A prominent role of KRAB-ZNF transcription factors in mammalian speciation?

Trends in Genetics

Volumn 29, Issue 3, 2013, Pages 130-139

  Nowick, Katja ^a   Carneiro, Miguel ^b   Faria, Rui ^b,c  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b CENTRO DE INVESTIGAÇÃO EM BIODIVERSIDADE E RECURSOS GENÉTICOS   (Portugal)

^c UNIVERSITAT POMPEU FABRA   (Spain)

Author keywords

BDM incompatibilities; Gene regulatory networks; Hybrid sterility; Post zygotic isolation; Prdm9; Zinc finger gene

Indexed keywords

ANTINUCLEAR ANTIBODY; KRUPPEL ASSOCIATED BOX DOMAIN ZINC FONGER PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN;

CELL CYCLE REGULATION; CELL DIFFERENTIATION; COPY NUMBER VARIATION; DNA BINDING; DNA POLYMORPHISM; DOWN REGULATION; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; GENE CONTROL; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENETIC CODE; GENETIC EPISTASIS; GENETIC VARIABILITY; GENOME ANALYSIS; HUMAN; HYBRID; MAMMAL; MOLECULAR EVOLUTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; REPRODUCTIVE ISOLATION; REVIEW; RNA METABOLISM; SEX DETERMINATION PROCESS; SIGNAL TRANSDUCTION; SPECIES DIFFERENTIATION; SPERMATOGENESIS; X CHROMOSOME;

ANIMALS; GENETIC SPECIATION; HUMANS; REPRESSOR PROTEINS; TRANSCRIPTION FACTORS; ZINC FINGERS;

MAMMALIA;

EID: 84875254039     PISSN: 01689525     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tig.2012.11.007     Document Type: Review

References (81)

1. Coyne J., Orr H.A. Speciation 2004, Sinauer Associates.
2. Dobzhansky T. Genetics and the Origin of Species 1937, Columbia University Press.
3. Muller H.J. Isolating mechanisms, evolution and temperature. Biol. Symp. 1942, 6:71-125.
4. Bateson W. Heredity and variation in modern lights. Darwin and Modern Science 1909, 85-101. Cambridge University Press. A.C. Seward (Ed.).
5. Orr H.A. Dobzhansky, Bateson and the genetics of speciation. Genetics 1996, 144:1331-1335.
6. Barbash D.A., et al. A rapidly evolving MYB-related protein causes species isolation in Drosophila. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:5302-5307.
7. Masly J.P., Presgraves D.C. High-resolution genome-wide dissection of the two rules of speciation in Drosophila. PLoS Biol. 2007, 5:e243.
8. Bayes J.J., Malik H.S. Altered heterochromatin binding by a hybrid sterility protein in Drosophila species. Science 2009, 326:1538-1541.
9. Mihola O., et al. A mouse speciation gene encodes a meiotic histone H3 methyltransferase. Science 2009, 323:373-375.
10. Phadnis N., Orr H.A. A single gene causes both male sterility and segregation distortion in Drosophila hybrids. Science 2009, 323:376-378.
11. Presgraves D.C., et al. Adaptive evolution drives divergence of a hybrid inviability gene between two species of Drosophila. Nature 2003, 243:715-719.
12. Brideau N.J., et al. Two Dobzhansky-Muller genes interact to cause hybrid lethality in Drosophila. Science 2006, 314:1292-1295.
13. Oliver P.L., et al. Accelerated evolution of the Prdm9 speciation gene across diverse metazoan taxa. PLoS Genet. 2009, 5:e1000753.
14. Presgraves D.C. The molecular evolutionary basis of species formation. Nat. Rev. Genet. 2010, 11:175-180.
15. Johnson N.A. Hybrid incompatibility genes: remnants of a genomics battlefield?. Trends Genet. 2010, 26:317-325.
16. Good J.M., et al. Widespread over-expression of the X chromosome in sterile F1 mice. PLoS Genet. 2010, 6:e1001148.
17. Ortíz-Barrientos D., et al. Gene expression divergence and the origin of hybrid dysfunctions. Genetica 2007, 129:71-81.
18. Michalak P., Noor M.A.F. Association of misexpression with sterility in hybrids of Drosophila simulans and D. mauritiana. J. Mol. Evol. 2004, 59:277-282.
19. Landry C.R., et al. Genome clashes in hybrids: insights from gene expression. Heredity 2007, 99:483-493.
20. Haerty W., Singh R.S. Gene regulation divergence is a major contributor to the evolution of Dobzhansky-Muller incompatibilities between species of Drosophila. Mol. Biol. Evol. 2006, 23:1707-1714.
21. Presgraves D.C. Sex chromosomes and speciation in Drosophila. Trends Genet. 2008, 24:336-343.
22. Meiklejohn C.D., Tao Y. Genetic conflict and sex chromosome evolution. Trends Ecol. Evol. 2010, 25:215-223.
23. Presgraves D.C., Orr H.A. Haldane's rule in taxa lacking a hemizygous X. Science 1998, 282:952-954.
24. Fitzpatrick B.M. Rates of evolution of hybrid inviability in birds and mammals. Evolution 2004, 58:1639-1881.
25. Birtle Z., Ponting C.P. Meisetz and the birth of the KRAB motif. Bioinformatics 2006, 22:2841-2845.
26. Hayashi K., et al. A histone H3 methyltransferase controls epigenetic events required for meiotic prophase. Nature 2005, 438:374-378.
27. Ségurel L., et al. The case of the fickle fingers: how the PRDM9 zinc finger protein specifies meiotic recombination hotspots in humans. PLoS Biol. 2011, 9:e1001211.
28. Forejt J. Hybrid sterility in the mouse. Trends Genet. 1996, 12:412-417.
29. 1 hybrid sterility in house mice. Evolution 2012, 66:3321-3335.
30. Knight R.D., Shimeld S.M. Identification of conserved C2H2 zinc-finger gene families in the Bilateria. Genome Bio. 2001, 2. research0016.1-research0016.8.
31. Gonzalez-Lamuno D., et al. Expression and regulation of the transcriptional repressor ZNF43 in Ewing sarcoma cells. Pediatr. Pathol. Mol. Med. 2002, 21:531-540.
32. Huang C., et al. Characterization of ZNF23, a KRAB-containing protein that is downregulated in human cancers and inhibits cell cycle progression. Exp. Cell Res. 2007, 313:254-263.
33. Alcaraz W.A., et al. Modifier genes and non-genetic factors reshape anatomical deficits in Zfp423-deficient mice. Hum. Mol. Genet. 2011, 20:3822-3830.
34. Kamiya D., et al. Intrinsic transition of embryonic stem-cell differentiation into neural progenitors. Nature 2011, 470:503-509.
35. Mackay D.J., et al. Hypomethylation of multiple imprinted loci in individuals with transient neonatal diabetes is associated with mutations in ZFP57. Nat. Genet. 2008, 40:949-951.
36. Ponting C.P. What are the genomic drivers of the rapid evolution of PRDM9?. Trends Genet. 2011, 27:165-271.
37. Wolf D., Goff S.P. Embryonic stem cells use ZFP809 to silence retroviral DNAs. Nature 2009, 458:1201-1204.
38. Looman C., et al. MZF6D, a novel KRAB zinc-finger gene expressed exclusively in meiotic male germ cells. DNA Cell Biol. 2003, 22:489-496.
39. Passananti C., et al. The product of Zfp59 (Mfg2), a mouse gene expressed at the spermatid stage of spermatogenesis, accumulates in spermatozoa nuclei. Cell Growth Differ. 1995, 6:1037-1044.
40. Thomas J.H., Emerson R.O. Evolution of C2H2-zinc finger genes revisited. BMC Evol. Biol. 2009, 9:51.
41. Huntley S., et al. A comprehensive catalog of human KRAB-associated zinc finger genes: insights into the evolutionary history of a large family of transcriptional repressors. Genome Res. 2006, 16:669-677.
42. Emerson R.O., Thomas J.H. Adaptive evolution in zinc finger transcription factors. PLoS Genet. 2009, 5:e1000325.
43. Hamilton A.T., et al. Evolutionary expansion and divergence in the ZNF91 subfamily of primate-specific zinc finger genes. Genome Res. 2006, 16:584-594.
44. Nowick K., et al. Rapid sequence and expression divergence suggest selection for novel function in primate-specific KRAB-ZNF genes. Mol. Biol. Evol. 2010, 27:2606-2617.
45. Bustamante C.D., et al. Natural selection on protein-coding genes in the human genome. Nature 2005, 437:1153-1157.
46. Nielsen R., et al. A scan for positively selected genes in the genomes of humans and chimpanzees. PLoS Biol. 2005, 3:e170.
47. Ding G., et al. SysZNF: the C2H2 zinc finger gene database. Nucleic Acids Res. 2009, 37:D267-D273.
48. Forejt J., et al. Hybrid male sterility genes in the mouse subspecific crosses. Evolution of the House Mouse 2012, 482-503. Cambridge University Press. M. Macholán (Ed.).
49. Baudat F., et al. PRDM9 is a major determinant of meiotic recombination hotspots in humans and mice. Science 2010, 327:836-840.
50. Perry G.H., et al. Hotspots for copy number variation in chimpanzees and humans. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:8006-8011.
51. Nei M., Rooney A.P. Concerted and birth-and-death evolution of multigene families. Annu. Rev. Genet. 2005, 39:121-152.
52. Nowick K., et al. Gain, loss and divergence in primate zinc-finger genes: a rich resource for evolution of gene regulatory differences between species. PLoS ONE 2011, 6:e21553.
53. Schmidt D., et al. Five-vertebrate ChIP-seq reveals the evolutionary dynamics of transcription factor binding. Science 2010, 328:1036-1040.
54. Thomas J.H., Schneider S. Coevolution of retroelements and tandem zinc finger genes. Genome Res. 2011, 21:1800-1812.
55. Henikoff S., et al. The centromere paradox: stable inheritance with rapidly evolving DNA. Science 2001, 293:1098-10102.
56. White M.A., et al. Genetic dissection of a key reproductive barrier between nascent subspecies of house mice, Mus musculus domesticus and Mus musculus musculus. Genetics 2011, 169:289-304.
57. Grey C., et al. Mouse PRDM9 DNA-binding specificity determines sites of histone H3 lysine 4 trimethylation for initiation of meiotic recombination. PLoS Biol. 2011, 9:e1001176.
58. Brayer K.J., et al. The protein-binding potential of C2H2 zinc finger domains. Cell Biochem. Biophys. 2008, 51:9-19.
59. Nowick K., Stubbs L. Lineage-specific transcription factors and the evolution of gene regulatory networks. Brief. Funct. Genomics 2010, 9:65-78.
60. Innan H., Kondrashov F. The evolution of gene duplications: classifying and distinguishing between models. Nat. Rev. Genet. 2010, 11:97-108.
61. Lorenz P., et al. The ancient mammalian KRAB zinc finger gene cluster on human chromosome 8q24.3 illustrates principles of C2H2 zinc finger evolution associated with unique expression profiles in human tissues. BMC Genomics 2010, 11:206.
62. Hinman V.F., et al. Evolution of gene regulatory network architectures: examples of subcircuit conservation and plasticity between classes of echinoderms. Biochim. Biophys. Acta 2009, 1789:326-332.
63. Wolf J.B.W., et al. Speciation genetics: current status and evolving approaches. Phil. Trans. R. Soc. B. 2010, 3650:1717-1733.
64. Kim J., et al. Imprinting and evolution of two Kruppel-type zinc-finger genes, ZIM3 and ZNF264, located in the PEG3/USP29 imprinted domain. Genomics 2001, 77:91-98.
65. Gimelbrant A., et al. Widespread monoallelic expression on human autosomes. Science 2007, 318:1136-1140.
66. Tadepally H.D., et al. Evolution of C2H2-zinc finger genes and subfamilies in mammals: species-specific duplication and loss of clusters, genes and effector domains. BMC Evol. Biol. 2008, 8:176.
67. Kosiol C., et al. Patterns of positive selection in six mammalian genomes. PLoS Genet. 2008, 4:e1000144.
68. Chung W.Y., et al. Rapid and asymmetric divergence of duplicate genes in the human gene coexpression network. BMC Bioinformatics 2006, 7:46.
69. Nowick K., et al. Rapid expansion and divergence suggest a central and distinct role for KRAB-ZNF genes in vertebrate evolution. Focus on Zinc Finger Protein Research 2009, 13-29. Research Signpost. K. Yoshida (Ed.).
70. Oldham M.C., et al. Conservation and evolution of gene coexpression networks in human and chimpanzee brains. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:17973-17978.
71. Amoutzias G.D., et al. A protein interaction atlas for the nuclear receptors: properties and quality of a hub-based dimerisation network. BMC Syst. Biol. 2007, 1:34.
72. Krebs C.J., et al. Expansion and diversification of KRAB zinc-finger genes within a cluster including Regulator of sex-limitation 1 and 2. Genomics 2005, 85:752-761.
73. Hurst L.D., Pomiankowski A. Causes of sex ratio bias may account for unisexual sterility in hybrids: a new explanation of Haldane's rule and related phenomena. Genetics 1991, 128:841-858.
74. Kondrashov A.S., et al. Dobzhansky-Muller incompatibilities in protein evolution. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:14878-14883.
75. Bellefroid E.J., et al. Clustered organization of homologous KRAB zinc-finger genes with enhanced expression in human T lymphoid cells. EMBO J. 1993, 12:1363-1374.
76. Thiesen H.J. Conserved KRAB protein domain identified upstream from the zinc finger region of Kox 8. Nucleic Acids Res. 1991, 19:3996.
77. Krishna S.S., et al. Structural classification of zinc fingers: survey and summary. Nucleic Acids Res. 2003, 31:532-550.
78. Lam K.N., et al. Sequence specificity is obtained from the majority of modular C2H2 zinc-finger arrays. Nucleic Acids Res. 2011, 39:4680-4690.
79. Wolfe S.A., et al. Beyond the 'recognition code': structures of two Cys2His2 zinc finger/TATA box complexes. Structure 2001, 9:717-723.
80. Friedman J.R., et al. KAP-1, a novel corepressor for the highly conserved KRAB repression domain. Genes Dev. 1996, 10:2067-2078.
81. Schultz D.C., et al. Targeting histone deacetylase complexes via KRAB-zinc finger proteins: the PHD and bromodomains of KAP-1 form a cooperative unit that recruits a novel isoform of the Mi-2alpha subunit of NuRD. Genes Dev. 2001, 15:428-443.