Insights into the hyperglycosylation of human chorionic gonadotropin revealed by glycomics analysis
Human chorionic gonadotropin (hCG) is a glycoprotein hormone that is essential for the maintenance of pregnancy. Glycosylation of hCG is known to be essential for its biological activity. "Hyperglycosylated" variants secreted during early pregnancy have been proposed to be involved in init...
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| Published in: | PloS one Vol. 15; no. 2; p. e0228507 |
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| Main Authors: | , , , , , , , , , , , , , , , , , |
| Format: | Journal Article |
| Language: | English |
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11.02.2020
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| ISSN: | 1932-6203, 1932-6203 |
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| Abstract | Human chorionic gonadotropin (hCG) is a glycoprotein hormone that is essential for the maintenance of pregnancy. Glycosylation of hCG is known to be essential for its biological activity. "Hyperglycosylated" variants secreted during early pregnancy have been proposed to be involved in initial implantation of the embryo and as a potential diagnostic marker for gestational diseases. However, what constitutes "hyperglycosylation" is not yet fully understood. In this study, we perform comparative N-glycomic analysis of hCG expressed in the same individuals during early and late pregnancy to help provide new insights into hCG function, reveal new targets for diagnostics and clarify the identity of hyperglycosylated hCG. hCG was isolated in urine collected from women at 7 weeks and 20 weeks' gestation. hCG was also isolated in urine from women diagnosed with gestational trophoblastic disease (GTD). We used glycomics methodologies including matrix assisted laser desorption/ionisation-time of flight (MALDI-TOF) mass spectrometry (MS) and MS/MS methods to characterise the N-glycans associated with hCG purified from the individual samples. The structures identified on the early pregnancy (EP-hCG) and late pregnancy (LP-hCG) samples corresponded to mono-, bi-, tri-, and tetra-antennary N-glycans. A novel finding was the presence of substantial amounts of bisected type N-glycans in pregnancy hCG samples, which were present at much lower levels in GTD samples. A second novel observation was the presence of abundant LewisX antigens on the bisected N-glycans. GTD-hCG had fewer glycoforms which constituted a subset of those found in normal pregnancy. When compared to EP-hCG, GTD-hCG samples had decreased signals for tri- and tetra-antennary N-glycans. In terms of terminal epitopes, GTD-hCG had increased signals for sialylated structures, while LewisX antigens were of very minor abundance. hCG carries the same N-glycans throughout pregnancy but in different proportions. The N-glycan repertoire is more diverse than previously reported. Bisected and LewisX structures are potential targets for diagnostics. hCG isolated from pregnancy urine inhibits NK cell cytotoxicity in vitro at nanomolar levels and bisected type glycans have previously been implicated in the suppression of NK cell cytotoxicity, suggesting that hCG-related bisected type N-glycans may directly suppress NK cell cytotoxicity. |
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| AbstractList | Human chorionic gonadotropin (hCG) is a glycoprotein hormone that is essential for the maintenance of pregnancy. Glycosylation of hCG is known to be essential for its biological activity. "Hyperglycosylated" variants secreted during early pregnancy have been proposed to be involved in initial implantation of the embryo and as a potential diagnostic marker for gestational diseases. However, what constitutes "hyperglycosylation" is not yet fully understood. In this study, we perform comparative N-glycomic analysis of hCG expressed in the same individuals during early and late pregnancy to help provide new insights into hCG function, reveal new targets for diagnostics and clarify the identity of hyperglycosylated hCG. hCG was isolated in urine collected from women at 7 weeks and 20 weeks' gestation. hCG was also isolated in urine from women diagnosed with gestational trophoblastic disease (GTD). We used glycomics methodologies including matrix assisted laser desorption/ionisation-time of flight (MALDI-TOF) mass spectrometry (MS) and MS/MS methods to characterise the N-glycans associated with hCG purified from the individual samples. The structures identified on the early pregnancy (EP-hCG) and late pregnancy (LP-hCG) samples corresponded to mono-, bi-, tri-, and tetra-antennary N-glycans. A novel finding was the presence of substantial amounts of bisected type N-glycans in pregnancy hCG samples, which were present at much lower levels in GTD samples. A second novel observation was the presence of abundant LewisX antigens on the bisected N-glycans. GTD-hCG had fewer glycoforms which constituted a subset of those found in normal pregnancy. When compared to EP-hCG, GTD-hCG samples had decreased signals for tri- and tetra-antennary N-glycans. In terms of terminal epitopes, GTD-hCG had increased signals for sialylated structures, while LewisX antigens were of very minor abundance. hCG carries the same N-glycans throughout pregnancy but in different proportions. The N-glycan repertoire is more diverse than previously reported. Bisected and LewisX structures are potential targets for diagnostics. hCG isolated from pregnancy urine inhibits NK cell cytotoxicity in vitro at nanomolar levels and bisected type glycans have previously been implicated in the suppression of NK cell cytotoxicity, suggesting that hCG-related bisected type N-glycans may directly suppress NK cell cytotoxicity. Human chorionic gonadotropin (hCG) is a glycoprotein hormone that is essential for the maintenance of pregnancy. Glycosylation of hCG is known to be essential for its biological activity. "Hyperglycosylated" variants secreted during early pregnancy have been proposed to be involved in initial implantation of the embryo and as a potential diagnostic marker for gestational diseases. However, what constitutes "hyperglycosylation" is not yet fully understood. In this study, we perform comparative N-glycomic analysis of hCG expressed in the same individuals during early and late pregnancy to help provide new insights into hCG function, reveal new targets for diagnostics and clarify the identity of hyperglycosylated hCG. hCG was isolated in urine collected from women at 7 weeks and 20 weeks' gestation. hCG was also isolated in urine from women diagnosed with gestational trophoblastic disease (GTD). We used glycomics methodologies including matrix assisted laser desorption/ionisation-time of flight (MALDI-TOF) mass spectrometry (MS) and MS/MS methods to characterise the N-glycans associated with hCG purified from the individual samples. The structures identified on the early pregnancy (EP-hCG) and late pregnancy (LP-hCG) samples corresponded to mono-, bi-, tri-, and tetra-antennary N-glycans. A novel finding was the presence of substantial amounts of bisected type N-glycans in pregnancy hCG samples, which were present at much lower levels in GTD samples. A second novel observation was the presence of abundant LewisX antigens on the bisected N-glycans. GTD-hCG had fewer glycoforms which constituted a subset of those found in normal pregnancy. When compared to EP-hCG, GTD-hCG samples had decreased signals for tri- and tetra-antennary N-glycans. In terms of terminal epitopes, GTD-hCG had increased signals for sialylated structures, while LewisX antigens were of very minor abundance. hCG carries the same N-glycans throughout pregnancy but in different proportions. The N-glycan repertoire is more diverse than previously reported. Bisected and LewisX structures are potential targets for diagnostics. hCG isolated from pregnancy urine inhibits NK cell cytotoxicity in vitro at nanomolar levels and bisected type glycans have previously been implicated in the suppression of NK cell cytotoxicity, suggesting that hCG-related bisected type N-glycans may directly suppress NK cell cytotoxicity.Human chorionic gonadotropin (hCG) is a glycoprotein hormone that is essential for the maintenance of pregnancy. Glycosylation of hCG is known to be essential for its biological activity. "Hyperglycosylated" variants secreted during early pregnancy have been proposed to be involved in initial implantation of the embryo and as a potential diagnostic marker for gestational diseases. However, what constitutes "hyperglycosylation" is not yet fully understood. In this study, we perform comparative N-glycomic analysis of hCG expressed in the same individuals during early and late pregnancy to help provide new insights into hCG function, reveal new targets for diagnostics and clarify the identity of hyperglycosylated hCG. hCG was isolated in urine collected from women at 7 weeks and 20 weeks' gestation. hCG was also isolated in urine from women diagnosed with gestational trophoblastic disease (GTD). We used glycomics methodologies including matrix assisted laser desorption/ionisation-time of flight (MALDI-TOF) mass spectrometry (MS) and MS/MS methods to characterise the N-glycans associated with hCG purified from the individual samples. The structures identified on the early pregnancy (EP-hCG) and late pregnancy (LP-hCG) samples corresponded to mono-, bi-, tri-, and tetra-antennary N-glycans. A novel finding was the presence of substantial amounts of bisected type N-glycans in pregnancy hCG samples, which were present at much lower levels in GTD samples. A second novel observation was the presence of abundant LewisX antigens on the bisected N-glycans. GTD-hCG had fewer glycoforms which constituted a subset of those found in normal pregnancy. When compared to EP-hCG, GTD-hCG samples had decreased signals for tri- and tetra-antennary N-glycans. In terms of terminal epitopes, GTD-hCG had increased signals for sialylated structures, while LewisX antigens were of very minor abundance. hCG carries the same N-glycans throughout pregnancy but in different proportions. The N-glycan repertoire is more diverse than previously reported. Bisected and LewisX structures are potential targets for diagnostics. hCG isolated from pregnancy urine inhibits NK cell cytotoxicity in vitro at nanomolar levels and bisected type glycans have previously been implicated in the suppression of NK cell cytotoxicity, suggesting that hCG-related bisected type N-glycans may directly suppress NK cell cytotoxicity. Human chorionic gonadotropin (hCG) is a glycoprotein hormone that is essential for the maintenance of pregnancy. Glycosylation of hCG is known to be essential for its biological activity. "Hyperglycosylated" variants secreted during early pregnancy have been proposed to be involved in initial implantation of the embryo and as a potential diagnostic marker for gestational diseases. However, what constitutes "hyperglycosylation" is not yet fully understood. In this study, we perform comparative N-glycomic analysis of hCG expressed in the same individuals during early and late pregnancy to help provide new insights into hCG function, reveal new targets for diagnostics and clarify the identity of hyperglycosylated hCG. hCG was isolated in urine collected from women at 7 weeks and 20 weeks' gestation. hCG was also isolated in urine from women diagnosed with gestational trophoblastic disease (GTD). We used glycomics methodologies including matrix assisted laser desorption/ionisation-time of flight (MALDI-TOF) mass spectrometry (MS) and MS/MS methods to characterise the N-glycans associated with hCG purified from the individual samples. The structures identified on the early pregnancy (EP-hCG) and late pregnancy (LP-hCG) samples corresponded to mono-, bi-, tri-, and tetra-antennary N-glycans. A novel finding was the presence of substantial amounts of bisected type N-glycans in pregnancy hCG samples, which were present at much lower levels in GTD samples. A second novel observation was the presence of abundant Lewis.sup.X antigens on the bisected N-glycans. GTD-hCG had fewer glycoforms which constituted a subset of those found in normal pregnancy. When compared to EP-hCG, GTD-hCG samples had decreased signals for tri- and tetra-antennary N-glycans. In terms of terminal epitopes, GTD-hCG had increased signals for sialylated structures, while Lewis.sup.X antigens were of very minor abundance. hCG carries the same N-glycans throughout pregnancy but in different proportions. The N-glycan repertoire is more diverse than previously reported. Bisected and Lewis.sup.X structures are potential targets for diagnostics. hCG isolated from pregnancy urine inhibits NK cell cytotoxicity in vitro at nanomolar levels and bisected type glycans have previously been implicated in the suppression of NK cell cytotoxicity, suggesting that hCG-related bisected type N-glycans may directly suppress NK cell cytotoxicity. |
| Audience | Academic |
| Author | Bourne, Tom Dell, Anne Almeida, Paula Haslam, Stuart M. Davis, Mark Johnson, Mark R. Bobdiwala, Shabnam Harvey, Richard Ibeto, Linda Norman Taylor, Julian Antonopoulos, Aristotelis Al-Memar, Maya Pang, Poh-Choo Seckl, Michael Clark, Gary Davis, Paul Panico, Maria Grassi, Paola |
| AuthorAffiliation | 4 Mologic LTD, Bedford Technology Park, Bedfordshire, United Kingdom 5 Division of Cancer, Department of Surgery and Cancer, Imperial College London, London, United Kingdom 6 Department of Obstetrics, Gynaecology and Women's Health, University of Missouri, Columbia, Missouri, United States of America Universidade de Sao Paulo, BRAZIL 2 Academic Department of Obstetrics and Gynaecology, Chelsea and Westminster Hospital, London, United Kingdom 1 Department of Life Sciences, Imperial College London, London, United Kingdom 3 Tommys' National Centre for Miscarriage Research, Queen Charlottes' & Chelsea Hospital, Imperial College, London, United Kingdom |
| AuthorAffiliation_xml | – name: 3 Tommys' National Centre for Miscarriage Research, Queen Charlottes' & Chelsea Hospital, Imperial College, London, United Kingdom – name: 2 Academic Department of Obstetrics and Gynaecology, Chelsea and Westminster Hospital, London, United Kingdom – name: Universidade de Sao Paulo, BRAZIL – name: 4 Mologic LTD, Bedford Technology Park, Bedfordshire, United Kingdom – name: 1 Department of Life Sciences, Imperial College London, London, United Kingdom – name: 5 Division of Cancer, Department of Surgery and Cancer, Imperial College London, London, United Kingdom – name: 6 Department of Obstetrics, Gynaecology and Women's Health, University of Missouri, Columbia, Missouri, United States of America |
| Author_xml | – sequence: 1 givenname: Linda orcidid: 0000-0002-3570-6674 surname: Ibeto fullname: Ibeto, Linda – sequence: 2 givenname: Aristotelis surname: Antonopoulos fullname: Antonopoulos, Aristotelis – sequence: 3 givenname: Paola surname: Grassi fullname: Grassi, Paola – sequence: 4 givenname: Poh-Choo surname: Pang fullname: Pang, Poh-Choo – sequence: 5 givenname: Maria surname: Panico fullname: Panico, Maria – sequence: 6 givenname: Shabnam surname: Bobdiwala fullname: Bobdiwala, Shabnam – sequence: 7 givenname: Maya surname: Al-Memar fullname: Al-Memar, Maya – sequence: 8 givenname: Paul surname: Davis fullname: Davis, Paul – sequence: 9 givenname: Mark surname: Davis fullname: Davis, Mark – sequence: 10 givenname: Julian surname: Norman Taylor fullname: Norman Taylor, Julian – sequence: 11 givenname: Paula surname: Almeida fullname: Almeida, Paula – sequence: 12 givenname: Mark R. surname: Johnson fullname: Johnson, Mark R. – sequence: 13 givenname: Richard surname: Harvey fullname: Harvey, Richard – sequence: 14 givenname: Tom surname: Bourne fullname: Bourne, Tom – sequence: 15 givenname: Michael surname: Seckl fullname: Seckl, Michael – sequence: 16 givenname: Gary surname: Clark fullname: Clark, Gary – sequence: 17 givenname: Stuart M. surname: Haslam fullname: Haslam, Stuart M. – sequence: 18 givenname: Anne surname: Dell fullname: Dell, Anne |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/32045434$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | COPYRIGHT 2020 Public Library of Science 2020 Ibeto et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2020 Ibeto et al 2020 Ibeto et al |
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| DOI | 10.1371/journal.pone.0228507 |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Competing Interests: Affiliation with Mologic LTD UK I can confirm that this commercial affiliation does not alter our adherence to PLOS ONE policies on sharing data and materials.” (as detailed online in guide for authors http://journals.plos.org/plosone/s/competing-interests). |
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| SubjectTerms | Antigenic determinants Antigens Biological activity Biology and Life Sciences Biomarkers Cancer Carbohydrate Sequence Chorionic gonadotropin Chorionic Gonadotropin, beta Subunit, Human - blood Chorionic Gonadotropin, beta Subunit, Human - metabolism Chorionic Gonadotropin, beta Subunit, Human - urine Chorionic gonadotropins Comparative analysis Cytotoxicity Diagnostic systems Diseases Embryo Embryos Epitopes Female Female identity Gestation Gestational Age Gestational Trophoblastic Disease - blood Gestational Trophoblastic Disease - metabolism Gestational Trophoblastic Disease - urine Glycan Glycomics - methods Glycoproteins Glycosylation Gonadotropins Gynecology Health aspects Hormones Humans Identity Implantation Killer cells Life sciences Mass spectrometry Mass spectroscopy Medicine and Health Sciences Miscarriage N-glycans Natural killer cells Novels Obstetrics Physical Sciences Pituitary (anterior) Pituitary hormones Placental hormones Polysaccharides Polysaccharides - metabolism Preeclampsia Pregnancy Pregnant women Protein Processing, Post-Translational Research and Analysis Methods Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization Spectroscopy Tandem Mass Spectrometry Time Toxicity Trophoblastic disease Tumors Urine Womens health |
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| Title | Insights into the hyperglycosylation of human chorionic gonadotropin revealed by glycomics analysis |
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