Hepatic extracellular matrix alterations in dogs naturally infected with Leishmania (Leishmania) chagasi

International Journal of Experimental Pathology

Volumn 90, Issue 5, 2009, Pages 538-548

  Tafuri, Wagner Luiz ^a   Melo, Ferdinan Almeida ^a   Moura, Eliane Perlatto ^a   Ribeiro, Raul Rio ^a   Alves, Cíntia Fontes ^a   Caliari, Marcelo Vidigal ^a   Tafuri, Washington Luiz ^a   Da Silva Calabrese, Kátia ^b  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b INSTITUTO OSWALDO CRUZ   (Brazil)

Author keywords

Canine visceral leishmaniasis; Extracellular matrix; Pathology

Indexed keywords

COLLAGEN; FIBRONECTIN; HEMATOXYLIN; LAMININ; PARAFFIN;

AMASTIGOTE; ANIMAL TISSUE; ARTICLE; AUTOPSY; CONTROLLED STUDY; DOG; EXTRACELLULAR MATRIX; FIBROGENESIS; IMMUNOFLUORESCENCE; LEISHMANIA CHAGASI; LIVER; NONHUMAN; PRIORITY JOURNAL; SILVER STAINING; VISCERAL LEISHMANIASIS;

ANIMALS; COLLAGEN; DOG DISEASES; DOGS; EXTRACELLULAR MATRIX; FIBRONECTINS; LAMININ; LEISHMANIA INFANTUM; LEISHMANIASIS, VISCERAL; LIVER; LIVER CIRRHOSIS;

EID: 70349313291     PISSN: 09599673     EISSN: 13652613     Source Type: Journal    
DOI: 10.1111/j.1365-2613.2009.00681.x     Document Type: Article

References (68)

1. Abath F.G., Morais C.N., Montenegro C.E., Wynn T.A., Montenegro S.M. (2006) Immunopathogenic mechanisms in schistosomiasis: what can be learnt from human studies? Trends Parasitol. 22, 85 91.
2. Anderson D.C., Buckner R.G., Glenn B.L., MacVean D.W. (1980) Endemic canine leishmaniasis. Vet. Pathol. 17, 94 96.
3. Andrade Z.A. (1991) Contribution to the study of septal fibrosis of the liver. Int. J. Exp. Pathol. 72, 553 562.
4. Andrade Z.A. Andrade S.G. (1966) Some new aspects of the kala-azar pathology. (Morphologic study of 13 autopsy cases). Rev. Inst. Med. Trop. Sao Paulo 8, 259 266.
5. Anosa V.O. Idowu A.L. (1983) The clinico-haematological features and pathology of leishmaniasis in a dog in Nigeria. Zentralbl Veterinarmed B 30, 600 608.
6. Ashford R.W. (2000) The leishmaniases as emerging and reemerging zoonoses. Int. J. Parasitol. 30, 1269 1281.
7. Bandyopadhyay K., Karmakar S., Ghosh A., Das P.K. (2001) Role of 67 kDa cell surface laminin binding protein of Leishmania donovani in pathogenesis. J. Biochem. 130, 141 148.
8. Bandyopadhyay K., Karmakar S., Biswas A., Das P.K. (2003) Membrane orientation of laminin binding protein. Eur. J. Biochem. 270, 3806 3813.
9. Baneth G., Koutinas A.F., Solano-Gallego L., Bourdeau P., Ferrer L. (2008) Canine leishmaniosis - new concepts and insights on an expanding zoonosis: part one. Trends Parasitol. 24, 324 330.
10. Beck K., Hunter I., Engel J. (1990) Structure and function of laminin: anatomy of a multidomain glycoprotein. FASEB J. 4, 148 160.
11. Bogliolo L. (1956) Nova contribuição ao conhecimento da anatomia patológica da leishmaniose visceral. A propósito de um caso brasileiro e com especial referência à fibrose hepática leishmaniótica. O Hospital 3, 101 164.
12. Burns J.M. Jr., Shreffler W.G., Benson D.R., Ghalib H.W., Badaro R., Reed S.G. (1993) Molecular characterization of a kinesin-related antigen of Leishmania chagasi that detects specific antibody in African and American visceral leishmaniasis. Proc. Natl. Acad. Sci. USA 90, 775 779.
13. Caliari M. (1997) Principios de Morfometria Digital. Belo Hrozionte : UFMG.
14. Chang K.P., Nacy C.A., Pearson R.D. (1986) Intracellular parasitism of macrophages in leishmaniasis: in vitro systems and their applications. Methods Enzymol. 132, 603 626.
15. Ciaramella P., Oliva G., Luna R.D., Gradoni L., Ambrosio R., Cortese L., Scalone A., Persechino A. (1997) A retrospective clinical study of canine leishmaniasis in 150 dogs naturally infected by Leishmania infantum. Vet Rec 141, 539 543.
16. Corbett C.E., Duarte M.I., Bustamante S.E. (1993) Regression of diffuse intralobular liver fibrosis associated with visceral leishmaniasis. Am. J. Trop. Med. Hyg. 49, 616 624.
17. Costa M.M., Lima W.G., Figueiredo M.M., Michalick M.S., Tafuri W.L. (2008) Cervical, mandibular, and parotid lymph nodes of dogs naturally infected with Leishmania infantum: a histopathologic and immunohistochemistry study and its correlation with facial skin lesions. Vet. Pathol. 45, 613 616.
18. da Costa-Val A.P., Cavalcanti R.R., de Figueiredo Gontijo N. et al. (2007) Canine visceral leishmaniasis: relationships between clinical status, humoral immune response, haematology and Lutzomyia (Lutzomyia) longipalpis infectivity. Vet. J. 174, 636 643.
19. Duarte M.I. Corbett C.E. (1987) Histopathological patterns of the liver involvement in visceral leishmaniasis. Rev. Inst. Med. Trop. Sao Paulo 29, 131 136.
20. Eng F.J. Friedman S.L. (2000) Fibrogenesis I. New insights into hepatic stellate cell activation: the simple becomes complex. Am. J. Physiol. Gastrointest. Liver Physiol. 279, G7 G11.
21. Ferrer L., Rabanal R.M., Domingo M., Ramos J.A., Fondevila D. (1988) Identification of Leishmania donovani amastigotes in canine tissues by immunoperoxidase staining. Res. Vet. Sci. 44, 194 196.
22. Friedman S.L. (2000) Molecular regulation of hepatic fibrosis, an integrated cellular response to tissue injury. J. Biol. Chem. 275, 2247 2250.
23. Ghosh A., Kole L., Bandyopadhyay K., Sarkar K., Das P.K. (1996) Evidence of a laminin binding protein on the surface of Leishmania donovani. Biochem. Biophys. Res. Commun. 226, 101 106.
24. Giunchetti R.C., Mayrink W., Genaro O. et al. (2006) Relationship between canine visceral leishmaniosis and the Leishmania (Leishmania) chagasi burden in dermal inflammatory foci. J. Comp. Pathol. 135, 100 107.
25. Gonzalez J.L., Rollan E., Novoa C., Castano M. (1988) Structural and ultrastructural hepatic changes in experimental canine leishmaniasis. Histol. Histopathol. 3, 323 329.
26. Grimaldi G. Jr., Tesh R.B., McMahon-Pratt D. (1989) A review of the geographic distribution and epidemiology of leishmaniasis in the New World. Am. J. Trop. Med. Hyg. 41, 687 725.
27. Guyot C., Lepreux S., Combe C. et al. (2006) Hepatic fibrosis and cirrhosis: the (myo)fibroblastic cell subpopulations involved. Int. J. Biochem. Cell Biol. 38, 135 151.
28. Houghton R.L., Petrescu M., Benson D.R. et al. (1998) A cloned antigen (recombinant K39) of Leishmania chagasi diagnostic for visceral leishmaniasis in human immunodeficiency virus type 1 patients and a prognostic indicator for monitoring patients undergoing drug therapy. J. Infect. Dis. 177, 1339 1344.
29. Hynes R.O. (1992) Integrins: versatility, modulation, and signaling in cell adhesion. Cell 69, 11 25.
30. Keenan C.M., Hendricks L.D., Lightner L., Webster H.K., Johnson A.J. (1984) Visceral leishmaniasis in the German shepherd dog. I. Infection, clinical disease, and clinical pathology. Vet. Pathol. 21, 74 79.
31. Korom S., Hancock W.W., Coito A.J., Kupiec-Weglinski J.W. (1998) Blockade of very late antigen-4 integrin binding to fibronectin in allograft recipients. II. Treatment with connecting segment-1 peptides prevents chronic rejection by attenuating arteriosclerotic development and suppressing intragraft T cell and macrophage activation. Transplantation 65, 854 859. (Pubitemid 28160679)
32. Kulkarni M.M., Jones E.A., McMaster W.R., McGwire B.S. (2008) Fibronectin binding and proteolytic degradation by Leishmania and effects on macrophage activation. Infect. Immun. 76, 1738 1747.
33. Lage R.S., Oliveira G.C., Busek S.U. et al. (2007) Analysis of the cytokine profile in spleen cells from dogs naturally infected by Leishmania chagasi. Vet. Immunol. Immunopathol. 115, 135 145.
34. Li D. Friedman S.L. (1999) Liver fibrogenesis and the role of hepatic stellate cells: new insights and prospects for therapy. J. Gastroenterol. Hepatol. 14, 618 633.
35. Lima W.G., Michalick M.S., de Melo M.N., Luiz Tafuri W. (2004) Canine visceral leishmaniasis: a histopathological study of lymph nodes. Acta Trop. 92, 43 53.
36. Lima WG, Oliveira PS, Caliari MV, Gonçalves R, Michalick MS, Melo MN, Tafuri WL, Tafuri WL. (2007) Histopathological and immunohistochemical study of type 3 complement receptors (CD11b/CD18) in livers and spleens of asymptomatic and symptomatic dogs naturally infected with Leishmania (Leishmania) chagasi. Vet Immunol Immunopathol 117, 129 136.
37. Maher J.J. Bissell D.M. (1993) Cell-matrix interactions in liver. Semin. Cell Biol. 4, 189 201.
38. Margonari C., Freitas C.R., Ribeiro R.C. et al. (2006) Epidemiology of visceral leishmaniasis through spatial analysis, in Belo Horizonte municipality, state of Minas Gerais, Brazil. Mem. Inst. Oswaldo Cruz 101, 31 38.
39. Martinez-Hernandez A. Amenta P.S. (1995) The extracellular matrix in hepatic regeneration. FASEB J. 9, 1401 1410.
40. Martinez-Moreno A., Martinez-Cruz M.S., Blanco A., Hernandez-Rodriguez S. (1993) Immunological and histological study of T- and B-lymphocyte activity in canine visceral leishmaniosis. Vet. Parasitol. 51, 49 59.
41. McGwire B.S., Chang K.P., Engman D.M. (2003) Migration through the extracellular matrix by the parasitic protozoan Leishmania is enhanced by surface metalloprotease gp63. Infect. Immun. 71, 1008 1010.
42. Melo F., Amaral M., Oliveira P. et al. (2008) Diffuse intralobular liver fibrosis in dogs naturally infected with Leishmania (Leishmania) chagasi. Am. J. Trop. Med. Hyg. 79, 198 204.
43. Montes G.S. (1996) Structural biology of the fibres of the collagenous and elastic systems. Cell Biol. Int. 20, 15 27.
44. Murray H.W. (2001) Tissue granuloma structure-function in experimental visceral leishmaniasis. Int. J. Exp. Pathol. 82, 249 267.
45. Nattan-Larrier L. (1918) Les cirrhoses hepatiques due au Kalazar. Bull. Acad. Med. 89, 402 408.
46. Oliveira G.G., Santoro F., Sadigursky M. (1993) The subclinical form of experimental visceral leishmaniasis in dogs. Mem. Inst. Oswaldo Cruz 88, 243 248.
47. Papadogiannakis E.I., Koutinas A.F., Saridomichelakis M.N. et al. (2005) Cellular immunophenotyping of exfoliative dermatitis in canine leishmaniosis (Leishmania infantum). Vet. Immunol. Immunopathol. 104, 227 237.
48. Proctor R.A. (1987) Fibronectin: an enhancer of phagocyte function. Rev. Infect. Dis. 9 (Suppl. 4 S412 S419.
49. Quinnell R.J., Courtenay O., Shaw M.A. et al. (2001) Tissue cytokine responses in canine visceral leishmaniasis. J. Infect. Dis. 183, 1421 1424.
50. Rallis T., Day M.J., Saridomichelakis M.N. et al. (2005) Chronic hepatitis associated with canine leishmaniosis (Leishmania infantum): a clinicopathological study of 26 cases. J. Comp. Pathol. 132, 145 152.
51. Reis A.B., Teixeira-Carvalho A., Giunchetti R.C. et al. (2006) Phenotypic features of circulating leucocytes as immunological markers for clinical status and bone marrow parasite density in dogs naturally infected by Leishmania chagasi. Clin. Exp. Immunol. 146, 303 311.
52. Rodgers R.J. Irving Rodgers H.F. (2002) Extracellular matrix of the bovine ovarian membrana granulosa. Mol. Cell. Endocrinol. 191, 57 64.
53. Rogers L. (1908) A peculiar intralobular cirrhosis of the liver produced by the protozoal parasite of Kala-azar. Ann. Trop. Med. a. Parasitol. 2, 147 152.
54. Ruoslahti E. (1988) Fibronectin and its receptors. Annu. Rev. Biochem. 57, 375 413.
55. Sanchez M.A., Diaz N.L., Zerpa O., Negron E., Convit J., Tapia F.J. (2004) Organ-specific immunity in canine visceral leishmaniasis: analysis of symptomatic and asymptomatic dogs naturally infected with Leishmania chagasi. Am. J. Trop. Med. Hyg. 70, 618 624.
56. Schuppan D. (1990) Structure of the extracellular matrix in normal and fibrotic liver: collagens and glycoproteins. Semin. Liver Dis. 10, 1 10. (Pubitemid 20163701)
57. Solano-Gallego L., Fernandez-Bellon H., Morell P. et al. (2004) Histological and immunohistochemical study of clinically normal skin of Leishmania infantum-infected dogs. J. Comp. Pathol. 130, 7 12.
58. Strauss-Ayali D., Baneth G., Jaffe C.L. (2007) Splenic immune responses during canine visceral leishmaniasis. Vet. Res. 38, 547 564.
59. Sundar S., Pai K., Sahu M., Kumar V., Murray H.W. (2002) Immunochromatographic strip-test detection of anti-K39 antibody in Indian visceral leishmaniasis. Ann. Trop. Med. Parasitol. 96, 19 23.
60. Tafuri W.L., Barbosa A.J., Michalick M.S. et al. (1996) Histopathology and immunocytochemical study of type 3 and type 4 complement receptors in the liver and spleen of dogs naturally and experimentally infected with Leishmania (Leishmania) chagasi. Rev. Inst. Med. Trop. Sao Paulo 38, 81 89.
61. Tafuri W.L., de Oliveira M.R., Melo M.N. (2001) Canine visceral leishmaniosis: a remarkable histopathological picture of one case reported from Brazil. Vet. Parasitol. 96, 203 212.
62. Tafuri W.L., Santos R.L., Arantes R.M., Goncalves R., de Melo M.N., Michalick M.S. (2004) An alternative immunohistochemical method for detecting Leishmania amastigotes in paraffin-embedded canine tissues. J. Immunol. Methods 292, 17 23.
63. Tesh R.B. (1995) Control of zoonotic visceral leishmaniasis: is it time to change strategies? Am. J. Trop. Med. Hyg. 52, 287 292.
64. Tryphonas L., Zawidzka Z., Bernard M.A., Janzen E.A. (1977) Visceral leishmaniasis in a dog: clinical, hematological and pathological observations. Can. J. Comp. Med. 41, 1 12.
65. Vannier-Santos M.A., Saraiva E.M., Martiny A., Neves A., de Souza W. (1992) Fibronectin shedding by Leishmania may influence the parasite-macrophage interaction. Eur. J. Cell Biol. 59, 389 397.
66. Wyler D.J. (1987) Fibronectin in parasitic diseases. Rev. Infect. Dis. 9 (Suppl. 4 S391 S399.
67. Wyler D.J., Sypek J.P., McDonald J.A. (1985) In vitro parasite-monocyte interactions in human leishmaniasis: possible role of fibronectin in parasite attachment. Infect. Immun. 49, 305 311.
68. Xavier S.C., de Andrade H.M., Monte S.J. et al. (2006) Comparison of paraffin-embedded skin biopsies from different anatomical regions as sampling methods for detection of Leishmania infection in dogs using histological, immunohistochemical and PCR methods. BMC Vet. Res. 2, 17.