Toxic effects of X-linked adrenoleukodystrophy-associated, very long chain fatty acids on glial cells and neurons from rat hippocampus in culture
Abstract
Saturated very long chain fatty acids (VLCFAs; > or =C22:0) accumulate in X-linked adrenoleukodystrophy (X-ALD, OMIM 300100), a severe hereditary neurodegenerative disease, due to peroxisomal impairment. Previous studies analysed the development of X-ALD in humans and gene knockout animal models. However, the toxic effect of VLCFA leading to severe symptoms with progressive and multifocal demyelination, adrenal insufficiency and inflammation still remains unclear. To understand the toxic effects of VLCFA in the brain, here we exposed neural cells to VLCFA and analysed the cellular consequences. We found that oligodendrocytes and astrocytes challenged with docosanoic- (C22:0), tetracosanoic- (C24:0) and hexacosanoic acids (C24:0) die within 24 h. VLCFA-induced depolarization of mitochondria in situ and increased intracellular Ca2+ level in all three brain cell types provides indications about the mechanism of toxicity of VLCFA. Interestingly, VLCFAs affect to the largest degree the myelin-producing oligodendrocytes. In isolated mitochondria, VLCFAs exert a detrimental effect by affecting the inner mitochondrial membrane and promoting the permeability transition. In conclusion, we suggest that there is a potent toxic activity of VLCFA due to dramatic cell physiological effects with mitochondrial dysfunction and Ca2+ deregulation. This provides the first evidence for mitochondrial-based cell death mechanisms in neurodegenerative disease with peroxisomal defects and subsequent VLCFA accumulation.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
A direct cytotoxic effect on oligodendrocytes and astrocytes has been observed in rats following exposure to C26:0 lipids.
“A direct cytotoxic effect on oligodendrocyte and astrocytes has been observed in rats, following exposure to C26:0 lipids (14).”
From X-linked adrenoleukodystrophy and primary adrenal insufficiency (2023) · cites this paper as [14]
Cites
Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue
Mccarthy, K., & de Vellis, J. (1980) · Journal of Cell Biology · doi:10.1083/jcb.85.3.890 · Cited by 3,915 · see citing works
Korshunov, S. S., Skulachev, V. P., & Starkov, A. A. (1997) · FEBS Letters · doi:10.1016/s0014-5793(97)01159-9 · Cited by 1,727 · see citing works
Generation of reactive oxygen species by the mitochondrial electron transport chain
Liu, Y., Fiskum, G., & Schubert, D. (2002) · Journal of Neurochemistry · doi:10.1046/j.0022-3042.2002.00744.x · Cited by 1,260 · see citing works
Putative X-linked adrenoleukodystrophy gene shares unexpected homology with ABC transporters
Mosser, J., Douar, A.-M., Sarde, C.-O., Kioschis, P., Feil, R., Moser, H., Poustka, A.-M., Mandel, J.-L., & Aubourg, P. (1993) · Nature · doi:10.1038/361726a0 · Cited by 1,202 · see citing works
Peroxisomal and Mitochondrial Defects in the Cerebro-Hepato-Renal Syndrome
Goldfischer, S. L., Moore, C. L., Johnson, T., Spiro, A. J., Valsamis, M. P., Wisniewski, H. K., Ritch, R. H., Norton, W. T., Rapin, I., & Gartner, L. M. (1973) · Science · doi:10.1126/science.182.4107.62 · Cited by 791 · see citing works
Identification of lymphotoxin and tumor necrosis factor in multiple sclerosis lesions.
Selmaj, K. W., Raine, C. S., Cannella, B., & Brosnan, C. F. (1991) · Journal of Clinical Investigation · doi:10.1172/jci115102 · Cited by 726 · see citing works
Molecular mechanisms of glutamate-dependent neurodegeneration in ischemia and traumatic brain injury
Arundine, M., & Tymianski, M. (2004) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-003-3319-x · Cited by 635 · see citing works
Relationship between configuration, function, and permeability in calcium-treated mitochondria.
Hunter, D. R., Haworth, R. A., & Southard, J. H. (1976) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)33220-9 · Cited by 619 · see citing works
Hajnóczky, G., Csordás, G., Das, S., Garcı́a-Pérez, C., Saotome, M., Roy, S. S., & Yi, M. (2006) · Cell Calcium · doi:10.1016/j.ceca.2006.08.016 · Cited by 613 · see citing works
Votyakova, T. V., & Reynolds, I. J. (2001) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2001.00548.x · Cited by 601 · see citing works
Calcium, mitochondria and reperfusion injury: a pore way to die
Halestrap, A. P. (2006) · Biochemical Society Transactions · doi:10.1042/bst20060232 · Cited by 558 · see citing works
Adrenoleukodystrophy: phenotype, genetics, pathogenesis and therapy
Moser, H. (1997) · Brain · doi:10.1093/brain/120.8.1485 · Cited by 478 · see citing works
Qualitative alteration in substrate specificity of mitochondrial monoamine oxidase in brain
Moskvitina, T. A., Kamyshanskaya, N. S., Kaverina, L. P., & Gorkin, V. Z. (1976) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1976.tb04462.x · Cited by 440 · see citing works
Astrocyte apoptosis: implications for neuroprotection
Takuma, K., Baba, A., & Matsuda, T. (2004) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2004.02.001 · Cited by 435 · see citing works
Peroxisome biogenesis disorders
Gould, S. J., & Valle, D. L. (2000) · Trends in Genetics · doi:10.1016/s0168-9525(00)02056-4 · Cited by 354 · see citing works
Kemp, S., Pujol, A., Waterham, H. R., van Geel, B. M., Boehm, C. D., Raymond, G. V., Cutting, G. R., Wanders, R. J. A., & Moser, H. W. (2001) · Human Mutation · doi:10.1002/humu.1227 · Cited by 332 · see citing works
POWERS, J. M., LIU, Y., MOSER, A. B., & MOSER, H. W. (1992) · Journal of Neuropathology and Experimental Neurology · doi:10.1097/00005072-199211000-00007 · Cited by 265 · see citing works
[27] Primary glial cultures as a model for studying hormone action
Hamprecht, B., & Löffler, F. (1985) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/0076-6879(85)09097-8 · Cited by 250 · see citing works
Gene redundancy and pharmacological gene therapy: Implications for X-linked adrenoleukodystrophy
Kemp, S., Wei, H.-M., Lu, J.-F., Braiterman, L. T., McGuinness, M. C., Moser, A. B., Watkins, P. A., & Smith, K. D. (1998) · Nature Medicine · doi:10.1038/3242 · Cited by 249 · see citing works
Adrenoleukodystrophy: Incidence, new mutation rate, and results of extended family screening
Bezman, L., Moser, A. B., Raymond, G. V., Watkins, P. A., Smith, K. D., KASS, N. E., & Moser, H. W. (2001) · Annals of Neurology · doi:10.1002/ana.101.abs · Cited by 237 · see citing works
Singh, I., Moser, A. E., Moser, H. W., & Kishimoto, Y. (1984) · Pediatric Research · doi:10.1203/00006450-198403000-00016 · Cited by 234 · see citing works
Cocco, T., Di, M., Papa, P., & Lorusso, M. P. (1999) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(99)00034-9 · Cited by 228 · see citing works
Budd, S. L., Castilho, R. F., & Nicholls, D. G. (1997) · FEBS Letters · doi:10.1016/s0014-5793(97)01088-0 · Cited by 226 · see citing works
Peroxisomal disorders I: biochemistry and genetics of peroxisome biogenesis disorders
Wanders, R. J. A., & Waterham, H. R. (2004) · Clinical Genetics · doi:10.1111/j.1399-0004.2004.00329.x · Cited by 220 · see citing works
Pujol, A. (2002) · Human Molecular Genetics · doi:10.1093/hmg/11.5.499 · Cited by 214 · see citing works
Baumgart, E., Vanhorebeek, I., Grabenbauer, M., Borgers, M., Declercq, P. E., Fahimi, H. D., & Baes, M. (2001) · The American Journal of Pathology · doi:10.1016/s0002-9440(10)62534-5 · Cited by 210 · see citing works
Peroxisomal Disorders: Genotype, Phenotype, Major Neuropathologic Lesions, and Pathogenesis
Powers, J. M., & Moser, H. W. (1998) · Brain Pathology · doi:10.1111/j.1750-3639.1998.tb00139.x · Cited by 208 · see citing works
Peroxisome Biogenesis Disorders
Grønborg, S. W., Gould, S. J., & Valle, D. L. (2003) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev.genom.4.070802.110424 · Cited by 203 · see citing works
Aitken, R. J., Wingate, J. K., Iuliis, G. N. D., Koppers, A. J., & McLaughlin, E. A. (2006) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2006-1309 · Cited by 199 · see citing works
Ho, J. K., Moser, H., Kishimoto, Y., & Hamilton, J. A. (1995) · Journal of Clinical Investigation · doi:10.1172/jci118182 · Cited by 199 · see citing works
Oligodendrocyte lineage and the motor neuron connection
Richardson, W. D., Smith, H., Sun, T., Pringle, N., Hall, A., & Woodruff, R. (2000) · Glia · doi:10.1002/(sici)1098-1136(20000115)29:2 · Cited by 198 · see citing works
X-linked adrenoleukodystrophy: Genes, mutations, and phenotypes
Smith, K. D., Kemp, S., Braiterman, L. T., Lu, J.-F., Wei, H.-M., Geraghty, M., Stetten, G., Bergin, J. S., Pevsner, J., & Watkins, P. A. (1999) · Neurochemical Research · doi:10.1023/a:1022535930009 · Cited by 190 · see citing works
Schönfeld, P., & Wojtczak, L. (2007) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2007.04.005 · Cited by 163 · see citing works
Hall, A. M., Wiczer, B. M., Herrmann, T. R. W., Stremmel, W., & Bernlohr, D. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m412629200 · Cited by 151 · see citing works
Analysis of very long-chain fatty acids using electrospray ionization mass spectrometry
Valianpour, F., Selhorst, J. J. M., van Lint, L. E. M., van Gennip, A. H., Wanders, R. J. A., & Kemp, S. (2003) · Molecular Genetics and Metabolism · doi:10.1016/s1096-7192(03)00098-2 · Cited by 150 · see citing works
Role of ALDP (ABCD1) and Mitochondria in X-Linked Adrenoleukodystrophy
McGuinness, M. C., Lu, J.-F., Zhang, H.-P., Dong, G.-X., Heinzer, A. K., Watkins, P. A., Powers, J., & Smith, K. D. (2003) · Molecular and Cellular Biology · doi:10.1128/mcb.23.2.744-753.2003 · Cited by 147 · see citing works
Mitochondria and ischemic reperfusion damage in the adult and in the developing brain
Blomgren, K., Zhu, C., Hallin, U., & Hagberg, H. (2003) · Biochemical and Biophysical Research Communications · doi:10.1016/s0006-291x(03)00628-4 · Cited by 143 · see citing works
Ranking the toxicity of fatty acids on Jurkat and Raji cells by flow cytometric analysis
de Lima, T. M., Kanunfre, C. C., Pompéia, C., Verlengia, R., & Curi, R. (2002) · Toxicology in Vitro · doi:10.1016/s0887-2333(02)00095-4 · Cited by 142 · see citing works
Adreno-leukodystrophy: Oxidative Stress of Mice and Men
Powers, J. M., Pei, Z., Heinzer, A. K., Brose, R. D., Moser, A. B., Moser, H. W., Watkins, P. A., & Smith, K. D. (2005) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/01.jnen.0000190064.28559.a4 · Cited by 131 · see citing works
Verhoeven‐Duif, N. M., Roe, D. S., Kok, R. M., Wanders, R. J. A., Jakobs, C., & Roe, C. R. (1998) · Journal of Lipid Research · doi:10.1016/s0022-2275(20)34204-8 · Cited by 131 · see citing works
Neurotransmitter‐mediated calcium signalling in oligodendrocyte physiology and pathology
Butt, A. M. (2006) · Glia · doi:10.1002/glia.20424 · Cited by 128 · see citing works
Lipid metabolism in peroxisomes in relation to human disease
Wanders, R. J. A., & Tager, J. M. (1998) · Molecular Aspects of Medicine · doi:10.1016/s0098-2997(98)00003-x · Cited by 122 · see citing works
The neurobiology of X-linked adrenoleukodystrophy, a demyelinating peroxisomal disorder
Dubois-Dalcq, M., Feigenbaum, V., & Aubourg, P. (1999) · Trends in Neurosciences · doi:10.1016/s0166-2236(98)01319-8 · Cited by 121 · see citing works
Effects of Palmitate on Ca2+ Handling in Adult Control and ob/ob Cardiomyocytes
Fauconnier, J., Andersson, D. C., Zhang, S., Lanner, J. T., Wibom, R., Katz, A., Bruton, J. D., & Westerblad, H. (2007) · Diabetes · doi:10.2337/db06-0739 · Cited by 116 · see citing works
Expression of the adrenoleukodystrophy protein in the human and mouse central nervous system
Fouquet, F., Zhou, J. M., Ralston, E., Murray, K., Troalen, F., Magal, E., Robain, O., Dubois-Dalcq, M., & Aubourg, P. (1997) · Neurobiology of Disease · doi:10.1006/nbdi.1997.0127 · Cited by 115 · see citing works
Ubl, J. J., Vöhringer, C., & Reiser, G. (1998) · Neuroscience · doi:10.1016/s0306-4522(97)00686-6 · Cited by 103 · see citing works
Self-citationRotenone-like Action of the Branched-chain Phytanic Acid Induces Oxidative Stress in Mitochondria
Schönfeld, P., & Reiser, G. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m513198200 · Cited by 103 · see citing works
Self-citationTheda, C., Moser, A. B., Powers, J. M., & Moser, H. W. (1992) · Journal of the Neurological Sciences · doi:10.1016/0022-510x(92)90028-j · Cited by 99 · see citing works
van Geel, B. M., Assies, J., Weverling, G. J., & Barth, P. G. (1994) · Neurology · doi:10.1212/wnl.44.12.2343 · Cited by 90 · see citing works
Mitochondrial energy dissipation by fatty acids
Bernardi, P., Penzo, D., & Wojtczak, L. (2002) · Vitamins and hormones · doi:10.1016/s0083-6729(02)65061-7 · Cited by 85 · see citing works
Kahlert, S., Zündorf, G., & Reiser, G. (2004) · Journal of Neuroscience Research · doi:10.1002/jnr.20322 · Cited by 82 · see citing works
Self-citationSingh, I., & Kishimoto, Y. (1983) · Journal of Lipid Research · doi:10.1016/s0022-2275(20)37973-6 · Cited by 72 · see citing works
Reiser, G., Schönfeld, P., & Kahlert, S. (2006) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2005.11.002 · Cited by 63 · see citing works
Self-citationKahlert, S., Schönfeld, P., & Reiser, G. (2004) · Neurobiology of Disease · doi:10.1016/j.nbd.2004.08.010 · Cited by 63 · see citing works
Self-citationWang, Y., Luo, W., Stricker, R., & Reiser, G. (2006) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2006.03950.x · Cited by 61 · see citing works
Self-citationSchönfeld, P., Kahlert, S., & Reiser, G. (2004) · Biochemical Journal · doi:10.1042/bj20040583 · Cited by 55 · see citing works
Self-citationX‐linked adrenoleukodystrophy: Biochemical diagnosis and enzyme defect
Wanders, R. J. A., van Roermund, C. W. T., Lageweg, W., Jakobs, B. S., Schutgens, R. B. H., Nijenhuis, A. A., & Tager, J. M. (1992) · Journal of Inherited Metabolic Disease · doi:10.1007/bf01799620 · Cited by 51 · see citing works
Schönfeld, P., & Struy, H. (1999) · FEBS Letters · doi:10.1016/s0014-5793(99)01009-1 · Cited by 45 · see citing works
Bernstein, M., Behnisch, T., Balschun, D., Reymann, K. G., & Reiser, G. (1998) · Neuropharmacology · doi:10.1016/s0028-3908(98)00012-4 · Cited by 44 · see citing works
Self-citationOezen, I., Rossmanith, W., Forss‐Petter, S., Kemp, S., Voigtländer, T., Moser-Thier, K., Wanders, R. J. A., Bittner, R. E., & Berger, J. (2005) · Human Molecular Genetics · doi:10.1093/hmg/ddi125 · Cited by 37 · see citing works
Schönfeld, P., Kahlert, S., & Reiser, G. (2006) · Experimental Gerontology · doi:10.1016/j.exger.2006.02.013 · Cited by 24 · see citing works
Self-citationPaik, M., Kim, K., Yoon, H.-R., & Kim, H.-J. (2001) · Journal of Chromatography B Biomedical Sciences and Applications · doi:10.1016/s0378-4347(01)00263-8 · Cited by 22 · see citing works
Wang, L., & Tsai, C. (2000) · Neuroscience Letters · doi:10.1016/s0304-3940(00)01027-2 · Cited by 19 · see citing works
Peroxisomal beta-oxidation enzyme gene expression in the developing mouse brain
Knoll‐Gellida, A., Salles, J., Sargueil, F., Cassagne, C., & Garbay, B. (2000) · Neuroscience Letters · doi:10.1016/s0304-3940(00)01068-5 · Cited by 14 · see citing works
Mitochondrial polarization in rat hippocampal astrocytes is resistant to cytosolic Ca2+ loads
Kahlert, S., Schild, L., & Reiser, G. (2001) · Journal of Neuroscience Research · doi:10.1002/jnr.10052 · Cited by 12 · see citing works
Self-citationOn the Front of X-Linked Adrenoleukodystrophy
Aubourg, P. R. (1999) · Neurochemical Research · doi:10.1023/a:1022583813171 · Cited by 12 · see citing works
Biase, A. D., Avellino, C., Pieroni, F., Quaresima, T., Grisolia, A., Cappa, M., & Salvati, S. (1997) · Neurochemical Research · doi:10.1023/a:1022451108063 · Cited by 12 · see citing works
The X-Linked Adrenoleukodystrophy (X-ALD) and Oxidative Stress
Al-Omar, M. A. (2006) · Journal of Herbal Pharmacotherapy · doi:10.1080/j157v06n03_07 · Cited by 5 · see citing works
Increased activity of surviving locus ceruleus neurons in Alzheimer's disease
Moser (1999) · Pure Amsterdam UMC · doi:10.1002/1531-8249(199901)45:1
Flagged first, then by citations
Cited by
Sorted by citations
Engelen, M., Kemp, S., de Visser, M., van Geel, B. M., Wanders, R. J., Aubourg, P., & Poll-The, B. (2012) · Orphanet Journal of Rare Diseases · doi:10.1186/1750-1172-7-51 · Cited by 562 · see citing works
Schönfeld, P., & Reiser, G. (2013) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2013.128 · Cited by 457 · see citing works
Self-citationMyelin Proteomics: Molecular Anatomy of an Insulating Sheath
Jahn, O., Tenzer, S., & Werner, H. B. (2009) · Molecular Neurobiology · doi:10.1007/s12035-009-8071-2 · Cited by 331 · see citing works
X-linked adrenoleukodystrophy: Clinical, metabolic, genetic and pathophysiological aspects
Kemp, S., Berger, J., & Aubourg, P. (2012) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2012.03.012 · Cited by 283 · see citing works
The peroxisome: an update on mysteries 2.0
Islinger, M., Völkl, A., Fahimi, H. D., & Schrader, M. (2018) · Histochemistry and Cell Biology · doi:10.1007/s00418-018-1722-5 · Cited by 287 · see citing works
The peroxisome: an update on mysteries
Islinger, M., Grille, S., Fahimi, H. D., & Schrader, M. (2012) · Histochemistry and Cell Biology · doi:10.1007/s00418-012-0941-4 · Cited by 279 · see citing works
Adrenoleukodystrophy—Neuroendocrine pathogenesis and redefinition of natural history
Kemp, S., Huffnagel, I. C., Linthorst, G. E., Wanders, R. J., & Engelen, M. (2016) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2016.90 · Cited by 275 · see citing works
Emerging roles for lipids in non-apoptotic cell death
Magtanong, L., Ko, P., & Dixon, S. J. (2016) · Cell Death and Differentiation · doi:10.1038/cdd.2016.25 · Cited by 259 · see citing works
Pathophysiology of X-linked adrenoleukodystrophy
Berger, J., Forss-Petter, S., & Eichler, F. S. (2014) · Biochimie · doi:10.1016/j.biochi.2013.11.023 · Cited by 238 · see citing works
Rönicke, R., Mikhaylova, M., Rönicke, S., Meinhardt, J., Schröder, U. H., Fändrich, M., Reiser, G., Kreutz, M. R., & Reymann, K. G. (2010) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2010.01.011 · Cited by 246 · see citing works
Self-citationEdvardson, S., Hama, H., Shaag, A., Gomori, J. M., Berger, I., Soffer, D., Korman, S. H., Taustein, I., Saada, A., & Elpeleg, O. N. (2008) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2008.10.010 · Cited by 218 · see citing works
Peroxisome‐mitochondria interplay and disease
Schrader, M., Costello, J. L., Godinho, L. F., & Islinger, M. (2015) · Journal of Inherited Metabolic Disease · doi:10.1007/s10545-015-9819-7 · Cited by 217 · see citing works
Turk, B. R., Theda, C., Fatemi, A. S., & Moser, A. B. (2020) · International Journal of Developmental Neuroscience · doi:10.1002/jdn.10003 · Cited by 206 · see citing works
Rose, J., Brian, C., Pappa, A., Panayiotidis, M. I., & Franco, R. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.536682 · Cited by 196 · see citing works
Peroxisomes in brain development and function
Berger, J., Dorninger, F., Forss-Petter, S., & Kunze, M. (2016) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2015.12.005 · Cited by 194 · see citing works
“Furthermore, it has been reported that VLCFA can disturb calcium homeostasis and causemitochondrial dysfunction in neuronal cell cultures aswell as toxicity to oligodendrocytes [133].”
BackgroundX-Linked Adrenoleukodystrophy: Pathogenesis and Treatment
Engelen, M., Kemp, S., & Poll-The, B.-T. (2014) · Current Neurology and Neuroscience Reports · doi:10.1007/s11910-014-0486-0 · Cited by 187 · see citing works
Peroxisomal ABC transporters: Structure, function and role in disease
Morita, M., & Imanaka, T. (2012) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2012.02.009 · Cited by 183 · see citing works
Peroxisomes, lipid metabolism and lipotoxicity
Wanders, R. J. A., Ferdinandusse, S., Brites, P., & Kemp, S. (2010) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2010.01.001 · Cited by 169 · see citing works
Fatty acid metabolism in the progression and resolution of CNS disorders
Bogie, J. F. J., Haidar, M., Kooij, G., & Hendriks, J. J. A. (2020) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2020.01.004 · Cited by 167 · see citing works
Marquez, B., & Françoise Van Bambeke, A. (2011) · Current Drug Targets · doi:10.2174/138945011795378504 · Cited by 165 · see citing works
Pathomechanisms underlying X-adrenoleukodystrophy: A three-hit hypothesis
Singh, I., & Pujol, A. (2010) · Brain Pathology · doi:10.1111/j.1750-3639.2010.00392.x · Cited by 148 · see citing works
Baarine, M., Andreoletti, P., Athias, A., Nury, T., Zarrouk, A., Ragot, K., Véjux, A., Riedinger, J., Kattan, Z., Bessède, G., et al. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.03.058 · Cited by 119 · see citing works
Fatty Acids - Induced Lipotoxicity and Inflammation
Savary, S., Trompier, D., Andreoletti, P., Le Borgne, F., Demarquoy, J., & Lizard, G. (2012) · Current Drug Metabolism · doi:10.2174/138920012803762729 · Cited by 111 · see citing works
Galea, E., Launay, N., Portero-Otin, M., Ruiz, M., Pamplona, R., Aubourg, P., Ferrer, I., & Pujol, A. (2012) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2012.02.005 · Cited by 108 · see citing works
Trompier, D., Véjux, A., Zarrouk, A., Gondcaille, C., Geillon, F., Nury, T., Savary, S., & Lizard, G. (2013) · Biochimie · doi:10.1016/j.biochi.2013.09.009 · Cited by 99 · see citing works
Schönfeld, P., & Reiser, G. (2017) · Neurochemistry International · doi:10.1016/j.neuint.2017.03.018 · Cited by 99 · see citing works
Self-citationCurrent and Future Pharmacological Treatment Strategies in X‐Linked Adrenoleukodystrophy
Berger, J., Pujol, A., Aubourg, P. R., & Forss‐Petter, S. (2010) · Brain Pathology · doi:10.1111/j.1750-3639.2010.00393.x · Cited by 90 · see citing works
Zarrouk, A., Véjux, A., Nury, T., Hajj, H. I. E., Haddad, M., Cherkaoui‐Malki, M., Riedinger, J., Hammami, M., & Lizard, G. (2012) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2012/623257 · Cited by 90 · see citing works
Fourcade, S., Ferrer, I., & Pujol, A. (2015) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2015.05.041 · Cited by 77 · see citing works
Organelle interplay in peroxisomal disorders
Thoms, S., Grønborg, S. W., & Gärtner, J. (2009) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2009.05.002 · Cited by 74 · see citing works
Functional genomic analysis unravels a metabolic-inflammatory interplay in adrenoleukodystrophy
Schlüter, A., Espinosa, L., Fourcade, S., Galino, J., López, E., Ilieva, E., Morató, L., Asheuer, M., Cook, T., McLaren, A., et al. (2012) · Human Molecular Genetics · doi:10.1093/hmg/ddr536 · Cited by 72 · see citing works
How the brain fights fatty acids’ toxicity
Schönfeld, P., & Reiser, G. (2021) · Neurochemistry International · doi:10.1016/j.neuint.2021.105050 · Cited by 70 · see citing works
Self-citationHartley, M. D., Kirkemo, L. L., Banerji, T., & Scanlan, T. S. (2017) · Endocrinology · doi:10.1210/en.2016-1842 · Cited by 71 · see citing works
Schönfeld, P., & Reiser, G. (2016) · Aging and Disease · doi:10.14336/ad.2015.0823 · Cited by 69 · see citing works
Self-citationThyroid Hormone Signaling in Oligodendrocytes: from Extracellular Transport to Intracellular Signal
Lee, J. Y., & Petratos, S. (2016) · Molecular Neurobiology · doi:10.1007/s12035-016-0013-1 · Cited by 70 · see citing works
Kumar, V., & Chandra, R. (2020) · 3 Biotech · doi:10.1007/s13205-020-02310-5 · Cited by 68 · see citing works
Launay, N., Ruíz, M., Grau, L., Ortega, F. J., Ilieva, E. V., Martínez, J. J., Galea, E., Ferrer, I., Knecht, E., Pujol, A., et al. (2016) · Acta Neuropathologica · doi:10.1007/s00401-016-1655-9 · Cited by 63 · see citing works
Rönicke, S., Kruska, N., Kahlert, S., & Reiser, G. (2009) · Neurobiology of Disease · doi:10.1016/j.nbd.2009.08.005 · Cited by 62 · see citing works
Self-citationKruska, N., Schönfeld, P., Pujol, A., & Reiser, G. (2015) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2015.01.005 · Cited by 56 · see citing works
Self-citationLipids in the Physiopathology of Hereditary Spastic Paraplegias
Darios, F. D., Mochel, F., & Stévanin, G. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.00074 · Cited by 56 · see citing works
Fourcade, S., López-Erauskin, J., Ruiz, M., Ferrer, I., & Pujol, A. (2014) · Biochimie · doi:10.1016/j.biochi.2013.09.012 · Cited by 55 · see citing works
Aberrant regulation of the GSK‐3β/NRF2 axis unveils a novel therapy for adrenoleukodystrophy
Ranea‐Robles, P., Launay, N., Ruíz, M., Calingasan, N. Y., Dumont, M., Naudí, A., Portero‐Otín, M., Pamplona, R., Ferrer, I., Beal, M. F., et al. (2018) · EMBO Molecular Medicine · doi:10.15252/emmm.201708604 · Cited by 55 · see citing works
Microglial dysfunction as a key pathological change in adrenomyeloneuropathy
Gong, Y., Sasidharan, N., Laheji, F., Frosch, M., Musolino, P., Tanzi, R., Kim, D. Y., Biffi, A., El Khoury, J., & Eichler, F. (2017) · Annals of Neurology · doi:10.1002/ana.25085 · Cited by 54 · see citing works
Leukodystrophies with late disease onset: an update
Köhler, W. (2010) · Current Opinion in Neurology · doi:10.1097/wco.0b013e328338313a · Cited by 54 · see citing works
Nury, T., Sghaier, R., Zarrouk, A., Ménétrier, F., Uzun, T., Leoni, V., Caccia, C., Meddeb, W., Namsi, A., Sassi, K., et al. (2018) · Biochimie · doi:10.1016/j.biochi.2018.07.009 · Cited by 54 · see citing works
Baarine, M., Ragot, K., Genin, E. C., Hajj, H. I. E., Trompier, D., Andreoletti, P., Ghandour, M. S., Ménétrier, F., Cherkaoui‐Malki, M., Savary, S., et al. (2009) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2009.06311.x · Cited by 51 · see citing works
Khan, M., Singh, J., Gilg, A. G., Uto, T., & Singh, I. (2010) · Journal of Lipid Research · doi:10.1194/jlr.m002329 · Cited by 49 · see citing works
Therapy of X-linked adrenoleukodystrophy
Semmler, A., Köhler, W., Jung, H. H., Weller, M., & Linnebank, M. (2008) · Expert Review of Neurotherapeutics · doi:10.1586/14737175.8.9.1367 · Cited by 49 · see citing works
Baarine, M., Beeson, C. C., Singh, A. K., & Singh, I. (2014) · Journal of Neurochemistry · doi:10.1111/jnc.12992 · Cited by 48 · see citing works
C26:0-Carnitine Is a New Biomarker for X-Linked Adrenoleukodystrophy in Mice and Man
van de Beek, M.-C., Dijkstra, I. M. E., van Lenthe, H., Ofman, R., Goldhaber-Pasillas, D., Schauer, N., Schackmann, M., Engelen-Lee, J.-Y., Vaz, F. M., Kulik, W., et al. (2016) · PLOS ONE · doi:10.1371/journal.pone.0154597 · Cited by 48 · see citing works
Lipid-induced endoplasmic reticulum stress in X-linked adrenoleukodystrophy
van de Beek, M.-C., Ofman, R., Dijkstra, I. M. E., Wijburg, F. A., Engelen, M., Wanders, R. J. A., & Kemp, S. (2017) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2017.06.003 · Cited by 46 · see citing works
Peroxisomal Disorders: A Review on Cerebellar Pathologies
Munter, S. D., Verheijden, S., Régal, L., & Baes, M. I. (2015) · Brain Pathology · doi:10.1111/bpa.12290 · Cited by 44 · see citing works
Baarine, M., Ragot, K., Athias, A., Nury, T., Kattan, Z., Genin, E. C., Andreoletti, P., Ménétrier, F., Riedinger, J.-M., Bardou, M., et al. (2012) · NeuroToxicology · doi:10.1016/j.neuro.2011.10.007 · Cited by 43 · see citing works
Metabolic rerouting via SCD1 induction impacts X-linked adrenoleukodystrophy
Raas, Q., van de Beek, M.-C., Forss‐Petter, S., Dijkstra, I. M. E., Deschiffart, A., Freshner, B. C., Stevenson, T. J., Jaspers, Y. R. J., Nagtzaam, L., Wanders, R. J. A., et al. (2021) · Journal of Clinical Investigation · doi:10.1172/jci142500 · Cited by 41 · see citing works
Rodríguez-Pascau, L., Vilalta, A., Cerrada, M., Traver, E., Forss-Petter, S., Weinhofer, I., Bauer, J., Kemp, S., Pina, G., Pascual, S., et al. (2021) · Science Translational Medicine · doi:10.1126/scitranslmed.abc0555 · Cited by 40 · see citing works
Functional Characterization of IPSC-Derived Brain Cells as a Model for X-Linked Adrenoleukodystrophy
Baarine, M., Khan, M., Singh, A., & Singh, I. (2015) · PLOS ONE · doi:10.1371/journal.pone.0143238 · Cited by 38 · see citing works
Lee, D., Long, N. P., Jung, J., Kim, T., Na, E., Kang, Y. P., Kwon, S. W., & Jang, J. (2018) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2018.11.123 · Cited by 37 · see citing works
Singh, J., Khan, M., & Singh, I. (2011) · Journal of Lipid Research · doi:10.1194/jlr.m017491 · Cited by 37 · see citing works
Mitochondrial Dysfunction in Demyelinating Diseases
Carvalho, K. S. (2013) · Seminars in Pediatric Neurology · doi:10.1016/j.spen.2013.09.001 · Cited by 35 · see citing works
Kim, Y., Nam, I., Lee, D., Bhandari, S., Charton, L., Kwak, S., Lim, J., Hong, K., Kim, S., Lee, J. N., et al. (2019) · Journal of Cellular Physiology · doi:10.1002/jcp.28954 · Cited by 35 · see citing works
Protective function of autophagy during VLCFA-induced cytotoxicity in a neurodegenerative cell model
Doria, M., Nury, T., Delmas, D., Moreau, T., Lizard, G., & Véjux, A. (2019) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2019.04.016 · Cited by 33 · see citing works
Kimmerling, K. A., Oswald, S. J., Huebner, J. L., Little, D., Kraus, V. B., Kang, J. X., Wu, C., & Guilak, F. (2020) · Arthritis Research & Therapy · doi:10.1186/s13075-020-02170-7 · Cited by 33 · see citing works
Groh, J., & Martini, R. (2017) · Glia · doi:10.1002/glia.23162 · Cited by 32 · see citing works
Zhou, J., Terluk, M. R., Orchard, P. J., Cloyd, J. C., & Kartha, R. V. (2021) · Biomedicines · doi:10.3390/biomedicines9121826 · Cited by 30 · see citing works
Ghzaiel, I., Zarrouk, A., Essadek, S., Martine, L., Hammouda, S., Yammine, A., Ksila, M., Nury, T., Meddeb, W., Tahri-Joutey, M., et al. (2022) · Steroids · doi:10.1016/j.steroids.2022.109032 · Cited by 30 · see citing works
Singh, I., Singh, A. K., & Contreras, M. A. (2009) · Journal of Child Neurology · doi:10.1177/0883073809338327 · Cited by 30 · see citing works
Emerging cellular themes in leukodystrophies
Nowacki, J. C., Fields, A. M., & Fu, M. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.902261 · Cited by 29 · see citing works
Sivachenko, A., Gordon, H. B., Kimball, S. S., Gavin, E., Bonkowsky, J. L., & Letsou, A. (2016) · Disease Models & Mechanisms · doi:10.1242/dmm.022244 · Cited by 29 · see citing works
X-linked adrenoleukodystrophy and primary adrenal insufficiency
Cappa, M., Todisco, T., & Bizzarri, C. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1309053 · Cited by 28 · see citing works
Dietary rescue of lipotoxicity-induced mitochondrial damage in Peroxin19 mutants
Sellin, J., Wingen, C., Gosejacob, D., Senyilmaz, D., Hänschke, L., Büttner, S., Meyer, K., Bano, D., Nicotera, P., Teleman, A. A., et al. (2018) · PLoS Biology · doi:10.1371/journal.pbio.2004893 · Cited by 27 · see citing works
Pillai, B. K., Jasuja, R., Simard, J. R., & Hamilton, J. A. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.043737 · Cited by 27 · see citing works
Bezine, M., Debbabi, M., Nury, T., Khalifa, R. B., Samadi, M. H., Cherkaoui‐Malki, M., Véjux, A., Raas, Q., Seze, J. D., Moreau, T., et al. (2017) · Chemistry and Physics of Lipids · doi:10.1016/j.chemphyslip.2017.03.006 · Cited by 26 · see citing works
Stradomska, T. J., Syczewska, M., Jamroz, E., Pleskaczyńska, A., Kruczek, P., Ciara, E., & Tylki‐Szymańska, A. (2020) · PLoS ONE · doi:10.1371/journal.pone.0238796 · Cited by 25 · see citing works
Singh, J., Khan, M., Pujol, A., Baarine, M., & Singh, I. (2013) · PLoS ONE · doi:10.1371/journal.pone.0070712 · Cited by 24 · see citing works
Singh, J., Khan, M., & Singh, I. (2013) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2013.01.004 · Cited by 21 · see citing works
Wang, R., Monuki, E. S., Powers, J., Schwartz, P. H., Watkins, P. A., Shi, Y., Moser, A. B., Shrier, D. A., Waterham, H. R., Nugent, D. J., et al. (2014) · Journal of Inherited Metabolic Disease · doi:10.1007/s10545-014-9698-3 · Cited by 22 · see citing works
(2006) · Springer eBooks · doi:10.1007/3-540-29623-9_9160 · Cited by 21 · see citing works
Discovery of Novel, Orally Bioavailable Pyrimidine Ether-Based Inhibitors of ELOVL1
Boyd, M. J., Collier, P. N., Clark, M. P., Deng, H., Kesavan, S., Ronkin, S. M., Waal, N. D., Wang, J., Cao, J., Li, P., et al. (2021) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.1c00948 · Cited by 19 · see citing works
The Role of Oxidative Stress and Inflammation in X-Link Adrenoleukodystrophy
Yu, J., Chen, T., Guo, X., Zafar, M. I., Li, H., Wang, Z., & Zheng, J. (2022) · Frontiers in Nutrition · doi:10.3389/fnut.2022.864358 · Cited by 19 · see citing works
The pathology of X-linked adrenoleukodystrophy: Tissue specific changes as a clue to pathophysiology
Yska, H. A. F., Engelen, M., & Bugiani, M. (2024) · Orphanet Journal of Rare Diseases · doi:10.1186/s13023-024-03105-0 · Cited by 20 · see citing works
Hama, K., Nagai, T., 西澤, 千., Ikeda, K., Morita, M., Satoh, N., Nakanishi, H., Imanaka, T., Shimozawa, N., Taguchi, R., et al. (2013) · Lipids · doi:10.1007/s11745-013-3848-5 · Cited by 20 · see citing works
In Vivo NMR Studies of the Brain with Hereditary or Acquired Metabolic Disorders
Sherry, E. B., Lee, P., & Choi, I.-Y. (2015) · Neurochemical Research · doi:10.1007/s11064-015-1772-1 · Cited by 18 · see citing works
Nury, T., Doria, M., Lizard, G., & Véjux, A. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21020641 · Cited by 20 · see citing works
Bezine, M., Maatoug, S., Khalifa, R. B., Debbabi, M., Zarrouk, A., Wang, Y., Griffiths, W. J., Nury, T., Samadi, M. H., Véjux, A., et al. (2018) · Biochimie · doi:10.1016/j.biochi.2018.02.008 · Cited by 19 · see citing works
Etiology and treatment of adrenoleukodystrophy: new insights from Drosophila
Gordon, H. B., Valdez, L., & Letsou, A. (2018) · Disease Models & Mechanisms · doi:10.1242/dmm.031286 · Cited by 19 · see citing works
Beneficial reward-to-risk action of glucosamine during pathogenesis of osteoarthritis
Kang, Y.-H., Park, S., Ahn, C., Song, J., Kim, D., & Jin, E. (2015) · European journal of medical research · doi:10.1186/s40001-015-0176-7 · Cited by 19 · see citing works
Pujol, A. (2015) · Endocrine development · doi:10.1159/000439340 · Cited by 18 · see citing works
Verheijden, S., Beckers, L., Munter, S. D., Veldhoven, P. P. V., & Baes, M. I. (2013) · Biochimie · doi:10.1016/j.biochi.2013.08.009 · Cited by 18 · see citing works
Discovery and Optimization of Pyrazole Amides as Inhibitors of ELOVL1
Come, J. H., Senter, T. J., Clark, M. P., Court, J. J., Gale-Day, Z. J., Gu, W., Krueger, E. B., Liang, J., Morris, M., Nanthakumar, S. S., et al. (2021) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.1c00944 · Cited by 16 · see citing works
ABCD1 Gene Mutations: Mechanisms and Management of Adrenomyeloneuropathy
Volmrich, A. M., Cuénant, L. M., Forghani, I., Hsieh, S. L., & Shapiro, L. T. (2022) · The Application of Clinical Genetics · doi:10.2147/tacg.s359479 · Cited by 17 · see citing works
Nury, T., Yammine, A., Ménétrier, F., Zarrouk, A., Véjux, A., & Lizard, G. (2020) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-60204-8_3 · Cited by 17 · see citing works
Monternier, P., Singh, J., Parasar, P., Theurey, P., DeWitt, S. H., Jacques, V., Klett, E. L., Kaur, N., Nagaraja, T. N., Moller, D. E., et al. (2022) · Journal of Inherited Metabolic Disease · doi:10.1002/jimd.12510 · Cited by 17 · see citing works
Marchetti, D. P., Reinhardt, L. S., Jacques, C. E. D., Guerreiro, G., Mescka, C. P., Deon, M., Coelho, D. D. M., Moura, D. J., Viario, A. G., Poletto, F. S., et al. (2018) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-018-0626-1 · Cited by 17 · see citing works
Trompier, D., & Savary, S. (2013) · Colloquium Series on The Genetic Basis of Human Disease · doi:10.4199/c00075ed1v01y201303gbd004 · Cited by 16 · see citing works
Turk, B. R., Theda, C., Fatemi, A. S., & Moser, A. B. (2019) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2019.11.002 · Cited by 17 · see citing works
Peroxisomes attenuate cytotoxicity of very long-chain fatty acids
Ali, H., Kobayashi, M., Morito, K., Hasi, R. Y., Aihara, M., Hayashi, J., Kawakami, R., Tsuchiya, K., Sango, K., & Tanaka, T. (2022) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2022.159259 · Cited by 15 · see citing works
Schönfeld, P., Kruska, N., & Reiser, G. (2009) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2009.09.008 · Cited by 15 · see citing works
Self-citationAntioxidant Response in Human X-Linked Adrenoleukodystrophy Fibroblasts
Petrillo, S., D’Amico, J., Nicita, F., Torda, C., Vasco, G., Bertini, E., Cappa, M., & Piemonte, F. (2022) · Antioxidants · doi:10.3390/antiox11112125 · Cited by 13 · see citing works
Pathophysiology of X-Linked Adrenoleukodystrophy: Updates on Molecular Mechanisms
Parasar, P., Kaur, N., & Singh, J. (2024) · Journal of Biotechnology and Biomedicine · doi:10.26502/jbb.2642-91280151 · Cited by 12 · see citing works
Adrenoleukodystrophy: a forgotten diagnosis in children with primary Addison's disease: Figure 1
Nascimento, M., Rodrigues, N., Espada, F., & Fonseca, M. (2012) · BMJ Case Reports · doi:10.1136/bcr-2012-006308 · Cited by 12 · see citing works
- Authors
- Hein, S., Schonfeld, P., Kahlert, S., & Reiser, G.
- Affiliations
- Otto-von-Guericke-Universität Magdeburg (DE)
- Corresponding author
- Reiser, G.
- ORCID
- Kahlert, S.
- Venue
- Human Molecular Genetics
- Publisher
- Oxford University Press (OUP)
- Published
- 2008-03-04
- Volume
- 17
- Issue
- 12
- Pages
- 1750-1761
- ISSN
- 0964-6906 (ISSN-L)
- 1460-2083
- OpenAlex
- W2167261850
- Cited by
- 180
- References
- 69
- Citations by year
- 2026: 10 · 2025: 5 · 2024: 17 · 2023: 6 · 2022: 11 · 2021: 13 · 2020: 15 · 2019: 4 · 2018: 11 · 2017: 7 · 2016: 11 · 2015: 10 · 2014: 8 · 2013: 15 · 2012: 9
- FWCI
- 5.98
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Human Molecular Genetics (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Clinical Biochemistry › Metabolism and Genetic Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Health Sciences › Medicine › Physiology › Lysosomal Storage Disorders Research
- Keywords
- X-linked adrenoleukodystrophy, very long chain fatty acids, oligodendrocytes, astrocytes, hippocampus, mitochondrial depolarization, mitochondrial permeability transition, peroxisomal dysfunction, neurodegeneration, docosanoic acid, tetracosanoic acid, hexacosanoic acid, cell death
- MeSH terms
- Adrenoleukodystrophy, Animals, Astrocytes, Cells, Cultured, Fatty Acids, Hippocampus, Mitochondria, Neuroglia, Neurons, Oligodendroglia, Cell Death, Rats, Wistar, Reactive Oxygen Species, Calcium Signaling, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review