Endothelial activation and dysregulation in malaria: A potential target for novel therapeutics

Current Opinion in Hematology

Volumn 18, Issue 3, 2011, Pages 177-185

  Kim, Hani ^a   Higgins, Sarah ^a   Liles, W Conrad ^a,b   Kain, Kevin C ^a,b  

^a TORONTO GENERAL HOSPITAL   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

angiopoietin; endothelial activation; nitric oxide; severe malaria; vascular endothelial growth factor

Indexed keywords

ANGIOPOIETIN 1; ANGIOPOIETIN 2; ANGIOPOIETIN RECEPTOR; ARGININE; CARBON MONOXIDE; HEME OXYGENASE 1; NITRIC OXIDE; VASCULOTROPIN;

APOPTOSIS; ARTICLE; BRAIN MALARIA; CELL ACTIVATION; CELL FUNCTION; DISEASE SEVERITY; ENDOTHELIUM CELL; HUMAN; MORTALITY; NONHUMAN; PLASMODIUM; PRIORITY JOURNAL;

ANIMALS; ANTIMALARIALS; BIOLOGICAL MARKERS; ENDOTHELIAL CELLS; HUMANS; MALARIA, CEREBRAL; MOLECULAR TARGETED THERAPY; NITRIC OXIDE;

EID: 79955039531     PISSN: 10656251     EISSN: 15317048     Source Type: Journal    
DOI: 10.1097/MOH.0b013e328345a4cf     Document Type: Article

References (99)

1. WHO. World Malaria Report. 2010.
2. Boivin MJ. Effects of early cerebral malaria on cognitive ability in Senegalese children. J Dev Behav Pediatr 2002; 23:353-364. (Pubitemid 35244146)
3. Boivin MJ, BangiranaP, ByarugabaJ, et al. Cognitive impairment after cerebral malaria in children: a prospective study. Pediatrics 2007; 119:e360-e366. (Pubitemid 46397732)
4. Van Hensbroek MLB, Palmer A, Jaffar S, et al. Residual neurologic sequelae after childhood cerebral malaria. J Pediatr 1997; 131:125-129. (Pubitemid 27498320)
5. Dondorp A, Nosten F, Stepniewska K, et al. Artesunate versus quinine for treatment of severe falciparum malaria: a randomised trial. Lancet 2005; 366:717-725.
6. Dondorp AM, Fanello CI, Hendriksen ICE, et al. Artesunate versus quinine in the treatment of severe falciparum malaria in African children (AQUAMAT): an open-label, randomised trial. Lancet 2010; 376:1647-1657.
7. John CC, Kutamba E, Mugarura K, et al. Adjunctive therapy for cerebral malaria and other severe forms of Plasmodium falciparum malaria. Expert Rev Anti Infect Ther 2010; 8:997-1008.
8. Beare NAV, Harding SP, Taylor TE, et al. Perfusion abnormalities in children with cerebral malaria and malarial retinopathy. J Infect Dis 2009; 199:263-271.
9. White VA, Lewallen S, Beare NAV, et al. Retinal pathology of pediatric cerebral malaria in Malawi. PLoS One 2009; 4:e4317.
10. Conroy A, Phiri H, Hawkes M, et al. Endothelium-based biomarkers are associated with cerebral malaria in Malawian children: a retrospective case-control study. PLOS One 2010; 5:e15291.
11. Schofield L, Grau GE. Immunological processes in malaria pathogenesis. Nat Rev Immunol 2005; 5:722-735. (Pubitemid 43086173)
12. Li J-J, Huang Y-Q, Basch R, et al. Thrombin induces the release of angio-poietin-1 from platelets. Thromb Haemost 2001; 85:204-206. (Pubitemid 32140561)
13. Stratmann A, Risau W, Plate KH. Cell type-specific expression of angiopoie-tin-1 and angiopoietin-2 suggests a role in glioblastoma angiogenesis. Am J Pathol 1998; 153:1459-1466. (Pubitemid 28509902)
14. Davis S, Aldrich TH, Jones PF, et al. Isolation of angiopoietin-1,a ligandforthe TIE2 receptor, by secretion-Trap expression cloning. Cell 1996; 87:1161-1169. (Pubitemid 27010100)
15. Partanen J, Armstrong E, Makela TP, et al. A novel endothelial cell surface receptor tyrosine kinase with extracellular epidermal growth factor homology domains. Mol Cell Biol 1992; 12:1698-1707.
16. Dumont DJ, YamaguchiTP, Conlon RA, et al. Tek, a novel tyrosine kinase gene located on mouse chromosome 4, is expressed in endothelial cells and their presumptive precursors. Oncogene 1992; 7:1471-1480.
17. Fukuhara S, Sako K, Minami T, et al. Differential function of Tie2 at cell-cell contacts and cell-substratum contacts regulated by angiopoietin-1. Nat Cell Biol 2008; 10:513-526. (Pubitemid 351627371)
18. Saharinen P, Eklund L, Miettinen J, et al. Angiopoietins assemble distinct Tie2 signalling complexes in endothelial cell-cell and cell-matrix contacts. Nat Cell Biol 2008; 10:527-537. (Pubitemid 351627372)
19. Kim I, Moon S-O, Park SK, et al. Angiopoietin-1 reduces VEGF-stimulated leukocyte adhesion to endothelial cells by reducing ICAM-1, VCAM-1, and E-selectin expression. Circ Res 2001; 89:477-479. (Pubitemid 34132640)
20. Kim I, Oh J-L, Ryu YS, et al. Angiopoietin-1 negatively regulates expression and activity of tissue factor in endothelial cells. FASEB J 2002; 16:126-128.
21. Fiedler U, Scharpfenecker M, Koidl S, et al. The Tie-2 ligand angiopoietin-2 is stored in and rapidly released upon stimulation from endothelial cell Weibel-Palade bodies. Blood 2004; 103:4150-4156. (Pubitemid 38685356)
22. Maisonpierre PC, Suri C, Jones PF, et al. Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis. Science 1997; 277:55-60. (Pubitemid 27450643)
23. Reiss Y, Droste J, Heil M, et al. Angiopoietin-2 impairs revascularization after limb ischemia. Circ Res 2007; 101:88-96. (Pubitemid 47094627)
24. Fiedler U, Reiss Y, Scharpfenecker M, et al. Angiopoietin-2 sensitizes endothelial cells to TNF-alpha and has a crucial role in the induction of inflammation. Nat Med 2006; 12:235-239. (Pubitemid 43214752)
25. Conroy A, Lafferty E, Lovegrove F, et al. Whole blood angiopoietin-1 and -2 levels discriminate cerebral and severe (noncerebral) malaria from uncompli cated malaria. Malar J 2009; 8:295-301.
26. Yeo TW, Lampah DA, Gitawati R, et al. Angiopoietin-2 is associated with decreased endothelial nitric oxide and poor clinical outcome in severe falciparum malaria. Proc Natl Acad Sci USA 2008; 105:17097-17102.
27. Lovegrove FE, Tangpukdee N, Opoka RO, et al. Serum angiopoietin-1 and -2 levels discriminate cerebral malaria from uncomplicated malaria and predict clinical outcome in African children. PLoS One 2009; 4:e4912.
28. Kim DH, Jung YJ, Lee AS, et al. COMP-angiopoietin-1 decreases lipopoly-saccharide-induced acute kidney injury. Kidney Int 2009; 76:1180-1191.
29. Mei SH, McCarter SD, Deng Y, et al. Prevention of LPS-induced acute lung injury in mice by mesenchymal stem cells overexpressing angiopoietin 1. PLoS Med 2007; 4:e269.
30. Thurston G, Rudge JS, Ioffe E, et al. Angiopoietin-1 protects the adult vasculature against plasma leakage. Nat Med 2000; 6:460-463. (Pubitemid 30208166)
31. Van Slyke P, Alami J, Martin D, et al. Acceleration of diabetic wound healing by an angiopoietin peptide mimetic. Tissue Eng A 2009; 15:1269-1280.
32. Falcon BL, Hashizume H, Koumoutsakos P, et al. Contrasting actions of selective inhibitors of angiopoietin-1 and angiopoietin-2 on the normalization of tumor blood vessels. Am J Pathol 2009; 175:2159-2170.
33. Oliner J, Min H, Leal J, etal. Suppression of angiogenesis and tumor growth by selective inhibition of angiopoietin-2. Cancer Cell 2004; 6:507-516. (Pubitemid 39469986)
34. Tabruyn SP, Colton K, Morisada T, et al. Angiopoietin-2-driven vascular remodeling in airway inflammation. Am J Pathol 2010; 177:3233-3243.
35. Huang H. Angiopoietin-2 specific CVX-060 inhibits tumor growth coopera tively with chemotherapy. In: Annual Meeting of American Association of Cancer Research; San Diego, CA, USA.; 2008; Abstr. 2393.
36. Achen MG, Jeltsch M, Kukk E, et al. Vascular endothelial growth factor D (VEGF-D) is a ligand for the tyrosine kinases VEGF receptor 2 (Flk1) and VEGF receptor 3 (Flt4). Proc Natl Acad Sci USA 1998; 95:548-553. (Pubitemid 28083780)
37. Maglione D, GuerrieroV, VigliettoG, et al. Isolation of a human placenta cDNA coding for a protein related to the vascular permeability factor. Proc Natl Acad Sci USA 1991; 88:9267-9271. (Pubitemid 21915612)
38. Joukov V, Pajusola K, Kaipainen A, et al. A novel vascular endothelial growth factor, VEGF-C, is a ligand for the Flt4 (VEGFR-3) and KDR (VEGFR-2) receptor tyrosine kinases. EMBO J 1996; 15:1751. (Pubitemid 26112397)
39. Olofsson B, Pajusola K, Kaipainen A, et al. Vascular endothelial growth factor B, a novel growth factor for endothelial cells. Proc Natl Acad Sci USA 1996; 93:2576-2581. (Pubitemid 26104389)
40. Vries CD, Escobedo JA, Ueno H, et al. The fms-like tyrosine kinase, a receptor for vascular endothelial growth factor. Science 1992; 255:989-991.
41. Pajusola K, Aprelikova O, Korhonen J, et al. FLT4 receptor tyrosine kinase contains seven immunoglobulin-like loops and is expressed in multiple human tissues and cell lines. Cancer Res 1992; 52:5738-5743.
42. Quinn TP, Peters KG, De Vries C, et al. Fetal liver kinase 1 is a receptor for vascular endothelial growth factor and is selectively expressed in vascular endothelium. Proc Natl Acad Sci USA 1993; 90:7533-7537. (Pubitemid 23249984)
43. Senger DR, Galli SJ, Dvorak AM, et al. Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science 1983; 219:983-985.
44. Zhang ZG, Zhang L, Jiang Q, et al. VEGF enhances angiogenesis and promotes blood-brain barrier leakage in the ischemic brain. J Clin Invest 2000; 106:829-838.
45. Nottebaum AF, Cagna G, Winderlich M, et al. VE-PTP maintains the endothelial barrier via plakoglobin and becomes dissociated from VE-cadherin by leukocytes and by VEGF. J Exp Med 2008; 205:2929-2945.
46. Eliceiri BP, Paul R, Schwartzberg PL, et al. Selective requirement for Src kinases during VEGF-induced angiogenesis and vascular permeability. Mol Cell 1999; 4:915-924. (Pubitemid 30054898)
47. Eriksson A, Cao R, Roy J, et al. Small GTP-binding protein Rac is an essential mediator of vascular endothelial growth factor-induced endothelial fenestrations and vascular permeability. Circulation 2003; 107:1532-1538. (Pubitemid 36378493)
48. Matsushita K, Yamakuchi M, Morrell CN, et al. Vascular endothelial growth factor regulation of Weibel-Palade-body exocytosis. Blood 2005; 105:207-214. (Pubitemid 40053084)
49. Oh H, Takagi H, Suzuma K, et al. Hypoxia and vascular endothelial growth factor selectively up-regulateangiopoietin-2 in bovine microvascular endothelial cells. J Biol Chem 1999; 274:15732-15739.
50. Findley CM, Cudmore MJ, Ahmed A, et al. VEGF induces Tie2 shedding via a phosphoinositide 3-kinase/Akt dependent pathway to modulate Tie2 signaling. Arterioscler Thromb Vasc Biol 2007; 27:2619-2626. (Pubitemid 350158914)
51. Kim I, Moon S-O, Hoon Kim S, et al. Vascular endothelial growth factor expression of intercellular adhesion molecule 1 (ICAM-1), vascular cell adhesion molecule 1 (VCAM-1), and E-selectin through nuclear factor-KB activation in endothelial cells. J Biol Chem 2001; 276:7614-7620.
52. Casals-Pascual C, Idro R, Gicheru N, et al. High levels of erythropoietin are associated with protection against neurological sequelae in African children with cerebral malaria. Proc Natl Acad Sci USA 2008; 105:2634-2639. (Pubitemid 351520565)
53. Epiphanio S, Campos MG, Pamplona A, et al. VEGF promotes malaria-associated acute lung injury in mice. PLoS Pathog 2010; 6:e1000916.
54. Jain V, Armah HB, Tongren JE, et al. Plasma IP-10, apoptotic and angiogenic factors associated with fatal cerebral malaria in India. Malar J 2008; 7:83.
55. Sachanonta N, Medana IM, Roberts R, et al. Host vascular endothelial growth factor is trophic for Plasmodium falciparum-infected red blood cells. Asian Pac J Allergy Immunol 2008; 26:37-45. (Pubitemid 351843469)
56. Mohle R, Green D, Moore MAS, et al. Constitutive production and thrombin-induced release of vascular endothelial growth factor by human megakaryocytes and platelets. Proc Natl Acad Sci USA 1997; 94:663-668. (Pubitemid 27053690)
57. Isenberg JS, Martin-Manso G, Maxhimer JB, et al. Regulation of nitric oxide signalling bythrombospondin 1: implicationsforantiangiogenic therapies. Nat Rev Cancer 2009; 9:182-194.
58. Fukumura D, Gohongi T, Kadambi A, et al. Predominant role of endothelial nitric oxide synthase in vascular endothelial growth factor-induced angiogenesis and vascular permeability. Proc Natl Acad Sci USA 2001; 98:2604-2609. (Pubitemid 32209529)
59. Babaei S, Teichert-Kuliszewska K, Zhang Q, et al. Angiogenic actions of angiopoietin-1 require endothelium-derived nitric oxide. Am J Pathol 2003; 162:1927-1936. (Pubitemid 36613050)
60. Rockett KA, Awburn MM, Cowden WB, et al. Killing of Plasmodium falciparum in vitro by nitric oxide derivatives. Infect Immun 1991; 59:3280-3283.
61. Gramaglia I, Sobolewski P, Meays D, et al. Low nitric oxide bioavailability contributes to the genesis of experimental cerebral malaria. Nat Med 2006; 12:1417-1422. (Pubitemid 44924501)
62. Matsushita K, Morrell CN, Cambien B, etal. Nitric oxide regulates exocytosis by s-nitrosylation of N-ethylmaleimide-sensitive factor. Cell 2003; 115:139-150. (Pubitemid 37329578)
63. De Caterina R, Libby P, Peng HB, et al. Nitric oxide decreases cytokine-induced endothelial activation. Nitric oxide selectively reduces endothelial expression of adhesion molecules and proinflammatory cytokines. J Clin Invest 1995; 96:60-68.
64. SeriromS, Raharjo WH,Chotivanich K, et al. Antiadhesive effect of nitric oxide on Plasmodium falciparum cytoadherence under flow. Am J Pathol 2003; 162:1651-1660. (Pubitemid 36512848)
65. ZacharekA, Chen J, Zhang C, etal. Nitric oxide regulates angiopoietin 1/Tie2 expression after stroke. Neurosci Lett 2006; 404:28-32. (Pubitemid 44041773)
66. Iuvone T, D'Acquisto F, Carnuccio R, etal. Nitric oxide inhibits LPS-induced tumor necrosis factor synthesis in vitro and in vivo. Life Sci 1996; 59:L207-L211.
67. Perez-Ruiz A, Montes R, Velasco F, et al. Regulation by nitric oxide of endotoxin-induced tissue factor and plasminogen activator inhibitor-1 in endothelial cells. Thromb Haemost 2002; 88:1060-1065. (Pubitemid 36018796)
68. Lopansri BK, Anstey NM, Weinberg JB, et al. Low plasma arginine concentrations in children with cerebral malaria and decreased nitric oxide production. Lancet 2003; 361:676-678. (Pubitemid 36246553)
69. Anstey NM, Weinberg JB, Hassanali MY, et al. Nitric oxide in Tanzanian children with malaria: inverse relationship between malaria severity and nitric oxide production/nitric oxide synthase type 2 expression. J Exp Med 1996; 184:557-567. (Pubitemid 26324109)
70. YeoTW, Lampah DA, Gitawati R, etal. Impaired nitric oxide bioavailability and L-arginine reversible endothelial dysfunction in adults with falciparum malaria. J Exp Med 2007; 204:2693-2704. (Pubitemid 350044792)
71. Yeo TW, Lampah DA, Gitawati R, et al. Recovery of endothelial function in severe falciparum malaria: relationship with improvement in plasma L-arginine and blood lactate concentrations. J Infect Dis 2008; 198:602-608.
72. RotherRP, Bell L, Hillmen P, etal. The clinical sequelae of intravascular hemolysis and extracellular plasma hemoglobin. JAMA 2005; 293:1653-1662. (Pubitemid 40471796)
73. Reiter CD, Wang X, Tanus-Santos JE, et al. Cell-free hemoglobin limits nitric oxide bioavailability in sickle-cell disease. Nat Med 2002; 8:1383-1389. (Pubitemid 36019423)
74. Yeo TW, Lampah DA, Tjitra E, et al. Relationship of cell-free hemoglobin to impaired endothelial nitric oxide bioavailability and perfusion in severe falci parum malaria. J Infect Dis 2009; 200:1522-1529.
75. YeoTW, Lampah DA,Tjitra E, etal. Increased asymmetric dimethylarginine in severe falciparum malaria: association with impaired nitric oxide bioavailability and fatal outcome. PLoS Pathog 2010; 6:e1000868.
76. Yeo TW, Lampah DA, Gitawati R, et al. Safety profile of L-arginine infusion in moderately severe falciparum malaria. PLoS One 2008; 3:e2347.
77. Sokol J, Jacobs SE, Bohn D. Inhaled nitric oxide for acute hypoxic respiratory failure in children and adults: a meta-analysis. Anesth Analg 2003; 97:989-998. (Pubitemid 37158678)
78. Finer NN, Barrington KJ. Nitric oxide for respiratory failure in infants born at or near term. Cochrane Database Syst Rev 2006; 4:CD000399.
79. Barrington KJ, Finer NN. Inhaled nitric oxide for respiratory failure in preterm infants. Cochrane Database Syst Rev 2007; 3:CD000509.
80. Hunt NH, Stocker R. Heme moves to center stage in cerebral malaria. Nat Med 2007; 13:667-669. (Pubitemid 46889743)
81. Weinberg JB, Lopansri BK, Mwaikambo E, etal. Arginine, nitric oxide, carbon monoxide, and endothelial function in severe malaria. Curr Opin Infect Dis 2008; 21:468-475.
82. Pamplona A, Ferreira A, Balla J, et al. Heme oxygenase-1 and carbon monoxide suppress the pathogenesis of experimental cerebral malaria. Nat Med 2007; 13:703-710. (Pubitemid 46889755)
83. Chung HT, Choi BM, Kwon YG, etal. Interactive relations between nitric oxide (NO) and carbon monoxide (CO): heme oxygenase-1/CO pathway is a key modulator in NO-mediated antiapoptosis and antiinflammation. Methods Enzymol 2008; 441:329-338.
84. Bouton C, Demple B. Nitric oxide-inducible expression of heme oxygenase-1 in human cells. Translation-independent stabilization of the mRNA and evidence for direct action of nitric oxide. J Biol Chem 2000; 275:32688-32693.
85. Conroy A, Glover SJ, Hawkes M, et al. Angiopoietin-2-levels predict mortality in Malawian children with cerebral malaria: a retrospective case-control study. In: Annual Meeting of American Society of Tropical Medicine and Hygiene; Atlanta, GA, USA; 2010; Abstr. 541.
86. Erdman LK, Higgins S, Wolofsky KT, et al. Angiopoietin-2 and soluble Tie2 are associated with severe and fatal malaria in Ugandan children. In: Annual Meeting of American Society of Tropical Medicine and Hygiene; Washington, DC, USA; 2009; Abstr. 2923.
87. Clark I, Awburn M, Harper C, et al. Induction of HO-1 in tissue macrophages and monocytes in fatal falciparum malaria and sepsis. Malar J 2003; 2:41-53.
88. Cunnington AJ, Kendrick SFW, Wamola B, et al. Carboxyhemoglobin levels in Kenyan children with Plasmodium falciparum malaria. Am J Trop Med Hyg 2004; 71:43-47. (Pubitemid 38902642)
89. Lackner P, Burger C, Pfaller K, et al. Apoptosis in experimental cerebral malaria: spatial profile of cleaved caspase-3 and ultrastructural alterations in different disease stages. Neuropathol Appl Neurobiol 2007; 33:560-571. (Pubitemid 47390077)
90. Zang-Edou ES, Bisvigou U, Taoufiq Z, et al. Inhibition of Plasmodium falciparum field isolates-mediated endothelial cell apoptosis by fasudil: therapeutic implications for severe malaria. PLoS One 2010; 5:e13221.
91. Wilson NO, Huang MB, Anderson W, et al. Soluble factors from Plasmodium falciparum-infected erythrocytes induce apoptosis in human brain vascular endothelial and neuroglia cells. Mol Biochem Parasitol 2008; 162:172-176.
92. Taoufiq Z, Gay F, Balvanyos J, et al. Rho kinase inhibition in severe malaria: thwarting parasite-induced collateral damage to endothelia. J Infect Dis 2008; 197:1062-1073. (Pubitemid 351590036)
93. Pino P, Vouldoukis I, Kolb JP, et al. Plasmodium falciparum -infected erythrocyte adhesion induces caspase activation and apoptosis in human endothelial cells. J Infect Dis 2003; 187:1283-1290. (Pubitemid 36438969)
94. Toure FS, Ouwe-Missi-Oukem-Boyer O, Bisvigou U, et al. Apoptosis: a potential triggering mechanism of neurological manifestation in Plasmodium falciparum malaria. Parasite Immunol 2008; 30:47-51. (Pubitemid 350264529)
95. Helmers AJ, Lovegrove FE, Harlan JM, et al. Failure of two distinct antiapop-totic approaches to reduce mortality in experimental cerebral malaria. Am J Trop Med Hyg 2008; 79:823-825.
96. Waknine-Grinberg JH, McQuillan JA, Hunt N, et al. Modulation of cerebral malaria by fasudil and other immune-modifying compounds. Exp Parasitol 2010; 125:141-146.
97. Potter SM, Chan-Ling T, Rosinova E, et al. A role for Fas-Fas ligand interactions during the late-stage neuropathological processes of experimental cerebral malaria. J Neuroimmunol 2006; 173:96-107.
98. Bridges DJ, Bunn J, van Mourik JA, et al. Rapid activation of endothelial cells enables Plasmodium falciparum adhesion to platelet-decorated von Will-ebrand factor strings. Blood 2010; 115:1472-1474.
99. Mellberg S, Dimberg A, Bahram F, et al. Transcriptional profiling reveals a critical role for tyrosine phosphatase VE-PTP in regulation of VEGFR2 activity and endothelial cell morphogenesis. FASEB J 2009; 23:1490-1502.