Hostname: page-component-78c5997874-mlc7c Total loading time: 0 Render date: 2024-11-15T11:14:22.211Z Has data issue: false hasContentIssue false
  • English
  • Français

CD14+ monocytes are the main leucocytic sources of CXCL10 in response to Plasmodium falciparum

Published online by Cambridge University Press:  13 December 2019

Lisa J. Ioannidis ,
Emily Eriksson  and
Diana S. Hansen Open the ORCID record for Diana S. Hansen [Opens in a new window]
Lisa J. Ioannidis
Affiliation:
The Walter and Eliza Hall Institute of Medical Research, 1G Royal Parade, Parkville, Victoria3052, Australia The Department of Medical Biology, The University of Melbourne, Parkville, Victoria3010, Australia
Emily Eriksson
Affiliation:
The Walter and Eliza Hall Institute of Medical Research, 1G Royal Parade, Parkville, Victoria3052, Australia The Department of Medical Biology, The University of Melbourne, Parkville, Victoria3010, Australia
Diana S. Hansen*
Affiliation:
The Walter and Eliza Hall Institute of Medical Research, 1G Royal Parade, Parkville, Victoria3052, Australia The Department of Medical Biology, The University of Melbourne, Parkville, Victoria3010, Australia
*
Author for correspondence: Diana S. Hansen, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The CXCR3 chemokine CXCL10 or IFN-γ inducible protein 10 (IP-10) has been identified as an important biomarker of cerebral malaria (CM) mortality in children. Studies in mouse malaria infection models have shown that CXCL10 blockade alleviates brain intravascular inflammation and protects infected mice from CM. Despite the key role that CXCL10 plays in the development of CM, the leucocytic sources of CXCL10 in response to human malaria are not known. Here we investigated CXCL10 responses to Plasmodium falciparum in peripheral blood mononuclear cells (PBMCs). We found that PBMCs from malaria-unexposed donors produce CXCL10 in response to P. falciparum and that this response is IFN-γ-dependent. Moreover, CD14+ monocytes were identified as the main leucocytic sources of CXCL10 in peripheral blood, suggesting an important role for innate immune responses in the activation of this pathway involved in the development of symptomatic malaria.

Keywords

Chemokinesmalariamonocytespathogenesis
Type
Research Article
Information
Parasitology , Volume 147 , Issue 4 , April 2020 , pp. 465 - 470
Check for updates
Copyright
Copyright © Cambridge University Press 2019

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Amani, V, Vigario, AM, Belnoue, E, Marussig, M, Fonseca, L, Mazier, D and Renia, L (2000) Involvement of IFN-gamma receptor-medicated signaling in pathology and anti-malarial immunity induced by Plasmodium berghei infection. European Journal of Immunology 30, 1646–1655.3.0.CO;2-0>CrossRefGoogle ScholarPubMed
Armah, H, Dodoo, AK, Wiredu, EK, Stiles, JK, Adjei, AA, Gyasi, RK and Tettey, Y (2005) High-level cerebellar expression of cytokines and adhesion molecules in fatal, paediatric, cerebral malaria. Annals of Tropical Medicine & Parasitology 99, 629–647.CrossRefGoogle ScholarPubMed
Armah, HB, Wilson, NO, Sarfo, BY, Powell, MD, Bond, VC, Anderson, W, Adjei, AA, Gyasi, RK, Tettey, Y, Wiredu, EK, Tongren, JE, Udhayakumar, V and Stiles, JK (2007) Cerebrospinal fluid and serum biomarkers of cerebral malaria mortality in Ghanaian children. Malaria Journal 6, 147.CrossRefGoogle ScholarPubMed
Asensio, VC, Maier, J, Milner, R, Boztug, K, Kincaid, C, Moulard, M, Phillipson, C, Lindsley, K, Krucker, T, Fox, HS and Campbell, IL (2001) Interferon-independent, human immunodeficiency virus type 1 gp120-mediated induction of CXCL10/IP-10 gene expression by astrocytes in vivo and in vitro. Journal of Virology 75, 7067–7077.CrossRefGoogle ScholarPubMed
Bandow, K, Kusuyama, J, Shamoto, M, Kakimoto, K, Ohnishi, T and Matsuguchi, T (2012) LPS-induced chemokine expression in both MyD88-dependent and -independent manners is regulated by Cot/Tpl2-ERK axis in macrophages. FEBS Letters 586, 1540–1546.CrossRefGoogle ScholarPubMed
Bodnar, RJ, Yates, CC and Wells, A (2006) IP-10 blocks vascular endothelial growth factor-induced endothelial cell motility and tube formation via inhibition of calpain. Circulation Research 98, 617–625.CrossRefGoogle ScholarPubMed
Bouharoun-Tayoun, H, Oeuvray, C, Lunel, F and Druilhe, P (1995) Mechanisms underlying the monocyte-mediated antibody-dependent killing of Plasmodium falciparum asexual blood stages. Journal of Experimental Medicine 182, 409–418.CrossRefGoogle ScholarPubMed
Brownell, J, Bruckner, J, Wagoner, J, Thomas, E, Loo, YM, Gale, M Jr, Liang, TJ and Polyak, SJ (2014) Direct, interferon-independent activation of the CXCL10 promoter by NF-kappaB and interferon regulatory factor 3 during hepatitis C virus infection. Journal of Virology 88, 1582–1590.CrossRefGoogle ScholarPubMed
Campanella, GSV, Tager, AM, El Khoury, JK, Thomas, SY, Abrazinski, TA, Manice, LA, Colvin, RA and Lustert, AD (2008) Chemokine receptor CXCR3 and its ligands CXCL9 and CXCL10 are required for the development of murine cerebral malaria. Proceedings of the National Academy of Sciences of the USA 105, 4814–4819.CrossRefGoogle ScholarPubMed
Campanella, GS, Colvin, RA and Luster, AD (2010) CXCL10 can inhibit endothelial cell proliferation independently of CXCR3. PLoS ONE 5, e12700.CrossRefGoogle ScholarPubMed
Cheeran, MC, Hu, S, Sheng, WS, Peterson, PK and Lokensgard, JR (2003) CXCL10 production from cytomegalovirus-stimulated microglia is regulated by both human and viral interleukin-10. Journal of Virology 77, 4502–4515.CrossRefGoogle ScholarPubMed
D'Ombrain, MC, Hansen, DS, Simpson, KM and Schofield, L (2007a) Gammadelta-T cells expressing NK receptors predominate over NK cells and conventional T cells in the innate IFN-gamma response to Plasmodium falciparum malaria. European Journal of Immunology 37, 1864–1873.CrossRefGoogle Scholar
D'Ombrain, MC, Voss, TS, Maier, AG, Pearce, JA, Hansen, DS, Cowman, AF and Schofield, L (2007b) Plasmodium falciparum erythrocyte membrane protein-1 specifically suppresses early production of host interferon-gamma. Cell Host & Microbe 2, 130–138.CrossRefGoogle Scholar
Grau, GE, Mackenzie, CD, Carr, RA, Redard, M, Pizzolato, G, Allasia, C, Cataldo, C, Taylor, TE and Molyneux, ME (2003) Platelet accumulation in brain microvessels in fatal pediatric cerebral malaria. Journal of Infectious Diseases 187, 461–466.CrossRefGoogle ScholarPubMed
Hanum, S, Hayano, M and Kojima, S (2003) 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. International Immunology 15, 633–640.CrossRefGoogle Scholar
Hochman, SE, Madaline, TF, Wassmer, SC, Mbale, E, Choi, N, Seydel, KB, Whitten, RO, Varughese, J, Grau, GE, Kamiza, S, Molyneux, ME, Taylor, TE, Lee, S, Milner, DA Jr and Kim, K (2015) Fatal pediatric cerebral malaria is associated with intravascular monocytes and platelets that are increased with HIV co-infection. MBio 6, 1–15. doi: 10.1128/mBio.01390-15. doi: 10.1128/mBio.01390-15.CrossRefGoogle Scholar
Ioannidis, LJ, Nie, CQ and Hansen, DS (2014) The role of chemokines in severe malaria: more than meets the eye. Parasitology 141, 602–613.CrossRefGoogle ScholarPubMed
Ioannidis, LJ, Nie, CQ, Ly, A, Ryg-Cornejo, V, Chiu, CY and Hansen, DS (2016) Monocyte- and neutrophil-derived CXCL10 impairs efficient control of blood-stage malaria infection and promotes severe disease. Journal of Immunology 196, 1227–1238.CrossRefGoogle ScholarPubMed
Jain, V, Armah, HB, Tongren, JE, Ned, RM, Wilson, NO, Crawford, S, Joel, PK, Singh, MP, Nagpal, AC, Dash, AP, Udhayakumar, V, Singh, N and Stiles, JK (2008) Plasma IP-10, apoptotic and angiogenic factors associated with fatal cerebral malaria in India. Malaria Journal 7, 83.CrossRefGoogle ScholarPubMed
John, CC, Opika-Opoka, R, Byarugaba, J, Idro, R and Boivin, MJ (2006) Low levels of RANTES are associated with mortality in children with cerebral malaria. Journal of Infectious Diseases 194, 837–845.CrossRefGoogle ScholarPubMed
John, CC, Park, GS, Sam-Agudu, N, Opoka, RO and Bolvin, MJ (2008) Elevated serum levels of IL-1rα in children with Plasmodium falciparum malaria are associated with increased severity of disease. Cytokine 41, 204–208.CrossRefGoogle Scholar
Khaw, LT, Ball, HJ, Golenser, J, Combes, V, Grau, GE, Wheway, J, Mitchell, AJ and Hunt, NH (2013) Endothelial cells potentiate interferon-gamma production in a novel tripartite culture model of human cerebral malaria. PLoS ONE 8, e69521.CrossRefGoogle Scholar
King, T and Lamb, T (2015) Interferon-gamma: the Jekyll and Hyde of malaria. PLoS Pathogens 11, e1005118.CrossRefGoogle ScholarPubMed
Kopydlowski, KM, Salkowski, CA, Cody, MJ, van Rooijen, N, Major, J, Hamilton, TA and Vogel, SN (1999) Regulation of macrophage chemokine expression by lipopolysaccharide in vitro and in vivo. Journal of Immunology 163, 1537–1544.Google ScholarPubMed
Medoff, BD, Sauty, A, Tager, AM, Maclean, JA, Smith, RN, Mathew, A, Dufour, JH and Luster, AD (2002) IFN-gamma-inducible protein 10 (CXCL10) contributes to airway hyperreactivity and airway inflammation in a mouse model of asthma. Journal of Immunology 168, 5278–5286.CrossRefGoogle Scholar
Miller, LH, Baruch, DI, Marsh, K and Doumbo, OK (2002) The pathogenic basis of malaria. Nature 415, 673–679.CrossRefGoogle ScholarPubMed
Miu, J, Mitchell, AJ, Muller, M, Carter, SL, Manders, PM, McQuillan, JA, Saunders, BM, Ball, HJ, Lu, B, Campbell, LL and Hunt, NH (2008) Chemokine gene expression during fatal murine cerebral malaria and protection due to CXCR3 deficiency. Journal of Immunology 180, 1217–1230.CrossRefGoogle ScholarPubMed
Molyneux, ME, Engelmann, H, Taylor, TE, Wirima, JJ, Aderka, D, Wallach, D and Grau, GE (1993) Circulating plasma receptors for tumour necrosis factor in Malawian children with severe falciparum malaria. Cytokine 5, 604–609.CrossRefGoogle ScholarPubMed
Murphy, SC and Breman, JG (2001) Gaps in the childhood malaria burden in Africa: cerebral malaria, neurological sequelae, anemia, respiratory distress, hypoglycemia, and complications of pregnancy. American Journal of Tropical Medicine and Hygiene 64, 57–67.CrossRefGoogle ScholarPubMed
Nie, CQ, Bernard, NJ, Norman, MU, Amante, FH, Lundie, RJ, Crabb, BS, Heath, WR, Engwerda, CR, Hickey, MJ, Schofield, L and Hansen, DS (2009) IP-10-mediated T cell homing promotes cerebral inflammation over splenic immunity to malaria infection. PLoS Pathogens 5, e1000369.CrossRefGoogle ScholarPubMed
Park, C, Lee, S, Cho, IH, Lee, HK, Kim, D, Choi, SY, Oh, SB, Park, K, Kim, JS and Lee, SJ (2006) TLR3-mediated Signal induces proinflammatory cytokine and chemokine gene expression in astrocytes: differential signaling mechanisms of TLR3-induced IP-10 and IL-8 gene expression. Glia 53, 248–256.CrossRefGoogle ScholarPubMed
Patnaik, JK, Das, BS, Mishra, SK, Mohanty, S, Satpathy, SK and Mohanty, D (1994) Vascular clogging, mononuclear cell margination, and enhanced vascular permeability in the pathogenesis of human cerebral malaria. American Journal of Tropical Medicine and Hygiene 51, 642–647.CrossRefGoogle ScholarPubMed
Porta, J, Carota, A, Pizzolato, GP, Wildi, E, Widmer, MC, Margairaz, C and Grau, GE (1993) Immunopathological changes in human cerebral malaria. Clinical Neuropathology 12, 142–146.Google ScholarPubMed
Sorensen, EW, Lian, J, Ozga, AJ, Miyabe, Y, Ji, SW, Bromley, SK, Mempel, TR and Luster, AD (2018) CXCL10 stabilizes T cell-brain endothelial cell adhesion leading to the induction of cerebral malaria. JCI Insight 3, 1–19. doi: 10.1172/jci.insight.98911.CrossRefGoogle Scholar
Spurrell, JC, Wiehler, S, Zaheer, RS, Sanders, SP and Proud, D (2005) Human airway epithelial cells produce IP-10 (CXCL10) in vitro and in vivo upon rhinovirus infection. American Journal Of Physiology. Lung Cellular And Molecular Physiology 289, L85–L95.CrossRefGoogle ScholarPubMed
Stanisic, DI, Cutts, J, Eriksson, E, Fowkes, FJ, Rosanas-Urgell, A, Siba, P, Laman, M, Davis, TM, Manning, L, Mueller, I and Schofield, L (2014) Γδ T cells and CD14+ monocytes are predominant cellular sources of cytokines and chemokines associated with severe malaria. Journal of Infectious Diseases 210, 295–305.CrossRefGoogle ScholarPubMed
Taylor, TE, Fu, WJ, Carr, RA, Whitten, RO, Mueller, JS, Fosiko, NM, Lewallen, S, Liomba, NG and Molyneux, ME (2004) Differentiating the pathologies of cerebral malaria by postmortem parasite counts. Nature Medicine 10, 143–145.CrossRefGoogle ScholarPubMed
Turner, GD, Morrison, H, Jones, M, Davis, TM, Looareesuwan, S, Buley, ID, Gatter, KC, Newbold, CI, Pukritayakamee, S, Nagachinta, B, White, NJ and Berendt, AR (1994) An immunohistochemical study of the pathology of fatal malaria. Evidence for widespread endothelial activation and a potential role for intercellular adhesion molecule-1 in cerebral sequestration. American Journal of Pathology 145, 1057–1069.Google Scholar
van der Heyde, HC, Nolan, J, Combes, V, Gramaglia, I and Grau, GE (2006) A unified hypothesis for the genesis of cerebral malaria: sequestration, inflammation and hemostasis leading to microcirculatory dysfunction. Trends in Parasitology 22, 503–508.CrossRefGoogle ScholarPubMed
Walter, PR, Garin, Y and Blot, P (1982) Placental pathologic changes in malaria. A histologic and ultrastructural study. American Journal of Pathology 109, 330–342.Google ScholarPubMed
WHO (2016) World Malaria Report 2016. Geneva: World Health Organisation.Google Scholar
Wilson, NO, Jain, V, Roberts, CE, Lucchi, N, Joel, PK, Singh, MP, Nagpal, AC, Dash, AP, Udhayakumar, V, Singh, N and Stiles, JK (2011) CXCL4 And CXCL10 predict risk of fatal cerebral malaria. Disease Markers 30, 39–49.CrossRefGoogle ScholarPubMed
Yates-Binder, CC, Rodgers, M, Jaynes, J, Wells, A, Bodnar, RJ and Turner, T (2012) An IP-10 (CXCL10)-derived peptide inhibits angiogenesis. PLoS ONE 7, e40812.CrossRefGoogle ScholarPubMed
Ziegler-Heitbrock, L, Ancuta, P, Crowe, S, Dalod, M, Grau, V, Hart, DN, Leenen, PJ, Liu, YJ, MacPherson, G, Randolph, GJ, Scherberich, J, Schmitz, J, Shortman, K, Sozzani, S, Strobl, H, Zembala, M, Austyn, JM and Lutz, MB (2010) Nomenclature of monocytes and dendritic cells in blood. Blood 116, e74–e80.CrossRefGoogle ScholarPubMed
Supplementary material: File

Ioannidis et al. supplementary material

Figure S1

Download Ioannidis et al. supplementary material(File)
File 2.7 MB