Evolutionary constraints in the β-globin cluster: The signature of purifying selection at the δ-globin (HBD) locus and its role in developmental gene regulation

Genome Biology and Evolution

Volumn 5, Issue 3, 2013, Pages 559-571

  Moleirinho, Ana ^a   Seixas, Susana ^a   Lopes, Alexandra M ^a   Bento, Celeste ^b   Prata, Maria J ^a   Amorim, António ^a  

^a UNIVERSITY OF PORTO   (Portugal)

^b CENTRO HOSPITALAR E UNIVERSITÁRIO DE COIMBRA   (Portugal)

Author keywords

Chromatin interactions; Gene diversity; Hemoglobin switch; globin cluster

Indexed keywords

PAN; PRIMATES;

EID: 84876571638     PISSN: None     EISSN: 17596653     Source Type: Journal    
DOI: 10.1093/gbe/evt029     Document Type: Article

References (101)

1. Akey JM, et al. 2004. Population history and natural selection shape patterns of genetic variation in 132 genes. PLoS Biol. 2:7.
2. Altshuler DM, et al. 2012. An integrated map of genetic variation from 1,092 human genomes. Nature 491:56-65.
3. Bamshad M, Wooding SP. 2003. Signatures of natural selection in the human genome. Nat Rev Genet. 4:99-111.
4. Bandelt HJ, Forster P, Rohl A. 1999. Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol. 16:37-48.
5. Bank A. 2006. Regulation of human fetal hemoglobin: new players, new complexities. Blood 107:435-443.
6. Bank A, Mears J, Ramirez F. 1980. Disorders of human hemoglobin. Science 207:486-493.
7. Bank A, et al. 2005. Role of intergenic human g-d-globin sequences in human hemoglobin switching and reactivation of fetal hemoglobin in adult erythroid cells. Ann N Y Acad Sci. 1054:48-54.
8. Barreiro LB, et al. 2009. Evolutionary dynamics of human toll-like receptors and their different contributions to host defense. PLoS Genet. 5: e1000562.
9. Barrett JC, Fry B, Maller J, Daly MJ. 2005. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21: 263-265.
10. Beauchemin H, Trudel M. 2009. Evidence for a bigenic chromatin subdomain in regulation of the fetal-to-adult hemoglobin switch. Mol Cell Biol. 29:1635-1648.
11. Borg J, Georgitsi M, Aleporou-Marinou V, Kollia P, Patrinos GP. 2009. Genetic recombination as a major cause of mutagenesis in the human globin gene clusters. Clin Biochem. 42:1839-1850.
12. Bulger M, Groudine M. 1999. Looping versus linking: toward a model for long-distance gene activation. Genes Dev. 13:2465-2477.
13. Cao A, Moi P. 2000. Genetic modifying factors in b-thalassemia. Clin Chem Lab Med. 38:123-132.
14. Chakalova L, et al. 2005. Developmental regulation of the b-globin gene locus. In: Jeanteur P, editor. Epigenetics and chromatin. Berlin (Germany): Springer. p. 183-206.
15. Chakravarti A, et al. 1984. Nonuniform recombination within the human beta-globin gene cluster. Am J Hum Genet. 36:1239-1258.
16. Chang LYE, Slightom JL. 1984. Isolation and nucleotide sequence analysis of the b-type globin pseudogene from human, gorilla and chimpanzee. J Mol Biol. 180:767-783.
17. Chen FC, Li WH. 2001. Genomic divergences between humans and other hominoids and the effective population size of the common ancestor of humans and chimpanzees. Am J Hum Genet. 68: 444-456.
18. de Bruin SH, Janssen LHM. 1973. Comparison of the oxygen and proton binding behavior of human hemoglobin A and A2. Biochim Biophys Acta. 295:490-494.
19. Dostie J, et al. 2006. Chromosome conformation capture carbon copy (5C): a massively parallel solution for mapping interactions between genomic elements. Genome Res. 16:1299-1309.
20. Excoffier L. 2002. Human demographic history: refining the recent African origin model. Curr Opin Genet Dev. 12:675-682.
21. Fay JC, Wu CI. 2000. Hitchhiking under positive Darwinian selection. Genetics 155:1405-1413.
22. Frisse L, et al. 2001. Gene conversion and different population histories may explain the contrast between polymorphism and linkage disequilibrium levels. Am J Hum Genet. 69:831-843.
23. Fullerton SM, et al. 2000. Apolipoprotein E variation at the sequence haplotype level: implications for the origin and maintenance of a major human polymorphism. Am J Hum Genet. 67: 881-900.
24. Gabriel SB, et al. 2002. The structure of haplotype blocks in the human genome. Science 296:2225-2229.
25. Galanello R, Origa R. 2010. Beta-thalassemia. Orphanet J Rare Dis. 5:11.
26. Galarneau G, et al. 2010. Fine-mapping at three loci known to affect fetal hemoglobin levels explains additional genetic variation. Nat Genet. 42:1049-1051.
27. Garrigan D, Hammer MF. 2006. Reconstructing human origins in the genomic era. Nat Rev Genet. 7:669-680.
28. Giambona A, Passarello C, Renda D, Maggio A. 2009. The significance of the hemoglobin A2 value in screening for hemoglobinopathies. Clin Biochem. 42:1786-1796.
29. Goodman M, Koop BF, Czelusniak J, Weiss ML, Slightom JL. 1984. The eta-globin gene: its long evolutionary history in the beta-globin gene family of mammals. J Mol Biol. 180:803-823.
30. Griffiths RC, Tavare S. 1994. Sampling theory for neutral alleles in a varying environment. Philos Trans R Soc Lond B Biol Sci. 344: 403-410.
31. Gutenkunst RN, Hernandez RD, Williamson SH, Bustamante CD. 2009. Inferring the joint demographic history of multiple populations from multidimensional SNP frequency data. PLoS Genet. 5: e1000695.
32. Hardies SC, Edgell MH, Hutchison CA. 1984. Evolution of the mammalian beta-globin gene cluster. J Biol Chem. 259:3748-3756.
33. Harding RM, et al. 1997. Archaic African and Asian lineages in the genetic ancestry of modern humans. Am J Hum Genet. 60:772-789.
34. Harju S, McQueen KJ, Peterson KR. 2002. Chromatin structure and control of b-like globin gene switching. Exp Biol Med. 227: 683-700.
35. Harpending HC, et al. 1998. Genetic traces of ancient demography. Proc Natl Acad Sci U S A. 95:1961-1967.
36. Holwerda S, De Laat W. 2012. Chromatin loops, gene positioning and gene expression. Front Genet. 3:217.
37. Hou C, Dale R, Dean A. 2010. Cell type specificity of chromatin organization mediated by CTCF and cohesin. Proc Natl Acad Sci U S A. 107: 3651-3656.
38. Hudson RR. 2002. Generating samples under a Wright-Fisher neutral model of genetic variation. Bioinformatics 18:337-338.
39. Hudson RR, Kreitman M, Aguadé M. 1987. A test of neutral molecular evolution based on nucleotide data. Genetics 116: 153-159.
40. Johnson RM, Gumucio D, Goodman M. 2002. Globin gene switching in primates. Comp Biochem Physiol A Mol Integr Physiol. 133: 877-883.
41. Keinan A, Clark AG. 2012. Recent explosive human population growth has resulted in an excess of rare genetic variants. Science 336: 740-743.
42. Kim HL, Igawa T, Kawashima A, Satta Y, Takahata N. 2010. Divergence, demography and gene loss along the human lineage. Philos Trans R Soc B: Biol Sci. 365:2451-2457.
43. Kwiatkowski DP. 2005. Howmalaria has affected the human genome and what human genetics can teach us about malaria. Am J Hum Genet. 77:171-192.
44. Lacerra G, et al. 2008. Molecular evidences of single mutational events followed by recurrent crossing-overs in the common delta-globin alleles in the Mediterranean area. Gene 410:129-138.
45. Liu L, et al. 2009. High-density SNP genotyping to define beta-globin locus haplotypes. Blood Cells Mol Dis. 42:16-24.
46. Maeda N, Bliska JB, Smithies O. 1983. Recombination and balanced chromosome polymorphism suggested by DNA sequences 5′ to the human delta-globin gene. Proc Natl Acad Sci U S A. 80: 5012-5016.
47. Martin SL, Zimmer EA, Kan YW, Wilson AC. 1980. Silent delta-globin gene in OldWorld monkeys. Proc Natl Acad Sci U S A. 77:3563-3566.
48. Martinez-Arias R, et al. 2001. Sequence variability of a human pseudogene. Genome Res. 11:1071-1085.
49. Mathias RA, et al. 2012. Adaptive evolution of the FADS gene cluster within Africa. PLoS One 7:e44926.
50. MeyerM, et al. 2012. A high-coverage genome sequence froman Archaic Denisovan individual. Science 338:222-226.
51. Morgado A, et al. 2007. Mutational spectrum of delta-globin gene in the Portuguese population. Eur J Haematol. 79:422-428.
52. Mosca A, Paleari R, Ivaldi G, Galanello R, Giordano PC. 2009. The role of haemoglobin A2 testing in the diagnosis of thalassaemias and related haemoglobinopathies. J Clin Pathol. 62:13-17.
53. Mukherjee S, Sarkar-Roy N, Wagener DK, Majumder PP. 2009. Signatures of natural selection are not uniform across genes of innate immune system, but purifying selection is the dominant signature. Proc Natl Acad Sci U S A. 106:7073-7078.
54. Myers RM, et al. 2011. A user's guide to the encyclopedia of DNA elements (ENCODE). PLoS Biol. 9:19.
55. Nei M, Li WH. 1979. Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci U S A. 76:5269-5273.
56. Nikolaou C, Althammer S, Beato M, Guigo R. 2010. Structural constraints revealed in consistent nucleosome positions in the genome of S. cerevisiae. Epigenetics Chromatin 3:1756-8935.
57. Noordermeer D, de Laat W. 2008. Joining the loops: beta-globin gene regulation. IUBMB Life 60:824-833.
58. Opazo JC, Hoffmann FG, Storz JF. 2008. Genomic evidence for independent origins of b-like globin genes in monotremes and therian mammals. Proc Natl Acad Sci U S A. 105:1590-1595.
59. Orkin SH, Higgs DR. 2010. Sickle cell disease at 100 years. Science 329: 291-292.
60. Ottolenghi S, et al. 1979. Globin gene deletion in HPFH, δ° β ° thalassaemia and Hb Lepore disease. Nature 278:654-657.
61. Pagnier J, et al. 1984. Evidence for the multicentric origin of the sickle cell hemoglobin gene in Africa. Proc Natl Acad Sci U S A. 81: 1771-1773.
62. Papadakis MN, Patrinos GP. 1999. Contribution of gene conversion in the evolution of the human β-like globin gene family. Hum Genet. 104:117-125.
63. Patrinos GP, et al. 2004a.Multiple interactions between regulatory regions are required to stabilize an active chromatin hub. Genes Dev. 18: 1495-1509.
64. Patrinos GP, et al. 2004b. Improvements in the HbVar database of human hemoglobin variants and thalassemia mutations for population and sequence variation studies. Nucleic Acids Res. 32: D537-D541.
65. Patterson N, Richter DJ, Gnerre S, Lander ES, Reich D. 2006. Genetic evidence for complex speciation of humans and chimpanzees. Nature 441:1103-1108.
66. Phylipsen M, Gallivan MVE, Arkesteijn SGJ, Harteveld CL, Giordano PC. 2011. Occurrence of common and rare d-globin gene defects in two multiethnic populations: thirteen new mutations and the significance of d-globin gene defects in b-thalassemia diagnostics. Int J Lab Hematol. 33:85-91.
67. Reich D, et al. 2011. Denisova admixture and the first modern human dispersals into Southeast Asia and Oceania. Am J Hum Genet. 89: 516-528.
68. Rozas J. 2009. DNA sequence polymorphism analysis using DnaSP. Methods Mol Biol. 537:337-350.
69. Sabeti PC, et al. 2002. Detecting recent positive selection in the human genome from haplotype structure. Nature 419:832-837.
70. Sankaran VG, et al. 2008. Human fetal hemoglobin expression is regulated by the developmental stage-specific repressor BCL11A. Science 322: 1839-1842.
71. Sankaran VG, et al. 2011. A functional element necessary for fetal hemoglobin silencing. N Engl J Med. 365:807-814.
72. Sankaran VG, Xu J, Orkin SH. 2010. Advances in the understanding of haemoglobin switching. Br J Haematol. 149:181-194.
73. Sankaran VG, et al. 2009. Developmental and species-divergent globin switching are driven by BCL11A. Nature 460:1093-1097.
74. Sanyal A, Lajoie BR, Jain G, Dekker J. 2012. The long-range interaction landscape of gene promoters. Nature 489:109-113.
75. Schaffner SF, et al. 2005. Calibrating a coalescent simulation of human genome sequence variation. Genome Res. 15:1576-1583.
76. Schechter AN. 2008. Hemoglobin research and the origins of molecular medicine. Blood 112:3927-3938.
77. Smith RA, Ho PJ, Clegg JB, Kidd JR, Thein SL. 1998. Recombination breakpoints in the human beta-globin gene cluster. Blood 92: 4415-4421.
78. Splinter E, et al. 2006. CTCF mediates long-range chromatin looping and local histone modification in the beta-globin locus. Genes Dev. 20: 2349-2354.
79. Spritz R, Giebel L. 1988. The structure and evolution of the spider monkey delta-globin gene. Mol Biol Evol. 5:21-29.
80. Stajich JE, Hahn MW. 2005. Disentangling the effects of demography and selection in human history. Mol Biol Evol. 22:63-73.
81. Steinberg M, Adams JG 3rd. 1991. Hemoglobin A2: origin, evolution, and aftermath. Blood 78:2165-2177.
82. Stephens M, Donnelly P. 2003. A comparison of Bayesian methods for haplotype reconstruction from population genotype data. Am J Hum Genet. 73:1162-1169.
83. Stephens M, Smith NJ, Donnelly P. 2001. A new statistical method for haplotype reconstruction from population data. Am J Hum Genet. 68: 978-989.
84. Tajima F. 1989. Statisticalmethod for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585-595.
85. Thein S. 2005. Genetic modifiers of beta-thalassemia. Haematologica 90: 649-660.
86. Tishkoff SA, Verrelli BC. 2003. Patterns of human genetic diversity: implications for human evolutionary history and disease. Annu Rev Genomics Hum Genet. 4:293-340.
87. Tolhuis B, Palstra RJ, Splinter E, Grosveld F, de Laat W. 2002. Looping and interaction between hypersensitive sites in the active beta-globin locus. Mol Cell. 10:1453-1465.
88. Vakoc CR, et al. 2005. Proximity among distant regulatory elements at the b-globin locus requires GATA-1 and FOG-1. Mol Cell. 17: 453-462.
89. Voight BF, et al. 2005. Interrogating multiple aspects of variation in a full resequencing data set to infer human population size changes. Proc Natl Acad Sci U S A. 102:18508-18513.
90. Wall JD, Frisse LA, Hudson RR, Di Rienzo A. 2003. Comparative linkage-disequilibrium analysis of the beta-globin hotspot in primates. Am J Hum Genet. 73:1330-1340.
91. Wall JD, Przeworski M. 2000. When did the human population size start increasing? Genetics 155:1865-1874.
92. Wang G, Vasquez KM. 2006. Non-B DNA structure-induced genetic instability. Mutat Res. 598:103-119.
93. Ward LD, Kellis M. 2012. Evidence of abundant purifying selection in humans for recently acquired regulatory functions. Science 337: 1675-1678.
94. Watterson GA. 1975. On the number of segregating sites in genetical models without recombination. Theor Popul Biol. 7: 256-276.
95. Webster MT, Clegg JB, Harding RM. 2003. Common 5′ ß-globin RFLP haplotypes harbour a surprising level of ancestral sequencemosaicism. Hum Genet. 113:123-139.
96. Webster MT, Wells RS, Clegg JB. 2002. Analysis of variation in the human b-globin gene cluster using a novel DHPLC technique. Mutat Res. 501: 99-103.
97. Wlasiuk G, Nachman MW. 2010. Adaptation and constraint at Toll-like receptors in primates. Mol Biol Evol. 27:2172-2186.
98. WHO. 2011. World malaria report. Geneva (Switzerland): World Health Organization.
99. Xu J, et al. 2010. Transcriptional silencing of {gamma}-globin by BCL11A involves long-range interactions and cooperation with SOX6. Genes Dev. 24:783-798.
100. Zeng K, Fu Y, Shi S, Wu C. 2006. Statistical tests for detecting positive selection by utilizing high-frequency variants. Genetics 174: 1431-1439.
101. Zhang J. 2003. Evolution by gene duplication: an update. Trends Ecol Evol. 18:292-298.