CCL24 contributes to HCC malignancy via RhoB- VEGFA-VEGFR2 angiogenesis pathway and indicates poor prognosis

Oncotarget

Volumn 8, Issue 3, 2017, Pages 5135-5148

  Jin, Lei ^a   Liu, Wei Ren ^a   Tian, Meng Xin ^a   Jiang, Xi Fei ^a   Wang, Han ^a   Zhou, Pei Yun ^a   Ding, Zhen Bin ^a   Peng, Yuan Fei ^a   Dai, Zhi ^a   Qiu, Shuang Jian ^a   Zhou, Jian ^a   Fan, Jia ^a   Shi, Ying Hong ^a  

^a FUDAN UNIVERSITY   (China)

Author keywords

CCL24; HCC; Prognosis; RhoB; VEGFA

Indexed keywords

CHEMOKINE RECEPTOR CCR3; EOTAXIN 2; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; SMALL INTERFERING RNA; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 2; CCL24 PROTEIN, HUMAN; CCR3 PROTEIN, HUMAN; FGFR2 PROTEIN, HUMAN; FIBROBLAST GROWTH FACTOR RECEPTOR 2; RHOB GUANINE NUCLEOTIDE BINDING PROTEIN; VEGFA PROTEIN, HUMAN;

ADULT; AGE RELATED MACULAR DEGENERATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER PROGNOSIS; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; COHORT ANALYSIS; CONTROLLED STUDY; ENZYME MECHANISM; FEMALE; FOLLOW UP; HEPATOCELLULAR CARCINOMA CELL LINE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; LIVER CARCINOGENESIS; LIVER CELL CARCINOMA; LIVER METASTASIS; LUNG METASTASIS; MAJOR CLINICAL STUDY; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; RETINA NEOVASCULARIZATION; RETROSPECTIVE STUDY; SIGNAL TRANSDUCTION; TH2 CELL; TISSUE MICROARRAY; TUMOR VASCULARIZATION; UMBILICAL VEIN ENDOTHELIAL CELL; VALIDATION PROCESS; WESTERN BLOTTING; ANIMAL; CANCER TRANSPLANTATION; GENE EXPRESSION REGULATION; GENETICS; LIVER TUMOR; METABOLISM; PATHOLOGY; PROGNOSIS; SURVIVAL ANALYSIS; TUMOR CELL LINE; UPREGULATION;

ANIMALS; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; CHEMOKINE CCL24; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; LIVER NEOPLASMS; MALE; MICE; NEOPLASM TRANSPLANTATION; PROGNOSIS; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 2; RECEPTORS, CCR3; RHOB GTP-BINDING PROTEIN; SURVIVAL ANALYSIS; TH2 CELLS; UP-REGULATION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 85012022690     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.14095     Document Type: Article

References (39)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011; 61: 69-90. doi: 10.3322/caac.20107.
2. Liu WR, Tian MX, Jin L, Yang LX, Ding ZB, Shen YH, Peng YF, Zhou J, Qiu SJ, Dai Z, Fan J, Shi YH. High levels of hepatitis B surface antigen are associated with poorer survival and early recurrence of hepatocellular carcinoma in patients with low hepatitis B viral loads. Ann Surg Oncol. 2015; 22: 843-50. doi: 10.1245/s10434-014-4043-5.
3. Wang F, Yang JL, Yu KK, Xu M, Xu YZ, Chen L, Lu YM, Fang HS, Wang XY, Hu ZQ, Li FF, Kan L, Luo J, et al. Activation of the NF-kappaB pathway as a mechanism of alcohol enhanced progression and metastasis of human hepatocellular carcinoma. Mol Cancer. 2015; 14: 10. doi: 10.1186/s12943-014-0274-0.
4. Yu J, Shen J, Sun TT, Zhang X, Wong N. Obesity, insulin resistance, NASH and hepatocellular carcinoma. Semin Cancer Biol. 2013; 23: 483-91. doi: 10.1016/j. semcancer.2013.07.003.
5. Chen J, Jin R, Zhao J, Liu J, Ying H, Yan H, Zhou S, Liang Y, Huang D, Liang X, Yu H, Lin H, Cai X. Potential molecular, cellular and microenvironmental mechanism of sorafenib resistance in hepatocellular carcinoma. Cancer Lett. 2015; 367: 1-11. doi: 10.1016/j.canlet.2015.06.019.
6. Simioni C, Cani A, Martelli AM, Zauli G, Alameen AA, Ultimo S, Tabellini G, McCubrey JA, Capitani S, Neri LM. The novel dual PI3K/mTOR inhibitor NVP-BGT226 displays cytotoxic activity in both normoxic and hypoxic hepatocarcinoma cells. Oncotarget. 2015; 6: 17147-60. doi: 10.18632/oncotarget.3940.
7. Mlecnik B, Tosolini M, Charoentong P, Kirilovsky A, Bindea G, Berger A, Camus M, Gillard M, Bruneval P, Fridman WH, Pages F, Trajanoski Z, Galon J. Biomolecular network reconstruction identifies T-cell homing factors associated with survival in colorectal cancer. Gastroenterology. 2010; 138: 1429-40. doi: 10.1053/j. gastro.2009.10.057.
8. Kryczek I, Lin Y, Nagarsheth N, Peng D, Zhao L, Zhao E, Vatan L, Szeliga W, Dou Y, Owens S, Zgodzinski W, Majewski M, Wallner G, et al. IL-22(+)CD4(+) T cells promote colorectal cancer stemness via STAT3 transcription factor activation and induction of the methyltransferase DOT1L. Immunity. 2014; 40: 772-84. doi: 10.1016/j. immuni.2014.03.010.
9. Patel VP, Kreider BL, Li Y, Li H, Leung K, Salcedo T, Nardelli B, Pippalla V, Gentz S, Thotakura R, Parmelee D, Gentz R, Garotta G. Molecular and functional characterization of two novel human C-C chemokines as inhibitors of two distinct classes of myeloid progenitors. J Exp Med. 1997; 185: 1163-72.
10. Neilsen CV, Bryce PJ. Interleukin-13 directly promotes oesophagus production of CCL11 and CCL24 and the migration of eosinophils. Clin Exp Allergy. 2010; 40: 427-34 doi: 10.1111/j.1365-2222.2009.03419.x.
11. Radinger M, Johansson AK, Sitkauskiene B, Sjostrand M, Lotvall J. Eotaxin-2 regulates newly produced and CD34 airway eosinophils after allergen exposure. J Allergy Clin Immunol. 2004; 113: 1109-16. doi: 10.1016/j. jaci.2004.03.022.
12. Ying S, Meng Q, Zeibecoglou K, Robinson DS, Macfarlane A, Humbert M, Kay AB. Eosinophil chemotactic chemokines (eotaxin, eotaxin-2, RANTES, monocyte chemoattractant protein-3 (MCP-3), and MCP-4), and C-C chemokine receptor 3 expression in bronchial biopsies from atopic and nonatopic (Intrinsic) asthmatics. J Immunol. 1999; 163: 6321-9.
13. Burke-Gaffney A, Hellewell PG. Eotaxin stimulates eosinophil adhesion to human lung microvascular endothelial cells. Biochem Biophys Res Commun. 1996; 227: 35-40. doi: 10.1006/bbrc.1996.1463.
14. Cheadle EJ, Riyad K, Subar D, Rothwell DG, Ashton G, Batha H, Sherlock DJ, Hawkins RE, Gilham DE. Eotaxin-2 and colorectal cancer: a potential target for immune therapy. Clin Cancer Res. 2007; 13: 5719-28. doi: 10.1158/1078-0432.CCR-07-1145.
15. Cho H, Lim SJ, Won KY, Bae GE, Kim GY, Min JW, Noh BJ. Eosinophils in Colorectal Neoplasms Associated with Expression of CCL-11 and CCL-24. J Pathol Transl Med. 2015 doi: 10.4132/jptm.2015.10.16.
16. Miyagaki T, Sugaya M, Murakami T, Asano Y, Tada Y, Kadono T, Okochi H, Tamaki K, Sato S. CCL11-CCR3 interactions promote survival of anaplastic large cell lymphoma cells via ERK1/2 activation. Cancer Res. 2011; 71: 2056-65. doi: 10.1158/0008-5472.CAN-10-3764.
17. Kleinhans M, Tun-Kyi A, Gilliet M, Kadin ME, Dummer R, Burg G, Nestle FO. Functional expression of the eotaxin receptor CCR3 in CD30+ cutaneous T-cell lymphoma. Blood. 2003; 101: 1487-93. doi: 10.1182/blood-2002-02-0475.
18. Takeda A, Baffi JZ, Kleinman ME, Cho WG, Nozaki M, Yamada K, Kaneko H, Albuquerque RJ, Dridi S, Saito K, Raisler BJ, Budd SJ, Geisen P, et al. CCR3 is a target for age-related macular degeneration diagnosis and therapy. Nature. 2009; 460: 225-30. doi: 10.1038/nature08151.
19. Hoeben A, Landuyt B, Highley MS, Wildiers H, Van Oosterom AT, De Bruijn EA. Vascular endothelial growth factor and angiogenesis. Pharmacol Rev. 2004; 56: 549-80. doi: 10.1124/pr.56.4.3.
20. Larche M. Immunoregulation by targeting T cells in the treatment of allergy and asthma. Curr Opin Immunol. 2006; 18: 745-50. doi: 10.1016/j.coi.2006.09.013.
21. Fan J, Malik AB. Toll-like receptor-4 (TLR4) signaling augments chemokine-induced neutrophil migration by modulating cell surface expression of chemokine receptors. Nat Med. 2003; 9: 315-21. doi: 10.1038/nm832.
22. Gong JH, Shin D, Han SY, Kim JL, Kang YH. Kaempferol suppresses eosionphil infiltration and airway inflammation in airway epithelial cells and in mice with allergic asthma. J Nutr. 2012; 142: 47-56. doi: 10.3945/jn.111.150748.
23. Grise F, Bidaud A, Moreau V. Rho GTPases in hepatocellular carcinoma. Biochim Biophys Acta. 2009; 1795: 137-51. doi: 10.1016/j.bbcan.2008.12.003.
24. Benvenuti F, Hugues S, Walmsley M, Ruf S, Fetler L, Popoff M, Tybulewicz VL, Amigorena S. Requirement of Rac1 and Rac2 expression by mature dendritic cells for T cell priming. Science. 2004; 305: 1150-3. doi: 10.1126/science.1099159.
25. Yang JQ, Kalim KW, Li Y, Zhang S, Hinge A, Filippi MD, Zheng Y, Guo F. RhoA orchestrates glycolysis for TH2 cell differentiation and allergic airway inflammation. J Allergy Clin Immunol. 2016; 137: 231-45 e4. doi: 10.1016/j. jaci.2015.05.004.
26. Tian M, Li Y, Liu W, Jin L, Jiang X, Wang X, Ding Z, Peng Y, Zhou J, Fan J, Cao Y, Wang W, Shi Y. The nanomechanical signature of liver cancer tissues and its molecular origin. Nanoscale. 2015; 7: 12998-3010. doi: 10.1039/c5nr02192h.
27. Bais C, Van Geelen A, Eroles P, Mutlu A, Chiozzini C, Dias S, Silverstein RL, Rafii S, Mesri EA. Kaposi's sarcoma associated herpesvirus G protein-coupled receptor immortalizes human endothelial cells by activation of the VEGF receptor-2/KDR. Cancer Cell. 2003; 3: 131-43.
28. Lin L, Chen YS, Yao YD, Chen JQ, Chen JN, Huang SY, Zeng YJ, Yao HR, Zeng SH, Fu YS, Song EW. CCL18 from tumor-associated macrophages promotes angiogenesis in breast cancer. Oncotarget. 2015; 6: 34758-73. doi: 10.18632/oncotarget.5325.
29. Bao L, Shi VY, Chan LS. IL-4 up-regulates epidermal chemotactic, angiogenic, and pro-inflammatory genes and down-regulates antimicrobial genes in vivo and in vitro: relevant in the pathogenesis of atopic dermatitis. Cytokine. 2013; 61: 419-25. doi: 10.1016/j.cyto.2012.10.031.
30. Landi A, Broadhurst D, Vernon SD, Tyrrell DL, Houghton M. Reductions in circulating levels of IL-16, IL-7 and VEGF-A in myalgic encephalomyelitis/chronic fatigue syndrome. Cytokine. 2016; 78: 27-36. doi: 10.1016/j. cyto.2015.11.018.
31. Takahashi H, Shibuya M. The vascular endothelial growth factor (VEGF)/VEGF receptor system and its role under physiological and pathological conditions. Clin Sci (Lond). 2005; 109: 227-41. doi: 10.1042/CS20040370.
32. Goel HL, Mercurio AM. VEGF targets the tumour cell. Nat Rev Cancer. 2013; 13: 871-82. doi: 10.1038/nrc3627.
33. Sivaraj KK, Takefuji M, Schmidt I, Adams RH, Offermanns S, Wettschureck N. G13 controls angiogenesis through regulation of VEGFR-2 expression. Dev Cell. 2013; 25: 427-34. doi: 10.1016/j.devcel.2013.04.008.
34. Gerald D, Adini I, Shechter S, Perruzzi C, Varnau J, Hopkins B, Kazerounian S, Kurschat P, Blachon S, Khedkar S, Bagchi M, Sherris D, Prendergast GC, et al. RhoB controls coordination of adult angiogenesis and lymphangiogenesis following injury by regulating VEZF1-mediated transcription. Nat Commun. 2013; 4: 2824. doi: 10.1038/ncomms3824.
35. Yoneda M, Hirokawa YS, Ohashi A, Uchida K, Kami D, Watanabe M, Yokoi T, Shiraishi T, Wakusawa S. RhoB enhances migration and MMP1 expression of prostate cancer DU145. Exp Mol Pathol. 2010; 88: 90-5. doi: 10.1016/j.yexmp.2009.09.010.
36. Hoeppner LH, Sinha S, Wang Y, Bhattacharya R, Dutta S, Gong X, Bedell VM, Suresh S, Chun C, Ramchandran R, Ekker SC, Mukhopadhyay D. RhoC maintains vascular homeostasis by regulating VEGF-induced signaling in endothelial cells. J Cell Sci. 2015; 128: 3556-68. doi: 10.1242/jcs.167601.
37. Okabe H, Satoh S, Kato T, Kitahara O, Yanagawa R, Yamaoka Y, Tsunoda T, Furukawa Y, Nakamura Y. Genomewide analysis of gene expression in human hepatocellular carcinomas using cDNA microarray: identification of genes involved in viral carcinogenesis and tumor progression. Cancer Res. 2001; 61: 2129-37.
38. Rose R, Weyand M, Lammers M, Ishizaki T, Ahmadian MR, Wittinghofer A. Structural and mechanistic insights into the interaction between Rho and mammalian Dia. Nature. 2005; 435: 513-8. doi: 10.1038/nature03604.
39. Wojciak-Stothard B, Zhao L, Oliver E, Dubois O, Wu Y, Kardassis D, Vasilaki E, Huang M, Mitchell JA, Harrington LS, Prendergast GC, Wilkins MR. Role of RhoB in the regulation of pulmonary endothelial and smooth muscle cell responses to hypoxia. Circ Res. 2012; 110: 1423-34. doi: 10.1161/CIRCRESAHA.112.264473.