Glyco-functionalised quantum dots and their progress in cancer diagnosis and treatment

Abstract

Despite all major breakthroughs in recent years of research, we are still unsuccessful to effectively diagnose and treat cancer that has express and metastasizes. Thus, the development of a novel approach for cancer detection and treatment is crucial. Recent progress in Glyconanotechnology has allowed the use of glycans and lectins as bio-functional molecules for many biological and biomedical applications. With the known advantages of quantum dots (QDs) and versatility of carbohydrates and lectins, Glyco-functionalised QD is a new prospect in constructing biomedical imaging platform for cancer behaviour study as well as treatment. In this review, we aim to describe the current utilisation of Glyco-functionalised QDs as well as their future prospective to interpret and confront cancer.

Graphical abstract

Keywords

carbohydrate / leptin / glyco-functionalised QD / bioimaging / cancer diagnosis and treatment

References

[1] Bentolila L A, Ebenstein Y, Weiss S. Quantum dots for in vivo small-animal imaging. Journal of Nuclear Medicine: Official Publication, Society of Nuclear Medicine, 2009, 50(4): 493–496

[2] Byers R J, Hitchman E R. Quantum dots brighten biological imaging. Progress in Histochemistry and Cytochemistry, 2011, 45(4): 201–237

[3] Tholouli E, Sweeney E, Barrow E, Clay V, Hoyland J, Byers R. Quantum dots light up pathology. Journal of Pathology, 2008, 216(3): 275–285

[4] He X, Gao J, Gambhir S S, Cheng Z. Near-infrared fluorescent nanoprobes for cancer molecular imaging: Status and challenges. Trends in Molecular Medicine, 2010, 16(12): 574–583

[5] Hilderbrand S A, Weissleder R. Near-infrared fluorescence: Application to in vivo molecular imaging. Current Opinion in Chemical Biology, 2010, 14(1): 71–79

[6] Wang Y, Chen L. Quantum dots, lighting up the research and development of nanomedicine. Nanomedicine (London), 2011, 7(4): 385–402

[7] Varki A, Cummings R D, Esko J D, Freeze H H, Stanley P, Bertozzi C R, Hart G W, Etzler M E. Essentials of Glycobiology. 3rd ed. New York: Cold Spring Harbor Laboratory Press, 2009

[8] Calvaresi E C, Hergenrother P J. Glucose conjugation for the specific targeting and treatment of cancer. Chemical Science (Cambridge), 2013, 4(6): 2319–2333

[9] Kottari N, Chabre Y M, Sharma R, Roy R. Applications of glyconanoparticles as “sweet” glycobiological therapeutics and diagnostics. In: Multifaceted Development and Application of Biopolymers for Biology, Biomedicine and Nanotechnology. Dutta P K, Dutta J, eds. Berlin: Springer International Publishing, 2013

[10] Marradi M, Chiodo F, Garcia I, Penades S. Glyconanoparticles as multifunctional and multimodal carbohydrate systems. Chemical Society Reviews, 2013, 42(11): 4728–4745

[11] Luczkowiak J, Munoz A, Sanchez-Navarro M, Ribeiro-Viana R, Ginieis A, Illescas B M, Martin N, Delgado R, Rojo J. Glycofullerenes inhibit viral infection. Biomacromolecules, 2013, 14(2): 431–437

[12] Ribeiro-Viana R, Sánchez-Navarro M, Luczkowiak J, Koeppe J R, Delgado R, Rojo J, Davis B G. Virus-like glycodendrinanoparticles displaying quasi-equivalent nested polyvalency upon glycoprotein platforms potently block viral infection. Nature Communications, 2012, 3(1): 1303

[13] Fasting C, Schalley C A, Weber M, Seitz O, Hecht S, Koksch B, Dernedde J, Graf C, Knapp E W, Haag R. Multivalency as a chemical organization and action principle. Angewandte Chemie International Edition, 2012, 51(42): 10472–10498

[14] Liu B, Lu X, Ruan H, Cui J, Li H. Synthesis and applications of glyconanoparticles. Current Organic Chemistry, 2016, 20(14): 1502–1511

[15] Reichardt N C, Martin-Lomas M, Penades S. Glyconanotechnology. Chemical Society Reviews, 2013, 42(10): 4358–4376

[16] Sharon N, Lis H. History of lectins: From hemagglutinins to biological recognition molecules. Glycobiology, 2004, 14(11): 53R–62R

[17] Sharon N, Lis H. Lectins as cell recognition molecules. Science, 1989, 246(4927): 227–234

[18] Ashwell G, Harford J. Carbohydrate-specific receptors of the liver. Annual Review of Biochemistry, 1982, 51(1): 531–554

[19] Belardi B, Bertozzi C R. Chemical lectinology: Tools for probing the ligands and dynamics of mammalian lectins in vivo. Chemistry & Biology, 2015, 22(8): 983–993

[20] André S, Kaltner H, Manning J C, Murphy P V, Gabius H J. Lectins: Getting familiar with translators of the sugar code. Molecules (Basel, Switzerland), 2015, 20(2): 1788–1823

[21] Surolia A, Bachhawat B K, Podder S K. Interaction between lectin from ricinus communis and liposomes containing gangliosides. Nature, 1975, 257(5529): 802–804

[22] Häuselmann I, Borsig L. Altered tumor-cell glycosylation promotes metastasis. Frontiers in Oncology, 2014, 4: 28

[23] Friedel M, Andre S, Goldschmidt H, Gabius H J, Schwartz-Albiez R. Galectin-8 enhances adhesion of multiple myeloma cells to vascular endothelium and is an adverse prognostic factor. Glycobiology, 2016, 26(10): 1048–1058

[24] Compagno D, Gentilini L D, Jaworski F M, Pérez I G, Contrufo G, Laderach D J. Glycans and galectins in prostate cancer biology, angiogenesis and metastasis. Glycobiology, 2014, 24(10): 899–906

[25] Vazquez-Levin M H, Marin-Briggiler C I, Caballero J N, Veiga M F. Epithelial and neural cadherin expression in the mammalian reproductive tract and gametes and their participation in fertilization-related events. Developmental Biology, 2015, 401(1): 2–16

[26] Ng K, Ferreyra J, Higginbottom S, Lynch J, Kashyap P, Gopinath S, Naidu N, Choudhury B, Weimer B, Monack D, Sonnenburg J L. Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens. Nature, 2013, 502(7469): 96–99

[27] Becer C R. The glycopolymer code: Synthesis of glycopolymers and multivalent carbohydrate-lectin interactions. Macromolecular Rapid Communications, 2012, 33(9): 742–752

[28] Kazunori M, Miki H, Takayasu I, Yoshinao Y, Kazukiyo K. Self-organized glycoclusters along DNA: Effect of the spatial arrangement of galactoside residues on cooperative lectin recognition. Chemistry (Weinheim an der Bergstrasse, Germany), 2004, 10(2): 352–359

[29] Brus L E. Electron-electron and electron-hole interactions in small semiconductor crystallites: The size dependence of the lowest excited electronic state. Journal of Chemical Physics, 1984, 80(9): 4403–4409

[30] Alivisatos A P, Gu W, Larabell C. Quantum dots as cellular probes. Annual Review of Biomedical Engineering, 2005, 7(1): 55–76

[31] Foote M. The importance of planned dose of chemotherapy on time: Do we need to change our clinical practice? Oncologist, 1998, 3(5): 365–368

[32] Naumov G, Akslen L, Folkman J. Role of angiogenesis in human tumor dormancy: Animal models of the angiogenic switch. Cell Cycle (Georgetown, Tex.), 2006, 5(16): 1779–1787

[33] Frangioni J V. New technologies for human cancer imaging. Journal of Clinical Oncology, 2008, 26(24): 4012–4021

[34] Liu J, Levine A L, Mattoon J S, Yamaguchi M, Lee R J, Pan X, Rosol T J. Nanoparticles as image enhancing agents for ultrasonography. Physics in Medicine and Biology, 2006, 51(9): 2179–2189

[35] Massoud T F, Gambhir S S. Molecular imaging in living subjects: Seeing fundamental biological processes in a new light. Genes & Development, 2003, 17(5): 545–580

[36] Albrecht T, Blomley M J K, Burns P N, Wilson S, Harvey C J, Leen E, Claudon M, Calliada F, Correas J M, LaFortune M, . Improved detection of hepatic metastases with pulse-inversion US during the liver-specific phase of SHU 508A: Multicenter study. Radiology, 2003, 227(2): 361–370

[37] Blomley M J, Cooke J C, Unger E C, Monaghan M J, Cosgrove D O. Microbubble contrast agents: A new era in ultrasound. BMJ (Clinical Research Ed.), 2001, 322(7296): 1222–1225

[38] Cormode D P, Skajaa T, Fayad Z A, Mulder W J. Nanotechnology in medical imaging: Probe design and applications. Arteriosclerosis, Thrombosis, and Vascular Biology, 2009, 29(7): 992–1000

[39] Weissleder R. Scaling down imaging: Molecular mapping of cancer in mice. Nature Reviews. Cancer, 2002, 2(1): 8–11

[40] Caravan P, Ellison J J, McMurry T J, Lauffer R B. Gadolinium(iii) chelates as MRI contrast agents: Structure, dynamics, and applications. Chemical Reviews, 1999, 99(9): 2293–2352

[41] Hoult D I, Phil D. Sensitivity and power deposition in a high-field imaging experiment. Journal of Magnetic Resonance Imaging, 2000, 12(1): 46–67

[42] Jongmin S, Md A R, Kyeong K M, Ho I G, Hee L J, Su L I. Hollow manganese oxide nanoparticles as multifunctional agents for magnetic resonance imaging and drug delivery. Angewandte Chemie International Edition, 2009, 48(2): 321–324

[43] Smith A M, Duan H, Mohs A M, Nie S. Bioconjugated quantum dots for in vivo molecular and cellular imaging. Advanced Drug Delivery Reviews, 2008, 60(11): 1226–1240

[44] Zhang H, Yee D, Wang C. Quantum dots for cancer diagnosis and therapy: Biological and clinical perspectives. Nanomedicine (London), 2008, 3(1): 83–91

[45] Wang H, Li H, Zhang W, Wei L M, Yu H X, Yang P Y. Multiplex profiling of glycoproteins using a novel bead-based lectin array. Proteomics, 2014, 14(1): 78–86

[46] Munkley J, Elliott D J. Hallmarks of glycosylation in cancer. Oncotarget, 2016, 7(23): 35478–35489

[47] Liu X, Nie H, Zhang Y B, Yao Y F, Maitikabili A, Qu Y P, Shi S L, Chen C Y, Li Y. Cell surface-specific N-glycan profiling in breast cancer. PLoS One, 2013, 8(8): 11

[48] Scott E, Munkley J. Glycans as biomarkers in prostate cancer. International Journal of Molecular Sciences, 2019, 20(6): 20

[49] Andrade C G, Cabral Filho P E, Tenório D P L, Santos B S, Beltrão E I C, Fontes A, Carvalho L B. Evaluation of glycophenotype in breast cancer by quantum dot-lectin histochemistry. International Journal of Nanomedicine, 2013, 8: 4623–4629

[50] He D, Wang D, Shi X, Quan W, Xiong R, Yu C, Huang H. Simultaneous fluorescence analysis of the different carbohydrates expressed on living cell surfaces using functionalized quantum dots. RSC Advances, 2017, 7(20): 12374–12381

[51] Cunha C R A, Andrade C G, Pereira M I A, Cabral Filho P E, Carvalho L B Jr, Coelho L C B B, Santos B S, Fontes A, Correia M T S. Quantum dot-cramoll lectin as novel conjugates to glycobiology. Journal of Photochemistry and Photobiology. B, Biology, 2018, 178: 85–91

[52] Akca O, Unak P, Medine E I, Sakarya S, Yurt Kilcar A, Ichedef C, Bekis R, Timur S. Radioiodine labeled CdSe/CdS quantum dots: Lectin targeted dual probes. Radiochimica Acta, 2014, 102(9): 849

[53] Kara A, Ünak P, Selçuki C, Akça Ö, Medine E İ, Sakarya S. PHA-L lectin and carbohydrate relationship: Conjugation with CdSe/CdS nanoparticles, radiolabeling and in vitro affinities on MCF-7 cells. Journal of Radioanalytical and Nuclear Chemistry, 2014, 299(1): 807–813

[54] Santos B, de Farias P, de Menezes F, de Ferreira R, Júnior S, Figueiredo R, de Carvalho L, Beltrão E I C. CdS-Cd(OH)₂ core shell quantum dots functionalized with concanavalin a lectin for recognition of mammary tumors. Physica Status Solidi. C, Current Topics in Solid State Physics, 2006, 3(11): 4017–4022

[55] Ohyanagi T, Nagahori N, Shimawaki K, Hinou H, Yamashita T, Sasaki A, Jin T, Iwanaga T, Kinjo M, Nishimura S I. Importance of sialic acid residues illuminated by live animal imaging using phosphorylcholine self-assembled monolayer-coated quantum dots. Journal of the American Chemical Society, 2011, 133(32): 12507–12517

[56] Bavireddi H, Kikkeri R. Glyco-β-cyclodextrin capped quantum dots: Synthesis, cytotoxicity and optical detection of carbohydrate-protein interactions. Analyst (London), 2012, 137(21): 5123–5127

[57] Shinchi H, Wakao M, Nakagawa S, Mochizuki E, Kuwabata S, Suda Y. Stable sugar-chain-immobilized fluorescent nanoparticles for probing lectin and cells. Chemistry, an Asian Journal, 2012, 7(11): 2678–2682

[58] Shinchi H, Wakao M, Nagata N, Sakamoto M, Mochizuki E, Uematsu T, Kuwabata S, Suda Y. Cadmium-free sugar-chain-immobilized fluorescent nanoparticles containing low-toxicity ZnS-AgInS₂ cores for probing lectin and cells. Bioconjugate Chemistry, 2014, 25(2): 286–295

[59] Zhai Y, Dasog M, Snitynsky R B, Purkait T K, Aghajamali M, Hahn A H, Sturdy C B, Lowary T L, Veinot J G C. Water-soluble photoluminescent D-mannose and L-alanine functionalized silicon nanocrystals and their application to cancer cell imaging. Journal of Materials Chemistry. B, Materials for Biology and Medicine, 2014, 2(47): 8427–8433

[60] Lai C H, Hütter J, Hsu C W, Tanaka H, Varela-Aramburu S, De Cola L, Lepenies B, Seeberger P H. Analysis of carbohydrate-carbohydrate interactions using sugar-functionalized silicon nanoparticles for cell imaging. Nano Letters, 2016, 16(1): 807–811

[61] Hsu C W, Septiadi D, Lai C H, Chen P K, Seeberger P H, De Cola L. Glucose-modified silicon nanoparticles for cellular imaging. ChemPlusChem, 2017, 82(4): 660–667

[62] Cheng F F, Liang G X, Shen Y Y, Rana R K, Zhu J J. N-Acetylglucosamine biofunctionalized CdSeTe quantum dots as fluorescence probe for specific protein recognition. Analyst (London), 2013, 138(2): 666–670

[63] Ahire J H, Chambrier I, Mueller A, Bao Y, Chao Y. Synthesis of D-mannose capped silicon nanoparticles and their interactions with MCF-7 human breast cancerous cells. ACS Applied Materials & Interfaces, 2013, 5(15): 7384–7391

[64] Ahire J H, Behray M, Webster C A, Wang Q, Sherwood V, Saengkrit N, Ruktanonchai U, Woramongkolchai N, Chao Y. Synthesis of carbohydrate capped silicon nanoparticles and their reduced cytotoxicity, in vivo toxicity, and cellular uptake. Advanced Healthcare Materials, 2015, 4(12): 1877–1886

[65] Dalal C, Jana N R. Galactose multivalency effect on the cell uptake mechanism of bioconjugated nanoparticles. Journal of Physical Chemistry C, 2018, 122(44): 25651–25660

[66] Zayed D G, Ebrahim S M, Helmy M W, Khattab S N, Bahey-El-Din M, Fang J Y, Elkhodairy K A, Elzoghby A O. Combining hydrophilic chemotherapy and hydrophobic phytotherapy via tumor-targeted albumin-QDs nano-hybrids: Covalent coupling and phospholipid complexation approaches. Journal of Nanobiotechnology, 2019, 17(1): 19

[67] Yin C, Ying L, Zhang P C, Zhuo R X, Kang E T, Leong K W, Mao H Q. High density of immobilized galactose ligand enhances hepatocyte attachment and function. Journal of Biomedical Materials Research. Part A, 2003, 67A(4): 1093–1104

[68] Hata S, Ishii K. Effect of galactose on binding and endocytosis of asiaioglycoprotein in cultured rat hepatocytes. Annals of Nuclear Medicine, 1998, 12(5): 255–259

[69] Mishra N, Yadav N P, Rai V K, Sinha P, Yadav K S, Jain S, Arora S. Efficient hepatic delivery of drugs: Novel strategies and their significance. BioMed Research International, 2013, 2013: 20

[70] Yousef S, Alsaab H O, Sau S, Iyer A K. Development of asialoglycoprotein receptor directed nanoparticles for selective delivery of curcumin derivative to hepatocellular carcinoma. Heliyon, 2018, 4(12): e01071

[71] Pranatharthiharan S, Patel M D, Malshe V C, Pujari V, Gorakshakar A, Madkaikar M, Ghosh K, Devarajan P V. Asialoglycoprotein receptor targeted delivery of doxorubicin nanoparticles for hepatocellular carcinoma. Drug Delivery, 2017, 24(1): 20–29

[72] Abe M, Manola J B, Oh W K, Parslow D L, George D J, Austin C L, Kantoff P W. Plasma levels of heat shock protein 70 in patients with prostate cancer: A potential biomarker for prostate cancer. Clinical Prostate Cancer, 2004, 3(1): 49–53

[73] Ciocca D R, Calderwood S K. Heat shock proteins in cancer: Diagnostic, prognostic, predictive, and treatment implications. Cell Stress & Chaperones, 2005, 10(2): 86–103

[74] Garrido C, Brunet M, Didelot C, Zermati Y, Schmitt E, Kroemer G. Heat shock proteins 27 and 70: Anti-apoptotic proteins with tumorigenic properties. Cell Cycle (Georgetown, Tex.), 2006, 5(22): 2592–2601

[75] Ahire J H, Wang Q, Coxon P R, Malhotra G, Brydson R, Chen R, Chao Y. Highly luminescent and nontoxic amine-capped nanoparticles from porous silicon: Synthesis and their use in biomedical imaging. ACS Applied Materials & Interfaces, 2012, 4(6): 3285–3292

[76] Zhang L W, Monteiro-Riviere N A. Mechanisms of quantum dot nanoparticle cellular uptake. Toxicological Sciences, 2009, 110(1): 138–155

[77] Yuan F L, Li S H, Fan Z T, Meng X Y, Fan L Z, Yang S H. Shining carbon dots: Synthesis and biomedical and optoelectronic applications. Nano Today, 2016, 11(5): 565–586

[78] Zhang M, Bai L L, Shang W H, Xie W J, Ma H, Fu Y Y, Fang D C, Sun H, Fan L Z, Han M, . Facile synthesis of water-soluble, highly fluorescent graphene quantum dots as a robust biological label for stem cells. Journal of Materials Chemistry, 2012, 22(15): 7461–7467

[79] Fan Z T, Zhou S X, Garcia C, Fan L Z, Zhou J B. pH-responsive fluorescent graphene quantum dots for fluorescence-guided cancer surgery and diagnosis. Nanoscale, 2017, 9(15): 4928–4933

[80] Wang Q, Bao Y, Zhang X, Coxon P R, Jayasooriya U A, Chao Y. Uptake and toxicity studies of poly-acrylic acid functionalized silicon nanoparticles in cultured mammalian cells. Advanced Healthcare Materials, 2012, 1(2): 189–198

[81] Park J H, Gu L, von Maltzahn G, Ruoslahti E, Bhatia S N, Sailor M J. Biodegradable luminescent porous silicon nanoparticles for in vivo applications. Nature Materials, 2009, 8(4): 331–336

[82] Chen H, Cui S, Tu Z, Gu Y, Chi X. In vivo monitoring of organ-selective distribution of cdhgte/SiO₂ nanoparticles in mouse model. Journal of Fluorescence, 2012, 22(2): 699–706

[83] Qu Y, Li W, Zhou Y, Liu X, Zhang L, Wang L, Li Y F, Iida A, Tang Z, Zhao Y, . Full assessment of fate and physiological behavior of quantum dots utilizing caenorhabditis elegans as a model organism. Nano Letters, 2011, 11(8): 3174–3183

[84] Schipper M L, Iyer G, Koh A L, Cheng Z, Ebenstein Y, Aharoni A, Keren S, Bentolila L A, Li J, Rao J, . Particle size, surface coating, and pegylation influence the biodistribution of quantum dots in living mice. Small, 2009, 5(1): 126–134

[85] Choi HS, Liu W, Misra P, Tanaka E, Zimmer J P, Ipe B I, Bawendi M G, Frangioni J V. Renal clearance of quantum dots. Nature Biotechnology, 2007, 25(10): 1165–1170

[86] Zhu Y, Hong H, Xu Z P, Li Z, Cai W. Quantum dot-based nanoprobes for in vivo targeted imaging. Current Molecular Medicine, 2013, 13(10): 1549–1567

[87] Vela-Ramirez J E, Goodman J T, Boggiatto P M, Roychoudhury R, Pohl N L B, Hostetter J M, Wannemuehler M J, Narasimhan B. Safety and biocompatibility of carbohydrate-functionalized polyanhydride nanoparticles. AAPS Journal, 2015, 17(1): 256–267