ACS Publications. Most Trusted. Most Cited. Most Read
My Activity
CONTENT TYPES

Phosphoramidate End Labeling of Inorganic Polyphosphates: Facile Manipulation of Polyphosphate for Investigating and Modulating Its Biological Activities

View Author Information
Departments of Biochemistry
§ Chemistry
University of Illinois at Urbana−Champaign, Urbana, Illinois 61801, United States
*To whom correspondence should be addressed. E-mail: [email protected]. Tel: 217-265-4036. Fax: 217-265-5290.
Cite this: Biochemistry 2010, 49, 45, 9935–9941
Publication Date (Web):October 19, 2010
https://doi.org/10.1021/bi1014437
Copyright © 2010 American Chemical Society

    Article Views

    1557

    Altmetric

    -

    Citations

    LEARN ABOUT THESE METRICS
    Other access options

    Abstract

    Abstract Image

    Polyphosphates, linear polymers of inorganic phosphates linked by phosphoanhydride bonds, are widely present among organisms and play diverse roles in biology, including functioning as potent natural modulators of the human blood clotting system. However, studies of protein−polyphosphate interactions are hampered by a dearth of methods for derivatizing polyphosphate or immobilizing it onto solid supports. We now report that EDAC (1-ethyl-3-[3-(dimethylamino)propyl]carbodiimide) efficiently promotes the covalent attachment of a variety of primary amine-containing labels and probes to the terminal phosphates of polyphosphates via stable phosphoramidate linkages. Using 31P NMR, we confirmed that EDAC-mediated reactions between primary amines and polyphosphate result in phosphoramidate linkages with the terminal phosphate groups. We show that polyphosphate can be biotinylated, labeled with fluorophores, and immobilized onto solid supports, that immobilized polyphosphate can be readily used to quantify protein binding affinities, that covalently derivatized or immobilized polyphosphate retains its ability to trigger blood clotting, and that derivatizing the ends of polyphosphate with spermidine protects it from exopolyphosphatase degradation. Our findings open up essentially the entire armamentarium of protein chemistry to modifying polyphosphate, which should greatly facilitate studies of its biological roles.

    Read this article

    To access this article, please review the available access options below.

    Get instant access

    Purchase Access

    Read this article for 48 hours. Check out below using your ACS ID or as a guest.

    Recommended

    Access through Your Institution

    You may have access to this article through your institution.

    Your institution does not have access to this content. You can change your affiliated institution below.

    Cited By

    This article is cited by 57 publications.

    1. Scott M. Shepard, Henning J. Jessen, Christopher C. Cummins. Beyond Triphosphates: Reagents and Methods for Chemical Oligophosphorylation. Journal of the American Chemical Society 2022, 144 (17) , 7517-7530. https://doi.org/10.1021/jacs.1c07990
    2. Viktor Mojr, Mohammad Roghanian, Hedvig Tamman, Duy Dinh Do Pham, Magdalena Petrová, Radek Pohl, Hiraku Takada, Katleen Van Nerom, Hanna Ainelo, Julien Caballero-Montes, Steffi Jimmy, Abel Garcia-Pino, Vasili Hauryliuk, Dominik Rejman. Nonhydrolysable Analogues of (p)ppGpp and (p)ppApp Alarmone Nucleotides as Novel Molecular Tools. ACS Chemical Biology 2021, 16 (9) , 1680-1691. https://doi.org/10.1021/acschembio.1c00398
    3. Werner E.G. Müller, Heinz C. Schröder, Xiaohong Wang. Inorganic Polyphosphates As Storage for and Generator of Metabolic Energy in the Extracellular Matrix. Chemical Reviews 2019, 119 (24) , 12337-12374. https://doi.org/10.1021/acs.chemrev.9b00460
    4. Gabriella M. Fernandes-Cunha, Colin J. McKinlay, Jessica R. Vargas, Henning J. Jessen, Robert M. Waymouth, Paul A. Wender. Delivery of Inorganic Polyphosphate into Cells Using Amphipathic Oligocarbonate Transporters. ACS Central Science 2018, 4 (10) , 1394-1402. https://doi.org/10.1021/acscentsci.8b00470
    5. Cristina Azevedo, Jyoti Singh, Nicole Steck, Alexandre Hofer, Felix A. Ruiz, Tanya Singh, Henning J. Jessen, Adolfo Saiardi. Screening a Protein Array with Synthetic Biotinylated Inorganic Polyphosphate To Define the Human PolyP-ome. ACS Chemical Biology 2018, 13 (8) , 1958-1963. https://doi.org/10.1021/acschembio.8b00357
    6. Alexander J. Donovan, Joseph Kalkowski, Magdalena Szymusiak, Canhui Wang, Stephanie A. Smith, Robert F. Klie, James H. Morrissey, and Ying Liu . Artificial Dense Granules: A Procoagulant Liposomal Formulation Modeled after Platelet Polyphosphate Storage Pools. Biomacromolecules 2016, 17 (8) , 2572-2581. https://doi.org/10.1021/acs.biomac.6b00577
    7. Magdalena Szymusiak, Alexander J. Donovan, Stephanie A. Smith, Ross Ransom, Hao Shen, Joseph Kalkowski, James H. Morrissey, and Ying Liu . Colloidal Confinement of Polyphosphate on Gold Nanoparticles Robustly Activates the Contact Pathway of Blood Coagulation. Bioconjugate Chemistry 2016, 27 (1) , 102-109. https://doi.org/10.1021/acs.bioconjchem.5b00524
    8. Carleigh F. F. Hebbard, Yan Wang, Catherine J. Baker, and James H. Morrissey . Synthesis and Evaluation of Chromogenic and Fluorogenic Substrates for High-Throughput Detection of Enzymes That Hydrolyze Inorganic Polyphosphate. Biomacromolecules 2014, 15 (8) , 3190-3196. https://doi.org/10.1021/bm500872g
    9. Julieta Sacchetto, Eduardo Gutierrez, Guillermo F. Reta, Eduardo Gatica, Sandra Miskoski, María P. Montaña, José Natera, Walter A. Massad. A novel eco-friendly polymeric photosensitizer based on chitosan and flavin mononucleotide. Photochemical & Photobiological Sciences 2023, 22 (12) , 2827-2837. https://doi.org/10.1007/s43630-023-00489-z
    10. Yating Mao, Mingyang Tan, Tia C. L. Kohs, Joanna L. Sylman, Anh T. P. Ngo, Cristina Puy, Owen J. T. McCarty, Travis W. Walker. Transient particle tracking microrheology of plasma coagulation via the intrinsic pathway. Applied Rheology 2023, 33 (1) https://doi.org/10.1515/arh-2022-0129
    11. Takaya Ogawa, Gopinathan M. Anilkumar, Takanori Tamaki, Hidenori Ohashi, Takeo Yamaguchi. Low humidity dependence of proton conductivity in modified zirconium( iv )-hydroxy ethylidene diphosphonates. Materials Chemistry Frontiers 2022, 6 (21) , 3271-3278. https://doi.org/10.1039/D2QM00428C
    12. Florina Veider, Zeynep Burcu Akkuş-Dağdeviren, Patrick Knoll, Andreas Bernkop-Schnürch. Design of nanostructured lipid carriers and solid lipid nanoparticles for enhanced cellular uptake. International Journal of Pharmaceutics 2022, 624 , 122014. https://doi.org/10.1016/j.ijpharm.2022.122014
    13. Tammy K. Truong, Rida A. Malik, Xintong Yao, James C. Fredenburgh, Alan R. Stafford, Hasam M. Madarati, Colin A. Kretz, Jeffrey I. Weitz. Identification of the histidine‐rich glycoprotein domains responsible for contact pathway inhibition. Journal of Thrombosis and Haemostasis 2022, 20 (4) , 821-832. https://doi.org/10.1111/jth.15631
    14. Brian S. Mantilla, Cristina Azevedo, Paul W. Denny, Adolfo Saiardi, Roberto Docampo, . The Histidine Ammonia Lyase of Trypanosoma cruzi Is Involved in Acidocalcisome Alkalinization and Is Essential for Survival under Starvation Conditions. mBio 2021, 12 (6) https://doi.org/10.1128/mBio.01981-21
    15. Ahad Sabab, Sha Liu, Shari Javadiyan, C. John McAdam, Lyall R. Hanton, Alistair Jukes, Sarah Vreugde, Peter-John Wormald. The effect of chemical and structural modifiers on the haemostatic process and cytotoxicity of the beta-chitin patch. Scientific Reports 2021, 11 (1) https://doi.org/10.1038/s41598-021-97781-8
    16. Rida A. Malik, Ji Zhou, James C. Fredenburgh, Tammy K. Truong, Jeff R. Crosby, Alexey S. Revenko, Jeffrey I. Weitz. Polyphosphate-induced thrombosis in mice is factor XII dependent and is attenuated by histidine-rich glycoprotein. Blood Advances 2021, 5 (18) , 3540-3551. https://doi.org/10.1182/bloodadvances.2021004567
    17. Claire S Whyte, Nicola J Mutch. uPA-mediated plasminogen activation is enhanced by polyphosphate. Haematologica 2021, 106 (2) , 522-531. https://doi.org/10.3324/haematol.2019.237966
    18. Jeffery J. Nielsen, Stewart A. Low, Neal T. Ramseier, Rahul V. Hadap, Nicholas A. Young, Mingding Wang, Philip S. Low. Analysis of the bone fracture targeting properties of osteotropic ligands. Journal of Controlled Release 2021, 329 , 570-584. https://doi.org/10.1016/j.jconrel.2020.09.047
    19. Mei Li Khong, Lina Li, Maria E. Solesio, Evgeny V. Pavlov, Julian A. Tanner. Inorganic polyphosphate controls cyclophilin B‐mediated collagen folding in osteoblast‐like cells. The FEBS Journal 2020, 287 (20) , 4500-4524. https://doi.org/10.1111/febs.15249
    20. Catherine J. Baker, Stephanie A. Smith, James H. Morrissey, . Diversification of polyphosphate end-labeling via bridging molecules. PLOS ONE 2020, 15 (8) , e0237849. https://doi.org/10.1371/journal.pone.0237849
    21. Peyman Dinarvand, Likui Yang, Indranil Biswas, Hemant Giri, Alireza R. Rezaie. Plasmodium falciparum histidine rich protein HRPII inhibits the anti‐inflammatory function of antithrombin. Journal of Thrombosis and Haemostasis 2020, 18 (6) , 1473-1483. https://doi.org/10.1111/jth.14713
    22. Justine Lempart, Eric Tse, James A Lauer, Magdalena I Ivanova, Alexandra Sutter, Nicholas Yoo, Philipp Huettemann, Daniel Southworth, Ursula Jakob. Mechanistic insights into the protective roles of polyphosphate against amyloid cytotoxicity. Life Science Alliance 2019, 2 (5) , e201900486. https://doi.org/10.26508/lsa.201900486
    23. Jyoti Singh, Nicole Steck, Debaditya De, Alexandre Hofer, Alexander Ripp, Ilya Captain, Manfred Keller, Paul A. Wender, Rashna Bhandari, Henning J. Jessen. A Phosphoramidite Analogue of Cyclotriphosphate Enables Iterative Polyphosphorylations. Angewandte Chemie 2019, 131 (12) , 3968-3973. https://doi.org/10.1002/ange.201814366
    24. Jyoti Singh, Nicole Steck, Debaditya De, Alexandre Hofer, Alexander Ripp, Ilya Captain, Manfred Keller, Paul A. Wender, Rashna Bhandari, Henning J. Jessen. A Phosphoramidite Analogue of Cyclotriphosphate Enables Iterative Polyphosphorylations. Angewandte Chemie International Edition 2019, 58 (12) , 3928-3933. https://doi.org/10.1002/anie.201814366
    25. Borros Arneth. Coevolution of the coagulation and immune systems. Inflammation Research 2019, 68 (2) , 117-123. https://doi.org/10.1007/s00011-018-01210-y
    26. Lihan Xie, Ursula Jakob. Inorganic polyphosphate, a multifunctional polyanionic protein scaffold. Journal of Biological Chemistry 2019, 294 (6) , 2180-2190. https://doi.org/10.1074/jbc.REV118.002808
    27. Raquel S. Negreiros, Noelia Lander, Guozhong Huang, Ciro D. Cordeiro, Stephanie A. Smith, James H. Morrissey, Roberto Docampo. Inorganic polyphosphate interacts with nucleolar and glycosomal proteins in trypanosomatids. Molecular Microbiology 2018, 110 (6) , 973-994. https://doi.org/10.1111/mmi.14131
    28. Julia M. Diaz, Alisia Holland, James G. Sanders, Karrie Bulski, Douglas Mollett, Chau-Wen Chou, Dennis Phillips, Yuanzhi Tang, Solange Duhamel. Dissolved Organic Phosphorus Utilization by Phytoplankton Reveals Preferential Degradation of Polyphosphates Over Phosphomonoesters. Frontiers in Marine Science 2018, 5 https://doi.org/10.3389/fmars.2018.00380
    29. Joanna L. Sylman, Uranbileg Daalkhaijav, Ying Zhang, Elliot M. Gray, Parsa A. Farhang, Tiffany T. Chu, Jevgenia Zilberman-Rudenko, Cristina Puy, Erik I. Tucker, Stephanie A. Smith, James H. Morrissey, Travis W. Walker, Xiaolin L. Nan, András Gruber, Owen J. T. McCarty. Differential Roles for the Coagulation Factors XI and XII in Regulating the Physical Biology of Fibrin. Annals of Biomedical Engineering 2017, 45 (5) , 1328-1340. https://doi.org/10.1007/s10439-016-1771-7
    30. Rūta Gerasimaitė, Andreas Mayer. Ppn2, a novel Zn 2+ -dependent polyphosphatase in the acidocalcisome-like yeast vacuole. Journal of Cell Science 2017, 130 (9) , 1625-1636. https://doi.org/10.1242/jcs.201061
    31. Ju Hun Yeon, Nima Mazinani, Travis S. Schlappi, Karen Y. T. Chan, James R. Baylis, Stephanie A. Smith, Alexander J. Donovan, Damien Kudela, Galen D. Stucky, Ying Liu, James H. Morrissey, Christian J. Kastrup. Localization of Short-Chain Polyphosphate Enhances its Ability to Clot Flowing Blood Plasma. Scientific Reports 2017, 7 (1) https://doi.org/10.1038/srep42119
    32. Joshua M. Gajsiewicz, Stephanie A. Smith, James H. Morrissey. Polyphosphate and RNA Differentially Modulate the Contact Pathway of Blood Clotting. Journal of Biological Chemistry 2017, 292 (5) , 1808-1814. https://doi.org/10.1074/jbc.M116.754325
    33. Joanne L. Mitchell, Ausra S. Lionikiene, Georgi Georgiev, Anja Klemmer, Chelsea Brain, Paul Y. Kim, Nicola J. Mutch. Polyphosphate colocalizes with factor XII on platelet-bound fibrin and augments its plasminogen activator activity. Blood 2016, 128 (24) , 2834-2845. https://doi.org/10.1182/blood-2015-10-673285
    34. Linda Labberton, Ellinor Kenne, Andy T. Long, Katrin F. Nickel, Antonio Di Gennaro, Rachel A. Rigg, James S. Hernandez, Lynn Butler, Coen Maas, Evi X. Stavrou, Thomas Renné. Neutralizing blood-borne polyphosphate in vivo provides safe thromboprotection. Nature Communications 2016, 7 (1) https://doi.org/10.1038/ncomms12616
    35. Lakshmi C. Wijeyewickrema, Emilie Lameignere, Lilian Hor, Renee C. Duncan, Toshikazu Shiba, Richard J. Travers, Piyushkumar R. Kapopara, Victor Lei, Stephanie A. Smith, Hugh Kim, James H. Morrissey, Robert N. Pike, Edward M. Conway. Polyphosphate is a novel cofactor for regulation of complement by a serpin, C1 inhibitor. Blood 2016, 128 (13) , 1766-1776. https://doi.org/10.1182/blood-2016-02-699561
    36. Patrick M. Suess, Richard H. Gomer. Extracellular Polyphosphate Inhibits Proliferation in an Autocrine Negative Feedback Loop in Dictyostelium discoideum. Journal of Biological Chemistry 2016, 291 (38) , 20260-20269. https://doi.org/10.1074/jbc.M116.737825
    37. Elena N. Dedkova. Inorganic polyphosphate in cardiac myocytes: from bioenergetics to the permeability transition pore and cell survival. Biochemical Society Transactions 2016, 44 (1) , 25-34. https://doi.org/10.1042/BST20150218
    38. Nicola J. Mutch. Polyphosphate as a haemostatic modulator. Biochemical Society Transactions 2016, 44 (1) , 18-24. https://doi.org/10.1042/BST20150207
    39. Stephanie A. Smith, James H. Morrissey. Inorganic Polyphosphate in Blood Coagulation. 2016, 159-176. https://doi.org/10.1007/978-3-319-41073-9_11
    40. Claire S. Whyte, Irina N. Chernysh, Marco M. Domingues, Simon Connell, John W. Weisel, Robert A. S. Ariens, Nicola J. Mutch. Polyphosphate delays fibrin polymerisation and alters the mechanical properties of the fibrin network. Thrombosis and Haemostasis 2016, 116 (11) , 897-903. https://doi.org/10.1160/TH16-01-0062
    41. Wei Fang, Guo-Ping Sheng, Long-Fei Wang, Xiao-Dong Ye, Han-Qing Yu. Quantitative evaluation of noncovalent interactions between polyphosphate and dissolved humic acids in aqueous conditions. Environmental Pollution 2015, 207 , 123-129. https://doi.org/10.1016/j.envpol.2015.09.001
    42. Rami A. Al-Horani, David Gailani, Umesh R. Desai. Allosteric inhibition of factor XIa. Sulfated non-saccharide glycosaminoglycan mimetics as promising anticoagulants. Thrombosis Research 2015, 136 (2) , 379-387. https://doi.org/10.1016/j.thromres.2015.04.017
    43. Stephanie A. Smith, Richard J. Travers, James H. Morrissey. How it all starts: Initiation of the clotting cascade. Critical Reviews in Biochemistry and Molecular Biology 2015, 50 (4) , 326-336. https://doi.org/10.3109/10409238.2015.1050550
    44. Stephanie A. Smith, James H. Morrissey. 2013 Scientific Sessions Sol Sherry Distinguished Lecture in Thrombosis. Arteriosclerosis, Thrombosis, and Vascular Biology 2015, 35 (6) , 1298-1305. https://doi.org/10.1161/ATVBAHA.115.301927
    45. J.H. Morrissey, S.A. Smith. Polyphosphate as modulator of hemostasis, thrombosis, and inflammation. Journal of Thrombosis and Haemostasis 2015, 13 , S92-S97. https://doi.org/10.1111/jth.12896
    46. R. J. Travers, S. A. Smith, J. H. Morrissey. Polyphosphate, platelets, and coagulation. International Journal of Laboratory Hematology 2015, 37 (S1) , 31-35. https://doi.org/10.1111/ijlh.12349
    47. Cristina Azevedo, Thomas Livermore, Adolfo Saiardi. Protein Polyphosphorylation of Lysine Residues by Inorganic Polyphosphate. Molecular Cell 2015, 58 (1) , 71-82. https://doi.org/10.1016/j.molcel.2015.02.010
    48. Richard J. Travers, Rajesh A. Shenoi, Manu Thomas Kalathottukaren, Jayachandran N. Kizhakkedathu, James H. Morrissey. Nontoxic polyphosphate inhibitors reduce thrombosis while sparing hemostasis. Blood 2014, 124 (22) , 3183-3190. https://doi.org/10.1182/blood-2014-05-577932
    49. Stephanie A. Smith, James H. Morrissey. Polyphosphate. Current Opinion in Hematology 2014, 21 (5) , 388-394. https://doi.org/10.1097/MOH.0000000000000069
    50. R. Engel, C.M. Brain, J. Paget, A.S. Lionikiene, N.J. Mutch. Single‐chain factor XII exhibits activity when complexed to polyphosphate. Journal of Thrombosis and Haemostasis 2014, 12 (9) , 1513-1522. https://doi.org/10.1111/jth.12663
    51. James H. Morrissey. Contributions of Platelet Polyphosphate to Hemostasis and Thrombosis. 2014, 236-245. https://doi.org/10.1002/9781118833391.ch17
    52. Beth A. Bouchard, Jay R. Silveira, Paula B. Tracy. Interactions Between Platelets and the Coagulation System. 2013, 425-451. https://doi.org/10.1016/B978-0-12-387837-3.00021-3
    53. Stephanie A. Smith, Sharon H. Choi, Julie N. R. Collins, Richard J. Travers, Brian C. Cooley, James H. Morrissey. Inhibition of polyphosphate as a novel strategy for preventing thrombosis and inflammation. Blood 2012, 120 (26) , 5103-5110. https://doi.org/10.1182/blood-2012-07-444935
    54. James H. Morrissey, Sharon H. Choi, Stephanie A. Smith. Polyphosphate: an ancient molecule that links platelets, coagulation, and inflammation. Blood 2012, 119 (25) , 5972-5979. https://doi.org/10.1182/blood-2012-03-306605
    55. Maureen McMichael. New Models of Hemostasis. Topics in Companion Animal Medicine 2012, 27 (2) , 40-45. https://doi.org/10.1053/j.tcam.2012.07.005
    56. James H. Morrissey. Polyphosphate: a link between platelets, coagulation and inflammation. International Journal of Hematology 2012, 95 (4) , 346-352. https://doi.org/10.1007/s12185-012-1054-5
    57. Sharon H. Choi, Stephanie A. Smith, James H. Morrissey. Polyphosphate is a cofactor for the activation of factor XI by thrombin. Blood 2011, 118 (26) , 6963-6970. https://doi.org/10.1182/blood-2011-07-368811

    Pair your accounts.

    Export articles to Mendeley

    Get article recommendations from ACS based on references in your Mendeley library.

    Pair your accounts.

    Export articles to Mendeley

    Get article recommendations from ACS based on references in your Mendeley library.

    You’ve supercharged your research process with ACS and Mendeley!

    STEP 1:
    Click to create an ACS ID

    Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

    Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

    Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

    MENDELEY PAIRING EXPIRED
    Your Mendeley pairing has expired. Please reconnect