114 research outputs found

    TGF-beta 1 induces human alveolar epithelial to mesenchymal cell transition (EMT)

    Get PDF
    Background: Fibroblastic foci are characteristic features in lung parenchyma of patients with idiopathic pulmonary fibrosis (IPF). They comprise aggregates of mesenchymal cells which underlie sites of unresolved epithelial injury and are associated with progression of fibrosis. However, the cellular origins of these mesenchymal phenotypes remain unclear. We examined whether the potent fibrogenic cytokine TGF-β1 could induce epithelial mesenchymal transition (EMT) in the human alveolar epithelial cell line, A549, and investigated the signaling pathway of TGF-β1-mediated EMT. Methods: A549 cells were examined for evidence of EMT after treatment with TGF-β1. EMT was assessed by: morphology under phase-contrast microscopy; Western analysis of cell lysates for expression of mesenchymal phenotypic markers including fibronectin EDA (Fn-EDA), and expression of epithelial phenotypic markers including E-cadherin (E-cad). Markers of fibrogenesis, including collagens and connective tissue growth factor (CTGF) were also evaluated by measuring mRNA level using RT-PCR, and protein by immunofluorescence or Western blotting. Signaling pathways for EMT were characterized by Western analysis of cell lysates using monoclonal antibodies to detect phosphorylated Erk1/2 and Smad2 after TGF-β1 treatment in the presence or absence of MEK inhibitors. The role of Smad2 in TGF-β1-mediated EMT was investigated using siRNA. Results: The data showed that TGF-β1, but not TNF-α or IL-1β, induced A549 cells with an alveolar epithelial type II cell phenotype to undergo EMT in a time-and concentration-dependent manner. The process of EMT was accompanied by morphological alteration and expression of the fibroblast phenotypic markers Fn-EDA and vimentin, concomitant with a downregulation of the epithelial phenotype marker E-cad. Furthermore, cells that had undergone EMT showed enhanced expression of markers of fibrogenesis including collagens type I and III and CTGF. MMP-2 expression was also evidenced. TGF-β1-induced EMT occurred through phosphorylation of Smad2 and was inhibited by Smad2 gene silencing; MEK inhibitors failed to attenuate either EMT-associated Smad2 phosphorylation or the observed phenotypic changes. Conclusion: Our study shows that TGF-β1 induces A549 alveolar epithelial cells to undergo EMT via Smad2 activation. Our data support the concept of EMT in lung epithelial cells, and suggest the need for further studies to investigate the phenomenon

    PPAR-γ Ligands Repress TGFβ-Induced Myofibroblast Differentiation by Targeting the PI3K/Akt Pathway: Implications for Therapy of Fibrosis

    Get PDF
    Transforming growth factor beta (TGFβ) induced differentiation of human lung fibroblasts to myofibroblasts is a key event in the pathogenesis of pulmonary fibrosis. Although the typical TGFβ signaling pathway involves the Smad family of transcription factors, we have previously reported that peroxisome proliferator-activated receptor-γ (PPAR-γ) ligands inhibit TGFβ-mediated differentiation of human lung fibroblasts to myofibroblasts via a Smad-independent pathway. TGFβ also activates the phosphatidylinositol 3 kinase/protein kinase B (PI3K/Akt) pathway leading to phosphorylation of AktS473. Here, we report that PPAR-γ ligands, 2-cyano-3,12-dioxooleana-1,9-dien-28-oic acid (CDDO) and 15-deoxy-(12,14)-15d-prostaglandin J2 (15d-PGJ2), inhibit human myofibroblast differentiation of normal and idiopathic pulmonary fibrotic (IPF) fibroblasts, by blocking Akt phosphorylation at Ser473 by a PPAR-γ-independent mechanism. The PI3K inhibitor LY294002 and a dominant-negative inactive kinase-domain mutant of Akt both inhibited TGFβ-stimulated myofibroblast differentiation, as determined by Western blotting for α-smooth muscle actin and calponin. Prostaglandin A1 (PGA1), a structural analogue of 15d-PGJ2 with an electrophilic center, also reduced TGFβ-driven phosphorylation of Akt, while CAY10410, another analogue that lacks an electrophilic center, did not; implying that the activity of 15d-PGJ2 and CDDO is dependent on their electrophilic properties. PPAR-γ ligands inhibited TGFβ-induced Akt phosphorylation via both post-translational and post-transcriptional mechanisms. This inhibition is independent of MAPK-p38 and PTEN but is dependent on TGFβ-induced phosphorylation of FAK, a kinase that acts upstream of Akt. Thus, PPAR-γ ligands inhibit TGFβ signaling by affecting two pro-survival pathways that culminate in myofibroblast differentiation. Further studies of PPAR-γ ligands and small electrophilic molecules may lead to a new generation of anti-fibrotic therapeutics

    Growth factor restriction impedes progression of wound healing following cataract surgery: identification of VEGF as a putative therapeutic target

    Get PDF
    Secondary visual loss occurs in millions of patients due to a wound-healing response, known as posterior capsule opacification (PCO), following cataract surgery. An intraocular lens (IOL) is implanted into residual lens tissue, known as the capsular bag, following cataract removal. Standard IOLs allow the anterior and posterior capsules to become physically connected. This places pressure on the IOL and improves contact with the underlying posterior capsule. New open bag IOL designs separate the anterior capsule and posterior capsules and further reduce PCO incidence. It is hypothesised that this results from reduced cytokine availability due to greater irrigation of the bag. We therefore explored the role of growth factor restriction on PCO using human lens cell and tissue culture models. We demonstrate that cytokine dilution, by increasing medium volume, significantly reduced cell coverage in both closed and open capsular bag models. This coincided with reduced cell density and myofibroblast formation. A screen of 27 cytokines identified nine candidates whose expression profile correlated with growth. In particular, VEGF was found to regulate cell survival, growth and myofibroblast formation. VEGF provides a therapeutic target to further manage PCO development and will yield best results when used in conjunction with open bag IOL designs

    Serotonin and corticosterone rhythms in mice exposed to cigarette smoke and in patients with COPD:implication for COPD-associated neuropathogenesis

    Get PDF
    The circadian timing system controls daily rhythms of physiology and behavior, and disruption of clock function can trigger stressful life events. Daily exposure to cigarette smoke (CS) can lead to alteration in diverse biological and physiological processes. Smoking is associated with mood disorders, including depression and anxiety. Patients with chronic obstructive pulmonary disease (COPD) have abnormal circadian rhythms, reflected by daily changes in respiratory symptoms and lung function. Corticosterone (CORT) is an adrenal steroid that plays a considerable role in stress and anti-inflammatory responses. Serotonin (5-hydroxytryptamine; 5HT) is a neurohormone, which plays a role in sleep/wake regulation and affective disorders. Secretion of stress hormones (CORT and 5HT) is under the control of the circadian clock in the suprachiasmatic nucleus. Since smoking is a contributing factor in the development of COPD, we hypothesize that CS can affect circadian rhythms of CORT and 5HT secretion leading to sleep and mood disorders in smokers and patients with COPD. We measured the daily rhythms of plasma CORT and 5HT in mice following acute (3 d), sub-chronic (10 d) or chronic (6 mo) CS exposure and in plasma from non-smokers, smokers and patients with COPD. Acute and chronic CS exposure affected both the timing (peak phase) and amplitude of the daily rhythm of plasma CORT and 5HT in mice. Acute CS appeared to have subtle time-dependent effects on CORT levels but more pronounced effects on 5HT. As compared with CORT, plasma 5HT was slightly elevated in smokers but was reduced in patients with COPD. Thus, the effects of CS on plasma 5HT were consistent between mice and patients with COPD. Together, these data reveal a significant impact of CS exposure on rhythms of stress hormone secretion and subsequent detrimental effects on cognitive function, depression-like behavior, mood/anxiety and sleep quality in smokers and patients with COPD

    Micro-computed tomography of pulmonary fibrosis in mice induced by adenoviral gene transfer of biologically active transforming growth factor-β1

    Get PDF
    <p>Abstract</p> <p>Background</p> <p>Micro-computed tomography (micro-CT) is a novel tool for monitoring acute and chronic disease states in small laboratory animals. Its value for assessing progressive lung fibrosis in mice has not been reported so far. Here we examined the importance of in vivo micro-CT as non-invasive tool to assess progression of pulmonary fibrosis in mice over time.</p> <p>Methods</p> <p>Pulmonary fibrosis was induced in mice by intratracheal delivery of an adenoviral gene vector encoding biologically active TGF-ß1 (AdTGF-ß1). Respiratory gated and ungated micro-CT scans were performed at 1, 2, 3, and 4 weeks post pulmonary adenoviral gene or control vector delivery, and were then correlated with respective histopathology-based Ashcroft scoring of pulmonary fibrosis in mice. Visual assessment of image quality and consolidation was performed by 3 observers and a semi-automated quantification algorithm was applied to quantify aerated pulmonary volume as an inverse surrogate marker for pulmonary fibrosis.</p> <p>Results</p> <p>We found a significant correlation between classical Ashcroft scoring and micro-CT assessment using both visual assessment and the semi-automated quantification algorithm. Pulmonary fibrosis could be clearly detected in micro-CT, image quality values were higher for respiratory gated exams, although differences were not significant. For assessment of fibrosis no significant difference between respiratory gated and ungated exams was observed.</p> <p>Conclusions</p> <p>Together, we show that micro-CT is a powerful tool to assess pulmonary fibrosis in mice, using both visual assessment and semi-automated quantification algorithms. These data may be important in view of pre-clinical pharmacologic interventions for the treatment of lung fibrosis in small laboratory animals.</p

    Microarray identifies ADAM family members as key responders to TGF-β1 in alveolar epithelial cells

    Get PDF
    The molecular mechanisms of Idiopathic Pulmonary Fibrosis (IPF) remain elusive. Transforming Growth Factor beta 1(TGF-β1) is a key effector cytokine in the development of lung fibrosis. We used microarray and computational biology strategies to identify genes whose expression is significantly altered in alveolar epithelial cells (A549) in response to TGF-β1, IL-4 and IL-13 and Epstein Barr virus. A549 cells were exposed to 10 ng/ml TGF-β1, IL-4 and IL-13 at serial time points. Total RNA was used for hybridisation to Affymetrix Human Genome U133A microarrays. Each in vitro time-point was studied in duplicate and an average RMA value computed. Expression data for each time point was compared to control and a signal log ratio of 0.6 or greater taken to identify significant differential regulation. Using normalised RMA values and unsupervised Average Linkage Hierarchical Cluster Analysis, a list of 312 extracellular matrix (ECM) proteins or modulators of matrix turnover was curated via Onto-Compare and Gene-Ontology (GO) databases for baited cluster analysis of ECM associated genes. Interrogation of the dataset using ontological classification focused cluster analysis revealed coordinate differential expression of a large cohort of extracellular matrix associated genes. Of this grouping members of the ADAM (A disintegrin and Metalloproteinase domain containing) family of genes were differentially expressed. ADAM gene expression was also identified in EBV infected A549 cells as well as IL-13 and IL-4 stimulated cells. We probed pathologenomic activities (activation and functional activity) of ADAM19 and ADAMTS9 using siRNA and collagen assays. Knockdown of these genes resulted in diminished production of collagen in A549 cells exposed to TGF-β1, suggesting a potential role for these molecules in ECM accumulation in IPF

    Androgen deprivation modulates the inflammatory response induced by irradiation

    Get PDF
    <p>Abstract</p> <p>Background</p> <p>The aim of this study was to determine whether radiation (RT)-induced inflammatory responses and organ damage might be modulated by androgen deprivation therapies.</p> <p>Methods</p> <p>The mRNA and tissue sections obtained from the lungs, intestines and livers of irradiated mice with or without androgen deprivation were analyzed by real-time PCR and histological analysis. Activation of NF-kappa B was examined by measuring nuclear protein levels in the intestine and lung 24 h after irradiation. We also examined the levels of cyclooxygenase-2 (COX-2), TGF-β1 and p-AKT to elucidate the related pathway responsible to irradiation (RT) -induced fibrosis.</p> <p>Results</p> <p>We found androgen deprivation by castration significantly augmented RT-induced inflammation, associated with the increase NF-κB activation and COX-2 expression. However, administration of flutamide had no obvious effect on the radiation-induced inflammation response in the lung and intestine. These different responses were probably due to the increase of RT-induced NF-κB activation and COX-2 expression by castration or lupron treatment. In addition, our data suggest that TGF-β1 and the induced epithelial-mesenchymal transition (EMT) via the PI3K/Akt signaling pathway may contribute to RT-induced fibrosis.</p> <p>Conclusion</p> <p>When irradiation was given to patients with total androgen deprivation, the augmenting effects on the RT-induced inflammation and fibrosis should take into consideration for complications associated with radiotherapy.</p

    Caffeic acid phenethyl ester decreases acute pneumonitis after irradiation in vitro and in vivo

    Get PDF
    BACKGROUND: Lung cancer is relatively resistant to radiation treatment and radiation pneumonitis is a major obstacle to increasing the radiation dose. We previously showed that Caffeic acid phenethyl ester (CAPE) induces apoptosis and increases radiosensitivity in lung cancer. To determine whether CAPE, an antioxidant and an inhibitor of NF-kappa B, could be a useful adjuvant agent for lung cancer treatment, we examine the effects of CAPE on irradiated normal lung tissue in this study. METHODS: We compared the effects of CAPE on cytotoxicity and intracellular oxidative stress in normal lung fibroblast and a lung cancer cell line. For in vivo analysis, whole thorax radiation (single dose 10 Gy and 20 Gy) was delivered to BALB/c male mice with or without CAPE pretreatment. NF- kappaB activation and the expression levels of acute inflammatory cytokines were evaluated in mice after irradiation. RESULTS: The in vitro studies showed that CAPE cause no significant cytotoxicity in normal lung as compared to lung cancer cells. This is probably due to the differential effect on the expression of NF-kappa B between normal and malignant lung cells. The results from in vivo study showed that CAPE treatment decreased the expression of inflammatory cytokines including IL-1 alpha and beta, IL-6, TNF-alpha and TGF- beta, after irradiation. Moreover, histological and immunochemical data revealed that CAPE decreased radiation- induced interstitial pneumonitis and TGF-beta expression. CONCLUSION: This study suggests that CAPE decreases the cascade of inflammatory responses induced by thoracic irradiation without causing toxicity in normal lung tissue. This provides a rationale for combining CAPE and thoracic radiotherapy for lung cancer treatment in further clinical studies

    How a slow-ovipositing parasitoid can succed as a biological control agent of the invasive mealybug Phenacoccus peruvianus: implications for future classical and conservation biological control programs

    Full text link
    [EN] Phenaccocus peruvianus Granara de Willink (Hemiptera: pseudococcidae) is an invasive mealybug that has become a pest of ornamental plants in Europe and has recently been detected in California, USA. In this work, we studied the tritrophic interaction among this mealybug, its main parasitoid Acerophagus n. sp. near coccois (Hymenoptera: Encyrtidae) and tending ants to disclose the success of this parasitoid controlling P. peruvianus. Acerophagus n. sp. near coccois accepted mealybugs for parasitism regardless of their size but did not hostfeed. We recorded three active defenses of P. peruvianus. Host handling time-consuming process that required more than 30 min. Tending ants, Lasius grandis (Hymenoptera: Encyrtidae), reduced the time spent by parasitoids in a patch and disrupted oviposition attempts. The low numbers of ants tending mealybugs colonies in Spain and France could explain why this parasitoid, with a long handling time, is an efficient biological control agent for P. peruvianus.Beltrà Ivars, A.; Soto Sánchez, AI.; Tena Barreda, A. (2015). How a slow-ovipositing parasitoid can succed as a biological control agent of the invasive mealybug Phenacoccus peruvianus: implications for future classical and conservation biological control programs. BioControl. 60(4):473-484. https://doi.org/10.1007/s10526-015-9663-6S473484604Arakelian G (2013) Bougainvillea mealybug (Phenacoccus peruvianus). Factsheet 2013. County of Los Angeles. Department of agricultural commissioner/weights and measures, USABartlett BR (1961) The influence of ants upon parasites, predators, and scale insects. Ann Entomol Soc Am 54:543–551Bartlett BR (1978) Pseudococcidae. In: Clausen CP (ed) Introduced parasites and predators of arthropod pests and weeds: a world review, 1st edn. Agricultural Research Service USDA, Washington, USA, pp 137–170Barzman MS, Daane KM (2001) Host-handling behaviors in parasitoids of black scale, Saissetia oleae (Homoptera: Coccidae): a case for ant-mediated evolution. J Anim Ecol 70:237–247Beltrà A, Soto A, Germain JF, Matile-Ferrero D, Mazzeo G, Pellizzari G, Russo A, Franco JC, Williams DJ (2010) The Bougainvillea mealybug Phenacoccus peruvianus, a rapid invader from South America to Europe. Entomol Hell 19:137–143Beltrà A, Garcia-Marí F, Soto A (2013a) Seasonal phenology, spatial distribution, and sampling plan for the invasive mealybug Phenacoccus peruvianus (Hemiptera: Pseudococcidae). J Econ Entomol 106:1486–1494Beltrà A, Tena A, Soto A (2013b) Fortuitous biological control of the invasive mealybug Phenacoccus peruvianus in Southern Europe. BioControl 58:309–317Beltrà A, Tena A, Soto A (2013c) Reproductive strategies and food sources used by Acerophagus n. sp. near coccois, a new successful parasitoid of the invasive mealybug Phenacoccus peruvianus. J Pest Sci 86:253–259Berlinger MJ, Golberg AM (1978) The effect of the fruit sepals on the citrus mealybug population and on its parasite. Entomol Exp Appl 24:238–243Blumstein DT, Daniel JC (2007) Quantifying behavior the JWatcher way. Sinauer Associates Inc., Sunderland, UKBoavida C, Ahounou M, Vos M, Neuenschwander P, van Alphen JJM (1995) Host stage selection and sex allocation by Gyranusoidea tebygi (Hymenoptera: Encyrtidae), a parasitoid of the mango mealybug, Rastrococcus invadens (Homoptera: Pseudococcidae). Biol Control 5:487–496Bokonon-Ganta AH, Neuenschwander P, van Alphen JJM, Vos M (1995) Host stage selection and sex allocation by Anagyrus mangicola (Hymenoptera: Encyrtidae), a parasitoid of the mango mealybug, Rastrococcus invadens (Homoptera: Pseudococcidae). Biol Control 5:479–486Bugila AAA, Franco JC, Borges da Silva E, Branco M (2014a) Defense response of native and alien mealybugs (Hemiptera: Pseudococcidae) against the solitary parasitoid Anagyrus sp. nr. pseudococci (Girault) (Hymenoptera: Encyrtidae). J Insect Behav 27:439–453Bugila AAA, Branco M, Borges da Silva E, Franco JC (2014b) Host selection behavior and specificity of the solitary parasitoid of mealybugs Anagyrus sp. nr. pseudococci (Girault) (Hymenoptera, Encyrtidae). Biocontrol Sci Techn 24:22–38Bynum EK (1937) Pseudococcobius terryi Fullaway, a Hawaiian parasite of Gray Sugarcane mealybug in the United States. J Econ Entomol 30:756–761Cadée N, van Alphen JJM (1997) Host selection and sex allocation in Leptomastidea abnormis, a parasitoid of the citrus mealybug Planococcus citri. Entomol Exp Appl 83:277–284Clausen CP (1924) The parasites of Pseudococcus maritimus (Ehrhorn) in California (Hymenoptera, Chalcidoidea). Part II. Biological studies and life histories. UC Pub Entomol 3:253–288Daane KM, Barzman MS, Caltagirone LE, Hagen KS (2000) Metaphycus anneckei and Metaphycus hageni: two discrete species parasitic on black scale, Saissetia oleae. BioControl 45:269–284Daane KM, Bentley WJ, Walton VM, Malakar-Kuenen R, Millar JC, Ingels CA, Weber EA, Gispert C (2006) New controls investigated for vine mealybug. Calif Agric 60:31–38Daane KM, Sime KR, Fallon J, Cooper ML (2007) Impacts of Argentine ants on mealybugs and their natural enemies in California’s coastal vineyards. Ecol Entomol 32:583–596De Farias AM, Hopper KR (1999) Oviposition behavior of Aphelinus asychis (Hymenoptera: Aphelinidae) and Aphidius matricariae (Hymenoptera: Aphidiidae) and defense behavior of their host Diuraphis noxia (Homoptera: Aphididae). Environ Entomol 28:858–862Dorn B, Mattiacci L, Bellotti AC, Dorn S (2001) Host specificity and comparative foraging behavior of Aenasius vexans and Acerophagus coccois, two endo-parasitoids of the cassava mealybug. Entomol Exp Appl 99:331–339Eisner T, Silberglied RE (1988) A chrysopid larva that cloaks itself in mealybug wax. Psyche 95:15–20Flanders SE (1963) Predation by parasitic Hymenoptera, the basis of ant-induced outbreaks of a host species. J Econ Entomol 56:116Foldi I (1983) Structure et fonctions des glandes tégumentaires de cochenilles Pseudococcines et de leurs secretions. Ann Soc Entomol Fr 19:155–156Foldi I (1997) Defense strategies in scale insects: phylogenetic inference and evolutionary scenarios (Hemiptera, Coccoidea). In: Grandcolas P (ed) The origin of biodiversity in insects: phylogenetic tests of evolutionary scenarios, 1st edn. Muséum National d’Histoire Naturelle, Paris, France, pp 203–230Godfray HCJ (1994) Parasitoids: behavioral and evolutionary ecology. Princeton University Press, Princeton, USAGonzález-Hernández H, Johnson MW, Reimer NJ (1999) Impact of Pheidole megacephala (F.) (Hymenoptera: Formicidae) on the biological control of Dysmicoccus brevipes (Cockerell) (Homoptera: Pseudococcidae). Biol Control 15:145–152Gross P (1993) Insect behavioral and morphological defenses against parasitoids. Annu Rev Entomol 38:251–273Gullan PJ (1997) Relationships with ants. In: Ben-Dov Y, Hodgson CJ (eds) Soft scale insects—their biology natural enemies and control, 1st edn. Elsevier, Amsterdam, The Netherlands, pp 351–373Gullan PJ, Kosztarab M (1997) Adaptations in scale insects. Annu Rev Entomol 42:23–50Hcidari M, Jahan M (2000) A study of ovipositional behavior of Anagyrus pseudococci a parasitoid of mealybugs. J Agric Sci Technol 2:49–53Honda JY, Luck RF (1995) Scale morphology effects on feeding behavior and biological control potential of Rhyzobius lophanthae (Coleoptera: Coccinellidae). Ann Entomol Soc Am 88:441–450Joyce AL, Hoddle MS, Bellows TS, Gonzalez D (2001) Oviposition behavior of Coccidoxenoides peregrinus, a parasitoid of Planococcus ficus. Entomol Exp Appl 98:49–57Karamaouna F (1999) Biology of the parasitoids Leptomastix epona (Walker) and Pseudaphycus flavidulus (Brèthes) and behavioural interactions with the host mealybug Pseudococcus viburni (Signoret). Ph.D. Thesis, University of London, UK, p 333Karamaouna F, Copland MJ (2000) Oviposition behavior, influence of experience on host size selection, and niche overlap of the solitary Leptomastix epona and the gregarious Pseudaphycus flavidulus, two endoparasitoids of the mealybug Pseudococcus viburni. Entomol Exp Appl 97:301–308Klotz JH, Hansen L, Pospischil R, Rust M (2008) Urban ants of North America and Europe. Cornell University Press, Ithaca, USAMailleux AC, Deneubourg JL, Detrain C (2003) Regulation of ants foraging to resource productivity. P R Soc Lond B Bio 270:1609–1616Majerus ME, Sloggett JJ, Godeau JF, Hemptinne JL (2007) Interactions between ants and aphidophagous and coccidophagous ladybirds. Popul Ecol 49:15–27Mgocheki N, Addison P (2009) Interference of ants (Hymenoptera: Formicidae) with biological control of the vine mealybug Planococcus ficus (Signoret) (Hemiptera: Pseudococcidae). Biol Control 49:180–185Moore D (1988) Agents used for biological control of mealybugs (Pseudococcidae). Biocontrol News Inf 9:209–225Paris CI, Espadaler X (2009) Honeydew collection by the invasive garden ant Lasius neglectus versus the native ant L grandis. Arthropod Plant Interact 3:75–85Pekas A, Tena A, Aguilar A, Garcia-Marí F (2011) Spatio-temporal patterns and interactions with honeydew-producing Hemiptera of ants in a Mediterranean citrus orchard. Agric Forest Entomol 13:89–97Pennacchio F, Strand MR (2006) Evolution of developmental strategies in parasitic Hymenoptera. Annu Rev Entomol 51:233–258Pijls JW, Hofker KD, Staalduinen MJ, van Alphen JJM (1995) Interspecific host discrimination and competition in Apoanagyrus (Epidinocarsis) lopezi and A(E) diversicornis parasitoids of the cassava mealybug Phenacoccus manihoti. Ecol Entomol 20:326–332Robert Y (1987) Dispersion and migration. In: Minks AK, Harrewijn P (eds) Aphids—their biology, natural enemies and control, 1st edn. Elsevier, Amsterdam, The Netherlands, pp 299–313Sandanayaka WRM, Charles JG, Allan DJ (2009) Aspects of the reproductive biology of Pseudaphycus maculipennis (Hym: Encyrtidae), a parasitoid of obscure mealybug, Pseudococcus viburni (Hem: Pseudococcidae). Biol Control 48:30–35Sarkar D (2008) Lattice: multivariate data visualization with R. Springer, New York, USASime KR, Daane KM (2014) Rapid, non-discriminatory oviposition behaviors are favored in mealybug parasitoids when Argentine ants are present. Environ Entomol 43:995–1002Tena A, Garcia-Marí F (2008) Suitability of citricola scale Coccus pseudomagnoliarum (Hemiptera: Coccidae) as host of Metaphycus helvolus (Hymenoptera: Encyrtidae): Influence of host size and encapsulation. Biol Control 46:341–347Tena A, Hoddle CD, Hoddle MS (2013) Competition between honeydew producers in an ant–hemipteran interaction may enhance biological control of an invasive pest. Bull Entomol Res 103:714–723The R Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austriavan Driesche RG, Belloti A, Herrera CJ, Castello JA (1987a) Host preferences of two encyrtid parasitoids for the Columbian Phenacoccus spp. of cassava mealybugs. Entomol Exp Appl 43:261–266van Driesche RG, Belloti A, Herrera CJ, Castello JA (1987b) Host feeding and ovipositor insertion as sources of mortality in the mealybug Phenacoccus herreni caused by two encyrtids Epidinocarsis diversicornis and Acerophagus coccois. Entomol Exp Appl 44:97–100Vet LE, Dicke M (1992) Ecology of infochemical use by natural enemies in a tritrophic context. Annu Rev Entomol 37:141–172Völkl W, Woodring J, Fischer M, Lorenz MW, Hoffmann KH (1999) Ant-aphid mutualisms: the impact of honeydew production and honeydew sugar composition on ant preferences. Oecologia 118:483–491Wajnberg E (1989) Analysis of variations of handling-time in Trichogramma maidis. Entomophaga 34:397–407Way MJ (1963) Mutualism between ants and honeydew-producing Homoptera. Annu Rev Entomol 8:307–344Weiss MR (2006) Defecation behavior and ecology of insects. Annu Rev Entomol 51:635–661Wyckhuys KAG, Stone L, Desneux N, Hoelmer KA, Hopper KR, Heimpel GE (2008) Parasitism of the soybean aphid Aphis glycines by Binodoxys communis: the role of aphid defensive behavior and parasitoid reproductive performance. Bull Entomol Res 98:361–370Zain-ul-Abdin, Arif MJ, Suhail A, Gogi MD, Arshad M, Wakil W, Abbas SK, Altaf A, Shaina H, Manzoor A (2012) Molecular analysis of the venom of mealybug parasitoid Aenasius bambawalei Hayat (Hymenoptera: Encyrtidae). Pak Entomol 34:189–193Zinna G (1959) Specializzazione entomoparassitica negli Encyrtidae: studio morfologico etologico e fisiologico del Leptomastix dactylopii. Howard Boll Lab agr Filippo Silvestri 18:1–14
    corecore