LDL receptor-related protein-1 is a sialic-acid-independent receptor for myelin-associatedglycoprotein that functions in neurite outgrowth inhibition by MAG and CNS myelin

Journal of Cell Science

Volumn 126, Issue 1, 2013, Pages 209-220

  Stiles, Travis L ^a   Dickendesher, Travis L ^b   Gaultier, Alban ^a,c   Fernandez Castaneda, Anthony ^a   Mantuano, Elisabetta ^a   Giger, Roman J ^b   Gonias, Steven L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF VIRGINIA   (United States)

Author keywords

LDL receptor related protein 1; LRP1; Myelin; Myelin associated glycoprotein; Neurite outgrowth; p75NTR; RhoA

Indexed keywords

CHONDROITIN SULFATE; HYBRID PROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; MYELIN; MYELIN ASSOCIATED GLYCOPROTEIN; NEUROTROPHIN RECEPTOR P75; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SIALIC ACID;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; NERVE CELL; NERVE FIBER GROWTH; NONHUMAN; PC12 CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PURIFICATION; RNA INTERFERENCE;

ANIMALS; CELL LINE; CENTRAL NERVOUS SYSTEM; CHO CELLS; COS CELLS; CRICETINAE; LOW DENSITY LIPOPROTEIN RECEPTOR-RELATED PROTEIN-1; MASS SPECTROMETRY; MYELIN SHEATH; MYELIN-ASSOCIATED GLYCOPROTEIN; N-ACETYLNEURAMINIC ACID; NEURITES; PC12 CELLS; PROTEIN BINDING; RATS; RECEPTORS, NERVE GROWTH FACTOR;

MAMMALIA;

EID: 84875616437     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.113191     Document Type: Article

References (68)

1. Atwal, J. K., Pinkston-Gosse, J., Syken, J., Stawicki, S., Wu, Y., Shatz, C. and Tessier-Lavigne, M. (2008). PirB is a functional receptor for myelin inhibitors of axonal regeneration. Science 322, 967-970.
2. Boucher, P., Gotthardt, M., Li, W. P., Anderson, R. G. and Herz, J. (2003). LRP: role in vascular wall integrity and protection from atherosclerosis. Science 300, 329-332.
3. Bu, G., Maksymovitch, E. A., Nerbonne, J. M. and Schwartz, A. L. (1994). Expression and function of the low density lipoprotein receptor-related protein (LRP) in mammalian central neurons. J. Biol. Chem. 269, 18521-18528.
4. Busch, S. A. and Silver, J. (2007). The role of extracellular matrix in CNS regeneration. Curr. Opin. Neurobiol. 17, 120-127.
5. Cai, D., Shen, Y., De Bellard, M., Tang, S. and Filbin, M. T. (1999). Prior exposure to neurotrophins blocks inhibition of axonal regeneration by MAG and myelin via a cAMP-dependent mechanism. Neuron 22, 89-101.
6. Campana, W. M., Li, X., Dragojlovic, N., Janes, J., Gaultier, A. and Gonias, S. L. (2006). The low-density lipoprotein receptor-related protein is a pro-survival receptor in Schwann cells: possible implications in peripheral nerve injury. J. Neurosci. 26, 11197-11207.
7. Cao, Z., Qiu, J., Domeniconi, M., Hou, J., Bryson, J. B., Mellado, W. and Filbin, M. T. (2007) The inhibition site on myelin-associated glycoprotein is within Igdomain 5 and is distinct from the sialic acid binding site. J. Neuroscience 27, 9146-9154.
8. Chivatakarn, O., Kaneko, S., He, Z., Tessier-Lavigne, M. and Giger, R. J. (2007).The Nogo-66 receptor NgR1 is required only for the acute growth cone-collapsing butnot the chronic growth-inhibitory actions of myelin inhibitors. J. Neurosci. 27, 7117-7124
9. Dickendesher, T L., Baldwin, K. T., Mironova, Y. A., Koriyama, Y., Raiker, S. J., Askew, K. L., Wood, A., Geoffroy, C. G., Zheng, B. and Liepmann, C. D. et al. (2012) NgR1 and NgR3 are receptors for chondroitin sulfate proteoglycans. Nat. Neurosci. 15, 703-712.
10. Fawcett, J. (2009). Molecular control of brain plasticity and repair. Prog. Brain Res.175, 501-509.
11. Filbin, M. T. (2003). Myelin-associated inhibitors of axonal regeneration in the adult mammalian CNS. Nat. Rev. Neurosci. 4, 703-713.
12. FitzGerald, D. J., Fryling, C. M., Zdanovsky, A., Saelinger, C. B., Kounnas, M., Winkles, J. A., Strickland, D. and Leppla, S. (1995). Pseudomonas exotoxinmediated selection yields cells with altered expression of low-density lipoprotein receptor-related protein. J. Cell Biol. 129, 1533-1541.
13. Fu, Q., Hue, J. and Li, S. (2007). Nonsteroidal anti-inflammatory drugs promote axon regeneration via RhoA inhibition. J. Neurosci. 27, 4154-4164.
14. Fuentealba, R. A., Liu, Q., Kanekiyo, T., Zhang, J. and Bu, G. (2009). Low density lipoprotein receptor-related protein 1 promotes anti-apoptotic signaling in neurons by activating Akt survival pathway. J. Biol. Chem. 284, 34045-34053.
15. Fujita, Y., Takashima, R., Endo, S., Takai, T. and Yamashita, T. (2011). The p75 receptor mediates axon growth inhibition through an association with PIR-B. Cell Death Dis 2, e198.
16. Gaultier, A., Arandjelovic, S., Niessen, S., Overton, C. D., Linton, M. F., Fazio, S., Campana, W. M., Cravatt, B. F., 3rd and Gonias, S. L. (2008). Regulation of tumor necrosis factor receptor-1 and the IKK-NF-kappaB pathway by LDL receptorrelated protein explains the antiinflammatory activity of this receptor. Blood 111, 5316-5325.
17. Gaultier, A., Wu, X., Le Moan, N., Takimoto, S., Mukandala, G., Akassoglou, K., Campana, W. M. and Gonias, S. L. (2009). Low-density lipoprotein receptor-related protein 1 is an essential receptor for myelin phagocytosis. J. Cell Sci. 122, 1155-1162.
18. Gaultier, A., Simon, G., Niessen, S., Dix, M. M., Takimoto, S., Cravatt, B. F. and Gonias, S. L. (2010) LDL Receptor-related Protein 1 Regulates the Abundance of Diverse Cell-signaling Proteins in the Plasma Membrane Proteome. J. Proteome Res. 9, 6689-6695.
19. Goh, E. L., Young, J. K., Kuwako, K., Tessier-Lavigne, M., He, Z., Griffin, J. W. and Ming, G. L. (2008). beta1-integrin mediates myelin-associated glycoprotein signaling in neuronal growth cones. Mol. Brain 1, 10.
20. Gorovoy, M., Gaultier, A., Campana, W. M., Firestein, G. S. and Gonias, S. L. (2010). Inflammatory mediators promote production of shed LRP1/CD91, which regulates cell signaling and cytokine expression by macrophages. J. Leukoc. Biol. 88, 769-778.
21. Hayashi, H., Campenot, R. B., Vance, D. E. and Vance, J. E. (2007) Apolipoprotein E-containing lipoproteins protect neurons from apoptosis via a signaling pathway involving low-density lipoprotein receptor-related protein-1. J. Neuroscience 27, 1933-1941.
22. Jalink, K., van Corven, E. J., Hengeveld, T., Morii, N., Narumiya, S. andMoolenaar, W. H.(1994). Inhibition of lysophosphatidate-and thrombin-induced neurite retraction and neuronal cell rounding by ADP ribosylation of the small GTPbinding protein Rho. J. Cell Biol. 126, 801-810
23. Jeon, C Y., Moon, M. Y., Kim, J. H., Kim, H. J., Kim, J. G., Li, Y., Jin, J. K., Kim, P. H., Kim, H. C., Meier, K. E. et al. (2012). Control of neurite outgrowth by RhoA inactivation. J. Neurochem. 120, 684-698.
24. Joset, A., Dodd, D. A., Halegoua, S. and Schwab, M. E. (2010). Pincher-generated Nogo-A endosomes mediate growth cone collapse and retrograde signaling. J. Cell Biol. 188, 271-285.
25. Kim, J. E., Liu, B. P., Park, J. H. and Strittmatter, S. M. (2004). Nogo-66 receptor prevents raphespinal and rubrospinal axon regeneration and limits functional recovery from spinal cord injury. Neuron 44, 439-451.
26. Kozma, R., Sarner, S., Ahmed, S. and Lim, L. (1997). Rho family GTPases and neuronal growth cone remodelling: relationship between increased complexity induced by Cdc42Hs, Rac1, and acetylcholine and collapse induced by RhoA and lysophosphatidic acid. Mol. Cell. Biol. 17, 1201-1211.
27. Kuhn, T. B., Brown, M. D., Wilcox, C. L., Raper, J. A. and Bamburg, J. R. (1999). Myelin and collapsin-1 induce motor neuron growth cone collapse through different pathways: inhibition of collapse by opposing mutants of rac1. J. Neurosci. 19, 1965-1975.
28. Lillis, A. P., Greenlee, M. C., Mikhailenko, I., Pizzo, S. V., Tenner, A. J., Strickland, D. K. and Bohlson, S. S. (2008). Murine low-density lipoprotein receptor-related protein 1 (LRP) is required for phagocytosis of targets bearing LRP ligands but is not required for C1q-triggered enhancement of phagocytosis. J. Immunol. 181, 364-373.
29. Liu, Q., Zhang, J., Tran, H., Verbeek, M. M., Reiss, K., Estus, S. and Bu, G. (2009). LRP1 shedding in human brain: roles of ADAM10 and ADAM17. Mol. Neurodegener. 4, 17.
30. Lopes, M. B., Bogaev, C. A., Gonias, S. L. and VandenBerg, S. R. (1994). Expression of alpha 2-macroglobulin receptor/low density lipoprotein receptor-related protein is increased in reactive and neoplastic glial cells. FEBS Lett. 338, 301-305.
31. Madura, T., Yamashita, T., Kubo, T., Fujitani, M., Hosokawa, K. and Tohyama, M. (2004). Activation of Rho in the injured axons following spinal cord injury. EMBO Rep. 5, 412-417.
32. Mantuano, E., Mukandala, G., Li, X., Campana, W. M. and Gonias, S. L. (2008). Molecular dissection of the human alpha2-macroglobulin subunit reveals domains with antagonistic activities in cell signaling. J. Biol. Chem. 283, 19904-19911.
33. May, P., Rohlmann, A., Bock, H. H., Zurhove, K., Marth, J. D., Schomburg, E. D., Noebels, J. L., Beffert, U., Sweatt, J. D., Weeber, E. J. et al. (2004). Neuronal LRP1 functionally associates with postsynaptic proteins and is required for normal motor function in mice. Mol. Cell. Biol. 24, 8872-8883.
34. Mehta, N. R., Lopez, P. H., Vyas, A. A. and Schnaar, R. L. (2007). Gangliosides and Nogo receptors independently mediate myelin-associated glycoprotein inhibition of neurite outgrowth in different nerve cells. J. Biol. Chem. 282, 27875-27886.
35. Mukhopadhyay, G., Doherty, P., Walsh, F. S., Crocker, P. R. and Filbin, M. T. (1994). A novel role for myelin-associated glycoprotein as an inhibitor of axonal regeneration. Neuron 13, 757-767.
36. Niederöst, B., Oertle, T., Fritsche, J., McKinney, R. A. and Bandtlow, C. E. (2002). Nogo-A and myelin-associated glycoprotein mediate neurite growth inhibition by antagonistic regulation of RhoA and Rac1. J. Neurosci. 22, 10368-10376.
37. Norton, W. T. and Poduslo, S. E. (1973). Myelination in rat brain: method of myelin isolation. J. Neurochem. 21, 749-757.
38. Oberdoerster, J. (2001) Isolation of cerebellar granule cells from neonatal rats. Curr. Protoc. Toxicol. 12, 9, 12.7.1-12.7.10.
39. Park, J. B., Yiu, G., Kaneko, S., Wang, J., Chang, J., He, X. L., Garcia, K. C. and He, Z. (2005). A TNF receptor family member, TROY, is a coreceptor with Nogoreceptor inmediating the inhibitory activity of myelin inhibitors. Neuron 45, 345-351.
40. Polavarapu, R., Gongora, M. C., Yi, H., Ranganthan, S., Lawrence, D. A., Strickland, D. and Yepes, M. (2007). Tissue-type plasminogen activator-mediated shedding of astrocytic low-density lipoprotein receptor-related protein increases the permeability of the neurovascular unit. Blood 109, 3270-3278.
41. Qiu, Z., Hyman, B. T. and Rebeck, G. W. (2004). Apolipoprotein E receptors mediate neurite outgrowth through activation of p44/42 mitogen-activated protein kinase in primary neurons. J. Biol. Chem. 279, 34948-34956.
42. Quinn, K. A., Pye, V. J., Dai, Y. P., Chesterman, C. N. and Owensby, D. A. (1999). Characterization of the soluble form of the low density lipoprotein receptor-related protein (LRP). Exp. Cell Res. 251, 433-441.
43. Rebeck, G. W. (2009). Nontraditional signaling mechanisms of lipoprotein receptors. Sci. Signal. 2, pe28.
44. Robak, L. A., Venkatesh, K., Lee, H., Raiker, S. J., Duan, Y., Lee-Osbourne, J., Hofer, T., Mage, R. G., Rader, C. and Giger, R. J. (2009). Molecular basis of the interactions of the Nogo-66 receptor and its homolog NgR2 with myelin-associated glycoprotein: development of NgROMNI-Fc, a novel antagonist of CNS myelin inhibition. J. Neurosci. 29, 5768-5783.
45. Schmandke, A., Schmandke, A. and Strittmatter, S. M. (2007). ROCK and Rho: biochemistry and neuronal functions of Rho-associated protein kinases. Neuroscientist 13, 454-469.
46. Schwab, M. E. (2010). Functions of Nogo proteins and their receptors in the nervous system. Nat. Rev. Neurosci. 11, 799-811.
47. Schwab, M. E., Kapfhammer, J. P. and Bandtlow, C. E. (1993). Inhibitors of neurite growth. Annu. Rev. Neurosci. 16, 565-595.
48. Shao, Z., Browning, J. L., Lee, X., Scott, M. L., Shulga-Morskaya, S., Allaire, N., Thill, G., Levesque, M., Sah, D., McCoy, J. M. et al. (2005). TAJ/TROY, an orphan TNF receptor family member, binds Nogo-66 receptor 1 and regulates axonal regeneration. Neuron 45, 353-359.
49. Shi, Y., Mantuano, E., Inoue, G., Campana, W. M. and Gonias, S. L. (2009). Ligand binding to LRP1 transactivates Trk receptors by a Src family kinase-dependent pathway. Sci. Signal. 2, ra18.
50. Steuble, M., Gerrits, B., Ludwig, A., Mateos, J. M., Diep, T. M., Tagaya, M., Stephan, A., Schätzle, P., Kunz, B., Streit, P. et al. (2010). Molecular characterization of a trafficking organelle: dissecting the axonal paths of calsyntenin-1 transport vesicles. Proteomics 10, 3775-3788.
51. Strickland, D. K., Gonias, S. L. and Argraves, W. S. (2002). Diverse roles for the LDL receptor family. Trends Endocrinol. Metab. 13, 66-74.
52. Tan, E. Y., Law, J. W., Wang, C. H. and Lee, A. Y. (2007). Development of a cell transducible RhoA inhibitor TAT-C3 transferase and its encapsulation in biocompatible microspheres to promote survival and enhance regeneration of severed neurons. Pharm. Res. 24, 2297-2308.
53. Tang, S., Shen, Y. J., DeBellard, M. E., Mukhopadhyay, G., Salzer, J. L., Crocker, P. R. and Filbin, M. T. (1997). Myelin-associated glycoprotein interacts with neurons via a sialic acid binding site at ARG118 and a distinct neurite inhibition site. J. Cell Biol. 138, 1355-1366.
54. Venkatesh, K., Chivatakarn, O., Sheu, S. S. and Giger, R. J. (2007). Molecular dissection of the myelin-associated glycoprotein receptor complex reveals cell typespecific mechanisms for neurite outgrowth inhibition. J. Cell Biol. 177, 393-399.
55. Vinson, M., Strijbos, P. J., Rowles, A., Facci, L., Moore, S. E., Simmons, D. L. and Walsh, F. S. (2001). Myelin-associated glycoprotein interacts with ganglioside GT1b. A mechanism for neurite outgrowth inhibition. J. Biol. Chem. 276, 20280-20285.
56. Vyas, A. A., Patel, H. V., Fromholt, S. E., Heffer-Lauc, M., Vyas, K. A., Dang, J., Schachner, M. and Schnaar, R. L. (2002). Gangliosides are functional nerve cell ligands for myelin-associated glycoprotein (MAG), an inhibitor of nerve regeneration. Proc. Natl. Acad. Sci. USA 99, 8412-8417.
57. Wang, K. C., Kim, J. A., Sivasankaran, R., Segal, R. and He, Z. (2002). P75 interacts with the Nogo receptor as a co-receptor for Nogo, MAG and OMgp. Nature 420, 74-78.
58. Webb, D. J., Thomas, K. S. and Gonias, S. L. (2001). Plasminogen activator inhibitor 1 functions as a urokinase response modifier at the level of cell signaling and thereby promotes MCF-7 cell growth. J. Cell Biol. 152, 741-752.
59. Wight, P. A. and Dobretsova, A. (1997). The first intron of the myelin proteolipid protein gene confers cell type-specific expression by a transcriptional repression mechanism in non-expressing cell types. Gene 201, 111-117.
60. Willnow, T. E., Orth, K. and Herz, J. (1994). Molecular dissection of ligand binding sites on the low density lipoprotein receptor-related protein. J. Biol. Chem. 269, 15827-15832.
61. Winters, J. J., Ferguson, C. J., Lenk, G. M., Giger-Mateeva, V. I., Shrager, P., Meisler, M. H. and Giger, R. J. (2011). Congenital CNS hypomyelination in the Fig4 null mouse is rescued by neuronal expression of the PI(3,5)P(2) phosphatase Fig4. J. Neurosci. 31, 17736-17751.
62. Wolf, B. B., Lopes, M. B., VandenBerg, S. R. and Gonias, S. L. (1992). Characterization and immunohistochemical localization of alpha 2-macroglobulin receptor (low-density lipoprotein receptor-related protein) in human brain. Am. J. Pathol. 141, 37-42.
63. Wörter, V., Schweigreiter, R., Kinzel, B., Mueller, M., Barske, C., Böck, G., Frentzel, S. and Bandtlow, C. E. (2009). Inhibitory activity of myelin-associated glycoprotein on sensory neurons is largely independent of NgR1 and NgR2 and resides within Ig-Like domains 4 and 5. PLoS ONE 4, e5218.
64. Yamashita, T. and Tohyama, M. (2003). The p75 receptor acts as a displacement factor that releases Rho from Rho-GDI. Nat. Neurosci. 6, 461-467.
65. Yamashita, T., Higuchi, H. and Tohyama, M. (2002). The p75 receptor transduces the signal from myelin-associated glycoprotein to Rho. J. Cell Biol. 157, 565-570.
66. Yiu, G. and He, Z. (2006). Glial inhibition of CNS axon regeneration. Nat. Rev. Neurosci. 7, 617-627.
67. Zheng, B., Atwal, J., Ho, C., Case, L., He, X. L., Garcia, K. C., Steward, O. and Tessier-Lavigne, M. (2005). Genetic deletion of the Nogo receptor does not reduce neurite inhibition in vitro or promote corticospinal tract regeneration in vivo. Proc. Natl. Acad. Sci. USA 102, 1205-1210.
68. Zilberberg, A., Yaniv, A. and Gazit, A. (2004). The low density lipoprotein receptor-1, LRP1, interacts with the human frizzled-1 (HFz1) and down-regulates the canonical Wnt signaling pathway. J. Biol. Chem. 279, 17535-17542.