Genetic inhibition of discoidin domain receptor 1 protects mice against crescentic glomerulonephritis

FASEB Journal

Volumn 26, Issue 10, 2012, Pages 4079-4091

  Kerroch, Monique ^a,d   Guerrot, Dominique ^a,d   Vandermeersch, Sophie ^a,d   Placier, Sandrine ^a,d   Mesnard, Laurent ^a,c,d   Jouanneau, Chantal ^a,d   Rondeau, Eric ^a,c,d   Ronco, Pierre ^a,b,d   Boffa, Jean Jacques ^a,b,d   Chatziantoniou, Christos ^a,d   Dussaule, Jean Claude ^a,d,e  

^a HÔPITAL TENON   (France)

^b Service de Nephrologie et Dialyse   (France)

^c ASSISTANCE PUBLIQUE HÔPITAUX DE PARIS   (France)

^d SORBONNE UNIVERSITÉ   (France)

^e HÔPITAL SAINT ANTOINE   (France)

Author keywords

Prevention of chronic kidney disease; Renal fibrosis; Renal inflammation; Renal pharmacogenetics

Indexed keywords

ANTISENSE OLIGODEOXYNUCLEOTIDE; COLLAGEN RECEPTOR; CREATININE; DISCOIDIN; DISCOIDIN DOMAIN RECEPTOR 1; DISCOIDIN DOMAIN RECEPTOR 1 BLOCKING AGENT; INTERLEUKIN 1BETA; NEPHRIN; PROTEIN; TOXIN; TRANSCRIPTOME; UNCLASSIFIED DRUG; UREA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CREATININE URINE LEVEL; DEATH; FEMALE; GLOMERULUS; HISTOLOGY; HYPERTENSION; IN VIVO STUDY; KIDNEY FUNCTION; MOUSE; NEPHROTOXIC SERUM; NONHUMAN; PODOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEINURIA; RAPIDLY PROGRESSIVE GLOMERULONEPHRITIS; SERUM; SURVIVAL; TRANSCRIPTOMICS; WILD TYPE;

ANIMALS; BLOOD PRESSURE; BLOOD UREA NITROGEN; BLOTTING, WESTERN; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GLOMERULONEPHRITIS; HUMANS; IMMUNOHISTOCHEMISTRY; KIDNEY GLOMERULUS; MICE; MICE, MUTANT STRAINS; MICE, TRANSGENIC; PROTEINURIA; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTORS, MITOGEN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

MUS; OVIS ARIES;

EID: 84868089019     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-194902     Document Type: Article

References (45)

1. Ronco, P., and Chatziantoniou, C. (2008) Matrix metalloproteinases and matrix receptors in progression and reversal of kidney disease: therapeutic perspectives. Kidney Int. 74, 873-878
2. Vogel, W. F., Abdulhussein, R., and Ford, C. E. (2006) Sensing extracellular matrix: an update on discoidin domain receptor function. Cell. Signal. 18, 1108-1116
3. Curat, C. A., and Vogel, W. F. (2002) Discoidin domain receptor 1 controls growth and adhesion of mesangial cells. J. Am. Soc. Nephrol. 13, 2648-2656
4. Vogel, W., Gish, G. D., Alves, F., and Pawson, T. (1997) The discoidin domain receptor tyrosine kinases are activated by collagen. Mol. Cell 1, 13-23
5. Hou, G., Vogel, W. F., and Bendeck, M. P. (2002) Tyrosine kinase activity of discoidin domain receptor 1 is necessary for smooth muscle cell migration and matrix metalloproteinase expression. Circ. Res. 90, 1147-1149
6. Agarwal, G., Mihai, C., and Iscru, D. F. (2007) Interaction of discoidin domain receptor 1 with collagen type 1. J. Mol. Biol. 367, 443-455
7. Hou, G., Vogel, W., and Bendeck, M. P. (2001) The discoidin domain receptor tyrosine kinase DDR1 in arterial wound repair. J. Clin. Invest. 107, 727-735
8. Meyer zum Gottesberge, A. M., Gross, O., Becker-Lendzian, U., Massing, T., and Vogel, W. F. (2008) Inner ear defects and hearing loss in mice lacking the collagen receptor DDR1. Lab. Invest. 88, 27-37
9. Vogel, W., Aszódi, A., Alves, F., and Pawson, T. (2001) Discoidin domain receptor 1 tyrosine kinase has an essential role in mammary gland development. Mol. Cell. Biol. 21, 2906-2917
10. Hidalgo-Carcedo, C., Hooper, S., Chaudhry, S. I., Williamson, P., Harrington, K., Leitinger, B., and Sahai, E. (2011) Collective cell migration requires suppression of actomyosin at cell-cell contacts mediated by DDR1 and the cell polarity regulators Par3 and Par6. Nat. Cell Biol. 13, 49-58
11. Park, H. S., Kim, K. R., Lee, H. J., Choi, H. N., Kim, D. K., Kim, B. T., and Moon, W. S. (2007) Overexpression of discoidin domain receptor 1 increases the migration and invasion of hepatocellular carcinoma cells in association with matrix metalloproteinase. Oncol. Rep. 18, 1435-1441
12. Guerrot, D., Kerroch, M., Placier, S., Vandermeersch, S., Trivin, C., Mael-Ainin, M., Chatziantoniou, C., and Dussaule, J. C. (2011) Discoidin domain receptor 1 is a major mediator of inflammation and fibrosis in obstructive nephropathy. Am. J. Pathol. 179, 83-91
13. Franco, C., Britto, K., Wong, E., Hou, G., Zhu, S. N., Chen, M., Cybulsky, M. I., and Bendeck, M. P. (2009) Discoidin domain receptor 1 on bone marrow-derived cells promotes macrophage accumulation during atherogenesis. Circ. Res. 105, 1141-1148
14. Flamant, M., Placier, S., Rodenas, A., Curat, C. A., Vogel, W. F., Chatziantoniou, C., and Dussaule, J. C. (2006) Discoidin domain receptor 1 null mice are protected against hypertensioninduced renal disease, J. Am. Soc. Nephrol. 17, 3374-3381
15. Gross, O., Girgert, R., Beirowki, B., Kretzler, M., Kang, H. G., Kruegel, J., Miosge, N., Busse, A. C., Segerer, S., Vogel, W. F., Muller, G. A., and Weber, M. (2010) Loss of collagen-receptor DDR1 delays renal fibrosis in hereditary type IV collagen disease, Matrix Biol. 29, 346-356
16. Mesnard, L., Keller, A. C., Michel, M. L., Vandermeersch, S., Rafat, C., Letavernier, E., Tillet, Y., Rondeau, E., and Leite-de- Moraes, M. C. (2009) Invariant natural killer T cells and TGF-beta attenuate anti-GBM glomerulonephritis. J. Am. Soc. Nephrol. 20, 1282-1292
17. Lendrum, A. C., Fraser, D. S., Slidders, W., and Henderson, R. (1962) Studies on the character and staining of fibrin. J. Clin. Pathol. 15, 401-413
18. Mundel, P., Reiser, J., Zuniga Mejia Borja, A., Pavenstadt, H., Davidson, G. R., Kriz, W., and Zeller, R. (1997) Rearrangements of the cytoskeleton and cell contacts induce process formation during differentiation of conditionally immortalized mouse podocyte cell lines. Exp. Cell Res. 236, 248-258
19. Mukai, E., Kume, N., Hayashida, K., Minami, M., Yamada, Y., Seino, Y., and Kita, T. (2004) Heparin-binding EGF-like growth factor induces expression of lectin-like oxidized LDL receptor-1 in vascular smooth muscle cells. Atherosclerosis 176, 289-296
20. Kamohara, H., Yamashiro, S., Galligan, C., and Yoshimura, T. (2001) Discoidin domain receptor 1 isoform-a (DDR1alpha) promotes migration of leukocytes in three-dimensional collagen lattices. FASEB J. 15, 2724-2726
21. Ruiz, P. A., and Jarai, G. (2011) Collagen I induces discoidin domain receptor (DDR) 1 expression through DDR2 and a JAK2-ERK1/2-mediated mechanism in primary human lung fibroblasts. J. Biol. Chem. 286, 12912-12923
22. Avivi-Green, C., Singal, M., and Vogel, W. F. (2006) Discoidin domain receptor 1-deficient mice are resistant to bleomycininduced lung fibrosis, Am. J. Respir. Crit. Care. Med. 174, 420-427
23. Gross, O., Beirowski, B., Harvey, S. J., McFadden, C., Chen, D., Tam, S., Thorner, P. S., Smyth, N., Addicks, K., Bloch, W., Ninomiya, Y., Sado, Y., Weber, M., and Vogel, W. F. (2004) DDR1-deficient mice show localized subepithelial GBM thickening with focal loss of slit diaphragms and proteinuria. Kidney Int. 66, 102-111
24. Marshall, C. B., Krofft, R. D., Blonski, M. J., Kowalewska, J., Logar, C. M., Pippin, J. W., Kim, F., Feil, R., Alpers, C. E., and Shankland, S. J. (2011) Role of smooth muscle protein SM22 α in glomerular epithelial cell injury. Am. J. Physiol. Renal Physiol. 300, F1026-F1042
25. Franco, C., Hou, G., Ahmad, P. J., Fu, E. Y. K., Koh, L., Vogel, W. F., and Bendeck, M. P. (2008) Discoidin domain receptor 1 deletion decreases atherosclerosis by accelerating cell matrix accumulation and reducing inflammation in low-density lipoprotein receptor-deficient mice. Circ. Res. 102, 1202-1211
26. Tipping, P. G., and Timoshanko, J. (2005) Contributions of intrinsic renal cells to crescentic glomerulonephritis. Nephron Exp. Nephrol. 101, 173-178
27. Timoshanko, J. R., Kitching, A. R., Iwakura, Y., Holdsworth, S. R., and Tipping, P. G. (2004) Leukocyte-derived interleukin-1beta interacts with renal interleukin-1 receptor I to promote renal tumor necrosis factor and glomerular injury in murine crescentic glomerulonephritis. Am. J. Pathol. 164, 1967-1977
28. Takano, Y., Yamauchi, K., Hayakawa, K., Hiramatsu, N., Kasai, A., Okamura, M., Yokouchi M, Shitamura, A., Yao, J., and Kitamura, M. (2007) Transcriptional suppression of nephrin in podocytes by macrophages: roles of inflammatory cytokines and involvement of the PI3K/Akt pathway. FEBS Lett. 581, 421-426
29. Bruggeman, L. A., Drawz, P. E., Kahoud, N., Lin, K., Barisoni, L., and Nelson, P. J. (2011) TNFR2 interposes the proliferative and NF-B-mediated inflammatory response by podocytes to TNF-α. Lab. Invest. 91, 413-425
30. Feng, L., Garcia, G. E., Yang, Y., Xia, Y., Gabbai, F. B., Peterson, O. W., Abraham, J. A., Blantz, R. C., and Wilson, C. B. (2000) Heparin-binding EGF-like growth factor contributes to reduced glomerular filtration rate during glomerulonephritis in rats. J. Clin. Invest. 105, 341-350
31. Bollée, G., Flamant, M., Schordan, S., Fligny, C., Rumpel, E., Milon, M., Schordan, E., Sabaa, N., Vandermeersch, S., Galaup, A., Rodenas, A., Casal, I., Sunnarborg, S. W., Salant, D. J., Kopp, J. B., Threadgill, D. W., Quaggin, S. E., Dussaule, J. C., Germain, S., Mesnard, L., Endlich, K., Boucheix, C., Belenfant, X., Callard, P., Endlich, N., and Tharaux, P. L. (2011) Epidermal growth factor receptor promotes glomerular injury and renal failure in rapidly progressive crescentic glomerulonephritis. Nat. Med. 17, 1242-1250
32. Seo, M. C., Kim, S., Kim, S. H., Zheng, L. T., Park, E. K., Lee, W. H., and Suk, K. (2008) Discoidin domain receptor 1 mediates collagen-induced inflammatory activation of microglia in culture. J. Neurosci. Res. 86, 1087-1095
33. Matsuyama, W., Wang, L., Farrar, W. L., Faure, M., and Yoshimura, T. (2004) Activation of discoidin domain receptor 1 isoform b with collagen up-regulates chemokine production in human macrophages: role of p38 mitogen-activated protein kinase and NF-kappa B. J. Immunol. 172, 2332-2340
34. Sheryanna, A., Bhangal, G., McDaid, J., Smith, J., Manning, A., Foxwell, B. M., Feldmann, M., Cook, H. T., Pusey, C. D., and Tam, F. W. (2007) Inhibition of p38 mitogen-activated protein kinase is effective in the treatment of experimental crescentic glomerulonephritis and suppresses monocyte chemoattractant protein-1 but not IL-1beta or IL-6. J. Am. Soc. Nephrol. 18, 1167-1179
35. Das, S., Ongusaha, P. P., Yang, Y. S., Park, J. M., Aaronson, S. A., and Lee, S. W. (2006) Discoidin domain receptor 1 receptor tyrosine kinase induces cyclooxygenase-2 and promotes chemoresistance through nuclear factor-kappa B pathway activation. Cancer Res. 66, 8123-8130
36. Singh, S. K., Jeansson, M., and Quaggin, S. E. (2011) New insights into the pathogenesis of cellular crescents. Curr. Opin. Nephrol. Hypertens. 20, 258-262
37. Burt, D., Salvidio, G., Tarabra, E., Barutta, F., Pinach, S., Dentelli, P., Camussi, G., Perin, P. C., and Gruden, G. (2007) The monocyte chemoattractant protein-1/cognate CC chemokine receptor 2 system affects cell motility in cultured human podocytes. Am. J. Pathol. 171, 1789-1799
38. Klein, J., Gonzalez, J., Decramer, S., Bandin, F., Neau, E., Salant, D. J., Heeringa, P., Pesquero, J. B., Schanstra, J. P., and Bascands, J. L. (2010) Blockade of the kinin B1 receptor ameliorates glomerulonephritis. J. Am. Soc. Nephrol. 2, 1157-1164
39. Hachehouche, L. N., Chetoui, N., and Aoudjit, F. (2010) Implication of discoidin domain receptor 1 in T cell migration in three-dimensional collagen. Mol. Immunol. 47, 1866-1869
40. Kitching, A. R., Kong, Y. Z., Huang, X. R., Davenport, P., Edgtton, K. L., Carmeliet, P., Holdsworth, S. R., and Tipping, P. G. (2003) Plasminogen activator inhibitor-1 is a significant determinant of renal injury in experimental crescentic glomerulonephritis. J. Am. Soc. Nephrol. 14, 1487-1495
41. Hertig, A., Berrou, J., Allory, Y., Breton, L., Commo, F., Costa De Beauregard, M.A., Carmeliet, P., and Rondeau, E. (2003) Type 1 plasminogen activator inhibitor deficiency aggravates the course of experimental glomerulonephritis through overactivation of transforming growth factor beta. FASEB J. 17, 1904-1906
42. Franco, C., Ahmad, P. J., Hou, G., Wong, E., and Bendeck, M. P. (2010) Increased cell and matrix accumulation during atherogenesis in mice with vessel wall-specific deletion of discoidin domain receptor 1. Circ. Res. 106, 1775-1783
43. Flynn, L., Blissett, A., Calomeni, E., and Agarwal, G. (2010) Inhibition of collagen fibrillogenesis by cells expressing soluble extracellular domains of DDR1 and DDR2. J. Mol. Biol. 395, 533-543
44. Day, E., Waters, B., Spiegel, K., Alnadaf, T., Manley, P. W., Buchdunger, E., Walker, C., and Jarai, G. (2008) Inhibition of collagen-induced discoidin domain receptor 1 and 2 activation by imatinib, nilotinib, and dasatinib. Eur. J. Pharmacol. 599, 44-53
45. Roig, B., Franco-Pons, N., Martorell, L., Tomàs, J., Vogel, W. F., and Vilella, E. (2010) Expression of the tyrosine kinase discoidin domain receptor 1 (DDR1) in human central nervous system myelin. Brain Res. 1336, 22-29