{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,16]],"date-time":"2026-10-16T03:17:09Z","timestamp":1792120629780,"version":"4.4.0"},"reference-count":126,"publisher":"MDPI AG","issue":"17","license":[{"start":{"date-parts":[[2020,8,23]],"date-time":"2020-08-23T00:00:00Z","timestamp":1598140800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>The endosomal recycling pathway lies at the heart of the membrane trafficking machinery in the cell. It plays a central role in determining the composition of the plasma membrane and is thus critical for normal cellular homeostasis. However, defective endosomal recycling has been linked to a wide range of diseases, including cancer and some of the most common neurological disorders. It is also frequently subverted by many diverse human pathogens in order to successfully infect cells. Despite its importance, endosomal recycling remains relatively understudied in comparison to the endocytic and secretory transport pathways. A greater understanding of the molecular mechanisms that support transport through the endosomal recycling pathway will provide deeper insights into the pathophysiology of disease and will likely identify new approaches for their detection and treatment. This review will provide an overview of the normal physiological role of the endosomal recycling pathway, describe the consequences when it malfunctions, and discuss potential strategies for modulating its activity.<\/jats:p>","DOI":"10.3390\/ijms21176074","type":"journal-article","created":{"date-parts":[[2020,8,23]],"date-time":"2020-08-23T21:28:06Z","timestamp":1598218086000},"page":"6074","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":136,"title":["The Endosomal Recycling Pathway\u2014At the Crossroads of the Cell"],"prefix":"10.3390","volume":"21","author":[{"given":"Mary J.","family":"O\u2019Sullivan","sequence":"first","affiliation":[{"name":"Membrane Trafficking and Disease Laboratory, School of Biochemistry &amp; Cell Biology, Biosciences Institute, University College Cork, T12 YT20 Cork, Ireland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9693-7022","authenticated-orcid":false,"given":"Andrew J.","family":"Lindsay","sequence":"additional","affiliation":[{"name":"Membrane Trafficking and Disease Laboratory, School of Biochemistry &amp; Cell Biology, Biosciences Institute, University College Cork, T12 YT20 Cork, Ireland"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2020,8,23]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1260419","DOI":"10.1126\/science.1260419","article-title":"Tissue-based map of the human proteome","volume":"347","author":"Uhlen","year":"2015","journal-title":"Science"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"597","DOI":"10.1038\/nrm2755","article-title":"Pathways and mechanisms of endocytic recycling","volume":"10","author":"Grant","year":"2009","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_3","first-page":"1","article-title":"Clathrin-independent pathways do not contribute significantly to endocytic flux","volume":"2014","author":"Bitsikas","year":"2014","journal-title":"Elife"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"196","DOI":"10.1007\/s10354-016-0432-7","article-title":"Endocytic pathways and endosomal trafficking: A primer","volume":"166","author":"Elkin","year":"2016","journal-title":"Wien. Med. Wochenschr."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"a016949","DOI":"10.1101\/cshperspect.a016949","article-title":"Endocytosis and cancer","volume":"5","author":"Mellman","year":"2013","journal-title":"Cold Spring Harb. Perspect. Biol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1529","DOI":"10.1007\/s00018-015-2105-x","article-title":"Endocytic membrane trafficking and neurodegenerative disease","volume":"73","author":"Schreij","year":"2016","journal-title":"Cell. Mol. Life Sci."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"505","DOI":"10.1093\/jb\/mvt034","article-title":"Emerging roles of recycling endosomes","volume":"153","author":"Taguchi","year":"2013","journal-title":"J. Biochem."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"513","DOI":"10.1038\/nrm2728","article-title":"Rab GTPases as coordinators of vesicle traffic","volume":"10","author":"Stenmark","year":"2009","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1080\/21541248.2016.1276999","article-title":"Molecular control of Rab activity by GEFs, GAPs and GDI","volume":"9","author":"Goody","year":"2018","journal-title":"Small GTPases"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1080\/21541248.2017.1336191","article-title":"Rab GTPases and their interacting protein partners: Structural insights into Rab functional diversity","volume":"9","author":"Pylypenko","year":"2018","journal-title":"Small GTPases"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"12190","DOI":"10.1074\/jbc.M108665200","article-title":"Rab coupling protein (RCP), a novel Rab4 and Rab11 effector protein","volume":"277","author":"Lindsay","year":"2002","journal-title":"J. Biol. Chem."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"27193","DOI":"10.1074\/jbc.M200757200","article-title":"Rab11-FIP2 functions in transferrin recycling and associates with endosomal membranes via its COOH-terminal domain","volume":"277","author":"Lindsay","year":"2002","journal-title":"J. Biol. Chem."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"39067","DOI":"10.1074\/jbc.M104831200","article-title":"Identification and Characterization of a Family of Rab11-interacting Proteins","volume":"276","author":"Hales","year":"2001","journal-title":"J. Biol. Chem."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1437","DOI":"10.1016\/S1097-2765(00)00140-4","article-title":"A Rab11\/Rip11 protein complex regulates apical membrane trafficking via recycling endosomes","volume":"6","author":"Prekeris","year":"2000","journal-title":"Mol. Cell"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1042\/BC20090068","article-title":"Class I Rab11-family interacting proteins are binding targets for the Rab14 GTPase","volume":"102","author":"Kelly","year":"2010","journal-title":"Biol. Cell"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"643","DOI":"10.1091\/mbc.e12-09-0659","article-title":"Rab11-family interacting proteins define spatially and temporally distinct regions within the dynamic Rab11a-dependent recycling system","volume":"24","author":"Baetz","year":"2013","journal-title":"Mol. Biol. Cell"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"R922","DOI":"10.1016\/j.cub.2018.06.042","article-title":"The exocyst complex","volume":"28","author":"Mei","year":"2018","journal-title":"Curr. Biol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"43027","DOI":"10.1074\/jbc.M402264200","article-title":"Sec15 is an effector for the Rab11 GTPase in mammalian cells","volume":"279","author":"Zhang","year":"2004","journal-title":"J. Biol. Chem."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"294","DOI":"10.1016\/j.chom.2013.08.001","article-title":"Cholera toxin disrupts barrier function by inhibiting exocyst-mediated trafficking of host proteins to intestinal cell junctions","volume":"14","author":"Guichard","year":"2013","journal-title":"Cell Host Microbe"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"854","DOI":"10.1038\/nature09446","article-title":"Anthrax toxins cooperatively inhibit endocytic recycling by the Rab11\/Sec15 exocyst","volume":"467","author":"Guichard","year":"2010","journal-title":"Nature"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"445","DOI":"10.1016\/j.celrep.2014.01.002","article-title":"Recycling endosome tubule morphogenesis from sorting endosomes requires the kinesin motor KIF13A","volume":"6","author":"Delevoye","year":"2014","journal-title":"Cell Rep."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"3824","DOI":"10.1242\/jcs.032441","article-title":"The Rip11\/Rab11-FIP5 and kinesin II complex regulates endocytic protein recycling","volume":"121","author":"Schonteich","year":"2008","journal-title":"J. Cell Sci."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"816","DOI":"10.4049\/jimmunol.1002161","article-title":"Kinesin 5B Is Necessary for Delivery of Membrane and Receptors during Fc\u03b3R-Mediated Phagocytosis","volume":"186","author":"Silver","year":"2011","journal-title":"J. Immunol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1843","DOI":"10.1091\/mbc.12.6.1843","article-title":"Myosin Vb is associated with plasma membrane recycling systems","volume":"12","author":"Lapierre","year":"2001","journal-title":"Mol. Biol. Cell"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"3420","DOI":"10.1091\/mbc.e13-05-0236","article-title":"Identification and characterization of multiple novel Rab-myosin Va interactions","volume":"24","author":"Lindsay","year":"2013","journal-title":"Mol. Biol. Cell"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"535","DOI":"10.1016\/j.cell.2008.09.057","article-title":"Myosin Vb Mobilizes Recycling Endosomes and AMPA Receptors for Postsynaptic Plasticity","volume":"135","author":"Wang","year":"2008","journal-title":"Cell"},{"key":"ref_27","first-page":"2820","article-title":"A specific subset of RabGTPases controls cell surface exposure of MT1-MMP, extracellular matrix degradation and three-dimensional invasion of macrophages","volume":"126","author":"Wiesner","year":"2013","journal-title":"J. Cell Sci."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1744","DOI":"10.1091\/mbc.e04-10-0867","article-title":"Rab11 in recycling endosomes regulates the sorting and basolateral transport of E-cadherin","volume":"16","author":"Lock","year":"2005","journal-title":"Mol. Biol. Cell"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"587","DOI":"10.1083\/jcb.201506112","article-title":"Cargo-selective apical exocytosis in epithelial cells is conducted by Myo5B, Slp4a, Vamp7, and Syntaxin 3","volume":"211","author":"Vogel","year":"2015","journal-title":"J. Cell Biol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"e201811014","DOI":"10.1083\/jcb.201811014","article-title":"GRAF2, WDR44, and MICAL1 mediate Rab8\/10\/11\u2013dependent export of E-cadherin, MMP14, and CFTR \u0394F508","volume":"219","author":"Vallis","year":"2020","journal-title":"J. Cell Biol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"318","DOI":"10.1111\/jnc.13691","article-title":"The clinical symptoms of Parkinson\u2019s disease","volume":"139","author":"Sveinbjornsdottir","year":"2016","journal-title":"J. Neurochem."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"6732","DOI":"10.1093\/hmg\/ddu391","article-title":"The small GTPase Rab11 co-localizes with \u03b1-synuclein in intracellular inclusions and modulates its aggregation, secretion and toxicity","volume":"23","author":"Chutna","year":"2014","journal-title":"Hum. Mol. Genet."},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Gon\u00e7alves, S.A., Macedo, D., Raquel, H., Sim\u00f5es, P.D., Giorgini, F., Ramalho, J.S., Barral, D.C., Moita, L.F., and Outeiro, T.F. (2016). shRNA-Based Screen Identifies Endocytic Recycling Pathway Components That Act as Genetic Modifiers of Alpha-Synuclein Aggregation, Secretion and Toxicity. PLoS Genet., 12.","DOI":"10.1371\/journal.pgen.1005995"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"314","DOI":"10.1111\/ane.12563","article-title":"The genetic background of Parkinson\u2019s disease: Current progress and future prospects","volume":"134","author":"Kalinderi","year":"2016","journal-title":"Acta Neurol. Scand."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41419-018-0410-7","article-title":"Alteration of endosomal trafficking is associated with early-onset parkinsonism caused by SYNJ1 mutations","volume":"9","author":"Fasano","year":"2018","journal-title":"Cell Death Dis."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"733","DOI":"10.1038\/ng.3589","article-title":"Identification of TMEM230 mutations in familial Parkinson\u2019s disease","volume":"48","author":"Deng","year":"2016","journal-title":"Nat. Genet."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1161","DOI":"10.12688\/f1000research.14506.1","article-title":"Current understanding of Alzheimer\u2019s disease diagnosis and treatment","volume":"7","author":"Weller","year":"2018","journal-title":"F1000Research"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1016\/S0002-9440(10)64538-5","article-title":"Endocytic pathway abnormalities precede amyloid \u03b2 deposition in sporadic alzheimer\u2019s disease and down syndrome: Differential effects of APOE genotype and presenilin mutations","volume":"157","author":"Cataldo","year":"2000","journal-title":"Am. J. Pathol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1263","DOI":"10.1093\/hmg\/8.7.1263","article-title":"Presenilins interact with Rab11, a small GTPase involved in the regulation of vesicular transport","volume":"8","author":"Dumanchin","year":"1999","journal-title":"Hum. Mol. Genet."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"997","DOI":"10.1111\/tra.12088","article-title":"Intracellular Itinerary of Internalised \u03b2-Secretase, BACE1, and Its Potential Impact on \u03b2-Amyloid Peptide Biogenesis","volume":"14","author":"Chia","year":"2013","journal-title":"Traffic"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/1750-1326-9-1","article-title":"Axonal BACE1 dynamics and targeting in hippocampal neurons: A role for Rab11 GTPase","volume":"9","author":"Fernandez","year":"2014","journal-title":"Mol. Neurodegener."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1536","DOI":"10.1016\/j.celrep.2013.12.005","article-title":"A Paired RNAi and RabGAP overexpression screen identifies Rab11 as a regulator of \u03b2-amyloid production","volume":"5","author":"Udayar","year":"2013","journal-title":"Cell Rep."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"759","DOI":"10.1016\/j.celrep.2016.09.034","article-title":"Defective Transcytosis of APP and Lipoproteins in Human iPSC-Derived Neurons with Familial Alzheimer\u2019s Disease Mutations","volume":"17","author":"Woodruff","year":"2016","journal-title":"Cell Rep."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"381","DOI":"10.1038\/s41586-020-2156-5","article-title":"LRP1 is a master regulator of tau uptake and spread","volume":"580","author":"Rauch","year":"2020","journal-title":"Nature"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"14308","DOI":"10.1074\/jbc.M109.046672","article-title":"Low density lipoprotein receptor-related protein 1 (LRP1) forms a signaling complex with platelet-derived growth factor receptor-\u03b2 in endosomes and regulates activation of the MAPK pathway","volume":"285","author":"Muratoglu","year":"2010","journal-title":"J. Biol. Chem."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"973","DOI":"10.1038\/ejhg.2017.87","article-title":"Characterization of pathogenic SORL1 genetic variants for association with Alzheimer\u2019s disease: A clinical interpretation strategy","volume":"25","author":"Holstege","year":"2017","journal-title":"Eur. J. Hum. Genet."},{"key":"ref_47","first-page":"1","article-title":"SORLA regulates endosomal trafficking and oncogenic fitness of HER2","volume":"10","author":"Sahgal","year":"2019","journal-title":"Nat. Commun."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"2061","DOI":"10.12688\/f1000research.20762.1","article-title":"Recent advances in understanding and managing malabsorption: Focus on microvillus inclusion disease","volume":"8","author":"Jayawardena","year":"2019","journal-title":"F1000Research"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"307","DOI":"10.1097\/MPG.0b013e3181eea177","article-title":"Functional characterization of mutations in the myosin Vb gene associated with microvillus inclusion disease","volume":"52","author":"Szperl","year":"2011","journal-title":"J. Pediatr. Gastroenterol. Nutr."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"2947","DOI":"10.1172\/JCI71651","article-title":"Myosin Vb uncoupling from RAB8A and RAB11A elicits microvillus inclusion disease","volume":"124","author":"Knowles","year":"2014","journal-title":"J. Clin. Investig."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"453","DOI":"10.1111\/tra.12486","article-title":"Abnormal Rab11-Rab8-vesicles cluster in enterocytes of patients with microvillus inclusion disease","volume":"18","author":"Vogel","year":"2017","journal-title":"Traffic"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1053\/j.gastro.2014.04.002","article-title":"Loss of syntaxin 3 causes variant microvillus inclusion disease","volume":"147","author":"Wiegerinck","year":"2014","journal-title":"Gastroenterology"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"333","DOI":"10.1002\/humu.23386","article-title":"MYO5B, STX3, and STXBP2 mutations reveal a common disease mechanism that unifies a subset of congenital diarrheal disorders: A mutation update","volume":"39","author":"Dhekne","year":"2018","journal-title":"Hum. Mutat."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"176","DOI":"10.3389\/fcell.2018.00176","article-title":"A comprehensive review on the interaction between the host GTPase Rab11 and influenza A virus","volume":"6","author":"Amorim","year":"2019","journal-title":"Front. Cell Dev. Biol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"8365","DOI":"10.1128\/JVI.00209-15","article-title":"Intracellular Transport of Vaccinia Virus in HeLa Cells Requires WASH-VPEF\/FAM21-Retromer Complexes and Recycling Molecules Rab11 and Rab22","volume":"89","author":"Hsiao","year":"2015","journal-title":"J. Virol."},{"key":"ref_56","doi-asserted-by":"crossref","unstructured":"Acosta, E.G., Castilla, V., and Damonte, E.B. (2012). Differential Requirements in Endocytic Trafficking for Penetration of Dengue Virus. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0044835"},{"key":"ref_57","doi-asserted-by":"crossref","unstructured":"Vale-Costa, S., and Amorim, M.J. (2016). Recycling endosomes and viral infection. Viruses, 8.","DOI":"10.3390\/v8030064"},{"key":"ref_58","first-page":"1","article-title":"Influenza virus genome reaches the plasma membrane via a modified endoplasmic reticulum and Rab11-dependent vesicles","volume":"8","author":"Fournier","year":"2017","journal-title":"Nat. Commun."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41467-019-09549-4","article-title":"Influenza A virus ribonucleoproteins form liquid organelles at endoplasmic reticulum exit sites","volume":"10","author":"Alenquer","year":"2019","journal-title":"Nat. Commun."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"S388","DOI":"10.1093\/infdis\/jiy460","article-title":"Budding of Ebola Virus Particles Requires the Rab11-Dependent Endocytic Recycling Pathway","volume":"218","author":"Nanbo","year":"2018","journal-title":"J. Infect. Dis."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"15143","DOI":"10.1073\/pnas.2434327100","article-title":"Apical recycling systems regulate directional budding of respiratory syncytial virus from polarized epithelial cells","volume":"100","author":"Brock","year":"2003","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"10209","DOI":"10.1073\/pnas.0712144105","article-title":"Respiratory syncytial virus uses a Vps4-independent budding mechanism controlled by Rab11-FIP2","volume":"105","author":"Utley","year":"2008","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"5848","DOI":"10.1128\/JVI.00307-10","article-title":"The Rab11 pathway is required for influenza A virus budding and filament formation","volume":"84","author":"Bruce","year":"2010","journal-title":"J. Virol."},{"key":"ref_64","doi-asserted-by":"crossref","unstructured":"Lim, Y., Ng, Y., Tam, J., and Liu, D. (2016). Human Coronaviruses: A Review of Virus\u2013Host Interactions. Diseases, 4.","DOI":"10.3390\/diseases4030026"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"365","DOI":"10.1080\/21541248.2016.1240494","article-title":"Diverted recycling\u2014Shigella subversion of Rabs","volume":"9","author":"Enninga","year":"2018","journal-title":"Small GTPases"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"e12857","DOI":"10.1111\/cmi.12857","article-title":"The recycling endosome and bacterial pathogens","volume":"20","author":"Allgood","year":"2018","journal-title":"Cell. Microbiol."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"96","DOI":"10.1016\/j.cbi.2016.10.005","article-title":"Inhibitors of retrograde trafficking active against ricin and Shiga toxins also protect cells from several viruses, Leishmania and Chlamydiales","volume":"267","author":"Gupta","year":"2017","journal-title":"Chem. Biol. Interact."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"1251","DOI":"10.1038\/nm1125","article-title":"The RAB25 small GTPase determines aggressiveness of ovarian and breast cancers","volume":"10","author":"Cheng","year":"2004","journal-title":"Nat. Med."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"64591","DOI":"10.18632\/oncotarget.19571","article-title":"Rab25 GTPase: Functional roles in cancer","volume":"8","author":"Wang","year":"2017","journal-title":"Oncotarget"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"496","DOI":"10.1016\/j.devcel.2007.08.012","article-title":"Rab25 Associates with \u03b15\u03b21 Integrin to Promote Invasive Migration in 3D Microenvironments","volume":"13","author":"Caswell","year":"2007","journal-title":"Dev. Cell"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1038\/sj.bjc.6605983","article-title":"Rab25 as a tumour suppressor in colon carcinogenesis","volume":"104","author":"Goldenring","year":"2011","journal-title":"Br. J. Cancer"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"1927","DOI":"10.3892\/ol.2015.3433","article-title":"Downregulation of Rab25 activates Akt1 in head and neck squamous cell carcinoma","volume":"10","author":"Seven","year":"2015","journal-title":"Oncol. Lett."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"2799","DOI":"10.1002\/ijc.24900","article-title":"Tumor suppressor function of Rab25 in triple-negative breast cancer","volume":"126","author":"Cheng","year":"2010","journal-title":"Int. J. Cancer"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"653","DOI":"10.1080\/15592294.2016.1205176","article-title":"RAB25 expression is epigenetically downregulated in oral and oropharyngeal squamous cell carcinoma with lymph node metastasis","volume":"11","author":"Clausen","year":"2016","journal-title":"Epigenetics"},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41598-017-14314-y","article-title":"Promoter DNA methylation analysis reveals a novel diagnostic CpG-based biomarker and RAB25 hypermethylation in clear cell renel cell carcinoma","volume":"7","author":"Gu","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"4099","DOI":"10.1158\/0008-5472.CAN-18-4075","article-title":"Recycling endosomes in mature epithelia restrain tumorigenic signaling","volume":"79","author":"Nie","year":"2019","journal-title":"Cancer Res."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"27800","DOI":"10.18632\/oncotarget.15359","article-title":"Rab11a promotes proliferation and invasion through regulation of YAP in non-small cell lung cancer","volume":"8","author":"Dong","year":"2017","journal-title":"Oncotarget"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"5093","DOI":"10.12659\/MSM.911454","article-title":"Rab11 functions as an oncoprotein via nuclear factor kappa B (NF-\u03baB) signaling pathway in human bladder carcinoma","volume":"24","author":"Gong","year":"2018","journal-title":"Med. Sci. Monit."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"13821","DOI":"10.1007\/s13277-016-5172-1","article-title":"Rab11a sustains GSK3\u03b2\/Wnt\/\u03b2-catenin signaling to enhance cancer progression in pancreatic cancer","volume":"37","author":"Yu","year":"2016","journal-title":"Tumor Biol."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41467-020-16832-2","article-title":"Rab11b-mediated integrin recycling promotes brain metastatic adaptation and outgrowth","volume":"11","author":"Howe","year":"2020","journal-title":"Nat. Commun."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1007\/s12272-019-01129-w","article-title":"Rab25 and RCP in cancer progression","volume":"42","author":"Cho","year":"2019","journal-title":"Arch. Pharm. Res."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"1010428317691010","DOI":"10.1177\/1010428317691010","article-title":"Increased Eps15 homology domain 1 and RAB11FIP3 expression regulate breast cancer progression via promoting epithelial growth factor receptor recycling","volume":"39","author":"Tong","year":"2017","journal-title":"Tumor Biol."},{"key":"ref_83","first-page":"3797","article-title":"Hypoxia-induced Rab11-family interacting protein 4 expression promotes migration and invasion of colon cancer and correlates with poor prognosis","volume":"17","author":"Wang","year":"2018","journal-title":"Mol. Med. Rep."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"14646","DOI":"10.1038\/ncomms14646","article-title":"Phosphorylation of Rab-coupling protein by LMTK3 controls Rab14-dependent EphA2 trafficking to promote cell:cell repulsion","volume":"8","author":"Gundry","year":"2017","journal-title":"Nat. Commun."},{"key":"ref_85","first-page":"1","article-title":"The role of the oncogenic Rab35 in cancer invasion, metastasis, and immune evasion, especially in leukemia","volume":"11","author":"Villagomez","year":"2018","journal-title":"Small GTPases"},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"3698","DOI":"10.1038\/s41388-018-0202-7","article-title":"Rab34 regulates adhesion, migration, and invasion of breast cancer cells","volume":"37","author":"Sun","year":"2018","journal-title":"Oncogene"},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"205","DOI":"10.4161\/cam.27841","article-title":"p53 in cell invasion, podosomes, and invadopodia","volume":"8","author":"Mak","year":"2014","journal-title":"Cell Adhes. Migr."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"a001107","DOI":"10.1101\/cshperspect.a001107","article-title":"Mutant p53 gain-of-function in cancer","volume":"2","author":"Oren","year":"2010","journal-title":"Cold Spring Harb. Perspect. Biol."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"122","DOI":"10.1038\/s41556-018-0223-z","article-title":"Integrin trafficking in cells and tissues","volume":"21","author":"Icha","year":"2019","journal-title":"Nat. Cell Biol."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1083\/jcb.200804140","article-title":"Rab-coupling protein coordinates recycling of \u03b15\u03b21 integrin and EGFR1 to promote cell migration in 3D microenvironments","volume":"183","author":"Caswell","year":"2008","journal-title":"J. Cell Biol."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"1327","DOI":"10.1016\/j.cell.2009.11.026","article-title":"Mutant p53 Drives Invasion by Promoting Integrin Recycling","volume":"139","author":"Muller","year":"2009","journal-title":"Cell"},{"key":"ref_92","doi-asserted-by":"crossref","unstructured":"Pavlakis, E., and Stiewe, T. (2020). p53\u2019s Extended Reach: The Mutant p53 Secretome. Biomolecules, 10.","DOI":"10.3390\/biom10020307"},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41467-018-07339-y","article-title":"Mutant p53s generate pro-invasive niches by influencing exosome podocalyxin levels","volume":"9","author":"Novo","year":"2018","journal-title":"Nat. Commun."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"107879","DOI":"10.1016\/j.celrep.2020.107879","article-title":"Mutant p53 Drives Cancer Metastasis via RCP-Mediated Hsp90\u03b1 Secretion","volume":"32","author":"Zhang","year":"2020","journal-title":"Cell Rep."},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1016\/j.ceb.2007.02.010","article-title":"Receptor tyrosine kinases: Mechanisms of activation and signaling","volume":"19","author":"Hubbard","year":"2007","journal-title":"Curr. Opin. Cell Biol."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s12943-018-0782-4","article-title":"Mechanisms of receptor tyrosine kinase activation in cancer","volume":"17","author":"Du","year":"2018","journal-title":"Mol. Cancer"},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"a009035","DOI":"10.1101\/cshperspect.a009035","article-title":"Effects of membrane trafficking on signaling by receptor tyrosine kinases","volume":"5","author":"Miaczynska","year":"2013","journal-title":"Cold Spring Harb. Perspect. Biol."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s12943-017-0753-1","article-title":"Function of the c-Met receptor tyrosine kinase in carcinogenesis and associated therapeutic opportunities","volume":"17","author":"Zhang","year":"2018","journal-title":"Mol. Cancer"},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"678","DOI":"10.1002\/ijc.20598","article-title":"c-Met overexpression in node-positive breast cancer identifies patients with poor clinical outcome independent of Her2\/neu","volume":"113","author":"Lengyel","year":"2005","journal-title":"Int. J. Cancer"},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"830","DOI":"10.1016\/j.humpath.2006.11.015","article-title":"Poor prognosis in breast carcinomas correlates with increased expression of targetable CD146 and c-Met and with proteomic basal-like phenotype","volume":"38","author":"Garcia","year":"2007","journal-title":"Hum. Pathol."},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"827","DOI":"10.1038\/ncb2257","article-title":"A direct role for Met endocytosis in tumorigenesis","volume":"13","author":"Joffre","year":"2011","journal-title":"Nat. Cell Biol."},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"1566","DOI":"10.1007\/s00018-008-7440-8","article-title":"The epidermal growth factor receptor family: Biology driving targeted therapeutics","volume":"65","author":"Wieduwilt","year":"2008","journal-title":"Cell. Mol. Life Sci."},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1016\/j.tcb.2013.11.002","article-title":"EGF receptor trafficking: Consequences for signaling and cancer","volume":"24","author":"Tomas","year":"2014","journal-title":"Trends Cell Biol."},{"key":"ref_104","doi-asserted-by":"crossref","first-page":"609","DOI":"10.1038\/nrm2748","article-title":"Endocytosis and signalling: Intertwining molecular networks","volume":"10","author":"Sorkin","year":"2009","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_105","doi-asserted-by":"crossref","unstructured":"Chung, B.M., Raja, S.M., Clubb, R.J., Tu, C., George, M., Band, V., and Band, H. (2009). Aberrant trafficking of NSCLC-associated EGFR mutants through the endocytic recycling pathway promotes interaction with Src. BMC Cell Biol., 10.","DOI":"10.1186\/1471-2121-10-84"},{"key":"ref_106","doi-asserted-by":"crossref","first-page":"608","DOI":"10.1038\/nsmb.3218","article-title":"Multilayered proteomics reveals molecular switches dictating ligand-dependent EGFR trafficking","volume":"23","author":"Francavilla","year":"2016","journal-title":"Nat. Struct. Mol. Biol."},{"key":"ref_107","doi-asserted-by":"crossref","first-page":"424","DOI":"10.3390\/membranes4030424","article-title":"The mysterious ways of ErbB2\/HER2 trafficking","volume":"4","author":"Bertelsen","year":"2014","journal-title":"Membranes"},{"key":"ref_108","doi-asserted-by":"crossref","first-page":"1767","DOI":"10.1056\/NEJMra1514296","article-title":"Molecular and biochemical aspects of the PD-1 checkpoint pathway","volume":"375","author":"Boussiotis","year":"2016","journal-title":"N. Engl. J. Med."},{"key":"ref_109","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1016\/j.cellimm.2016.09.009","article-title":"PD-1\/PD-L and autoimmunity: A growing relationship","volume":"310","author":"Zamani","year":"2016","journal-title":"Cell. Immunol."},{"key":"ref_110","doi-asserted-by":"crossref","unstructured":"Vaddepally, R.K., Kharel, P., Pandey, R., Garje, R., and Chandra, A.B. (2020). Review of indications of FDA-approved immune checkpoint inhibitors per NCCN guidelines with the level of evidence. Cancers, 12.","DOI":"10.3390\/cancers12030738"},{"key":"ref_111","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1038\/nature23643","article-title":"CMTM6 maintains the expression of PD-L1 and regulates anti-Tumour immunity","volume":"549","author":"Burr","year":"2017","journal-title":"Nature"},{"key":"ref_112","doi-asserted-by":"crossref","first-page":"106","DOI":"10.1038\/nature23669","article-title":"Identification of CMTM6 and CMTM4 as PD-L1 protein regulators","volume":"549","author":"Mezzadra","year":"2017","journal-title":"Nature"},{"key":"ref_113","first-page":"218","article-title":"Plinabulin, an inhibitor of tubulin polymerization, targets KRAS signaling through disruption of endosomal recycling","volume":"10","author":"Cimino","year":"2019","journal-title":"Biomed. Rep."},{"key":"ref_114","doi-asserted-by":"crossref","first-page":"683","DOI":"10.1124\/mol.114.096602","article-title":"Mis-trafficking of endosomal urokinase proteins triggers drug-induced glioma nonapoptotic cell death","volume":"87","author":"Pasupuleti","year":"2015","journal-title":"Mol. Pharmacol."},{"key":"ref_115","doi-asserted-by":"crossref","first-page":"937","DOI":"10.1016\/j.ejmech.2008.08.011","article-title":"Primaquine revisited six decades after its discovery","volume":"44","author":"Vale","year":"2009","journal-title":"Eur. J. Med. Chem."},{"key":"ref_116","doi-asserted-by":"crossref","first-page":"394","DOI":"10.1078\/0171-9335-00062","article-title":"Primaquine interferes with membrane recycling from endosomes to the plasma membrane through a direct interaction with endosomes which does not involve neutralisation of endosomal pH nor osmotic swelling of endosomes","volume":"79","author":"Geuze","year":"2000","journal-title":"Eur. J. Cell Biol."},{"key":"ref_117","doi-asserted-by":"crossref","first-page":"6914","DOI":"10.1016\/j.bmcl.2009.10.081","article-title":"Anti-tumoral activity of imidazoquines, a new class of antimalarials derived from primaquine","volume":"19","author":"Fernandes","year":"2009","journal-title":"Bioorganic Med. Chem. Lett."},{"key":"ref_118","doi-asserted-by":"crossref","first-page":"655","DOI":"10.1016\/j.bbrc.2013.10.095","article-title":"Co-treatment with the anti-malarial drugs mefloquine and primaquine highly sensitizes drug-resistant cancer cells by increasing P-gp inhibition","volume":"441","author":"Kim","year":"2013","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_119","doi-asserted-by":"crossref","first-page":"1641","DOI":"10.21873\/anticanres.11171","article-title":"Anti-malarial drugs primaquine and chloroquine have different sensitization effects with anti-mitotic drugs in resistant cancer cells","volume":"36","author":"Choi","year":"2016","journal-title":"Anticancer Res."},{"key":"ref_120","doi-asserted-by":"crossref","first-page":"1139","DOI":"10.1016\/j.drudis.2017.03.012","article-title":"Targeting Rabs as a novel therapeutic strategy for cancer therapy","volume":"22","author":"Qin","year":"2017","journal-title":"Drug Discov. Today"},{"key":"ref_121","doi-asserted-by":"crossref","first-page":"589","DOI":"10.1038\/leu.2011.282","article-title":"Bisphosphonates as antimyeloma drugs","volume":"26","author":"Modi","year":"2012","journal-title":"Leukemia"},{"key":"ref_122","doi-asserted-by":"crossref","first-page":"2498","DOI":"10.1002\/anie.201308568","article-title":"Direct Targeting of Rab-GTPase-Effector Interactions","volume":"53","author":"Spiegel","year":"2014","journal-title":"Angew. Chem. Int. Ed."},{"key":"ref_123","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41467-017-00888-8","article-title":"Stapled peptide inhibitors of RAB25 target context-specific phenotypes in cancer","volume":"8","author":"Mitra","year":"2017","journal-title":"Nat. Commun."},{"key":"ref_124","doi-asserted-by":"crossref","first-page":"1400","DOI":"10.3892\/mmr.2014.2880","article-title":"MicroRNA-338-3p functions as a tumor suppressor in human nonsmallcell lung carcinoma and targets Ras-related protein 14","volume":"11","author":"Sun","year":"2015","journal-title":"Mol. Med. Rep."},{"key":"ref_125","doi-asserted-by":"crossref","first-page":"101665","DOI":"10.1016\/j.pneurobio.2019.101665","article-title":"Targeting the transferrin receptor for brain drug delivery","volume":"181","author":"Johnsen","year":"2019","journal-title":"Prog. Neurobiol."},{"key":"ref_126","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1023\/A:1026246500788","article-title":"Transferrin receptor ligand-targeted toxin conjugate (Tf-CRM107) therapy of malignant gliomas","volume":"65","author":"Weaver","year":"2003","journal-title":"J. Neurooncol."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/21\/17\/6074\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T10:05:30Z","timestamp":1760177130000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/21\/17\/6074"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,8,23]]},"references-count":126,"journal-issue":{"issue":"17","published-online":{"date-parts":[[2020,9]]}},"alternative-id":["ijms21176074"],"URL":"https:\/\/doi.org\/10.3390\/ijms21176074","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,8,23]]}}}