CRISP3 expression drives prostate cancer invasion and progression

in Endocrine-Related Cancer

Correspondence should be addressed to L Furic or M O’Bryan: luc.furic@petermac.org or moira.obryan@monash.edu

*(M Volpert and L Furic contributed equally to this work)

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Identifying the factors stimulating prostate cancer cells migration and invasion has the potential to bring new therapeutic targets to the clinic. Cysteine-rich secretory protein 3 (CRISP3) is one of the most highly upregulated proteins during the transition of a healthy human prostatic epithelium to prostate cancer. Here we show using a genetically engineered mouse model of prostate cancer that CRISP3 production greatly facilitates disease progression from carcinoma in situ to invasive prostate cancer in vivo. This interpretation was confirmed using both human and mouse prostate cancer cell lines, which showed that exposure to CRISP3 enhanced cell motility and invasion. Further, using mass spectrometry, we show that CRISP3 induces changes in abundance of a subset of cell-cell adhesion proteins, including LASP1 and TJP1 both in vivo and in vitro. Collectively, these data identify CRISP3 as being pro-tumorigenic in the prostate and validate it as a potential target for therapeutic intervention.

Supplementary Materials

    • Supplementary Figure 1. shRNA knockdown of CRISP3 in LNCaP cells CRISP3 knockdown of 79% and 81% was observed in stable LNCaP cell lines transfected with shRNA clone IDs V3LHS_349261 (shRNA1) and V3LHS_349262 (shRNA2) respectively, compared with a missense shRNA control. N=2, error bars represent ±S.E.M.
    • Supplementary Figure 2. The generation and confirmation of Crisp3-/- knockout mice (A) LoxP sites were targeted either side of exons 3-4, causing Cre-recombinase-mediated recombination to give rise to a truncated Crisp3 sequence. Recombination introduced a remature stop codon in exon 5. (B) Multiplex PCR genotyping of the Crisp3 knockout line whereby the wild type (WT) and knockout (KO) alleles gave rise to 492 bp and 343 bp products, respectively. ‘Het’ indicates heterozygous. (C) RT-PCR gave products of predicted sizes of 544 and 339 bp when amplified from Crisp3+/+ and Crisp3-/- salivary gland, respectively. (D) CRISP3 immunohistochemistry in the salivary gland of Crisp3+/+ (left panel) and Crisp3-/- (right panel) 7 month old mice. Scale bars=100 μm.
    • Supplementary Figure 3. Crisp3 knockout had no effect on whole body weight. Crisp3-/- mice (black bars) had normal whole-body weight from 2-7 months of age compared with wild type control animals (white bars). N=5-8 animals.
    • Supplementary Figure 4. Hi-MYC+ Crisp3 mouse generations. Mice of the appropriate genotypes were generated using two consecutive rounds of breeding Crisp3-/- C57BL/6 mice were bred with the Hi-MYC FVB strain to produce either Hi-MYC- or Hi- MYC+ Crisp3+/- mice. These were interbred to produce offspring for analysis.
    • Supplementary Figure 5. Crisp3 knockout delays the formation of in situ lesions and suppresses progression to invasive adenocarcinoma at 7 months in the Hi-MYC model Six representative Hi-MYC+Crisp3+/+ and Hi-MYC+Crisp3-/- whole lateral prostate lobes at 7 months, stained with haematoxylin and eosin.
    • Supplementary Figure 6: Characterisation of Hi_MYC+Crisp3+/+ and Hi-MYC+Crisp3-/- cells. Isolated and cultured Hi_MYC+Crisp3+/+ (WT1) and Hi-MYC+Crisp3-/- (KO1) cells expressed high levels of the androgen receptor (AR) consistent with characterised HM-5 cells isolated from FVB-Hi-MYC mice, human PC3 prostate cancer cells and normal prostate fibroblast cells (NPF). These cells also expressed epithelial marker E-cadherin to a similar level as HM-5 and PC3 cells and lacked, or lowly expressed, stromal fibroblast marker alpha-smooth muscle actin (α-SMA), whereas mouse embryonic fibroblast line (NIH/3T3) and human prostate fibroblast cells (NPF) retained high expression of these markers. These features are consistent with the prostate epithelial cell phenotype.
    • Supplementary Figure 7: CRISP3 promotes invasive adenocarcinoma formation confirmed by migration assay using live-cell microscope. (A-B) CRISP3 production (Hi_MYC+Crisp3+/+, T2) was associated with an increased migratory ability, as measured using a scratch assay, compared to Crisp3 null cells (Hi-MYC+Crisp3-/-, KO2). N=3 assays per cell line, n = 3 technical replicates, data are mean ± S.D., statistical analysis: unpaired Student’s t-test, ** P < 0.01, *** P < 0.001. Time points were 2, 4, 6, 8, 10, 12, 16, 20 and 24 h (h). (C) Representative images of MYC+Crisp3+/+ and Hi-MYC+Crisp3-/- cells migration at different time points (y-axis). Scale bar =100 μm.
    • Supplementary Figure 8. Confirmation of the absence of CRISP3 production in Hi- MYC+Crisp3-/- prostate cancer cells. Representative images of paired (A and B) Hi-MYC+Crisp3+/+ and Hi-MYC+Crisp3-/- prostate cancer cells immunofluorescence staining using a CRISP3 antibody (green). Nuclei were stained with DAPI (blue). CRISP3 was detected in Hi-MYC+Crisp3+/+ cells, but not in Hi-MYC+Crisp3-/- cells. These images also confirm the specificity of the CRISP3 antibody. Representative images from n = 3 replicates of each Hi-MYC cell line, scale bars = 20 μm.
    • Supplementary figure 9. LASP1 and TJP1 expression in CRISP3 non-exposed versus exposed cells as measured by western blotting. (A) PC3 cells. PC3 cells treated +/- 50 μg/ml purified recombinant CRISP3 for 4 h. The loading control was α-tubulin. n = 3 replicates of PC3 cells, data are mean ± S.D.; statistical analysis: unpaired Student’s t-test, * P < 0.05. Untreated PC3 culture results were normalized to 1.0 and treated PC3 cells compared directly within individual experiments. (B) In Hi-MYC+Crisp3+/+ prostate cancer cells compared to Hi-MYC+Crisp3-/- cells. The loading control was α-tubulin. n = 3 replicates of each Hi-MYC cell line, data are mean ± S.D., statistical analysis: one-way ANOVA with Tukey’s multiple comparisons. Crisp3 expressing cell results were normalized to 1.0 and KO cells were normalized to the average quantification value of the corresponding WT cells. Different letters

 

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