#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Leucine zipper transcription factor-like 1 binds adaptor protein complex-1 and 2 and participates in trafficking of transferrin receptor 1


Autoři: Kanyarat Promchan aff001;  Ven Natarajan aff001
Působiště autorů: Laboratory of Molecular Cell Biology, Leidos Biomedical Research, Inc., Frederick National Laboratory for Cancer Research, Frederick, MD, United States of America aff001
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0226298

Souhrn

LZTFL1 participates in immune synapse formation, ciliogenesis, and the localization of ciliary proteins, and knockout of LZTFL1 induces abnormal distribution of heterotetrameric adaptor protein complex-1 (AP-1) in the Lztfl1-knockout mouse photoreceptor cells, suggesting that LZTFL1 is involved in intracellular transport. Here, we demonstrate that in vitro LZTFL1 directly binds to AP-1 and AP-2 and coimmunoprecipitates AP-1 and AP-2 from cell lysates. DxxFxxLxxxR motif of LZTFL1 is essential for these bindings, suggesting LZTFL1 has roles in AP-1 and AP-2-mediated protein trafficking. Since AP-1 and AP-2 are known to be involved in transferrin receptor 1 (TfR1) trafficking, the effect of LZTFL1 on TfR1 recycling was analyzed. TfR1, AP-1 and LZTFL1 from cell lysates could be coimmunoprecipitated. However, pull-down results indicate there is no direct interaction between TfR1 and LZTFL1, suggesting that LZTFL1 interaction with TfR1 is indirect through AP-1. We report the colocalization of LZTFL1 and AP-1, AP-1 and TfR1 as well as LZTFL1 and TfR1 in the perinuclear region (PNR) and the cytoplasm, suggesting a potential complex between LZTFL1, AP-1 and TfR1. The results from the disruption of adaptin recruitment with brefeldin A treatment suggested ADP-ribosylation factor-dependent localization of LZFL1 and AP-1 in the PNR. Knockdown of AP-1 reduces the level of LZTFL1 in the PNR, suggesting that AP-1 plays a role in LZTFL1 trafficking. Knockout of LZTFL1 reduces the cell surface level and the rate of internalization of TfR1, leading to a decrease of transferrin uptake, efflux, and internalization. However, knockout of LZTFL1 did not affect the cell surface levels of epidermal growth factor receptor and cation-independent mannose 6-phosphate receptor, indicating that LZTFL1 specifically regulates the cell surface level of TfR1. These data support a novel role of LZTFL1 in regulating the cell surface TfR1 level by interacting with AP-1 and AP-2.

Klíčová slova:

Small interfering RNAs – Sequence motif analysis – Cell membranes – Membrane proteins – Cell staining – Immunoprecipitation – HeLa cells – Immunofluorescence


Zdroje

1. Seo S, Zhang Q, Bugge K, Breslow DK, Searby CC, Nachury MV, et al. A novel protein LZTFL1 regulates ciliary trafficking of the BBSome and Smoothened. PLoS Genet. 2011;7(11):e1002358. Epub 2011/11/11. doi: 10.1371/journal.pgen.1002358 22072986; PubMed Central PMCID: PMC3207910.

2. Wang L, Guo J, Wang Q, Zhou J, Xu C, Teng R, et al. LZTFL1 suppresses gastric cancer cell migration and invasion through regulating nuclear translocation of beta-catenin. J Cancer Res Clin Oncol. 2014;140(12):1997–2008. Epub 2014/07/10. doi: 10.1007/s00432-014-1753-9 25005785.

3. Wei Q, Zhou W, Wang W, Gao B, Wang L, Cao J, et al. Tumor-suppressive functions of leucine zipper transcription factor-like 1. Cancer Res. 2010;70(7):2942–50. Epub 2010/03/18. doi: 10.1158/0008-5472.CAN-09-3826 20233871; PubMed Central PMCID: PMC2848875.

4. Pacheco-Pinedo EC, Durham AC, Stewart KM, Goss AM, Lu MM, Demayo FJ, et al. Wnt/beta-catenin signaling accelerates mouse lung tumorigenesis by imposing an embryonic distal progenitor phenotype on lung epithelium. J Clin Invest. 2011;121(5):1935–45. Epub 2011/04/15. doi: 10.1172/JCI44871 21490395; PubMed Central PMCID: PMC3083778.

5. Jiang H, Promchan K, Lin BR, Lockett S, Chen D, Marshall H, et al. LZTFL1 Upregulated by All-Trans Retinoic Acid during CD4+ T Cell Activation Enhances IL-5 Production. J Immunol. 2016;196(3):1081–90. Epub 2015/12/25. doi: 10.4049/jimmunol.1500719 26700766; PubMed Central PMCID: PMC4724573.

6. Schaefer E, Lauer J, Durand M, Pelletier V, Obringer C, Claussmann A, et al. Mesoaxial polydactyly is a major feature in Bardet-Biedl syndrome patients with LZTFL1 (BBS17) mutations. Clin Genet. 2014;85(5):476–81. Epub 2013/05/23. doi: 10.1111/cge.12198 23692385.

7. Jiang J, Promchan K, Jiang H, Awasthi P, Marshall H, Harned A, et al. Depletion of BBS Protein LZTFL1 Affects Growth and Causes Retinal Degeneration in Mice. J Genet Genomics. 2016;43(6):381–91. Epub 2016/06/18. doi: 10.1016/j.jgg.2015.11.006 27312011; PubMed Central PMCID: PMC4925197.

8. Datta P, Allamargot C, Hudson JS, Andersen EK, Bhattarai S, Drack AV, et al. Accumulation of non-outer segment proteins in the outer segment underlies photoreceptor degeneration in Bardet-Biedl syndrome. Proc Natl Acad Sci U S A. 2015;112(32):E4400–9. Epub 2015/07/29. doi: 10.1073/pnas.1510111112 26216965; PubMed Central PMCID: PMC4538681.

9. Bonifacino JS, Traub LM. Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu Rev Biochem. 2003;72:395–447. Epub 2003/03/26. doi: 10.1146/annurev.biochem.72.121801.161800 12651740.

10. Boehm M, Bonifacino JS. Adaptins: the final recount. Mol Biol Cell. 2001;12(10):2907–20. Epub 2001/10/13. doi: 10.1091/mbc.12.10.2907 11598180; PubMed Central PMCID: PMC60144.

11. Nakatsu F, Hase K, Ohno H. The Role of the Clathrin Adaptor AP-1: Polarized Sorting and Beyond. Membranes (Basel). 2014;4(4):747–63. Epub 2014/11/12. doi: 10.3390/membranes4040747 25387275; PubMed Central PMCID: PMC4289864.

12. Beattie EC, Howe CL, Wilde A, Brodsky FM, Mobley WC. NGF signals through TrkA to increase clathrin at the plasma membrane and enhance clathrin-mediated membrane trafficking. J Neurosci. 2000;20(19):7325–33. Epub 2000/09/29. doi: 10.1523/JNEUROSCI.20-19-07325.2000 11007890.

13. Waguri S, Dewitte F, Le Borgne R, Rouille Y, Uchiyama Y, Dubremetz JF, et al. Visualization of TGN to endosome trafficking through fluorescently labeled MPR and AP-1 in living cells. Mol Biol Cell. 2003;14(1):142–55. Epub 2003/01/17. doi: 10.1091/mbc.E02-06-0338 12529433; PubMed Central PMCID: PMC140234.

14. Owen DJ, Vallis Y, Noble ME, Hunter JB, Dafforn TR, Evans PR, et al. A structural explanation for the binding of multiple ligands by the alpha-adaptin appendage domain. Cell. 1999;97(6):805–15. Epub 1999/06/25. doi: 10.1016/s0092-8674(00)80791-6 10380931.

15. Traub LM, Downs MA, Westrich JL, Fremont DH. Crystal structure of the alpha appendage of AP-2 reveals a recruitment platform for clathrin-coat assembly. Proc Natl Acad Sci U S A. 1999;96(16):8907–12. Epub 1999/08/04. doi: 10.1073/pnas.96.16.8907 10430869; PubMed Central PMCID: PMC17706.

16. Schmid EM, Ford MG, Burtey A, Praefcke GJ, Peak-Chew SY, Mills IG, et al. Role of the AP2 beta-appendage hub in recruiting partners for clathrin-coated vesicle assembly. PLoS Biol. 2006;4(9):e262. Epub 2006/08/15. doi: 10.1371/journal.pbio.0040262 16903783; PubMed Central PMCID: PMC1540706.

17. Folsch H, Pypaert M, Maday S, Pelletier L, Mellman I. The AP-1A and AP-1B clathrin adaptor complexes define biochemically and functionally distinct membrane domains. J Cell Biol. 2003;163(2):351–62. Epub 2003/10/29. doi: 10.1083/jcb.200309020 14581457; PubMed Central PMCID: PMC2173537.

18. Gravotta D, Carvajal-Gonzalez JM, Mattera R, Deborde S, Banfelder JR, Bonifacino JS, et al. The clathrin adaptor AP-1A mediates basolateral polarity. Dev Cell. 2012;22(4):811–23. Epub 2012/04/21. doi: 10.1016/j.devcel.2012.02.004 22516199; PubMed Central PMCID: PMC3690600.

19. Perez Bay AE, Schreiner R, Mazzoni F, Carvajal-Gonzalez JM, Gravotta D, Perret E, et al. The kinesin KIF16B mediates apical transcytosis of transferrin receptor in AP-1B-deficient epithelia. Embo j. 2013;32(15):2125–39. Epub 2013/06/12. doi: 10.1038/emboj.2013.130 23749212; PubMed Central PMCID: PMC3730227.

20. Perez Bay AE, Schreiner R, Benedicto I, Rodriguez-Boulan EJ. Galectin-4-mediated transcytosis of transferrin receptor. J Cell Sci. 2014;127(Pt 20):4457–69. Epub 2014/09/03. doi: 10.1242/jcs.153437 25179596; PubMed Central PMCID: PMC4197088.

21. Ishaq M, Lin BR, Bosche M, Zheng X, Yang J, Huang D, et al. LIM kinase 1—dependent cofilin 1 pathway and actin dynamics mediate nuclear retinoid receptor function in T lymphocytes. BMC Mol Biol. 2011;12:41. Epub 2011/09/20. doi: 10.1186/1471-2199-12-41 21923909; PubMed Central PMCID: PMC3187726.

22. Mi L, Hood BL, Stewart NA, Xiao Z, Govind S, Wang X, et al. Identification of potential protein targets of isothiocyanates by proteomics. Chem Res Toxicol. 2011;24(10):1735–43. Epub 2011/08/16. doi: 10.1021/tx2002806 21838287; PubMed Central PMCID: PMC3493163.

23. Maddon PJ, Dalgleish AG, McDougal JS, Clapham PR, Weiss RA, Axel R. The T4 gene encodes the AIDS virus receptor and is expressed in the immune system and the brain. Cell. 1986;47(3):333–48. Epub 1986/11/07. doi: 10.1016/0092-8674(86)90590-8 3094962.

24. Costes SV, Daelemans D, Cho EH, Dobbin Z, Pavlakis G, Lockett S. Automatic and quantitative measurement of protein-protein colocalization in live cells. Biophys J. 2004;86(6):3993–4003. Epub 2004/06/11. doi: 10.1529/biophysj.103.038422 15189895; PubMed Central PMCID: PMC1304300.

25. Webster J, Oxley D. Protein identification by MALDI-TOF mass spectrometry. Methods Mol Biol. 2012;800:227–40. Epub 2011/10/04. doi: 10.1007/978-1-61779-349-3_15 21964792.

26. Kaplan OI, Molla-Herman A, Cevik S, Ghossoub R, Kida K, Kimura Y, et al. The AP-1 clathrin adaptor facilitates cilium formation and functions with RAB-8 in C. elegans ciliary membrane transport. J Cell Sci. 2010;123(Pt 22):3966–77. Epub 2010/10/29. doi: 10.1242/jcs.073908 20980383; PubMed Central PMCID: PMC2972276.

27. Dinkel H, Van Roey K, Michael S, Davey NE, Weatheritt RJ, Born D, et al. The eukaryotic linear motif resource ELM: 10 years and counting. Nucleic Acids Res. 2014;42(Database issue):D259–66. Epub 2013/11/12. doi: 10.1093/nar/gkt1047 24214962; PubMed Central PMCID: PMC3964949.

28. Edeling MA, Mishra SK, Keyel PA, Steinhauser AL, Collins BM, Roth R, et al. Molecular switches involving the AP-2 beta2 appendage regulate endocytic cargo selection and clathrin coat assembly. Dev Cell. 2006;10(3):329–42. Epub 2006/03/07. doi: 10.1016/j.devcel.2006.01.016 16516836.

29. Traub LM, Bonifacino JS. Cargo recognition in clathrin-mediated endocytosis. Cold Spring Harb Perspect Biol. 2013;5(11):a016790. Epub 2013/11/05. doi: 10.1101/cshperspect.a016790 24186068; PubMed Central PMCID: PMC3809577.

30. Alvarez Arias DA, McCarty N, Lu L, Maldonado RA, Shinohara ML, Cantor H. Unexpected role of clathrin adaptor AP-1 in MHC-dependent positive selection of T cells. Proc Natl Acad Sci U S A. 2010;107(6):2556–61. Epub 2010/02/06. doi: 10.1073/pnas.0913671107 20133794; PubMed Central PMCID: PMC2823916.

31. Bonifacino JS. Adaptor proteins involved in polarized sorting. J Cell Biol. 2014;204(1):7–17. Epub 2014/01/08. doi: 10.1083/jcb.201310021 24395635; PubMed Central PMCID: PMC3882786.

32. Bonifacino JS, Glick BS. The mechanisms of vesicle budding and fusion. Cell. 2004;116(2):153–66. Epub 2004/01/28. doi: 10.1016/s0092-8674(03)01079-1 14744428.

33. Lippincott-Schwartz J, Yuan LC, Bonifacino JS, Klausner RD. Rapid redistribution of Golgi proteins into the ER in cells treated with brefeldin A: evidence for membrane cycling from Golgi to ER. Cell. 1989;56(5):801–13. Epub 1989/03/10. doi: 10.1016/0092-8674(89)90685-5 2647301.

34. Strous GJ, Berger EG, van Kerkhof P, Bosshart H, Berger B, Geuze HJ. Brefeldin A induces a microtubule-dependent fusion of galactosyltransferase-containing vesicles with the rough endoplasmic reticulum. Biol Cell. 1991;71(1–2):25–31. Epub 1991/01/01. doi: 10.1016/0248-4900(91)90048-r 1912946.

35. Caster AH, Kahn RA. Recruitment of the Mint3 adaptor is necessary for export of the amyloid precursor protein (APP) from the Golgi complex. J Biol Chem. 2013;288(40):28567–80. Epub 2013/08/24. doi: 10.1074/jbc.M113.481101 23965993; PubMed Central PMCID: PMC3789957.

36. Wood SA, Park JE, Brown WJ. Brefeldin A causes a microtubule-mediated fusion of the trans-Golgi network and early endosomes. Cell. 1991;67(3):591–600. Epub 1991/11/01. doi: 10.1016/0092-8674(91)90533-5 1657400.

37. Caster AH, Sztul E, Kahn RA. A role for cargo in Arf-dependent adaptor recruitment. J Biol Chem. 2013;288(21):14788–804. Epub 2013/04/11. doi: 10.1074/jbc.M113.453621 23572528; PubMed Central PMCID: PMC3663503.

38. Shinotsuka C, Yoshida Y, Kawamoto K, Takatsu H, Nakayama K. Overexpression of an ADP-ribosylation factor-guanine nucleotide exchange factor, BIG2, uncouples brefeldin A-induced adaptor protein-1 coat dissociation and membrane tubulation. J Biol Chem. 2002;277(11):9468–73. Epub 2002/01/05. doi: 10.1074/jbc.M112427200 11777925.

39. Shinotsuka C, Waguri S, Wakasugi M, Uchiyama Y, Nakayama K. Dominant-negative mutant of BIG2, an ARF-guanine nucleotide exchange factor, specifically affects membrane trafficking from the trans-Golgi network through inhibiting membrane association of AP-1 and GGA coat proteins. Biochem Biophys Res Commun. 2002;294(2):254–60. Epub 2002/06/08. doi: 10.1016/S0006-291X(02)00456-4 12051703.

40. Jian J, Yang Q, Huang X. Src regulates Tyr(20) phosphorylation of transferrin receptor-1 and potentiates breast cancer cell survival. J Biol Chem. 2011;286(41):35708–15. Epub 2011/08/24. doi: 10.1074/jbc.M111.271585 21859709; PubMed Central PMCID: PMC3195600.

41. Cao H, Schroeder B, Chen J, Schott MB, McNiven MA. The Endocytic Fate of the Transferrin Receptor Is Regulated by c-Abl Kinase. J Biol Chem. 2016;291(32):16424–37. Epub 2016/05/27. doi: 10.1074/jbc.M116.724997 27226592; PubMed Central PMCID: PMC4974358.

42. Wymant JM, Hiscox S, Westwell AD, Urbe S, Clague MJ, Jones AT. The Role of BCA2 in the Endocytic Trafficking of EGFR and Significance as a Prognostic Biomarker in Cancer. J Cancer. 2016;7(15):2388–407. Epub 2016/12/21. doi: 10.7150/jca.15055 27994678; PubMed Central PMCID: PMC5166551.

43. Cotton CU, Hobert ME, Ryan S, Carlin CR. Basolateral EGF receptor sorting regulated by functionally distinct mechanisms in renal epithelial cells. Traffic. 2013;14(3):337–54. Epub 2012/12/05. doi: 10.1111/tra.12032 23205726; PubMed Central PMCID: PMC4304763.

44. Sorkina T, Bild A, Tebar F, Sorkin A. Clathrin, adaptors and eps15 in endosomes containing activated epidermal growth factor receptors. J Cell Sci. 1999;112 (Pt 3):317–27. Epub 1999/01/14. 9885285.

45. Honing S, Sosa M, Hille-Rehfeld A, von Figura K. The 46-kDa mannose 6-phosphate receptor contains multiple binding sites for clathrin adaptors. J Biol Chem. 1997;272(32):19884–90. Epub 1997/08/08. doi: 10.1074/jbc.272.32.19884 9242653.

46. Le Borgne R, Hoflack B. Mannose 6-phosphate receptors regulate the formation of clathrin-coated vesicles in the TGN. J Cell Biol. 1997;137(2):335–45. Epub 1997/04/21. doi: 10.1083/jcb.137.2.335 9128246; PubMed Central PMCID: PMC2139777.

47. Ghosh P, Kornfeld S. The cytoplasmic tail of the cation-independent mannose 6-phosphate receptor contains four binding sites for AP-1. Arch Biochem Biophys. 2004;426(2):225–30. Epub 2004/05/26. doi: 10.1016/j.abb.2004.02.011 15158672.

48. Klumperman J, Kuliawat R, Griffith JM, Geuze HJ, Arvan P. Mannose 6-phosphate receptors are sorted from immature secretory granules via adaptor protein AP-1, clathrin, and syntaxin 6-positive vesicles. J Cell Biol. 1998;141(2):359–71. Epub 1998/05/23. doi: 10.1083/jcb.141.2.359 9548715; PubMed Central PMCID: PMC2148452.

49. Stahlschmidt W, Robertson MJ, Robinson PJ, McCluskey A, Haucke V. Clathrin terminal domain-ligand interactions regulate sorting of mannose 6-phosphate receptors mediated by AP-1 and GGA adaptors. J Biol Chem. 2014;289(8):4906–18. Epub 2014/01/11. doi: 10.1074/jbc.M113.535211 24407285; PubMed Central PMCID: PMC3931052.

50. Beydoun R, Hamood MA, Gomez Zubieta DM, Kondapalli KC. Na(+)/H(+) Exchanger 9 Regulates Iron Mobilization at the Blood-Brain Barrier in Response to Iron Starvation. J Biol Chem. 2017;292(10):4293–301. Epub 2017/01/29. doi: 10.1074/jbc.M116.769240 28130443; PubMed Central PMCID: PMC5354498.

51. Robb AD, Ericsson M, Wessling-Resnick M. Transferrin receptor 2 mediates a biphasic pattern of transferrin uptake associated with ligand delivery to multivesicular bodies. Am J Physiol Cell Physiol. 2004;287(6):C1769–75. Epub 2004/08/20. doi: 10.1152/ajpcell.00337.2004 15317665.

52. Graham RM, Reutens GM, Herbison CE, Delima RD, Chua AC, Olynyk JK, et al. Transferrin receptor 2 mediates uptake of transferrin-bound and non-transferrin-bound iron. J Hepatol. 2008;48(2):327–34. Epub 2007/12/18. doi: 10.1016/j.jhep.2007.10.009 18083267.

53. Chen J, Wang J, Meyers KR, Enns CA. Transferrin-directed internalization and cycling of transferrin receptor 2. Traffic. 2009;10(10):1488–501. Epub 2009/08/18. doi: 10.1111/j.1600-0854.2009.00961.x 19682329; PubMed Central PMCID: PMC2746864.

54. Lou X, Shin YK. SNARE zippering. Biosci Rep. 2016;36(3). Epub 2016/05/08. doi: 10.1042/BSR20160004 27154457; PubMed Central PMCID: PMC4859083.

55. Harbury PA. Springs and zippers: coiled coils in SNARE-mediated membrane fusion. Structure. 1998;6(12):1487–91. Epub 1998/12/24. doi: 10.1016/s0969-2126(98)00147-6 9862813.

56. Lundmark R, Carlsson SR. The beta-appendages of the four adaptor-protein (AP) complexes: structure and binding properties, and identification of sorting nexin 9 as an accessory protein to AP-2. Biochem J. 2002;362(Pt 3):597–607. Epub 2002/03/07. doi: 10.1042/0264-6021:3620597 11879186; PubMed Central PMCID: PMC1222423.

57. Laporte SA, Oakley RH, Holt JA, Barak LS, Caron MG. The interaction of beta-arrestin with the AP-2 adaptor is required for the clustering of beta 2-adrenergic receptor into clathrin-coated pits. J Biol Chem. 2000;275(30):23120–6. Epub 2000/04/20. doi: 10.1074/jbc.M002581200 10770944.

58. Kang RS, Folsch H. ARH cooperates with AP-1B in the exocytosis of LDLR in polarized epithelial cells. J Cell Biol. 2011;193(1):51–60. Epub 2011/03/30. doi: 10.1083/jcb.201012121 21444685; PubMed Central PMCID: PMC3082197.

59. Nakatsu F, Ohno H. Adaptor protein complexes as the key regulators of protein sorting in the post-Golgi network. Cell Struct Funct. 2003;28(5):419–29. Epub 2004/01/28. doi: 10.1247/csf.28.419 14745134.

60. Owen DJ, Vallis Y, Pearse BM, McMahon HT, Evans PR. The structure and function of the beta 2-adaptin appendage domain. Embo j. 2000;19(16):4216–27. Epub 2000/08/16. doi: 10.1093/emboj/19.16.4216 10944104; PubMed Central PMCID: PMC302036.

61. Reed SE, Hodgson LR, Song S, May MT, Kelly EE, McCaffrey MW, et al. A role for Rab14 in the endocytic trafficking of GLUT4 in 3T3-L1 adipocytes. J Cell Sci. 2013;126(Pt 9):1931–41. Epub 2013/02/28. doi: 10.1242/jcs.104307 23444368; PubMed Central PMCID: PMC3666250.

62. Xie S, Bahl K, Reinecke JB, Hammond GR, Naslavsky N, Caplan S. The endocytic recycling compartment maintains cargo segregation acquired upon exit from the sorting endosome. Mol Biol Cell. 2016;27(1):108–26. Epub 2015/10/30. doi: 10.1091/mbc.E15-07-0514 26510502; PubMed Central PMCID: PMC4694750.

63. Dellibovi-Ragheb T, Altan-Bonnet N. Cloud storage for endosomes. EMBO J. 2016;35(16):1724–5. Epub 2016/07/06. doi: 10.15252/embj.201695080 27378788; PubMed Central PMCID: PMC5010045.

64. Jongsma ML, Berlin I, Wijdeven RH, Janssen L, Janssen GM, Garstka MA, et al. An ER-Associated Pathway Defines Endosomal Architecture for Controlled Cargo Transport. Cell. 2016;166(1):152–66. Epub 2016/07/02. doi: 10.1016/j.cell.2016.05.078 27368102; PubMed Central PMCID: PMC4930482.

65. Folsch H, Pypaert M, Schu P, Mellman I. Distribution and function of AP-1 clathrin adaptor complexes in polarized epithelial cells. J Cell Biol. 2001;152(3):595–606. Epub 2001/02/07. doi: 10.1083/jcb.152.3.595 11157985; PubMed Central PMCID: PMC2195989.

66. Starks RD, Beyer AM, Guo DF, Boland L, Zhang Q, Sheffield VC, et al. Regulation of Insulin Receptor Trafficking by Bardet Biedl Syndrome Proteins. PLoS Genet. 2015;11(6):e1005311. Epub 2015/06/24. doi: 10.1371/journal.pgen.1005311 26103456; PubMed Central PMCID: PMC4478011.

67. Simonetti B, Cullen PJ. Actin-dependent endosomal receptor recycling. Curr Opin Cell Biol. 2019;56:22–33. Epub 2018/09/19. doi: 10.1016/j.ceb.2018.08.006 30227382.

68. Wei Q, Gu YF, Zhang QJ, Yu H, Peng Y, Williams KW, et al. Lztfl1/BBS17 controls energy homeostasis by regulating the leptin signaling in the hypothalamic neurons. J Mol Cell Biol. 2018;10(5):402–10. Epub 2018/11/14. doi: 10.1093/jmcb/mjy022 30423168.


Článok vyšiel v časopise

PLOS One


2020 Číslo 1
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#