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Effect of human dental pulp derived mesenchymal stem cells on breast cancer stem cells

Year 2023, , 396 - 405, 18.09.2023

Gizem İnetaş Yengin , Öykü Gönül Geyik Hüsnü Alper Bağrıyanık Zeynep Yüce , Gülperi Öktem

https://doi.org/10.19161/etd.1360783

Abstract

Aim: Cancer stem cells are cells that can renew themselves, have a high differentiation capacity and have the ability to invade normal tissue with long-term proliferation. With these abilities, it plays a role in tumor growth and metastasis by creating resistance to traditional cancer treatment. It is important to conduct research on cancer stem cell mechanisms for successful cancer treatments. The aim of this study is to investigate the effects of human dental pulp-derived mesenchymal stem cells on breast cancer stem cells by cell viability, cell cycle and apoptosis methods.
Materials and Methods: Breast cancer cells (MCF7) were separated by flow cytometry with CD44+/CD24- staining. The CD44+/CD24- population was called breast cancer stem cells. Mesenchymal stem cells isolated from dental pulp were cultured and characterized. Mesenchymal stem cell group was labeled with mCitrine and breast cancer stem cell group with mCherry by plasmid transfection. These cells were co-cultured for 48 hours and then cell proliferation, cell cycle and apoptosis analyzes were performed.
Results: Statistically significant changes were observed in cell viability, cell cycle and apoptosis values of breast cancer stem cells co-cultured with dental pulp-derived mesenchymal stem cells compared to the control group over time. When the co-culture group was compared to the control, an increase in the G0/G1 stage was observed depending on time. Yellow fluorescent-labeled hybrid cells were observed in the examination of co-cultured cells with fluorescent microscope, and a decrease in cell number was observed in immunofluorescent Ki67 staining.
Conclusion: When mesenchymal stem cells from dental pulp were co-cultured with breast cancer stem cells, an increase in the G0/G1 stage of breast cancer stem cells was observed depending on time. After co-culture, it has been observed that dental pulp-derived mesenchymal stem cells have cell proliferation inhibitory effects on breast cancer stem cells and promote apoptosis. In conclusion, dental pulp derived mesenchymal stem cells may have a therapeutic effect on breast cancer stem cells.

Keywords

Breast cancer cancer stem cell mesenchymal stem cell dental pulp stem cell co-culture.

References

  • Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, et al. Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries. CA: A Cancer Journal for Clinicians [Internet]. 2021 Feb 4;71(3):209–49.
  • Siegel RL, Miller KD, Jemal A. Cancer statistics, 2017. CA: A Cancer Journal for Clinicians. 2017 Jan;67(1):7–30.
  • Şencan, İ., & Keskinkılıç, B. Türkiye kanser istatistikleri. TC Sağlık Bakanlığı Türkiye Halk Sağlığı Kurumu, 2017; 19-44.
  • Korkaya H, Liu S, Wicha MS. Breast cancer stem cells, cytokine networks, and the tumor microenvironment. Journal of Clinical Investigation. 2011 Oct 3;121(10):3804–9.
  • Ridge SM, Sullivan FJ, Glynn SA. Mesenchymal stem cells: key players in cancer progression. Molecular Cancer [Internet]. 2017 Feb 1;16(1).
  • Batlle E, Clevers H. Cancer stem cells revisited. Nature medicine [Internet]. 2017 [cited 2019 Oct 15];23(10):1124–34.
  • Balkwill FR, Capasso M, Hagemann T. The tumor microenvironment at a glance. Journal of Cell Science. 2012 Dec 1;125(23):5591–6.
  • Mimeault M, Hauke R, Mehta PP, Batra SK. Recent advances in cancer stem/progenitor cell research: therapeutic implications for overcoming resistance to the most aggressive cancers. Journal of Cellular and Molecular Medicine. 2007 Sep;11(5):981–1011.
  • Abugomaa A, Elbadawy M. Patient-derived organoid analysis of drug resistance in precision medicine: is there a value? Expert Review of Precision Medicine and Drug Development. 2020 Jan 2;5(1):1–5.
  • Hass R, Kasper C, Böhm S, Jacobs R. Different populations and sources of human mesenchymal stem cells (MSC): A comparison of adult and neonatal tissue-derived MSC. Cell Communication and Signaling. 2011 May 14;9(1).
  • Heldring N, Mäger I, Wood MJA, Le Blanc K, Andaloussi SEL. Therapeutic Potential of Multipotent Mesenchymal Stromal Cells and Their Extracellular Vesicles. Human Gene Therapy [Internet]. 2015 Aug;26(8):506–17
  • Karnoub AE, Dash AB, Vo AP, Sullivan A, Brooks MW, Bell GW, et al. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature. 2007 Oct;449(7162):557–63.
  • López de Andrés J, Griñán-Lisón C, Jiménez G, Marchal JA. Cancer stem cell secretome in the tumor microenvironment: a key point for an effective personalized cancer treatment. Journal of Hematology & Oncology. 2020 Oct 15;13(1).
  • Liang W, Chen X, Zhang S, Fang J, Chen M, Xu Y, et al. Mesenchymal stem cells as a double-edged sword in tumor growth: focusing on MSC-derived cytokines. Cellular & Molecular Biology Letters. 2021 Jan 20;26(1).
  • Bartosh TJ, Ullah M, Zeitouni S, Beaver J, Prockop DJ. Cancer cells enter dormancy after cannibalizing mesenchymal stem/stromal cells (MSCs). Proceedings of the National Academy of Sciences. 2016 Oct 3;113(42):E6447–56.
  • Luo M, Brooks M, Wicha M. Epithelial-Mesenchymal Plasticity of Breast Cancer Stem Cells: Implications for Metastasis and Therapeutic Resistance. Current Pharmaceutical Design. 2015 Feb 3;21(10):1301–10
  • Patil VR, Kharat AH, Kulkarni DG, Kheur SM, Bhonde RR. Long term explant culture for harvesting homogeneous population of human dental pulp stem cells. Cell Biology International. 2018 Nov 22;42(12):1602–10.
  • Nakashima M, Iohara K, Murakami M. Dental pulp stem cells and regeneration. Endodontic Topics. 2013 Mar;28(1):38–50.
  • Gronthos S, Mankani M, Brahim J, Robey PG, Shi S. Postnatal human dental pulp stem cells (DPSCs) in vitro and invivo. Proceedings of the National Academy of Sciences. 2000 Nov 21;97(25):13625–30.
  • Doğan A, Demirci S, Apdik H, Apdik EA, Şahin F. Dental pulp stem cells (DPSCs) increase prostate cancer cell proliferation and migration under in vitro conditions. Tissue and Cell. 2017 Dec;49(6):711–8
  • Nikkhah E, Kalalinia F, Asgharian Rezaee M, Tayarani-Najaran Z. Suppressive effects of dental pulp stem cells and its conditioned medium on development and migration of colorectal cancer cells through MAPKinase pathways. Iranian journal of basic medical sciences [Internet]. 2021;24(9):1292–300.
  • Merckx G, Lo Monaco M, Lambrichts I, Himmelreich U, Bronckaers A, Wolfs E. Safety and Homing of Human Dental Pulp Stromal Cells in Head and Neck Cancer. Stem Cell Reviews and Reports [Internet]. 2021 Oct 1;17(5):1619–34.
  • Borensztejn K, Tyrna P, Gaweł AM, Dziuba I, Wojcik C, Bialy LP, et al. Classification of Cell-in-Cell Structures: Different Phenomena with Similar Appearance. Cells [Internet]. 2021 Sep 28;10(10):2569.
  • Fais S, Overholtzer M. Cell-in-cell phenomena in cancer. Nature Reviews Cancer. 2018 Nov 12;18(12):758–66.
  • Durgan J, Florey O. Cancer cell cannibalism: Multiple triggers emerge for entosis. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research. 2018 Jun;1865(6):831–41
  • Wang X, Li Y, Li J, Li L, Zhu H, Chen H, et al. Cell-in-Cell Phenomenon and Its Relationship With Tumor Microenvironment and Tumor Progression: A Review. Frontiers in Cell and Developmental Biology. 2019 Dec 3;7
  • Sharma N, Dey P. Cell cannibalism and cancer. Diagnostic Cytopathology. 2010; 39(3), 229-233
  • Durgan J, Tseng Y-Y, Hamann JC, Domart M-C, Collinson L, Hall A, et al. Mitosis can drive cell cannibalism through entosis. Yap A, editor. eLife [Internet]. 2017 Jul 11;6:e27134.
  • Raoof M, Yaghoobi MM, Derakhshani A, Kamal-Abadi AM, Ebrahimi B, Abbasnejad M, et al. A modified efficient method for dental pulp stem cell isolation. Dental research journal [Internet]. 2014;11(2):244–50.
  • Al Madhoun A, Sindhu S, Haddad D, Atari M, Ahmad R, Al-Mulla F. Dental Pulp Stem Cells Derived From Adult Human Third Molar Tooth: A Brief Review. Frontiers in Cell and Developmental Biology [Internet]. 2021 Oct 12;9:717624.
  • Alsulaimani RS, Ajlan SA, Aldahmash AM, Alnabaheen MS, Ashri NY. Isolation of dental pulp stem cells from a single donor and characterization of their ability to differentiate after 2 years of cryopreservation. Saudi Medical Journal [Internet]. 2016 May;37(5):551–60.
  • Al-Habib M, Huang GT-J . Dental Mesenchymal Stem Cells: Dental Pulp Stem Cells, Periodontal Ligament Stem Cells, Apical Papilla Stem Cells, and Primary Teeth Stem Cells-Isolation, Characterization, and Expansion for Tissue Engineering. Methods in Molecular Biology (Clifton, NJ) [Internet]. 2019;1922:59–76.
  • Wang W, Zhang L, Wang Y, Ding Y, Chen T, Wang Y, et al. Involvement of miR-451 in resistance to paclitaxel by regulating YWHAZ in breast cancer. Cell Death & Disease [Internet]. 2017 Oct 1;8(10):e3071–1.
  • Akekawatchai C, Roytrakul S, Phaonakrop N, Jaresitthikunchai J, Jitrapakdee S. Proteomic Analysis of the Anoikis-Resistant Human Breast Cancer Cell Lines. Methods in Molecular Biology (Clifton, NJ) [Internet]. 2020;2138:185–93.
  • Kolf CM, Cho E, Tuan RS. Mesenchymal stromal cells: biology of adult mesenchymal stem cells: regulation of niche, self-renewal and differentiation. Arthritis Research & Therapy. 2007;9(1):204.
  • Margiana R, Markov A, Zekiy AO, Hamza MU, Al-Dabbagh KA, Al-Zubaidi SH, et al. Clinical application of mesenchymal stem cell in regenerative medicine: a narrative review. Stem Cell Research & Therapy. 2022 Jul 28;13(1).
  • Deo D, Marchioni M, Rao P. Mesenchymal Stem/Stromal Cells in Organ Transplantation. Pharmaceutics [Internet]. 2022 Apr 1 [cited 2023 Feb 20];14(4):791.
  • Ledesma-Martínez E, Mendoza-Núñez VM, Santiago-Osorio E. Mesenchymal Stem Cells Derived from Dental Pulp: A Review. Stem Cells International. 2016;2016:1–12.
  • Liu S, Ginestier C, Ou SJ, Clouthier SG, Patel SH, Monville F, et al. Breast Cancer Stem Cells Are Regulated by Mesenchymal Stem Cells through Cytokine Networks. Cancer Research. 2011 Jan 11;71(2):614–2
  • Qiao L, Xu Z, Zhao T, Ye L, Zhang X. Dkk-1 secreted by mesenchymal stem cells inhibits growth of breast cancer cells via depression of Wnt signalling. Cancer Letters. 2008 Sep;269(1):67–77.
  • Mandel K, Yang Y, Schambach A, Glage S, Otte A, Hass R. Mesenchymal Stem Cells Directly Interact with Breast Cancer Cells and Promote Tumor Cell Growth In Vitro and In Vivo. Stem Cells and Development. 2013 Dec;22(23):3114–27.
  • Casson J, Davies OG, Smith C-A, Dalby MJ, Berry CC. Mesenchymal stem cell-derived extracellular vesicles may promote breast cancer cell dormancy. Journal of Tissue Engineering. 2018 Jan;9:204173141881009.
  • Melzer C, von der Ohe J, Luo T, Hass R. Spontaneous Fusion of MSC with Breast Cancer Cells Can Generate Tumor Dormancy. International Journal of Molecular Sciences [Internet]. 2021 May 31;22(11):5930
  • Ramasamy R, Lam EW-F, Soeiro I, Tisato V, Bonnet D, Dazzi F. Mesenchymal stem cells inhibit proliferation and apoptosis of tumor cells: impact on in vivo tumor growth. Leukemia. 2006 Dec 14;21(2):304–10.
  • Gilazieva Z, Ponomarev A, Rizvanov A, Solovyeva V. The Dual Role of Mesenchymal Stromal Cells and Their Extracellular Vesicles in Carcinogenesis. Biology [Internet]. 2022 May 25;11(6):813
  • Li X, Fan Q, Peng X, Yang S, Wei S, Liu J, et al. Mesenchymal/stromal stem cells: necessary factors in tumour progression. Cell Death Discovery [Internet]. 2022 Jul 22;8(1):333

İnsan diş pulpası kaynaklı mezenkimal kök hücrelerin meme kanseri kök hücreleri üzerine etkisi

Year 2023, , 396 - 405, 18.09.2023

Gizem İnetaş Yengin , Öykü Gönül Geyik Hüsnü Alper Bağrıyanık Zeynep Yüce , Gülperi Öktem

https://doi.org/10.19161/etd.1360783

Abstract

Amaç: Kanser kök hücreleri; kendini yenileyebilen, farklılaşma kapasitesi yüksek ve uzun süreli proliferasyon ile normal dokuya invazyon kabiliyeti olan hücrelerdir. Bu yetenekleriyle geleneksel kanser tedavisine direnç oluşturarak tümör büyümesi ve metastazda rol oynar. Başarılı kanser tedavileri için kanser kök hücre mekanizmalarına yönelik araştırmalar yapmak önem taşımaktadır. Bu çalışmanın amacı, insan diş pulpası kaynaklı mezenkimal kök hücrelerin meme kanseri kök hücreleri üzerine etkisinin hücre canlılığı, hücre döngüsü ve apoptoz yöntemleriyle araştırılmasıdır.
Gereç ve Yöntem: Meme kanseri hücreleri (MCF7) akış sitometrisi ile CD44+/CD24- boyaması yapılarak ayrılmıştır. CD44+/CD24- popülasyonuna meme kanseri kök hücresi denilmiştir. Diş pulpasından izole edilen mezenkimal kök hücreler kültüre edilip karakterizasyonu yapılmıştır. Mezenkimal kök hücre grubu mCitrine, meme kanseri kök hücresi grubu ise mCherry ile plazmit transfeksiyonu yapılarak işaretlenmiştir. Bu hücreler 48 saat boyunca ko-kültüre edilmiş ve sonrasında hücre canlılığı, hücre döngüsü ve apoptoz analizleri yapılmıştır.
Bulgular: Diş pulpası kaynaklı mezenkimal kök hücreler ile ko-kültüre edilen meme kanseri kök hücrelerinin kontrol grubuna göre hücre canlılığı, hücre döngüsü ve apoptoz değerlerinde zamana bağlı olarak istatistiksel anlamlı değişiklikler görülmüştür. Ko-kültüre grubu kontrole göre kıyaslandığında zamana bağlı olarak G0/G1 evresinde artış gözlenmiştir. Ko-kültüre edilen hücrelerin floresan mikroskop ile yapılan incelemesinde sarı floresan işaretli hibrit hücreler gözlenmiştir ve immüno-floresan Ki67 boyamasında hücre sayısında azalma gözlenmiştir.
Sonuç: Ko-kültür sonrası diş pulpası kaynaklı mezenkimal kök hücrelerin meme kanser kök hücreleri üzerinde hücre proliferasyonunu inhibe edici etkileri olduğu ve apoptozu teşvik ettiği gözlenmiştir. Sonuç olarak, meme kanser kök hücreleri üzerinde diş pulpası kaynaklı mezenkimal kök hücrelerin tedaviye yönelik bir etkisi olabilir.

Keywords

Meme kanseri kanser kök hücresi mezenkimal kök hücre diş pulpası kök hücresi ko-kültür.

Thanks

Çalışma, Ege Üniversitesi Bilimsel Araştırma Projeleri Koordinasyon Birimi TYL-2019-20624 numaralı proje kapsamında desteklenmiştir. Çalışmada dental pulpa temini katkılarından dolayı Dr. Dt. İlkay Aydoğdu ve Doç.Dr. Onur Şahin’e teşekkür ederiz.

References

  • Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, et al. Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries. CA: A Cancer Journal for Clinicians [Internet]. 2021 Feb 4;71(3):209–49.
  • Siegel RL, Miller KD, Jemal A. Cancer statistics, 2017. CA: A Cancer Journal for Clinicians. 2017 Jan;67(1):7–30.
  • Şencan, İ., & Keskinkılıç, B. Türkiye kanser istatistikleri. TC Sağlık Bakanlığı Türkiye Halk Sağlığı Kurumu, 2017; 19-44.
  • Korkaya H, Liu S, Wicha MS. Breast cancer stem cells, cytokine networks, and the tumor microenvironment. Journal of Clinical Investigation. 2011 Oct 3;121(10):3804–9.
  • Ridge SM, Sullivan FJ, Glynn SA. Mesenchymal stem cells: key players in cancer progression. Molecular Cancer [Internet]. 2017 Feb 1;16(1).
  • Batlle E, Clevers H. Cancer stem cells revisited. Nature medicine [Internet]. 2017 [cited 2019 Oct 15];23(10):1124–34.
  • Balkwill FR, Capasso M, Hagemann T. The tumor microenvironment at a glance. Journal of Cell Science. 2012 Dec 1;125(23):5591–6.
  • Mimeault M, Hauke R, Mehta PP, Batra SK. Recent advances in cancer stem/progenitor cell research: therapeutic implications for overcoming resistance to the most aggressive cancers. Journal of Cellular and Molecular Medicine. 2007 Sep;11(5):981–1011.
  • Abugomaa A, Elbadawy M. Patient-derived organoid analysis of drug resistance in precision medicine: is there a value? Expert Review of Precision Medicine and Drug Development. 2020 Jan 2;5(1):1–5.
  • Hass R, Kasper C, Böhm S, Jacobs R. Different populations and sources of human mesenchymal stem cells (MSC): A comparison of adult and neonatal tissue-derived MSC. Cell Communication and Signaling. 2011 May 14;9(1).
  • Heldring N, Mäger I, Wood MJA, Le Blanc K, Andaloussi SEL. Therapeutic Potential of Multipotent Mesenchymal Stromal Cells and Their Extracellular Vesicles. Human Gene Therapy [Internet]. 2015 Aug;26(8):506–17
  • Karnoub AE, Dash AB, Vo AP, Sullivan A, Brooks MW, Bell GW, et al. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature. 2007 Oct;449(7162):557–63.
  • López de Andrés J, Griñán-Lisón C, Jiménez G, Marchal JA. Cancer stem cell secretome in the tumor microenvironment: a key point for an effective personalized cancer treatment. Journal of Hematology & Oncology. 2020 Oct 15;13(1).
  • Liang W, Chen X, Zhang S, Fang J, Chen M, Xu Y, et al. Mesenchymal stem cells as a double-edged sword in tumor growth: focusing on MSC-derived cytokines. Cellular & Molecular Biology Letters. 2021 Jan 20;26(1).
  • Bartosh TJ, Ullah M, Zeitouni S, Beaver J, Prockop DJ. Cancer cells enter dormancy after cannibalizing mesenchymal stem/stromal cells (MSCs). Proceedings of the National Academy of Sciences. 2016 Oct 3;113(42):E6447–56.
  • Luo M, Brooks M, Wicha M. Epithelial-Mesenchymal Plasticity of Breast Cancer Stem Cells: Implications for Metastasis and Therapeutic Resistance. Current Pharmaceutical Design. 2015 Feb 3;21(10):1301–10
  • Patil VR, Kharat AH, Kulkarni DG, Kheur SM, Bhonde RR. Long term explant culture for harvesting homogeneous population of human dental pulp stem cells. Cell Biology International. 2018 Nov 22;42(12):1602–10.
  • Nakashima M, Iohara K, Murakami M. Dental pulp stem cells and regeneration. Endodontic Topics. 2013 Mar;28(1):38–50.
  • Gronthos S, Mankani M, Brahim J, Robey PG, Shi S. Postnatal human dental pulp stem cells (DPSCs) in vitro and invivo. Proceedings of the National Academy of Sciences. 2000 Nov 21;97(25):13625–30.
  • Doğan A, Demirci S, Apdik H, Apdik EA, Şahin F. Dental pulp stem cells (DPSCs) increase prostate cancer cell proliferation and migration under in vitro conditions. Tissue and Cell. 2017 Dec;49(6):711–8
  • Nikkhah E, Kalalinia F, Asgharian Rezaee M, Tayarani-Najaran Z. Suppressive effects of dental pulp stem cells and its conditioned medium on development and migration of colorectal cancer cells through MAPKinase pathways. Iranian journal of basic medical sciences [Internet]. 2021;24(9):1292–300.
  • Merckx G, Lo Monaco M, Lambrichts I, Himmelreich U, Bronckaers A, Wolfs E. Safety and Homing of Human Dental Pulp Stromal Cells in Head and Neck Cancer. Stem Cell Reviews and Reports [Internet]. 2021 Oct 1;17(5):1619–34.
  • Borensztejn K, Tyrna P, Gaweł AM, Dziuba I, Wojcik C, Bialy LP, et al. Classification of Cell-in-Cell Structures: Different Phenomena with Similar Appearance. Cells [Internet]. 2021 Sep 28;10(10):2569.
  • Fais S, Overholtzer M. Cell-in-cell phenomena in cancer. Nature Reviews Cancer. 2018 Nov 12;18(12):758–66.
  • Durgan J, Florey O. Cancer cell cannibalism: Multiple triggers emerge for entosis. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research. 2018 Jun;1865(6):831–41
  • Wang X, Li Y, Li J, Li L, Zhu H, Chen H, et al. Cell-in-Cell Phenomenon and Its Relationship With Tumor Microenvironment and Tumor Progression: A Review. Frontiers in Cell and Developmental Biology. 2019 Dec 3;7
  • Sharma N, Dey P. Cell cannibalism and cancer. Diagnostic Cytopathology. 2010; 39(3), 229-233
  • Durgan J, Tseng Y-Y, Hamann JC, Domart M-C, Collinson L, Hall A, et al. Mitosis can drive cell cannibalism through entosis. Yap A, editor. eLife [Internet]. 2017 Jul 11;6:e27134.
  • Raoof M, Yaghoobi MM, Derakhshani A, Kamal-Abadi AM, Ebrahimi B, Abbasnejad M, et al. A modified efficient method for dental pulp stem cell isolation. Dental research journal [Internet]. 2014;11(2):244–50.
  • Al Madhoun A, Sindhu S, Haddad D, Atari M, Ahmad R, Al-Mulla F. Dental Pulp Stem Cells Derived From Adult Human Third Molar Tooth: A Brief Review. Frontiers in Cell and Developmental Biology [Internet]. 2021 Oct 12;9:717624.
  • Alsulaimani RS, Ajlan SA, Aldahmash AM, Alnabaheen MS, Ashri NY. Isolation of dental pulp stem cells from a single donor and characterization of their ability to differentiate after 2 years of cryopreservation. Saudi Medical Journal [Internet]. 2016 May;37(5):551–60.
  • Al-Habib M, Huang GT-J . Dental Mesenchymal Stem Cells: Dental Pulp Stem Cells, Periodontal Ligament Stem Cells, Apical Papilla Stem Cells, and Primary Teeth Stem Cells-Isolation, Characterization, and Expansion for Tissue Engineering. Methods in Molecular Biology (Clifton, NJ) [Internet]. 2019;1922:59–76.
  • Wang W, Zhang L, Wang Y, Ding Y, Chen T, Wang Y, et al. Involvement of miR-451 in resistance to paclitaxel by regulating YWHAZ in breast cancer. Cell Death & Disease [Internet]. 2017 Oct 1;8(10):e3071–1.
  • Akekawatchai C, Roytrakul S, Phaonakrop N, Jaresitthikunchai J, Jitrapakdee S. Proteomic Analysis of the Anoikis-Resistant Human Breast Cancer Cell Lines. Methods in Molecular Biology (Clifton, NJ) [Internet]. 2020;2138:185–93.
  • Kolf CM, Cho E, Tuan RS. Mesenchymal stromal cells: biology of adult mesenchymal stem cells: regulation of niche, self-renewal and differentiation. Arthritis Research & Therapy. 2007;9(1):204.
  • Margiana R, Markov A, Zekiy AO, Hamza MU, Al-Dabbagh KA, Al-Zubaidi SH, et al. Clinical application of mesenchymal stem cell in regenerative medicine: a narrative review. Stem Cell Research & Therapy. 2022 Jul 28;13(1).
  • Deo D, Marchioni M, Rao P. Mesenchymal Stem/Stromal Cells in Organ Transplantation. Pharmaceutics [Internet]. 2022 Apr 1 [cited 2023 Feb 20];14(4):791.
  • Ledesma-Martínez E, Mendoza-Núñez VM, Santiago-Osorio E. Mesenchymal Stem Cells Derived from Dental Pulp: A Review. Stem Cells International. 2016;2016:1–12.
  • Liu S, Ginestier C, Ou SJ, Clouthier SG, Patel SH, Monville F, et al. Breast Cancer Stem Cells Are Regulated by Mesenchymal Stem Cells through Cytokine Networks. Cancer Research. 2011 Jan 11;71(2):614–2
  • Qiao L, Xu Z, Zhao T, Ye L, Zhang X. Dkk-1 secreted by mesenchymal stem cells inhibits growth of breast cancer cells via depression of Wnt signalling. Cancer Letters. 2008 Sep;269(1):67–77.
  • Mandel K, Yang Y, Schambach A, Glage S, Otte A, Hass R. Mesenchymal Stem Cells Directly Interact with Breast Cancer Cells and Promote Tumor Cell Growth In Vitro and In Vivo. Stem Cells and Development. 2013 Dec;22(23):3114–27.
  • Casson J, Davies OG, Smith C-A, Dalby MJ, Berry CC. Mesenchymal stem cell-derived extracellular vesicles may promote breast cancer cell dormancy. Journal of Tissue Engineering. 2018 Jan;9:204173141881009.
  • Melzer C, von der Ohe J, Luo T, Hass R. Spontaneous Fusion of MSC with Breast Cancer Cells Can Generate Tumor Dormancy. International Journal of Molecular Sciences [Internet]. 2021 May 31;22(11):5930
  • Ramasamy R, Lam EW-F, Soeiro I, Tisato V, Bonnet D, Dazzi F. Mesenchymal stem cells inhibit proliferation and apoptosis of tumor cells: impact on in vivo tumor growth. Leukemia. 2006 Dec 14;21(2):304–10.
  • Gilazieva Z, Ponomarev A, Rizvanov A, Solovyeva V. The Dual Role of Mesenchymal Stromal Cells and Their Extracellular Vesicles in Carcinogenesis. Biology [Internet]. 2022 May 25;11(6):813
  • Li X, Fan Q, Peng X, Yang S, Wei S, Liu J, et al. Mesenchymal/stromal stem cells: necessary factors in tumour progression. Cell Death Discovery [Internet]. 2022 Jul 22;8(1):333
There are 46 citations in total.

Details

Primary Language Turkish
Subjects Regenerative Medicine (Incl. Stem Cells), Histology and Embryology
Journal Section Research Articles
Authors

Gizem İnetaş Yengin 0000-0002-9421-651X

Öykü Gönül Geyik 0000-0003-3014-1253

Hüsnü Alper Bağrıyanık 0000-0003-4064-7637

Zeynep Yüce 0000-0002-2762-0942

Gülperi Öktem 0000-0003-1914-2503

Publication Date September 18, 2023
Submission Date December 6, 2022
Published in Issue Year 2023

Cite

Vancouver İnetaş Yengin G, Geyik ÖG, Bağrıyanık HA, Yüce Z, Öktem G. İnsan diş pulpası kaynaklı mezenkimal kök hücrelerin meme kanseri kök hücreleri üzerine etkisi. ETD. 2023;62(3):396-405.

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