Gene bionetworks involved in the epigenetic transgenerational inheritance of altered mate preference: environmental epigenetics and evolutionary biology

详细信息    查看全文

• 作者：Michael K Skinner (1)
  Marina I Savenkova (1)
  Bin Zhang (2)
  Andrea C Gore (3)
  David Crews (4)
  
  1. Center for Reproductive Biology ; School of Biological Sciences ; Washington State University ; Pullman ; WA ; 99164-4236 ; USA
  2. Department of Genetics & Genomic Sciences ; Institute of Genomics and Multiscale Biology ; Mount Sinai School of Medicine ; New York ; NY ; 10029 ; USA
  3. Pharmacology and Toxicology ; Austin ; Texas
  4. Section of Integrative Biology ; University of Texas at Austin ; Austin ; TX ; 78712 ; USA
  
• 关键词：Epigenetics ; Brain ; Networks ; Evolution ; Behavior
• 刊名：BMC Genomics
• 出版年：2014
• 出版时间：December 2014
• 年：2014
• 卷：15
• 期：1
• 全文大小：1,517 KB
• 参考文献：1. Charlesworth, B, Charlesworth, D (2009) Darwin and genetics. Genetics 183: pp. 757-766 CrossRef
  2. Stein, RA (2012) Epigenetics and environmental exposures. J Epidemiol Community Health 66: pp. 8-13 CrossRef
  3. Kalinowski, ST (2002) Evolutionary and statistical properties of three genetic distances. Mol Ecol 11: pp. 1263-1273 CrossRef
  4. Wilkins, AS (2007) Genetic networks as transmitting and amplifying devices for natural genetic tinkering. Novartis Found Symp 284: pp. 71-86 CrossRef
  5. Jirtle, RL, Skinner, MK (2007) Environmental epigenomics and disease susceptibility. Nat Rev Genet 8: pp. 253-262 CrossRef
  6. Crews, D, McLachlan, JA (2006) Epigenetics, evolution, endocrine disruption, health, and disease. Endocrinology 147: pp. S4-S10 CrossRef
  7. Damiani, G (2007) The Yin and Yang of anti-Darwinian epigenetics and Darwinian genetics. Riv Biol 100: pp. 361-402
  8. Day, T, Bonduriansky, R (2011) A unified approach to the evolutionary consequences of genetic and nongenetic inheritance. Am Nat 178: pp. E18-E36 CrossRef
  9. Kuzawa, CW, Thayer, ZM (2011) Timescales of human adaptation: the role of epigenetic processes. Epigenomics 3: pp. 221-234 CrossRef
  10. Flatscher, R, Frajman, B, Schonswetter, P, Paun, O (2012) Environmental heterogeneity and phenotypic divergence: can heritable epigenetic variation aid speciation?. Genet Res Int 2012: pp. 698421
  11. Klironomos, FD, Berg, J, Collins, S (2013) How epigenetic mutations can affect genetic evolution: model and mechanism. Bioessays 35: pp. 571-578 CrossRef
  12. Darwin, C (1871) The Descent of Man, and Selection in Relation to Sex. T. Murray, London CrossRef
  13. Anway, MD, Cupp, AS, Uzumcu, M, Skinner, MK (2005) Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 308: pp. 1466-1469 CrossRef
  14. Guerrero-Bosagna, C, Settles, M, Lucker, BJ, Skinner, MK (2010) Epigenetic transgenerational actions of vinclozolin on promoter regions of the sperm epigenome. PLoS One 5: pp. e13100 CrossRef
  15. Skinner, MK, Manikkam, M, Guerrero-Bosagna, C (2010) Epigenetic transgenerational actions of environmental factors in disease etiology. Trends Endocrinol Metab 21: pp. 214-222 CrossRef
  16. Manikkam, M, Guerrero-Bosagna, C, Tracey, R, Haque, MM, Skinner, MK (2012) Transgenerational actions of environmental compounds on reproductive disease and epigenetic biomarkers of ancestral exposures. PLoS One 7: pp. e31901 CrossRef
  17. Skinner, MK, Manikkam, M, Tracey, R, Nilsson, E, Haque, MM, Guerrero-Bosagna, C (2013) Ancestral DDT exposures promote epigenetic transgenerational inheritance of obesity. BMC Med 11: pp. 228 CrossRef
  18. Kelce, WR, Gray, LE, Wilson, EM (1998) Antiandrogens as environmental endocrine disruptors. Reprod Fertil Dev 10: pp. 105-111 CrossRef
  19. Morgan, HD, Santos, F, Green, K, Dean, W, Reik, W (2005) Epigenetic reprogramming in mammals. Hum Mol Genet 14 Spec No 1: pp. R47-R58 CrossRef
  20. Anway, MD, Leathers, C, Skinner, MK (2006) Endocrine disruptor vinclozolin induced epigenetic transgenerational adult-onset disease. Endocrinology 147: pp. 5515-5523 CrossRef
  21. Anway, MD, Skinner, MK (2008) Transgenerational effects of the endocrine disruptor vinclozolin on the prostate transcriptome and adult onset disease. Prostate 68: pp. 517-529 CrossRef
  22. Nilsson, EE, Anway, MD, Stanfield, J, Skinner, MK (2008) Transgenerational epigenetic effects of the endocrine disruptor vinclozolin on pregnancies and female adult onset disease. Reproduction 135: pp. 713-721 CrossRef
  23. Skinner, MK, Anway, MD, Savenkova, MI, Gore, AC, Crews, D (2008) Transgenerational epigenetic programming of the brain transcriptome and anxiety behavior. PLoS One 3: pp. e3745 CrossRef
  24. Anway, MD, Rekow, SS, Skinner, MK (2008) Transgenerational epigenetic programming of the embryonic testis transcriptome. Genomics 91: pp. 30-40 CrossRef
  25. Skinner, MK, Manikkam, M, Haque, MM, Zhang, B, Savenkova, M (2012) Epigenetic transgenerational inheritance of somatic transcriptomes and epigenetic control regions. Genome Biol 13: pp. R91 CrossRef
  26. Crews, D, Gillette, R, Scarpino, SV, Manikkam, M, Savenkova, MI, Skinner, MK (2012) Epigenetic transgenerational inheritance of altered stress responses. Proc Natl Acad Sci USA 109: pp. 9143-9148 CrossRef
  27. Crews, D, Gore, AC, Hsu, TS, Dangleben, NL, Spinetta, M, Schallert, T, Anway, MD, Skinner, MK (2007) Transgenerational epigenetic imprints on mate preference. Proc Natl Acad Sci USA 104: pp. 5942-5946 CrossRef
  28. Friend, SH (2010) The need for precompetitive integrative bionetwork disease model building. Clin Pharmacol Ther 87: pp. 536-539 CrossRef
  29. Schadt, EE, Lamb, J, Yang, X, Zhu, J, Edwards, S, Guhathakurta, D, Sieberts, SK, Monks, S, Reitman, M, Zhang, C, Lum, PY, Leonardson, A, Thieringer, R, Metzger, JM, Yang, L, Castle, J, Zhu, H, Kash, SF, Drake, TA, Sachs, A, Lusis, AJ (2005) An integrative genomics approach to infer causal associations between gene expression and disease. Nat Genet 37: pp. 710-717 CrossRef
  30. Yang, X, Deignan, JL, Qi, H, Zhu, J, Qian, S, Zhong, J, Torosyan, G, Majid, S, Falkard, B, Kleinhanz, RR, Karlsson, J, Castellani, LW, Mumick, S, Wang, K, Xie, T, Coon, M, Zhang, C, Estrada-Smith, D, Farber, CR, Wang, SS, van Nas, A, Ghazalpour, A, Zhang, B, Macneil, DJ, Lamb, JR, Dipple, KM, Reitman, ML, Mehrabian, M, Lum, PY, Schadt, EE (2009) Validation of candidate causal genes for obesity that affect shared metabolic pathways and networks. Nat Genet 41: pp. 415-423 CrossRef
  31. Nilsson, EE, Savenkova, MI, Schindler, R, Zhang, B, Schadt, EE, Skinner, MK (2010) Gene bionetwork analysis of ovarian primordial follicle development. PLoS One 5: pp. e11637 CrossRef
  32. Nilsson, E, Zhang, B, Skinner, MK (2013) Gene bionetworks that regulate ovarian primordial follicle assembly. BMC Genomics 14: pp. 496 CrossRef
  33. Zhu, J, Zhang, B, Smith, EN, Drees, B, Brem, RB, Kruglyak, L, Bumgarner, RE, Schadt, EE (2008) Integrating large-scale functional genomic data to dissect the complexity of yeast regulatory networks. Nat Genet 40: pp. 854-861 CrossRef
  34. Millstein, J, Zhang, B, Zhu, J, Schadt, EE (2009) Disentangling molecular relationships with a causal inference test. BMC Genet 10: pp. 23 CrossRef
  35. Pandey, G, Zhang, B, Chang, AN, Myers, CL, Zhu, J, Kumar, V, Schadt, EE (2010) An integrative multi-network and multi-classifier approach to predict genetic interactions. PLoS Comput Biol 6: pp. e1000928 CrossRef
  36. DiBenedictis, BT, Ingraham, KL, Baum, MJ, Cherry, JA (2012) Disruption of urinary odor preference and lordosis behavior in female mice given lesions of the medial amygdala. Physiol Behav 105: pp. 554-559 CrossRef
  37. Anway, MD, Memon, MA, Uzumcu, M, Skinner, MK (2006) Transgenerational effect of the endocrine disruptor vinclozolin on male spermatogenesis. J Androl 27: pp. 868-879 CrossRef
  38. Ghazalpour, A, Doss, S, Zhang, B, Wang, S, Plaisier, C, Castellanos, R, Brozell, A, Schadt, EE, Drake, TA, Lusis, AJ, Horvath, S (2006) Integrating genetic and network analysis to characterize genes related to mouse weight. PLoS Genet 2: pp. e130 CrossRef
  39. Sakata, JT, Crews, D (2004) Developmental sculpting of social phenotype and plasticity. Neurosci Biobehav Rev 28: pp. 95-112 CrossRef
  40. Skinner, MK (2011) Role of epigenetics in developmental biology and transgenerational inheritance. Birth Defects Res C Embryo Today 93: pp. 51-55 CrossRef
  41. Skinner, MK (2011) Environmental epigenetic transgenerational inheritance and somatic epigenetic mitotic stability. Epigenetics 6: pp. 838-842 CrossRef
  42. Skinner, M, Guerrero-Bosagna, C, Haque, MM, Nilsson, E, Bhandari, R, McCarrey, J (2013) Environmentally induced transgenerational epigenetic reprogramming of primordial germ cells and subsequent germline. PLoS One 8: pp. e66318 CrossRef
  43. Salian, S, Doshi, T, Vanage, G (2009) Impairment in protein expression profile of testicular steroid receptor coregulators in male rat offspring perinatally exposed to Bisphenol A. Life Sci 85: pp. 11-18 CrossRef
  44. Bruner-Tran, KL, Osteen, KG (2011) Developmental exposure to TCDD reduces fertility and negatively affects pregnancy outcomes across multiple generations. Reprod Toxicol 31: pp. 344-350 CrossRef
  45. Waterland, RA, Travisano, M, Tahiliani, KG, Rached, MT, Mirza, S (2008) Methyl donor supplementation prevents transgenerational amplification of obesity. Int J Obes (Lond) 32: pp. 1373-1379 CrossRef
  46. Painter, RC, Osmond, C, Gluckman, P, Hanson, M, Phillips, DI, Roseboom, TJ (2008) Transgenerational effects of prenatal exposure to the Dutch famine on neonatal adiposity and health in later life. BJOG 115: pp. 1243-1249 CrossRef
  47. Pembrey, ME, Bygren, LO, Kaati, G, Edvinsson, S, Northstone, K, Sjostrom, M, Golding, J (2006) Sex-specific, male-line transgenerational responses in humans. Eur J Hum Genet 14: pp. 159-166 CrossRef
  48. Dias, BG, Ressler, KJ (2014) Parental olfactory experience influences behavior and neural structure in subsequent generations. Nat Neurosci 17: pp. 89-96 CrossRef
  49. Buck, LB (2004) Olfactory receptors and odor coding in mammals. Nutr Rev 62: pp. S184-S188 CrossRef
  50. Brennan, PA, Zufall, F (2006) Pheromonal communication in vertebrates. Nature 444: pp. 308-315 CrossRef
  51. Dulac, C, Wagner, S (2006) Genetic analysis of brain circuits underlying pheromone signaling. Annu Rev Genet 40: pp. 449-467 CrossRef
  52. Green, RE, Krause, J, Briggs, AW, Maricic, T, Stenzel, U, Kircher, M, Patterson, N, Li, H, Zhai, W, Fritz, MH, Hansen, NF, Durand, EY, Malaspinas, AS, Jensen, JD, Marques-Bonet, T, Alkan, C, Prufer, K, Meyer, M, Burbano, HA, Good, JM, Schultz, R, Aximu-Petri, A, Butthof, A, Hober, B, Hoffner, B, Siegemund, M, Weihmann, A, Nusbaum, C, Lander, ES, Russ, (2010) A draft sequence of the Neandertal genome. Science 328: pp. 710-722 CrossRef
  53. Kim, SY, Kim, YS (2008) A gene sets approach for identifying prognostic gene signatures for outcome prediction. BMC Genomics 9: pp. 177 CrossRef
  54. Williams, G (1966) Adaptation and Natural Selection: A Critique of Some Current Evolutionary Thought. Princeton Univ. Press, Princeton, NJ
  55. Crews, D Diversity of hormone-behavior relations in reproductive behavior. In: Becker, JBM, McCarthy, M, Crews, D eds. (1992) Introduction to Behavioral Endocrinology. pp. 143-186
  56. Crews, D (1998) The evolutionary antecedents to love. Psychoneuroendocrinology 23: pp. 751-764 CrossRef
  57. Gowaty, PA, Anderson, WW, Bluhm, CK, Drickamer, LC, Kim, YK, Moore, AJ (2007) The hypothesis of reproductive compensation and its assumptions about mate preferences and offspring viability. Proc Natl Acad Sci USA 104: pp. 15023-15027 CrossRef
  58. Mattle, B, Wilson, AB (2009) Body size preferences in the pot-bellied seahorse Hippocampus abdominalis: choosy males and indiscriminate females. Behav Ecol Sociobiol 63: pp. 1403-1410 CrossRef
  59. Carson, HL (1987) The contribution of sexual behavior to Darwinian fitness. Behav Genet 17: pp. 597-611 CrossRef
  60. Carson, HL (2003) Mate choice theory and the mode of selection in sexual populations. Proc Natl Acad Sci U S A 100: pp. 6584-6587 CrossRef
  61. Gowaty, PA, Steinichen, R, Anderson, WW (2002) Mutual interest between the sexes and reproductive success in Drosophila pseudoobscura. Evolution 56: pp. 2537-2540 CrossRef
  62. Stunden, CE, Bluhm, CK, Cheng, KM, Rajamahendran, R (1999) Factors affecting reproductive performance in captive Mallard ducks. Theriogenology 52: pp. 435-446 CrossRef
  63. Drickamer, LC, Gowaty, PA, Holmes, CM (2000) Free female mate choice in house mice affects reproductive success and offspring viability and performance. Anim Behav 59: pp. 371-378 CrossRef
  64. Drickamer, LCGP, Wagner, DM (2003) Free mutual mate preferences in house mice affect reproductive success and offspring performance. Animal Behav 65: pp. 105-114 CrossRef
  65. Kirkpatrick, M, Ryan, MJ (1991) The evolution of mating preferences and the paradox of the lek. Nature 350: pp. 33-38 CrossRef
  66. Ryan, M (1990) Sexual selection, sensory systems, and sensory exploitation. Oxford Survey Evol Biol 7: pp. 157-196
  67. Beach, F Animal models for human sexuality. In: Potter, RWJ eds. (1979) Sex, Hormones and Behaviour. Ciba Foundation Symposium 62, Excerpta Medica, Amsterdam, pp. 113-143
  68. Crews, D (2005) Evolution of neuroendocrine mechanisms that regulate sexual behavior. Trends Endocrinol Metab 16: pp. 354-361 CrossRef
  69. Paxinos, G, Watson, C (2007) The Rat Brain in Stereotaxic Coordinates. Academic, New York
  70. Bosotti, R, Locatelli, G, Healy, S, Scacheri, E, Sartori, L, Mercurio, C, Calogero, R, Isacchi, A (2007) Cross platform microarray analysis for robust identification of differentially expressed genes. BMC Bioinforma 8: pp. S5 CrossRef
  71. Zhang, B, Horvath, S (2005) A general framework for weighted gene co-expression network analysis. Stat Appl Genet Mol Biol.
  72. Zhu, J, Wiener, MC, Zhang, C, Fridman, A, Minch, E, Lum, PY, Sachs, JR, Schadt, EE (2007) Increasing the power to detect causal associations by combining genotypic and expression data in segregating populations. PLoS Comput Biol 3: pp. e69 CrossRef
  73. Ravasz, E, Somera, AL, Mongru, DA, Oltvai, ZN, Barabasi, AL (2002) Hierarchical organization of modularity in metabolic networks. Science 297: pp. 1551-1555 CrossRef
  74. Langfelder, P, Zhang, B, Horvath, S (2008) Defining clusters from a hierarchical cluster tree: the dynamic tree cut package for r. Bioinformatics 24: pp. 719-720 CrossRef
  75. Lum, PY, Chen, Y, Zhu, J, Lamb, J, Melmed, S, Wang, S, Drake, TA, Lusis, AJ, Schadt, EE (2006) Elucidating the murine brain transcriptional network in a segregating mouse population to identify core functional modules for obesity and diabetes. J Neurochem 97: pp. 50-62 CrossRef
  76. Chen, Y, Zhu, J, Lum, PY, Yang, X, Pinto, S, MacNeil, DJ, Zhang, C, Lamb, J, Edwards, S, Sieberts, SK, Leonardson, A, Castellini, LW, Wang, S, Champy, MF, Zhang, B, Emilsson, V, Doss, S, Ghazalpour, A, Horvath, S, Drake, TA, Lusis, AJ, Schadt, EE (2008) Variations in DNA elucidate molecular networks that cause disease. Nature 452: pp. 429-435 CrossRef
  77. Gargalovic, PS, Imura, M, Zhang, B, Gharavi, NM, Clark, MJ, Pagnon, J, Yang, WP, He, A, Truong, A, Patel, S, Nelson, SF, Horvath, S, Berliner, JA, Kirchgessner, TG, Lusis, AJ (2006) Identification of inflammatory gene modules based on variations of human endothelial cell responses to oxidized lipids. Proc Natl Acad Sci U S A 103: pp. 12741-12746 CrossRef
  78. Horvath, S, Zhang, B, Carlson, M, Lu, KV, Zhu, S, Felciano, RM, Laurance, MF, Zhao, W, Qi, S, Chen, Z, Lee, Y, Scheck, AC, Liau, LM, Wu, H, Geschwind, DH, Febbo, PG, Kornblum, HI, Cloughesy, TF, Nelson, SF, Mischel, PS (2006) Analysis of oncogenic signaling networks in glioblastoma identifies ASPM as a molecular target. Proc Natl Acad Sci U S A 103: pp. 17402-17407 CrossRef
  79. Emilsson, V, Thorleifsson, G, Zhang, B, Leonardson, AS, Zink, F, Zhu, J, Carlson, S, Helgason, A, Walters, GB, Gunnarsdottir, S, Mouy, M, Steinthorsdottir, V, Eiriksdottir, GH, Bjornsdottir, G, Reynisdottir, I, Gudbjartsson, D, Helgadottir, A, Jonasdottir, A, Styrkarsdottir, U, Gretarsdottir, S, Magnusson, KP, Stefansson, H, Fossdal, R, Kristjansson, K, Gislason, HG, Stefansson, T, Leifsson, BG, Thorsteinsdottir, U, Lamb, JR, Gulcher, (2008) Genetics of gene expression and its effect on disease. Nature 452: pp. 423-428 CrossRef
  80. Schadt, EE, Molony, C, Chudin, E, Hao, K, Yang, X, Lum, PY, Kasarskis, A, Zhang, B, Wang, S, Suver, C, Zhu, J, Millstein, J, Sieberts, S, Lamb, J, GuhaThakurta, D, Derry, J, Storey, JD, Avila-Campillo, I, Kruger, MJ, Johnson, JM, Rohl, CA, van Nas, A, Mehrabian, M, Drake, TA, Lusis, AJ, Smith, RC, Guengerich, FP, Strom, SC, Schuetz, E, Rushmore, TH (2008) Mapping the genetic architecture of gene expression in human liver. PLoS Biol 6: pp. e107 CrossRef
  81. Zhu, J, Zhang, B, Schadt, EE (2008) A systems biology approach to drug discovery. Adv Genet 60: pp. 603-635 CrossRef
  82. Draghici, S, Khatri, P, Tarca, AL, Amin, K, Done, A, Voichita, C, Georgescu, C, Romero, R (2007) A systems biology approach for pathway level analysis. Genome Res 17: pp. 1537-1545 CrossRef
  
• 刊物主题：Life Sciences, general; Microarrays; Proteomics; Animal Genetics and Genomics; Microbial Genetics and Genomics; Plant Genetics & Genomics;
• 出版者：BioMed Central
• ISSN：1471-2164

文摘

Background Mate preference behavior is an essential first step in sexual selection and is a critical determinant in evolutionary biology. Previously an environmental compound (the fungicide vinclozolin) was found to promote the epigenetic transgenerational inheritance of an altered sperm epigenome and modified mate preference characteristics for three generations after exposure of a gestating female. Results The current study investigated gene networks involved in various regions of the brain that correlated with the altered mate preference behavior in the male and female. Statistically significant correlations of gene clusters and modules were identified to associate with specific mate preference behaviors. This novel systems biology approach identified gene networks (bionetworks) involved in sex-specific mate preference behavior. Observations demonstrate the ability of environmental factors to promote the epigenetic transgenerational inheritance of this altered evolutionary biology determinant. Conclusions Combined observations elucidate the potential molecular control of mate preference behavior and suggests environmental epigenetics can have a role in evolutionary biology.