- Introduction
- Methods
- Results
- ABA supplementation increased circulating ABA levels and decreased parasitemia, gametocytemia, and disease pathology in P. yoelii-infected mice.
- ABA supplementation of mice reduced P. yoelii transmission to mosquitoes.
- ABA does not alter P. falciparum growth and gametocyte development in vitro.
- Supplementation of ABA in a P. falciparum-infected blood meal reduced transmission to An. stephensi by increasing nitric oxide production in the mosquito midgut.
- Discussion
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
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World Health Organization, 2015. World Malaria Report 2015. Available at: http://www.who.int/malaria/publications/world-malaria-report-2015/report/en/. Accessed December 1, 2015.
-
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Bruzzone S, Moreschi I, Usai C, Guida L, Salis A, Scarfi S, Millo E, De Flora A, Zocchi E, 2007. Abscisic acid is an endogenous cytokine in human granulocytes with cyclic ADP-ribose as second messenger. Proc Natl Acad Sci USA 104: 5759–5764.
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Zocchi E, Carpaneto A, Cerrano C, Bavestrello G, Giovine M, Bruzzone S, Guida L, Franco L, Usai C, 2001. The temperature-signaling cascade in sponges involves a heat-gated cation channel, abscisic acid, and cyclic ADP-ribose. Proc Natl Acad Sci USA 98: 14859–14864.
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Nagamune K, Hicks LM, Fux B, Brossier F, Chini EN, Sibley LD, 2008. Abscisic acid controls calcium-dependent egress and development in Toxoplasma gondii. Nature 451: 207–210.
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Mehrotra R, Bhalothia P, Bansal P, Basantani MK, Bharti V, Mehrotra S, 2014. Abscisic acid and abiotic stress tolerance—different tiers of regulation. J Plant Physiol 171: 486–496.
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Zocchi E, Basile G, Cerrano C, Bavestrello G, Giovine M, Bruzzone S, Guida L, Carpaneto A, Magrassi R, Usai C, 2003. ABA- and cADPR-mediated effects on respiration and filtration downstream of the temperature-signaling cascade in sponges. J Cell Sci 116: 629–636.
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Bruzzone S, Ameri P, Briatore L, Mannino E, Basile G, Andraghetti G, Grozio A, Magnone M, Guida L, Scarfi S, Salis A, Damonte G, Sturla L, Nencioni A, Fenoglio D, Fiory F, Miele C, Beguinot F, Ruvolo V, Bormioli M, Colombo G, Maggi D, Murialdo G, Cordera R, De Flora A, Zocchi E, 2011. The plant hormone abscisic acid increases in human plasma after hyperglycemia and stimulates glucose consumption by adipocyte myoblasts. FASEB J 26: 1251–1260.
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Puce S, Basile G, Bavestrello G, Bruzzone S, Cerrano C, Giovine M, Arillo A, Zocchi E, 2004. Abscisic acid signaling through cyclic ADP-ribose in hydroid regeneration. J Biol Chem 279: 39783–39788.
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Negri P, Maggi MD, Ramirez L, de Feudis L, Szwarski N, Quintana S, Eguaras MJ, Lamattina L, 2015. Abscisic acid enhances the immune response in Apis mellifera and contributes to the colony fitness. Apidologie (Celle) 46: 542–557.
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Bruzzone S, Basile G, Mannino E, Sturla L, Magnone M, Grozio A, Salis A, Fresia C, Vigliarolo T, Guida L, De Flora A, Tossi V, Cassia R, Lamattina L, Zocchi E, 2012. Autocrine abscisic acid mediates the UV-B-induced inflammatory response in human granulocytes and keratinocytes. J Cell Physiol 227: 2502–2510.
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Marois E, 2011. The multifaceted mosquito anti-Plasmodium response. Curr Opin Microbiol 14: 429–435.
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Roux CM, Butler BP, Chau JY, Paixao TA, Cheung KW, Santos TL, Luckhart S, Tsolis RM, 2010. Both hemolytic anemia and malaria parasite-specific factors increase susceptibility to Nontyphoidal Salmonella enterica serovar Typhimurium infection in mice. Infect Immun 78: 1520–1527.
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Drexler AL, Pietri JE, Pakpour N, Hauck E, Wang B, Glennon EK, Georgis M, Riehle MA, Luckhart S, 2014. Human IGF1 regulates midgut oxidative stress and epithelial homeostasis to balance lifespan and Plasmodium falciparum resistance in Anopheles stephensi. PLoS Pathog 10: e1004231.
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Supplementation with Abscisic Acid Reduces Malaria Disease Severity and Parasite Transmission
Elizabeth K. K. Glennon
Elizabeth K. K. Glennon
Department of Medical Microbiology and Immunology, School of Medicine, University of California, Davis, Davis, California; Department of Veterinary Pathobiology, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, Texas; Department of Plant Biology, University of California, Davis, Davis, California
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L. Garry Adams
L. Garry Adams
Department of Medical Microbiology and Immunology, School of Medicine, University of California, Davis, Davis, California; Department of Veterinary Pathobiology, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, Texas; Department of Plant Biology, University of California, Davis, Davis, California
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Derrick R. Hicks
Derrick R. Hicks
Department of Medical Microbiology and Immunology, School of Medicine, University of California, Davis, Davis, California; Department of Veterinary Pathobiology, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, Texas; Department of Plant Biology, University of California, Davis, Davis, California
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Katayoon Dehesh
Katayoon Dehesh
Department of Medical Microbiology and Immunology, School of Medicine, University of California, Davis, Davis, California; Department of Veterinary Pathobiology, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, Texas; Department of Plant Biology, University of California, Davis, Davis, California
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Shirley Luckhart
Shirley Luckhart
Department of Medical Microbiology and Immunology, School of Medicine, University of California, Davis, Davis, California; Department of Veterinary Pathobiology, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, Texas; Department of Plant Biology, University of California, Davis, Davis, California
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Nearly half of the world's population is at risk for malaria. Increasing drug resistance has intensified the need for novel therapeutics, including treatments with intrinsic transmission-blocking properties. In this study, we demonstrate that the isoprenoid abscisic acid (ABA) modulates signaling in the mammalian host to reduce parasitemia and the formation of transmissible gametocytes and in the mosquito host to reduce parasite infection. Oral ABA supplementation in a mouse model of malaria was well tolerated and led to reduced pathology and enhanced gene expression in the liver and spleen consistent with infection recovery. Oral ABA supplementation also increased mouse plasma ABA to levels that can signal in the mosquito midgut upon blood ingestion. Accordingly, we showed that supplementation of a Plasmodium falciparum-infected blood meal with ABA increased expression of mosquito nitric oxide synthase and reduced infection prevalence in a nitric oxide-dependent manner. Identification of the mechanisms whereby ABA reduces parasite growth in mammals and mosquitoes could shed light on the balance of immunity and metabolism across eukaryotes and provide a strong foundation for clinical translation.
Author Notes
Financial support: This work was supported by the University of California, Davis College of Biological Sciences Dean's Kingdom Crossing Project, funded by the Stanley and Jacqueline Schilling Endowment. The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Disclosure: Shirley Luckhart and Elizabeth K. K. Glennon are authors on a provisional patent.
Authors' addresses: Elizabeth K. K. Glennon and Shirley Luckhart, Department of Medical Microbiology and Immunology, University of California, Davis, Davis, CA, E-mails: ekglennon@ucdavis.edu and sluckhart@ucdavis.edu. L. Garry Adams, Department of Veterinary Pathobiology, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, TX, E-mail: gadams@cvm.tamu.edu. Derrick R. Hicks, Department of Plant Pathology, University of California, Davis, Davis, CA, E-mail: drhicks1@uw.edu. Katayoon Dehesh, Department of Plant Biology, University of California, Davis, Davis, CA, E-mail: kdehesh@ucdavis.edu.
- Introduction
- Methods
- Results
- ABA supplementation increased circulating ABA levels and decreased parasitemia, gametocytemia, and disease pathology in P. yoelii-infected mice.
- ABA supplementation of mice reduced P. yoelii transmission to mosquitoes.
- ABA does not alter P. falciparum growth and gametocyte development in vitro.
- Supplementation of ABA in a P. falciparum-infected blood meal reduced transmission to An. stephensi by increasing nitric oxide production in the mosquito midgut.
- Discussion
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
World Health Organization, 2015. World Malaria Report 2015. Available at: http://www.who.int/malaria/publications/world-malaria-report-2015/report/en/. Accessed December 1, 2015.
-
2.
Bruzzone S, Moreschi I, Usai C, Guida L, Salis A, Scarfi S, Millo E, De Flora A, Zocchi E, 2007. Abscisic acid is an endogenous cytokine in human granulocytes with cyclic ADP-ribose as second messenger. Proc Natl Acad Sci USA 104: 5759–5764.
-
3.
Zocchi E, Carpaneto A, Cerrano C, Bavestrello G, Giovine M, Bruzzone S, Guida L, Franco L, Usai C, 2001. The temperature-signaling cascade in sponges involves a heat-gated cation channel, abscisic acid, and cyclic ADP-ribose. Proc Natl Acad Sci USA 98: 14859–14864.
-
4.
Nagamune K, Hicks LM, Fux B, Brossier F, Chini EN, Sibley LD, 2008. Abscisic acid controls calcium-dependent egress and development in Toxoplasma gondii. Nature 451: 207–210.
-
5.
Mehrotra R, Bhalothia P, Bansal P, Basantani MK, Bharti V, Mehrotra S, 2014. Abscisic acid and abiotic stress tolerance—different tiers of regulation. J Plant Physiol 171: 486–496.
-
6.
Zocchi E, Basile G, Cerrano C, Bavestrello G, Giovine M, Bruzzone S, Guida L, Carpaneto A, Magrassi R, Usai C, 2003. ABA- and cADPR-mediated effects on respiration and filtration downstream of the temperature-signaling cascade in sponges. J Cell Sci 116: 629–636.
-
7.
Bruzzone S, Ameri P, Briatore L, Mannino E, Basile G, Andraghetti G, Grozio A, Magnone M, Guida L, Scarfi S, Salis A, Damonte G, Sturla L, Nencioni A, Fenoglio D, Fiory F, Miele C, Beguinot F, Ruvolo V, Bormioli M, Colombo G, Maggi D, Murialdo G, Cordera R, De Flora A, Zocchi E, 2011. The plant hormone abscisic acid increases in human plasma after hyperglycemia and stimulates glucose consumption by adipocyte myoblasts. FASEB J 26: 1251–1260.
-
8.
Puce S, Basile G, Bavestrello G, Bruzzone S, Cerrano C, Giovine M, Arillo A, Zocchi E, 2004. Abscisic acid signaling through cyclic ADP-ribose in hydroid regeneration. J Biol Chem 279: 39783–39788.
-
9.
Scarfi S, Ferraris C, Fruscione F, Fresia C, Guida L, Bruzzone S, Usai C, Parodi A, Millo E, Salis A, Burastero G, De Flora A, 2008. Cyclic ADP-ribose-mediated expansion and stimulation of human mesenchymal stem cells by the plant hormone abscisic acid. Stem Cells 26: 2855–2864.
-
10.
Bodrato N, Franco L, Fresia C, Guida L, Usai C, Salis A, Moreschi I, Ferraris C, Verderio C, Basile G, Bruzzone S, Scarfi S, De Flora A, Zocchi E, 2009. Abscisic acid activates the murine microglial cell line N9 through the second messenger cyclic ADP-ribose. J Biol Chem 284: 14777–14787.
-
11.
Guri AJ, Evans NP, Hontecillas R, Bassaganya-Riera J, 2011. T cell PPARγ is required for the anti-inflammatory efficacy of abscisic acid against experimental IBD. J Nutr Biochem 22: 812–819.
-
12.
Guri AJ, Hontecillas R, Bassaganya-Riera J, 2010. Abscisic acid ameliorates experimental IBD by downregulating cellular adhesion molecule expression and suppressing immune cell infiltration. Clin Nutr 29: 824–831.
-
13.
Rupani AB, Amarapurkar AD, 2009. Hepatic changes in fatal malaria: an emerging problem. Ann Trop Med Parasitol 103: 119–127.
-
14.
Schofield L, 2007. Intravascular infiltrates and organ-specific inflammation in malaria pathogenesis. Immunol Cell Biol 85: 130–137.
-
15.
Negri P, Maggi MD, Ramirez L, de Feudis L, Szwarski N, Quintana S, Eguaras MJ, Lamattina L, 2015. Abscisic acid enhances the immune response in Apis mellifera and contributes to the colony fitness. Apidologie (Celle) 46: 542–557.
-
16.
Luckhart S, Crampton AL, Zamora R, Lieber MJ, Dos Santos PC, Peterson TM, Emmith N, Lim J, Wink DA, Vodovotz Y, 2003. Mammalian transforming growth factor beta 1 activated after ingestion by Anopheles stephensi modulates immunity. Infect Immun 71: 3000–3009.
-
17.
Pakpour N, Corby-Harris V, Green GP, Smithers HM, Cheung KW, Riehle MA, Luckhart S, 2012. Ingested human insulin inhibits the mosquito NF-κB-dependent immune response to Plasmodium falciparum. Infect Immun 80: 2141–2149.
-
18.
Bruzzone S, Basile G, Mannino E, Sturla L, Magnone M, Grozio A, Salis A, Fresia C, Vigliarolo T, Guida L, De Flora A, Tossi V, Cassia R, Lamattina L, Zocchi E, 2012. Autocrine abscisic acid mediates the UV-B-induced inflammatory response in human granulocytes and keratinocytes. J Cell Physiol 227: 2502–2510.
-
19.
Marois E, 2011. The multifaceted mosquito anti-Plasmodium response. Curr Opin Microbiol 14: 429–435.
-
20.
Roux CM, Butler BP, Chau JY, Paixao TA, Cheung KW, Santos TL, Luckhart S, Tsolis RM, 2010. Both hemolytic anemia and malaria parasite-specific factors increase susceptibility to Nontyphoidal Salmonella enterica serovar Typhimurium infection in mice. Infect Immun 78: 1520–1527.
-
21.
Engelberth MJ, Engelberth J, 2009. Monitoring plant hormones during stress responses. J Vis Exp 28: 1127.
-
22.
Schmelz EA, Alborn HT, Engelberth J, Tumlinson JH, 2003. Nitrogen deficiency increases volicitin-induced volatile emission, jasmonic acid accumulation, and ethylene sensitivity in maize. Plant Physiol 133: 295–306.
-
23.
Engelberth J, Schmelz EA, Alborn HT, Cardoza YJ, Huang J, Tumlinson JH, 2003. Simultaneous quantification of jasmonic acid and salicylic acid in plants by vapor-phase extraction and gas chromatography-chemical ionization-mass spectrometry. Anal Biochem 312: 242–250.
-
24.
Drexler AL, Pietri JE, Pakpour N, Hauck E, Wang B, Glennon EK, Georgis M, Riehle MA, Luckhart S, 2014. Human IGF1 regulates midgut oxidative stress and epithelial homeostasis to balance lifespan and Plasmodium falciparum resistance in Anopheles stephensi. PLoS Pathog 10: e1004231.
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