Evidence of histidine and aspartic acid phosphorylation in human prostate cancer cells

Naunyn-Schmiedeberg's Archives of Pharmacology

Volumn 388, Issue 2, 2015, Pages 161-173

  Lapek, John D ^a   Tombline, Gregory ^a   Kellersberger, Katherine A ^b   Friedman, Michelle R ^a   Friedman, Alan E ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b BRUKER DALTONIK GMBH   (Germany)

Author keywords

Aspartic acid; Histidine; NM23 H1; Phosphoproteome

Indexed keywords

ASPARTIC ACID; HISTIDINE; NME1 PROTEIN, HUMAN; NUCLEOSIDE DIPHOSPHATE KINASE NM23;

AMINO ACID SEQUENCE; ARTICLE; CELL MOTILITY; CONFORMATIONAL TRANSITION; EVIDENCE BASED PRACTICE; HUMAN; HUMAN CELL; INDEL MUTATION; MALE; MOLECULAR WEIGHT; PROSTATE CANCER; PROSTATE CANCER CELL LINE; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; TANDEM MASS SPECTROMETRY; CELL LINE; METABOLISM; PHOSPHORYLATION; PROSTATE TUMOR; PROTEOMICS; TUMOR CELL LINE;

ASPARTIC ACID; CELL LINE; CELL LINE, TUMOR; HISTIDINE; HUMANS; MALE; NM23 NUCLEOSIDE DIPHOSPHATE KINASES; PHOSPHORYLATION; PROSTATIC NEOPLASMS; PROTEOMICS;

EID: 84934271472     PISSN: 00281298     EISSN: 14321912     Source Type: Journal    
DOI: 10.1007/s00210-014-1063-4     Document Type: Article

References (50)

1. An R et al. Expressions of nucleoside diphosphate kinase (nm23) in tumor tissues are related with metastasis and length of survival of patients with hepatocellular carcinoma Biomed Environ Sci 23:267-272. doi:10.1016/S0895-3988(10)60062-1
2. Attwood PV, Piggott MJ, Zu XL, Besant PG (2007) Focus on phosphohistidine. Amino Acids 32:145-156. doi:10.1007/s00726-006-0443-6
3. Bailey TL, Elkan C (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers Proceedings / International Conference on Intelligent Systems for Molecular Biology; ISMB International Conference on Intelligent Systems for Molecular Biology 2:28-36
4. Besant PG, Attwood PV (2000) Int J Biochem Cell Biol 32:243-253
5. Besant PG, Attwood PV (2005) Mammalian histidine kinases. Biochim Biophys Acta 1754:281-290. doi:10.1016/j.bbapap.2005.07.026
6. Besant PG, Attwood PV (2009) Detection and analysis of protein histidine phosphorylation. Mol Cell Biochem 329:93-106. doi:10.1007/s11010-009-0117-2
7. Ciesla J, Fraczyk T, Rode W (2011) Phosphorylation of basic amino acid residues in proteins: important but easily missed. Acta Biochim Pol 58:137-148
8. Conrads TP, Issaq HJ, Veenstra TD (2002) New tools for quantitative phosphoproteome analysis. Biochem Biophys Res Commun 290:885-890. doi:10.1006/bbrc.2001.6275
9. Cuello F et al (2003) Activation of heterotrimeric G proteins by a high energy phosphate transfer via nucleoside diphosphate kinase (NDPK) B and Gbeta subunits. Complex formation of NDPK B with Gbeta gamma dimers and phosphorylation of His-266 IN Gbeta. J Biol Chem 278:7220-7226. doi:10.1074/jbc.M210304200M210304200
10. Cunha GR, Lung B (1979) The importance of stroma in morphogenesis and functional activity of urogenital epithelium. In Vitro 15:50-71
11. Cunha GR, Hayward SW, Wang YZ, Ricke WA (2003) Role of the stromal microenvironment in carcinogenesis of the prostate. Int J Cancer 107:1-10. doi:10.1002/ijc.11335
12. Cunha GR et al (2004) Hormonal, cellular, and molecular regulation of normal and neoplastic prostatic development. J Steroid Biochem Mol Biol 92:221-236. doi:10.1016/j.jsbmb.2004.10.017
13. Ficarro SB et al (2002) Phosphoproteome analysis by mass spectrometry and its application to Saccharomyces cerevisiae. Nat Biotechnol 20:301-305. doi:10.1038/nbt0302-301
14. Filiz G, Adim S, Aytac B, Akar E, Vuruskan H Significance of nm23 immunoexpression in the prognosis of renal cell carcinoma J Int Med Res 38:620-624
15. Gounaris K, Thomas S, Najarro P, Selkirk ME (2001) Secreted variant of nucleoside diphosphate kinase from the intracellular parasitic nematode. Trichinella spiralis Infect Immu 69:3658-3662. doi:10.1128/IAI.69.6.3658-3662.2001
16. Gullon S, Vicente RL, Mellado RP (2012) A novel two-component system involved in secretion stress response in Streptomyces lividans. PLoS One 7:e48987. doi:10.1371/journal.pone.0048987
17. Hartsough MT et al (2002) Nm23-H1 metastasis suppressor phosphorylation of kinase suppressor of Ras via a histidine protein kinase pathway. J bio chem 277:32389-32399. doi:10.1074/jbc.M203115200
18. Hippe HJ et al (2009) The interaction of nucleoside diphosphate kinase B with Gbetagamma dimers controls heterotrimeric G protein function. Proc Natl Acad Sci U S A 106:16269-16274
19. Hoch JA (2000) Two-component and phosphorelay signal transduction. Curr Opin Microbiol 3:165-170
20. Horak CE et al (2007) Nm23-H1 suppresses metastasis by inhibiting expression of the lysophosphatidic acid receptor EDG2. Cancer Res 67:11751-11759. doi:10.1158/0008-5472.CAN-07-3175
21. Hyyrylainen HL et al (2001) A novel two-component regulatory system in Bacillus subtilis for the survival of severe secretion stress. Mol Microbiol 41:1159-1172
22. Karin M, Ben-Neriah Y (2000) Phosphorylation meets ubiquitination: the control of NF-[kappa]B activity. Annu Rev Immunol 18:621-663. doi:10.1146/annurev.immunol.18.1.621
23. Klumpp S, Krieglstein J (2009) Reversible phosphorylation of histidine residues in proteins from vertebrates. Sci Signal 2:13
24. Kroemer G, Marino G, Levine B (2010) Autophagy and the integrated stress response. Mol Cell 40:280-293. doi:10.1016/j.molcel.2010.09.023
25. Kuchma SL, Connolly JP, O'Toole GA (2005) A three-component regulatory system regulates biofilm maturation and type III secretion in Pseudomonas aeruginosa. J Bacteriol 187:1441-1454. doi:10.1128/JB.187.4.1441-1454.2005
26. Lapek JD Jr, Tombline G, Friedman AE (2011) Mass spectrometry detection of histidine phosphorylation on NM23-H1. J Proteome Res 10:751-755. doi:10.1021/pr100905m
27. Lapek JD Jr, McGrath JL, Ricke WA, Friedman AE (2012) LC/LC-MS/MS of an innovative prostate human epithelial cancer (PHEC) in vitro model system. J Chromatogr B Anal Technol Biomed Life Sci 893-894:34-42. doi:10.1016/j.jchromb.2012.02.029
28. Lee HY, Lee H (1999) Inhibitory activity of nm23-H1 on invasion and colonization of human prostate carcinoma cells is not mediated by its NDP kinase activity. Cancer Lett 145:93-99
29. Liu Q, Cobb JS, Johnson JL, Wang Q, Agar JN (2014) Performance comparisons of nano-LC systems, electrospray sources and LC-MS-MS platforms. J Chromatogr Sci 52:120-127. doi:10.1093/chromsci/bms255
30. Macek B, Mijakovic I (2011) Site-specific analysis of bacterial phosphoproteomes. Proteomics 11:3002-3011. doi:10.1002/pmic.201100012
31. Macek B, Gnad F, Soufi B, Kumar C, Olsen JV, Mijakovic I, Mann M (2008) Phosphoproteome analysis of E. coli reveals evolutionary conservation of bacterial Ser/Thr/Tyr phosphorylation. Mol Cell Proteomics 7:299-307. doi:10.1074/mcp.M700311-MCP200
32. Marshall JC, Lee JH, Steeg PS (2009) Clinical-translational strategies for the elevation of Nm23-H1 metastasis suppressor gene expression. Mol Cell Biochem 329:115-120. doi:10.1007/s11010-009-0116-3
33. Marshall JC et al (2012) Effect of inhibition of the lysophosphatidic acid receptor 1 on metastasis and metastatic dormancy in breast cancer. J Natl Cancer Inst 104:1306-1319. doi:10.1093/jnci/djs319
34. Miller MB, Bassler BL (2001) Quorum sensing in bacteria. Annu Rev Microbiol 55:165-199. doi:10.1146/annurev.micro.55.1.165
35. Ng WL, Bassler BL (2009) Bacterial quorum-sensing network architectures. Annu Rev Genet 43:197-222. doi:10.1146/annurev-genet-102108-134304
36. Pearson MA, Reczek D, Bretscher A, Karplus PA (2000) Structure of the ERM protein moesin reveals the FERM domain fold masked by an extended actin binding tail domain. Cell 101:259-270
37. Perkins DN, Pappin DJ, Creasy DM, Cottrell JS (1999) Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20:3551-3567. doi:10.1002/(SICI)1522-2683(19991201)20:18<3551::AID-ELPS3551>3.0.CO;2-2
38. Ricke WA, Ishii K, Ricke EA, Simko J, Wang Y, Hayward SW, Cunha GR (2006) Steroid hormones stimulate human prostate cancer progression and metastasis. Int J Cancer 118:2123-2131. doi:10.1002/ijc.21614
39. Roymans D, Willems R, Van Blockstaele DR, Slegers H (2002) Nucleoside diphosphate kinase (NDPK/NM23) and the waltz with multiple partners: possible consequences in tumor metastasis. Clin Exp Metastasis 19:465-476
40. Salerno M, Palmieri D, Bouadis A, Halverson D, Steeg PS (2005) Nm23-H1 metastasis suppressor expression level influences the binding properties, stability, and function of the kinase suppressor of Ras1 (KSR1) Erk scaffold in breast carcinoma cells. Mol Cell Biol 25:1379-1388. doi:10.1128/MCB. 25.4.1379-1388.2005
41. Schlessinger J (2000) Cell signaling by receptor tyrosine kinases. Cell 103:211-225
42. Shevchenko A, Tomas H, Havlis J, Olsen JV, Mann M (2006) In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc 1:2856-2860. doi:10.1038/nprot.2006.468
43. Smtih DL, Bruegger BB, Halpern RM, Smith RA (1973) New histone kinases in nuclei of rat tissues. Nature 246:103-104
44. Srivastava S et al (2006) Histidine phosphorylation of the potassium channel KCa3.1 by nucleoside diphosphate kinase B is required for activation of KCa3.1 and CD4 T cells. Mol Cell 24:665-675
45. Steeg PS, Bevilacqua G, Kopper L, Thorgeirsson UP, Talmadge JE, Liotta LA, Sobel ME (1988) Evidence for a novel gene associated with low tumor metastatic potential. J Natl Cancer Inst 80:200-204
46. Tao WA et al (2005) Quantitative phosphoproteome analysis using a dendrimer conjugation chemistry and tandem mass spectrometry. Nat Methods 2:591-598. doi:10.1038/nmeth776
47. Wagner PD, Vu ND (1995) Phosphorylation of ATP-citrate lyase by nucleoside diphosphate kinase. J Biol Chem 270:21758-21764
48. Wagner PD, Vu ND (2000) Histidine to aspartate phosphotransferase activity of nm23 proteins: phosphorylation of aldolase C on Asp-319. Biochem J 346(3):623-630
49. Westers H, Westers L, Darmon E, van Dijl JM, Quax WJ, Zanen G (2006) The CssRS two-component regulatory system controls a general secretion stress response in Bacillus subtilis. FEBS J 273:3816-3827. doi:10.1111/j.1742-4658.2006.05389.x
50. Wiener MC, Sachs JR, Deyanova EG, Yates NA (2004) Differential mass spectrometry: a label-free LC-MS method for finding significant differences in complex peptide and protein mixtures. Anal Chem 76:6085-6096. doi:10.1021/ac0493875