Do plant secondary compounds induce epigenetic changes that confer resistance or susceptibility to toxicosis in animals?

EAAP Scientific Series

Volumn 131, Issue 1, 2012, Pages 33-44

  Welch, K D ^a   Provenza, F D ^b   Pfister, J A ^a  

^a USDA ARS POISONOUS PLANT RESEARCH LABORATORY   (United States)

^b UTAH STATE UNIVERSITY   (United States)

Author keywords

Behaviour; Epigenetics; Genome; Toxins

Indexed keywords

ANIMALIA; RODENTIA;

EID: 84861409880     PISSN: 00712477     EISSN: None     Source Type: Book Series    
DOI: 10.3920/978-90-8686-741-7_3     Document Type: Review

References (100)

1. Allison, M.J., 1978. The role of ruminal microbes in the metabolism of toxic constituents from plants. In: R.F. Keeler, K.R. Van Kampen, and L.F. James (Eds.) Effects of poisonous plants on livestock. Academic Press, New York, USA, pp. 101-118.
2. Anway, M.D., A.S. Cupp, M. Uzumcu and M.K. Skinner, 2005. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 308: 1466-1469.
3. Barker, D.J.P., 2007. The origins of the developmental origins theory. Journal of Internal Medicine 261: 412-417.
4. Bhat T.K., B. Singh, and O.P. Sharma, 1998. Microbial degradation of tannins: a current perspective. Biodegradation 9: 343-357.
5. Biquand, S. and V. Biquand-Guyot, 1992. The influence of peers, lineage and environment on food selection of the criollo goat (Capra hircus). Appl. Anim. Behav. Sci. 34: 231-245.
6. Bossdorf, O., C.L. Richards and M. Pigliucci, 2008. Epigenetics for ecologists. Ecology Letters 11: 106-115.
7. Burke, M.D. and D. G. Upshall, 1976. Species and phenobarbitone-induced differences in the kinetic constants of liver microsomal harmine o-demethylation. Xenobiotica 6: 321-328.
8. Chadwick M.A., P.V. Vercoe, I.H. Williams and D.K. Revell, 2009a. Programming sheep production on saltbrush: adaptations of offspring from ewes that consumed high amounts of salt during pregnancy and early lactation. Anim. Prod. Sci. 49: 311-317.
9. Chadwick M.A., P.V. Vercoe, I.H. Williams and D.K. Revell, 2009b. Dietary exposure of pregnant ewes to salt dictates how their offspring respond to salt. Physiol. Behav. 97: 437-445.
10. Chadwick M.A., P.V. Vercoe, I.H. Williams and D.K. Revell, 2009c. Feeding pregnant ewes a high-salt diet or saltbrush suppresses their offspring's postnatal rennin activity. Animal 3: 972-979.
11. Champagne, F.A., I.C. Weaver, J. Diorio, S. Dymov, M. Szyf and M.J. Meaney, 2006. Maternal care associated with methylation of the estrogen receptor-alpha1b promoter and estrogen receptor-alpha expression in the medial preoptic area of female offspring. Endocrinology 147: 2909-2915.
12. Cheeke, P.R., 1994. A review of the functional an evolutionary roles of the liver in the detoxification of poisonous plants, with special reference to pyrrolizidine alkaloids. Vet. Human Tox. 36: 240-247.
13. Coppersmith, R. and M. Leon, 1984. Enhanced neural response to familiar olfactory cues. Science 225: 849-851.
14. Craig, A.M, C.J. Latham, L.L. Blythe, W.B. Shmotzer, and O.A. O'Connor. 1992. Metabolism of toxic pyrrolizidine alkaloids from tansy ragwort (Senecio jacobaea) in ovine ruminal fluid under anaerobic conditions. Appl. Environ. Microbiol. 58: 2730-2736.
15. Crews, D., A.C. Gore, T.S. Hsu, N.L. Dangleben, M. Spinetta, T. Schallert, M.D. Anway and M.K. Skinner, 2007. Transgenerational epigenetic imprints on mate preference. Proc. Natl. Acad. Sci. USA 104: 5942-5946.
16. Cropley, J.E., C.M. Suter, K.B. Beckman and D.I. Martin. 2006. Germ-line epigenetic modification of the murine Avy allele by nutritional supplementation. Proc. Natl. Acad. Sci. USA 103: 17308-17312.
17. Curtis, K.S., E.G. Krause, D.L. Wong and R.J. Contreras, 2004. Gestational and early postnatal dietary NaCl levels affect NaCl intake, but not stimulated water intake, by adult rats. American Journal of Physiology - Regulatory, Integrative and Comparative Physiology 286: R1043-R1050.
18. Darwin, C., 1859. On the orgins of species. Harvard Univ. Press, Cambridge, MA, USA (reprinted 1964). Darwin, F. (Ed.) 1888. Charles Darwin: life and letters. London, UK: Murray.
19. Dearing, M.D. and S. Cork, 1999. The role of detoxification of plant secondary compounds on diet breadth in mammalian herbivores. Journal of Chemical Ecology 25: 1205-1220.
20. Dearing, M.D., W.J. Foley, and S. McLean. 2005. The influence of plant secondary metabolites on the nutritional ecology of herbivorous terrestrial vertebrates. Annual Rev. Ecol. Syst. 36: 169-189.
21. Delgoda, R. and A.C.G. Westlake, 2004. Herbal interactions involving cytochrome P450 enzymes. Toxicol. Rev. 23: 239-249.
22. Digby, S.N., D.G. Masters, D.Blache, P.I. Hynd and D.K.Revell, 2009. Offspring born to ewes fed high salt during pregnancy have altered responses to oral salt loads. Animal 4: 81-88.
23. Digby, S.N., D. Blache, D.G. Masters and D.K. Revell, 2010. Responses to saline drinking water in offspring born to ewes fed high salt during pregnancy. Small Ruminant Research 91: 87-92.
24. Distel, R.A., J.J. Villalba and H.E. Laborde, 1994. Effects of early experience on voluntary intake of low-quality roughage by sheep. J. Anim. Sci. 72: 1191-1195.
25. Distel, R.A., J.J. Villalba, H.E. Laborde and M.A. Burgos, 1996. Persistence of the effects of early experience on consumption of low-quality roughage by sheep. J. Anim. Sci. 74: 965-968.
26. Distel, R.A. and F.D. Provenza, 1991. Experience early in life affects voluntary intake of blackbrush by goats. J. Chem. Ecol. 17: 431-450.
27. Doidge, N., 2007. The brain that changes itself: stories of personal triumph from the frontiers of brain science. Penguin Books, New York, NY, USA.
28. Dolinoy, D.C., 2008. The agouti mouse model: an epigenetic biosensor for nutritional and environmental alterations on the fetal epigenome. Nutr. Rev. 66 Suppl 1: S7-11.
29. Dolinoy, D.C., D. Huang, and R.L. Jirtle, 2007. Maternal nutrient supplementation counteracts bisphenol A-induced DNA hypomethylation in early development. Proc. Natl. Acad. Sci. USA 104: 13056-13061.
30. Dolinoy, D.C., J.R. Weidman, R.A. Waterland and R.L. Jirtle, 2006. Maternal genistein alters coat color and protects Avy mouse offspring from obesity by modifying the fetal epigenome. Environ. Health Perspect. 114: 567-572.
31. Dufty, A.M. Jr., J. Clobert, and A.P. Moller, 2002. Hormones, developmental plasticity and adaptation. Trends Ecol. Evol. 17: 190-196.
32. Duhl, D.M., H. Vrieling, K.A. Miller, G.L. Wolff and G.S. Barsh, 1994. Neomorphic agouti mutations in obese yellow mice. Nat. Genet. 8: 59-65.
33. Eichelbaum, M., M. Ingelman-Sundberg and W.E. Evans, 2006. Pharmacogenomics and individualized drug therapy. Annu. Rev. Med. 57: 119-137.
34. Esteller, M., 2007. Cancer epigenomics: DNA methylomes and histone-modification maps. Nat. Rev. Genet. 8: 286-298.
35. Fischle, W., Y. Wang and C.D. Allis, 2003. Histone and chromatin cross-talk. Curr. Opin. Cell Biol. 15: 172-183.
36. Fraga, M.F., E. Ballestar, M.F. Paz, S. Ropero, F. Setien, M. L. Ballestar, D. Heine-Suner, J. C. Cigudosa, M. Urioste, J. Benitez, M. Boix-Chornet, A. Sanchez-Aguilera, C. Ling, E. Carlsson, P. Poulsen, A. Vaag, Z. Stephan, T.D. Spector, Y.Z. Wu, C. Plass and M. Esteller, 2005. Epigenetic differences arise during the lifetime of monozygotic twins. Proc. Natl. Acad. Sci. USA 102: 10604-10609.
37. Fonne-Pfister, R. and U.A. Meyer, 1988. Xenobiotic and endobiotic inhibitors of cytochrome P-450dbl function, the target of the debrisoquine/sparteine type polymorphism. Biochem Pharmacol 37: 3829-3835.
38. Foley, J.W., G.R. Iason and C. McArthur, 1999. Role of plant secondary metabolites in the nutritional ecology of mammalian herbivores: how far have we come in 25 years? In: Nutritional Ecology of Herbivores, H.G. Jung and G.C. Fahey (Eds.), American Society of Animal Science, Savoy, IL, USA, pp. 130209.
39. Forrester L.M., G.E. Neal, D.J. Judah, M.J. Glancey and C.R. Wolf, 1990. Evidence for involvement of multiple forms of cytochrome P-450 in aflatoxin B1 metabolism in human liver. Proc. Nat. Acad. Sci. USA 87: 8306-8310.
40. Gregg, C., J. Zhang, B. Weissbourd, S. Luo, G.P. Schroth, D. Haig and C. Dulac, 2010b. High-resolution analysis of parent-of-origin allelic expression in the mouse brain. Science 329: 643-648.
41. Gregg, C., J. Zhang, J.E. Butler, D. Haig, and C. Dulac, 2010a. Sex-specific parent-of-origin allelic expression in the mouse brain. Science 329: 682-685.
42. Green, G.C., R.L. Elwin, B.E. Mottershead and J.J. Lynch, 1984. Long-term effects of early experience to supplementary feeding in sheep. Proc. Aust. Soc. Anim. Prod. 15: 373-375.
43. Guo, L., N. Mei, W. Liao, P.C. Chan and P.P. Fu, 2010. Ginkgo biloba extract induces gene expression changes in xenobiotics metabolism and the Myc-centered network. OMICS 14: 75-90.
44. Haig, D., 2004. Genomic imprinting and kinship: how good is the evidence? Annual Review of Genetics 38: 553-585.
45. Haig, D. and C. Graham, 1991. Genomic imprinting and the strange case of the insulin-like growth-factor II receptor, Cell 64: 1045-1046.
46. Hales, C.N. and D.J.P. Barker, 2001. The thrifty phenotype hypothesis. Brit. Med. Bull. 60: 5-20.
47. Hedman, R. and H. Pettersson, 1997. Transformation of nivalenol by gastrointestinal microbes. Arch Anim. Nutr. 50: 321-329.
48. Holliday, R. and J.E. Pugh, 1975. DNA modification mechanisms and gene activity during development. Science 187: 226-232.
49. Howery, L.D., F.D. Provenza, R.E. Banner and C.B. Scott, 1998. Social and environmental factors influence cattle distribution on rangeland. Appl. Anim. Behav. Sci. 55: 231-244.
50. Hulshoff Pol, H.E., H.W. Hoek, E. Susser, A.S. Brown, A. Dingemans, H.G. Schnack, N.E. van Haren, L.M. Pereira Ramos, C.C. Gispen-de Wied and R.S. Kahn, 2000. Prenatal exposure to famine and brain morphology in schizophrenia. American Journal of Psychiatry 157: 1170-1172.
51. Huw Jones, R. and S.E. Ozanne, 2009. Fetal programming of glucose-insulin metabolism. Molecular and Cellular Endocrinology 297: 4-9.
52. Ingelman-Sundberg, M., 2005. Genetic polymorphisms of cytochrome P450 2D6 (CYP2D6): clinical consequences, evolutionary aspects and functional diversity. The Pharmacogenomics Journal 5: 6-13.
53. Ingelman-Sundberg, M., S.C. Sim, A. Gomez and C. Rodriguez-Antona, 2007. Influence of cytochrome P450 polymorphisms on drug therapies: pharmacogenetic, pharmacoepigenetic and clinical aspects. Pharmacol. Ther. 116: 496-526.
54. Jessop, N.S. and A.W. Illius, 1997. Modeling animal responses to plant toxicants. In: J.P.F. D'Mello (Ed.) Handbook of plant and fungal toxicants. CRC Press, Boca Raton, Fl, USA, pp. 243-253.
55. Jirtle, R.L. and M.K. Skinner, 2007. Environmental epigenomics and disease susceptibility. Nat. Rev. Genet. 8: 253-262.
56. LeDoux, J., 2002. Synaptic self: how our brains become who we are. Viking Penguin, New York, USA.
57. Lumey, L.H. and A.D. Stein, 1997. Offspring birth weights after maternal intrauterine undernutrition: a comparison within sibships. Am. J. Epidemiol. 146: 810-819.
58. Magnanou, E., J.R. Malenke and M.D. Dearing, 2009. Expression of biotransformation genes in woodrat (Neotoma) herbivores on novel and ancestral diets: identification of candidate genes responsible for dietary shifts. Molecular Ecology 18: 2401-2414.
59. Martin-Gronert, M.S. and S.E. Ozanne, 2006. Maternal nutrition during pregnancy and health of the offspring. Biochemical Society Transactions 34: 779-782.
60. Miranda, C.L., P.R. Cheeke, and D.R. Buhler, 1980. Effect of pyrrolizidine alkaloids from tansy ragwort (Senecio jacobaea) on hepatic drug-metabolizing enzymes in male rats. Biochem. Pharmacol. 29: 2645-2649.
61. Mirza, S.N. and F.D. Provenza, 1990. Preference of the mother affects selection and avoidance of foods by lambs differing in age. Appl. Anim. Behav. Sci. 28: 255-263.
62. Mirza, S.N. and F.D. Provenza, 1992. Effects of age and conditions of exposure on maternally mediated food selection in lambs. Appl. Anim. Behav. Sci. 33: 35-42.
63. Ngo, S.N.T., R.A. Mckinnon and I. Stupans, 2003. The effects of Eucalyptus terpenes on hepatic cytochrome P450 CYP4A, peroxisomal Acyl CoA oxidase (AOX) and peroxisome proliferator activated receptor alpha (PPARalpha) in the common brush tail possum (Trichosurus vulpecula). Comp. Biochem. Physiol. C 136: 165-173.
64. Nolte, D.L., F.D. Provenza, R. Callan and K.E. Panter, 1992a. Garlic in the ovine fetal environment. Physiol. Behav. 52: 1091-1093.
65. Nolte, D.L. and F.D. Provenza, 1992b. Food preferences in lambs after exposure to flavors in milk. Appl. Anim. Behav. Sci. 32: 381-389.
66. Nolte, D.L. and F.D. Provenza, 1992c. Food preferences in lambs after exposure to flavors in solid foods. Appl. Anim. Behav. Sci. 32: 337-347.
67. Ortega Reyes, L., F.D. Provenza, C.F. Parker and P.G. Hatfield, 1992. Drylot performance and ruminal papillae development of lambs exposed to a high concentrate diet while nursing. Small Rum. Res. 7: 101-112.
68. Paul, A.M., 2010. How the nine months before birth shape the rest of our lives. Free Press, New York, USA.
69. Pembrey, M., 1996. Imprinting and transgenerational modulation of gene expression; human growth as a model. Acta Genet. Med. Gemellol. (Roma.) 45: 111-125.
70. Provenza, F.D., 1995a. Tracking variable environments: there is more than one kind of memory. J. Chem. Ecol. 21: 911-923.
71. Provenza, F.D., 1995b. Postingestive feedback as an elementary determinant of food preference and intake in ruminants. J. Range Manage. 48: 2-17.
72. Provenza, F.D., 2003. Foraging behavior: managing to survive in a world of change. Utah State Univ., Logan, USA.
73. Provenza, F.D., 2008. What does it mean to be locally adapted and who cares anyway? J. Anim. Sci. 86: E271-E284.
74. Provenza, F.D. and J.J. Villalba, 2006. Foraging in domestic vertebrates: linking the internal and external milieu. In: V.L. Bels (Ed.) Feeding in domestic vertebrates: from structure to function. CABI Publ., Oxford, UK, pp. 210-240.
75. Quintana, P.J.E., T. Dodd-Butera, C. Shaputnic, M. Ramirez-Zetina, A.C. Batista and M. Mercedes Sierra, 2004. Interindividual variation in levels of the detoxifying enzyme glutathione S-transferase pi (GSTP1) in placentas from a Mexican population. Journal of Children's Health 2: 41-51.
76. Roseboom, T., S. De Rooij and R. Painter, 2006. The Dutch famine and its long-term consequences for adult health. Early Human Development 82: 485-491.
77. Schlichting, C.D. and M. Pigliucci, 1998. Phenotypic evolution: a reaction norm perspective. Sinauer Publications, Sinauer, MA, USA.
78. Schuetz, E.G., K.N. Furuya and J. D. Schuetz, 1995. Interindividual variation in expression of P-glycoprotein in normal human liver and secondary hepatic neoplasms. J. Pharmacol. Exp. Ther. 275: 1011-1018.
79. Scrimshaw N.S., 1996. Nutrition and health from womb to tomb. Nutrition Today 31(2): 55-67.
80. Simitzis, P.E., S.G. Deligeorgis, J.A. Bizelis and K. Fegeros, 2008. Feeding preferences in lambs influenced by prenatal flavour exposure. Physiol. Behav. 93: 529-536.
81. Skinner, M.K. and C. Guerrero-Bosagna, 2009. Environmental signals and transgenerational epigenetics. Epigenomics 1: 111-117.
82. Skinner, M.K., M. Manikkam, and C. Guerrero-Bosagna, 2010. Epigenetic transgenerational actions of environmental factors in disease etiology. Trends Endocrinol. Metab 21: 214-222.
83. Sorensen, J.S. and M.D. Dearing, 2003. Elimination rates of specialist and generalist woodrats dosed with alphapinene. Oecologia 134: 88-94.
84. Sorensen, J.S. and M.D. Dearing, 2006. Efflux transporters as a novel herbivore countermechanism to plant chemical defenses. Journal of Chemical Ecology 32: 1181-1196.
85. Sorensen, J.S., C.A. Turnbull and M.D. Dearing, 2004a. A specialist herbivore (Neotoma stephensi) absorbs fewer plant toxins than a generalist (Neotoma albigula). Physiol. Biochem. Zool. 77: 139-148.
86. Sorensen, J.S., C. A. Turnbull and M. D. Dearing, 2004b. Absorption of toxins in specialist and generalist woodrats (Neotoma spp). Physiological Biochemistry and Zoology. 77: 305-312.
87. Squibb, R.C., F.D. Provenza and D.F. Balph, 1990. Effect of age of exposure on consumption of a shrub by sheep. J. Anim. Sci. 68: 987-997.
88. St. Clair, D., M. Xu, P. Wang, Y. Yu, Y. Fang, F. Zhang, X. Zheng, N. Gu, G. Feng, P. Sham, and L. He, 2005. Rates of adult schizophrenia following prenatal exposure to the Chinese famine of 1959-1961. Journal of the American Medical Association 294: 557-562.
89. Szyf, M., 2007. The dynamic epigenome and its implications in toxicology. Toxicol. Sci. 100: 7-23.
90. Tarry-Adkins, J.L., M. S. Martin-Gronert, J.-H. Chen, R.L. Cripps and S.E. Ozanne, 2008. Maternal diet influences DNA damage, aortic telomere length, oxidative stress, and antioxidant defense capacity in rats. FASEB J. 22: 2037-2044.
91. Thorhallsdottir, A.G., F.D. Provenza and D.F. Balph, 1990. Ability of lambs to learn about novel foods while observing or participating with social models. Appl. Anim. Behav. Sci. 25: 25-33.
92. Tzack, A.G., E.D. Ungar, S.Y. Landau, A. Perevolotsky, H. Muklada and J.W. Walker, 2009. Breed and maternal effects on the intake of tannin-rich browse by juvenile goats (Capra hircus). Appl. Anim. Behav. Sci. 119: 71-77.
93. Turner, A.M. and K.V. Morris, 2010. Controlling transcription with noncoding RNAs in mammalian cells. Biotechniques 48: ix-xvi.
94. Wade, M.J., 1998. The evolutionary genetics of maternal effects. In: T.A. Mousseau and C.W. Fox (Eds.) Maternal effects as adaptations. Oxford Univ. Press, New York, NY, USA, pp. 5-21.
95. Waterland, R.A., J. Lin, C.A. Smith and R.L. Jirtle, 2006. Post-weaning diets affects genomic imprinting at the insulinlike growth factor 2 (Igf2) locus. Human Molecular Genetics 15: 705-716.
96. Weaver, I.C., J. Diorio, J.R. Seckl, M. Szyf and M.J. Meaney, 2004. Early environmental regulation of hippocampal glucocorticoid receptor gene expression: characterization of intracellular mediators and potential genomic target sites. Ann. NY Acad. Sci. 1024: 182-212.
97. Weston, A.D., T.R. Ozolins and N.A. Brown, 2006. Thoracic skeletal defects and cardiac malformations: a common epigenetic link? Birth Defects Res. C. Embryo. Today 78: 354-370.
98. Wiedmeier, R.D., F.D. Provenza and E.A. Burritt, 2002. Exposure to ammoniated wheat straw as suckling calves improves performance of mature beef cows wintered on ammoniated wheat straw. J. Anim. Sci. 80: 2340-2348.
99. Wilkinson, L.S., 2010. Which parental gene gets the upper hand? Science 329: 636-637.
100. Wilkinson, L.S., W. Davies and A.R. Isles, 2007. Genomic imprinting effects on brain development and function. Nature Reviews Neuroscience 8: 832-843.