Heparan sulfate disaccharide measurement from biological samples using pre-column derivatization, UPLC-MS and single ion monitoring

Article


Antia, I., Yagnik, D., Pantoja Munoz, L., Shah, A. and Hills, F. 2017. Heparan sulfate disaccharide measurement from biological samples using pre-column derivatization, UPLC-MS and single ion monitoring. Analytical Biochemistry. 530, pp. 17-30. https://doi.org/10.1016/j.ab.2017.04.019
TypeArticle
TitleHeparan sulfate disaccharide measurement from biological samples using pre-column derivatization, UPLC-MS and single ion monitoring
AuthorsAntia, I., Yagnik, D., Pantoja Munoz, L., Shah, A. and Hills, F.
Abstract

Glycosaminoglycans are a heterogeneous family of linear polysaccharides comprised of repeating disaccharide subunits that mediate many effects at the cellular level. There is increasing evidence that the nature of these effects is determined by differences in disaccharide composition. However, the determination of GAG disaccharide composition in biological samples remains challenging and time-consuming. We have developed a method that uses derivatization and selected ion recording and RP-UPLCMS resulting in rapid separation and quantification of twelve heparin/heparin sulfate disaccharides from 5 μg GAG. Limits of detection and quantitation were 0.02–0.15 and 0.07–0.31 μg/ml respectively. We have applied this method to the novel analysis of disaccharide levels extracted from heparan sulfate and human cancer cell lines. Heparan sulfate disaccharides extracted from biological samples following actinase and heparinase incubation and derivatized using reductive amination with 2-aminoacridone. Derivatized disaccharides were analyzed used UPLC-MS with single ion monitoring. Eight HS disaccharide subunits were separated and quantified from HS and cell lines in eleven minutes per sample. In all samples the most abundant subunits present were the unsulfated ΔUA-GlcNAc, ΔUA-GlcNAc,6S and ΔUA,2S-GlcNS,6S. There was considerable variation in the proportions and concentrations of disaccharides between different cell lines. Further studies are needed to examine the significance of these differences.

KeywordsHeparan sulfate; Cancer cell lines; Glycosaminoglycan; Proteoglycan; 2-aminoacridone; RP-UPLC-MS
Research GroupBiomarkers for Cancer group
LanguageEnglish
PublisherElsevier
JournalAnalytical Biochemistry
ISSN0003-2697
Electronic1096-0309
Publication dates
Online30 Apr 2017
Print01 Aug 2017
Publication process dates
Deposited05 May 2017
Accepted27 Apr 2017
Submitted24 Jan 2017
Output statusPublished
Accepted author manuscript
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Copyright Statement

© 2017. This author's accepted manuscript version is made available under the CC-BY-NC-ND 4.0 license http://creativecommons.org/licenses/by-nc-nd/4.0/

Digital Object Identifier (DOI)https://doi.org/10.1016/j.ab.2017.04.019
Web of Science identifierWOS:000404077200004
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Wilson, L., Cockburn, E., Paice, K., Sinclair, S., Faki, T., Hills, F., Gondek, M., Wood, A. and Dimitriou, L. 2018. Recovery following a marathon: a comparison of cold water immersion, whole body cryotherapy and a placebo control. European Journal of Applied Physiology. 118 (1), pp. 153-163. https://doi.org/10.1007/s00421-017-3757-z
High performance liquid chromatography of non-protein amino acids extracted from Acacia seeds
Shah, A., Younie, D., Adlard, M. and Evans, C. 1992. High performance liquid chromatography of non-protein amino acids extracted from Acacia seeds. Phytochemical Analysis. 3 (1), pp. 20-25. https://doi.org/10.1002/pca.2800030104
Non-protein amino acids in seeds of neotropical species of acacia
Evans, C., Shah, A., Adlard, M. and Arce, M. 1992. Non-protein amino acids in seeds of neotropical species of acacia. Phytochemistry. 32 (1), pp. 123-126. https://doi.org/10.1016/0031-9422(92)80116-V
Development of colorimetric method for the detection of amines bound to solid support
Shah, A., de Biasi, V., Camilleri, P. and Rahman, S. 1997. Development of colorimetric method for the detection of amines bound to solid support. Analytical Communications. 34 (11), pp. 325-328. https://doi.org/10.1039/A705630C
Development of a spectrophotometric method for the measurement of thiols at trace levels
Shah, A., de Biasi, V. and Camilleri, P. 1995. Development of a spectrophotometric method for the measurement of thiols at trace levels. Analytical Proceedings including Analytical Communications. 32 (4), pp. 149-153. https://doi.org/10.1039/AI9953200149
Capillary electrophoresis in the pharmaceutical industry: applications in discovery and chemical development
Hadley, M., Gilges, M., Senior, J., Shah, A. and Camilleri, P. 2000. Capillary electrophoresis in the pharmaceutical industry: applications in discovery and chemical development. Journal of Chromatography B: Biomedical Sciences and Applications. 745 (1), pp. 177-188. https://doi.org/10.1016/S0378-4347(00)00153-5
Development of a protocol for the automated analysis of amino acids in brain tissue samples and microdialysates
Shah, A., de Biasi, V., Taylor, S., Roberts, C., Hemmati, P., Munton, R., West, A., Routledge, C. and Camilleri, P. 1999. Development of a protocol for the automated analysis of amino acids in brain tissue samples and microdialysates. Journal of Chromatography B: Biomedical Sciences and Applications. 735 (2), pp. 133-140. https://doi.org/10.1016/S0378-4347(99)00403-X
Orexin A activates locus coeruleus cell firing and increases arousal in the rat
Hagan, J., Leslie, R., Patel, S., Evans, M., Wattam, T., Holmes, S., Benham, C., Taylor, S., Routledge, C., Hemmati, P., Munton, R., Ashmeade, T., Shah, A., Hatcher, J., Hatcher, P., Jones, D., Smith, M., Piper, D., Hunter, A., Porter, R. and Upton, N. 1999. Orexin A activates locus coeruleus cell firing and increases arousal in the rat. Proceedings of the National Academy of Sciences. 96 (19), pp. 10911-10916. https://doi.org/10.1073/pnas.96.19.10911
Amino acid neurotransmitters: separation approaches and diagnostic value
Shah, A., Crespi, F. and Heidbreder, C. 2002. Amino acid neurotransmitters: separation approaches and diagnostic value. Journal of Chromatography B. 781 (1-2), pp. 151-163. https://doi.org/10.1016/S1570-0232(02)00621-9
High-performance liquid chromatography/tandem mass spectrometry assay for the determination of 1-methyl-4-phenyl pyridinium (MPP+) in brain tissue homogenates
Hows, M., Ashmeade, T., Billinton, A., Perren, M., Austin, A., Virley, D., Organ, A. and Shah, A. 2004. High-performance liquid chromatography/tandem mass spectrometry assay for the determination of 1-methyl-4-phenyl pyridinium (MPP+) in brain tissue homogenates. Journal of Neuroscience Methods. 137 (2), pp. 221-226. https://doi.org/10.1016/j.jneumeth.2004.02.011
High-performance liquid chromatography/tandem mass spectrometric assay for the simultaneous measurement of dopamine, norepinephrine, 5-hydroxytryptamine and cocaine in biological samples
Hows, M., Lacroix, L., Heidbreder, C., Organ, A. and Shah, A. 2004. High-performance liquid chromatography/tandem mass spectrometric assay for the simultaneous measurement of dopamine, norepinephrine, 5-hydroxytryptamine and cocaine in biological samples. Journal of Neuroscience Methods. 138 (1-2), pp. 123-132. https://doi.org/10.1016/j.jneumeth.2004.03.021
Rapid high-throughput assay for the measurement of amino acids from microdialysates and brain tissue using monolithic C18-bonded reversed-phase columns
Dawson, L., Organ, A., Winter, P., Lacroix, L., Shilliam, C., Heidbreder, C. and Shah, A. 2004. Rapid high-throughput assay for the measurement of amino acids from microdialysates and brain tissue using monolithic C18-bonded reversed-phase columns. Journal of Chromatography B. 807 (2), pp. 235-241. https://doi.org/10.1016/j.jchromb.2004.04.012
Selective antagonism at dopamine D3 receptors enhances monoaminergic and cholinergic neurotransmission in the rat anterior cingulate cortex
Lacroix, L., Hows, M., Shah, A., Hagan, J. and Heidbreder, C. 2003. Selective antagonism at dopamine D3 receptors enhances monoaminergic and cholinergic neurotransmission in the rat anterior cingulate cortex. Neuropsychopharmacology. 28, pp. 839-849. https://doi.org/10.1038/sj.npp.1300114
High-performance liquid chromatography/tandem mass spectrometry assay for the rapid high sensitivity measurement of basal acetylcholine from microdialysates
Hows, M., Organ, A., Murray, S., Dawson, L., Foxton, R., Heidbreder, C., Hughes, Z., Lacroix, L. and Shah, A. 2002. High-performance liquid chromatography/tandem mass spectrometry assay for the rapid high sensitivity measurement of basal acetylcholine from microdialysates. Journal of Neuroscience Methods. 121 (1), pp. 33-39. https://doi.org/10.1016/S0165-0270(02)00228-5
Increased responsiveness of dopamine to atypical, but not typical antipsychotics in the medial prefrontal cortex of rats reared in isolation
Heidbreder, C., Foxton, R., Cilia, J., Hughes, Z., Shah, A., Atkins, A., Hunter, J., Hagan, J. and Jones, D. 2001. Increased responsiveness of dopamine to atypical, but not typical antipsychotics in the medial prefrontal cortex of rats reared in isolation. Psychopharmacology. 156 (2-3), pp. 338-351. https://doi.org/10.1007/s002130100760
Development of a high-pressure gradient pumping system for parallel liquid chromatography/mass spectrometry for the analysis of combinatorial libraries
Tolson, D., Organ, A. and Shah, A. 2001. Development of a high-pressure gradient pumping system for parallel liquid chromatography/mass spectrometry for the analysis of combinatorial libraries. Rapid Communications in Mass Spectrometry. 15 (14), pp. 1244-1249. https://doi.org/10.1002/rcm.359
The evaluation of interdigitated array electrodes for the measurement of catecholamines and indoleamines
Senior, J., Shah, A., Monteux, C. and de Biasi, V. 2001. The evaluation of interdigitated array electrodes for the measurement of catecholamines and indoleamines. Journal of Pharmaceutical and Biomedical Analysis. 24 (5-6), pp. 843-848. https://doi.org/10.1016/S0731-7085(00)00551-3
Development and application of a sensitive high performance ion-exchange chromatography method for the simultaneous measurement of dopamine, 5-hydroxytryptamine and norepinephrine in microdialysates from the rat brain
Heidbreder, C., Lacroix, L., Atkins, A., Organ, A., Murray, S., West, A. and Shah, A. 2001. Development and application of a sensitive high performance ion-exchange chromatography method for the simultaneous measurement of dopamine, 5-hydroxytryptamine and norepinephrine in microdialysates from the rat brain. Journal of Neuroscience Methods. 112 (2), pp. 135-144. https://doi.org/10.1016/S0165-0270(01)00460-5
Determination of β-lactams and their biosynthetic intermediates in fermentation media by pre-column derivatisation followed by fluorescence detection
Shah, A. and Adlard, M. 1988. Determination of β-lactams and their biosynthetic intermediates in fermentation media by pre-column derivatisation followed by fluorescence detection. Journal of Chromatography B: Biomedical Sciences and Applications. 424, pp. 325-336. https://doi.org/10.1016/S0378-4347(00)81109-3
Evaluation of expression and function of the H+/myo-inositol transporter HMIT;
Di Daniel, E., Mok, S., Mead, E., Mutinelli, C., Zambello, E., Caberlotto, L., Pell, T., Langmead, C., Shah, A., Duddy, G., Kew, J. and Maycox, P. 2009. Evaluation of expression and function of the H+/myo-inositol transporter HMIT; BMC Cell Biology. 10. https://doi.org/10.1186/1471-2121-10-54
Platelet activating acetylhydrolase involved in inflammation resolution in macrophages and neutrophils which have been stimulated with urate crystals
Yagnik, D. 2015. Platelet activating acetylhydrolase involved in inflammation resolution in macrophages and neutrophils which have been stimulated with urate crystals. The 12th World Congress on Inflammation. Boston, USA 08 - 12 Aug 2015 Springer. https://doi.org/10.1007/s00011-015-0839-4
Elucidating the intra-species proteotypes of pseudomonas aeruginosa from cystic fibrosis
Olkun, A., Shah, A. and Shah, H. 2017. Elucidating the intra-species proteotypes of pseudomonas aeruginosa from cystic fibrosis. in: Shah, H. and Gharbia, S. (ed.) MALDI-TOF and Tandem MS for Clinical Microbiology Oxford, UK Wiley. pp. 579-592
Subtyping of Staphylococcus spp. Based upon MALDI-TOF MS data analysis
Xu, Z., Olkun, A., Vranckx, K., Mkrtchyan, H., Shah, A., Pot, B., Cutler, R. and Shah, H. 2017. Subtyping of Staphylococcus spp. Based upon MALDI-TOF MS data analysis. in: Shah, H. and Gharbia, S. (ed.) MALDI-TOF and Tandem MS for Clinical Microbiology Oxford, UK Wiley. pp. 563-578
Determination of antimicrobial resistance using tandem mass spectrometry
Shah, A., Serafim, V., Xu, Z., Mkrtchyan, H. and Shah, H. 2017. Determination of antimicrobial resistance using tandem mass spectrometry. in: Shah, H. and Gharbia, S. (ed.) MALDI-TOF and Tandem MS for Clinical Microbiology Oxford, UK Wiley. pp. 399-418
Microbial DNA analysis by MALDI-TOF mass spectrometry
Honisch, C., Serafim, V., Hennessy, N., Allen, D., Ring, C., Pantoja Munoz, L., Gharbia, S., Shah, A. and Shah, H. 2017. Microbial DNA analysis by MALDI-TOF mass spectrometry. in: Shah, H. and Gharbia, S. (ed.) MALDI-TOF and Tandem MS for Clinical Microbiology Oxford Wiley. pp. 187-209
A study of the inhibition of biofilm formation on multiple surfaces by a biosurfactant containing four discrete lipopeptides
Khonsari, S., Gonzalez Baez, A., Nguyen, H., Pantoja Munoz, L. and Purchase, D. 2017. A study of the inhibition of biofilm formation on multiple surfaces by a biosurfactant containing four discrete lipopeptides. Microbiology Society Annual Conference. Edinburgh, United Kingdom 03 - 06 Apr 2017
Competition intensity and fatigue in elite fencing
Turner, A., Kilduff, L., Mrashall, G., Phillips, J., Noto, A., Buttigeig, C., Gondek, M., Hills, F. and Dimitriou, L. 2017. Competition intensity and fatigue in elite fencing. The Journal of Strength and Conditioning Research. 31 (11), pp. 3128-3136. https://doi.org/10.1519/JSC.0000000000001758
Influence of cold water immersion and cherry juice on recovery following a 42.2km trail run
Paice, K., Dimitriou, L., Wilson, L., Hills, F., Sinclair, S., Gondek, M., Kwan, X. and Wood, A. 2017. Influence of cold water immersion and cherry juice on recovery following a 42.2km trail run. BASES Conference 2017. Nottingham, UK 28 - 29 Nov 2017 Taylor and Francis. pp. s92 https://doi.org/10.1080/02640414.2017.1378421
Classification of cancer cell lines using matrix-assisted laser desorption/ionization time-of-flight mass spectrometry and statistical analysis
Serafim, V., Shah, A., Puiu, M., Andreescu, N., Coricovac, D., Nosyrev, A., Spandidos, D., Tsatsakis, A., Dehelean, C. and Pinzaru, I. 2017. Classification of cancer cell lines using matrix-assisted laser desorption/ionization time-of-flight mass spectrometry and statistical analysis. International Journal of Molecular Medicine. 40 (4), pp. 1096-1104. https://doi.org/10.3892/ijmm.2017.3083
Rapid identification of E. coli bacteriophages using mass spectrometry
Serafim, V., Ring, C., Pantoja Munoz, L., Shah, H. and Shah, A. 2017. Rapid identification of E. coli bacteriophages using mass spectrometry. Journal of Proteomics and Enzymology. 6 (1), pp. 1-5. https://doi.org/10.4172/2470-1289.1000130
Detection of the tau protein in human serum by a sensitive four-electrode electrochemical biosensor
Wang, S., Acha, D., Shah, A., Hills, F., Roitt, I., Demosthenous, A. and Bayford, R. 2017. Detection of the tau protein in human serum by a sensitive four-electrode electrochemical biosensor. Biosensors and Bioelectronics. 92, pp. 482-488. https://doi.org/10.1016/j.bios.2016.10.077
The mechanisms of detoxification of As(III), dimethylarsinic acid (DMA) and As(V) in the microalga Chlorella vulgaris
Pantoja Munoz, L., Purchase, D., Jones, H., Raab, A., Urgast, D., Feldmann, J. and Garelick, H. 2016. The mechanisms of detoxification of As(III), dimethylarsinic acid (DMA) and As(V) in the microalga Chlorella vulgaris. Aquatic Toxicology. 175, pp. 56-72. https://doi.org/10.1016/j.aquatox.2016.02.020
Therapeutic potential of delivering arsenic trioxide into HPV-infected cervical cancer cells using liposomal nanotechnology
Wang, X., Li, D., Ghali, L., Xia, R., Pantoja Munoz, L., Garelick, H., Bell, C. and Wen, S. 2016. Therapeutic potential of delivering arsenic trioxide into HPV-infected cervical cancer cells using liposomal nanotechnology. Nanoscale Research Letters. 11 (1), pp. 1-8. https://doi.org/10.1186/s11671-016-1307-y
Consideration of the bioavailability of metal/metalloid species in freshwaters: experiences regarding the implementation of biotic ligand model-based approaches in risk assessment frameworks
Rüdel, H., Diaz Muñiz, C., Garelick, H., Kandile, N., Miller, B., Pantoja Munoz, L., Peijnenburg, W., Purchase, D., Shevah, Y., Van Sprang, P., Vijer, M. and Vink, J. 2015. Consideration of the bioavailability of metal/metalloid species in freshwaters: experiences regarding the implementation of biotic ligand model-based approaches in risk assessment frameworks. Environmental Science and Pollution Research. 22 (10), pp. 7405-7421. https://doi.org/10.1007/s11356-015-4257-5
Determination of urinary cortisol, cortisone and 6-sulfatoxymelatonin using dilute and shoot ultra-high pressure liquid chromatography-tandem mass spectrometry
Sniecinska-Cooper, A., Shah, A., Dimitriou, D., Iles, R., Butler, S. and Bayford, R. 2015. Determination of urinary cortisol, cortisone and 6-sulfatoxymelatonin using dilute and shoot ultra-high pressure liquid chromatography-tandem mass spectrometry. Journal of Chromatography B. 978-79, pp. 18-23. https://doi.org/10.1016/j.jchromb.2014.11.016
The role of vitamin In type 2 diabetes
Ali, A., Appiah, S., Shah, A. and Ghali, L. 2014. The role of vitamin In type 2 diabetes. Middlesex University Postgraduate Summer Conference. London, UK 19 Jun 2014
The mechanisms of arsenic detoxification by the green microalgae chlorella vulgaris
Pantoja Munoz, L. 2014. The mechanisms of arsenic detoxification by the green microalgae chlorella vulgaris. PhD thesis Middlesex University Science and Technology
Macrophage derived platelet activating factor implicated in the resolution phase of gouty inflammation
Yagnik, D. 2014. Macrophage derived platelet activating factor implicated in the resolution phase of gouty inflammation. International Journal of Inflammation. 2014, pp. 1-6. https://doi.org/10.1155/2014/526496
The mechanisms of arsenic bioremediation from water by the green microalgae Chlorella vulgaris
Pantoja Munoz, L., Purchase, D., Jones, H., Feldmann, J. and Garelick, H. 2014. The mechanisms of arsenic bioremediation from water by the green microalgae Chlorella vulgaris. THE BNASS / TraceSpec Tandem Conference. Aberdeen, Scotland, UK 31 Aug - 04 Sep 2014
The removal of arsenate from water using iron-modified diatomite (D-Fe): isotherm and column experiments
Pantoja Munoz, L., Jones, H., Garelick, H., Mohamedbakr, H. and Burkitbayev, M. 2014. The removal of arsenate from water using iron-modified diatomite (D-Fe): isotherm and column experiments. Environmental Science and Pollution Research. 21 (1), pp. 495-506. https://doi.org/10.1007/s11356-013-1891-7
Enhanced determination of As-phytochelatin complexes in Chlorella vulgaris using focused sonication for extraction of water-soluble species
Pantoja Munoz, L., Purchase, D., Jones, H., Feldmann, J. and Garelick, H. 2014. Enhanced determination of As-phytochelatin complexes in Chlorella vulgaris using focused sonication for extraction of water-soluble species. Analytical Methods. 6 (3), pp. 791-797. https://doi.org/10.1039/C3AY41629A
Placental syndecan-1 and sulphated glycosaminoglycans are decreased in preeclampsia
Heyer-Chauhan, N., Ovbude, I., Hills, A., Sullivan, M. and Hills, F. 2013. Placental syndecan-1 and sulphated glycosaminoglycans are decreased in preeclampsia. Journal of Perinatal Medicine. https://doi.org/10.1515/jpm-2013-0097
Chronic fluoxetine differentially modulates the hippocampal microtubular and serotonergic system in grouped and isolation reared rats
Bianchi, M., Fone, K., Shah, A., Atkins, A., Dawson, L., Heidbreder, C., Hagan, J. and Marsden, C. 2009. Chronic fluoxetine differentially modulates the hippocampal microtubular and serotonergic system in grouped and isolation reared rats. European Neuropsychopharmacology. 19 (11), pp. 778-790. https://doi.org/10.1016/j.euroneuro.2009.06.005
IGFBP-1 in the placenta, membranes and fetal circulation: levels at term and preterm delivery
Hills, F., Gunn, L., Hardiman, P., Thanaratnam, S. and Chard, T. 1996. IGFBP-1 in the placenta, membranes and fetal circulation: levels at term and preterm delivery. Early Human Development. 44 (1), pp. 71-76.
A high-performance liquid chromatography/tandem mass spectrometry assay for the simultaneous measurement of acetylcholine and clozapine in microdialysis samples
Shah, A. 2013. A high-performance liquid chromatography/tandem mass spectrometry assay for the simultaneous measurement of acetylcholine and clozapine in microdialysis samples. Journal of Chromatography A.
Fluoxetine administration modulates the cytoskeletal microtubular system in the rat hippocampus
Bianchi, M., Shah, A., Fone, K., Atkins, A., Dawson, L., Heidbreder, C., Hows, M., Hagan, J. and Marsden, C. 2009. Fluoxetine administration modulates the cytoskeletal microtubular system in the rat hippocampus. Synapse. 63 (4), pp. 359-364. https://doi.org/10.1002/syn.20614
Effects of N-acetylaspartylglutamate (NAAG) at group II mGluRs and NMDAR
Fricker, A., Mok, M., De la Flor, R., Shah, A., Woolley, M., Dawson, L. and Kew, J. 2009. Effects of N-acetylaspartylglutamate (NAAG) at group II mGluRs and NMDAR. Neuropharmacology. 56 (6-7), pp. 1060-1067. https://doi.org/10.1016/j.neuropharm.2009.03.002
Development and application of a liquid chromatography/tandem mass spectrometric assay for measurement of N-acetylaspartate, N-acetylaspartylglutamate and glutamate in brain slice superfusates and tissue extracts
Shah, A., De la Flor, R., Atkins, A., Slone-Murphy, J. and Dawson, L. 2008. Development and application of a liquid chromatography/tandem mass spectrometric assay for measurement of N-acetylaspartate, N-acetylaspartylglutamate and glutamate in brain slice superfusates and tissue extracts. Journal of Chromatography B. 876 (2), pp. 153-158. https://doi.org/10.1016/j.jchromb.2008.10.012
Development of Zwitterionic Hydrophilic Liquid Chromatography (ZICⓇHILIC-MS) metabolomics method for Shotgun analysis of human urine
Trivedi, D., Jones, H., Shah, A. and Iles, R. 2012. Development of Zwitterionic Hydrophilic Liquid Chromatography (ZICⓇHILIC-MS) metabolomics method for Shotgun analysis of human urine. Journal of Chromatography & Separation Techniques. 03 (06). https://doi.org/10.4172/2157-7064.1000144
Differential proteolysis of insulin-like growth factor binding protein-1 (IGFBP-1) in pregnancy
Hills, F., Iles, R. and Sullivan, M. 2013. Differential proteolysis of insulin-like growth factor binding protein-1 (IGFBP-1) in pregnancy. Journal of Perinatal Medicine. 41 (3), pp. 241-249. https://doi.org/10.1515/jpm-2012-0086
Insulin-like growth factor-II and heparin are anti-apoptotic survival factors in human villous cytotrophoblast
Hills, F., Mehmet, H. and Sullivan, M. 2012. Insulin-like growth factor-II and heparin are anti-apoptotic survival factors in human villous cytotrophoblast. European Journal of Obstetrics, Gynecology, and Reproductive Biology. 163 (1), pp. 11-16. https://doi.org/10.1016/j.ejogrb.2012.03.013
Superovulation, IGFBP-1 and birth weight.
Johnson, M., Irvine, R., Hills, F., Bolton, V., Abbas, A., Brooks, A., Allman, A., Chard, T. and Nicolaides, K. 1995. Superovulation, IGFBP-1 and birth weight. European Journal of Obstetrics, Gynaecology and Reproductive Biology. 59 (2), pp. 193-195.
The effects of labor on maternal and fetal levels of insulin-like growth factor binding protein-1
Hills, F., Crawford, R., Harding, S., Farkas, F. and Chard, T. 1994. The effects of labor on maternal and fetal levels of insulin-like growth factor binding protein-1. American Journal of Obstetrics and Gynecology. 171 (5), pp. 1292-1295.
Insulin-related growth factor binding protein-1 levels in ovum donation pregnancies.
Brooks, A., Johnson, M., Hills, F., Chard, T., Irvine, R. and Abdalla, H. 1995. Insulin-related growth factor binding protein-1 levels in ovum donation pregnancies. European Journal of Obstetrics, Gynaecology and Reproductive Biology. 59 (1), pp. 91-94.
Elevated levels of insulin-like growth factor binding protein-1 in fetal distress.
Crawford, R., Hills, F., Farkas, A. and Chard, T. 1995. Elevated levels of insulin-like growth factor binding protein-1 in fetal distress. British Journal of Obstetrics and Gynaecology. 102 (7), pp. 538-540.
Lack of evidence for a circadian rhythm of IGFBP-1 in the mother and fetus during labour.
Harding, S., Mensah, A., Hills, F., Howell, R. and Chard, T. 1995. Lack of evidence for a circadian rhythm of IGFBP-1 in the mother and fetus during labour. British Journal of Obstetrics and Gynaecology. 102 (11), pp. 891-893.
Raised circulating levels of interleukin-6 in women with an intrauterine contraceptive device.
Wolley, J., Saleem, S., Hills, F., Salem, H., El-Nashar, E. and Chard, T. 1996. Raised circulating levels of interleukin-6 in women with an intrauterine contraceptive device. Gynecologic and Obstetric Investigation. 42 (4), pp. 241-243.
Circulating levels of IGF-I and IGF-binding protein-1 throughout pregnancy: relation to birthweight and maternal weight.
Hills, F., English, J. and Chard, T. 1996. Circulating levels of IGF-I and IGF-binding protein-1 throughout pregnancy: relation to birthweight and maternal weight. Journal of Endocrinology. 148 (2), pp. 303-309. https://doi.org/10.1677/joe.0.1480303
Mechanism of action of the intrauterine contraceptive device: evidence for a specific biochemical deficiency in the endometrium.
Seleem, S., Hills, F., Salem, H., El-Nashar, E. and Chard, T. 1996. Mechanism of action of the intrauterine contraceptive device: evidence for a specific biochemical deficiency in the endometrium. Human Reproduction. 11 (6), pp. 1220-1222.
Antenatal dexamethasone therapy does not affect circulating concentrations of insulin-like growth factor binding protein-1.
Ogueh, O., Hills, F., Chard, T. and Johnson, M. 1998. Antenatal dexamethasone therapy does not affect circulating concentrations of insulin-like growth factor binding protein-1. Human Reproduction. 13 (6), pp. 1714-1716. https://doi.org/10.1093/humrep/13.6.1714
Effects of co-trimoxazole, erythromycin, amoxycillin, tetracycline and chloroquine on sperm function in vitro
Hargreaves, C., Rogers, S., Hills, F., Rahman, F., Howell, R. and Homa, S. 1998. Effects of co-trimoxazole, erythromycin, amoxycillin, tetracycline and chloroquine on sperm function in vitro. Human Reproduction. 13 (7), pp. 1878-1886.
Reciprocal imprinting of human GRB10 in placental trophoblast and brain: evolutionary conservation of reversed allelic expression
Monk, D., Arnaud, P., Frost, J., Hills, F., Stanier, P., Feil, R. and Moore, G. 2009. Reciprocal imprinting of human GRB10 in placental trophoblast and brain: evolutionary conservation of reversed allelic expression. Human Molecular Genetics. 18 (16), pp. 3066-3074. https://doi.org/10.1093/hmg/ddp248
Heparin prevents programmed cell death in human trophoblast
Hills, F., Abrahams, V., Gonzalez-Timon, B., Francis, J., Cloke, B., Hinkson, L., Rai, R., Regan, L., Mor, G., Sullivan, M., Lam, E. and Brosens, J. 2006. Heparin prevents programmed cell death in human trophoblast. Molecular Human Reproduction. 12 (4), pp. 237-242.
A longitudinal study of maternal plasma insulin-like growth factor binding protein-1 concentrations during normal pregnancy and pregnancies complicated by pre-eclampsia
Anim-Nyame, N., Hills, F., Soorana, S., Steer, P. and Johnson, M. 2000. A longitudinal study of maternal plasma insulin-like growth factor binding protein-1 concentrations during normal pregnancy and pregnancies complicated by pre-eclampsia. Human Reproduction. 15 (10), pp. 2215-2219. https://doi.org/10.1093/humrep/15.10.2215
Interactions between progesterone receptor isoforms in myometrial cells in human labour
Pieber, D., Allport, V., Hills, F., Johnson, M. and Bennett, P. 2001. Interactions between progesterone receptor isoforms in myometrial cells in human labour. Molecular Human Reproduction. 7 (9), pp. 875-879. https://doi.org/10.1093/molehr/7.9.875
Regulated expression of signal transducer and activator of transcription, Stat5, and its enhancement of PRL expression in human endometrial stromal cells in vitro
Mak, I., Brosens, J., Christian, M., Hills, F., Chamley, L., Regan, L. and White, J. 2002. Regulated expression of signal transducer and activator of transcription, Stat5, and its enhancement of PRL expression in human endometrial stromal cells in vitro. Journal of Clinical Endocrinology and Metabolism. 87 (6), pp. 2581-2588. https://doi.org/10.1210/jc.87.6.2581
Progesterone represses interleukin-8 and cyclo-oxygenase-2 in human lower segment fibroblast cells and amnion epithelial cells
Loudon, J., Elliott, C., Hills, F. and Bennett, P. 2003. Progesterone represses interleukin-8 and cyclo-oxygenase-2 in human lower segment fibroblast cells and amnion epithelial cells. Biology of Reproduction. 69 (1), pp. 331-337.
The relationship between insulin and insulin-like growth factor binding protein-1 is modified by pre-eclampsia.
Anim-Nyame, N., Hills, F., Soorana, S., Steer, P. and Johnson, M. 2003. The relationship between insulin and insulin-like growth factor binding protein-1 is modified by pre-eclampsia. Gynecological endocrinology.. 17 (6), pp. 471-476. https://doi.org/10.1080/09513590312331290408
The insulin-like growth factor system in mammalian pregnancy: a workshop report
Carter, A., Hills, F., O'Gorman, D., Robets, C., Soorana, S., Watson, C. and Westwood, M. 2004. The insulin-like growth factor system in mammalian pregnancy: a workshop report. Placenta. 25 (Supple), pp. S53-S56. https://doi.org/10.1016/j.placenta.2004.01.019
Imprinting of IGF2 P0 transcript and novel alternatively spliced INS-IGF2 isoforms show differences between mouse and human
Monk, D., Sanches, R., Arnaud, P., Apostolidou, S., Hills, F., Abu-Amero, S., Murrell, A., Friess, H., Reik, W. and Stanier, P. 2006. Imprinting of IGF2 P0 transcript and novel alternatively spliced INS-IGF2 isoforms show differences between mouse and human. Human Molecular Genetics. 15 (8), pp. 1259-1269. https://doi.org/10.1093/hmg/ddl041
Noninflammatory phagocytosis of monosodium urate monohydrate crystals by mouse macrophages: implications for the control of joint inflammation in gout
Yagnik, D., Hillyer, P., Marshall, D., Smythe, C., Krausz, T., Haskard, D. and Landis, R. 2000. Noninflammatory phagocytosis of monosodium urate monohydrate crystals by mouse macrophages: implications for the control of joint inflammation in gout. Arthritis and Rheumatism. 43 (8), pp. 1779-1789.
Monocyte Fc gamma receptor expression in patients undergoing coronary artery bypass grafting
Stefanou, D., Asimakopoulos, G., Yagnik, D., Haskard, D., Anderson, J., Philippidis, P., Landis, R. and Taylor, K. 2004. Monocyte Fc gamma receptor expression in patients undergoing coronary artery bypass grafting. Annals of Thoracic Surgery. 77 (3), pp. 951-955.
Safe disposal of inflammatory monosodium urate monohydrate crystals by differentiated macrophages
Landis, R., Yagnik, D., Florey, O., Philippidis, P., Emons, V., Mason, J. and Haskard, D. 2002. Safe disposal of inflammatory monosodium urate monohydrate crystals by differentiated macrophages. Arthritis and Rheumatism. 46 (11), pp. 3026-3033. https://doi.org/10.1002/art.10614
Macrophage release of transforming growth factor beta1 during resolution of monododium urate monohydrate crystal-induced inflammation
Yagnik, D., Evans, B., Florey, O. and Mason, J. 2004. Macrophage release of transforming growth factor beta1 during resolution of monododium urate monohydrate crystal-induced inflammation. Arthritis and Rheumatism. 50 (7), pp. 2273-2280. https://doi.org/10.1002/art.20317
STOX1 is not imprinted and is not likely to be involved in preeclampsia.
Hills, F., Iglesias-Platas, I., Jebbink, J. and Monk, D. 2007. STOX1 is not imprinted and is not likely to be involved in preeclampsia. Nature Genetics. 39 (3), pp. 279-280. https://doi.org/10.1038/ng0307-279
Limited evolutionary conservation of imprinting in the human placenta
Hills, F., Apostolidou, S., Arnaud, P. and Monk, D. 2006. Limited evolutionary conservation of imprinting in the human placenta. Proceedings of the National Academy of Sciences. 103 (17), pp. 6623-6628. https://doi.org/10.1073/pnas.0511031103
Regulation of human villous trophoblast by insulin-like growth factors and insulin-like growth factor-binding protein-1
Hills, F., Chard, T., Elder, M. and Sullivan, M. 2004. Regulation of human villous trophoblast by insulin-like growth factors and insulin-like growth factor-binding protein-1. Journal of Endocrinology. 183 (3), pp. 487-496. https://doi.org/10.1677/joe.1.05867
Polyclonal anti-tumor necrosis factor-alpha Fab used as an ancillary treatment for severe malaria.
Looareesuwan, S., Sjorstrom, L., Krudsood, S., Wilairatana, P., Porter, R., Hills, F. and Warrell, D. 1999. Polyclonal anti-tumor necrosis factor-alpha Fab used as an ancillary treatment for severe malaria. American Journal of Tropical Medicine and Hygiene. 61 (1), pp. 26-33. https://doi.org/10.4269/ajtmh.1999.61.26