Browse > Article
http://dx.doi.org/10.3347/kjp.2010.48.1.15

Possible Role of Heme Oxygenase-1 and Prostaglandins in the Pathogenesis of Cerebral Malaria: Heme Oxygenase-1 Induction by Prostaglandin $D_2$ and Metabolite by a Human Astrocyte Cell Line  

Kuesap, Jiraporn (Graduate Porgram in Biomedical Sciences, Clinical Coordination and Training Center, Thammasat University)
Na-Bangchang, Kesara (Graduate Porgram in Biomedical Sciences, Clinical Coordination and Training Center, Thammasat University)
Publication Information
Parasites, Hosts and Diseases / v.48, no.1, 2010 , pp. 15-21 More about this Journal
Abstract
Astrocytes are the most abundant cells in the central nervous system that play roles in maintaining the blood-brain-barrier and in neural injury, including cerebral malaria, a severe complication of Plasmodium falciparum infection. Prostaglandin (PG) $D_2$ is abundantly produced in the brain and regulates the sleep response. Moreover, $PGD_2$ is a potential factor derived from P. falciparum within erythrocytes. Heme oxygenase-1 (HO-1) is catalyzing enzyme in heme breakdown process to release iron, carbon monoxide, and biliverdin/bilirubin, and may influence iron supply to the P. falciparum parasites. Here, we showed that treatment of a human astrocyte cell line, CCF-STTG1, with $PGD_2$ significantly increased the expression levels of HO-1 mRNA by RT-PCR. Western blot analysis showed that $PGD_2$ treatment increased the level of HO-1 protein, in a dose- and time-dependent manner. Thus, $PGD_2$ may be involved in the pathogenesis of cerebral malaria by inducing HO-1 expression in malaria patients.
Keywords
Plasmodium falciparum; astrocyte; heme oxygenase; iron; cerebral malaria; prostaglandin $D_2$;
Citations & Related Records

Times Cited By Web Of Science : 1  (Related Records In Web of Science)
Times Cited By SCOPUS : 1
연도 인용수 순위
1 Murayama S, Inoue K, Kawakami H, Bouldin TW, Suzuki K. A unique pattern of astrocytosis in the primary motor area in amyotrophic lateral sclerosis. Acta Neuropathol 1991; 82: 456-461.   DOI   ScienceOn
2 Sisodiya SM, Martinian L, Scheffer GL, van der Valk P, Scheper RJ, Harding BN, Thom M. Vascular colocalization of P-glycoprotein, multidrug-resistance associated protein 1, breast cancer resistance protein and major vault protein in human epileptogenic pathologies. Neuropathol Appl Neurobiol 2006; 32: 51-63.   DOI   ScienceOn
3 Hirai H, Tanaka K, Yoshie O, Ogawa K, Kenmotsu K, Takamori Y, Ichimasa M, Sugamura K, Nakamura M, Takano S, Nagata K. Prostaglandin D2 selectively induces chemotaxis in T helper type 2 cells, eosinophils, and basophils via seven-transmembrane receptor CRTH2. J Exp Med 2001; 193: 255-261.   DOI   ScienceOn
4 Kuesap J, Li B, Satarug S, Takeda K, Numata I, Na-Bangchang K, Shibahara S. Prostaglandin D2 induces heme oxygenase-1 in human retinal pigment epithelial cells. Biochem Biophys Res Commun 2008; 367: 413-419.   DOI   ScienceOn
5 Qin S, McLaughlin AP, De Vries GW. Protection of RPE cells from oxidative injury by 15-deoxy-delta12,14-prostaglandin J2 by augmenting GSH and activating MAPK. Invest Ophthalmol Vis Sci 2006; 47: 5098-5105.   DOI   ScienceOn
6 Abbott NJ. Astrocyte-endothelial interactions and blood-brain barrier permeability. J Anat 2002; 200: 629-638.   DOI   ScienceOn
7 Tontsch U, Bauer HC. Glial cells and neurons induce blood-brain barrier related enzymes in cultured cerebral endothelial cells.Brain Res 1991; 539: 247-253.   DOI   ScienceOn
8 Sperri PE, Grant MB, Gomez J, Vernadakis A. Endothelial cell conditioned media mediated regulation of glutamine synthase activity in glial cells. Dev Brain Res 1997; 104: 205-208.   DOI   ScienceOn
9 Kimpara T, Takeda A, Watanabe K, Itoyama Y, Ikawa S, Watanabe M, Arai H, Sasaki H, Higuchi S, Okita N, Takase S, Saito H, Takahashi K, Shibahara S. Microsatellite polymorphism in the human heme oxygenase-1 gene promoter and its application in association studies with Alzheimer and Parkinson disease. Hum Genet 1997; 100: 145-147.   DOI   ScienceOn
10 Urade Y, Hayaishi O. Biochemical, structural, genetic, physiological, and pathophysiological features of lipocalin-type prostaglandin D synthase. Biochim Biophys Acta 2000; 1482: 259-271.   DOI   ScienceOn
11 Giao PT, de Vries PJ. Pharmacokinetic interactions of antimalarial agents. Clin Pharmacokinet 2001; 40: 343-373.   DOI   ScienceOn
12 Neuhaus J, Risau W, Wolburg H. Induction of blood-brain barrier characteristics in bovine brain endothelial cells by rat astroglial cells in transfilter coculture. Ann N Y Acad Sci 1991; 633: 578-580.   DOI   ScienceOn
13 Na-bangchang K, Congpoung K. Current malaria status and distribution of drug resistance in East and Southeast Asia with special focus to Thailand. Tohoku J Exp Med 2007; 211: 99-113.   DOI   ScienceOn
14 Mattson MP, Chan SL. Neuronal and glial calcium signaling in Alzheimer's disease. Cell Calcium 2003; 34: 385-397.   DOI   ScienceOn
15 Ballabh P, Braun A, Nedergaard M. The blood-brain barrier: an overview: structure, regulation, and clinical implications. Neurobiol Dis 2004; 16: 1-13.   DOI   ScienceOn
16 Maxwell K, Berliner JA, Cancilla PA. Induction of gamma-glutamyl transpeptidase in cultured cerebral endothelial cells by a product released by astrocytes. Brain Res 1987; 410: 309-314.   DOI   ScienceOn
17 Chen Y, Swanson RA. Astrocytes and brain injury. J Cereb Blood Flow Metab 2003; 23: 137-149.   DOI
18 Diedrich JF, Minnigan H, Carp RI, Whitaker JN, Race R, Frey W-2nd, Haase AT. Neuropathological changes in scrapie and Alzheimer's disease are associated with increased expression of apolipoprotein E and cathepsin D in astrocytes. J Virol 1991; 65: 4759-4768.
19 Aarnoudse AL, van Schaik RH, Dieleman J, Molokhia M, van Riemsdijk MM, Ligthelm RJ, Overbosch D, van der Heiden IP, Stricker BH. MDR1 gene polymorphisms are associated with neuropsychiatric adverse effects of mefloquine. Clin Pharmacol Ther 2006; 80: 367-374.   DOI   ScienceOn
20 Combes V, Coltel N, Faille D, Wassmer SC, Grau GE. Cerebral malaria: role of microparticles and platelets in alterations of the blood-brain barrier. Int J Parasitol 2006; 36: 541-546.   DOI   ScienceOn
21 Hoffman SL. Artemether in severe malaria-still too many deaths. N Engl J Med 1996; 335: 124-126.   DOI   ScienceOn
22 Phillips-Howard PA, ter Kuile FO. CNS adverse events associated with antimalarial agents: fact or fiction? Drug Safety 1995; 12: 370-383.   DOI   ScienceOn
23 Loscher W, Potschka H. Blood-brain barrier active efflux transporters: ATP-binding cassette gene family. NeuroRx 2005; 2: 86-98.   DOI   ScienceOn
24 Barraud LS, Fernandez C, German FM, Gantier JC, Gimenez F, Farinotti R. MDR1A (ABCB1) deficient CF-1 mutant mice is susceptible to cerebral malaria induced by Plasmodium berghei anka. J Parasitol 2008; 11: 1.
25 White NJ, Looareesuwan S, Warrell DA, Warrell MJ, Bunnag D, Harinasuta T. Quinine pharmacokinetics and toxicity in cerebral and uncomplicated falciparum malaria. Am J Med 1982; 73: 564-572.   DOI   ScienceOn
26 Brewer TG, Genovese RF, Newman DB, Li Q. Factors relating to neurotoxicity of artemisinin antimalarial drugs "listening to artemether". Med Trop 1998; 58: 22-27.
27 Miller LG, Panosian CB. Ataxia and slurred speech after artesunate treatment for falciparum malaria. N Engl J Med 1997; 336: 1328   DOI   ScienceOn
28 Wesche DL, Da Coster MA, Tortella FC, Brewer TG. Neurotoxicity of artemisinin analogs in vitro. Antimicrob Agents Chemother 1994; 38: 1813-1819.   DOI   ScienceOn
29 Karbwang J, Tin T, Rimchala W, Sukontason K, Namsiripongpun V, Thanavibul A, Na-Bangchang K, Laothavorn P, Bunnag D, Harinasuta T. Comparison of artemether and quinine in the treatment of severe falciparum malaria in south-east Thailand. Trans R Soc Trop Med Hyg 1995; 89: 668-671.   DOI   ScienceOn
30 Kacem K, Lacombe P, Seylaz J, Bonvento G. Structural organization of the perivascular astrocyte endfeet and their relationship with the endothelial glucose transporter: a confocal microscopy study. Glia 1998; 23: 1-10.   DOI   ScienceOn
31 Debault LE, Cancilla PA. Glutamyl transpeptidase in isolated brain endothelial cells: induction by glial cells in vitro. Science 1979; 207: 653-655.
32 Harry GJ, Billingsley M, Bruinink A, Campbell IL, Classen W, Dorman DC, Galli C, Ray D, Smith RA, Tilson HA. In vitro techniques for the assessment of neurotoxicity. Environ Health Perspect 1998; 106: 131-158.   DOI
33 Viviani B, Corsini E, Galli CL, Padovani A, Ciusani E, Marinovich M. Dying neural cells activate glia through the release of a protease product. Glia 2000; 32: 84-90.   DOI   ScienceOn
34 Lanz R, Polster P, Brune K. Antipyretic analgesics inhibit prostaglandin release from astrocytes and macrophages similarly. Eur J Pharmacol 1986; 130: 105-109.   DOI   ScienceOn
35 Arcari P, Martinelli R, Salvatore F. The complete sequence of a full length cDNA for human liver glyceraldehyde-3-phosphate dehydrogenase: evidence for multiple mRNA species. Nucleic Acids Res 1984; 12: 9179-9189.   DOI   ScienceOn
36 Tzeng S F, Hsiao HY, Mak OT. Prostaglandins and cyclooxygenases in glial cells during brain inflammation. Curr Drug Targets Inflamm 2005; 4: 335-340.   DOI   ScienceOn
37 Estrada C, Bready JV, Berliner JA, Pardridge WM, Cancilla PA. Astrocyte growth stimulation by a soluble factor produced by cerebral endothelial cells in vitro. J Neuropathol Exp Neurol 1990; 49: 539-549.   DOI
38 McCoubrey Jr WK, Ewing JF, Maines MD. Human heme oxygenase-2: characterization and expression of a full-length cDNA and evidence suggesting that the two HO-2 transcripts may differ by choice of polyadenylation signal. Arch Biochem Biophys 1992; 295: 13-20.   DOI   ScienceOn
39 Alvarez-Maqueda M, El Bekay R, Alba G, Monteseirin J, Chacon P, Vega A, Martin-Nieto J, Bedoya FJ, Pintado E, Sobrino F. 15-deoxy-delta 12,14-prostaglandin J2 induces heme oxygenase-1 gene expression in a reactive oxygen species-dependent manner in human lymphocytes. J Biol Chem 2004; 279: 21929-21937.   DOI   ScienceOn
40 Obata T, Nakano Y, Looareesuwan S, Ohtomo H, Aikawa M. Prostaglandin spectrum in falciparum malaria patients. International Congress Series 2002; 1233: 475-478.   DOI   ScienceOn
41 Beare NA, Taylor TE, Harding SP, Lewallen S, Molyneux ME. Malarial retinopathy: a newly established diagnostic sign in severe malaria. Am J Trop Med Hyg 2006; 75: 790-797.
42 Kubata BK, Eguchi N, Urade Y, Yamashita K, Mitamura T, Tai K, Hayaishi O, Horii T. Plasmodium falciparum produces prostaglandins that are pyrogenic, somnogenic, and immunosuppressive substances in humans. J Exp Med 1998; 188: 1197-1202.   DOI   ScienceOn
43 Yoshida T, Biro P, Cohen T, Muller RM, Shibahara S. Human heme oxygenase cDNA and induction of its mRNA by hemin. Eur J Biochem 1988; 171: 457-461.   DOI   ScienceOn
44 Boie Y, Sawyer N, Slipetz DM, Metters KM, Abramovitz M. Molecular cloning and characterization of the human prostanoid DP receptor. J Biol Chem 1995; 270: 18910-18916.   DOI   ScienceOn
45 Pettipher R, Hansel TT, Armer, R. Antagonism of the prostaglandin D2 receptors DP1 and CRTH2 as an approach to treat allergic diseases. Nat Rev Drug Discov 2007; 6: 313-325.   DOI   ScienceOn
46 Eguchi N, Minami T, Shirafuji N, Kanaoka Y, Tanaka T, Nagata A, Yoshida N, Urade Y, Ito S, Hayashi O. Lack of tactile pain (allodynia) in lipocalin-type prostaglandin D synthase-deficient mice. Proc Natl Acad Sci USA 1999; 96: 726-730.   DOI   ScienceOn
47 Urade Y, Fujimoto N, Hayaishi O. Purification and characterization of rat brain prostaglandin synthetase. J Biol Chem 1985; 260: 12410-12415.
48 Yamada N, Yamaya M, Okinaga S, Nakayama K, Sekizawa K, Shibahara S, Sasaki H. Microsatellite polymorphism in the heme oxygenase-1 gene promoter is associated with susceptibility to emphysema. Am J Hum Genet 2000; 66: 187-195.   DOI   ScienceOn
49 Takeda M, Kikuchi M, Ubalee R, Na-Bangchang K, Ruangweerayut R, Shibahara S, Imai S, Hirayama K. Microsatellite polymorphism in the heme oxygenease-1 gene promoter is associated with susceptibility to cerebral malaria in Myanmar. Jpn J Infect Dis 2005; 58: 268-271.
50 Zhuang H, Pin S, Li X, Dore' S. Regulation of heme oxygenase expression by cyclopentenone prostaglandins. Exp Biol Med 2003; 228: 499-505.   DOI
51 Ma N, Madigan MC, Chan-Ling T, Hunt NH. Compromised blood-nerve barrier, astrogliosis, and myelin disruption in optic nerves during fatal murine cerebral malaria. Glia 1997; 19: 135-151.   DOI   ScienceOn
52 Blanco YC, Farias AS, Goelnitz U, Lopes SC, Arrais-Silva WW, Carvalho BO, Amino R, Wunderlich G, Santos LM, Giorgio S, Costa FT. Hyperbaric oxygen prevents early death caused by experimental cerebral malaria. PLoS ONE 2008; 3: e3126.   DOI   ScienceOn
53 Brown H, Hien TT, Day N, Mai NT, Chuong LV, Chau TT, Loc PP, Phu NH, Bethell D, Farrar J, Gatter K, White N, Turner G. Evidence of blood-brain barrier dysfunction in human cerebral malaria. Neuropathol Appl Neurobiol 1999; 25: 331-40.   DOI
54 Brown HC, Chau TT, Mai NT, Day NP, Sinh DX, White NJ, Hien TT, Farrar J, Turner GD. Blood-brain barrier function in cerebral malaria and CNS infections in Vietnam. Neurology 2000; 55:104-111.   DOI   ScienceOn
55 Shibahara S, Kitamuro T, Takahashi K. Heme degradation and human disease: diversity is the soul of life. Antioxid Redox Signal 2002; 4: 593-602.   DOI   ScienceOn
56 Schluesener HJ, Kremsner PG, Meyermann R. Heme oxygenase-1 in lesions of human cerebral malaria. Acta Neuropathol 2001; 101: 65-68.
57 Shibahara S. The heme oxygenase dilemma in cellular homeostasis: new insights for the feedback regulation of heme catabolism. Tohoku J Exp Med 2003; 200: 167-186.   DOI   ScienceOn
58 Shibahara S, Han F, Li B, Takeda K. Hypoxia and heme oxygenases: Oxygen sensing and regulation of expression. Antiox Redox Signal 2007; 9: 2209-2225.   DOI
59 Furuyama K, Kaneko K, Vargas PD. Heme as a magnificent molecule with multiple missions: heme determines its own fate and governs cellular homeostasis. Tohoku J Exp Med 2007; 213: 1-16.   DOI   ScienceOn
60 Hayashi Y, Nomura M, Yamagishi S, Harada S, Yamashita J, Yamamoto H. Induction of various blood-brain barrier properties in non-neural endothelial cells by close apposition to co-cultured astrocytes. Glia 1997; 19: 13-26.   DOI   ScienceOn
61 Sobue K, Yamamoto N, Yoneda K, Hodgson ME, Yamashiro K, Tsuruoka N, Tsuda T, Katsuya H, Miura Y, Asai K, Kato T. Induction of blood-brain barrier properties in immortalized bovine brain endothelial cells by astrocytic factors. Neurosci Res 1999;35: 155-164.   DOI   ScienceOn
62 Aloisi F, Borsellino G, Care A, Testa U, Gallo P, Russo G, Peschle C, Levi G. Cytokine regulation of astrocyte function: in-vitro studies using cells from the human brain. Int J Dev Neurosci 1995; 13: 265-274.   DOI   ScienceOn
63 Janzer RC, Raff MC. Astrocytes induce blood-brain barrier properties in endothelial cells. Nature 1987; 325: 253-257.   DOI   ScienceOn
64 Clark IA, Ilschner S, MacMicking JD, Cowden WB. TNF and Plasmodium berghei ANKA-induced cerebral malaria. Immunol Lett 1990; 25: 195-198.   DOI   ScienceOn