Cellular delivery and photochemical release of a caged inositol-pyrophosphate induces PH-domain translocation in cellulo

Nature Communications

Volumn 7, Issue , 2016, Pages

  Pavlovic, Igor ^a   Thakor, Divyeshsinh T ^a   Vargas, Jessica R ^b   McKinlay, Colin J ^b   Hauke, Sebastian ^c   Anstaett, Philipp ^a   Camunã, Rafael C ^d   Bigler, Laurent ^a   Gasser, Gilles ^a   Schultz, Carsten ^c   Wender, Paul A ^b   Jessen, Henning J ^e  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b STANFORD UNIVERSITY   (United States)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^d UNIVERSITY OF MÁLAGA   (Spain)

^e UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DIPHOSPHO MYO INOSITOL PENTAKISPHOSPHATE; GUANIDINE; NANOCAGE; PYROPHOSPHORIC ACID DERIVATIVE; UNCLASSIFIED DRUG; INOSITOL HEPTAKISPHOSPHATE; INOSITOL PHOSPHATE; NANOMATERIAL; NANOPARTICLE; PROTEIN KINASE B;

CELLS AND CELL COMPONENTS; ENZYME ACTIVITY; IRRADIATION; NANOPARTICLE; PH; PHOSPHATASE; SIGNALING; TRANSLOCATION;

ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; CYTOPLASM; CYTOSOL; FEMALE; HUMAN; HUMAN CELL; INTRACELLULAR TRANSPORT; IRRADIATION; PH; PHOTOCHEMISTRY; SYNTHESIS; CHEMISTRY; CONFOCAL MICROSCOPY; DRUG DELIVERY SYSTEM; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; HELA CELL LINE; MATRIX-ASSISTED LASER DESORPTION-IONIZATION MASS SPECTROMETRY; METABOLISM; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN TERTIARY STRUCTURE; SIGNAL TRANSDUCTION;

CELL MEMBRANE; CYTOPLASM; DRUG DELIVERY SYSTEMS; FLOW CYTOMETRY; HELA CELLS; HUMANS; INOSITOL PHOSPHATES; MAGNETIC RESONANCE SPECTROSCOPY; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; NANOPARTICLES; NANOSTRUCTURES; PHOTOCHEMICAL PROCESSES; PROTEIN STRUCTURE, TERTIARY; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 84957068217     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms10622     Document Type: Article

References (52)

1. Bennett, M., Onnebo, S. M. N., Azevedo, C., Saiardi, A. Inositol pyrophosphates: metabolism and signalling. Cell. Mol. Life Sci. 63, 552-564 (2006).
2. Monserrate, J. P., York, J. D. Inositol phosphate synthesis and the nuclear processes they affect. Curr. Opin. Cell Biol. 22, 365-373 (2010).
3. Shears, S. B., Weaver, J. D., Wang, H. Structural insight into inositol pyrophosphate turnover. Adv. Biol. Regul. 53, 19-27 (2013).
4. Wilson, M. S. C., Livermore, T. M., Saiardi, A. Inositol pyrophosphates: between signalling and metabolism. Biochem. J. 452, 369-379 (2013).
5. Rao, F. et al. Inositol pyrophosphates promote tumor growth and metastasis by antagonizing liver kinase B1. Proc. Natl Acad. Sci. USA 112, 1773-1778 (2015).
6. Rao, F. et al. Inositol hexakisphosphate kinase-1 mediates assembly/disassembly of the CRL4-signalosome complex to regulate DNA repair and cell death. Proc. Natl Acad. Sci. USA 111, 16005-16010 (2014).
7. Laha, D. et al. VIH2 regulates the synthesis of inositol pyrophosphate InsP8 and jasmonate-dependent defenses in Arabidopsis. Plant Cell 27, 1082-1097 (2015).
8. Illies, C. et al. Requirement of inositol pyrophosphates for full exocytotic capacity in pancreatic beta cells. Science 318, 1299-1302 (2007).
9. Chakraborty, A. et al. Inositol pyrophosphates inhibit akt signalling, thereby regulating insulin sensitivity and weight gain. Cell 143, 897-910 (2010).
10. Luo, H. R. et al. Inositol pyrophosphates mediate chemotaxis in dictyostelium via pleckstrin homology domain-PtdIns(3,4,5)P3 interactions. Cell 114, 559-572 (2003).
11. Wu, M. X. et al. Elucidating diphosphoinositol polyphosphate function with nonhydrolyzable analogues. Angew. Chem. Int. Ed. 53, 7192-7197 (2014).
12. Mackenzie, R. W., Elliott, B. T. Akt/PKB activation and insulin signalling: a novel insulin signalling pathway in the treatment of type 2 diabetes. Diabetes Metab. Syndr. Obes. 7, 55-64 (2014).
13. Yu, H. T., Li, J. B., Wu, D. D., Qiu, Z. J., Zhang, Y. Chemistry and biological applications of photo-labile organic molecules. Chem. Soc. Rev. 39, 464-473 (2010).
14. Ozaki, S., DeWald, D. B., Shope, J. C., Chen, J., Prestwich, G. D. Intracellular delivery of phosphoinositides and inositol phosphates using polyamine carriers. Proc. Natl Acad. Sci. USA 97, 11286-11291 (2000).
15. Best, M. D., Zhang, H. L., Prestwich, G. D. Inositol polyphosphates, diphosphoinositol polyphosphates and phosphatidylinositol polyphosphate lipids: Structure, synthesis, development of probes for studying biological activity. Nat. Prod. Rep. 27, 1403-1430 (2010).
16. Hoglinger, D., Nadler, A., Schultz, C. Caged lipids as tools for investigating cellular signalling. Biochim. Biophys. Acta 1841, 1085-1096 (2014).
17. Kantevari, S., Gordon, G. R. J., MacVicar, B. A., Ellis-Davies, G. C. R. A practical guide to the synthesis and use of membrane-permeant acetoxymethyl esters of caged inositol polyphosphates. Nat. Protoc. 6, 327-337 (2011).
18. Li, W. H., Llopis, J., Whitney, M., Zlokarnik, G., Tsien, R. Y. Cell-permeant caged InsP(3) ester shows that Ca2\+ spike frequency can optimize gene expression. Nature 392, 936-941 (1998).
19. Pavlovic, I. et al. Prometabolites of 5-Diphospho-myo-inositol Pentakisphosphate. Angew. Chem. Int. Ed. 54, 9622-9626 (2015).
20. Glennon, M. C., Shears, S. B. Turnover of inositol pentakisphosphates, inositol hexakisphosphate and diphosphoinositol polyphosphates in primary cultured-hepatocytes. Biochem. J. 293, 583-590 (1993).
21. Geihe, E. I. et al. Designed guanidinium-rich amphipathic oligocarbonate molecular transporters complex, deliver and release siRNA in cells. Proc. Natl Acad. Sci. USA 109, 13171-13176 (2012).
22. Albert, C. et al. Biological variability in the structures of diphosphoinositol polyphosphates in Dictyostelium discoideum and mammalian cells. Biochem. J. 327, 553-560 (1997).
23. Capolicchio, S., Thakor, D. T., Linden, A., Jessen, H. J. Synthesis of unsymmetric diphospho-inositol polyphosphates. Angew. Chem. Int. Ed. 52, 6912-6916 (2013).
24. Capolicchio, S., Wang, H. C., Thakor, D. T., Shears, S. B., Jessen, H. J. Synthesis of densely phosphorylated Bis-1,5-diphospho-myo-inositol tetrakisphosphate and its enantiomer by bidirectional P-anhydride formation. Angew. Chem. Int. Ed. 53, 9508-9511 (2014).
25. Falck, J. R. et al. Synthesis and structure of cellular mediators-inositol polyphosphate diphosphates. J. Am. Chem. Soc. 117, 12172-12175 (1995).
26. Laussmann, T., Reddy, K. M., Reddy, K. K., Falck, J. R., Vogel, G. Diphospho-myo-inositol phosphates from Dictyostelium identified as D-6-diphospho-myo-inositol pentakisphosphate and D-5,6-bisdiphosphomyo-inositol tetrakisphosphate. Biochem. J. 322, 31-33 (1997).
27. Reddy, K. M., Reddy, K. K., Falck, J. R. Synthesis of 2-and 5-diphospho-myoinositol pentakisphosphate (2-and 5-PP-InsP(5)), intracellular mediators. Tetrahedron Lett. 38, 4951-4952 (1997).
28. Wang, H. C. et al. Synthetic inositol phosphate analogues reveal that PPIP5K2 has a surface-mounted substrate capture site that is a target for drug discovery. Chem. Biol. 21, 689-699 (2014).
29. Wu, M., Dul, B. E., Trevisan, A. J., Fiedler, D. Synthesis and characterization of non-hydrolysable diphosphoinositol polyphosphate messengers. Chem. Sci. 4, 405-410 (2013).
30. Zhang, H., Thompson, J., Prestwich, G. D. A scalable synthesis of the IP7Isomer, 5-PP-Ins(1,2,3,4,6)P5. Org. Lett. 11, 1551-1554 (2009).
31. Watanabe, Y., Nakamura, T., Mitsumoto, H. Protection of phosphate with the 9-fluorenylmethyl group. Synthesis of unsaturated-acyl phosphatidylinositol 4,5-bisphosphate. Tetrahedron Lett. 38, 7407-7410 (1997).
32. Mentel, M., Laketa, V., Subramanian, D., Gillandt, H., Schultz, C. Photoactivatable and cell-membrane-permeable phosphatidylinositol 3,4,5-trisphosphate. Angew. Chem. Int. Ed. 50, 3811-3814 (2011).
33. Subramanian, D. et al. Activation of membrane-permeant caged PtdIns(3)P induces endosomal fusion in cells. Nat. Chem. Biol. 6, 324-326 (2010).
34. Jessen, H. J., Schulz, T., Balzarini, J., Meier, C. Bioreversible protection of nucleoside diphosphates. Angew. Chem. Int. Ed. 47, 8719-8722 (2008).
35. Thomson, W. et al. Synthesis, bioactivation and anti-hiv activity of the Bis (4-Acyloxybenzyl) and Mono(4-Acyloxybenzyl) esters of the 5'-monophosphate of Azt. J. Chem. Soc. Perkin Trans. 1, 1239-1245 (1993).
36. Cremosnik, G. S., Hofer, A., Jessen, H. J. Iterative synthesis of nucleoside oligophosphates with phosphoramidites. Angew. Chem. Int. Ed. 53, 286-289 (2014).
37. Hofer, A. et al. A Modular synthesis of modified phosphoanhydrides. Chem. Eur. J. 21, 10116-10122 (2015).
38. Losito, O., Szijgyarto, Z., Resnick, A. C., Saiardi, A. Inositol pyrophosphates and their unique metabolic complexity: analysis by gel electrophoresis. PLoS ONE 4, e5580 (2009).
39. Anstaett, P., Leonidova, A., Gasser, G. Caged phosphate and the slips and misses in determination of quantum yields for ultraviolet-A-induced photouncaging. ChemPhysChem 16, 1857-1860 (2015).
40. Anstaett, P., Leonidova, A., Janett, E., Bochet, C. G., Gasser, G. Reply to commentary by trentham et al. on "caged phosphate and the slips and misses in determination of quantum yields for ultraviolet-a-induced photouncaging" by Gasser et al. ChemPhysChem 16, 1863-1866 (2015).
41. Corrie, J. E., Kaplan, J. H., Forbush, B., Ogden, D. C., Trentham, D. R. Commentary on "caged phosphate and the slips and misses in determination of quantum yields for ultraviolet-a-induced photouncaging" by G. Gasser and Co-Workers. ChemPhysChem 16, 1861-1862 (2015).
42. Schonleber, R. O., Bendig, J., Hagen, V., Giese, B. Rapid photolytic release of cytidine 5-diphosphate from a coumarin derivative: A new tool for the investigation of ribonucleotide reductases. Bioorg. Med. Chem. 10, 97-101 (2002).
43. Stanzl, E. G., Trantow, B. M., Vargas, J. R., Wender, P. A. Fifteen years of cell-penetrating guanidinium-rich molecular transporters: basic science, research tools, clinical applications. Acc. Chem. Res. 46, 2944-2954 (2013).
44. Lee, H. L. et al. Single-molecule motions of oligoarginine transporter conjugates on the plasma membrane of Chinese hamster ovary cells. J. Am. Chem. Soc. 130, 9364-9370 (2008).
45. Rothbard, J. B., Jessop, T. C., Lewis, R. S., Murray, B. A., Wender, P. A. Role of membrane potential and hydrogen bonding in the mechanism of translocation of guanidinium-rich peptides into cells. J. Am. Chem. Soc. 126, 9506-9507 (2004).
46. Wender, P. A., Galliher, W. C., Goun, E. A., Jones, L. R., Pillow, T. H. The design of guanidinium-rich transporters and their internalization mechanisms. Adv. Drug Deliv. Rev. 60, 452-472 (2008).
47. Wilson, M. S. C., Bulley, S. J., Pisani, F., Irvine, R. F., Saiardi, A. A novel method for the purification of inositol phosphates from biological samples reveals that no phytate is present in human plasma or urine. Open Biol. 5, 150014 (2015).
48. Cormack, B. P., Valdivia, R. H., Falkow, S. FACS-optimized mutants of the green fluorescent protein (GFP). Gene 173, 33-38 (1996).
49. Laketa, V. et al. PIP(3) induces the recycling of receptor tyrosine kinases. Sci. Signal. 7, ra5 (2014).
50. Jo, H. et al. Small molecule-induced cytosolic activation of protein kinase Akt rescues ischemia-elicited neuronal death. Proc. Natl Acad. Sci. USA 109, 10581-10586 (2012).
51. Lemmon, M. A. Pleckstrin homology (PH) domains and phosphoinositides. Biochem. Soc. Symp. 74, 81-93 (2007).
52. Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676-682 (2012).