Increased CD11b and Hypoxia-Inducible Factors-1alpha Expressions in the Lung Tissue and Surfactant Protein-D Levels in Serum Are Related with Acute Lung Injury in Severe Malaria of C57BL/6 Mice
Abstract
Background: We aimed to reveal the role of CD11b and hypoxia-inducible factors-1alpha (HIF-1α) expressions on monocytes and alveolar macrophages of lung tissue, and the levels of serum surfactant protein-D (SP-D) in severe malaria-associated acute lung injury (ALI).
Methods: The C57BL/6 mice were divided into control group, renal malaria group (inoculated with 106 Plasmodium berghei ANKA), and cerebral malaria group (inoculated with 107 P. berghei ANKA). The expressions of CD11b and HIF-1α in lung tissue were observed by immunohistochemistry, and serum SP-D levels were measured by ELISA. This study was conducted from June 2014 to February 2015 in the Laboratory of Parasitology, Faculty of Medicine, Universitas Brawijaya, Malang.
Results: The CD11b expression on pulmonary tissue of renal and cerebral malaria mice were significantly higher than control mice (P=0.002; P=0.002), as well as the HIF-1α expression on pulmonary tissue (P=0.002; P=0.002). The level of serum SP-D in renal malaria and cerebral malaria mice were significantly higher than control mice (P=0.002; P=0.002). We found a strong correlation between the expression of CD11b and HIF-1α in lung tissue (r=0.937, P=0.000), as well as between CD11b expression and serum SP-D levels (r=0.907, P=0.000) and between HIF-1α expression and serum SP-D levels (r=0.913, P=0.000).
Conclusion: Severe malaria-associated ALI increased the expression of CD11b and HIF-1α in the lung tissue and increased serum SP-D levels of C57BL/6 mice significantly.World Health Organization. Management of severe malaria: A practical handbook. Geneva: World Health Organization; 2012.
Cox-Singh J, Davis TME, Lee K-S, Shamsul SSG, Matusop A, Ratnam S, et al. Plasmodium knowlesi malaria in humans is widely distributed and potentially life-threatening. Clin Infect Dis. 2008; 46:165-71.
Andrade BB, Reis-Filho A, Souza-Neto SM, Clarêncio J, Camargo LMA, Barral A, et al. Severe Plasmodium vivax malaria exhibits marked inflammatory imbalance. Malar J. 2010; 9:13.
Mohan A, Sharma SK, Bollineni S. Acute lung injury and acute respiratory distress syndrome in malaria. J Vector Borne Dis. 2008; 45:179-93.
Taylor WR, Hanson J, Turner GD, White NJ, Dondorp AM. Respiratory manifestations of malaria. Chest. 2012; 142:492-505.
Van den Steen PE, Deroost K, Deckers J, Van Herck E, Struyf S, Opdenakker G. Pathogenesis of malaria-associated acute respiratory distress syndrome. Trends Parasitol. 2013; 29:346-58.
Sarkar S, Saha K, Das CS. Three cases of ARDS: An emerging complication of Plasmodium vivax malaria. Lung India. 2010; 27:154-7.
Chua CLL, Brown G, Hamilton JA, Rogerson S, Boeuf P. Monocytes and macrophages in malaria: protection or pathology? Trends Parasitol. 2013; 29:26-34.
Johnston LK, Rims CR, Gill SE, McGuire JK, Manicone AM. Pulmonary macrophage subpopulations in the induction and resolution of acute lung injury. Am J Respir Cell Mol Biol. 2012; 47:417-26.
Meerschaert J, Furie MB. The adhesion molecules used by monocytes for migration across endothelium include CD11a/CD18, CD11b/CD18, and VLA-4 on monocytes and ICAM-1, VCAM-1, and other ligands on endothelium. J Immunol. 1995; 154:4099-112.
Wang Y, Roller J, Menger MD, Thorlacius H. Sepsis-induced leukocyte adhesion in the pulmonary microvasculature in vivo is mediated by CD11a and CD11b. Eur J Pharmacol. 2013; 702:135-41.
Baer K, Klotz C, Kappe SHI, Schnieder T, Frevert U. Release of hepatic Plasmodium yoelii merozoites into the pulmonary microvasculature. PLoS Pathog. 2007; 3:e171.
Harris AJ, Thompson AAR, Whyte MKB, Walmsley SR. HIF-mediated innate immune responses: Cell signaling and therapeutic implications. Hypoxia. 2014; 2:47-58.
Anand RJ, Gribar SC, Li J, Kohler JW, Branca MF, Dubowski T, et al. Hypoxia causes an increase in phagocytosis by macrophages in a HIF-1α-dependent manner. J Leukoc Biol. 2007; 82:1257-65.
Becker PM, Alcasabas A, Yu AY, Semenza GL, Bunton TE. Oxygen-independent upregulation of vascular endothelial growth factor and vascular barrier dysfunction during ventilated pulmonary ischemia in isolated ferret lungs. Am J Respir Cell Mol Biol. 2000; 22:272-9.
Lee SH, Lee SH, Kim CH, Yang KS, Lee EJ, Min KH, et al. Increased expression of vascular endothelial growth factor and hypoxia inducible factor-1α in lung tissue of patients with chronic bronchitis. Clin Biochem. 2014; 47:552-9.
Epiphanio S, Campos MG, Pamplona A, Carapau D, Pena AC, Ataíde R, et al. VEGF promotes malaria-associated acute lung injury in mice. PLoS Pathog. 2010; 6:e1000916.
Senft AP, Korfhagen TR, Whitsett JA, LeVine AM. Surfactant protein D regulates the cell surface expression of alveolar macrophage β2-integrins. Am J Physiol Lung Cell Mol Physiol. 2007; 292:L469-L75.
McCormack FX, Whitsett JA. The pulmonary collectins, SP-A and SP-D, orchestrate innate immunity in the lung. J Clin Invest. 2002; 109:707-12.
Sakamoto K, Hashimoto N, Kondoh Y, Imaizumi K, Aoyama D, Kohnoh T, et al. Differential modulation of surfactant protein D under acute and persistent hypoxia in acute lung injury. Am J Physiol Lung Cell Mol Physiol. 2012; 303:L43-L53.
Eisner MD, Parsons P, Matthay MA, Ware L, Greene K. Acute Respiratory Distress Syndrome Network. Plasma surfactant protein levels and clinical outcomes in patients with acute lung injury. Thorax. 2003; 58:983-8.
Ware LB, Koyama T, Billheimer DD, Wu W, Bernard GR, Thompson BT, et al. Prognostic and pathogenetic value of combining clinical and biochemical indices in patients with acute lung injury. Chest. 2010; 137:288-96.
Pan T, Nielsen LD, Allen MJ, Shannon KM, Shannon JM, Selman M, et al. Serum SP-D is a marker of lung injury in rats. Am J Physiol Lung Cell Mol Physiol. 2002; 282:L824-L32.
Gaunsbaek MQ, Rasmussen KJ, Beers MF, Atochina-Vasserman EN, Hansen S. Lung surfactant protein D (SP-D) response and regulation during acute and chronic lung injury. Lung. 2013; 191:295-303.
Elias RM, Correa-Costa M, Barreto CR, Silva RC, Hayashida CY, Castoldi Â, et al. Oxidative stress and modification of renal vascular permeability are associated with acute kidney injury during P. berghei ANKA Infection. PLoS ONE. 2012; 7:e44004.
Abreu TP, Silva LSS, Takiya CM, Souza MC, Henriques MG, Pinheiro AAS, et al. Mice rescued from severe malaria are protected against renal injury during a second kidney insult. PLoS One. 2014; 9:e93634.
de Oca M, Engwerda C, Haque A. Plasmodium berghei ANKA (PbA) infection of C57BL/6J mice: a model of severe malaria. In: Allen IC, editor. Mouse Models of Innate Immunity. Humana Press; 2013.p.203-13.
Nguansangiam S, Day NPJ, Hien TT, Mai NTH, Chaisri U, Riganti M, et al. A quantitative ultrastructural study of renal pathology in fatal Plasmodium falciparum malaria. Trop Med Int Health. 2007; 12:1037-50.
Martins YC, Smith MJ, Pelajo-Machado M, Werneck GL, Lenzi HL, Daniel-Ribeiro CT, et al. Characterization of cerebral malaria in the outbred Swiss Webster mouse infected by Plasmodium berghei ANKA. Int J Exp Pathol. 2009; 90:119-30.
Matute-Bello G, Downey G, Moore BB, Groshong SD, Matthay MA, Slutsky AS, et al. An official american thoracic society workshop report: Features and measurements of experimental acute lung injury in animals. Am J Respir Cell Mol Biol. 2011; 44:725-38.
Souza MC, Silva JD, Pádua TA, Capelozzi VL, Rocco PRM, Henriques MdG. Early and late acute lung injury and their association with distal organ damage in murine malaria. Respir Physiol Neurobiol. 2013; 186:65-72.
Aitken EH, Negri EM, Barboza R, Lima MRI, Álvarez JM, Marinho CRF, et al. Ultrastructure of the lung in a murine model of malaria-associated acute lung injury/acute respiratory distress syndrome. Malar J. 2014; 13:230.
Deroost K, Tyberghein A, Lays N, Noppen S, Schwarzer E, Vanstreels E, et al. Hemozoin induces lung inflammation and correlates with malaria-associated acute respiratory distress syndrome. Am J Respir Cell Mol Biol. 2013; 48:589-600.
Gordon S, Taylor PR. Monocyte and macrophage heterogeneity. Nat Rev Immunol. 2005; 5:953-64.
Tacke F, Randolph GJ. Migratory fate and differentiation of blood monocyte subsets. Immunobiology. 2006; 211:609-18.
Lagasse HAD, Scott A. Lung macrophages control malaria-induced pulmonary inflammation [abstract]. J Immunol. 2011;186 Abstr Suppl:56.17.
Turner GD, Morisson H, Jones M, Davis TM, Looareesuwan S, Buley ID, et al. An immunohistochemical study of the pathology of fatal malaria. Am J Pathol. 1994; 145:1057–69.
McGilvray ID, Serghides L, Kapus A, Rotstein OD, Kain KC. Nonopsonic monocyte/macrophage phagocytosis of Plasmodium falciparum–parasitized erythrocytes: a role for CD36 in malarial clearance. Blood. 2000; 96:3231-40.
Shimoda LA, Semenza GL. HIF and the lung: Role of hypoxia-inducible factors in pulmonary development and disease. Am J Respir Crit Care Med. 2011; 183:152-6.
Hempel C, Hoyer N, Kildemoes A, Jendresen CB, Kurtzhals JAL. Systemic and cerebral vascular endothelial growth factor levels increase in murine cerebral malaria along with increased calpain and caspase activity and can be reduced by erythropoietin treatment. Front Immunol. 2014; 5:291.
Boeuf P, Tan A, Romagosa C, Radford J, Mwapasa V, Molyneux ME, et al. Placental hypoxia during placental malaria. J Infect Dis. 2008; 197:757-65.
Sørensen GL, Hjelmborg JvB, Kyvik KO, Fenger M, Høj A, Bendixen C, et al. Genetic and environmental influences of surfactant protein D serum levels. Am J Physiol Lung Cell Mol Physiol. 2006; 290:L1010-L7.
Winkler C, Atochina-Vasserman EN, Holz O, Beers MF, Erpenbeck VJ, Krug N, et al. Comprehensive characterisation of pulmonary and serum surfactant protein D in COPD. Respir Res. 2011; 12:29.
Husby S, Herskind AM, Jensenius JC, Holmskov U. Heritability estimates for the constitutional levels of the collectins mannan-binding lectin and lung surfactant protein D. A study of unselected like-sexed mono- and dizygotic twins at the age of 6–9 years. Immunology. 2002; 106:389-94.
Madsen J, Kliem A, Tornøe I, Skjødt K, Koch C, Holmskov U. Localization of lung surfactant protein D on mucosal surfaces in human tissues. J Immunol. 2000; 164:5866-70.
Akiyama J, Hoffman A, Brown C, Allen L, Edmondson J, Poulain F, et al. Tissue distribution of surfactant proteins A and D in the mouse. J Histochem Cytochem. 2002; 50:993-6.
Acosta-Iborra B, Elorza A, Olazabal IM, Martín-Cofreces NB, Martin-Puig S, Miró M, et al. Macrophage oxygen sensing modulates antigen presentation and phagocytic functions involving IFN-gamma production through the HIF-1 alpha transcription factor. J Immunol. 2009; 182:3155-64.
Kong T, Eltzschig HK, Karhausen J, Colgan SP, Shelley CS. Leukocyte adhesion during hypoxia is mediated by HIF-1-dependent induction of β(2) integrin gene expression. Proc Natl Acad Sci U S A. 2004; 101:10440-5.
Tan SM. The leucocyte beta2 (CD18) integrins: the structure, functional regulation and signalling properties. Biosci Rep. 2012; 32:241-69.
Strauss-Ayali D, Conrad SM, Mosser DM. Monocyte subpopulations and their differentiation patterns during infection. J Leukoc Biol. 2007; 82:244-52.
Bruick RK. Oxygen sensing in the hypoxic response pathway: Regulation of the hypoxia-inducible transcription factor. Genes Dev. 2003; 17:2614-23.
| Files | ||
| Issue | Vol 11 No 3 (2016) | |
| Section | Original Article(s) | |
| Keywords | ||
| Acute lung injury Severe malaria CD11b HIF-1alpha SP-D | ||
| Rights and permissions | |
|
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
