The effectiveness of an anti-human IL-6 receptor monoclonal antibody combined with chemotherapy to target colon cancer stem-like cells

International Journal of Oncology

Volumn 46, Issue 4, 2015, Pages 1551-1559

  Ying, Jin ^a   Tsujii, Masahiko ^a   Kondo, Jumpei ^a   Hayashi, Yoshito ^a   Kato, Motohiko ^a   Akasaka, Tomofumi ^a   Inoue, Takuta ^a   Shiraishi, Eri ^a   Inoue, Tahahiro ^a   Hiyama, Satoshi ^a   Tsujii, Yoshiki ^a   Maekawa, Akira ^a   Kawai, Shoichiro ^a   Fujinaga, Tetsuji ^a   Araki, Maekawa ^a   Shinzaki, Shinichiro ^a   Watabe, Kenji ^a   Nishida, Tsutomu ^a   Iijima, Hideki ^a   Takehara, Tetsuo ^a  

^a OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Cancer stem cells; Colon cancer; IL 6; Notch 3; STAT3

Indexed keywords

4 [[(4 METHYLPHENYL)SULFONYLOXY]ACETAMIDO]SALICYLIC ACID; BMI1 PROTEIN; BREAST CANCER RESISTANCE PROTEIN; CELL PROTEIN; FLUOROURACIL; INTERLEUKIN 6; KRUPPEL LIKE FACTOR 4; LGR5 PROTEIN; MESSENGER RNA; NOTCH3 RECEPTOR; OCTAMER TRANSCRIPTION FACTOR 4; SMALL INTERFERING RNA; STAT3 PROTEIN; TOCILIZUMAB; UNCLASSIFIED DRUG; ANTINEOPLASTIC ANTIMETABOLITE; IL6 PROTEIN, HUMAN; INTERLEUKIN 6 RECEPTOR; MONOCLONAL ANTIBODY; NOTCH RECEPTOR; NOTCH3 PROTEIN, HUMAN; STAT3 PROTEIN, HUMAN;

ADHERENT CELL; ARTICLE; CANCER CELL CULTURE; CANCER PROGNOSIS; CANCER RESISTANCE; CANCER STEM CELL; CELL ADHESION; CELL PROLIFERATION; COLON CANCER; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOLOGY; DRUG EFFICACY; DRUG POTENTIATION; DRUG TARGETING; FIBROBLAST; GENE EXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TUMOR SPHEROID; UPREGULATION; XENOTRANSPLANTATION; ANTAGONISTS AND INHIBITORS; COLORECTAL NEOPLASMS; CULTURE TECHNIQUE; DRUG EFFECTS; DRUG RESISTANCE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; TUMOR CELL LINE;

ANTIBODIES, MONOCLONAL, HUMANIZED; ANTIMETABOLITES, ANTINEOPLASTIC; CELL CULTURE TECHNIQUES; CELL LINE, TUMOR; CELL PROLIFERATION; COLORECTAL NEOPLASMS; DRUG RESISTANCE, NEOPLASM; FLUOROURACIL; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INTERLEUKIN-6; NEOPLASTIC STEM CELLS; RECEPTORS, INTERLEUKIN-6; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR;

EID: 84923078160     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.2015.2851     Document Type: Article

References (79)

1. GABRILOVICH D: Mechanisms and functional significance of tumour-induced dendritic-cell defects. Nat Rev Immunol 4: 941-952, 2004.
2. FANG DD, KIM YJ, LEE CN, et al: Expansion of CD133 (+) colon Cancer cultures retaining stem Cell properties to enable Cancer stem Cell target discovery. Br J Cancer 102: 1265-1275, 2010.
3. DICK JE: Stem Cell concepts renew Cancer research. Blood 112: 4793-4807, 2008.
4. SUKACH AN and IVANOV EN: Formation of spherical colonies as a property of stem cells. Tsitologiia 49: 916-922, 2007 (In Russian).
5. SINGH SK, CLARKE ID, TERASAKI M, BONN VE, HAWKINS C, SQUIRE J and DIRKS PB: Identifcation of a Cancer stem Cell in human brain tumors. Cancer Res 63: 5821-5828, 2003.
6. FARNIE G, CLARKE RB, SPENCE K, PINNOCK N, BRENNAN K, ANDERSON NG and BUNDRED NJ: Novel Cell culture technique for primary ductal carcinoma in situ: Role of Notch and epidermal growth factor receptor signaling pathways. J Natl Cancer Inst 99: 616-627, 2007.
7. VERMEULEN L, TODARO M, DE SOUSA MELLO F, SPRICK MR, KEMPER K, PEREZ ALEA M, RICHEL DJ, STASSI G and MEDEMA JP: Single-cell cloning of colon Cancer stem cells reveals a multi-lineage differentiation capacity. Proc Natl Acad Sci USA 105: 13427-13432, 2008.
8. VAN DER FLIER LG, VAN GIJN ME, HATZIS P, et al: Transcription factor achaetescute-like 2 controls intestinal stem Cell fate. Cell 136: 903-912, 2009.
9. BARKER N, VAN ES JH, KUIPERS J, et al: Identifcation of stem cells in small intestine and colon by marker Gene Lgr5. Nature 449: 1003-1007, 2007.
10. LENG Z, TAO K, XIA Q, TAN J, YUE Z, CHEN J, XI H, LI J and ZHENG H: Kruppel-like factor 4 acts as an Oncogene in colon Cancer stem cell-enriched spheroid cells. PLoS One 8: E56082, 2013.
11. SANGIORGI E and CAPECCHI MR: Bmi1 is expressed in vivo in intestinal stem cells. Nat Genet 40: 915-920, 2008.
12. WEN K, FU Z, WU X, FENG J, CHEN W and QIAN J: Oct-4 is required for an antiapoptotic behavior of chemoresistant colorectal Cancer cells enriched for Cancer stem cells: Effects associated with STAT3/Survivin. Cancer Lett 333: 56-65, 2013.
13. TAKAHASHI K, TANABE K, OHNUKI M, NARITA M, ICHISAKA T, TOMODA K and YAMANAKA S: Induction of pluripotent stem cells from adult human fbroblasts by defned factors. Cell 131: 861-872, 2007.
14. ISHIHARA K and HIRANO T: IL-6 in autoimmune disease and chronic infammatory proliferative disease. Cytokine Growth Factor Rev 13: 357-368, 2002.
15. NIAN M, LEE P, KHAPER N and LIU P: Infammatory cytokines and postmyocardial infarction remodeling. Circ Res 94: 1543-1553, 2004.
16. WU CW, WANG SR, CHAO MF, WU TC, LUI WY, P'ENG FK and CHI CW: Serum interleukin-6 levels reflect disease status of gastric cancer. Am J Gastroenterol 91: 1417-1422, 1996.
17. KOONTONGKAEW S, AMORNPHIMOLTHAM P and YAPONG B: Tumor-stroma interactions infuence cytokine expression and matrix metalloproteinase activities in paired primary and metastatic head and neck Cancer cells. Cell Biol Int 33: 165-173, 2009.
18. BURGER RA, GROSEN EA, IOLI GR, et al: Spontaneous release of interleukin-6 by primary cultures of lymphoid and tumor Cell populations purifed from human ovarian carcinoma. J Interferon Cytokine Res 15: 255-260, 1995.
19. KNUPFER H and PREISS R: Serum interleukin-6 levels in colorectal Cancer patients-a summary of published results. Int J Colorectal Dis 25: 135-140, 2010.
20. HSU CP and CHUNG YC: Infuence of interleukin-6 on the inva-siveness of human colorectal carcinoma. Anticancer Res 26: 4607-4614, 2006.
21. CORVINUS FM, ORTH C, MORIGGL R, et al: Persistent STAT3 activation in colon Cancer is associated with enhanced Cell proliferation and tumor growth. Neoplasia 7: 545-555, 2005.
22. LIN L, FUCHS J, LI C, OLSON V, BEKAII-SAAB T and LIN J: STAT3 signaling pathway is necessary for Cell survival and tumor sphere forming capacity in ALDH(+)/CD133(+) stem cell-like human colon Cancer cells. Biochem Biophys Res Commun 416: 246-251, 2011.
23. CHENG X, JIN G, ZHANG X, TIAN M and ZOU L: Stage-dependent STAT3 activation is involved in the differentiation of rat hippocampus neural stem cells. Neurosci Lett 493: 18-23, 2011.
24. LUO Y, MUGHAL MR, OUYANG TG, JIANG H, LUO W, YU QS, GREIG NH and MATTSON MP: Plumbagin promotes the generation of astrocytes from rat spinal cord neural progenitors via activation of the transcription factor Stat3. J Neurochem 115: 1337-1349, 2010.
25. SANSONE P, STORCI G, TAVOLARI S, et al: IL-6 triggers malignant features in mammospheres from human ductal breast carcinoma and normal mammary gland. J Clin Invest 117: 3988-4002, 2007.
26. FAN X, MATSUI W, KHAKI L, STEARN D, CHUN J, LI YM and EBERHART CG: Notch pathway inhibition depletes stem-like cells and blocks engraftment in embryonal brain tumors. Cancer Res 66: 7445-7452, 2006.
27. FAN X, OUYANG N, TENG H and YAO H: Isolation and characterization of spheroid cells from the HT29 colon Cancer Cell line. Int J Colorectal Dis 26: 1279-1285, 2011.
28. FLETCHER JI, HABER M, HENDERSON MJ and NORRIS MD: ABC transporters in cancer: More than just drug effux pumps. Nat Rev Cancer 10: 147-156, 2010.
29. OLSZEWSKI WL, KUBICKA U, TARNOWSKI W, BIELECKI K, ZIOLKOWSKA A and WESOLOWSKA A: Activation of human peritoneal immune cells in early stages of gastric and colon cancer. Surgery 141: 212-221, 2007.
30. LIN L, LIU A, PENG Z, LIN HJ, LI PK, LI PK, LI C and LIN J: STAT3 is necessary for proliferation and survival in colon cancer-initiating cells. Cancer Res 71: 7226-7237, 2011.
31. BRUCE WR and VAN DER GAAG H: A quantitative assay for the number of murine lymphoma cells capable of proliferation in vivo. Nature 199: 79-80, 1963.
32. WILLSON JK, BITTNER GN, OBERLEY TD, MEISNER LF and WEESE JL: Cell culture of human colon adenomas and carcinomas. Cancer Res 47: 2704-2713, 1987.
33. SINGH SK, HAWKINS C, CLARKE ID, SQUIRE JA, BAYANI J, HIDE T, HENKELMAN RM, CUSIMANO MD and DIRKS PB: Identifcation of human brain tumour initiating cells. Nature 432: 396-401, 2004.
34. DEY D, SAXENA M, PARANJAPE AN, KRISHNAN V, GIRADDI R, KUMAR M V, MUKHERJEE G and RANGARAJAN A: Phenotypic and functional characterization of human mammary stem/progenitor cells in long term culture. PLoS One 4: E5329, 2009.
35. TODARO M, ALEA MP, DI STEFANO AB, et al: Colon Cancer stem cells dictate tumor growth and resist Cell death by production of interleukin-4. Cell Stem Cell 1: 389-402, 2007.
36. LOPEZ J, POITEVIN A, MENDOZA-MARTINEZ V, PEREZ-PLASENCIA C and GARCIA-CARRANCA A: Cancer-initiating cells derived from established cervical Cell lines exhibit stem-cell markers and increased radioresistance. BMC Cancer 12: 48, 2012.
37. CHRISTGEN M, BALLMAIER M, BRUCHHARDT H, VON WASIELEWSKI R, KREIPE H and LEHMANN U: Identifcation of a distinct side population of Cancer cells in the Cal-51 human breast carcinoma Cell line. Mol Cell Biochem 306: 201-212, 2007.
38. HAN B and ZHANG JT: Multidrug resistance in Cancer chemotherapy and xenobiotic protection mediated by the half ATP-binding cassette transporter ABCG2. Curr Med Chem Anticancer Agents 4: 31-42, 2004.
39. LICHTENAUER UD, SHAPIRO I, OSSWALD A, MEURER S, KULLE A, REINCKE M, RIEPE F and BEUSCHLEIN F: Characterization of NCI-H295R cells as an in vitro model of hyperaldosteronism. Horm Metab Res 45: 124-129, 2013.
40. GABRIEL E, SCHIEVENBUSCH S, KOLOSSOV E, HENGSTLER JG, ROTSHTEYN T, BOHLEN H, NIERHOFF D, HESCHELER J and DROBINSKAYA L: Differentiation and selection of hepatocyte precursors in suspension spheroid culture of transgenic murine embryonic stem cells. PLoS One 7: E44912, 2012.
41. OHATA H, ISHIGURO T, AIHARA Y, et al: Induction of the stem-like Cell regulator CD44 by Rho kinase inhibition contributes to the maintenance of colon cancer-initiating cells. Cancer Res 72: 5101-5110, 2012.
42. SCHELLER J and ROSE-JOHN S: Interleukin-6 and its receptor: From bench to bedside. Med Microbiol Immunol 195: 173-183, 2006.
43. FISMAN EZ and TENENBAUM A: The ubiquitous interleukin-6: A time for reappraisal. Cardiovasc Diabetol 9: 62, 2010.
44. YI H, CHO HJ, CHO SM, JO K, PARK JA, LEE SH, CHANG BJ, KIM JS and SHIN HC: Effect of 5-FU and MTX on the expression of drug-resistance related Cancer stem Cell markers in nn-small Cell lung Cancer cells. Korean J Physiol Pharmacol 16: 11-16, 2012.
45. CONZE D, WEISS L, REGEN PS, BHUSHAN A, WEAVER D, JOHNSON P and RINCON M: Autocrine production of interleukin 6 causes multidrug resistance in breast Cancer cells. Cancer Res 61: 8851-8858, 2001.
46. KIM SY, KANG JW, SONG X, KIM BK, YOO YD, KWON YT and LEE YJ: Role of the IL-6-JAK1-STAT3-Oct-4 pathway in the conversion of non-stem Cancer cells into Cancer stem-like cells. Cell Signal 25: 961-969, 2013.
47. GARZIA L, ANDOLFO I, CUSANELLI E, et al: MicroRNA-199b-5p impairs Cancer stem cells through negative regulation of HES1 in medulloblastoma. PLoS One 4: E4998, 2009.
48. WANG Z, LI Y, KONG D, et al: Acquisition of epithelial-mesen-chymal transition phenotype of gemcitabine-resistant pancreatic Cancer cells is linked with activation of the notch signaling pathway. Cancer Res 69: 2400-2407, 2009.
49. LEVINA V, MARRANGONI AM, DEMARCO R, GORELIK E and LOKSHIN AE: Drug-selected human lung Cancer stem cells: Cytokine network, tumorigenic and metastatic properties. PLoS One 3: E3077, 2008.
50. BAO B, ALI S, AHMAD A, et al: Hypoxia-induced aggressiveness of pancreatic Cancer cells is due to increased expression of VEGF, IL-6 and miR-21, which can be attenuated by CDF treatment. PLoS One 7: E50165, 2012.
51. GRIVENNIKOV S and KARIN M: Autocrine IL-6 signaling: A key event in tumorigenesis? Cancer Cell 13: 7-9, 2008.
52. RADTKE F and RAJ K: The role of Notch in tumorigenesis: Oncogene or tumour suppressor? Nat Rev Cancer 3: 756-767, 2003.
53. LEONG KG and KARSAN A: Recent insights into the role of Notch signaling in tumorigenesis. Blood 107: 2223-2233, 2006.
54. REEDIJK M, ODORCIC S, ZHANG H, CHETTY R, TENNERT C, DICKSON BC, LOCKWOOD G, GALLINGER S and EGAN SE: Activation of Notch signaling in human colon adenocarcinoma. Int J Oncol 33: 1223-1229, 2008.
55. ZHANG H, LI W, NAN F, REN F, WANG H, XU Y and ZHANG F: MicroRNA expression profle of colon Cancer stem-like cells in HT29 adenocarcinoma Cell line. Biochem and Biophys Res Commun 404: 273-278, 2011.
56. SULLIVAN JP, SPINOLA M, DODGE M, et al: Aldehyde dehydrogenase activity selects for lung adenocarcinoma stem cells dependent on notch signaling. Cancer Res 70: 9937-9948, 2010.
57. MCAULIFFE SM, MORGAN SL, WYANT GA, et al: Targeting Notch, a key pathway for ovarian Cancer stem cells, sensitizes tumors to platinum therapy. Proc Natl Acad Sci USA 109: E2939-E2948, 2012.
58. MA XT, WANG S, YE YJ, DU RY, CUI ZR and SOMSOUK M: Constitutive activation of Stat3 signaling pathway in human colorectal carcinoma. World J Gastroenterol 10: 1569-1573, 2004.
59. ASHIZAWA T, MIYATA H, IIZUKA A, et al: Effect of the STAT3 inhibitor STX-0119 on the proliferation of Cancer stem-like cells derived from recurrent glioblastoma. Int J Oncol 43: 219-227, 2013.
60. SONG X, WANG M, ZHANG L, ZHANG J, WANG X, LUI W, GU X and LV C: Changes in Cell ultrastructure and inhibition of JAK1/STAT3 signaling pathway in CBRH-7919 cells with astaxanthin. Toxicol Mech Methods 22: 679-686, 2012.
61. LIN Q, LAI R, CHIRIEAC LR, et al: Constitutive activation of JAK3/STAT3 in colon carcinoma tumors and Cell lines: Inhibition of JAK3/STAT3 signaling induces apoptosis and Cell cycle arrest of colon carcinoma cells. Am J Pathol 167: 969-980, 2005.
62. DECKER T and KOVARIK P: Serine phosphorylation of STATs. Oncogene 19: 2628-2637, 2000.
63. WEN Z, ZHONG Z and DARNELL JE Jr: Maximal activation of transcription by Stat1 and Stat3 requires both tyrosine and serine phosphorylation. Cell 82: 241-250, 1995.
64. TAKAOKA A, TANAKA N, MITANI Y, et al: Protein tyrosine kinase Pyk2 mediates the Jak-dependent activation of MAPK and Stat1 in IFN-gamma, bu not IFN-alpha, signaling. EMBO J 18: 2480-2488, 1999.
65. COPPO P, DUSANTER-FOURT I, MILLOT G, et al: Constitutive and specifc activation of STAT3 by BCR-ABL in embryonic stem cells. Oncogene 22: 4102-4110, 2003.
66. ZHANG Y, LIU G and DONG Z: MSK1 and JNKs mediate phos-phorylation of STAT3 in UVA-irradiated mouse epidermal JB6 cells. J Biol Chem 276: 42534-42542, 2001.
67. LIM CP and CAO X: Serine phosphorylation and negative regulation of Stat3 by JNK. J Biol Chem 274: 31055-31061, 1999.
68. CERESA BP and PESSIN JE: Insulin stimulates the serine phos-phorylation of the signal transducer and activator of transcription (STAT3) isoform. J Biol Chem 271: 12121-12124, 1996.
69. CERESA BP, HORVATH CM and PESSIN JE: Signal transducer and activator of transcription-3 serine phosphorylation by insulin is mediated by a Ras/Raf/MEK-dependent pathway. Endocrinology 138: 4131-4137, 1997.
70. ANDROUTSELLIS-THEOTOKIS A, LEKER RR, SOLDNER F, et al: Notch signaling regulates stem Cell numbers in vitro and in vivo. Nature 442: 823-826, 2006.
71. NAGAO M, SUGIMORI M and NAKAFUKU M: Cross talk between notch and growth factor/cytokine signaling pathways in neural stem cells. Mol Cell Biol 27: 3982-3994, 2007.
72. RAJAN P and MCKAY RD: Multiple routes to astrocytic differentiation in the CNS. J. Neurosci 18: 3620-3629, 1998.
73. KWAK YD, DANTUMA E, MERCHANT S, BUSHNEV S and SUGAYA K: Amyloid-beta precursor protein induces glial differentiation of neural progenitor cells by activation of the IL-6/gp130 signaling pathway. Neurotox Res 18: 328-338, 2010.
74. PENG H, SUN L, JIA B, LAN X, ZHU B, WU Y and ZHENG J: HIV-1-infected and immune-activated macrophages induce astrocytic differentiation of human cortical neural progenitor cells via the STAT3 pathway. PLoS One 6: E19439, 2011.
75. LUO M, LIU Z, CHEN G, HAO H, LU T, CUI Y, LEI M, VERFAILLIE CM and LIU Z: High glucose enhances TGF-beta1 expression in rat bone marrow stem cells via ERK1/2-mediated inhibition of STAT3 signaling. Life Sci 90: 509-518, 2012.
76. YOSHIMATSU T, KAWAGUCHI D, OISHI K, TAKEDA K, AKIRA S, MASUYAMA N and GOTOH Y: Non-cell-autonomous action of STAT3 in maintenance of neural precursor cells in the mouse neocortex. Development 133: 2553-2563, 2006.
77. + cord blood cells through the activation of Jak-PI3K-STAT3 pathway. Am J Pathol 180: 351-364, 2012.
78. DE LA IGLESIA N, PURAM SV and BONNI A: STAT3 regulation of glioblastoma pathogenesis. Curr Mol Med 9: 580-590, 2009.
79. KONDO J, ENDO H, OKUYAMA H, ISHIKAWA O, LISHI H, TSUJII M, OHUE M and INOUE M: Retaining cell-cell contact enables preparation and culture of spheroids composed of pure primary Cancer cells from colorectal cancer. Proc Natl Acad Sci USA 108: 6235-6240, 2011.