CD147 and downstream ADAMTSs promote the tumorigenicity of Kaposi's sarcoma-associated herpesvirus infected endothelial cells

Oncotarget

Volumn 7, Issue 4, 2016, Pages 3806-3818

  Dai, Lu ^a,b   Trillo Tinoco, Jimena ^b   Chen, Yihan ^a   Bonstaff, Karlie ^b   Valle, Luis Del ^b   Parsons, Chris ^b   Ochoa, Augusto C ^b   Zabaleta, Jovanny ^b   Toole, Bryan P ^c   Qin, Zhiqiang ^a,b  

^a TONGJI UNIVERSITY SCHOOL OF MEDICINE   (China)

^b LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

CD147; Kaposi's sarcoma; KSHV; Microarray

Indexed keywords

ADAMTS1 PROTEIN; ADAMTS9 PROTEIN; CD147 ANTIGEN; INTERLEUKIN 6; METALLOPROTEINASE; UNCLASSIFIED DRUG; VASCULOTROPIN; ADAM PROTEIN; ADAMTS1 PROTEIN, HUMAN; BSG PROTEIN, HUMAN; MESSENGER RNA;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER TISSUE; CELL INVASION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE ASSOCIATION; GENE EXPRESSION; HUMAN; HUMAN HERPESVIRUS 8; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HUMAN TISSUE; IN VIVO STUDY; KAPOSI SARCOMA; MICROARRAY ANALYSIS; MOUSE; MOUSE MODEL; NONHUMAN; NUDE MOUSE; PROTEIN EXPRESSION; PROTEIN TARGETING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UMBILICAL VEIN ENDOTHELIAL CELL; UPREGULATION; VIRUS CELL INTERACTION; ANIMAL; APOPTOSIS; CELL CULTURE; CELL PROLIFERATION; DRUG SCREENING; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; PATHOGENICITY; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; VASCULAR ENDOTHELIUM; VIROLOGY; VIRUS CELL TRANSFORMATION; WESTERN BLOTTING;

ADAM PROTEINS; ADAMTS1 PROTEIN; ANIMALS; ANTIGENS, CD147; APOPTOSIS; BLOTTING, WESTERN; CELL PROLIFERATION; CELL TRANSFORMATION, VIRAL; CELLS, CULTURED; ENDOTHELIUM, VASCULAR; GENE EXPRESSION PROFILING; HERPESVIRUS 8, HUMAN; HUMANS; MICE; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SARCOMA, KAPOSI; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84957998539     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.6584     Document Type: Article

References (47)

1. Chang Y, Cesarman E, Pessin MS, Lee F, Culpepper J, Knowles DM, Moore PS. Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposi's sarcoma. Science. 1994; 266:1865-1869.
2. Engels EA, Biggar RJ, Hall HI, Cross H, Crutchfield A, Finch JL, Grigg R, Hylton T, Pawlish KS, McNeel TS, Goedert JJ. Cancer risk in people infected with human immunodeficiency virus in the United States. Int J Cancer. 2008; 123:187-194.
3. Bonnet F, Lewden C, May T, Heripret L, Jougla E, Bevilacqua S, Costagliola D, Salmon D, Chene G, Morlat P. Malignancy-related causes of death in human immunodeficiency virus-infected patients in the era of highly active antiretroviral therapy. Cancer. 2004; 101:317-324.
4. Jenkins FJ, Hoffman LJ, Liegey-Dougall A. Reactivation of and primary infection with human herpesvirus 8 among solid-organ transplant recipients. J Infect Dis. 2002; 185:1238-1243.
5. Luppi M, Barozzi P, Santagostino G, Trovato R, Schulz TF, Marasca R, Bottalico D, Bignardi L, Torelli G. Molecular evidence of organ-related transmission of Kaposi sarcomaassociated herpesvirus or human herpesvirus-8 in transplant patients. Blood. 2000; 96:3279-3281.
6. Ariza-Heredia EJ, Razonable RR. Human herpes virus 8 in solid organ transplantation. Transplantation. 2011; 92: 837-844.
7. Biswas C, Zhang Y, DeCastro R, Guo H, Nakamura T, Kataoka H, Nabeshima K. The human tumor cell-derived collagenase stimulatory factor (renamed EMMPRIN) is a member of the immunoglobulin superfamily. Cancer Res. 1995; 55:434-439.
8. Yan L, Zucker S, Toole BP. Roles of the multifunctional glycoprotein, emmprin (basigin; CD147), in tumour progression. Thromb Haemost. 2005; 93:199-204.
9. Grass GD, Dai L, Qin Z, Parsons C, Toole BP. CD147: regulator of hyaluronan signaling in invasiveness and chemoresistance. Adv Cancer Res. 2014; 123:351-373.
10. Qin Z, Dai L, Slomiany MG, Toole BP, Parsons C. Direct activation of emmprin and associated pathogenesis by an oncogenic herpesvirus. Cancer Res. 2010; 70:3884-3889.
11. Dai L, Bratoeva M, Toole BP, Qin Z, Parsons C. KSHV activation of VEGF secretion and invasion for endothelial cells is mediated through viral up-regulation of emmprininduced signal transduction. Int J Cancer. 2012; 131: 834-843.
12. Qin Z, Dai L, Bratoeva M, Slomiany MG, Toole BP, Parsons C. Cooperative roles for emmprin and LYVE-1 in the regulation of chemoresistance for primary effusion lymphoma. Leukemia. 2011; 25:1598-1609.
13. An FQ, Folarin HM, Compitello N, Roth J, Gerson SL, McCrae KR, Fakhari FD, Dittmer DP, Renne R. Long-terminfected telomerase-immortalized endothelial cells: a model for Kaposi's sarcoma-associated herpesvirus latency in vitro and in vivo. J Virol. 2006; 80:4833-4846.
14. McAllister SC, Hansen SG, Ruhl RA, Raggo CM, DeFilippis VR, Greenspan D, Fruh K, Moses AV. Kaposi sarcoma-associated herpesvirus (KSHV) induces heme oxygenase-1 expression and activity in KSHV-infected endothelial cells. Blood. 2004; 103:3465-3473.
15. Alcendor DJ, Knobel S, Desai P, Zhu WQ, Hayward GS. KSHV regulation of fibulin-2 in Kaposi's sarcoma: implications for tumorigenesis. Am J Pathol. 2011; 179:1443-1454.
16. Cross NA, Chandrasekharan S, Jokonya N, Fowles A, Hamdy FC, Buttle DJ, Eaton CL. The expression and regulation of ADAMTS-1,-4,-5,-9, and-15, and TIMP-3 by TGFbeta1 in prostate cells: relevance to the accumulation of versican. Prostate. 2005; 63:269-275.
17. Ricciardelli C, Frewin KM, Tan Ide A, Williams ED, Opeskin K, Pritchard MA, Ingman WV, Russell DL. The ADAMTS1 protease gene is required for mammary tumor growth and metastasis. Am J Pathol. 2011; 179:3075-3085.
18. Okada Y. Tumor cell-matrix interaction: pericellular matrix degradation and metastasis. Verh Dtsch Ges Pathol. 2000; 84:33-42.
19. Demircan K, Gunduz E, Gunduz M, Beder LB, Hirohata S, Nagatsuka H, Cengiz B, Cilek MZ, Yamanaka N, Shimizu K, Ninomiya Y. Increased mRNA expression of ADAMTS metalloproteinases in metastatic foci of head and neck cancer. Head Neck. 2009; 31:793-801.
20. Tan Ide A, Ricciardelli C, Russell DL. The metalloproteinase ADAMTS1: a comprehensive review of its role in tumorigenic and metastatic pathways. Int J Cancer. 2013; 133:2263-2276.
21. Kim SH, Sierra RA, McGee DJ, Zabaleta J. Transcriptional profiling of gastric epithelial cells infected with wild type or arginase-deficient Helicobacter pylori. BMC Microbiol. 2012; 12:175.
22. Cavallin LE, Goldschmidt-Clermont P, Mesri EA. Molecular and cellular mechanisms of KSHV oncogenesis of Kaposi's sarcoma associated with HIV/AIDS. PLoS Pathog. 2014; 10:e1004154.
23. Mesri EA, Feitelson MA, Munger K. Human viral oncogenesis: a cancer hallmarks analysis. Cell Host Microbe. 2014; 15:266-282.
24. Mesri EA, Cesarman E, Boshoff C. Kaposi's sarcoma and its associated herpesvirus. Nat Rev Cancer. 2010; 10: 707-719.
25. Riva G, Barozzi P, Torelli G, Luppi M. Immunological and inflammatory features of Kaposi's sarcoma and other Kaposi's sarcoma-associated herpesvirus/human herpesvirus 8-associated neoplasias. AIDS Rev. 2010; 12:40-51.
26. Ensoli B, Sturzl M. Kaposi's sarcoma: a result of the interplay among inflammatory cytokines, angiogenic factors and viral agents. Cytokine Growth Factor Rev. 1998; 9:63-83.
27. Sivakumar R, Sharma-Walia N, Raghu H, Veettil MV, Sadagopan S, Bottero V, Varga L, Levine R, Chandran B. Kaposi's sarcoma-associated herpesvirus induces sustained levels of vascular endothelial growth factors A and C early during in vitro infection of human microvascular dermal endothelial cells: biological implications. J Virol. 2008; 82:1759-1776.
28. Qian LW, Xie J, Ye F, Gao SJ. Kaposi's sarcoma-associated herpesvirus infection promotes invasion of primary human umbilical vein endothelial cells by inducing matrix metalloproteinases. J Virol. 2007; 81:7001-7010.
29. Ballestas ME, Chatis PA, Kaye KM. Efficient persistence of extrachromosomal KSHV DNA mediated by latencyassociated nuclear antigen. Science. 1999; 284:641-644.
30. Dai L, Chen Y, Toole B, Parsons C, Qin Z. Induction of hyaluronan production by oncogenic KSHV and the contribution to viral pathogenesis in AIDS patients. Cancer Lett. 2015; 362:158-166.
31. Cheng F, Pekkonen P, Laurinavicius S, Sugiyama N, Henderson S, Gunther T, Rantanen V, Kaivanto E, Aavikko M, Sarek G, Hautaniemi S, Biberfeld P, Aaltonen L, et al. KSHV-initiated notch activation leads to membrane-type-1 matrix metalloproteinase-dependent lymphatic endothelial-to-mesenchymal transition. Cell Host Microbe. 2011; 10:577-590.
32. Gasperini P, Espigol-Frigole G, McCormick PJ, Salvucci O, Maric D, Uldrick TS, Polizzotto MN, Yarchoan R, Tosato G. Kaposi sarcoma herpesvirus promotes endothelial-to-mesenchymal transition through Notchdependent signaling. Cancer Res. 2012; 72:1157-1169.
33. Wu J, Ru NY, Zhang Y, Li Y, Wei D, Ren Z, Huang XF, Chen ZN, Bian H. HAb18G/CD147 promotes epithelialmesenchymal transition through TGF-beta signaling and is transcriptionally regulated by Slug. Oncogene. 2011; 30:4410-4427.
34. Grass GD, Bratoeva M, Toole BP. Regulation of invadopodia formation and activity by CD147. J Cell Sci. 2012; 125:777-788.
35. Grass GD, Tolliver LB, Bratoeva M, Toole BP. CD147, CD44, and the epidermal growth factor receptor (EGFR) signaling pathway cooperate to regulate breast epithelial cell invasiveness. J Biol Chem. 2013; 288:26089-26104.
36. Wang J, Fu L, Gu F, Ma Y. Notch1 is involved in migration and invasion of human breast cancer cells. Oncol Rep. 2011; 26:1295-1303.
37. Quemener C, Gabison EE, Naimi B, Lescaille G, Bougatef F, Podgorniak MP, Labarchede G, Lebbe C, Calvo F, Menashi S, Mourah S. Extracellular matrix metalloproteinase inducer up-regulates the urokinasetype plasminogen activator system promoting tumor cell invasion. Cancer Res. 2007; 67:9-15.
38. Kuno K, Matsushima K. ADAMTS-1 protein anchors at the extracellular matrix through the thrombospondin type I motifs and its spacing region. J Biol Chem. 1998; 273:13912-13917.
39. Hatipoglu OF, Hirohata S, Cilek MZ, Ogawa H, Miyoshi T, Obika M, Demircan K, Shinohata R, Kusachi S, Ninomiya Y. ADAMTS1 is a unique hypoxic early response gene expressed by endothelial cells. J Biol Chem. 2009; 284:16325-16333.
40. Ke X, Fei F, Chen Y, Xu L, Zhang Z, Huang Q, Zhang H, Yang H, Chen Z, Xing J. Hypoxia up-regulates CD147 through a combined effect of HIF-1alpha and Sp1 to promote glycolysis and tumor progression in epithelial solid tumors. Carcinogenesis. 2012; 33:1598-1607.
41. Cai Q, Lan K, Verma SC, Si H, Lin D, Robertson ES. Kaposi's sarcoma-associated herpesvirus latent protein LANA interacts with HIF-1 alpha to up-regulate RTA expression during hypoxia: Latency control under low oxygen conditions. J Virol. 2006; 80:7965-7975.
42. Ma Q, Cavallin LE, Yan B, Zhu S, Duran EM, Wang H, Hale LP, Dong C, Cesarman E, Mesri EA, Goldschmidt-Clermont PJ. Antitumorigenesis of antioxidants in a transgenic Rac1 model of Kaposi's sarcoma. Proc Natl Acad Sci U S A. 2009; 106:8683-8688.
43. Shin YC, Joo CH, Gack MU, Lee HR, Jung JU. Kaposi's sarcoma-associated herpesvirus viral IFN regulatory factor 3 stabilizes hypoxia-inducible factor-1 alpha to induce vascular endothelial growth factor expression. Cancer Res. 2008; 68:1751-1759.
44. Sodhi A, Montaner S, Patel V, Zohar M, Bais C, Mesri EA, Gutkind JS. The Kaposi's sarcoma-associated herpes virus G protein-coupled receptor up-regulates vascular endothelial growth factor expression and secretion through mitogen-activated protein kinase and p38 pathways acting on hypoxia-inducible factor 1alpha. Cancer Res. 2000; 60:4873-4880.
45. Dai L, Trillo-Tinoco J, Bai L, Kang B, Xu Z, Wen X, Del Valle L, Qin Z. Systematic analysis of a xenograft mice model for KSHV+ primary effusion lymphoma (PEL). PLoS One. 2014; 9:e90349.
46. Qin Z, Dai L, Defee M, Findlay VJ, Watson DK, Toole BP, Cameron J, Peruzzi F, Kirkwood K, Parsons C. Kaposi's sarcoma-associated herpesvirus suppression of DUSP1 facilitates cellular pathogenesis following de novo infection. J Virol. 2013; 87:621-635.
47. Workman C, Jensen LJ, Jarmer H, Berka R, Gautier L, Nielser HB, Saxild HH, Nielsen C, Brunak S, Knudsen S. A new non-linear normalization method for reducing variability in DNA microarray experiments. Genome Biol. 2002; 3:research0048.