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Published in: Malaria Journal 1/2021

01-12-2021 | Plasmodium Falciparum | Research

Phagocytosis and activation of bone marrow‐derived macrophages by Plasmodium falciparum gametocytes

Authors: Yolanda Corbett, Silvia Parapini, Federica Perego, Valeria Messina, Serena Delbue, Paola Misiano, Mario Falchi, Francesco Silvestrini, Donatella Taramelli, Nicoletta Basilico, Sarah D’Alessandro

Published in: Malaria Journal | Issue 1/2021

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Abstract

Background

The innate immune response against various life cycle stages of the malaria parasite plays an important role in protection against the disease and regulation of its severity. Phagocytosis of asexual erythrocytic stages is well documented, but little and contrasting results are available about phagocytic clearance of sexual stages, the gametocytes, which are responsible for the transmission of the parasites from humans to mosquitoes. Similarly, activation of host macrophages by gametocytes has not yet been carefully addressed.

Methods

Phagocytosis of early or late Plasmodium falciparum gametocytes was evaluated through methanol fixed cytospin preparations of immortalized mouse C57Bl/6 bone marrow-derived macrophages treated for 2 h with P. falciparum and stained with Giemsa, and it was confirmed through a standardized bioluminescent method using the transgenic P. falciparum 3D7elo1-pfs16-CBG99 strain. Activation was evaluated by measuring nitric oxide or cytokine levels in the supernatants of immortalized mouse C57Bl/6 bone marrow-derived macrophages treated with early or late gametocytes.

Results

The results showed that murine bone marrow-derived macrophages can phagocytose both early and late gametocytes, but only the latter were able to induce the production of inflammatory mediators, specifically nitric oxide and the cytokines tumour necrosis factor and macrophage inflammatory protein 2.

Conclusions

These results support the hypothesis that developing gametocytes interact in different ways with innate immune cells of the host. Moreover, the present study proposes that early and late gametocytes act differently as targets for innate immune responses.
Literature
1.
go back to reference WHO. World Malaria Report. Geneva, World Health Organization, 2020. WHO. World Malaria Report. Geneva, World Health Organization, 2020.
2.
go back to reference Ngotho P, Soares AB, Hentzschel F, Achcar F, Bertuccini L, Marti M. Revisiting gametocyte biology in malaria parasites. FEMS Microbiol Rev. 2019;43:401–14.PubMedPubMedCentralCrossRef Ngotho P, Soares AB, Hentzschel F, Achcar F, Bertuccini L, Marti M. Revisiting gametocyte biology in malaria parasites. FEMS Microbiol Rev. 2019;43:401–14.PubMedPubMedCentralCrossRef
3.
go back to reference Joice R, Nilsson SK, Montgomery J, Dankwa S, Egan E, Morahan B, et al. Plasmodium falciparum transmission stages accumulate in the human bone marrow. Sci Transl Med. 2014;6:244re245.CrossRef Joice R, Nilsson SK, Montgomery J, Dankwa S, Egan E, Morahan B, et al. Plasmodium falciparum transmission stages accumulate in the human bone marrow. Sci Transl Med. 2014;6:244re245.CrossRef
4.
go back to reference De Niz M, Meibalan E, Mejia P, Ma S, Brancucci NMB, Agop-Nersesian C, et al. gametocytes display homing and vascular transmigration in the host bone marrow. Sci Adv. 2018;4:eaat3775.PubMedPubMedCentralCrossRef De Niz M, Meibalan E, Mejia P, Ma S, Brancucci NMB, Agop-Nersesian C, et al. gametocytes display homing and vascular transmigration in the host bone marrow. Sci Adv. 2018;4:eaat3775.PubMedPubMedCentralCrossRef
5.
go back to reference Farfour E, Charlotte F, Settegrana C, Miyara M, Buffet P. The extravascular compartment of the bone marrow: a niche for Plasmodium falciparum gametocyte maturation? Malar J. 2012;11:285.PubMedPubMedCentralCrossRef Farfour E, Charlotte F, Settegrana C, Miyara M, Buffet P. The extravascular compartment of the bone marrow: a niche for Plasmodium falciparum gametocyte maturation? Malar J. 2012;11:285.PubMedPubMedCentralCrossRef
6.
go back to reference Abdulsalam AH, Sabeeh N, Bain BJ. Immature Plasmodium falciparum gametocytes in bone marrow. Am J Hematol. 2010;85:943.PubMedCrossRef Abdulsalam AH, Sabeeh N, Bain BJ. Immature Plasmodium falciparum gametocytes in bone marrow. Am J Hematol. 2010;85:943.PubMedCrossRef
7.
go back to reference Aguilar R, Magallon-Tejada A, Achtman AH, Moraleda C, Joice R, Cisteró P, et al. Molecular evidence for the localization of Plasmodium falciparum immature gametocytes in bone marrow. Blood. 2014;123:959–66.PubMedPubMedCentralCrossRef Aguilar R, Magallon-Tejada A, Achtman AH, Moraleda C, Joice R, Cisteró P, et al. Molecular evidence for the localization of Plasmodium falciparum immature gametocytes in bone marrow. Blood. 2014;123:959–66.PubMedPubMedCentralCrossRef
8.
go back to reference Craig AG, Khairul MF, Patil PR. Cytoadherence and severe malaria. Malays J Med Sci. 2012;19:5–18.PubMed Craig AG, Khairul MF, Patil PR. Cytoadherence and severe malaria. Malays J Med Sci. 2012;19:5–18.PubMed
9.
go back to reference Silvestrini F, Tibúrcio M, Bertuccini L, Alano P. Differential adhesive properties of sequestered asexual and sexual stages of Plasmodium falciparum on human endothelial cells are tissue independent. PLoS One. 2012;7:e31567.PubMedPubMedCentralCrossRef Silvestrini F, Tibúrcio M, Bertuccini L, Alano P. Differential adhesive properties of sequestered asexual and sexual stages of Plasmodium falciparum on human endothelial cells are tissue independent. PLoS One. 2012;7:e31567.PubMedPubMedCentralCrossRef
10.
go back to reference Rogers NJ, Targett GA, Hall BS. Plasmodium falciparum gametocyte adhesion to C32 cells via CD36 is inhibited by antibodies to modified band 3. Infect Immun. 1996;64:4261–8.PubMedPubMedCentralCrossRef Rogers NJ, Targett GA, Hall BS. Plasmodium falciparum gametocyte adhesion to C32 cells via CD36 is inhibited by antibodies to modified band 3. Infect Immun. 1996;64:4261–8.PubMedPubMedCentralCrossRef
11.
go back to reference Rogers NJ, Hall BS, Obiero J, Targett GA, Sutherland CJ. A model for sequestration of the transmission stages of Plasmodium falciparum: adhesion of gametocyte-infected erythrocytes to human bone marrow cells. Infect Immun. 2000;68:3455–62.PubMedPubMedCentralCrossRef Rogers NJ, Hall BS, Obiero J, Targett GA, Sutherland CJ. A model for sequestration of the transmission stages of Plasmodium falciparum: adhesion of gametocyte-infected erythrocytes to human bone marrow cells. Infect Immun. 2000;68:3455–62.PubMedPubMedCentralCrossRef
12.
go back to reference Neveu G, Dupuy F, Ladli M, Barbieri D, Naissant B, Richard C, et al. Plasmodium falciparum gametocyte-infected erythrocytes do not adhere to human primary erythroblasts. Sci Rep. 2018;8:17886.PubMedPubMedCentralCrossRef Neveu G, Dupuy F, Ladli M, Barbieri D, Naissant B, Richard C, et al. Plasmodium falciparum gametocyte-infected erythrocytes do not adhere to human primary erythroblasts. Sci Rep. 2018;8:17886.PubMedPubMedCentralCrossRef
14.
go back to reference Alano P. The emerging role of the human bone marrow as a privileged developmental niche for the transmission stages of the malaria parasite Plasmodium falciparum. Ann Ist Super Sanita. 2017;53:96–9.PubMed Alano P. The emerging role of the human bone marrow as a privileged developmental niche for the transmission stages of the malaria parasite Plasmodium falciparum. Ann Ist Super Sanita. 2017;53:96–9.PubMed
15.
go back to reference Messina V, Valtieri M, Rubio M, Falchi M, Mancini F, Mayor A, et al. Gametocytes of the malaria parasite Plasmodium falciparum interact with and stimulate bone marrow mesenchymal cells to secrete angiogenetic factors. Front Cell Infect Microbiol. 2018;8:50.PubMedPubMedCentralCrossRef Messina V, Valtieri M, Rubio M, Falchi M, Mancini F, Mayor A, et al. Gametocytes of the malaria parasite Plasmodium falciparum interact with and stimulate bone marrow mesenchymal cells to secrete angiogenetic factors. Front Cell Infect Microbiol. 2018;8:50.PubMedPubMedCentralCrossRef
17.
go back to reference Neveu G, Richard C, Dupuy F, Behera P, Volpe F, Subramani PA, et al. Plasmodium falciparum sexual parasites develop in human erythroblasts and affect erythropoiesis. Blood. 2020;136:1381–93.PubMedCrossRefPubMedCentral Neveu G, Richard C, Dupuy F, Behera P, Volpe F, Subramani PA, et al. Plasmodium falciparum sexual parasites develop in human erythroblasts and affect erythropoiesis. Blood. 2020;136:1381–93.PubMedCrossRefPubMedCentral
18.
go back to reference Smalley ME, Abdalla S, Brown J. The distribution of Plasmodium falciparum in the peripheral blood and bone marrow of Gambian children. Trans R Soc Trop Med Hyg. 1981;75:103–5.PubMedCrossRef Smalley ME, Abdalla S, Brown J. The distribution of Plasmodium falciparum in the peripheral blood and bone marrow of Gambian children. Trans R Soc Trop Med Hyg. 1981;75:103–5.PubMedCrossRef
19.
go back to reference Del Portillo HA, Ferrer M, Brugat T, Martin-Jaular L, Langhorne J, Lacerda MV. The role of the spleen in malaria. Cell Microbiol. 2012;14:343–55.PubMedCrossRef Del Portillo HA, Ferrer M, Brugat T, Martin-Jaular L, Langhorne J, Lacerda MV. The role of the spleen in malaria. Cell Microbiol. 2012;14:343–55.PubMedCrossRef
20.
go back to reference Buffet PA, Safeukui I, Deplaine G, Brousse V, Prendki V, Thellier M, et al. The pathogenesis of Plasmodium falciparum malaria in humans: insights from splenic physiology. Blood. 2011;117:381–92.PubMedPubMedCentralCrossRef Buffet PA, Safeukui I, Deplaine G, Brousse V, Prendki V, Thellier M, et al. The pathogenesis of Plasmodium falciparum malaria in humans: insights from splenic physiology. Blood. 2011;117:381–92.PubMedPubMedCentralCrossRef
22.
go back to reference Smith TG, Serghides L, Patel SN, Febbraio M, Silverstein RL, Kain KC. CD36-mediated nonopsonic phagocytosis of erythrocytes infected with stage I and IIA gametocytes of Plasmodium falciparum. Infect Immun. 2003;71:393–400.PubMedPubMedCentralCrossRef Smith TG, Serghides L, Patel SN, Febbraio M, Silverstein RL, Kain KC. CD36-mediated nonopsonic phagocytosis of erythrocytes infected with stage I and IIA gametocytes of Plasmodium falciparum. Infect Immun. 2003;71:393–400.PubMedPubMedCentralCrossRef
23.
go back to reference Bansal GP, Weinstein CS, Kumar N. Insight into phagocytosis of mature sexual (gametocyte) stages of Plasmodium falciparum using a human monocyte cell line. Acta Trop. 2016;157:96–101.PubMedPubMedCentralCrossRef Bansal GP, Weinstein CS, Kumar N. Insight into phagocytosis of mature sexual (gametocyte) stages of Plasmodium falciparum using a human monocyte cell line. Acta Trop. 2016;157:96–101.PubMedPubMedCentralCrossRef
24.
go back to reference Healer J, Graszynski A, Riley E. Phagocytosis does not play a major role in naturally acquired transmission-blocking immunity to Plasmodium falciparum malaria. Infect Immun. 1999;67:2334–9.PubMedPubMedCentralCrossRef Healer J, Graszynski A, Riley E. Phagocytosis does not play a major role in naturally acquired transmission-blocking immunity to Plasmodium falciparum malaria. Infect Immun. 1999;67:2334–9.PubMedPubMedCentralCrossRef
25.
26.
go back to reference Kalantari P, Deoliveira RB, Chan J, Corbett Y, Rathinam V, Stutz A, et al. Dual engagement of the NLRP3 and AIM2 inflammasomes by Plasmodium-derived hemozoin and DNA during malaria. Cell Rep. 2014;6:196–210.PubMedPubMedCentralCrossRef Kalantari P, Deoliveira RB, Chan J, Corbett Y, Rathinam V, Stutz A, et al. Dual engagement of the NLRP3 and AIM2 inflammasomes by Plasmodium-derived hemozoin and DNA during malaria. Cell Rep. 2014;6:196–210.PubMedPubMedCentralCrossRef
27.
go back to reference Hornung V, Bauernfeind F, Halle A, Samstad EO, Kono H, Rock KL, et al. Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat Immunol. 2008;9:847–56.PubMedPubMedCentralCrossRef Hornung V, Bauernfeind F, Halle A, Samstad EO, Kono H, Rock KL, et al. Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat Immunol. 2008;9:847–56.PubMedPubMedCentralCrossRef
28.
go back to reference Cevenini L, Camarda G, Michelini E, Siciliano G, Calabretta MM, Bona R, et al. Multicolor bioluminescence boosts malaria research: quantitative dual-color assay and single-cell imaging in Plasmodium falciparum parasites. Anal Chem. 2014;86:8814–21.PubMedPubMedCentralCrossRef Cevenini L, Camarda G, Michelini E, Siciliano G, Calabretta MM, Bona R, et al. Multicolor bioluminescence boosts malaria research: quantitative dual-color assay and single-cell imaging in Plasmodium falciparum parasites. Anal Chem. 2014;86:8814–21.PubMedPubMedCentralCrossRef
29.
go back to reference D’Alessandro S, Camarda G, Corbett Y, Siciliano G, Parapini S, Cevenini L, et al. A chemical susceptibility profile of the Plasmodium falciparum transmission stages by complementary cell-based gametocyte assays. J Antimicrob Chemother. 2016;71:1148–58.PubMedCrossRef D’Alessandro S, Camarda G, Corbett Y, Siciliano G, Parapini S, Cevenini L, et al. A chemical susceptibility profile of the Plasmodium falciparum transmission stages by complementary cell-based gametocyte assays. J Antimicrob Chemother. 2016;71:1148–58.PubMedCrossRef
30.
go back to reference D’Alessandro S, Silvestrini F, Dechering K, Corbett Y, Parapini S, Timmerman M, et al. A Plasmodium falciparum screening assay for anti-gametocyte drugs based on parasite lactate dehydrogenase detection. J Antimicrob Chemother. 2013;68:2048–58.PubMedCrossRef D’Alessandro S, Silvestrini F, Dechering K, Corbett Y, Parapini S, Timmerman M, et al. A Plasmodium falciparum screening assay for anti-gametocyte drugs based on parasite lactate dehydrogenase detection. J Antimicrob Chemother. 2013;68:2048–58.PubMedCrossRef
31.
go back to reference Corbett Y, D’Alessandro S, Parapini S, Scaccabarozzi D, Kalantari P, Zava S, et al. Interplay between Plasmodium falciparum haemozoin and L-arginine: implication for nitric oxide production. Malar J. 2018;17:456.PubMedPubMedCentralCrossRef Corbett Y, D’Alessandro S, Parapini S, Scaccabarozzi D, Kalantari P, Zava S, et al. Interplay between Plasmodium falciparum haemozoin and L-arginine: implication for nitric oxide production. Malar J. 2018;17:456.PubMedPubMedCentralCrossRef
32.
go back to reference Schwarzer E, Turrini F, Ulliers D, Giribaldi G, Ginsburg H, Arese P. Impairment of macrophage functions after ingestion of Plasmodium falciparum-infected erythrocytes or isolated malarial pigment. J Exp Med. 1992;176:1033–41.PubMedCrossRef Schwarzer E, Turrini F, Ulliers D, Giribaldi G, Ginsburg H, Arese P. Impairment of macrophage functions after ingestion of Plasmodium falciparum-infected erythrocytes or isolated malarial pigment. J Exp Med. 1992;176:1033–41.PubMedCrossRef
33.
go back to reference Prato M, D’Alessandro S, Van den Steen PE, Opdenakker G, Arese P, Taramelli D, et al. Natural haemozoin modulates matrix metalloproteinases and induces morphological changes in human microvascular endothelium. Cell Microbiol. 2011;13:1275–85.PubMedCrossRef Prato M, D’Alessandro S, Van den Steen PE, Opdenakker G, Arese P, Taramelli D, et al. Natural haemozoin modulates matrix metalloproteinases and induces morphological changes in human microvascular endothelium. Cell Microbiol. 2011;13:1275–85.PubMedCrossRef
34.
go back to reference Griess J. Bemerkungen zu der abhandlung der H.H. Weselsky und Benedikt “Ueber einige azoverbindungen.”. Chemische Berichte. 1879;12:426–8.CrossRef Griess J. Bemerkungen zu der abhandlung der H.H. Weselsky und Benedikt “Ueber einige azoverbindungen.”. Chemische Berichte. 1879;12:426–8.CrossRef
35.
go back to reference Elliott JA, Winn WC. Treatment of alveolar macrophages with cytochalasin D inhibits uptake and subsequent growth of Legionella pneumophila. Infect Immun. 1986;51:31–6.PubMedPubMedCentralCrossRef Elliott JA, Winn WC. Treatment of alveolar macrophages with cytochalasin D inhibits uptake and subsequent growth of Legionella pneumophila. Infect Immun. 1986;51:31–6.PubMedPubMedCentralCrossRef
36.
go back to reference Parroche P, Lauw FN, Goutagny N, Latz E, Monks BG, Visintin A, et al. Malaria hemozoin is immunologically inert but radically enhances innate responses by presenting malaria DNA to Toll-like receptor 9. Proc Natl Acad Sci USA. 2007;104:1919–24.PubMedCrossRefPubMedCentral Parroche P, Lauw FN, Goutagny N, Latz E, Monks BG, Visintin A, et al. Malaria hemozoin is immunologically inert but radically enhances innate responses by presenting malaria DNA to Toll-like receptor 9. Proc Natl Acad Sci USA. 2007;104:1919–24.PubMedCrossRefPubMedCentral
37.
go back to reference Corbett Y, Parapini S, D’Alessandro S, Scaccabarozzi D, Rocha BC, Egan TJ, et al. Involvement of Nod2 in the innate immune response elicited by malarial pigment hemozoin. Microbes Infect. 2015;17:184–94.PubMedCrossRef Corbett Y, Parapini S, D’Alessandro S, Scaccabarozzi D, Rocha BC, Egan TJ, et al. Involvement of Nod2 in the innate immune response elicited by malarial pigment hemozoin. Microbes Infect. 2015;17:184–94.PubMedCrossRef
38.
go back to reference Naotunne TS, Karunaweera ND, Mendis KN, Carter R. Cytokine-mediated inactivation of malarial gametocytes is dependent on the presence of white blood cells and involves reactive nitrogen intermediates. Immunology. 1993;78:555–62.PubMedPubMedCentral Naotunne TS, Karunaweera ND, Mendis KN, Carter R. Cytokine-mediated inactivation of malarial gametocytes is dependent on the presence of white blood cells and involves reactive nitrogen intermediates. Immunology. 1993;78:555–62.PubMedPubMedCentral
39.
go back to reference Long GH, Chan BH, Allen JE, Read AF, Graham AL. Blockade of TNF receptor 1 reduces disease severity but increases parasite transmission during Plasmodium chabaudi chabaudi infection. Int J Parasitol. 2008;38:1073–81.PubMedCrossRef Long GH, Chan BH, Allen JE, Read AF, Graham AL. Blockade of TNF receptor 1 reduces disease severity but increases parasite transmission during Plasmodium chabaudi chabaudi infection. Int J Parasitol. 2008;38:1073–81.PubMedCrossRef
40.
go back to reference Naotunne TS, Karunaweera ND, Del Giudice G, Kularatne MU, Grau GE, Carter R, et al. Cytokines kill malaria parasites during infection crisis: extracellular complementary factors are essential. J Exp Med. 1991;173:523–9.PubMedCrossRef Naotunne TS, Karunaweera ND, Del Giudice G, Kularatne MU, Grau GE, Carter R, et al. Cytokines kill malaria parasites during infection crisis: extracellular complementary factors are essential. J Exp Med. 1991;173:523–9.PubMedCrossRef
41.
go back to reference Stone WJ, Dantzler KW, Nilsson SK, Drakeley CJ, Marti M, Bousema T, et al. Naturally acquired immunity to sexual stage P. falciparum parasites. Parasitology. 2016;143:187–98.PubMedCrossRef Stone WJ, Dantzler KW, Nilsson SK, Drakeley CJ, Marti M, Bousema T, et al. Naturally acquired immunity to sexual stage P. falciparum parasites. Parasitology. 2016;143:187–98.PubMedCrossRef
42.
go back to reference Vermeulen AN, Ponnudurai T, Beckers PJ, Verhave J, Smith MA, Meuwissen JH. Sequential expression of antigens on sexual stages of Plasmodium falciparum accessible to transmission-blocking antibodies in the mosquito. J Exp Med. 1985;162:1460–76.PubMedCrossRef Vermeulen AN, Ponnudurai T, Beckers PJ, Verhave J, Smith MA, Meuwissen JH. Sequential expression of antigens on sexual stages of Plasmodium falciparum accessible to transmission-blocking antibodies in the mosquito. J Exp Med. 1985;162:1460–76.PubMedCrossRef
43.
go back to reference Contreras CE, Ploton IN, Siliciano RF, Karp CL, Viscidi R, Kumar N. Mapping of specific and promiscuous HLA-DR-restricted T-cell epitopes on the Plasmodium falciparum 27-kilodalton sexual stage-specific antigen. Infect Immun. 1998;66:3579–90.PubMedPubMedCentralCrossRef Contreras CE, Ploton IN, Siliciano RF, Karp CL, Viscidi R, Kumar N. Mapping of specific and promiscuous HLA-DR-restricted T-cell epitopes on the Plasmodium falciparum 27-kilodalton sexual stage-specific antigen. Infect Immun. 1998;66:3579–90.PubMedPubMedCentralCrossRef
44.
go back to reference Ascenzi P, Gradoni L. Nitric oxide limits parasite development in vectors and in invertebrate intermediate hosts. IUBMB Life. 2002;53:121–3.PubMedCrossRef Ascenzi P, Gradoni L. Nitric oxide limits parasite development in vectors and in invertebrate intermediate hosts. IUBMB Life. 2002;53:121–3.PubMedCrossRef
45.
go back to reference Chakravorty SJ, Carret C, Nash GB, Ivens A, Szestak T, Craig AG. Altered phenotype and gene transcription in endothelial cells, induced by Plasmodium falciparum-infected red blood cells: pathogenic or protective? Int J Parasitol. 2007;37:975–87.PubMedPubMedCentralCrossRef Chakravorty SJ, Carret C, Nash GB, Ivens A, Szestak T, Craig AG. Altered phenotype and gene transcription in endothelial cells, induced by Plasmodium falciparum-infected red blood cells: pathogenic or protective? Int J Parasitol. 2007;37:975–87.PubMedPubMedCentralCrossRef
46.
go back to reference Treeratanapiboon L, Psathaki K, Wegener J, Looareesuwan S, Galla HJ, Udomsangpetch R. In vitro study of malaria parasite induced disruption of blood-brain barrier. Biochem Biophys Res Commun. 2005;35:810–8.CrossRef Treeratanapiboon L, Psathaki K, Wegener J, Looareesuwan S, Galla HJ, Udomsangpetch R. In vitro study of malaria parasite induced disruption of blood-brain barrier. Biochem Biophys Res Commun. 2005;35:810–8.CrossRef
48.
go back to reference Turner GD, Morrison H, Jones M, Davis TM, Looareesuwan S, Buley ID, et al. 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. Am J Pathol. 1994;145:1057–69.PubMedPubMedCentral Turner GD, Morrison H, Jones M, Davis TM, Looareesuwan S, Buley ID, et al. 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. Am J Pathol. 1994;145:1057–69.PubMedPubMedCentral
49.
50.
go back to reference Matzer SP, Baumann T, Lukacs NW, Röllinghoff M, Beuscher HU. Constitutive expression of macrophage-inflammatory protein 2 (MIP-2) mRNA in bone marrow gives rise to peripheral neutrophils with preformed MIP-2 protein. J Immunol. 2001;167:4635–43.PubMedCrossRef Matzer SP, Baumann T, Lukacs NW, Röllinghoff M, Beuscher HU. Constitutive expression of macrophage-inflammatory protein 2 (MIP-2) mRNA in bone marrow gives rise to peripheral neutrophils with preformed MIP-2 protein. J Immunol. 2001;167:4635–43.PubMedCrossRef
51.
go back to reference Burdon PC, Martin C, Rankin SM. The CXC chemokine MIP-2 stimulates neutrophil mobilization from the rat bone marrow in a CD49d-dependent manner. Blood. 2005;105:2543–8.PubMedCrossRef Burdon PC, Martin C, Rankin SM. The CXC chemokine MIP-2 stimulates neutrophil mobilization from the rat bone marrow in a CD49d-dependent manner. Blood. 2005;105:2543–8.PubMedCrossRef
52.
53.
go back to reference Tahar R, Boudin C, Thiery I, Bourgouin C. Immune response of Anopheles gambiae to the early sporogonic stages of the human malaria parasite Plasmodium falciparum. EMBO J. 2002;21:6673–80.PubMedPubMedCentralCrossRef Tahar R, Boudin C, Thiery I, Bourgouin C. Immune response of Anopheles gambiae to the early sporogonic stages of the human malaria parasite Plasmodium falciparum. EMBO J. 2002;21:6673–80.PubMedPubMedCentralCrossRef
54.
go back to reference Ramdani G, Naissant B, Thompson E, Breil F, Lorthiois A, Dupuy F, et al. cAMP-signalling regulates gametocyte-infected erythrocyte deformability required for malaria parasite transmission. PLoS Pathog. 2015;11:e1004815.PubMedPubMedCentralCrossRef Ramdani G, Naissant B, Thompson E, Breil F, Lorthiois A, Dupuy F, et al. cAMP-signalling regulates gametocyte-infected erythrocyte deformability required for malaria parasite transmission. PLoS Pathog. 2015;11:e1004815.PubMedPubMedCentralCrossRef
56.
go back to reference Dietrich N, Rohde M, Geffers R, Kröger A, Hauser H, Weiss S, et al. Mast cells elicit proinflammatory but not type I interferon responses upon activation of TLRs by bacteria. Proc Natl Acad Sci USA. 2010;107:8748–53.PubMedCrossRefPubMedCentral Dietrich N, Rohde M, Geffers R, Kröger A, Hauser H, Weiss S, et al. Mast cells elicit proinflammatory but not type I interferon responses upon activation of TLRs by bacteria. Proc Natl Acad Sci USA. 2010;107:8748–53.PubMedCrossRefPubMedCentral
57.
go back to reference Kim MY, Kim JH, Cho JY. Cytochalasin B modulates macrophage-mediated inflammatory responses. Biomol Ther (Seoul). 2014;22:295–300.CrossRef Kim MY, Kim JH, Cho JY. Cytochalasin B modulates macrophage-mediated inflammatory responses. Biomol Ther (Seoul). 2014;22:295–300.CrossRef
Metadata
Title
Phagocytosis and activation of bone marrow‐derived macrophages by Plasmodium falciparum gametocytes
Authors
Yolanda Corbett
Silvia Parapini
Federica Perego
Valeria Messina
Serena Delbue
Paola Misiano
Mario Falchi
Francesco Silvestrini
Donatella Taramelli
Nicoletta Basilico
Sarah D’Alessandro
Publication date
01-12-2021
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2021
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-021-03589-2

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