Expression of hypoxic marker carbonic anhydrase IX predicts poor prognosis in resectable hepatocellular carcinoma

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Huang, Wei Ju ^a,b   Jeng, Yung Ming ^a,c   Lai, Hong Shiee ^c   Fong, Iok U ^a   Sheu, Fang Yu Bonnie ^d   Lai, Po Lin ^c   Yuan, Ray Hwang ^c  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b HSIN SHENG COLLEGE OF MEDICAL CARE AND MANAGEMENT   (Taiwan)

^c NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

^d UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA FETOPROTEIN; CARBONATE DEHYDRATASE IX; CA9 PROTEIN, HUMAN; CARBONATE DEHYDRATASE; TUMOR ANTIGEN; TUMOR MARKER;

ADOLESCENT; ADULT; AGE; AGED; ARTICLE; CANCER PROGNOSIS; CANCER STAGING; CONTROLLED STUDY; CORRELATION ANALYSIS; DISEASE FREE SURVIVAL; FEMALE; GENDER; HUMAN; IMMUNOHISTOCHEMISTRY; LIVER CELL CARCINOMA; MAJOR CLINICAL STUDY; MALE; MULTIVARIATE ANALYSIS; OVERALL SURVIVAL; PROTEIN EXPRESSION; TUMOR VOLUME; CARCINOMA, HEPATOCELLULAR; CELL HYPOXIA; CYTOLOGY; DISEASE COURSE; GENE EXPRESSION REGULATION; LIVER; LIVER NEOPLASMS; METABOLISM; MIDDLE AGED; PATHOLOGY; PROGNOSIS; RECURRENT DISEASE; TUMOR INVASION; VERY ELDERLY; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; ANTIGENS, NEOPLASM; BIOMARKERS, TUMOR; CARBONIC ANHYDRASE IX; CARBONIC ANHYDRASES; CARCINOMA, HEPATOCELLULAR; CELL HYPOXIA; DISEASE PROGRESSION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LIVER; LIVER NEOPLASMS; MALE; MIDDLE AGED; NEOPLASM INVASIVENESS; NEOPLASM STAGING; PROGNOSIS; RECURRENCE; YOUNG ADULT;

EID: 84928911836     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0119181     Document Type: Article

References (50)

1. Befeler AS, Di Bisceglie AM. Hepatocellular carcinoma: diagnosis and treatment. Gastroenterology. 2002;122:1609-1619. PMID: 12016426
2. Schafer DF, Sorrell MF. Hepatocellular carcinoma. Lancet. 1999;353:1253-1257. PMID: 10217098
3. Pan HW, Ou YH, Peng SY, Liu SH, Lai PL, Lee PH, et al. Overexpression of osteopontin is associated with intrahepatic metastasis, early recurrence, and poorer prognosis of surgically resected hepatocellular carcinoma. Cancer. 2003;98:119-127. PMID: 12833464
4. Yang MH, Wu MZ, Chiou SH, Chen PM, Chang SY, Liu CJ, et al. Direct regulation of TWIST by HIF-1alpha promotes metastasis. Nat Cell Biol. 2008;10:295-305. doi: 10.1038/ncb1691 PMID: 18297062
5. Abaza M, Luqmani YA. The influence of pH and hypoxia on tumor metastasis. Expert Rev Anticancer Ther. 2013;13:1229-1242. doi: 10.1586/14737140.2013.843455 PMID: 24099530
6. Nurwidya F, Takahashi F, Minakata K, Murakami A, Takahashi K. From tumor hypoxia to cancer progression: the implications of hypoxia-inducible factor-1 expression in cancers. Anat Cell Biol. 2012;45:73-78. doi: 10.5115/acb.2012.45.2.73 PMID: 22822460
7. Semenza GL. HIF-1 and tumor progression: pathophysiology and therapeutics. Trends Mol Med. 2002;8:S62-67. PMID: 11927290
8. Sokkar P, Sathis V, Ramachandran M. Computational modeling on the recognition of the HRE motif by HIF-1: molecular docking and molecular dynamics studies. J Mol Model. 2012;18:1691-1700. doi: 10. 1007/s00894-011-1150-0 PMID: 21814878
9. Pastorek J, Pastorekova S, Callebaut I, Mornon JP, Zelnik V, Opavsky R, et al. 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. 1994;9:2877-2888. PMID: 8084592
10. Wykoff CC, Beasley NJ, Watson PH, Turner KJ, Pastorek J, Sibtain A, et al. Hypoxia-inducible expression of tumor-associated carbonic anhydrases. Cancer Res. 2000;60:7075-7083. PMID: 11156414
11. McDonald PC, Winum JY, Supuran CT, Dedhar S. Recent developments in targeting carbonic anhydrase IX for cancer therapeutics. Oncotarget. 2012;3:84-97. PMID: 22289741
12. Kaluz S, Kaluzová M, Liao SY, Lerman M, Stanbridge EJ. Transcriptional control of the tumor- and hypoxiamarker carbonic anhydrase 9: A one transcription factor (HIF-1) show? Biochim Biophys Acta. 2009;1795:167-172.
13. Ditte P, Dequiedt F, Svastova E, Hulikova A, Ohradanova-Repic A, Zatovicova M, et al. Phosphorylation of carbonic anhydrase IX controls its ability to mediate extracellular acidification in hypoxic tumors. Cancer Res. 2011;71:7558-7567. doi: 10.1158/0008-5472. CAN-11-2520 PMID: 22037869
14. Svastova E, Witarski W, Csaderova L, Kosik I, Skvarkova L, Hulikova A, et al. Carbonic anhydrase IX interacts with bicarbonate transporters in lamellipodia and increases cell migration via its catalytic domain. J Biol Chem. 2012;287:3392-3402. doi: 10.1074/jbc. M111.286062 PMID: 22170054
15. Swinson DE, Jones JL, Richardson D, Wykoff C, Turley H, Pastorek J, et al. Carbonic anhydrase IX expression, a novel surrogate marker of tumor hypoxia, is associated with a poor prognosis in non-smallcell lung cancer. J Clin Oncol. 2003;21:473-482. PMID: 12560438
16. Hussain SA, Ganesan R, Reynolds G, Gross L, Stevens A, Pastorek J, et al. Hypoxia-regulated carbonic anhydrase IX expression is associated with poor survival in patients with invasive breast cancer. Br J Cancer. 2007;96:104-109. PMID: 17213826
17. Troost EG, Bussink J, Kaanders JH, Van Eerd J, Peters JP, Rijken PF, et al. Comparison of different methods of CAIX quantification in relation to hypoxia in three human head and neck tumor lines. Radiother Oncol. 2005;76:194-199. PMID: 16024110
18. Hoskin PJ, Sibtain A, Daley FM, Wilson GD. GLUT1 and CAIX as intrinsic markers of hypoxia in bladder cancer: relationship with vascularity and proliferation as predictors of outcome of ARCON. Br J Cancer. 2003;89:1290-1297. PMID: 14520462
19. Haapasalo JA, Nordfors KM, Hilvo M, Rantala IJ, Soini Y, Parkkila AK, et al. Expression of carbonic anhydrase IX in astrocytic tumors predicts poor prognosis. Clin Cancer Res. 2006;12:473-477. PMID: 16428489
20. Loncaster JA, Harris AL, Davidson SE, Logue JP, Hunter RD, Wycoff CC, et al. Carbonic anhydrase (CA IX) expression, a potential new intrinsic marker of hypoxia: correlations with tumor oxygen measurements and prognosis in locally advanced carcinoma of the cervix. Cancer Res. 2001;61:6394-6399. PMID: 11522632
21. Driessen A, Landuyt W, Pastorekova S, Moons J, Goethals L, Haustermans K, et al. Expression of carbonic anhydrase IX (CA IX), a hypoxia-related protein, rather than vascular-endothelial growth factor (VEGF), a pro-angiogenic factor, correlates with an extremely poor prognosis in esophageal and gastric adenocarcinomas. Ann Surg. 2006;243:334-340. PMID: 16495697
22. Lee-Kong SA, Ruby JA, Chessin DB, Pucciarelli S, Shia J, Riedel ER, et al. Hypoxia-related proteins in patients with rectal cancer undergoing neoadjuvant combined modality therapy. Dis Colon Rectum. 2012;55:990-995. doi: 10.1097/DCR.0b013e31825bd80c PMID: 22874607
23. Måseide K, Kandel RA, Bell RS, Catton CN, O'Sullivan B, Wunder JS, et al. Carbonic anhydrase IX as a marker for poor prognosis in soft tissue sarcoma. Clin Cancer Res. 2004;10:4464-4471. PMID: 15240538
24. Liu Z, Yang Z, Jiang S, Zou Q, Yuan Y, Li J, et al. Paxillin and carbonic anhydrase IX are prognostic markers in gallbladder squamous cell/adenosquamous carcinomas and adenocarcinomas. Histopathology. 2014;64:921-934. doi: 10.1111/his.12341 PMID: 24354963
25. Yuan RH, Jeng YM, Chen HL, Hsieh FJ, Yang CY, Lee PH, et al. Opposite roles of human pancreatitisassociated protein and REG1A expression in hepatocellular carcinoma: association of pancreatitisassociated protein expression with low-stage hepatocellular carcinoma, beta-catenin mutation, and favorable prognosis. Clin Cancer Res. 2005;11:2568-2575. PMID: 15814635
26. Yuan RH, Jeng YM, Chen HL, Lai PL, Pan HW, Hsieh FJ, et al. Stathmin overexpression cooperates with p53 mutation and osteopontin overexpression, and is associated with tumour progression, early recurrence, and poor prognosis in hepatocellular carcinoma. J Pathol. 2006;209:549-558. PMID: 16739096
27. Edmondson HA, Steiner PE. Primary carcinoma of the liver: a study of 100 cases among 48, 900 necropsies. Cancer. 1954;7:462-503. PMID: 13160935
28. Edge SB, Byrd DR, Compton CC, Fritz AG, Greene FL, Trotti A, editors. AJCC cancer staging manual. 7th ed. New York, NY: Springer, 2010.
29. Yuan RH, Lai HS, Hsu HC, Lai PL, Jeng YM. Expression of Bile Duct Transcription Factor HNF1β Predicts Early Tumor Recurrence and Is a Stage-Independent Prognostic Factor in Hepatocellular Carcinoma. J Gastrointest Surg. 2014;18:1784-1794. doi: 10.1007/s11605-014-2596-z PMID: 25052070
30. Peng SY, Chen WJ, Lai PL, Jeng YM, Sheu JC, Hsu HC. High alpha-fetoprotein level correlates with high stage, early recurrence and poor prognosis of hepatocellular carcinoma: significance of hepatitis virus infection, age, p53 and beta-catenin mutations. Int J Cancer. 2004;112:44-50. PMID: 15305374
31. Rosmorduc O, Housset C. Hypoxia: a link between fibrogenesis, angiogenesis, and carcinogenesis in liver disease. Semin Liver Dis. 2010;30:258-270. doi: 10.1055/s-0030-1255355 PMID: 20665378
32. Dong ZZ, Yao M, Wang L, Wu W, Gu X, Yao DF. Hypoxia-inducible factor-1alpha: molecular-targeted therapy for hepatocellular carcinoma. Mini Rev Med Chem. 2013;13:1295-1304. PMID: 22512580
33. Li S, Yao D, Wang L, Wu W, Qiu L, Yao M, et al. Expression characteristics of hypoxia-inducible factor-1α and its clinical values in diagnosis and prognosis of hepatocellular carcinoma. Hepat Mon. 2011;11:821-828. doi: 10.5812/kowsar.1735143X.771 PMID: 22224081
34. Tanaka M, Masaki Y, Tanaka K, Miyazaki M, Kato M, Sugimoto R, et al. Reduction of fatty acid oxidation and responses to hypoxia correlate with the progression of de-differentiation in HCC. Mol Med Rep. 2013;7:365-370. doi: 10.3892/mmr.2012.1201 PMID: 23178736
35. Takacova M, Bullova P, Simko V, Skvarkova L, Poturnajova M, Feketeova L, et al. Expression pattern of carbonic anhydrase IX in Medullary thyroid carcinoma supports a role for RET-mediated activation of the HIF pathway. Am J Pathol. 2014;184:953-965. doi: 10.1016/j.ajpath.2014.01.002 PMID: 24518567
36. Genega EM, Ghebremichael M, Najarian R, Fu Y, Wang Y, Argani P, et al. Carbonic anhydrase IX expression in renal neoplasms: correlation with tumor type and grade. Am J Clin Pathol. 2010;134:873-879. doi: 10.1309/AJCPPPR57HNJMSLZ PMID: 21088149
37. Tan EY, Yan M, Campo L, Han C, Takano E, Turley H, et al. The key hypoxia regulated gene CAIX is upregulated in basal-like breast tumours and is associated with resistance to chemotherapy. Br J Cancer. 2009;100:405-411. doi: 10.1038/sj.bjc.6604844 PMID: 19165203
38. Luong-Player A, Liu H, Wang HL, Lin F. Immunohistochemical reevaluation of carbonic anhydrase IX (CA IX) expression in tumors and normal tissues. Am J Clin Pathol. 2014;141:219-225. doi: 10.1309/AJCPVJDS28KNYZLD PMID: 24436269
39. Yu SJ, Yoon JH, Lee JH, Myung SJ, Jang ES, Kwak MS, et al. Inhibition of hypoxia-inducible carbonic anhydrase-IX enhances hexokinase II inhibitor-induced hepatocellular carcinoma cell apoptosis. Acta Pharmacol Sin. 2011;32:912-920. doi: 10.1038/aps.2011.24 PMID: 21666701
40. Fiaschi T, Giannoni E, Taddei ML, Cirri P, Marini A, Pintus G, et al. Carbonic anhydrase IX from cancerassociated fibroblasts drives epithelial-mesenchymal transition in prostate carcinoma cells. Cell Cycle. 2013;12:1791-1801. doi: 10.4161/cc.24902 PMID: 23656776
41. Lock FE, McDonald PC, Lou Y, Serrano I, Chafe SC, Ostlund C, et al. Targeting carbonic anhydrase IX depletes breast cancer stem cells within the hypoxic niche. Oncogene. 2013;32:5210-5219. doi: 10. 1038/onc.2012.550 PMID: 23208505
42. Brennan DJ, Jirstrom K, Kronblad A, Millikan RC, Landberg G, Duffy MJ, et al. CA IX is an independent prognostic marker in premenopausal breast cancer patients with one to three positive lymph nodes and a putative marker of radiation resistance. Clin Cancer Res. 2006;12:6421-6431. PMID: 17085655
43. Liao SY, Darcy KM, Randall LM, Tian C, Monk BJ, Burger RA, et al. Prognostic relevance of carbonic anhydrase-IX in high-risk, early-stage cervical cancer: a Gynecologic Oncology Group study. Gynecol Oncol. 2010;116:452-458. doi: 10.1016/j.ygyno. 2009.10.062 PMID: 19913895
44. Poon RT, Fan ST, Ng IO, Lo CM, Liu CL, Wong J. Different risk factors and prognosis for early and late intrahepatic recurrence after resection of hepatocellular carcinoma. Cancer. 2000;89:500-507. PMID: 10931448
45. Peng SY, Ou YH, Chen WJ, Li HY, Liu SH, Pan HW, et al. Aberrant expressions of annexin A10 short isoform, osteopontin and alpha-fetoprotein at chromosome 4q cooperatively contribute to progression and poor prognosis of hepatocellular carcinoma. Int J Oncol. 2005;26:1053-1061. PMID: 15754002
46. Bache M, Reddemann R, Said HM, Holzhausen HJ, Taubert H, Becker A, et al. Immunohistochemical detection of osteopontin in advanced head-and-neck cancer: prognostic role and correlation with oxygen electrode measurements, hypoxia-inducible-factor-1alpha-related markers, and hemoglobin levels. Int J Radiat Oncol Biol Phys. 2006;66:1481-1487. PMID: 17056190
47. Eckert AW, Lautner MH, Schütze A, Bolte K, Bache M, Kappler M, et al. Co-expression of Hif1alpha and CAIX is associated with poor prognosis in oral squamous cell carcinoma patients. J Oral Pathol Med. 2010;39:313-317. doi: 10.1111/j.1600-0714.2009.00829.x PMID: 19780905
48. Farinati F, Sergio A, Giacomin A, Di Nolfo MA, Del Poggio P, Benvegnù L, et al. Is female sex a significant favorable prognostic factor in hepatocellular carcinoma? Eur J Gastroenterol Hepatol. 2009;21:1212-1218. doi: 10.1097/MEG.0b013e32831a86f8 PMID: 19465859
49. Cabibbo G, Enea M, Attanasio M, Bruix J, Craxì A, Cammà C. A meta-analysis of survival rates of untreated patients in randomized clinical trials of hepatocellular carcinoma. Hepatology. 2010;51:1274-1283. doi: 10.1002/hep. 23485 PMID: 20112254
50. Giannini EG, Farinati F, Ciccarese F, Pecorelli A, Rapaccini GL, Di Marco M, et al. Prognosis of untreated hepatocellular carcinoma. Hepatology. 2015;61:184-90. doi: 10.1002/hep. 27443 PMID: 25234419