Plasmodium berghei ookinetes induce nitric oxide production in Anopheles pseudopunctipennis midguts cultured in vitro

Herrera-Ortíz, Antonia; Lanz‐Mendoza, Humberto; Martínez-Barnetche, Jesús; Hernández‐Martínez, Salvador; Villarreal-Treviño, Cuauhtémoc; Aguilar-Marcelino, Liliana; Rodrı́guez, Mario H.

doi:10.1016/j.ibmb.2004.05.007

Cited by 40 publications

(45 citation statements)

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“…We previously documented immune responses to local microorganisms in midguts of An. pseudopunctipennis (Herrera-Ortiz et al, 2004). The participation of PGs in hemolymph cellular immune responses against bacteria, fungi, and virus was previously demonstrated in hemipterans, lepidopterans, and orthopterans (Büyükgüzel et al, 2007;Garcia et al, 2004;Jurenka et al, 1997;Lord et al, 2002;Miller et al, 1999), but this is the first report on the induction of PGE 2 by bacteria in the midgut of an insect.…”

Section: Archives Of Insect Biochemistry and Physiology May 2008mentioning

confidence: 69%

“…Dissections were carried out in 40 µl sterile phosphate buffer saline (PBS: 140 mM NaCl, 2.6 mM KCl, 1.5 mM KH 2 PO 4 , 20 mM Na 2 HPO 4 , pH 7.3). Groups of 10 midguts, fat bodies, Malpighian tubules, and ovarioles were collected separately in 24-well multichamber plates (Herrera-Ortiz et al, 2004) (Nalgene Nunc Co., Naperville, IL) containing 500 µl of Schneider's medium (GIBCO-BRL). The organs were cultured at 22-24°C for 60 min and viability was assessed by observing motility and by 3-(4,5-dimetil-2-thiazolil)-2,5-difenyl-2H tetrazolium bromide (MTT, Sigma Chem) reduction (Lanz-Mendoza et al, 2002).…”

Section: Culture Of Mosquito Organsmentioning

confidence: 99%

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Prostaglandin E₂ modulates the expression of antimicrobial peptides in the fat body and midgut of Anopheles albimanus

Muñoz

Martínez-Barnetche

Lanz‐Mendoza

et al. 2008

Arch Insect Biochem Physiol

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Prostaglandins (PGs) participate in the regulation of vertebrate and in at least six insect orders' immune responses. We identified PGE 2 in midgut, fat body, Malpighian tubules, and ovarioles of Anopheles albimanus (Aa) mosquitoes. Our data indicate that PGE 2 synthesis in cultured midguts responds to the presence of two bacterial species, Micrococcus luteus and Klebsiella pneumoniae. The production of mRNA coding for antimicrobial peptides Aa-Attacin, Aa-Cecropin, and Aa-Gambicin was observed in cultured fat bodies and midguts. The production of these messengers was reduced in the presence of dexamethasone, and this effect was reversed by arachidonic acid. Adding PGE 2 to cultures resulted in increased Aa-cecropin mRNA and decreased Aa-attacin and Aa-gambicin mRNAs. Arch. Insect Biochem. Physiol. 68:14-25, 2008 KEYWORDS: insect immunity; arachidonic acid; dexamethasone; Anopheles albimanus; antimicrobial peptides INTRODUCTIONInsects resist the constant threat of invasion by microorganisms with integumental barriers and the presence of peritrophic matrix in their digestive tracts. When microbes overcome these first-line defenses, they encounter well-organized immune reactions that resemble mammalian innate immunity. Circulating hemocytes phagocytose microbial invaders and respond by forming microaggregates and nodules. Hemocytes also encapsulate those invaders, such as parasitoid eggs, too big to phagocytose (Stanley, 2006;Stanley and Miller, 2006). These cellular defense mechanisms are practically immediate upon microbial invasion, but complex humoral responses, including hemolymph clotting (Blandin and Levashina, 2004), melanization, and the production of antimicrobial peptides (Yu and Kanost, 2003;Lemaitre and Hoffmann, 2007) are deployed later.Eicosanoids including prostaglandins (PGs) are fatty acid metabolites that in mammals are produced by many cell types, including epithelial and immune cells, and play key roles in hemostasis and immune regulation, among many other functions (Harris et al., 2002). The biosynthesis of PGs in insects is initiated by a phospholipase A 2 (PLA 2 ) that cleaves membrane phospholipids (C20 polyunsaturated fatty acids including arachidonic acid [AA]), and the resulting products are converted to PGs' bioactive forms by cyclooxygenases (COX) (Stanley, 2000(Stanley, , 2006, but products of the lipoxygenase pathway (LOX) have been also documented (Galdelhak et al., 1995). The induction of eicosanoid biosynthesis by bacteria has been observed in several insect species (Stanley, 2006 and Miller, 2006). The information on the participation of eicosanoids in insect humoral immune responses is limited; PGs mediate the expression of genes encoding the antibacterial peptide cecropine and lysozime in the silkworm Bombyx mori (Morishima et al., 1997) and regulate the activation of prophenoloxidase (PPO) in two insect species, Galleria mellonella (Downer et al., 1997) and Rhodnius prolixus (García et al., 2004). However, they do not activate PPO in other insects (Lord et al., 2002;Goldswor...

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Section: Archives Of Insect Biochemistry and Physiology May 2008mentioning

confidence: 69%

Section: Culture Of Mosquito Organsmentioning

confidence: 99%

Prostaglandin E₂ modulates the expression of antimicrobial peptides in the fat body and midgut of Anopheles albimanus

Muñoz

Martínez-Barnetche

Lanz‐Mendoza

et al. 2008

Arch Insect Biochem Physiol

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“…Dietary provision of the NOS substrate, L-arginine, or a NOS inhibitor, L-NAME, reduced or increased oocyst numbers in infected mosquitoes, respectively ; demonstrating that parasite numbers are limited by NO (Luckhart et al 1998). P. bergheiinfected blood meals also induce iNOS in the midguts of A. pseudopunctipennis, as does L-DOPA ; indicating the participation of H 2 O 2 (Herrera- Ortiz et al 2004). P. falciparum has been shown to induce expression of AsNOS as early as 6 h post-infection (Crampton and Luckhart, 2001 ;Lim et al 2005).…”

Section: N I T R I C O X I D Ementioning

confidence: 99%

“…Several workers have demonstrated that RNIs reduce malaria transmission by affecting gametocyte infectivity, and this inactivation has been associated with the presence of white blood cells (Motard et al 1993 ;Naotunne et al 1993). Furthermore the killing effect of NO on ookinetes has been demonstrated by trypan blue staining (Herrera-Ortiz et al 2004).…”

Section: N I T R I C O X I D Ementioning

confidence: 99%

“…There is evidence that H 2 O 2 causes the death of P. berghei ookinetes (Herrera-Ortiz et al 2004) but it is unclear whether this death equates to the apoptotic-like death observed in ookinetes in vivo and in vitro (Al-Olayan, Williams and Hurd, 2002). However, what is certain is that very few of the thousands of mosquito stages that begin their development in this hostile environment survive to become oocysts (Vaughan, Hensley and Beier, 1994 a ;Vaughan, Noden and Beier, 1994 b;Alavi et al 2003).…”

Section: P a R A S I T E D E A T Hmentioning

confidence: 99%

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Apoptosis-like death as a feature of malaria infection in mosquitoes

2006

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Malaria parasites of the genus Plasmodium make a hazardous journey through their mosquito vectors. The majority die in the process, many as a result of the action of mosquito defence mechanisms. The mosquito too is not unscathed by the encounter with these parasites. Tissue damage occurs as a result of mid-gut invasion and reproductive fitness is lost when many developing ovarian follicles are resorbed. Here we discuss some of the mechanisms that are involved in killing the parasite and in the self-defence mechanisms employed by the mosquito to repair the mid-gut epithelium and to manipulate resources altering the trade-off position that balances reproduction and survival. In all cases, cells die by apoptotic-like mechanisms. In the midgut cells, apoptosis-induction pathways are being elucidated, the molecules involved in apoptosis are being recognised and Drosophila homologues sought. The death of ookinetes in the mosquito mid-gut lumen is associated with caspase-like activity and, although homologues of mammalian caspases are not present in the malaria genome, other cysteine proteases that are potential candidates have been discussed. In the ovary, apoptosis of patches of follicular epithelial cells is followed by resorption of the developing follicle and a subsequent loss of egg production in that follicle.

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Induction of DNA synthesis in Anopheles albimanus tissue cultures in response to a Saccharomyces cerevisiae challenge

Hernández‐Martínez

Román-Martínez

Martínez-Barnetche

et al. 2006

Arch Insect Biochem Physiol

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DNA synthesis was detected by the incorporation of 5-bromo-2' deoxy-uridine (BrdU) in adult Anopheles albimanus organs in culture in response to a challenge with Saccharomyces cerevisiae. Abdomens of mosquitoes inoculated with Roswell Park Memorial Institute medium (RPMI, control) or yeast were cultivated in RPMI plus ConA and BrdU for 5 days. DNA was obtained by phenolic extraction and the incorporated BrdU was quantified by ELISA using anti-BrdU peroxidase-labeled antibodies. Abdomen tissues of mosquitoes inoculated with yeast showed higher DNA synthesis than controls. Organs from untreated mosquitoes cultured in the presence of zymosan also synthesized DNA but at a lower level than tissues from yeast-inoculated mosquitoes. In similar experiments, DNA synthesis was inhibited by the addition of colchicine. DNA synthesis, evidenced by epifluorescence using an anti-BrdU fluorescein-labeled antibody, occurred in fat body, epithelial cells in pleural membranes, and the dorsal vessel. Pleural membranes showed the highest number of labeled cells. These tissues were also labeled with anti-PCNA (proliferating cell nuclear antigen) antibodies, two of which were able to produce polytene chromosomes under yeast stimulation. These results demonstrate that different An. albimanus tissues undergo DNA synthesis in response to foreign particles.

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Plasmodium berghei ookinetes induce nitric oxide production in Anopheles pseudopunctipennis midguts cultured in vitro

Cited by 40 publications

References 35 publications

Prostaglandin E₂ modulates the expression of antimicrobial peptides in the fat body and midgut of Anopheles albimanus

Prostaglandin E₂ modulates the expression of antimicrobial peptides in the fat body and midgut of Anopheles albimanus

Apoptosis-like death as a feature of malaria infection in mosquitoes

Induction of DNA synthesis in Anopheles albimanus tissue cultures in response to a Saccharomyces cerevisiae challenge

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Plasmodium berghei ookinetes induce nitric oxide production in Anopheles pseudopunctipennis midguts cultured in vitro

Cited by 40 publications

References 35 publications

Prostaglandin E2 modulates the expression of antimicrobial peptides in the fat body and midgut of Anopheles albimanus

Prostaglandin E2 modulates the expression of antimicrobial peptides in the fat body and midgut of Anopheles albimanus

Apoptosis-like death as a feature of malaria infection in mosquitoes

Induction of DNA synthesis in Anopheles albimanus tissue cultures in response to a Saccharomyces cerevisiae challenge

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Prostaglandin E₂ modulates the expression of antimicrobial peptides in the fat body and midgut of Anopheles albimanus

Prostaglandin E₂ modulates the expression of antimicrobial peptides in the fat body and midgut of Anopheles albimanus