key: cord-016971-7esuj4ye authors: Mironov, Alexander A.; Pavelka, Margit title: The Golgi apparatus and main discoveries in the field of intracellular transport date: 2008 journal: The Golgi Apparatus DOI: 10.1007/978-3-211-76310-0_2 sha: doc_id: 16971 cord_uid: 7esuj4ye In this chapter, we summarize important findings in the field of intracellular transport, which have considerably contributed to the understanding of the function and organization of the Golgi apparatus (GA). It is not possible to mention all authors in this huge field. We apologize for gaps and incompleteness, and are thankful for suggestions and corrections. . The Golgi apparatus and main discoveries in the field of physiology of intracellular transport 1898 Discovery of the GA 1951 Confirmation of the presence of the GA (Dalton 1951) 1961 The regional distribution of the thiamine-pyrophosphatase activity within the GA (Novikoff and Goldfischer 1961) 1964 The trans ER (Novikoff 1964; Novikoff et al. 1964) 1964 GERL concept (Novikoff 1964) 1964 Isolation of Golgi membranes from cells (Morr e and Mollenhauer 1964) 1964 The process of sulphation in the GA (Godman and Lane 1964) 1966 The sugar-nucleotide transport from the cytosol to the Golgi lumen across the Golgi membranes, the role of the GA in glycosylation (Neutra and Leblond 1966) 1966 The origin of lysosomes and the function of clathrin-coated vesicles during protein absorption (Bainton and Farquhar 1966; Friend and Farquhar 1967) 1967 The intracellular transport (Jamieson and Palade 1967a,b) 1969 Galactosyltransferase as a Golgi marker (Whur et al. 1969; Morr e et al. 1969) 1976 Isolation of clathrin-coated vesicles (Pearse 1976 (Pearse ) 1977 The PM-to-Golgi transport of the endogenously added marker (Herzog and Farquhar 1977) 1980 M6P-mediated sorting of Golgi enzymes at the GA (Tabas and Kornfeld 1980) 1981 Clathrin-coated buds in the trans side of the GA (Griffiths et al. 1981) 1982 Immunocytochemical localization of galactosyltransferase Berger 1982) 1983 Topology of N-glycosylation (Dunphy and Rothman 1983) 1984 Reconstitution of intra-Golgi transport in vitro (Balch et al. 1984) 1984 The 15 C temperature block (Saraste and Kuismanen 1984) 1985 Clathrin-independent endocytosis (Moya et al. 1985; Sandvig et al. 1985 Sandvig et al. ) 1985 Sandvig et al. -1987 The mitotic form of the GA and mechanisms of mitotic Golgi transformation in animal cells (Featherstone et al. 1985; Lucocq et al. 1987 Lucocq et al. ) 1986 The COPI-coated vesicles and characterization of molecular mechanisms involved into the function of COPI coat (Orci et al. 1986; Serafini et al. 1991 Serafini et al. ) 1986 The structure and function of the TGN and the 20 C temperature block Simons 1986) 1987 KDEL-signal for the retention of luminally located proteins (Munro and Pelham 1987) 1989 BFA was applied for the study of intra-Golgi transport (Doms et al. 1989; Lippincott-Schwartz et al. 1989 ) 1990 SNAREs (Newman et al. 1990 ) 1990 The main genes involved in intracellular transport, the genetic evidence in favour of the vesicular model of the transport in yeast (Kaiser and Schekman 1990) 1991 A Golgi retention signal in the membrane-spanning domain (Swift and Machamer 1991) 1993 The role of oligomerization for the retention of Golgi enzymes (Weisz et al. 1993 (Weisz et al. ) 1993 The role of PM-derived signalling for intra -Golgi transport (De Matteis et al. 1993 Golgi matrix (Slusarewicz et al. 1994 ) and cis-Golgin, GM130 (Nakamura et al. 1995 ) 1994 COPI-dependent retrieval sorting signals (Cosson and Letourneur 1994) gaps (all authors quoted in the consecutive chapters deserve to be listed here). The list is open for suggestions. The development of the research in the field of intracellular transport has been comprehensively discussed in 1998 at the conference in Pavia devoted to the 100th anniversary of the Golgi discovery. Historically, the first mechanism that had been proposed for intracellular transport was the progression. The origin of the progression model (or the concept of cis-to-trans flow) links to Grasses name (1957) who proposed that the continuous formation of cis Golgi cisternae balances the conversion of trans one into secretory granules. However, the first experimental data in favour of the progression concept were obtained in 1971 (Franke et al. 1971) . In 1967, it has been demonstrated that proteins newly synthesized in the ER appeared, after a few minutes, not only over Golgi stacks but also over round profiles surrounding the GA and the conclusion that secretory proteins bypass the GA was made (Jamieson and Palade 1967a,b, 1968a,b) . Then, in 1981, the vesicular model replaced the progression model because the main support for the progression model, the cis-trans movement of scales in algae has been considered to be a rare formula connected with unusual geometry and size of the product (Farquhar and Palade 1981) . Ironically, the major supporting data for the vesicular model at that time was based on the isolation of Golgi-derived clathrin-coated vesicles (Rothman et al. 1980 ). However, after the discovery of coat protein I (COPI) (Orci et al. 1986 ), the vesicular model was changed, and instead of clathrin-dependent vesicles, COPI-dependent vesicles were proposed to serve as anterograde carriers. The strongest support for the vesicular model appeared from the experiments in yeast with the temperature sensitive Sec genes (Kaiser and Schekman 1990). The in vitro isolation of functional (containing VSVG and able to fuse with acceptor Golgi membranes) COPI-coated vesicles (Osterman et al. 1993 ) was interpreted as the second proof for the role of COPI-coated vesicles in the anterograde intra-Golgi transport. Importantly, however, that the first author of this paper later stressed, that actually, these data support the cisterna maturation model (Ostermann 2001) . On the other hand, it has also been demonstrated that 20 min after fusion of two (or more) cells (one cell is VSV-infected, another is a non-infected cell) and formation of a heterokaryon, VSVG seems to move from the GA derived from the infected cell to the GA derived from non-infected cells . These results were interpreted as confirmation of the ability of vesicular carriers to diffuse through the cytosol of the heterokaryon from one GA to another. However, later, the Rothman group (Orci et al. 1998) laid less emphasis on the heterokaryon experiments, suggesting that those observations appeared as a result of the treatment of cells with an acidic medium. Instead, the string theory was proposed, according to which a proteinaceous-like string links vesicles to cisternal elements and prevents budded vesicles from diffusing away, while still allowing them to diffuse laterally. With time, due to accumulation of contradictions, the current vesicular paradigm became less and less effective in the explanation of growing body of observations (Mironov et al. 1997) . As a result, the original version of the vesicular paradigm began to be modified not only by the opponents of the vesicular model but also by its authors and proponents (Orci et al. 1998) . In order to resolve accumulated contradictions within the field, almost simultaneously several groups (Bannykh and Balch 1997; Mironov et al. 1997; Glick et al. 1997; Schekman and Mellman 1997) have published the cisterna maturation-progression model based on the COPI vesicles-mediated Golgi enzyme recycling. The first experimental confirmation that large aggregated cargo, such as procollagen I, can be transported through the GA by maturation mechanism came in 1998 . Previous stereological observations in P. scheffelii suggesting that their scales being much too large to be packaged into vesicles are transported by the progression of Golgi cisternae towards the plasmalemma were published not in an original paper but in a review (Becker et al. 1995) and were not confirmed later because glycoprotein and polysaccharide synthesis are uncoupled during flagella regeneration (Perasso et al. 2000) . Next, it has been demonstrated (Mironov et al. 2001 ) that both diffusible and non-diffusible cargoes are transported in the same carriers through the Golgi stacks. It has been proved that vesicles are not transport carriers for cargo in the intra-Golgi transport not only in situ, but also in vitro, in cell-free assay (Happe and Weidman 1998) . After these publications, there was a short period when the cisterna maturation model became dominant. With time new contradictions not compatible with the cisterna maturation-progression model have accumulated (Mironov et al. 2005 ). The attempts to use transport models based on combination of basic principles were not successful (see Chapter 3.2). Therefore now, there is no consensus on the models of intra-Golgi transport. The existence of the maturation mechanism is almost finally established for the secretion of large polymeric structures incompatible in size with COPI-dependent vesicles in many types of cells and under the infection of some viruses. Jamieson JD, Palade GE (1967a) Intracellular transport of secretory proteins in the Application of GFP-technology for the study of the GA in living cells (Cole et al. 1996) 1996 Characterization of the ER exit sites Characterization of ER-to-Golgi transport carriers in living cells Characterization of post-Golgi transport carriers in living cells The role of endocytic TGN in the formation of the most-trans Golgi cisterna Tomographic reconstruction of the GA The concentration of regulatory secretory proteins within the Golgi cisternae The understanding of the evolution of small GTPases had changed the model of the Golgi evolution Characterization of Golgi-to-apical PM transport carriers in living cells Characterization of the Golgi-to-endosome carriers in living cells The role of GM130 in the maintenance of the Golgi ribbon The role of ER-to-Golgi transport in the maintenance of the Golgi ribbon Origin of granules in polymorphonuclear leukocytes. Two types derived from opposite faces of the Golgi complex in developing granulocytes Reconstitution of the transport of protein between successive compartments of the Golgi measured by the coupled incorporation of N-acetylglucosamine The organization of endoplasmic reticulum export complexes Membrane dynamics at the endoplasmic reticulum-Golgi interface COPII: a membrane coat formed by Sec proteins that drive vesicle budding from the endoplasmic reticulum Anterograde transport of algal scales through the Golgi complex is not mediated by vesicles The Golgi apparatus: from discovery to contemporary studies Procollagen traverses the Golgi stack without leaving the lumen of cisternae: evidence for cisternal maturation Diffusional mobility of Golgi proteins in membranes of living cells The Golgi apparatus and main discoveries * 11 Coatomer interaction with di-lysine endoplasmic reticulum retention motif Observations of the Golgi substance with the electron microscope Receptor and protein kinase C-mediated regulation of ARF binding to the Golgi complex AP-3: an adaptor-like protein complex with ubiquitous expression AP-4, a novel protein complex related to clathrin adaptors Brefeldin A redistributes resident and itinerant Golgi proteins to the endoplasmic reticulum Camillo Golgi and the discovery of the Golgi apparatus Compartmentation of asparagine-linked oligosaccharide processing in the Golgi apparatus The Golgi apparatus (complex)-(1954-1981)-from artifact to center stage Conserved structural features of the synaptic fusion complex: SNARE proteins reclassified as Q-and R-SNAREs Newly synthesized G protein of vesicular stomatitis virus is not transported to the Golgi complex in mitotic cells Synthesis and turnover of membrane proteins in rat liver: an examination of the membrane flow hypothesis Functions of coated vesicles during protein absorption in the rat vas deferens A cisternal maturation mechanism can explain the asymmetry of the Golgi stack On the site of sulfation in the chondrocyte Golgi C (1898a) Intorno alla struttura della cellula nervosa Sur la structure des cellules nerveuses des ganglions spinaux Grasse PP (1957) Ultrastructure, polarity and reproduction of Golgi apparatus The role of clathrin-coated vesicles in acrosome formation The trans Golgi network: sorting at the exit site of the Golgi complex Cell-free transport to distinct Golgi cisternae is compartment specific and ARF independent Luminal membrane retrieved after exocytosis reaches most Golgi cisternae in secretory cells Kinetic analysis of secretory protein traffic and characterization of Golgi to plasma membrane transport in living cells A C-terminal signal prevents secretion of luminal ER proteins Characterization of a cis-Golgi matrix protein, GM130 Radioautographic comparison of the uptake of galactose-H and glucose-H3 in the Golgi region of various cells secreting glycoproteins or mucopolysaccharides BET1, BOS1, and SEC22 are members of a group of interacting yeast genes required for transport from the endoplasmic reticulum to the Golgi complex Nucleosidediphosphatase activity in the Golgi apparatus and its usefulness for cytological studies GERL, its form and function in neurons of rat spinal ganglia Golgi apparatus and lysosomes The ER to Golgi interface is the major concentration site of secretory proteins in the exocrine pancreatic cell A new type of coated vesicular carrier that appears not to contain clathrin: its possible role in protein transport within the Golgi stack Vesicles on strings: morphological evidence for processive transport within the Golgi stack Stepwise assembly of functionally active transport vesicles Stoichiometry and kinetics of transport vesicle fusion with Golgi membranes Endocytic routes to the Golgi apparatus Clathrin: a unique protein associated with intracellular transfer of membrane by coated vesicles The Golgi apparatus of the scaly green flagellate Scherffelia dubia: uncoupling of glycoprotein and polysaccharide synthesis during flagellar regeneration Correlative light-electron microscopy reveals the tubular-saccular ultrastructure of carriers operating between Golgi apparatus and plasma membrane Ultrastructure of long-range transport carriers moving from the trans Golgi network to peripheral endosomes ER-to-Golgi transport visualized in living cells GM130 and GRASP65-dependent lateral cisternal fusion allows uniform Golgi-enzyme distribution Immunocytochemical localization of galactosyltransferase in HeLa cells: codistribution with thiamine pyrophosphatase in trans-Golgi cisternae Transport of the membrane glycoprotein of vesicular stomatitis virus to the cell surface in two stages by clathrincoated vesicles Intercompartmental transport in the Golgi complex is a dissociative process: facile transfer of membrane protein between two Golgi populations Effect of potassium depletion of cells on their sensitivity to diphtheria toxin and pseudomonas toxin Pre-and post-Golgi vacuoles operate in the transport of Semliki Forest virus membrane glycoproteins to the cell surface Visualization of ER-to-Golgi transport in living cells reveals a sequential mode of action for COPII and COPI Does COPI go both ways? ADP-ribosylation factor is a subunit of the coat of Golgi-derived COP-coated vesicles: a novel role for a GTP-binding protein Isolation of a matrix that binds medial Golgi enzymes A Golgi retention signal in a membrane-spanning domain of coronavirus E1 protein Biosynthetic intermediates of beta-glucuronidase contain high mannose oligosaccharides with blocked phosphate residues Secretory traffic triggers the formation of tubular continuities across Golgi sub-compartments Microtubuledependent transport of secretory vesicles visualized in real time with a GFP-tagged secretory protein Oligomerization of a membrane protein correlates with its retention in the Golgi complex Radioautographic visualization of the incorporation of galactose-3H and mannose-3H by rat thyroids in vitro in relation to the stages of thyroglobulin synthesis