Transcriptional Regulation of the Colorectal Cancer Stem Cell Markers, Nanog and Oct4, Induced by a Thermodynamic-Based Therapy Approach
Abstract
Background: Cancer stem cells (CSC), as responsible issues to cancer development and progression, play a crucial role in tumorigenesis, recurrence, metastasis, and chemoresistance. Both hyperthermia and photodynamic therapy (PDT) may be effective for cancer treatment, particularly when combined with other therapeutic approaches. This study aimed to evaluate the effect of hyperthermia combined with PDT on colorectal CSC and the gene expression of the CSC markers, presenting a more effective approach for cancer therapy.
Methods: The study was conducted in the Pasteur institute of Iran, Tehran, Iran in 2018. We evaluated the anticancer role of hyperthermia, Gold nanoparticles coated with curcumin (Cur-GNPs) in PDT and combination of the two approaches on cell viability and the expression of CSC markers, Nanog and Oct4 in colorectal cancer cell line HT-29. The cytotoxicity effect of Cur-GNPs against the cells was assessed in vitro. The cell viability was assessed using MTT assay, and the expression analysis of the CSC genes was evaluated using a q-real-time PCR.
Results: Cell viability was decreased by PDT (P=0.015) and the combination therapy (P=0.006) but not by hyperthermia alone (P=0.4), compared to control. Also, the expression of CSC markers, Nanog and Oct4 was shown to significantly down-regulate in all hyperthermia, PDT and combination groups.
Conclusion: Hyperthermia combined with PDT was indicated to be more efficient in eliminating tumors than hyperthermia or PDT alone.
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16. Kalamida D, Karagounis IV, Mitrakas A, et al (2015). Fever-range hyperthermia vs. hypothermia effect on cancer cell viability, proliferation and HSP90 expression. PLoS One, 10(1):e0116021.
17. Hadi F, Tavakkol S, Laurent S, et al (2019). Combinatorial effects of radiofrequency hyperthermia and radiotherapy in the presence of magneto‐plasmonic nanoparticles on MCF‐7 breast cancer cells. J Cell Physiol, 234(11):20028-20035.
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21. Zhang Z-J, Wang K-P, Mo J-G, et al (2020). Photodynamic therapy regulates fate of cancer stem cells through reactive oxygen species. World J Stem Cells, 12(7):562-584.
22. Kazantzis K, Koutsonikoli K, Mavroidi B, et al (2020). Curcumin derivatives as photosensitizers in photodynamic therapy: photophysical properties and in vitro studies with prostate cancer cells. Photochem Photobiol Sci, 19(2):193-206.
23. Szlasa W, Supplitt S, Drąg-Zalesińska M, et al (2020). Effects of curcumin based PDT on the viability and the organization of actin in melanotic (A375) and amelanotic melanoma (C32)–in vitro studies. Biomed Pharmacother, 132:110883.
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26. Gao F, Ye Y, Zhang Y, et al (2013). Water bath hyperthermia reduces stemness of colon cancer cells. Clin Biochem, 46(16-17):1747-50.
27. Moyer HR, Delman KA. (2008). The role of hyperthermia in optimizing tumor response to regional therapy. Int J Hyperthermia, 24(3):251-261.
28. Chung H-J, Lee H-K, Kwon KB, et al (2018). Transferrin as a thermosensitizer in radiofrequency hyperthermia for cancer treatment. Sci Rep, 8(1):13505.
29. Pelicci PG, Dalton P, Orecchia R. (2011). Heating cancer stem cells to reduce tumor relapse. Breast Cancer Res, 13(3):305.
30. Lin F-C, Hsu C-H, Lin Y-Y. (2018). Nano-therapeutic cancer immunotherapy using hyperthermia-induced heat shock proteins: insights from mathematical modeling. Int J Nanomedicine, 13:3529-3539.
31. El-Daly SM, Abba ML, Gamal-Eldeen AM. (2017). The role of microRNAs in photodynamic therapy of cancer. Eur J Med Chem, 142:550-555.
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33. Shen Y-A, Lin C-H, Chi W-H, et al (2013). Resveratrol impedes the stemness, epithelial-mesenchymal transition, and metabolic reprogramming of cancer stem cells in nasopharyngeal carcinoma through p53 activation. Evid Based Complement Alternat Med, 2013: 590393.
34. Li H, Zhang J, Tong JHM, et al (2019). Targeting the oncogenic p53 mutants in colorectal cancer and other solid tumors. Int J Mol Sci, 20(23):5999.
35. Yang B, Liu H, Yang H, et al (2019). Combinatorial photochemotherapy on liver cancer stem cells with organoplatinum (ii) metallacage-based nanoparticles. J Mater Chem B, 7(42):6476-6487.
36. de Faria CM, Costa CS, Bagnato VS, et al (2021). Photobiomodulation effects on photodynamic therapy in HNSCC cell lines. J Photochem Photobiol B, 217:112170.
37. Galiardi-Campoy AEB, Machado FC, Carvalho T, et al (2021). Effects of photodynamic therapy mediated by emodin in cervical carcinoma cells. Photodiagnosis Photodyn Ther, 35: 102394.
38. Kurokawa H, Ito H, Terasaki M, et al (2019). Hyperthermia enhances photodynamic therapy by regulation of HCP1 and ABCG2 expressions via high level ROS generation. Sci Rep, 9(1):1638.
39. Xu J, Gao J, Wei QJ. (2016). Combination of photodynamic therapy with radiotherapy for cancer treatment. J Nanomater, 2016: 8507924.
40. Lu C-H, Kuo Y-Y, Lin G-B, et al (2020). Application of non-invasive low-intensity pulsed electric field with thermal cycling-hyperthermia for synergistically enhanced anticancer effect of chlorogenic acid on PANC-1 cells. PLoS One, 15(1):e0222126.
41. Noghreiyan AV, Imanparast A, Ara ES, et al (2020). In-vitro investigation of cold atmospheric plasma induced photodynamic effect by Indocyanine green and Protoporphyrin IX. Photodiagnosis Photodyn Ther, 31:101822.
2. Emami SS, Akbari A, Zare A-A, et al (2019). MicroRNA expression levels and histopathological features of colorectal cancer. J Gastrointest Cancer, 50(2):276-284.
3. Rawla P, Sunkara T, Barsouk A. (2019). Epidemiology of colorectal cancer: incidence, mortality, survival, and risk factors. Prz Gastroenterol, 14(2):89-103.
4. Takimoto R, Kamigaki T, Okada S, et al (2019). Prognostic factors for colorectal cancer patients treated with combination of immune-cell therapy and first-line chemotherapy: A retrospective study. Anticancer Res, 39(8):4525-4532.
5. Kim J-E, Shin J-Y, Cho M-H. (2012). Magnetic nanoparticles: an update of application for drug delivery and possible toxic effects. Arch Toxicol, 86(5):685-700.
6. Medema JP (2013). Cancer stem cells: the challenges ahead. Nat Cell Biol, 15(4):338-44.
7. Akbari A, Farahnejad Z, Akhtari J, et al (2016). Staphylococcus aureus enterotoxin B down-regulates the expression of transforming growth factor-beta (TGF-β) signaling transducers in human glioblastoma. Jundishapur J Microbiol, 9(5): e27297.
8. Cojoc M, Mäbert K, Muders MH, et al, (2015). A role for cancer stem cells in therapy resistance: cellular and molecular mechanisms. Semin Cancer Biol, 31:16-27.
9. Zhu P, Fan Z. (2018). Cancer stem cells and tumorigenesis. Biophys Rep, 4(4):178-188.
10. Kolosnjaj-Tabi J, Wilhelm C. (2017). Magnetic nanoparticles in cancer therapy: how can thermal approaches help? Nanomedicine (Lond), 12(6):573-575.
11. Mobini GR., Ghahremani MH, Amanpour S, et al (2016). Transforming growth factor beta-induced factor 2-linked X (TGIF2LX) regulates two morphogenesis genes, Nir1 and Nir2 in human colorectal. Acta Med Iran, 54(5):302-7.
12. Rentsch M, Schiergens T, Khandoga A, et al (2016). Surgery for Colorectal Cancer-Trends, Developments, and Future Perspectives. Visc Med, 32(3):184-191.
13. Song X, Kim HC, Kim SY, et al (2012). Hyperthermia‐enhanced TRAIL‐and mapatumumab‐induced apoptotic death is mediated through mitochondria in human colon cancer cells. J Cell Biochem, 113(5):1547-1558.
14. Lutgens L, van der Zee J, Pijls‐Johannesma M, et al (2010). Combined use of hyperthermia and radiation therapy for treating locally advanced cervix carcinoma. Cochrane Database Syst Rev, 2010(3):CD006377.
15. Sadhukha T, Niu L, Wiedmann TS, et al (2013). Effective elimination of cancer stem cells by magnetic hyperthermia. Mol Pharm, 10(4):1432-1441.
16. Kalamida D, Karagounis IV, Mitrakas A, et al (2015). Fever-range hyperthermia vs. hypothermia effect on cancer cell viability, proliferation and HSP90 expression. PLoS One, 10(1):e0116021.
17. Hadi F, Tavakkol S, Laurent S, et al (2019). Combinatorial effects of radiofrequency hyperthermia and radiotherapy in the presence of magneto‐plasmonic nanoparticles on MCF‐7 breast cancer cells. J Cell Physiol, 234(11):20028-20035.
18. Agostinis P, Berg K, Cengel KA, et al (2011). Photodynamic therapy of cancer: an update. CA Cancer J Clin, 61(4):250-281.
19. dos Santos AlF, de Almeida DRQ, Terra LF, et al (2019). Photodynamic therapy in cancer treatment-an update review. J Cancer Metastasis Treat, 5:25.
20. Kwiatkowski S, Knap B, Przystupski D, et al (2018). Photodynamic therapy–mechanisms, photosensitizers and combinations. Biomed Pharmacother, 106:1098-1107.
21. Zhang Z-J, Wang K-P, Mo J-G, et al (2020). Photodynamic therapy regulates fate of cancer stem cells through reactive oxygen species. World J Stem Cells, 12(7):562-584.
22. Kazantzis K, Koutsonikoli K, Mavroidi B, et al (2020). Curcumin derivatives as photosensitizers in photodynamic therapy: photophysical properties and in vitro studies with prostate cancer cells. Photochem Photobiol Sci, 19(2):193-206.
23. Szlasa W, Supplitt S, Drąg-Zalesińska M, et al (2020). Effects of curcumin based PDT on the viability and the organization of actin in melanotic (A375) and amelanotic melanoma (C32)–in vitro studies. Biomed Pharmacother, 132:110883.
24. Tiwari PM, Vig K, Dennis VA, et al (2011). Functionalized gold nanoparticles and their biomedical applications. Nanomaterials (Basel), 1(1):31-63.
25. Shaabani E, Amini SM, Kharrazi S, et al (2017). Curcumin coated gold nanoparticles: synthesis, characterization, cytotoxicity, antioxidant activity and its comparison with citrate coated gold nanoparticles. Nanomed J, 4(2):115-125.
26. Gao F, Ye Y, Zhang Y, et al (2013). Water bath hyperthermia reduces stemness of colon cancer cells. Clin Biochem, 46(16-17):1747-50.
27. Moyer HR, Delman KA. (2008). The role of hyperthermia in optimizing tumor response to regional therapy. Int J Hyperthermia, 24(3):251-261.
28. Chung H-J, Lee H-K, Kwon KB, et al (2018). Transferrin as a thermosensitizer in radiofrequency hyperthermia for cancer treatment. Sci Rep, 8(1):13505.
29. Pelicci PG, Dalton P, Orecchia R. (2011). Heating cancer stem cells to reduce tumor relapse. Breast Cancer Res, 13(3):305.
30. Lin F-C, Hsu C-H, Lin Y-Y. (2018). Nano-therapeutic cancer immunotherapy using hyperthermia-induced heat shock proteins: insights from mathematical modeling. Int J Nanomedicine, 13:3529-3539.
31. El-Daly SM, Abba ML, Gamal-Eldeen AM. (2017). The role of microRNAs in photodynamic therapy of cancer. Eur J Med Chem, 142:550-555.
32. Ozsvari B, Sotgia F, Lisanti MP. (2017). A new mutation-independent approach to cancer therapy: Inhibiting oncogenic RAS and MYC, by targeting mitochondrial biogenesis. Aging (Albany NY), 9(10):2098-2116.
33. Shen Y-A, Lin C-H, Chi W-H, et al (2013). Resveratrol impedes the stemness, epithelial-mesenchymal transition, and metabolic reprogramming of cancer stem cells in nasopharyngeal carcinoma through p53 activation. Evid Based Complement Alternat Med, 2013: 590393.
34. Li H, Zhang J, Tong JHM, et al (2019). Targeting the oncogenic p53 mutants in colorectal cancer and other solid tumors. Int J Mol Sci, 20(23):5999.
35. Yang B, Liu H, Yang H, et al (2019). Combinatorial photochemotherapy on liver cancer stem cells with organoplatinum (ii) metallacage-based nanoparticles. J Mater Chem B, 7(42):6476-6487.
36. de Faria CM, Costa CS, Bagnato VS, et al (2021). Photobiomodulation effects on photodynamic therapy in HNSCC cell lines. J Photochem Photobiol B, 217:112170.
37. Galiardi-Campoy AEB, Machado FC, Carvalho T, et al (2021). Effects of photodynamic therapy mediated by emodin in cervical carcinoma cells. Photodiagnosis Photodyn Ther, 35: 102394.
38. Kurokawa H, Ito H, Terasaki M, et al (2019). Hyperthermia enhances photodynamic therapy by regulation of HCP1 and ABCG2 expressions via high level ROS generation. Sci Rep, 9(1):1638.
39. Xu J, Gao J, Wei QJ. (2016). Combination of photodynamic therapy with radiotherapy for cancer treatment. J Nanomater, 2016: 8507924.
40. Lu C-H, Kuo Y-Y, Lin G-B, et al (2020). Application of non-invasive low-intensity pulsed electric field with thermal cycling-hyperthermia for synergistically enhanced anticancer effect of chlorogenic acid on PANC-1 cells. PLoS One, 15(1):e0222126.
41. Noghreiyan AV, Imanparast A, Ara ES, et al (2020). In-vitro investigation of cold atmospheric plasma induced photodynamic effect by Indocyanine green and Protoporphyrin IX. Photodiagnosis Photodyn Ther, 31:101822.
| Files | ||
| Issue | Vol 52 No 4 (2023) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijph.v52i4.12458 | |
| Keywords | ||
| Colorectal cancer stem cell Nanog Hyperthermia Photodynamic therapy | ||
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How to Cite
1.
Ghorbani Z, Heidari M, Jafarinia M, Rohani M, Akbari A. Transcriptional Regulation of the Colorectal Cancer Stem Cell Markers, Nanog and Oct4, Induced by a Thermodynamic-Based Therapy Approach. Iran J Public Health. 2023;52(4):848-856.
