2015 ). Adaptive developmental plasticity: what is it, how can we recognize it and when can it evolve? Proceedings of the Royal Society B: Biological Sciences 282, 20151005. | |
dc.identifier.citedreference | Ooi, S. K. T. & Bestor, T. H. ( 2008 ). Cytosine methylation: remaining faithful. Current Biology 18, R174 – R176. | |
dc.identifier.citedreference | Painter, R. C., Roseboom, T. J. & Bleker, O. P. ( 2005 ). Prenatal exposure to the Dutch famine and disease in later life: an overview. Reproductive Toxicology 20, 345 – 352. | |
dc.identifier.citedreference | Pener, M. P. ( 1991 ). Locust phase polymorphism and its endocrine relations. Advances in Insect Physiology 23, 1 – 79. | |
dc.identifier.citedreference | Pener, M. P. & Simpson, S. J. ( 2009 ). Locust phase polyphenism: an update. Advances in Insect Physiology 36, 1 – 272. | |
dc.identifier.citedreference | Pener, M. P. & Yerushalmi, Y. ( 1998 ). The physiology of locust phase polymorphism: an update. Journal of Insect Physiology 44, 365 – 377. | |
dc.identifier.citedreference | Pfeifer, G. P., Steigerwald, S. D., Hansen, R. S., Gartler, S. M. & Riggs, A. D. ( 1990 ). Polymerase chain reaction‐aided genomic sequencing of an X chromosome‐linked CpG island: methylation patterns suggest clonal inheritance, CpG site autonomy, and an explanation of activity state stability. Proceedings of the National Academy of Sciences of the United States of America 87, 8252 – 8256. | |
dc.identifier.citedreference | Pigliucci, M. ( 1998 ). Developmental phenotypic plasticity: where internal programming meets the external environment. Current Opinion in Plant Biology 1, 87 – 91. | |
dc.identifier.citedreference | Ravelli, A. C. J., Vandermeulen, J. H. P., Michels, R. P. J., Osmond, C., Barker, D. J. P., Hales, C. N. & Bleker, O. P. ( 1998 ). Glucose‐tolerance in adults after prenatal exposure to famine. The Lancet 351, 173 – 177. | |
dc.identifier.citedreference | Razin, A. & Riggs, A. D. ( 1980 ). DNA methylation and gene function. Science 210, 604 – 610. | |
dc.identifier.citedreference | Reik, W., Dean, W. & Walter, J. ( 2001 ). Epigenetic reprogramming in mammalian development. Science 293, 1089 – 1093. | |
dc.identifier.citedreference | Riggs, A. D. ( 1975 ). X inactivation, differentiation, and DNA methylation. Cytogenetics and Cell Genetics 14, 9 – 25. | |
dc.identifier.citedreference | Riggs, A. D. & Xiong, Z. ( 2004 ). Methylation and epigenetic fidelity. Proceedings of the National Academy of Science 101, 4 – 5. | |
dc.identifier.citedreference | Robinson, K. L., Tohidi‐Esfahani, D., Lo, N., Simpson, S. J. & Sword, G. A. ( 2011 ). Evidence for widespread genomic methylation in the migratory locust, Locusta migratoria (orthoptera: Acrididae). PLoS One 6, e28167. | |
dc.identifier.citedreference | Robinson, K. L., Tohidi‐Esfahani, D., Ponton, F., Simpson, S. J., Sword, G. A. & Lo, N. ( 2016 ). Alternative migratory locust phenotypes are associated with differences in the expression of genes encoding the methylation machinery. Insect Molecular Biology 25, 105 – 115. | |
dc.owningcollname | Interdisciplinary and Peer-Reviewed |
Files in this item
Remediation of Harmful Language
The University of Michigan Library aims to describe library materials in a way that respects the people and communities who create, use, and are represented in our collections. Report harmful or offensive language in catalog records, finding aids, or elsewhere in our collections anonymously through our metadata feedback form. More information at Remediation of Harmful Language.
Accessibility
If you are unable to use this file in its current format, please select the Contact Us link and we can modify it to make it more accessible to you.