Plasminogen activator inhibitor 1, fibroblast apoptosis resistance, and aging-related susceptibility to lung fibrosis

Experimental Gerontology

Volumn 61, Issue , 2015, Pages 62-75

  Huang, Wen Tan ^a   Akhter, Hasina ^a   Jiang, Chunsun ^c   MacEwen, Mark ^b   Ding, Qiang ^c   Antony, Veena ^c   Thannickal, Victor John ^c   Liu, Rui Ming ^a,c  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b University of Alabama at Birmingham   (United States)

^c University of Alabama at Birmingham   (United States)

Author keywords

Aging; Fibroblast apoptosis; Idiopathic pulmonary fibrosis; Plasminogen activator inhibitor 1

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; BLEOMYCIN; CASPASE 3; HYDROGEN PEROXIDE; PLASMINOGEN ACTIVATOR INHIBITOR 1; SMALL INTERFERING RNA; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA;

AGE; AGED; AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL COUNT; CELL LEVEL; CONTROLLED STUDY; DISEASE PREDISPOSITION; FIBROSING ALVEOLITIS; IN VITRO STUDY; JUVENILE ANIMAL; LUNG FIBROBLAST; LUNG HOMOGENATE; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RISK FACTOR; SUSCEPTIBLE POPULATION; TISSUE LEVEL; ANIMAL; BRONCHOALVEOLAR LAVAGE FLUID; C57BL MOUSE; CYTOLOGY; FIBROBLAST; PHYSIOLOGY; PULMONARY FIBROSIS;

AGING; ANIMALS; APOPTOSIS; BLEOMYCIN; BRONCHOALVEOLAR LAVAGE FLUID; FIBROBLASTS; MALE; MICE; MICE, INBRED C57BL; PLASMINOGEN ACTIVATOR INHIBITOR 1; PULMONARY FIBROSIS; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84913530827     PISSN: 05315565     EISSN: 18736815     Source Type: Journal    
DOI: 10.1016/j.exger.2014.11.018     Document Type: Article

References (70)

1. Abderrahmani R., Francois A., Buard V., Tarlet G., Blirando K., Hneino M., Vaurijoux A., Benderitter M., Sabourin J.C., Milliat F. PAI-1-dependent endothelial cell death determines severity of radiation-induced intestinal injury. PLoS One 2012, 7:e35740.
2. Aillaud M.F., Pignol F., Alessi M.C., Harle J.R., Escande M., Mongin M., Juhan-Vague I. Increase in plasma concentration of plasminogen activator inhibitor, fibrinogen, von Willebrand factor, factor VIII:C and in erythrocyte sedimentation rate with age. Thromb. Haemost. 1986, 55:330-332.
3. Araki T., Katsura H., Sawabe M., Kida K. A clinical study of idiopathic pulmonary fibrosis based on autopsy studies in elderly patients. Intern. Med. 2003, 42:483-489.
4. Bajou K., Peng H., Laug W.E., Maillard C., Noel A., Foidart J.M., Martial J.A., DeClerck Y.A. Plasminogen activator inhibitor-1 protects endothelial cells from FasL-mediated apoptosis. Cancer Cell 2008, 14:324-334.
5. Beier J.I., Kaiser J.P., Guo L., Martinez-Maldonado M., Arteel G.E. Plasminogen activator inhibitor-1 deficient mice are protected from angiotensin II-induced fibrosis. Arch. Biochem. Biophys. 2011, 510:19-26.
6. Bhandary Y.P., Shetty S.K., Marudamuthu A.S., Ji H.L., Neuenschwander P.F., Boggaram V., Morris G.F., Fu J., Idell S., Shetty S. Regulation of lung injury and fibrosis by p53-mediated changes in urokinase and plasminogen activator inhibitor-1. Am. J. Pathol. 2013, 183:131-143.
7. Boucher J., Macotela Y., Bezy O., Mori M.A., Kriauciunas K., Kahn C.R. A kinase-independent role for unoccupied insulin and IGF-1 receptors in the control of apoptosis. Sci. Signal. 2010, 3:ra87.
8. Bruce M.C., Honaker C.E., Cross R.J. Lung fibroblasts undergo apoptosis following alveolarization. Am. J. Respir. Cell Mol. Biol. 1999, 20:228-236.
9. Calabresi C., Arosio B., Galimberti L., Scanziani E., Bergottini R., Annoni G., Vergani C. Natural aging, expression of fibrosis-related genes and collagen deposition in rat lung. Exp. Gerontol. 2007, 42:1003-1011.
10. Casanova A., Giron R.M., Molina M., Xaubet A., Ancochea J. Predictive factors for survival in patients with idiopathic pulmonary fibrosis. Med. Clin. (Barc.) 2009, 133:333-336.
11. Cesari M., Pahor M., Incalzi R.A. REVIEW: plasminogen activator inhibitor-1 (PAI-1): a key factor linking fibrinolysis and age-related subclinical and clinical conditions. Cardiovasc. Ther. 2010, 28:e72-e91.
12. Chang W., Wei K., Jacobs S.S., Upadhyay D., Weill D., Rosen G.D. SPARC suppresses apoptosis of idiopathic pulmonary fibrosis fibroblasts through constitutive activation of beta-catenin. J. Biol. Chem. 2010, 285:8196-8206.
13. Chen S.C., Henry D.O., Reczek P.R., Wong M.K. Plasminogen activator inhibitor-1 inhibits prostate tumor growth through endothelial apoptosis. Mol. Cancer Ther. 2008, 7:1227-1236.
14. Chuang-Tsai S., Sisson T.H., Hattori N., Tsai C.G., Subbotina N.M., Hanson K.E., Simon R.H. Reduction in fibrotic tissue formation in mice genetically deficient in plasminogen activator inhibitor-1. Am. J. Pathol. 2003, 163:445-452.
15. Courey A.J., Horowitz J.C., Kim K.K., Koh T.J., Novak M.L., Subbotina N., Warnock M., Xue B., Cunningham A.K., Lin Y., Goldklang M.P., Simon R.H., Lawrence D.A., Sisson T.H. The vitronectin-binding function of PAI-1 exacerbates lung fibrosis in mice. Blood 2011, 118:2313-2321.
16. Dimova E.Y., Kietzmann T. Metabolic, hormonal and environmental regulation of plasminogen activator inhibitor-1 (PAI-1) expression: lessons from the liver. Thromb. Haemost. 2008, 100:992-1006.
17. Dong J., Fujii S., Imagawa S., Matsumoto S., Matsushita M., Todo S., Tsutsui H., Sobel B.E. IL-1 and IL-6 induce hepatocyte plasminogen activator inhibitor-1 expression through independent signaling pathways converging on C/EBPdelta. Am. J. Physiol. Cell Physiol. 2007, 292:C209-C215.
18. Eitzman D.T., McCoy R.D., Zheng X., Fay W.P., Shen T., Ginsburg D., Simon R.H. Bleomycin-induced pulmonary fibrosis in transgenic mice that either lack or overexpress the murine plasminogen activator inhibitor-1 gene. J. Clin. Invest. 1996, 97:232-237.
19. Eren M., Boe A.E., Murphy S.B., Place A.T., Nagpal V., Morales-Nebreda L., Urich D., Quaggin S.E., Budinger G.R., Mutlu G.M., Miyata T., Vaughan D.E. PAI-1-regulated extracellular proteolysis governs senescence and survival in Klotho mice. Proc. Natl. Acad. Sci. U. S. A. 2014, 111(19):7090-7095.
20. Fell C.D., Martinez F.J., Liu L.X., Murray S., Han M.K., Kazerooni E.A., Gross B.H., Myers J., Travis W.D., Colby T.V., Toews G.B., Flaherty K.R. Clinical predictors of a diagnosis of idiopathic pulmonary fibrosis. Am. J. Respir. Crit. Care Med. 2010, 181:832-837.
21. Fernandez Perez E.R., Daniels C.E., Schroeder D.R., St Sauver J., Hartman T.E., Bartholmai B.J., Yi E.S., Ryu J.H. Incidence, prevalence, and clinical course of idiopathic pulmonary fibrosis: a population-based study. Chest 2010, 137:129-137.
22. Hattori N., Degen J.L., Sisson T.H., Liu H., Moore B.B., Pandrangi R.G., Simon R.H., Drew A.F. Bleomycin-induced pulmonary fibrosis in fibrinogen-null mice. J. Clin. Invest. 2000, 106:1341-1350.
23. Hecker L., Logsdon N.J., Kurundkar D., Kurundkar A., Bernard K., Hock T., Meldrum E., Sanders Y.Y., Thannickal V.J. Reversal of persistent fibrosis in aging by targeting nox4-nrf2 redox imbalance. Sci. Transl. Med. 2014, 6:231-247.
24. Horowitz J.C., Rogers D.S., Simon R.H., Sisson T.H., Thannickal V.J. Plasminogen activation induced pericellular fibronectin proteolysis promotes fibroblast apoptosis. Am. J. Respir. Cell Mol. Biol. 2008, 38:78-87.
25. Hou B., Eren M., Painter C.A., Covington J.W., Dixon J.D., Schoenhard J.A., Vaughan D.E. Tumor necrosis factor {alpha} activates the human plasminogen activator inhibitor-1 gene through a distal nuclear factor {kappa}B site. J. Biol. Chem. 2004, 279:18127-18136.
26. Huang Y., Haraguchi M., Lawrence D.A., Border W.A., Yu L., Noble N.A. A mutant, noninhibitory plasminogen activator inhibitor type 1 decreases matrix accumulation in experimental glomerulonephritis. J. Clin. Invest. 2003, 112:379-388.
27. Huang K., Mitzner W., Rabold R., Schofield B., Lee H., Biswal S., Tankersley C.G. Variation in senescent-dependent lung changes in inbred mouse strains. J. Appl. Physiol. 2007, 102:1632-1639.
28. Huang K., Rabold R., Schofield B., Mitzner W., Tankersley C.G. Age-dependent changes of airway and lung parenchyma in C57BL/6J mice. J. Appl. Physiol. 2007, 102:200-206.
29. Huang W.T., Vayalil P.K., Miyata T., Hagood J., Liu R.M. Therapeutic value of small molecule inhibitor to plasminogen activator inhibitor-1 for lung fibrosis. Am. J. Respir. Cell Mol. Biol. 2012, 46:87-95.
30. Ichimura A., Matsumoto S., Suzuki S., Dan T., Yamaki S., Sato Y., Kiyomoto H., Ishii N., Okada K., Matsuo O., Hou F.F., Vaughan D.E., van Ypersele de Strihou C., Miyata T. A small molecule inhibitor to plasminogen activator inhibitor 1 inhibits macrophage migration. Arterioscler. Thromb. Vasc. Biol. 2013, 33:935-942.
31. Izuhara Y., Yamaoka N., Kodama H., Dan T., Takizawa S., Hirayama N., Meguro K., van Ypersele de Strihou C., Miyata T. A novel inhibitor of plasminogen activator inhibitor-1 provides antithrombotic benefits devoid of bleeding effect in nonhuman primates. J. Cereb. Blood Flow Metab. 2010, 30:904-912.
32. Kaikita K., Fogo A.B., Ma L., Schoenhard J.A., Brown N.J., Vaughan D.E. Plasminogen activator inhibitor-1 deficiency prevents hypertension and vascular fibrosis in response to long-term nitric oxide synthase inhibition. Circulation 2001, 104:839-844.
33. Kinnula V.L. Redox imbalance and lung fibrosis. Antioxid. Redox Signal. 2008, 10:249-252.
34. Kinnula V.L., Myllarniemi M. Oxidant-antioxidant imbalance as a potential contributor to the progression of human pulmonary fibrosis. Antioxid. Redox Signal. 2008, 10:727-738.
35. Knier B., Cordasic N., Klanke B., Heusinger-Ribeiro J., Daniel C., Veelken R., Hartner A., Hilgers K.F. Effect of the plasminogen-plasmin system on hypertensive renal and cardiac damage. J. Hypertens. 2011, 29:1602-1612.
36. Kruithof E.K. Regulation of plasminogen activator inhibitor type 1 gene expression by inflammatory mediators and statins. Thromb. Haemost. 2008, 100:969-975.
37. Liu R.M. Oxidative stress, plasminogen activator inhibitor 1, and lung fibrosis. Antioxid. Redox Signal. 2008, 10:303-319.
38. Liu R.M., Choi J., Wu J.H., Gaston Pravia K.A., Lewis K.M., Brand J.D., Mochel N.S., Krzywanski D.M., Lambeth J.D., Hagood J.S., Forman H.J., Thannickal V.J., Postlethwait E.M. Oxidative modification of nuclear mitogen-activated protein kinase phosphatase 1 is involved in transforming growth factor beta1-induced expression of plasminogen activator inhibitor 1 in fibroblasts. J. Biol. Chem. 2010, 285:16239-16247.
39. Liu R.M., van Groen T., Katre A., Cao D., Kadisha I., Ballinger C., Wang L., Carroll S.L., Li L. Knockout of plasminogen activator inhibitor 1 gene reduces amyloid beta peptide burden in a mouse model of Alzheimer's disease. Neurobiol. Aging 2011, 32:1079-1089.
40. Liu R.M., Vayalil P.K., Ballinger C., Dickinson D.A., Huang W.T., Wang S., Kavanagh T.J., Matthews Q.L., Postlethwait E.M. Transforming growth factor beta suppresses glutamate-cysteine ligase gene expression and induces oxidative stress in a lung fibrosis model. Free Radic. Biol. Med. 2012, 53:554-563.
41. Matsuo S., Lopez-Guisa J.M., Cai X., Okamura D.M., Alpers C.E., Bumgarner R.E., Peters M.A., Zhang G., Eddy A.A. Multifunctionality of PAI-1 in fibrogenesis: evidence from obstructive nephropathy in PAI-1-overexpressing mice. Kidney Int. 2005, 67:2221-2238.
42. Moriwaki H., Stempien-Otero A., Kremen M., Cozen A.E., Dichek D.A. Overexpression of urokinase by macrophages or deficiency of plasminogen activator inhibitor type 1 causes cardiac fibrosis in mice. Circ. Res. 2004, 95:637-644.
43. Naik P.N., Horowitz J.C., Moore T.A., Wilke C.A., Toews G.B., Moore B.B. Pulmonary fibrosis induced by gamma-herpes virus in aged mice is associated with increased fibroblast responsiveness to transforming growth factor-beta. J. Gerontol. A Biol. Sci. Med. Sci. 2012, 67:714-725.
44. Niederer F., Trenkmann M., Ospelt C., Karouzakis E., Neidhart M., Stanczyk J., Kolling C., Gay R.E., Detmar M., Gay S., Jungel A., Kyburz D. Down-regulation of microRNA-34a* in rheumatoid arthritis synovial fibroblasts promotes apoptosis resistance. Arthritis Rheum. 2012, 64:1771-1779.
45. Okada H., Woodcock-Mitchell J., Mitchell J., Sakamoto T., Marutsuka K., Sobel B.E., Fujii S. Induction of plasminogen activator inhibitor type 1 and type 1 collagen expression in rat cardiac microvascular endothelial cells by interleukin-1 and its dependence on oxygen-centered free radicals. Circulation 1998, 97:2175-2182.
46. Oszajca K., Bieniasz M., Brown G., Swiatkowska M., Bartkowiak J., Szemraj J. Effect of oxidative stress on the expression of t-PA, u-PA, u-PAR, and PAI-1 in endothelial cells. Biochem. Cell Biol. 2008, 86:477-486.
47. Park J.M., Lee J.S., Lee K.R., Ha S.J., Hong E.K. Cordyceps militaris extract protects human dermal fibroblasts against oxidative stress-induced apoptosis and premature senescence. Nutrients 2014, 6:3711-3726.
48. Pinheiro G.A., Antao V.C., Wood J.M., Wassell J.T. Occupational risks for idiopathic pulmonary fibrosis mortality in the United States. Int. J. Occup. Environ. Health 2008, 14:117-123.
49. Poggi M., Paulmyer-Lacroix O., Verdier M., Peiretti F., Bastelica D., Boucraut J., Lijnen H.R., Juhan-Vague I., Alessi M.C. Chronic plasminogen activator inhibitor-1 (PAI-1) overexpression dampens CD25+ lymphocyte recruitment after lipopolysaccharide endotoxemia in mouse lung. J. Thromb. Haemost. 2007, 5:2467-2475.
50. Raghu G., Weycker D., Edelsberg J., Bradford W.Z., Oster G. Incidence and prevalence of idiopathic pulmonary fibrosis. Am. J. Respir. Crit. Care Med. 2006, 174:810-816.
51. Redente E.F., Jacobsen K.M., Solomon J.J., Lara A.R., Faubel S., Keith R.C., Henson P.M., Downey G.P., Riches D.W. Age and sex dimorphisms contribute to the severity of bleomycin-induced lung injury and fibrosis. Am. J. Physiol. Lung Cell. Mol. Physiol. 2011, 301:L510-L518.
52. Roelofs J.J.T.H., Teske G.J.D., Bonta P.I., de Vries C.J.M., Meijers J.C.M., Weening J.J., van der Poll T., Florquin S. Plasminogen activator inhibitor-1 regulates neutrophil influx during acute pyelonephritis. Kidney Int. 2008, 75:52-59.
53. Senoo T., Hattori N., Tanimoto T., Furonaka M., Ishikawa N., Fujitaka K., Haruta Y., Murai H., Yokoyama A., Kohno N. Suppression of plasminogen activator inhibitor-1 by RNA interference attenuates pulmonary fibrosis. Thorax 2010, 65:334-340.
54. Seo J.Y., Park J., Yu M.R., Kim Y.S., Ha H., Lee H.B. Positive feedback loop between plasminogen activator inhibitor-1 and transforming growth factor-beta1 during renal fibrosis in diabetes. Am. J. Nephrol. 2009, 30:481-490.
55. Serrano R., Barrenetxe J., Orbe J., Rodriguez J.A., Gallardo N., Martinez C., Andres A., Paramo J.A. Tissue-specific PAI-1 gene expression and glycosylation pattern in insulin-resistant old rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2009, 297:R1563-R1569.
56. Shetty S.K., Bhandary Y.P., Marudamuthu A.S., Abernathy D., Velusamy T., Starcher B., Shetty S. Regulation of airway and alveolar epithelial cell apoptosis by p53-Induced plasminogen activator inhibitor-1 during cigarette smoke exposure injury. Am. J. Respir. Cell Mol. Biol. 2012, 47:474-483.
57. Sueblinvong V., Neujahr D.C., Mills S.T., Roser-Page S., Ritzenthaler J.D., Guidot D., Rojas M., Roman J. Predisposition for disrepair in the aged lung. Am. J. Med. Sci. 2012, 344:41-51.
58. Szigeti A., Hocsak E., Rapolti E., Racz B., Boronkai A., Pozsgai E., Debreceni B., Bognar Z., Bellyei S., Sumegi B., Gallyas F. Facilitation of mitochondrial outer and inner membrane permeabilization and cell death in oxidative stress by a novel Bcl-2 homology 3 domain protein. J. Biol. Chem. 2010, 285:2140-2151.
59. Takeshita K., Yamamoto K., Ito M., Kondo T., Matsushita T., Hirai M., Kojima T., Nishimura M., Nabeshima Y., Loskutoff D.J., Saito H., Murohara T. Increased expression of plasminogen activator inhibitor-1 with fibrin deposition in a murine model of aging, "Klotho" mouse. Semin. Thromb. Hemost. 2002, 28:545-554.
60. Thannickal V.J., Horowitz J.C. Evolving concepts of apoptosis in idiopathic pulmonary fibrosis. Proc. Am. Thorac. Soc. 2006, 3:350-356.
61. To M., Takagi D., Akashi K., Kano I., Haruki K., Barnes P.J., Ito K. Sputum plasminogen activator inhibitor-1 elevation by oxidative stress-dependent nuclear factor-kappaB activation in COPD. Chest 2013, 144:515-521.
62. Vayalil P.K., Iles K.E., Choi J., Yi A.K., Postlethwait E.M., Liu R.M. Glutathione suppresses TGF-beta-induced PAI-1 expression by inhibiting p38 and JNK MAPK and the binding of AP-1, SP-1, and Smad to the PAI-1 promoter. Am. J. Physiol. Lung Cell. Mol. Physiol. 2007, 293:L1281-L1292.
63. von Montfort C., Beier J.I., Kaiser J.P., Guo L., Joshi-Barve S., Pritchard M.T., States J.C., Arteel G.E. PAI-1 plays a protective role in CCl4-induced hepatic fibrosis in mice: role of hepatocyte division. Am. J. Physiol. Gastrointest. Liver Physiol. 2010, 298:G657-G666.
64. Wang H., Zhang Y., Heuckeroth R.O. PAI-1 deficiency reduces liver fibrosis after bile duct ligation in mice through activation of tPA. FEBS Lett. 2007, 581:3098-3104.
65. Weisberg A.D., Albornoz F., Griffin J.P., Crandall D.L., Elokdah H., Fogo A.B., Vaughan D.E., Brown N.J. Pharmacological inhibition and genetic deficiency of plasminogen activator inhibitor-1 attenuates angiotensin ii/salt-induced aortic remodeling. Arterioscler. Thromb. Vasc. Biol. 2005, 25:365-371.
66. Xu Z., Castellino F.J., Ploplis V.A. Plasminogen activator inhibitor-1 (PAI-1) is cardioprotective in mice by maintaining microvascular integrity and cardiac architecture. Blood 2010, 115:2038-2047.
67. Yamaoka N., Kodama H., Izuhara Y., Miyata T., Meguro K. Structure-activity relationships of new N-acylanthranilic acid derivatives as plasminogen activator inhibitor-1 inhibitors. Chem. Pharm. Bull. (Tokyo) 2011, 59:215-224.
68. Zhang D.W., Zheng M., Zhao J., Li Y.Y., Huang Z., Li Z., Han J. Multiple death pathways in TNF-treated fibroblasts: RIP3- and RIP1-dependent and independent routes. Cell Res. 2011, 21:368-371.
69. Zhang Y.P., Li W.B., Wang W.L., Liu J., Song S.X., Bai L.L., Hu Y.Y., Yuan Y.D., Zhang M. siRNA against plasminogen activator inhibitor-1 ameliorates bleomycin-induced lung fibrosis in rats. Acta Pharmacol. Sin. 2012, 33(7):897-908.
70. Zhang Y.P., Wang W.L., Liu J., Li W.B., Bai L.L., Yuan Y.D., Song S.X. Plasminogen activator inhibitor-1 promotes the proliferation and inhibits the apoptosis of pulmonary fibroblasts by Ca(2+) signaling. Thromb. Res. 2013, 131:64-71.