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Published in: International Urology and Nephrology 8/2018

01-08-2018 | Nephrology - Original Paper

Silencing of CXCL12 performs a protective effect on C5b-9-induced injury in podocytes

Authors: Wengang Sha, Lei Shen, Ling Zhou, Deyu Xu, Jing Yang, Guoyuan Lu

Published in: International Urology and Nephrology | Issue 8/2018

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Abstract

Purpose

Podocytes, terminal differentiation cell in glomerulu, are crucial to kidney-related diseases such as membranous nephropathy (MN). MN is characterized by podocyte injury and glomerular basement membrane thickening. This paper focused to investigate the expression of chemokine (C-X-C motif) ligand 12 (CXCL12) in MN patients and its possible role in podocyte injury.

Methods

Through the enzyme-linked immunosorbent assay, CXCL12 level in the serum and urine of MN patients was examined. Further, several assays of cell viability, apoptosis, quantitative real-time PCR and western blot were applied to explore the effects of CXCL12 in the model of podocyte injury.

Results

We found a significant increase of CXCL12 in serum and urine of MN patients, which indicated that CXCL12 may be involved in the progression of MN. And in vitro C5b-9-induced podocyte injury model, the proliferation of podocytes was inhibited whereas CXCL12/CXCR4 and phosphorylated STAT3 (p-STAT3) were increased. Silencing of CXCL12 remarkably promoted cell proliferation, inhibited cell apoptosis and suppressed CXCL12/CXCR4, p-STAT3 and caspase 3. Consistently, STAT3 inhibitor and berberine (a CXCL12 antagonist) also reduced CXCL12 treatment-induced apoptosis.

Conclusions

All data suggested that silencing of CXCL12 had a protective effect on podocyte injury, which may be through inhibiting CXCL12/STAT3 signaling pathway.
Literature
1.
go back to reference Ayalon R Jr, Beck LH Jr (2015) Membranous nephropathy: not just a disease for adults. Pediatr Nephrol 30(1):31–39CrossRefPubMed Ayalon R Jr, Beck LH Jr (2015) Membranous nephropathy: not just a disease for adults. Pediatr Nephrol 30(1):31–39CrossRefPubMed
2.
go back to reference Nachman P, Jennette J, Falk R (2008) Primary glomerular disease. In: Brenner BM (ed) Brenner and Rector’s The Kidney. Saunders, Philadelphia, PA, pp 987–1066 Nachman P, Jennette J, Falk R (2008) Primary glomerular disease. In: Brenner BM (ed) Brenner and Rector’s The Kidney. Saunders, Philadelphia, PA, pp 987–1066
3.
go back to reference Ruggenenti P, Chiurchiu C, Brusegan V, Abbate M, Perna A, Filippi C, Remuzzi G (2003) Rituximab in idiopathic membranous nephropathy: a one-year prospective study. J Am Soc Nephrol 14(7):1851–1857CrossRefPubMed Ruggenenti P, Chiurchiu C, Brusegan V, Abbate M, Perna A, Filippi C, Remuzzi G (2003) Rituximab in idiopathic membranous nephropathy: a one-year prospective study. J Am Soc Nephrol 14(7):1851–1857CrossRefPubMed
4.
go back to reference Sinico RA, Mezzina N, Trezzi B, Ghiggeri G, Radice A (2016) Immunology of membranous nephropathy: from animal models to humans. Clin Exp Immunol 183(2):157CrossRefPubMed Sinico RA, Mezzina N, Trezzi B, Ghiggeri G, Radice A (2016) Immunology of membranous nephropathy: from animal models to humans. Clin Exp Immunol 183(2):157CrossRefPubMed
5.
go back to reference Debiec H, Guigonis V, Mougenot B, Decobert F, Haymann JP, Bensman A, Deschênes G, Ronco PM (2002) Antenatal membranous glomerulonephritis due to anti-neutral endopeptidase antibodies. N Engl J Med 346(26):2053CrossRefPubMed Debiec H, Guigonis V, Mougenot B, Decobert F, Haymann JP, Bensman A, Deschênes G, Ronco PM (2002) Antenatal membranous glomerulonephritis due to anti-neutral endopeptidase antibodies. N Engl J Med 346(26):2053CrossRefPubMed
6.
go back to reference Kuroki A (2009) M-type phospholipase A2 receptor as target antigen in idiopathic membranous nephropathy. N Engl J Med (NEJM) 361(1):11–21CrossRef Kuroki A (2009) M-type phospholipase A2 receptor as target antigen in idiopathic membranous nephropathy. N Engl J Med (NEJM) 361(1):11–21CrossRef
7.
go back to reference Hoxha E, Harendza S, Zahner G, Panzer U, Steinmetz O, Kai F, Helmchen U, Stahl RAK (2011) An immunofluorescence test for phospholipase-A2-receptor antibodies and its clinical usefulness in patients with membranous glomerulonephritis. Nephrol Dial Transp 26(8):2526–2532CrossRef Hoxha E, Harendza S, Zahner G, Panzer U, Steinmetz O, Kai F, Helmchen U, Stahl RAK (2011) An immunofluorescence test for phospholipase-A2-receptor antibodies and its clinical usefulness in patients with membranous glomerulonephritis. Nephrol Dial Transp 26(8):2526–2532CrossRef
8.
go back to reference Prunotto M, Carnevali ML, Candiano G, Murtas C, Bruschi M, Corradini E, Trivelli A, Magnasco A, Petretto A, Santucci L (2010) Autoimmunity in membranous nephropathy targets aldose reductase and SOD2. J Am Soc Nephrol (JASN) 21(3):507CrossRef Prunotto M, Carnevali ML, Candiano G, Murtas C, Bruschi M, Corradini E, Trivelli A, Magnasco A, Petretto A, Santucci L (2010) Autoimmunity in membranous nephropathy targets aldose reductase and SOD2. J Am Soc Nephrol (JASN) 21(3):507CrossRef
9.
go back to reference Murtas C, Ravani P, Ghiggeri GM (2011) New insights into membranous glomerulonephritis: from bench to bedside. Nephrol Dial Transp 26(8):2428CrossRef Murtas C, Ravani P, Ghiggeri GM (2011) New insights into membranous glomerulonephritis: from bench to bedside. Nephrol Dial Transp 26(8):2428CrossRef
10.
go back to reference Bruschi M, Carnevali ML, Murtas C, Candiano G, Petretto A, Prunotto M, Gatti R, Argentiero L, Magistroni R, Garibotto G (2011) Direct characterization of target podocyte antigens and auto-antibodies in human membranous glomerulonephritis: alfa-enolase and borderline antigens. J Proteomics 74(10):2008–2017CrossRefPubMed Bruschi M, Carnevali ML, Murtas C, Candiano G, Petretto A, Prunotto M, Gatti R, Argentiero L, Magistroni R, Garibotto G (2011) Direct characterization of target podocyte antigens and auto-antibodies in human membranous glomerulonephritis: alfa-enolase and borderline antigens. J Proteomics 74(10):2008–2017CrossRefPubMed
11.
go back to reference Burns JM, Summers BC, Yu W, Melikian A, Berahovich R, Miao Z, Penfold MET, Sunshine MJ, Dan RL, Kuo CJ (2006) A novel chemokine receptor for SDF-1 and I-TAC involved in cell survival, cell adhesion, and tumor development. J Exp Med 203(9):2201CrossRefPubMedPubMedCentral Burns JM, Summers BC, Yu W, Melikian A, Berahovich R, Miao Z, Penfold MET, Sunshine MJ, Dan RL, Kuo CJ (2006) A novel chemokine receptor for SDF-1 and I-TAC involved in cell survival, cell adhesion, and tumor development. J Exp Med 203(9):2201CrossRefPubMedPubMedCentral
12.
go back to reference Sayyed SG, Hägele H, Kulkarni OP, Endlich K, Segerer S, Eulberg D, Klussmann S, Anders HJ (2009) Podocytes produce homeostatic chemokine stromal cell-derived factor-1/CXCL12, which contributes to glomerulosclerosis, podocyte loss and albuminuria in a mouse model of type 2 diabetes. Diabetologia 52(11):2445–2454CrossRefPubMed Sayyed SG, Hägele H, Kulkarni OP, Endlich K, Segerer S, Eulberg D, Klussmann S, Anders HJ (2009) Podocytes produce homeostatic chemokine stromal cell-derived factor-1/CXCL12, which contributes to glomerulosclerosis, podocyte loss and albuminuria in a mouse model of type 2 diabetes. Diabetologia 52(11):2445–2454CrossRefPubMed
13.
go back to reference Liao X, Pirapakaran T, Luo XM (2016) Chemokines and chemokine receptors in the development of lupus nephritis. Mediat Inflamm (2, article e63) Liao X, Pirapakaran T, Luo XM (2016) Chemokines and chemokine receptors in the development of lupus nephritis. Mediat Inflamm (2, article e63)
14.
go back to reference Schramme A, Abdelbakky MS, Gutwein P, Obermüller N, Baer PC, Hauser IA, Ludwig A, Gauer S, Schäfer L, Sobkowiak E (2008) Characterization of CXCL16 and ADAM10 in the normal and transplanted kidney. Kidney Int 74(3):328–338CrossRefPubMed Schramme A, Abdelbakky MS, Gutwein P, Obermüller N, Baer PC, Hauser IA, Ludwig A, Gauer S, Schäfer L, Sobkowiak E (2008) Characterization of CXCL16 and ADAM10 in the normal and transplanted kidney. Kidney Int 74(3):328–338CrossRefPubMed
16.
go back to reference Gutwein P, Abdel-Bakky MS, Schramme A, Kai D, Kämpfer-Kolb N, Amann K, Hauser IA, Obermüller N, Bartel C, Abdel-Aziz AAH (2009) CXCL16 is expressed in podocytes and acts as a scavenger receptor for oxidized low-density lipoprotein. Am J Pathol 174(6):2061–2072CrossRefPubMedPubMedCentral Gutwein P, Abdel-Bakky MS, Schramme A, Kai D, Kämpfer-Kolb N, Amann K, Hauser IA, Obermüller N, Bartel C, Abdel-Aziz AAH (2009) CXCL16 is expressed in podocytes and acts as a scavenger receptor for oxidized low-density lipoprotein. Am J Pathol 174(6):2061–2072CrossRefPubMedPubMedCentral
18.
go back to reference Wegenka UM, Buschmann J, Lütticken C, Heinrich PC, Horn F (1993) Acute-phase response factor, a nuclear factor binding to acute-phase response elements, is rapidly activated by interleukin-6 at the posttranslational level. Mol Cell Biol 13(1):276–288CrossRefPubMedPubMedCentral Wegenka UM, Buschmann J, Lütticken C, Heinrich PC, Horn F (1993) Acute-phase response factor, a nuclear factor binding to acute-phase response elements, is rapidly activated by interleukin-6 at the posttranslational level. Mol Cell Biol 13(1):276–288CrossRefPubMedPubMedCentral
19.
go back to reference Lutticken C, Wegenka UM, Yuan J, Buschmann J, Schindler C, Ziemiecki A, Harpur AG, Wilks AF, Yasukawa K, Taga T (1994) Association of transcription factor APRF and protein kinase Jak1 with the interleukin-6 signal transducer gp130. Science 263(5143):89CrossRefPubMed Lutticken C, Wegenka UM, Yuan J, Buschmann J, Schindler C, Ziemiecki A, Harpur AG, Wilks AF, Yasukawa K, Taga T (1994) Association of transcription factor APRF and protein kinase Jak1 with the interleukin-6 signal transducer gp130. Science 263(5143):89CrossRefPubMed
20.
go back to reference Akira S, Nishio Y, Inoue M, Wang XJ, Wei S, Matsusaka T, Yoshida K, Sudo T, Naruto M, Kishimoto T (1994) Molecular cloning of APRF, a novel IFN-stimulated gene factor 3 p91-related transcription factor involved in the gp130-mediated signaling pathway. Cell 77(1):63CrossRefPubMed Akira S, Nishio Y, Inoue M, Wang XJ, Wei S, Matsusaka T, Yoshida K, Sudo T, Naruto M, Kishimoto T (1994) Molecular cloning of APRF, a novel IFN-stimulated gene factor 3 p91-related transcription factor involved in the gp130-mediated signaling pathway. Cell 77(1):63CrossRefPubMed
21.
go back to reference Schindler C, Levy DE, Decker T (2007) JAK-STAT signaling: from interferons to cytokines. J Biol Chem 282(28):20059CrossRefPubMed Schindler C, Levy DE, Decker T (2007) JAK-STAT signaling: from interferons to cytokines. J Biol Chem 282(28):20059CrossRefPubMed
22.
go back to reference Dai Y, Gu L, Yuan W, Yu Q, Ni Z, Ross MJ, Kaufman L, Xiong H, Salant DJ, He JC, Chuang PY (2013) Podocyte-specific deletion of signal transducer and activator of transcription 3 attenuates nephrotoxic serum-induced glomerulonephritis. Kidney Int 84(5):950–961CrossRefPubMedPubMedCentral Dai Y, Gu L, Yuan W, Yu Q, Ni Z, Ross MJ, Kaufman L, Xiong H, Salant DJ, He JC, Chuang PY (2013) Podocyte-specific deletion of signal transducer and activator of transcription 3 attenuates nephrotoxic serum-induced glomerulonephritis. Kidney Int 84(5):950–961CrossRefPubMedPubMedCentral
23.
go back to reference Feng X, Lu TC, Chuang PY, Fang W, Ratnam K, Xiong H, Ouyang X, Shen Y, Levy DE, Hyink D (2009) Reduction of Stat3 activity attenuates HIV-induced kidney injury. J Am Soc Nephrol (JASN) 20(10):2138CrossRef Feng X, Lu TC, Chuang PY, Fang W, Ratnam K, Xiong H, Ouyang X, Shen Y, Levy DE, Hyink D (2009) Reduction of Stat3 activity attenuates HIV-induced kidney injury. J Am Soc Nephrol (JASN) 20(10):2138CrossRef
24.
go back to reference Liu R, Zhong Y, Li X, Chen H, Jim B, Zhou MM, Chuang PY, He JC (2014) Role of transcription factor acetylation in diabetic kidney disease. Diabetes 63(7):2440–2453CrossRefPubMedPubMedCentral Liu R, Zhong Y, Li X, Chen H, Jim B, Zhou MM, Chuang PY, He JC (2014) Role of transcription factor acetylation in diabetic kidney disease. Diabetes 63(7):2440–2453CrossRefPubMedPubMedCentral
25.
go back to reference Zhang W, Chen X, Shi S, Wei R, Wang J, Yamanaka N, Hong Q (2005) Expression and activation of STAT3 in chronic proliferative immune complex glomerulonephritis and the effect of fosinopril. Nephrol Dial Transp 20(5):892CrossRef Zhang W, Chen X, Shi S, Wei R, Wang J, Yamanaka N, Hong Q (2005) Expression and activation of STAT3 in chronic proliferative immune complex glomerulonephritis and the effect of fosinopril. Nephrol Dial Transp 20(5):892CrossRef
26.
go back to reference Arakawa T, Masaki T, Hirai T, Doi S, Kuratsune M, Arihiro K, Kohno N, Yorioka N (2008) Activation of signal transducer and activator of transcription 3 correlates with cell proliferation and renal injury in human glomerulonephritis. Nephrol Dial Transp 23(11):3418–3426CrossRef Arakawa T, Masaki T, Hirai T, Doi S, Kuratsune M, Arihiro K, Kohno N, Yorioka N (2008) Activation of signal transducer and activator of transcription 3 correlates with cell proliferation and renal injury in human glomerulonephritis. Nephrol Dial Transp 23(11):3418–3426CrossRef
27.
go back to reference He JC, Husain M, Sunamoto M, D’Agati VD, Klotman ME, Iyengar R, Klotman PE (2004) Nef stimulates proliferation of glomerular podocytes through activation of Src-dependent Stat3 and MAPK1,2 pathways. J Clin Investig 114(5):643–651CrossRefPubMed He JC, Husain M, Sunamoto M, D’Agati VD, Klotman ME, Iyengar R, Klotman PE (2004) Nef stimulates proliferation of glomerular podocytes through activation of Src-dependent Stat3 and MAPK1,2 pathways. J Clin Investig 114(5):643–651CrossRefPubMed
28.
go back to reference Liu X, Xiao Q, Bai X, Yu Z, Sun M, Zhao H, Mi X, Wang E, Yao W, Jin F (2014) Activation of STAT3 is involved in malignancy mediated by CXCL12-CXCR4 signaling in human breast cancer. Oncol Rep 32(6):2760CrossRefPubMed Liu X, Xiao Q, Bai X, Yu Z, Sun M, Zhao H, Mi X, Wang E, Yao W, Jin F (2014) Activation of STAT3 is involved in malignancy mediated by CXCL12-CXCR4 signaling in human breast cancer. Oncol Rep 32(6):2760CrossRefPubMed
30.
go back to reference Hong JY, Kang B, Ahyoun K, Seoyeon H, Jinhee A, Sunhwa L, Jonghyen K, Jae-Hak P, Doo-Sung C (2011) Development of a highly sensitive real-time one step RT-PCR combined complementary locked primer technology and conjugated minor groove binder probe. Virol J 8(1):1–6CrossRef Hong JY, Kang B, Ahyoun K, Seoyeon H, Jinhee A, Sunhwa L, Jonghyen K, Jae-Hak P, Doo-Sung C (2011) Development of a highly sensitive real-time one step RT-PCR combined complementary locked primer technology and conjugated minor groove binder probe. Virol J 8(1):1–6CrossRef
31.
go back to reference Pippin JW, Durvasula R, Petermann A, Hiromura K, Couser WG, Shankland SJ (2003) DNA damage is a novel response to sublytic complement C5b-9-induced injury in podocytes. J Clin Investig 111(6):877CrossRefPubMed Pippin JW, Durvasula R, Petermann A, Hiromura K, Couser WG, Shankland SJ (2003) DNA damage is a novel response to sublytic complement C5b-9-induced injury in podocytes. J Clin Investig 111(6):877CrossRefPubMed
32.
go back to reference Atreya R, Mudter J, Finotto S, Müllberg J, Jostock T, Wirtz S, Schütz M, Bartsch B, Holtmann M, Becker C, Strand D, Czaja J, Schlaak J, Lehr HA, Autschbach F, Schürmann G, Nishimoto N, Yoshizaki K, Ito H, Neurath MF (2010) Blockade of interleukin 6 trans signaling suppresses T-cell resistance against apoptosis in chronic intestinal inflammation: evidence in Crohn disease and experimental colitis in vivo. Nat Med. https://doi.org/10.1038/nm1110-1341 CrossRef Atreya R, Mudter J, Finotto S, Müllberg J, Jostock T, Wirtz S, Schütz M, Bartsch B, Holtmann M, Becker C, Strand D, Czaja J, Schlaak J, Lehr HA, Autschbach F, Schürmann G, Nishimoto N, Yoshizaki K, Ito H, Neurath MF (2010) Blockade of interleukin 6 trans signaling suppresses T-cell resistance against apoptosis in chronic intestinal inflammation: evidence in Crohn disease and experimental colitis in vivo. Nat Med. https://​doi.​org/​10.​1038/​nm1110-1341 CrossRef
33.
go back to reference Mitsuyama K, Matsumoto S, Rosejohn S, Suzuki A, Hara T, Tomiyasu N, Handa K, Tsuruta O, Funabashi H, Scheller J (2006) STAT3 activation via interleukin 6 trans-signalling contributes to ileitis in SAMP1/Yit mice. Gut 55(9):1263–1269CrossRefPubMedPubMedCentral Mitsuyama K, Matsumoto S, Rosejohn S, Suzuki A, Hara T, Tomiyasu N, Handa K, Tsuruta O, Funabashi H, Scheller J (2006) STAT3 activation via interleukin 6 trans-signalling contributes to ileitis in SAMP1/Yit mice. Gut 55(9):1263–1269CrossRefPubMedPubMedCentral
34.
go back to reference Finotto S, Eigenbrod T, Karwot R, Boross I, Doganci A, Ito H, Nishimoto N, Yoshizaki K, Kishimoto T, Rosejohn S (2007) Local blockade of IL-6R signaling induces lung CD4+T cell apoptosis in a murine model of asthma via regulatory T cells. Int Immunol 19(6):685–693CrossRefPubMed Finotto S, Eigenbrod T, Karwot R, Boross I, Doganci A, Ito H, Nishimoto N, Yoshizaki K, Kishimoto T, Rosejohn S (2007) Local blockade of IL-6R signaling induces lung CD4+T cell apoptosis in a murine model of asthma via regulatory T cells. Int Immunol 19(6):685–693CrossRefPubMed
35.
go back to reference Rabe B, Chalaris A, May U, Waetzig GH, Seegert D, Williams AS, Jones SA, Rose-John S, Scheller J (2008) Transgenic blockade of interleukin 6 transsignaling abrogates inflammation. Blood 111(3):1021CrossRefPubMed Rabe B, Chalaris A, May U, Waetzig GH, Seegert D, Williams AS, Jones SA, Rose-John S, Scheller J (2008) Transgenic blockade of interleukin 6 transsignaling abrogates inflammation. Blood 111(3):1021CrossRefPubMed
36.
go back to reference Matsumoto S, Hara T, Mitsuyama K, Yamamoto M, Tsuruta O, Sata M, Scheller J, Rosejohn S, Kado S, Takada T (2010) Essential roles of IL-6 trans-signaling in colonic epithelial cells, induced by the IL-6/soluble-IL-6 receptor derived from lamina propria macrophages, on the development of colitis-associated premalignant cancer in a murine model. J Immunol 184(3):1543–1551CrossRefPubMed Matsumoto S, Hara T, Mitsuyama K, Yamamoto M, Tsuruta O, Sata M, Scheller J, Rosejohn S, Kado S, Takada T (2010) Essential roles of IL-6 trans-signaling in colonic epithelial cells, induced by the IL-6/soluble-IL-6 receptor derived from lamina propria macrophages, on the development of colitis-associated premalignant cancer in a murine model. J Immunol 184(3):1543–1551CrossRefPubMed
37.
go back to reference Greenhill CJ, Rosejohn S, Lissilaa R, Ferlin W, Ernst M, Hertzog PJ, Mansell A, Jenkins BJ (2010) IL-6 trans-signaling modulates TLR4-dependent inflammatory responses via STAT3. J Immunol 52(1–2):1199 Greenhill CJ, Rosejohn S, Lissilaa R, Ferlin W, Ernst M, Hertzog PJ, Mansell A, Jenkins BJ (2010) IL-6 trans-signaling modulates TLR4-dependent inflammatory responses via STAT3. J Immunol 52(1–2):1199
38.
go back to reference Lesina M, Kurkowski MU, Ludes K, Rose-John S, Treiber M, Klöppel G, Yoshimura A, Reindl W, Sipos B, Akira S (2011) Stat3/Socs3 activation by IL-6 transsignaling promotes progression of pancreatic intraepithelial neoplasia and development of pancreatic cancer. Cancer Cell 19(4):456–469CrossRefPubMed Lesina M, Kurkowski MU, Ludes K, Rose-John S, Treiber M, Klöppel G, Yoshimura A, Reindl W, Sipos B, Akira S (2011) Stat3/Socs3 activation by IL-6 transsignaling promotes progression of pancreatic intraepithelial neoplasia and development of pancreatic cancer. Cancer Cell 19(4):456–469CrossRefPubMed
39.
go back to reference Lo CW, Chen MW, Hsiao M, Wang S, Chen CA, Hsiao SM, Chang JS, Lai TC, Rose-John S, Kuo ML (2011) IL-6 trans-signaling in formation and progression of malignant ascites in ovarian cancer. Cancer Res 71(2):424–434CrossRefPubMed Lo CW, Chen MW, Hsiao M, Wang S, Chen CA, Hsiao SM, Chang JS, Lai TC, Rose-John S, Kuo ML (2011) IL-6 trans-signaling in formation and progression of malignant ascites in ovarian cancer. Cancer Res 71(2):424–434CrossRefPubMed
40.
go back to reference Jasiewicz M, Knapp M, Waszkiewicz E, Ptaszynska-Kopczynska K, Szpakowicz A, Sobkowicz B, Musial WJ, Kaminski KA (2015) Enhanced IL-6 trans-signaling in pulmonary arterial hypertension and its potential role in disease-related systemic damage. Cytokine 76(2):187–192CrossRefPubMed Jasiewicz M, Knapp M, Waszkiewicz E, Ptaszynska-Kopczynska K, Szpakowicz A, Sobkowicz B, Musial WJ, Kaminski KA (2015) Enhanced IL-6 trans-signaling in pulmonary arterial hypertension and its potential role in disease-related systemic damage. Cytokine 76(2):187–192CrossRefPubMed
41.
go back to reference Dalla VM, Mussap M, Gallina P, Bruseghin M, Cernigoi AM, Saller A, Plebani M, Fioretto P (2005) Acute-phase markers of inflammation and glomerular structure in patients with type 2 diabetes. J Am Soc Nephrol (JASN) 16(Suppl 1):S78CrossRef Dalla VM, Mussap M, Gallina P, Bruseghin M, Cernigoi AM, Saller A, Plebani M, Fioretto P (2005) Acute-phase markers of inflammation and glomerular structure in patients with type 2 diabetes. J Am Soc Nephrol (JASN) 16(Suppl 1):S78CrossRef
42.
go back to reference Suzuki D, Miyazaki M, Naka R, Koji T, Yagame M, Jinde K, Endoh M, Nomoto Y, Sakai H (1995) In situ hybridization of interleukin 6 in diabetic nephropathy. Diabetes 44(10):1233–1238CrossRefPubMed Suzuki D, Miyazaki M, Naka R, Koji T, Yagame M, Jinde K, Endoh M, Nomoto Y, Sakai H (1995) In situ hybridization of interleukin 6 in diabetic nephropathy. Diabetes 44(10):1233–1238CrossRefPubMed
Metadata
Title
Silencing of CXCL12 performs a protective effect on C5b-9-induced injury in podocytes
Authors
Wengang Sha
Lei Shen
Ling Zhou
Deyu Xu
Jing Yang
Guoyuan Lu
Publication date
01-08-2018
Publisher
Springer Netherlands
Published in
International Urology and Nephrology / Issue 8/2018
Print ISSN: 0301-1623
Electronic ISSN: 1573-2584
DOI
https://doi.org/10.1007/s11255-018-1799-8

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