234
Views
1
CrossRef citations to date
0
Altmetric
Original Articles

The small heat shock protein HSPB5 attenuates the severity of lupus nephritis in lupus-prone mice

, , &
Pages 192-202 | Received 29 Sep 2021, Accepted 07 Jan 2022, Published online: 09 Feb 2022

References

  • Tsokos GC. Systemic lupus erythematosus. N Engl J Med. 2011;365(22):2110–2121.
  • Tsokos GC, Lo MS, Reis PC, et al. New insights into the immunopathogenesis of systemic lupus erythematosus. Nat Rev Rheumatol. 2016;12(12):716–730.
  • Perl A. Pathogenic mechanisms in systemic lupus erythematosus. Autoimmunity. 2010;43(1):1–6.
  • McGaha TL, Madaio MP. Lupus nephritis: animal modeling of a complex disease syndrome pathology. Drug Discov Today Dis Models. 2014;11:13–18.
  • Jaryal A, Vikrant S. Current status of lupus nephritis. Indian J Med Res. 2017;145(2):167–178.
  • Maria NI, Davidson A. Renal macrophages and dendritic cells in SLE nephritis. Curr Rheumatol Rep. 2017;19(12):81.
  • Furie R, Rovin BH, Houssiau F, et al. Two-Year, randomized, controlled trial of belimumab in lupus nephritis. N Engl J Med. 2020;383(12):1117–1128.
  • Arriens C, Polyakova S, Adzerikho I, et al. Op0277 Aurora phase 3 study demonstrates voclosporin statistical superiority over standard of care in lupus nephritis (ln). Ann Rheum Dis. 2020;79(Suppl 1):172–173.
  • Chebotareva N, Bobkova I, Shilov E. Heat shock proteins and kidney disease: perspectives of HSP therapy. Cell Stress Chaperones. 2017;22(3):319–343.
  • Sreedharan R, Van Why SK. Heat shock proteins in the kidney. Pediatr Nephrol. 2016;31(10):1561–1570.
  • Wachstein J, Tischer S, Figueiredo C, et al. HSP70 enhances immunosuppressive function of CD4(+)CD25(+)FoxP3(+) T regulatory cells and cytotoxicity in CD4(+)CD25(-) T cells. PLoS One. 2012;7(12):e51747.
  • Mirza S, Muthana M, Fairburn B, et al. The stress protein gp96 is not an activator of resting rat bone marrow-derived dendritic cells, but is a costimulator and activator of CD3+ T cells. Cell Stress Chaperones. 2006;11(4):364–378.
  • van Noort JM, Bsibsi M, Nacken PJ, et al. Activation of an immune-regulatory macrophage response and inhibition of lung inflammation in a mouse model of COPD using heat-shock protein alpha B-crystallin-loaded PLGA microparticles. Biomaterials. 2013;34(3):831–840.
  • Rothbard JB, Rothbard JJ, Soares L, et al. Identification of a common immune regulatory pathway induced by small heat shock proteins, amyloid fibrils, and nicotine. Proc Natl Acad Sci U S A. 2018;115(27):7081–7086.
  • Bsibsi M, Holtman IR, Gerritsen WH, et al. Alpha-B-Crystallin induces an Immune-Regulatory and antiviral microglial response in preactive multiple sclerosis lesions. J Neuropathol Exp Neurol. 2013;72(10):970–979.
  • Holtman IR, Bsibsi M, Gerritsen WH, et al. Identification of highly connected hub genes in the protective response program of human macrophages and microglia activated by alpha B-crystallin: Hub genes in protective macrophages and microglia. Glia. 2017;65(3):460–473.
  • Finlay TM, Palmer AL, Ousman SS. Murine neutrophils treated with alphaB-crystallin reduce IL-12p40 production by dendritic cells. Immunology. 2018;155(1):72–84.
  • Arac A, Brownell SE, Rothbard JB, et al. Systemic augmentation of alphaB-crystallin provides therapeutic benefit twelve hours post-stroke onset via immune modulation. Proc Natl Acad Sci USA. 2011;108(32):13287–13292.
  • Klopstein A, Santos-Nogueira E, Francos-Quijorna I, et al. Beneficial effects of αB-crystallin in spinal cord contusion injury. J Neurosci. 2012;32(42):14478–14488.
  • Zhang Y, Chen Y, Wu J, et al. Activation of dopamine D2 receptor suppresses neuroinflammation through αB-Crystalline by inhibition of NF-κB nuclear translocation in experimental ICH mice model. Stroke. 2015;46(9):2637–2646.
  • Park H, Park H, Hwang HJ, et al. Alpha B-crystallin prevents ventricular arrhythmia by attenuating inflammation and oxidative stress in rat with autoimmune myocarditis. Int J Cardiol. 2015;182:399–402.
  • Ousman SS, Tomooka BH, van Noort JM, et al. Protective and therapeutic role for alphaB-crystallin in autoimmune demyelination. Nature. 2007;448(7152):474–479.
  • Quach QL, Metz LM, Thomas JC, Rothbard JB, et al. CRYAB modulates the activation of CD4+ T cells from relapsing-remitting multiple sclerosis patients. Mult Scler. 2013;19(14):1867–1877.
  • van Noort JM, Bsibsi M, Nacken PJ, et al. Therapeutic intervention in multiple sclerosis with alpha B-Crystallin: a randomized controlled phase IIa trial. PLoS One. 2015;10(11):e0143366.
  • Lim E-MF, Hoghooghi V, Hagen KM, et al. Presence and activation of pro-inflammatory macrophages are associated with CRYAB expression in vitro and after peripheral nerve injury. J Neuroinflammation. 2021;18(1):82.
  • Liu S, Tobias R, McClure S, et al. Removal of endotoxin from recombinant protein preparations. Clin Biochem. 1997;30(6):455–463.
  • Teodorowicz M, Perdijk O, Verhoek I, et al. Optimized triton X-114 assisted lipopolysaccharide (LPS) removal method reveals the immunomodulatory effect of food proteins. PLoS One. 2017;12(3):e0173778.
  • Alperovich G, Rama I, Lloberas N, et al. New immunosuppresor strategies in the treatment of murine lupus nephritis. Lupus. 2007;16(1):18–24.
  • Rose T, Grützkau A, Klotsche J, et al. Are interferon-related biomarkers advantageous for monitoring disease activity in systemic lupus erythematosus? A longitudinal benchmark study. Rheumatology (Oxford)). 2017;56(9):1618–1626.
  • Zan H, Zhang J, Ardeshna S, et al. Lupus-prone MRL/faslpr/lpr mice display increased AID expression and extensive DNA lesions, comprising deletions and insertions, in the immunoglobulin locus: concurrent upregulation of somatic hypermutation and class switch DNA recombination . Autoimmunity. 2009;42(2):89–103.
  • Toong C, Adelstein S, Phan TG. Clearing the complexity: immune complexes and their treatment in lupus nephritis. Int J Nephrol Renovasc Dis. 2011;4:17–28.
  • Suárez-Fueyo A, Bradley SJ, Klatzmann D, et al. T cells and autoimmune kidney disease. Nat Rev Nephrol. 2017;13(6):329–343.
  • Yung S, Chan TM. Mechanisms of kidney injury in lupus nephritis - the role of anti-dsDNA. Front Immunol. 2015;6(475):475.
  • Bethunaickan R, Berthier CC, Ramanujam M, et al. A unique hybrid renal mononuclear phagocyte activation phenotype in murine systemic lupus erythematosus nephritis. J Immunol. 2011;186(8):4994–5003.
  • Chang A, Henderson SG, Brandt D, et al. In situ B cell-mediated immune responses and tubulointerstitial inflammation in human lupus nephritis. J Immunol. 2011;186(3):1849–18491860.
  • Yu F, Wu L, Tan Y, et al. Tubulointerstitial lesions of patients with lupus nephritis classified by the 2003 international society of nephrology and renal pathology society system. Kidney Int. 2010;77(9):820–829.
  • Londoño Jimenez A, Mowrey WB, Putterman C, et al. Brief report: Tubulointerstitial damage in lupus nephritis: a comparison of the factors associated with tubulointerstitial inflammation and renal scarring. Arthritis Rheumatol. 2018;70(11):1801–1806.
  • Maria NI, Davidson A. Protecting the kidney in systemic lupus erythematosus: from diagnosis to therapy. Nat Rev Rheumatol. 2020;16(5):255–267.
  • Lan-Ting H, You-Ming C, Li-Xin W, et al. Clinicopathological factors for tubulointerstitial injury in lupus nephritis. Clin Rheumatol. 2020;39(5):1617–1626.
  • Wilson PC, Kashgarian M, Moeckel G. Interstitial inflammation and interstitial fibrosis and tubular atrophy predict renal survival in lupus nephritis. Clinical Kidney Journal. 2018;11(2):207–218.
  • Hsieh C, Chang A, Brandt D, et al. Predicting outcomes of lupus nephritis with tubulointerstitial inflammation and scarring. Arthritis Care Res (Hoboken)). 2011;63(6):865–874.
  • Rijnink EC, Teng YKO, Wilhelmus S, et al. Clinical and histopathologic characteristics associated with renal outcomes in lupus nephritis. Clin J Am Soc Nephrol. 2017;12(5):734–743.
  • Andersen MH. The balance players of the adaptive immune system. Cancer Res. 2018;78(6):1379–1382.
  • Csóka B, Selmeczy Z, Koscsó B, et al. Adenosine promotes alternative macrophage activation via A2A and A2B receptors. Faseb J. 2012;26(1):376–386.
  • Zhou S, Qi Q, Wang X, et al. SjHSP60 induces CD4+ CD25+ Foxp3+ tregs via TLR4-Mal-drived production of TGF-β in macrophages. Immunol Cell Biol. 2018;96(9):958–968.
  • Qian-Qian Q, Xiao-Fan W, Li-Na Z, et al. [Schistosoma japonicum heat shock protein 60 enhances regulatory T cell immunosuppressive function by promoting the expressions of IL-10 and TGF-β]. Zhongguo Xue Xi Chong Bing Fang Zhi Za Zhi. 2018;30(1):42–46.
  • Hsu W-T, Ho S-Y, Jian T-Y, et al. Helicobacter pylori-derived heat shock protein 60 increases the induction of regulatory T-cells associated with persistent infection. Microb Pathog. 2018;119:152–161.
  • Motta A, Schmitz C, Rodrigues L, et al. Mycobacterium tuberculosis heat-shock protein 70 impairs maturation of dendritic cells from bone marrow precursors, induces interleukin-10 production and inhibits T-cell proliferation in vitro. Immunology. 2007;121(4):462–472.
  • Detanico T, Rodrigues L, Sabritto AC, et al. Mycobacterial heat shock protein 70 induces interleukin-10 production: immunomodulation of synovial cell cytokine profile and dendritic cell maturation. Clin Exp Immunol. 2004;135(2):336–342.
  • Siddiqui KF, Amir M, Gurram RK, et al. Latency-associated protein Acr1 impairs dendritic cell maturation and functionality: a possible mechanism of immune evasion by Mycobacterium tuberculosis. J Infect Dis. 2014;209(9):1436–1445.
  • Mubin N, Pahari S, Owais M, et al. Mycobacterium tuberculosis host cell interaction: Role of latency associated protein acr-1 in differential modulation of macrophages. PLoS One. 2018;13(11):e0206459.
  • Amir M, Aqdas M, Nadeem S, et al. Diametric role of the Latency-Associated protein Acr1 of Mycobacterium tuberculosis in modulating the functionality of pre- and post-maturational stages of dendritic cells. Front Immunol. 2017;8(624):624.
  • Biesen R, Demir C, Barkhudarova F, et al. Sialic acid-binding Ig-like lectin 1 expression in inflammatory and resident monocytes is a potential biomarker for monitoring disease activity and success of therapy in systemic lupus erythematosus. Arthritis Rheum. 2008;58(4):1136–1145.
  • Geginat J, Vasco M, Gerosa M, et al. IL-10 producing regulatory and helper T-cells in systemic lupus erythematosus. Semin Immunol. 2019;44:101330.
  • Yin Z, Bahtiyar G, Zhang N, et al. IL-10 regulates murine lupus. J Immunol. 2002;169(4):2148–2155.
  • Cash H, Relle M, Menke J, et al. Interleukin 6 (IL-6) deficiency delays lupus nephritis in MRL-Faslpr mice: the IL-6 pathway as a new therapeutic target in treatment of autoimmune kidney disease in systemic lupus erythematosus. J Rheumatol. 2010;37(1):60–70.
  • Arazi A, Rao DA, Berthier CC, Accelerating Medicines Partnership in SLE network, et al. The immune cell landscape in kidneys of patients with lupus nephritis. Nat Immunol. 2019;20(7):902–914.
  • He DN, Chen WL, Long KX, et al. Association of serum CXCL13 with intrarenal ectopic lymphoid tissue formation in lupus nephritis. J Immunol Res. 2016;2016(4832543):4832543.
  • Biswas SK, Mantovani A. Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm. Nat Immunol. 2010;11(10):889–896.
  • Kurnellas MP, Brownell SE, Su L, et al. Chaperone activity of small heat shock proteins underlies therapeutic efficacy in experimental autoimmune encephalomyelitis. J Biol Chem. 2012;287(43):36423–36434.
  • Davies B, Morris T. Physiological parameters in laboratory animals and humans. Pharm Res. 1993;10(7):1093–1095.
  • Sreekumar PG, Kannan R, Kitamura M, et al. αB crystallin is apically secreted within exosomes by polarized human retinal pigment epithelium and provides neuroprotection to adjacent cells. Blagosklonny MV, editor. PLoS One. 2010;5(10):e12578
  • Kim M, Park SW, Kim M, et al. Selective renal overexpression of human heat shock protein 27 reduces renal ischemia-reperfusion injury in mice. Am J Physiol Renal Physiol. 2010;299(2):F347–58.
  • Mao Y-W, Liu J-P, Xiang H, et al. Human alphaA- and alphaB-crystallins bind to bax and Bcl-X(S) to sequester their translocation during staurosporine-induced apoptosis. Cell Death Differ. 2004 May;11(5):512–526.
  • Lou Q, Hu Y, Ma Y, et al. Heat shock factor 1 induces crystallin-αB to protect against cisplatin nephrotoxicity. Am J Physiol Renal Physiol. 2016;311(1):F94–102.
  • Rothbard JB, Kurnellas MP, Brownell S, et al. Therapeutic effects of systemic administration of chaperone αB-Crystallin associated with binding proinflammatory plasma proteins*. J Biol Chem. 2012;287(13):9708–9721.
  • Dörner T, Furie R. Novel paradigms in systemic lupus erythematosus. The Lancet. 2019;393(10188):2344–2358.
  • Stokes MB, Foster K, Markowitz GS, et al. Development of glomerulonephritis during anti-TNF-alpha therapy for rheumatoid arthritis. Nephrol Dial Transplant. 2005;20(7):1400–14001406.
  • Matsuo Y, Mizoguchi F, Kohsaka H, et al. Tocilizumab-induced immune complex glomerulonephritis in a patient with rheumatoid arthritis. Rheumatology (Oxford)). 2013;52(7):1341–1343.
  • Schmidt T, Paust H-J, Krebs CF, et al. Function of the Th17/interleukin-17A immune response in murine lupus nephritis. Arthritis Rheumatol. 2015;67(2):475–487.
  • Scalapino KJ, Tang Q, Bluestone JA, et al. Suppression of disease in New Zealand black/New Zealand white Lupus-Prone mice by adoptive transfer of ex vivo expanded regulatory T cells. J Immunol. 2006;177(3):1451–1459.

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.