Role of the Hyaluronan Receptor, Stabilin-2/HARE, in Health and Disease
Abstract
:1. Introduction
2. Characteristics of Stabilin-2/HARE
- Fas1: Recombinant cells that express high levels of Stabilin-2 often become sticky in that they stick to each other. Park et al. investigated how this occurred and found that Fas1 domains are responsible for homophilic cell–cell adhesion which also required a divalent cation such as Mn2+, Mg2+ or Ca2+ [14]. Fas1 domains also interact with integrins in a heterophilic fashion. Using mouse recombinant L-cells expressing Stabilin-2 and following up with human SECs, they found that the Fas1 domains of Stabilin-2 adhere with αMβ2 integrins on the surface of leukocytes and that this adherence was firm and not associated with rolling nor transmigration [15]. Further studies by the same laboratory showed that aged or apoptotic cells such as erythrocytes are immobilized by Stabilin-2 through the interaction of αVβ5 integrins and that engulfment occurs via the GULP adaptor-mediated activation of Rac1. These experiments were also performed in L-cells stably expressing Stabilin-2 in which phagocytosis could occur [16]. Since SECs do not employ phagocytic mechanisms, SECs may immobilize the target cells in the sinusoid allowing Kupffer cells to engulf them. Alternatively, immune cells expressing Stabilin-2 may phagocytose dead or apoptotic cells.
- EGF: The inner leaflet of the plasma membrane of erythrocytes is enriched in phosphatidylserine (PS), which flips to the outer leaflet when the cells die [17]. The exposure of PS is a signal for phagocytic cells to “eat” the dead cell and clear it from circulation. Park et al. discovered that the EGF domains of Stabilin-2 (and Stabilin-1) recognize PS as a binding ligand and may immobilize apoptotic/aged cells in the sinusoids for engulfment by Kupffer cells [18,19]. The interaction required Ca2+ and occurred at pH 7.3, but was optimal at pH 6.8. Furthermore, the intriguing part of this story is that the second EGF domain in each cluster is more atypical than the other EGF domains and there is a conserved histidine which aligns with position 1403 of the third cluster. This histidine is conserved within each EGF cluster and between both Stabilin receptors. Mutagenesis of the histidine did not affect binding affinity for PS, but did affect binding enhancement at lower pH, suggesting that the histidine is protonated at lower pH (pKa ~6.0) and that other residues in the binding loop are involved with PS interaction [20].
- Link: The Link domain is the HA binding domain for Stabilin-2. It is located between the last EGF and Fas1 domains near the transmembrane region. Deletion of the Link domain results in complete ablation of HA binding [21,22]. The Link domain of Stabilin-2 has highest homology to the Link domain of tumor necrosis factor-stimulated gene-6 (TSG-6). In silico modeling suggests that the tyrosine residues are critical for HA binding [23]. Unlike the Stabilin-2 Link, the TSG-6 Link also binds heparin at a distal site within the domain [24]. Stabilin-2 also binds heparin, but not within the link domain and the precise location is unknown at this time [25]. Although HA binds the Stabilin-2 Link domain with high affinity approaching 20 nM, the interaction is relatively weak compared to other hyalectins. With the use of atomic force microscopy for direct measurement of the interaction of the protein with a low megaDalton polymer, HA bound to Stabilin-2 with 25 picoNewtons (pN) in comparison to TSG-6 (24 pN), CD44 (34 pN), versican (37 pN) and aggrecan (>52 pN) [26]. Having both high affinity and the ability to release the cargo once in the early endosomes is critical for this receptor, in contrast to the other hyalectins which only bind and form stable matrices.
3. Ligand Binding of the LINK Domain
4. Stabilin-2 as a Cellular Signaling Receptor
5. Physiological Functions of Stabilin-2
6. Stabilin-2 and Cancer Metastasis
7. Conclusions and Perspectives
Funding
Conflicts of Interest
References
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Organ | Tissue | Function | Reference |
---|---|---|---|
Liver | Sinusoidal endothelia | HA and other blood borne molecule catabolism | [8,45,67] |
Lymph node | Medullary sinuses | HA catabolism | [8,45,67] |
Spleen | Venous sinusoids | Not Determined | [8,45,67] |
Bone marrow | Venous sinusoids | Bone cell homing | [44,45] |
Eye | Corneal and cuboidal epithelium | Not Determined | [45] |
Kidney | Renal papillae | Not Determined | [45] |
Brain | Ependymal cells of choroid plexuses | Not Determined | [45] |
Heart | Mesenchymal cells of heart valves | Not Determined | [45] |
Striated Muscle | Myocyte | Myoblast fusion in myogenesis | [55,59] |
Blood | Human monocyte derived macrophages | Clearance of cell corpse | [18] |
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Harris, E.N.; Baker, E. Role of the Hyaluronan Receptor, Stabilin-2/HARE, in Health and Disease. Int. J. Mol. Sci. 2020, 21, 3504. https://doi.org/10.3390/ijms21103504
Harris EN, Baker E. Role of the Hyaluronan Receptor, Stabilin-2/HARE, in Health and Disease. International Journal of Molecular Sciences. 2020; 21(10):3504. https://doi.org/10.3390/ijms21103504
Chicago/Turabian StyleHarris, Edward N., and Erika Baker. 2020. "Role of the Hyaluronan Receptor, Stabilin-2/HARE, in Health and Disease" International Journal of Molecular Sciences 21, no. 10: 3504. https://doi.org/10.3390/ijms21103504