Comparación de los perfiles de transcripción de pacientes con fiebre de dengue y fiebre hemorrágica por dengue que muestra diferencias en la respuesta inmunitaria y claves en la inmunopatogénesis
Palabras clave:
dengue, transcripción genética, análisis de micromatrices, fiebre hemorrágica del dengue, proteínas del sistema del complemento, citocinas
Resumen
Introducción. El dengue puede manifestarse como una enfermedad leve o evolucionar hasta una enfermedad grave, llamada fiebre hemorrágica por dengue, cuyos mecanismos de inmunopatogénesis no son claros.
Objetivo. Utilizar un análisis de microarreglos para identificar los genes de la respuesta inmunitaria diferencialmente expresados en niños colombianos con dengue leve y grave.
Materiales y métodos. Se evaluaron los cambios de la expresión génica de células mononucleares de sangre periférica de niños con fiebre de dengue y fiebre hemorrágica por dengue en fase aguda, mediante el microarreglo de Affymetrix HG-U133_Plus_2.
Resultados. Los pacientes con fiebre hemorrágica por dengue expresaron transcritos para interleucina 6, quimiocinas, complemento y pentraxina 3, al igual que inhibidores de la actividad de linfocitos (gen 3 de activación de linfocitos y catepsina L1). Un modelo de interacción desarrollado para estos genes mostró al factor tisular como central en la red generada. Por el contrario, los pacientes con fiebre de dengue expresaron inhibidores de la actividad de citocinas, complemento y leucotrienos [lactotransferrina, inhibidor peptidasa serpina del complemento C1, leucotrieno B (4-omega hidroxilasa 2)].
Conclusiones. Los resultados podrían indicar que durante la fiebre de dengue, los inhibidores de citocinas y del complemento logran controlar el daño al endotelio y el aumento de la permeabilidad vascular, mientras que, en los pacientes con fiebre hemorrágica por dengue, la disfunción de las células inmunitarias y la acción no regulada del complemento y de las citocinas, conducen a un estado de "hipercoagulacion" y daño endotelial. La identificación del papel patógeno de las moléculas encontradas podría contribuir a la interpretación de la patogenia y al desarrollo de fármacos terapéuticos.
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Referencias bibliográficas
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4. Kurane I. Dengue hemorrhagic fever with special emphasis on immunopathogenesis. Comp Immunol Microbiol Infect Dis. 2007;30:329-40.
5. Green S, Rothman A. Immunopathological mechanisms in dengue and dengue hemorrhagic fever. Curr Opin Infect Dis. 2006;19:429-36.
6. Kliks SC, Nimmanitya S, Nisalak A, Burke DS. Evidence that maternal dengue antibodies are important in the development of dengue hemorrhagic fever in infants. Am J Trop Med Hyg. 1988;38:411-9.
7. Organización Mundial de la Salud. Dengue hemorrhagic fever: Diagnosis, treatment, prevention and control. Chapter 2. Clinical diagnosis. Geneve: World Health Organization; 1997. Fecha de consulta: 12 de noviembre de 2008. Disponible en: http://www.who.int/csr/resources/publications/dengue/012-23.pdf.
8. Chien LJ, Liao TL, Shu PY, Huang JH, Gubler DJ, Chang GJ. Development of real-time reverse transcriptase PCR assays to detect and serotype dengue viruses J Clin Microbiol. 2006;44:1295-304.
9. Prada-Arismendy J, Castellanos JE. Real time PCR. Application in dengue studies. Colomb Med. 2010, in press.
10. Chen RF, Liu JW, Yeh WT, Wang L, Chang JC, Yu HR, et al. Altered T helper 1 reaction but not increase of virus load in patients with dengue hemorrhagic fever. FEMS Immunol Med Microbiol. 2005;44:43-50.
11. Warke RV, Xhaja K, Martin KJ, Fournier MF, Shaw SK, Brizuela N, et al. Dengue virus induces novel changes in gene expression of human umbilical vein endothelial cells. J Virol. 2003;77:11822-32.
12. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics. 2003;4:249-64.
13. Hosack DA, Dennis G Jr, Sherman BT, Lane HC, Lempicki RA. Identifying biological themes within lists of genes with EASE. Genome Biol. 2003;4:R70.
14. Hayden MS, West AP, Ghosh S. NF-kappaB and the immune response. Oncogene. 2006;25:6758-80.
15. Wang M, Windgassen D, Papoutsakis ET. Comparative analysis of transcriptional profiling of CD3+, CD4+ and CD8+ T cells identifies novel immune response players in T-cell activation. BMC Genomics. 2008;9:225.
16. Zenz R, Eferl R, Scheinecker C, Redlich K, Smolen J, Schonthaler HB, et al. Activator protein 1 (Fos/Jun) functions in inflammatory bone and skin disease. Arthritis Res Ther. 2008;10:201-6.
17. Bozza FA, Cruz OG, Zagne SM, Azeredo EL, Nogueira RM, Assis EF, et al. Multiplex cytokine profile from dengue patients: MIP-1beta and IFN-gamma as predictive factors for severity. BMC Infect Dis. 2008;8:86-97.
18. Liou JT, Chen ZY, Ho LJ, Yang SP, Chang DM, Liang CC, et al. Differential effects of triptolide and tetrandrine on activation of COX-2, NF-kappaB, and AP-1 and virus production in dengue virus-infected human lung cells. Eur J Pharmacol. 2008;589:288-98.
19. Raghupathy R, Chaturvedi UC, Al-Sayer H, Elbishbishi EA, Agarwal R, Nagar R, et al. Elevated levels of IL-8 in dengue hemorrhagic fever. J Med Virol. 1998;56:280-5.
20. Suharti C, van Gorp EC, Setiati TE, Dolmans WM, Djokomoeljanto RJ, Hack CE, et al. The role of cytokines in activation of coagulation and fibrinolysis in dengue shock syndrome. Thromb Haemost. 2002;87:42-6.
21. Coornaert B, Carpentier I, Beyaert R. A20: Central gatekeeper in inflammation and immunity. J Biol Chem. 2009;284:8217-21.
22. Milner CM, Higman VA, Day AJ. TSG-6: a pluripotent inflammatory mediator? Biochem Soc Trans. 2006;34:446-50.
23. Yasui K, Baba A. Therapeutic potential of superoxide dismutase (SOD) for resolution of inflammation. Inflamm Res. 2006;55:359-63.
24. Gough SC, Walker LS, Sansom DM. CTLA4 gene polymorphism and autoimmunity. Immunol Rev. 2005;204:102-15.
25. Fujimoto Y, Tedder TF. CD83: A regulatory molecule of the immune system with great potential for therapeutic application. J Med Dent Sci. 2006;53:85-91.
26. Puddu P, Valenti P, Gessani S. Immunomodulatory effects of lactoferrin on antigen presenting cells. Biochimie. 2009;91:11-8.
27. Christmas P, Tolentino K, Primo V, Berry KZ, Murphy RC, Chen M, et al. Cytochrome P-450 4F18 is the leukotriene B4 omega-1/omega-2 hydroxylase in mouse polymorphonuclear leukocytes: identification as the functional orthologue of human polymorphonuclear leukocyte CYP4F3A in the down-regulation of responses to LTB4. J Biol Chem. 2006;281:7189-96.
28. Cheng ZD, Liu MY, Chen G, Zhang HM, Qin GJ, Liang G, et al. Anti-vascular permeability of the cleaved reactive center loop within the carboxyl-terminal domain of C1 inhibitor. Mol Immunol. 2008;45:1743-51.
29. Ubol S, Masrinoul P, Chaijaruwanich J, Kalayanarooj S, Charoensirisuthikul T, Kasisith J. Differences in global gene expression in peripheral blood mononuclear cells indicate a significant role of the innate responses in progression of dengue fever but not dengue hemorrhagic fever. J Infect Dis. 2008;197:1459-67.
30. Long HT, Hibberd ML, Hien TT, Dung NM, Van Ngoc T, Farrar J, et al. Patterns of gene transcript abundance in the blood of children with severe or uncomplicated dengue highlight differences in disease evolution and host response to dengue virus infection. J Infect Dis. 2009;199:537-46.
31. Suharti C, van Gorp EC, Dolmans WM, Setiati TE, Hack CE, Djokomoeljanto R, et al. Cytokine patterns during dengue shock syndrome. Eur Cytokine Netw. 2003;14:172-7.
32. Lee YR, Liu MT, Lei HY, Liu CC, Wu JM, Lin YS, et al. MCP-1, a highly expressed chemokine in dengue haemorrhagic fever/dengue shock syndrome patients, may cause permeability change, possibly through reduced tight junctions of vascular endothelium cells. J Gen Virol. 2006;87:3623-30.
33. Avirutnan P, Punyadee N, Noisakran S, Komoltri C, Thiemmeca S, Auethavornanan K, et al. Vascular leakage in severe dengue virus infections: A potential role for the nonstructural viral protein NS1 and complement. J Infect Dis. 2006;193:1078-88.
34. Mairuhu AT, Peri G, Setiati TE, Hack CE, Koraka P, Soemantri A, et al. Elevated plasma levels of the long pentraxin, pentraxin 3, in severe dengue virus infections. J Med Virol. 2005;76:547-52.
35. Krzewski K, Chen X, Strominger JL. WIP is essential for lytic granule polarization and NK cell cytotoxicity. Proc Natl Acad Sci USA. 2008;105:2568-73.
36. Jovic M, Naslavsky N, Rapaport D, Horowitz M, Caplan S. EHD1 regulates beta1 integrin endosomal transport: effects on focal adhesions, cell spreading and migration. J Cell Sci. 2007;120:802-14.
37. Jiang Z, Johnson HJ, Nie H, Qin J, Bird TA, Li X. Pellino 1 is required for interleukin-1 (IL-1)-mediated signaling through its interaction with the IL-1 receptor-associated kinase 4 (IRAK4)-IRAK-tumor necrosis factor receptor-associated factor 6 (TRAF6) complex. J Biol Chem. 2003;278:10952-6.
38. Lopes CC, Dietrich CP, Nader HB. Specific structural features of syndecans and heparan sulfate chains are needed for cell signaling. Braz J Med Biol Res. 2006;39:157-67.
39. Green S, Pichyangkul S, Vaughn DW, Kalayanarooj S, Nimmannitya S, Nisalak A, et al. Early CD69 expression on peripheral blood lymphocytes from children with dengue hemorrhagic fever. J Infect Dis. 1999;180:1429-35.
40. Mathew A, Kurane I, Green S, Vaughn DW, Kalayanarooj S, Suntayakorn S, et al. Impaired T cell proliferation in acute dengue infection. J Immunol. 1999;162:5609-15.
41. Simmons CP, Dong T, Chau NV, Dung NT, Chau TN, Thao le TT, et al. Early T-cell responses to dengue virus epitopes in Vietnamese adults with secondary dengue virus infections. J Virol. 2005;79:5665-75.
42. Workman CJ, Cauley LS, Kim IJ, Blackman MA, Woodland DL, Vignali DA. Lymphocyte activation gene-3 (CD223) regulates the size of the expanding T cell population following antigen activation in vivo. J Immunol. 2004;172:5450-5.
43. Dinarello CA. Blocking IL-1 in systemic inflammation. J Exp Med. 2005;201:1355-9.
44. Michallet MC, Saltel F, Flacher M, Revillard JP, Genestier L. Cathepsin-dependent apoptosis triggered by supraoptimal activation of T lymphocytes: a possible mechanism of high dose tolerance. J Immunol. 2004;172:5405-14.
45. Simmons CP, Popper S, Dolocek C, Chau TN, Griffiths M, Dung NT, et al. Patterns of host genome-wide gene transcript abundance in the peripheral blood of patients with acute dengue hemorrhagic fever. J Infect Dis. 2007;195:1097-107.
46. Becerra A, Warke RV, Martin K, Xhaja K, de Bosch N, Rothman AL, et al. Gene expression profiling of dengue infected human primary cells identifies secreted mediators in vivo. J Med Virol. 2009;81:1403-11.
47. Maly MA, Tomasov P, Hájek P, Blasko P, Hrachovinová I, Salaj P, et al. The role of tissue factor in thrombosis and hemostasis. Physiol Res. 2007;56:685-95.
48. Schouten M, Wiersinga WJ, Levi M, van der Poll T. Inflammation, endothelium, and coagulation in sepsis. J Leukoc Biol. 2008;83:536-45.
49. Suharti C, van Gorp EC, Setiati TE, Dolmans WM, Djokomoeljanto RJ, Hack CE, et al. The role of cytokines in activation of coagulation and fibrinolysis in dengue shock syndrome. Thromb Haemost. 2002;87:42-6.
50. Sosothikul D, Seksarn P, Pongsewalak S, Thisyakorn U, Lusher J. Activation of endothelial cells, coagulation and fibrinolysis in children with dengue virus infection.Thromb Haemost. 2007;97:627-34.
51. Srichaikul T, Nimmannitya S. Haematology in dengue and dengue haemorrhagic fever. Baillieres Best Pract Res Clin Haematol. 2000;13:261-76.
52. Hetland O, Brovold AB, Holme R, Gaudernack G, Prydz H. Thromboplastin (tissue factor) in plasma membranes of human monocytes. Biochem J. 1985;228:735-43.
2. Organización Mundial de la Salud. Dengue hemorrhagic fever and dengue shock syndrome in the context of the integrated management of childhood illness. Ginebra: World Health Organization; 2005. Fecha de consulta: 7 de febrero de 2009. Disponible en: http://www.who.int/childadolescenthealth/New_Publications/CHILD_HEALTH/DP/WHO_FCH_CAH_013.pdf.
3. Martínez-Gutiérrez M, Castellanos JE. Dengue hemorrágico. ¿Una aberración inmunológica? Revista Escuela Colombiana de Medicina. 2006;11:10-9.
4. Kurane I. Dengue hemorrhagic fever with special emphasis on immunopathogenesis. Comp Immunol Microbiol Infect Dis. 2007;30:329-40.
5. Green S, Rothman A. Immunopathological mechanisms in dengue and dengue hemorrhagic fever. Curr Opin Infect Dis. 2006;19:429-36.
6. Kliks SC, Nimmanitya S, Nisalak A, Burke DS. Evidence that maternal dengue antibodies are important in the development of dengue hemorrhagic fever in infants. Am J Trop Med Hyg. 1988;38:411-9.
7. Organización Mundial de la Salud. Dengue hemorrhagic fever: Diagnosis, treatment, prevention and control. Chapter 2. Clinical diagnosis. Geneve: World Health Organization; 1997. Fecha de consulta: 12 de noviembre de 2008. Disponible en: http://www.who.int/csr/resources/publications/dengue/012-23.pdf.
8. Chien LJ, Liao TL, Shu PY, Huang JH, Gubler DJ, Chang GJ. Development of real-time reverse transcriptase PCR assays to detect and serotype dengue viruses J Clin Microbiol. 2006;44:1295-304.
9. Prada-Arismendy J, Castellanos JE. Real time PCR. Application in dengue studies. Colomb Med. 2010, in press.
10. Chen RF, Liu JW, Yeh WT, Wang L, Chang JC, Yu HR, et al. Altered T helper 1 reaction but not increase of virus load in patients with dengue hemorrhagic fever. FEMS Immunol Med Microbiol. 2005;44:43-50.
11. Warke RV, Xhaja K, Martin KJ, Fournier MF, Shaw SK, Brizuela N, et al. Dengue virus induces novel changes in gene expression of human umbilical vein endothelial cells. J Virol. 2003;77:11822-32.
12. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics. 2003;4:249-64.
13. Hosack DA, Dennis G Jr, Sherman BT, Lane HC, Lempicki RA. Identifying biological themes within lists of genes with EASE. Genome Biol. 2003;4:R70.
14. Hayden MS, West AP, Ghosh S. NF-kappaB and the immune response. Oncogene. 2006;25:6758-80.
15. Wang M, Windgassen D, Papoutsakis ET. Comparative analysis of transcriptional profiling of CD3+, CD4+ and CD8+ T cells identifies novel immune response players in T-cell activation. BMC Genomics. 2008;9:225.
16. Zenz R, Eferl R, Scheinecker C, Redlich K, Smolen J, Schonthaler HB, et al. Activator protein 1 (Fos/Jun) functions in inflammatory bone and skin disease. Arthritis Res Ther. 2008;10:201-6.
17. Bozza FA, Cruz OG, Zagne SM, Azeredo EL, Nogueira RM, Assis EF, et al. Multiplex cytokine profile from dengue patients: MIP-1beta and IFN-gamma as predictive factors for severity. BMC Infect Dis. 2008;8:86-97.
18. Liou JT, Chen ZY, Ho LJ, Yang SP, Chang DM, Liang CC, et al. Differential effects of triptolide and tetrandrine on activation of COX-2, NF-kappaB, and AP-1 and virus production in dengue virus-infected human lung cells. Eur J Pharmacol. 2008;589:288-98.
19. Raghupathy R, Chaturvedi UC, Al-Sayer H, Elbishbishi EA, Agarwal R, Nagar R, et al. Elevated levels of IL-8 in dengue hemorrhagic fever. J Med Virol. 1998;56:280-5.
20. Suharti C, van Gorp EC, Setiati TE, Dolmans WM, Djokomoeljanto RJ, Hack CE, et al. The role of cytokines in activation of coagulation and fibrinolysis in dengue shock syndrome. Thromb Haemost. 2002;87:42-6.
21. Coornaert B, Carpentier I, Beyaert R. A20: Central gatekeeper in inflammation and immunity. J Biol Chem. 2009;284:8217-21.
22. Milner CM, Higman VA, Day AJ. TSG-6: a pluripotent inflammatory mediator? Biochem Soc Trans. 2006;34:446-50.
23. Yasui K, Baba A. Therapeutic potential of superoxide dismutase (SOD) for resolution of inflammation. Inflamm Res. 2006;55:359-63.
24. Gough SC, Walker LS, Sansom DM. CTLA4 gene polymorphism and autoimmunity. Immunol Rev. 2005;204:102-15.
25. Fujimoto Y, Tedder TF. CD83: A regulatory molecule of the immune system with great potential for therapeutic application. J Med Dent Sci. 2006;53:85-91.
26. Puddu P, Valenti P, Gessani S. Immunomodulatory effects of lactoferrin on antigen presenting cells. Biochimie. 2009;91:11-8.
27. Christmas P, Tolentino K, Primo V, Berry KZ, Murphy RC, Chen M, et al. Cytochrome P-450 4F18 is the leukotriene B4 omega-1/omega-2 hydroxylase in mouse polymorphonuclear leukocytes: identification as the functional orthologue of human polymorphonuclear leukocyte CYP4F3A in the down-regulation of responses to LTB4. J Biol Chem. 2006;281:7189-96.
28. Cheng ZD, Liu MY, Chen G, Zhang HM, Qin GJ, Liang G, et al. Anti-vascular permeability of the cleaved reactive center loop within the carboxyl-terminal domain of C1 inhibitor. Mol Immunol. 2008;45:1743-51.
29. Ubol S, Masrinoul P, Chaijaruwanich J, Kalayanarooj S, Charoensirisuthikul T, Kasisith J. Differences in global gene expression in peripheral blood mononuclear cells indicate a significant role of the innate responses in progression of dengue fever but not dengue hemorrhagic fever. J Infect Dis. 2008;197:1459-67.
30. Long HT, Hibberd ML, Hien TT, Dung NM, Van Ngoc T, Farrar J, et al. Patterns of gene transcript abundance in the blood of children with severe or uncomplicated dengue highlight differences in disease evolution and host response to dengue virus infection. J Infect Dis. 2009;199:537-46.
31. Suharti C, van Gorp EC, Dolmans WM, Setiati TE, Hack CE, Djokomoeljanto R, et al. Cytokine patterns during dengue shock syndrome. Eur Cytokine Netw. 2003;14:172-7.
32. Lee YR, Liu MT, Lei HY, Liu CC, Wu JM, Lin YS, et al. MCP-1, a highly expressed chemokine in dengue haemorrhagic fever/dengue shock syndrome patients, may cause permeability change, possibly through reduced tight junctions of vascular endothelium cells. J Gen Virol. 2006;87:3623-30.
33. Avirutnan P, Punyadee N, Noisakran S, Komoltri C, Thiemmeca S, Auethavornanan K, et al. Vascular leakage in severe dengue virus infections: A potential role for the nonstructural viral protein NS1 and complement. J Infect Dis. 2006;193:1078-88.
34. Mairuhu AT, Peri G, Setiati TE, Hack CE, Koraka P, Soemantri A, et al. Elevated plasma levels of the long pentraxin, pentraxin 3, in severe dengue virus infections. J Med Virol. 2005;76:547-52.
35. Krzewski K, Chen X, Strominger JL. WIP is essential for lytic granule polarization and NK cell cytotoxicity. Proc Natl Acad Sci USA. 2008;105:2568-73.
36. Jovic M, Naslavsky N, Rapaport D, Horowitz M, Caplan S. EHD1 regulates beta1 integrin endosomal transport: effects on focal adhesions, cell spreading and migration. J Cell Sci. 2007;120:802-14.
37. Jiang Z, Johnson HJ, Nie H, Qin J, Bird TA, Li X. Pellino 1 is required for interleukin-1 (IL-1)-mediated signaling through its interaction with the IL-1 receptor-associated kinase 4 (IRAK4)-IRAK-tumor necrosis factor receptor-associated factor 6 (TRAF6) complex. J Biol Chem. 2003;278:10952-6.
38. Lopes CC, Dietrich CP, Nader HB. Specific structural features of syndecans and heparan sulfate chains are needed for cell signaling. Braz J Med Biol Res. 2006;39:157-67.
39. Green S, Pichyangkul S, Vaughn DW, Kalayanarooj S, Nimmannitya S, Nisalak A, et al. Early CD69 expression on peripheral blood lymphocytes from children with dengue hemorrhagic fever. J Infect Dis. 1999;180:1429-35.
40. Mathew A, Kurane I, Green S, Vaughn DW, Kalayanarooj S, Suntayakorn S, et al. Impaired T cell proliferation in acute dengue infection. J Immunol. 1999;162:5609-15.
41. Simmons CP, Dong T, Chau NV, Dung NT, Chau TN, Thao le TT, et al. Early T-cell responses to dengue virus epitopes in Vietnamese adults with secondary dengue virus infections. J Virol. 2005;79:5665-75.
42. Workman CJ, Cauley LS, Kim IJ, Blackman MA, Woodland DL, Vignali DA. Lymphocyte activation gene-3 (CD223) regulates the size of the expanding T cell population following antigen activation in vivo. J Immunol. 2004;172:5450-5.
43. Dinarello CA. Blocking IL-1 in systemic inflammation. J Exp Med. 2005;201:1355-9.
44. Michallet MC, Saltel F, Flacher M, Revillard JP, Genestier L. Cathepsin-dependent apoptosis triggered by supraoptimal activation of T lymphocytes: a possible mechanism of high dose tolerance. J Immunol. 2004;172:5405-14.
45. Simmons CP, Popper S, Dolocek C, Chau TN, Griffiths M, Dung NT, et al. Patterns of host genome-wide gene transcript abundance in the peripheral blood of patients with acute dengue hemorrhagic fever. J Infect Dis. 2007;195:1097-107.
46. Becerra A, Warke RV, Martin K, Xhaja K, de Bosch N, Rothman AL, et al. Gene expression profiling of dengue infected human primary cells identifies secreted mediators in vivo. J Med Virol. 2009;81:1403-11.
47. Maly MA, Tomasov P, Hájek P, Blasko P, Hrachovinová I, Salaj P, et al. The role of tissue factor in thrombosis and hemostasis. Physiol Res. 2007;56:685-95.
48. Schouten M, Wiersinga WJ, Levi M, van der Poll T. Inflammation, endothelium, and coagulation in sepsis. J Leukoc Biol. 2008;83:536-45.
49. Suharti C, van Gorp EC, Setiati TE, Dolmans WM, Djokomoeljanto RJ, Hack CE, et al. The role of cytokines in activation of coagulation and fibrinolysis in dengue shock syndrome. Thromb Haemost. 2002;87:42-6.
50. Sosothikul D, Seksarn P, Pongsewalak S, Thisyakorn U, Lusher J. Activation of endothelial cells, coagulation and fibrinolysis in children with dengue virus infection.Thromb Haemost. 2007;97:627-34.
51. Srichaikul T, Nimmannitya S. Haematology in dengue and dengue haemorrhagic fever. Baillieres Best Pract Res Clin Haematol. 2000;13:261-76.
52. Hetland O, Brovold AB, Holme R, Gaudernack G, Prydz H. Thromboplastin (tissue factor) in plasma membranes of human monocytes. Biochem J. 1985;228:735-43.
Cómo citar
1.
Houghton-Triviño N, Martín K, Giaya K, Rodríguez JA, Bosch I, Castellanos JE. Comparación de los perfiles de transcripción de pacientes con fiebre de dengue y fiebre hemorrágica por dengue que muestra diferencias en la respuesta inmunitaria y claves en la inmunopatogénesis. Biomed. [Internet]. 1 de diciembre de 2010 [citado 6 de abril de 2025];30(4):587-97. Disponible en: https://revistabiomedicaorg.biteca.online/index.php/biomedica/article/view/297
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2010-12-01
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