MicroRNA-339-5p down-regulates protein expression of β-site amyloid precursor protein-cleaving enzyme 1 (BACE1) in human primary brain cultures and is reduced in brain tissue specimens of Alzheimer disease subjects
Alzheimer disease (AD) results, in part, from the excess accumulation of the amyloid-β (Aβ) peptide as neuritic plaques in the brain. The short Aβ peptide is derived from the large transmembrane Aβ precursor protein (APP). The rate-limiting step in the production of Aβ from APP is mediated by the β-...
Saved in:
| Published in: | The Journal of biological chemistry Vol. 289; no. 8; p. 5184 |
|---|---|
| Main Authors: | , , |
| Format: | Journal Article |
| Language: | English |
| Published: |
United States
21.02.2014
|
| Subjects: | |
| ISSN: | 1083-351X, 1083-351X |
| Online Access: | Get more information |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| Abstract | Alzheimer disease (AD) results, in part, from the excess accumulation of the amyloid-β (Aβ) peptide as neuritic plaques in the brain. The short Aβ peptide is derived from the large transmembrane Aβ precursor protein (APP). The rate-limiting step in the production of Aβ from APP is mediated by the β-site APP-cleaving enzyme 1 (BACE1). Dysregulation of BACE1 levels leading to excess Aβ deposition is implicated in sporadic AD. Thus, elucidating the full complement of regulatory pathways that control BACE1 expression is key to identifying novel drug targets central to the Aβ-generating process. MicroRNAs (miRNAs) are expected to participate in this molecular network. Here, we identified a known miRNA, miR-339-5p, as a key contributor to this regulatory network. Two distinct miR-339-5p target sites were predicted in the BACE1 3'-UTR by in silico analyses. Co-transfection of miR-339-5p with a BACE1 3'-UTR reporter construct resulted in significant reduction in reporter expression. Mutation of both target sites eliminated this effect. Delivery of the miR-339-5p mimic also significantly inhibited expression of BACE1 protein in human glioblastoma cells and human primary brain cultures. Delivery of target protectors designed against the miR-339-5p BACE1 3'-UTR target sites in primary human brain cultures significantly elevated BACE1 expression. Finally, miR-339-5p levels were found to be significantly reduced in brain specimens isolated from AD patients as compared with age-matched controls. Therefore, miR-339-5p regulates BACE1 expression in human brain cells and is most likely dysregulated in at least a subset of AD patients making this miRNA a novel drug target. |
|---|---|
| AbstractList | Alzheimer disease (AD) results, in part, from the excess accumulation of the amyloid-β (Aβ) peptide as neuritic plaques in the brain. The short Aβ peptide is derived from the large transmembrane Aβ precursor protein (APP). The rate-limiting step in the production of Aβ from APP is mediated by the β-site APP-cleaving enzyme 1 (BACE1). Dysregulation of BACE1 levels leading to excess Aβ deposition is implicated in sporadic AD. Thus, elucidating the full complement of regulatory pathways that control BACE1 expression is key to identifying novel drug targets central to the Aβ-generating process. MicroRNAs (miRNAs) are expected to participate in this molecular network. Here, we identified a known miRNA, miR-339-5p, as a key contributor to this regulatory network. Two distinct miR-339-5p target sites were predicted in the BACE1 3'-UTR by in silico analyses. Co-transfection of miR-339-5p with a BACE1 3'-UTR reporter construct resulted in significant reduction in reporter expression. Mutation of both target sites eliminated this effect. Delivery of the miR-339-5p mimic also significantly inhibited expression of BACE1 protein in human glioblastoma cells and human primary brain cultures. Delivery of target protectors designed against the miR-339-5p BACE1 3'-UTR target sites in primary human brain cultures significantly elevated BACE1 expression. Finally, miR-339-5p levels were found to be significantly reduced in brain specimens isolated from AD patients as compared with age-matched controls. Therefore, miR-339-5p regulates BACE1 expression in human brain cells and is most likely dysregulated in at least a subset of AD patients making this miRNA a novel drug target. Alzheimer disease (AD) results, in part, from the excess accumulation of the amyloid-β (Aβ) peptide as neuritic plaques in the brain. The short Aβ peptide is derived from the large transmembrane Aβ precursor protein (APP). The rate-limiting step in the production of Aβ from APP is mediated by the β-site APP-cleaving enzyme 1 (BACE1). Dysregulation of BACE1 levels leading to excess Aβ deposition is implicated in sporadic AD. Thus, elucidating the full complement of regulatory pathways that control BACE1 expression is key to identifying novel drug targets central to the Aβ-generating process. MicroRNAs (miRNAs) are expected to participate in this molecular network. Here, we identified a known miRNA, miR-339-5p, as a key contributor to this regulatory network. Two distinct miR-339-5p target sites were predicted in the BACE1 3'-UTR by in silico analyses. Co-transfection of miR-339-5p with a BACE1 3'-UTR reporter construct resulted in significant reduction in reporter expression. Mutation of both target sites eliminated this effect. Delivery of the miR-339-5p mimic also significantly inhibited expression of BACE1 protein in human glioblastoma cells and human primary brain cultures. Delivery of target protectors designed against the miR-339-5p BACE1 3'-UTR target sites in primary human brain cultures significantly elevated BACE1 expression. Finally, miR-339-5p levels were found to be significantly reduced in brain specimens isolated from AD patients as compared with age-matched controls. Therefore, miR-339-5p regulates BACE1 expression in human brain cells and is most likely dysregulated in at least a subset of AD patients making this miRNA a novel drug target.Alzheimer disease (AD) results, in part, from the excess accumulation of the amyloid-β (Aβ) peptide as neuritic plaques in the brain. The short Aβ peptide is derived from the large transmembrane Aβ precursor protein (APP). The rate-limiting step in the production of Aβ from APP is mediated by the β-site APP-cleaving enzyme 1 (BACE1). Dysregulation of BACE1 levels leading to excess Aβ deposition is implicated in sporadic AD. Thus, elucidating the full complement of regulatory pathways that control BACE1 expression is key to identifying novel drug targets central to the Aβ-generating process. MicroRNAs (miRNAs) are expected to participate in this molecular network. Here, we identified a known miRNA, miR-339-5p, as a key contributor to this regulatory network. Two distinct miR-339-5p target sites were predicted in the BACE1 3'-UTR by in silico analyses. Co-transfection of miR-339-5p with a BACE1 3'-UTR reporter construct resulted in significant reduction in reporter expression. Mutation of both target sites eliminated this effect. Delivery of the miR-339-5p mimic also significantly inhibited expression of BACE1 protein in human glioblastoma cells and human primary brain cultures. Delivery of target protectors designed against the miR-339-5p BACE1 3'-UTR target sites in primary human brain cultures significantly elevated BACE1 expression. Finally, miR-339-5p levels were found to be significantly reduced in brain specimens isolated from AD patients as compared with age-matched controls. Therefore, miR-339-5p regulates BACE1 expression in human brain cells and is most likely dysregulated in at least a subset of AD patients making this miRNA a novel drug target. |
| Author | Long, Justin M Ray, Balmiki Lahiri, Debomoy K |
| Author_xml | – sequence: 1 givenname: Justin M surname: Long fullname: Long, Justin M organization: From the Laboratory of Molecular Neurogenetics, Institute of Psychiatric Research, Departments of Psychiatry and – sequence: 2 givenname: Balmiki surname: Ray fullname: Ray, Balmiki – sequence: 3 givenname: Debomoy K surname: Lahiri fullname: Lahiri, Debomoy K |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/24352696$$D View this record in MEDLINE/PubMed |
| BookMark | eNpNkUtvEzEQgC1URNvAmRvysRwc_Fhvdo8hCi1SCxICiVvktSeto107eNaF9Gf1h_TK38FRUom5zOvTPM_JSYgBCHkr-FTwWfVh09npjRBqqkUjK_GCnAneKKa0-Hnyn31KzhE3vEjVilfkVFZKy7qtz8jfG29T_PZlzpRqmd5SF38HluA292YEpNsUR_CBwp9tAkQfA41r-vTI0I9AzbDro3eFApsTxvTMM9uDuffhlkJ42A1ABb34OF8sxXtait3lwYSC-sGkHe2SKTGb-zGXFtQERz3SBC5bcHv8AIweMQPFLVg_QMD9HPP-4Q6Kl6jzCAZLOncbsCO-Ji_Xpkd4c9QT8uPT8vviil1_vfy8mF8zW1VqZPVadDDTdTOTFWirlHRONLZ1zjbGtYYLzl1tjLKNko1TTlsNRnbAOyX3N5-Qi0PdsvivDDiuBo8W-t4EiBlXQnPRlGPLWUHfHdHcDeBWx_1Xz8-Q_wAU15La |
| CitedBy_id | crossref_primary_10_1007_s12035_023_03626_y crossref_primary_10_3233_JAD_190583 crossref_primary_10_1038_s41398_020_0709_x crossref_primary_10_1016_j_biopsych_2020_02_001 crossref_primary_10_3390_biom11020195 crossref_primary_10_1016_j_bbrc_2016_08_067 crossref_primary_10_3390_genes11090983 crossref_primary_10_1186_s13195_021_00862_z crossref_primary_10_1007_s11011_023_01265_9 crossref_primary_10_1007_s12035_019_1562_x crossref_primary_10_3233_JAD_220116 crossref_primary_10_1155_2019_7935310 crossref_primary_10_1016_j_biopha_2018_02_043 crossref_primary_10_1111_acel_13033 crossref_primary_10_3233_JAD_180259 crossref_primary_10_3390_ijms24065909 crossref_primary_10_1007_s13237_023_00427_5 crossref_primary_10_4103_aian_aian_202_22 crossref_primary_10_1002_alz_14230 crossref_primary_10_1016_j_biopha_2024_116691 crossref_primary_10_3390_molecules25153337 crossref_primary_10_3389_fnagi_2021_632891 crossref_primary_10_3892_etm_2016_3366 crossref_primary_10_3389_fgene_2019_00153 crossref_primary_10_1007_s12031_014_0428_y crossref_primary_10_3233_JAD_191303 crossref_primary_10_1007_s00221_017_4989_1 crossref_primary_10_1016_j_jnutbio_2015_07_020 crossref_primary_10_3233_JAD_181078 crossref_primary_10_3390_pharmaceutics13091397 crossref_primary_10_1016_j_neubiorev_2018_11_007 crossref_primary_10_1038_srep19946 crossref_primary_10_1177_0706743718772514 crossref_primary_10_3389_fnagi_2021_641080 crossref_primary_10_61958_NDAA5301 crossref_primary_10_1007_s12035_015_9484_8 crossref_primary_10_1096_fj_201801846R crossref_primary_10_3390_jpm11121275 crossref_primary_10_1177_0271678X251366082 crossref_primary_10_1016_j_ymthe_2021_11_006 crossref_primary_10_1016_j_cellsig_2020_109696 crossref_primary_10_1016_j_pneurobio_2017_03_004 crossref_primary_10_1016_j_jchemneu_2023_102236 crossref_primary_10_3892_ijmm_2017_3348 crossref_primary_10_3389_fbioe_2019_00222 crossref_primary_10_3390_jcm8070963 crossref_primary_10_1097_PAI_0000000000000147 crossref_primary_10_1002_wrna_1463 crossref_primary_10_1016_j_bbrc_2014_08_092 crossref_primary_10_3390_cells11010163 crossref_primary_10_1016_j_bbagrm_2020_194562 crossref_primary_10_1007_s11010_024_05164_0 crossref_primary_10_3389_fnagi_2022_880167 crossref_primary_10_3390_cells12101378 crossref_primary_10_1373_clinchem_2014_232165 crossref_primary_10_1007_s13311_019_00753_0 crossref_primary_10_3390_ijms21144977 crossref_primary_10_1186_s12974_024_03031_9 crossref_primary_10_1080_14728222_2021_1916469 crossref_primary_10_4103_1673_5374_221147 crossref_primary_10_3389_fneur_2017_00342 crossref_primary_10_1177_0271678X241254772 crossref_primary_10_1007_s11596_020_2283_0 crossref_primary_10_3233_JAD_180487 crossref_primary_10_3389_fneur_2020_538301 crossref_primary_10_1007_s12035_019_01676_9 crossref_primary_10_1038_s41380_018_0266_3 crossref_primary_10_1038_srep26052 crossref_primary_10_3233_JAD_215349 crossref_primary_10_1186_s13148_017_0365_z crossref_primary_10_1016_j_neurobiolaging_2019_06_005 crossref_primary_10_1242_jcs_147553 crossref_primary_10_3389_fphar_2019_00665 crossref_primary_10_3390_ijms242216259 crossref_primary_10_1038_s41388_019_0771_0 crossref_primary_10_1016_j_heliyon_2024_e27307 crossref_primary_10_1016_j_brainres_2024_148791 crossref_primary_10_1007_s11011_024_01431_7 crossref_primary_10_1016_j_arr_2024_102614 crossref_primary_10_1038_nrg3934 crossref_primary_10_1172_JCI149160 crossref_primary_10_1186_s13578_023_01190_5 crossref_primary_10_1186_s12888_023_04565_7 crossref_primary_10_1186_s40035_024_00428_7 crossref_primary_10_1016_j_brainres_2021_147622 crossref_primary_10_3390_nu8090556 crossref_primary_10_1016_j_omtn_2020_01_009 crossref_primary_10_1002_jcb_28276 crossref_primary_10_1016_j_jpsychires_2016_09_003 crossref_primary_10_1002_ajmg_b_32457 crossref_primary_10_1515_revneuro_2017_0042 crossref_primary_10_3389_fnmol_2020_00160 crossref_primary_10_1016_j_mad_2016_12_003 crossref_primary_10_3390_biom13010018 crossref_primary_10_1007_s12035_023_03859_x crossref_primary_10_1016_S1474_4422_16_00065_X crossref_primary_10_1016_j_envpol_2024_125440 crossref_primary_10_3390_ijms18122698 crossref_primary_10_1016_j_omtn_2024_102439 crossref_primary_10_1002_jcb_28361 crossref_primary_10_3892_etm_2018_6359 crossref_primary_10_1016_j_neuint_2019_104642 crossref_primary_10_1007_s11064_018_2475_1 crossref_primary_10_3389_fnins_2017_00386 crossref_primary_10_1186_s13041_014_0063_0 crossref_primary_10_3390_ijms151120266 crossref_primary_10_3233_JAD_150395 crossref_primary_10_3389_fnmol_2024_1386735 crossref_primary_10_2217_nmt_14_52 crossref_primary_10_1038_s41380_019_0610_2 crossref_primary_10_1111_jnc_13507 crossref_primary_10_1007_s00775_019_01739_1 crossref_primary_10_3389_fnagi_2016_00013 crossref_primary_10_1007_s12035_019_1500_y crossref_primary_10_1038_s41380_021_01351_3 crossref_primary_10_1007_s10529_020_02915_z crossref_primary_10_1007_s11033_025_10284_x crossref_primary_10_2174_1381612828666220408124809 crossref_primary_10_3390_nu9090927 crossref_primary_10_1016_j_bbr_2023_114359 crossref_primary_10_3389_fnmol_2024_1370449 crossref_primary_10_1007_s10561_020_09896_3 crossref_primary_10_3390_diagnostics12122975 crossref_primary_10_1016_j_trsl_2014_05_006 crossref_primary_10_1038_s41598_022_05164_4 crossref_primary_10_3389_fncel_2018_00224 crossref_primary_10_1016_j_ijcard_2015_04_021 crossref_primary_10_1002_alz_70399 crossref_primary_10_3389_fnmol_2016_00129 |
| ContentType | Journal Article |
| DBID | CGR CUY CVF ECM EIF NPM 7X8 |
| DOI | 10.1074/jbc.M113.518241 |
| 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 | Anatomy & Physiology Chemistry |
| EISSN | 1083-351X |
| ExternalDocumentID | 24352696 |
| Genre | Research Support, Non-U.S. Gov't Journal Article Research Support, N.I.H., Extramural |
| GrantInformation_xml | – fundername: NIA NIH HHS grantid: AG18884 – fundername: NIA NIH HHS grantid: AG042804 – fundername: NIA NIH HHS grantid: R01 AG018379 – fundername: NIA NIH HHS grantid: R01 AG018884 – fundername: NIA NIH HHS grantid: R21 AG042804 – fundername: NHLBI NIH HHS grantid: HL107920 |
| GroupedDBID | --- -DZ -ET -~X 0R~ 18M 29J 2WC 34G 39C 4.4 53G 5BI 5GY 5RE 5VS 79B 85S AAEDW AAFWJ AALRI AARDX AAXUO ABDNZ ABOCM ABPPZ ABRJW ACGFO ACNCT ADBBV ADIYS ADNWM ADVLN AENEX AEXQZ AFOSN AFPKN AITUG AKRWK ALMA_UNASSIGNED_HOLDINGS AMRAJ AOIJS BAWUL BTFSW CGR CJ0 CS3 CUY CVF DIK DU5 E3Z EBS ECM EIF EJD F5P FDB FRP GROUPED_DOAJ GX1 H13 HH5 HYE IH2 KQ8 L7B N9A NPM OK1 P0W P2P R.V RHF RHI RNS ROL RPM SJN TBC TN5 TR2 UHB UKR UPT VQA W8F WH7 WOQ XSW YQT YSK YWH YZZ Z5M ~02 ~KM .7T 7X8 AAYWO ABUFD ACVFH ADCNI AEUPX AFPUW AIGII AKBMS AKYEP |
| ID | FETCH-LOGICAL-c443t-6f1be7568724e5c332dd18c9ddc8ad9a0100d6aa3c8328d3d5c5ea2be0b325182 |
| IEDL.DBID | 7X8 |
| ISICitedReferencesCount | 167 |
| ISICitedReferencesURI | http://www.webofscience.com/api/gateway?GWVersion=2&SrcApp=Summon&SrcAuth=ProQuest&DestLinkType=CitingArticles&DestApp=WOS_CPL&KeyUT=000331607900060&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D |
| ISSN | 1083-351X |
| IngestDate | Sun Nov 09 10:19:49 EST 2025 Wed Feb 19 02:29:34 EST 2025 |
| IsDoiOpenAccess | false |
| IsOpenAccess | true |
| IsPeerReviewed | true |
| IsScholarly | true |
| Issue | 8 |
| Keywords | Gene Regulation Noncoding RNA MicroRNA Secretases β-Peptide Aging Alzheimer Disease Human Neuron Dementia Human Brain Tissue |
| Language | English |
| LinkModel | DirectLink |
| MergedId | FETCHMERGED-LOGICAL-c443t-6f1be7568724e5c332dd18c9ddc8ad9a0100d6aa3c8328d3d5c5ea2be0b325182 |
| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 |
| OpenAccessLink | https://dx.doi.org/10.1074/jbc.M113.518241 |
| PMID | 24352696 |
| PQID | 1501835227 |
| PQPubID | 23479 |
| ParticipantIDs | proquest_miscellaneous_1501835227 pubmed_primary_24352696 |
| PublicationCentury | 2000 |
| PublicationDate | 2014-02-21 |
| PublicationDateYYYYMMDD | 2014-02-21 |
| PublicationDate_xml | – month: 02 year: 2014 text: 2014-02-21 day: 21 |
| PublicationDecade | 2010 |
| PublicationPlace | United States |
| PublicationPlace_xml | – name: United States |
| PublicationTitle | The Journal of biological chemistry |
| PublicationTitleAlternate | J Biol Chem |
| PublicationYear | 2014 |
| SSID | ssj0000491 |
| Score | 2.5168798 |
| Snippet | Alzheimer disease (AD) results, in part, from the excess accumulation of the amyloid-β (Aβ) peptide as neuritic plaques in the brain. The short Aβ peptide is... |
| SourceID | proquest pubmed |
| SourceType | Aggregation Database Index Database |
| StartPage | 5184 |
| SubjectTerms | 3' Untranslated Regions - genetics Aged Aged, 80 and over Alzheimer Disease - enzymology Alzheimer Disease - genetics Alzheimer Disease - pathology Amyloid beta-Peptides - metabolism Amyloid Precursor Protein Secretases - genetics Argonaute Proteins - metabolism Aspartic Acid Endopeptidases - genetics Base Sequence Brain - pathology Cell Line, Tumor Cell Shape Cells, Cultured Computational Biology Conserved Sequence - genetics Demography Down-Regulation - genetics Female Gene Knockdown Techniques Humans Male MicroRNAs - genetics MicroRNAs - metabolism Molecular Sequence Data Protein Binding - genetics Reproducibility of Results Time Factors |
| Title | MicroRNA-339-5p down-regulates protein expression of β-site amyloid precursor protein-cleaving enzyme 1 (BACE1) in human primary brain cultures and is reduced in brain tissue specimens of Alzheimer disease subjects |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/24352696 https://www.proquest.com/docview/1501835227 |
| Volume | 289 |
| WOSCitedRecordID | wos000331607900060&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/eLvHCXMwpV3fa9UwFA7qBH3xx6Zz_uIIIvqQrWnSpn2Setnw5V6GKNy3S5qk7MpuOttN3P4s_xBf_Xc8J23ZkyAIpVA4bUJySL9zcvJ9jL12SYOxSSO4kTrhyijHa6K7K3yqa6GdSXIbxSb0YlEsl-XxmHDrx7LKaU2MC7VrLeXIDwQxzxFa0O_PvnFSjaLd1VFC4ybbkghlyKv18potHNGvGArsJVWsLydqH60OvtZ2fy6E3M8QYCvxd3wZ_zNH9_-3hw_YvRFhQjW4xEN2w4dttlMFjK43l_AGYs1nTKZvszuzSe9th_2eU23ep0XFpSx5dgYOA3TeDVr1vofI6LAO4H-MtbMB2gZ-_eTUPpgNRv5rh1aUwO_bbrLn2AlDWQvw4epy40HA2w_V7FC8A_xYlAhE00h5ATXpVcBABoItmuBg3UNH7LLekflgcB6dBeiQKGkT9NSP6vTqxONTB-OWE_QXNeWY-kfsy9Hh59lHPso-cKuUPOd5I2qvs7zQqfKZlTJ1ThS2dM4WxpUGI8jE5cZIi6tR4aTLbOZNWvuklilN52N2K7TBP2HgfOmLxmqd14nKM2tcVuCFIDbzhfLlHns1TeUKR5v2Skzw7UW_up7MPbY7-MNqHIxVqkhUoMyf_sPbz9hdhFgqHoIXz9lWg4uKf8Fu2-84Vt3L6K94XxzP_wBL8vob |
| 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=MicroRNA-339-5p+down-regulates+protein+expression+of+%CE%B2-site+amyloid+precursor+protein-cleaving+enzyme+1+%28BACE1%29+in+human+primary+brain+cultures+and+is+reduced+in+brain+tissue+specimens+of+Alzheimer+disease+subjects&rft.jtitle=The+Journal+of+biological+chemistry&rft.au=Long%2C+Justin+M&rft.au=Ray%2C+Balmiki&rft.au=Lahiri%2C+Debomoy+K&rft.date=2014-02-21&rft.issn=1083-351X&rft.eissn=1083-351X&rft.volume=289&rft.issue=8&rft.spage=5184&rft_id=info:doi/10.1074%2Fjbc.M113.518241&rft.externalDBID=NO_FULL_TEXT |
| thumbnail_l | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1083-351X&client=summon |
| thumbnail_m | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1083-351X&client=summon |
| thumbnail_s | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1083-351X&client=summon |