Targeting the isoprenoid pathway to abrogate progression of pulmonary fibrosis

Free Radical Biology and Medicine

Volumn 86, Issue , 2015, Pages 47-56

  Osborn Heaford, Heather L ^a   Murthy, Shubha ^a   Gu, Linlin ^b   Larson Casey, Jennifer L ^a,b   Ryan, Alan J ^a   Shi, Lei ^c   Glogauer, Michael ^d   Neighbors, Jeffrey D ^e   Hohl, Raymond ^a   Carter, A Brent ^a,b,c,f  

^a UNIVERSITY OF IOWA   (United States)

^b University of Alabama at Birmingham   (United States)

^c UNIVERSITY OF IOWA   (United States)

^d UNIVERSITY OF TORONTO   (Canada)

^e University of Iowa   (United States)

^f VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Isoprenoid; Macrophage; Mitochondria; Pathway; Pulmonary fibrosis; Rac1; Reactive oxygen species

Indexed keywords

BISPHOSPHONIC ACID DERIVATIVE; CYSTEINE; DIGERANYL BISPHOSPHONATE; ENZYME INHIBITOR; GERANYLGERANYL PYROPHOSPHATE; HYDROGEN PEROXIDE; ISOPRENOID; RAC1 PROTEIN; RAC2 PROTEIN; UNCLASSIFIED DRUG; NEUROPEPTIDE; RAC1 PROTEIN, MOUSE; TERPENE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASBESTOSIS; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CYTOPLASM; DISEASE COURSE; FIBROSING ALVEOLITIS; GENE TARGETING; GERANYLGERANYLATION; HUMAN; LUNG ALVEOLUS MACROPHAGE; LUNG FIBROSIS; LUNG INJURY; MITOCHONDRIAL RESPIRATION; MOUSE; NONHUMAN; OSMOTIC PUMP; PRIORITY JOURNAL; PROTEIN INDUCTION; PROTEIN PROCESSING; ADOLESCENT; ADULT; ANIMAL; C57BL MOUSE; CASE CONTROL STUDY; DRUG EFFECTS; ENZYME ACTIVATION; METABOLISM; MIDDLE AGED; MOLECULARLY TARGETED THERAPY; OXIDATIVE STRESS; PATHOLOGY; PRECLINICAL STUDY; PULMONARY FIBROSIS; YOUNG ADULT;

MUS;

ADOLESCENT; ADULT; ANIMALS; CASE-CONTROL STUDIES; DIPHOSPHONATES; DISEASE PROGRESSION; DRUG EVALUATION, PRECLINICAL; ENZYME ACTIVATION; HUMANS; MACROPHAGES, ALVEOLAR; MICE, INBRED C57BL; MIDDLE AGED; MOLECULAR TARGETED THERAPY; NEUROPEPTIDES; OXIDATIVE STRESS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PULMONARY FIBROSIS; RAC1 GTP-BINDING PROTEIN; TERPENES; YOUNG ADULT;

EID: 84933046841     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2015.04.031     Document Type: Article

References (58)

1. T.E. King Jr., M.I. Schwarz, K. Brown, J.A. Tooze, T.V. Colby, J.A. Waldron Jr., A. Flint, W. Thurlbeck, and R.M. Cherniack Idiopathic pulmonary fibrosis: relationship between histopathologic features and mortality Am. J. Respir. Crit. Care Med. 164 2001 1025 1032
2. T.E. King Jr., J.A. Tooze, M.I. Schwarz, K.R. Brown, and R.M. Cherniack Predicting survival in idiopathic pulmonary fibrosis: scoring system and survival model Am. J. Respir. Crit. Care Med. 164 2001 1171 1181
3. D.A. Schwartz, R.A. Helmers, J.R. Galvin, D.S. Van Fossen, K.L. Frees, C.S. Dayton, L.F. Burmeister, and G.W. Hunninghake Determinants of survival in idiopathic pulmonary fibrosis Am. J. Respir. Crit. Care Med. 149 1994 450 454
4. 2 generation J. Biol. Chem. 286 2011 15597 15607
5. S. Murthy, A. Adamcakova-Dodd, S.S. Perry, L.A. Tephly, R.M. Keller, N. Metwali, D.K. Meyerholz, Y. Wang, M. Glogauer, P.S. Thorne, and A.B. Carter Modulation of reactive oxygen species by Rac1 or catalase prevents asbestos-induced pulmonary fibrosis Am. J. Physiol. Lung Cell Mol. Physiol 297 2009 L846 L855
6. H.L. Osborn-Heaford, A.J. Ryan, S. Murthy, A.M. Racila, C. He, J.C. Sieren, D.R. Spitz, and A.B. Carter Mitochondrial Rac1 GTPase import and electron transfer from cytochrome c are required for pulmonary fibrosis J. Biol. Chem. 287 2012 3301 3312
7. 2 generation regulates MMP-9 gene expression in macrophages via inhibition of SP-1 and AP-1 J. Biol. Chem. 285 2010 25062 25073
8. A. Hall Small GTP-binding proteins and the regulation of the actin cytoskeleton Annu. Rev. Cell Biol. 10 1994 31 54
9. A.W. Roberts, C. Kim, L. Zhen, J.B. Lowe, R. Kapur, B. Petryniak, A. Spaetti, J.D. Pollock, J.B. Borneo, G.B. Bradford, S.J. Atkinson, M.C. Dinauer, and D.A. Williams Deficiency of the hematopoietic cell-specific Rho family GTPase Rac2 is characterized by abnormalities in neutrophil function and host defense Immunity 10 1999 183 196
10. C.M. Wells, M. Walmsley, S. Ooi, V. Tybulewicz, and A.J. Ridley Rac1-deficient macrophages exhibit defects in cell spreading and membrane ruffling but not migration J.Cell Sci. 117 2004 1259 1268
11. F. Kheradmand, E. Werner, P. Tremble, M. Symons, and Z. Werb Role of Rac1 and oxygen radicals in collagenase-1 expression induced by cell shape change Science 280 1998 898 902
12. M. Ozaki, S.S. Deshpande, P. Angkeow, J. Bellan, C.J. Lowenstein, M.C. Dinauer, P.J. Goldschmidt-Clermont, and K. Irani Inhibition of the Rac1 GTPase protects against nonlethal ischemia/reperfusion-induced necrosis and apoptosis in vivo FASEB J 14 2000 418 429
13. M. Ozaki, S.S. Deshpande, P. Angkeow, S. Suzuki, and K. Irani Rac1 regulates stress-induced, redox-dependent heat shock factor activation J. Biol. Chem. 275 2000 35377 35383
14. C.H. Woo, H.J. You, S.H. Cho, Y.W. Eom, J.S. Chun, Y.J. Yoo, and J.H. Kim Leukotriene B(4) stimulates Rac-ERK cascade to generate reactive oxygen species that mediates chemotaxis J. Biol. Chem. 277 2002 8572 8578
15. P.Y. Zeng, N. Rane, W. Du, J. Chintapalli, and G.C. Prendergast Role for RhoB and PRK in the suppression of epithelial cell transformation by farnesyltransferase inhibitors Oncogene 22 2003 1124 1134
16. J.F. Xu, G.R. Washko, K. Nakahira, H. Hatabu, A.S. Patel, I.E. Fernandez, M. Nishino, Y. Okajima, T. Yamashiro, J.C. Ross, R.S. Estepar, A.A. Diaz, H.P. Li, J.M. Qu, B.E. Himes, C.E. Come, K. D'Aco, F.J. Martinez, M.K. Han, D.A. Lynch, J.D. Crapo, D. Morse, S.W. Ryter, E.K. Silverman, I.O. Rosas, A.M. Choi, G.M. Hunninghake, and C.O. Investigators Statins and pulmonary fibrosis: the potential role of NLRP3 inflammasome activation Am. J. Respir. Crit. Care Med. 185 2012 547 556
17. J.R. Erickson, M.L. Joiner, X. Guan, W. Kutschke, J. Yang, C.V. Oddis, R.K. Bartlett, J.S. Lowe, S.E. O'Donnell, N. Aykin-Burns, M.C. Zimmerman, K. Zimmerman, A.J. Ham, R.M. Weiss, D.R. Spitz, M.A. Shea, R.J. Colbran, P.J. Mohler, and M.E. Anderson A dynamic pathway for calcium-independent activation of CaMKII by methionine oxidation Cell 133 2008 462 474
18. M. Glogauer, C.C. Marchal, F. Zhu, A. Worku, B.E. Clausen, I. Foerster, P. Marks, G.P. Downey, M. Dinauer, and D.J. Kwiatkowski Rac1 deletion in mouse neutrophils has selective effects on neutrophil functions J. Immunol. 170 2003 5652 5657
19. C. He, A.J. Ryan, S. Murthy, and A.B. Carter Accelerated development of pulmonary fibrosis via Cu,Zn-superoxide dismutase-induced alternative activation of macrophages J. Biol. Chem. 288 2013 20745 20757
20. L.W. Shull, A.J. Wiemer, R.J. Hohl, and D.F. Wiemer Synthesis and biological activity of isoprenoid bisphosphonates Bioorg. Med. Chem. 14 2006 4130 4136
21. B.M. Wasko, A. Dudakovic, and R.J. Hohl Bisphosphonates induce autophagy by depleting geranylgeranyl diphosphate J. Pharmacol. Exp. Ther. 337 2011 540 546
22. M.M. Weivoda, and R.J. Hohl The effects of direct inhibition of geranylgeranyl pyrophosphate synthase on osteoblast differentiation J. Cell. Biochem. 112 2011 1506 1513
23. A. Yamauchi, C. Kim, S. Li, C.C. Marchal, J. Towe, S.J. Atkinson, and M.C. Dinauer Rac2-deficient murine macrophages have selective defects in superoxide production and phagocytosis of opsonized particles J. Immunol. 173 2004 5971 5979
24. X. Zhao, K.A. Carnevale, and M.K. Cathcart Human monocytes use Rac1, not Rac2, in the NADPH oxidase complex J. Biol. Chem. 278 2003 40788 40792
25. C.R. Kliment, and T.D. Oury Oxidative stress, extracellular matrix targets, and idiopathic pulmonary fibrosis Free Radic. Biol. Med. 49 2010 707 717
26. K. Psathakis, D. Mermigkis, G. Papatheodorou, S. Loukides, P. Panagou, V. Polychronopoulos, N.M. Siafakas, and D. Bouros Exhaled markers of oxidative stress in idiopathic pulmonary fibrosis European J. Clin. Invest 36 2006 362 367
27. I. Rahman, E. Skwarska, M. Henry, M. Davis, C.M. O'Connor, M.X. FitzGerald, A. Greening, and W. MacNee Systemic and pulmonary oxidative stress in idiopathic pulmonary fibrosis Free Radic. Biol. Med. 27 1999 60 68
28. M. Jain, S. Rivera, E.A. Monclus, L. Synenki, A. Zirk, J. Eisenbart, C. Feghali-Bostwick, G.M. Mutlu, G.R. Budinger, and N.S. Chandel Mitochondrial reactive oxygen species regulate transforming growth factor-beta signaling J. Biol. Chem. 288 2013 770 777
29. G.J. Blauw, A.M. Lagaay, A.H. Smelt, and R.G. Westendorp Stroke, statins, and cholesterol. A meta-analysis of randomized, placebo-controlled, double-blind trials with HMG-CoA reductase inhibitors Stroke 28 1997 946 950
30. J.W. Nawrocki, S.R. Weiss, M.H. Davidson, D.L. Sprecher, S.L. Schwartz, P.J. Lupien, P.H. Jones, H.E. Haber, and D.M. Black Reduction of LDL cholesterol by 25% to 60% in patients with primary hypercholesterolemia by atorvastatin, a new HMG-CoA reductase inhibitor Arterioscler. Thromb. Vasc. Biol. 15 1995 678 682
31. Y. Kureishi, Z. Luo, I. Shiojima, A. Bialik, D. Fulton, D.J. Lefer, W.C. Sessa, and K. Walsh The HMG-CoA reductase inhibitor simvastatin activates the protein kinase Akt and promotes angiogenesis in normocholesterolemic animals Nat. Med 6 2000 1004 1010
32. J.L. Larson-Casey, S. Murthy, A.J. Ryan, and A.B. Carter Modulation of the mevalonate pathway by Akt regulates macrophage survival and development of pulmonary fibrosis J. Biol. Chem. 289 2014 36204 36219
33. T.D. Le Cras, T.R. Korfhagen, C. Davidson, S. Schmidt, M. Fenchel, M. Ikegami, J.A. Whitsett, and W.D. Hardie Inhibition of PI3K by PX-866 prevents transforming growth factor-alpha-induced pulmonary fibrosis Am. J. Pathol. 176 2010 679 686
34. L.F. Li, S.K. Liao, C.C. Huang, M.J. Hung, and D.A. Quinn Serine/threonine kinase-protein kinase B and extracellular signal-regulated kinase regulate ventilator-induced pulmonary fibrosis after bleomycin-induced acute lung injury: a prospective, controlled animal experiment Crit. Care 12 2008 R103
35. Y. Lu, N. Azad, L. Wang, A.K. Iyer, V. Castranova, B.H. Jiang, and Y. Rojanasakul Phosphatidylinositol-3-kinase/Akt regulates bleomycin-induced fibroblast proliferation and collagen production Am. J. Respir. Cell Mol. Biol. 42 2010 432 441
36. R. Vittal, J.C. Horowitz, B.B. Moore, H. Zhang, F.J. Martinez, G.B. Toews, T.J. Standiford, and V.J. Thannickal Modulation of prosurvival signaling in fibroblasts by a protein kinase inhibitor protects against fibrotic tissue injury Am. J. Pathol. 166 2005 367 375
37. H. Xia, D. Diebold, R. Nho, D. Perlman, J. Kleidon, J. Kahm, S. Avdulov, M. Peterson, J. Nerva, P. Bitterman, and C. Henke Pathological integrin signaling enhances proliferation of primary lung fibroblasts from patients with idiopathic pulmonary fibrosis J. Exp. Med. 205 2008 1659 1672
38. D. Pruefer, J. Makowski, M. Schnell, U. Buerke, M. Dahm, H. Oelert, U. Sibelius, U. Grandel, F. Grimminger, W. Seeger, J. Meyer, H. Darius, and M. Buerke Simvastatin inhibits inflammatory properties of Staphylococcus aureus alpha-toxin Circulation 106 2002 2104 2110
39. A.M. Lefer, B. Campbell, Y.K. Shin, R. Scalia, R. Hayward, and D.J. Lefer Simvastatin preserves the ischemic-reperfused myocardium in normocholesterolemic rat hearts Circulation 100 1999 178 184
40. D. Pruefer, R. Scalia, and A.M. Lefer Simvastatin inhibits leukocyte-endothelial cell interactions and protects against inflammatory processes in normocholesterolemic rats Arterioscler. Thromb. Vasc. Biol. 19 1999 2894 2900
41. S.W. Chensue, K. Warmington, J.H. Ruth, N. Lukacs, and S.L. Kunkel Mycobacterial and schistosomal antigen-elicited granuloma formation in IFN-gamma and IL-4 knockout mice: analysis of local and regional cytokine and chemokine networks J. Immunol. 159 1997 3565 3573
42. J.S. Duffield, S.J. Forbes, C.M. Constandinou, S. Clay, M. Partolina, S. Vuthoori, S. Wu, R. Lang, and J.P. Iredale Selective depletion of macrophages reveals distinct, opposing roles during liver injury and repair J. Clin. Invest. 115 2005 56 65
43. R. Shechter, O. Miller, G. Yovel, N. Rosenzweig, A. London, J. Ruckh, K.W. Kim, E. Klein, V. Kalchenko, P. Bendel, S.A. Lira, S. Jung, and M. Schwartz Recruitment of beneficial M2 macrophages to injured spinal cord is orchestrated by remote brain choroid plexus Immunity 38 2013 555 569
44. A. Prasse, D.V. Pechkovsky, G.B. Toews, W. Jungraithmayr, F. Kollert, T. Goldmann, E. Vollmer, J. Muller-Quernheim, and G. Zissel A vicious circle of alveolar macrophages and fibroblasts perpetuates pulmonary fibrosis via CCL18 Am. J. Respir. Crit. Care Med. 173 2006 781 792
45. D.J. Hosfield, Y. Zhang, D.R. Dougan, A. Broun, L.W. Tari, R.V. Swanson, and J. Finn Structural basis for bisphosphonate-mediated inhibition of isoprenoid biosynthesis J. Biol. Chem. 279 2004 8526 8529
46. R.G. Russell, and M.J. Rogers Bisphosphonates: from the laboratory to the clinic and back again Bone 25 1999 97 106
47. Rogers, M.J., Frith, J.C., Luckman, S.P., Coxon, F.P., Benford, H.L., Monkkonen, J., Auriola, S., Chilton, K.M., and Russell, R.G. (1999) Molecular mechanisms of action of bisphosphonates. Bone 24, 73S-79S
48. H.C. Dan, K. Jiang, D. Coppola, A. Hamilton, S.V. Nicosia, S.M. Sebti, and J.Q. Cheng Phosphatidylinositol-3-OH kinase/AKT and survivin pathways as critical targets for geranylgeranyltransferase I inhibitor-induced apoptosis Oncogene 23 2004 706 715
49. M.A. Morgan, J. Wegner, E. Aydilek, A. Ganser, and C.W. Reuter Synergistic cytotoxic effects in myeloid leukemia cells upon cotreatment with farnesyltransferase and geranylgeranyl transferase-I inhibitors Leukemia 17 2003 1508 1520
50. A.K. Sjogren, K.M. Andersson, M. Liu, B.A. Cutts, C. Karlsson, A.M. Wahlstrom, M. Dalin, C. Weinbaum, P.J. Casey, A. Tarkowski, B. Swolin, S.G. Young, and M.O. Bergo GGTase-I deficiency reduces tumor formation and improves survival in mice with K-RAS-induced lung cancer J. Clin. Invest. 117 2007 1294 1304
51. J. Sun, J. Ohkanda, D. Coppola, H. Yin, M. Kothare, B. Busciglio, A.D. Hamilton, and S.M. Sebti Geranylgeranyltransferase I inhibitor GGTI-2154 induces breast carcinoma apoptosis and tumor regression in H-Ras transgenic mice Cancer Res. 63 2003 8922 8929
52. O.M. Khan, M.X. Ibrahim, I.M. Jonsson, C. Karlsson, M. Liu, A.K. Sjogren, F.J. Olofsson, M. Brisslert, S. Andersson, C. Ohlsson, L.M. Hulten, M. Bokarewa, and M.O. Bergo Geranylgeranyltransferase type I (GGTase-I) deficiency hyperactivates macrophages and induces erosive arthritis in mice J. Clin. Invest. 121 2011 628 639
53. M.A. Hagler, T.M. Hadley, H. Zhang, K. Mehra, C.M. Roos, H.V. Schaff, R.M. Suri, and J.D. Miller TGF-beta signalling and reactive oxygen species drive fibrosis and matrix remodelling in myxomatous mitral valves Cardiovasc. Res. 99 2013 175 184
54. S. Soberanes, D. Urich, C.M. Baker, Z. Burgess, S.E. Chiarella, E.L. Bell, A.J. Ghio, A. De Vizcaya-Ruiz, J. Liu, K.M. Ridge, D.W. Kamp, N.S. Chandel, P.T. Schumacker, G.M. Mutlu, and G.R. Budinger Mitochondrial complex III-generated oxidants activate ASK1 and JNK to induce alveolar epithelial cell death following exposure to particulate matter air pollution J. Biol. Chem. 284 2009 2176 2186
55. K.K. Kim, M.C. Kugler, P.J. Wolters, L. Robillard, M.G. Galvez, A.N. Brumwell, D. Sheppard, and H.A. Chapman Alveolar epithelial cell mesenchymal transition develops in vivo during pulmonary fibrosis and is regulated by the extracellular matrix Proc. Natl. Acad. Sci. USA 103 2006 13180 13185
56. Y. Li, D. Jiang, J. Liang, E.B. Meltzer, A. Gray, R. Miura, L. Wogensen, Y. Yamaguchi, and P.W. Noble Severe lung fibrosis requires an invasive fibroblast phenotype regulated by hyaluronan and CD44 J. Exp. Med. 208 2011 1459 1471
57. C. Ramos, M. Montano, J. Garcia-Alvarez, V. Ruiz, B.D. Uhal, M. Selman, and A. Pardo Fibroblasts from idiopathic pulmonary fibrosis and normal lungs differ in growth rate, apoptosis, and tissue inhibitor of metalloproteinases expression Am. J. Respir. Cell Mol. Biol. 24 2001 591 598
58. Y. Zhou, X. Huang, L. Hecker, D. Kurundkar, A. Kurundkar, H. Liu, T.H. Jin, L. Desai, K. Bernard, and V.J. Thannickal Inhibition of mechanosensitive signaling in myofibroblasts ameliorates experimental pulmonary fibrosis J. Clin. Invest. 123 2013 1096 1108