{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,25]],"date-time":"2026-09-25T23:20:51Z","timestamp":1790378451230,"version":"4.1.0"},"reference-count":60,"publisher":"American Chemical Society (ACS)","issue":"1","license":[{"start":{"date-parts":[[2015,12,30]],"date-time":"2015-12-30T00:00:00Z","timestamp":1451433600000},"content-version":"vor","delay-in-days":365,"URL":"https:\/\/pubs.acs.org\/page\/policy\/authorchoice_termsofuse.html"}],"funder":[{"DOI":"10.13039\/100000049","name":"National Institute on Aging","doi-asserted-by":"publisher","award":["NA"],"award-info":[{"award-number":["NA"]}],"id":[{"id":"10.13039\/100000049","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000078","name":"Division of Materials Research","doi-asserted-by":"publisher","award":["DMR 1255281"],"award-info":[{"award-number":["DMR 1255281"]}],"id":[{"id":"10.13039\/100000078","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2015,1,21]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Mitochondria are critical regulators of cellular function and survival. Delivery of therapeutic and diagnostic agents into mitochondria is a challenging task in modern pharmacology because the molecule to be delivered needs to first overcome the cell membrane barrier and then be able to actively target the intracellular organelle. Current strategy of conjugating either a cell penetrating peptide (CPP) or a subcellular targeting sequence to the molecule of interest only has limited success. We report here a dual peptide conjugation strategy to achieve effective delivery of a non-membrane-penetrating dye 5-carboxyfluorescein (5-FAM) into mitochondria through the incorporation of both a mitochondrial targeting sequence (MTS) and a CPP into one conjugated molecule. Notably, circular dichroism studies reveal that the combined use of \u03b1-helix and PPII-like secondary structures has an unexpected, synergistic contribution to the internalization of the conjugate. Our results suggest that although the use of positively charged MTS peptide allows for improved targeting of mitochondria, with MTS alone it showed poor cellular uptake. With further covalent linkage of the MTS-5-FAM conjugate to a CPP sequence (R8), the dually conjugated molecule was found to show both improved cellular uptake and effective mitochondria targeting. We believe these results offer important insight into the rational design of peptide conjugates for intracellular delivery.<\/jats:p>","DOI":"10.1021\/bc500408p","type":"journal-article","created":{"date-parts":[[2014,12,30]],"date-time":"2014-12-30T07:03:18Z","timestamp":1419922998000},"page":"71-77","source":"Crossref","is-referenced-by-count":87,"title":["Dual Peptide Conjugation Strategy for Improved Cellular\nUptake and Mitochondria Targeting"],"prefix":"10.1021","volume":"26","author":[{"given":"Ran","family":"Lin","sequence":"first","affiliation":[{"name":"The Johns Hopkins University , , , , ,","place":["Baltimore, Maryland, United States, 21218"]},{"name":"The Johns Hopkins University , , , , ,","place":["Baltimore, Maryland, United States, 21218"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pengcheng","family":"Zhang","sequence":"additional","affiliation":[{"name":"The Johns Hopkins University , , , , ,","place":["Baltimore, Maryland, United States, 21218"]},{"name":"The Johns Hopkins University , , , , ,","place":["Baltimore, Maryland, United States, 21218"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andrew. G.","family":"Cheetham","sequence":"additional","affiliation":[{"name":"The Johns Hopkins University , , , , ,","place":["Baltimore, Maryland, United States, 21218"]},{"name":"The Johns Hopkins University , , , , ,","place":["Baltimore, Maryland, United States, 21218"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jeremy","family":"Walston","sequence":"additional","affiliation":[{"name":"The Johns Hopkins University , , , , ,","place":["Baltimore, Maryland, United States, 21218"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peter","family":"Abadir","sequence":"additional","affiliation":[{"name":"The Johns Hopkins University , , , , ,","place":["Baltimore, Maryland, United States, 21218"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Honggang","family":"Cui","sequence":"additional","affiliation":[{"name":"The Johns Hopkins University , , , , ,","place":["Baltimore, Maryland, United States, 21218"]},{"name":"The Johns Hopkins University , , , , ,","place":["Baltimore, Maryland, United States, 21218"]},{"name":"The Johns Hopkins University , , , , ,","place":["Baltimore, Maryland, United States, 21218"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"316","published-online":{"date-parts":[[2014,12,30]]},"reference":[{"key":"2026090301352803200_cit1","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1152\/physrev.00013.2006","article-title":"Mitochondrial\nmembrane permeabilization\nin cell death","volume":"87","author":"Kroemer","year":"2007","journal-title":"Physiol. Rev."},{"key":"2026090301352803200_cit2","doi-asserted-by":"crossref","first-page":"787","DOI":"10.1038\/nature05292","article-title":"Mitochondrial dysfunction and oxidative\nstress in neurodegenerative\ndiseases","volume":"443","author":"Lin","year":"2006","journal-title":"Nature"},{"key":"2026090301352803200_cit3","doi-asserted-by":"crossref","first-page":"447","DOI":"10.1038\/nrd3137","article-title":"Targeting mitochondria for cancer\ntherapy","volume":"9","author":"Fulda","year":"2010","journal-title":"Nat. Rev. Drug Discovery"},{"key":"2026090301352803200_cit4","doi-asserted-by":"crossref","first-page":"14849","DOI":"10.1073\/pnas.1101507108","article-title":"Identification and characterization\nof a functional\nmitochondrial angiotensin system","volume":"108","author":"Abadir","year":"2011","journal-title":"Proc. Natl.\nAcad. Sci. U.S.A."},{"key":"2026090301352803200_cit5","doi-asserted-by":"crossref","first-page":"1852","DOI":"10.1093\/nar\/29.9.1852","article-title":"Targeting peptide\nnucleic acid (PNA) oligomers to mitochondria within cells by conjugation\nto lipophilic cations: implications for mitochondrial DNA replication,\nexpression and disease","volume":"29","author":"Muratovska","year":"2001","journal-title":"Nucleic Acids Res."},{"key":"2026090301352803200_cit6","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1016\/0092-8674(95)90457-3","article-title":"Mitochondrial\nprotein import - reversible\nbinding of the presequence at the trans side of the outer-membrane\ndrives partial translocation and unfolding","volume":"80","author":"Mayer","year":"1995","journal-title":"Cell"},{"key":"2026090301352803200_cit7","doi-asserted-by":"crossref","first-page":"31763","DOI":"10.1074\/jbc.271.50.31763","article-title":"The protein\nimport system of mitochondria","volume":"271","author":"Schatz","year":"1996","journal-title":"J. Biol. Chem."},{"key":"2026090301352803200_cit8","doi-asserted-by":"crossref","first-page":"290","DOI":"10.1016\/S0962-8924(00)01771-2","article-title":"Protein\ntransduction: unrestricted\ndelivery into all cells?","volume":"10","author":"Schwarze","year":"2000","journal-title":"Trends Cell Biol."},{"key":"2026090301352803200_cit9","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S0378-5173(02)00337-X","article-title":"Arginine-rich\npeptides: potential for intracellular delivery of macromolecules and\nthe mystery of the translocation mechanisms","volume":"245","author":"Futaki","year":"2002","journal-title":"Int. J. Pharm."},{"key":"2026090301352803200_cit10","doi-asserted-by":"crossref","first-page":"401","DOI":"10.1016\/S0168-3659(01)00392-3","article-title":"DQAsome\/DNA complexes release DNA\nupon contact with isolated mouse liver mitochondria","volume":"75","author":"Weissig","year":"2001","journal-title":"J. Controlled Release"},{"key":"2026090301352803200_cit11","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1016\/j.mito.2006.12.003","article-title":"Mitochondrial\ndrug delivery and mitochondrial disease therapy - An approach to liposome-based\ndelivery targeted to mitochondria","volume":"7","author":"Yamada","year":"2007","journal-title":"Mitochondrion"},{"key":"2026090301352803200_cit12","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1021\/cb400821p","article-title":"Molecular\nvehicles for mitochondrial chemical biology\nand drug delivery","volume":"9","author":"Jean","year":"2014","journal-title":"ACS Chem. Biol."},{"key":"2026090301352803200_cit13","doi-asserted-by":"crossref","first-page":"2808","DOI":"10.1007\/s11095-011-0530-6","article-title":"Development\nof Novel Peptides for\nMitochondrial Drug Delivery: Amino Acids Featuring Delocalized Lipophilic\nCations","volume":"28","author":"Kelley","year":"2011","journal-title":"Pharm. 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Eng."},{"key":"2026090301352803200_cit21","doi-asserted-by":"crossref","first-page":"2081","DOI":"10.1002\/cbic.200900017","article-title":"Mitochondria-penetrating\npeptides: sequence effects and model cargo transport","volume":"10","author":"Yousif","year":"2009","journal-title":"ChemBioChem"},{"key":"2026090301352803200_cit22","doi-asserted-by":"crossref","first-page":"1335","DOI":"10.1002\/j.1460-2075.1986.tb04364.x","article-title":"Mitochondrial\ntargeting sequences may form amphiphilic helices","volume":"5","author":"Vonheijne","year":"1986","journal-title":"EMBO J."},{"key":"2026090301352803200_cit23","doi-asserted-by":"crossref","first-page":"9872","DOI":"10.1021\/bi00494a017","article-title":"2D NMR\nand structural model for a mitochondrial signal peptide bound to a\nmicelle","volume":"29","author":"Karslake","year":"1990","journal-title":"Biochemistry"},{"key":"2026090301352803200_cit24","doi-asserted-by":"crossref","first-page":"14298","DOI":"10.1016\/S0021-9258(18)77300-6","article-title":"Import of chemically synthesized\nsignal peptides into\nrat-liver mitochondria","volume":"265","author":"Pak","year":"1990","journal-title":"J. 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Chem."},{"key":"2026090301352803200_cit28","doi-asserted-by":"crossref","first-page":"1189","DOI":"10.1016\/0092-8674(88)90263-2","article-title":"Cellular uptake\nof the tat protein from human immunodeficiency\nvirus","volume":"55","author":"Frankel","year":"1988","journal-title":"Cell"},{"key":"2026090301352803200_cit29","doi-asserted-by":"crossref","first-page":"5965","DOI":"10.1021\/nn401667z","article-title":"Self-assembled Tat\nnanofibers as effective drug carrier and transporter","volume":"7","author":"Zhang","year":"2013","journal-title":"ACS Nano"},{"key":"2026090301352803200_cit30","doi-asserted-by":"crossref","first-page":"604","DOI":"10.1021\/bc300585h","article-title":"Cellular uptake\nand cytotoxicity of drug-peptide conjugates regulated by conjugation\nsite","volume":"24","author":"Zhang","year":"2013","journal-title":"Bioconjugate Chem."},{"key":"2026090301352803200_cit31","doi-asserted-by":"crossref","first-page":"964","DOI":"10.1021\/mp400619v","article-title":"Enhanced\ncellular\nentry and efficacy of Tat conjugates by rational design of the auxiliary\nsegment","volume":"11","author":"Zhang","year":"2014","journal-title":"Mol. Pharmaceutics"},{"key":"2026090301352803200_cit32","doi-asserted-by":"crossref","first-page":"1880","DOI":"10.1021\/bc800160b","article-title":"Shape effects\nof nanoparticles conjugated with cell-penetrating peptides (HIV Tat\nPTD) on CHO cell uptake","volume":"19","author":"Zhang","year":"2008","journal-title":"Bioconjugate Chem."},{"key":"2026090301352803200_cit33","doi-asserted-by":"crossref","first-page":"84","DOI":"10.1016\/S0962-8924(98)80017-2","article-title":"Trojan peptides: the penetratin system\nfor intracellular delivery","volume":"8","author":"Derossi","year":"1998","journal-title":"Trends Cell Biol."},{"key":"2026090301352803200_cit34","doi-asserted-by":"crossref","first-page":"318","DOI":"10.1034\/j.1399-3011.2000.00723.x","article-title":"Polyarginine\nenters cells more efficiently than other polycationic homopolymers","volume":"56","author":"Mitchell","year":"2000","journal-title":"J. Pept. 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Med."},{"key":"2026090301352803200_cit39","doi-asserted-by":"crossref","first-page":"1179","DOI":"10.1016\/0092-8674(88)90262-0","article-title":"Autonomous functional domains of chemically synthesized\nhuman immunodeficiency virus Tat trans-activator protein","volume":"55","author":"Green","year":"1988","journal-title":"Cell"},{"key":"2026090301352803200_cit40","doi-asserted-by":"crossref","first-page":"5836","DOI":"10.1074\/jbc.M007540200","article-title":"Arginine-rich\npeptides - An abundant\nsource of membrane-permeable peptides having potential as carriers\nfor intracellular protein delivery","volume":"276","author":"Futaki","year":"2001","journal-title":"J. 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Evidence that nonspecific electrostatic interactions\nmediate effective binding of VSV to cells","volume":"133","author":"Bailey","year":"1984","journal-title":"Virology"},{"key":"2026090301352803200_cit48","doi-asserted-by":"crossref","first-page":"9246","DOI":"10.1016\/j.biomaterials.2012.09.027","article-title":"Dual-functional liposomes\nbased on pH-responsive cell-penetrating peptide and hyaluronic acid\nfor tumor-targeted anticancer drug delivery","volume":"33","author":"Jiang","year":"2012","journal-title":"Biomaterials"},{"key":"2026090301352803200_cit49","doi-asserted-by":"crossref","first-page":"819","DOI":"10.1016\/j.chembiol.2012.05.022","article-title":"Arginine topology\ncontrols escape of minimally cationic\nproteins from early endosomes to the cytoplasm","volume":"19","author":"Appelbaum","year":"2012","journal-title":"Chem. 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Biophys.\nActa, Biomembr."},{"key":"2026090301352803200_cit52","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1016\/S0005-2736(02)00373-5","article-title":"Conformational states of the cell-penetrating\npeptide penetratin when interacting with phospholipid vesicles: effects\nof surface charge and peptide concentration","volume":"1563","author":"Magzoub","year":"2002","journal-title":"Biochim. Biophys. Acta, Biomembr."},{"key":"2026090301352803200_cit53","doi-asserted-by":"crossref","first-page":"1119","DOI":"10.1016\/j.bbamem.2010.03.005","article-title":"Secondary\nstructure of cell-penetrating peptides controls membrane interaction\nand insertion","volume":"1798","author":"Eiriksdottir","year":"2010","journal-title":"Biochim. Biophys. Acta, Biomembr."},{"key":"2026090301352803200_cit54","doi-asserted-by":"crossref","first-page":"8245","DOI":"10.1073\/pnas.150518097","article-title":"Structure-activity\nanalysis of buforin II, a histone H2A-derived antimicrobial peptide:\nThe proline hinge is responsible for the cell-penetrating ability\nof buforin II","volume":"97","author":"Park","year":"2000","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"2026090301352803200_cit55","doi-asserted-by":"crossref","first-page":"848","DOI":"10.1111\/j.1600-0854.2007.00572.x","article-title":"A comprehensive\nmodel for the cellular uptake of cationic cell-penetrating peptides","volume":"8","author":"Duchardt","year":"2007","journal-title":"Traffic"},{"key":"2026090301352803200_cit56","doi-asserted-by":"crossref","first-page":"723","DOI":"10.1146\/annurev.biochem.76.052705.163409","article-title":"Translocation of proteins into mitochondria","volume":"76","author":"Neupert","year":"2007","journal-title":"Annu. Rev. 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U.S.A."},{"key":"2026090301352803200_cit58","doi-asserted-by":"crossref","first-page":"2559","DOI":"10.1021\/nl801908y","article-title":"Organelle-targeted\nnanocarriers: Specific delivery\nof liposomal ceramide to mitochondria enhances its cytotoxicity in\nvitro and in vivo","volume":"8","author":"Boddapati","year":"2008","journal-title":"Nano Lett."},{"key":"2026090301352803200_cit59","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1016\/j.devcel.2013.03.006","article-title":"A small molecule\ninhibitor of redox-regulated\nprotein translocation into mitochondria","volume":"25","author":"Dabir","year":"2013","journal-title":"Dev.\nCell"},{"key":"2026090301352803200_cit60","doi-asserted-by":"crossref","first-page":"377","DOI":"10.1007\/s00109-004-0629-x","article-title":"Differences\nin subcellular distribution and toxicity\nof green and red emitting CdTe quantum dots","volume":"83","author":"Lovric","year":"2005","journal-title":"J. Mol. 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