Circulating bone morphogenetic protein 1-3 isoform increases renal fibrosis

Journal of the American Society of Nephrology

Volumn 22, Issue 4, 2011, Pages 681-692

  Grgurevic, Lovorka ^a   Macek, Boris ^b   Healy, David R ^c   Brault, Amy L ^c   Erjavec, Igor ^a   Cipcic, Antonio ^a   Grgurevic, Ivica ^d   Rogic, Dunja ^e   Galesic, Kresimir ^d   Brkljacic, Jelena ^a   Stern Padovan, Ranka ^e   Paralkar, Vishwas M ^c   Vukicevic, Slobodan ^a  

^a UNIVERSITY OF ZAGREB   (Croatia)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c PFIZER GLOBAL RESEARCH AND DEVELOPMENT   (United States)

^d University of Zagreb School of Medicine   (Croatia)

^e KBC Zagreb   (Croatia)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; BETA1 INTEGRIN; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 6; COLLAGEN TYPE 1; CONNECTIVE TISSUE GROWTH FACTOR; CREATININE; DECORIN; DENTIN MATRIX PROTEIN 1; GROWTH DIFFERENTIATION FACTOR 15; NEUTRALIZING ANTIBODY; OSTEOGENIC PROTEIN 1; OSTEOGENIN; PROCOLLAGEN C PROTEINASE; RECOMBINANT CYTOKINE; TRANSFORMING GROWTH FACTOR BETA1; WNT PROTEIN;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL STRAIN HEK293; CHRONIC KIDNEY DISEASE; CLINICAL ARTICLE; CONTROLLED STUDY; CREATININE BLOOD LEVEL; EMBRYO; FEMALE; FETUS; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HUMAN TISSUE; KIDNEY FIBROSIS; KIDNEY FUNCTION; LIQUID CHROMATOGRAPHY; MALE; MASS SPECTROMETRY; NONHUMAN; PRENATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN CLEAVAGE; PROTEIN LOCALIZATION; RAT; SIGNAL TRANSDUCTION; SURVIVAL RATE; TISSUE DISTRIBUTION;

EID: 79953316844     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2010070722     Document Type: Article

References (63)

1. Vukicevic S, Basic V, Rogic D, Basic N, Shih MS, Shepard A, Jin D, Dattatreyamurty B, Jones W, Dorai H, Ryan S, Griffiths D, Maliakal J, Jelic M, Pastorcic M, Stavljenic A, Sampath TK: Osteogenic protein-1 (bone morphogenetic protein-7) reduces severity of injury after ischemic acute renal failure in rat. J Clin Invest 102: 202-214, 1998 (Pubitemid 28323847)
2. Borovecki F, Basic N, Jelic M, Rogic D, Dorai H, Stavljenic-Rukavina A, Sampath KT, Vukicevic S: The role of bone morphogenetic proteins in kidney development and repair. In: Bone Morphogenetic Proteins: From Laboratory to Clinical Practice, edited by Vukicevic S, Sampath TK, Boston, Birkauser Verlag AG, 2002, pp 263-288
3. Li T, Surendran K, Zawaideh MA, Mathew S, Hruska KA: Bone morphogenetic protein 7: A novel treatment for chronic renal and bone disease. Curr Opin Nephrol Hypertens 13: 417-422, 2004 (Pubitemid 38901621)
4. Breitkopf K, Muller A, Ciuclan L, Wiercinska E, ten Dijke P, Dooley S: Bone morphogenetic protein (BMP)-9: A new member of the TGF-β superfamily is secreted by activated hepatic stelate cells. J Hepatol 50: S110, 2009
5. Vukicevic S, Grgurevic L: BMP-6 and mesenchymal stem cell differentiation. Cytokine Growth Factor Rev 20: 441-448, 2009
6. Grgurevic L: Proteomic identification of bone morphogenetic proteins and related molecules in biological fluids. Ph.D. thesis, Medical School, University of Zagreb, Zagreb, Croatia, 2007
7. Wozney JM, Rosen V, Celeste AJ, Mitsock LM, Whitters MJ, Kriz RW, Hewick RM, Wang EA: Novel regulators of bone formation: Molecular clones and activities. Science 242: 1528-1534, 1988 (Pubitemid 19023695)
8. Pfleiderer G, Zwilling R, Sonneborn HH: On the evolution of endopeptidases, 3. A protease of molecular weight 11,000 and a trypsinlike fraction from Astacus fluviatilis fabr. Hoppe Seylers Z Physiol Chem 348: 1319-1331, 1967
9. Ge G, Greenspan DS: Developmental roles of the BMP1/TLD metalloproteinases. Birth Defects Res C Embryo Today 78: 47-68, 2006 (Pubitemid 43726175)
10. Hopkins DR, Keles S, Greenspan DS: The bone morphogenetic protein 1/Tolloid-like metalloproteinases. Matrix Biol 26: 508-523, 2007 (Pubitemid 47575882)
11. Wolfman NM, McPherron AC, Pappano WN, Davies MV, Song K, Tomkinson KN, Wright JF, Zhao L, Sebald SM, Greenspan DS, Lee SJ: Activation of latent myostatin by the BMP-1/tolloid family of metalloproteinases. Proc Natl Acad Sci U S A 100: 15842-15846, 2003 (Pubitemid 38021077)
12. Ge G, Greenspan DS: BMP1 controls TGFbeta1 activation via cleavage of latent TGFbeta-binding protein. J Cell Biol 175: 111-120, 2006 (Pubitemid 44537203)
13. Suzuki N, Labosky PA, Furuta Y, Hargett L, Dunn R, Fogo AB, Takahara K, Peters DM, Greenspan DS, Hogan BL: Failure of ventral body wall closure in mouse embryos lacking a procollagen C-proteinase encoded by Bmp1, a mammalian gene related to Drosophila tolloid. Development 122: 3587-3595, 1996 (Pubitemid 26396000)
14. Garrigue-Antar L, Barker C, Kadler KE: Identification of amino acid residues in bone morphogenetic protein-1 important for procollagen C-proteinase activity. J Biol Chem 276: 26237-26242, 2001
15. Vukicevic S, Grgurevic L, Macek B: BMP-1 procollagen C-proteinase for diagnosis and treatment of bone and soft tissue defects and disorders. USPTO No. 7850964
16. Simic P, Culej JB, Orlic I, Grgurevic L, Draca N, Spaventi R, Vukicevic S: Systemically administered bone morphogenetic protein-6 restores bone in aged ovariectomized rats by increasing bone formation and suppressing bone resorption. J Biol Chem 281: 25509-25521, 2006 (Pubitemid 44401940)
17. Buijs JT, Rentsch CA, van der Horst G, van Overveld PG, Wetterwald A, Schwaninger R, Henriquez NV, Ten Dijke P, Borovecki F, Markwalder R, Thalmann GN, Papapoulos SE, Pelger RC, Vukicevic S, Cecchini MG, Löwik CW, van der Pluijm G: BMP7, a putative regulator of epithelial homeostasis in the human prostate, is a potent inhibitor of prostate cancer bone metastasis in vivo. Am J Pathol 171: 1047-1057, 2007 (Pubitemid 47441001)
18. Janitz M, Heiser V, Bottcher U, Landt O, Lauster R: Three alternatively spliced variants of the gene coding for the human bone morphogenetic protein-1. J Mol Med 76: 141-146, 1998 (Pubitemid 28085094)
19. Jasuja R, Ge G, Voss NG, Lyman-Gingerich J, Branam AM, Pelegri FJ, Greenspan DS: Bone morphogenetic protein 1 prodomain specifically binds and regulates signaling by bone morphogenetic proteins 2 and 4. J Biol Chem 282: 9053-9062, 2007 (Pubitemid 47093539)
20. Nguyen TQ, Goldschmeding R: Bone morphogenetic protein-7 and connective tissue growth factor: Novel targets for treatment of renal fibrosis. Pharm Res 25: 2416-2426, 2008
21. Nguyen TQ, Chon H, van Nieuwenhoven FA, Braam B, Verhaar MC, Goldschmeding R: Myofibroblast progenitor cells are increased in number in patients with type 1 diabetes and express less bone morphogenetic protein 6: A novel clue to adverse tissue remodeling. Diabetologia 49: 1039-1048, 2006
22. Liu Y: Renal fibrosis. New insights in pathogenesis and therapeutics. Kidney Int 69: 213-217, 2006
23. Border WA, Okuda S, Languino LR, Sporn MB, Ruoslahti E: Suppression of experimental glomerulonephritis by antiserum against transforming growth factor beta 1. Nature 346: 371-374, 1990
24. Sharma K, Jin Y, Guo J, Ziyadeh FN: Neutralization of TGF-beta by anti-TGF-beta antibody attenuates kidney hypertrophy and the enhanced extracellular matrix gene expression in STZ-induced diabetic mice. Diabetes 45: 522-530, 1996
25. Akagi Y, Isaka Y, Arai M, Kaneko T, Takenaka M, Moriyama T, Kaneda Y, Ando A, Orita Y, Kamada T, Ueda N, Imai E: Inhibition of TGF-beta 1 expression by antisense oligonucleotides suppressed extracellular matrix accumulation in experimental glomerulonephritis. Kidney Int 50: 148-155, 1996 (Pubitemid 26323708)
26. Border WA, Noble NA, Yamamoto T, Harper JR, Yamaguchi Y, Pierschbacher MD, Ruoslahti E: Natural inhibitor of transforming growth factor-beta protects against scarring in experimental kidney disease. Nature 360: 361-364, 1992 (Pubitemid 23000677)
27. Isaka Y, Akagi Y, Ando Y, Tsujie M, Sudo T, Ohno N, Border WA, Noble NA, Kaneda Y, Hori M, Imai E: Gene therapy by transforming growth factor-beta receptor-IgG Fc chimera suppressed extracellular matrix accumulation in experimental glomerulonephritis. Kidney Int 55: 465-475, 1999 (Pubitemid 29082873)
28. Moon JA, Kim HT, Cho IS, Sheen YY, Kim DK: IN-1130, a novel transforming growth factor-beta type I receptor kinase (ALK5) inhibitor, suppresses renal fibrosis in obstructive nephropathy. Kidney Int 70: 1234-1243, 2006 (Pubitemid 44435174)
29. Yamaguchi Y, Mann DM, Ruoslahti E: Negative regulation of transforming growth factor-beta by the proteoglycan decorin. Nature 346: 281-284, 1990
30. Danielson KG, Baribault H, Holmes DF, Graham H, Kadler KE, Iozzo RV: Targeted disruption of decorin leads to abnormal collagen fibril morphology and skin fragility. J Cell Biol 136: 729-743, 1997 (Pubitemid 27083772)
31. Ferdous Z, Wei VM, Iozzo R, Höök M, Grande-Allen KJ: Decorin-transforming growth factor-interaction regulates matrix organization and mechanical characteristics of three-dimensional collagen matrices. J Biol Chem 282: 35887-35898, 2007 (Pubitemid 350277129)
32. Huijun W, Long C, Zhigang Z, Feng J, Muyi G: Ex vivo transfer of the decorin gene into rat glomerulus via a mesangial cell vector suppressed extracellular matrix accumulation in experimental glomerulonephritis. Exp Mol Pathol 78: 17-24, 2005 (Pubitemid 41373312)
33. von Marschall Z, Fisher LW: Decorin is processed by three isoforms of bone morphogenetic protein-1 (BMP1). Biochem Biophys Res Commun 391: 1374-1378, 2010
34. Kagami S, Border WA, Ruoslahti E, Noble NA: Coordinated expression of beta 1 integrins and transforming growth factor-beta-induced matrix proteins in glomerulonephritis. Lab Invest 69: 68-76, 1993 (Pubitemid 23222248)
35. Ruoslahti E, Noble NA, Kagami S, Border WA: Integrins. Kidney Int Suppl 44: S17-S22, 1994 (Pubitemid 24014403)
36. Ständer M, Naumann U, Wick W, Weller M: Transforming growth factor-beta and p-21: Multiple molecular targets of decorin-mediated suppression of neoplastic growth. Cell Tissue Res 296: 221-227, 1999 (Pubitemid 29219174)
37. Schaefer L, Macakova K, Raslik I, Micegova M, Gröne HJ, Schönherr E, Robenek H, Echtermeyer FG, Grässel S, Bruckner P, Schaefer RM, Iozzo RV, Kresse H: Absence of decorin adversely influences tubulointerstitial fibrosis of the obstructed kidney by enhanced apoptosis and increased inflammatory reaction. Am J Pathol 160: 1181-1191, 2002 (Pubitemid 34224603)
38. Goldoni S, Humphries A, Nyström A, Sattar S, Owens RT, McQuillan DJ, Ireton K, Iozzo RV: Decorin is a novel antagonistic ligand of the Met receptor. J Cell Biol 185: 743-754, 2009
39. Yan Q, Sui W, Xie S, Chen H, Xie S, Zou G, Guo J, Zou H: Expression and role of integrin-linked kinase and collagen IV in human renal allografts with interstitial fibrosis and tubular atrophy. Transpl Immunol 23: 1-5, 2010
40. Liu S, Kapoor M, Denton CP, Abraham DJ, Leask A: Loss of peroxisome proliferator-activated receptor gamma in mouse fibroblasts results in increased susceptibility to bleomycin-induced skin fibrosis. Arthritis Rheum 60: 2817-2821, 2009
41. Norman JT, Fine LG: Progressive renal disease: fibroblasts, extracellular matrix, and integrins. Exp Nephrol 7: 167-177, 1999 (Pubitemid 29210179)
42. Gjorevski N, Nelson CM: Bidirectional extracellular matrix signaling during tissue morphogenesis. Cytokine Growth Factor Rev 20: 459-465, 2009
43. Goodwin A, Jenkins G: Role of integrin-mediated TGFbeta activation in the pathogenesis of pulmonary fibrosis. Biochem Soc Trans 37: 849-854, 2009
44. Ortega-Velazquez R, Gonzalez-Rubio M, Ruiz-Torres MP, Diez-Marques ML, Iglesias MC, Rodríguez-Puyol M, Rodríguez-Puyol D: Collagen I upregulates extracellular matrix gene expression and secretion of TGF-beta 1 by cultured human mesangial cells. Am J Physiol Cell Physiol 286: C1335-C1343, 2004 (Pubitemid 38649983)
45. Dorai H, Vukicevic S, Sampath K: Bone morphogenetic protein-7 (osteogenic protein-1) inhibits smooth muscle cell proliferation and stimulates the expression of markers that are characteristic of SMC phenotype in vitro. J Cell Physiol 184: 37-45, 2000 (Pubitemid 30349626)
46. Vukicevic S, Simic P, Grgurevic L, Borovecki F, Sampath TK: Systemic administration of bone morphogenetic proteins. In: Bone Morphogenetic Proteins: From Local to Systemic Therapeutics, edited by Vukicevic S, Sampath TK, Boston, Birkauser Verlag AG, 2008, pp 317-337
47. Helder MN, Ozkaynak E, Sampath KT, Luyten FP, Latin V, Oppermann H, Vukicevic S: Expression pattern of osteogenic protein-1 (bone morphogenetic protein-7) in human and mouse development. J Histochem Cytochem 43: 1035-1044, 1995
48. Simic P, Vukicevic S: Bone morphogenetic proteins in development and homeostasis of kidney. Cytokine Growth Factor Rev 16: 299-308, 2005 (Pubitemid 40910319)
49. Abreu JG, Ketpura NI, Reversade B, De Robertis EM: Connective-tissue growth factor (CTGF) modulates cell signalling by BMP and TGF-beta Nat Cell Biol 4: 599-604, 2002
50. Grgurevic L, Macek B, Durdevic D, Vukicevic S: Detection of bone and cartilage-related proteins in plasma of patients with a bone fracture using liquid chromatography-mass spectrometry. Int Orthop 31: 743-751, 2007 (Pubitemid 350160306)
51. Vukicevic S, Latin V, Chen P, Batorsky R, Reddi AH, Sampath TK: Localization of osteogenic protein-1 (bone morphogenetic protein-7) during human embryonic development: High affinity binding to basement membranes. Biochem Biophys Res Commun 198: 693-700, 1994 (Pubitemid 24178423)
52. Sampath TK, Coughlin JE, Whetstone RM, Banach D, Corbett C, Ridge RJ, Ozkaynak E, Oppermann H, Rueger DC: Bovine osteogenic protein is composed of dimers of OP-1 and BMP-2A, two members of the transforming growth factor-beta superfamily. J Biol Chem 265: 13198-13205, 1990
53. Grgurevic L, Macek B, Erjavec I, Mann M, Vukicevic S: Urine release of systemically administered bone morphogenetic protein hybrid molecule. J Nephrol 20: 311-319, 2007 (Pubitemid 47570361)
54. Moschcovich L, Bernocco S, Font B, Rivkin H, Eichenberger D, Chejanovsky N, Hulmes DJ, Kessler E: Folding and activity of recombinant human procollagen C-proteinase enhancer. Eur J Biochem 268: 2991-2996, 2001 (Pubitemid 32862984)
55. Vukicevic S, Kopp JB, Luyten FP, Sampath TK: Induction of nephrogenic mesenchyme by osteogenic protein 1 (bone morphogenetic protein 7). Proc Natl Acad Sci U S A 93: 9021-9026, 1996 (Pubitemid 26282011)
56. Chang SC, Hoang B, Thomas JT, Vukicevic S, Luyten FP, Ryba NJ, Kozak CA, Reddi AH, Moos M Jr: Cartilage-derived morphogenetic proteins. New members of the transforming growth factor-beta superfamily predominantly expressed in long bones during human embryonic development. J Biol Chem 269: 28227-28234, 1994
57. Vukicevic S, Simic P, Borovecki F, Grgurevic L, Rogic D, Orlic I, Grasser WA, Thompson DD, Paralkar VM: Role of EP2 and EP4 receptor-selective agonists of prostaglandin E(2) in acute and chronic kidney failure. Kidney Int 70: 1099-1106, 2006 (Pubitemid 44344080)
58. Kobayashi K, Luo M, Zhang Y, Wilkes DC, Ge G, Grieskamp T, Yamada C, Liu TC, Huang G, Basson CT, Kispert A, Greenspan DS, Sato TN: Secreted Frizzled-related protein 2 is a procollagen C proteinase enhancer with a role in fibrosis associated with myocardial infarction. Nat Cell Biol 11: 46-55, 2009
59. Vukicevic S, Luyten FP, Reddi AH: Stimulation of the expression of osteogenic and chondrogenic phenotypes in vitro by osteogenin. Proc Natl Acad Sci U S A 86: 8793-8797, 1989 (Pubitemid 20010311)
60. Gansevoort RT, de Jong PE: Challenges for the present CKD classification system. Curr Opin Nephrol Hypertens 19: 308-314, 2010
61. Inman GJ, Herrera B: A rapid and sensitive bioassay for the simultaneous measurement of multiple bone morphogenetic proteins. Identification and quantification of BMP4, BMP6 and BMP9 in bovine and human serum. BMC Cell Biology 10: 20, 2009
62. Pfaffl MW: A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acid Research 29: 45, 2001
63. Sigmond J, Kroep JR, Loves W, Codacci-Pisanelli G, Peters GJ: Quantitative real time PCR of deoxycytidine kinase mRNA by Light Cycler PCR in relation to enzyme activity and gemcitabine sensitivity. Cancer Lett 213: 173-179, 2004 (Pubitemid 39140975)