Crystal structure of an inactive Akt2 kinase domain

Structure

Volumn 11, Issue 1, 2003, Pages 21-30

  Huang, Xin ^a   Begley, Michael ^a,b   Morgenstern, Kurt A ^a   Gu, Yan ^a   Rose, Paul ^a   Zhao, Huilin ^a   Zhu, Xiaotian ^a  

^a AMGEN INC   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

AGC serine threonine kinase; Akt PKB; Kinase domain; Signal transduction; Tumorigenesis; X ray crystal structure

Indexed keywords

ADENOSINE TRIPHOSPHATE; CYSTEINE; ISOPROTEIN; PEPTIDE; PROTEIN KINASE B; PROTEIN KINASE B BETA; PROTEIN SERINE KINASE; THREONINE PROTEINASE; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BINDING SITE; CANCER; CARBOXY TERMINAL SEQUENCE; CELL SURVIVAL; CONTROLLED STUDY; CRYSTAL STRUCTURE; DISULFIDE BOND; ENZYME STRUCTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FAMILY;

ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; BINDING SITES; CYCLIC AMP-DEPENDENT PROTEIN KINASES; HUMANS; LIGANDS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; SEQUENCE ALIGNMENT;

ANIMALIA;

EID: 0037229885     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0969-2126(02)00937-1     Document Type: Article

References (68)

1. Bellacosa A., Testa J.R., Staal S.P., Tsichlis P.N. A retroviral oncogene, akt, encoding a serine-threonine kinase containing an SH2-like region. Science. 254:1991;274-277.
2. Coffer P.J., Woodgett J.R. Molecular cloning and characterisation of a novel putative protein- serine kinase related to the cAMP-dependent and protein kinase C families. Eur. J. Biochem. 201:1991;475-481.
3. Jones P.F., Jakubowicz T., Pitossi F.J., Maurer F., Hemmings B.A. Molecular cloning and identification of a serine/threonine protein kinase of the second-messenger subfamily. Proc. Natl. Acad. Sci. USA. 88:1991;4171-4175.
4. Staal S.P., Hartley J.W., Rowe W.P. Isolation of transforming murine leukemia viruses from mice with a high incidence of spontaneous lymphoma. Proc. Natl. Acad. Sci. USA. 74:1977;3065-3067.
5. Staal S.P. Molecular cloning of the akt oncogene and its human homologues AKT1 and AKT2. amplification of AKT1 in a primary human gastric adenocarcinoma Proc. Natl. Acad. Sci. USA. 84:1987;5034-5037.
6. Hanks S.K., Hunter T. Protein kinases 6. The eukaryotic protein kinase superfamily. kinase (catalytic) domain structure and classification FASEB J. 9:1995;576-596.
7. Datta K., Bellacosa A., Chan T.O., Tsichlis P.N. Akt is a direct target of the phosphatidylinositol 3-kinase. Activation by growth factors, v-src and v-Ha-ras, in Sf9 and mammalian cells. J. Biol. Chem. 271:1996;30835-30839.
8. Jiang B.H., Aoki M., Zheng J.Z., Li J., Vogt P.K. Myogenic signaling of phosphatidylinositol 3-kinase requires the serine-threonine kinase Akt/protein kinase B. Proc. Natl. Acad. Sci. USA. 96:1999;2077-2081.
9. Coffer P.J., Jin J., Woodgett J.R. Protein kinase B (c-Akt). a multifunctional mediator of phosphatidylinositol 3-kinase activation Biochem. J. 335:1998;1-13.
10. Chan T.O., Rittenhouse S.E., Tsichlis P.N. AKT/PKB and other D3 phosphoinositide-regulated kinases. kinase activation by phosphoinositide-dependent phosphorylation Annu. Rev. Biochem. 68:1999;965-1014.
11. Jones P.F., Jakubowicz T., Hemmings B.A. Molecular cloning of a second form of rac protein kinase. Cell Regul. 2:1991;1001-1009.
12. Nakatani K., Sakaue H., Thompson D.A., Weigel R.J., Roth R.A. Identification of a human Akt3 (protein kinase B gamma) which contains the regulatory serine phosphorylation site. Biochem. Biophys. Res. Commun. 257:1999;906-910.
13. Alessi D.R., Cohen P. Mechanism of activation and function of protein kinase B. Curr. Opin. Genet. Dev. 8:1998;55-62.
14. Cho H., Thorvaldsen J.L., Chu Q., Feng F., Birnbaum M.J. Akt1/pkbalpha is required for normal growth but dispensable for maintenance of glucose homeostasis in mice. J. Biol. Chem. 276:2001;38349-38352.
15. Chen W.S., Xu P.Z., Gottlob K., Chen M.L., Sokol K., Shiyanova T., Roninson I., Weng W., Suzuki R., Tobe K.et al. Growth retardation and increased apoptosis in mice with homozygous disruption of the Akt1 gene. Genes Dev. 15:2001;2203-2208.
16. Cho H., Mu J., Kim J.K., Thorvaldsen J.L., Chu Q., Crenshaw E.B. III, Kaestner K.H., Bartolomei M.S., Shulman G.I., Birnbaum M.J. Insulin resistance and a diabetes mellitus-like syndrome in mice lacking the protein kinase Akt2 (PKB beta). Science. 292:2001;1728-1731.
17. Ahmad S., Singh N., Glazer R.I. Role of AKT1 in 17beta-estradiol- and insulin-like growth factor I (IGF- I)-dependent proliferation and prevention of apoptosis in MCF-7 breast carcinoma cells. Biochem. Pharmacol. 58:1999;425-430.
18. Klippel A., Kavanaugh W.M., Pot D., Williams L.T. A specific product of phosphatidylinositol 3-kinase directly activates the protein kinase Akt through its pleckstrin homology domain. Mol. Cell. Biol. 17:1997;338-344.
19. Stokoe D., Stephens L.R., Copeland T., Gaffney P.R., Reese C.B., Painter G.F., Holmes A.B., McCormick F., Hawkins P.T. Dual role of phosphatidylinositol-3,4,5-trisphosphate in the activation of protein kinase B. Science. 277:1997;567-570.
20. Steck P.A., Pershouse M.A., Jasser S.A., Yung W.K., Lin H., Ligon A.H., Langford L.A., Baumgard M.L., Hattier T., Davis T.et al. Identification of a candidate tumour suppressor gene, MMAC1, at chromosome 10q23.3 that is mutated in multiple advanced cancers. Nat. Genet. 15:1997;356-362.
21. Marte B.M., Downward J. PKB/Akt. connecting phosphoinositide 3-kinase to cell survival and beyond Trends Biochem. Sci. 22:1997;355-358.
22. Frech M., Andjelkovic M., Ingley E., Reddy K.K., Falck J.R., Hemmings B.A. High affinity binding of inositol phosphates and phosphoinositides to the pleckstrin homology domain of RAC/protein kinase B and their influence on kinase activity. J. Biol. Chem. 272:1997;8474-8481.
23. Franke T.F., Kaplan D.R., Cantley L.C., Toker A. Direct regulation of the Akt proto-oncogene product by phosphatidylinositol-3,4-bisphosphate. Science. 275:1997;665-668.
24. Meier R., Hemmings B.A. Regulation of protein kinase B. J. Recept. Signal Transduct. Res. 19:1999;121-128.
25. Vanhaesebroeck B., Alessi D.R. The PI3K-PDK1 connection. more than just a road to PKB Biochem. J. 346:2000;561-576.
26. Alessi D.R., Deak M., Casamayor A., Caudwell F.B., Morrice N., Norman D.G., Gaffney P., Reese C.B., MacDougall C.N., Harbison D.et al. 3-phosphoinositide-dependent protein kinase-1 (PDK1). structural and functional homology with the Drosophila DSTPK61 kinase Curr. Biol. 7:1997;776-789.
27. Stephens L., Anderson K., Stokoe D., Erdjument-Bromage H., Painter G.F., Holmes A.B., Gaffney P.R., Reese C.B., McCormick F., Tempst P.et al. Protein kinase B kinases that mediate phosphatidylinositol 3,4,5-trisphosphate-dependent activation of protein kinase B. Science. 279:1998;710-714.
28. Alessi D.R., James S.R., Downes C.P., Holmes A.B., Gaffney P.R., Reese C.B., Cohen P. Characterization of a 3-phosphoinositide-dependent protein kinase which phosphorylates and activates protein kinase Balpha. Curr. Biol. 7:1997;261-269.
29. Toker A., Newton A.C. Akt/protein kinase B is regulated by autophosphorylation at the hypothetical PDK-2 site. J. Biol. Chem. 275:2000;8271-8274.
30. Balendran A., Casamayor A., Deak M., Paterson A., Gaffney P., Currie R., Downes C.P., Alessi D.R. PDK1 acquires PDK2 activity in the presence of a synthetic peptide derived from the carboxyl terminus of PRK2. Curr. Biol. 9:1999;393-404.
31. Persad S., Attwell S., Gray V., Delcommenne M., Troussard A., Sanghera J., Dedhar S. Inhibition of integrin-linked kinase (ILK) suppresses activation of protein kinase B/Akt and induces cell cycle arrest and apoptosis of PTEN-mutant prostate cancer cells. Proc. Natl. Acad. Sci. USA. 97:2000;3207-3212.
32. Rane M.J., Coxon P.Y., Powell D.W., Webster R., Klein J.B., Pierce W., Ping P., McLeish K.R. p38 Kinase-dependent MAPKAPK-2 activation functions as 3-phosphoinositide-dependent kinase-2 for Akt in human neutrophils. J. Biol. Chem. 276:2001;3517-3523.
33. Vazquez F., Sellers W.R. The PTEN tumor suppressor protein. an antagonist of phosphoinositide 3-kinase signaling Biochim. Biophys. Acta. 1470:2000;M21-M35.
34. Cantley L.C., Neel B.G. New insights into tumor suppression. PTEN suppresses tumor formation by restraining the phosphoinositide 3-kinase/AKT pathway Proc. Natl. Acad. Sci. USA. 96:1999;4240-4245.
35. Li J., Yen C., Liaw D., Podsypanina K., Bose S., Wang S.I., Puc J., Miliaresis C., Rodgers L., McCombie R.et al. PTEN, a putative protein tyrosine phosphatase gene mutated in human brain, breast, and prostate cancer. Science. 275:1997;1943-1947.
36. Teng D.H., Hu R., Lin H., Davis T., Iliev D., Frye C., Swedlund B., Hansen K.L., Vinson V.L., Gumpper K.L.et al. MMAC1/PTEN mutations in primary tumor specimens and tumor cell lines. Cancer Res. 57:1997;5221-5225.
37. Aoki M., Batista O., Bellacosa A., Tsichlis P., Vogt P.K. The akt kinase. molecular determinants of oncogenicity Proc. Natl. Acad. Sci. USA. 95:1998;14950-14955.
38. Bellacosa A., de Feo D., Godwin A.K., Bell D.W., Cheng J.Q., Altomare D.A., Wan M., Dubeau L., Scambia G., Masciullo V.et al. Molecular alterations of the AKT2 oncogene in ovarian and breast carcinomas. Int. J. Cancer. 64:1995;280-285.
39. Czech M.P. PIP2 and PIP3. complex roles at the cell surface Cell. 100:2000;603-606.
40. Nakatani K., Thompson D.A., Barthel A., Sakaue H., Liu W., Weigel R.J., Roth R.A. Up-regulation of Akt3 in estrogen receptor-deficient breast cancers and androgen-independent prostate cancer lines. J. Biol. Chem. 274:1999;21528-21532.
41. Knighton D.R., Zheng J.H., Ten Eyck L.F., Ashford V.A., Xuong N.H., Taylor S.S., Sowadski J.M. Crystal structure of the catalytic subunit of cyclic adenosine monophosphate-dependent protein kinase. Science. 253:1991;407-414.
42. Knighton D.R., Zheng J.H., Ten Eyck L.F., Xuong N.H., Taylor S.S., Sowadski J.M. Structure of a peptide inhibitor bound to the catalytic subunit of cyclic adenosine monophosphate-dependent protein kinase. Science. 253:1991;414-420.
43. Bossemeyer D., Engh R.A., Kinzel V., Ponstingl H., Huber R. Phosphotransferase and substrate binding mechanism of the cAMP-dependent protein kinase catalytic subunit from porcine heart as deduced from the 2.0 A structure of the complex with Mn2+ adenylyl imidodiphosphate and inhibitor peptide PKI(5-24). EMBO J. 12:1993;849-859.
44. Narayana N., Cox S., Shaltiel S., Taylor S.S., Xuong N. Crystal structure of a polyhistidine-tagged recombinant catalytic subunit of cAMP-dependent protein kinase complexed with the peptide inhibitor PKI(5-24) and adenosine. Biochemistry. 36:1997;4438-4448.
45. Narayana N., Cox S., Nguyen-huu X., Ten Eyck L.F., Taylor S.S. A binary complex of the catalytic subunit of cAMP-dependent protein kinase and adenosine further defines conformational flexibility. Structure. 5:1997;921-935.
46. Narayana N., Diller T.C., Koide K., Bunnage M.E., Nicolaou K.C., Brunton L.L., Xuong N.H., Ten Eyck L.F., Taylor S.S. Crystal structure of the potent natural product inhibitor balanol in complex with the catalytic subunit of cAMP-dependent protein kinase. Biochemistry. 38:1999;2367-2376.
47. Zheng J., Knighton D.R., Xuong N.H., Taylor S.S., Sowadski J.M., Ten Eyck L.F. Crystal structures of the myristylated catalytic subunit of cAMP-dependent protein kinase reveal open and closed conformations. Protein Sci. 2:1993;1559-1573.
48. Jimenez J.S., Kupfer A., Gani V., Shaltiel S. Salt-induced conformational changes in the catalytic subunit of adenosine cyclic 3′,5′-phosphate dependent protein kinase. Use for establishing a connection between one sulfhydryl group and the gamma-P subsite in the ATP site of this subunit. Biochemistry. 21:1982;1623-1630.
49. Nelson N.C., Taylor S.S. Selective protection of sulfhydryl groups in cAMP-dependent protein kinase II. J. Biol. Chem. 258:1983;10981-10987.
50. First E.A., Bubis J., Taylor S.S. Subunit interaction sites between the regulatory and catalytic subunits of cAMP-dependent protein kinase. Identification of a specific interchain disulfide bond. J. Biol. Chem. 263:1988;5176-5182.
51. Salerno A., Lawrence D.S. Covalent modification with concomitant inactivation of the cAMP-dependent protein kinase by affinity labels containing only L-amino acids. J. Biol. Chem. 268:1993;13043-13049.
52. Yan X., Corbin J.D., Francis S.H., Lawrence D.S. Precision targeting of protein kinases. An affinity label that inactivates the cGMP- but not the cAMP-dependent protein kinase. J. Biol. Chem. 271:1996;1845-1848.
53. Landgraf W., Regulla S., Meyer H.E., Hofmann F. Oxidation of cysteines activates cGMP-dependent protein kinase. J. Biol. Chem. 266:1991;16305-16311.
54. Ward N.E., Gravitt K.R., O'Brian C.A. Irreversible inactivation of protein kinase C by a peptide-substrate analog. J. Biol. Chem. 270:1995;8056-8060.
55. Ward N.E., Gravitt K.R., O'Brian C.A. Covalent modification of protein kinase C isozymes by the inactivating peptide substrate analog N-biotinyl-Arg-Arg-Arg-Cys-Leu-Arg-Arg-Leu. Evidence that the biotinylated peptide is an active-site affinity label. J. Biol. Chem. 271:1996;24193-24200.
56. Gopalakrishna R., Chen Z.H., Gundimeda U. Selenocompounds induce a redox modulation of protein kinase C in the cell, compartmentally independent from cytosolic glutathione. its role in inhibition of tumor promotion Arch. Biochem. Biophys. 348:1997;37-48.
57. Gopalakrishna R., Gundimeda U., Chen Z.H. Cancer-preventive selenocompounds induce a specific redox modification of cysteine-rich regions in Ca(2+)-dependent isoenzymes of protein kinase C. Arch. Biochem. Biophys. 348:1997;25-36.
58. Yuan C.J., Huang C.Y., Graves D.J. Oxidation and site-directed mutagenesis of the sulfhydryl groups of a truncated gamma catalytic subunit of phosphorylase kinase. Functional and structural effects. J. Biol. Chem. 269:1994;24367-24373.
59. Mohammadi M., Schlessinger J., Hubbard S.R. Structure of the FGF receptor tyrosine kinase domain reveals a novel autoinhibitory mechanism. Cell. 86:1996;577-587.
60. Xu W., Harrison S.C., Eck M.J. Three-dimensional structure of the tyrosine kinase c-Src. Nature. 385:1997;595-602.
61. Xu W., Doshi A., Lei M., Eck M.J., Harrison S.C. Crystal structures of c-Src reveal features of its autoinhibitory mechanism. Mol. Cell. 3:1999;629-638.
62. Zhang F., Strand A., Robbins D., Cobb M.H., Goldsmith E.J. Atomic structure of the MAP kinase ERK2 at 2.3 Å resolution. Nature. 367:1994;704-711.
63. Canagarajah B.J., Khokhlatchev A., Cobb M.H., Goldsmith E.J. Activation mechanism of the MAP kinase ERK2 by dual phosphorylation. Cell. 90:1997;859-869.
64. Hubbard S.R., Wei L., Ellis L., Hendrickson W.A. Crystal structure of the tyrosine kinase domain of the human insulin receptor. Nature. 372:1994;746-754.
65. Hubbard S.R. Crystal structure of the activated insulin receptor tyrosine kinase in complex with peptide substrate and ATP analog. EMBO J. 16:1997;5572-5581.
66. Smith C.M., Shindyalov I.N., Veretnik S., Gribskov M., Taylor S.S., Ten Eyck L.F., Bourne P.E. The protein kinase resource. Trends Biochem. Sci. 22:1997;444-446.
67. Gopalakrishna R., Jaken S. Protein kinase C signaling and oxidative stress. Free Radic. Biol. Med. 28:2000;1349-1361.
68. Yang J., Cron P., Thompson V., Good V.M., Hess D., Hemmings B.A., Barford D. Molecular mechanism for the regulation of protein kinase B/Akt by hydrophobic motif phosphorylation. Mol. Cell. 9:2002;1227-1240.