Paralemmin, a prenyl-palmitoyl-anchored phosphoprotein abundant in neurons and implicated in plasma membrane dynamics and cell process formation

Journal of Cell Biology

Volumn 143, Issue 3, 1998, Pages 795-813

  Kutzleb, Christian ^a   Sanders, Gabriele ^a   Yamamoto, Raina ^a   Wang, Xiaolu ^a   Lichte, Beate ^a   Petrasch Parwez, Elisabeth ^a   Kilimann, Manfred W ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

Cortical cytoskeleton; Farnesylation; Lipidation; Membrane traffic; Synapse

Indexed keywords

PHOSPHOPROTEIN;

ANIMAL CELL; ARTICLE; CELL FRACTIONATION; CHICKEN; HUMAN; MOLECULAR CLONING; MOUSE; NERVE CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; RNA SPLICING;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; BRAIN; CELL FRACTIONATION; CELL MEMBRANE; CHICKENS; CLONING, MOLECULAR; COS CELLS; DNA, COMPLEMENTARY; ELECTROPHORESIS; ENDOPEPTIDASES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; IMMUNOBLOTTING; IMMUNOENZYME TECHNIQUES; MEMBRANE PROTEINS; MICE; MICROSCOPY, FLUORESCENCE; MOLECULAR SEQUENCE DATA; NEURONS; PHOSPHOPROTEINS; PHOSPHORYLATION; RABBITS; RATS; RNA SPLICING; RNA, MESSENGER; SEQUENCE HOMOLOGY, AMINO ACID; TISSUE DISTRIBUTION;

ANIMALIA; GALLUS GALLUS;

EID: 0032476649     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.143.3.795     Document Type: Article

References (65)

1. Aarts, L.H.J., L.H. Schrama, W.J. Hage, J.L. Bos, W.H. Gispen, and P. Schotman. 1998. B-50/GAP-43-induced formation of filopodia depends on Rho-GTPase. Mol. Biol. Cell. 9:1279-1292.
2. Adamson, P., C.J. Marshall, A. Hall, and P.A. Tilbrook. 1992. Post-translational modifications of p21rho proteins. J. Biol. Chem. 267:20033-20038.
3. Aigner, L., S. Arber, J.P. Kapfhammer, T. Laux, C. Schneider, F. Botteri, H.-R. Brenner, and P. Caroni. 1995. Overexpression of the neural growth-associated protein GAP-43 induces nerve sprouting in the adult nervous system of transgenic mice. Cell. 83:269-278.
4. Allen, L.H., and A. Aderem. 1995. A role for MARCKS, the α isozyme of protein kinase C and myosin I in zymosan phagozytosis by macrophages. J. Exp. Med. 182:829-840.
5. Babitch, J.A., T.B. Breithaupt, T.-C. Chiu, R. Garadi, and D.L. Helseth. 1976. Preparation of chick brain synaptosomes and synaptosomal membranes. Biochim. Biophys. Acta. 433:75-89.
6. Bordier, C. 1981. Phase separation of integral membrane proteins in Triton X-114 solution. J. Biol. Chem. 256:1604-1607.
7. Burwinkel, B., Y.S. Shin, H.D. Bakker, J. Deutsch, M.J. Lozano, I. Maire, and M.W. Kilimann. 1996. Mutation hotspots in the PHKA2 gene in X-linked liver glycogenosis due to phosphorylase kinase deficiency with atypical activity in blood cells (XLG2). Hum. Mol. Genet. 5:653-658.
8. Burwinkel, B., G. Miglierini, D.E. Jenne, D.J. Gilbert, N.G. Copeland, N.A. Jenkins, H.Z. Ring, U. Francke, and M.W. Kilimann. 1998. Structure of the human paralemmin gene (PALM), mapping to human chromosome 19p13.3 and mouse chromosome 10, and exclusion of coding mutations in grizzled, mocha, jittery and hesitant mice. Genomics. 49:462-466.
9. Cadwallader, K.A., H. Paterson, S.G. Macdonald, and J.F. Hancock. 1994. N-terminally myristoylated ras proteins require palmitoylation or a polybasic domain for plasma membrane localization. Mol. Cell. Biol. 14:4722-4730.
10. Caroni, P., L. Aigner, and C. Schneider. 1997. Intrinsic neuronal determinants locally regulate extrasynaptic and synaptic growth at the adult neuromuscular junction. J. Cell Biol. 136:679-692.
11. Chapman, E.R., R.P. Estep, and D.R. Storm. 1992. Palmitylation of neuromodulin (GAP-43) is not required for phosphorylation by protein kinase C. J. Biol. Chem. 267:25233-25238.
12. Clarke, S. 1992. Protein isoprenylation and methylation at carboxyl-terminal cysteine residues. Annu. Rev. Biochem. 61:355-386.
13. De Camilli, P., A. Thomas, R. Cofiell, F. Folli, B. Lichte, G. Piccolo, H.-M. Meinck, M. Austoni, G. Fassetta, G. Bottazzo, et al. 1993. The synaptic vesicle-associated protein amphiphysin is the 128-kD autoantigen of stiff-man syndrome with breast cancer. J. Exp. Med. 178:2219-2223.
14. Dekker, L.V., P.N.E. De Graan, A.B. Oestreicher, D.H.G. Versteeg, and W.H. Gispen. 1989. Inhibition of noradrenaline release by antibodies to B-50 (GAP-43). Nature. 342:74-76.
15. Dodt, G., N. Braverman, C. Wong, A. Moser, H.W. Moser, P. Watkins, D. Valle, and S.J. Gould. 1995. Mutations in the PTS1 receptor gene PXR1 define complementation group 2 of the peroxisome biogenesis disorders. Nat. Genet. 9:115-125.
16. Dropcho, E.J. 1996. Antiamphiphysin antibodies with small-cell lung carcinoma and paraneoplastic encephalomyelitis. Ann. Neurol. 39:659-667.
17. Evan, G.I., G.K. Lewis, G. Ramsay, and J.M. Bishop. 1985. Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product. Mol. Cell. Biol. 5:3610-3616.
18. Feany, M.B., S. Lee, R.H. Edwards, and K.M. Buckley. 1992. The synaptic vesicle protein SV2 is a novel type of transmembrane transporter. Cell. 70:861-867.
19. Fischer, M., S. Kaech, D. Knutti, and A. Matus. 1998. Rapid actin-based plasticity in dendritic spines. Neuron. 20:847-854.
20. Gamby, C., M.C. Waage, R.G. Allen, and L. Baizer. 1996a. Growth-associated protein-43 (GAP-43) facilitates peptide hormone secretion in mouse anterior pituitary AtT-20 cells. J. Biol. Chem. 271:10023-10028.
21. Gamby, C., M.C. Waage, R.G. Allen, and L. Baizer. 1996b. Analysis of the role of calmodulin binding and sequestration in neuromodulin (GAP-43) function. J. Biol. Chem. 271:26698-26705.
22. Giannakouros, T., and A.I. Magee. 1992. Protein prenylation and associated modifications. In Lipid Modifications of Proteins. M.J. Schlesinger, editor. CRC Press, Boca Raton, FL. 135-162.
23. Gorgels, T.G.M.F., M. Van Lookeren Campagne, A.B. Oestreicher, A.A.M. Gribnau, and W.H. Gispen. 1989. B-50/GAP43 is localized at the cytoplasmic side of the plasma membrane in developing and adult rat pyramidal tract. J. Neurosci. 9:3861-3869.
24. Hagler, D.J., and Y. Goda. 1998. Synaptic adhesion: the building blocks of memory? Neuron. 20:1059-1062.
25. Hancock, J.F., K. Cadwallader, H. Paterson, and C.J. Marshall. 1991. A CAAX or a CAAL motif and a second signal are sufficient for plasma membrane targeting of ras proteins. EMBO (Eur. Mol. Biol. Organ.) J. 10:4033-4039.
26. Hartwig, J.H., M. Thelen, A. Rosen, P.A. Janmey, A.C. Nairn, and A. Aderem. 1992. MARCKS is an actin filament crosslinking protein regulated by protein kinase C and calcium-calmodulin. Nature. 356:618-622.
27. Hell, J.W., P.R. Maycox, H. Stadler, and R. Jahn. 1988. Uptake of GABA by rat brain synaptic vesicles isolated by a new procedure. EMBO (Eur. Mol. Biol. Organ.) J. 7:3023-3029.
28. Hens, J.J.H., F. Benfenati, H.B. Nielander, F. Valtorta, W.H. Gispen, and P.N.E. DeGraan. 1993. B-50/GAP-43 binds to actin filaments without affecting actin polymerization and filament organization. J. Neurochem. 61:1530-1533.
29. Hoesche, C., A. Sauerwald, R.W. Veh, B. Krippl, and M.W. Kilimann. 1993. The 5′-flanking region of the rat synapsin I gene directs neuron-specific and developmentally regulated reporter gene expression in transgenic mice. J. Biol. Chem. 268:26494-26502.
30. Hoesche, C., P. Bartsch, and M.W. Kilimann. 1995. The CRE consensus sequence in the synapsin I gene promoter region confers constitutive activation but no regulation by cAMP in neuroblastoma cells. Biochim. Biophys. Acta. 1261:249-256.
31. Holtmaat, A.J.G.D., P.A. Dijkhuizen, A.B. Oestreicher, H.J. Romijn, N.M.T. Van der Lugt, A. Berns, F.L. Margolis, W.H. Gispen, and J. Verhaagen. 1995. Direct expression of the growth-associated protein B-50/GAP-43 to olfactory neurons in transgenic mice results in changes in axon morphology and extraglomerular fiber growth. J. Neurosci. 15:7953-7965.
32. Johnston, G.C., J.A. Prendergast, and R.A. Singer. 1991. The Saccharomyces cerevisiae MYO2 gene encodes an essential myosin for vectorial transport of vesicles. J. Cell Biol. 113:539-551.
33. Karnik, S.S., K.D. Ridge, S. Bhattacharya, and H.G. Khorana. 1993. Palmitoylation of bovine opsin and its cysteine mutants in COS cells. Proc. Natl. Acad. Sci. USA. 90:40-44.
34. Karns, L.R., S.-C. Ng, J. A. Freeman, and M.C. Fishman. 1987. Cloning of complementary DNA for GAP-43, a neuronal growth-related protein. Science. 236:597-600.
35. Kennelly, P.J., and E.G. Krebs. 1991. Consensus sequences as substrate specificity determinants for protein kinases and protein phosphatases. J. Biol. Chem. 266:15555-15558.
36. Kloc, M., B. Reddy, S. Crawford, and L.D. Etkin. 1991. A novel 110-kDa maternal CAAX box-containing protein from Xenopus is palmitoylated and isoprenylated when expressed in baculovirus. J. Biol. Chem. 266:8206-8212.
37. Kloc, M., X.X. Li, and L.D. Etkin. 1993. Two upstream cysteines and the CAAX motif but not the polybasic domain are required for membrane association of Xlcaax in Xenopus oocytes. Biochemistry. 32:8207-8212.
38. Lichte, B., R.W. Veh, H.E. Meyer, and M.W. Kilimann. 1992. Amphiphysin, a novel protein associated with synaptic vesicles. EMBO (Eur. Mol. Biol. Organ.) J. 11:2521-2530.
39. Magee, T., and C. Newman. 1992. The role of lipid anchors for small G proteins in membrane trafficking. Trends Cell Biol. 2:318-323.
40. McNcw, J.A., M. Sögaard, N.M. Lampen, S. Machida, R.R. Ye, L. Lacomis, P. Tempst, J.E. Rothman, and T.H. Söllner. 1997. Ykt6p, a prenylated SNARE essential for endoplasmic reticulum-Golgi transport. J. Biol. Chem. 272: 17776-17783.
41. Mercer, J.A., P.K. Seperack, M.C. Strobel, N.G. Copeland, and N.A. Jenkins. 1991. Novel myosin heavy chain encoded by murine dilute coat colour locus. Nature. 349:709-713.
42. Ouimet, C.C., J.K.T. Wang, S.I. Walaas, K.A. Albert, and P. Greengard. 1990. Localization of the MARCKS (87 kDa) protein, a major specific substrate for protein kinase C, in rat brain. J. Neurosci. 10:1683-1698.
43. Pastural, E., F.J. Barrat, R. Dufourcq-Lagelouse, S. Certain, O. Sanal, N. Jabado, R. Seger, C. Griscelli, A. Fischer, and G. de Saint Basile. 1997. Griscelli disease maps to chromosome 15q21 and is associated with mutations in the myosin-Va gene. Nat. Genet. 16:289-292.
44. 2+-dependent interaction with the synaptobrevin-synaptophysin complex. J. Cell Biol. 137:1589-1601.
45. Pryde, J.G. 1986. Triton X-114: A detergent that has come in from the cold. Trends Biochem. Sci. 11:160-163.
46. Rechsteiner, M., and S.W. Rogers. 1996. PEST sequences and regulation by proteolysis. Trends Biochem. Sci. 21:267-271.
47. Ryan, T.A. 1998. Probing a complex question: when are SNARE proteins ensnared? Nat. Neurosci. 1:175-177.
48. Sanders, G., B. Lichte, H.E. Meyer, and M.W. Kilimann. 1992. cDNA encoding the chicken ortholog of the mouse dilute gene product. FEBS (Fed. Eur. Biochem. Soc.) Lett. 311:295-298.
49. Shupliakov, O., P. Löw, D. Grabs, H. Gad, H. Chen, C. David, K. Takei, P. De Camilli, and L. Brodin. 1997. Synaptic vesicle endocytosis impaired by disruption of dynamin-SH3 domain interactions. Science. 276:259-263.
50. Songyang, Z., K.L. Carraway III, M.J. Eck, S.C. Harrison, R.A. Feldman, M. Mohammadi, J. Schlessinger, S.R. Hubbard, D.P. Smith, C. Eng, et al. 1995. Catalytic specificity of protein tyrosine kinases is critical for selective signalling. Nature. 373:536-539.
51. Songyang, Z., K.P. Lu, Y.T. Kwon, L.-H. Tsai, O. Filhol, C. Cochet, D.A. Brickey, T.R. Soderling, C. Bartleson, et al. 1996. A structural basis for substrate specificities of protein Ser/Thr kinases: primary sequence preference of casein kinases I and II, NIMA, phosphorylase kinase, calmodulin-dependent kinase II, CDK5, and Erk1. Mol. Cell. Biol. 16:6486-6493.
52. Strittmatter, S.M., S.C. Cannon, E.M. Ross, T. Higashijima, and M.C. Fishman. 1993. GAP-43 augments G protein-coupled receptor transduction in Xenopus laevis oocytes. Proc. Natl. Acad. Sci. USA. 90:5327-5331.
53. Strittmatter, S.M., D. Valenzuela, and M.C. Fishman. 1994. An amino-terminal domain of the growth-associated protein GAP-43 mediates its effects on filopodial formation and cell spreading. J. Cell Sci. 107:195-204.
54. Strittmatter, S.M., C. Fankhauser, P.L. Huang, H. Mashimoto, and M.C. Fishman. 1995. Neuronal pathfinding is abnormal in mice lacking the neuronal growth cone protein GAP-43. Cell. 80:445-452.
55. Stumpo, D.J., C.B. Bock, J.S. Tuttle, and P.J. Blackshear. 1995. MARCKS deficiency in mice leads to abnormal brain development and perinatal death. Proc. Natl. Acad. Sci. USA. 92:944-948.
56. Van Lookeren Campagne, M., A.B. Oestreicher, P.M.P. Van Bergen en Henegouwen, and W.H. Gispen. 1990. Ultrastructural double localization of B-50/ GAP43 and synaptophysin (p38) in the neonatal and adult rat hippocampus. J. Neurocytol. 19:948-961.
57. Verhaagen, J., W.T.J.M.C. Hermens, A.B. Oestreicher, W.H. Gispen, S.D. Rabkin, D.W. Pfaff, and M.G. Kaplitt. 1994. Expression of the growth-associated protein B-50/GAP43 via a defective herpes-simplex virus vector results in profound morphological changes in non-neuronal cells. Mol. Brain Res. 26:26-36.
58. Wang, F.-S., J.S. Wolenski, R.E. Cheney, M.S. Mooseker, and D.G. Jay. 1996. Function of myosin-V in filopodial extension of neuronal growth cones. Science. 273:660-663.
59. Wang, X., and M.W. Kilimann. 1997. Identification of two new μ-adaptin-related proteins, μ-ARP1 and μ-ARP2. FEBS (Fed. Eur. Biochem. Soc.) Lett. 402:57-61.
60. Weber, T., B.V. Zemelman, J.A. McNew, B. Westermann, M. Gmachl, F. Parlati, T.H. Söllner, and J.E. Rothman. 1998. SNAREpins: minimal machinery for membrane fusion. Cell. 92:759-772.
61. Widmer, F., and P. Caroni. 1993. Phosphorylation-site mutagenesis of the growth-associated protein GAP-43 modulates its effects on cell spreading and morphology. J. Cell Biol. 120:503-512.
62. Wiederkehr, A., J. Staple, and P. Caroni. 1997. The motility-associated proteins GAP-43, MARCKS, and CAP-23 share unique targeting and surface activity-inducing properties. Exp. Cell Res. 236:103-116.
63. Wüllrich, A., C. Hamacher, A. Schneider, and M.W. Kilimann. 1993. The multiphosphorylation domain of the phosphorylase kinase αM and αL subunits is a hotspot of differential mRNA processing and of molecular evolution. J. Biol. Chem. 268:23208-23214.
64. Yankner, B.A., L.I. Benowitz, L. Villa-Komaroff, and R.L. Neve. 1990. Transfection of PC12 cells with the human GAP-43 gene: effects on neurite outgrowth and regeneration. Mol. Brain Res. 7:39-44.
65. Zuber, M.X., D.W. Goodman, L.R. Karns, and M.C. Fishman. 1989. The neural growth-associated protein GAP-43 induces filopodia in non-neuronal cells. Science. 244:1193-1195.