Pharmacological and genetic depletion of fibrinogen protects from kidney fibrosis

American Journal of Physiology - Renal Physiology

Volumn 307, Issue 4, 2014, Pages

  Craciun, Florin L ^a   Ajay, Amrendra K ^a   Hoffmann, Dana ^a   Saikumar, Janani ^a   Fabian, Steven L ^a   Bijol, Vanesa ^a   Humphreys, Benjamin D ^a   Vaidya, Vishal S ^a,b,c  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Ancrod; Chronic kidney disease; Fibrinogen; Kidney fibrosis

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; ANCROD; BLOOD CLOTTING FACTOR; COLLAGEN TYPE 1; FIBRINOGEN; FIBRINOGEN ALPHA; FIBRINOGEN BETA; FIBRINOGEN GAMMA; INTERLEUKIN 6; SMAD2 PROTEIN; STAT3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; FIBRINOGENOLYSIS; FIBROBLAST; FOLIC ACID NEPHROPATHY; IN VITRO STUDY; IN VIVO STUDY; KIDNEY DISEASE; KIDNEY FIBROSIS; MALE; MOLECULAR INTERACTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; SIGNAL TRANSDUCTION; URETER OBSTRUCTION; URINARY EXCRETION;

ANCROD; CHRONIC KIDNEY DISEASE; FIBRINOGEN; KIDNEY FIBROSIS; TRANSFORMING GROWTH FACTOR-Β1;

ANCROD; ANIMALS; DISEASE PROGRESSION; FIBRINOGEN; FIBROSIS; HEP G2 CELLS; HUMANS; INTERLEUKIN-6; KIDNEY; KIDNEY DISEASES; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; SMAD2 PROTEIN; STAT3 TRANSCRIPTION FACTOR; TRANSFORMING GROWTH FACTOR BETA1; URETERAL OBSTRUCTION;

EID: 84906070120     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00189.2014     Document Type: Article

References (64)

1. Abraham AP, Ma FY, Mulley WR, Ozols E, Nikolic-Paterson DJ. Macrophage infiltration and renal damage are independent of matrix metalloproteinase 12 in the obstructed kidney. Nephrology (Carlton) 17: 322-329, 2012.
2. Ajay AK, Kim TM, Ramirez-Gonzalez V, Park PJ, Frank DA, Vaidya VS. A bioinformatics approach identifies signal transducer and activator of transcription-3 and checkpoint kinase 1 as upstream regulators of kidney injury molecule-1 after kidney injury. J Am Soc Nephrol 25: 105-118, 2014.
3. Ajay AK, Saikumar J, Bijol V, Vaidya VS. Heterozygosity for fibrinogen results in efficient resolution of kidney ischemia reperfusion injury. PLOS ONE 7: e45628, 2012.
4. Akassoglou K, Kombrinck KW, Degen JL, Strickland S. Tissue plasminogen activator-mediated fibrinolysis protects against axonal degeneration and demyelination after sciatic nerve injury. J Cell Biol 149: 1157-1166, 2000.
5. Akassoglou K, Yu WM, Akpinar P, Strickland S. Fibrin inhibits peripheral nerve remyelination by regulating Schwann cell differentiation. Neuron 33: 861-875, 2002.
6. Akhurst RJ, Hata A. Targeting the TGFβ signalling pathway in disease. Nat Rev Drug Discov 11: 790-811, 2012.
7. Ancrod Stroke Study Investigators. Ancrod for the treatment of acute ischemic brain infarction. The Ancrod Stroke Study Investigators. Stroke 25: 1755-1759, 1994.
8. Atkinson JM, Pullen N, Johnson TS. An inhibitor of thrombin activated fibrinolysis inhibitor (TAFI) can reduce extracellular matrix accumulation in an in vitro model of glucose induced ECM expansion. Matrix Biol 32: 277-287, 2013.
9. Baumann H, Isseroff H, Latimer JJ, Jahreis GP. Phorbol ester modulates interleukin 6-and interleukin 1-regulated expression of acute phase plasma proteins in hepatoma cells. J Biol Chem 263: 17390-17396, 1988.
10. Becker GJ, Hewitson TD. Animal models of chronic kidney disease: useful but not perfect. Nephrol Dial Transplant 28: 2432-2438, 2013.
11. Bouissou F, Barthe P, Pierragi M. Severe idiopathic nephrotic syndrome with tubular dysfunction (report of nine pediatric cases). Clin Nephrol 14: 135-176, 1980.
12. Chawla LS, Amdur RL, Amodeo S, Kimmel PL, Palant CE. The severity of acute kidney injury predicts progression to chronic kidney disease. Kidney Int 79: 1361-1369, 2011.
13. Coca SG, Singanamala S, Parikh CR. Chronic kidney disease after acute kidney injury: a systematic review and meta-analysis. Kidney Int 81: 442-448, 2012.
14. Coresh J, Selvin E, Stevens LA, Manzi J, Kusek JW, Eggers P, Van Lente F, Levey AS. Prevalence of chronic kidney disease in the United States. JAMA 298: 2038-2047, 2007.
15. Davalos D, Akassoglou K. Fibrinogen as a key regulator of inflammation in disease. Semin Immunopathol 34: 43-62, 2012.
16. de Giorgio-Miller A, Bottoms S, Laurent G, Carmeliet P, Herrick S. Fibrin-induced skin fibrosis in mice deficient in tissue plasminogen activator. Am J Pathol 167: 721-753, 2005.
17. Docherty NG, Godson C. Fibrinogen as a damage-associated mitogenic signal for the renal fibroblast. Kidney Int 80: 1014-1016, 2011.
18. Doolittle RF. Fibrinogen and fibrin. Annu Rev Biochem 53: 195-229, 1984.
19. Drew A, Tucker H, Liu H, Witte D, Degen J, Tipping P. Crescentic glomerulonephritis is diminished in fibrinogen-deficient mice. Am J Physiol Renal Physiol 281: F1157-F1163, 2001.
20. Eddy AA, Lopez-Guisa JM, Okamura DM, Yamaguchi I. Investigating mechanisms of chronic kidney disease in mouse models. Pediatr Nephrol 27: 1233-1247, 2012.
21. Elger B, Hornberger W, Schwarz M, Seega J. MRI study on delayed ancrod therapy of focal cerebral ischaemia in rats. Eur J Pharmacol 336: 7-14, 1997.
22. Ewart MR, Hatton MW, Basford JM, Dodgson KS. The proteolytic action of Arvin on human fibrinogen. Biochem J 118: 603-609, 1970.
23. Farris AB, Colvin RB. Renal interstitial fibrosis: mechanisms and evaluation. Curr Opin Nephrol Hypertens 21: 289-300, 2012.
24. Floege J, Hackmann B, Kliem V, Kriz W, Alpers C, Johnson R, Kühn K, Koch K, Brunkhorst R. Age-related glomerulosclerosis and interstitial fibrosis in Milan normotensive rats: a podocyte disease. Kidney Int 51: 230-273, 1997.
25. Forbes MS, Thornhill BA, Minor JJ, Gordon KA, Galarreta CI, Chevalier RL. Fight-or-flight: murine unilateral ureteral obstruction causes extensive proximal tubular degeneration, collecting duct dilatation, and minimal fibrosis. Am J Physiol Renal Physiol 303: F120-F129, 2012.
26. Friedman SL, Sheppard D, Duffield JS, Violette S. Therapy for fibrotic diseases: nearing the starting line. Sci Transl Med 5: 167sr1, 2013.
27. Fuller GM, Zhang Z. Transcriptional control mechanism of fibrinogen gene expression. Ann NY Acad Sci 936: 469-479, 2001.
28. Gentle ME, Shi S, Daehn I, Zhang T, Qi H, Yu L, D'Agati VD, Schlondorff DO, Bottinger EP. Epithelial cell TGFβ signaling induces acute tubular injury and interstitial inflammation. J Am Soc Nephrol 24: 787-799, 2013.
29. Giannakis E, Samuel C, Hewitson T, Boon WM, Macris M, Reeve S, Lawrence J, Ian Smith A, Tregear G, Wade J. Aberrant protein expression in plasma and kidney tissue during experimental obstructive nephropathy. Proteomics Clin Appl 3: 1211-1235, 2009.
30. Goldberg R, Dennen P. Long-term outcomes of acute kidney injury. Adv Chronic Kidney Dis 15: 297-307, 2008.
31. Grams ME, Chow EK, Segev DL, Coresh J. Lifetime incidence of CKD stages 3-5 in the United States. Am J Kidney Dis 62: 245-252, 2013.
32. Hattori N, Degen J, Sisson T, Liu H, Moore B, Pandrangi R, Simon R, Drew A. Bleomycin-induced pulmonary fibrosis in fibrinogen-null mice. J Clin Invest 106: 1341-1391, 2000.
33. Hennerici MG, Kay R, Bogousslavsky J, Lenzi GL, Verstraete M, Orgogozo JM. Intravenous ancrod for acute ischaemic stroke in the European Stroke Treatment with Ancrod Trial: a randomised controlled trial. Lancet 368: 1871-1878, 2006.
34. Hoffmann D, Bijol V, Krishnamoorthy A, Gonzalez VR, Frendl G, Zhang Q, Goering PL, Brown RP, Waikar SS, Vaidya VS. Fibrinogen excretion in the urine and immunoreactivity in the kidney serves as a translational biomarker for acute kidney injury. Am J Pathol 181: 818-828, 2012.
35. James MT, Hemmelgarn BR, Wiebe N, Pannu N, Manns BJ, Klarenbach SW, Tonelli M. Glomerular filtration rate, proteinuria, and the incidence and consequences of acute kidney injury: a cohort study. Lancet 376: 2096-2103, 2010.
36. Kant JA, Fornace AJ Jr, Saxe D, Simon MI, McBride OW, Crabtree GR. Evolution and organization of the fibrinogen locus on chromosome 4: gene duplication accompanied by transposition and inversion. Proc Natl Acad Sci USA 82: 2344-2348, 1985.
37. Kim S, Nadel J. Fibrinogen binding to ICAM-1 promotes EGFR-dependent mucin production in human airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 297: L174-L183, 2009.
38. Krishnamoorthy A, Ajay AK, Hoffmann D, Kim TM, Ramirez V, Campanholle G, Bobadilla NA, Waikar SS, Vaidya VS. Fibrinogen β-derived Bβ15-42 peptide protects against kidney ischemia/reperfusion injury. Blood 118: 1934-1942, 2011.
39. Levey AS, Atkins R, Coresh J, Cohen EP, Collins AJ, Eckardt KU, Nahas ME, Jaber BL, Jadoul M, Levin A, Powe NR, Rossert J, Wheeler DC, Lameire N, Eknoyan G. Chronic kidney disease as a global public health problem: approaches and initiatives-a position statement from Kidney Disease Improving Global Outcomes. Kidney Int 72: 247-259, 2007.
40. Levy DE, Trammel J, Wasiewski WW. Ancrod for acute ischemic stroke: a new dosing regimen derived from analysis of prior ancrod stroke studies. J Stroke Cerebrovasc Dis 18: 23-27, 2009.
41. Lopez-Hernandez FJ, Lopez-Novoa JM. Role of TGF-β in chronic kidney disease: an integration of tubular, glomerular and vascular effects. Cell Tissue Res 347: 141-154, 2012.
42. Lopez-Novoa JM, Rodriguez-Pena AB, Ortiz A, Martinez-Salgado C, Lopez Hernandez FJ. Etiopathology of chronic tubular, glomerular and renovascular nephropathies: clinical implications. J Transl Med 9: 13, 2011.
43. Luyendyk JP, Kassel KM, Allen K, Guo GL, Li G, Cantor GH, Copple BL. Fibrinogen deficiency increases liver injury and early growth response-1 (Egr-1) expression in a model of chronic xenobiotic-induced cholestasis. Am J Pathol 178: 1117-1125, 2011.
44. Makino H, Theng L, Kumagai I, Takatori K, Ota Z, Yoshifusa H. [Progressive glomerular sclerosis and renal failure in rat with 7/8 nephrectomy model]. Nihon Jinzo Gakkai Shi 32: 127-163, 1990.
45. Martino MM, Briquez PS, Ranga A, Lutolf MP, Hubbell JA. Heparinbinding domain of fibrin(ogen) binds growth factors and promotes tissue repair when incorporated within a synthetic matrix. Proc Natl Acad Sci USA 110: 4563-4568, 2013.
46. Matsushita K, Ballew SH, Astor BC, Jong PE, Gansevoort RT, Hemmelgarn BR, Levey AS, Levin A, Wen CP, Woodward M, Coresh J; Chronic Kidney Disease Prognosis Consortium. Cohort profile: the Chronic Kidney Disease Prognosis Consortium. Int J Epidemiol 42: 1660-1668, 2013.
47. Meguid El Nahas A, Bello AK. Chronic kidney disease: the global challenge. Lancet 365: 331-340, 2005.
48. Meng XM, Chung AC, Lan HY. Role of the TGF-β/BMP-7/Smad pathways in renal diseases. Clin Sci (Lond) 124: 243-254, 2013.
49. Nagy J, Brasch H, Deák G, Sámik J, Säle T, Trinn C, Burger T. IgA glomerulonephritis: light microscopic and immunohistological studies. Acta Morphol Hung 32: 143-197, 1984.
50. Nguyen MD, Simpson-Haidaris PJ. Cell type-specific regulation of fibrinogen expression in lung epithelial cells by dexamethasone and interleukin-1β. Am J Respir Cell Mol Biol 22: 209-217, 2000.
51. Pang M, Ma L, Gong R, Tolbert E, Mao H, Ponnusamy M, Chin YE, Yan H, Dworkin LD, Zhuang S. A novel STAT3 inhibitor, S3I-201, attenuates renal interstitial fibroblast activation and interstitial fibrosis in obstructive nephropathy. Kidney Int 78: 257-268, 2010.
52. Ruppert C, Markart P, Wygrecka M, Preissner KT, Gunther A. Role of coagulation and fibrinolysis in lung and renal fibrosis. Hamostaseologie 28: 30-32, 34-36, 2008.
53. Schachtrup C, Ryu JK, Helmrick MJ, Vagena E, Galanakis DK, Degen JL, Margolis RU, Akassoglou K. Fibrinogen triggers astrocyte scar formation by promoting the availability of active TGF-β after vascular damage. J Neurosci 30: 5843-5854, 2010.
54. Sherman DG, Atkinson RP, Chippendale T, Levin KA, Ng K, Futrell N, Hsu CY, Levy DE. Intravenous ancrod for treatment of acute ischemic stroke: the STAT study: a randomized controlled trial. Stroke Treatment with Ancrod Trial. JAMA 283: 2395-2403, 2000.
55. Sorensen I, Susnik N, Inhester T, Degen JL, Melk A, Haller H, Schmitt R. Fibrinogen, acting as a mitogen for tubulointerstitial fibroblasts, promotes renal fibrosis. Kidney Int 80: 1035-1044, 2011.
56. Stenvinkel P. Chronic kidney disease: a public health priority and harbinger of premature cardiovascular disease. J Intern Med 268: 456-467, 2010.
57. Suh TT, Holmback K, Jensen NJ, Daugherty CC, Small K, Simon DI, Potter S, Degen JL. Resolution of spontaneous bleeding events but failure of pregnancy in fibrinogen-deficient mice. Genes Dev 9: 2020-2033, 1995.
58. Swenson S, Markland FS Jr. Snake venom fibrin(ogen)olytic enzymes. Toxicon 45: 1021-1039, 2005.
59. Thakar CV, Arrigain S, Worley S, Yared JP, Paganini EP. A clinical score to predict acute renal failure after cardiac surgery. J Am Soc Nephrol 16: 162-168, 2005.
60. Verschuur M, de Jong M, Felida L, de Maat MP, Vos HL. A hepatocyte nuclear factor-3 site in the fibrinogen β promoter is important for interleukin 6-induced expression, and its activity is influenced by the adjacent-148C/T polymorphism. J Biol Chem 280: 16763-16771, 2005.
61. Vidal B, Serrano A, Tjwa M, Suelves M, Ardite E, De Mori R, Baeza-Raja B, Martínez de Lagrán M, Lafuste P, Ruiz-Bonilla V, Jardí M, Gherardi R, Christov C, Dierssen M, Carmeliet P, Degen J, Dewerchin M, Muñoz-Cánoves P. Fibrinogen drives dystrophic muscle fibrosis via a TGFβ/alternative macrophage activation pathway. Genes Dev 22: 1747-1799, 2008.
62. Wang Y, Pratt JR, Hartley B, Evans B, Zhang L, Sacks SH. Expression of tissue type plasminogen activator and type 1 plasminogen activator inhibitor, and persistent fibrin deposition in chronic renal allograft failure. Kidney Int 52: 371-377, 1997.
63. Wynn T. Common and unique mechanisms regulate fibrosis in various fibroproliferative diseases. J Clin Invest 117: 524-533, 2007.
64. Yuan HT, Li XZ, Pitera JE, Long DA, Woolf AS. Peritubular capillary loss after mouse acute nephrotoxicity correlates with down-regulation of vascular endothelial growth factor-A and hypoxia-inducible factor-1α. Am J Pathol 163: 2289-2301, 2003.