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. 2020 Jan 16;10(5):2309–2326. doi: 10.7150/thno.39486

Table 2.

Summary of EV protein biomarkers identified in PCa for clinical diagnosis

Putative PCa marker Human sample EV source Markers for EV identification EV isolation Stage of the disease Main result Ref.
CK18 PCa patients (n=6), healthy controls (n=5) Plasma, cell line (DU145) CD81, TSG101 UC; Precipitation N/A CK18 were significantly enriched in EVs and in line with CK18 IHC in human PCa tissues 95
PSA PCa patients (n=15), BHP patients (n=15), healthy controls (n=15) Plasma, cell line (LNCaP) CD81, TSG101 UC Prostate adenocarcinoma,
total PSA was > 2.5 ng/ml
LNCaP EVs express significant levels of PSA
PCa had four-fold higher PSA-specific exosomes than BPH and healthy controls
Acidic condition stimulated the release of PSA-specific exosome
24
PTEN PCa patients (n=30), healthy controls (n=8) Plasma, cell lines (DU145, PC-3, U87, HAOEC, HAOSMC, HPEC) Flotilin-1 UC Advanced (T3/T4) tumour stage PTEN was detected in PCa cell/plasma exosomes instead of normal cell/plasma exosomes 96
PSMA PCa patients (n=82), BPH patients (n=28) Plasma CD63 Precipitation Low- (n = 17); intermediate- (n = 36);
high-risk (n = 29) PCa according to the National Comprehensive Cancer Network risk group
PSMA EVs concentration was higher in PCa than BPH
Patients with lower PSMA EVs concentration had a larger prostate volume, lower GS and lower risk of biochemical failure
97
Survivin PCa patients (n=39), BPH patients (n=20), healthy controls (n=16) Plasma; serum Lamp1 UC; Precipitation Plasma: ten low-grade PCa cases (GS 6);
ten high-grade PCa cases (GS 9);
Nineteen serum samples: N/A
Survivin existed in plasma exosomes of normal, BPH and PCa
Survivin level in PCa exosome was significantly higher than BPH and Control
Survivin exosome level in relapsed chemotherapy patients was higher than controls
98
GGT PCa patients (n=31), BPH patients (n=8) Serum, cell lines (LNCaP, C4, C4-2, C4-2B) CD9, PDCD6IP UC, Size-Exclusion Chromatography, Immunoaffinity intonations PCa patients: PSA: 4.20-28.23 ng/mL
BPH patients: 4.42-25.40 ng/mL
GGT1 was elevated in exosomes isolated from C4-2 and C4-2B cells
The level of GGT-specific exosomes was significantly higher in PCa than BPH
58
P-gp CRPC patients (6 therapy-naïve and 4 clinically docetaxel-resistant PCa patients) Serum, cell lines (PC-3, PC3-R) CD9 UC 6 therapy-naïve: PSA: 1.481-7.875 ng/mL, GS 6-8;
4 clinically docetaxel resistant PCa patients:
PSA: 26.177-25313.0 ng/mL, GS 8-10
P-gp was higher in PC-3R exosomes than PC-3
P-gp exosome level was higher in clinically docetaxel-resistant patients than in therapy-naïve patients
99
δ-Catenin, caveolin-1, CD59 PCa patients (n=16)
PCa inactive patients (n=15)
Urine, Cell lines (PC-3, CWR22Rv-1) UC PSA: 0.3-667 ng/mL, GS 6-8 δ-Catenin, caveolin-1, CD59 were detected in cell-free urine EVs
δ-Catenin had a significant increase in PCa compared to PCa inactive patients
100
FABP5 PCa patients (n=30), negative control group* (n=17) Urine, cell lines (PC3, DU145) CD9, CD63, CD81 UC GS6, PSA: 4.1-126 (n=6);
GS8-9, PSA: 6.8-311 (n=6);
low-risk PCa, GS6, PSA: 2.9-10.6 (n=5);
high-risk PCa, GS7-9, PSA: 4.3-3143 (n=13)
FABP5 was overexpressed in PCa EVs compared to negative control group
FABP5 in urinary EVs was significantly associated with GS
101
TMEM256- LAMTOR1, ADIRF, VATL, Rab, PSA, FOLH1/ PMSA, TGM4, TMPRSS PCa patients (n=17), healthy controls (n=15) Urine CD9, CD81, TSG101 UC GS6-9, PSA: 4.5-23 (n=16);
1 patient N/A due to the low exosomal protein yield and excluded from the proteomic analysis
Combined TMEM256- LAMTOR1 augmented the sensitivity to 100% with AUC= 0.94
ADIRF, VATL and 18 different Rab proteins were enriched in PCa urinary exosomes
PSA, FOLH1/PMSA, TGM4, TMPRSS were enriched in the urinary exosomes as well but with lower degree of specificity and /or sensitivity compared to TMEM256- LAMTOR1
102
PARK7- Flotillin 2 PCa patients (n=26), healthy controls (n=16) Urine N/A UC GS6-8, PSA: 4.4-22.6 (n=26) Flotillin 1, Flotillin 2, Rab3B can be used to separate PCa and healthy males
Flotillin 2 detected by Western blot has AUC-0.914
ELISA tests of Flotillin 2 and PARK7 can discriminate PCa from control with AUC of 0.65 and 0.71 respectively
Combination of Flotillin 2 and PARK7 improved the diagnostic accuracy and robustness
103
ADSV-TGM4,
CD63-GLPK5-SPHM-PSA-PAP
PCa patients (n=53), BPH patients (n=54) Urine CD81, TSG101, RaB5 UC Low-grade PCa GS ≤ 7 (3+4) (n=22);
high-grade PCa GS ≥ 7 (4+3) (n=31)
Combination of protein panel improved the ability to distinguish benign from PCa samples
ADSV-TGM4 AUC=0.65
CD63-GLPK5-SPHM-PSA-PAP AUC=0.70
104
ITGA3, ITGB1 Metastatic PCa patients (n=3), PCa patients (n=5), BPH patients (n=5) Urine, cell lines (LNCaP, PC3) PDCD6IP UC Metastatic PCa patients (n=3); PCa patients (n=5), ITGA3 showed low level in LNCaP exosomes and was hardly detectable in PC3 exosomes.
ITGB1 was not detectable in LNCaP exosomes and had some expression in PC3 exosomes
ITGA3, ITGB1 had a higher level in metastatic patient than BHP and PCa
105

Notes: *The “negative” group comprised the patients who received prostate biopsy due to elevated PSA levels and were diagnosed pathologically as negative. Abbreviations: ADIRF : adipogenesis regulatory factor; ADSV: Adseverin; AUC, Area under the curve; BPH: benign prostatic hyperplasia; PCa, prostate cancer; CD9: CD9 molecule; CD63: CD63 molecule; CD81: CD81 molecule; CK18, cytokeratin 18; CRPC, Castration-resistant prostate cancer; ELISA: enzyme-linked immunosorbent assays; EVs: Extracellular vesicles; FABP5: Fatty acid binding protein 5; GGT: Gamma-glutamyltransferase; GLPK5: Putative glycerol kinase 5; GS, Gleason score; IHC, Immunohistochemistry; ITGA3: Integrin subunit alpha 3; ITGB1: Integrin Subunit Beta 1; LAMTOR1: Late endosomal/lysosomal adaptor, MAPK and MTOR activator 1; N/A: not applicable; PARK7: Parkinsonism associated deglycase; PAP: Prostatic acid phosphatase; PDCD6IP: programmed cell death 6 interacting protein; P-gp: P-glycoprotein; PSA, Prostate specific antigen; PSMA, Prostate-specific membrane antigen; PTEN: Phosphatase and tensin homolog; RaB5: RAB5A, member RAS oncogene family; RAB3B: RAB3B, member RAS oncogene family; SPHM: N-sulphoglucosamine sulphohydrolase; TGM4: Transglutaminase-4; TMEM256: Transmembrane protein 256; TMPRSS: transmembrane protease, serine 2; TSG101: Tumour susceptibility gene 101; VATL: V-type proton ATPase 16 kDa proteolipid subunit