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Published in: Journal of Translational Medicine 1/2019

Open Access 01-12-2019 | Metastasis | Review

The emerging role of WISP proteins in tumorigenesis and cancer therapy

Authors: Yi Liu, Yizuo Song, Miaomiao Ye, Xiaoli Hu, Z. Peter Wang, Xueqiong Zhu

Published in: Journal of Translational Medicine | Issue 1/2019

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Abstract

Accumulated evidence has demonstrated that WNT1 inducible signaling pathway protein (WISP) genes, which belong to members of the CCN growth factor family, play a pivotal role in tumorigenesis and progression of a broad spectrum of human cancers. Mounting studies have identified that WISP proteins (WISP1-3) exert different biological functions in various human malignancies. Emerging evidence indicates that WISP proteins are critically involved in cell proliferation, apoptosis, invasion and metastasis in cancers. Because the understanding of a direct function of WISP proteins in cancer development and progression has begun to emerge, in this review article, we describe the physiological function of WISP proteins in a variety of human cancers. Moreover, we highlight the current understanding of how the WISP protein is involved in tumorigenesis and cancer progression. Furthermore, we discuss that targeting WISP proteins could be a promising strategy for the treatment of human cancers. Hence, the regulation of WISP proteins could improve treatments for cancer patients.
Literature
2.
go back to reference Pennica D, Swanson TA, Welsh JW, Roy MA, Lawrence DA, Lee J, et al. WISP genes are members of the connective tissue growth factor family that are up-regulated in wnt-1-transformed cells and aberrantly expressed in human colon tumors. Proc Natl Acad Sci USA. 1998;95:14717–22.PubMedCrossRefPubMedCentral Pennica D, Swanson TA, Welsh JW, Roy MA, Lawrence DA, Lee J, et al. WISP genes are members of the connective tissue growth factor family that are up-regulated in wnt-1-transformed cells and aberrantly expressed in human colon tumors. Proc Natl Acad Sci USA. 1998;95:14717–22.PubMedCrossRefPubMedCentral
4.
go back to reference Saxena N, Banerjee S, Sengupta K, Zoubine MN, Banerjee SK. Differential expression of WISP-1 and WISP-2 genes in normal and transformed human breast cell lines. Mol Cell Biochem. 2001;228:99–104.PubMedCrossRef Saxena N, Banerjee S, Sengupta K, Zoubine MN, Banerjee SK. Differential expression of WISP-1 and WISP-2 genes in normal and transformed human breast cell lines. Mol Cell Biochem. 2001;228:99–104.PubMedCrossRef
5.
go back to reference Xie D, Nakachi K, Wang H, Elashoff R, Koeffler HP. Elevated levels of connective tissue growth factor, WISP-1, and CYR61 in primary breast cancers associated with more advanced features. Can Res. 2001;61:8917–23. Xie D, Nakachi K, Wang H, Elashoff R, Koeffler HP. Elevated levels of connective tissue growth factor, WISP-1, and CYR61 in primary breast cancers associated with more advanced features. Can Res. 2001;61:8917–23.
6.
go back to reference Chiang KC, Yeh CN, Chung LC, Feng TH, Sun CC, Chen MF, et al. WNT-1 inducible signaling pathway protein-1 enhances growth and tumorigenesis in human breast cancer. Sci Rep. 2015;5:8686.PubMedPubMedCentralCrossRef Chiang KC, Yeh CN, Chung LC, Feng TH, Sun CC, Chen MF, et al. WNT-1 inducible signaling pathway protein-1 enhances growth and tumorigenesis in human breast cancer. Sci Rep. 2015;5:8686.PubMedPubMedCentralCrossRef
7.
go back to reference Klinke DJ 2nd. Induction of Wnt-inducible signaling protein-1 correlates with invasive breast cancer oncogenesis and reduced type 1 cell-mediated cytotoxic immunity: a retrospective study. PLoS Comput Biol. 2014;10:e1003409.PubMedCrossRef Klinke DJ 2nd. Induction of Wnt-inducible signaling protein-1 correlates with invasive breast cancer oncogenesis and reduced type 1 cell-mediated cytotoxic immunity: a retrospective study. PLoS Comput Biol. 2014;10:e1003409.PubMedCrossRef
8.
go back to reference Chiang KC, Hsu SY, Lin SJ, Yeh CN, Pang JH, Wang SY, et al. PTEN insufficiency increases breast cancer cell metastasis in vitro and in vivo in a xenograft zebrafish model. Anticancer Res. 2016;36:3997–4005.PubMed Chiang KC, Hsu SY, Lin SJ, Yeh CN, Pang JH, Wang SY, et al. PTEN insufficiency increases breast cancer cell metastasis in vitro and in vivo in a xenograft zebrafish model. Anticancer Res. 2016;36:3997–4005.PubMed
9.
go back to reference Davies SR, Watkins G, Mansel RE, Jiang WG. Differential expression and prognostic implications of the CCN family members WISP-1, WISP-2, and WISP-3 in human breast cancer. Ann Surg Oncol. 2007;14:1909–18.PubMedCrossRef Davies SR, Watkins G, Mansel RE, Jiang WG. Differential expression and prognostic implications of the CCN family members WISP-1, WISP-2, and WISP-3 in human breast cancer. Ann Surg Oncol. 2007;14:1909–18.PubMedCrossRef
10.
go back to reference Taghavi A, Akbari ME, Hashemi-Bahremani M, Nafissi N, Khalilnezhad A, Poorhosseini SM, et al. Gene expression profiling of the 8q22-24 position in human breast cancer: TSPYL5, MTDH, ATAD2 and CCNE2 genes are implicated in oncogenesis, while WISP1 and EXT1 genes may predict a risk of metastasis. Oncol Lett. 2016;12:3845–55.PubMedPubMedCentralCrossRef Taghavi A, Akbari ME, Hashemi-Bahremani M, Nafissi N, Khalilnezhad A, Poorhosseini SM, et al. Gene expression profiling of the 8q22-24 position in human breast cancer: TSPYL5, MTDH, ATAD2 and CCNE2 genes are implicated in oncogenesis, while WISP1 and EXT1 genes may predict a risk of metastasis. Oncol Lett. 2016;12:3845–55.PubMedPubMedCentralCrossRef
11.
go back to reference Inadera H, Hashimoto S, Dong HY, Suzuki T, Nagai S, Yamashita T, et al. WISP-2 as a novel estrogen-responsive gene in human breast cancer cells. Biochem Biophys Res Commun. 2000;275:108–14.PubMedCrossRef Inadera H, Hashimoto S, Dong HY, Suzuki T, Nagai S, Yamashita T, et al. WISP-2 as a novel estrogen-responsive gene in human breast cancer cells. Biochem Biophys Res Commun. 2000;275:108–14.PubMedCrossRef
12.
go back to reference Inadera H, Dong HY, Matsushima K. WISP-2 is a secreted protein and can be a marker of estrogen exposure in MCF-7 cells. Biochem Biophys Res Commun. 2002;294:602–8.PubMedCrossRef Inadera H, Dong HY, Matsushima K. WISP-2 is a secreted protein and can be a marker of estrogen exposure in MCF-7 cells. Biochem Biophys Res Commun. 2002;294:602–8.PubMedCrossRef
13.
go back to reference Banerjee S, Saxena N, Sengupta K, Tawfik O, Mayo MS, Banerjee SK. WISP-2 gene in human breast cancer: estrogen and progesterone inducible expression and regulation of tumor cell proliferation. Neoplasia. 2003;5:63–73.PubMedPubMedCentralCrossRef Banerjee S, Saxena N, Sengupta K, Tawfik O, Mayo MS, Banerjee SK. WISP-2 gene in human breast cancer: estrogen and progesterone inducible expression and regulation of tumor cell proliferation. Neoplasia. 2003;5:63–73.PubMedPubMedCentralCrossRef
14.
go back to reference Inadera H. Estrogen-induced genes, WISP-2 and pS2, respond divergently to protein kinase pathway. Biochem Biophys Res Commun. 2003;309:272–8.PubMedCrossRef Inadera H. Estrogen-induced genes, WISP-2 and pS2, respond divergently to protein kinase pathway. Biochem Biophys Res Commun. 2003;309:272–8.PubMedCrossRef
15.
go back to reference Zoubine MN, Banerjee S, Saxena NK, Campbell DR, Banerjee SK. WISP-2: a serum-inducible gene differentially expressed in human normal breast epithelial cells and in MCF-7 breast tumor cells. Biochem Biophys Res Commun. 2001;282:421–5.PubMedCrossRef Zoubine MN, Banerjee S, Saxena NK, Campbell DR, Banerjee SK. WISP-2: a serum-inducible gene differentially expressed in human normal breast epithelial cells and in MCF-7 breast tumor cells. Biochem Biophys Res Commun. 2001;282:421–5.PubMedCrossRef
16.
go back to reference Banerjee S, Dhar G, Haque I, Kambhampati S, Mehta S, Sengupta K, et al. CCN5/WISP-2 expression in breast adenocarcinoma is associated with less frequent progression of the disease and suppresses the invasive phenotypes of tumor cells. Can Res. 2008;68:7606–12.CrossRef Banerjee S, Dhar G, Haque I, Kambhampati S, Mehta S, Sengupta K, et al. CCN5/WISP-2 expression in breast adenocarcinoma is associated with less frequent progression of the disease and suppresses the invasive phenotypes of tumor cells. Can Res. 2008;68:7606–12.CrossRef
17.
go back to reference Dhar G, Banerjee S, Dhar K, Tawfik O, Mayo MS, Vanveldhuizen PJ, et al. Gain of oncogenic function of p53 mutants induces invasive phenotypes in human breast cancer cells by silencing CCN5/WISP-2. Can Res. 2008;68:4580–7.CrossRef Dhar G, Banerjee S, Dhar K, Tawfik O, Mayo MS, Vanveldhuizen PJ, et al. Gain of oncogenic function of p53 mutants induces invasive phenotypes in human breast cancer cells by silencing CCN5/WISP-2. Can Res. 2008;68:4580–7.CrossRef
18.
go back to reference Noman MZ, Janji B, Abdou A, Hasmim M, Terry S, Tan TZ, et al. The immune checkpoint ligand PD-L1 is upregulated in EMT-activated human breast cancer cells by a mechanism involving ZEB-1 and miR-200. Oncoimmunology. 2017;6:e1263412.PubMedPubMedCentralCrossRef Noman MZ, Janji B, Abdou A, Hasmim M, Terry S, Tan TZ, et al. The immune checkpoint ligand PD-L1 is upregulated in EMT-activated human breast cancer cells by a mechanism involving ZEB-1 and miR-200. Oncoimmunology. 2017;6:e1263412.PubMedPubMedCentralCrossRef
19.
go back to reference Haque I, Banerjee S, De A, Maity G, Sarkar S, Majumdar M, et al. CCN5/WISP-2 promotes growth arrest of triple-negative breast cancer cells through accumulation and trafficking of p27(Kip1) via Skp2 and FOXO3a regulation. Oncogene. 2015;34:3152–63.PubMedCrossRef Haque I, Banerjee S, De A, Maity G, Sarkar S, Majumdar M, et al. CCN5/WISP-2 promotes growth arrest of triple-negative breast cancer cells through accumulation and trafficking of p27(Kip1) via Skp2 and FOXO3a regulation. Oncogene. 2015;34:3152–63.PubMedCrossRef
20.
go back to reference Fritah A, Saucier C, De Wever O, Bracke M, Bieche I, Lidereau R, et al. Role of WISP-2/CCN5 in the maintenance of a differentiated and noninvasive phenotype in human breast cancer cells. Mol Cell Biol. 2008;28:1114–23.PubMedCrossRef Fritah A, Saucier C, De Wever O, Bracke M, Bieche I, Lidereau R, et al. Role of WISP-2/CCN5 in the maintenance of a differentiated and noninvasive phenotype in human breast cancer cells. Mol Cell Biol. 2008;28:1114–23.PubMedCrossRef
21.
go back to reference Ferrand N, Gnanapragasam A, Dorothee G, Redeuilh G, Larsen AK, Sabbah M. Loss of WISP2/CCN5 in estrogen-dependent MCF7 human breast cancer cells promotes a stem-like cell phenotype. PLoS ONE. 2014;9:e87878.PubMedPubMedCentralCrossRef Ferrand N, Gnanapragasam A, Dorothee G, Redeuilh G, Larsen AK, Sabbah M. Loss of WISP2/CCN5 in estrogen-dependent MCF7 human breast cancer cells promotes a stem-like cell phenotype. PLoS ONE. 2014;9:e87878.PubMedPubMedCentralCrossRef
22.
go back to reference van Golen KL, Davies S, Wu ZF, Wang Y, Bucana CD, Root H, et al. A novel putative low-affinity insulin-like growth factor-binding protein, LIBC (lost in inflammatory breast cancer), and RhoC GTPase correlate with the inflammatory breast cancer phenotype. Clin Cancer Res. 1999;5:2511–9.PubMed van Golen KL, Davies S, Wu ZF, Wang Y, Bucana CD, Root H, et al. A novel putative low-affinity insulin-like growth factor-binding protein, LIBC (lost in inflammatory breast cancer), and RhoC GTPase correlate with the inflammatory breast cancer phenotype. Clin Cancer Res. 1999;5:2511–9.PubMed
23.
go back to reference Kleer CG, Zhang Y, Pan Q, van Golen KL, Wu ZF, Livant D, et al. WISP3 is a novel tumor suppressor gene of inflammatory breast cancer. Oncogene. 2002;21:3172–80.PubMedCrossRef Kleer CG, Zhang Y, Pan Q, van Golen KL, Wu ZF, Livant D, et al. WISP3 is a novel tumor suppressor gene of inflammatory breast cancer. Oncogene. 2002;21:3172–80.PubMedCrossRef
24.
go back to reference Kleer CG, Zhang Y, Pan Q, Gallagher G, Wu M, Wu ZF, et al. WISP3 and RhoC guanosine triphosphatase cooperate in the development of inflammatory breast cancer. Breast Cancer Res BCR. 2004;6:R110–5.PubMedCrossRef Kleer CG, Zhang Y, Pan Q, Gallagher G, Wu M, Wu ZF, et al. WISP3 and RhoC guanosine triphosphatase cooperate in the development of inflammatory breast cancer. Breast Cancer Res BCR. 2004;6:R110–5.PubMedCrossRef
25.
go back to reference Huang W, Zhang Y, Varambally S, Chinnaiyan AM, Banerjee M, Merajver SD, et al. Inhibition of CCN6 (Wnt-1-induced signaling protein 3) down-regulates E-cadherin in the breast epithelium through induction of snail and ZEB1. Am J Pathol. 2008;172:893–904.PubMedPubMedCentralCrossRef Huang W, Zhang Y, Varambally S, Chinnaiyan AM, Banerjee M, Merajver SD, et al. Inhibition of CCN6 (Wnt-1-induced signaling protein 3) down-regulates E-cadherin in the breast epithelium through induction of snail and ZEB1. Am J Pathol. 2008;172:893–904.PubMedPubMedCentralCrossRef
26.
go back to reference Zhang Y, Pan Q, Zhong H, Merajver SD, Kleer CG. Inhibition of CCN6 (WISP3) expression promotes neoplastic progression and enhances the effects of insulin-like growth factor-1 on breast epithelial cells. Breast Cancer Res BCR. 2005;7:R1080–9.PubMedCrossRef Zhang Y, Pan Q, Zhong H, Merajver SD, Kleer CG. Inhibition of CCN6 (WISP3) expression promotes neoplastic progression and enhances the effects of insulin-like growth factor-1 on breast epithelial cells. Breast Cancer Res BCR. 2005;7:R1080–9.PubMedCrossRef
27.
go back to reference Hayes MJ, Thomas D, Emmons A, Giordano TJ, Kleer CG. Genetic changes of Wnt pathway genes are common events in metaplastic carcinomas of the breast. Clin Cancer Res. 2008;14:4038–44.PubMedPubMedCentralCrossRef Hayes MJ, Thomas D, Emmons A, Giordano TJ, Kleer CG. Genetic changes of Wnt pathway genes are common events in metaplastic carcinomas of the breast. Clin Cancer Res. 2008;14:4038–44.PubMedPubMedCentralCrossRef
28.
go back to reference Huang W, Gonzalez ME, Toy KA, Banerjee M, Kleer CG. Blockade of CCN6 (WISP3) activates growth factor-independent survival and resistance to anoikis in human mammary epithelial cells. Cancer Res. 2010;70:3340–50.PubMedPubMedCentralCrossRef Huang W, Gonzalez ME, Toy KA, Banerjee M, Kleer CG. Blockade of CCN6 (WISP3) activates growth factor-independent survival and resistance to anoikis in human mammary epithelial cells. Cancer Res. 2010;70:3340–50.PubMedPubMedCentralCrossRef
29.
go back to reference Kleer CG, Zhang Y, Pan Q, Merajver SD. WISP3 (CCN6) is a secreted tumor-suppressor protein that modulates IGF signaling in inflammatory breast cancer. Neoplasia. 2004;6:179–85.PubMedPubMedCentralCrossRef Kleer CG, Zhang Y, Pan Q, Merajver SD. WISP3 (CCN6) is a secreted tumor-suppressor protein that modulates IGF signaling in inflammatory breast cancer. Neoplasia. 2004;6:179–85.PubMedPubMedCentralCrossRef
30.
go back to reference Lorenzatti G, Huang W, Pal A, Cabanillas AM, Kleer CG. CCN6 (WISP3) decreases ZEB1-mediated EMT and invasion by attenuation of IGF-1 receptor signaling in breast cancer. J Cell Sci. 2011;124:1752–8.PubMedPubMedCentralCrossRef Lorenzatti G, Huang W, Pal A, Cabanillas AM, Kleer CG. CCN6 (WISP3) decreases ZEB1-mediated EMT and invasion by attenuation of IGF-1 receptor signaling in breast cancer. J Cell Sci. 2011;124:1752–8.PubMedPubMedCentralCrossRef
31.
go back to reference Pal A, Huang W, Li X, Toy KA, Nikolovska-Coleska Z, Kleer CG. CCN6 modulates BMP signaling via the Smad-independent TAK1/p38 pathway, acting to suppress metastasis of breast cancer. Cancer Res. 2012;72:4818–28.PubMedPubMedCentralCrossRef Pal A, Huang W, Li X, Toy KA, Nikolovska-Coleska Z, Kleer CG. CCN6 modulates BMP signaling via the Smad-independent TAK1/p38 pathway, acting to suppress metastasis of breast cancer. Cancer Res. 2012;72:4818–28.PubMedPubMedCentralCrossRef
32.
go back to reference Pal A, Huang W, Toy KA, Kleer CG. CCN6 knockdown disrupts acinar organization of breast cells in three-dimensional cultures through up-regulation of type III TGF-beta receptor. Neoplasia. 2012;14:1067–74.PubMedPubMedCentralCrossRef Pal A, Huang W, Toy KA, Kleer CG. CCN6 knockdown disrupts acinar organization of breast cells in three-dimensional cultures through up-regulation of type III TGF-beta receptor. Neoplasia. 2012;14:1067–74.PubMedPubMedCentralCrossRef
33.
go back to reference Huang W, Martin EE, Burman B, Gonzalez ME, Kleer CG. The matricellular protein CCN6 (WISP3) decreases Notch1 and suppresses breast cancer initiating cells. Oncotarget. 2016;7:25180–93.PubMedPubMedCentral Huang W, Martin EE, Burman B, Gonzalez ME, Kleer CG. The matricellular protein CCN6 (WISP3) decreases Notch1 and suppresses breast cancer initiating cells. Oncotarget. 2016;7:25180–93.PubMedPubMedCentral
34.
go back to reference Martin EE, Huang W, Anwar T, Arellano-Garcia C, Burman B, Guan JL, et al. MMTV-cre;Ccn6 knockout mice develop tumors recapitulating human metaplastic breast carcinomas. Oncogene. 2017;36:2275–85.PubMedCrossRef Martin EE, Huang W, Anwar T, Arellano-Garcia C, Burman B, Guan JL, et al. MMTV-cre;Ccn6 knockout mice develop tumors recapitulating human metaplastic breast carcinomas. Oncogene. 2017;36:2275–85.PubMedCrossRef
35.
go back to reference Cervello M, Giannitrapani L, Labbozzetta M, Notarbartolo M, D’Alessandro N, Lampiasi N, et al. Expression of WISPs and of their novel alternative variants in human hepatocellular carcinoma cells. Ann NY Acad Sci. 2004;1028:432–9.PubMedCrossRef Cervello M, Giannitrapani L, Labbozzetta M, Notarbartolo M, D’Alessandro N, Lampiasi N, et al. Expression of WISPs and of their novel alternative variants in human hepatocellular carcinoma cells. Ann NY Acad Sci. 2004;1028:432–9.PubMedCrossRef
36.
go back to reference Calvisi DF, Conner EA, Ladu S, Lemmer ER, Factor VM, Thorgeirsson SS. Activation of the canonical Wnt/beta-catenin pathway confers growth advantages in c-Myc/E2F1 transgenic mouse model of liver cancer. J Hepatol. 2005;42:842–9.PubMedCrossRef Calvisi DF, Conner EA, Ladu S, Lemmer ER, Factor VM, Thorgeirsson SS. Activation of the canonical Wnt/beta-catenin pathway confers growth advantages in c-Myc/E2F1 transgenic mouse model of liver cancer. J Hepatol. 2005;42:842–9.PubMedCrossRef
37.
go back to reference Ge J, Zhang XH, Wang F, Wang Y, Li QY, Tao W, et al. Effect of siRNA on Wisp-1 gene expression, proliferation, migration and adhesion of mouse hepatocellular carcinoma cells. Asian Pac J Trop Med. 2015;8:821–8.PubMedCrossRef Ge J, Zhang XH, Wang F, Wang Y, Li QY, Tao W, et al. Effect of siRNA on Wisp-1 gene expression, proliferation, migration and adhesion of mouse hepatocellular carcinoma cells. Asian Pac J Trop Med. 2015;8:821–8.PubMedCrossRef
38.
go back to reference Zhang H, Li W, Huang P, Lin L, Ye H, Lin D, et al. Expression of CCN family members correlates with the clinical features of hepatocellular carcinoma. Oncol Rep. 2015;33:1481–92.PubMedCrossRef Zhang H, Li W, Huang P, Lin L, Ye H, Lin D, et al. Expression of CCN family members correlates with the clinical features of hepatocellular carcinoma. Oncol Rep. 2015;33:1481–92.PubMedCrossRef
39.
go back to reference Fukutomi T, Zhou Y, Kawai S, Eguchi H, Wands JR, Li J. Hepatitis C virus core protein stimulates hepatocyte growth: correlation with upregulation of wnt-1 expression. Hepatology. 2005;41:1096–105.PubMedCrossRef Fukutomi T, Zhou Y, Kawai S, Eguchi H, Wands JR, Li J. Hepatitis C virus core protein stimulates hepatocyte growth: correlation with upregulation of wnt-1 expression. Hepatology. 2005;41:1096–105.PubMedCrossRef
40.
go back to reference Liu J, Ding X, Tang J, Cao Y, Hu P, Zhou F, et al. Enhancement of canonical Wnt/beta-catenin signaling activity by HCV core protein promotes cell growth of hepatocellular carcinoma cells. PLoS ONE. 2011;6:e27496.PubMedPubMedCentralCrossRef Liu J, Ding X, Tang J, Cao Y, Hu P, Zhou F, et al. Enhancement of canonical Wnt/beta-catenin signaling activity by HCV core protein promotes cell growth of hepatocellular carcinoma cells. PLoS ONE. 2011;6:e27496.PubMedPubMedCentralCrossRef
41.
go back to reference Chen Z, Tang J, Cai X, Huang Y, Gao Q, Liang L, et al. HBx mutations promote hepatoma cell migration through the Wnt/beta-catenin signaling pathway. Cancer Sci. 2016;107:1380–9.PubMedPubMedCentralCrossRef Chen Z, Tang J, Cai X, Huang Y, Gao Q, Liang L, et al. HBx mutations promote hepatoma cell migration through the Wnt/beta-catenin signaling pathway. Cancer Sci. 2016;107:1380–9.PubMedPubMedCentralCrossRef
42.
go back to reference Anastas JN, Moon RT. WNT signalling pathways as therapeutic targets in cancer. Nat Rev Cancer. 2013;13:11–26.CrossRefPubMed Anastas JN, Moon RT. WNT signalling pathways as therapeutic targets in cancer. Nat Rev Cancer. 2013;13:11–26.CrossRefPubMed
44.
go back to reference Tomimaru Y, Koga H, Yano H, de la Monte S, Wands JR, Kim M. Upregulation of T-cell factor-4 isoform-responsive target genes in hepatocellular carcinoma. Liver Int. 2013;33:1100–12.PubMedPubMedCentralCrossRef Tomimaru Y, Koga H, Yano H, de la Monte S, Wands JR, Kim M. Upregulation of T-cell factor-4 isoform-responsive target genes in hepatocellular carcinoma. Liver Int. 2013;33:1100–12.PubMedPubMedCentralCrossRef
45.
go back to reference Fischer H, Salahshor S, Stenling R, Bjork J, Lindmark G, Iselius L, et al. COL11A1 in FAP polyps and in sporadic colorectal tumors. BMC Cancer. 2001;1:17.PubMedPubMedCentralCrossRef Fischer H, Salahshor S, Stenling R, Bjork J, Lindmark G, Iselius L, et al. COL11A1 in FAP polyps and in sporadic colorectal tumors. BMC Cancer. 2001;1:17.PubMedPubMedCentralCrossRef
46.
go back to reference Wang J, Zhang GY, Li XH. Effect of indomethacin on Bfl-1, WISP-1 and proliferating cell nuclear antigen in colon cancer cell line HCT116 cells. Chin J Dig Dis. 2006;7:219–24.PubMedCrossRef Wang J, Zhang GY, Li XH. Effect of indomethacin on Bfl-1, WISP-1 and proliferating cell nuclear antigen in colon cancer cell line HCT116 cells. Chin J Dig Dis. 2006;7:219–24.PubMedCrossRef
47.
go back to reference Lin H, Liu W, Fang Z, Liang X, Li J, Bai Y, et al. Overexpression of DHX32 contributes to the growth and metastasis of colorectal cancer. Sci Rep. 2015;5:9247.PubMedPubMedCentralCrossRef Lin H, Liu W, Fang Z, Liang X, Li J, Bai Y, et al. Overexpression of DHX32 contributes to the growth and metastasis of colorectal cancer. Sci Rep. 2015;5:9247.PubMedPubMedCentralCrossRef
48.
go back to reference Wu J, Long Z, Cai H, Du C, Liu X, Yu S, et al. High expression of WISP1 in colon cancer is associated with apoptosis, invasion and poor prognosis. Oncotarget. 2016;7:49834–47.PubMedPubMedCentral Wu J, Long Z, Cai H, Du C, Liu X, Yu S, et al. High expression of WISP1 in colon cancer is associated with apoptosis, invasion and poor prognosis. Oncotarget. 2016;7:49834–47.PubMedPubMedCentral
49.
go back to reference Lee JH, Choi YJ, Je EM, Kim HS, Yoo NJ, Lee SH. Frameshift mutation of WISP3 gene and its regional heterogeneity in gastric and colorectal cancers. Hum Pathol. 2016;50:146–52.PubMedCrossRef Lee JH, Choi YJ, Je EM, Kim HS, Yoo NJ, Lee SH. Frameshift mutation of WISP3 gene and its regional heterogeneity in gastric and colorectal cancers. Hum Pathol. 2016;50:146–52.PubMedCrossRef
50.
go back to reference Jia S, Qu T, Feng M, Ji K, Li Z, Jiang W, et al. Association of Wnt1-inducible signaling pathway protein-1 with the proliferation, migration and invasion in gastric cancer cells. Tumour Biol. 2017;39:1010428317699755.PubMedCrossRef Jia S, Qu T, Feng M, Ji K, Li Z, Jiang W, et al. Association of Wnt1-inducible signaling pathway protein-1 with the proliferation, migration and invasion in gastric cancer cells. Tumour Biol. 2017;39:1010428317699755.PubMedCrossRef
51.
go back to reference Ji J, Jia S, Jia Y, Ji K, Hargest R, Jiang WG. WISP-2 in human gastric cancer and its potential metastatic suppressor role in gastric cancer cells mediated by JNK and PLC-gamma pathways. Br J Cancer. 2015;113:921–33.PubMedPubMedCentralCrossRef Ji J, Jia S, Jia Y, Ji K, Hargest R, Jiang WG. WISP-2 in human gastric cancer and its potential metastatic suppressor role in gastric cancer cells mediated by JNK and PLC-gamma pathways. Br J Cancer. 2015;113:921–33.PubMedPubMedCentralCrossRef
52.
go back to reference Li L, Cui Y, Ji JF, Jiang WG. Clinical Correlation Between WISP2 and beta-Catenin in Gastric Cancer. Anticancer Res. 2017;37:4469–73.PubMed Li L, Cui Y, Ji JF, Jiang WG. Clinical Correlation Between WISP2 and beta-Catenin in Gastric Cancer. Anticancer Res. 2017;37:4469–73.PubMed
53.
go back to reference Tanaka S, Sugimachi K, Maehara S, Shimada M, Maehara Y. A loss of function mutation in WISP3 derived from microsatellite unstable gastric carcinoma. Gastroenterology. 2003;125:1563–4.PubMedCrossRef Tanaka S, Sugimachi K, Maehara S, Shimada M, Maehara Y. A loss of function mutation in WISP3 derived from microsatellite unstable gastric carcinoma. Gastroenterology. 2003;125:1563–4.PubMedCrossRef
54.
go back to reference Fang F, Zhao WY, Li RK, Yang XM, Li J, Ao JP, et al. Silencing of WISP3 suppresses gastric cancer cell proliferation and metastasis and inhibits Wnt/beta-catenin signaling. Int J Clin Exp Pathol. 2014;7:6447–61.PubMedPubMedCentral Fang F, Zhao WY, Li RK, Yang XM, Li J, Ao JP, et al. Silencing of WISP3 suppresses gastric cancer cell proliferation and metastasis and inhibits Wnt/beta-catenin signaling. Int J Clin Exp Pathol. 2014;7:6447–61.PubMedPubMedCentral
55.
go back to reference Wang Q, Liu H, Liu T, Shu S, Jiang H, Cheng S, et al. BRCA2 dysfunction promotes malignant transformation of pancreatic intraepithelial neoplasia. Anticancer Agents Med Chem. 2013;13:261–9.PubMedCrossRef Wang Q, Liu H, Liu T, Shu S, Jiang H, Cheng S, et al. BRCA2 dysfunction promotes malignant transformation of pancreatic intraepithelial neoplasia. Anticancer Agents Med Chem. 2013;13:261–9.PubMedCrossRef
56.
go back to reference Ghosh P, Banerjee S, Maity G, De A, Banerjee SK. Detection of CCN1 and CCN5 mRNA in human cancer samples using a modified in situ hybridization technique. Methods Mol Biol. 2017;1489:495–504.PubMedCrossRef Ghosh P, Banerjee S, Maity G, De A, Banerjee SK. Detection of CCN1 and CCN5 mRNA in human cancer samples using a modified in situ hybridization technique. Methods Mol Biol. 2017;1489:495–504.PubMedCrossRef
57.
go back to reference Dhar G, Mehta S, Banerjee S, Gardner A, McCarty BM, Mathur SC, et al. Loss of WISP-2/CCN5 signaling in human pancreatic cancer: a potential mechanism for epithelial–mesenchymal-transition. Cancer Lett. 2007;254:63–70.PubMedCrossRef Dhar G, Mehta S, Banerjee S, Gardner A, McCarty BM, Mathur SC, et al. Loss of WISP-2/CCN5 signaling in human pancreatic cancer: a potential mechanism for epithelial–mesenchymal-transition. Cancer Lett. 2007;254:63–70.PubMedCrossRef
58.
go back to reference Wu MY, Xie X, Xu ZK, Xie L, Chen Z, Shou LM, et al. PP2A inhibitors suppress migration and growth of PANC-1 pancreatic cancer cells through inhibition on the Wnt/beta-catenin pathway by phosphorylation and degradation of beta-catenin. Oncol Rep. 2014;32:513–22.PubMedPubMedCentralCrossRef Wu MY, Xie X, Xu ZK, Xie L, Chen Z, Shou LM, et al. PP2A inhibitors suppress migration and growth of PANC-1 pancreatic cancer cells through inhibition on the Wnt/beta-catenin pathway by phosphorylation and degradation of beta-catenin. Oncol Rep. 2014;32:513–22.PubMedPubMedCentralCrossRef
59.
go back to reference Soon LL, Yie TA, Shvarts A, Levine AJ, Su F, Tchou-Wong KM. Overexpression of WISP-1 down-regulated motility and invasion of lung cancer cells through inhibition of Rac activation. J Biol Chem. 2003;278:11465–70.PubMedCrossRef Soon LL, Yie TA, Shvarts A, Levine AJ, Su F, Tchou-Wong KM. Overexpression of WISP-1 down-regulated motility and invasion of lung cancer cells through inhibition of Rac activation. J Biol Chem. 2003;278:11465–70.PubMedCrossRef
60.
go back to reference Matsubara D, Niki T, Ishikawa S, Goto A, Ohara E, Yokomizo T, et al. Differential expression of S100A2 and S100A4 in lung adenocarcinomas: clinicopathological significance, relationship to p53 and identification of their target genes. Cancer Sci. 2005;96:844–57.PubMedCrossRef Matsubara D, Niki T, Ishikawa S, Goto A, Ohara E, Yokomizo T, et al. Differential expression of S100A2 and S100A4 in lung adenocarcinomas: clinicopathological significance, relationship to p53 and identification of their target genes. Cancer Sci. 2005;96:844–57.PubMedCrossRef
61.
go back to reference Chen PP, Li WJ, Wang Y, Zhao S, Li DY, Feng LY, et al. Expression of Cyr61, CTGF, and WISP-1 correlates with clinical features of lung cancer. PLoS ONE. 2007;2:e534.PubMedPubMedCentralCrossRef Chen PP, Li WJ, Wang Y, Zhao S, Li DY, Feng LY, et al. Expression of Cyr61, CTGF, and WISP-1 correlates with clinical features of lung cancer. PLoS ONE. 2007;2:e534.PubMedPubMedCentralCrossRef
62.
go back to reference Chen J, Yin J, Li X, Wang Y, Zheng Y, Qian C, et al. WISP1 polymorphisms contribute to platinum-based chemotherapy toxicity in lung cancer patients. Int J Mol Sci. 2014;15:21011–27.PubMedPubMedCentralCrossRef Chen J, Yin J, Li X, Wang Y, Zheng Y, Qian C, et al. WISP1 polymorphisms contribute to platinum-based chemotherapy toxicity in lung cancer patients. Int J Mol Sci. 2014;15:21011–27.PubMedPubMedCentralCrossRef
63.
go back to reference Chen J, Yin JY, Li XP, Wang Y, Zheng Y, Qian CY, et al. Association of Wnt-inducible signaling pathway protein 1 genetic polymorphisms with lung cancer susceptibility and platinum-based chemotherapy response. Clin Lung Cancer. 2015;16(298–304):e1–2. Chen J, Yin JY, Li XP, Wang Y, Zheng Y, Qian CY, et al. Association of Wnt-inducible signaling pathway protein 1 genetic polymorphisms with lung cancer susceptibility and platinum-based chemotherapy response. Clin Lung Cancer. 2015;16(298–304):e1–2.
64.
go back to reference Margalit O, Eisenbach L, Amariglio N, Kaminski N, Harmelin A, Pfeffer R, et al. Overexpression of a set of genes, including WISP-1, common to pulmonary metastases of both mouse D122 Lewis lung carcinoma and B16-F10.9 melanoma cell lines. Br J Cancer. 2003;89:314–9.PubMedPubMedCentralCrossRef Margalit O, Eisenbach L, Amariglio N, Kaminski N, Harmelin A, Pfeffer R, et al. Overexpression of a set of genes, including WISP-1, common to pulmonary metastases of both mouse D122 Lewis lung carcinoma and B16-F10.9 melanoma cell lines. Br J Cancer. 2003;89:314–9.PubMedPubMedCentralCrossRef
65.
go back to reference Zhang YW, Zheng Y, Wang JZ, Lu XX, Wang Z, Chen LB, et al. Integrated analysis of DNA methylation and mRNA expression profiling reveals candidate genes associated with cisplatin resistance in non-small cell lung cancer. Epigenetics. 2014;9:896–909.PubMedPubMedCentralCrossRef Zhang YW, Zheng Y, Wang JZ, Lu XX, Wang Z, Chen LB, et al. Integrated analysis of DNA methylation and mRNA expression profiling reveals candidate genes associated with cisplatin resistance in non-small cell lung cancer. Epigenetics. 2014;9:896–909.PubMedPubMedCentralCrossRef
66.
go back to reference Zhang Y, Wang X, Han L, Zhou Y, Sun S. Green tea polyphenol EGCG reverse cisplatin resistance of A549/DDP cell line through candidate genes demethylation. Biomed Pharmacother. 2015;69:285–90.PubMedCrossRef Zhang Y, Wang X, Han L, Zhou Y, Sun S. Green tea polyphenol EGCG reverse cisplatin resistance of A549/DDP cell line through candidate genes demethylation. Biomed Pharmacother. 2015;69:285–90.PubMedCrossRef
67.
go back to reference Renieri A, Mencarelli MA, Cetta F, Baldassarri M, Mari F, Furini S, et al. Oligogenic germline mutations identified in early non-smokers lung adenocarcinoma patients. Lung Cancer. 2014;85:168–74.PubMedCrossRef Renieri A, Mencarelli MA, Cetta F, Baldassarri M, Mari F, Furini S, et al. Oligogenic germline mutations identified in early non-smokers lung adenocarcinoma patients. Lung Cancer. 2014;85:168–74.PubMedCrossRef
68.
go back to reference Shao H, Cai L, Grichnik JM, Livingstone AS, Velazquez OC, Liu ZJ. Activation of Notch1 signaling in stromal fibroblasts inhibits melanoma growth by upregulating WISP-1. Oncogene. 2011;30:4316–26.PubMedCrossRef Shao H, Cai L, Grichnik JM, Livingstone AS, Velazquez OC, Liu ZJ. Activation of Notch1 signaling in stromal fibroblasts inhibits melanoma growth by upregulating WISP-1. Oncogene. 2011;30:4316–26.PubMedCrossRef
69.
go back to reference Kulkarni YM, Chambers E, McGray AJ, Ware JS, Bramson JL, Klinke DJ 2nd. A quantitative systems approach to identify paracrine mechanisms that locally suppress immune response to Interleukin-12 in the B16 melanoma model. Integr Biol (Camb). 2012;4:925–36.PubMedPubMedCentralCrossRef Kulkarni YM, Chambers E, McGray AJ, Ware JS, Bramson JL, Klinke DJ 2nd. A quantitative systems approach to identify paracrine mechanisms that locally suppress immune response to Interleukin-12 in the B16 melanoma model. Integr Biol (Camb). 2012;4:925–36.PubMedPubMedCentralCrossRef
70.
go back to reference Shao H, Cai L, Moller M, Issac B, Zhang L, Owyong M, et al. Notch1-WISP-1 axis determines the regulatory role of mesenchymal stem cell-derived stromal fibroblasts in melanoma metastasis. Oncotarget. 2016;7:79262–73.PubMedPubMedCentral Shao H, Cai L, Moller M, Issac B, Zhang L, Owyong M, et al. Notch1-WISP-1 axis determines the regulatory role of mesenchymal stem cell-derived stromal fibroblasts in melanoma metastasis. Oncotarget. 2016;7:79262–73.PubMedPubMedCentral
71.
go back to reference Moore SR, Persons DL, Sosman JA, Bobadilla D, Bedell V, Smith DD, et al. Detection of copy number alterations in metastatic melanoma by a DNA fluorescence in situ hybridization probe panel and array comparative genomic hybridization: a southwest oncology group study (S9431). Clin Cancer Res. 2008;14:2927–35.PubMedCrossRef Moore SR, Persons DL, Sosman JA, Bobadilla D, Bedell V, Smith DD, et al. Detection of copy number alterations in metastatic melanoma by a DNA fluorescence in situ hybridization probe panel and array comparative genomic hybridization: a southwest oncology group study (S9431). Clin Cancer Res. 2008;14:2927–35.PubMedCrossRef
72.
go back to reference Ono M, Inkson CA, Sonn R, Kilts TM, de Castro LF, Maeda A, et al. WISP1/CCN4: a potential target for inhibiting prostate cancer growth and spread to bone. PLoS ONE. 2013;8:e71709.PubMedPubMedCentralCrossRef Ono M, Inkson CA, Sonn R, Kilts TM, de Castro LF, Maeda A, et al. WISP1/CCN4: a potential target for inhibiting prostate cancer growth and spread to bone. PLoS ONE. 2013;8:e71709.PubMedPubMedCentralCrossRef
73.
go back to reference Tai HC, Chang AC, Yu HJ, Huang CY, Tsai YC, Lai YW, et al. Osteoblast-derived WNT-induced secreted protein 1 increases VCAM-1 expression and enhances prostate cancer metastasis by down-regulating miR-126. Oncotarget. 2014;5:7589–98.PubMedPubMedCentralCrossRef Tai HC, Chang AC, Yu HJ, Huang CY, Tsai YC, Lai YW, et al. Osteoblast-derived WNT-induced secreted protein 1 increases VCAM-1 expression and enhances prostate cancer metastasis by down-regulating miR-126. Oncotarget. 2014;5:7589–98.PubMedPubMedCentralCrossRef
74.
go back to reference Chang AC, Chen PC, Lin YF, Su CM, Liu JF, Lin TH, et al. Osteoblast-secreted WISP-1 promotes adherence of prostate cancer cells to bone via the VCAM-1/integrin alpha4beta1 system. Cancer Lett. 2018;426:47–56.PubMedCrossRef Chang AC, Chen PC, Lin YF, Su CM, Liu JF, Lin TH, et al. Osteoblast-secreted WISP-1 promotes adherence of prostate cancer cells to bone via the VCAM-1/integrin alpha4beta1 system. Cancer Lett. 2018;426:47–56.PubMedCrossRef
75.
go back to reference Jung EK, Kim SA, Yoon TM, Lee KH, Kim HK, Lee DH, et al. WNT1-inducible signaling pathway protein-1 contributes to tumor progression and treatment failure in oral squamous cell carcinoma. Oncol Lett. 2017;14:1719–24.PubMedPubMedCentralCrossRef Jung EK, Kim SA, Yoon TM, Lee KH, Kim HK, Lee DH, et al. WNT1-inducible signaling pathway protein-1 contributes to tumor progression and treatment failure in oral squamous cell carcinoma. Oncol Lett. 2017;14:1719–24.PubMedPubMedCentralCrossRef
76.
go back to reference Chuang JY, Chang AC, Chiang IP, Tsai MH, Tang CH. Apoptosis signal-regulating kinase 1 is involved in WISP-1-promoted cell motility in human oral squamous cell carcinoma cells. PLoS ONE. 2013;8:e78022.PubMedPubMedCentralCrossRef Chuang JY, Chang AC, Chiang IP, Tsai MH, Tang CH. Apoptosis signal-regulating kinase 1 is involved in WISP-1-promoted cell motility in human oral squamous cell carcinoma cells. PLoS ONE. 2013;8:e78022.PubMedPubMedCentralCrossRef
77.
go back to reference Chuang JY, Chen PC, Tsao CW, Chang AC, Lein MY, Lin CC, et al. WISP-1 a novel angiogenic regulator of the CCN family promotes oral squamous cell carcinoma angiogenesis through VEGF-A expression. Oncotarget. 2015;6:4239–52.PubMedPubMedCentral Chuang JY, Chen PC, Tsao CW, Chang AC, Lein MY, Lin CC, et al. WISP-1 a novel angiogenic regulator of the CCN family promotes oral squamous cell carcinoma angiogenesis through VEGF-A expression. Oncotarget. 2015;6:4239–52.PubMedPubMedCentral
78.
go back to reference Clausen MJ, Melchers LJ, Mastik MF, Slagter-Menkema L, Groen HJ, van der Laan BF, et al. Identification and validation of WISP1 as an epigenetic regulator of metastasis in oral squamous cell carcinoma. Genes Chromosom Cancer. 2016;55:45–59.PubMedCrossRef Clausen MJ, Melchers LJ, Mastik MF, Slagter-Menkema L, Groen HJ, van der Laan BF, et al. Identification and validation of WISP1 as an epigenetic regulator of metastasis in oral squamous cell carcinoma. Genes Chromosom Cancer. 2016;55:45–59.PubMedCrossRef
79.
go back to reference Lin CC, Chen PC, Lein MY, Tsao CW, Huang CC, Wang SW, et al. WISP-1 promotes VEGF-C-dependent lymphangiogenesis by inhibiting miR-300 in human oral squamous cell carcinoma cells. Oncotarget. 2016;7:9993–10005.PubMedPubMedCentral Lin CC, Chen PC, Lein MY, Tsao CW, Huang CC, Wang SW, et al. WISP-1 promotes VEGF-C-dependent lymphangiogenesis by inhibiting miR-300 in human oral squamous cell carcinoma cells. Oncotarget. 2016;7:9993–10005.PubMedPubMedCentral
80.
go back to reference Lau HK, Wu ER, Chen MK, Hsieh MJ, Yang SF, Wang LY, et al. Effect of genetic variation in microRNA binding site in WNT1-inducible signaling pathway protein 1 gene on oral squamous cell carcinoma susceptibility. PLoS ONE. 2017;12:e0176246.PubMedPubMedCentralCrossRef Lau HK, Wu ER, Chen MK, Hsieh MJ, Yang SF, Wang LY, et al. Effect of genetic variation in microRNA binding site in WNT1-inducible signaling pathway protein 1 gene on oral squamous cell carcinoma susceptibility. PLoS ONE. 2017;12:e0176246.PubMedPubMedCentralCrossRef
81.
go back to reference van Kempen PM, Noorlag R, Braunius WW, Moelans CB, Rifi W, Savola S, et al. Clinical relevance of copy number profiling in oral and oropharyngeal squamous cell carcinoma. Cancer Med. 2015;4:1525–35.PubMedPubMedCentralCrossRef van Kempen PM, Noorlag R, Braunius WW, Moelans CB, Rifi W, Savola S, et al. Clinical relevance of copy number profiling in oral and oropharyngeal squamous cell carcinoma. Cancer Med. 2015;4:1525–35.PubMedPubMedCentralCrossRef
82.
go back to reference Kouzu Y, Uzawa K, Kato M, Higo M, Nimura Y, Harada K, et al. WISP-2 expression in human salivary gland tumors. Int J Mol Med. 2006;17:567–73.PubMed Kouzu Y, Uzawa K, Kato M, Higo M, Nimura Y, Harada K, et al. WISP-2 expression in human salivary gland tumors. Int J Mol Med. 2006;17:567–73.PubMed
83.
go back to reference Nagai Y, Watanabe M, Ishikawa S, Karashima R, Kurashige J, Iwagami S, et al. Clinical significance of Wnt-induced secreted protein-1 (WISP-1/CCN4) in esophageal squamous cell carcinoma. Anticancer Res. 2011;31:991–7.PubMed Nagai Y, Watanabe M, Ishikawa S, Karashima R, Kurashige J, Iwagami S, et al. Clinical significance of Wnt-induced secreted protein-1 (WISP-1/CCN4) in esophageal squamous cell carcinoma. Anticancer Res. 2011;31:991–7.PubMed
84.
go back to reference Zhang H, Luo H, Hu Z, Peng J, Jiang Z, Song T, et al. Targeting WISP1 to sensitize esophageal squamous cell carcinoma to irradiation. Oncotarget. 2015;6:6218–34.PubMedPubMedCentral Zhang H, Luo H, Hu Z, Peng J, Jiang Z, Song T, et al. Targeting WISP1 to sensitize esophageal squamous cell carcinoma to irradiation. Oncotarget. 2015;6:6218–34.PubMedPubMedCentral
85.
go back to reference Li WF, Zhang L, Li HY, Zheng SS, Zhao L. WISP-1 contributes to fractionated irradiation-induced radioresistance in esophageal carcinoma cell lines and mice. PLoS ONE. 2014;9:e94751.PubMedPubMedCentralCrossRef Li WF, Zhang L, Li HY, Zheng SS, Zhao L. WISP-1 contributes to fractionated irradiation-induced radioresistance in esophageal carcinoma cell lines and mice. PLoS ONE. 2014;9:e94751.PubMedPubMedCentralCrossRef
86.
go back to reference Zhang H, Luo H, Jiang Z, Yue J, Hou Q, Xie R, et al. Fractionated irradiation-induced EMT-like phenotype conferred radioresistance in esophageal squamous cell carcinoma. J Radiat Res. 2016;57:370–80.PubMedPubMedCentralCrossRef Zhang H, Luo H, Jiang Z, Yue J, Hou Q, Xie R, et al. Fractionated irradiation-induced EMT-like phenotype conferred radioresistance in esophageal squamous cell carcinoma. J Radiat Res. 2016;57:370–80.PubMedPubMedCentralCrossRef
87.
go back to reference French DM, Kaul RJ, D’Souza AL, Crowley CW, Bao M, Frantz GD, et al. WISP-1 is an osteoblastic regulator expressed during skeletal development and fracture repair. Am J Pathol. 2004;165:855–67.PubMedPubMedCentralCrossRef French DM, Kaul RJ, D’Souza AL, Crowley CW, Bao M, Frantz GD, et al. WISP-1 is an osteoblastic regulator expressed during skeletal development and fracture repair. Am J Pathol. 2004;165:855–67.PubMedPubMedCentralCrossRef
88.
go back to reference Ono M, Inkson CA, Kilts TM, Young MF. WISP-1/CCN4 regulates osteogenesis by enhancing BMP-2 activity. J Bone Miner Res. 2011;26:193–208.PubMedCrossRef Ono M, Inkson CA, Kilts TM, Young MF. WISP-1/CCN4 regulates osteogenesis by enhancing BMP-2 activity. J Bone Miner Res. 2011;26:193–208.PubMedCrossRef
89.
go back to reference Kohara H, Tabata Y. Enhancement of ectopic osteoid formation following the dual release of bone morphogenetic protein 2 and Wnt1 inducible signaling pathway protein 1 from gelatin sponges. Biomaterials. 2011;32:5726–32.PubMedCrossRef Kohara H, Tabata Y. Enhancement of ectopic osteoid formation following the dual release of bone morphogenetic protein 2 and Wnt1 inducible signaling pathway protein 1 from gelatin sponges. Biomaterials. 2011;32:5726–32.PubMedCrossRef
90.
go back to reference Wu CL, Tsai HC, Chen ZW, Wu CM, Li TM, Fong YC, et al. Ras activation mediates WISP-1-induced increases in cell motility and matrix metalloproteinase expression in human osteosarcoma. Cell Signal. 2013;25:2812–22.PubMedCrossRef Wu CL, Tsai HC, Chen ZW, Wu CM, Li TM, Fong YC, et al. Ras activation mediates WISP-1-induced increases in cell motility and matrix metalloproteinase expression in human osteosarcoma. Cell Signal. 2013;25:2812–22.PubMedCrossRef
91.
go back to reference Tsai HC, Tzeng HE, Huang CY, Huang YL, Tsai CH, Wang SW, et al. WISP-1 positively regulates angiogenesis by controlling VEGF-A expression in human osteosarcoma. Cell Death Dis. 2017;8:e2750.PubMedPubMedCentralCrossRef Tsai HC, Tzeng HE, Huang CY, Huang YL, Tsai CH, Wang SW, et al. WISP-1 positively regulates angiogenesis by controlling VEGF-A expression in human osteosarcoma. Cell Death Dis. 2017;8:e2750.PubMedPubMedCentralCrossRef
92.
go back to reference Hou CH, Chiang YC, Fong YC, Tang CH. WISP-1 increases MMP-2 expression and cell motility in human chondrosarcoma cells. Biochem Pharmacol. 2011;81:1286–95.PubMedCrossRef Hou CH, Chiang YC, Fong YC, Tang CH. WISP-1 increases MMP-2 expression and cell motility in human chondrosarcoma cells. Biochem Pharmacol. 2011;81:1286–95.PubMedCrossRef
93.
go back to reference Yanagita T, Kubota S, Kawaki H, Kawata K, Kondo S, Takano-Yamamoto T, et al. Expression and physiological role of CCN4/Wnt-induced secreted protein 1 mRNA splicing variants in chondrocytes. FEBS J. 2007;274:1655–65.PubMedCrossRef Yanagita T, Kubota S, Kawaki H, Kawata K, Kondo S, Takano-Yamamoto T, et al. Expression and physiological role of CCN4/Wnt-induced secreted protein 1 mRNA splicing variants in chondrocytes. FEBS J. 2007;274:1655–65.PubMedCrossRef
94.
go back to reference Yu C, Le AT, Yeger H, Perbal B, Alman BA. NOV (CCN3) regulation in the growth plate and CCN family member expression in cartilage neoplasia. J Pathol. 2003;201:609–15.PubMedCrossRef Yu C, Le AT, Yeger H, Perbal B, Alman BA. NOV (CCN3) regulation in the growth plate and CCN family member expression in cartilage neoplasia. J Pathol. 2003;201:609–15.PubMedCrossRef
95.
go back to reference Fong YC, Lin CY, Su YC, Chen WC, Tsai FJ, Tsai CH, et al. CCN6 enhances ICAM-1 expression and cell motility in human chondrosarcoma cells. J Cell Physiol. 2012;227:223–32.PubMedCrossRef Fong YC, Lin CY, Su YC, Chen WC, Tsai FJ, Tsai CH, et al. CCN6 enhances ICAM-1 expression and cell motility in human chondrosarcoma cells. J Cell Physiol. 2012;227:223–32.PubMedCrossRef
96.
go back to reference Lin CY, Tzeng HE, Li TM, Chen HT, Lee Y, Yang YC, et al. WISP-3 inhibition of miR-452 promotes VEGF-A expression in chondrosarcoma cells and induces endothelial progenitor cells angiogenesis. Oncotarget. 2017;8:39571–81.PubMedPubMedCentral Lin CY, Tzeng HE, Li TM, Chen HT, Lee Y, Yang YC, et al. WISP-3 inhibition of miR-452 promotes VEGF-A expression in chondrosarcoma cells and induces endothelial progenitor cells angiogenesis. Oncotarget. 2017;8:39571–81.PubMedPubMedCentral
97.
go back to reference Tang Q, Jiang X, Li H, Lin Z, Zhou X, Luo X, et al. Expression and prognostic value of WISP-1 in patients with endometrial endometrioid adenocarcinoma. J Obstet Gynaecol Res. 2011;37:606–12.PubMedCrossRef Tang Q, Jiang X, Li H, Lin Z, Zhou X, Luo X, et al. Expression and prognostic value of WISP-1 in patients with endometrial endometrioid adenocarcinoma. J Obstet Gynaecol Res. 2011;37:606–12.PubMedCrossRef
99.
go back to reference Zheng M, Simon R, Kononen J, Sauter G, Mihatsch MJ, Moch H. Analysis of gene expression profiles among 3 epithelial ovarian tumor subtypes using cDNA and tissue microarrays. Ai Zheng. 2004;23:771–6.PubMed Zheng M, Simon R, Kononen J, Sauter G, Mihatsch MJ, Moch H. Analysis of gene expression profiles among 3 epithelial ovarian tumor subtypes using cDNA and tissue microarrays. Ai Zheng. 2004;23:771–6.PubMed
100.
go back to reference Mason HR, Lake AC, Wubben JE, Nowak RA, Castellot JJ Jr. The growth arrest-specific gene CCN5 is deficient in human leiomyomas and inhibits the proliferation and motility of cultured human uterine smooth muscle cells. Mol Hum Reprod. 2004;10:181–7.PubMedCrossRef Mason HR, Lake AC, Wubben JE, Nowak RA, Castellot JJ Jr. The growth arrest-specific gene CCN5 is deficient in human leiomyomas and inhibits the proliferation and motility of cultured human uterine smooth muscle cells. Mol Hum Reprod. 2004;10:181–7.PubMedCrossRef
101.
go back to reference Bourdeau I, Antonini SR, Lacroix A, Kirschner LS, Matyakhina L, Lorang D, et al. Gene array analysis of macronodular adrenal hyperplasia confirms clinical heterogeneity and identifies several candidate genes as molecular mediators. Oncogene. 2004;23:1575–85.PubMedCrossRef Bourdeau I, Antonini SR, Lacroix A, Kirschner LS, Matyakhina L, Lorang D, et al. Gene array analysis of macronodular adrenal hyperplasia confirms clinical heterogeneity and identifies several candidate genes as molecular mediators. Oncogene. 2004;23:1575–85.PubMedCrossRef
102.
go back to reference Xie D, Nakachi K, Wang H, Elashoff R, Koeffler HP. Elevated levels of connective tissue growth factor, WISP-1, and CYR61 in primary breast cancers associated with more advanced features. Cancer Res. 2001;61:8917–23.PubMed Xie D, Nakachi K, Wang H, Elashoff R, Koeffler HP. Elevated levels of connective tissue growth factor, WISP-1, and CYR61 in primary breast cancers associated with more advanced features. Cancer Res. 2001;61:8917–23.PubMed
103.
go back to reference Banerjee S, Dhar G, Haque I, Kambhampati S, Mehta S, Sengupta K, et al. CCN5/WISP-2 expression in breast adenocarcinoma is associated with less frequent progression of the disease and suppresses the invasive phenotypes of tumor cells. Cancer Res. 2008;68:7606–12.PubMedCrossRef Banerjee S, Dhar G, Haque I, Kambhampati S, Mehta S, Sengupta K, et al. CCN5/WISP-2 expression in breast adenocarcinoma is associated with less frequent progression of the disease and suppresses the invasive phenotypes of tumor cells. Cancer Res. 2008;68:7606–12.PubMedCrossRef
104.
go back to reference Dhar G, Banerjee S, Dhar K, Tawfik O, Mayo MS, Vanveldhuizen PJ, et al. Gain of oncogenic function of p53 mutants induces invasive phenotypes in human breast cancer cells by silencing CCN5/WISP-2. Cancer Res. 2008;68:4580–7.PubMedCrossRef Dhar G, Banerjee S, Dhar K, Tawfik O, Mayo MS, Vanveldhuizen PJ, et al. Gain of oncogenic function of p53 mutants induces invasive phenotypes in human breast cancer cells by silencing CCN5/WISP-2. Cancer Res. 2008;68:4580–7.PubMedCrossRef
Metadata
Title
The emerging role of WISP proteins in tumorigenesis and cancer therapy
Authors
Yi Liu
Yizuo Song
Miaomiao Ye
Xiaoli Hu
Z. Peter Wang
Xueqiong Zhu
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Journal of Translational Medicine / Issue 1/2019
Electronic ISSN: 1479-5876
DOI
https://doi.org/10.1186/s12967-019-1769-7

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