Ovarian cancer spheroid cells with stem cell-like properties contribute to tumor generation, metastasis and chemotherapy resistance through hypoxia-resistant metabolism

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Liao, Jianqun ^a   Qian, Feng ^a   Tchabo, Nana ^c   Mhawech Fauceglia, Paulette ^a   Beck, Amy ^a   Qian, Zikun ^a   Wang, Xinhui ^b   Huss, Wendy J ^a   Lele, Shashikant B ^a   Morrison, Carl D ^a   Odunsi, Kunle ^a  

^a ROSWELL PARK CANCER INSTITUTE   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c Atlantic Health   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE DEHYDROGENASE; ANTINEOPLASTIC AGENT;

ANAEROBIC GLYCOLYSIS; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER CHEMOTHERAPY; CANCER STEM CELL; CANCER THERAPY; CELL AGGREGATION; CELL INVASION; CELL MIGRATION; CELL SURVIVAL; CLONOGENESIS; ENZYME ACTIVITY; GENE EXPRESSION PROFILING; GLUCOSE METABOLISM; HUMAN; HUMAN CELL; HYPOXIA; IN VITRO STUDY; METASTASIS; NUCLEOTIDE SEQUENCE; OVARY CANCER; OVARY CARCINOMA; PENTOSE PHOSPHATE CYCLE; SPHEROID CELL; STEM CELL; TUMOR GROWTH; XENOGRAFT;

ALDEHYDE DEHYDROGENASE; ANIMALS; ANOXIA; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; DISEASE MODELS, ANIMAL; DRUG RESISTANCE, NEOPLASM; FEMALE; HUMANS; IMMUNOCOMPROMISED HOST; NEOPLASM METASTASIS; NEOPLASTIC STEM CELLS; OVARIAN NEOPLASMS; SPHEROIDS, CELLULAR; TUMOR BURDEN; TUMOR CELLS, CULTURED; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84896965787     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0084941     Document Type: Article

References (59)

1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, et al. (2009) Cancer statistics, 2009. CA Cancer J Clin 59: 225-249.
2. Armstrong D (2010) Update on treatment options for newly diagnosed ovarian cancer. Clin Adv Hematol Oncol 8: 675-678.
3. Colombo N, Van Gorp T, Parma G, Amant F, Gatta G, et al. (2006) Ovarian cancer. Crit Rev Oncol Hematol 60: 159-179. (Pubitemid 44636248)
4. Cannistra SA (2004) Cancer of the ovary. N Engl J Med 351: 2519-2529.
5. Burleson KM, Boente MP, Pambuccian SE, Skubitz AP (2006) Disaggregation and invasion of ovarian carcinoma ascites spheroids. J Transl Med 4: 6.
6. L'Esperance S, Bachvarova M, Tetu B, Mes-Masson AM, Bachvarov D (2008) Global gene expression analysis of early response to chemotherapy treatment in ovarian cancer spheroids. BMC Genomics 9: 99.
7. Shield K, Riley C, Quinn MA, Rice GE, Ackland ML, et al. (2007) Alpha2beta1 integrin affects metastatic potential of ovarian carcinoma spheroids by supporting disaggregation and proteolysis. J Carcinog 6: 11.
8. Zietarska M, Maugard CM, Filali-Mouhim A, Alam-Fahmy M, Tonin PN, et al. (2007) Molecular description of a 3D in vitro model for the study of epithelial ovarian cancer (EOC). Mol Carcinog 46: 872-885. (Pubitemid 47549773)
9. Shield K, Ackland ML, Ahmed N, Rice GE (2009) Multicellular spheroids in ovarian cancer metastases: Biology and pathology. Gynecol Oncol 113: 143-148.
10. Boros LG, Lapis K, Szende B, Tomoskozi-Farkas R, Balogh A, et al. (2001) Wheat germ extract decreases glucose uptake and RNA ribose formation but increases fatty acid synthesis in MIA pancreatic adenocarcinoma cells. Pancreas 23: 141-147. (Pubitemid 32692123)
11. Boros LG, Lee PW, Brandes JL, Cascante M, Muscarella P, et al. (1998) Nonoxidative pentose phosphate pathways and their direct role in ribose synthesis in tumors: Is cancer a disease of cellular glucose metabolism? Med Hypotheses 50: 55-59. (Pubitemid 28046401)
12. Dang CV, Semenza GL (1999) Oncogenic alterations of metabolism. Trends Biochem Sci 24: 68-72. (Pubitemid 29346576)
13. Boros LG, Cascante M, Lee WN (2002) Metabolic profiling of cell growth and death in cancer: Applications in drug discovery. Drug Discov Today 7: 364-372. (Pubitemid 34226656)
14. Raamsdonk LM, Teusink B, Broadhurst D, Zhang N, Hayes A, et al. (2001) A functional genomics strategy that uses metabolome data to reveal the phenotype of silent mutations. Nat Biotechnol 19: 45-50. (Pubitemid 32051955)
15. Bertozzi CC, Chang CY, Jairaj S, Shan X, Huang J, et al. (2006) Multiple initial culture conditions enhance the establishment of cell lines from primary ovarian cancer specimens. In Vitro Cell Dev Biol Anim 42: 58-62. (Pubitemid 44264507)
16. Shepherd TG, Theriault BL, Campbell EJ, Nachtigal MW (2006) Primary culture of ovarian surface epithelial cells and ascites-derived ovarian cancer cells from patients. Nat Protoc 1: 2643-2649.
17. Zhang S, Balch C, Chan MW, Lai HC, Matei D, et al. (2008) Identification and characterization of ovarian cancer-initiating cells from primary human tumors. Cancer Res 68: 4311-4320.
18. Crouch SP, Kozlowski R, Slater KJ, Fletcher J (1993) The use of ATP bioluminescence as a measure of cell proliferation and cytotoxicity. J Immunol Methods 160: 81-88.
19. Pejovic T, Pande NT, Mori M, Mhawech-Fauceglia P, Harrington C, et al. (2009) Expression profiling of the ovarian surface kinome reveals candidate genes for early neoplastic changes. Transl Oncol 2: 341-349.
20. Vizan P, Boros LG, Figueras A, Capella G, Mangues R, et al. (2005) K-ras codon-specific mutations produce distinctive metabolic phenotypes in NIH3T3 mice [corrected] fibroblasts. Cancer Res 65: 5512-5515. (Pubitemid 40911149)
21. Lee WN, Boros LG, Puigjaner J, Bassilian S, Lim S, et al. (1998) Mass isotopomer study of the nonoxidative pathways of the pentose cycle with [1,2-13C2]glucose. Am J Physiol 274: E843-851.
22. Katz J, Lee WN, Wals PA, Bergner EA (1989) Studies of glycogen synthesis and the Krebs cycle by mass isotopomer analysis with [U-13C]glucose in rats. J Biol Chem 264: 12994-13004.
23. Kasho VN, Cheng S, Jensen DM, Ajie H, Lee WN, et al. (1996) Feasibility of analysing [13C]urea breath tests for Helicobacter pylori by gas chromatographymass spectrometry in the selected ion monitoring mode. Aliment Pharmacol Ther 10: 985-995. (Pubitemid 26412930)
24. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF (2003) Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A 100: 3983-3988. (Pubitemid 36418143)
25. Collins AT, Berry PA, Hyde C, Stower MJ, Maitland NJ (2005) Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res 65: 10946-10951. (Pubitemid 41713363)
26. Dalerba P, Dylla SJ, Park IK, Liu R, Wang X, et al. (2007) Phenotypic characterization of human colorectal cancer stem cells. Proc Natl Acad Sci U S A 104: 10158-10163. (Pubitemid 47175279)
27. Li C, Heidt DG, Dalerba P, Burant CF, Zhang L, et al. (2007) Identification of pancreatic cancer stem cells. Cancer Res 67: 1030-1037.
28. Patrawala L, Calhoun T, Schneider-Broussard R, Li H, Bhatia B, et al. (2006) Highly purified CD44+ prostate cancer cells from xenograft human tumors are enriched in tumorigenic and metastatic progenitor cells. Oncogene 25: 1696-1708.
29. Hill RP, Perris R (2007) ''Destemming'' cancer stem cells. J Natl Cancer Inst 99: 1435-1440.
30. Kelly PN, Dakic A, Adams JM, Nutt SL, Strasser A (2007) Tumor growth need not be driven by rare cancer stem cells. Science 317: 337. (Pubitemid 47106366)
31. Clarke MF, Dick JE, Dirks PB, Eaves CJ, Jamieson CH, et al. (2006) Cancer stem cells-perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res 66: 9339-9344. (Pubitemid 44623625)
32. Loh YH, Wu Q, Chew JL, Vega VB, Zhang W, et al. (2006) The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat Genet 38: 431-440.
33. Mohle R, Kanz L (2007) Hematopoietic growth factors for hematopoietic stem cell mobilization and expansion. Semin Hematol 44: 193-202. (Pubitemid 47031228)
34. Wiese C, Rolletschek A, Kania G, Blyszczuk P, Tarasov KV, et al. (2004) Nestin expression-a property of multi-lineage progenitor cells? Cell Mol Life Sci 61: 2510-2522. (Pubitemid 39586514)
35. Bapat SA, Mali AM, Koppikar CB, Kurrey NK (2005) Stem and progenitor-like cells contribute to the aggressive behavior of human epithelial ovarian cancer. Cancer Res 65: 3025-3029. (Pubitemid 40524578)
36. Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, et al. (2007) ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 1: 555-567. (Pubitemid 350056407)
37. Carpentino JE, Hynes MJ, Appelman HD, Zheng T, Steindler DA, et al. (2009) Aldehyde dehydrogenase-expressing colon stem cells contribute to tumorigenesis in the transition from colitis to cancer. Cancer Res 69: 8208-8215.
38. van den Hoogen C, van der Horst G, Cheung H, Buijs JT, Lippitt JM, et al. (2010) High aldehyde dehydrogenase activity identifies tumor-initiating and metastasis-initiating cells in human prostate cancer. Cancer Res 70: 5163-5173.
39. Charafe-Jauffret E, Ginestier C, Bertucci F, Cabaud O, Wicinski J, et al. (2013) ALDH1-positive cancer stem cells predict engraftment of primary breast tumors and are governed by a common stem cell program. Cancer Res.
40. Puiffe ML, Le Page C, Filali-Mouhim A, Zietarska M, Ouellet V, et al. (2007) Characterization of ovarian cancer ascites on cell invasion, proliferation, spheroid formation, and gene expression in an in vitro model of epithelial ovarian cancer. Neoplasia 9: 820-829. (Pubitemid 47623422)
41. Warburg O (1956) On the origin of cancer cells. Science 123: 309-314.
42. Lyssiotis CA, Vander-Heiden MG, Munoz-Pinedo C, Emerling BM (2012) Emerging concepts: Linking hypoxic signaling and cancer metabolism. Cell Death Dis 3: E303.
43. Kondoh H (2008) Cellular life span and the Warburg effect. Exp Cell Res 314: 1923-1928.
44. Naora H, Montell DJ (2005) Ovarian cancer metastasis: Integrating insights from disparate model organisms. Nat Rev Cancer 5: 355-366. (Pubitemid 40637827)
45. Allen HJ, Porter C, Gamarra M, Piver MS, Johnson EA (1987) Isolation and morphologic characterization of human ovarian carcinoma cell clusters present in effusions. Exp Cell Biol 55: 194-208. (Pubitemid 18019795)
46. Aaberg-Jessen C, Norregaard A, Christensen K, Pedersen CB, Andersen C, et al. (2013) Invasion of primary glioma-and cell line-derived spheroids implanted into corticostriatal slice cultures. Int J Clin Exp Pathol 6: 546-560.
47. Luca AC, Mersch S, Deenen R, Schmidt S, Messner I, et al. (2013) Impact of the 3D Microenvironment on Phenotype, Gene Expression, and EGFR Inhibition of Colorectal Cancer Cell Lines. PLoS One 8: E59689.
48. Vang S, Wu HT, Fischer A, Miller DH, Maclaughlan S, et al. (2013) Identification of Ovarian Cancer Metastatic miRNAs. PLoS One 8: E58226.
49. Burleson KM, Hansen LK, Skubitz AP (2004) Ovarian carcinoma spheroids disaggregate on type I collagen and invade live human mesothelial cell monolayers. Clin Exp Metastasis 21: 685-697.
50. Burleson KM, Casey RC, Skubitz KM, Pambuccian SE, Oegema TR Jr, et al. (2004) Ovarian carcinoma ascites spheroids adhere to extracellular matrix components and mesothelial cell monolayers. Gynecol Oncol 93: 170-181. (Pubitemid 38429567)
51. Chiaradonna F, Moresco RM, Airoldi C, Gaglio D, Palorini R, et al. (2012) From cancer metabolism to new biomarkers and drug targets. Biotechnol Adv 30: 30-51.
52. Ward PS, Thompson CB (2012) Metabolic reprogramming: A cancer hallmark even warburg did not anticipate. Cancer Cell 21: 297-308.
53. Chen CT, Hsu SH, Wei YH (2010) Upregulation of mitochondrial function and antioxidant defense in the differentiation of stem cells. Biochim Biophys Acta 1800: 257-263.
54. Prigione A, Fauler B, Lurz R, Lehrach H, Adjaye J (2010) The senescencerelated mitochondrial/oxidative stress pathway is repressed in human induced pluripotent stem cells. Stem Cells 28: 721-733.
55. Zhou Y, Zhou Y, Shingu T, Feng L, Chen Z, et al. (2011) Metabolic alterations in highly tumorigenic glioblastoma cells: Preference for hypoxia and high dependency on glycolysis. J Biol Chem 286: 32843-32853.
56. Yuan S, Wang F, Chen G, Zhang H, Feng L, et al. (2013) Effective elimination of cancer stem cells by a novel drug combination strategy. Stem Cells 31: 23-34.
57. Nakano A, Tsuji D, Miki H, Cui Q, El Sayed SM, et al. (2011) Glycolysis inhibition inactivates ABC transporters to restore drug sensitivity in malignant cells. PLoS One 6: E27222.
58. Liu PP, Liao J, Tang ZJ, Wu WJ, Yang J, et al. (2013) Metabolic regulation of cancer cell side population by glucose through activation of the Akt pathway. Cell Death Differ.
59. Keith B, Simon MC (2007) Hypoxia-inducible factors, stem cells, and cancer. Cell 129: 465-472. (Pubitemid 46660978)