Increased expression of chemerin in squamous esophageal cancer myofibroblasts and role in recruitment of mesenchymal stromal cells

PLoS ONE

Volumn 9, Issue 8, 2014, Pages

  Kumar, J Dinesh ^a   Holmberg, Chris ^a   Kandola, Sandhir ^a   Steele, Islay ^a   Hegyi, Peter ^b   Tiszlavicz, Laszlo ^b   Jenkins, Rosalind ^a   Beynon, Robert J ^a   Peeney, David ^a   Giger, Olivier T ^a   Alqahtani, Ahlam ^a   Wang, Timothy C ^d   Charvat, Trevor T ^c   Penfold, Mark ^c   Dockray, Graham J ^a   Varro, Andrea ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b UNIVERSITY OF SZEGED   (Hungary)

^c Department of Pharmacology Institute of Translational Medicine University of Liverpool ^*  (United States)

^d NewYork Presbyterian Hospital   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 2 MORPHOLINO 8 PHENYLCHROMONE; 3 [8 [(DIMETHYLAMINO)METHYL] 6,7,8,9 TETRAHYDROPYRIDO[1,2 A]INDOL 10 YL] 4 (1 METHYL 1H INDOL 3 YL) 1H PYRROLE 2,5 DIONE; 4 (4 FLUOROPHENYL) 2 (4 HYDROXYPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; CCX 826; CCX 832; CCX 836; CHEMERIN; CHEMERIN RECEPTOR 23; GELATINASE A; JANUS KINASE 2; LY 291002; MACROPHAGE MIGRATION INHIBITION FACTOR; MITOGEN ACTIVATED PROTEIN KINASE 1; NEUTRALIZING ANTIBODY; PHORBOL 13 ACETATE 12 MYRISTATE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; CHEMERIN PROTEIN, HUMAN; CHEMOKINE; CHEMOKINE RECEPTOR; CMKLR1 PROTEIN, HUMAN; ISOMERASE; MIF PROTEIN, HUMAN; MITOGEN ACTIVATED PROTEIN KINASE; MMP2 PROTEIN, HUMAN; PROTEIN KINASE C; SIGNAL PEPTIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL; CARCINOGENESIS; CELL HOMING; CELL MIGRATION; CELLULAR SECRETION; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME PHOSPHORYLATION; ESOPHAGEAL SQUAMOUS CELL CARCINOMA; HUMAN; HUMAN CELL; HUMAN TISSUE; MESENCHYMAL STROMA CELL; MYOFIBROBLAST; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; XENOGRAFT; ANIMAL; BAGG ALBINO MOUSE; CANCER TRANSPLANTATION; CHEMOTAXIS; ESOPHAGUS TUMOR; METABOLISM; NUDE MOUSE; PATHOLOGY; PHYSIOLOGY; SECRETION (PROCESS); TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; CHEMOKINES; CHEMOTAXIS; ESOPHAGEAL NEOPLASMS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; INTRAMOLECULAR OXIDOREDUCTASES; MACROPHAGE MIGRATION-INHIBITORY FACTORS; MATRIX METALLOPROTEINASE 2; MESENCHYMAL STROMAL CELLS; MICE, INBRED BALB C; MICE, NUDE; MITOGEN-ACTIVATED PROTEIN KINASES; MYOFIBROBLASTS; NEOPLASM TRANSPLANTATION; PROTEIN KINASE C; RECEPTORS, CHEMOKINE; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION;

EID: 84940246040     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0104877     Document Type: Article

References (50)

1. Quail DF, Joyce JA (2013) Microenvironmental regulation of tumor progression and metastasis. Nat Med 19: 1423-1437.
2. De Wever O, Demetter P, Mareel M, Bracke M (2008) Stromal myofibroblasts are drivers of invasive cancer growth. IntJCancer 123: 2229-2238.
3. Holmberg C, Quante M, Steele I, Kumar J, Balabanova S, et al. (2012) Release of TGFbetaig-h3 by gastric myofibroblasts slows tumor growth and is decreased with cancer progression. Carcinogenesis 33: 1553-1562.
4. Orimo A, Gupta PB, Sgroi DC, renzana-Seisdedos F, Delaunay T, et al. (2005) Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion. Cell 121: 335-348. (Pubitemid 40692295)
5. Jiang L, Gonda TA, Gamble MV, Salas M, Seshan V, et al. (2008) Global hypomethylation of genomic DNA in cancer-associated myofibroblasts. Cancer Res 68: 9900-9908.
6. Quante M, Tu SP, Tomita H, Gonda T, Wang SS, et al. (2011) Bone marrow-derived myofibroblasts contribute to the mesenchymal stem cell niche and promote tumor growth. Cancer Cell 19: 257-272.
7. Quante M, Wang TC (2009) Stem cells in gastroenterology and hepatology. Nat Rev Gastroenterol Hepatol 6: 724-737.
8. Studeny M, Marini FC, Dembinski JL, Zompetta C, Cabreira-Hansen M, et al. (2004) Mesenchymal stem cells: potential precursors for tumor stroma and targeted-delivery vehicles for anticancer agents. J Natl Cancer Inst 96: 1593-1603. (Pubitemid 39534883)
9. Honczarenko M, Le Y, Swierkowski M, Ghiran I, Glodek AM, et al. (2006) Human bone marrow stromal cells express a distinct set of biologically functional chemokine receptors. Stem Cells 24: 1030-1041. (Pubitemid 44464736)
10. Sordi V, Malosio ML, Marchesi F, Mercalli A, Melzi R, et al. (2005) Bone marrow mesenchymal stem cells express a restricted set of functionally active chemokine receptors capable of promoting migration to pancreatic islets. Blood 106: 419-427. (Pubitemid 40981232)
11. Jemal A, Bray F, Center MM, Ferlay J, Ward E, et al. (2011) Global cancer statistics. CA Cancer J Clin 61: 69-90.
12. Noma K, Smalley KS, Lioni M, Naomoto Y, Tanaka N, et al. (2008) The essential role of fibroblasts in esophageal squamous cell carcinoma-induced angiogenesis. Gastroenterology 134: 1981-1993. (Pubitemid 351790740)
13. Grugan KD, Miller CG, Yao Y, Michaylira CZ, Ohashi S, et al. (2010) Fibroblast-secreted hepatocyte growth factor plays a functional role in esophageal squamous cell carcinoma invasion. Proc Natl Acad Sci U S A 107: 11026-11031.
14. Wittamer V, Franssen JD, Vulcano M, Mirjolet JF, Le Poul E, et al. (2003) Specific recruitment of antigen-presenting cells by chemerin, a novel processed ligand from human inflammatory fluids. J Exp Med 198: 977-985. (Pubitemid 37248614)
15. Meder W, Wendland M, Busmann A, Kutzleb C, Spodsberg N, et al. (2003) Characterization of human circulating TIG2 as a ligand for the orphan receptor ChemR23. FEBS Lett 555: 495-499. (Pubitemid 37532599)
16. Zabel BA, Allen SJ, Kulig P, Allen JA, Cichy J, et al. (2005) Chemerin activation by serine proteases of the coagulation, fibrinolytic, and inflammatory cascades. J Biol Chem 280: 34661-34666. (Pubitemid 41504597)
17. Goralski KB, McCarthy TC, Hanniman EA, Zabel BA, Butcher EC, et al. (2007) Chemerin, a novel adipokine that regulates adipogenesis and adipocyte metabolism. J Biol Chem 282: 28175-28188. (Pubitemid 47529521)
18. Pachynski RK, Zabel BA, Kohrt HE, Tejeda NM, Monnier J, et al. (2012) The chemoattractant chemerin suppresses melanoma by recruiting natural killer cell antitumor defenses. J Exp Med 209: 1427-1435.
19. Parolini S, Santoro A, Marcenaro E, Luini W, Massardi L, et al. (2007) The role of chemerin in the colocalization of NK and dendritic cell subsets into inflamed tissues. Blood 109: 3625-3632. (Pubitemid 46641708)
20. McCaig C, Duval C, Hemers E, Steele I, Pritchard DM, et al. (2006) The role of matrix metalloproteinase-7 in redefining the gastric microenvironment in response to Helicobacter pylori. Gastroenterology 130: 1754-1763. (Pubitemid 43668841)
21. Wu KC, Jackson LM, Galvin AM, Gray T, Hawkey CJ, et al. (1999) Phenotypic and functional characterisation of myofibroblasts, macrophages, and lymphocytes migrating out of the human gastric lamina propria following the loss of epithelial cells. Gut 44: 323-330. (Pubitemid 29119325)
22. Wroblewski LE, Noble PJ, Pagliocca A, Pritchard DM, Hart CA, et al. (2003) Stimulation of MMP-7 (matrilysin) by Helicobacter pylori in human gastric epithelial cells: role in epithelial cell migration. J Cell Sci 116: 3017-3026. (Pubitemid 36926990)
23. Holmberg C, Ghesquiere B, Impens F, Gevaert K, Kumar JD, et al. (2013) Mapping proteolytic processing in the secretome of gastric cancer-associated myofibroblasts reveals activation of MMP-1, MMP-2, and MMP-3. J Proteome Res 12: 3413-3422.
24. Hemers E, Duval C, McCaig C, Handley M, Dockray GJ, et al. (2005) Insulin-like growth factor binding protein-5 is a target of matrix metalloproteinase-7: implications for epithelial-mesenchymal signaling. Cancer Res 65: 7363-7369. (Pubitemid 41161269)
25. Varro A, Noble PJ, Pritchard DM, Kennedy S, Hart CA, et al. (2004) Helicobacter pylori induces plasminogen activator inhibitor 2 (PAI-2) in gastric epithelial cells through NF-kB and RhoA: implications for invasion and apoptosis Cancer Res 64: 1695-1702. (Pubitemid 38428691)
26. Watts SW, Dorrance AM, Penfold ME, Rourke JL, Sinal CJ, et al. (2013) Chemerin connects fat to arterial contraction. Arterioscler Thromb Vasc Biol 33: 1320-1328.
27. Noble PJ, Wilde G, White MR, Pennington SR, Dockray GJ, et al. (2003) Stimulation of gastrin-CCKB receptor promotes migration of gastric AGS cells via multiple paracrine pathways. AmJPhysiol 284: G75-G84. (Pubitemid 36076252)
28. Satija NK, Sharma D, Afrin F, Tripathi RP, Gangenahalli G (2013) High throughput transcriptome profiling of lithium stimulated human mesenchymal stem cells reveals priming towards osteoblastic lineage. PLoS One 8: e55769.
29. Barnea G, Strapps W, Herrada G, Berman Y, Ong J, et al. (2008) The genetic design of signaling cascades to record receptor activation. Proc Natl Acad Sci U S A 105: 64-69.
30. Houghton J, Stoicov C, Nomura S, Rogers AB, Carlson J, et al. (2004) Gastric cancer originating from bone marrow-derived cells. Science 306: 1568-1571. (Pubitemid 39564955)
31. Bhowmick NA, Neilson EG, Moses HL (2004) Stromal fibroblasts in cancer initiation and progression. Nature 432: 332-337. (Pubitemid 39551661)
32. Bremnes RM, Donnem T, Al-Saad S, Al-Shibli K, Andersen S, et al. (2011) The role of tumor stroma in cancer progression and prognosis: emphasis on carcinoma-associated fibroblasts and non-small cell lung cancer. J Thorac Oncol 6: 209-217.
33. Farmer P, Bonnefoi H, Anderle P, Cameron D, Wirapati P, et al. (2009) A stroma-related gene signature predicts resistance to neoadjuvant chemotherapy in breast cancer. NatMed 15: 68-74.
34. Kalluri R, Zeisberg M (2006) Fibroblasts in cancer. NatRevCancer 6: 392-401.
35. Olumi AF, Grossfeld GD, Hayward SW, Carroll PR, Tlsty TD, et al. (1999) Carcinoma-associated fibroblasts direct tumor progression of initiated human prostatic epithelium. Cancer Res 59: 5002-5011. (Pubitemid 29472907)
36. Skalnikova H, Motlik J, Gadher SJ, Kovarova H (2011) Mapping of the secretome of primary isolates of mammalian cells, stem cells and derived cell lines. Proteomics 11: 691-708.
37. De Boeck A, Hendrix A, Maynard D, Van Bockstal M, Daniels A, et al. (2013) Differential secretome analysis of cancer-associated fibroblasts and bone marrow-derived precursors to identify microenvironmental regulators of colon cancer progression. Proteomics 13: 379-388.
38. Zheng Y, Luo S, Wang G, Peng Z, Zeng W, et al. (2008) Downregulation of tazarotene induced gene-2 (TIG2) in skin squamous cell carcinoma. Eur - J Dermatol 18: 638-641.
39. Lin W, Chen YL, Jiang L, Chen JK (2011) Reduced expression of chemerin is associated with a poor prognosis and a lowed infiltration of both dendritic cells and natural killer cells in human hepatocellular carcinoma. Clin Lab 57: 879-885.
40. Somja J, Demoulin S, Roncarati P, Herfs M, Bletard N, et al. (2013) Dendritic cells in Barrett's esophagus carcinogenesis: an inadequate microenvironment for antitumor immunity? Am J Pathol 182: 2168-2179.
41. Wang C, Wu WK, Liu X, To KF, Chen GG, et al. (2014) Increased serum chemerin level promotes cellular invasiveness in gastric cancer: a clinical and experimental study. Peptides 51: 131-138.
42. Ho IA, Lam PY (2013) Signaling molecules and pathways involved in MSC tumor tropism. Histol Histopathol 28: 1427-1438.
43. Smith H, Whittall C, Weksler B, Middleton J (2012) Chemokines stimulate bidirectional migration of human mesenchymal stem cells across bone marrow endothelial cells. Stem Cells Dev 21: 476-486.
44. Teo GS, Ankrum JA, Martinelli R, Boetto SE, Simms K, et al. (2012) Mesenchymal stem cells transmigrate between and directly through tumor necrosis factor-alpha-activated endothelial cells via both leukocyte-like and novel mechanisms. Stem Cells 30: 2472-2486.
45. Lozito TP, Tuan RS (2011) Mesenchymal stem cells inhibit both endogenous and exogenous MMPs via secreted TIMPs. J Cell Physiol 226: 385-396.
46. Chamberlain G, Smith H, Rainger GE, Middleton J (2011) Mesenchymal stem cells exhibit firm adhesion, crawling, spreading and transmigration across aortic endothelial cells: effects of chemokines and shear. PLoS One 6: e25663.
47. De Becker A, Van Hummelen P, Bakkus M, Vande Broek I, De Wever J, et al. (2007) Migration of culture-expanded human mesenchymal stem cells through bone marrow endothelium is regulated by matrix metalloproteinase-2 and tissue inhibitor of metalloproteinase-3. Haematologica 92: 440-449. (Pubitemid 350144289)
48. Ozaki Y, Nishimura M, Sekiya K, Suehiro F, Kanawa M, et al. (2007) Comprehensive analysis of chemotactic factors for bone marrow mesenchymal stem cells. Stem Cells Dev 16: 119-129. (Pubitemid 46362597)
49. Fischer-Valuck BW, Barrilleaux BL, Phinney DG, Russell KC, Prockop DJ, et al. (2010) Migratory response of mesenchymal stem cells to macrophage migration inhibitory factor and its antagonist as a function of colony-forming efficiency. Biotechnol Lett 32: 19-27.
50. Muruganandan S, Parlee SD, Rourke JL, Ernst MC, Goralski KB, et al. (2011) Chemerin, a novel peroxisome proliferator-activated receptor gamma (PPAR-gamma) target gene that promotes mesenchymal stem cell adipogenesis. J Biol Chem 286: 23982-23995.