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Title: Intracellular distribution and stability of a luminescent rhenium(I) tricarbonyl tetrazolato complex using epifluorescence microscopy in conjunction with X-ray fluorescence imaging

Abstract

Optical fluorescence microscopy was used in conjunction with X-ray fluorescence microscopy to monitor the stability and intracellular distribution of the luminescent rhenium(I) complex fac-[Re(CO)3(phen)L], where phen = 1,10-phenathroline and L = 5-(4-iodophenyl)tetrazolato, in 22Rv1 cells. The rhenium complex showed no signs of ancillary ligand dissociation, a conclusion based on data obtained via X-ray fluorescence imaging aligning iodine and rhenium distributions. A diffuse reticular localisation was detected for the complex, in the nuclear/perinuclear region of cells, by either optical or X-ray fluorescence techniques. Furthermore, X-ray fluorescence also showed that the Re-I complex disrupted the homeostasis of some biologically relevant elements, such as chlorine, potassium and zinc.

Authors:
 [1]; ORCiD logo [1];  [2];  [2];  [3];  [4];  [2];  [5];  [5];  [4];  [4];  [6];  [7]
  1. The Univ. of Adelaide (Australia)
  2. Univ. of South Australia, Adelaide (Australia)
  3. The Univ. of Sydney (Australia)
  4. Dept. of Chemistry, Perth (Australia)
  5. Argonne National Lab. (ANL), Argonne, IL (United States)
  6. Univ. of Western Australia, Crawley (Australia)
  7. Univ. of Bologna, Bologna (Italy)
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States)
Sponsoring Org.:
Australian Research Council; USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1374605
Grant/Contract Number:  
AC02-06CH11357
Resource Type:
Accepted Manuscript
Journal Name:
Metallomics
Additional Journal Information:
Journal Volume: 9; Journal Issue: 4; Journal ID: ISSN 1756-5901
Publisher:
Royal Society of Chemistry
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; 46 INSTRUMENTATION RELATED TO NUCLEAR SCIENCE AND TECHNOLOGY

Citation Formats

Wedding, Jason L., Harris, Hugh H., Bader, Christie A., Plush, Sally E., Mak, Rachel, Massi, Massimiliano, Brooks, Douglas A., Lai, Barry, Vogt, Stefan, Werrett, Melissa V., Simpson, Peter V., Skelton, Brian W., and Stagni, Stefano. Intracellular distribution and stability of a luminescent rhenium(I) tricarbonyl tetrazolato complex using epifluorescence microscopy in conjunction with X-ray fluorescence imaging. United States: N. p., 2016. Web. doi:10.1039/c6mt00243a.
Wedding, Jason L., Harris, Hugh H., Bader, Christie A., Plush, Sally E., Mak, Rachel, Massi, Massimiliano, Brooks, Douglas A., Lai, Barry, Vogt, Stefan, Werrett, Melissa V., Simpson, Peter V., Skelton, Brian W., & Stagni, Stefano. Intracellular distribution and stability of a luminescent rhenium(I) tricarbonyl tetrazolato complex using epifluorescence microscopy in conjunction with X-ray fluorescence imaging. United States. doi:10.1039/c6mt00243a.
Wedding, Jason L., Harris, Hugh H., Bader, Christie A., Plush, Sally E., Mak, Rachel, Massi, Massimiliano, Brooks, Douglas A., Lai, Barry, Vogt, Stefan, Werrett, Melissa V., Simpson, Peter V., Skelton, Brian W., and Stagni, Stefano. Wed . "Intracellular distribution and stability of a luminescent rhenium(I) tricarbonyl tetrazolato complex using epifluorescence microscopy in conjunction with X-ray fluorescence imaging". United States. doi:10.1039/c6mt00243a. https://www.osti.gov/servlets/purl/1374605.
@article{osti_1374605,
title = {Intracellular distribution and stability of a luminescent rhenium(I) tricarbonyl tetrazolato complex using epifluorescence microscopy in conjunction with X-ray fluorescence imaging},
author = {Wedding, Jason L. and Harris, Hugh H. and Bader, Christie A. and Plush, Sally E. and Mak, Rachel and Massi, Massimiliano and Brooks, Douglas A. and Lai, Barry and Vogt, Stefan and Werrett, Melissa V. and Simpson, Peter V. and Skelton, Brian W. and Stagni, Stefano},
abstractNote = {Optical fluorescence microscopy was used in conjunction with X-ray fluorescence microscopy to monitor the stability and intracellular distribution of the luminescent rhenium(I) complex fac-[Re(CO)3(phen)L], where phen = 1,10-phenathroline and L = 5-(4-iodophenyl)tetrazolato, in 22Rv1 cells. The rhenium complex showed no signs of ancillary ligand dissociation, a conclusion based on data obtained via X-ray fluorescence imaging aligning iodine and rhenium distributions. A diffuse reticular localisation was detected for the complex, in the nuclear/perinuclear region of cells, by either optical or X-ray fluorescence techniques. Furthermore, X-ray fluorescence also showed that the Re-I complex disrupted the homeostasis of some biologically relevant elements, such as chlorine, potassium and zinc.},
doi = {10.1039/c6mt00243a},
journal = {Metallomics},
number = 4,
volume = 9,
place = {United States},
year = {2016},
month = {11}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

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Cited by: 9 works
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Figures / Tables:

Figure 1 Figure 1: Structure of the investgated complex Re-I.

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Works referenced in this record:

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{Re III Cl 3 } Core Complexes with Bifunctional Single Amino Acid Chelates
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Rhenium fac tricarbonyl bisimine complexes: biologically useful fluorochromes for cell imaging applications
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Applications of luminescent inorganic and organometallic transition metal complexes as biomolecular and cellular probes
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Uptake, Distribution, and Speciation of Selenoamino Acids by Human Cancer Cells: X-ray Absorption and Fluorescence Methods
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Induction of DNA-Double-Strand Breaks by Auger Electrons from 99mTc Complexes with DNA-Binding Ligands
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Correlative microXRF and optical immunofluorescence microscopy of adherent cells labeled with ultrasmall gold particles
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Silicon nitride as a versatile growth substrate for microspectroscopic imaging and mapping of individual cells
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XAS and XFM studies of selenium and copper speciation and distribution in the kidneys of selenite-supplemented rats
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Comprehensive Radiolabeling, Stability, and Tissue Distribution Studies of Technetium-99m Single Amino Acid Chelates (SAAC)
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The one-pot synthesis and the fluorescence and cytotoxicity studies of chlorotricarbonyl(α-diimine)rhenium(I), fac-(CO)3(α-diimine)ReCl, complexes
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Modulation of the organelle specificity in Re( i ) tetrazolato complexes leads to labeling of lipid droplets
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Rhenium tetrazolato complexes coordinated to thioalkyl-functionalised phenanthroline ligands: synthesis, photophysical characterisation, and incubation in live HeLa cells
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Ultrafast Excited-State Dynamics of [Re(L)(CO) 3 (bpy)] n Complexes: Involvement of the Solvent
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Progress with, and prospects for, metal complexes in cell imaging
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Complexes in context: Attempting to control the cellular uptake and localisation of rhenium fac-tricarbonyl polypyridyl complexes
journal, January 2011

  • Balasingham, Rebeca G.; Coogan, Michael P.; Thorp-Greenwood, Flora L.
  • Dalton Transactions, Vol. 40, Issue 44
  • DOI: 10.1039/c1dt11219h

Metabolism of Selenite in Human Lung Cancer Cells: X-Ray Absorption and Fluorescence Studies
journal, November 2011

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    Works referencing / citing this record:

    Imaging nuclear, endoplasmic reticulum and plasma membrane events in real time
    journal, September 2016

    • Bader, Christie A.; Sorvina, Alexandra; Simpson, Peter V.
    • FEBS Letters, Vol. 590, Issue 18
    • DOI: 10.1002/1873-3468.12365

    Induction of DNA-Double-Strand Breaks by Auger Electrons from 99mTc Complexes with DNA-Binding Ligands
    journal, January 2005

    • Häfliger, Pascal; Agorastos, Nikos; Spingler, Bernhard
    • ChemBioChem, Vol. 6, Issue 2
    • DOI: 10.1002/cbic.200400210

    Organometallic Compounds: An Opportunity for Chemical Biology?
    journal, May 2012


    A Phenylbenzothiazole Conjugate with the Tricarbonyl fac-[M(I)(CO)3]+ (M = Re, 99Tc, 99mTc) Core for Imaging of β-Amyloid Plaques
    journal, August 2012

    • Sagnou, Marina; Tzanopoulou, Stamatia; Raptopoulou, Catherine P.
    • European Journal of Inorganic Chemistry, Vol. 2012, Issue 27
    • DOI: 10.1002/ejic.201200450

    Current use and future potential of organometallic radiopharmaceuticals
    journal, November 2002

    • Schibli, Roger; Schubiger, August
    • European Journal of Nuclear Medicine and Molecular Imaging, Vol. 29, Issue 11
    • DOI: 10.1007/s00259-002-0900-8

    Selenite-mediated production of superoxide radical anions in A549 cancer cells is accompanied by a selective increase in SOD1 concentration, enhanced apoptosis and Se–Cu bonding
    journal, February 2014

    • Weekley, Claire M.; Jeong, Gloria; Tierney, Michael E.
    • JBIC Journal of Biological Inorganic Chemistry, Vol. 19, Issue 6
    • DOI: 10.1007/s00775-014-1113-x

    Cyclic and acyclic polyamines as chelators of rhenium-186 and Rhenium-188 for therapeutic use
    journal, May 1996


    The one-pot synthesis and the fluorescence and cytotoxicity studies of chlorotricarbonyl(α-diimine)rhenium(I), fac-(CO)3(α-diimine)ReCl, complexes
    journal, September 2008

    • Orsa, Dejene K.; Haynes, Gregory K.; Pramanik, Saroj K.
    • Inorganic Chemistry Communications, Vol. 11, Issue 9
    • DOI: 10.1016/j.inoche.2008.05.033

    Correlative microXRF and optical immunofluorescence microscopy of adherent cells labeled with ultrasmall gold particles
    journal, July 2006


    Alkoxy bridged binuclear rhenium (I) complexes as a potential sensor for β-amyloid aggregation
    journal, December 2014


    Basic aqueous chemistry of [M(OH2)3(CO)3]+ (M=Re, Tc) directed towards radiopharmaceutical application
    journal, September 1999


    Novel Tat-Peptide Chelates for Direct Transduction of Technetium-99m and Rhenium into Human Cells for Imaging and Radiotherapy
    journal, November 2000

    • Polyakov, Valery; Sharma, Vijay; Dahlheimer, Julie L.
    • Bioconjugate Chemistry, Vol. 11, Issue 6
    • DOI: 10.1021/bc000008y

    Comprehensive Radiolabeling, Stability, and Tissue Distribution Studies of Technetium-99m Single Amino Acid Chelates (SAAC)
    journal, August 2009

    • Maresca, Kevin P.; Hillier, Shawn M.; Femia, Frank J.
    • Bioconjugate Chemistry, Vol. 20, Issue 8
    • DOI: 10.1021/bc900192b

    Protein and Peptide Labeling with (Cyclopentadienyl)tricarbonyl Rhenium and Technetium
    journal, November 1998

    • Spradau, Todd W.; Katzenellenbogen, John A.
    • Bioconjugate Chemistry, Vol. 9, Issue 6
    • DOI: 10.1021/bc980043t

    Uptake, Distribution, and Speciation of Selenoamino Acids by Human Cancer Cells: X-ray Absorption and Fluorescence Methods
    journal, March 2011

    • Weekley, Claire M.; Aitken, Jade B.; Vogt, Stefan
    • Biochemistry, Vol. 50, Issue 10
    • DOI: 10.1021/bi101678a

    Underestimated Potential of Organometallic Rhenium Complexes as Anticancer Agents
    journal, August 2014

    • Leonidova, Anna; Gasser, Gilles
    • ACS Chemical Biology, Vol. 9, Issue 10
    • DOI: 10.1021/cb500528c

    Therapeutic Radiopharmaceuticals
    journal, September 1999

    • Volkert, Wynn A.; Hoffman, Timothy J.
    • Chemical Reviews, Vol. 99, Issue 9
    • DOI: 10.1021/cr9804386

    {Re III Cl 3 } Core Complexes with Bifunctional Single Amino Acid Chelates
    journal, November 2002

    • Banerjee, Sangeeta Ray; Wei, Lihui; Levadala, Murali K.
    • Inorganic Chemistry, Vol. 41, Issue 22
    • DOI: 10.1021/ic020391d

    Synthesis, Structural, and Photophysical Investigation of Diimine Triscarbonyl Re(I) Tetrazolato Complexes.
    journal, February 2011

    • Werrett, Melissa V.; Chartrand, Daniel; Gale, Julian D.
    • Inorganic Chemistry, Vol. 50, Issue 4
    • DOI: 10.1021/ic1015516

    Biologically Compatible, Phosphorescent Dimetallic Rhenium Complexes Linked through Functionalized Alkyl Chains: Syntheses, Spectroscopic Properties, and Applications in Imaging Microscopy
    journal, January 2012

    • Balasingham, Rebeca G.; Thorp-Greenwood, Flora L.; Williams, Catrin F.
    • Inorganic Chemistry, Vol. 51, Issue 3
    • DOI: 10.1021/ic201654d

    Luminescent Rhenium(I)-Dipyrrinato Complexes
    journal, November 2011

    • McLean, Tracey M.; Moody, Janice L.; Waterland, Mark R.
    • Inorganic Chemistry, Vol. 51, Issue 1
    • DOI: 10.1021/ic201877t

    Fluorescent Rhenium-Naphthalimide Conjugates as Cellular Imaging Agents
    journal, March 2014

    • Langdon-Jones, Emily E.; Symonds, Nadine O.; Yates, Sara E.
    • Inorganic Chemistry, Vol. 53, Issue 7
    • DOI: 10.1021/ic500142z

    Measurement of photoluminescence quantum yields. Review
    journal, April 1971

    • Crosby, Glenn A.; Demas, James N.
    • The Journal of Physical Chemistry, Vol. 75, Issue 8, p. 991-1024
    • DOI: 10.1021/j100678a001

    A Nonemissive Iridium(III) Complex That Specifically Lights-Up the Nuclei of Living Cells
    journal, July 2011

    • Li, Chunyan; Yu, Mengxiao; Sun, Yun
    • Journal of the American Chemical Society, Vol. 133, Issue 29
    • DOI: 10.1021/ja202344c

    Metabolism of Selenite in Human Lung Cancer Cells: X-Ray Absorption and Fluorescence Studies
    journal, November 2011

    • Weekley, Claire M.; Aitken, Jade B.; Vogt, Stefan
    • Journal of the American Chemical Society, Vol. 133, Issue 45
    • DOI: 10.1021/ja206203c

    Organometallic Anticancer Compounds
    journal, January 2011

    • Gasser, Gilles; Ott, Ingo; Metzler-Nolte, Nils
    • Journal of Medicinal Chemistry, Vol. 54, Issue 1
    • DOI: 10.1021/jm100020w

    Ultrafast Excited-State Dynamics of [Re(L)(CO) 3 (bpy)] n Complexes: Involvement of the Solvent
    journal, May 2010

    • El Nahhas, Amal; Cannizzo, Andrea; van Mourik, Frank
    • The Journal of Physical Chemistry A, Vol. 114, Issue 22
    • DOI: 10.1021/jp101999m

    Rhenium fac tricarbonyl bisimine complexes: biologically useful fluorochromes for cell imaging applications
    journal, January 2007

    • Amoroso, Angelo J.; Coogan, Michael P.; Dunne, Jennifer E.
    • Chem. Commun., Issue 29
    • DOI: 10.1039/b706657k

    Application of d6 transition metal complexes in fluorescence cell imaging
    journal, January 2010

    • Fernández-Moreira, Vanesa; Thorp-Greenwood, Flora L.; Coogan, Michael P.
    • Chem. Commun., Vol. 46, Issue 2
    • DOI: 10.1039/b917757d

    Silicon nitride as a versatile growth substrate for microspectroscopic imaging and mapping of individual cells
    journal, January 2010

    • Carter, Elizabeth A.; Rayner, Benjamin S.; McLeod, Andrew I.
    • Molecular BioSystems, Vol. 6, Issue 7
    • DOI: 10.1039/c001499k

    Complexes in context: Attempting to control the cellular uptake and localisation of rhenium fac-tricarbonyl polypyridyl complexes
    journal, January 2011

    • Balasingham, Rebeca G.; Coogan, Michael P.; Thorp-Greenwood, Flora L.
    • Dalton Transactions, Vol. 40, Issue 44
    • DOI: 10.1039/c1dt11219h

    Applications of luminescent inorganic and organometallic transition metal complexes as biomolecular and cellular probes
    journal, January 2012

    • Lo, Kenneth Kam-Wing; Choi, Alex Wing-Tat; Law, Wendell Ho-Tin
    • Dalton Transactions, Vol. 41, Issue 20
    • DOI: 10.1039/c2dt11892k

    Distinct cellular fates for KP1019 and NAMI-A determined by X-ray fluorescence imaging of single cells
    journal, January 2012

    • Aitken, Jade B.; Antony, Sumy; Weekley, Claire M.
    • Metallomics, Vol. 4, Issue 10
    • DOI: 10.1039/c2mt20072d

    Subcellular redistribution and mitotic inheritance of transition metals in proliferating mouse fibroblast cells
    journal, January 2013

    • McRae, Reagan; Lai, Barry; Fahrni, Christoph J.
    • Metallomics, Vol. 5, Issue 1
    • DOI: 10.1039/c2mt20176c

    Progress with, and prospects for, metal complexes in cell imaging
    journal, January 2014

    • Coogan, Michael P.; Fernández-Moreira, Vanesa
    • Chem. Commun., Vol. 50, Issue 4
    • DOI: 10.1039/c3cc45229h

    XAS and XFM studies of selenium and copper speciation and distribution in the kidneys of selenite-supplemented rats
    journal, January 2014

    • Weekley, Claire M.; Shanu, Anu; Aitken, Jade B.
    • Metallomics, Vol. 6, Issue 9
    • DOI: 10.1039/c4mt00088a

    Modulation of the organelle specificity in Re( i ) tetrazolato complexes leads to labeling of lipid droplets
    journal, January 2014

    • Bader, Christie A.; Brooks, Robert D.; Ng, Yeap S.
    • RSC Adv., Vol. 4, Issue 31
    • DOI: 10.1039/c4ra00050a

    Rhenium tetrazolato complexes coordinated to thioalkyl-functionalised phenanthroline ligands: synthesis, photophysical characterisation, and incubation in live HeLa cells
    journal, January 2015

    • Werrett, Melissa V.; Wright, Phillip J.; Simpson, Peter V.
    • Dalton Transactions, Vol. 44, Issue 47
    • DOI: 10.1039/c5dt03470a

    Unprecedented staining of polar lipids by a luminescent rhenium complex revealed by FTIR microspectroscopy in adipocytes
    journal, January 2016

    • Bader, C. A.; Carter, E. A.; Safitri, A.
    • Molecular BioSystems, Vol. 12, Issue 7
    • DOI: 10.1039/c6mb00242k

    Fluorescence probes for prokaryotic and eukaryotic cells using Re(CO) 3 + complexes with an electron withdrawing ancillary ligand
    journal, January 2016

    • Carreño, A.; Gacitúa, M.; Fuentes, J. A.
    • New Journal of Chemistry, Vol. 40, Issue 9
    • DOI: 10.1039/c6nj00905k

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      Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.