Idiopathic pulmonary fibrosis: Aberrant recapitulation of developmental programs?

PLoS Medicine

Volumn 5, Issue 3, 2008, Pages 0373-0380

  Selman, Moisés ^a   Pardo, Annie ^b   Kaminski, Naftali ^c  

^a INSTITUTO NACIONAL DE ENFERMEDADES RESPIRATORIAS   (Mexico)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^c UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; SONIC HEDGEHOG PROTEIN; TRANSFORMING GROWTH FACTOR BETA; WNT PROTEIN;

DEVELOPMENTAL GENE; EPITHELIUM CELL; FIBROBLAST; FIBROMATOSIS; FIBROSING ALVEOLITIS; GENE EXPRESSION; HUMAN; INTERSTITIAL LUNG DISEASE; LUNG; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASTICITY; REVIEW; ARTICLE; CELL PROLIFERATION; GENETIC TRANSCRIPTION; GENETICS; LUNG FIBROSIS; MESODERM; METABOLISM; MORPHOGENESIS; PATHOLOGY; PRENATAL DEVELOPMENT; SIGNAL TRANSDUCTION;

CELL PROLIFERATION; EPITHELIAL CELLS; FIBROBLASTS; GENES, DEVELOPMENTAL; HUMANS; LUNG; MESODERM; MORPHOGENESIS; PULMONARY FIBROSIS; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

EID: 41549108935     PISSN: 15491277     EISSN: 15491676     Source Type: Journal    
DOI: 10.1371/journal.pmed.0050062     Document Type: Review

References (79)

1. Gross TJ, Hunninghake GW (2001) Idiopathic pulmonary fibrosis. N Engl J Med 345: 517-525.
2. Selman M, King TE, Pardo A (2001) Idiopathic pulmonary fibrosis: prevailing and evolving hypotheses about its pathogenesis and implications for therapy. Ann Intern Med 134: 136-151.
3. Selman M, Pardo A, Barrera L, Estrada A, Watson SR, et al. (2006) Gene expression profiles distinguish idiopathic pulmonary fibrosis from hypersensitivity pneumonitis. Am J Respir Crit Care Med 173: 188-198.
4. Thannickal VJ, Toews GB, White ES, Lynch JP 3rd, Martinez FJ (2004) Mechanisms of pulmonary fibrosis. Annu Rev Med 55: 395-417.
5. Zuo F, Kaminski N, Eugui E, Allard J, Yakhini Z, et al. (2002) Gene expression analysis reveals matrilysin as a key regulator of pulmonary fibrosis in mice and humans. Proc Natl Acad Sci U S A 99: 6292-6297.
6. Pardo A, Gibson K, Cisneros J, Richards TJ, Yang Y, et al. (2005) Up-regulation and profibrotic role of osteopontin in human idiopathic pulmonary fibrosis. PLoS Med 2: e251 doi:10.1371/journal.pmed.0020251
7. Studer SM, Kaminski N (2007) Towards systems biology of human pulmonary fibrosis. Proc Am Thorac Soc 4: 85-91.
8. Park KS, Wells JM, Zorn AM, Wert SE, Laubach VE, et al. (2006) Transdifferentiation of ciliated cells during repair of the respiratory epithelium. Am J Respir Cell Mol Biol 34: 151-157.
9. Schock F, Perrimon N (2002) Molecular mechanisms of epithelial morphogenesis. Annu Rev Cell Dev Biol 18: 463-493.
10. Thiery JP, Sleeman JP (2006) Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol 7: 131-142.
11. Moustakas A, Heldin CH (2007) Signaling networks guiding epithelial-mesenchymal transitions during embryogenesis and cancer progression. Cancer Sci 98: 1512-1520.
12. Zavadil J, Bottinger EP (2005) TGF-beta and epithelial-to-mesenchymal transitions. Oncogene 24: 5764-5774.
13. Huber MA, Kraut N, Beug H (2005) Molecular requirements for epithelial-mesenchymal transition during tumor progression. Curr Opin Cell Biol 17: 548-558.
14. Christiansen JJ, Rajasekaran AK (2006) Reassessing epithelial to mesenchymal transition as a prerequisite for carcinoma invasion and metastasis. Cancer Res 66: 8319-8326.
15. Lee JM, Dedhar S, Kalluri R, Thompson EW (2006) The epithelial- mesenchymal transition: new insights in signaling, development, and disease. J Cell Biol 172: 973-981.
16. Willis BC, Borok Z (2007) TGF-β-induced EMT: mechanisms and implications for fibrotic lung disease. Am J Physiol Lung Cell Mol Physiol 293: L525-L534.
17. Iwano M, Plieth D, Danoff TM, Xue C, Okada H, et al. (2002) Evidence that fibroblasts derive from epithelium during tissue fibrosis. J Clin Invest 110: 341-350.
18. Chaffer CL, Brennan JP, Slavin JL, Blick T, Thompson EW, et al. (2006) Mesenchymal-to-epithelial transition facilitates bladder cancer metastasis: role of fibroblast growth factor receptor-2. Cancer Res 66: 11271-11278.
19. Zeisberg M, Yang C, Martino M, Duncan MB, Rieder F, et al. (2007) Fibroblasts derive from hepatocytes in liver fibrosis via epithelial to mesenchymal transition. J Biol Chem 282: 23337-23347.
20. Alonso SR, Tracey L, Ortiz P, Pérez-Gómez B, Palacios J, et al. (2007) A high-throughput study in melanoma identifies epithelialmesenchymal transition as a major determinant of metastasis. Cancer Res 67: 3450-3460.
21. Horikawa T, Yang J, Kondo S, Yoshizaki T, Joab I, et al. (2007) Twist and epithelial-mesenchymal transition are induced by the EBV oncoprotein latent membrane protein 1 and are associated with metastatic nasopharyngeal carcinoma. Cancer Res 67: 1970-1978.
22. Vasko V, Espinosa AV, Scouten W, He H, Auer H, et al. (2007) Gene expression and functional evidence of epithelial-to-mesenchymal transition in papillary thyroid carcinoma invasion. Proc Natl Acad Sci U S A 104: 2803-2808.
23. Lange-Sperandio B, Trautmann A, Eickelberg O, Jayachandran A, Oberle S, et al. (2007) Leukocytes induce epithelial to mesenchymal transition after unilateral ureteral obstruction in neonatal mice. Am J Pathol 171: 861-871.
24. Willis BC, Liebler JM, Luby-Phelps K, Nicholson AG, Crandall ED, et al. (2005) Induction of epithelial-mesenchymal transition in alveolar epithelial cells by transforming growth factor-beta1: potential role in idiopathic pulmonary fibrosis. Am J Pathol 166: 1321-1332.
25. Kim KK, Kugler MC, Wolters PJ, Robillard L, Galvez MG, et al. (2006) Alveolar epithelial cell mesenchymal transition develops in vivo during pulmonary fibrosis and is regulated by the extracellular matrix. Proc Natl Acad Sci U S A 103: 13180-13185.
26. Nawshad A, Hay ED (2003) TGFbeta3 signaling activates transcription of the LEF1 gene to induce epithelial mesenchymal transformation during mouse palate development. J Cell Biol 163: 1291-1301.
27. Romano LA, Runyan RB (2000) Slug is an essential target of TGFbeta2 signaling in the developing chicken heart. Dev Biol 223: 91-102.
28. LaGamba D, Nawshad A, Hay ED (2005) Microarray analysis of gene expression during epithelial-mesenchymal transformation. Dev Dyn 234: 132-142.
29. Lin SJ, Lerch TF, Cook RW, Jardetzky TS, Woodruff TK (2006) The structural basis of TGF-beta, bone morphogenetic protein, and activin ligand binding. Reproduction 132: 179-190.
30. Wahab NA, Mason RM (2006) A critical look at growth factors and epithelial-to-mesenchymal transition in the adult kidney. Interrelationships between growth factors that regulate EMT in the adult kidney. Nephron Exp Nephrol 104: e129-e134.
31. Zeisberg M, Shah AA, Kalluri R (2005) Bone morphogenic protein-7 induces mesenchymal to epithelial transition in adult renal fibroblasts and facilitates regeneration of injured kidney. Biol Chem 280: 8094-8100.
32. Khokha MK, Hsu D, Brunet LJ, Dionne MS, Harland RM (2003) Gremlin is the BMP antagonist required for maintenance of Shh and Fgf signals during limb patterning. Nat Genet 34: 303-307.
33. Koli K, Myllarniemi M, Vuorinen K, Salmenkivi K, Ryynanen MJ, et al. (2006) Bone morphogenetic protein-4 inhibitor gremlin is overexpressed in idiopathic pulmonary fibrosis. Am J Pathol 169: 61-71.
34. Dolan V, Murphy M, Sadlier D, Lappin D, Doran P, et al. (2005) Expression of gremlin, a bone morphogenetic protein antagonist, in human diabetic nephropathy. Am J Kidney Dis 45: 1034-1039.
35. Davies JA, Perera AD, Walker CL (1999) Mechanisms of epithelial development and neoplasia in the metanephric kidney. Int J Dev Biol 43: 473-478.
36. Romio L, Fry AM, Winyard PJ, Malcolm S, Woolf AS, et al. (2004) OFD1 is a centrosomal/basal body protein expressed during mesenchymal-epithelial transition in human nephrogenesis. J Am Soc Nephrol 15: 2556-2568.
37. Warburton D, Schwarz M, Tefft D, Flores-Delgado G, Anderson KD, et al. (2000) The molecular basis of lung morphogenesis. Mech Dev 92: 55-81.
38. Boutet A, De Frutos CA, Maxwell PH, Mayol MJ, Romero J, et al. (2006) Snail activation disrupts tissue homeostasis and induces fibrosis in the adult kidney. EMBO J 25: 5603-5613.
39. Selman M, Pardo A (2006). Role of epithelial cells in idiopathic pulmonary fibrosis: from innocent targets to serial killers. Proc Am Thorac Soc 3: 364-372.
40. Karner C, Wharton KA, Carroll TJ (2006) Apical-basal polarity, Wnt signaling and vertebrate organogenesis. Semin Cell Dev Biol 17: 214-222.
41. Cadigan KM, Liu YI (2006) Wnt signaling: complexity at the surface. J Cell Sci 119: 395-402.
42. Veeman MT, Axelrod JD, Moon RT (2003) A second canon. Functions and mechanisms of beta-catenin-independent Wnt signaling. Dev Cell 5: 367-377.
43. Mucenski ML, Nation JM, Thitoff AR, Besnard V, Xu Y, et al. (2005) Beta-catenin regulates differentiation of respiratory epithelial cells in vivo. Am J Physiol Lung Cell Mol Physiol 289: L971-L979.
44. Shu W, Jiang YQ, Lu MM, Morrisey EE (2002) Wnt7b regulates mesenchymal proliferation vascular development in the lung. Development 129: 4831-4842.
45. Shannon JM, Hyatt BA (2004) Epithelial-mesenchymal interactions in the developing lung. Annu Rev Physiol 66: 625-645.
46. Li C, Xiao J, Hormi K, Borok Z, Minoo P (2002) Wnt5a participates in distal lung morphogenesis. Dev Biol 248: 68-81.
47. Stewart GA, Hoyne GF, Ahmad SA, Jarman E, Wallace WA, et al. (2003) 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 199: 488-495.
48. Coon DR, Roberts DJ, Loscertales M, Kradin R (2006) Differential epithelial expression of SHH and FOXF1 in usual and nonspecific interstitial pneumonia. Exp Mol Pathol 80: 119-123.
49. Chilosi M, Poletti V, Zamo A, Lestani M, Montagna L, et al. (2003) Aberrant Wnt/beta-catenin pathway activation in idiopathic pulmonary fibrosis. Am J Pathol 162: 1495-1502.
50. Cool CD, Groshong SD, Rai PR, Henson PM, Stewart JS, et al. (2006) Fibroblast foci are not discrete sites of lung injury or repair: the fibroblast reticulum. Am J Respir Crit Care Med 174: 654-658.
51. Cheon S, Poon R, Yu C, Khoury M, Shenker R, et al. (2005) Prolonged beta-catenin stabilization and tcf-dependent transcriptional activation in hyperplastic cutaneous wounds. Lab Invest 85: 416-425.
52. Cheon SS, Cheah AY, Turley S, Nadesan P, Poon R, et al. (2002) Beta-catenin stabilization dysregulates mesenchymal cell proliferation, motility, and invasiveness and causes aggressive fibromatosis and hyperplastic cutaneous wounds. Proc Natl Acad Sci U S A 99: 6973-6978.
53. Sato M (2006) Upregulation of the Wnt/beta-catenin pathway induced by transforming growth factor-beta in hypertrophic scars and keloids. Acta Derm Venereol 86: 300-307.
54. Skubitz KM, Skubitz AP (2004) Gene expression in aggressive fibromatosis. J Lab Clin Med. 2004; 143: 89-98.
55. Acharya PS, Zukas A, Chandan V, Katzenstein AL, Pure E (2006) Fibroblast activation protein: a serine protease expressed at the remodeling interface in idiopathic pulmonary fibrosis. Hum Pathol 37: 352-360.
56. Niedermeyer J, Garin-Chesa P, Kriz M, Hilberg F, Mueller E, et al. (2001) Expression of the fibroblast activation protein during mouse embryo development. Int J Dev Biol 45: 445-447.
57. Park JE, Lenter MC, Zimmermann RN, Garin-Chesa P, Old LJ, et al. (1999) Fibroblast activation protein, a dual specificity serine protease expressed in reactive human tumor stromal fibroblasts. J Biol Chem 274: 36505-36512.
58. Aertgeerts K, Levin I, Shi L, Snell GP, Jennings A, et al. (2005) Structural and kinetic analysis of the substrate specificity of human fibroblast activation protein alpha. J Biol Chem 280: 19441-19444.
59. Armanios MY, Chen JJ, Cogan JD, Alder JK, Ingersoll RG, et al. (2007) Telomerase mutations in families with idiopathic pulmonary fibrosis. N Engl J Med 356: 1317-1326.
60. Tsakiri KD, Cronkhite JT, Kuan PJ, Xing C, Raghu G, et al. (2007) Adult-onset pulmonary fibrosis caused by mutations in telomerase. Proc Natl Acad Sci U S A 104: 7552-7557.
61. Matsuo T, Hiyama E, Sugita T, Shimose S, Kubo T, et al. (2007) Telomere length and telomerase activity in extra-abdominal desmoid tumors. Anticancer Res 27: 411-415.
62. Phatak P, Burger AM (2007) Telomerase and its potential for therapeutic intervention. Br J Pharmacol 152: 1003-1011.
63. Holt SE, Shay JW, Wright WE (1996) Refining the telomere-telomerase hypothesis of aging and cancer. Nat Biotechnol 14: 1734-1741.
64. Morlá M, Busquets X, Pons J, Sauleda J, MacNee W, et al. (2006) Telomere shortening in smokers with and without COPD. Eur Respir J 27: 525-528.
65. Gericke A, Munson M, Ross AH (2006) Regulation of the PTEN phosphatase. Gene 374: 1-9.
66. Di Cristofano A, Pesce B, Cordon-Cardo C, Pandolfi, PP (1998) Pten is essential for embryonic development and tumour suppression. Nat Genet 19: 348-355.
67. Stiles B, Groszer M, Wang S, Jiao J, Wu H (2004) PTEN less means more. Dev Biol 273: 175-184.
68. Nho RS, Xia H, Diebold D, Kahm J, Kleidon J, et al. (2006) PTEN regulates fibroblast elimination during collagen matrix contraction. J Biol Chem 281: 33291-33301.
69. Thannickal VJ, Horowitz JC (2006) Evolving concepts of apoptosis in idiopathic pulmonary fibrosis. Proc Am Thorac Soc 3: 350-356.
70. Lappi-Blanco E, Soini Y, Paakko P (1999) Apoptotic activity is increased in the newly formed fibromyxoid connective tissue in bronchiolitis obliterans organizing pneumonia. Lung 177: 367-376.
71. White ES, Atrasz RG, Hu B, Phan SH, Stambolic V, et al. (2006) Negative regulation of myofibroblast differentiation by PTEN (Phosphatase and Tensin Homolog Deleted on chromosome 10). Am J Respir Crit Care Med 173: 112-121.
72. Hjelmeland AB, Hjelmeland MD, Shi Q, Hart JL, Bigner DD, et al. (2005) Loss of phosphatase and tensin homologue increases transforming growth factor beta-mediated invasion with enhanced SMAD3 transcriptional activity. Cancer Res 65: 11276-11281.
73. Mahimainathan L, Das F, Venkatesan B, Choudhury GG (2006) Mesangial cell hypertrophy by high glucose is mediated by downregulation of the tumor suppressor PTEN. Diabetes 55: 2115-2125.
74. Tian Q, He XC, Hood L, Li L (2005) Bridging the BMP and Wnt pathways by PI3 kinase/Akt and 14-3-3zeta. Cell Cycle 4: 215-216.
75. He XC, Zhang J, Tong WG, Tawfik O, Ross J, et al. (2004) BMP signaling inhibits intestinal stem cell self-renewal through suppression of Wnt-b-catenin signaling. Nat Genet 36: 1117-1121.
76. Weaver M, Batts L, Hogan BL (2003) Tissue interactions pattern the mesenchyme of the embryonic mouse lung. Dev Biol 258: 169-184.
77. Bellusci S, Furuta Y, Rush MG, Henderson R, Winnier G, et al. (1997) Involvement of Sonic hedgehog (Shh) in mouse embryonic lung growth and morphogenesis. Development 124: 53-63.
78. Zeisberg M, Hanai J, Sugimoto H, Mammoto T, Charytan D, et al. (2003) BMP-7 counteracts TGF-beta1-induced epithelial-to-mesenchymal transition and reverses chronic renal injury. Nat Med 9: 964-968.
79. Gazdhar A, Fachinger P, van Leer C, Pierog J, Gugger M, et al. (2007) Gene transfer of hepatocyte growth factor by electroporation reduces bleomycin-induced lung fibrosis. Am J Physiol Lung Cell Mol Physiol; 292: L529-L536.