Neofunctionalization of the Sec1 α1,2fucosyltransferase Paralogue in Leporids Contributes to Glycan Polymorphism and Resistance to Rabbit Hemorrhagic Disease Virus

PLoS Pathogens

Volumn 11, Issue 4, 2015, Pages

  Nyström, Kristina ^a,b   Abrantes, Joana ^a,c   Lopes, Ana Margarida ^c,d   Le Moullac Vaidye, Béatrice ^a   Marchandeau, Stéphane ^e   Rocher, Jézabel ^a   Ruvoën Clouet, Nathalie ^a,f   Esteves, Pedro J ^c,d,g   Le Pendu, Jacques ^a  

^a UNIVERSITÉ DE NANTES   (France)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

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

^d UNIVERSITY OF PORTO   (Portugal)

^e OFFICE NATIONAL DE LA CHASSE ET DE LA FAUNE SAUVAGE   (France)

^f LUNAM UNIVERSITÉ   (France)

^g INSTITUTO DE INVESTIGAÇÃO E FORMAÇÃO AVANÇADA EM CIÊNCIAS E TECNOLOGIAS DA SAÚDE   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

FUCOSYLTRANSFERASE; GENOMIC DNA; MESSENGER RNA; POLYSACCHARIDE;

ALLELE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING ASSAY; BINDING SITE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DISEASE RESISTANCE; DNA EXTRACTION; DNA POLYMORPHISM; DUODENUM; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; FUCOSYLTRANSFERASE GENE; GENE; GENE CONVERSION; GENE DUPLICATION; GENE EXPRESSION; GENE LOCUS; GENETIC VARIABILITY; INTESTINE MUCOSA; LAGOVIRUS; MOLECULAR CLONING; NONHUMAN; PHYLOGENETIC TREE; RABBIT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEC1 GENE; SURVIVAL; ANIMAL; CALICIVIRUS INFECTION; GENETIC POLYMORPHISM; GENETIC TRANSFECTION; GENETICS; LAGOMORPH; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; RABBIT HEMORRHAGIC DISEASE VIRUS;

ANIMALIA; CALICIVIRIDAE; LEPORIDAE; MAMMALIA; ORYCTOLAGUS CUNICULUS; RABBIT HEMORRHAGIC DISEASE VIRUS;

ANIMALS; BASE SEQUENCE; CALICIVIRIDAE INFECTIONS; DISEASE RESISTANCE; FUCOSYLTRANSFERASES; HEMORRHAGIC DISEASE VIRUS, RABBIT; LAGOMORPHA; MOLECULAR SEQUENCE DATA; POLYMERASE CHAIN REACTION; POLYMORPHISM, GENETIC; POLYSACCHARIDES; RABBITS; TRANSFECTION;

EID: 84929484386     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004759     Document Type: Article

References (64)

1. Innan H, Kondrashov F, (2010) The evolution of gene duplications: classifying and distinguishing between models. Nat Rev Genet 11: 97–108. doi: 10.1038/nrg2689 20051986
2. Katju V, (2012) In with the Old, in with the New: The Promiscuity of the Duplication Process Engenders Diverse Pathways for Novel Gene Creation. International Journal of Evolutionary Biology 2012: 341932. 23008799
3. Saunier K, Barreaud JP, Eggen J, Oriol R, Levéziel H, et al. (2001) Organization of the bovine alpha2-fucosyltransferase gene cluster suggests that the Sec1 gene might have been shaped through a nonautonomous L1-retrotransposition event within the same locus. Mol Biol Evol 18: 2083–2091. 11606704
4. Abrantes J, Posada D, Guillon P, Esteves PJ, Le Pendu J, (2009) Widespread gene conversion of alpha-2-fucosyltransferase genes in mammals. J Mol Evol 69: 22–31. doi: 10.1007/s00239-009-9239-0 19533213
5. Oriol R, Candelier JJ, Mollicone R, (2000) Molecular genetics of H. Vox Sang 78: 105–118. 10938937
6. Apoil PA, Roubinet F, Despiau S, Mollicone R, Oriol R, et al. (2000) Evolution of a2-fucosyltransferase genes in primates: relation between an intronic Alu-Y element and red cell expression of ABH antigen. Mol Biol Evol 17: 337–351. 10723735
7. Bureau V, Marionneau S, Cailleau-Thomas A, Le Moullac-Vaydie B, Liehr T, et al. (2001) Comparison of the three rat GDP-L-fucose:b-D-galactoside 2-a-L-fucosyltransferases FTA, FTB and FTC. Eur J Biochem 268: 1006–1019. 11179967
8. Borges BN, Paiva TS, Harada ML, (2008) Evolution of the SEC1 gene in New World monkey lineages (Primates, Platyrrhini). Genet Mol Res 7: 663–678. 18752194
9. Iwamori M, Domino SE, (2004) Tissue-specific loss of fucosylated glycolipids in mice targeted deletion of alpha(1,2)fucosyltransferase genes. Biochem J 380: 75–81. 14967068
10. Oriol R, Le Pendu J, Mollicone R, (1986) Genetics of ABO, H, Lewis, X and related antigens. Vox Sang 51: 161–171. 2433836
11. Ravn V, Dabelsteen E, (2000) Tissue distribution of histo-blood group antigens. APMIS 108: 1–28. 10698081
12. Amin MA, Ruth JH, Haas CS, Pakozdi A, Mansfield PJ, et al. (2008) H-2g, a glucose analog of blood group H antigen, mediates mononuclear cell recruitment via Src and phosphatidylinositol 3-kinase pathways. Arthritis Rheum 58: 689–695. doi: 10.1002/art.23296 18311817
13. Garcia-Vallejo JJ, van Liempt E, da Costa Martins P, Beckers C, van het Hof B, et al. (2008) DC-SIGN mediates adhesion and rolling of dendritic cells on primary human umbilical vein endothelial cells through Lewis Y antigen expressed on ICAM-2. Mol Immunol 45: 2359–2369. 18155766
14. Moehler TM, Sauer S, Witzel M, Andrulis M, Garcia-Vallejo JJ, et al. (2008) Involvement of alpha 1-2-fucosyltransferase (FUT1) and surface-expressed Lewis(y) (CD174) in first endothelial cell-cell contacts during angiogenesis. J Cell Physiol 215: 27–36. doi: 10.1002/jcp.21285 18205178
15. St John JA, Claxton C, Robinson MW, Yamamoto F, Domino SE, et al. (2006) Genetic manipulation of blood group carbohydrates alters development and pathfinding of primary sensory axons of the olfactory systems. Dev Biol 298: 470–484. 16884711
16. Marionneau S, Cailleau-Thomas A, Rocher J, Le Moullac-Vaidye B, Ruvoën-clouet N, et al. (2001) ABH and Lewis histo-blood group antigens, a model for the meaning of oligosaccharide diversity in the face of a changing world. Biochimie 83: 565–573. 11522384
17. Stapleton A, Nudelman E, Clausen E, Hakomori S, I, Stamm W, E, (1992) Binding of uropathogenic Escherichia coli R45 to glycolipids extracted from vaginal epithelial cells is dependent on histo-blood group secretor status. J Clin Invest 90: 965–972. 1522244
18. Ruiz-Palacios GM, Cervantes LE, Ramos P, Chavez-Munguia B, Newburg DS, (2003) Campylobacter jejuni binds intestinal H(O) antigen and fucosyloligosaccharides of human milk inhibit its binding and infection. J Biol Chem 278: 14112–14120. 12562767
19. Tan M, Jiang X, (2011) Norovirus-host interaction: Multi-selections by human histo-blood group antigens. Trends Microbiol 19: 382–388. doi: 10.1016/j.tim.2011.05.007 21705222
20. Hu L, Crawford SE, Czako R, Cortes-Penfield NW, Smith DF, et al. (2012) Cell attachment protein VP8* of a human rotavirus specifically interacts with A-type histo-blood group antigen. Nature 485: 256–259. doi: 10.1038/nature10996 22504179
21. Liu Y, Huang P, Tan M, Biesiada J, Meller J, et al. (2012) Rotavirus VP8*: phylogeny, host range, and interaction with histo-blood group antigens. J Virol 86: 9899–9910. doi: 10.1128/JVI.00979-12 22761376
22. Hitoshi S, Kusunoki S, Kanazawa I, Tsuji S, (1995) Molecular cloning and expression of two types of rabbit b-galactoside a1,2fucosyltransferase. J Biol Chem 270: 8844–8850. 7721792
23. Guillon P, Ruvöen-Clouet N, Le Moullac-Vaidye B, Marchandeau S, Le Pendu J, (2009) Association between expression of the H histo-blood group antigen, α1,2 fucosyltransferases polymorphism of wild rabbits, and sensitivity to rabbit hemorrhagic disease virus. Glycobiology 19: 21–28. doi: 10.1093/glycob/cwn098 18842963
24. Teshima KM, Innan H, (2004) The effect of conversion on the divergence between duplicated genes. Genetics 166: 1553–1560. 15082568
25. Liu SJ, Xue HP, Pu BQ, Quian NH, (1984) A new viral disease in rabbit. Anim Husb Vet Med 16: 235–255.
26. Abrantes J, van der Loo W, Le Pendu J, Esteves PJ, (2011) Rabbit haemorrhagic disease (RHD) and rabbit haemorrhagic disease virus (RHDV): a review. Veterinary Research in press. doi: 10.1186/1297-9716-43-12 22325049
27. Ruvoën-Clouet N, Ganière JP, André-Fontaine G, Blanchard D, Le Pendu J, (2000) Binding of Rabbit Hemorrhagic Disease Virus to antigens of the ABH histo-blood group family. J Virol 74: 11950–11954. 11090195
28. Ruvöen-Clouet N, Belliot G, Le Pendu J, (2013) Noroviruses and histo-blood groups: the impact of common host genetic polymorphisms on virus transmission and evolution. Rev Med Virol 23: 355–366. doi: 10.1002/rmv.1757 23959967
29. Ilver D, Arnqvist A, Ögren J, Frick IM, Kersulyte D, et al. (1998) Helicobacter pylori adhesin binding fucosylated histo-blood group antigens revealed by retagging. Science 279: 373–377. 9430586
30. Azevedo M, Eriksson S, Mendes N, Serpa J, Figueiredo C, et al. (2008) Infection by Helicobacter pylori expressing the BabA adhesin is influenced by the secretor phenotype. J Pathol 215: 308–316. doi: 10.1002/path.2363 18498114
31. Koda Y, Soejima M, Kimura H, (2001) The polymorphisms of fucosyltransferases. Leg Med (Tokyo) 3: 2–14.
32. Ferrer-Admetlla A, Sikora M, Laayouni H, Esteve A, Roubinet F, et al. (2009) A natural history of FUT2 polymorphism in humans. Mol Biol Evol 26: 1993–2003. doi: 10.1093/molbev/msp108 19487333
33. Silva LM, Carvalho AS, Guillon P, Seixas S, Azevedo M, et al. (2010) Infection-associated FUT2 (fucosyltransferase 2) genetic variation and impact on functionality assessed by in vivo studies. Glycoconj J 27: 61–68. doi: 10.1007/s10719-009-9255-8 19757028
34. Le Pendu J, Ruvöen-Clouet N, Kindberg E, Svensson L, (2006) Mendelian resistance to human norovirus infections. Sem Immunol 18: 375–386.
35. Hitoshi S, Kusunoki S, Kanazawa I, Tsuji S, (1996) Molecular cloning and expression of a third type of rabbit GDP-L-fucose: b-D-galactoside 2-a-L-fucosyltransferase. J Biol Chem 271: 16975–16981. 8663168
36. Nyström K, Le Gall-Recule G, Grassi P, Abrantes J, Ruvoën-Clouet N, et al. (2011) Histo-Blood Group Antigens act as attachment factors of Rabbit Hemorrhagic Disease Virus infection in a virus strain-dependent manner. PLoS Pathogens 7: e1002188. doi: 10.1371/journal.ppat.1002188 21901093
37. Le Pendu J, Cartron JP, Lemieux R, U, Oriol R, (1985) The presence of at least two different H-blood group-related b-D-gal a-2-L-fucosyltransferases in human serum and the genetics of blood group H substances. Am J Hum Genet 37: 749–760. 9556663
38. Sarnesto A, Köhlin T, Hindsgaul O, Thurin J, Blaszczyk-Thurin M, (1992) Purification of the secretor-type b-galactoside a1-2fucosyltransferase from human serum. J Biol Chem 267: 2737–2744. 1733969
39. Masutani H, Kimura H, (1995) Purification and characterization of secretory-type GDP-L-fucose: b-D-galactoside 2-a-L-fucosyltransferase from human gastric mucosa. J Biochem 118: 541–545. 8690714
40. Esteves PJ, Lanning D, Ferrand N, Knight KL, Zhai SK, et al. (2004) Allelic variation at the VHa locus in natural populations of rabbit (Oryctolagus cuniculus, L.). J Immunol 172: 1044–1053. 14707078
41. Surridge AK, van der Loo W, Abrantes J, Carneiro M, Hewitt GM, et al. (2008) Diversity and evolutionary history of the MHC DQA gene in leporids. Immunogenetics 60: 515–525. doi: 10.1007/s00251-008-0309-z 18584169
42. Abrantes J, Areal H, Esteves PJ, (2013) Insights into the European rabbit (Oryctolagus cuniculus) innate immune system: genetic diversity of the toll-like receptor 3 (TLR3) in wild populations and domestic breeds BMC Genetics 14: 73. doi: 10.1186/1471-2156-14-73 23964588
43. Varki A, Esko JD, Colley KJ, Varki A, Cummings RD, Esko JD, Freeze HH, Stanley P, (2009) Cellular organization of localization. In: et al., editors. Essentials of Glycobiology. 2dn Edition ed. New York: Cold Spring Harbor.
44. Hashimoto K, Madej T, Bryant SH, Panchenko AR, (2010) Functional states of homooligomers: insights from the evolutionof glycosyltransferases. J Mol Biol 399: 196–206. doi: 10.1016/j.jmb.2010.03.059 20381499
45. Faik A, Bar-Peled M, DeRocher AE, Zeng WQ, Perrin RM, et al. (2000) Biochemical characterization of an alpha-1,2fucosyltransferase that catalyzes the last step of cell wall xyloglucan biosyntesis in pea. J Biol Chem 275: 15082–15089. 10747946
46. Sousa VL, Costa MT, Palma AS, Enguita F, Costa J, (2001) Localization, purification and specificity of the full-length membrane-bound form of human recombinant alpha 1,3/4-fucosyltransferase from BHK-21B cells. Biochem J 357: 803–810. 11463351
47. El-Battari A, Prorok M, Angata K, Mathieu S, Zerfaoui M, et al. (2003) Different glycosyltransferases are differentially processed for secretion, dimerization, and autoglycosylation. Glycobiology 13: 941–953. 14514709
48. Ihara H, Ikeda Y, Koyota S, Endo T, Honke H, et al. (2002) A catalytically inactive beta 1,4-N-acetylglucosaminyltransferase III (GnT-III) behaves as a dominant nege-ative GnT-III inhibitor. Eur J Biochem 269: 193–201. 11784313
49. Matsunami K, Miyagawa S, Nakagawa K, Hideaki O, Shirakura R, (2006) Molecular cloning of pigGnT-I and I.2: an application to xenotransplantation. Biochemical and Biophysical Resarch Communication 343: 677–683. 16563346
50. Olson FJ, Bäckström M, Karlsson H, Burchell J, Hansson GC, (2005) A MUC1 tandem repeat reporter protein produced in CHO-K1 cells has sialylated core 1 O-glycans and becomes more densely glycosylated if coexpressed with polypeptide-GalNAc-T4 transferase. Glycobiology 15: 177–191. 15456735
51. Bellemare J, Rouleau M, Harvey M, Têtu B, Guillemette C, (2010) Alternative-splicing forms of major phase II conjugating UGT1A gene negatively regulate glucuronidation in human carcinoma cell lines. Pharmacogenomics J 10: 431–441. doi: 10.1038/tpj.2009.64 19997083
52. Hitoshi S, Koijima N, Kusunoki S, Inokuchi J, Kanazawa I, et al. (1996) Expression of the beta-galactoside alpha 1,2-fucosyltransferase gene suppresses axonal outgrowth of neuro2a neuroblastoma cells. J Neurochem 66: 1633–1640. 8627320
53. Wagner FF, Flegel WA, (1997) Polymorphism of the h allele and the population frequency of sporadic nonfunctional alleles. Transfusion 37: 284–290. 9122901
54. Queney G, Ferrand N, Marchandeau S, Azevodo M, Mougel F, et al. (2000) Absence of a genetic bottleneck in a wild rabbit (Oryctolagus cuniculus) population exposed to a severe viral epizootic. Molecular Ecology 9: 1253–1264. 10972766
55. Queney G, Ferrand N, Weiss S, Mougel F, Monnerot M, (2001) Stationary distributions of microsatellite loci between divergent population groups of the European rabbit (Oryctolagus cuniculus). Mol Biol and Evol 18: 2169–2178. 11719566
56. Le Gall-Recule G, Zwingelstein F, Laurent S, De Boisseron C, Portejoie Y, et al. (2003) Phylogenetic analysis of rabbit haemorrhagic disease virus in France between 1993 and 2000 and the characterization of RHDV antigenic variants. Arch Virol 148: 65–81. 12536296
57. Matthee CA, van Vuuren BJ, Bell D, Robinson TJ, (2004) A molecular supermatrix of the rabbits and hares (Leporidae) allows for the identification of five intercontinental exchanges during the Miocene. Syst Biol 53: 443–447.
58. Esteves PJ, Lanning D, Ferrand N, Knight KL, Zhai SK, et al. (2005) The evolution of the immunoglobulin heavy chain variable region (IgVH) in Leporids: an unusual case of transspecies polymorphism. Immunogenetics 57: 874–882. 16247606
59. van der Loo W, Abrantes J, Esteves PJ, (2009) Sharing of endogenous lentiviral gene fragments among leporid lineages separated for more than 12 million years. J Virol 83: 2386–2388. doi: 10.1128/JVI.01116-08 19109386
60. Hall T, (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41: 95–98.
61. Kosakovsky-Pond SL, Frost SD, (2005b) Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 21: 2531–2533. 15713735
62. Delport W, Poon AF, Frost SDW, Kosakovsky-Pond SL, (2010) Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology. Bioinformatics 26: 2455–2457. doi: 10.1093/bioinformatics/btq429 20671151
63. Kosakovsky-Pond SL, Posada D, Gravenor MB, Woelk CH, Frost S, (2006) GARD: A Genetic Algorithm for Recombination Detection. Bioinformatics 22: 3096–3098. 17110367
64. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: molecular evolutionary genetic analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol and Evol 28: 2731–2739. doi: 10.1093/molbev/msr121 21546353