CD47-SIRPα interactions regulate macrophage uptake of Plasmodium falciparum-infected erythrocytes and clearance of malaria in vivo

Infection and Immunity

Volumn 84, Issue 7, 2016, Pages 2002-2011

  Ayi, Kodjo ^a   Lu, Ziyue ^a   Serghides, Lena ^a   Ho, Jenny M ^b   Finney, Constance ^a,d   Wang, Jean C Y ^b   Conrad Liles, W ^a,b,c   Kain, Kevin C ^a,b  

^a TORONTO GENERAL HOSPITAL   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF WASHINGTON   (United States)

^d UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CD47 ANTIGEN; HYBRID PROTEIN; REGULATOR PROTEIN; SIGNAL REGULATORY PROTEIN ALPHA; UNCLASSIFIED DRUG; CYTOKINE; IMMUNOGLOBULIN RECEPTOR; PROTEIN BINDING; PTPNS1 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ERYTHROCYTE; GENETIC VARIABILITY; IN VITRO STUDY; INNATE IMMUNITY; MACROPHAGE; MALARIA CONTROL; MALARIA FALCIPARUM; MOUSE; NONHUMAN; PARASITE CLEARANCE; PARASITE LOAD; PARASITEMIA; PHAGOCYTOSIS; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; ANIMAL; DISEASE MODEL; ENDOTHELIUM CELL; GROWTH, DEVELOPMENT AND AGING; HOST PARASITE INTERACTION; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; PARASITOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; ANTIGENS, CD47; CYTOKINES; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; ERYTHROCYTES; HOST-PARASITE INTERACTIONS; IMMUNITY, INNATE; MACROPHAGES; MALARIA, FALCIPARUM; MICE; MICE, KNOCKOUT; PHAGOCYTOSIS; PLASMODIUM FALCIPARUM; PROTEIN BINDING; RECEPTORS, IMMUNOLOGIC; SIGNAL TRANSDUCTION;

EID: 84976892921     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01426-15     Document Type: Article

References (53)

1. Lindberg FP, Gresham HD, Schwarz E, Brown EJ. 1993. Molecular cloning of integrin-associated protein: an immunoglobulin family member with multiple membrane-spanning domains implicated in alpha V beta 3 dependent ligand binding. J Cell Biol 123:485-496. http://dx.doi .org/10.1083/jcb.123.2.485.
2. Oldenborg PA, Zheleznyak A, Fang YF, Lagenaur CF, Gresham HD. 2000. Role of CD47 as a marker of self on red blood cells. Science 288: 2051-2054. http://dx.doi.org/10.1126/science.288.5473.2051.
3. Jaiswal S, Jamieson CH, Pang WW, Park CY, Chao MP, Majeti R, Traver D, van Rooijen N, Weissman IL. 2009. CD47 is upregulated on circulating hematopoietic stem cells and leukemia cells to avoid phagocytosis. Cell 138:271-285. http://dx.doi.org/10.1016/j.cell.2009.05.046.
4. Matozaki T, Murata Y, Okazawa H, Ohnishi H. 2009. Functions and molecular mechanisms of the CD47-SIRP alpha signalling pathway. Trends Cell Biol 19:72-80. http://dx.doi.org/10.1016/j.tcb.2008.12.001.
5. Ishikawa-Sekigami T, Kaneko Y, Okazawa H, Tomizawa T, Okajo J, Saito Y, Okuzawa C, Sugawara-Yokoo M, Nishiyama U, Ohnishi H, Matozaki T, Nojima Y. 2006. SHPS-1 promotes the survival of circulating erythrocytes through inhibition of phagocytosis by splenic macrophages. Blood 107:341-348. http://dx.doi.org/10.1182/blood-2005-05-1896.
6. Okazawa H, Motegi S, Ohyama N, Ohnishi H, Tomizawa T, Kaneko Y, Oldenborg PA, Ishikawa O, Matozaki T. 2005. Negative regulation of phagocytosis in macrophages by the CD47-SHPS-1 system. J Immunol 174:2004-2011. http://dx.doi.org/10.4049/jimmunol.174.4.2004.
7. Neznanov N, Neznanova L, Kondratov RV, Burdelya L, Kandel ES, O'Rourke DM, Ullrich A, Gudkov AV. 2003. Dominant negative form of signal-regulatory protein-alpha (SIRPalpha/SHPS-1) inhibits tumor necrosis factor-mediated apoptosis by activation of NF-kappa B. J Biol Chem 2003 278:3809-3815.
8. Lindberg FP, Bullard DC, Caver TE, Gresham HD, Beaudet AL, Brown EJ. 1996. Decreased resistance to bacterial infection and granulocyte defects in IAP-deficient mice. Science 274:795-798. http://dx.doi.org/10.1126/science.274.5288.795.
9. Verdrengh M, Lindberg FP, Ryden C, Tarkowski A. 1999. Integrinassociated protein (IAP)-deficient mice are less susceptible to developing Staphylococcus aureus-induced arthritis. Microbes Infect 1:745-751. http://dx.doi.org/10.1016/S1286-4579(99)80076-8.
10. Su X, Johansen M, Looney MR, Brown EJ, Matthay MA. 2008. CD47 deficiency protects mice from lipopolysaccharide-induced acute lung injury and Escherichia coli pneumonia. J Immunol 180:6947-6953. http: //dx.doi.org/10.4049/jimmunol.180.10.6947.
11. Fujioka Y, Matozaki T, Noguchi T, Iwamatsu A, Yamao T, Takahashi N, Tsuda M, Takada T, Kasuga M. 1996. A novel membrane glycoprotein, SHPS-1, that binds the SH2-domain-containing protein tyrosine phosphatase SHP-2 in response to mitogens and cell adhesion. Mol Cell Biol 16:6887-6899. http://dx.doi.org/10.1128/MCB.16.12.6887.
12. Stevenson MM, Riley EM. 2004. Innate immunity to malaria. Nat Rev Immunol 4:169-180. http://dx.doi.org/10.1038/nri1311.
13. Banerjee R, Khandelwal S, Kozakai Y, Sahu B, Kumar S. 2015. CD47 regulates the phagocytic clearance and replication of the Plasmodium yoelii malaria parasite. Proc Natl Acad Sci USA 112:3062-3067. http://dx.doi .org/10.1073/pnas.1418144112.
14. Serghides L, Kim H, Lu Z, Kain DC, Miller C, Francis RC, Liles WC, Zapol WM, Kain KC. 2011. Inhaled nitric oxide reduces endothelial activation and parasite accumulation in the brain, and enhances survival in experimental cerebral malaria. PLoS One 6:e27714. http://dx.doi.org /10.1371/journal.pone.0027714.
15. Ayi K, Turrini F, Piga A, Arese P. 2004. Enhanced phagocytosis of ring-parasitized mutant erythrocytes: a common mechanism that may explain protection against falciparum malaria in sickle trait and betathalassemia trait. Blood 104:3364-3371. http://dx.doi.org/10.1182/blood -2003-11-3820.
16. McGilvray ID, Serghides L, Kapus A, Rotstein OD, Kain KC. 2000. Nonopsonic monocyte/macrophage phagocytosis of Plasmodium falciparum- parasitized erythrocytes: a role for CD36 in malarial clearance. Blood 66:3231-3240.
17. Theocharides AP, Jin L, Cheng PY, Prasolava TK, Malko AV, Ho JM, Poeppl AG, van Rooijen N, Minden MD, Danska JS, Dick JE, Wang JC. 2012. Disruption of SIRPa signalling in macrophages eliminates human acute myeloid leukemia stem cells in xenografts. J Exp Med 209:1883-1899. http://dx.doi.org/10.1084/jem.20120502.
18. Patel SN, Serghides L, Smith TG, Silverstein RL, Kurtz TW, Pravenec M, Kain KC. 2004. CD36 mediates the phagocytosis of Plasmodium falciparum- infected erythrocytes by rodent macrophages. J Infect Dis 189: 204-213. http://dx.doi.org/10.1086/380764.
19. Carroll RW, Wainwright MS, Kim KY, Kidambi T, Gómez ND, Taylor T, Haldar K. 2010. A rapid murine coma and behavior scale for quantitative assessment of murine cerebral malaria. PLoS One 5:e13124. http: //dx.doi.org/10.1371/journal.pone.0013124.
20. Day NP, Hien TT, Schollaardt T, Loc PP, Chuong LV, Chau TT, Mai NT, Phu NH, Sinh DX, White NJ, Ho M. 1999. The prognostic and pathophysiologic role of pro- and anti-inflammatory cytokines in severe malaria. J Infect Dis 180:1288-1297. http://dx.doi.org/10.1086/315016.
21. Grau GE, Taylor TE, Molyneux ME, Wirima JJ, Vassalli P, Hommel M, Lambert PH. 1989. Tumor necrosis factor and disease severity in children with falciparum malaria. N Engl J Med 320:1586-1591. http://dx.doi.org /10.1056/NEJM198906153202404.
22. Mitchell AJ, Hansen AM, Hee L, Ball HJ, Potter SM, Walker JC, Hunt NH. 2005. Early cytokine production is associated with protection from murine cerebral malaria. Infect Immun 73:5645-5653. http://dx.doi.org /10.1128/IAI.73.9.5645-5653.2005.
23. Turner GD, Morrison H, Jones M, Davis TM, Looareesuwan S, Buley ID, Gatter KC, Newbold CI, Pukritayakamee S, Nagachinta B, White NJ, Berendt AR. 1994. An immunohistochemical study of the pathology of fatal malaria. Evidence for widespread endothelial activation and a potential role for intracellular adhesion molecule-1 in cerebral sequestration. Am J Pathol 145:1057-1069.
24. Lovegrove FE, Tangpukdee N, Opoka RO, Lafferty EI, Rajwans N, Hawkes M, Krudsood S, Looareesuwan S, John CC, Liles WC, Kain KC. 2009. Serum angiopoietin-1 and -2 levels discriminate cerebral malaria from uncomplicated malaria and predict clinical outcome in African children. PLoS One 4:e4912. http://dx.doi.org/10.1371/journal.pone.0004912.
25. Erdman LK, Dhabandia A, Musoke C, Conroy AL, Hawkes M, Higgins S, Rajwans N, Wolofsky KT, Streiner DL, Liles WC, Cserti-Gazdewich CM, Kain KC. 2011. Combinations of host biomarkers predict mortality among Uganda children with severe malaria: a retrospective case-control study. PLoS One 6:e17440. http://dx.doi.org/10.1371/journal.pone .0017440.
26. Veillette A, Thibaudeau E, Latour S. 1998. High expression of inhibitory receptor SHPS-1 and its association with protein-tyrosine phosphatase SHP-1 in macrophages. J Biol Chem 273:22719-22728. http://dx.doi.org /10.1074/jbc.273.35.22719.
27. Shultz LD, Schweitzer PA, Rajan TV, Yi T, Ihle JN. 1993. Mutations at the murine motheaten locus are within the hematopoietic cell proteintyrosine phosphatase (Hcph) gene. Cell 73:1445-1454. http://dx.doi.org /10.1016/0092-8674(93)90369-2.
28. Kozlowski M, Mlinaric-Rascan I, Feng GS, Shen R, Pawson T, Siminovitch KA. 1993. Expression and catalytic activity of the tyrosine phosphatase PTP1C is severely impaired in motheaten and viable motheaten mice. J Exp Med 178:2157-2163. http://dx.doi.org/10.1084/jem.178.6.2157.
29. Takenaka K, Prasolava TK, Wang JC, Mortin-Toth SM, Khalouei S, Gan OI, Dick JE, Danska JS. 2007. Polymorphism in Sirpa modulates engraftment of human hematopoietic stem cells. Nat Immunol 8:1313-1323. http://dx.doi.org/10.1038/ni1527.
30. Hempel C, Kohnke H, Maretty L, Jensen PØ, Staalsø T, Kurtzhals JA. 2014. Plasmodium falciparum avoids change in erythrocytic surface expression of phagocytosis markers during inhibition of nitric oxide synthase activity. Mol Biochem Parasitol 198:29-36. http://dx.doi.org/10.1016/j.molbiopara.2014.11.003.
31. Tilly AK, Thiede J, Metwally N, Lubiana P, Bachmann A, Roeder T, Rockliffe N, Lorenzen S, Tannich E, Gutsmann T, Bruchhaus I. 2015. Type of in vitro cultivation influences cytoadhesion, knob structure, protein localization and transcriptome profile of Plasmodium falciparum. Sci Rep 5:16766. http://dx.doi.org/10.1038/srep16766.
32. Turrini F, Giribaldi G, Carta F, Mannu F, Arese P. 2003. Mechanisms of band 3 oxidation and clustering in the phagocytosis of Plasmodium falciparum- infected erythrocytes. Redox Rep 8:300-303. http://dx.doi.org/10.1179/135100003225002943.
33. Bratosin D, Mazurier J, Tissier JP, Estaquier J, Huart JJ, Ameisen JC, Aminoff D, Montreuil J. 1998. Cellular and molecular mechanism of senescent erythrocyte phagocytosis by macrophages. A review. Biochimie 80:173-195. http://dx.doi.org/10.1016/S0300-9084(98)80024-2.
34. Lutz HU, Fasler S, Stammler P, Bussolino F, Arese P. 1988. Naturally occurring anti-band 3 antibodies and complement in phagocytosis of oxidatively- stressed and in clearance of senescent red cells. Blood Cells 14: 175-203.
35. Low PS, Waugh SM, Zinke K, Drenckhahn D. 1985. The role of hemoglobin denaturation and band 3 clustering in red blood cell aging. Science 227:531-533. http://dx.doi.org/10.1126/science.2578228.
36. Olsson M, Nilsson A, Oldenborg PA. 2006. Target cell CD47 regulates macrophage activation and erythrophagocytosis. Transfus Clin Biol 13: 39-43. http://dx.doi.org/10.1016/j.tracli.2006.02.013.
37. Olsson M, Oldenborg PA. 2008. CD47 on experimentally senescent murine RBCs inhibits phagocytosis following Fcgamma receptor-mediated but not scavenger receptor-mediated recognition by macrophages. Blood 112:4259-4267. http://dx.doi.org/10.1182/blood-2008-03-143008.
38. Khandelwal S, van Rooijen N, Saxena RK. 2007. Reduced expression of CD47 during murine red blood cell (RBC) senescence and its role in RBC clearance from the circulation. Transfusion 47:1725-1732. http://dx.doi .org/10.1111/j.1537-2995.2007.01348.x.
39. Burger P, Hilarius-Stokman P, de Korte D, van den Berg TK, van Bruggen R. 2012. CD47 functions as a molecular switch for erythrocyte phagocytosis. Blood 119:5512-5521. http://dx.doi.org/10.1182/blood -2011-10-386805.
40. Golenser J, Chevion M. 1989. Oxidative stress and malaria: host-parasite relationships in normal and abnormal erythrocytes. Semin Hematol 26: 313-325.
41. Hunt NH, Stocker R. 1990. Oxidative stress and the redox status of malaria-infected erythrocytes. Blood Cells 16:499-526.
42. Sosale NG, Rouhiparkouhi T, Bradshaw AM, Dimova R, Lipowsky R, Discher DE. 2015. Cell rigidity and shape override CD47's "self" signalling in phagocytosis by hyperactivating myosin-II. Blood 125:542-552. http://dx.doi.org/10.1182/blood-2014-06-585299.
43. Nacer A, Movila A, Baer K, Mikolajczak SA, Kappe SH, Frevert U. 2012. Neuroimmunological blood brain barrier opening in experimental cerebral malaria. PLoS Pathog 8:e1002982. http://dx.doi.org/10.1371/journal .ppat.1002982.
44. Hernandez-Valladares M, Naessens J, Musoke AJ, Sekikawa K, Rihet P, Ole-Moiyoi OK, Busher P, Iraqi FA. 2006. Pathology of Tnf-deficient mice infected with Plasmodium chabaudi adami 408XZ. Exp Parasitol 114:271-278. http://dx.doi.org/10.1016/j.exppara.2006.04.003.
45. Körner H, McMorran B, Schlüter D, Fromm P. 2010. The role of TNF in parasitic diseases: still more questions than answers. Int J Parasitol 40: 879-888. http://dx.doi.org/10.1016/j.ijpara.2010.03.011.
46. Demeure CE, Tanaka H, Mateo V, Rubio M, Delespesse G, Sarfati M. 2000. CD47 engagement inhibits cytokine production and maturation of human dendritic cells. J Immunol 164:2193-2199. http://dx.doi.org/10.4049/jimmunol.164.4.2193.
47. Oldenborg PA, Gresham HD, Lindberg FP. 2001. CD47-signal regulatory protein α (SIRPalpha) regulates Fcgamma and complement receptor- mediated phagocytosis. J Exp Med 193:855-862. http://dx.doi.org/10.1084/jem.193.7.855.
48. Waller KL, Stubberfield LM, Dubljevic V, Nunomura W, An X, Mason AJ. 2007. Interactions of Plasmodium falciparum erythrocyte membrane protein 3 with the red blood cell membrane skeleton. Biochim Biophys Acta 1768:2145-2156. http://dx.doi.org/10.1016/j.bbamem.2007.04.027.
49. Pei X, Guo X, Coppel R, Bhattacharjee S, Haldar K. 2007. The ringinfected erythrocyte surface antigen (RESA) of Plasmodium falciparum stabilizes spectrin tetramers and suppresses further invasion. Blood 110: 1036-1042. http://dx.doi.org/10.1182/blood-2007-02-076919.
50. Lutz HU. 2013. Comment concerning the role of CD47 and signal regulatory protein alpha in regulating the clearance of aged red blood cells. Transfus Med Hemother 40:140 -141. http://dx.doi.org/10.1159 /000350507.
51. Bruce LJ, Beckmann R, Ribeiro ML, Peters LL, Chasis JA. 2003. A band 3-based macrocomplex of integral and peripheral proteins in the RBC membrane. Blood 101:4180-4188. http://dx.doi.org/10.1182/blood-2002-09-2824.
52. Lutz HU, Bogdanova A. 2013. Mechanisms tagging senescent red blood cells for clearance in healthy humans. Front Physiol 4:387. http://dx.doi .org/10.3389/fphys.2013.00387.
53. Canadian Council on Animal Care. 1993. Guide to the care and use of experimental animals, 2nd ed, vol 1. Canadian Council on Animal Care, Ottawa, ON, Canada.