New chemical scaffolds for human African trypanosomiasis lead discovery from a screen of tyrosine kinase inhibitor drugs

Antimicrobial Agents and Chemotherapy

Volumn 58, Issue 4, 2014, Pages 2202-2210

  Behera, Ranjan ^a   Thomas, Sarah M ^a   Mensa Wilmot, Kojo ^a  

^a UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 ANILINOQUINAZOLINE; 6 (4 HYDROXYPHENYL) 4 (ALPHA METHYLBENZYLAMINO) 7H PYRROLO[2,3 D]PYRIMIDINE; 6 [4 (4 ETHYL 1 PIPERAZINYLMETHYL)PHENYL] 4 (ALPHA METHYLBENZYLAMINO) 7H PYRROLO[2,3 D]PYRIMIDINE; AXITINIB; CANERTINIB; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ERLOTINIB; IMATINIB; LAPATINIB; PENTAMIDINE; PLATELET DERIVED GROWTH FACTOR RECEPTOR; PYRROLOPYRIMIDINE DERIVATIVE; QUINAZOLINE DERIVATIVE; SUNITINIB; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR;

AFRICAN TRYPANOSOMIASIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DEATH; CELL DENSITY; CELL KILLING; CONTROLLED STUDY; DRUG BIOAVAILABILITY; DRUG BLOOD LEVEL; DRUG CYTOTOXICITY; DRUG EFFICACY; DRUG EXPOSURE; DRUG INHIBITION; DRUG SCREENING; DRUG SENSITIVITY; FEMALE; GROWTH INHIBITION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PARASITEMIA; PRIORITY JOURNAL; SURVIVAL; TRYPANOSOMA;

ANIMALS; BENZAMIDES; FEMALE; HELA CELLS; HUMANS; IMIDAZOLES; INDAZOLES; INDOLES; MICE; MORPHOLINES; PIPERAZINES; PROTEIN KINASE INHIBITORS; PURINES; PYRIMIDINES; PYRROLES; QUINAZOLINES; TRYPANOSOMIASIS, AFRICAN;

EID: 84896944261     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.01691-13     Document Type: Article

References (64)

1. Croft SL, Barrett MP, Urbina JA. 2005. Chemotherapy of trypanosomiases and leishmaniasis. Trends Parasitol. 21:508-512. http://dx.doi.org/10.1016/j.pt. 2005.08.026. (Pubitemid 41447021)
2. Renslo AR, McKerrow JH. 2006. Drug discovery and development for neglected parasitic diseases. Nat. Chem. Biol. 2:701-710. http://dx.doi.org/10. 1038/nchembio837. (Pubitemid 44764212)
3. McKerrow JH. 1996. Parasitic infections-molecular diagnosis and rational drug design. Biologicals 24:207-208. http://dx.doi.org/10.1006/biol.1996.0028. (Pubitemid 27023384)
4. Barrett MP, Mottram JC, Coombs GH. 1999. Recent advances in identifying and validating drug targets in trypanosomes and leishmanias. Trends Microbiol. 7:82-88. http://dx.doi.org/10.1016/S0966-842X(98)01433-4. (Pubitemid 29273940)
5. Hammarton TC, Mottram JC, Doerig C. 2003. The cell cycle of parasitic protozoa: potential for chemotherapeutic exploitation. Prog. Cell Cycle Res. 5:91-101.
6. Hopkins AL, Groom CR. 2002. The druggable genome. Nat. Rev. Drug Discov. 1:727-730. http://dx.doi.org/10.1038/nrd892. (Pubitemid 37361545)
7. Hardy LW, Peet NP. 2004. The multiple orthogonal tools approach to define molecular causation in the validation of druggable targets. Drug Discov. Today 9:117-126. http://dx.doi.org/10.1016/S1359-6446(03)02969-6. (Pubitemid 38198310)
8. Pink R, Hudson A, Mouriès MA, Bendig M. 2005. Opportunities and challenges in antiparasitic drug discovery. Nat. Rev. Drug Discov. 4:727-740. http://dx.doi.org/10.1038/nrd1824. (Pubitemid 43090494)
9. Jacobs RT, Nare B, Phillips MA. 2011. State of the art in African trypanosome drug discovery. Curr. Top. Med. Chem. 11:1255-1274. http://dx.doi.org/10.2174/156802611795429167.
10. Gelb MH, Van Voorhis WC, Buckner FS, Yokoyama K, Eastman R, Carpenter EP, Panethymitaki C, Brown KA, Smith DF. 2003. Protein farnesyl and N-myristoyl transferases: piggy-back medicinal chemistry targets for the development of antitrypanosomatid and antimalarial therapeutics. Mol. Biochem. Parasitol. 126:155-163. http://dx.doi.org/10.1016/S0166-6851(02)00282-7. (Pubitemid 36255614)
11. Gelb MH, Hol WG. 2002. Parasitology. Drugs to combat tropical protozoan parasites. Science 297:343-344. http://dx.doi.org/10.1126/science.1073126. (Pubitemid 34790750)
12. Pollastri MP, Campbell RK. 2011. Target repurposing for neglected diseases. Future Med. Chem. 3:1307-1315. http://dx.doi.org/10.4155/fmc.11.92.
13. Johnson LN. 2009. Protein kinase inhibitors: contributions from structure to clinical compounds. Q. Rev. Biophys. 42:1-40. http://dx.doi.org/10.1017/ S0033583508004745.
14. Sebolt-Leopold JS, English JM. 2006. Mechanisms of drug inhibition of signalling molecules. Nature 441:457-462. http://dx.doi.org/10.1038/nature04874. (Pubitemid 44050141)
15. Levitzki A, Mishani E. 2006. Tyrphostins and other tyrosine kinase inhibitors. Annu. Rev. Biochem. 75:93-109. http://dx.doi.org/10.1146/annurev. biochem.75.103004.142657. (Pubitemid 44118027)
16. Bhagwat M, Aravind L. 2007. PSI-BLAST tutorial. Methods Mol. Biol. 395:177-186. http://dx.doi.org/10.1007/978-1-59745-514-5-10. (Pubitemid 350183294)
17. Osherov N, Levitzki A. 1994. Epidermal-growth-factor-dependent activation of the src-family kinases. Eur. J. Biochem. 225:1047-1053. http://dx.doi.org/ 10.1111/j.1432-1033.1994.1047b.x.
18. Zhu XF, Liu ZC, Xie BF, Li ZM, Feng GK, Yang D, Zeng YX. 2001. EGFR tyrosine kinase inhibitor AG1478 inhibits cell proliferation and arrests cell cycle in nasopharyngeal carcinoma cells. Cancer Lett. 169:27-32. http://dx.doi.org/10.1016/S0304-3835(01)00547-X. (Pubitemid 32532093)
19. Grünwald V, Hidalgo M. 2003. Development of the epidermal growth factor receptor inhibitor OSI-774. Semin. Oncol. 30(3 Suppl 6):23-31. http://dx.doi.org/10.1016/S0093-7754(03)70022-0. (Pubitemid 36712856)
20. Lackey KE. 2006. Lessons from the drug discovery of lapatinib, a dual ErbB1/2 tyrosine kinase inhibitor. Curr. Top. Med. Chem. 6:435-460. http://dx.doi.org/10.2174/156802606776743156.
21. Xia W, Mullin RJ, Keith BR, Liu LH, Ma H, Rusnak DW, Owens G, Alligood KJ, Spector NL. 2002. Anti-tumor activity of GW572016: a dual tyrosine kinase inhibitor blocks EGF activation of EGFR/erbB2 and downstream Erk1/2 and AKT pathways. Oncogene 21:6255-6263. http://dx.doi.org/10.1038/sj.onc.1205794.
22. Katiyar S, Kufareva I, Behera R, Thomas SM, Ogata Y, Pollastri M, Abagyan R, Mensa-Wilmot K. 2013. Lapatinib-binding protein kinases in the African trypanosome: identification of cellular targets for kinase-directed chemical scaffolds. PLoS One 8:e56150. http://dx.doi.org/10.1371/journal.pone.0056150.
23. Subramanya S, Mensa-Wilmot K. 2010. Diacylglycerol-stimulated endocytosis of transferrin in trypanosomatids is dependent on tyrosine kinase activity. PLoS One 5:e8538. http://dx.doi.org/10.1371/journal.pone.0008538.
24. Subramanya S, Hardin CF, Steverding D, Mensa-Wilmot K. 2009. Glycosylphosphatidylinositol-specific phospholipaseCregulates transferrin endocytosis in the African trypanosome. Biochem. J. 417:685-694. http://dx.doi.org/10.1042/BJ20080167.
25. Traxler P, Allegrini PR, Brandt R, Brueggen J, Cozens R, Fabbro D, Grosios K, Lane HA, McSheehy P, Mestan J, Meyer T, Tang C, Wartmann M, Wood J, Caravatti G. 2004. AEE788: a dual family epidermal growth factor receptor/ErbB2 and vascular endothelial growth factor receptor tyrosine kinase inhibitor with antitumor and antiangiogenic activity. Cancer Res. 64:4931-4941. http://dx.doi.org/10.1158/0008-5472.CAN-03-3681. (Pubitemid 38924540)
26. Slichenmyer WJ, Elliott WL, Fry DW. 2001. CI-1033, a pan-erbB tyrosine kinase inhibitor. Semin. Oncol. 28(5 Suppl 16):80-85. http://dx.doi.org/10.1016/ S0093-7754(01)90285-4. (Pubitemid 33065113)
27. Allen LF, Lenehan PF, Eiseman IA, Elliott WL, Fry DW. 2002. Potential benefits of the irreversible pan-erbB inhibitor, CI-1033, in the treatment of breast cancer. Semin. Oncol. 29(3 Suppl 11):11-21. http://dx.doi.org/10.1016/ S0093-7754(02)70122-X. (Pubitemid 34816061)
28. Patel G, Karver CE, Behera R, Guyett PJ, Sullenberger C, Edwards P, Roncal NE, Mensa-Wilmot K, Pollastri MP. 2013. Kinase scaffold repurposing for neglected disease drug discovery: discovery of an efficacious, lapatinib-derived lead compound for trypanosomiasis. J. Med. Chem. 56:3820-3832. http://dx.doi.org/10.1021/jm400349k.
29. Hirumi H, Hirumi K. 1994. Axenic culture of African trypanosome bloodstream forms. Parasitol. Today 10:80-84. http://dx.doi.org/10.1016/0169- 4758(94)90402-2. (Pubitemid 24052922)
30. Smaill JB, Showalter HD, Zhou H, Bridges AJ, McNamara DJ, Fry DW, Nelson JM, Sherwood V, Vincent PW, Roberts BJ, Elliott WL, Denny WA. 2001. Tyrosine kinase inhibitors. 18. 6-Substituted 4-anilinoquinazolines and 4-anilinopyrido[3,4-d]pyrimidines as soluble, irreversible inhibitors of the epidermal growth factor receptor. J. Med. Chem. 44:429-440. http://dx.doi.org/ 10.1021/jm000372i. (Pubitemid 32113588)
31. Mellinghoff IK, Tran C, Sawyers CL. 2002. Growth inhibitory effects of the dual ErbB1/ErbB2 tyrosine kinase inhibitor PKI-166 on human prostate cancer xenografts. Cancer Res. 62:5254-5259. (Pubitemid 35024599)
32. Bruns CJ, Solorzano CC, Harbison MT, Ozawa S, Tsan R, Fan D, Abbruzzese J, Traxler P, Buchdunger E, Radinsky R, Fidler IJ. 2000. Blockade of the epidermal growth factor receptor signaling by a novel tyrosine kinase inhibitor leads to apoptosis of endothelial cells and therapy of human pancreatic carcinoma. Cancer Res. 60:2926-2935. (Pubitemid 30395817)
33. Abrams TJ, Lee LB, Murray LJ, Pryer NK, Cherrington JM. 2003. SU11248 inhibits KIT and platelet-derived growth factor receptor beta in preclinical models of human small cell lung cancer. Mol. Cancer Ther. 2:471-478.
34. Mendel DB, Laird AD, Xin X, Louie SG, Christensen JG, Li G, Schreck RE, Abrams TJ, Ngai TJ, Lee LB, Murray LJ, Carver J, Chan E, Moss KG, Haznedar JO, Sukbuntherng J, Blake RA, Sun L, Tang C, Miller T, Shirazian S, McMahon G, Cherrington JM. 2003. In vivo antitumor activity of SU11248, a novel tyrosine kinase inhibitor targeting vascular endothelial growth factor and platelet-derived growth factor receptors: determination of a pharmacokinetic/pharmacodynamic relationship. Clin. Cancer Res. 9:327-337. (Pubitemid 36109749)
35. Rugo HS, Herbst RS, Liu G, Park JW, Kies MS, Steinfeldt HM, Pithavala YK, Reich SD, Freddo JL, Wilding G. 2005. Phase I trial of the oral antiangiogenesis agent AG-013736 in patients with advanced solid tumors: pharmacokinetic and clinical results. J. Clin. Oncol. 23:5474-5483. http://dx.doi.org/10.1200/JCO.2005.04.192.
36. Schindler T, Bornmann W, Pellicena P, Miller WT, Clarkson B, Kuriyan J. 2000. Structural mechanism for STI-571 inhibition of Abelson tyrosine kinase. Science 289:1938-1942. http://dx.doi.org/10.1126/science.289.5486.1938.
37. Fang G, Kim CN, Perkins CL, Ramadevi N, Winton E, Wittmann S, Bhalla KN. 2000. CGP57148B (STI-571) induces differentiation and apoptosis and sensitizes Bcr-Abl-positive human leukemia cells to apoptosis due to antileukemic drugs. Blood 96:2246-2253.
38. Nwaka S, Ramirez B, Brun R, Maes L, Douglas F, Ridley R. 2009. Advancing drug innovation for neglected diseases - criteria for lead progression. PLoS Negl. Trop. Dis. 3:e440. http://dx.doi.org/10.1371/journal.pntd.0000440.
39. Bai F, Freeman BB, III, Fraga CH, Fouladi M, Stewart CF. 2006. Determination of lapatinib (GW572016) in human plasma by liquid chromatography electrospray tandem mass spectrometry (LC-ESI-MS/MS). J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 831:169-175. http://dx.doi.org/10.1016/j.jchromb. 2005.11.044. (Pubitemid 43155792)
40. Midgley RS, Kerr DJ, Flaherty KT, Stevenson JP, Pratap SE, Koch KM, Smith DA, Versola M, Fleming RA, Ward C, O'Dwyer PJ, Middleton MR. 2007. A phase I and pharmacokinetic study of lapatinib in combination with infusional 5-fluorouracil, leucovorin and irinotecan. Ann. Oncol. 18:2025-2029. (Pubitemid 350286244)
41. Calvo E, Tolcher AW, Hammond LA, Patnaik A, de Bono JS, Eiseman IA, Olson SC, Lenehan PF, McCreery H, Lorusso P, Rowinsky EK. 2004. Administration of CI-1033, an irreversible pan-erbB tyrosine kinase inhibitor, is feasible on a 7-day on, 7-day off schedule: a phase I pharmacokinetic and food effect study. Clin. Cancer Res. 10:7112-7120. http://dx.doi.org/10.1158/1078-0432.CCR-04-1187. (Pubitemid 39487694)
42. Ellis AG, Doherty MM, Walker F, Weinstock J, Nerrie M, Vitali A, Murphy R, Johns TG, Scott AM, Levitzki A, McLachlan G, Webster LK, Burgess AW, Nice EC. 2006. Preclinical analysis of the analinoquinazoline AG1478, a specific small molecule inhibitor of EGF receptor tyrosine kinase. Biochem. Pharmacol. 71:1422-1434. http://dx.doi.org/10.1016/j.bcp.2006.01.020.
43. Nakagawa K, Minami H, Kanezaki M, Mukaiyama A, Minamide Y, Uejima H, Kurata T, Nogami T, Kawada K, Mukai H, Sasaki Y, Fukuoka M. 2009. Phase I dose-escalation and pharmacokinetic trial of lapatinib (GW572016), a selective oral dual inhibitor of ErbB-1 and -2 tyrosine kinases, in Japanese patients with solid tumors. Jpn. J. Clin. Oncol. 39:116-123. http://dx.doi.org/10.1093/jjco/ hyn135.
44. Hudachek SF, Gustafson DL. 2013. Physiologically based pharmacokinetic model of lapatinib developed in mice and scaled to humans. J. Pharmacokinet. Pharmacodyn. 40:157-176. http://dx.doi.org/10.1007/s10928-012-9295-8.
45. Simon GR, Garrett CR, Olson SC, Langevin M, Eiseman IA, Mahany JJ, Williams CC, Lush R, Daud A, Munster P, Chiappori A, Fishman M, Bepler G, Lenehan PF, Sullivan DM. 2006. Increased bioavailability of intravenous versus oral CI-1033, a pan erbB tyrosine kinase inhibitor: results of a phase I pharmacokinetic study. Clin. Cancer Res. 12:4645-4651. http://dx.doi.org/10. 1158/1078-0432.CCR-05-2379. (Pubitemid 44297817)
46. Jakobsen PH, Wang MW, Nwaka S. 2011. Innovative partnerships for drug discovery against neglected diseases. PLoS Negl. Trop. Dis. 5:e1221. http://dx.doi.org/10.1371/journal.pntd.0001221.
47. DiMasi JA, Hansen RW, Grabowski HG. 2003. The price of innovation: new estimates of drug development costs. J. Health Econ. 22:151-185. http://dx.doi.org/10.1016/S0167-6296(02)00126-1. (Pubitemid 36279392)
48. Ochiana SO, Pandarinath V, Wang Z, Kapoor R, Ondrechen MJ, Ruben L, Pollastri MP. 2013. The human Aurora kinase inhibitor danusertib is a lead compound for anti-trypanosomal drug discovery via target repurposing. Eur. J. Med. Chem. 62:777-784. http://dx.doi.org/10.1016/j.ejmech.2012.07.038.
49. Field MC. 2009. Drug screening by crossing membranes: a novel approach to identification of trypanocides. Biochem. J. 419:e1-e3. http://dx.doi.org/10. 1042/BJ20090283.
50. Patham B, Duffy J, Lane A, Davis RC, Wipf P, Fewell SW, Brodsky JL, Mensa-Wilmot K. 2009. Post-translational import of protein into the endoplasmic reticulum of a trypanosome: an in vitro system for discovery of anti-trypanosomal chemical entities. Biochem. J. 419:507-517. http://dx.doi.org/10.1042/BJ20081787.
51. Steverding D. 2000. The transferrin receptor of Trypanosoma brucei. Parasitol. Int. 48:191-198. http://dx.doi.org/10.1016/S1383-5769(99)00018-5.
52. Brose N, Betz A, Wegmeyer H. 2004. Divergent and convergent signaling by the diacylglycerol second messenger pathway in mammals. Curr. Opin. Neurobiol. 14:328-340. http://dx.doi.org/10.1016/j.conb.2004.05.006. (Pubitemid 38759863)
53. Baselga J. 2006. Targeting tyrosine kinases in cancer: the second wave. Science 312:1175-1178. http://dx.doi.org/10.1126/science.1125951. (Pubitemid 43801135)
54. Wood ER, Truesdale AT, McDonald OB, Yuan D, Hassell A, Dickerson SH, Ellis B, Pennisi C, Horne E, Lackey K, Alligood KJ, Rusnak DW, Gilmer TM, Shewchuk L. 2004. A unique structure for epidermal growth factor receptor bound to GW572016 (Lapatinib): relationships among protein conformation, inhibitor off-rate, and receptor activity in tumor cells. Cancer Res. 64:6652-6659. http://dx.doi.org/10.1158/0008-5472.CAN-04-1168. (Pubitemid 39297926)
55. Urbaniak MD. 2009. Casein kinase 1 isoform 2 is essential for bloodstream form Trypanosoma brucei. Mol. Biochem. Parasitol. 166:183-185. http://dx.doi.org/10.1016/j.molbiopara.2009.03.001.
56. Li Z, Umeyama T, Wang CC. 2008. The chromosomal passenger complex and a mitotic kinesin interact with the Tousled-like kinase in trypanosomes to regulate mitosis and cytokinesis. PLoS One 3:e3814. http://dx.doi.org/10.1371/ journal.pone.0003814.
57. Ojo KK, Gillespie JR, Riechers AJ, Napuli AJ, Verlinde CL, Buckner FS, Gelb MH, Domostoj MM, Wells SJ, Scheer A, Wells TN, Van Voorhis WC. 2008. Glycogen synthase kinase 3 is a potential drug target for African trypanosomiasis therapy. Antimicrob. Agents Chemother. 52:3710-3717. http://dx.doi.org/10.1128/AAC.00364-08.
58. Lippa B, Pan G, Corbett M, Li C, Kauffman GS, Pandit J, Robinson S, Wei L, Kozina E, Marr ES, Borzillo G, Knauth E, Barbacci-Tobin EG, Vincent P, Troutman M, Baker D, Rajamohan F, Kakar S, Clark T, Morris J. 2008. Synthesis and structure based optimization of novel Akt inhibitors. Bioorg. Med. Chem. Lett. 18:3359-3363. http://dx.doi.org/10.1016/j.bmcl.2008.04.034. (Pubitemid 351718323)
59. Clark MP, George KM, Bookland RG, Chen J, Laughlin SK, Thakur KD, Lee W, Davis JR, Cabrera EJ, Brugel TA, VanRens JC, Laufersweiler MJ, Maier JA, Sabat MP, Golebiowski A, Easwaran V, Webster ME, De B, Zhang G. 2007. Development of new pyrrolopyrimidine-based inhibitors of Janus kinase 3 (JAK3). Bioorg. Med. Chem. Lett. 17:1250-1253. http://dx.doi.org/10.1016/j.bmcl.2006.12.018. (Pubitemid 46240854)
60. Blake JF, Kallan NC, Xiao D, Xu R, Bencsik JR, Skelton NJ, Spencer KL, Mitchell IS, Woessner RD, Gloor SL, Risom T, Gross SD, Martinson M, Morales TH, Vigers GP, Brandhuber BJ. 2010. Discovery of pyrrolopyrimidine inhibitors of Akt. Bioorg. Med. Chem. Lett. 20:5607-5612. http://dx.doi.org/10.1016/j.bmcl. 2010.08.053.
61. Polli JW, Humphreys JE, Harmon KA, Castellino S, O'Mara MJ, Olson KL, John-Williams LS, Koch KM, Serabjit-Singh CJ. 2008. The role of efflux and uptake transporters in [N-{3-chloro-4-[(3-fluorobenzyl)oxy-]phenyl}-6-[5-({[2- (methylsulfonyl)ethyl]amino}methyl)-2-furyl]-4-quinazolinamine (GW572016, lapatinib) disposition and drug interactions. Drug Metab. Dispos. 36:695-701. http://dx.doi.org/10.1124/dmd.107.018374. (Pubitemid 351468376)
62. Gluck S, Castrellon A. 2009. Lapatinib plus capecitabine resolved human epidermal growth factor receptor 2-positive brain metastases. Am. J. Ther. 16:585-590. http://dx.doi.org/10.1097/MJT.0b013e31818bee2b.
63. Meco D, Servidei T, Zannoni GF, Martinelli E, Prisco MG, de Waure C, Riccardi R. 2010. Dual inhibitor AEE788 reduces tumor growth in preclinical models of medulloblastoma. Transl. Oncol. 3:326-335.
64. Berezowska S, Diermeier-Daucher S, Brockhoff G, Busch R, Duyster J, Grosu AL, Schlegel J. 2010. Effect of additional inhibition of human epidermal growth factor receptor 2 with the bispecific tyrosine kinase inhibitor AEE788 on the resistance to specific EGFR inhibition in glioma cells. Int. J. Mol. Med. 26:713-721. http://dx.doi.org/10.3892/ijmm-00000518.