Losartan ameliorates dystrophic epidermolysis bullosa and uncovers new disease mechanisms

EMBO Molecular Medicine

Volumn 7, Issue 9, 2015, Pages 1211-1228

  Nyström, Alexander ^a   Thriene, Kerstin ^a,b   Mittapalli, Venugopal ^a   Kern, Johannes S ^a   Kiritsi, Dimitra ^a   Dengjel, Jörn ^a,b   Bruckner Tuderman, Leena ^a,b  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Collagen VII; Dystrophic epidermolysis bullosa; Fibrosis; Losartan; TGF

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; COMPLEMENT COMPONENT C7; FIBRONECTIN; INTERLEUKIN 6; LOSARTAN; MESSENGER RNA; SMAD2 PROTEIN; SMAD3 PROTEIN; TENASCIN; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; IMMUNOLOGIC FACTOR; PROTEOME;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHRONIC DRUG ADMINISTRATION; CONTROLLED STUDY; ELASTIC FIBER; EPIDERMOLYSIS BULLOSA DYSTROPHICA; FEMALE; FOREFOOT; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; INFLAMMATORY INFILTRATE; JOINT CONTRACTURE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEOMICS; SKIN FIBROBLAST; SKIN FIBROSIS; ANIMAL; ANTAGONISTS AND INHIBITORS; DISEASE MODEL; INFLAMMATION; PATHOLOGY; TREATMENT OUTCOME;

ANIMALS; DISEASE MODELS, ANIMAL; EPIDERMOLYSIS BULLOSA DYSTROPHICA; IMMUNOLOGIC FACTORS; INFLAMMATION; LOSARTAN; MICE; PROTEOME; TRANSFORMING GROWTH FACTOR BETA; TREATMENT OUTCOME;

EID: 84940789515     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.15252/emmm.201505061     Document Type: Article

References (63)

1. Akhurst RJ, Hata A (2012) Targeting the TGFbeta signalling pathway in disease. Nat Rev Drug Discovery 11: 790-811
2. Bruckner-Tuderman L (2010) Dystrophic epidermolysis bullosa: pathogenesis and clinical features. Dermatol Clin 28: 107-114
3. Campistol JM, Inigo P, Jimenez W, Lario S, Clesca PH, Oppenheimer F, Rivera F (1999) Losartan decreases plasma levels of TGF-beta1 in transplant patients with chronic allograft nephropathy. Kidney Int 56: 714-719
4. Chung HJ, Uitto J (2010) Type VII collagen: the anchoring fibril protein at fault in dystrophic epidermolysis bullosa. Dermatol Clin 28: 93-105
5. Colmenero J, Bataller R, Sancho-Bru P, Dominguez M, Moreno M, Forns X, Bruguera M, Arroyo V, Brenner DA, Gines P (2009) Effects of losartan on hepatic expression of nonphagocytic NADPH oxidase and fibrogenic genes in patients with chronic hepatitis C. Am J Physiol Gastrointest Liver Physiol 297: G726-G734
6. Cook JR, Carta L, Benard L, Chemaly ER, Chiu E, Rao SK, Hampton TG, Yurchenco P, Gen TACRC, Costa KD et al (2014) Abnormal muscle mechanosignaling triggers cardiomyopathy in mice with Marfan syndrome. J Clin Invest 124: 1329-1339
7. Cox J, Mann M (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol 26: 1367-1372
8. Cox J, Neuhauser N, Michalski A, Scheltema RA, Olsen JV, Mann M (2011) Andromeda: a peptide search engine integrated into the MaxQuant environment. J Proteome Res 10: 1794-1805
9. Davila-Seijo P, Hernandez-Martin A, Morcillo-Makow E, Rajan C, Garcia-Doval I (2014) Current dystrophic epidermolysis bullosa research does not match research needs perceived by patients and clinicians. J Am Acad Dermatol 71: 1008-1011
10. Dietz HC (2010) TGF-beta in the pathogenesis and prevention of disease: a matter of aneurysmic proportions. J Clin Invest 120: 403-407
11. Fine JD, Bruckner-Tuderman L, Eady RA, Bauer EA, Bauer JW, Has C, Heagerty A, Hintner H, Hovnanian A, Jonkman MF et al (2014) Inherited epidermolysis bullosa: updated recommendations on diagnosis and classification. J Am Acad Dermatol 70: 1103-1126
12. Fine JD, Johnson LB, Weiner M, Li KP, Suchindran C (2009) Epidermolysis bullosa and the risk of life-threatening cancers: the National EB Registry experience, 1986-2006. J Am Acad Dermatol 60: 203-211
13. Fritsch A, Loeckermann S, Kern JS, Braun A, Bosl MR, Bley TA, Schumann H, von Elverfeldt D, Paul D, Erlacher M et al (2008) A hypomorphic mouse model of dystrophic epidermolysis bullosa reveals mechanisms of disease and response to fibroblast therapy. J Clin Invest 118: 1669-1679
14. Gay-Jordi G, Guash E, Benito B, Brugada J, Nattel S, Mont L, Serrano-Mollar A (2013) Losartan prevents heart fibrosis induced by long-term intensive exercise in an animal model. PLoS ONE 8: e55427
15. Grafe I, Yang T, Alexander S, Homan EP, Lietman C, Jiang MM, Bertin T, Munivez E, Chen Y, Dawson B et al (2014) Excessive transforming growth factor-beta signaling is a common mechanism in osteogenesis imperfecta. Nat Med 20: 670-675
16. Gubinelli E, Angelo C, Pacifico V (2010) A case of dystrophic epidermolysis bullosa improved with etanercept for concomitant psoriatic arthritis. Am J Clin Dermatol 11(Suppl 1): 53-54
17. Habashi JP, Doyle JJ, Holm TM, Aziz H, Schoenhoff F, Bedja D, Chen Y, Modiri AN, Judge DP, Dietz HC (2011) Angiotensin II type 2 receptor signaling attenuates aortic aneurysm in mice through ERK antagonism. Science 332: 361-365
18. Habashi JP, Judge DP, Holm TM, Cohn RD, Loeys BL, Cooper TK, Myers L, Klein EC, Liu G, Calvi C et al (2006) Losartan, an AT1 antagonist, prevents aortic aneurysm in a mouse model of Marfan syndrome. Science 312: 117-121
19. Henderson NC, Sethi T (2009) The regulation of inflammation by galectin-3. Immunol Rev 230: 160-171
20. Hinz B (2009) Tissue stiffness, latent TGF-beta1 activation, and mechanical signal transduction: implications for the pathogenesis and treatment of fibrosis. Curr Rheumatol Rep 11: 120-126
21. Hoste E, Arwert EN, Lal R, South AP, Salas-Alanis JC, Murrell DF, Donati G, Watt FM (2015) Innate sensing of microbial products promotes wound-induced skin cancer. Nat Commun 6: 5932
22. Hsu CK, Wang SP, Lee JY, McGrath JA (2014) Treatment of hereditary epidermolysis bullosa: updates and future prospects. Am J Clin Dermatol 15: 1-6
23. Isaka Y, Brees DK, Ikegaya K, Kaneda Y, Imai E, Noble NA, Border WA (1996) Gene therapy by skeletal muscle expression of decorin prevents fibrotic disease in rat kidney. Nat Med 2: 418-423
24. Jang YC, Tsou R, Gibran NS, Isik FF (2000) Vitronectin deficiency is associated with increased wound fibrinolysis and decreased microvascular angiogenesis in mice. Surgery 127: 696-704
25. Kanno Y, Kuroki A, Okada K, Tomogane K, Ueshima S, Matsuo O, Matsuno H (2007) Alpha2-antiplasmin is involved in the production of transforming growth factor beta1 and fibrosis. J Thromb Haemost 5: 2266-2273
26. Kim JS, Kim JG, Moon MY, Jeon CY, Won HY, Kim HJ, Jeon YJ, Seo JY, Kim JI, Kim J et al (2006) Transforming growth factor-beta1 regulates macrophage migration via RhoA. Blood 108: 1821-1829
27. Kojima T, Miyaishi O, Saga S, Ishiguro N, Tsutsui Y, Iwata H (1998) The retention of abnormal type I procollagen and correlated expression of HSP 47 in fibroblasts from a patient with lethal osteogenesis imperfecta. J Pathol 184: 212-218
28. Koukoulis GK, Shen J, Virtanen I, Gould VE (2001) Vitronectin in the cirrhotic liver: an immunomarker of mature fibrosis. Hum Pathol 32: 1356-1362
29. Kuttner V, Mack C, Rigbolt KT, Kern JS, Schilling O, Busch H, Bruckner-Tuderman L, Dengjel J (2013) Global remodelling of cellular microenvironment due to loss of collagen VII. Mol Syst Biol 9: 657
30. Lacro RV, Dietz HC, Sleeper LA, Yetman AT, Bradley TJ, Colan SD, Pearson GD, Selamet Tierney ES, Levine JC, Atz AM et al (2014) Atenolol versus losartan in children and young adults with Marfan's syndrome. N Engl J Med 371: 2061-2071
31. Leask A, Abraham DJ (2004) TGF-beta signaling and the fibrotic response. FASEB J 18: 816-827
32. Lee S, Solow-Cordero DE, Kessler E, Takahara K, Greenspan DS (1997) Transforming growth factor-beta regulation of bone morphogenetic protein-1/procollagen C-proteinase and related proteins in fibrogenic cells and keratinocytes. J Biol Chem 272: 19059-19066
33. Lim DS, Lutucuta S, Bachireddy P, Youker K, Evans A, Entman M, Roberts R, Marian AJ (2001) Angiotensin II blockade reverses myocardial fibrosis in a transgenic mouse model of human hypertrophic cardiomyopathy. Circulation 103: 789-791
34. Lisse TS, Thiele F, Fuchs H, Hans W, Przemeck GK, Abe K, Rathkolb B, Quintanilla-Martinez L, Hoelzlwimmer G, Helfrich M et al (2008) ER stress-mediated apoptosis in a new mouse model of osteogenesis imperfecta. PLoS Genet 4: e7
35. Loeys BL (2015) Angiotensin receptor blockers: a panacea for Marfan syndrome and related disorders? Drug Discov Today 20: 262-266
36. Montaldo C, Mattei S, Baiocchini A, Rotiroti N, Del Nonno F, Pucillo LP, Cozzolino AM, Battistelli C, Amicone L, Ippolito G et al (2014) Spike-in SILAC proteomic approach reveals the vitronectin as an early molecular signature of liver fibrosis in hepatitis C infections with hepatic iron overload. Proteomics 14: 1107-1115
37. Murphy-Ullrich JE, Poczatek M (2000) Activation of latent TGF-beta by thrombospondin-1: mechanisms and physiology. Cytokine Growth Factor Rev 11: 59-69
38. Naito T, Masaki T, Nikolic-Paterson DJ, Tanji C, Yorioka N, Kohno N (2004) Angiotensin II induces thrombospondin-1 production in human mesangial cells via p38 MAPK and JNK: a mechanism for activation of latent TGF-beta1. Am J Physiol Renal Physiol 286: F278-F287
39. Ng YZ, Pourreyron C, Salas-Alanis JC, Dayal JH, Cepeda-Valdes R, Yan W, Wright S, Chen M, Fine JD, Hogg FJ et al (2012) Fibroblast-derived dermal matrix drives development of aggressive cutaneous squamous cell carcinoma in patients with recessive dystrophic epidermolysis bullosa. Cancer Res 72: 3522-3534
40. Nystrom A, Velati D, Mittapalli VR, Fritsch A, Kern JS, Bruckner-Tuderman L (2013) Collagen VII plays a dual role in wound healing. J Clin Invest 123: 3498-3509
41. Odorisio T, Di Salvio M, Orecchia A, Di Zenzo G, Piccinni E, Cianfarani F, Travaglione A, Uva P, Bellei B, Conti A et al (2014) Monozygotic twins discordant for recessive dystrophic epidermolysis bullosa phenotype highlight the role of TGF-beta signalling in modifying disease severity. Hum Mol Genet 23: 3907-3922
42. Pees C, Laccone F, Hagl M, Debrauwer V, Moser E, Michel-Behnke I (2013) Usefulness of losartan on the size of the ascending aorta in an unselected cohort of children, adolescents, and young adults with Marfan syndrome. Am J Cardiol 112: 1477-1483
43. Petrof G, Martinez-Queipo M, Mellerio JE, Kemp P, McGrath JA (2013) Fibroblast cell therapy enhances initial healing in recessive dystrophic epidermolysis bullosa wounds: results of a randomized, vehicle-controlled trial. Br J Dermatol 169: 1025-1033
44. Radosavljevic G, Volarevic V, Jovanovic I, Milovanovic M, Pejnovic N, Arsenijevic N, Hsu DK, Lukic ML (2012) The roles of Galectin-3 in autoimmunity and tumor progression. Immunol Res 52: 100-110
45. Ramirez F, Rifkin DB (2012) Is losartan the drug for all seasons? Curr Opin Pharmacol 12: 223-224
46. Rappsilber J, Mann M, Ishihama Y (2007) Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nat Protoc 2: 1896-1906
47. Seiffert D (1997) Constitutive and regulated expression of vitronectin. Histol Histopathol 12: 787-797
48. Seiffert D, Curriden SA, Jenne D, Binder BR, Loskutoff DJ (1996) Differential regulation of vitronectin in mice and humans in vitro. J Biol Chem 271: 5474-5480
49. Shevchenko A, Tomas H, Havlis J, Olsen JV, Mann M (2006) In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc 1: 2856-2860
50. Sprenger A, Kuttner V, Bruckner-Tuderman L, Dengjel J (2013) Global proteome analyses of SILAC-labeled skin cells. Methods Mol Biol 961: 179-191
51. Sun D, Kar S, Carr BI (1995) Differentially expressed genes in TGF-beta 1 sensitive and resistant human hepatoma cells. Cancer Lett 89: 73-79
52. Szklarczyk D, Franceschini A, Wyder S, Forslund K, Heller D, Huerta-Cepas J, Simonovic M, Roth A, Santos A, Tsafou KP et al (2015) STRING v10: protein-protein interaction networks, integrated over the tree of life. Nucleic Acids Res 43: D447-D452
53. Terui Y, Saito T, Watanabe H, Togashi H, Kawata S, Kamada Y, Sakuta S (2002) Effect of angiotensin receptor antagonist on liver fibrosis in early stages of chronic hepatitis C. Hepatology 36: 1022
54. Tsuruta Y, Park YJ, Siegal GP, Liu G, Abraham E (2007) Involvement of vitronectin in lipopolysaccaride-induced acute lung injury. J Immunol 179: 7079-7086
55. Uzel MI, Scott IC, Babakhanlou-Chase H, Palamakumbura AH, Pappano WN, Hong HH, Greenspan DS, Trackman PC (2001) Multiple bone morphogenetic protein 1-related mammalian metalloproteinases process pro-lysyl oxidase at the correct physiological site and control lysyl oxidase activation in mouse embryo fibroblast cultures. J Biol Chem 276: 22537-22543
56. Varki R, Sadowski S, Uitto J, Pfendner E (2007) Epidermolysis bullosa. II. Type VII collagen mutations and phenotype-genotype correlations in the dystrophic subtypes. J Med Genet 44: 181-192
57. Venugopal SS, Yan W, Frew JW, Cohn HI, Rhodes LM, Tran K, Melbourne W, Nelson JA, Sturm M, Fogarty J et al (2013) A phase II randomized vehicle-controlled trial of intradermal allogeneic fibroblasts for recessive dystrophic epidermolysis bullosa. J Am Acad Dermatol 69(898-908): e897
58. Wagner JE, Ishida-Yamamoto A, McGrath JA, Hordinsky M, Keene DR, Woodley DT, Chen M, Riddle MJ, Osborn MJ, Lund T et al (2010) Bone marrow transplantation for recessive dystrophic epidermolysis bullosa. N Engl J Med 363: 629-639
59. Wang X, Abraham S, McKenzie JA, Jeffs N, Swire M, Tripathi VB, Luhmann UF, Lange CA, Zhai Z, Arthur HM et al (2013a) LRG1 promotes angiogenesis by modulating endothelial TGF-beta signalling. Nature 499: 306-311
60. Wang X, Ghasri P, Amir M, Hwang B, Hou Y, Khalili M, Lin A, Keene D, Uitto J, Woodley DT et al (2013b) Topical application of recombinant type VII collagen incorporates into the dermal-epidermal junction and promotes wound closure. Mol Ther 21: 1335-1344
61. Wing MG, Seilly DJ, Bridgman DJ, Harrison RA (1993) Rapid isolation and biochemical characterization of rat C1 and C1q. Mol Immunol 30: 433-440
62. Wolf G, Ziyadeh FN, Stahl RA (1999) Angiotensin II stimulates expression of transforming growth factor beta receptor type II in cultured mouse proximal tubular cells. J Mol Med (Berl) 77: 556-564
63. Zarei M, Sprenger A, Gretzmeier C, Dengjel J (2013) Rapid combinatorial ERLIC-SCX solid-phase extraction for in-depth phosphoproteome analysis. J Proteome Res 12: 5989-5995