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Microglia immunophenotyping in gliomas

  • Authors:
    • Laura Annovazzi
    • Marta Mellai
    • Enrica Bovio
    • Samanta Mazzetti
    • Bianca Pollo
    • Davide Schiffer
  • View Affiliations / Copyright

    Affiliations: Research Center, Policlinico di Monza Foundation, I‑13100 Vercelli, Italy, Neuropathology Unit, Istituto Neurologico ‘Carlo Besta’ IRCCS Foundation, I‑20133 Milano, Italy
    Copyright: © Annovazzi et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
  • Pages: 998-1006
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    Published online on: November 9, 2017
       https://doi.org/10.3892/ol.2017.7386
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Abstract

Microglia, once assimilated to peripheral macrophages, in gliomas has long been discussed and currently it is hypothesized to play a pro‑tumor role in tumor progression. Uncertain between M1 and M2 polarization, it exchanges signals with glioma cells to create an immunosuppressive microenvironment and stimulates cell proliferation and migration. Four antibodies are currently used for microglia/macrophage identification in tissues that exhibit different cell forms and cell localization. The aim of the present work was to describe the distribution of the different cell forms and to deduce their significance on the basis of what is known on their function from the literature. Normal resting microglia, reactive microglia, intermediate and bumpy forms and macrophage‑like cells can be distinguished by Iba1, CD68, CD16 and CD163 and further categorized by CD11b, CD45, c‑MAF and CD98. The number of microglia/macrophages strongly increased from normal cortex and white matter to infiltrating and solid tumors. The ramified microglia accumulated in infiltration areas of both high‑ and low‑grade gliomas, when hypertrophy and hyperplasia occur. In solid tumors, intermediate and bumpy forms prevailed and there is a large increase of macrophage‑like cells in glioblastoma. The total number of microglia cells did not vary among the three grades of malignancy, but macrophage‑like cells definitely prevailed in high‑grade gliomas and frequently expressed CD45 and c‑MAF. CD98+ cells were present. Microglia favors tumor progression, but many aspects suggest that the phagocytosing function is maintained. CD98+ cells can be the product of fusion, but also of phagocytosis. Microglia correlated with poorer survival in glioblastoma, when considering CD163+ cells, whereas it did not change prognosis in isocitrate dehydrogenase‑mutant low grade gliomas.
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View References

1 

Graeber MB and Streit WJ: Microglia: Biology and pathology. Acta Neuropathol. 119:89–105. 2010. View Article : Google Scholar : PubMed/NCBI

2 

Lawson LJ, Perry VH, Dri P and Gordon S: Heterogeneity in the distribution and morphology of microglia in the normal adult mouse brain. Neuroscience. 39:151–170. 1990. View Article : Google Scholar : PubMed/NCBI

3 

Kettenmann H, Hanisch UK, Noda M and Verkhratsky A: Physiology of microglia. Physiol Rev. 91:461–553. 2011. View Article : Google Scholar : PubMed/NCBI

4 

Simmons GW, Pong WW, Emnett RJ, White CR, Gianino SM, Rodriguez FJ and Gutmann DH: Neurofibromatosis-1 heterozygosity increases microglia in a spatially-and temporally-restricted pattern relevant to mouse optic glioma formation and growth. J Neuropathol Exp Neurol. 70:51–62. 2011. View Article : Google Scholar : PubMed/NCBI

5 

Klein R and Roggendorf W: Increased microglia proliferation separates pilocytic astrocytomas from diffuse astrocytomas: A double labeling study. Acta Neuropathol. 101:245–248. 2001.PubMed/NCBI

6 

Komohara Y, Ohnishi K, Kuratsu J and Takeya M: Possible involvement of the M2 anti-inflammatory macrophage phenotype in growth of human gliomas. J Pathol. 216:15–24. 2008. View Article : Google Scholar : PubMed/NCBI

7 

Shinonaga M, Chang CC, Suzuki N, Sato M and Kuwabara T: Immunohistological evaluation of macrophage infiltrates in brain tumors. Correlation with peritumoral edema. J Neurosurg. 68:259–265. 1988. View Article : Google Scholar : PubMed/NCBI

8 

Roggendorf W, Strupp S and Paulus W: Distribution and characterization of microglia/macrophages in human brain tumors. Acta Neuropathol. 92:288–293. 1996. View Article : Google Scholar : PubMed/NCBI

9 

Nishie A, Ono M, Shono T, Fukushi J, Otsubo M, Onoue H, Ito Y, Inamura T, Ikezaki K, Fukui M, et al: Macrophage infiltration and heme oxygenase-1 expression correlate with angiogenesis in human gliomas. Clin Cancer Res. 5:1107–1113. 1999.PubMed/NCBI

10 

Badie B and Schartner JM: Flow cytometric characterization of tumor-associated macrophages in experimental gliomas. Neurosurgery. 46:957–962. 2000. View Article : Google Scholar : PubMed/NCBI

11 

Watters JJ, Schartner JM and Badie B: Microglia function in brain tumors. J Neurosci Res. 81:447–455. 2005. View Article : Google Scholar : PubMed/NCBI

12 

Markovic DS, Vinnakota K, Chirasani S, Synowitz M, Raguet H, Stock K, Sliwa M, Lehmann S, Kälin R, van Rooijen N, et al: Gliomas induce and exploit microglial MT1-MMP expression for tumor expansion. Proc Natl Acad Sci USA. 106:pp. 12530–12535. 2009; View Article : Google Scholar : PubMed/NCBI

13 

Zhai H, Heppner FL and Tsirka SE: Microglia/macrophages promote glioma progression. Glia. 59:472–485. 2011. View Article : Google Scholar : PubMed/NCBI

14 

Kaminska B: Microglia in Gliomas: Friend or Foe?Glioma Cell Biology. Sedo A and Mentlein R: Springer-Verlag; Berlin: pp. 241–270. 2014

15 

Schiffer D, Mellai M, Bovio E and Annovazzi L: The neuropathological basis to the functional role of microglia/macrophages in gliomas. Neurol Sci. 2017. View Article : Google Scholar

16 

Gabrusiewicz K, Ellert-Miklaszewska A, Lipko M, Sielska M, Frankowska M and Kaminska B: Characteristics of the alternative phenotype of microglia/macrophages and its modulation in experimental gliomas. PLoS One. 6:e239022011. View Article : Google Scholar : PubMed/NCBI

17 

Durafourt BA, Moore CS, Zammit DA, Johnson TA, Zaguia F, Guiot MC, Bar-Or A and Antel JP: Comparison of polarization properties of human adult microglia and blood-derived macrophages. Glia. 60:717–727. 2012. View Article : Google Scholar : PubMed/NCBI

18 

Perry VH and Teeling J: Microglia and macrophages of the central nervous system: The contribution of microglia priming and systemic inflammation to chronic neurodegeneration. Semin Immunopathol. 35:601–612. 2013. View Article : Google Scholar : PubMed/NCBI

19 

Glass R and Synowitz M: CNS macrophages and peripheral myeloid cells in brain tumours. Acta Neuropathol. 128:347–362. 2014. View Article : Google Scholar : PubMed/NCBI

20 

Szulzewsky F, Pelz A, Feng X, Synowitz M, Markovic D, Langmann T, Holtman IR, Wang X, Eggen BJ, Boddeke HW, et al: Glioma-associated microglia/macrophages display an expression profile different from M1 and M2 polarization and highly express Gpnmb and Spp1. PLoS One. 10:e01166442015. View Article : Google Scholar : PubMed/NCBI

21 

Hussain SF, Yang D, Suki D, Aldape K, Grimm E and Heimberger AB: The role of human glioma-infiltrating microglia/macrophages in mediating antitumor immune responses. Neuro Oncol. 8:261–279. 2006. View Article : Google Scholar : PubMed/NCBI

22 

Parney IF, Waldron JS and Parsa AT: Flow cytometry and in vitro analysis of human glioma-associated macrophages. Laboratory investigation. J Neurosurg. 110:572–582. 2009. View Article : Google Scholar : PubMed/NCBI

23 

Li W and Graeber MB: The molecular profile of microglia under the influence of glioma. Neuro Oncol. 14:958–978. 2012. View Article : Google Scholar : PubMed/NCBI

24 

Wei J, Gabrusiewicz K and Heimberger A: The controversial role of microglia in malignant gliomas. Clin Dev Immunol. 2013:2852462013. View Article : Google Scholar : PubMed/NCBI

25 

Prinz M, Tay TL, Wolf Y and Jung S: Microglia: Unique and common features with other tissue macrophages. Acta Neuropathol. 128:319–331. 2014. View Article : Google Scholar : PubMed/NCBI

26 

Hambardzumyan D, Gutmann DH and Kettenmann H: The role of microglia and macrophages in glioma maintenance and progression. Nat Neurosci. 19:20–27. 2016. View Article : Google Scholar : PubMed/NCBI

27 

Müller A, Brandenburg S, Turkowski K, Müller S and Vajkoczy P: Resident microglia, and not peripheral macrophages, are the main source of brain tumor mononuclear cells. Int J Cancer. 137:278–288. 2015. View Article : Google Scholar : PubMed/NCBI

28 

Zhou W, Ke SQ, Huang Z, Flavahan W, Fang X, Paul J, Wu L, Sloan AE, McLendon RE, Li X, et al: Periostin secreted by glioblastoma stem cells recruits M2 tumour-associated macrophages and promotes malignant growth. Nat Cell Biol. 17:170–182. 2015. View Article : Google Scholar : PubMed/NCBI

29 

Szulzewsky F, Arora S, de Witte L, Ulas T, Markovic D, Schultze JL, Holland EC, Synowitz M, Wolf SA and Kettenmann H: Human glioblastoma-associated microglia/monocytes express a distinct RNA profile compared to human control and murine samples. Glia. 64:1416–1436. 2016. View Article : Google Scholar : PubMed/NCBI

30 

Kennedy BC, Showers CR, Anderson DE, Anderson L, Canoll P, Bruce JN and Anderson RC: Tumor-associated macrophages in glioma: Friend or foe? J Oncol 2013. 4869122013.

31 

Wu A, Wei J, Kong LY, Wang Y, Priebe W, Qiao W, Sawaya R and Heimberger AB: Glioma cancer stem cells induce immunosuppressive macrophages/microglia. Neuro Oncol. 12:1113–1125. 2010. View Article : Google Scholar : PubMed/NCBI

32 

Ye XZ, Xu SL, Xin YH, Yu SC, Ping YF, Chen L, Xiao HL, Wang B, Yi L, Wang QL, et al: Tumor-associated microglia/macrophages enhance the invasion of glioma stem-like cells via TGF-β1 signaling pathway. J Immunol. 189:444–453. 2012. View Article : Google Scholar : PubMed/NCBI

33 

Brandenburg S, Müller A, Turkowski K, Radev YT, Rot S, Schmidt C, Bungert AD, Acker G, Schorr A, Hippe A, et al: Resident microglia rather than peripheral macrophages promote vascularization in brain tumors and are source of alternative pro-angiogenic factors. Acta Neuropathol. 131:365–378. 2016. View Article : Google Scholar : PubMed/NCBI

34 

Coniglio S, Miller I, Symons M and Segall JE: Coculture assays to study macrophage and microglia stimulation of glioblastoma invasion. J Vis Exp. 20:1162016.

35 

Louis DN, Ohgaki H, Wiestler OD and Cavenee WK: WHO classification of tumours of the Central Nervous System. 4th. IARC Press; Lyon: pp. 1–408. 2016

36 

Mellai M, Piazzi A, Caldera V, Monzeglio O, Cassoni P, Valente G and Schiffer D: IDH1 and IDH2 mutations, immunohistochemistry and associations in a series of brain tumors. J Neurooncol. 105:345–357. 2011. View Article : Google Scholar : PubMed/NCBI

37 

Kondo S and Okabe S: In vivo two-photon microscopy of microglia. Methods Mol Biol. 1041:319–335. 2013. View Article : Google Scholar : PubMed/NCBI

38 

Bayerl SH, Niesner R, Cseresnyes Z, Radbruch H, Pohlan J, Brandenburg S, Czabanka MA and Vajkoczy P: Time lapse in vivo microscopy reveals distinct dynamics of microglia-tumor environment interactions-a new role for the tumor perivascular space as highway for trafficking microglia. Glia. 64:1210–1226. 2016. View Article : Google Scholar : PubMed/NCBI

39 

Nimmerjahn A: Two-photon imaging of microglia in the mouse cortex in vivo. Cold Spring Harb Protoc. 5:pii: pdb.prot069294. 2012.

40 

Greter M, Lelios I and Croxford AL: Microglia versus myeloid cell nomenclature during brain inflammation. Front Immunol. 6:2492015. View Article : Google Scholar : PubMed/NCBI

41 

Barros MH, Hauck F, Dreyer JH, Kempkes B and Niedobitek G: Macrophage polarisation: An immunohistochemical approach for identifying M1 and M2 macrophages. PLoS One. 8:e809082013. View Article : Google Scholar : PubMed/NCBI

42 

da Fonseca AC and Badie B: Microglia and macrophages in malignant gliomas: Recent discoveries and implications for promising therapies. Clin Dev Immunol. 2013:2641242013.PubMed/NCBI

43 

Morioka T, Baba T, Black KL and Streit WJ: Immunophenotypic analysis of infiltrating leukocytes and microglia in an experimental rat glioma. Acta Neuropathol. 83:590–597. 1992. View Article : Google Scholar : PubMed/NCBI

44 

Morimura T, Neuchrist C, Kitz K, Budka H, Scheiner O, Kraft D and Lassmann H: Monocyte subpopulations in human gliomas: Expression of Fc and complement receptors and correlation with tumor proliferation. Acta Neuropathol. 80:287–294. 1990. View Article : Google Scholar : PubMed/NCBI

45 

Vinnakota K, Hu F, Ku MC, Georgieva PB, Szulzewsky F, Pohlmann A, Waiczies S, Waiczies H, Niendorf T, Lehnardt S, et al: Toll-like receptor 2 mediates microglia/brain macrophage MT1-MMP expression and glioma expansion. Neuro Oncol. 15:1457–1468. 2013. View Article : Google Scholar : PubMed/NCBI

46 

Schiffer D: Pathology and neuroepidemiology of the brain and nervous system. Curr Opin Oncol. 3:449–458. 1991. View Article : Google Scholar : PubMed/NCBI

47 

Hochreiter-Hufford A and Ravichandran KS: Clearing the dead: Apoptotic cell sensing, recognition, engulfment, and digestion. Cold Spring Harb Perspect Biol. 5:a0087482013. View Article : Google Scholar : PubMed/NCBI

48 

Kamper P, Bendix K, Hamilton-Dutoit S, Honoré B, Nyengaard JR and d'Amore F: Tumor-infiltrating macrophages correlate with adverse prognosis and Epstein-Barr virus status in classical Hodgkin's lymphoma. Haematologica. 96:269–276. 2011. View Article : Google Scholar : PubMed/NCBI

49 

Zaki MA, Wada N, Ikeda J, Shibayama H, Hashimoto K, Yamagami T, Tatsumi Y, Tsukaguchi M, Take H, Tsudo M, et al: Prognostic implication of types of tumor-associated macrophages in Hodgkin lymphoma. Virchows Arch. 459:361–366. 2011. View Article : Google Scholar : PubMed/NCBI

50 

Ino Y, Yamazaki-Itoh R, Shimada K, Iwasaki M, Kosuge T, Kanai Y and Hiraoka N: Immune cell infiltration as an indicator of the immune microenvironment of pancreatic cancer. Br J Cancer. 108:914–923. 2013. View Article : Google Scholar : PubMed/NCBI

51 

Herrera M, Herrera A, Domínguez G, Silva J, García V, García JM, Gómez I, Soldevilla B, Muñoz C, Provencio M, et al: Cancer-associated fibroblast and M2 macrophage markers together predict outcome in colorectal cancer patients. Cancer Sci. 104:437–444. 2013. View Article : Google Scholar : PubMed/NCBI

52 

Forstreuter F, Lucius R and Mentlein R: Vascular endothelial growth factor induces chemotaxis and proliferation of microglial cells. J Neuroimmunol. 132:93–98. 2002. View Article : Google Scholar : PubMed/NCBI

53 

Kerber M, Reiss Y, Wickersheim A, Jugold M, Kiessling F, Heil M, Tchaikovski V, Waltenberger J, Shibuya M, Plate KH and Machein MR: Flt-1 signaling in macrophages promotes glioma growth in vivo. Cancer Res. 68:7342–7351. 2008. View Article : Google Scholar : PubMed/NCBI

54 

Li Y, Liu DX, Li MY, Qin XX, Fang WG, Zhao WD and Chen YH: Ephrin-A3 and ephrin-A4 contribute to microglia-induced angiogenesis in brain endothelial cells. Anat Rec (Hoboken). 297:1908–1918. 2014. View Article : Google Scholar : PubMed/NCBI

55 

Rymo SF, Gerhardt H, Wolfhagen Sand F, Lang R, Uv A and Betsholtz C: A two-way communication between microglial cells and angiogenic sprouts regulates angiogenesis in aortic ring cultures. PLoS One. 6:e158462011. View Article : Google Scholar : PubMed/NCBI

56 

Ding P, Wang W, Wang J, Yang Z and Xue L: Expression of tumor-associated macrophage in progression of human glioma. Cell Biochem Biophys. 70:1625–1631. 2014. View Article : Google Scholar : PubMed/NCBI

57 

Mantovani A, Allavena P and Sica A: Tumour-associated macrophages as a prototypic type II polarised phagocyte population: Role in tumour progression. Eur J Cancer. 40:1660–1667. 2004. View Article : Google Scholar : PubMed/NCBI

58 

Lan C, Huang X, Lin S, Huang H, Cai Q, Wan T, Lu J and Liu J: Expression of M2-polarized macrophages is associated with poor prognosis for advanced epithelial ovarian cancer. Technol Cancer Res Treat. 12:259–267. 2013. View Article : Google Scholar : PubMed/NCBI

59 

Edin S, Wikberg ML, Dahlin AM, Rutegård J, Öberg Å, Oldenborg PA and Palmqvist R: The distribution of macrophages with a M1 or M2 phenotype in relation to prognosis and the molecular characteristics of colorectal cancer. PLoS One. 7:e470452012. View Article : Google Scholar : PubMed/NCBI

60 

Lisi L, Stigliano E, Lauriola L, Navarra P and Dello Russo C: Proinflammatory-activated glioma cells induce a switch in microglial polarization and activation status, from a predominant M2b phenotype to a mixture of M1 and M2a/B polarized cells. ASN Neuro. 6:171–183. 2014. View Article : Google Scholar : PubMed/NCBI

61 

Noorani I, Petty G, Grundy PL, Sharpe G, Willaime-Morawek S, Harris S, Thomas GJ, Nicoll JA and Boche D: Novel association between microglia and stem cells in human gliomas: A contributor to tumour proliferation? J Pathol Clin Res. 1:67–75. 2015. View Article : Google Scholar : PubMed/NCBI

62 

Takeuchi H, Kubota T, Kitai R, Nakagawa T and Hashimoto N: CD98 immunoreactivity in multinucleated giant cells of glioblastomas: An immunohistochemical double labeling study. Neuropathology. 28:127–131. 2008. View Article : Google Scholar : PubMed/NCBI

63 

Huysentruyt LC, Akgoc Z and Seyfried TN: Hypothesis: Are neoplastic macrophages/microglia present in glioblastoma multiforme? ASN Neuro. 3(pii): e000642011.PubMed/NCBI

64 

Bjerknes R, Bjerkvig R and Laerum OD: Phagocytic capacity of normal and malignant rat glial cells in culture. J Natl Cancer Inst. 78:279–288. 1987.PubMed/NCBI

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Copy and paste a formatted citation
Spandidos Publications style
Annovazzi L, Mellai M, Bovio E, Mazzetti S, Pollo B and Schiffer D: Microglia immunophenotyping in gliomas. Oncol Lett 15: 998-1006, 2018.
APA
Annovazzi, L., Mellai, M., Bovio, E., Mazzetti, S., Pollo, B., & Schiffer, D. (2018). Microglia immunophenotyping in gliomas. Oncology Letters, 15, 998-1006. https://doi.org/10.3892/ol.2017.7386
MLA
Annovazzi, L., Mellai, M., Bovio, E., Mazzetti, S., Pollo, B., Schiffer, D."Microglia immunophenotyping in gliomas". Oncology Letters 15.1 (2018): 998-1006.
Chicago
Annovazzi, L., Mellai, M., Bovio, E., Mazzetti, S., Pollo, B., Schiffer, D."Microglia immunophenotyping in gliomas". Oncology Letters 15, no. 1 (2018): 998-1006. https://doi.org/10.3892/ol.2017.7386
Copy and paste a formatted citation
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Spandidos Publications style
Annovazzi L, Mellai M, Bovio E, Mazzetti S, Pollo B and Schiffer D: Microglia immunophenotyping in gliomas. Oncol Lett 15: 998-1006, 2018.
APA
Annovazzi, L., Mellai, M., Bovio, E., Mazzetti, S., Pollo, B., & Schiffer, D. (2018). Microglia immunophenotyping in gliomas. Oncology Letters, 15, 998-1006. https://doi.org/10.3892/ol.2017.7386
MLA
Annovazzi, L., Mellai, M., Bovio, E., Mazzetti, S., Pollo, B., Schiffer, D."Microglia immunophenotyping in gliomas". Oncology Letters 15.1 (2018): 998-1006.
Chicago
Annovazzi, L., Mellai, M., Bovio, E., Mazzetti, S., Pollo, B., Schiffer, D."Microglia immunophenotyping in gliomas". Oncology Letters 15, no. 1 (2018): 998-1006. https://doi.org/10.3892/ol.2017.7386
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