Skip to main content
Top
Published in: Head and Neck Pathology 4/2020

01-12-2020 | Oral Cancer | Review

Pericyte in Oral Squamous Cell Carcinoma: A Systematic Review

Authors: Isabella Bittencourt Valle, Lauren Frenzel Schuch, Janine Mayra da Silva, Alfonso Gala-García, Ivana Márcia Alves Diniz, Alexander Birbrair, Lucas Guimarães Abreu, Tarcília Aparecida Silva

Published in: Head and Neck Pathology | Issue 4/2020

Login to get access

Abstract

The microenvironment of oral cancer is highly dynamic and has been proved to affect tumor progression. Pericytes are blood vessels surrounding cells that have recently gained attention for their roles in vascular and cancer biology. The objective of the present study was to survey the scientific literature for conclusive evidence about whether pericytes are part of blood vessels in oral squamous cell carcinoma (OSCC) and their roles in the tumor microenvironment and clinical outcomes. A systematic electronic search was undertaken in Medline Ovid, PubMed, Web of Science, and Scopus. Eligibility criteria were: publications adopting in vivo models of OSCC that included pericyte detection and assessment by pericyte markers (e.g., α-smooth muscle actin, neuron-glial antigen 2 and platelet-derived growth factor receptor-β). The search yielded seven eligible studies (from 2008 to 2018). The markers most commonly used for pericyte detection were α-smooth muscle actin and neuron-glial antigen 2. The studies reviewed showed the presence of immature vessels exhibiting a reduction of pericyte coverage in OSCC and indicated that anti-cancer therapies could contribute to vessel normalization and pericyte regain. The pericyte population is significantly affected during OSCC development and cancer therapy. While these findings might suggest a role for pericytes in OSCC progression, the limited data available do not allow us to conclude whether they modify the tumor microenvironment and clinical outcome.
Appendix
Available only for authorised users
Literature
1.
go back to reference Rouget C. Memoire sur le developpement, la structures et les proprietes des capillaires sanguins et lymphatiques. Archs Physiol Norm Pathol. 1873;5:603–33. Rouget C. Memoire sur le developpement, la structures et les proprietes des capillaires sanguins et lymphatiques. Archs Physiol Norm Pathol. 1873;5:603–33.
2.
go back to reference Armulik A, Genové G, Betsholtz C. Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev Cell. 2011;21:193–21515.PubMed Armulik A, Genové G, Betsholtz C. Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev Cell. 2011;21:193–21515.PubMed
3.
go back to reference Prazeres PH, Sena IFG, Borges IDT, et al. Pericytes are heterogeneous in their origin within the same tissue. Dev Biol. 2017;427:6–11.PubMedCentral Prazeres PH, Sena IFG, Borges IDT, et al. Pericytes are heterogeneous in their origin within the same tissue. Dev Biol. 2017;427:6–11.PubMedCentral
4.
go back to reference Diaz-Flores L, Gutierrez R, Varela H, Rancel N, Valladares F. Microvascular pericytes: A review of their morphological and functional characteristics. Histol Histopathol. 1991;6:269–86.PubMed Diaz-Flores L, Gutierrez R, Varela H, Rancel N, Valladares F. Microvascular pericytes: A review of their morphological and functional characteristics. Histol Histopathol. 1991;6:269–86.PubMed
5.
go back to reference Crisan M, Yap S, Casteilla L, et al. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell. 2008;3:301–13.PubMed Crisan M, Yap S, Casteilla L, et al. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell. 2008;3:301–13.PubMed
6.
go back to reference Ayres-Sander CE, Lauridsen H, Maier CL, Sava P, Pober JS, Gonzalez AL. Transendothelial migration enables subsequent transmigration of neutrophils through underlying pericytes. PLoS ONE. 2013;8:1–12. Ayres-Sander CE, Lauridsen H, Maier CL, Sava P, Pober JS, Gonzalez AL. Transendothelial migration enables subsequent transmigration of neutrophils through underlying pericytes. PLoS ONE. 2013;8:1–12.
7.
go back to reference Kitahara H, Kajikawa S, Ishii Y, et al. The novel pathogenesis of retinopathy mediated by multiple RTK signals is uncovered in newly developed mouse model. EBioMedicine. 2018;31:190–201.PubMedPubMedCentral Kitahara H, Kajikawa S, Ishii Y, et al. The novel pathogenesis of retinopathy mediated by multiple RTK signals is uncovered in newly developed mouse model. EBioMedicine. 2018;31:190–201.PubMedPubMedCentral
8.
go back to reference Shaw I, Rider S, Mullins J, Hughes J, Péault B. Pericytes in the renal vasculature: roles in health and disease. Nat Rev Nephrol. 2018;14:521–34.PubMed Shaw I, Rider S, Mullins J, Hughes J, Péault B. Pericytes in the renal vasculature: roles in health and disease. Nat Rev Nephrol. 2018;14:521–34.PubMed
9.
go back to reference Von Tell D, Armulik A, Betsholtz C. Pericytes and vascular stability. Exp Cell Res. 2006;312:623–9. Von Tell D, Armulik A, Betsholtz C. Pericytes and vascular stability. Exp Cell Res. 2006;312:623–9.
10.
go back to reference Mathiisen TM, Lehre KP, Danbolt NC, Ottersen OP. The perivascular astroglial sheath provides a complete covering of the brain microvessels: an electron microscopic 3D reconstruction. Glia. 2010;58:1094–103.PubMed Mathiisen TM, Lehre KP, Danbolt NC, Ottersen OP. The perivascular astroglial sheath provides a complete covering of the brain microvessels: an electron microscopic 3D reconstruction. Glia. 2010;58:1094–103.PubMed
11.
12.
go back to reference Díaz-Flores L, Gutiérrez R, Madrid JF, et al. Pericytes. Morphofunction, interactions and pathology in a quiescent and activated mesenchymal cell niche. Histol Histopathol. 2009;24:909–69.PubMed Díaz-Flores L, Gutiérrez R, Madrid JF, et al. Pericytes. Morphofunction, interactions and pathology in a quiescent and activated mesenchymal cell niche. Histol Histopathol. 2009;24:909–69.PubMed
13.
go back to reference Park DY, Lee J, Kim J, et al. Plastic roles of pericytes in the blood–retinal barrier. Nat Commun. 2017;8:1–16. Park DY, Lee J, Kim J, et al. Plastic roles of pericytes in the blood–retinal barrier. Nat Commun. 2017;8:1–16.
14.
go back to reference Sagare AP, Bell RD, Zhao Z, Ma Q, Winkler EA, Ramanathan A, Zlokovic BV. Pericyte loss influences Alzheimer-like neurodegeneration in mice. Nat Commun. 2013;4:1–14. Sagare AP, Bell RD, Zhao Z, Ma Q, Winkler EA, Ramanathan A, Zlokovic BV. Pericyte loss influences Alzheimer-like neurodegeneration in mice. Nat Commun. 2013;4:1–14.
15.
go back to reference Eberhard A, Kahlert S, Goede V, Hemmerlein B, Plate KH, Augustin HG. Heterogeneity of angiogenesis and blood vessel maturation in human tumors: implications for antiangiogenic tumor therapies. Cancer Res. 2000;60:1388–93.PubMed Eberhard A, Kahlert S, Goede V, Hemmerlein B, Plate KH, Augustin HG. Heterogeneity of angiogenesis and blood vessel maturation in human tumors: implications for antiangiogenic tumor therapies. Cancer Res. 2000;60:1388–93.PubMed
16.
go back to reference Gee MS, Procopio WN, Makonnen S, Feldman MD, Yeilding NM, Lee WMF. Tumor vessel development and maturation impose limits on the effectiveness of anti-vascular therapy. Am J Pathol. 2003;162:183–93.PubMedPubMedCentral Gee MS, Procopio WN, Makonnen S, Feldman MD, Yeilding NM, Lee WMF. Tumor vessel development and maturation impose limits on the effectiveness of anti-vascular therapy. Am J Pathol. 2003;162:183–93.PubMedPubMedCentral
17.
go back to reference Sinha D, Chong L, George J, et al. Pericytes promote malignant ovarian cancer progression in mice and predict poor prognosis in serous ovarian cancer patients. Clin Cancer Res. 2006;22:1813–24. Sinha D, Chong L, George J, et al. Pericytes promote malignant ovarian cancer progression in mice and predict poor prognosis in serous ovarian cancer patients. Clin Cancer Res. 2006;22:1813–24.
18.
go back to reference Yonenaga Y, Mori A, Onodera H, et al. Absence of smooth muscle actin-positive pericyte coverage of tumor vessels correlates with hematogenous metastasis and prognosis of colorectal cancer patients. Oncology. 2005;69:159–66.PubMed Yonenaga Y, Mori A, Onodera H, et al. Absence of smooth muscle actin-positive pericyte coverage of tumor vessels correlates with hematogenous metastasis and prognosis of colorectal cancer patients. Oncology. 2005;69:159–66.PubMed
19.
go back to reference Baluk P, Morikawa S, Haskell A, Mancuso M, McDonald DM. Abnormalities of basement membrane on blood vessels and endothelial sprouts in tumors. Am J Pathol. 2002;160:985–1000.PubMedPubMedCentral Baluk P, Morikawa S, Haskell A, Mancuso M, McDonald DM. Abnormalities of basement membrane on blood vessels and endothelial sprouts in tumors. Am J Pathol. 2002;160:985–1000.PubMedPubMedCentral
20.
go back to reference Raza A, Franklin MJ, Dudek AZ. Pericytes and vessel maturation during tumor angiogenesis and metastasis. Am J Hematol. 2010;85:593–8.PubMed Raza A, Franklin MJ, Dudek AZ. Pericytes and vessel maturation during tumor angiogenesis and metastasis. Am J Hematol. 2010;85:593–8.PubMed
21.
go back to reference Hosaka K, Yang Y, Seki T, et al. Pericyte-fibroblast transition promotes tumor growth and metastasis. Proc Natl Acad Sci USA. 2016;113:5618–27. Hosaka K, Yang Y, Seki T, et al. Pericyte-fibroblast transition promotes tumor growth and metastasis. Proc Natl Acad Sci USA. 2016;113:5618–27.
22.
go back to reference Supakul S, Yao K, Ochi H, et al. Pericytes as a source of osteogenic cells in bone fracture healing. Int J Mol Sci. 2019;20:1–14. Supakul S, Yao K, Ochi H, et al. Pericytes as a source of osteogenic cells in bone fracture healing. Int J Mol Sci. 2019;20:1–14.
23.
go back to reference Dellavalle A, Sampaolesi M, Tonlorenzi R, et al. Pericytes of human skeletal muscle are myogenic precursors distinct from satellite cells. Nat Cell Biol. 2007;9:255–67.PubMed Dellavalle A, Sampaolesi M, Tonlorenzi R, et al. Pericytes of human skeletal muscle are myogenic precursors distinct from satellite cells. Nat Cell Biol. 2007;9:255–67.PubMed
24.
go back to reference Farrington-Rock C, Crofts NJ, Doherty MJ, Ashton BA, Griffin-Jones C, Canfield AE. Chondrogenic and adipogenic potential of microvascular pericytes. Circulation. 2004;110:2226–32.PubMed Farrington-Rock C, Crofts NJ, Doherty MJ, Ashton BA, Griffin-Jones C, Canfield AE. Chondrogenic and adipogenic potential of microvascular pericytes. Circulation. 2004;110:2226–32.PubMed
25.
26.
go back to reference Lu C, Shahzad MM, Moreno-Smith M, et al. Targeting pericytes with a PDGF-B aptamer in human ovarian carcinoma models. Cancer Biol Ther. 2010;3:176–82. Lu C, Shahzad MM, Moreno-Smith M, et al. Targeting pericytes with a PDGF-B aptamer in human ovarian carcinoma models. Cancer Biol Ther. 2010;3:176–82.
27.
go back to reference Zhou W, Chen C, Shi Y, et al. Targeting glioma stem cell-derived pericytes disrupts the blood-tumor barrier and improves chemotherapeutic efficacy. Cell Stem Cell. 2017;5:591–603. Zhou W, Chen C, Shi Y, et al. Targeting glioma stem cell-derived pericytes disrupts the blood-tumor barrier and improves chemotherapeutic efficacy. Cell Stem Cell. 2017;5:591–603.
28.
go back to reference Guerra DAP, Paiva AE, Sena IFG, Azevedo PO, Silva WN, Mintz A, Birbrair A. Targeting glioblastoma-derived pericytes improves chemotherapeutic outcome. Angiogenesis. 2018;4:667–75. Guerra DAP, Paiva AE, Sena IFG, Azevedo PO, Silva WN, Mintz A, Birbrair A. Targeting glioblastoma-derived pericytes improves chemotherapeutic outcome. Angiogenesis. 2018;4:667–75.
29.
go back to reference Thijssen VL, Paulis YW, Nowak-Sliwinska P, et al. Targeting PDGF-mediated recruitment of pericytes blocks vascular mimicry and tumor growth. J Pathol. 2018;4:447–58. Thijssen VL, Paulis YW, Nowak-Sliwinska P, et al. Targeting PDGF-mediated recruitment of pericytes blocks vascular mimicry and tumor growth. J Pathol. 2018;4:447–58.
30.
go back to reference Liu SY, Chang LC, Pan LF, Hung YJ, Lee CH, Shieh YS. Clinicopathologic significance of tumor cell-lined vessel and microenvironment in oral squamous cell carcinoma. Oral Oncol. 2008;44:277–85.PubMed Liu SY, Chang LC, Pan LF, Hung YJ, Lee CH, Shieh YS. Clinicopathologic significance of tumor cell-lined vessel and microenvironment in oral squamous cell carcinoma. Oral Oncol. 2008;44:277–85.PubMed
31.
go back to reference Margaritescu C, Simionescu C, Pirici D, Mogoanta L, Ciurea R, Stepan A. Immunohistochemical characterization of tumoral vessels in oral squamous cell carcinoma. Rom J Morphol Embryol. 2008;49:447–58.PubMed Margaritescu C, Simionescu C, Pirici D, Mogoanta L, Ciurea R, Stepan A. Immunohistochemical characterization of tumoral vessels in oral squamous cell carcinoma. Rom J Morphol Embryol. 2008;49:447–58.PubMed
32.
go back to reference Li C, Sun CJ, Fan JC, et al. Angiopoietin-2 expression is correlated with angiogenesis and overall survival in oral squamous cell carcinoma. Med Oncol. 2013;30:1–10. Li C, Sun CJ, Fan JC, et al. Angiopoietin-2 expression is correlated with angiogenesis and overall survival in oral squamous cell carcinoma. Med Oncol. 2013;30:1–10.
33.
go back to reference Zhou H, Yang Y-H, Basile J. The Semaphorin 4D- Plexin-B1- RhoA signaling axis recruits pericytes and regulates vascular permeability through endothelial production of PDGF-B and ANGPTL4. Angiogenesis. 2014;17:261–74.PubMed Zhou H, Yang Y-H, Basile J. The Semaphorin 4D- Plexin-B1- RhoA signaling axis recruits pericytes and regulates vascular permeability through endothelial production of PDGF-B and ANGPTL4. Angiogenesis. 2014;17:261–74.PubMed
34.
go back to reference Chung TK, Warram J, Day KE, Hartman Y, Rosenthal EL. Time-dependent pretreatment with bevacuzimab increases tumor specific uptake of cetuximab in preclinical oral cavity cancer studies. Cancer Biol Ther. 2015;16:790–8.PubMedPubMedCentral Chung TK, Warram J, Day KE, Hartman Y, Rosenthal EL. Time-dependent pretreatment with bevacuzimab increases tumor specific uptake of cetuximab in preclinical oral cavity cancer studies. Cancer Biol Ther. 2015;16:790–8.PubMedPubMedCentral
35.
go back to reference Ludwig N, Yerneni SS, Razzo BM, Whiteside TL. Exosomes from HNSCC promote angiogenesis through reprogramming of endothelial cells. Mol Cancer Res. 2018;16:1798–808.PubMed Ludwig N, Yerneni SS, Razzo BM, Whiteside TL. Exosomes from HNSCC promote angiogenesis through reprogramming of endothelial cells. Mol Cancer Res. 2018;16:1798–808.PubMed
36.
go back to reference Prince AC, Patel NG, Moore LS, et al. Adjuvant anti-angiogenic therapy enhances chemotherapeutic uptake in a murine model of head and neck cancer. J Drug Target. 2018;27:193–200.PubMed Prince AC, Patel NG, Moore LS, et al. Adjuvant anti-angiogenic therapy enhances chemotherapeutic uptake in a murine model of head and neck cancer. J Drug Target. 2018;27:193–200.PubMed
37.
go back to reference Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med. 2009;151:264–9.PubMed Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med. 2009;151:264–9.PubMed
38.
go back to reference Hooijmans CR, Rovers MM, de Vries RBM, Leenaars M, Ritskes-Hoitinga M, Langendam MW. SYRCLE’s risk of bias tool for animal studies. BMC Med Res Methodol. 2014;14:1–9. Hooijmans CR, Rovers MM, de Vries RBM, Leenaars M, Ritskes-Hoitinga M, Langendam MW. SYRCLE’s risk of bias tool for animal studies. BMC Med Res Methodol. 2014;14:1–9.
39.
go back to reference Moola S, Munn Z, Tufanaru C, et al (2017) Checklist for analytical cross sectional studies. JBI Reviewer's Manual Moola S, Munn Z, Tufanaru C, et al (2017) Checklist for analytical cross sectional studies. JBI Reviewer's Manual
40.
go back to reference Vanlandewijck M, He L, Mäe MA, et al. A molecular atlas of cell types and zonation in the brain vasculature. Nature. 2018;554:475–80.PubMed Vanlandewijck M, He L, Mäe MA, et al. A molecular atlas of cell types and zonation in the brain vasculature. Nature. 2018;554:475–80.PubMed
41.
go back to reference Lindahl P, Johansson BR, Levéen P, Betsholtz C. Pericyte loss and microaneurysm formation in PDGF-B-deficient mice. Science. 1997;277:242–5.PubMed Lindahl P, Johansson BR, Levéen P, Betsholtz C. Pericyte loss and microaneurysm formation in PDGF-B-deficient mice. Science. 1997;277:242–5.PubMed
42.
go back to reference Stratman AN, Malotte KM, Mahan RD, et al. Pericyte recruitment during vasculogenic tube assembly stimulates endothelial basement membrane matrix formation. Blood. 2009;114:5091–101.PubMedPubMedCentral Stratman AN, Malotte KM, Mahan RD, et al. Pericyte recruitment during vasculogenic tube assembly stimulates endothelial basement membrane matrix formation. Blood. 2009;114:5091–101.PubMedPubMedCentral
43.
go back to reference Velez DO, Tsui B, Goshia T, et al. 3D collagen architecture induces a conserved migratory and transcriptional response linked to vasculogenic mimicry. Nat Commun. 2017;8:1651.PubMedPubMedCentral Velez DO, Tsui B, Goshia T, et al. 3D collagen architecture induces a conserved migratory and transcriptional response linked to vasculogenic mimicry. Nat Commun. 2017;8:1651.PubMedPubMedCentral
45.
go back to reference Hall CN, Reynell C, Gesslein B, et al. Capillary pericytes regulate cerebral blood flow in health and disease. Nature. 2014;7494:55–60. Hall CN, Reynell C, Gesslein B, et al. Capillary pericytes regulate cerebral blood flow in health and disease. Nature. 2014;7494:55–60.
46.
47.
go back to reference Asada N, Kunisaki Y, Pierce H, et al. Differential cytokine contributions of perivascular haematopoietic stem cell niches. Nat Cell Biol. 2017;19:214–23.PubMedPubMedCentral Asada N, Kunisaki Y, Pierce H, et al. Differential cytokine contributions of perivascular haematopoietic stem cell niches. Nat Cell Biol. 2017;19:214–23.PubMedPubMedCentral
48.
go back to reference Azevedo PO, Sena IFG, Andreotti JP, et al. Pericytes modulate myelination in the central nervous system. J Cell Physiol. 2018;8:5523–9. Azevedo PO, Sena IFG, Andreotti JP, et al. Pericytes modulate myelination in the central nervous system. J Cell Physiol. 2018;8:5523–9.
49.
go back to reference Borges I, Sena I, Azevedo P, et al. Lung as a niche for hematopoietic progenitors. Stem Cell Rev. 2017;13:567–74.PubMedCentral Borges I, Sena I, Azevedo P, et al. Lung as a niche for hematopoietic progenitors. Stem Cell Rev. 2017;13:567–74.PubMedCentral
50.
go back to reference Murgai M, Ju W, Eason M, et al. KLF4-dependent perivascular cell plasticity mediates pre-metastatic niche formation and metastasis. Nat Med. 2018;23:1176–90. Murgai M, Ju W, Eason M, et al. KLF4-dependent perivascular cell plasticity mediates pre-metastatic niche formation and metastasis. Nat Med. 2018;23:1176–90.
51.
go back to reference Hill RA, Tong L, Yuan P, Murikinati S, Gupta S, Grutzendler J. Regional blood flow in the normal and ischemic brain is controlled by arteriolar smooth muscle cell contractility and not by capillary pericytes. Neuron. 2015;87:95–110.PubMedPubMedCentral Hill RA, Tong L, Yuan P, Murikinati S, Gupta S, Grutzendler J. Regional blood flow in the normal and ischemic brain is controlled by arteriolar smooth muscle cell contractility and not by capillary pericytes. Neuron. 2015;87:95–110.PubMedPubMedCentral
52.
go back to reference Guimaraes-Camboa N, Cattaneo P, Sun Y, et al. Pericytes of multiple organs do not behave as mesenchymal stem cells in vivo. Cell Stem Cell. 2017;20:345–59.PubMedPubMedCentral Guimaraes-Camboa N, Cattaneo P, Sun Y, et al. Pericytes of multiple organs do not behave as mesenchymal stem cells in vivo. Cell Stem Cell. 2017;20:345–59.PubMedPubMedCentral
53.
go back to reference Birbrair A, Zhang T, Wang ZM, Messi ML, Enikolopov GN, Mintz A, Delbono O. Role of pericytes in skeletal muscle regeneration and fat accumulation. Stem Cells Dev. 2013;16:2298–314. Birbrair A, Zhang T, Wang ZM, Messi ML, Enikolopov GN, Mintz A, Delbono O. Role of pericytes in skeletal muscle regeneration and fat accumulation. Stem Cells Dev. 2013;16:2298–314.
54.
go back to reference Birbrair A, Zhang T, Wang ZM, Messi ML, Mintz A, Delbono O. Pericytes at the intersection between tissue regeneration and pathology. Clin Sci. 2015;128:81–93. Birbrair A, Zhang T, Wang ZM, Messi ML, Mintz A, Delbono O. Pericytes at the intersection between tissue regeneration and pathology. Clin Sci. 2015;128:81–93.
55.
go back to reference Shivamallappa SM, Venkatraman NT, Shreedhar B, Mohanty L, Shenoy S. Role of angiogenesis in oral squamous cell carcinoma development and metastasis: an immunohistochemical study. Int J Oral Sci. 2011;3:216–24.PubMedPubMedCentral Shivamallappa SM, Venkatraman NT, Shreedhar B, Mohanty L, Shenoy S. Role of angiogenesis in oral squamous cell carcinoma development and metastasis: an immunohistochemical study. Int J Oral Sci. 2011;3:216–24.PubMedPubMedCentral
57.
go back to reference Ozawa MG, Yao VJ, Chanthery YH, et al. Angiogenesis with pericyte abnormalities in a transgenic model of prostate carcinoma. Cancer. 2005;10:2104–15. Ozawa MG, Yao VJ, Chanthery YH, et al. Angiogenesis with pericyte abnormalities in a transgenic model of prostate carcinoma. Cancer. 2005;10:2104–15.
58.
go back to reference Basile JR, Castilho RM, Williams VP, Gutkind JS. Semaphorin 4D provides a link between axon guidance processes and tumor-induced angiogenesis. Proc Natl Acad Sci USA. 2006;103:9017–22.PubMedPubMedCentral Basile JR, Castilho RM, Williams VP, Gutkind JS. Semaphorin 4D provides a link between axon guidance processes and tumor-induced angiogenesis. Proc Natl Acad Sci USA. 2006;103:9017–22.PubMedPubMedCentral
59.
go back to reference Saleem SN, Abdel-Mageed AB. Tumor-derived exosomes in oncogenic reprogramming and cancer progression. Cell Mol Life Sci. 2015;72:1–10.PubMed Saleem SN, Abdel-Mageed AB. Tumor-derived exosomes in oncogenic reprogramming and cancer progression. Cell Mol Life Sci. 2015;72:1–10.PubMed
60.
61.
go back to reference Ning X, Zhang H, Wang C, Song X. Exosomes released by gastric cancer cells induce transition of pericytes into cancer-associated fibroblasts. Med Sci Monit. 2018;24:2350–9.PubMedPubMedCentral Ning X, Zhang H, Wang C, Song X. Exosomes released by gastric cancer cells induce transition of pericytes into cancer-associated fibroblasts. Med Sci Monit. 2018;24:2350–9.PubMedPubMedCentral
62.
go back to reference Ishii G, Ochiai A, Neri S. Phenotypic and functional heterogeneity of cancer-associated fibroblast within the tumor microenvironment. Adv Drug Deliv Rev. 2016;1:186–96. Ishii G, Ochiai A, Neri S. Phenotypic and functional heterogeneity of cancer-associated fibroblast within the tumor microenvironment. Adv Drug Deliv Rev. 2016;1:186–96.
63.
go back to reference Kalluri R, Zeisberg M. Fibroblasts in cancer. Nat Rev Cancer. 2006;6:392–401.PubMed Kalluri R, Zeisberg M. Fibroblasts in cancer. Nat Rev Cancer. 2006;6:392–401.PubMed
64.
go back to reference Voisin MB, Pröbstl D, Nourshargh S. Venular basement membranes ubiquitously express matrix protein low-expression regions. Am J Pathol. 2010;176:482–95.PubMedPubMedCentral Voisin MB, Pröbstl D, Nourshargh S. Venular basement membranes ubiquitously express matrix protein low-expression regions. Am J Pathol. 2010;176:482–95.PubMedPubMedCentral
65.
go back to reference Zhang L, Wang Y, Rashid MH. Malignant pericytes expressing GT198 give rise to tumor cells through angiogenesis. Oncotarget. 2017;8:51591–607.PubMedPubMedCentral Zhang L, Wang Y, Rashid MH. Malignant pericytes expressing GT198 give rise to tumor cells through angiogenesis. Oncotarget. 2017;8:51591–607.PubMedPubMedCentral
66.
go back to reference Lugano R, Ramachandran M, Dimberg A. Tumor angiogenesis: causes, consequences, challenges and opportunities. Cell Mol Life Sci. 2019;77:1745–70.PubMedPubMedCentral Lugano R, Ramachandran M, Dimberg A. Tumor angiogenesis: causes, consequences, challenges and opportunities. Cell Mol Life Sci. 2019;77:1745–70.PubMedPubMedCentral
67.
go back to reference Maj E, Papiernik D, Wietrzyk J. Antiangiogenic cancer treatment: The great discovery and greater complexity. Int J Oncol. 2016;5:1773–844. Maj E, Papiernik D, Wietrzyk J. Antiangiogenic cancer treatment: The great discovery and greater complexity. Int J Oncol. 2016;5:1773–844.
68.
go back to reference Loges S, Schmidt T, Carmeliet P. Mechanisms of resistance to anti-angiogenic therapy and development of third-generation anti-angiogenic drug candidates. Genes Cancer. 2010;1:12–25.PubMedPubMedCentral Loges S, Schmidt T, Carmeliet P. Mechanisms of resistance to anti-angiogenic therapy and development of third-generation anti-angiogenic drug candidates. Genes Cancer. 2010;1:12–25.PubMedPubMedCentral
69.
go back to reference Bergers G, Song S, Meyer-Morse N, Bergsland E, Hanahan D. Benefits of targeting both pericytes and endothelial cells in the tumor vasculature with kinase inhibitors. J Clin Investig. 2003;111:1287–95.PubMedPubMedCentral Bergers G, Song S, Meyer-Morse N, Bergsland E, Hanahan D. Benefits of targeting both pericytes and endothelial cells in the tumor vasculature with kinase inhibitors. J Clin Investig. 2003;111:1287–95.PubMedPubMedCentral
70.
go back to reference Meng MB, Zaorsky NG, Deng L, et al. Pericytes: a double-edged sword in cancer therapy. Future Oncol. 2015;11:169–79.PubMed Meng MB, Zaorsky NG, Deng L, et al. Pericytes: a double-edged sword in cancer therapy. Future Oncol. 2015;11:169–79.PubMed
71.
go back to reference Koonce NA, Griffin RJ, Dings RPM. Galectin-1 inhibitor otx008 induces tumor vessel normalization and tumor growth inhibition in human head and neck squamous cell carcinoma models. Int J Mol Sci. 2017;18:1–9. Koonce NA, Griffin RJ, Dings RPM. Galectin-1 inhibitor otx008 induces tumor vessel normalization and tumor growth inhibition in human head and neck squamous cell carcinoma models. Int J Mol Sci. 2017;18:1–9.
72.
go back to reference Mondini M, Nizard M, Tran T, et al. Synergy of radiotherapy and a cancer vaccine for the treatment of HPV-associated head and neck cancer. Mol Cancer Ther. 2015;6:1336–455. Mondini M, Nizard M, Tran T, et al. Synergy of radiotherapy and a cancer vaccine for the treatment of HPV-associated head and neck cancer. Mol Cancer Ther. 2015;6:1336–455.
73.
go back to reference Nisancioglu MH, Betsholtz C, Genové G. The absence of pericytes does not increase the sensitivity of tumor vasculature to vascular endothelial growth factor-A blockade. Cancer Res. 2010;70:5109–15.PubMed Nisancioglu MH, Betsholtz C, Genové G. The absence of pericytes does not increase the sensitivity of tumor vasculature to vascular endothelial growth factor-A blockade. Cancer Res. 2010;70:5109–15.PubMed
Metadata
Title
Pericyte in Oral Squamous Cell Carcinoma: A Systematic Review
Authors
Isabella Bittencourt Valle
Lauren Frenzel Schuch
Janine Mayra da Silva
Alfonso Gala-García
Ivana Márcia Alves Diniz
Alexander Birbrair
Lucas Guimarães Abreu
Tarcília Aparecida Silva
Publication date
01-12-2020
Publisher
Springer US
Published in
Head and Neck Pathology / Issue 4/2020
Electronic ISSN: 1936-0568
DOI
https://doi.org/10.1007/s12105-020-01188-2

Other articles of this Issue 4/2020

Head and Neck Pathology 4/2020 Go to the issue