Cytokine & Growth Factor Reviews
Volume 21, Issue 1 , Pages 41-48 , February 2010

CC chemokine ligand 2 (CCL2) promotes prostate cancer tumorigenesis and metastasis

  • Jian Zhang
  • ,
  • Lalit Patel
  • ,
  • Kenneth J. Pienta

      Affiliations

    • Corresponding Author InformationCorresponding author at: 1500 E. Medical Center Drive, 7303 CCC, Ann Arbor, MI 48109-5946, United States. Tel.: +1 734 647 3421; fax: +1 734 647 9480.

References 

  1. Balkwill F. Cancer and the chemokine network. Nat Rev Cancer. 2004;4(July (7)):540–550
  2. Taichman RS, Loberg RD, Mehra R, Pienta KJ. The evolving biology and treatment of prostate cancer. J Clin Invest. 2007;117(September (9)):2351–2361
  3. Balkwill F. Chemokine biology in cancer. Semin Immunol. 2003;15(February (1)):49–55
  4. Craig MJ, Loberg RD. CCL2 (Monocyte Chemoattractant Protein-1) in cancer bone metastases. Cancer Metastasis Rev. 2006;25(December (4)):611–619
  5. Charo IF, Taubman MB. Chemokines in the pathogenesis of vascular disease. Circ Res. 2004;95(October (9)):858–866
  6. Loberg RD, Day LL, Harwood J, Ying C, St John LN, Giles R, et al. CCL2 is a potent regulator of prostate cancer cell migration and proliferation. Neoplasia. 2006;8(July (7)):578–586
  7. Loberg RD, Tantivejkul K, Craig M, Neeley CK, Pienta KJ. PAR1-mediated RhoA activation facilitates CCL2-induced chemotaxis in PC-3 cells. J Cell Biochem. 2007;101(August (5)):1292–1300
  8. Lu Y, Cai Z, Galson DL, Xiao G, Liu Y, George DE, et al. Monocyte chemotactic protein-1 (MCP-1) acts as a paracrine and autocrine factor for prostate cancer growth and invasion. Prostate. 2006;66(September (12)):1311–1318
  9. Lu Y, Xiao G, Galson DL, Nishio Y, Mizokami A, Keller ET, et al. PTHrP-induced MCP-1 production by human bone marrow endothelial cells and osteoblasts promotes osteoclast differentiation and prostate cancer cell proliferation and invasion in vitro. Int J Cancer. 2007;121(August (4)):724–733
  10. Valente AJ, Graves DT, Vialle-Valentin CE, Delgado R, Schwartz CJ. Purification of a monocyte chemotactic factor secreted by nonhuman primate vascular cells in culture. Biochemistry. 1988;27(March (11)):4162–4168
  11. Yoshimura T, Robinson EA, Tanaka S, Appella E, Kuratsu J, Leonard EJ. Purification and amino acid analysis of two human glioma-derived monocyte chemoattractants. J Exp Med. 1989;169(April (4)):1449–1459
  12. Matsushima K, Larsen CG, DuBois GC, Oppenheim JJ. Purification and characterization of a novel monocyte chemotactic and activating factor produced by a human myelomonocytic cell line. J Exp Med. 1989;169(April (4)):1485–1490
  13. Mehrabian M, Sparkes RS, Mohandas T, Fogelman AM, Lusis AJ. Localization of monocyte chemotactic protein-1 gene (SCYA2) to human chromosome 17q11.2–q21.1. Genomics. 1991;9(January (1)):200–203
  14. Enjuanes A, Benavente Y, Bosch F, Martin-Guerrero I, Colomer D, Perez-Alvarez S, et al. Genetic variants in apoptosis and immunoregulation-related genes are associated with risk of chronic lymphocytic leukemia. Cancer Res. 2008;68(December (24)):10178–10186
  15. Rovin BH, Lu L, Saxena R. A novel polymorphism in the MCP-1 gene regulatory region that influences MCP-1 expression. Biochem Biophys Res Commun. 1999;259(June (2)):344–348
  16. Ghilardi G, Biondi ML, La Torre A, Battaglioli L, Scorza R. Breast cancer progression and host polymorphisms in the chemokine system: role of the macrophage chemoattractant protein-1 (MCP-1)-2518 G allele. Clin Chem. 2005;51(February (2)):452–455
  17. Tse KP, Tsang NM, Chen KD, Li HP, Liang Y, Hsueh C, et al. MCP-1 Promoter Polymorphism at 2518 is associated with metastasis of nasopharyngeal carcinoma after treatment. Clin Cancer Res. 2007;13(November (21)):6320–6326
  18. Smith MW, Dean M, Carrington M, Winkler C, Huttley GA, Lomb DA, et al. Contrasting genetic influence of CCR2 and CCR5 variants on HIV-1 infection and disease progression. Hemophilia Growth and Development Study (HGDS), Multicenter AIDS Cohort Study (MACS), Multicenter Hemophilia Cohort Study (MHCS), San Francisco City Cohort (SFCC), ALIVE Study. Science. 1997;277(August (5328)):959–965
  19. Lu Y, Chen Q, Corey E, Xie W, Fan J, Mizokami A, et al. Activation of MCP-1/CCR2 axis promotes prostate cancer growth in bone. Clin Exp Metastasis. 2009;26(2):161–169
  20. O’Brien SJ, Moore JP. The effect of genetic variation in chemokines and their receptors on HIV transmission and progression to AIDS. Immunol Rev. 2000;177(October):99–111
  21. Zafiropoulos A, Crikas N, Passam AM, Spandidos DA. Significant involvement of CCR2-64I and CXCL12-3a in the development of sporadic breast cancer. J Med Genet. 2004;41(May (5)):e59
  22. Zheng B, Wiklund F, Gharizadeh B, Sadat M, Gambelunghe G, Hallmans G, et al. Genetic polymorphism of chemokine receptors CCR2 and CCR5 in Swedish cervical cancer patients. Anticancer Res. 2006;26(September–October (5B)):3669–3674
  23. Bost KL, Bento JL, Petty CC, Schrum LW, Hudson MC, Marriott I. Monocyte chemoattractant protein-1 expression by osteoblasts following infection with Staphylococcus aureus or Salmonella. J Interferon Cytokine Res. 2001;21(May (5)):297–304
  24. Vanderkerken K, Vande Broek I, Eizirik DL, Van Valckenborgh E, Asosingh K, Van Riet I, et al. Monocyte chemoattractant protein-1 (MCP-1), secreted by bone marrow endothelial cells, induces chemoattraction of 5T multiple myeloma cells. Clin Exp Metastasis. 2002;19(1):87–90
  25. Lu Y, Cai Z, Xiao G, Keller ET, Mizokami A, Yao Z, et al. Monocyte chemotactic protein-1 mediates prostate cancer-induced bone resorption. Cancer Res. 2007;67(April (8)):3646–3653
  26. Roca H, Varsos Z, Pienta KJ. CCL2 protects prostate cancer PC3 cells from autophagic death via phosphatidylinositol 3-kinase/AKT-dependent survivin up-regulation. J Biol Chem. 2008;283(September (36)):25057–25073
  27. Roca H, Varsos ZS, Mizutani K, Pienta KJ. CCL2, survivin and autophagy: new links with implications in human cancer. Autophagy. 2008;4(October (7)):969–971
  28. van Golen KL, Ying C, Sequeira L, Dubyk CW, Reisenberger T, Chinnaiyan AM, et al. CCL2 induces prostate cancer transendothelial cell migration via activation of the small GTPase Rac. J Cell Biochem. 2008;104(August (5)):1587–1597
  29. Fox SB, Harris AL. Markers of tumor angiogenesis: clinical applications in prognosis and anti-angiogenic therapy. Invest New Drugs. 1997;15(1):15–28
  30. Salcedo R, Ponce ML, Young HA, Wasserman K, Ward JM, Kleinman HK, et al. Human endothelial cells express CCR2 and respond to MCP-1: direct role of MCP-1 in angiogenesis and tumor progression. Blood. 2000;96(July (1)):34–40
  31. Goede V, Brogelli L, Ziche M, Augustin HG. Induction of inflammatory angiogenesis by monocyte chemoattractant protein-1. Int J Cancer. 1999;82(August (5)):765–770
  32. Li X, Loberg R, Liao J, Ying C, Snyder LA, Pienta KJ, et al. A destructive cascade mediated by CCL2 facilitates prostate cancer growth in bone. Cancer Res. 2009;69(February (4)):1685–1692
  33. Loberg RD, Ying C, Craig M, Yan L, Snyder LA, Pienta KJ. CCL2 as an important mediator of prostate cancer growth in vivo through the regulation of macrophage infiltration. Neoplasia. 2007;9(July (7)):556–562
  34. Soria G, Ben-Baruch A. The inflammatory chemokines CCL2 and CCL5 in breast cancer. Cancer Lett. 2008;267(August (2)):271–285
  35. Aggarwal R, Ghobrial IM, Roodman GD. Chemokines in multiple myeloma. Exp Hematol. 2006;34(October (10)):1289–1295
  36. Ueno T, Toi M, Saji H, Muta M, Bando H, Kuroi K, et al. Significance of macrophage chemoattractant protein-1 in macrophage recruitment, angiogenesis, and survival in human breast cancer. Clin Cancer Res. 2000;6(August (8)):3282–3289
  37. Hong KH, Ryu J, Han KH. Monocyte chemoattractant protein-1-induced angiogenesis is mediated by vascular endothelial growth factor-A. Blood. 2005;105(February (4)):1405–1407
  38. Gu L, Tseng S, Horner RM, Tam C, Loda M, Rollins BJ. Control of TH2 polarization by the chemokine monocyte chemoattractant protein-1. Nature. 2000;404(March (6776)):407–411
  39. Kelly PM, Davison RS, Bliss E, McGee JO. Macrophages in human breast disease: a quantitative immunohistochemical study. Br J Cancer. 1988;57(February (2)):174–177
  40. Sica A, Schioppa T, Mantovani A, Allavena P. Tumour-associated macrophages are a distinct M2 polarised population promoting tumour progression: potential targets of anti-cancer therapy. Eur J Cancer. 2006;42(April (6)):717–727
  41. Stephens TC, Currie GA, Peacock JH. Repopulation of gamma-irradiated Lewis lung carcinoma by malignant cells and host macrophage progenitors. Br J Cancer. 1978;38(November (5)):573–582
  42. Lewis CE, Pollard JW. Distinct role of macrophages in different tumor microenvironments. Cancer Res. 2006;66(January (2)):605–612
  43. Negus RP, Stamp GW, Hadley J, Balkwill FR. Quantitative assessment of the leukocyte infiltrate in ovarian cancer and its relationship to the expression of C–C chemokines. Am J Pathol. 1997;150(May (5)):1723–1734
  44. Azenshtein E, Luboshits G, Shina S, Neumark E, Shahbazian D, Weil M, et al. The CC chemokine RANTES in breast carcinoma progression: regulation of expression and potential mechanisms of promalignant activity. Cancer Res. 2002;62(February (4)):1093–1102
  45. Mantovani A, Bottazzi B, Colotta F, Sozzani S, Ruco L. The origin and function of tumor-associated macrophages. Immunol Today. 1992;13(July (7)):265–270
  46. Morrissey C, Kostenuik PL, Brown LG, Vessella RL, Corey E. Host-derived RANKL is responsible for osteolysis in a C4-2 human prostate cancer xenograft model of experimental bone metastases. BMC Cancer. 2007;7:148
  47. Mizutani K, Sud S, Pienta KJ. Prostate cancer promotes CD11b positive cells to differentiate into osteoclasts. J Cell Biochem. 2009;106(March (4)):563–569
  48. Daly C, Rollins BJ. Monocyte chemoattractant protein-1 (CCL2) in inflammatory disease and adaptive immunity: therapeutic opportunities and controversies. Microcirculation. 2003;10(June (3–4)):247–257
  49. Musso T, Cappello P, Stornello S, Ravarino D, Caorsi C, Otero K, et al. IL-10 enhances CCL2 release and chemotaxis induced by CCL16 in human monocytes. Int J Immunopathol Pharmacol. 2005;18(April–June (2)):339–349
  50. Loetscher P, Seitz M, Baggiolini M, Moser B. Interleukin-2 regulates CC chemokine receptor expression and chemotactic responsiveness in T lymphocytes. J Exp Med. 1996;184(August (2)):569–577
  51. Viola A, Contento RL, Molon B. T cells and their partners: the chemokine dating agency. Trends Immunol. 2006;27(September (9)):421–427
  52. Karpus WJ, Lukacs NW, Kennedy KJ, Smith WS, Hurst SD, Barrett TA. Differential CC chemokine-induced enhancement of T helper cell cytokine production. J Immunol. 1997;158(May (9)):4129–4136
  53. Rollins BJ, Pober JS. Interleukin-4 induces the synthesis and secretion of MCP-1/JE by human endothelial cells. Am J Pathol. 1991;138(June (6)):1315–1319
  54. Gu L, Rutledge B, Fiorillo J, Ernst C, Grewal I, Flavell R, et al. In vivo properties of monocyte chemoattractant protein-1. J Leukoc Biol. 1997;62(November (5)):577–580
  55. Nakamura K, Kitani A, Strober W. Cell contact-dependent immunosuppression by CD4(+)CD25(+) regulatory T cells is mediated by cell surface-bound transforming growth factor beta. J Exp Med. 2001;194(September (5)):629–644
  56. Asseman C, Mauze S, Leach MW, Coffman RL, Powrie F. An essential role for interleukin 10 in the function of regulatory T cells that inhibit intestinal inflammation. J Exp Med. 1999;190(October (7)):995–1004
  57. Cederbom L, Hall H, Ivars F. CD4+ CD25+ regulatory T cells down-regulate co-stimulatory molecules on antigen-presenting cells. Eur J Immunol. 2000;30(June (6)):1538–1543
  58. Ermann J, Szanya V, Ford GS, Paragas V, Fathman CG, Lejon K. CD4(+)CD25(+) T cells facilitate the induction of T cell anergy. J Immunol. 2001;167(October (8)):4271–4275
  59. Nagai H, Horikawa T, Hara I, Fukunaga A, Oniki S, Oka M, et al. In vivo elimination of CD25+ regulatory T cells leads to tumor rejection of B16F10 melanoma, when combined with interleukin-12 gene transfer. Exp Dermatol. 2004;13(October (10)):613–620
  60. Mahnke K, Schonfeld K, Fondel S, Ring S, Karakhanova S, Wiedemeyer K, et al. Depletion of CD4+CD25+ human regulatory T cells in vivo: kinetics of Treg depletion and alterations in immune functions in vivo and in vitro. Int J Cancer. 2007;120(June (12)):2723–2733
  61. Jordan JT, Sun W, Hussain SF, DeAngulo G, Prabhu SS, Heimberger AB. Preferential migration of regulatory T cells mediated by glioma-secreted chemokines can be blocked with chemotherapy. Cancer Immunol Immunother. 2008;57(January (1)):123–131
  62. Serafini P, Borrello I, Bronte V. Myeloid suppressor cells in cancer: recruitment, phenotype, properties, and mechanisms of immune suppression. Semin Cancer Biol. 2006;16(February (1)):53–65
  63. Filipazzi P, Valenti R, Huber V, Pilla L, Canese P, Iero M, et al. Identification of a new subset of myeloid suppressor cells in peripheral blood of melanoma patients with modulation by a granulocyte-macrophage colony-stimulation factor-based antitumor vaccine. J Clin Oncol. 2007;25(June (18)):2546–2553
  64. Liu C, Yu S, Kappes J, Wang J, Grizzle WE, Zinn KR, et al. Expansion of spleen myeloid suppressor cells represses NK cell cytotoxicity in tumor-bearing host. Blood. 2007;109(May (10)):4336–4342
  65. Kim JH, Dhanasekaran SM, Mehra R, Tomlins SA, Gu W, Yu J, et al. Integrative analysis of genomic aberrations associated with prostate cancer progression. Cancer Res. 2007;67(September (17)):8229–8239
  66. Bunt SK, Yang L, Sinha P, Clements VK, Leips J, Ostrand-Rosenberg S. Reduced inflammation in the tumor microenvironment delays the accumulation of myeloid-derived suppressor cells and limits tumor progression. Cancer Res. 2007;67(October (20)):10019–10026
  67. Rodriguez PC, Hernandez CP, Quiceno D, Dubinett SM, Zabaleta J, Ochoa JB, et al. Arginase I in myeloid suppressor cells is induced by COX-2 in lung carcinoma. J Exp Med. 2005;202(October (7)):931–939
  68. Huang B, Lei Z, Zhao J, Gong W, Liu J, Chen Z, et al. CCL2/CCR2 pathway mediates recruitment of myeloid suppressor cells to cancers. Cancer Lett. 2007;252(July (1)):86–92
  69. Herman JG, Stadelman HL, Roselli CE. Curcumin blocks CCL2-induced adhesion, motility and invasion, in part, through down-regulation of CCL2 expression and proteolytic activity. Int J Oncol. 2009;34(May (5)):1319–1327
  70. Valta MP, Tuomela J, Vuorikoski H, Loponen N, Vaananen RM, Pettersson K, et al. FGF-8b induces growth and rich vascularization in an orthotopic PC-3 model of prostate cancer. J Cell Biochem. 2009;(July (1)):769–784

PII: S1359-6101(09)00116-6

doi: 10.1016/j.cytogfr.2009.11.009

Cytokine & Growth Factor Reviews
Volume 21, Issue 1 , Pages 41-48 , February 2010