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Research Article

Metastatic progression of prostate cancer is mediated by autonomous binding of galectin-4-O-glycan to cancer cells

Chin-Hsien Tsai, Sheue-Fen Tzeng, Tai-Kuang Chao, Chia-Yun Tsai, Yu-Chih Yang, Ming-Ting Lee, Jiuan-Jiuan Hwang, Yu-Ching Chou, Mong-Hsun Tsai, Tai-Lung Cha and Pei-Wen Hsiao
Chin-Hsien Tsai
Agricultural Biotechnology Research Center, Academia Sinica
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Sheue-Fen Tzeng
Agricultural Biotechnology Research Center, Academia Sinica
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Tai-Kuang Chao
Department of Pathology, Tri-Service General Hospital, National Defense Medical Center
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Chia-Yun Tsai
Agricultural Biotechnology Research Center, Academia Sinica
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Yu-Chih Yang
Agricultural Biotechnology Research Center, Academia Sinica
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Ming-Ting Lee
Institute of Biochemical Sciences, National Taiwan University
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Jiuan-Jiuan Hwang
Institute of Physiology, National Yang-Ming University
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Yu-Ching Chou
School of Public Health, National Defense Medical Center
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Mong-Hsun Tsai
Institute of Biotechnology, National Taiwan University
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Tai-Lung Cha
Division of Urology, Tri-Service General Hospital, National Defense Medical Center
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Pei-Wen Hsiao
Agricultural Biotechnology Research Center, Academia Sinica
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  • For correspondence: pwhsiao@gate.sinica.edu.tw
DOI: 10.1158/0008-5472.CAN-16-0641
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Abstract

Metastatic prostate cancer (PCa) continues to pose a difficult therapeutic challenge. PCa progression is associated with aberrant O-glycosylation of cancer cell surface receptors, but the functional impact of such events are uncertain. Here we report spontaneous metastasis of human PCa xenografts which express high levels of galectin-4 along with genetic signatures of EGFR-HER2 signaling and O-glycosylation. Galectin-4 expression in clinical specimens of PCa correlated with poor patient survival. Galectin-4 binding to multiple receptor tyrosine kinases stimulated their autophosphorylation, activated expression of pERK, pAkt, fibronectin and Twist1, and lowered expression of E-cadherin, thereby faciliating epithelial-mesenchyme transition, invasion and metastasis. In vivo investigations established that galectin-4 expression enabled PCa cells to repopulate tumors in orthotopic and heterotopic tissues. Notably, these effects of galectin-4 relied upon O-glycosylation mediated by C1GALT1, a galactosyltransferase implicated in other cancers. Parallel changes in galectin-4 and O-glycosylation triggered aberrant receptor signaling and more aggressive invasive character in PCa cells, which through better survival in the circulation also contributed to the bulk cell progeny of distal tumors. Our findings establish galectin-4 and C1GALT1-mediated glycosylation in a signaling axis that is activated during CaP progression, with implications for therapeutic targeting of advanced metastatic disease.

  • Received March 7, 2016.
  • Revision received June 28, 2016.
  • Accepted July 17, 2016.
  • Copyright {copyright, serif}2016, American Association for Cancer Research.
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Published OnlineFirst August 2, 2016
doi: 10.1158/0008-5472.CAN-16-0641

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Metastatic progression of prostate cancer is mediated by autonomous binding of galectin-4-O-glycan to cancer cells
Chin-Hsien Tsai, Sheue-Fen Tzeng, Tai-Kuang Chao, Chia-Yun Tsai, Yu-Chih Yang, Ming-Ting Lee, Jiuan-Jiuan Hwang, Yu-Ching Chou, Mong-Hsun Tsai, Tai-Lung Cha and Pei-Wen Hsiao
Cancer Res August 2 2016 DOI: 10.1158/0008-5472.CAN-16-0641

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Metastatic progression of prostate cancer is mediated by autonomous binding of galectin-4-O-glycan to cancer cells
Chin-Hsien Tsai, Sheue-Fen Tzeng, Tai-Kuang Chao, Chia-Yun Tsai, Yu-Chih Yang, Ming-Ting Lee, Jiuan-Jiuan Hwang, Yu-Ching Chou, Mong-Hsun Tsai, Tai-Lung Cha and Pei-Wen Hsiao
Cancer Res August 2 2016 DOI: 10.1158/0008-5472.CAN-16-0641
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Cancer Research Online ISSN: 1538-7445
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