The PKD-Dependent Biogenesis of TGN-to-Plasma Membrane Transport Carriers
Abstract
:1. Introduction
1.1. Membrane Trafficking
1.2. Multiple Export Pathways from the TGN
2. PKD Is a Key Regulator of TGN Export and Golgi Lipid Homeostasis
2.1. Discovery of PKD as a Central Regulator of TGN Export
2.2. PKD Structure
2.3. PKD Roles in Constitutive and Regulated Protein Secretion
2.4. PKD Recruitment to the TGN and Activation
2.5. PKD Phosphorylates Substrates at the TGN
- PI4KIIIß: PKD phosphorylates PI4KIIIß, triggering its activation [83]. Active PI4KIIIß phosphorylates the lipid phosphatidylinositol (PI) in the 4-position to yield PI 4-phosphate (PI4P). Interestingly, it has been suggested that ARF1 plays a determinant role in the localization and activation of PI4KIIIß, hence underscoring the interconnection amongst all these components associated to PKD-mediated transport carrier formation [17].
- CERT: PKD phosphorylates the ceramide transport protein (CERT) [94]. CERT localizes to ER-Golgi membrane contact sites (MCSs), and it was the first lipid transfer protein (LTP) found to shuttle lipids between two distinct membranes without a vesicular intermediate [95]. CERT contains a canonical PH domain, which has specificity for binding to PI4P and hence targets this protein to the trans-Golgi/TGN membranes; an FFAT (two phenylalanines in an acidic tract) motif for interaction with the ER-localized vesicle-associated membrane protein-associated proteins (VAPs); and a steroidogenic acute regulatory protein-related lipid transfer (START) domain, which is responsible for the directional transfer of ceramide from the ER to the Golgi membranes [95]. Upon phosphorylation by PKD, CERT does not bind PI4P and is therefore released from the TGN, which supposedly improves the efficiency of non-vesicular lipid transfer by enhancing its dynamics at ER-Golgi MCSs.
- OSBP: Another substrate of PKD at ER-Golgi MCSs is the oxysterol-binding protein (OSBP) [96]. OSBP is a member of the OSBP-related protein (ORP)/oxysterol-binding homology (Osh) family of sterol sensor proteins. Similar to CERT, OSBP contains a PH domain that binds PI4P and also to ARF1-GTP, thus targeting OSBP to the late Golgi membranes; as well as an FFAT motif for trans ER anchoring through VAPs. In addition, OSBP contains an OSBP-related domain (ORD), which acts as a bidirectional lipid transfer domain that catalyzes the transport of cholesterol from the ER to the trans-Golgi membranes, and the reciprocal transport of PI4P from the Golgi to the ER membrane [97]. Mechanistically, there is experimental evidence suggesting that OSBP can function as a ferry-bridge protein, meaning that it combines its tethering function—by linking the ER and Golgi membranes together—with its lipid transfer function—by shuttling lipids between these two membranes [98]. Importantly, this ferry-bridge mode of action has also been proposed for other proteins with a similar domain structure, such as CERT [98]. Likewise to CERT, PKD-mediated phosphorylation of OSBP releases it from PI4P at the TGN for efficient lipid transfer [17,96].
3. CARTS Are PKD-Dependent Transport Carriers from the TGN to the Cell Surface
3.1. Isolation and Identification of CARTS
3.2. Features of CARTS Pathway
4. Lipid Requirements for PKD-Mediated CARTS Formation
4.1. ER-Golgi MCSs Are a Platform for Non-Vesicular, Bi-Directional Trafficking of Lipids
4.2. The Cycle of PI4P at the ER-Golgi Interface
4.3. Sources of DAG at the TGN for PKD Recruitment and Activation
4.4. SM Metabolism and Cab45-Mediated Secretory Cargo Sorting at the TGN
5. Signaling at the Golgi Membranes for the Regulation of Protein Secretion
5.1. GPCR-Mediated Signaling
5.2. Sac1-Mediated Signaling
5.3. Mechanical Signals
6. Summary and Concluding Remarks
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
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Transport Carriers | Protein Name | Topology | Secretion Type | References |
---|---|---|---|---|
PKD-dependent carriers (General) | CD4 | TM | Constitutive | [25] |
TGN46 | TM | Constitutive | [25] | |
Furin | TM | Constitutive | [32] | |
VSV-G (Basolateral PM) | TM | Constitutive | [25,26] | |
ss-HRP | Soluble | Constitutive | [27] | |
Insulin | Soluble | Regulated | [33,34] | |
Chromogranin A | Soluble | Regulated | [35,36] | |
ß1-integrin (Basolateral PM) | TM | Constitutive | [26] | |
E-cadherin (Basolateral PM) | TM | Constitutive | [26] | |
CtBP1/BARS-dependent carriers | VSV-G | TM | Constitutive | [37] |
Low-density lipoprotein (LDL) receptor | TM | Constitutive | [38] | |
Human growth hormone (hGH) | Soluble | Constitutive | [38] | |
CARTS | TGN46 | TM | Constitutive | [39] |
ss-HRP | Soluble | Constitutive | [39,40] | |
PAUF | Soluble | Constitutive | [39] | |
Lysozyme C | Soluble | Constitutive | [39] | |
Synaptotagmin II | TM | Constitutive | [39] | |
FM4-GPI (CD58) | GPI-AP | Constitutive | [41] | |
EQ-SM (SM reporter protein) | MA | Constitutive | [41] | |
SM-rich transport carriers | EQ-SM (SM reporter protein) | MA | Constitutive | [42] |
FM4-GPI (CD58) | GPI-AP | Constitutive | [42] | |
Cab45 | Soluble | Constitutive | [43,44,45] | |
ss-HRP | Soluble | Constitutive | [44,46] | |
Lysozyme C | Soluble | Constitutive | [45,47] | |
Cartilage oligomeric matrix protein (COMP) | Soluble | Constitutive | [45,47] | |
Lipoprotein lipase | MA | Constitutive | [48] | |
Syndecan-1 | TM | Constitutive | [48] | |
Rab6-positive carriers (General) | VSV-G | TM | Constitutive | [49,50] |
Neuropeptide Y (NPY) | Soluble | Constitutive | [49,51] | |
TNFα | Soluble | Constitutive | [52,53,54] | |
Herpes Simplex virus 1 (HSV1) glycoproteins gD/gE | TM | Constitutive | [55] | |
Collagen type X | Soluble | Constitutive | [53] | |
CD59 | GPI-AP | Constitutive | [53] | |
Placenta alkaline phosphatase (PLAP) | GPI-AP | Constitutive | [53] | |
ß1-integrin | TM | Constitutive | [56] | |
Membrane type 1-matrix metalloproteinase (MT1-MMP) | TM | Constitutive | [57] |
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Wakana, Y.; Campelo, F. The PKD-Dependent Biogenesis of TGN-to-Plasma Membrane Transport Carriers. Cells 2021, 10, 1618. https://doi.org/10.3390/cells10071618
Wakana Y, Campelo F. The PKD-Dependent Biogenesis of TGN-to-Plasma Membrane Transport Carriers. Cells. 2021; 10(7):1618. https://doi.org/10.3390/cells10071618
Chicago/Turabian StyleWakana, Yuichi, and Felix Campelo. 2021. "The PKD-Dependent Biogenesis of TGN-to-Plasma Membrane Transport Carriers" Cells 10, no. 7: 1618. https://doi.org/10.3390/cells10071618
APA StyleWakana, Y., & Campelo, F. (2021). The PKD-Dependent Biogenesis of TGN-to-Plasma Membrane Transport Carriers. Cells, 10(7), 1618. https://doi.org/10.3390/cells10071618