Drug Delivery Systems Using Surface Markers for Targeting Cancer Stem Cells

Author(s): James T. Oswald*, Haritosh Patel, Daid Khan, Ninweh N. Jeorje, Hossein Golzar, Erin L. Oswald, Shirley Tang

Journal Name: Current Pharmaceutical Design

Volume 26 , Issue 17 , 2020


Become EABM
Become Reviewer
Call for Editor

Abstract:

The innate abilities of cancer stem cells (CSCs), such as multi-drug resistance, drug efflux, quiescence and ionizing radiation tolerance, protect them from most traditional chemotherapeutics. As a result, this small subpopulation of persistent cells leads to more aggressive and chemoresistant cancers, causing tumour relapse and metastasis. This subpopulation is differentiated from the bulk tumour population through a wide variety of surface markers expressed on the cell surface. Recent developments in nanomedicine and targeting delivery methods have given rise to new possibilities for specifically targeting these markers and preferentially eliminating CSCs. Herein, we first summarize the range of surface markers identifying CSC populations in a variety of cancers; then, we discuss recent attempts to actively target CSCs and their niches using liposomal, nanoparticle, carbon nanotube and viral formulations.

Keywords: Cancer Stem Cells (CSC), nanoparticles, targeted delivery, stem cell surface markers, liposomes, surface markers.

[1]
Booth CM, Karim S, Mackillop WJ. Real-world data: towards achieving the achievable in cancer care. Nat Rev Clin Oncol 2019; 16(5): 312-25.
[http://dx.doi.org/10.1038/s41571-019-0167-7] [PMID: 30700859]
[2]
Ayob AZ, Ramasamy TS. Cancer stem cells as key drivers of tumour progression. J Biomed Sci 2018; 25(1): 20.
[http://dx.doi.org/10.1186/s12929-018-0426-4] [PMID: 29506506]
[3]
Cancer Stem Cells: Targeting the Roots of Cancer, Seeds of Metastasis, and Sources of Therapy Resistance | Cancer Research. Available at:. https://cancerres.aacrjournals.org/content/75/6/924.short
[4]
Phi LTH, Sari IN, Yang Y-G, et al. Cancer Stem Cells (CSCs) in Drug Resistance and their Therapeutic Implications in Cancer Treatment. Available at:. https://www.hindawi.com/jour nals/sci/2018/5416923/
[5]
Prieto-Vila M, Takahashi R-U, Usuba W, Kohama I, Ochiya T. drug resistance driven by cancer stem cells and their niche. Int J Mol Sci 2017; 18(12): 18.
[http://dx.doi.org/10.3390/ijms18122574] [PMID: 29194401]
[6]
Shiozawa Y, Nie B, Pienta KJ, Morgan TM, Taichman RS. Cancer stem cells and their role in metastasis. Pharmacol Ther 2013; 138(2): 285-93.
[http://dx.doi.org/10.1016/j.pharmthera.2013.01.014] [PMID: 23384596]
[7]
López-Lázaro M. The stem cell division theory of cancer. Crit Rev Oncol Hematol 2018; 123: 95-113.
[http://dx.doi.org/10.1016/j.critrevonc.2018.01.010] [PMID: 29482784]
[8]
Mukherjee S, Kong J, Brat DJ. Cancer stem cell division: when the rules of asymmetry are broken. Stem Cells Dev 2015; 24(4): 405-16.
[http://dx.doi.org/10.1089/scd.2014.0442] [PMID: 25382732]
[9]
Clevers H. The cancer stem cell: premises, promises and challenges. Nat Med 2011; 17(3): 313-9.
[http://dx.doi.org/10.1038/nm.2304] [PMID: 21386835]
[10]
Tomasetti C, Vogelstein B. Cancer etiology. Variation in cancer risk among tissues can be explained by the number of stem cell divisions. Science 2015; 347(6217): 78-81.
[http://dx.doi.org/10.1126/science.1260825] [PMID: 25554788]
[11]
Bonnet D, Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 1997; 3(7): 730-7.
[http://dx.doi.org/10.1038/nm0797-730] [PMID: 9212098]
[12]
Saygin C, Matei D, Majeti R, Reizes O, Lathia JD. Targeting cancer stemness in the clinic: from hype to hope. Cell Stem Cell 2019; 24(1): 25-40.
[http://dx.doi.org/10.1016/j.stem.2018.11.017] [PMID: 30595497]
[13]
Kreso A, Dick JE. Evolution of the cancer stem cell model. Cell Stem Cell 2014; 14(3): 275-91.
[http://dx.doi.org/10.1016/j.stem.2014.02.006] [PMID: 24607403]
[14]
Liu X, Fan D. The epithelial-mesenchymal transition and cancer stem cells: functional and mechanistic links. Curr Pharm Des 2015; 21(10): 1279-91.
[http://dx.doi.org/10.2174/1381612821666141211115611] [PMID: 25506898]
[15]
Nakano M, Kikushige Y, Miyawaki K, et al. Dedifferentiation process driven by TGF-beta signaling enhances stem cell properties in human colorectal cancer. Oncogene 2019; 38(6): 780-93.
[http://dx.doi.org/10.1038/s41388-018-0480-0] [PMID: 30181548]
[16]
Begicevic R-R, Falasca M. ABC Transporters in Cancer Stem Cells: Beyond Chemoresistance. Int J Mol Sci 2017; 18(11): 18.
[http://dx.doi.org/10.3390/ijms18112362] [PMID: 29117122]
[17]
Charles N, Ozawa T, Squatrito M, et al. Perivascular nitric oxide activates notch signaling and promotes stem-like character in PDGF-induced glioma cells. Cell Stem Cell 2010; 6(2): 141-52.
[http://dx.doi.org/10.1016/j.stem.2010.01.001] [PMID: 20144787]
[18]
Muz B, de la Puente P, Azab F, Azab AK. The role of hypoxia in cancer progression, angiogenesis, metastasis, and resistance to therapy. Hypoxia (Auckl) 2015; 3: 83-92.
[http://dx.doi.org/10.2147/HP.S93413] [PMID: 27774485]
[19]
Li XS, Xu Q, Fu XY, Luo WS. ALDH1A1 overexpression is associated with the progression and prognosis in gastric cancer. BMC Cancer 2014; 14: 705.
[http://dx.doi.org/10.1186/1471-2407-14-705] [PMID: 25253129]
[20]
Ferreira JA, Peixoto A, Neves M, et al. Mechanisms of cisplatin resistance and targeting of cancer stem cells: Adding glycosylation to the equation. Drug Resist Updat 2016; 24: 34-54.
[http://dx.doi.org/10.1016/j.drup.2015.11.003] [PMID: 26830314]
[21]
Wang Y, Shi J, Chai K, Ying X, Zhou BP. The Role of Snail in EMT and Tumorigenesis. Curr Cancer Drug Targets 2013; 13(9): 963-72.
[http://dx.doi.org/10.2174/15680096113136660102] [PMID: 24168186]
[22]
Wang K, Wu X, Wang J, Huang J. Cancer stem cell theory: therapeutic implications for nanomedicine. Int J Nanomedicine 2013; 8: 899-908.
[PMID: 23467584]
[23]
Zhou B-BS, Zhang H, Damelin M, Geles KG, Grindley JC, Dirks PB. Tumour-initiating cells: challenges and opportunities for anticancer drug discovery. Nat Rev Drug Discov 2009; 8(10): 806-23.
[http://dx.doi.org/10.1038/nrd2137] [PMID: 19794444]
[24]
Dylla SJ, Beviglia L, Park IK, et al. Colorectal cancer stem cells are enriched in xenogeneic tumors following chemotherapy. PLoS One 2008; 3(6) e2428
[http://dx.doi.org/10.1371/journal.pone.0002428] [PMID: 18560594]
[25]
BikDD Eliminates Breast Cancer Initiating Cells and Synergizes with Lapatinib for Breast Cancer Treatment | Elsevier Enhanced Reader. Available at:. https://reader.elsevier.com/rea der/sd/pii/S1535610811002674?token=8BA7B3ACB9DED5566C9F78A46BBF87C9360657C3982992010B1BCA63E25F7250A72B03B66C9DE2B5D3976EB67A3C8CC5
[26]
Identification of Selective Inhibitors of Cancer Stem Cells by High- Throughput Screening | Elsevier Enhanced Reader. Available at:. https://reader.elsevier.com/reader/sd/pii/S0092867409007818?token=75386C7F0C6C3BA127F0AD31D1534F374828FD038A2234B97D0FB7EEA787674C6B83D60A7C6F75F9648E6B7BBD40486A
[27]
Identification of Drugs Including& Dopamine&Receptor Antagonist that Selectively Target Cancer Stem Cells | Elsevier Enhanced Reader. Available at:. https://reader.elsevier.com/rea der/sd/pii/S0092867412005715?token=8689BADD7C2DDA2D1A12061FD58B4A41779D8EEF33920F27923E0EB25E8EB4A2823A2C92D81B1602EEF19B754062D739
[28]
Ablation of Fbxw7 Eliminates Leukemia-Initiating Cells by Preventing Quiescence | Elsevier Enhanced Reader. Available at:. https://reader.elsevier.com/reader/sd/pii/S1535610813000457?token=F97B3DEB12BF31682C09841E08A74A34F022F66AE66E1C6D8DD06765D3CEEB34D60F9F54072A64C10BAFD61E68D5F9B9
[29]
Chen P, Huang H, Wu J, et al. Bone marrow stromal cells protect acute myeloid leukemia cells from anti-CD44 therapy partly through regulating PI3K/Akt-p27(Kip1) axis. Mol Carcinog 2015; 54(12): 1678-85.
[http://dx.doi.org/10.1002/mc.22239] [PMID: 25408361]
[30]
Vey N, Delaunay J, Martinelli G, et al. Phase I clinical study of RG7356, an anti-CD44 humanized antibody, in patients with acute myeloid leukemia. Oncotarget 2016; 7(22): 32532-42.
[http://dx.doi.org/10.18632/oncotarget.8687] [PMID: 27081038]
[31]
Codd AS, Kanaseki T, Torigo T, Tabi Z. Cancer stem cells as targets for immunotherapy. Immunology 2018; 153(3): 304-14.
[http://dx.doi.org/10.1111/imm.12866] [PMID: 29150846]
[32]
Shibata M, Hoque MO. Targeting cancer stem cells: a strategy for effective eradication of cancer. Cancers (Basel) 2019; 11(5): 11.
[http://dx.doi.org/10.3390/cancers11050732] [PMID: 31137841]
[33]
Wang H, He X. Nanoparticles for targeted drug delivery to cancer stem cells and tumor. Methods Mol Biol 2018; 1831: 59-67.
[http://dx.doi.org/10.1007/978-1-4939-8661-3_6] [PMID: 30051425]
[34]
Batlle E, Clevers H. Cancer stem cells revisited. Nat Med 2017; 23(10): 1124-34.
[http://dx.doi.org/10.1038/nm.4409] [PMID: 28985214]
[35]
Velasco-Velázquez MA, Popov VM, Lisanti MP, Pestell RG. The role of breast cancer stem cells in metastasis and therapeutic implications. Am J Pathol 2011; 179(1): 2-11.
[http://dx.doi.org/10.1016/j.ajpath.2011.03.005] [PMID: 21640330]
[36]
Liu P, Wang Z, Brown S, et al. Liposome encapsulated Disulfiram inhibits NFκB pathway and targets breast cancer stem cells in vitro and in vivo. Oncotarget 2014; 5(17): 7471-85.
[http://dx.doi.org/10.18632/oncotarget.2166] [PMID: 25277186]
[37]
Jin C, Bai L, Lin L, Wang S, Yin X. Paclitaxel-loaded nanoparticles decorated with bivalent fragment HAb18 F(ab’)2 and cell penetrating peptide for improved therapeutic effect on hepatocellular carcinoma. Artif Cells Nanomed Biotechnol 2018; 46(5): 1076-84.
[http://dx.doi.org/10.1080/21691401.2017.1360325] [PMID: 28776396]
[38]
Glackin CA. Nanoparticle delivery of TWIST small interfering rna and anticancer drugs: a therapeutic approach for combating cancer. Enzymes 2018; 44: 83-101.
[http://dx.doi.org/10.1016/bs.enz.2018.08.004] [PMID: 30360816]
[39]
Wang K, Sun D. Cancer stem cells of hepatocellular carcinoma. Oncotarget 2018; 9(33): 23306-14.
[http://dx.doi.org/10.18632/oncotarget.24623] [PMID: 29796190]
[40]
Sahlberg SH, Spiegelberg D, Glimelius B, Stenerlöw B, Nestor M. Evaluation of cancer stem cell markers CD133, CD44, CD24: association with AKT isoforms and radiation resistance in colon cancer cells. PLoS One 2014; 9(4) e94621
[http://dx.doi.org/10.1371/journal.pone.0094621] [PMID: 24760019]
[41]
Mahira S, Kommineni N, Husain GM, Khan W. Cabazitaxel and silibinin co-encapsulated cationic liposomes for CD44 targeted delivery: A new insight into nanomedicine based combinational chemotherapy for prostate cancer. Biomed Pharmacother 2019; 110: 803-17.
[http://dx.doi.org/10.1016/j.biopha.2018.11.145] [PMID: 30554119]
[42]
Wang T, Hou J, Su C, Zhao L, Shi Y. Hyaluronic acid-coated chitosan nanoparticles induce ROS-mediated tumor cell apoptosis and enhance antitumor efficiency by targeted drug delivery via CD44. J Nanobiotechnology 2017; 15(1): 7.
[http://dx.doi.org/10.1186/s12951-016-0245-2] [PMID: 28068992]
[43]
Horton SJ, Huntly BJP. Recent advances in acute myeloid leukemia stem cell biology. Haematologica 2012; 97(7): 966-74.
[http://dx.doi.org/10.3324/haematol.2011.054734] [PMID: 22511496]
[44]
Brown HK, Tellez-Gabriel M, Heymann D. Cancer stem cells in osteosarcoma. Cancer Lett 2017; 386: 189-95.
[http://dx.doi.org/10.1016/j.canlet.2016.11.019] [PMID: 27894960]
[45]
Wu H, Shi H, Zhang H, et al. Prostate stem cell antigen antibody-conjugated multiwalled carbon nanotubes for targeted ultrasound imaging and drug delivery. Biomaterials 2014; 35(20): 5369-80.
[http://dx.doi.org/10.1016/j.biomaterials.2014.03.038] [PMID: 24709520]
[46]
Akunuru S, Palumbo J, Zhai QJ, Zheng Y. Rac1 targeting suppresses human non-small cell lung adenocarcinoma cancer stem cell activity. PLoS One 2011; 6(2) e16951
[http://dx.doi.org/10.1371/journal.pone.0016951] [PMID: 21347385]
[47]
Zakaria N, Satar NA, Abu Halim NH, et al. Targeting lung cancer stem cells: research and clinical impacts. Front Oncol 2017; 7: 80.
[http://dx.doi.org/10.3389/fonc.2017.00080] [PMID: 28529925]
[48]
Marzagalli M, Moretti RM, Messi E, et al. Targeting melanoma stem cells with the Vitamin E derivative δ-tocotrienol. Sci Rep 2018; 8(1): 587.
[http://dx.doi.org/10.1038/s41598-017-19057-4] [PMID: 29330434]
[49]
Parmiani G. Melanoma cancer stem cells: markers and functions. Cancers (Basel) 2016; 8(3): 8.
[http://dx.doi.org/10.3390/cancers8030034] [PMID: 26978405]
[50]
Rao CV, Mohammed A. New insights into pancreatic cancer stem cells. World J Stem Cells 2015; 7(3): 547-55.
[http://dx.doi.org/10.4252/wjsc.v7.i3.547] [PMID: 25914762]
[51]
Aigner S, Sthoeger ZM, Fogel M, et al. CD24, a mucin-type glycoprotein, is a ligand for P-selectin on human tumor cells. Blood 1997; 89(9): 3385-95.
[http://dx.doi.org/10.1182/blood.V89.9.3385] [PMID: 9129046]
[52]
Qiao S, Zhao Y, Geng S, et al. A novel double-targeted nondrug delivery system for targeting cancer stem cells. Int J Nanomedicine 2016; 11: 6667-78.
[http://dx.doi.org/10.2147/IJN.S116230] [PMID: 27994463]
[53]
Cho D-Y, Lin S-Z, Yang W-K, et al. Targeting cancer stem cells for treatment of glioblastoma multiforme. Cell Transplant 2013; 22(4): 731-9.
[http://dx.doi.org/10.3727/096368912X655136] [PMID: 23594862]
[54]
Cortes-Dericks L, Schmid RA. CD44 and its ligand hyaluronan as potential biomarkers in malignant pleural mesothelioma: evidence and perspectives. Respir Res 2017; 18(1): 58.
[http://dx.doi.org/10.1186/s12931-017-0546-5] [PMID: 28403901]
[55]
Glumac PM, LeBeau AM. The role of CD133 in cancer: a concise review. Clin Transl Med 2018; 7(1): 18.
[http://dx.doi.org/10.1186/s40169-018-0198-1] [PMID: 29984391]
[56]
Hammar S, Dacic S. Immunohistology of lung and pleural neoplasms. Immunohistochem 2010; pp. 369-463.
[57]
Chen W-C, Chang Y-S, Hsu H-P, et al. Therapeutics targeting CD90-integrin-AMPK-CD133 signal axis in liver cancer. Oncotarget 2015; 6(40): 42923-37.
[http://dx.doi.org/10.18632/oncotarget.5976] [PMID: 26556861]
[58]
Zhang Y, Yang Y, Hong H, Cai W. Multimodality molecular imaging of CD105 (Endoglin) expression. Int J Clin Exp Med 2011; 4(1): 32-42.
[PMID: 21394284]
[59]
Rothstein DM, Livak MF, Kishimoto K, et al. Targeting signal 1 through CD45RB synergizes with CD40 ligand blockade and promotes long term engraftment and tolerance in stringent transplant models. J Immunol 2001; 166(1): 322-9.
[http://dx.doi.org/10.4049/jimmunol.166.1.322] [PMID: 11123308]
[60]
Dunne M, Zheng J, Rosenblat J, Jaffray DA, Allen C. APN/CD13-targeting as a strategy to alter the tumor accumulation of liposomes. J Control Release 2011; 154(3): 298-305.
[http://dx.doi.org/10.1016/j.jconrel.2011.05.022] [PMID: 21640146]
[61]
Carmon KS, Gong X, Lin Q, Thomas A, Liu Q. R-spondins function as ligands of the orphan receptors LGR4 and LGR5 to regulate Wnt/beta-catenin signaling. Proc Natl Acad Sci USA 2011; 108(28): 11452-7.
[http://dx.doi.org/10.1073/pnas.1106083108] [PMID: 21693646]
[62]
Trzpis M, McLaughlin PMJ, de Leij LMFH, Harmsen MC. Epithelial cell adhesion molecule: more than a carcinoma marker and adhesion molecule. Am J Pathol 2007; 171(2): 386-95.
[http://dx.doi.org/10.2353/ajpath.2007.070152] [PMID: 17600130]
[63]
Laszlo GS, Gudgeon CJ, Harrington KH, Walter RB. T-cell ligands modulate the cytolytic activity of the CD33/CD3 BiTE antibody construct, AMG 330. Blood Cancer J 2015; 5 e340
[http://dx.doi.org/10.1038/bcj.2015.68] [PMID: 26295610]
[64]
AbuSamra DB. CD34 is a ligand for vascular selectins on human hematopoietic stem/progenitor cells. Blood 2015; 126: 2399-9.
[http://dx.doi.org/10.1182/blood.V126.23.2399.2399]
[65]
Blázquez-Prunera A, Díez JM, Gajardo R, Grancha S. Human mesenchymal stem cells maintain their phenotype, multipotentiality, and genetic stability when cultured using a defined xeno-free human plasma fraction. Stem Cell Res Ther 2017; 8(1): 103.
[http://dx.doi.org/10.1186/s13287-017-0552-z] [PMID: 28449711]
[66]
Göbel K, Pankratz S, Asaridou C-M, et al. Blood coagulation factor XII drives adaptive immunity during neuroinflammation via CD87-mediated modulation of dendritic cells. Nat Commun 2016; 7: 11626.
[http://dx.doi.org/10.1038/ncomms11626] [PMID: 27188843]
[67]
van Meerten T, Hagenbeek A. CD20-targeted therapy: a breakthrough in the treatment of non-Hodgkin’s lymphoma. Neth J Med 2009; 67(7): 251-9.
[PMID: 19687518]
[68]
Macdonald J, Henri J, Roy K, et al. EpCAM Immunotherapy versus specific targeted delivery of drugs. Cancers (Basel) 2018; 10(1): 10.
[http://dx.doi.org/10.3390/cancers10010019] [PMID: 29329202]
[69]
Sagiv E, Starr A, Rozovski U, et al. Targeting CD24 for treatment of colorectal and pancreatic cancer by monoclonal antibodies or small interfering RNA. Cancer Res 2008; 68(8): 2803-12.
[http://dx.doi.org/10.1158/0008-5472.CAN-07-6463] [PMID: 18413748]
[70]
Fonsatti E, Sigalotti L, Arslan P, Altomonte M, Maio M. Emerging role of endoglin (CD105) as a marker of angiogenesis with clinical potential in human malignancies. Curr Cancer Drug Targets 2003; 3(6): 427-32.
[http://dx.doi.org/10.2174/1568009033481741] [PMID: 14683500]
[71]
Goldstein LA, Zhou DF, Picker LJ, et al. A human lymphocyte homing receptor, the hermes antigen, is related to cartilage proteoglycan core and link proteins. Cell 1989; 56(6): 1063-72.
[http://dx.doi.org/10.1016/0092-8674(89)90639-9] [PMID: 2466576]
[72]
Chen C, Zhao S, Karnad A, Freeman JW. The biology and role of CD44 in cancer progression: therapeutic implications. J Hematol Oncol 2018; 11(1): 64.
[http://dx.doi.org/10.1186/s13045-018-0605-5] [PMID: 29747682]
[73]
Wang L, Zuo X, Xie K, Wei D. The role of CD44 and cancer stem cells. Methods Mol Biol 2018; 1692: 31-42.
[http://dx.doi.org/10.1007/978-1-4939-7401-6_3] [PMID: 28986884]
[74]
Lu B, Huang X, Mo J, Zhao W. Drug delivery using nanoparticles for cancer stem-like cell targeting. Front Pharmacol 2016; 7: 84.
[http://dx.doi.org/10.3389/fphar.2016.00084] [PMID: 27148051]
[75]
Yan Y, Zuo X, Wei D. Concise review: emerging role of CD44 in cancer stem cells: a promising biomarker and therapeutic target. Stem Cells Transl Med 2015; 4(9): 1033-43.
[http://dx.doi.org/10.5966/sctm.2015-0048] [PMID: 26136504]
[76]
Aires A, Ocampo SM, Simões BM, et al. Multifunctionalized iron oxide nanoparticles for selective drug delivery to CD44-positive cancer cells. Nanotechnology 2016; 27(6) 065103
[http://dx.doi.org/10.1088/0957-4484/27/6/065103] [PMID: 26754042]
[77]
Li Z. CD133: a stem cell biomarker and beyond. Exp Hematol Oncol 2013; 2(1): 17.
[http://dx.doi.org/10.1186/2162-3619-2-17] [PMID: 23815814]
[78]
Ni M, Xiong M, Zhang X, et al. Poly(lactic-co-glycolic acid) nanoparticles conjugated with CD133 aptamers for targeted salinomycin delivery to CD133+ osteosarcoma cancer stem cells. Int J Nanomedicine 2015; 10: 2537-54.
[PMID: 25848270]
[79]
Desai A, Yan Y, Gerson SL. Concise reviews: cancer stem cell targeted therapies: toward clinical success. Stem Cells Transl Med 2019; 8(1): 75-81.
[http://dx.doi.org/10.1002/sctm.18-0123] [PMID: 30328686]
[80]
Kopan R. Notch signaling. Cold Spring Harb Perspect Biol 2012; 4(10): 4.
[http://dx.doi.org/10.1101/cshperspect.a011213] [PMID: 23028119]
[81]
Mamaeva V, Niemi R, Beck M, et al. Inhibiting notch activity in breast cancer stem cells by glucose functionalized nanoparticles carrying γ-secretase inhibitors. Mol Ther 2016; 24(5): 926-36.
[http://dx.doi.org/10.1038/mt.2016.42] [PMID: 26916284]
[82]
Kim W-T, Ryu CJ. Cancer stem cell surface markers on normal stem cells. BMB Rep 2017; 50(6): 285-98.
[http://dx.doi.org/10.5483/BMBRep.2017.50.6.039] [PMID: 28270302]
[83]
Harris KS, Kerr BA. Prostate Cancer Stem Cell Markers Drive Progression, Therapeutic Resistance, and Bone Metastasis. Available at:. https://www.hindawi.com/journals/sci/2017/8629234/
[84]
Samad A, Sultana Y, Aqil M. Liposomal drug delivery systems: an update review. Curr Drug Deliv 2007; 4(4): 297-305.
[http://dx.doi.org/10.2174/156720107782151269] [PMID: 17979650]
[85]
Shen Y-A, Li W-H, Chen P-H, He C-L, Chang Y-H, Chuang C-M. Intraperitoneal delivery of a novel liposome-encapsulated paclitaxel redirects metabolic reprogramming and effectively inhibits cancer stem cells in Taxol(®)-resistant ovarian cancer. Am J Transl Res 2015; 7(5): 841-55.
[PMID: 26175846]
[86]
Maeda H. Tumor-selective delivery of macromolecular drugs via the EPR effect: background and future prospects. Bioconjug Chem 2010; 21(5): 797-802.
[http://dx.doi.org/10.1021/bc100070g] [PMID: 20397686]
[87]
Gao N, Bozeman EN, Qian W, et al. Tumor penetrating theranostic nanoparticles for enhancement of targeted and image-guided drug delivery into peritoneal tumors following intraperitoneal delivery. Theranostics 2017; 7(6): 1689-704.
[http://dx.doi.org/10.7150/thno.18125] [PMID: 28529645]
[88]
Cao J, Li C, Wei X, et al. Selective targeting and eradication of LGR5+ cancer stem cells using RSPO-conjugated doxorubicin liposomes. Mol Cancer Ther 2018; 17(7): 1475-85.
[http://dx.doi.org/10.1158/1535-7163.MCT-17-0694] [PMID: 29695632]
[89]
Han N-K, Shin DH, Kim JS, Weon KY, Jang C-Y, Kim J-S. Hyaluronan-conjugated liposomes encapsulating gemcitabine for breast cancer stem cells. Int J Nanomedicine 2016; 11: 1413-25.
[http://dx.doi.org/10.2147/IJN.S95850] [PMID: 27103799]
[90]
Samson AAS, Park S, Kim S-Y, Min D-H, Jeon NL, Song JM. Liposomal co-delivery-based quantitative evaluation of chemosensitivity enhancement in breast cancer stem cells by knockdown of GRP78/CLU. J Liposome Res 2019; 29(1): 44-52.
[http://dx.doi.org/10.1080/08982104.2017.1420081] [PMID: 29262741]
[91]
Rao W, Wang H, Han J, et al. Chitosan-decorated doxorubicin-encapsulated nanoparticle targets and eliminates tumor reinitiating cancer stem-like cells. ACS Nano 2015; 9(6): 5725-40.
[http://dx.doi.org/10.1021/nn506928p] [PMID: 26004286]
[92]
Li Y, Shi S, Ming Y, et al. Specific cancer stem cell-therapy by albumin nanoparticles functionalized with CD44-mediated targeting. J Nanobiotechnology 2018; 16(1): 99.
[http://dx.doi.org/10.1186/s12951-018-0424-4] [PMID: 30501644]
[93]
Naujokat C, Steinhart R. Salinomycin as a drug for targeting human cancer stem cells. BioMed Res Inter 2012; 2012: 17.
[http://dx.doi.org/10.1155/2012/950658]
[94]
Mi Y, Huang Y, Deng J. The enhanced delivery of salinomycin to CD133+ ovarian cancer stem cells through CD133 antibody conjugation with poly(lactic-co-glycolic acid)-poly(ethylene glycol) nanoparticles. Oncol Lett 2018; 15(5): 6611-21.
[http://dx.doi.org/10.3892/ol.2018.8140] [PMID: 29725407]
[95]
Misra SK, De A, Pan D. Targeted delivery of STAT-3 modulator to breast cancer stem-like cells downregulates a series of stemness genes. Mol Cancer Ther 2018; 17(1): 119-29.
[http://dx.doi.org/10.1158/1535-7163.MCT-17-0070] [PMID: 29138265]
[96]
Singh P, Pandit S, Mokkapati VRSS, Garg A, Ravikumar V, Mijakovic I. Gold nanoparticles in diagnostics and therapeutics for human cancer. Int J Mol Sci 2018; 19(7): 19.
[http://dx.doi.org/10.3390/ijms19071979] [PMID: 29986450]
[97]
Cai W, Gao T, Hong H, Sun J. Applications of gold nanoparticles in cancer nanotechnology. Nanotechnol Sci Appl 2008; 1: 17-32.
[http://dx.doi.org/10.2147/NSA.S3788] [PMID: 24198458]
[98]
Iodice C, Cervadoro A, Palange A, et al. Enhancing photothermal cancer therapy by clustering gold nanoparticles into spherical polymeric nanoconstructs. Opt Lasers Eng 2016; 76: 74-81.
[http://dx.doi.org/10.1016/j.optlaseng.2015.04.017]
[99]
Ojea-Jiménez I, Romero FM, Bastús NG, Puntes V. Small gold nanoparticles synthesized with sodium citrate and heavy water: insights into the reaction mechanism. J Phys Chem C 2010; 114: 1800-4.
[http://dx.doi.org/10.1021/jp9091305]
[100]
Zhao Y, Zhao W, Lim YC, Liu T. Salinomycin-loaded gold nanoparticles for treating cancer stem cells by ferroptosis-induced cell death. Mol Pharm 2019; 16(6): 2532-9.
[http://dx.doi.org/10.1021/acs.molpharmaceut.9b00132] [PMID: 31009228]
[101]
Tomuleasa C, Soriţău O, Orza A, et al. Gold nanoparticles conjugated with cisplatin/doxorubicin/capecitabine lower the chemoresistance of hepatocellular carcinoma-derived cancer cells. J Gastrointestin Liver Dis 2012; 21(2): 187-96.
[PMID: 22720309]
[102]
Massagué J, Blain SW, Lo RS. TGFbeta signaling in growth control, cancer, and heritable disorders. Cell 2000; 103(2): 295-309.
[http://dx.doi.org/10.1016/S0092-8674(00)00121-5] [PMID: 11057902]
[103]
Meng H, Zhao Y, Dong J, et al. Two-wave nanotherapy to target the stroma and optimize gemcitabine delivery to a human pancreatic cancer model in mice. ACS Nano 2013; 7(11): 10048-65.
[http://dx.doi.org/10.1021/nn404083m] [PMID: 24143858]
[104]
Tsai Y-S, Chen Y-H, Cheng P-C, et al. TGF-β1 conjugated to gold nanoparticles results in protein conformational changes and attenuates the biological function. Small 2013; 9(12): 2119-28.
[http://dx.doi.org/10.1002/smll.201202755] [PMID: 23335450]
[105]
Peng C-A, Wang C-H. CD133-Positive Cancer Stem-like Cells Ablated by Gold Nanorod-Mediated near-Infrared Laser Treatment Proceedings of the The 4th IEEE International NanoElectronics Conference. 1-2.
[http://dx.doi.org/10.1109/INEC.2011.5991788]
[106]
Kobayashi N, Izumi H, Morimoto Y. Review of toxicity studies of carbon nanotubes. J Occup Health 2017; 59(5): 394-407.
[http://dx.doi.org/10.1539/joh.17-0089-RA] [PMID: 28794394]
[107]
Miao Y, Zhang H, Pan Y, et al. Single-walled carbon nanotube: One specific inhibitor of cancer stem cells in osteosarcoma upon downregulation of the TGFβ1 signaling. Biomaterials 2017; 149: 29-40.
[http://dx.doi.org/10.1016/j.biomaterials.2017.09.032] [PMID: 28988062]
[108]
Burke AR, Singh RN, Carroll DL, et al. The resistance of breast cancer stem cells to conventional hyperthermia and their sensitivity to nanoparticle-mediated photothermal therapy. Biomaterials 2012; 33(10): 2961-70.
[http://dx.doi.org/10.1016/j.biomaterials.2011.12.052] [PMID: 22245557]
[109]
Yao H-J, Zhang Y-G, Sun L, Liu Y. The effect of hyaluronic acid functionalized carbon nanotubes loaded with salinomycin on gastric cancer stem cells. Biomaterials 2014; 35(33): 9208-23.
[http://dx.doi.org/10.1016/j.biomaterials.2014.07.033] [PMID: 25115788]
[110]
Sato-Dahlman M, Miura Y, Huang JL, et al. CD133-targeted oncolytic adenovirus demonstrates anti-tumor effect in colorectal cancer. Oncotarget 2017; 8(44): 76044-56.
[http://dx.doi.org/10.18632/oncotarget.18340] [PMID: 29100290]
[111]
Chaurasiya S, Chen NG, Warner SG. Oncolytic virotherapy versus cancer stem cells: a review of approaches and mechanisms. Cancers (Basel) 2018; 10(4): 10.
[http://dx.doi.org/10.3390/cancers10040124] [PMID: 29671772]
[112]
Zhang X, Meng S, Zhang R, et al. GP73-regulated oncolytic adenoviruses possess potent killing effect on human liver cancer stem-like cells. Oncotarget 2016; 7(20): 29346-58.
[http://dx.doi.org/10.18632/oncotarget.8830] [PMID: 27121064]
[113]
Warner SG, Haddad D, Au J, et al. Oncolytic herpes simplex virus kills stem-like tumor-initiating colon cancer cells. Mol Ther Oncolytics 2016; 3: 16013.
[http://dx.doi.org/10.1038/mto.2016.13] [PMID: 27347556]
[114]
Lapidot T, Sirard C, Vormoor J, et al. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 1994; 367(6464): 645-8.
[http://dx.doi.org/10.1038/367645a0] [PMID: 7509044]
[115]
Askmyr M, Ågerstam H, Hansen N, et al. Selective killing of candidate AML stem cells by antibody targeting of IL1RAP. Blood 2013; 121(18): 3709-13.
[http://dx.doi.org/10.1182/blood-2012-09-458935] [PMID: 23479569]
[116]
Blair A, Sutherland HJ. Primitive acute myeloid leukemia cells with long-term proliferative ability in vitro and in vivo lack surface expression of c-kit (CD117). Exp Hematol 2000; 28(6): 660-71.
[http://dx.doi.org/10.1016/S0301-472X(00)00155-7] [PMID: 10880752]
[117]
Bruserud Ø, Aasebø E, Hernandez-Valladares M, Tsykunova G, Reikvam H. Therapeutic targeting of leukemic stem cells in acute myeloid leukemia - the biological background for possible strategies. Expert Opin Drug Discov 2017; 12(10): 1053-65.
[http://dx.doi.org/10.1080/17460441.2017.1356818] [PMID: 28748730]
[118]
Hosen N, Park CY, Tatsumi N, et al. CD96 is a leukemic stem cell-specific marker in human acute myeloid leukemia. Proc Natl Acad Sci USA 2007; 104(26): 11008-13.
[http://dx.doi.org/10.1073/pnas.0704271104] [PMID: 17576927]
[119]
Jaiswal S, Jamieson CHM, Pang WW, et al. CD47 is upregulated on circulating hematopoietic stem cells and leukemia cells to avoid phagocytosis. Cell 2009; 138(2): 271-85.
[http://dx.doi.org/10.1016/j.cell.2009.05.046] [PMID: 19632178]
[120]
Kikushige Y, Shima T, Takayanagi S, et al. TIM-3 is a promising target to selectively kill acute myeloid leukemia stem cells. Cell Stem Cell 2010; 7(6): 708-17.
[http://dx.doi.org/10.1016/j.stem.2010.11.014] [PMID: 21112565]
[121]
van Rhenen A, van Dongen GAMS, Kelder A, et al. The novel AML stem cell associated antigen CLL-1 aids in discrimination between normal and leukemic stem cells. Blood 2007; 110(7): 2659-66.
[http://dx.doi.org/10.1182/blood-2007-03-083048] [PMID: 17609428]
[122]
Busfield SJ, Biondo M, Wong M, et al. Targeting of acute myeloid leukemia in vitro and in vivo with an anti-CD123 mAb engineered for optimal ADCC. Leukemia 2014; 28(11): 2213-21.
[http://dx.doi.org/10.1038/leu.2014.128] [PMID: 24705479]
[123]
He SZ, Busfield S, Ritchie DS, et al. A Phase 1 study of the safety, pharmacokinetics and anti-leukemic activity of the anti-CD123 monoclonal antibody CSL360 in relapsed, refractory or high-risk acute myeloid leukemia. Leuk Lymphoma 2015; 56(5): 1406-15.
[124]
Frankel AE, Woo JH, Ahn C, et al. Activity of SL-401, a targeted therapy directed to interleukin-3 receptor, in blastic plasmacytoid dendritic cell neoplasm patients. Blood 2014; 124(3): 385-92.
[http://dx.doi.org/10.1182/blood-2014-04-566737] [PMID: 24859366]
[125]
Chichili GR, Huang L, Li H, et al. CD3xCD123 bispecific DART for redirecting host T cells to myelogenous leukemia: preclinical activity and safety in nonhuman primates. Sci Transl Med 2015; 7(289): 82-2.
[126]
Al-Hussaini M, Rettig MP, Ritchey JK, et al. Targeting CD123 in acute myeloid leukemia using a T-cell-directed dual-affinity retargeting platform. Blood 2016; 127(1): 122-31.
[http://dx.doi.org/10.1182/blood-2014-05-575704] [PMID: 26531164]
[127]
Terai K, Bi D, Liu Z, et al. A novel oncolytic herpes capable of cell-specific transcriptional targeting of CD133± cancer cells induces significant tumor regression. Stem Cells 2018; 36(8): 1154-69.
[http://dx.doi.org/10.1002/stem.2835] [PMID: 29658163]
[128]
Mantwill K, Naumann U, Seznec J, et al. YB-1 dependent oncolytic adenovirus efficiently inhibits tumor growth of glioma cancer stem like cells. J Transl Med 2013; 11: 216.
[http://dx.doi.org/10.1186/1479-5876-11-216] [PMID: 24044901]
[129]
Kaid C, Goulart E, Caires-Júnior LC, et al. Zika virus selectively kills aggressive human embryonal cns tumor cells in vitro and in vivo. Cancer Res 2018; 78(12): 3363-74.
[http://dx.doi.org/10.1158/0008-5472.CAN-17-3201] [PMID: 29700002]
[130]
Garcia-Carbonero R, Salazar R, Duran I, et al. Phase 1 study of intravenous administration of the chimeric adenovirus enadenotucirev in patients undergoing primary tumor resection. J Immunother Cancer 2017; 5(1): 71.
[http://dx.doi.org/10.1186/s40425-017-0277-7] [PMID: 28923104]
[131]
Annett S, Robson T. Targeting cancer stem cells in the clinic: Current status and perspectives. Pharmacol Ther 2018; 187: 13-30.
[http://dx.doi.org/10.1016/j.pharmthera.2018.02.001] [PMID: 29421575]
[132]
Mattheolabakis G, Milane L, Singh A, Amiji MM. Hyaluronic acid targeting of CD44 for cancer therapy: from receptor biology to nanomedicine. J Drug Target 2015; 23(7-8): 605-18.
[http://dx.doi.org/10.3109/1061186X.2015.1052072] [PMID: 26453158]
[133]
Weiden J, Tel J, Figdor CG. Synthetic immune niches for cancer immunotherapy. Nat Rev Immunol 2018; 18(3): 212-9.
[http://dx.doi.org/10.1038/nri.2017.89] [PMID: 28853444]
[134]
Hu Z, Ott PA, Wu CJ. Towards personalized, tumour-specific, therapeutic vaccines for cancer. Nat Rev Immunol 2018; 18(3): 168-82.
[http://dx.doi.org/10.1038/nri.2017.131] [PMID: 29226910]
[135]
Zhang H, Chen J. Current status and future directions of cancer immunotherapy. J Cancer 2018; 9(10): 1773-81.
[http://dx.doi.org/10.7150/jca.24577] [PMID: 29805703]
[136]
Leng Z, Xia Q, Chen J, et al. Lgr5+CD44+EpCAM+ strictly defines cancer stem cells in human colorectal cancer. Cell Physiol Biochem 2018; 46(2): 860-72.
[http://dx.doi.org/10.1159/000488743] [PMID: 29627827]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 26
ISSUE: 17
Year: 2020
Published on: 07 June, 2020
Page: [2057 - 2071]
Pages: 15
DOI: 10.2174/1381612826666200406084900
Price: $65

Article Metrics

PDF: 20
HTML: 3