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

Volumn 111, Issue 11, 2008, Pages 5316-5325

  Gaultier, Alban ^a   Arandjelovic, Sanja ^a   Niessen, Sherry ^b   Overton, Cheryl D ^c   Linton, MacRae F ^c   Fazio, Sergio ^c   Campana, W Marie ^d   Cravatt III, Benjamin F ^b   Gonias, Steven L ^a,e  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d University of California   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; COMPLEMENT; COMPLEMENT COMPONENT C1R; COMPLEMENT COMPONENT C1S; COMPLEMENTARY DNA; CYTOKINE; I KAPPA B KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOGLOBULIN G; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 6; IODINE 125; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; LUCIFERASE; MONOCYTE CHEMOTACTIC PROTEIN 1; PROTEINASE; RECOMBINANT TUMOR NECROSIS FACTOR ALPHA; RNA; SERINE DEHYDRATASE; SODIUM IODIDE; TUMOR NECROSIS FACTOR RECEPTOR 1; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN ASSOCIATED PROTEIN; MESSENGER RNA;

ANIMAL CELL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; COMPLEMENT ACTIVATION; CONTROLLED STUDY; ENDOCYTOSIS; ENZYME ACTIVATION; ENZYME ASSAY; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; IMMUNOBLOTTING; INFLAMMATION; INTERNALIZATION; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; POLYACRYLAMIDE GEL ELECTROPHORESIS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; ANIMAL; CELL CULTURE; FLOW CYTOMETRY; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CELLS, CULTURED; COMPLEMENT ACTIVATION; COMPLEMENT SYSTEM PROTEINS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ELECTROPHORETIC MOBILITY SHIFT ASSAY; FLOW CYTOMETRY; GENE EXPRESSION; GENE EXPRESSION REGULATION; I-KAPPA B KINASE; INFLAMMATION; LDL-RECEPTOR RELATED PROTEIN-ASSOCIATED PROTEIN; MICE; NF-KAPPA B; POLYMERASE CHAIN REACTION; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE I; RNA, MESSENGER; SIGNAL TRANSDUCTION;

EID: 45949089484     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2007-12-127613     Document Type: Article

References (67)

1. Strickland DK, Gonias SL, Argraves WS. Diverse roles for the LDL receptor family. Trends Endocrinol Metab. 2002;13:66-74.
2. Herz J, Hamann U, Rogne S, Myklebost O, Gausepohl H, Stanley KK. 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. EMBO J. 1988;7:4119-4127.
3. Strickland DK, Ashcom JD, Williams S, Burgess WH, Migliorini M, Argraves WS. Sequence identity between the alpha 2-macroglobulin receptor and low density lipoprotein receptor-related protein suggests that this molecule is a multifunctional receptor. J Biol Chem. 1990;265:17401-17404.
4. Gonias SL, Wu L, Salicioni AM. Low density lipoprotein receptor-related protein: regulation of the plasma membrane proteome. Thromb Haemost. 2004;91:1056-1064.
5. Ma Z, Thomas KS, Webb DJ, et al. Regulation of Rac1 activation by the low density lipoprotein receptor-related protein. J Cell Biol. 2002;159: 1061-1070.
6. Webb DJ, Nguyen DH, Gonias SL. Extracellular signal-regulated kinase functions in the urokinase receptor-dependent pathway by which neutralization of low density lipoprotein receptor-related protein promotes fibrosarcoma cell migration and matrigel invasion. J Cell Sci. 2000;113:123-134.
7. Willnow TE, Herz J. Genetic deficiency in low density lipoprotein receptor-related protein confers cellular resistance to Pseudomonas exotoxin A: evidence that this protein is required for uptake and degradation of multiple ligands. J Cell Sci. 1994;107:719-726.
8. Willnow TE, Moehring JM, Inocencio NM, Moehring TJ, Herz J. The low-density-lipoprotein receptor-related protein (LRP) is processed by furin in vivo and in vitro. Biochem J. 1996;313:71-76.
9. Mikhailenko I, Battey FD, Migliorini M, et al. Recognition of alpha 2-macroglobulin by the low density lipoprotein receptor-related protein requires the cooperation of two ligand binding cluster regions. J Biol Chem. 2001;276:39484-39491.
10. Bacskai BJ, Xia MQ, Strickland DK, Rebeck GW, Hyman BT. The endocytic receptor protein LRP also mediates neuronal calcium signaling via N-methyl-D-aspartate receptors. Proc Natl Acad Sci USA. 2000;97:11551-11556.
11. Hu K, Yang J, Tanaka S, Gonias SL, Mars WM, Liu Y. Tissue-type plasminogen activator acts as a cytokine that triggers intracellular signal transduction and induces matrix met alloproteinase-9 gene expression. J Biol Chem. 2006;281:2120-2127.
12. Zhu Y, Hui DY. Apolipoprotein E binding to low density lipoprotein receptor-related protein-1 inhibits cell migration via activation of cAMP-dependent protein kinase A. J Biol Chem. 2003;278:36257-36263.
13. Barnes H, Ackermann EJ, van der Geer P. v-Src
14. induces Shc binding to tyrosine 63 in the cytoplasmic domain of the LDL receptor-related protein 1. Oncogene. 2003;22:3589-3597.
15. Gotthardt M, Trommsdorff M, Nevitt MF, et al. 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;275:25616-25624.
16. Lutz C, Nimpf J, Jenny M, et al. Evidence of functional modulation of the MEKK/JNK/cJun signaling cascade by the low density lipoprotein receptor-related protein (LRP). J Biol Chem. 2002;277:43143-43151.
17. Loukinova E, Ranganathan S, Kuznetsov S, et al. Platelet-derived growth factor (PDGF)-induced tyrosine phosphorylation of the low density lipoprotein receptor-related protein (LRP): evidence for integrated co-receptor function between LRP and the PDGF. J Biol Chem. 2002;277:15499-15506.
18. Campana WM, Li X, Dragojlovic N, Janes J, Gaultier A, Gonias SL. The low-density lipoprotein receptor-related protein is a pro-survival receptor in Schwann cells: possible implications in peripheral nerve injury. J Neurosci. 2006;26:11197-11207.
19. Gaultier A, Salicioni AM, Arandjelovic S, Gonias SL. Regulation of the composition of the extracellular matrix by low density lipoprotein receptor-related protein-1. J Biol Chem. 2006;281:7332-7340.
20. Orr AW, Elzie CA, Kucik DF, Murphy-Ullrich JE. Thrombospondin signaling through the calreticulin/LDL receptor-related protein co-complex stimulates random and directed cell migration. J Cell Sci. 2003;116:2917-2927.
21. Overton CD, Yancey PG, Major AS, Linton MF, Fazio S. Deletion of macrophage LDL receptor-related protein increases atherogenesis in the mouse. Circ Res. 2007;100:670-677.
22. Boucher P, Gotthardt M, Li WP, Anderson RG, Herz J. LRP: role in vascular wall integrity and protection from atherosclerosis. Science. 2003;300:329-332.
23. Gaultier A, Arandjelovic S, Li X, et al. A shed form of low density lipoprotein receptor-related protein regulates peripheral nerve injury and neuropathic pain. J Clin Invest. 2008;118:167-172.
24. Jessani N, Liu Y, Humphrey M, Cravatt BF. Enzyme activity profiles of the secreted and membrane proteome that depict cancer cell invasiveness. Proc Natl Acad Sci USA. 2002;99:10335-10340.
25. Duncan RC, Wijeyewickrema LC, Pike RN. The initiating proteases of the complement system: controlling the cleavage. Biochimie. 2008;90:387-395.
26. Baud V, Karin M. Signal transduction bytumor necrosis factor and its relatives. Trends Cell Biol. 2001;11:372-377.
27. Karin M, Greten FR. NF-kappa B: linking inflammation and immunity to cancer development and progression. Nat RevImmunol. 2005;5:749-759.
28. Karin M, Lawrence T, Nizet V. Innate immunity gone awry: linking microbial infections to chronic inflammation and cancer. Cell. 2006;124:823-835.
29. Webb DJ, Hussaini IM, Weaver AM, et al. Activated alpha 2-macroglobulin promotes mitogenesis in rat vascular smooth muscle cells by a mechanism that is independent of growth-factor-carrier activity. Eur J Biochem. 1995;234:714-722.
30. Salicioni AM, Mizelle KS, Loukinova E, Mikhailenko I, Strickland DK, Gonias SL. The low density lipoprotein receptor-related protein mediates fibronectin catabolism and inhibits fibronectin accumulation on cell surfaces. J Biol Chem. 2002;277:16160-16166.
31. Montel V, Gaultier A, Lester RD, Campana WM, Gonias SL. The low-density lipoprotein receptor-related protein regulates cancer cell survival and metastasis development. Cancer Res. 2007;67:9817-9824.
32. Kidd D, Liu Y, Cravatt BF. Profiling serine hydrolase activities in complex proteomes. Biochemistry. 2001;40:4005-4015.
33. Jessani N, Niessen S, Wei BQ, et al. Astream-lined platform for high-content functional proteomics of primary human specimens. Nat Methods. 2005;2:691-697.
34. Thellin O, Zorzi W, Lakaye B, et al. Housekeeping genes as internal standards: use and limits. J Biotechnol. 1999;75:291-295.
35. Gaultier A, Cousin H, Darribere T, Alfandari D. ADAM13 disintegrin and cysteine-rich domains bind to the second heparin-binding domain of fibronectin. J Biol Chem. 2002;277:23336-23344.
36. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227:680-685.
37. Ameloot P, Fiers W, De Bleser P, Ware CF, Van-denabeele P, Brouckaert P. Identification of tumor necrosis factor (TNF) amino acids crucial for binding to the murine p75 TNF receptor and construction of receptor-selective mutants. J Biol Chem. 2001;276:37426-37430.
38. Liu Y, Patricelli MP, Cravatt BF. Activity-based protein profiling: the serine hydrolases. Proc Natl Acad Sci USA. 1999;96:14694-14699.
39. Kounnas MZ, Henkin J, Argraves WS, Strickland DK. Low density lipoprotein receptor-related protein/alpha 2-macroglobulin receptor mediates cellular uptake of pro-urokinase. J Biol Chem. 1993;268:21862-21867.
40. Willnow TE, Orth K, Herz J. Molecular dissection of ligand binding sites on the low density lipoprotein receptor-related protein. J Biol Chem. 1994;269:15827-15832.
41. Storm D, Herz J, Trinder P, Loos M. C1 inhibitor-C1s complexes are internalized and degraded by the low density lipoprotein receptor-related protein. J Biol Chem. 1997;272:31043-31050.
42. Dewan A, Liu M, Hartman S, et al. HTRA1 promoter polymorphism in wet age-related macular degeneration. Science. 2006;314:989-992.
43. Oka C, Tsujimoto R, Kajikawa M, et al. HtrA1 serine protease inhibits signaling mediated by Tgfbeta family proteins. Development. 2004;131:1041-1053.
44. Budayova-Spano M, Lacroix M, Thielens NM, Arlaud GJ, Fontecilla-Camps JC, Gaboriaud C. The crystal structure of the zymogen catalytic domain of complement protease C1r reveals that a disruptive mechanical stress is required to trigger activation oftheC1 complex. EMBO J. 2002;21:231-239.
45. Budayova-Spano M, Grabarse W, Thielens NM, et al. Monomeric structures of the zymogen and active catalytic domain of complement protease c1r: further insights into the c1 activation mechanism. Structure. 2002;10:1509-1519.
46. Sim RB, Reboul A, Arlaud GJ, Villiers CL, Colomb MG. Interaction of125I-labelled complementsub-components C-1r and C-1s with protease inhibitors in plasma. FEBS Lett. 1979;97:111-115.
47. Herz J, Strickland DK. LRP: a multifunctional scavenger and signaling receptor. J Clin Invest. 2001;108:779-784.
48. Shin HM, Kim MH, Kim BH, et al. Inhibitory action of novel aromatic diamine compound on lipopoly-saccharide-induced nuclear translocation of NF-kappaB without affecting IkappaB degradation. FEBS Lett. 2004;571:50-54.
49. Karin M. How NF-kappaB is activated: the role of
50. the IkappaB kinase (IKK) complex. Oncogene. 1999;18:6867-6874.
51. Karin M, Ben-Neriah Y. Phosphorylation meets ubiquitination: the control of NF-[kappa]B activity. Annu Rev Immunol. 2000;18:621-663.
52. Viatour P, Merville MP, Bours V, Chariot A. Phos-phorylation of NF-kappaB and IkappaB proteins: implications in cancer and inflammation. Trends Biochem Sci. 2005;30:43-52.
53. Yang M, Huang H, Li J, Li D, Wang H. Tyrosine phosphorylation of the LDL receptor-related protein (LRP) and activation of the ERK pathway are required for connective tissue growth factor to potentiate myofibroblast differentiation. FASEB J. 2004;18:1920-1921.
54. Conese M, Nykjaer A, Petersen CM, et al. alpha-2 Macroglobulin receptor/Ldl receptor-related protein (Lrp)-dependent internalization of the urokinase receptor. J Cell Biol. 1995;131:1609-1622.
55. Chan FK, Chun HJ, Zheng L, Siegel RM, Bui KL, Lenardo MJ. A domain in TNF receptors that mediates ligand-independent receptor assembly and signaling. Science. 2000;288:2351-2354.
56. Yu G, Rux AH, Ma P, Bdeir K, Sachais BS. Endothelial expression of E-selectin is induced by the platelet-specific chemokine platelet factor 4 through LRP in an NF-kappaB-dependent manner. Blood. 2005;105:3545-3551.
57. 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;171:1281-1290.
58. Karin M, Lin A. NF-kappaB at the crossroads of life and death. Nat Immunol. 2002;3:221-227.
59. Sizemore N, Leung S, Stark GR. Activation of phosphatidylinositol 3-kinase in response to interleukin-1 leads to phosphorylation and activation of the NF-kappaB p65/RelAsubunit. Mol Cell Biol. 1999;19:4798-4805.
60. Frank MM, Fries LF. The role of complement in inflammation and phagocytosis. Immunol Today. 1991;12:322-326.
61. Gaboriaud C, Thielens NM, Gregory LA, Rossi V, Fontecilla-Camps JC, Arlaud GJ. Structure and activation of the C1 complex of complement: unraveling the puzzle. Trends Immunol. 2004;25:368-373.
62. Sim RB, Tsiftsoglou SA. Proteases of the complement system. Biochem Soc Trans. 2004;32:21-27.
63. Meilinger M, Gschwentner C, Burger I, et al. Metabolism of activated complement component C3 is mediated by the low density lipoprotein receptor-related protein/alpha(2)-macroglobulin receptor. J Biol Chem. 1999;274:38091-38096.
64. Hussaini IM, LaMarre J, Lysiak JJ, Karns LR, VandenBerg SR, Gonias SL. Transcriptional regulation of LDL receptor-related protein by IFN-gamma and the antagonistic activity of TGF-beta(1) in the RAW 264.7 macrophage-like cell line. J Leukoc Biol. 1996;59:733-739.
65. LaMarre J, Wolf BB, Kittler EL, Quesenberry PJ, Gonias SL. Regulation of macrophage alpha 2-macroglobulin receptor/low density lipoprotein receptor-related protein by lipopolysaccharide and interferon-gamma. J Clin Invest. 1993;91:1219-1224.
66. Gasque P, Ischenko A, Legoedec J, Mauger C, Schouft MT, Fontaine M. Expression of the complement classical pathway by human glioma in culture: a model for complement expression by nerve cells. J Biol Chem. 1993;268:25068-25074.
67. Schmaier AH, Amenta S, Xiong T, Heda GD, GewirtzAM. Expression of platelet C1 inhibitor. Blood. 1993;82:465-474.