Publications

^corresponding author

2018

Yan HH, Siu HC, Law S, Ho SL, Yue SS, Tsui WY, Chan D, Chan AS, Ma S, Lam KO, Bartfeld S, Man AH, Lee BC, Chan AS, Wong JW, Cheng PS, Chan AK, Zhang J, Shi J, Fan X, Kwong DL, Mak TW, Yuen ST, Clevers H, Leung SY. A comprehensive human gastric cancer organoid biobank captures tumor subtypes heterogeneity and enables therapeutic screening. Cell Stem Cell 2018; Epub ahead of print.
PMID: 30344100

Chan LH#, Zhou L#, Ng KY#, Wong TL#, Lee TK, Sharma R, Loong JH, Ching YP, Yuan YF, Xie D, Lo CM, Man K, Artegiani B, Clevers H, Yan HH, Leung SY, Richard S, Guan XY, Huen MS, Ma S^. PRMT6 regulates RAS/RAF binding and MEK/ERK-mediated cancer stemness activities in hepatocellular carcinoma through CRAF methylation. Cell Rep 2018; 25:690-701. #equal contribution
PMID: 30332648

Sin ST, Li Y, Liu M, Yuan YF, Ma S, Guan XY. Down-regulation of TROP-2 predicts poor prognosis of hepatocellular carcinoma patients. Hepatol Commun 2018; in press.

Tong M, Che N, Zhou L, Luk ST, Kau PW, Chai S, Ngan ES, Lo CM, Man K, Ding J, Lee TK, Ma S^. Efficacy of annexin A3 blockade in sensitizing hepatocellular carcinoma to sorafenib and regorafenib. J Hepatol 2018; 69:826-39.
PMID: 29885413

Cheng BY#, Lau EY#, Leung DH#, Ho NP, Cheng LK, Lin CH, Lo RC, Ma S, Ng IO, Lee TK. IRAK1 augments cancer stemness and drug resistance via the AP-1/AKR1B10 signaling cascade in hepatocellular carcinoma. Cancer Res 2018; 78:2332-42. #equal contribution
PMID: 29483095

2017

Lau MC#, Ng KY#, Wong TL, Tong M, Lee TK, Ming XY, Law S, Lee NP, Cheung AL, Qin YR, Chan KW, Ning W, Guan XY, Ma S^. FSTL1 promotes metastasis and chemoresistance in esophageal squamous cell carcinoma through NFκB-BMP signaling crosstalk. Cancer Res 2017; 77:5886-99. #equal contribution
PMID: 28883005

Ng KY, Chan LH, Chai S, Tong M, Guan XY, Lee NP, Yuan YF, Xie D, Lee TK, Dusetti NJ, Carrier A, Ma S^. TP53INP1 down-regulation activates a p73-dependent DUSP10/ERK signaling pathway to promote metastasis of hepatocellular carcinoma. Cancer Res 2017; 77:4602-12.
PMID: 28674078

Ma MK, Lau EY, Leung DH, Lo J, Ho NP, Cheng LK, Ma S, Lin CH, Copland JA, Lo RC, Ng IO, Lee TK. Stearoyl-CoA desaturase regulates sorafenib resistance via modulation of ER stress induced differentiation. J Hepatol 2017; 67:979-90.
PMID: 28647567

Wong TL#, Che N#, Ma S^. Reprogramming of central carbon metabolism in cancer stem cells. Biochim Biophys Acta 2017; 1863:1728-38. #equal contribution (invited review)
PMID: 28502706

2016

Ming XY, Fu L, Zhang LY, Qin YR, Cao TT, Chan KW, Ma S, Xie D, Guan XY. Integrin α7 is a functional cancer stem cell surface marker in esophageal squamous cell carcinoma. Nat Commun 2016; 7:13568.
PMID: 27924820

Ma S^. Deciphering ZIC2/OCT4 signaling as a vulnerability in liver cancer stem cells. Transl Cancer Res 2016; in press. (invited editorial)

Chai S, Ng KY, Tong M, Lau EY, Lee TK, Chan KW, Yuan YF, Cheung TT, Cheung ST, Wang XQ, Wong N, Lo CM, Man K, Guan XY, Ma S^. Octamer4/microRNA-1246 signaling axis drives Wnt/β-catenin activation in liver cancer stem cells. Hepatology 2016; 64:2062-76.
(Comment by Wu WK, et al. A transcriptional-microRNA network for β-catenin-driven stemness in hepatocellular carcinoma. Transl Cancer Res 2016; in press)
(Comment by Eshelman and Yochum. The Wnt/β-catenin pathway is activated in miR-1246 in liver cancer stem cells. Transl Cancer Res 2016; in press)
PMID: 27639189

Fung TM#, Ng KY#, Tong M, Chen JN, Chai S, Chan KT, Law S, Lee NP, Choi MY, Li B, Cheung AL, Tsao SW, Qin YR, Guan XY, Chan KW, Ma S^. Neuropilin-2 promotes tumorigenicity and metastasis in esophageal squamous cell carcinoma through ERK MAPK/ETV4/MMP/E-cadherin deregulation. J Pathol 2016; 239:309-19. #equal contribution
PMID: 27063000

Lau EY, Lo J, Cheng BY, Ma MK, Lee MF, Ng KY, Chai S, Lin N, Tsang FS, Ma S, Ng IO, Lee TK. Cancer-associated fibroblasts regulate tumor-initiating cell plasticity in hepatocellular carcinoma through c-Met/FRA1/HEY1 signaling. Cell Rep 2016; 15:1175-89.
PMID: 27134167

Ng KY, Chai S, Tong M, Guan XY, Lin CH, Ching YP, Xie D, Cheng AS, Ma S^. C-terminal truncated hepatitis B virus X protein promotes hepatocellular carcinogenesis through induction of cancer and stem cell-like properties. Oncotarget 2016; 7:24005-17.
PMID: 27006468

Zhang LY, Wu JL, Qiu HB, Dong SS, Zhu YH, Lee VH, Qin YR, Li Y, Chen J, Liu HB, Bi J, Ma S, Guan XY, Fu L. PSCA acts as a tumor suppressor by facilitating the nuclear translocation of RB1CC1 in esophageal squamous cell carcinoma. Carcinogenesis 2016; 37:320-32.
PMID: 26785734

Li J, Zhang BZ, Qin YR, Bi J, Liu HB, Li Y, Cai MY, Ma S, Chan KW, Xie D, Guan XY. CD68 and interleukin 13, prospective immune markers for esophageal squamous cell carcinoma prognosis prediction. Oncotarget 2016; 7:15525-38.
PMID: 26771842

Li J, Chen JN, Zeng TT, He F, Chen SP, Ma S, Bi J, Zhu XF, Guan XY. CD133+ liver cancer stem cells resist interferon-gamma induced autophagy. BMC Cancer 2016; 16:15.
PMID: 26758620

Tang KD, Holzapfel BM, Liu J, Lee TK, Ma S, Jovanovic L, An J, Russell PJ, Clements JA, Hutmacher DW, Ling MT. Tie-2 regulates the stemness and metastatic properties of prostate cancer cells. Oncotarget 2016; 7:2572-84.
PMID: 25978029

Tang KD, Liu J, Jovanovic L, An J, Hill MM, Vela I, Lee TK, Ma S, Nelson C, Russell PJ, Clements JA, Ling MT. Adipocytes promote prostate cancer stem cell self-renewal through amplification of the cholecystokinin autocrine loop. Oncotarget 2016;7:4939-48.
PMID: 26700819

2015

Won C, Kim BH, Yi EH, Choi KJ, Kim EK, Jeong JM, Lee JH, Jang JJ, Yoon JH, Jeong WI, Park IC, Kim TW, Bae SS, Factor VM, Ma S, Thorgeirsson SS, Lee YH, Ye SK. STAT3-mediated CD133 upregulation contributes to promotion of hepatocellular carcinoma. Hepatology 2015; 62:1160-73.
PMID: 26154152

Song Y, Pan G, Chen L, Ma S, Zeng T, Chan TH, Li L, Lian Q, Chow R, Cai X, Li Y, Li Y, Liu M, Li Y, Zhu Y, Wong N, Yuan YF, Pei D, Guan XY. Loss of ATOH8 increases stem cell features of hepatocellular carcinoma cells. Gastroenterology 2015; 149:1068-81.
PMID: 26099525

Tong M, Fung TM, Luk ST, Ng KY, Lee TK, Lin CH, Yam JW, Chan KW, Ng F, Zheng BJ, Yuan YF, Xie D, Lo CM, Man K, Guan XY, Ma S^. ANXA3/JNK signaling promotes self-renewal and tumor growth and its blockade provides a therapeutic target for hepatocellular carcinoma. Stem Cell Reports 2015; 5:45-59.
PMID: 26095609
Patents granted: Above findings have directly led to two successful patent applications (Patent US. 9487831 B2, Nov 8 2016 and Patent US. 10,000,558, Jun 19 2018) for the use of the ANXA3 antibody for the detection and targeting of HCC.
Licenses of intellectual property to external parties: Since 2016, ANXA3 antibody licensed to Merck Millipore for sale and use by research community.

Chan LH, Luk ST, Ma S^. Turning hepatic cancer stem cells inside out – a deeper understanding through multiple perspectives. Mol Cells 2015; 38:202-9. (invited review)
PMID: 25666349

2014

Liu L, Dai Y, Chen J, Zeng T, Li Y, Chen L, Zhu YH, Li J, Li Y, Ma S, Xie D, Yuan YF, Guan XY. Maelstrom promotes hepatocellular carcinoma metastasis by inducing epithelial-mesenchymal transition by way of Akt/GSK-3β/Snail signaling. Hepatology 2014; 59:531-43.
PMID: 23929794

Lee TK, Cheung VC, Lu P, Lau EY, Ma S, Tang KH, Tong M, Lo J, Ng IO. Blockade of CD47 mediated CTSS-PAR2 signaling provides a therapeutic target for hepatocellular carcinoma. Hepatology 2014; 60:179-91.
(Comment by Roberts DD, et al. Therapeutic targeting of the thrombospondin-1 receptor CD47 to treat liver cancer. J Cell Commun Signal 2015; 9:101-2)
PMID: 24523067

Chai S#, Tong M#, Ng KY#, Kwan PS, Chan YP, Fung TM, Lee TK, Wong N, Xie D, Yuan YF, Guan XY, Ma S^. Regulatory role of miR-142-3p on the functional hepatic cancer stem cell marker CD133. Oncotarget 2014; 5:5725-35. #equal contribution
PMID: 25015418

2013

Tang KH, Dai Y, Tong M, Chan YP, Kwan PS, Fu L, Qin YR, Tsao SW, Lung HL, Lung ML, Tong DK, Law S, Chan KW, Ma S^, Guan XY. A CD90+ tumor-initiating cell population with an aggressive signature and metastatic capacity in esophageal cancer. Cancer Res 2013; 73:2322-32.
PMID: 23382045

Dai YD, Liu LL, Zeng TT, Zhu YH, Li JC, Chen LL, Li Y, Yuan YF, Ma S^, Guan XY. Characterization of the oncogenic function of centromere protein F in hepatocellular carcinoma. Biochem Biophys Res Commun 2013; 436:711-8.
PMID: 23791740

Ma S^. Biology and clinical implications of CD133+ liver cancer stem cells. Exp Cell Res 2013; 319:126-32. (invited review)
PMID: 22999864

Chai S, Ma S^. Clinical implications of miRNA in liver cancer stem cells. Chin J Cancer 2013; 32:419-26. (invited perspective article)
PMID: 23668930

2012

Tang KH, Ma S^, Lee TK, Chan YP, Kwan PS, Tong CM, Ng IO, Man K, To KF, Lai PB, Lo CM, Guan XY, Chan KW. CD133+ liver tumor-initiating cells promote tumor angiogenesis, growth and self-renewal through neurotensin/interleukin-8/CXCL1 signaling. Hepatology 2012; 55:807-20.
PMID: 21994122

Ma S, Bao JY, Kwan PS, Chan YP, Tong M, Fu L, Zhang N, Tong AH, Qin YR, Tsao SW, Chan KW, Lok S, Guan XY. Identification of PTK6, via RNA sequencing analysis, as a suppressor of esophageal squamous cell carcinoma. Gastroenterology 2012; 143:675-86.
PMID: 22705009

Tong M, Chan KW, Bao JY, Wong KY, Chen JN, Kwan PS, Tang KH, Fu L, Qin YR, Lok S, Guan XY, Ma S^. Rab25 is a tumor suppressor gene with anti-angiogenic and anti-invasive activities in esophageal squamous cell carcinoma. Cancer Res 2012; 72:6024-35.
PMID: 22991305

2011

Lee TK, Murthy SR, Cawley NX, Dhanvantari S, Hewitt SM, Lou H, Lau T, Ma S, Huynh T, Wesley RA, Ng IO, Pacak K, Poon RT, Loh PY. An N-terminal truncated carboxypeptidase E splice isoform induces tumor growth and is a biomarker for predicting future metastasis in human cancers. J Clin Invest 2011; 121:880-92.
(Selected as “Editor’s Pick” in J Clin Invest 2011)
(Recommended by F1000 Prime – Kumar A and Halwan B, 2011)
PMID: 21285511

Lee TK, Castilho A, Cheung VC, Tang KH, Ma S, Ng IO. Lupeol targets liver tumor initiating cells through PTEN modulation. Hepatology 2011; 53:160-70.
PMID: 20979057

Luk SU, Yap WN, Chiu YT, Lee DT, Ma S, Lee TK, Vasireddy RS, Wong YC, Ching YP, Nelson C, Yap YL, Ling MT. Gamma-tocotrienol as an effective agent in targeting prostate cancer stem cell-like population. Int J Cancer 2011; 128:2182-91.
PMID: 20617516

Ma S^, Chan YP, Kwan PS, Lee TK, Yan M, Tang KH, Ling MT, Vielkind J, Guan XY, Chan KW. microRNA-616 induces androgen-independent growth of prostate cancer cells by suppressing expression of tissue factor pathway inhibitor TFPI-2. Cancer Res 2011; 71:583-92.
PMID: 21224345

Ma S^, Guan XY. miRegulators in cancer stem cells of solid tumors. Cell Cycle 2011; 10:571-2. (invited commentary article)
PMID: 21311235

Luk SU, Lee TK, Liu J, Lee DT, Chiu YT, Ma S, Ng IO, Wong YC, Chan FL, Ling MT. Chemopreventive effect of PSP through targeting of prostate cancer stem cell-like population. PLoS One 2011; 6:e19804.
PMID: 21603625

Lee TK, Castilho A, Cheung VC, Tang KH, Ma S, Ng IO. CD24+ liver tumor-initiating cells drive self-renewal and tumor initiation through Stat3-mediated Nanog regulation. Cell Stem Cell 2011; 9:50-63.
(Awarded the 2012 Faculty Outstanding Research Output Prize, Faculty of Medicine, HKU)
(Selected as one of the top ten “featured research papers” of Cell Stem Cell in 2012)
PMID: 21726833

Tong CM*, Ma S*, Guan XY. Biology of hepatic cancer stem cells. J Gastroenterol Hepatol 2011; 26:1229-37. (*both authors contributed equally) (invited review)
PMID: 21557770

Tang KH*, Ma S*, Guan XY. Liver tumor-initiating cells / cancer stem cells: past studies, current status and future perspectives. In: Advances in Cancer Stem Cell Biology (R Scatena, A Mordente, B Giardina, Eds.) Springer Publishing 2011, ISBN 978-1-4614-0808-6. (*both authors contributed equally)

2010

Ma S^, Tang KH, Chan YP, Lee TK, Kwan PS, Castilho A, Ng IO, Man K, Wong N, To KF, Zheng BJ, Lai PB, Lo CM, Chan KW, Guan XY. miR-130b promotes CD133+ liver tumor-initiating cell growth and self-renewal via tumor protein 53-induced nuclear protein 1. Cell Stem Cell 2010; 7:694-707.
(Awarded the 2011 Faculty Outstanding Research Output Prize, Faculty of Medicine, HKU)
PMID: 21112564

Chen LL, Chan TH, Yuan YF, Hu L, Huang J, Ma S, Wang J, Dong SS, Tang KH, Xie D, Li Y, Guan XY. CHD1L promotes hepatocellular carcinoma progression and metastasis in mice and is associated with these processes in human patients. J Clin Invest 2010; 120:1178-91.
(Comment by Teoh NC. Pre-“EMT”ing key processes in liver carcinogenesis: Growing evidence for how malignant hepatocytes invade and conquer. Hepatology 2010; 52:384-8)
(Comment by Jou J and Diehl AM. Epithelial-mesenchymal transitions and hepatocarcinogenesis. J Clin Invest 2010; 120:1031-4)
PMID: 20335658

Ma S, Chan KW, Guan XY. Cancer stem cells – Concepts, methodologies and therapeutic implications. In: Cancer Stem Cells (XY Guan, Ed.). Research Signpost 2010, ISBN: 978-81-7895-465-3.

Ma S, Tang KH, Chan KW, Guan XY. Liver cancer stem cells – A review of current literature and protocols. In: Cancer Stem Cells (XY Guan, Ed.). Research Signpost 2010, ISBN: 978-81-7895-465-3.

Lee TK, Castilho A, Ma S, Ng IO. Epithelial-mesenchymal transition in cancer stem cells. In: Cancer Stem Cells (XY Guan, Ed.). Research Signpost 2010, ISBN: 978-81-7895-465-3.

2009

Ma S, Chan YP, Woolcock B, Hu L, Wong KY, Ling MT, Bainbridge T, Webber D, Chan THM, Guan XY, Lam W, Vielkind J, Chan KW. DNA fingerprinting tags novel altered chromosomal regions and identifies the involvement of SOX5 in the progression of prostate cancer. Int J Cancer 2009; 124:2323-32.
PMID: 19173284

Chen LL, Hu L, Chan THM, Tsao SW, Xie D, Huo KK, Ma S, Fu L, Zheng BJ, Guan XY. CHD1L suppresses the nucleus-to-mitochondria translocation of Nur77 to sustain hepatocellular carcinoma cell survival. Hepatology 2009; 50:122-9.
PMID: 19441106

Lee TK, Castilho A, Ma S, Ng IO. Liver cancer stem cells: Implications for a new therapeutic target. Liver Int 2009; 29: 955-65.
PMID: 19490415

2008

Ma S, Lee TK, Zheng BJ, Chan KW, Guan XY. CD133+ HCC cancer stem cells promote chemoresistance by preferential expression of the Akt/PKB survival pathway. Oncogene 2008; 27:1749-58.
(F1000 Rating: 8 Must Read; Mishra L: 2008. F1000.com/1096034)
PMID: 17891174

Ma S, Chan KW, Lee TK, Tang KH, Wo JY, Zheng BJ, Guan XY. Aldehyde dehydrogenase discriminates the CD133 liver cancer stem cell populations. Mol Cancer Res 2008; 6:1146-53.
(Most cited paper in Mol Cancer Res in 2008)
PMID: 18644979

Ma S, Chan KW and Guan XY. In search of liver cancer stem cells. Stem Cell Rev 2008, 4:179-92.
PMID: 18663610

2007

Ma S, Chan KW, Hu L, Lee TK, Wo JY, Ng IO, Zheng BJ, Guan XY. Identification and characterization of tumorigenic liver cancer stem/progenitor cells. Gastroenterology 2007; 132:2542-56.
PMID: 17570225

Ma S, Guan XY, Beh PS, Wong KY, Chan YP, Yuen HF, Vielkind J, Chan KW. Significance of LMO2 expression in progression of prostate cancer. J Pathol 2007; 211:278-85.
PMID: 17167821

Ma S, Guan XY, Lee TK, Chan KW. Clinicopathological significance of missing in metastasis B expression in hepatocellular carcinoma. Hum Pathol 2007; 38:1201-6.
PMID: 17442377

Lee TK, Poon RT, Wo JY, Ma S, Guan XY, Myers JN, Yuen AP. Lupeol suppresses cisplatin-induced nuclear factor-kappaB activation in head and neck squamous cell carcinoma and inhibits local invasion and nodal metastasis in orthotopic nude mouse model. Cancer Res 2007; 67:8800-9.
PMID: 17875721

Ma S, Hu L, Huang XH, Cao LQ, Chan KW, Wang Q, Guan XY. Establishment and characterization of a human cholangiocarcinoma cell line. Oncol Rep 2007; 18:1195-200.
PMID: 17914572

Lee TK, Poon RT, Man K, Guan XY, Ma S, Liu XB, Myers JN, Yuen AP. Fascin over-expression is associated with aggressiveness of oral squamous cell carcinoma. Cancer Lett 2007; 253:308-15.
PMID: 17499430

2006

Shen J, Ma S, Chan P, Lee W, Fung PC, Cheung RT, Tong Y, Liu KJ. Nitric oxide down-regulates caveolin-1 expression in rat brains during focal cerebral ischemia and reperfusion injury. J Neurochem 2006; 96:1078-89.
PMID: 16417587