Efficient Golgi Forward Trafficking Requires GOLPH3-Driven, PI4P-Dependent Membrane Curvature

Rahajeng, Juliati; Kuna, Ramya S.; Makowski, Stefanie L.; Tran, Thuy Tt; Buschman, Matthew D.; Li, Sheng; Cheng, Norton; Ng, Minna; Field, Seth J.

doi:10.1016/j.devcel.2019.05.038

Cited by 66 publications

(72 citation statements)

References 60 publications

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“…Altogether, our data show that CgA binds to specific species of PA which in turn could act as lipid cofactors 55 at the TGN to induce membrane remodeling and curvature in order to initiate secretory granule budding, concomitantly or prior to the recruitment of cytosolic proteins such as GOLPH3, 54 arfaptins, 56,57 the actomyosin 1b complex, 58 or the membrane‐associated myristoylated protein HID1, 59 but also small GTPase of the Arf family, 60 all of which are also essential actors in this fundamental biological process necessary for regulated secretion. Further studies are now needed to evaluate the connection of CgA/PA interaction with the additional machinery involved in secretory granule biogenesis, in living neuroendocrine cells, and the potential implication of this interaction in diseases related to hormone secretion deregulation.…”

Section: Discussionmentioning

confidence: 51%

“…It is of note that our lipidomic analysis indicates that these shorter forms of PA are scarce in Golgi or secretory granule membranes suggesting that only a tiny fraction of PA could trigger the fission of budding vesicle, while larger proportion of PA is required for budding. A recent study revealed that PI4P in the cytosolic leaflet of the TGN membrane recruits cytosolic proteins such as GOLPH3 through its membrane curvature ability, 54 suggesting that PA could also initiate this process by activating Golgi PIP‐kinase to produce PI4P in the cytosolic leaflet.…”

Section: Discussionmentioning

confidence: 55%

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Chromogranin A preferential interaction with Golgi phosphatidic acid induces membrane deformation and contributes to secretory granule biogenesis

et al. 2020

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Chromogranin A (CgA) is a key luminal actor of secretory granule biogenesis at the trans-Golgi network (TGN) level but the molecular mechanisms involved remain obscure. Here, we investigated the possibility that CgA acts synergistically with specific membrane lipids to trigger secretory granule formation. We show that CgA preferentially interacts with the anionic glycerophospholipid phosphatidic acid (PA).In accordance, bioinformatic analysis predicted a PA-binding domain (PABD) in CgA sequence that effectively bound PA (36:1) or PA (40:6) in membrane models.We identified PA (36:1) and PA (40:6) as predominant species in Golgi and granule membranes of secretory cells, and we found that CgA interaction with these PA species promotes artificial membrane deformation and remodeling. Furthermore, we demonstrated that disruption of either CgA PABD or phospholipase D (PLD) activity significantly alters secretory granule formation in secretory cells. Our findings show for the first time the ability of CgA to interact with PLD-generated PA, which allows 6770 |

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Section: Discussionmentioning

confidence: 51%

Section: Discussionmentioning

confidence: 55%

Chromogranin A preferential interaction with Golgi phosphatidic acid induces membrane deformation and contributes to secretory granule biogenesis

et al. 2020

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“…Finally, also enzyme-unrelated activities of GOLPH3 have been proposed to contribute to its oncogenicity. Among these, the GOLPH3 effects on cargo export from the TGN, and on the DNA damage response have been thoroughly characterized (Dippold et al, 2009;Farber-Katz et al, 2014;Halberg et al, 2016;Rahajeng et al, 2019;Xie et al, 2018). It will be interesting to examine how these mechanisms synergize with the effects of GOLPH3 on GSL metabolism described in this study.…”

Section: Discussionmentioning

confidence: 82%

The Glyco-enzyme adaptor GOLPH3 Links Intra-Golgi Transport Dynamics to Glycosylation Patterns and Cell Proliferation

Rizzo

Russo

Kurokawa

et al. 2019

Preprint

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Glycans are ubiquitous sugar polymers with major biological functions that are assembled by glyco-enzymes onto cargo molecules during their transport through the Golgi complex. How the Golgi determines glycan assembly is poorly understood. By relying on the Golgi cisternal maturation model and using the glyco-enzyme adaptor and oncoprotein GOLPH3 as a molecular tool, we define the first example of how the Golgi controls glycosylation and associated cell functions. GOLPH3, acting as a component of the cisternal maturation mechanism, selectively binds and recycles a subset of glyco-enzymes of the glycosphingolipid synthetic pathway, hinders their escape to the lysosomes and hence increases their levels through a novel lysosomal degradation-regulated mechanism. This enhances the production of specific growth-inducing glycosphingolipids and reprograms the glycosphingolipid pathway to potentiate mitogenic signaling and cell proliferation. These findings unravel unforeseen organizing principles of Golgi-dependent glycosylation and delineate a paradigm for glycan assembly by the Golgi transport mechanisms. Moreover, they indicate a new role of cisternal maturation as a regulator of glycosylation, and outline a novel mechanism of action for GOLPH3-induced proliferation.

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“…Knock-down of J o u r n a l P r e -p r o o f GOLPH3 or MYO18A or actin depolymerisation impairs trafficking of tsVSV-G from the Golgi to the plasma membrane. Additionally, GOLPH3 induces membrane curvature, by inserting a loop into the proximal leaflet of the bilayer and this property is required for efficient trans-Golgi to plasma membrane trafficking [179]. However, GOLPH3 has also been shown to specifically bind and recycle a subset of Golgi enzymes involved in glycan assembly on sphingolipids [180].…”

Section: Golph3mentioning

confidence: 99%

Direct trafficking pathways from the Golgi apparatus to the plasma membrane

Stalder

Gershlick

2020

Seminars in Cell & Developmental Biology

106

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In eukaryotic cells, protein sorting is a highly regulated mechanism important for many physiological events. After synthesis in the endoplasmic reticulum and trafficking to the Golgi apparatus, proteins sort to many different cellular destinations including the endolysosomal system and the extracellular space. Secreted proteins need to be delivered directly to the cell surface. Sorting of secreted proteins from the Golgi apparatus has been a topic of interest for over thirty years, yet there is still no clear understanding of the machinery that forms the post-Golgi carriers. Most evidence points to these post-Golgi carriers being tubular pleomorphic structures that bud from the trans-face of the Golgi. In this review, we present the background studies and highlight the key components of this pathway, we then discuss the machinery implicated in the formation of these carriers, their translocation across the cytosol, and their fusion at the plasma membrane.Abbreviations: ATP, adenosine triphosphate; BFA, Brefeldin A; CARTS, CARriers of the TGN to the cell Surface; CI-MPR, cation-independent mannose-6 phosphate receptor; CtBP3/BARS, C-terminus binding protein 3/BFA adenosine diphosphate-ribosylated substrate; ER, endoplasmic reticulum; GlcCer, glucosylceramide; PAUF, pancreatic adenocarcinoma up-regulated factor; PM, plasma membrane; RUSH, retention using selective hooks; SBP, streptavidin-binding peptide; SM, sphingomyelin; SNARE, soluble N-ethylmaleimide sensitive fusion protein attachment protein receptor;SPCA1, secretory pathway calcium ATPase 1; TGN, trans-Golgi Network; TIRF, total internal reflection fluorescence; ts, temperature sensitive; VSV, vesicular stomatitis virus J o u r n a l P r e -p r o o f J o u r n a l P r e -p r o o f J o u r n a l P r e -p r o o f J o u r n a l P r e -p r o o f

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Efficient Golgi Forward Trafficking Requires GOLPH3-Driven, PI4P-Dependent Membrane Curvature

Cited by 66 publications

References 60 publications

Chromogranin A preferential interaction with Golgi phosphatidic acid induces membrane deformation and contributes to secretory granule biogenesis

Chromogranin A preferential interaction with Golgi phosphatidic acid induces membrane deformation and contributes to secretory granule biogenesis

The Glyco-enzyme adaptor GOLPH3 Links Intra-Golgi Transport Dynamics to Glycosylation Patterns and Cell Proliferation

Direct trafficking pathways from the Golgi apparatus to the plasma membrane

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