High levels of soluble CD40 ligand and matrix metalloproteinase-9 in serum are associated with favorable clinical evolution in human visceral leishmaniasis

BMC Infectious Diseases

Volumn 13, Issue 1, 2013, Pages

  de Oliveira, Fabrícia Alvisi ^a   Vanessa Oliveira Silva, Carla ^a   Damascena, Nayra Prata ^a   Passos, Rodrigo Oliveira ^a   Duthie, Malcolm S ^b   Guderian, Jeffrey A ^b   Bhatia, Ajay ^b   de Moura, Tatiana Rodrigues ^a   Reed, Steven G ^b   de Almeida, Roque Pacheco ^a,c   de Jesus, Amélia Ribeiro ^a,c  

^a FEDERAL UNIVERSITY OF SERGIPE   (Brazil)

^b INFECTIOUS DISEASE RESEARCH INSTITUTE   (United States)

^c CNPq   (Brazil)

Author keywords

Biomarkers; Clinical outcome; Matrix metalloproteinase 9; Soluble CD40 ligand; Visceral leishmaniasis

Indexed keywords

ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; BIOLOGICAL MARKER; CD40 LIGAND; GELATINASE B;

ADOLESCENT; ADULT; ALANINE AMINOTRANSFERASE BLOOD LEVEL; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; CLINICAL ARTICLE; CONTROLLED STUDY; CORRELATION COEFFICIENT; DISEASE ASSOCIATION; DISEASE CLASSIFICATION; DISEASE SEVERITY; ENDEMIC DISEASE; ENZYME ASSAY; ENZYME KINETICS; FEMALE; FOLLOW UP; HIGH RISK POPULATION; HUMAN; INTERMETHOD COMPARISON; LIVER SIZE; LOW RISK POPULATION; MALE; PARASITE LOAD; PROBABILITY; PROSPECTIVE STUDY; PROTEIN BLOOD LEVEL; SPLEEN SIZE; STUDENT T TEST; VISCERAL LEISHMANIASIS; WILCOXON SIGNED RANKS TEST;

ADOLESCENT; ADULT; ANTIGENS, CD40; BIOLOGICAL MARKERS; CHILD; FEMALE; HUMANS; LEISHMANIASIS, VISCERAL; MALE; MATRIX METALLOPROTEINASE 9; PARASITE LOAD; PROGNOSIS;

EID: 84880334844     PISSN: None     EISSN: 14712334     Source Type: Journal    
DOI: 10.1186/1471-2334-13-331     Document Type: Article

References (49)

1. Carvalho EM, Badaro R, Reed SG, Jones TC, Johnson WD. Absence of gamma interferon and interleukin 2 production during active visceral leishmaniasis. J Clin Invest 1985, 76:2066-2069. 10.1172/JCI112209, 424308, 3935667.
2. Rai AK, Thakur CP, Singh A, Seth T, Srivastava SK, Singh P, Mitra DK. Regulatory T cells suppress T cell activation at the pathologic site of human visceral leishmaniasis. PLoS One 2012, 7:e31551. 10.1371/journal.pone.0031551, 3275558, 22347492.
3. Goto H, Prianti M. Immunoactivation and immunopathogeny during active visceral leishmaniasis. Rev Inst Med Trop Sao Paulo 2009, 51:241-246. 10.1590/S0036-46652009000500002, 19893975.
4. Barral-Netto M, Diez R, Badaro R, Sampaio D, Barral A, Carvalho EM, Falcoff E. Serum interferon activity of patients with leishmaniasis. Braz J Med Biol Res 1989, 22:1485-1487.
5. Carvalho EM, Barral A, Pedral-Sampaio D, Barral-Netto M, Badaro R, Rocha H, Johnson WD. Immunologic markers of clinical evolution in children recently infected with Leishmania donovani chagasi. J Infect Dis 1992, 165:535-540. 10.1093/infdis/165.3.535, 1347057.
6. Carvalho EM, Bacellar OA, Reed S, Barral A, Rocha H. Visceral leishmaniasis: a disease associated with inability of lymphocytes to activate macrophages to kill leishmania. Braz J Med Biol Res 1988, 21:85-92.
7. Bacellar O, D'Oliveira A, Jeronimo S, Carvalho EM. IL-10 and IL-12 are the main regulatory cytokines in visceral leishmaniasis. Cytokine 2000, 12:1228-1231. 10.1006/cyto.2000.0694, 10930301.
8. Holaday BJ, Pompeu MM, Jeronimo S, Texeira MJ, Sousa A, Vasconcelos AW, Pearson RD, Abrams JS, Locksley RM. Potential role for interleukin-10 in the immunosuppression associated with kala azar. J Clin Invest 1993, 92:2626-2632. 10.1172/JCI116878, 288459, 8254019.
9. Murray HW, Moreira AL, Lu CM, DeVecchio JL, Matsuhashi M, Ma X, Heinzel FP. Determinants of response to interleukin-10 receptor blockade immunotherapy in experimental visceral leishmaniasis. J Infect Dis 2003, 188:458-464. 10.1086/376510, 12870129.
10. Verma S, Kumar R, Katara GK, Singh LC, Negi NS, Ramesh V, Salotra P. Quantification of parasite load in clinical samples of leishmaniasis patients: IL-10 level correlates with parasite load in visceral leishmaniasis. PLoS One 2010, 5:e10107. 10.1371/journal.pone.0010107, 2852412, 20404924.
11. McDyer JF, Goletz TJ, Thomas E, June CH, Seder RA. CD40 ligand/CD40 stimulation regulates the production of IFN-gamma from human peripheral blood mononuclear cells in an IL-12- and/or CD28-dependent manner. J Immunol 1998, 160:1701-1707.
12. van Kooten C, Banchereau J. CD40-CD40 ligand. J Leukoc Biol 2000, 67:2-17.
13. Subauste CS. CD40 and the immune response to parasitic infections. Semin Immunol 2009, 21:273-282. 10.1016/j.smim.2009.06.003, 2758065, 19616968.
14. Mathur RK, Awasthi A, Saha B. The conundrum of CD40 function: host protection or disease promotion?. Trends Parasitol 2006, 22:117-122. 10.1016/j.pt.2006.01.003, 16446115.
15. Mathur RK, Awasthi A, Wadhone P, Ramanamurthy B, Saha B. Reciprocal CD40 signals through p38MAPK and ERK-1/2 induce counteracting immune responses. Nat Med 2004, 10:540-544. 10.1038/nm1045, 15107845.
16. Subauste CS, Wessendarp M, Sorensen RU, Leiva LE. CD40-CD40 ligand interaction is central to cell-mediated immunity against Toxoplasma gondii: patients with hyper IgM syndrome have a defective type 1 immune response that can be restored by soluble CD40 ligand trimer. J Immunol 1999, 162:6690-6700.
17. Campbell KA, Ovendale PJ, Kennedy MK, Fanslow WC, Reed SG, Maliszewski CR. CD40 ligand is required for protective cell-mediated immunity to Leishmania major. Immun 1996, 3:283-289.
18. Habib M, Noval Rivas M, Chamekh M, Wieckowski S, Sun X, Bianco A, Trouche N, Chaloin O, Dumortier H, Goldman M, Guichard G, Fournel S, Vray B. Cutting edge: small molecule CD40 ligand mimetics promote control of parasitemia and enhance T cells producing IFN-gamma during experimental Trypanosoma cruzi infection. J Immunol 2007, 178:6700-6704.
19. Schonbeck U, Libby P. The CD40/CD154 receptor/ligand dyad. Cell Mol Life Sci 2001, 58:4-43. 10.1007/PL00000776, 11229815.
20. Malik N, Greenfield BW, Wahl AF, Kiener PA. Activation of human monocytes through CD40 induces matrix metalloproteinases. J Immunol 1996, 156:3952-3960.
21. Hsu YM, Lucci J, Su L, Ehrenfels B, Garber E, Thomas D. Heteromultimeric complexes of CD40 ligand are present on the cell surface of human T lymphocytes. J Biol Chem 1997, 272:911-915. 10.1074/jbc.272.2.911, 8995381.
22. Graf D, Muller S, Korthauer U, van Kooten C, Weise C, Kroczek RA. A soluble form of TRAP (CD40 ligand) is rapidly released after T cell activation. Eur J Immunol 1995, 25:1749-1754. 10.1002/eji.1830250639, 7615003.
23. Haanen JB, Schumacher TN. Vaccine leads to memory loss. Nat Med 2007, 13:248-250. 10.1038/nm0307-248, 17342116.
24. Nagase H, Woessner JF. Matrix metalloproteinases. J Biol Chem 1999, 274:21491-21494. 10.1074/jbc.274.31.21491, 10419448.
25. Taylor JL, Hattle JM, Dreitz SA, Troudt JM, Izzo LS, Basaraba RJ, Orme IM, Matrisian LM, Izzo AA. Role for matrix metalloproteinase 9 in granuloma formation during pulmonary Mycobacterium tuberculosis infection. Infect Immun 2006, 74:6135-6144. 10.1128/IAI.02048-05, 1695484, 16982845.
26. Gutierrez FR, Lalu AA, Mariano FS, Milanezi CM, Cena J, Gerlach RF, Santos JE, Torres-Duenas D, Cunha FQ, Schulz R, Silva JS. Increased activities of cardiac matrix metalloproteinases matrix metalloproteinase (MMP)-2 and MMP-9 are associated with mortality during the acute phase of experimental Trypanosoma cruzi infection. J Infect Dis 2008, 197:1468-1476. 10.1086/587487, 18444803.
27. Heeschen C, Dimmeler S, Hamm CW, van den Brand MJ, Boersma E, Zeiher AM, Simoons ML. Soluble CD40 ligand in acute coronary syndromes. N Engl J Med 2003, 348:1104-1111. 10.1056/NEJMoa022600, 12646667.
28. Tousoulis D, Androulakis E, Papageorgiou N, Briasoulis A, Siasos G, Antoniades C, Stefanadis C. From atherosclerosis to acute coronary syndromes: the role of soluble CD40 ligand. Trends Cardiovasc Med 2010, 20:153-164. 10.1016/j.tcm.2010.12.004, 21742271.
29. Lorente L, Martin MM, Varo N, Borreguero-Leon JM, Sole-Violan J, Blanquer J, Labarta L, Diaz C, Jimenez A, Pastor E, Belmonte F, Orbe J, Rodriguez JA, Gomez-Melini E, Ferrer-Aguero JM, Ferreres J, Lliminana MC, Paramo JA. Association between serum soluble CD40 ligand levels and mortality in patients with severe sepsis. Crit Care 2011, 15:R97. 10.1186/cc10104, 3219362, 21406105.
30. Sipsas NV, Sfikakis PP, Kontos A, Kordossis T. Levels of soluble CD40 ligand (CD154) in serum are increased in human immunodeficiency virus type 1-infected patients and correlate with CD4(+) T-cell counts. Clin Diagn Lab Immunol 2002, 9:558-561. 120000, 11986259.
31. Costa JD, de Melo AC N, Vermelho AB, Meirelles N, Porrozzi R. In vitro evidence for metallopeptidase participation in hepatocyte damage induced by Leishmania chagasi-infected macrophages. Acta Trop 2008, 106:175-183. 10.1016/j.actatropica.2008.03.006, 18433728.
32. Melo GD, Marangoni NR, Marcondes M, Lima VM, Machado GF. High levels of serum matrix metalloproteinases in dogs with natural visceral leishmaniosis: a preliminary report. Vet J 2011, 188:243-245. 10.1016/j.tvjl.2010.03.017, 20418130.
33. Schulz A, Mellenthin K, Schonian G, Fleischer B, Drosten C. Detection, differentiation, and quantitation of pathogenic leishmania organisms by a fluorescence resonance energy transfer-based real-time PCR assay. J Clin Microbiol 2003, 41:1529-1535. 10.1128/JCM.41.4.1529-1535.2003, 153923, 12682141.
34. Heymans S, Luttun A, Nuyens D, Theilmeier G, Creemers E, Moons L, Dyspersin GD, Cleutjens JP, Shipley M, Angellilo A, Levi M, Nube O, Baker A, Keshet E, Lupu F, Herbert JM, Smits JF, Shapiro SD, Baes M, Borgers M, Collen D, Daemen MJ, Carmeliet P. Inhibition of plasminogen activators or matrix metalloproteinases prevents cardiac rupture but impairs therapeutic angiogenesis and causes cardiac failure. Nat Med 1999, 5:1135-1142. 10.1038/13459, 10502816.
35. Palombo D, Maione M, Cifiello BI, Udini M, Maggio D, Lupo M. Matrix metalloproteinases. Their role in degenerative chronic diseases of abdominal aorta. J Cardiovasc Surg (Torino) 1999, 40:257-260.
36. Lima ID, Queiroz JW, Lacerda HG, Queiroz PV, Pontes NN, Barbosa JD, Martins DR, Weirather JL, Pearson RD, Wilson ME, Jeronimo SM. Leishmania infantum chagasi in northeastern Brazil: asymptomatic infection at the urban perimeter. AmJTrop Med Hyg 2012, 86:99-107.
37. Caldas AJ, Costa JM, Silva AA, Vinhas V, Barral A. Risk factors associated with asymptomatic infection by Leishmania chagasi in north-east Brazil. Trans R Soc Trop Med Hyg 2002, 96:21-28. 10.1016/S0035-9203(02)90227-0, 11925984.
38. Murray HW, Lu CM, Brooks EB, Fichtl RE, DeVecchio JL, Heinzel FP. Modulation of T-cell costimulation as immunotherapy or immunochemotherapy in experimental visceral leishmaniasis. Infect Immun 2003, 71:6453-6462. 10.1128/IAI.71.11.6453-6462.2003, 219611, 14573667.
39. Murray HW, Montelibano C, Peterson R, Sypek JP. Interleukin-12 regulates the response to chemotherapy in experimental visceral Leishmaniasis. J Infect Dis 2000, 182:1497-1502. 10.1086/315890, 11023473.
40. Portillo JAC, Feliciano LM, Okenka G, Heizel F, Subauste MC, Subauste C. CD40 and tumour necrosis factor-a co-operate to up-regulate inducuble nitric oxide synthase expression in macrophages. Immunobiol 2007, 135:135-150.
41. Sui Z, Sniderhan LF, Schifitto G, Phipps RP, Gelbard HA, Dewhurst S, Maggirwar SB. Functional synergy between CD40 ligand and HIV-1 Tat contributes to inflammation: implications in HIV type 1 dementia. J Immunol 2007, 178:3226-3326.
42. Opdenakker G, Van den Steen PE, Dubois B, Nelissen I, Van Coillie E, Masure S, Proost P, Van Damme J. Gelatinase B functions as regulator and effector in leukocyte biology. J Leukoc Biol 2001, 69:851-859.
43. Donhauser N, Pritschet K, Helm M, Harrer T, Schuster P, Ries M, Bischof G, Vollmer J, Smola S, Schmidt B. Chronic immune activation in HIV-1 infection contributes to reduced interferon alpha production via enhanced CD40:CD40 ligand interaction. PLoS One 2012, 7:e33925. 10.1371/journal.pone.0033925, 3309969, 22470494.
44. Olmo M, Saumoy M, Alonso-Villaverde C, Penaranda M, Gutierrez F, Romeu J, Larrousse M, Curto J, Domingo P, Oteo J, Vila A, Podzamczer D. Impact of antiretroviral therapy interruption on plasma biomarkers of cardiovascular risk and lipids: 144-week final data from the STOPAR study. HIV Med 2012, 13:488-498.
45. Teixeira MM, Gazzinelli RT, Silva JS. Chemokines, inflammation and Trypanosoma cruzi infection. Trends Parasitol 2002, 18:262-265. 10.1016/S1471-4922(02)02283-3, 12036740.
46. Gong Y, Hart E, Shchurin A, Hoover-Plow J. Inflammatory macrophage migration requires MMP-9 activation by plasminogen in mice. J Clin Invest 2008, 118:3012-3024. 10.1172/JCI32750, 2491456, 18677407.
47. Reichel CA, Rehberg M, Bihari P, Moser CM, Linder S, Khandoga A, Krombach F. Gelatinases mediate neutrophil recruitment in vivo: evidence for stimulus specificity and a critical role in collagen IV remodeling. J Leukoc Biol 2008, 83:864-874. 10.1189/jlb.1007666, 18174361.
48. Elmetwali T, Searle PF, McNeish I, Young LS, Palmer DH. CD40 ligand induced cytotoxicity in carcinoma cells is enhanced by inhibition of metalloproteinase cleavage and delivery via a conditionally-replicating adenovirus. Mol Cancer 2010, 9:52. 10.1186/1476-4598-9-52, 2847953, 20211016.
49. Geurts N, Opdenakker G, Van den Steen PE. Matrix metalloproteinases as therapeutic targets in protozoan parasitic infections. Pharmacol Ther 2012, 133:257-279. 10.1016/j.pharmthera.2011.11.008, 22138604.