Novel tubulin antagonist pretubulysin displays antivascular properties in vitro and in vivo

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 34, Issue 2, 2014, Pages 294-303

  Kretzschmann, Verena K ^a,d   Gellrich, Donata ^b   Ullrich, Angelika ^c   Zahler, Stefan ^a   Vollmar, Angelika M ^a   Kazmaier, Uli ^c   Fürst, Robert ^d  

^a UNIVERSITY OF MUNICH   (Germany)

^b LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^c SAARLAND UNIVERSITY   (Germany)

^d GOETHE UNIVERSITY   (Germany)

Author keywords

drug research; endothelial cells; neoplasms; pharmacology

Indexed keywords

DRUG RESEARCH; ENDOTHELIAL CELLS; NEOPLASMS; PHARMACOLOGY;

ACTOMYOSIN; ANGIOGENESIS INHIBITORS; ANIMALS; CAPILLARY PERMEABILITY; CELLS, CULTURED; CRICETINAE; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; INTERCELLULAR JUNCTIONS; MALE; MELANOMA, EXPERIMENTAL; MESOCRICETUS; MICE; MICE, INBRED C57BL; MYOSIN-LIGHT-CHAIN KINASE; NECROSIS; NEOVASCULARIZATION, PATHOLOGIC; NEOVASCULARIZATION, PHYSIOLOGIC; OLIGOPEPTIDES; REGIONAL BLOOD FLOW; RHO-ASSOCIATED KINASES; RHOA GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION; SOFT TISSUE NEOPLASMS; STRESS FIBERS; TIME FACTORS; TUBULIN; TUBULIN MODULATORS; TUMOR BURDEN;

EID: 84895064404     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.113.302155     Document Type: Article

References (36)

1. Dark GG, Hill SA, Prise VE, Tozer GM, Pettit GR, Chaplin DJ. Combretastatin A-4, an agent that displays potent and selective toxicity toward tumor vasculature. Cancer Res. 1997;57:1829-1834
2. Cooney MM, van Heeckeren W, Bhakta S, Ortiz J, Remick SC. Drug insight: Vascular disrupting agents and angiogenesis-novel approaches for drug delivery. Nat Clin Pract Oncol. 2006;3:682-692
3. Iyer S, Chaplin DJ, Rosenthal DS, Boulares AH, Li LY, Smulson ME. Induction of apoptosis in proliferating human endothelial cells by the tumor-specific antiangiogenesis agent combretastatin A-4. Cancer Res. 1998;58:4510-4514
4. Tozer GM, Kanthou C, Parkins CS, Hill SA. The biology of the combretastatins as tumour vascular targeting agents. Int J Exp Pathol. 2002;83:21-38
5. Tozer GM, Prise VE, Wilson J, Cemazar M, Shan S, Dewhirst MW, Barber PR, Vojnovic B, Chaplin DJ. Mechanisms associated with tumor vascular shut-down induced by combretastatin A-4 phosphate: Intravital microscopy and measurement of vascular permeability. Cancer Res. 2001;61:6413-6422
6. Chaplin DJ, Pettit GR, Hill SA. Anti-vascular approaches to solid tumour therapy: Evaluation of combretastatin A4 phosphate. Anticancer Res. 1999;19:189-195
7. Hill SA, Chaplin DJ, Lewis G, Tozer GM. Schedule dependence of combretastatin A4 phosphate in transplanted and spontaneous tumour models. Int J Cancer. 2002;102:70-74
8. Siemann DW, Shi W. Efficacy of combined antiangiogenic and vascular disrupting agents in treatment of solid tumors. Int J Radiat Oncol Biol Phys. 2004;60:1233-1240
9. Grosios K, Loadman PM, Swaine DJ, Pettit GR, Bibby MC. Combination chemotherapy with combretastatin A-4 phosphate and 5-fluorouracil in an experimental murine colon adenocarcinoma. Anticancer Res. 2000;20:229-233
10. Murata R, Siemann DW, Overgaard J, Horsman MR. Interaction between combretastatin A-4 disodium phosphate and radiation in murine tumors. Radiother Oncol. 2001;60:155-161
11. Sandmann A, Sasse F, Müller R. Identification and analysis of the core biosynthetic machinery of tubulysin, a potent cytotoxin with potential anticancer activity. Chem Biol. 2004;11:1071-1079
12. Kaur G, Hollingshead M, Holbeck S, Schauer-Vukasinović V, Camalier RF, Dömling A, Agarwal S. Biological evaluation of tubulysin A: A potential anticancer and antiangiogenic natural product. Biochem J. 2006;396:235-242
13. Sasse F, Steinmetz H, Heil J, Höfle G, Reichenbach H. Tubulysins, new cytostatic peptides from myxobacteria acting on microtubuli. Production, isolation, physico-chemical and biological properties. J Antibiot (Tokyo).2000;53:879-885
14. Höfle G, Glaser N, Leibold T, Karama U, Sasse F, Steinmetz H. Semisynthesis and degradation of the tubulin inhibitors epothilone and tubulysin. Pure Appl. Chem. 2003;75:167-178
15. Peltier HM, McMahon JP, Patterson AW, Ellman JA. The total synthesis of tubulysin D. J Am Chem Soc. 2006;128:16018-16019
16. Pando O, Dörner S, Preusentanz R, Denkert A, Porzel A, Richter W, Wessjohann L. First total synthesis of tubulysin B. Org Lett. 2009;11:5567-5569
17. Shibue T, Hirai T, Okamoto I, Morita N, Masu H, Azumaya I, Tamura O. Total syntheses of tubulysins. Chemistry. 2010;16:11678-11688
18. Ullrich A, Chai Y, Pistorius D, Elnakady YA, Herrmann JE, Weissman KJ, Kazmaier U, Müller R. Pretubulysin, a potent and chemically accessible tubulysin precursor from Angiococc Engl. 2009;48:4422-4425
19. Ullrich A, Herrmann J, Müller R, Kazmaier U. Synthesis and biological evaluation of pretubulysin and derivatives. Eur J Org Chem. 2009;2009:6367-6378
20. Herrmann J, Elnakady YA, Wiedmann RM, Ullrich A, Rohde M, Kazmaier U, Vollmar AM, Müller R. Pretubulysin: From hypothetical biosynthetic intermediate to potential lead in tumor therapy. PLoS One. 2012;7:e37416
21. Eirich J, Burkhart JL, Ullrich A, Rudolf GC, Vollmar A, Zahler S, Kazmaier U, Sieber SA. Pretubulysin derived probes as novel tools for monitoring the microtubule network via activity-based protein profiling and fluorescence microscopy. Mol Biosyst. 2012;8:2067-2075
22. Rath S, Liebl J, Fürst R, Ullrich A, Burkhart JL, Kazmaier U, Herrmann J, Müller R, Günther M, Schreiner L, Wagner E, Vollmar AM, Zahler S. Anti-Angiogenic effects of the tubulysin precursor pretubulysin and of simplified pretubulysin derivatives. Br J Pharmacol. 2012;167:1048-1061
23. Kanthou C, Tozer GM. The tumor vascular targeting agent combretastatin A-4-phosphate induces reorganization of the actin cytoskeleton and early membrane blebbing in human endothelial cells. Blood. 2002;99:2060-2069
24. Verin AD, Birukova A, Wang P, Liu F, Becker P, Birukov K, Garcia JG. Microtubule disassembly increases endothelial cell barrier dysfunction: Role of MLC phosphorylation. Am J Physiol Lung Cell Mol Physiol. 2001;281:L565-L574
25. Birukova AA, Birukov KG, Gorshkov B, Liu F, Garcia JG, Verin AD. MAP kinases in lung endothelial permeability induced by microtubule disassembly. Am J Physiol Lung Cell Mol Physiol. 2005;289:L75-L84
26. Bogatcheva NV, Adyshev D, Mambetsariev B, Moldobaeva N, Verin AD. Involvement of microtubules, p38, and Rho kinases pathway in2-methoxyestradiol- induced lung vascular barrier dysfunction. Am J Physiol Lung Cell Mol Physiol. 2007;292:L487-L499
27. van Horck FP, Ahmadian MR, Haeusler LC, Moolenaar WH, Kranenburg O. Characterization of p190RhoGEF, a RhoA-specific guanine nucleotide exchange factor that interacts with microtubules. J Biol Chem. 2001; 276:4948-4956
28. Ren Y, Li R, Zheng Y, Busch H. Cloning and characterization of GEF-H1, a microtubule-Associated guanine nucleotide exchange factor for Rac and Rho GTPases. J Biol Chem. 1998;273:34954-34960
29. Krendel M, Zenke FT, Bokoch GM. Nucleotide exchange factor GEF-H1mediates cross-talk between microtubules and the actin cytoskeleton. Nat Cell Biol. 2002;4:294-301
30. Guay J, Lambert H, Gingras-Breton G, Lavoie JN, Huot J, Landry J. Regulation of actin filament dynamics by p38 map kinase-mediated phosphorylation of heat shock protein 27. J Cell Sci. 1997;110 (Pt 3):357-368
31. Huot J, Houle F, Marceau F, Landry J. Oxidative stress-induced actin reorganization mediated by the p38 mitogen-Activated protein kinase/heat shock protein 27 pathway in vascular endothelial cells. Circ Res. 1997;80:383-392
32. Kanthou C, Greco O, Stratford A, Cook I, Knight R, Benzakour O, Tozer G. The tubulin-binding agent combretastatin A-4-phosphate arrests endothelial cells in mitosis and induces mitotic cell death. Am J Pathol. 2004;165:1401-1411
33. Vincent L, Kermani P, Young LM, Cheng J, Zhang F, Shido K, Lam G, Bompais-Vincent H, Zhu Z, Hicklin DJ, Bohlen P, Chaplin DJ, May C, Rafii S. Combretastatin A4 phosphate induces rapid regression of tumor neovessels and growth through interference with vascular endothelialcadherin signaling. J Clin Invest. 2005;115:2992-3006
34. Tozer GM, Kanthou C, Baguley BC. Disrupting tumour blood vessels. Nat Rev Cancer. 2005;5:423-435
35. Galbraith SM, Chaplin DJ, Lee F, Stratford MR, Locke RJ, Vojnovic B, Tozer GM. Effects of combretastatin A4 phosphate on endothelial cell morphology in vitro and relationship to tumour vascular targeting activity in vivo. Anticancer Res. 2001;21(1A):93-102
36. Lominadze D, Mchedlishvili G. Red blood cell behavior at low flow rate in microvessels. Microvasc Res. 1999;58:187-189