Natural haemozoin modulates matrix metalloproteinases and induces morphological changes in human microvascular endothelium

Cellular Microbiology

Volumn 13, Issue 8, 2011, Pages 1275-1285

  Prato, Mauro ^a   D'Alessandro, Sarah ^a,b   Van den Steen, Philippe E ^c   Opdenakker, Ghislain ^c   Arese, Paolo ^a   Taramelli, Donatella ^a,b   Basilico, Nicoletta ^a,b  

^a UNIVERSITY OF TURIN   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

GELATINASE A; GELATINASE B; HEMOZOIN; MATRIX METALLOPROTEINASE; STROMELYSIN; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TISSUE INHIBITOR OF METALLOPROTEINASE 2;

ARTICLE; BASEMENT MEMBRANE; BLOOD BRAIN BARRIER; BRAIN MALARIA; CELL ACTIVATION; CELL STRUCTURE; CONTROLLED STUDY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; INFLAMMATION; MICROTUBULE; MICROVASCULAR ENDOTHELIAL CELL; MICROVASCULARIZATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; REGULATORY MECHANISM; WESTERN BLOTTING;

CELL SHAPE; ENDOTHELIAL CELLS; ENZYME ACTIVATORS; HEMEPROTEINS; HOST-PATHOGEN INTERACTIONS; HUMANS; MATRIX METALLOPROTEINASE 1; MATRIX METALLOPROTEINASE 3; MATRIX METALLOPROTEINASE 9; PLASMODIUM FALCIPARUM; UP-REGULATION;

EID: 79960389341     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2011.01620.x     Document Type: Article

References (80)

1. Ades, E.W., Candal, F.J., Swerlick, R.A., George, V.G., Summers, S., Bosse, D.C., and Lawley, T.J. (1992) HMEC-1: establishment of an immortalized human microvascular endothelial cell line. J Invest Dermatol 99: 683-690.
2. Agrawal, S., Anderson, P., Durbeej, M., van Rooijen, N., Ivars, F., Opdenakker, G., and Sorokin, L.M. (2006) Dystroglycan is selectively cleaved at the parenchymal basement membrane at sites of leukocyte extravasation in experimental autoimmune encephalomyelitis. J Exp Med 203: 1007-1019.
3. Andrews, K.T., and Lanzer, M. (2002) Maternal malaria: Plasmodium falciparum sequestration in the placenta. Parasitol Res 88: 715-723.
4. Basilico, N., Speciale, L., Parapini, S., Ferrante, P., and Taramelli, D. (2002) Endothelin-1 production by a microvascular endothelial cell line treated with Plasmodium falciparum parasitized red blood cells. Clin Sci (Lond) 103 (Suppl. 48): S464-S466.
5. Basilico, N., Tognazioli, C., Picot, S., Ravagnani, F., and Taramelli, D. (2003) Synergistic and antagonistic interactions between haemozoin and bacterial endotoxin on human and mouse macrophages. Parassitologia 45: 135-140.
6. Basilico, N., Parapini, S., Sisto, F., Omodeo-Sale, F., Coghi, P., Ravagnani, F., etal. (2010) The lipid moiety of haemozoin (Malaria Pigment) and P.falciparum parasitised red blood cells bind synthetic and native endothelin-1. J Biomed Biotechnol 2010: ID854927.
7. Beeson, J.G., Reeder, J.C., Rogerson, S.J., and Brown, G.V. (2001) Parasite adhesion and immune evasion in placental malaria. Trends Parasitol 17: 331-337.
8. Bonifacio, A., Finaurini, S., Krafft, C., Parapini, S., Taramelli, D., and Sergo, V. (2008) Spatial distribution of heme species in erythrocytes infected with Plasmodium falciparum by use of resonance Raman imaging and multivariate analysis. Anal Bioanal Chem 392: 1277-1282.
9. Bosman, G.J., Werre, J.M., Willekens, F.L., and Novotny, V.M. (2008) Erythrocyte ageing in vivo and in vitro: structural aspects and implications for transfusion. Transfus Med 18: 335-347.
10. Brown, H., Rogerson, S., Taylor, T., Tembo, M., Mwenechanya, J., Molyneux, M., and Turner, G. (2001) Blood-brain barrier function in cerebral malaria in Malawian children. Am J Trop Med Hyg 64: 207-213.
11. Cauwe, B., Van den Steen, P.E., and Opdenakker, G. (2007) The biochemical, biological, and pathological kaleidoscope of cell surface substrates processed by matrix metalloproteinases. Crit Rev Biochem Mol Biol 42: 113-185.
12. Chakravorty, S.J., Hughes, K.R., and Craig, A.G. (2008) Host response to cytoadherence in Plasmodium falciparum. Biochem Soc Trans 36: 221-228.
13. Chen, F., Ohashi, N., Li, W., Eckman, C., and Nguyen, J.H. (2009) Disruptions of occludin and claudin-5 in brain endothelial cells in vitro and in brains of mice with acute liver failure. Hepatology 50: 1914-1923.
14. Coltel, N., Combes, V., Hunt, N.H., and Grau, G.E. (2004) Cerebral malaria - a neurovascular pathology with many riddles still to be solved. Curr Neurovasc Res 1: 91-110.
15. Cuzner, M.L., and Opdenakker, G. (1999) Plasminogen activators and matrix metalloproteases, mediators of extracellular proteolysis in inflammatory demyelination of the central nervous system. J Neuroimmunol 94: 1-14.
16. D'Alessandro, S., Gelati, M., Basilico, N., Parati, E.A., Haynes, R.K., and Taramelli, D. (2007) Differential effects on angiogenesis of two antimalarial compounds, dihydroartemisinin and artemisone: implications for embryotoxicity. Toxicology 241: 66-74.
17. Deininger, M.H., Fimmen, B., Kremsner, P.G., Meyermann, R., and Schluesener, H.J. (2002) Accumulation of endostatin/collagenXVIII in brains of patients who died with cerebral malaria. J Neuroimmunol 131: 216-221.
18. Deininger, M.H., Winkler, S., Kremsner, P.G., Meyermann, R., and Schluesener, H.J. (2003) Angiogenic proteins in brains of patients who died with cerebral malaria. J Neuroimmunol 142: 101-111.
19. Dell'Agli, M., Galli, G.V., Bulgari, M., Basilico, N., Romeo, S., Bhattacharya, D., etal. (2010) Ellagitannins of the fruit rind of pomegranate (Punica granatum) antagonize in vitro the host inflammatory response mechanisms involved in the onset of malaria. Malar J 9: 208.
20. Dietmann, A., Helbok, R., Lackner, P., Issifou, S., Lell, B., Matsiegui, P.B., etal. (2008) Matrix metalloproteinases and their tissue inhibitors (TIMPs) in Plasmodium falciparum malaria: serum levels of TIMP-1 are associated with disease severity. J Infect Dis 197: 1614-1620.
21. Egan, T.J., Combrinck, J.M., Egan, J., Hearne, G.R., Marques, H.M., Ntenteni, S., etal. (2002) Fate of haem iron in the malaria parasite Plasmodium falciparum. Biochem J 365: 343-347.
22. Fauser, S., Deininger, M.H., Kremsner, P.G., Magdolen, V., Luther, T., Meyermann, R., and Schluesener, H.J. (2000) Lesion associated expression of urokinase-type plasminogen activator receptor (uPAR, CD87) in human cerebral malaria. J Neuroimmunol 111: 234-240.
23. Gearing, A.J., Beckett, P., Christodoulou, M., Churchill, M., Clements, J.M., Crimmin, M., etal. (1995) Matrix metalloproteinases and processing of pro-TNF-alpha. J Leukoc Biol 57: 774-777.
24. Geurts, N., Martens, E., Van Aelst, I., Proost, P., Opdenakker, G., and Van den Steen, P.E. (2008) Beta-hematin interaction with the hemopexin domain of gelatinase B/MMP-9 provokes autocatalytic processing of the propeptide, thereby priming activation by MMP-3. Biochemistry 47: 2689-2699.
25. Gillrie, M.R., Krishnegowda, G., Lee, K., Buret, A.G., Robbins, S.M., Looareesuwan, S., etal. (2007) Src-family kinase dependent disruption of endothelial barrier function by Plasmodium falciparum merozoite proteins. Blood 110: 3426-3435.
26. Giribaldi, G., Ulliers, D., Schwarzer, E., Roberts, I., Piacibello, W., and Arese, P. (2004) Hemozoin- and 4-hydroxynonenal-mediated inhibition of erythropoiesis. Possible role in malarial dyserythropoiesis and anemia. Haematologica 89: 492-493.
27. Giribaldi, G., Prato, M., Ulliers, D., Gallo, V., Schwarzer, E., Akide-Ndunge, O.B., etal. (2010) Involvement of inflammatory chemokines in survival of human monocytes fed with malarial pigment. Infect Immun 78: 4912-4921.
28. Goldie, P., Roth, E.F., Jr, Oppenheim, J., and Vanderberg, J.P. (1990) Biochemical characterization of Plasmodium falciparum hemozoin. Am J Trop Med Hyg 43: 584-596.
29. Grau, G.E., Mackenzie, C.D., Carr, R.A., Redard, M., Pizzolato, G., Allasia, C., etal. (2003) Platelet accumulation in brain microvessels in fatal pediatric cerebral malaria. J Infect Dis 187: 461-466.
30. Green, J.A., Thi Hong Chau, T., Farrar, J.J., Friedland, J.S., and Thwaites, G.E. (2011) CNS infection, CSF matrix metalloproteinase concentrations, and clinical/laboratory features. Neurology 76: 577-579.
31. Griffith, J.W., Sun, T., McIntosh, M.T., and Bucala, R. (2009) Pure hemozoin is inflammatory in vivo and activates the NALP3 inflammasome via release of uric acid. J Immunol 183: 5208-5220.
32. Hahn-Dantona, E., Ramos-DeSimone, N., Sipley, J., Nagase, H., French, D.L., and Quigley, J.P. (1999) Activation of proMMP-9 by a plasmin/MMP-3 cascade in a tumor cell model. Regulation by tissue inhibitors of metalloproteinases. Ann NY Acad Sci 878: 372-387.
33. Hanemaaijer, R., Koolwijk, P., le Clercq, L., de Vree, W.J., and van Hinsbergh, V.W. (1993) Regulation of matrix metalloproteinase expression in human vein and microvascular endothelial cells. Effects of tumour necrosis factor alpha, interleukin 1 and phorbol ester. Biochem J 296: 803-809.
34. Hu, J., Van den Steen, P.E., Sang, Q.X., and Opdenakker, G. (2007) Matrix metalloproteinase inhibitors as therapy for inflammatory and vascular diseases. Nat Rev Drug Discov 6: 480-498.
35. Hunt, N.H., and Grau, G.E. (2003) Cytokines: accelerators and brakes in the pathogenesis of cerebral malaria. Trends Immunol 24: 491-499.
36. Hunt, N.H., Golenser, J., Chan-Ling, T., Parekh, S., Rae, C., Potter, S., etal. (2006) Immunopathogenesis of cerebral malaria. Int J Parasitol 36: 569-582.
37. Ito, A., Mukaiyama, A., Itoh, Y., Nagase, H., Thogersen, I.B., Enghild, J.J., etal. (1996) Degradation of interleukin 1beta by matrix metalloproteinases. J Biol Chem 271: 14657-14660.
38. Jaramillo, M., Godbout, M., and Olivier, M. (2005) Hemozoin induces macrophage chemokine expression through oxidative stress-dependent and -independent mechanisms. J Immunol 174: 475-484.
39. Khadjavi, A., Giribaldi, G., and Prato, M. (2010) From control to eradication of malaria: the end of being stuck in second gear? Asian Pac J Trop Med 3: 412-420.
40. Masure, S., Billiau, A., Van Damme, J., and Opdenakker, G. (1990) Human hepatoma cells produce an 85 kDa gelatinase regulated by phorbol 12-myristate 13-acetate. Biochim Biophys Acta 1054: 317-325.
41. Medana, I.M., and Turner, G.D. (2006) Human cerebral malaria and the blood-brain barrier. Int J Parasitol 36: 555-568.
42. Mitola, S., Strasly, M., Prato, M., Ghia, P., and Bussolino, F. (2003) IL-12 regulates an endothelial cell-lymphocyte network: effect on metalloproteinase-9 production. J Immunol 171: 3725-3733.
43. Omodeo-Sale, F., Basilico, N., Folini, M., Olliaro, P., and Taramelli, D. (1998) Macrophage populations of different origins have distinct susceptibilities to lipid peroxidation induced by beta-haematin (malaria pigment). FEBS Lett 433: 215-218.
44. Omodeo-Sale, F., Motti, A., Basilico, N., Parapini, S., Olliaro, P., and Taramelli, D. (2003) Accelerated senescence of human erythrocytes cultured with Plasmodium falciparum. Blood 102: 705-711.
45. Opdenakker, G., Van den Steen, P.E., Dubois, B., Nelissen, I., Van Coillie, E., Masure, S., etal. (2001) Gelatinase B functions as regulator and effector in leukocyte biology. J Leukoc Biol 69: 851-859.
46. Overall, C.M., and Lopez-Otin, C. (2002) Strategies for MMP inhibition in cancer: innovations for the post-trial era. Nat Rev Cancer 2: 657-672.
47. Patnaik, J.K., Das, B.S., Mishra, S.K., Mohanty, S., Satpathy, S.K., and Mohanty, D. (1994) Vascular clogging, mononuclear cell margination, and enhanced vascular permeability in the pathogenesis of human cerebral malaria. Am J Trop Med Hyg 51: 642-647.
48. Pisciotta, J.M., and Sullivan, D. (2008) Hemozoin: oil versus water. Parasitol Int 57: 89-96.
49. Pongponratn, E., Turner, G.D., Day, N.P., Phu, N.H., Simpson, J.A., Stepniewska, K., etal. (2003) An ultrastructural study of the brain in fatal Plasmodium falciparum malaria. Am J Trop Med Hyg 69: 345-359.
50. Prato, M., and Giribaldi, G. (2011) Matrix metalloproteinase-9 and haemozoin: wedding rings for human host and Plasmodium falciparum parasite in complicated malaria. J Trop Med 2011: ID628435.
51. Prato, M., Giribaldi, G., Polimeni, M., Gallo, V., and Arese, P. (2005) Phagocytosis of hemozoin enhances matrix metalloproteinase-9 activity and TNF-alpha production in human monocytes: role of matrix metalloproteinases in the pathogenesis of falciparum malaria. J Immunol 175: 6436-6442.
52. Prato, M., Gallo, V., Giribaldi, G., and Arese, P. (2008) Phagocytosis of haemozoin (malarial pigment) enhances metalloproteinase-9 activity in human adherent monocytes: role of IL-1beta and 15-HETE. Malar J 7: 157.
53. Prato, M., Giribaldi, G., and Arese, P. (2009) Hemozoin triggers tumor necrosis factor alpha-mediated release of lysozyme by human adherent monocytes: new evidences on leukocyte degranulation in P.falciparum malaria. Asian Pac J Trop Med 2: 35-40.
54. Prato, M., Gallo, V., and Arese, P. (2010a) Higher production of tumor necrosis factor alpha in hemozoin-fed human adherent monocytes is dependent on lipidic component of malarial pigment: new evidences on cytokine regulation in Plasmodium falciparum malaria. Asian Pac J Trop Med 3: 85-89.
55. Prato, M., Gallo, V., Valente, E., Khadjavi, A., Mandili, G., and Giribaldi, G. (2010b) Malarial pigment enhances heat shock protein-27 in THP-1 cells: new perspectives for in vitro studies on monocyte apoptosis prevention. Asian Pac J Trop Med 3: 934-938.
56. Prato, M., Gallo, V., Giribaldi, G., Aldieri, E., and Arese, P. (2010c) Role of the NF-kappaB transcription pathway in the haemozoin- and 15-HETE-mediated activation of matrix metalloproteinase-9 in human adherent monocytes. Cell Microbiol 12: 1780-1791.
57. Rosenberg, G.A. (2002) Matrix metalloproteinases in neuroinflammation. Glia 39: 279-291.
58. Rosenberg, G.A., and Yang, Y. (2007) Vasogenic edema due to tight junction disruption by matrix metalloproteinases in cerebral ischemia. Neurosurg Focus 22: E4.
59. Schubert-Unkmeir, A., Konrad, C., Slanina, H., Czapek, F., Hebling, S., and Frosch, M. (2010) Neisseria meningitidis induces brain microvascular endothelial cell detachment from the matrix and cleavage of occludin: a role for MMP-8. PLoS Pathog 6: e1000874.
60. Schwarzer, E., Kuhn, H., Valente, E., and Arese, P. (2003) Malaria-parasitized erythrocytes and hemozoin nonenzymatically generate large amounts of hydroxy fatty acids that inhibit monocyte functions. Blood 101: 722-728.
61. Schwarzer, E., Skorokhod, O.A., Barrera, V., and Arese, P. (2008) Hemozoin and the human monocytes - a brief review of their interactions. Parassitologia 50: 143-145.
62. Shio, M.T., Kassa, F.A., Bellemare, M.J., and Olivier, M. (2010) Innate inflammatory response to the malarial pigment hemozoin. Microbes Infect 12: 889-899.
63. Skorokhod, O.A., Alessio, M., Mordmuller, B., Arese, P., and Schwarzer, E. (2004) Hemozoin (malarial pigment) inhibits differentiation and maturation of human monocyte-derived dendritic cells: a peroxisome proliferator-activated receptor-gamma-mediated effect. J Immunol 173: 4066-4074.
64. Skorokhod, O.A., Caione, L., Marrocco, T., Migliardi, G., Barrera, V., Arese, P., etal. (2010) Inhibition of erythropoiesis in malaria anemia: role of hemozoin and hemozoin-generated 4-hydroxynonenal. Blood 116: 4328-4337.
65. Strasly, M., Cavallo, F., Geuna, M., Mitola, S., Colombo, M.P., Forni, G., and Bussolino, F. (2001) IL-12 inhibition of endothelial cell functions and angiogenesis depends on lymphocyte-endothelial cell cross-talk. J Immunol 166: 3890-3899.
66. Szklarczyk, A., Stins, M., Milward, E.A., Ryu, H., Fitzsimmons, C., Sullivan, D., and Conant, K. (2007) Glial activation and matrix metalloproteinase release in cerebral malaria. J Neurovirol 13: 2-10.
67. Taramelli, D., Basilico, N., De Palma, A.M., Saresella, M., Ferrante, P., Mussoni, L., and Olliaro, P. (1998) The effect of synthetic malaria pigment (beta-haematin) on adhesion molecule expression and interleukin-6 production by human endothelial cells. Trans R Soc Trop Med Hyg 92: 57-62.
68. Taramelli, D., Recalcati, S., Basilico, N., Olliaro, P., and Cairo, G. (2000) Macrophage preconditioning with synthetic malaria pigment reduces cytokine production via heme iron-dependent oxidative stress. Lab Invest 80: 1781-1788.
69. Toth, M., Chvyrkova, I., Bernardo, M.M., Hernandez-Barrantes, S., and Fridman, R. (2003) Pro-MMP-9 activation by the MT1-MMP/MMP-2 axis and MMP-3: role of TIMP-2 and plasma membranes. Biochem Biophys Res Commun 308: 386-395.
70. Tripathi, A.K., Sullivan, D.J., and Stins, M.F. (2006) Plasmodium falciparum-infected erythrocytes increase intercellular adhesion molecule 1 expression on brain endothelium through NF-{kappa}B. Infect Immun 74: 3262-3270.
71. Tripathi, A.K., Sullivan, D.J., and Stins, M.F. (2007) Plasmodium falciparum-infected erythrocytes decrease the integrity of human blood-brain barrier endothelial cell monolayers. J Infect Dis 195: 942-950.
72. Tripathi, A.K., Sha, W., Shulaev, V., Stins, M.F., and Sullivan, D.J., Jr (2009) Plasmodium falciparum infected erythrocytes induce NF-{kappa}B regulated inflammatory pathways in human cerebral endothelium. Blood 114: 4243-4252.
73. Turner, G. (1997) Cerebral malaria. Brain Pathol 7: 569-582.
74. Van den Steen, P.E., Proost, P., Wuyts, A., Van Damme, J., and Opdenakker, G. (2000) Neutrophil gelatinase B potentiates interleukin-8 tenfold by aminoterminal processing, whereas it degrades CTAP-III, PF-4, and GRO-alpha and leaves RANTES and MCP-2 intact. Blood 96: 2673-2681.
75. Van den Steen, P.E., Van Aelst, I., Starckx, S., Maskos, K., Opdenakker, G., and Pagenstecher, A. (2006a) Matrix metalloproteinases, tissue inhibitors of MMPs and TACE in experimental cerebral malaria. Lab Invest 86: 873-888.
76. Van den Steen, P.E., Van Aelst, I., Hvidberg, V., Piccard, H., Fiten, P., Jacobsen, C., etal. (2006b) The hemopexin and O-glycosylated domains tune gelatinase B/MMP-9 bioavailability via inhibition and binding to cargo receptors. J Biol Chem 281: 18626-18637.
77. Van den Steen, P.E., Wuyts, A., Husson, S.J., Proost, P., Van Damme, J., and Opdenakker, G. (2003) Gelatinase B/MMP-9 and neutrophil collagenase/MMP-8 process the chemokines human GCP-2/CXCL6, ENA-78/CXCL5 and mouse GCP-2/LIX and modulate their physiological activities. Eur J Biochem 270: 3739-3749.
78. Van Lint, P., and Libert, C. (2007) Chemokine and cytokine processing by matrix metalloproteinases and its effect on leukocyte migration and inflammation. J Leukoc Biol 82: 1375-1381.
79. Vandooren, J., Geurts, N., Martens, E., Van den Steen, P.E., De Jonghe, S., Herdewijn, P., and Opdenakker, G. (2011) Gelatin degradation assay reveals MMP-9 inhibitors and function of O-glycosylated domain. World J Biol Chem 2: 14-24.
80. Wang, F.Q., So, J., Reierstad, S., and Fishman, D.A. (2005) Matrilysin (MMP-7) promotes invasion of ovarian cancer cells by activation of progelatinase. Int J Cancer 114: 19-31.