Skip to main content
Erschienen in: Clinical Oral Investigations 10/2019

28.01.2019 | Original Article

Influence of buffy coat–derived putative endothelial progenitor cells on tumor growth and neovascularization in oral squamous cell carcinoma xenografts

verfasst von: Marius Otto, Sebastian Blatt, Andreas Pabst, Robert Mandic, Johanna Schwarz, Andreas Neff, Thomas Ziebart

Erschienen in: Clinical Oral Investigations | Ausgabe 10/2019

Einloggen, um Zugang zu erhalten

Abstract

Objectives

The aim of this murine in vivo study was to investigate whether buffy coat–derived putative endothelial progenitor cells (BCEPC) alter tumor growth and neovascularization in oral squamous cell carcinomas (OSCC).

Materials and methods

A murine xenograft model using the PCI-13 oral cancer cell line was deployed of which n = 24 animals received 2 × 106 BCEPC by transfusion whereas the control group (n = 24) received NaCl (0.9%) instead. Tumor size, volume, and capillary density were determined by sonography and measurement with a caliper. Immunohistochemical analysis was carried out with antibodies specific for Cytokeratins, Flt-4, Podoplanin, and Vimentin.

Results

In the experimental group, systemic application of BCEPC significantly increased tumor volume to 362.49% (p = 0.0012) and weight to 352.38% (p = 0.0018) as well as vascular densities to 162.15% (p = 0.0021) compared with control tumors. In addition, BCEPC-treated xenografts exhibited higher Cytokeratin expression levels by a factor of 1.47 (p = 0.0417), Podoplanin by a factor of 3.3 (p = 0.0020) and Vimentin by a factor of 2.5 (p = 0.0001), respectively.

Conclusions

Immunohistochemical investigations support the notion that BCEPC transfusion influences neovascularization and lymphatic vessel density, thereby possibly promoting tumor progression. Future studies, which will include gene expression analysis, should help to define the possible role of BCEPC during OSCC progression in more detail.

Clinical relevance

Endothelial progenitor cells (EPCs) could serve as a target structure for the treatment of OSCC and possibly other solid tumors.
Literatur
1.
Zurück zum Zitat Vigneswaran N, Williams MD (2014) Epidemiologic trends in head and neck cancer and aids in diagnosis. Oral Maxillofac Surg Clin North Am 26:123–141CrossRefPubMedPubMedCentral Vigneswaran N, Williams MD (2014) Epidemiologic trends in head and neck cancer and aids in diagnosis. Oral Maxillofac Surg Clin North Am 26:123–141CrossRefPubMedPubMedCentral
2.
Zurück zum Zitat Lippman SM, Spitz M, Trizna Z, Benner SE, Hong WK (1994) Epidemiology, biology, and chemoprevention of aerodigestive cancer. Cancer 74:2719–2725CrossRefPubMed Lippman SM, Spitz M, Trizna Z, Benner SE, Hong WK (1994) Epidemiology, biology, and chemoprevention of aerodigestive cancer. Cancer 74:2719–2725CrossRefPubMed
3.
Zurück zum Zitat Bose P, Brockton NT, Dort JC (2013) Head and neck cancer: from anatomy to biology. Int J Cancer 133:2013–2023CrossRefPubMed Bose P, Brockton NT, Dort JC (2013) Head and neck cancer: from anatomy to biology. Int J Cancer 133:2013–2023CrossRefPubMed
4.
Zurück zum Zitat Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, Witzenbichler B, Schatteman G, Isner JM (1997) Isolation of putative progenitor endothelial cells for angiogenesis. Science 275:964–967CrossRefPubMed Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, Witzenbichler B, Schatteman G, Isner JM (1997) Isolation of putative progenitor endothelial cells for angiogenesis. Science 275:964–967CrossRefPubMed
5.
Zurück zum Zitat Walter DH, Rittig K, Bahlmann FH, Kirchmair R, Silver M, Murayama T, Nishimura H, Losordo DW, Asahara T, Isner JM (2002) Statin therapy accelerates reendothelialization. Circulation 105:3017–3024CrossRefPubMed Walter DH, Rittig K, Bahlmann FH, Kirchmair R, Silver M, Murayama T, Nishimura H, Losordo DW, Asahara T, Isner JM (2002) Statin therapy accelerates reendothelialization. Circulation 105:3017–3024CrossRefPubMed
6.
Zurück zum Zitat Werner N, Nickenig G (2004) Vascular progenitor cells and atherogenesis. DMW Dtsch Med Wochenschr 129:1269–1275CrossRef Werner N, Nickenig G (2004) Vascular progenitor cells and atherogenesis. DMW Dtsch Med Wochenschr 129:1269–1275CrossRef
7.
Zurück zum Zitat Ziebart T, Yoon C-H, Trepels T, Wietelmann A, Braun T, Kiessling F, Stein S, Grez M, Ihling C, Muhly-Reinholz M, Carmona G, Urbich C, Zeiher AM, Dimmeler S (2008) Sustained persistence of transplanted proangiogenic cells contributes to neovascularization and cardiac function after ischemia. Circ Res 103:1327–1334CrossRefPubMed Ziebart T, Yoon C-H, Trepels T, Wietelmann A, Braun T, Kiessling F, Stein S, Grez M, Ihling C, Muhly-Reinholz M, Carmona G, Urbich C, Zeiher AM, Dimmeler S (2008) Sustained persistence of transplanted proangiogenic cells contributes to neovascularization and cardiac function after ischemia. Circ Res 103:1327–1334CrossRefPubMed
8.
Zurück zum Zitat Ziebart T, Pabst A, Klein MO, Kämmerer P, Gauss L, Brüllmann D, Al-Nawas B, Walter C (2011) Bisphosphonates: restrictions for vasculogenesis and angiogenesis: inhibition of cell function of endothelial progenitor cells and mature endothelial cells in vitro. Clin Oral Investig 15:105–111CrossRefPubMed Ziebart T, Pabst A, Klein MO, Kämmerer P, Gauss L, Brüllmann D, Al-Nawas B, Walter C (2011) Bisphosphonates: restrictions for vasculogenesis and angiogenesis: inhibition of cell function of endothelial progenitor cells and mature endothelial cells in vitro. Clin Oral Investig 15:105–111CrossRefPubMed
9.
Zurück zum Zitat Ratajska A, Jankowska-Steifer E, Czarnowska E, Olkowski R, Gula G, Niderla-Bielińska J, Flaht-Zabost A, Jasińska A (2016) Vasculogenesis and its cellular therapeutic applications. Cells Tissues Organs Ratajska A, Jankowska-Steifer E, Czarnowska E, Olkowski R, Gula G, Niderla-Bielińska J, Flaht-Zabost A, Jasińska A (2016) Vasculogenesis and its cellular therapeutic applications. Cells Tissues Organs
10.
Zurück zum Zitat Sridharan V, Margalit DN, Lynch SA, Severgnini M, Hodi FS, Haddad RI, Tishler RB, Schoenfeld JD (2016) Effects of definitive chemoradiation on circulating immunologic angiogenic cytokines in head and neck cancer patients. J Immunother Cancer 4:32CrossRefPubMedPubMedCentral Sridharan V, Margalit DN, Lynch SA, Severgnini M, Hodi FS, Haddad RI, Tishler RB, Schoenfeld JD (2016) Effects of definitive chemoradiation on circulating immunologic angiogenic cytokines in head and neck cancer patients. J Immunother Cancer 4:32CrossRefPubMedPubMedCentral
11.
Zurück zum Zitat Lin Y, Weisdorf DJ, Solovey A, Hebbel RP (2000) Origins of circulating endothelial cells and endothelial outgrowth from blood. J Clin Invest 105:71–77CrossRefPubMedPubMedCentral Lin Y, Weisdorf DJ, Solovey A, Hebbel RP (2000) Origins of circulating endothelial cells and endothelial outgrowth from blood. J Clin Invest 105:71–77CrossRefPubMedPubMedCentral
12.
Zurück zum Zitat Hur J, Yoon C-H, Kim H-S, Choi J-H, Kang H-J, Hwang K-K, Oh B-H, Lee M-M, Park Y-B (2004) Characterization of two types of endothelial progenitor cells and their different contributions to neovasculogenesis. Arterioscler Thromb Vasc Biol 24:288–293CrossRefPubMed Hur J, Yoon C-H, Kim H-S, Choi J-H, Kang H-J, Hwang K-K, Oh B-H, Lee M-M, Park Y-B (2004) Characterization of two types of endothelial progenitor cells and their different contributions to neovasculogenesis. Arterioscler Thromb Vasc Biol 24:288–293CrossRefPubMed
13.
Zurück zum Zitat Urbich C, Aicher A, Heeschen C, Dernbach E, Hofmann WK, Zeiher AM, Dimmeler S (2005) Soluble factors released by endothelial progenitor cells promote migration of endothelial cells and cardiac resident progenitor cells. J Mol Cell Cardiol 39:733–742CrossRefPubMed Urbich C, Aicher A, Heeschen C, Dernbach E, Hofmann WK, Zeiher AM, Dimmeler S (2005) Soluble factors released by endothelial progenitor cells promote migration of endothelial cells and cardiac resident progenitor cells. J Mol Cell Cardiol 39:733–742CrossRefPubMed
14.
15.
Zurück zum Zitat Ziebart T, Blatt S, Günther C, Völxen N, Pabst A, Sagheb K, Kühl S, Lambrecht T (2016) Significance of endothelial progenitor cells (EPC) for tumorigenesis of head and neck squamous cell carcinoma (HNSCC): possible marker of tumor progression and neovascularization? Clin Oral Investig 20:2293–2300CrossRefPubMed Ziebart T, Blatt S, Günther C, Völxen N, Pabst A, Sagheb K, Kühl S, Lambrecht T (2016) Significance of endothelial progenitor cells (EPC) for tumorigenesis of head and neck squamous cell carcinoma (HNSCC): possible marker of tumor progression and neovascularization? Clin Oral Investig 20:2293–2300CrossRefPubMed
16.
Zurück zum Zitat Moschetta M, Mishima Y, Sahin I, Manier S, Glavey S, Vacca A, Roccaro AM, Ghobrial IM (2014) Role of endothelial progenitor cells in cancer progression. Biochim Biophys Acta 1846(1):26–39PubMed Moschetta M, Mishima Y, Sahin I, Manier S, Glavey S, Vacca A, Roccaro AM, Ghobrial IM (2014) Role of endothelial progenitor cells in cancer progression. Biochim Biophys Acta 1846(1):26–39PubMed
17.
Zurück zum Zitat Wildt S (2015) Hairless NOD scid mouse. 9018441 Wildt S (2015) Hairless NOD scid mouse. 9018441
18.
Zurück zum Zitat Vasa M, Fichtlscherer S, Aicher A, Adler K, Urbich C, Martin H, Zeiher AM, Dimmeler S (2001) Number and migratory activity of circulating endothelial progenitor cells inversely correlate with risk factors for coronary artery disease. Circ Res 89:E1–E7CrossRefPubMed Vasa M, Fichtlscherer S, Aicher A, Adler K, Urbich C, Martin H, Zeiher AM, Dimmeler S (2001) Number and migratory activity of circulating endothelial progenitor cells inversely correlate with risk factors for coronary artery disease. Circ Res 89:E1–E7CrossRefPubMed
19.
Zurück zum Zitat Seeger FH, Tonn T, Krzossok N, Zeiher AM, Dimmeler S (2007) Cell isolation procedures matter: a comparison of different isolation protocols of bone marrow mononuclear cells used for cell therapy in patients with acute myocardial infarction. Eur Heart J 28:766–772CrossRefPubMed Seeger FH, Tonn T, Krzossok N, Zeiher AM, Dimmeler S (2007) Cell isolation procedures matter: a comparison of different isolation protocols of bone marrow mononuclear cells used for cell therapy in patients with acute myocardial infarction. Eur Heart J 28:766–772CrossRefPubMed
20.
Zurück zum Zitat Tomayko MM, Reynolds CP (1989) Determination of subcutaneous tumor size in athymic (nude) mice. Cancer Chemother Pharmacol 24:148–154CrossRefPubMed Tomayko MM, Reynolds CP (1989) Determination of subcutaneous tumor size in athymic (nude) mice. Cancer Chemother Pharmacol 24:148–154CrossRefPubMed
21.
Zurück zum Zitat Cardiff RD, Miller CH, Munn RJ (2014) Manual immunohistochemistry staining of mouse tissues using the avidin-biotin complex (ABC) technique. Cold Spring Harb Protoc 2014:659–662PubMed Cardiff RD, Miller CH, Munn RJ (2014) Manual immunohistochemistry staining of mouse tissues using the avidin-biotin complex (ABC) technique. Cold Spring Harb Protoc 2014:659–662PubMed
22.
Zurück zum Zitat Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, Tinevez J-Y, White DJ, Hartenstein V, Eliceiri K, Tomancak P, Cardona A (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9:676–682CrossRefPubMed Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, Tinevez J-Y, White DJ, Hartenstein V, Eliceiri K, Tomancak P, Cardona A (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9:676–682CrossRefPubMed
23.
Zurück zum Zitat Ge YZ, Wu R, Lu TZ, Xin H, Yu P, Zhao Y, Liu H, Xu Z, Xu LW, Shen JW, Xu X, Zhou LH, Li WC, Zhu JG, Jia RP (2015) Circulating endothelial progenitor cell: a promising biomarker in clinical oncology. Med Oncol 32(1):332CrossRefPubMed Ge YZ, Wu R, Lu TZ, Xin H, Yu P, Zhao Y, Liu H, Xu Z, Xu LW, Shen JW, Xu X, Zhou LH, Li WC, Zhu JG, Jia RP (2015) Circulating endothelial progenitor cell: a promising biomarker in clinical oncology. Med Oncol 32(1):332CrossRefPubMed
24.
Zurück zum Zitat George AL, Bangalore-Prakash P, Rajoria S, Suriano R, Shanmugam A, Mittelman A, Tiwari RK (2011) Endothelial progenitor cell biology in disease and tissue regeneration. J Hematol Oncol 4:24CrossRefPubMedPubMedCentral George AL, Bangalore-Prakash P, Rajoria S, Suriano R, Shanmugam A, Mittelman A, Tiwari RK (2011) Endothelial progenitor cell biology in disease and tissue regeneration. J Hematol Oncol 4:24CrossRefPubMedPubMedCentral
25.
Zurück zum Zitat Brunner M, Thurnher D, Heiduschka G, Grasl M, Brostjan C, Erovic BM (2008) Elevated levels of circulating endothelial progenitor cells in head and neck cancer patients. J Surg Oncol 98(7):545–550CrossRefPubMed Brunner M, Thurnher D, Heiduschka G, Grasl M, Brostjan C, Erovic BM (2008) Elevated levels of circulating endothelial progenitor cells in head and neck cancer patients. J Surg Oncol 98(7):545–550CrossRefPubMed
26.
Zurück zum Zitat Umemura T, Higashi Y (2008) Endothelial progenitor cells: therapeutic target for cardiovascular diseases. J Pharmacol Sci 108(1):1–6CrossRefPubMed Umemura T, Higashi Y (2008) Endothelial progenitor cells: therapeutic target for cardiovascular diseases. J Pharmacol Sci 108(1):1–6CrossRefPubMed
27.
Zurück zum Zitat Hristov M, Erl W, Weber PC (2003) Endothelial progenitor cells: mobilization, differentiation, and homing. Arterioscler Thromb Vasc Biol 23(7):1185–1189CrossRefPubMed Hristov M, Erl W, Weber PC (2003) Endothelial progenitor cells: mobilization, differentiation, and homing. Arterioscler Thromb Vasc Biol 23(7):1185–1189CrossRefPubMed
28.
Zurück zum Zitat Moccia F, Poletto V (2015) May the remodeling of the Ca(2)(+) toolkit in endothelial progenitor cells derived from cancer patients suggest alternative targets for anti-angiogenic treatment? Biochim Biophys Acta 1853(9):1958–1973CrossRefPubMed Moccia F, Poletto V (2015) May the remodeling of the Ca(2)(+) toolkit in endothelial progenitor cells derived from cancer patients suggest alternative targets for anti-angiogenic treatment? Biochim Biophys Acta 1853(9):1958–1973CrossRefPubMed
29.
Zurück zum Zitat Laurenzana A, Margheri F, Chilla A, Biagioni A, Margheri G, Calorini L et al (2016) Endothelial progenitor cells as shuttle of anticancer agents. Hum Gene Ther 27:784–791CrossRefPubMed Laurenzana A, Margheri F, Chilla A, Biagioni A, Margheri G, Calorini L et al (2016) Endothelial progenitor cells as shuttle of anticancer agents. Hum Gene Ther 27:784–791CrossRefPubMed
30.
Zurück zum Zitat Torimura T, Ueno T, Taniguchi E, Masuda H, Iwamoto H, Nakamura T, Inoue K, Hashimoto O, Abe M, Koga H, Barresi V, Nakashima E, Yano H, Sata M (2012) Interaction of endothelial progenitor cells expressing cytosine deaminase in tumor tissues and 5-fluorocytosine administration suppresses growth of 5-fluorouracil-sensitive liver cancer in mice. Cancer Sci 103(3):542–548CrossRefPubMedPubMedCentral Torimura T, Ueno T, Taniguchi E, Masuda H, Iwamoto H, Nakamura T, Inoue K, Hashimoto O, Abe M, Koga H, Barresi V, Nakashima E, Yano H, Sata M (2012) Interaction of endothelial progenitor cells expressing cytosine deaminase in tumor tissues and 5-fluorocytosine administration suppresses growth of 5-fluorouracil-sensitive liver cancer in mice. Cancer Sci 103(3):542–548CrossRefPubMedPubMedCentral
31.
Zurück zum Zitat Kaur S, Bajwa PA (2014) Tete-a tete’ between cancer stem cells and endothelial progenitor cells in tumor angiogenesis. Clin Transl Oncol 16(2):115–121CrossRefPubMed Kaur S, Bajwa PA (2014) Tete-a tete’ between cancer stem cells and endothelial progenitor cells in tumor angiogenesis. Clin Transl Oncol 16(2):115–121CrossRefPubMed
32.
Zurück zum Zitat Zhao X, Liu H-Q, Li J, Liu X-L (2016) Endothelial progenitor cells promote tumor growth and progression by enhancing new vessel formation. Oncol Lett 12:793–799CrossRefPubMedPubMedCentral Zhao X, Liu H-Q, Li J, Liu X-L (2016) Endothelial progenitor cells promote tumor growth and progression by enhancing new vessel formation. Oncol Lett 12:793–799CrossRefPubMedPubMedCentral
33.
Zurück zum Zitat Janic B, Arbab AS (2010) The role and therapeutic potential of endothelial progenitor cells in tumor neovascularization. ScientificWorldJournal 10:1088–1099CrossRefPubMedPubMedCentral Janic B, Arbab AS (2010) The role and therapeutic potential of endothelial progenitor cells in tumor neovascularization. ScientificWorldJournal 10:1088–1099CrossRefPubMedPubMedCentral
34.
Zurück zum Zitat Neuchrist C, Erovic BM, Handisurya A, Fischer MB, Steiner GE, Hollemann D, Gedlicka C, Saaristo A, Burian M (2003) Vascular endothelial growth factor C and vascular endothelial growth factor receptor 3 expression in squamous cell carcinomas of the head and neck. Head Neck 25:464–474CrossRefPubMed Neuchrist C, Erovic BM, Handisurya A, Fischer MB, Steiner GE, Hollemann D, Gedlicka C, Saaristo A, Burian M (2003) Vascular endothelial growth factor C and vascular endothelial growth factor receptor 3 expression in squamous cell carcinomas of the head and neck. Head Neck 25:464–474CrossRefPubMed
35.
Zurück zum Zitat Ge Q, Zhang H, Hou J, Wan L, Cheng W, Wang X, Dong D, Chen C, Xia J, Guo J, Chen X, Wu X (2018) VEGF secreted by mesenchymal stem cells mediates the differentiation of endothelial progenitor cells into endothelial cells via paracrine mechanisms. Mol Med Rep 17:1667–1675PubMed Ge Q, Zhang H, Hou J, Wan L, Cheng W, Wang X, Dong D, Chen C, Xia J, Guo J, Chen X, Wu X (2018) VEGF secreted by mesenchymal stem cells mediates the differentiation of endothelial progenitor cells into endothelial cells via paracrine mechanisms. Mol Med Rep 17:1667–1675PubMed
36.
Zurück zum Zitat Buttler K, Badar M, Seiffart V, Laggies S, Gross G, Wilting J, Weich HA (2014) De novo hem- and lymphangiogenesis by endothelial progenitor and mesenchymal stem cells in immunocompetent mice. Cell Mol Life Sci 71:1513–1527CrossRefPubMed Buttler K, Badar M, Seiffart V, Laggies S, Gross G, Wilting J, Weich HA (2014) De novo hem- and lymphangiogenesis by endothelial progenitor and mesenchymal stem cells in immunocompetent mice. Cell Mol Life Sci 71:1513–1527CrossRefPubMed
37.
Zurück zum Zitat Parmar P, Marwah N, Parshad S, Yadav T, Batra A, Sen R (2018) Clinicopathological significance of tumor lymphatic vessel density in head and neck squamous cell carcinoma. Indian J Otolaryngol Head Neck Surg 70:102–110CrossRefPubMed Parmar P, Marwah N, Parshad S, Yadav T, Batra A, Sen R (2018) Clinicopathological significance of tumor lymphatic vessel density in head and neck squamous cell carcinoma. Indian J Otolaryngol Head Neck Surg 70:102–110CrossRefPubMed
38.
Zurück zum Zitat Mermod M, Bongiovanni M, Petrova TV, Dubikovskaya EA, Simon C, Tolstonog G, Monnier Y (2017) Correlation between podoplanin expression and extracapsular spread in squamous cell carcinoma of the oral cavity using subjective immunoreactivity scores and semiquantitative image analysis. Head Neck 39:98–108CrossRefPubMed Mermod M, Bongiovanni M, Petrova TV, Dubikovskaya EA, Simon C, Tolstonog G, Monnier Y (2017) Correlation between podoplanin expression and extracapsular spread in squamous cell carcinoma of the oral cavity using subjective immunoreactivity scores and semiquantitative image analysis. Head Neck 39:98–108CrossRefPubMed
39.
Zurück zum Zitat Li T, Wang G, Tan Y, Wang H (2014) Inhibition of lymphangiogenesis of endothelial progenitor cells with VEGFR-3 siRNA delivered with PEI-alginate nanoparticles. Int J Biol Sci 10:160–170CrossRefPubMedPubMedCentral Li T, Wang G, Tan Y, Wang H (2014) Inhibition of lymphangiogenesis of endothelial progenitor cells with VEGFR-3 siRNA delivered with PEI-alginate nanoparticles. Int J Biol Sci 10:160–170CrossRefPubMedPubMedCentral
40.
Zurück zum Zitat Smith A, Teknos TN, Pan Q (2013) Epithelial to mesenchymal transition in head and neck squamous cell carcinoma. Oral Oncol 49:287–292CrossRefPubMed Smith A, Teknos TN, Pan Q (2013) Epithelial to mesenchymal transition in head and neck squamous cell carcinoma. Oral Oncol 49:287–292CrossRefPubMed
41.
Zurück zum Zitat Aruga N, Kijima H, Masuda R, Onozawa H, Yoshizawa T, Tanaka M, Inokuchi S, Iwazaki M (2018) Epithelial-mesenchymal transition (EMT) is correlated with patient’s prognosis of lung squamous cell carcinoma. Tokai J Exp Clin Med 43:5–13PubMed Aruga N, Kijima H, Masuda R, Onozawa H, Yoshizawa T, Tanaka M, Inokuchi S, Iwazaki M (2018) Epithelial-mesenchymal transition (EMT) is correlated with patient’s prognosis of lung squamous cell carcinoma. Tokai J Exp Clin Med 43:5–13PubMed
42.
Zurück zum Zitat Joseph JP, Harishankar MK, Pillai AA, Devi A (2018) Hypoxia induced EMT: a review on the mechanism of tumor progression and metastasis in OSCC. Oral Oncol 80:23–32CrossRefPubMed Joseph JP, Harishankar MK, Pillai AA, Devi A (2018) Hypoxia induced EMT: a review on the mechanism of tumor progression and metastasis in OSCC. Oral Oncol 80:23–32CrossRefPubMed
43.
Zurück zum Zitat Tania M, Khan MA, Fu J (2014) Epithelial to mesenchymal transition inducing transcription factors and metastatic cancer. Tumour Biol 35:7335–7342CrossRefPubMed Tania M, Khan MA, Fu J (2014) Epithelial to mesenchymal transition inducing transcription factors and metastatic cancer. Tumour Biol 35:7335–7342CrossRefPubMed
44.
Zurück zum Zitat Madonna R, De Caterina R (2015) Circulating endothelial progenitor cells: do they live up to their name? Vasc Pharmacol 67-69:2–5CrossRef Madonna R, De Caterina R (2015) Circulating endothelial progenitor cells: do they live up to their name? Vasc Pharmacol 67-69:2–5CrossRef
45.
Zurück zum Zitat Fadini GP, Losordo D, Dimmeler S (2012) Critical reevaluation of endothelial progenitor cell phenotypes for therapeutic and diagnostic use. Circ Res 110:624–637CrossRefPubMedPubMedCentral Fadini GP, Losordo D, Dimmeler S (2012) Critical reevaluation of endothelial progenitor cell phenotypes for therapeutic and diagnostic use. Circ Res 110:624–637CrossRefPubMedPubMedCentral
46.
Zurück zum Zitat Zhao Y, Yu P, Wu R, Ge Y, Wu J, Zhu J, Jia R (2013) Renal cell carcinoma-adjacent tissues enhance mobilization and recruitment of endothelial progenitor cells to promote the invasion of the neoplasm. Biomed Pharmacother 67:643–649CrossRefPubMed Zhao Y, Yu P, Wu R, Ge Y, Wu J, Zhu J, Jia R (2013) Renal cell carcinoma-adjacent tissues enhance mobilization and recruitment of endothelial progenitor cells to promote the invasion of the neoplasm. Biomed Pharmacother 67:643–649CrossRefPubMed
47.
Zurück zum Zitat Kong Z, Hong Y, Zhu J, Cheng X, Liu Y (2018) Endothelial progenitor cells improve functional recovery in focal cerebral ischemia of rat by promoting angiogenesis via VEGF. J Clin Neurosci 55:116–121CrossRefPubMed Kong Z, Hong Y, Zhu J, Cheng X, Liu Y (2018) Endothelial progenitor cells improve functional recovery in focal cerebral ischemia of rat by promoting angiogenesis via VEGF. J Clin Neurosci 55:116–121CrossRefPubMed
Metadaten
Titel
Influence of buffy coat–derived putative endothelial progenitor cells on tumor growth and neovascularization in oral squamous cell carcinoma xenografts
verfasst von
Marius Otto
Sebastian Blatt
Andreas Pabst
Robert Mandic
Johanna Schwarz
Andreas Neff
Thomas Ziebart
Publikationsdatum
28.01.2019
Verlag
Springer Berlin Heidelberg
Erschienen in
Clinical Oral Investigations / Ausgabe 10/2019
Print ISSN: 1432-6981
Elektronische ISSN: 1436-3771
DOI
https://doi.org/10.1007/s00784-019-02806-2

Weitere Artikel der Ausgabe 10/2019

Clinical Oral Investigations 10/2019 Zur Ausgabe

Newsletter

Bestellen Sie unseren kostenlosen Newsletter Update Zahnmedizin und bleiben Sie gut informiert – ganz bequem per eMail.