Colorectal Cancer Stem Cell Biomarkers: Biological Traits and Prognostic Insights


Cite item

Full Text

Abstract

Due to self-renewal, differentiation, and limitless proliferation properties, Cancer Stem Cells (CSCs) increase the probability of tumor development. These cells are identified by using CSC markers, which are highly expressed proteins on the cell surface of CSCs. Recently, the therapeutic application of CSCs as novel biomarkers improved both the prognosis and diagnosis outcome of colorectal Cancer. In the present review, we focused on a specific panel of colorectal CSC markers, including LGR5, ALDH, CD166, CD133, and CD44, which offers a targeted and comprehensive analysis of their functions. The selection criteria for these markersCancer were based on their established significance in Colorectal Cancer (CRC) pathogenesis and clinical outcomes, providing novel insights into the CSC biology of CRC. Through this approach, we aim to elevate understanding and stimulate further research for developing effective diagnostic and therapeutic strategies in CRC.

About the authors

Atena Soleimani

Department of Biochemistry,, Mashhad University of Medical Sciences

Email: info@benthamscience.net

Nikoo Saeedi

Medical School, Islamic Azad University,

Email: info@benthamscience.net

Abdulridha Al-Asady

Department of Pharmacology, University of Warith Al-Anbiyaa

Email: info@benthamscience.net

Elnaz Nazari

Department of Physiology, Mashhad University of Medical Sciences

Email: info@benthamscience.net

Reyhane Hanaie

Department of Metabolic Syndrome Research Center, Mashhad University of Medical Sciences

Email: info@benthamscience.net

Majid Khazaei

Department of Physiology, Mashhad University of Medical Sciences,

Email: info@benthamscience.net

Elnaz Ghorbani

Department of Microbiology,, Mashhad University of Medical Sciences

Email: info@benthamscience.net

Hamed Akbarzade

Department of Biochemistry,, Mashhad University of Medical Sciences

Email: info@benthamscience.net

Mikhail Ryzhikov

Department of Biochemistry, Saint Louis University

Email: info@benthamscience.net

Amir Avan

Department of Genetics, Mashhad University of Medical Sciences

Email: info@benthamscience.net

Seyed Mehr

Department of Biochemistry, Mashhad University of Medical Sciences

Author for correspondence.
Email: info@benthamscience.net

References

  1. Siegel RL, Wagle NS, Cercek A, Smith RA, Jemal A. Colorectal cancer statistics, 2023. CA Cancer J Clin 2023; 73(3): 233-54. doi: 10.3322/caac.21772 PMID: 36856579
  2. Siegel RL, Miller KD, Fuchs HE, Jemal A. Cancer statistics, 2022. CA Cancer J Clin 2022; 72(1): 7-33. doi: 10.3322/caac.21708 PMID: 35020204
  3. Morgan E, Arnold M, Gini A, et al. Global burden of colorectal cancer in 2020 and 2040: Incidence and mortality estimates from GLOBOCAN. Gut 2023; 72(2): 338-44. doi: 10.1136/gutjnl-2022-327736 PMID: 36604116
  4. Xi Y, Xu P. Global colorectal cancer burden in 2020 and projections to 2040. Transl Oncol 2021; 14(10): 101174. doi: 10.1016/j.tranon.2021.101174 PMID: 34243011
  5. Arnold M, Sierra MS, Laversanne M, Soerjomataram I, Jemal A, Bray F. Global patterns and trends in colorectal cancer incidence and mortality. Gut 2017; 66(4): 683-91. doi: 10.1136/gutjnl-2015-310912 PMID: 26818619
  6. Fearon ER, Vogelstein B. A genetic model for colorectal tumorigenesis. Cell 1990; 61(5): 759-67. doi: 10.1016/0092-8674(90)90186-I PMID: 2188735
  7. Su R, Wu X, Tao L, Wang C. The role of epigenetic modifications in colorectal cancer metastasis. Clin Exp Metastasis 2022; 39(4): 521-39. doi: 10.1007/s10585-022-10163-w PMID: 35429301
  8. Winawer S, Fletcher R, Rex D, et al. Colorectal cancer screening and surveillance: Clinical guidelines and rationale? Update based on new evidence. Gastroenterology 2003; 124(2): 544-60. doi: 10.1053/gast.2003.50044 PMID: 12557158
  9. Winawer SJ, Fletcher RH, Miller L, et al. Colorectal cancer screening: Clinical guidelines and rationale. Gastroenterology 1997; 112(2): 594-642. doi: 10.1053/gast.1997.v112.agast970594 PMID: 9024315
  10. Ho MF, Lai VC, Ng DCK, Ng SSM. Prognosis of patients with unresectable stage IV Colon cancer undergoing primary tumor resection: A multicenter study of minimally symptomatic or asymptomatic primary tumor. Asian J Surg 2023; 46(9): 3710-5. doi: 10.1016/j.asjsur.2022.11.127 PMID: 36522225
  11. Park J, Baik H, Kang SH, et al. Comparison between oxaliplatin therapy and capecitabine monotherapy for high-risk stage II – III elderly patients with colon cancer. Asian J Surg 2022; 45(1): 448-55. doi: 10.1016/j.asjsur.2021.07.067 PMID: 34364765
  12. Ishiyama Y, Tachimori Y, Harada T, et al. Oncologic outcomes after laparoscopic versus open multivisceral resection for local advanced colorectal cancer: A meta-analysis. Asian J Surg 2023; 46(1): 6-12. doi: 10.1016/j.asjsur.2022.02.047 PMID: 35568616
  13. Dai S, Zhao W, Yue L, Qian X. A competing risk for nomogram of the role of metastasectomy in patients with colorectal cancer and liver metastases. Asian J Surg 2023; 46(6): 2468-71. doi: 10.1016/j.asjsur.2022.12.066 PMID: 36567218
  14. Ogunwobi OO, Mahmood F, Akingboye A. Biomarkers in colorectal cancer: Current research and future prospects. Int J Mol Sci 2020; 21(15): 5311. doi: 10.3390/ijms21155311 PMID: 32726923
  15. Chen W, Frankel WL. A practical guide to biomarkers for the evaluation of colorectal cancer. Mod Pathol 2019; 32(1) (Suppl. 1): 1-15. doi: 10.1038/s41379-018-0136-1 PMID: 30600322
  16. Ricci-Vitiani L, Fabrizi E, Palio E, De Maria R. Colon cancer stem cells. J Mol Med 2009; 87(11): 1097-104. doi: 10.1007/s00109-009-0518-4 PMID: 19727638
  17. Miller SJ, Lavker RM, Sun TT. Interpreting epithelial cancer biology in the context of stem cells: Tumor properties and therapeutic implications. Biochim Biophys Acta 2005; 1756(1): 25-52. PMID: 16139432
  18. Alison MR, Islam S, Wright NA. Stem cells in cancer: Instigators and propagators? J Cell Sci 2010; 123(14): 2357-68. doi: 10.1242/jcs.054296 PMID: 20592182
  19. Dean M, Fojo T, Bates S. Tumour stem cells and drug resistance. Nat Rev Cancer 2005; 5(4): 275-84. doi: 10.1038/nrc1590 PMID: 15803154
  20. Ailles LE, Weissman IL. Cancer stem cells in solid tumors. Curr Opin Biotechnol 2007; 18(5): 460-6. doi: 10.1016/j.copbio.2007.10.007 PMID: 18023337
  21. Bao S, Wu Q, McLendon RE, et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006; 444(7120): 756-60. doi: 10.1038/nature05236 PMID: 17051156
  22. Todaro M, Francipane MG, Medema JP, Stassi G. Colon cancer stem cells: Promise of targeted therapy. Gastroenterology 2010; 138(6): 2151-62. doi: 10.1053/j.gastro.2009.12.063 PMID: 20420952
  23. Markowitz SD, Bertagnolli MM. Molecular origins of cancer: Molecular basis of colorectal cancer. N Engl J Med 2009; 361(25): 2449-60. doi: 10.1056/NEJMra0804588 PMID: 20018966
  24. Vries RGJ, Huch M, Clevers H. Stem cells and cancer of the stomach and intestine. Mol Oncol 2010; 4(5): 373-84. doi: 10.1016/j.molonc.2010.05.001 PMID: 20598659
  25. Vaiopoulos AG, Kostakis ID, Koutsilieris M, Papavassiliou AG. Colorectal cancer stem cells. Stem Cells 2012; 30(3): 363-71. doi: 10.1002/stem.1031 PMID: 22232074
  26. Rey I. Cancer stem cells and signaling pathways in colorectal cancer. Indones J Gastroenterol Hepatol Digest Endosc 2018; 19(1): 37-41.
  27. Zhang M, Atkinson RL, Rosen JM. Selective targeting of radiation-resistant tumor-initiating cells. Proc Natl Acad Sci USA 2010; 107(8): 3522-7. doi: 10.1073/pnas.0910179107 PMID: 20133717
  28. Clevers H. The cancer stem cell: Premises, promises and challenges. Nat Med 2011; 17(3): 313-9. doi: 10.1038/nm.2304 PMID: 21386835
  29. Gupta PB, Fillmore CM, Jiang G, et al. Stochastic state transitions give rise to phenotypic equilibrium in populations of cancer cells. Cell 2011; 146(4): 633-44. doi: 10.1016/j.cell.2011.07.026 PMID: 21854987
  30. Taniguchi H, Moriya C, Igarashi H, et al. Cancer stem cells in human gastrointestinal cancer. Cancer Sci 2016; 107(11): 1556-62. doi: 10.1111/cas.13069 PMID: 27575869
  31. Parizadeh SM, Jafarzadeh-Esfehani R, Hassanian SM, et al. Targeting cancer stem cells as therapeutic approach in the treatment of colorectal cancer. Int J Biochem Cell Biol 2019; 110: 75-83. doi: 10.1016/j.biocel.2019.02.010 PMID: 30818083
  32. Dahal Lamichane B, Jung SY, Yun J, et al. AGR2 is a target of canonical Wnt/β-catenin signaling and is important for stemness maintenance in colorectal cancer stem cells. Biochem Biophys Res Commun 2019; 515(4): 600-6. doi: 10.1016/j.bbrc.2019.05.154 PMID: 31178140
  33. Shirmohamadi M, Eghbali E, Najjary S, et al. Regulatory mechanisms of microRNAs in colorectal cancer and colorectal cancer stem cells. J Cell Physiol 2020; 235(2): 776-89. doi: 10.1002/jcp.29042 PMID: 31264216
  34. Das PK, Islam F, Lam AK. The roles of cancer stem cells and therapy resistance in colorectal carcinoma. Cells 2020; 9(6): 1392. doi: 10.3390/cells9061392 PMID: 32503256
  35. Kim H, Yu Y, Choi S, et al. Evodiamine eliminates colon cancer stem cells via suppressing Notch and Wnt signaling. Molecules 2019; 24(24): 4520. doi: 10.3390/molecules24244520 PMID: 31835579
  36. Feng HC, Lin JY, Hsu SH, et al. Low folate metabolic stress reprograms DNA methylation-activated sonic hedgehog signaling to mediate cancer stem cell-like signatures and invasive tumour stage-specific malignancy of human colorectal cancers. Int J Cancer 2017; 141(12): 2537-50. doi: 10.1002/ijc.31008 PMID: 28833104
  37. Chang SC, Ding JL. Ubiquitination and SUMOylation in the chronic inflammatory tumor microenvironment. Biochim Biophys Acta Rev Cancer 2018; 1870(2): 165-75. doi: 10.1016/j.bbcan.2018.08.002 PMID: 30318471
  38. Ylä-Herttuala S. The pharmacology of gene therapy. Mol Ther 2017; 25(8): 1731-2. doi: 10.1016/j.ymthe.2017.07.007 PMID: 28739283
  39. Smith DC, Eisenberg PD, Manikhas G, et al. A phase I dose escalation and expansion study of the anticancer stem cell agent demcizumab (anti-DLL4) in patients with previously treated solid tumors. Clin Cancer Res 2014; 20(24): 6295-303. doi: 10.1158/1078-0432.CCR-14-1373 PMID: 25324140
  40. Wei F, Zhang T, Deng SC, et al. PD-L1 promotes colorectal cancer stem cell expansion by activating HMGA1-dependent signaling pathways. Cancer Lett 2019; 450: 1-13. doi: 10.1016/j.canlet.2019.02.022 PMID: 30776481
  41. Imperial R, Ahmed Z, Toor OM, et al. Comparative proteogenomic analysis of right-sided colon cancer, left-sided colon cancer and rectal cancer reveals distinct mutational profiles. Mol Cancer 2018; 17(1): 177. doi: 10.1186/s12943-018-0923-9 PMID: 30577807
  42. Barker N, van Es JH, Kuipers J, et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 2007; 449(7165): 1003-7. doi: 10.1038/nature06196 PMID: 17934449
  43. Haegebarth A, Clevers H. Wnt signaling, lgr5, and stem cells in the intestine and skin. Am J Pathol 2009; 174(3): 715-21. doi: 10.2353/ajpath.2009.080758 PMID: 19197002
  44. Kozovska Z, Gabrisova V, Kucerova L. Colon cancer: Cancer stem cells markers, drug resistance and treatment. Biomed Pharmacother 2014; 68(8): 911-6. doi: 10.1016/j.biopha.2014.10.019 PMID: 25458789
  45. Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature 2001; 414(6859): 105-11. doi: 10.1038/35102167 PMID: 11689955
  46. Fumagalli A, Oost KC, Kester L, Morgner J, Bornes L, Bruens L. Plasticity of Lgr5-negative cancer cells drives metastasis in colorectal cancer. Cell stem cell 2020; 26(4): 569-78. doi: 10.1016/j.stem.2020.02.008
  47. Jang BG, Kim HS, Chang WY, Bae JM, Kim WH, Kang GH. Expression profile of LGR5 and its prognostic significance in colorectal cancer progression. Am J Pathol 2018; 188(10): 2236-50. doi: 10.1016/j.ajpath.2018.06.012 PMID: 30036518
  48. Liu YS, Hsu HC, Tseng KC, Chen HC, Chen SJ. Lgr5 promotes cancer stemness and confers chemoresistance through ABCB1 in colorectal cancer. Biomed Pharmacother 2013; 67(8): 791-9. doi: 10.1016/j.biopha.2013.08.001 PMID: 24138824
  49. Han Y, Xue X, Jiang M, et al. LGR5, a relevant marker of cancer stem cells, indicates a poor prognosis in colorectal cancer patients: A meta-analysis. Clin Res Hepatol Gastroenterol 2015; 39(2): 267-73. doi: 10.1016/j.clinre.2014.07.008 PMID: 25193236
  50. Wu XS, Xi HQ, Chen L. Lgr5 is a potential marker of colorectal carcinoma stem cells that correlates with patient survival. World J Surg Oncol 2012; 10(1): 244. doi: 10.1186/1477-7819-10-244 PMID: 23153436
  51. Liu Z, Dai W, Jiang L, Cheng Y. Over-expression of LGR5 correlates with poor survival of colon cancer in mice as well as in patients. Neoplasma 2014; 61(2): 177-85. doi: 10.4149/neo_2014_016 PMID: 24063790
  52. Salehizadeh S, Hasanzad M, Kadijani AA, Akbari A. The expression analysis of intestinal cancer stem cell marker lgr5 in colorectal cancer patients and the correlation with histopathological markers. J Gastrointest Cancer 2020; 51(2): 591-9.
  53. Ding H, Wang C. Role of Lgr5-positive cells in colorectal cancer. Tumour Biol 2015; 36(9): 6759-64. doi: 10.1007/s13277-015-3357-7 PMID: 25835970
  54. Jia H, Xiang L, Wang Z, Zhou Q. A study on the mechanism of low-expressed cancer stem cell marker lgr5 in inhibition of the proliferation and invasion of colorectal carcinoma. Cell Biochem Biophys 2015; 73(2): 393-7. doi: 10.1007/s12013-015-0640-6 PMID: 27352328
  55. Nagata H, Ishihara S, Abe H, et al. LGR5 expression predicts peritoneal recurrence after curative resection of primary colon cancer. Br J Cancer 2019; 120(10): 996-1002. doi: 10.1038/s41416-019-0442-5 PMID: 31000786
  56. Armstrong L, Stojkovic M, Dimmick I, et al. Phenotypic characterization of murine primitive hematopoietic progenitor cells isolated on basis of aldehyde dehydrogenase activity. Stem Cells 2004; 22(7): 1142-51. doi: 10.1634/stemcells.2004-0170 PMID: 15579635
  57. Magni M, Shammah S, Schiró R, Mellado W, Dalla-Favera R, Gianni AM. Induction of cyclophosphamide-resistance by aldehyde-dehydrogenase gene transfer. Blood 1996; 87(3): 1097-103. doi: 10.1182/blood.V87.3.1097.bloodjournal8731097 PMID: 8562935
  58. Huang EH, Hynes MJ, Zhang T, et al. Aldehyde dehydrogenase 1 is a marker for normal and malignant human colonic stem cells (SC) and tracks SC overpopulation during colon tumorigenesis. Cancer Res 2009; 69(8): 3382-9. doi: 10.1158/0008-5472.CAN-08-4418 PMID: 19336570
  59. Carpentino JE, Hynes MJ, Appelman HD, et al. Aldehyde dehydrogenase-expressing colon stem cells contribute to tumorigenesis in the transition from colitis to cancer. Cancer Res 2009; 69(20): 8208-15. doi: 10.1158/0008-5472.CAN-09-1132 PMID: 19808966
  60. Zhou F, Mu YD, Liang J, et al. Aldehyde dehydrogenase 1: A specific cancer stem cell marker for human colorectal carcinoma. Mol Med Rep 2015; 11(5): 3894-9. doi: 10.3892/mmr.2015.3195 PMID: 25585687
  61. Chen J, Xia Q, Jiang B, et al. Prognostic value of cancer stem cell marker ALDH1 expression in colorectal cancer: A systematic review and meta-analysis. PLoS One 2015; 10(12): e0145164. doi: 10.1371/journal.pone.0145164 PMID: 26682730
  62. Yang W, Wang Y, Wang W, Chen Z, Bai G. Expression of aldehyde dehydrogenase 1A1 (ALDH1A1) as a prognostic biomarker in colorectal cancer using immunohistochemistry. Med Sci Monit 2018; 24: 2864-72. doi: 10.12659/MSM.910109 PMID: 29748529
  63. Hessman CJ, Bubbers EJ, Billingsley KG, Herzig DO, Wong MH. Loss of expression of the cancer stem cell marker aldehyde dehydrogenase 1 correlates with advanced-stage colorectal cancer. Am J Surg 2012; 203(5): 649-53. doi: 10.1016/j.amjsurg.2012.01.003 PMID: 22405917
  64. Khorrami S, Zavaran Hosseini A, Mowla SJ, Malekzadeh R. Verification of ALDH activity as a biomarker in colon cancer stem cells-derived HT-29 cell line. Iran J Cancer Prev 2015; 8(5): e3446. doi: 10.17795/ijcp-3446 PMID: 26634106
  65. Mohamed SY, Kaf RM, Ahmed MM, Elwan A, Ashour HR, Ibrahim A. The prognostic value of cancer stem cell markers (Notch1, ALDH1, and CD44) in primary colorectal carcinoma. J Gastrointest Cancer 2019; 50(4): 824-37. doi: 10.1007/s12029-018-0156-6 PMID: 30136202
  66. Miraglia S, Godfrey W, Yin AH, et al. A novel five-transmembrane hematopoietic stem cell antigen: Isolation, characterization, and molecular cloning. Blood 1997; 90(12): 5013-21. doi: 10.1182/blood.V90.12.5013 PMID: 9389721
  67. Pilati P, Mocellin S, Bertazza L, et al. Prognostic value of putative circulating cancer stem cells in patients undergoing hepatic resection for colorectal liver metastasis. Ann Surg Oncol 2012; 19(2): 402-8. doi: 10.1245/s10434-011-2132-2 PMID: 22071867
  68. Catalano V, Di Franco S, Iovino F, Dieli F, Stassi G, Todaro M. CD133 as a target for colon cancer. Expert Opin Ther Targets 2012; 16(3): 259-67. doi: 10.1517/14728222.2012.667404 PMID: 22385077
  69. Horst D, Scheel SK, Liebmann S, et al. The cancer stem cell marker CD133 has high prognostic impact but unknown functional relevance for the metastasis of human colon cancer. J Pathol 2009; 219(4): 427-34. doi: 10.1002/path.2597 PMID: 19621338
  70. Pohl A, El-Khoueiry A, Yang D, et al. Pharmacogenetic profiling of CD133 is associated with response rate (RR) and progression-free survival (PFS) in patients with metastatic colorectal cancer (mCRC), treated with bevacizumab-based chemotherapy. Pharmacogenomics J 2013; 13(2): 173-80. doi: 10.1038/tpj.2011.61 PMID: 22231565
  71. Shih T, Lindley C. Bevacizumab: An angiogenesis inhibitor for the treatment of solid malignancies. Clin Ther 2006; 28(11): 1779-802. doi: 10.1016/j.clinthera.2006.11.015 PMID: 17212999
  72. Sanders MA, Majumdar AP. Colon cancer stem cells: Implications in carcinogenesis. Front Biosci 2011; 16(1): 1651-62. doi: 10.2741/3811 PMID: 21196254
  73. Stanisavljević L, Myklebust MP, Leh S, Dahl O. LGR5 and CD133 as prognostic and predictive markers for fluoropyrimidine-based adjuvant chemotherapy in colorectal cancer. Acta Oncol 2016; 55(12): 1425-33. doi: 10.1080/0284186X.2016.1201215 PMID: 27435662
  74. Shikina A, Shinto E, Hashiguchi Y, et al. Differential clinical benefits of 5-fluorouracil-based adjuvant chemotherapy for patients with stage III colorectal cancer according to CD133 expression status. Jpn J Clin Oncol 2014; 44(1): 42-8. doi: 10.1093/jjco/hyt168 PMID: 24244031
  75. Li R, Dong H, Zhu J, Yi H, Liu S. Overexpression of CD133 confers poor prognosis in colorectal cancer: A systematic review and meta-analysis. Int J Clin Exp Med 2019; 12(2): 1492-502.
  76. Wang BB, Li ZJ, Zhang FF, Hou HT, Yu JK, Li F. Clinical significance of stem cell marker CD133 expression in colorectal cancer. Histol Histopathol 2016; 31(3): 299-306. PMID: 26442717
  77. Wang K, Xu J, Zhang J, Huang J. Prognostic role of CD133 expression in colorectal cancer: A meta-analysis. BMC Cancer 2012; 12(1): 573. doi: 10.1186/1471-2407-12-573 PMID: 23216926
  78. Pals ST, Hogervorst F, Keizer GD, Thepen T, Horst E, Figdor CC. Identification of a widely distributed 90-kDa glycoprotein that is homologous to the Hermes-1 human lymphocyte homing receptor. J Immunol 1989; 143(3): 851-7.
  79. Screaton GR, Bell MV, Jackson DG, Cornelis FB, Gerth U, Bell JI. Genomic structure of DNA encoding the lymphocyte homing receptor CD44 reveals at least 12 alternatively spliced exons. Proc Natl Acad Sci USA 1992; 89(24): 12160-4. doi: 10.1073/pnas.89.24.12160 PMID: 1465456
  80. Wielenga VJM, van der Neut R, Offerhaus GJA, Pals ST. CD44 glycoproteins in colorectal cancer: Expression, function, and prognostic value. Adv Cancer Res 1999; 77: 169-87. doi: 10.1016/S0065-230X(08)60787-3 PMID: 10549358
  81. Huh JW, Kim HR, Kim YJ, et al. Expression of standard CD44 in human colorectal carcinoma: Association with prognosis. Pathol Int 2009; 59(4): 241-6. doi: 10.1111/j.1440-1827.2009.02357.x PMID: 19351367
  82. Lee SY, Kim KA, Kim CH, Kim YJ, Lee JH, Kim HR. CD44-shRNA recombinant adenovirus inhibits cell proliferation, invasion, and migration, and promotes apoptosis in HCT116 colon cancer cells. Int J Oncol 2017; 50(1): 329-36. doi: 10.3892/ijo.2016.3801 PMID: 27959393
  83. Wielenga VJ, Heider KH, Offerhaus GJ, et al. Expression of CD44 variant proteins in human colorectal cancer is related to tumor progression. Cancer Res 1993; 53(20): 4754-6. PMID: 7691404
  84. Wielenga VJ, van der Voort R, Mulder JW, et al. CD44 splice variants as prognostic markers in colorectal cancer. Scand J Gastroenterol 1998; 33(1): 82-7. doi: 10.1080/00365529850166257 PMID: 9489913
  85. Katoh S, Goi T, Naruse T, et al. Cancer stem cell marker in circulating tumor cells: Expression of CD44 variant exon 9 is strongly correlated to treatment refractoriness, recurrence and prognosis of human colorectal cancer. Anticancer Res 2015; 35(1): 239-44. PMID: 25550556
  86. Miyoshi S, Tsugawa H, Matsuzaki J, et al. Inhibiting xCT improves 5-fluorouracil resistance of gastric cancer induced by CD44 variant 9 expression. Anticancer Res 2018; 38(11): 6163-70. doi: 10.21873/anticanres.12969 PMID: 30396933
  87. Ozawa M, Ichikawa Y, Zheng Y-W, et al. Prognostic significance of CD44 variant 2 upregulation in colorectal cancer. Br J Cancer 2014; 111(2): 365-74. doi: 10.1038/bjc.2014.253 PMID: 24921913
  88. Nakano M, Taguchi R, Kikushige Y, et al. RHAMM marks proliferative subpopulation of human colorectal cancer stem cells. Cancer Sci 2023; 114(7): 2895-906. doi: 10.1111/cas.15795 PMID: 36945114
  89. Gerger A, Zhang W, Yang D, et al. Common cancer stem cell gene variants predict colon cancer recurrence. Clin Cancer Res 2011; 17(21): 6934-43. doi: 10.1158/1078-0432.CCR-11-1180 PMID: 21918173
  90. Tachezy M, Zander H, Gebauer F, et al. Activated leukocyte cell adhesion molecule (CD166)-Its prognostic power for colorectal cancer patients. J Surg Res 2012; 177(1): e15-20. doi: 10.1016/j.jss.2012.02.013 PMID: 22482754
  91. Weichert W, Knösel T, Bellach J, Dietel M, Kristiansen G. ALCAM/CD166 is overexpressed in colorectal carcinoma and correlates with shortened patient survival. J Clin Pathol 2004; 57(11): 1160-4. doi: 10.1136/jcp.2004.016238 PMID: 15509676
  92. Ribeiro KB, da Silva Zanetti J, Ribeiro-Silva A, et al. KRAS mutation associated with CD44/CD166 immunoexpression as predictors of worse outcome in metastatic colon cancer. Cancer Biomark 2016; 16(4): 513-21. doi: 10.3233/CBM-160592 PMID: 27062566
  93. Shafaei S, Sharbatdaran M, Kamrani G, Khafri S. The association between CD166 detection rate and clinicopathologic parameters of patients with colorectal cancer. Caspian J Intern Med 2013; 4(4): 768-72. PMID: 24294471
  94. Hansen AG, Freeman TJ, Arnold SA, et al. Elevated ALCAM shedding in colorectal cancer correlates with poor patient outcome. Cancer Res 2013; 73(10): 2955-64. doi: 10.1158/0008-5472.CAN-12-2052 PMID: 23539446
  95. Rey I, Lindarto D, Yusuf F, Putra A. CD166 as cancer stem cells marker based on colorectal cancer location and individual characteristic. J Kedokteran Syiah Kuala 2022.
  96. Hadjimichael C, Chanoumidou K, Papadopoulou N, Arampatzi P, Papamatheakis J, Kretsovali A. Common stemness regulators of embryonic and cancer stem cells. World J Stem Cells 2015; 7(9): 1150-84. doi: 10.4252/wjsc.v7.i9.1150 PMID: 26516408
  97. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006; 126(4): 663-76. doi: 10.1016/j.cell.2006.07.024 PMID: 16904174
  98. Amini S, Fathi F, Mobalegi J, Sofimajidpour H, Ghadimi T. The expressions of stem cell markers: OCT4, Nanog, Sox2, nucleostemin, Bmi, Zfx, Tcl1, Tbx3, Dppa4, and Esrrb in bladder, colon, and prostate cancer, and certain cancer cell lines. Anat Cell Biol 2014; 47(1): 1-11. doi: 10.5115/acb.2014.47.1.1 PMID: 24693477
  99. Shi G, Jin Y. Role of OCT4 in maintaining and regaining stem cell pluripotency. Stem Cell Res Ther 2010; 1(5): 39. doi: 10.1186/scrt39 PMID: 21156086
  100. Zhang Q, Han Z, Zhu Y, Chen J, Li W. The role and specific mechanism of OCT4 in cancer stem cells: A review. Int J Stem Cells 2020; 13(3): 312-25. doi: 10.15283/ijsc20097 PMID: 32840233
  101. Dai X, Ge J, Wang X, Qian X, Zhang C, Li X. OCT4 regulates epithelial-mesenchymal transition and its knockdown inhibits colorectal cancer cell migration and invasion. Oncol Rep 2013; 29(1): 155-60. doi: 10.3892/or.2012.2086 PMID: 23076549
  102. Beiraghdar M, Talebi A, Kianersi K. Comparison of gene expression of SOX2 and OCT4 in normal tissue, polyps, and colon adenocarcinoma using immunohistochemical staining. Adv Biomed Res 2015; 4(1): 234. doi: 10.4103/2277-9175.167958 PMID: 26645019
  103. Neumann J, Bahr F, Horst D, et al. SOX2 expression correlates with lymph-node metastases and distant spread in right-sided colon cancer. BMC Cancer 2011; 11(1): 518. doi: 10.1186/1471-2407-11-518 PMID: 22168803
  104. Avery S, Inniss K, Moore H. The regulation of self-renewal in human embryonic stem cells. Stem Cells Dev 2006; 15(5): 729-40. doi: 10.1089/scd.2006.15.729 PMID: 17105408
  105. Masui S, Nakatake Y, Toyooka Y, et al. Pluripotency governed by Sox2 via regulation of Oct3/4 expression in mouse embryonic stem cells. Nat Cell Biol 2007; 9(6): 625-35. doi: 10.1038/ncb1589 PMID: 17515932
  106. Ibrahim EE, Babaei-Jadidi R, Saadeddin A, et al. Embryonic NANOG activity defines colorectal cancer stem cells and modulates through AP1- and TCF-dependent mechanisms. Stem Cells 2012; 30(10): 2076-87. doi: 10.1002/stem.1182 PMID: 22851508
  107. Pan G, Thomson JA. Nanog and transcriptional networks in embryonic stem cell pluripotency. Cell Res 2007; 17(1): 42-9. doi: 10.1038/sj.cr.7310125 PMID: 17211451
  108. Leng Z, Tao K, Xia Q, et al. Krüppel-like factor 4 acts as an oncogene in colon cancer stem cell-enriched spheroid cells. PLoS One 2013; 8(2): e56082. doi: 10.1371/journal.pone.0056082 PMID: 23418515
  109. Roudi R, Barodabi M, Madjd Z, Roviello G, Corona SP, Panahi M. Expression patterns and clinical significance of the potential cancer stem cell markers OCT4 and NANOG in colorectal cancer patients. Mol Cell Oncol 2020; 7(5): 1788366. doi: 10.1080/23723556.2020.1788366 PMID: 32944642
  110. Gentric G, Mieulet V, Mechta-Grigoriou F. Heterogeneity in cancer metabolism: New concepts in an old field. Antioxid Redox Signal 2017; 26(9): 462-85. doi: 10.1089/ars.2016.6750 PMID: 27228792
  111. Paldino E, Tesori V, Casalbore P, Gasbarrini A, Puglisi MA. Tumor initiating cells and chemoresistance: Which is the best strategy to target colon cancer stem cells? Biomed Res Int 2014; 2014: 859871. doi: 10.1155/2014/859871
  112. Menendez J, Joven J, Cufí S, et al. The Warburg effect version 2.0: Metabolic reprogramming of cancer stem cells. Cell Cycle 2013; 12(8): 1166-79. doi: 10.4161/cc.24479 PMID: 23549172
  113. Wang M, Han D, Yuan Z, et al. Long non-coding RNA H19 confers 5-Fu resistance in colorectal cancer by promoting SIRT1-mediated autophagy. Cell Death Dis 2018; 9(12): 1149. doi: 10.1038/s41419-018-1187-4 PMID: 30451820
  114. Zu G, Ji A, Zhou T, Che N. Clinicopathological significance of SIRT1 expression in colorectal cancer: A systematic review and meta analysis. Int J Surg 2016; 26: 32-7. doi: 10.1016/j.ijsu.2016.01.002 PMID: 26763348
  115. Su BC, Xiao KM, Wang K, Yang SF, Huang ZX, Luo JW. ATGL promotes colorectal cancer growth by regulating autophagy process and SIRT1 expression. Med Oncol 2023; 40(12): 350. doi: 10.1007/s12032-023-02148-w PMID: 37935950
  116. Yu DF, Jiang SJ, Pan ZP, et al. Expression and clinical significance of Sirt1 in colorectal cancer. Oncol Lett 2016; 11(2): 1167-72. doi: 10.3892/ol.2015.3982 PMID: 26893713
  117. Wang XW, Jiang YH, Ye W, Shao CF, Xie JJ, Li X. SIRT1 promotes the progression and chemoresistance of colorectal cancer through the p53/miR-101/KPNA3 axis. Cancer Biol Ther 2023; 24(1): 2235770. doi: 10.1080/15384047.2023.2235770 PMID: 37575080
  118. Yang Y, Yuan H, Zhao L, et al. Targeting the miR-34a/LRPPRC/MDR1 axis collapse the chemoresistance in P53 inactive colorectal cancer. Cell Death Differ 2022; 29(11): 2177-89. doi: 10.1038/s41418-022-01007-x PMID: 35484333
  119. Qiao PF, Yao L, Zeng ZL. Catalpol-mediated microRNA-34a suppresses autophagy and malignancy by regulating SIRT1 in colorectal cancer. Oncol Rep 2020; 43(4): 1053-66. doi: 10.3892/or.2020.7494 PMID: 32323786
  120. Zhang Q, Wang J, Li N, et al. miR-34a increases the sensitivity of colorectal cancer cells to 5-fluorouracil in vitro and in vivo. Am J Cancer Res 2018; 8(2): 280-90. PMID: 29511598
  121. Lucena-Cacace A, Otero-Albiol D, Jiménez-García MP, Muñoz- Galvan S, Carnero A. NAMPT is a potent oncogene in colon cancer progression that modulates cancer stem cell properties and resistance to therapy through Sirt1 and PARP. Clin Cancer Res 2018; 24(5): 1202-15. doi: 10.1158/1078-0432.CCR-17-2575 PMID: 29203587
  122. Yao J, Yang J, Yang Z, et al. FBXW11 contributes to stem-cell- like features and liver metastasis through regulating HIC1-mediated SIRT1 transcription in colorectal cancer. Cell Death Dis 2021; 12(10): 930. doi: 10.1038/s41419-021-04185-7 PMID: 34642302
  123. Chen X, Sun K, Jiao S, et al. High levels of SIRT1 expression enhance tumorigenesis and associate with a poor prognosis of colorectal carcinoma patients. Sci Rep 2014; 4(1): 7481. doi: 10.1038/srep07481 PMID: 25500546
  124. Ashrafizadeh M, Mirzaei S, Hushmandi K, et al. Therapeutic potential of AMPK signaling targeting in lung cancer: Advances, challenges and future prospects. Life Sci 2021; 278: 119649. doi: 10.1016/j.lfs.2021.119649 PMID: 34043989
  125. Ananthram KJ, Rajeev M, Aneesh TP. Insights into the role of mTOR/AMPK as a potential target for anticancer therapy. Curr Drug Ther 2021; 16(4): 299-312. doi: 10.2174/1574885516666210812092321
  126. Ng CAW, Jiang AA, Toh EMS, et al. Metformin and colorectal cancer: A systematic review, meta-analysis and meta-regression. Int J Colorectal Dis 2020; 35(8): 1501-12. doi: 10.1007/s00384-020-03676-x PMID: 32592092
  127. Ashamalla M, Youssef I, Yacoub M, Jayarangaiah A, Gupta N, Ray J. Obesity, diabetes and gastrointestinal malignancy: The role of metformin and other anti-diabetic therapy. Glob J Obes 2018; 5(2): 8.
  128. León-González AJ, Jiménez-Vacas JM, Fuentes-Fayos AC, et al. Role of metformin and other metabolic drugs in the prevention and therapy of endocrine-related cancers. Curr Opin Pharmacol 2021; 60: 17-26. doi: 10.1016/j.coph.2021.06.002 PMID: 34311387
  129. Zhang Y, Guan M, Zheng Z, Zhang Q, Gao F, Xue Y. Effects of metformin on CD133+ colorectal cancer cells in diabetic patients. PLoS One 2013; 8(11): e81264. doi: 10.1371/journal.pone.0081264 PMID: 24278407
  130. Kim SH, Kim SC, Ku JL. Metformin increases chemo-sensitivity via gene downregulation encoding DNA replication proteins in 5- Fu resistant colorectal cancer cells. Oncotarget 2017; 8(34): 56546-57. doi: 10.18632/oncotarget.17798 PMID: 28915611
  131. Sethy C, Kundu CN. 5-Fluorouracil (5-FU) resistance and the new strategy to enhance the sensitivity against cancer: Implication of DNA repair inhibition. Biomed Pharmacother 2021; 137: 111285. doi: 10.1016/j.biopha.2021.111285 PMID: 33485118
  132. Lee J, Choi EA, Kim YS, et al. Metformin usage and the risk of colorectal cancer: A national cohort study. Int J Colorectal Dis 2021; 36(2): 303-10. doi: 10.1007/s00384-020-03765-x PMID: 32968891
  133. Canha MI, Ramos G, Prata R, Lages Martins P, Viúla Ramos M, Coimbra J. Is metformin associated with a lower prevalence of polyps, adenomas, and colorectal carcinoma in patients with diabetes mellitus? J Gastrointest Cancer 2023; 1-9. doi: 10.1007/s12029-023-00989-2 PMID: 37987968
  134. Jahanafrooz Z, Mosafer J, Akbari M, Hashemzaei M, Mokhtarzadeh A, Baradaran B. Colon cancer therapy by focusing on colon cancer stem cells and their tumor microenvironment. J Cell Physiol 2020; 235(5): 4153-66. doi: 10.1002/jcp.29337 PMID: 31647128
  135. Zhang R, Qi F, Zhao F, et al. Cancer-associated fibroblasts enhance tumor-associated macrophages enrichment and suppress NK cells function in colorectal cancer. Cell Death Dis 2019; 10(4): 273. doi: 10.1038/s41419-019-1435-2 PMID: 30894509
  136. Luo S, Yang G, Ye P, et al. Macrophages are a double-edged sword: molecular crosstalk between tumor-associated macrophages and cancer stem cells. Biomolecules 2022; 12(6): 850. doi: 10.3390/biom12060850 PMID: 35740975
  137. Lin CC, Liao TT, Yang MH. Immune adaptation of colorectal cancer stem cells and their interaction with the tumor microenvironment. Front Oncol 2020; 10: 588542. doi: 10.3389/fonc.2020.588542 PMID: 33312953
  138. Ishimoto T, Izumi D, Sakamoto Y, Miyamoto Y, Baba H. Molecular insights into colorectal cancer stem cell regulation by environmental factors. J Cancer Metastasis Treat 2015; 1(3): 156-62. doi: 10.4103/2394-4722.165532
  139. Tauriello DVF, Batlle E. Targeting the microenvironment in advanced colorectal cancer. Trends Cancer 2016; 2(9): 495-504. doi: 10.1016/j.trecan.2016.08.001 PMID: 28741478
  140. Shi J, Fan L, Li B, Pan H. Molecular mechanism of integrin αvβ6 in liver metastasis of colon cancer based on SDF-1/CXCR4. Cell Mol Biol 2022; 67(5): 88-95. doi: 10.14715/cmb/2021.67.6.12 PMID: 35818267
  141. Sun L, Li Q, Guo Y, et al. Extract of Caulis Spatholobi, a novel platelet inhibitor, efficiently suppresses metastasis of colorectal cancer by targeting tumor cell-induced platelet aggregation. Biomed Pharmacother 2020; 123: 109718. doi: 10.1016/j.biopha.2019.109718 PMID: 31918208
  142. Zou W, Zhao J, Li Y, et al. Rat bone marrow-derived mesenchymal stem cells promote the migration and invasion of colorectal cancer stem cells. OncoTargets Ther 2020; 13: 6617-28. doi: 10.2147/OTT.S249353 PMID: 32764957
  143. Shimokawa M, Ohta Y, Nishikori S, et al. Visualization and targeting of LGR5+ human colon cancer stem cells. Nature 2017; 545(7653): 187-92. doi: 10.1038/nature22081 PMID: 28355176
  144. Huang JL, Oshi M, Endo I, Takabe K. Clinical relevance of stem cell surface markers CD133, CD24, and CD44 in colorectal cancer. Am J Cancer Res 2021; 11(10): 5141-54. PMID: 34765317
  145. Sadeghi A, Roudi R, Mirzaei A, Zare Mirzaei A, Madjd Z, Abolhasani M. CD44 epithelial isoform inversely associates with invasive characteristics of colorectal cancer. Biomarkers Med 2019; 13(6): 419-26. doi: 10.2217/bmm-2018-0337 PMID: 30942083

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2024 Bentham Science Publishers