Surface proteomic analysis of osteosarcoma identifies EPHA2 as receptor for targeted drug delivery

British Journal of Cancer

Volumn 109, Issue 8, 2013, Pages 2142-2154

  Posthumadeboer, J ^a   Piersma, S R ^a   Pham, T V ^a   Van Egmond, P W ^a   Knol, J C ^a   Cleton Jansen, A M ^b   Van Geer, M A ^c   Van Beusechem, V W ^a   Kaspers, G J L ^a   Van Royen, B J ^a,d   Jimenez C R ^a   Helder, M N ^a,d  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c ACADEMIC MEDICAL CENTER   (Netherlands)

^d VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

drug delivery; EPHA2; osteosarcoma; proteomics; targeted therapy

Indexed keywords

ADAM10 ENDOPEPTIDASE; ADENOVIRUS VECTOR; ALPHA4 INTEGRIN; ALPHA6 INTEGRIN; BASAL CELL ADHESION MOLECULE; BETA4 INTEGRIN; CD70 ANTIGEN; COXSACKIE VIRUS AND ADENOVIRUS RECEPTOR; EPHRIN RECEPTOR A2; EPHRIN RECEPTOR B2; EPHRIN RECEPTOR B4; INSULIN RECEPTOR; LEUCINE RICH REPEAT CONTAINING PROTEIN 15; MEMBRANE PROTEIN; METAL TRANSPORTER CNNM3; METAL TRANSPORTER CNNM4; NEURAL CELL ADHESION MOLECULE 1; PLEXIN D1; PROTOCADHERIN FAT 1; RECEPTOR TYPE TYROSINE PROTEIN PHOSPHATASE ETA; SCAVENGER RECEPTOR CLASS B MEMBER 1; SODIUM BICARBONATE COTRANSPORTER 3; SOMATOMEDIN C RECEPTOR; SUSHI DOMAIN CONTAINING 5; SYNDECAN 4; TENEURIN 2; TENEURIN 3; TRANSMEMBRANE PROTEIN 2; TYROSINE PROTEIN KINASE RECEPTOR UFO; UNCLASSIFIED DRUG; UROKINASE PLASMINOGEN ACTIVATOR SURFACE RECEPTOR;

ARTICLE; BIOTINYLATION; CANCER CELL CULTURE; CELL SURFACE; CONTROLLED STUDY; DRUG DELIVERY SYSTEM; FEMALE; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LIQUID CHROMATOGRAPHY; MALE; OSTEOBLAST; OSTEOSARCOMA; OUTCOME ASSESSMENT; OVERALL SURVIVAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEOMICS; TANDEM MASS SPECTROMETRY; TISSUE MICROARRAY; UPREGULATION;

BONE NEOPLASMS; CELL LINE, TUMOR; CHROMATOGRAPHY, LIQUID; DATA MINING; FEMALE; FLOW CYTOMETRY; HUMANS; MALE; MEMBRANE PROTEINS; MIDDLE AGED; MOLECULAR TARGETED THERAPY; OSTEOSARCOMA; PROGNOSIS; PROTEOME; PROTEOMICS; RECEPTOR, EPHA2; TANDEM MASS SPECTROMETRY; UP-REGULATION;

EID: 84885898627     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2013.578     Document Type: Article

References (55)

1. Abdou AG, Abd el-Wahed MM, Asaad NY, Samaka RM, Abdallaha R (2010) Ephrin A4 expression in osteosarcoma, impact on prognosis, and patient outcome. Indian J Cancer 47: 46-52.
2. Albrethsen J, Knol JC, Piersma SR, Pham TV, de Wit M, Mongera S, Carvalho B, Verheul HM, Fijneman RJ, Meijer GA, Jimenez CR (2010) Subnuclear proteomics in colorectal cancer: Identification of proteins enriched in the nuclear matrix fraction and regulation in adenoma to carcinoma progression. Mol Cell Proteomics 9: 988-1005.
3. Altman DG (1991) Practical Statistics for Medical Research. Chapmann & Hall: London.
4. Avnet S, Sciacca L, Salerno M, Gancitano G, Cassarino MF, Longhi A, Zakikhani M, Carboni JM, Gottardis M, Giunti A, Pollak M, Vigneri R, Baldini N (2009) Insulin receptor isoform A and insulin-like growth factor II as additional treatment targets in human osteosarcoma. Cancer Res 69: 2443-2452.
5. Bielack SS, Kempf-Bielack B, Delling G, Exner GU, Flege S, Helmke K, Kotz R, Salzer-Kuntschik M, Werner M, Winkelmann W, Zoubek A, Jurgens H, Winkler K (2002) Prognostic factors in high-grade osteosarcoma of the extremities or trunk: An analysis of 1,702 patients treated on neoadjuvant cooperative osteosarcoma study group protocols. J Clin Oncol 20: 776-790.
6. Cai Y, Mohseny AB, Karperien M, Hogendoorn PC, Zhou G, Cleton-Jansen AM (2010) Inactive Wnt/beta-catenin pathway in conventional high-grade osteosarcoma. J Pathol 220: 24-33.
7. Chen K, Fallen S, Abaan HO, Hayran M, Gonzalez C, Wodajo F, MacDonald T, Toretsky JA, Uren A (2008) Wnt10b induces chemotaxis of osteosarcoma and correlates with reduced survival. Pediatr Blood Cancer 51: 349-355.
8. Cox J, Mann M (2007) Is proteomics the new genomics? Cell 130: 395-398.
9. De Wit M, Jimenez CR, Carvalho B, Belien JA, Delis-van Diemen PM, Mongera S, Piersma SR, Vikas M, Navani S, Ponten F, Meijer GA, Fijneman RJ (2012) Cell surface proteomics identifies glucose transporter type 1 and prion protein as candidate biomarkers for colorectal adenomato- carcinoma progression. Gut 61: 855-864.
10. Dickerson EB, Blackburn WH, Smith MH, Kapa LB, Lyon LA, McDonald JF (2010) Chemosensitization of cancer cells by siRNA using targeted nanogel delivery. BMC Cancer 10: 10.
11. Folio C, Mora MI, Zalacain M, Corrales FJ, Segura V, Sierrasesumaga L, Toledo G, San-Julian M, Patino-Garcia A (2009) Proteomic analysis of chemonaive pediatric osteosarcomas and corresponding normal bone reveals multiple altered molecular targets. J Proteome Res 8: 3882-3888.
12. Fritsche-Guenther R, Noske A, Ungethum U, Kuban RJ, Schlag PM, Tunn PU, Karle J, Krenn V, Dietel M, Sers C (2010) De novo expression of EphA2 in osteosarcoma modulates activation of the mitogenic signalling pathway. Histopathology 57: 836-850.
13. Gorlick R, Anderson P, Andrulis I, Arndt C, Beardsley GP, Bernstein M, Bridge J, Cheung NK, Dome JS, Ebb D, Gardner T, Gebhardt M, Grier H, Hansen M, Healey J, Helman L, Hock J, Houghton J, Houghton P, Huvos A, Khanna C, Kieran M, Kleinerman E, Ladanyi M, Lau C, Malkin D, Marina N, Meltzer P, Meyers P, Schofield D, Schwartz C, Smith MA, Toretsky J, Tsokos M, Wexler L, Wigginton J, Withrow S, Schoenfeldt M, Anderson B (2003) Biology of childhood osteogenic sarcoma and potential targets for therapeutic development: Meeting summary. Clin Cancer Res 9: 5442-5453.
14. Guo QC, Shen JN, Jin S, Wang J, Huang G, Zhang LJ, Huang G, Yin JQ, Zou CY, Li MT (2007a) Comparative proteomic analysis of human osteosarcoma and SV40-immortalized normal osteoblastic cell lines. Acta Pharmacol Sin 28: 850-858.
15. Guo Y, Rubin EM, Xie J, Zi X, Hoang BH (2008) Dominant negative LRP5 decreases tumorigenicity and metastasis of osteosarcoma in an animal model. Clin Orthop Relat Res 466: 2039-2045.
16. Guo Y, Zi X, Koontz Z, Kim A, Xie J, Gorlick R, Holcombe RF, Hoang BH (2007b) Blocking Wnt/LRP5 signaling by a soluble receptor modulates the epithelial to mesenchymal transition and suppresses met and metalloproteinases in osteosarcoma Saos-2 cells. J Orthop Res 25: 964-971.
17. Hammond SA, Lutterbuese R, Roff S, Lutterbuese P, Schlereth B, Bruckheimer E, Kinch MS, Coats S, Baeuerle PA, Kufer P, Kiener PA (2007) Selective targeting and potent control of tumor growth using an EphA2/CD3- Bispecific single-chain antibody construct. Cancer Res 67: 3927-3935.
18. Hua Y, Jia X, Sun M, Zheng L, Yin L, Zhang L, Cai Z (2011) Plasma membrane proteomic analysis of human osteosarcoma and osteoblastic cells: Revealing NDRG1 as a marker for osteosarcoma. Tumour Biol 32: 1013-1021.
19. Hughes DP (2009) Strategies for the targeted delivery of therapeutics for osteosarcoma. Expert Opin Drug Deliv 6: 1311-1321.
20. Jia SF, Worth LL, Kleinerman ES (1999) A nude mouse model of human osteosarcoma lung metastases for evaluating new therapeutic strategies. Clin Exp Metastasis 17: 501-506.
21. Kansara M, Thomas DM (2007) Molecular pathogenesis of osteosarcoma. DNA Cell Biol 26: 1-18.
22. Khanna C, Wan X, Bose S, Cassaday R, Olomu O, Mendoza A, Yeung C, Gorlick R, Hewitt SM, Helman LJ (2004) The membrane-cytoskeleton linker ezrin is necessary for osteosarcoma metastasis. Nat Med 10: 182-186.
23. Kim SY, Lee CH, Midura BV, Yeung C, Mendoza A, Hong SH, Ren L, Wong D, Korz W, Merzouk A, Salari H, Zhang H, Hwang ST, Khanna C, Helman LJ (2008) Inhibition of the CXCR4/CXCL12 chemokine pathway reduces the development of murine pulmonary metastases. Clin Exp Metastasis 25: 201-211.
24. Kolb EA, Kamara D, Zhang W, Lin J, Hingorani P, Baker L, Houghton P, Gorlick R (2010) R1507, a fully human monoclonal antibody targeting IGF-1R, is effective alone and in combination with rapamycin in inhibiting growth of osteosarcoma xenografts. Pediatr Blood Cancer 55: 67-75.
25. Krishnan K, Khanna C, Helman LJ (2005) The biology of metastases in pediatric sarcomas. Cancer J 11: 306-313.
26. Landen Jr CN, Chavez-Reyes A, Bucana C, Schmandt R, Deavers MT, Lopez- Berestein G, Sood AK (2005) Therapeutic EphA2 gene targeting in vivo using neutral liposomal small interfering RNA delivery. Cancer Res 65: 6910-6918.
27. Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33: 159-174.
28. Lee JW, Stone RL, Lee SJ, Nam EJ, Roh JW, Nick AM, Han HD, Shahzad MM, Kim HS, Mangala LS, Jennings NB, Mao S, Gooya J, Jackson D, Coleman RL, Sood AK (2010) EphA2 targeted chemotherapy using an antibody drug conjugate in endometrial carcinoma. Clin Cancer Res 16: 2562-2570.
29. Liu X, Zeng B, Ma J, Wan C (2009) Comparative proteomic analysis of osteosarcoma cell and human primary cultured osteoblastic cell. Cancer Invest 27: 345-352.
30. Lund R, Leth-Larsen R, Jensen ON, Ditzel HJ (2009) Efficient isolation and quantitative proteomic analysis of cancer cell plasma membrane proteins for identification of metastasis-associated cell surface markers. J Proteome Res 8: 3078-3090.
31. Mansky PJ, Liewehr DJ, Steinberg SM, Chrousos GP, Avila NA, Long L, Bernstein D, Mackall CL, Hawkins DS, Helman LJ (2002) Treatment of metastatic osteosarcoma with the somatostatin analog OncoLar: Significant reduction of insulin-like growth factor-1 serum levels. J Pediatr Hematol Oncol 24: 440-446.
32. Marco RA, Diaz-Montero CM, Wygant JN, Kleinerman ES, McIntyre BW (2003) Alpha 4 integrin increases anoikis of human osteosarcoma cells. J Cell Biochem 88: 1038-1047.
33. McQueen P, Ghaffar S, Guo Y, Rubin EM, Zi X, Hoang BH (2011) The Wnt signaling pathway: Implications for therapy in osteosarcoma. Expert Rev Anticancer Ther 11: 1223-1232.
34. Mitra S, Duggineni S, Koolpe M, Zhu X, Huang Z, Pasquale EB (2010) Structure-activity relationship analysis of peptides targeting the EphA2 receptor. Biochemistry 49: 6687-6695.
35. Mohseny AB, Szuhai K, Romeo S, Buddingh EP, Briaire-de Bruijn I, de Jong D, van Pel M, Cleton-Jansen AM, Hogendoorn PC (2009) Osteosarcoma originates from mesenchymal stem cells in consequence of aneuploidization and genomic loss of Cdkn2. J Pathol 219: 294-305.
36. Pasquale EB (2010) Eph receptors and ephrins in cancer: bidirectional signalling and beyond. Nat Rev Cancer 10: 165-180.
37. Pham TV, Piersma SR, Oudgenoeg G, Jimenez CR (2012) Label-free mass spectrometry-based proteomics for biomarker discovery and validation. Expert Rev Mol Diagn 12: 343-359.
38. Pham TV, Piersma SR, Warmoes M, Jimenez CR (2010) On the beta-binomial model for analysis of spectral count data in label-free tandem mass spectrometry-based proteomics. Bioinformatics 26: 363-369.
39. Piersma SR, Fiedler U, Span S, Lingnau A, PhamTV, Hoffmann S, KubbutatMH, Jimenez CR (2010) Workflow comparison for label-free, quantitative secretome proteomics for cancer biomarker discovery: Method evaluation, differential analysis, and verification in serum. J Proteome Res 9: 1913-1922.
40. PosthumaDeBoer J, van Egmond PW, Helder MN, de Menezes RX, Cleton- Jansen AM, Belien JA, Verheul HM, van Royen BJ, Kaspers GJ, Van Beusechem VW (2012) Targeting JNK-interacting-protein-1 (JIP1) sensitises osteosarcoma to doxorubicin. Oncotarget 3: 1169-1181.
41. Rochet N, Dubousset J, Mazeau C, Zanghellini E, Farges MF, de Novion HS, Chompret A, Delpech B, Cattan N, Frenay M, Gioanni J (1999) Establishment, characterisation and partial cytokine expression profile of a new human osteosarcoma cell line (CAL 72). Int J Cancer 82: 282-285.
42. Rosen G, Caparros B, Huvos AG, Kosloff C, Nirenberg A, Cacavio A, Marcove RC, Lane JM, Mehta B, Urban C (1982) Preoperative chemotherapy for osteogenic sarcoma: Selection of postoperative adjuvant chemotherapy based on the response of the primary tumor to preoperative chemotherapy. Cancer 49: 1221-1230.
43. Rubin EM, Guo Y, Tu K, Xie J, Zi X, Hoang BH (2010) Wnt inhibitory factor 1 decreases tumorigenesis and metastasis in osteosarcoma. Mol Cancer Ther 9: 731-741.
44. Scarberry KE, Dickerson EB, McDonald JF, Zhang ZJ (2008) Magnetic nanoparticle-peptide conjugates for in vitro and in vivo targeting and extraction of cancer cells. J Am Chem Soc 130: 10258-10262.
45. Scheurer SB, Rybak JN, Roesli C, Brunisholz RA, Potthast F, Schlapbach R, Neri D, Elia G (2005) Identification and relative quantification of membrane proteins by surface biotinylation and two-dimensional peptide mapping. Proteomics 5: 2718-2728.
46. Stevens TJ, Arkin IT (2000) Do more complex organisms have a greater proportion of membrane proteins in their genomes? Proteins 39: 417-420.
47. Tandon M, Vemula SV, Mittal SK (2011) Emerging strategies for EphA2 receptor targeting for cancer therapeutics. Expert Opin Ther Targets 15: 31-51.
48. Udayakumar D, Zhang G, Ji Z, Njauw CN, Mroz P, Tsao H (2011) Epha2 is a critical oncogene in melanoma. Oncogene 30: 4921-4929.
49. Van Geer MA, Bakker CT, Koizumi N, Mizuguchi H, Wesseling JG, Oude Elferink RP, Bosma PJ (2009) Ephrin A2 receptor targeting does not increase adenoviral pancreatic cancer transduction in vivo. World J Gastroenterol 15: 2754-2762.
50. Van Geer MA, Brevoord D, Kuhlmann KF, Bakker CT, Mizuguchi H, Wesseling JG, Ten Kate FJ, Gouma DJ, Oude Elferink RP, Bosma PJ (2010) A fiber modified adenovirus vector that targets to the EphrinA2 receptor reveals enhanced gene transfer to ex vivo pancreatic cancer. Int J Oncol 36: 233-244.
51. Varelias A, Koblar SA, Cowled PA, Carter CD, Clayer M (2002) Human osteosarcoma expresses specific ephrin profiles: Implications for tumorigenicity and prognosis. Cancer 95: 862-869.
52. Wan X, Kim SY, Guenther LM, Mendoza A, Briggs J, Yeung C, Currier D, Zhang H, Mackall C, Li WJ, Tuan RS, Deyrup AT, Khanna C, Helman L (2009) Beta4 integrin promotes osteosarcoma metastasis and interacts with ezrin. Oncogene 28: 3401-3411.
53. Wu CC, Yates III JR (2003) The application of mass spectrometry to membrane proteomics. Nat Biotechnol 21: 262-267.
54. Zhang YK, Zhang XH, Li JM, Sun dS, Yang Q, Diao DM (2009) A proteomic study on a human osteosarcoma cell line Saos-2 treated with diallyl trisulfide. Anticancer Drugs 20: 702-712.
55. Zhang Z, Zhang L, Hua Y, Jia X, Li J, Hu S, Peng X, Yang P, Sun M, Ma F, Cai Z (2010) Comparative proteomic analysis of plasma membrane proteins between human osteosarcoma and normal osteoblastic cell lines. BMC Cancer 10: 206