TSH-mediated TNFα production in human fibrocytes is inhibited by teprotumumab, an IGF-1R antagonist

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Chen, Hong ^a,b   Shan, Shannon J C ^a   Mester, Tünde ^a   Wei, Yi Hsuan ^a   Douglas, Raymond S ^a,c  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^c VA ANN ARBOR HEALTHCARE SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MESSENGER RNA; PROTEIN KINASE B; SOMATOMEDIN C RECEPTOR; TEPROTUMUMAB; THYROTROPIN; TUMOR NECROSIS FACTOR ALPHA; MONOCLONAL ANTIBODY; R-1507 MONOCLONAL ANTIBODY; TUMOR NECROSIS FACTOR;

ARTICLE; CELL LEVEL; CELLS BY BODY ANATOMY; CONTROLLED STUDY; DISEASE ACTIVITY; DRUG EFFECT; DRUG MECHANISM; ENDOCRINE OPHTHALMOPATHY; FIBROCYTE; GENE EXPRESSION; HUMAN; HUMAN CELL; MOLECULAR DYNAMICS; MOLECULAR PATHOLOGY; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; ANTAGONISTS AND INHIBITORS; CELL CULTURE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; GRAVES OPHTHALMOPATHY; IMMUNOLOGY; METABOLISM; MONOCYTE; STEM CELL;

ANTIBODIES, MONOCLONAL; CELLS, CULTURED; GENE EXPRESSION REGULATION; GRAVES OPHTHALMOPATHY; HUMANS; MONOCYTES; NF-KAPPA B; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR, IGF TYPE 1; RNA, MESSENGER; STEM CELLS; THYROTROPIN; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84939176836     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0130322     Document Type: Article

References (48)

1. Chesney J, Bucala R. Peripheral blood fibrocytes: mesenchymal precursor cells and the pathogenesis of fibrosis. Current rheumatology reports. 2000; 2(6):501-5. PMID: 11123104.
2. Mehrad B, Burdick MD, Zisman DA, Keane MP, Belperio JA, Strieter RM. Circulating peripheral blood fibrocytes in human fibrotic interstitial lung disease. Biochemical and biophysical research communications. 2007; 353(1):104-8. doi: 10.1016/j.bbrc.2006.11.149 PMID: 17174272.
3. Moeller A, Gilpin SE, Ask K, Cox G, Cook D, Gauldie J, et al. Circulating fibrocytes are an indicator of poor prognosis in idiopathic pulmonary fibrosis. American journal of respiratory and critical care medicine. 2009; 179(7):588-94. doi: 10.1164/rccm.200810-1534OC PMID: 19151190.
4. Herzog EL, Bucala R. Fibrocytes in health and disease. Experimental hematology. 2010; 38(7):548-56. doi: 10.1016/j.exphem.2010.03.004 PMID: 20303382; PubMed Central PMCID: PMC3136351.
5. Bucala R, Spiegel LA, Chesney J, Hogan M, Cerami A. Circulating fibrocytes define a new leukocyte subpopulation that mediates tissue repair. Molecular medicine. 1994; 1(1):71-81. PMID: 8790603; PubMed Central PMCID: PMC2229929.
6. Strieter RM, Gomperts BN, Keane MP. The role of CXC chemokines in pulmonary fibrosis. The Journal of clinical investigation. 2007; 117(3):549-56. doi: 10.1172/JCI30562 PMID: 17332882; PubMed Central PMCID: PMC1804376.
7. Phillips RJ, Burdick MD, Hong K, Lutz MA, Murray LA, Xue YY, et al. Circulating fibrocytes traffic to the lungs in response to CXCL12 and mediate fibrosis. The Journal of clinical investigation. 2004; 114(3):438-46. doi: 10.1172/JCI20997 PMID: 15286810; PubMed Central PMCID: PMC484979.
8. Chesney J, Bacher M, Bender A, Bucala R. The peripheral blood fibrocyte is a potent antigen-presenting cell capable of priming naive T cells in situ. Proceedings of the National Academy of Sciences of the United States of America. 1997; 94(12):6307-12. PMID: 9177213; PubMed Central PMCID: PMC21045.
9. Hartlapp I, Abe R, Saeed RW, Peng T, Voelter W, Bucala R, et al. Fibrocytes induce an angiogenic phenotype in cultured endothelial cells and promote angiogenesis in vivo. FASEB journal: official publication of the Federation of American Societies for Experimental Biology. 2001; 15(12):2215-24. doi: 10.1096/fj.01-0049com PMID: 11641248.
10. Bianchetti L, Barczyk M, Cardoso J, Schmidt M, Bellini A, Mattoli S. Extracellular matrix remodelling properties of human fibrocytes. Journal of cellular and molecular medicine. 2012; 16(3):483-95. doi: 10.1111/j.1582-4934.2011.01344.x PMID: 21595824.
11. Abe R, Donnelly SC, Peng T, Bucala R, Metz CN. Peripheral blood fibrocytes: differentiation pathway and migration to wound sites. Journal of immunology. 2001; 166(12):7556-62. PMID: 11390511.
12. Hong KM, Belperio JA, Keane MP, Burdick MD, Strieter RM. Differentiation of human circulating fibrocytes as mediated by transforming growth factor-beta and peroxisome proliferator-activated receptor gamma. The Journal of biological chemistry. 2007; 282(31):22910-20. doi: 10.1074/jbc.M703597200 PMID: 17556364.
13. Schmidt M, Sun G, Stacey MA, Mori L, Mattoli S. Identification of circulating fibrocytes as precursors of bronchial myofibroblasts in asthma. Journal of immunology. 2003; 171(1):380-9. PMID: 12817021.
14. Kisseleva T, Uchinami H, Feirt N, Quintana-Bustamante O, Segovia JC, Schwabe RF, et al. Bone marrow-derived fibrocytes participate in pathogenesis of liver fibrosis. Journal of hepatology. 2006; 45(3):429-38. doi: 10.1016/j.jhep.2006.04.014 PMID: 16846660.
15. Sakai N, Wada T, Yokoyama H, Lipp M, Ueha S, Matsushima K, et al. Secondary lymphoid tissue chemokine (SLC/CCL21)/CCR7 signaling regulates fibrocytes in renal fibrosis. Proceedings of the National Academy of Sciences of the United States of America. 2006; 103(38):14098-103. doi: 10.1073/pnas.0511200103 PMID: 16966615; PubMed Central PMCID: PMC1599918.
16. Haudek SB, Xia Y, Huebener P, Lee JM, Carlson S, Crawford JR, et al. Bone marrow-derived fibroblast precursors mediate ischemic cardiomyopathy in mice. Proceedings of the National Academy of Sciences of the United States of America. 2006; 103(48):18284-9. doi: 10.1073/pnas.0608799103 PMID: 17114286; PubMed Central PMCID: PMC1643845.
17. Zulli A, Buxton BF, Black MJ, Hare DL. CD34 Class III positive cells are present in atherosclerotic plaques of the rabbit model of atherosclerosis. Histochemistry and cell biology. 2005; 124(6):517-22. doi: 10.1007/s00418-005-0072-2 PMID: 16177890.
18. Varcoe RL, Mikhail M, Guiffre AK, Pennings G, Vicaretti M, Hawthorne WJ, et al. The role of the fibrocyte in intimal hyperplasia. Journal of thrombosis and haemostasis: JTH. 2006; 4(5):1125-33. doi: 10.1111/j.1538-7836.2006.01924.x PMID: 16689767.
19. Galligan CL, Fish EN. Circulating fibrocytes contribute to the pathogenesis of collagen antibody-induced arthritis. Arthritis and rheumatism. 2012; 64(11):3583-93. doi: 10.1002/art.34589 PMID: 22729466.
20. Wang J, Jiao H, Stewart TL, Shankowsky HA, Scott PG, Tredget EE. Improvement in postburn hypertrophic scar after treatment with IFN-alpha2b is associated with decreased fibrocytes. Journal of interferon & cytokine research: the official journal of the International Society for Interferon and Cytokine Research. 2007; 27(11):921-30. doi: 10.1089/jir.2007.0008 PMID: 18052725.
21. Yang L, Scott PG, Dodd C, Medina A, Jiao H, Shankowsky HA, et al. Identification of fibrocytes in post-burn hypertrophic scar. Wound repair and regeneration: official publication of the Wound Healing Society [and] the European Tissue Repair Society. 2005; 13(4):398-404. doi: 10.1111/j.1067-1927.2005.130407.x PMID: 16008729.
22. Shan SJ, Douglas RS. The pathophysiology of thyroid eye disease. Journal of neuro-ophthalmology: the official journal of the North American Neuro-Ophthalmology Society. 2014; 34(2):177-85. doi: 10.1097/WNO.0000000000000132 PMID: 24821101.
23. Wang Y, Smith TJ. Current concepts in the molecular pathogenesis of thyroid-associated ophthalmopathy. Investigative ophthalmology & visual science. 2014; 55(3):1735-48. doi: 10.1167/iovs.14-14002 PMID: 24651704; PubMed Central PMCID: PMC3968932.
24. Smith RS, Smith TJ, Blieden TM, Phipps RP. Fibroblasts as sentinel cells. Synthesis of chemokines and regulation of inflammation. The American journal of pathology. 1997; 151(2):317-22. PMID: 9250144; PubMed Central PMCID: PMC1858004.
25. Smith TJ, Tsai CC, Shih MJ, Tsui S, Chen B, Han R, et al. Unique attributes of orbital fibroblasts and global alterations in IGF-1 receptor signaling could explain thyroid-associated ophthalmopathy. Thyroid. 2008; 18(9):983-8. doi: 10.1089/thy.2007.0404 PMID: WOS:000259449900009.
26. Tsui S, Naik V, Hoa N, Hwang CJ, Afifiyan NF, Sinha Hikim A, et al. Evidence for an association between thyroid-stimulating hormone and insulin-like growth factor 1 receptors: a tale of two antigens implicated in Graves' disease. Journal of immunology. 2008; 181(6):4397-405. PMID: 18768899; PubMed Central PMCID: PMC2775538.
27. Tramontano D, Cushing GW, Moses AC, Ingbar SH. Insulin-like growth factor-I stimulates the growth of rat thyroid cells in culture and synergizes the stimulation of DNA synthesis induced by TSH and Graves'-IgG. Endocrinology. 1986; 119(2):940-2. doi: 10.1210/endo-119-2-940 PMID: 2874015.
28. Clement S, Refetoff S, Robaye B, Dumont JE, Schurmans S. Low TSH requirement and goiter in transgenic mice overexpressing IGF-I and IGF-Ir receptor in the thyroid gland. Endocrinology. 2001; 142(12):5131-9. doi: 10.1210/endo.142.12.8534 PMID: 11713206.
29. Kumar S, Iyer S, Bauer H, Coenen M, Bahn RS. A stimulatory thyrotropin receptor antibody enhances hyaluronic acid synthesis in graves' orbital fibroblasts: inhibition by an IGF-I receptor blocking antibody. The Journal of clinical endocrinology and metabolism. 2012; 97(5):1681-7. doi: 10.1210/jc.2011-2890 PMID: 22399503; PubMed Central PMCID: PMC3339886.
30. Gillespie EF, Papageorgiou KI, Fernando R, Raychaudhuri N, Cockerham KP, Charara LK, et al. Increased expression of TSH receptor by fibrocytes in thyroid-associated ophthalmopathy leads to chemokine production. The Journal of clinical endocrinology and metabolism. 2012; 97(5):E740-6. doi: 10.1210/jc.2011-2514 PMID: 22399514; PubMed Central PMCID: PMC3339887.
31. Douglas RS, Afifiyan NF, Hwang CJ, Chong K, Haider U, Richards P, et al. Increased generation of fibrocytes in thyroid-associated ophthalmopathy. The Journal of clinical endocrinology and metabolism. 2010; 95(1):430-8. doi: 10.1210/jc.2009-1614 PMID: 19897675; PubMed Central PMCID: PMC2805489.
32. Smith TJ, Padovani-Claudio DA, Lu Y, Raychaudhuri N, Fernando R, Atkins S, et al. Fibroblasts expressing the thyrotropin receptor overarch thyroid and orbit in Graves' disease. The Journal of clinical endocrinology and metabolism. 2011; 96(12):3827-37. doi: 10.1210/jc.2011-1249 PMID: 21956421; PubMed Central PMCID: PMC3232631.
33. Gianoukakis AG, Khadavi N, Smith TJ. Cytokines, Graves' disease, and thyroid-associated ophthalmopathy. Thyroid. 2008; 18(9):953-8. Epub 2008/08/21. doi: 10.1089/thy.2007.0405 PMID: 18713026; PubMed Central PMCID: PMC2879490.
34. Hiromatsu Y, Yang D, Bednarczuk T, Miyake I, Nonaka K, Inoue Y. Cytokine profiles in eye muscle tissue and orbital fat tissue from patients with thyroid-associated ophthalmopathy. The Journal of clinical endocrinology and metabolism. 2000; 85(3):1194-9. doi: 10.1210/jcem.85.3.6433 PMID: 10720061.
35. Vassalli P. The pathophysiology of tumor necrosis factors. Annual review of immunology. 1992; 10:411-52. doi: 10.1146/annurev.iy.10.040192.002211 PMID: 1590993.
36. Heufelder AE, Bahn RS. Detection and localization of cytokine immunoreactivity in retro-ocular connective tissue in Graves' ophthalmopathy. European journal of clinical investigation. 1993; 23(1):10-7. PMID: 8444271.
37. Durrani OM, Reuser TQ, Murray PI. Infliximab: a novel treatment for sight-threatening thyroid associated ophthalmopathy. Orbit. 2005; 24(2):117-9. doi: 10.1080/01676830590912562 PMID: 16191800.
38. Paridaens D, van den Bosch WA, van der Loos TL, Krenning EP, van Hagen PM. The effect of etanercept on Graves' ophthalmopathy: a pilot study. Eye. 2005; 19(12):1286-9. doi: 10.1038/sj.eye.6701768 PMID: 15550932.
39. Prummel MF, Mourits MP, Berghout A, Krenning EP, van der Gaag R, Koornneef L, et al. Prednisone and cyclosporine in the treatment of severe Graves' ophthalmopathy. The New England journal of medicine. 1989; 321(20):1353-9. doi: 10.1056/NEJM198911163212002 PMID: 2519530.
40. Ayabe R, Rootman DB, Hwang CJ, Ben-Artzi A, Goldberg R. Adalimumab as steroid-sparing treatment of inflammatory-stage thyroid eye disease. Ophthalmic plastic and reconstructive surgery. 2014; 30(5):415-9. doi: 10.1097/IOP.0000000000000211 PMID: 24978425.
41. Raychaudhuri N, Fernando R, Smith TJ. Thyrotropin regulates IL-6 expression in CD34+ fibrocytes: clear delineation of its cAMP-independent actions. PloS one. 2013; 8(9):e75100. doi: 10.1371/journal.pone.0075100 PMID: 24086448; PubMed Central PMCID: PMC3783445.
42. Li B, Smith TJ. PI3K/AKT pathway mediates induction of IL-1RA by TSH in fibrocytes: modulation by PTEN. The Journal of clinical endocrinology and metabolism. 2014; 99(9):3363-72. doi: 10.1210/jc.2014-1257 PMID: 24840811; PubMed Central PMCID: PMC4154109.
43. Chen H, Mester T, Raychaudhuri N, Kauh CY, Gupta S, Smith TJ, et al. Teprotumumab, an IGF-1R blocking monoclonal antibody inhibits TSH and IGF-1 action in fibrocytes. The Journal of clinical endocrinology and metabolism. 2014; 99(9):E1635-40. doi: 10.1210/jc.2014-1580 PMID: 24878056; PubMed Central PMCID: PMC4154099.
44. Gillespie EF, Raychaudhuri N, Papageorgiou KI, Atkins SJ, Lu Y, Charara LK, et al. Interleukin-6 production in CD40-engaged fibrocytes in thyroid-associated ophthalmopathy: involvement of Akt and NF-kappaB. Investigative ophthalmology & visual science. 2012; 53(12):7746-53. doi: 10.1167/iovs.12-9861 PMID: 23092922; PubMed Central PMCID: PMC3506052.
45. MacNaul KL, Hutchinson NI, Parsons JN, Bayne EK, Tocci MJ. Analysis of IL-1 and TNF-alpha gene expression in human rheumatoid synoviocytes and normal monocytes by in situ hybridization. Journal of immunology. 1990; 145(12):4154-66. PMID: 2258613.
46. Brennan FM, Chantry D, Jackson A, Maini R, Feldmann M. Inhibitory effect of TNF alpha antibodies on synovial cell interleukin-1 production in rheumatoid arthritis. Lancet. 1989; 2(8657):244-7. PMID: 2569055.
47. Terrando N, Monaco C, Ma D, Foxwell BM, Feldmann M, Maze M. Tumor necrosis factor-alpha triggers a cytokine cascade yielding postoperative cognitive decline. Proceedings of the National Academy of Sciences of the United States of America. 2010; 107(47):20518-22. doi: 10.1073/pnas.1014557107 PMID: 21041647; PubMed Central PMCID: PMC2996666.
48. Goldfeld AE, Doyle C, Maniatis T. Human tumor necrosis factor alpha gene regulation by virus and lipopolysaccharide. Proceedings of the National Academy of Sciences of the United States of America. 1990; 87(24):9769-73. PMID: 2263628; PubMed Central PMCID: PMC55255.