KRT19 directly interacts with β-catenin/RAC1 complex to regulate NUMB-dependent NOTCH signaling pathway and breast cancer properties

Oncogene

Volumn 36, Issue 3, 2017, Pages 332-349

  Saha, S K ^a   Choi, H Y ^a   Kim, B W ^a   Dayem, A A ^a   Yang, G M ^a   Kim, K S ^a   Yin, Y F ^a   Cho, S G ^a  

^a Konkuk University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; CD133 ANTIGEN; CHEMOKINE RECEPTOR CXCR4; CYTOKERATIN 19; NERVE CELL ADHESION MOLECULE; NOTCH RECEPTOR; NUMB PROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; PROTEIN; PROTEIN P53; RAC1 PROTEIN; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG; UVOMORULIN; CTNNB1 PROTEIN, HUMAN; MEMBRANE PROTEIN; NERVE PROTEIN; NUMB PROTEIN, HUMAN; RAC1 PROTEIN, HUMAN;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; CANCER RESISTANCE; CANCER STEM CELL; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TUMOR INVASION; UBIQUITINATION; UPREGULATION; ANIMAL; BREAST TUMOR; CANCER TRANSPLANTATION; CELL MOTION; CELL NUCLEUS; FEMALE; GENE EXPRESSION REGULATION; GENE KNOCKDOWN; GENETICS; HEP-G2 CELL LINE; MCF-7 CELL LINE; METABOLISM; PATHOLOGY; TUMOR CELL LINE;

ANIMALS; BETA CATENIN; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; CELL NUCLEUS; CELL PROLIFERATION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; HEP G2 CELLS; HUMANS; KERATIN-19; MCF-7 CELLS; MEMBRANE PROTEINS; MICE; NEOPLASM INVASIVENESS; NEOPLASM TRANSPLANTATION; NERVE TISSUE PROTEINS; RAC1 GTP-BINDING PROTEIN; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 84976315191     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2016.221     Document Type: Article

References (95)

1. Lopez de Silanes I, Quesada MP, Esteller M. Aberrant regulation of messenger RNA 3'-untranslated region in human cancer. Cell Oncol 2007; 29: 1-17.
2. Ignatiadis M, Xenidis N, Perraki M, Apostolaki S, Politaki E, Kafousi M et al. Different prognostic value of cytokeratin-19 mrna-positive circulating tumor cells according to estrogen receptor and HER2 status in early-stage breast cancer. J Clin Oncol 2007; 25: 5194-5202.
3. Bozionellou V, Mavroudis D, Perraki M, Papadopoulos S, Apostolaki S, Stathopoulos E et al. Trastuzumab administration can effectively target chemotherapy-resistant cytokeratin-19 messenger RNA-positive tumor cells in the peripheral blood and bone marrow of patients with breast cancer. Clin Cancer Res 2004; 10: 8185-8194.
4. Coulombe PA, Wong P. Cytoplasmic intermediate filaments revealed as dynamic and multipurpose scaffolds. Nat Cell Biol 2004; 6: 699-706.
5. Omary MB, Ku N-O, Tao G-Z, Toivola DM, Liao J. 'Heads and tails' of intermediate filament phosphorylation: multiple sites and functional insights. Trends Biochem Sci 2006; 31: 383-394.
6. Hendrix MJ, Seftor EA, Chu Y-W, Trevor KT, Seftor RE. Role of intermediate filaments in migration, invasion and metastasis. Cancer Metastasis Rev 1996; 15: 507-525.
7. Caulin C, Ware CF, Magin TM, Oshima RG. Keratin-dependent, epithelial resistance to tumor necrosis factor-induced apoptosis. J Cell Biol 2000; 149: 17-22.
8. Kim S, Wong P, Coulombe PA. A keratin cytoskeletal protein regulates protein synthesis and epithelial cell growth. Nature 2006; 441: 362-365.
9. Wu Y-J, Rheinwald JG. A new small (40 kd) keratin filament protein made by some cultured human squamous cell carcinomas. Cell 1981; 25: 627-635.
10. Fradette J, Germain L, Seshaiah P, Coulombe PA. The type I keratin possesses distinct and context-dependent assembly properties. J Biol Chem 1998; 273: 35176-35184.
11. Stone MR, O'Neill A, Lovering RM, Strong J, Resneck WG, Reed PW et al. Absence of keratin in mice causes skeletal myopathy with mitochondrial and sarcolemmal reorganization. J Cell Sci 2007; 120: 3999-4008.
12. Ju J-h, Yang W, Lee K-m, Oh S, Nam K, Shim S et al. Regulation of cell proliferation and migration by keratin19-induced nuclear import of early growth response-1 in breast cancer cells. Clin Cancer Res 2013; 19: 4335-4346.
13. Govaere O, Komuta M, Berkers J, Spee B, Janssen C, de Luca F et al. Keratin 19: a key role player in the invasion of human hepatocellular carcinomas. Gut 2014; 63: 674-685.
14. Kawai T, Yasuchika K, Ishii T, Katayama H, Yoshitoshi EY, Ogiso S et al. Keratin 19, a cancer stem cell marker in human hepatocellular crcinoma. Clin Cancer Res 2015; 21: 3081-3091.
15. Ma XJ, Dahiya S, Richardson E, Erlander M, Sgroi DC. Gene expression profiling of the tumor microenvironment during breast cancer progression. Breast Cancer Res 2009; 11: R7.
16. Roessler S, Jia H-L, Budhu A, Forgues M, Ye Q-H, Lee J-S et al. A unique metastasis gene signature enables prediction of tumor relapse in early-stage hepatocellular carcinoma patients. Cancer Res 2010; 70: 10202-10212.
17. Skrzypczak M, Goryca K, Rubel T, Paziewska A, Mikula M, Jarosz D et al. Correction: modeling oncogenic signaling in colon tumors by multidirectional analyses of microarray data directed for maximization of analytical reliability. PloS One 2010; 5: 10.1371/annotation/1378c585739-a585354-585734fc585739-a585737d585730- d585735ae585726fa585706ca.
18. Xiao Y-F, Yong X, Tang B, Qin Y, Zhang J-W, Zhang D et al. Notch and Wnt signaling pathway in cancer: crucial role and potential therapeutic targets (Review). Int J Oncol 2016; 48: 437-449.
19. Bernemann C, Hülsewig C, Ruckert C, Schäfer S, Blümel L, Hempel G et al. Influence of secreted frizzled receptor protein 1 (SFRP1) on neoadjuvant chemotherapy in triple negative breast cancer does not rely on WNT signaling. Mol Cancer 2014; 13: 1.
20. Ayyanan A, Civenni G, Ciarloni L, Morel C, Mueller N, Lefort K et al. Increased Wnt signaling triggers oncogenic conversion of human breast epithelial cells by a Notch-dependent mechanism. Proc Natl Acad Sci USA 2006; 103: 3799-3804.
21. Camps J, Pitt JJ, Emons G, Hummon AB, Case CM, Grade M et al. Genetic amplification of the NOTCH modulator LNX2 upregulates the WNT/β-catenin pathway in colorectal cancer. Cancer Res 2013; 73: 2003-2013.
22. Kim H-A, Koo B-K, Cho J-H, Kim Y-Y, Seong J, Chang HJ et al. Notch1 counteracts WNT/β-catenin signaling through chromatin modification in colorectal cancer. J Clin Invest 2012; 122: 3248-3259.
23. Kwon C, Cheng P, King IN, Andersen P, Shenje L, Nigam V et al. Notch posttranslationally regulates β-catenin protein in stem and progenitor cells. Nat Cell Biol 2011; 13: 1244-1251.
24. Peignon G, Durand A, Cacheux W, Ayrault O, Terris B, Laurent-Puig P et al. Complex interplay between β-catenin signalling and Notch effectors in intestinal tumorigenesis. Gut 2011; 60: 166-176.
25. Rodilla V, Villanueva A, Obrador-Hevia A, Robert-Moreno À, Fernández-Majada V, Grilli A et al. Jagged1 is the pathological link between Wnt and Notch pathways in colorectal cancer. Proc Natl Acad Sci USA 2009; 106: 6315-6320.
26. Lamb R, Ablett MP, Spence K, Landberg G, Sims AH, Clarke RB. Wnt pathway activity in breast cancer sub-types and stem-like cells. PloS One 2013; 8: e67811.
27. Valkenburg KC, Graveel CR, Zylstra-Diegel CR, Zhong Z, Williams BO. Wnt/β- catenin signaling in normal and cancer stem cells. Cancers 2011; 3: 2050-2079.
28. Jang G-B, Kim J-Y, Cho S-D, Park K-S, Jung J-Y, Lee H-Y et al. Blockade of Wnt/β- catenin signaling suppresses breast cancer metastasis by inhibiting CSC-like phenotype. Sci Rep 2015; 5: 12465.
29. Borggrefe T, Oswald F. The Notch signaling pathway: transcriptional regulation at Notch target genes. Cell Mol Life Sci 2009; 66: 1631-1646.
30. Oswald F, Täuber B, Dobner T, Bourteele S, Kostezka U, Adler G et al. p300 acts as a transcriptional coactivator for mammalian Notch-1. Mol Cell Biol 2001; 21: 7761-7774.
31. Wallberg AE, Pedersen K, Lendahl U, Roeder RG. p300 and PCAF act cooperatively to mediate transcriptional activation from chromatin templates by notch intracellular domains in vitro. Mol Cell Biol 2002; 22: 7812-7819.
32. Saint Just RM, Hansson M, Wallberg A. A proline repeat domain in the Notch co-activator MAML1 is important for the p300-mediated acetylation of MAML1. Biochem J 2007; 404: 289-298.
33. Gulino A, Di Marcotullio L, Screpanti I. The multiple functions of Numb. Exp Cell Res 2010; 316: 900-906.
34. Boulter L, Govaere O, Bird TG, Radulescu S, Ramachandran P, Pellicoro A et al. Macrophage derived Wnt signalling opposes Notch signalling in a Numb mediated manner to specify HPC fate in chronic liver disease in human and mouse. Nat Med 2012; 18: 572-579.
35. Katoh M, Katoh M. NUMB is a break of WNT-Notch signaling cycle. Int J Mol Med 2006; 18: 517-521.
36. Cheng X, Huber TL, Chen VC, Gadue P, Keller GM. Numb mediates the interaction between Wnt and Notch to modulate primitive erythropoietic specification from the hemangioblast. Development 2008; 135: 3447-3458.
37. Strazzabosco M, Fabris L. The balance between Notch/Wnt signaling regulates progenitor cells' commitment during liver repair: mystery solved? J Hepatol 2013; 58: 181-183.
38. Finak G, Bertos N, Pepin F, Sadekova S, Souleimanova M, Zhao H et al. Stromal gene expression predicts clinical outcome in breast cancer. Nat Med 2008; 14: 518-527.
39. Radvanyi L, Singh-Sandhu D, Gallichan S, Lovitt C, Pedyczak A, Mallo G et al. The gene associated with trichorhinophalangeal syndrome in humans is overexpressed in breast cancer. Proc Natl Acad Sci USA 2005; 102: 11005-11010.
40. Zhao H, Langerød A, Ji Y, Nowels KW, Nesland JM, Tibshirani R et al. Different gene expression patterns in invasive lobular and ductal carcinomas of the breast. Mol Biol Cell 2004; 15: 2523-2536.
41. Liu X-H, Wu Y, Yao S, Levine AC, Kirschenbaum A, Collier L et al. Androgens up-regulate transcription of the notch inhibitor numb in c2c12 myoblasts via wnt/β-catenin signaling to t cell factor elements in the numb promoter. J Biol Chem 2013; 288: 17990-17998.
42. Esufali S, Bapat B. Cross-talk between Rac1 GTPase and dysregulated Wnt signaling pathway leads to cellular redistribution of β-catenin and TCF/LEFmediated transcriptional activation. Oncogene 2004; 23: 8260-8271.
43. Wu X, Tu X, Joeng KS, Hilton MJ, Williams DA, Long F. Rac1 Activation Controls Nuclear Localization of β-catenin during Canonical Wnt Signaling. Cell 2008; 133: 340-353.
44. Phelps RA, Chidester S, Dehghanizadeh S, Phelps J, Sandoval IT, Rai K et al. A two-step model for colon adenoma initiation and progression caused by APC loss. Cell 2009; 137: 623-634.
45. Myant KB, Cammareri P, McGhee EJ, Ridgway RA, Huels DJ, Cordero JB et al. ROS production and NF-κB activation triggered by RAC1 facilitate WNT-driven intestinal stem cell proliferation and colorectal cancer initiation. Cell stem cell 2013; 12: 761-773.
46. Pethe VV, Charames GS, Bapat B. Rac1b recruits Dishevelled and β-catenin to Wnt target gene promoters independent of Wnt3A stimulation. Int J Oncol 2011; 39: 805-810.
47. Stathopoulos E, Sanidas E, Kafousi M, Mavroudis D, Askoxylakis J, Bozionelou V et al. Detection of CK-19 mRNA-positive cells in the peripheral blood of breast cancer patients with histologically and immunohistochemically negative axillary lymph nodes. Ann Oncol 2005; 16: 240-246.
48. Yang X-R, Xu Y, Shi G-M, Fan J, Zhou J, Ji Y et al. Cytokeratin 10 and cytokeratin 19: predictive markers for poor prognosis in hepatocellular carcinoma patients after curative resection. Clin Cancer Res 2008; 14: 3850-3859.
49. Chen T-F, Jiang G-L, Fu X-L, Wang L-J, Qian H, Wu K-L et al. CK19 mRNA expression measured by reverse-transcription polymerase chain reaction (RT-PCR) in the peripheral blood of patients with non-small cell lung cancer treated by chemo-radiation: an independent prognostic factor. Lung Cancer 2007; 56: 105-114.
50. Charafe-Jauffret E, Ginestier C, Monville F, Finetti P, Adelaide J, Cervera N et al. Gene expression profiling of breast cell lines identifies potential new basal markers. Oncogene 2006; 25: 2273-2284.
51. Ju J, Oh S, Lee K, Yang W, Nam K, Moon H et al. Cytokeratin19 induced by HER2/ERK binds and stabilizes HER2 on cell membranes. Cell Death Differ 2014; 22: 665-676.
52. Bambang IF, Lu D, Li H, Chiu L-L, Lau QC, Koay E et al. Cytokeratin 19 regulates endoplasmic reticulum stress and inhibits ERp29 expression via p38 MAPK/XBP-1 signaling in breast cancer cells. Exp Cell Res 2009; 315: 1964-1974.
53. Kim H, Choi GH, Na DC, Ahn EY, Kim GI, Lee JE et al. Human hepatocellular carcinomas with 'Stemness'-related marker expression: keratin 19 expression and a poor prognosis. Hepatology 2011; 54: 1707-1717.
54. Pui C-H. T cell acute lymphoblastic leukemia: NOTCHing the way toward a better treatment outcome. Cancer Cell 2009; 15: 85-87.
55. Zardawi SJ, Zardawi I, McNeil CM, Millar EK, McLeod D, Morey AL et al. High Notch1 protein expression is an early event in breast cancer development and is associated with the HER-2 molecular subtype. Histopathology 2010; 56: 286-296.
56. Artavanis-Tsakonas S, Rand MD, Lake RJ. Notch signaling: cell fate control and signal integration in development. Science 1999; 284: 770-776.
57. Bolos V, Grego-Bessa J, de la Pompa JL. Notch signaling in development and cancer. Endocr Rev 2007; 28: 339-363.
58. Wang Z, Banerjee S, Li Y, Rahman KW, Zhang Y, Sarkar FH. Down-regulation of Notch-1 inhibits invasion by inactivation of nuclear factor-κB, vascular endothelial growth factor, and matrix metalloproteinase-9 in pancreatic cancer cells. Cancer Res 2006; 66: 2778-2784.
59. Sahlgren C, Gustafsson MV, Jin S, Poellinger L, Lendahl U. Notch signaling mediates hypoxia-induced tumor cell migration and invasion. Proc Natl Acad Sci USA 2008; 105: 6392-6397.
60. Wang Z, Li Y, Banerjee S, Kong D, Ahmad A, Nogueira V et al. Down-regulation of Notch-1 and Jagged-1 inhibits prostate cancer cell growth, migration and invasion, and induces apoptosis via inactivation of Akt, mTOR, and NF-kappaB signaling pathways. J Cell Biochem 2010; 109: 726-736.
61. Carter S, Vousden KH. A role for Numb in p53 stabilization. Genome Biol 2008; 9: 221.
62. Nishimura T, Kaibuchi K. Numb controls integrin endocytosis for directional cell migration with aPKC and PAR-3. Dev Cell 2007; 13: 15-28.
63. Westhoff B, Colaluca IN, D'Ario G, Donzelli M, Tosoni D, Volorio S et al. Alterations of the Notch pathway in lung cancer. Proc Natl Acad Sci USA 2009; 106: 22293-22298.
64. Karaczyn A, Bani-Yaghoub M, Tremblay R, Kubu C, Cowling R, Adams TL et al. Two novel human NUMB isoforms provide a potential link between development and cancer. Neural Dev 2010; 5: 31.
65. McGill MA, McGlade CJ. Mammalian numb proteins promote Notch1 receptor ubiquitination and degradation of the Notch1 intracellular domain. J Biol Chem 2003; 278: 23196-23203.
66. Frise E, Knoblich JA, Younger-Shepherd S, Jan LY, Jan YN. The Drosophila Numb protein inhibits signaling of the Notch receptor during cell-cell interaction in sensory organ lineage. Proc Natl Acad Sci USA 1996; 93: 11925-11932.
67. Esufali S, Charames GS, Bapat B. Suppression of nuclear Wnt signaling leads to stabilization of Rac1 isoforms. FEBS Lett 2007; 581: 4850-4856.
68. Buongiorno P, Pethe VV, Charames GS, Esufali S, Bapat B. Rac1 GTPase and the Rac1 exchange factor Tiam1 associate with Wnt-responsive promoters to enhance beta-catenin/TCF-dependent transcription in colorectal cancer cells. Mol Cancer 2008; 7: 73.
69. Jamieson C, Lui C, Brocardo MG, Martino-Echarri E, Henderson BR. Rac1 augments Wnt signaling by stimulating β-catenin-lymphoid enhancer factor-1 complex assembly independent of β-catenin nuclear import. J Cell Sci 2015; 128: 3933-3946.
70. Holliday DL, Speirs V. Choosing the right cell line for breast cancer research. Breast Cancer Res 2011; 13: 215.
71. Lien H, Hsiao Y, Lin Y, Yao Y, Juan H, Kuo W et al. Molecular signatures of metaplastic carcinoma of the breast by large-scale transcriptional profiling: identification of genes potentially related to epithelial-mesenchymal transition. Oncogene 2007; 26: 7859-7871.
72. Wang Y, Klijn JG, Zhang Y, Sieuwerts AM, Look MP, Yang F et al. Gene-expression profiles to predict distant metastasis of lymph-node-negative primary breast cancer. Lancet 2005; 365: 671-679.
73. Sotiriou C, Wirapati P, Loi S, Harris A, Fox S, Smeds J et al. Gene expression profiling in breast cancer: understanding the molecular basis of histologic grade to improve prognosis. J Natl Cancer Inst 2006; 98: 262-272.
74. Liu R, Wang X, Chen GY, Dalerba P, Gurney A, Hoey T et al. The prognostic role of a gene signature from tumorigenic breast-cancer cells. N Engl J Med 2007; 356: 217-226.
75. Buyse M, Loi S, Van't Veer L, Viale G, Delorenzi M, Glas AM et al. Validation and clinical utility of a 70-gene prognostic signature for women with node-negative breast cancer. J Natl Cancer Inst 2006; 98: 1183-1192.
76. Patsialou A, Wang Y, Pignatelli J, Chen X, Entenberg D, Oktay M et al. Autocrine CSF1R signaling mediates switching between invasion and proliferation downstream of TGFβ in claudin-low breast tumor cells. Oncogene 2015; 34: 2721-2731.
77. Kabir NN, Rönnstrand L, Kazi JU. Keratin 19 expression correlates with poor prognosis in breast cancer. Mol Biol Rep 2014; 41: 7729-7735.
78. Tee MK, Rogatsky I, Tzagarakis-Foster C, Cvoro A, An J, Christy RJ et al. Estradiol and selective estrogen receptor modulators differentially regulate target genes with estrogen receptors α and β. Mol Biol Cell 2004; 15: 1262-1272.
79. Moggs JG, Tinwell H, Spurway T, Chang H-S, Pate I, Lim FL et al. Phenotypic anchoring of gene expression changes during estrogen-induced uterine growth. Environ Health Perspect 2004; 112: 1589-1606.
80. Moggs JG, Ashby J, Tinwell H, Lim FL, Moore DJ, Kimber I et al. The need to decide if all estrogens are intrinsically similar. Environ Health Perspect 2004; 112: 1137-1142.
81. Rizzo P, Miao H, D'Souza G, Osipo C, Yun J, Zhao H et al. Cross-talk between notch and the estrogen receptor in breast cancer suggests novel therapeutic approaches. Cancer Res 2008; 68: 5226-5235.
82. Lee CW, Simin K, Liu Q, Plescia J, Guha M, Khan A et al. A functional Notch-survivin gene signature in basal breast cancer. Breast Cancer Res 2008; 10: R97.
83. Chen J-Q, Russo J. ERα-negative and triple negative breast cancer: molecular features and potential therapeutic approaches. Biochim Biophys Acta Rev Cancer 2009; 1796: 162-175.
84. Shao S, Zhao X, Zhang X, Luo M, Zuo X, Huang S et al. Notch1 signaling regulates the epithelial-mesenchymal transition and invasion of breast cancer in a Slugdependent manner. Mol Cancer 2015; 14: 1-17.
85. Salmon P, Trono D. Production and titration of lentiviral vectors. Curr Protoc Hum Genet 2007; 12.10: 1-24.
86. Dayem AA, Kim B, Gurunathan S, Choi HY, Yang G, Saha SK et al. Biologically synthesized silver nanoparticles induce neuronal differentiation of SH-SY5Y cells via modulation of reactive oxygen species, phosphatases, and kinase signaling pathways. Biotechnol J 2014; 9: 934-943.
87. Moon S-H, Kim D-K, Cha Y, Jeon I, Song J, Park K-S. PI3K/Akt and Stat3 signaling regulated by PTEN control of the cancer stem cell population, proliferation and senescence in a glioblastoma cell line. Int J Oncol 2013; 42: 921-928.
88. Leung W-H, Vong QP, Lin W, Janke L, Chen T, Leung W. Modulation of NKG2D ligand expression and metastasis in tumors by spironolactone via RXRγ activation. J Exp Med 2013; 210: 2675-2692.
89. Kujawski M, Kortylewski M, Lee H, Herrmann A, Kay H, Yu H. Stat3 mediates myeloid cell-dependent tumor angiogenesis in mice. J Clin Invest 2008; 118: 3367-3377.
90. Hua G, Liu Y, Li X, Xu P, Luo Y. Targeting glucose metabolism in chondrosarcoma cells enhances the sensitivity to doxorubicin through the inhibition of lactate dehydrogenase-A. Oncol Rep 2014; 31: 2727-2734.
91. Shaw FL, Harrison H, Spence K, Ablett MP, Simões BM, Farnie G et al. A detailed mammosphere assay protocol for the quantification of breast stem cell activity. J Mammary Gland Biol Neoplasia 2012; 17: 111-117.
92. Yu F, Yao H, Zhu P, Zhang X, Pan Q, Gong C et al. let-7 regulates self renewal and tumorigenicity of breast cancer cells. Cell 2007; 131: 1109-1123.
93. Lee JM, Kim IS, Kim H, Lee JS, Kim K, Yim HY et al. RORα attenuates Wnt/β-catenin signaling by PKCα-dependent phosphorylation in colon cancer. Mol Cell 2010; 37: 183-195.
94. Nishikawa S, Konno M, Hamabe A, Hasegawa S, Kano Y, Fukusumi T et al. Surgically resected human tumors reveal the biological significance of the gastric cancer stem cell markers CD44 and CD26. Oncol Lett 2015; 9: 2361-2367.
95. Feldman JP, Goldwasser R, Mark S, Schwartz J, Orion I. A mathematical model for tumor volume evaluation using two-dimensions. J Appl Quant Methods 2009; 4: 455-462.