Predictive value of sphingosine kinase 1 expression in neoadjuvant treatment of breast cancer

Journal of Cancer Research and Clinical Oncology

Volumn 139, Issue 10, 2013, Pages 1681-1689

  Ruckhäberle, Eugen ^a   Karn, Thomas ^a   Denkert, Carsten ^b   Loibl, Sibylle ^c   Ataseven, Beyhan ^d   Reimer, Toralf ^e   Becker, Sven ^a   Holtrich, Uwe ^a   Rody, Achim ^f   Darb Esfahani, Silvia ^b   Nekljudova, Valentina ^c   Von Minckwitz, Gunter ^a,c  

^a GOETHE UNIVERSITY   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c GERMAN BREAST GROUP   (Germany)

^d Rotkreuzklinikum ^*  (Germany)

^e Hospital Klinikum Südstadt   (Germany)

^f UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

Author keywords

Breast cancer; Neoadjuvant systemic therapy; Prediction of response; Sphingolipids

Indexed keywords

CYCLOPHOSPHAMIDE; DOCETAXEL; DOXORUBICIN; ESTROGEN RECEPTOR; RECOMBINANT GRANULOCYTE COLONY STIMULATING FACTOR; SPHINGOSINE KINASE 1; TAMOXIFEN;

ADJUVANT THERAPY; ADULT; AGE; ARTICLE; BREAST BIOPSY; BREAST CANCER; CANCER ADJUVANT THERAPY; CANCER GRADING; CANCER SURVIVAL; COHORT ANALYSIS; CONTROLLED STUDY; DRUG RESPONSE; FEMALE; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MULTICENTER STUDY (TOPIC); MULTIPLE CYCLE TREATMENT; PREDICTIVE VALUE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RANDOMIZED CONTROLLED TRIAL (TOPIC); SCORING SYSTEM; TISSUE MICROARRAY;

BREAST NEOPLASMS; CHEMOTHERAPY, ADJUVANT; DISEASE-FREE SURVIVAL; FEMALE; HUMANS; KAPLAN-MEIER ESTIMATE; MIDDLE AGED; NEOADJUVANT THERAPY; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PROPORTIONAL HAZARDS MODELS; RANDOMIZED CONTROLLED TRIALS AS TOPIC; RECEPTOR, ERBB-2; RECEPTORS, ESTROGEN; TREATMENT OUTCOME;

EID: 84884674485     PISSN: 01715216     EISSN: 14321335     Source Type: Journal    
DOI: 10.1007/s00432-013-1490-5     Document Type: Article

References (37)

1. Antoon JW, Meacham WD, Bratton MR, Slaughter EM, Rhodes LV, Ashe HB, Wiese TE, Burow ME, Beckman BS (2011) Pharmacological inhibition of sphingosine kinase isoforms alters estrogen receptor signaling in human breast cancer. J Mol Endocrinol 46(3):205-216. doi: 10.1530/JME-10-0116
2. Antoon JW, White MD, Driver JL, Burow ME, Beckman BS (2012) Sphingosine kinase isoforms as a therapeutic target in endocrine therapy resistant luminal and basal-A breast cancer. Exp Biol Med (Maywood) 237(7):832-844. doi: 10.1258/ebm.2012.012028
3. Darb-Esfahani S, Loibl S, Müller BM, Roller M, Denkert C, Komor M, Schlüns K, Blohmer JU, Budczies J, Gerber B, Noske A, Du Bois A, Weichert W, Jackisch C, Dietel M, Richter K, Kaufmann M, von Minckwitz G (2009) Identification of biology-based breast cancer types with distinct predictive and prognostic features: role of steroid hormone and HER2 receptor expression in patients treated with neoadjuvant anthracycline/taxane-based chemotherapy. Breast Cancer Res 11(5):R69. doi: 10.1186/bcr2363
4. Elston CW, Ellis IO (1991) Pathological prognostic factors in breast cancer. I. The value of histological grade in breast cancer: experience from a large study with long-term follow-up. Histopathology 19(5):403-410
5. Furuya H, Shimizu Y, Kawamori T (2011) Sphingolipids in cancer. Cancer Metastasis Rev 30(3-4):567-576. doi: 10.1007/s10555-011-9304-1
6. Fyrst H, Saba JD (2010) An update on sphingosine-1-phosphate and other sphingolipid mediators. Nat Chem Biol 6(7):489-497. doi: 10.1038/nchembio.392
7. Goldhirsch A, Wood WC, Coates AS, Gelber RD, Thürlimann B, Senn H (2011) Strategies for subtypes - dealing with the diversity of breast cancer: highlights of the St. Gallen International Expert Consensus on the Primary Therapy of Early Breast Cancer 2011. Ann Oncol 22(8):1736-1747. doi: 10.1093/annonc/mdr304
8. Hait NC, Oskeritzian CA, Paugh SW, Milstien S, Spiegel S (2006) Sphingosine kinases, sphingosine 1-phosphate, apoptosis and diseases. Biochim Biophys Acta 1758(12):2016-2026. doi: 10.1016/j.bbamem.2006.08.007
9. Iwamoto T, Bianchini G, Booser D, Qi Y, Coutant C, Shiang CY, Santarpia L, Matsuoka J, Hortobagyi GN, Symmans WF, Holmes FA, O'Shaughnessy J, Hellerstedt B, Pippen J, Andre F, Simon R, Pusztai L (2011) Gene pathways associated with prognosis and chemotherapy sensitivity in molecular subtypes of breast cancer. J Natl Cancer Inst 103(3):264-272. doi: 10.1093/jnci/djq524
10. Juul N, Szallasi Z, Eklund AC, Li Q, Burrell RA, Gerlinger M, Valero V, Andreopoulou E, Esteva FJ, Symmans WF, Desmedt C, Haibe-Kains B, Sotiriou C, Pusztai L, Swanton C (2010) Assessment of an RNA interference screen-derived mitotic and ceramide pathway metagene as a predictor of response to neoadjuvant paclitaxel for primary triple-negative breast cancer: a retrospective analysis of five clinical trials. Lancet Oncol 11(4):358-365. doi: 10.1016/S1470-2045(10) 70018-8
11. Kaufmann M, Pusztai L (2011) Use of standard markers and incorporation of molecular markers into breast cancer therapy: consensus recommendations from an International Expert Panel. Cancer 117(8):1575-1582. doi: 10.1002/cncr.25660
12. Kaufmann M, von Minckwitz G, Mamounas EP, Cameron D, Carey LA, Cristofanilli M, Denkert C, Eiermann W, Gnant M, Harris JR, Karn T, Liedtke C, Mauri D, Rouzier R, Ruckhaeberle E, Semiglazov V, Symmans WF, Tutt A, Pusztai L (2012) Recommendations from an international consensus conference on the current status and future of neoadjuvant systemic therapy in primary breast cancer. Ann Surg Oncol 19(5):1508-1516. doi: 10.1245/s10434-011-2108-2
13. Lee AJX, Roylance R, Sander J, Gorman P, Endesfelder D, Kschischo M, Jones NP, East P, Nicke B, Spassieva S, Obeid LM, Birkbak NJ, Szallasi Z, McKnight NC, Rowan AJ, Speirs V, Hanby AM, Downward J, Tooze SA, Swanton C (2012) CERT depletion predicts chemotherapy benefit and mediates cytotoxic and polyploid-specific cancer cell death through autophagy induction. J Pathol 226(3):482-494. doi: 10.1002/path.2998
14. Long JS, Edwards J, Watson C, Tovey S, Mair KM, Schiff R, Natarajan V, Pyne NJ, Pyne S (2010) Sphingosine kinase 1 induces tolerance to human epidermal growth factor receptor 2 and prevents formation of a migratory phenotype in response to sphingosine 1-phosphate in estrogen receptor-positive breast cancer cells. Mol Cell Biol 30(15):3827-3841. doi: 10.1128/MCB.01133-09
15. Makhoul I, Kiwan E (2011) Neoadjuvant systemic treatment of breast cancer. J Surg Oncol 103(4):348-357. doi: 10.1002/jso.21696
16. McShane LM, Altman DG, Sauerbrei W, Taube SE, Gion M, Clark GM (2005) Reporting recommendations for tumor marker prognostic studies. J Clin Oncol 23(36):9067-9072. doi: 10.1200/JCO.2004.01.0454
17. Meacham WD, Antoon JW, Burow ME, Struckhoff AP, Beckman BS (2009) Sphingolipids as determinants of apoptosis and chemoresistance in the MCF-7 cell model system. Exp Biol Med (Maywood) 234(11):1253-1263. doi: 10.3181/0902-MR-77
18. Ogretmen B, Hannun YA (2004) Biologically active sphingolipids in cancer pathogenesis and treatment. Nat Rev Cancer 4(8):604-616. doi: 10.1038/nrc1411
19. Ohotski J, Long JS, Orange C, Elsberger B, Mallon E, Doughty J, Pyne S, Pyne NJ, Edwards J (2012) Expression of sphingosine 1-phosphate receptor 4 and sphingosine kinase 1 is associated with outcome in oestrogen receptor-negative breast cancer. Br J Cancer 106(8):1453-1459. doi: 10.1038/bjc.2012.98
20. Ohotski J, Edwards J, Elsberger B, Watson C, Orange C, Mallon E, Pyne S, Pyne NJ (2013) Identification of novel functional and spatial associations between sphingosine kinase 1, sphingosine 1-phosphate receptors and other signaling proteins that affect prognostic outcome in estrogen receptor-positive breast cancer. Int J Cancer 132(3):605-616. doi: 10.1002/ijc.27692
21. Ponnusamy S, Meyers-Needham M, Senkal CE, Saddoughi SA, Sentelle D, Selvam SP, Salas A, Ogretmen B (2010) Sphingolipids and cancer: ceramide and sphingosine-1-phosphate in the regulation of cell death and drug resistance. Future Oncol 6(10):1603-1624. doi: 10.2217/fon.10.116
22. Rody A, Karn T, Solbach C, Gaetje R, Munnes M, Kissler S, Ruckhäberle E, Minckwitz GV, Loibl S, Holtrich U, Kaufmann M (2007) The erbB2+ cluster of the intrinsic gene set predicts tumor response of breast cancer patients receiving neoadjuvant chemotherapy with docetaxel, doxorubicin and cyclophosphamide within the GEPARTRIO trial. Breast 16(3):235-240. doi: 10.1016/j.breast.2007.02.006
23. Rouzier R, Perou CM, Symmans WF, Ibrahim N, Cristofanilli M, Anderson K, Hess KR, Stec J, Ayers M, Wagner P, Morandi P, Fan C, Rabiul I, Ross JS, Hortobagyi GN, Pusztai L (2005) Breast cancer molecular subtypes respond differently to preoperative chemotherapy. Clin Cancer Res 11(16):5678-5685. doi: 10.1158/1078-0432.CCR-04-2421
24. Ruckhäberle E, Rody A, Engels K, Gaetje R, von Minckwitz G, Schiffmann S, Grösch S, Geisslinger G, Holtrich U, Karn T, Kaufmann M (2008) Microarray analysis of altered sphingolipid metabolism reveals prognostic significance of sphingosine kinase 1 in breast cancer. Breast Cancer Res Treat 112(1):41-52. doi: 10.1007/s10549-007-9836-9
25. Sarkar S, Maceyka M, Hait NC, Paugh SW, Sankala H, Milstien S, Spiegel S (2005) Sphingosine kinase 1 is required for migration, proliferation and survival of MCF-7 human breast cancer cells. FEBS Lett 579(24):5313-5317. doi: 10.1016/j.febslet.2005.08.055
26. Sauer L, Nunes J, Salunkhe V, Skalska L, Kohama T, Cuvillier O, Waxman J, Pchejetski D (2009) Sphingosine kinase 1 inhibition sensitizes hormone-resistant prostate cancer to docetaxel. Int J Cancer 125(11):2728-2736. doi: 10.1002/ijc.24640
27. Schulz KF, Altman DG, Moher D (2010) CONSORT 2010 Statement: updated guidelines for reporting parallel group randomised trials. J Clin Epidemiol 63(8):834-840. doi: 10.1016/j.jclinepi.2010.02.005
28. Sobue S, Nemoto S, Murakami M, Ito H, Kimura A, Gao S, Furuhata A, Takagi A, Kojima T, Nakamura M, Ito Y, Suzuki M, Banno Y, Nozawa Y, Murate T (2008) Implications of sphingosine kinase 1 expression level for the cellular sphingolipid rheostat: relevance as a marker for daunorubicin sensitivity of leukemia cells. Int J Hematol 87(3):266-275. doi: 10.1007/s12185-008-0052-0
29. Spiegel S (1999) Sphingosine 1-phosphate: a prototype of a new class of second messengers. J Leukoc Biol 65(3):341-344
30. Sukocheva OA, Wang L, Albanese N, Pitson SM, Vadas MA, Xia P (2003) Sphingosine kinase transmits estrogen signaling in human breast cancer cells. Mol Endocrinol 17(10):2002-2012. doi: 10.1210/me.2003-0119
31. Sukocheva O, Wadham C, Holmes A, Albanese N, Verrier E, Feng F, Bernal A, Derian CK, Ullrich A, Vadas MA, Xia P (2006) Estrogen transactivates EGFR via the sphingosine 1-phosphate receptor Edg-3: the role of sphingosine kinase-1. J Cell Biol 173(2):301-310. doi: 10.1083/jcb.200506033
32. Sukocheva O, Wadham C, Xia P (2009a) Role of sphingolipids in the cytoplasmic signaling of estrogens. Steroids 74(7):562-567. doi: 10.1016/j.steroids.2008.12.014
33. Sukocheva O, Wang L, Verrier E, Vadas MA, Xia P (2009b) Restoring endocrine response in breast cancer cells by inhibition of the sphingosine kinase-1 signaling pathway. Endocrinology 150(10):4484-4492. doi: 10.1210/en.2009-0391
34. Takabe K, Kim RH, Allegood JC, Mitra P, Ramachandran S, Nagahashi M, Harikumar KB, Hait NC, Milstien S, Spiegel S (2010) Estradiol induces export of sphingosine 1-phosphate from breast cancer cells via ABCC1 and ABCG2. J Biol Chem 285(14):10477-10486. doi: 10.1074/jbc.M109.064162
35. von Minckwitz G, Raab G, Caputo A, Schütte M, Hilfrich J, Blohmer JU, Gerber B, Costa SD, Merkle E, Eidtmann H, Lampe D, Jackisch C, Du Bois A, Kaufmann M (2005) Doxorubicin with cyclophosphamide followed by docetaxel every 21 days compared with doxorubicin and docetaxel every 14 days as preoperative treatment in operable breast cancer: the GEPARDUO study of the German Breast Group. J Clin Oncol 23(12):2676-2685. doi: 10.1200/JCO.2005.05.078
36. von Minckwitz G, Untch M, Blohmer J, Costa SD, Eidtmann H, Fasching PA, Gerber B, Eiermann W, Hilfrich J, Huober J, Jackisch C, Kaufmann M, Konecny GE, Denkert C, Nekljudova V, Mehta K, Loibl S (2012) Definition and impact of pathologic complete response on prognosis after neoadjuvant chemotherapy in various intrinsic breast cancer subtypes. J Clin Oncol 30(15):1796-1804. doi: 10.1200/JCO.2011.38.8595
37. Watson C, Long JS, Orange C, Tannahill CL, Mallon E, McGlynn LM, Pyne S, Pyne NJ, Edwards J (2010) High expression of sphingosine 1-phosphate receptors, S1P1 and S1P3, sphingosine kinase 1, and extracellular signal-regulated kinase-1/2 is associated with development of tamoxifen resistance in estrogen receptor-positive breast cancer patients. Am J Pathol 177(5):2205-2215. doi: 10.2353/ajpath.2010.100220