Pregnancy enhances the innate immune response in experimental cutaneous leishmaniasis through hormone-modulated nitric oxide production

Journal of Leukocyte Biology

Volumn 83, Issue 6, 2008, Pages 1413-1422

  Osorio, Yaneth ^a,b,c   Bonilla, Diana L ^b   Peniche, Alex G ^b   Melby, Peter C ^a,c   Travi, Bruno L ^a,b,c  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^b CENTRO INTERNACIONAL DE ENTRENAMIENTO E INVESTIGACIONES MÉDICAS CIDEIM   (Colombia)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Estrogen; Hamster; Leishmania

Indexed keywords

ESTRADIOL; ESTROGEN; INDUCIBLE NITRIC OXIDE SYNTHASE; MESSENGER RNA; N6 (1 IMINOETHYL)LYSINE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE INHIBITOR; PREGNANE DERIVATIVE; CYTOKINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; EXPERIMENTAL INFECTION; FEMALE; HAMSTER; INNATE IMMUNITY; LEISHMANIA PANAMENSIS; LYMPH NODE CELL; NEUTROPHIL; NONHUMAN; PERITONEUM MACROPHAGE; PREGNANCY; PRIORITY JOURNAL; SKIN LEISHMANIASIS; ANIMAL; BIOSYNTHESIS; IMMUNOLOGY; MACROPHAGE; PREGNANCY COMPLICATION;

ANIMALIA; CRICETINAE; LEISHMANIA PANAMENSIS;

ANIMALS; CRICETINAE; CYTOKINES; ESTROGENS; FEMALE; IMMUNITY, NATURAL; LEISHMANIASIS, CUTANEOUS; MACROPHAGES; NEUTROPHILS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; PREGNANCY; PREGNANCY COMPLICATIONS, PARASITIC; PREGNANES;

EID: 45949100431     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0207130     Document Type: Article

References (51)

1. Jansson, L., Holmdahl, R. (1998) Estrogen-mediated immunosuppression in autoimmune diseases. Inflamm. Res. 47, 290-301.
2. Jiang, S. P., Vacchio, M. S. (1998) Multiple mechanisms of peripheral T cell tolerance to the fetal "allograft". J. Immunol. 160, 3086-3090.
3. Weinberg, E. D. (1984) Pregnancy-associated depression of cell-mediated immunity. Rev. Infect. Dis. 6, 814-831.
4. Kelemen, K., Paldi, A., Tinneberg, H., Torok, A., Szekeres-Bartho, J. (1998) Early recognition of pregnancy by the maternal immune system. Am. J. Reprod. Immunol. 39, 351-355.
5. Szereday, L., Varga, P., Szekeres-Bartho, J. (1997) Cytokine production by lymphocytes in pregnancy. Am. J. Reprod. Immunol. 38, 418-422.
6. Wegmann, T. G., Lin, H., Guilbert, L., Mosmann, T. R. (1993) Bidirectional cytokine interactions in the maternal-fetal relationship: is successful pregnancy a TH2 phenomenon? Immunol. Today 14, 353-356.
7. Krishnan, L., Guilbert, L. J., Russell, A. S., Wegmann, T. G., Mosmann, T. R., Belosevic, M. (1996) Pregnancy impairs resistance of C57BL/6 mice to Leishmania major infection and causes decreased antigen-specific IFN-γ response and increased production of T helper 2 cytokines. J. Immunol. 156, 644-652.
8. Luft, B. J., Remington, J. S. (1982) Effect of pregnancy on resistance to Listeria monocytogenes and Toxoplasma gondii infections in mice. Infect. Immun. 38, 1164-1171.
9. Matzdorff, A. C., Matthes, K., Kemkes-Matthes, B., Pralle, H. (1997) [Visceral leishmaniasis with an unusually long incubation time]. Dtsch. Med. Wochenschr. 122, 890-894.
10. Meinecke, C. K., Schottelius, J., Oskam, L., Fleischer, B. (1999) Congenital transmission of visceral leishmaniasis (Kala Azar) from an asymptomatic mother to her child. Pediatrics 104, e65.
11. Pagliano, P., Carannante, N., Rossi, M., Gramiccia, M., Gradoni, L., Faella, F. S., Gaeta, G. B. (2005) Visceral leishmaniasis in pregnancy: a case series and a systematic review of the literature. J. Antimicrob. Chemother. 55, 229-233.
12. Sacks, G., Sargent, I., Redman, C. (1999) An innate view of human pregnancy. Immunol. Today 20, 114-118.
13. Koumandakis, E., Koumandaki, I., Kaklamani, E., Sparos, L., Aravantinos, D., Trichopoulos, D. (1986) Enhanced phagocytosis of mononuclear phagocytes in pregnancy. Br. J. Obstet. Gynaecol. 93, 1150-1154.
14. Luppi, P., Haluszczak, C., Betters, D., Richard, C. A., Trucco, M., DeLoia, J. A. (2002) Monocytes are progressively activated in the circulation of pregnant women. J. Leukoc. Biol. 72, 874-884.
15. Sacks, G. P., Redman, C. W., Sargent, I. L. (2003) Monocytes are primed to produce the Th1 type cytokine IL-12 in normal human pregnancy: an intracellular flow cytometric analysis of peripheral blood mononuclear cells. Clin. Exp. Immunol. 131, 490-497.
16. Aga, E., Katschinski, D. M., van Zandbergen, G., Laufs, H., Hansen, B., Muller, K., Solbach, W., Laskay, T. (2002) Inhibition of the spontaneous apoptosis of neutrophil granulocytes by the intracellular parasite Leishmania major. J. Immunol. 169, 898-905.
17. Laskay, T., van Zandbergen, G., Solbach, W. (2003) Neutrophil granulocytes - Trojan horses for Leishmania major and other intracellular microbes? Trends Microbiol. 11, 210-214.
18. Boorman, G. A., Luster, M. I., Dean, J. H., Wilson, R. E. (1980) The effect of adult exposure to diethylstilbestrol in the mouse on macrophage function and numbers. J. Reticuloendothel. Soc. 28, 547-560.
19. Cannon, J. G., St Pierre, B. A. (1997) Gender differences in host defense mechanisms. J. Psychiatr. Res. 31, 99-113.
20. Edwards III, C. K., Schepper, J. M., Yunger, L. M., Kelley, K. W. (1988) Somatotropin and prolactin enhance respiratory burst activity of macrophages. Ann. N. Y. Acad. Sci. 540, 698-699.
21. Stenger, S., Donhauser, N., Thuring, H., Rollinghoff, M., Bogdan, C. (1996) Reactivation of latent leishmaniasis by inhibition of inducible nitric oxide synthase. J. Exp. Med. 183, 1501-1514.
22. Ali, M., Buhimschi, I., Chwalisz, K., Garfield, R. E. (1997) Changes in expression of the nitric oxide synthase isoforms in rat uterus and cervix during pregnancy and parturition. Mol. Hum. Reprod. 3, 995-1003.
23. Conrad, K. P., Joffe, G. M., Kruszyna, H., Kruszyna, R., Rochelle, L. G., Smith, R. P., Chavez, J. E., Mosher, M. D. (1993) Identification of increased nitric oxide biosynthesis during pregnancy in rats. FASEB J. 7, 566-571.
24. Stefano, G. B., Prevot, V., Beauvillain, J. C., Fimiani, C., Welters, I., Cadet, P., Breton, C., Pestel, J., Salzet, M., Bilfinger, T. V. (1999) Estradiol coupling to human monocyte nitric oxide release is dependent on intracellular calcium transients: evidence for an estrogen surface receptor. J. Immunol. 163, 3758-3763.
25. Walsh, L. S., Ollendorff, A., Mershon, J. L. (2003) Estrogen increases inducible nitric oxide synthase gene expression. Am. J. Obstet. Gynecol. 188, 1208-1210.
26. You, H. J., Kim, J. Y., Jeong, H. G. (2003) 17 -Estradiol increases inducible nitric oxide synthase expression in macrophages. Biochem. Biophys. Res. Commun. 303, 1129-1134.
27. Chwalisz, K., Winterhager, E., Thienel, T., Garfield, R. E. (1999) Synergistic role of nitric oxide and progesterone during the establishment of pregnancy in the rat. Hum. Reprod. 14, 542-552.
28. Maul, H., Longo, M., Saade, G. R., Garfield, R. E. (2003) Nitric oxide and its role during pregnancy: from ovulation to delivery. Curr. Pharm. Des. 9, 359-380.
29. Gomez-Ochoa, P., Gascon, F. M., Lucientes, J., Larraga, V., Castillo, J. A. (2003) Lactating females Syrian hamster (Mesocricetus auratus) show protection against experimental Leishmania infantum infection. Vet. Parasitol. 116, 61-64.
30. Satoskar, A., Al-Quassi, H. H., Alexander, J. (1998) Sex-determined resistance against Leishmania mexicana is associated with the preferential induction of a Th1-like response and IFN-γ production by female but not male DBA/2 mice. Immunol. Cell Biol. 76, 159-166.
31. Travi, B. L., Osorio, Y., Melby, P. C., Chandrasekar, B., Arteaga, L., Saravia, N. G. (2002) Gender is a major determinant of the clinical evolution and immune response in hamsters infected with Leishmania spp. Infect. Immun. 70, 2288-2296.
32. Osorio, Y., Melby, P. C., Pirmez, C., Chandrasekar, B., Guarin, N., Travi, B. L. (2003) The site of cutaneous infection influences the immunological response and clinical outcome of hamsters infected with Leishmania panamensis. Parasite Immunol. 25, 139-148.
33. Roy, G., Dumas, C., Sereno, D., Wu, Y., Singh, A. K., Tremblay, M. J., Ouellette, M., Olivier, M., Papadopoulou, B. (2000) Episomal and stable expression of the luciferase reporter gene for quantifying Leishmania spp. infections in macrophages and in animal models. Mol. Biochem. Parasitol. 110, 195-206.
34. Henao, H. H., Osorio, Y., Saravia, N. G., Gomez, A., Travi, B. (2004) [Efficacy and toxicity of pentavalent antimonials (Glucantime and Pentostam) in an American cutaneous leishmaniasis animal model: luminometry application]. Biomedica 24, 393-402.
35. Melby, P. C., Tryon, V. V., Chandrasekar, B., Freeman, G. L. (1998) Cloning of Syrian hamster (Mesocricetus auratus) cytokine cDNAs and analysis of cytokine mRNA expression in experimental visceral leishmaniasis. Infect. Immun. 66, 2135-2142.
36. Perez, L. E., Chandrasekar, B., Saldarriaga, O. A., Zhao, W., Arteaga, L. T., Travi, B. L., Melby, P. C. (2006) Reduced nitric oxide synthase 2 (NOS2) promoter activity in the Syrian hamster renders the animal functionally deficient in NOS2 activity and unable to control an intracellular pathogen. J. Immunol. 176, 5519-5528.
37. Lim, L. C., England, D. M., Glowacki, N. J., DuChateau, B. K., Schell, R. F. (1995) Involvement of CD4+ T lymphocytes in induction of severe destructive Lyme arthritis in inbred LSH hamsters. Infect. Immun. 63, 4818-4825.
38. Liu, H., Steiner, B. M., Alder, J. D., Baertschy, D. K., Schell, R. F. (1990) Immune T cells sorted by flow cytometry confer protection against infection with Treponema pallidum subsp. pertenue in hamsters. Infect. Immun. 58, 1685-1690.
39. Boyum, A. (1974) Separation of blood leucocytes, granulocytes and lymphocytes. Tissue Antigens 4, 269-274.
40. Lo, F., Kaufman, S. (2001) Effect of 5 α-pregnan-3 α-ol-20-one on nitric oxide biosynthesis and plasma volume in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 280, R1902-R1905.
41. Barral, A., Barral-Netto, M., Yong, E. C., Brownell, C. E., Twardzik, D. R., Reed, S. G. (1993) Transforming growth factor β- as a virulence mechanism for Leishmania braziliensis. Proc. Natl. Acad. Sci. USA 90, 3442-3446.
42. Miller, L., Hunt, J. S. (1996) Sex steroid hormones and macrophage function. Life Sci. 59, 1-14.
43. Laufs, H., Muller, K., Fleischer, J., Reiling, N., Jahnke, N., Jensenius, J. C., Solbach, W., Laskay, T. (2002) Intracellular survival of Leishmania major in neutrophil granulocytes after uptake in the absence of heat-labile serum factors. Infect. Immun. 70, 826-835.
44. Ribeiro-Gomes, F. L., Otero, A. C., Gomes, N. A., Moniz-De-Souza, M. C., Cysne-Finkelstein, L., Arnholdt, A. C., Calich, V. L., Coutinho, S. G., Lopes, M. F., DosReis, G. A. (2004) Macrophage interactions with neutrophils regulate Leishmania major infection. J. Immunol. 172, 4454-4462.
45. Van Zandbergen, G., Klinger, M., Mueller, A., Dannenberg, S., Gebert, A., Solbach, W., Laskay, T. (2004) Cutting edge: neutrophil granulocyte serves as a vector for Leishmania entry into macrophages. J. Immunol. 173, 6521-6525.
46. Melby, P. C., Chandrasekar, B., Zhao, W., Coe, J. E. (2001) The hamster as a model of human visceral leishmaniasis: progressive disease and impaired generation of nitric oxide in the face of a prominent Th1-like response. J. Immunol. 166, 1912-1920.
47. Basu, R., Bhaumik, S., Basu, J. M., Naskar, K., De, T., Roy, S. (2005) Kinetoplastid membrane protein-11 DNA vaccination induces complete protection against both pentavalent antimonial-sensitive and -resistant strains of Leishmania donovani that correlates with inducible nitric oxide synthase activity and IL-4 generation: evidence for mixed Th1- and Th2-like responses in visceral leishmaniasis. J. Immunol. 174, 7160-7171.
48. Ramirez-Emiliano, J., Gonzalez-Hernandez, A., Arias-Negrete, S. (2005) Expression of inducible nitric oxide synthase mRNA and nitric oxide production during the development of liver abscess in hamster inoculated with Entamoeba histolytica. Curr. Microbiol. 50, 299-308.
49. MacRitchie, A. N., Jun, S. S., Chen, Z., German, Z., Yuhanna, I. S., Sherman, T. S., Shaul, P. W. (1997) Estrogen upregulates endothelial nitric oxide synthase gene expression in fetal pulmonary artery endothelium. Circ. Res. 81, 355-362.
50. Karpuzoglu, E., Fenaux, J. B., Phillips, R. A., Lengi, A. J., Elvinger, F., Ansar Ahmed, S. (2006) Estrogen up-regulates inducible nitric oxide synthase, nitric oxide, and cyclooxygenase-2 in splenocytes activated with T cell stimulants: role of interferon-γ. Endocrinology 147, 662- 671.
51. Karpuzoglu, E., Phillips, R. A., Gogal Jr., R. M., Ansar Ahmed, S. (2007) IFN-γ-inducing transcription factor, T-bet is upregulated by estrogen in murine splenocytes: role of IL-27 but not IL-12. Mol. Immunol. 44, 1808-1814.