Ceramide-Induced Apoptosis in Renal Tubular Cells: A Role of Mitochondria and Sphingosine-1-Phoshate
Abstract
:1. Introduction
2. Ceramide Biosynthesis and Degrading Pathways in Mammalian Cells
2.1. De Novo Synthesis Pathway
2.2. Hydrolysis of the Sphingomyelin (SM) Pathway
2.3. Salvage Pathway
2.4. Degrading Pathway
3. Compartmentalization of Ceramide Metabolism and Trafficking of Ceramide
3.1. Intracellular Localization of the Enzymes Involved in Ceramide Metabolism
3.2. Ceramide Compartmentalization and Trafficking
3.2.1. Endoplasmic Reticulum (ER) and Golgi
3.2.2. Mitochondria
3.2.3. Plasma Membrane and Lysosomes/Endosomes
3.2.4. Nuclei
3.3. Ceramide Compartmentalization and Trafficking in Renal Tubular Cells (RTCs)
4. Ceramide-Induced Apoptosis
4.1. Overview of Apoptosis
4.2. Ceramide-Induced Apoptosis in RTCs
Stimuli | Species | Cell Line for in Vitro */ Tissue for in Vivo | Increased Sphingolipid | Enzymes Involving Ceramide Metabolism | Ref. |
---|---|---|---|---|---|
In vitro study | |||||
Cadmium | Rat | PTCs | Ceramide | CerSs↑ | [60,61] |
Heat stress | Dog | MDCK cells | Ceramide | CerSs↑ | [56] |
Hypoxia/reoxygenation | Pig/Rat | LLC-PK1 cells/NRK-52E cells | Ceramide | CerSs↑ | [31,32,50] |
Interleukin-1β | Human | A498 cells ** | Ceramide | A-SMase↑, N-SMase↑ | [59] |
Isoflurane | Mouse Human | PTCs/HK-2 cells | Ceramide/Sphingosine | A-SMase→, N-SMase→, CerS→ | [62] |
Microcystin | Human | HEK293 cells | Ceramide | unknown | [63] |
Nickel | Rat | PTCs | Ceramide | CerSs↑ | [64] |
Oxalate | Pig/Dog | LLC-PK1 cells/MDCK cells | Ceramide | CerSs↑, SMases↑ | [54,57] |
Oxidants | Human | HK-2 cells | Ceramide/Sphingosine↓ | N-CDases→, N-SMase↓, A-SMase→, CerSs→ | [53] |
P-finbriae of E. coli | Human | A498cells ** | Ceramide | A-SMases→, N-SMase→, A-SMase↓, N-SMase→ | [58,59] |
Radiocontrast | Pig | LLC-PK1 cells | Ceramide | CerSs↑ | [65] |
Shiga-toxin B | Human | A498cells ** | Ceramide | A-SMase→, N-SMase→ | [58] |
St. enterotoxin B | Human | PTCs | Ceramide | N-SMase↑ | [66] |
TNF-α | Dog/ Human | MDCK cells/A498 cells ** | Ceramide | A-SMase↑, N-SMase↑ | [54,59] |
Ultraviolet light | Mouse | BMK cells | Ceramide | CerSs↑ | [38] |
In vivo study | |||||
Anti-GBM Ab-induced ARF | Mouse | Kidney | Ceramide | A-SMase↑, N-SMase↑ | [52] |
Carbon tetrachloride | Rat | Kidney | Ceramide | A-SMase→, N-SMase↑ | [67] |
Developing kidney | Rat | Kidney | Ceramide/S1P↓ | CerSs↑, SphKs↓ | [68,69] |
Ischemia/reperfusion | Mouse | Kidney | Ceramide | A-SMase↓, N-SMase↓ | [51,52] |
Isoflurane | Mouse | Kidney | Ceramide/Sphingosine | A-SMase→, ↑ #, N-SMase→, CDase↑ | [62] |
Myohemoglobinuria | Mouse | Kidney | Ceramide | A-SMase↓, N-SMase↓ | [52] |
Ureteral obstruction | Rat | Kidney | Ceramide | unknown | [70] |
4.3. A Role of Balance between Ceramide and Sphingosine-1 Phosphate (S1P) in RTCs
4.3.1. Sphingosine/Sphinganine
4.3.2. Ceramide and S1P
Sphingosine Kinases (SphKs)
S1P/S1P Receptors as a Survival Factor
S1P Phosphatase and S1P Lyase as Pro-Apoptotic Factors
4.4. Ceramide Compartmentalization and Trafficking in Ceramide-Induced Apoptosis
5. Ceramide-Induced Signaling Pathway for Apoptosis
5.1. Overview of a Role of Mitochondria in Ceramide-Induced Apoptosis
5.2. Mitochondrial Outer Membrane Permeability (MOMP) and Bcl-2 Family Proteins
5.2.1. Mitochondrial Integrity Regulated by Bcl-2 Family Proteins
5.2.2. Ceramide-Induced Bax/Bak Pore Formation in Mitochondria
5.2.3. Ceramide Channel Regulated by Bcl-2 Family Proteins
5.2.4. Voltage-Dependent Anion Channel (VDAC) and Mitochondrial Permeability Transition (MPT) Pore
Stimuli | Cell Line/Tissue | Enzymes Involving MOMP | Bcl-2 Proteins that Regulate Cer-Induced MOMP | Channel for Cer-Induced MOMP | Comments | Ref. |
---|---|---|---|---|---|---|
In other types of cells | ||||||
t-Bid, N-SMase | Murine liver mo./HeLa cells | N-SMase↑ | tBid-induced Bax oligomerization/ conformational change | MAC | Bax cooperates with Hex and Bak cooperates with S1P to induce t-Bid-mediated MOMP. Bcl-xL and N-SMase inhibitor inhibit MOMP. | [108] |
UV light | HeLa cells | A-SMase↑ | Bax conformational change | MAC | Bcl-2 inhibits MOMP. Bax change requires A-SMase activation. | [109] |
C16-Cer | HeLa cells | NA | Bax conformational change | MAC | Cer but not UV induces Bax change in A-SMase-deficient cells. Bcl-2 prevents Cer-induced Bax change. | [109] |
Irradiation | HeLa cells | CerS↑ in MAM | Bax↑ | MAC | Oligomeric Bax insertion into MOM causes MOMP. | [110] |
C16-Cer | Mo. of HeLa cells/ mouse liver | NA | tBid-induced Bax↑ | MAC | Cer induces MCRM *, favoring Bax insertion to MOM and oligomerization. | [110] |
C16-Cer | Rat liver mo. | NA | t-Bid-induced Bak↑ | Cer channel | Cer and Bax synergistically induce MOMP. Oligomeric Bax enhances Cer channel formation. | [112] |
C16-Cer | Rat liver mo. | NA | Bcl-xL/CED-9 prevents MOMP | Cer channel | Bcl-xL/CED-9 prevents and disassembles Cer channel. | [114] |
In renal tubular cells | ||||||
Radiocontrast | LLC-PK1 cells | CerS↑ | Bax↑, Bcl-2↓ | probably MAC | CerS inhibition reverses the change in Bax/Bcl-2. | [65] |
C2-Cer | HK-2 cells | NA | Bax↑ | probably MAC | [71] | |
C16-Cer | BMK cells | NA | MOMP occurs in Bax−/−Bak−/− cells | Cer channel | Bax/Bak is dispensable for Cer channel formation. | [114] |
C2-Cer | HEK293 cells | NA | Bad dephosphorylation | MPT pore | Bad/Bcl-xL/VDAC but not Bax/Bak regulate MPT pore opening. | [123] |
5.2.5. Ceramide-Induced Mitochondrial Calcium Uptake and Fission Regulate MOMP
5.2.6. Ceramide-Induced MOMP in the Regulation of Apoptosis of RTCs
5.2.7. Ceramide-Induced and Ceramide-Independent MOMP in Apoptosis
5.3. Regulation of the Enzyme Involved in Ceramide Metabolism by Bcl-2 Family Proteins
5.4. Ceramide-Induced Generation of Reactive Oxygen Species (ROS) and Its Regulation by Bcl-2 Family Proteins
5.4.1. Mitochondria and ROS Generation in Ceramide-Induced Apoptosis
5.4.2. Can ROS and Redox State Regulate the Enzymes Involved in Ceramide Metabolism?
5.4.3. A Role of Bcl-2 Family Proteins and ROS Production in Ceramide-Induced Apoptosis
Stimuli | Cell Line/Tissue | Cer-Induced Alteration of ROS/AOS | Enzymes for Cer Production Regulated by ROS | Bcl-2 Proteins Regulated by ROS/AOS | Cell Death | Ref. |
---|---|---|---|---|---|---|
Hypoxia | LLC-PK1 cells, NRK-52E cells | ROS↑ | CerS↑, A-SMase→, N-SMase→ | unknown | Necrosis/Apoptosis | [31,32] |
Oxidant | LLC-PK1 cells | Oxidant induces Cer | CerS↑, A-SMase→, N-SMase→ | unknown | Apoptosis/Necrosis | [33] |
Oxidant | HK-2 cells | Oxidant induces Cer | N-SMase↓, A-SMase→, CerS→, GSH activates N-SMase. | unknown | Necrosis | [53] |
Oxalate | MDCK cells, LLC-PK1 cells | ROS↑ | CerS↑, SMase↑ | unknown | Apoptosis | [54,57] |
Cadmium | Rat RTCs | ROS↑ | unknown | unknown | Apoptosis | [61] |
Carbon tetrachloride | Rat kidney | ROS↑, AOS↓ | N-SMase↑, A-SMase→ | unknown | Apoptosis | [67] |
C2-Cer | HK-2 cells | ROS↑ | NA | Bax↑ | Apoptosis | [71] |
Radiocontrast | LLC-PK1 cells | ROS↑ | CerS↑ | Bax↑, Bcl-2↓ | Apoptosis | [65,166] |
5.4.4. Do Ceramide-Induced ROS Regulate the Expression of Bcl-2 Family Proteins in Ceramide-Induced Apoptosis?
5.4.5. A Role of Ceramide-Induced ROS in Apoptosis of RTCs
6. Interconnection between Mitochondria and ER in the Regulation of Calcium Homeostasis in Ceramide-Induced Apoptosis
6.1. Calcium Homeostasis in the ER and Ceramide-Induced Apoptosis
6.2. Regulation of Calcium Homeostasis between the ER and Mitochondria by Bcl-2 Family Proteins in Ceramide-Induced Apoptosis
7. Ceramide- and Sphingosine-1-Phosphate-Induced Cell Signaling Pathways in the Regulation of Apoptosis
7.1. Mitogen-Activated Protein Kinases (MAPKs) and Ceramide-Induced Apoptosis
7.1.1. Ceramide-Induced Regulation of MAPKs in Apoptosis
7.1.2. Mechanism of Ceramide-Induced Activation of MAPKs
7.1.3. MAPKs Regulate the Enzymes Involved in Ceramide Metabolism
7.1.4. A Crosstalk between MAPKs and Bcl-2 Family Proteins in the Regulation of Ceramide-Induced Apoptosis
7.2. Signaling Molecules Other than MAPKs Regulated by Ceramide
7.3. S1P-Induced Signaling Pathway in Apoptosis of RTCs
8. Strategy for Preventing Ceramide-Induced Apoptosis of RTCs by Growth Factors
9. Conclusions and Future Perspective
Acknowledgments
Abbreviations
ACEC | apical ceramide-enriched compartment |
AIF | apoptosis inducing factor |
ANT | adenine nucleotide translocase |
AP-1 | activator protein 1 |
APF-1 | apoptosis protease-activating factor-1 |
AR | adenosine receptor |
ATP | adenosine 5'-triphosphate |
BI-1 | Bax inhibitor-1 |
BMK | baby mouse kidney |
CDases | ceramidases |
CDK5 | cyclin-dependent kinase 5 |
CerSs | ceramide synthases |
CERT | ceramide transfer protein |
C1P | ceramide-1-phosphate |
CREB | cAMP response element binding protein |
Δψm | mitochondrial membrane potential |
Drp1 | dynamin-related protein 1 |
EGF | epidermal growth factor |
EGFR | EGF receptor |
ER | endoplasmic reticulum |
ERK | extracellular signal-regulated kinase |
FAK | focal adhesion kinase |
GSH | glutathione |
GSLs | glycosphingolipids |
GSSG | oxidized GSH |
HEK | human embryonic kidney |
HIF | hypoxia-inducible factor |
HSP | heat shock protein |
IAP | inhibitor of apoptosis |
IGF-1 | insulin-like growth factor-1 |
IGF-II | insulin-like growth factor-II |
IP3R | 1,4,5-trisphosphate receptor |
IL | interleukin |
I/R | ischemia/reperfusion |
JNK | c-Jun N-terminal kinases |
3-keto-dihydro-Sph | 3-keto-dihydrosphingosine |
LPS | lipopolysaccharide |
MAMs | mitochondrial-associated membranes |
MAPKKK | mitogen-activated protein kinase kinase kinases |
MAPKs | mitogen-activated protein kinases |
MDCK | Madin-Dabry canine kidney |
MEKK | MAP/ERK kinase kinase |
MIM | mitochondrial inner membrane |
MLKs | mixed linage kinases |
MOM | mitochondrial outer membrane |
MOMP | mitochondrial outer membrane permeability |
MPT | mitochondrial permeability transition |
PDGF | platelet-derived growth factor |
PDGFR | PDGF receptor |
PERK | protein kinase R-like endoplasmic reticulum kinase |
PI3K | phosphatidylinositol 3-kinase |
PKA | protein kinase A |
PKC | protein kinase C |
PLA2 | phospholipase A2 |
PLC | phospholipase C |
PP2A | protein phosphatase 2A |
ROS | reactive oxygen species |
RTCs | renal tubular cells |
SAPK | stress activated protein kinase |
SERCA | sarcoplasmic-endoplasmic reticulum Ca2+-ATPase |
SM | sphingomyelin |
SMases | sphingomyelinases |
SMSs | SM synthases |
SphKs | sphingosine kinases |
S1P | sphingosine-1 phosphate |
S1PRs | S1P receptors |
SPT | serine palmitoyl transferase |
STAT | signal transducer and activator of transcription |
tBid | truncated Bid |
TNF | tumor necrosis factor |
UV | ultraviolet |
VDAC | voltage-dependent anion channel |
Conflicts of Interest
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Ueda, N. Ceramide-Induced Apoptosis in Renal Tubular Cells: A Role of Mitochondria and Sphingosine-1-Phoshate. Int. J. Mol. Sci. 2015, 16, 5076-5124. https://doi.org/10.3390/ijms16035076
Ueda N. Ceramide-Induced Apoptosis in Renal Tubular Cells: A Role of Mitochondria and Sphingosine-1-Phoshate. International Journal of Molecular Sciences. 2015; 16(3):5076-5124. https://doi.org/10.3390/ijms16035076
Chicago/Turabian StyleUeda, Norishi. 2015. "Ceramide-Induced Apoptosis in Renal Tubular Cells: A Role of Mitochondria and Sphingosine-1-Phoshate" International Journal of Molecular Sciences 16, no. 3: 5076-5124. https://doi.org/10.3390/ijms16035076
APA StyleUeda, N. (2015). Ceramide-Induced Apoptosis in Renal Tubular Cells: A Role of Mitochondria and Sphingosine-1-Phoshate. International Journal of Molecular Sciences, 16(3), 5076-5124. https://doi.org/10.3390/ijms16035076