Protein Localization of Aquaporins in the Adult Female Disease Vector Mosquito,

Overview

Journal Front Insect Sci

Date 2024 May 3

PMID 38699443

Authors

Britney Picinic

Jean-Paul V Paluzzi

Andrew Donini

Affiliations

Soon will be listed here.

Abstract

The female mosquito is a vector for several arboviral diseases, due to their blood feeding behavior and their association with urban communities. While ion transport in has been studied, much less is known about mechanisms of water transport. Rapid water and ion excretion occurs in the adult female mosquito post blood meal and involves a set of organs including the midgut, Malpighian tubules (MTs), and hindgut. The MTs are responsible for the formation of primary urine and are considered the most important site for active transport of ions. Within the cells of the MTs, along with various ion transporters, there are aquaporin water channels that aid in the transport of water across the tubule cell membrane. Six aquaporin genes have been molecularly identified in (AQP1-6) and found to be responsible for the transport of water and in some cases, small solutes such as glycerol. In this study, we used immunohistochemistry to localize AaAQP1, 2, 4, 5, and 6 in the adult female , in non-blood fed and post blood feeding (0.5 and 24hr) conditions. We further examined the main water transporting aquaporin, AaAQP1, using western blotting to determine protein abundance changes in isolated MTs pre- and post-blood feeding. Using fluorescence hybridization, mRNA was found exclusively in the principal cells of female MTs. Finally, we used immunogold staining with transmission electron microscopy to determine subcellular localization of AaAQP1 in the Malpighian tubules under non-blood fed conditions. Interestingly, AaAQP1 was found to be predominantly in the principal cells of the MTs, dispersed throughout the brush border; however, there was also evidence of some AaAQP1 localization in the stellate cells of the MTs.

References

Hixson B, Bing X, Yang X, Bonfini A, Nagy P, Buchon N . A transcriptomic atlas of reveals detailed functional organization of major body parts and gut regional specializations in sugar-fed and blood-fed adult females. Elife. 2022; 11. PMC: 9113746. DOI: 10.7554/eLife.76132. View

Vega-Rua A, Zouache K, Girod R, Failloux A, Lourenco-de-Oliveira R . High level of vector competence of Aedes aegypti and Aedes albopictus from ten American countries as a crucial factor in the spread of Chikungunya virus. J Virol. 2014; 88(11):6294-306. PMC: 4093877. DOI: 10.1128/JVI.00370-14. View

Kandel Y, Pinch M, Lamsal M, Martinez N, Hansen I . Exploratory phosphoproteomics profiling of Aedes aegypti Malpighian tubules during blood meal processing reveals dramatic transition in function. PLoS One. 2022; 17(7):e0271248. PMC: 9269769. DOI: 10.1371/journal.pone.0271248. View

Holmes C, Brown E, Sharma D, Warden M, Pathak A, Payton B . Dehydration Alters Transcript Levels in the Mosquito Midgut, Likely Facilitating Rapid Rehydration following a Bloodmeal. Insects. 2023; 14(3). PMC: 10056721. DOI: 10.3390/insects14030274. View

Duchesne L, Hubert J, Verbavatz J, Thomas D, Pietrantonio P . Mosquito (Aedes aegypti ) aquaporin, present in tracheolar cells, transports water, not glycerol, and forms orthogonal arrays in Xenopus oocyte membranes. Eur J Biochem. 2003; 270(3):422-9. DOI: 10.1046/j.1432-1033.2003.03389.x. View

Sajadi F, Fernanda Vergara-Martinez M, Paluzzi J . The V-type H-ATPase is targeted in antidiuretic hormone control of the Malpighian "renal" tubules. Proc Natl Acad Sci U S A. 2023; 120(51):e2308602120. PMC: 10743368. DOI: 10.1073/pnas.2308602120. View

Piermarini P, Esquivel C, Denton J . Malpighian Tubules as Novel Targets for Mosquito Control. Int J Environ Res Public Health. 2017; 14(2). PMC: 5334665. DOI: 10.3390/ijerph14020111. View

Sreedharan S, Kothandan G, Sankaranarayanan K . Structural insights into the Aedes aegypti aquaporins and aquaglyceroporins - an in silico study. J Recept Signal Transduct Res. 2016; 36(6):543-557. DOI: 10.3109/10799893.2016.1141954. View

Pinch M, Mitra S, Rodriguez S, Li Y, Kandel Y, Dungan B . Fat and Happy: Profiling Mosquito Fat Body Lipid Storage and Composition Post-blood Meal. Front Insect Sci. 2024; 1:693168. PMC: 10926494. DOI: 10.3389/finsc.2021.693168. View

10.

Staniscuaski F, Paluzzi J, Real-Guerra R, Carlini C, Orchard I . Expression analysis and molecular characterization of aquaporins in Rhodnius prolixus. J Insect Physiol. 2013; 59(11):1140-50. DOI: 10.1016/j.jinsphys.2013.08.013. View

11.

Piermarini P, Dunemann S, Rouhier M, Calkins T, Raphemot R, Denton J . Localization and role of inward rectifier K(+) channels in Malpighian tubules of the yellow fever mosquito Aedes aegypti. Insect Biochem Mol Biol. 2015; 67:59-73. DOI: 10.1016/j.ibmb.2015.06.006. View

12.

Cui Y, Franz A . Heterogeneity of midgut cells and their differential responses to blood meal ingestion by the mosquito, Aedes aegypti. Insect Biochem Mol Biol. 2020; 127:103496. PMC: 7739889. DOI: 10.1016/j.ibmb.2020.103496. View

13.

Beyenbach K, Piermarini P . Transcellular and paracellular pathways of transepithelial fluid secretion in Malpighian (renal) tubules of the yellow fever mosquito Aedes aegypti. Acta Physiol (Oxf). 2010; 202(3):387-407. PMC: 3032036. DOI: 10.1111/j.1748-1716.2010.02195.x. View

14.

Wieczorek H, Beyenbach K, Huss M, Vitavska O . Vacuolar-type proton pumps in insect epithelia. J Exp Biol. 2009; 212(Pt 11):1611-9. PMC: 2683008. DOI: 10.1242/jeb.030007. View

15.

Patrick M, Aimanova K, Sanders H, Gill S . P-type Na+/K+-ATPase and V-type H+-ATPase expression patterns in the osmoregulatory organs of larval and adult mosquito Aedes aegypti. J Exp Biol. 2006; 209(Pt 23):4638-51. DOI: 10.1242/jeb.02551. View

16.

Drake L, Boudko D, Marinotti O, Carpenter V, Dawe A, Hansen I . The Aquaporin gene family of the yellow fever mosquito, Aedes aegypti. PLoS One. 2011; 5(12):e15578. PMC: 3014591. DOI: 10.1371/journal.pone.0015578. View

17.

Attardo G, Hansen I, Raikhel A . Nutritional regulation of vitellogenesis in mosquitoes: implications for anautogeny. Insect Biochem Mol Biol. 2005; 35(7):661-75. DOI: 10.1016/j.ibmb.2005.02.013. View

18.

Overend G, Cabrero P, Halberg K, Ranford-Cartwright L, Woods D, Davies S . A comprehensive transcriptomic view of renal function in the malaria vector, Anopheles gambiae. Insect Biochem Mol Biol. 2015; 67:47-58. DOI: 10.1016/j.ibmb.2015.05.007. View

19.

OConnor K, Beyenbach K . Chloride channels in apical membrane patches of stellate cells of Malpighian tubules of Aedes aegypti. J Exp Biol. 2001; 204(Pt 2):367-78. DOI: 10.1242/jeb.204.2.367. View

20.

Misyura L, Yerushalmi G, Donini A . A mosquito entomoglyceroporin, AQP5, participates in water transport across the Malpighian tubules of larvae. J Exp Biol. 2017; 220(Pt 19):3536-3544. DOI: 10.1242/jeb.158352. View