Anti-VEGF antibody therapy induces tumor hypoxia and stanniocalcin 2 expression and potentiates growth of human colon cancer xenografts

International Journal of Cancer

Volumn 135, Issue 2, 2014, Pages 295-307

  Miyazaki, Shinichiro ^a   Kikuchi, Hirotoshi ^a   Iino, Ichirota ^a   Uehara, Takashi ^a   Setoguchi, Tomohiko ^a   Fujita, Takeshi ^a   Hiramatsu, Yoshihiro ^a   Ohta, Manabu ^a   Kamiya, Kinji ^a   Kitagawa, Kyoko ^a   Kitagawa, Masatoshi ^a   Baba, Satoshi ^a   Konno, Hiroyuki ^a  

^a HAMAMATSU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

angiogenesis; colon cancers; hypoxia; stanniocalcin 2; VEGF

Indexed keywords

ALDEHYDE DEHYDROGENASE; ALDEHYDE DEHYDROGENASE ISOENZYME 1; HYPOCALCIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; STANNIOCALCIN 2; UNCLASSIFIED DRUG; VASCULOTROPIN ANTIBODY;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER INHIBITION; CELL COUNT; COLON CANCER; COLORECTAL LIVER METASTASIS; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG EFFECT; DRUG MECHANISM; DRUG RESPONSE; GENE EXPRESSION; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MALE; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; STANNIOCALCIN 2 GENE; TUMOR MICROENVIRONMENT; TUMOR VOLUME; TUMOR XENOGRAFT; UPREGULATION;

ANGIOGENESIS; COLON CANCERS; HYPOXIA; STANNIOCALCIN 2; VEGF;

ANGIOGENESIS INHIBITORS; ANIMALS; ANTIBODIES, MONOCLONAL, HUMANIZED; BLOTTING, WESTERN; CELL HYPOXIA; CELL LINE, TUMOR; COLONIC NEOPLASMS; DISEASE PROGRESSION; DRUG RESISTANCE, NEOPLASM; GENE KNOCKDOWN TECHNIQUES; GLYCOPROTEINS; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MICE; MICE, INBRED BALB C; MICE, NUDE; NEOVASCULARIZATION, PATHOLOGIC; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REAL-TIME POLYMERASE CHAIN REACTION; UP-REGULATION; VASCULAR ENDOTHELIAL GROWTH FACTOR A; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84900037425     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.28686     Document Type: Article

References (42)

1. Cunningham D, Atkin W, Lenz HJ, et al. Colorectal cancer. Lancet 2010; 375: 1030-47.
2. Folkman J,. Angiogenesis in psoriasis: therapeutic implications. J Invest Dermatol 1972; 59: 40-3.
3. Donnem T, Hu J, Ferguson M, et al. Vessel co-option in primary human tumors and metastases: an obstacle to effective anti-angiogenic treatment? Cancer Med 2013; 2: 427-36.
4. Hurwitz H, Fehrenbacher L, Novotny W, et al. Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. New Eng J Med 2004; 350: 2335-42.
5. Ellis LM, Hicklin DJ,. VEGF-targeted therapy: mechanisms of anti-tumour activity. Nat Rev Cancer 2008; 8: 579-91.
6. Nazer B, Humphreys BD, Moslehi J,. Effects of novel angiogenesis inhibitors for the treatment of cancer on the cardiovascular system: focus on hypertension. Circulation 2011; 124: 1687-91.
7. Casanovas O, Hicklin DJ, Bergers G, Hanahan D,. Drug resistance by evasion of antiangiogenic targeting of VEGF signaling in late-stage pancreatic islet tumors. Cancer Cell 2005; 8: 299-309.
8. Pàez-Ribes M, Allen E, Hudock J, et al. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell 2009; 15: 220-31.
9. Conley SJ, Gheordunescu E, Kakarala P, et al. Antiangiogenic agents increase breast cancer stem cells via the generation of tumor hypoxia. Proc Natl Acad Sci 2012; 109: 2784-9.
10. Cacheux W, Boisserie T, Staudacher L, et al. Reversible tumor growth acceleration following bevacizumab interruption in metastatic colorectal cancer patients scheduled for surgery. Ann Oncol 2008; 19: 1659-61.
11. Miles D, Harbeck N, Escudier B, et al. Disease course patterns after discontinuation of bevacizumab: pooled analysis of randomized phase III trials. J Clin Oncol 2011; 29: 83-8.
12. Davies JM, Goldberg RM,. Treatment of metastatic colorectal cancer. Sem Oncol 2011; 38: 552-60.
13. Yamamoto M, Kikuchi H, Ohta M, et al. TSU68 prevents liver metastasis of colon cancer xenografts by modulating the premetastatic niche. Cancer Res 2008; 68: 9754-62.
14. Shoji T, Konno H, Tanaka T, et al. Orthotopic implantation of a colon cancer xenograft induces high expression of cyclooxygenase-2. Cancer Lett 2003; 195: 235-41.
15. Tanaka T, Konno H, Matsuda I, et al. Prevention of hepatic metastasis of human colon cancer by angiogenesis inhibitor TNP-470. Cancer Res 1995; 55: 836-9.
16. Konno H, Tanaka T, Matsuda I, et al. Comparison of the inhibitory effect of the angiogenesis inhibitor, TNP-470, and mitomycin C on the growth and liver metastasis of human colon cancer. Int J Cancer J Int du cancer 1995; 61: 268-71.
17. Kikuchi H, Pino MS, Zeng M, et al. Oncogenic KRAS and BRAF differentially regulate hypoxia-inducible factor-1 and -2 in colon cancer. Cancer Res 2009; 69: 8499-506.
18. Weidner N, Semple JP, Welch WR, et al. Tumor angiogenesis and metastasis-correlation in invasive breast carcinoma. New Eng J Med 1991; 324: 1-8.
19. Mahy P, De Bast M, Gallez B, et al. In vivo colocalization of 2-nitroimidazole EF5 fluorescence intensity and electron paramagnetic resonance oximetry in mouse tumors. Radiotherapy Oncol 2003; 67: 53-61.
20. Subramanian A,. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci 2005; 102: 15545-50.
21. Majmundar AJ, Wong WJ, Simon MC,. Hypoxia-inducible factors and the response to hypoxic stress. Mol Cell 2010; 40: 294-309.
22. Huang EH, Hynes MJ, Zhang T, et al. Aldehyde dehydrogenase 1 is a marker for normal and malignant human colonic stem cells (SC) and tracks SC overpopulation during colon tumorigenesis. Cancer Res 2009; 69: 3382-9.
23. Todaro M, Francipane MG, Medema JP, et al. Colon cancer stem cells: promise of targeted therapy. Gastroenterology 2010; 138: 2151-62.
24. Ieta K, Tanaka F, Yokobori T, et al. Clinicopathological significance ofstanniocalcin 2gene expression in colorectal cancer. Int J Cancer 2009; 125: 926-31.
25. Law AY, Wong CK,. Stanniocalcin-2 is a HIF-1 target gene that promotes cell proliferation in hypoxia. Exp Cell Res 2010; 316: 466-76.
26. Volland S, Kugler W, Schweigerer L, et al. Stanniocalcin 2 promotes invasion and is associated with metastatic stages in neuroblastoma. Int J Cancer 2009; 125: 2049-57.
27. Law AYS, Wong CKC,. Stanniocalcin-2 promotes epithelial-mesenchymal transition and invasiveness in hypoxic human ovarian cancer cells. Exp Cell Res 2010; 316: 3425-34.
28. Zuniga RM, Torcuator R, Jain R, et al. Rebound tumour progression after the cessation of bevacizumab therapy in patients with recurrent high-grade glioma. J Neurooncol 2010; 99: 237-42.
29. Bergers G, Hanahan D,. Modes of resistance to anti-angiogenic therapy. Nat Rev Cancer 2008; 8: 592-603.
30. Yeung BHY, Law AYS, Wong CKC,. Evolution and roles of stanniocalcin. Mol Cell Endocrinol 2012; 349: 272-80.
31. Chang AC, Jellinek DA, Reddel RR,. Mammalian stanniocalcins and cancer. Endocr Relat Cancer 2003; 10: 359-73.
32. Meyer H-A, Tölle A, Jung M, et al. Identification of Stanniocalcin 2 as prognostic marker in renal cell carcinoma. Eur Urol 2009; 55: 669-78.
33. Joensuu K, Heikkila P, Andersson LC,. Tumor dormancy: elevated expression of stanniocalcins in late relapsing breast cancer. Cancer Lett 2008; 265: 76-83.
34. Tamura K, Furihata M, Chung S-Y, et al. Stanniocalcin 2 overexpression in castration-resistant prostate cancer and aggressive prostate cancer. Cancer Sci 2009; 100: 914-9.
35. Yokobori T, Mimori K, Ishii H, et al. Clinical significance of stanniocalcin 2 as a prognostic marker in gastric cancer. Ann Surg Oncol 2010; 17: 2601-7.
36. Law AYS, Lai KP, Ip CKM, et al. Epigenetic and HIF-1 regulation of stanniocalcin-2 expression in human cancer cells. Exp Cell Res 2008; 314: 1823-30.
37. Ito D, Walker JR, Thompson CS, et al. Characterization of Stanniocalcin 2, a novel target of the mammalian unfolded protein response with cytoprotective properties. Mol Cell Biol 2004; 24: 9456-69.
38. Wang H, Wu K, Sun Y, et al. STC2 is upregulated in hepatocellular carcinoma and promotes cell proliferation and migration in vitro. BMB Rep 2012; 45: 629-34.
39. Lin Q, Yun Z,. Impact of the hypoxic tumor microenvironment on the regulation of cancer stem cell characteristics. Cancer Biol Ther 2010; 9: 949-56.
40. Filatova A, Acker T, Garvalov BK,. The cancer stem cell niche(s): the crosstalk between glioma stem cells and their microenvironment. Biochimica et biophysica acta 2013; 1830: 2496-508.
41. Clevers H,. The cancer stem cell: premises, promises and challenges. Nat Med 2011; 17: 313-9.
42. Loupakis F, Schirripa M, Caparello C, et al. Histopathologic evaluation of liver metastases from colorectal cancer in patients treated with FOLFOXIRI plus bevacizumab. Brit J Cancer 2013; 108: 2549-56.