Endothelial CCR2 Signaling Induced by Colon Carcinoma Cells Enables Extravasation via the JAK2-Stat5 and p38MAPK Pathway

Cancer Cell

Volumn 22, Issue 1, 2012, Pages 91-105

  Wolf, Monika Julia ^a   Hoos, Alexandra ^c   Bauer, Judith ^d   Boettcher, Steffen ^b   Knust, Markus ^e   Weber, Achim ^b   Simonavicius, Nicole ^d   Schneider, Christoph ^f   Lang, Matthias ^e   Stürzl, Michael ^g   Croner, Roland S ^g   Konrad, Andreas ^g   Manz, Markus G ^b   Moch, Holger ^b   Aguzzi, Adriano ^a   van Loo, Geert ^h   Pasparakis, Manolis ⁱ   Prinz, Marco ^e   Borsig, Lubor ^c   Heikenwalder, Mathias ^a,d  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^b UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^c UNIVERSITY OF ZURICH   (Switzerland)

^d TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^e UNIVERSITY OF FREIBURG   (Germany)

^f ETH ZURICH   (Switzerland)

^g UNIVERSITY HOSPITAL ERLANGEN   (Germany)

^h DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

ⁱ UNIVERSITY OF COLOGNE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR2; CXCL1 CHEMOKINE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; JANUS KINASE 2; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE P38; MONOCYTE CHEMOTACTIC PROTEIN 1; MONOCYTE CHEMOTACTIC PROTEIN 3; STAT3 PROTEIN; STAT5 PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL PERMEABILITY; BONE MARROW CELL; CELL MIGRATION; COLON CARCINOMA; CONTROLLED STUDY; EXTRAVASATION; IN VITRO STUDY; IN VIVO STUDY; LUNG METASTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; UPREGULATION;

MUS;

EID: 84863756518     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccr.2012.05.023     Document Type: Article

References (40)

1. Agrawal S., Gollapudi S., Su H., Gupta S. Leptin activates human B cells to secrete TNF-α, IL-6, and IL-10 via JAK2/STAT3 and p38MAPK/ERK1/2 signaling pathway. J. Clin. Immunol. 2011, 31:472-478.
2. Allavena P., Germano G., Marchesi F., Mantovani A. Chemokines in cancer related inflammation. Exp. Cell Res. 2011, 317:664-673.
3. Boring L., Gosling J., Chensue S.W., Kunkel S.L., Farese R.V., Broxmeyer H.E., Charo I.F. Impaired monocyte migration and reduced type 1 (Th1) cytokine responses in C-C chemokine receptor 2 knockout mice. J. Clin. Invest. 1997, 100:2552-2561.
4. Borsig L., Wong R., Hynes R.O., Varki N.M., Varki A. Synergistic effects of L- and P-selectin in facilitating tumor metastasis can involve non-mucin ligands and implicate leukocytes as enhancers of metastasis. Proc. Natl. Acad. Sci. USA 2002, 99:2193-2198.
5. Chambers A.F., Groom A.C., MacDonald I.C. Dissemination and growth of cancer cells in metastatic sites. Nat. Rev. Cancer 2002, 2:563-572.
6. Clausen B.E., Burkhardt C., Reith W., Renkawitz R., Förster I. Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res. 1999, 8:265-277.
7. Feng D., Nagy J.A., Pyne K., Dvorak H.F., Dvorak A.M. Neutrophils emigrate from venules by a transendothelial cell pathway in response to FMLP. J. Exp. Med. 1998, 187:903-915.
8. Granot Z., Henke E., Comen E.A., King T.A., Norton L., Benezra R. Tumor entrained neutrophils inhibit seeding in the premetastatic lung. Cancer Cell 2011, 20:300-314.
9. Gupta G.P., Massagué J. Cancer metastasis: building a framework. Cell 2006, 127:679-695.
10. Hiratsuka S., Watanabe A., Aburatani H., Maru Y. Tumour-mediated upregulation of chemoattractants and recruitment of myeloid cells predetermines lung metastasis. Nat. Cell Biol. 2006, 8:1369-1375.
11. Hohl T.M., Rivera A., Lipuma L., Gallegos A., Shi C., Mack M., Pamer E.G. Inflammatory monocytes facilitate adaptive CD4 T cell responses during respiratory fungal infection. Cell Host Microbe 2009, 6:470-481.
12. Joyce J.A., Pollard J.W. Microenvironmental regulation of metastasis. Nat. Rev. Cancer 2009, 9:239-252.
13. Kim S., Takahashi H., Lin W.W., Descargues P., Grivennikov S., Kim Y., Luo J.L., Karin M. Carcinoma-produced factors activate myeloid cells through TLR2 to stimulate metastasis. Nature 2009, 457:102-106.
14. Kuziel W.A., Morgan S.J., Dawson T.C., Griffin S., Smithies O., Ley K., Maeda N. Severe reduction in leukocyte adhesion and monocyte extravasation in mice deficient in CC chemokine receptor 2. Proc. Natl. Acad. Sci. USA 1997, 94:12053-12058.
15. Läubli H., Borsig L. Selectins promote tumor metastasis. Semin. Cancer Biol. 2010, 20:169-177.
16. Läubli H., Stevenson J.L., Varki A., Varki N.M., Borsig L. L-selectin facilitation of metastasis involves temporal induction of Fut7-dependent ligands at sites of tumor cell arrest. Cancer Res. 2006, 66:1536-1542.
17. Läubli H., Spanaus K.S., Borsig L. Selectin-mediated activation of endothelial cells induces expression of CCL5 and promotes metastasis through recruitment of monocytes. Blood 2009, 114:4583-4591.
18. Leuschner F., Dutta P., Gorbatov R., Novobrantseva T.I., Donahoe J.S., Courties G., Lee K.M., Kim J.I., Markmann J.F., Marinelli B., et al. Therapeutic siRNA silencing in inflammatory monocytes in mice. Nat. Biotechnol. 2011, 29:1005-1010.
19. Loberg R.D., Ying C., Craig M., Day L.L., Sargent E., Neeley C., Wojno K., Snyder L.A., Yan L., Pienta K.J. Targeting CCL2 with systemic delivery of neutralizing antibodies induces prostate cancer tumor regression in vivo. Cancer Res. 2007, 67:9417-9424.
20. Lu X., Kang Y. Chemokine (C-C motif) ligand 2 engages CCR2+ stromal cells of monocytic origin to promote breast cancer metastasis to lung and bone. J. Biol. Chem. 2009, 284:29087-29096.
21. Mantovani A., Sica A. Macrophages, innate immunity and cancer: balance, tolerance, and diversity. Curr. Opin. Immunol. 2010, 22:231-237.
22. McIntyre T.M., Prescott S.M., Weyrich A.S., Zimmerman G.A. Cell-cell interactions: leukocyte-endothelial interactions. Curr. Opin. Hematol. 2003, 10:150-158.
23. Mellado M., Rodríguez-Frade J.M., Aragay A., del Real G., Martín A.M., Vila-Coro A.J., Serrano A., Mayor F., Martínez-A C. The chemokine monocyte chemotactic protein 1 triggers Janus kinase 2 activation and tyrosine phosphorylation of the CCR2B receptor. J. Immunol. 1998, 161:805-813.
24. Mildner A., Mack M., Schmidt H., Brück W., Djukic M., Zabel M.D., Hille A., Priller J., Prinz M. CCR2+Ly-6Chi monocytes are crucial for the effector phase of autoimmunity in the central nervous system. Brain 2009, 132:2487-2500.
25. Mishra P., Banerjee D., Ben-Baruch A. Chemokines at the crossroads of tumor-fibroblast interactions that promote malignancy. J. Leukoc. Biol. 2011, 89:31-39.
26. Mizutani K., Sud S., McGregor N.A., Martinovski G., Rice B.T., Craig M.J., Varsos Z.S., Roca H., Pienta K.J. The chemokine CCL2 increases prostate tumor growth and bone metastasis through macrophage and osteoclast recruitment. Neoplasia 2009, 11:1235-1242.
27. O'Hayre M., Salanga C.L., Handel T.M., Allen S.J. Chemokines and cancer: migration, intracellular signalling and intercellular communication in the microenvironment. Biochem. J. 2008, 409:635-649.
28. Peinado H., Lavotshkin S., Lyden D. The secreted factors responsible for pre-metastatic niche formation: old sayings and new thoughts. Semin. Cancer Biol. 2011, 21:139-146.
29. Qian B.Z., Pollard J.W. Macrophage diversity enhances tumor progression and metastasis. Cell 2010, 141:39-51.
30. Qian B.Z., Li J., Zhang H., Kitamura T., Zhang J., Campion L.R., Kaiser E.A., Snyder L.A., Pollard J.W. CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature 2011, 475:222-225.
31. Reutershan J., Morris M.A., Burcin T.L., Smith D.F., Chang D., Saprito M.S., Ley K. Critical role of endothelial CXCR2 in LPS-induced neutrophil migration into the lung. J. Clin. Invest. 2006, 116:695-702.
32. Salcedo R., Ponce M.L., Young H.A., Wasserman K., Ward J.M., Kleinman H.K., Oppenheim J.J., Murphy W.J. Human endothelial cells express CCR2 and respond to MCP-1: direct role of MCP-1 in angiogenesis and tumor progression. Blood 2000, 96:34-40.
33. Sanz-Moreno V., Gaggioli C., Yeo M., Albrengues J., Wallberg F., Viros A., Hooper S., Mitter R., Féral C.C., Cook M., et al. ROCK and JAK1 signaling cooperate to control actomyosin contractility in tumor cells and stroma. Cancer Cell 2011, 20:229-245.
34. Sawanobori Y., Ueha S., Kurachi M., Shimaoka T., Talmadge J.E., Abe J., Shono Y., Kitabatake M., Kakimi K., Mukaida N., Matsushima K. Chemokine-mediated rapid turnover of myeloid-derived suppressor cells in tumor-bearing mice. Blood 2008, 111:5457-5466.
35. Soria G., Ofri-Shahak M., Haas I., Yaal-Hahoshen N., Leider-Trejo L., Leibovich-Rivkin T., Weitzenfeld P., Meshel T., Shabtai E., Gutman M., Ben-Baruch A. Inflammatory mediators in breast cancer: coordinated expression of TNFα & IL-1β with CCL2 & CCL5 and effects on epithelial-to-mesenchymal transition. BMC Cancer 2011, 11:130.
36. Tremblay P.L., Auger F.A., Huot J. Regulation of transendothelial migration of colon cancer cells by E-selectin-mediated activation of p38 and ERK MAP kinases. Oncogene 2006, 25:6563-6573.
37. Yoshidome H., Kohno H., Shida T., Kimura F., Shimizu H., Ohtsuka M., Nakatani Y., Miyazaki M. Significance of monocyte chemoattractant protein-1 in angiogenesis and survival in colorectal liver metastases. Int. J. Oncol. 2009, 34:923-930.
38. Yu H., Pardoll D., Jove R. STATs in cancer inflammation and immunity: a leading role for STAT3. Nat. Rev. Cancer 2009, 9:798-809.
39. Zhang J., Patel L., Pienta K.J. CC chemokine ligand 2 (CCL2) promotes prostate cancer tumorigenesis and metastasis. Cytokine Growth Factor Rev. 2010, 21:41-48.
40. Zijlmans H.J., Fleuren G.J., Baelde H.J., Eilers P.H., Kenter G.G., Gorter A. The absence of CCL2 expression in cervical carcinoma is associated with increased survival and loss of heterozygosity at 17q11.2. J. Pathol. 2006, 208:507-517.