Reemergence of hedgehog mediates epithelial-mesenchymal crosstalk in pulmonary fibrosis

American Journal of Respiratory Cell and Molecular Biology

Volumn 52, Issue 4, 2015, Pages 418-428

  Hu, Biao ^a   Liu, Jianhua ^a   Wu, Zhe ^a   Liu, Tianju ^a   Ullenbruch, Matthew R ^a   Ding, Lin ^a   Henke, Craig A ^b   Bitterman, Peter B ^b   Phan, Sem H ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Fibrosis; Hedgehog; Myofibroblast

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; HYDROXYPROLINE; SMOOTHENED PROTEIN; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR GLI1; TRANSFORMING GROWTH FACTOR BETA; ACTIN; GLI1 PROTEIN, HUMAN; PROTEIN BINDING; SHH PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLEOMYCIN-INDUCED PULMONARY FIBROSIS; CELL DIFFERENTIATION; CELL LYSATE; CELL SUSPENSION; CELLS; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA PROBE; EPITHELIAL MESENCHYMAL TRANSITION; FLOW CYTOMETRY; GEL MOBILITY SHIFT ASSAY; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IN VIVO STUDY; LUNG ALVEOLUS EPITHELIUM CELL; LUNG ALVEOLUS MACROPHAGE; LUNG FIBROSIS; MYOFIBROBLAST; NONHUMAN; POLYMERASE CHAIN REACTION; PRIMARY CULTURE; PROMOTER REGION; PROTEIN EXPRESSION; SITE DIRECTED MUTAGENESIS; TRANSCRIPTION INITIATION SITE; WESTERN BLOTTING; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL CULTURE; GENETICS; KNOCKOUT MOUSE; METABOLISM; NUCLEOTIDE SEQUENCE; PATHOLOGY;

ERINACEIDAE; MUS; RODENTIA;

ACTINS; ANIMALS; BASE SEQUENCE; CELLS, CULTURED; EPITHELIAL-MESENCHYMAL TRANSITION; HEDGEHOG PROTEINS; HUMANS; MICE, INBRED C57BL; MICE, KNOCKOUT; MYOFIBROBLASTS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PULMONARY FIBROSIS; TRANSCRIPTION FACTORS; ZINC FINGER PROTEIN GLI1;

EID: 84929659148     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2014-0108OC     Document Type: Article

References (48)

1. Fischer A, du Bois R. Interstitial lung disease in connective tissue disorders. Lancet 2012;380:689-698.
2. Noble PW, Barkauskas CE, Jiang D. Pulmonary fibrosis: patterns and perpetrators. J Clin Invest 2012;122:2756-2762.
3. Hu B, Phan SH. Myofibroblasts. Curr Opin Rheumatol 2013;25:71-77.
4. Hinz B, Phan SH, Thannickal VJ, Prunotto M, Desmouliè re A, Varga J, De Wever O, Mareel M, Gabbiani G. Recent developments in myofibroblast biology: paradigms for connective tissue remodeling. Am J Pathol 2012;180:1340-1355.
5. McMahon AP, Ingham PW, Tabin CJ. Developmental roles and clinical significance of hedgehog signaling. Curr Top Dev Biol 2003;53:1-114.
6. Echelard Y, Epstein DJ, St-Jacques B, Shen L, Mohler J, McMahon JA, McMahon AP. Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell 1993;75:1417-1430.
7. Bitgood MJ, Shen L, McMahon AP. Sertoli cell signaling by Desert hedgehog regulates the male germline. Curr Biol 1996;6:298-304.
8. Vortkamp A, Lee K, Lanske B, Segre GV, Kronenberg HM, Tabin CJ. Regulation of rate of cartilage differentiation by Indian hedgehog and PTH-related protein. Science 1996;273:613-622.
9. Kumar S, Balczarek KA, Lai ZC. Evolution of the hedgehog gene family. Genetics 1996;142:965-972.
10. Taipale J, Cooper MK, Maiti T, Beachy PA. Patched acts catalytically to suppress the activity of Smoothened. Nature 2002;418:892-897.
11. Polizio AH, Chinchilla P, Chen X, Manning DR, Riobo NA. Sonic Hedgehog activates the GTPases Rac1 and RhoA in a Gliindependent manner through coupling of smoothened to Gi proteins. Sci Signal 2011;4:pt7.
12. Kinzler KW, Vogelstein B. The GLI gene encodes a nuclear protein which binds specific sequences in the human genome. Mol Cell Biol 1990;10:634-642.
13. Bumcrot DA, Takada R, McMahon AP. Proteolytic processing yields two secreted forms of sonic hedgehog. Mol Cell Biol 1995;15: 2294-2303.
14. Lee JJ, Ekker SC, von Kessler DP, Porter JA, Sun BI, Beachy PA. Autoproteolysis in hedgehog protein biogenesis. Science 1994;266:1528-1537.
15. Porter JA, Young KE, Beachy PA. Cholesterol modification of hedgehog signaling proteins in animal development. Science 1996; 274:255-259.
16. Pepinsky RB, Zeng C, Wen D, Rayhorn P, Baker DP, Williams KP, Bixler SA, Ambrose CM, Garber EA, Miatkowski K, et al. Identification of a palmitic acid-modified form of human Sonic hedgehog. J Biol Chem 1998;273:14037-14045.
17. Chen MH, Li YJ, Kawakami T, Xu SM, Chuang PT. Palmitoylation is required for the production of a soluble multimeric Hedgehog protein complex and long-range signaling in vertebrates. Genes Dev 2004; 18:641-659.
18. Feng J, White B, Tyurina OV, Guner B, Larson T, Lee HY, Karlstrom RO, Kohtz JD. Synergistic and antagonistic roles of the Sonic hedgehog N- and C-terminal lipids. Development 2004;131:4357-4370.
19. Furmanski AL, Saldana JI, Ono M, Sahni H, Paschalidis N, D'Acquisto F, Crompton T. Tissue-derived hedgehog proteins modulate Th differentiation and disease. J Immunol 2013;190:2641-2649.
20. Kolesová H, Roelink H, Grim M. Sonic hedgehog is required for the assembly and remodeling of branchial arch blood vessels. Dev Dyn 2008;237:1923-1934.
21. Stewart GA, Hoyne GF, Ahmad SA, Jarman E, Wallace WA, Harrison DJ, Haslett C, Lamb JR, Howie SE. Expression of the developmental Sonic hedgehog (Shh) signalling pathway is up-regulated in chronic lung fibrosis and the Shh receptor patched 1 is present in circulating T lymphocytes. J Pathol 2003;199:488-495.
22. Coon DR, Roberts DJ, Loscertales M, Kradin R. Differential epithelial expression of SHH and FOXF1 in usual and nonspecific interstitial pneumonia. Exp Mol Pathol 2006;80:119-123.
23. Bolaños AL, Milla CM, Lira JC, Ramírez R, Checa M, Barrera L, García-Alvarez J, Carbajal V, Becerril C, Gaxiola M, et al. Role of Sonic Hedgehog in idiopathic pulmonary fibrosis. Am J Physiol Lung Cell Mol Physiol 2012;303:L978-L990.
24. Cigna N, Farrokhi Moshai E, Brayer S, Marchal-Somme J, Wémeau-Stervinou L, Fabre A, Mal H, Lesèche G, Dehoux M, Soler P, et al. The hedgehog system machinery controls transforming growth factor-b-dependent myofibroblastic differentiation in humans: involvement in idiopathic pulmonary fibrosis. Am J Pathol 2012;181:2126-2137.
25. Fitch PM, Howie SE, Wallace WA. Oxidative damage and TGF-b differentially induce lung epithelial cell sonic hedgehog and tenascin-C expression: implications for the regulation of lung remodelling in idiopathic interstitial lung disease. Int J Exp Pathol 2011;92:8-17.
26. Dang H, Wang S, Yang L, Fang F, Xu F. Upregulation of Shh and Ptc1 in hyperoxia-induced acute lung injury in neonatal rats. Mol Med Rep 2012;6:297-302.
27. Horn A, Palumbo K, Cordazzo C, Dees C, Akhmetshina A, Tomcik M, Zerr P, Avouac J, Gusinde J, Zwerina J, et al. Hedgehog signaling controls fibroblast activation and tissue fibrosis in systemic sclerosis. Arthritis Rheum 2012;64:2724-2733.
28. Pazzaglia S, Cifaldi L, Saran A, Nobili V, Fruci D, Alisi A. Hedgehog/hyaluronic acid interaction network in nonalcoholic fatty liver disease, fibrosis, and hepatocellular carcinoma. Hepatology 2012;56:1589.
29. Guy CD, Suzuki A, Zdanowicz M, Abdelmalek MF, Burchette J, Unalp A, Diehl AM; NASH CRN. Hedgehog pathway activation parallels histologic severity of injury and fibrosis in human nonalcoholic fatty liver disease. Hepatology 2012;55:1711-1721.
30. Philips GM, Chan IS, Swiderska M, Schroder VT, Guy C, Karaca GF, Moylan C, Venkatraman T, Feuerlein S, Syn WK, et al. Hedgehog signaling antagonist promotes regression of both liver fibrosis and hepatocellular carcinoma in a murine model of primary liver cancer. PLoS ONE 2011;6:e23943.
31. Farrokhi Moshai E, Wemeau-Stervinou L, Cigna N, Brayer S, Marchal Somme J, Crestani B, Mailleux AA. Targeting the hedgehog-gli pathway inhibits bleomycin-induced lung fibrosis in mice. Am J Respir Cell Mol Biol 2014;51:11-25.
32. Liu L, Kugler MC, Loomis CA, Samdani R, Zhao Z, Chen GJ, Brandt JP, Brownell I, Joyner AL, Rom WN, et al. Hedgehog signaling in neonatal and adult lung. Am J Respir Cell Mol Biol 2013;48:703-710.
33. Michelotti GA, Xie G, Swiderska M, Choi SS, Karaca G, Krüger L, Premont R, Yang L, Syn WK, Metzger D, et al. Smoothened is a master regulator of adult liver repair. J Clin Invest 2013;123:2380-2394.
34. Long F, Zhang XM, Karp S, Yang Y, McMahon AP. Genetic manipulation of hedgehog signaling in the endochondral skeleton reveals a direct role in the regulation of chondrocyte proliferation. Development 2001;128:5099-5108.
35. Zheng B, Zhang Z, Black CM, de Crombrugghe B, Denton CP. Liganddependent genetic recombination in fibroblasts : a potentially powerful technique for investigating gene function in fibrosis. Am J Pathol 2002;160:1609-1617.
36. Xia H, Diebold D, Nho R, Perlman D, Kleidon J, Kahm J, Avdulov S, Peterson M, Nerva J, Bitterman P, et al. Pathological integrin signaling enhances proliferation of primary lung fibroblasts from patients with idiopathic pulmonary fibrosis. J Exp Med 2008;205: 1659-1672.
37. Hu B, Wu Z, Nakashima T, Phan SH. Mesenchymal-specific deletion of C/EBPb suppresses pulmonary fibrosis. Am J Pathol 2012;180: 2257-2267.
38. Hu B, Tack DC, Liu T, Wu Z, Ullenbruch MR, Phan SH. Role of Smad3 in the regulation of rat telomerase reverse transcriptase by TGFbeta. Oncogene 2006;25:1030-1041.
39. Roper JM, Staversky RJ, Finkelstein JN, Keng PC, O'Reilly MA. Identification and isolation of mouse type II cells on the basis of intrinsic expression of enhanced green fluorescent protein. Am J Physiol Lung Cell Mol Physiol 2003;285:L691-L700.
40. Lo B, Hansen S, Evans K, Heath JK, Wright JR. Alveolar epithelial type II cells induce T cell tolerance to specific antigen. J Immunol 2008; 180:881-888.
41. Hu B, Wu Z, Hergert P, Henke CA, Bitterman PB, Phan SH. Regulation of myofibroblast differentiation by poly(ADP-ribose) polymerase 1. Am J Pathol 2013;182:71-83.
42. Choy SW, Cheng SH. Hedgehog signaling. Vitam Horm 2012;88: 1-23.
43. Fisher CE, Ahmad SA, Fitch PM, Lamb JR, Howie SE. FITC-induced murine pulmonary inflammation: CC10 up-regulation and concurrent Shh expression. Cell Biol Int 2005;29:868-876.
44. Benson RA, Lowrey JA, Lamb JR, Howie SE. The Notch and Sonic hedgehog signalling pathways in immunity. Mol Immunol 2004;41: 715-725.
45. Horn A, Kireva T, Palumbo-Zerr K, Dees C, Tomcik M, Cordazzo C, Zerr P, Akhmetshina A, Ruat M, Distler O, et al. Inhibition of hedgehog signalling prevents experimental fibrosis and induces regression of established fibrosis. Ann Rheum Dis 2012;71:785-789.
46. Choi SS, Omenetti A, Syn WK, Diehl AM. The role of Hedgehog signaling in fibrogenic liver repair. Int J Biochem Cell Biol 2011;43:238-244.
47. Syn WK, Jung Y, Omenetti A, Abdelmalek M, Guy CD, Yang L, Wang J, Witek RP, Fearing CM, Pereira TA, et al. Hedgehog-mediated epithelial-to-mesenchymal transition and fibrogenic repair in nonalcoholic fatty liver disease. Gastroenterology 2009;137: 1478-1488, e8.
48. Ding H, Zhou D, Hao S, Zhou L, He W, Nie J, Hou FF, Liu Y. Sonic hedgehog signaling mediates epithelial-mesenchymal communication and promotes renal fibrosis. J Am Soc Nephrol 2012;23:801-813.