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Garrido Zea, E. F. ., Rocha Orjuela, R. L. ., & Burgos Herrera, L. C. . (2017). Sulfato de heparán y sulfato de condroitina: aspectos generales de su participación durante el desarrollo de Plasmodium falciparum. Biosalud, 16(1), 80–90. https://doi.org/10.17151/biosa.2017.16.1.9
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La malaria es considerada una de las enfermedades infecciosas de mayor importancia alrededor del mundo debido a la alta morbimortalidad que causa cada año en países tropicales. A pesar de los esfuerzos de investigación en malaria, muchos de los mecanismos que entrañan las interacciones hospedero-parásito aún no son claros, lo que constituye un gran obstáculo en el manejo y control de la malaria. Numerosos estudios se han llevado a cabo en los últimos años en busca de una mejor comprensión de los mecanismos fisiopatológicos, diseño de nuevas drogas, diseño de una vacuna y bloqueo de la transmisión. En todos estos temas de investigación, un elemento común son los glicanos como moléculas clave en el ciclo de vida de los parásitos de la malaria. El objetivo de esta revisión es mostrar como los glicanos se necesitan para el desarrollo y la transmisión de Plasmodium y como esta información resulta ser una valiosa herramienta en la investigación para combatir la malaria. Métodos: La presente revisión se basó principalmente en artículos originales publicados entre 1985 y 2015, obtenidos de las bases de datos PubMed y EmBase. La búsqueda fue hecha en inglés y se usaron las palabras clave: glicanos sulfatados, malaria, Anopheles y Plasmodium. Conclusión: Los glicoconjugados sulfatados están íntimamente vinculados al desarrollo, la transmisión y la supervivencia de Plasmodium, tanto en el hospedero intermediario como en el hospedero definitivo. Una mejor comprensión del rol de los glicoconjugados sulfatados en la infección malárica permitiría el desarrollo de nuevas alternativas terapéuticas, así como el diseño de estrategias para inhibir la transmisión.
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1. Alam A. Serine Proteases of Malaria Parasite Plasmodium falciparum: Potential as Antimalarial Drug Targets. Hindawi Publ Corp. 2014; 2014:1–7.
2. Houzé S, Hoang N-T, Lozach O, Le Bras J, Meijer L, Galons H, et al. Several human cyclin-dependent kinase inhibitors, structurally related to roscovitine, as new anti-malarial agents. Molecules [Internet]. 2014 Jan [cited 2014 Dec 2]; 19(9):15237–57.
3. Gardner MJ, Hall N, Fung E, White O, Berriman M, Hyman RW, et al. Genome sequence of the humanmalaria parasite Plasmodium falciparum. Nature [Internet]. 2002 Oct 3; 419(6906):498–511.
4. Susomboon P, Iwagami M, Tangpukdee N, Krusood S, Looareesuwan S, Kano S. Differences in genetic population structures of Plasmodium falciparum isolates from patients along Thai-Myanmar border with severe or uncomplicated malaria. Malar J [Internet]. 2008 Jan [cited 2014 Dec 2]; 7:212.
5. Tao D, Ubaida-Mohien C, Mathias DK, King JG, Pastrana-Mena R, Tripathi A, et al. Sex-partitioning of the Plasmodium falciparum Stage V Gametocyte Proteome Provides Insight into falciparum-specific Cell Biology. Mol Cell Proteomics [Internet]. 2014; 13(10):2705–24.
6. Khan SM, Franke-Fayard B, Mair GR, Lasonder E, Janse CJ, Mann M, et al. Proteome analysis of separated male and female gametocytes reveals novel sex-specific Plasmodium biology. Cell [Internet]. 2005 Jun 3 [cited 2014 Dec 2]; 121(5):675–87.
7. Chen BQ, Barragan A, Fernandez V, Sundström A, Schlichtherle M, Sahlén A, et al. Identification of Plasmodium falciparum Erythrocyte Membrane Protein 1 (PfEMP1) as the Rosetting Ligand of the Malaria. J Exp M. 1998;187(1):15–23.
8. von Itzstein M, Plebanski M, Cooke BM, Coppel RL. Hot, sweet and sticky: the glycobiology of Plasmodium falciparum. Trends Parasitol [Internet]. 2008 May [cited 2014 Dec 2]; 24(5):210–8.
9. Dinglasan RRMJ-L. Flipping the paradigm on malaria transmission-blocking vaccines. Trends Parasitol. 2008; 24(8):364–70.
10. Dinglasan RR, Alaganan A, Ghosh AK, Saito A, van Kuppevelt TH, Jacobs-Lorena M. Plasmodium falciparum ookinetes require mosquito midgut chondroitin sulfate proteoglycans for cell invasion. Proc Natl Acad Sci U S A [Internet]. 2007 Oct 2; 104(40):15882–7.
11. Pinzon-Ortiz C1, Friedman J, Esko J SP. The binding of the circumsporozoite protein to cell surface heparan sulfate proteoglycans is required for plasmodium sporozoite attachment to target cells. J Biol Chem. 2014; 276(29):26784–91.
12. MacPherson GG, Warrell MJ, White NJ, Looareesuwan S, Warrell DA. Human cerebral malaria. A quantitative ultrastructural analysis of parasitized erythrocyte sequestration. Am J Pathol. 1985; 119(3):385–401.
13. Bannister LH, Sherman IW. Plasmodium. Encycl Life Sci. 2009; (December):1–12.
14. Mathews, CK; Van Holde, KE; Ahern KG. Biochemistry. 3rd ed. Madrid, Spain: Wesley; 2002. 335-48p.
15. Brooks S, Schumacher U. Functional and Molecular Glycobiology. First. Oxford , UK: BIOS Scientific Publishers Ltd; 2002. 160-9 p.
16. Chappell D, Jacob M, Becker BF, Hoffmann-Kiefer K, Conzen P. Expedition glycocalyx. A newly discovered “Great Barrier Reef”. Anaesthesist. 2008; 57(10):959–69.
17. Esko JD, Selleck SB. Order out of chaos: assembly of ligand binding sites in heparan sulfate. Annu Rev Biochem. 2002; 71:435–71.
18. Cohen M, Hurtado-Ziola N, Varki A. ABO blood group glycans modulate sialic acid recognition on erythrocytes. Blood. 2009; 114(17):3668–76.
19. Anstee DJ. The relationship between blood groups and disease. Blood. 2010; 115:4635–43.
20. Barragan A, Kremsner PG, Wahlgren M, Carlson J. Blood group A antigen is a coreceptor in Plasmodium falciparum rosetting. Infect Immun [Internet]. 2000 May; 68(5):2971–5.
21. Achur RN, Valiyaveettil M, Alkhalil A, Ockenhouse CF, Gowda DC. Characterization of proteoglycans of human placenta and identification of unique chondroitin sulfate proteoglycans of the intervillous spaces that mediate the adherence of Plasmodium falciparum-infected erythrocytes to the placenta. J Biol Chem [Internet]. 2000 Dec 22 [cited 2014 Dec 2]; 275(51):40344–56.
22. Mota MM, Rodriguez A. Migration through host cells: the first steps of Plasmodium sporozoites in the mammalian host. Cell Microbiol [Internet]. 2004 Dec [cited 2014 Dec 2]; 6(12):1113–8.
23. Rennenberg A, Lehmann C, Heitmann A, Witt T, Hansen G, Nagarajan K, et al. Exoerythrocytic Plasmodium parasites secrete a cysteine protease inhibitor involved in sporozoite invasion and capable of blocking cell death of host hepatocytes. PLoS Pathog [Internet]. 2010 Mar [cited 2014 Dec 2];6(3):e1000825.
24. Coppi A, Tewari R, Bishop JR, Bennett BL, Lawrence R. Heparan sulfate proteoglycans provide a signal to Plasmodium sporozoites to stop migrating and productively invade host cells. Cell Host Microbe. 2008; 2(5):316–27.
25. Srivastava A, Gangnard S, Round A, Dechavanne S, Juillerat A, Raynal B, et al. Full-length extracellular region of the var2CSA variant of PfEMP1 is required for specific, high-affinity binding to CSA. Proc Natl Acad Sci U S A [Internet]. 2010 Mar 16 [cited 2014 Dec 2]; 107(11):4884–9.
26. Vogt AM, Barragan A, Chen Q, Kironde F, Spillmann D, Wahlgren M. Heparan sulfate on endothelial cells mediates the binding of Plasmodium falciparum – infected erythrocytes via the DBL1 domain of PfEMP1. Blood. 2003; 101(6):2405–11.
27. Fried M, Duffy P. Adherence of Plasmodium falciparum to chondroitin sulfate A in the human placenta. Science (80- ) [Internet]. 1996 [cited 2014 Jun 17]; 272(June):1502–4.
28. Valiyaveettil M, Achur RN, Alkhalil A, Ockenhouse CF, Gowda DC. Plasmodium falciparum cytoadherence to human placenta: evaluation of hyaluronic acid and chondroitin 4-sulfate for binding of infected erythrocytes. Exp Parasitol [Internet]. 2001; 99(2):57–65.
29. Beeson JG, Rogerson SJ, Brown G V. Evaluating specific adhesion of Plasmodium falciparum-infected erythrocytes to immobilised hyaluronic acid with comparison to binding of mammalian cells. Int J Parasitol [Internet]. 2002 Sep; 32(10):1245–52.
30. Rogerson S, Chaiyaroj S. Chondroitin sulfate A is a cell surface receptor for Plasmodium falciparuminfected erythrocytes. J Exp Med [Internet]. 1995 [cited 2014 May 20]; 182(July):15–20.
31. Barragan A, Spillmann D, Kremsner PG, Wahlgren M, Carson J. Plasmodium falciparum: molecular background to strain-specific rosette disruption by glycosaminoglycans and sulfated glycoconjugates. Exp Parasitol. 1999; 91(2):133–43.
32. Jones CJ AJ. Glycosylation at the fetomaternal interface: does the glycocode play a critical role in implantation? Glycoconj J. 2009; 26(3):359–66.
33. Garrido E. Glicosaminoglicanos como posibles reguladores de inflamación durante la malaria placentaria. Rev Chil Obstet Ginecol [Internet]. 2014; 79(4):288–93.
34. Sinnis P, Coppi A, Toida T, Toyoda H, Kinoshita A. Mosquito heparan sulfate and its potential role in malaria infection and transmission. J Biol Chem. 2007; 282(35):25376–84.
35. Atkinson SC, Armistead JS, Mathias K., Sandeu MM, Tao D, Borhani-Dizaji N, et al. Structural analysis of Anopheles midgut aminopeptidase N reveals a novel malaria transmission-blocking vaccine B-cell epitope. Nat Struct Mol Biol. 2015; 22(7):532–9.
36. Landoni M, Duschak VG., Peres VJ., Nonami H, Erra-Balsells R, Katzin A, et al. Plasmodium falciparum biosynthesizes sulfoglycosphingolipids. Mol Biochem Parasitol. 2007; 154(1):22–9.
37. Shams-Eldina H, Santos de Macedo C, Niehus S, Dorna C, Kimmel J., Azzouz N, et al. Plasmodium falciparum dolichol phosphate mannose synthase represents a novel clade. Biochem Biophys Res Comun. 2008; 370(3):388–93.
38. Leitgeb AM, Blomqvist K, Cho-Ngwa F, Samje M, N de P, Titanji V, et al. Low anticoagulant heparin disrupts Plasmodium falciparum rosettes in fresh clinical isolates. Am J Trop Med Hyg [Internet]. 2011 Mar [cited 2016 May 12]; 84(3):390–6.
39. Valle-Delgado JJ, Urbán P, Fernàndez-Busquets X. Demonstration of specific binding of heparin to Plasmodium falciparum-infected vs. non-infected red blood cells by single-molecule force spectroscopy. Nanoscale [Internet]. 2013;5(9):3673–80.
40. Marques J, Moles E, Urban P, Prohens R, Busquets MA, Sevrin C, et al. Application of heparin as a dual agent with antimalarial and liposome targeting activities toward Plasmodium-infected red blood cells. Nanomedicine Nanotechnology, Biol Med [Internet]. 2014; 10(8):1719–28.
2. Houzé S, Hoang N-T, Lozach O, Le Bras J, Meijer L, Galons H, et al. Several human cyclin-dependent kinase inhibitors, structurally related to roscovitine, as new anti-malarial agents. Molecules [Internet]. 2014 Jan [cited 2014 Dec 2]; 19(9):15237–57.
3. Gardner MJ, Hall N, Fung E, White O, Berriman M, Hyman RW, et al. Genome sequence of the humanmalaria parasite Plasmodium falciparum. Nature [Internet]. 2002 Oct 3; 419(6906):498–511.
4. Susomboon P, Iwagami M, Tangpukdee N, Krusood S, Looareesuwan S, Kano S. Differences in genetic population structures of Plasmodium falciparum isolates from patients along Thai-Myanmar border with severe or uncomplicated malaria. Malar J [Internet]. 2008 Jan [cited 2014 Dec 2]; 7:212.
5. Tao D, Ubaida-Mohien C, Mathias DK, King JG, Pastrana-Mena R, Tripathi A, et al. Sex-partitioning of the Plasmodium falciparum Stage V Gametocyte Proteome Provides Insight into falciparum-specific Cell Biology. Mol Cell Proteomics [Internet]. 2014; 13(10):2705–24.
6. Khan SM, Franke-Fayard B, Mair GR, Lasonder E, Janse CJ, Mann M, et al. Proteome analysis of separated male and female gametocytes reveals novel sex-specific Plasmodium biology. Cell [Internet]. 2005 Jun 3 [cited 2014 Dec 2]; 121(5):675–87.
7. Chen BQ, Barragan A, Fernandez V, Sundström A, Schlichtherle M, Sahlén A, et al. Identification of Plasmodium falciparum Erythrocyte Membrane Protein 1 (PfEMP1) as the Rosetting Ligand of the Malaria. J Exp M. 1998;187(1):15–23.
8. von Itzstein M, Plebanski M, Cooke BM, Coppel RL. Hot, sweet and sticky: the glycobiology of Plasmodium falciparum. Trends Parasitol [Internet]. 2008 May [cited 2014 Dec 2]; 24(5):210–8.
9. Dinglasan RRMJ-L. Flipping the paradigm on malaria transmission-blocking vaccines. Trends Parasitol. 2008; 24(8):364–70.
10. Dinglasan RR, Alaganan A, Ghosh AK, Saito A, van Kuppevelt TH, Jacobs-Lorena M. Plasmodium falciparum ookinetes require mosquito midgut chondroitin sulfate proteoglycans for cell invasion. Proc Natl Acad Sci U S A [Internet]. 2007 Oct 2; 104(40):15882–7.
11. Pinzon-Ortiz C1, Friedman J, Esko J SP. The binding of the circumsporozoite protein to cell surface heparan sulfate proteoglycans is required for plasmodium sporozoite attachment to target cells. J Biol Chem. 2014; 276(29):26784–91.
12. MacPherson GG, Warrell MJ, White NJ, Looareesuwan S, Warrell DA. Human cerebral malaria. A quantitative ultrastructural analysis of parasitized erythrocyte sequestration. Am J Pathol. 1985; 119(3):385–401.
13. Bannister LH, Sherman IW. Plasmodium. Encycl Life Sci. 2009; (December):1–12.
14. Mathews, CK; Van Holde, KE; Ahern KG. Biochemistry. 3rd ed. Madrid, Spain: Wesley; 2002. 335-48p.
15. Brooks S, Schumacher U. Functional and Molecular Glycobiology. First. Oxford , UK: BIOS Scientific Publishers Ltd; 2002. 160-9 p.
16. Chappell D, Jacob M, Becker BF, Hoffmann-Kiefer K, Conzen P. Expedition glycocalyx. A newly discovered “Great Barrier Reef”. Anaesthesist. 2008; 57(10):959–69.
17. Esko JD, Selleck SB. Order out of chaos: assembly of ligand binding sites in heparan sulfate. Annu Rev Biochem. 2002; 71:435–71.
18. Cohen M, Hurtado-Ziola N, Varki A. ABO blood group glycans modulate sialic acid recognition on erythrocytes. Blood. 2009; 114(17):3668–76.
19. Anstee DJ. The relationship between blood groups and disease. Blood. 2010; 115:4635–43.
20. Barragan A, Kremsner PG, Wahlgren M, Carlson J. Blood group A antigen is a coreceptor in Plasmodium falciparum rosetting. Infect Immun [Internet]. 2000 May; 68(5):2971–5.
21. Achur RN, Valiyaveettil M, Alkhalil A, Ockenhouse CF, Gowda DC. Characterization of proteoglycans of human placenta and identification of unique chondroitin sulfate proteoglycans of the intervillous spaces that mediate the adherence of Plasmodium falciparum-infected erythrocytes to the placenta. J Biol Chem [Internet]. 2000 Dec 22 [cited 2014 Dec 2]; 275(51):40344–56.
22. Mota MM, Rodriguez A. Migration through host cells: the first steps of Plasmodium sporozoites in the mammalian host. Cell Microbiol [Internet]. 2004 Dec [cited 2014 Dec 2]; 6(12):1113–8.
23. Rennenberg A, Lehmann C, Heitmann A, Witt T, Hansen G, Nagarajan K, et al. Exoerythrocytic Plasmodium parasites secrete a cysteine protease inhibitor involved in sporozoite invasion and capable of blocking cell death of host hepatocytes. PLoS Pathog [Internet]. 2010 Mar [cited 2014 Dec 2];6(3):e1000825.
24. Coppi A, Tewari R, Bishop JR, Bennett BL, Lawrence R. Heparan sulfate proteoglycans provide a signal to Plasmodium sporozoites to stop migrating and productively invade host cells. Cell Host Microbe. 2008; 2(5):316–27.
25. Srivastava A, Gangnard S, Round A, Dechavanne S, Juillerat A, Raynal B, et al. Full-length extracellular region of the var2CSA variant of PfEMP1 is required for specific, high-affinity binding to CSA. Proc Natl Acad Sci U S A [Internet]. 2010 Mar 16 [cited 2014 Dec 2]; 107(11):4884–9.
26. Vogt AM, Barragan A, Chen Q, Kironde F, Spillmann D, Wahlgren M. Heparan sulfate on endothelial cells mediates the binding of Plasmodium falciparum – infected erythrocytes via the DBL1 domain of PfEMP1. Blood. 2003; 101(6):2405–11.
27. Fried M, Duffy P. Adherence of Plasmodium falciparum to chondroitin sulfate A in the human placenta. Science (80- ) [Internet]. 1996 [cited 2014 Jun 17]; 272(June):1502–4.
28. Valiyaveettil M, Achur RN, Alkhalil A, Ockenhouse CF, Gowda DC. Plasmodium falciparum cytoadherence to human placenta: evaluation of hyaluronic acid and chondroitin 4-sulfate for binding of infected erythrocytes. Exp Parasitol [Internet]. 2001; 99(2):57–65.
29. Beeson JG, Rogerson SJ, Brown G V. Evaluating specific adhesion of Plasmodium falciparum-infected erythrocytes to immobilised hyaluronic acid with comparison to binding of mammalian cells. Int J Parasitol [Internet]. 2002 Sep; 32(10):1245–52.
30. Rogerson S, Chaiyaroj S. Chondroitin sulfate A is a cell surface receptor for Plasmodium falciparuminfected erythrocytes. J Exp Med [Internet]. 1995 [cited 2014 May 20]; 182(July):15–20.
31. Barragan A, Spillmann D, Kremsner PG, Wahlgren M, Carson J. Plasmodium falciparum: molecular background to strain-specific rosette disruption by glycosaminoglycans and sulfated glycoconjugates. Exp Parasitol. 1999; 91(2):133–43.
32. Jones CJ AJ. Glycosylation at the fetomaternal interface: does the glycocode play a critical role in implantation? Glycoconj J. 2009; 26(3):359–66.
33. Garrido E. Glicosaminoglicanos como posibles reguladores de inflamación durante la malaria placentaria. Rev Chil Obstet Ginecol [Internet]. 2014; 79(4):288–93.
34. Sinnis P, Coppi A, Toida T, Toyoda H, Kinoshita A. Mosquito heparan sulfate and its potential role in malaria infection and transmission. J Biol Chem. 2007; 282(35):25376–84.
35. Atkinson SC, Armistead JS, Mathias K., Sandeu MM, Tao D, Borhani-Dizaji N, et al. Structural analysis of Anopheles midgut aminopeptidase N reveals a novel malaria transmission-blocking vaccine B-cell epitope. Nat Struct Mol Biol. 2015; 22(7):532–9.
36. Landoni M, Duschak VG., Peres VJ., Nonami H, Erra-Balsells R, Katzin A, et al. Plasmodium falciparum biosynthesizes sulfoglycosphingolipids. Mol Biochem Parasitol. 2007; 154(1):22–9.
37. Shams-Eldina H, Santos de Macedo C, Niehus S, Dorna C, Kimmel J., Azzouz N, et al. Plasmodium falciparum dolichol phosphate mannose synthase represents a novel clade. Biochem Biophys Res Comun. 2008; 370(3):388–93.
38. Leitgeb AM, Blomqvist K, Cho-Ngwa F, Samje M, N de P, Titanji V, et al. Low anticoagulant heparin disrupts Plasmodium falciparum rosettes in fresh clinical isolates. Am J Trop Med Hyg [Internet]. 2011 Mar [cited 2016 May 12]; 84(3):390–6.
39. Valle-Delgado JJ, Urbán P, Fernàndez-Busquets X. Demonstration of specific binding of heparin to Plasmodium falciparum-infected vs. non-infected red blood cells by single-molecule force spectroscopy. Nanoscale [Internet]. 2013;5(9):3673–80.
40. Marques J, Moles E, Urban P, Prohens R, Busquets MA, Sevrin C, et al. Application of heparin as a dual agent with antimalarial and liposome targeting activities toward Plasmodium-infected red blood cells. Nanomedicine Nanotechnology, Biol Med [Internet]. 2014; 10(8):1719–28.
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