Breeding scheme and maternal small RNAs affect the efficiency of transgenerational inheritance of a paramutation in mice

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Yuan, Shuiqiao ^a   Oliver, Daniel ^a   Schuster, Andrew ^a   Zheng, Huili ^a   Yan, Wei ^a,b  

^a UNIVERSITY OF NEVADA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NEVADA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; SMALL INTERFERING RNA; STEM CELL FACTOR RECEPTOR;

ALLELE; ANIMAL; BREEDING; C57BL MOUSE; FEMALE; GENE LOCUS; GENE TARGETING; GENETIC EPIGENESIS; GENETICS; INHERITANCE; MALE; METABOLISM; MOUSE; MUTATION; PHENOTYPE;

ALLELES; ANIMALS; BREEDING; EPIGENESIS, GENETIC; FEMALE; GENE KNOCK-IN TECHNIQUES; GENETIC LOCI; INHERITANCE PATTERNS; MALE; MICE; MICE, INBRED C57BL; MICRORNAS; MUTATION; PHENOTYPE; PROTO-ONCOGENE PROTEINS C-KIT; RNA, SMALL INTERFERING;

EID: 84925610182     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep09266     Document Type: Article

References (45)

1. Guerrero-Bosagna, C. & Skinner, M. K. Environmentally induced epigenetic transgenerational inheritance of male infertility. Current opinion in genetics & development 26C, 79-88 (2014).
2. Chandler, V. L. Paramutation: from maize to mice. Cell 128, 641-645 (2007).
3. Chandler, V. L. & Stam, M. Chromatin conversations: mechanisms and implications of paramutation. Nature reviews. Genetics 5, 532-544 (2004).
4. Hollick, J. B. Paramutation and development. Annual review of cell and developmental biology 26, 557-579 (2010).
5. Cuzin, F., Grandjean, V. & Rassoulzadegan, M. Inherited variation at the epigenetic level: paramutation from the plant to the mouse. Current opinion in genetics & development 18, 193-196 (2008).
6. Cuzin, F. & Rassoulzadegan, M. Non-Mendelian epigenetic heredity: gametic RNAs as epigenetic regulators and transgenerational signals. Essays in biochemistry 48, 101-106 (2010).
7. Hollick, J. B. Paramutation: a trans-homolog interaction affecting heritable gene regulation. Current opinion in plant biology 15, 536-543 (2012).
8. Brink, R. A. & Williams, E. Mutable R-navajo alleles of cyclic origin in maize. Genetics 73, 273-296 (1973).
9. Brink, R. A. Paramutation. Annual review of genetics 7, 129-152 (1973).
10. Grandjean, V. et al. The miR-124-Sox9 paramutation: RNA-mediated epigenetic control of embryonic and adult growth. Development 136, 3647-3655 (2009).
11. Wagner, K. D. et al. RNA induction and inheritance of epigenetic cardiac hypertrophy in the mouse. Developmental cell 14, 962-969 (2008).
12. Rassoulzadegan, M. et al. RNA-mediated non-mendelian inheritance of an epigenetic change in the mouse. Nature 441, 469-474 (2006).
13. Kiani, J. et al. RNA-mediated epigenetic heredity requires the cytosine methyltransferase Dnmt2. PLoS genetics 9, e1003498 (2013).
14. Adams, I. R. & Meehan, R. R. From paramutation to paradigm. PLoS genetics 9, e1003537 (2013).
15. Jirtle, R. L. & Skinner, M. K. Environmental epigenomics and disease susceptibility. Nature reviews. Genetics 8, 253-262 (2007).
16. Crews, D., Gillette, R., Miller-Crews, I., Gore, A. C. & Skinner, M. K. Nature, nurture and epigenetics. Molecular and cellular endocrinology (2014).
17. Nilsson, E. E. & Skinner, M. K. Environmentally induced epigenetic transgenerational inheritance of disease susceptibility. Translational research: the journal of laboratory and clinical medicine (2014).
18. Skinner, M. K. Endocrine disruptor induction of epigenetic transgenerational inheritance of disease. Molecular and cellular endocrinology (2014).
19. Anway, M. D., Cupp, A. S., Uzumcu, M. & Skinner, M. K. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 308, 1466-1469 (2005).
20. Manikkam, M., Tracey, R., Guerrero-Bosagna, C. & Skinner, M. K. Plastics derived endocrine disruptors (BPA, DEHP and DBP) induce epigenetic transgenerational inheritance of obesity, reproductive disease and sperm epimutations. PloS one 8, e55387 (2013).
21. Manikkam, M., Haque, M. M., Guerrero-Bosagna, C., Nilsson, E. E. & Skinner, M. K. Pesticide Methoxychlor Promotes the Epigenetic Transgenerational Inheritance of Adult-Onset Disease through the Female Germline. PloS one 9, e102091 (2014).
22. Manikkam, M., Tracey, R., Guerrero-Bosagna, C. & Skinner, M. K. Dioxin (TCDD) induces epigenetic transgenerational inheritance of adult onset disease and sperm epimutations. PloS one 7, e46249 (2012).
23. Doyle, T. J., Bowman, J. L., Windell, V. L., McLean, D. J. & Kim, K. H. Transgenerational effects of di-(2-ethylhexyl) phthalate on testicular germ cell associations and spermatogonial stem cells in mice. Biology of reproduction 88, 112 (2013).
24. Skinner, M. K. et al. Ancestral dichlorodiphenyltrichloroethane (DDT) exposure promotes epigenetic transgenerational inheritance of obesity. BMC medicine 11, 228 (2013).
25. Tracey, R., Manikkam, M., Guerrero-Bosagna, C. & Skinner, M. K. Hydrocarbons (jet fuel JP-8) induce epigenetic transgenerational inheritance of obesity, reproductive disease and sperm epimutations. Reproductive toxicology 36, 104-116 (2013).
26. Rechavi, O. et al. Starvation-Induced Transgenerational Inheritance of Small RNAs in C. elegans. Cell 158, 277-287 (2014).
27. Niculescu, M. D. Nutritional epigenetics. ILAR journal/National Research Council, Institute of Laboratory Animal Resources 53, 270-278 (2012).
28. Waterland, R. A., Travisano, M. & Tahiliani, K. G. Diet-induced hypermethylation at agouti viable yellow is not inherited transgenerationally through the female. FASEB journal: official publication of the Federation of American Societies for Experimental Biology 21, 3380-3385 (2007).
29. McCarrey, J. R. Distinctions between transgenerational and nontransgenerational epimutations. Molecular and cellular endocrinology (2014).
30. Skinner, M. K., Haque, C. G., Nilsson, E., Bhandari, R. & McCarrey, J. R. Environmentally induced transgenerational epigenetic reprogramming of primordial germ cells and the subsequent germ line. PloS one 8, e66318 (2013).
31. Ro, S. et al. A model to study the phenotypic changes of interstitial cells of Cajal in gastrointestinal diseases. Gastroenterology 138, 1068-1078, e1061-1062 (2010).
32. Arnheiter, H. Mammalian paramutation: a tail's tale? Pigment cell research/ sponsored by the European Society for Pigment Cell Research and the International Pigment Cell Society 20, 36-40 (2007).
33. Clark, B. S. & Blackshaw, S. Long non-coding RNA-dependent transcriptional regulation in neuronal development and disease. Frontiers in genetics 5, 164 (2014).
34. Sun, M. & Kraus, W. L. Minireview: Long noncoding RNAs: new "links" between gene expression and cellular outcomes in endocrinology. Molecular endocrinology 27, 1390-1402 (2013).
35. Casas, E. & Vavouri, T. Sperm epigenomics: challenges and opportunities. Frontiers in genetics 5, 330 (2014).
36. Kohli, R. M. & Zhang, Y. TET enzymes, TDG and the dynamics of DNA demethylation. Nature 502, 472-479 (2013).
37. Yuan, S., Ortogero, N., Wu, Q., Zheng, H. & Yan, W. Murine Follicular Development Requires Oocyte DICER, but Not DROSHA. Biology of reproduction 91(2):39 (2014).
38. Frost, R. J. et al. MOV10L1 is necessary for protection of spermatocytes against retrotransposons by Piwi-interacting RNAs. Proceedings of the National Academy of Sciences of the United States of America 107, 11847-11852 (2010).
39. Zheng, K. et al.Mouse MOV10L1 associates with Piwi proteins and is an essential component of the Piwi-interacting RNA (piRNA) pathway. Proceedings of the National Academy of Sciences of the United States of America 107, 11841-11846 (2010).
40. Klein, S. et al. Interstitial cells of Cajal integrate excitatory and inhibitory neurotransmission with intestinal slow-wave activity. Nature communications 4, 1630 (2013).
41. Bao, J. & Yan, W. Male germline control of transposable elements. Biology of reproduction 86, 162, 161-114 (2012).
42. Wu, Q. et al. The RNase III enzyme DROSHA is essential for microRNA production and spermatogenesis. The Journal of biological chemistry 287, 25173-25190 (2012).
43. Korhonen, H. M. et al. Dicer is required for haploid male germ cell differentiation in mice. PloS one 6, e24821 (2011).
44. Hayashi, K. et al.MicroRNA biogenesis is required for mouse primordial germ cell development and spermatogenesis. PloS one 3, e1738 (2008).
45. Bao, J., Ma, H. Y., Schuster, A., Lin, Y. M. & Yan, W. Incomplete cre-mediated excision leads to phenotypic differences between Stra8-iCre; Mov10l1(lox/lox) and Stra8-iCre; Mov10l1(lox/Delta) mice. Genesis 51, 481-490 (2013).