CD36 and Fyn Kinase Mediate Malaria-Induced Lung Endothelial Barrier Dysfunction in Mice Infected with Plasmodium berghei

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Anidi, Ifeanyi U ^a   Servinsky, Laura E ^b   Rentsendorj, Otgonchimeg ^b   Stephens, R Scott ^b   Scott, Alan L ^a   Pearse, David B ^b  

^a JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^b DEPARTMENT OF PATHOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD36 ANTIGEN; HYDROGEN PEROXIDE; PROTEIN KINASE FYN; REACTIVE OXYGEN METABOLITE;

ALBUMIN REFLECTION COEFFICIENT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CD36 GENE; CELL COMPARTMENTALIZATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; CORRELATION ANALYSIS; ERYTHROCYTE; FYN GENE; GENE INACTIVATION; LUNG BLOOD VESSEL; LUNG ENDOTHELIUM; LUNG PERFUSION; MALARIA; MALE; MEMBRANE CONDUCTANCE; MEMBRANE PERMEABILITY; MICROVASCULAR ENDOTHELIAL CELL; MOUSE; NONHUMAN; PARACELLULAR FLUID CONDUCTANCE; PLASMODIUM BERGHEI; PROTEIN FUNCTION; PROTEIN SYNTHESIS; PULMONARY ENDOTHELIAL BARRIER; TRANSENDOTHELIAL ELECTRICAL RESISTANCE;

ANIMALS; ANTIGENS, CD36; BLOOD-AIR BARRIER; ERYTHROCYTES; GENE KNOCKDOWN TECHNIQUES; LUNG; MALARIA; MICE; MICE, KNOCKOUT; PERMEABILITY; PLASMODIUM BERGHEI; PNEUMOCYTES; PROTO-ONCOGENE PROTEINS C-FYN; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 84881573428     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0071010     Document Type: Article

References (61)

1. Mohan A, Sharma SK, Bollineni S, (2008) Acute lung injury and acute respiratory distress syndrome in malaria. J Vector Borne Dis 45: 179-193.
2. Taylor WR, Canon V, White NJ, (2006) Pulmonary manifestations of malaria: recognition and management. Treat Respir Med 5: 419-428.
3. Gruring C, Heiber A, Kruse F, Ungefehr J, Gilberger TW, et al. (2011) Development and host cell modifications of Plasmodium falciparum blood stages in four dimensions. Nat Commun 2: 165 ncomms1169 [pii];10.1038/ncomms1169 [doi].
4. Miller LH, Baruch DI, Marsh K, Doumbo OK, (2002) The pathogenic basis of malaria. Nature 415: 673-679.
5. Sherman IW, Eda S, Winograd E, (2003) Cytoadherence and sequestration in Plasmodium falciparum: defining the ties that bind. Microbes and Infection 5: 897-909.
6. Gamain B, Smith JD, Viebig NK, Gysin J, Scherf A, (2007) Pregnancy-associated malaria: parasite binding, natural immunity and vaccine development. Int J Parasitol 37: 273-283 S0020-7519(06)00403-6 [pii]; 10.1016/j.ijpara.2006.11.011 [doi].
7. Haldar K, Murphy SC, Milner DA, Taylor TE, (2007) Malaria: mechanisms of erythrocytic infection and pathological correlates of severe disease. Annu Rev Pathol 2: 217-249 10.1146/annurev.pathol.2.010506.091913 [doi].
8. Seydel KB, Milner DA Jr, Kamiza SB, Molyneux ME, Taylor TE, (2006) The distribution and intensity of parasite sequestration in comatose Malawian children. J Infect Dis 194: 208-5 JID35876 [pii]; 10.1086/505078 [doi].
9. Fonager J, Pasini EM, Braks JA, Klop O, Ramesar J, et al. (2012) Reduced CD36-dependent tissue sequestration of Plasmodium-infected erythrocytes is detrimental to malaria parasite growth in vivo. J Exp Med 209: 93-107.
10. Franke-Fayard B, Janse CJ, Cunha-Rodrigues M, Ramesar J, Buscher P, et al. (2005) Murine malaria parasite sequestration: CD36 is the major receptor, but cerebral pathology is unlinked to sequestration. Proc Natl Acad Sci U S A 102: 11468-11473.
11. Lovegrove FE, Gharib SA, Pena-Castillo L, Patel SN, Ruzinski JT, et al. (2008) Parasite burden and CD36-mediated sequestration are determinants of acute lung injury in an experimental malaria model. PLoS Pathog 4: e1000068.
12. van der Heyde HC, Bauer P, Sun G, Chang WL, Yin L, et al. (2001) Assessing vascular permeability during experimental cerebral malaria by a radiolabeled monoclonal antibody technique. Infect Immun 69: 3460-3465.
13. Chang WL, Jones SP, Lefer DJ, Welbourne T, Sun G, et al. (2001) CD8(+)-T-cell depletion ameliorates circulatory shock in Plasmodium berghei-infected mice. Infect Immun 69: 7341-7348.
14. Janse CJ, Waters AP (1995) Plasmodium berghei: the application of cultivation and purification techniques to molecular studies of malaria parasites. Parasitol Today 11: 138-143. 0169-4758(95)80133-2 [pii].
15. Mons B, Janse CJ, Boorsma EG, Van der Kaay HJ, (1985) Synchronized erythrocytic schizogony and gametocytogenesis of Plasmodium berghei in vivo and in vitro. Parasitology 91 (Pt 3): 423-430.
16. Cunha-Rodrigues M, Portugal S, Febbraio M, Mota MM, (2007) Bone marrow chimeric mice reveal a dual role for CD36 in Plasmodium berghei ANKA infection. Malar J 6: 32 1475-2875-6-32 [pii]; ---10.1186/1475-2875-6-32 [doi].
17. Bull HA, Brickell PM, Dowd PM, (1994) Src-related protein tyrosine kinases are physically associated with the surface antigen CD36 in human dermal microvascular endothelial cells. FEBS Lett 351: 41-44.
18. Jimenez B, Volpert OV, Crawford SE, Febbraio M, Silverstein RL, et al. (2000) Signals leading to apoptosis-dependent inhibition of neovascularization by thrombospondin-1. Nat Med 6: 41-48.
19. Michel CC, Curry FE, (1999) Microvascular permeability. Physiol Rev 79: 703-761.
20. Pearse DB, Becker PM, Permutt S, (2001) Effect of changing vascular volume on measurement of protein reflection coefficient in ischemic lungs. Am J Physiol Heart Circ Physiol 280: H918-H924.
21. Davis SP, Amrein M, Gillrie MR, Lee K, Muruve DA, et al. (2012) Plasmodium falciparum-induced CD36 clustering rapidly strengthens cytoadherence via p130CAS-mediated actin cytoskeletal rearrangement. FASEB J 26: 1119-1130 fj.11-196923 [pii]; -10.1096/fj.11-196923 [doi].
22. Han J, Shuvaev VV, Muzykantov VR, (2011) Catalase and superoxide dismutase conjugated with platelet-endothelial cell adhesion molecule antibody distinctly alleviate abnormal endothelial permeability caused by exogenous reactive oxygen species and vascular endothelial growth factor. J Pharmacol Exp Ther 338: 82-91 jpet.111.180620 [pii]; 10.1124/jpet.111.180620 [doi].
23. Pearse DB, Shimoda LA, Verin AD, Bogatcheva N, Moon C, et al. (2003) Effect of cGMP on lung microvascular endothelial barrier dysfunction following hydrogen peroxide. Endothelium 10: 309-317.
24. Atamna H, Ginsburg H, (1993) Origin of reactive oxygen species in erythrocytes infected with Plasmodium falciparum. Mol Biochem Parasitol 61: 231-241.
25. Butzloff S, Groves MR, Wrenger C, Muller IB, (2012) Cytometric quantification of singlet oxygen in the human malaria parasite Plasmodium falciparum. Cytometry A 81: 698-703 10.1002/cyto.a.22081 [doi].
26. Mishra NC, Kabilan L, Sharma A, (1994) Oxidative stress and malaria-infected erythrocytes. Indian J Malariol 31: 77-87.
27. Pino P, Vouldoukis I, Kolb JP, Mahmoudi N, Sportes-Livage I, et al. (2003) Plasmodium falciparum--infected erythrocyte adhesion induces caspase activation and apoptosis in human endothelial cells. J Infect Dis 187: 1283-1290.
28. Postma NS, Mommers EC, Eling WM, Zuidema J, (1996) Oxidative stress in malaria; implications for prevention and therapy. Pharm World Sci 18: 121-129.
29. Cambos M, Bazinet S, Abed E, Sanchez-Dardon J, Bernard C, et al. (2010) The IL-12p70/IL-10 interplay is differentially regulated by free heme and hemozoin in murine bone-marrow-derived macrophages. Int J Parasitol 40: 1003-1012 S0020-7519(10)00065-2 [pii]; 10.1016/j.ijpara.2010.02.007 [doi].
30. Qin Y, Lu M, Gong X, (2008) Dihydrorhodamine 123 is superior to 2,7-dichlorodihydrofluorescein diacetate and dihydrorhodamine 6G in detecting intracellular hydrogen peroxide in tumor cells. Cell Biology International 32: 224-228 doi: 10.1016/j.cellbi.2007.08.028.
31. Sakurada H, Koizumi H, Ohkawara A, Ueda T, Kamo N, (1992) Use of dihydrorhodamine 123 for detecting intracellular generation of peroxides upon UV irradiation in epidermal keratinocytes. Arch Dermatol Res 284: 114-116.
32. Cox-Singh J, Hiu J, Lucas SB, Divis PC, Zulkarnaen M, et al. (2010) Severe malaria - a case of fatal Plasmodium knowlesi infection with post-mortem findings: a case report. Malar J 9: 10 1475-2875-9-10 [pii]; ---10.1186/1475-2875-9-10 [doi].
33. Mota MM, Jarra W, Hirst E, Patnaik PK, Holder AA, (2000) Plasmodium chabaudi-infected erythrocytes adhere to CD36 and bind to microvascular endothelial cells in an organ-specific way. Infect Immun 68: 4135-4144.
34. Smith JD, Kyes S, Craig AG, Fagan T, Hudson-Taylor D, et al. (1998) Analysis of adhesive domains from the A4VAR Plasmodium falciparum erythrocyte membrane protein-1 identifies a CD36 binding domain. Mol Biochem Parasitol 97: 133-148.
35. Febbraio M, Hajjar DP, Silverstein RL, (2001) CD36: a class B scavenger receptor involved in angiogenesis, atherosclerosis, inflammation, and lipid metabolism. J Clin Invest 108: 785-791.
36. Curry FR, Adamson RH, (2010) Vascular permeability modulation at the cell, microvessel, or whole organ level: towards closing gaps in our knowledge. Cardiovasc Res 87: 218-229.
37. Schmidt EP, Yang Y, Janssen WJ, Gandjeva A, Perez MJ, et al. (2012) The pulmonary endothelial glycocalyx regulates neutrophil adhesion and lung injury during experimental sepsis. Nat Med. nm.2843 [pii]; 10.1038/nm.2843 [doi].
38. Moldobaeva A, Welsh-Servinsky LE, Shimoda LA, Stephens RS, Verin AD, et al. (2006) Role of protein kinase G in barrier-protective effects of cGMP in human pulmonary artery endothelial cells. Am J Physiol Lung Cell Mol Physiol 290: L919-L930.
39. Sponaas AM, Freitas do Rosario AP, Voisine C, Mastelic B, Thompson J, et al. (2009) Migrating monocytes recruited to the spleen play an important role in control of blood stage malaria. Blood 114: 5522-5531.
40. Deroost K, Tyberghein A, Lays N, Noppen S, Schwarzer E, et al. (2013) Hemozoin induces lung inflammation and correlates with malaria-associated acute respiratory distress syndrome. Am J Respir Cell Mol Biol 48: 589-600 rcmb.2012-0450OC [pii]; -10.1165/rcmb.2012-0450OC [doi].
41. Stevenson MM, Riley EM, (2004) Innate immunity to malaria. Nat Rev Immunol 4: 169-180 10.1038/nri1311 [doi];nri1311 [pii].
42. Gillrie MR, Krishnegowda G, Lee K, Buret AG, Robbins SM, et al. (2007) Src-family kinase dependent disruption of endothelial barrier function by Plasmodium falciparum merozoite proteins. Blood 110: 3426-3435.
43. Gillrie MR, Lee K, Gowda DC, Davis SP, Monestier M, et al. (2012) Plasmodium falciparum histones induce endothelial proinflammatory response and barrier dysfunction. Am J Pathol 180: 1028-1039.
44. Hu G, Minshall RD, (2009) Regulation of transendothelial permeability by Src kinase. Microvasc Res 77: 21-25.
45. Frame MC, Fincham VJ, Carragher NO, Wyke JA, (2002) v-Src's hold over actin and cell adhesions. Nat Rev Mol Cell Biol 3: 233-245.
46. Giannoni E, Buricchi F, Raugei G, Ramponi G, Chiarugi P, (2005) Intracellular reactive oxygen species activate Src tyrosine kinase during cell adhesion and anchorage-dependent cell growth. Mol Cell Biol 25: 6391-6403.
47. Appleby MW, Gross JA, Cooke MP, Levin SD, Qian X, et al. (1992) Defective T cell receptor signaling in mice lacking the thymic isoform of p59fyn. Cell 70: 751-763. 0092-8674(92)90309-Z [pii].
48. Filby A, Seddon B, Kleczkowska J, Salmond R, Tomlinson P, et al. (2007) Fyn regulates the duration of TCR engagement needed for commitment to effector function. J Immunol 179: 4635-4644. 179/7/4635 [pii].
49. Gadue P, Morton N, Stein PL, (1999) The Src family tyrosine kinase Fyn regulates natural killer T cell development. J Exp Med 190: 1189-1196.
50. Stein PL, Lee HM, Rich S, Soriano P (1992) pp59fyn mutant mice display differential signaling in thymocytes and peripheral T cells. Cell 70: 741-750. 0092-8674(92)90308-Y [pii].
51. Febbraio M, Abumrad NA, Hajjar DP, Sharma K, Cheng W, et al. (1999) A null mutation in murine CD36 reveals an important role in fatty acid and lipoprotein metabolism. J Biol Chem 274: 19055-19062.
52. Graewe S, Retzlaff S, Struck N, Janse CJ, Heussler VT, (2009) Going live: a comparative analysis of the suitability of the RFP derivatives RedStar, mCherry and tdTomato for intravital and in vitro live imaging of Plasmodium parasites. Biotechnol J 4: 895-902.
53. Rentsendorj O, Damarla M, Aggarwal NR, Choi JY, Johnston L, et al. (2011) Knockdown of lung phosphodiesterase 2A attenuates alveolar inflammation and protein leak in a two-hit mouse model of acute lung injury. Am J Physiol Lung Cell Mol Physiol 301: L161-L170.
54. Siracusa MC, Reece JJ, Urban JF Jr, Scott AL, (2008) Dynamics of lung macrophage activation in response to helminth infection. J Leukoc Biol 84: 1422-1433.
55. Dodd-o JM, Hristopoulos ML, Kibler K, Gutkowska J, Mukaddam-Daher S, et al. (2008) The role of natriuretic peptide receptor-A signaling in unilateral lung ischemia-reperfusion injury in the intact mouse. Am J Physiol Lung Cell Mol Physiol 294: L714-L723.
56. Pearse DB, Sylvester JT, (1996) Vascular injury in isolated sheep lungs. Role of ischemia, extracorporeal perfusion, and oxygen. Am J Respir Crit Care Med 153: 196-202.
57. Moldobaeva A, Wagner EM, (2005) Difference in proangiogenic potential of systemic and pulmonary endothelium: role of CXCR2. Am J Physiol Lung Cell Mol Physiol 288: L1117-L1123.
58. Stephens RS, Rentsendorj O, Servinsky LE, Moldobaeva A, Damico R, et al. (2010) cGMP increases antioxidant function and attenuates oxidant cell death in mouse lung microvascular endothelial cells by a protein kinase G-dependent mechanism. Am J Physiol Lung Cell Mol Physiol 299: L323-L333.
59. Bolcato-Bellemin AL, Bonnet ME, Creusat G, Erbacher P, Behr JP, (2007) Sticky overhangs enhance siRNA-mediated gene silencing. Proc Natl Acad Sci U S A 104: 16050-16055.
60. Rentsendorj O, Mirzapoiazova T, Adyshev D, Servinsky LE, Renne T, et al. (2008) Role of vasodilator-stimulated phosphoprotein in cGMP-mediated protection of human pulmonary artery endothelial barrier function. Am J Physiol Lung Cell Mol Physiol 294: L686-L697.
61. Schmidt EP, Damarla M, Rentsendorj O, Servinsky LE, Zhu B, et al. (2008) Soluble guanylyl cyclase contributes to ventilator-induced lung injury in mice. Am J Physiol Lung Cell Mol Physiol 295: L1056-L1065.