Stromal expression of hypoxia regulated proteins is an adverse prognostic factor in colorectal carcinomas

Cellular Oncology

Volumn 29, Issue 3, 2007, Pages 229-240

  Cleven, Arjen H G ^a   Van Engeland, Manon ^a   Wouters, Bradly G ^a   De Bruïne, Adriaan P ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

Epithelial expression; Hypoxia; Patient outcome; Stromal expression

Indexed keywords

CARBONATE DEHYDRATASE IX; GLUCOSE TRANSPORTER 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 2ALPHA;

AGED; ARTICLE; COLORECTAL CARCINOMA; CONTROLLED STUDY; CORRELATION ANALYSIS; EPITHELIUM TUMOR; FEMALE; HUMAN; HUMAN TISSUE; HYPOXIA; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; PROGNOSIS; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; STATISTICAL SIGNIFICANCE; STROMA; STROMA CELL; SURVIVAL RATE;

ADULT; AGED; AGED, 80 AND OVER; ANOXIA; ANTIGENS, NEOPLASM; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CARBONIC ANHYDRASES; COLORECTAL NEOPLASMS; EPITHELIAL CELLS; FEMALE; GLUCOSE TRANSPORTER TYPE 1; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MALE; MIDDLE AGED; MULTIVARIATE ANALYSIS; PROGNOSIS; PROPORTIONAL HAZARDS MODELS; STROMAL CELLS; SURVIVAL ANALYSIS; TUMOR MARKERS, BIOLOGICAL;

EID: 34249815207     PISSN: 15705870     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (54)

1. E.O. Aboagye, R.J. Maxwell, A.B. Kelson, M. Tracy, A.D. Lewis, M.A. Graham, M.R. Horsman, J.R. Griffiths and P. Workman, Preclinical evaluation of the fluorinated 2-nitroimidazole N-(2-hydroxy-3,3,3-trifluoropropyl)-2-(2-nitro- 1-imidazolyl) acetamide (SR-4554) as a probe for the measurement of tumor hypoxia, Cancer Res. 57 (1997), 3314-3318.
2. N.J.P. Beasley, C.C. Wykoff, P.H. Watson, R.D. Leek, H. Turley, K. Gatter, J. Pastorek, G.J. Cox, P. Ratcliffe and A.L. Harris, Carbonic anhydrase IX, an endogenous hypoxia marker, expression in head and neck squamous cell carcinoma and its relationship to hypoxia, necrosis, and microvessel density, Cancer Res. 61 (2001), 5262-5267.
3. J. Bussink, J.H.A.M. Kaanders and A.J. van der Kogel, Tumor hypoxia at the micro-regional level: clinical relevance and predictive value of exogenous and endogenous hypoxic cell markers, Radiother. Oncol. 67 (2003), 3-15.
4. D.J. Ceradini, A.R. Kulkarni, M.J. Callaghan, O.M. Tepper, N. Bastidas, M.E. Kleinman, J.M. Capla, R.D. Galiano, J.P. Levine and G.C. Gurtner, Progenitor cell trafficking is regulated by hypoxia gradients through HIF-1 induction of SDF-1, Nat. Med. 10 (2004), 858-864.
5. C.G. Colpaert, P.B. Vermeulen, S.B. Fox, A.L. Harris, L.Y. Dirix and E.A. van Marck, The presence of a fibrotic focus in invasive breast carcinoma correlates with the expression of carbonic anhydrase IX and is a marker of hypoxia and poor prognosis, Breast Cancer Res. Treat. 81 (2003), 137-147.
6. A.E. Greijer, M.C. de Jong, G.L. Scheffer, A. Shvarts, P.J. van Diest, E. van der Wall, Hypoxia-induced acidification causes mitoxantrone resistance not mediated by drug transporters in human breast cancer cells, Cell. Oncol. 27 (2005), 43-49.
7. R.S. Haber, A. Rathan, K.R. Weiser, P. A., S.H. Itzkowitz, C. Bodian, G. Slater, A. Weiss and D.E. Burstein, GLUT1 Glucose Transporter Expression in Colorectal Carcinoma, American Cancer Society (1998), 34-39.
8. M. Hockel and P. Vaupel, Tumor hypoxia: definitions and current clinical, biologic, and molecular aspects, J. Natl. Cancer Inst. 93 (2001), 266-276.
9. P.J. Hoskin, A. Sibtain, F.M. Daley and G.D. Wilson, GLUT1 and CA9 as intrinsic markers of hypoxia in bladder cancer: relationship with vascularity and proliferation as predictors of outcome in ARCON, Br. J. Cancer 89 (2003), 1290-1297.
10. M. Hu, J. Yao, L. Cai, K.E. Bachman, F. van den Brule, V. Velculescu and K. Polyak, Distinct epigenetic changes in the stromal cells of breast cancers, Nat. Genet. 37 (2005), 899-905.
11. N. Ingram and C.D. Porter, Transcriptional targeting of acute hypoxia in the tumour stroma is a novel and viable strategy for cancer gene therapy, Gene Ther. 12 (2005), 1058-1069.
12. K. Ishiguro, T. Yoshida, H. Yagishita, Y. Numata and T. Okayasu, Epithelial and stromal genetic instability contributes to genesis of colorectal adenomas, Gut 55 (2006) 695-702.
13. M.S. Joesting, S. Perrin, B. Elenbaas, S.E. Fawell, J.S. Rubin, O.E. Franco, S.W. Hayward, G.R. Cunha and P.C. Marker, Identification of SFRP1 as a candidate mediator of stromal-to-epithelial signaling in prostate cancer, Cancer Res. 65 (2005), 10423-10430.
14. A.C. Koong, N.C. Denko, K.M. Hudson, C. Schindler, L. Swiersz, C. Koch, S. Evans, H. Ibrahim, Q.T. Le, D.J. Terris and A.J. Giaccia, Candidate genes for the hypoxic tumor phenotype, Cancer Res. 60 (2000), 883-887.
15. M.I. Koukourakis, A. Giatromanolaki, R.A. Brekken, E. Sivridis, K.C. Gatter, A.L. Harris and E.H. Sage, Enhanced expression of SPARC/osteonectin in the tumor-associated stroma of non-small cell lung cancer is corrrelated with markers of hypoxia/acidity and with poor prognosis of patients, Cancer Res. 63 (2003), 5376-5380.
16. M.I. Koukourakis, A. Giatromanolaki, A.L. Harris and E. Sivridis, Comparison of metabolic pathways between cancer cells and stromal cells in colorectal carcinomas: a metabolic survival role for tumor-associated stroma, Cancer Res. 66 (2006), 632-637.
17. M.I. Koukourakis, A. Giatromanolaki, A. Polychronidis, C. Simopoulos, K.C. Gatter, A.L. Harris and E. Sivridis, Endogenous markers of hypoxia/anaerobic metabolism and anemia in primary colorectal cancer, Cancer Sci. 97 (2006), 582-588.
18. M.I. Koukourakis, A. Giatromanolaki, E. Sivridis, K.C. Gatter and A.L. Harris, Lactate dehydrogenase 5 expression in operable colorectal cancer: strong association with survival and activated vascular endothelial growth factor pathway - a report of the Tumour Angiogenesis Research Group, J. Clin. Oncol. 24 (2006), 4301-4308.
19. T. Kuwai, Y. Kitadai, S. Tanaka, S. Onogowa, N. Matsutani, E. Kaio, M. Ito and K. Chayama, Expression of hypoxia-inducible factor-1 alpha is associated with tumor vascularisation in human colorectal carcinoma, Int. J. Cancer 105 (2003), 176-181.
20. J.A. Loncaster, A.L. Harris, S.E. Davidson, J.P. Logue, R.D. Hunter, C.C. Wykoff, J. Pastorek, P. Ratcliffe, I.J. Stratford and C.M.L. West, Carbonic anhydrase (CAIX) expression, a potential new intrinsic marker of hypoxia: correlations with tumor oxygen measurements and prognosis in locally advanced carcinoma of the cervix, Cancer Res. 61 (2001), 6394-6399.
21. C. Lussier, J. Sodek and J. Beaulieu, Expression of SPARC/osteonectin/ BM40 in the human gut: predominance in the stroma of the remodeling distal intestine, J. Cell. Biochem. 81 (2001), 463-476.
22. M.L. Macheda, S. Rogers and J.D. Best, Molecular and cellular regulation of glucose transporter (GLUT) proteins in cancer, J. Cell. Physiol. 202 (2005), 654-662.
23. C. Menon and D.L. Fraker, Tumor oxygenation status as a prognostic marker, Cancer Lett. 221 (2005), 225-235.
24. M.M. Mueller and N.E. Fusenig, Friends or foes-bipolar effects of the tumour stroma in cancer, Nat. Rev. Cancer 4 (2004), 839-849.
25. R. Opavsky, S. Pastorekova, V. Zelnik, A. Gibadulinova, E.J. Stanbridge, J. Zavada, R. Kettmann and J. Pastorek, Human MN/CA9 gene, a novel member of carbonic anhydrase family: structure and exon to protein domain relationships, Genomics 33 (1996), 480-487.
26. A. Orimo, P.B. Gupta, D.C. Sgroi, F. Arenzana-Seisdedos, T. Delaunay, R. Naeem, V.J. Carey, A.L. Richardson and R.A. Weinberg, Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion, Cell 121 (2005), 335-348.
27. S.K. Park, A.M. Dadak, V.H. Haase, L. Fontana, A.J. Giaccia and R.S. Johnson, Hypoxia-induced gene expression occurs solely through the action of hypoxia-inducible factor 1 alpha (HIF-1alpha): role of cytoplasmic trapping of HIF-2 alpha, Mol. Cell. Biol. 23 (2003), 4959-4971.
28. J. Pastorek, S. Pastorekova, I. Callebaut, J.P. Mornon, V. Zelnik, R. Opavsky, M. Zat'ovicova, S. Liao, D. Portetelle and E.J. Stanbridge, Cloning and characterization of MN, a human tumor-associated protein with a domain homologous to carbonic anhydrase and a putative helix-loop-helix DNA binding segment, Oncogene 9 (1994), 2877-2888.
29. L. Peduto, V.E. Reuter, A. Sehara-Fujisawa, D.R. Shaffer, H.I. Scher and C.P. Blobel, ADAM12 is highly expressed in carcinoma-associated stroma and is required for mouse prostate tumor progression, Oncogene 25 (2006), 5462-5466.
30. L. Poellinger and R.S. Johnson, HIF-1 and hypoxic response: the plot thickens, Curr. Opin. Genet. Dev. 14 (2004), 81-85.
31. J. Pouyssegur, F. Dayan and N.M. Mazure, Hypoxia signalling in cancer and approaches to enforce tumour regression, Nature 441 (2006), 437-443.
32. R. Ravi, B. Mookerjee, Z.W. Bhujwalla, C.H. Sutter, D. Artemov, Q. Zeng, L.E. Dillehay, A. Madan, G.L. Semenza and A. Bedi, Regulation of tumor angiogenesis by p53-induced degradation of hypoxia-inducible factor 1 alpha, Genes Dev. 14 (2000), 34-44.
33. N. Robertson, C. Potter and A.L. Harris, Role of carbonic anhydrase IX in human tumor cell growth, survival, and invasion, Cancer Res. 64 (2004), 6160-6165.
34. L. Roncucci, R. Fante, L. Losi, C. Di Gregorio, A. Micheli, P. Benatti, N. Madenis, D. Ganazzi, M.T. Cassinadri, P. Lauriola and M. Ponz de Leon, Survival for colon and rectal cancer in a population-based cancer registry, Eur. J. Cancer 32 (1996), 295-302.
35. J. Saarnio, S. Parkkila, A. Parkkila, K. Haukipuro, S. Pastorekova, J. Pastorek, M.I. Kairaluoma and T.J. Karttunen, Immunohistochemical study of colorectal tumors for expression of a novel transmembrane carbonic anhydrase, MN/CA IX, with potential value as a marker of cell proliferation, Am. J. Pathol. 153 (1998), 279-285.
36. M. Sakashita, N. Aoyama, R. Minami, S. Maekawa, K. Kuroda, D. Shirasaka, T. Ichihara, Y. Kuroda, S. Maeda and M. Kasuga, Glut1 expression in T1 and T2 stage colorectal carcinomas: its relationship to clinicopathological features, Eur. J. Cancer 37 (2001), 204-209.
37. C. Schmaltz, P. Harrigan Hardenbergh, A. Wells and D.E. Fisher, Regulation of proliferation-survival decisions during tumor cell hypoxia, Mol. Cell. Biol. 18 (1998), 2845-2854.
38. A.M. Shannon, D.J. Bouchier-Hayes, C.M. Condron and D. Toomey, Tumour hypoxia, chemotherapeutic resistance and hypoxia-related therapies, Cancer Treat. Rev. 29 (2003), 297-307.
39. E. Sivridis, A. Giatromanolaki, K. Gatter, A.L. Harris and M.I. Koukourakis, Association of hypoxia-inducible factors 1 alpha and 2 alpha with activated angiogenic pathways and prognosis in patients with endometrial carcinoma, Cancer 95 (2002), 1055-1063.
40. E. Sivridis, A. Giatromanolaki and M.I. Koukourakis, Proliferating fibroblasts at the invading tumour edge of colorectal adenocarcinomas are associated with endogenous markers of hypoxia, acidity, and oxidative stress, J. Clin. Pathol. 58 (2005), 1033-1038.
41. S. Sobhanifar, C. Aquino-Parsons, E.J. Stanbridge and P. Olive, Reduced Expression of hypoxia-inducible factor-1 alpha in perinecrotic regions of solid tumors, Cancer Res. 65 (2005), 7259-7266.
42. D.E.B. Swinson, J.L. Jones, D. Richardson, C. Wykoff, H. Turley, J. Pastorek, N. Taub, A.L. Harris and K.J. O'Byrne, Carbonic anhydrase IX expression, a novel surrogate marker of tumor hypoxia, is associated with poor prognosis in non-small-cell lung cancer, J. Clin. Oncol. 21 (2003), 473-482.
43. C. Tan, R.G. Noronha de, A.J. Roecker, B. Pyrzynska, F. Khwaja, Z. Zhang, H. Zhang, Q. Teng, A.C. Nicholson, P. Giannakakou, W. Zhou, J.J. Olson, M.M. Pereira, K.C. Nicolaou and E.G. van Meir, Identification of a novel small-molecule inhibitor of the hypoxia-inducible factor 1 pathway, Cancer Res. 65 (2005), 605-612.
44. K.J. Turner, J.P. Crew, C.C. Wykoff, P.H. Watson, R. Poulsom, J. Pastorek, P.J. Ratcliffe, D. Cranston and A.L. Harris, The hypoxia-inducible genes VEGF and CA9 are differentially regulated in superficial vs invasive bladder cancer, Br. J. Cancer 86 (2002), 1276-1282.
45. T. Uchida, F. Rossignol, M.A. Matthay, R.Mounier, S. Couette, E. Clottes and C. Clerici, Prolonged hypoxia differentially regulates hypoxia-inducible factor (HIF)-1alpha and HIF-2 alpha expression in lung epithelial cells, J. Biol. Chem. 279 (2004), 14871-14878.
46. G.J. van der Bij, S.J. Oosterling, S. Meijer, R.H. Beelen and M. van Egmond, The role of macrophages in tumor development, Cell. Oncol. 27 (2005), 203-213.
47. 2 tension measurements, Cancer Res. 51 (1991), 3316-3322.
48. S. Vosseler, N. Mirancea, P. Bohlen, M.M. Mueller and N.E. Fusenig, Angiogenesis Inhibition by vascular endothelial growth factor receptor-2 blockade reduces stromal matrix metalloproteinase expression, normalizes stromal tissue, and reverts epithelial tumor phenotype in surface heterotransplants, Cancer Res. 65 (2005), 1294-1305.
49. T. Wiggers, J. Jeekel, J.W. Arends, A.P. Brinkhorst, H.M. Kluck, C.I. Luyck, J.D.K. Munting, J.A.C.M. Povel, A.P.M. Rutten, A. Volovics and J.M. Greep, No-touch isolation technique in colon cancer: a controlled prospective trial, Br. J. Surg. 75 (1988), 409-415.
50. B.G. Wouters, M. Koritzinsky, R.K. Chiu, J. Theys, J. Buijsen and P. Lambin, Modulation of cell death in the tumor microenvironment, Semin. Radiat. Oncol. 13 (2003), 31-41.
51. B.G. Wouters, T. Van den Beucken, M.G. Magagnin, P. Lambin and C. Koumenis, Targeting hypoxia tolerance in cancer, Drug Resist. Updat. 7 (2004), 25-49.
52. C.C. Wykoff, N.J. Beasley, P.H. Watson, K.J. Turner, J. Pastorek, A. Sibtain, G.D. Wilson, H. Turley, K.L. Talks, P.H. Maxwell, C.W. Pugh, P.J. Ratcliffe and A.L. Harris, Hypoxiainducible expression of tumor-associated carbonic anhydrases, Cancer Res. 60 (2000), 7075-7083.
53. H. Yoshimura, D.K. Dhar, H. Kohno, H. Kubota, F. Toshiyuki, S. Ueda, S. Kinugasa, M. Tachibana and N. Nagasue, Prognostic impact of hypoxia-inducible factors 1 alpha and 2 alpha in colorectal cancer patients: correlation with tumor angiogenesis and cyclooxygenase-2 expression, Clin. Cancer Res. 10 (2004), 8554-8560.
54. M. Younes, L.V. Lechago and J. Lechago, Overexpression of the human erytrocyte glucose transporter occurs as a late event in human colorectal carginogenesis and is associated with an increased incidence of lymph node metastases, Clin. Cancer Res. 2 (1996), 1151-1154.