Inhibitor of differentiation 1 promotes endothelial survival in a bleomycin model of lung injury in mice

American Journal of Pathology

Volumn 171, Issue 4, 2007, Pages 1113-1126

  Zhang, Huimin ^a   Lawson, William E ^b   Polosukhin, Vasiliy V ^b   Pozzi, Ambra ^b   Blackwell, Timothy S ^b   Litingtung, Ying ^a   Chiang, Chin ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLEOMYCIN; INHIBITOR OF DIFFERENTIATION 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; DOWN REGULATION; FIBROGENESIS; FLOW CYTOMETRY; HOMEOSTASIS; LUNG ENDOTHELIUM; LUNG INJURY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION;

EID: 35348893705     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.2353/ajpath.2007.070226     Document Type: Article

References (90)

1. Ruzinova MB, Benezra R: Id proteins in development, cell cycle and cancer. Trends Cell Biol 2003, 13:410-418
2. Sun XH, Copeland NG, Jenkins NA, Baltimore D: Id proteins Id1 and Id2 selectively inhibit DNA binding by one class of helix-loop-helix proteins. Mol Cell Biol 1991, 11:5603-5611
3. Zebedee Z, Hara E: Id proteins in cell cycle control and cellular senescence. Oncogene 2001, 20:8317-8325
4. Benezra R, Rafii S, Lyden D: The Id proteins and angiogenesis. Oncogene 2001, 20:8334-8341
5. Wong YC, Wang X, Ling MT: Id-1 expression and cell survival. Apoptosis 2004, 9:279-289
6. Lyden D, Young AZ, Zagzag D, Yan W, Gerald W, O'Reilly R, Bader BL, Hynes RO, Zhuang Y, Manova K, Benezra R: Id1 and Id3 are required for neurogenesis, angiogenesis and vascularization of tumour xenografts. Nature 1999, 401:670-677
7. Engel I, Murre C: The function of E- and Id proteins in lymphocyte development. Nat Rev Immunol 2001, 1:193-199
8. Iavarone A, Lasorella A: Id proteins in neural cancer. Cancer Lett 2004, 204:189-196
9. Li H, Gerald WL, Benezra R: Utilization of bone marrow-derived endothelial cell precursors in spontaneous prostate tumors varies with tumor grade. Cancer Res 2004, 64:6137-6143
10. de Candia P, Benera R, Solit DB: A role for Id proteins in mammary gland physiology and tumorigenesis. Adv Cancer Res 2004, 92:81-94
11. Ling MT, Lau TC, Zhou C, Chua CW, Kwok WK, Wang Q, Wang X, Wong YC: Overexpression of Id-1 in prostate cancer cells promotes angiogenesis through the activation of vascular endothelial growth factor (VEGF). Carcinogenesis 2005, 26:1668-1676
12. Nishiyama K, Takaji K, Kataoka K, Kurihara Y, Yoshimura M, Kato A, Ogawa H, Kurihara H: Id1 gene transfer confers angiogenic property on fully differentiated endothelial cells and contributes to therapeutic angiogenesis. Circulation 2005, 112:2840-2850
13. Alani RM, Young AZ, Shifflett CB: Id1 regulation of cellular senescence through transcriptional repression of p16/Ink4a. Proc Natl Acad Sci USA 2001, 98:7812-7816
14. Sharpless NE, Bardeesy N, Lee KH, Carrasco D, Castrillon DH, Aguirre AJ, Wu EA, Horner JW, DePinho RA: Loss of p16Ink4a with retention of p19Arf predisposes mice to tumorigenesis. Nature 2001, 413:86-91
15. Tang J, Gordon GM, Nickoloff BJ, Foreman KE: The helix-loop-helix protein id-1 delays onset of replicative senescence in human endothelial cells. Lab Invest 2002, 82:1073-1079
16. Frank DB, Abtahi A, Yamaguchi DJ, Manning S, Shyr Y, Pozzi A, Baldwin HS, Johnson JE, de Caestecker MP: Bone morphogenetic protein 4 promotes pulmonary vascular remodeling in hypoxic pulmonary hypertension. Circ Res 2005, 97:496-504
17. Jen Y, Manova K, Benezra R: Expression patterns of Id1, Id2, and Id3 are highly related but distinct from that of Id4 during mouse embryogenesis. Dev Dyn 1996, 207:235-252
18. Chambers RC, Leoni P, Kaminski N, Laurent GJ, Heller RA: Global expression profiling of fibroblast responses to transforming growth factor-beta1 reveals the induction of inhibitor of differentiation-1 and provides evidence of smooth muscle cell phenotypic switching. Am J Pathol 2003, 162:533-546
19. Chua F, Gauldie J, Laurent GJ: Pulmonary fibrosis: searching for model answers. Am J Respir Cell Mol Biol 2005, 33:9-13
20. Zhang HY, Gharaee-Kermani M, Zhang K, Karmiol S, Phan SH: Lung fibroblast alpha-smooth muscle actin expression and contractile phenotype in bleomycin-induced pulmonary fibrosis. Am J Pathol 1996, 148:527-537
21. Cutroneo KR, Phan SH: TGF-beta1-induced Smad 3 binding to the Smad 7 gene: knockout of Smad 7 gene transcription by sense phosphorothioate oligos, autoregulation, and effect on TGF-β1 secretion: bleomycin acts through TGF-β1. J Cell Biochem 2003, 89:474-483
22. Desmoulière A, Geinoz A, Gabbiani F, Gabbiani G: Transforming growth factor-β1 induces alpha-smooth muscle actin expression in granulation tissue myofibroblasts and in quiescent and growing cultured fibroblasts. J Cell Biol 1993, 122:103-111
23. Nakao A, Fujii M, Matsumura R, Kumano K, Saito Y, Miyazono K, Iwamoto I: Transient gene transfer and expression of Smad7 prevents bleomycin-induced lung fibrosis in mice. J Clin Invest 1999, 104:5-11
24. Bonniaud P, Margetts PJ, Kolb M, Schroeder JA, Kapoun AM, Damm D, Murphy A, Chakravarty S, Dugar S, Higgins L, Protter AA, Gauldie J: Progressive transforming growth factor β1-induced lung fibrosis is blocked by an orally active ALK5 kinase inhibitor. Am J Respir Crit Care Med 2005, 171:889-898
25. Chen J, Stubbe J: Bleomycins: towards better therapeutics. Nat Rev Cancer 2005, 5:102-112
26. Phan SH: Fibroblast phenotypes in pulmonary fibrosis. Am J Respir Cell Mol Biol 2003, 29:S87-S92
27. Phan SH: The myofibroblast in pulmonary fibrosis. Chest 2002, 122:286S-289S
28. Kuhn III C, Boldt J, King Jr TE, Crouch E, Vartio T, McDonald JA: An immunohistochemical study of architectural remodeling and connective tissue synthesis in pulmonary fibrosis. Am Rev Respir Dis 1989, 140:1693-1703
29. Zhang K, Rekhter MD, Gordon D, Phan SH: Myofibroblasts and their role in lung collagen gene expression during pulmonary fibrosis. A combined immunohistochemical and in situ hybridization study. Am J Pathol 1994, 145:114-125
30. Tomasek JJ, Gabbiani G, Hinz B, Chaponnier C, Brown RA: Myofibroblasts and mechano-regulation of connective tissue remodeling. Nat Rev Mol Cell Biol 2002, 3:349-363
31. Selman M, King TE, Pardo A: Idiopathic pulmonary fibrosis: prevailing and evolving hypotheses about its pathogenesis and implications for therapy. Ann Intern Med 2001, 134:136-151
32. Gustafsson E, Brakebusch C, Hietanen K, Fassler R: Tie-1-directed expression of Cre recombinase in endothelial cells of embryoid bodies and transgenic mice. J Cell Sci 2001, 114:671-676
33. Li Y, Zhang H, Litingtung Y, Chiang C: Cholesterol modification restricts the spread of Shh gradient in the limb bud. Proc Natl Acad Sci USA 2006, 103:6548-6553
34. Lawson WE, Polosukhin VV, Zoia O, Stathopoulos GT, Han W, Plieth D, Loyd JE, Neilson EG, Blackwell TS: Characterization of fibroblast-specific protein 1 in pulmonary fibrosis. Am J Respir Crit Care Med 2005, 171:899-907
35. Londhe VA, Belperio JA, Keane MP, Burdick MD, Xue YY, Strieter RM: CXCR2 is critical for dsRNA-induced lung injury: relevance to viral lung infection. J Inflamm (Lond) 2005, 2:4
36. Pozzi A, Moberg PE, Miles LA, Wagner S, Soloway P, Gardner HA: Elevated matrix metalloprotease and angiostatin levels in integrin α1 knockout mice cause reduced tumor vascularization. Proc Natl Acad Sci USA 2000, 97:2202-2207
37. Lorimore SA, Coates PJ, Scobie GE, Milne G, Wright EG: Inflammatory-type responses after exposure to ionizing radiation in vivo: a mechanism for radiation-induced bystander effects? Oncogene 2001, 20:7085-7095
38. Lawson WE, Polosukhin VV, Stathopoulos GT, Zoia O, Han W, Lane KB, Li B, Donnelly EF, Holburn GE, Lewis KG, Collins RD, Hull WM, Glasser SW, Whitsett JA, Blackwell TS: Increased and prolonged pulmonary fibrosis in surfactant protein C-deficient mice following intratracheal bleomycin. Am J Pathol 2005, 167:1267-1277
39. Reddy GK, Enwemeka CS: A simplified method for the analysis of hydroxyproline in biological tissues. Clin Biochem 1996, 29:225-229
40. Balyasnikova IV, Visintine DJ, Gunnerson HB, Paisansathan C, Baughman VL, Minshall RD, Danilov SM: Propofol attenuates lung endothelial injury induced by ischemia-reperfusion and oxidative stress. Anesth Analg 2005, 100:929-936
41. Novak A. Guo C, Yang W, Nagy A, Lobe CG: Z/EG, a double reporter mouse line that expresses enhanced green fluorescent protein upon Cre-mediated excision. Genesis 2000, 28:147-155
42. Urase K, Mukasa T, Igarashi H, Ishii Y, Yasugi S, Momoi MY, Momoi T: Spatial expression of Sonic hedgehog in the lung epithelium during branching morphogenesis. Biochem Biophys Res Commun 1996, 225:161-166
43. Litingtung Y, Lei L, Westphal H, Chiang C: Sonic hedgehog is essential to foregut development. Nat Genet 1998, 20:58-61
44. Bitgood MJ. McMahon AP: Hedgehog and Bmp genes are coexpressed at many diverse sites of cell-cell interaction in the mouse embryo. Dev Biol 1995, 172:126-138
45. Bellusci S, Furuta Y, Rush MG, Henderson R, Winnier G, Hogan BL: Involvement of Sonic hedgehog (Shh) in mouse embryonic lung growth and morphogenesis. Development 1997, 124:53-63
46. Nakamura N, Miyagi E, Murata S, Kawaoi A, Katoh R: Expression of thyroid transcription factor-1 in normal and neoplastic lung tissues. Mod Pathol 2002, 15:1058-1067
47. Leeanansaksiri W, Wang H, Gooya JM, Renn K, Abshari M, Tsai S, Keller JR: IL-3 induces inhibitor of DNA-binding protein-1 in hemopoietic progenitor cells and promotes myeloid cell development. J Immunol 2005, 174:7014-7021
48. Ling MT, Wang X, Ouyang XS, Xu K, Tsao SW, Wong YC: Id-1 expression promotes cell survival through activation of NF-kappaB signalling pathway in prostate cancer cells. Oncogene 2003, 22:4498-4508
49. Hui CM, Cheung PY, Ling MT, Tsao SW, Wang X, Wong YC, Cheung AL: Id-1 promotes proliferation of p53-deficient esophageal cancer cells. Int J Cancer 2006, 119:508-514
50. Cheung HW, Ling MT, Tsao SW, Wong YC, Wang X: Id-1-induced Raf/MEK pathway activation is essential for its protective role against taxol-induced apoptosis in nasopharyngeal carcinoma cells. Carcinogenesis 2004, 25:881-887
51. Chang F, Steelman LS, Shelton JG, Lee JT, Navolanic PM, Blalock WL, Franklin R, McCubrey JA: Regulation of cell cycle progression and apoptosis by the Ras/Raf/MEK/ERK pathway. Int J Oncol 2003, 22:469-480
52. Rivo J, Zeira E, Galun E, Einav S, Linden J, Matot I: Attenuation of reperfusion lung injury and apoptosis by A2a adenosine receptor activation is associated with modulation of Bcl-2 and Bax expression and activation of extracellular signal-regulated kinases. Shock 2007, 27:266-273
53. Azuma A, Takahashi S, Nose M, Araki K, Araki M, Takahashi T, Hirose M, Kawashima H, Miyasaka M, Kudoh S: Role of E-selectin in bleomycin induced lung fibrosis in mice. Thorax 2000, 55:147-152
54. Takabatake N, Arao T, Sata M, Abe S, Inoue S, Shibata Y, Takeishi Y, Kubota I: Involvement of pulmonary endothelial cell injury in the pathogenesis of pulmonary fibrosis: clinical assessment by 1231-MIBG lung scintigraphy. Eur J Nucl Med Mol Imaging 2005, 32:221-228
55. Brown LF, Dvorak AM, Dvorak HF: Leaky vessels, fibrin deposition, and fibrosis: a sequence of events common to solid tumors and to many other types of disease. Am Rev Respir Dis 1989, 140:1104-1107
56. Magro CM, Waldman WJ, Knight DA, Allen JN, Nadasdy T, Frambach GE, Ross P, Marsh CB: Idiopathic pulmonary fibrosis related to endothelial injury and antiendothelial cell antibodies. Hum Immunol 2006, 67:284-297
57. Renzoni EA, Walsh DA, Salmon M, Wells AU, Sestini P, Nicholson AG, Veeraraghavan S, Bishop AE, Romanska HM, Pantelidis P, Black CM, Du Bois RM: Interstitial vascularity in fibrosing alveolitis. Am J Respir Crit Care Med 2003, 167:438-443
58. Perk J, Gil-Bazo I, Chin Y, de Candia P, Chen JJ, Zhao Y, Chao S, Cheong W, Ke Y, Al-Ahmadie H, Gerald WL, Brogi E, Benezra R: Reassessment of id1 protein expression in human mammary, prostate, and bladder cancers using a monospecific rabbit monoclonal anti-id1 antibody. Cancer Res 2006, 66:10870-10877
59. Khan TA, Bianchi C, Ruel M, Voisine P, Li J, Liddicoat JR, Sellke FW: Mitogen-activated protein kinase inhibition and cardioplegia-cardiopulmonary bypass reduce coronary myogenic tone. Circulation 2003, 108(Suppl 1):II348-II353
60. Yue TL, Wang C, Gu JL, Ma XL, Kumar S, Lee JC, Feuerstein GZ, Thomas H, Maleeff B, Ohlstein EH: Inhibition of extracellular signal-regulated kinase enhances ischemia/reoxygenation-induced apoptosis in cultured cardiac myocytes and exaggerates reperfusion injury in isolated perfused heart. Circ Res 2000, 86:692-699
61. Yoshida K, Kuwano K, Hagimoto N, Watanabe K, Matsuba T, Fujita M, Inoshima I, Hara N: MAP kinase activation and apoptosis in lung tissues from patients with idiopathic pulmonary fibrosis. J Pathol 2002, 198:388-396
62. Magro CM, Allen J, Pope-Harman A, Waldman WJ, Moh P, Rothrauff S, Ross P Jr: The role of microvascular injury in the evolution of idiopathic pulmonary fibrosis. Am J Clin Pathol 2003, 119:556-567
63. Wang Q, Hyde DM, Giri SN: Abatement of bleomycin-induced increases in vascular permeability, inflammatory cell infiltration, and fibrotic lesions in hamster lungs by combined treatment with taurine and niacin. Lab Invest 1992, 67:234-242
64. Kaplan JD, Trulock EP, Anderson DJ, Schuster DP: Pulmonary vascular permeability in interstitial lung disease. A positron emission tomographic study. Am Rev Respir Dis 1992, 145:1495-1498
65. Peterson LM, Evans ML, Graham MM, Eary JF, Dahlen DD: Vascular response to radiation injury in the rat lung. Radiat Res 1992, 129:139-148
66. 131I- Metaiodobenzylguanidine and 125I-iodoamphetamine. Parameters of lung endothelial cell function and pulmonary vascular area. Eur J Nucl Med 1989, 15:207-210
67. Kasper M, Schobl R, Haroske G, Fischer R, Neubert F, Dimmer V, Muller M: Distribution of von Willebrand factor in capillary endothelial cells of rat lungs with pulmonary fibrosis. Exp Toxicol Pathol 1996, 48:283-288
68. Kawanami O, Jiang HX, Mochimaru H, Yoneyama H, Kudoh S, Ohkuni H, Ooami H, Ferrans VJ: Alveolar fibrosis and capillary alteration in experimental pulmonary silicosis in rats. Am J Respir Crit Care Med 1995, 151:1946-1955
69. Ward WF, Sharplin J, Franko AJ, Hinz JM: Radiation-induced pulmonary endothelial dysfunction and hydroxyproline accumulation in four strains of mice. Radiat Res 1989, 120:113-120
70. Piguet PF, Vesin C: Pulmonary platelet trapping induced by bleomycin: correlation with fibrosis and involvement of the β2 integrins. Int J Exp Pathol 1994, 75:321-328
71. Drab M, Verkade P, Elger M, Kasper M, Lohn M, Lauterbach B, Menne J, Lindschau C, Mende F, Luft FC, Schedl A, Haller H, Kurzchalia TV: Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 gene-disrupted mice. Science 2001, 293:2449-2452
72. Fichtner F, Koslowski R, Augstein A, Hempel U, Rohlecke C, Kasper M: Bleomycin induces IL-8 and ICAM-1 expression in microvascular pulmonary endothelial cells. Exp Toxicol Pathol 2004, 55:497-503
73. Burdick MD, Murray LA, Keane MP, Xue YY, Zisman DA, Belperio JA, Strieter RM: CXCL11 attenuates bleomycin-induced pulmonary fibrosis via inhibition of vascular remodeling. Am J Respir Crit Care Med 2005, 171:261-268
74. Calabrese F, Giacometti C, Rea F, Loy M, Valente M: Idiopathic interstitial pneumonias: Primum movens: epithelial, endothelial or whatever. Sarcoidosis Vasc Diffuse Lung Dis 2005, 22(Suppl 1): S15-S23
75. Kim CB: Advancing the field of lung stem cell biology. Front Biosci 2007, 12:3117-3124
76. Gomperts BN, Strieter RM: Stem cells and chronic lung disease. Annu Rev Med 2007, 58:285-298
77. Jankovic V, Ciarrocchi A, Boccuni P, DeBlasio T, Benezra R, Nimer SD: Id1 restrains myeloid commitment, maintaining the self-renewal capacity of hematopoietic stem cells. Proc Natl Acad Sci USA 2007, 104:1260-1265
78. Hollnagel A, Oehlmann V, Heymer J, Ruther U, Nordheim A: Id genes are direct targets of bone morphogenetic protein induction in embryonic stem cells. J Biol Chem 1999, 274:19838-19845
79. Valdimarsdottir G, Goumans MJ, Rosendahl A, Brugman M, Itoh S, Lebrin F, Sideras P, ten Dijke P: Stimulation of Id1 expression by bone morphogenetic protein is sufficient and necessary for bone morphogenetic protein-induced activation of endothelial cells. Circulation 2002, 106:2263-2270
80. Itoh F, Itoh S, Goumans MJ, Valdimarsdottir G, Iso T, Dotto GP, Hamamori Y, Kedes L, Kato M, ten Dijke Pt P: Synergy and antagonism between Notch and BMP receptor signaling pathways in endothelial cells. EMBO J 2004, 23:541-551
81. Lyden D, Hattori K, Dias S, Costa C, Blaikie P, Butros L, Chadburn A, Heissig B, Marks W, Witte L, Wu Y, Hicklin D, Zhu Z, Hackett NR, Crystal RG, Moore MA, Hajjar KA, Manova K, Benezra R, Rafii S: Impaired recruitment of bone-marrow-derived endothelial and hematopoietic precursor cells blocks tumor angiogenesis and growth. Nat Med 2001, 7:1194-1201
82. Pittet JF, Griffiths MJ, Geiser T, Kaminski N, Dalton SL, Huang X, Brown LA, Gotwals PJ, Koteliansky VE, Matthay MA, Sheppard D: TGF-β is a critical mediator of acute lung injury. J Clin Invest 2001, 107:1537-1544
83. Santana A, Saxena B, Noble NA, Gold LI, Marshall BC: Increased expression of transforming growth factor beta isoforms (β1, 82, β3) in bleomycin-induced pulmonary fibrosis. Am J Respir Cell Mol Biol 1995, 13:34-44
84. Bartram U, Speer CP: The role of transforming growth factor β in lung development and disease. Chest 2004, 125:754-765
85. Zhao J, Shi W, Wang YL, Chen H, Bringas Jr P, Datto MB, Frederick JP, Wang XF, Warburton D: Smad3 deficiency attenuates bleomycin-induced pulmonary fibrosis in mice. Am J Physiol 2002, 282:L585-L593
86. Wang Q, Hyde DM, Gotwals PJ, Giri SN: Effects of delayed treatment with transforming growth factor-beta soluble receptor in a three-dose bleomycin model of lung fibrosis in hamsters. Exp Lung Res 2002, 28:405-417
87. Kowanetz M, Valcourt U, Bergstrom R, Heldin CH, Moustakas A: Id2 and Id3 define the potency of cell proliferation and differentiation responses to transforming growth factor beta and bone morphogenetic protein. Mol Cell Biol 2004, 24:4241-4254
88. Kang Y, Chen CR, Massague J: A self-enabling TGFβ response coupled to stress signaling: smad engages stress response factor ATF3for Id1 repression in epithelial cells. Mol Cell 2003, 11:915-926
89. Goumans MJ, Valdimarsdottir G, Itoh S, Rosendahl A, Sideras P, ten Dijke P: Balancing the activation state of the endothelium via two distinct TGF-β type I receptors. EMBO J 2002, 21:1743-1753
90. Tzeng SF, Kahn M, Liva S, De Vellis J: Tumor necrosis factor-α regulation of the Id gene family in astrocytes and microglia during CNS inflammatory injury. Glia 1999, 26:139-152