Analysis of procainamide-derivatised heparan sulphate disaccharides in biological samples using hydrophilic interaction liquid chromatography mass spectrometry

Article

Antia, I., Mathew, K., Yagnik, D., Hills, F. and Shah, A. 2018. Analysis of procainamide-derivatised heparan sulphate disaccharides in biological samples using hydrophilic interaction liquid chromatography mass spectrometry. Analytical and Bioanalytical Chemistry. 410 (1), pp. 131-143. https://doi.org/10.1007/s00216-017-0703-1
TypeArticle
TitleAnalysis of procainamide-derivatised heparan sulphate disaccharides in biological samples using hydrophilic interaction liquid chromatography mass spectrometry
AuthorsAntia, I., Mathew, K., Yagnik, D., Hills, F. and Shah, A.
Abstract

Glycosaminoglycans (GAGs) are a family of linear heteropolysaccharides made up of repeating disaccharide units that are found on the surface and extracellular matrix of animal cells. They are known to play a critical role in a wide range of cellular processes including proliferation, differentiation and invasion. To elucidate the mechanism of action of these molecules, it is essential to quantify their disaccharide composition. Analytical methods that have been reported involve either chemical or enzymatic depolymerisation of GAGs followed by separation of non-derivatised (native) or derivatised disaccharide subunits and detection by either UV/fluorescence or MS. However, the measurement of these disaccharides is challenging due to their hydrophilic and labile nature. Here we report a pre-column LC-MS method for the quantification of GAG disaccharide subunits. Heparan sulphate (HS) was extracted from cell lines using a combination of molecular weight cutoff and anion exchange spin filters and digested using a mixture of heparinases I, II and III. The resulting subunits were derivatised with procainamide, separated using hydrophilic interaction liquid chromatography and detected using electrospray ionisation operated in positive ion mode. Eight HS disaccharides were separated and detected together with an internal standard. The limit of detection was found to be in the range 0.6–4.9 ng/mL. Analysis of HS extracted from all cell lines tested in this study revealed a significant variation in their composition with the most abundant disaccharide being the non-sulphated ∆UA–GlcNAc. Some structural functional relationships are discussed demonstrating the viability of the pre-column method for studying GAG biology

Research GroupBiomarkers for Cancer group
PublisherSpringer
JournalAnalytical and Bioanalytical Chemistry
ISSN1618-2642
Electronic1618-2650
Publication dates
Online02 Nov 2017
Print31 Jan 2018
Publication process dates
Deposited01 Nov 2017
Accepted11 Oct 2017
Output statusPublished
Accepted author manuscript
Copyright Statement

This is a post-peer-review, pre-copyedit version of an article published in Analytical and Bioanalytical Chemistry. The final authenticated version is available online at: http://dx.doi.org/10.1007/s00216-017-0703-1

Digital Object Identifier (DOI)https://doi.org/10.1007/s00216-017-0703-1
LanguageEnglish
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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
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
Detection and quantification of human chorionic gonadotropin levels in human placental choriocarcinoma cell lines
Gondek, M., Hills, F. and Burczynska, B. 2017. Detection and quantification of human chorionic gonadotropin levels in human placental choriocarcinoma cell lines. Summer Conference 2017. Middlesex University Jun 2017
The effect of plasma volume on changes in biomarkers of muscle damage, inflammation, oxidative stress and leukocyte differentialfollowing a 42.2 km trail run, and the efficacy of recovery interventions
Cockburn, E., Hills, F., Wilson, L., Paice, K., Wood, A. and Dimitriou, L. 2017. The effect of plasma volume on changes in biomarkers of muscle damage, inflammation, oxidative stress and leukocyte differentialfollowing a 42.2 km trail run, and the efficacy of recovery interventions. BASES-FEPSAC Conference 2017. Nottingham, UK 28 - 29 Nov 2017 Taylor & Francis (Routledge). pp. s26
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 Xue Bin, X., Wood, A. and Cockburn, E. 2017. Influence of cold water immersion and cherry juice on recovery following a 42.2km trail run. BASES-FEPSAC Conference 2017. Nottingham, UK 28 - 29 Nov 2017 Taylor & Francis (Routledge). pp. s92
The influence of cold water immersion on markers of recovery following resistance exercise
Wilson, L., Dimitriou, L., Hills, F., Gondek, M. and Cockburn, E. 2017. The influence of cold water immersion on markers of recovery following resistance exercise. BASES-FEPSAC Conference 2017. Nottingham, UK 28 - 29 Nov 2017 Taylor & Francis (Routledge). pp. s66
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
Heparan sulfate disaccharide measurement from biological samples using pre-column derivatization, UPLC-MS and single ion monitoring
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
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
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
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
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
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
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.
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
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
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.