Mechanisms of acquired resistance to tyrosine kinase inhibitors in clear-cell renal cell carcinoma (ccRCC)

Current Signal Transduction Therapy

Volumn 8, Issue 3, 2013, Pages 219-228

  Bielecka, Zofia F ^a,b   Czarnecka, Anna M ^a   Solarek, Wojciech ^a,b   Kornakiewicz, Anna ^a,b   Szczylik, Cezary ^a  

^a MILITARY INSTITUTE OF MEDICINE   (Poland)

^b MEDICAL UNIVERSITY OF WARSAW   (Poland)

Author keywords

Acquired drug resistance; Angiogenic switch; Anti angiogenic therapy; Axitinib; Clear cell renal cell carcinoma; Epithelialmesenchymal transition; Non genetic resistance mechanisms; Pazopanib; Sorafenib; Sunitinib; Tivozanib; Tyrosine kinase inhibitors

Indexed keywords

AXITINIB; PAZOPANIB; PROTEIN TYROSINE KINASE INHIBITOR; SORAFENIB; SUNITINIB; TIVOZANIB; VASCULOTROPIN;

ACQUIRED DRUG RESISTANCE; ANGIOGENIC SWITCH; ARTICLE; B LYMPHOCYTE; CANCER CELL; CELL SURVIVAL; CELLULAR DISTRIBUTION; CELLULAR PARAMETERS; DRUG BLOOD LEVEL; DRUG RESISTANCE; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; KIDNEY CARCINOMA; LYSOSOMAL SEQUESTRATION; NONHUMAN; PERICYTE; PERICYTE COVERAGE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TUMOR ASSOCIATED LEUKOCYTE;

EID: 84900545283     PISSN: 15743624     EISSN: None     Source Type: Journal    
DOI: 10.2174/1574362409666140206223014     Document Type: Article

References (82)

1. Gupta K, Miller JD, Li JZ et al. Epidemiologic and socioeconomic burden of metastatic renal cell carcinoma (mRCC): A literature review. Cancer Treatment Reviews 2008; 34: 193-205.
2. Ljungberg B et al. The epidemiology of renal cell carcinoma. European Urology 2011; 60: 615-21.
3. Murai M, Oya M. Renal cell carcinoma: etiology, incidence and epidemiology. Curr Opin Urol 2004; 14: 229-233.
4. Iacovelli R, Alesini D, Palazzo A et al. Targeted therapies and complete responses in first line treatment of metastatic renal cell carcinoma. A meta-analysis of published trials. Cancer Treat Rev 2013; doi: 10.1016/j.ctrv.2013.09.003. [Epub ahead of print].
5. Escudier B, Eisen T, Stadler WM et al. Sorafenib in advanced clear-cell renal-cell carcinoma. N Engl J Med 2007; 356(2): 125- 34. Erratum in: N Engl J Med. 2007; 357(2): 203. (Pubitemid 46089673
6. Motzer RJ, Hutson TE. Sunitinib versus Interferon Alfa in Metastatic Renal-Cell Carcinoma. N Engl J Med. 2007 Jan 11; 356(2): 115-24.
7. Coppin C. Sunitinib for advanced renal cell cancer. Biologics 2008; 2(1): 97-105.
8. Tafreshi A, Thientosapol E, Liew MS et al. Efficacy of sorafenib in advanced renal cell carcinoma independent of prior treatment, histology or prognostic group. Asia Pac J Clin Oncol 2013; doi: 10.1111/ajco.12122 [Epub ahead of print].
9. Cella D, Escudier B, Rini B et al. Patient-reported outcomes for axitinib vs sorafenib in metastatic renal cell carcinoma: phase III (AXIS) trial. Br J Cancer 2013; 108(8): 1571-8.
10. Rini BI, Escudier B, Tomczak P et al. Comparative effectiveness of axitinib versus sorafenib in advanced renal cell carcinoma (AXIS): a randomised phase 3 trial. Lancet 2011; 378(9807): 1931-9.
11. Sternberg CN, Davis ID, Mardiak J et al. Pazopanib in locally advanced or metastatic renal cell carcinoma: results of a randomized phase III trial. J Clin Oncol 2010; 28(6): 1061-8.
12. Motzer RJ, Nosov D, Eisen T et al. Tivozanib Versus Sorafenib As Initial Targeted Therapy for Patients With Metastatic Renal Cell Carcinoma: Results From a Phase III Trial. J Clin Oncol 2013; 31(30): 3791-9.
13. Bhargava P, Robinson MO. Development of second-generation VEGFR tyrosine kinase inhibitors: current status. Curr Oncol Rep 2011; 13: 103-11.
14. Arora A, Scholar EM. Role of tyrosine kinase inhibitors in cancer therapy. J Pharmacol Exp Ther 2005; 315: 71-79.
15. Gotink KJ, Verheul HMW. Anti-angiogenic tyrosine kinase inhibitors: what is their mechanism of action? Angiogenesis 2010; 13: 1-14.
16. Hicklin DJ, Ellis LM. Role of the vascular endothelial growth factor pathway in tumor growth and angiogenesis. J Clin Oncol Of J Am Soc Clin Oncol 2005; 23: 1011-27.
17. Parikh AA, Ellis LM. The vascular endothelial growth factor family and its receptors. Hematol Oncol Clin North Am 2004; 18: 951-71.
18. Posner I, Engel M, Gazit A, Levitzki A. Kinetics of inhibition by tyrphostins of the tyrosine kinase activity of the epidermal growth factor receptor and analysis by a new computer program. Mol Pharmacol 1994; 45: 673-683.
19. Johnson LN. Protein kinase inhibitors: contributions from structure to clinical compounds. Q Rev Biophys 2009; 42: 1-40.
20. Karashima T, Fukuhara H, Tamura K et al. Expression of angiogenesis-related gene profiles and development of resistance to tyrosine-kinase inhibitor in advanced renal cell carcinoma: characterization of sorafenib-resistant cells derived from a cutaneous metastasis. Int J Urol 2013; 20(9): 923-30.
21. Figlin RA, Kaufmann I, Brechbiel J. Targeting PI3K and mTORC2 in metastatic renal cell carcinoma: new strategies for overcoming resistance to VEGFR and mTORC1 inhibitors. Int J Cancer 2013; 133(4): 788-96.
22. Rini BI, Atkins MB. Resistance to targeted therapy in renal-cell carcinoma. Lancet Oncol 2009; 10(10): 992-1000.
23. Eisenhauer EA, Therasse P, Bogaerts J et al. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1) Eur J Cancer 2009; 45(2): 228-47.
24. Rosa R, Damiano V, Nappi L. Angiogenic and signalling proteins correlate with sensitivity to sequential treatment in renal cell cancer. Br J Cancer 2013; 109(3): 686-93.
25. Khattak M, Larkin J. Sequential therapy with targeted agents in metastatic renal cell carcinoma: beyond second-line and overcoming drug resistance. World J Urol 2013; doi: 10.1007/ s00345-012-103-z.
26. Buczek M, Escudier B, Bartnik E et al. Resistance to tyrosine kinase inhibitors in clear-cell renal cell carcinoma: From the patient's bed to molecular mechanisms. Biochim Biophys Acta 2013; doi: 10.1016/j.bbcan.2013.10. 001.
27. Huang D, Ding Y, Li Y et al. Sunitinib acts primarily on tumor endothelium rather than tumor cells to inhibit the growth of renal cell carcinoma. Cancer Res 2010; 70(3): 1053-62.
28. Ravaud A, Digue L, Trufflandier N et al. VEGFR TKI 'resistance' or transient clinical insensitivity to VEGFR TKI in metastatic renal cell carcinoma. Ann Oncol 2010; 21(2): 431-2.
29. Grünwald V, Weikert S, Seidel C et al. Efficacy of sunitinib reexposure after failure of an mTOR inhibitor in patients with metastatic RCC. Onkologie 2011; 34(6): 310-4.
30. Harada K, Miyake H, Kusuda Y, Fujisawa M. Expression of epithelial-mesenchymal transition markers in renal cell carcinoma: impact on prognostic outcomes in patients undergoing radical nephrectomy. BJU Int 2012; 110(1): E1131-7.
31. Hugo H, Ackland ML, Blick T et al. Epithelial-mesenchymal and mesenchymal-epithelial transitions in carcinoma progression. J Cell Physiol 2007; 213(2): 374-83.
32. Klymkowsky MW, Savagner P. Epithelial-mesenchymal transition: a cancer researcher's conceptual friend and foe. Am J Pathol 2009; 174(5): 1588-93.
33. Chaffer CL, Weinberg RA. A perspective on cancer cell metastasis. Science 2011; 331(6024): 1559-64.
34. Hammers HJ, Verheul HM, Salumbides B et al. Reversible epithelial to mesenchymal transition and acquired resistance to sunitinib in patients with renal cell carcinoma: evidence from a xenograft study. Mol Cancer Ther 2010; 9(6): 1525-35.
35. Ackland ML, Newgreen DF, Fridman M et al. Epidermal growth factor-induced epithelial-mesenchymal transition in human breast carcinoma cells. Lab Invest 2003; 83(3): 435-48.
36. Behnsawy HM, Shigemura K, Meligy FY et al. Possible role of sonic hedgehog and epithelial-mesenchymal transition in renal cell cancer progression. Korean J Urol 2013; 54(8): 547-54.
37. Ghersi G. Roles of molecules involved in epithelial/mesenchymal transition during angiogenesis. Front Biosci 2008; 1(13): 2335-55.
38. Frederick BA, Helfrich BA, Coldren CD et al. Epithelial to mesenchymal transition predicts gefitinib resistance in cell lines of head and neck squamous cell carcinoma and non-small cell lung carcinoma. Mol Cancer Ther 2007; 6(6): 1683-91.
39. Yu M, Bardia A, Wittner BS et al. Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition. Science 2013; 339(6119): 580-4.
40. Insan MB, Jaitak V. New Approaches to Target Cancer Stem Cells: Current Scenario. Mini Rev Med Chem 2013 [Epub ahead of print]
41. Huang B, Huang YJ, Yao ZJ et al. Cancer stem cell-like side population cells in clear cell renal cell carcinoma cell line 769P. PLoS One. 2013; 8(7): e68293. doi: 10.1371/journal.pone.0068293.
42. Hollier BG, Evans K, Mani SA. The epithelial-to-mesenchymal transition and cancer stem cells: a coalition against cancer therapies. J Mammary Gland Biol Neoplasia 2009; 14(1): 29-43.
43. Singh A, Settleman J. EMT, cancer stem cells and drug resistance: an emerging axis of evil in the war on cancer. Oncogene 2010; 29(34): 4741-51.
44. Zhang Q-w, Liu L, Gong C-y et al. Prognostic Significance of Tumor-Associated Macrophages in Solid Tumor: A Meta-Analysis of the Literature 2012. PLoS ONE 7(12): e50946.doi: 10.1371/ journal.pone.0050946
45. Heusinkveld M, van der Burg SH. Identification and manipulation of tumor associated macrophages in human cancers. J Transl Med 2009; 9: 216.
46. Capece D, Fischietti M, Verzella M. The Inflammatory Microenvironment in Hepatocellular Carcinoma: A Pivotal Role for Tumor-Associated Macrophages Volume 2013, doi: 10.1155/2013/ 187204.
47. Tang X et al. Tumor-associated macrophages as potential diagnostic and prognostic biomarkers in breast cancer. Cancer Lett 2013; 332(1): 3-10.
48. de Vries M, Briaire-de Bruijn I, Malessy MJ et al. Tumorassociated macrophages are related to volumetric growth of vestibular schwannomas. Otol Neurotol 2013; 34(2): 347-52.
49. Liu CY, Xu JY, Shi XY et al. M2-polarized tumor-associated macrophages promoted epithelial-mesenchymal transition in pancreatic cancer cells, partially through TLR4/IL-10 signaling pathway. Lab Invest 2013; 93(7): 844-54.
50. Ikemoto S, Yoshida N, Narita K et al. Role of tumor-associated macrophages in renal cell carcinoma. Oncol Rep 2003; 10(6): 1843-9.
51. Santoni M, Massari F, Amantini C et al. Emerging role of tumorassociated macrophages as therapeutic targets in patients with metastatic renal cell carcinoma. Cancer Immunol Immunother 2013 [Epub ahead of print]
52. Balkwill F. TNF-alpha in promotion and progression of cancer. Cancer Metastasis Rev 2006; 25(3): 409-16.
53. Mantovani A, Sozzani S, Locati M et al. Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol 2002; 23(11): 549-55.
54. Dannenmann SR, Thielicke J, Stöckli M et al. Tumor-associated macrophages subvert T-cell function and correlate with reduced survival in clear cell renal cell carcinoma. Oncoimmunology 2013; 2(3): e23562.
55. Huang D, Ding Y, Zhou M. et al. Interleukin-8 mediates resistance to antiangiogenic agent. Cancer Res 2010; 70(3): 1063-71.
56. Mizukami Y, Jo WS, Duerr EM et al. Induction of interleukin-8 preserves the angiogenic response in HIF-1alpha-deficient colon cancer cells. Nat Med 2005; 11(9): 992-7.
57. Porta C, Paglino C, Imariso I et al. Changes in circulating proangiogenic cytokines, other than VEGF, before progression to sunitinib therapy in advanced renal cell carcinoma patients. Oncology 2013; 84(2): 115-22.
58. Saylor P, Escudier B. Michaelson MD. Importance of fibroblast growth factor receptor in neovascularization and tumor escape from antiangiogenic therapy. Clin Genitourin Cancer 2012: 10(2): 77- 83.
59. Bhatt RS, Wang X, Zhang L et al. Renal cancer resistance to antiangiogenic therapy is delayed by restoration of angiostatic signaling. Mol Cancer Ther 2010; 9(10): 2793-802.
60. Bergers D, Hanahan D. Modes of resistance to antiangiogenic therapy. Nat Rev Cancer 2008; 8(8): 592-603.
61. Bergers G, Benjamin LE. Tumorigenesis and the angiogenic switch. Nat Rev Cancer 2003; 3(6): 401-10.
62. Cao Y, Zhong W, Sun Y. Improvement of antiangiogenic cancer therapy by understanding the mechanisms of angiogenic factor interplay and drug resistance. Semin Cancer Biol 2009; 19(5): 338- 43.
63. Tamaskar I, Dhillon J, Pili R. Resistance to angiogenesis inhibitors in renal cell carcinoma. Clin Adv Hematol Oncol 2011; 9(2): 101- 10.
64. Hirschi KK, d'Amore PA. Control of angiogenesis by the pericyte: molecular mechanisms and significance. EXS 1997; 79(49).
65. Allt G, Lawrenson JG. Pericytes: cell biology and pathology. Cells Tissues Organs 2001; 169(1): 1-11.
66. Ribatti D, Nico B, Crivellato E. The role of pericytes in angiogenesis. Int J Dev Biol 2011; 55(3): 261-8.
67. Armulik A, Genové G, Betsholtz C. Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev Cell 2011; 21(2): 193-215.
68. Hall AP. Review of the pericyte during angiogenesis and its role in cancer and diabetic retinopathy. Toxicol Pathol 2006; 34(6): 763- 75.
69. Cao Z, Shang B, Zhang G et al. Tumor cell-mediated neovascularization and lymphangiogenesis contrive tumor progression and cancer metastasis. Biochim Biophys Acta 2013; 1836(2): 273-286.
70. Nisancioglu MH, Betsholtz C, Genové G. The absence of pericytes does not increase the sensitivity of tumor vasculature to vascular endothelial growth factor-A blockade. Cancer Res 2010; 70(12): 5109-15.
71. Pàez-Ribes M, Allen E, Hudock J et al. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell 2009; 15(3): 220-31.
72. Cooke VG, LeBleu VS, Keskin D Pericyte depletion results in hypoxia-associated epithelial-to-mesenchymal transition and metastasis mediated by met signaling pathway. Cancer Cell 2012; 21(1): 66-81.
73. Escudier B, Eisen T, Stadler WM et al. Sorafenib in advanced clear-cell renal-cell carcinoma. N Engl J Med 2007; 356(2): 125- 34. (Pubitemid 46089673
74. Gotink KJ, Broxterman HJ, Labots M. et al. Lysosomal sequestration of sunitinib: a novel mechanism of drug resistance. Clin Cancer Res 2011; 17(23): 7337-46.
75. Houk BE, Bello CL, Poland B et al. Relationship between exposure to sunitinib and efficacy and tolerability endpoints in patients with cancer: results of a pharmacokinetic/pharmacodynamic metaanalysis. Cancer Chemother Pharmacol 2010; 66(2): 357-71.
76. Khalil B, Hudson J, Williams R, et al. An individualised dose/schedule strategy for sunitinib in metastatic renal cell cancer (mRCC) on progression-free survival (PFS): Correlation with dynamic microbubble ultrasound (DCE-US) data. J Clin Oncol 2011; 29: [abstr.e15149].
77. Ravaud A, Gross-Goupil M. Overcoming resistance to tyrosine kinase inhibitors in renal cell carcinoma. Cancer Treatment Reviews 2012; doi: 10.1016/j.ctrv.2012.01.003.
78. Sierra JR, Cepero V, Giordano S. Molecular mechanisms of acquired resistance to tyrosine kinase therapy. Mol Cancer 2010; 9(75).
79. Randall Logan, Alex Kong, Jeffrey P. Krise et al. Evaluating the Roles of Autophagy and Lysosomal Trafficking Defects in Intracellular Distribution-Based Drug-Drug Interactions Involving Lysosomes. Journal of Pharmaceutical Sciences 2013; 102(11): 4173-4180.
80. Azam F, Mehta S, Harris AL. Mechanisms of resistance to antiangiogenesis therapy. Eur J Cancer 2010; 46(8): 1323-32.
81. Dewhirst MW, Cao Y, Moeller B. Cycling hypoxia and free radicals regulate angiogenesis and therapy response. Nat Rev Cancer 2008; 8: 425-37.
82. Cristofanilli M, Charnsangavej C, Hortobagyi GN. Angiogenesis modulation in cancer research: novel clinical approaches. Nat Rev Drug Discov 2002; 1(6): 415-26.