Abstract
Glioma is the prevalent aggressive primary brain tumor, with a very poor prognosis. The absence of advanced understanding of the roles played by the cells within the glioma microenvironment limits the development of effective drugs. A recent study indicates that periostin expressed by pericytes is crucial for glioma angiogenesis. Here, we describe succinctly the results and implications of this discovery in what we know about pericytes within the glioma microenvironment. The emerging knowledge from this work will benefit the development of therapies for gliomas.
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References
Allsopp G, Gamble HJ (1979) An electron microscopic study of the pericytes of the developing capillaries in human fetal brain and muscle. J Anat 128(Pt 1):155–168
Almeida VM, Paiva AE, Sena IFG, Mintz A, Magno LAV, Birbrair A (2018) Pericytes make spinal cord breathless after injury. Neuroscientist 24(5):440–447. https://doi.org/10.1177/1073858417731522
Andreotti JP, Lousado L, Magno LAV, Birbrair A (2017) Hypothalamic neurons take center stage in the neural stem cell niche. Cell Stem Cell 21(3):293–294. https://doi.org/10.1016/j.stem.2017.08.005
Andreotti JP, Paiva AE, Prazeres P, Guerra DAP, Silva WN, Vaz RS, Mintz A, Birbrair A (2018a) The role of natural killer cells in the uterine microenvironment during pregnancy. Cell Mol Immunol 15(11):941–943. https://doi.org/10.1038/s41423-018-0023-1
Andreotti JP, Prazeres P, Magno LAV, Romano-Silva MA, Mintz A, Birbrair A (2018b) Neurogenesis in the postnatal cerebellum after injury. Int J Dev Neurosci 67:33–36. https://doi.org/10.1016/j.ijdevneu.2018.03.002
Andreotti JP, Silva WN, Costa AC, Picoli CC, Bitencourt FCO, Coimbra-Campos LMC, Resende RR, Magno LAV, Romano-Silva MA, Mintz A, Birbrair A (2019) Neural stem cell niche heterogeneity. Semin Cell Dev Biol 95:42–53. https://doi.org/10.1016/j.semcdb.2019.01.005
Armulik A, Genove G, Betsholtz C (2011) Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev Cell 21(2):193–215. https://doi.org/10.1016/j.devcel.2011.07.001
Asada N, Kunisaki Y, Pierce H, Wang Z, Fernandez NF, Birbrair A, Ma'ayan A, Frenette PS (2017) Differential cytokine contributions of perivascular haematopoietic stem cell niches. Nat Cell Biol 19(3):214–223. https://doi.org/10.1038/ncb3475
Azevedo PO, Lousado L, Paiva AE, Andreotti JP, Santos GSP, Sena IFG, Prazeres P, Filev R, Mintz A, Birbrair A (2017) Endothelial cells maintain neural stem cells quiescent in their niche. Neuroscience 363:62–65. https://doi.org/10.1016/j.neuroscience.2017.08.059
Azevedo PO, Paiva AE, Santos GSP, Lousado L, Andreotti JP, Sena IFG, Tagliati CA, Mintz A, Birbrair A (2018a) Cross-talk between lung cancer and bones results in neutrophils that promote tumor progression. Cancer Metastasis Rev 37(4):779–790. https://doi.org/10.1007/s10555-018-9759-4
Azevedo PO, Sena IFG, Andreotti JP, Carvalho-Tavares J, Alves-Filho JC, Cunha TM, Cunha FQ, Mintz A, Birbrair A (2018b) Pericytes modulate myelination in the central nervous system. J Cell Physiol 233(8):5523–5529. https://doi.org/10.1002/jcp.26348
Balabanov R, Beaumont T, Dore-Duffy P (1999) Role of central nervous system microvascular pericytes in activation of antigen-primed splenic T-lymphocytes. J Neurosci Res 55(5):578–587
Balabanov R, Washington R, Wagnerova J, Dore-Duffy P (1996) CNS microvascular pericytes express macrophage-like function, cell surface integrin alpha M, and macrophage marker ED-2. Microvasc Res 52(2):127–142. https://doi.org/10.1006/mvre.1996.0049
Bechmann I, Priller J, Kovac A, Bontert M, Wehner T, Klett FF, Bohsung J, Stuschke M, Dirnagl U, Nitsch R (2001) Immune surveillance of mouse brain perivascular spaces by blood-borne macrophages. Eur J Neurosci 14(10):1651–1658
Bell RD, Winkler EA, Sagare AP, Singh I, LaRue B, Deane R, Zlokovic BV (2010) Pericytes control key neurovascular functions and neuronal phenotype in the adult brain and during brain aging. Neuron 68(3):409–427. https://doi.org/10.1016/j.neuron.2010.09.043
Birbrair A (2017) Stem cell microenvironments and beyond. Adv Exp Med Biol 1041:1–3. https://doi.org/10.1007/978-3-319-69194-7_1
Birbrair A, Borges IDT, Gilson Sena IF, Almeida GG, da Silva ML, Goncalves R, Mintz A, Delbono O (2017a) How plastic are pericytes? Stem Cells Dev 26(14):1013–1019. https://doi.org/10.1089/scd.2017.0044
Birbrair A, Delbono O (2015) Pericytes are essential for skeletal muscle formation. Stem Cell Rev 11(4):547–548. https://doi.org/10.1007/s12015-015-9588-6
Birbrair A, Frenette PS (2016) Niche heterogeneity in the bone marrow. Ann N Y Acad Sci 1370(1):82–96. https://doi.org/10.1111/nyas.13016
Birbrair A, Sattiraju A, Zhu D, Zulato G, Batista I, Nguyen VT, Messi ML, Solingapuram Sai KK, Marini FC, Delbono O, Mintz A (2017b) Novel peripherally derived neural-like stem cells as therapeutic carriers for treating glioblastomas. Stem Cells Trans Med 6(2):471–481. https://doi.org/10.5966/sctm.2016-0007
Birbrair A, Wang ZM, Messi ML, Enikolopov GN, Delbono O (2011) Nestin-GFP transgene reveals neural precursor cells in adult skeletal muscle. PLoS One 6(2):e16816. https://doi.org/10.1371/journal.pone.0016816
Birbrair A, Zhang T, Files DC, Mannava S, Smith T, Wang ZM, Messi ML, Mintz A, Delbono O (2014a) Type-1 pericytes accumulate after tissue injury and produce collagen in an organ-dependent manner. Stem Cell Res Ther 5(6):122. https://doi.org/10.1186/scrt512
Birbrair A, Zhang T, Wang ZM, Messi ML, Enikolopov GN, Mintz A, Delbono O (2013a) Role of pericytes in skeletal muscle regeneration and fat accumulation. Stem Cells Dev 22(16):2298–2314. https://doi.org/10.1089/scd.2012.0647
Birbrair A, Zhang T, Wang ZM, Messi ML, Enikolopov GN, Mintz A, Delbono O (2013b) Skeletal muscle neural progenitor cells exhibit properties of NG2-glia. Exp Cell Res 319(1):45–63. https://doi.org/10.1016/j.yexcr.2012.09.008
Birbrair A, Zhang T, Wang ZM, Messi ML, Enikolopov GN, Mintz A, Delbono O (2013c) Skeletal muscle pericyte subtypes differ in their differentiation potential. Stem Cell Res 10(1):67–84. https://doi.org/10.1016/j.scr.2012.09.003
Birbrair A, Zhang T, Wang ZM, Messi ML, Mintz A, Delbono O (2013d) Type-1 pericytes participate in fibrous tissue deposition in aged skeletal muscle. Am J Physiol Cell Physiol 305(11):C1098–1113. https://doi.org/10.1152/ajpcell.00171.2013
Birbrair A, Zhang T, Wang ZM, Messi ML, Mintz A, Delbono O (2014b) Pericytes: multitasking cells in the regeneration of injured, diseased, and aged skeletal muscle. Frontiers Aging Neurosci 6:245. https://doi.org/10.3389/fnagi.2014.00245
Birbrair A, Zhang T, Wang ZM, Messi ML, Mintz A, Delbono O (2015) Pericytes at the intersection between tissue regeneration and pathology. Clin Sci 128(2):81–93. https://doi.org/10.1042/CS20140278
Birbrair A, Zhang T, Wang ZM, Messi ML, Olson JD, Mintz A, Delbono O (2014c) Type-2 pericytes participate in normal and tumoral angiogenesis. Am J Physiol Cell Physiol 307(1):C25–38. https://doi.org/10.1152/ajpcell.00084.2014
Borges IDT, Sena IFG, de Azevedo PO, Andreotti JP, de Almeida VM, de Paiva AE, Pinheiro Dos Santos GS, de Paula Guerra DA, Dias Moura Prazeres PH, Mesquita LL, B. SLS, Leonel C, Mintz A, Birbrair A, (2017) Lung as a niche for hematopoietic progenitors. Stem Cell Rev Rep. https://doi.org/10.1007/s12015-017-9747-z
Bouchard BA, Shatos MA, Tracy PB (1997) Human brain pericytes differentially regulate expression of procoagulant enzyme complexes comprising the extrinsic pathway of blood coagulation. Arterioscler Thromb Vasc Biol 17(1):1–9
Buckingham ME, Meilhac SM (2011) Tracing cells for tracking cell lineage and clonal behavior. Dev Cell 21(3):394–409. https://doi.org/10.1016/j.devcel.2011.07.019
Caspani EM, Crossley PH, Redondo-Garcia C, Martinez S (2014) Glioblastoma: a pathogenic crosstalk between tumor cells and pericytes. PLoS One 9(7):e101402. https://doi.org/10.1371/journal.pone.0101402
Castejon OJ (2011) Ultrastructural pathology of cortical capillary pericytes in human traumatic brain oedema. Folia Neuropathologica 49(3):162–173
Cheng L, Huang Z, Zhou W, Wu Q, Donnola S, Liu JK, Fang X, Sloan AE, Mao Y, Lathia JD, Min W, McLendon RE, Rich JN, Bao S (2013) Glioblastoma stem cells generate vascular pericytes to support vessel function and tumor growth. Cell 153(1):139–152. https://doi.org/10.1016/j.cell.2013.02.021
Coatti GC, Frangini M, Valadares MC, Gomes JP, Lima NO, Cavacana N, Assoni AF, Pelatti MV, Birbrair A, de Lima ACP, Singer JM, Rocha FMM, Da Silva GL, Mantovani MS, Macedo-Souza LI, Ferrari MFR, Zatz M (2017) Pericytes extend survival of ALS SOD1 mice and induce the expression of antioxidant enzymes in the murine model and in IPSCs derived neuronal cells from an ALS patient. Stem Cell Rev Rep 13(5):686–698. https://doi.org/10.1007/s12015-017-9752-2
Costa MA, Paiva AE, Andreotti JP, Cardoso MV, Cardoso CD, Mintz A, Birbrair A (2018) Pericytes constrict blood vessels after myocardial ischemia. J Mol Cell Cardiol. https://doi.org/10.1016/j.yjmcc.2018.01.014
Crisan M, Corselli M, Chen WC, Peault B (2012) Perivascular cells for regenerative medicine. J Cell Mol Med. https://doi.org/10.1111/j.1582-4934.2012.01617.x
de Alvarenga EC, Silva WN, Vasconcellos R, Paredes-Gamero EJ, Mintz A, Birbrair A (2018) Promyelocytic leukemia protein in mesenchymal stem cells is essential for leukemia progression. Ann Hematol 97(10):1749–1755. https://doi.org/10.1007/s00277-018-3463-x
De Vleeschouwer S, Bergers G (2017) Glioblastoma: to target the tumor cell or the microenvironment? In: De Vleeschouwer S (ed) Glioblastoma. Brisbane (AU). https://doi.org/10.15586/codon.glioblastoma.2017.ch16
Dias Moura Prazeres PH, Sena IFG, Borges IDT, de Azevedo PO, Andreotti JP, de Paiva AE, de Almeida VM, de Paula Guerra DA, Pinheiro Dos Santos GS, Mintz A, Delbono O, Birbrair A (2017) Pericytes are heterogeneous in their origin within the same tissue. Dev Biol 427(1):6–11. https://doi.org/10.1016/j.ydbio.2017.05.001
Enge M, Bjarnegard M, Gerhardt H, Gustafsson E, Kalen M, Asker N, Hammes HP, Shani M, Fassler R, Betsholtz C (2002) Endothelium-specific platelet-derived growth factor-B ablation mimics diabetic retinopathy. EMBO J 21(16):4307–4316
Fabry Z, Fitzsimmons KM, Herlein JA, Moninger TO, Dobbs MB, Hart MN (1993) Production of the cytokines interleukin 1 and 6 by murine brain microvessel endothelium and smooth muscle pericytes. J Neuroimmunol 47(1):23–34
Fisher M (2009) Pericyte signaling in the neurovascular unit. Stroke 40(3 Suppl):S13–15. https://doi.org/10.1161/STROKEAHA.108.533117
Gerl K, Miquerol L, Todorov VT, Hugo CP, Adams RH, Kurtz A, Kurt B (2015) Inducible glomerular erythropoietin production in the adult kidney. Kidney Int 88(6):1345–1355. https://doi.org/10.1038/ki.2015.274
Goncalves WA, Rezende BM, de Oliveira MPE, Ribeiro LS, Fattori V, da Silva WN, Prazeres P, Queiroz-Junior CM, Santana KTO, Costa WC, Beltrami VA, Costa VV, Birbrair A, Verri WA Jr, Lopes F, Cunha TM, Teixeira MM, Amaral FA, Pinho V (2019) Sensory Ganglia-specific TNF expression is associated with persistent nociception after resolution of inflammation. Front Immunol 10:3120. https://doi.org/10.3389/fimmu.2019.03120
Göritz C, Dias DO, Tomilin N, Barbacid M, Shupliakov O, Frisén J (2011) A pericyte origin of spinal cord scar tissue. Science 333(6039):238–242
Guerra DAP, Paiva AE, Sena IFG, Azevedo PO, Batista ML Jr, Mintz A, Birbrair A (2018a) Adipocytes role in the bone marrow niche. Cytometry A 93(2):167–171. https://doi.org/10.1002/cyto.a.23301
Guerra DAP, Paiva AE, Sena IFG, Azevedo PO, Silva WN, Mintz A, Birbrair A (2018b) Targeting glioblastoma-derived pericytes improves chemotherapeutic outcome. Angiogenesis 21(4):667–675. https://doi.org/10.1007/s10456-018-9621-x
Guillemin GJ, Brew BJ (2004) Microglia, macrophages, perivascular macrophages, and pericytes: a review of function and identification. J Leukoc Biol 75(3):388–397. https://doi.org/10.1189/jlb.0303114
Hasan M, Glees P (1990) The fine structure of human cerebral perivascular pericytes and juxtavascular phagocytes: their possible role in hydrocephalic edema resolution. J Hirnforsch 31(2):237–249
Hellstrom M, Gerhardt H, Kalen M, Li X, Eriksson U, Wolburg H, Betsholtz C (2001) Lack of pericytes leads to endothelial hyperplasia and abnormal vascular morphogenesis. J Cell Biol 153(3):543–553
Henriques F, Lopes MA, Franco FO, Knobl P, Santos KB, Bueno LL, Correa VA, Bedard AH, Guilherme A, Birbrair A, Peres SB, Farmer SR, Batista ML Jr (2018) Toll-like receptor-4 disruption suppresses adipose tissue remodeling and increases survival in cancer cachexia syndrome. Sci Rep 8(1):18024. https://doi.org/10.1038/s41598-018-36626-3
Hong LZ, Wei XW, Chen JF, Shi Y (2013) Overexpression of periostin predicts poor prognosis in non-small cell lung cancer. Oncol Lett 6(6):1595–1603. https://doi.org/10.3892/ol.2013.1590
Huizer K, Zhu C, Chirifi I, Krist B, Zorgman D, van der Weiden M, van den Bosch TPP, Dumas J, Cheng C, Kros JM, Mustafa DA (2020) Periostin is expressed by pericytes and is crucial for angiogenesis in glioma. J Neuropathol Exp Neurol. https://doi.org/10.1093/jnen/nlaa067
Isasi E, Olivera-Bravo S (2020) Pericytes in neurometabolic diseases. Curr Tissue Microenviron Rep 1:131–141
Jeynes B (1985) Reactions of granular pericytes in a rabbit cerebrovascular ischemia model. Stroke 16(1):121–125
Kamouchi M, Ago T, Kitazono T (2011) Brain pericytes: emerging concepts and functional roles in brain homeostasis. Cell Mol Neurobiol 31(2):175–193. https://doi.org/10.1007/s10571-010-9605-x
Kanashiro A, Hiroki CH, da Fonseca DM, Birbrair A, Ferreira RG, Bassi GS, Fonseca MD, Kusuda R, Cebinelli GCM, da Silva KP, Wanderley CW, Menezes GB, Alves-Fiho JC, Oliveira AG, Cunha TM, Pupo AS, Ulloa L, Cunha FQ (2020) The role of neutrophils in neuro-immune modulation. Pharmacol Res 151:104580. https://doi.org/10.1016/j.phrs.2019.104580
Khan JA, Mendelson A, Kunisaki Y, Birbrair A, Kou Y, Arnal-Estape A, Pinho S, Ciero P, Nakahara F, Ma'ayan A, Bergman A, Merad M, Frenette PS (2016) Fetal liver hematopoietic stem cell niches associate with portal vessels. Science 351(6269):176–180. https://doi.org/10.1126/science.aad0084
Kikuchi Y, Kunita A, Iwata C, Komura D, Nishiyama T, Shimazu K, Takeshita K, Shibahara J, Kii I, Morishita Y, Yashiro M, Hirakawa K, Miyazono K, Kudo A, Fukayama M, Kashima TG (2014) The niche component periostin is produced by cancer-associated fibroblasts, supporting growth of gastric cancer through ERK activation. Am J Pathol 184(3):859–870. https://doi.org/10.1016/j.ajpath.2013.11.012
Kim JA, Tran ND, Li Z, Yang F, Zhou W, Fisher MJ (2006) Brain endothelial hemostasis regulation by pericytes. J Cereb Blood Flow Metab 26(2):209–217. https://doi.org/10.1038/sj.jcbfm.9600181
Krex D, Klink B, Hartmann C, von Deimling A, Pietsch T, Simon M, Sabel M, Steinbach JP, Heese O, Reifenberger G, Weller M, Schackert G, German Glioma N (2007) Long-term survival with glioblastoma multiforme. Brain 130(Pt 10):2596–2606. https://doi.org/10.1093/brain/awm204
Kudo Y, Iizuka S, Yoshida M, Nguyen PT, Siriwardena SB, Tsunematsu T, Ohbayashi M, Ando T, Hatakeyama D, Shibata T, Koizumi K, Maeda M, Ishimaru N, Ogawa I, Takata T (2012) Periostin directly and indirectly promotes tumor lymphangiogenesis of head and neck cancer. PLoS One 7(8):e44488. https://doi.org/10.1371/journal.pone.0044488
Leonel C, Sena IFG, Silva WN, Prazeres P, Fernandes GR, Mancha Agresti P, Martins Drumond M, Mintz A, Azevedo VAC, Birbrair A (2019) Staphylococcus epidermidis role in the skin microenvironment. J Cell Mol Med 23(9):5949–5955. https://doi.org/10.1111/jcmm.14415
Leveen P, Pekny M, Gebre-Medhin S, Swolin B, Larsson E, Betsholtz C (1994) Mice deficient for PDGF B show renal, cardiovascular, and hematological abnormalities. Genes Dev 8(16):1875–1887
Lindahl P, Johansson BR, Leveen P, Betsholtz C (1997) Pericyte loss and microaneurysm formation in PDGF-B-deficient mice. Science 277(5323):242–245
Lousado L, Prazeres P, Andreotti JP, Paiva AE, Azevedo PO, Santos GSP, Filev R, Mintz A, Birbrair A (2017) Schwann cell precursors as a source for adrenal gland chromaffin cells. Cell Death Dis 8(10):e3072. https://doi.org/10.1038/cddis.2017.456
Magno LAV, Tenza-Ferrer H, Collodetti M, Aguiar MFG, Rodrigues APC, da Silva RS, Silva JDP, Nicolau NF, Rosa DVF, Birbrair A, Miranda DM, Romano-Silva MA (2019) Optogenetic stimulation of the M2 cortex reverts motor dysfunction in a mouse model of Parkinson’s disease. J Neurosci 39(17):3234–3248. https://doi.org/10.1523/JNEUROSCI.2277-18.2019
Manini I, Caponnetto F, Bartolini A, Ius T, Mariuzzi L, Di Loreto C, Beltrami AP, Cesselli D (2018) Role of microenvironment in glioma invasion: what we learned from in vitro models. Int J Mol Sci. https://doi.org/10.3390/ijms19010147
Miranda VHS, Gomes TR, Eller DE, Ferraz LCN, Chaves AT, Bicalho KA, Silva CEC, Birbrair A, Pascoal Xavier MA, de Goes AM, Correa-Oliveira R, Alves EAR, Bozzi A (2020) Liver damage in schistosomiasis is reduced by adipose tissue-derived stem cell therapy after praziquantel treatment. PLoS Negl Trop Dis 14(8):e0008635. https://doi.org/10.1371/journal.pntd.0008635
Ostrom QT, Gittleman H, Liao P, Rouse C, Chen Y, Dowling J, Wolinsky Y, Kruchko C, Barnholtz-Sloan J (2014) CBTRUS statistical report: primary brain and central nervous system tumors diagnosed in the United States in 2007–2011. Neuro Oncol 16(Suppl 4):iv1–iv63. https://doi.org/10.1093/neuonc/nou223
Paiva AE, Lousado L, Almeida VM, Andreotti JP, Santos GSP, Azevedo PO, Sena IFG, Prazeres P, Borges IT, Azevedo V, Mintz A, Birbrair A (2017) Endothelial cells as precursors for osteoblasts in the metastatic prostate cancer bone. Neoplasia 19(11):928–931. https://doi.org/10.1016/j.neo.2017.08.007
Paiva AE, Lousado L, Guerra DAP, Azevedo PO, Sena IFG, Andreotti JP, Santos GSP, Goncalves R, Mintz A, Birbrair A (2018) Pericytes in the premetastatic niche. Can Res 78(11):2779–2786. https://doi.org/10.1158/0008-5472.CAN-17-3883
Pallone TL, Zhang Z, Rhinehart K (2003) Physiology of the renal medullary microcirculation. Am J Physiol Renal Physiol 284(2):F253–266. https://doi.org/10.1152/ajprenal.00304.2002
Payne LB, Hoque M, Houk C, Darden J, Chappell JC (2020) Pericytes in vascular development. Curr Tissue Microenviron Rep 1:143–154
Picoli CC, Coimbra-Campos LMC, Guerra DAP, Silva WN, Prazeres P, Costa AC, Magno LAV, Romano-Silva MA, Mintz A, Birbrair A (2019) Pericytes act as key players in spinal cord injury. Am J Pathol 189(7):1327–1337. https://doi.org/10.1016/j.ajpath.2019.03.008
Picoli CC, Costa AC, Rocha BGS, Silva WN, Santos GSP, Prazeres PHDM, Costa PAC, Oropeza A, Silva RA, Azevedo VAC, Resende RR, Cunha TM, Mintz A, Birbrair A (2020) Sensory nerves in the spotlight of the stem cell niche. Stem Cells Transl Med. In press.
Prazeres P, Almeida VM, Lousado L, Andreotti JP, Paiva AE, Santos GSP, Azevedo PO, Souto L, Almeida GG, Filev R, Mintz A, Goncalves R, Birbrair A (2018a) Macrophages generate pericytes in the developing brain. Cell Mol Neurobiol 38(4):777–782. https://doi.org/10.1007/s10571-017-0549-2
Prazeres P, Leonel C, Silva WN, Rocha BGS, Santos GSP, Costa AC, Picoli CC, Sena IFG, Goncalves WA, Vieira MS, Costa PAC, Campos L, Lopes MTP, Costa MR, Resende RR, Cunha TM, Mintz A, Birbrair A (2020) Ablation of sensory nerves favours melanoma progression. J Cell Mol Med. https://doi.org/10.1111/jcmm.15381
Prazeres P, Turquetti AOM, Azevedo PO, Barreto RSN, Miglino MA, Mintz A, Delbono O, Birbrair A (2018b) Perivascular cell alphav integrins as a target to treat skeletal muscle fibrosis. Int J Biochem Cell Biol 99:109–113. https://doi.org/10.1016/j.biocel.2018.04.002
Quail DF, Joyce JA (2013) Microenvironmental regulation of tumor progression and metastasis. Nat Med 19(11):1423–1437. https://doi.org/10.1038/nm.3394
Roberts LM, Munson J (2020) Modulating microenvironments for treating glioblastoma. Curr Tissue Microenviron Rep 1:99–111
Rouget C (1873) Mémoire sur le développement, la structure et les proprietés physiologiques des capillaires sanguins et lymphatiques. Arch de Phys 5:603
Santos GSP, Magno LAV, Romano-Silva MA, Mintz A, Birbrair A (2019) Pericyte plasticity in the brain. Neurosci Bull 35(3):551–560. https://doi.org/10.1007/s12264-018-0296-5
Santos GSP, Prazeres P, Mintz A, Birbrair A (2018) Role of pericytes in the retina. Eye 32(3):483–486. https://doi.org/10.1038/eye.2017.220
Sena IFG, Borges IT, Lousado L, Azevedo PO, Andreotti JP, Almeida VM, Paiva AE, Santos GSP, Guerra DAP, Prazeres P, Souto L, Mintz A, Birbrair A (2017a) LepR+ cells dispute hegemony with Gli1+ cells in bone marrow fibrosis. Cell Cycle 16(21):2018–2022. https://doi.org/10.1080/15384101.2017.1367072
Sena IFG, Paiva AE, Prazeres P, Azevedo PO, Lousado L, Bhutia SK, Salmina AB, Mintz A, Birbrair A (2018) Glioblastoma-activated pericytes support tumor growth via immunosuppression. Cancer Med 7(4):1232–1239. https://doi.org/10.1002/cam4.1375
Sena IFG, Prazeres P, Santos GSP, Borges IT, Azevedo PO, Andreotti JP, Almeida VM, Paiva AE, Guerra DAP, Lousado L, Souto L, Mintz A, Birbrair A (2017b) Identity of Gli1(+) cells in the bone marrow. Exp Hematol 54:12–16. https://doi.org/10.1016/j.exphem.2017.06.349
Silva WN, Leonel C, Prazeres P, Sena IFG, Guerra DAP, Heller D, Diniz IMA, Fortuna V, Mintz A, Birbrair A (2018a) Role of Schwann cells in cutaneous wound healing. Wound Repair Regen 26(5):392–397. https://doi.org/10.1111/wrr.12647
Silva WN, Prazeres P, Paiva AE, Lousado L, Turquetti AOM, Barreto RSN, de Alvarenga EC, Miglino MA, Goncalves R, Mintz A, Birbrair A (2018b) Macrophage-derived GPNMB accelerates skin healing. Exp Dermatol 27(6):630–635. https://doi.org/10.1111/exd.13524
Sims DE (1991) Recent advances in pericyte biology–implications for health and disease. Can J Cardiol 7(10):431–443
Sims DE (2000) Diversity within pericytes. Clin Exp Pharmacol Physiol 27(10):842–846
Snippert HJ, Clevers H (2011) Tracking adult stem cells. EMBO Rep 12(2):113–122. https://doi.org/10.1038/embor.2010.216
Soderblom C, Luo X, Blumenthal E, Bray E, Lyapichev K, Ramos J, Krishnan V, Lai-Hsu C, Park KK, Tsoulfas P, Lee JK (2013) Perivascular fibroblasts form the fibrotic scar after contusive spinal cord injury. J Neurosci 33(34):13882–13887. https://doi.org/10.1523/JNEUROSCI.2524-13.2013
Soriano P (1994) Abnormal kidney development and hematological disorders in PDGF beta-receptor mutant mice. Genes Dev 8(16):1888–1896
Spitzer TL, Rojas A, Zelenko Z, Aghajanova L, Erikson DW, Barragan F, Meyer M, Tamaresis JS, Hamilton AE, Irwin JC, Giudice LC (2012) Perivascular human endometrial mesenchymal stem cells express pathways relevant to self-renewal, lineage specification, and functional phenotype. Biol Reprod 86(2):58. https://doi.org/10.1095/biolreprod.111.095885
Stark K, Eckart A, Haidari S, Tirniceriu A, Lorenz M, von Bruhl ML, Gartner F, Khandoga AG, Legate KR, Pless R, Hepper I, Lauber K, Walzog B, Massberg S (2013) Capillary and arteriolar pericytes attract innate leukocytes exiting through venules and 'instruct' them with pattern-recognition and motility programs. Nat Immunol 14(1):41–51. https://doi.org/10.1038/ni.2477
Tanaka S, Louis DN, Curry WT, Batchelor TT, Dietrich J (2013) Diagnostic and therapeutic avenues for glioblastoma: no longer a dead end? Nat Rev Clin Oncol 10(1):14–26. https://doi.org/10.1038/nrclinonc.2012.204
Thanabalasundaram G, Schneidewind J, Pieper C, Galla HJ (2011) The impact of pericytes on the blood-brain barrier integrity depends critically on the pericyte differentiation stage. Int J Biochem Cell Biol 43(9):1284–1293. https://doi.org/10.1016/j.biocel.2011.05.002
Thomas WE (1999) Brain macrophages: on the role of pericytes and perivascular cells. Brain Res Brain Res Rev 31(1):42–57
Tu Z, Li Y, Smith DS, Sheibani N, Huang S, Kern T, Lin F (2011) Retinal pericytes inhibit activated T cell proliferation. Invest Ophthalmol Vis Sci 52(12):9005–9010. https://doi.org/10.1167/iovs.11-8008
Utispan K, Thuwajit P, Abiko Y, Charngkaew K, Paupairoj A, Chau-in S, Thuwajit C (2010) Gene expression profiling of cholangiocarcinoma-derived fibroblast reveals alterations related to tumor progression and indicates periostin as a poor prognostic marker. Mol Cancer 9:13. https://doi.org/10.1186/1476-4598-9-13
Valdor R, Garcia-Bernal D, Bueno C, Rodenas M, Moraleda JM, Macian F, Martinez S (2017) Glioblastoma progression is assisted by induction of immunosuppressive function of pericytes through interaction with tumor cells. Oncotarget 8(40):68614–68626. https://doi.org/10.18632/oncotarget.19804
Valle IB, Schuch LF, da Silva JM, Gala-Garcia A, Diniz IMA, Birbrair A, Abreu LG, Silva TA (2020) Pericyte in oral squamous cell carcinoma: a systematic review. Head Neck Pathol. https://doi.org/10.1007/s12105-020-01188-2
Vannucci L (2015) Stroma as an active player in the development of the tumor microenvironment. Cancer Microenvironment 8(3):159–166. https://doi.org/10.1007/s12307-014-0150-x
Verbeek MM, Westphal JR, Ruiter DJ, de Waal RM (1995) T lymphocyte adhesion to human brain pericytes is mediated via very late antigen-4/vascular cell adhesion molecule-1 interactions. J Immunol 154(11):5876–5884
Weller M, Wick W, Aldape K, Brada M, Berger M, Pfister SM, Nishikawa R, Rosenthal M, Wen PY, Stupp R, Reifenberger G (2015) Glioma Nat Rev Dis Primers 1:15017. https://doi.org/10.1038/nrdp.2015.17
Winkler EA, Sagare AP, Zlokovic BV (2014) The pericyte: a forgotten cell type with important implications for Alzheimer's disease? Brain Pathol 24(4):371–386. https://doi.org/10.1111/bpa.12152
Zhou W, Chen C, Shi Y, Wu Q, Gimple RC, Fang X, Huang Z, Zhai K, Ke SQ, Ping YF, Feng H, Rich JN, Yu JS, Bao S, Bian XW (2017) Targeting glioma stem cell-derived pericytes disrupts the blood-tumor barrier and improves chemotherapeutic efficacy. Cell Stem Cell 21(5):591–603. https://doi.org/10.1016/j.stem.2017.10.002
Zhou W, Ke SQ, Huang Z, Flavahan W, Fang X, Paul J, Wu L, Sloan AE, McLendon RE, Li X, Rich JN, Bao S (2015) Periostin secreted by glioblastoma stem cells recruits M2 tumour-associated macrophages and promotes malignant growth. Nat Cell Biol 17(2):170–182. https://doi.org/10.1038/ncb3090
Zhu M, Saxton RE, Ramos L, Chang DD, Karlan BY, Gasson JC, Slamon DJ (2011) Neutralizing monoclonal antibody to periostin inhibits ovarian tumor growth and metastasis. Mol Cancer Ther 10(8):1500–1508. https://doi.org/10.1158/1535-7163.MCT-11-0046
Zimmermann KW (1923) Der feinere Bau der Blutkapillaren. Z Anat Entwicklungsgesch 68:29–109
Acknowledgements
Alexander Birbrair is supported by a grant from Instituto Serrapilheira/Serra-1708-15285, a grant from Pró-reitoria de Pesquisa/Universidade Federal de Minas Gerais (PRPq/UFMG) (Edital 05/2016), a grant from CNPQ (Universal, Process No. 405977/2018-2), a grant from National Institute of Science and Technology in Theranostics and Nanobiotechnology (CNPq/CAPES/FAPEMIG, Process No. 465669/2014-0), a grant from FAPEMIG [Rede Mineira de Engenharia de Tecidos e Terapia Celular (REMETTEC, RED-00570-16)], a grant from FAPEMIG [Rede De Pesquisa Em Doenças Infecciosas Humanas E Animais Do Estado De Minas Gerais (RED-00313-16)], and a productivity fellowship from the National Council for Scientific and Technological Development (CNPq); Akiva Mintz is supported by the National Institute of Health (1R01CA179072-01A1) and by the American Cancer Society Mentored Research Scholar grant (124443-MRSG-13-121-01-CDD).
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Bernardes, S.S., Pinto, M.C.X., Amorim, J.H. et al. Glioma Pericytes Promote Angiogenesis by Producing Periostin. Cell Mol Neurobiol 42, 557–564 (2022). https://doi.org/10.1007/s10571-020-00975-3
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DOI: https://doi.org/10.1007/s10571-020-00975-3