Blockade of CCR5 receptor prevents M2 microglia phenotype in a microglia-glioma paradigm

Neurochemistry International

Volumn 108, Issue , 2017, Pages 100-108

  Laudati, Emilia ^a   Currò, Diego ^a   Navarra, Pierluigi ^a   Lisi, Lucia ^a  

^a CATHOLIC UNIVERSITY   (Italy)

Author keywords

AKT; Arginase; Glioblastoma; iNOS; Microglia; mTOR

Indexed keywords

ARG1 PROTEIN; CHEMOKINE RECEPTOR CCR5; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; I KAPPA B; INTERLEUKIN 10; INTERLEUKIN 1BETA; MAMMALIAN TARGET OF RAPAMYCIN; MARAVIROC; NITRIC OXIDE; PROTEIN; PROTEIN KINASE B; UNCLASSIFIED DRUG; CHEMOKINE RECEPTOR CCR5 ANTAGONIST;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ACTIVATION; CELL MIGRATION; CELL STIMULATION; COMPARATIVE STUDY; CONTROLLED STUDY; DISEASE ASSOCIATION; ENZYME INHIBITION; GENE EXPRESSION; GENE FUNCTION; GLIOMA; GLIOMA CELL; MICROGLIA; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; RAT; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; CELL PROLIFERATION; DOSE RESPONSE; DRUG EFFECTS; HUMAN; METABOLISM; PHENOTYPE; PHYSIOLOGY; TUMOR CELL LINE;

ANIMALS; CCR5 RECEPTOR ANTAGONISTS; CELL LINE, TUMOR; CELL PROLIFERATION; DOSE-RESPONSE RELATIONSHIP, DRUG; GLIOMA; HUMANS; MICROGLIA; PHENOTYPE; RATS; RECEPTORS, CCR5;

EID: 85014736905     PISSN: 01970186     EISSN: 18729754     Source Type: Journal    
DOI: 10.1016/j.neuint.2017.03.002     Document Type: Article

References (39)

1. Allen, S.J., Crown, S.E., Handel, T.M., Chemokine: receptor structure, interactions, and antagonism. Annu. Rev. Immunol. 25 (2007), 787–820.
2. Buckner, J.C., Brown, P.D., O'Neill, B.P., Meyer, F.B., Wetmore, C.J., Uhm, J.H., Central nervous system tumors. Mayo Clin. Proc. 82:10 (2007), 1271–1286 (Review).
3. Charles, N.A., Holland, E.C., Gilbertson, R., Glass, R., Kettenmann, H., The brain tumor microenvironment. Glia 60:3 (2012), 502–514 (Review).
4. Choi, S.A., Lee, J.Y., Kwon, S.E., Wang, K.C., Phi, J.H., Choi, J.W., Jin, X., Lim, J.Y., Kim, H., Kim, S.K., Human adipose tissue-derived mesenchymal stem cells target brain tumor-initiating cells. PLoS One, 10(6), 2015, e0129292.
5. Dello Russo, C., Lisi, L., Tentori, L., Navarra, P., Graziani, G., Combs, C.K., Exploiting microglial functions for the treatment of glioblastoma. Curr. Cancer Drug Targets 95:3 (2016), 480–488.
6. Dello Russo, C., Lisi, L., Tringali, G., Navarra, P., Involvement of mTOR kinase in cytokine-dependent microglial activation and cell proliferation. Biochem. Pharmacol. 78:9 (2009), 1242–1251.
7. Gadani, S.P., Cronk, J.C., Norris, G.T., Kipnis, J., IL-4 in the brain: a cytokine to remember. J. Immunol. 189:9 (2012), 4213–4219.
8. Galvão, R.P., Zong, H., Inflammation and gliomagenesis: Bi-Directional communication at early and late stages of tumor progression. Curr. Pathobiol. Rep. 1:1 (2013), 19–28.
9. Held-Feindt, J., Hattermann, K., Müerköster, S.S., Wedderkopp, H., Knerlich-Lukoschus, F., Ungefroren, H., Mehdorn, H.M., Mentlein, R., CX3CR1 promotes recruitment of human glioma-infiltrating microglia/macrophages (GIMs). Exp. Cell Res. 316:9 (2010), 1553–1566.
10. Horvath, R.J., DeLeo, J.A., Morphine enhances microglial migration through modulation of P2X4 receptor signaling. J. Neurosci. 29:4 (2009), 998–1005.
11. Hütter, G., Bodor, J., Ledger, S., Boyd, M., Millington, M., Tsie, M., Symonds, G., CCR5 targeted cell therapy for HIV and prevention of viral escape. 27 Viruses 7:8 (2015), 4186–4203.
12. Kakinuma, T., Hwang, S.T., Chemokines, chemokine receptors, and cancer metastasis. J. Leukoc. Biol. 79:4 (2006), 639–651.
13. Kubiatowski, T., Jang, T., Lachyankar, M.B., Salmonsen, R., Nabi, R.R., Quesenberry, P.J., Litofsky, N.S., Ross, A.H., Recht, L.D., Association of increased phosphatidylinositol 3-kinase signaling with increased invasiveness and gelatinase activity in malignant gliomas. J. Neurosurg. 95:3 (2001), 480–488.
14. Lee, H.C., Park, I.C., Park, M.J., An, S., Woo, S.H., Jin, H.O., Chung, H.Y., Lee, S.J., Gwak, H.S., Hong, Y.J., Yoo, D.H., Rhee, C.H., Hong, S.I., Sulindac and its metabolites inhibit invasion of glioblastoma cells via down-regulation of Akt/PKB and MMP-2. J. Cell Biochem. 94:3 (2005), 597–610.
15. Li, D., Wang, C., Yao, Y., Chen, L., Liu, G., Zhang, R., Liu, Q., Shi, F.D., Hao, J., mTORC1 pathway disruption ameliorates brain inflammation following stroke via a shift in microglia phenotype from M1 type to M2 type. FASEB J. 30:10 (2016), 3388–3399.
16. Li, W., Graeber, M.B., The molecular profile of microglia under the influence of glioma. Neuro Oncol. 14:8 (2012), 958–978.
17. Lisi, L., Laudati, E., Navarra, P., Dello Russo, C., The mTOR kinase inhibitors polarize glioma-activated microglia to express a M1 phenotype. J. Neuroinflammation, 11, 2014, 125.
18. Lisi, L., Navarra, P., Feinstein, D.L., Dello Russo, C., The mTOR kinase inhibitor rapamycin decreases iNOS mRNA stability in astrocytes. J. Neuroinflammation, 8(1), 2011, 1.
19. Lisi, L., Stigliano, E., Lauriola, L., Navarra, P., 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 6:3 (2014), 171–183.
20. Lisi, L., Tramutola, A., De Luca, A., Navarra, P., Dello Russo, C., Modulatory effects of the CCR5 antagonist maraviroc on microglial pro-inflammatory activation elicited by gp120. J. Neurochem. 120:1 (2012), 106–114.
21. Lu, M., Wu, B., Structural studies of G protein-coupled receptors. IUBMB Life 68:11 (2016), 894–903.
22. Mantovani, A., The growing diversity and spectrum of action of myeloid-derived suppressor cells. Eur. J. Immunol. 40:12 (2010), 3317–3320.
23. Martin-Blondel, G., Brassat, D., Bauer, J., Lassmann, H., Liblau, R.S., CCR5 blockade for neuroinflammatory diseases–beyond control of HIV. Nat. Rev. Neurol. 12:2 (2016), 95–105.
24. Okada, H., Kohanbash, G., Zhu, X., Kastenhuber, E.R., Hoji, A., Ueda, R., Fujita, M., Immunotherapeutic approaches for glioma. Crit. Rev. Immunol. 29:1 (2009), 1–42.
25. Oppermann, M., Chemokine receptor CCR5: insights into structure, function, and regulation. Cell Signal 16:11 (2004), 1201–1210.
26. Osuka, S., Van Meir, E.G., Overcoming therapeutic resistance in glioblastoma: the way forward. J. Clin. Invest. 127:2 (2017), 415–426.
27. Paschoal, V.A., Amano, M.T., Belchior, T., Magdalon, J., Chimin, P., Andrade, M.L., Ortiz-Silva, M., Castro, É., Yamashita, A.S., Rosa Neto, J.C., Câmara, N.O., Festuccia, W.T., mTORC1 inhibition with rapamycin exacerbates adipose tissue inflammation in obese mice and dissociates macrophage phenotype from function. Immunobiology 222:2 (2017), 261–271.
28. Paw, I., Carpenter, R.C., Watabe, K., Debinski, W., Lo, H.W., Mechanisms regulating glioma invasion. Cancer Lett. 362:1 (2015), 1–7.
29. Pham, K., Luo, D., Liu, C., Harrison, J.K., CCL5, CCR1 and CCR5 in murine glioblastoma: immune cell infiltration and survival rates are not dependent on individualexpression of either CCR1 or CCR5. J. Neuroimmunol. 246:1–2 (2012), 10–17.
30. Piotrowska, A., Kwiatkowski, K., Rojewska, E., Makuch, W., Mika, J., Maraviroc reduces neuropathic pain through polarization of microglia and astroglia - evidence from in vivo and in vitro studies. Neuropharmacology 108 (2016), 207–219.
31. Ransohoff, R.M.l., A polarizing question: do M1 and M2 microglia exist?. Nat. Neurosci. 19:8 (2016), 987–991.
32. Robinson, S.C., Scott, K.A., Wilson, J.L., Thompson, R.G., Proudfoot, A.E., Balkwill, F.R., A chemokine receptor antagonist inhibits experimental breast tumor growth. Cancer Res. 63:23 (2003), 8360–8365.
33. Rolle, C.E., Sengupta, S., Lesniak, M.S., Mechanisms of immune evasion by gliomas. Adv. Exp. Med. Biol. 746 (2012), 53–76.
34. Sliwa, M., Markovic, D., Gabrusiewicz, K., Synowitz, M., Glass, R., Zawadzka, M., Wesolowska, A., Kettenmann, H., Kaminska, B., The invasion promoting effect of microglia on glioblastoma cells is inhibited by cyclosporin A. Brain 130:Pt 2 (2007), 476–489.
35. Soria, G., Ben-Baruch, A., The inflammatory chemokines CCL2 and CCL5 in breast cancer. Cancer Lett. 267:2 (2008), 271–285.
36. Vairano, M., Dello Russo, C., Pozzoli, G., Battaglia, A., Scambia, G., Tringali, G., Aloe-Spiriti, M.A., Preziosi, P., Navarra, P., Erythropoietin exerts anti-apoptotic effects on rat microglial cells in vitro. Eur. J. Neurosci. 16:4 (2002), 584–592.
37. Vakilian, A., Khorramdelazad, H., Heidari, P., Sheikh Rezaei, Z., Hassanshahi, G., CCL2/CCR2 signaling pathway in glioblastoma multiforme. Neurochem. Int. 103 (2017), 1–7.
38. You, W., Wang, Z., Li, H., Shen, H., Xu, X., Jia, G., Chen, G., Inhibition of mammalian target of rapamycin attenuates early brain injury through modulating microglial polarization after experimental subarachnoid hemorrhage in rats. J. Neurol. Sci. 367 (2016), 224–231.
39. Zhao, L., Wang, Y., Xue, Y., Lv, W., Zhang, Y., He, S., Critical roles of chemokines receptor CCR5 in regulating glioblastoma proliferation and invasion. Acta Biochim. Biophys. Sin. (Shanghai) 47:11 (2015), 890–898.