248
Views
6
CrossRef citations to date
0
Altmetric
Original Article

Bortezomib treatment prevents glomerulosclerosis associated with lupus nephritis in a murine model through suppressive effects on the immune and renin–angiotensin systems

, , , &
Pages 77-86 | Received 03 Dec 2015, Accepted 23 Mar 2016, Published online: 11 May 2016

References

  • Imran TF, Yick F, Verma S, Estiverne C, Ogbonnaya-Odor C, Thiruvarudsothy S, et al. Lupus nephritis: an update. Clin Exp Nephrol. 2016;20(1):1–13.
  • Weening JJ, D’Agati VD, Schwartz MM, Seshan SV, Alpers CE, Appel GB, et al. The classification of glomerulonephritis in systemic lupus erythematosus revisited. J Am Soc Nephrol. 2004;15(2):241–50.
  • Mondini A, Messa P, Rastaldi MP. The sclerosing glomerulus in mice and man: novel insights. Curr Opin Nephrol Hypertens. 2014;23(3):239–44.
  • Ding Y, Choi ME. Regulation of autophagy by TGF-beta: emerging role in kidney fibrosis. Semin Nephrol. 2014;34(1):62–71.
  • Frankland-Searby S, Bhaumik SR. The 26S proteasome complex: an attractive target for cancer therapy. Biochim Biophys Acta. 2012;1825(1):64–76.
  • Hainz N, Thomas S, Neubert K, Meister S, Benz K, Rauh M, et al. The proteasome inhibitor bortezomib prevents lupus nephritis in the NZB/W F1 mouse model by preservation of glomerular and tubulointerstitial architecture. Nephron Exp Nephrol. 2012;120(2):e47–58.
  • Pellom ST Jr, Dudimah DF, Thounaojam MC, Sayers TJ, Shanker A. Modulatory effects of bortezomib on host immune cell functions. Immunotherapy. 2015;7(9):1011–22.
  • Adams J. The proteasome: a suitable antineoplastic target. Nat Rev Cancer. 2004;4(5):349–60.
  • Verbrugge SE, Scheper RJ, Lems WF, de Gruijl TD, Jansen G. Proteasome inhibitors as experimental therapeutics of autoimmune diseases. Arthritis Res Ther. 2015;17:17. doi: 10.1186/s13075-015-0529-1.
  • Neubert K, Meister S, Moser K, Weisel F, Maseda D, Amann K, et al. The proteasome inhibitor bortezomib depletes plasma cells and protects mice with lupus-like disease from nephritis. Nat Med. 2008;14(7):748–55.
  • Alexander T, Sarfert R, Klotsche J, Kühl AA, Rubbert-Roth A, Lorenz HM, et al. The proteasome inhibitior bortezomib depletes plasma cells and ameliorates clinical manifestations of refractory systemic lupus erythematosus. Ann Rheum Dis. 2015;74(7):1474–8.
  • Ichikawa HT, Conley T, Muchamuel T, Jiang J, Lee S, Owen T, et al. Beneficial effect of novel proteasome inhibitors in murine lupus via dual inhibition of type I interferon and autoantibody-secreting cells. Arthritis Rheum. 2012;64(2):493–503.
  • Khodadadi L, Cheng Q, Alexander T, Sercan-Alp O, Klotsche J, Radbruch A, et al. Bortezomib plus continuous B cell depletion results in sustained plasma cell depletion and amelioration of lupus nephritis in NZB/W F1 mice. PLoS One. 2015;10(8):e0135081. doi: 10.1371/journal.pone.0135081.
  • Kawano S, Lin Q, Amano H, Kaneko T, Nishikawa K, Tsurui H, et al. Phenotype conversion from rheumatoid arthritis to systemic lupus erythematosus by introduction of Yaa mutation into FcγRIIB-deficient C57BL/6 mice. Eur J Immunol. 2013;43(3):770–8.
  • Nozawa K, Fujishiro M, Kawasaki M, Yamaguchi A, Ikeda K, Morimoto S, et al. Inhibition of connective tissue growth factor ameliorates disease in a murine model of rheumatoid arthritis. Arthritis Rheum. 2013;65(6):1477–86.
  • Shiohira S, Yoshida T, Sugiura H, Nishida M, Nitta K, Tsuchiya K. Sphingosine-1-phosphate acts as a key molecule in the direct mediation of renal fibrosis. Physiol Rep 2013;1(7):e00172. doi: 10.1002/phy2.172.
  • Worthmann K, Gueler F, von Vietinghoff S, Davalos-Misslitz A, Wiehler F, Davidson A, et al. Pathogenetic role of glomerular CXCL13 expression in lupus nephritis. Clin Exp Immunol. 2014;178(1):20–7.
  • Yung S, Ng CY, Ho SK, Cheung KF, Chan KW, Zhang Q, et al. Anti-dsDNA antibody induces soluble fibronectin secretion by proximal renal tubular epithelial cells and downstream increase of TGF-β1 and collagen synthesis. J Autoimmun. 2015;58:111–22.
  • Cassese G, Lindenau S, de Boer B, Arce S, Hauser A, Riemekasten G, et al. Inflamed kidneys of NZB/W mice are a major site for the homeostasis of plasma cells. Eur J Immunol. 2001;31(9):2726–32.
  • Wang W, Rangel-Moreno J, Owen T, Barnard J, Nevarez S, Ichikawa HT, et al. Long-term B cell depletion in murine lupus eliminates autoantibody-secreting cells and is associated with alterations in the kidney plasma cell niche. J Immunol. 2014;192(7):3011–20.
  • Lee HT, Shiao YM, Wu TH, Chen WS, Hsu YH, Tsai SF, et al. Serum BLC/CXCL13 concentrations and renal expression of CXCL13/CXCR5 in patients with systemic lupus erythematosus and lupus nephritis. J Rheumatol. 2010;37(1):45–52.
  • Yap DY, Lai KN. Pathogenesis of renal disease in systemic lupus erythematosus – the role of autoantibodies and lymphocytes subset abnormalities. Int J Mol Sci. 2015;16(4):7917–31.
  • Berges C, Haberstock H, Fuchs D, Miltz M, Sadeghi M, Opelz G, et al. Proteasome inhibition suppresses essential immune functions of human CD4+ T cells. Immunology. 2008;124(2):234–46.
  • Jacob CO, van der Meide PH, McDevitt HO. In vivo treatment of (NZB X NZW) F1 lupus-like nephritis with monoclonal antibody to gamma interferon. J Exp Med. 1987;166(3):798–803.
  • Nakajima A, Hirose S, Yagita H, Okumura K. Roles of IL-4 and IL-12 in the development of lupus in NZB/W F1 mice. J Immunol. 1997;158(3):1466–72.
  • Shimizu S, Sugiyama N, Masutani K, Sadanaga A, Miyazaki Y, Inoue Y, et al. Membranous glomerulonephritis development with Th2-type immune deviations in MRL/lpr mice deficient for IL-27 receptor (WSX-1). J Immunol. 2005;175(11):7185–92.
  • Enghard P, Langnickel D, Riemekasten G. T cell cytokine imbalance towards production of IFN-gamma and IL-10 in NZB/W F1 lupus-prone mice is associated with autoantibody levels and nephritis. Scand J Rheumatol. 2006;35(3):209–16.
  • Moran E, Carbone F, Augusti V, Patrone F, Ballestrero A, Nencioni A. Proteasome inhibitors as immunosuppressants: biological rationale and clinical experience. Semin Hematol. 2012;49(3):270–6.
  • Grabias BM, Konstantopoulos K. The physical basis of renal fibrosis: effects of altered hydrodynamic forces on kidney homeostasis. Am J Physiol Renal Physiol. 2014;306(5):F473–85.
  • Sharma K, Ziyadeh FN, Alzahabi B, McGowan TA, Kapoor S, Kurnik BR, et al. Increased renal production of transforming growth factor-beta1 in patients with type II diabetes. Diabetes. 1997;46(5):854–9.
  • Fragiadaki M, Ikeda T, Witherden A, Mason RM, Abraham D, Bou-Gharios G. High doses of TGF-β potently suppress type I collagen via the transcription factor CUX1. Mol Biol Cell. 2011;22(11):1836–44.
  • Yang CW, Yu CC, Ko YC, Huang CC. Aminoguanidine reduces glomerular inducible nitric oxide synthase (iNOS) and transforming growth factor-beta 1 (TGF-beta1) mRNA expression and diminishes glomerulosclerosis in NZB/W F1 mice. Clin Exp Immunol. 1998;113(2):258–64.
  • Urushihara M, Kinoshita Y, Kondo S, Kagami S. Involvement of the intrarenal renin–angiotensin system in experimental models of glomerulonephritis. J Biomed Biotechnol. 2012;2012:601786. doi: 10.1155/2012/601786.
  • Kinoshita Y, Kondo S, Urushihara M, Suga K, Matsuura S, Takamatsu M, et al. Angiotensin II type I receptor blockade suppresses glomerular renin–angiotensin system activation, oxidative stress, and progressive glomerular injury in rat anti-glomerular basement membrane glomerulonephritis. Transl Res. 2011;158(4):235–48.
  • Taddeo A, Khodadadi L, Voigt C, Mumtaz IM, Cheng Q, Moser K, et al. Long-lived plasma cells are early and constantly generated in New Zealand Black/New Zealand White F1 mice and their therapeutic depletion requires a combined targeting of autoreactive plasma cells and their precursors. Arthritis Res Ther. 2015;17:39. doi: 10.1186/s13075-015-0551-3.
  • Schwartz N, Goilav B, Putterman C. The pathogenesis, diagnosis and treatment of lupus nephritis. Curr Opin Rheumatol. 2014;26(5):502–9.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.