Mammalian viviparity: a complex niche in the evolution of genomic imprinting
Open accessAbstract
Evolution of mammalian reproductive success has witnessed a strong dependence on maternal resources through placental in utero development. Genomic imprinting, which has an active role in mammalian viviparity, also reveals a biased role for matrilineal DNA in its regulation. The co-existence of three matrilineal generations as one (mother, foetus and post-meiotic oocytes) has provided a maternal niche for transgenerational co-adaptive selection pressures to operate. In utero foetal growth has required increased maternal feeding in advance of foetal energetic demands; the mammary glands are primed for milk production in advance of birth, while the maternal hypothalamus is hormonally primed by the foetal placenta for nest building and post-natal care. Such biological forward planning resulted from maternal-foetal co-adaptation facilitated by co-expression of the same imprinted allele in the developing hypothalamus and placenta. This co-expression is concurrent with the placenta interacting with the adult maternal hypothalamus thereby providing a transgenerational template on which selection pressures may operate ensuring optimal maternalism in this and the next generation. Invasive placentation has further required the maternal immune system to adapt and positively respond to the foetal allotype. Pivotal to these mammalian evolutionary developments, genomic imprinting emerged as a monoallelic gene dosage regulatory mechanism of tightly interconnected gene networks providing developmental genetic stability for in utero development.
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This leads to differential selection pressures on maternally and paternally inherited alleles in the conceptus with respect to resource allocation and is manifested as genomic imprinting, a mechanism for monoallelically regulating gene dosage in a parent-of-origin fashion.
“This leads to differential selection pressures on maternally and paternally inherited alleles in the conceptus with respect to resource allocation and is manifested as genomic imprinting, a mechanism for monoallelically regulating gene dosage in a parent-of-origin fashion (305, 391).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [305]
Changes in placental phenotype in response to environmental cues can be seen as a co-adaptive response mutually beneficial to the mother and fetus in the successful outcome of pregnancy.
“Changes in placental phenotype in response to environmental cues can, therefore, be seen as a co-adaptive response mutually beneficial to the mother and fetus in the successful outcome of pregnancy (305).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [305]
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Cites
CTCF: Master Weaver of the Genome
Phillips‐Cremins, J. E., & Corces, V. G. (2009) · Cell · doi:10.1016/j.cell.2009.06.001 · Cited by 1,540 · see citing works
Architecture of the human regulatory network derived from ENCODE data
Gerstein, M., Kundaje, A. B., Hariharan, M., Landt, S. G., Yan, K., Cheng, C., Mu, X. J., Khurana, E., Rozowsky, J. S., Alexander, R. P., et al. (2012) · Nature · doi:10.1038/nature11245 · Cited by 1,418 · see citing works
Placental development: Lessons from mouse mutants
Rossant, J., & Cross, J. C. (2001) · Nature Reviews Genetics · doi:10.1038/35080570 · Cited by 1,273 · see citing works
Immunology of placentation in eutherian mammals
Moffett, A., & Loke, C. (2006) · Nature reviews. Immunology · doi:10.1038/nri1897 · Cited by 843 · see citing works
The H19 lincRNA is a developmental reservoir of miR-675 that suppresses growth and Igf1r
Keniry, A., Oxley, D., Monnier, P., Kyba, M., Dandolo, L., Smits, G., & Reik, W. (2012) · Nature Cell Biology · doi:10.1038/ncb2521 · Cited by 806 · see citing works
Biased gene conversion and the evolution of mammalian genomic landscapes
Duret, L., & Galtier, N. (2009) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev-genom-082908-150001 · Cited by 737 · see citing works
Widespread Monoallelic Expression on Human Autosomes
Gimelbrant, A., Hutchinson, J. N., Thompson, B. R., & Chess, A. (2007) · Science · doi:10.1126/science.1148910 · Cited by 655 · see citing works
Sry : the master switch in mammalian sex determination
Kashimada, K., & Koopman, P. A. (2010) · Development · doi:10.1242/dev.048983 · Cited by 354 · see citing works
Sex-Specific Parent-of-Origin Allelic Expression in the Mouse Brain
Gregg, C. J., Zhang, J., Butler, J. E., Haig, D., & Dulac, C. G. (2010) · Science · doi:10.1126/science.1190831 · Cited by 347 · see citing works
The Rise of Oxygen over the Past 205 Million Years and the Evolution of Large Placental Mammals
Falkowski, P. G., Katz, M. E., Milligan, A. J., Fennel, K., Cramer, B. S., Aubry, M.-P., Berner, R. A., Novacek, M. J., & Zapol, W. M. (2005) · Science · doi:10.1126/science.1116047 · Cited by 333 · see citing works
Analysis of the platypus genome suggests a transposon origin for mammalian imprinting
Pask, A. J., Papenfuss, A. T., Ager, E. I., McColl, K. A., Speed, T. P., & Renfree, M. B. (2009) · Genome biology · doi:10.1186/gb-2009-10-1-r1 · Cited by 328 · see citing works
SOX3 is required during the formation of the hypothalamo-pituitary axis
Rizzoti, K., Brunelli, S., Carmignac, D. F., Thomas, P. Q., Robinson, I. C. A. F., & Lovell-Badge, R. H. (2004) · Nature Genetics · doi:10.1038/ng1309 · Cited by 313 · see citing works
Dynamic link of DNA demethylation, DNA strand breaks and repair in mouse zygotes
Wossidlo, M., Arand, J., Sebastiano, V., Lepikhov, K., Boiani, M., Reinhardt, R., Schöler, H. R., & Walter, J. (2010) · The EMBO Journal · doi:10.1038/emboj.2010.80 · Cited by 245 · see citing works
Natural killer cell-triggered vascular transformation: maternal care before birth?
Zhang, J., Chen, Z., Smith, G. N., & Croy, B. A. (2010) · Cellular and Molecular Immunology · doi:10.1038/cmi.2010.38 · Cited by 238 · see citing works
C19MC microRNAs are processed from introns of large Pol-II, non-protein-coding transcripts
Bortolin‐Cavaillé, M., Dance, M., Weber, M., & Cavaillé, J. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp205 · Cited by 231 · see citing works
Coadaptation in mother and infant regulated by a paternally expressed imprinted gene
Curley, J. P., Barton, S. C., Surani, M. A., & Keverne, E. B. (2004) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2004.2725 · Cited by 223 · see citing works
Self-citationA Maternal–Offspring Coadaptation Theory for the Evolution of Genomic Imprinting
Wolf, J. B., & Hager, R. (2006) · PLoS Biology · doi:10.1371/journal.pbio.0040380 · Cited by 213 · see citing works
Kagami, M., Nagai, T., Fukami, M., Yamazawa, K., & Ogata, T. (2007) · Journal of Assisted Reproduction and Genetics · doi:10.1007/s10815-006-9096-3 · Cited by 201 · see citing works
Mechanisms and consequences of widespread random monoallelic expression
Chess, A. (2012) · Nature Reviews Genetics · doi:10.1038/nrg3239 · Cited by 186 · see citing works
Derijck, A. A. H. A., van der Heijden, G. W., Giele, M., Philippens, M. E. P., & de Boer, P. (2008) · Human Molecular Genetics · doi:10.1093/hmg/ddn090 · Cited by 182 · see citing works
The origin and evolution of genomic imprinting and viviparity in mammals
Renfree, M. B., Suzuki, S., & Kaneko‐Ishino, T. (2012) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2012.0151 · Cited by 179 · see citing works
Evolution of Genomic Imprinting: Insights from Marsupials and Monotremes
Renfree, M. B., Hore, T. A., Shaw, G., Graves, J. A. M., & Pask, A. J. (2009) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev-genom-082908-150026 · Cited by 178 · see citing works
Disruption of maternal DNA repair increases sperm-derived chromosomal aberrations
Marchetti, F., Essers, J., Kanaar, R., & Wyrobek, A. J. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0705257104 · Cited by 170 · see citing works
How it’s Made: Organisational Effects of Hormones on the Developing Brain
McCarthy, M. M. (2010) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2010.02021.x · Cited by 138 · see citing works
FOXL2 versus SOX9: A lifelong “battle of the sexes”
Veitia, R. A. (2010) · BioEssays · doi:10.1002/bies.200900193 · Cited by 131 · see citing works
Genomic imprinting in the placenta
Wagschal, A., & Feil, R. (2006) · Cytogenetic and Genome Research · doi:10.1159/000090819 · Cited by 130 · see citing works
Increased body fat in mice with a targeted mutation of the paternally expressed imprinted gene Peg3
Curley, J. P., Pinnock, S. B., Dickson, S. L., Thresher, R. R., Miyoshi, N., Surani, M. A., & Keverne, E. B. (2005) · The FASEB Journal · doi:10.1096/fj.04-3216fje · Cited by 128 · see citing works
Self-citationPlacental protection of the fetal brain during short-term food deprivation
Broad, K. D., & Keverne, E. B. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1106022108 · Cited by 109 · see citing works
Self-citationAn imprinting element from the mouse H19 locus functions as a silencer in Drosophila
Lyko, F., Brenton, J. D., Surani, M. A., & Paro, R. (1997) · Nature Genetics · doi:10.1038/ng0697-171 · Cited by 106 · see citing works
Coadaptation and conflict, misconception and muddle, in the evolution of genomic imprinting
Haig, D. (2013) · Heredity · doi:10.1038/hdy.2013.97 · Cited by 89 · see citing works
Imprinted genes in mouse placental development and the regulation of fetal energy stores
Tunster, S. J., Jensen, A. B., & John, R. M. (2013) · Reproduction · doi:10.1530/rep-12-0511 · Cited by 85 · see citing works
Broad, K. D., Curley, J. P., & Keverne, E. B. (2009) · Developmental Neurobiology · doi:10.1002/dneu.20702 · Cited by 73 · see citing works
Self-citationPeg3/Pw1 Is Involved in p53-mediated Cell Death Pathway in Brain Ischemia/Hypoxia
Yamaguchi, A., Taniguchi, M., Hori, O., Ogawa, S., Tojo, N., Matsuoka, N., Miyake, S., Kasai, K., Sugimoto, H., Tamatani, M., et al. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m107435200 · Cited by 73 · see citing works
Schulz, R., Proudhon, C., Bestor, T. H., Woodfine, K., Lin, C., Lin, S., Prissette, M., Oakey, R. J., & Bourc’his, D. (2010) · PLoS Genetics · doi:10.1371/journal.pgen.1001214 · Cited by 72 · see citing works
Genomic imprinting mechanisms in embryonic and extraembryonic mouse tissues
Hudson, Q. J., Kuliński, T. M., Huetter, S. P., & Barlow, D. P. (2010) · Heredity · doi:10.1038/hdy.2010.23 · Cited by 69 · see citing works
Genomic imprinting in marsupial placentation
Renfree, M. B., Ager, E. I., Shaw, G., & Pask, A. J. (2008) · Reproduction · doi:10.1530/rep-08-0264 · Cited by 63 · see citing works
Review: Toward an integrated evolutionary understanding of the mammalian placenta
Wildman, D. E. (2011) · Placenta · doi:10.1016/j.placenta.2011.01.005 · Cited by 57 · see citing works
More than insulator: multiple roles of CTCF at the H19-Igf2 imprinted domain
Singh, P., Lee, D., & Szabó, P. E. (2012) · Frontiers in Genetics · doi:10.3389/fgene.2012.00214 · Cited by 55 · see citing works
Lonstein, J. S., Rood, B. D., & Vries, G. J. D. (2002) · Hormones and Behavior · doi:10.1006/hbeh.2001.1740 · Cited by 53 · see citing works
Sato, Y., Shinka, T., Sakamoto, K., Ewis, A. A., & Nakahori, Y. (2009) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-009-0308-x · Cited by 53 · see citing works
Importance of the matriline for genomic imprinting, brain development and behaviour
Keverne, E. B. (2012) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2011.0327 · Cited by 49 · see citing works
Self-citationVaiman, D., Mondon, F., Garcès-Duran, A., Mignot, T.-M., Robert, B., Rebourcet, R., Jammes, H., Chelbi, S. T., Quetin, F., Marceau, G., et al. (2005) · BMC Genomics · doi:10.1186/1471-2164-6-111 · Cited by 48 · see citing works
Molecular evolution of imprinted genes: no evidence for antagonistic coevolution
McVean, G. T., & Hurst, L. D. (1997) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1997.0105 · Cited by 47 · see citing works
Mechanisms of long range silencing by imprinted macro non-coding RNAs
Pauler, F. M., Barlow, D. P., & Hudson, Q. J. (2012) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2012.02.005 · Cited by 46 · see citing works
Rabinovitz, S., Kaufman, Y., Ludwig, G., Razin, A., & Shemer, R. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1116661109 · Cited by 41 · see citing works
Imprinted genes show unique patterns of sequence conservation
Hutter, B., Bieg, M., Helms, V., & Paulsen, M. (2010) · BMC Genomics · doi:10.1186/1471-2164-11-649 · Cited by 39 · see citing works
Evolution of genomic imprinting as a coordinator of coadapted gene expression
Wolf, J. B. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1205686110 · Cited by 35 · see citing works
Monoallelic gene expression and mammalian evolution
Keverne, B. (2009) · BioEssays · doi:10.1002/bies.200900074 · Cited by 35 · see citing works
O’Connell, M. J., Loughran, N. B., Walsh, T., Donoghue, M. T. A., Schmid, K. J., & Spillane, C. (2010) · Mammalian Genome · doi:10.1007/s00335-010-9283-5 · Cited by 27 · see citing works
Regulation of murine placentogenesis by the retroviral genes Syncytin-A, Syncytin-B and Peg10
Henke, C., Ruebner, M., Faschingbauer, F., Stolt, C. C., Schaefer, N., Lang, N. R., Beckmann, M. W., Strissel, P. L., & Strick, R. (2013) · Differentiation · doi:10.1016/j.diff.2013.02.002 · Cited by 26 · see citing works
Systems properties of proteins encoded by imprinted genes
Sandhu, K. S. (2010) · Epigenetics · doi:10.4161/epi.5.7.12883 · Cited by 25 · see citing works
Reprogramming of DNA Replication Timing
Shufaro, Y., Lacham‐Kaplan, O., Tzuberi, B.-Z., McLaughlin, J. K., Trounson, A. O., Cedar, H., & Reubinoff, B. E. (2010) · Stem Cells · doi:10.1002/stem.303 · Cited by 21 · see citing works
Guibert, S., Zhao, Z., Sjölinder, M., Göndör, A., Fernandez-Woodbridge, A., Pant, V., & OHLSSON, R. I. (2012) · Epigenetics · doi:10.4161/epi.19487 · Cited by 21 · see citing works
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Keverne, E. B. (2006) · Cambridge University Press eBooks · doi:10.1017/cbo9780511545207.012 · Cited by 17 · see citing works
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Kuliński, T. M., Barlow, D. P., & Hudson, Q. J. (2013) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2013.02.012 · Cited by 10 · see citing works
Arney, K. L., Bae, E., Olsen, C., & Drewell, R. A. (2006) · Development Genes and Evolution · doi:10.1007/s00427-006-0102-7 · Cited by 7 · see citing works
Pink, C. J., & Hurst, L. D. (2011) · PLoS ONE · doi:10.1371/journal.pone.0024480 · Cited by 6 · see citing works
Chromosomal networks as mediators of epigenetic states: The maternal genome connection
Sumida, N., & OHLSSON, R. I. (2010) · Epigenetics · doi:10.4161/epi.5.4.11538 · Cited by 6 · see citing works
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- Authors
- Keverne, E. B.
- Affiliations
- University of Cambridge (GB)
- Corresponding author
- Keverne, E B
- Venue
- Heredity
- Published
- 2014-02-26
- Volume
- 113
- Issue
- 2
- Pages
- 138-144
- ISSN
- 0018-067X (ISSN-L)
- 1365-2540
- PMC
- PMC4105457
- OpenAlex
- W1968011921
- Cited by
- 17
- References
- 59
- Citations by year
- 2026: 1 · 2024: 2 · 2022: 1 · 2021: 1 · 2019: 2 · 2018: 1 · 2017: 6 · 2016: 2 · 2014: 1
- FWCI
- 1.95
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Heredity (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Syndromes and Imprinting
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic and phenotypic traits in livestock
- Keywords
- genomic imprinting, placenta, fetal growth, mammary gland development, placental hormones, maternal-fetal immune tolerance, monoallelic expression, in utero development
- MeSH terms
- Adaptation, Biological, Alleles, Animals, Biological Evolution, Female, Gene Expression Regulation, Humans, Male, Mammals, Reproduction, Genomic Imprinting, Gene Regulatory Networks
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