Cysteine 70 of ankyrin-G is S-palmitoylated and is required for function of ankyrin-G in membrane domain assembly

Journal of Biological Chemistry

Volumn 287, Issue 52, 2012, Pages 43995-44005

  He, Meng ^a   Jenkins, Paul ^a   Bennett, Vann ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANKYRIN; E-CADHERINS; HIPPOCAMPAL NEURONS; MADIN-DARBY CANINE KIDNEY CELLS; MDCK CELLS; MEMBRANE ASSOCIATION; MEMBRANE DOMAIN; PALMITOYLATION; PROTEIN COMPOSITION; SODIUM CHANNEL; SPECTRIN;

ACYLATION; AMINO ACIDS; BIOSYNTHESIS; CELL MEMBRANES; MASS SPECTROMETRY; NEURONS;

MEMBRANES;

ANKYRIN; ANKYRIN G; CYSTEINE; CYSTEINE 70; UNCLASSIFIED DRUG; VOLTAGE GATED SODIUM CHANNEL;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BINDING SITE; BIOGENESIS; BIOSYNTHESIS; CONTROLLED STUDY; EPITHELIUM CELL; HIPPOCAMPUS; IN VITRO STUDY; MASS SPECTROMETRY; MOLECULAR DYNAMICS; MOLECULAR EVOLUTION; MOUSE; MUTAGENESIS; NERVE CELL; NERVE FIBER; NEWBORN; NONHUMAN; PALMITOYLATION; POLARIZATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; WILD TYPE;

AMINO ACID SUBSTITUTION; ANIMALS; ANKYRINS; AXONS; CADHERINS; CAENORHABDITIS ELEGANS; CELL LINE; CYSTEINE; DOGS; DROSOPHILA MELANOGASTER; HIPPOCAMPUS; HUMANS; LIPOYLATION; MEMBRANE MICRODOMAINS; MICE; MUTATION, MISSENSE; NERVE TISSUE PROTEINS; SPECTRIN;

VERTEBRATA;

EID: 84871565497     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.417501     Document Type: Article

References (43)

1. Bennett, V., and Healy, J. (2008) Organizing the fluid membrane bilayer. Diseases linked to spectrin and ankyrin. Trends Mol. Med. 14, 28-36
2. Jenkins, S. M., and Bennett, V. (2001) Ankyrin-G coordinates assembly of the spectrin-based membrane skeleton, voltage-gated sodium channels, and L1 CAMs at Purkinje neuron initial segments. J. Cell Biol. 155, 739-746
3. Zhou, D., Lambert, S., Malen, P. L., Carpenter, S., Boland, L. M., and Bennett, V. (1998) AnkyrinG is required for clustering of voltage-gated Na channels at axon initial segments and for normal action potential firing. J. Cell Biol. 143, 1295-1304 (Pubitemid 28559830)
4. Pan, Z., Kao, T., Horvath, Z., Lemos, J., Sul, J. Y., Cranstoun, S. D., Bennett, V., Scherer, S. S., and Cooper, E. C. (2006) A common ankyrin-G-based mechanism retains KCNQ and NaV channels at electrically active domains of the axon. J. Neurosci. 26, 2599-2613 (Pubitemid 43357843)
5. Hedstrom, K. L., Xu, X., Ogawa, Y., Frischknecht, R., Seidenbecher, C. I., Shrager, P., and Rasband, M. N. (2007) Neurofascin assembles a specialized extracellular matrix at the axon initial segment. J. Cell Biol. 178, 875-886 (Pubitemid 47347370)
6. Hedstrom, K. L., Ogawa, Y., and Rasband, M. N. (2008) AnkyrinG is required for maintenance of the axon initial segment and neuronal polarity. J. Cell Biol. 183, 635-640
7. Sobotzik, J. M., Sie, J. M., Politi, C., Del Turco, D., Bennett, V., Deller, T., and Schultz, C. (2009) AnkyrinG is required to maintain axo-dendritic polarity in vivo. Proc. Natl. Acad. Sci. U.S.A. 106, 17564-17569
8. Kizhatil, K., and Bennett, V. (2004) Lateral membrane biogenesis in human bronchial epithelial cells requires 190-kDa ankyrin-G. J. Biol. Chem. 279, 16706-16714 (Pubitemid 38509373)
9. Kizhatil, K., Baker, S. A., Arshavsky, V. Y., and Bennett, V. (2009) Ankyrin-G promotes cyclic nucleotide-gated channel transport to rod photoreceptor sensory cilia. Science 323, 1614-1617
10. Ayalon, G., Davis, J. Q., Scotland, P. B., and Bennett, V. (2008) An ankyrin-based mechanism for functional organization of dystrophin and dystroglycan. Cell 135, 1189-1200
11. Lowe, J. S., Palygin, O., Bhasin, N., Hund, T. J., Boyden, P. A., Shibata, E., Anderson, M. E., and Mohler, P. J. (2008) Voltage-gated Nav channel targeting in the heart requires an ankyrin-G dependent cellular pathway. J. Cell Biol. 180, 173-186
12. Mohler, P. J., Rivolta, I., Napolitano, C., LeMaillet, G., Lambert, S., Priori, S. G., and Bennett, V. (2004) Nav1.5 E1053K mutation causing Brugada syndrome blocks binding to ankyrin-G and expression of Nav1.5 on the surface of cardiomyocytes. Proc. Natl. Acad. Sci. U.S.A. 101, 17533-17538 (Pubitemid 39657438)
13. Hund, T. J., Koval, O. M., Li, J., Wright, P. J., Qian, L., Snyder, J. S., Gudmundsson, H., Kline, C. F., Davidson, N. P., Cardona, N., Rasband, M. N., Anderson, M. E., and Mohler, P. J. (2010) A β(IV)-spectrin/CaMKII signaling complex is essential for membrane excitability in mice. J. Clin. Invest. 120, 3508-3519
14. Zhang, X., and Bennett, V. (1998) Restriction of 480/270-kD ankyrin G to axon proximal segments requires multiple ankyrin G-specific domains. J. Cell Biol. 142, 1571-1581 (Pubitemid 28452604)
15. Boiko, T., Vakulenko, M., Ewers, H., Yap, C. C., Norden, C., and Winckler, B. (2007) Ankyrin-dependent and -independent mechanisms orchestrate axonal compartmentalization of L1 family members neurofascin and L1/ neuron-glia cell adhesion molecule. J. Neurosci. 27, 590-603 (Pubitemid 46143763)
16. Dzhashiashvili, Y., Zhang, Y., Galinska, J., Lam, I., Grumet, M., and Salzer, J. L. (2007) Nodes of Ranvier and axon initial segments are ankyrin G-dependent domains that assemble by distinct mechanisms. J. Cell Biol. 177, 857-870 (Pubitemid 46873091)
17. Galiano, M. R., Jha, S., Ho, T. S., Zhang, C., Ogawa, Y., Chang, K. J., Stankewich, M. C., Mohler, P. J., and Rasband, M. N. (2012)Adistal axonal cytoskeleton forms an intra-axonal boundary that controls axon initial segment assembly. Cell 149, 1125-1139
18. 2-spectrin collaborate in biogenesis of lateral membrane of human bronchial epithelial cells. J. Biol. Chem. 282, 2029-2037
19. Levental, I., Grzybek, M., and Simons, K. (2010) Greasing their way. Lipid modifications determine protein association with membrane rafts. Biochemistry 49, 6305-6316
20. Bennett, V., and Stenbuck, P. J. (1980) Human erythrocyte ankyrin. Purification and properties. J. Biol. Chem. 255, 2540-2548 (Pubitemid 10036053)
21. Staufenbiel, M. (1987) Ankyrin-bound fatty acid turns over rapidly at the erythrocyte plasma membrane. Mol. Cell Biol. 7, 2981-2984
22. Drisdel, R. C., Alexander, J. K., Sayeed, A., and Green, W. N. (2006) Assays of protein palmitoylation. Methods 40, 127-134 (Pubitemid 44442970)
23. Martinez-Palomo, A., Meza, I., Beaty, G., and Cereijido, M. (1980) Experimental modulation of occluding junctions in a cultured transporting epithelium. J. Cell Biol. 87, 736-745 (Pubitemid 11161805)
24. Siliciano, J. D., and Goodenough, D. A. (1988) Localization of the tight junction protein, ZO-1, is modulated by extracellular calcium and cell-cell contact in Madin-Darby canine kidney epithelial cells. J. Cell Biol. 107, 2389-2399
25. Mattey, D. L., and Garrod, D. R. (1986) Calcium-induced desmosome formation in cultured kidney epithelial cells. J. Cell Sci. 85, 95-111
26. Gumbiner, B., Stevenson, B., and Grimaldi, A. (1988) The role of the cell adhesion molecule uvomorulin in the formation and maintenance of the epithelial junctional complex. J. Cell Biol. 107, 1575-1587
27. 2+-dependent association with sites of cell-cell contact. J. Cell Biol. 109, 557-569
28. Busche, S., Kremmer, E., and Posern, G. (2010) E-cadherin regulates MAL-SRF-mediated transcription in epithelial cells. J. Cell Sci. 123, 2803-2809
29. +)ATPase and implications for the organization of membrane domains in polarized cells. Nature 328, 533-536
30. Salaun, C., Greaves, J., and Chamberlain, L. H. (2010) The intracellular dynamic of protein palmitoylation. J. Cell Biol. 191, 1229-1238
31. Staufenbiel, M. (1988) Fatty acids covalently bound to erythrocyte proteins undergo a differential turnover in vivo. J. Biol. Chem. 263, 13615-13622
32. Peters, L. L., John, K. M., Lu, F. M., Eicher, E. M., Higgins, A., Yialamas, M., Turtzo, L. C., Otsuka, A. J., and Lux, S. E. (1995) Ank3 (epithelial ankyrin), a widely distributed new member of the ankyrin gene family and the major ankyrin in kidney, is expressed in alternatively spliced forms, including forms that lack the repeat domain. J. Cell Biol. 130, 313-330
33. Forrester, M. T., Hess, D. T., Thompson, J. W., Hultman, R., Moseley, M. A., Stamler, J. S., and Casey, P. J. (2011) Site-specific analysis of protein S-acylation by resin-assisted capture. J. Lipid Res. 52, 393-398
34. Jennings, B. C., and Linder, M. E. (2012)DHHCprotein S-acyltransferases use similar ping-pong kinetic mechanisms but display different acyl-CoA specificities. J. Biol. Chem. 287, 7236-7245
35. Kizhatil, K., Davis, J. Q., Davis, L., Hoffman, J., Hogan, B. L., and Bennett, V. (2007) Ankyrin-G is a molecular partner of E-cadherin in epithelial cells and early embryos. J. Biol. Chem. 282, 26552-26561 (Pubitemid 47443799)
36. Henis, Y. I., Rotblat, B., and Kloog, Y. (2006) FRAP beam-size analysis to measure palmitoylation-dependent membrane association dynamics and microdomain partitioning of Ras proteins. Methods 40, 183-190 (Pubitemid 44442976)
37. Kordeli, E., Lambert, S., and Bennett, V. (1995) AnkyrinG. A new ankyrin gene with neural-specific isoforms localized at the axonal initial segment and node of Ranvier. J. Biol. Chem. 270, 2352-2359
38. Greaves, J., and Chamberlain, L. H. (2010) S-acylation by the DHHC protein family. Biochem. Soc. Trans. 38, 522-524
39. Aicart-Ramos, C., Valero, R. A., and Rodriguez-Crespo, I. (2011) Protein palmitoylation and subcellular trafficking. Biochim. Biophys. Acta 1808, 2981-2994
40. Delint-Ramirez, I., Willoughby, D., Hammond, G. V., Ayling, L. J., and Cooper, D. M. (2011) Palmitoylation targets AKAP79 protein to lipid rafts and promotes its regulation of calcium-sensitive adenylyl cyclase type 8. J. Biol. Chem. 286, 32962-32975
41. Linder, M. E., and Deschenes, R. J. (2007) Palmitoylation. Policing protein stability and traffic. Nat. Rev. Mol. Cell Biol. 8, 74-84 (Pubitemid 46012016)
42. Fragoso, R., Ren, D., Zhang, X., Su, M. W., Burakoff, S. J., and Jin, Y. J. (2003) Lipid raft distribution of CD4 depends on its palmitoylation and association with Lck and evidence for CD4-induced lipid raft aggregation as an additional mechanism to enhance CD3 signaling. J. Immunol. 170, 913-921 (Pubitemid 36070545)
43. Ren, Q., and Bennett, V. (1998) Palmitoylation of neurofascin at a site in the membrane-spanning domain highly conserved among the L1 family of cell adhesion molecules. J. Neurochem. 70, 1839-1849 (Pubitemid 28207805)