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Erschienen in: Lasers in Medical Science 5/2022

04.02.2022 | Original Article

Photodynamic therapy mediated by nanoparticles Aluminum Chloro Phthalocyanine in oral squamous carcinoma cells

verfasst von: Lilian Mendes Borburema Cangussu, Ludmilla Regina de Souza, Marcela Gonçalves de Souza, Renato Sobral Monteiro Junior, Luis Alexandre Muehlmann, Paulo Narcizo de Souza, Lucyana Conceição Farias, Sérgio Henrique Sousa Santos, Alfredo Maurício Batista de Paula, André Luiz Sena Guimarães

Erschienen in: Lasers in Medical Science | Ausgabe 5/2022

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Abstract

The aim of this study is to investigate the antineoplastic potential of photodynamic therapy (PDT) mediated by an aluminum-phthalocyanine chloride nanoemulsion (AlPc-NE), against an oral squamous cell carcinoma (OSCC) cell line in vitro. Both OSCC (SCC9) and A431 cell lines were studied in vitro. Four study groups were used: Group 1 (phosphate-buffered saline [PBS]), Group 2 (PBS + 28.3 J/cm2 irradiation), Group 3 (AlPc-NE alone), and Group 4 (AlPc-NE + 28.3 J/cm2 irradiation). To test the effect of PDT with AlPc-NE, cell viability, migration, and cell death assays were performed. Moreover, the expressions of Ki-67 and TP53 were evaluated using immunoassays. The results showed that PDT mediated by all AlPc-NE concentrations evaluated (i.e., 0.7, 0.35, and 0.17 nM AlPc) significantly reduced the viability of SCC9 cells. Migration and cell death assays also revealed that PDT with AlPc-NE significantly reduced the rate of migration and increased cell death compared to the control groups. In addition, it was found that PDT with AlPc-NE reduced Ki-67 and mutated TP53 immunoexpression. PDT with AlPc-NE is effective in reducing the viability and migration of SCC9. Moreover, PDT with AlPc-NE nanoemulsions reduces the cell proliferation and expression of mutant TP53.
Literatur
1.
Zurück zum Zitat Bray F et al (2018) Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 68(6):394–424CrossRefPubMed Bray F et al (2018) Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 68(6):394–424CrossRefPubMed
2.
Zurück zum Zitat Global burden of disease cancer collaoration et al (2019) Global regional, and national cancer incidence, mortality, years of life lost, years lived with disability, and disability-adjusted life-years for 29 cancer groups, 1990 to 2017: a systematic analysis for the global burden of disease study. JAMA Oncol 5(12):1749–1768. https://doi.org/10.1001/jamaoncol.2019.2996 Global burden of disease cancer collaoration et al (2019) Global regional, and national cancer incidence, mortality, years of life lost, years lived with disability, and disability-adjusted life-years for 29 cancer groups, 1990 to 2017: a systematic analysis for the global burden of disease study. JAMA Oncol 5(12):1749–1768. https://​doi.​org/​10.​1001/​jamaoncol.​2019.​2996
3.
Zurück zum Zitat Righini CA et al (2008) Risk factors for cancers of the oral cavity, pharynx (cavity excluded) and larynx. Presse Med 37(9):1229–1240PubMedCrossRef Righini CA et al (2008) Risk factors for cancers of the oral cavity, pharynx (cavity excluded) and larynx. Presse Med 37(9):1229–1240PubMedCrossRef
4.
Zurück zum Zitat De Paula AM et al (2009) Analysis of 724 cases of primary head and neck squamous cell carcinoma (HNSCC) with a focus on young patients and p53 immunolocalization. Oral Oncol 45(9):777–782PubMedCrossRef De Paula AM et al (2009) Analysis of 724 cases of primary head and neck squamous cell carcinoma (HNSCC) with a focus on young patients and p53 immunolocalization. Oral Oncol 45(9):777–782PubMedCrossRef
5.
Zurück zum Zitat Min S-K et al (2017) Conditional relative survival of oral cavity cancer: Based on Korean Central Cancer Registry. Oral Oncol 72:73–79PubMedCrossRef Min S-K et al (2017) Conditional relative survival of oral cavity cancer: Based on Korean Central Cancer Registry. Oral Oncol 72:73–79PubMedCrossRef
6.
Zurück zum Zitat Guimaraes TA et al (2016) Metformin increases PDH and suppresses HIF-1alpha under hypoxic conditions and induces cell death in oral squamous cell carcinoma. Oncotarget 7(34):55057–55068PubMedPubMedCentralCrossRef Guimaraes TA et al (2016) Metformin increases PDH and suppresses HIF-1alpha under hypoxic conditions and induces cell death in oral squamous cell carcinoma. Oncotarget 7(34):55057–55068PubMedPubMedCentralCrossRef
7.
Zurück zum Zitat Guimaraes TA et al (2016) Evaluation of the antineoplastic activity of gallic acid in oral squamous cell carcinoma under hypoxic conditions. Anticancer Drugs 27(5):407–416PubMedCrossRef Guimaraes TA et al (2016) Evaluation of the antineoplastic activity of gallic acid in oral squamous cell carcinoma under hypoxic conditions. Anticancer Drugs 27(5):407–416PubMedCrossRef
8.
Zurück zum Zitat Shah JP, Gil Z (2009) Current concepts in management of oral cancer – Surgery. Oral Oncol 45(4):394–401PubMedCrossRef Shah JP, Gil Z (2009) Current concepts in management of oral cancer – Surgery. Oral Oncol 45(4):394–401PubMedCrossRef
9.
Zurück zum Zitat Sobecki M et al (2017) Cell-cycle regulation accounts for variability in Ki-67 expression levels. Cancer Res 77(10):2722–2734PubMedCrossRef Sobecki M et al (2017) Cell-cycle regulation accounts for variability in Ki-67 expression levels. Cancer Res 77(10):2722–2734PubMedCrossRef
11.
Zurück zum Zitat Biel MA (2007) Photodynamic therapy treatment of early oral and laryngeal cancers. Photochem Photobiol 83(5):1063–1068PubMedCrossRef Biel MA (2007) Photodynamic therapy treatment of early oral and laryngeal cancers. Photochem Photobiol 83(5):1063–1068PubMedCrossRef
12.
Zurück zum Zitat Chen HM et al (2005) Successful treatment of an extensive verrucous carcinoma with topical 5-aminolevulinic acid-mediated photodynamic therapy. J Oral Pathol Med 34(4):253–256PubMedCrossRef Chen HM et al (2005) Successful treatment of an extensive verrucous carcinoma with topical 5-aminolevulinic acid-mediated photodynamic therapy. J Oral Pathol Med 34(4):253–256PubMedCrossRef
13.
Zurück zum Zitat Castilho-Fernandes A et al (2017) Photodynamic process induced by chloro-aluminum phthalocyanine nanoemulsion in glioblastoma. Photodiagn Photodyn Ther 19:221–228CrossRef Castilho-Fernandes A et al (2017) Photodynamic process induced by chloro-aluminum phthalocyanine nanoemulsion in glioblastoma. Photodiagn Photodyn Ther 19:221–228CrossRef
15.
Zurück zum Zitat Huang Z et al (2008) Photodynamic therapy for treatment of solid tumors–potential and technical challenges. Technol Cancer Res Treat 7(4):309–320PubMedCrossRef Huang Z et al (2008) Photodynamic therapy for treatment of solid tumors–potential and technical challenges. Technol Cancer Res Treat 7(4):309–320PubMedCrossRef
16.
Zurück zum Zitat Py-Daniel KR et al (2016) Highly efficient photodynamic therapy colloidal system based on chloroaluminum phthalocyanine/pluronic micelles. Eur J Pharm Biopharm 103:23–31PubMedCrossRef Py-Daniel KR et al (2016) Highly efficient photodynamic therapy colloidal system based on chloroaluminum phthalocyanine/pluronic micelles. Eur J Pharm Biopharm 103:23–31PubMedCrossRef
17.
Zurück zum Zitat Nunes SM, Sguilla FS, Tedesco AC (2004) Photophysical studies of zinc phthalocyanine and chloroaluminum phthalocyanine incorporated into liposomes in the presence of additives. Braz J Med Biol Res 37(2):273–284PubMedCrossRef Nunes SM, Sguilla FS, Tedesco AC (2004) Photophysical studies of zinc phthalocyanine and chloroaluminum phthalocyanine incorporated into liposomes in the presence of additives. Braz J Med Biol Res 37(2):273–284PubMedCrossRef
18.
Zurück zum Zitat Moll UM et al (2005) Transcription-independent pro-apoptotic functions of p53. Curr Opin Cell Biol 17(6):631–636PubMedCrossRef Moll UM et al (2005) Transcription-independent pro-apoptotic functions of p53. Curr Opin Cell Biol 17(6):631–636PubMedCrossRef
19.
Zurück zum Zitat Longo JPF et al (2016) Prevention of distant lung metastasis after photodynamic therapy application in a breast cancer tumor model. J Biomed Nanotechnol 12(4):689–699PubMedCrossRef Longo JPF et al (2016) Prevention of distant lung metastasis after photodynamic therapy application in a breast cancer tumor model. J Biomed Nanotechnol 12(4):689–699PubMedCrossRef
20.
Zurück zum Zitat Muehlmann LA et al (2015) Aluminium-phthalocyanine chloride nanoemulsions for anticancer photodynamic therapy: development and in vitro activity against monolayers and spheroids of human mammary adenocarcinoma MCF-7 cells. J Nanobiotechnology 13:36PubMedPubMedCentralCrossRef Muehlmann LA et al (2015) Aluminium-phthalocyanine chloride nanoemulsions for anticancer photodynamic therapy: development and in vitro activity against monolayers and spheroids of human mammary adenocarcinoma MCF-7 cells. J Nanobiotechnology 13:36PubMedPubMedCentralCrossRef
21.
Zurück zum Zitat Morgado LF et al (2017) Photodynamic Therapy treatment of onychomycosis with Aluminium-Phthalocyanine Chloride nanoemulsions: a proof of concept clinical trial. J Photochem Photobiol B 173:266–270PubMedCrossRef Morgado LF et al (2017) Photodynamic Therapy treatment of onychomycosis with Aluminium-Phthalocyanine Chloride nanoemulsions: a proof of concept clinical trial. J Photochem Photobiol B 173:266–270PubMedCrossRef
22.
Zurück zum Zitat Chan SW et al (2008) A role for TAZ in migration, invasion, and tumorigenesis of breast cancer cells. Cancer Res 68(8):2592–2598PubMedCrossRef Chan SW et al (2008) A role for TAZ in migration, invasion, and tumorigenesis of breast cancer cells. Cancer Res 68(8):2592–2598PubMedCrossRef
23.
Zurück zum Zitat Kasibhatla S et al (2006) Acridine Orange/Ethidium Bromide (AO/EB) staining to detect apoptosis. Cold Spring Harb Protoc 2006(3): pdb.prot4493 Kasibhatla S et al (2006) Acridine Orange/Ethidium Bromide (AO/EB) staining to detect apoptosis. Cold Spring Harb Protoc 2006(3): pdb.prot4493
24.
Zurück zum Zitat Santos EMS et al (2018) Gallic acid modulates phenotypic behavior and gene expression in oral squamous cell carcinoma cells by interfering with leptin pathway. Pathol Res Pract 214(1):30–37PubMedCrossRef Santos EMS et al (2018) Gallic acid modulates phenotypic behavior and gene expression in oral squamous cell carcinoma cells by interfering with leptin pathway. Pathol Res Pract 214(1):30–37PubMedCrossRef
26.
Zurück zum Zitat Fraga CA et al (2012) A high HIF-1alpha expression genotype is associated with poor prognosis of upper aerodigestive tract carcinoma patients. Oral Oncol 48(2):130–135PubMedCrossRef Fraga CA et al (2012) A high HIF-1alpha expression genotype is associated with poor prognosis of upper aerodigestive tract carcinoma patients. Oral Oncol 48(2):130–135PubMedCrossRef
27.
Zurück zum Zitat Fonseca-Silva T et al (2012) Analysis of p16(CDKN2A) methylation and HPV-16 infection in oral mucosal dysplasia. Pathobiology 79(2):94–100PubMedCrossRef Fonseca-Silva T et al (2012) Analysis of p16(CDKN2A) methylation and HPV-16 infection in oral mucosal dysplasia. Pathobiology 79(2):94–100PubMedCrossRef
28.
Zurück zum Zitat Pereira CS et al (2012) Impact of the epithelial dysplasia grading and Ki67 proliferation index in the adjacent non-malignant mucosa on recurrence and survival in head and neck squamous cell carcinoma. Pathol Res Pract 208(11):651–656PubMedCrossRef Pereira CS et al (2012) Impact of the epithelial dysplasia grading and Ki67 proliferation index in the adjacent non-malignant mucosa on recurrence and survival in head and neck squamous cell carcinoma. Pathol Res Pract 208(11):651–656PubMedCrossRef
29.
Zurück zum Zitat de Oliveira MV et al (2013) Prognostic value of microvessel density and p53 expression on the locoregional metastasis and survival of the patients with head and neck squamous cell carcinoma. Appl Immunohistochem Mol Morphol 21(5):444–451PubMedCrossRef de Oliveira MV et al (2013) Prognostic value of microvessel density and p53 expression on the locoregional metastasis and survival of the patients with head and neck squamous cell carcinoma. Appl Immunohistochem Mol Morphol 21(5):444–451PubMedCrossRef
30.
Zurück zum Zitat Barclay CW, Foster EC, Taylor CL (2018) Restorative aspects of oral cancer reconstruction. Br Dent J 225(9):848–854PubMedCrossRef Barclay CW, Foster EC, Taylor CL (2018) Restorative aspects of oral cancer reconstruction. Br Dent J 225(9):848–854PubMedCrossRef
31.
Zurück zum Zitat Muehlmann LA et al (2014) Aluminum-phthalocyanine chloride associated to poly(methyl vinyl ether-co-maleic anhydride) nanoparticles as a new third-generation photosensitizer for anticancer photodynamic therapy. Int J Nanomedicine 9:1199–1213PubMedPubMedCentralCrossRef Muehlmann LA et al (2014) Aluminum-phthalocyanine chloride associated to poly(methyl vinyl ether-co-maleic anhydride) nanoparticles as a new third-generation photosensitizer for anticancer photodynamic therapy. Int J Nanomedicine 9:1199–1213PubMedPubMedCentralCrossRef
32.
Zurück zum Zitat Castano AP, Demidova TN, Hamblin MR (2004) Mechanisms in photodynamic therapy: part one—-photosensitizers, photochemistry and cellular localization. Photodiagn Photodyn Ther 1(4):279–293CrossRef Castano AP, Demidova TN, Hamblin MR (2004) Mechanisms in photodynamic therapy: part one—-photosensitizers, photochemistry and cellular localization. Photodiagn Photodyn Ther 1(4):279–293CrossRef
34.
Zurück zum Zitat Justus CR et al (2014) In vitro cell migration and invasion assays. J Vis Exp: JoVE 88:51046 Justus CR et al (2014) In vitro cell migration and invasion assays. J Vis Exp: JoVE 88:51046
35.
Zurück zum Zitat Domingos PLB et al (2017) Hypoxia reduces the E-cadherin expression and increases OSCC cell migration regardless of the E-cadherin methylation profile. Pathol Res Pract 213(5):496–501PubMedCrossRef Domingos PLB et al (2017) Hypoxia reduces the E-cadherin expression and increases OSCC cell migration regardless of the E-cadherin methylation profile. Pathol Res Pract 213(5):496–501PubMedCrossRef
38.
Zurück zum Zitat Scholzen T, Gerdes J (2000) The Ki-67 protein: from the known and the unknown. J Cell Physiol 182(3):311–322PubMedCrossRef Scholzen T, Gerdes J (2000) The Ki-67 protein: from the known and the unknown. J Cell Physiol 182(3):311–322PubMedCrossRef
39.
Zurück zum Zitat Jing Y et al (2018) Higher Ki67 expression in fibroblast like cells at invasive front indicates better clinical outcomes in oral squamous cell carcinoma patients. Biosci Rep 38(6) Jing Y et al (2018) Higher Ki67 expression in fibroblast like cells at invasive front indicates better clinical outcomes in oral squamous cell carcinoma patients. Biosci Rep 38(6)
40.
Zurück zum Zitat Li C-F et al (2014) AMACR amplification and overexpression in primary imatinib-naïve gastrointestinal stromal tumors: a driver of cell proliferation indicating adverse prognosis. Oncotarget 5(22):11588–11603PubMedPubMedCentralCrossRef Li C-F et al (2014) AMACR amplification and overexpression in primary imatinib-naïve gastrointestinal stromal tumors: a driver of cell proliferation indicating adverse prognosis. Oncotarget 5(22):11588–11603PubMedPubMedCentralCrossRef
41.
Zurück zum Zitat Mohamed AA et al (2018) Assessment of expression of Ki-67 in benign and malignant prostatic lesions among sudanese patients. Open Access Maced J Med Sci 6(10):1809–1812PubMedPubMedCentralCrossRef Mohamed AA et al (2018) Assessment of expression of Ki-67 in benign and malignant prostatic lesions among sudanese patients. Open Access Maced J Med Sci 6(10):1809–1812PubMedPubMedCentralCrossRef
42.
Zurück zum Zitat Farias LC et al (2010) Effect of age on the association between p16CDKN2A methylation and DNMT3B polymorphism in head and neck carcinoma and patient survival. Int J Oncol 37(1):167–176PubMed Farias LC et al (2010) Effect of age on the association between p16CDKN2A methylation and DNMT3B polymorphism in head and neck carcinoma and patient survival. Int J Oncol 37(1):167–176PubMed
45.
Zurück zum Zitat Pinheiro UB et al (2015) Fuzzy clustering demonstrates that codon 72 SNP rs1042522 of TP53 gene associated with HNSCC but not with prognoses. Tumour Biol 36(12):9259–9265PubMedCrossRef Pinheiro UB et al (2015) Fuzzy clustering demonstrates that codon 72 SNP rs1042522 of TP53 gene associated with HNSCC but not with prognoses. Tumour Biol 36(12):9259–9265PubMedCrossRef
46.
Zurück zum Zitat Souza LR et al (2011) Immunohistochemical analysis of p53, APE1, hMSH2 and ERCC1 proteins in actinic cheilitis and lip squamous cell carcinoma. Histopathology 58(3):352–360PubMedCrossRef Souza LR et al (2011) Immunohistochemical analysis of p53, APE1, hMSH2 and ERCC1 proteins in actinic cheilitis and lip squamous cell carcinoma. Histopathology 58(3):352–360PubMedCrossRef
47.
Zurück zum Zitat Pereira T et al (2018) MicroRNA profiling reveals dysregulated microRNAs and their target gene regulatory networks in cemento-ossifying fibroma. J Oral Pathol Med 47(1):78–85PubMedCrossRef Pereira T et al (2018) MicroRNA profiling reveals dysregulated microRNAs and their target gene regulatory networks in cemento-ossifying fibroma. J Oral Pathol Med 47(1):78–85PubMedCrossRef
48.
Zurück zum Zitat Hientz K et al (2017) The role of p53 in cancer drug resistance and targeted chemotherapy. Oncotarget 8(5):8921–8946PubMedCrossRef Hientz K et al (2017) The role of p53 in cancer drug resistance and targeted chemotherapy. Oncotarget 8(5):8921–8946PubMedCrossRef
49.
Metadaten
Titel
Photodynamic therapy mediated by nanoparticles Aluminum Chloro Phthalocyanine in oral squamous carcinoma cells
verfasst von
Lilian Mendes Borburema Cangussu
Ludmilla Regina de Souza
Marcela Gonçalves de Souza
Renato Sobral Monteiro Junior
Luis Alexandre Muehlmann
Paulo Narcizo de Souza
Lucyana Conceição Farias
Sérgio Henrique Sousa Santos
Alfredo Maurício Batista de Paula
André Luiz Sena Guimarães
Publikationsdatum
04.02.2022
Verlag
Springer London
Erschienen in
Lasers in Medical Science / Ausgabe 5/2022
Print ISSN: 0268-8921
Elektronische ISSN: 1435-604X
DOI
https://doi.org/10.1007/s10103-022-03517-z

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