Non-model organisms are generally more difficult and/or time consuming to work with than model organisms. In addition, epigenetic analysis of model organisms is facilitated by well-established protocols, and commercially-available reagents and kits that may not be available for, or previously tested on, non-model organisms. Given the evolutionary conservation and widespread nature of many epigenetic mechanisms, a powerful method to analyze epigenetic phenomena from non-model organisms would be to use transgenic model organisms containing an epigenetic region of interest from the non-model. Interestingly, while transgenic Drosophila and mice have provided significant insight into the molecular mechanisms and evolutionary conservation of the epigenetic processes that target epigenetic control regions in other model organisms, this method has so far been under-exploited for non-model organism epigenetic analysis. This paper details several experiments that have examined the epigenetic processes of genomic imprinting and paramutation, by transferring an epigenetic control region from one model organism to another. These cross-species experiments demonstrate that valuable insight into both the molecular mechanisms and evolutionary conservation of epigenetic processes may be obtained via transgenic experiments, which can then be used to guide further investigations and experiments in the species of interest. 1. Introduction Transgenic model organisms have been widely used to study a variety of epigenetic processes and mechanisms. The majority of these studies have examined epigenetic control regions (i.e., DNA sequences targeted by epigenetic modifications, also referred to herein as epigenetic sequences) that have been relocated to a novel chromosomal position in the same model organism, an approach that can provide valuable information regarding the minimum sequences required at the endogenous locus, as well as the mechanisms and proteins that contribute to epigenetic expression or repression [1–6]. An alternative, but less used, type of transgenic epigenetic study involves transferring an epigenetic control region from one species into another. This cross-species approach can provide valuable insight into the molecular mechanisms that act on an epigenetic sequence of interest, which may be difficult to study at the endogenous locus, and can be facilitated in transgenic studies by including easy-to-monitor reporter genes adjacent to the epigenetic sequence in the transgenic construct. In addition, this method holds tremendous potential in the study of the
References
[1]
F. Sleutels and D. P. Barlow, “Investigation of elements sufficient to imprint the mouse Air promoter,” Molecular and Cellular Biology, vol. 21, no. 15, pp. 5008–5017, 2001.
[2]
M. J. Cranston, T. L. Spinka, D. A. Elson, and M. S. Bartolomei, “Elucidation of the minimal sequence required to imprint H19 transgenes,” Genomics, vol. 73, no. 1, pp. 98–107, 2001.
[3]
J. F. X. Ainscough, T. Koidet, M. Tada, S. Barton, and M. A. Surani, “Imprinting of Igf2 and H19 from a 130？kb YAC transgene,” Development, vol. 124, no. 18, pp. 3621–3632, 1997.
[4]
F. Cerrato, A. Sparago, I. Di Matteo et al., “The two-domain hypothesis in Beckwith-Wiedemann syndrome: autonomous imprinting of the telomeric domain of the distal chromosome 7 cluster,” Human Molecular Genetics, vol. 14, no. 4, pp. 503–511, 2005.
[5]
C. Gebert, D. Kunkel, A. Grinberg, and K. Pfeifer, “H19 imprinting control region methylation requires an imprinted environment only in the male germ line,” Molecular and Cellular Biology, vol. 30, no. 5, pp. 1108–1115, 2010.
[6]
H. Matsuzaki, E. Okamura, A. Fukamizu, and K. Tanimoto, “CTCF binding is not the epigenetic mark that establishes post-fertilization methylation imprinting in the transgenic H19 ICR,” Human Molecular Genetics, vol. 19, no. 7, pp. 1190–1198, 2010.
[7]
S. I. S. Grewal and J. C. Rice, “Regulation of heterochromatin by histone methylation and small RNAs,” Current Opinion in Cell Biology, vol. 16, no. 3, pp. 230–238, 2004.
[8]
M. A. Matzke and J. A. Birchler, “RNAi-mediated pathways in the nucleus,” Nature Reviews Genetics, vol. 6, no. 1, pp. 24–35, 2005.
[9]
H. Cerutti and J. A. Casas-Mollano, “On the origin and functions of RNA-mediated silencing: from protists to man,” Current Genetics, vol. 50, no. 2, pp. 81–99, 2006.
[10]
J. Nakayama, J. C. Rice, B. D. Strahl, C. D. Allis, and S. I. S. Grewal, “Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly,” Science, vol. 292, no. 5514, pp. 110–113, 2001.
[11]
G. Wang, A. Ma, C. M. Chow et al., “Conservation of heterochromatin protein 1 function,” Molecular and Cellular Biology, vol. 20, no. 18, pp. 6970–6983, 2000.
[12]
A. Zemach, I. E. McDaniel, P. Silva, and D. Zilberman, “Genome-wide evolutionary analysis of eukaryotic DNA methylation,” Science, vol. 328, no. 5980, pp. 916–919, 2010.
[13]
S. Feng, S. J. Cokus, X. Zhang et al., “Conservation and divergence of methylation patterning in plants and animals,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 19, pp. 8689–8694, 2010.
[14]
A. J. Bannister and T. Kouzarides, “Regulation of chromatin by histone modifications,” Cell Research, vol. 21, no. 3, pp. 381–395, 2011.
[15]
B. Li, M. Carey, and J. L. Workman, “The role of chromatin during transcription,” Cell, vol. 128, no. 4, pp. 707–719, 2007.
[16]
S. J. Els？sser and S. D'Arcy, “Towards a mechanism for histone chaperones,” Biochimica et Biophysica Acta.
[17]
A. Dean, “In the loop: long range chromatin interactions and gene regulation,” Briefings in Functional Genomics, vol. 10, no. 1, pp. 3–10, 2011.
[18]
B. Schuettengruber, D. Chourrout, M. Vervoort, B. Leblanc, and G. Cavalli, “Genome Regulation by Polycomb and Trithorax Proteins,” Cell, vol. 128, no. 4, pp. 735–745, 2007.
[19]
C. Grimaud, F. Bantignies, M. Pal-Bhadra, P. Ghana, U. Bhadra, and G. Cavalli, “RNAi components are required for nuclear clustering of polycomb group response elements,” Cell, vol. 124, no. 5, pp. 957–971, 2006.
[20]
S. Schmitt and R. Paro, “RNA at the steering wheel,” Genome Biology, vol. 7, no. 5, article 218, 2006.
[21]
H. H. Kavi, H. R. Fernandez, W. Xie, and J. A. Birchler, “Polycomb, pairing and PIWI—RNA silencing and nuclear interactions,” Trends in Biochemical Sciences, vol. 31, no. 9, pp. 485–487, 2006.
[22]
C. A. Bunker and R. E. Kingston, “Transcriptional repression by Drosophila and mammalian polycomb group proteins in transfected mammalian cells,” Molecular and Cellular Biology, vol. 14, no. 3, pp. 1721–1732, 1994.
[23]
G. Schotta, A. Ebert, V. Krauss et al., “Central role of Drosophila SU(VAR)3-9 in histone H3-K9 methylation and heterochromatic gene silencing,” The EMBO Journal, vol. 21, no. 5, pp. 1121–1131, 2002.
[24]
J. S. Tea and L. Luo, “The chromatin remodeling factor Bap55 functions through the TIP60 complex to regulate olfactory projection neuron dendrite targeting,” Neural Development, vol. 6, article 5, 2011.
[25]
J. Muller, S. Gaunt, and P. A. Lawrence, “Function of the Polycomb protein is conserved in mice and flies,” Development, vol. 121, no. 9, pp. 2847–2852, 1995.
[26]
J. C. Eissenberg, M. Wong, and J. C. Chrivia, “Human SRCAP and Drosophila melanogaster DOM are homologs that function in the Notch signaling pathway,” Molecular and Cellular Biology, vol. 25, no. 15, pp. 6559–6569, 2005.
[27]
A. Bird, “DNA methylation patterns and epigenetic memory,” Genes and Development, vol. 16, no. 1, pp. 6–21, 2002.
[28]
B. H. Ramsahoye, D. Biniszkiewicz, F. Lyko, V. Clark, A. P. Bird, and R. Jaenisch, “Non-CpG methylation is prevalent in embryonic stem cells and may be mediated by DNA methyltransferase 3a,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 10, pp. 5237–5242, 2000.
[29]
T. R. Haines, D. I. Rodenhiser, and P. J. Ainsworth, “Allele-specific non-CpG methylation of the Nf1 gene during early mouse development,” Developmental Biology, vol. 240, no. 2, pp. 585–598, 2001.
[30]
S. W. L. Chan, I. R. Henderson, and S. E. Jacobsen, “Gardening the genome: DNA methylation in Arabidopsis thaliana,” Nature Reviews Genetics, vol. 6, no. 5, pp. 351–360, 2005.
[31]
F. Lyko, B. H. Ramsahoye, and R. Jaenisch, “DNA methylation in Drosophila melanogaster,” Nature, vol. 408, no. 6812, pp. 538–540, 2000.
[32]
L. M. Field, F. Lyko, M. Mandrioli, and G. Prantera, “DNA methylation in insects,” Insect Molecular Biology, vol. 13, no. 2, pp. 109–115, 2004.
[33]
Y. Gruenbaum, R. Naveh-Many, H. Cedar, and A. Razin, “Sequence specificity of methylation in higher plant DNA,” Nature, vol. 292, no. 5826, pp. 860–862, 1981.
[34]
F. Fuks, “DNA methylation and histone modifications: teaming up to silence genes,” Current Opinion in Genetics and Development, vol. 15, no. 5, pp. 490–495, 2005.
[35]
T. Vaissière, C. Sawan, and Z. Herceg, “Epigenetic interplay between histone modifications and DNA methylation in gene silencing,” Mutation Research, vol. 659, no. 1-2, pp. 40–48, 2008.
[36]
A. Kloc, M. Zaratiegui, E. Nora, and R. Martienssen, “RNA interference guides histone modification during the S phase of chromosomal replication,” Current Biology, vol. 18, no. 7, pp. 490–495, 2008.
[37]
M. Zaratiegui, D. V. Irvine, and R. A. Martienssen, “Noncoding RNAs and gene silencing,” Cell, vol. 128, no. 4, pp. 763–776, 2007.
[38]
E. Bernstein and C. D. Allis, “RNA meets chromatin,” Genes and Development, vol. 19, no. 14, pp. 1635–1655, 2005.
[39]
J. I. Martín-Subero and M. Esteller, “Profiling epigenetic alterations in disease,” Advances in Experimental Medicine and Biology, vol. 711, pp. 162–177, 2011.
[40]
S. Sharma, T. K. Kelly, and P. A. Jones, “Epigenetics in cancer,” Carcinogenesis, vol. 31, no. 1, pp. 27–36, 2009.
[41]
R. J. Scott and M. Spielman, “Deeper into the maize: new insights into genomic imprinting in plants,” BioEssays, vol. 28, no. 12, pp. 1167–1171, 2006.
[42]
M. Alleman and J. Doctor, “Genomic imprinting in plants: observations and evolutionary implications,” Plant Molecular Biology, vol. 43, no. 2-3, pp. 147–161, 2000.
[43]
S. Khosla, G. Mendiratta, and V. Brahmachari, “Genomic imprinting in the mealybugs,” Cytogenetic and Genome Research, vol. 113, no. 1–4, pp. 41–52, 2006.
[44]
V. Lloyd, “Parental imprinting in Drosophila,” Genetica, vol. 109, no. 1-2, pp. 35–44, 2000.
[45]
C. J. Bean, C. E. Schaner, and W. G. Kelly, “Meiotic pairing and imprinted X chromatin assembly in Caenorhabditis elegans,” Nature Genetics, vol. 36, no. 1, pp. 100–105, 2004.
[46]
C. C. Martin and R. McGowan, “Genotype-specific modifiers of transgene methylation and expression in the zebrafish, Danio rerio,” Genetical Research, vol. 65, no. 1, pp. 21–28, 1995.
[47]
I. M. Morison, J. P. Ramsay, and H. G. Spencer, “A census of mammalian imprinting,” Trends in Genetics, vol. 21, no. 8, pp. 457–465, 2005.
[48]
A. J. Wood and R. J. Oakey, “Genomic imprinting in mammals: emerging themes and established theories,” PLoS genetics, vol. 2, no. 11, article e147, 2006.
[49]
V. L. Chandler and M. Stam, “Chromatin conversations: mechanisms and implications of paramutation,” Nature Reviews Genetics, vol. 5, no. 7, pp. 532–544, 2004.
[50]
M. S. Bartolomei, S. Zemel, and S. M. Tilghman, “Parental imprinting of the mouse H19 gene,” Nature, vol. 351, no. 6322, pp. 153–155, 1991.
[51]
T. M. DeChiara, E. J. Robertson, and A. Efstratiadis, “Parental imprinting of the mouse insulin-like growth factor II gene,” Cell, vol. 64, no. 4, pp. 849–859, 1991.
[52]
J. L. Thorvaldsen, K. L. Duran, and M. S. Bartolomei, “Deletion of the H19 differentially methylated domain results in loss of imprinted expression of H19 and Igf2,” Genes and Development, vol. 12, no. 23, pp. 3693–3702, 1998.
[53]
J. F. X. Ainscough, L. Dandolo, and M. Azim Surani, “Appropriate expression of the mouse H19 gene utilises three or more distinct enhancer regions spread over more than 130？kb,” Mechanisms of Development, vol. 91, no. 1-2, pp. 365–368, 2000.
[54]
P. A. Leighton, J. R. Saam, R. S. Ingram, C. L. Stewart, and S. M. Tilghman, “An enhancer deletion affects both H19 and Igf2 expression,” Genes and Development, vol. 9, no. 17, pp. 2079–2089, 1995.
[55]
K. Davies, L. Bowden, P. Smith et al., “Disruption of mesodermal enhancers for Igf2 in the minute mutant,” Development, vol. 129, no. 7, pp. 1657–1668, 2002.
[56]
C. R. Kaffer, M. Srivastava, K. Y. Park et al., “A transcriptional insulator at the imprinted H19/Igf2 locus,” Genes and Development, vol. 14, no. 15, pp. 1908–1919, 2000.
[57]
T. Moore, M. Constancia, M. Zubair et al., “Multiple imprinted sense and antisense transcripts, differential methylation and tandem repeats in a putative imprinting control region upstream of mouse Igf2,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 23, pp. 12509–12514, 1997.
[58]
M. Constancia, W. Dean, S. Lopes, T. Moore, G. Kelsey, and W. Reik, “Deletion of a silencer element in Igf2 results in loss of imprinting independent of H19,” Nature Genetics, vol. 26, no. 2, pp. 203–206, 2000.
[59]
A. Murrell, S. Heeson, L. Bowden et al., “An intragenic methylated region in the imprinted Igf2 gene augments transcription,” EMBO Reports, vol. 2, no. 12, pp. 1101–1106, 2001.
[60]
S. Eden, M. Constancia, T. Hashimshony et al., “An upstream repressor element plays a role in Igf2 imprinting,” The EMBO Journal, vol. 20, no. 13, pp. 3518–3525, 2001.
[61]
T. Koide, J. Ainscough, M. Wijgerde, and M. A. Surani, “Comparative analysis of Igf-2/H19 imprinted domain: identification of a highly conserved intergenic DNase I hypersensitive region,” Genomics, vol. 24, no. 1, pp. 1–8, 1994.
[62]
J. F. X. Ainscough, R. M. John, S. C. Barton, and M. Azim Surani, “A skeletal muscle-specific mouse Igf2 repressor lies 40 kb downstream of the gene,” Development, vol. 127, no. 18, pp. 3923–3930, 2000.
[63]
B. K. Jones, J. Levorse, and S. M. Tilghman, “Deletion of a nuclease-sensitive region between the Igf2 and H19 genes leads to Igf2 misregulation and increased adiposity,” Human Molecular Genetics, vol. 10, no. 8, pp. 807–814, 2001.
[64]
H. Moon, G. Filippova, D. Loukinov et al., “CTCF is conserved from Drosophila to humans and confers enhancer blocking of the Fab-8 insulator,” EMBO Reports, vol. 6, no. 2, pp. 165–170, 2005.
[65]
W. A. MacDonald, D. Menon, N. J. Bartlett et al., “The Drosophila homolog of the mammalian imprint regulator, CTCF, maintains the maternal genomic imprint in Drosophila melanogaster,” BMC Biology, vol. 8, article 105, 2010.
[66]
A. T. Hark, C. J. Schoenherr, D. J. Katz, R. S. Ingram, J. M. Levorse, and S. M. Tilghman, “CTCF mediates methylation-sensitive enhancer-blocking activity at the H19/Igf2 locus,” Nature, vol. 405, no. 6785, pp. 486–489, 2000.
[67]
A. C. Bell and G. Felsenfeld, “Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene,” Nature, vol. 405, no. 6785, pp. 482–485, 2000.
[68]
K. D. Tremblay, J. R. Saam, R. S. Ingram, S. M. Tilghman, and M. S. Bartolomei, “A paternal-specific methylation imprint marks the alleles of the mouse H19 gene,” Nature Genetics, vol. 9, no. 4, pp. 407–413, 1995.
[69]
S. Kurukuti, V. K. Tiwari, G. Tavoosidana et al., “CTCF binding at the H19 imprinting control region mediates maternally inherited higher-order chromatin conformation to restrict enhancer access to Igf2,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 28, pp. 10684–10689, 2006.
[70]
A. Murrell, S. Heeson, and W. Reik, “Interaction between differentially methylated regions partitions the imprinted genes Igf2 and H19 into parent-specific chromatin loops,” Nature Genetics, vol. 36, no. 8, pp. 889–893, 2004.
[71]
S. Y. Young, S. Jeong, Q. Rong, K. Y. Park, J. H. Chung, and K. Pfeifer, “Analysis of the H19ICR insulator,” Molecular and Cellular Biology, vol. 27, no. 9, pp. 3499–3510, 2007.
[72]
T. Li, J. F. Hu, X. Qiu et al., “CTCF regulates allelic expression of Igf2 by orchestrating a promoter-polycomb repressive complex 2 intrachromosomal loop,” Molecular and Cellular Biology, vol. 28, no. 20, pp. 6473–6482, 2008.
[73]
L. Han, D. H. Lee, and P. E. Szabó, “CTCF is the master organizer of domain-wide allele-specific chromatin at the H19/Igf2 imprinted region,” Molecular and Cellular Biology, vol. 28, no. 3, pp. 1124–1135, 2008.
[74]
R. I. Verona, J. L. Thorvaldsen, K. J. Reese, and M. S. Bartolomei, “The transcriptional status but not the imprinting control region determines allele-specific histone modifications at the imprinted H19 locus,” Molecular and Cellular Biology, vol. 28, no. 1, pp. 71–82, 2008.
[75]
S. R. Schulze and L. L. Wallrath, “Gene regulation by chromatin structure: paradigms established in Drosophila melanogaster,” Annual Review of Entomology, vol. 52, pp. 171–192, 2007.
[76]
F. Lyko, J. D. Brenton, M. A. Surani, and R. Paro, “An imprinting element from the mouse H19 locus functions as a silencer in Drosophila,” Nature Genetics, vol. 16, no. 2, pp. 171–173, 1997.
[77]
R. A. Drewell, J. D. Brenton, J. F. X. Ainscough et al., “Deletion of a silencer element disrupts H19 imprinting independently of a DNA methylation epigenetic switch,” Development, vol. 127, no. 16, pp. 3419–3428, 2000.
[78]
K. L. Arney, E. Bae, C. Olsen, and R. A. Drewell, “The human and mouse H19 imprinting control regions harbor an evolutionarily conserved silencer element that functions on transgenes in Drosophila,” Development Genes and Evolution, vol. 216, no. 12, pp. 811–819, 2006.
[79]
S. Schoenfelder, G. Smits, P. Fraser, W. Reik, and R. Paro, “Non-coding transcripts in the H19 imprinting control region mediate gene silencing in transgenic Drosophila,” EMBO Reports, vol. 8, no. 11, pp. 1068–1073, 2007.
[80]
D. Umlauf, Y. Goto, R. Cao et al., “Imprinting along the Kcnq1 domain on mouse chromosome 7 involves repressive histone methylation and recruitment of Polycomb group complexes,” Nature Genetics, vol. 36, no. 12, pp. 1296–1300, 2004.
[81]
C. Maison, D. Bailly, A. H. F. M. Peters et al., “Higher-order structure in pericentric heterochromatin involves a distinct pattern of histone modification and an RNA component,” Nature Genetics, vol. 30, no. 3, pp. 329–334, 2002.
[82]
C. Mayer, K. M. Schmitz, J. Li, I. Grummt, and R. Santoro, “Intergenic transcripts regulate the epigenetic state of rRNA genes,” Molecular Cell, vol. 22, no. 3, pp. 351–361, 2006.
[83]
S. Erhardt, F. Lyko, J. F. X. Ainscough, M. A. Surani, and R. Paro, “Polycomb-group proteins are involved in silencing processes caused by a transgenic element from the murine imprinted H19/Igf2 region in Drosophila,” Development Genes and Evolution, vol. 213, no. 7, pp. 336–344, 2003.
[84]
Y. Jinno, K. Sengoku, M. Nakao et al., “Mouse/human sequence divergence in a region with a paternal-specific methylation imprint at the human H19 locus,” Human Molecular Genetics, vol. 5, no. 8, pp. 1155–1161, 1996.
[85]
B. K. Jones, J. Levorse, and S. M. Tilghman, “A human H19 transgene exhibits impaired paternal-specific imprint acquisition and maintenance in mice,” Human Molecular Genetics, vol. 11, no. 4, pp. 411–418, 2002.
[86]
D. R. Dorer and S. Henikoff, “Transgene repeat arrays interact with distant heterochromatin and cause silencing in cis and trans,” Genetics, vol. 147, no. 3, pp. 1181–1190, 1997.
[87]
D. Garrick, S. Fiering, D. I. K. Martin, and E. Whitelaw, “Repeat-induced gene silencing in mammals,” Nature Genetics, vol. 18, no. 1, pp. 56–59, 1998.
[88]
W. J. Haun and N. M. Springer, “Maternal and paternal alleles exhibit differential histone methylation and acetylation at maize imprinted genes,” Plant Journal, vol. 56, no. 6, pp. 903–912, 2008.
[89]
C. Goday and M. F. Ruiz, “Differential acetylation of histones H3 and H4 in paternal and maternal germline chromosomes during development of sciarid flies,” Journal of Cell Science, vol. 115, part 24, pp. 4765–4775, 2002.
[90]
P. G. Greciano and C. Goday, “Methylation of histone H3 at Lys4 differs between paternal and maternal chromosomes in Sciara ocellaris germline development,” Journal of Cell Science, vol. 119, part 22, pp. 4667–4677, 2006.
[91]
V. Joanis and V. Lloyd, “Genomic imprinting in Drosophila is maintained by the products of Suppressor of variegation and trithorax group, but not Polycomb group, genes,” Molecular Genetics and Genomics, vol. 268, no. 1, pp. 103–112, 2002.
[92]
P. E. Jullien, A. Katz, M. Oliva, N. Ohad, and F. Berger, “Polycomb group complexes self-regulate imprinting of the polycomb group gene MEDEA in Arabidopsis,” Current Biology, vol. 16, no. 5, pp. 486–492, 2006.
[93]
C. K？hler, D. R. Page, V. Gagliardini, and U. Grossniklaus, “The Arabidopsis thaliana MEDEA Polycomb group protein controls expression of PHERES1 by parental imprinting,” Nature Genetics, vol. 37, no. 1, pp. 28–30, 2005.
[94]
F. Lyko, K. Buiting, B. Horsthemke, and R. Paro, “Identification of a silencing element in the human 15q11-q13 imprinting center by using transgenic Drosophila,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 4, pp. 1698–1702, 1998.
[95]
B. Kantor, Y. Kaufman, K. Makedonski, A. Razin, and R. Shemer, “Establishing the epigenetic status of the Prader-Willi/Angelman imprinting center in the gametes and embryo,” Human Molecular Genetics, vol. 13, no. 22, pp. 2767–2779, 2004.
[96]
B. Kantor, K. Makedonski, Y. Green-Finberg, R. Shemer, and A. Razin, “Control elements within the PWS/AS imprinting box and their function in the imprinting process,” Human Molecular Genetics, vol. 13, no. 7, pp. 751–762, 2004.
[97]
B. Kantor, R. Shemer, and A. Razin, “The Prader-Willi/Angelman imprinted domain and its control center,” Cytogenetic and Genome Research, vol. 113, no. 1–4, pp. 300–305, 2006.
[98]
Y. Kaufman, M. Heled, J. Perk, A. Razin, and R. Shemer, “Protein-binding elements establish in the oocyte the primary imprint of the Prader-Willi/Angelman syndromes domain,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 25, pp. 10242–10247, 2009.
[99]
T. Arima, K. Yamasaki, R. M. John et al., “The human HYMAI/PLAGL1 differentially methylated region acts as an imprint control region in mice,” Genomics, vol. 88, no. 5, pp. 650–658, 2006.
[100]
V. L. Chandler, J. P. Radicella, T. P. Robbins, J. Chen, and D. Turks, “Two regulatory genes of the maize anthocyanin pathway are homologous: isolation of B utilizing R genomic sequences,” The Plant Cell, vol. 1, no. 12, pp. 1175–1183, 1989.
[101]
E. H. Coe, “The properties, origin, and mechanism of conversion-type inheritance at the B locus in maize,” Genetics, vol. 53, no. 6, pp. 1035–1063, 1966.
[102]
G. I. Patterson, C. J. Thorpe, and V. L. Chandler, “Paramutation, an allelic interaction, is associated with a stable and heritable reduction of transcription of the maize b regulatory gene,” Genetics, vol. 135, no. 3, pp. 881–894, 1993.
[103]
M. Stam, C. Belele, J. E. Dorweiler, and V. L. Chandler, “Differential chromatin structure within a tandem array 100 kb upstream of the maize b1 locus is associated with paramutation,” Genes and Development, vol. 16, no. 15, pp. 1906–1918, 2002.
[104]
M. Haring, R. Bader, M. Louwers, A. Schwabe, R. van Driel, and M. Stam, “The role of DNA methylation, nucleosome occupancy and histone modifications in paramutation,” Plant Journal, vol. 63, no. 3, pp. 366–378, 2010.
[105]
M. Louwers, R. Bader, M. Haring, R. van Driel, W. de Laat, and M. Stam, “Tissue- and expression level-specific chromatin looping at maize b1 epialleles,” Plant Cell, vol. 21, no. 3, pp. 832–842, 2009.
[106]
J. E. Dorweiler, C. C. Carey, K. M. Kubo, J. B. Hollick, J. L. Kermicle, and V. L. Chandler, “Mediator of paramutation 1 is required for establishment and maintenance of paramutation at multiple maize loci,” Plant Cell, vol. 12, no. 11, pp. 2101–2118, 2000.
[107]
M. Alleman, L. Sidorenko, K. McGinnis et al., “An RNA-dependent RNA polymerase is required for paramutation in maize,” Nature, vol. 442, no. 7100, pp. 295–298, 2006.
[108]
L. Sidorenko, J. E. Dorweiler, A. M. Cigan et al., “A dominant mutation in mediator of paramutation2, one of three second-largest subunits of a plant-specific RNA polymerase, disrupts multiple siRNA silencing processes,” PLoS Genetics, vol. 5, no. 11, Article ID e1000725, 2009.
[109]
J. B. Hollick, J. L. Kermicle, and S. E. Parkinson, “Rmr6 maintains meiotic inheritance of paramutant states in Zea mays,” Genetics, vol. 171, no. 2, pp. 725–740, 2005.
[110]
K. F. Erhard Jr., J. L. Stonaker, S. E. Parkinson, J. P. Lim, C. J. Hale, and J. B. Hollick, “RNA polymerase IV functions in paramutation in Zea mays,” Science, vol. 323, no. 5918, pp. 1201–1205, 2009.
[111]
D. Pontier, G. Yahubyan, D. Vega et al., “Reinforcement of silencing at transposons and highly repeated sequences requires the concerted action of two distinct RNA polymerases IV in Arabidopsis,” Genes and Development, vol. 19, no. 17, pp. 2030–2040, 2005.
[112]
A. T. Wierzbicki, J. R. Haag, and C. S. Pikaard, “Noncoding transcription by RNA polymerase Pol IVb/Pol V mediates transcriptional silencing of overlapping and adjacent genes,” Cell, vol. 135, no. 4, pp. 635–648, 2008.
[113]
T. Kanno, B. Huettel, M. F. Mette et al., “Atypical RNA polymerase subunits required for RNA-directed DNA methylation,” Nature Genetics, vol. 37, no. 7, pp. 761–765, 2005.
[114]
A. J. Herr, M. B. Jensen, T. Dalmay, and D. C. Baulcombe, “RNA polymerase IV directs silencing of endogenous DNA,” Science, vol. 308, no. 5718, pp. 118–120, 2005.
[115]
Y. Onodera, J. R. Haag, T. Ream, P. C. Nunes, O. Pontes, and C. S. Pikaard, “Plant nuclear RNA polymerase IV mediates siRNA and DNA methylation-dependent heterochromatin formation,” Cell, vol. 120, no. 5, pp. 613–622, 2005.
[116]
C. S. Pikaard, J. R. Haag, T. Ream, and A. T. Wierzbicki, “Roles of RNA polymerase IV in gene silencing,” Trends in Plant Science, vol. 13, no. 7, pp. 390–397, 2008.
[117]
K. Brzeska, J. Brzeski, J. Smith, and V. L. Chandler, “Transgenic expression of CBBP, a CXC domain protein, establishes paramutation in maize,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 12, pp. 5516–5521, 2010.
[118]
V. L. Chandler, “Paramutation: from maize to mice,” Cell, vol. 128, no. 4, pp. 641–645, 2007.
[119]
M. A. Arteaga-Vazquez and V. L. Chandler, “Paramutation in maize: RNA mediated trans-generational gene silencing,” Current Opinion in Genetics & Gevelopment, vol. 20, no. 2, pp. 156–163, 2010.
[120]
S. W. Chan, X. Zhang, Y. V. Bernatavichute, and S. E. Jacobsen, “Two-step recruitment of RNA-directed DNA methylation to tandem repeats,” PLoS Biology, vol. 4, no. 11, article e363, 2006.
[121]
L. A. McEachern, Inter-kingdom epigenetics: characterization of maize b1 tandem repeat-mediated silencing in Drosophila melanogaster, Ph.D. thesis, Dalhousie University, Halifax, Canada, 2010, http://dalspace.library.dal.ca/handle/10222/13036.
[122]
E. Kurenova, L. Champion, H. Biessmann, and J. M. Mason, “Directional gene silencing induced by a complex subtelomeric satellite from Drosophila,” Chromosoma, vol. 107, no. 5, pp. 311–320, 1998.
[123]
K. A. Haynes, A. A. Caudy, L. Collins, and S. C. R. Elgin, “Element 1360 and RNAi components contribute to HP1-dependent silencing of a pericentric reporter,” Current Biology, vol. 16, no. 22, pp. 2222–2227, 2006.
[124]
F. K. Teixeira and V. Colot, “Repeat elements and the Arabidopsis DNA methylation landscape,” Heredity, vol. 105, no. 1, pp. 14–23, 2010.
[125]
C. M. Suter and D. I. K. Martin, “Paramutation: the tip of an epigenetic iceberg?” Trends in Genetics, vol. 26, no. 1, pp. 9–14, 2010.
