Progress Toward the Development of Noscapine and Derivatives as Anticancer Agents

Journal of Medicinal Chemistry

Volumn 58, Issue 15, 2015, Pages 5699-5727

  DeBono, Aaron ^a   Capuano, Ben ^a   Scammells, Peter J ^a  

^a MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALOID DERIVATIVE; ANTIMITOTIC AGENT; ANTINEOPLASTIC AGENT; COLCHICINE DERIVATIVE; COMBRETASTATIN; NATURAL PRODUCT; NOSCAPINE; NOSCAPINE DERIVATIVE; PODOPHYLLOTOXIN; TAXANE DERIVATIVE; TETRAHYDROISOQUINOLINE DERIVATIVE; TUBULIN; UNCLASSIFIED DRUG; VINCA ALKALOID;

ANTINEOPLASTIC ACTIVITY; ARTICLE; BLOOD BRAIN BARRIER; CANCER CELL LINE; CHEMICAL MODIFICATION; CHROMOSOME ABERRATION; DRUG PROTEIN BINDING; GLIOMA; HUMAN; IMMUNOFLUORESCENCE; MICROTUBULE; MITOSIS; NONHUMAN; STRUCTURE ACTIVITY RELATION; DRUG SCREENING; NEOPLASMS; PATHOLOGY; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; DRUG SCREENING ASSAYS, ANTITUMOR; HUMANS; NEOPLASMS; NOSCAPINE;

EID: 84939165293     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/jm501180v     Document Type: Article

References (147)

1. Proc. Natl. Acad. Sci. U. S. A. 1998, 95, 1601-1606
2. Ye, K.; Ke, Y.; Keshava, N.; Shanks, J.; Kapp, J. A.; Tekmal, R. R.; Petros, J.; Joshi, H. C. Opium Alkaloid Noscapine Is an Antitumor Agent That Arrests Metaphase and Induces Apoptosis in Dividing Cells Proc. Natl. Acad. Sci. U. S. A. 1998, 95, 1601-1606
3. Ferlay, J.; Shin, H.-R.; Bray, F.; Forman, D.; Mathers, C.; Parkin, D. M. Estimates of Worldwide Burden of Cancer in 2008: GLOBOCAN 2008 Int. J. Cancer 2010, 127, 2893-2917
4. Ho, W.; Shubhada, S.; Mills, L.; Negrello, T.; Hao, M.; Connell, E. Cancer in Australia: An Overview 2012; Australian Institute of Health and Welfare & Australasian Association of Cancer Registries: Canberra, 2012; no. 74, pp 1-215
5. Kavallaris, M. Microtubules and Resistance to Tubulin-Binding Agents Nature Rev. Cancer 2010, 10, 194-204
6. Wittmann, T.; Hyman, A.; Desai, A. The Spindle: A Dynamic Assembly of Microtubules and Motors Nature Cell Biol. 2001, 3, E28-E34
7. Singh, H.; Singh, P.; Kumari, K.; Chandra, A.; Dass, S. K.; Chandra, R. A Review on Noscapine, and Its Impact on Heme Metabolism Curr. Drug Metab. 2013, 14, 351-360
8. Zhou, J.; Shu, H.-B.; Joshi, H. C. Regulation of Tubulin Synthesis and Cell Cycle Progression in Mammalian Cells by ?-Tubulin-Mediated Microtubule Nucleation J. Cell. Biochem. 2002, 84, 472-483
9. Campos, S. M.; Dizon, D. Antimitotic Inhibitors Hematol. Oncol. Clin. North Am. 2012, 607-628
10. Wilson, L.; Jordan, M. A. Microtubule Dynamics: Taking Aim at a Moving Target Chem. Biol. 1995, 2, 569-573
11. Zhou, J.; Giannakakou, P. Targeting Microtubules for Cancer Chemotherapy Curr. Med. Chem.: Anti-cancer Agents 2005, 5, 65-71
12. Margolis, R. L.; Wilson, L. Opposite End Assembly and Disassembly of Microtubules at Steady State in Vitro Cell 1978, 13, 1-8
13. Zhou, J.; Panda, D.; Landen, J. W.; Wilson, L.; Joshi, H. C. Minor Alteration of Microtubule Dynamics Causes Loss of Tension across Kinetochore Pairs and Activates the Spindle Checkpoint J. Biol. Chem. 2002, 277, 17200-17208
14. Cragg, G. M.; Grothaus, P. G.; Newman, D. J. Impact of Natural Products on Developing New Anti-Cancer Agents Chem. Rev. 2009, 109, 3012-3043
15. Nogales, E.; Wolf, S. G.; Downing, K. H. Structure of the Aβ Tubulin Dimer by Electron Crystallography Nature 1998, 391, 199-203
16. Ravelli, R. B. G.; Gigant, B.; Curmi, P. A.; Jourdain, I.; Lachkar, S.; Sobel, A.; Knossow, M. Insight Into Tubulin Regulation From a Complex with Colchicine and a Stathmin-Like Domain Nature 2004, 428, 198-202
17. Gigant, B.; Wang, C.; Ravelli, R. B. G.; Roussi, F.; Steinmetz, M. O.; Curmi, P. A.; Sobel, A.; Knossow, M. Structural Basis for the Regulation of Tubulin by Vinblastine Nature 2005, 435, 519-522
18. Burkhart, C. A.; Berman, J. W.; Swindell, C. S.; Horwitz, S. B. Relationship between the Structure of Taxol and Other Taxanes on Induction of Tumor Necrosis Factor-A Gene Expression and Cytotoxicity Cancer Res. 1994, 54, 5779-5782
19. Noble, R. L.; Beer, C. T.; Cutts, J. H. Role of Chance Observations in Chemotherapy: Vinca Rosea Ann. N. Y. Acad. Sci. 2006, 76, 882-894
20. Svoboda, G. H.; Neuss, N.; Gorman, M. Alkaloids of Vinca rosea Linn. (Catharanthus roseus G. Don.) v. Preparation and Characterization of Alkaloids J. Pharm. Sci. 2006, 48, 659-666
21. Bunn, P. A.; Kelly, K. New Chemotherapeutic Agents Prolong Survival and Improve Quality of Life in Non-Small Cell Lung Cancer: A Review of the Literature and Future Directions Clin. Cancer. Res. 1998, 4, 1087-1100
22. Crown, J. Optimising Treatment Outcomes: A Review of Current Management Strategies in First-Line Chemotherapy of Metastatic Breast Cancer Eur. J. Cancer 1997, 33 (Suppl 7) S15-S19
23. Johnson, S. A.; Harper, P.; Hortobagyi, G. N.; Pouillart, P. Vinorelbine: an Overview Cancer Treat. Rev. 1996, 22, 127-142
24. Ngan, V. K.; Bellman, K.; Panda, D.; Hill, B. T.; Jordan, M. A.; Wilson, L. Novel Actions of the Antitumor Drugs Vinflunine and Vinorelbine on Microtubules Cancer Res. 2000, 60, 5054-5051
25. Dhamodharan, R.; Jordan, M. A.; Thrower, D.; Wilson, L.; Wadsworth, P. Vinblastine Suppresses Dynamics of Individual Microtubules in Living Interphase Cells Mol. Biol. Chem. 1995, 6, 1215-1229
26. Wilson, L.; Jordan, M. A.; Morse, A.; Margolis, R. L. Interaction of Vinblastine with Steady-State Microtubules in Vitro J. Mol. Biol. 1982, 159, 125-149
27. Haskins, K. M.; Donoso, J. A.; Himes, R. H. Spirals and Paracrystals Induced by Vinca Alkaloids: Evidence That Microtubule-Associated Proteins Act as Polycations J. Cell Sci. 1981, 47, 237-247
28. Jordan, M. A.; Margolis, R. L.; Himes, R. H.; Wilson, L. Identification of a Distinct Class of Vinblastine Binding Sites on Microtubules J. Mol. Biol. 1986, 187, 61-73
29. Chen, X.-M.; Liu, J.; Wang, T.; Shang, J. Colchicine-Induced Apoptosis in Human Normal Liver L-02 Cells by Mitochondrial Mediated Pathways Toxicol. In Vitro 2012, 26, 649-655
30. Arai, T.; Okuyama, T. Purification and Properties of Colchicine-Binding Protein from the Bovine Brain Seikagaku 1973, 45, 19-29
31. Bhattacharyya, B.; Wolff, J. Promotion of Fluorescence Upon Binding of Colchicine to Tubulin Proc. Natl. Acad. Sci. U. S. A. 1974, 71, 2627-2631
32. Skoufias, D. A.; Wilson, L. Mechanism of Inhibition of Microtubule Polymerization by Colchicine: Inhibitory Potencies of Unliganded Colchicine and Tubulin-Colchicine Complexes Biochemistry 1992, 31, 738-746
33. Uppuluri, S.; Knipling, L.; Sackett, D. L.; Wolff, J. Localization of the Colchicine-Binding Site of Tubulin Proc. Natl. Acad. Sci. U. S. A. 1993, 90, 11598-11602
34. Margolis, R. L.; Wilson, L. Addition of Colchicine-Tubulin Complex to Microtubule Ends: The Mechanism of Substoichiometric Colchicine Poisoning Proc. Natl. Acad. Sci. U. S. A. 1977, 74, 3466-3470
35. Wolff, J.; Knipling, L.; Cahnmann, H. J.; Palumbo, G. Direct Photoaffinity Labeling of Tubulin with Colchicine Proc. Natl. Acad. Sci. U. S. A. 1991, 88, 2820-2824
36. Wani, M. C.; Taylor, H. L.; Wall, M. E.; Coggon, P. Plant Antitumor Agents. VI. Isolation and Structure of Taxol, a Novel Antileukemic and Antitumor Agent From Taxus Brevifolia J. Am. Chem. Sci. 1971, 93, 2325-2327
37. Wall, M. E.; Wani, M. C. Camptothecin and Taxol: Discovery to Clinic-Thirteenth Bruce F. Cain Memorial Award Lecture Cancer Res. 1995, 55, 753-760
38. Schiff, P. B.; Fant, J.; Horwitz, S. B. Promotion of Microtubule Assembly in Vitro by Taxol Nature 1979, 277, 665-667
39. Schiff, P. B.; Horwitz, S. B. Taxol Assembles Tubulin in the Absence of Exogenous Guanosine 5′-Triphosphate or Microtubule-Associated Proteins Biochemistry 1981, 20, 3247-3252
40. Hamel, E.; del Campo, A. A.; Lowe, M. C.; Lin, C. M. Interactions of Taxol, Microtubule-Associated Proteins, and Guanine Nucleotides in Tubulin Polymerization J. Biol. Chem. 1981, 256, 11887-11894
41. Rao, S.; Krauss, N. E.; Heerding, J. M.; Swindell, C. S.; Ringel, I.; Orr, G. A.; Horwitz, S. B. 3′-(P-Azidobenzamido)Taxol Photolabels the N-Terminal 31 Amino Acids of Beta-Tubulin J. Biol. Chem. 1994, 269, 3132-3134
42. Snyder, J. P. The Microtubule-Pore Gatekeeper Nature Chem. Biol. 2007, 3, 81-82
43. Pettit, G. R.; Cragg, G. M.; Herald, D. L. Isolation and Structure of Combretastatin Can. J. Chem. 1982, 60, 1374-1376
44. Rustin, G. J. S. Phase I Clinical Trial of Weekly Combretastatin A4 Phosphate: Clinical and Pharmacokinetic Results J. Clin. Oncol. 2003, 21, 2815-2822
45. Young, S. L.; Chaplin, D. J. Combretastatin A4 Phosphate: Background and Current Clinical Status, Expert Opinion on Investigational Drugs, Informa Healthcare Expert Opin. Invest. Drugs. 2004, 13, 1171-1182
46. Cooney, M. M.; Radivoyevitch, T.; Dowlati, A.; Overmoyer, B.; Levitan, N.; Robertson, K.; Levine, S. L.; DeCaro, K.; Buchter, C.; Taylor, A.; Stambler, B. S.; Remick, S. C. Cardiovascular Safety Profile of Combretastatin A4 Phosphate in a Single-Dose Phase I Study in Patients with Advanced Cancer Clin. Cancer Res. 2004, 10, 96-100
47. Tron, G. C.; Pirali, T.; Sorba, G.; Pagliai, F.; Busacca, S.; Genazzani, A. A. Medicinal Chemistry of Combretastatin A4: Present and Future Directions J. Med. Chem. 2006, 49, 3033-3044
48. McGown, A. T.; Fox, B. W. Differential Cytotoxicity of Combretastatins A1 and A4 in Two Daunorubicin-Resistant P388 Cell Lines Cancer Chemother. Pharmacol. 1990, 26, 79-81
49. Bellina, F.; Cauteruccio, S.; Monti, S.; Rossi, R. Novel Imidazole-Based Combretastatin a-4 Analogues: Evaluation of Their in Vitro Antitumor Activity and Molecular Modeling Study of Their Binding to the Colchicine Site of Tubulin Bioorg. Med. Chem. Lett. 2006, 16, 5757-5762
50. Lin, C. M.; Ho, H. H.; Pettit, G. R.; Hamel, E. Antimitotic Natural Products Combretastatin a-4 and Combretastatin a-2: Studies on the Mechanism of Their Inhibition of the Binding of Colchicine to Tubulin Biochemistry 1989, 28, 6984-6991
51. McGown, A. T.; Fox, B. W. Structural and Biochemical Comparison of the Anti-Mitotic Agents Colchicine, Combretastatin A4 and Amphethinile Anti-Cancer Drug Des. 1989, 3, 249-254
52. Gordaliza, M.; Garcia, P. A.; del Corral, J. M. Podophyllotoxin: Distribution, Sources, Applications and New Cytotoxic Derivatives Toxicon 2004, 44, 441-459
53. Labruère, R.; Gautier, B.; Testud, M.; Seguin, J.; Lenoir, C.; Desbene-Finck, S.; Helissey, P.; Chabot, G. G.; Vidal, M.; Giorgi-Renault, S. Design, Synthesis, and Biological Evaluation of the First Podophyllotoxin Analogues as Potential Vascular-Disrupting Agents ChemMedChem 2010, 5, 2016-2025
54. Bohlin, L.; Rosen, B. Podophyllotoxin Derivatives: Drug Discovery and Development Drug Discovery Today 1996, 1, 343-351
55. Gottesman, M. M.; Fojo, T.; Bates, S. E. Multidrug Resistance in Cancer: Role of ATP-Dependent Transporters Nature Rev. Cancer 2002, 2, 48-58
56. Jain, R. K. Delivery of Molecular Medicine to Solid Tumors: Lessons from in Vivo Imaging of Gene Expression and Function J. Controlled Release 2001, 74, 7-25
57. Green, S. K.; Frankel, A.; Kerbel, R. S. Adhesion-Dependent Multicellular Drug Resistance Anti-Cancer Drug Des. 1999, 14, 153-168
58. Jain, R. K. Normalizing Tumor Vasculature with Anti-Angiogenic Therapy: A New Paradigm for Combination Therapy Nature Med. 2001, 7, 987-989
59. Chen, C.; Chin, J. E.; Ueda, K.; Clark, D. P.; Pastan, I. Internal Duplication and Homology with Bacterial Transport Proteins in the Mdr1 (P-Glycoprotein) Gene From Multidrug-Resistant Human Cells Cell 1986, 47, 381-389
60. Chin, K. V.; Pastan, I.; Gottesman, M. M. Function and Regulation of the Human Multidrug Resistance Gene Adv. Cancer Res. 1993, 156-180
61. Schuetz, E. G.; Beck, W. T.; Schuetz, J. D. Modulators and Substrates of P-Glycoprotein and Cytochrome P4503A Coordinately Up-Regulate These Proteins in Human Colon Carcinoma Cells Mol. Pharmacol. 1996, 49, 311-318
62. Segal, M. S.; Goldstein, M. M.; Attinger, E. O. The Use of Noscapine (Narcotine) as an Antitussive Agent Chest 1957, 32, 305-309
63. Krueger, H. M.; Eddy, N. B.; Sumwalt, M.; Martin, H. The Pharmacology of the Opium Alkaloids, No. 165; US Government Printing Office: Washington, DC, 1941.
64. Winter, C. A.; Flataker, L. Toxicity Studies on Noscapine Toxicol. Appl. Pharmacol. 1961, 3, 96-106
65. 3H]Noscapine in Guinea Pig Brain Tissue Eur. J. Pharmacol. 1988, 145, 195-203
66. Craviso, G. L.; Musacchio, J. M. High-Affinity Dextromethorphan Binding Sites in Guinea Pig Brain. II. Competition Experiments Mol. Pharmacol. 1983, 23, 629-640
67. Dahlström, B.; Mellstrand, T.; Löfdahl, C. G. Pharmakokinetic Properties of Noscapine Eur. J. Clin. Pharmacol. 1982, 22, 535-539
68. Ashour, A.; Hegazy, M. A. M.; Moustafa, A. A.; Kelani, K. O.; Fattah, L. E. A. Validated Stability-Indicating TLC Method for the Determination of Noscapine Drug Test. Anal. 2009, 1, 327-338
69. Lettre, H.; Albrecht, M. Narcotin, Ein Mitosegift Naturwissenschaften 1942, 12, 184-185
70. Lettre, H. Synergists and Antagonists of Mitotic Poisons Ann. N. Y. Acad. Sci. 1954, 58, 1264-1275
71. Nicklas, R. B. How Cells Get the Right Chromosomes Science 1997, 275, 632-637
72. Langermann, J. V.; Lorenz, H.; Boehm, O.; Flemming, A.; Bernsdorf, A.; Kockerling, M.; Schinzer, Z.; Seidel-Morgenstern, A. (3 R∗,5′S∗)-6,7-Dimethoxy-3-(4′-methoxy-6′-methyl-5′,6′,7′,8′-tetrahydro-1,3-dioxolo[4,5-g]isoquinolin-5′-yl)isobenzofuran-1(3H)-one (Racemic A-Noscapine) Acta Crystallogr., Sect. E: Struct Rep. Online 2010, 66, o570-o570
73. Naik, P. K.; Chatterji, B. P.; Vangapandu, S. N.; Aneja, R.; Chandra, R.; Kanteveri, S.; Joshi, H. C. Rational Design, Synthesis and Biological Evaluations of Amino-Noscapine: A High Affinity Tubulin-Binding Noscapinoid J. Comput.-Aided Mol. Des. 2011, 25, 443-454
74. Naik, P. K.; Santoshi, S.; Rai, A.; Joshi, H. C. Molecular Modelling and Competition Binding Study of Br-Noscapine and Colchicine Provide Insight Into Noscapinoid-Tubulin Binding Site J. Mol. Graphics Modell. 2011, 29, 947-955
75. Alisaraie, L.; Tuszynski, J. A. Determination of Noscapine's Localization and Interaction with the Tubulin-A/B Heterodimer Chem. Biol. Drug Des. 2011, 78, 535-546
76. Zhou, J.; Gupta, K.; Aggarwal, S.; Aneja, R.; Chandra, R.; Panda, D.; Joshi, H. C. Brominated Derivatives of Noscapine Are Potent Microtubule-Interfering Agents That Perturb Mitosis and Inhibit Cell Proliferation Mol. Pharmacol. 2003, 63, 799-807
77. Jablonski, S. A.; Chan, G.; Cooke, C. A.; Earnshaw, W. C. The hBUB1 and hBUBR1 Kinases Sequentially Assemble onto Kinetochores During Prophase with hBUBR1 Concentrating at the Kinetochore Plates in Mitosis Chromosoma 1998, 107, 386-396
78. Shin, H.-J.; Baek, K.-H.; Jeon, A.-H.; Park, M.-T.; Lee, S.-J.; Kang, C.-M.; Lee, H.-S.; Yoo, S.-H.; Chung, D.-H.; Sung, Y.-C.; McKeon, F.; Lee, C.-W. Dual Roles of Human BubR1, a Mitotic Checkpoint Kinase, in the Monitoring of Chromosomal Instability Cancer Cell 2003, 4, 483-497
79. Biggins, S.; Murray, A. W. Sister Chromatid Cohesion in Mitosis Curr. Opin. Cell Biol. 1998, 10, 769-775
80. Sarrazin, M.; Briand, C.; Menendez, M.; Laynez, J. Mechanism of Binding of the New Antimitotic Drug MDL 27048 to the Colchicine Site of Tubulin: Equilibrium Studies Biochemistry 1992, 31, 11125-11132
81. Chakrabarti, G.; Sengupta, S.; Bhattacharyya, B. Thermodynamics of Colchicinoid-Tubulin Interactions J. Biol. Chem. 1996, 271, 2897-2901
82. Ray, K.; Bhattacharyya, B.; Biswas, B. B. Role of B-Ring of Colchicine in Its Binding to Tubulin J. Biol. Chem. 1981, 256, 6241-6244
83. Burger, P. C.; Jouvet, A.; Scheithauer, B. W. The 2007 WHO Classification of Tumours of the Central Nervous System Acta Neuropathol. 2007, 114, 97-109
84. Hofer, S.; Herrmann, R. Chemotherapy for Malignant Brain Tumors of Astrocytic and Oligodendroglial Lineage J. Cancer Res. Clin. Oncol. 2001, 127, 91-95
85. Landen, J. W.; Hau, V.; Wang, M.; Davis, T.; Ciliax, B.; Wainer, B. H.; Van Meir, E. G.; Glass, J. D.; Joshi, H. C.; Archer, D. R. Noscapine Crosses the Blood-Brain Barrier and Inhibits Glioblastoma Growth Clin. Cancer Res. 2004, 10, 5187-5201
86. Ashby, L. S.; Ryken, T. C. Management of Malignant Glioma: Steady Progress with Multimodal Approaches Neurosurg. Focus 2006, 20 (E3) 1-13
87. Stupp, R.; Mason, W. P.; van den Bent, M. J.; Weller, M.; Fisher, B.; Taphoorn, M. J. B.; Belanger, K.; Brandes, A. A.; Marosi, C.; Bogdahn, U.; Curschmann, J.; Janzer, R. C.; Ludwin, S. K.; Gorlia, T.; Allgeier, A.; Lacombe, D.; Cairncross, J. G.; Eisenhauer, E.; Mirimanoff, R. O. Radiotherapy Plus Concomitant and Adjuvant Temozolomide for Glioblastoma New Engl. J. Med. 2005, 352, 987-996
88. Lu, C.; Shervington, A. Chemoresistance in Gliomas Mol. Cell. Biochem. 2008, 312, 71-80
89. Jhaveri, N.; Cho, H.; Torres, S.; Wang, W.; Schönthal, A. H. Noscapine Inhibits Tumor Growth in TMZ-Resistant Gliomas Cancer Lett. 2011, 312, 245-252
90. Newcomb, E. W.; Lukyanov, Y.; Schnee, T.; Ali, M. A.; Lan, L.; Zagzag, D. Noscapine Inhibits Hypoxia-Mediated HIF-1alpha Expression and Angiogenesis in Vitro: A Novel Function for an Old Drug Int. J. Oncol. 2006, 28, 1121-1130
91. Chougule, M.; Patel, A. R.; Sachdeva, P.; Jackson, T.; Singh, M. Anticancer Activity of Noscapine, an Opioid Alkaloid in Combination with Cisplatin in Human Non-Small Cell Lung Cancer Lung Cancer 2011, 71, 271-282
92. Hiser, L.; Herrington, B.; Lobert, S. Effect of Noscapine and Vincristine Combination on Demyelination and Cell Proliferation in Vitro Leuk. Lymphoma 2008, 49, 1603-1609
93. Aneja, R.; Joshi, H. C.; Vandapandu, S.; Noscapine Analogs and their Use in Treating Cancers, Including Drug-Resistant Cancers. WO 2008/109609 A1, 2008.
94. Naik, P. K.; Lopus, M.; Aneja, R.; Vangapandu, S. N.; Joshi, H. C. In Silico Inspired Design and Synthesis of a Novel Tubulin-Binding Anti-Cancer Drug: Folate Conjugated Noscapine (Targetin) J. Comput.-Aided Mol. Des. 2012, 26, 233-247
95. Min/+ Mouse Model Int. J. Cancer 2012, 131, 1435-1444
96. Jackson, T.; Chougule, M. B.; Ichite, N.; Patlolla, R. R.; Singh, M. Antitumor Activity of Noscapine in Human Non-Small Cell Lung Cancer Xenograft Model Cancer Chemother. Pharmacol. 2008, 63, 117-126
97. Mita, A. C.; Mita, M. M.; Nawrocki, S. T.; Giles, F. J. Survivin: Key Regulator of Mitosis and Apoptosis and Novel Target for Cancer Therapeutics Clin. Cancer Res. 2008, 14, 5000-5005
98. Karna, P.; Sharp, S. M.; Yates, C.; Prakash, S.; Aneja, R. EM011 Activates a Survivin-Dependent Apoptotic Program in Human Non-Small Cell Lung Cancer Cells Mol. Cancer 2009, 8, 93
99. Li, S.; He, J.; Li, S.; Cao, G.; Tang, S.; Tong, Q.; Joshi, H. C. Noscapine Induced Apoptosis via Downregulation of Survivin in Human Neuroblastoma Cells Having Wild Type or Null P53 PLoS One 2012, 7, e40076
100. Aneja, R.; Ghaleb, A. M.; Zhou, J.; Yang, V. W.; Joshi, H. C. P53 and P21 Determine the Sensitivity of Noscapine-Induced Apoptosis in Colon Cancer Cells Cancer Res. 2007, 67, 3862-3870
101. Aneja, R.; Zhou, J.; Vangapandu, S. N.; Chandra, R.; Joshi, H. C. Drug-Resistant T-Lymphoid Tumors Undergo Apoptosis Selectively in Response to an Antimicrotubule Agent, EM011 Blood 2006, 107, 2486-2492
102. Aneja, R.; Miyagi, T.; Karna, P.; Ezell, T.; Shukla, D.; Vij Gupta, M.; Yates, C.; Chinni, S. R.; Zhau, H.; Chung, L. W. K.; Joshi, H. C. A Novel Microtubule-Modulating Agent Induces Mitochondrially Driven Caspase-Dependent Apoptosis via Mitotic Checkpoint Activation in Human Prostate Cancer Cells Eur. J. Cancer 2010, 46, 1668-1678
103. Karna, P.; Rida, P. C. G.; Pannu, V.; Gupta, K. K.; Dalton, W. B.; Joshi, H. C.; Yang, V. W.; Zhou, J.; Aneja, R. A Novel Microtubule-Modulating Noscapinoid Triggers Apoptosis by Inducing Spindle Multipolarity via Centrosome Amplification and Declustering Cell Death Differ. 2011, 18, 632-644
104. Aneja, R.; Kalia, V.; Ahmed, R.; Joshi, H. C. Nonimmunosuppressive Chemotherapy: EM011-Treated Mice Mount Normal T-Cell Responses to an Acute Lymphocytic Choriomeningitis Virus Infection Mol. Cancer Ther. 2007, 6, 2891-2899
105. Dey, B. B.; Srinivasan, T. K. Cotarnine series. IV. 5-Bromonarcotine, 5-Bromocotarnine, 5-Bromohydrocotarnine and 5-Bromonarceine and Their Derivatives J. Indian Chem. Soc. 1935, 12, 526-536
106. Aggarwal, S.; Ghosh, N. N.; Aneja, R.; Joshi, H. A Convenient Synthesis of Aryl-Substituted N-Carbamoyl/N-Thiocarbamoyl Narcotine and Related Compounds Helv. Chim. Acta 2002, 85, 2458-2462
107. Giannakakou, P.; Sackett, D. L.; Kang, Y. K.; Zhan, Z.; Buters, J. T. M.; Fojo, T.; Poruchynsky, M. S. Paclitaxel-Resistant Human Ovarian Cancer Cells Have Mutant B-Tubulins that Exhibit Impaired Paclitaxel-Driven Polymerization J. Biol. Chem. 1997, 272, 17118-17125
108. Pryor, D. E.; O'Brate, A.; Bilcer, G.; Díaz, J. F.; Wang, Y. The Microtubule Stabilizing Agent Laulimalide Does Not Bind in the Taxoid Site, Kills Cells Resistant to Paclitaxel and Epothilones, and May Not Require Its Epoxide Moiety for Activity Biochemistry 2002, 41, 9109-9115
109. Zughaier, S.; Karna, P.; Stephens, D.; Aneja, R. Potent Anti-Inflammatory Activity of Novel Microtubule-Modulating Brominated Noscapine Analogs PLoS One 2010, 5, e9165
110. Aneja, R.; Vangapandu, S. N.; Lopus, M. Synthesis of Microtubule-Interfering Halogenated Noscapine Analogs That Perturb Mitosis in Cancer Cells Followed by Cell Death Biochem. Pharmacol. 2006, 72, 415-426
111. Aneja, R.; Vangapandu, S. N.; Joshi, H. C. Synthesis and Biological Evaluation of a Cyclic Ether Fluorinated Noscapine Analog Bioorg. Med. Chem. 2006, 14, 8352-8258
112. Aneja, R.; Vangapandu, S. N.; Lopus, M.; Chandra, R.; Panda, D.; Joshi, H. C. Development of a Novel Nitro-Derivative of Noscapine for the Potential Treatment of Drug-Resistant Ovarian Cancer and T-Cell Lymphoma Mol. Pharmacol. 2006, 69, 1801-1809
113. Manchukonda, N. K.; Sridhar, B.; Naik, P. K.; Joshi, H. C. Copper(I) Mediated Facile Synthesis of Potent Tubulin Polymerization Inhibitor, 9-Amino-a-noscapine From Natural a-Noscapine Bioorg. Med. Chem. 2012, 22, 2983-2987
114. Santoshi, S.; Naik, P. K.; Joshi, H. C. Rational Design of Novel Anti-Microtubule Agent (9-Azido-noscapine) from Quantitative Structure Activity Relationship (QSAR) Evaluation of Noscapinoids J. Biomol. Screening 2011, 16, 1047-1058
115. Markiewicz, J. T.; Wiest, O.; Helquist, P. Synthesis of Primary Aryl Amines Through a Copper-Assisted Aromatic Substitution Reaction with Sodium Azide J. Org. Chem. 2010, 75, 4887-4890
116. Porcù, E.; Sipos, A.; Basso, G.; Hamel, E.; Bai, R.; Stempfer, V.; Udvardy, A.; Bényei, A. C.; Schmidhammer, H.; Antus, S.; Viola, G. Novel 9′-Substituted-Noscapines: Synthesis with Suzuki Cross-Coupling, Structure Elucidation and Biological Evaluation Eur. J. Med. Chem. 2014, 84, 476-490
117. Schmidhammer, H.; Klötzer, W. Neue Reaktionen an Phthalidisochinolinalkaloiden. Alkoxytauschreaktionen Und Isomerisierungen an A- Und B-Narcotin Arch. Pharm. 1978, 311, 664-671
118. Anderson, J. T.; Ting, A. E.; Boozer, S.; Brunden, K. R.; Danzig, J.; Dent, T.; Harrington, J. J.; Murphy, S. M.; Perry, R.; Raber, A.; Rundlett, S. E.; Wang, J.; Wang, N.; Bennani, Y. L. Discovery of S-Phase Arresting Agents Derived From Noscapine J. Med. Chem. 2005, 48, 2756-2758
119. Anderson, J. T.; Ting, A. E.; Boozer, S.; Brunden, K. R.; Crumrine, C.; Danzig, J.; Dent, T.; Faga, L.; Harrington, J. J.; Hodnick, W. F.; Murphy, S. M.; Pawlowski, G.; Perry, R.; Raber, A.; Rundlett, S. E.; Stricker-Krongrad, A.; Wang, J.; Bennani, Y. L. Identification of Novel and Improved Antimitotic Agents Derived From Noscapine J. Med. Chem. 2005, 48, 7096-7098
120. Mishra, R. C.; Karna, P.; Gundala, S. R.; Pannu, V.; Stanton, R.; Gupta, K. K.; Robinson, H. M.; Lopus, M.; Wilson, L.; Henary, M. Second Generation Benzofuranone Ring Substituted Noscapine Analogs: Synthesis and Biological Evaluation Biochem. Pharmacol. 2011, 82, 110-121
121. Ray, S.; Chaturvedi, D. Application of Organic Carbamates in Drug Design. Part 1: Anticancer Agents-Recent Reports Drugs Future 2004, 29, 343
122. Altieri, D. C. Survivin, Versatile Modulation of Cell Division and Apoptosis in Cancer Oncogene 2003, 22, 8581-8589
123. Oosawa, F.; Asakura, S. Thermodynamics of the Polymerization of Protein; Academic Press: London, New York, 1975.
124. Bennani, Y. L.; Gu, W.; Canales, A.; Díaz, F. J.; Eustace, B. K.; Hoover, R. R.; Jiménez-Barbero, J.; Nezami, A.; Wang, T. Tubulin Binding, Protein-Bound Conformation in Solution, and Antimitotic Cellular Profiling of Noscapine and Its Derivatives J. Med. Chem. 2012, 55, 1920-1925
125. Braun, J. V. Die Aufspaltung Cyclischer Basen Durch Bromcyan Ber. Dtsch. Chem. Ges. 1909, 42, 2035-2057
126. Grierson, D. The Polonovski Reaction Org. React. 2004, 39, 85-295
127. Allen, A. C.; Cooper, D. A.; Moore, J. M.; Gloger, M. Illicit Heroin Manufacturing By-Products: Capillary Gas Chromatographic Determination and Structural Elucidation of Narcotine- and Norlaudanosine-Related Compounds Anal. Chem. 1984, 56, 2940-2947
128. McCamley, K.; Ripper, J. A.; Singer, R. D. Efficient N-Demethylation of Opiate Alkaloids Using a Modified Nonclassical Polonovski Reaction J. Org. Chem. 2003, 68, 9847-9850
129. Dong, Z.; Scammells, P. J. New Methodology for the N-Demethylation of Opiate Alkaloids J. Org. Chem. 2007, 72, 9881-9885
130. Kok, G.; Ashton, T. D.; Scammells, P. J. An Improved Process for the N-Demethylation of Opiate Alkaloids Using an Iron(II) Catalyst in Acetate Buffer Adv. Synth. Catal. 2009, 351, 283-286
131. Kok, G.; Scammells, P. Polonovski-Type N-Demethylation of N-Methyl Alkaloids Using Substituted Ferrocene Redox Catalysts Synthesis 2012, 44, 2587-2594
132. Debono, A. J.; Xie, J. H.; Ventura, S.; Pouton, C. W.; Capuano, B.; Scammells, P. J. Synthesis and Biological Evaluation of N-Substituted Noscapine Analogues ChemMedChem 2012, 7, 2122-2133
133. Aggarwal, S.; Ghosh, N. N.; Aneja, R. Mass Spectral Studies on Aryl-Substituted N-Carbamoyl/N-Thiocarbamoyl Narcotine and Related Compounds Rapid Commun. Mass Spectrom. 2002, 16, 923-928
134. Manchukonda, N. K.; Naik, P. K.; Santoshi, S.; Lopus, M.; Joseph, S.; Sridhar, B.; Kantevari, S. Rational Design, Synthesis, and Biological Evaluation of Third Generation A-Noscapine Analogues as Potent Tubulin Binding Anti-Cancer Agents PLoS One 2013, 8, e77970
135. Henary, M.; Narayana, L.; Ahad, S.; Gundala, S. R.; Mukkavilli, R.; Sharma, V.; Owens, E. A.; Yadav, Y.; Nagaraju, M.; Hamelberg, D.; Tandon, V.; Panda, D.; Aneja, R. Novel Third-Generation Water-Soluble Noscapine Analogs as Superior Microtubule-Interfering Agents with Enhanced Antiproliferative Activity Biochem. Pharmacol. 2014, 92, 192-205
136. Debono, A. J.; Mistry, S. J.; Xie, J.; Muthiah, D.; Phillips, J.; Ventura, S.; Callaghan, R.; Pouton, C. W.; Capuano, B.; Scammells, P. J. The Synthesis and Biological Evaluation of Multifunctionalised Derivatives of Noscapine as Cytotoxic Agents ChemMedChem 2014, 9, 399-410
137. Verma, A. K.; Jha, R. R.; Chaudhary, R. 2-(1-Benzotriazolyl)pyridine: A Robust Bidentate Ligand for the Palladium-Catalyzed C-C (Suzuki, Heck, Fujiwara-Moritani, Sonogashira), C-N and C-S Coupling Reactions Adv. Synth. Catal. 2013, 355, 421-438
138. Woodahl, E. L.; Crouthamel, M. H.; Bui, T.; Shen, D. D.; Ho, R. J. Y. MDR1 (ABCB1) G1199A (Ser400Asn) Polymorphism Alters Transepithelial Permeability and Sensitivity to Anticancer Agents Cancer Chemother. Pharmacol. 2009, 64, 183-188
139. Limtrakul, P.; Chearwae, W.; Shukla, S.; Phisalphong, C.; Ambudkar, S. V. Modulation of Function of Three ABC Drug Transporters, P-Glycoprotein (ABCB1), Mitoxantrone Resistance Protein (ABCG2) and Multidrug Resistance Protein 1 (ABCC1) by Tetrahydrocurcumin, a Major Metabolite of Curcumin Mol. Cell. Biochem. 2007, 296, 85-95
140. Wetzel, S.; Bon, R. S.; Kumar, K.; Waldmann, H. Biology-Oriented Synthesis Angew. Chem., Int. Ed. 2011, 50, 10800-10826
141. Kumar, K.; Waldmann, H. Synthesis of Natural Product Inspired Compound Collections Angew. Chem., Int. Ed. 2009, 48, 3224-3242
142. Vetter, I. R.; Waldmann, H. From Protein Domains to Drug Candidates-Natural Products as Guiding Principles in the Design and Synthesis of Compound Libraries Angew. Chem., Int. Ed. 2002, 41, 2878-2890
143. Zimmermann, T. J.; Roy, S.; Martinez, N. E.; Ziegler, S. Biology-Oriented Synthesis of a Tetrahydroisoquinoline-Based Compound Collection Targeting Microtubule Polymerization ChemBioChem 2013, 14, 295-300
144. Flynn, D. L.; Zelle, R. E.; Grieco, P. A. A Mild Two-Step Method for the Hydrolysis of Lactams and Secondary Amides J. Org. Chem. 1983, 48, 2424-2426
145. Taylor, A. M.; Schreiber, S. L. Enantioselective Addition of Terminal Alkynes to Isolated Isoquinoline Iminiums Org. Lett. 2006, 8, 143-146
146. Aneja, R.; Mishra, R. C. Synthesis and Characterization of Second Generation Benzofuranone Ring Substituted Noscapine Analogs. US 2014/0121233 A1, 2014.
147. Tripathi, M.; Reddy, P. L.; Rawat, D. S. Noscapine and its Analogues as Anti-Cancer Agents J. Chem. Biol. Interfaces 2014, 4, 1-22