TWEAK/Fn14 and non-canonical NF-kappaB signaling in kidney disease

Frontiers in Immunology

Volumn 4, Issue DEC, 2013, Pages

  Poveda, Jonay ^a   Tabara, Luis C ^a   Fernandez Fernandez, Beatriz ^a   Martin Cleary, Catalina ^a   Sanz, Ana B ^a   Selgas, Rafael ^b   Ortiz, Alberto ^a   Sanchez Niño, Maria D ^b  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b HOSPITAL UNIVERSITARIO LA PAZ IDIPAZ   (Spain)

Author keywords

Acute kidney injury; Fibrosis; Inflammation; Kidney; Lupus nephritis; Podocyte; Proteinuria

Indexed keywords

EID: 84892160220     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2013.00447     Document Type: Short Survey

References (77)

1. Kidney Disease: Improving Global Outcomes (KDIGO) Acute Kidney Injury Work Group. KDIGO clinical practice guideline for acute kidney injury. Kidney Int Suppl (2012) 2:1-138. doi: 10.1038/kisup.2012.3.
2. Kidney Disease: Improving Global Outcomes (KDIGO) CKD Work Group. KDIGO 2012 clinical practice guideline for the evaluation and management of chronic kidney disease. Kidney Int Suppl (2013) 3:1-150. doi:10.1038/kisup.2012.73.
3. Fernandez FB, Elewa U, Sanchez-Nino MD, Rojas-Rivera JE, Martin-Cleary C, Egido J, et al. 2012 update on diabetic kidney disease: the expanding spectrum, novel pathogenic insights and recent clinical trials. Minerva Med (2012) 103:219-34.
4. Sanz AB, Sanchez-Nino MD, Ortiz A. TWEAK, a multifunctional cytokine in kidney injury. Kidney Int (2011) 80:708-18. doi:10.1038/ki.2011.180.
5. Sanz AB, Sanchez-Nino MD, Martin-Cleary C, Ortiz A, Ramos AM. Progress in the development of animal models of acute kidney injury and its impact on drug discovery. Expert Opin Drug Discov (2013) 8:879-95. doi:10.1517/17460441.2013.793667.
6. Chicheportiche Y, Bourdon PR, Xu H, Hsu YM, Scott H, Hession C, et al. TWEAK, a new secreted ligand in the tumor necrosis factor family that weakly induces apoptosis. J Biol Chem (1997) 272:32401-10. doi:10.1074/jbc.272.51.32401.
7. He F, Dang W, Saito K, Watanabe S, Kobayashi N, Guntert P, et al. Solution structure of the cysteine-rich domain in Fn14, a member of the tumor necrosis factor receptor superfamily. Protein Sci (2009) 18:650-6. doi:10.1002/pro.49.
8. 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. doi:10.1042/BJ20021730.
9. Sanz AB, Sanchez-Nino MD, Izquierdo MC, Jakubowski A, Justo P, Blanco-Colio LM, et al. Tweak induces proliferation in renal tubular epithelium: a role in uninephrectomy induced renal hyperplasia. J Cell Mol Med (2009) 13:3329-42. doi:10.1111/j.1582-4934.2009.00766.x.
10. Justo P, Sanz AB, Sanchez-Nino MD, Winkles JA, Lorz C, Egido J, et al. Cytokine cooperation in renal tubular cell injury: the role of TWEAK. Kidney Int (2006) 70:1750-8. doi:10.1038/sj.ki.5001866.
11. Ortiz A, Lorz C, Catalan MP, Danoff TM, Yamasaki Y, Egido J, et al. Expression of apoptosis regulatory proteins in tubular epithelium stressed in culture or following acute renal failure. Kidney Int (2000) 57:969-81. doi:10.1046/j.1523-1755.2000.00925.x.
12. Nakayama M, Ishidoh K, Kojima Y, Harada N, Kominami E, Okumura K, et al. Fibroblast growth factor-inducible 14 mediates multiple pathways of TWEAK-induced cell death. J Immunol (2003) 170:341-8.
13. Vince JE, Chau D, Callus B, Wong WW, Hawkins CJ, Schneider P, et al. TWEAK-FN14 signaling induces lysosomal degradation of a cIAP1-TRAF2 complex to sensitize tumor cells to TNFalpha. J Cell Biol (2008) 182:171-84. doi:10.1083/jcb.200801010.
14. Martin CC, Moreno JA, Fernandez B, Ortiz A, Parra EG, Gracia C, et al. Glomerular haematuria, renal interstitial haemorrhage and acute kidney injury. Nephrol Dial Transplant (2010) 25:4103-6. doi:10.1093/ndt/gfq493.
15. Kaplan MJ, Lewis EE, Shelden EA, Somers E, Pavlic R, McCune WJ, et al. The apoptotic ligands TRAIL, TWEAK, and Fas ligand mediate monocyte death induced by autologous lupus T cells. J Immunol (2002) 169:6020-9.
16. Nakayama M, Kayagaki N, Yamaguchi N, Okumura K, Yagita H. Involvement of TWEAK in interferon gamma-stimulated monocyte cytotoxicity. J Exp Med (2000) 192:1373-80. doi:10.1084/jem.192.9.1373.
17. Campbell S, Burkly LC, Gao HX, Berman JW, Su L, Browning B, et al. Proinflammatory effects of TWEAK/Fn14 interactions in glomerular mesangial cells. J Immunol (2006) 176:1889-98.
18. Gao HX, Campbell SR, Burkly LC, Jakubowski A, Jarchum I, Banas B, et al. TNF-like weak inducer of apoptosis (TWEAK) induces inflammatory and proliferative effects in human kidney cells. Cytokine (2009) 46:24-35. doi:10.1016/j.cyto.2008.12.001.
19. Sanchez-Nino MD, Poveda J, Sanz AB, Mezzano S, Carrasco S, Fernandez-Fernandez B, et al. Fn14 in podocytes and proteinuric kidney disease. Biochim Biophys Acta (2013) 1832:2232-43. doi:10.1016/j.bbadis.2013.08.010.
20. Sanz AB, Justo P, Sanchez-Nino MD, Blanco-Colio LM, Winkles JA, Kreztler M, et al. The cytokine TWEAK modulates renal tubulointerstitial inflammation. J Am Soc Nephrol (2008) 19:695-703. doi:10.1681/ASN.2007050577.
21. Linkermann A, Brasen JH, Darding M, Jin MK, Sanz AB, Heller JO, et al. Two independent pathways of regulated necrosis mediate ischemia-reperfusion injury. Proc Natl Acad Sci U S A (2013) 110:12024-9. doi:10.1073/pnas.1305538110.
22. Ucero AC, Benito-Martin A, Fuentes-Calvo I, Santamaria B, Blanco J, Lopez-Novoa JM, et al. TNF-related weak inducer of apoptosis (TWEAK) promotes kidney fibrosis and Ras-dependent proliferation of cultured renal fibroblast. Biochim Biophys Acta (2013) 1832:1744-55. doi:10.1016/j.bbadis.2013.05.032.
23. Sanz AB, Sanchez-Nino MD, Izquierdo MC, Jakubowski A, Justo P, Blanco-Colio LM, et al. TWEAK activates the non-canonical NFkappaB pathway in murine renal tubular cells: modulation of CCL21. PLoS One (2010) 5:e8955. doi:10.1371/journal.pone.0008955.
24. Hotta K, Sho M, Yamato I, Shimada K, Harada H, Akahori T, et al. Direct targeting of fibroblast growth factor-inducible 14 protein protects against renal ischemia reperfusion injury. Kidney Int (2011) 79:179-88. doi:10.1038/ki.2010.379.
25. Xia Y, Campbell SR, Broder A, Herlitz L, Abadi M, Wu P, et al. Inhibition of the TWEAK/Fn14 pathway attenuates renal disease in nephrotoxic serum nephritis. Clin Immunol (2012) 145:108-21. doi:10.1016/j.clim.2012.08.008.
26. Izquierdo MC, Sanz AB, Mezzano S, Blanco J, Carrasco S, Sanchez-Nino MD, et al. TWEAK (tumor necrosis factor-like weak inducer of apoptosis) activates CXCL16 expression during renal tubulointerstitial inflammation. Kidney Int (2012) 81:1098-107. doi:10.1038/ki.2011.475.
27. Lu J, Szeto CC, Tam LS, Lai FM, Li EK, Chow KM, et al. Relationship of intrarenal gene expression and the histological class of lupus nephritis-a study on repeat renal biopsy. J Rheumatol (2012) 39:1942-7. doi:10.3899/jrheum.120177.
28. Lu J, Kwan BC, Lai FM, Choi PC, Tam LS, Li EK, et al. Gene expression of TWEAK/Fn14 and IP-10/CXCR3 in glomerulus and tubulointerstitium of patients with lupus nephritis. Nephrology (Carlton) (2011) 16:426-32. doi:10.1111/j.1440-1797.2011.01449.x.
29. Schwartz N, Su L, Burkly LC, Mackay M, Aranow C, Kollaros M, et al. Urinary TWEAK and the activity of lupus nephritis. J Autoimmun (2006) 27:242-50. doi:10.1016/j.jaut.2006.12.003.
30. Schwartz N, Rubinstein T, Burkly LC, Collins CE, Blanco I, Su L, et al. Urinary TWEAK as a biomarker of lupus nephritis: a multicenter cohort study. Arthritis Res Ther (2009) 11:R143. doi:10.1186/ar2816.
31. Xuejing Z, Jiazhen T, Jun L, Xiangqing X, Shuguang Y, Fuyou L. Urinary TWEAK level as a marker of lupus nephritis activity in 46 cases. J Biomed Biotechnol (2012) 2012:359647. doi:10.1155/2012/359647.
32. El-Shehaby A, Darweesh H, El-Khatib M, Momtaz M, Marzouk S, El-Shaarawy N, et al. Correlations of urinary biomarkers, TNF-like weak inducer of apoptosis (TWEAK), osteoprotegerin (OPG), monocyte chemoattractant protein-1 (MCP-1), and IL-8 with lupus nephritis. J Clin Immunol (2011) 31:848-56. doi:10.1007/s10875-011-9555-1.
33. Moreno JA, Izquierdo MC, Sanchez-Nino MD, Suarez-Alvarez B, Lopez-Larrea C, Jakubowski A, et al. The inflammatory cytokines TWEAK and TNFalpha reduce renal klotho expression through NFkappaB. J Am Soc Nephrol (2011) 22:1315-25. doi:10.1681/ASN.2010101073.
34. Zhao Z, Burkly LC, Campbell S, Schwartz N, Molano A, Choudhury A, 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) 179:7949-58.
35. Munoz-Garcia B, Moreno JA, Lopez-Franco O, Sanz AB, Martin-Ventura JL, Blanco J, 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) 29:2061-8. doi:10.1161/ATVBAHA.109.194852.
36. Jakubowski A, Ambrose C, Parr M, Lincecum JM, Wang MZ, Zheng TS, et al. TWEAK induces liver progenitor cell proliferation. J Clin Invest (2005) 115:2330-40. doi:10.1172/JCI23486.
37. Girgenrath M, Weng S, Kostek CA, Browning B, Wang M, Brown SA, et al. TWEAK, via its receptor Fn14, is a novel regulator of mesenchymal progenitor cells and skeletal muscle regeneration. EMBO J (2006) 25:5826-39. doi:10.1038/sj.emboj.7601441.
38. Sanz AB, Sanchez-Nino MD, Ramos AM, Moreno JA, Santamaria B, Ruiz-Ortega M, et al. NF-kappaB in renal inflammation. J Am Soc Nephrol (2010) 21:1254-62. doi:10.1681/ASN.2010020218.
39. Moynagh PN. The NF-kappaB pathway. J Cell Sci (2005) 118:4589-92. doi:10.1242/jcs.02579.
40. Hoffmann A, Natoli G, Ghosh G. Transcriptional regulation via the NF-kappaB signaling module. Oncogene (2006) 25:6706-16. doi:10.1038/sj.onc.1209933.
41. Hayden MS, Ghosh S. Shared principles in NF-kappaB signaling. Cell (2008) 132:344-62. doi:10.1016/j.cell.2008.01.020.
42. Perkins ND. Integrating cell-signalling pathways with NF-kappaB and IKK function. Nat Rev Mol Cell Biol (2007) 8:49-62. doi:10.1038/nrm2083.
43. Hayden MS, Ghosh S. Signaling to NF-kappaB. Genes Dev (2004) 18:2195-224. doi:10.1101/gad.1228704.
44. Karin M, Ben-Neriah Y. Phosphorylation meets ubiquitination: the control of NF-[kappa]B activity. Annu Rev Immunol (2000) 18:621-63. doi:10.1146/annurev.immunol.18.1.621.
45. Senftleben U, Cao Y, Xiao G, Greten FR, Krahn G, Bonizzi G, et al. Activation by IKKalpha of a second, evolutionary conserved, NF-kappa B signaling pathway. Science (2001) 293:1495-9. doi:10.1126/science.1062677.
46. Karin M. How NF-kappaB is activated: the role of the IkappaB kinase (IKK) complex. Oncogene (1999) 18:6867-74. doi:10.1038/sj.onc.1203219.
47. Tergaonkar V. NFkappaB pathway: a good signaling paradigm and therapeutic target. Int J Biochem Cell Biol (2006) 38:1647-53. doi:10.1016/j.biocel.2006.03.023.
48. Gilmore TD. Introduction to NF-kappaB: players, pathways, perspectives. Oncogene (2006) 25:6680-4. doi:10.1038/sj.onc.1209954.
49. Scheidereit C. IkappaB kinase complexes: gateways to NF-kappaB activation and transcription. Oncogene (2006) 25:6685-705. doi:10.1038/sj.onc.1209934.
50. Xiao G, Harhaj EW, Sun SC. NF-kappaB-inducing kinase regulates the processing of NF-kappaB2 p100. Mol Cell (2001) 7:401-9. doi:10.1016/S1097-2765(01)00187-3.
51. Xiao G, Fong A, Sun SC. Induction of p100 processing by NF-kappaB-inducing kinase involves docking IkappaB kinase alpha (IKKalpha) to p100 and IKKalpha-mediated phosphorylation. J Biol Chem (2004) 279:30099-105. doi:10.1074/jbc.M401428200.
52. Dejardin E. The alternative NF-kappaB pathway from biochemistry to biology: pitfalls and promises for future drug development. Biochem Pharmacol (2006) 72:1161-79. doi:10.1016/j.bcp.2006.08.007.
53. Dejardin E, Droin NM, Delhase M, Haas E, Cao Y, Makris C, et al. The lymphotoxin-beta receptor induces different patterns of gene expression via two NF-kappaB pathways. Immunity (2002) 17:525-35. doi:10.1016/S1074-7613(02)00423-5.
54. Coope HJ, Atkinson PG, Huhse B, Belich M, Janzen J, Holman MJ, et al. CD40 regulates the processing of NF-kappaB2 p100 to p52. EMBO J (2002) 21:5375-85. doi:10.1093/emboj/cdf542.
55. Claudio E, Brown K, Park S, Wang H, Siebenlist U. BAFF-induced NEMO-independent processing of NF-kappa B2 in maturing B cells. Nat Immunol (2002) 3:958-65. doi:10.1038/ni842.
56. Kayagaki N, Yan M, Seshasayee D, Wang H, Lee W, French DM, et al. BAFF/BLyS receptor 3 binds the B cell survival factor BAFF ligand through a discrete surface loop and promotes processing of NF-kappaB2. Immunity (2002) 17:515-24. doi:10.1016/S1074-7613(02)00425-9.
57. Novack DV, Yin L, Hagen-Stapleton A, Schreiber RD, Goeddel DV, Ross FP, et al. The IkappaB function of NF-kappaB2 p100 controls stimulated osteoclastogenesis. J Exp Med (2003) 198:771-81. doi:10.1084/jem.20030116.
58. 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) 278:36005-12. doi:10.1074/jbc.M304266200.
59. Rowe AM, Murray SE, Raue HP, Koguchi Y, Slifka MK, Parker DC. A cell-intrinsic requirement for NF-kappaB-inducing kinase in CD4 and CD8 T cell memory. J Immunol (2013) 191:3663-72. doi:10.4049/jimmunol.1301328.
60. Hofmann J, Mair F, Greter M, Schmidt-Supprian M, Becher B. NIK signaling in dendritic cells but not in T cells is required for the development of effector T cells and cell-mediated immune responses. J Exp Med (2011) 208:1917-29. doi:10.1084/jem.20110128.
61. Sheng L, Zhou Y, Chen Z, Ren D, Cho KW, Jiang L, et al. NF-kappaB-inducing kinase (NIK) promotes hyperglycemia and glucose intolerance in obesity by augmenting glucagon action. Nat Med (2012) 18:943-9. doi:10.1038/nm.2756.
62. Choudhary S, Sinha S, Zhao Y, Banerjee S, Sathyanarayana P, Shahani S, et al. NF-kappaB-inducing kinase (NIK) mediates skeletal muscle insulin resistance: blockade by adiponectin. Endocrinology (2011) 152:3622-7. doi:10.1210/en.2011-1343.
63. Hacker H, Chi L, Rehg JE, Redecke V. NIK prevents the development of hypereosinophilic syndrome-like disease in mice independent of IKKalpha activation. J Immunol (2012) 188:4602-10. doi:10.4049/jimmunol.1200021.
64. Thu YM, Su Y, Yang J, Splittgerber R, Na S, Boyd A, et al. NF-kappaB inducing kinase (NIK) modulates melanoma tumorigenesis by regulating expression of pro-survival factors through the beta-catenin pathway. Oncogene (2012) 31:2580-92. doi:10.1038/onc.2011.427.
65. Chung S, Sundar IK, Hwang JW, Yull FE, Blackwell TS, Kinnula VL, et al. NF-kappaB inducing kinase, NIK mediates cigarette smoke/TNFalpha-induced histone acetylation and inflammation through differential activation of IKKs. PLoS One (2011) 6:e23488. doi:10.1371/journal.pone.0023488.
66. Cheung HH, St Jean M, Beug ST, Lejmi-Mrad R, LaCasse E, Baird SD, et al. SMG1 and NIK regulate apoptosis induced by Smac mimetic compounds. Cell Death Dis (2011) 2:e146. doi:10.1038/cddis.2011.25.
67. Starkey JM, Haidacher SJ, LeJeune WS, Zhang X, Tieu BC, Choudhary S, et al. Diabetes-induced activation of canonical and noncanonical nuclear factor-kappaB pathways in renal cortex. Diabetes (2006) 55:1252-9. doi:10.2337/db05-1554.
68. Zhao Y, Banerjee S, LeJeune WS, Choudhary S, Tilton RG. NF-kappaB-inducing kinase increases renal tubule epithelial inflammation associated with diabetes. Exp Diabetes Res (2011) 2011:192564. doi:10.1155/2011/192564.
69. Loverre A, Ditonno P, Crovace A, Gesualdo L, Ranieri E, Pontrelli P, et al. Ischemia-reperfusion induces glomerular and tubular activation of proinflammatory and antiapoptotic pathways: differential modulation by rapamycin. J Am Soc Nephrol (2004) 15:2675-86. doi:10.1097/01.ASN.0000139932.00971.E4.
70. Feng B, Chen G, Zheng X, Sun H, Zhang X, Zhang ZX, et al. Small interfering RNA targeting RelB protects against renal ischemia-reperfusion injury. Transplantation (2009) 87:1283-9. doi:10.1097/TP.0b013e3181a1905e.
71. Benedetti G, Fokkelman M, Yan K, Fredriksson L, Herpers B, Meerman J, et al. The nuclear factor kappaB family member RelB facilitates apoptosis of renal epithelial cells caused by cisplatin/tumor necrosis factor alpha synergy by suppressing an epithelial to mesenchymal transition-like phenotypic switch. Mol Pharmacol (2013) 84:128-38. doi:10.1124/mol.112.084053.
72. Sun CY, Hsu HH, Wu MS. p-Cresol sulfate and indoxyl sulfate induce similar cellular inflammatory gene expressions in cultured proximal renal tubular cells. Nephrol Dial Transplant (2013) 28:70-8. doi:10.1093/ndt/gfs133.
73. Poveda J, Sanchez-Niño MD, Glorieux G, Sanz AB, Egido J, Vanholder R, et al. p-Cresyl sulphate has pro-inflammatory and cytotoxic actions on human proximal tubular epithelial cells. Nephrol Dial Transplant (2013). doi:10.1093/ndt/gft367. [Epub ahead of print].
74. Hehner SP, Hofmann TG, Droge W, Schmitz ML. The antiinflammatory sesquiterpene lactone parthenolide inhibits NF-kappa B by targeting the I kappa B kinase complex. J Immunol (1999) 163:5617-23.
75. Sakai N, Wada T, Yokoyama H, Lipp M, Ueha S, Matsushima K, et al. Secondary lymphoid tissue chemokine (SLC/CCL21)/CCR7 signaling regulates fibrocytes in renal fibrosis. Proc Natl Acad Sci U S A (2006) 103:14098-103. doi:10.1073/pnas.0511200103.
76. Carragher D, Johal R, Button A, White A, Eliopoulos A, Jenkinson E, et al. A stroma-derived defect in NF-kappaB2-/-mice causes impaired lymph node development and lymphocyte recruitment. J Immunol (2004) 173:2271-9.
77. Li K, McGee LR, Fisher B, Sudom A, Liu J, Rubenstein SM, et al. Inhibiting NF-kappaB-inducing kinase (NIK): discovery, structure-based design, synthesis, structure-activity relationship, and co-crystal structures. Bioorg Med Chem Lett (2013) 23:1238-44. doi:10.1016/j.bmcl.2013.01.012.