Top

Published in:

Open Access 01-12-2014 | Original Article

SATB1 is an independent prognostic factor in radically resected upper gastrointestinal tract adenocarcinoma

Authors: Charlotta Hedner, Alexander Gaber, Dejan Korkocic, Björn Nodin, Mathias Uhlén, Eugenia Kuteeva, Henrik Johannesson, Karin Jirström, Jakob Eberhard

Published in: Virchows Archiv | Issue 6/2014

Abstract

Gastric cancer is the second most common cause of cancer-related death worldwide, and the incidence of esophageal adenocarcinoma is rising. While some progress has been made in treatment strategies, overall survival remains very poor for patients with adenocarcinoma in the upper gastrointestinal tract. Special AT-rich sequence binding protein 1 (SATB1) is a global genome organizer that has been demonstrated to promote aggressive tumor behavior in several different types of cancer, including gastric cancer. The prognostic value of SATB1 expression in esophageal cancer has, however, not yet been described. In this study, expression of SATB1 was examined by immunohistochemistry on tissue microarrays prepared from tissue samples from 175 patients with adenocarcinoma of the esophagus, cardia, or stomach and containing normal tissue, intestinal metaplasia, primary tumors, and metastases. A well-validated antibody was used. We found SATB1 to be an independent prognostic factor in patients with a radically resected tumor, correlating with shorter overall survival as well as with shorter recurrence-free survival. SATB1 expression was also found to be significantly lower in primary tumors associated with intestinal metaplasia than those without intestinal metaplasia. This observation is of potential biological interest as it has been proposed that intestinal metaplasia-associated tumors constitute a less aggressive phenotype.

Available only for authorised users

Bertuccio P, Chatenoud L, Levi F, Praud D, Ferlay J, Negri E, Malvezzi M, La Vecchia C (2009) Recent patterns in gastric cancer: a global overview. Int J Cancer 125(3):666–673PubMedCrossRef

Lauwers GY (2009) Epithelial neoplasms of the stomach. In:Odze RD, Goldblum JR (eds) Surgical pathology of the GI tract, liver, biliary tract and pancreas, volume 1, 2nd edn. Elsevier, Philadelphia, p 563–580

Parkin DM, Bray F, Ferlay J, Pisani P (2005) Global cancer statistics, 2002. CA Cancer J Clin 55(2):74–108PubMedCrossRef

Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM (2010) Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 127(12):2893–2917PubMedCrossRef

Devesa SS, Blot WJ, Fraumeni JF Jr (1998) Changing patterns in the incidence of esophageal and gastric carcinoma in the United States. Cancer 83(10):2049–2053PubMedCrossRef

Cunningham D, Allum WH, Stenning SP, Thompson JN, Van de Velde CJ, Nicolson M, Scarffe JH, Lofts FJ, Falk SJ, Iveson TJ et al (2006) Perioperative chemotherapy versus surgery alone for resectable gastroesophageal cancer. N Engl J Med 355(1):11–20PubMedCrossRef

van Hagen P, Hulshof MC, van Lanschot JJ, Steyerberg EW, van Berge Henegouwen MI, Wijnhoven BP, Richel DJ, Nieuwenhuijzen GA, Hospers GA, Bonenkamp JJ et al (2012) Preoperative chemoradiotherapy for esophageal or junctional cancer. N Engl J Med 366(22):2074–2084PubMedCrossRef

Bang YJ, Van Cutsem E, Feyereislova A, Chung HC, Shen L, Sawaki A, Lordick F, Ohtsu A, Omuro Y, Satoh T et al (2010) Trastuzumab in combination with chemotherapy versus chemotherapy alone for treatment of HER2-positive advanced gastric or gastro-oesophageal junction cancer (ToGA): a phase 3, open-label, randomised controlled trial. Lancet 376(9742):687–697PubMedCrossRef

Kohwi-Shigematsu T, Poterlowicz K, Ordinario E, Han HJ, Botchkarev VA, Kohwi Y (2013) Genome organizing function of SATB1 in tumor progression. Semin Cancer Biol 23(2):72–79PubMedCentralPubMedCrossRef

10.

Dickinson LA, Joh T, Kohwi Y, Kohwi-Shigematsu T (1992) A tissue-specific MAR/SAR DNA-binding protein with unusual binding site recognition. Cell 70(4):631–645PubMedCrossRef

11.

Yasui D, Miyano M, Cai S, Varga-Weisz P, Kohwi-Shigematsu T (2002) SATB1 targets chromatin remodelling to regulate genes over long distances. Nature 419(6907):641–645PubMedCrossRef

12.

Han HJ, Russo J, Kohwi Y, Kohwi-Shigematsu T (2008) SATB1 reprogrammes gene expression to promote breast tumour growth and metastasis. Nature 452(7184):187–193PubMedCrossRef

13.

Nodin B, Hedner C, Uhlen M, Jirstrom K (2012) Expression of the global regulator SATB1 is an independent factor of poor prognosis in high grade epithelial ovarian cancer. J Ovarian Res 5(1):24PubMedCentralPubMedCrossRef

14.

Nodin B, Johannesson H, Wangefjord S, O’Connor DP, Lindquist KE, Uhlen M, Jirstrom K, Eberhard J (2012) Molecular correlates and prognostic significance of SATB1 expression in colorectal cancer. Diagn Pathol 7:115PubMedCentralPubMedCrossRef

15.

Meng WJ, Yan H, Zhou B, Zhang W, Kong XH, Wang R, Zhan L, Li Y, Zhou ZG, Sun XF (2012) Correlation of SATB1 overexpression with the progression of human rectal cancer. Int J Color Dis 27(2):143–150CrossRef

16.

Zhang J, Zhang B, Zhang X, Sun Y, Wei X, McNutt MA, Lu S, Liu Y, Zhang D, Wang M et al (2013) SATB1 expression is associated with biologic behavior in colorectal carcinoma in vitro and in vivo. PLoS ONE 8(1):e47902PubMedCentralPubMedCrossRef

17.

Zhao XD, Ji WY, Zhang W, He LX, Yang J, Liang HJ, Wang LL (2010) Overexpression of SATB1 in laryngeal squamous cell carcinoma. ORL J Otorhinolaryngol Relat Spec 72(1):1–5PubMedCrossRef

18.

Al-Sohaily S, Henderson C, Selinger C, Pangon L, Segelov E, Kohonen-Corish M, Warusavitarne J (2013) Loss of special AT-rich sequence-binding protein 1 (SATB1) predicts poor survival in patients with colorectal cancer. Histopathology 65(2):155–63. doi:10.1111/his.12295

19.

Iorns E, Hnatyszyn HJ, Seo P, Clarke J, Ward T, Lippman M (2010) The role of SATB1 in breast cancer pathogenesis. J Natl Cancer Inst 102(16):1284–1296PubMedCrossRef

20.

Hanker LC, Karn T, Mavrova-Risteska L, Ruckhaberle E, Gaetje R, Holtrich U, Kaufmann M, Rody A, Wiegratz I (2011) SATB1 gene expression and breast cancer prognosis. Breast 20(4):309–313PubMedCrossRef

21.

Kohwi-Shigematsu T, Han HJ, Russo J, Kohwi Y (2010) Re: The role of SATB1 in breast cancer pathogenesis. J Natl Cancer Inst 102(24):1879–1880, author reply 1880–1871PubMedCentralPubMedCrossRef

22.

Lu X, Cheng C, Zhu S, Yang Y, Zheng L, Wang G, Shu X, Wu K, Liu K, Tong Q (2010) SATB1 is an independent prognostic marker for gastric cancer in a Chinese population. Oncol Rep 24(4):981–987PubMed

23.

Cheng C, Lu X, Wang G, Zheng L, Shu X, Zhu S, Liu K, Wu K, Tong Q (2010) Expression of SATB1 and heparanase in gastric cancer and its relationship to clinicopathologic features. APMIS 118(11):855–863PubMedCrossRef

24.

Sun F, Lu X, Li H, Peng Z, Wu K, Wang G, Tong Q (2012) Special AT-rich sequence binding protein 1 regulates the multidrug resistance and invasion of human gastric cancer cells. Oncol Lett 4(1):156–162PubMedCentralPubMed

25.

Fristedt R, Gaber A, Hedner C, Nodin B, Uhlen M, Eberhard J, Jirstrom K (2014) Expression and prognostic significance of the polymeric immunoglobulin receptor in esophageal and gastric adenocarcinoma. J Transl Med 12(1):83PubMedCentralPubMedCrossRef

26.

Jonsson L, Hedner C, Gaber A, Korkocic D, Nodin B, Uhlen M, Eberhard J, Jirstrom K (2014) High expression of RNA-binding motif protein 3 in esophageal and gastric adenocarcinoma correlates with intestinal metaplasia-associated tumours and independently predicts a reduced risk of recurrence and death. Biomark Res 2:11PubMedCentralPubMedCrossRef

27.

Edge SB, Compton CC (2010) The American Joint Committee on Cancer: the 7th edition of the AJCC cancer staging manual and the future of TNM. Ann Surg Oncol 17(6):1471–1474PubMedCrossRef

28.

Kononen J, Bubendorf L, Kallioniemi A, Barlund M, Schraml P, Leighton S, Torhorst J, Mihatsch MJ, Sauter G, Kallioniemi OP (1998) Tissue microarrays for high-throughput molecular profiling of tumor specimens. Nat Med 4(7):844–847PubMedCrossRef

29.

Larsson A, Fridberg M, Gaber A, Nodin B, Leveen P, Jonsson G, Uhlen M, Birgisson H, Jirstrom K (2012) Validation of podocalyxin-like protein as a biomarker of poor prognosis in colorectal cancer. BMC Cancer 12:282PubMedCentralPubMedCrossRef

30.

Wang S, Zhou J, Wang XY, Hao JM, Chen JZ, Zhang XM, Jin H, Liu L, Zhang YF, Liu J et al (2009) Down-regulated expression of SATB2 is associated with metastasis and poor prognosis in colorectal cancer. J Pathol 219(1):114–122PubMedCrossRef

31.

Eberhard J, Gaber A, Wangefjord S, Nodin B, Uhlen M, Ericson Lindquist K, Jirstrom K (2012) A cohort study of the prognostic and treatment predictive value of SATB2 expression in colorectal cancer. Br J Cancer 106(5):931–938PubMedCentralPubMedCrossRef

32.

Demicco EG, Farris AB 3rd, Baba Y, Agbor-Etang B, Bergethon K, Mandal R, Daives D, Fukuoka J, Shimizu M, Dias-Santagata D et al (2011) The dichotomy in carcinogenesis of the distal esophagus and esophagogastric junction: intestinal-type vs cardiac-type mucosa-associated adenocarcinoma. Mod Pathol 24(9):1177–1190PubMedCrossRef

33.

Yamayoshi A, Yasuhara M, Galande S, Kobori A, Murakami A (2011) Decoy-DNA against special AT-rich sequence binding protein 1 inhibits the growth and invasive ability of human breast cancer. Oligonucleotides 21(2):115–121PubMedCrossRef

34.

Gheldof A, Berx G (2013) Cadherins and epithelial-to-mesenchymal transition. Prog Mol Biol Transl Sci 116:317–336PubMedCrossRef

35.

Fang XF, Hou ZB, Dai XZ, Chen C, Ge J, Shen H, Li XF, Yu LK, Yuan Y (2013) Special AT-rich sequence-binding protein 1 promotes cell growth and metastasis in colorectal cancer. World J Gastroenterol 19(15):2331–2339PubMedCentralPubMedCrossRef

36.

Torhorst J, Bucher C, Kononen J, Haas P, Zuber M, Kochli OR, Mross F, Dieterich H, Moch H, Mihatsch M et al (2001) Tissue microarrays for rapid linking of molecular changes to clinical endpoints. Am J Pathol 159(6):2249–2256PubMedCentralPubMedCrossRef

Title: SATB1 is an independent prognostic factor in radically resected upper gastrointestinal tract adenocarcinoma
Authors: Charlotta Hedner
Alexander Gaber
Dejan Korkocic
Björn Nodin
Mathias Uhlén
Eugenia Kuteeva
Henrik Johannesson
Karin Jirström
Jakob Eberhard
Publication date: 01-12-2014
Publisher: Springer Berlin Heidelberg
Published in: Virchows Archiv / Issue 6/2014
Print ISSN: 0945-6317
Electronic ISSN: 1432-2307
DOI: https://doi.org/10.1007/s00428-014-1667-6

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

SATB1 is an independent prognostic factor in radically resected upper gastrointestinal tract adenocarcinoma

Abstract

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 6/2014

JMY protein, a regulator of P53 and cytoplasmic actin filaments, is expressed in normal and neoplastic tissues

Gene expression profiling of giant cell tumor of bone reveals downregulation of extracellular matrix components decorin and lumican associated with lung metastasis

Evaluation of clinico-pathological features and Helicobacter pylori infection in gastric inflammatory fibroid polyps

Acinar cell carcinomas of the pancreas: a molecular analysis in a series of 57 cases

Total burden of intraplaque hemorrhage in coronary arteries relates to the use of coumarin-type anticoagulants but not platelet aggregation inhibitors

Consensus statement with recommendations on active surveillance inclusion criteria and definition of progression in men with localized prostate cancer: the critical role of the pathologist