Identification of the low density lipoprotein (LDL) receptor-related protein-1 interactome in central nervous system myelin suggests a role in the clearance of necrotic cell debris

Journal of Biological Chemistry

Volumn 288, Issue 7, 2013, Pages 4538-4548

  Fernandez Castaneda, Anthony ^a   Arandjelovic, Sanja ^b   Stiles, Travis L ^c   Schlobach, Ryan K ^a   Mowen, Kerri A ^b   Gonias, Steven L ^c   Gaultier, Alban ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AFFINITY PURIFICATION; APOPTOTIC CELLS; CENTRAL NERVOUS SYSTEMS; INTERACTOME; INTRACELLULAR PROTEINS; LOW DENSITY LIPOPROTEINS; NECROTIC CELLS; NOVEL LIGANDS; PROTEOMICS; SCAVENGER RECEPTOR;

DEBRIS; LIGANDS; MOLECULAR BIOLOGY;

PROTEINS;

CELL PROTEIN; CHEMOKINE RECEPTOR CCR2; CHEMOKINE RECEPTOR CCR4; CYCLIC NUCLEOTIDE PHOSPHODIESTERASE; HYBRID PROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; PROTEIN ARGININE DEIMINASE; PROTEIN ARGININE DEIMINASE 2; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DEAMINATION; ENDOCYTOSIS; IN VITRO STUDY; INHIBITION KINETICS; LIGAND BINDING; MASS SPECTROMETRY; MYELIN SHEATH; NERVE CELL NECROSIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION;

ANIMALS; APOPTOSIS; CENTRAL NERVOUS SYSTEM; CITRULLINE; CLONING, MOLECULAR; ENDOCYTOSIS; GLUTATHIONE TRANSFERASE; GREEN FLUORESCENT PROTEINS; HOMEOSTASIS; HUMANS; JURKAT CELLS; LIGANDS; LOW DENSITY LIPOPROTEIN RECEPTOR-RELATED PROTEIN-1; MASS SPECTROMETRY; MICE; MULTIPLE SCLEROSIS; MYELIN SHEATH; NECROSIS; PHAGOCYTOSIS; PROTEOMICS;

EID: 84874088008     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.384693     Document Type: Article

References (50)

1. Compston, A., and Coles, A. (2008) Multiple sclerosis. Lancet 372, 1502-1517
2. Barnett, M. H., and Prineas, J. W. (2004) Relapsing and remitting multiple sclerosis: pathology of the newly forming lesion. Ann. Neurol. 55, 458-468
3. Botto, M., DellAgnola, C, and Bygrave., A. E., Thompson, E. M., Cook, H. T., Petry, F., Loos, M., Pandolfi, P. P., and Walport, M. J. (1998) Homozygous C1q deficiency causes glomerulonephritis associated with multiple apoptotic bodies. Nat. Genet. 19, 56-59
4. 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
5. Gardai, S. J., and McPhillips., K. A., Frasch, S. C, Janssen, W. J., Starefeldt, A., Murphy-Ullrich, J. E., Bratton, D. L., Oldenborg, P. A., Michalak, M., and Henson, P. M. (2005) Cell-surface calreticulin initiates clearance of viable or apoptotic cells through trans-activation of LRP on the phagocyte. Cell 123, 321-334
6. Ogden, C A., deCathelineau, A., Hoffmann, P. R., Bratton, D., Ghebrehiwet, B., Fadok, V. A., and Henson, P.M. (2001) C1q and mannose binding lectin engagement of cell surface calreticulin and CD91 initiates macropinocytosis and uptake of apoptotic cells. J. Exp. Med. 194, 781-795
7. Herz, J., Hamann, U., Rogne, S., Myklebost, O., Gausepohl, H., and Stanley, K. K. (1988) Surface location and high affinity for calcium of a 500-kd liver membrane protein closely related to the LDL-receptor suggest a physiological role as lipoprotein receptor. EMBOJ. 7, 4119-4127
8. Strickland, D. K., and Ashcom., J. D., Williams, S., Burgess, W. H, Migliorini, M., and Argraves, W. S. (1990) Sequence identity between the α 2-macroglobulin receptor and low density lipoprotein receptor-related protein suggests that this molecule is a multifunctional receptor. J. Biol. Chem. 265, 17401-17404
9. Lillis, A. P., Van Duyn, L. B., Murphy-Ullrich, J. E., and Strickland, D. K. (2008) LDL receptor-related protein 1: unique tissue-specific functions revealed by selective gene knockout studies. Physiol. Rev. 88, 887-918
10. Gonias, S. L., Wu, L., and Salicioni, A. M. (2004) Low density lipoprotein receptor-related protein: regulation of the plasma membrane proteome. Thromb. Haemost. 91, 1056-1064
11. Gonias, S. L., Gaultier, A., and Jo, M. (2011) Regulation of the urokinase receptor (uPAR) by LDL receptor-related protein-1 (LRP1). Curr. Pharm. Des. 17, 1962-1969
12. 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-κB pathway by LDL receptor-related protein explains the antiinflammatory activity of this receptor. Blood 111, 5316-5325
13. Zurhove, K., Nakajima, C, Herz, J., Bock, H. H, and May, P. (2008) γ-Secretase limits the inflammatory response through the processing of LRP1. Sci. Signal 1, ra15
14. Stiles, T. L., and Dickendesher., T. L., Gaultier, A., Fernandez-Castaneda, A., Mantuano, E., and Giger., R. J., and Gonias, S. L. (2012) LDL Receptor-related Protein-1 is a sialic acid-independent receptor for myelin-associated glycoprotein (MAG) that functions in neurite outgrowth inhibition by MAG and CNS myelin. J. Cell Sci. [Epub ahead of print]
15. Neels, J. G., van Den Berg, B. M., Lookene, A., Olivecrona, G., Pannekoek, H, and van Zonneveld, A. J. (1999) The second and fourth cluster of class A cysteine-rich repeats of the low density lipoprotein receptor-related protein share ligand-binding properties. J. Biol. Chem. 274, 31305-31311
16. Herz, J., and Goldstein., J. L., Strickland, D. K., Ho, Y. K., and Brown, M. S. (1991) 39-kDa protein modulates binding of ligands to low density lipoprotein receptor-related protein/a 2-macroglobulin receptor. J. Biol. Chem. 266, 21232-21238
17. Lee, J., Gravel, M., Zhang, R., Thibault, P., and Braun, P. E. (2005) Process outgrowth in oligodendrocytes is mediated by CNP, a novel microtubule assembly myelin protein. J. Cell Biol, 170, 661-673
18. Kozlov, G., Lee, J., Elias, D., Gravel, M., Gutierrez, P., Ekiel, I., Braun, P. E., and Gehring, K. (2003) Structural evidence that brain cyclic nucleotide phosphodiesterase is a member of the 2H phosphodiesterase superfamily. J. Biol. Chem. 278, 46021-46028
19. Lappe-Siefke, C, Goebbels, S., Gravel, M., Nicksch, E., Lee, J., Braun, P. E., Griffiths, I. R., and Nave, K. A. (2003) Disruption of Cnp1 uncouples oligodendroglial functions in axonal support and myelination. Nat. Genet. 33, 366-374
20. Muraro, P. A., Kalbus, M., Afshar, G., McFarland, H. F., and Martin, R. (2002) T cell response to 2',3'-cyclic nucleotide 3'-phosphodiesterase (CNPase) in multiple sclerosis patients. J. Neuroimmunol. 130, 233-242
21. Rösener, M., and Muraro., P. A., Riethmüller, A., Kalbus, M., Sappler, G., Thompson, R. J., Lichtenfels, R., Sommer, N, and McFarland., H. F., and Martin, R. (1997) 2',3'-cyclic nucleotide 3'-phosphodiesterase: a novel candidate autoantigen in demyelinating diseases. J. Neuroimmunol. 75, 28-34
22. Lamensa, J. W., and Moscarello, M. A. (1993) Deimination of human myelin basic protein by a peptidylarginine deiminase from bovine brain. J. Neurochem. 61, 987-996
23. Vossenaar, E. R., and Zendman., A. J., van Venrooij, W. J., and Pruijn, G. J. (2003) PAD, a growing family of citrullinating enzymes: genes, features and involvement in disease. BioEssays 25, 1106-1118
24. Wood, D. D., and Ackerley., C. A., Brand, B. v., Zhang, L., Raijmakers, R., and Mastronardi., F. G., and Moscarello, M. A. (2008) Myelin localization of peptidylarginine deiminases 2 and 4: comparison of PAD2 and PAD4 activities. Lab. Invest. 88, 354-364
25. Moscarello, M. A., and Wood., D. D., Ackerley, C, and Boulias, C. (1994) Myelin in multiple sclerosis is developmentally immature. J. Clin. Invest. 94, 146-154
26. Wood, D. D., and Bilbao., J. M., O'Connors, P., and Moscarello, M. A. (1996) Acute multiple sclerosis (Marburg type) is associated with developmentally immature myelin basic protein. Ann. Neurol. 40, 18-24
27. Kim, J. K., and Mastronardi., F. G., Wood, D. D., Lubman, D. M., Zand, R., and Moscarello, M. A. (2003) Multiple sclerosis: an important role for post-translational modifications of myelin basic protein in pathogenesis. Mol. Cell Proteomics 2, 453-462
28. Musse, A. A., and Harauz, G. (2007) Molecular "negativity" may underlie multiple sclerosis: Role of the myelin basic protein family in the pathogenesis of MS. Neurobiology of Multiple Sclerosis 79, 149-172
29. Mastronardi, F. G., Noor, A., Wood, D. D., Paton, T., and Moscarello, M. A. (2007) Peptidyl argininedeiminase 2 CpG island in multiple sclerosis white matter is hypomethylated. J. Neurosci. Res. 85, 2006-2016
30. Musse, A. A., Li, Z., Ackerley, C. A., Bienzle, D., Lei, H., Poma, R., Harauz, G., and Moscarello., M. A., and Mastronardi, F. G. (2008) Peptidylarginine deiminase 2 (PAD2) overexpression in transgenic mice leads to myelin loss in the central nervous system. Dis. Model Mech. 1, 229-240
31. Savill, J., and Fadok, V. (2000) Corpse clearance defines the meaning of cell death. Nature 407, 784-788
32. Stern, M., Savill, J., and Haslett, C. (1996) Human monocyte-derived macrophage phagocytosis of senescent eosinophils undergoing apoptosis. Mediation by α v β 3/CD36/thrombospondin recognition mechanism and lack of phlogistic response. Am. J. Pathol. 149, 911-921
33. Gorovoy, M., Gaultier, A., Campana, W. M., and 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
34. Studzinski, D. M., and Benjamins, J. A. (2003) Regulation of CNS glial phenotypes in N20.1 cells. J. Neurosci. Res. 73, 31-41
35. Norton, W. T., and Poduslo, S. E. (1973) Myelination in rat brain: method of myelin isolation. J. Neurochem. 21, 749-757
36. Gaultier, A., Simon, G., Niessen, S., Dix, M., Takimoto, S., Cravatt, B. F., 3rd, 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
37. Emonard, H, Bellon, G., Troeberg, L., Berton, A., Robinet, A., Henriet, P., Marbaix, E., Kirkegaard, K., Patthy, L., Eeckhout, Y., Nagase, H, Hornebeck, W., and Courtoy, P. J. (2004) Low density lipoprotein receptor-related protein mediates endocytic clearance of pro-MMP-2.TIMP-2 complex through a thrombospondin-independent mechanism. J. Biol. Chem. 279, 54944-54951
38. Hahn-Dantona, E., Ruiz, J. F., Bornstein, P., and Strickland, D. K. (2001) The low density lipoprotein receptor-related protein modulates levels of matrix metalloproteinase 9 (MMP-9) by mediating its cellular catabolism. J. Biol. Chem. 276, 15498-15503
39. Gravel, M., Peterson, J., Yong, V. W., Kottis, V., Trapp, B., and Braun, P. E. (1996) Overexpression of 2',3'-cyclic nucleotide 3'-phosphodiesterase in transgenic mice alters oligodendrocyte development and produces aberrant myelination. Mol. Cell Neurosci. 7, 453-466
40. Bifulco, M., Laezza, C, Stingo, S., and Wolff, J. (2002) 2',3'-Cyclic nucleotide 3'-phosphodiesterase: a membrane-bound, microtubule-associated protein and membrane anchor for tubulin. Proc. Natl. Acad. Sci. U.S.A. 99, 1807-1812
41. Adie, E. J., and Francis., M. J., Davies, J., Smith, L., Marenghi, A., Hather, C, Hadingham, K., Michael, N. P., Milligan, G., and Game, S. (2003) CypHer 5: a generic approach for measuring the activation and trafficking of G protein-coupled receptors in live cells. Assay Drug Dev. Technol. 1, 251-259
42. Henn, A., Lund, S., Hedtjam, M., Porzgen, P., and Leist, M. (2009) The suitability of BV2 cells as alternative model system for primary microglia cultures or animal experiments of brain inflammation. ALTEX 26, 83-94
43. Elliott, M. R., and Ravichandran, K. S. (2010) Clearance of apoptotic cells: implications in health and disease. J. Cell Biol. 189, 1059-1070
44. Mantuano, E., Inoue, G., Li, X., Takahashi, K., Gaultier, A., Gonias, S. L., and Campana, W. M. (2008) The hemopexin domain of matrix metalloproteinase-9 activates cell signaling and promotes migration of schwann cells by binding to low-density lipoprotein receptor-related protein. J. Neurosci. 28, 11571-11582
45. Miyaoka, Y., Tanaka, M., Imamura, T., Takada, S., and Miyajima, A. (2010) A novel regulatory mechanism for Fgf18 signaling involving cysteine-rich FGF receptor (Cfr) and S-like protein (Dlk). Development 137, 159-167
46. Hidalgo, A., and Peired., A. J., Wild, M. K., Vestweber, D., and Frenette, P. S. (2007) Complete identification of E-selectin ligands on neutrophils reveals distinct functions of PSGL-1, ESL-1, and CD44. Immunity 26, 477-489
47. Garner, C. C, Garner, A., Huber, G., Kozak, C, and Matus, A. (1990) Molecular cloning of microtubule-associated protein 1 (MAP1A) and microtubule-associated protein 5 (MAP1B): identification of distinct genes and their differential expression in developing brain. J. Neurochem. 55, 146-154
48. Buser, A. M., Erne, B., Werner, H. B., and Nave., K. A., and Schaeren-Wiemers, N. (2009) The septin cytoskeleton in myelinating glia. Mol. Cell Neurosci. 40, 156-166
49. Hall, P. A., and Russell, S. E. (2012) Mammalian septins: dynamic hetero-mers with roles in cellular morphogenesis and compartmentalization. The Journal of pathology 226, 287-299
50. Bauer, N. G., Richter-Landsberg, C, and Ffrench-Constant, C. (2009) Role of the oligodendroglial cytoskeleton in differentiation and myelination. Glia 57, 1691-1705