Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-27T19:02:54.641Z Has data issue: false hasContentIssue false
  • English
  • Français

The role of metalloproteases in Leishmania species infection in the New World: a systematic review

Published online by Cambridge University Press:  13 March 2018

Letícia Sayuri Murase ,
João Vítor Perez de Souza ,
Quirino Alves de Lima Neto ,
Tatiane França Perles de Mello ,
Bruna Muller Cardoso ,
Daniele Stéfanie Sara Lopes Lera-Nonose ,
Jorge Juarez Vieira Teixeira ,
Maria Valdrinez Campana Lonardoni  and
Izabel Galhardo Demarchi Open the ORCID record for Izabel Galhardo Demarchi [Opens in a new window]
Letícia Sayuri Murase
Affiliation:
Graduation in Biomedicine, Department of Clinical Analysis and Biomedicine, State University of Maringá, Maringá, PR, Brazil
João Vítor Perez de Souza
Affiliation:
Graduation in Biomedicine, Department of Clinical Analysis and Biomedicine, State University of Maringá, Maringá, PR, Brazil
Quirino Alves de Lima Neto
Affiliation:
Department of Biochemistry, State University of Maringá, PR, Brazil
Tatiane França Perles de Mello
Affiliation:
Biosciences and Physiopathology by the Graduate Program of the State University of Maringá, Maringá, PR, Brazil
Bruna Muller Cardoso
Affiliation:
Biosciences and Physiopathology by the Graduate Program of the State University of Maringá, Maringá, PR, Brazil
Daniele Stéfanie Sara Lopes Lera-Nonose
Affiliation:
Postgraduate in Health Sciences of the State University of Maringá, Maringá, PR, Brazil
Jorge Juarez Vieira Teixeira
Affiliation:
Department of Clinical Analysis and Biomedicine, State University of Maringá, Maringá, PR, Brazil
Maria Valdrinez Campana Lonardoni
Affiliation:
Department of Clinical Analysis and Biomedicine, State University of Maringá, Maringá, PR, Brazil
Izabel Galhardo Demarchi*
Affiliation:
Department of Clinical Analysis and Biomedicine, State University of Maringá, Maringá, PR, Brazil
*
Author for correspondence: Izabel Galhardo Demarchi, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

This is a systematic review on the role of metalloproteases in the pathogenicity of the American tegumentary leishmaniasis (ATL) caused by New World Leishmania species. The review followed the PRISMA method, searching for articles in PubMed, EMBASE, LILACS and ISI Web of Science, by employing the following terms: ‘leishmaniasis’, ‘cutaneous leishmaniasis’, ‘mucocutaneous leishmaniasis’, ‘diffuse cutaneous leishmaniasis’, ‘Leishmania’ and ‘metalloproteases’. GP63 of New World Leishmania species is a parasite metalloproteases involved in the degradation and cleavage of many biological molecules as kappa-B nuclear factor, fibronectin, tyrosine phosphatases. GP63 is capable of inhibiting the activity of the complement system and reduces the host's immune functions, allowing the survival of the parasite and its dissemination. High serological/tissue levels of host matrix metalloproteases (MMP)-9 have been associated with tissue damage during the infection, while high transcriptional levels of MMP-2 related with a satisfactory response to treatment. Host MMPs serological and tissue levels have been investigated using Western Blot, zymography, and Real Time polymerase chain reaction. GP63 detection characterizes species and virulence in promastigotes isolated from lesions samples using techniques mentioned previously. The monitoring of host MMPs levels and GP63 in Leishmania isolated from host samples could be used on the laboratory routine to predict the prognostic and treatment efficacy of ATL.

Keywords

Diagnosisglycoprotein 63immunologyLeishmaniaLeishmaniasismetalloproteaseprognosis
Type
Review Article
Information
Parasitology , Volume 145 , Issue 12 , October 2018 , pp. 1499 - 1509
Check for updates
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Arrais-Silva, WW, Paffaro, VA, Yamada, AT and Giorgio, S (2005) Expression of hypoxia-inducible factor-1-alpha in the cutaneous lesions of BALB/c mice infected with Leishmania amazonensis. Experimental and molecular pathology 78, 49–54.Google Scholar
Beller, EM, Glasziou, PP, Altman, DG, Hopewell, S, Bastian, H, Chalmers, I, Gøtzsche, PC, Lasserson, TTovey, D and Group, for the P. for A. (2013). PRISMA for abstracts: reporting systematic reviews in journal and conference abstracts. PLoS Medicine 10, e1001419.Google Scholar
Bennis, I, Thys, S, Filali, H, De Brouwere, V, Sahibi, H and Boelaert, M (2017) Psychosocial impact of scars due to cutaneous leishmaniasis on high school students in Errachidia province, Morocco. Infectious Diseases of Poverty 6, 46.Google Scholar
Birkedal-Hansen, H, Moore, WG, Bodden, MK, Windsor, LJ, Birkedal-Hansen, B, DeCarlo, A and Engler, JA (1993) Matrix metalloproteinases: a review. Critical Reviews in Oral Biology and Medicine: An Official Publication of the American Association of Oral Biologists 4, 197–250.Google Scholar
Brazil, Ministry of Health (2017) Secretaria de Vigilância em Saúde. Departamento de Vigilância das Doenças Transmissíveis. Manual de vigilância da leishmaniose tegumentar [recurso eletrônico]/Ministério da Saúde, Secretaria de Vigilância em Saúde, Departamento de Vigilância das Doenças Transmissíveis.–Brasília: Ministério da Saúde, p. 189.Google Scholar
Calegari-Silva, TC, Pereira, RMS, Dione, L, De-melo, B, Saraiva, EM, Soares, DC, Bellio, M and Lopes, UG (2009) NF-kB-mediated repression of iNOS expression in Leishmania amazonensis macrophage infection. Immunology Letters 127, 19–26.Google Scholar
Campos, TM, Passos, ST, Novais, FO, Beiting, DP, Costa, RS, Queiroz, A, Mosser, D, Scott, P, Carvalho, EM and Carvalho, LP (2014) Matrix metalloproteinase 9 production by monocytes is enhanced by TNF and participates in the pathology of human cutaneous Leishmaniasis. PLoS Neglected Tropical Diseases 8, e3282.Google Scholar
Carvalhal, DGF, Barbosa, AJ, D'El-Rei Hermida, M, Clarencio, J, Pinheiro, NFJ, Veras, PST and dos-Santos, WLC (2004) The modelling of mononuclear phagocyte-connective tissue adhesion in vitro: application to disclose a specific inhibitory effect of Leishmania infection. Experimental Parasitology 107, 189–199.Google Scholar
Chang, C and Werb, Z (2001) The many faces of metalloproteases: cell growth, invasion, angiogenesis and metastasis. Trends in Cell Biology 11, S37–S43.Google Scholar
Contreras, I, Gómez, MA, Nguyen, O, Shio, MT, McMaster, RW and Olivier, M (2010) Leishmania-induced inactivation of the macrophage transcription factor AP-1 Is mediated by the parasite metalloprotease GP63. Plos Pathogens 6, e1001148.Google Scholar
Cuervo, P, Saboia-Vahia, L, Costa Silva-Filho, F, Fernandes, O, Cupolillo, E and De Jesus, JB (2006) A zymographic study of metalloprotease activities in extracts and extracellular secretions of Leishmania (Viannia) braziliensis strains. Parasitology 132, 177–185.Google Scholar
Cuervo, P, Santos, AL, Alves, CR, Menezes, GC, Silva, BA, Britto, C, Fernandes, O, Cupolillo, E, de Jesus, BJ (2008) Cellular localization and expression of gp63 homologous metalloproteases in Leishmania (Viannia) braziliensis strains. Acta Tropica 106, 143–148.Google Scholar
de Oliveira, FA, Vanessa Oliveira Silva, C, Damascena, NP, Passos, RO, Duthie, MS, Guderian, Ja, Bhatia, A, de Moura, TR, Reed, SG, de Almeida, RP and de Jesus, AR (2013) 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 13, 331.Google Scholar
Espir, TT, Figueira, LDP, Naiff, MDF, Guimarães, A, Ramalho-ortigão, M, Malheiro, A, Maria, A and Franco, R (2014) The role of inflammatory, anti-inflammatory, and regulatory cytokines in patients infected with cutaneous Leishmaniasis in Amazonas State, Brazil. Journal of Immunology Research 2014, 1–10.Google Scholar
Fraga, AC, Oliveira, MV, Alves, LR, Viana, AG, Sousa, AA, Carvalho, SF, De Paula, AM, Botelho, AC and Guimarães, AL (2012) Immunohistochemical profile of HIF-1 α, VEGF-A, VEGFR2 and MMP9 proteins in tegumentary Leishmaniasis. Anais Brasileiros de Demartologia 87, 709–713.Google Scholar
Gadisa, E, Tasew, G, Abera, A, Gelaye, W, Chanyalew, M, Abebe, M, Laskay, T and Aseffa, A (2017) Serological signatures of clinical cure following successful treatment with sodium stibogluconate in Ethiopian visceral leishmaniasis. Cytokine 91, 6–9.Google Scholar
Gomez, MA, Contreras, I, Halle, M, Tremblay, ML, McMaster, RW and Olivier, M (2009a) Leishmania GP63 alters host signaling through cleavage-activated protein tyrosine phosphatases. Science Signaling 2, ra58.Google Scholar
Gomez, MA, Stuible, M, Shimizu, H, Mcmaster, WR, Olivier, M and Tremblay, ML (2009b) The Leishmania surface protease GP63 cleaves multiple intracellular proteins and actively participates in p38 mitogen-activated protein kinase inactivation. 284, 6893–6908.Google Scholar
Gontijo, B, De, M and De Carvalho, LR (2003) Leishmaniose tegumentar Americana. American Cutaneous leishmaniasis. Medicina Tropical 36, 71–80.Google Scholar
Gregory, DJ, Godbout, M, Contreras, I, Forget, G and Olivier, M (2008) A novel form of NF-kB is induced by Leishmania infection: involvement in macrophage gene expression 1. European Journal of Immunology 38, 1071–1081.Google Scholar
Hallé, M, Gomez, MA, Stuible, M, Shimizu, H, McMaster, WR, Olivier, M and Tremblay, ML (2009) The Leishmania surface protease GP63 cleaves multiple intracellular proteins and actively participates in p38 mitogen-activated protein kinase inactivation. The Journal of Biological Chemistry 284, 6893–6908.Google Scholar
Isnard, A, Shio, MT and Olivier, M (2012) Impact of Leishmania metalloprotease GP63 on macrophage signaling. Frontiers in Cellular and Infection Microbiology 2, 72.Google Scholar
Kulkarni, MM, Jones, EA, Mcmaster, WR, Mcgwire, BS, Kulkarni, MM, Jones, EA, Mcmaster, WR and Mcgwire, BS (2008) Fibronectin binding and proteolytic degradation by Leishmania and effects on macrophage activation fibronectin binding and proteolytic degradation by Leishmania and effects on macrophage activation. Infection and Immunity 76, 1738–1747.Google Scholar
Kulkarni, MM, Olson, CL, Engman, DM and Mcgwire, BS (2009) Trypanosoma cruzi GP63 proteins undergo stage-specific differential posttranslational modification and are important for host cell infection. Infection and Immunity 77, 2193–2200.Google Scholar
Liarte, DB, Mendonca, IL, Luz, FC, Abreu, EA, Mello, GW, Farias, TJ, Ferreira, AF, Millington, MA and Costa, CH (2001) QBC for the diagnosis of human and canine American visceral Leishmaniasis: preliminary data. Revista da Sociedade Brasileira de Medicina Tropical 34, 577–581.Google Scholar
Lima, AKC, Elias, CGR, Souza, JEO, Santos, ALS and Dutra, PML (2009) Dissimilar peptidase production by avirulent and virulent promastigotes of Leishmania braziliensis: inference on the parasite proliferation and interaction with macrophages. Parasitology 136, 1179–1191.Google Scholar
Machado, GF, Melo, GD, Moraes, OC, Souza, MS, Marcondes, M, Perri, SHV and Vasconcelos, RO (2010) Differential alterations in the activity of matrix metalloproteinases within the nervous tissue of dogs in distinct manifestations of visceral leishmaniasis. Veterinary Immunology and Immunopathology 136, 340–345.Google Scholar
Maretti-Mira, AC, de Pinho Rodrigues, KM, de Oliveira-Neto, MP, Pirmez, C and Craft, N (2011 a) Acta Tropica MMP-9 activity is induced by Leishmania braziliensis infection and correlates with mucosal Leishmaniasis. Acta Tropica 119, 160–164.Google Scholar
Maretti-Mira, AC, De Oliveira-Neto, MP, Da-Cruz, AM, De Oliveira, MP, Craft, N and Pirmez, C (2011 b) Therapeutic failure in American cutaneous Leishmaniasis is associated with gelatinase activity and cytokine expression. Clinical and Experimental Immunology 163, 207–214.Google Scholar
Marangoni, NR, Melo, GD, Moraes, OC, Souza, MS, Perri, SHV and Machado, GF (2011) Levels of matrix metalloproteinase-2 and metalloproteinase-9 in the cerebrospinal fluid of dogs with visceral leishmaniasis. Parasite Immunology 33, 330–334.Google Scholar
Matheoud, D, Moradin, N, Bellemare-Pelletier, A, Shio, MT, Hong, WJ, Olivier, M, Gagnon, É, Desjardins, M and Descoteaux, A (2013) Leishmania evades host immunity by inhibiting antigen cross-presentation through direct cleavage of the SNARE VAMP8. Cell Host and Microbe 14, 15–25.Google Scholar
Mauricio, IL, Gaunt, MW, Stothard, JR and Miles, MA (2007) Glycoprotein 63 (gp63) genes show gene conversion and reveal the evolution of Old World Leishmania. International Journal for Parasitology 37, 565–576.Google Scholar
Melo, GD, Marangoni, NR, Marcondes, M, Lima, VMF and Machado, GF (2011) High levels of serum matrix metalloproteinases in dogs with natural visceral leishmaniosis: a preliminary report. Veterinary Journal (London, England: 1997) 188, 243–245.Google Scholar
Melo, GD, Marcondes, M and Machado, GF (2012) Canine cerebral leishmaniasis: potential role of matrix metalloproteinase-2 in the development of neurological disease. Veterinary Immunology and Immunopathology 148, 260–266.Google Scholar
Oliveira, WN, Ribeiro, LE, Schrieffer, A, Machado, P, Carvalho, EM and Bacellar, O (2014) The role of inflammatory and anti-inflammatory cytokines in the pathogenesis of human tegumentary Leishmaniasis. Cytokine 66, 127–132.Google Scholar
Petropolis, DB, Rodrigues, JCF, Viana, NB, Pontes, B, Pereira, CFa and Silva-Filho, FC (2014) Leishmania amazonensis promastigotes in 3D Collagen I culture: an in vitro physiological environment for the study of extracellular matrix and host cell interactions. PeerJ 2, e317.Google Scholar
Reichel, CA, Rehberg, M, Bihari, P, Moser, CM, Linder, S, Khandoga, A and Krombach, F (2008) Gelatinases mediate neutrophil recruitment in vivo: evidence for stimulus specificity and a critical role in collagen IV remodeling. Journal of Leukocyte Biology 83, 864–874.Google Scholar
Shio, MT and Olivier, M (2010) Editorial: Leishmania survival mechanisms: the role of host phosphatases. Journal of Leukocyte Biology 88, 1–3.Google Scholar
Shio, MT, Hassani, K, Isnard, A, Ralph, B, Contreras, I, Gomez, MA, Abu-Dayyeh, I and Olivier, M (2012) Host cell signalling and Leishmania mechanisms of evasion. Journal of Tropical Medicine 2012, 819512.Google Scholar
Thiakaki, M, Kolli, B, Chang, K and Soteriadou, K (2006) Down-regulation of gp63 level in Leishmania amazonensis promastigotes reduces their infectivity in BALB / c mice. Microbes and Infection 8, 1455–1463.Google Scholar
Tupperwar, N, Vineeth, V, Rath, S and Vaidya, T (2008) Development of a real-time polymerase chain reaction assay for the quantification of Leishmania species and the monitoring of systemic distribution of the pathogen. Diagnostic Microbiology and Infectious Disease 61, 23–30.Google Scholar
WHO, World Health Organization (2010) Control of the Leishmaniasis: Report of a Meeting of the WHO. Expert Committee on the Control of Leishmaniasis. “WHO technical report series”, WHO: Geneva, Switzerland, no. 949, pp. 201.Google Scholar
Yao, C (2010) Major surface protease of Trypanosomatids: one size fits all. Infection and Immunity 78, 22–31.Google Scholar
Zarember, KA and Malech, HL (2005) HIF-1 α: a master regulator of innate host defenses. The Journal of Clinical Investigation 115, 2003–2005.Google Scholar
Supplementary material: File

Murase et al. supplementary material 1

Supplementary Table

Download Murase et al. supplementary material 1(File)
File 24 KB