Chromatin position effects assayed by thousands of reporters integrated in parallel
Reporter genes integrated into the genome are a powerful tool to reveal effects of regulatory elements and local chromatin context on gene expression. However, so far such reporter assays have been of low throughput. Here, we describe a multiplexing approach for the parallel monitoring of transcript...
Saved in:
| Published in: | Cell Vol. 154; no. 4; p. 914 |
|---|---|
| Main Authors: | , , , , , , , , , |
| Format: | Journal Article |
| Language: | English |
| Published: |
United States
15.08.2013
|
| Subjects: | |
| ISSN: | 1097-4172, 1097-4172 |
| Online Access: | Get more information |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| Abstract | Reporter genes integrated into the genome are a powerful tool to reveal effects of regulatory elements and local chromatin context on gene expression. However, so far such reporter assays have been of low throughput. Here, we describe a multiplexing approach for the parallel monitoring of transcriptional activity of thousands of randomly integrated reporters. More than 27,000 distinct reporter integrations in mouse embryonic stem cells, obtained with two different promoters, show ∼1,000-fold variation in expression levels. Data analysis indicates that lamina-associated domains act as attenuators of transcription, likely by reducing access of transcription factors to binding sites. Furthermore, chromatin compaction is predictive of reporter activity. We also found evidence for crosstalk between neighboring genes and estimate that enhancers can influence gene expression on average over ∼20 kb. The multiplexed reporter assay is highly flexible in design and can be modified to query a wide range of aspects of gene regulation. |
|---|---|
| AbstractList | Reporter genes integrated into the genome are a powerful tool to reveal effects of regulatory elements and local chromatin context on gene expression. However, so far such reporter assays have been of low throughput. Here, we describe a multiplexing approach for the parallel monitoring of transcriptional activity of thousands of randomly integrated reporters. More than 27,000 distinct reporter integrations in mouse embryonic stem cells, obtained with two different promoters, show ∼1,000-fold variation in expression levels. Data analysis indicates that lamina-associated domains act as attenuators of transcription, likely by reducing access of transcription factors to binding sites. Furthermore, chromatin compaction is predictive of reporter activity. We also found evidence for crosstalk between neighboring genes and estimate that enhancers can influence gene expression on average over ∼20 kb. The multiplexed reporter assay is highly flexible in design and can be modified to query a wide range of aspects of gene regulation. Reporter genes integrated into the genome are a powerful tool to reveal effects of regulatory elements and local chromatin context on gene expression. However, so far such reporter assays have been of low throughput. Here, we describe a multiplexing approach for the parallel monitoring of transcriptional activity of thousands of randomly integrated reporters. More than 27,000 distinct reporter integrations in mouse embryonic stem cells, obtained with two different promoters, show ∼1,000-fold variation in expression levels. Data analysis indicates that lamina-associated domains act as attenuators of transcription, likely by reducing access of transcription factors to binding sites. Furthermore, chromatin compaction is predictive of reporter activity. We also found evidence for crosstalk between neighboring genes and estimate that enhancers can influence gene expression on average over ∼20 kb. The multiplexed reporter assay is highly flexible in design and can be modified to query a wide range of aspects of gene regulation.Reporter genes integrated into the genome are a powerful tool to reveal effects of regulatory elements and local chromatin context on gene expression. However, so far such reporter assays have been of low throughput. Here, we describe a multiplexing approach for the parallel monitoring of transcriptional activity of thousands of randomly integrated reporters. More than 27,000 distinct reporter integrations in mouse embryonic stem cells, obtained with two different promoters, show ∼1,000-fold variation in expression levels. Data analysis indicates that lamina-associated domains act as attenuators of transcription, likely by reducing access of transcription factors to binding sites. Furthermore, chromatin compaction is predictive of reporter activity. We also found evidence for crosstalk between neighboring genes and estimate that enhancers can influence gene expression on average over ∼20 kb. The multiplexed reporter assay is highly flexible in design and can be modified to query a wide range of aspects of gene regulation. |
| Author | Pindyurin, Alexey V Wessels, Lodewyk F A van Lohuizen, Maarten Berns, Anton Akhtar, Waseem Meuleman, Wouter de Ridder, Jeroen Pagie, Ludo van Steensel, Bas de Jong, Johann |
| Author_xml | – sequence: 1 givenname: Waseem surname: Akhtar fullname: Akhtar, Waseem organization: Division of Molecular Genetics, The Netherlands Cancer Institute, Plesmanlaan 121, 1066 CX Amsterdam, the Netherlands – sequence: 2 givenname: Johann surname: de Jong fullname: de Jong, Johann – sequence: 3 givenname: Alexey V surname: Pindyurin fullname: Pindyurin, Alexey V – sequence: 4 givenname: Ludo surname: Pagie fullname: Pagie, Ludo – sequence: 5 givenname: Wouter surname: Meuleman fullname: Meuleman, Wouter – sequence: 6 givenname: Jeroen surname: de Ridder fullname: de Ridder, Jeroen – sequence: 7 givenname: Anton surname: Berns fullname: Berns, Anton – sequence: 8 givenname: Lodewyk F A surname: Wessels fullname: Wessels, Lodewyk F A – sequence: 9 givenname: Maarten surname: van Lohuizen fullname: van Lohuizen, Maarten – sequence: 10 givenname: Bas surname: van Steensel fullname: van Steensel, Bas |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/23953119$$D View this record in MEDLINE/PubMed |
| BookMark | eNpNkD9PwzAUxC1URP_AF2BAHlkS_Ow4sUdUUUCqxADMke3YNFUSB9sd-u1JRZGY7p3up9PTLdFs8INF6BZIDgTKh31ubNfllADLSZUTEBdoAURWWQEVnf2752gZ454QIjjnV2hOmeQMQC7Q-3oXfK9SO-DRxza1fsDWOWtSxCpGdbQN1kecdv4Q1dBE7B0OdvQh2RBxOyT7FVSaoFOBCqrrbHeNLp3qor056wp9bp4-1i_Z9u35df24zQwTPGWCOtAOHK20FIUUk-dMm9KWyolKA-MFBc6M0aUhTgKhtDSN1IoSM4UNXaH7394x-O-Djanu23iaRA12ereGgpYcClnBhN6d0YPubVOPoe1VONZ_Q9AfzARjUg |
| CitedBy_id | crossref_primary_10_1016_j_molcel_2023_02_011 crossref_primary_10_7554_eLife_32911 crossref_primary_10_1016_j_neuron_2020_05_038 crossref_primary_10_1038_nature23884 crossref_primary_10_1101_gr_224717_117 crossref_primary_10_1101_gr_241653_118 crossref_primary_10_1016_j_scienta_2023_112161 crossref_primary_10_1146_annurev_genet_071719_030438 crossref_primary_10_1093_hmg_ddv096 crossref_primary_10_1002_biot_201900313 crossref_primary_10_1371_journal_pgen_1007276 crossref_primary_10_1007_s00018_020_03731_4 crossref_primary_10_1134_S0006297924601813 crossref_primary_10_1038_s41556_020_00620_7 crossref_primary_10_1038_nprot_2014_072 crossref_primary_10_3389_fgene_2021_618189 crossref_primary_10_1038_mtna_2016_101 crossref_primary_10_1038_nbt_4285 crossref_primary_10_3389_fcell_2022_913458 crossref_primary_10_1016_j_cmi_2016_02_013 crossref_primary_10_1038_nprot_2017_148 crossref_primary_10_1093_plcell_koab093 crossref_primary_10_1186_s13059_023_02955_4 crossref_primary_10_1016_j_tcb_2025_03_001 crossref_primary_10_1093_nar_gkx601 crossref_primary_10_1016_j_cels_2024_08_007 crossref_primary_10_1016_j_tig_2016_05_004 crossref_primary_10_3390_cells8010030 crossref_primary_10_1038_nmeth_2885 crossref_primary_10_1038_s41598_018_28161_y crossref_primary_10_1016_j_molcel_2019_12_021 crossref_primary_10_1016_j_tig_2015_07_001 crossref_primary_10_1126_science_aac6529 crossref_primary_10_3389_fgene_2023_1237092 crossref_primary_10_1038_s41467_018_04451_x crossref_primary_10_1371_journal_pone_0174744 crossref_primary_10_1186_s13059_020_02156_3 crossref_primary_10_1002_bies_201400036 crossref_primary_10_3389_fgene_2022_818344 crossref_primary_10_1016_j_devcel_2025_02_013 crossref_primary_10_1101_gr_217075_116 crossref_primary_10_1038_s41588_024_02053_6 crossref_primary_10_1038_s41467_020_18368_x crossref_primary_10_1146_annurev_biochem_060614_034115 crossref_primary_10_3389_fimmu_2021_633825 crossref_primary_10_1016_j_molcel_2022_12_032 crossref_primary_10_1101_gr_276449_121 crossref_primary_10_1007_s11033_021_06160_z crossref_primary_10_1038_s41556_020_00630_5 crossref_primary_10_1038_s41588_021_00860_9 crossref_primary_10_1038_s41596_025_01244_7 crossref_primary_10_1073_pnas_1800650115 crossref_primary_10_1126_science_aak9849 crossref_primary_10_1242_dmm_046516 crossref_primary_10_7554_eLife_25100 crossref_primary_10_1038_s41467_018_03408_4 crossref_primary_10_1016_j_cell_2017_04_022 crossref_primary_10_1371_journal_pgen_1004250 crossref_primary_10_1242_dev_148304 crossref_primary_10_1371_journal_pone_0252674 crossref_primary_10_1038_nmeth_2679 crossref_primary_10_1093_nar_gkaa210 crossref_primary_10_1093_nar_gkae012 crossref_primary_10_1038_s41588_024_01706_w crossref_primary_10_1016_j_ceb_2025_102561 crossref_primary_10_1016_j_cels_2016_04_011 crossref_primary_10_1016_j_cobme_2017_10_011 crossref_primary_10_3389_fgene_2014_00335 crossref_primary_10_1038_s41467_023_41468_3 crossref_primary_10_3389_fgene_2016_00082 crossref_primary_10_1093_nar_gku1398 crossref_primary_10_3389_fbioe_2024_1327172 crossref_primary_10_1038_sdata_2017_20 crossref_primary_10_1146_annurev_biophys_052118_115638 crossref_primary_10_1016_j_gde_2024_102234 crossref_primary_10_1016_j_tig_2019_09_002 crossref_primary_10_1016_j_cell_2013_09_011 crossref_primary_10_1016_j_biochi_2024_08_002 crossref_primary_10_3389_fgeed_2020_609650 crossref_primary_10_1016_j_ymthe_2020_11_025 crossref_primary_10_1146_annurev_bioeng_071516_044649 crossref_primary_10_1038_s44318_024_00214_1 crossref_primary_10_3390_ijms242115771 crossref_primary_10_1101_gr_184341_114 crossref_primary_10_1038_s41598_020_77638_2 crossref_primary_10_1007_s12257_020_0093_7 crossref_primary_10_3390_antib8010010 crossref_primary_10_1007_s00412_023_00796_5 crossref_primary_10_1016_j_dnarep_2016_05_007 crossref_primary_10_1021_acssynbio_4c00678 crossref_primary_10_1016_j_molcel_2021_03_032 crossref_primary_10_1371_journal_pcbi_1011286 crossref_primary_10_1016_j_cels_2016_03_009 crossref_primary_10_1038_s41467_024_52599_6 crossref_primary_10_3389_fgene_2021_785947 crossref_primary_10_1186_s13045_022_01271_x crossref_primary_10_15252_msb_202010075 crossref_primary_10_1038_s41434_018_0021_z crossref_primary_10_1534_genetics_114_173187 crossref_primary_10_1016_j_molcel_2016_04_035 crossref_primary_10_1016_j_stem_2014_05_017 crossref_primary_10_1038_nrg3591 crossref_primary_10_15252_msb_20177548 crossref_primary_10_1038_s41576_019_0128_0 crossref_primary_10_1002_adhm_202000030 crossref_primary_10_1016_j_synbio_2024_04_007 crossref_primary_10_1007_s12038_019_9968_1 crossref_primary_10_1186_s12864_019_5847_2 crossref_primary_10_1002_bies_201500184 crossref_primary_10_1371_journal_pbio_3002347 crossref_primary_10_1134_S0006297918040077 crossref_primary_10_1038_s41467_019_09551_w crossref_primary_10_2217_epi_15_40 crossref_primary_10_1371_journal_pone_0122253 crossref_primary_10_1101_gad_310367_117 crossref_primary_10_1016_j_cell_2015_07_035 crossref_primary_10_1038_ncomms12621 crossref_primary_10_1093_molbev_msab104 crossref_primary_10_1016_j_cell_2019_03_009 crossref_primary_10_1371_journal_pone_0226570 crossref_primary_10_1093_nar_gkae062 crossref_primary_10_1371_journal_pbio_2005542 crossref_primary_10_1016_j_cell_2025_04_017 crossref_primary_10_1186_s13059_015_0719_9 crossref_primary_10_1146_annurev_genom_121219_083616 crossref_primary_10_1016_j_ceb_2014_03_003 crossref_primary_10_1002_bit_28390 crossref_primary_10_1016_j_ygeno_2015_06_009 crossref_primary_10_1093_nar_gku828 crossref_primary_10_1007_s00412_015_0534_9 crossref_primary_10_1016_j_ygeno_2015_06_005 crossref_primary_10_1016_j_ygeno_2015_06_004 crossref_primary_10_1101_gad_351800_124 crossref_primary_10_1016_j_ygeno_2015_06_001 crossref_primary_10_1016_j_ygeno_2015_06_003 crossref_primary_10_1186_s13068_017_0872_3 crossref_primary_10_1038_nrg3682 crossref_primary_10_1093_nar_gkw203 crossref_primary_10_12688_f1000research_11581_1 crossref_primary_10_1186_s13059_015_0747_5 crossref_primary_10_1038_s41598_022_13536_z crossref_primary_10_1002_bies_201900188 crossref_primary_10_1186_s13059_022_02665_3 crossref_primary_10_1016_j_bpj_2017_03_024 crossref_primary_10_1038_s41576_019_0209_0 crossref_primary_10_1186_s13059_015_0823_x crossref_primary_10_1007_s11010_014_2036_0 crossref_primary_10_1016_j_cels_2022_11_005 crossref_primary_10_1042_BST20210858 crossref_primary_10_1002_jssc_70159 crossref_primary_10_1101_gr_163519_113 crossref_primary_10_1016_j_ceb_2016_03_022 crossref_primary_10_1016_j_tibtech_2019_02_007 crossref_primary_10_1038_nsmb_3328 crossref_primary_10_1038_s41556_025_01735_5 crossref_primary_10_15252_embr_202255146 crossref_primary_10_3389_fphys_2021_786299 crossref_primary_10_1007_s12195_016_0437_8 crossref_primary_10_1016_j_ymthe_2024_09_033 crossref_primary_10_1038_s41576_018_0063_5 crossref_primary_10_1186_s13072_018_0235_8 crossref_primary_10_1242_dev_149427 crossref_primary_10_1042_BST20230917 crossref_primary_10_1016_j_dnarep_2023_103565 crossref_primary_10_1038_s41467_022_29697_4 crossref_primary_10_3390_cancers11040585 crossref_primary_10_1093_nar_gkw942 crossref_primary_10_3389_fpls_2021_674209 crossref_primary_10_1038_s41576_025_00841_2 crossref_primary_10_1093_biolre_ioz115 crossref_primary_10_1016_j_gene_2016_02_024 crossref_primary_10_1080_19491034_2021_1927503 crossref_primary_10_1016_j_gde_2019_04_008 crossref_primary_10_1016_j_gde_2019_04_007 crossref_primary_10_1016_j_jmb_2019_12_017 crossref_primary_10_1002_biot_201800226 crossref_primary_10_1186_s13059_016_0992_2 crossref_primary_10_1101_gr_212308_116 crossref_primary_10_1038_s41467_021_24436_7 crossref_primary_10_1016_j_cels_2019_02_004 crossref_primary_10_1186_s13059_016_1046_5 crossref_primary_10_1186_s13059_020_02002_6 crossref_primary_10_1007_s00418_015_1346_y crossref_primary_10_1101_gr_211433_116 crossref_primary_10_3389_fendo_2017_00058 crossref_primary_10_1101_gad_351424_123 crossref_primary_10_1016_j_tcb_2014_07_004 crossref_primary_10_1016_j_tcb_2019_06_001 crossref_primary_10_1016_j_cell_2019_08_013 crossref_primary_10_1016_j_gde_2013_10_014 crossref_primary_10_1038_s41467_024_49232_x crossref_primary_10_1042_BST20170153 crossref_primary_10_3389_fpls_2019_01209 crossref_primary_10_1038_nsmb_3358 crossref_primary_10_1016_j_bpj_2019_01_011 crossref_primary_10_1186_s13059_024_03277_9 crossref_primary_10_1042_BST20180503 crossref_primary_10_1016_j_molcel_2021_11_035 crossref_primary_10_1186_s13072_016_0096_y crossref_primary_10_1371_journal_pone_0223759 crossref_primary_10_1073_pnas_1410764111 crossref_primary_10_1016_j_chembiol_2022_02_005 crossref_primary_10_1134_S0026893322030049 crossref_primary_10_1016_j_gde_2017_01_003 crossref_primary_10_1016_j_semcdb_2018_07_008 crossref_primary_10_1177_11779322211072333 crossref_primary_10_3390_ijms232415485 crossref_primary_10_1002_bies_201500051 crossref_primary_10_1101_gr_276025_121 crossref_primary_10_1042_BCJ20240474 crossref_primary_10_3390_cells10092362 crossref_primary_10_1016_j_mce_2016_02_019 crossref_primary_10_1186_s13059_020_02003_5 crossref_primary_10_1038_ng_3878 crossref_primary_10_1038_s41467_019_09185_y crossref_primary_10_1073_pnas_1605862113 crossref_primary_10_1002_bies_201600032 crossref_primary_10_1038_s41592_024_02260_3 |
| ContentType | Journal Article |
| Copyright | Copyright © 2013 Elsevier Inc. All rights reserved. |
| Copyright_xml | – notice: Copyright © 2013 Elsevier Inc. All rights reserved. |
| DBID | CGR CUY CVF ECM EIF NPM 7X8 |
| DOI | 10.1016/j.cell.2013.07.018 |
| DatabaseName | Medline MEDLINE MEDLINE (Ovid) MEDLINE MEDLINE PubMed MEDLINE - Academic |
| DatabaseTitle | MEDLINE Medline Complete MEDLINE with Full Text PubMed MEDLINE (Ovid) MEDLINE - Academic |
| DatabaseTitleList | MEDLINE MEDLINE - Academic |
| Database_xml | – sequence: 1 dbid: NPM name: PubMed url: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed sourceTypes: Index Database – sequence: 2 dbid: 7X8 name: MEDLINE - Academic url: https://search.proquest.com/medline sourceTypes: Aggregation Database |
| DeliveryMethod | no_fulltext_linktorsrc |
| Discipline | Biology |
| EISSN | 1097-4172 |
| ExternalDocumentID | 23953119 |
| Genre | Research Support, Non-U.S. Gov't Journal Article |
| GroupedDBID | --- --K -DZ -ET -~X 0R~ 0WA 1RT 1~5 29B 2FS 2WC 3EH 4.4 457 4G. 53G 5GY 5RE 5VS 62- 6J9 7-5 85S AAEDT AAEDW AAFWJ AAHBH AAIKJ AAKRW AAKUH AALRI AAMRU AAQFI AAVLU AAXUO AAYJJ AAYWO ABCQX ABDGV ABJNI ABMAC ABOCM ACGFO ACGFS ACNCT ACVFH ADBBV ADCNI ADEZE ADVLN ADXHL AEFWE AENEX AEUPX AEXQZ AFPUW AFTJW AGCQF AGHFR AGHSJ AGKMS AHHHB AIDAL AIGII AITUG AKAPO AKBMS AKRWK AKYEP ALMA_UNASSIGNED_HOLDINGS AMRAJ APXCP ASPBG AVWKF AZFZN BAWUL CGR CS3 CUY CVF DIK DU5 E3Z EBS ECM EFKBS EIF EJD F5P FCP FDB FIRID HH5 IH2 IHE IXB J1W JIG K-O KOO KQ8 L7B LX5 M3Z M41 N9A NPM O-L O9- OK1 P2P RIG RNS ROL RPZ SCP SDG SDP SES SSZ TAE TN5 TR2 TWZ UKR UPT WH7 YYQ YZZ ZCA 7X8 |
| ID | FETCH-LOGICAL-c385t-82f1bf1f27b9849882f53bc6e6af87b13542153ccb6c0f910226cd9ba20c135d2 |
| IEDL.DBID | 7X8 |
| ISICitedReferencesCount | 249 |
| ISICitedReferencesURI | http://www.webofscience.com/api/gateway?GWVersion=2&SrcApp=Summon&SrcAuth=ProQuest&DestLinkType=CitingArticles&DestApp=WOS_CPL&KeyUT=000323202500020&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D |
| ISSN | 1097-4172 |
| IngestDate | Thu Oct 02 07:12:29 EDT 2025 Mon Jul 21 06:04:03 EDT 2025 |
| IsDoiOpenAccess | false |
| IsOpenAccess | true |
| IsPeerReviewed | true |
| IsScholarly | true |
| Issue | 4 |
| Language | English |
| License | Copyright © 2013 Elsevier Inc. All rights reserved. |
| LinkModel | DirectLink |
| MergedId | FETCHMERGED-LOGICAL-c385t-82f1bf1f27b9849882f53bc6e6af87b13542153ccb6c0f910226cd9ba20c135d2 |
| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 |
| OpenAccessLink | https://dx.doi.org/10.1016/j.cell.2013.07.018 |
| PMID | 23953119 |
| PQID | 1426514971 |
| PQPubID | 23479 |
| ParticipantIDs | proquest_miscellaneous_1426514971 pubmed_primary_23953119 |
| PublicationCentury | 2000 |
| PublicationDate | 2013-08-15 |
| PublicationDateYYYYMMDD | 2013-08-15 |
| PublicationDate_xml | – month: 08 year: 2013 text: 2013-08-15 day: 15 |
| PublicationDecade | 2010 |
| PublicationPlace | United States |
| PublicationPlace_xml | – name: United States |
| PublicationTitle | Cell |
| PublicationTitleAlternate | Cell |
| PublicationYear | 2013 |
| References | 24161983 - Nat Methods. 2013 Oct;10(10):937 |
| References_xml | – reference: 24161983 - Nat Methods. 2013 Oct;10(10):937 |
| SSID | ssj0008555 |
| Score | 2.5476494 |
| Snippet | Reporter genes integrated into the genome are a powerful tool to reveal effects of regulatory elements and local chromatin context on gene expression. However,... |
| SourceID | proquest pubmed |
| SourceType | Aggregation Database Index Database |
| StartPage | 914 |
| SubjectTerms | Animals Chromatin - metabolism Chromosomal Position Effects Embryonic Stem Cells - metabolism Genes, Reporter Genetic Techniques High-Throughput Nucleotide Sequencing Mice Promoter Regions, Genetic |
| Title | Chromatin position effects assayed by thousands of reporters integrated in parallel |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/23953119 https://www.proquest.com/docview/1426514971 |
| Volume | 154 |
| WOSCitedRecordID | wos000323202500020&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D |
| hasFullText | |
| inHoldings | 1 |
| isFullTextHit | |
| isPrint | |
| link | http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwpV1LS8QwEA7qKnjx_VhfRPAabJOmTU4i4uJBlwUV9laSNEFB2nV3EfbfO9OHexIEL72UhnaSZr6Z-TIfIVdSSuMlhCWFd5JhRzpmtOQs4s4J7aPEuXqmH7PhUI3HetQm3GYtrbLbE-uNuqgc5sivY3Al4Nx1Ft9MPhmqRmF1tZXQWCU9AVAGKV3ZeNktXMla9RSLrCwBT90emmn4XZgYR2qXqJt3xup3iFm7msH2f19yh2y1IJPeNqtil6z4co9sNLKTi33yjB1xEamWtONs0ZbXQQFLm4UvqF3Q-VuFlJ1iRqtAm9oCYEX602CioDiAmaIay8cBeR3cv9w9sFZcgTmh5JwpHmIb4sAzq1WiAWgHKaxLfWqCymwsZAJoQDhnUxcFjYFh6gptDY8c3Cz4IVkrq9IfE5pw7oPIPMeTUQoQl-Ep9zDV2jtrvO6Ty85aOSxeNLwpPXxCvrRXnxw1Js8nTZeNnAsN-0OsT_7w9CnZ5LVMBUTE8oz0Avy6_pysu6_5-2x6Ua8KuA5HT9_-jsHN |
| linkProvider | ProQuest |
| openUrl | ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Chromatin+position+effects+assayed+by+thousands+of+reporters+integrated+in+parallel&rft.jtitle=Cell&rft.au=Akhtar%2C+Waseem&rft.au=de+Jong%2C+Johann&rft.au=Pindyurin%2C+Alexey+V&rft.au=Pagie%2C+Ludo&rft.date=2013-08-15&rft.issn=1097-4172&rft.eissn=1097-4172&rft.volume=154&rft.issue=4&rft.spage=914&rft_id=info:doi/10.1016%2Fj.cell.2013.07.018&rft.externalDBID=NO_FULL_TEXT |
| thumbnail_l | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1097-4172&client=summon |
| thumbnail_m | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1097-4172&client=summon |
| thumbnail_s | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1097-4172&client=summon |