Lgals6, a 2-million-year-old gene in mice: A case of positive darwinian selection and presence/absence polymorphism

Genetics

Volumn 178, Issue 3, 2008, Pages 1533-1545

  Houzelstein, Denis ^a   Gonçalves, Isabelle R ^a,b   Orth, Annie ^c   Bonhomme, François ^c   Netter, Pierre ^a  

^a INSTITUT JACQUES MONOD   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c INSTITUT DES SCIENCES DE L EVOLUTION   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GALECTIN; GALECTIN 4; LGALS6 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DNA POLYMORPHISM; GENE; GENE DUPLICATION; GENE FUNCTION; GENE SEQUENCE; GENETIC SELECTION; GENOME; INFECTION; LGALS4 GENE; LGALS6 GENE; MOUSE; MOUSE STRAIN; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; GENETIC POLYMORPHISM; GENETICS; GEOGRAPHY; HISTORY; MOLECULAR GENETICS; PHYLOGENY; STATISTICAL MODEL;

MUS; MUS MUSCULUS; MUS PAHARI;

AMINO ACID SEQUENCE; ANIMALS; GALECTIN 4; GALECTINS; GENE DUPLICATION; GENOME; GEOGRAPHY; HISTORY, ANCIENT; LIKELIHOOD FUNCTIONS; MICE; MICE, INBRED STRAINS; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYMORPHISM, GENETIC; SELECTION (GENETICS);

EID: 45149100538     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.107.082792     Document Type: Article

References (74)

1. ADAMS, D. J., E. T. DERMITZAKIS, T. COX, J. SMITH, R. DAVIES et al., 2005 Complex haplotypes, copy number polymorphisms and coding variation in two recently divergent mouse strains. Nat. Genet. 37: 532-536.
2. AITMAN, T. J., R. DONG, T. J. VYSE, P. J. NORSWORTHY, M. D. JOHNSON et al., 2006 Copy number polymorphismin Fcgr3 predisposes to glomerulonephritis in rats and humans. Nature 439: 851-855.
3. BAILEY, J. A., Z. GU, R. A. CLARK, K. REINERT, R. V. SAMONTE et al., 2002 Recent segmental duplications in the human genome. Science 297: 1003-1007.
4. BAILEY, J. A., D. M. CHURCH, M. VENTURA, M. ROCCHI and E. E. EICHLER, 2004 Analysis of segmental duplications and genome assembly in the mouse. Genome Res. 14: 789-801.
5. BECK, J. A., S. LLOYD, M. HAFEZPARAST, M. LENNON-PIERCE, J. T. EPPIG et al., 2000 Genealogies of mouse inbred strains. Nat. Genet. 24: 23-25.
6. BIDON-WAGNER, N., and J. P. LE PENNEC, 2004 Human galectin-8 isoforms and cancer. Glycoconj. J. 19: 557-563.
7. BISHOP, T. R., M. W. MILLER, A. WANG and P. M. DIERKS, 1998 Multiple copies of the ALA-D gene are located at the Lv locus in Mus domesticus mice. Genomics 48: 221-231.
8. BRACCIA, A., M. VILLANI, L. IMMERDAL, L. L. NIELS-CHRISTIANSEN, B. T. NYSTROM et al., 2003 Microvillar membrane microdomains exist at physiological temperature. Role of galectin-4 as lipid raft stabilizer revealed by "superrafts." J. Biol. Chem. 278: 15679-15684.
9. BUCKLAND, P. R., 2003 Polymorphically duplicated genes: their relevance to phenotypic variation in humans. Ann. Med. 35: 308-315.
10. CASTRESANA, J., 2000 Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 17: 540-552.
11. CHAMARY, J. V., J. L. PARMLEY and L. D. HURST, 2006 Hearing silence: non-neutral evolution at synonymous sites in mammals. Nat. Rev. Genet. 7: 98-108.
12. DANIELSEN, E. M., and G. H. HANSEN, 2006 Lipid raft organization and function in brush borders of epithelial cells. Mol. Membr. Biol. 23: 71-79.
13. DANN, S. M., and L. ECKMANN, 2007 Innate immune defenses in the intestinal tract. Curr. Opin. Gastroenterol. 23: 115-120.
14. DELACOUR, D., V. GOUYER, J. P. ZANETTA, H. DROBECQ, E. LETEURTRE et al., 2005 Galectin-4 and sulfatides in apical membrane trafficking in enterocyte-like cells. J. Cell Biol. 169: 491-501.
15. DUMIC, J., S. DABELIC and M. FLOGEL, 2006 Galectin-3: an open-ended story. Biochim. Biophys. Acta 1760: 616-635.
16. FEUK, L., A. R. CARSON and S. W. SCHERER, 2006 Structural variation in the human genome. Nat. Rev. Genet. 7: 85-97.
17. FORCE, A., M. LYNCH, F. B. PICKETT, A. AMORES, Y. L. YAN et al., 1999 Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151: 1531-1545.
18. FREEMAN, J. L., G. H. PERRY, L. FEUK, R. REDON, S. A. MCCARROLL et al., 2006 Copy number variation: new insights in genome diversity. Genome Res. 16: 949-961.
19. GALTIER, N., M. GOUY and C. GAUTIER, 1996 SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Comput. Appl. Biosci. 12: 543-548.
20. GAYRAL, P., P. CAMINADE, P. BOURSOT and N. GALTIER, 2007 The evolutionary fate of recently duplicated retrogenes in mice. J. Evol. Biol. 20: 617-626.
21. GITT, M. A., C. COLNOT, F. POIRIER, K. J. NANI, S. H. BARONDES et al., 1998a Galectin-4 and galectin-6 are two closely related lectins expressed in mouse gastrointestinal tract. J. Biol. Chem. 273: 2954-2960.
22. GITT, M. A., Y. R. XIA, R. E. ATCHISON, A. J. LUSIS, S. H. BARONDES et al., 1998b Sequence, structure, and chromosomal mapping of the mouse Lgals6 gene, encoding galectin-6. J. Biol. Chem. 273: 2961-2970.
23. GONZALEZ, E., H. KULKARNI, H. BOLIVAR, A. MANGANO, R. SANCHEZ et al., 2005 The influence of CCL3L1 gene-containing segmental duplications on HIV-1/AIDS susceptibility. Science 307: 1434-1440.
24. GROWNEY, J. D., and W. F. DIETRICH, 2000 High-resolution genetic and physical map of the Lgn1 interval in C57BL/6J implicates Naip2 or Naip5 in Legionella pneumophila pathogenesis. Genome Res. 10: 1158-1171.
25. GUÉNET, J. L., 2005 Themouse genome. Genome Res. 15: 1729-1740.
26. GUÉNET, J. L., and F. BONHOMME, 2003 Wild mice: an ever-increasing contribution to a popular mammalian model. Trends Genet. 19: 24-31.
27. GUINDON, S., and O. GASCUEL, 2003 A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52: 696-704.
28. HOUZELSTEIN, D., I. R. GONCALVES, A. J. FADDEN, S. S. SIDHU, D. N. COOPER et al., 2004 Phylogenetic analysis of the vertebrate galectin family. Mol. Biol. Evol. 21: 1177-1187.
29. IAFRATE, A. J., L. FEUK, M. N. RIVERA, M. L. LISTEWNIK, P. K. DONAHOE et al., 2004 Detection of large-scale variation in the human genome. Nat. Genet. 36: 949-951.
30. ISIDORE, E., B. SCHERRER, B. CHALHOUB, C. FEUILLET and B. KELLER, 2005 Ancient haplotypes resulting from extensive molecular rearrangements in the wheat A genome have been maintained in species of three different ploidy levels. Genome Res. 15: 526-536.
31. LEFFLER, H., S. CARLSSON, M. HEDLUND, Y. QIAN and F. POIRIER, 2004 Introduction to galectins. Glycoconj. J. 19: 433-440.
32. LENSCH, M., M. LOHR, R. RUSSWURM, M. VIDAL, H. KALTNER, et al., 2006 Unique sequence and expression profiles of rat galectins-5 and -9 as a result of species-specific gene divergence. Int. J. Biochem. Cell Biol. 38: 1741-1758.
33. LEVASSEUR, A., P. GOURET, L. LESAGE- MEESSEN, M. ASTHER, M. ASTHER et al., 2006 Tracking the connection between evolutionary and functional shifts using the fungal lipase/feruloyl esterase A family. BMC Evol. Biol. 6: 92.
34. LI, J., T. JIANG, J. H. MAO, A. BALMAIN, L. PETERSON et al., 2004 Genomic segmental polymorphisms in inbred mouse strains. Nat. Genet. 36: 952-954.
35. LI, P., and J. BOUSQUET, 1992 Relative-rate test for nucleotide substitutions between two lineages. Mol. Biol. Evol. 9: 1185-1189.
36. LIU, F. T., and G. A. RABINOVICH, 2005 Galectins as modulators of tumour progression. Nat. Rev. Cancer 5: 29-41.
37. LOBSANOV, Y. D., M. A. GITT, H. LEFFLER, S. H. BARONDES and J. M. RINI, 1993 X-ray crystal structure of the human dimeric S-Lac lectin, L-14-II, in complex with lactose at 2.9-A resolution. J. Biol. Chem. 268: 27034-27038.
38. LONG, M., E. BETRAN, K. THORNTON and W. WANG, 2003 The origin of new genes: glimpses from the young and old. Nat. Rev. Genet. 4: 865-875.
39. LYNCH, V. J., 2007 Inventing an arsenal: adaptive evolution and neofunctionalization of snake venom phospholipase A2 genes. BMC Evol. Biol. 7: 2.
40. MORGENSTERN, B., 1999 DIALIGN 2: improvement of the segment-to-segment approach to multiple sequence alignment. Bioinformatics 15: 211-218.
41. NEI, M., 2005 Selectionism and neutralism in molecular evolution. Mol. Biol. Evol. 22: 2318-2342.
42. NEI, M., and T. GOJOBORI, 1986 Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol. Biol. Evol. 3: 418-426.
43. NEI, M., and S. KUMAR, 2000 Molecular Evolution and Phylogenetics. Oxford University Press, Oxford.
44. NGUYEN, D. Q., C. WEBBER and C. P. PONTING, 2006 Bias of selection on human copy-number variants. PLoS Genet. 2: e20.
45. NIELSEN, R., and Z. YANG, 1998 Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics 148: 929-936.
46. NIO, J., Y. KON and T. IWANAGA, 2005 Differential cellular expression of galectin family mRNAs in the epithelial cells of the mouse digestive tract. J. Histochem. Cytochem. 53: 1323-1334.
47. OGAWA, T., T. SHIRAI, C. SHIONYU- MITSUYAMA, T. YAMANE, H. KAMIYA et al., 2004 The speciation of conger eel galectins by rapid adaptive evolution. Glycoconj. J. 19: 451-458.
48. OHNO, S., 1970 Evolution by Gene Duplication. Springer-Verlag, Berlin.
49. OTTO, S. P., and P. YONG, 2002 The evolution of gene duplicates. Adv. Genet. 46: 451-483.
50. PEMBERTON, A. D., P. A. KNIGHT, J. GAMBLE, W. H. COLLEDGE, J. K. LEE et al., 2004 Innate BALB/c enteric epithelial responses to Trichinella spiralis: inducible expression of a novel goblet cell lectin, intelectin-2, and its natural deletion in C57BL/10 mice. J. Immunol. 173: 1894-1901.
51. ROBINSON-RECHAVI, M., and D. HUCHON, 2000 RRTree: relative-rate tests between groups of sequences on a phylogenetic tree. Bioinformatics 16: 296-297.
52. ROBINSON, M., M. GOUY, C. GAUTIER and D. MOUCHIROUD, 1998 Sensitivity of the relative-rate test to taxonomic sampling. Mol. Biol. Evol. 15: 1091-1098.
53. SAKAI, T., Y. KIKKAWA, I. MIURA, T. INOUE, K. MORIWAKI et al., 2005 Origins of mouse inbred strains deduced from wholegenome scanning by polymorphic microsatellite loci. Mamm. Genome 16: 11-19.
54. SALCEDO, T., A. GERALDES and M. W. NACHMAN, 2007 Nucleotide variation in wild and inbred mice. Genetics 177: 2277-2291.
55. SEBAT, J., B. LAKSHMI, J. TROGE, J. ALEXANDER, J. YOUNG et al., 2004 Large-scale copy number polymorphism in the human genome. Science 305: 525-528.
56. SILVER, L. M., 1995 Mouse Genetics. Oxford University Press, New York.
57. SNIJDERS, A. M., N. J. NOWAK, B. HUEY, J. FRIDLYAND, S. LAW et al., 2005 Mapping segmental and sequence variations among laboratory mice using BAC array CGH. Genome Res. 15: 302-311.
58. SUZUKI, H., T. SHIMADA, M. TERASHIMA, K. TSUCHIYA and K. APLIN, 2004 Temporal, spatial, and ecological modes of evolution of Eurasian Mus based on mitochondrial and nuclear gene sequences. Mol. Phylogenet. Evol. 33: 626-646.
59. TAGUCHI, Y., T. KOIDE, T. SHIROISHI and T. YAGI, 2005 Molecular evolution of cadherin-related neuronal receptor/protocadherin (alpha) (CNR/Pcdh(alpha)) gene cluster in Mus musculus subspecies. Mol. Biol. Evol. 22: 1433-1443.
60. TAYLOR, J. S., and J. RAES, 2004 Duplication and divergence: the evolution of new genes and old ideas. Annu. Rev. Genet. 38: 615-643.
61. THOMPSON, J. D., D. G. HIGGINS and T. J. GIBSON, 1994 CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22: 4673-4680.
62. TIAN, D., M. B. TRAW, J. Q. CHEN, M. KREITMAN and J. BERGELSON, 2003 Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423: 74-77.
63. TUZUN, E., J. A. BAILEY and E. E. EICHLER, 2004 Recent segmental duplications in the working draft assembly of the brown Norway rat. Genome Res. 14: 493-506.
64. VALLENDER, E. J., and B. T. LAHN, 2004 Positive selection on the human genome. Hum. Mol. Genet. 13(2): R245-R254.
65. WADE, C. M., and M. J. DALY, 2005 Genetic variation in laboratory mice. Nat. Genet. 37: 1175-1180.
66. WADE, C. M., E. J. R. KULBOKAS, A. W. KIRBY, M. C. ZODY, J. C. MULLIKIN et al., 2002 The mosaic structure of variation in the laboratory mouse genome. Nature 420: 574-578.
67. WRACKMEYER, U., G. H. HANSEN, T. SEYA and E. M. DANIELSEN, 2006 Intelectin: a novel lipid raft-associated protein in the enterocyte brush border. Biochemistry 45: 9188-9197.
68. YANG, Z., 1997 PAML: a program package for phylogenetic analysis by maximum likelihood. Comput. Appl. Biosci. 13: 555-556.
69. YANG, Z., and R. NIELSEN, 2000 Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol. Biol. Evol. 17: 32-43.
70. YANG, Z., and R. NIELSEN, 2002 Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages. Mol. Biol. Evol. 19: 908-917.
71. YANG, Z., W. S. WONG and R. NIELSEN, 2005 Bayes empirical bayes inference of amino acid sites under positive selection. Mol. Biol. Evol. 22: 1107-1118.
72. YANG, H., T. A. BELL, G. A. CHURCHILL and F. PARDO-MANUEL DE VILLENA, 2007 On the subspecific origin of the laboratory mouse. Nat. Genet. 39: 1100-1107.
73. ZHANG, J., 2003 Evolution by gene duplication: an update. Trends Ecol. Evol. 18: 292-298.
74. ZHANG, J., R. NIELSEN and Z. YANG, 2005 Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol. Biol. Evol. 22: 2472-2479.