Lipid Desaturation Is a Metabolic Marker and Therapeutic Target of Ovarian Cancer Stem Cells

Cell Stem Cell

Volumn 20, Issue 3, 2017, Pages 303-314.e5

  Li, Junjie ^a   Condello, Salvatore ^b   Thomes Pepin, Jessica ^c   Ma, Xiaoxiao ^d   Xia, Yu ^d   Hurley, Thomas D ^e,f   Matei, Daniela ^b,g   Cheng, Ji Xin ^a,d,h  

^a PURDUE UNIVERSITY   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c INDIANA UNIVERSITY   (United States)

^d PURDUE UNIVERSITY   (United States)

^e INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^g JESSE BROWN VA MEDICAL CENTER   (United States)

^h Purdue University   (United States)

Author keywords

cancer stem cells; lipid desaturation; NF B; ovarian cancer; Raman spectroscopic imaging; SCD1

Indexed keywords

ALDEHYDE DEHYDROGENASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; INTERLEUKIN 8; OCTAMER TRANSCRIPTION FACTOR 4; SATURATED FATTY ACID; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; UNSATURATED FATTY ACID; ACYL COENZYME A DESATURASE; LIPID; TUMOR MARKER;

ARTICLE; CANCER STEM CELL; CARCINOGENESIS; CONTROLLED STUDY; DOWN REGULATION; FATTY ACID DESATURATION; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIPID ANALYSIS; LIPID METABOLISM; OVARIAN CANCER CELL LINE; OVARY CANCER; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RAMAN SPECTROMETRY; SIGNAL TRANSDUCTION; TUMOR SPHEROID; ANIMAL; CELL PROLIFERATION; CELL SEPARATION; CHEMISTRY; FLOW CYTOMETRY; GENETICS; METABOLISM; MOLECULARLY TARGETED THERAPY; MULTICELLULAR SPHEROID; NUDE MOUSE; OVARY TUMOR; PATHOLOGY; TUMOR CELL LINE;

ALDEHYDE DEHYDROGENASE; ANIMALS; BIOMARKERS, TUMOR; CARCINOGENESIS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SEPARATION; DOWN-REGULATION; FATTY ACID DESATURASES; FEMALE; FLOW CYTOMETRY; HUMANS; LIPIDS; MICE, NUDE; MOLECULAR TARGETED THERAPY; NEOPLASTIC STEM CELLS; NF-KAPPA B; OVARIAN NEOPLASMS; SIGNAL TRANSDUCTION; SPHEROIDS, CELLULAR;

EID: 85009354143     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2016.11.004     Document Type: Article

References (53)

1. Bjerkvig, R., Tysnes, B.B., Aboody, K.S., Najbauer, J., Terzis, A.J.A., Opinion: the origin of the cancer stem cell: current controversies and new insights. Nat. Rev. Cancer 5 (2005), 899–904.
2. Camandola, S., Leonarduzzi, G., Musso, T., Varesio, L., Carini, R., Scavazza, A., Chiarpotto, E., Baeuerle, P.A., Poli, G., Nuclear factor kB is activated by arachidonic acid but not by eicosapentaenoic acid. Biochem. Biophys. Res. Commun. 229 (1996), 643–647.
3. Camp, C.H. Jr., Yegnanarayanan, S., Eftekhar, A.A., Sridhar, H., Adibi, A., Multiplex coherent anti-Stokes Raman scattering (MCARS) for chemically sensitive, label-free flow cytometry. Opt. Express 17 (2009), 22879–22889.
4. Camp, C.H. Jr., Yegnanarayanan, S., Eftekhar, A.A., Adibi, A., Label-free flow cytometry using multiplex coherent anti-Stokes Raman scattering (MCARS) for the analysis of biological specimens. Opt. Lett. 36 (2011), 2309–2311.
5. Cheng, J.-X., Xie, X.S., Vibrational spectroscopic imaging of living systems: An emerging platform for biology and medicine. Science, 350, 2015, aaa8870.
6. Chua, H.L., Bhat-Nakshatri, P., Clare, S.E., Morimiya, A., Badve, S., Nakshatri, H., NF-kappaB represses E-cadherin expression and enhances epithelial to mesenchymal transition of mammary epithelial cells: potential involvement of ZEB-1 and ZEB-2. Oncogene 26 (2007), 711–724.
7. Chute, J.P., Muramoto, G.G., Whitesides, J., Colvin, M., Safi, R., Chao, N.J., McDonnell, D.P., Inhibition of aldehyde dehydrogenase and retinoid signaling induces the expansion of human hematopoietic stem cells. Proc. Natl. Acad. Sci. USA 103 (2006), 11707–11712.
8. Clevers, H., The cancer stem cell: premises, promises and challenges. Nat. Med. 17 (2011), 313–319.
9. Condello, S., Morgan, C.A., Nagdas, S., Cao, L., Turek, J., Hurley, T.D., Matei, D., β-Catenin-regulated ALDH1A1 is a target in ovarian cancer spheroids. Oncogene 34 (2015), 2297–2308.
10. Flesken-Nikitin, A., Odai-Afotey, A.A., Nikitin, A.Y., Role of the stem cell niche in the pathogenesis of epithelial ovarian cancers. Mol. Cell. Oncol., 1, 2014, e963435.
11. Foster, R., Buckanovich, R.J., Rueda, B.R., Ovarian cancer stem cells: working towards the root of stemness. Cancer Lett. 338 (2013), 147–157.
12. Fu, D., Holtom, G., Freudiger, C., Zhang, X., Xie, X.S., Hyperspectral imaging with stimulated raman scattering by chirped femtosecond lasers. J. Phys. Chem. B 117 (2013), 4634–4640.
13. Ginestier, C., Wicinski, J., Cervera, N., Monville, F., Finetti, P., Bertucci, F., Wicha, M.S., Birnbaum, D., Charafe-Jauffret, E., Retinoid signaling regulates breast cancer stem cell differentiation. Cell Cycle 8 (2009), 3297–3302.
14. Jia, D., Yang, W., Li, L., Liu, H., Tan, Y., Ooi, S., Chi, L., Filion, L.G., Figeys, D., Wang, L., β-Catenin and NF-κB co-activation triggered by TLR3 stimulation facilitates stem cell-like phenotypes in breast cancer. Cell Death Differ. 22 (2015), 298–310.
15. Jordan, C.T., Guzman, M.L., Noble, M., Cancer stem cells. N. Engl. J. Med. 355 (2006), 1253–1261.
16. Kamphorst, J.J., Cross, J.R., Fan, J., de Stanchina, E., Mathew, R., White, E.P., Thompson, C.B., Rabinowitz, J.D., Hypoxic and Ras-transformed cells support growth by scavenging unsaturated fatty acids from lysophospholipids. Proc. Natl. Acad. Sci. USA 110 (2013), 8882–8887.
17. Karin, M., Cao, Y., Greten, F.R., Li, Z.W., NF-kappaB in cancer: from innocent bystander to major culprit. Nat. Rev. Cancer 2 (2002), 301–310.
18. Lewis, D.A., Travers, J.B., Machado, C., Somani, A.K., Spandau, D.F., Reversing the aging stromal phenotype prevents carcinoma initiation. Aging (Albany, N.Y.) 3 (2011), 407–416.
19. Li, S., Kendall, S.E., Raices, R., Finlay, J., Covarrubias, M., Liu, Z., Lowe, G., Lin, Y.H., Teh, Y.H., Leigh, V., et al. TWIST1 associates with NF-kappaB subunit RELA via carboxyl-terminal WR domain to promote cell autonomous invasion through IL8 production. BMC Biol., 10, 2012, 10.1186/1741-7007-10-73.
20. Liu, G., Lynch, J.K., Freeman, J., Liu, B., Xin, Z., Zhao, H., Serby, M.D., Kym, P.R., Suhar, T.S., Smith, H.T., et al. Discovery of potent, selective, orally bioavailable stearoyl-CoA desaturase 1 inhibitors. J. Med. Chem. 50 (2007), 3086–3100.
21. Liu, P.P., Liao, J., Tang, Z.J., Wu, W.J., Yang, J., Zeng, Z.L., Hu, Y., Wang, P., Ju, H.Q., Xu, R.H., Huang, P., Metabolic regulation of cancer cell side population by glucose through activation of the Akt pathway. Cell Death Differ. 21 (2014), 124–135.
22. Liu, B., Lee, H.J., Zhang, D., Liao, C.-S., Ji, N., Xia, Y., Cheng, J.-X., Label-free spectroscopic detection of membrane potential using stimulated Raman scattering. Appl. Phys. Lett., 106, 2015, 173704.
23. Ma, I., Allan, A.L., The role of human aldehyde dehydrogenase in normal and cancer stem cells. Stem Cell Rev. 7 (2011), 292–306.
24. Ma, X., Xia, Y., Pinpointing double bonds in lipids by Paternò-Büchi reactions and mass spectrometry. Angew. Chem. Int. Ed. Engl. 53 (2014), 2592–2596.
25. Marcato, P., Dean, C.A., Giacomantonio, C.A., Lee, P.W.K., Aldehyde dehydrogenase: its role as a cancer stem cell marker comes down to the specific isoform. Cell Cycle 10 (2011), 1378–1384.
26. Meirelles, K., Benedict, L.A., Dombkowski, D., Pepin, D., Preffer, F.I., Teixeira, J., Tanwar, P.S., Young, R.H., MacLaughlin, D.T., Donahoe, P.K., Wei, X., Human ovarian cancer stem/progenitor cells are stimulated by doxorubicin but inhibited by Mullerian inhibiting substance. Proc. Natl. Acad. Sci. USA 109 (2012), 2358–2363.
27. Miranda-Lorenzo, I., Dorado, J., Lonardo, E., Alcala, S., Serrano, A.G., Clausell-Tormos, J., Cioffi, M., Megias, D., Zagorac, S., Balic, A., et al. Intracellular autofluorescence: a biomarker for epithelial cancer stem cells. Nat. Methods 11 (2014), 1161–1169.
28. Mitra, A.K., Davis, D.A., Tomar, S., Roy, L., Gurler, H., Xie, J., Lantvit, D.D., Cardenas, H., Fang, F., Liu, Y., et al. In vivo tumor growth of high-grade serous ovarian cancer cell lines. Gynecol. Oncol. 138 (2015), 372–377.
29. Movasaghi, Z., Rehman, S., Rehman, I.U., Raman spectroscopy of biological tissues. Appl. Spectrosc. Rev. 42 (2007), 493–541.
30. Nakamura, M.T., Nara, T.Y., Structure, function, and dietary regulation of delta6, delta5, and delta9 desaturases. Annu. Rev. Nutr. 24 (2004), 345–376.
31. Obukowicz, M.G., Welsch, D.J., Salsgiver, W.J., Martin-Berger, C.L., Chinn, K.S., Duffin, K.L., Raz, A., Needleman, P., Novel, selective delta6 or delta5 fatty acid desaturase inhibitors as antiinflammatory agents in mice. J. Pharmacol. Exp. Ther. 287 (1998), 157–166.
32. Pandey, P.R., Okuda, H., Watabe, M., Pai, S.K., Liu, W., Kobayashi, A., Xing, F., Fukuda, K., Hirota, S., Sugai, T., et al. Resveratrol suppresses growth of cancer stem-like cells by inhibiting fatty acid synthase. Breast Cancer Res. Treat. 130 (2011), 387–398.
33. Pattabiraman, D.R., Weinberg, R.A., Tackling the cancer stem cells - what challenges do they pose?. Nat. Rev. Drug Discov. 13 (2014), 497–512.
34. Poletto, A.C., Furuya, D.T., David-Silva, A., Ebersbach-Silva, P., Santos, C.L., Corrêa-Giannella, M.L., Passarelli, M., Machado, U.F., Oleic and linoleic fatty acids downregulate Slc2a4/GLUT4 expression via NFKB and SREBP1 in skeletal muscle cells. Mol. Cell. Endocrinol. 401 (2015), 65–72.
35. Ponti, D., Costa, A., Zaffaroni, N., Pratesi, G., Petrangolini, G., Coradini, D., Pilotti, S., Pierotti, M.A., Daidone, M.G., Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer Res. 65 (2005), 5506–5511.
36. Roongta, U.V., Pabalan, J.G., Wang, X., Ryseck, R.P., Fargnoli, J., Henley, B.J., Yang, W.P., Zhu, J., Madireddi, M.T., Lawrence, R.M., et al. Cancer cell dependence on unsaturated fatty acids implicates stearoyl-CoA desaturase as a target for cancer therapy. Mol. Cancer Res. 9 (2011), 1551–1561.
37. Sansone, P., Ceccarelli, C., Berishaj, M., Chang, Q., Rajasekhar, V.K., Perna, F., Bowman, R.L., Vidone, M., Daly, L., Nnoli, J., et al. Self-renewal of CD133(hi) cells by IL6/Notch3 signalling regulates endocrine resistance in metastatic breast cancer. Nat. Commun., 7, 2016, 10442, 10.1038/ncomms10442.
38. Santos, C.R., Schulze, A., Lipid metabolism in cancer. FEBS J. 279 (2012), 2610–2623.
39. Shanmugam, R., Kusumanchi, P., Appaiah, H., Cheng, L., Crooks, P., Neelakantan, S., Peat, T., Klaunig, J., Matthews, W., Nakshatri, H., Sweeney, C.J., A water soluble parthenolide analog suppresses in vivo tumor growth of two tobacco-associated cancers, lung and bladder cancer, by targeting NF-κB and generating reactive oxygen species. Int. J. Cancer 128 (2011), 2481–2494.
40. Shostak, K., Chariot, A., NF-κB, stem cells and breast cancer: the links get stronger. Breast Cancer Res. 13 (2011), 214–220.
41. Silva, I.A., Bai, S., McLean, K., Yang, K., Griffith, K., Thomas, D., Ginestier, C., Johnston, C., Kueck, A., Reynolds, R.K., et al. Aldehyde dehydrogenase in combination with CD133 defines angiogenic ovarian cancer stem cells that portend poor patient survival. Cancer Res. 71 (2011), 3991–4001.
42. Slipchenko, M.N., Le, T.T., Chen, H.T., Cheng, J.-X., High-speed vibrational imaging and spectral analysis of lipid bodies by compound Raman microscopy. J. Phys. Chem. B 113 (2009), 7681–7686.
43. Szotek, P.P., Pieretti-Vanmarcke, R., Masiakos, P.T., Dinulescu, D.M., Connolly, D., Foster, R., Dombkowski, D., Preffer, F., Maclaughlin, D.T., Donahoe, P.K., Ovarian cancer side population defines cells with stem cell-like characteristics and Mullerian Inhibiting Substance responsiveness. Proc. Natl. Acad. Sci. USA 103 (2006), 11154–11159.
44. Tirinato, L., Liberale, C., Di Franco, S., Candeloro, P., Benfante, A., La Rocca, R., Potze, L., Marotta, R., Ruffilli, R., Rajamanickam, V.P., et al. Lipid droplets: a new player in colorectal cancer stem cells unveiled by spectroscopic imaging. Stem Cells 33 (2015), 35–44.
45. Tumanov, S., Bulusu, V., Kamphorst, J.J., Chapter six - analysis of fatty acid metabolism using stable isotope tracers and mass spectrometry. Christian, M.M., (eds.) Methods Enzymol, 2015, Academic Press, 197–217.
46. van der Zee, M., Sacchetti, A., Cansoy, M., Joosten, R., Teeuwssen, M., Heijmans-Antonissen, C., Ewing-Graham, P.C., Burger, C.W., Blok, L.J., Fodde, R., IL6/JAK1/STAT3 signaling blockade in endometrial cancer affects the ALDHhi/CD126+ stem-like component and reduces tumor burden. Cancer Res. 75 (2015), 3608–3622.
47. Visvader, J.E., Lindeman, G.J., Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat. Rev. Cancer 8 (2008), 755–768.
48. Wang, H.-W., Bao, N., Le, T.L., Lu, C., Cheng, J.-X., Microfluidic CARS cytometry. Opt. Express 16 (2008), 5782–5789.
49. Wang, X., Sun, Y., Wong, J., Conklin, D.S., PPARγ maintains ERBB2-positive breast cancer stem cells. Oncogene 32 (2013), 5512–5521.
50. Yang, W.C., Adamec, J., Regnier, F.E., Enhancement of the LC/MS analysis of fatty acids through derivatization and stable isotope coding. Anal. Chem. 79 (2007), 5150–5157.
51. Zhang, C., Zhang, D., Cheng, J.-X., Coherent Raman scattering microscopy in biology and medicine. Annu. Rev. Biomed. Eng. 17 (2015), 415–445.
52. Zhou, J., Zhang, Y., Cancer stem cells: models, mechanisms and implications for improved treatment. Cell Cycle 7 (2008), 1360–1370.
53. Zhou, B.B., Zhang, H., Damelin, M., Geles, K.G., Grindley, J.C., Dirks, P.B., Tumour-initiating cells: challenges and opportunities for anticancer drug discovery. Nat. Rev. Drug Discov. 8 (2009), 806–823.