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Review Article

Biotin conjugates in targeted drug delivery: is it mediated by a biotin transporter, a yet to be identified receptor, or (an)other unknown mechanism(s)?

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Article: 2276663 | Received 08 Aug 2023, Accepted 24 Oct 2023, Published online: 13 Nov 2023

References

  • Bebenek I, Bannister R, Dubinion J, Fortin M, Liu M, Motter AL, Rohde CM, Wrzesinski C. COVID-19 therapeutics and vaccines: a race to save lives. Toxicol Sci. 2022;185(2):119–127.
  • Vargason AM, Anselmo AC, Mitragotri S. The evolution of commercial drug delivery technologies. Nat Biomed Eng. 2021;5(9):951–967.
  • Liu M, Fang X, Yang Y, Wang C. Peptide-enabled targeted delivery systems for therapeutic applications. Front Bioeng Biotechnol. 2021;9:701504.
  • Majumdar S, Siahaan TJ. Peptide-mediated targeted drug delivery. Med Res Rev. 2012;32(3):637–658.
  • Firer MA, Gellerman G. Targeted drug delivery for cancer therapy: the other side of antibodies. J Hematol Oncol. 2012;5(1):70.
  • Tan X, Jia F, Wang P, Zhang K. Nucleic acid-based drug delivery strategies. J Control Release. 2020;323:240–252.
  • Chen K, Zhang Y, Zhu L, Chu H, Shao X, Asakiya C, Huang K, Xu W. Insights into nucleic acid-based self-assembling nanocarriers for targeted drug delivery and controlled drug release. J Control Release. 2022;341:869–891.
  • Russell-Jones G, McTavish K, McEwan J, Rice J, Nowotnik D. Vitamin-mediated targeting as a potential mechanism to increase drug uptake by tumours. J Inorg Biochem. 2004;98(10):1625–1633.
  • Narmani A, Rezvani M, Farhood B, Darkhor P, Mohammadnejad J, Amini B, Refahi S, Abdi Goushbolagh N. Folic acid functionalized nanoparticles as pharmaceutical carriers in drug delivery systems. Drug Dev Res. 2019;80(4):404–424.
  • Xiao W, Fu Q, Zhao Y, Zhang L, Yue Q, Hai L, Guo L, Wu Y. Ascorbic acid-modified brain-specific liposomes drug delivery system with "lock-in" function. Chem Phys Lipids. 2019;224:104727.
  • Clardy SM, Allis DG, Fairchild TJ, Doyle RP. Vitamin B12 in drug delivery: breaking through the barriers to a B12 bioconjugate pharmaceutical. Expert Opin Drug Deliv. 2011;8(1):127–140.
  • Chahibi Y, Akyildiz IF, Song OS. Antibody-based molecular communication for targeted drug delivery systems. Annu Int Conf IEEE Eng Med Biol Soc. 2014;2014:5707–5710.
  • Awwad S, Angkawinitwong U. Overview of antibody drug delivery. Pharmaceutics. 2018;10(3):83.
  • Gu L, Duan Z, Li X, Li X, Li Y, Li X, Xu G, Gao P, Zhang H, Gu Z, et al. Enzyme-triggered deep tumor penetration of a dual-drug nanomedicine enables an enhanced cancer combination therapy. Bioact Mater. 2023;26:102–115.
  • Mitchell MJ, Billingsley MM, Haley RM, Wechsler ME, Peppas NA, Langer R. Engineering precision nanoparticles for drug delivery. Nat Rev Drug Discov. 2021;20(2):101–124.
  • Battogtokh G, Choi YS, Kang DS, Park SJ, Shim MS, Huh KM, Cho YY, Lee JY, Lee HS, Kang HC. Mitochondria-targeting drug conjugates for cytotoxic, anti-oxidizing and sensing purposes: current strategies and future perspectives. Acta Pharm Sin B. 2018;8(6):862–880.
  • Zheng Y, Ji X, Yu B, Ji K, Gallo D, Csizmadia E, Zhu M, Choudhury MR, De La Cruz LKC, Chittavong V, et al. Enrichment-triggered prodrug activation demonstrated through mitochondria-targeted delivery of doxorubicin and carbon monoxide. Nat Chem. 2018;10(7):787–794.
  • Yue Y, Huo F, Lee S, Yin C, Yoon J. A review: the trend of progress about pH probes in cell application in recent years. Analyst. 2016;142(1):30–41.
  • Ambiliraj DB, Francis B, Reddy MLP. Lysosome-targeting luminescent lanthanide complexes: from molecular design to bioimaging. Dalton Trans. 2022;51(20):7748–7762.
  • Gregor A, Lind M, Newman H, Grant R, Hadley DM, Barton T, Osborn C. Phase II studies of RMP-7 and carboplatin in the treatment of recurrent high grade glioma. RMP-7 European Study Group. J Neurooncol. 1999;44(2):137–145.
  • Liu LB, Xue YX, Liu YH. Bradykinin increases the permeability of the blood–tumor barrier by the caveolae-mediated transcellular pathway. J Neurooncol. 2010;99(2):187–194.
  • Hampl R, Bičíková M, Sosvorová L. Hormones and the blood–brain barrier. Horm Mol Biol Clin Investig. 2015;21(3):159–164.
  • Yang W, Gao S, Gao X, Karnati VV, Ni W, Wang B, Hooks WB, Carson J, Weston B. Diboronic acids as fluorescent probes for cells expressing sialyl Lewis X. Bioorg Med Chem Lett. 2002;12(16):2175–2177.
  • Gao X, Zhu M, Fan H, Yang W, Ni W, Karnati VV, Gao S, Carson J, Weston B, Wang B. A fluorescent bisboronic acid compound that selectively labels cells expressing oligosaccharide Lewis X. Bioorg Med Chem Lett. 2015;25(12):2501–2504.
  • Chu Y, Wang D, Wang K, Liu ZL, Weston B, Wang B. Fluorescent conjugate of sLe(x)-selective bisboronic acid for imaging application. Bioorg Med Chem Lett. 2013;23(23):6307–6309.
  • Yang W, Fan H, Gao X, Gao S, Karnati VV, Ni W, Hooks WB, Carson J, Weston B, Wang B. The first fluorescent diboronic acid sensor specific for hepatocellular carcinoma cells expressing sialyl Lewis X. Chem Biol. 2004;11(4):439–448.
  • Li S, Yu B, Wang J, Zheng Y, Zhang H, Walker MJ, Yuan Z, Zhu H, Zhang J, Wang PG, et al. Biomarker-based metabolic labeling for redirected and enhanced immune response. ACS Chem Biol. 2018;13(6):1686–1694.
  • Jiang J, Wang W, Sane DC, Wang B. Synthesis of RGD analogs as potential vectors for targeted drug delivery. Bioorg Chem. 2001;29(6):357–379.
  • Berreau LM. Targeted delivery of carbon monoxide. In: Wang B, Otterbein LE, editors. Carbon monoxide in drug discovery: basics, pharmacology, and therapeutic potential. Hoboken (NJ): John Wiley and Sons; 2022. p. 259–285. ISBN: 9781119783404.
  • Das SK, Ghilzai NMK, Scolaro KL. Drug delivery: principles and applications. Am J Pharm Educ. 2006;70(4):94.
  • Ren WX, Han J, Uhm S, Jang YJ, Kang C, Kim JH, Kim JS. Recent development of biotin conjugation in biological imaging, sensing, and target delivery. Chem Commun. 2015;51(52):10403–10418.
  • Vadlapudi AD, Vadlapatla RK, Mitra AK. Sodium dependent multivitamin transporter (SMVT): a potential target for drug delivery. Curr Drug Targets. 2012;13(7):994–1003.
  • Luo S, Kansara VS, Zhu X, Mandava NK, Pal D, Mitra AK. Functional characterization of sodium-dependent multivitamin transporter in MDCK-MDR1 cells and its utilization as a target for drug delivery. Mol Pharm. 2006;3(3):329–339.
  • McMahon RJ. Biotin in metabolism and molecular biology. Annu Rev Nutr. 2002;22(1):221–239.
  • León-Del-Río A. Biotin in metabolism, gene expression, and human disease. J Inherit Metab Dis. 2019;42(4):647–654.
  • Zempleni J, Wijeratne SS, Hassan YI. Biotin. Biofactors. 2009;35(1):36–46.
  • Tong L. Structure and function of biotin-dependent carboxylases. Cell Mol Life Sci. 2013;70(5):863–891.
  • Dakshinamurti K, Chalifour LE. The biotin requirement of HeLa cells. J Cell Physiol. 1981;107(3):427–438.
  • Zempleni J, Helm RM, Mock DM. In vivo biotin supplementation at a pharmacologic dose decreases proliferation rates of human peripheral blood mononuclear cells and cytokine release. J Nutr. 2001;131(5):1479–1484.
  • Luong JHT, Vashist SK. Chemistry of biotin–streptavidin and the growing concern of an emerging biotin interference in clinical immunoassays. ACS Omega. 2020;5(1):10–18.
  • Crisp SE, Griffin JB, White BR, Toombs CF, Camporeale G, Said HM, Zempleni J. Biotin supply affects rates of cell proliferation, biotinylation of carboxylases and histones, and expression of the gene encoding the sodium-dependent multivitamin transporter in JAr choriocarcinoma cells. Eur J Nutr. 2004;43(1):23–31.
  • Schenker S, Hu ZQ, Johnson RF, Yang Y, Frosto T, Elliott BD, Henderson GI, Mock DM. Human placental biotin transport: normal characteristics and effect of ethanol. Alcohol Clin Exp Res. 1993;17(3):566–575.
  • Weiner D, Wolf B. Biotin uptake, utilization, and efflux in normal and biotin-deficient rat hepatocytes. Biochem Med Metab Biol. 1991;46(3):344–363.
  • Mock DM, Malik MI. Distribution of biotin in human plasma: most of the biotin is not bound to protein. Am J Clin Nutr. 1992;56(2):427–432.
  • Maiti S, Paira P. Biotin conjugated organic molecules and proteins for cancer therapy: a review. Eur J Med Chem. 2018;145:206–223.
  • Chen S, Zhao X, Chen J, Chen J, Kuznetsova L, Wong SS, Ojima I. Mechanism-based tumor-targeting drug delivery system. Validation of efficient vitamin receptor-mediated endocytosis and drug release. Bioconjug Chem. 2010;21(5):979–987.
  • Horn MA, Heinstein PF, Low PS. Biotin-mediated delivery of exogenous macromolecules into soybean cells. Plant Physiol. 1990;93(4):1492–1496.
  • Strydom S, Van Jaarsveld P, Van Helden E, Ariatti M, Hawtrey A. Studies on the transfer of DNA into cells through use of avidin–polylysine conjugates complexed to biotinylated transferrin and DNA. J Drug Target. 1993;1(2):165–174.
  • Sakahara H, Saga T. Avidin–biotin system for delivery of diagnostic agents. Adv Drug Deliv Rev. 1999;37(1–3):89–101.
  • Lindgren M, Gallet X, Soomets U, Hällbrink M, Bråkenhielm E, Pooga M, Brasseur R, Langel U. Translocation properties of novel cell penetrating transportan and penetratin analogues. Bioconjug Chem. 2000;11(5):619–626.
  • Lee HJ, Pardridge WM. Pharmacokinetics and delivery of tat and tat–protein conjugates to tissues in vivo. Bioconjug Chem. 2001;12(6):995–999.
  • Chen LL, Frankel AD, Harder JL, Fawell S, Barsoum J, Pepinsky B. Increased cellular uptake of the human immunodeficiency virus-1 Tat protein after modification with biotin. Anal Biochem. 1995;227(1):168–175.
  • Ferraretto A, Sonnino S, Soria MR, Masserini M. Characterization of biotinylated liposomes sensitive to temperature and pH: new tools for anti-cancer drug delivery. Chem Phys Lipids. 1996;82(2):133–139.
  • Loughrey HC, Ferraretto A, Cannon AM, Acerbis G, Sudati F, Bottiroli G, Masserini M, Soria MR. Characterisation of biotinylated liposomes for in vivo targeting applications. FEBS Lett. 1993;332(1–2):183–188.
  • Soria MR, Loughrey H, Ferraretto A, Cannon A-M, Acerbis G, Sudati F, Bottiroli G, Masserini M. Targeting applications of biotinylated liposomes. J Liposome Res. 1993;3(3):543–549.
  • Urdal DL, Hakomori S. Tumor-associated ganglio-N-triosylceramide. Target for antibody-dependent, avidin-mediated drug killing of tumor cells. J Biol Chem. 1980;255(21):10509–10516.
  • Bayer EA, Rivnay B, Skutelsky E. On the mode of liposome-cell interactions. Biotin-conjugated lipids as ultrastructural probes. Biochim Biophys Acta. 1979;550(3):464–473.
  • Choudhury I, Wang J, Rabson AB, Stein S, Pooyan S, Stein S, Leibowitz MJ. Inhibition of HIV-1 replication by a Tat RNA-binding domain peptide analog. J Acquir Immune Defic Syndr Hum Retrovirol. 1998;17(2):104–111.
  • Ramanathan S, Pooyan S, Stein S, Prasad PD, Wang J, Leibowitz MJ, Ganapathy V, Sinko PJ. Targeting the sodium-dependent multivitamin transporter (SMVT) for improving the oral absorption properties of a retro-inverso Tat nonapeptide. Pharm Res. 2001;18(7):950–956.
  • Yang W, Cheng Y, Xu T, Wang X, Wen LP. Targeting cancer cells with biotin–dendrimer conjugates. Eur J Med Chem. 2009;44(2):862–868.
  • Lu R, Zhou L, Yue Q, Liu Q, Cai X, Xiao W, Hai L, Guo L, Wu Y. Liposomes modified with double-branched biotin: a novel and effective way to promote breast cancer targeting. Bioorg Med Chem. 2019;27(14):3115–3127.
  • Nosrati H, Barzegari P, Danafar H, Kheiri Manjili H. Biotin-functionalized copolymeric PEG-PCL micelles for in vivo tumour-targeted delivery of artemisinin. Artif Cells Nanomed Biotechnol. 2019;47(1):104–114.
  • Lee Y, Lee S, Jon S. Biotinylated bilirubin nanoparticles as a tumor microenvironment-responsive drug delivery system for targeted cancer therapy. Adv Sci. 2018;5(6):1800017.
  • Kim SY, Cho SH, Lee YM, Chu L-Y. Biotin-conjugated block copolymeric nanoparticles as tumor-targeted drug delivery systems. Macromol Res. 2007;15(7):646–655.
  • Beckett D. Biotin sensing: universal influence of biotin status on transcription. Annu Rev Genet. 2007;41(1):443–464.
  • Gravel RA, Narang MA. Molecular genetics of biotin metabolism: old vitamin, new science. J Nutr Biochem. 2005;16(7):428–431.
  • Kuroishi T. Regulation of immunological and inflammatory functions by biotin. Can J Physiol Pharmacol. 2015;93(12):1091–1096.
  • León-Del-Río A. Biotin-dependent regulation of gene expression in human cells. J Nutr Biochem. 2005;16(7):432–434.
  • Lesch HP, Kaikkonen MU, Pikkarainen JT, Ylä-Herttuala S. Avidin–biotin technology in targeted therapy. Expert Opin Drug Deliv. 2010;7(5):551–564.
  • Quick M, Shi L. The sodium/multivitamin transporter: a multipotent system with therapeutic implications. Vitam Horm. 2015;98:63–100.
  • Riveron-Negrete L, Fernandez-Mejia C. Pharmacological effects of biotin in animals. Mini Rev Med Chem. 2017;17(6):529–540.
  • Said HM. Cell and molecular aspects of human intestinal biotin absorption. J Nutr. 2009;139(1):158–162.
  • Said HM. Biotin: biochemical, physiological and clinical aspects. Subcell Biochem. 2012;56:1–19.
  • Sirithanakorn C, Cronan JE. Biotin, a universal and essential cofactor: synthesis, ligation and regulation. FEMS Microbiol Rev. 2021;45(4):fuab003.
  • Zempleni J, Teixeira DC, Kuroishi T, Cordonier EL, Baier S. Biotin requirements for DNA damage prevention. Mutat Res. 2012;733(1–2):58–60.
  • Zempleni J. Uptake, localization, and noncarboxylase roles of biotin. Annu Rev Nutr. 2005;25(1):175–196.
  • Zempleni J, Kuroishi T. Biotin. Adv Nutr. 2012;3(2):213–214.
  • Mock DM. Biotin: from nutrition to therapeutics. J Nutr. 2017;147(8):1487–1492.
  • Fam KT, Collot M, Klymchenko AS. Probing biotin receptors in cancer cells with rationally designed fluorogenic squaraine dimers. Chem Sci. 2020;11(31):8240–8248.
  • Bhuniya S, Maiti S, Kim EJ, Lee H, Sessler JL, Hong KS, Kim JS. An activatable theranostic for targeted cancer therapy and imaging. Angew Chem Int Ed Engl. 2014;53(17):4469–4474.
  • Li K, Dong W, Liu Q, Lv G, Xie M, Sun X, Qiu L, Lin J. A biotin receptor-targeted silicon(IV) phthalocyanine for in vivo tumor imaging and photodynamic therapy. J Photochem Photobiol B. 2019;190:1–7.
  • Bongarzone S, Sementa T, Dunn J, Bordoloi J, Sunassee K, Blower PJ, Gee A. Imaging biotin trafficking in vivo with positron emission tomography. J Med Chem. 2020;63(15):8265–8275.
  • Cetin M, Youn YS, Capan Y, Lee KC. Preparation and characterization of salmon calcitonin–biotin conjugates. AAPS PharmSciTech. 2008;9(4):1191–1197.
  • Doerflinger A, Quang NN, Gravel E, Pinna G, Vandamme M, Ducongé F, Doris E. Biotin-functionalized targeted polydiacetylene micelles. Chem Commun. 2018;54(29):3613–3616.
  • Vinothini K, Rajendran NK, Munusamy MA, Alarfaj AA, Rajan M. Development of biotin molecule targeted cancer cell drug delivery of doxorubicin loaded κ-carrageenan grafted graphene oxide nanocarrier. Mater Sci Eng C Mater Biol Appl. 2019;100:676–687.
  • Kunjiappan S, Pavadai P, Vellaichamy S, Ram Kumar Pandian S, Ravishankar V, Palanisamy P, Govindaraj S, Srinivasan G, Premanand A, Sankaranarayanan M, et al. Surface receptor-mediated targeted drug delivery systems for enhanced cancer treatment: a state-of-the-art review. Drug Dev Res. 2021;82(3):309–340.
  • Del Alamo D, Sala D, McHaourab HS, Meiler J. Sampling alternative conformational states of transporters and receptors with AlphaFold2. Elife. 2022;11:e75751.
  • Ma TY, Dyer DL, Said HM. Human intestinal cell line Caco-2: a useful model for studying cellular and molecular regulation of biotin uptake. Biochim Biophys Acta. 1994;1189(1):81–88.
  • Vadlapudi AD, Vadlapatla RK, Pal D, Mitra AK. Biotin uptake by T47D breast cancer cells: functional and molecular evidence of sodium-dependent multivitamin transporter (SMVT). Int J Pharm. 2013;441(1–2):535–543.
  • Janoria KG, Hariharan S, Paturi D, Pal D, Mitra AK. Biotin uptake by rabbit corneal epithelial cells: role of sodium-dependent multivitamin transporter (SMVT). Curr Eye Res. 2006;31(10):797–809.
  • Said HM, Redha R, Nylander W. A carrier-mediated, Na+ gradient-dependent transport for biotin in human intestinal brush-border membrane vesicles. Am J Physiol. 1987;253(5 Pt 1):G631–G636.
  • Said HM, Ortiz A, McCloud E, Dyer D, Moyer MP, Rubin S. Biotin uptake by human colonic epithelial NCM460 cells: a carrier-mediated process shared with pantothenic acid. Am J Physiol. 1998;275(5):C1365–C1371.
  • Kansara V, Luo S, Balasubrahmanyam B, Pal D, Mitra AK. Biotin uptake and cellular translocation in human derived retinoblastoma cell line (Y-79): a role of hSMVT system. Int J Pharm. 2006;312(1–2):43–52.
  • Subedi D, Ashley AK, Chavez MV, Smirnov SN. Mixed silane monolayers reveal the disparity of biotin and folate in targeting cancer cells. ACS Appl Nano Mater. 2020;3(6):5372–5380.
  • Pandeya A, Yang L, Alegun O, Karunasena C, Risko C, Li Z, Wei Y. Biotinylation as a tool to enhance the uptake of small molecules in Gram-negative bacteria. PLOS One. 2021;16(11):e0260023.
  • Vijay N, Morris ME. Role of monocarboxylate transporters in drug delivery to the brain. Curr Pharm Des. 2014;20(10):1487–1498.
  • Daberkow RL, White BR, Cederberg RA, Griffin JB, Zempleni J. Monocarboxylate transporter 1 mediates biotin uptake in human peripheral blood mononuclear cells. J Nutr. 2003;133(9):2703–2706.
  • Grafe F, Wohlrab W, Neubert RH, Brandsch M. Transport of biotin in human keratinocytes. J Invest Dermatol. 2003;120(3):428–433.
  • Holling T, Nampoothiri S, Tarhan B, Schneeberger PE, Vinayan KP, Yesodharan D, Roy AG, Radhakrishnan P, Alawi M, Rhodes L, et al. Novel biallelic variants expand the SLC5A6-related phenotypic spectrum. Eur J Hum Genet. 2022;30(4):439–449.
  • Wang H, Huang W, Fei YJ, Xia H, Yang-Feng TL, Leibach FH, Devoe LD, Ganapathy V, Prasad PD. Human placental Na+-dependent multivitamin transporter. Cloning, functional expression, gene structure, and chromosomal localization. J Biol Chem. 1999;274(21):14875–14883.
  • Chatterjee NS, Kumar CK, Ortiz A, Rubin SA, Said HM. Molecular mechanism of the intestinal biotin transport process. Am J Physiol. 1999;277(4):C605–C613.
  • Prasad PD, Wang H, Kekuda R, Fujita T, Fei YJ, Devoe LD, Leibach FH, Ganapathy V. Cloning and functional expression of a cDNA encoding a mammalian sodium-dependent vitamin transporter mediating the uptake of pantothenate, biotin, and lipoate. J Biol Chem. 1998;273(13):7501–7506.
  • Chen H, Xie LQ, Qin J, Jia Y, Cai X, Nan W, Yang W, Lv F, Zhang QQ. Surface modification of PLGA nanoparticles with biotinylated chitosan for the sustained in vitro release and the enhanced cytotoxicity of epirubicin. Colloids Surf B Biointerfaces. 2016;138:1–9.
  • Uchida Y, Ito K, Ohtsuki S, Kubo Y, Suzuki T, Terasaki T. Major involvement of Na+-dependent multivitamin transporter (SLC5A6/SMVT) in uptake of biotin and pantothenic acid by human brain capillary endothelial cells. J Neurochem. 2015;134(1):97–112.
  • Bildstein L, Dubernet C, Couvreur P. Prodrug-based intracellular delivery of anticancer agents. Adv Drug Deliv Rev. 2011;63(1–2):3–23.
  • Halestrap AP. The monocarboxylate transporter family – structure and functional characterization. IUBMB Life. 2012;64(1):1–9.
  • Halestrap AP, Price NT. The proton-linked monocarboxylate transporter (MCT) family: structure, function and regulation. Biochem J. 1999;343(Pt 2):281–299.
  • Jackson VN, Halestrap AP. The kinetics, substrate, and inhibitor specificity of the monocarboxylate (lactate) transporter of rat liver cells determined using the fluorescent intracellular pH indicator, 2′,7′-bis(carboxyethyl)-5(6)-carboxyfluorescein. J Biol Chem. 1996;271(2):861–868.
  • Zempleni J, Mock DM. Uptake and metabolism of biotin by human peripheral blood mononuclear cells. Am J Physiol. 1998;275(2):C382–C388.
  • Sudo K. Enzyme kinetics for enzyme immunoassay. Nihon Rinsho. 1995;53(9):2134–2139.
  • Su D, Kosciuk T, Yang M, Price IR, Lin H. Binding affinity determines substrate specificity and enables discovery of substrates for N-myristoyltransferases. ACS Catal. 2021;11(24):14877–14883.
  • Schultz SG. Membrane transport, general concepts. In: Lennarz WJ, Lane MD, editors. Encyclopedia of biological chemistry. 2nd ed. Academic Press; 2013. p. 49–51.
  • Stillwell W. Membrane transport. In: An introduction to biological membranes; 2016. p. 423–451.
  • de Carvalho FD, Quick M. Surprising substrate versatility in SLC5A6: Na+-coupled I– transport by the human Na+/multivitamin transporter (hSMVT). J Biol Chem. 2011;286(1):131–137.
  • Wang W, Ackermann D, Mehlich AM, König S. False labelling due to quenching failure of N-hydroxy-succinimide-ester-coupled dyes. Proteomics. 2010;10(7):1525–1529.
  • Russell-Jones G, McTavish K, McEwan J. Preliminary studies on the selective accumulation of vitamin-targeted polymers within tumors. J Drug Target. 2011;19(2):133–139.
  • Patel M, Vadlapatla RK, Shah S, Mitra AK. Molecular expression and functional activity of sodium dependent multivitamin transporter in human prostate cancer cells. Int J Pharm. 2012;436(1–2):324–331.
  • Baur B, Baumgartner ER. Biotin and biocytin uptake into cultured primary calf brain microvessel endothelial cells of the blood–brain barrier. Brain Res. 2000;858(2):348–355.
  • Chirapu SR, Rotter CJ, Miller EL, Varma MV, Dow RL, Finn MG. High specificity in response of the sodium-dependent multivitamin transporter to derivatives of pantothenic acid. Curr Top Med Chem. 2013;13(7):837–842.
  • Saha S, Majumdar R, Hussain A, Dighe RR, Chakravarty AR. Biotin-conjugated tumour-targeting photocytotoxic iron(III) complexes. Philos Trans A Math Phys Eng Sci. 2013;371(1995):20120190.
  • Jung D, Maiti S, Lee JH, Lee JH, Kim JS. Rational design of biotin–disulfide–coumarin conjugates: a cancer targeted thiol probe and bioimaging. Chem Commun. 2014;50(23):3044–3047.
  • McConnell DB. Biotin’s lessons in drug design. J Med Chem. 2021;64(22):16319–16327.
  • Maiti S, Park N, Han JH, Jeon HM, Lee JH, Bhuniya S, Kang C, Kim JS. Gemcitabine–coumarin–biotin conjugates: a target specific theranostic anticancer prodrug. J Am Chem Soc. 2013;135(11):4567–4572.
  • Hu W, Fang L, Hua W, Gou S. Biotin–Pt (IV)–indomethacin hybrid: a targeting anticancer prodrug providing enhanced cancer cellular uptake and reversing cisplatin resistance. J Inorg Biochem. 2017;175:47–57.
  • Zhang X, Qi J, Lu Y, He W, Li X, Wu W. Biotinylated liposomes as potential carriers for the oral delivery of insulin. Nanomedicine. 2014;10(1):167–176.
  • Zhu W, Song Z, Wei P, Meng N, Teng F, Yang F, Liu N, Feng R. Y-shaped biotin-conjugated poly (ethylene glycol)–poly (epsilon-caprolactone) copolymer for the targeted delivery of curcumin. J Colloid Interface Sci. 2015;443:1–7.
  • Shi JF, Wu P, Jiang ZH, Wei XY. Synthesis and tumor cell growth inhibitory activity of biotinylated annonaceous acetogenins. Eur J Med Chem. 2014;71:219–228.
  • Heo DN, Yang DH, Moon HJ, Lee JB, Bae MS, Lee SC, Lee WJ, Sun IC, Kwon IK. Gold nanoparticles surface-functionalized with paclitaxel drug and biotin receptor as theranostic agents for cancer therapy. Biomaterials. 2012;33(3):856–866.
  • Huang GN. Biotinylation of cell surface proteins. Bio Protoc. 2012;2(9):e170.
  • Li Y, Wang Y, Mao J, Yao Y, Wang K, Qiao Q, Fang Z, Ye M. Sensitive profiling of cell surface proteome by using an optimized biotinylation method. J Proteomics. 2019;196:33–41.
  • Li M, Peng F, Wang G, Liang X, Shao M, Chen Z, Chen Y. Coupling of cell surface biotinylation and SILAC-based quantitative proteomics identified myoferlin as a potential therapeutic target for nasopharyngeal carcinoma metastasis. Front Cell Dev Biol. 2021;9:621810.
  • Hörmann K, Stukalov A, Müller AC, Heinz LX, Superti-Furga G, Colinge J, Bennett KL. A surface biotinylation strategy for reproducible plasma membrane protein purification and tracking of genetic and drug-induced alterations. J Proteome Res. 2016;15(2):647–658.
  • Kirkemo LL, Elledge SK, Yang J, Byrnes JR, Glasgow JE, Blelloch R, Wells JA. Cell-surface tethered promiscuous biotinylators enable comparative small-scale surface proteomic analysis of human extracellular vesicles and cells. Elife. 2022;11:e73982.
  • Hong M, Xu W, Yoshida T, Tanaka K, Wolff DJ, Zhou F, Inouye M, You G. Human organic anion transporter hOAT1 forms homooligomers. J Biol Chem. 2005;280(37):32285–32290.
  • Niinae T, Ishihama Y, Imami K. Biotinylation-based proximity labelling proteomics: basics, applications and technical considerations. J Biochem. 2021;170(5):569–576.
  • Liu G, Choi MH, Ma H, Guo X, Lo PC, Kim J, Zhang L. Bioorthogonal conjugation-assisted purification method for profiling cell surface proteome. Anal Chem. 2022;94(3):1901–1909.
  • Kähne T, Ansorge S. Non-radioactive labelling and immunoprecipitation analysis of leukocyte surface proteins using different methods of protein biotinylation. J Immunol Methods. 1994;168(2):209–218.
  • Karhemo PR, Ravela S, Laakso M, Ritamo I, Tatti O, Mäkinen S, Goodison S, Stenman UH, Hölttä E, Hautaniemi S, et al. An optimized isolation of biotinylated cell surface proteins reveals novel players in cancer metastasis. J Proteomics. 2012;77:87–100.
  • Langó T, Kuffa K, Tóth G, Turiák L, Drahos L, Tusnády GE. Comprehensive discovery of the accessible primary amino group-containing segments from cell surface proteins by fine-tuning a high-throughput biotinylation method. Int J Mol Sci. 2022;24(1):273.
  • Alandejani SA, Malaczynska J, Bluth MJ, Das B, Norin AJ. Moesin: a novel receptor on NK lymphocytes binds to TOMM40 on K562 leukemia cells initiating cytolysis. Hum Immunol. 2022;83(5):418–427.
  • Kumar V, Nguyen TB, Tóth B, Juhasz V, Unadkat JD. Optimization and application of a biotinylation method for quantification of plasma membrane expression of transporters in cells. AAPS J. 2017;19(5):1377–1386.
  • Belleannee C, Belghazi M, Labas V, Teixeira-Gomes AP, Gatti JL, Dacheux JL, Dacheux F. Purification and identification of sperm surface proteins and changes during epididymal maturation. Proteomics. 2011;11(10):1952–1964.
  • Prasad PD, Ganapathy V. Keratinocytes join forces with immune cells in the prosecution of SMVT as a "false" biotin transporter. J Invest Dermatol. 2003;120(3):xi–xii.
  • Li H, Bruce G, Childerhouse N, Keegan G, Mantovani G, Stolnik S. Biotin receptor-mediated intracellular delivery of synthetic polypeptide–protein complexes. J Control Release. 2023;357:333–341.
  • Mosquera J, García I, Liz-Marzán LM. Cellular uptake of nanoparticles versus small molecules: a matter of size. Acc Chem Res. 2018;51(9):2305–2313.
  • Sun XY, Gan QZ, Ouyang JM. Size-dependent cellular uptake mechanism and cytotoxicity toward calcium oxalate on Vero cells. Sci Rep. 2017;7(1):41949.
  • Matsson P, Kihlberg J. How big is too big for cell permeability? J Med Chem. 2017;60(5):1662–1664.
  • Montizaan D, Yang K, Reker-Smit C, Salvati A. Comparison of the uptake mechanisms of zwitterionic and negatively charged liposomes by HeLa cells. Nanomedicine. 2020;30:102300.
  • Rennick JJ, Johnston APR, Parton RG. Key principles and methods for studying the endocytosis of biological and nanoparticle therapeutics. Nat Nanotechnol. 2021;16(3):266–276.
  • Bitsikas V, Corrêa IR Jr., Nichols BJ. Clathrin-independent pathways do not contribute significantly to endocytic flux. Elife. 2014;3:e03970.
  • Kaksonen M, Roux A. Mechanisms of clathrin-mediated endocytosis. Nat Rev Mol Cell Biol. 2018;19(5):313–326.
  • Bobulescu IA, Di Sole F, Moe OW. Na+/H+ exchangers: physiology and link to hypertension and organ ischemia. Curr Opin Nephrol Hypertens. 2005;14(5):485–494.
  • Schnitzer JE, Oh P, Pinney E, Allard J. Filipin-sensitive caveolae-mediated transport in endothelium: reduced transcytosis, scavenger endocytosis, and capillary permeability of select macromolecules. J Cell Biol. 1994;127(5):1217–1232.
  • Schwartz AL. Receptor cell biology: receptor-mediated endocytosis. Pediatr Res. 1995;38(6):835–843.
  • Shen Z, Ye H, Kröger M, Li Y. Aggregation of polyethylene glycol polymers suppresses receptor-mediated endocytosis of PEGylated liposomes. Nanoscale. 2018;10(9):4545–4560.
  • Gao H, Shi W, Freund LB. Mechanics of receptor-mediated endocytosis. Proc Natl Acad Sci U S A. 2005;102(27):9469–9474.
  • Liu AP, Aguet F, Danuser G, Schmid SL. Local clustering of transferrin receptors promotes clathrin-coated pit initiation. J Cell Biol. 2010;191(7):1381–1393.
  • Ramanathan S, Qiu B, Pooyan S, Zhang G, Stein S, Leibowitz MJ, Sinko PJ. Targeted PEG-based bioconjugates enhance the cellular uptake and transport of a HIV-1 TAT nonapeptide. J Control Release. 2001;77(3):199–212.
  • Li M, Yu Y. Innate immune receptor clustering and its role in immune regulation. J Cell Sci. 2021;134(4):134.
  • Duke T, Graham I. Equilibrium mechanisms of receptor clustering. Prog Biophys Mol Biol. 2009;100(1–3):18–24.
  • Caré BR, Soula HA. Impact of receptor clustering on ligand binding. BMC Syst Biol. 2011;5(1):48.
  • Rompicharla SVK, Kumari P, Bhatt H, Ghosh B, Biswas S. Biotin functionalized PEGylated poly(amidoamine) dendrimer conjugate for active targeting of paclitaxel in cancer. Int J Pharm. 2019;557:329–341.
  • Dutta D, Alex SM, Bobba KN, Maiti KK, Bhuniya S. New insight into a cancer theranostic probe: efficient cell-specific delivery of SN-38 guided by biotinylated poly(vinyl alcohol). ACS Appl Mater Interfaces. 2016;8(49):33430–33438.
  • Yellepeddi VK, Kumar A, Palakurthi S. Biotinylated poly(amido)amine (PAMAM) dendrimers as carriers for drug delivery to ovarian cancer cells in vitro. Anticancer Res. 2009;29(8):2933–2943.
  • Tian X, Yin H, Zhang S, Luo Y, Xu K, Ma P, Sui C, Meng F, Liu Y, Jiang Y, et al. Bufalin loaded biotinylated chitosan nanoparticles: an efficient drug delivery system for targeted chemotherapy against breast carcinoma. Eur J Pharm Biopharm. 2014;87(3):445–453.