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Malpighamoeba infection compromises fluid secretion and P-glycoprotein detoxification in Malpighian tubules

  • 1.

    Maddrell, S. & Gardiner, B. Excretion of alkaloids by Malpighian tubules of insects. J. Exp. Biol. 64, 267–281 (1976).

    CAS  PubMed  Google Scholar 

  • 2.

    Després, L., David, J.-P. & Gallet, C. The evolutionary ecology of insect resistance to plant chemicals. Trends Ecol. Evol. 22, 298–307 (2007).

    PubMed  Article  Google Scholar 

  • 3.

    Goulson, D., Nicholls, E., Botías, C. & Rotheray, E. L. Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347, 1255957 (2015).

    PubMed  Article  CAS  Google Scholar 

  • 4.

    Richardson, L. L. et al. Secondary metabolites in floral nectar reduce parasite infections in bumblebees. Proc. R. Soc. B Biol. Sci. 282, 20142471 (2015).

    Article  Google Scholar 

  • 5.

    Manson, J. S., Otterstatter, M. C. & Thomson, J. D. Consumption of a nectar alkaloid reduces pathogen load in bumble bees. Oecologia 162, 81–89 (2010).

    ADS  PubMed  Article  Google Scholar 

  • 6.

    Alaux, C. et al. Interactions between Nosema microspores and a neonicotinoid weaken honeybees (Apis mellifera). Environ. Microbiol. 12, 774–782 (2010).

    PubMed  PubMed Central  Article  Google Scholar 

  • 7.

    Vidau, C. et al. Exposure to sublethal doses of fipronil and thiacloprid highly increases mortality of honeybees previously infected by Nosema ceranae. PLoS ONE 6, e21550 (2011).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 8.

    McMillan, L. E., Miller, D. W. & Adamo, S. A. Eating when ill is risky: immune defense impairs food detoxification in the caterpillar Manduca sexta. J. Exp. Biol. 221, jeb173336 (2018).

    PubMed  Article  Google Scholar 

  • 9.

    King, R. L. & Taylor, A. B. Malpighamœba locustae, n. sp. (Amoebidae), a protozoan parasitic in the Malpighian tubes of grasshoppers. Trans. Am. Microsc. Soc. 55, 6–10 (1936).

    Article  Google Scholar 

  • 10.

    Taylor, A. B. & King, R. L. Further studies on the parasitic amebae found in grasshoppers. Trans. Am. Microsc. Soc. 56, 172–176 (1937).

    Article  Google Scholar 

  • 11.

    Bailey, L. Honey bee pathology. Annu. Rev. Entomol. 13, 191–212 (1968).

    Article  Google Scholar 

  • 12.

    Harry, O. G. & Finlayson, L. H. Histopathology of secondary infections of Malpighamoeba locustae (Protozoa, Amoebidae) in the desert locust, Schistocerca gregaria (Orthoptera, Acrididae). J. Invertebr. Pathol. 25, 25–33 (1975).

    Article  Google Scholar 

  • 13.

    Harry, O. G. & Finlayson, L. H. The life-cycle, ultrastructure and mode of feeding of the locust amoeba Malpighamoeba locustae. Parasitology 72, 127 (1976).

    Article  Google Scholar 

  • 14.

    Liu, T. P. Scanning electron microscope observations on the pathological changes of Malpighian tubules in the worker honeybee, Apis mellifera, infected by Malpighamoeba mellificae. J. Invertebr. Pathol. 46, 125–132 (1985).

    Article  Google Scholar 

  • 15.

    Wright, S. H. & Dantzler, W. H. Molecular and cellular physiology of renal organic cation and anion transport. Physiol. Rev. 84, 987–1049 (2004).

    CAS  PubMed  Article  Google Scholar 

  • 16.

    Gaertner, L. S., Murray, C. L. & Morris, C. E. Transepithelial transport of nicotine and vinblastine in isolated Malpighian tubules of the tobacco hornworm (Manduca sexta) suggests a P-glycoprotein-like mechanism. J. Exp. Biol. 201, 2637–2645 (1998).

    CAS  PubMed  Google Scholar 

  • 17.

    Rheault, M. R., Plaumann, J. S. & O’Donnell, M. J. Tetraethylammonium and nicotine transport by the Malpighian tubules of insects. J. Insect Physiol. 52, 487–498 (2006).

    CAS  PubMed  Article  Google Scholar 

  • 18.

    Leader, J. P. & O’Donnell, M. J. Transepithelial transport of fluorescent p-glycoprotein and MRP2 substrates by insect Malpighian tubules: confocal microscopic analysis of secreted fluid droplets. J. Exp. Biol. 208, 4363–4376 (2005).

    CAS  PubMed  Article  Google Scholar 

  • 19.

    Rossi, M., De Battisti, D. & Niven, J. E. Transepithelial transport of P-glycoprotein substrate by the Malpighian tubules of the desert locust. PLoS ONE 14, e0223569 (2019).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 20.

    Dermauw, W. & Van Leeuwen, T. The ABC gene family in arthropods: comparative genomics and role in insecticide transport and resistance. Insect Biochem. Mol. Biol. 45, 89–110 (2014).

    CAS  PubMed  Article  Google Scholar 

  • 21.

    Eytan, G. D., Regev, R., Oren, G., Hurwitz, C. D. & Assaraf, Y. G. Efficiency of P-glycoprotein–mediated exclusion of rhodamine dyes from multidrug-resistant cells is determined by their passive transmembrane movement rate. Eur. J. Biochem. 248, 104–112 (1997).

    CAS  PubMed  Article  Google Scholar 

  • 22.

    Murray, C. L. A P-glycoprotein-like mechanism in the nicotine-resistant insect, Manduca sexta (University of Ottawa, Ottawa, 1996).

    Google Scholar 

  • 23.

    O’Donnell, M. Insect excretory mechanisms. Adv. Insect Physiol. 35, 1–122 (2008).

    Article  Google Scholar 

  • 24.

    Berridge, M. J. The physiology of excretion in the cotton stainer, Dysdercus fasciatus, Signoret. IV. Hormonal control of excretion. J. Exp. Biol. 44, 553–566 (1966).

    CAS  PubMed  Google Scholar 

  • 25.

    Ramsay, J. A. Active transport of water by the Malpighian tubules of the stick insect, Dixippus Morosus (Orthoptera, Phasmidae). J. Exp. Biol. 31, 104–113 (1954).

    CAS  Google Scholar 

  • 26.

    Maddrell, S. Active transport of water by insect Malpighian tubules. J. Exp. Biol. 207, 894–896 (2004).

    PubMed  Article  Google Scholar 

  • 27.

    Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671 (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 28.

    R Core Team. R: a language and environment for statistical computing (R Foundation for Statistical Computing, Vienna, Austria, 2019). https://www.R-project.org/.

  • 29.

    Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).

    Article  Google Scholar 

  • 30.

    Burnham, K. P. & Anderson, D. R. A practical information-theoretic approach. in Model Selection Multimodel Inference 2nd edn (Springer, New York, 2002).

  • 31.

    Maddrell, S. H. P. & O’Donnell, M. J. Insect Malpighian tubules: V-ATPase action in ion and fluid transport. J. Exp. Biol. 172, 417–429 (1992).

    CAS  PubMed  Google Scholar 

  • 32.

    Wieczorek, H., Beyenbach, K. W., Huss, M. & Vitavska, O. Vacuolar-type proton pumps in insect epithelia. J. Exp. Biol. 212, 1611–1619 (2009).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 33.

    Garrett, M. A., Bradley, T. J., Meredith, J. E. & Phillips, J. E. Ultrastructure of the Malpighian tubules of Schistocerca gregaria. J. Morphol. 195, 313–325 (1988).

    PubMed  Article  Google Scholar 

  • 34.

    Ugwu, M. C., Oli, A., Esimone, C. O. & Agu, R. U. Organic cation rhodamines for screening organic cation transporters in early stages of drug development. J. Pharmacol. Toxicol. Methods 82, 9–19 (2016).

    CAS  PubMed  Article  Google Scholar 

  • 35.

    Maddrell, S. H. P., Gardiner, B. O. C., Pilcher, D. E. M. & Reynolds, S. E. Active transport by insect Malpighian tubules of acidic dyes and of acylamides. J. Exp. Biol. 61, 357–377 (1974).

    CAS  PubMed  Google Scholar 

  • 36.

    Hinks, C. F. & Ewen, A. B. Pathological effects of the parasite Malameba locustae in males of the migratory grasshopper Melanoplus sanguinipes and its interaction with the insecticide, cypermethrin. Entomol. Exp. Appl. 42, 39–44 (1986).

    CAS  Article  Google Scholar 

  • 37.

    Sreeramulu, K., Liu, R. & Sharom, F. J. Interaction of insecticides with mammalian P-glycoprotein and their effect on its transport function. Biochim. Biophys. Acta BBA Biomembr. 1768, 1750–1757 (2007).

    CAS  Article  Google Scholar 

  • 38.

    Bernays, E. A. & Chapman, R. F. Plant chemistry and acridoid feeding behaviour. Biochem. Asp. Plant Anim. Coevol. 99, 41 (1978).

    Google Scholar 

  • 39.

    Habig, W. H., Pabst, M. J. & Jakoby, W. B. Glutathione S-transferases the first enzymatic step in mercapturic acid formation. J. Biol. Chem. 249, 7130–7139 (1974).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 40.

    Stahlschmidt, Z. R., Acker, M., Kovalko, I. & Adamo, S. A. The double-edged sword of immune defence and damage control: do food availability and immune challenge alter the balance?. Funct. Ecol. 29, 1445–1452 (2015).

    Article  Google Scholar 

  • 41.

    Jeschke, V., Gershenzon, J. & Vassão, D. G. A mode of action of glucosinolate-derived isothiocyanates: detoxification depletes glutathione and cysteine levels with ramifications on protein metabolism in Spodoptera littoralis. Insect Biochem. Mol. Biol. 71, 37–48 (2016).

    CAS  PubMed  Article  Google Scholar 

  • 42.

    Phillips, J. E. Rectal absorption in the desert locust, Schistocerca gregaria Forskal. I. Water. J. Exp. Biol. 41, 15–38 (1964).

    CAS  PubMed  Google Scholar 

  • 43.

    Phillips, J. Comparative physiology of insect renal function. Am. J. Physiol. Regul. Integr. Comp. Physiol. 241, R241–R257 (1981).

    CAS  Article  Google Scholar 

  • 44.

    Proux, J. Lack of responsiveness of Malpighian tubules to the AVP-like insect diuretic hormone on migratory locusts infected with the protozoan Malameba locustae. J. Invertebr. Pathol. 58, 353–361 (1991).

    CAS  Article  Google Scholar 

  • 45.

    Phillips, J. E. Rectal absorption in the desert locust, Schistocerca gregaria Forskal. II. Sodium, potassium and chloride. J. Exp. Biol. 41, 39–67 (1964).

    CAS  PubMed  Google Scholar 

  • 46.

    Misof, B. et al. Phylogenomics resolves the timing and pattern of insect evolution. Science 346, 763–767 (2014).

    ADS  CAS  PubMed  Article  Google Scholar 

  • 47.

    Venter, I. G. Egg development in the brown locust, Locustana pardalina (Walker), with special reference to the effect of infestation by Malameba locustae. South Afr. J. Agric. Sci. 9, 429–434 (1966).

    Google Scholar 


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