Loss of collagen-receptor DDR1 delays renal fibrosis in hereditary type IV collagen disease

Matrix Biology

Volumn 29, Issue 5, 2010, Pages 346-356

  Gross, Oliver ^a,b   Girgert, Rainer ^a   Beirowski, Bogdan ^b   Kretzler, Matthias ^c   Kang, Hee Gyung ^c,g   Kruegel, Jenny ^d   Miosge, Nicolai ^d   Busse, Ann Christin ^d   Segerer, Stephan ^e   Vogel, Wolfgang F ^f   Müller, Gerhard Anton ^a   Weber, Manfred ^b  

^a UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^b UNIVERSITY OF WITTEN HERDECKE   (Germany)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF GÖTTINGEN   (Germany)

^e UNIVERSITY OF ZURICH   (Switzerland)

^f UNIVERSITY OF TORONTO   (Canada)

^g Seoul National University Children's Hospital   (South Korea)

Author keywords

Alport syndrome; Collagen receptors; Hereditary kidney disease; Renal fibrosis; Type IV collagen

Indexed keywords

COLLAGEN RECEPTOR; CONNECTIVE TISSUE GROWTH FACTOR; DISCOIDIN; DISCOIDIN DOMAIN RECEPTOR 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; UREA; CD3 ANTIGEN; COLLAGEN TYPE 4; CTGF PROTEIN, MOUSE; DDR1 PROTEIN, MOUSE; PROTEIN TYROSINE KINASE; RNA;

ALPORT SYNDROME; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHRONIC INFLAMMATION; COLLAGEN DISEASE; DOWN REGULATION; EXTRACELLULAR MATRIX; FEMALE; HEREDITARY TYPE IV COLLAGEN DISEASE; IMMUNOGOLD STAINING; IN SITU HYBRIDIZATION; KIDNEY FIBROSIS; KIDNEY FUNCTION; LIFESPAN; LYMPHOCYTIC INFILTRATION; MACROPHAGE; MOUSE; NEPHRITIS; NONHUMAN; PATHOGENESIS; PODOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEINURIA; T LYMPHOCYTE; UREA NITROGEN BLOOD LEVEL; UREMIA; ANIMAL; BLOOD; CHEMISTRY; ELECTRON MICROSCOPY; FIBROSIS; GENETICS; GLOMERULUS; HUMAN; IMMUNOHISTOCHEMISTRY; INSTITUTE FOR CANCER RESEARCH MOUSE; KNOCKOUT MOUSE; LONGEVITY; MALE; METABOLISM; PATHOPHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ULTRASTRUCTURE;

ANIMALS; ANTIGENS, CD3; COLLAGEN TYPE IV; CONNECTIVE TISSUE GROWTH FACTOR; FEMALE; FIBROSIS; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; KIDNEY GLOMERULUS; LONGEVITY; MALE; MICE; MICE, INBRED ICR; MICE, KNOCKOUT; MICROSCOPY, ELECTRON; NEPHRITIS, HEREDITARY; NF-KAPPA B; PROTEINURIA; RECEPTOR PROTEIN-TYROSINE KINASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA; TRANSFORMING GROWTH FACTOR BETA; UREA;

ANIMALIA; MUS;

EID: 77954458648     PISSN: 0945053X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.matbio.2010.03.002     Document Type: Article

References (35)

1. Abdulhussein R., Koo D.H., Vogel W.F. Identification of disulfide-linked dimers of the receptor tyrosine kinase DDR1. J. Biol. Chem. 2 2008, 283(18):12026-12033.
2. Abrahamson D.R., Hudson B.G., Stroganova L., Borza D.B., St John P.L. Cellular origins of glomerular basement membrane type IV collagen networks. J. Am. Soc. Nephrol. 2009, 20(7):1471-1479. Jul, Electronic publication 2009 May 7.
3. Avivi-Green C., Singal M., Vogel W.F. Discoidin domain receptor 1-deficient mice are resistant to bleomycin-induced lung fibrosis. Am. J. Respir. Crit. Care 15 2006, 174(4):420-427.
4. Borza D.B., Bondar O., Todd P., Sundaramoorthy M., Sado Y., Ninomiya Y., Hudson B.G. Quaternary organization of the goodpasture autoantigen, the alpha 3(IV) collagen chain. Sequestration of two cryptic autoepitopes by intrapromoter interactions with the alpha4 and alpha5 NC1 domains. J. Biol. Chem. 2002, 277:40075-40083.
5. Cohen C.D., Frach K., Schlöndorff D., Kretzler M. Quantitative gene expression analysis in renal biopsies: a novel protocol for a high-throughput multicenter application. Kidney Int. 2002, 61:133-140.
6. Cosgrove D., Meehan D.T., Grunkemeyer J.A., Kornak J.M., Sayers R., Hunter W.J., Samuelson G.C. Collagen COL4A3 knockout: a mouse model for autosomal Alport syndrome. Genes Dev. 1996, 10:2981-2992.
7. Cosgrove D., Rodgers K., Meehan D., Miller C., Bovard K., Gilroy A., Gardner H., Kotelianski V., Gotwals P., Amatucci A., Kalluri R. Integrin alpha1beta1 and transforming growth factor-beta1 play distinct roles in alport glomerular pathogenesis and serve as dual targets for metabolic therapy. Am. J. Pathol. 2000, 157:1649-1659.
8. Curat C.A., Vogel W.F. Discoidin domain receptor 1 controls growth and adhesion of mesangial cells. J. Am. Soc. Nephrol. 2002, 13:2648-2656.
9. Flamant M., Placier S., Rodenas A., Curat C.A., Vogel W.F., Chatziantoniou C., Dussaule J.C. Discoidin domain receptor 1 null mice are protected against hypertension-induced renal disease. J. Am. Soc. Nephrol. 2006, 17(12):3374-3381.
10. Franco C., Hou G., Ahmad P.J., Fu E.Y., Koh L., Vogel W.F., Bendeck M.P. Discoidin domain receptor 1 (ddr1) deletion decreases atherosclerosis by accelerating matrix accumulation and reducing inflammation in low-density lipoprotein receptor-deficient mice. Circ. Res. 23 2008, 102(10):1202-1211.
11. Gross O., Netzer K.-O., Lambrecht R., Jung C., Seibold S., Leinonen A., Weber M. Meta-analysis of genotype-phenotype correlation in X-linked Alport Syndrome: impact on genetic counseling. Nephrol. Dial. Transpl. 2002, 17:1218-1227.
12. Gross O., Beirowski B., Koepke M.-L., Kuck J., Reiner M., Addicks K., Smyth N., Schulze-Lohoff E., Weber M. Preemptive ramipril therapy delays renal failure and reduces renal fibrosis in COL4A3-knockout mice with Alport syndrome. Kidney Int. 2003, 63:438-446.
13. Gross O., Schulze-Lohoff E., Koepke M.-L., Beirowski B., Addicks K., Bloch W., Smyth N., Weber M. Antifibrotic, nephroprotective potential of ACE-inhibitor vs AT1 antagonist in a murine model of renal fibrosis. Nephrol. Dial. Transplant. 2004, 19:1716-1723.
14. 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., Vogel W. DDR1-deficient mice show localized subepithelial GBM thickening with focal loss of slit diaphragms and proteinuria. Kidney Int. 2004, 66:102-111.
15. Hou G., Vogel W.F., Bendeck M.P. Tyrosine kinase activity of discoidin domain receptor 1 is necessary for smooth muscle cell migration and matrix metalloproteinase expression. Circ. Res. 2002, 90:1147-1149.
16. Hudson B.G., Tryggvason K., Sundaramoorthy M., Neilson E.G. Alport's syndrome, Goodpasture's syndrome, and type IV collagen. N. Engl. J. Med. 2003, 348:2543-2556.
17. Kashtan C.E. Familial hematuria due to type IV collagen mutations: alport syndrome and thin basement membrane nephropathy. Curr. Opin. Pediatr. 2004, 16(2):177-181.
18. Kriz W. Fenestrated glomerular capillaries are unique. J. Am. Soc. Nephrol. 2008, 19:1439-1440.
19. Kruegel J., Sadowski B., Miosge N. Nidogen-1 and nidogen-2 in healthy human cartilage and in late-stage osteoarthritis cartilage. Arthritis Rheum. 2008, 58(5):1422-1432.
20. Lebleu V.S., Sugimoto H., Miller C.A., Gattone V.H., Kalluri R. Lymphocytes are dispensable for glomerulonephritis but required for renal interstitial fibrosis in matrix defect-induced Alport renal disease. Lab. Invest. 2008, 88(3):284-292.
21. L'hote C.G., Thomas P.H., Ganesan T.S. Functional analysis of discoidin domain receptor 1: effect of adhesion on DDR1 phosphorylation. FASEB J. 2002, 16:234-236.
22. Matsuyama W., Wang L., Farrar W.L., Faure M., Yoshimura T. 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. 15 2004, 172(4):2332-2340.
23. Meyer zum Gottesberge A.M., Gross O., Becker-Lendzian U., Massing T., Vogel W.F. Inner ear defects and hearing loss in mice lacking the collagen receptor DDR1. Lab. Invest. 2007, 88(1):27-37.
24. Miner J.H., Sanes J.R. Collagen IV alpha 3, alpha 4, and alpha 5 chains in rodent basal laminae: sequence, distribution, association with laminins, and developmental switches. J. Cell Biol. 1994, 127:879-891.
25. Miosge N., Sasaki T., Timpl R. Angiogenesis inhibitor endostatin is a distinct component of elastic fibers in vessel walls. FASEB J. 1999, 13(13):1743-1750.
26. Mundel P., Shankland S.J. Podocyte biology and response to injury. J. Am. Soc. Nephrol. 2002, 13:3005-3015.
27. Noordeen N.A., Carafoli F., Hohenester E., Horton M.A., Leitinger B. A transmembrane leucine zipper is required for activation of the dimeric receptor tyrosine kinase DDR1. J. Biol. Chem. 11 2006, 281(32):22744-22751.
28. Rao V.H., Meehan D.T., Delimont D., Nakajima M., Wada T., Gratton M.A., Cosgrove D. Role for macrophage metalloelastase in glomerular basement membrane damage associated with alport syndrome. Am. J. Pathol. 2006, 169(1):32-46.
29. Rodewald R., Karnovsky M.J. Porous substructure of the glomerular slit diaphragm in the rat and mouse. J. Cell. Biol. 1974, 60:423-433.
30. Rodgers K.D., Rao V., Meehan D.T., Fager N., Gotwals P., Ryan S.T., Koteliansky V., Nemori R., Cosgrove D. Monocytes may promote myofibroblast accumulation and apoptosis in Alport renal fibrosis. Kidney Int. 2003, 63(4):1338-1355.
31. Ronco P., Chatziantoniou C. Matrix metalloproteinases and matrix receptors in progression and reversal of kidney disease: therapeutic perspectives. Kidney Int. 2008, 74(7):873-878.
32. Saleem M.A., Ni L., Witherden I., Tryggvason K., Ruotsalainen V., Mundel P., Mathieson P.W. Co-localization of nephrin, podocin, and the actin cytoskeleton: evidence for a role in podocyte foot process formation. Am. J. Pathol. 2002, 161:1459-1466.
33. Segerer S., Heller F., Lindenmeyer M.T., Schmid H., Cohen C.D., Draganovici D., Mandelbaum J., Nelson P.J., Gröne H.J., Gröne E.F., Figel A.M., Nössner E., Schlöndorff D. Compartment specific expression of dendritic cell markers in human glomerulonephritis. Kidney Int. 2008, 74:37-46.
34. Vogel W., Brakebusch C., Fässler R., Alves F., Ruggiero F., Pawson T. Discoidin domain receptor 1 is activated independently of beta1 integrin. J. Biol. Chem. 2000, 275(8):5779-5784.
35. Vogel W.F., Abdulhussein R., Ford C.E. Sensing extracellular matrix: an update on discoidin domain receptor function. Cell. Signal. 2006, 18(8):1108-1116.