Curcumin: novel treatment in neonatal hypoxic-ischaemic brain injury

Rocha-Ferreira, E., Sisa, C., Bright, S., Fautz, T., Harris, M., Contreras Riquelme, I., Agwu, C., Kurulday, T., Mistry, B., Hill, D., Lange, S. and Hristova, M. 2019. Curcumin: novel treatment in neonatal hypoxic-ischaemic brain injury. Frontiers in Physiology. 10 1351. https://doi.org/10.3389/fphys.2019.01351

TitleCurcumin: novel treatment in neonatal hypoxic-ischaemic brain injury
TypeJournal article
AuthorsRocha-Ferreira, E.
Sisa, C.
Bright, S.
Fautz, T.
Harris, M.
Contreras Riquelme, I.
Agwu, C.
Kurulday, T.
Mistry, B.
Hill, D.
Lange, S.
Hristova, M.
Abstract

Hypoxic-ischaemic encephalopathy (HIE) is a major cause of mortality and morbidity in neonates, with an estimated global incidence of 3/1000 live births. HIE brain damage is associated with an inflammatory response and oxidative stress, resulting in the activation of cell death pathways. At present, therapeutic hypothermia is the only clinically approved treatment available for HIE. This approach, however, is only partially effective. There is therefore an unmet clinical need for the development of novel therapeutic interventions for the treatment of HIE.
Curcumin is an antioxidant reactive oxygen species scavenger, with reported anti-tumour and anti-inflammatory activity. Curcumin has been shown to attenuate mitochondrial dysfunction, stabilise the cell membrane, stimulate proliferation, and reduce injury severity in adult models of spinal cord injury, cancer, and cardiovascular disease. The role of curcumin in neonatal HIE has not been widely studied due to its low bioavailability and limited aqueous solubility. The aim of this study was to investigate the effect of curcumin treatment in neonatal HIE, including time of administration and dose-dependent effects.
Our results indicate that curcumin administration prior to HIE in neonatal mice elevated cell and tissue loss, as well as glial activation compared to HI alone. However, immediate post-treatment with curcumin was significantly neuroprotective, reducing grey and white matter tissue loss, TUNEL+ cell death, microglia activation, reactive astrogliosis and iNOS oxidative stress when compared to vehicle-treated littermates. This effect was dose-dependent, with 200µg/g body weight as the optimal dose-regimen, and was maintained when curcumin treatment was delayed by 60min or 120min post-HI. Cell proliferation measurements showed no changes between curcumin and HI alone, suggesting that the protective effects of curcumin on the neonatal brain following HI are most likely due to curcumin’s anti-inflammatory and antioxidant properties, as seen in the reduced glial and iNOS activity.
In conclusion, this study suggests curcumin as a potent neuroprotective agent with potential for the treatment of HIE. The delayed application of curcumin further increases its clinical relevance.

KeywordsCurcumin, hypoxia, ischaemia, Neuroprotection, neonate, Oxidative Stress
Article number1351
JournalFrontiers in Physiology
Journal citation10
ISSN1664-042X
Year2019
PublisherFrontiers
Publisher's version
Digital Object Identifier (DOI)https://doi.org/10.3389/fphys.2019.01351
Web address (URL)https://www.frontiersin.org/articles/10.3389/fphys.2019.01351/abstract
Publication dates
Published online13 Nov 2019
LicenseCC BY 4.0

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Magnadóttir, B., Bragason, B.T., Bricknell, I.R., Bowden, T., Nicholas, A.P., Hristova, M., Gudmundsdottir, S., Dodds, A.W. and Lange, S. 2019. Peptidylarginine deiminase and deiminated proteins are detected throughout early halibut ontogeny - Complement components C3 and C4 are post-translationally deiminated in halibut (Hippoglossus hippoglossus L.). Developmental and Comparative Immunology. 92, pp. 1-19. https://doi.org/10.1016/j.dci.2018.10.016

The physiological variability of channel density in hippocampal CA1 pyramidal cells and interneurons explored using a unified data-driven modeling workflow
Migliore, R., Lupascu, C.A., Bologna, L.L., Romani, R., Courcol, J-D., Antonel, S., Van Geit, W.A.H., Thompson, A.M., Mercer, A., Lange, S., Falck, J., Rossert, C.A., Shi, Y., Hagens, O., Pezzoli, M., Freund, T.F., Muller, E.B., Kali, S., Schurmann, F., Markram, H. and Migliore, M. 2018. The physiological variability of channel density in hippocampal CA1 pyramidal cells and interneurons explored using a unified data-driven modeling workflow. PLOS Computational Biology. 14 (9) e1006423. https://doi.org/10.1371/journal.pcbi.1006423

Cannabidiol (CBD) is a Novel Inhibitor for Exosome and Microvesicle (EMV) Release in Cancer
Kosgodage, U., Mould, R., Henley, A., Nunn, A.V.W., Guy, G.W., Thomas, E.L., Inal, J.M., Bell, J.D. and Lange, S. 2018. Cannabidiol (CBD) is a Novel Inhibitor for Exosome and Microvesicle (EMV) Release in Cancer. Frontiers in Pharmacology. 9 889. https://doi.org/10.3389/fphar.2018.00889

Post-translational Protein Deimination in Cod (Gadus morhua L.) Ontogeny: Novel Roles in Tissue Remodelling and Mucosal Immune Defences?
Magnadóttir, B., Hayes, P.M., Hristova, M., Bragason, B., Nicholas, A.P., Dodds, A.W., Gudmundsdottir, S. and Lange, S. 2018. Post-translational Protein Deimination in Cod (Gadus morhua L.) Ontogeny: Novel Roles in Tissue Remodelling and Mucosal Immune Defences? Developmental and Comparative Immunology. 87, pp. 157-170. https://doi.org/10.1016/j.dci.2018.06.006

Pentraxins CRP-I and CRP-II are post-translationally deiminated and differ in tissue specificity in cod (Gadus morhua L.) ontogeny
Magnadóttir, B., Hayes, P.M., Gisladottir, B., Bragason, B., Hristova, M., Nicholas, A.P., Gudmundsdottir, S. and Lange, S. 2018. Pentraxins CRP-I and CRP-II are post-translationally deiminated and differ in tissue specificity in cod (Gadus morhua L.) ontogeny. Developmental and Comparative Immunology. 87, pp. 1-11. https://doi.org/10.1016/j.dci.2018.05.014

Data-driven computational modeling of CA1 hippocampal principal cells and interneurons
Lange, S., migliore, S. and Lupascu, A.C. 2017. Data-driven computational modeling of CA1 hippocampal principal cells and interneurons. 26th Annual Computational Neuroscience Meeting (CNS*2017). Antwerp, Belgium 15 - 20 Jul 2017 BioMed Central. https://doi.org/10.1186/s12868-017-0372-1

Treatment of Prostate Cancer Using Deimination Antagonists and Microvesicle Technology
Lange, S., Kholia, S., Kosgodage, U. and Inal, J.M. 2017. Treatment of Prostate Cancer Using Deimination Antagonists and Microvesicle Technology. in: Nicholas, A.P., Bhattacharya, S. and Thompson, P.R. (ed.) Protein Deimination in Human Health and Disease Cham, Switzerland Springer. pp. 413-425

Protein Deimination in Protein Misfolding Disorders - Modelled in Human induced Pluripotent Stem Cells (iPSCs)
Lange, S., Wray, S., Devine, M., Matarin, M. and Hardy, J. 2017. Protein Deimination in Protein Misfolding Disorders - Modelled in Human induced Pluripotent Stem Cells (iPSCs). in: Nicholas, A.P., Battacharya, S.K. and Thompson, P.R. (ed.) Protein Deimination in Human Health and Disease Cham, Switzerland Springer. pp. 227-239

Peptidylarginine Deiminases-Roles in Cancer and Neurodegeneration and Possible Avenues for Therapeutic Intervention via Modulation of Exosome and Microvesicle (EMV) Release?
Lange, S., Gallagher, M, Kholia, S., Kosgodage, U., Hristova, M., Hardy, J. and Inal, J.M. 2017. Peptidylarginine Deiminases-Roles in Cancer and Neurodegeneration and Possible Avenues for Therapeutic Intervention via Modulation of Exosome and Microvesicle (EMV) Release? International Journal of Molecular Sciences. 18 (6) 1196. https://doi.org/10.3390/ijms18061196

Chloramidine/Bisindolylmaleimide-I-Mediated Inhibition of Exosome and Microvesicle Release and Enhanced Efficacy of Cancer Chemotherapy
Kosgodage, U., Trindade R.P., Thompson, P.R., Inal, J.M. and Lange, S. 2017. Chloramidine/Bisindolylmaleimide-I-Mediated Inhibition of Exosome and Microvesicle Release and Enhanced Efficacy of Cancer Chemotherapy. International Journal of Molecular Sciences. 18 (5) 1007. https://doi.org/10.3390/ijms18051007

The emerging role of exosome and microvesicle- (EMV-) based cancer therapeutics and immunotherapy
Moore, C., Kosgodage, U., Lange, S. and Inal, J.M. 2017. The emerging role of exosome and microvesicle- (EMV-) based cancer therapeutics and immunotherapy. International Journal of Cancer. 141 (3), pp. 428-436. https://doi.org/10.1002/ijc.30672

Data-driven model of the hippocampus using the HBP Brain Simulation Platform
Romani, A., Antille, N., Atenekeng, G., Courcol, J.D., Devresse, A., Dynes, J.A., Gevaert, M., Gonzalo, J.K., Gulyas, A., Kali, S., Kanari, L., Lange, S., Mercer, A., Migliore, M., Muller, E.B., Palacios, J.P., Ramaswamy, S., Reimann, M., Riquelme, R.L., Rössert, C.A., Ying, S., Shillcock, J., Telefont, M., Van Geit, W.A.H., Vanherpe, L., Markram, H. and Thomson, A. 2016. Data-driven model of the hippocampus using the HBP Brain Simulation Platform. 10th FENS Forum of Neuroscience. Copenhagen, Denmark 02 - 06 Jul 2016

PF7.09 Non-phagocytic epithelial cells take up microvesicles by micropinocytosis
Lange, S., Kosgodage, U. and Inal, J.M. 2016. PF7.09 Non-phagocytic epithelial cells take up microvesicles by micropinocytosis. The Fifth International Meeting of ISEV, ISEV 2016. Rotterdam, Netherlands 04 - 07 May 2016 Co-Action Publishing.

PW1.04. Inhibitors of microvesicle release with the potential to enhance effectivity of cancer chemotherapy
Lange, S., Kosgodage, U. and Inal, J.M. 2016. PW1.04. Inhibitors of microvesicle release with the potential to enhance effectivity of cancer chemotherapy. The Fifth International Meeting of ISEV, ISEV 2016. Rotterdam, Netherlands 04 - 07 May 2016 Co-Action Publishing. https://doi.org/10.3402/jev.v5.31552

Peptidylarginine deiminases as drug targets in neonatal hypoxic-ischemic encephalopathy
Lange, S. 2016. Peptidylarginine deiminases as drug targets in neonatal hypoxic-ischemic encephalopathy. Frontiers in Neurology. 7 22. https://doi.org/10.3389/fneur.2016.00022

Prostate cancer cells stimulated by calcium-mediated activation of protein kinase C undergo a refractory period before re-releasing calcium-bearing microvesicles
Lange, S., Stratton, D., Moore, C., Inal, J., Zheng, L. and Li, Z. 2015. Prostate cancer cells stimulated by calcium-mediated activation of protein kinase C undergo a refractory period before re-releasing calcium-bearing microvesicles. Biochemical and Biophysical Research Communications. 460 (3), pp. 511-517. https://doi.org/10.1016/j.bbrc.2015.03.061

Microvesicles released constitutively from prostate cancer cells differ biochemically and functionally to stimulated microvesicles released through sublytic C5b-9
Lange, S., Stratton, D., Moore, C., Antwi-Baffour, S. and Inal, J. 2015. Microvesicles released constitutively from prostate cancer cells differ biochemically and functionally to stimulated microvesicles released through sublytic C5b-9. Biochemical and Biophysical Research Communications. 460 (3), p. 589–595. https://doi.org/10.1016/j.bbrc.2015.03.074

Data-driven Hippocampus CA1 Modeling in the Human Brain Project
Romani, A., Antille, N., Mercer, A., Dynes, J.A., Falk, J., Gevaert, M., Gonzalo, J.K., Kali, S., Kanari, L., Migliore, M., Lange, S., Muller, E.B., Ramaswamy, S., Reimann, M., Riquelme, R.J.L., Rössert, C.A., Shi, Y., Telefont, M., Van Geit, W.A.H., Markram, H., Thomson, A. and W.A.H. Van Geit 2015. Data-driven Hippocampus CA1 Modeling in the Human Brain Project. Neuroscience 2015. Chicago 17 Oct 2015 Society for Neuroscience.

A novel role for peptidylarginine deiminases in microvesicle release reveals therapeutic potential of PAD inhibition in sensitizing prostate cancer cells to chemotherapy
Kholia, S., Jorfi, S., Thompson, P.R., Causey, C.P., Nicholas, A.P., Inal, J. and Lange, S. 2015. A novel role for peptidylarginine deiminases in microvesicle release reveals therapeutic potential of PAD inhibition in sensitizing prostate cancer cells to chemotherapy. Journal of Extracellular Vesicles. 4 (1) 26192. https://doi.org/10.3402/jev.v4.26192

Inhibition of microvesiculation sensitizes prostate cancer cells to chemotherapy and reduces docetaxel dose required to limit tumor growth in vivo
Jorfi, S., Ansa-Addo, E.A., Kholia, S., Stratton, D., Valley, S., Lange, S. and Inal, J. 2015. Inhibition of microvesiculation sensitizes prostate cancer cells to chemotherapy and reduces docetaxel dose required to limit tumor growth in vivo. Scientific Reports. 5 (13006) 13006. https://doi.org/10.1038/srep13006

Label-free real-time acoustic sensing of microvesicle release from prostate cancer (PC3) cells using a Quartz Crystal Microbalance
Lange, S., Stratton, D., Kholia, S., Jorfi, S., Antwi-Baffour, S. and Inal, J. 2014. Label-free real-time acoustic sensing of microvesicle release from prostate cancer (PC3) cells using a Quartz Crystal Microbalance. Biochemical and Biophysical Research Communications. 453 (3), p. 619–624. https://doi.org/10.1016/j.bbrc.2014.09.132

Peptidylarginine deiminases (PADs): novel drug targets for prevention of neuronal damage following hypoxic ischemic insult (HI) in neonates
Lange, S., Rocha-Ferreira, E., Thei, L., Mawjee, P., Thompson, P.R., Nicholas, A.P., Hristova, M., Peebles, D. and Raivich, G. 2014. Peptidylarginine deiminases (PADs): novel drug targets for prevention of neuronal damage following hypoxic ischemic insult (HI) in neonates. Journal of Neurochemistry. 130 (4), pp. 555-562. https://doi.org/10.1111/jnc.12744

The Role of Infection and the TNF Family of Cytokines in Neonatal Hypoxic-Ischemic Brain Injury
Rocha-Ferreira, E., Francesch-Domenech, E., Thei, L., Rahim, A., Lange, S., Peebles, D., Hristova, M. and Raivich, G. 2014. The Role of Infection and the TNF Family of Cytokines in Neonatal Hypoxic-Ischemic Brain Injury. Reproductive Sciences. 21 (3 suppl), pp. 108A-109A. https://doi.org/10.1177/1933719114528275

Pulsed extremely low-frequency magnetic fields stimulate microvesicle release from human monocytic leukaemia cells
Lange, S., Stratton, D. and Inal, J. 2013. Pulsed extremely low-frequency magnetic fields stimulate microvesicle release from human monocytic leukaemia cells. Biochemical and Biophysical Research Communications. 430 (2), pp. 470-475. https://doi.org/10.1016/j.bbrc.2012.12.012

The Role of Deimination as a Response to Trauma and Hypoxic Injury in the Developing CNS
Ferretti, P., Lange, S., U, KP and Raivich, G. 2013. The Role of Deimination as a Response to Trauma and Hypoxic Injury in the Developing CNS. in: Nicholas, A. and Bhattacharya, S. (ed.) Protein Deimination in Human Health and Disease Springer. pp. 281-294

Blood/plasma secretome and microvesicles
Inal, J.M., Kosgodage, U., Azam, S., Stratton, D., Antwi-Baffour, S. and Lange, S. 2013. Blood/plasma secretome and microvesicles. Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids. 1834 (11), pp. 2317-2325. https://doi.org/10.1016/j.bbapap.2013.04.005

Interplay of host–pathogen microvesicles and their role in infectious disease
Inal, J.M., Ansa-Addo, E.A. and Lange, S. 2013. Interplay of host–pathogen microvesicles and their role in infectious disease. Biochemical Society Transactions. 41 (1), pp. 258-262. https://doi.org/10.1042/BST20120257

Inhibition of Protein Deimination Ameliorates Neuronal Damage Caused by Hypoxic Ischemic Insult in the Neonatal Brain
Lange, S., Rocha-Ferreira, E., Hristova, M., Thei, L., Mawjee, P., Thompson, P.R., Nicholas, T. and Raivich, G. 2013. Inhibition of Protein Deimination Ameliorates Neuronal Damage Caused by Hypoxic Ischemic Insult in the Neonatal Brain. British Neuroscience Association Abstracts. 22, pp. P1-B-071.

Microvesicles in Health and Disease
Inal, J.M., Ansa-Addo, E.A., Stratton, D., Kholia, S., Antwi-Baffour, S., Jorfi, S. and Lange, S. 2012. Microvesicles in Health and Disease. Archivum Immunologiae et Therapiae Experimentalis. 60 (2), pp. 107-121. https://doi.org/10.1007/s00005-012-0165-2

TNF gene deletion prevents lipopolysaccharide-mediated sensitisation of the neonatal mouse brain to hypoxic-ischaemic insult
Sahota, A., Kendall, G., Lange, S. and Raivich, G. 2012. TNF gene deletion prevents lipopolysaccharide-mediated sensitisation of the neonatal mouse brain to hypoxic-ischaemic insult. BMC Proceedings. 6 (Suppl 4), p. O9. https://doi.org/10.1186/1753-6561-6-S4-O9

Characterisation of microvesicles released from cells constitutively and upon stimulation
Stratton, D., Antwi-Baffour, S., Williams, G., Grant, R., Lange, S. and Inal, J.M. 2012. Characterisation of microvesicles released from cells constitutively and upon stimulation. Journal of Extracellular Vesicles. 1.

Isolation of microvesicles and exosomes by filtration and estimation of normal reference range in blood plasma
Grant, R., Ansa-Addo, E., Stratton, S., Antwi-Baffour, S., Jorfi, S., Kholia, S., Krige, L., Lange, S. and Inal, J.M. 2012. Isolation of microvesicles and exosomes by filtration and estimation of normal reference range in blood plasma. Journal of Extracellular Vesicles. 1.

The intracellular parasite, Trypanosoma cruzi, utilizes microvesicle release to invade host cells
Inal, J.M., Ansa-Addo, E., Cestari, I., Pathak, P.I., McCrossan, M.V., Lange, S. and Ramirez, M. 2012. The intracellular parasite, Trypanosoma cruzi, utilizes microvesicle release to invade host cells. Journal of Extracellular Vesicles. 1.

Kisspeptin prevention of Amyloid-β Peptide neurotoxicity in vitro
Milton, N.G.N., Chilumuri, A., Rocha-Ferreira, E., Nercessian, A.N. and Ashioti, M. 2012. Kisspeptin prevention of Amyloid-β Peptide neurotoxicity in vitro. ACS chemical neuroscience. 3 (9), pp. 706-719. https://doi.org/10.1021/cn300045d

A filtration-based protocol to isolate human plasma membrane-derived vesicles and exosomes from blood plasma
Lange, S., Grant, R., Ansa-Addo, E.A., Stratton, D., Antwi-Baffour, S., Jorfi, S., Kholia, S., Krige, L. and Inal, J. 2011. A filtration-based protocol to isolate human plasma membrane-derived vesicles and exosomes from blood plasma. Journal of Immunological Methods. 371 (1-2), pp. 143-151. https://doi.org/10.1016/j.jim.2011.06.024

Protein deiminases: new players in the developmentally regulated loss of neural regenerative ability
Lange, S., Gogel, S., Yeung K-Y, Nicholas, A.P., Causey, C.P., Thompson, P.R., Greene, N.D.E. and Ferretti, P. 2011. Protein deiminases: new players in the developmentally regulated loss of neural regenerative ability. Developmental Biology. 355 (2), pp. 205-214. https://doi.org/10.1016/j.ydbio.2011.04.015

Post-translational regulation of CRMP in developing and regenerating chick spinal cord
Lange, S., Gogel, S., Leung Kit-Y, Greene, N.D.E. and Ferretti, P. 2010. Post-translational regulation of CRMP in developing and regenerating chick spinal cord. Developmental Neurobiology. 70 (6), pp. 456-471. https://doi.org/10.1002/dneu.20789

Human plasma membrane-derived vesicles inhibit the phagocytosis of apoptotic cells: possible role in SLE
Lange, S., Antwi-Baffour, S., Kholia, S., Ansa-Addo, E.A., Stratton, D., Aryee Y, K. and Inal, J. 2010. Human plasma membrane-derived vesicles inhibit the phagocytosis of apoptotic cells: possible role in SLE. Biochemical and Biophysical Research Communications. 398 (2), pp. 278-283. https://doi.org/10.1016/j.bbrc.2010.06.079

Human plasma membrane-derived vesicles halt proliferation and induce differentiation of THP-1 acute monocytic leukemia cells
Lange, S., Ansa-Addo, E.A., McCrossan, M.V. and Inal, J. 2010. Human plasma membrane-derived vesicles halt proliferation and induce differentiation of THP-1 acute monocytic leukemia cells. Journal of Immunology. 185 (9), pp. 5236-5246. https://doi.org/10.4049/jimmunol.1001656

Red cell PMVs, plasma membrane-derived vesicles calling out for standards
Hind, E., Heugh, S., Ansa-Addo, E.A., Antwi-Baffour, S., Lange, S. and Inal, J.M. 2010. Red cell PMVs, plasma membrane-derived vesicles calling out for standards. Biochemical and Biophysical Research Communications. 399 (4), pp. 465-469. https://doi.org/10.1016/j.bbrc.2010.07.095

Spinal cord regeneration: A role for peptidylarginine deiminase (PAD) in secondary injury response
Lange, S. 2010. Spinal cord regeneration: A role for peptidylarginine deiminase (PAD) in secondary injury response. SfN Minisymposium on Deimination in Opthalmic and Neurodegenerative diseases. San Diego Convention Center, California 16 Nov 2010

Spinal cord regeneration: peptidylarginine deiminase (PAD) and epigentic regulation of injury response
Lange, S., Ferretti, P., Goegel, S., Leung, K.T., Nicholas, A.P., Thompson, P.R. and Greene, N.D.E. 2010. Spinal cord regeneration: peptidylarginine deiminase (PAD) and epigentic regulation of injury response. FENS Forum 2010. Amsterdam 04 Jul 2010 Federation of European Neuroscience Societies.

Changes in progenitor populations and ongoing neurogenesis in the regenerating chick spinal cord
Lange, S., Whalley, K., Gogel, S. and Ferretti, P. 2009. Changes in progenitor populations and ongoing neurogenesis in the regenerating chick spinal cord. Developmental Biology. 332 (2), p. 234–245. https://doi.org/10.1016/j.ydbio.2009.05.569

Proteome changes in developing and injured chick spinal cord
Goegel, S., Lange, S., Greene, N.D.E. and Ferretti, P. 2007. Proteome changes in developing and injured chick spinal cord. Neuron Glia Biology. pp. S122-S122.

Differential gene expression following chick spinal cord injury at permissive and non permissive stages for regeneration
Lange, S., Goegel, S., Greene, N.D.E. and Ferretti, P. 2007. Differential gene expression following chick spinal cord injury at permissive and non permissive stages for regeneration. Neuron Glia Biology. pp. S121-S121.

The complement regulatory receptor CRIT is expressed in the developing kidney
Lange, S., Hui Kwok-M, Schifferli, J. and Inal, J.M. 2007. The complement regulatory receptor CRIT is expressed in the developing kidney. Molecular Immunology. 44 (16), p. 3991. https://doi.org/10.1016/j.molimm.2007.06.213

Complement C2 and CRIT are involved in the terminal differentiation of monocytes
Inal, J.M., Eva, W., Lange, S., Shamshiev, A. and Schifferli, J. 2007. Complement C2 and CRIT are involved in the terminal differentiation of monocytes. Journal of Immunology. 178, p. 83.17.

Immunostimulation of larvae and juveniles of cod, Gadus morhua L.
Lange, S., Magnadóttir, B., Gudmundsdóttir, B.K., Bambir, S.H., Steinarsson, A., Oddgeirsson, M., Bowden, T., Bricknell, I., Dalmo, R.A. and Gudmundsdottir, S. 2006. Immunostimulation of larvae and juveniles of cod, Gadus morhua L. Journal of Fish Diseases. 29 (3), p. 147–155. https://doi.org/10.1111/j.1365-2761.2006.00701.x.

CRIT is expressed on podocytes in normal human kidney and upregulated in membranous nephropathy
Lange, S., Moll, S., Mihatsch M, J., Schifferli, J. and Inal, J. 2006. CRIT is expressed on podocytes in normal human kidney and upregulated in membranous nephropathy. Kidney International. 69 (11), p. 1961–1968. https://doi.org/10.1038/sj.ki.5000379

Complement component C3 transcription in Atlantic halibut (Hippoglossus hippoglossus L.) larvae
Lange, S., Bambir, S.H., Dodds, A.W., Bowden, T., Bricknell, I., Espelid, S. and Magnadóttir, B. 2006. Complement component C3 transcription in Atlantic halibut (Hippoglossus hippoglossus L.) larvae. Fish & Shellfish Immunology. 20 (3), p. 285–294. https://doi.org/10.1016/j.fsi.2005.05.004

Complement C2 receptor inhibitor trispanning: a novel human complement inhibitory receptor
Lange, S., Inal, J., Hui Kwok-M, Miot, S., Ramirez, M., Schneider, B. and Krueger, G. 2005. Complement C2 receptor inhibitor trispanning: a novel human complement inhibitory receptor. The Journal of Immunology. 174 (1), pp. 356-366.

The ontogenic transcription of complement component C3 and Apolipoprotein A-I tRNA in Atlantic cod (Gadus morhua L.): a role in development and homeostasis?
Lange, S., Dodds, A.W., Bambir, S.H., Gudmundsdottir, S. and Magnadóttir, B. 2005. The ontogenic transcription of complement component C3 and Apolipoprotein A-I tRNA in Atlantic cod (Gadus morhua L.): a role in development and homeostasis? Developmental & Comparative Immunology. 29 (12), p. 1065–1077. https://doi.org/10.1016/j.dci.2005.03.009

The Complement Systems of Two Teleost Species with Emphasis on Ontogeny
Lange, S. 2005. The Complement Systems of Two Teleost Species with Emphasis on Ontogeny. PhD thesis University of Iceland Faculty of Medicine

Ontogeny of humoral immune parameters in fish
Magnadóttir, B., Lange, S., Gudmundsdottir, S., Bogwald, J. and Dalmo, R.A. 2005. Ontogeny of humoral immune parameters in fish. Fish and Shellfish Immunology. 19 (5), pp. 429-439. https://doi.org/10.1016/j.fsi.2005.03.010

The ontogeny of complement component C3 in Atlantic cod (Gadus morhua L.)—an immunohistochemical study
Lange, S., Bambir, S., Dodds, A.W. and Magnadóttir, B. 2004. The ontogeny of complement component C3 in Atlantic cod (Gadus morhua L.)—an immunohistochemical study. Fish & Shellfish Immunology. 16 (3), pp. 359-367. https://doi.org/10.1016/j.fsi.2003.06.001

Is Apolipoprotein A-I a regulating protein for the complement system of cod (Gadus morhua L.)?
Magnadóttir, B. and Lange, S. 2004. Is Apolipoprotein A-I a regulating protein for the complement system of cod (Gadus morhua L.)? Fish and Shellfish Immunology. 16 (2), pp. 265-269. https://doi.org/10.1016/S1050-4648(03)00061-5

Isolation and characterization of complement component C3 from Atlantic cod (Gadus morhua L.) and Atlantic halibut (Hippoglossus hippoglossus L.)
Lange, S., Dodds, A.W. and Magnadóttir, B. 2004. Isolation and characterization of complement component C3 from Atlantic cod (Gadus morhua L.) and Atlantic halibut (Hippoglossus hippoglossus L.). Fish and Shellfish Immunology. 16 (2), pp. 227-239. https://doi.org/10.1016/S1050-4648(03)00081-0

Spontaneous haemolytic activity of Atlantic halibut (Hippoglossus hippoglossus L.) and sea bass (Dicentrarchus labrax) serum
Lange, S. and Magnadóttir, B. 2003. Spontaneous haemolytic activity of Atlantic halibut (Hippoglossus hippoglossus L.) and sea bass (Dicentrarchus labrax) serum. Comparative Biochemistry and Physiology - Part B: Biochemistry & Molecular Biology. 136 (1), pp. 99-106. https://doi.org/10.1016/S1096-4959(03)00173-8

Protection against atypical furunculosis in Atlantic halibut, Hippoglossus hippoglossus (L.); comparison of a commercial furunculosis vaccine and an autogenous vaccine
Gudmundsdottir, S., Lange, S., Magnadóttir, B. and Gudmundsdóttir, B.K. 2003. Protection against atypical furunculosis in Atlantic halibut, Hippoglossus hippoglossus (L.); comparison of a commercial furunculosis vaccine and an autogenous vaccine. Journal of Fish Diseases. 26 (6), pp. 331-338. https://doi.org/10.1046/j.1365-2761.2003.00462.x

Humoral immune parameters of cultured Atlantic halibut (Hippoglossus hippoglossus L.)
Lange, S., Guđmundsdottir, B.K. and Magnadóttir, B. 2001. Humoral immune parameters of cultured Atlantic halibut (Hippoglossus hippoglossus L.). Fish and Shellfish Immunology. 11 (6), pp. 523-535. https://doi.org/10.1006/fsim.2000.0333

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