Oskar-induced endocytic activation and actin remodeling for anchorage of the Drosophila germ plasm

Abstract

and akiran@cdb.riken.jp i n many animals, germ-cell fate is specified by inheritance of the germ plasm, which is enriched in maternal rnas and proteins. assembly of the drosophila germ (pole) plasm begins with the localization and translation of oskar (osk) rna at the oocyte posterior pole. osk rna produces two isoforms, long and short osk. short osk recruits other pole plasm components, and long osk restricts them to the oocyte cortex. although molecular functions of long osk remain mysterious, it is known to be involved in endocytic activation and actin cytoskeletal remodeling. We identified several vesicular trafficking machinery components that act downstream of long osk in pole plasm assembly. these included the rab5 effector protein rabenosyn-5 (rbsn-5) and the Golgi/endosomal protein mon2, both of which were crucial for osk-induced actin remodeling and the anchoring of pole plasm components. We propose that, in response to long osk, the rab5/rbsn-5-dependent endocytic pathway promotes the formation of specialized vesicles, and mon2 acts on these vesicles as a scaffold to instruct actin nucleators like cappuccino and spire to remodel the actin cytoskeleton, which anchors pole plasm components to the cortex. this mechanism may be applicable to the asymmetric localization of macromolecular structures such as protein-rna complexes in other systems. Drosophila Germ Plasm AssemblyThe assembly of the germ (pole) plasm in Drosophila oogenesis is a useful model

Long Oskar Controls Mitochondrial Inheritance in Drosophila melanogaster

“…Instead, it is known to be present on endosomes where it is thought to stimulate endocytosis together with Rab5 and Rbsn-5 (Tanaka and Nakamura, 2011). To determine how Long Oskar traps mitochondria at the posterior, we conducted co-immunoprecipitation experiments to identify Long Oskar interacting proteins by mass spectrometry.…”

“…Short Oskar is an integral member of germ plasm and is both necessary and sufficient to form functional PGCs (Ephrussi and Lehmann, 1992; Ewen-Campen et al, 2012; Smith et al, 1992). In stark contrast, Long Oskar is distinctly localized to endocytic membranes and is not required for PGC formation per se (Tanaka and Nakamura, 2011; Vanzo et al, 2007). Long Oskar may instead function to help anchor the germ plasm by promoting yolk endocytosis and remodeling of the actin cytoskeleton (Tanaka and Nakamura, 2011; Vanzo et al, 2007).…”

“…In stark contrast, Long Oskar is distinctly localized to endocytic membranes and is not required for PGC formation per se (Tanaka and Nakamura, 2011; Vanzo et al, 2007). Long Oskar may instead function to help anchor the germ plasm by promoting yolk endocytosis and remodeling of the actin cytoskeleton (Tanaka and Nakamura, 2011; Vanzo et al, 2007). Unexpectedly, we did not identify any endocytic proteins in our Long Oskar co-immunoprecipitation experiments (Table S2).…”

mRNA localization in theDrosophilagermline

“…23 At the posterior, the actin cytoskeleton, the actin binding proteins Lasp, Didum, Spire, Cappuccino, the Myosin-V motor, MTs and Dynein are all required for proper posterior accumulation and maintenance. [69][70][71][72][73][74][75] The involvement of both kinesin and Dynein in osk mRNA localization suggests that RNP particles are exposed to opposing directional forces during localization. How particles in vivo transition between plus and minus end movement remains unclear and an aim for future research.…”

BioArchitecture

“…In the Drosophila oocyte polarized endocytosis appears to result in specialized vesicles which act as vehicle for local action of actin regulators 19 . Evidence is also emerging that the spectrin-adducin membrane skeleton directly organizes the cortical actin filaments at adherens and tight junctions 20 .…”