LIV-1 Promotes Prostate Cancer Epithelial-to-Mesenchymal Transition and Metastasis through HB-EGF Shedding and EGFR-Mediated ERK Signaling
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{"title"=>"LIV-1 promotes prostate cancer epithelial-to-mesenchymal transition and metastasis through HB-EGF shedding and EGFR-mediated ERK signaling", "type"=>"journal", "authors"=>[{"first_name"=>"Hui Wen", "last_name"=>"Lue", "scopus_author_id"=>"24335919900"}, {"first_name"=>"Xiaojian", "last_name"=>"Yang", "scopus_author_id"=>"23053566700"}, {"first_name"=>"Ruoxiang", "last_name"=>"Wang", "scopus_author_id"=>"8648266100"}, {"first_name"=>"Weiping", "last_name"=>"Qian", "scopus_author_id"=>"35072040200"}, {"first_name"=>"Roy Z.H.", "last_name"=>"Xu", "scopus_author_id"=>"54418091100"}, {"first_name"=>"Robert", "last_name"=>"Lyles", "scopus_author_id"=>"7007140219"}, {"first_name"=>"Adeboye O.", "last_name"=>"Osunkoya", "scopus_author_id"=>"20434188200"}, {"first_name"=>"Binhua P.", "last_name"=>"Zhou", "scopus_author_id"=>"35101110400"}, {"first_name"=>"Robert L.", "last_name"=>"Vessella", "scopus_author_id"=>"7007065462"}, {"first_name"=>"Majd", "last_name"=>"Zayzafoon", "scopus_author_id"=>"6507783654"}, {"first_name"=>"Zhi Ren", "last_name"=>"Liu", "scopus_author_id"=>"21233831100"}, {"first_name"=>"Haiyen E.", "last_name"=>"Zhau", "scopus_author_id"=>"7004099055"}, {"first_name"=>"Leland W.K.", "last_name"=>"Chung", "scopus_author_id"=>"7102299103"}], "year"=>2011, "source"=>"PLoS ONE", "identifiers"=>{"pui"=>"362925712", "scopus"=>"2-s2.0-81155137295", "isbn"=>"1932-6203 (Electronic)\\n1932-6203 (Linking)", "pmid"=>"22110740", "sgr"=>"81155137295", "issn"=>"19326203", "doi"=>"10.1371/journal.pone.0027720"}, "id"=>"236fded4-37ee-31c1-bb0e-3e6ab90ee9d7", "abstract"=>"LIV-1, a zinc transporter, is an effector molecule downstream from soluble growth factors. This protein has been shown to promote epithelial-to-mesenchymal transition (EMT) in human pancreatic, breast, and prostate cancer cells. Despite the implication of LIV-1 in cancer growth and metastasis, there has been no study to determine the role of LIV-1 in prostate cancer progression. Moreover, there was no clear delineation of the molecular mechanism underlying LIV-1 function in cancer cells. In the present communication, we found increased LIV-1 expression in benign, PIN, primary and bone metastatic human prostate cancer. We characterized the mechanism by which LIV-1 drives human prostate cancer EMT in an androgen-refractory prostate cancer cells (ARCaP) prostate cancer bone metastasis model. LIV-1, when overexpressed in ARCaP(E) (derivative cells of ARCaP with epithelial phenotype) cells, promoted EMT irreversibly. LIV-1 overexpressed ARCaP(E) cells had elevated levels of HB-EGF and matrix metalloproteinase (MMP) 2 and MMP 9 proteolytic enzyme activities, without affecting intracellular zinc concentration. The activation of MMPs resulted in the shedding of heparin binding-epidermal growth factor (HB-EGF) from ARCaP(E) cells that elicited constitutive epidermal growth factor receptor (EGFR) phosphorylation and its downstream extracellular signal regulated kinase (ERK) signaling. These results suggest that LIV-1 is involved in prostate cancer progression as an intracellular target of growth factor receptor signaling which promoted EMT and cancer metastasis. LIV-1 could be an attractive therapeutic target for the eradication of pre-existing human prostate cancer and bone and soft tissue metastases.", "link"=>"http://www.mendeley.com/research/liv1-promotes-prostate-cancer-epithelialtomesenchymal-transition-metastasis-through-hbegf-shedding-e", "reader_count"=>28, "reader_count_by_academic_status"=>{"Researcher"=>8, "Student > Ph. D. Student"=>9, "Student > Postgraduate"=>3, "Other"=>2, "Student > Master"=>3, "Lecturer"=>1, "Professor"=>1, "Professor > Associate Professor"=>1}, "reader_count_by_user_role"=>{"Researcher"=>8, "Student > Ph. D. Student"=>9, "Student > Postgraduate"=>3, "Other"=>2, "Student > Master"=>3, "Lecturer"=>1, "Professor"=>1, "Professor > Associate Professor"=>1}, "reader_count_by_subject_area"=>{"Engineering"=>1, "Biochemistry, Genetics and Molecular Biology"=>2, "Agricultural and Biological Sciences"=>17, "Medicine and Dentistry"=>7, "Chemistry"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>7}, "Chemistry"=>{"Chemistry"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>17}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>2}}, "reader_count_by_country"=>{"United States"=>1, "Italy"=>1, "Australia"=>1, "France"=>1, "Thailand"=>1, "Spain"=>1}, "group_count"=>2}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/712592"], "description"=>"<p>Upon intracardiac inoculation, ARCaP<sub>E</sub> clones overexpressing LIV-1 caused metastatic tumor formation in athymic mice (<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0027720#pone-0027720-t001\" target=\"_blank\">Table 1</a>). Representative results depict the metastatic tumors. <b>A,</b> a tibial tumor (arrow) was identified by X-ray (Pathomorphology). The tumor was subjected to H&E staining for histopathologic confirmation. Compared to the tibia of the opposite leg (Normal), the tibial tumor (Tumor) showed histopathology typical of a metastatic bone lesion. <b>B,</b> an adrenal gland metastasis (held by forceps) destroyed the gland (Pathomorphology). Compared to the unaffected gland (Normal), tumor cells were found in every part of the affected gland (Tumor) (250 ×).</p>", "links"=>[], "tags"=>["overexpression", "promoted", "cancer"], "article_id"=>382938, "categories"=>["Cancer", "Molecular Biology", "Medicine", "Cell Biology"], "users"=>["Hui-Wen Lue", "Xiaojian Yang", "Ruoxiang Wang", "Weiping Qian", "Roy Z. H. Xu", "Robert Lyles", "Adeboye O. Osunkoya", "Binhua P. Zhou", "Robert L. Vessella", "Majd Zayzafoon", "Zhi-Ren Liu", "Haiyen E. Zhau", "Leland W. K. Chung"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027720.g005", "stats"=>{"downloads"=>4, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_LIV_1_overexpression_promoted_cancer_bone_and_soft_tissue_metastasis_/382938", "title"=>"LIV-1 overexpression promoted cancer bone and soft tissue metastasis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 11:40:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/712490"], "description"=>"<p>Upon subcutaneous inoculation, the two ARCaP<sub>E</sub> clones overexpressing LIV-1 (LIV8 and LIV14) were compared with vector control clones (con1 and con2) for tumor formation in athymic mice. Growth of the tumors at day 23, 32, 43, and 50 is shown. Each result represents the mean ± standard deviation of six tumors. An asterisk indicates statistical significance compared to the con1 control clone (<i>P</i><0.05).</p>", "links"=>[], "tags"=>["overexpression", "promoted", "subcutaneous"], "article_id"=>382837, "categories"=>["Cancer", "Molecular Biology", "Medicine", "Cell Biology"], "users"=>["Hui-Wen Lue", "Xiaojian Yang", "Ruoxiang Wang", "Weiping Qian", "Roy Z. H. Xu", "Robert Lyles", "Adeboye O. Osunkoya", "Binhua P. Zhou", "Robert L. Vessella", "Majd Zayzafoon", "Zhi-Ren Liu", "Haiyen E. Zhau", "Leland W. K. Chung"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027720.g004", "stats"=>{"downloads"=>1, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_LIV_1_overexpression_promoted_subcutaneous_tumor_growth_/382837", "title"=>"LIV-1 overexpression promoted subcutaneous tumor growth.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 11:40:08"}
  • {"files"=>["https://ndownloader.figshare.com/files/712256"], "description"=>"<p>The produced antibodies to LIV-1 were subjected to validation for specificity. <b>A,</b> HEK293 cells transiently transfected with the LIV-1 expression construct were subjected to Western blotting analysis with the antibodies to LIV-1 (upper panel). Antibody specificity was determined by pre-absorbing the antibody with the immunizing peptide (middle panel). <b>B,</b> ARCaP<sub>E</sub> cells were transiently transfected with the LIV-1 expression construct to overexpress LIV-1 and ARCaP<sub>M</sub> cells with the specific siRNA to suppress LIV-1 expression. In the upper 2 panels, Western blotting was performed 48 hours later with the antibodies to LIV-1. In the lower 2 panels, these cells were examined by RT-PCR to confirm the LIV-1 expression. β-actin was used as control in Western blotting and GAPDH was used as control for RT-PCR analysis. <b>C,</b> IHC was conducted to further confirm LIV-1 Ab specificity in ARCaP<sub>E</sub> cells transiently transfected with the LIV-1 expression construct and ARCaP<sub>M</sub> cells transiently transfected with the specific siRNA (200 ×).</p>", "links"=>[], "tags"=>["antibodies"], "article_id"=>382609, "categories"=>["Cancer", "Molecular Biology", "Medicine", "Cell Biology"], "users"=>["Hui-Wen Lue", "Xiaojian Yang", "Ruoxiang Wang", "Weiping Qian", "Roy Z. H. Xu", "Robert Lyles", "Adeboye O. Osunkoya", "Binhua P. Zhou", "Robert L. Vessella", "Majd Zayzafoon", "Zhi-Ren Liu", "Haiyen E. Zhau", "Leland W. K. Chung"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027720.g002", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Validation_of_the_antibodies_to_LIV_1_/382609", "title"=>"Validation of the antibodies to LIV-1.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 11:38:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/713185"], "description"=>"<p>*LIV-1-overexpression clones (LIV#8 and LIV#14) and vector-transfected clones (con1 and con2) were intracardially inoculated to athymic mice. Incidence and sites of metastasis were followed up to 4 months by necropsy and histopathologic confirmation.</p>", "links"=>[], "tags"=>["prostate", "cancer"], "article_id"=>383536, "categories"=>["Cancer", "Molecular Biology", "Medicine", "Cell Biology"], "users"=>["Hui-Wen Lue", "Xiaojian Yang", "Ruoxiang Wang", "Weiping Qian", "Roy Z. H. Xu", "Robert Lyles", "Adeboye O. Osunkoya", "Binhua P. Zhou", "Robert L. Vessella", "Majd Zayzafoon", "Zhi-Ren Liu", "Haiyen E. Zhau", "Leland W. K. Chung"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027720.t001", "stats"=>{"downloads"=>2, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_LIV_1_promotes_prostate_cancer_cell_metastasis_/383536", "title"=>"LIV-1 promotes prostate cancer cell metastasis.<sup>*</sup>", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-20 11:43:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/712869"], "description"=>"<p>LIV-1 overexpressing cells (LIV#8 and LIV#14) showed increased phosphorylated EGFR (p-EGFR) and ERK (p-ERK). <b>B,</b> EGFR inhibitor (AG1478) treatment reduced phosphorylated EGFR and ERK in LIV#8 clone. <b>C,</b> inhibition of EGFR suppressed migratory ability and invasive ability of LIV-1 overexpressing clones in transwell assays 24 hours after treatment. <b>D,</b> inhibition of ERK signaling resulted in similar suppression of cellular motility as EGFR inhibition. <b>*</b> indicates statistical significance compared to the control of the same group (<i>P</i><0.05).</p>", "links"=>[], "tags"=>["overexpressing", "cells", "displayed", "constitutively", "activated", "egfr"], "article_id"=>383211, "categories"=>["Cancer", "Molecular Biology", "Medicine", "Cell Biology"], "users"=>["Hui-Wen Lue", "Xiaojian Yang", "Ruoxiang Wang", "Weiping Qian", "Roy Z. H. Xu", "Robert Lyles", "Adeboye O. Osunkoya", "Binhua P. Zhou", "Robert L. Vessella", "Majd Zayzafoon", "Zhi-Ren Liu", "Haiyen E. Zhau", "Leland W. K. Chung"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027720.g007", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_LIV_1_overexpressing_cells_displayed_constitutively_activated_EGFR_signaling_A_/383211", "title"=>"LIV-1 overexpressing cells displayed constitutively activated EGFR signaling. A,", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 11:42:08"}
  • {"files"=>["https://ndownloader.figshare.com/files/712397"], "description"=>"<p>ARCaP<sub>E</sub> clones overexpressing LIV-1 displayed EMT-like changes in gene expression, cellular morphology and behavior. <b>A,</b> all four LIV-1 overexpressing ARCaP<sub>E</sub> clones showed EMT-like expressional changes as detected by Western blotting, while the two vector control clones (1 and 2) retained an epithelial cell-like expression profile. <b>B,</b> cellular morphology of the LIV-1 overexpressing cells showed marked changes from the control clones (200 ×). <b>C,</b> LIV-1 overexpressing cells (LIV#8 and LIV#14 were compared with vector control clones 1 and 2 and parental ARCaP<sub>E</sub> and ARCaP<sub>M</sub> cells for altered migratory capability in transwell assays. Each result is the mean ± standard deviation of a triplicate assay. <b>D,</b> the LIV-1 overexpressing #8 and #14 clones were compared with vector control clones 1 and 2 and parental ARCaP<sub>E</sub> and ARCaP<sub>M</sub> cells for altered invasiveness. <b>*</b> indicates statistical significance compared to the con1 control clone (<i>P</i><0.05).</p>", "links"=>[], "tags"=>["overexpression", "induced"], "article_id"=>382748, "categories"=>["Cancer", "Molecular Biology", "Medicine", "Cell Biology"], "users"=>["Hui-Wen Lue", "Xiaojian Yang", "Ruoxiang Wang", "Weiping Qian", "Roy Z. H. Xu", "Robert Lyles", "Adeboye O. Osunkoya", "Binhua P. Zhou", "Robert L. Vessella", "Majd Zayzafoon", "Zhi-Ren Liu", "Haiyen E. Zhau", "Leland W. K. Chung"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027720.g003", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_LIV_1_overexpression_induced_EMT_/382748", "title"=>"LIV-1 overexpression induced EMT.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 11:39:35"}
  • {"files"=>["https://ndownloader.figshare.com/files/712751"], "description"=>"<p><b>A,</b> RT-PCR and Western blotting were used to determine LIV-1 expression in different prostate cancer cell lines. β-actin was used as control in Western blotting and GAPDH was used as control for RT-PCR analysis. <b>B,</b> representative IHC images showed increased LIV-1 expression in human prostate specimens from benign to bone metastasis (125 ×). <b>C,</b> Interval plot of LIV-1 expression is shown versus prostate cancer progression from normal/benign, PIN, primary cancer to bone metastasis. The data are shown with 95% confidence interval (n  =  number of cases analyzed). The median expression for LIV-1 in bone was significantly greater than in normal/benign, PIN, and primary cancer (<i>P</i><0.001) and in primary cancer only (P = 0.002) as analyzed by Mann-Whitney test.</p>", "links"=>[], "tags"=>["prostate", "cancer"], "article_id"=>383097, "categories"=>["Cancer", "Molecular Biology", "Medicine", "Cell Biology"], "users"=>["Hui-Wen Lue", "Xiaojian Yang", "Ruoxiang Wang", "Weiping Qian", "Roy Z. H. Xu", "Robert Lyles", "Adeboye O. Osunkoya", "Binhua P. Zhou", "Robert L. Vessella", "Majd Zayzafoon", "Zhi-Ren Liu", "Haiyen E. Zhau", "Leland W. K. Chung"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027720.g006", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_LIV_1_expression_is_associated_with_human_prostate_cancer_progression_/383097", "title"=>"LIV-1 expression is associated with human prostate cancer progression.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 11:41:34"}
  • {"files"=>["https://ndownloader.figshare.com/files/712119"], "description"=>"<p>The role of LIV-1 was assessed by its changed expression during EMT. <b>A,</b> ARCaP<sub>E</sub> cells were treated for 48 hours with growth factors to induce EMT. RT-PCR and Western blotting were used to show increased LIV-1 expression (left panel), and the dose responsiveness of the expression (right panel). <b>B,</b> Western blotting was used to confirm EMT-like expressional changes in the treated ARCaP<sub>E</sub> cells. <b>C,</b> mesenchymal cell-like ARCaP<sub>M</sub> cells were subjected to siRNA knockdown for LIV-1 expression for 48 hours. RT-PCR and Western blotting were used to detect expressional changes reflecting reversal of EMT in the treated cells. <b>D,</b> Scratch wound healing and transwell invasion assays were used to determine migratory and invasive behavior in siRNA treated ARCaP<sub>M</sub> cells. * indicates statistical significance compared to the con1 control clone (P<0.05). <b>E,</b> ARCaP<sub>E</sub> cells were transfected with LIV-1 expression construct. RT-PCR and western blotting were performed 48 hours after transfection to detect expressional changes reflecting EMT-like events. GAPDH served as an internal control for RT-PCR reactions, and β-actin was used as a loading control in Western blotting.</p>", "links"=>[], "tags"=>["mediator"], "article_id"=>382468, "categories"=>["Cancer", "Molecular Biology", "Medicine", "Cell Biology"], "users"=>["Hui-Wen Lue", "Xiaojian Yang", "Ruoxiang Wang", "Weiping Qian", "Roy Z. H. Xu", "Robert Lyles", "Adeboye O. Osunkoya", "Binhua P. Zhou", "Robert L. Vessella", "Majd Zayzafoon", "Zhi-Ren Liu", "Haiyen E. Zhau", "Leland W. K. Chung"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027720.g001", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_LIV_1_is_a_mediator_in_ARCaP_E_cell_EMT_/382468", "title"=>"LIV-1 is a mediator in ARCaP<sub>E</sub> cell EMT.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 11:37:56"}
  • {"files"=>["https://ndownloader.figshare.com/files/713001"], "description"=>"<p><b>A,</b> LIV-1 overexpressing cells (LIV#8) and control cells (con1) were treated with EGF and AG1478 for 2 hours. Western blotting showed that the EGF-elicited EGFR and ERK phosphorylation was blocked by the AG1478 inhibitor. <b>B,</b> RT-PCR showed increased HB-EGF, MMP2 and MMP9 expression in LIV-1 overexpressing cells. <b>C,</b> LIV-1 overexpressing cells (LIV#8 and LIV#14) were cultured in serum-free medium for 24 hours and the culture media were used to determine the MMP2 and MMP9 enzymatic activity by zymogram assay. <b>D,</b> the effect of MMP2/9 enzymatic activity on HB-EGF shedding was evaluated by ELISA. LIV-1 overexpressing clones (LIV#8 and LIV#14) secreted more HB-EGF than control clones (con1 and con2), and the secretion was reduced by MMP2/9 inhibition. <b>∗</b> indicates statistical significance compared to the control of the group (<i>P</i><0.05). <b>E,</b> Western blotting showed that inhibition of MMP2/9 activity suppressed EGFR and the downstream ERK phosphorylation. <b>F,</b> LIV-1 overexpressing cells were treated with MMP 2/9 inhibitor III for 24 hours in Transwell motility assays. Both migration and invasion of the treated cells were decreased. <b>*</b> indicates statistical significance compared to the control group (<i>P</i><0.05). <b>G,</b> diagram depicts the proposed role of LIV-1 in prostate cancer cell EMT and metastasis.</p>", "links"=>[], "tags"=>["up-regulated", "liv-1", "overexpressing"], "article_id"=>383346, "categories"=>["Cancer", "Molecular Biology", "Medicine", "Cell Biology"], "users"=>["Hui-Wen Lue", "Xiaojian Yang", "Ruoxiang Wang", "Weiping Qian", "Roy Z. H. Xu", "Robert Lyles", "Adeboye O. Osunkoya", "Binhua P. Zhou", "Robert L. Vessella", "Majd Zayzafoon", "Zhi-Ren Liu", "Haiyen E. Zhau", "Leland W. K. Chung"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027720.g008", "stats"=>{"downloads"=>1, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_HB_EGF_level_and_MMP2_9_activity_were_up_regulated_in_LIV_1_overexpressing_cells_/383346", "title"=>"HB-EGF level and MMP2/9 activity were up-regulated in LIV-1 overexpressing cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 11:42:50"}

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