TWEAK/Fn14 pathway: An immunological switch for shaping tissue responses

Immunological Reviews

Volumn 244, Issue 1, 2011, Pages 99-114

  Burkly, Linda C ^a   Michaelson, Jennifer S ^a   Zheng, Timothy S ^a  

^a BIOGEN   (United States)

Author keywords

Disease; Fn14; Immune system; Inflammation; Tissue responses; TWEAK

Indexed keywords

FIBROBLAST GROWTH FACTOR INDUCIBLE MOLECULE 14; RECEPTOR PROTEIN; STRESS ACTIVATED PROTEIN KINASE; TOLL LIKE RECEPTOR; TUMOR NECROSIS FACTOR LIKE WEAK INDUCER OF APOPTOSIS; UNCLASSIFIED DRUG;

ACUTE KIDNEY FAILURE; ANGIOGENESIS; CATABOLISM; CELL PROLIFERATION; CHRONIC GRAFT VERSUS HOST DISEASE; FIBROSIS; HUMAN; IMMUNOPATHOLOGY; INFLAMMATION; KIDNEY DISEASE; KIDNEY FIBROSIS; LIVER REGENERATION; LUPUS ERYTHEMATOSUS NEPHRITIS; MUSCLE REGENERATION; NERVE CELL; PARENCHYMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; STEM CELL; STROMA CELL; TISSUE INJURY; TISSUE REACTION;

ANIMALS; APOPTOSIS; DENDRITIC CELLS; ENDOTHELIAL CELLS; EPITHELIAL CELLS; GENE EXPRESSION; HUMANS; IMMUNITY, INNATE; INFLAMMATION; KILLER CELLS, NATURAL; MICE; MICE, TRANSGENIC; MUSCLE, SKELETAL; RECEPTORS, TUMOR NECROSIS FACTOR; SIGNAL TRANSDUCTION; STEM CELLS; TUMOR NECROSIS FACTORS;

EID: 80054865852     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/j.1600-065X.2011.01054.x     Document Type: Review

References (92)

1. Chicheportiche Y, et al. TWEAK, a new secreted ligand in the tumor necrosis factor family that weakly induces apoptosis. J Biol Chem 1997;272:32401-32410.
2. Wiley SR, et al. A novel TNF receptor family member binds TWEAK and is implicated in angiogenesis. Immunity 2001;15:837-846.
3. Bover LC, et al. A previously unrecognized protein-protein interaction between TWEAK and CD163: potential biological implications. J Immunol 2007;178:8183-8194.
4. Burkly LC, Michaelson JS, Hahm K, Jakubowski A, Zheng TS. TWEAKing tissue remodeling by a multifunctional cytokine: role of TWEAK/Fn14 pathway in health and disease. Cytokine 2007;40:1-16.
5. Zheng TS, Burkly LC. No end in site: TWEAK/Fn14 activation and autoimmunity associated- end-organ pathologies. J Leukoc Biol 2008;84:338-347.
6. Maecker H, et al. TWEAK attenuates the transition from innate to adaptive immunity. Cell 2005;123:931-944.
7. Desplat-Jego S, et al. TWEAK is expressed by glial cells, induces astrocyte proliferation and increases EAE severity. J Neuroimmunol 2002;133:116-123.
8. Donohue PJ, et al. TWEAK is an endothelial cell growth and chemotactic factor that also potentiates FGF-2 and VEGF-A mitogenic activity. Arterioscler Thromb Vasc Biol 2003;23:594-600.
9. Desplat-Jego S, et al. TWEAK is expressed at the cell surface of monocytes during multiple sclerosis. J Leukoc Biol 2009;85:132-135.
10. Burkly LC, Dohi T. The TWEAK/Fn14 pathway in tissue remodeling: for better or for worse. Adv Exp Med Biol 2011;691:305-322.
11. Girgenrath M, et al. TWEAK, via its receptor Fn14, is a novel regulator of mesenchymal progenitor cells and skeletal muscle regeneration. EMBO J 2006;25:5826-5839.
12. Park MC, Chung SJ, Park YB, Lee SK. Relationship of serum TWEAK level to cytokine level, disease activity, and response to anti-TNF treatment in patients with rheumatoid arthritis. Scand J Rheumatol 2008;37:173-178.
13. van Kuijk AW, Wijbrandts CA, Vinkenoog M, Zheng TS, Reedquist KA, Tak PP. TWEAK and its receptor Fn14 in the synovium of patients with rheumatoid arthritis compared to psoriatic arthritis and its response to TNF blockade. Ann Rheum Dis 2010;69:301-304.
14. Serafini B, Magliozzi R, Rosicarelli B, Reynolds R, Zheng TS, Aloisi F. Expression of TWEAK and its receptor Fn14 in the multiple sclerosis brain: implications for inflammatory tissue injury. J Neuropathol Exp Neurol 2008;67:1137-1148.
15. Lu J, et al. Gene expression of TWEAK/Fn14 and IP-10/CXCR3 in glomerulus and tubulointerstitium of patients with lupus nephritis. Nephrology (Carlton) 2011;16:426-432.
16. Schwartz N, et al. Urinary TWEAK as a biomarker of lupus nephritis: a multicenter cohort study. Arthritis Res Ther 2009;11:R143.
17. Zimmermann M, et al. TNF-like weak inducer of apoptosis (TWEAK) and TNF-alpha cooperate in the induction of keratinocyte apoptosis. J Allergy Clin Immunol 2011;127:200-207, e210.
18. Nakayama M, Kayagaki N, Yamaguchi N, Okumura K, Yagita H. Involvement of TWEAK in interferon gamma-stimulated monocyte cytotoxicity. J Exp Med 2000;192:1373-1380.
19. Anderson P. Post-transcriptional control of cytokine production. Nat Immunol 2008;9:353-359.
20. Chicheportiche Y, Fossati-Jimack L, Moll S, Ibnou-Zekri N, Izui S. Down-regulated expression of TWEAK mRNA in acute and chronic inflammatory pathologies. Biochem Biophys Res Commun 2000;279:162-165.
21. Meighan-Mantha RL, et al. The mitogen-inducible Fn14 gene encodes a type I transmembrane protein that modulates fibroblast adhesion and migration. J Biol Chem 1999;274:33166-33176.
22. Winkles JA. The TWEAK-Fn14 cytokine-receptor axis: discovery, biology and therapeutic targeting. Nat Rev Drug Discov 2008;7:411-425.
23. Kim SH, et al. TWEAK can induce pro-inflammatory cytokines and matrix metalloproteinase-9 in macrophages. Circ J 2004;68:396-399.
24. Schapira K, et al. Fn14-Fc fusion protein regulates atherosclerosis in ApoE-/- mice and inhibits macrophage lipid uptake in vitro. Arterioscler Thromb Vasc Biol 2009;29:2021-2027.
25. Jakubowski A, et al. TWEAK induces liver progenitor cell proliferation. J Clin Invest 2005;115:2330-2340.
26. Michaelson JS, Burkly LC. therapeutic targeting of TWEAK/Fn14 in cancer: exploiting the intrinsic tumor cell killing capacity of the pathway. Results Probl Cell Differ 2009; 49:145-160.
27. Dohi T, et al. TWEAK/Fn14 pathway: a nonredundant role in intestinal damage in mice through a TWEAK/intestinal epithelial cell axis. Gastroenterology 2009;136:912-923.
28. Brown SA, Richards CM, Hanscom HN, Feng SL, Winkles JA. The Fn14 cytoplasmic tail binds tumour-necrosis-factor-receptor-associated factors 1, 2, 3 and 5 and mediates nuclear factor-kappaB activation. Biochem J 2003;371:395-403.
29. Saitoh T, Nakayama M, Nakano H, Yagita H, Yamamoto N, Yamaoka S. TWEAK induces NF-kappaB2 p100 processing and long lasting NF-kappaB activation. J Biol Chem 2003;278:36005-36012.
30. Brown SA, Ghosh A, Winkles JA. Full-length, membrane-anchored TWEAK can function as a juxtacrine signaling molecule and activate the NF-kappaB pathway. J Biol Chem 2010;285:17432-17441.
31. Roos C, et al. Soluble and transmembrane TNF-like weak inducer of apoptosis differentially activate the classical and noncanonical NF-kappa B pathway. J Immunol 2010;185:1593-1605.
32. Bakkar N, et al. IKK/NF-kappaB regulates skeletal myogenesis via a signaling switch to inhibit differentiation and promote mitochondrial biogenesis. J Cell Biol 2008;180:787-802.
33. Campbell S, et al. Proinflammatory effects of TWEAK/Fn14 interactions in glomerular mesangial cells. J Immunol 2006;176:1889-1898.
34. Gao HX, et al. TNF-like weak inducer of apoptosis (TWEAK) induces inflammatory and proliferative effects in human kidney cells. Cytokine 2009;46:24-35.
35. Hosokawa Y, Hosokawa I, Ozaki K, Nakae H, Matsuo T. Proinflammatory effects of tumour necrosis factor-like weak inducer of apoptosis (TWEAK) on human gingival fibroblasts. Clin Exp Immunol 2006;146:540-549.
36. Sanz AB, et al. The cytokine TWEAK modulates renal tubulointerstitial inflammation. J Am Soc Nephrol 2008;19:695-703.
37. Sanz AB, et al. TWEAK activates the non-canonical NFkappaB pathway in murine renal tubular cells: modulation of CCL21. PLoS ONE 2010;5:e8955.
38. Scholzke MN, Rottinger A, Murikinati S, Gehrig N, Leib C, Schwaninger M. TWEAK regulates proliferation and differentiation of adult neural progenitor cells. Mol Cell Neurosci 2011;46:325-332.
39. Dogra C, Changotra H, Wedhas N, Qin X, Wergedal JE, Kumar A. TNF-related weak inducer of apoptosis (TWEAK) is a potent skeletal muscle-wasting cytokine. FASEB J 2007;21:1857-1869.
40. Li H, Mittal A, Makonchuk DY, Bhatnagar S, Kumar A. Matrix metalloproteinase-9 inhibition ameliorates pathogenesis and improves skeletal muscle regeneration in muscular dystrophy. Hum Mol Genet 2009;18:2584-2598.
41. Dai L, Gu L, Ding C, Qiu L, Di W. TWEAK promotes ovarian cancer cell metastasis via NF-kappaB pathway activation and VEGF expression. Cancer Lett 2009;283:159-167.
42. Willis AL, et al. The fibroblast growth factor-inducible 14 receptor is highly expressed in HER2-positive breast tumors and regulates breast cancer cell invasive capacity. Mol Cancer Res 2008;6:725-734.
43. Tran NL, McDonough WS, Savitch BA, Sawyer TF, Winkles JA, Berens ME. The tumor necrosis factor-like weak inducer of apoptosis (TWEAK)-fibroblast growth factor-inducible 14 (Fn14) signaling system regulates glioma cell survival via NFkappaB pathway activation and BCL-XL/BCL-W expression. J Biol Chem 2005;280:3483-3492.
44. Potrovita I, et al. Tumor necrosis factor-like weak inducer of apoptosis-induced neurodegeneration. J Neurosci 2004;24:8237-8244.
45. Dogra C, Hall SL, Wedhas N, Linkhart TA, Kumar A. Fibroblast growth factor inducible 14 (Fn14) is required for the expression of myogenic regulatory factors and differentiation of myoblasts into myotubes. Evidence for TWEAK-independent functions of Fn14 during myogenesis. J Biol Chem 2007;282:15000-15010.
46. Justo P, et al. Cytokine cooperation in renal tubular cell injury: the role of TWEAK. Kidney Int 2006;70:1750-1758.
47. Polavarapu R, Gongora MC, Winkles JA, Yepes M. Tumor necrosis factor-like weak inducer of apoptosis increases the permeability of the neurovascular unit through nuclear factor-kappa B pathway activation. J Neurosci 2005;25:10094-10100.
48. Kumar M, Makonchuk DY, Li H, Mittal A, Kumar A. TNF-like weak inducer of apoptosis (TWEAK) activates proinflammatory signaling pathways and gene expression through the activation of TGF-beta-activated kinase 1. J Immunol 2009;182:2439-2448.
49. Li H, et al. Tumor necrosis factor-related weak inducer of apoptosis augments matrix metalloproteinase 9 (MMP-9) production in skeletal muscle through the activation of nuclear factor-kappaB-inducing kinase and p38 mitogen-activated protein kinase: a potential role of MMP-9 in myopathy. J Biol Chem 2009;284:4439-4450.
50. Novoyatleva T, et al. TWEAK is a positive regulator of cardiomyocyte proliferation. Cardiovasc Res 2010;85:681-690.
51. Vincent C, et al. Pro-inflammatory cytokines TNF-related weak inducer of apoptosis (TWEAK) and TNFalpha induce the mitogen-activated protein kinase (MAPK)-dependent expression of sclerostin in human osteoblasts. J Bone Miner Res 2009;24:1434-1449.
52. Saas P, et al. TWEAK stimulation of astrocytes and the proinflammatory consequences. Glia 2000;32:102-107.
53. Sanz AB, et al. Tweak induces proliferation in renal tubular epithelium: a role in uninephrectomy-induced renal hyperplasia. J Cell Mol Med 2009;13:3229-3342.
54. Ando T, et al. TWEAK/Fn14 interaction regulates RANTES production, BMP-2-induced differentiation, and RANKL expression in mouse osteoblastic MC3T3-E1 cells. Arthritis Res Ther 2006;8:R146.
55. Haile WB, et al. Tumor necrosis factor-like weak inducer of apoptosis and fibroblast growth factor-inducible 14 mediate cerebral ischemia-induced poly (ADP-ribose) polymerase-1 activation and neuronal death. Neuroscience 2010;171:1256-1264.
56. Nakayama M, et al. Multiple pathways of TWEAK-induced cell death. J Immunol 2002;168:734-743.
57. Nakayama M, et al. Fibroblast growth factor-inducible 14 mediates multiple pathways of TWEAK-induced cell death. J Immunol 2003;170:341-348.
58. Wang D, Fung JN, Tuo Y, Hu L, Chen C. TWEAK/Fn14 promotes apoptosis of human endometrial cancer cells via caspase pathway. Cancer Lett 2010;294:91-100.
59. Michaelson JS, et al. Development of an Fn14 agonistic antibody as an anti-tumor agent. MAbs 2011;3:362-375.
60. Bhatnagar S, Mittal A, Gupta SK, Kumar A. TWEAK causes myotube atrophy through coordinated activation of ubiquitin-proteasome system, autophagy, and caspases. J Cell Physiol 2011;doi:.
61. Vince CE, et al. TWEAK-FN14 signaling induces lysosomal degradation of a cIAP1-TRAF2 complex to sensitize tumor cells to TNFα. J Cell Biol 2008;182:171-184.
62. Wicovsky A, et al. TNF-like weak inducer of apoptosis inhibits proinflammatory TNF receptor-1 signaling. Cell Death Differ 2009;16:1445-1459.
63. Schneider P, et al. TWEAK can induce cell death via endogenous TNF and TNF receptor 1. Eur J Immunol 1999;29:1785-1792.
64. Vince JE, et al. TWEAK-FN14 signaling induces lysosomal degradation of a cIAP1-TRAF2 complex to sensitize tumor cells to TNFalpha. J Cell Biol 2008;182:171-184.
65. Hartupee J, Liu C, Novotny M, Li X, Hamilton T. IL-17 enhances chemokine gene expression through mRNA stabilization. J Immunol 2007;179:4135-4141.
66. Han ES, Mekasha S, Ingalls RR. Fibroblast growth factor-inducible 14 (Fn14) is expressed in the lower genital tract and may play a role in amplifying inflammation during infection. J Reprod Immunol 2010;84:16-23.
67. Munoz-Garcia B, et al. Tumor necrosis factor-like weak inducer of apoptosis (TWEAK) enhances vascular and renal damage induced by hyperlipidemic diet in ApoE-knockout mice. Arterioscler Thromb Vasc Biol 2009;29:2061-2068.
68. Jin L, et al. Induction of RANTES by TWEAK/Fn14 interaction in human keratinocytes. J Invest Dermatol 2004;122:1175-1179.
69. Tirnitz-Parker JE, et al. Tumor necrosis factor-like weak inducer of apoptosis is a mitogen for liver progenitor cells. Hepatology 2010;52:291-302.
70. Hotta K, et al. Direct targeting of fibroblast growth factor-inducible 14 protein protects against renal ischemia reperfusion injury. Kidney Int 2011;79:179-188.
71. Jain RK. Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science 2005;307:58-62.
72. Mittal A, et al. The TWEAK-Fn14 system is a critical regulator of denervation-induced skeletal muscle atrophy in mice. J Cell Biol 2010;188:833-849.
73. Laskin DL, Sunil VR, Gardner CR, Laskin JD. Macrophages and tissue injury: agents of defense or destruction? Annu Rev Pharmacol Toxicol 2011;51:267-288.
74. Feng SL, et al. The Fn14 immediate-early response gene is induced during liver regeneration and highly expressed in both human and murine hepatocellular carcinomas. Am J Pathol 2000;156:1253-1261.
75. Meijer C, et al. Kupffer cell depletion by CI2MDP-liposomes alters hepatic cytokine expression and delays liver regeneration after partial hepatectomy. Liver 2000;20:66-77.
76. Schuppan D, Popov Y. Rationale and targets for antifibrotic therapies. Gastroenterol Clin Biol 2009;33:949-957.
77. Bodine-Fowler S. Skeletal muscle regeneration after injury: an overview. J Voice 1994;8:53-62.
78. Campion DR. The muscle satellite cell: a review. Int Rev Cytol 1984;87:225-251.
79. Merly F, Lescaudron L, Rouaud T, Crossin F, Gardahaut MF. Macrophages enhance muscle satellite cell proliferation and delay their differentiation. Muscle Nerve 1999;22:724-732.
80. Lescaudron L, et al. Blood borne macrophages are essential for the triggering of muscle regeneration following muscle transplant. Neuromuscul Disord 1999;9:72-80.
81. Zhao Z, et al. TWEAK/Fn14 interactions are instrumental in the pathogenesis of nephritis in the chronic graft-versus-host model of systemic lupus erythematosus. J Immunol 2007;179:7949-7958.
82. Molano A, Lakhani P, Aran A, Burkly LC, Michaelson JS, Putterman C. TWEAK stimulation of kidney resident cells in the pathogenesis of graft versus host induced lupus nephritis. Immunol Lett 2009;125:119-128.
83. Harada N, Nakayama M, Nakano H, Fukuchi Y, Yagita H, Okumura K. Pro-inflammatory effect of TWEAK/Fn14 interaction on human umbilical vein endothelial cells. Biochem Biophys Res Commun 2002;299:488-493.
84. Bauer JW, et al. Interferon-regulated chemokines as biomarkers of systemic lupus erythematosus disease activity: a validation study. Arthritis Rheum 2009;60:3098-3107.
85. Hill GS, et al. Predictive power of the second renal biopsy in lupus nephritis: significance of macrophages. Kidney Int 2001;59:304-316.
86. Jain M, et al. A novel role for tumor necrosis factor-like weak inducer of apoptosis (TWEAK) in the development of cardiac dysfunction and failure. Circulation 2009;119:2058-2068.
87. Dogra C, Changotra H, Mohan S, Kumar A. Tumor necrosis factor-like weak inducer of apoptosis inhibits skeletal myogenesis through sustained activation of nuclear factor-kappaB and degradation of MyoD protein. J Biol Chem 2006;281:10327-10336.
88. Mittal A, et al. The TWEAK-Fn14 system is a critical regulator of denervation-induced skeletal muscle atrophy in mice. J Cell Biol 2010;188:833-849.
89. Mittal A, Bhatnagar S, Kumar A, Paul PK, Kuang S. Genetic ablation of TWEAK augments regeneration and post-injury growth of skeletal muscle in mice. Am J Pathol 2010;177:1732-1742.
90. Furling D, Lemieux D, Taneja K, Puymirat J. Decreased levels of myotonic dystrophy protein kinase (DMPK) and delayed differentiation in human myotonic dystrophy myoblasts. Neuromuscul Disord 2001;11:728-735.
91. Jansson M, Darin N, Kyllerman M, Martinsson T, Wahlstrom J, Oldfors A. Multiple mitochondrial DNA deletions in hereditary inclusion body myopathy. Acta Neuropathol 2000;100:23-28.
92. Greenberg SA. Type 1 interferons and myositis. Arthritis Res Ther 2010;12(Suppl.):S4.