Parasites, Hosts and Diseases

  • 제57권2호
  • /
  • Pages.117-125
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  • 2019
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  • 2982-5164(pISSN)
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  • 1738-0006(eISSN)
The Korea Society for Parasitology and Tropical Medicine (대한기생충학·열대의학회)
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Induction of Angiogenesis by Malarial Infection through Hypoxia Dependent Manner

  • Park, Mi-Kyung (Department of Parasitology and Genetics, Kosin University College of Medicine) ;
  • Ko, Eun-Ji (Department of Parasitology and Genetics, Kosin University College of Medicine) ;
  • Jeon, Kyung-Yoon (Department of Parasitology and Genetics, Kosin University College of Medicine) ;
  • Kim, Hyunsu (Department of Parasitology and Genetics, Kosin University College of Medicine) ;
  • Jo, Jin-Ok (Department of Parasitology and Genetics, Kosin University College of Medicine) ;
  • Baek, Kyung-Wan (Department of Parasitology, College of Medicine, Pusan National University) ;
  • Kang, Yun-Jeong (Department of Parasitology and Genetics, Kosin University College of Medicine) ;
  • Choi, Yung Hyun (Anti-Aging Research Center and Department of Biochemistry, Dongeui University College of Korean Medicine) ;
  • Hong, Yeonchul (Department of Parasitology and Tropical Medicine, Kyungpook National University School of Medicine) ;
  • Ock, Mee Sun (Department of Parasitology and Genetics, Kosin University College of Medicine) ;
  • Cha, Hee-Jae (Department of Parasitology and Genetics, Kosin University College of Medicine)
  • 투고 : 2018.10.22
  • 심사 : 2019.03.14
  • 발행 : 2019.04.30
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초록

Malarial infection induces tissue hypoxia in the host through destruction of red blood cells. Tissue hypoxia in malarial infection may increase the activity of $HIF1{\alpha}$ through an intracellular oxygen-sensing pathway. Activation of $HIF1{\alpha}$ may also induce vascular endothelial growth factor (VEGF) to trigger angiogenesis. To investigate whether malarial infection actually generates hypoxia-induced angiogenesis, we analyzed severity of hypoxia, the expression of hypoxia-related angiogenic factors, and numbers of blood vessels in various tissues infected with Plasmodium berghei. Infection in mice was performed by intraperitoneal injection of $2{\times}10^6$ parasitized red blood cells. After infection, we studied parasitemia and survival. We analyzed hypoxia, numbers of blood vessels, and expression of hypoxia-related angiogenic factors including VEGF and $HIF1{\alpha}$. We used Western blot, immunofluorescence, and immunohistochemistry to analyze various tissues from Plasmodium berghei-infected mice. In malaria-infected mice, parasitemia was increased over the duration of infection and directly associated with mortality rate. Expression of VEGF and $HIF1{\alpha}$ increased with the parasitemia in various tissues. Additionally, numbers of blood vessels significantly increased in each tissue type of the malaria-infected group compared to the uninfected control group. These results suggest that malarial infection in mice activates hypoxiainduced angiogenesis by stimulation of $HIF1{\alpha}$ and VEGF in various tissues.

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참고문헌

  1. Ng S, March S, Galstian A, Hanson K, Carvalho T, Mota MM, Bhatia SN. Hypoxia promotes liver-stage malaria infection in primary human hepatocytes in vitro. Dis Model Mech 2014; 7: 215-224. https://doi.org/10.1242/dmm.013490
  2. Hansen DS. Inflammatory responses associated with the induction of cerebral malaria: lessons from experimental murine models. PLoS Pathog 2012; 8: e1003045. https://doi.org/10.1371/journal.ppat.1003045
  3. Engwerda CR, Beattie L, Amante FH. The importance of the spleen in malaria. Trends Parasitol 2005; 21: 75-80. https://doi.org/10.1016/j.pt.2004.11.008
  4. Deininger MH, Winkler S, Kremsner PG, Meyermann R, Schluesener HJ. Angiogenic proteins in brains of patients who died with cerebral malaria. J Neuroimmunol 2003; 142: 101-111. https://doi.org/10.1016/S0165-5728(03)00250-9
  5. Muehlenbachs A, Mutabingwa TK, Edmonds S, Fried M, Duffy PE. Hypertension and maternal-fetal conflict during placental malaria. PLoS Med 2006; 3: e446. https://doi.org/10.1371/journal.pmed.0030446
  6. de Souza JB, Riley EM. Cerebral malaria: the contribution of studies in animal models to our understanding of immunopathogenesis. Microbes Infect 2002; 4: 291-300. https://doi.org/10.1016/S1286-4579(02)01541-1
  7. Basir R, Rahiman SF, Hasballah K, Chong W, Talib H, Yam M, Jabbarzare M, Tie T, Othman F, Moklas M, Abdullah W, Ahmad Z. Plasmodium berghei ANKA Infection in ICR Mice as a Model of Cerebral Malaria. Iran J Parasitol 2012; 7: 62-74.
  8. Craig AG, Grau GE, Janse C, Kazura JW, Milner D, Barnwell JW, Turner G, Langhorne J; participants of the Hinxton Retreat meeting on Animal Models for Research on Severe Malaria. The role of animal models for research on severe malaria. PLoS Pathog 2012; 8: e1002401. https://doi.org/10.1371/journal.ppat.1002401
  9. Hall N, Karras M, Raine JD, Carlton JM, Kooij TW, Berriman M, Florens L, Janssen CS, Pain A, Christophides GK, James K, Rutherford K, Harris B, Harris D, Churcher C, Quail MA, Ormond D, Doggett J, Trueman HE, Mendoza J, Bidwell SL, Rajandream MA, Carucci DJ, Yates JR 3rd, Kafatos FC, Janse CJ, Barrell B, Turner CM, Waters AP, Sinden RE. A comprehensive survey of the Plasmodium life cycle by genomic, transcriptomic, and proteomic analyses. Science 2005; 307: 82-86. https://doi.org/10.1126/science.1103717
  10. Risau W. Mechanisms of angiogenesis. Nature 1997; 386: 671-674. https://doi.org/10.1038/386671a0
  11. Banai S, Shweiki D, Pinson A, Chandra M, Lazarovici G, Keshet E. Upregulation of vascular endothelial growth factor expression induced by myocardial ischaemia: implications for coronary angiogenesis. Cardiovasc Res 1994; 28: 1176-1179. https://doi.org/10.1093/cvr/28.8.1176
  12. Shweiki D, Itin A, Soffer D, Keshet E. Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature 1992; 359: 843-845. https://doi.org/10.1038/359843a0
  13. Ema M, Taya S, Yokotani N, Sogawa K, Matsuda Y, Fujii-Kuriyama Y. A novel bHLH-PAS factor with close sequence similarity to hypoxia-inducible factor 1alpha regulates the VEGF expression and is potentially involved in lung and vascular development. Proc Natl Acad Sci USA 1997; 94: 4273-4278. https://doi.org/10.1073/pnas.94.9.4273
  14. Hioki A, Yoshino M, Kano S, Ohtomo H. Pathophysiology of hypoxia in mice infected with Plasmodium berghei. Parasitol Res 1987; 73: 298-302. https://doi.org/10.1007/BF00531081
  15. Canavese M, Spaccapelo R. Protective or pathogenic effects of vascular endothelial growth factor (VEGF) as potential biomarker in cerebral malaria. Pathog Glob Health 2014; 108: 67-75. https://doi.org/10.1179/2047773214Y.0000000130
  16. Furuta T, Kimura M, Watanabe N. Elevated levels of vascular endothelial growth factor (VEGF) and soluble vascular endothelial growth factor receptor (VEGFR)-2 in human malaria. Am J Trop Med Hyg 2010; 82: 136-139. https://doi.org/10.4269/ajtmh.2010.09-0203
  17. Kang YJ, Jo JO, Cho MK, Yu HS, Cha HJ, Ock MS. Trichinella spiralis infection induces beta-actin co-localized with thymosin beta4. Vet Parasitol 2012; 187: 480-485. https://doi.org/10.1016/j.vetpar.2012.01.017
  18. Yun KY, Ko EJ, Kim HY, Lee JY, Eo WK, Ock MS, Kim HS, Kim KH, Cha HJ. Long interspersed element-1 open reading frame 1 protein expression profiles in ovarian cancers. Genes Genom 2017; 39: 1157-1162. https://doi.org/10.1007/s13258-017-0589-5
  19. Wang D, Stockard CR, Harkins L, Lott P, Salih C, Yuan K, Buchsbaum D, Hashim A, Zayzafoon M, Hardy RW, Hameed O, Grizzle W, Siegal GP. Immunohistochemistry in the evaluation of neovascularization in tumor xenografts. Biotech Histochem 2008; 83: 179-189. https://doi.org/10.1080/10520290802451085
  20. Elias RM, Correa-Costa M, Barreto CR, Silva RC, Hayashida CY, Castoldi A, Goncalves GM, Braga TT, Barboza R, Rios FJ, Keller AC, Cenedeze MA, Hyane MI, D'Imperio-Lima MR, Figueiredo-Neto AM, Reis MA, Marinho CR, Pacheco-Silva A, Camara NO. Oxidative stress and modification of renal vascular permeability are associated with acute kidney injury during P. berghei ANKA infection. PLoS One 2012; 7: e44004. https://doi.org/10.1371/journal.pone.0044004
  21. Boeuf P, Tan A, Romagosa C, Radford J, Mwapasa V, Molyneux ME, Meshnick SR, Hunt NH, Rogerson SJ. Placental hypoxia during placental malaria. J Infect Dis 2008; 197: 757-765. https://doi.org/10.1086/526521
  22. Ataide R, Murillo O, Dombrowski JG, Souza RM, Lima FA, Lima GF, Hristov AD, Valle SC, Di Santi SM, Epiphanio S, Marinho CR. Malaria in pregnancy interacts with and alters the angiogenic profiles of the placenta. PLoS Negl Trop Dis 2015; 9: e0003824. https://doi.org/10.1371/journal.pntd.0003824
  23. Yang Y, Liu Q, Lu J, Adah D, Yu S, Zhao S, Yao Y, Qin L, Qin L, Chen X. Exosomes from Plasmodium-infected hosts inhibit tumor angiogenesis in a murine Lewis lung cancer model. Oncogenesis 2017; 6: e351. https://doi.org/10.1038/oncsis.2017.52
  24. Chen L, He Z, Qin L, Li Q, Shi X, Zhao S, Chen L, Zhong N, Chen X. Antitumor effect of malaria parasite infection in a murine Lewis lung cancer model through induction of innate and adaptive immunity. PLoS One 2011; 6: e24407. https://doi.org/10.1371/journal.pone.0024407

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