Have a personal or library account? Click to login
Cytokine CCL5 and receptor CCR5 axis in glioblastoma multiforme Cover

Cytokine CCL5 and receptor CCR5 axis in glioblastoma multiforme

Open Access
|Nov 2019

References

  1. Philips A, Henshaw DL, Lamburn G, O’Carroll MJ. Brain tumours: rise in glioblastoma multiforme incidence in England 1995-2015 suggests an adverse environmental or lifestyle factor. J Environ Public Health 2018: 2170208. doi: 10.1155/2018/7910754
  2. Molenaar RJ, Maciejewski JP, Wilmink JW, Van Noorden CJF. Wild-type and mutated IDH1/2 enzymes and therapy responses. Oncogene 2018; 37: 1949-60. doi: 10.1038/s41388-017-0077-z
  3. Louis DN, Perry A, Reifenberger G, von Deimling A, Figarella-Branger D, Cavenee WK, et al. The 2016 World Health Organization classification of tumors of the central nervous system: a summary. Acta Neuropathol 2016; 131: 803-20. doi: 10.1007/s00401-016-1545-1
  4. Stupp R, Hegi ME, Mason WP, van den Bent MJ, Taphoorn MJ, Janzer RC, et al. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol 2009; 10: 459-66. doi: 10.1016/S1470-2045(09)70025-7
  5. Stupp R, Hegi ME, Gorlia T, Erridge SC, Perry J, Hong YK, et al. Cilengitide combined with standard treatment for patients with newly diagnosed glioblastoma with methylated MGMT promoter (CENTRIC EORTC 26071-22072 study): a multicentre, randomised, open-label, phase 3 trial. Lancet Oncol 2014; 15: 1100-8. doi: 10.1016/S1470-2045(14)70379-1
  6. Hegi ME, Genbrugge E, Gorlia T, Stupp R, Gilbert MR, Chinot OL, et al. MGMT promoter methylation cutoff with safety margin for selecting glioblastoma patients into trials omitting temozolomide: a pooled analysis of four clinical trials. Clin Cancer Res 2018; 25: 1809-16. doi: 10.1158/1078-0432.ccr-18-3181
  7. Lathia JD. Mack SC, Mulkearns-Hubert EE, Valentim CL, Rich JN. Cancer stem cells in glioblastoma. Genes Dev 2015; 29: 1203-17. doi: 10.1101/gad.261982.115
  8. Van Meir EG, Hadjipanayis CG, Norden AD, Shu HK, Wen PY, Olson JJ. Exciting new advances in neuro-oncology: the avenue to a cure for malignant glioma. CA Cancer J Clin 2010; 60: 166-93. doi: 10.3322/caac.20069
  9. Phillips HS, Kharbanda S, Chen R, Forrest WF, Soriano RH, Wu TD, et al. Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis. Cancer Cell 2006: 9: 157-73. doi: 10.1016/j.ccr.2006.02.019
  10. Verhaak RGW, Hoadley KA, Purdom E, Wang V, Qi Y, Wilkerson MD, et al. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 2010; 17: 98-110. doi: 10.1016/j.ccr.2009.12.020
  11. Teng J, da Hora CC, Kantar RS, Nakano I, Wakimoto H, Batchelor TT, et al. Dissecting inherent intratumor heterogeneity in patient-derived glioblastoma culture models. Neuro Oncol 2017; 19: 820-32. doi: 10.1093/neuonc/now253
  12. Salmon H, Remark R, Gnjatic S, Merad M. Host tissue determinants of tumour immunity. Nat Rev Cancer 2019; 19: 215-27. doi: 10.1038/s41568-019-0125-9
  13. Broekman ML, Maas SLN, Abels ER, Mempel TR, Krichevsky AM, Breakefield XO. Multidimensional communication in the microenvirons of glioblastoma. Nat Rev Neurol 2018; 14: 482-95. doi: 10.1038/s41582-018-0025-8
  14. Thorsson V, Gibbs DL, Brown SD, Wolf D, Bortone DS, Ou Yang TH, et al. The immune landscape of cancer. Immunity 2018; 48: 812-30. e14. doi: 10.1016/j.immuni.2018.03.023
  15. Matias D, Balça-Silva J, da Graça GC, Wanjiru CM, Macharia LW, Nascimento CP, et al. Microglia/astrocytes-glioblastoma crosstalk: crucial molecular mechanisms and microenvironmental factors. Front Cell Neurosci 2018; 12: 1-22. doi: 10.3389/fncel.2018.00235
  16. Motaln H, Koren A, Gruden K, Ramšak Ž, Schichor C, Lah TT. Heterogeneous glioblastoma cell cross-talk promotes phenotype alterations and enhanced drug resistance. Oncotarget 2015; 6: 40998-1017. doi: 10.18632/oncotarget.5701
  17. Oliveira MN, Pillat MM, Motaln H, Ulrich H, Lah TT. Kinin-B1 receptor stimulation promotes invasion and is involved in cell-cell interaction of co-cultured glioblastoma and mesenchymal stem cells. Sci Rep 2018; 8: 1299. doi: 10.1038/s41598-018-19359-1
  18. Balkwill F. Cancer and the chemokine network. Nat Rev Cancer 2004; 4: 240-50. doi: 10.1038/nrc1388
  19. Lazennec G, Richmond A. Chemokines and chemokine receptors: new insights into cancer-related inflammation. Trends Mol Med 2010; 16: 133-44. doi: 10.1016/j.molmed.2010.01.003
  20. Aldinucci D, Casagrande N. Inhibition of the CCL5/CCR5 axis against the progression of gastric cancer. Int J Mol Sci 2018; 19: 1477. doi: 10.3390/ ijms19051477
  21. Ben-Baruch A. Inflammation-associated immune suppression in cancer: the roles played by cytokines, chemokines and additional mediators. Sem Cancer Biology 2006; 16: 38-52. doi: 10.1016/j.semcancer.2005.07.006
  22. Schall TJ, Bacon K, Toy KJ, Goeddel DV. Selective attraction of monocytes and T lymphocytes of the memory phenotype by cytokine RANTES. Nature 1990; 347: 669-71. doi: 10.1038/347669a0
  23. Soria G, Ben-Baruch A. The inflammatory chemokines CCL2 and CCL5 in breast cancer. Cancer Lett 2008; 267: 271-85. doi: 10.1016/j.canlet.2008.03.018
  24. Cocchi F, Tresoldi E, Björndal A, Fredriksson R, Colognesi C, Deng HK, et al. Identification of RANTES, MIP-1α, and MIP-1β as the major HIV-suppressive factors produced by CD8+T cells. Science 1995; 270: 1811-5. doi: 10.1126/science.270.5243.1811
  25. Alkhatib G. The biology of CCR5 and CXCR4. Curr Opin HIV AIDS 2009; 4: 96-103. doi: 10.1097/COH.0b013e328324bbec
  26. Roscic-Mrkic B, Fischer M, Leemann C, Manrique A, Gordon CJ, Moore JP, et al. RANTES (CCL5) uses the proteoglycan CD44 as an auxiliary receptor to mediate cellular activation signals and HIV-1 enhancement. Blood 2003; 102: 1169-77. doi: 10.1182/blood-2003-02-0488
  27. Liu B, Hassan Z, Amisten S, King AJ, Bowe JE, Huang GC, et al. The novel chemokine receptor, G-protein-coupled receptor 75, is expressed by islets and is coupled to stimulation of insulin secretion and improved glucose homeostasis. Diabetologia 2013; 56: 2467-76. doi: 10.1007/s00125-013-3022-x
  28. Velasco-Velazquez M, Xolalpa W, Pestell RG. The potential to target CCL5/CCR5 in breast cancer. Expert Opin Ther Targets 2014; 18: 1-11. doi: 10.1517/14728222.2014.949238
  29. Pan Y, Smithson LJ, Ma Y, Hambardzumyan D, Gutmann DH. Ccl5 establishes an autocrine high-grade glioma growth regulatory circuit critical for mesenchymal glioblastoma survival. Oncotarget 2017; 8: 32977-89. doi: 10.18632/ oncotarget.16516
  30. Cambien B, Richard-Fiardo P, Karimdjee BF, Martini V, Ferrua B, Pitard B, et al. CCL5 neutralization restricts cancer growth and potentiates the targeting of PDGFRβ in colorectal carcinoma. PLoS One 2011; 6: e28842. doi: 10.1371/journal.pone.0028842
  31. Huang CY, Fong YC, Lee CY, Chen MY, Tsai HC, Hsu HC, et al. CCL5 increases lung cancer migration via PI3K, Akt and NF-κB pathways. Biochem Pharmacol 2009; 77: 794-803. doi: 10.1016/j.bcp.2008.11.014
  32. Vaday GG, Peehl DM, Kadam PA, Lawrence DM. Expression of CCL5 (RANTES) and CCR5 in prostate cancer. Prostate 2006; 66: 124-34. doi: 10.1002/pros.20306
  33. Pervaiz A, Zepp M, Mahmood S, Ali DM, Berger MR, Adwan H. CCR5 blockage by maraviroc: a potential therapeutic option for metastatic breast cancer. Cellular Oncology 2018; 42: 93-106. doi: 10.1007/s13402-018-0415-3
  34. Jiao X, Velasco-Velázquez MA, Wang M, Li Z, Rui H, Peck AR, et al. CCR5 Governs DNA damage repair and breast cancer stem cell expansion. Cancer Res 2018; 78: 1657-71. doi: 10.1158/0008-5472.CAN-17-0915
  35. Niwa Y, Akamatsu H, Niwa H, Sumi H, Ozaki Y, Abe A. Correlation of tissue and plasma RANTES levels with disease course in patients with breast or cervical cancer. Clin Cancer Res 2001; 7: 285-9. doi: 10.1158/1078-0432. ccr-06-0074
  36. Sugasawa H, Ichikura T, Kinoshita M, Ono S, Majima T, Tsujimoto H, et al. Gastric cancer cells exploit CD4+ cell-derived CCL5 for their growth and prevention of CD8+ cell-involved tumor elimination. Int J Cancer 2008; 122: 2535-41. doi: 10.1002/ijc.23401 doi:10.1002/ijc.23401
  37. Yaal-Hahoshen N, Shina S, Leider-Trejo L, Barnea I, Shabtai EL, Azenshtein E, et al. The chemokine CCL5 as a potential prognostic factor predicting disease progression in stage II breast cancer patients. Clinical Cancer Res 2006; 12: 4474-80. doi: 10.1158/1078-0432.CCR-06-0074
  38. Sushil KS, Mishra MK. CCR5/CCL5 axis interaction promotes migratory and invasiveness of pancreatic cancer cells. Sci Rep 2018; 8: 1323. doi: 10.1038/ s41598-018-19643-0
  39. Pham K, Luo D, Liu C, Harrison JK. CCL5, CCR1 and CCR5 in murine glioblastoma: Immune cell infiltration and survival rates are not dependent on individual expression of either CCR1 or CCR5. J Neuroimmunol 2012; 246: 10-7. doi: 10.1016/j.jneuroim.2012.02.009
  40. Borsig L, Wolf MJ, Roblek M, Lorentzen A, Heikenwalder M. Inflammatory chemokines and metastasis-tracing the accessory. Brit Dental J 2014; 33: 3217-24. doi: 10.1038/onc.2013.272
  41. Oppermann M. Chemokine receptor CCR5: Insights into structure, function, and regulation. Cellular Signalling 2004; 16: 1201-10. doi: 10.1016/j. cellsig.2004.04.007
  42. Rosenbaum DM, Rasmussen SGF, Kobilka BK. The structure and function of G-protein-coupled receptors. Nature 2009; 459: 356-63. doi: 10.1038/ nature08144
  43. Griffith JW, Sokol CL, Luster AD. Chemokines and chemokine receptors: Positioning cells for host defense and immunity. Annu Rev Immunol 2014; 32: 659-702. doi: 10.1146/annurev-immunol-032713-120145
  44. Kaplon H, Reichert JM. Antibodies to watch in 2019. MAbs 2019; 11: 219-38. doi: 10.1080/19420862.2018.1556465
  45. Dhody K, Pourhassan N, Kazempour K, Green D, Badri S, Mekonnen H, et al. PRO 140, a monoclonal antibody targeting CCR5, as a long-acting, single-agent maintenance therapy for HIV-1 infection. HIV Clin Trials 2018; 19: 85-93. doi: 10.1080/15284336.2018.1452842
  46. Jiao X, Nawab O, Patel T, Kossenkov AV, Halama N, Jaeger D, et al. Recent advances targeting CCR5 for cancer and its role in immuno-oncology. Cancer Res Cancers 2019; 179: 4801-7. doi: 10.1158/0008-5472.CAN-19-1167
  47. Kouno J, Nagai H, Nagahata T, Onda M, Yamaguchi H, Adachi K, et al. Up-regulation of CC chemokine, CCL3L1, and receptors, CCR3, CCR5 in human glioblastoma that promotes cell growth. J Neurooncol 2004; 70: 301-7. doi: 10.1007/s11060-004-9165-3
  48. Laudati E, Currò D, Navarra P, Lisi L. Blockade of CCR5 receptor prevents M2 microglia phenotype in a microglia-glioma paradigm. Neurochem Int 2017; 108: 100-8. doi: 10.1016/j.neuint.2017.03.002
  49. Velasco-Velazquez M, Jiao X, De La Fuente M, Pestell TG, Ertel A, Lisanti MP, et al. CCR5 antagonist blocks metastasis of basal breast cancer cells. Cancer Res 2012; 72: 3839-50. doi: 10.1158/0008-5472.CAN-11-3917
  50. Peng WT, Sun WY, Li XR, Sun JC, Du JJ, Wei W. Emerging roles of G protein-coupled receptors in hepatocellular carcinoma. Int J Mol Sci 2018; 19: pii: E1366. doi: 10.3390/ijms19051366
  51. Murooka TT, Rahbar R, Platanias LC, Fish EN. CCL5-mediated T-cell chemotaxis involves the initiation of mRNA translation through mTOR/4E-BPl. Blood 2008; 111: 4892-901. doi: 10.1182/blood-2007-11-125039
  52. Kahn J, Hayman TJ, Jamal M, Rath BH, Kramp T, Camphausen K, et al. The mTORC1/mTORC2 inhibitor AZD2014 enhances the radiosensitivity of glioblastoma stem-like cells. Neuro Oncol 2014; 16: 29-37. doi: 10.1093/neuonc/not139
  53. Mecca C, Giambanco I, Bruscoli S, Bereshchenko O, Fioretti B, Riccardi C, et al. PP242 counteracts glioblastoma cell proliferation, migration, invasiveness and stemness properties by inhibiting mTORC2/AKT. Front Cell Neurosci 2018; 10: 12:99. doi: 10.3389/fncel.2018.00099
  54. Mecca C, Giambanco I, Donato R, Arcuri C. Targeting mTOR in glioblastoma: rationale and preclinical/clinical evidence. Dis Markers 2018; 18: 1-10. doi: 10.1155/2018/9230479
  55. Murooka TT, Rahbar R, Fish EN. CCL5 promotes proliferation of MCF-7 cells through mTOR-dependent mRNA translation. Biochem Biophys Res Commun 2009; 387: 381-6. doi: 10.1016/j.bbrc.2009.07.035
  56. Zhao L, Wang Y, Xue Y, Lv W, Zhang Y, He S. Critical roles of chemokine receptor CCR5 in regulating glioblastoma proliferation and invasion. Acta Biochim Biophys Sin 2015; 47: 890-8. doi: 10.1093/abbs/gmv095
  57. Wolf K, Friedl P. Extracellular matrix determinants of proteolytic and non-proteolytic cell migration. Trends Cell Biol 2011; 21: 746-8. doi: 10.1016/j. tcb.2011.09.006
  58. Friedl P, Wolf K. Tumour-cell invasion and migration: Diversity and escape mechanisms. Nat Rev Cancer 2003; 3: 362-74. doi: 10.1038/nrc1075
  59. Lah TT, Duran Alonso MB, Van Noorden CJF. Antiprotease therapy in cancer: hot or not? Expert Opin Biol Ther 2006; 6: 257-79. doi: 10.1517/14712598.6.3.257
  60. Bouzahzah B, Albanese C, Ahmed F, Pixley F, Lisanti MP, Segall JD, et al. Rho family GTPases regulate mammary epithelium cell growth and metastasis through distinguishable pathways. Mol Med 2001; 7: 816-30.
  61. Sicoli D, Jiao X, Ju X, Velasco-Velazquez M, Ertel A, Addya S, et al. CCR5 receptor antagonists block metastasis to bone of v-Src oncogene-transformed metastatic prostate cancer cell lines. Cancer Res 2014; 74: 7103-14. doi: 10.1158/0008-5472.CAN-14-0612
  62. Gole B, Huszthy PC, Popović M, Jeruc J, Ardebili YS, Bjerkvig R, et al. The regulation of cysteine cathepsins and cystatins in human gliomas. Int J Cancer 2012; 131: 1779-89. doi: 10.1002/ijc.27453
  63. Colin C, Voutsinos-Porche B, Nanni I, Fina F, Metellus P, Intagliata D, et al. High expression of cathepsin B and plasminogen activator inhibitor type-1 are strong predictors of survival in glioblastomas. Acta Neuropathol 2009; 118: 745-54. doi: 10.1007/s00401-009-0592-2
  64. Wang Y, Liu T, Yang N Xu S, Li X, Wang D, et al. Hypoxia and macrophages, promote glioblastoma invasion by the CCL4-CCR5 axis. Oncol Rep 2016; 36: 3522-8. doi: 10.3892/or.2016.5171
  65. Müller S, Kohanbash G, Liu SJ, Alvarado B, Carrera D, Bhaduri A, et al. Single-cell profiling of human gliomas reveals macrophage ontogeny as a basis for regional differences in macrophage activation in the tumor microenvironment. Genome Biol 2017; 18: 234. doi: 10.1186/s13059-017-1362-4
  66. Matias D, Balça-Silva J, da Graça GC, Wanjiru CM, Macharia LW, Nascimento CP, et al. Microglia/astrocytes-glioblastoma crosstalk: crucial molecular mechanisms and microenvironmental factors. Front Cell Neurosci 2018; 12: 235. doi: 10.3389/fncel.2018.00235
  67. Morisse MC, Jouannet S, Dominguez-Villar M, Sanson M, Idbaih A. Interactions between tumor-associated macrophages and tumor cells in glioblastoma: unraveling promising targeted therapies. Expert Rev Neurother 2018; 18: 729-37. doi: 10.1080/14737175.2018.1510321
  68. Ransohoff RM. A polarizing question: Do M1 and M2 microglia exist. Nature Neuroscience 2016; 19: 987-91. doi: 10.1038/nn.4338
  69. Ban Y, Mai J, Li X, Mitchell-Flack M, Zhang T, Zhang, L, et al. Targeting autocrine CCL5-CCR5 axis reprograms immunosuppressive myeloid cells and reinvigorates antitumor immunity. Cancer Res 2017; 77: 2857-68. doi: 10.1158/0008-5472.CAN-16-2913
  70. Hira VVV, Aderetti DA, van Noorden CJF. Glioma stem cell nichesn in human glioblastoma are periarteriolar. J Histochem Cytochem 2018; 66: 349-58. doi: 10.1369/0022155417752676
  71. Solga AC, Pong WW, Kim KY, Cimino PJ, Toonen JA, Walker J, et al. RNA sequencing of tumor-associated microglia reveals Ccl5 as a stromal chemokine critical for neurofibromatosis-1 glioma growth. Neoplasia 2015; 17: 776-88. doi: 10.1016/j.neo.2015.10.002
  72. Chakraborty R, Rooney C, Dotti G, Savoldo B. Changes in chemokine receptor expression of regulatory T cells after ex vivo culture. J Immunother 2012; 35: 329-36. doi: 10.1097/CJI.0b013e318255adcc
  73. Wang SW, Liu SC, Sun HL, Huang TY. CCL5/CCR5 axis induces vascular endothelial growth factor-mediated tumor angiogenesis in human osteosarcoma microenvironment. Carcinogenesis 2014; 36: 104-14. doi: 10.1093/carcin/bgu218
DOI: https://doi.org/10.2478/raon-2019-0057 | Journal eISSN: 1581-3207 | Journal ISSN: 1318-2099
Language: English
Page range: 397 - 406
Submitted on: Aug 14, 2019
|
Accepted on: Oct 15, 2019
|
Published on: Nov 20, 2019
In partnership with: Paradigm Publishing Services
Publication frequency: 4 issues per year

© 2019 Miha Koprivnikar Kranjc, Metka Novak, Richard G. Pestell, Tamara T. Lah, published by Association of Radiology and Oncology
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License.