Systemic therapy for metastatic non-clear-cell renal cell carcinoma: Recent progress and future directions

Hematology/Oncology Clinics of North America

Volumn 25, Issue 4, 2011, Pages 853-869

  Chowdhury, Simon ^a   Matrana, Marc R ^b   Tsang, Christopher ^a   Atkinson, Bradley ^b   Choueiri, Toni K ^c   Tannir, Nizar M ^b  

^a GUY S HOSPITAL   (United Kingdom)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Chromophobe; Collecting duct carcinoma; Non clear cell renal cell carcinoma; Papillary; Renal medullary carcinoma; Sarcomatoid dedifferentiation; Targeted therapy; Unclassified

Indexed keywords

ABELSON KINASE; ALPHA INTERFERON; BEVACIZUMAB; BORTEZOMIB; CAPECITABINE; CARBOPLATIN; CISPLATIN; DOCETAXEL; DOXORUBICIN; EPIDERMAL GROWTH FACTOR RECEPTOR; ERLOTINIB; EVEROLIMUS; FLUOROURACIL; FORETINIB; FUMARATE HYDRATASE; GEMCITABINE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INTERLEUKIN 2; PAZOPANIB; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PLATELET DERIVED GROWTH FACTOR RECEPTOR; PROTEIN KINASE B; SORAFENIB; SUNITINIB; TEMSIROLIMUS; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2;

CHROMOPHOBE ADENOMA; CHROMOSOME TRANSLOCATION; CLEAR CELL RENAL CELL CARCINOMA; COLLECTING DUCT RENAL CELL CARCINOMA; COMPARATIVE STUDY; DRUG ACTIVITY; DRUG INHIBITION; FOLLICULAR CARCINOMA; HUMAN; KIDNEY CARCINOMA; KIDNEY TUBULE; LIGAND BINDING; MUCINOUS CARCINOMA; NON CLEAR CELL RENAL CELL CARCINOMA; PAPILLARY CARCINOMA; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RENAL MEDULLARY CARCINOMA; REVIEW; SARCOMATOID RENAL CELL CARCINOMA; SIGNAL TRANSDUCTION; SPINDLE CELL CARCINOMA; SYSTEMIC THERAPY; TUBULOCYSTIC CARCINOMA;

BENZENESULFONATES; CARCINOMA, RENAL CELL; CLINICAL TRIALS AS TOPIC; HUMANS; INDOLES; KIDNEY NEOPLASMS; NEOPLASM METASTASIS; PROTEIN KINASE INHIBITORS; PYRIDINES; PYRIMIDINES; PYRROLES; SULFONAMIDES; TREATMENT OUTCOME;

EID: 79960380836     PISSN: 08898588     EISSN: 15581977     Source Type: Journal    
DOI: 10.1016/j.hoc.2011.05.003     Document Type: Review

References (94)

1. Jemal A., Siegel R., Ward E., et al. Cancer statistics, 2008. CA Cancer J Clin 2008, 58:71-96.
2. Beck S.D., Patel M.I., Snyder M.E., et al. Effect of papillary and chromophobe cell type on disease-free survival after nephrectomy for renal cell carcinoma. Ann Surg Oncol 2004, 11:71-77.
3. Cheville J.C., Lohse C.M., Zincke H., et al. Comparisons of outcome and prognostic features among histologic subtypes of renal cell carcinoma. Am J Surg Pathol 2003, 27:612-624.
4. Patard J.J., Leray E., Rioux-Leclercq N., et al. Prognostic value of histologic subtypes in renal cell carcinoma: a multicenter experience. J Clin Oncol 2005, 23:2763-2771.
5. Reuter V.E. The pathology of renal epithelial neoplasms. Semin Oncol 2006, 33:534-543.
6. Motzer R.J., Mazumdar M., Bacik J., et al. Survival and prognostic stratification of 670 patients with advanced renal cell carcinoma. J Clin Oncol 1999, 17:2530-2540.
7. Ronnen E.A., Kondagunta G.V., Ishill N., et al. Treatment outcome for metastatic papillary renal cell carcinoma patients. Cancer 2006, 107:2617-2621.
8. Escudier B., Eisen T., Stadler W.M., et al. Sorafenib in advanced clear-cell renal-cell carcinoma. N Engl J Med 2007, 356:125-134.
9. Motzer R.J., Hutson T.E., Tomczak P., et al. Sunitinib versus interferon alfa in metastatic renal-cell carcinoma. N Engl J Med 2007, 356:115-124.
10. Jacobsen J., Grankvist K., Rasmuson T., et al. Different isoform patterns for vascular endothelial growth factor between clear cell and papillary renal cell carcinoma. BJU Int 2006, 97:1102-1108.
11. Ljungberg B.J., Jacobsen J., Rudolfsson S.H., et al. Different vascular endothelial growth factor (VEGF), VEGF-receptor 1 and -2 mRNA expression profiles between clear cell and papillary renal cell carcinoma. BJU Int 2006, 98:661-667.
12. Preston R.S., Philp A., Claessens T., et al. Absence of the Birt-Hogg-Dube gene product is associated with increased hypoxia-inducible factor transcriptional activity and a loss of metabolic flexibility. Oncogene 2011, 30:1159-1173.
13. Swartz M.A., Karth J., Schneider D.T., et al. Renal medullary carcinoma: clinical, pathologic, immunohistochemical, and genetic analysis with pathogenetic implications. Urology 2002, 60:1083-1089.
14. Krause D.S., Van Etten R.A. Tyrosine kinases as targets for cancer therapy. N Engl J Med 2005, 353:172-187.
15. Schlessinger J. Cell signaling by receptor tyrosine kinases. Cell 2000, 103:211-225.
16. Hudson C.C., Liu M., Chiang G.G., et al. Regulation of hypoxia-inducible factor 1alpha expression and function by the mammalian target of rapamycin. Mol Cell Biol 2002, 22:7004-7014.
17. Hara S., Oya M., Mizuno R., et al. Akt activation in renal cell carcinoma: contribution of a decreased PTEN expression and the induction of apoptosis by an Akt inhibitor. Ann Oncol 2005, 16:928-933.
18. Shin Lee J., Seok Kim H., Bok Kim Y., et al. Expression of PTEN in renal cell carcinoma and its relation to tumor behavior and growth. J Surg Oncol 2003, 84:166-172.
19. Vignot S., Faivre S., Aguirre D., et al. mTOR-targeted therapy of cancer with rapamycin derivatives. Ann Oncol 2005, 16:525-537.
20. Delahunt B., Eble J.N., McCredie M.R., et al. Morphologic typing of papillary renal cell carcinoma: comparison of growth kinetics and patient survival in 66 cases. Hum Pathol 2001, 32:590-595.
21. Yang X.J., Tan M.H., Kim H.L., et al. A molecular classification of papillary renal cell carcinoma. Cancer Res 2005, 65:5628-5637.
22. Kosaka T., Mikami S., Miyajima A., et al. Papillary renal cell carcinoma: clinicopathological characteristics in 40 patients. Clin Exp Nephrol 2008, 12:195-199.
23. Schmidt L., Junker K., Nakaigawa N., et al. Novel mutations of the MET proto-oncogene in papillary renal carcinomas. Oncogene 1999, 18:2343-2350.
24. van den Berg E., van der Hout A.H., Oosterhuis J.W., et al. Cytogenetic analysis of epithelial renal-cell tumors: relationship with a new histopathological classification. Int J Cancer 1993, 55(2):223-227.
25. Linehan W.M., Walther M.M., Zbar B. The genetic basis of cancer of the kidney. J Urol 2003, 170:2163-2172.
26. Mendel D.B., Laird A.D., Xin X., et al. 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 2003, 9:327-337.
27. O'Farrell A.M., Abrams T.J., Yuen H.A., et al. SU11248 is a novel FLT3 tyrosine kinase inhibitor with potent activity in vitro and in vivo. Blood 2003, 101:3597-3605.
28. Faivre S., Delbaldo C., Vera K., et al. Safety, pharmacokinetic, and antitumor activity of SU11248, a novel oral multitarget tyrosine kinase inhibitor, in patients with cancer. J Clin Oncol 2006, 24:25-35.
29. O'Farrell A.M., Foran J.M., Fiedler W., et al. An innovative phase I clinical study demonstrates inhibition of FLT3 phosphorylation by SU11248 in acute myeloid leukemia patients. Clin Cancer Res 2003, 9:5465-5476.
30. Gore M.E., Porta C., Oudard S., et al. Sunitinib in metastatic renal cell carcinoma (mRCC): preliminary assessment of toxicity in an expanded access trial with subpopulation analysis. J Clin Oncol 2007, 25(20 Suppl):5010. [abstract].
31. Plimack E.R., Jonash E., Bekele B.N., et al. Sunitinib in non-clear cell renal cell carcinoma (ncc-RCC): a phase II study. J Clin Oncol 2008, 26(20 Suppl):5112. [abstract].
32. Plimack E.R., Jonash E., Bekele B.N., et al. Sunitinib in papillary renal cell carcinoma (pRCC): results from a single-arm phase II study. J Clin Oncol 2010, 28(Suppl):4604. [abstract].
33. Ravaud A., Oudard S., Gravis-Mescam G., et al. First-line sunitinib in type I and II papillary renal cell carcinoma (PRCC): SUPAP, a phase II study of the French Genito-Urinary Group (GETUG) and the Group of Early Phase trials (GEP). J Clin Oncol 2009, 27(Suppl):5146. [abstract].
34. Molina A.M., Feldman D.R., Ginsberg M.S., et al. Phase II trial of sunitinib in patients with metastatic non-clear cell renal cell carcinoma. Invest New Drugs 2010, [Epub ahead of print].
35. Lee J., Ahn J., Lim S., et al. Multicenter prospective phase II study of sunitinib in non-clear cell type renal cell carcinoma. J Clin Oncol 2011, 29(Suppl 7). [abstract: 325].
36. Wilhelm S.M., Carter C., Tang L., et al. BAY 43-9006 exhibits broad spectrum oral antitumor activity and targets the RAF/MEK/ERK pathway and receptor tyrosine kinases involved in tumor progression and angiogenesis. Cancer Res 2004, 64:7099-7109.
37. Sridhar S.S., Hedley D., Siu L.L. Raf kinase as a target for anticancer therapeutics. Mol Cancer Ther 2005, 4:677-685.
38. Ratain M.J., Eisen T., Stadler W.M., et al. Phase II placebo-controlled randomized discontinuation trial of sorafenib in patients with metastatic renal cell carcinoma. J Clin Oncol 2006, 24:2505-2512.
39. Choueiri T.K., Plantade A., Elson P., et al. Efficacy of sunitinib and sorafenib in metastatic papillary and chromophobe renal cell carcinoma. J Clin Oncol 2008, 26:127-131.
40. Stadler W.M., Figlin R.A., McDermott D.F., et al. Safety and efficacy results of the advanced renal cell carcinoma sorafenib expanded access program in North America. Cancer 2010, 116:1272-1280.
41. Beck J., Bajata E., Escudier B., et al. A large open-label, non-comparative phase III study of the multi-targeted kinase inhibitor sorafenib in European patients with advanced renal cell carcinoma. Eur J Cancer 2007, (Suppl 7):244. [abstract: 4506].
42. Unnithan J, Vaziri S, Wood D, et al. Characterization of type II papillary renal cell carcinoma and efficacy of sorafenib. Genitourinary Cancers Symposium 2008 [abstract: 409].
43. Hudes G., Carducci M., Tomczak P., et al. Temsirolimus, interferon alfa, or both for advanced renal-cell carcinoma. N Engl J Med 2007, 356:2271-2281.
44. Dutcher J.P., de Souza P., McDermott D., et al. Effect of temsirolimus versus interferon-alpha on outcome of patients with advanced renal cell carcinoma of different tumor histologies. Med Oncol 2009, 26:202-209.
45. Yang S., de Souza P., Alemao E., et al. Quality of life in patients with advanced renal cell carcinoma treated with temsirolimus or interferon-alpha. Br J Cancer 2010, 102:1456-1460.
46. Perera A.D., Kleymenova E.V., Walker C.L. Requirement for the von Hippel-Lindau tumor suppressor gene for functional epidermal growth factor receptor blockade by monoclonal antibody C225 in renal cell carcinoma. Clin Cancer Res 2000, 6:1518-1523.
47. Gordon M.S., Hussey M., Nagle R.B., et al. Phase II study of erlotinib in patients with locally advanced or metastatic papillary histology renal cell cancer: SWOG S0317. J Clin Oncol 2009, 27:5788-5793.
48. Eder J.P., Shapiro G.I., Appleman L.J., et al. A phase I study of foretinib, a multi-targeted inhibitor of c-Met and vascular endothelial growth factor receptor 2. Clin Cancer Res 2010, 16:3507-3516.
49. Srinivasan R., Choueiri T.K., Vaishampayan U., et al. A phase II study of the dual MET/VEGFR2 inhibitor XL880 in patients (pts) with papillary renal carcinoma (PRC). J Clin Oncol 2008, 26(20 Suppl):5103. [abstract].
50. Srinivasan R., Linehan W., Vaishampayan U., et al. A phase II study of two dosing regimens of GSK 1363089 (GSK089), a dual MET/VEGFR2 inhibitor, in patients (pts) with papillary renal carcinoma (PRC). J Clin Oncol 2009, 27(Suppl). [abstract: 5103].
51. Bannasch P., Schacht U., Storch E. Morphogenese undhobe Mikromorphologie epithelialer Nierentumoren bei Nitrosomorpholine-vergifteten Ratten. I. Induktion und Histologie der Tumon. Z Krebsforsch Klin Onkol Cancer Res Clin Oncol 1974, 81:311-331. [in German].
52. Thoenes W., Storkel S., Rumpelt H.J. Human chromophobe cell renal carcinoma. Virchows Arch B Cell Pathol Incl Mol Pathol 1985, 48:207-217.
53. Crotty T.B., Farrow G.M., Lieber M.M. Chromophobe cell renal carcinoma: clinicopathological features of 50 cases. J Urol 1995, 154:964-967.
54. Stec R., Grala B., Maczewski M., et al. Chromophobe renal cell cancer-review of the literature and potential methods of treating metastatic disease. J Exp Clin Cancer Res 2009, 28:134.
55. Gad S., Lefevre S.H., Khoo S.K., et al. Mutations in BHD and TP53 genes, but not in HNF1beta gene, in a large series of sporadic chromophobe renal cell carcinoma. Br J Cancer 2007, 96:336-340.
56. Yamazaki K., Sakamoto M., Ohta T., et al. Overexpression of KIT in chromophobe renal cell carcinoma. Oncogene 2003, 22:847-852.
57. Kovacs A., Störkel S., Thoenes W., et al. Mitochondrial and chromosomal DNA alterations in human chromophobe renal cell carcinomas. J Pathol 1992, 167:273-277.
58. Marur S., Eliason J., Heilbrun L.K., et al. Phase II trial of capecitabine and weekly docetaxel in metastatic renal cell carcinoma. Urology 2008, 72:898-902.
59. Davis C.J., Mostofi F.K., Sesterhenn I.A. Renal medullary carcinoma: the seventh sickle cell nephropathy. Am J Surg Pathol 1995, 19:1-11.
60. Berman L.B. Sickle cell nephropathy. JAMA 1974, 228:1279.
61. Sathyamoorthy K., Teo A., Atallah M. Renal medullary carcinoma in a patient with sickle-cell disease. Nat Clin Pract Urol 2006, 3:279-283.
62. Patel K., Livni N., Macdonald D. Renal medullary carcinoma, a rare cause of hematuria in sickle cell trait. Br J Haematol 2006, 132:1.
63. Yan B.C., Mackinnon A.C., Al-Ahmadie H.A. Recent developments in the pathology of renal tumors: morphology and molecular characteristics of select entities. Arch Pathol Lab Med 2009, 133:1026-1032.
64. Srigley J.R., Delahunt B. Uncommon and recently described renal carcinomas. Mod Pathol 2009, 22(Suppl 2):S2-S23.
65. Tannir NM, Lim ZD, Rao P, et al. Outcome of patients with renal medullary carcinoma (RMC) treated in the era of targeted therapies (TT): a multicenter experience. GU ASCO Symposium. Orlando (FL), February 18, 2011.
66. Albadine R., Wang W., Brownlee N.A., et al. Topoisomerase II alpha status in renal medullary carcinoma: immuno-expression and gene copy alterations of a potential target of therapy. J Urol 2009, 182(2):735-740.
67. Schaeffer E.M., Guzzo T.J., Furge K.A., et al. Renal medullary carcinoma: molecular, pathological and clinical evidence for treatment with topoisomerase-inhibiting therapy. BJU Int 2010, 106(1):62-65.
68. Cheng J.X., Tretiakova M., Gong C., et al. Renal medullary carcinoma: rhabdoid features and the absence of INI1 expression as markers of aggressive behavior. Mod Pathol 2008, 21(6):647-652.
69. Mariño-Enríquez A., Ou W.B., Weldon C.B., et al. ALK rearrangement in sickle cell trait-associated renal medullary carcinoma. Genes Chromosomes Cancer 2011, 50(3):146-153.
70. Heng D.Y., Choueiri T.K. Non-clear cell renal cancer: features and medical management. J Natl Compr Canc Netw 2009, 7:659-665.
71. Aghajanian C., Soignet S., Dizon D.S., et al. A phase I trial of the novel proteasome inhibitor PS341 in advanced solid tumor malignancies. Clin Cancer Res 2002, 8:2505-2511.
72. Kondagunta G.V., Drucker B., Schwartz L., et al. Phase II trial of bortezomib for patients with advanced renal cell carcinoma. J Clin Oncol 2004, 22:3720-3725.
73. Ronnen E.A., Kondagunta G.V., Motzer R.J. Medullary renal cell carcinoma and response to therapy with bortezomib. J Clin Oncol 2006, 24:e14.
74. Ansari J., Fatima A., Chaudhri S., et al. Sorafenib induces therapeutic response in a patient with metastatic collecting duct carcinoma of kidney. Onkologie 2009, 32:44-46.
75. MacLennan G.T., Farrow G.M., Bostwick D.G. Low-grade collecting duct carcinoma of the kidney: report of 13 cases of low-grade mucinous tubulocystic renal carcinoma of possible collecting duct origin. Urology 1997, 50:679-684.
76. Cossu-Rocca P., Eble J.N., Delahunt B., et al. Renal mucinous tubular and spindle carcinoma lacks the gains of chromosomes 7 and 17 and losses of chromosome Y that are prevalent in papillary renal cell carcinoma. Mod Pathol 2006, 19:488-493.
77. Amin M.B., MacLennan G.T., Gupta R., et al. Tubulocystic carcinoma of the kidney clinicopathologic analysis of 31 cases of a distinctive rare subtype of renal cell carcinoma. Am J Surg Pathol 2009, 33:384-392.
78. Mego M., Sycova-Mila Z., Rejlekova K., et al. Expand+sunitinib in the treatment of tubulocystic carcinoma of the kidney. A case report. Ann Oncol 2008, 19(9):1655-1656.
79. Argani P., Ladanyi M. Translocation carcinoma of the kidney. Clin Lab Med 2005, 25:363-378.
80. Camparo P., Vasiliu V., Molinie V., et al. Renal translocation carcinomas-clinicopathologic, immunohistochemical and gene expression profiling analysis of 31 cases with a review of the literature. Am J Surg Pathol 2008, 35:656-670.
81. Argani P., Lal P., Hutchinson B., et al. Aberrant nuclear immunoreactivity for TFE3 in neoplasms with TFE3 gene fusions: a sensitive and specific immunohistochemical assay. Am J Surg Pathol 2003, 27:750-761.
82. Choueiri T.K., Lim Z.D., Hirsch M.S., et al. Vascular endothelial growth factor-targeted therapy for the treatment of adult metastatic Xp11.2 translocation renal cell carcinoma. Cancer 2010, 116:5219-5225.
83. Malouf G.G., Camparo P., Oudard S., et al. Targeted agents in metastatic Xp11 translocation/TFE3 gene fusion renal cell carcinoma (RCC): a report from the Juvenile RCC Network. Ann Oncol 2010, 21:1834-1838.
84. Dhillon J., Tannir N.M., Matin S.F., et al. Thyroid-like follicular carcinoma of the kidney with metastases to the lungs and retroperitoneal lymph nodes. Hum Pathol 2011, 42:146-150.
85. Mian B.M., Bhadkamkar N., Slaton J.W., et al. Prognostic factors and survival of patients with sarcomatoid renal cell carcinoma. J Urol 2002, 167:65-70.
86. Abel E.J., Culp S.H., Matin S.F., et al. Percutaneous biopsy of primary tumor in metastatic renal cell carcinoma to predict high risk pathological features: comparison with nephrectomy assessment. J Urol 2010, 184:1877-1881.
87. Shuch B., Said J., La Rochelle J.C., et al. Cytoreductive nephrectomy for kidney cancer with sarcomatoid histology-is up-front resection indicated and, if not, is it avoidable?. J Urol 2009, 182:2164-2171.
88. Golshayan A.R., George S., Heng D.Y., et al. Metastatic sarcomatoid renal cell carcinoma treated with vascular endothelial growth factor-targeted therapy. J Clin Oncol 2009, 27:235-241.
89. Escudier B., Droz J.P., Rolland F., et al. Doxorubicin and ifosfamide in patients with metastatic sarcomatoid renal cell carcinoma: a phase II study of the Genitourinary Group of the French Federation of Cancer Centers. J Urol 2002, 168:959-961.
90. Nanus D.M., Garino A., Milowsky M.I., et al. Active chemotherapy for sarcomatoid and rapidly progressing renal cell carcinoma. Cancer 2004, 101:1545-1551.
91. Dutcher J.P., Nanus D. Long-term survival of patients with sarcomatoid renal cell cancer treated with chemotherapy. Med Oncol 2010, [Epub ahead of print].
92. Haas N, Manola J, Pins M. ECOG 8802: Phase II trial of doxorubicin and gemcitabine in metastatic renal cell carcinoma with sarcomatoid features. 2009 ASCO Genitourinary Cancers Symposium. Orlando (FL) [abstract: 285].
93. Michaelson M. Combination sunitinib and gemcitabine in sarcomatoid and/or poor-risk patients with metastatic renal cell carcinoma. NCT00556049.
94. Pagliaro L. Capecitabine, gemcitabine, and bevacizumab in combination for patients with sarcomatoid renal cell carcinoma. NCT00496587.