Anti-proliferative but not anti-angiogenic tyrosine kinase inhibitors enrich for cancer stem cells in soft tissue sarcoma

BMC Cancer

Volumn 14, Issue 1, 2014, Pages

  Canter, Robert J ^a   Ames, Erik ^a   Mac, Stephanie ^a   Grossenbacher, Steven K ^a   Chen, Mingyi ^a   Li, Chin Shang ^b   Borys, Dariusz ^a   Smith, Rachel C ^a   Tellez, Joe ^a   Sayers, Thomas J ^c   Monjazeb, Arta M ^a   Murphy, William J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

Author keywords

ALDH; Cancer stem cells; Pazopanib; Regorafenib; Soft tissue sarcoma; Sorafenib; Tyrosine kinase inhibitors

Indexed keywords

ALDEHYDE DEHYDROGENASE; CD133 ANTIGEN; CD24 ANTIGEN; HERMES ANTIGEN; PAZOPANIB; PLACEBO; PROTEIN TYROSINE KINASE INHIBITOR; REGORAFENIB; SORAFENIB; ALDEHYDE DEHYDROGENASE ISOENZYME 1; ANGIOGENESIS INHIBITOR; CARBANILAMIDE DERIVATIVE; ISOENZYME; LEUKOCYTE ANTIGEN; NICOTINAMIDE; PROTEIN KINASE INHIBITOR; PYRIMIDINE DERIVATIVE; RETINAL DEHYDROGENASE; SULFONAMIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CANCER ADJUVANT THERAPY; CANCER STEM CELL; CANCER SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG EXPOSURE; DRUG MECHANISM; FEMALE; FLOW CYTOMETRY; HISTOLOGY; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; LIVER METASTASIS; LUNG METASTASIS; MOUSE; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; SARCOMA CELL LINE; SOFT TISSUE SARCOMA; TISSUE MICROARRAY; TUMOR XENOGRAFT; ANALOGS AND DERIVATIVES; ANIMAL; CELL PROLIFERATION; CELL SURVIVAL; DRUG EFFECTS; DRUG SCREENING; LIVER NEOPLASMS; LUNG NEOPLASMS; METABOLISM; NEOADJUVANT THERAPY; NONOBESE DIABETIC MOUSE; SARCOMA; SECONDARY; TUMOR CELL LINE;

ANGIOGENESIS INHIBITORS; ANIMALS; ANTIGENS, CD; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; FEMALE; HUMANS; ISOENZYMES; LIVER NEOPLASMS; LUNG NEOPLASMS; MICE, INBRED NOD; NEOADJUVANT THERAPY; NEOPLASTIC STEM CELLS; NIACINAMIDE; PHENYLUREA COMPOUNDS; PROTEIN KINASE INHIBITORS; PYRIMIDINES; RETINAL DEHYDROGENASE; SARCOMA; SULFONAMIDES; TISSUE ARRAY ANALYSIS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84988528048     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-14-756     Document Type: Article

References (37)

1. Visvader JE, Lindeman GJ: Cancer stem cells: current status and evolving complexities. Cell Stem Cell 2012, 10(6):717-728.
2. Ishizawa K, Rasheed ZA, Karisch R, Wang Q, Kowalski J, Susky E, Pereira K, Karamboulas C, Moghal N, Rajeshkumar NV, Hidalgo M, Tsao M, Ailles L, Waddell TK, Maitra A, Neel BG, Matsui W: Tumor-initiating cells are rare in many human tumors. Cell Stem Cell 2010, 7(3):279-282.
3. Chen J, Li Y, Yu TS, McKay RM, Burns DK, Kernie SG, Parada LF: A restricted cell population propagates glioblastoma growth after chemotherapy. Nature 2012, 488(7412):522-526.
4. Jiang X, Gwye Y, Russell D, Cao C, Douglas D, Hung L, Kovar H, Triche TJ, Lawlor ER: CD133 expression in chemo-resistant Ewing sarcoma cells. BMC Cancer 2010, 10:116.
5. Li X, Lewis MT, Huang J, Gutierrez C, Osborne CK, Wu MF, Hilsenbeck SG, Pavlick A, Zhang X, Chamness GC, Wong H, Rosen J, Chang JC: Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy. J Natl Cancer Inst 2008, 100(9):672-679.
6. Charafe-Jauffret E, Ginestier C, Bertucci F, Cabaud O, Wicinski J, Finetti P, Josselin E, Adelaide J, Nguyen TT, Monville F, Jacquemier J, Thomassin-Piana J, Pinna G, Jalaguier A, Lambaudie E, Houvenaeghel G, Xerri L, Harel-Bellan A, Chaffanet M, Viens P, Birnbaum D: ALDH1-positive cancer stem cells predict engraftment of primary breast tumors and are governed by a common stem cell program. Cancer Res 2013, 73(24):7290-7300.
7. van den Hoogen C, van der Horst G, Cheung H, Buijs JT, Lippitt JM, Guzman-Ramirez N, Hamdy FC, Eaton CL, Thalmann GN, Cecchini MG, Pelger RC, van der Pluijm G: High aldehyde dehydrogenase activity identifies tumor-initiating and metastasis-initiating cells in human prostate cancer. Cancer Res 2010, 70(12):5163-5173.
8. Wang L, Park P, Zhang H, La Marca F, Lin CY: Prospective identification of tumorigenic osteosarcoma cancer stem cells in OS99-1 cells based on high aldehyde dehydrogenase activity. Int J Cancer 2011, 128(2):294-303.
9. Schepers AG, Snippert HJ, Stange DE, van den Born M, van Es JH, van de Wetering M, Clevers H: Lineage tracing reveals Lgr5+ stem cell activity in mouse intestinal adenomas. Science 2012, 337(6095):730-735.
10. Driessens G, Beck B, Caauwe A, Simons BD, Blanpain C: Defining the mode of tumour growth by clonal analysis. Nature 2012, 488(7412):527-530.
11. Dela Cruz FS: Cancer stem cells in pediatric sarcomas. Front Oncol 2013, 3:168.
12. Valent P, Bonnet D, De Maria R, Lapidot T, Copland M, Melo JV, Chomienne C, Ishikawa F, Schuringa JJ, Stassi G, Huntly B, Herrmann H, Soulier J, Roesch A, Schuurhuis GJ, Wöhrer S, Arock M, Zuber J, Cerny-Reiterer S, Johnsen HE, Andreeff M, Eaves C: Cancer stem cell definitions and terminology: the devil is in the details. Nat Rev Cancer 2012, 12(11):767-775.
13. Charafe-Jauffret E, Ginestier C, Iovino F, Tarpin C, Diebel M, Esterni B, Houvenaeghel G, Extra JM, Bertucci F, Jacquemier J, Xerri L, Dontu G, Stassi G, Xiao Y, Barsky SH, Birnbaum D, Viens P, Wicha MS: Aldehyde dehydrogenase 1-positive cancer stem cells mediate metastasis and poor clinical outcome in inflammatory breast cancer. Clin Cancer Res 2010, 16(1):45-55.
14. Deng S, Yang X, Lassus H, Liang S, Kaur S, Ye Q, Li C, Wang LP, Roby KF, Orsulic S, Connolly DC, Zhang Y, Montone K, Bützow R, Coukos G, Zhang L: Distinct expression levels and patterns of stem cell marker, aldehyde dehydrogenase isoform 1 (ALDH1), in human epithelial cancers. PLoS One 2010, 5(4):e10277.
15. Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, Brown M, Jacquemier J, Viens P, Kleer CG, Liu S, Schott A, Hayes D, Birnbaum D, Wicha MS, Dontu G: ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 2007, 1(5):555-567.
16. Kitamura H, Torigoe T, Hirohashi Y, Asanuma H, Inoue R, Nishida S, Tanaka T, Fukuta F, Masumori N, Sato N, Tsukamoto T: Prognostic impact of the expression of ALDH1 and SOX2 in urothelial cancer of the upper urinary tract. Mod Pathol 2013, 26(1):117-124.
17. Le Magnen C, Bubendorf L, Rentsch CA, Mengus C, Gsponer J, Zellweger T, Rieken M, Thalmann GN, Cecchini MG, Germann M, Bachmann A, Wyler S, Heberer M, Spagnoli GC: Characterization and clinical relevance of ALDHbright populations in prostate cancer. Clin Cancer Res 2013, 19(19):5361-5371.
18. Li T, Su Y, Mei Y, Leng Q, Leng B, Liu Z, Stass SA, Jiang F: ALDH1A1 is a marker for malignant prostate stem cells and predictor of prostate cancer patients' outcome. Lab Invest 2010, 90(2):234-244.
19. Awad O, Yustein JT, Shah P, Gul N, Katuri V, O'Neill A, Kong Y, Brown ML, Toretsky JA, Loeb DM: High ALDH activity identifies chemotherapyresistant Ewing's sarcoma stem cells that retain sensitivity to EWS-FLI1 inhibition. PLoS One 2010, 5(11):e13943.
20. Wilhelm SM, Carter C, Tang L, Wilkie D, McNabola A, Rong H, Chen C, Zhang X, Vincent P, McHugh M, Cao Y, Shujath J, Gawlak S, Eveleigh D, Rowley B, Liu L, Adnane L, Lynch M, Auclair D, Taylor I, Gedrich R, Voznesensky A, Riedl B, Post LE, Bollag G, Trail PA: 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(19):7099-7109.
21. Hasskarl J: Sorafenib: targeting multiple tyrosine kinases in cancer. Recent Results Cancer Res 2014, 201:145-164.
22. Maki RG, D'Adamo DR, Keohan ML, Saulle M, Schuetze SM, Undevia SD, Livingston MB, Cooney MM, Hensley ML, Mita MM, Takimoto CH, Kraft AS, Elias AD, Brockstein B, Blachère NE, Edgar MA, Schwartz LH, Qin LX, Antonescu CR, Schwartz GK: Phase II study of sorafenib in patients with metastatic or recurrent sarcomas. Clin Cancer Res 2009, 27(19):3133-3140.
23. von Mehren M, Rankin C, Goldblum JR, Demetri GD, Bramwell V, Ryan CW, Borden E: Phase 2 Southwest Oncology Group-directed intergroup trial (S0505) of sorafenib in advanced soft tissue sarcomas. Cancer 2012, 118(3):770-776.
24. Canter RJ, Borys D, Olusanya A, Li CS, Lee LY, Boutin RD, Christensen SD, Tamurian RM, Monjazeb AM: Phase I trial of Neoadjuvant conformal radiotherapy plus sorafenib for patients with locally advanced soft tissue sarcoma of the extremity. Ann Surg Oncol 2014, 21(5):1616-1623.
25. Hamed HA, Tavallai S, Grant S, Poklepovic A, Dent P: Sorafenib/Regorafenib and Lapatinib interact to kill CNS tumor cells. J Cell Physiol 2015, 230(1):131-139.
26. Ettrich TJ, Seufferlein T: Regorafenib. Recent Results Cancer Res 2014, 201:185-196.
27. Ranieri G, Mammi M, Donato Di Paola E, Russo E, Gallelli L, Citraro R, Gadaleta CD, Marech I, Ammendola M, De Sarro G: Pazopanib a tyrosine kinase inhibitor with strong anti-angiogenetic activity: a new treatment for metastatic soft tissue sarcoma. Crit Rev Oncol Hematol 2014, 89(2):322-329.
28. van der Graaf WT, Blay JY, Chawla SP, Kim DW, Bui-Nguyen B, Casali PG, Schoffski P, Aglietta M, Staddon AP, Beppu Y, Le Cesne A, Gelderblom H, Judson IR, Araki N, Ouali M, Marreaud S, Hodge R, Dewji MR, Coens C, Demetri GD, Fletcher CD, Dei Tos AP, Hohenberger P, EORTC Soft Tissue and Bone Sarcoma Group; PALETTE study group: Pazopanib for metastatic soft-tissue sarcoma (PALETTE): a randomised, double-blind, placebocontrolled phase 3 trial. Lancet 2012, 379(9829):1879-1886.
29. McCormack PL: Pazopanib: a review of its use in the management of advanced renal cell carcinoma. Drugs 2014, 74(10):1111-1125.
30. Guryanova OA, Wu Q, Cheng L, Lathia JD, Huang Z, Yang J, MacSwords J, Eyler CE, McLendon RE, Heddleston JM, Shou W, Hambardzumyan D, Lee J, Hjelmeland AB, Sloan AE, Bredel M, Stark GR, Rich JN, Bao S: Nonreceptor tyrosine kinase BMX maintains self-renewal and tumorigenic potential of glioblastoma stem cells by activating STAT3. Cancer Cell 2011, 19(4):498-511.
31. Plastaras JP, Kim SH, Liu YY, Dicker DT, Dorsey JF, McDonough J, Cerniglia G, Rajendran RR, Gupta A, Rustgi AK, Diehl JA, Smith CD, Flaherty KT, El-Deiry WS: Cell cycle dependent and schedule-dependent antitumor effects of sorafenib combined with radiation. Cancer Res 2007, 67(19):9443-9454.
32. Honoki K, Fujii H, Kubo A, Kido A, Mori T, Tanaka Y, Tsujiuchi T: Possible involvement of stem-like populations with elevated ALDH1 in sarcomas for chemotherapeutic drug resistance. Oncol Rep 2010, 24(2):501-505.
33. Tanei T, Morimoto K, Shimazu K, Kim SJ, Tanji Y, Taguchi T, Tamaki Y, Noguchi S: Association of breast cancer stem cells identified by aldehyde dehydrogenase 1 expression with resistance to sequential Paclitaxel and epirubicin-based chemotherapy for breast cancers. Clin Cancer Res 2009, 15(12):4234-4241.
34. Chen J, Guo T, Zhang L, Qin LX, Singer S, Maki RG, Taguchi T, Dematteo R, Besmer P, Antonescu CR: CD133 and CD44 are universally overexpressed in GIST and do not represent cancer stem cell markers. Genes Chromosomes Cancer 2012, 51(2):186-195.
35. Trucco M, Loeb D: Sarcoma stem cells: do we know what we are looking for? Sarcoma 2012, 2012:291705.
36. Lipinski M, Braham K, Philip I, Wiels J, Philip T, Goridis C, Lenoir GM, Tursz T: Neuroectoderm-associated antigens on Ewing's sarcoma cell lines. Cancer Res 1987, 47(1):183-187.
37. Moody SA, Klein SL, Karpinski BA, Maynard TM, Lamantia AS: On becoming neural: what the embryo can tell us about differentiating neural stem cells. Am J Stem Cells 2013, 2(2):74-94.