VPS10P-domain receptors - Regulators of neuronal viability and function

Nature Reviews Neuroscience

Volumn 9, Issue 12, 2008, Pages 899-909

  Willnow, Thomas E ^a   Petersen, Claus M ^b   Nykjaer, Anders ^b  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b AARHUS UNIVERSITY   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE RECEPTOR; NEUROTROPHIN; PROTEIN SORLA; PROTEIN SORTILIN; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; CELL DEATH; CELL FUNCTION; CELL VIABILITY; CYTOLOGY; HUMAN; MOOD DISORDER; NERVE CELL; NONHUMAN; PATHOPHYSIOLOGY; POSTTRAUMATIC STRESS DISORDER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; PROTEIN TRANSPORT; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CELL SURVIVAL; HUMANS; MODELS, BIOLOGICAL; NERVE TISSUE PROTEINS; NEURONS; PROTEIN TRANSPORT; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION;

EID: 56549111118     PISSN: 1471003X     EISSN: 14710048     Source Type: Journal    
DOI: 10.1038/nrn2516     Document Type: Review

References (118)

1. Marcusson, E. G., Horazdovsky, B. F., Cereghino, J. L., Gharakhanian, E. & Emr, S. D. The sorting receptor for yeast vacuolar carboxypeptidase Y is encoded by the VPS10 gene. Cell 77, 579-586 (1994).
2. Hampe, W. et al. A head-activator binding protein is present in hydra in a soluble and a membrane-anchored form. Development 126, 4077-4086 (1999).
3. Petersen, C. M. et al. Molecular identification of a novel candidate sorting receptor purified from human brain by receptor-associated protein affinity chromatography. J. Biol. Chem. 272, 3599-3605 (1997).
4. Yamazaki, H. et al. Elements of neural adhesion molecules and a yeast vacuolar protein sorting receptor are present in a novel mammalian low density lipoprotein receptor family member. J. Biol. Chem. 271, 24761-24768 (1996).
5. Jacobsen, L. et al. Molecular characterization of a novel human hybrid-type receptor that binds the α2-macroglobulin receptor-associated protein. J. Biol. Chem. 271, 31379-31383 (1996).
6. Hermey, G., Riedel, I. B., Hampe, W., Schaller, H. C. & Hermans-Borgmeyer, I. Identification and characterization of SorCS, a third member of a novel receptor family. Biochem. Biophys. Res. Commun. 266, 347-351 (1999).
7. Rezgaoui, M. et al. Identification of SorCS2, a novel member of the VPS10 domain containing receptor family, prominently expressed in the developing mouse brain. Mech. Dev. 100, 335-338 (2001).
8. Hampe, W., Rezgaoui, M., Hermans-Borgmeyer, I. & Schaller, H. C. The genes for the human VPS10 domain-containing receptors are large and contain many small exons. Hum. Genet. 108, 529-536 (2001).
9. Paiardini, A. & Caputo, V. Insights into the interaction of sortilin with proneurotrophins: a computational approach. Neuropeptides 42, 205-214 (2008).
10. Rogaeva, E. et al. The neuronal sortilin-related receptor SORL1 is genetically associated with Alzheimer disease. Nature Genet. 39, 168-177 (2007). The first in a series of studies that demonstrated an association between SORL1 and late-onset AD.
11. Grupe, A. et al. A scan of chromosome 10 identifies a novel locus showing strong association with late-onset Alzheimer disease. Am. J. Hum. Genet. 78, 78-88 (2006).
12. Baum, A. E. et al. A genome-wide association study implicates diacylglycerol kinase eta (DGKH) and several other genes in the etiology of bipolar disorder. Mol. Psychiatry 13, 197-207 (2008).
13. Lu, T. et al. Gene regulation and DNA damage in the ageing human brain. Nature 429, 883-891 (2004).
14. Kathiresan, S. et al. Six new loci associated with blood low-density lipoprotein cholesterol, high-density lipoprotein cholesterol or triglycerides in humans. Nature Genet. 40, 189-197 (2008).
15. Clee, S. M. et al. Positional cloning of Sorcs1, a type 2 diabetes quantitative trait locus. Nature Genet. 38, 688-693 (2006).
16. Granhall, C., Park, H. B., Fakhrai-Rad, H. & Luthman, H. High-resolution quantitative trait locus analysis reveals multiple diabetes susceptibility loci mapped to intervals < 800 kb in the species-conserved Niddm 1i of the GK rat. Genetics 174, 1565-1572 (2006).
17. Taira, K. et al. LR11, a mosaic LDL receptor family member, mediates the uptake of ApoE-rich lipoproteins in vitro. Arterioscler. Thromb. Vasc. Biol. 21, 1501-1506 (2001).
18. Nilsson, S. K. et al. Apolipoprotein A-V interaction with members of the low density lipoprotein receptor gene family. Biochemistry 46, 3896-3904 (2007).
19. Nilsson, S. K. et al. Endocytosis of apolipoprotein A-V by members of the low density lipoprotein receptor and the VPS10p domain receptor families. J. Biol. Chem. 283, 25920-25927 (2008).
20. Nielsen, M. S., Jacobsen, C., Olivecrona, G., Gliemann, J. & Petersen, C. M. Sortilin/neurotensin receptor-3 binds and mediates degradation of lipoprotein lipase. J. Biol. Chem. 274, 8832-8836 (1999).
21. Bonifacino, J. S. & Rojas, R. Retrograde transport from endosomes to the trans-Golgi network. Nature Rev. Mol. Cell Biol. 7, 568-579 (2006).
22. Nielsen, M. S. et al. The sortilin cytoplasmic tail conveys Golgi-endosome transport and binds the VHS domain of the GGA2 sorting protein. EMBO J. 20, 2180-2190 (2001).
23. Jacobsen, L. et al. Activation and functional characterization of the mosaic receptor SorLA/LR11. J. Biol. Chem. 276, 22788-22796 (2001).
24. Sarret, P. et al. Distribution of NTS3 receptor/sortilin mRNA and protein in the rat central nervous system. J. Comp. Neurol. 461, 483-505 (2003).
25. Hermey, G. et al. SorCS1, a member of the novel sorting receptor family, is localized in somata and dendrites of neurons throughout the murine brain. Neurosci. Lett. 313, 83-87 (2001).
26. Nielsen, M. S. et al. Sorting by the cytoplasmic domain of the amyloid precursor protein binding receptor SorLA. Mol. Cell. Biol. 27, 6842-6851 (2007). Demonstrated golgi-to-endosome sorting by SORLA and SORLA downregulation in response to retromer (SNX1 and VPS35) knock down.
27. Morinville, A. et al. Internalization and trafficking of neurotensin via NTS3 receptors in HT29 cells. Int. J. Biochem. Cell Biol. 36, 2153-2168 (2004).
28. Mari, M. et al. SNX1 defines an early endosomal recycling exit for sortilin and mannose 6-phosphate receptors. Traffic 9, 380-393 (2008).
29. Seaman, M. N. Cargo-selective endosomal sorting for retrieval to the Golgi requires retromer. J. Cell Biol. 165, 111-122 (2004).
30. Seaman, M. N. Identification of a novel conserved sorting motif required for retromer-mediated endosome-to-TGN retrieval. J. Cell Sci. 120, 2378-2389 (2007). Identified motifs for retromer interaction in the cytoplasmic domains of CI-MPR and sortilin.
31. Scott, G. K., Fei, H., Thomas, L., Medigeshi, G. R. & Thomas, G. A PACS-1, GGA3 and CK2 complex regulates CI-MPR trafficking. EMBO J. 25, 4423-4435 (2006).
32. Westergaard, U. B. et al. SorCS3 does not require propeptide cleavage to bind nerve growth factor. FEBS Lett. 579, 1172-1176 (2005).
33. Nielsen, M. S. et al. Different motifs regulate trafficking of SorCS1 isoforms. Traffic 9, 980-994 (2008).
34. Hermey, G. et al. Characterization of sorCS1, an alternatively spliced receptor with completely different cytoplasmic domains that mediate different trafficking in cells. J. Biol. Chem. 278, 7390-7396 (2003).
35. Chao, M. V. Neurotrophins and their receptors: a convergence point for many signalling pathways. Nature Rev. Neurosci. 4, 299-309 (2003).
36. Reichardt, L. F. Neurotrophin-regulated signalling pathways. Philos. Trans. R. Soc. Lond. B Biol. Sci. 361, 1545-1564 (2006).
37. NTR regulates death signaling and is required for subsequent cleavage by γ-secretase. Mol. Cell. Neurosci. 37, 346-358 (2008).
38. Kenchappa, R. S. et al. Ligand-dependent cleavage of the P75 neurotrophin receptor is necessary for NRIF nuclear translocation and apoptosis in sympathetic neurons. Neuron 50, 219-232 (2006).
39. Lee, R., Kermani, P., Teng, K. K. & Hempstead, B. L. Regulation of cell survival by secreted proneurotrophins. Science 294, 1945-1948 (2001). Identified proNTs as cell-death-inducing ligands.
40. Mowla, S. J. et al. Biosynthesis and post-translational processing of the precursor to brain-derived neurotrophic factor. J. Biol. Chem. 276, 12660-12666 (2001).
41. Nykjaer, A. et al. Sortilin is essential for proNGF-induced neuronal cell death. Nature 427, 843-848 (2004). Demonstrated that sortilin is a high-affinity receptor for proNgF that is required for endocytosis and induction of cell death by proNTs.
42. Matsumoto, T. et al. Biosynthesis and processing of endogenous BDNF: CNS neurons store and secrete BDNF, not pro-BDNF. Nature Neurosci. 11, 131-133 (2008).
43. Mowla, S. J. et al. Differential sorting of nerve growth factor and brain-derived neurotrophic factor in hippocampal neurons. J. Neurosci. 19, 2069-2080 (1999).
44. NTR and sortilin. J. Neurosci. 25, 5455-5463 (2005).
45. - co-transporter KCC2. Development 130, 1267-1280 (2003).
46. Fauchais, A. L. et al. Role of endogenous brain-derived neurotrophic factor and sortilin in B cell survival. J. Immunol. 181, 3027-3038 (2008).
47. Bruno, M. A. & Cuello, A. C. Activity-dependent release of precursor nerve growth factor, conversion to mature nerve growth factor, and its degradation by a protease cascade. Proc. Natl Acad. Sci. USA 103, 6735-6740 (2006).
48. Hasan, W., Pedchenko, T., Krizsan-Agbas, D., Baum, L. & Smith, P. G. Sympathetic neurons synthesize and secrete pro-nerve growth factor protein. J. Neurobiol. 57, 38-53 (2003).
49. Srinivasan, B., Roque, C. H., Hempstead, B. L., Al-Ubaidi, M. R. & Roque, R. S. Microglia-derived pronerve growth factor promotes photoreceptor cell death via p75 neurotrophin receptor. J. Biol. Chem. 279, 41839-41845 (2004).
50. Domeniconi, M., Hempstead, B. L. & Chao, M. V. Pro-NGF secreted by astrocytes promotes motor neuron cell death. Mol. Cell. Neurosci. 34, 271-279 (2007).
51. Fahnestock, M., Michalski, B., Xu, B. & Coughlin, M. D. The precursor pro-nerve growth factor is the predominant form of nerve growth factor in brain and is increased in Alzheimer's disease. Mol. Cell. Neurosci. 18, 210-220 (2001).
52. Stoica, G., Lungu, G., Kim, H. T. & Wong, P. K. Up-regulation of pro-nerve growth factor, neurotrophin receptor p75, and sortilin is associated with retrovirus-induced spongiform encephalomyelopathy. Brain Res. 1208, 204-216 (2008).
53. Harrington, A. W. et al. Secreted proNGF is a pathophysiological death-inducing ligand after adult CNS injury. Proc. Natl Acad. Sci. USA 101, 6226-6230 (2004).
54. Beattie, M. S. et al. ProNGF induces p75-mediated death of oligodendrocytes following spinal cord injury. Neuron 36, 375-386 (2002).
55. Volosin, M. et al. Interaction of survival and death signaling in basal forebrain neurons: roles of neurotrophins and proneurotrophins. J. Neurosci. 26, 7756-7766 (2006).
56. NTR-mediated apoptosis via neurotrophin receptor-interacting factor in hippocampal neurons after seizures. J. Neurosci. 28, 9870-9879 (2008).
57. Yune, T. Y. et al. Minocycline alleviates death of oligodendrocytes by inhibiting pro-nerve growth factor production in microglia after spinal cord injury. J. Neurosci. 27, 7751-7761 (2007).
58. Sobottka, B., Reinhardt, D., Brockhaus, M., Jacobsen, H. & Metzger, F. ProNGF inhibits NGF-mediated TrkA activation in PC12 cells. J. Neurochem. 15 Sep 2008 (doi:10.1111/j.1471-4159.2008.05690.x).
59. NTR and sortilin increase after facial nerve injury. Laryngoscope 118, 87-93 (2008).
60. Jansen, P. et al. Roles for the pro-neurotrophin receptor sortilin in neuronal development, aging and brain injury. Nature Neurosci. 10, 1449-1457 (2007). Described the phenotype of the SORT1-knockout mouse and provided genetic evidence for an in vivo function of the receptor in proNT-induced apoptosis.
61. NTR in retina of rat following elevated intraocular pressure-induced retinal ischemia. Neurosci. Lett. 429, 169-174 (2007).
62. Al-Shawi, R. et al. Neurotoxic and neurotrophic roles of proNGF and the receptor sortilin in the adult and ageing nervous system. Eur. J. Neurosci. 27, 2103-2114 (2008).
63. Nakamura, K., Namekata, K., Harada, C. & Harada, T. Intracellular sortilin expression pattern regulates proNGF-induced naturally occurring cell death during development. Cell Death Differ. 14, 1552-1554 (2007).
64. NTR: potential mediators of injury-induced apoptosis in the mouse dorsal root ganglion. Brain Res. 1183, 32-42 (2007).
65. Bronfman, F. C., Tcherpakov, M., Jovin, T. M. & Fainzilber, M. Ligand-induced internalization of the p75 neurotrophin receptor: a slow route to the signaling endosome. J. Neurosci. 23, 3209-3220 (2003).
66. Bronfman, F. C. Metalloproteases and γ-secretase: new membrane partners regulating p75 neurotrophin receptor signaling? J. Neurochem. 103 (Suppl. 1), 91-100 (2007).
67. NTR by TACE and nuclear trafficking of the p75 intracellular domain. Mol. Cell. Neurosci. 36, 449-461 (2007).
68. NTR and apoptosis. Am. J. Pathol. 169, 119-131 (2006).
69. NTR from a clathrin-independent to a clathrin-dependent endocytic pathway coupled to axonal transport. Traffic 8, 1736-1749 (2007).
70. Wang, H. et al. Axonal transport of BDNF precursor in primary sensory neurons. Eur. J. Neurosci. 24, 2444-2452 (2006).
71. Deinhardt, K. et al. Rab5 and Rab7 control endocytic sorting along the axonal retrograde transport pathway. Neuron 52, 293-305 (2006).
72. Gargano, N., Levi, A. & Alema, S. Modulation of nerve growth factor internalization by direct interaction between p75 and TrkA receptors. J. Neurosci. Res. 50, 1-12 (1997).
73. Martin, S., Vincent, J. P. & Mazella, J. Involvement of the neurotensin receptor-3 in the neurotensin-induced migration of human microglia. J. Neurosci. 23, 1198-1205 (2003).
74. Truzzi, F. et al. Neurotrophins and their receptors stimulate melanoma cell proliferation and migration. J. Invest. Dermatol. 128, 2031-2040 (2008).
75. Buttigieg, H., Kawaja, M. D. & Fahnestock, M. Neurotrophic activity of proNGF in vivo. Exp. Neurol. 204, 832-835 (2007).
76. Boutilier, J. et al. Proneurotrophins require endocytosis and intracellular proteolysis to induce TrkA activation. J. Biol. Chem. 283, 12709-12716 (2008). This study demonstrated that the survival-promoting activities of proNTs require conversion into mature NTs in an endosomal compartment.
77. Hebert, E. Mannose-6-phosphate/insulin-like growth factor II receptor expression and tumor development. Biosci. Rep. 26, 7-17 (2006).
78. Chen, Z. Y. et al. Sortilin controls intracellular sorting of brain-derived neurotrophic factor to the regulated secretory pathway. J. Neurosci. 25, 6156-6166 (2005).
79. Trommsdorff, M., Borg, J. P., Margolis, B. & Herz, J. Interaction of cytosolic adaptor proteins with neuronal apolipoprotein E receptors and the amyloid precursor protein. J. Biol. Chem. 273, 33556-33560 (1998).
80. Martinowich, K., Manji, H. & Lu, B. New insights into BDNF function in depression and anxiety. Nature Neurosci. 10, 1089-1093 (2007).
81. Chen, Z. Y. et al. Genetic variant BDNF (Val66Met) polymorphism alters anxiety-related behavior. Science 314, 140-143 (2006).
82. Scherzer, C. R. et al. Loss of apolipoprotein E receptor LR11 in Alzheimer disease. Arch. Neurol. 61, 1200-1205 (2004).
83. Dodson, S. E. et al. LR11/SorLA expression is reduced in sporadic Alzheimer disease but not in familial Alzheimer disease. J. Neuropathol. Exp. Neurol. 65, 866-872 (2006).
84. Lee, J. H. et al. The association between genetic variants in SORL1 and Alzheimer disease in an urban, multiethnic, community-based cohort. Arch. Neurol. 64, 501-506 (2007).
85. King, G. D. & Scott Turner, R. Adaptor protein interactions: modulators of amyloid precursor protein metabolism and Alzheimer's disease risk? Exp. Neurol. 185, 208-219 (2004).
86. Koo, E. H. The β-amyloid precursor protein (APP) and Alzheimer's disease: does the tail wag the dog? Traffic 3, 763-770 (2002).
87. Reinhard, C., Hebert, S. S. & De Strooper, B. The amyloid-β precursor protein: integrating structure with biological function. EMBO J. 24, 3996-4006 (2005).
88. Andersen, O. M. et al. Neuronal sorting protein-related receptor sorLA/LR11 regulates processing of the amyloid precursor protein. Proc. Natl Acad. Sci. USA 102, 13461-13466 (2005). A demonstration of SORLA's role as the neuronal trafficking receptor for APP and a description of a defect in this receptor's gene in the mouse.
89. Offe, K. et al. The lipoprotein receptor LR11 regulates amyloidβ production and amyloid precursor protein traffic in endosomal compartments. J. Neurosci. 26, 1596-1603 (2006).
90. Andersen, O. M. et al. Molecular dissection of the interaction between amyloid precursor protein and its neuronal trafficking receptor SorLA/LR11. Biochemistry 45, 2618-2628 (2006).
91. Rohe, M. et al. Sortilin-related receptor with A-type repeats (SORLA) affects the amyloid precursor protein-dependent stimulation of ERK signaling and adult neurogenesis. J. Biol. Chem. 283, 14826-14834 (2008).
92. Ma, Q. L. et al. Omega-3 fatty acid docosahexaenoic acid increases SorLA/LR11, a sorting protein with reduced expression in sporadic Alzheimer's disease (AD): relevance to AD prevention. J. Neurosci. 27, 14299-14307 (2007).
93. Schmidt, V. et al. SorLA/LR11 regulates processing of amyloid precursor protein via interaction with adaptors GGA and PACS-1. J. Biol. Chem. 282, 32956-32964 (2007).
94. De Strooper, B. & Annaert, W. Proteolytic processing and cell biological functions of the amyloid precursor protein. J. Cell Sci. 113, 1857-1870 (2000).
95. Small, S. A. & Gandy, S. Sorting through the cell biology of Alzheimer's disease: intracellular pathways to pathogenesis. Neuron 52, 15-31 (2006).
96. Peraus, G. C., Masters, C. L. & Beyreuther, K. Late compartments of amyloid precursor protein transport in SY5Y cells are involved in β-amyloid secretion. J. Neurosci. 17, 7714-7724 (1997).
97. Khvotchev, M. & Sudhof, T. C. Proteolytic processing of amyloid-β precursor protein by secretases does not require cell surface transport. J. Biol. Chem. 279, 47101-47108 (2004).
98. Nixon, R. A. & Cataldo, A. M. Lysosomal system pathways: genes to neurodegeneration in Alzheimer's disease. J. Alzheimers Dis. 9, 277-289 (2006).
99. von Arnim, C. A. et al. Demonstration of BACE (β-secretase) phosphorylation and its interaction with GGA1 in cells by fluorescence-lifetime imaging microscopy. J. Cell Sci. 117, 5437-5445 (2004).
100. von Arnim, C. A. et al. GGA1 acts as a spatial switch altering amyloid precursor protein trafficking and processing. J. Neurosci. 26, 9913-9922 (2006).
101. Tesco, G. et al. Depletion of GGA3 stabilizes BACE and enhances β-secretase activity. Neuron 54, 721-737 (2007).
102. Wahle, T. et al. GGA proteins regulate retrograde transport of BACE1 from endosomes to the trans-Golgi network. Mol. Cell. Neurosci. 29, 453-461 (2005).
103. Small, S. A. Retromer sorting: a pathogenic pathway in late-onset Alzheimer disease. Arch. Neurol. 65, 323-328 (2008).
104. Seaman, M. N. Recycle your receptors with retromer. Trends Cell Biol. 15, 68-75 (2005).
105. Small, S. A. et al. Model-guided microarray implicates the retromer complex in Alzheimer's disease. Ann. Neurol. 58, 909-919 (2005).
106. Muhammad, A. et al. Retromer deficiency observed in Alzheimer's disease causes hippocampal dysfunction, neurodegeneration, and Aβ accumulation. Proc. Natl Acad. Sci. USA 105, 7327-7332 (2008).
107. Nothwehr, S. F., Ha, S. A. & Bruinsma, P. Sorting of yeast membrane proteins into an endosome-to-Golgi pathway involves direct interaction of their cytosolic domains with Vps35p. J. Cell Biol. 151, 297-310 (2000).
108. Beffert, U., Stolt, P. C. & Herz, J. Functions of lipoprotein receptors in neurons. J. Lipid Res. 45, 403-409 (2004).
109. Pietrzik, C. U. et al. FE65 constitutes the functional link between the low-density lipoprotein receptor-related protein and the amyloid precursor protein. J. Neurosci. 24, 4259-4265 (2004).
110. Pietrzik, C. U., Busse, T., Merriam, D. E., Weggen, S. & Koo, E. H. The cytoplasmic domain of the LDL receptor-related protein regulates multiple steps in APP processing. EMBO J. 21, 5691-5700 (2002).
111. Munck Petersen, C. et al. Propeptide cleavage conditions sortilin/neurotensin receptor-3 for ligand binding. EMBO J. 18, 595-604 (1999).
112. Westergaard, U. B. et al. Functional organization of the sortilin Vps10p domain. J. Biol. Chem. 279, 50221-50229 (2004).
113. Hermey, G., Sjogaard, S., Petersen, C. M., Nykjaer, A. & Gliemann, J. Tumour necrosis factor-α convertase mediates ectodomain shedding of Vps10p-domain receptor family members. Biochem. J. 395, 285-293 (2006).
114. Navarro, V., Vincent, J. P. & Mazella, J. Shedding of the luminal domain of the neurotensin receptor-3/sortilin in the HT29 cell line. Biochem. Biophys. Res. Commun. 298, 760-764 (2002).
115. Hampe, W. et al. Ectodomain shedding, translocation and synthesis of SorLA are stimulated by its ligand head activator. J. Cell Sci. 113, 4475-4485 (2000).
116. Nyborg, A. C., Ladd, T. B., Zwizinski, C. W., Lah, J. J. & Golde, T. E. Sortilin, SorCS1b, and SorLA Vps10p sorting receptors, are novel γ-secretase substrates. Mol. Neurodegener. 1, 3 (2006).
117. Hermey, G. et al. The three sorCS genes are differentially expressed and regulated by synaptic activity. J. Neurochem. 88, 1470-1476 (2004).
118. Bergami, M. et al. Uptake and recycling of pro-BDNF for transmitter-induced secretion by cortical astrocytes. J. Cell Biol. 183, 213-221 (2008).