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Published in: Malaria Journal 1/2012

Open Access 01-12-2012 | Research

Allicin enhances host pro-inflammatory immune responses and protects against acute murine malaria infection

Authors: Yonghui Feng, Xiaotong Zhu, Qinghui Wang, Yongjun Jiang, Hong Shang, Liwang Cui, Yaming Cao

Published in: Malaria Journal | Issue 1/2012

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Abstract

Background

During malaria infection, multiple pro-inflammatory mediators including IFN-γ, TNF and nitric oxide (NO) play a crucial role in the protection against the parasites. Modulation of host immunity is an important strategy to improve the outcome of malaria infection. Allicin is the major biologically active component of garlic and shows anti-microbial activity. Allicin is also active against protozoan parasites including Plasmodium, which is thought to be mediated by inhibiting cysteine proteases. In this study, the immunomodulatory activities of allicin were assessed during acute malaria infection using a rodent malaria model Plasmodium yoelii 17XL.

Methods

To determine whether allicin modulates host immune responses against malaria infection, mice were treated with allicin after infection with P. yoelii 17XL. Mortality was checked daily and parasitaemia was determined every other day. Pro-inflammatory mediators and IL-4 were quantified by ELISA, while NO level was determined by the Griess method. The populations of dendritic cells (DCs), macrophages, CD4+ T and regulatory T cells (Treg) were assessed by FACS.

Results

Allicin reduced parasitaemia and prolonged survival of the host in a dose-dependent manner. This effect is at least partially due to improved host immune responses. Results showed that allicin treatment enhanced the production of pro-inflammatory mediators such as IFN-γ, TNF, IL-12p70 and NO. The absolute numbers of CD4+ T cells, DCs and macrophages were significantly higher in allicin-treated mice. In addition, allicin promoted the maturation of CD11c+ DCs, whereas it did not cause major changes in IL-4 and the level of anti-inflammatory cytokine IL-10.

Conclusions

Allicin could partially protect host against P. yoelii 17XL through enhancement of the host innate and adaptive immune responses.
Appendix
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Literature
1.
go back to reference WHO: World Malaria Report 2009. 2010, Geneva: World Health Organization WHO: World Malaria Report 2009. 2010, Geneva: World Health Organization
2.
go back to reference Wykes MN, Good MF: What have we learnt from mouse models for the study of malaria?. Eur J Immunol. 2009, 39: 2004-2007. 10.1002/eji.200939552.CrossRefPubMed Wykes MN, Good MF: What have we learnt from mouse models for the study of malaria?. Eur J Immunol. 2009, 39: 2004-2007. 10.1002/eji.200939552.CrossRefPubMed
3.
go back to reference Stevenson MM, Riley EM: Innate immunity to malaria. Nat Rev Immunol. 2004, 4: 169-180. 10.1038/nri1311.CrossRefPubMed Stevenson MM, Riley EM: Innate immunity to malaria. Nat Rev Immunol. 2004, 4: 169-180. 10.1038/nri1311.CrossRefPubMed
4.
go back to reference Schofield L, Grau GE: Immunological processes in malaria pathogenesis. Nat Rev Immunol. 2005, 5: 722-735. 10.1038/nri1686.CrossRefPubMed Schofield L, Grau GE: Immunological processes in malaria pathogenesis. Nat Rev Immunol. 2005, 5: 722-735. 10.1038/nri1686.CrossRefPubMed
5.
go back to reference Urban BC, Ing R, Stevenson MM: Early interactions between blood-stage Plasmodium parasites and the immune system. Curr Top Microbiol Immunol. 2005, 297: 25-70. 10.1007/3-540-29967-X_2.PubMed Urban BC, Ing R, Stevenson MM: Early interactions between blood-stage Plasmodium parasites and the immune system. Curr Top Microbiol Immunol. 2005, 297: 25-70. 10.1007/3-540-29967-X_2.PubMed
6.
go back to reference Amante FH, Good MF: Prolonged Th1-like response generated by a Plasmodium yoelii-specific T cell clone allows complete clearance of infection in reconstituted mice. Parasite Immunol. 1997, 19: 111-126. 10.1046/j.1365-3024.1997.d01-187.x.CrossRefPubMed Amante FH, Good MF: Prolonged Th1-like response generated by a Plasmodium yoelii-specific T cell clone allows complete clearance of infection in reconstituted mice. Parasite Immunol. 1997, 19: 111-126. 10.1046/j.1365-3024.1997.d01-187.x.CrossRefPubMed
7.
go back to reference Wang R, Charoenvit Y, Corradin G, De La Vega P, Franke ED, Hoffman SL: Protection against malaria by Plasmodium yoelii sporozoite surface protein 2 linear peptide induction of CD4+ T cell- and IFN-gamma-dependent elimination of infected hepatocytes. J Immunol. 1996, 157: 4061-4067.PubMed Wang R, Charoenvit Y, Corradin G, De La Vega P, Franke ED, Hoffman SL: Protection against malaria by Plasmodium yoelii sporozoite surface protein 2 linear peptide induction of CD4+ T cell- and IFN-gamma-dependent elimination of infected hepatocytes. J Immunol. 1996, 157: 4061-4067.PubMed
8.
go back to reference Awasthi A, Kumar A, Upadhyay SN, Yamada T, Matsunaga Y: Nitric oxide protects against chloroquine resistant Plasmodium yoeliinigeriensis parasites in vitro. Exp Parasitol. 2003, 105: 184-191. 10.1016/j.exppara.2003.12.008.CrossRefPubMed Awasthi A, Kumar A, Upadhyay SN, Yamada T, Matsunaga Y: Nitric oxide protects against chloroquine resistant Plasmodium yoeliinigeriensis parasites in vitro. Exp Parasitol. 2003, 105: 184-191. 10.1016/j.exppara.2003.12.008.CrossRefPubMed
9.
go back to reference Couper KN, Blount DG, Hafalla JC, van Rooijen N, de Souza JB, Riley EM: Macrophage-mediated but gamma interferon-independent innate immune responses control the primary wave of Plasmodium yoelii parasitemia. Infect Immun. 2007, 75: 5806-5818. 10.1128/IAI.01005-07.PubMedCentralCrossRefPubMed Couper KN, Blount DG, Hafalla JC, van Rooijen N, de Souza JB, Riley EM: Macrophage-mediated but gamma interferon-independent innate immune responses control the primary wave of Plasmodium yoelii parasitemia. Infect Immun. 2007, 75: 5806-5818. 10.1128/IAI.01005-07.PubMedCentralCrossRefPubMed
10.
go back to reference Cambos M, Belanger B, Jacques A, Roulet A, Scorza T: Natural regulatory (CD4 + CD25 + FOXP3+) T cells control the production of pro-inflammatory cytokines during Plasmodium chabaudi adami infection and do not contribute to immune evasion. Int J Parasitol. 2008, 38: 229-238. 10.1016/j.ijpara.2007.07.006.CrossRefPubMed Cambos M, Belanger B, Jacques A, Roulet A, Scorza T: Natural regulatory (CD4 + CD25 + FOXP3+) T cells control the production of pro-inflammatory cytokines during Plasmodium chabaudi adami infection and do not contribute to immune evasion. Int J Parasitol. 2008, 38: 229-238. 10.1016/j.ijpara.2007.07.006.CrossRefPubMed
11.
go back to reference Wu Y, Wang QH, Zheng L, Feng H, Liu J, Ma SH, Cao YM: Plasmodium yoelii: distinct CD4(+)CD25(+) regulatory T cell responses during the early stages of infection in susceptible and resistant mice. Exp Parasitol. 2007, 115: 301-304. 10.1016/j.exppara.2006.09.015.CrossRefPubMed Wu Y, Wang QH, Zheng L, Feng H, Liu J, Ma SH, Cao YM: Plasmodium yoelii: distinct CD4(+)CD25(+) regulatory T cell responses during the early stages of infection in susceptible and resistant mice. Exp Parasitol. 2007, 115: 301-304. 10.1016/j.exppara.2006.09.015.CrossRefPubMed
12.
go back to reference Bueno LL, Morais CG, Araujo FF, Gomes JA, Correa-Oliveira R, Soares IS, Lacerda MV, Fujiwara RT, Braga EM: Plasmodium vivax: induction of CD4 + CD25 + FoxP3+ regulatory T cells during infection are directly associated with level of circulating parasites. PLoS One. 2010, 5: e9623-10.1371/journal.pone.0009623.PubMedCentralCrossRefPubMed Bueno LL, Morais CG, Araujo FF, Gomes JA, Correa-Oliveira R, Soares IS, Lacerda MV, Fujiwara RT, Braga EM: Plasmodium vivax: induction of CD4 + CD25 + FoxP3+ regulatory T cells during infection are directly associated with level of circulating parasites. PLoS One. 2010, 5: e9623-10.1371/journal.pone.0009623.PubMedCentralCrossRefPubMed
13.
go back to reference Steinman RM, Hemmi H: Dendritic cells: translating innate to adaptive immunity. Curr Top Microbiol Immunol. 2006, 311: 17-58. 10.1007/3-540-32636-7_2.PubMed Steinman RM, Hemmi H: Dendritic cells: translating innate to adaptive immunity. Curr Top Microbiol Immunol. 2006, 311: 17-58. 10.1007/3-540-32636-7_2.PubMed
14.
15.
go back to reference Butt MS, Sultan MT, Butt MS, Iqbal J: Garlic: nature's protection against physiological threats. Crit Rev Food Sci Nutr. 2009, 49: 538-551. 10.1080/10408390802145344.CrossRefPubMed Butt MS, Sultan MT, Butt MS, Iqbal J: Garlic: nature's protection against physiological threats. Crit Rev Food Sci Nutr. 2009, 49: 538-551. 10.1080/10408390802145344.CrossRefPubMed
16.
go back to reference Goncagul G, Ayaz E: Antimicrobial effect of garlic (Allium sativum). Recent Pat Antiinfect Drug Discov. 2010, 5: 91-93. 10.2174/157489110790112536.CrossRefPubMed Goncagul G, Ayaz E: Antimicrobial effect of garlic (Allium sativum). Recent Pat Antiinfect Drug Discov. 2010, 5: 91-93. 10.2174/157489110790112536.CrossRefPubMed
17.
go back to reference Ankri S, Mirelman D: Antimicrobial properties of allicin from garlic. Microbes Infect. 1999, 1: 125-129. 10.1016/S1286-4579(99)80003-3.CrossRefPubMed Ankri S, Mirelman D: Antimicrobial properties of allicin from garlic. Microbes Infect. 1999, 1: 125-129. 10.1016/S1286-4579(99)80003-3.CrossRefPubMed
18.
go back to reference Ramoutar RR, Brumaghim JL: Antioxidant and anticancer properties and mechanisms of inorganic selenium, oxo-sulfur, and oxo-selenium compounds. Cell Biochem Biophys. 2010, 58: 1-23. 10.1007/s12013-010-9088-x.CrossRefPubMed Ramoutar RR, Brumaghim JL: Antioxidant and anticancer properties and mechanisms of inorganic selenium, oxo-sulfur, and oxo-selenium compounds. Cell Biochem Biophys. 2010, 58: 1-23. 10.1007/s12013-010-9088-x.CrossRefPubMed
19.
go back to reference Sun X, Ku DD: Allicin in garlic protects against coronary endothelial dysfunction and right heart hypertrophy in pulmonary hypertensive rats. Am J Physiol Heart Circ Physiol. 2006, 291: H2431-H2438. 10.1152/ajpheart.00384.2006.CrossRefPubMed Sun X, Ku DD: Allicin in garlic protects against coronary endothelial dysfunction and right heart hypertrophy in pulmonary hypertensive rats. Am J Physiol Heart Circ Physiol. 2006, 291: H2431-H2438. 10.1152/ajpheart.00384.2006.CrossRefPubMed
20.
go back to reference Antony ML, Singh SV: Molecular mechanisms and targets of cancer chemoprevention by garlic-derived bioactive compound diallyl trisulfide. Indian J Exp Biol. 2011, 49: 805-816.PubMedCentralPubMed Antony ML, Singh SV: Molecular mechanisms and targets of cancer chemoprevention by garlic-derived bioactive compound diallyl trisulfide. Indian J Exp Biol. 2011, 49: 805-816.PubMedCentralPubMed
21.
go back to reference Nagini S: Cancer chemoprevention by garlic and its organosulfur compounds-panacea or promise?. Anticancer Agents Med Chem. 2008, 8: 313-321. 10.2174/187152008783961879.CrossRefPubMed Nagini S: Cancer chemoprevention by garlic and its organosulfur compounds-panacea or promise?. Anticancer Agents Med Chem. 2008, 8: 313-321. 10.2174/187152008783961879.CrossRefPubMed
22.
go back to reference Anthony JP, Fyfe L, Smith H: Plant active components - a resource for antiparasitic agents?. Trends Parasitol. 2005, 21: 462-468. 10.1016/j.pt.2005.08.004.CrossRefPubMed Anthony JP, Fyfe L, Smith H: Plant active components - a resource for antiparasitic agents?. Trends Parasitol. 2005, 21: 462-468. 10.1016/j.pt.2005.08.004.CrossRefPubMed
23.
go back to reference Wabwoba BW, Anjili CO, Ngeiywa MM, Ngure PK, Kigondu EM, Ingonga J, Makwali J: Experimental chemotherapy with Allium sativum (Liliaceae) methanolic extract in rodents infected with Leishmania major and Leishmania donovani. J Vector Borne Dis. 2010, 47: 160-167.PubMed Wabwoba BW, Anjili CO, Ngeiywa MM, Ngure PK, Kigondu EM, Ingonga J, Makwali J: Experimental chemotherapy with Allium sativum (Liliaceae) methanolic extract in rodents infected with Leishmania major and Leishmania donovani. J Vector Borne Dis. 2010, 47: 160-167.PubMed
24.
go back to reference Gamboa-Leon MR, Aranda-Gonzalez I, Mut-Martin M, Garcia-Miss MR, Dumonteil E: In vivo and in vitro control of Leishmania mexicana due to garlic-induced NO production. Scand J Immunol. 2007, 66: 508-514. 10.1111/j.1365-3083.2007.02000.x.CrossRefPubMed Gamboa-Leon MR, Aranda-Gonzalez I, Mut-Martin M, Garcia-Miss MR, Dumonteil E: In vivo and in vitro control of Leishmania mexicana due to garlic-induced NO production. Scand J Immunol. 2007, 66: 508-514. 10.1111/j.1365-3083.2007.02000.x.CrossRefPubMed
25.
go back to reference Mantawy MM, Ali HF, Rizk MZ: Therapeutic effects of Allium sativum and Allium cepa in Schistosoma mansoni experimental infection. Rev Inst Med Trop São Paulo. 2011, 53: 155-163. 10.1590/S0036-46652011000300007.CrossRefPubMed Mantawy MM, Ali HF, Rizk MZ: Therapeutic effects of Allium sativum and Allium cepa in Schistosoma mansoni experimental infection. Rev Inst Med Trop São Paulo. 2011, 53: 155-163. 10.1590/S0036-46652011000300007.CrossRefPubMed
26.
go back to reference Nahed HA, Hoda AT, Yomna IM: Effects of garlic on albino mice experimentally infected with Schistosoma mansoni: a parasitological and ultrastructural study. Trop Biomed. 2009, 26: 40-50.PubMed Nahed HA, Hoda AT, Yomna IM: Effects of garlic on albino mice experimentally infected with Schistosoma mansoni: a parasitological and ultrastructural study. Trop Biomed. 2009, 26: 40-50.PubMed
27.
go back to reference Lun ZR, Burri C, Menzinger M, Kaminsky R: Antiparasitic activity of diallyl trisulfide (Dasuansu) on human and animal pathogenic protozoa (Trypanosoma sp., Entamoeba histolytica and Giardia lamblia) in vitro. Ann Soc Belg Med Trop. 1994, 74: 51-59.PubMed Lun ZR, Burri C, Menzinger M, Kaminsky R: Antiparasitic activity of diallyl trisulfide (Dasuansu) on human and animal pathogenic protozoa (Trypanosoma sp., Entamoeba histolytica and Giardia lamblia) in vitro. Ann Soc Belg Med Trop. 1994, 74: 51-59.PubMed
28.
go back to reference Ankri S, Miron T, Rabinkov A, Wilchek M, Mirelman D: Allicin from garlic strongly inhibits cysteine proteinases and cytopathic effects of Entamoeba histolytica. Antimicrob Agents Chemother. 1997, 41: 2286-2288.PubMedCentralPubMed Ankri S, Miron T, Rabinkov A, Wilchek M, Mirelman D: Allicin from garlic strongly inhibits cysteine proteinases and cytopathic effects of Entamoeba histolytica. Antimicrob Agents Chemother. 1997, 41: 2286-2288.PubMedCentralPubMed
29.
go back to reference Perez HA, De la Rosa M, Apitz R: In vivo activity of ajoene against rodent malaria. Antimicrob Agents Chemother. 1994, 38: 337-339. 10.1128/AAC.38.2.337.PubMedCentralCrossRefPubMed Perez HA, De la Rosa M, Apitz R: In vivo activity of ajoene against rodent malaria. Antimicrob Agents Chemother. 1994, 38: 337-339. 10.1128/AAC.38.2.337.PubMedCentralCrossRefPubMed
30.
go back to reference Coppi A, Cabinian M, Mirelman D, Sinnis P: Antimalarial activity of allicin, a biologically active compound from garlic cloves. Antimicrob Agents Chemother. 2006, 50: 1731-1737. 10.1128/AAC.50.5.1731-1737.2006.PubMedCentralCrossRefPubMed Coppi A, Cabinian M, Mirelman D, Sinnis P: Antimalarial activity of allicin, a biologically active compound from garlic cloves. Antimicrob Agents Chemother. 2006, 50: 1731-1737. 10.1128/AAC.50.5.1731-1737.2006.PubMedCentralCrossRefPubMed
31.
go back to reference Amagase H: Clarifying the real bioactive constituents of garlic. J Nutr. 2006, 136: 716S-725S.PubMed Amagase H: Clarifying the real bioactive constituents of garlic. J Nutr. 2006, 136: 716S-725S.PubMed
32.
go back to reference Waag T, Gelhaus C, Rath J, Stich A, Leippe M, Schirmeister T: Allicin and derivates are cysteine protease inhibitors with antiparasitic activity. Bioorg Med Chem Lett. 2010, 20: 5541-5543. 10.1016/j.bmcl.2010.07.062.CrossRefPubMed Waag T, Gelhaus C, Rath J, Stich A, Leippe M, Schirmeister T: Allicin and derivates are cysteine protease inhibitors with antiparasitic activity. Bioorg Med Chem Lett. 2010, 20: 5541-5543. 10.1016/j.bmcl.2010.07.062.CrossRefPubMed
33.
go back to reference Amagase H, Petesch BL, Matsuura H, Kasuga S, Itakura Y: Intake of garlic and its bioactive components. J Nutr. 2001, 131: 955S-962S.PubMed Amagase H, Petesch BL, Matsuura H, Kasuga S, Itakura Y: Intake of garlic and its bioactive components. J Nutr. 2001, 131: 955S-962S.PubMed
34.
go back to reference Kyo E, Uda N, Kasuga S, Itakura Y: Immunomodulatory effects of aged garlic extract. J Nutr. 2001, 131: 1075S-1079S.PubMed Kyo E, Uda N, Kasuga S, Itakura Y: Immunomodulatory effects of aged garlic extract. J Nutr. 2001, 131: 1075S-1079S.PubMed
35.
go back to reference Lau BH, Yamasaki T, Gridley DS: Garlic compounds modulate macrophage and T-lymphocyte functions. Mol Biother. 1991, 3: 103-107. 10.1007/BF02172082.CrossRefPubMed Lau BH, Yamasaki T, Gridley DS: Garlic compounds modulate macrophage and T-lymphocyte functions. Mol Biother. 1991, 3: 103-107. 10.1007/BF02172082.CrossRefPubMed
36.
go back to reference Bhattacharyya M, Girish GV, Karmohapatra SK, Samad SA, Sinha AK: Systemic production of IFN-alpha by garlic (Allium sativum) in humans. J Interferon Cytokine Res. 2007, 27: 377-382. 10.1089/jir.2006.0124.CrossRefPubMed Bhattacharyya M, Girish GV, Karmohapatra SK, Samad SA, Sinha AK: Systemic production of IFN-alpha by garlic (Allium sativum) in humans. J Interferon Cytokine Res. 2007, 27: 377-382. 10.1089/jir.2006.0124.CrossRefPubMed
37.
go back to reference Morihara N, Sumioka I, Moriguchi T, Uda N, Kyo E: Aged garlic extract enhances production of nitric oxide. Life Sci. 2002, 71: 509-517. 10.1016/S0024-3205(02)01706-X.CrossRefPubMed Morihara N, Sumioka I, Moriguchi T, Uda N, Kyo E: Aged garlic extract enhances production of nitric oxide. Life Sci. 2002, 71: 509-517. 10.1016/S0024-3205(02)01706-X.CrossRefPubMed
38.
go back to reference Hodge G, Hodge S, Han P: Allium sativum (garlic) suppresses leukocyte inflammatory cytokine production in vitro: potential therapeutic use in the treatment of inflammatory bowel disease. Cytometry. 2002, 48: 209-215. 10.1002/cyto.10133.CrossRefPubMed Hodge G, Hodge S, Han P: Allium sativum (garlic) suppresses leukocyte inflammatory cytokine production in vitro: potential therapeutic use in the treatment of inflammatory bowel disease. Cytometry. 2002, 48: 209-215. 10.1002/cyto.10133.CrossRefPubMed
39.
go back to reference Ghazanfari T, Hassan ZM, Ebtekar M, Ahmadiani A, Naderi G, Azar A: Garlic induces a shift in cytokine pattern in Leishmania major-infected BALB/c mice. Scand J Immunol. 2000, 52: 491-495. 10.1046/j.1365-3083.2000.00803.x.CrossRefPubMed Ghazanfari T, Hassan ZM, Ebtekar M, Ahmadiani A, Naderi G, Azar A: Garlic induces a shift in cytokine pattern in Leishmania major-infected BALB/c mice. Scand J Immunol. 2000, 52: 491-495. 10.1046/j.1365-3083.2000.00803.x.CrossRefPubMed
40.
go back to reference Ghazanfari T, Hassan ZM, Khamesipour A: Enhancement of peritoneal macrophage phagocytic activity against Leishmania major by garlic (Allium sativum) treatment. J Ethnopharmacol. 2006, 103: 333-337. 10.1016/j.jep.2005.08.026.CrossRefPubMed Ghazanfari T, Hassan ZM, Khamesipour A: Enhancement of peritoneal macrophage phagocytic activity against Leishmania major by garlic (Allium sativum) treatment. J Ethnopharmacol. 2006, 103: 333-337. 10.1016/j.jep.2005.08.026.CrossRefPubMed
41.
go back to reference Zhu X, Pan Y, Zheng L, Cui L, Cao Y: Polysaccharides from the Chinese medicinal herb Achyranthes bidentata enhance anti-malarial immunity during Plasmodium yoelii 17XL infection in mice. Malar J. 2012, 11: 49-10.1186/1475-2875-11-49.PubMedCentralCrossRefPubMed Zhu X, Pan Y, Zheng L, Cui L, Cao Y: Polysaccharides from the Chinese medicinal herb Achyranthes bidentata enhance anti-malarial immunity during Plasmodium yoelii 17XL infection in mice. Malar J. 2012, 11: 49-10.1186/1475-2875-11-49.PubMedCentralCrossRefPubMed
42.
go back to reference Cao YM, Tsuboi T, Torii M: Nitric oxide inhibits the development of Plasmodium yoelii gametocytes into gametes. Parasitol Int. 1998, 47: 157-166.CrossRef Cao YM, Tsuboi T, Torii M: Nitric oxide inhibits the development of Plasmodium yoelii gametocytes into gametes. Parasitol Int. 1998, 47: 157-166.CrossRef
43.
go back to reference Zhou LD, Zhang QH, Zhang Y, Liu J, Cao YM: The shiitake mushroom-derived immuno-stimulant lentinan protects against murine malaria blood-stage infection by evoking adaptive immune-responses. Int Immunopharmacol. 2009, 9: 455-462. 10.1016/j.intimp.2009.01.010.CrossRefPubMed Zhou LD, Zhang QH, Zhang Y, Liu J, Cao YM: The shiitake mushroom-derived immuno-stimulant lentinan protects against murine malaria blood-stage infection by evoking adaptive immune-responses. Int Immunopharmacol. 2009, 9: 455-462. 10.1016/j.intimp.2009.01.010.CrossRefPubMed
44.
go back to reference Sedegah M, Finkelman F, Hoffman SL: Interleukin 12 induction of interferon gamma-dependent protection against malaria. Proc Natl Acad Sci U S A. 1994, 91: 10700-10702. 10.1073/pnas.91.22.10700.PubMedCentralCrossRefPubMed Sedegah M, Finkelman F, Hoffman SL: Interleukin 12 induction of interferon gamma-dependent protection against malaria. Proc Natl Acad Sci U S A. 1994, 91: 10700-10702. 10.1073/pnas.91.22.10700.PubMedCentralCrossRefPubMed
45.
go back to reference Doolan DL, Hoffman SL: IL-12 and NK cells are required for antigen-specific adaptive immunity against malaria initiated by CD8+ T cells in the Plasmodium yoelii model. J Immunol. 1999, 163: 884-892.PubMed Doolan DL, Hoffman SL: IL-12 and NK cells are required for antigen-specific adaptive immunity against malaria initiated by CD8+ T cells in the Plasmodium yoelii model. J Immunol. 1999, 163: 884-892.PubMed
46.
go back to reference Su Z, Stevenson MM: IL-12 is required for antibody-mediated protective immunity against blood-stage Plasmodium chabaudi AS malaria infection in mice. J Immunol. 2002, 168: 1348-1355.CrossRefPubMed Su Z, Stevenson MM: IL-12 is required for antibody-mediated protective immunity against blood-stage Plasmodium chabaudi AS malaria infection in mice. J Immunol. 2002, 168: 1348-1355.CrossRefPubMed
47.
go back to reference Stephens R, Albano FR, Quin S, Pascal BJ, Harrison V, Stockinger B, Kioussis D, Weltzien HU, Langhorne J: Malaria-specific transgenic CD4(+) T cells protect immunodeficient mice from lethal infection and demonstrate requirement for a protective threshold of antibody production for parasite clearance. Blood. 2005, 106: 1676-1684. 10.1182/blood-2004-10-4047.CrossRefPubMed Stephens R, Albano FR, Quin S, Pascal BJ, Harrison V, Stockinger B, Kioussis D, Weltzien HU, Langhorne J: Malaria-specific transgenic CD4(+) T cells protect immunodeficient mice from lethal infection and demonstrate requirement for a protective threshold of antibody production for parasite clearance. Blood. 2005, 106: 1676-1684. 10.1182/blood-2004-10-4047.CrossRefPubMed
48.
go back to reference Ing R, Segura M, Thawani N, Tam M, Stevenson MM: Interaction of mouse dendritic cells and malaria-infected erythrocytes: uptake, maturation, and antigen presentation. J Immunol. 2006, 176: 441-450.CrossRefPubMed Ing R, Segura M, Thawani N, Tam M, Stevenson MM: Interaction of mouse dendritic cells and malaria-infected erythrocytes: uptake, maturation, and antigen presentation. J Immunol. 2006, 176: 441-450.CrossRefPubMed
49.
go back to reference Schwartz IF, Hershkovitz R, Iaina A, Gnessin E, Wollman Y, Chernichowski T, Blum M, Levo Y, Schwartz D: Garlic attenuates nitric oxide production in rat cardiac myocytes through inhibition of inducible nitric oxide synthase and the arginine transporter CAT-2 (cationic amino acid transporter-2). Clin Sci (Lond). 2002, 102: 487-493. 10.1042/CS20010221.CrossRef Schwartz IF, Hershkovitz R, Iaina A, Gnessin E, Wollman Y, Chernichowski T, Blum M, Levo Y, Schwartz D: Garlic attenuates nitric oxide production in rat cardiac myocytes through inhibition of inducible nitric oxide synthase and the arginine transporter CAT-2 (cationic amino acid transporter-2). Clin Sci (Lond). 2002, 102: 487-493. 10.1042/CS20010221.CrossRef
50.
go back to reference Hasan N, Yusuf N, Toossi Z, Islam N: Suppression of Mycobacterium tuberculosis induced reactive oxygen species (ROS) and TNF-alpha mRNA expression in human monocytes by allicin. FEBS Lett. 2006, 580: 2517-2522. 10.1016/j.febslet.2006.03.071.CrossRefPubMed Hasan N, Yusuf N, Toossi Z, Islam N: Suppression of Mycobacterium tuberculosis induced reactive oxygen species (ROS) and TNF-alpha mRNA expression in human monocytes by allicin. FEBS Lett. 2006, 580: 2517-2522. 10.1016/j.febslet.2006.03.071.CrossRefPubMed
51.
go back to reference Bruck R, Aeed H, Brazovsky E, Noor T, Hershkoviz R: Allicin, the active component of garlic, prevents immune-mediated, concanavalin A-induced hepatic injury in mice. Liver Int. 2005, 25: 613-621. 10.1111/j.1478-3231.2005.01050.x.CrossRefPubMed Bruck R, Aeed H, Brazovsky E, Noor T, Hershkoviz R: Allicin, the active component of garlic, prevents immune-mediated, concanavalin A-induced hepatic injury in mice. Liver Int. 2005, 25: 613-621. 10.1111/j.1478-3231.2005.01050.x.CrossRefPubMed
52.
go back to reference Kyung KH: Antimicrobial properties of allium species. Curr Opin Biotechnol. 2012, 23: 142-147. 10.1016/j.copbio.2011.08.004.CrossRefPubMed Kyung KH: Antimicrobial properties of allium species. Curr Opin Biotechnol. 2012, 23: 142-147. 10.1016/j.copbio.2011.08.004.CrossRefPubMed
53.
go back to reference Fujisawa H, Watanabe K, Suma K, Origuchi K, Matsufuji H, Seki T, Ariga T: Antibacterial potential of garlic-derived allicin and its cancellation by sulfhydryl compounds. Biosci Biotechnol Biochem. 2009, 73: 1948-1955. 10.1271/bbb.90096.CrossRefPubMed Fujisawa H, Watanabe K, Suma K, Origuchi K, Matsufuji H, Seki T, Ariga T: Antibacterial potential of garlic-derived allicin and its cancellation by sulfhydryl compounds. Biosci Biotechnol Biochem. 2009, 73: 1948-1955. 10.1271/bbb.90096.CrossRefPubMed
54.
go back to reference Rennenberg A, Lehmann C, Heitmann A, Witt T, Hansen G, Nagarajan K, Deschermeier C, Turk V, Hilgenfeld R, Heussler VT: Exoerythrocytic Plasmodium parasites secrete a cysteine protease inhibitor involved in sporozoite invasion and capable of blocking cell death of host hepatocytes. PLoS Pathog. 2010, 6: e1000825-10.1371/journal.ppat.1000825.PubMedCentralCrossRefPubMed Rennenberg A, Lehmann C, Heitmann A, Witt T, Hansen G, Nagarajan K, Deschermeier C, Turk V, Hilgenfeld R, Heussler VT: Exoerythrocytic Plasmodium parasites secrete a cysteine protease inhibitor involved in sporozoite invasion and capable of blocking cell death of host hepatocytes. PLoS Pathog. 2010, 6: e1000825-10.1371/journal.ppat.1000825.PubMedCentralCrossRefPubMed
55.
go back to reference Chen G, Feng H, Liu J, Qi ZM, Wu Y, Guo SY, Li DM, Wang JC, Cao YM: Characterization of immune responses to single or mixed infections with P. yoelii 17XL and P. chabaudi AS in different strains of mice. Parasitol Int. 2010, 59: 400-406. 10.1016/j.parint.2010.05.005.CrossRefPubMed Chen G, Feng H, Liu J, Qi ZM, Wu Y, Guo SY, Li DM, Wang JC, Cao YM: Characterization of immune responses to single or mixed infections with P. yoelii 17XL and P. chabaudi AS in different strains of mice. Parasitol Int. 2010, 59: 400-406. 10.1016/j.parint.2010.05.005.CrossRefPubMed
56.
go back to reference Taylor-Robinson AW, Phillips RS, Severn A, Moncada S, Liew FY: The role of TH1 and TH2 cells in a rodent malaria infection. Science. 1993, 260: 1931-1934. 10.1126/science.8100366.CrossRefPubMed Taylor-Robinson AW, Phillips RS, Severn A, Moncada S, Liew FY: The role of TH1 and TH2 cells in a rodent malaria infection. Science. 1993, 260: 1931-1934. 10.1126/science.8100366.CrossRefPubMed
57.
go back to reference Taverne J, Sheikh N, de Souza JB, Playfair JH, Probert L, Kollias G: Anaemia and resistance to malaria in transgenic mice expressing human tumour necrosis factor. Immunology. 1994, 82: 397-403.PubMedCentralPubMed Taverne J, Sheikh N, de Souza JB, Playfair JH, Probert L, Kollias G: Anaemia and resistance to malaria in transgenic mice expressing human tumour necrosis factor. Immunology. 1994, 82: 397-403.PubMedCentralPubMed
58.
go back to reference McCall MB, Sauerwein RW: Interferon-gamma–central mediator of protective immune responses against the pre-erythrocytic and blood stage of malaria. J Leukoc Biol. 2010, 88: 1131-1143. 10.1189/jlb.0310137.CrossRefPubMed McCall MB, Sauerwein RW: Interferon-gamma–central mediator of protective immune responses against the pre-erythrocytic and blood stage of malaria. J Leukoc Biol. 2010, 88: 1131-1143. 10.1189/jlb.0310137.CrossRefPubMed
59.
go back to reference Perry JA, Rush A, Wilson RJ, Olver CS, Avery AC: Dendritic cells from malaria-infected mice are fully functional APC. J Immunol. 2004, 172: 475-482.CrossRefPubMed Perry JA, Rush A, Wilson RJ, Olver CS, Avery AC: Dendritic cells from malaria-infected mice are fully functional APC. J Immunol. 2004, 172: 475-482.CrossRefPubMed
60.
go back to reference Banchereau J, Steinman RM: Dendritic cells and the control of immunity. Nature. 1998, 392: 245-252. 10.1038/32588.CrossRefPubMed Banchereau J, Steinman RM: Dendritic cells and the control of immunity. Nature. 1998, 392: 245-252. 10.1038/32588.CrossRefPubMed
61.
go back to reference Wykes MN, Liu XQ, Beattie L, Stanisic DI, Stacey KJ, Smyth MJ, Thomas R, Good MF: Plasmodium strain determines dendritic cell function essential for survival from malaria. PLoS Pathog. 2007, 3: e96-10.1371/journal.ppat.0030096.PubMedCentralCrossRefPubMed Wykes MN, Liu XQ, Beattie L, Stanisic DI, Stacey KJ, Smyth MJ, Thomas R, Good MF: Plasmodium strain determines dendritic cell function essential for survival from malaria. PLoS Pathog. 2007, 3: e96-10.1371/journal.ppat.0030096.PubMedCentralCrossRefPubMed
62.
go back to reference Ing R, Stevenson MM: Dendritic cell and NK cell reciprocal cross talk promotes gamma interferon-dependent immunity to blood-stage Plasmodium chabaudi AS infection in mice. Infect Immun. 2009, 77: 770-782. 10.1128/IAI.00994-08.PubMedCentralCrossRefPubMed Ing R, Stevenson MM: Dendritic cell and NK cell reciprocal cross talk promotes gamma interferon-dependent immunity to blood-stage Plasmodium chabaudi AS infection in mice. Infect Immun. 2009, 77: 770-782. 10.1128/IAI.00994-08.PubMedCentralCrossRefPubMed
63.
go back to reference Iwasaki A, Medzhitov R: Toll-like receptor control of the adaptive immune responses. Nat Immunol. 2004, 5: 987-995. 10.1038/ni1112.CrossRefPubMed Iwasaki A, Medzhitov R: Toll-like receptor control of the adaptive immune responses. Nat Immunol. 2004, 5: 987-995. 10.1038/ni1112.CrossRefPubMed
64.
go back to reference Pasare C, Medzhitov R: Toll-like receptors: linking innate and adaptive immunity. Adv Exp Med Biol. 2005, 560: 11-18. 10.1007/0-387-24180-9_2.CrossRefPubMed Pasare C, Medzhitov R: Toll-like receptors: linking innate and adaptive immunity. Adv Exp Med Biol. 2005, 560: 11-18. 10.1007/0-387-24180-9_2.CrossRefPubMed
65.
go back to reference Coban C, Ishii KJ, Kawai T, Hemmi H, Sato S, Uematsu S, Yamamoto M, Takeuchi O, Itagaki S, Kumar N, Horii T, Akira S: Toll-like receptor 9 mediates innate immune activation by the malaria pigment hemozoin. J Exp Med. 2005, 201: 19-25. 10.1084/jem.20041836.PubMedCentralCrossRefPubMed Coban C, Ishii KJ, Kawai T, Hemmi H, Sato S, Uematsu S, Yamamoto M, Takeuchi O, Itagaki S, Kumar N, Horii T, Akira S: Toll-like receptor 9 mediates innate immune activation by the malaria pigment hemozoin. J Exp Med. 2005, 201: 19-25. 10.1084/jem.20041836.PubMedCentralCrossRefPubMed
66.
go back to reference Wu X, Gowda NM, Kumar S, Gowda DC: Protein-DNA complex is the exclusive malaria parasite component that activates dendritic cells and triggers innate immune responses. J Immunol. 2010, 184: 4338-4348. 10.4049/jimmunol.0903824.PubMedCentralCrossRefPubMed Wu X, Gowda NM, Kumar S, Gowda DC: Protein-DNA complex is the exclusive malaria parasite component that activates dendritic cells and triggers innate immune responses. J Immunol. 2010, 184: 4338-4348. 10.4049/jimmunol.0903824.PubMedCentralCrossRefPubMed
67.
go back to reference Kalis C, Gumenscheimer M, Freudenberg N, Tchaptchet S, Fejer G, Heit A, Akira S, Galanos C, Freudenberg MA: Requirement for TLR9 in the immunomodulatory activity of Propionibacterium acnes. J Immunol. 2005, 174: 4295-4300.CrossRefPubMed Kalis C, Gumenscheimer M, Freudenberg N, Tchaptchet S, Fejer G, Heit A, Akira S, Galanos C, Freudenberg MA: Requirement for TLR9 in the immunomodulatory activity of Propionibacterium acnes. J Immunol. 2005, 174: 4295-4300.CrossRefPubMed
68.
go back to reference Franklin BS, Parroche P, Ataide MA, Lauw F, Ropert C, de Oliveira RB, Pereira D, Tada MS, Nogueira P, da Silva LH, Bjorkbacka H, Golenbock DT, Gazzinelli RT: Malaria primes the innate immune response due to interferon-gamma induced enhancement of toll-like receptor expression and function. Proc Natl Acad Sci U S A. 2009, 106: 5789-5794. 10.1073/pnas.0809742106.PubMedCentralCrossRefPubMed Franklin BS, Parroche P, Ataide MA, Lauw F, Ropert C, de Oliveira RB, Pereira D, Tada MS, Nogueira P, da Silva LH, Bjorkbacka H, Golenbock DT, Gazzinelli RT: Malaria primes the innate immune response due to interferon-gamma induced enhancement of toll-like receptor expression and function. Proc Natl Acad Sci U S A. 2009, 106: 5789-5794. 10.1073/pnas.0809742106.PubMedCentralCrossRefPubMed
69.
go back to reference Lang A, Lahav M, Sakhnini E, Barshack I, Fidder HH, Avidan B, Bardan E, Hershkoviz R, Bar-Meir S, Chowers Y: Allicin inhibits spontaneous and TNF-alpha induced secretion of proinflammatory cytokines and chemokines from intestinal epithelial cells. Clin Nutr. 2004, 23: 1199-1208. 10.1016/j.clnu.2004.03.011.CrossRefPubMed Lang A, Lahav M, Sakhnini E, Barshack I, Fidder HH, Avidan B, Bardan E, Hershkoviz R, Bar-Meir S, Chowers Y: Allicin inhibits spontaneous and TNF-alpha induced secretion of proinflammatory cytokines and chemokines from intestinal epithelial cells. Clin Nutr. 2004, 23: 1199-1208. 10.1016/j.clnu.2004.03.011.CrossRefPubMed
70.
go back to reference Hisaeda H, Maekawa Y, Iwakawa D, Okada H, Himeno K, Kishihara K, Tsukumo S, Yasutomo K: Escape of malaria parasites from host immunity requires CD4+ CD25+ regulatory T cells. Nat Med. 2004, 10: 29-30. 10.1038/nm975.CrossRefPubMed Hisaeda H, Maekawa Y, Iwakawa D, Okada H, Himeno K, Kishihara K, Tsukumo S, Yasutomo K: Escape of malaria parasites from host immunity requires CD4+ CD25+ regulatory T cells. Nat Med. 2004, 10: 29-30. 10.1038/nm975.CrossRefPubMed
71.
go back to reference Hisaeda H, Tetsutani K, Imai T, Moriya C, Tu L, Hamano S, Duan X, Chou B, Ishida H, Aramaki A, Shen J, Ishii KJ, Coban C, Akira S, Takeda K, Yasutomo K, Torii M, Himeno K: Malaria parasites require TLR9 signaling for immune evasion by activating regulatory T cells. J Immunol. 2008, 180: 2496-2503.CrossRefPubMed Hisaeda H, Tetsutani K, Imai T, Moriya C, Tu L, Hamano S, Duan X, Chou B, Ishida H, Aramaki A, Shen J, Ishii KJ, Coban C, Akira S, Takeda K, Yasutomo K, Torii M, Himeno K: Malaria parasites require TLR9 signaling for immune evasion by activating regulatory T cells. J Immunol. 2008, 180: 2496-2503.CrossRefPubMed
Metadata
Title
Allicin enhances host pro-inflammatory immune responses and protects against acute murine malaria infection
Authors
Yonghui Feng
Xiaotong Zhu
Qinghui Wang
Yongjun Jiang
Hong Shang
Liwang Cui
Yaming Cao
Publication date
01-12-2012
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2012
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/1475-2875-11-268

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