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Importance of Endocytic Pathways in Liver Function and Disease

Barbara Schroeder, Mark A. McNiven

10.1002/cphy.c140001

Source: Volume 4, Issue 4, October 2014

Published online: September 2014

Full Article on Wiley Online Library



Abstract

Hepatocellular endocytosis is a highly dynamic process responsible for the internalization of a variety of different receptor ligand complexes, trophic factors, lipids, and, unfortunately, many different pathogens. The uptake of these external agents has profound effects on seminal cellular processes including signaling cascades, migration, growth, and proliferation. The hepatocyte, like other well‐polarized epithelial cells, possesses a host of different endocytic mechanisms and entry routes to ensure the selective internalization of cargo molecules. These pathways include receptor‐mediated endocytosis, lipid raft associated endocytosis, caveolae, or fluid‐phase uptake, although there are likely many others. Understanding and defining the regulatory mechanisms underlying these distinct entry routes, sorting and vesicle formation, as well as the postendocytic trafficking pathways is of high importance especially in the liver, as their mis‐regulation can contribute to aberrant liver pathology and liver diseases. Further, these processes can be “hijacked” by a variety of different infectious agents and viruses. This review provides an overview of common components of the endocytic and postendocytic trafficking pathways utilized by hepatocytes. It will also discuss in more detail how these general themes apply to liver‐specific processes including iron homeostasis, HBV infection, and even hepatic steatosis. © 2014 American Physiological Society. Compr Physiol 4:1403‐1417, 2014.

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Figure 1. Figure 1. Endocytic trafficking routes in hepatocytes. (A) Overview of degradative and recycling pathways that are controlled by RabGTPases and marked by specific phospho‐inositides. (B) Assembly of the clathrin coat at the plasma membrane. Clathrin forms a triskelion (blue) that is connected to the cargo (green) via adaptor proteins (orange). The large GTPase Dynamin 2 (Dyn2, red) controls the scission of the nascent vesicle which is subsequently trafficked to endosomes for further sorting. (C) Early endosomes are the sorting stations in the cell. Different cargo molecules are concentrated at distinct subdomains of the sorting endosomes: cargo destined for degradation is marked by ubiquitination, which is recognized by the ESCRT machinery while nonubiquitinated cargo accumulates at distinct subdomains of the early endosome and is recylcled back to the plasma membrane via a Rab11‐ or Rab4‐dependent pathway. (D) ESCRT complexes recognize and sort ubiquitinated cargo into intraluminal vesicles (ILVs) of late endosomes to form multivesicular bodies (MVBs). Subsequent fusion with lysosomes leads to the degradation of the cargo molecule. (D) Immunofluerescence images showing the colocalization of Dynamin 2 (Dyn2, green) and Clathrin (red) in Clone 9 cells. The image was kindly provided by Dr. H. Cao, Mayo Clinic, Rochester. PM: plasma membrane; EE: early endosome; LE: late endosome; MVB: multivesicular body; lys: lysosome; DUB: deubiquitinating enzymes.
Figure 2. Figure 2. Trafficking pathways of the Transferrin Receptor 1 and 2 essential for iron homeostasis. (A) Schematic representation of the domain structure of transferrin receptor 1 and 2 (TfR1 and 2) illustrating a cytoplasmic domain (CD), transmembrane domain (TM), protease‐like domain and a C‐terminal helical domain. While the CD is quite distinct between the two receptors, the ectodomains share about 45% identity. (B) Localization of TfR1 and TfR2 in Clone 9 cells. Both receptors were stained with specific antibodies. Due to the loss of TfR2 in cultured primary hepatocytes, this receptor was stably expressed in Clone 9 cells and then stained. The images were kindly provided by Dr. H. Cao, Mayo Clinic, Rochester. (C) Overview of the different trafficking pathways used by TfR1 and TfR2. While TfR1 is recycled back to the plasma membrane in a Rab11‐dependent manner, TfR2 has been reported to enter the degradative pathway; however, the exact trafficking routes of TfR2 remain to be determined. PM: plasma membrane; CCP: clathrin‐coated pit; EE: early endosome; LE: late endosome; MVB: multivesicular body; LYS: lysosome.
Figure 3. Figure 3. Hepatocytes accumulate lipid droplets under steatotic conditions. (A) Cartoon depicting the composition of a lipid droplet (LD) and its associated proteins. The cartoon was reprinted from Krahmer et al. with permission (69). (B‐B'') Accumulation of lipid droplets in VA‐13 cells under nonfed conditions (B), upon oleate exposure (B'), or after oleate + EtOH treatment (B''). LDs were visualized using Oil Red O stain. Note that the oleate‐induced accumulation of LDs is further enhanced by cotreatment with EtOH mimicking fatty liver disease. (C) Association of PLIN2 (perilipin‐2) (green) on LDs (red) in Hep3B human hepatoma cells after o/n feeding with 150 micromolar/Litre oleate. (D) Close association of GFP‐Rab7 (green) with LDs (red) in Hep3B cells after o/n feeding with 150 micromolar/Litre oleate. (E) Localization of GFP‐Cav1 (green) on LDs (red) in HuH7 human hepatoma cells after o/n feeding with 150 micromolar/Litre oleate. (F‐I) TEM images from Hep3B cells loaded with 150 micromolar/Litre oelate on/showing LDs under resting (F) and starved (G‐I) conditions. Arrows point to sites of potential fusion events (F) or LDs engulfed by a gigantic autophagosome (G). Starvation was induced by incubation in medium with 0.1% FBS for 24 h. (G‐I) show three different examples of autophagic breakdown of LDs which are engulfed by lysosomes (electron dense compartments surrounding LDs). All TEM images were provided by Eugene Krueger, Mayo Clinic, Rochester.
Figure 4. Figure 4. Autophagy contributes to lipid droplet breakdown. (A) Cartoon showing the different stages of autophagosome formation. During the nucleation phase, an isolation membrane forms which then extends around the cargo destined for autophagic degradation to form an autophagosome. The autophagosome eventually fuses with lysosomes to a hybrid compartment, named the autolysosome, in which cargo proteins are degraded. Cartoon reprinted from Melendez and Levine with permission (91). (B‐E) EM gallery depicting the different stages of autophagosome and autolysosome formation as described in (A). The gallery shows the entrance of cargo into endosomes (B), maturing autophagosomes containing still recognizable, but partially degraded material (C), heterogeneous intraluminal material (D) and lysosomes with fully degraded material leading to a less dense appearance. EM images reprinted from Nixon with permission (103). (F, G) Visualization of autophagosome formation in Hep3B hepatoma cells. Hep3B cells expressing GFP‐LC3, an autophagic marker, were compared under resting (F) and starved conditions (24 h in medium containing 0.1% FBS). Note that starvation results in a redistribution of LC3 from the cytosol and nucleus to distinct vesicular structures. (H) Colocalization of autophagosomes (green) and lysosomes (red) on lipid droplets (LDs, blue). Hep3B cells expressing mCherry‐LAMP1 were starved for 24 h in medium containing 0.1% serum and the autophagosomes were stained using a LC3 antibody (green). LDs were visualized using MDH (blue). The image was kindly provided by Shaun Weller, Mayo Clinic, Rochester.
Figure 5. Figure 5. Hepatitis B virus hijacks the endocytic system to ensure proper reproduction. (A) Cartoon (© James A. Perkins; used by permission) depicting the hepatitis B virion (HBV). HBV is comprised of a core, embedding the virus DNA and polymerase, and a protein‐rich capsid consisting of large, small and medium surface proteins as indicated. (B) Cartoon showing the current model for HBV/MVB (multivesicular body) association and their involvement in virus reproduction. Cartoon modified after Patient with permission (109). HBV assembly potentially starts on the limiting membrane of MVBs and may eventually be delivered to intraluminal vesicles (ILVs). The fully assembled virus may then be separated from the MVB in the form of exosomes and delivered to the plasma membrane (PM), where it is released by fusion with the PM or by exocytosis to reinfect neighboring cells. (C and D) HBV associates with components of the ESCRT machinery in late endosomes. Confocal images show colocalization of the large HBs (LHBs, red) with Hrs (green), a component of the ESCRT‐0 complex (C), or with the late endosomal/MVB marker GFP‐Rab7wt (green; D). Boxes depict the regions that are enlarged in (C' and D'), respectively. Arrows point to the sites of colocalization with the marker as indicated. The immune‐fluorescence images were kindly provided by Dr. Jun Inoue, Mayo Clinic, Rochester. (E) TEM image showing virus particles (dense regions) residing in MVBs in HepG2.2.15 cells. Image provided by Eugene Krueger, Mayo Clinic, Rochester.


Figure 1. Endocytic trafficking routes in hepatocytes. (A) Overview of degradative and recycling pathways that are controlled by RabGTPases and marked by specific phospho‐inositides. (B) Assembly of the clathrin coat at the plasma membrane. Clathrin forms a triskelion (blue) that is connected to the cargo (green) via adaptor proteins (orange). The large GTPase Dynamin 2 (Dyn2, red) controls the scission of the nascent vesicle which is subsequently trafficked to endosomes for further sorting. (C) Early endosomes are the sorting stations in the cell. Different cargo molecules are concentrated at distinct subdomains of the sorting endosomes: cargo destined for degradation is marked by ubiquitination, which is recognized by the ESCRT machinery while nonubiquitinated cargo accumulates at distinct subdomains of the early endosome and is recylcled back to the plasma membrane via a Rab11‐ or Rab4‐dependent pathway. (D) ESCRT complexes recognize and sort ubiquitinated cargo into intraluminal vesicles (ILVs) of late endosomes to form multivesicular bodies (MVBs). Subsequent fusion with lysosomes leads to the degradation of the cargo molecule. (D) Immunofluerescence images showing the colocalization of Dynamin 2 (Dyn2, green) and Clathrin (red) in Clone 9 cells. The image was kindly provided by Dr. H. Cao, Mayo Clinic, Rochester. PM: plasma membrane; EE: early endosome; LE: late endosome; MVB: multivesicular body; lys: lysosome; DUB: deubiquitinating enzymes.


Figure 2. Trafficking pathways of the Transferrin Receptor 1 and 2 essential for iron homeostasis. (A) Schematic representation of the domain structure of transferrin receptor 1 and 2 (TfR1 and 2) illustrating a cytoplasmic domain (CD), transmembrane domain (TM), protease‐like domain and a C‐terminal helical domain. While the CD is quite distinct between the two receptors, the ectodomains share about 45% identity. (B) Localization of TfR1 and TfR2 in Clone 9 cells. Both receptors were stained with specific antibodies. Due to the loss of TfR2 in cultured primary hepatocytes, this receptor was stably expressed in Clone 9 cells and then stained. The images were kindly provided by Dr. H. Cao, Mayo Clinic, Rochester. (C) Overview of the different trafficking pathways used by TfR1 and TfR2. While TfR1 is recycled back to the plasma membrane in a Rab11‐dependent manner, TfR2 has been reported to enter the degradative pathway; however, the exact trafficking routes of TfR2 remain to be determined. PM: plasma membrane; CCP: clathrin‐coated pit; EE: early endosome; LE: late endosome; MVB: multivesicular body; LYS: lysosome.


Figure 3. Hepatocytes accumulate lipid droplets under steatotic conditions. (A) Cartoon depicting the composition of a lipid droplet (LD) and its associated proteins. The cartoon was reprinted from Krahmer et al. with permission (69). (B‐B'') Accumulation of lipid droplets in VA‐13 cells under nonfed conditions (B), upon oleate exposure (B'), or after oleate + EtOH treatment (B''). LDs were visualized using Oil Red O stain. Note that the oleate‐induced accumulation of LDs is further enhanced by cotreatment with EtOH mimicking fatty liver disease. (C) Association of PLIN2 (perilipin‐2) (green) on LDs (red) in Hep3B human hepatoma cells after o/n feeding with 150 micromolar/Litre oleate. (D) Close association of GFP‐Rab7 (green) with LDs (red) in Hep3B cells after o/n feeding with 150 micromolar/Litre oleate. (E) Localization of GFP‐Cav1 (green) on LDs (red) in HuH7 human hepatoma cells after o/n feeding with 150 micromolar/Litre oleate. (F‐I) TEM images from Hep3B cells loaded with 150 micromolar/Litre oelate on/showing LDs under resting (F) and starved (G‐I) conditions. Arrows point to sites of potential fusion events (F) or LDs engulfed by a gigantic autophagosome (G). Starvation was induced by incubation in medium with 0.1% FBS for 24 h. (G‐I) show three different examples of autophagic breakdown of LDs which are engulfed by lysosomes (electron dense compartments surrounding LDs). All TEM images were provided by Eugene Krueger, Mayo Clinic, Rochester.


Figure 4. Autophagy contributes to lipid droplet breakdown. (A) Cartoon showing the different stages of autophagosome formation. During the nucleation phase, an isolation membrane forms which then extends around the cargo destined for autophagic degradation to form an autophagosome. The autophagosome eventually fuses with lysosomes to a hybrid compartment, named the autolysosome, in which cargo proteins are degraded. Cartoon reprinted from Melendez and Levine with permission (91). (B‐E) EM gallery depicting the different stages of autophagosome and autolysosome formation as described in (A). The gallery shows the entrance of cargo into endosomes (B), maturing autophagosomes containing still recognizable, but partially degraded material (C), heterogeneous intraluminal material (D) and lysosomes with fully degraded material leading to a less dense appearance. EM images reprinted from Nixon with permission (103). (F, G) Visualization of autophagosome formation in Hep3B hepatoma cells. Hep3B cells expressing GFP‐LC3, an autophagic marker, were compared under resting (F) and starved conditions (24 h in medium containing 0.1% FBS). Note that starvation results in a redistribution of LC3 from the cytosol and nucleus to distinct vesicular structures. (H) Colocalization of autophagosomes (green) and lysosomes (red) on lipid droplets (LDs, blue). Hep3B cells expressing mCherry‐LAMP1 were starved for 24 h in medium containing 0.1% serum and the autophagosomes were stained using a LC3 antibody (green). LDs were visualized using MDH (blue). The image was kindly provided by Shaun Weller, Mayo Clinic, Rochester.


Figure 5. Hepatitis B virus hijacks the endocytic system to ensure proper reproduction. (A) Cartoon (© James A. Perkins; used by permission) depicting the hepatitis B virion (HBV). HBV is comprised of a core, embedding the virus DNA and polymerase, and a protein‐rich capsid consisting of large, small and medium surface proteins as indicated. (B) Cartoon showing the current model for HBV/MVB (multivesicular body) association and their involvement in virus reproduction. Cartoon modified after Patient with permission (109). HBV assembly potentially starts on the limiting membrane of MVBs and may eventually be delivered to intraluminal vesicles (ILVs). The fully assembled virus may then be separated from the MVB in the form of exosomes and delivered to the plasma membrane (PM), where it is released by fusion with the PM or by exocytosis to reinfect neighboring cells. (C and D) HBV associates with components of the ESCRT machinery in late endosomes. Confocal images show colocalization of the large HBs (LHBs, red) with Hrs (green), a component of the ESCRT‐0 complex (C), or with the late endosomal/MVB marker GFP‐Rab7wt (green; D). Boxes depict the regions that are enlarged in (C' and D'), respectively. Arrows point to the sites of colocalization with the marker as indicated. The immune‐fluorescence images were kindly provided by Dr. Jun Inoue, Mayo Clinic, Rochester. (E) TEM image showing virus particles (dense regions) residing in MVBs in HepG2.2.15 cells. Image provided by Eugene Krueger, Mayo Clinic, Rochester.
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Article Title: Importance of Endocytic Pathways in Liver Function and Disease
 

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Barbara Schroeder, Mark A. McNiven. Importance of Endocytic Pathways in Liver Function and Disease. Compr Physiol 2014, 4: 1403-1417. doi: 10.1002/cphy.c140001