Protective or pathogenic effects of vascular endothelial growth factor (VEGF) as potential biomarker in cerebral malaria

References

• Shikani HJ, Freeman BD, Lisanti MP, Weiss LM, Tanowitz HB, Desruisseaux MS. Cerebral malaria: we have come a long way. Am J Pathol. 2012;181(5):1484–92.
   PubMed Web of Science ®Google Scholar
• Newton CR, Krishna S. Severe falciparum malaria in children: current understanding of pathophysiology and supportive treatment. Pharmacol Ther. 1998;79(1):1–53.
   PubMed Web of Science ®Google Scholar
• Hunt NH, Grau GE. Cytokines: accelerators and brakes in the pathogenesis of cerebral malaria. Trends Immunol. 2003;24(9):491–9.
   PubMed Web of Science ®Google Scholar
• Martin C. Experimental use of nonhuman primates is not a simple problem. Nat Med. 2008;14(10):1011; discussion 1012–3.
   PubMed Web of Science ®Google Scholar
• Langhorne J, Buffet P, Galinski M, Good M, Harty J, Leroy D, et al. The relevance of non-human primate and rodent malaria models for humans. Malar J. 2011;10(1):23.
   PubMed Web of Science ®Google Scholar
• Jambou R, Combes V, Jambou MJ, Weksler BB, Couraud PO, Grau GE. Plasmodium falciparum adhesion on human brain microvascular endothelial cells involves transmigration-like cup formation and induces opening of intercellular junctions. PLoS Pathog. 2010;6(7):e1001021.
   Web of Science ®Google Scholar
• Khaw LT, Ball HJ, Golenser J, Combes V, Grau GE, Wheway J, et al. Endothelial cells potentiate interferon-gamma production in a novel tripartite culture model of human cerebral malaria. PLoS One. 2013;8(7):e69521.
   Web of Science ®Google Scholar
• Moxon CA, Wassmer SC, Milner DA Jr, Chisala NV, Taylor TE, Seydel KB, et al. Loss of endothelial protein C receptors links coagulation and inflammation to parasite sequestration in cerebral malaria in African children. Blood. 2013;122(5):842–51.
   PubMed Web of Science ®Google Scholar
• van der Poll T. The endothelial protein C receptor and malaria. Blood. 2013;122(5):624–5.
   PubMed Web of Science ®Google Scholar
• Abbott NJ, Ronnback L, Hansson E. Astrocyte-endothelial interactions at the blood–brain barrier. Nat Rev Neurosci. 2006;7(1):41–53.
   PubMed Web of Science ®Google Scholar
• Renia L, Howland SW, Claser C, Charlotte Gruner A, Suwanarusk R, Hui Teo T, et al. Cerebral malaria: mysteries at the blood–brain barrier. Virulence. 2012;3(2):193–201.
   PubMed Web of Science ®Google Scholar
• Medana IM, Turner GD. Human cerebral malaria and the blood–brain barrier. Int J Parasitol. 2006;36(5):555–68.
   PubMed Web of Science ®Google Scholar
• Penet MF, Viola A, Confort-Gouny S, Le Fur Y, Duhamel G, Kober F, et al. Imaging experimental cerebral malaria in vivo: significant role of ischemic brain edema. J Neurosci. 2005;25(32):7352–8.
   PubMed Web of Science ®Google Scholar
• Liu TP, Fu Y, Xu WY. Immunopathological mechanism of cerebral malaria. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi. 2011;29(1):64–7.
   PubMedGoogle Scholar
• Medana IM, Day NP, Roberts R, Sachanonta N, Turley H, Pongponratn E, et al. Induction of the vascular endothelial growth factor pathway in the brain of adults with fatal falciparum malaria is a non-specific response to severe disease. Histopathology. 2010;57(2):282–94.
   PubMed Web of Science ®Google Scholar
• Greenberg DA, Jin K. From angiogenesis to neuropathology. Nature. 2005;438(7070):954–9.
   PubMed Web of Science ®Google Scholar
• Ferrara N, Gerber HP, LeCouter J. The biology of VEGF and its receptors. Nat Med. 2003;9(6):669–76.
   PubMed Web of Science ®Google Scholar
• Ferrara N, Davis-Smyth T. The biology of vascular endothelial growth factor. Endocr Rev. 1997;18(1):4–25.
   PubMed Web of Science ®Google Scholar
• Gerber HP, Dixit V, Ferrara N. Vascular endothelial growth factor induces expression of the antiapoptotic proteins Bcl-2 and A1 in vascular endothelial cells. J Biol Chem. 1998;273(21):13313–6.
   PubMed Web of Science ®Google Scholar
• Yuan F, Chen Y, Dellian M, Safabakhsh N, Ferrara N, Jain RK. Time-dependent vascular regression and permeability changes in established human tumor xenografts induced by an anti-vascular endothelial growth factor/vascular permeability factor antibody. Proc Natl Acad Sci U S A. 1996;93(25):14765–70.
   PubMed Web of Science ®Google Scholar
• Senger DR, Galli SJ, Dvorak AM, Perruzzi CA, Harvey VS, Dvorak HF. Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science. 1983;219(4587):983–5.
   PubMed Web of Science ®Google Scholar
• Dvorak HF, Brown LF, Detmar M, Dvorak AM. Vascular permeability factor/vascular endothelial growth factor, microvascular hyperpermeability, and angiogenesis. Am J Pathol. 1995;146(5):1029–39.
   PubMed Web of Science ®Google Scholar
• Azzouz M, Ralph GS, Storkebaum E, Walmsley LE, Mitrophanous KA, Kingsman SM, et al. VEGF delivery with retrogradely transported lentivector prolongs survival in a mouse ALS model. Nature. 2004;429(6990):413–7.
   PubMed Web of Science ®Google Scholar
• Yeo TW, Lampah DA, Gitawati R, Tjitra E, Kenangalem E, Piera K, et al. Angiopoietin-2 is associated with decreased endothelial nitric oxide and poor clinical outcome in severe falciparum malaria. Proc Natl Acad Sci U S A. 2008;105(44):17097–102.
   PubMed Web of Science ®Google Scholar
• Gerber HP, Condorelli F, Park J, Ferrara N. Differential transcriptional regulation of the two vascular endothelial growth factor receptor genes. Flt-1, but not Flk-1/KDR, is up-regulated by hypoxia. J Biol Chem. 1997;272(38):23659–67.
   PubMed Web of Science ®Google Scholar
• LeCouter J, Moritz DR, Li B, Phillips GL, Liang XH, Gerber HP, et al. Angiogenesis-independent endothelial protection of liver: role of VEGFR-1. Science. 2003;299(5608):890–3.
   PubMed Web of Science ®Google Scholar
• Kawasaki T, Kitsukawa T, Bekku Y, Matsuda Y, Sanbo M, Yagi T, et al. A requirement for neuropilin-1 in embryonic vessel formation. Development. 1999;126(21):4895–902.
   PubMed Web of Science ®Google Scholar
• Niu G, Wright KL, Huang M, Song L, Haura E, Turkson J, et al. Constitutive Stat3 activity up-regulates VEGF expression and tumor angiogenesis. Oncogene. 2002;21(13):2000–8.
   PubMed Web of Science ®Google Scholar
• Furuta T, Kimura M, Watanabe N. Elevated levels of vascular endothelial growth factor (VEGF) and soluble vascular endothelial growth factor receptor (VEGFR)-2 in human malaria. Am J Trop Med Hyg. 2010;82(1):136–9.
   PubMed Web of Science ®Google Scholar
• Goldberg MA, Schneider TJ. Similarities between the oxygen-sensing mechanisms regulating the expression of vascular endothelial growth factor and erythropoietin. J Biol Chem. 1994;269(6):4355–9.
   PubMed Web of Science ®Google Scholar
• Cross MJ, Dixelius J, Matsumoto T, Claesson-Welsh L. VEGF-receptor signal transduction. Trends Biochem Sci. 2003;28(9):488–94.
   PubMed Web of Science ®Google Scholar
• Sondell M, Lundborg G, Kanje M. Vascular endothelial growth factor has neurotrophic activity and stimulates axonal outgrowth, enhancing cell survival and Schwann cell proliferation in the peripheral nervous system. J Neurosci. 1999;19(14):5731–40.
   PubMed Web of Science ®Google Scholar
• Silverman WF, Krum JM, Mani N, Rosenstein JM. Vascular, glial and neuronal effects of vascular endothelial growth factor in mesencephalic explant cultures. Neuroscience. 1999;90(4):1529–41.
   PubMed Web of Science ®Google Scholar
• Rosenstein JM, Mani N, Khaibullina A, Krum JM. Neurotrophic effects of vascular endothelial growth factor on organotypic cortical explants and primary cortical neurons. J Neurosci. 2003;23(35):11036–44.
   PubMed Web of Science ®Google Scholar
• Jin KL, Mao XO, Greenberg DA. Vascular endothelial growth factor rescues HN33 neural cells from death induced by serum withdrawal. J Mol Neurosci. 2000;14(3):197–203.
   PubMed Web of Science ®Google Scholar
• Jin KL, Mao XO, Greenberg DA. Vascular endothelial growth factor: direct neuroprotective effect in in vitro ischemia. Proc Natl Acad Sci U S A. 2000;97(18):10242–7.
   PubMed Web of Science ®Google Scholar
• Jin K, Mao XO, Batteur SP, McEachron E, Leahy A, Greenberg DA. Caspase-3 and the regulation of hypoxic neuronal death by vascular endothelial growth factor. Neuroscience. 2001;108(2):351–8.
   PubMed Web of Science ®Google Scholar
• Rosenstein JM, Mani N, Silverman WF, Krum JM. Patterns of brain angiogenesis after vascular endothelial growth factor administration in vitro and in vivo. Proc Natl Acad Sci U S A. 1998;95(12):7086–91.
   PubMed Web of Science ®Google Scholar
• Krum JM, Mani N, Rosenstein JM. Angiogenic and astroglial responses to vascular endothelial growth factor administration in adult rat brain. Neuroscience. 2002;110(4):589–604.
   PubMed Web of Science ®Google Scholar
• Oosthuyse B, Moons L, Storkebaum E, Beck H, Nuyens D, Brusselmans K, et al. Deletion of the hypoxia-response element in the vascular endothelial growth factor promoter causes motor neuron degeneration. Nat Genet. 2001;28(2):131–8.
   PubMed Web of Science ®Google Scholar
• Kalaria RN, Cohen DL, Premkumar DR, Nag S, LaManna JC, Lust WD. Vascular endothelial growth factor in Alzheimer’s disease and experimental cerebral ischemia. Brain Res Mol Brain Res. 1998;62(1):101–5.
   PubMedGoogle Scholar
• Del Bo R, Scarlato M, Ghezzi S, Martinelli Boneschi F, Fenoglio C, Galbiati S, et al. Vascular endothelial growth factor gene variability is associated with increased risk for AD. Ann Neurol. 2005;57(3):373–80.
   PubMed Web of Science ®Google Scholar
• Carmeliet P, Ruiz de Almodovar C. VEGF ligands and receptors: implications in neurodevelopment and neurodegeneration. Cell Mol Life Sci. 2013;70(10):1763–78.
   PubMed Web of Science ®Google Scholar
• Leung DW, Cachianes G, Kuang WJ, Goeddel DV, Ferrara N. Vascular endothelial growth factor is a secreted angiogenic mitogen. Science. 1989;246(4935):1306–9.
   PubMed Web of Science ®Google Scholar
• Krum JM, Khaibullina A. Inhibition of endogenous VEGF impedes revascularization and astroglial proliferation: roles for VEGF in brain repair. Exp Neurol. 2003;181(2):241–57.
   PubMed Web of Science ®Google Scholar
• Widenfalk J, Lipson A, Jubran M, Hofstetter C, Ebendal T, Cao Y, et al. Vascular endothelial growth factor improves functional outcome and decreases secondary degeneration in experimental spinal cord contusion injury. Neuroscience. 2003;120(4):951–60.
   PubMed Web of Science ®Google Scholar
• Jain V, Armah HB, Tongren JE, Ned RM, Wilson NO, Crawford S, et al. Plasma IP-10, apoptotic and angiogenic factors associated with fatal cerebral malaria in India. Malar J. 2008;7:83.
   PubMed Web of Science ®Google Scholar
• Muehlenbachs A, Mutabingwa TK, Edmonds S, Fried M, Duffy PE. Hypertension and maternal-fetal conflict during placental malaria. PLoS Med. 2006;3(11):e446.
   Web of Science ®Google Scholar
• Deininger MH, Winkler S, Kremsner PG, Meyermann R, Schluesener HJ. Angiogenic proteins in brains of patients who died with cerebral malaria. J Neuroimmunol. 2003;142(1–2):101–11.
   PubMed Web of Science ®Google Scholar
• Sachanonta N, Medana IM, Roberts R, Jones M, Day NP, White NJ, et al. Host vascular endothelial growth factor is trophic for Plasmodium falciparum-infected red blood cells. Asian Pac J Allergy Immunol. 2008;26(1):37–45.
   PubMed Web of Science ®Google Scholar
• Lu M, Perez VL, Ma N, Miyamoto K, Peng HB, Liao JK, et al. VEGF increases retinal vascular ICAM-1 expression in vivo. Invest Ophthalmol Vis Sci. 1999;40(8):1808–12.
   PubMed Web of Science ®Google Scholar
• Armah HB, Wilson NO, Sarfo BY, Powell MD, Bond VC, Anderson W, et al. Cerebrospinal fluid and serum biomarkers of cerebral malaria mortality in Ghanaian children. Malar J. 2007;6:147.
   PubMed Web of Science ®Google Scholar
• Epiphanio S, Campos MG, Pamplona A, Carapau D, Pena AC, Ataíde R, et al. VEGF promotes malaria-associated acute lung injury in mice. PLoS Pathog. 2010;6(5):e1000916.
   Web of Science ®Google Scholar
• Pongponratn E, Turner GD, Day NP, Phu NH, Simpson JA, Stepniewska K, et al. An ultrastructural study of the brain in fatal Plasmodium falciparum malaria. Am J Trop Med Hyg. 2003;69(4):345–59.
   PubMed Web of Science ®Google Scholar
• Casals-Pascual C, Idro R, Gicheru N, Gwer S, Kitsao B, Gitau E, et al. High levels of erythropoietin are associated with protection against neurological sequelae in African children with cerebral malaria. Proc Natl Acad Sci U S A. 2008;105(7):2634–9.
   PubMed Web of Science ®Google Scholar
• Croitoru-Lamoury J, Guillemin GJ, Boussin FD, Mognetti B, Gigout LI, Chéret A, et al. Expression of chemokines and their receptors in human and simian astrocytes: evidence for a central role of TNF alpha and IFN gamma in CXCR4 and CCR5 modulation. Glia. 2003;41(4):354–70.
   PubMed Web of Science ®Google Scholar
• Hanum PS, Hayano M, Kojima S. Cytokine and chemokine responses in a cerebral malaria-susceptible or -resistant strain of mice to Plasmodium berghei ANKA infection: early chemokine expression in the brain. Int Immunol. 2003;15(5):633–40.
   PubMed Web of Science ®Google Scholar
• Gengrinovitch S, Greenberg SM, Cohen T, Gitay-Goren H, Rockwell P, Maione TE, et al. Platelet factor-4 inhibits the mitogenic activity of VEGF121 and VEGF165 using several concurrent mechanisms. J Biol Chem. 1995;270(25):15059–65.
   PubMed Web of Science ®Google Scholar
• Lucchi NW, Jain V, Wilson NO, Singh N, Udhayakumar V, Stiles JK. Potential serological biomarkers of cerebral malaria. Dis Markers. 2011;31(6):327–35.
   PubMed Web of Science ®Google Scholar
• John CC, Panoskaltsis-Mortari A, Opoka RO, Park GS, Orchard PJ, Jurek AM, et al. Cerebrospinal fluid cytokine levels and cognitive impairment in cerebral malaria. Am J Trop Med Hyg. 2008;78(2):198–205.
   PubMed Web of Science ®Google Scholar
• John CC, Opika-Opoka R, Byarugaba J, Idro R, Boivin MJ. Low levels of RANTES are associated with mortality in children with cerebral malaria. J Infect Dis. 2006;194(6):837–45.
   PubMed Web of Science ®Google Scholar
• Conroy AL, Lafferty EI, Lovegrove FE, Krudsood S, Tangpukdee N, Liles WC, et al. Whole blood angiopoietin-1 and -2 levels discriminate cerebral and severe (non-cerebral) malaria from uncomplicated malaria. Malar J. 2009;8:295.
   PubMed Web of Science ®Google Scholar
• Lovegrove FE, Tangpukdee N, Opoka RO, Lafferty EI, Rajwans N, Hawkes M, 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(3):e4912.
   Web of Science ®Google Scholar
• Wilson NO, Jain V, Roberts CE, Lucchi N, Joel PK, Singh MP, et al. CXCL4 and CXCL10 predict risk of fatal cerebral malaria. Dis Markers. 2011;30(1):39–49.
   PubMed Web of Science ®Google Scholar
• Bangirana P, Giordani B, John CC, Page C, Opoka RO, Boivin MJ. Immediate neuropsychological and behavioral benefits of computerized cognitive rehabilitation in Ugandan pediatric cerebral malaria survivors. J Dev Behav Pediatr. 2009;30(4):310–8.
   PubMed Web of Science ®Google Scholar
• Lucchi NW, Demas A, Narayanan J, Sumari D, Kabanywanyi A, Kachur SP, et al. Real-time fluorescence loop mediated isothermal amplification for the diagnosis of malaria. PLoS One. 2010;5(10):e13733.
   Web of Science ®Google Scholar
• Lee WG, Kim YG, Chung BG, Demirci U, Khademhosseini A. Nano/microfluidics for diagnosis of infectious diseases in developing countries. Adv Drug Deliv Rev. 2010;62(4–5):449–57.
   PubMed Web of Science ®Google Scholar
• Zhao X, Bermak A, Boussaid F. A low cost CMOS polarimetric ophthalmoscope scheme for cerebral malaria diagnostic. Int Fed Inform Process. 2012;379:1–9.
   Google Scholar
• John CC, Kutamba E, Mugarura K, Opoka RO. Adjunctive therapy for cerebral malaria and other severe forms of Plasmodium falciparum malaria. Expert Rev Anti Infect Ther. 2010;8(9): 997–1008.
   PubMed Web of Science ®Google Scholar