ID	Duplex structure	Position	Score	MFE
1	miRNA 3' gugAAUG-AAGAAACGUCUACUc 5' |||: |||| ||||||| Target 5' tcaTTATGCACTTTACAGATGAg 3'	448 - 470	159.00	-16.80
2	miRNA 3' gugAAUGAAGAAACGUCUACuc 5' ||| | ||| |||||| Target 5' aagTTAATGGTTT-CAGATGtg 3'	1385 - 1405	138.00	-7.70
3	miRNA 3' gugAAUGAAGAAACGUCUACUc 5' ||: ||| | |:||:||| Target 5' ccgTTG-TTC-TCGTAGGTGAa 3'	1330 - 1349	125.00	-10.40

Mutant ID	Mutant Position	Mutant Source
COSN19727720	9	COSMIC
COSN26984408	15	COSMIC
COSN31506735	23	COSMIC
COSN26984407	24	COSMIC
COSN30131600	47	COSMIC
COSN30154776	48	COSMIC
COSN31498723	50	COSMIC
COSN509406	51	COSMIC
COSN26984406	59	COSMIC
COSN31500482	91	COSMIC
COSN26440743	100	COSMIC
COSN509404	130	COSMIC
COSN30530182	137	COSMIC
COSN25107220	141	COSMIC
COSN1760521	215	COSMIC
COSN14661410	224	COSMIC
COSN20115258	267	COSMIC
COSN20115260	267	COSMIC
COSN28158976	267	COSMIC
COSN1210917	268	COSMIC
COSN31536392	284	COSMIC
COSN30110488	291	COSMIC
COSN31482309	308	COSMIC
COSN23682603	352	COSMIC
COSN1210923	459	COSMIC
COSN20115264	639	COSMIC
COSN31584204	642	COSMIC
COSN17977501	766	COSMIC
COSN31592764	962	COSMIC
COSN31563554	992	COSMIC
COSN28734761	1155	COSMIC
COSN8604970	1155	COSMIC
COSN15660487	1193	COSMIC
COSN31563474	1218	COSMIC
COSN31570050	1220	COSMIC
COSN31517812	1305	COSMIC
COSN26562236	1452	COSMIC
COSN5183593	1473	COSMIC
COSN21549639	1508	COSMIC
COSN22852709	1508	COSMIC
COSN29685857	1531	COSMIC
COSN15663102	1532	COSMIC
COSN20115267	1824	COSMIC
COSN27205375	1824	COSMIC

Mutant ID	Mutant Position	Mutant Source
rs7359977	1	dbSNP
rs1271696761	2	dbSNP
rs757629749	3	dbSNP
rs779454394	5	dbSNP
rs200018037	8	dbSNP
rs201601323	9	dbSNP
rs1445312702	13	dbSNP
rs747594530	14	dbSNP
rs1364230532	15	dbSNP
rs769356196	17	dbSNP
rs762907550	18	dbSNP
rs774775900	18	dbSNP
rs1289849798	19	dbSNP
rs1384638568	21	dbSNP
rs371426361	23	dbSNP
rs762623417	24	dbSNP
rs372957121	25	dbSNP
rs770662121	26	dbSNP
rs774108455	27	dbSNP
rs1357146798	28	dbSNP
rs201056488	30	dbSNP
rs762233338	30	dbSNP
rs1048378804	31	dbSNP
rs543672421	32	dbSNP
rs1261111095	34	dbSNP
rs1485385656	38	dbSNP
rs926268598	39	dbSNP
rs752739121	40	dbSNP
rs760614454	45	dbSNP
rs764240371	46	dbSNP
rs372884117	47	dbSNP
rs375818896	48	dbSNP
rs768047262	48	dbSNP
rs757578396	49	dbSNP
rs779330542	50	dbSNP
rs750789749	51	dbSNP
rs758868314	53	dbSNP
rs1237544779	57	dbSNP
rs1000249863	59	dbSNP
rs1174784251	60	dbSNP
rs1225015386	65	dbSNP
rs546903569	66	dbSNP
rs780963972	68	dbSNP
rs1395468118	69	dbSNP
rs1441274021	70	dbSNP
rs891554375	76	dbSNP
rs1332256491	77	dbSNP
rs373601491	78	dbSNP
rs1024148888	85	dbSNP
rs1447768750	87	dbSNP
rs1393499690	89	dbSNP
rs1193251617	90	dbSNP
rs1469144273	92	dbSNP
rs1006262376	101	dbSNP
rs533336127	102	dbSNP
rs747854078	107	dbSNP
rs377117054	110	dbSNP
rs1001487922	111	dbSNP
rs1236799465	112	dbSNP
rs1217303196	118	dbSNP
rs1034266090	122	dbSNP
rs1234597758	124	dbSNP
rs1302163748	124	dbSNP
rs201356901	124	dbSNP
rs1381489946	127	dbSNP
rs959429048	127	dbSNP
rs1385566141	132	dbSNP
rs1030399881	134	dbSNP
rs1421524696	134	dbSNP
rs1373727477	136	dbSNP
rs1173200836	137	dbSNP
rs1379635080	140	dbSNP
rs955218583	140	dbSNP
rs987962228	141	dbSNP
rs973825264	143	dbSNP
rs1199456020	144	dbSNP
rs920582389	147	dbSNP
rs1484376261	148	dbSNP
rs141429373	150	dbSNP
rs538696961	150	dbSNP
rs1458849565	151	dbSNP
rs772368897	158	dbSNP
rs983520507	158	dbSNP
rs1297566058	159	dbSNP
rs912094597	163	dbSNP
rs7359860	165	dbSNP
rs1353605655	166	dbSNP
rs1312324150	170	dbSNP
rs1404610165	174	dbSNP
rs555189815	179	dbSNP
rs922176866	180	dbSNP
rs1374014302	181	dbSNP
rs936240688	183	dbSNP
rs1054549648	186	dbSNP
rs891424372	193	dbSNP
rs377555924	199	dbSNP
rs1474494921	200	dbSNP
rs1257492073	203	dbSNP
rs370809735	204	dbSNP
rs1201664002	210	dbSNP
rs1378776847	216	dbSNP
rs1247902097	217	dbSNP
rs1194890060	218	dbSNP
rs907074940	219	dbSNP
rs1339776108	224	dbSNP
rs1259791516	225	dbSNP
rs1001351046	232	dbSNP
rs1034155062	233	dbSNP
rs1448760773	234	dbSNP
rs1342355549	235	dbSNP
rs991893997	237	dbSNP
rs1174418895	238	dbSNP
rs1391070938	238	dbSNP
rs962968376	238	dbSNP
rs917653048	240	dbSNP
rs929511038	240	dbSNP
rs1166294488	243	dbSNP
rs1473461986	243	dbSNP
rs995395598	243	dbSNP
rs1466367408	244	dbSNP
rs1361587309	245	dbSNP
rs1048360594	246	dbSNP
rs1238483764	246	dbSNP
rs1349890014	246	dbSNP
rs373707840	246	dbSNP
rs78673746	246	dbSNP
rs1333699224	253	dbSNP
rs1439079157	257	dbSNP
rs1394224908	258	dbSNP
rs758047356	260	dbSNP
rs1407608723	261	dbSNP
rs1375897143	262	dbSNP
rs1389523048	263	dbSNP
rs942286829	264	dbSNP
rs1491338001	265	dbSNP
rs1491575293	266	dbSNP
rs113517572	267	dbSNP
rs1283546895	267	dbSNP
rs1445187245	267	dbSNP
rs1859247	267	dbSNP
rs866187056	268	dbSNP
rs200924200	269	dbSNP
rs1331652017	271	dbSNP
rs900524174	274	dbSNP
rs1232410053	284	dbSNP
rs966208299	289	dbSNP
rs974897578	290	dbSNP
rs922102368	294	dbSNP
rs1198884629	295	dbSNP
rs184125310	297	dbSNP
rs936254744	298	dbSNP
rs1030452262	306	dbSNP
rs1479446562	312	dbSNP
rs891881087	320	dbSNP
rs1171329710	321	dbSNP
rs1212073058	322	dbSNP
rs1395331297	323	dbSNP
rs1192652577	324	dbSNP
rs1010284230	327	dbSNP
rs376456234	328	dbSNP
rs912923727	329	dbSNP
rs1433139222	331	dbSNP
rs1193882347	332	dbSNP
rs1197845876	337	dbSNP
rs967878343	338	dbSNP
rs1208854671	340	dbSNP
rs945730745	343	dbSNP
rs1478156108	346	dbSNP
rs1170047788	349	dbSNP
rs567512223	352	dbSNP
rs906963810	353	dbSNP
rs1033582468	359	dbSNP
rs937050829	362	dbSNP
rs1295122162	366	dbSNP
rs959060454	367	dbSNP
rs991778741	368	dbSNP
rs1055637223	369	dbSNP
rs1281225166	372	dbSNP
rs535019876	376	dbSNP
rs1407987358	379	dbSNP
rs1218770557	380	dbSNP
rs995860784	383	dbSNP
rs1168391581	386	dbSNP
rs1025556711	388	dbSNP
rs886459852	389	dbSNP
rs1277012081	390	dbSNP
rs1478737616	390	dbSNP
rs1255343090	391	dbSNP
rs1004824693	392	dbSNP
rs539852068	393	dbSNP
rs909386490	394	dbSNP
rs1018875369	395	dbSNP
rs1488321978	396	dbSNP
rs1272695748	398	dbSNP
rs966120486	401	dbSNP
rs1291985359	404	dbSNP
rs368568511	404	dbSNP
rs571581280	405	dbSNP
rs538645708	406	dbSNP
rs1379335515	407	dbSNP
rs562082138	408	dbSNP
rs1029585141	409	dbSNP
rs1051848034	410	dbSNP
rs1010641795	411	dbSNP
rs529543097	411	dbSNP
rs756940491	412	dbSNP
rs1417441252	414	dbSNP
rs755962995	416	dbSNP
rs1479753396	418	dbSNP
rs1425807811	423	dbSNP
rs903746297	424	dbSNP
rs1459423576	427	dbSNP
rs1368833013	430	dbSNP
rs1000803021	433	dbSNP
rs537126071	442	dbSNP
rs1309532217	443	dbSNP
rs945723867	444	dbSNP
rs1325106145	445	dbSNP
rs749039895	449	dbSNP
rs1166933625	450	dbSNP
rs201839606	450	dbSNP
rs950498255	450	dbSNP
rs983502260	453	dbSNP
rs542357882	454	dbSNP
rs11550178	460	dbSNP
rs1441904442	462	dbSNP
rs1251564711	465	dbSNP
rs908894781	471	dbSNP
rs1400500825	472	dbSNP
rs1287832173	474	dbSNP
rs1359204758	475	dbSNP
rs963933640	477	dbSNP
rs1212946907	480	dbSNP
rs749732458	481	dbSNP
rs554841890	482	dbSNP
rs1241925653	487	dbSNP
rs1320732254	488	dbSNP
rs188381085	489	dbSNP
rs1471938255	492	dbSNP
rs770843132	496	dbSNP
rs1369558938	498	dbSNP
rs1287113309	501	dbSNP
rs1451704653	502	dbSNP
rs1159440347	503	dbSNP
rs1355112083	503	dbSNP
rs937080414	504	dbSNP
rs1198526888	505	dbSNP
rs1055540960	506	dbSNP
rs1270085594	507	dbSNP
rs1487660621	509	dbSNP
rs1484235917	510	dbSNP
rs898361027	513	dbSNP
rs1255804579	514	dbSNP
rs1443003906	517	dbSNP
rs1043422033	520	dbSNP
rs540560175	521	dbSNP
rs565197750	522	dbSNP
rs1001151730	532	dbSNP
rs747069012	534	dbSNP
rs1054963425	535	dbSNP
rs1401934805	538	dbSNP
rs1373787893	540	dbSNP
rs1172278760	541	dbSNP
rs1466857100	542	dbSNP
rs559788591	546	dbSNP
rs1420254193	547	dbSNP
rs1477754669	560	dbSNP
rs914713738	563	dbSNP
rs386805725	566	dbSNP
rs1195131304	567	dbSNP
rs1342939928	572	dbSNP
rs1484442860	574	dbSNP
rs1255031258	578	dbSNP
rs1024786309	588	dbSNP
rs375515934	589	dbSNP
rs1302915712	593	dbSNP
rs887042026	594	dbSNP
rs1449988564	601	dbSNP
rs181565951	602	dbSNP
rs1353703090	604	dbSNP
rs1016307610	607	dbSNP
rs1008078544	609	dbSNP
rs1018906571	610	dbSNP
rs1223715831	612	dbSNP
rs1465438215	614	dbSNP
rs1282695993	617	dbSNP
rs1173524837	618	dbSNP
rs1473927293	618	dbSNP
rs1314442291	620	dbSNP
rs768795280	621	dbSNP
rs779041980	622	dbSNP
rs901818985	629	dbSNP
rs1458097489	631	dbSNP
rs202074571	631	dbSNP
rs3214177	631	dbSNP
rs368669353	631	dbSNP
rs397741757	631	dbSNP
rs1259894674	633	dbSNP
rs1210991806	639	dbSNP
rs201632557	641	dbSNP
rs1211788449	642	dbSNP
rs1255455994	642	dbSNP
rs1460188633	646	dbSNP
rs563487538	647	dbSNP
rs1239784281	648	dbSNP
rs1283626096	648	dbSNP
rs1245632527	652	dbSNP
rs1440014474	655	dbSNP
rs1342420896	656	dbSNP
rs772308362	662	dbSNP
rs1446492167	665	dbSNP
rs954966169	669	dbSNP
rs987615467	669	dbSNP
rs1405787329	670	dbSNP
rs957795203	671	dbSNP
rs1390672078	672	dbSNP
rs1163272453	680	dbSNP
rs913415408	684	dbSNP
rs946089405	691	dbSNP
rs978870948	694	dbSNP
rs926069573	696	dbSNP
rs1416071787	698	dbSNP
rs1211618072	706	dbSNP
rs1450906991	707	dbSNP
rs1176221382	708	dbSNP
rs1290517154	709	dbSNP
rs1210506253	717	dbSNP
rs1358636728	723	dbSNP
rs1284120485	727	dbSNP
rs1239748712	728	dbSNP
rs1311853630	732	dbSNP
rs778602720	737	dbSNP
rs1020843631	739	dbSNP
rs540579006	740	dbSNP
rs1406585501	743	dbSNP
rs895046569	746	dbSNP
rs949319847	747	dbSNP
rs185763616	759	dbSNP
rs1381795848	760	dbSNP
rs981656178	765	dbSNP
rs886278975	766	dbSNP
rs947536980	766	dbSNP
rs1477614072	767	dbSNP
rs1247203856	768	dbSNP
rs928319466	768	dbSNP
rs549050647	769	dbSNP
rs1261070227	770	dbSNP
rs567549081	772	dbSNP
rs898940120	773	dbSNP
rs1442005600	776	dbSNP
rs1275935298	780	dbSNP
rs1278139790	783	dbSNP
rs995825138	783	dbSNP
rs776809738	785	dbSNP
rs190708330	786	dbSNP
rs1220293104	787	dbSNP
rs546757696	790	dbSNP
rs571919525	791	dbSNP
rs1200773275	792	dbSNP
rs987730252	794	dbSNP
rs943968315	795	dbSNP
rs550793852	798	dbSNP
rs967567859	799	dbSNP
rs760013596	800	dbSNP
rs1437461255	801	dbSNP
rs866447477	802	dbSNP
rs762076233	803	dbSNP
rs1442172223	806	dbSNP
rs926044518	809	dbSNP
rs893234433	816	dbSNP
rs1316528088	817	dbSNP
rs141382834	820	dbSNP
rs765577801	821	dbSNP
rs917260055	822	dbSNP
rs949267939	827	dbSNP
rs1359403316	828	dbSNP
rs1020458052	829	dbSNP
rs556967037	831	dbSNP
rs967531344	833	dbSNP
rs1171364743	834	dbSNP
rs770782004	834	dbSNP
rs886392439	837	dbSNP
rs1357738081	844	dbSNP
rs1479135343	845	dbSNP
rs1003165373	846	dbSNP
rs940524824	847	dbSNP
rs1035924068	849	dbSNP
rs552896405	851	dbSNP
rs958385732	853	dbSNP
rs991182196	857	dbSNP
rs1212684271	863	dbSNP
rs1172171238	864	dbSNP
rs773511856	873	dbSNP
rs919560375	875	dbSNP
rs1309901987	877	dbSNP
rs952499022	880	dbSNP
rs898892725	886	dbSNP
rs995941071	887	dbSNP
rs763252872	890	dbSNP
rs890129216	895	dbSNP
rs1008606509	896	dbSNP
rs982906420	898	dbSNP
rs764262821	899	dbSNP
rs1162692831	902	dbSNP
rs1020526628	903	dbSNP
rs1185713935	912	dbSNP
rs568748895	915	dbSNP
rs1237914005	918	dbSNP
rs943873500	923	dbSNP
rs1000349535	925	dbSNP
rs1264206782	926	dbSNP
rs536384737	928	dbSNP
rs1033612095	929	dbSNP
rs1321856518	933	dbSNP
rs1291546183	938	dbSNP
rs1237556032	941	dbSNP
rs55923173	944	dbSNP
rs1303015686	946	dbSNP
rs1375729853	951	dbSNP
rs761965323	951	dbSNP
rs991538532	952	dbSNP
rs1350581707	953	dbSNP
rs574382481	953	dbSNP
rs1040964046	955	dbSNP
rs1379932097	957	dbSNP
rs146271397	958	dbSNP
rs752049877	959	dbSNP
rs1212979549	961	dbSNP
rs1488502041	962	dbSNP
rs572944103	963	dbSNP
rs1213852532	966	dbSNP
rs1050469065	967	dbSNP
rs540442687	968	dbSNP
rs558742825	969	dbSNP
rs367825254	976	dbSNP
rs544175689	977	dbSNP
rs1387238737	980	dbSNP
rs1369669008	992	dbSNP
rs1041820557	995	dbSNP
rs903373165	996	dbSNP
rs759532151	997	dbSNP
rs931681418	1000	dbSNP
rs1050170069	1002	dbSNP
rs1299093469	1010	dbSNP
rs1003026475	1016	dbSNP
rs58612681	1017	dbSNP
rs866770445	1018	dbSNP
rs1434208398	1019	dbSNP
rs1432098506	1020	dbSNP
rs1190876500	1023	dbSNP
rs958959627	1028	dbSNP
rs903410933	1029	dbSNP
rs1013548630	1030	dbSNP
rs1026661071	1038	dbSNP
rs1033144779	1039	dbSNP
rs958865070	1040	dbSNP
rs952477504	1041	dbSNP
rs755762330	1043	dbSNP
rs1024333135	1051	dbSNP
rs777580279	1058	dbSNP
rs764315137	1061	dbSNP
rs1302569596	1063	dbSNP
rs56136663	1063	dbSNP
rs1466877654	1064	dbSNP
rs976568960	1070	dbSNP
rs1408927835	1071	dbSNP
rs1169229661	1074	dbSNP
rs575528885	1075	dbSNP
rs542584464	1076	dbSNP
rs757031860	1082	dbSNP
rs530593560	1084	dbSNP
rs947356237	1085	dbSNP
rs1050279319	1087	dbSNP
rs911624652	1096	dbSNP
rs1256054446	1099	dbSNP
rs1041851762	1101	dbSNP
rs561064033	1102	dbSNP
rs528526382	1106	dbSNP
rs903279638	1107	dbSNP
rs778878268	1108	dbSNP
rs936225872	1109	dbSNP
rs938723514	1110	dbSNP
rs1396953863	1111	dbSNP
rs1290714917	1112	dbSNP
rs546796324	1113	dbSNP
rs182270980	1114	dbSNP
rs1401681592	1120	dbSNP
rs1169076637	1123	dbSNP
rs1261855770	1129	dbSNP
rs1367516953	1131	dbSNP
rs745837505	1131	dbSNP
rs1013203485	1133	dbSNP
rs1446196509	1133	dbSNP
rs374038485	1134	dbSNP
rs764889676	1136	dbSNP
rs1236092407	1138	dbSNP
rs1177793401	1139	dbSNP
rs1458110866	1140	dbSNP
rs1027649812	1146	dbSNP
rs888145458	1149	dbSNP
rs1024447894	1150	dbSNP
rs868531697	1151	dbSNP
rs1238912610	1157	dbSNP
rs1385297478	1158	dbSNP
rs1307455658	1164	dbSNP
rs1446515539	1165	dbSNP
rs1212760312	1170	dbSNP
rs907268571	1174	dbSNP
rs1004714326	1177	dbSNP
rs1163401417	1179	dbSNP
rs1389437751	1181	dbSNP
rs1426109386	1182	dbSNP
rs1383722181	1184	dbSNP
rs1378107984	1190	dbSNP
rs1422097466	1193	dbSNP
rs1440152107	1195	dbSNP
rs1234512865	1196	dbSNP
rs1196722593	1197	dbSNP
rs1004274071	1198	dbSNP
rs532884414	1203	dbSNP
rs1223338266	1204	dbSNP
rs1361777604	1210	dbSNP
rs1284230114	1218	dbSNP
rs1399083461	1218	dbSNP
rs963031564	1221	dbSNP
rs974135300	1221	dbSNP
rs1015185733	1223	dbSNP
rs1281747759	1227	dbSNP
rs1027560113	1229	dbSNP
rs528970793	1230	dbSNP
rs953297712	1238	dbSNP
rs1358222811	1239	dbSNP
rs1297259195	1240	dbSNP
rs1420053732	1241	dbSNP
rs1336238203	1244	dbSNP
rs1170621743	1246	dbSNP
rs985938155	1246	dbSNP
rs1378139771	1248	dbSNP
rs1200231365	1251	dbSNP
rs1341335868	1251	dbSNP
rs911739263	1253	dbSNP
rs976433143	1256	dbSNP
rs1452158172	1259	dbSNP
rs1028146547	1265	dbSNP
rs1314134671	1266	dbSNP
rs954010027	1267	dbSNP
rs1242230839	1273	dbSNP
rs1261179068	1274	dbSNP
rs1280859022	1282	dbSNP
rs1284555320	1283	dbSNP
rs935655246	1284	dbSNP
rs568860870	1287	dbSNP
rs1337829609	1288	dbSNP
rs768705374	1293	dbSNP
rs1346614215	1294	dbSNP
rs1331882616	1298	dbSNP
rs915128049	1301	dbSNP
rs1482514567	1302	dbSNP
rs536272662	1311	dbSNP
rs548172923	1314	dbSNP
rs1481439943	1315	dbSNP
rs1461509326	1317	dbSNP
rs1193064118	1324	dbSNP
rs945281704	1325	dbSNP
rs948987981	1326	dbSNP
rs1442264588	1327	dbSNP
rs1182557633	1329	dbSNP
rs1206081212	1329	dbSNP
rs1241693036	1330	dbSNP
rs1256806931	1332	dbSNP
rs1316621073	1332	dbSNP
rs543915315	1333	dbSNP
rs924565520	1338	dbSNP
rs938757829	1339	dbSNP
rs566580705	1341	dbSNP
rs539991105	1342	dbSNP
rs1363788872	1352	dbSNP
rs894684023	1353	dbSNP
rs1174435683	1356	dbSNP
rs1402938420	1357	dbSNP
rs1469509540	1359	dbSNP
rs1169748318	1360	dbSNP
rs776756677	1365	dbSNP
rs1016087252	1366	dbSNP
rs1180387277	1366	dbSNP
rs1472611163	1367	dbSNP
rs1048669629	1368	dbSNP
rs1185828179	1369	dbSNP
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rs1181513415	1825	dbSNP
rs1037241971	1828	dbSNP
rs900870284	1831	dbSNP
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rs1341057097	1835	dbSNP
rs1157760997	1837	dbSNP
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rs1049373772	1839	dbSNP
rs1383427642	1848	dbSNP
rs1336914046	1857	dbSNP
rs889549469	1863	dbSNP
rs931459239	1867	dbSNP
rs570501052	1871	dbSNP
rs1010614473	1872	dbSNP

- Cell, 2010

RNA transcripts are subject to posttranscriptional gene regulation involving hundreds of RNA-binding proteins (RBPs) and microRNA-containing ribonucleoprotein complexes (miRNPs) expressed in a cell-type dependent fashion. We developed a cell-based crosslinking approach to determine at high resolution and transcriptome-wide the binding sites of cellular RBPs and miRNPs. The crosslinked sites are revealed by thymidine to cytidine transitions in the cDNAs prepared from immunopurified RNPs of 4-thiouridine-treated cells. We determined the binding sites and regulatory consequences for several intensely studied RBPs and miRNPs, including PUM2, QKI, IGF2BP1-3, AGO/EIF2C1-4 and TNRC6A-C. Our study revealed that these factors bind thousands of sites containing defined sequence motifs and have distinct preferences for exonic versus intronic or coding versus untranslated transcript regions. The precise mapping of binding sites across the transcriptome will be critical to the interpretation of the rapidly emerging data on genetic variation between individuals and how these variations contribute to complex genetic diseases.

- Nature methods, 2011

Cross-linking and immunoprecipitation (CLIP) is increasingly used to map transcriptome-wide binding sites of RNA-binding proteins. We developed a method for CLIP data analysis, and applied it to compare CLIP with photoactivatable ribonucleoside-enhanced CLIP (PAR-CLIP) and to uncover how differences in cross-linking and ribonuclease digestion affect the identified sites. We found only small differences in accuracies of these methods in identifying binding sites of HuR, which binds low-complexity sequences, and Argonaute 2, which has a complex binding specificity. We found that cross-link-induced mutations led to single-nucleotide resolution for both PAR-CLIP and CLIP. Our results confirm the expectation from original CLIP publications that RNA-binding proteins do not protect their binding sites sufficiently under the denaturing conditions used during the CLIP procedure, and we show that extensive digestion with sequence-specific RNases strongly biases the recovered binding sites. This bias can be substantially reduced by milder nuclease digestion conditions.

- Nature, 2013

Circular RNAs (circRNAs) in animals are an enigmatic class of RNA with unknown function. To explore circRNAs systematically, we sequenced and computationally analysed human, mouse and nematode RNA. We detected thousands of well-expressed, stable circRNAs, often showing tissue/developmental-stage-specific expression. Sequence analysis indicated important regulatory functions for circRNAs. We found that a human circRNA, antisense to the cerebellar degeneration-related protein 1 transcript (CDR1as), is densely bound by microRNA (miRNA) effector complexes and harbours 63 conserved binding sites for the ancient miRNA miR-7. Further analyses indicated that CDR1as functions to bind miR-7 in neuronal tissues. Human CDR1as expression in zebrafish impaired midbrain development, similar to knocking down miR-7, suggesting that CDR1as is a miRNA antagonist with a miRNA-binding capacity ten times higher than any other known transcript. Together, our data provide evidence that circRNAs form a large class of post-transcriptional regulators. Numerous circRNAs form by head-to-tail splicing of exons, suggesting previously unrecognized regulatory potential of coding sequences.

- mBio, 2013

UNLABELLED: The question of how HIV-1 interfaces with cellular microRNA (miRNA) biogenesis and effector mechanisms has been highly controversial. Here, we first used deep sequencing of small RNAs present in two different infected cell lines (TZM-bl and C8166) and two types of primary human cells (CD4(+) peripheral blood mononuclear cells [PBMCs] and macrophages) to unequivocally demonstrate that HIV-1 does not encode any viral miRNAs. Perhaps surprisingly, we also observed that infection of T cells by HIV-1 has only a modest effect on the expression of cellular miRNAs at early times after infection. Comprehensive analysis of miRNA binding to the HIV-1 genome using the photoactivatable ribonucleoside-induced cross-linking and immunoprecipitation (PAR-CLIP) technique revealed several binding sites for cellular miRNAs, a subset of which were shown to be capable of mediating miRNA-mediated repression of gene expression. However, the main finding from this analysis is that HIV-1 transcripts are largely refractory to miRNA binding, most probably due to extensive viral RNA secondary structure. Together, these data demonstrate that HIV-1 neither encodes viral miRNAs nor strongly influences cellular miRNA expression, at least early after infection, and imply that HIV-1 transcripts have evolved to avoid inhibition by preexisting cellular miRNAs by adopting extensive RNA secondary structures that occlude most potential miRNA binding sites. IMPORTANCE: MicroRNAs (miRNAs) are a ubiquitous class of small regulatory RNAs that serve as posttranscriptional regulators of gene expression. Previous work has suggested that HIV-1 might subvert the function of the cellular miRNA machinery by expressing viral miRNAs or by dramatically altering the level of cellular miRNA expression. Using very sensitive approaches, we now demonstrate that neither of these ideas is in fact correct. Moreover, HIV-1 transcripts appear to largely avoid regulation by cellular miRNAs by adopting an extensive RNA secondary structure that occludes the ability of cellular miRNAs to interact with viral mRNAs. Together, these data suggest that HIV-1, rather than seeking to control miRNA function in infected cells, has instead evolved a mechanism to become largely invisible to cellular miRNA effector mechanisms.

- Genome biology, 2014

BACKGROUND: Various microRNAs (miRNAs) are up- or downregulated in tumors. However, the repression of cognate miRNA targets responsible for the phenotypic effects of this dysregulation in patients remains largely unexplored. To define miRNA targets and associated pathways, together with their relationship to outcome in breast cancer, we integrated patient-paired miRNA-mRNA expression data with a set of validated miRNA targets and pathway inference. RESULTS: To generate a biochemically-validated set of miRNA-binding sites, we performed argonaute-2 photoactivatable-ribonucleoside-enhanced crosslinking and immunoprecipitation (AGO2-PAR-CLIP) in MCF7 cells. We then defined putative miRNA-target interactions using a computational model, which ranked and selected additional TargetScan-predicted interactions based on features of our AGO2-PAR-CLIP binding-site data. We subselected modeled interactions according to the abundance of their constituent miRNA and mRNA transcripts in tumors, and we took advantage of the variability of miRNA expression within molecular subtypes to detect miRNA repression. Interestingly, our data suggest that miRNA families control subtype-specific pathways; for example, miR-17, miR-19a, miR-25, and miR-200b show high miRNA regulatory activity in the triple-negative, basal-like subtype, whereas miR-22 and miR-24 do so in the HER2 subtype. An independent dataset validated our findings for miR-17 and miR-25, and showed a correlation between the expression levels of miR-182 targets and overall patient survival. Pathway analysis associated miR-17, miR-19a, and miR-200b with leukocyte transendothelial migration. CONCLUSIONS: We combined PAR-CLIP data with patient expression data to predict regulatory miRNAs, revealing potential therapeutic targets and prognostic markers in breast cancer.

- Neoplasia (New York, N.Y.), 2016

MicroRNA (miRNA) deregulation in prostate cancer (PCa) contributes to PCa initiation and metastatic progression. To comprehensively define the cancer-associated changes in miRNA targeting and function in commonly studied models of PCa, we performed photoactivatable ribonucleoside-enhanced cross-linking immunoprecipitation of the Argonaute protein in a panel of PCa cell lines modeling different stages of PCa progression. Using this comprehensive catalogue of miRNA targets, we analyzed miRNA targeting on known drivers of PCa and examined tissue-specific and stage-specific pathway targeting by miRNAs. We found that androgen receptor is the most frequently targeted PCa oncogene and that miR-148a targets the largest number of known PCa drivers. Globally, tissue-specific and stage-specific changes in miRNA targeting are driven by homeostatic response to active oncogenic pathways. Our findings indicate that, even in advanced PCa, the miRNA pool adapts to regulate continuing alterations in the cancer genome to balance oncogenic molecular changes. These findings are important because they are the first to globally characterize miRNA changes in PCa and demonstrate how the miRNA target spectrum responds to staged tumorigenesis.