Efficient ADAM22 surface expression is mediated by phosphorylation-dependent interaction with 14-3-3 protein family members

Journal of Cell Science

Volumn 119, Issue 16, 2006, Pages 3296-3305

  Gödde, Nathan J ^a   D'Abaco, Giovanna M ^b   Paradiso, Lucy ^a   Novak, Ulrike ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b ROYAL MELBOURNE HOSPITAL   (Australia)

Author keywords

14 3 3 protein; ADAM22 protein; Adhesion; Diarginine retention; Forward transport; Membrane localization

Indexed keywords

MEMBRANE PROTEIN; PROTEIN 14 3 3; PROTEIN ADAM22; SERINE; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; BRAIN; CELL SURFACE; CONTROLLED STUDY; CYTOPLASM; ENDOPLASMIC RETICULUM; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MUTANT; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; TISSUE DISTRIBUTION;

14-3-3 PROTEINS; ADAM PROTEINS; BINDING SITES; BRAIN; CELLS, CULTURED; ENDOPLASMIC RETICULUM; GLIOMA; HUMANS; IMMUNOPRECIPITATION; KIDNEY; NERVE TISSUE PROTEINS; PHOSPHORYLATION; POINT MUTATION; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 33748800249     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.03065     Document Type: Article

References (85)

1. Abram, C. L., Seals, D. F., Pass, I., Salinsky, D., Maurer, L., Roth, T. M. and Courtneidge, S. A. (2003). The adaptor protein fish associates with members of the ADAMS family and localizes to podosomes of Src-transformed cells. J. Biol. Chem. 278, 16844-16851.
2. Argraves, W. S., Pytela, R., Suzuki, S., Milian, J. L., Pierschbacher, M. D. and Ruoslahti, E. (1986). cDNA sequences from the alpha subunit of the fibronectin receptor predict a transmembrane domain and a short cytoplasmic peptide. J. Biol. Chem. 261, 12922-12924.
3. Blobel, C. P. (2005). ADAMS: key components in EGFR signalling and development. Nat. Rev. Mol. Cell Biol. 6, 32-43.
4. Boston, P. F., Jackson, P. and Thompson, R. J. (1982). Human 14-3-3 protein: radioimmunoassay, tissue distribution, and cerebrospinal fluid levels in patients with neurological disorders. J. Neurochem. 38, 1475-1482.
5. Braselmann, S. and McCormick, F. (1995). Bcr and Raf form a complex in vivo via 14-3-3 proteins. EMBO J. 14, 4839-4848.
6. Campbell, J. K., Gurung, R., Romero, S., Speed, C. J., Andrews, R. K., Berndt, M. C. and Mitchell, C. A. (1997). Activation of the 43 kDa inositol polyphosphate 5-phosphatase by 14-3-3zeta. Biochemistry 36, 15363-15370.
7. Chaudhri, M., Scarabel, M. and Aitken, A. (2003). Mammalian and yeast 14-3-3 isoforms form distinct patterns of dimers in vivo. Biochem. Biophys. Res. Commun. 300, 679-685.
8. Chen, H. K., Fernandez-Funez, P., Acevedo, S. F., Lam, Y. C., Kaytor, M. D., Fernandez, M. H., Aitken, A., Skoulakis, E. M, Orr, H. T., Botas, J. et al. (2003). Interaction of Akt-phosphorylated ataxin-1 with 14-3-3 mediates neurodegeneration in spinocerebellar ataxia type 1. Cell 113, 457-468.
9. Coblitz, B., Shikano, S., Wu, M., Gabelli, S. B., Cockrell, L. M., Spieker, M., Hanyu, Y., Fu, H., Amzel, L. M. and Li, M. (2005). C-terminal recognition by 14-3-3 proteins for surface expression of membrane receptors. J. Biol. Chem. 280, 36263-36272.
10. Cousin, H., Gaultier, A., Bleux, C., Darribere, T. and Alfandari, D. (2000). PACSIN2 is a regulator of the metalloprotease/disintegrin ADAM13. Dev. Biol. 227, 197-210.
11. D'Abaco, G. M., Ng, K., Paradiso, L., Godde, N. J., Kaye, A. and Novak, U. (2006). ADAM22, expressed in normal brain but not in high-grade gliomas, inhibits cellular proliferation via the disintegrin domain. Neurosurgery 58, 179-186.
12. Davezac, N., Baldin, V., Gabrielli, B., Forrest, A., Theis-Febvre, N., Yashida, M. and Ducommun, B. (2000). Regulation of CDC25B phosphatases subcellular localization. Oncogene 19, 2179-2185.
13. Dumaz, N. and Marais, R. (2003). Protein kinase A blocks Raf-1 activity by stimulating 14-3-3 binding and blocking Raf-1 interaction with Ras. J. Biol. Chem. 278, 29819-29823.
14. Evans, J. P. (2001). Fertilin beta and other ADAMS as integrin ligands: insights into cell adhesion and fertilization. BioEssays 23, 628-639.
15. Foucault, I., Liu, Y. C., Bernard, A. and Deckert, M. (2003). The chaperone protein 14-3-3 interacts with 3BP2/SH3BP2 and regulates its adapter function. J. Biol. Chem. 278, 7146-7153.
16. Fu, H., Subramanian, R. R. and Masters, S. C. (2000). 14-3-3 proteins: structure, function, and regulation. Annu. Rev. Pharmacol. Toxicol. 40, 617-647.
17. Gulliano, M. F., Huet, C., Frygelius, J., Polgren, A., Wewer, U. M. and Engvall, E. (2000). Binding of ADAM12, a marker of skeletal muscle regeneration, to the muscle-specific actin-binding protein, alpha-actinin-2, is required for myoblast fusion. J. Biol. Chem. 275, 13933-13939.
18. Garcia-Guzman, M., Dolfi, F., Russello, M. and Vuori, K. (1999). Cell adhesion regulates the interaction between the docking protein p130(Cas) and the 14-3-3 proteins. J. Biol. Chem. 274, 5762-5768.
19. Gilpin, B. J., Loechel, F., Mattei, M. G., Engvall, E., Albrechtsen, R. and Wewer, U. M. (1998). A novel, secreted form of human ADAM 12 (meltrin alpha) provokes myogenesis in vivo. J. Biol. Chem. 273, 157-166.
20. Han, D. C., Rodriguez, L. G. and Guan, J. L. (2001). Identification of a novel interaction between integrin beta1 and 14-3-3beta. Oncogene 20, 346-357.
21. Harada, T., Nishie, A., Torigoe, K., Ikezaki, K., Shono, T., Maehara, Y., Kuwano, M. and Wada, M. (2000). The specific expression of three novel splice variant forms of human metalloprotease-like disintegrin-like cysteine-rich protein 2 gene in brain tissues and gliomas. Jpn. J. Cancer Res. 91, 1001-1006.
22. Hermeking, H. (2003). The 14-3-3 cancer connection. Nat. Rev. Cancer 3, 931-943.
23. Huang, L., Feng, L., Yang, L., Zhou, W., Zhao, S. and Li, C. (2002). Screen and identification of proteins interacting with ADAM19 cytoplasmic tail. Mol. Biol. Rep. 29, 317-323.
24. Izumi, Y., Hirata, M., Hasuwa, H., Iwamoto, R., Umata, T., Miyado, K., Tamai, Y., Kurisaki, T., Sehara-Fujisawa, A., Ohno, S. et al. (1998). A metalloprotease-disintegrin, MDC9/meltrin-gamma/ADAM9 and PKCdelta are involved in TPA-induced ectodomain shedding of membrane-anchored heparin-binding EGF-like growth factor. EMBO J. 17, 7260-7272.
25. Jeanclos, E. M., Lin, L., Treuil, M. W., Rao, J., DeCoster, M. A. and Anand, R. (2001). The chaperone protein 14-3-3eta interacts with the nicotinic acetylcholine receptor alpha 4 subunit. Evidence for a dynamic role in subunit stabilization. J. Biol. Chem. 276, 28281-28290.
26. Jones, D. H., Ley, S. and Aitken, A. (1995). Isoforms of 14-3-3 protein can form homo- and heterodimers in vivo and in vitro: implications for function as adapter proteins. FEBS Lett. 368, 55-58.
27. Jongeneel, C. V., Bouvier, J. and Bairoch, A. (1989). A unique signature identifies a family of zinc-dependent metallopeptidases. FEBS Lett. 242, 211-214.
28. Kovacina, K. S., Park, G. Y., Bae, S. S., Guzzetta, A. W., Schaefer, E., Birnbaum, M. J. and Roth, R. A. (2003). Identification of a proline-rich Akt substrate as a 14-3-3 binding partner. J. Biol. Chem. 278, 10189-10194.
29. Layfield, R., Fergusson, J., Aitken, A., Lowe, J., Landon, M. and Mayer, R. J. (1996). Neurofibrillary tangles of Alzheimer's disease brains contain 14-3-3 proteins. Neurosci. Lett. 209, 57-60.
30. Li, E., Brown, S. L., Stupack, D. G., Puente, X. S., Cheresh, D. A. and Nemerow, G. R. (2001). Integrin alpha(v)beta1 is an adenovirus coreceptor. J. Virol. 75, 5405-5409.
31. Liu, M. Y., Cai, S., Espejo, A., Bedford, M. T. and Walker, C. L. (2002). 14-3-3 interacts with the tumor suppressor tuberin at Akt phosphorylation site(s). Cancer Res. 62, 6475-6480.
32. Lock, P., Abram, C. L., Gibson, T. and Courtneidge, S. A. (1998). A new method for isolating tyrosine kinase substrates used to identify fish, an SH3 and PX domain-containing protein, and Src substrate. EMBO J. 17, 4346-4357.
33. Loechel, F., Overgaard, M. T., Oxvig, C., Albrechtsen, R. and Wewer, U. M. (1999). Regulation of human ADAM 12 protease by the prodomain. Evidence for a functional cysteine switch. J. Biol. Chem. 274, 13427-13433.
34. Lum, L., Reid, M. S. and Blobel, C. P. (1998). Intracellular maturation of the mouse metalloprotease disintegrin MDC15. J. Biol. Chem. 273, 26236-26247.
35. Mackintosh, C. (2004). Dynamic interactions between 14-3-3 proteins and phosphoproteins regulate diverse cellular processes. Biochem. J. 381, 329-342.
36. Mahimkar, R. M., Visaya, O., Pollock, A. S. and Lovett, D. H. (2005). The disintegrin domain of ADAM9: a ligand for multiple beta1 renal integrins. Biochem. J. 385, 461-468.
37. Masters, S. C., Pederson, K. J., Zhang, L., Barbieri, J. T. and Fu, H. (1999). Interaction of 14-3-3 with a nonphosphorylated protein ligand, exoenzyme S of Pseudomonas aeruginosa. Biochemistry 38, 5216-5221.
38. Milla, M. E., Leesnitzer, M. A., Moss, M. L., Clay, W. C., Carter, H. L., Miller, A. B., Su, J. L., Lambert, M. H., Willard, D. H., Sheeley, D. M. et al. (1999). Specific sequence elements are required for the expression of functional tumor necrosis factor-alpha-converting enzyme (TACE). J. Biol. Chem. 274, 30563-30570.
39. Mori, S., Tanaka, M., Nanba, D., Nishiwaki, E., Ishiguro, H., Higashiyama, S. and Matsuura, N. (2003). PACSIN3 binds ADAM12/meltrin alpha and up-regulates ectodomain shedding of heparin-binding epidermal growth factor-like growth factor. J. Biol. Chem. 278, 46029-46034.
40. Muslin, A. J. and Xing, H. (2000). 14-3-3 proteins: regulation of subcellular localization by molecular interference. Cell Signal. 12, 703-709.
41. Muslin, A. J., Tanner, J. W., Allen, P. M. and Shaw, A. S. (1996). Interaction of 14-3-3 with signaling proteins is mediated by the recognition of phosphoserine. Cell 84, 889-897.
42. Nelson, K. K., Schlondorff, J. and Blobel, C. P. (1999). Evidence for an interaction of the metalloprotease-disintegrin tumour necrosis factor alpha convertase (TACE) with mitotic arrest deficient 2 (MAD2), and of the metalloprotease-disintegrin MDC9 with a novel MAD2-related protein, MAD2beta. Biochem. J. 343, 673-680.
43. Novak, U. (2004). ADAM proteins in the brain. J. Clin. Neurosci. 11, 227-235.
44. Nufer, O. and Hauri, H. P. (2003). ER export: call 14-3-3. Curr. Biol. 13, R391-R393.
45. Obsil, T., Ghirlando, R., Anderson, D. E., Hickman, A. B. and Dyda, F. (2003). Two 14-3-3 binding motifs are required for stable association of Forkhead transcription factor FOXO4 with 14-3-3 proteins and inhibition of DNA binding. Biochemistry 42, 15264-15272.
46. O'Kelly, I., Butler, M. H., Zilberberg, N. and Goldstein, S. A. (2002). Forward transport. 14-3-3 binding overcomes retention in endoplasmic reticulum by dibasic signals. Cell 111, 577-588.
47. Pan, D. and Rubin, G. M. (1997). Kuzbanian controls proteolytic processing of Notch and mediates lateral inhibition during Drosophila and vertebrate neurogenesis. Cell 90, 271-280.
48. Peng, C. Y., Graves, P. R., Thoma, R. S., Wu, Z., Shaw, A. S. and Piwnica-Worms, H. (1997). Mitotic and G2 checkpoint control: regulation of 14-3-3 protein binding by phosphorylation of Cdc25C on serine-216. Science 277, 1501-1505.
49. Poghosyan, Z., Robbins, S. M., Houslay, M. D., Webster, A., Murphy, G. and Edwards, D. R. (2002). Phosphorylation-dependent interactions between ADAM15 cytoplasmic domain and Src family protein-tyrosine kinases. J. Biol. Chem. 277, 4999-5007.
50. Poindexter, K., Nelson, N., DuBose, R. F., Black, R. A. and Cerretti, D. P. (1999). The identification of seven metalloproteinase-disintegrin (ADAM) genes from genomic libraries. Gene 237, 61-70.
51. Pozuelo Rubio, M., Geraghty, K. M., Wong, B. H., Wood, N. T., Campbell, D. G., Morrice, N. and Mackintosh, C. (2004). 14-3-3-affinity purification of over 200 human phosphoproteins reveals new links to regulation of cellular metabolism, proliferation and trafficking. Biochem. J. 379, 395-408.
52. Prasad, G. L., Valverius, E. M., McDuffie, E. and Cooper, H. L. (1992). Complementary DNA cloning of a novel epithelial cell marker protein, HME1, that may be down-regulated in neoplastic mammary cells. Cell Growth Differ. 3, 507-513.
53. Primakoff, P., Hyatt, H. and Tredick-Kline, J. (1987). Identification and purification of a sperm surface protein with a potential role in sperm-egg membrane fusion. J. Cell Biol. 104, 141-149.
54. Pytela, R., Pierschbacher, M. D. and Ruoslahti, E. (1985). Identification and isolation of a 140 kd cell surface glycoprotein with properties expected of a fibronectin receptor. Cell 40, 191-198.
55. Rosner, M. and Hengstschlager, M. (2006). 14-3-3 proteins are involved in the regulation of mammalian cell proliferation. Amino Acids 30, 105-109.
56. Sagane, K., Ohya, Y., Hasegawa, Y. and Tanaka, I. (1998). Metalloproteinase-like, disintegrin-like, cysteine-rich proteins MDC2 and MDC3: novel human cellular disintegrins highly expressed in the brain. Biochem. J. 334, 93-98.
57. Sagane, K., Hayakawa, K., Kai, J., Hirohashi, T., Takahashi, E., Miyamoto, N., Ino, M., Oki, T., Yamazaki, K. and Nagasu, T. (2005). Ataxia and peripheral nerve hypomyelination in ADAM22-deficient mice. BMC Neurosci. 6, 33.
58. Santoro, M. M., Gaudino, G. and Marchisio, P. C. (2003). The MSP receptor regulates alpha6beta4 and alpha3beta1 integrins via 14-3-3 proteins in keratinocyte migration. Dev. Cell 5, 257-271.
59. Shikano, S., Coblitz, B., Sun, H. and Li, M. (2005). Genetic isolation of transport signals directing cell surface expression. Nat. Cell Biol. 7, 985-992.
60. Sotillos, S., Roch, F. and Campuzano, S. (1997). The metalloprotease-disintegrin Kuzbanian participates in Notch activation during growth and patterning of Drosophila imaginal discs. Development 124, 4769-4779.
61. Stocker, W., Grams, F., Baumann, U., Reinemer, P. Gomis-Ruth, F. X., McKay, D. B. and Bode, W. (1995). The metzincins-topological and sequential relations between the astacins, adamalysins, serralysins, and matrixins (collagenases) define a superfamily of zinc-peptidases. Protein Sci. 4, 823-840.
62. Sugiyama, A., Miyagi, Y., Komiya, Y., Kurabe, N., Kitanaka, C., Kato, N., Nagashima, Y., Kuchino, Y. and Tashiro, F. (2003). Forced expression of antisense 14-3-3beta RNA suppresses tumor cell growth in vitro and in vivo. Carcinogenesis 24, 1549-1559.
63. Sundberg, C., Thodeti, C. K., Kveiborg, M., Larsson, C., Parker, P., Albrechtsen, R. and Wewer, U. M. (2004). Regulation of ADAM12 cell-surface expression by protein kinase C epsilon. J. Biol. Chem. 279, 51601-51611.
64. Tanaka, M., Nanba, D., Mori, S., Shiba, F., Ishiguro, H., Yoshino, K., Matsuura, N. and Higashiyama, S. (2004). ADAM binding protein Eve-1 is required for ectodomain shedding of epidermal growth factor receptor ligands. J. Biol. Chem. 279, 41950-41959.
65. Toyo-oka, K., Shionoya, A., Gambello, M. J., Cardoso, C., Leventer, R., Ward, H. L., Ayala, R., Tsai, L. H., Dobyns, W., Ledbetter, D. et al. (2003). 14-3-3epsilon is important for neuronal migration by binding to NUDEL: a molecular explanation for Miller-Dieker syndrome. Nat. Genet. 34, 274-285.
66. Ubl, A., Berg, D., Holzmann, C., Kruger, R., Berger, K., Arzberger, T., Bornemann, A. and Riess, O. (2002). 14-3-3 protein is a component of Lewy bodies in Parkinson's disease-mutation analysis and association studies of 14-3-3 eta. Brain Res. Mol. Brain Res. 108, 33-39.
67. Van Der Hoeven, P. C., Van Der Wal, J. C., Ruurs, P. and Van Blitterswijk, W. J. (2000). Protein kinase C activation by acidic proteins including 14-3-3. Biochem. J. 347, 781-785.
68. Vincenz, C. and Dixit, V. M. (1996). 14-3-3 proteins associate with A20 in an isoform-specific manner and function both as chaperone and adapter molecules. J. Biol. Chem. 271, 20029-20034.
69. Wang, B., Yang, H., Liu, Y. C., Jelinek, T., Zhang, L., Ruoslahti, E. and Fu, H. (1999). Isolation of high-affinity peptide antagonists of 14-3-3 proteins by phage display. Biochemistry 38, 12499-12504.
70. Wang, B., Liu, K., Lin, F. T. and Lin, W. C. (2004). A role for 14-3-3 tau in E2F1 stabilization and DNA damage-induced apoptosis. J. Biol. Chem. 279, 54140-54152.
71. Waterman, M. J., Stavridi, E. S., Waterman, J. L. and Halazonetis, T. D. (1998). ATM-dependent activation of p53 involves dephosphorylation and association with 14-3-3 proteins. Nat. Genet. 19, 175-178.
72. White, J. M. (2003). ADAMs: modulators of cell-cell and cell-matrix interactions. Curr. Opin. Cell Biol. 15, 598-606.
73. Wolfsberg, T. G., Straight, P. D., Gerena, R. L., Huovila, A. P., Primakoff, P., Myles, D. G. and White, J. M. (1995). ADAM, a widely distributed and developmentally regulated gene family encoding membrane proteins with a disintegrin and metalloprotease domain. Dev. Biol. 169, 378-383.
74. Yaffe, M. B. (2002). How do 14-3-3 proteins work? - Gatekeeper phosphorylation and the molecular anvil hypothesis. FEBS Lett. 513, 53-57.
75. Yaffe, M. B., Rittinger, K., Volinia, S., Caron, P. R., Aitken, A., Leffers, H., Gamblin, S. J., Smerdon, S. J. and Cantley, L. C. (1997). The structural basis for 14-3-3:phosphopeptide binding specificity. Cell 91, 961-971.
76. Yagami-Hiromasa, T., Sato, T., Kurisaki, T., Kamijo, K., Nabeshima, Y. and Fujisawa-Sehara, A. (1995). A metalloprotease-disintegrin participating in myoblast fusion. Nature 377, 652-656.
77. Yang, P., Baker, K. A. and Hagg, T. (2005). A disintegrin and metalloprotease 21 (ADAM21) is associated with neurogenesis and axonal growth in developing and adult rodent CNS. J. Comp. Neurol. 490, 163-179.
78. Yuan, H., Michelsen, K. and Schwappach, B. (2003). 14-3-3 dimers probe the assembly status of multimeric membrane proteins. Curr. Biol. 13, 638-646.
79. Zeng, Y., Forbes, K. C., Wu, Z., Moreno, S., Piwnica-Worms, H. and Enoch, T. (1998). Replication checkpoint requires phosphorylation of the phosphatase Cdc25 by Cds1 or Chk1. Nature 395, 507-510.
80. Zha, J., Harada, H., Yang, E., Jockel, J. and Korsmeyer, S. J. (1996). Serine phosphorylation of death agonist BAD in response to survival factor results in binding to 14-3-3 not BCL-X(L). Cell 87, 619-628.
81. Zhai, J., Lin, H., Shamim, M., Schlaepfer, W. W. and Canete-Soler, R. (2001). Identification of a novel interaction of 14-3-3 with p190RhoGEF. J. Biol. Chem. 276, 41318-41324.
82. Zheng, W., Schwarzer, D., Lebeau, A., Weller, J. L., Klein, D. C. and Cole, P. A. (2005). Cellular stability of serotonin N-acetyltransferase conferred by phosphonodifluoromethylene alanine (Pfa) substitution for Ser-205. J. Biol. Chem. 280, 10462-10467.
83. Zheng, Y., Schlondorff, J. and Blobel, C. P. (2002). Evidence for regulation of the tumor necrosis factor alpha-convertase (TACE) by protein-tyrosine phosphatase PTPH1. J. Biol. Chem. 277, 42463-42470.
84. Zhu, P., Sum, Y., Xu, R., Sang, Y., Zhao, J., Liu, G., Cai, L., Li, C. and Zhao, S. (2003). The interaction between ADAM 22 and 14-3-3zeta: regulation of cell adhesion and spreading. Biochem. Biophys. Res. Commun. 301, 991-999.
85. Zhu, P., Sang, Y., Xu, H., Zhao, J., Xu, R., Sun, Y., Xu, T., Wang, X., Chen, L., Feng, H. et al. (2005). ADAM22 plays an important role in cell adhesion and spreading with the assistance of 14-3-3. Biochem. Biophys. Res. Commun. 331, 938-946.