Tropisetron suppresses collagen synthesis in skin fibroblasts via α7 nicotinic acetylcholine receptor and attenuates fibrosis in a scleroderma mouse model

Arthritis and Rheumatism

Volumn 65, Issue 3, 2013, Pages 792-804

  Stegemann, Agatha ^a   Sindrilaru, Anca ^b   Eckes, Beate ^c   Del Rey, Adriana ^d   Heinick, Alexander ^a   Schulte, Jan S ^a   Müller, Frank U ^a   Grando, Sergei A ^e   Fiebich, Bernd L ^f   Scharffetter Kochanek, Karin ^b   Luger, Thomas A ^a   Böhm, Markus ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b UNIVERSITY OF ULM   (Germany)

^c UNIVERSITY OF COLOGNE   (Germany)

^d PHILIPPS UNIVERSITY MARBURG   (Germany)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BLEOMYCIN; BUNGAROTOXIN RECEPTOR; CALCIUM ION; COLLAGEN; CYCLIC AMP; TRANSFORMING GROWTH FACTOR BETA1; TROPISETRON;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASSAY; COLLAGEN SYNTHESIS; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCLERODERMA; SIGNAL TRANSDUCTION; SKIN FIBROBLAST; SKIN FIBROSIS; WESTERN BLOTTING;

EID: 84874428687     PISSN: 00043591     EISSN: 15290131     Source Type: Journal    
DOI: 10.1002/art.37809     Document Type: Article

References (51)

1. Leask A, Abraham DJ,. TGF-β signaling and the fibrotic response. FASEB J 2004; 18: 816-27.
2. Mori Y, Chen SJ, Varga J,. Expression and regulation of intracellular SMAD signaling in scleroderma skin fibroblasts. Arthritis Rheum 2003; 48: 1964-78.
3. Hunzelmann N, Krieg T,. Scleroderma: from pathophysiology to novel therapeutic approaches. Exp Dermatol 2010; 19: 393-400.
4. Gabrielli A, Avvedimento EV, Krieg T,. Scleroderma. N Engl J Med 2009; 360: 1989-2003.
5. Bohm M, Raghunath M, Sunderkotter C, Schiller M, Stander S, Brzoska T, et al. Collagen metabolism is a novel target of the neuropeptide α-melanocyte-stimulating hormone. J Biol Chem 2004; 279: 6959-66.
6. Kokot A, Sindrilaru A, Schiller M, Sunderkotter C, Kerkhoff C, Eckes B, et al. Melanocyte-stimulating hormone suppresses bleomycin-induced collagen synthesis and reduces tissue fibrosis in a mouse model of scleroderma: melanocortin peptides as a novel treatment for scleroderma? Arthritis Rheum 2009; 60: 592-603.
7. Coleiro B, Marshall SE, Denton CP, Howell K, Blann A, Welsh KI, et al. Treatment of Raynaud's phenomenon with the selective serotonin reuptake inhibitor fluoxetine. Rheumatology (Oxford) 2001; 40: 1038-43.
8. Dees C, Akhmetshina A, Zerr P, Reich N, Palumbo K, Horn A, et al. Platelet-derived serotonin links vascular disease and tissue fibrosis. J Exp Med 2011; 208: 961-72.
9. Druce M, Rockall A, Grossman AB,. Fibrosis and carcinoid syndrome: from causation to future therapy. Nat Rev Endocrinol 2009; 5: 276-83.
10. Durward G, Blackford S, Roberts D, Jones MK,. Cutaneous scleroderma in association with carcinoid syndrome. Postgrad Med J 1995; 71: 299-300.
11. Ratnavel RC, Burrows NP, Pye RJ,. Scleroderma and the carcinoid syndrome. Clin Exp Dermatol 1994; 19: 83-5.
12. Slominski A, Pisarchik A, Zbytek B, Tobin DJ, Kauser S, Wortsmann J,. Functional activity of serotoninergic and melatoninergic systems expressed in the skin. J Cell Physiol 2003; 196: 144-53.
13. Hoyer D, Clarke DE, Fozard JR, Hartig PR, Martin GR, Mylecharane EJ, et al. International Union of Pharmacology classification of receptors for 5-hydroxytryptamine (serotonin). Pharmacol Rev 1994; 46: 157-203.
14. Bockaert J, Sebben M, Dumuis A,. Pharmacological characterization of 5-hydroxytryptamine 4 (5-HT4) receptors positively coupled to adenylate cyclase in adult guinea pig hippocampal membranes: effect of substituted benzamide derivatives. Mol Pharmacol 1990; 37: 408-11.
15. Kessler D, Dethlefsen S, Haase I, Plomann H, Hirche F, Krieg T, et al. Fibroblasts in mechanically stressed collagen lattices assume a "synthetic" phenotype. J Biol Chem 2001; 276: 36575-85.
16. Subcommittee for Scleroderma Criteria of the American Rheumatism Association Diagnostic and Therapeutic Criteria Committee. Preliminary criteria for the classification of systemic sclerosis (scleroderma). Arthritis Rheum 1980; 23: 581-90.
17. Ramser B, Kokot A, Metze D, Weiss N, Luger TA, Bohm M,. Hydroxychloroquine modulates metabolic activity and proliferation and induces autophagic cell death of human dermal fibroblasts. J Invest Dermatol 2009; 129: 2419-26.
18. Durk T, Panther E, Muller T, Sorichter S, Ferrari D, Pizzirani C, et al. 5-Hydroxytryptamine modulates cytokine and chemokine production in LPS-primed human monocytes via stimulation of different 5-HTR subtypes. Int Immunol 2005; 17: 599-606.
19. De Rosa MJ, Esandi MD, Garelli A, Rayes D, Bouzat C,. Relationship between α7 nAChR and apoptosis in human lymphocytes. J Neuroimmunol 2005; 160: 154-61.
20. Wei PL, Chan YJ, Ho YS, Lee CH, Yang YY, An J, et al. Tobacco-specific carcinogen enhances colon cancer cell migration through α7-nicotinic acetylcholine receptor. Ann Surg 2009; 249: 978-85.
21. Schiller M, Dennler S, Anderegg U, Kokot A, Simon JC, Luger TA, et al. Increased cAMP levels modulate TGF-β/SMAD-induced expression of extracellular matrix components and other key fibroblast effector functions. J Biol Chem 2010; 285: 409-21.
22. Livak KJ, Schmittgen TJ,. Analysis of relative gene expression data using real-time quantitative PCR and the 2 -ΔΔC T method. Methods 2001; 25: 402-8.
23. Dennler S, Itoh S, Vivien D, Ten Dijke P, Huet S, Gauthier JM,. Direct binding of Smad3 and Smad4 to critical TGF β-inducible elements in the promoter of human plasminogen activator inhibitor-type 1 gene. EMBO J 1998; 17: 3091-100.
24. Yamamoto T, Takagawa S, Katayama I, Yamazaki K, Hamazaki Y, Shinkai H, et al. Animal model of sclerotic skin. I. Local injections of bleomycin induce sclerotic skin mimicking scleroderma. J Invest Dermatol 1999; 112: 456-62.
25. Yamamoto T, Takagawa S, Katayama I, Mizushima Y, Nishioka K,. Effect of superoxide dismutase on bleomycin-induced dermal sclerosis: implications for the treatment of systemic sclerosis. J Invest Dermatol 1999; 113: 843-7.
26. Verrecchia F, Mauviel A,. Control of connective tissue gene expression by TGFβ: role of Smad proteins in fibrosis. Curr Rheumatol Rep 2004; 4: 143-9.
27. Schiller M, Javelaud D, Mauviel A,. TGF-β-induced SMAD signaling and gene regulation: consequences for extracellular matrix remodeling and wound healing. J Dermatol Sci 2004; 35: 83-92.
28. Verrecchia F, Mauviel A, Farge D,. Transforming growth factor-β signaling through the Smad proteins: role in systemic sclerosis. Autoimmun Rev 2005; 5: 563-9.
29. Varga J,. Scleroderma and Smads: dysfunctional Smad family dynamics culminating in fibrosis [review]. Arthritis Rheum 2002; 46: 1703-13.
30. Schiller M, Verrecchia F, Mauviel A,. Cyclic adenosine 3′,5′-monophosphate-elevating agents inhibit transforming growth factor-β-induced SMAD3/4-dependent transcription via protein kinase A-dependent mechanism. Oncogene 2003; 22: 8881-90.
31. Verrecchia F, Chu ML, Mauviel A,. Identification of novel TGF-β/Smad gene targets in dermal fibroblasts using a combined cDNA microarray/promoter transactivation approach. J Biol Chem 2001; 276: 17058-62.
32. Voloshenyuk TG, Landesman ES, Khoutorova E, Hart AD, Gardner JD,. Induction of cardiac fibroblast lysyl oxidase by TGF-β1 requires PI3K/Akt, Smad3, and MAPK signaling. Cytokine 2011; 55: 90-7.
33. Kapeller J, Moller D, Lasitschka F, Autschbach F, Hovius R, Rappold G, et al. Serotonin receptor diversity in the human colon: expression of serotonin type 3 receptor subunits 5-HT3C, 5-HT3D, and 5-HT3E. J Comp Neurol 2011; 519: 420-32.
34. Chetty N, Coupar IM, Tan YY, Desmond PV, Irving HR,. Distribution of serotonin receptors and interacting proteins in the human sigmoid colon. Neurogastroenterol Motil 2009; 21: 551-8, e14-5.
35. Macor JE, Gurley D, Lanthorn T, Loch L, Mack RA, Mullen G, et al. The 5-HT3 antagonist tropisetron (ICS 205-930) is a potent and selective α7 nicotinic receptor partial agonist. Bioorg Med Chem Lett 2001; 11: 319-21.
36. Papke RL, Schiff HC, Jack BA, Horenstein NA,. Molecular dissection of tropisetron, an α7 nicotinic acetylcholine receptor-selective partial agonist. Neurosci Lett 2005; 378: 140-4.
37. Arredondo J, Hall LL, Ndoye A, Nguyen VT, Chernyavsky AI, Bercovich D, et al. Central role of fibroblast α3 nicotinic acetylcholine receptor in mediating cutaneous effects of nicotine. Lab Invest 2003; 83: 207-25.
38. Chen DN, Patrick JW,. The α-bungarotoxin-binding nicotinic acetylcholine receptor from rat brain contains only the α7 subunit. J Biol Chem 1997; 272: 24024-9.
39. Steinbach JH,. Mechanism of action of the nicotinic acetylcholine receptor. Ciba Found Symp 1990; 152: 53-61.
40. Albuquerque EX, Pereira EF, Alkondon M, Schrattenholz A, Maelicke A,. Nicotinic acetylcholine receptors on hippocampal neurons: distribution on the neuronal surface and modulation of receptor activity. J Recept Signal Transduct Res 1997; 17: 243-66.
41. Kurzen H, Wessler I, Kirkpatrick CJ, Kawashima K, Grando SA,. The non-neuronal cholinergic system of human skin. Horm Metab Res 2007; 39: 125-35.
42. Arredondo J, Chernyavsky AI, Jolkovsky DL, Pinkerton KE, Grando SA,. Receptor-mediated tobacco toxicity: cooperation of the Ras/Raf-1/MEK1/ERK and JAK-2/STAT-3 pathways downstream of α7 nicotinic receptor in oral keratinocytes. FASEB J 2006; 20: 2093-101.
43. Park G, Yoon BS, Moon JH, Kim B, Jun EK, Oh S, et al. Green tea polyphenol epigallocatechin-3-gallate suppresses collagen production and proliferation in keloid fibroblasts via inhibition of the STAT3-signaling pathway. J Invest Dermatol 2008; 128: 2429-41.
44. Avouac J, Furnrohr BG, Tomcik M, Palumbo K, Zerr P, Horn A, et al. Inactivation of the transcription factor STAT-4 prevents inflammation-driven fibrosis in animal models of systemic sclerosis. Arthritis Rheum 2011; 63: 800-9.
45. Sugano N, Shimada K, Ito K, Murai S,. Nicotine inhibits the production of inflammatory mediators in U937 cells through modulation of nuclear factor-κB activation. Biochem Biophys Res Commun 1998; 252: 25-8.
46. Arredondo J, Nguyen VT, Chernyavsky AI, Bercovich D, Orr-Urtreger A, Vetter DE, et al. Functional role of α7 nicotinic receptor in physiological control of cutaneous homeostasis. Life Sci 2003; 72: 2063-7.
47. Van Westerloo DJ, Giebelen IA, Florquin S, Bruno MJ, Larosa GJ, Ulloa L, et al. The vagus nerve and nicotinic receptors modulate experimental pancreatitis severity in mice. Gastroenterology 2006; 130: 1822-30.
48. Pavlov VA, Ochani M, Yang LH, Gallowitsch-Puerta M, Ochan K, Lin X, et al. Selective α7-nicotinic acetylcholine receptor agonist GTS-21 improves survival in murine endotoxemia and severe sepsis. Crit Care Med 2007; 35: 1139-44.
49. Van Maanen MA, Lebre MC, van der Poll T, LaRosa GJ, Elbaum D, Vervoordeldonk JM, et al. Stimulation of nicotinic acetylcholine receptors attenuates collagen-induced arthritis in mice. Arthritis Rheum 2009; 60: 114-22.
50. Van Maanen MA, Stoof SP, La Rosa GJ, Vervoordeldonk JM, Tak PP,. Role of the cholinergic nervous system in rheumatoid arthritis: aggravation of arthritis in nicotinic acetylcholine receptor α7 subunit gene knockout mice. Ann Rheum Dis 2011; 69: 1717-23.
51. Galitovskiy V, Qian J, Chernyavsky AI, Marchenko S, Gindi V, Edwards RA, et al. Cytokine-induced alterations of α7 nicotinic receptor in colonic CD4 T cells mediate dichotomous response to nicotine in murine models of Th1/Th17- versus Th2-mediated colitis. J Immunol 2011; 187: 2677-87.