Fumagillin prodrug nanotherapy suppresses macrophage inflammatory response via endothelial nitric oxide

ACS Nano

Volumn 8, Issue 7, 2014, Pages 7305-7317

  Zhou, Hui Fang ^a   Yan, Huimin ^a   Hu, Ying ^a   Springer, Luke E ^a   Yang, Xiaoxia ^a   Wickline, Samuel A ^a   Pan, Dipanjan ^a,b   Lanza, Gregory M ^a   Pham, Christine T N ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

AMP activated protein kinase; angiogenesis; autophagy; fumagillin prodrug; nanotherapy; nitric oxide

Indexed keywords

AMINO ACIDS; ANTIBIOTICS; ASPERGILLUS; MACROPHAGES; NITRIC OXIDE; PATHOLOGY;

AMP-ACTIVATED PROTEIN KINASE; ANGIOGENESIS; AUTOPHAGY; NANOTHERAPY; PRODRUGS;

DISEASES;

ANGIOGENESIS INHIBITOR; CYCLOHEXANE DERIVATIVE; CYTOKINE; FUMAGILLIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; NANOPARTICLE; NITRIC OXIDE; PRODRUG; SESQUITERPENE; TRANSCRIPTION FACTOR RELA; TRIACYLGLYCEROL LIPASE; UNSATURATED FATTY ACID;

ANIMAL; ARTHRITIS; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; ENDOTHELIUM CELL; ENZYME ACTIVATION; IMMUNOLOGY; INFLAMMATION; MACROPHAGE; MALE; METABOLISM; MOUSE; NANOMEDICINE; PATHOLOGY; SIGNAL TRANSDUCTION;

AMP-ACTIVATED PROTEIN KINASES; ANGIOGENESIS INHIBITORS; ANIMALS; ARTHRITIS; CYCLOHEXANES; CYTOKINES; ENDOTHELIAL CELLS; ENZYME ACTIVATION; FATTY ACIDS, UNSATURATED; INFLAMMATION; LIPASE; MACROPHAGES; MALE; MICE; NANOMEDICINE; NANOPARTICLES; NITRIC OXIDE; PRODRUGS; SESQUITERPENES; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR RELA;

EID: 84904736444     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn502372n     Document Type: Article

References (69)

1. Ebos, J. M.; Kerbel, R. S. Antiangiogenic Therapy: Impact on Invasion, Disease Progression, and Metastasis Nat. Rev. Clin. Oncol. 2011, 8, 210-221
2. Jayson, G. C.; Hicklin, D. J.; Ellis, L. M. Antiangiogenic Therapy-Evolving View Based on Clinical Trial Results Nat. Rev. Clin. Oncol. 2012, 9, 297-303
3. Ferrara, N. Role of Myeloid Cells in Vascular Endothelial Growth Factor-Independent Tumor Angiogenesis Curr. Opin. Hematol. 2010, 17, 219-224
4. Levine, B.; Mizushima, N.; Virgin, H. W. Autophagy in Immunity and Inflammation Nature 2011, 469, 323-335
5. White, E.; DiPaola, R. S. The Double-Edged Sword of Autophagy Modulation in Cancer Clin. Cancer Res. 2009, 15, 5308-5316
6. Jones, S. A.; Mills, K. H.; Harris, J. Autophagy and Inflammatory Diseases Immunol. Cell Biol. 2013, 91, 250-258
7. Sin, N.; Meng, L.; Wang, M. Q.; Wen, J. J.; Bornmann, W. G.; Crews, C. M. The Anti-Angiogenic Agent Fumagillin Covalently Binds and Inhibits the Methionine Aminopeptidase, MetAP-2 Proc. Natl. Acad. Sci. U.S.A. 1997, 94, 6099-6103
8. Liu, S.; Widom, J.; Kemp, C. W.; Crews, C. M.; Clardy, J. Structure of Human Methionine Aminopeptidase-2 Complexed with Fumagillin Science 1998, 282, 1324-1327
9. Ingber, D.; Fujita, T.; Kishimoto, S.; Sudo, K.; Kanamaru, T.; Brem, H.; Folkman, J. Synthetic Analogues of Fumagillin that Inhibit Angiogenesis and Suppress Tumour Growth Nature 1990, 348, 555-557
10. Pan, D.; Sanyal, N.; Schmieder, A. H.; Senpan, A.; Kim, B.; Yang, X.; Hu, G.; Allen, J. S.; Gross, R. W.; Wickline, S. A. et al. Antiangiogenic Nanotherapy with Lipase-Labile Sn-2 Fumagillin Prodrug Nanomedicine (London) 2012, 7, 1507-1519
11. Zhou, H. F.; Yan, H.; Senpan, A.; Wickline, S. A.; Pan, D.; Lanza, G. M.; Pham, C. T.N. Suppression of Inflammation in a Mouse Model of Rheumatoid Arthritis Using Targeted Lipase-Labile Fumagillin Prodrug Nanoparticles Biomaterials 2012, 33, 8632-8640
12. Ji, H.; Gauguier, D.; Ohmura, K.; Gonzalez, A.; Duchatelle, V.; Danoy, P.; Garchon, H. J.; Degott, C.; Lathrop, M.; Benoist, C. et al. Genetic Influences on the End-Stage Effector Phase of Arthritis J. Exp. Med. 2001, 194, 321-330
13. 3-Targeted Nanotherapy Suppresses Inflammatory Arthritis in Mice FASEB J. 2009, 23, 2978-2985
14. Zhou, H. F.; Hu, G.; Wickline, S. A.; Lanza, G. M.; Pham, C. T.N. Synergistic Effect of Antiangiogenic Nanotherapy Combined with Methotrexate in the Treatment of Experimental Inflammatory Arthritis Nanomedicine (London) 2010, 5, 1065-1074
15. Bernier, S. G.; Lazarus, D. D.; Clark, E.; Doyle, B.; Labenski, M. T.; Thompson, C. D.; Westlin, W. F.; Hannig, G. A Methionine Aminopeptidase-2 Inhibitor, PPI-2458, for the Treatment of Rheumatoid Arthritis Proc. Natl. Acad. Sci. U.S.A. 2004, 101, 10768-10773
16. Bainbridge, J.; Madden, L.; Essex, D.; Binks, M.; Malhotra, R.; Paleolog, E. M. Methionine Aminopeptidase-2 Blockade Reduces Chronic Collagen-Induced Arthritis: Potential Role for Angiogenesis Inhibition Arthritis Res. Ther. 2007, 9, R127
17. Yoshida, T.; Kaneko, Y.; Tsukamoto, A.; Han, K.; Ichinose, M.; Kimura, S. Suppression of Hepatoma Growth and Angiogenesis by a Fumagillin Derivative TNP470: Possible Involvement of Nitric Oxide Synthase Cancer Res. 1998, 58, 3751-3756
18. Brune, B. Nitric Oxide: NO Apoptosis or Turning It ON? Cell Death Differ. 2003, 10, 864-869
19. Kobayashi, Y. The Regulatory Role of Nitric Oxide in Proinflammatory Cytokine Expression during the Induction and Resolution of Inflammation J. Leukoc. Biol. 2010, 88, 1157-1162
20. Shibata, T.; Nagata, K.; Kobayashi, Y. Cutting edge: A Critical Role of Nitric Oxide in Preventing Inflammation upon Apoptotic Cell Clearance J. Immunol. 2007, 179, 3407-3411
21. Miller, M. R.; Megson, I. L. Recent Developments in Nitric Oxide Donor Drugs Br. J. Pharmacol. 2007, 151, 305-321
22. Rehman, A.; Whiteman, M.; Halliwell, B. Scavenging of Hydroxyl Radicals but Not of Peroxynitrite by Inhibitors and Substrates of Nitric Oxide Synthases Br. J. Pharmacol. 1997, 122, 1702-1706
23. Zhang, J.; Xie, Z.; Dong, Y.; Wang, S.; Liu, C.; Zou, M. H. Identification of Nitric Oxide as an Endogenous Activator of the AMP-Activated Protein Kinase in Vascular Endothelial Cells J. Biol. Chem. 2008, 283, 27452-27461
24. Meares, G. P.; Hughes, K. J.; Naatz, A.; Papa, F. R.; Urano, F.; Hansen, P. A.; Benveniste, E. N.; Corbett, J. A. IRE1-Dependent Activation of AMPK in Response to Nitric Oxide Mol. Cell. Biol. 2011, 31, 4286-4297
25. Sag, D.; Carling, D.; Stout, R. D.; Suttles, J. Adenosine 5′-Monophosphate-Activated Protein Kinase Promotes Macrophage Polarization to an Anti-Inflammatory Functional Phenotype J. Immunol. 2008, 181, 8633-8641
26. Yang, Z.; Kahn, B. B.; Shi, H.; Xue, B. Z. Macrophage α1 AMP-Activated Protein Kinase (α1AMPK) Antagonizes Fatty Acid-Induced Inflammation through SIRT1 J. Biol. Chem. 2010, 285, 19051-19059
27. Galic, S.; Fullerton, M. D.; Schertzer, J. D.; Sikkema, S.; Marcinko, K.; Walkley, C. R.; Izon, D.; Honeyman, J.; Chen, Z. P.; van Denderen, B. J. et al. Hematopoietic AMPK β1 Reduces Mouse Adipose Tissue Macrophage Inflammation and Insulin Resistance in Obesity J. Clin. Invest. 2011, 121, 4903-4915
28. Nath, N.; Giri, S.; Prasad, R.; Salem, M. L.; Singh, A. K.; Singh, I. 5-Aminoimidazole-4-Carboxamide Ribonucleoside: a Novel Immunomodulator with Therapeutic Efficacy in Experimental Autoimmune Encephalomyelitis J. Immunol. 2005, 175, 566-574
29. Zhao, X.; Zmijewski, J. W.; Lorne, E.; Liu, G.; Park, Y. J.; Tsuruta, Y.; Abraham, E. Activation of AMPK Attenuates Neutrophil Proinflammatory Activity and Decreases the Severity of Acute Lung Injury Am. J. Physiol. Lung Cell. Mol. Physiol. 2008, 295, L497-504
30. Bai, A.; Ma, A. G.; Yong, M.; Weiss, C. R.; Ma, Y.; Guan, Q.; Bernstein, C. N.; Peng, Z. AMPK Agonist Downregulates Innate and Adaptive Immune Responses in TNBS-Induced Murine Acute and Relapsing Colitis Biochem. Pharmacol. 2010, 80, 1708-1717
31. Srivastava, R. A.; Pinkosky, S. L.; Filippov, S.; Hanselman, J. C.; Cramer, C. T.; Newton, R. S. AMP-Activated Protein Kinase: An Emerging Drug Target to Regulate Imbalances in Lipid and Carbohydrate Metabolism to Treat Cardio-Metabolic Diseases J. Lipid Res. 2012, 53, 2490-2514
32. Zhou, G.; Myers, R.; Li, Y.; Chen, Y.; Shen, X.; Fenyk-Melody, J.; Wu, M.; Ventre, J.; Doebber, T.; Fujii, N. et al. Role of AMP-Activated Protein Kinase in Mechanism of Metformin Action J. Clin. Invest. 2001, 108, 1167-1174
33. Mosser, D. M.; Edwards, J. P. Exploring the Full Spectrum of Macrophage Activation Nat. Rev. Immunol. 2008, 8, 958-969
34. Martinez, F. O.; Helming, L.; Gordon, S. Alternative Activation of Macrophages: An Immunologic Functional Perspective Annu. Rev. Immunol. 2009, 27, 451-483
35. Inoki, K.; Zhu, T.; Guan, K. L. TSC2Mediates Cellular Energy Response to Control Cell Growth and Survival Cell 2003, 115, 577-590
36. Stein, M.; Keshav, S.; Harris, N.; Gordon, S. Interleukin 4 Potently Enhances Murine Macrophage Mannose Receptor Activity: A Marker of Alternative Immunologic Macrophage Activation J. Exp. Med. 1992, 176, 287-292
37. Meley, D.; Bauvy, C.; Houben-Weerts, J. H.; Dubbelhuis, P. F.; Helmond, M. T.; Codogno, P.; Meijer, A. J. AMP-Activated Protein Kinase and the Regulation of Autophagic Proteolysis J. Biol. Chem. 2006, 281, 34870-34879
38. Levine, B.; Kroemer, G. Autophagy in the Pathogenesis of Disease Cell 2008, 132, 27-42
39. Mizushima, N.; Yoshimori, T.; Levine, B. Methods in Mammalian Autophagy Research Cell 2010, 140, 313-326
40. Bjorkoy, G.; Lamark, T.; Brech, A.; Outzen, H.; Perander, M.; Overvatn, A.; Stenmark, H.; Johansen, T. p62/SQSTM1 Forms Protein Aggregates Degraded by Autophagy and Has a Protective Effect on Huntingtin-Induced Cell Death J. Cell Biol. 2005, 171, 603-614
41. Harris, J. Autophagy and Cytokines Cytokine 2011, 56, 140-144
42. Simmonds, R. E.; Foxwell, B. M. Signalling, Inflammation and Arthritis: NF-κB and its Relevance to Arthritis and Inflammation Rheumatology (Oxford) 2008, 47, 584-590
43. Forstermann, U.; Sessa, W. C. Nitric Oxide Synthases: Regulation and Function Eur. Heart J. 2012, 33 (829-37) 837a-837d
44. Farrell, A. J.; Blake, D. R.; Palmer, R. M.; Moncada, S. Increased Concentrations of Nitrite in Synovial Fluid and Serum Samples Suggest Increased Nitric Oxide Synthesis in Rheumatic Diseases Ann. Rheum. Dis. 1992, 51, 1219-1222
45. Grabowski, P. S.; England, A. J.; Dykhuizen, R.; Copland, M.; Benjamin, N.; Reid, D. M.; Ralston, S. H. Elevated Nitric Oxide Production in Rheumatoid Arthritis. Detection Using the Fasting Urinary Nitrate:Creatinine Ratio Arthritis Rheum. 1996, 39, 643-647
46. McInnes, I. B.; Leung, B. P.; Field, M.; Wei, X. Q.; Huang, F. P.; Sturrock, R. D.; Kinninmonth, A.; Weidner, J.; Mumford, R.; Liew, F. Y. Production of Nitric Oxide in the Synovial Membrane of Rheumatoid and Osteoarthritis Patients J. Exp. Med. 1996, 184, 1519-1524
47. McCartney-Francis, N.; Allen, J. B.; Mizel, D. E.; Albina, J. E.; Xie, Q. W.; Nathan, C. F.; Wahl, S. M. Suppression of Arthritis by an Inhibitor of Nitric Oxide Synthase J. Exp. Med. 1993, 178, 749-754
48. Bao, F.; Wu, P.; Xiao, N.; Qiu, F.; Zeng, Q. P. Nitric Oxide-Driven Hypoxia Initiates Synovial Angiogenesis, Hyperplasia and Inflammatory Lesions in Mice PloS One 2012, 7, e34494
49. Veihelmann, A.; Landes, J.; Hofbauer, A.; Dorger, M.; Refior, H. J.; Messmer, K.; Krombach, F. Exacerbation of Antigen-Induced Arthritis in Inducible Nitric Oxide Synthase-Deficient Mice Arthritis Rheum. 2001, 44, 1420-1427
50. McCartney-Francis, N. L.; Song, X.; Mizel, D. E.; Wahl, S. M. Selective Inhibition of Inducible Nitric Oxide Synthase Exacerbates Erosive Joint Disease J. Immunol. 2001, 166, 2734-2740
51. Veihelmann, A.; Hofbauer, A.; Krombach, F.; Dorger, M.; Maier, M.; Refior, H. J.; Messmer, K. Differential Function of Nitric Oxide in Murine Antigen-Induced Arthritis Rheumatology (Oxford) 2002, 41, 509-517
52. Gomaa, A. A.; Elshenawy, M. M.; Afifi, N. A.; Mohammed, E. A.; Thabit, R. H. Dual Effect of Nitric Oxide Donor on Adjuvant Arthritis Int. Immunopharmacol. 2009, 9, 439-447
53. Leite, A. C.; Cunha, F. Q.; Dal-Secco, D.; Fukada, S. Y.; Girao, V. C.; Rocha, F. A. Effects of Nitric Oxide on Neutrophil Influx Depends on the Tissue: Role of Leukotriene B4 and Adhesion Molecules Br. J. Pharmacol. 2009, 156, 818-825
54. Tripathi, D. N.; Chowdhury, R.; Trudel, L. J.; Tee, A. R.; Slack, R. S.; Walker, C. L.; Wogan, G. N. Reactive Nitrogen Species Regulate Autophagy through ATM-AMPK-TSC2-Mediated Suppression of mTORC1 Proc. Natl. Acad. Sci. U.S.A. 2013, 110, E2950-2957
55. Fisslthaler, B.; Fleming, I. Activation and Signaling by the AMP-Activated Protein Kinase in Endothelial Cells Circ. Res. 2009, 105, 114-127
56. Cacicedo, J. M.; Yagihashi, N.; Keaney, J. F., Jr.; Ruderman, N. B.; Ido, Y. AMPK Inhibits Fatty Acid-Induced Increases in NF-κB Transactivation in Cultured Human Umbilical Vein Endothelial Cells Biochem. Biophys. Res. Commun. 2004, 324, 1204-1299
57. Okayasu, T.; Tomizawa, A.; Suzuki, K.; Manaka, K.; Hattori, Y. PPARα Activators Upregulate eNOS Activity and Inhibit Cytokine-Induced NF-κB Activation through AMP-Activated Protein Kinase Activation Life Sci. 2008, 82, 884-891
58. Hattori, Y.; Nakano, Y.; Hattori, S.; Tomizawa, A.; Inukai, K.; Kasai, K. High Molecular Weight Adiponectin Activates AMPK and Suppresses Cytokine-Induced NF-κB Activation in Vascular Endothelial Cells FEBS Lett. 2008, 582, 1719-1724
59. Laplante, M.; Sabatini, D. M. mTOR Signaling in Growth Control and Disease Cell 2012, 149, 274-293
60. Shintani, T.; Klionsky, D. J. Autophagy in Health and Disease: A Double-Edged Sword Science 2004, 306, 990-995
61. Codogno, P.; Meijer, A. J. Autophagy and Signaling: their Role in Cell Survival and Cell Death Cell Death Differ. 2005, 12 (Suppl 2) 1509-1518
62. Bruyn, G. A.; Tate, G.; Caeiro, F.; Maldonado-Cocco, J.; Westhovens, R.; Tannenbaum, H.; Bell, M.; Forre, O.; Bjorneboe, O.; Tak, P. P. et al. Everolimus in Patients with Rheumatoid Arthritis Receiving Concomitant Methotrexate: A 3-Month, Double-Blind, Randomised, Placebo-Controlled, Parallel-Group, Proof-of-Concept Study Ann. Rheum. Dis. 2008, 67, 1090-1095
63. Qing, G.; Yan, P.; Xiao, G. Hsp90 Inhibition Results in Autophagy-Mediated Proteasome-Independent Degradation of IκB Kinase (IKK) Cell Res. 2006, 16, 895-901
64. Salminen, A.; Hyttinen, J. M.; Kauppinen, A.; Kaarniranta, K. Context-Dependent Regulation of Autophagy by IKK-NF-κB Signaling: Impact on the Aging Process Int. J. Cell Biol. 2012, 2012, 849541
65. Moscat, J.; Diaz-Meco, M. T. p62 at the Crossroads of Autophagy, Apoptosis, and Cancer Cell 2009, 137, 1001-1004
66. Lee, H. M.; Shin, D. M.; Yuk, J. M.; Shi, G.; Choi, D. K.; Lee, S. H.; Huang, S. M.; Kim, J. M.; Kim, C. D.; Lee, J. H. et al. Autophagy Negatively Regulates Keratinocyte Inflammatory Responses via Scaffolding Protein p62/SQSTM1 J. Immunol. 2011, 186, 1248-1258
67. Duran, A.; Linares, J. F.; Galvez, A. S.; Wikenheiser, K.; Flores, J. M.; Diaz-Meco, M. T.; Moscat, J. The Signaling Adaptor p62 is an Important NF-κB Mediator in Tumorigenesis Cancer Cell 2008, 13, 343-354
68. Meoli, D. F.; Sadeghi, M. M.; Krassilnikova, S.; Bourke, B. N.; Giordano, F. J.; Dione, D. P.; Su, H.; Edwards, D. S.; Liu, S.; Harris, T. D. et al. Noninvasive Imaging of Myocardial Angiogenesis Following Experimental Myocardial Infarction J. Clin. Invest. 2004, 113, 1684-1691
69. 3)-Targeted Theranostic Nanoparticles in the MDA-MB-435 Xenograft Mouse Model FASEB J. 2008, 22, 4179-4189