CCL2/CCR2 signaling pathway in glioblastoma multiforme

Neurochemistry International

Volumn 103, Issue , 2017, Pages 1-7

  Vakilian, Alireza ^a   Khorramdelazad, Hossein ^a   Heidari, Parisa ^b   Sheikh Rezaei, Zahra ^b   Hassanshahi, Gholamhossein ^a,b  

^a RAFSANJAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b KERMAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

CC chemokine; CCL2; GBM; Glioblastoma; MCP 1

Indexed keywords

CHEMOKINE RECEPTOR CCR2; MONOCYTE CHEMOTACTIC PROTEIN 1; CCR2 PROTEIN, HUMAN; CHEMOKINE RECEPTOR;

BIOLOGICAL FUNCTIONS; CANCER GROWTH; CELL INFILTRATION; CELL MIGRATION; GLIOBLASTOMA; HUMAN; IMMUNOCOMPETENT CELL; MACROPHAGE; MICROGLIA; MONOCYTE; NONHUMAN; PATHOGENESIS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; SURVIVAL RATE; TUMOR INVASION; VASCULAR ENDOTHELIUM; ANIMAL; BRAIN TUMOR; DRUG EFFECTS; METABOLISM; PHYSIOLOGY;

ANIMALS; BRAIN NEOPLASMS; CHEMOKINE CCL2; GLIOBLASTOMA; HUMANS; RECEPTORS, CCR2; RECEPTORS, CHEMOKINE; SIGNAL TRANSDUCTION;

EID: 85007092820     PISSN: 01970186     EISSN: 18729754     Source Type: Journal    
DOI: 10.1016/j.neuint.2016.12.013     Document Type: Review

References (105)

1. Ahmadi, Z., Arababadi, M.K., Hassanshahi, G., CXCL10 activities, biological structure, and source along with its significant role played in pathophysiology of type I diabetes mellitus. Inflammation 36:2 (2013), 364–371.
2. Ahmadi, Z., Hassanshahi, G., Khorramdelazad, H., Zainodini, N., Koochakzadeh, L., An overlook to the characteristics and roles played by eotaxin network in the pathophysiology of food allergies: allergic asthma and atopic dermatitis. Inflammation, 2016, 1–15.
3. Ajuebor, M.N., Flower, R.J., Hannon, R., Christie, M., Bowers, K., Verity, A., Perretti, M., Endogenous monocyte chemoattractant protein-1 recruits monocytes in the zymosan peritonitis model. J. Leukoc. Biol. 63:1 (1998), 108–116.
4. Aminzadeh, F., Ghorashi, Z., Nabati, S., Ghasemshirazi, M., Arababadi, M.K., Shamsizadeh, A., Karimabad, M.N., Khorramdelazad, H., Darakhshan, S., Hassanshahi, G., Differential expression of CXC chemokines CXCL10 and CXCL12 in term and pre-term neonates and their mothers. Am. J. Reproductive Immunol. 68:4 (2012), 338–344.
5. Badie, B., Schartner, J., Klaver, J., Vorpahl, J., In vitro modulation of microglia motility by glioma cells is mediated by hepatocyte growth factor/scatter factor. Neurosurgery 44:5 (1999), 1077–1082.
6. Bajetto, A., Barbieri, F., Dorcaratto, A., Barbero, S., Daga, A., Porcile, C., Ravetti, J.L., Zona, G., Spaziante, R., Corte, G., Expression of CXC chemokine receptors 1–5 and their ligands in human glioma tissues: role of CXCR4 and SDF1 in glioma cell proliferation and migration. Neurochem. Int. 49:5 (2006), 423–432.
7. Bartoli, C., Civatte, M., Pellissier, J., Figarella-Branger, D., CCR2A and CCR2B, the two isoforms of the monocyte chemoattractant protein-1 receptor are up-regulated and expressed by different cell subsets in idiopathic inflammatory myopathies. Acta neuropathol. 102:4 (2001), 385–392.
8. Beall, C., Mahajan, S., Kuhn, D., Kolattukudy, P., Site-directed mutagenesis of monocyte chemoattractant protein-1 identifies two regions of the polypeptide essential for biological activity. Biochem. J. 313 (1996), 633–640.
9. Ben-Baruch, A., The Inflammatory CC Chemokines CCL2 and CCL5 in Malignancy: Leukocyte Migration and beyond. 2012.
10. Ben-Neriah, Y., Karin, M., Inflammation meets cancer, with NF-[kappa] B as the matchmaker. Nat. Immunol. 12:8 (2011), 715–723.
11. Bowman, R.L., Joyce, J.A., Therapeutic targeting of tumor-associated macrophages and microglia in glioblastoma. Immunotherapy 6 (2014), 663–666.
12. Brown, Z., Robson, R.L., Westwick, J., Regulation and expression of chemokines: potential role in glomerulonephritis. J. Leukoc. Biol. 59:1 (1996), 75–80.
13. Carvalho da Fonseca, A.C., Badie, B., Microglia and macrophages in malignant gliomas: recent discoveries and implications for promising therapies. Clin. Dev. Immunol., 2013, 2013, 5 Article ID 264124.
14. Charles, N.A., Holland, E.C., Gilbertson, R., Glass, R., Kettenmann, H., The brain tumor microenvironment. Glia 59:8 (2011), 1169–1180.
15. Charo, I.F., Myers, S.J., Herman, A., Franci, C., Connolly, A.J., Coughlin, S.R., Molecular cloning and functional expression of two monocyte chemoattractant protein 1 receptors reveals alternative splicing of the carboxyl-terminal tails. Proc. Natl. Acad. Sci. 91:7 (1994), 2752–2756.
16. Cho, M.-L., Yoon, B.-Y., Ju, J.-H., Jung, Y.O., Jhun, J.-Y., Park, M.-K., Park, S.-H., Cho, C.-S., Kim, H.-Y., Expression of CCR2A, an isoform of MCP-1 receptor, is increased by MCP-1, CD40 ligand and TGF-β in fibroblast like synoviocytes of patients with RA. Exp. Mol. Med. 39:4 (2007), 499–507.
17. Chun, E., Lavoie, S., Michaud, M., Gallini, C.A., Kim, J., Soucy, G., Odze, R., Glickman, J.N., Garrett, W.S., CCL2 promotes colorectal carcinogenesis by enhancing polymorphonuclear myeloid-derived suppressor cell population and function. Cell. Rep. 12:2 (2015), 244–257.
18. Cochran, B.H., Reffel, A.C., Stiles, C.D., Molecular cloning of gene sequences regulated by platelet-derived growth factor. Cell 33:3 (1983), 939–947.
19. Coniglio, S.J., Eugenin, E., Dobrenis, K., Stanley, E.R., West, B.L., Symons, M.H., Segall, J.E., Microglial stimulation of glioblastoma invasion involves epidermal growth factor receptor (EGFR) and colony stimulating factor 1 receptor (CSF-1R) signaling. Mol. Med., 18(3), 2012, 519.
20. Derakhshan, R., Arababadi, M.K., Ahmadi, Z., Karimabad, M.N., Salehabadi, V.A., Abedinzadeh, M., Khorramdelazad, H., Balaei, P., Kennedy, D., Hassanshahi, G., Increased circulating levels of SDF-1 (CXCL12) in type 2 diabetic patients are correlated to disease state but are unrelated to polymorphism of the SDF-1β gene in the Iranian population. Inflammation 35:3 (2012), 900–904.
21. Desbaillets, I., Tada, M., De Tribolet, N., Diserens, A.C., Hamou, M.F., Van Meir, E.G., Human astrocytomas and glioblastomas express monocyte chemoattractant protein-1 (MCP-1) in vivo and in vitro. Int. J. cancer 58:2 (1994), 240–247.
22. Deshmane, S.L., Kremlev, S., Amini, S., Sawaya, B.E., Monocyte chemoattractant protein-1 (MCP-1): an overview. J. interferon & cytokine Res. 29:6 (2009), 313–326.
23. Ebisawa, M., Yamada, T., Bickel, C., Klunk, D., Schleimer, R.P., Eosinophil transendothelial migration induced by cytokines. III. Effect of the chemokine RANTES. J. Immunol. 153:5 (1994), 2153–2160.
24. Feng, W., Flores-Villanueva, P., Mokrousov, I., Wu, X., Xiao, J., Jiao, W., Sun, L., Miao, Q., Shen, C., Shen, D., CCL2− 2518 (A/G) polymorphisms and tuberculosis susceptibility: a meta-analysis [Review article]. Int. J. Tuberc. Lung Dis. 16:2 (2012), 150–156.
25. Feria, M., Díaz-González, F., The CCR2 Receptor as a Therapeutic Target. 2006.
26. Fuentes, M.E., Durham, S.K., Swerdel, M.R., Lewin, A.C., Barton, D.S., Megill, J.R., Bravo, R., Lira, S.A., Controlled recruitment of monocytes and macrophages to specific organs through transgenic expression of monocyte chemoattractant protein-1. J. Immunol. 155:12 (1995), 5769–5776.
27. Furth, R., Diesselhoff-Den Dulk, M., Method to prove ingestion of particles by macrophages with light microscopy. Scand. J. Immunol. 12:3 (1980), 265–269.
28. Gong, J.-H., Clark-Lewis, I., Antagonists of monocyte chemoattractant protein 1 identified by modification of functionally critical NH2-terminal residues. J. Exp. Med. 181:2 (1995), 631–640.
29. Gong, J.-H., Ratkay, L.G., Waterfield, J.D., Clark-Lewis, I., An antagonist of monocyte chemoattractant protein 1 (MCP-1) inhibits arthritis in the MRL-lpr mouse model. J. Exp. Med. 186:1 (1997), 131–137.
30. Gunn, M.D., Nelken, N.A., Liao, X., Williams, L.T., Monocyte chemoattractant protein-1 is sufficient for the chemotaxis of monocytes and lymphocytes in transgenic mice but requires an additional stimulus for inflammatory activation. J. Immunol. 158:1 (1997), 376–383.
31. Haberstroh, U., Stilo, K., Pocock, J., Wolf, G., Helmchen, U., Wenzel, U., Zahner, G., Stahl, R., Thaiss, F., L-arginine suppresses lipopolysaccharide-induced expression of RANTES in glomeruli. J. Am. Soc. Nephrol. 9:2 (1998), 203–210.
32. Handel, T.M., Domaille, P.J., Heteronuclear (1H, 13C, 15N) NMR assignments and solution structure of the monocyte chemoattractant protein-1 (MCP-1) dimer. Biochemistry 35:21 (1996), 6569–6584.
33. Hassanshahi, G., Amin, M., Shunmugavel, A., Vazirinejad, R., Vakilian, A., Sanji, M., Shamsizadeh, A., RafatPanah, H., Poor, N.M., Moosavi, S.R., Temporal expression profile of CXC chemokines in serum of patients with spinal cord injury. Neurochem. Int. 63:5 (2013), 363–367.
34. Hayashida, K., Nanki, T., Girschick, H., Yavuz, S., Ochi, T., Lipsky, P.E., Synovial stromal cells from rheumatoid arthritis patients attract monocytes by producing MCP-1 and IL-8. Arthritis Res. 3:2 (2001), 118–126.
35. 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.
36. Hernández-Aguilera, A., Cabré, N., Luciano-Mateo, F., Rodríguez-Gallego, E., Guirro, M., Fernández-Arroyo, S., Mariné-Casadó, R., Camps, J., Joven, J., Expression of functional and silent receptors of CCL2 in human coronary arteries. Atherosclerosis 241:1 (2015), e91–e92.
37. Hu, W., Li, X., Zhang, C., Yang, Y., Jiang, J., Wu, C., Tumor-associated macrophages in cancers. Clin. Transl. Oncol., 2015, 1–8.
38. Huse, J.T., Holland, E.C., Targeting brain cancer: advances in the molecular pathology of malignant glioma and medulloblastoma. Nat. Rev. cancer 10:5 (2010), 319–331.
39. Hussain, S.F., Yang, D., Suki, D., Aldape, K., Grimm, E., Heimberger, A.B., The role of human glioma-infiltrating microglia/macrophages in mediating antitumor immune responses. Neuro-oncology 8:3 (2006), 261–279.
40. Jala, V., Bodduluri, S., Chilton, P., Bodduluri, H., CCR2 mediated inflammation and gut microbiota in promoting intestinal cancer (CCR5P. 214). J. Immunol., 194(1 Suppl. ment), 2015, 186 116-186.116.
41. Jordan, J.T., Sun, W., Hussain, S.F., DeAngulo, G., Prabhu, S.S., Heimberger, A.B., Preferential migration of regulatory T cells mediated by glioma-secreted chemokines can be blocked with chemotherapy. Cancer Immunol. Immunother. 57:1 (2008), 123–131.
42. Khorramdelazad, H., Bagheri, V., Hassanshahi, G., Zeinali, M., Vakilian, A., New insights into the role of stromal cell-derived factor 1 (SDF-1/CXCL12) in the pathophysiology of multiple sclerosis. J. Neuroimmunol. 290 (2016), 70–75.
43. Kielian, T., van Rooijen, N., Hickey, W.F., MCP-1 expression in CNS-1 astrocytoma cells: implications for macrophage infiltration into tumors in vivo. J. neuro-oncology 56:1 (2002), 1–12.
44. Kitamoto, S., Egashira, K., Anti-monocyte Chemoattractant Protein-1 Gene Therapy for Cardiovascular Diseases. 2003.
45. Kitamura, T., Qian, B.-Z., Soong, D., Cassetta, L., Noy, R., Sugano, G., Kato, Y., Li, J., Pollard, J.W., CCL2-induced chemokine cascade promotes breast cancer metastasis by enhancing retention of metastasis-associated macrophages. J. Exp. Med. 212:7 (2015), 1043–1059.
46. Kothur, K., Wienholt, L., Brilot, F., Dale, R.C., CSF cytokines/chemokines as biomarkers in neuroinflammatory CNS disorders: a systematic review. Cytokine 77 (2016), 227–237.
47. Kucheryavykh, L.Y., Rivera-Pagán, A.F., Rolón-Reyes, K., Skatchkov, S.N., Eaton, M.J., Role of monocyte chemotactic protein-1 (MCP-1) in the tumor microenvironment. Cancer Res., 73(8 Suppl. ment), 2013, 1429 1429.
48. Kuratsu, J.-i., Yoshizato, K., Yoshimura, T., Leonard, E.J., Takeshima, H., Ushio, Y., Quantitative study of monocyte chemoattractant protein-1 (MCP-1) in cerebrospinal fluid and cyst fluid from patients with malignant glioma. J. Natl. Cancer Inst. 85:22 (1993), 1836–1839.
49. Kurihara, T., Warr, G., Loy, J., Bravo, R., Defects in macrophage recruitment and host defense in mice lacking the CCR2 chemokine receptor. J. Exp. Med. 186:10 (1997), 1757–1762.
50. Le, D.M., Besson, A., Fogg, D.K., Choi, K.-S., Waisman, D.M., Goodyer, C.G., Rewcastle, B., Yong, V.W., Exploitation of astrocytes by glioma cells to facilitate invasiveness: a mechanism involving matrix metalloproteinase-2 and the urokinase-type plasminogen activator–plasmin cascade. J. Neurosci. 23:10 (2003), 4034–4043.
51. Lindemann, C., Marschall, V., Weigert, A., Klingebiel, T., Fulda, S., Smac mimetic-induced upregulation of CCL2/MCP-1 triggers migration and invasion of glioblastoma cells and influences the tumor microenvironment in a paracrine manner. Neoplasia 17:6 (2015), 481–489.
52. Liu, Y., Wu, H.-W., Sheard, M.A., Sposto, R., Somanchi, S.S., Cooper, L.J., Lee, D.A., Seeger, R.C., Growth and activation of natural killer cells ex vivo from children with neuroblastoma for adoptive cell therapy. Clin. Cancer Res. 19:8 (2013), 2132–2143.
53. Liu, Z., Haelens, A., Wuyts, A., Struyf, S., Pang, X., Proost, P., Chen, W., Van Damme, J., Isolation of a lymphocyte chemotactic factor produced by the murine thymic epithelial cell line MTEC1: identification as a 30 kDa glycosylated form of MCP-1. Eur. cytokine Netw. 7:3 (1996), 381–388.
54. Lubkowski, J., Bujacz, G., Boqué, L., Alexander, W., The structure of MCP-1 in two crystal forms provides a rare example of variable quaternary interactions. Nat. Struct. Mol. Biol. 4:1 (1997), 64–69.
55. Mafuvadze, B., Fang, W.B., Cheng, N., Abstract P4-05-02: overexpression of the chemokine receptor CCR2 in the breast epithelium is associated with progression of DCIS. Cancer Res., 75(9 Suppl. ment), 2015 P4–05-02-P04-05-02.
56. Meunier, S., Bernassau, J.-M., Guillemot, J.-C., Ferrara, P., Darbon, H., Determination of the three-dimensional structure of CC chemokine monocyte chemoattractant protein 3 by 1H two-dimensional NMR spectroscopy. Biochemistry 36:15 (1997), 4412–4422.
57. Miller, R.E., Tran, P.B., Das, R., Ghoreishi-Haack, N., Ren, D., Miller, R.J., Malfait, A.-M., CCR2 chemokine receptor signaling mediates pain in experimental osteoarthritis. Proc. Natl. Acad. Sci. 109:50 (2012), 20602–20607.
58. Mishra, R., Kovalska, J., Janda, J., Vannucci, L., Rajmon, R., Horak, V., Tumor progression is associated with increasing CD11b+ cells and CCL2 in lewis rat sarcoma. Anticancer Res. 35:2 (2015), 703–711.
59. Moogooei, M., Shamaei, M., Khorramdelazad, H., Fattahpour, S., Seyedmehdi, S.M., Moogooei, M., Hassanshahi, G., Khandani, B.K., The intricate expression of CC chemokines in glial tumors: evidence for involvement of CCL2 and CCL5 but not CCL11. Acta Medica Iran. 53:12 (2015), 770–777.
60. Moosavi, S.R., Khorramdelazad, H., Amin, M., Fatahpoor, S., Moogooei, M., Karimabad, M.N., Paghale, M.J., Vakilian, A., Hassanshahi, G., The SDF-1 3'A genetic variation is correlated with elevated intra-tumor tissue and circulating concentration of CXCL12 in glial tumors. J. Mol. Neurosci. 50:2 (2013), 298–304.
61. Mukaida, N., Baba, T., Chemokines in tumor development and progression. Exp. Cell. Res. 318:2 (2012), 95–102.
62. Ni, W., Egashira, K., Kitamoto, S., Kataoka, C., Koyanagi, M., Inoue, S., Imaizumi, K., Akiyama, C., Nishida, K.-i., Takeshita, A., New anti–monocyte chemoattractant protein-1 gene therapy attenuates atherosclerosis in apolipoprotein E–knockout mice. Circulation 103:16 (2001), 2096–2101.
63. Oh, J.-W., Schwiebert, L.M., Benveniste, E.N., Cytokine regulation of CC and CXC chemokine expression by human astrocytes. J. neurovirology 5:1 (1999), 82–94.
64. Okada, M., Saio, M., Kito, Y., Ohe, N., Yano, H., Yoshimura, S., Iwama, T., Takami, T., Tumor-associated macrophage/microglia infiltration in human gliomas is correlated with MCP-3, but not MCP-1. Int. J. Oncol. 34:6 (2009), 1621–1627.
65. Ostadebrahimi, H., Jamali, Z., Nazari, M., Bahri, M., Farahmandnia, Z., Khandany, B.K., Taheri, M., Khorramdelazad, H., Hakimizadeh, E., Zaker, F., CXC chemokines CXCL1, CXCL9, CXCL10 and CXCL12 are variably expressed in patients with sickle cell disease and carriers: are they predictive tools for disease complications?. Clin. Lab. 60:1 (2013), 99–104.
66. Palframan, R.T., Jung, S., Cheng, G., Weninger, W., Luo, Y., Dorf, M., Littman, D.R., Rollins, B.J., Zweerink, H., Rot, A., Inflammatory chemokine transport and presentation in hev a remote control mechanism for monocyte recruitment to lymph nodes in inflamed tissues. J. Exp. Med. 194:9 (2001), 1361–1374.
67. Platten, M., Kretz, A., Naumann, U., Aulwurm, S., Egashira, K., Isenmann, S., Weller, M., Monocyte chemoattractant protein–1 increases microglial infiltration and aggressiveness of gliomas. Ann. neurology 54:3 (2003), 388–392.
68. Polverini, P.J., Cotran, R.S., Gimbrone, M.A., Unanue, E.R., Activated Macrophages Induce Vascular Proliferation. 1977.
69. Proudfoot, A.E., Chemokine receptors: multifaceted therapeutic targets. Nat. Rev. Immunol. 2:2 (2002), 106–115.
70. Reid, C., Rushe, M., Jarpe, M., van Vlijmen, H., Dolinski, B., Qian, F., Cachero, T.G., Cuervo, H., Yanachkova, M., Nwankwo, C., Structure activity relationships of monocyte chemoattractant proteins in complex with a blocking antibody. Protein Eng. Des. Sel. 19:7 (2006), 317–324.
71. Rodero, M.P., Combadière, C., Boissonnas, A., Role of chemokines and chemokine receptors in cancer. Springer Cancer Immunol., 2015, 121–142.
72. Rutar, M., Provis, J.M., Role of chemokines in shaping macrophage activity in AMD. Springer Retin. Degener. Dis., 2016, 11–16.
73. Salacz, M.E., Kast, R.E., Saki, N., Brüning, A., Karpel-Massler, G., Halatsch, M.-E., Toward a noncytotoxic glioblastoma therapy: blocking MCP-1 with the MTZ Regimen. OncoTargets Ther., 9, 2016, 2535.
74. Salmaggi, A., Gelati, M., Pollo, B., Frigerio, S., Eoli, M., Silvani, A., Broggi, G., Ciusani, E., Croci, D., Boiardi, A., CXCL12 in malignant glial tumors: a possible role in angiogenesis and cross-talk between endothelial and tumoral cells. J. neuro-oncology 67:3 (2004), 305–317.
75. Sanders, S.K., Crean, S.M., Boxer, P.A., Kellner, D., LaRosa, G.J., Hunt, S.W., Functional differences between monocyte chemotactic protein-1 receptor A and monocyte chemotactic protein-1 receptor B expressed in a Jurkat T cell. J. Immunol. 165:9 (2000), 4877–4883.
76. Sarvaiya, P.J., Guo, D., Ulasov, I., Gabikian, P., Lesniak, M.S., Chemokines in tumor progression and metastasis. Oncotarget, 4(12), 2013, 2171.
77. Schaper, J., König, R., Franz, D., Schaper, W., The endothelial surface of growing coronary collateral arteries. Intimal margination and diapedesis of monocytes. Virchows Arch. A 370:3 (1976), 193–205.
78. Scholz, D., Cai, W.-j., Schaper, W., Arteriogenesis, a new concept of vascular adaptation in occlusive disease. Angiogenesis 4:4 (2001), 247–257.
79. Scholz, D., Ito, W., Fleming, I., Deindl, E., Sauer, A., Wiesnet, M., Busse, R., Schaper, J., Schaper, W., Ultrastructure and molecular histology of rabbit hind-limb collateral artery growth (arteriogenesis). Virchows Arch. 436:3 (2000), 257–270.
80. Sciumè, G., Santoni, A., Bernardini, G., Chemokines and glioma: invasion and more. J. Neuroimmunol. 224:1 (2010), 8–12.
81. Semple, B.D., Kossmann, T., Morganti-Kossmann, M.C., Role of chemokines in CNS health and pathology: a focus on the CCL2/CCR2 and CXCL8/CXCR2 networks. J. Cereb. Blood Flow Metabolism 30:3 (2010), 459–473.
82. Sordet, O., Rébé, C., Plenchette, S., Zermati, Y., Hermine, O., Vainchenker, W., Garrido, C., Solary, E., Dubrez-Daloz, L., Specific involvement of caspases in the differentiation of monocytes into macrophages. Blood 100:13 (2002), 4446–4453.
83. Sørensen, T.L., Ransohoff, R., Strieter, R., Sellebjerg, F., Chemokine CCL2 and chemokine receptor CCR2 in early active multiple sclerosis. Eur. J. Neurology 11:7 (2004), 445–449.
84. Takeshima, H., Kuratsu, J.-I., Takeya, M., Yoshimura, T., Ushio, Y., Expression and localization of messenger RNA and protein for monocyte chemoattractant protein-1 in human malignant glioma. J. Neurosurg. 80:6 (1994), 1056–1062.
85. Terasaki, M., Sugita, Y., Arakawa, F., Okada, Y., Ohshima, K., Shigemori, M., CXCL12/CXCR4 signaling in malignant brain tumors: a potential pharmacological therapeutic target. Brain tumor pathol. 28:2 (2011), 89–97.
86. Tsuyada, A., Chow, A., Wu, J., Somlo, G., Chu, P., Loera, S., Luu, T., Li, A.X., Wu, X., Ye, W., CCL2 mediates cross-talk between cancer cells and stromal fibroblasts that regulates breast cancer stem cells. Cancer Res. 72:11 (2012), 2768–2779.
87. Uguccioni, M., D'Apuzzo, M., Loetscher, M., Dewald, B., Baggiolini, M., Actions of the chemotactic cytokines MCP-1, MCP-2, MCP-3, RANTES, MIP-1α and MIP-1β on human monocytes. Eur. J. Immunol. 25:1 (1995), 64–68.
88. Valković, T., Dobrila, F., Melato, M., Sasso, F., Rizzardi, C., Jonjić, N., Correlation between vascular endothelial growth factor, angiogenesis, and tumor-associated macrophages in invasive ductal breast carcinoma. Virchows Arch. 440:6 (2002), 583–588.
89. Van Coillie, E., Van Damme, J., Opdenakker, G., The MCP/eotaxin subfamily of CC chemokines. Cytokine & growth factor Rev. 10:1 (1999), 61–86.
90. van Furth, R., Cohn, Z.A., The origin and kinetics of mononuclear phagocytes. J. Exp. Med. 128:3 (1968), 415–435.
91. Van Furth, R., Diesselhoff-Den Dulk, M.M., Mattie, H., Quantitative study on the production and kinetics of mononuclear phagocytes during an acute inflammatory reaction. J. Exp. Med. 138:6 (1973), 1314–1330.
92. Vazirinejad, R., Ahmadi, Z., Kazemi Arababadi, M., Hassanshahi, G., Kennedy, D., The biological functions, structure and sources of CXCL10 and its outstanding part in the pathophysiology of multiple sclerosis. Neuroimmunomodulation 21:6 (2014), 322–330.
93. von Hanwehr, R.I., Hofman, F.M., Taylor, C.R., Apuzzo, M.L., Mononuclear lymphoid populations infiltrating the microenvironment of primary CNS tumors: characterization of cell subsets with monoclonal antibodies. J. Neurosurg. 60:6 (1984), 1138–1147.
94. Wang, S.-C., Hong, J.-H., Hsueh, C., Chiang, C.-S., Tumor-secreted SDF-1 promotes glioma invasiveness and TAM tropism toward hypoxia in a murine astrocytoma model. Lab. Investig. 92:1 (2012), 151–162.
95. Wieser, V., Moschen, A.R., Tilg, H., Inflammation, cytokines and insulin resistance: a clinical perspective. Archivum Immunol. Ther. Exp. 61:2 (2013), 119–125.
96. Wolf, M.J., Hoos, A., Bauer, J., Boettcher, S., Knust, M., Weber, A., Simonavicius, N., Schneider, C., Lang, M., Stürzl, M., Endothelial CCR2 signaling induced by colon carcinoma cells enables extravasation via the JAK2-Stat5 and p38MAPK pathway. Cancer Cell. 22:1 (2012), 91–105.
97. Yadav, A., Saini, V., Arora, S., MCP-1: chemoattractant with a role beyond immunity: a review. Clin. Chim. acta 411:21 (2010), 1570–1579.
98. Yang, J., Lv, X., Xiang, Y., Guo, X., Chen, J., Guan, X., CCL2/CCR2 axis signaling promotes metastasis of nasopharyngeal carcinoma by activating ERK1/2 pathway via upregulating MMP2 and MMP9. Cancer Res., 75(15 Suppl. ment), 2015, 2254 2254.
99. Yeo, T.K., Ahad, M.A., Kuo, N.-w., Spagnolo, P., Menezo, V., Lympany, P., Lightman, S., Chemokine gene polymorphisms in idiopathic anterior uveitis. Cytokine 35:1 (2006), 29–35.
100. Yoshimura, T., Robinson, E.A., Tanaka, S., Appella, E., Kuratsu, J.-l., Leonard, E.J., Purification and amino acid analysis of two human glioma-derived monocyte chemoattractants. J. Exp. Med. 169:4 (1989), 1449–1459.
101. Zachariae, C., Anderson, A., Thompson, H., Appella, E., Mantovani, A., Oppenheim, J., Matsushima, K., Properties of monocyte chemotactic and activating factor (MCAF) purified from a human fibrosarcoma cell line. J. Exp. Med. 171:6 (1990), 2177–2182.
102. Zhang, H., Hinkle, C.C., O'Neill, S., Caughey, J., Lynch, E., Lynch, G., Shah, R., Ahima, R.S., Reilly, M.P., CX3CR1 and CCR2 synergistically modulate inflammatory but not metabolic effects of high-fat feeding. Circulation, 132(Suppl. 3), 2015, A16039 A16039.
103. Zhang, J., Sarkar, S., Cua, R., Zhou, Y., Hader, W., Yong, V.W., A dialog between glioma and microglia that promotes tumor invasiveness through the CCL2/CCR2/interleukin-6 axis. Carcinog. bgr, 289, 2011.
104. Zhang, Y., Rollins, B.J., A dominant negative inhibitor indicates that monocyte chemoattractant protein 1 functions as a dimer. Mol. Cell. Biol. 15:9 (1995), 4851–4855.
105. Zhu, X., Fujita, M., Snyder, L.A., Okada, H., Systemic delivery of neutralizing antibody targeting CCL2 for glioma therapy. J. neuro-oncology 104:1 (2011), 83–92.