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Published in: Malaria Journal 1/2012

Open Access 01-12-2012 | Research

Genetic variations in genes involved in heparan sulphate biosynthesis are associated with Plasmodium falciparum parasitaemia: a familial study in Burkina Faso

Authors: Alexandre Atkinson, Séverine Garnier, Sarwat Afridi, Francis Fumoux, Pascal Rihet

Published in: Malaria Journal | Issue 1/2012

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Abstract

Background

There is accumulating evidence that host heparan sulphate proteoglycans play an important role in the life cycle of Plasmodium through their heparan sulphate chains, suggesting that genetic variations in genes involved in heparan sulphate biosynthesis may influence parasitaemia. Interestingly, Hs3st3a1 and Hs3st3b1 encoding enzymes involved in the biosynthesis of heparan sulphate are located within a chromosomal region linked to Plasmodium chabaudi parasitaemia in mice. This suggests that HS3ST3A1 and HS3ST3B1 may influence P. falciparum parasitaemia in humans.

Methods

Polymorphisms within HS3ST3A1 and HS3ST3B1 were identified in 270 individuals belonging to 44 pedigrees and living in Burkina Faso. Linkage and association between parasitaemia and the polymorphisms were assessed with MERLIN and FBAT. A genetic interaction analysis was also conducted based on the PGMDR approach.

Results

Linkage between P. falciparum parasitaemia and the chromosomal region containing HS3ST3A1 and HS3ST3B1 was detected on the basis of the 20 SNPs identified. In addition, rs28470223 located within the promoter of HS3ST3A1 was associated with P. falciparum parasitaemia, whereas the PGMDR analysis revealed a genetic interaction between HS3ST3A1 and HS3ST3B1. Seventy-three significant multi-locus models were identified after correcting for multiple tests; 37 significant multi-locus models included rs28470223, whereas 38 multi-locus models contained at least one mis-sense mutation within HS3ST3B1.

Conclusion

Genetic variants of HS3ST3A1 and HS3ST3B1 are associated with P. falciparum parasitaemia. This suggests that those variants alter both the function of heparan sulphate proteoglycans and P. falciparum parasitaemia.
Appendix
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Literature
1.
go back to reference Sinnis P, Coppi A, Toida T, Toyoda H, Kinoshita-Toyoda A, Xie J, Kemp MM, Linhardt RJ: Mosquito heparan sulphate and its potential role in malaria infection and transmission. J Biol Chem. 2007, 282: 25376-25384. 10.1074/jbc.M704698200.PubMedCentralCrossRefPubMed Sinnis P, Coppi A, Toida T, Toyoda H, Kinoshita-Toyoda A, Xie J, Kemp MM, Linhardt RJ: Mosquito heparan sulphate and its potential role in malaria infection and transmission. J Biol Chem. 2007, 282: 25376-25384. 10.1074/jbc.M704698200.PubMedCentralCrossRefPubMed
2.
go back to reference Coppi A, Tewari R, Bishop JR, Bennett BL, Lawrence R, Esko JD, Billker O, Sinnis P: Heparan sulphate proteoglycans provide a signal to Plasmodium sporozoites to stop migrating and productively invade host cells. Cell Host Microbe. 2007, 2: 316-327. 10.1016/j.chom.2007.10.002.PubMedCentralCrossRefPubMed Coppi A, Tewari R, Bishop JR, Bennett BL, Lawrence R, Esko JD, Billker O, Sinnis P: Heparan sulphate proteoglycans provide a signal to Plasmodium sporozoites to stop migrating and productively invade host cells. Cell Host Microbe. 2007, 2: 316-327. 10.1016/j.chom.2007.10.002.PubMedCentralCrossRefPubMed
3.
go back to reference Kobayashi K, Kato K, Sugi T, Takemae H, Pandey K, Gong H, Tohya Y, Akashi H: Plasmodium falciparum BAEBL binds to heparan sulphate proteoglycans on the human erythrocyte surface. J Biol Chem. 2010, 285: 1716-1725. 10.1074/jbc.M109.021576.PubMedCentralCrossRefPubMed Kobayashi K, Kato K, Sugi T, Takemae H, Pandey K, Gong H, Tohya Y, Akashi H: Plasmodium falciparum BAEBL binds to heparan sulphate proteoglycans on the human erythrocyte surface. J Biol Chem. 2010, 285: 1716-1725. 10.1074/jbc.M109.021576.PubMedCentralCrossRefPubMed
4.
go back to reference Vogt AM, Winter G, Wahlgren M, Spillmann D: Heparan sulphate identified on human erythrocytes: a Plasmodium falciparum receptor. Biochem J. 2004, 381: 593-597. 10.1042/BJ20040762.PubMedCentralCrossRefPubMed Vogt AM, Winter G, Wahlgren M, Spillmann D: Heparan sulphate identified on human erythrocytes: a Plasmodium falciparum receptor. Biochem J. 2004, 381: 593-597. 10.1042/BJ20040762.PubMedCentralCrossRefPubMed
5.
go back to reference Chen Q, Barragan A, Fernandez V, Sundstrom A, Schlichtherle M, Sahlen A, Carlson J, Datta S, Wahlgren M: Identification of Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1) as the rosetting ligand of the malaria parasite P. falciparum. J Exp Med. 1998, 187: 15-23. 10.1084/jem.187.1.15.PubMedCentralCrossRefPubMed Chen Q, Barragan A, Fernandez V, Sundstrom A, Schlichtherle M, Sahlen A, Carlson J, Datta S, Wahlgren M: Identification of Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1) as the rosetting ligand of the malaria parasite P. falciparum. J Exp Med. 1998, 187: 15-23. 10.1084/jem.187.1.15.PubMedCentralCrossRefPubMed
6.
go back to reference Vogt AM, Barragan A, Chen Q, Kironde F, Spillmann D, Wahlgren M: Heparan sulphate on endothelial cells mediates the binding of Plasmodium falciparum-infected erythrocytes via the DBL1alpha domain of PfEMP1. Blood. 2003, 101: 2405-2411. 10.1182/blood-2002-07-2016.CrossRefPubMed Vogt AM, Barragan A, Chen Q, Kironde F, Spillmann D, Wahlgren M: Heparan sulphate on endothelial cells mediates the binding of Plasmodium falciparum-infected erythrocytes via the DBL1alpha domain of PfEMP1. Blood. 2003, 101: 2405-2411. 10.1182/blood-2002-07-2016.CrossRefPubMed
7.
go back to reference Prydz K, Dalen KT: Synthesis and sorting of proteoglycans. J Cell Sci. 2000, 113 (Pt 2): 193-205.PubMed Prydz K, Dalen KT: Synthesis and sorting of proteoglycans. J Cell Sci. 2000, 113 (Pt 2): 193-205.PubMed
8.
go back to reference Shukla D, Liu J, Blaiklock P, Shworak NW, Bai X, Esko JD, Cohen GH, Eisenberg RJ, Rosenberg RD, Spear PG: A novel role for 3-O-sulphated heparan sulphate in herpes simplex virus 1 entry. Cell. 1999, 99: 13-22. 10.1016/S0092-8674(00)80058-6.CrossRefPubMed Shukla D, Liu J, Blaiklock P, Shworak NW, Bai X, Esko JD, Cohen GH, Eisenberg RJ, Rosenberg RD, Spear PG: A novel role for 3-O-sulphated heparan sulphate in herpes simplex virus 1 entry. Cell. 1999, 99: 13-22. 10.1016/S0092-8674(00)80058-6.CrossRefPubMed
9.
go back to reference Xu D, Tiwari V, Xia G, Clement C, Shukla D, Liu J: Characterization of heparan sulphate 3-O-sulphotransferase isoform 6 and its role in assisting the entry of herpes simplex virus type 1. Biochem J. 2005, 385: 451-459. 10.1042/BJ20040908.PubMedCentralCrossRefPubMed Xu D, Tiwari V, Xia G, Clement C, Shukla D, Liu J: Characterization of heparan sulphate 3-O-sulphotransferase isoform 6 and its role in assisting the entry of herpes simplex virus type 1. Biochem J. 2005, 385: 451-459. 10.1042/BJ20040908.PubMedCentralCrossRefPubMed
10.
go back to reference Shworak NW, Liu J, Petros LM, Zhang L, Kobayashi M, Copeland NG, Jenkins NA, Rosenberg RD: Multiple isoforms of heparan sulphate D-glucosaminyl 3-O-sulfotransferase. Isolation, characterization, and expression of human cdnas and identification of distinct genomic loci. J Biol Chem. 1999, 274: 5170-5184. 10.1074/jbc.274.8.5170.CrossRefPubMed Shworak NW, Liu J, Petros LM, Zhang L, Kobayashi M, Copeland NG, Jenkins NA, Rosenberg RD: Multiple isoforms of heparan sulphate D-glucosaminyl 3-O-sulfotransferase. Isolation, characterization, and expression of human cdnas and identification of distinct genomic loci. J Biol Chem. 1999, 274: 5170-5184. 10.1074/jbc.274.8.5170.CrossRefPubMed
11.
go back to reference Liu J, Shworak NW, Sinay P, Schwartz JJ, Zhang L, Fritze LM, Rosenberg RD: Expression of heparan sulphate D-glucosaminyl 3-O-sulfotransferase isoforms reveals novel substrate specificities. J Biol Chem. 1999, 274: 5185-5192. 10.1074/jbc.274.8.5185.CrossRefPubMed Liu J, Shworak NW, Sinay P, Schwartz JJ, Zhang L, Fritze LM, Rosenberg RD: Expression of heparan sulphate D-glucosaminyl 3-O-sulfotransferase isoforms reveals novel substrate specificities. J Biol Chem. 1999, 274: 5185-5192. 10.1074/jbc.274.8.5185.CrossRefPubMed
12.
go back to reference Joubert BR, Lange EM, Franceschini N, Mwapasa V, North KE, Meshnick SR: A whole genome association study of mother-to-child transmission of HIV in Malawi. Genome Med. 2010, 2: 17-PubMedCentralCrossRefPubMed Joubert BR, Lange EM, Franceschini N, Mwapasa V, North KE, Meshnick SR: A whole genome association study of mother-to-child transmission of HIV in Malawi. Genome Med. 2010, 2: 17-PubMedCentralCrossRefPubMed
13.
go back to reference Bobardt MD, Salmon P, Wang L, Esko JD, Gabuzda D, Fiala M, Trono D, Van der Schueren B, David G, Gallay PA: Contribution of proteoglycans to human immunodeficiency virus type 1 brain invasion. J Virol. 2004, 78: 6567-6584. 10.1128/JVI.78.12.6567-6584.2004.PubMedCentralCrossRefPubMed Bobardt MD, Salmon P, Wang L, Esko JD, Gabuzda D, Fiala M, Trono D, Van der Schueren B, David G, Gallay PA: Contribution of proteoglycans to human immunodeficiency virus type 1 brain invasion. J Virol. 2004, 78: 6567-6584. 10.1128/JVI.78.12.6567-6584.2004.PubMedCentralCrossRefPubMed
14.
go back to reference Aucan C, Traore Y, Tall F, Nacro B, Traore-Leroux T, Fumoux F, Rihet P: High immunoglobulin G2 (IgG2) and low IgG4 levels are associated with human resistance to Plasmodium falciparum malaria. Infect Immun. 2000, 68: 1252-1258. 10.1128/IAI.68.3.1252-1258.2000.PubMedCentralCrossRefPubMed Aucan C, Traore Y, Tall F, Nacro B, Traore-Leroux T, Fumoux F, Rihet P: High immunoglobulin G2 (IgG2) and low IgG4 levels are associated with human resistance to Plasmodium falciparum malaria. Infect Immun. 2000, 68: 1252-1258. 10.1128/IAI.68.3.1252-1258.2000.PubMedCentralCrossRefPubMed
15.
go back to reference Rihet P, Traore Y, Abel L, Aucan C, Traore-Leroux T, Fumoux F: Malaria in humans: Plasmodium falciparum blood infection levels are linked to chromosome 5q31-q33. Am J Hum Genet. 1998, 63: 498-505. 10.1086/301967.PubMedCentralCrossRefPubMed Rihet P, Traore Y, Abel L, Aucan C, Traore-Leroux T, Fumoux F: Malaria in humans: Plasmodium falciparum blood infection levels are linked to chromosome 5q31-q33. Am J Hum Genet. 1998, 63: 498-505. 10.1086/301967.PubMedCentralCrossRefPubMed
16.
go back to reference Kwiatkowski DP: How malaria has affected the human genome and what human genetics can teach us about malaria. Am J Hum Genet. 2005, 77: 171-192. 10.1086/432519.PubMedCentralCrossRefPubMed Kwiatkowski DP: How malaria has affected the human genome and what human genetics can teach us about malaria. Am J Hum Genet. 2005, 77: 171-192. 10.1086/432519.PubMedCentralCrossRefPubMed
17.
go back to reference Flori L, Sawadogo S, Esnault C, Delahaye NF, Fumoux F, Rihet P: Linkage of mild malaria to the major histocompatibility complex in families living in Burkina Faso. Hum Mol Genet. 2003, 12: 375-378. 10.1093/hmg/ddg033.CrossRefPubMed Flori L, Sawadogo S, Esnault C, Delahaye NF, Fumoux F, Rihet P: Linkage of mild malaria to the major histocompatibility complex in families living in Burkina Faso. Hum Mol Genet. 2003, 12: 375-378. 10.1093/hmg/ddg033.CrossRefPubMed
18.
go back to reference Sakuntabhai A, Ndiaye R, Casademont I, Peerapittayamongkol C, Rogier C, Tortevoye P, Tall A, Paul R, Turbpaiboon C, Phimpraphi W, Trape JF, Spiegel A, Heath S, Mercereau-Puijalon O, Dieye A, Julier C: Genetic determination and linkage mapping of Plasmodium falciparum malaria related traits in Senegal. PLoS One. 2008, 3: e2000-10.1371/journal.pone.0002000.PubMedCentralCrossRefPubMed Sakuntabhai A, Ndiaye R, Casademont I, Peerapittayamongkol C, Rogier C, Tortevoye P, Tall A, Paul R, Turbpaiboon C, Phimpraphi W, Trape JF, Spiegel A, Heath S, Mercereau-Puijalon O, Dieye A, Julier C: Genetic determination and linkage mapping of Plasmodium falciparum malaria related traits in Senegal. PLoS One. 2008, 3: e2000-10.1371/journal.pone.0002000.PubMedCentralCrossRefPubMed
19.
go back to reference Timmann C, Evans JA, Konig IR, Kleensang A, Ruschendorf F, Lenzen J, Sievertsen J, Becker C, Enuameh Y, Kwakye KO, Opoku E, Browne EN, Ziegler A, Nurnberg P, Horstmann RD: Genome-wide linkage analysis of malaria infection intensity and mild disease. PLoS Genet. 2007, 3: e48-10.1371/journal.pgen.0030048.PubMedCentralCrossRefPubMed Timmann C, Evans JA, Konig IR, Kleensang A, Ruschendorf F, Lenzen J, Sievertsen J, Becker C, Enuameh Y, Kwakye KO, Opoku E, Browne EN, Ziegler A, Nurnberg P, Horstmann RD: Genome-wide linkage analysis of malaria infection intensity and mild disease. PLoS Genet. 2007, 3: e48-10.1371/journal.pgen.0030048.PubMedCentralCrossRefPubMed
20.
go back to reference Flori L, Kumulungui B, Aucan C, Esnault C, Traore AS, Fumoux F, Rihet P: Linkage and association between Plasmodium falciparum blood infection levels and chromosome 5q31-q33. Genes Immun. 2003, 4: 265-268. 10.1038/sj.gene.6363960.CrossRefPubMed Flori L, Kumulungui B, Aucan C, Esnault C, Traore AS, Fumoux F, Rihet P: Linkage and association between Plasmodium falciparum blood infection levels and chromosome 5q31-q33. Genes Immun. 2003, 4: 265-268. 10.1038/sj.gene.6363960.CrossRefPubMed
21.
go back to reference Jepson A, Sisay-Joof F, Banya W, Hassan-King M, Frodsham A, Bennett S, Hill AV, Whittle H: Genetic linkage of mild malaria to the major histocompatibility complex in Gambian children: study of affected sibling pairs. BMJ. 1997, 315: 96-97. 10.1136/bmj.315.7100.96.PubMedCentralCrossRefPubMed Jepson A, Sisay-Joof F, Banya W, Hassan-King M, Frodsham A, Bennett S, Hill AV, Whittle H: Genetic linkage of mild malaria to the major histocompatibility complex in Gambian children: study of affected sibling pairs. BMJ. 1997, 315: 96-97. 10.1136/bmj.315.7100.96.PubMedCentralCrossRefPubMed
22.
go back to reference Bongfen SE, Laroque A, Berghout J, Gros P: Genetic and genomic analyses of host-pathogen interactions in malaria. Trends Parasitol. 2009, 25: 417-422. 10.1016/j.pt.2009.05.012.CrossRefPubMed Bongfen SE, Laroque A, Berghout J, Gros P: Genetic and genomic analyses of host-pathogen interactions in malaria. Trends Parasitol. 2009, 25: 417-422. 10.1016/j.pt.2009.05.012.CrossRefPubMed
23.
go back to reference Verra F, Mangano VD, Modiano D: Genetics of susceptibility to Plasmodium falciparum: from classical malaria resistance genes towards genome-wide association studies. Parasite Immunol. 2009, 31: 234-253. 10.1111/j.1365-3024.2009.01106.x.CrossRefPubMed Verra F, Mangano VD, Modiano D: Genetics of susceptibility to Plasmodium falciparum: from classical malaria resistance genes towards genome-wide association studies. Parasite Immunol. 2009, 31: 234-253. 10.1111/j.1365-3024.2009.01106.x.CrossRefPubMed
24.
go back to reference Hernandez-Valladares M, Naessens J, Iraqi FA: Genetic resistance to malaria in mouse models. Trends Parasitol. 2005, 21: 352-355. 10.1016/j.pt.2005.06.010.CrossRefPubMed Hernandez-Valladares M, Naessens J, Iraqi FA: Genetic resistance to malaria in mouse models. Trends Parasitol. 2005, 21: 352-355. 10.1016/j.pt.2005.06.010.CrossRefPubMed
25.
go back to reference Stevenson MM, Gros P, Olivier M, Fortin A, Serghides L: Cerebral malaria: human versus mouse studies. Trends Parasitol. 2010, 26: 274-275. 10.1016/j.pt.2010.03.008.CrossRefPubMed Stevenson MM, Gros P, Olivier M, Fortin A, Serghides L: Cerebral malaria: human versus mouse studies. Trends Parasitol. 2010, 26: 274-275. 10.1016/j.pt.2010.03.008.CrossRefPubMed
26.
go back to reference Hernandez-Valladares M, Naessens J, Gibson JP, Musoke AJ, Nagda S, Rihet P, Ole-MoiYoi OK, Iraqi FA: Confirmation and dissection of QTL controlling resistance to malaria in mice. Mamm Genome. 2004, 15: 390-398. 10.1007/s00335-004-3042-4.CrossRefPubMed Hernandez-Valladares M, Naessens J, Gibson JP, Musoke AJ, Nagda S, Rihet P, Ole-MoiYoi OK, Iraqi FA: Confirmation and dissection of QTL controlling resistance to malaria in mice. Mamm Genome. 2004, 15: 390-398. 10.1007/s00335-004-3042-4.CrossRefPubMed
27.
go back to reference Hernandez-Valladares M, Rihet P, ole-MoiYoi OK, Iraqi FA: Mapping of a new quantitative trait locus for resistance to malaria in mice by a comparative mapping approach with human chromosome 5q31-q33. Immunogenetics. 2004, 56: 115-117. 10.1007/s00251-004-0667-0.CrossRefPubMed Hernandez-Valladares M, Rihet P, ole-MoiYoi OK, Iraqi FA: Mapping of a new quantitative trait locus for resistance to malaria in mice by a comparative mapping approach with human chromosome 5q31-q33. Immunogenetics. 2004, 56: 115-117. 10.1007/s00251-004-0667-0.CrossRefPubMed
28.
go back to reference Lou XY, Chen GB, Yan L, Ma JZ, Mangold JE, Zhu J, Elston RC, Li MD: A combinatorial approach to detecting gene-gene and gene-environment interactions in family studies. Am J Hum Genet. 2008, 83: 457-467. 10.1016/j.ajhg.2008.09.001.PubMedCentralCrossRefPubMed Lou XY, Chen GB, Yan L, Ma JZ, Mangold JE, Zhu J, Elston RC, Li MD: A combinatorial approach to detecting gene-gene and gene-environment interactions in family studies. Am J Hum Genet. 2008, 83: 457-467. 10.1016/j.ajhg.2008.09.001.PubMedCentralCrossRefPubMed
29.
go back to reference Rihet P, Abel L, Traore Y, Traore-Leroux T, Aucan C, Fumoux F: Human malaria: segregation analysis of blood infection levels in a suburban area and a rural area in Burkina Faso. Genet Epidemiol. 1998, 15: 435-450. 10.1002/(SICI)1098-2272(1998)15:5<435::AID-GEPI1>3.0.CO;2-#.CrossRefPubMed Rihet P, Abel L, Traore Y, Traore-Leroux T, Aucan C, Fumoux F: Human malaria: segregation analysis of blood infection levels in a suburban area and a rural area in Burkina Faso. Genet Epidemiol. 1998, 15: 435-450. 10.1002/(SICI)1098-2272(1998)15:5<435::AID-GEPI1>3.0.CO;2-#.CrossRefPubMed
30.
go back to reference Rozen S, Skaletsky H: Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol. 2000, 132: 365-386.PubMed Rozen S, Skaletsky H: Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol. 2000, 132: 365-386.PubMed
31.
go back to reference Abecasis GR, Cherny SS, Cookson WO, Cardon LR: Merlin-rapid analysis of dense genetic maps using sparse gene flow trees. Nat Genet. 2002, 30: 97-101. 10.1038/ng786.CrossRefPubMed Abecasis GR, Cherny SS, Cookson WO, Cardon LR: Merlin-rapid analysis of dense genetic maps using sparse gene flow trees. Nat Genet. 2002, 30: 97-101. 10.1038/ng786.CrossRefPubMed
32.
33.
go back to reference Abecasis GR, Cookson WO: GOLD-graphical overview of linkage disequilibrium. Bioinformatics. 2000, 16: 182-183. 10.1093/bioinformatics/16.2.182.CrossRefPubMed Abecasis GR, Cookson WO: GOLD-graphical overview of linkage disequilibrium. Bioinformatics. 2000, 16: 182-183. 10.1093/bioinformatics/16.2.182.CrossRefPubMed
34.
go back to reference Barrett JC, Fry B, Maller J, Daly MJ: Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics. 2005, 21: 263-265. 10.1093/bioinformatics/bth457.CrossRefPubMed Barrett JC, Fry B, Maller J, Daly MJ: Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics. 2005, 21: 263-265. 10.1093/bioinformatics/bth457.CrossRefPubMed
35.
go back to reference Sham PC, Purcell S, Cherny SS, Abecasis GR: Powerful regression-based quantitative-trait linkage analysis of general pedigrees. Am J Hum Genet. 2002, 71: 238-253. 10.1086/341560.PubMedCentralCrossRefPubMed Sham PC, Purcell S, Cherny SS, Abecasis GR: Powerful regression-based quantitative-trait linkage analysis of general pedigrees. Am J Hum Genet. 2002, 71: 238-253. 10.1086/341560.PubMedCentralCrossRefPubMed
36.
go back to reference Abecasis GR, Cardon LR, Cookson WO: A general test of association for quantitative traits in nuclear families. Am J Hum Genet. 2000, 66: 279-292. 10.1086/302698.PubMedCentralCrossRefPubMed Abecasis GR, Cardon LR, Cookson WO: A general test of association for quantitative traits in nuclear families. Am J Hum Genet. 2000, 66: 279-292. 10.1086/302698.PubMedCentralCrossRefPubMed
37.
go back to reference Ritchie MD, Hahn LW, Roodi N, Bailey LR, Dupont WD, Parl FF, Moore JH: Multifactor-dimensionality reduction reveals high-order interactions among estrogen-metabolism genes in sporadic breast cancer. Am J Hum Genet. 2001, 69: 138-147. 10.1086/321276.PubMedCentralCrossRefPubMed Ritchie MD, Hahn LW, Roodi N, Bailey LR, Dupont WD, Parl FF, Moore JH: Multifactor-dimensionality reduction reveals high-order interactions among estrogen-metabolism genes in sporadic breast cancer. Am J Hum Genet. 2001, 69: 138-147. 10.1086/321276.PubMedCentralCrossRefPubMed
38.
39.
go back to reference Jallow M, Teo YY, Small KS, Rockett KA, Deloukas P, Clark TG, Kivinen K, Bojang KA, Conway DJ, Pinder M, Sirugo G, Sisay-Joof F, Usen S, Auburn S, Bumpstead SJ, Campino S, Coffey A, Dunham A, Fry AE, Green A, Gwilliam R, Hunt SE, Inouye M, Jeffreys AE, Mendy A, Palotie A, Potter S, Ragoussis J, Rogers J, Rowlands K, Somaskantharajah E, Whittaker P, Widden C, Donnelly P, Howie B, Marchini J, Morris A, SanJoaquin M, Achidi EA, Agbenyega T, Allen A, Amodu O, Corran P, Djimde A, Dolo A, Doumbo OK, Drakeley C, Dunstan S, Evans J, Farrar J, Fernando D, Hien TT, Horstmann RD, Ibrahim M, Karunaweera N, Kokwaro G, Koram KA, Lemnge M, Makani J, Marsh K, Michon P, Modiano D, Molyneux ME, Mueller I, Parker M, Peshu N, Plowe CV, Puijalon O, Reeder J, Reyburn H, Riley EM, Sakuntabhai A, Singhasivanon P, Sirima S, Tall A, Taylor TE, Thera M, Troye-Blomberg M, Williams TN, Wilson M, Kwiatkowski DP: Genome-wide and fine-resolution association analysis of malaria in West Africa. Nat Genet. 2009, 41: 657-665. 10.1038/ng.388.PubMedCentralCrossRefPubMed Jallow M, Teo YY, Small KS, Rockett KA, Deloukas P, Clark TG, Kivinen K, Bojang KA, Conway DJ, Pinder M, Sirugo G, Sisay-Joof F, Usen S, Auburn S, Bumpstead SJ, Campino S, Coffey A, Dunham A, Fry AE, Green A, Gwilliam R, Hunt SE, Inouye M, Jeffreys AE, Mendy A, Palotie A, Potter S, Ragoussis J, Rogers J, Rowlands K, Somaskantharajah E, Whittaker P, Widden C, Donnelly P, Howie B, Marchini J, Morris A, SanJoaquin M, Achidi EA, Agbenyega T, Allen A, Amodu O, Corran P, Djimde A, Dolo A, Doumbo OK, Drakeley C, Dunstan S, Evans J, Farrar J, Fernando D, Hien TT, Horstmann RD, Ibrahim M, Karunaweera N, Kokwaro G, Koram KA, Lemnge M, Makani J, Marsh K, Michon P, Modiano D, Molyneux ME, Mueller I, Parker M, Peshu N, Plowe CV, Puijalon O, Reeder J, Reyburn H, Riley EM, Sakuntabhai A, Singhasivanon P, Sirima S, Tall A, Taylor TE, Thera M, Troye-Blomberg M, Williams TN, Wilson M, Kwiatkowski DP: Genome-wide and fine-resolution association analysis of malaria in West Africa. Nat Genet. 2009, 41: 657-665. 10.1038/ng.388.PubMedCentralCrossRefPubMed
40.
go back to reference Moon AF, Edavettal SC, Krahn JM, Munoz EM, Negishi M, Linhardt RJ, Liu J, Pedersen LC: Structural analysis of the sulfotransferase (3-o-sulfotransferase isoform 3) involved in the biosynthesis of an entry receptor for herpes simplex virus 1. J Biol Chem. 2004, 279: 45185-45193. 10.1074/jbc.M405013200.PubMedCentralCrossRefPubMed Moon AF, Edavettal SC, Krahn JM, Munoz EM, Negishi M, Linhardt RJ, Liu J, Pedersen LC: Structural analysis of the sulfotransferase (3-o-sulfotransferase isoform 3) involved in the biosynthesis of an entry receptor for herpes simplex virus 1. J Biol Chem. 2004, 279: 45185-45193. 10.1074/jbc.M405013200.PubMedCentralCrossRefPubMed
41.
go back to reference Pinzon-Ortiz C, Friedman J, Esko J, Sinnis P: The binding of the circumsporozoite protein to cell surface heparan sulphate proteoglycans is required for Plasmodium sporozoite attachment to target cells. J Biol Chem. 2001, 276: 26784-26791. 10.1074/jbc.M104038200.PubMedCentralCrossRefPubMed Pinzon-Ortiz C, Friedman J, Esko J, Sinnis P: The binding of the circumsporozoite protein to cell surface heparan sulphate proteoglycans is required for Plasmodium sporozoite attachment to target cells. J Biol Chem. 2001, 276: 26784-26791. 10.1074/jbc.M104038200.PubMedCentralCrossRefPubMed
42.
go back to reference Kulane A, Ekre HP, Perlmann P, Rombo L, Wahlgren M, Wahlin B: Effect of different fractions of heparin on Plasmodium falciparum merozoite invasion of red blood cells in vitro. AmJTrop Med Hyg. 1992, 46: 589-594. Kulane A, Ekre HP, Perlmann P, Rombo L, Wahlgren M, Wahlin B: Effect of different fractions of heparin on Plasmodium falciparum merozoite invasion of red blood cells in vitro. AmJTrop Med Hyg. 1992, 46: 589-594.
43.
go back to reference Xiao L, Yang C, Patterson PS, Udhayakumar V, Lal AA: Sulphated polyanions inhibit invasion of erythrocytes by plasmodial merozoites and cytoadherence of endothelial cells to parasitized erythrocytes. Infect Immun. 1996, 64: 1373-1378.PubMedCentralPubMed Xiao L, Yang C, Patterson PS, Udhayakumar V, Lal AA: Sulphated polyanions inhibit invasion of erythrocytes by plasmodial merozoites and cytoadherence of endothelial cells to parasitized erythrocytes. Infect Immun. 1996, 64: 1373-1378.PubMedCentralPubMed
45.
go back to reference Lortat-Jacob H: The molecular basis and functional implications of chemokine interactions with heparan sulphate. Curr Opin Struct Biol. 2009, 19: 543-548. 10.1016/j.sbi.2009.09.003.CrossRefPubMed Lortat-Jacob H: The molecular basis and functional implications of chemokine interactions with heparan sulphate. Curr Opin Struct Biol. 2009, 19: 543-548. 10.1016/j.sbi.2009.09.003.CrossRefPubMed
46.
go back to reference Joubert BR, Franceschini N, Mwapasa V, North KE, Meshnick SR: Regulation of CCR5 expression in human placenta: insights from a study of mother-to-child transmission of HIV in Malawi. PLoS One. 2010, 5: e9212-10.1371/journal.pone.0009212.PubMedCentralCrossRefPubMed Joubert BR, Franceschini N, Mwapasa V, North KE, Meshnick SR: Regulation of CCR5 expression in human placenta: insights from a study of mother-to-child transmission of HIV in Malawi. PLoS One. 2010, 5: e9212-10.1371/journal.pone.0009212.PubMedCentralCrossRefPubMed
47.
go back to reference Kaur G, Mehra N: Genetic determinants of HIV-1 infection and progression to AIDS: susceptibility to HIV infection. Tissue Antigens. 2009, 73: 289-301. 10.1111/j.1399-0039.2009.01220.x.CrossRefPubMed Kaur G, Mehra N: Genetic determinants of HIV-1 infection and progression to AIDS: susceptibility to HIV infection. Tissue Antigens. 2009, 73: 289-301. 10.1111/j.1399-0039.2009.01220.x.CrossRefPubMed
Metadata
Title
Genetic variations in genes involved in heparan sulphate biosynthesis are associated with Plasmodium falciparum parasitaemia: a familial study in Burkina Faso
Authors
Alexandre Atkinson
Séverine Garnier
Sarwat Afridi
Francis Fumoux
Pascal Rihet
Publication date
01-12-2012
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2012
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/1475-2875-11-108

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