Protein markers of cancer-associated fibroblasts and tumor-initiating cells reveal subpopulations in freshly isolated ovarian cancer ascites

BMC Cancer

Volumn 12, Issue , 2012, Pages

  Wintzell, My ^a   Hjerpe, Elisabet ^b   Åvall Lundqvist, Elisabeth ^b   Shoshan, Maria ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

Cancer associated fibroblasts; Dissemination ascites; EMT; Ovarian carcinoma; Tumor initiating cells

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; BETA3 INTEGRIN; EPITHELIAL CELL ADHESION MOLECULE; HERMES ANTIGEN; OCTAMER TRANSCRIPTION FACTOR 4; OCTAMER TRANSCRIPTION FACTOR 4A; TRANSCRIPTION FACTOR NANOG; UNCLASSIFIED DRUG; UVOMORULIN; VIMENTIN;

ARTICLE; ASCITES CELL; CANCER ASSOCIATED FIBROBLAST; CANCER STAGING; CANCER STEM CELL; CLINICAL ARTICLE; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; FIBROBLAST; HUMAN; HUMAN CELL; MALIGNANT ASCITES; OVARY CANCER; PROTEIN EXPRESSION; SUMOYLATION; WESTERN BLOTTING;

ACTINS; ANTIGENS, CD44; ANTIGENS, NEOPLASM; ASCITES; BLOTTING, WESTERN; CADHERINS; CELL ADHESION MOLECULES; CELL LINE, TUMOR; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; FIBROBLASTS; HOMEODOMAIN PROTEINS; HUMANS; MUSCLE, SMOOTH; NEOPLASTIC STEM CELLS; OCTAMER TRANSCRIPTION FACTOR-3; OVARIAN NEOPLASMS; SPHEROIDS, CELLULAR; SUMOYLATION; TUMOR CELLS, CULTURED; TUMOR MARKERS, BIOLOGICAL;

EID: 84865056040     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-12-359     Document Type: Article

References (52)

1. Landen CN, Birrer MJ, Sood AK. Early events in the pathogenesis of epithelial ovarian cancer. J Clin Oncol 2008, 26(6):995-1005. 10.1200/JCO.2006.07.9970, 18195328.
2. Ahmed N, Thompson EW, Quinn MA. Epithelial-mesenchymal interconversions in normal ovarian surface epithelium and ovarian carcinomas: an exception to the norm. J Cell Physiol 2007, 213(3):581-588. 10.1002/jcp.21240, 17708542.
3. Veatch AL, Carson LF, Ramakrishnan S. Differential expression of the cell-cell adhesion molecule E-cadherin in ascites and solid human ovarian tumor cells. Int J Cancer 1994, 58(3):393-399. 10.1002/ijc.2910580315, 7519585.
4. Sodek KL, Ringuette MJ, Brown TJ. Compact spheroid formation by ovarian cancer cells is associated with contractile behavior and an invasive phenotype. Int J Cancer 2009, 124(9):2060-2070. 10.1002/ijc.24188, 19132753.
5. Burleson KM, Hansen LK, Skubitz AP. Ovarian carcinoma spheroids disaggregate on type I collagen and invade live human mesothelial cell monolayers. Clin Exp Metastasis 2004, 21(8):685-697.
6. Shield K, Ackland ML, Ahmed N, Rice GE. Multicellular spheroids in ovarian cancer metastases: biology and pathology. Gynecol Oncol 2009, 113(1):143-148. 10.1016/j.ygyno.2008.11.032, 19135710.
7. Christiansen JJ, Rajasekaran AK. Reassessing epithelial to mesenchymal transition as a prerequisite for carcinoma invasion and metastasis. Cancer Res 2006, 66(17):8319-8326. 10.1158/0008-5472.CAN-06-0410, 16951136.
8. Bapat SA, Mali AM, Koppikar CB, Kurrey NK. Stem and progenitor-like cells contribute to the aggressive behavior of human epithelial ovarian cancer. Cancer Res 2005, 65(8):3025-3029.
9. Berry NB, Bapat SA. Ovarian cancer plasticity and epigenomics in the acquisition of a stem-like phenotype. J Ovarian Res 2008, 1:8. 10.1186/1757-2215-1-8, 2612659, 19025622.
10. Zhang S, Balch C, Chan MW, Lai HC, Matei D, Schilder JM, Yan PS, Huang TH, Nephew KP. Identification and characterization of ovarian cancer-initiating cells from primary human tumors. Cancer Res 2008, 68(11):4311-4320. 10.1158/0008-5472.CAN-08-0364, 2553722, 18519691.
11. Gires O. Lessons from common markers of tumor-initiating cells in solid cancers. Cell Mol Life Sci 2011, 68(24):4009-4022. 10.1007/s00018-011-0772-9, 21786143.
12. Das B, Tsuchida R, Malkin D, Koren G, Baruchel S, Yeger H. Hypoxia enhances tumor stemness by increasing the invasive and tumorigenic side population fraction. Stem Cells 2008, 26(7):1818-1830. 10.1634/stemcells.2007-0724, 18467664.
13. Hill RP, Marie-Egyptienne DT, Hedley DW. Cancer stem cells, hypoxia and metastasis. Semin Radiat Oncol 2009, 19(2):106-111. 10.1016/j.semradonc.2008.12.002, 19249648.
14. Ostman A, Augsten M. Cancer-associated fibroblasts and tumor growth-bystanders turning into key players. Curr Opin Genet Dev 2009, 19(1):67-73. 10.1016/j.gde.2009.01.003, 19211240.
15. Zhang Y, Tang H, Cai J, Zhang T, Guo J, Feng D, Wang Z. Ovarian cancer-associated fibroblasts contribute to epithelial ovarian carcinoma metastasis by promoting angiogenesis, lymphangiogenesis and tumor cell invasion. Cancer Lett 2011, 303(1):47-55. 10.1016/j.canlet.2011.01.011, 21310528.
16. Willers IM, Isidoro A, Ortega AD, Fernandez PL, Cuezva JM. Selective inhibition of beta-F1-ATPase mRNA translation in human tumours. Biochem J 2010, 426(3):319-326. 10.1042/BJ20091570, 20028336.
17. Isidoro A, Casado E, Redondo A, Acebo P, Espinosa E, Alonso AM, Cejas P, Hardisson D, Fresno Vara JA, Belda-Iniesta C, et al. Breast carcinomas fulfill the Warburg hypothesis and provide metabolic markers of cancer prognosis. Carcinogenesis 2005, 26(12):2095-2104. 10.1093/carcin/bgi188, 16033770.
18. Lopez-Rios F, Sanchez-Arago M, Garcia-Garcia E, Ortega AD, Berrendero JR, Pozo-Rodriguez F, Lopez-Encuentra A, Ballestin C, Cuezva JM. Loss of the mitochondrial bioenergetic capacity underlies the glucose avidity of carcinomas. Cancer Res 2007, 67(19):9013-9017. 10.1158/0008-5472.CAN-07-1678, 17909002.
19. Montoya J, Perez-Martos A, Garstka HL, Wiesner RJ. Regulation of mitochondrial transcription by mitochondrial transcription factor A. Mol Cell Biochem 1997, 174(1-2):227-230.
20. Kanki T, Ohgaki K, Gaspari M, Gustafsson CM, Fukuoh A, Sasaki N, Hamasaki N, Kang D. Architectural role of mitochondrial transcription factor A in maintenance of human mitochondrial DNA. Mol Cell Biol 2004, 24(22):9823-9834. 10.1128/MCB.24.22.9823-9834.2004, 525493, 15509786.
21. Alvero AB, Chen R, Fu HH, Montagna M, Schwartz PE, Rutherford T, Silasi DA, Steffensen KD, Waldstrom M, Visintin I, et al. Molecular phenotyping of human ovarian cancer stem cells unravels the mechanisms for repair and chemoresistance. Cell Cycle 2009, 8(1):158-166. 10.4161/cc.8.1.7533, 3041590, 19158483.
22. Bapat SA. Human ovarian cancer stem cells. Reproduction 2010, 140(1):33-41. 10.1530/REP-09-0389, 20368192.
23. Marhaba R, Klingbeil P, Nuebel T, Nazarenko I, Buechler MW, Zoeller M. CD44 and EpCAM: cancer-initiating cell markers. Curr Mol Med 2008, 8(8):784-804. 10.2174/156652408786733667, 19075676.
24. van der Gun BT, Melchers LJ, Ruiters MH, de Leij LF, McLaughlin PM, Rots MG. EpCAM in carcinogenesis: the good, the bad or the ugly. Carcinogenesis 2010, 31(11):1913-1921. 10.1093/carcin/bgq187, 20837599.
25. Pham PV, Phan NL, Nguyen NT, Truong NH, Duong TT, Le DV, Truong KD, Phan NK. Differentiation of breast cancer stem cells by knockdown of CD44: promising differentiation therapy. J Transl Med 2011, 9:209. 10.1186/1479-5876-9-209, 3251542, 22152097.
26. Kryczek I, Liu S, Roh M, Vatan L, Szeliga W, Wei S, Banerjee M, Mao Y, Kotarski J, Wicha MS, et al. Expression of aldehyde dehydrogenase and CD133 defines ovarian cancer stem cells. Int J Cancer 2012, 130(1):29-39. 10.1002/ijc.25967, 21480217.
27. Kusumbe AP, Mali AM, Bapat SA. CD133-expressing stem cells associated with ovarian metastases establish an endothelial hierarchy and contribute to tumor vasculature. Stem Cells 2009, 27(3):498-508. 10.1634/stemcells.2008-0868, 19253934.
28. Hermansen SK, Christensen KG, Jensen SS, Kristensen BW. Inconsistent immunohistochemical expression patterns of four different CD133 antibody clones in glioblastoma. J Histochem Cytochem 2011, 59(4):391-407. 10.1369/0022155411400867, 3201141, 21411810.
29. Bidlingmaier S, Zhu X, Liu B. The utility and limitations of glycosylated human CD133 epitopes in defining cancer stem cells. J Mol Med (Berl) 2008, 86(9):1025-1032.
30. Wu C, Alman BA. Side population cells in human cancers. Cancer Lett 2008, 268(1):1-9. 10.1016/j.canlet.2008.03.048, 18487012.
31. Song J, Chang I, Chen Z, Kang M, Wang CY. Characterization of side populations in HNSCC: highly invasive, chemoresistant and abnormal Wnt signaling. PLoS One 2010, 5(7):e11456. 10.1371/journal.pone.0011456, 2897893, 20625515.
32. Hu L, McArthur C, Jaffe RB. Ovarian cancer stem-like side-population cells are tumourigenic and chemoresistant. Br J Cancer 2010, 102(8):1276-1283. 10.1038/sj.bjc.6605626, 2856005, 20354527.
33. Ishikawa T, Nakagawa H. Human ABC transporter ABCG2 in cancer chemotherapy and pharmacogenomics. J Exp Ther Oncol 2009, 8(1):5-24.
34. Fayad W, Brnjic S, Berglind D, Blixt S, Shoshan MC, Berndtsson M, Olofsson MH, Linder S. Restriction of cisplatin induction of acute apoptosis to a subpopulation of cells in a three-dimensional carcinoma culture model. Int J Cancer 2009, 125(10):2450-2455. 10.1002/ijc.24627, 19670329.
35. Maubant S, Cruet-Hennequart S, Dutoit S, Denoux Y, Crouet H, Henry-Amar M, Gauduchon P. Expression of alpha V-associated integrin beta subunits in epithelial ovarian cancer and its relation to prognosis in patients treated with platinum-based regimens. J Mol Histol 2005, 36(1-2):119-129.
36. Partheen K, Levan K, Osterberg L, Claesson I, Sundfeldt K, Horvath G. External validation suggests Integrin beta 3 as prognostic biomarker in serous ovarian adenocarcinomas. BMC Cancer 2009, 9:336. 10.1186/1471-2407-9-336, 2754489, 19775429.
37. Sales KM, Winslet MC, Seifalian AM. Stem cells and cancer: an overview. Stem Cell Rev 2007, 3:249-255. 10.1007/s12015-007-9002-0, 17955391.
38. Dalerba P, Dylla SJ, Park IK, Liu R, Wang X, Cho RW, Hoey T, Gurney A, Huang EH, Simeone DM, et al. Phenotypic characterization of human colorectal cancer stem cells. Proc Natl Acad Sci U S A 2007, 104(24):10158-10163. 10.1073/pnas.0703478104, 1891215, 17548814.
39. Wang X, Dai J. Concise review: isoforms of OCT4 contribute to the confusing diversity in stem cell biology. Stem Cells 2010, 28(5):885-893. 2962909, 20333750.
40. Wei F, Scholer HR, Atchison ML. Sumoylation of Oct4 enhances its stability, DNA binding, and transactivation. J Biol Chem 2007, 282(29):21551-21560. 10.1074/jbc.M611041200, 17525163.
41. Rios-Doria J, Day KC, Kuefer R, Rashid MG, Chinnaiyan AM, Rubin MA, Day ML. The role of calpain in the proteolytic cleavage of E-cadherin in prostate and mammary epithelial cells. J Biol Chem 2003, 278(2):1372-1379. 10.1074/jbc.M208772200, 12393869.
42. Wend P, Holland JD, Ziebold U, Birchmeier W. Wnt signaling in stem and cancer stem cells. Semin Cell Dev Biol 2010, 21(8):855-863. 10.1016/j.semcdb.2010.09.004, 20837152.
43. Tunggal JK, Cowan DS, Shaikh H, Tannock IF. Penetration of anticancer drugs through solid tissue: a factor that limits the effectiveness of chemotherapy for solid tumors. Clin Cancer Res 1999, 5(6):1583-1586.
44. Chen YC, Hsu HS, Chen YW, Tsai TH, How CK, Wang CY, Hung SC, Chang YL, Tsai ML, Lee YY, et al. Oct-4 expression maintained cancer stem-like properties in lung cancer-derived CD133-positive cells. PLoS One 2008, 3(7):e2637. 10.1371/journal.pone.0002637, 2440807, 18612434.
45. Strauss R, Li ZY, Liu Y, Beyer I, Persson J, Sova P, Moller T, Pesonen S, Hemminki A, Hamerlik P, et al. Analysis of epithelial and mesenchymal markers in ovarian cancer reveals phenotypic heterogeneity and plasticity. PLoS One 2011, 6(1):e16186. 10.1371/journal.pone.0016186, 3021543, 21264259.
46. Cai J, Tang H, Xu L, Wang X, Yang C, Ruan S, Guo J, Hu S, Wang Z. Fibroblasts in omentum activated by tumor cells promote ovarian cancer growth, adhesion and invasiveness. Carcinogenesis 2012, 33(1):20-29. 10.1093/carcin/bgr230, 22021907.
47. Zhang J, Li YL, Zhou CY, Hu YT, Chen HZ. Expression of octamer-4 in serous and mucinous ovarian carcinoma. J Clin Pathol 2010, 63(10):879-883. 10.1136/jcp.2009.073593, 20876318.
48. Zhang Z, Liao B, Xu M, Jin Y. Post-translational modification of POU domain transcription factor Oct-4 by SUMO-1. FASEB J 2007, 21(12):3042-3051. 10.1096/fj.06-6914com, 17496161.
49. Moschos SJ, Mo YY. Role of SUMO/Ubc9 in DNA damage repair and tumorigenesis. J Mol Histol 2006, 37(5-7):309-319.
50. Masterson J, O'Dea S. Posttranslational truncation of E-cadherin and significance for tumour progression. Cells Tissues Organs 2007, 185(1-3):175-179.
51. Burkhalter RJ, Symowicz J, Hudson LG, Gottardi CJ, Stack MS. Integrin regulation of {beta}-catenin signaling in ovarian carcinoma. J Biol Chem 2011, 286(26):23467-23475. 10.1074/jbc.M110.199539, 3123110, 21518759.
52. Pan Y, Jiao J, Zhou C, Cheng Q, Hu Y, Chen H. Nanog is highly expressed in ovarian serous cystadenocarcinoma and correlated with clinical stage and pathological grade. Pathobiology 2010, 77(6):283-288. 10.1159/000320866, 21266826.