J Appl Biomed 19:181-189, 2021 | DOI: 10.32725/jab.2021.019

Does GD2 synthase (GD2S) detect cancer stem cells in blood samples of breast carcinomas?

Maryam Mansoori1, 2, Isa Abdi Rad3, Alireza Mirzaei4, Kevin J. Tam5, Seyed Mohsen Hosseini6, Rahim Mahmodlu7, Fatemeh Mansouri8, Leili Saeednejad Zanjani1, Zahra Madjd1, 2, *
1 Iran University of Medical Sciences, Oncopathology Research Center, Tehran, Iran
2 Iran University of Medical Sciences, Faculty of Advanced Technologies in Medicine, Department of Molecular Medicine, Tehran, Iran
3 Urmia University of Medical Sciences, Cellular and Molecular Research Center, Urmia, Iran
4 Iran University of Medical Sciences, Shafa Orthopedic Hospital, Bone and Joint Reconstruction Research Center, Tehran, Iran
5 University of British Columbia, Vancouver Prostate Centre, Department of Urologic Sciences, Vancouver, Canada
6 Omid specialty and subspecialty Hospital, Oncology and Radiotherapy Ward, Urmia, Iran
7 Urmia University of Medical Sciences, Faculty of Medicine, Imam Khomeini Hospital, Department of Surgery, Urmia, Iran
8 Urmia University of Medical Sciences, Faculty of Medicine, Department of Genetics and Immunology, Urmia, Iran

Introduction: Cancer stem cells (CSCs) are a theorized subset of cells within the tumor that is thought to drive disease recurrence and metastatic spread. The aim of this study is to investigate mRNA and protein levels of ganglioside GD2 synthase (GD2S), in breast cancer (BC) patients.

Methods: 65 PBMCs of preoperative BC patients without chemotherapy were compared to PBMCs after chemotherapy and controls.

Results: GD2S were significantly higher in BC patients after chemotherapy compared to pre-chemotherapy at both mRNA and protein. GD2S was higher in pre-chemotherapy blood samples compared to control samples.

Conclusions: Higher expression of GD2S in BC samples compared to healthy control indicates the potential utility of GD2S as a marker of malignancy.

Keywords: Breast cancer; Cancer stem cell; Circulating cancer stem cell; ELISA; qRT-PCR
Grants and funding:

This study was supported by a grant from Iran University of Medical Sciences (Grant # 94-03-87-26452).

Conflicts of interest:

The authors report no conflict of interests.

Received: November 28, 2020; Revised: August 23, 2021; Accepted: September 3, 2021; Prepublished online: September 16, 2021; Published: December 6, 2021  Show citation

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Mansoori M, Abdi Rad I, Mirzaei A, Tam KJ, Mohsen Hosseini S, Mahmodlu R, et al.. Does GD2 synthase (GD2S) detect cancer stem cells in blood samples of breast carcinomas? J Appl Biomed. 2021;19(4):181-189. doi: 10.32725/jab.2021.019. PubMed PMID: 34907737.
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    References

    1. Abubaker K, Latifi A, Luwor R, Nazaretian S, Zhu H, Quinn MA, et al. (2013). Short-term single treatment of chemotherapy results in the enrichment of ovarian cancer stem cell-like cells leading to an increased tumor burden. Mol Cancer 12: 24. DOI: 10.1186/1476-4598-12-24. Go to original source... Go to PubMed...
    2. Agnoletto C, Corra F, Minotti L, Baldassari F, Crudele F, Cook WJJ, et al. (2019). Heterogeneity in Circulating Tumor Cells: The Relevance of the Stem-Cell Subset. Cancers (Basel) 11(4): 483. DOI: 10.3390/cancers11040483. Go to original source... Go to PubMed...
    3. Ahmed M, Cheung NK (2014). Engineering anti-GD2 monoclonal antibodies for cancer immunotherapy. FEBS Lett 588(2): 288-297. DOI: 10.1016/j.febslet.2013.11.030. Go to original source... Go to PubMed...
    4. Ahmed R (2014). Selective Elimination of Malignant Melanoma Using the Novel Anti-tumor Agents, OSW-1 and PEITC. The University of Texas MD Anderson Cancer Center UTHealth Graduate School of Biomedical Sciences Dissertations and Theses.
    5. Aktas B, Tewes M, Fehm T, Hauch S, Kimmig R, Kasimir-Bauer S (2009). Stem cell and epithelial-mesenchymal transition markers are frequently overexpressed in circulating tumor cells of metastatic breast cancer patients. Breast Cancer Res 11(4): R46. DOI: 10.1186/bcr2333. Go to original source... Go to PubMed...
    6. Anampa J, Makower D, Sparano JA (2015). Progress in adjuvant chemotherapy for breast cancer: an overview. BMC Med 13: 195. DOI: 10.1186/s12916-015-0439-8. Go to original source... Go to PubMed...
    7. Azubuike SO, Muirhead C, Hayes L, McNally R (2018). Rising global burden of breast cancer: the case of sub-Saharan Africa (with emphasis on Nigeria) and implications for regional development: a review. World J Surg Oncol 16(1): 63. DOI: 10.1186/s12957-018-1345-2. Go to original source... Go to PubMed...
    8. Baba T, Convery PA, Matsumura N, Whitaker RS, Kondoh E, Perry T, et al. (2009). Epigenetic regulation of CD133 and tumorigenicity of CD133+ ovarian cancer cells. Oncogene 28(2): 209-218. DOI: 10.1038/onc.2008.374. Go to original source... Go to PubMed...
    9. Balic M, Lin H, Young L, Hawes D, Giuliano A, McNamara G, et al. (2006). Most early disseminated cancer cells detected in bone marrow of breast cancer patients have a putative breast cancer stem cell phenotype. Clin Cancer Res 12(19): 5615-5621. DOI: 10.1158/1078-0432.CCR-06-0169. Go to original source... Go to PubMed...
    10. Battula VL, Shi Y, Evans KW, Wang RY, Spaeth EL, Jacamo RO, et al. (2012). Ganglioside GD2 identifies breast cancer stem cells and promotes tumorigenesis. J Clin Invest 122(6): 2066-2078. DOI: 10.1172/JCI59735. Go to original source... Go to PubMed...
    11. Cavdarli S, Delannoy P, Groux-Degroote S (2020). O-acetylated Gangliosides as Targets for Cancer Immunotherapy. Cells 9(3): 741. DOI: 10.3390/cells9030741. Go to original source... Go to PubMed...
    12. Cazet A, Bobowski M, Rombouts Y, Lefebvre J, Steenackers A, Popa I, et al. (2012). The ganglioside G(D2) induces the constitutiveactivation of c-Met in MDA-MB-231 breast cancer cells expressing the G(D3) synthase. Glycobiology 22(6): 806-816. DOI: 10.1093/glycob/cws049. Go to original source... Go to PubMed...
    13. Chen K, Huang YH, Chen JL (2013). Understanding and targeting cancer stem cells: therapeutic implications and challenges. Acta Pharmacol Sin 34(6): 732-740. DOI: 10.1038/aps.2013.27. Go to original source... Go to PubMed...
    14. Chen W, Dong J, Haiech J, Kilhoffer MC, Zeniou M (2016). Cancer Stem Cell Quiescence and Plasticity as Major Challenges in Cancer Therapy. Stem Cells Int 2016: 1740936. DOI: 10.1155/2016/1740936. Go to original source... Go to PubMed...
    15. Cheung IY, Cheung NK (2001). Quantitation of marrow disease in neuroblastoma by real-time reverse transcription-PCR. Clin Cancer Res 7(6): 1698-1705.
    16. Cheung IY, Lo Piccolo MS, Kushner BH, Kramer K, Cheung NK (2003). Quantitation of GD2 synthase mRNA by real-time reverse transcriptase polymerase chain reaction: clinical utility in evaluating adjuvant therapy in neuroblastoma. J Clin Oncol 21(6): 1087-1093. DOI: 10.1200/JCO.2003.02.055. Go to original source... Go to PubMed...
    17. Chow EK, Fan LL, Chen X, Bishop JM (2012). Oncogene-specific formation of chemoresistant murine hepatic cancer stem cells. Hepatology 56(4): 1331-1341. DOI: 10.1002/hep.25776. Go to original source... Go to PubMed...
    18. da Silva A (2017). Investigating c-FLIP Suppression and TRAIL Treatment in Breast Cancer. PhD Thesis. Cardiff University.
    19. De Francesco EM, Sotgia F, Lisanti MP (2018). Cancer stem cells (CSCs): metabolic strategies for their identification and eradication. Biochem J 475(9): 1611-1634. DOI: 10.1042/BCJ20170164. Go to original source... Go to PubMed...
    20. Dehghan Esmatabadi MJ, Movahedi Motlagh F, Etemadzadeh A, Hajigholami S (2018). The Most Well-known Markers of CSCs and Their Role in Growth of Tumors, Drug Resistance and Metastasis. J Human Gen Genom 2(1): e65253. DOI: 10.5812/jhgg.65253. Go to original source...
    21. Doronin II, Vishnyakova PA, Kholodenko IV, Ponomarev ED, Ryazantsev DY, Molotkovskaya IM, et al. (2014). Ganglioside GD2 in reception and transduction of cell death signal in tumor cells. BMC Cancer 14: 295. DOI: 10.1186/1471-2407-14-295. Go to original source... Go to PubMed...
    22. Dylla SJ, Beviglia L, Park IK, Chartier C, Raval J, Ngan L, et al. (2008). Colorectal cancer stem cells are enriched in xenogeneic tumors following chemotherapy. PLoS One 3(6): e2428. DOI: 10.1371/journal.pone.0002428. Go to original source... Go to PubMed...
    23. Dzobo K, Senthebane DA, Rowe A, Thomford NE, Mwapagha LM, Al-Awwad N, et al. (2016). Cancer Stem Cell Hypothesis for Therapeutic Innovation in Clinical Oncology? Taking the Root Out, Not Chopping the Leaf. OMICS 20(12): 681-691. DOI: 10.1089/omi.2016.0152. Go to original source... Go to PubMed...
    24. Fitzgibbons P, Connolly J (2019). Protocol for the Examination of Biopsy Specimens From Patients With Invasive Carcinoma of the Breast. College of American Pathologists (CAP).
    25. Fleurence J, Fougeray S, Bahri M, Cochonneau D, Clemenceau B, Paris F, et al. (2017). Targeting O-Acetyl-GD2 Ganglioside for Cancer Immunotherapy. J Immunol Res 2017: 5604891. DOI: 10.1155/2017/5604891. Go to original source... Go to PubMed...
    26. Furukawa K, Takamiya K, Furukawa K (2002). Beta1,4-N-acetylgalactosaminyltransferase - GM2/GD2 synthase: a key enzyme to control the synthesis of brain-enriched complex gangliosides. Biochim Biophys Acta 1573(3): 356-362. DOI: 10.1016/s0304-4165(02)00403-8. Go to original source... Go to PubMed...
    27. Gregoire V, Ang K, Budach W, Grau C, Hamoir M, Langendijk JA, et al. (2014). Delineation of the neck node levels for head and neck tumors: a 2013 update. DAHANCA, EORTC, HKNPCSG, NCIC CTG, NCRI, RTOG, TROG consensus guidelines. Radiother Oncol 110(1): 172-181. DOI: 10.1016/j.radonc.2013.10.010. Go to original source... Go to PubMed...
    28. Grolz D, Hauch S, Schlumpberger M, Guenther K, Voss T, Sprenger-Haussels M, Oelmuller U (2018). Liquid Biopsy Preservation Solutions for Standardized Pre-Analytical Workflows-Venous Whole Blood and Plasma. Curr Pathobiol Rep 6(4): 275-286. DOI: 10.1007/s40139-018-0180-z. Go to original source... Go to PubMed...
    29. Hamilton G, Olszewski U (2013). Chemotherapy-induced Enrichment of Cancer Stem Cells in Lung Cancer. J Bioanal Biomed S9: 003. DOI: 10.4172/1948-593X.S9-003. Go to original source...
    30. Hermann PC, Huber SL, Herrler T, Aicher A, Ellwart JW, Guba M, et al. (2007). Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell 1(3): 313-323. DOI: 10.1016/j.stem.2007.06.002. Go to original source... Go to PubMed...
    31. Ho MM, Ng AV, Lam S, Hung JY (2007). Side population in human lung cancer cell lines and tumors is enriched with stem-like cancer cells. Cancer Res 67(10): 4827-33. DOI: 10.1158/0008-5472.CAN-06-3557. Go to original source... Go to PubMed...
    32. Inoue A, Takahashi H, Harada H, Kohno S, Ohue S, Kobayashi K, et al. (2010). Cancer stem-like cells of glioblastoma characteristically express MMP-13 and display highly invasive activity. Int J Oncol 37(5): 1121-1131. DOI: 10.3892/ijo_00000764. Go to original source... Go to PubMed...
    33. Kasimir-Bauer S, Hoffmann O, Wallwiener D, Kimmig R, Fehm T (2012). Expression of stem cell and epithelial-mesenchymal transition markers in primary breast cancer patients with circulating tumor cells. Breast Cancer Res 14(1): R15. DOI: 10.1186/bcr3099. Go to original source... Go to PubMed...
    34. Katoh S, Goi T, Naruse T, Ueda Y, Kurebayashi H, Nakazawa T, et al. (2015). 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 35: 239-244. Go to PubMed...
    35. Kwon KM, Chung TW, Kwak CH, Choi HJ, Kim KW, Ha SH, et al. (2017). Disialyl GD2 ganglioside suppresses ICAM-1-mediated invasiveness in human breast cancer MDA-MB231 cells. Int J Biol Sci 13(3): 265-275. DOI: 10.7150/ijbs.16903. Go to original source... Go to PubMed...
    36. Laurent VE, Otero LL, Vazquez V, Camarero S, Gabri MR, Labraga M, et al. (2010). Optimization of molecular detection of GD2 synthase mRNA in retinoblastoma. Mol Med Rep 3(2): 253-259. DOI: 10.3892/mmr_00000248. Go to original source... Go to PubMed...
    37. Lefebvre T, Delannoy P (2019). Disrupting membrane lipids composition promotes tumorigenesis: the other dark side of cholesterol and the potential implication of gangliosides. Transl Cancer Res 7(Suppl. 5): S587-S590. DOI: 10.21037/tcr.2018.04.26. Go to original source...
    38. Li C, Wu J-J, Hynes M, Dosch J, Sarkar B, Welling TH, et al. (2011). c-Met is a marker of pancreatic cancer stem cells and therapeutic target. Gastroenterology 141(6): 2218-2227.e5. DOI: 10.1053/j.gastro.2011.08.009. Go to original source... Go to PubMed...
    39. Liang YJ, Ding Y, Levery SB, Lobaton M, Handa K, Hakomori SI (2013). Differential expression profiles of glycosphingolipids in human breast cancer stem cells vs. cancer non-stem cells. Proc Natl Acad Sci U S A 110(13): 4968-4973. DOI: 10.1073/pnas.1302825110. Go to original source... Go to PubMed...
    40. Liang YJ, Wang CY, Wang IA, Chen YW, Li LT, Lin CY, et al. (2017). Interaction of glycosphingolipids GD3 and GD2 with growth factor receptors maintains breast cancer stem cell phenotype. Oncotarget 8(29): 47454-47473. DOI: 10.18632/oncotarget.17665. Go to original source... Go to PubMed...
    41. Lichtinghagen R, Musholt PB, Lein M, Romer A, Rudolph B, Kristiansen G, et al. (2002). Different mRNA and protein expression of matrix metalloproteinases 2 and 9 and tissue inhibitor of metalloproteinases 1 in benign and malignant prostate tissue. Eur Urol 42(4): 398-406. DOI: 10.1016/s0302-2838(02)00324-x. Go to original source... Go to PubMed...
    42. Lo Piccolo MS, Cheung NK, Cheung IY (2001). GD2 synthase: a new molecular marker for detecting neuroblastoma. Cancer 92(4): 924-931. DOI: 10.1002/1097-0142(20010815)92:43.0.co;2-o. Go to original source...
    43. Mahata B, Banerjee A, Kundu M, Bandyopadhyay U, Biswas K (2015). TALEN mediated targeted editing of GM2/GD2-synthase gene modulates anchorage independent growth by reducing anoikis resistance in mouse tumor cells. Sci Rep 5: 9048. DOI: 10.1038/srep09048. Go to original source... Go to PubMed...
    44. Mansoori M, Roudi R, Abbasi A, Abolhasani M, Abdi Rad I, Shariftabrizi A, Madjd Z (2019). High GD2 expression defines breast cancer cells with enhanced invasiveness. Exp Mol Pathol 109: 25-35. DOI: 10.1016/j.yexmp.2019.05.001. Go to original source... Go to PubMed...
    45. Marrugo-Ramirez J, Mir M, Samitier J (2018). Blood-Based Cancer Biomarkers in Liquid Biopsy: A Promising Non-Invasive Alternative to Tissue Biopsy. Int J Mol Sci 19(10): 2877. DOI: 10.3390/ijms19102877. Go to original source... Go to PubMed...
    46. Martinez C, Hofmann TJ, Marino R, Dominici M, Horwitz EM (2007). Human bone marrow mesenchymal stromal cells express the neural ganglioside GD2: a novel surface marker for the identification of MSCs. Blood 109(10): 4245-4248. DOI: 10.1182/blood-2006-08-039347. Go to original source... Go to PubMed...
    47. Massague J, Batlle E, Gomis RR (2017). Understanding the molecular mechanisms driving metastasis. Mol Oncol 11(1): 3-4. DOI: 10.1002/1878-0261.12024. Go to original source... Go to PubMed...
    48. Mathews L (Ed.) (2013). DNA Repair of Cancer Stem Cells. Heidelberg: Springer. Go to original source...
    49. Mirzaei A, Madjd Z, Kadijani AA, Tavakoli-Yaraki M, Modarresi MH, Verdi J, et al. (2016). Evaluation of circulating cellular DCLK1 protein, as the most promising colorectal cancer stem cell marker, using immunoassay based methods. Cancer Biomark 17(3): 301-311. DOI: 10.3233/CBM-160642. Go to original source... Go to PubMed...
    50. Mirzaei A, Tavoosidana G, Modarressi MH, Rad AA, Fazeli MS, Shirkoohi R, et al. (2015). Upregulation of circulating cancer stem cell marker, DCLK1 but not Lgr5, in chemoradiotherapy-treated colorectal cancer patients. Tumour Biol 36(6): 4801-4810. DOI: 10.1007/s13277-015-3132-9. Go to original source... Go to PubMed...
    51. Nazha B, Inal C, Owonikoko TK (2020). Disialoganglioside GD2 Expression in Solid Tumors and Role as a Target for Cancer Therapy. Front Oncol 10: 1000. DOI: 10.3389/fonc.2020.01000. Go to original source... Go to PubMed...
    52. Nian WQ, Chen FL, Ao XJ, Chen ZT (2011). CXCR4 positive cells from Lewis lung carcinoma cell line have cancer metastatic stem cell characteristics. Mol Cell Biochem 355(1-2): 241-248. DOI: 10.1007/s11010-011-0860-z. Go to original source... Go to PubMed...
    53. Owens TW, Naylor MJ (2013). Breast cancer stem cells. Front Physiol 4: 225. DOI: 10.3389/fphys.2013.00225. Go to original source... Go to PubMed...
    54. Pang R, Law WL, Chu AC, Poon JT, Lam CS, Chow AK, et al. (2010). A subpopulation of CD26+ cancer stem cells with metastatic capacity in human colorectal cancer. Cell Stem Cell 6(6): 603-615. DOI: 10.1016/j.stem.2010.04.001. Go to original source... Go to PubMed...
    55. Pawlik TM, Keyomarsi K (2004). Role of cell cycle in mediating sensitivity to radiotherapy. Int J Radiat Oncol Biol Phys 59(4): 928-942. DOI: 10.1016/j.ijrobp.2004.03.005. Go to original source... Go to PubMed...
    56. Pawlikowska P, Faugeroux V, Oulhen M, Aberlenc A, Tayoun T, Pailler E, et al. (2019). Circulating tumor cells (CTCs) for the noninvasive monitoring and personalization of non-small cell lung cancer (NSCLC) therapies. J Thorac Dis 11(Suppl 1): S45-S56. DOI: 10.21037/jtd.2018.12.80. Go to original source... Go to PubMed...
    57. Prabavathy D, Swarnalatha Y, Ramadoss N (2018). Lung cancer stem cells-origin, characteristics and therapy. Stem Cell Investig 5: 6. DOI: 10.21037/sci.2018.02.01. Go to original source... Go to PubMed...
    58. Saarenheimo J, Eigeliene N, Andersen H, Tiirola M, Jekunen A (2019). The Value of Liquid Biopsies for Guiding Therapy Decisions in Non-small Cell Lung Cancer. Front Oncol 9: 129. DOI: 10.3389/fonc.2019.00129. Go to original source... Go to PubMed...
    59. Sait S, Modak S (2017). Anti-GD2 immunotherapy for neuroblastoma. Expert Rev Anticancer Ther 17(10): 889-904. DOI: 10.1080/14737140.2017.1364995. Go to original source... Go to PubMed...
    60. Sarro SM, Unruh TL, Zuccolo J, Sanyal R, Luider JM, Auer-Grzesiak IA, et al. (2010). Quantification of CD20 mRNA and protein levels in chronic lymphocytic leukemia suggests a post-transcriptional defect. Leuk Res 34(12): 1670-1673. DOI: 10.1016/j.leukres.2010.06.031. Go to original source... Go to PubMed...
    61. Seigel GM, Campbell LM, Narayan M, Gonzalez-Fernandez F (2005). Cancer stem cell characteristics in retinoblastoma. Mol Vis 11: 729-737.
    62. Shebl FM, Pinto LA, Garcia-Pineres A, Lempicki R, Williams M, Harro C, et al. (2010). Comparison of mRNA and protein measures of cytokines following vaccination with human papillomavirus-16 L1 virus-like particles. Cancer Epidemiol Biomarkers Prev 19(4): 978-981. DOI: 10.1158/1055-9965.EPI-10-0064. Go to original source... Go to PubMed...
    63. Siegel RL, KD Miller, HE Fuchs, Jemal A (2021). Cancer Statistics, 2021. CA Cancer J Clin 71(1): 7-33. DOI: 10.3322/caac.21654. Go to original source... Go to PubMed...
    64. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, et al. (2004). Identification of human brain tumour initiating cells. Nature 432(7015): 396-401. DOI: 10.1038/nature03128. Go to original source... Go to PubMed...
    65. Sphyris N, Sarkar TR, Battula VL, Andreeff M, Mani SA (2015). GD2 and GD3 synthase: novel drug targets for cancer therapy. Mol Cell Oncol 2(3): e975068. DOI: 10.4161/23723556.2014.975068. Go to original source... Go to PubMed...
    66. Sun S, Wang Z (2011). Head neck squamous cell carcinoma c-Met(+) cells display cancer stem cell properties and are responsible for cisplatin-resistance and metastasis. Int J Cancer 129: 2337-2348. DOI: 10.1002/ijc.25927. Go to original source... Go to PubMed...
    67. Taquet N, Dumont S, Vonesch JL, Hentsch D, Reimund LM, Muller CD (2009). Differential between protein and mRNA expression of CCR7 and SSTR5 receptors in Crohn's disease patients. Mediators Inflamm 2009: 285812. DOI: 10.1155/2009/285812. Go to original source... Go to PubMed...
    68. Taylor WF, Jabbarzadeh E (2017). The use of natural products to target cancer stem cells. Am J Cancer Res 7(7): 1588-1605.
    69. Tirino V, Desiderio V, Paino F, De Rosa A, Papaccio F, Fazioli F, et al. (2011). Human primary bone sarcomas contain CD133+ cancer stem cells displaying high tumorigenicity in vivo. FASEB J 25(6): 2022-2030. DOI: 10.1096/fj.10-179036. Go to original source... Go to PubMed...
    70. Tirino V, Desiderio V, Paino F, De Rosa A, Papaccio F, La Noce M, et al. (2013). Cancer stem cells in solid tumors: an overview and new approaches for their isolation and characterization. FASEB J 27(1): 13-24. DOI: 10.1096/fj.12-218222. Go to original source... Go to PubMed...
    71. Todaro M, Gaggianesi M, Catalano V, Benfante A, Iovino F, Biffoni M, et al. (2014). CD44v6 is a marker of constitutive and reprogrammed cancer stem cells driving colon cancer metastasis. Cell Stem Cell 14(3): 342-356. DOI: 10.1016/j.stem.2014.01.009. Go to original source... Go to PubMed...
    72. Visvader JE, Lindeman GL (2012). Cancer stem cells: current status and evolving complexities. Cell Stem Cell 10(6): 717-728. DOI: 10.1016/j.stem.2012.05.007. Go to original source... Go to PubMed...
    73. Wang YH, Li F, Luo B, Wang XH, Sun HC, Liu S, et al. (2009). A side population of cells from a human pancreatic carcinoma cell line harbors cancer stem cell characteristics. Neoplasma 56(5): 371-378. DOI: 10.4149/neo_2009_05_371. Go to original source... Go to PubMed...
    74. Yang MH, Imrali A, Heeschen C (2015). Circulating cancer stem cells: the importance to select. Chin J Cancer Res 27(5): 437-449. DOI: 10.3978/j.issn.1000-9604.2015.04.08. Go to original source... Go to PubMed...
    75. Yeh SC, Wang PY, Lou YW, Khoo KH, Hsiao M, Hsu TL, et al. (2016). Glycolipid GD3 and GD3 synthase are key drivers for glioblastoma stem cells and tumorigenicity. Proc Natl Acad Sci U S A 113(20): 5592-5597. DOI: 10.1073/pnas.1604721113. Go to original source... Go to PubMed...
    76. Yoshida H, Koodie L, Jacobsen K, Hanzawa K, Miyamoto Y, Yamamoto M (2020). B4GALNT1 induces angiogenesis, anchorage independence growth and motility, and promotes tumorigenesis in melanoma by induction of ganglioside GM2/GD2. Sci Rep 10: 1199. DOI: 10.1038/s41598-019-57130-2. Go to original source... Go to PubMed...
    77. Zhang SS, Han ZP, Jing YY, Tao SF, Li TJ, Wang H, et al. (2012). CD133(+)CXCR4(+) colon cancer cells exhibit metastatic potential and predict poor prognosis of patients. BMC Med 10: 85. DOI: 10.1186/1741-7015-10-85. Go to original source... Go to PubMed...

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