Strong Expression of Polypeptide N-acetylgalactosaminyltransferase 3 Independently Predicts Shortened Disease-free Survival in Patients with Early Stage Oral Squamous Cell Carcinoma

Overview

Journal Tumour Biol

Publisher Sage Publications

Specialty Oncology

Date 2015 Aug 23

PMID 26296622

Citations 11

Authors

Yoshikazu Harada

Hiroto Izumi

Hirotsugu Noguchi

Akihiro Kuma

Yuichiro Kawatsu

Tomoko Kimura

Shohei Kitada

Hidetaka Uramoto

Ke-Yong Wang

Yasuyuki Sasaguri

Hiroshi Hijioka

Akihiko Miyawaki

Ryoichi Oya

Toshiyuki Nakayama

Kimitoshi Kohno

Sohsuke Yamada

Affiliations

Soon will be listed here.

Abstract

The polypeptide N-acetylgalactosaminyltransferase (GalNAc-Ts) family of enzymes regulates the critical initial steps of mucin-type O-glycosylation. Among GalNAc-Ts that may significantly influence cancer biology, thus affecting cell differentiation, adhesion, invasion, and/or metastasis, GalNAc-T3 exhibits a high expression in several human cancers, closely associated with tumor progression and a poor prognosis. However, the expression pattern of GalNAc-T3 in oral squamous cell carcinoma (OSCC) remains obscure. Since postoperative recurrence of even early stage OSCC (ESOSCC) occurs at an early phase, significantly affecting their clinical course and worse outcome, the identification of clinically significant accurate biomarkers is needed. Therefore, we investigated the correlation between the immunohistochemical GalNAc-T3 expression and various clinicopathological characteristics and recurrence using 110 paraffin-embedded tumor samples obtained from patients with surgically resected ESOSCC (T1-2N0). Recurrence was recognized in 37 of 110 (33.6 %) patients. The GalNAc-T3 expression was considered to be strongly positive when 20 % or more of the cancer cells showed positive cytoplasmic staining. Consequently, a strong expression of GalNAc-T3 was observed in 40 patients (36.4 %), showing a close relationship to poor differentiation, the presence of lymphatic and vascular invasion, and recurrence. Univariate and multivariate analyses further demonstrated that the patients with a strong GalNAc-T3+ status had markedly lower disease-free survival (DFS) rates, especially within the first 2 years postoperatively. Therefore, GalNAc-T3 might play a role in the pathogenesis of ESOSCC recurrence, and its immunohistochemical detection potentially predicts a shorter DFS and may be a useful parameter for providing clinical management against ESOSCC in the early postoperative phase.

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References

Gu C, Oyama T, Osaki T, Li J, Takenoyama M, Izumi H . Low expression of polypeptide GalNAc N-acetylgalactosaminyl transferase-3 in lung adenocarcinoma: impact on poor prognosis and early recurrence. Br J Cancer. 2004; 90(2):436-42. PMC: 2409559. DOI: 10.1038/sj.bjc.6601531. View

Bennett E, Mandel U, Clausen H, Gerken T, Fritz T, Tabak L . Control of mucin-type O-glycosylation: a classification of the polypeptide GalNAc-transferase gene family. Glycobiology. 2011; 22(6):736-56. PMC: 3409716. DOI: 10.1093/glycob/cwr182. View

Jemal A, Bray F, Center M, Ferlay J, Ward E, Forman D . Global cancer statistics. CA Cancer J Clin. 2011; 61(2):69-90. DOI: 10.3322/caac.20107. View

Hanley J . Receiver operating characteristic (ROC) methodology: the state of the art. Crit Rev Diagn Imaging. 1989; 29(3):307-35. View

Scully C, Bagan J . Oral squamous cell carcinoma overview. Oral Oncol. 2009; 45(4-5):301-8. DOI: 10.1016/j.oraloncology.2009.01.004. View

Ishida T, Hijioka H, Kume K, Miyawaki A, Nakamura N . Notch signaling induces EMT in OSCC cell lines in a hypoxic environment. Oncol Lett. 2013; 6(5):1201-1206. PMC: 3813785. DOI: 10.3892/ol.2013.1549. View

Yamamoto E, Kohama G, Sunakawa H, Iwai M, Hiratsuka H . Mode of invasion, bleomycin sensitivity, and clinical course in squamous cell carcinoma of the oral cavity. Cancer. 1983; 51(12):2175-80. DOI: 10.1002/1097-0142(19830615)51:12<2175::aid-cncr2820511205>3.0.co;2-m. View

Hagen F, Van Wuyckhuyse B, Tabak L . Purification, cloning, and expression of a bovine UDP-GalNAc: polypeptide N-acetyl-galactosaminyltransferase. J Biol Chem. 1993; 268(25):18960-5. View

Izumi H, Yasuniwa Y, Akiyama M, Yamaguchi T, Kuma A, Kitamura N . Forced Expression of ZNF143 Restrains Cancer Cell Growth. Cancers (Basel). 2013; 3(4):3909-20. PMC: 3763402. DOI: 10.3390/cancers3043909. View

10.

Wang Z, Bachvarova M, Morin C, Plante M, Gregoire J, Renaud M . Role of the polypeptide N-acetylgalactosaminyltransferase 3 in ovarian cancer progression: possible implications in abnormal mucin O-glycosylation. Oncotarget. 2014; 5(2):544-60. PMC: 3964228. DOI: 10.18632/oncotarget.1652. View

11.

Takeda T, Izumi H, Kitada S, Uramoto H, Tasaki T, Zhi L . The combination of a nuclear HMGB1-positive and HMGB2-negative expression is potentially associated with a shortened survival in patients with pancreatic ductal adenocarcinoma. Tumour Biol. 2014; 35(10):10555-69. DOI: 10.1007/s13277-014-2328-8. View

12.

Schwientek T, Bennett E, Flores C, Thacker J, Hollmann M, Reis C . Functional conservation of subfamilies of putative UDP-N-acetylgalactosamine:polypeptide N-acetylgalactosaminyltransferases in Drosophila, Caenorhabditis elegans, and mammals. One subfamily composed of l(2)35Aa is essential in Drosophila. J Biol Chem. 2002; 277(25):22623-38. DOI: 10.1074/jbc.M202684200. View

13.

Landers K, Burger M, Tebay M, Purdie D, Scells B, Samaratunga H . Use of multiple biomarkers for a molecular diagnosis of prostate cancer. Int J Cancer. 2004; 114(6):950-6. DOI: 10.1002/ijc.20760. View

14.

Oken M, Creech R, Tormey D, Horton J, Davis T, McFadden E . Toxicity and response criteria of the Eastern Cooperative Oncology Group. Am J Clin Oncol. 1982; 5(6):649-55. View

15.

Capote A, Escorial V, Munoz-Guerra M, Rodriguez-Campo F, Gamallo C, Naval L . Elective neck dissection in early-stage oral squamous cell carcinoma--does it influence recurrence and survival?. Head Neck. 2006; 29(1):3-11. DOI: 10.1002/hed.20482. View

16.

Sasahira T, Kirita T, Kuniyasu H . Update of molecular pathobiology in oral cancer: a review. Int J Clin Oncol. 2014; 19(3):431-6. DOI: 10.1007/s10147-014-0684-4. View

17.

Li Z, Yamada S, Inenaga S, Imamura T, Wu Y, Wang K . Polypeptide N-acetylgalactosaminyltransferase 6 expression in pancreatic cancer is an independent prognostic factor indicating better overall survival. Br J Cancer. 2011; 104(12):1882-9. PMC: 3111199. DOI: 10.1038/bjc.2011.166. View

18.

Ten Hagen K, Fritz T, Tabak L . All in the family: the UDP-GalNAc:polypeptide N-acetylgalactosaminyltransferases. Glycobiology. 2003; 13(1):1R-16R. DOI: 10.1093/glycob/cwg007. View

19.

Uramoto H, Izumi H, Ise T, Tada M, Uchiumi T, Kuwano M . p73 Interacts with c-Myc to regulate Y-box-binding protein-1 expression. J Biol Chem. 2002; 277(35):31694-702. DOI: 10.1074/jbc.M200266200. View

20.

Kawatsu Y, Kitada S, Uramoto H, Zhi L, Takeda T, Kimura T . The combination of strong expression of ZNF143 and high MIB-1 labelling index independently predicts shorter disease-specific survival in lung adenocarcinoma. Br J Cancer. 2014; 110(10):2583-92. PMC: 4021533. DOI: 10.1038/bjc.2014.202. View