ENDOCYTOSIS AND ITS INHIBITORS IN BASIDIOMYCETOUS FUNGUS RHIZOCTONIA SOLANI
Abstract
Endocytosis is a complex process of absorption from the external environment and further distribution within the cell of soluble substances, macromolecules, microparticles, and etc. which occurs with the participation of vesicles formed by the cytoplasmic membrane. Endocytosis in the cells of animals and humans is actively and successfully explored. Thus, the classification of this process in animals, based only on the characteristics of the formation of primary vesicles, includes up to ten different ways of endocytosis. Modern knowledge of endocytosis in mycelial fungi is not so extensive, so its study in this group of organisms is an actual and promising direction in fundamental and applied mycology. In the present work, we investigated the effect of six different inhibitors, acting both on the assembly of actin/tubulin cytoskeletons and on the formation of different types of endocytosis, on the dynamics of endocytosis in the phytopathogenic heterobasidial fungus Rhizoctonia solani The effect of inhibitors was evaluated by microscopic analysis of the mycelial cell absorption of a fluorescent marker of endocytosis AM4-64. As a result of the study, four types of inhibitor effects on R. solani endocytosis were revealed: from complete absence of action to severe suppression of different stages of fungal endocytosis. Four of the six inhibitors, used to inhibit endocytosis in animals and humans, have a suppressing effect on the endocytosis of the heterobasidial fungus R. solani, which indicates the conservative nature of individual mechanisms of endocytosis in the examined fungus and, possibly, in mycelial fungi as a whole. Various hypotheses on the principles of the action of the studied inhibitors on the endocytosis activity of fungi are proposed.
About the Authors
O. V. KamzolkinaRussian Federation
Department of Mycology and Algology, School of Biology
Leninskiye gory 1–12, Moscow, 119234, Russia
M. A. Кiselica
Russian Federation
Department of Mycology and Algology, School of Biology
Leninskiye gory 1–12, Moscow, 119234, Russia
O. A. Kudryavtseva
Russian Federation
Department of Mycology and Algology, School of Biology
Leninskiye gory 1–12, Moscow, 119234, Russia
O. V. Shtaer
Russian Federation
Department of Mycology and Algology, School of Biology
Leninskiye gory 1–12, Moscow, 119234, Russia
I. S. Mazheika
Russian Federation
Department of Mycology and Algology, School of Biology
Leninskiye gory 1–12, Moscow, 119234, Russia
ul. Gubkina 3, Moscow, 119333, Russia
References
1. Goode B.L., Eskin J.A., Wendland B. Actin and endocytosis in budding yeast // Genetics. 2015. Vol. 199. N 2. P. 315–358.
2. Tokarev A.A., Alfonso A., Segev N. Overview of intracellular compartments and trafficking pathways // Trafficking inside cells: Pathways, mechanisms and regulation / Ed. N. Segev. N.Y.: Springer, 2009. P. 3–14.
3. Penalva M.A. Endocytosis in filamentous fungi: Cinderella gets her reward // Curr. Opin. Microbiol. 2010. Vol. 13. N 6. P. 684–692.
4. Dutta D., Donaldson J.G. Search for inhibitors of endocytosis // Cell Logist. 2012. Vol. 2. N 4. P. 203–208.
5. Fuchs U., Steinberg G. Endocytosis in the plant-pathogenic fungus Ustilago maydis // Protoplasma. 2005. Vol. 226. N 1–2. P. 75–80.
6. Toshima J.Y., Toshima J., Kaksonen M., Martin A.C., King D.S., Drubin D.G. Spatial dynamics of receptor-mediated endocytic trafficking in budding yeast revealed by using fluorescent alpha-factor derivatives // Proc. Natl. Acad. Sci. U. S. A. 2006. Vol. 103. N 15. P. 5793–5798.
7. Weinberg J., Drubin D.G. Clathrin-mediated endocytosis in budding yeast // Trends Cell. Biol. 2012. Vol. 22. N 1. P. 1–13.
8. Epp E., Nazarova E., Regan H., Douglas L.M., Konopka J.B., Vogel J., Whiteway M. Clathrin- and Arp2/3-independent endocytosis in the fungal pathogen Candida albicans // MBio. 2013. Vol. 4. N 5. e00476-13.
9. Wang D., Sletto J., Tenay B., Kim K. Yeast dynamin implicated in endocytic scission and the disassembly of endocytic components // Commun. Integr. Biol. 2011. Vol. 4. N 2. P. 178–181.
10. Prosser D.C., Drivas T.G., Maldonado-Baez L., Wendland B. Existence of a novel clathrin- independent endocytic pathway in yeast that depends on Rho1 and formin // J. Cell Biol. 2011. Vol. 195. N 4. P. 657–671.
11. Fischer-Parton S., Parton R.M., Hickey P.C., Dijksterhuis J., Atkinson H.A., Read N.D. Confocal microscopy of FM4-64 as a tool for analysing endocytosis and vesicle trafficking in living fungal hyphae // J. Microsc. 2000. Vol. 198. N 3. P. 246–259.
12. Lee M.T., Szeto C.Y., Ng T.P., Kwan H.S. Endocytosis in the shiitake mushroom Lentinula edodes and involvement of GTPase LeRAB7 // Eukaryot. Cell. 2007. Vol. 6. N 12. P. 2406–2418.
13. Takeshita N., Diallinas G., Fischer R. The role of flotillin FloA and stomatin StoA in the maintenance of apical sterolrich membrane domains and polarity in the filamentous fungus Aspergillus nidulans // Mol. Microbiol. 2012. Vol. 83. N 6. P. 1136–1152.
14. Masuo K., Higuchi Y., Kikuma T., Arioka M., Kitamoto K. Functional analysis of Abp1p- interacting proteins involved in endocytosis of the MCC component in Aspergillus oryzae // Fungal Genet. Biol. 2013. Vol. 56. P. 125–134.
15. Straube A., Brill M., Oakey B.R., Horio T., Steinberg G. Microtubule organization requires cell cycle-dependent nucleation at dispersed cytoplasmic sites: polar and perinuclear microtubule organizing centers in the plant pathogen Ustilago maydis // Mol. Biol. Cell. 2003. Vol. 14. N 2. P. 642–657.
16. Walther A., Wendland J. Apical localization of actin patches and vacuolar dynamics in Ashbya gossypii depend on the WASP homolog Wal1p // J. Cell Sci. 2004. Vol. 117. N 21. P. 4947–4958.
17. Aghamohammadzadeh S., Ayscough K.R. Differential requirements for actin during yeast and mammalian endocytosis // Nat. Cell Biol. 2009. Vol. 11. N 8. P. 1039–1042.
18. Schuster M., Lipowsky R., Assmann M.-A., Lenz P., Steinberg G. Transient binding of dynein controls bidirectional long-range motility of early endosomes // Proc. Natl. Acad. Sci. U. S. A. 2011. Vol. 108. N 9. P. 3618–3623.
19. Ivanov A.I. Pharmacological inhibition of endocytic pathways: is it specific enough to be useful? // Exocytosis and endocytosis. Methods Mol. Biol. Vol. 440. / Ed. A.I. Ivanov. N.Y.: Humana press, 2008. P. 15–33.
20. Doherty G.J., McMahon H.T. Mechanisms of endocytosis // Annu. Rev. Biochem. 2009. Vol. 78. P. 857–902.
21. Willox A.K., Sahraoui Y.M., Royle S.J. Non-specificity of Pitstop 2 in clathrin-mediated endocytosis // Biol. Open. 2014. Vol. 3. N 5. P. 326–331.
22. Girao H., Geli M.I., Idrissi F.Z. Actin in the endocytic pathway: from yeast to mammals // FEBS Lett. 2008. Vol. 582. N 14. P. 2112–2119.
23. von Kleist L., Stahlschmidt W., Bulut H. et al. Role of the clathrin terminal domain in regulating coated pit dynamics revealed by small molecule inhibition // Cell. 2011. Vol. 146. N 3. P. 471–484.
24. Steinberg G. Endocytosis and early endosome motility in filamentous fungi // Curr. Opin. Microbiol. 2014. Vol. 20. N 100. P. 10–18.
25. Niemann A., Baltes J., Els sser H.P. Fluorescence properties and staining behavior of monodansylpentane, a structural homologue of the lysosomotropic agent monodansylcadaverine // J. Histochem. Cytochem. 2001. Vol. 49. N 2. P. 177–185.
Review
For citations:
Kamzolkina O.V., Кiselica M.A., Kudryavtseva O.A., Shtaer O.V., Mazheika I.S. ENDOCYTOSIS AND ITS INHIBITORS IN BASIDIOMYCETOUS FUNGUS RHIZOCTONIA SOLANI. Vestnik Moskovskogo universiteta. Seriya 16. Biologiya. 2017;72(3):149-157. (In Russ.)