VEGF and LPS synergistically silence inflammatory response to Plasmodium berghei infection and protect against cerebral malaria

Pathogens and Global Health

Volumn 109, Issue 6, 2015, Pages 255-265

  Canavese, Miriam ^a   Dottorini, Tania ^a   Crisanti, Andrea ^a  

^a UNIVERSITY OF PERUGIA   (Italy)

Author keywords

Angiogenesis; Cerebral malaria; Cytokines; Inflammation; Vascular endothelial growth factor

Indexed keywords

AXITINIB; CHEMOKINE; CYTOKINE; GAMMA INTERFERON; HEME OXYGENASE 1; LIPOPOLYSACCHARIDE; TRANSCRIPTION FACTOR NRF2; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN; ACUTE PHASE PROTEIN; CARRIER PROTEIN; IMIDAZOLE DERIVATIVE; INDAZOLE DERIVATIVE; LIPOPOLYSACCHARIDE-BINDING PROTEIN; MEMBRANE PROTEIN; PROTEIN KINASE INHIBITOR; VASCULAR ENDOTHELIAL GROWTH FACTOR A, MOUSE; VASCULOTROPIN A;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BRAIN DYSFUNCTION; BRAIN MALARIA; CELL INFILTRATION; CONTROLLED STUDY; CONVULSION; DISEASE COURSE; FEMALE; GENE EXPRESSION ASSAY; GENE REPRESSION; GENETIC TRANSCRIPTION; HISTOLOGY; IMMUNOHISTOCHEMISTRY; MOUSE; NERVOUS SYSTEM PARAMETERS; NONHUMAN; PARASITEMIA; PLASMODIUM BERGHEI INFECTION; REGULATORY MECHANISM; SURVIVAL; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; DISEASE MODEL; DRUG EFFECTS; DRUG POTENTIATION; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; ISOLATION AND PURIFICATION; MALARIA, CEREBRAL; METABOLISM; PLASMODIUM BERGHEI; REGULATORY T LYMPHOCYTE;

ACUTE-PHASE PROTEINS; ANIMALS; CARRIER PROTEINS; DISEASE MODELS, ANIMAL; DRUG SYNERGISM; IMIDAZOLES; IMMUNE TOLERANCE; INDAZOLES; LIPOPOLYSACCHARIDES; MALARIA, CEREBRAL; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; PARASITEMIA; PLASMODIUM BERGHEI; PROTEIN KINASE INHIBITORS; T-LYMPHOCYTES, REGULATORY; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84944535133     PISSN: 20477724     EISSN: 20477732     Source Type: Journal    
DOI: 10.1179/2047773215Y.0000000018     Document Type: Article

References (64)

1. de Souza JB, Riley EM. Cerebral malaria: the contribution of studies in animal models to our understanding of immunopathogenesis. Microbes Infect. 2002;4(3):291-300.
2. Mishra SK, Newton CR. Diagnosis and management of the neurological complications of falciparum malaria. Nat. Rev. Neurol. 2009;5(4):189-98.
3. Miller LH, Ackerman HC, Su XZ, Wellems TE. Malaria biology and disease pathogenesis: insights for new treatments. Nat. Med. 2013;19(2):156-67.
4. Carvalho LJ, Moreira Ada S, Daniel-Ribeiro CT, Martins YC. Vascular dysfunction as a target for adjuvant therapy in cerebral malaria. Mem. Inst. Oswaldo Cruz. 2014;109(5):577-88.
5. 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.
6. Jain V, Lucchi NW, Wilson NO, Blackstock AJ, Nagpal AC, Joel PK, et al. Plasma levels of angiopoietin-1 and -2 predict cerebral malaria outcome in Central India. Malaria J. 2011; 10:383.
7. Jeney V, Ramos S, Bergman ML, Bechmann I, Tischer J, Ferreira A, et al. Control of disease tolerance to malaria by nitric oxide and carbon monoxide. Cell Rep. 2014;8(1):126-36.
8. Rushworth SA, Chen XL, Mackman N, Ogborne RM, O’Connell MA. Lipopolysaccharide-induced heme oxygenase-1 expression in human monocytic cells is mediated via Nrf2 and protein kinase C. J. Immunol. 2005;175(7):4408-15.
9. Shih RH, Yang CM. Induction of heme oxygenase-1 attenuates lipopolysaccharide-induced cyclooxygenase-2 expression in mouse brain endothelial cells. J. Neuroinflamm. 2010;7:86.
10. Bouloumie A, Schini-Kerth VB, Busse R. Vascular endothelial growth factor up-regulates nitric oxide synthase expression in endothelial cells. Cardiovasc. Res. 1999;41(3):773-80.
11. Servos S, Zachary I, Martin JF. VEGF modulates NO production: the basis of a cytoprotective effect? Cardiovasc. Res. 1999;41(3):509-10.
12. Hunt NH, Grau GE. Cytokines: accelerators and brakes in the pathogenesis of cerebral malaria. Trends Immunol. 2003;24(9): 491-9.
13. Kwiatkowski D, Hill AV, Sambou I, Twumasi P, Castracane J, Manogue KR, et al. TNF concentration in fatal cerebral, nonfatal cerebral, and uncomplicated Plasmodium falciparum malaria. Lancet. 1990;336(8725):1201-4.
14. Grau GE, Fajardo LF, Piguet PF, Allet B, Lambert PH, Vassalli P. Tumornecrosis factor (cachectin)asanessentialmediator inmurine cerebral malaria. Science. 1987;237(4819):1210-2.
15. Grau GE, Heremans H, Piguet PF, Pointaire P, Lambert PH, Billiau A, et al. Monoclonal antibody against interferon gamma can prevent experimental cerebral malaria and its associated overproduction of tumor necrosis factor. Proc. Natl. Acad. Sci. U.S.A. 1989;86(14):5572-4.
16. Miller LH, Baruch DI, Marsh K, Doumbo OK. The pathogenic basis of malaria. Nature. 2002;415(6872):673-9.
17. Amani V, Vigario AM, Belnoue E, Marussig M, Fonseca L, Mazier D, et al. Involvement of IFN-gamma receptormedicated signaling in pathology and anti-malarial immunity induced by Plasmodium berghei infection. Eur. J. Immunol. 2000;30(6):1646-55.
18. Lucas R, Juillard P, Decoster E, Redard M, Burger D, Donati Y, et al. Crucial role of tumor necrosis factor (TNF) receptor 2 and membrane-bound TNF in experimental cerebral malaria. Eur. J. Immunol. 1997;27(7):1719-25.
19. Armah H, Wired EK, Dodoo AK, Adjei AA, Tettey Y, Gyasi R. Cytokines and adhesion molecules expression in the brain in human cerebral malaria. Int. J. Environ. Res. Public Health. 2005;2(1):123-31.
20. Hunt NH, Ball HJ, Hansen AM, Khaw LT, Guo J, Bakmiwewa S, et al. Cerebral malaria: gamma-interferon redux. Front. Cell. Infect. Microbiol. 2014;4:113.
21. Hansen DS. Inflammatory responses associated with the induction of cerebral malaria: lessons from experimental murine models. PLoS Pathog. 2012;8(12):e1003045.
22. Goncalves RM, Scopel KK, Bastos MS, Ferreira MU. Cytokine balance in human malaria: does Plasmodium vivax elicit more inflammatory responses than Plasmodium falciparum? PLoS One. 2012;7(9):e44394.
23. Warrell DA, Looareesuwan S, Warrell MJ, Kasemsarn P, Intaraprasert R, Bunnag D, et al. Dexamethasone proves deleterious in cerebral malaria. A double-blind trial in 100 comatose patients. N. Engl. J. Med. 1982;306(6):313-9.
24. van Hensbroek MB, Palmer A, Onyiorah E, Schneider G, Jaffar S, Dolan G, et al. The effect of a monoclonal antibody to tumor necrosis factor on survival from childhood cerebral malaria. J. Infect. Dis. 1996;174(5):1091-7.
25. Grau GE, Frei K, Piguet PF, Fontana A, Heremans H, Billiau A, et al. Interleukin 6 production in experimental cerebral malaria: modulation by anticytokine antibodies and possible role in hypergammaglobulinemia. J.Exp.Med. 1990;172(5):1505-8.
26. Angulo I, Fresno M. Cytokines in the pathogenesis of and protection against malaria. Clin. Diagn. Lab. Immunol. 2002;9(6):1145-52.
27. Mitchell AJ, Hansen AM, Hee L, Ball HJ, Potter SM, Walker JC, et al. Early cytokine production is associated with protection from murine cerebral malaria. Infect. Immun. 2005; 73(9):5645-53.
28. Brown H, Turner G, Rogerson S, Tembo M, Mwenechanya J, Molyneux M, et al. Cytokine expression in the brain in human cerebral malaria. J. Infect. Dis. 1999;180(5):1742-6.
29. Yanez DM, Manning DD, Cooley AJ, Weidanz WP, van der Heyde HC. Participation of lymphocyte subpopulations in the pathogenesis of experimental murine cerebral malaria. J. Immunol. 1996;157(4):1620-4.
30. Tan RS, Kara AU, Feng C, Asano Y, Sinniah R. Differential interleukin-10 expression in interferon regulatory factor-1 deficient mice during Plasmodium berghei blood-stage infection. Parasite Immunol. 2000;22(9):425-35.
31. Pamplona A, Ferreira A, Balla J, Jeney V, Balla G, Epiphanio S, et al. Heme oxygenase-1 and carbon monoxide suppress the pathogenesis of experimental cerebral malaria. Nat. Med. 2007;13(6):703-10.
32. Ziegler-Heitbrock HW. Molecular mechanism in tolerance to lipopolysaccharide. J. Inflamm. 1995;45(1):13-26.
33. Camhi SL, Alam J, Otterbein L, Sylvester SL, Choi AM. Induction of heme oxygenase-1 gene expression by lipopolysaccharide is mediated by AP-1 activation. Am. J. Respir. Cell Mol. Biol. 1995;13(4):387-98.
34. Itaya H, Imaizumi T, Yoshida H, Koyama M, Suzuki S, Satoh K. Expression of vascular endothelial growth factor in human monocyte/macrophages stimulated with lipopolysaccharide. Thromb. Haemost. 2001;85(1):171-6.
35. Hu-Lowe DD, Zou HY, Grazzini ML, Hallin ME, Wickman GR, Amundson K, et al. Nonclinical antiangiogenesis and antitumor activities of axitinib (AG-013736), an oral, potent, and selective inhibitor of vascular endothelial growth factor receptor tyrosine kinases 1, 2, 3. Clin. Cancer Res. 2008;14(22):7272-83.
36. Namura S, Zhu J, Fink K, Endres M, Srinivasan A, Tomaselli KJ, et al. Activation and cleavage of caspase-3 in apoptosis induced by experimental cerebral ischemia. J. Neurosci. 1998;18(10):3659-68.
37. Gown AM, Willingham MC. Improved detection of apoptotic cells in archival paraffin sections: immunohistochemistry using antibodies to cleaved caspase 3. J. Histochem. Cytochem. 2002;50(4):449-54.
38. Rock EP, Roth EF Jr, Rojas-Corona RR, Sherwood JA, Nagel RL, Howard RJ, et al. Thrombospondin mediates the cytoadherence of Plasmodium falciparum-infected red cells to vascular endothelium in shear flow conditions. Blood. 1988;71(1):71-5.
39. Ferrara N, Gerber HP, Le Couter J. The biology of VEGF and its receptors. Nat. Med. 2003;9(6):669-76.
40. Dulak J, Deshane J, Jozkowicz A, Agarwal A. Heme oxygenase-1 and carbon monoxide in vascular pathobiology: focus on angiogenesis. Circulation. 2008;117(2):231-41.
41. Tuder RM, Flook BE, Voelkel NF. Increased gene expression for VEGF and the VEGF receptors KDR/Flk and Flt in lungs exposed to acute or to chronic hypoxia. Modulation of gene expression by nitric oxide. J. Clin. Invest. 1995;95(4):1798-807.
42. Bussolati B, Ahmed A, Pemberton H, Landis RC, Di Carlo F, Haskard DO, et al. Bifunctional role for VEGF-inducedhemeoxygenase-1 in vivo: induction of angiogenesis and inhibition of leukocytic infiltration. Blood. 2004;103(3):761-6.
43. Kim EH, Na HK, Surh YJ. Upregulation of VEGF by 15-deoxy-Delta12, 14-prostaglandin J2 via heme oxygenase-1 and ERK1/2 signaling in MCF-7 cells. Ann. N.Y. Acad. Sci. 2006;1090:375-84.
44. Bussolati B, Mason JC. Dual role of VEGF-induced hemeoxygenase-1 in angiogenesis. Antioxid. Redox Signal. 2006; 8(7-8):1153-63.
45. Lin HH, Chen YH, Chang PF, Lee YT, Yet SF, Chau LY. Heme oxygenase-1 promotes neovascularization in ischemic heart by coinduction of VEGF and SDF-1. J. Mol. Cell. Cardiol. 2008;45(1):44-55.
46. Morbidelli L, Chang CH, Douglas JG, Granger HJ, Ledda F, Ziche M. Nitric oxide mediates mitogenic effect of VEGF on coronary venular endothelium. Am. J. Physiol. 1996;270(1Pt2):H411-5.
47. Chen XL, Dodd G, Thomas S, Zhang X, Wasserman MA, Rovin BH, et al. Activation of Nrf2/ARE pathway protects endothelial cells from oxidant injury and inhibits inflammatory gene expression. Am. J. Physiol. Heart Circ. Physiol. 2006;290(5):H1862-70.
48. Radaelli E, Del Piero F, Aresu L, Sciarrone F, Vicari N, Mattiello S, et al. Expression of major histocompatibility complex class II antigens in porcine leptospiral nephritis. Vet. Pathol. 2009;46(5):800-9.
49. Tang KF, Ren H, Cao J, Zeng GL, Xie J, Chen M, et al. Decreased Dicer expression elicits DNA damage and up-regulation of MICA and MICB. J. Cell Biol. 2008;182(2): 233-9.
50. Li Y, Hazarika S, Xie D, Pippen AM, Kontos CD, Annex BH. In mice with type 2 diabetes, a vascular endothelial growth factor (VEGF)-activating transcription factor modulates VEGF signaling and induces therapeutic angiogenesis after hindlimb ischemia. Diabetes. 2007;56(3):656-65.
51. Clifford RL, Deacon K, Knox AJ. Novel regulation of vascular endothelial growth factor-A (VEGF-A) by transforming growth factor (beta)1: requirement for Smads, (beta)-CATENIN, AND GSK3(beta). J. Biol. Chem. 2008;283(51):35337-53.
52. Lee YJ, Karl DL, Maduekwe UN, Rothrock C, Ryeom S, D’Amore PA, et al. Differential effects of VEGFR-1 and VEGFR-2 inhibition on tumor metastases based on host organ environment. Cancer Res. 2010;70(21):8357-67.
53. Wakabayashi H, Takakura N, Yamauchi K, Tamura Y. Modulation of immunity-related gene expression in small intestines of mice by oral administration of lactoferrin. Clin. Vaccine Immunol. 2006;13(2):239-45.
54. Takada K, Inaba M, Ichioka N, Ueda Y, Taira M, Baba S, et al. Treatment of senile osteoporosis in SAMP6 mice by intra-bone marrow injection of allogeneic bone marrow cells. Stem Cells. 2006;24(2):399-405.
55. Xu M, Morishima N, Mizoguchi I, Chiba Y, Fujita K, Kuroda M, et al. Regulation of the development of acute hepatitis by IL-23 through IL-22 and IL-17 production. Eur. J. Immunol. 2011;41(10):2828-39.
56. Legat A, Thomas S, Hermand P, Van Mechelen M, Goldman M, De Wit D. CD14-independent responses induced by a synthetic lipid A mimetic. Eur. J. Immunol. 2010;40(3): 797-802.
57. Longhi LN, da Silva RM, Fornazim MC, Spago MC, de Oliveira RT, Nowill AE, et al. Phenotypic and functional characterization of NK cells in human immune response against the dimorphic fungus Paracoccidioides brasiliensis. J. Immunol. 2012;189(2):935-45.
58. Bolisetty S, Traylor AM, Kim J, Joseph R, Ricart K, Landar A, et al. Heme oxygenase-1 inhibits renal tubular macroautophagy in acute kidney injury. J. Am. Soc. Nephrol. 2010;21(10):1702-12.
59. Hull TD, Bolisetty S, De Almeida AC, Litovsky SH, Prabhu SD, Agarwal A, et al. Heme oxygenase-1 expression protects the heart from acute injury caused by inducible Cre recombinase. Lab. Invest. 2013;93(8):868-79.
60. Shih AY, Imbeault S, Barakauskas V, Erb H, Jiang L, Li P, et al. Induction of the Nrf2-driven antioxidant response confers neuroprotection during mitochondrial stress in vivo. J. Biol. Chem. 2005;280(24):22925-36.
61. Shih AY, Erb H, Murphy TH. Dopamine activates Nrf2- regulated neuroprotective pathways in astrocytes and meningeal cells. J. Neurochem. 2007;101(1):109-19.
62. Giulietti A, Overbergh L, Valckx D, Decallonne B, Bouillon R, Mathieu C. An overview of real-time quantitative PCR: applications to quantify cytokine gene expression. Methods. 2001;25(4):386-401.
63. Yee CS, Yao Y, Xu Q, McCarthy B, Sun-Lin D, Tone M, et al. Enhanced production of IL-10 by dendritic cells deficient in CIITA. J. Immunol. 2005;174(3):1222-9.
64. Myoung J, Kang HS, Hou W, Meng L, Dal Canto MC, Kim BS. Epitope-specific CD8+T cells play a differential pathogenic role in the development of a viral disease model for multiple sclerosis. J. Virol. 2012;86(24):13717-28.