Background
Methods
Cell culture
Exosome isolation
Dynamic light scattering
Transmission electron microscopy
Western blot
RNA extraction & microRNA deep-sequencing
qRT-PCR and data analysis
Selection of initial set of miRNAs
Gene target predictions
Gene ontology and KEGG pathway enrichment
Statistical analysis
Results
Characterization of extracellular vesicles
microRNA profiling by small RNA deep-sequencing and qRT-PCR validation
miR | Gene ID | Fold-change | Regulation | p-value | p-value (corrected) |
---|---|---|---|---|---|
miR-9 | MI0008125_1 | 33.36 | up | 0.00E + 00 | 0.00E + 00 |
miR-9 | MI0008081_1 | 33.36 | up | 0.00E + 00 | 0.00E + 00 |
miR-9 | MI0008086_1 | 33.36 | up | 0.00E + 00 | 0.00E + 00 |
miR-122 | MI0008015_1 | 24.08 | up | 0.00E + 00 | 0.00E + 00 |
miR-183 | MI0008017_1 | 23.75 | up | 0.00E + 00 | 0.00E + 00 |
miR-182 | MI0010336_1 | 18.90 | up | 0.00E + 00 | 0.00E + 00 |
miR-106b | MI0008109_1 | 14.72 | up | 0.00E + 00 | 0.00E + 00 |
mIR-31 | MI0007994_1 | 14.32 | up | 0.00E + 00 | 0.00E + 00 |
miR-429 | MI0001644_1 | 12.47 | up | 0.00E + 00 | 0.00E + 00 |
miR-203 | MI0010363_1 | 11.79 | up | 0.00E + 00 | 0.00E + 00 |
miR-18a | MI0010324_1 | 10.34 | up | 0.00E + 00 | 0.00E + 00 |
miR-146a | MI0008094_1 | 10.13 | up | 0.00E + 00 | 0.00E + 00 |
miR-181c | MI0008034_1 | 9.99 | up | 0.00E + 00 | 0.00E + 00 |
miR-96 | MI0010356_1 | 9.65 | up | 0.00E + 00 | 0.00E + 00 |
miR-135b | MI0010334_1 | 9.25 | up | 0.00E + 00 | 0.00E + 00 |
miR-181b | MI0008153_1 | 8.75 | up | 0.00E + 00 | 0.00E + 00 |
miR-181b | MI0008127_1 | 8.75 | up | 0.00E + 00 | 0.00E + 00 |
miR-196a | MI0010360_1 | 8.69 | up | 0.00E + 00 | 0.00E + 00 |
miR-200b | MI0010361_1 | 8.11 | up | 0.00E + 00 | 0.00E + 00 |
miR-181a | MI0008152_1 | 7.78 | up | 0.00E + 00 | 0.00E + 00 |
miR-181a | MI0008126_1 | 7.62 | up | 0.00E + 00 | 0.00E + 00 |
miR-15b | MI0008083_1 | 7.26 | up | 0.00E + 00 | 0.00E + 00 |
miR-371 | MI0007996_1 | 7.11 | up | 0.00E + 00 | 0.00E + 00 |
miR-371 | MI0007996_2_1 | 7.11 | up | 0.00E + 00 | 0.00E + 00 |
miR-363 | MI0008176_1 | 7.01 | up | 0.00E + 00 | 0.00E + 00 |
miR-103 | MI0010357_1 | 6.82 | up | 0.00E + 00 | 0.00E + 00 |
miR-1841 | MI0008096_1 | 6.28 | up | 4.44E-16 | 6.49E-16 |
miR-30b | MI0008013_1 | 5.82 | up | 0.00E + 00 | 0.00E + 00 |
miR-200a | MI0010362_1 | 5.46 | up | 0.00E + 00 | 0.00E + 00 |
miR-34c | MI0008106_1 | 5.43 | up | 0.00E + 00 | 0.00E + 00 |
miR-146b | MI0008073_1 | 5.35 | up | 0.00E + 00 | 0.00E + 00 |
miR-331 | MI0010394_1 | 5.24 | up | 0.00E + 00 | 0.00E + 00 |
miR-147 | MI0010371_1 | 5.24 | up | 0.00E + 00 | 0.00E + 00 |
miR-155 | MI0008078_1 | 5.10 | up | 0.00E + 00 | 0.00E + 00 |
miR-20a | MI0008052_1 | 4.99 | up | 0.00E + 00 | 0.00E + 00 |
miR-19b | MI0008054_1 | 4.96 | up | 0.00E + 00 | 0.00E + 00 |
miR-19b | MI0008174_1 | 4.96 | up | 0.00E + 00 | 0.00E + 00 |
miR-107 | MI0008072_1 | 4.92 | up | 0.00E + 00 | 0.00E + 00 |
miR-181d | MI0008035_1 | 4.66 | up | 0.00E + 00 | 0.00E + 00 |
miR-200c | MI0008070_1 | 4.53 | up | 0.00E + 00 | 0.00E + 00 |
miR-345 | MI0008129_1 | 4.41 | up | 5.33E-15 | 7.54E-15 |
miR-130a | MI0008029_1 | 4.08 | up | 0.00E + 00 | 0.00E + 00 |
miR-29c | MI0008122_1 | 4.06 | up | 0.00E + 00 | 0.00E + 00 |
miR-29c | MI0015960_1 | 4.06 | up | 0.00E + 00 | 0.00E + 00 |
miR-15a | MI0008048_1 | 4.03 | up | 0.00E + 00 | 0.00E + 00 |
miR-19a | MI0008051_1 | 3.84 | up | 0.00E + 00 | 0.00E + 00 |
miR-16 | MI0008084_1 | 3.71 | up | 0.00E + 00 | 0.00E + 00 |
miR-93 | MI0008110_1 | 3.56 | up | 0.00E + 00 | 0.00E + 00 |
miR-1343 | MI0027953_1 | 3.53 | up | 0.00E + 00 | 0.00E + 00 |
miR-7 | MI0010330_1 | 3.51 | up | 0.00E + 00 | 0.00E + 00 |
miR-874 | MI0010429_1 | 3.51 | up | 4.76E-07 | 5.65E-07 |
miR-103 | MI0008098_1 | 3.48 | up | 0.00E + 00 | 0.00E + 00 |
miR-7 | MI0008033_1 | 3.46 | up | 0.00E + 00 | 0.00E + 00 |
miR-27a | MI0008040_1 | 3.46 | up | 0.00E + 00 | 0.00E + 00 |
miR-1839 | MI0008087_1 | 3.43 | up | 0.00E + 00 | 0.00E + 00 |
miR-196a | MI0008068_1 | 3.43 | up | 0.00E + 00 | 0.00E + 00 |
miR-20b | MI0010322_1 | 3.41 | up | 0.00E + 00 | 0.00E + 00 |
miR-660 | MI0008186_1 | 3.39 | up | 0.00E + 00 | 0.00E + 00 |
miR-215 | MI0010343_1 | 3.29 | up | 8.72E-06 | 9.96E-06 |
miR-186 | MI0008108_1 | 3.27 | up | 0.00E + 00 | 0.00E + 00 |
miR-495 | MI0008140_1 | 3.25 | up | 8.10E-12 | 1.07E-11 |
miR-339 | MI0008115_1 | 3.25 | up | 0.00E + 00 | 0.00E + 00 |
miR-421 | MI0008181_1 | 3.16 | up | 4.40E-14 | 6.13E-14 |
miR-16 | MI0008049_1 | 3.14 | up | 0.00E + 00 | 0.00E + 00 |
miR-27b | MI0008009_1 | 3.12 | up | 0.00E + 00 | 0.00E + 00 |
miR-543 | MI0008139_1 | 3.10 | up | 0.00E + 00 | 0.00E + 00 |
miR-205 | MI0010340_1 | 3.05 | up | 0.00E + 00 | 0.00E + 00 |
miR-29a | MI0008022_1 | 3.03 | up | 0.00E + 00 | 0.00E + 00 |
miR-192 | MI0008031_1 | 3.03 | up | 0.00E + 00 | 0.00E + 00 |
miR-340 | MI0010391_1 | 3.01 | up | 0.00E + 00 | 0.00E + 00 |
miR-503 | MI0008170_1 | 2.95 | up | 0.00E + 00 | 0.00E + 00 |
miR-1296 | MI0028014_1 | 2.93 | up | 2.45E-10 | 3.11E-10 |
miR-499 | MI0008059_1 | 2.91 | up | 0.00E + 00 | 0.00E + 00 |
miR-7 | MI0008085_1 | 2.89 | up | 0.00E + 00 | 0.00E + 00 |
miR-486 | MI0008027_2 | 2.87 | up | 4.44E-16 | 6.49E-16 |
miR-212 | MI0008155_1 | 2.87 | up | 6.12E-08 | 7.41E-08 |
miR-30d | MI0008012_1 | 2.81 | up | 0.00E + 00 | 0.00E + 00 |
miR-615 | MI0010419_1 | 2.73 | up | 5.27E-05 | 5.99E-05 |
miR-184 | MI0010337_1 | 2.71 | up | 4.44E-16 | 6.49E-16 |
miR-130b | MI0008064_1 | 2.66 | up | 3.81E-10 | 4.77E-10 |
miR-590 | MI0008114_1 | 2.64 | up | 0.00E + 00 | 0.00E + 00 |
miR-23a | MI0008039_1 | 2.58 | up | 0.00E + 00 | 0.00E + 00 |
miR-185 | MI0008065_1 | 2.55 | up | 0.00E + 00 | 0.00E + 00 |
miR-335 | MI0008020_1 | 2.53 | up | 0.00E + 00 | 0.00E + 00 |
miR-22 | MI0008157_1 | 2.51 | up | 0.00E + 00 | 0.00E + 00 |
miR-125b | MI0008077_1 | 2.50 | up | 0.00E + 00 | 0.00E + 00 |
miR-1307 | MI0008071_1 | 2.46 | up | 0.00E + 00 | 0.00E + 00 |
miR-1301 | MI0027930_1 | 2.43 | up | 2.22E-16 | 3.32E-16 |
miR-375 | MI0010368_1 | 2.38 | up | 4.60E-11 | 5.97E-11 |
miR-23b | MI0008008_1 | 2.31 | up | 0.00E + 00 | 0.00E + 00 |
miR-125b | MI0008103_1 | 2.30 | up | 0.00E + 00 | 0.00E + 00 |
miR-324 | MI0010395_1 | 2.27 | up | 6.64E-09 | 8.25E-09 |
miR-126 | MI0008154_1 | 2.25 | up | 1.22E-13 | 1.68E-13 |
miR-542 | MI0008171_1 | 2.25 | up | 5.30E-11 | 6.77E-11 |
miR-6529 | MI0027868_1 | 2.23 | up | 4.73E-11 | 6.08E-11 |
miR-323 | MI0008137_1 | 2.19 | up | 8.21E-07 | 9.69E-07 |
miR-365 | MI0001657_1 | 2.17 | up | 0.00E + 00 | 0.00E + 00 |
miR-365 | MI0001647_1 | 2.16 | up | 0.00E + 00 | 0.00E + 00 |
miR-92a | MI0008055_1 | 2.16 | up | 0.00E + 00 | 0.00E + 00 |
miR-374b | MI0008180_1 | 2.16 | up | 0.00E + 00 | 0.00E + 00 |
miR-1306 | MI0008066_1 | 2.13 | up | 0.00E + 00 | 0.00E + 00 |
miR-29b | MI0008121_1 | 2.11 | up | 0.00E + 00 | 0.00E + 00 |
miR-502 | MI0008187_1 | 2.10 | up | 0.00E + 00 | 0.00E + 00 |
miR-92a | MI0008175_1 | 2.10 | up | 0.00E + 00 | 0.00E + 00 |
miR-410 | MI0008149_1 | 1.97 | up | 3.84E-11 | 5.02E-11 |
miR-101 | MI0008107_1 | 1.95 | up | 0.00E + 00 | 0.00E + 00 |
miR-32 | MI0007992_1 | 1.95 | up | 4.17E-14 | 5.86E-14 |
miR-376a | MI0008141_1 | 1.93 | up | 5.33E-15 | 7.54E-15 |
miR-376a | MI0008142_1 | 1.93 | up | 5.33E-15 | 7.54E-15 |
miR-376a | MI0008143_1 | 1.93 | up | 5.33E-15 | 7.54E-15 |
miR-381 | MI0010390_1 | 1.92 | up | 0.00E + 00 | 0.00E + 00 |
miR-454 | MI0010426_1 | 1.91 | up | 3.81E-10 | 4.77E-10 |
miR-8859a | MI0027950_1 | 1.89 | up | 0.00E + 00 | 0.00E + 00 |
miR-140 | MI0008100_1 | 1.88 | up | 0.00E + 00 | 0.00E + 00 |
miR-425 | MI0008038_1 | 1.87 | up | 0.00E + 00 | 0.00E + 00 |
miR-500 | MI0008185_1 | 1.85 | up | 0.00E + 00 | 0.00E + 00 |
miR-2387 | MI0027966_1 | 1.84 | up | 1.14E-03 | 1.26E-03 |
miR-30a | MI0008000_1 | 1.83 | up | 0.00E + 00 | 0.00E + 00 |
miR-758 | MI0010424_1 | 1.82 | up | 3.43E-11 | 4.51E-11 |
miR-329b | MI0010398_1 | 1.82 | up | 6.91E-09 | 8.54E-09 |
miR-382 | MI0008145_1 | 1.80 | up | 2.95E-06 | 3.44E-06 |
miR-24 | MI0008010_1 | 1.78 | up | 0.00E + 00 | 0.00E + 00 |
miR-144 | MI0008158_1 | 1.75 | up | 9.22E-04 | 1.03E-03 |
miR-24 | MI0008041_1 | 1.75 | up | 0.00E + 00 | 0.00E + 00 |
miR-101 | MI0007995_1 | 1.73 | up | 0.00E + 00 | 0.00E + 00 |
miR-301b | MI0010349_1 | 1.68 | up | 4.74E-06 | 5.49E-06 |
miR-148b | MI0008069_1 | 1.68 | up | 0.00E + 00 | 0.00E + 00 |
miR-485 | MI0008146_1 | 1.65 | up | 2.96E-08 | 3.60E-08 |
miR-125a | MI0008005_1 | 1.65 | up | 0.00E + 00 | 0.00E + 00 |
miR-379 | MI0008134_1 | 1.62 | up | 0.00E + 00 | 0.00E + 00 |
let-7 g | MI0008036_1 | 1.62 | up | 0.00E + 00 | 0.00E + 00 |
miR-18b | MI0010323_1 | 1.62 | up | 2.79E-06 | 3.27E-06 |
miR-21 | MI0008165_1 | 1.61 | up | 0.00E + 00 | 0.00E + 00 |
miR-505 | MI0010407_1 | 1.59 | up | 3.46E-13 | 4.71E-13 |
miR-494 | MI0010404_1 | 1.57 | up | 0.00E + 00 | 0.00E + 00 |
miR-380 | MI0008136_1 | 1.55 | up | 6.32E-06 | 7.27E-06 |
miR-138a | MI0008056_1 | 1.52 | up | 9.49E-04 | 1.06E-03 |
miR-26a | MI0008058_1 | −1.51 | down | 0.00E + 00 | 0.00E + 00 |
miR-26a | MI0007990_1 | −1.51 | down | 0.00E + 00 | 0.00E + 00 |
miR-222 | MI0010346_1 | −1.56 | down | 0.00E + 00 | 0.00E + 00 |
miR-8884 | MI0027983_1 | −1.65 | down | 1.15E-08 | 1.41E-08 |
miR-490 | MI0010372_1 | −1.66 | down | 1.82E-03 | 1.99E-03 |
miR-30c | MI0008024_1 | −1.77 | down | 0.00E + 00 | 0.00E + 00 |
miR-30c | MI0008001_1 | −1.77 | down | 0.00E + 00 | 0.00E + 00 |
miR-99a | MI0008102_1 | −1.79 | down | 0.00E + 00 | 0.00E + 00 |
miR-99a | MI0008075_1 | −1.79 | down | 0.00E + 00 | 0.00E + 00 |
miR-127 | MI0008132_1 | −1.80 | down | 8.70E-05 | 9.83E-05 |
miR-30e | MI0008023_1 | −1.87 | down | 5.28E-12 | 7.04E-12 |
miR-889 | MI0027984_1 | −1.87 | down | 0.00E + 00 | 0.00E + 00 |
miR-374a | MI0008179_1 | −2.33 | down | 0.00E + 00 | 0.00E + 00 |
miR-455 | MI0007999_1 | −2.71 | down | 6.24E-14 | 8.63E-14 |
miR-145 | MI0010359_1 | −2.81 | down | 0.00E + 00 | 0.00E + 00 |
miR-574 | MI0008080_1 | −3.18 | down | 8.45E-08 | 1.01E-07 |
miR-152 | MI0008162_1 | −3.25 | down | 0.00E + 00 | 0.00E + 00 |
miR-148a | MI0008018_1 | −3.36 | down | 0.00E + 00 | 0.00E + 00 |
miR-8865 | MI0027958_1 | −3.53 | down | 1.82E-03 | 1.99E-03 |
miR-676 | MI0008188_1 | −3.71 | down | 3.65E-03 | 3.97E-03 |
miR-105a | MI0010377_1 | −4.63 | down | 6.60E-08 | 7.94E-08 |
miR-143 | MI0008092_1 | −5.78 | down | 0.00E + 00 | 0.00E + 00 |
miR-196b | MI0008016_1 | −6.92 | down | 1.64E-02 | 1.77E-02 |
miR-1 | MI0008118_1 | −7.52 | down | 0.00E + 00 | 0.00E + 00 |
miR-1 | MI0008060_1 | −7.52 | down | 0.00E + 00 | 0.00E + 00 |
miR-214 | MI0010342_1 | −9.13 | down | 4.89E-13 | 6.61E-13 |
miR-504 | MI0010406_1 | −10.06 | down | 1.11E-16 | 1.67E-16 |
miR-383 | MI0008026_1 | −10.41 | down | 1.28E-12 | 1.72E-12 |
miR-199 | MI0008151_1 | −14.03 | down | 0.00E + 00 | 0.00E + 00 |
miR-199 | MI0008042_1 | −14.03 | down | 0.00E + 00 | 0.00E + 00 |
miR-199 | MI0008124_1 | −19.70 | down | 0.00E + 00 | 0.00E + 00 |
miR-10a | MI0008161_1 | −41.07 | down | 0.00E + 00 | 0.00E + 00 |
miR-206 | MI0008002_1 | −91.77 | down | 0.00E + 00 | 0.00E + 00 |
microRNA | RNAseq | qRT-PCR | ||
---|---|---|---|---|
Fold-change | p-value | Fold-change | p-value | |
miR-18a | 10.34 | 0 | 6.82 | 0.004 |
miR-19a | 3.84 | 0 | 5.58 | 0.012 |
miR-181a | 7.70 | 0 | 8.30 | 0.004 |
In silico analysis of microRNA targets
miRNA | Total Targets Predicted | Targets with Score > 80 |
---|---|---|
cfa-miR-18a | 181 | 55 |
cfa-miR-19a | 646 | 300 |
cfa-miR-29c | 536 | 208 |
cfa-miR-31 | 359 | 98 |
cfa-miR-34c | 420 | 154 |
cfa-miR-105a | 362 | 105 |
cfa-miR-181a | 694 | 274 |
cfa-miR-206 | 358 | 133 |
cfa-miR-215 | 124 | 24 |
cfa-miR-345 | 215 | 58 |
cfa-miR-371 | 550 | 164 |
cfa-miR-495 | 729 | 263 |
cfa-miR-504 | 176 | 43 |
cfa-miR-615 | 163 | 39 |
cfa-miR-676 | 552 | 182 |
cfa-miR-1841 | 751 | 219 |
Gene ontology enrichment across all gene targets
GO biological process term | Number | Percent | p-Value | Benjamini |
---|---|---|---|---|
positive regulation of transcription from RNA polymerase II promoter | 87 | 4.8 | 5.10E-05 | 1.60E-01 |
ubiquitin-dependent protein catabolic process | 23 | 1.3 | 5.70E-04 | 6.30E-01 |
G1/S transition of mitotic cell cycle | 13 | 0.7 | 8.50E-04 | 6.20E-01 |
positive regulation of glucose import in response to insulin stimulus | 6 | 0.3 | 4.10E-03 | 8.70E-01 |
negative regulation of canonical Wnt signaling pathway | 18 | 1 | 5.30E-03 | 9.00E-01 |
regulation of establishment of cell polarity | 6 | 0.3 | 6.40E-03 | 9.10E-01 |
regulation of cell morphogenesis | 7 | 0.4 | 7.30E-03 | 8.80E-01 |
protein autophosphorylation | 22 | 1.2 | 7.70E-03 | 8.70E-01 |
vesicle fusion | 12 | 0.7 | 7.90E-03 | 8.60E-01 |
negative regulation of apoptotic process | 35 | 1.9 | 8.90E-03 | 8.70E-01 |
regulation of small GTPase mediated signal transduction | 6 | 0.3 | 9.50E-03 | 8.70E-01 |
regulation of mRNA stability | 6 | 0.3 | 9.50E-03 | 8.70E-01 |
TOR signaling | 6 | 0.3 | 9.50E-03 | 8.70E-01 |
intrinsic apoptotic signaling pathway by p53 class mediator | 7 | 0.4 | 9.90E-03 | 8.70E-01 |
negative regulation of extrinsic apoptotic signaling pathway | 9 | 0.5 | 1.10E-02 | 8.60E-01 |
histone ubiquitination | 5 | 0.3 | 1.10E-02 | 8.40E-01 |
neuronal stem cell population maintenance | 7 | 0.4 | 1.30E-02 | 8.40E-01 |
chromatin remodeling | 12 | 0.7 | 1.50E-02 | 8.60E-01 |
response to hypoxia | 15 | 0.8 | 1.60E-02 | 8.70E-01 |
mRNA splice site selection | 5 | 0.3 | 1.80E-02 | 8.70E-01 |
miRNA mediated inhibition of translation | 5 | 0.3 | 1.80E-02 | 8.70E-01 |
regulation of gene expression | 14 | 0.8 | 2.20E-02 | 8.80E-01 |
positive regulation of cell-substrate adhesion | 8 | 0.4 | 2.80E-02 | 9.00E-01 |
histone H3-K9 trimethylation | 3 | 0.2 | 3.30E-02 | 9.20E-01 |
histone H2A ubiquitination | 3 | 0.2 | 3.30E-02 | 9.20E-01 |
polarized epithelial cell differentiation | 3 | 0.2 | 3.30E-02 | 9.20E-01 |
regulation of blood coagulation | 5 | 0.3 | 3.50E-02 | 9.20E-01 |
positive regulation of cell proliferation | 34 | 1.9 | 3.80E-02 | 9.30E-01 |
positive regulation of erythrocyte differentiation | 6 | 0.3 | 4.00E-02 | 9.30E-01 |
negative regulation of cell migration | 13 | 0.7 | 4.30E-02 | 9.40E-01 |
histone H3-K4 trimethylation | 5 | 0.3 | 4.60E-02 | 9.50E-01 |
positive regulation of apoptotic process | 21 | 1.2 | 4.60E-02 | 9.40E-01 |
stem cell population maintenance | 9 | 0.5 | 5.00E-02 | 9.50E-01 |
cell migration | 19 | 1.0 | 5.32E-02 | 9.50E-01 |
Small subset of miRNAs having potential for clinical biomarker relevance
Functional annotation of miRNAs cfa-miR-18a, cfa-miR-19a, and cfa-miR-181a
Enriched Term | Gene Ontology Id | Target Genes (within all 16 miRNAs) | Targets in 3 miRNA Subset |
---|---|---|---|
G1/S transition of mitotic cell cycle | GO:0000082 | CCNE2, ACVR1B, EIF4E, CACUL1, CAMK2G, CAMK2D, USP37, RANBP1, RPS6KB1, PPP3CA, PHF8, LATS2, RBBP8 | 19a: CACUL1, RBBP81 181a: RPS6KB1 |
regulation of establishment of cell polarity | GO:2000114 | ROCK1, GATA3, KRIT1, RICTOR, ARFGEF1, KANK1 | 19a: ARFGEF1 181: KANK1 |
negative regulation of apoptotic process | GO:0043066 | FKBP8, TAF9B, NAA15, FOXO1, TP63, CITED2, SETX, PTK2, CASP3, DAB2, PRKAA1, RARB, HSPA5, AGO4, DNAJC3, KLHL20, CDK1, PDCD10, ADAMTS20, ZNF830, CBL, ASIC2, IGF1, RHBDD1, UBE2B, ASCL1, HSP90B1, GSK3B, HIPK3, VEGFA, ARF4, MAPK8, MDM4, APBB2, CAMK1D | 19a: HIPK3a, MDM4, MAPK8, ADAMTS20, KLHL20 181a: HIPK3a, HSP90B1, UBE2B, TAF9B, DNAJC3 |
establishment of cell polarity | GO:0030010 | RAB11FIP2, UST, RICTOR, WEE1, EPHB1, MARK1, KIF26B | 19a: WEE1 181a: RAB11FIP2, MARK1 |
intrinsic apoptotic signaling pathway by p53 class mediator | GO:0072332 | ZMAT1, ZMAT4, ZMAT3, PPP1R13B, ZNF385B, DDX5, ZNF346 | 19a: ZNF385B |
negative regulation of extrinsic apoptotic signaling pathway | GO:2001237 | PHIP, ZMYND11, NRP1, ITGA6, IGF1, PSME3, RPS6KB1, SGMS1, GCLM | 19a: ZMYND11 181a: GCLM, RPS6KB1 |
histone ubiquitination | GO:0016574 | SUZ12, UBE2A, HUWE1, UBE2B, PHC1 | 19a: UBE2A, SUZ12 181a: UBE2B |
neuronal stem cell population maintenance | GO:0097150 | NOTCH1, FOXO1, DLL1, FOXO3, CDH2, PROX1, MMP24 | 181a: PROX1 |
chromatin remodeling | GO:0006338 | ATRX, TOP1, RSF1, HNF1A, GATA3, MORF4L2, INO80, CHD1, TP63, ARID1B, SMARCA2, RERE | 19a: INO80a, SMARCA2, ATRX 181a: INO80a |
positive regulation of cell-substrate adhesion | GO:0010811 | PPM1F, SMOC2, CCDC80, JAK2, NID1, EDIL3, PRKCE, ABI3BP | 19a: SMOC2 181a: ABI3BP |
histone H3-K9 trimethylation | GO:0036124 | BEND3, ARID4A, ARID4B | |
histone H2A ubiquitination | GO:0033522 | UBE2A, UBR2, UBE2B | 19a: UBE2A 181a: UBE2B |
positive regulation of cell proliferation | GO:0008284 | KMT2D, CNBP, CACUL1, ESM1, IL34, CNOT7, CNOT6, TGFB2, PTK2, S1PR1, KRAS, CNOT6L, RARB, LOC488215, INSR, ACER3, UBE2A, PDCD10, KLB, SLC25A5, MECP2, ROGDI, IGF1, DLL1, TET1, SUZ12, ADM, HIPK1, HDAC1, VEGFA, HBEGF, MAB21L1, CARM1, EIF5A2 | 18a: KLB 19a: S1PR1a, CNOT7, CACUL1, NOT6, UBE2A, ROGDI, HIPK1, SUZ12 181a: S1PR1a, ESM1, CARM1, ADM |
negative regulation of cell migration | GO:0030336 | PTPRJ, RAP2A, ADARB1, RAP2C, OSBPL8, ABHD2, KANK1, THY1, SFRP1, ROBO1, RRAS, TP53INP1, SRGAP2 | 19a: RAP2C 181a: KANK1, OSBPL8, ADARB1 |
histone H3-K4 trimethylation | GO:0080182 | TET3, BEND3, ARID4A, KMT2A, CTR9 | 181a: KMT2A |
stem cell population maintenance | GO:0019827 | PHF19, EIF4E, NIPBL, MED28, MTF2, EOMES, KLF4, DDX6, CTR9 | 18a: PHF19 19a: DDX6 |
cell migration | GO:0016477 | CCDC88A, AVL9, CDH2, VAV2, EPHB3, SDC4, TGFB2, SDC1, SORBS2, GSK3B, ARF4, CDC42BPA, JAK2, LIMD1, LAMC1, CSK, KCTD13, NFATC2, USP33 | 18a: SDC4, SORBS2 19a: USP33a, NFATC2, CCDC88A, SDC1, EPHB3 181a: USP33a, AVL9, CDC42BPA |