Arginase II Expressed in Cancer-Associated Fibroblasts Indicates Tissue Hypoxia and Predicts Poor Outcome in Patients with Pancreatic Cancer

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Ino, Yoshinori ^a   Yamazaki Itoh, Rie ^a   Oguro, Seiji ^a   Shimada, Kazuaki ^b   Kosuge, Tomoo ^b   Zavada, Jan ^c   Kanai, Yae ^a   Hiraoka, Nobuyoshi ^a  

^a NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

^b NATIONAL CANCER CENTER HOSPITAL   (Japan)

^c INSTITUTE OF ORGANIC CHEMISTRY AND BIOCHEMISTRY   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; ARGINASE; ARGINASE II; CARBONATE DEHYDRATASE IX; GLUCOSE TRANSPORTER 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; UNCLASSIFIED DRUG;

ADULT; AGED; ARTICLE; CANCER LOCALIZATION; CANCER PROGNOSIS; CANCER SURVIVAL; DISEASE ASSOCIATION; DISEASE FREE SURVIVAL; ENZYME ACTIVITY; ENZYME LOCALIZATION; FEMALE; FIBROBLAST; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPOXEMIA; IMMUNE RESPONSE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MALE; OVERALL SURVIVAL; PANCREAS CARCINOMA; PREDICTION; PROTEIN EXPRESSION; SURVIVAL RATE;

ADULT; AGED; AGED, 80 AND OVER; ARGINASE; CARCINOMA, PANCREATIC DUCTAL; CELL HYPOXIA; FEMALE; FIBROBLASTS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; MIDDLE AGED; NECROSIS; PANCREATIC NEOPLASMS; PROGNOSIS;

EID: 84873735398     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0055146     Document Type: Article

References (40)

1. Hanahan D, Weinberg RA, (2011) Hallmarks of cancer: the next generation. Cell 144: 646-674.
2. Munder M, (2009) Arginase: an emerging key player in the mammalian immune system. Br J Pharmacol 158: 638-651.
3. Rodriguez PC, Zea AH, DeSalvo J, Culotta KS, Zabaleta J, et al. (2003) L-arginine consumption by macrophages modulates the expression of CD3 zeta chain in T lymphocytes. J Immunol 171: 1232-1239.
4. Morris SM Jr, (2009) Recent advances in arginine metabolism: roles and regulation of the arginases. Br J Pharmacol 157: 922-930.
5. Bronte V, Kasic T, Gri G, Gallana K, Borsellino G, et al. (2005) Boosting antitumor responses of T lymphocytes infiltrating human prostate cancers. J Exp Med 201: 1257-1268.
6. Rotondo R, Mastracci L, Piazza T, Barisione G, Fabbi M, et al. (2008) Arginase 2 is expressed by human lung cancer, but it neither induces immune suppression, nor affects disease progression. Int J Cancer 123: 1108-1116.
7. Siegel R, Ward E, Brawley O, Jemal A, (2011) Cancer statistics, 2011: the impact of eliminating socioeconomic and racial disparities on premature cancer deaths. CA Cancer J Clin 61: 212-236.
8. Center for Cancer Control and Information Services, National Cancer Center J (2009) Cancer Statistics in Japan.
9. Hruban RH, Boffetta P, Hiraoka N, Iacobuzio-Donahue C, Kato Y, et al. (2010) Ductal adenocarcinoma of the pancreas. In: Bosman FT, Carneiro F, Hruban RH, Theise ND, editors. World Health Organization Classification of Tumours Pathology & Genetics Tumours of the Digestive System. 4th ed. Lyon: IARCPress. 281-291.
10. Hruban RH, Pitman MB, Klimstra DS (2007) Ductal adenocarcinoma. In: Hruban RH, Pitman MB, Klimstra DS, editors. AFIP Atlas of Tumor Pathology Tumors of the pancreas. 4th ed. Washington, DC.: ARP Press. 111-164.
11. Lim JE, Chien MW, Earle CC, (2003) Prognostic factors following curative resection for pancreatic adenocarcinoma: a population-based, linked database analysis of 396 patients. Ann Surg 237: 74-85.
12. Philip PA, Mooney M, Jaffe D, Eckhardt G, Moore M, et al. (2009) Consensus report of the national cancer institute clinical trials planning meeting on pancreas cancer treatment. J Clin Oncol 27: 5660-5669.
13. Wenger RH, Stiehl DP, Camenisch G, (2005) Integration of oxygen signaling at the consensus HRE. Sci STKE 2005: re12.
14. Albina JE, Henry WL Jr, Mastrofrancesco B, Martin BA, Reichner JS, (1995) Macrophage activation by culture in an anoxic environment. J Immunol 155: 4391-4396.
15. Louis CA, Reichner JS, Henry WL Jr, Mastrofrancesco B, Gotoh T, et al. (1998) Distinct arginase isoforms expressed in primary and transformed macrophages: regulation by oxygen tension. Am J Physiol 274: R775-782.
16. Clarkson AN, Liu H, Rahman R, Jackson DM, Appleton I, et al. (2005) Clomethiazole: mechanisms underlying lasting neuroprotection following hypoxia-ischemia. FASEB J 19: 1036-1038.
17. Chen B, Calvert AE, Cui H, Nelin LD, (2009) Hypoxia promotes human pulmonary artery smooth muscle cell proliferation through induction of arginase. Am J Physiol Lung Cell Mol Physiol 297: L1151-1159.
18. Krotova K, Patel JM, Block ER, Zharikov S, (2010) Hypoxic upregulation of arginase II in human lung endothelial cells. Am J Physiol Cell Physiol 299: C1541-1548.
19. Toby IT, Chicoine LG, Cui H, Chen B, Nelin LD, (2010) Hypoxia-induced proliferation of human pulmonary microvascular endothelial cells depends on epidermal growth factor receptor tyrosine kinase activation. Am J Physiol Lung Cell Mol Physiol 298: L600-606.
20. Gerner EW, Meyskens FL Jr, (2004) Polyamines and cancer: old molecules, new understanding. Nat Rev Cancer 4: 781-792.
21. Wu G, Morris SM Jr, (1998) Arginine metabolism: nitric oxide and beyond. Biochem J 336 (Pt 1): 1-17.
22. Li H, Meininger CJ, Hawker JR Jr, Haynes TE, Kepka-Lenhart D, et al. (2001) Regulatory role of arginase I and II in nitric oxide, polyamine, and proline syntheses in endothelial cells. Am J Physiol Endocrinol Metab 280: E75-82.
23. Hasebe T, Tsuda H, Hirohashi S, Shimosato Y, Iwai M, et al. (1996) Fibrotic focus in invasive ductal carcinoma: an indicator of high tumor aggressiveness. Jpn J Cancer Res 87: 385-394.
24. Sica A, Melillo G, Varesio L, (2011) Hypoxia: a double-edged sword of immunity. J Mol Med (Berl) 89: 657-665.
25. Sica A, Bronte V, (2007) Altered macrophage differentiation and immune dysfunction in tumor development. J Clin Invest 117: 1155-1166.
26. Gabrilovich DI, Nagaraj S, (2009) Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 9: 162-174.
27. Ochoa AC, Zea AH, Hernandez C, Rodriguez PC (2007) Arginase, prostaglandins, and myeloid-derived suppressor cells in renal cell carcinoma. Clinical Cancer Research 13: 721 s-726 s.
28. Semenza GL, (2006) Development of novel therapeutic strategies that target HIF-1. Expert Opin Ther Targets 10: 267-280.
29. Grothey A, Galanis E, (2009) Targeting angiogenesis: progress with anti-VEGF treatment with large molecules. Nat Rev Clin Oncol 6: 507-518.
30. Semenza GL, (2009) HIF-1 inhibitors for cancer therapy: from gene expression to drug discovery. Curr Pharm Des 15: 3839-3843.
31. Hiraoka N, Ino Y, Sekine S, Tsuda H, Shimada K, et al. (2010) Tumour necrosis is a postoperative prognostic marker for pancreatic cancer patients with a high interobserver reproducibility in histological evaluation. British Journal of Cancer 103: 1057-1065.
32. Sessa C, Guibal A, Del Conte G, Ruegg C, (2008) Biomarkers of angiogenesis for the development of antiangiogenic therapies in oncology: tools or decorations? Nat Clin Pract Oncol 5: 378-391.
33. Sobin LH, Gospodarowicz MK, Wittekind C (2009) UICC TNM Atlas. Hoboken, NJ: Wiley-Blackwell.
34. Japan-Pancreas-Society (2003) Classification of Pancreatic Cancer. Tokyo, Japan: Kanehara.
35. Hiraoka N, Onozato K, Kosuge T, Hirohashi S, (2006) Prevalence of FOXP3+ regulatory T cells increases during the progression of pancreatic ductal adenocarcinoma and its premalignant lesions. Clinical Cancer Research 12: 5423-5434.
36. Pastorekova S, Zavadova Z, Kostal M, Babusikova O, Zavada J, (1992) A novel quasi-viral agent, MaTu, is a two-component system. Virology 187: 620-626.
37. Zavada J, Zavadova Z, Pastorek J, Biesova Z, Jezek J, et al. (2000) Human tumour-associated cell adhesion protein MN/CA IX: identification of M75 epitope and of the region mediating cell adhesion. British Journal of Cancer 82: 1808-1813.
38. Takahashi Y, Akishima-Fukasawa Y, Kobayashi N, Sano T, Kosuge T, et al. (2007) Prognostic value of tumor architecture, tumor-associated vascular characteristics, and expression of angiogenic molecules in pancreatic endocrine tumors. Clinical Cancer Research 13: 187-196.
39. Okami J, Simeone DM, Logsdon CD, (2004) Silencing of the hypoxia-inducible cell death protein BNIP3 in pancreatic cancer. Cancer Res 64: 5338-5346.
40. Hiraoka N, Yamazaki-Itoh R, Ino Y, Mizuguchi Y, Yamada T, et al. (2011) CXCL17 and ICAM2 are associated with a potential anti-tumor immune response in early intraepithelial stages of human pancreatic carcinogenesis. Gastroenterology 140: 310-321.