A Proteome-Derived Longitudinal Pharmacodynamic Biomarker for Diffuse Systemic Sclerosis Skin

Journal of Investigative Dermatology

Volumn 137, Issue 1, 2017, Pages 62-70

  Rice, Lisa M ^a   Mantero, Julio C ^a   Stifano, Giuseppina ^a   Ziemek, Jessica ^a   Simms, Robert W ^a   Gordon, Jessica ^b   Domsic, Robyn ^c   Lafyatis, Robert ^c  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HOSPITAL FOR SPECIAL SURGERY   (United States)

^c UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APTAMER; BIOLOGICAL MARKER; CONNECTIVE TISSUE GROWTH FACTOR; CXCL11 CHEMOKINE; CXCL13 CHEMOKINE; ENDOSTATIN; GAMMA INTERFERON; INTERLEUKIN 13; MESSENGER RNA; PHARMACODYNAMIC BIOMARKER; PLASMA PROTEIN; PROTEIN; PROTEIN ADAM12; PROTEIN FSTL3; PROTEIN P53; PROTEIN SERPINE1; PROTEIN ST2; PROTEOME; SMAD3 PROTEIN; SMAD4 PROTEIN; SOMATOMEDIN BINDING PROTEIN 2; SPONDIN 1; TENASCIN; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; TRANSCRIPTION FACTOR FKHRL1; TRANSCRIPTION FACTOR RUNX2; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR RECEPTOR 1; UNCLASSIFIED DRUG; CYTOKINE;

ADULT; AGED; ARTICLE; COHORT ANALYSIS; CONTROLLED STUDY; CYTOKINE RELEASE; DISEASE SEVERITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; LONGITUDINAL STUDY; MAJOR CLINICAL STUDY; MALE; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN EXPRESSION ASSAY; SKIN BIOPSY; SOMASCAN APTAMER TECHNOLOGY; SYSTEMIC SCLEROSIS; VALIDATION STUDY; BLOOD; CASE CONTROL STUDY; METABOLISM; MIDDLE AGED; PATHOPHYSIOLOGY; PHARMACOGENETIC TESTING; REPRODUCIBILITY; SCLERODERMA, DIFFUSE; SEVERITY OF ILLNESS INDEX; STATISTICAL MODEL;

ADULT; BIOMARKERS; CASE-CONTROL STUDIES; CYTOKINES; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMANS; LINEAR MODELS; LONGITUDINAL STUDIES; MALE; MIDDLE AGED; PHARMACOGENOMIC TESTING; PROTEOME; REPRODUCIBILITY OF RESULTS; SCLERODERMA, DIFFUSE; SEVERITY OF ILLNESS INDEX;

EID: 85006835206     PISSN: 0022202X     EISSN: 15231747     Source Type: Journal    
DOI: 10.1016/j.jid.2016.08.027     Document Type: Article

References (46)

1. Assassi, S., Swindell, W.R., Wu, M., Tan, F.D., Khanna, D., Furst, D.E., et al. Dissecting the heterogeneity of skin gene expression patterns in systemic sclerosis. Arthritis Rheumatol 67 (2015), 3016–3026.
2. Attur, M.G., Palmer, G.D., Al-Mussawir, H.E., Dave, M., Teixeira, C.C., Rifkin, D.B., et al. F-spondin, a neuroregulatory protein, is up-regulated in osteoarthritis and regulates cartilage metabolism via TGF-beta activation. FASEB J 23 (2009), 79–89.
3. Beirne, P., Pantelidis, P., Charles, P., Wells, A.U., Abraham, D.J., Denton, C.P., et al. Multiplex immune serum biomarker profiling in sarcoidosis and systemic sclerosis. Eur Respir J 34 (2009), 1376–1382.
4. Cordenonsi, M., Dupont, S., Maretto, S., Insinga, A., Imbriano, C., Piccolo, S., Links between tumor suppressors: p53 is required for TGF-beta gene responses by cooperating with Smads. Cell 113 (2003), 301–314.
5. Denton, C.P., Merkel, P.A., Furst, D.E., Khanna, D., Emery, P., Hsu, V.M., et al. Recombinant human anti-transforming growth factor beta1 antibody therapy in systemic sclerosis: a multicenter, randomized, placebo-controlled phase I/II trial of CAT-192. Arthritis Rheum 56 (2007), 323–333.
6. Doran, J.P., Veale, D.J., Biomarkers in systemic sclerosis. Rheumatology(47 Suppl. 5), 2008 v36–8.
7. Dupont, S., Zacchigna, L., Adorno, M., Soligo, S., Volpin, D., Piccolo, S., et al. Convergence of p53 and TGF-beta signaling networks. Cancer Lett 213 (2004), 129–138.
8. Dziadzio, M., Smith, R.E., Abraham, D.J., Black, C.M., Denton, C.P., Circulating levels of active transforming growth factor beta1 are reduced in diffuse cutaneous systemic sclerosis and correlate inversely with the modified Rodnan skin score. Rheumatology 44 (2005), 1518–1524.
9. Farina, G.A., York, M.R., Di Marzio, M., Collins, C.A., Meller, S., Homey, B., et al. Poly(I: C) drives type I IFN- and TGFbeta-mediated inflammation and dermal fibrosis simulating altered gene expression in systemic sclerosis. J Invest Dermatol 130 (2010), 2583–2593.
10. Friedman, J.H., Hastie, T., Tibshirani, R., Regularization paths for feneralized linear models via coordinate descent. J Stat Softw 33 (2010), 1–22.
11. Gold, L., Ayers, D., Bertino, J., Bock, C., Bock, A., Brody, E.N., et al. Aptamer-based multiplexed proteomic technology for biomarker discovery. PLoS One, 5, 2010, e15004.
12. Greenblatt, M.B., Aliprantis, A.O., The immune pathogenesis of scleroderma: context is everything. Curr Rheumatol Rep, 15, 2013, 297.
13. Guo, X., Higgs, B.W., Bay-Jensen, A.C., Karsdal, M.A., Yao, Y., Roskos, L.K., et al. Suppression of T cell activation and collagen accumulation by an Anti-IFNAR1 mAb, anifrolumab, in adult patients with systemic sclerosis. J Invest Dermatol 135 (2015), 2402–2409.
14. Hayakawa, H., Hayakawa, M., Kume, A., Tominaga, S., Soluble ST2 blocks interleukin-33 signaling in allergic airway inflammation. J Biol Chem 282 (2007), 26369–26380.
15. Hesselstrand, R., Kassner, A., Heinegard, D., Saxne, T., COMP: a candidate molecule in the pathogenesis of systemic sclerosis with a potential as a disease marker. Ann Rheum Dis 67 (2008), 1242–1248.
16. Krijthe J. Rtsne: T-distributed stochastic neighbor embedding using Barnes-Hut implementation. R package version 0.10, https://mran.microsoft.com/package/Rtsne/; 2015 (accessed July 2016).
17. Lafyatis, R., Application of biomarkers to clinical trials in systemic sclerosis. Curr Rheumatol Rep 14 (2012), 47–55.
18. Langfelder, P., Horvath, S., WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics, 9, 2008, 559.
19. Langfelder, P., Horvath, S., Fast R functions for robust correlations and hierarchical clustering. J Stat Softw, 46(11), 2012.
20. MacDonald, K.G., Dawson, N.A., Huang, Q., Dunne, J.V., Levings, M.K., Broady, R., Regulatory T cells produce profibrotic cytokines in the skin of patients with systemic sclerosis. J Allergy Clin Immunol, 135, 2015 946–e9.
21. Manetti, M., Ibba-Manneschi, L., Liakouli, V., Guiducci, S., Milia, A.F., Benelli, G., et al. The IL1-like cytokine IL33 and its receptor ST2 are abnormally expressed in the affected skin and visceral organs of patients with systemic sclerosis. Ann Rheum Dis 69 (2010), 598–605.
22. Mathes, A.L., Christmann, R.B., Stifano, G., Affandi, A.J., Radstake, T.R., Farina, G.A., et al. Global chemokine expression in systemic sclerosis (SSc): CCL19 expression correlates with vascular inflammation in SSc skin. Ann Rheum Dis 73 (2014), 1864–1872.
23. Milano, A., Pendergrass, S.A., Sargent, J.L., George, L.K., McCalmont, T.H., Connolly, M.K., et al. Molecular subsets in the gene expression signatures of scleroderma skin. PLoS One, 3, 2008, e2696.
24. Moinzadeh, P., Denton, C.P., Abraham, D., Ong, V., Hunzelmann, N., Eckes, B., et al. Biomarkers for skin involvement and fibrotic activity in scleroderma. J Eur Acad Dermatol Venereol 26 (2012), 267–276.
25. O'Reilly, S., Hugle, T., van Laar, J.M., T cells in systemic sclerosis: a reappraisal. Rheumatology 51 (2012), 1540–1549.
26. Palmer, G.D., Attur, M.G., Yang, Q., Liu, J., Moon, P., Beier, F., et al. F-spondin deficient mice have a high bone mass phenotype. PLoS One, 9, 2014, e98388.
27. Pendergrass, S.A., Lemaire, R., Francis, I.P., Mahoney, J.M., Lafyatis, R., Whitfield, M.L., Intrinsic gene expression subsets of diffuse cutaneous systemic sclerosis are stable in serial skin biopsies. J Invest Dermatol 132 (2012), 1363–1373.
28. Quillinan, N.P., McIntosh, D., Vernes, J., Haq, S., Denton, C.P., Treatment of diffuse systemic sclerosis with hyperimmune caprine serum (AIMSPRO): a phase II double-blind placebo-controlled trial. Ann Rheum Dis 73 (2014), 56–61.
29. RStudio Team. RStudio: integrated development for R. 2015, RStudio, Inc., Boston, MA http://www.rstudio.com/.
30. Rice, L.M., Padilla, C.M., McLaughlin, S.R., Mathes, A., Ziemek, J., Goummih, S., et al. Fresolimumab treatment decreases biomarkers and improves clinical symptoms in systemic sclerosis patients. J Clin Invest 125 (2015), 2795–2807.
31. Rice, L.M., Ziemek, J., Stratton, E.A., McLaughlin, S.R., Padilla, C.M., Mathes, A.L., et al. A longitudinal biomarker for the extent of skin disease in patients with diffuse cutaneous systemic sclerosis. Arthritis Rheumatol 67 (2015), 3004–3015.
32. Samarakoon, R., Overstreet, J.M., Higgins, S.P., Higgins, P.J., TGF-beta1 → SMAD/p53/USF2 → PAI-1 transcriptional axis in ureteral obstruction-induced renal fibrosis. Cell Tissue Res 347 (2012), 117–128.
33. Sato, S., Hasegawa, M., Takehara, K., Serum levels of interleukin-6 and interleukin-10 correlate with total skin thickness score in patients with systemic sclerosis. J Dermatol Sci 27 (2001), 140–146.
34. Schelldorfer, J., Meier, L., Bühlmann, P., GLMMLasso: An algorithm for high-dimensional generalized linear mixed models using L1-penalization. J Comput Graph Stat 23 (2014), 460–477.
35. Schiering, C., Krausgruber, T., Chomka, A., Frohlich, A., Adelmann, K., Wohlfert, E.A., et al. The alarmin IL-33 promotes regulatory T-cell function in the intestine. Nature 513 (2014), 564–568.
36. Steen, V.D., Autoantibodies in systemic sclerosis. Semin Arthritis Rheum 35 (2005), 35–42.
37. Takebayashi-Suzuki, K., Funami, J., Tokumori, D., Saito, A., Watabe, T., Miyazono, K., et al. Interplay between the tumor suppressor p53 and TGF beta signaling shapes embryonic body axes in Xenopus. Development 130 (2003), 3929–3939.
38. Team RC. R: a language and environment for statistical computing. 2016.
39. Tisbshirani, R., Regression shrinkage and selection via the lasso. J Royal Stat Soc 58 (1996), 267–288.
40. van Bon, L., Affandi, A.J., Broen, J., Christmann, R.B., Marijnissen, R.J., Stawski, L., et al. Proteome-wide analysis and CXCL4 as a biomarker in systemic sclerosis. N Engl J Med 370 (2014), 433–443.
41. van Bon, L., Cossu, M., Loof, A., Gohar, F., Wittkowski, H., Vonk, M., et al. Proteomic analysis of plasma identifies the Toll-like receptor agonists S100A8/A9 as a novel possible marker for systemic sclerosis phenotype. Ann Rheum Dis 73 (2014), 1585–1589.
42. Yamaguchi, Y., Ono, J., Masuoka, M., Ohta, S., Izuhara, K., Ikezawa, Z., et al. Serum periostin levels are correlated with progressive skin sclerosis in patients with systemic sclerosis. Br J Dermatol 168 (2013), 717–725.
43. Yanaba, K., Yoshizaki, A., Asano, Y., Kadono, T., Sato, S., Serum IL-33 levels are raised in patients with systemic sclerosis: association with extent of skin sclerosis and severity of pulmonary fibrosis. Clin Rheumatol 30 (2011), 825–830.
44. York, M.R., Nagai, T., Mangini, A.J., Lemaire, R., van Seventer, J.M., Lafyatis, R., A macrophage marker, Siglec-1, is increased on circulating monocytes in patients with systemic sclerosis and induced by type I interferons and toll-like receptor agonists. Arthritis Rheum 56 (2007), 1010–1020.
45. Zhao, Q., Chen, G., Role of IL-33 and its receptor in T cell-mediated autoimmune diseases. Biomed Res Int, 2014, 2014, 587376.
46. Zhu, S., Evans, S., Yan, B., Povsic, T.J., Tapson, V., Goldschmidt-Clermont, P.J., et al. Transcriptional regulation of Bim by FOXO3a and Akt mediates scleroderma serum-induced apoptosis in endothelial progenitor cells. Circulation 118 (2008), 2156–2165.