Skip to main content

Advertisement

SpringerLink
Log in

Glycosylated phospholipid-coated upconversion nanoparticles for bioimaging of non-muscle invasive bladder cancers

  • Original Paper
  • Published:
Microchimica Acta Aims and scope Submit manuscript

Abstract

Detection of non-muscle invasive bladder cancer (NMIBC) is crucial to facilitate complete tumor resection, thus improving the survival rate as well as reducing the recurrence frequency and treatment expense. Fluorescence imaging cystoscopy is an effective method for the detection of NMIBC. However, its application is limited as the commonly applied fluorescent agents such as dyes and photosensitizers usually lack specific tumor accumulation and are vulnerable to photobleaching. Furthermore, the broad emission band of conventional fluorescent agents limits their imaging and detection efficacy. To overcome these limitations, upconversion nanoparticles (UCNPs) have been selected as the fluorescent agent, due to their resistance to photobleaching, less background auto-fluorescence, and narrow emission bands. In order to achieve active tumor targeting, the UCNPs are coated with a glycosylated phospholipid layer. The glycosylated phospholipid-coated UCNPs exhibited high selective accumulation in cancer cells over normal cells and enhanced the upconversion luminescence (UCL) (at 540 nm and 660 nm) from bladder cancer cells under 980 nm laser irradiation.

Graphical abstract

Glycosylated phospholipid coating that promotes uptake of UCNPs by cancer cells, and UCL emitted from UCNPs under NIR (980 nm) laser irradiation for cancer cell imaging.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Cassell A, Yunusa B, Jalloh M, Mbodji MM, Diallo A, Ndoye M, Diallo Y, Labou Y, Niang Y, Gueye SM (2019) Non-muscle invasive bladder cancer: a review of the current trend in Africa. World J Urol 10(3):123. https://doi.org/10.14740/wjon1210

    Article  Google Scholar 

  2. Bunce C, Ayres BE, Griffiths TL, Mostafid H, Kelly J, Persad R, Kockelbergh R (2010) The role of hexylaminolaevulinate in the diagnosis and follow-up of non-muscle-invasive bladder cancer. BJU Int 105:2–7. https://doi.org/10.1111/j.1464-410X.2009.09150.x

    Article  PubMed  Google Scholar 

  3. Inoue K (2017) 5-Aminolevulinic acid-mediated photodynamic therapy for bladder cancer. Int J Urol 24(2):97–101. https://doi.org/10.1111/iju.13291

    Article  CAS  PubMed  Google Scholar 

  4. Russo GI, Sholklapper TN, Cocci A, Broggi G, Caltabiano R, Smith AB, Lotan Y, Morgia G, Kamat AM, Witjes JA (2021) Performance of narrow band imaging (Nbi) and photodynamic diagnosis (pdd) fluorescence imaging compared to white light cystoscopy (wlc) in detecting non-muscle invasive bladder cancer: a systematic review and lesion-level diagnostic meta-analysis. Cancers (Basel) 13(17):4378. https://doi.org/10.3390/cancers13174378

    Article  CAS  PubMed Central  Google Scholar 

  5. Lerner SP, Goh A (2015) Novel endoscopic diagnosis for bladder cancer. Cancer 121(2):169–178. https://doi.org/10.1002/cncr.28905

    Article  PubMed  Google Scholar 

  6. Saksena MA, Dahl DM, Harisinghani MG (2006) New imaging modalities in bladder cancer. World J Urol 24(5):473–480. https://doi.org/10.1007/s00345-006-0118-7

    Article  PubMed  Google Scholar 

  7. Martingano P, Stacul F, Cavallaro M, Casagrande F, Cernic S, Belgrano M, Cova M (2010) 64-Slice CT urography: 30 months of clinical experience. Radiol Med 115(6):920–935. https://doi.org/10.1007/s11547-010-0567-3

    Article  CAS  PubMed  Google Scholar 

  8. Sylvester RJ, van der MEIJDEN AP, Lamm DL, (2002) Intravesical bacillus Calmette-Guerin reduces the risk of progression in patients with superficial bladder cancer: a meta-analysis of the published results of randomized clinical trials. J Oncol 168(5):1964–1970. https://doi.org/10.1016/S0022-5347(05)64273-5

    Article  CAS  Google Scholar 

  9. Aydh A, Abufaraj M, Mori K, Quhal F, Pradere B, Motlagh RS, Mostafaei H, Karakiewicz PI, Shariat SF (2021) Performance of fluoro-2-deoxy-D-glucose positron emission tomography-computed tomography imaging for lymph node staging in bladder and upper tract urothelial carcinoma: a systematic review. Arab J Urol 19(1):59–66. https://doi.org/10.1080/2090598X.2020.1858012

    Article  Google Scholar 

  10. Crozier J, Papa N, Perera M, Ngo B, Bolton D, Sengupta S, Lawrentschuk N (2019) Comparative sensitivity and specificity of imaging modalities in staging bladder cancer prior to radical cystectomy: a systematic review and meta-analysis. World J Urol 37(4):667–690. https://doi.org/10.1007/s00345-018-2439-8

    Article  PubMed  Google Scholar 

  11. Golijanin J, Amin A, Moshnikova A, Brito JM, Tran TY, Adochite R-C, Andreev GO (2016) T Crawford, DM Engelman, OA Andreev, Targeted imaging of urothelium carcinoma in human bladders by an ICG pHLIP peptide ex vivo. Proc Natl Acad Sci U S A 113(42):11829–11834. https://doi.org/10.1073/pnas.1610472113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Witjes JA, Douglass J (2007) The role of hexaminolevulinate fluorescence cystoscopy in bladder cancer. Nat Clin Pract Urol 4(10):542–549. https://doi.org/10.1038/ncpuro0917

    Article  CAS  PubMed  Google Scholar 

  13. Nyk M, Kumar R, Ohulchanskyy TY, Bergey EJ, Prasad, (2008) PN High contrast in vitro and in vivo photoluminescence bioimaging using near infrared to near infrared up-conversion in Tm3+ and Yb3+ doped fluoride nanophosphors. Nano Lett 8(11):3834–3838. https://doi.org/10.1021/nl802223f

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Cho SK, Su L-J, Mao C, Wolenski CD, Flaig TW, Park W (2019) Multifunctional nanoclusters of NaYF4: Yb3+, Er3+ upconversion nanoparticle and gold nanorod for simultaneous imaging and targeted chemotherapy of bladder cancer. Mater Sci Eng C 97:784–792. https://doi.org/10.1016/j.msec.2018.12.113

    Article  CAS  Google Scholar 

  15. Pan Y, Volkmer J-P, Mach KE, Rouse RV, Liu J-J, Sahoo D, Chang T, Metzner TJ, Kang L, Van De Rijn M (2014) Endoscopic molecular imaging of human bladder cancer using a CD4S7 antibody. Sci Transl Med 6(260):260–260. https://doi.org/10.1126/scitranslmed.3009457

    Article  CAS  Google Scholar 

  16. Lokeshwar VB, Selzer MG, Urinary bladder tumor markers, (2006) Urol Oncol 24(6):528–537. https://doi.org/10.1016/j.urolonc.2006.07.003

    Article  CAS  PubMed  Google Scholar 

  17. Calvo MB, Figueroa A, Pulido EG, Campelo RG, Aparicio LA (2010) Potential role of sugar transporters in cancer and their relationship with anticancer therapy Int J Endocrinol 2010 https://doi.org/10.1016/10.1155/2010/205357

  18. Chen Z, Lu W, Garcia-Prieto C, Huang P (2007) The Warburg effect and its cancer therapeutic implications. J Bioenerg Biomembr 39(3):267–274. https://doi.org/10.1016/10.1007/s10863-007-9086-x

    Article  CAS  PubMed  Google Scholar 

  19. Calvaresi EC, Hergenrother PJ (2013) Glucose conjugation for the specific targeting and treatment of cancer. Chem Sci 4(6):2319–2333. https://doi.org/10.1039/C3SC22205E

    Article  CAS  PubMed  Google Scholar 

  20. Lee J-H, Kim Y-W, Chang S-G (2005) Glucose transporter-1 expression in urothelial papilloma of the bladder. Urol Int 74(3):268–271. https://doi.org/10.1159/000083561

    Article  CAS  PubMed  Google Scholar 

  21. Afonso J, Santos LL, Longatto-Filho A, Baltazar F (2020) Competitive glucose metabolism as a target to boost bladder cancer immunotherapy. Nat Rev Urol 17(2):77–106. https://doi.org/10.1038/s41585-019-0263-6

    Article  CAS  PubMed  Google Scholar 

  22. Zheng S, Chen Y, Miao W (2018) 99mTc-3PRGD2 for integrin receptor imaging of esophageal cancer compared study with 18F-FDG PET/CT Soc Nuclear Med https://doi.org/10.1007/s12149-018-1315-3

  23. Chan KK, Giovanni D, He H, Sum TC, Yong K-T (2021) Water-stable all-inorganic perovskite nanocrystals with nonlinear optical properties for targeted multiphoton bioimaging. ACS Appl Nano Mater 4(9):9022–9033. https://doi.org/10.1021/acsanm.1c01621

    Article  CAS  Google Scholar 

  24. Wu P, Yan X-P (2013) Doped quantum dots for chemo/biosensing and bioimaging. Chem Soc Rev 42(12):5489–5521. https://doi.org/10.1039/c3cs60017c

    Article  CAS  PubMed  Google Scholar 

  25. Chen X, Song J, Chen X, Yang H (2019) X-ray-activated nanosystems for theranostic applications. Chem Soc Rev 48(11):3073–3101. https://doi.org/10.1039/C8CS00921J

    Article  CAS  PubMed  Google Scholar 

  26. Wang M, Mi C, Zhang Y, Liu J, Li F, Mao C, Xu S (2009) NIR-responsive silica-coated NaYbF4: Er/Tm/Ho upconversion fluorescent nanoparticles with tunable emission colors and their applications in immunolabeling and fluorescent imaging of cancer cells. J Phys Chem C 113(44):19021–19027. https://doi.org/10.1021/jp906394z

    Article  CAS  Google Scholar 

  27. Hlaváček A, Farka Z, Mickert MJ, Kostiv U, Brandmeier JC, Horák D, Skládal P, Foret F, Gorris HH (2022) Bioconjugates of photon-upconversion nanoparticles for cancer biomarker detection and imaging Nat Protoc 1-45 https://doi.org/10.1038/s41596-021-00670-7

  28. Wang C, Cheng L, Liu Z (2011) Drug delivery with upconversion nanoparticles for multi-functional targeted cancer cell imaging and therapy. Biomaterials 32(4):1110–1120. https://doi.org/10.1016/j.biomaterials.2010.09.069

    Article  CAS  PubMed  Google Scholar 

  29. Liu J-N, Bu W-B, Shi J-L (2015) Silica coated upconversion nanoparticles: a versatile platform for the development of efficient theranostics. Acc Chem Res 48(7):1797–1805. https://doi.org/10.1021/acs.accounts.5b00078

    Article  CAS  PubMed  Google Scholar 

  30. Zhang Z, Jayakumar MKG, Zheng X, Shikha S, Zhang Y, Bansal A, Poon DJ, Chu PL, Yeo EL, Chua ML (2019) Upconversion superballs for programmable photoactivation of therapeutics. Nat Commun 10(1):1–12. https://doi.org/10.1038/s41467-019-12506-w

    Article  CAS  Google Scholar 

  31. Boyer J-C, Carling C-J, Gates BD, Branda NR (2010) Two-way photoswitching using one type of near-infrared light, upconverting nanoparticles, and changing only the light intensity. J Am Chem Soc 132(44):15766–15772. https://doi.org/10.1021/ja107184z

    Article  CAS  PubMed  Google Scholar 

  32. Y. Zhang Y, Lei P, Zhu X, Zhang Y, (2021) Full shell coating or cation exchange enhances luminescence. Nat Commun 12(1):1–10. https://doi.org/10.1038/s41467-021-26490-7

    Article  Google Scholar 

  33. Guo H, Li F, Qiu H, Xu W, Li P, Hou Y, Ding J, Chen X (2020) Synergistically enhanced mucoadhesive and penetrable polypeptide nanogel for efficient drug delivery to orthotopic bladder cancer Research https://doi.org/10.34133/2020/8970135

  34. Mei Q, Bansal A, Jayakumar MKG, Zhang Z, Zhang J, Huang H, Yu D, Ramachandra CJ, Hausenloy DJ, Soong TW (2019) Manipulating energy migration within single lanthanide activator for switchable upconversion emissions towards bidirectional photoactivation. Nat Commun 10(1):1–11. https://doi.org/10.1038/s41467-019-12374-4

    Article  CAS  Google Scholar 

  35. Chang S-G, Lee S-J, Lee C-H, Kim JI, Kim Y-W (2000) Expression of the human erythrocyte glucose transporter in transitional cell carcinoma of the bladder. Urology 55(3):448–452. https://doi.org/10.1016/S0090-4295(99)00474-4

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We acknowledge financial support from the Ministry of Education of Singapore (MOE 2016-T3-1-004, R-397-000-274-112, R-397-000-348-114, R-397-000-375-114) and the National University of Singapore.

We thank Ms. Xu Yuexin for her assistance in plotting graphical abstract.

Author information

Authors and Affiliations

  1. Department of Chemical and Biomolecular Engineering, College of Design and Engineering, National University of Singapore, Singapore, 117585, Singapore

    Bowen Sun & Koon Gee Neoh

  2. Department of Biomedical Engineering, College of Design and Engineering, National University of Singapore, Singapore, 117583, Singapore

    Bowen Sun, Sneha Sree Mullapudi & Yong Zhang

Authors
  1. Bowen Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sneha Sree Mullapudi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Koon Gee Neoh
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Yong Zhang or Koon Gee Neoh.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 1450 KB)

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sun, B., Mullapudi, S.S., Zhang, Y. et al. Glycosylated phospholipid-coated upconversion nanoparticles for bioimaging of non-muscle invasive bladder cancers. Microchim Acta 189, 349 (2022). https://doi.org/10.1007/s00604-022-05411-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00604-022-05411-5

Keywords

Search

Navigation