PKC induces internalization and retention of the EAAC1 glutamate transporter in recycling endosomes of MDCK cells

American Journal of Physiology - Cell Physiology

Volumn 297, Issue 4, 2009, Pages

  Padovano, Valeria ^a   Massari, Silvia ^a   Mazzucchelli, Silvia ^a   Pietrini, Grazia ^a  

^a UNIVERSITY OF MILAN   (Italy)

Author keywords

Common recycling endosomes; Cyclosporine A; Dynamin 1; Excitatory amino acid carrier; Pericentrion; Protein kinase C

Indexed keywords

4 AMINOBUTYRIC ACID CARRIER; BETAINE; CALCINEURIN; CYCLOSPORIN A; DYNAMIN I; EXCITATORY AMINO ACID TRANSPORTER 3; GLUTAMATE TRANSPORTER; GLUTAMIC ACID; MEMBRANE PROTEIN; PHORBOL 13 ACETATE 12 MYRISTATE; PHOSPHATASE; PROTEIN BGT1; PROTEIN KINASE C; PROTEIN KINASE C ALPHA; SERINE; UNCLASSIFIED DRUG;

ANIMAL CELL; APICAL MEMBRANE; ARTICLE; BASOLATERAL MEMBRANE; BIOACCUMULATION; CELL COMPARTMENTALIZATION; CELL STRAIN; CONTROLLED STUDY; ENDOSOME; ENZYME ACTIVATION; ENZYME ACTIVITY; IMMUNOFLUORESCENCE; INTERNALIZATION; INTRACELLULAR SPACE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SURFACE PROPERTY;

ANIMALS; CALCINEURIN; CARRIER PROTEINS; CELL COMPARTMENTATION; CELL LINE; DOGS; ENDOCYTOSIS; ENDOSOMES; ENZYME ACTIVATION; EXCITATORY AMINO ACID TRANSPORTER 3; GLUTAMIC ACID; PROTEIN KINASE C-ALPHA; TETRADECANOYLPHORBOL ACETATE;

EID: 70349923414     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00212.2009     Document Type: Article

References (42)

1. Akiduki S, Ikemoto MJ. Modulation of the neural glutamate transporter EAAC1 by the addicsin-interacting protein ARL6IP1. J Biol Chem 283: 31323-31332, 2008.
2. Altschuler Y, Barbas SM, Terlecky LJ, Tang K, Hardy S, Mostov KE, Schmid SL. Redundant and distinct functions for dynamin-1 and dynamin-2 isoforms. J Cell Biol 143: 1871-1881, 1998.
3. Aoyama K, Suh SW, Hamby AM, Liu J, Chan WY, Chen Y, Swanson RA. Neuronal glutathione deficiency and age-dependent neurodegeneration in the EAAC1 deficient mouse. Nat Neurosci 9: 119-126, 2006. (Pubitemid 43011917)
4. Arriza JL, Eliasof S, Kavanaugh MP, Amara SG. Excitatory amino acid transporter 5, a retinal glutamate transporter coupled to a chloride conductance. Proc Natl Acad Sci USA 94: 4155-4160, 1997. (Pubitemid 27180515)
5. Becker KP, Hannun YA. cPKC-dependent sequestration of membrane-recycling components in a subset of recycling endosomes. J Biol Chem 278: 52747-52754, 2003.
6. Butchbach ME, Lai L, Lin CL. Molecular cloning, gene structure, expression profile and functional characterization of the mouse glutamate transporter (EAAT3) interacting protein GTRAP3-18. Gene 292: 81-90, 2002. (Pubitemid 34761991)
7. Chang MY, Lee SH, Kim JH, Lee KH, Kim YS, Son H, Lee YS. Protein kinase C-mediated functional regulation of dopamine transporter is not achieved by direct phosphorylation of the dopamine transporter protein. J Neurochem 77: 754-761, 2001. (Pubitemid 32471848)
8. Cheng C, Glover G, Banker G, Amara SG. A novel sorting motif in the glutamate transporter excitatory amino acid transporter 3 directs its targeting in Madin-Darby canine kidney cells and hippocampal neurons. J Neurosci 22: 10643-10652, 2002. (Pubitemid 36005138)
9. Cousin MA, Robinson PJ. The dephosphins: dephosphorylation by calcineurin triggers synaptic vesicle endocytosis. Trends Neurosci 24: 659-665, 2001.
10. Damke H, Baba T, Warnock DE, Schmid SL. Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J Cell Biol 127: 915-934, 1994. (Pubitemid 24355982)
11. Fournier KM, Gonzalez MI, Robinson MB. Rapid trafficking of the neuronal glutamate transporter, EAAC1: evidence for distinct trafficking pathways differentially regulated by protein kinase C and platelet-derived growth factor. J Biol Chem 279: 34505-34513, 2004.
12. Gonzalez MI, Bannerman PG, Robinson MB. Phorbol myristate acetate-dependent interaction of protein kinase Calpha and the neuronal glutamate transporter EAAC1. J Neurosci 23: 5589-5593, 2003.
13. Griffiths G, Matteoni R, Back R, Hoflack B. Characterization of the cation-independent mannose 6-phosphate receptor-enriched prelysosomal compartment in NRK cells. J Cell Sci 95: 441-461, 1990. (Pubitemid 20108074)
14. Heuser JE, Anderson RG. Hypertonic media inhibit receptor-mediated endocytosis by blocking clathrin-coated pit formation. J Cell Biol 108: 389-400, 1989.
15. Idkowiak-Baldys J, Becker KP, Kitatani K, Hannun YA. Dynamic sequestration of the recycling compartment by classical protein kinase C. J Biol Chem 281: 22321-22331, 2006. (Pubitemid 44181934)
16. Isidoro C, De Stefanis D, Demoz M, Ogier-Denis E, Codogno P, Baccino FM. Expression and posttranslational fate of cathepsin D in HT-29 tumor cells depend on their enterocytic differentiation state. Cell Growth Differ 8: 1029-1037, 1997. (Pubitemid 27388098)
17. Kanai Y, Hediger MA. Primary structure and functional characterization of a high-affinity glutamate transporter. Nature 360: 467-471, 1992.
18. Lin CI, Orlov I, Ruggiero AM, Dykes-Hoberg M, Lee A, Jackson M, Rothstein JD. Modulation of the neuronal glutamate transporter EAAC1 by the interacting protein GTRAP3-18. Nature 410: 84-88, 2001. (Pubitemid 32225840)
19. Macia E, Ehrlich M, Massol R, Boucrot E, Brunner C, Kirchhausen T. Dynasore, a cell-permeable inhibitor of dynamin. Dev Cell 10: 839-850, 2006.
20. Massari S, Vanoni C, Longhi R, Rosa P, Pietrini G. Protein kinase C-mediated phosphorylation of the BGT1 epithelial gamma-aminobutyric acid transporter regulates its association with LIN7 PDZ proteins: a post-translational mechanism regulating transporter surface density. J Biol Chem 280: 7388-7397, 2005. (Pubitemid 40341297)
21. Peghini P, Janzen J, Stoffel W. Glutamate transporter EAAC-1-deficient mice develop dicarboxylic aminoaciduria and behavioral abnormalities but no neurodegeneration. EMBO J 16: 3822-3832, 1997. (Pubitemid 27280998)
22. Pelkmans L, Helenius A. Insider information: what viruses tell us about endocytosis. Curr Opin Cell Biol 15: 414-422, 2003. (Pubitemid 36928043)
23. Perego C, Vanoni C, Villa A, Longhi R, Kaech SM, Frohli E, Hajnal A, Kim SK, Pietrini G. PDZ-mediated interactions retain the epithelial GABA transporter on the basolateral surface of polarized epithelial cells. EMBO J 18: 2384-2393, 1999. (Pubitemid 29213272)
24. Perletti GP, Folini M, Lin HC, Mischak H, Piccinini F, Tashjian AH Jr. Overexpression of protein kinase C epsilon is oncogenic in rat colonic epithelial cells. Oncogene 12: 847-854, 1996. (Pubitemid 26072270)
25. Pietrini G, Matteoli M, Banker G, Caplan MJ. Isoforms of the Na,K-ATPase are present in both axons and dendrites of hippocampal neurons in culture. Proc Natl Acad Sci USA 89: 8414-8418, 1992.
26. Pietrini G, Suh YJ, Edelmann L, Rudnick G, Caplan MJ. The axonal gamma-aminobutyric acid transporter GAT-1 is sorted to the apical membranes of polarized epithelial cells. J Biol Chem 269: 4668-4674, 1994. (Pubitemid 24237841)
27. Pines G, Danbolt NC, Bjoras M, Zhang Y, Bendahan A, Eide L, Koepsell H, Storm-Mathisen J, Seeberg E, Kanner BI. Cloning and expression of a rat brain L-glutamate transporter. Nature 360: 464-467, 1992.
28. Robinson MB. Regulated trafficking of neurotransmitter transporters: common notes but different melodies. J Neurochem 80: 1-11, 2002.
29. Rodriguez-Boulan E, Kreitzer G, Musch A. Organization of vesicular trafficking in epithelia. Nat Rev Mol Cell Biol 6: 233-247, 2005.
30. Rosa P, Mantovani S, Rosboch R, Huttner WB. Monensin and brefeldin A differentially affect the phosphorylation and sulfation of secretory proteins. J Biol Chem 267: 12227-12232, 1992.
31. Royle SJ, Murrell-Lagnado RD. Constitutive cycling: a general mechanism to regulate cell surface proteins. Bioessays 25: 39-46, 2003.
32. Sahin B, Hawasli AH, Greene RW, Molkentin JD, Bibb JA. Negative regulation of cyclin-dependent kinase 5 targets by protein kinase C. Eur J Pharmacol 581: 270-275, 2008.
33. Sargiacomo M, Lisanti M, Graeve L, Le Bivic A, Rodriguez-Boulan E. Integral and peripheral protein composition of the apical and basolateral membrane domains in MDCK cells. J Membr Biol 107: 277-286, 1989. (Pubitemid 19085859)
34. Sheldon AL, Robinson MB. The role of glutamate transporters in neurodegenerative diseases and potential opportunities for intervention. Neurochem Int 51: 333-355, 2007. (Pubitemid 47503456)
35. Smillie KJ, Cousin MA. Dynamin I phosphorylation and the control of synaptic vesicle endocytosis. Biochem Soc Symp 72: 87-97, 2005. (Pubitemid 44804738)
36. Storck T, Schulte S, Hofmann K, Stoffel W. Structure, expression, and functional analysis of a Na(+)-dependent glutamate/aspartate transporter from rat brain. Proc Natl Acad Sci USA 89: 10955-10959, 1992.
37. Trotti D, Peng JB, Dunlop J, Hediger MA. Inhibition of the glutamate transporter EAAC1 expressed in Xenopus oocytes by phorbol esters. Brain Res 914: 196-203, 2001. (Pubitemid 32905446)
38. Vanoni C, Massari S, Losa M, Carrega P, Perego C, Conforti L, Pietrini G. Increased internalisation and degradation of GLT-1 glial glutamate transporter in a cell model for familial amyotrophic lateral sclerosis (ALS). J Cell Sci 117: 5417-5426, 2004. (Pubitemid 39562502)
39. Watabe M, Aoyama K, Nakaki T. A dominant role of GTRAP3-18 in neuronal glutathione synthesis. J Neurosci 28: 9404-9413, 2008.
40. Wu HY, Tomizawa K, Matsui H. Calpain-calcineurin signaling in the pathogenesis of calcium-dependent disorder. Acta Med Okayama 61: 123-137, 2007. (Pubitemid 47052599)
41. Yamauchi A, Kwon HM, Uchida S, Preston AS, Handler JS. Myoinositol and betaine transporters regulated by tonicity are basolateral in MDCK cells. Am J Physiol Renal Fluid Electrolyte Physiol 261: F197-F202, 1991.
42. Yu YX, Shen L, Xia P, Tang YW, Bao L, Pei G. Syntaxin 1A promotes the endocytic sorting of EAAC1 leading to inhibition of glutamate transport. J Cell Sci 119: 3776-3787, 2006. (Pubitemid 44614430)