Molecular profiling of cetuximab and bevacizumab treatment of colorectal tumours reveals perturbations in metabolic and hypoxic response pathways

Oncotarget

Volumn 6, Issue 35, 2015, Pages 38166-38180

  Greening, David W ^a   Lee, Sze Ting ^a,b,c   Ji, Hong ^a   Simpson, Richard J ^a   Rigopoulos, Angela ^a,c   Murone, Carmel ^a,c   Fang, Catherine ^a,c   Gong, Sylvia ^b   O'Keefe, Graeme ^a,b,c   Scott, Andrew M ^a,b,c  

^a LA TROBE UNIVERSITY   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c OLIVIA NEWTON JOHN CANCER RESEARCH INSTITUTE   (Australia)

Author keywords

Bevacizumab; Cancer therapeutics; Cetuximab; Hypoxia; Metabolism

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BEVACIZUMAB; CETUXIMAB; FASN PROTEIN; GLUCOSE; GLYCEROL 3 PHOSPATE DEHYDROGENASE; HSPG2 PROTEIN; OXIDOREDUCTASE; PROTEIN; PROTEOME; STAT3 PROTEIN; THBS1 PROTEIN; UNCLASSIFIED DRUG; ANGIOGENESIS INHIBITOR; PROTEIN KINASE INHIBITOR; TUMOR MARKER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER COMBINATION CHEMOTHERAPY; COLON CARCINOMA; COLORECTAL CARCINOMA; CONTROLLED STUDY; FATTY ACID METABOLISM; GLUCOSE METABOLISM; HISTOPATHOLOGY; HT 29 CELL LINE; HUMAN; HUMAN CELL; HYPOXIA; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; POSITRON EMISSION TOMOGRAPHY; PROTEIN ANALYSIS; PROTEIN DEFECT; PROTEOMICS; TUMOR MICROENVIRONMENT; TUMOR XENOGRAFT; WESTERN BLOTTING; ANIMAL; BAGG ALBINO MOUSE; CELL HYPOXIA; COLORECTAL NEOPLASMS; DRUG EFFECTS; DRUG SCREENING; ENERGY METABOLISM; GLYCOLYSIS; HT-29 CELL LINE; METABOLISM; NUDE MOUSE; PATHOLOGY; PROCEDURES; SIGNAL TRANSDUCTION; TIME FACTOR; TUMOR VOLUME;

ANGIOGENESIS INHIBITORS; ANIMALS; BEVACIZUMAB; BIOMARKERS, TUMOR; BLOTTING, WESTERN; CELL HYPOXIA; CETUXIMAB; COLORECTAL NEOPLASMS; ENERGY METABOLISM; GLYCOLYSIS; HT29 CELLS; HUMANS; IMMUNOHISTOCHEMISTRY; MICE, INBRED BALB C; MICE, NUDE; PROTEIN KINASE INHIBITORS; PROTEOMICS; SIGNAL TRANSDUCTION; TIME FACTORS; TUMOR BURDEN; TUMOR MICROENVIRONMENT; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84947748945     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.6241     Document Type: Article

References (62)

1. Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D, Bray F. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015: 136: E359-386.
2. Manfredi S, Lepage C, Hatem C, Coatmeur O, Faivre J, Bouvier AM. Epidemiology and management of liver metastases from colorectal cancer. Ann Surg. 2006: 244: 254-259.
3. Goldberg RM. Therapy for metastatic colorectal cancer. Oncologist. 2006: 11: 981-987.
4. Kelly H,Goldberg RM. Systemic therapy for metastatic colorectal cancer: current options, current evidence. J Clin Oncol. 2005: 23: 4553-4560.
5. Van Cutsem E, Cervantes A, Nordlinger B, Arnold D, Group EGW. Metastatic colorectal cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2014: 25 Suppl 3: iii1-9.
6. Wong Kee Song LM,Wilson BC. Endoscopic detection of early upper GI cancers. Best practice & research. Clinical gastroenterology. 2005: 19: 833-856.
7. Steele RJ. Modern challenges in colorectal cancer. The surgeon: journal of the Royal Colleges of Surgeons of Edinburgh and Ireland. 2006: 4: 285-291.
8. Habermann JK, Bader FG, Franke C, Zimmermann K, Gemoll T, Fritzsche B, Ried T, Auer G, Bruch HP, Roblick UJ. From the genome to the proteome-biomarkers in colorectal cancer. Langenbeck's archives of surgery/Deutsche Gesellschaft fur Chirurgie. 2008: 393: 93-104.
9. Kemeny NE. Treatment of metastatic colon cancer: "the times they are A-changing". J Clin Oncol. 2013: 31: 1913-1916.
10. Edwards MS, Chadda SD, Zhao Z, Barber BL, Sykes DP. A systematic review of treatment guidelines for metastatic colorectal cancer. Colorectal Dis. 2012: 14: e31-47.
11. O'Connor JP, Carano RA, Clamp AR, Ross J, Ho CC, Jackson A, Parker GJ, Rose CJ, Peale FV, Friesenhahn M, Mitchell CL, Watson Y, Roberts C, et al. Quantifying antivascular effects of monoclonal antibodies to vascular endothelial growth factor: insights from imaging. Clin Cancer Res. 2009: 15: 6674-6682.
12. Yuan F, Chen Y, Dellian M, Safabakhsh N, Ferrara N, Jain RK. Time-dependent vascular regression and permeability changes in established human tumor xenografts induced by an anti-vascular endothelial growth factor/vascular permeability factor antibody. Proc Natl Acad Sci U S A. 1996: 93: 14765-14770.
13. Lee CG, Heijn M, di Tomaso E, Griffon-Etienne G, Ancukiewicz M, Koike C, Park KR, Ferrara N, Jain RK, Suit HD,Boucher Y. Anti-Vascular endothelial growth factor treatment augments tumor radiation response under normoxic or hypoxic conditions. Cancer Res. 2000: 60: 5565-5570.
14. Borgstrom P, Hillan KJ, Sriramarao P, Ferrara N. Complete inhibition of angiogenesis and growth of microtumors by anti-vascular endothelial growth factor neutralizing antibody: novel concepts of angiostatic therapy from intravital videomicroscopy. Cancer Res. 1996: 56: 4032-4039.
15. Pavlidis ET,Pavlidis TE. Role of bevacizumab in colorectal cancer growth and its adverse effects: a review. World J Gastroenterol. 2013: 19: 5051-5060.
16. Kramer I,Lipp HP. Bevacizumab, a humanized anti-angiogenic monoclonal antibody for the treatment of colorectal cancer. J Clin Pharm Ther. 2007: 32: 1-14.
17. Keating GM. Bevacizumab: a review of its use in advanced cancer. Drugs. 2014: 74: 1891-1925.
18. Lenz HJ. Anti-EGFR mechanism of action: antitumor effect and underlying cause of adverse events. Oncology (Williston Park). 2006: 20: 5-13.
19. Spano JP, Lagorce C, Atlan D, Milano G, Domont J, Benamouzig R, Attar A, Benichou J, Martin A, Morere JF, Raphael M, Penault-Llorca F, Breau JL, et al. Impact of EGFR expression on colorectal cancer patient prognosis and survival. Ann Oncol. 2005: 16: 102-108.
20. Martinelli E, De Palma R, Orditura M, De Vita F, Ciardiello F. Anti-epidermal growth factor receptor monoclonal antibodies in cancer therapy. Clin Exp Immunol. 2009: 158: 1-9.
21. Blick SK,Scott LJ. Cetuximab: a review of its use in squamous cell carcinoma of the head and neck and metastatic colorectal cancer. Drugs. 2007: 67: 2585-2607.
22. Zhang W, Azuma M, Lurje G, Gordon MA, Yang D, Pohl A, Ning Y, Bohanes P, Gerger A, Winder T, Hollywood E, Danenberg KD, Saltz L, et al. Molecular predictors of combination targeted therapies (cetuximab, bevacizumab) in irinotecan-refractory colorectal cancer (BOND-2 study). Anticancer Res. 2010: 30: 4209-4217.
23. Saltz LB, Lenz HJ, Kindler HL, Hochster HS, Wadler S, Hoff PM, Kemeny NE, Hollywood EM, Gonen M, Quinones M, Morse M,Chen HX. Randomized phase II trial of cetuximab, bevacizumab, and irinotecan compared with cetuximab and bevacizumab alone in irinotecan-refractory colorectal cancer: the BOND-2 study. J Clin Oncol. 2007: 25: 4557-4561.
24. Lievre A, Bachet JB, Le Corre D, Boige V, Landi B, Emile JF, Cote JF, Tomasic G, Penna C, Ducreux M, Rougier P, Penault-Llorca F,Laurent-Puig P. KRAS mutation status is predictive of response to cetuximab therapy in colorectal cancer. Cancer Res. 2006: 66: 3992-3995.
25. Scott AM, Wolchok JD, Old LJ. Antibody therapy of cancer. Nat Rev Cancer. 2012: 12: 278-287.
26. Bergers G,Hanahan D. Modes of resistance to anti-angiogenic therapy. Nat Rev Cancer. 2008: 8: 592-603.
27. Tabernero J. The role of VEGF and EGFR inhibition: implications for combining anti-VEGF and anti-EGFR agents. Mol Cancer Res. 2007: 5: 203-220.
28. Ji H, Greening DW, Barnes TW, Lim JW, Tauro BJ, Rai A, Xu R, Adda C, Mathivanan S, Zhao W, Xue Y, Xu T, Zhu HJ, et al. Proteome profiling of exosomes derived from human primary and metastatic colorectal cancer cells reveal differential expression of key metastatic factors and signal transduction components. Proteomics. 2013: 13: 1672-1686.
29. Tauro BJ, Greening DW, Mathias RA, Mathivanan S, Ji H, Simpson RJ. Two distinct populations of exosomes are released from LIM1863 colon carcinoma cell-derived organoids. Mol. Cell. Proteomics. 2013: 12: 587-598.
30. Xu R, Greening DW, Rai A, Ji H, Simpson RJ. Highly-purified exosomes and shed microvesicles isolated from the human colon cancer cell line LIM1863 by sequential centrifugal ultrafiltration are biochemically and functionally distinct. Methods. 2015; In press.
31. Wild R, Fager K, Flefleh C, Kan D, Inigo I, Castaneda S, Luo FR, Camuso A, McGlinchey K, Rose WC. Cetuximab preclinical antitumor activity (monotherapy and combination based) is not predicted by relative total or activated epidermal growth factor receptor tumor expression levels. Mol Cancer Ther. 2006: 5: 104-113.
32. Kim SW, Hayashi M, Lo JF, Yang Y, Yoo JS, Lee JD. ADP-ribosylation factor 4 small GTPase mediates epidermal growth factor receptor-dependent phospholipase D2 activation. J Biol Chem. 2003: 278: 2661-2668.
33. Kim SW, Hayashi M, Lo JF, Yang Y, Yoo JS, Lee JD. ADP-ribosylation factor 4 small GTPase mediates epidermal growth factor receptor-dependent phospholipase D2 activation. J Biol Chem. 2003: 278: 2661-2668.
34. Monteleone F, Rosa R, Vitale M, D'Ambrosio C, Succoio M, Formisano L, Nappi L, Romano MF, Scaloni A, Tortora G, Bianco R,Zambrano N. Increased anaerobic metabolism is a distinctive signature in a colorectal cancer cellular model of resistance to antiepidermal growth factor receptor antibody. Proteomics. 2013: 13: 866-877.
35. Song YD, Zhang KF, Liu D, Guo YQ, Wang DY, Cui MY, Li G, Sun YX, Shen JH, Li XG, Zhang L,Shi FJ. Inhibition of EGFR-induced glucose metabolism sensitizes chondrosarcoma cells to cisplatin. Tumour biology: the J Int Soc Oncodevelopmental Biol Med. 2014: 35: 7017-7024.
36. Bian Y, Yu Y, Wang S, Li L. Up-regulation of fatty acid synthase induced by EGFR/ERK activation promotes tumor growth in pancreatic cancer. Biochem Biophys Res Commun. 2015: 463: 612-617.
37. Yang Y, Liu H, Li Z, Zhao Z, Yip-Schneider M, Fan Q, Schmidt CM, Chiorean EG, Xie J, Cheng L, Chen JH,Zhang JT. Role of fatty acid synthase in gemcitabine and radiation resistance of pancreatic cancers. Int J Biochem Mol Biol. 2011: 2: 89-98.
38. Carvalho MA, Zecchin KG, Seguin F, Bastos DC, Agostini M, Rangel AL, Veiga SS, Raposo HF, Oliveira HC, Loda M, Coletta RD,Graner E. Fatty acid synthase inhibition with Orlistat promotes apoptosis and reduces cell growth and lymph node metastasis in a mouse melanoma model. Int J Cancer. 2008: 123: 2557-2565.
39. Yang Y, Liu H, Li Z, Zhao Z, Yip-Schneider M, Fan Q, Schmidt CM, Chiorean EG, Xie J, Cheng L, Chen JH,Zhang JT. Role of fatty acid synthase in gemcitabine and radiation resistance of pancreatic cancers. International journal of biochemistry and molecular biology. 2011: 2: 89-98.
40. Flavin R, Peluso S, Nguyen PL, Loda M. Fatty acid synthase as a potential therapeutic target in cancer. Future oncology. 2010: 6: 551-562.
41. Sullivan R, Pare GC, Frederiksen LJ, Semenza GL, Graham CH. Hypoxia-induced resistance to anticancer drugs is associated with decreased senescence and requires hypoxia-inducible factor-1 activity. Mol Cancer Ther. 2008: 7: 1961-1973.
42. Hockel M,Vaupel P. Tumor hypoxia: definitions and current clinical, biologic, and molecular aspects. J Natl Cancer Inst. 2001: 93: 266-276.
43. Vaupel P,Mayer A. The clinical importance of assessing tumor hypoxia: relationship of tumor hypoxia to prognosis and therapeutic opportunities. Antioxid Redox Signal. 2015: 22: 878-880.
44. Luo HY, Wei W, Shi YX, Chen XQ, Li YH, Wang F, Qiu MZ, Li FH, Yan SL, Zeng MS, Huang P,Xu RH. Cetuximab enhances the effect of oxaliplatin on hypoxic gastric cancer cell lines. Oncology reports. 2010: 23: 1735-1745.
45. Selvakumaran M, Yao KS, Feldman MD, O'Dwyer PJ. Antitumor effect of the angiogenesis inhibitor bevacizumab is dependent on susceptibility of tumors to hypoxia-induced apoptosis. Biochemical pharmacology. 2008: 75: 627-638.
46. Whitehead RH, Macrae FA, St John DJ, Ma J. A colon cancer cell line (LIM1215) derived from a patient with inherited nonpolyposis colorectal cancer. J. Natl. Cancer Inst. 1985: 74: 759-765.
47. Le Bivic A, Hirn M, Reggio H. HT-29 cells are an in vitro model for the generation of cell polarity in epithelia during embryonic differentiation. Proc Natl Acad Sci U S A. 1988: 85: 136-140.
48. Bernhard OK, Greening DW, Barnes TW, Ji H, Simpson RJ. Detection of cadherin-17 in human colon cancer LIM1215 cell secretome and tumour xenograft-derived interstitial fluid and plasma. Biochim Biophys Acta. 2013: 1834: 2372-2379.
49. Gopal SK, Greening DW, Mathias RA, Ji H, Rai A, Chen M, Simpson RJ. YBX1/YB-1 induces partial EMT and tumourigenicity through secretion of angiogenic factors into the extracellular microenvironment Oncotarget. 2015: 6: 13718-30.
50. Clarke K, Lee FT, Brechbiel MW, Smyth FE, Old LJ, Scott AM. In vivo biodistribution of a humanized anti-Lewis Y monoclonal antibody (hu3S193) in MCF-7 xenografted BALB/c nude mice. Cancer Res. 2000: 60: 4804-4811.
51. Steinberg TH, Lauber WM, Berggren K, Kemper C, Yue S, Patton WF. Fluorescence detection of proteins in sodium dodecyl sulfate-polyacrylamide gels using environmentally benign, nonfixative, saline solution. Electrophoresis. 2000: 21: 497-508.
52. Tauro BJ, Mathias RA, Greening DW, Gopal SK, Ji H, Kapp EA, Coleman BM, Hill AF, Kusebauch U, Hallows JL, Shteynberg D, Moritz RL, Zhu HJ, et al. Oncogenic H-ras reprograms Madin-Darby canine kidney (MDCK) cell-derived exosomal proteins following epithelial-mesenchymal transition. Mol. Cell. Proteomics. 2013: 12: 2148-2159.
53. Shevchenko A, Tomas H, Havlis J, Olsen JV, Mann M. In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc. 2006: 1: 2856-2860.
54. Tauro BJ, Greening DW, Mathias RA, Ji H, Mathivanan S, Scott AM, Simpson RJ. Comparison of ultracentrifugation, density gradient separation, and immunoaffinity capture methods for isolating human colon cancer cell line LIM1863-derived exosomes. Methods. 2012: 56: 293-304.
55. Greening DW,Simpson RJ. A centrifugal ultrafiltration strategy for isolating the low-molecular weight ( < or = 25K) component of human plasma proteome. J Proteomics. 2010: 73: 637-648.
56. Olsen JV, de Godoy LM, Li G, Macek B, Mortensen P, Pesch R, Makarov A, Lange O, Horning S, Mann M. Parts per million mass accuracy on an Orbitrap mass spectrometer via lock mass injection into a C-trap. Mol Cell Proteomics. 2005: 4: 2010-2021.
57. Brosch M, Yu L, Hubbard T, Choudhary J. Accurate and sensitive peptide identification with Mascot Percolator. J Proteome Res. 2009: 8: 3176-3181.
58. Nesvizhskii AI,Aebersold R. Interpretation of shotgun proteomic data: the protein inference problem. Mol Cell Proteomics. 2005: 4: 1419-1440.
59. Keller A, Nesvizhskii AI, Kolker E, Aebersold R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Analytical chemistry. 2002: 74: 5383-5392.
60. Apweiler R, Bairoch A, Wu CH, Barker WC, Boeckmann B, Ferro S, Gasteiger E, Huang H, Lopez R, Magrane M, Martin MJ, Natale DA, O'Donovan C, et al. UniProt: the Universal Protein knowledgebase. Nucleic Acids Res. 2004: 32: D115-119.
61. Uhlen M, Bjorling E, Agaton C, Szigyarto CA, Amini B, Andersen E, Andersson AC, Angelidou P, Asplund A, Asplund C, Berglund L, Bergstrom K, Brumer H, et al. A human protein atlas for normal and cancer tissues based on antibody proteomics. Mol. Cell. Proteomics. 2005: 4: 1920-1932.
62. Benjamino Y,Hochberg F. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B-Stat. Methodol. 1995: 57: 289-300.