Cited by 177Hypothalamic control of reproductive hormonesProteoglycans and glycosaminoglycans researchSexual Differentiation and Disorders

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Heparan sulfate 6-O-sulfotransferase 1 , a gene involved in extracellular sugar modifications, is mutated in patients with idiopathic hypogonadotrophic hypogonadism

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Tornberg, Janne, Sykiotis, Gerasimos P., Keefe, Kimberly, Plummer, Lacey, Hoang, Xuan, Hall, Janet E., Quinton, Richard, Seminara, Stephanie B., Hughes, Virginia, Van Vliet, Guy, Van Uum, Stan, Crowley, William F., Habuchi, Hiroko, Kimata, Koji, Pitteloud, Nelly, Bülow, Hannes E.·2011·Proceedings of the National Academy of Sciences

DOI 10.1073/pnas.1102284108PMC PMC3136273

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Abstract

Neuronal development is the result of a multitude of neural migrations, which require extensive cell-cell communication. These processes are modulated by extracellular matrix components, such as heparan sulfate (HS) polysaccharides. HS is molecularly complex as a result of nonrandom modifications of the sugar moieties, including sulfations in specific positions. We report here mutations in HS 6-O-sulfotransferase 1 (HS6ST1) in families with idiopathic hypogonadotropic hypogonadism (IHH). IHH manifests as incomplete or absent puberty and infertility as a result of defects in gonadotropin-releasing hormone neuron development or function. IHH-associated HS6ST1 mutations display reduced activity in vitro and in vivo, suggesting that HS6ST1 and the complex modifications of extracellular sugars are critical for normal development in humans. Genetic experiments in Caenorhabditis elegans reveal that HS cell-specifically regulates neural branching in vivo in concert with other IHH-associated genes, including kal-1, the FGF receptor, and FGF. These findings are consistent with a model in which KAL1 can act as a modulatory coligand with FGF to activate the FGF receptor in an HS-dependent manner.

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Franco, B., Guioli, S., Pragliola, A., Incerti, B., Bardoni, B., Tonlorenzi, R., Carrozzo, R., Maestrini, E., Pieretti, M., Taillon-Miller, P., et al. (1991) · Nature · doi:10.1038/353529a0 · Cited by 846
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Dodé, C., Levilliers, J., Dupont, J., Paepe, A. D., Dû, N. L., Soussi‐Yanicostas, N., Coimbra, R. S., Delmaghani, S., Nouaille, S., Baverel, F., et al. (2003) · Nature Genetics · doi:10.1038/ng1122 · Cited by 839
Regulated Diversity of Heparan Sulfate*
Lindahl, U., Kusche-Gullberg, M., & Kjellén, L. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.39.24979 · Cited by 688
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Legouis, R., Hardelin, J.-P., Levilliers, J., Claverie, J.-M., Compain, S., Wunderle, V., Millasseau, P., Le Paslier, D., Cohen, D., & Caterina, D. (1991) · Cell · doi:10.1016/0092-8674(91)90193-3 · Cited by 678
Luteinizing hormone-releasing hormone (LHRH)-expressing cells do not migrate normally in an inherited hypogonadal (Kallmann) syndrome
Schwanzel-Fukuda, M., Bick, D., & Pfaff, D. W. (1989) · Molecular Brain Research · doi:10.1016/0169-328x(89)90076-4 · Cited by 616
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de Roux, N., Young, J., Misrahi, M., Genet, R., Chanson, P., Schaison, G., & Milgrom, E. (1997) · New England Journal of Medicine · doi:10.1056/nejm199711273372205 · Cited by 518
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Dodé, C., Teixeira, L., Levilliers, J., Fouveaut, C., Bouchard, P., Kottler, M.-L., Lespinasse, J., Lienhardt-Roussie, A., Mathieu, M., Moerman, A., et al. (2006) · PLoS Genetics · doi:10.1371/journal.pgen.0020175 · Cited by 457
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Inatani, M., Irie, F., Plump, A. S., Tessier-Lavigne, M., & Yamaguchi, Y. (2003) · Science · doi:10.1126/science.1090497 · Cited by 431

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Authors: Tornberg, J., Sykiotis, G. P., Keefe, K., Plummer, L., Hoang, X., Hall, J. E., Quinton, R., Seminara, S. B., Hughes, V., Van Vliet, G., Van Uum, S., Crowley, W. F., Habuchi, H., Kimata, K., Pitteloud, N., & Bülow, H. E.
Affiliations: Albert Einstein College of Medicine (US)
Harvard University (US)
Newcastle University (GB)
Centre Hospitalier Universitaire Sainte-Justine, Université de Montréal, Montreal, QC, Canada H3T 1C5;
Department of Medicine, Lawson Health Research Institute, University of Western Ontario, London, ON, Canada N6A 4V2; and
Aichi Medical University (JP)
ORCID: Sykiotis, Gerasimos P.
Keefe, Kimberly
Hall, Janet E.
Quinton, Richard
Seminara, Stephanie B.
Crowley, William F.
Kimata, Koji
Pitteloud, Nelly
Bülow, Hannes E.
Venue: Proceedings of the National Academy of Sciences
Publisher: National Academy of Sciences
Published: 2011-06-23
Volume: 108
Issue: 28
Pages: 11524-11529
ISSN: 0027-8424 (ISSN-L)
1091-6490
DOI: 10.1073/pnas.1102284108
PMC: PMC3136273
OpenAlex: W2098762562
Cited by: 177
References: 43
Citations by year: 2026: 9 · 2025: 7 · 2024: 2 · 2023: 4 · 2022: 13 · 2021: 17 · 2020: 11 · 2019: 11 · 2018: 11 · 2017: 9 · 2016: 17 · 2015: 19 · 2014: 19 · 2013: 15 · 2012: 10
FWCI: 16.57
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Proceedings of the National Academy of Sciences (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
IRIS (submittedVersion)
SERVAL (Université de Lausanne) (submittedVersion)
Funders: Japan Society for the Promotion of Science (23570148)
National Center for Research Resources (UL1RR025758, M01RR001066)
Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD015788, R01HD056264, R01HD055380, U54HD028138)
Topics: Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Proteoglycans and glycosaminoglycans research
Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Sexual Differentiation and Disorders
Keywords: idiopathic hypogonadotropic hypogonadism, heparan sulfate sulfation, extracellular matrix, GnRH neurons, neuronal migration, fibroblast growth factor receptor, FGF signaling, Caenorhabditis elegans, genetic mutations
MeSH terms: Adult, Amino Acid Sequence, Animals, Child, Female, Humans, Hypogonadism, Male, Middle Aged, Models, Molecular, Molecular Sequence Data, Mutation, Nerve Tissue Proteins, Pedigree, Species Specificity, Sulfotransferases, Extracellular Matrix Proteins, Caenorhabditis elegans, Genes, Helminth, Sequence Homology, Amino Acid, Kallmann Syndrome, Receptors, Fibroblast Growth Factor, Amino Acid Substitution, Mutation, Missense, Caenorhabditis elegans Proteins, Intercellular Signaling Peptides and Proteins, Receptor, Fibroblast Growth Factor, Type 1, In Vitro Techniques

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Heparan sulfate 6-O-sulfotransferase 1 , a gene involved in extracellular sugar modifications, is mutated in patients with idiopathic hypogonadotrophic hypogonadism

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