Albumin stimulates renal tubular inflammation through an HSP70-TLR4 axis in mice with early diabetic nephropathy

DMM Disease Models and Mechanisms

Volumn 8, Issue 10, 2015, Pages 1311-1321

  Jheng, Huei Fen ^a   Tsai, Pei Jane ^a   Chuang, Yi Lun ^a   Shen, Yi Ting ^b   Tai, Ting An ^a   Chen, Wen Chung ^b   Chou, Chuan Kai ^c   Ho, Li Chun ^d   Tang, Ming Jer ^a   Lai, Kuei Tai A ^e   Sung, Junne Ming ^b   Tsai, Yau Sheng ^a,b  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^b NATIONAL CHENG KUNG UNIVERSITY HOSPITAL   (Taiwan)

^c NATIONAL APPLIED RESEARCH LABORATORIES   (Taiwan)

^d E DA HOSPITAL   (Taiwan)

^e R and D Center NovoTaiwan Biotech   (Taiwan)

Author keywords

Albuminuria; Damage associated molecular pattern (DAMP); Diabetic nephropathy; Toll like receptor; Tubular injury

Indexed keywords

ALBUMIN; ANTIINFLAMMATORY AGENT; CASPASE 3; CUBILIN; GLUCOSE; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 70 ANTIBODY; HIGH MOBILITY GROUP B1 PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; KIDNEY INJURY MOLECULE 1; KNK 437; MONOCYTE CHEMOTACTIC PROTEIN 1; PIFITHRIN MU; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VER 155008; ALBUMINOID; AUTACOID; TLR2 PROTEIN, MOUSE; TLR4 PROTEIN, MOUSE;

ALBUMINURIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DIABETIC NEPHROPATHY; GENE EXPRESSION; GLOMERULOPATHY; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; INTERSTITIAL NEPHRITIS; KIDNEY BIOPSY; KIDNEY PROXIMAL TUBULE; KIDNEY TUBULE; KIDNEY TUBULE DAMAGE; MALE; MEDIATOR RELEASE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN SECRETION; RENAL PROTECTION; UPREGULATION; ANIMAL; BIOPSY; C57BL MOUSE; COMPLICATION; DEFICIENCY; DRUG EFFECTS; HEK293 CELL LINE; INFLAMMATION; LLC PK1 CELL LINE; METABOLISM; PATHOLOGY; PIG; SIGNAL TRANSDUCTION;

ALBUMINS; ALBUMINURIA; ANIMALS; APOPTOSIS; BIOPSY; DIABETIC NEPHROPATHIES; GLUCOSE; HEK293 CELLS; HMGB1 PROTEIN; HSP70 HEAT-SHOCK PROTEINS; HUMANS; INFLAMMATION; INFLAMMATION MEDIATORS; KIDNEY TUBULES, PROXIMAL; LLC-PK1 CELLS; MICE, INBRED C57BL; NF-KAPPA B; SIGNAL TRANSDUCTION; SWINE; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4; UP-REGULATION;

EID: 84943428718     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.019398     Document Type: Article

References (47)

1. Batsford, S., Duermueller, U., Seemayer, C., Mueller, C., Hopfer, H. and Mihatsch, M. (2011). Protein level expression of Toll-like receptors 2, 4 and 9 in renal disease. Nephrol. Dial. Transplant. 26, 1413-1416.
2. Birn, H. and Christensen, E. I. (2006). Renal albumin absorption in physiology and pathology. Kidney Int. 69, 440-449.
3. Breyer, M. D., Bottinger, E., Brosius, F. C., III, Coffman, T. M., Harris, R. C., Heilig, C. W. and Sharma, K. (2005). Mouse models of diabetic nephropathy. J. Am. Soc. Nephrol. 16, 27-45.
4. Brosius, F. C., III, Alpers, C. E., Bottinger, E. P., Breyer, M. D., Coffman, T. M., Gurley, S. B., Harris, R. C., Kakoki, M., Kretzler, M., Leiter, E. H. et al. (2009). Mouse models of diabetic nephropathy. J. Am. Soc. Nephrol. 20, 2503-2512.
5. Brown, H. J., and Lock, H. R., Wolfs, T. G. A. M., Buurman, W. A., Sacks, S. H. and Robson, M. G. (2007). Toll-like receptor 4 ligation on intrinsic renal cells contributes to the induction of antibody-mediated glomerulonephritis via CXCL1 and CXCL2. J. Am. Soc. Nephrol. 18, 1732-1739.
6. Burton, C. and Harris, K. P. G. (1996). The role of proteinuria in the progression of chronic renal failure. Am. J. Kidney Dis. 27, 765-775.
7. Cai, W.-F., Zhang, X.-W., Yan, H.-M., Ma, Y.-G., Wang, X.-X., Yan, J., Xin, B.-M., Lv, X.-X., Wang, Q.-Q., Wang, Z.-Y. et al. (2010). Intracellular or extracellular heat shock protein 70 differentially regulates cardiac remodelling in pressure overload mice. Cardiovasc. Res. 88, 140-149.
8. Calabrese, V., Mancuso, C., Sapienza, M., Puleo, E., Calafato, S., Cornelius, C., Finocchiaro, M., Mangiameli, A., Di Mauro, M., Stella, A. M. et al. (2007). Oxidative stress and cellular stress response in diabetic nephropathy. Cell Stress Chaperones 12, 299-306.
9. Chen, W.-C., Lin, H.-H. and Tang, M.-J. (2014). Regulation of proximal tubular cell differentiation and proliferation in primary culture by matrix stiffness and ECM components. Am. J. Physiol. Renal Physiol. 307, F695-F707.
10. Christensen, E.I., Birn, H., Storm, T., Weyer, K. and Nielsen, R. (2012). Endocytic receptors in the renal proximal tubule. Physiology 27, 223-236.
11. Cunningham, P. N., Wang, Y., Guo, R., He, G. and Quigg, R. J. (2004). Role of Tolllike receptor 4 in endotoxin-induced acute renal failure. J. Immunol. 172, 2629-2635.
12. Dasu, M. R., Devaraj, S., Park, S. and Jialal, I. (2010). Increased toll-like receptor (TLR) activation and TLR ligands in recently diagnosed type 2 diabetic subjects. Diabetes Care 33, 861-868.
13. Devaraj, S., Tobias, P., Kasinath, B. S., Ramsamooj, R., Afify, A. and Jialal, I. (2011). Knockout of toll-like receptor-2 attenuates both the proinflammatory state of diabetes and incipient diabetic nephropathy. Arterioscler. Thromb. Vasc. Biol. 31, 1796-1804.
14. Eddy, A. A. (1989). Interstitial nephritis induced by protein-overload proteinuria. Am. J. Pathol. 135, 719-733.
15. Gekle, M. (2005). Renal tubule albumin transport. Annu. Rev. Physiol. 67, 573-594.
16. Gilbert, R. E. and Cooper, M. E. (1999). The tubulointerstitium in progressive diabetic kidney disease: more than an aftermath of glomerular injury? Kidney Int. 56, 1627-1637.
17. Gross, J. L., de Azevedo, M. J., Silveiro, S. P., Canani, L. H., Caramori, M. L. and Zelmanovitz, T. (2005). Diabetic nephropathy: diagnosis, prevention, and treatment. Diabetes Care 28, 164-176.
18. Kaseda, R., Hosojima, M., Sato, H. and Saito, A. (2011). Role of megalin and cubilin in the metabolism of vitamin D(3). Ther. Apher. Dial. 15 Suppl. 1, 14-17.
19. Kuwabara, T., Mori, K., Mukoyama, M., Kasahara, M., Yokoi, H., Saito, Y., Ogawa, Y., Imamaki, H., Kawanishi, T., Ishii, A. et al. (2012). Exacerbation of diabetic nephropathy by hyperlipidaemia is mediated by Toll-like receptor 4 in mice. Diabetologia 55, 2256-2266.
20. Leemans, J. C., Stokman, G., Claessen, N., Rouschop, K. M., Teske, G. J. D., Kirschning, C. J., Akira, S., van der Poll, T., Weening, J. J. and Florquin, S. (2005). Renal-associated TLR2 mediates ischemia/reperfusion injury in the kidney. J. Clin. Invest. 115, 2894-2903.
21. Leheste, J.-R., Rolinski, B., Vorum, H., Hilpert, J., Nykjaer, A., Jacobsen, C., Aucouturier, P., Moskaug, J. O., Otto, A., Christensen, E. I. et al. (1999). Megalin knockout mice as an animal model of low molecular weight proteinuria. Am. J. Pathol. 155, 1361-1370.
22. Li, F., Yang, N., Zhang, L., Tan, H., Huang, B., Liang, Y., Chen, M. and Yu, X. (2010). Increased expression of toll-like receptor 2 in rat diabetic nephropathy. Am. J. Nephrol. 32, 179-186.
23. Lin, M., and Yiu, W. H., Wu, H. J., Chan, L. Y. Y., Leung, J. C. K., Au, W. S., Chan, K. W., Lai, K. N. and Tang, S. C. W. (2012). Toll-like receptor 4 promotes tubular inflammation in diabetic nephropathy. J. Am. Soc. Nephrol. 23, 86-102.
24. Lin, M., and Yiu, W. H., Li, R. X., Wu, H. J., Wong, D. W. L., Chan, L. Y. Y., Leung, J. C. K., Lai, K. N. and Tang, S. C. W. (2013). The TLR4 antagonist CRX-526 protects against advanced diabetic nephropathy. Kidney Int. 83, 887-900.
25. Liu, J., Li, K., He, Y., Zhang, J., Wang, H., Yang, J., Zhan, J. and Liang, H. (2011). Anticubilin antisense RNA ameliorates adriamycin-induced tubulointerstitial injury in experimental rats. Am. J. Med. Sci. 342, 494-502.
26. Liu, W. J., Xu, B.-H., Ye, L., Liang, D., Wu, H.-L., Zheng, Y.-Y., Deng, J. K., Li, B. and Liu, H.-F. (2015). Urinary proteins induce lysosomal membrane permeabilization and lysosomal dysfunction in renal tubular epithelial cells. Am. J. Physiol. Renal Physiol. 308, F639-F649.
27. Miyake, K. (2007). Innate immune sensing of pathogens and danger signals by cell surface Toll-like receptors. Semin. Immunol. 19, 3-10.
28. Molitch, M. E., and DeFronzo, R. A., Franz, M. J., Keane, W. F., and Mogensen, C. E., Parving, H. H. and Steffes, M. W. (2004). Nephropathy in diabetes. Diabetes Care 27 Suppl. 1, S79-S83.
29. Mudaliar, H., Pollock, C., Komala, M. G., and Chadban, S. J., Wu, H. and Panchapakesan, U. (2013). The role of toll-like receptor proteins (Tlr) 2 and 4 in mediating inflammation in proximal tubules. Am. J. Physiol. Renal Physiol. 305, F143-F154.
30. Nakhjavani, M., Morteza, A., Khajeali, L., Esteghamati, A., Khalilzadeh, O., Asgarani, F. and Outeiro, T. F. (2010). Increased serum HSP70 levels are associated with the duration of diabetes. Cell Stress Chaperones 15, 959-964.
31. Navarro-Gonzalez, J. F. and Mora-Fernandez, C. (2008). The role of inflammatory cytokines in diabetic nephropathy. J. Am. Soc. Nephrol. 19, 433-442.
32. Ohse, T., Inagi, R., Tanaka, T., Ota, T., Miyata, T., Kojima, I., Ingelfinger, J. R., Ogawa, S., Fujita, T. and Nangaku, M. (2006). Albumin induces endoplasmic reticulum stress and apoptosis in renal proximal tubular cells. Kidney Int. 70, 1447-1455.
33. Oken, D. E. and Flamenbaum, W. (1971). Micropuncture studies of proximal tubule albumin concentrations in normal and nephrotic rats. J. Clin. Invest. 50, 1498-1505.
34. Pulskens, W. P., Rampanelli, E., Teske, G. J., and Butter, L. M., Claessen, N., Luirink, I. K., van der Poll, T., Florquin, S. and Leemans, J. C. (2010). TLR4 promotes fibrosis but attenuates tubular damage in progressive renal injury. J. Am. Soc. Nephrol. 21, 1299-1308.
35. Remuzzi, G., Ruggenenti, P. and Benigni, A. (1997). Understanding the nature of renal disease progression. Kidney Int. 51, 2-15.
36. Rubartelli, A. and Lotze, M. T. (2007). Inside, outside, upside down: damage-associated molecular-pattern molecules (DAMPs) and redox. Trends Immunol. 28, 429-436.
37. Russo, L. M., and Sandoval, R. M., McKee, M., Osicka, T. M., and Collins, A. B., Brown, D., Molitoris, B. A. and Comper, W. D. (2007). The normal kidney filters nephrotic levels of albumin retrieved by proximal tubule cells: retrieval is disrupted in nephrotic states. Kidney Int. 71, 504-513.
38. Russo, L. M., and Sandoval, R. M., Campos, S. B., Molitoris, B. A., Comper, W. D. and Brown, D. (2009). Impaired tubular uptake explains albuminuria in early diabetic nephropathy. J. Am. Soc. Nephrol. 20, 489-494.
39. Schlecht, R., and Scholz, S. R., Dahmen, H., Wegener, A., Sirrenberg, C., Musil, D., Bomke, J., Eggenweiler, H.-M., Mayer, M. P. and Bukau, B. (2013). Functional analysis of Hsp70 inhibitors. PLoS ONE 8, e78443.
40. Sreedharan, R., Chen, S., Miller, M., Haribhai, D., Williams, C. B. and Van Why, S. K. (2014). Mice with an absent stress response are protected against ischemic renal injury. Kidney Int. 86, 515-524.
41. Tang, S., Leung, J. C. K., Abe, K., Chan, K. W., Chan, L.Y.Y., Chan, T. M. and Lai, K. N. (2003). Albumin stimulates interleukin-8 expression in proximal tubular epithelial cells in vitro and in vivo. J. Clin. Invest. 111, 515-527.
42. Thomas, M. C., Burns, W. C. and Cooper, M. E. (2005). Tubular changes in early diabetic nephropathy. Adv. Chronic Kidney Dis. 12, 177-186.
43. Tojo, A. and Endou, H. (1992). Intrarenal handling of proteins in rats using fractional micropuncture technique. Am. J. Physiol. 263, F601-F606.
44. Tojo, A., Onozato, M., Ha, H., Kurihara, H., Sakai, T., Goto, A., Fujita, T. and Endou, H. (2001). Reduced albumin reabsorption in the proximal tubule of early-stage diabetic rats. Histochem. Cell Biol. 116, 269-276.
45. Wang, Y., Rangan, G.K., Tay, Y.C. and Harris, D. C. (1999). Inductionofmonocyte chemoattractant protein-1 by albumin is mediated by nuclear factor kappaB in proximal tubule cells. J. Am. Soc. Nephrol. 10, 1204-1213.
46. Zhang, L., Fok, J. J. L., Mirabella, F., Aronson, L. I., and Fryer, R. A., Workman, P., Morgan, G. J. and Davies, F. E. (2013). Hsp70 inhibition induces myeloma cell death via the intracellular accumulation of immunoglobulin and the generation of proteotoxic stress. Cancer Lett. 339, 49-59.
47. Zoja, C., Morigi, M. and Remuzzi, G. (2003). Proteinuria and phenotypic change of proximal tubular cells. J. Am. Soc. Nephrol. 14 Suppl. 1, S36-S41.