Golgi’s way: a long path toward the new paradigm of the intra-Golgi transport

Abstract

The transport of proteins and lipids is one of the main cellular functions. The vesicular model, compartment (or cisterna) maturation model, and the diffusion model compete with each other for the right to be the paradigm within the field of the intra-Golgi transport. These models have significant difficulties explaining the existing experimental data. Recently, we proposed the kiss-and-run (KAR) model of intra-Golgi transport (Mironov and Beznoussenko in Int J Mol Sci 13(6):6800-6819, 2012), which can be symmetric, when fusion and fission occur in the same location, and asymmetric, when fusion and fission take place at different sites. Here, we compare the ability of main models of the intra-Golgi transport to explain the existing results examining the evidence in favor and against each model. We propose that the KAR model has the highest potential for the explanation of the majority of experimental observations existing within the field of intracellular transport.

Transport of soluble proteins through the Golgi occurs by diffusion via continuities across cisternae

“…Albumin is an abundant, non-glycosylated protein, while antitrypsin is N-glycosylated. The trafficking of soluble proteins (albumin in most experiments) was characterized and compared with that of PC-I (Weinstock and Leblond, 1974; Bonfanti et al, 1998; Mironov et al, 2001) and vesicular stomatitis virus G protein (VSVG) (Bergmann and Singer, 1983; Mironov et al, 2001; Patterson et al, 2008), because these cargoes have been extensively characterized and shown to move by cisternal progression (or rimmal progression [Lavieu et al, 2013] or compartment progression [Mironov et al, 2013]. For the sake of brevity, from now onward we will use the term compartment progression to describe the traffic of procollagen and other similar cargo).…”

“…Continuity-mediated transport has been observed to occur between endosomes and lysosomes (Luzio et al, 2007), and also the exocytic release of cargo from secretory granules (Rutter and Hill, 2006) or synaptic vesicles through transient pores (kiss-and-run) (Rizzoli and Jahn, 2007; Alabi and Tsien, 2013) at the plasma membrane can be considered to occur via this modality. For intra-Golgi transport, this mechanism has been discussed several times in the past (Mellman and Simons, 1992; Weidman, 1995; Mironov et al, 1997; Marsh et al, 2004; Trucco et al, 2004; Mironov et al, 2005; Beznoussenko et al, 2007; Glick and Luini, 2011) and a few recent intra-Golgi transport models including the mixing–partitioning (Patterson et al, 2008), the kiss-and-run (Mironov and Beznoussenko, 2012; Fusella et al, 2013; Mironov et al, 2013) and the cisternal progenitor schemes (Pfeffer, 2010) have been proposed that imply transient tubular continuities across cisternae. At the molecular/mechanistic level, Golgi tubule formation has been proposed to be initiated by COPI coatomer-mediated budding (Yang et al, 2011), and tubule elongation and fission appear to require the actions of cytosolic phospholipase A2 (cPLA2) and lysophosphatidic acid acyltransferase-γ (LPAATγ), respectively (San Pietro et al, 2009) (Yang et al, 2011).…”

The Golgi apparatus: insights from filamentous fungi

“…The cisterna maturation model prevails, postulating that cisternae form de novo, change their identity over time, by acquiring next stage-determining molecules and by recycling back the earlier stage molecules and eventually dissipate in secretory carriers, while cargo progresses along with the maturing cisternae toward the locale for which it is destined. However, it has gradually become obvious that this model is insufficient to explain all experimental observations, leading to integration of modifications to its central theme (some excellent reviews on this debate can be found in Glick and Luini [2011] and Mironov et al [2013]. A condensed introduction to the field of Golgi biology can be found in Munro [2011b], while a detailed analysis of the status of Golgi research, up to some years ago, can be found in Mironov and Pavelka [2008b]).…”

Golgi apparatus dis- and reorganizations studied with the aid of 2-deoxy-d-glucose and visualized by 3D-electron tomography

“…Different transport mechanisms, including vesicular traffic, membrane maturation and transport via membrane continuities and contact sites, have been shown and apply to different types of cells, depending on the molecules and materials to be transported but are possibly active in the same cell side by side (e.g., Trucco et al 2004; Mironov et al 2013; Glick and Nakano 2009; Pfeffer 2013; Pellett et al 2013; Rizzo et al 2013; Lavieu et al 2013, 2014; Rothman 2014; Beznoussenko et al 2014, 2016; Lee et al 2014; Cheung et al 2015; Nakano 2015; Dancourt et al 2016). The reorganizations in response to 2DG show an increasing appearance of membrane continuities and connections, which start in the early phases of treatment with the occurrence of intra-stack networks and proceed with the formation and further remodeling of the Golgi bodies.…”