LDL receptor-related protein 1 regulates the abundance of diverse cell-signaling proteins in the plasma membrane proteome

Journal of Proteome Research

Volumn 9, Issue 12, 2010, Pages 6689-6695

  Gaultier, Alban ^a   Simon, Gabriel ^b   Niessen, Sherry ^b   Dix, Melissa ^b   Takimoto, Shinako ^a   Cravatt, Benjamin F ^b   Gonias, Steven L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; NEUROPILIN 1; PROTEINASE K; PROTEOME; SEMAPHORIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL LINE; CELL MEMBRANE; CONTROLLED STUDY; GENE SILENCING; IMMUNOPRECIPITATION; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; SIGNAL TRANSDUCTION;

ANIMALS; CELL LINE; CELL MEMBRANE; CHO CELLS; CHROMATOGRAPHY, LIQUID; CRICETINAE; CRICETULUS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; LIVER; MACROPHAGES; MASS SPECTROMETRY; MEMBRANE MICRODOMAINS; MEMBRANE PROTEINS; MICE; NERVE TISSUE PROTEINS; NEUROPILIN-1; PROTEIN BINDING; PROTEOMICS; RECEPTORS, CELL SURFACE; RECEPTORS, LDL; RNA INTERFERENCE; SEMAPHORINS; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEINS;

EID: 78649807482     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr1008288     Document Type: Article

References (64)

1. Strickland, D. K.; Gonias, S. L.; Argraves, W. S. Diverse roles for the LDL receptor family Trends Endocrinol. Metab. 2002, 13 (2) 66-74
2. Mantuano, E.; Inoue, G.; Li, X.; Takahashi, K.; Gaultier, A.; Gonias, S. L.; Campana, W. M. 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. 2008, 28 (45) 11571-82
3. Qiu, Z.; Hyman, B.; Rebeck, G. Apolipoprotein E receptors mediate neurite outgrowth through activation of p44/42 mitogen-activated protein kinase in primary neurons J. Biol. Chem. 2004, 279 (33) 34948-56
4. Shi, Y.; Mantuano, E.; Inoue, G.; Campana, W. M.; Gonias, S. L. Ligand binding to LRP1 transactivates Trk receptors by a Src family kinase-dependent pathway Sci. Signal. 2009, 2 (68) ra18
5. Zhang, X.; Polavarapu, R.; She, H.; Mao, Z.; Yepes, M. Tissue-type plasminogen activator and the low-density lipoprotein receptor-related protein mediate cerebral ischemia-induced nuclear factor-kappaB pathway activation Am. J. Pathol. 2007, 171 (4) 1281-90
6. Zhuo, M.; Holtzman, D. M.; Li, Y.; Osaka, H.; DeMaro, J.; Jacquin, M.; Bu, G. Role of tissue plasminogen activator receptor LRP in hippocampal long-term potentiation J. Neurosci. 2000, 20 (2) 542-9
7. Boucher, P.; Gotthardt, M.; Li, W. P.; Anderson, R. G.; Herz, J. LRP: role in vascular wall integrity and protection from atherosclerosis Science 2003, 300 (5617) 329-32
8. Gaultier, A.; Arandjelovic, S.; Niessen, S.; Overton, C. D.; Linton, M. F.; Fazio, S.; Campana, W. M.; Cravatt, B. F., 3rd; Gonias, S. L. Regulation of tumor necrosis factor receptor-1 and the IKK-NF-kappaB pathway by LDL receptor-related protein explains the antiinflammatory activity of this receptor Blood 2008, 111 (11) 5316-25
9. Webb, D.; Thomas, K.; Gonias, S. 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. 2001, 152 (4) 741-752
10. Zurhove, K.; Nakajima, C.; Herz, J.; Bock, H. H.; May, P. Gamma-secretase limits the inflammatory response through the processing of LRP1 Sci. Signal. 2008, 1 (47) ra15
11. Muratoglu, S. C.; Mikhailenko, I.; Newton, C.; Migliorini, M.; Strickland, D. K. The LDL receptor-related protein 1 (LRP1) forms a signaling complex with the PDGF receptor-{beta} in endosomes and regulates activation of the mapk pathway J. Biol. Chem. 2010, 285, 14308-14317
12. Campana, W. M.; Li, X.; Dragojlovic, N.; Janes, J.; Gaultier, A.; Gonias, S. L. The low-density lipoprotein receptor-related protein is a pro-survival receptor in Schwann cells: possible implications in peripheral nerve injury J. Neurosci. 2006, 26 (43) 11197-207
13. Hayashi, H.; Campenot, R. B.; Vance, D. E.; Vance, J. E. Apolipoprotein E-containing lipoproteins protect neurons from apoptosis via a signaling pathway involving low-density lipoprotein receptor-related protein-1 J. Neurosci. 2007, 27 (8) 1933-41
14. Hu, K.; Yang, J.; Tanaka, S.; Gonias, S. L.; Mars, W. M.; Liu, Y. Tissue-type Plasminogen Activator Acts as a Cytokine That Triggers Intracellular Signal Transduction and Induces Matrix Metalloproteinase-9 Gene Expression J. Biol. Chem. 2006, 281 (4) 2120-7
15. Ma, Z.; Thomas, K. S.; Webb, D. J.; Moravec, R.; Salicioni, A. M.; Mars, W. M.; Gonias, S. L. Regulation of Rac1 activation by the low density lipoprotein receptor-related protein J. Cell Biol. 2002, 159 (6) 1061-70
16. Qiu, Z.; Strickland, D. K.; Hyman, B. T.; Rebeck, G. W. alpha 2-Macroglobulin exposure reduces calcium responses to N-methyl-D-aspartate via low density lipoprotein receptor-related protein in cultured hippocampal neurons J. Biol. Chem. 2002, 277 (17) 14458-66
17. Yepes, M.; Sandkvist, M.; Moore, E. G.; Bugge, T. H.; Strickland, D. K.; Lawrence, D. A. Tissue-type plasminogen activator induces opening of the blood-brain barrier via the LDL receptor-related protein J. Clin. Invest. 2003, 112 (10) 1533-40
18. Conese, M.; Nykjaer, A.; Petersen, C. M.; Cremona, O.; Pardi, R.; Andreasen, P. A.; Gliemann, J.; Christensen, E. I.; Blasi, F. alpha-2 Macroglobulin receptor/Ldl receptor-related protein(Lrp)-dependent internalization of the urokinase receptor J. Cell Biol. 1995, 131 (6 Pt 1) 1609-22
19. Hamik, A.; Setiadi, H.; Bu, G.; McEver, R. P.; Morrissey, J. H. Down-regulation of monocyte tissue factor mediated by tissue factor pathway inhibitor and the low density lipoprotein receptor-related protein J. Biol. Chem. 1999, 274 (8) 4962-9
20. Pietrzik, C. Y. I. S.; Jaeger, S.; Busse, T.; Weggen, S.; Koo, E. FE65 constitutes the functional link between the low-density lipoprotein receptor-related protein and the amyloid precursor protein J. Neurosci. 2004, 24 (17) 4259-65
21. Ulery, P. G.; Beers, J.; Mikhailenko, I.; Tanzi, R. E.; Rebeck, G. W.; Hyman, B. T.; Strickland, D. K. Modulation of beta-amyloid precursor protein processing by the low density lipoprotein receptor-related protein (LRP). Evidence that LRP contributes to the pathogenesis of Alzheimer's disease J. Biol. Chem. 2000, 275 (10) 7410-5
22. Parkyn, C. J.; Vermeulen, E. G.; Mootoosamy, R. C.; Sunyach, C.; Jacobsen, C.; Oxvig, C.; Moestrup, S.; Liu, Q.; Bu, G.; Jen, A.; Morris, R. J. LRP1 controls biosynthetic and endocytic trafficking of neuronal prion protein J. Cell Sci. 2008, 121 (Pt 6) 773-83
23. Gaultier, A.; Salicioni, A. M.; Arandjelovic, S.; Gonias, S. L. Regulation of the composition of the extracellular matrix by low density lipoprotein receptor-related protein-1: activities based on regulation of mRNA expression J. Biol. Chem. 2006, 281 (11) 7332-40
24. Overton, C. D.; Yancey, P. G.; Major, A. S.; Linton, M. F.; Fazio, S. Deletion of macrophage LDL receptor-related protein increases atherogenesis in the mouse Circ. Res. 2007, 100 (5) 670-7
25. Montel, V.; Gaultier, A.; Lester, R. D.; Campana, W. M.; Gonias, S. L. The low-density lipoprotein receptor-related protein regulates cancer cell survival and metastasis development Cancer Res. 2007, 67 (20) 9817-24
26. Cordwell, S.; Thingholm, T. Technologies for plasma membrane proteomics Proteomics 2009, 10, 611-627
27. Wu, C.; Yates, J. The application of mass spectrometry to membrane proteomics Nat. Biotechnol. 2003, 21 (3) 2627
28. Bledi, Y.; Inberg, A.; Linial, M. PROCEED: A proteomic method for analysing plasma membrane proteins in living mammalian cells Brief Funct. Genomic Proteomic 2003, 2 (3) 254-65
29. Gaultier, A.; Wu, X.; Le Moan, N.; Takimoto, S.; Mukandala, G.; Akassoglou, K.; Campana, W. M.; Gonias, S. L. Low-density lipoprotein receptor-related protein 1 is an essential receptor for myelin phagocytosis J. Cell Sci. 2009, 122 (Pt 8) 1155-62
30. Salicioni, A. M.; Gaultier, A.; Brownlee, C.; Cheezum, M. K.; Gonias, S. L. Low density lipoprotein receptor-related protein-1 promotes beta1 integrin maturation and transport to the cell surface J. Biol. Chem. 2004, 279 (11) 10005-12
31. FitzGerald, D. J.; Fryling, C. M.; Zdanovsky, A.; Saelinger, C. B.; Kounnas, M.; Winkles, J. A.; Strickland, D.; Leppla, S. Pseudomonas exotoxin-mediated selection yields cells with altered expression of low-density lipoprotein receptor-related protein J. Cell Biol. 1995, 129 (6) 1533-41
32. Hussaini, I. M.; Brown, M. D.; Weaver, A. M.; Carpenter, J.; Karns, L. R.; Vandenberg, S. R.; Gonias, S. L. Stable antisense RNA expression neutralizes the activity of low-density lipoprotein receptor-related protein and promotes urokinase accumulation in the medium of an astrocytic tumor cell line Antisense. Nucleic Acid Drug Dev. 1999, 9 (2) 183-90
33. Dix, M. M.; Simon, G. M.; Cravatt, B. F. Global mapping of the topography and magnitude of proteolytic events in apoptosis Cell 2008, 134 (4) 679-91
34. Tabb, D. L.; McDonald, W. H.; Yates, J. R., 3rd DTASelect and Contrast: tools for assembling and comparing protein identifications from shotgun proteomics J. Proteome Res. 2002, 1 (1) 21-6
35. Barnes, H.; Larsen, B.; Tyers, M.; van Der Geer, P. Tyrosine- phosphorylated low density lipoprotein receptor-related protein 1 (Lrp1) associates with the adaptor protein SHC in SRC-transformed cells J. Biol. Chem. 2001, 276 (22) 19119-25
36. Gonias, S. L.; Wu, L.; Salicioni, A. M. Low density lipoprotein receptor-related protein: regulation of the plasma membrane proteome Thromb. Haemost. 2004, 91 (6) 1056-64
37. Webb, D. J.; Nguyen, D. H.; Sankovic, M.; Gonias, S. L. The very low density lipoprotein receptor regulates urokinase receptor catabolism and breast cancer cell motility in vitro J. Biol. Chem. 1999, 274 (11) 7412-20
38. Herz, J.; Clouthier, D. E.; Hammer, R. E. LDL receptor-related protein internalizes and degrades uPA-PAI-1 complexes and is essential for embryo implantation Cell 1992, 71 (3) 411-21
39. 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.; Herz, J. Neuronal LRP1 functionally associates with postsynaptic proteins and is required for normal motor function in mice Mol. Cell. Biol. 2004, 24 (20) 8872-83
40. May, P.; Woldt, E.; Matz, R. L.; Boucher, P. The LDL receptor-related protein (LRP) family: an old family of proteins with new physiological functions Ann. Med. 2007, 39 (3) 219-28
41. May, P.; Reddy, Y. K.; Herz, J. Proteolytic processing of low density lipoprotein receptor-related protein mediates regulated release of its intracellular domain J. Biol. Chem. 2002, 277 (21) 18736-43
42. Boucher, P.; Liu, P.; Gotthardt, M.; Hiesberger, T.; Anderson, R. G.; Herz, J. Platelet-derived growth factor mediates tyrosine phosphorylation of the cytoplasmic domain of the low Density lipoprotein receptor-related protein in caveolae J. Biol. Chem. 2002, 277 (18) 15507-13
43. Kolodkin, A. L.; Matthes, D. J.; Goodman, C. S. The semaphorin genes encode a family of transmembrane and secreted growth cone guidance molecules Cell 1993, 75 (7) 1389-99
44. Behar, O.; Golden, J. A.; Mashimo, H.; Schoen, F. J.; Fishman, M. C. Semaphorin III is needed for normal patterning and growth of nerves, bones and heart Nature 1996, 383 (6600) 525-8
45. Suzuki, K.; Kumanogoh, A.; Kikutani, H. Semaphorins and their receptors in immune cell interactions Nat. Immunol. 2008, 9 (1) 17-23
46. Serini, G.; Valdembri, D.; Zanivan, S.; Morterra, G.; Burkhardt, C.; Caccavari, F.; Zammataro, L.; Primo, L.; Tamagnone, L.; Logan, M.; Tessier-Lavigne, M.; Taniguchi, M.; Puschel, A. W.; Bussolino, F. Class 3 semaphorins control vascular morphogenesis by inhibiting integrin function Nature 2003, 424 (6947) 391-7
47. Shi, W.; Kumanogoh, A.; Watanabe, C.; Uchida, J.; Wang, X.; Yasui, T.; Yukawa, K.; Ikawa, M.; Okabe, M.; Parnes, J. R.; Yoshida, K.; Kikutani, H. The class IV semaphorin CD100 plays nonredundant roles in the immune system: defective B and T cell activation in CD100-deficient mice Immunity 2000, 13 (5) 633-42
48. Hall, K. T.; Boumsell, L.; Schultze, J. L.; Boussiotis, V. A.; Dorfman, D. M.; Cardoso, A. A.; Bensussan, A.; Nadler, L. M.; Freeman, G. J. Human CD100, a novel leukocyte semaphorin that promotes B-cell aggregation and differentiation Proc. Natl. Acad. Sci. U.S.A. 1996, 93 (21) 11780-5
49. Sierra, J. R.; Corso, S.; Caione, L.; Cepero, V.; Conrotto, P.; Cignetti, A.; Piacibello, W.; Kumanogoh, A.; Kikutani, H.; Comoglio, P. M.; Tamagnone, L.; Giordano, S. Tumor angiogenesis and progression are enhanced by Sema4D produced by tumor-associated macrophages J. Exp. Med. 2008, 205 (7) 1673-85
50. Sun, Q.; Zhou, H.; Binmadi, N. O.; Basile, J. R. Hypoxia-inducible factor-1-mediated regulation of semaphorin 4D affects tumor growth and vascularity J. Biol. Chem. 2009, 284 (46) 32066-74
51. Zhu, L.; Bergmeier, W.; Wu, J.; Jiang, H.; Stalker, T. J.; Cieslak, M.; Fan, R.; Boumsell, L.; Kumanogoh, A.; Kikutani, H.; Tamagnone, L.; Wagner, D. D.; Milla, M. E.; Brass, L. F. Regulated surface expression and shedding support a dual role for semaphorin 4D in platelet responses to vascular injury Proc. Natl. Acad. Sci. U.S.A. 2007, 104 (5) 1621-6
52. Lee, H. K.; Bae, H. R.; Park, H. K.; Seo, I. A.; Lee, E. Y.; Suh, D. J.; Park, H. T. Cloning, characterization and neuronal expression profiles of tumor endothelial marker 7 in the rat brain Brain Res. Mol. Brain Res. 2005, 136 (1-2) 189-98
53. St Croix, B.; Rago, C.; Velculescu, V.; Traverso, G.; Romans, K. E.; Montgomery, E.; Lal, A.; Riggins, G. J.; Lengauer, C.; Vogelstein, B.; Kinzler, K. W. Genes expressed in human tumor endothelium Science 2000, 289 (5482) 1197-202
54. Beaty, R. M.; Edwards, J. B.; Boon, K.; Siu, I. M.; Conway, J. E.; Riggins, G. J. PLXDC1 (TEM7) is identified in a genome-wide expression screen of glioblastoma endothelium J. Neurooncol. 2007, 81 (3) 241-8
55. Lee, H. K.; Seo, I. A.; Park, H. K.; Park, Y. M.; Ahn, K. J.; Yoo, Y. H.; Park, H. T. Nidogen is a prosurvival and promigratory factor for adult Schwann cells J. Neurochem. 2007, 102 (3) 686-98
56. Halloran, M. C.; Wolman, M. A. Repulsion or adhesion: receptors make the call Curr. Opin. Cell. Biol. 2006, 18 (5) 533-40
57. Soker, S.; Takashima, S.; Miao, H. Q.; Neufeld, G.; Klagsbrun, M. Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor Cell 1998, 92 (6) 735-45
58. Fukasawa, M.; Matsushita, A.; Korc, M. Neuropilin-1 interacts with integrin beta1 and modulates pancreatic cancer cell growth, survival and invasion Cancer Biol. Ther. 2007, 6 (8) 1173-80
59. Matsushita, A.; Gotze, T.; Korc, M. Hepatocyte growth factor-mediated cell invasion in pancreatic cancer cells is dependent on neuropilin-1 Cancer Res. 2007, 67 (21) 10309-16
60. Ji, J. D.; Park-Min, K. H.; Ivashkiv, L. B. Expression and function of semaphorin 3A and its receptors in human monocyte-derived macrophages Hum. Immunol. 2009, 70 (4) 211-7
61. Hussaini, I. M.; Srikumar, K.; Quesenberry, P. J.; Gonias, S. L. Colony-stimulating factor-1 modulates alpha 2-macroglobulin receptor expression in murine bone marrow macrophages J. Biol. Chem. 1990, 265 (32) 19441-6
62. Brown, M. D.; Banker, G. A.; Hussaini, I. M.; Gonias, S. L.; VandenBerg, S. R. Low density lipoprotein receptor-related protein is expressed early and becomes restricted to a somatodendritic domain during neuronal differentiation in culture Brain Res. 1997, 747 (2) 313-7
63. Feng, W.; Zhang, M. Organization and dynamics of PDZ-domain-related supramodules in the postsynaptic density Nat. Rev. Neurosci. 2009, 10 (2) 87-99
64. Gotthardt, M.; Trommsdorff, M.; Nevitt, M. F.; Shelton, J.; Richardson, J. A.; Stockinger, W.; Nimpf, J.; Herz, J. Interactions of the low density lipoprotein receptor gene family with cytosolic adaptor and scaffold proteins suggest diverse biological functions in cellular communication and signal transduction J. Biol. Chem. 2000, 275 (33) 25616-24