journal article·2014-01Open access

Single-walled carbon nanohorns decorated with semiconductor quantum dots to evaluate intracellular transport

Kristen A. Zimmermann, David L. Inglefield, Jianfei Zhang, Harry C. Dorn, Timothy E. Long, Christopher G. Rylander, M. Nichole Rylander

Journal of Nanoparticle Research· Volume 16· Issue 1

Abstract

Single-walled carbon nanohorns (SWNHs) have great potential to enhance thermal and chemotherapeutic drug efficiencies for cancer therapies. Despite their diverse capabilities, minimal research has been conducted so far to study nanoparticle intracellular transport, which is an important step in designing efficient therapies. SWNHs, like many other carbon nanomaterials, do not have inherent fluorescence properties making intracellular transport information difficult to obtain. The goals of this project were to (1) develop a simple reaction scheme to decorate the exohedral surface of SWNHs with fluorescent quantum dots (QDs) and improve conjugate stability, and (2) evaluate SWNH-QD conjugate cellular uptake kinetics and localization in various cancer cell lines of differing origins and morphologies. In this study, SWNHs were conjugated to CdSe/ZnS core/shell QDs using a unique approach to carbodiimide chemistry. Transmission electron microscopy and electron dispersive spectroscopy verified the conjugation of SWNHs and QDs. Cellular uptake kinetics and efficiency were characterized in three malignant cell lines: U-87 MG (glioblastoma), MDA-MB-231 (breast cancer), and AY-27 (bladder transitional cell carcinoma) using flow cytometry. Cellular distribution was verified by confocal microscopy, and cytotoxicity was also evaluated using an alamarBlue assay. Results indicate that cellular uptake kinetics and efficiency are highly dependent on cell type, highlighting the significance of studying nanoparticle transport at the cellular level. Nanoparticle intracellular transport investigations may provide information to optimize treatment parameters (e.g., SWNH concentration, treatment time, etc.) depending on tumor etiology.
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Research context

OpenAlex topics: Carbon and Quantum Dots Applications · Advanced biosensing and bioanalysis techniques · Graphene and Nanomaterials Applications

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

References (72)

Show source-provided references
1. Ajima K, Yudasaka M, Murakami T, Maigne A, Shiba K, Ijima S (2005) Carbon nanohorns as anticancer drug carriers. Mol Pharm 2(6):475–480. doi: 10.1021/Mp050056610.1021/mp0500566 ↗
2. Al Faraj A, Cieslar K, Lacroix G, Gaillard S, Canot-Soulas E, Cremillieux Y (2009) In vivo imaging of carbon nanotube biodistribution using magnetic resonance imaging. Nano Lett 9(3):1023–1027. doi: 10.1021/Nl803260810.1021/nl8032608 ↗
3. Bhirde AA, Patel V, Gavard J, Zhang GF, Sousa AA, Masedunskas A, Leapman RD, Weigert R, Gutkind JS, Rusling JF (2009) Targeted killing of cancer cells in vivo and in vitro with EGF-directed carbon nanotube-based drug delivery. ACS Nano 3(2):307–316. doi: 10.1021/Nn800551s10.1021/nn800551s ↗
4. Bianco A, Kostarelos K, Prato M (2008) Opportunities and challenges of carbon-based nanomaterials for cancer therapy. Expert Opin Drug Deliv 5(3):331–342. doi: 10.1517/17425247.5.3.33110.1517/17425247.5.3.331 ↗
5. Bottini M, Cerignoli F, Dawson MI, Magrini A, Rosato N, Mustelin T (2006) Full-length single-walled carbon nanotubes decorated with streptavidin-conjugated quantum dots as multivalent intracellular fluorescent nanoprobes. Biomacromolecules 7(8):2259–2263. doi: 10.1021/bm060203110.1021/bm0602031 ↗
6. Burke A, Ding X, Singh R, Kraft RA, Levi-Polyachenko N, Rylander MN, Szot C, Buchanan C, Whitney J, Fisher J, Hatcher HC, D’Agostino R Jr, Kock ND, Ajayan PM, Carroll DL, Akman S, Torti FM, Torti SV (2009) Long-term survival following a single treatment of kidney tumors with multiwalled carbon nanotubes and near-infrared radiation. Proc Natl Acad Sci USA 106(31):12897–12902. doi: 10.1073/pnas.090519510610.1073/pnas.0905195106 ↗
7. Chen J, Rao AM, Lyuksyutov S, Itkis ME, Hamon MA, Hu H, Cohn RW, Eklund PC, Colbert DT, Smalley RE, Haddon RC (2001) Dissolution of full-length single-walled carbon nanotubes. J Phys Chem B 105(13):2525–252810.1021/jp002596i ↗
8. Chithrani BD, Ghazani AA, Chan WCW (2006) Determining the size and shape dependence of gold nanoparticle uptake into mammalian cells. Nano Lett 6(4):662–668. doi: 10.1021/Nl052396o10.1021/nl052396o ↗
9. Decuzzi P, Godin B, Tanaka T, Lee SY, Chiappini C, Liu X, Ferrari M (2010) Size and shape effects in the biodistribution of intravascularly injected particles. J Control Release 141(3):320–327. doi: 10.1016/j.jconrel.2009.10.01410.1016/j.jconrel.2009.10.014 ↗
10. Derfus AM, Chan WCW, Bhatia SN (2004) Probing the cytotoxicity of semiconductor quantum dots. Nano Lett 4(1):11–18. doi: 10.1021/Nl034733410.1021/nl0347334 ↗
11. Dhar S, Liu Z, Thomale J, Dai HJ, Lippard SJ (2008) Targeted single-wall carbon nanotube-mediated Pt(IV) prodrug delivery using folate as a homing device. J Am Chem Soc 130(34):11467–11476. doi: 10.1021/Ja803036e10.1021/ja803036e ↗
12. Dillon AC, Jones KM, Bekkedahl TA, Kiang CH, Bethune DS, Heben MJ (1997) Storage of hydrogen in single-walled carbon nanotubes. Nature 386(6623):377–37910.1038/386377a0 ↗
13. Dorn HC, Zhang JF, Ge JC, Shultz MD, Chung EN, Singh G, Shu CY, Fatouros PP, Henderson SC, Corwin FD, Geohegan DB, Puretzky AA, Rouleau CM, More K, Rylander C, Rylander MN, Gibson HW (2010) In vitro and in vivo studies of single-walled carbon nanohorns with encapsulated metallofullerenes and exohedrally functionalized quantum dots. Nano Lett 10(8):2843–2848. doi: 10.1021/nl100863510.1021/nl1008635 ↗
14. Dorozhkin PS, Tovstonog SV, Golberg D, Zhan JH, Ishikawa Y, Shiozawa M, Nakanishi H, Nakata K, Bando Y (2005) A liquid-Ga-filled carbon nanotube: a miniaturized temperature sensor and electrical switch. Small 1(11):1088–1093. doi: 10.1002/smll.20050015410.1002/smll.200500154 ↗
15. dos Santos T, Varela J, Lynch I, Salvati A, Dawson KA (2011) Quantitative assessment of the comparative nanoparticle-uptake efficiency of a range of cell lines. Small 7(23):3341–3349. doi: 10.1002/smll.20110107610.1002/smll.201101076 ↗
16. Endo M, Strano MS, Ajayan PM (2008) Potential applications of carbon nanotubes. In: Topics in applied physics: carbon nanotubes, vol 111. Springer, Berlin10.1007/978-3-540-72865-8_2 ↗
17. Feng GD, Fei Q, Xiao DH, Zhang ZQ, Huan YF (2009) A novel silica-coated multiwall carbon nanotube with CdTe quantum dots nanocomposite. Spectrochim Acta A 74(2):597–601. doi: 10.1016/j.saa.2009.06.05610.1016/j.saa.2009.06.056 ↗
18. Fisher JW, Sarkar S, Buchanan CF, Szot CS, Whitney J, Hatcher HC, Torti SV, Rylander CG, Rylander MN (2010) Photothermal response of human and murine cancer cells to multiwalled carbon nanotubes after laser irradiation. Cancer Res 70(23):9855–9864. doi: 10.1158/0008-5472.CAN-10-025010.1158/0008-5472.CAN-10-0250 ↗
19. Gao XH, Cui YY, Levenson RM, Chung LWK, Nie SM (2004) In vivo cancer targeting and imaging with semiconductor quantum dots. Nat Biotechnol 22(8):969–976. doi: 10.1038/Nbt99410.1038/nbt994 ↗
20. Geys J, Nemmar A, Verbeken E, Smolders E, Ratoi M, Hoylaerts MF, Nemery B, Hoet PHM (2008) Acute toxicity and prothrombotic effects of quantum dots: impact of surface charge. Environ Health Perspect 116(12):1607–1613. doi: 10.1289/Ehp.1156610.1289/ehp.11566 ↗
21. Grabinski C, Hussain S, Lafdi K, Braydich-Stolle L, Schlager J (2007) Effect of particle dimension on biocompatibility of carbon nanomaterials. Carbon 45(14):2828–2835. doi: 10.1016/j.carbon.2007.08.03910.1016/j.carbon.2007.08.039 ↗
22. Guo Y, Shi DL, Cho HS, Dong ZY, Kulkarni A, Pauletti GM, Wang W, Lian J, Liu W, Ren L, Zhang QQ, Liu GK, Huth C, Wang LM, Ewing RC (2008) In vivo imaging and drug storage by quantum-dot-conjugated carbon nanotubes. Adv Funct Mater 18(17):2489–2497. doi: 10.1002/adfm.20080040610.1002/adfm.200800406 ↗
23. Hardman R (2006) A toxicologic review of quantum dots: toxicity depends on physicochemical and environmental factors. Environ Health Perspect 114(2):165–172. doi: 10.1289/Ehp.828410.1289/ehp.8284 ↗
24. Haremza JM, Hahn MA, Krauss TD (2002) Attachment of single CdSe nanocrystals to individual single-walled carbon nanotubes. Nano Lett 2(11):1253–1258. doi: 10.1021/Nl025799m10.1021/nl025799m ↗
25. Hoshino A, Fujioka K, Oku T, Suga M, Sasaki YF, Ohta T, Yasuhara M, Suzuki K, Yamamoto K (2004) Physicochemical properties and cellular toxicity of nanocrystal quantum dots depend on their surface modification. Nano Lett 4(11):2163–2169. doi: 10.1021/Nl048715d10.1021/nl048715d ↗
26. Jain RK, Stylianopoulos T (2010) Delivering nanomedicine to solid tumors. Nat Rev Clin Oncol 7(11):653–664. doi: 10.1038/nrclinonc.2010.13910.1038/nrclinonc.2010.139 ↗
27. Kam NWS, Liu ZA, Dai HJ (2006) Carbon nanotubes as intracellular transporters for proteins and DNA: an investigation of the uptake mechanism and pathway. Angew Chem Int Ed 45(4):577–581. doi: 10.1002/anie.20050338910.1002/anie.200503389 ↗
28. Klibanov AL, Maruyama K, Beckerleg AM, Torchilin VP, Huang L (1991) Activity of amphipathic poly(ethylene glycol) 5000 to prolong the circulation time of liposomes depends on the liposome size and is unfavorable for immunoliposome binding to target. Biochim Biophys Acta 1062(2):142–14810.1016/0005-2736(91)90385-L ↗
29. Kostarelos K, Lacerda L, Pastorin G, Wu W, Wieckowski S, Luangsivilay J, Godefroy S, Pantarotto D, Briand JP, Muller S, Prato M, Bianco A (2007) Cellular uptake of functionalized carbon nanotubes is independent of functional group and cell type. Nat Nanotechnol 2(2):108–113. doi: 10.1038/nnano.2006.20910.1038/nnano.2006.209 ↗
30. Lee SM, Lee YH (2000) Hydrogen storage in single-walled carbon nanotubes. Appl Phys Lett 76(20):2877–287910.1063/1.126503 ↗
31. Li L, Daou TJ, Texier I, Tran TKC, Nguyen QL, Reiss P (2009) Highly luminescent CuInS(2)/ZnS core/shell nanocrystals: cadmium-free quantum dots for in vivo imaging. Chem Mater 21(12):2422–2429. doi: 10.1021/Cm900103b10.1021/cm900103b ↗
32. Li XL, Qin YJ, Picraux ST, Guo ZX (2011) Noncovalent assembly of carbon nanotube-inorganic hybrids. J Mater Chem 21(21):7527–7547. doi: 10.1039/C1jm10516g10.1039/c1jm10516g ↗
33. Li Y, Wang J, Wientjes MG, Au JL (2012) Delivery of nanomedicines to extracellular and intracellular compartments of a solid tumor. Adv Drug Deliv Rev 64(1):29–39. doi: 10.1016/j.addr.2011.04.00610.1016/j.addr.2011.04.006 ↗
34. Liu X, Shi L, Niu W, Li H, Xu G (2008) Amperometric glucose biosensor based on single-walled carbon nanohorns. Biosens Bioelectron 23(12):1887–1890. doi: 10.1016/j.bios.2008.02.01610.1016/j.bios.2008.02.016 ↗
35. Maruyama K (2011) Intracellular targeting delivery of liposomal drugs to solid tumors based on EPR effects. Adv Drug Deliv Rev 63(3):161–169. doi: 10.1016/j.addr.2010.09.00310.1016/j.addr.2010.09.003 ↗
36. Medintz IL, Uyeda HT, Goldman ER, Mattoussi H (2005) Quantum dot bioconjugates for imaging, labelling and sensing. Nat Mater 4(6):435–446. doi: 10.1038/Nmat139010.1038/nmat1390 ↗
37. Miyawaki J, Yudasaka M, Imai H, Yorimitsu H, Isobe H, Nakamura E, Iijima S (2006) In vivo magnetic resonance imaging of single-walled carbon nanohorns by labeling with magnetite nanoparticles. Adv Mater 18(8):1010–1014. doi: 10.1002/adma.20050217410.1002/adma.200502174 ↗
38. Miyawaki J, Matsumura S, Yuge R, Murakami T, Sato S, Tonnida A, Tsuruo T, Ichihashi T, Fujinami T, Irie H, Tsuchida K, Iijima S, Shiba K, Yudasaka M (2009) Biodistribution and ultrastructural localization of single-walled carbon nanohorns determined in vivo with embedded Gd(2)O(3) labels. ACS Nano 3(6):1399–1406. doi: 10.1021/Nn900484610.1021/nn9004846 ↗
39. Monteiro-Riviere NA, Inman AO, Zhang LW (2009) Limitations and relative utility of screening assays to assess engineered nanoparticle toxicity in a human cell line. Toxicol Appl Pharmacol 234(2):222–235. doi: 10.1016/j.taap.2008.09.03010.1016/j.taap.2008.09.030 ↗
40. Muralkami T, Ajima K, Miyawaki J, Yudasaka M, Iijima S, Shiba K (2004) Drug-loaded carbon nanohorns: adsorption and release of dexamethasone in vitro. Mol Pharm 1(6):399–405. doi: 10.1021/Mp049928e10.1021/mp049928e ↗
41. Ozkan CS, Ravindran S, Chaudhary S, Colburn B, Ozkan M (2003) Covalent coupling of quantum dots to multiwalled carbon nanotubes for electronic device applications. Nano Lett 3(4):447–453. doi: 10.1021/nl025968310.1021/nl0259683 ↗
42. Parak WJ, Gerion D, Pellegrino T, Zanchet D, Micheel C, Williams SC, Boudreau R, Le Gros MA, Larabell CA, Alivisatos AP (2003) Biological applications of colloidal nanocrystals. Nanotechnology 14(7):R15–R2710.1088/0957-4484/14/7/201 ↗
43. Porter AE, Gass M, Muller K, Skepper JN, Midgley PA, Welland M (2007) Direct imaging of single-walled carbon nanotubes in cells. Nat Nanotechnol 2(11):713–717. doi: 10.1038/nnano.2007.34710.1038/nnano.2007.347 ↗
44. Porter AE, Gass M, Bendall JS, Muller K, Goode A, Skepper JN, Midgley PA, Welland M (2009) Uptake of noncytotoxic acid-treated single-walled carbon nanotubes into the cytoplasm of human macrophage cells. ACS Nano 3(6):1485–1492. doi: 10.1021/Nn900416z10.1021/nn900416z ↗
45. Puretzky AA, Styers-Barnett DJ, Rouleau CM, Hu H, Zhao B, Ivanov IN, Geohegan DB (2008) Cumulative and continuous laser vaporization synthesis of single wall carbon nanotubes and nanohorns. Appl Phys A 93(4):849–855. doi: 10.1007/s00339-008-4744-310.1007/s00339-008-4744-3 ↗
46. Raffaelle RP, Landi BJ, Evans CM, Worman JJ, Castro SL, Bailey SG (2006) Noncovalent attachment of CdSe quantum dots to single wall carbon nanotubes. Mater Lett 60(29–30):3502–3506. doi: 10.1016/j.matlet.2006.03.05710.1016/j.matlet.2006.03.057 ↗
47. Raja PMV, Connolley J, Ganesan GP, Ci LJ, Ajayan PM, Nalamasu O, Thompson DM (2007) Impact of carbon nanotube exposure, dosage and aggregation on smooth muscle cells. Toxicol Lett 169(1):51–63. doi: 10.1016/j.toxlet.2006.12.00310.1016/j.toxlet.2006.12.003 ↗
48. Resch-Genger U, Grabolle M, Cavaliere-Jaricot S, Nitschke R, Nann T (2008) Quantum dots versus organic dyes as fluorescent labels. Nat Methods 5(9):763–775. doi: 10.1038/Nmeth.124810.1038/nmeth.1248 ↗
49. Richard C, Doan BT, Beloeil JC, Bessodes M, Toth E, Scherman D (2008) Noncovalent functionalization of carbon nanotubes with amphiphilic Gd3+ chelates: toward powerful T-1 and T-2 MRI contrast agents. Nano Lett 8(1):232–236. doi: 10.1021/N1072509z10.1021/nl072509z ↗
50. Schlapbach L, Zuttel A (2001) Hydrogen-storage materials for mobile applications. Nature 414(6861):353–35810.1038/35104634 ↗
51. Shi DL, Guo Y, Dong ZY, Lian J, Wang W, Liu G, Wang LM, Ewing RC (2007) Quantum-dot-activated luminescent carbon nanotubes via a nano scale surface functionalization for in vivo imaging. Adv Mater 19(8):4033
52. Siegel R, Naishadham D, Jemal A (2012) Cancer statistics. CA Cancer J Clin 62(1):10–29. doi: 10.3322/Caac.2013810.3322/caac.20138 ↗
53. Suehiro J, Zhou GB, Hara M (2003) Fabrication of a carbon nanotube-based gas sensor using dielectrophoresis and its application for ammonia detection by impedance spectroscopy. J Phys D 36(21):L109–L11410.1088/0022-3727/36/21/L01 ↗
54. Susumu K, Medintz IL, Mattoussi H (2009) Colloidal quantum dots: synthesis, photophysical properties, and biofunctionalization strategies. In: Mattoussi H, Cheon J (eds) Inorganic nanoprobes for biological sensing and imaging. Artech House, Inc., Norwood, pp 1–26
55. Tchoul MN, Ford WT, Lolli G, Resasco DE, Arepalli S (2007) Effect of mild nitric acid oxidation on dispersability, size, and structure of single-walled carbon nanotubes. Chem Mater 19(23):5765–5772. doi: 10.1021/Cm071758l10.1021/cm071758l ↗
56. Teeguarden JG, Hinderliter PM, Orr G, Thrall BD, Pounds JG (2007) Particokinetics in vitro: dosimetry considerations for in vitro nanoparticle toxicity assessments. Toxicol Sci 95(2):300–312. doi: 10.1093/toxsci/kfl16510.1093/toxsci/kfl165 ↗
57. Utsumi S, Miyawaki J, Tanaka H, Hattori Y, Itoi T, Ichikuni N, Kanoh H, Yudasaka M, Iijima S, Kaneko K (2005) Opening mechanism of internal nanoporosity of single-wall carbon nanohorn. J Phys Chem B 109(30):14319–14324. doi: 10.1021/Jp051266110.1021/jp0512661 ↗
58. Wang J, Liu GD, Jan MR (2004) Ultrasensitive electrical biosensing of proteins and DNA: carbon-nanotube derived amplification of the recognition and transduction events. J Am Chem Soc 126(10):3010–3011. doi: 10.1021/Ja031723w10.1021/ja031723w ↗
59. Wang L, Niu MG, Wu ZW (2009) In situ growth of CdSe/CdS quantum dots inside and outside of MWCNTs. Curr Appl Phys 9(5):1112–1116. doi: 10.1016/j.cap.2008.12.01210.1016/j.cap.2008.12.012 ↗
60. White B, Banerjee S, O’Brien S, Turro NJ, Herman IP (2007) Zeta-potential measurements of surfactant-wrapped individual single-walled carbon nanotubes. J Phys Chem C 111(37):13684–13690. doi: 10.1021/Jp070853e10.1021/jp070853e ↗
61. Whitney JR, Sarkar S, Zhang JF, Thao D, Young T, Manson MK, Campbell TA, Puretzky AA, Rouleau CM, More KL, Geohegan DB, Rylander CG, Dorn HC, Rylander MN (2011) Single walled carbon nanohorns as photothermal cancer agents. Laser Surg Med 43(1):43–51. doi: 10.1002/lsm.2102510.1002/lsm.21025 ↗
62. Woelfle C, Claus RO (2007) Transparent and flexible quantum dot–polymer composites using an ionic liquid as compatible polymerization medium. Nanotechnology 18(2). doi: 10.1088/0957-4484/18/2/02540210.1088/0957-4484/18/2/025402 ↗
63. Wong SS, Banerjee S (2002) Synthesis and characterization of carbon nanotube–nanocrystal heterostructures. Nano Lett 2(3):195–200. doi: 10.1021/nl015651n10.1021/nl015651n ↗
64. Wuister SF, Swart I, van Driel F, Hickey SG, Donega CD (2003) Highly luminescent water-soluble CdTe quantum dots. Nano Lett 3(4):503–507. doi: 10.1021/Nl034054t10.1021/nl034054t ↗
65. Xu JX, Yudasaka M, Kouraba S, Sekido M, Yamamoto Y, Iijima S (2008) Single wall carbon nanohorn as a drug carrier for controlled release. Chem Phys Lett 461(4–6):189–192. doi: 10.1016/j.cplett.2008.06.07710.1016/j.cplett.2008.06.077 ↗
66. Yong KT, Ding H, Roy I, Law WC, Bergey EJ, Maitra A, Prasad PN (2009) Imaging pancreatic cancer using bioconjugated InP quantum dots. ACS Nano 3(3):502–510. doi: 10.1021/Nn800893310.1021/nn8008933 ↗
67. Yuan F, Dellian M, Fukumura D, Leunig M, Berk DA, Torchilin VP, Jain RK (1995) Vascular-permeability in a human tumor xenograft—molecular-size dependence and cutoff size. Cancer Res 55(17):3752–3756
68. Yudasaka M, Iijima S, Yamada R, Bandow S, Suenaga K, Kokai F, Takahashi K (1999) Nano-aggregates of single-walled graphitic carbon nano-horns. Chem Phys Lett 309(3–4):165–170
69. Yudasaka M, Iijima S, Crespi VH (2008) Single-wall carbon nanohorns and nanocones. Top Appl Phys 111:605–62910.1007/978-3-540-72865-8_19 ↗
70. Zhang M, Murakami T, Ajima K, Tsuchida K, Sandanayaka ASD, Ito O, Iijima S, Yudasaka M (2008) Fabrication of ZnPc/protein nanohorns for double photodynamic and hyperthermic cancer phototherapy. Proc Natl Acad Sci USA 105(39):14773–14778. doi: 10.1073/pnas.080134910510.1073/pnas.0801349105 ↗
71. Zhu S, Han S, Zhang L, Parveen S, Xu G (2011) A novel fluorescent aptasensor based on single-walled carbon nanohorns. Nanoscale 3(11):4589–4592. doi: 10.1039/c1nr10774g10.1039/c1nr10774g ↗
72. Zimmer JP, Kim SW, Ohnishi S, Tanaka E, Frangioni JV, Bawendi MG (2006) Size series of small indium arsenide–zinc selenide core–shell nanocrystals and their application to in vivo imaging. J Am Chem Soc 128(8):2526–2527. doi: 10.1021/Ja057981610.1021/ja0579816 ↗