373
Views
10
CrossRef citations to date
0
Altmetric
Review

Targeting angiogenesis in metastatic renal cell carcinoma

, , , , , & show all
Pages 245-257 | Received 01 Nov 2018, Accepted 23 Jan 2019, Published online: 06 Feb 2019

References

  • Medina-Rico M, Ramos HL, Lobo M, et al. Epidemiology of renal cancer in developing countries: review of the literature. Can Urol Assoc J. 2018 Mar;12(3):E154. PubMed PMID: 29283089; PubMed Central PMCID: PMCPMC5869042.
  • Howlader N, Noone AM, Krapcho M, et al. SEER Cancer Statistics Review, 1975–2010. [Based on the November 2012 SEER data submission, posted to the SEER web site, April 2013.]. Bethesda, MD: National Cancer Institute. (2013; 9).
  • Jonasch E, Gao J, Rathmell WK. State of the art review: renal cell carcinoma. BMJ. 2014;349, g4797.
  • Wong MCS, Goggins WB, Yip BHK, et al. Incidence and mortality of kidney cancer: temporal patterns and global trends in 39 countries. Sci Rep. 2017;7(1):15698.
  • Hsieh JJ, Purdue MP, Signoretti S, et al. Renal cell carcinoma. Nat Rev Dis Primers. 2017;3:17009.
  • Ljungberg B, Campbell SC, Cho HY, et al. The epidemiology of renal cell carcinoma. Eur Urol. 2011;60(4):615–621.
  • Chow WH, Dong LM, Devesa SS. Epidemiology and risk factors for kidney cancer. Nat Rev Urol. 2010 May;7(5):245–257. PubMed PMID: 20448658; PubMed Central PMCID: PMCPMC3012455.
  • Nickerson ML, Jaeger E, Shi Y, et al. Improved identification of von Hippel-Lindau gene alterations in clear cell renal tumors. Clin Cancer Res. 2008 Aug 1;14(15):4726–4734. PubMed PMID: 18676741; PubMed Central PMCID: PMCPMC2629664.
  • Brugarolas J. Molecular genetics of clear-cell renal cell carcinoma. J clin oncol. 2014 Jun 20;32(18):1968. PubMed PMID: 24821879; PubMed Central PMCID: PMCPMC4050206.
  • Sanchez DJ, Simon MC. Genetic and metabolic hallmarks of clear cell renal cell carcinoma. Biochim Biophys Acta (BBA)- Rev Cancer. 2018 Aug;1870(1):23–31. PubMed PMID: 29959988.
  • Cho H, Kaelin WG editors. Targeting HIF2 in clear cell renal cell carcinoma. Cold Spring Harb Symp Quant Biol. 2016;81:113–121. Cold Spring Harbor Laboratory Press.
  • Semenza GL. Signal transduction to hypoxia-inducible factor 1. Biochem Pharmacol. 2002 Sep;64(5–6):993–998. PubMed PMID: 12213597.
  • Irwin DC, McCord JM, Nozik-Grayck E, et al. A potential role for reactive oxygen species and the HIF-1α–VEGF pathway in hypoxia-induced pulmonary vascular leak. Free Radic Biol Med. 2009;47(1):55–61.
  • Maxwell PH, Pugh CW, Ratcliffe PJ. Activation of the HIF pathway in cancer. Curr Opin Genet Dev. 2001 Jun;11(3):293–299. PubMed PMID: 11377966.
  • Shen C, Beroukhim R, Schumacher S, et al. Genetic and functional studies implicate HIF1α as a 14q kidney cancer suppressor gene. Cancer Dis. 2011: CD-11-0098.
  • Keith B, Johnson RS, Simon MC. HIF1α and HIF2α: sibling rivalry in hypoxic tumour growth and progression. Nat Rev Cancer. 2012;12(1):9.
  • Mitchell TJ, Rossi SH, Klatte T, et al. Genomics and clinical correlates of renal cell carcinoma. World J Urol. 2018 Aug, 36(12), 1899-1911. PubMed PMID: 30099580.
  • Hakimi AA, Pham CG, Hsieh JJ. A clear picture of renal cell carcinoma. Nat Genet. 2013 Aug;45(8):849. PubMed PMID: 23892664.
  • Lee H, Dai F, Zhuang L, et al. BAF180 regulates cellular senescence and hematopoietic stem cell homeostasis through p21. Oncotarget. 2016;7(15):19134.
  • Peña-Llopis S, Vega-Rubín-de-Celis S, Liao A, et al. BAP1 loss defines a new class of renal cell carcinoma. Nat Genet. 2012;44(7):751.
  • Motzer RJ, Barrios CH, Kim TM, et al. Phase II randomized trial comparing sequential first-line everolimus and second-line sunitinib versus first-line sunitinib and second-line everolimus in patients with metastatic renal cell carcinoma. J Clin Oncol. 2014 Sep 1;32(25):2765–2772. PubMed PMID: 25049330; PubMed Central PMCID: PMCPMC5569681.
  • Hsieh JJ, Chen D, Wang PI, et al. Genomic biomarkers of a randomized trial comparing first-line everolimus and sunitinib in patients with metastatic renal cell carcinoma. Eur Urol. 2017;71(3):405–414.
  • Porta C, Paglino C, Mosca A. Targeting PI3K/Akt/mTOR signaling in cancer. Front Oncol. 2014;4:64. PubMed PMID: 24782981; PubMed Central PMCID: PMCPMC3995050.
  • Conciatori F, Bazzichetto C, Falcone I, et al. Role of mTOR signaling in tumor microenvironment: an overview. Int J Mol Sci. 2018 Aug 19;19;8:2453. PubMed PMID: 30126252; PubMed Central PMCID: PMCPMC6121402.
  • Farhan MA, Carmine-Simmen K, Lewis JD, et al. Endothelial cell mTOR complex-2 regulates sprouting angiogenesis. PloS One. 2015;10(8):e0135245. PubMed PMID: 26295809; PubMed Central PMCID: PMCPMC4546419.
  • Porta C, Paglino C, Imarisio I. Sorafenib rechalenge in metastatic renal cell carcinoma. BJU Int. 2012 Sep;110(6b):E235–E235. PubMed PMID: 22332769.
  • Voss MH, Hakimi AA, Pham CG, et al. Tumor genetic analyses of patients with metastatic renal cell carcinoma and extended benefit from mTOR inhibitor therapy. Clin Cancer Res. 2014, 20(7); 1–10.
  • Kwiatkowski DJ, Choueiri TK, Fay AP, et al. Mutations in TSC1, TSC2, and MTOR are associated with response to rapalogs in patients with metastatic renal cell carcinoma. Clin Cancer Res. 2016 May 15;22(10):2445–2452. PubMed PMID: 26831717; PubMed Central PMCID: PMCPMC4976069.
  • Voss MH, Chen D, Reising A, et al. PTEN expression, not mutation status for TSC1, TSC2 or mTOR, correlates with outcome on everolimus in patients with renal cell carcinoma treated on RECORD-3. Clin Cancer Res. 2018. clincanres-1833.
  • Rodriguez-Vida A, Hutson TE, Bellmunt J, et al. New treatment options for metastatic renal cell carcinoma. ESMO Open. 2017;2(2):e000185.
  • Yang JC, Haworth L, Sherry RM, et al. A randomized trial of bevacizumab, an anti–vascular endothelial growth factor antibody, for metastatic renal cancer. N Engl J Med. 2003;349(5):427–434.
  • Escudier B, Porta C, Schmidinger M, et al. Renal cell carcinoma: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2014;25(suppl_3):iii49–iii56.
  • Ljungberg B, Bensalah K, Canfield S, et al. EAU guidelines on renal cell carcinoma: 2014 update. Eur Urol. 2015 May;67(5):913–924. PubMed PMID: 25616710.
  • Motzer RJ, Jonasch E, Agarwal N, et al. Kidney cancer, version 2.2017, NCCN clinical practice guidelines in oncology. J Natl Compr Canc Netw. 2017 Jun;15(6):804–834. PubMed PMID: 28596261.
  • Escudier B, Pluzanska A, Koralewski P, et al. Bevacizumab plus interferon alfa-2a for treatment of metastatic renal cell carcinoma: a randomised, double-blind phase III trial. Lancet. 2007 Dec 22;370(9605):2103–2111. PubMed PMID: 18156031.
  • Rini BI, Halabi S, Rosenberg JE, et al. Bevacizumab plus interferon alfa compared with interferon alfa monotherapy in patients with metastatic renal cell carcinoma: CALGB 90206. J Clin Oncol. 2008 Nov 20;26(33):5422. PubMed PMID: 18936475; PubMed Central PMCID: PMCPMC2651074.
  • Bracarda S, Bellmunt J, Melichar B, et al. Overall survival in patients with metastatic renal cell carcinoma initially treated with bevacizumab plus interferon‐α2a and subsequent therapy with tyrosine kinase inhibitors: a retrospective analysis of the phase III AVOREN trial. BJU Int. 2011;107(2):214–219.
  • Escudier B, Bellmunt J, Négrier S, et al. Phase III trial of bevacizumab plus interferon alfa-2a in patients with metastatic renal cell carcinoma (AVOREN): final analysis of overall survival. J Clin Oncol. 2010;28(13):2144–2150.
  • Rini BI, Halabi S, Rosenberg JE, et al. Phase III trial of bevacizumab plus interferon alfa versus interferon alfa monotherapy in patients with metastatic renal cell carcinoma: final results of CALGB 90206. J Clin Oncol. 2010 May 1;28(13):2137. PubMed PMID: 20368558; PubMed Central PMCID: PMCPMC2860433.
  • Motzer RJ, Hutson TE, Tomczak P, et al. Sunitinib versus interferon alfa in metastatic renal-cell carcinoma. N Engl J Med. 2007 Jan 11;356(2):115–124. PubMed PMID: 17215529.
  • Motzer RJ, Hutson TE, Tomczak P, et al. Overall survival and updated results for sunitinib compared with interferon alfa in patients with metastatic renal cell carcinoma. J Clin Oncol. 2009;27(22):3584.
  • Motzer RJ, Tannir NM, McDermott DF, et al. Nivolumab plus ipilimumab versus sunitinib in advanced renal-cell carcinoma. N Engl J Med. 2018 Apr 5;378(14):1277–1290. PubMed PMID: 29562145; PubMed Central PMCID: PMCPMC5972549.
  • Escudier B, Eisen T, Stadler WM, et al. Sorafenib in advanced clear-cell renal-cell carcinoma. N Engl J Med. 2007 Jan 11;356(2):125–134. PubMed PMID: 17215530.
  • Escudier B, Eisen T, Stadler WM, et al. Sorafenib for treatment of renal cell carcinoma: final efficacy and safety results of the phase III treatment approaches in renal cancer global evaluation trial. J Clin Oncol. 2009 Jul 10;27(20):3312–3318. PubMed PMID: 19451442.
  • Hutson TE, Escudier B, Esteban E, et al. Randomized phase III trial of temsirolimus versus sorafenib as second-line therapy after sunitinib in patients with metastatic renal cell carcinoma. J Clin Oncol. 2014;32(8):760–767.
  • 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 Feb 20;28(6):1061–1068. PubMed PMID: 20100962.
  • Motzer RJ, Hutson TE, Cella D, et al. Pazopanib versus sunitinib in metastatic renal-cell carcinoma. N Engl J Med. 2013 Aug 22;369(8):722–731. PubMed PMID: 23964934.
  • Escudier B, Porta C, Bono P, et al. Randomized, controlled, double-blind, cross-over trial assessing treatment preference for pazopanib versus sunitinib in patients with metastatic renal cell carcinoma: PISCES study. J Clin Oncol. 2014 May 10;32(14):1412–1418. PubMed PMID: 24687826.
  • 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 Dec 3;378(9807):1931–1939. PubMed PMID: 22056247; eng.
  • Hutson TE, Lesovoy V, Al-Shukri S, et al. Axitinib versus sorafenib as first-line therapy in patients with metastatic renal-cell carcinoma: a randomised open-label phase 3 trial. Lancet Oncol. 2013;14(13):1287–1294.
  • Choueiri TK, Escudier B, Powles T, et al. Cabozantinib versus everolimus in advanced renal-cell carcinoma. N Engl J Med. 2015 Nov 5;373(19):1814–1823. PubMed PMID: 26406150; PubMed Central PMCID: PMCPMC5024539.
  • Choueiri TK, Escudier B, Powles T, et al. Cabozantinib versus everolimus in advanced renal cell carcinoma (METEOR): final results from a randomised, open-label, phase 3 trial. Lancet Oncol. 2016;17(7):917–927. PubMed PMID: 27279544.
  • Choueiri TK, Halabi S, Sanford BL, et al. Cabozantinib versus sunitinib as initial targeted therapy for patients with metastatic renal cell carcinoma of poor or intermediate risk: the Alliance A031203 CABOSUN trial. J Clin Oncol. 2017;35(6):591–597.
  • Choueiri TK, Hessel C, Halabi S, et al. Cabozantinib versus sunitinib as initial therapy for metastatic renal cell carcinoma of intermediate or poor risk (Alliance A031203 CABOSUN randomised trial): progression-free survival by independent review and overall survival update. Eur J Cancer. 2018;94:115–125.
  • 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):3791–3799.
  • Garnick MB. Preserving the sanctity of overall survival for drugs approved on the basis of progression-free survival: tivozanib as a case study. J Clin Oncol. 2013.
  • Matsui J, Funahashi Y, Uenaka T, et al. Multi-kinase inhibitor E7080 suppresses lymph node and lung metastases of human mammary breast tumor MDA-MB-231 via inhibition of vascular endothelial growth factor-receptor (VEGF-R) 2 and VEGF-R3 kinase. Clin Cancer Res. 2008 Sep 1;14(17):5459–5465. PubMed PMID: 18765537.
  • Okamoto K, Kodama K, Takase K, et al. Antitumor activities of the targeted multi-tyrosine kinase inhibitor lenvatinib (E7080) against RET gene fusion-driven tumor models. Cancer Lett. 2013 Oct 28;340(1):97–103. PubMed PMID: 23856031.
  • Motzer RJ, Hutson TE, Glen H, et al. Lenvatinib, everolimus, and the combination in patients with metastatic renal cell carcinoma: a randomised, phase 2, open-label, multicentre trial. Lancet Oncol. 2015 Nov;16(15):1473–1482. PubMed PMID: 26482279.
  • Porta C, Sabbatini R, Procopio G, et al. Primary resistance to tyrosine kinase inhibitors in patients with advanced renal cell carcinoma: state-of-the-science. Expert Rev Anticancer Ther. 2012 Dec;12(12):1571–1577. PubMed PMID: 23181412.
  • Griffioen AW, Mans LA, de Graaf AMA, et al. Rapid angiogenesis onset after discontinuation of sunitinib treatment of renal cell carcinoma patients. Clin Cancer Res. 2012 Jul 15;18(14):3961–3971. PubMed PMID: 22573349; PubMed Central PMCID: PMCPMC4015630.
  • Mancuso MR, Davis R, Norberg SM, et al. Rapid vascular regrowth in tumors after reversal of VEGF inhibition. J Clin Invest. 2006 Oct;116(10):2610–2621. PubMed PMID: 17016557; PubMed Central PMCID: PMCPMC1578604.
  • Rankin EB, Fuh KC, Castellini L, et al. Direct regulation of GAS6/AXL signaling by HIF promotes renal metastasis through SRC and MET. Proc Nat Acad Sci. 2014;111(37):13373–13378.
  • Gibney GT, Aziz SA, Camp RL, et al. c-Met is a prognostic marker and potential therapeutic target in clear cell renal cell carcinoma. Ann Oncol. 2012;24(2):343–349.
  • Brodaczewska KK, Szczylik C, Kieda C. Immune consequences of anti-angiogenic therapyin renal cell carcinoma. J Oncol. 2018 Mar;22(1A):14. PubMed PMID: 29628789; PubMed Central PMCID: PMCPMC5885083.
  • Lee GR. Phenotypic and functional properties of tumor-infiltrating regulatory T cells. Mediators Inflamm. 2017;2017:5458178. PubMed PMID: 29463952; PubMed Central PMCID: PMCPMC5804416.
  • Vignali DAA, Collison LW, Workman CJ. How regulatory T cells work. Nat Rev Immunol. 2008;8(7):523.
  • Giallongo C, Tibullo D, Parrinello NL, et al. Granulocyte-like myeloid derived suppressor cells (G-MDSC) are increased in multiple myeloma and are driven by dysfunctional mesenchymal stem cells (MSC). Oncotarget. 2016 Dec 27;7(52):85764. PubMed PMID: 26967390; PubMed Central PMCID: PMCPMC5349872.
  • Gabrilovich DI, Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol. 2009;9(3):162.
  • Sevko A, Umansky V. Myeloid-derived suppressor cells interact with tumors in terms of myelopoiesis, tumorigenesis and immunosuppression: thick as thieves. J Cancer. 2013;4(1):3.
  • Serafini P, Mgebroff S, Noonan K, et al. Myeloid-derived suppressor cells promote cross-tolerance in B-cell lymphoma by expanding regulatory T cells. Cancer Res. 2008 Jul 1;68(13):5439–5449. PubMed PMID: 18593947; PubMed Central PMCID: PMCPMC2887390.
  • Farsaci B, Higgins JP, Hodge JW. Consequence of dose scheduling of sunitinib on host immune response elements and vaccine combination therapy. Int J Cancer. 2012 Apr 15;130(8):1948–1959. PubMed PMID: 21633954; PubMed Central PMCID: PMCPMC3232304.
  • Terme M, Pernot S, Marcheteau E, et al. VEGFA-VEGFR pathway blockade inhibits tumor-induced regulatory T-cell proliferation in colorectal cancer. Cancer Res. 2013 Jan 15;73(2):539–549. PubMed PMID: 23108136; eng.
  • Chen ML, Yan BS, Lu WC, et al. Sorafenib relieves cell-intrinsic and cell-extrinsic inhibitions of effector T cells in tumor microenvironment to augment antitumor immunity. Int J Cancer. 2014 Jan 15;134(2):319–331. PubMed PMID: 23818246; eng.
  • Cabrera R, Ararat M, Xu Y, et al. Immune modulation of effector CD4+ and regulatory T cell function by sorafenib in patients with hepatocellular carcinoma. Cancer Immunol Immunother. 2013 Apr;62(4):737–746. PubMed PMID: 23223899; PubMed Central PMCID: PMCPMC3863727. eng.
  • Jain RK. Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science (New York, NY). 2005 Jan 7;307(5706):58–62. PubMed PMID: 15637262; eng.
  • Jain RK. Normalizing tumor vasculature with anti-angiogenic therapy: a new paradigm for combination therapy. Nat Med. 2001 Sep;7(9):987–989. PubMed PMID: 11533692; eng.
  • Goel S, Duda DG, Xu L, et al. Normalization of the vasculature for treatment of cancer and other diseases. Physiol Rev. 2011 Jul;91(3):1071–1121. PubMed PMID: 21742796; PubMed Central PMCID: PMCPMC3258432. eng.
  • Dirkx AE, Oude Egbrink MG, Castermans K, et al. Anti-angiogenesis therapy can overcome endothelial cell anergy and promote leukocyte-endothelium interactions and infiltration in tumors. FASEB J. 2006 Apr;20(6):621–630. PubMed PMID: 16581970; eng.
  • Griffioen AW, Damen CA, Blijham GH, et al. Tumor angiogenesis is accompanied by a decreased inflammatory response of tumor-associated endothelium. Blood. 1996 Jul 15;88(2):667–673. PubMed PMID: 8695814; eng.
  • Messai Y, Gad S, Noman MZ, et al. Renal cell carcinoma programmed death-ligand 1, a new direct target of hypoxia-inducible factor-2 alpha, is regulated by von Hippel-Lindau gene mutation status. Eur Urol. 2016 Oct;70(4):623–632. PubMed PMID: 26707870; eng.
  • Amin A, Plimack ER, Infante JR, et al. Nivolumab (anti-PD-1; BMS-936558, ONO-4538) in combination with sunitinib or pazopanib in patients (pts) with metastatic renal cell carcinoma (mRCC). J clin oncol. 2014;32(15_suppl):5010.
  • McDermott DF, Atkins MB, Motzer RJ, et al. A phase II study of atezolizumab (atezo) with or without bevacizumab (bev) versus sunitinib (sun) in untreated metastatic renal cell carcinoma (mRCC) patients (pts). J clin oncol. 2017;35(6_suppl):431.
  • Motzer RJ, Powles T, Atkins MB, et al. IMmotion151: a randomized phase III study of atezolizumab plus bevacizumab vs sunitinib in untreated Metastatic Renal Cell Carcinoma (mRCC). J Clin Oncol. 2018;36(6_suppl):578.
  • Motzer RJ, Penkov K, Haanen JBAG, et al. LBA6_PRJAVELIN renal 101: A randomized, phase III study of avelumab + axitinib vs sunitinib as first-line treatment of advanced renal cell carcinoma (aRCC). Ann Oncol. 2018;29(suppl_8):mdy424.036-mdy424.036.
  • [cited 2018 Oct 30]. https://investors.merck.com/news/press-release-details/2018/Mercks-KEYTRUDA-pembrolizumab-in-Combination-with-Pfizers-Inlyta-axitinib-Significantly-Improved-Overall-Survival-OS-and-Progression-free-Survival-PFS-as-First-Line-Therapy-for-Advanced-or-Metastatic-Renal-Cell-Carcinoma/default.aspx
  • Motzer RJ, Grünwald V, Hutson TE, et al. A phase III trial to compare efficacy and safety of lenvatinib in combination with everolimus or pembrolizumab vs sunitinib alone in first-line treatment of patients (Pts) with metastatic renal cell carcinoma (RCC). J Clin Oncol. 2017.
  • Schödel J, Grampp S, Maher ER, et al. Hypoxia, hypoxia-inducible transcription factors, and renal cancer. Eur Urol. 2016;69(4):646–657. PubMed PMID: 26298207; PubMed Central PMCID: PMCPMC5012644.
  • Courtney KD, Infante JR, Lam ET, et al. Phase I dose-escalation trial of PT2385, a first-in-class hypoxia-inducible factor-2α antagonist in patients with previously treated advanced clear cell renal cell carcinoma. J Clin Oncol. 2018 Mar 20;36(9):867–874. PubMed PMID: 29257710; PubMed Central PMCID: PMCPMC5946714.
  • Noman MZ, Desantis G, Janji B, et al. PD-L1 is a novel direct target of HIF-1α, and its blockade under hypoxia enhanced MDSC-mediated T cell activation. J Exp Med. 2014;211(5):781–790.
  • Barsoum IB, Koti M, Siemens DR, et al. Mechanisms of hypoxia-mediated immune escape in cancer. Cancer Res. 2014 Dec 15;74(24):7185–7190. PubMed PMID: 25344227.
  • Ruf M, Moch H, Schraml P. PD-L1 expression is regulated by hypoxia inducible factor in clear cell renal cell carcinoma. Int J Cancer. 2016 Jul 15;139(2):396–403. PubMed PMID: 26945902.
  • Vogelzang NJ. Treatment options in metastatic renal carcinoma: an embarrassment of riches. J Clin Oncol. 2006 Jan 1;24(1):1–3. PubMed PMID: 16330665.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.