MONOCLONAL ANTIBODIES IN HIGH-GRADE GLIOMAS

Cover Page


Cite item

Full Text

Abstract

The review is devoted to a relatively young direction in therapy of malignant gliomas, which is based on applying monoclonal antibodies against tumour-associated antigens. The current data on efficacy of main therapeutic agents in clinical practice or clinical trials concerning high-grade gliomas, especially glioblastoma multiforme, is summarized. Of particular interest is bevacizumab, a humanized monoclonal antibody against vascular endothelial growth factor (anti-VEGF), which is widely used in glioblastoma. Major clinical trials devoted to bevacizumab monotherapy and combinations of bevacizumab with other therapeutic modalities in primary and recurrent glioblastoma conducted since 2006 till now are reviewed. The results of experimental and clinical application of monoclonal antibodies against epidermal growth factor receptor (EGFR) and its mutant variant EGFRvIII are analyzed, showing the most significant clinical effectiveness of nimotuzumab — a humanized monoclonal antibody. Significant part of the review is devoted to discussion of experimental and clinical data concerning efficacy of antibodies against VEGF receptor 2, platelet-derived growth factor receptor α, hepatocyte growth factor and its receptor c-Met. Unbiassed analysis of clinical trials on monoclonal antibodies does not allow us to conclude that passive immunotherapy directed against antigens listed above can significantly improve the overall survival of patients suffering from glioblastoma multiforme. This finding has encouraged us to mention several alternative approaches to passive immunotherapy and to list several prospective antigens for developing monoclonal antibodies.

 

About the authors

I. V. Chekhonin

Lomonosov Moscow State University, Russian Federation

Author for correspondence.
Email: Ivan-Chekhonin@yandex.ru
студент факультета фундаментальной медицины Московского государственного уни- верситета им. М.В.Ломоносова Адрес: 119192, Москва, Ломоносовский пр-т, д. 31, корп. 5, тел.: +7 (495) 637-15-06 Russian Federation

A. V. Leopol'd

Pirogov Russian National Scientific Medical University, Moscow, Russian Federation
Serbsky State Scientific Centre of Social and Forensic Psychiatry, Moscow, Russian Federation

Email: annavleopold@yandex.ru
кандидат биологических наук, научный сотрудник лаборатории иммунохимии отдела фундаментальной и прикладной нейробиологии ГНЦ социальной и судебной психиатрии им. В.П. Сербского Адрес: 119991, ГСП-2, Москва, Кропоткинский пер., д. 23, тел.: +7 (495) 695-02-62 Russian Federation

O. I. Gurina

Serbsky State Scientific Centre of Social and Forensic Psychiatry, Moscow, Russian Federation

Email: olga672@yandex.ru
доктор медицинских наук, профессор, руководитель лаборатории нейрохимии отдела фун- даментальной и прикладной нейробиологии ГНЦ социальной и судебной психиатрии им. В.П. Сербского Адрес: 119991, ГСП-2, Москва, Кропоткинский пер., д. 23, тел.: +7 (495) 637-15-06 Russian Federation

A. V. Semenova

Serbsky State Scientific Centre of Social and Forensic Psychiatry, Moscow, Russian Federation

Email: Anna-serbsky@yandex.ru
кандидат медицинских наук, старший научный сотрудник лаборатории иммунохимии отдела фундаментальной и прикладной нейробиологии ГНЦ социальной и судебной психиатрии им. В.П. Серб- ского Адрес: 119991, ГСП-2, Москва, Кропоткинский пер., д. 23, тел.: +7 (495) 695-02-62 Russian Federation

References

  1. Wen P.Y., Kesari S. N. Engl. J. Med. 2008; 359 (5): 492–507.
  2. Hou L.C., Veeravagu A., Hsu A.R., Tse V.C. Neurosurg. Focus. 2006; 20 (4): 5.
  3. Kohler G., Milstein C. Nature. 1975; 256 (5517): 495–497.
  4. Modjtahedi H., Ali S., Essapen S. Br. Med. Bull. 2012; 104: 41–59.
  5. Hwang W.Y., Foote J. Methods. 2005; 36 (1): 3–10.
  6. Lonberg N. Curr Opin Immunol. 2008; 20 (4): 450–459.
  7. Gedeon P.C., Choi B.D., Hodges T.R., Mitchell D.A., Big-ner D.D., Sampson J.H. Exp. Rev. Clin. Pharmacol. 2013; 6 (4): 375–386.
  8. Stockmeyer B., Elsasser D., Dechant M., Repp R., Gramatzki M., Glennie M.J., van de Winkel J.G., Valerius T. J. Imm. Methods. 2001; 248 (1–2): 103–111.
  9. Schlachetzki F., Zhu C., Pardridge W.M. J. Neurochem. 2002; 81 (1): 203–206.
  10. Roopenian D.C., Akilesh S. Nat. Rev. Immunol. 2007; 7 (9): 715–725.
  11. Skerra A., Pluckthun A. Science. 1988; 240 (4855): 1038–1041.
  12. Better M., Chang C.P., Robinson R.R., Horwitz A.H. Science. 1988; 240 (4855): 1041–1043.
  13. Choi B.D., Cai M., Bigner D.D., Mehta A.I., Kuan C.T., Sampson J.H. Exp. Opin. Biol. Ther. 2011; 11 (7): 843–853.
  14. De Jonge J., Brissinck J., Heirman C., Demanet C., Leo O., Mo-ser M., Thielemans K. Mol. Immunol. 1995; 32 (17–18): 1405–1412.
  15. World Health Organization. Medicines. INN stems. The use of stems in the selection of International Nonproprietary Names (INN) for pharmaceutical substances 2013. URL: http://www. who.int/medicines/services/inn/stembook/en/ (аvailable: 04.10.2014)
  16. Chaudhry I.H., O’Donovan D.G., Brenchley P.E., Reid H., Rob-erts I.S. Histopathology. 2001; 39 (4): 409–415.
  17. Alitalo K., Carmeliet P. Cancer Cell. 2002; 1 (3): 219–227.
  18. Gururangan S., Chi S.N., Young Poussaint T., Onar–Thomas A., Gilbertson R.J., Vajapeyam S., Friedman H.S., Packer R.J., Rood B.N., Boyett J.M., Kun L.E. J. Clin. Oncol. 2010; 28 (18): 3069–3075.
  19. Nghiemphu P.L., Liu W., Lee Y., Than T., Graham C., Lai A., Green R.M., Pope W.B., Liau L.M., Mischel P.S., Nelson S.F., Elashoff R., Cloughesy T.F. Neurology. 2009; 72 (14): 1217–1222.
  20. Imai K., Takaoka A. Nat. Rev. Cancer. 2006; 6 (9): 714–727.
  21. Van Cutsem E., Nordlinger B., Cervantes A. Ann. Oncol. 2010; 21 (Suppl 5): 93–97.
  22. Peters S., Adjei A.A., Gridelli C., Reck M., Kerr K., Felip E. Ann. Oncol. 2012; 23 (Suppl 7): 56–64.
  23. Stupp R., Brada M., van den Bent M.J., Tonn J.C., Pentheroudakis G. Ann. Oncol. 2014. doi: 10.1093/annonc/mdu050.
  24. Narita Y., Jpn J. Clin. Oncol. 2013; 43 (6): 587–595.
  25. Chamberlain M.C., Johnston S.K. J. Neurooncol. 2010; 96 (2): 259–269.
  26. Nagane M., Nishikawa R., Narita Y., Kobayashi H., Takano S., Shinoura N., Aoki T., Sugiyama K., Kuratsu J., Muragaki Y., Sawamura Y., Matsutani M., Jpn J. Clin. Oncol. 2012; 42 (10): 887–895.
  27. Pope W.B., Lai A., Nghiemphu P., Mischel P., Cloughesy T.F. Neurology. 2006; 66 (8): 1258–1260.
  28. Vredenburgh J.J., Desjardins A., Herndon J.E., Dowell J.M., Rear-don D.A., Quinn J.A., Rich J.N., Sathornsumetee S., Gururangan S., Wagner M., Bigner D.D., Friedman A.H., Friedman H.S. Clin. Cancer Res. 2007; 13 (4): 1253–1259.
  29. Friedman H.S., Prados M.D., Wen P.Y., Mikkelsen T., Schiff D., Abrey L.E., Yung W.K., Paleologos N., Nicholas M.K., Jensen R., Vredenburgh J., Huang J., Zheng M., Cloughesy T. J. Clin. Oncol. 2009; 27 (28): 4733–4740.
  30. Kreisl T.N., Kim L., Moore K., Duic P., Royce C., Stroud I., Garren N., Mackey M., Butman J.A., Camphausen K., Park J., Albert P.S., Fine H.A. J. Clin. Oncol. 2009; 27 (5): 740–745.
  31. Reardon D.A., Desjardins A., Vredenburgh J.J., Gururangan S., Sampson J.H., Sathornsumetee S., McLendon R.E., Herndon J.E., Marcello J.E., Norfleet J., Friedman A.H., Bigner D.D., Friedman H.S. Br. J. Cancer. 2009; 101 (12): 1986–1994.
  32. Reardon D.A., Desjardins A., Peters K.B., Vredenburgh J.J., Guru-rangan S., Sampson J.H., McLendon R.E., Herndon J.E., Coan A., Threatt S., Friedman A.H., Friedman H.S. Cancer. 2011; 117 (23): 5351–5358.
  33. Desjardins A., Reardon D.A., Coan A., Marcello J., Herndon J.E., Bailey L., Peters K.B., Friedman H.S., Vredenburgh J.J. Cancer. 2012; 118 (5): 1302–1312.
  34. Quant E.C., Norden A.D., Drappatz J., Muzikansky A., Doherty L., Lafrankie D., Ciampa A., Kesari S., Wen P.Y. Neuro Oncol. 2009; 11 (5): 550–555.
  35. Norden A.D., Young G.S., Setayesh K., Muzikansky A., Klufas R., Ross G.L., Ciampa A.S., Ebbeling L.G., Levy B., Drappatz J., Kesari S., Wen P.Y. Neurology. 2008; 70 (10): 779–787.
  36. Wong E.T., Gautam S., Malchow C., Lun M., Pan E., Brem S. J. Nat. Compr. Canc. Netw. 2011; 9 (4): 403–407.
  37. Seystahl K., Weller M. Exp. Opin. Investig Drugs. 2012; 21 (5): 605–617.
  38. Wick W., Weller M., van den Bent M., Stupp R. J. Clin. Oncol. 2010; 28 (12): 188–189.
  39. Boockvar J.A., Tsiouris A.J., Hofstetter C.P., Kovanlikaya I., Fralin S., Kesavabhotla K., Seedial S.M., Pannullo S.C., Schwartz T.H., Stieg P., Zimmerman R.D., Knopman J., Scheff R.J., Christos P., Vallabhajosula S., Riina H.A. J. Neurosurg. 2011; 114 (3): 624–632.
  40. Burkhardt J.K., Riina H., Shin B.J., Christos P., Kesavabhotla K., Hofstetter C.P., Tsiouris A.J., Boockvar J.A. World Neurosurg. 2012; 77 (1): 130–134.
  41. Vredenburgh J.J., Cloughesy T., Samant M., Prados M., Wen P.Y., Mikkelsen T., Schiff D., Abrey L.E., Yung W.K., Paleologos N., Nicholas M.K., Jensen R., Das A., Friedman H.S. Oncologist. 2010; 15 (12): 1329–1334.
  42. Iwamoto F.M., Abrey L.E., Beal K., Gutin P.H., Rosenblum M.K., Reuter V.E., DeAngelis L.M., Lassman A.B. Neurology. 2009; 73 (15): 1200–1206.
  43. Wen P.Y., Macdonald D.R., Reardon D.A., Cloughesy T.F., Sorensen A.G., Galanis E., Degroot J., Wick W., Gilbert M.R., Lassman A.B., Tsien C., Mikkelsen T., Wong E.T., Chamberlain M.C., Stupp R., Lamborn K.R., Vogelbaum M.A., van den Bent M.J., Chang S.M. J. Clin. Oncol. 2010; 28 (11): 1963–1972.
  44. Zuniga R.M., Torcuator R., Jain R., Anderson J., Doyle T., Schultz L., Mikkelsen T. J. Neurooncol. 2010; 99 (2): 237–242.
  45. Clark A.J., Lamborn K.R., Butowski N.A., Chang S.M., Prados M.D., Clarke J.L., McDermott M.W., Parsa A.T., Berger M.S., Aghi M.K. Neurosurgery. 2012; 70 (2): 361–370.
  46. Lai A., Tran A., Nghiemphu P.L., Pope W.B., Solis O.E., Selch M., Filka E., Yong W.H., Mischel P.S., Liau L.M., Phuphanich S., Black K., Peak S., Green R.M., Spier C.E., Kolevska T., Polikoff J., Fehrenbacher L., Elashoff R., Cloughesy T. J. Clin. Oncol. 2011; 29 (2): 142–148.
  47. Chinot O.L., de La Motte Rouge T., Moore N., Zeaiter A., Das A., Phillips H., Modrusan Z., Cloughesy T. Adv. Ther. 2011; 28 (4): 334–340.
  48. Gilbert M.R., Dignam J.J., Armstrong T.S., Wefel J.S., Blumenthal D.T., Vogelbaum M.A., Colman H., Chakravarti A., Pugh S., Won M., Jeraj R., Brown P.D., Jaeckle K.A., Schiff D., Stieber V.W., Brachman D.G., Werner-Wasik M., Tremont-Lukats I.W., Sulman E.P., Aldape K.D., Curran W.J., Jr., Mehta M.P. N. Engl. J. Med. 2014; 370 (8): 699–708.
  49. Gilbert M.R., Sulman E.P., Mehta M.P. N. Engl. J. Med. 2014; 370 (21): 2048–2049.
  50. Liguigli W., Tomasello G., Toppo L., Ratti M., Passalacqua R. Future Oncol. 2014; 10 (9): 1549–1557.
  51. Корчагина А.А., Шеин С.А., Гурина О.И., Чехонин В.П. Роль рецепторов VEGFR в неопластическом ангиогенезе и перспективы терапии опухолей мозга. Вестник РАМН. 2013; 11: 104–114.
  52. Ikeda T., Sun L., Tsuruoka N., Ishigaki Y., Yoshitomi Y., Yoshi-take Y., Yonekura H. Biochem J. 2011; 436 (2): 399–407.
  53. Heldin C.H., Westermark B. Physiol Rev. 1999; 79 (4): 1283–1316.
  54. Dong J., Grunstein J., Tejada M., Peale F., Frantz G., Liang W.C., Bai W., Yu L., Kowalski J., Liang X., Fuh G., Gerber H.P., Ferrara N. Embo J. 2004; 23 (14): 2800–2810.
  55. Fleming T.P., Saxena A., Clark W.C., Robertson J.T., Oldfield E.H., Aaronson S.A., Ali I.U. Cancer Res. 1992; 52 (16): 4550–4553.
  56. Loizos N., Xu Y., Huber J., Liu M., Lu D., Finnerty B., Rolser R., Malikzay A., Persaud A., Corcoran E., Deevi D.S., Balderes P., Bassi R., Jimenez X., Joynes C.J., Mangalampalli V.R., Steiner P., Tonra J.R., Wu Y., Pereira D.S., Zhu Z., Ludwig D.L., Hicklin D.J., Bohlen P., Witte L., Kussie P. Mol. Cancer Ther. 2005; 4 (3): 369–379.
  57. Chiorean E.G., Sweeney C., Youssoufian H., Qin A., Dontabhaktuni A., Loizos N., Nippgen J., Amato R. Cancer Chem. Pharmacol. 2014; 73 (3): 595–604.
  58. Hernandez-Pedro N.Y., Rangel-Lopez E., Vargas Felix G., Pineda B., Sotelo J. Autoimmune Dis. 2013. doi: 10.1155/2013/716813.
  59. Blakeley J.O. Ramucirumab or Anti-PDGFR Alpha Monoclonal Antibody IMC-3G3 in Treating Patients With Recurrent Glioblastoma Multiforme. Clinical Trials. gov: a registry and results database of publicly and privately supported clinical studies of human participants conducted around the world. URL: http:// clinicaltrials.gov/ct2/show/NCT00895180?term= (available:09.09.2014)
  60. Gherardi E., Youles M.E., Miguel R.N., Blundell T.L., Iamele L., Gough J., Bandyopadhyay A., Hartmann G., Butler P. J. Proc. Natl. Acad. Sci USA. 2003; 100 (21): 12039–12044.
  61. Koochekpour S., Jeffers M., Rulong S., Taylor G., Klineberg E., Hudson E.A., Resau J.H., Vande Woude G.F. Cancer Res. 1997; 57 (23): 5391–5398.
  62. Cao B., Su Y., Oskarsson M., Zhao P., Kort E.J., Fisher R.J., Wang L.M., Vande Woude G.F. Proc. Natl. Acad. Sci USA. 2001; 98 (13): 7443–7348.
  63. Burgess T., Coxon A., Meyer S., Sun J., Rex K., Tsuruda T., Chen Q., Ho S.Y., Li L., Kaufman S., McDorman K., Cattley R.C., Elliott G., Zhang K., Feng X., Jia X.C., Green L., Radinsky R., Kendall R. Cancer Res. 2006; 66 (3): 1721–1729.
  64. Buchanan I.M., Scott T., Tandle A.T., Burgan W.E., Burgess T.L., Tofilon P.J., Camphausen K. J. Cell. Mol. Med. 2011; 15 (9): 1999– 2006.
  65. Jun H.T., Sun J., Rex K., Radinsky R., Kendall R., Coxon A., Burgess T.L. Clin. Cancer Res. 2007; 13 (22 Pt 1): 6735–6742.
  66. Rex K., Lewis X.Z., Gobalakrishnan S., Glaus C., Silva M.D., Radinsky R., Burgess T.L., Gambhir S.S., Coxon A. Nuc. Med. Biol. 2013; 40 (4): 458–463.
  67. Wen P.Y., Schiff D., Cloughesy T.F., Raizer J.J., Laterra J., Smitt M., Wolf M., Oliner K.S., Anderson A., Zhu M., Loh E., Reardon D.A. Neuro Oncol. 2011; 13 (4): 437–446.
  68. Martens T., Schmidt N.O., Eckerich C., Fillbrandt R., Merchant M., Schwall R., Westphal M., Lamszus K. Clin. Cancer Res. 2006; 12 (20 Pt 1): 6144–6152.
  69. Xin Y., Jin D., Eppler S., Damico-Beyer L.A., Joshi A., Davis J.D., Kaur S., Nijem I., Bothos J., Peterson A., Patel P., Bai S. J. Clin. Pharmacol. 2013; 53 (11): 1103–1111.
  70. Massague J. J. Biol. Chem. 1983; 258 (22): 13614–13620.
  71. Kalman B., Szep E., Garzuly F., Post D.E. Neuromol. Med. 2013; 15 (2): 420–434.
  72. Ullrich A., Coussens L., Hayflick J.S., Dull T.J., Gray A., Tam A.W., Lee J., Yarden Y., Libermann T.A., Schlessinger J. et al. Nature. 1984; 309 (5967): 418–425.
  73. Wells A. Int. J. Biochem. Cell. Biol. 1999; 31 (6): 637–643.
  74. Ekstrand A.J., James C.D., Cavenee W.K., Seliger B., Petters-son R.F., Collins V.P. Cancer Res. 1991; 51 (8): 2164–2172.
  75. Jaros E., Perry R.H., Adam L., Kelly P.J., Crawford P.J., Kal-bag R.M., Mendelow A.D., Sengupta R.P., Pearson A.D. Br. J. Cancer. 1992; 66 (2): 373–385.
  76. Libermann T.A., Nusbaum H.R., Razon N., Kris R., Lax I., Soreq H., Whittle N., Waterfield M.D., Ullrich A., Schlessinger J. Nature. 1985; 313 (5998): 144–147.
  77. Mineo J.F., Bordron A., Baroncini M., Maurage C.A., Ramirez C., Siminski R.M., Berthou C., Dam Hieu P. J. Neurooncol. 2007; 85 (3): 281–287.
  78. Torp S.H., Gulati S., Johannessen E., Dalen A. J. Exp. Clin. Cancer Res. 2007; 26 (3): 353–359.
  79. Sugawa N., Ekstrand A.J., James C.D., Collins V.P. Proc. Natl. Acad Sci USA. 1990; 87 (21): 8602–8606.
  80. Boockvar J.A., Kapitonov D., Kapoor G., Schouten J., Counelis G.J., Bogler O., Snyder E.Y., McIntosh T.K., O’Rourke D.M. Mol. Cell. Neurosci. 2003; 24 (4): 1116–1130.
  81. Pedersen M.W., Tkach V., Pedersen N., Berezin V., Poulsen H.S. Int. J. Cancer. 2004; 108 (5): 643–653.
  82. Montgomery R.B., Guzman J., O’Rourke D.M., Stahl W.L. J. Biol. Chem. 2000; 275 (23): 17358–17363.
  83. Nagane M., Narita Y., Mishima K., Levitzki A., Burgess A.W., Cavenee W.K., Huang H.J. J. Neurosurg. 2001; 95 (3): 472–479.
  84. Inda M.M., Bonavia R., Mukasa A., Narita Y., Sah D.W., Vanden-berg S., Brennan C., Johns T.G., Bachoo R., Hadwiger P., Tan P., Depinho R.A., Cavenee W., Furnari F. Genes Dev. 2010; 24 (16): 1731–1745.
  85. Wikstrand C.J., McLendon R.E., Friedman A.H., Bigner D.D. Cancer Res. 1997; 57 (18): 4130–4140.
  86. Del Vecchio C.A., Giacomini C.P., Vogel H., Jensen K.C., Florio T., Merlo A., Pollack J.R., Wong A.J. Oncogene. 2013; 32 (21): 2670–2681.
  87. Humphrey P.A., Wong A.J., Vogelstein B., Zalutsky M.R., Fuller G.N., Archer G.E., Friedman H.S., Kwatra M.M., Bigner S.H., Bigner D.D. Proc. Natl. Acad. Sci USA. 1990; 87 (11): 4207–4211.
  88. Eller J.L., Longo S.L., Kyle M.M., Bassano D., Hicklin D.J., Canute G.W. Neurosurgery. 2005; 56 (1): 155–162.
  89. Patel D., Lahiji A., Patel S., Franklin M., Jimenez X., Hicklin D.J., Kang X. Anticancer Res. 2007; 27 (5a): 3355–3366.
  90. Fukai J., Nishio K., Itakura T., Koizumi F. Cancer Sci. 2008; 99 (10): 2062–2069.
  91. Taylor T.E., Furnari F.B., Cavenee W.K. Curr. Cancer Drug. Targets. 2012; 12 (3): 197–209.
  92. Schulz-Ertner D. Study of Cetuximab, Radiotherapy and Temozolomide in Primary Glioblastoma Multiforme (GERT). Clinical Trials. gov: a registry and results database of publicly and privately supported clinical studies of human participants conducted around the world. URL: http://clinicaltrials.gov/ct2/ show/NCT00311857?term=NCT00311857&rank=1 (available:09.09.2014)
  93. Neyns B., Sadones J., Joosens E., Bouttens F., Verbeke L., Bau-rain J.F., D’Hondt L., Strauven T., Chaskis C., In’t Veld P., Michotte A., De Greve J. Ann. Oncol. 2009; 20 (9): 1596–1603.
  94. Blesa J.M., Molla S.B., Esparcia M.F., Ortells J.M., Godoy M.P., Das A.M., Magan B.M., Pulla M.P., Sanchez J.L., Canales J.B., Candel V.A. Case Rep. Oncol. 2012; 5 (3): 676–681.
  95. Hasselbalch B., Lassen U., Hansen S., Holmberg M., Sorensen M., Kosteljanetz M., Broholm H., Stockhausen M.T., Poulsen H.S. Neuro Oncol. 2010; 12 (5): 508–516.
  96. Yi D., Hua T.X., Lin H.Y., Kui C.L., Ning L.X., Wang Z.Z. J. Neurooncol. 2011; 104 (1): 93–101.
  97. Bode U., Massimino M., Bach F., Zimmermann M., Khuhlaeva E., Westphal M., Fleischhack G. Exp. Opin. Biol. Ther. 2012; 12 (12): 1649–1659.
  98. Ramos T.C., Figueredo J., Catala M., Gonzalez S., Selva J.C., Cruz T.M., Toledo C., Silva S., Pestano Y., Ramos M., Leonard I., Torres O., Marinello P., Perez R., Lage A. Cancer Biol. Ther. 2006; 5 (4): 375–379.
  99. Solomon M.T., Selva J.C., Figueredo J., Vaquer J., Toledo C., Quintanal N., Salva S., Domingez R., Alert J., Marinello J.J., Catala M., Griego M.G., Martell J.A., Luaces P.L., Ballesteros J., de Castro N., Bach F., Crombet T. BMC Cancer. 2013. doi: 10.1186/1471-2407-13-299.
  100. Jungbluth A.A., Stockert E., Huang H.J., Collins V.P., Coplan K., Iversen K., Kolb D., Johns T.J., Scott A.M., Gullick W.J., Ritter G., Cohen L., Scanlan M.J., Cavenee W.K., Old L.J. Proc. Natl. Acad. Sci USA. 2003; 100 (2): 639–644.
  101. Johns T.G., McKay M.J., Cvrljevic A.N., Gan H.K., Taylor C., Xu H., Smyth F.E., Scott A.M. Int. J. Radiat. Oncol. Biol. Phys. 2010; 78 (2): 572–578.
  102. Wang H., Shi B., Zhang Q., Jiang H., Hu S., Kong J., Yao M., Yang S., Li Z. Faseb. J. 2012; 26 (1): 73–80.
  103. Choi B.D., Kuan C.T., Cai M., Archer G.E., Mitchell D.A., Gedeon P.C., Sanchez-Perez L., Pastan I., Bigner D.D., Sampson J.H. Proc. Natl. Acad. Sci. USA. 2013; 110 (1): 270–275.
  104. Chinot O.L., Wick W., Mason W., Henriksson R., Saran F., Nishikawa R., Carpentier A.F., Hoang-Xuan K., Kavan P., Cernea D., Brandes A.A., Hilton M., Abrey L., Cloughesy T. N. Engl. J. Med. 2014; 370 (8): 709–722.
  105. Fine H.A. N. Engl. J. Med. 2014; 370 (8): 764–765.
  106. De Bonis P., Lofrese G., Anile C., Pompucci A., Vigo V., Mangiola A. Immunotherapy. 2013; 5 (6): 647–659.
  107. Chandramohan V., Sampson J.H., Pastan I., Bigner D.D. Clin. Dev. Immunol. 2012. doi: 10.1155/2012/480429.
  108. Chandramohan V., Bao X., Kato Kaneko M., Kato Y., Keir S.T., Szafranski S.E., Kuan C.T., Pastan I.H., Bigner D.D. Int. J. Cancer. 2013; 132 (10): 2339–2348.
  109. Piao H., Kuan C.T., Chandramohan V., Keir S.T., Pegram C.N., Bao X., Mansson J.E., Pastan I.H., Bigner D.D. MAbs. 2013; 5 (5): 748–762.
  110. Wang L.H., Ni C.W., Lin Y.Z., Yin L., Jiang C.B., Lv C.T., Le Y., Lang Y., Zhao C.Y., Yang K., Jiao B.H., Yin J. Tumour Biol. 2014; 35 (2): 1157–1168.
  111. Chen L., Miao W., Tang X., Zhang H., Wang S., Luo F., Yan J. J. Biomed. Nanotechnol. 2013; 9 (4): 551–558.
  112. Hulper P., Schulz-Schaeffer W., Dullin C., Hoffmann P., Harper J., Kurtzberg L., Lonning S., Kugler W., Lakomek M., Erdlenbruch B. Int. J. Oncol. 2011; 38 (1): 51–59.
  113. Xiong J., Zhou L., Lim Y., Yang M., Zhu Y.H., Li Z.W., Zhou F.H., Xiao Z.C., Zhou X.F. Oncol. Rep. 2013; 30 (6): 2719–2724.
  114. Zhu X., Fujita M., Snyder L.A., Okada H. J. Neurooncol. 2011; 104 (1): 83–92.
  115. Sampson J.H., Schmittling R.J., Archer G.E., Congdon K.L., Nair S.K., Reap E.A., Desjardins A., Friedman A.H., Fried-man H.S., Herndon J.E., 2nd, Coan A., McLendon R.E., Rear-don D.A., Vredenburgh J.J., Bigner D.D., Mitchell D.A. PLoS One. 2012. doi: 10.1371/journal.pone.0031046.
  116. Kudo M., Jono H., Shinriki S., Yano S., Nakamura H., Makino K., Hide T., Muta D., Ueda M., Ota K., Ando Y., Kuratsu J. J. Neurosurg. 2009; 111 (2): 219–225.
  117. Cheng Z., Zhou S., Wang X., Xie F., Wu H., Liu G., Wang Q., Chen Y., Hu Y., Lu B., Zhang X. Hybridoma (Larchmt). 2009; 28 (1): 33–41.
  118. Weber T.G., Osl F., Renner A., Poschinger T., Galban S., Rehemtulla A., Scheuer W. Cancer Res. 2014; 74 (7): 1913–1923.
  119. Herrmann T., Grosse–Hovest L., Otz T., Krammer P.H., Rammensee H.G., Jung G. Cancer Res. 2008; 68 (4): 1221–1227.
  120. Emlet D.R., Gupta P., Holgado-Madruga M., Del Vecchio C.A., Mitra S.S., Han S.Y., Li G., Jensen K.C., Vogel H., Xu L.W., Skirboll S.S., Wong A.J. Cancer Res. 2014; 74 (4): 1238–1249.
  121. Lou Y.W., Wang P.Y., Yeh S.C., Chuang P.K., Li S.T., Wu C.Y., Khoo K.H., Hsiao M., Hsu T.L., Wong C.H. Proc. Natl. Acad. Sci USA. 2014; 111 (7): 2482–2487.
  122. Zhan Q., Yue W., Shaoshan H. Braz. J. Med. Biol. Res. 2011; 44 (5): 489–490.
  123. Carbonell W.S., DeLay M., Jahangiri A., Park C.C., Aghi M.K. Cancer Res. 2013; 73 (10): 3145–3154.
  124. Yoshida T., Matsuda Y., Naito Z., Ishiwata T. Pathol. Int. 2012; 62 (7): 463–470.
  125. Poli A., Wang J., Domingues O., Planaguma J., Yan T., Rygh C.B., Skaftnesmo K.O., Thorsen F., McCormack E., Hentges F., Pedersen P.H., Zimmer J., Enger P.O., Chekenya M. Oncotarget. 2013; 4 (9): 1527–1546.
  126. Matsutani T., Hiwasa T., Takiguchi M., Oide T., Kunimatsu M., Saeki N., Iwadate Y. J. Exp. Clin. Cancer Res. 2012. doi: 10.1186/1756-9966-31-85.
  127. Zheng X., Chang F., Zhang X., Rothman V.L., Tuszynski G.P. Exp. Mol. Pathol. 2012; 93 (1): 111–115.
  128. Day B.W., Stringer B.W., Al–Ejeh F., Ting M.J., Wilson J., Ens-bey K.S., Jamieson P.R., Bruce Z.C., Lim Y.C., Offenhauser C., Charmsaz S., Cooper L.T., Ellacott J.K., Harding A., Leveque L., Inglis P., Allan S., Walker D.G., Lackmann M., Osborne G., Khanna K.K., Reynolds B.A., Lickliter J.D., Boyd A.W. Cancer Cell. 2013; 23 (2): 238–248.
  129. Rogers A.E., Le J.P., Sather S., Pernu B.M., Graham D.K., Pierce A.M., Keating A.K. Oncogene. 2012; 31 (38): 4171–4181.
  130. Foehr E.D., Lorente G., Kuo J., Ram R., Nikolich K., Urfer R. Cancer Res. 2006; 66 (4): 2271–2278.
  131. Loftus J.C., Yang Z., Tran N.L., Kloss J., Viso C., Berens M.E., Lipinski C.A. Mol. Cancer Ther. 2009; 8 (6): 1505–1514.
  132. He J., Yin Y., Luster T.A., Watkins L., Thorpe P.E. Clin. Cancer Res. 2009; 15 (22): 6871–6880.
  133. Liang J., Piao Y., Holmes L., Fuller G.N., Henry V., Tiao N., de Groot J.F. Clin. Cancer Res. 2014; 20 (1): 187–198.
  134. Kato Kaneko M., Ogasawara S., Kato Y., Tohoku J. Exp. Med. 2013; 230 (2): 103–109.
  135. McIntyre A., Patiar S., Wigfield S., Li J.L., Ledaki I., Turley H.,
  136. Leek R., Snell C., Gatter K., Sly W.S., Vaughan-Jones R.D., Swietach P., Harris A.L. Clin. Cancer Res. 2012; 18 (11): 3100–3111.
  137. Shao R., Francescone R., Ngernyuang N., Bentley B., Taylor S.L., Moral L., Yan W. Carcinogenesis. 2014; 35 (2): 373–382.
  138. Areshkov P.O., Avdieiev S.S., Balynska O.V., Leroith D., Kavsan V.M. Int. J. Biol. Sci. 2012; 8 (1): 39–48.
  139. Flies D.B., Han X., Higuchi T., Zheng L., Sun J., Ye J.J., Chen L. J. Clin. Invest. 2014; 124 (5): 1966–1975.
  140. Newcomb E.W., Lukyanov Y., Kawashima N., Alonso-Basanta M., Wang S.C., Liu M., Jure-Kunkel M., Zag-zag D., Demaria S., Formenti S.C. Radiat. Res. 2010; 173 (4): 426–432.
  141. Fecci P.E., Ochiai H., Mitchell D.A., Grossi P.M., Sweeney A.E., Archer G.E., Cummings T., Allison J.P., Bigner D.D., Samp-son J.H. Clin. Cancer Res. 2007; 13 (7): 2158–2167.
  142. Yusubalieva G.M., Baklaushev V.P., Gurina O.I., Gulyaev M.V., Pirogov Y.A., Chekhonin V.P. Bull. Exp. Biol. Med. 2012; 153 (1): 163–169.
  143. Yusubalieva G.M., Baklaushev V.P., Gurina O.I., Zorkina Y.A., Gubskii I.L., Kobyakov G.L., Golanov A.V., Goryainov S.A., Gorlachev G.E., Konovalov A.N., Potapov A.A., Chekhonin V.P. Bull. Exp. Biol. Med. 2014; 157 (4): 510–115.

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 1970 "Paediatrician" Publishers LLC



This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies