Glutamic acid decarboxylase antibody-spectrum disorders and type 1 diabetes mellitus in a patient following allogenic hematopoietic cell transplantation with review of literature
Glutamic acid decarboxylase (GAD) is an enzyme that catalyzes the conversion of glutamic acid into γ-aminobutyric acid (GABA), the primary inhibitory neurotransmitter in the central nervous system (CNS). GAD is widely expressed in the CNS and pancreatic β-cells. GABA produced by GAD plays a role in...
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| Published in | Endocrine Journal Vol. 72; no. 3; pp. 333 - 340 |
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| Main Authors | , , , , , , , |
| Format | Journal Article |
| Language | English |
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The Japan Endocrine Society
01.01.2025
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| Abstract | Glutamic acid decarboxylase (GAD) is an enzyme that catalyzes the conversion of glutamic acid into γ-aminobutyric acid (GABA), the primary inhibitory neurotransmitter in the central nervous system (CNS). GAD is widely expressed in the CNS and pancreatic β-cells. GABA produced by GAD plays a role in regulating insulin secretion in pancreatic islets. Anti-GAD antibody is an established marker of type 1 diabetes mellitus (T1DM) and is also associated with stiff-person syndrome (SPS) and several other neurological disorders, including ataxia, cognitive impairment, limbic encephalitis, and epilepsy, collectively referred to as GAD antibody-spectrum disorders (GAD-SD). We report the case of a 17-year-old male patient who developed GAD-SD and T1DM after allogeneic hematopoietic cell transplantation (HCT). He presented with memory disorders, including feelings of déjà vu, accompanied by vomiting and headaches, and exhibited abnormal brain magnetic resonance imaging and electroencephalogram results. In addition to elevated fasting plasma glucose and glycated hemoglobin levels, markedly elevated anti-GAD antibody levels were detected in the serum and cerebrospinal fluid. Based on these findings, the patient was diagnosed with GAD-SD and T1DM and treated with methylprednisolone, followed by multiple daily insulin injections. We also reviewed previously reported cases of GAD-SD following HCT and multiple positive islet-related antibodies. |
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| AbstractList | Glutamic acid decarboxylase (GAD) is an enzyme that catalyzes the conversion of glutamic acid into γ-aminobutyric acid (GABA), the primary inhibitory neurotransmitter in the central nervous system (CNS). GAD is widely expressed in the CNS and pancreatic β-cells. GABA produced by GAD plays a role in regulating insulin secretion in pancreatic islets. Anti-GAD antibody is an established marker of type 1 diabetes mellitus (T1DM) and is also associated with stiff-person syndrome (SPS) and several other neurological disorders, including ataxia, cognitive impairment, limbic encephalitis, and epilepsy, collectively referred to as GAD antibody-spectrum disorders (GAD-SD). We report the case of a 17-year-old male patient who developed GAD-SD and T1DM after allogeneic hematopoietic cell transplantation (HCT). He presented with memory disorders, including feelings of déjà vu, accompanied by vomiting and headaches, and exhibited abnormal brain magnetic resonance imaging and electroencephalogram results. In addition to elevated fasting plasma glucose and glycated hemoglobin levels, markedly elevated anti-GAD antibody levels were detected in the serum and cerebrospinal fluid. Based on these findings, the patient was diagnosed with GAD-SD and T1DM and treated with methylprednisolone, followed by multiple daily insulin injections. We also reviewed previously reported cases of GAD-SD following HCT and multiple positive islet-related antibodies. Glutamic acid decarboxylase (GAD) is an enzyme that catalyzes the conversion of glutamic acid into γ-aminobutyric acid (GABA), the primary inhibitory neurotransmitter in the central nervous system (CNS). GAD is widely expressed in the CNS and pancreatic β-cells. GABA produced by GAD plays a role in regulating insulin secretion in pancreatic islets. Anti-GAD antibody is an established marker of type 1 diabetes mellitus (T1DM) and is also associated with stiff-person syndrome (SPS) and several other neurological disorders, including ataxia, cognitive impairment, limbic encephalitis, and epilepsy, collectively referred to as GAD antibody-spectrum disorders (GAD-SD). We report the case of a 17-year-old male patient who developed GAD-SD and T1DM after allogeneic hematopoietic cell transplantation (HCT). He presented with memory disorders, including feelings of déjà vu, accompanied by vomiting and headaches, and exhibited abnormal brain magnetic resonance imaging and electroencephalogram results. In addition to elevated fasting plasma glucose and glycated hemoglobin levels, markedly elevated anti-GAD antibody levels were detected in the serum and cerebrospinal fluid. Based on these findings, the patient was diagnosed with GAD-SD and T1DM and treated with methylprednisolone, followed by multiple daily insulin injections. We also reviewed previously reported cases of GAD-SD following HCT and multiple positive islet-related antibodies.Glutamic acid decarboxylase (GAD) is an enzyme that catalyzes the conversion of glutamic acid into γ-aminobutyric acid (GABA), the primary inhibitory neurotransmitter in the central nervous system (CNS). GAD is widely expressed in the CNS and pancreatic β-cells. GABA produced by GAD plays a role in regulating insulin secretion in pancreatic islets. Anti-GAD antibody is an established marker of type 1 diabetes mellitus (T1DM) and is also associated with stiff-person syndrome (SPS) and several other neurological disorders, including ataxia, cognitive impairment, limbic encephalitis, and epilepsy, collectively referred to as GAD antibody-spectrum disorders (GAD-SD). We report the case of a 17-year-old male patient who developed GAD-SD and T1DM after allogeneic hematopoietic cell transplantation (HCT). He presented with memory disorders, including feelings of déjà vu, accompanied by vomiting and headaches, and exhibited abnormal brain magnetic resonance imaging and electroencephalogram results. In addition to elevated fasting plasma glucose and glycated hemoglobin levels, markedly elevated anti-GAD antibody levels were detected in the serum and cerebrospinal fluid. Based on these findings, the patient was diagnosed with GAD-SD and T1DM and treated with methylprednisolone, followed by multiple daily insulin injections. We also reviewed previously reported cases of GAD-SD following HCT and multiple positive islet-related antibodies. |
| ArticleNumber | EJ24-0457 |
| Author | Watanabe, Kenichiro Fujisawa, Yasuko Takachi, Takayuki Murai, Yuki Yoshimura, Masaki Ogura, Taemi Sano, Shinichiro Ogata, Tsutomu |
| Author_xml | – sequence: 1 orcidid: 0000-0001-7178-9991 fullname: Sano, Shinichiro organization: Department of Diabetes and Metabolism, Shizuoka Children’s Hospital, Shizuoka 420-8660, Japan – sequence: 2 orcidid: 0000-0001-7178-9991 fullname: Ogura, Taemi organization: Department of Hematology and Oncology, Shizuoka Children’s Hospital, Shizuoka 420-8660, Japan – sequence: 3 orcidid: 0000-0001-7178-9991 fullname: Takachi, Takayuki organization: Department of Hematology and Oncology, Shizuoka Children’s Hospital, Shizuoka 420-8660, Japan – sequence: 4 orcidid: 0000-0001-7178-9991 fullname: Murai, Yuki organization: Department of Diabetes and Metabolism, Shizuoka Children’s Hospital, Shizuoka 420-8660, Japan – sequence: 5 orcidid: 0000-0001-7178-9991 fullname: Fujisawa, Yasuko organization: Department of Pediatrics, Hamamatsu University School of Medicine, Hamamatsu 431-3192, Japan – sequence: 6 orcidid: 0000-0001-7178-9991 fullname: Ogata, Tsutomu organization: Department of Pediatrics, Hamamatsu University School of Medicine, Hamamatsu 431-3192, Japan – sequence: 7 fullname: Watanabe, Kenichiro organization: Department of Hematology and Oncology, Shizuoka Children’s Hospital, Shizuoka 420-8660, Japan – sequence: 8 fullname: Yoshimura, Masaki organization: Department of Epilepsy, National Epilepsy Center, Shizuoka Institute of Epilepsy and Neurological Disorders, Shizuoka 420-8688, Japan |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/39631871$$D View this record in MEDLINE/PubMed |
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| Keywords | Glutamic acid decarboxylase antibody-spectrum disorder Hematopoietic cell transplantation Anti-glutamic acid decarboxylase antibody Type 1 diabetes mellitus |
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(1988) Autoantibodies to glutamic acid decarboxylase in a patient with stiff-man syndrome, epilepsy, and type I diabetes mellitus. N Engl J Med 318: 1012–1020. 24 Clow EC, Couban S, Grant IA (2008) Stiff-person syndrome associated with multiple myeloma following autologous bone marrow transplantation. Muscle Nerve 38: 1649–1652. 32 Martino G, Grimaldi LM, Bazzigaluppi E, Passini N, Sinigaglia F, et al. (1996) The insulin-dependent diabetes mellitus-associated ICA 105 autoantigen in stiff-man syndrome patients. J Neuroimmunol 69: 129–134. 5 Dalakas MC (2022) Stiff-person Syndrome and GAD Antibody-spectrum disorders: GABAergic neuronal excitability, immunopathogenesis and update on antibody therapies. Neurotherapeutics 19: 832–847. 17 Graus F, Saiz A, Dalmau J (2020) GAD antibodies in neurological disorders - insights and challenges. Nat Rev Neurol 16: 353–365. 25 Shargian-Alon L, Raanani P, Rozovski U, Siegal T, Yust-Katz S, et al. (2019) Immune mediated cerebellar ataxia: an unknown manifestation of graft-versus-host disease. Acta Haematol 141: 19–22. 1 Gagnon MM, Savard M (2016) Limbic encephalitis associated with GAD65 antibodies: brief review of the relevant literature. Can J Neurol Sci 43: 486–493. 6 Bai L, Ren H, Liang M, Lu Q, Lin N, et al. (2022) Neurological disorders associated with glutamic acid decarboxylase 65 antibodies: Clinical spectrum and prognosis of a cohort from China. Front Neurol 13: 990553. 2 Wendt A, Birnir B, Buschard K, Gromada J, Salehi A, et al. (2004) Glucose inhibition of glucagon secretion from rat alpha-cells is mediated by GABA released from neighboring beta-cells. Diabetes 53: 1038–1045. 10 Gabriel M, Hoeben BAW, Uhlving HH, Zajac-Spychala O, Lawitschka A, et al. (2021) A review of acute and long-term neurological complications following haematopoietic stem cell transplant for paediatric acute lymphoblastic leukaemia. Front Pediatr 9: 774853. 33 Christie MR, Genovese S, Cassidy D, Bosi E, Brown TJ, et al. (1994) Antibodies to islet 37k antigen, but not to glutamate decarboxylase, discriminate rapid progression to IDDM in endocrine autoimmunity. Diabetes 43: 1254–1259. 7 Heneberg P (2023) Diabetes in stiff-person syndrome. Trends Endocrinol Metab 34: 640–651. 8 Majhail NS, Chitphakdithai P, Logan B, King R, Devine S, et al. (2015) Significant improvement in survival after unrelated donor hematopoietic cell transplantation in the recent era. Biol Blood Marrow Transplant 21: 142–150. 27 Sequeira M, Lobo GG, Ferro M, Capela C (2024) Relapsing remitting encephalomyelitis with glutamic acid decarboxylase antibodies following autologous haematopoietic stem cell transplantation-coincidence or consequence? Neurol Sci 45: 813–815. 28 Rathore GS, Leung KS, Muscal E (2015) Autoimmune encephalitis following bone marrow transplantation. Pediatr Neurol 53: 253–256. 20 Yamamura S, Fukui T, Mori Y, Hayashi T, Yamamoto T, et al. (2019) Circulating anti-glutamic acid decarboxylase-65 antibody titers are positively associated with the capacity of insulin secretion in acute-onset type 1 diabetes with short duration in a Japanese population. J Diabetes Investig 10: 1480–1489. 12 Tsiortou P, Alexopoulos H, Dalakas MC (2021) GAD antibody-spectrum disorders: progress in clinical phenotypes, immunopathogenesis and therapeutic interventions. Ther Adv Neurol Disord 14: 17562864211003486. 18 Teshima T, Boelens JJ, Matsuoka KI (2023) Novel insights into GVHD and immune reconstitution after allogeneic hematopoietic cell transplantation. Blood Cell Ther 6: 42–48. 15 Madlener M, Strippel C, Thaler FS, Doppler K, Wandinger KP, et al. (2023) Glutamic acid decarboxylase antibody-associated neurological syndromes: clinical and antibody characteristics and therapy response. J Neurol Sci 445: 120540. 16 Muñoz-Lopetegi A, de Bruijn M, Boukhrissi S, Bastiaansen AEM, Nagtzaam MMP, et al. (2020) Neurologic syndromes related to anti-GAD65: clinical and serologic response to treatment. Neurol Neuroimmunol Neuroinflamm 7: e696. 14 Hümmert MW, Stadler M, Hambach L, Gingele S, Bredt M, et al. (2021) Severe allo-immune antibody-associated peripheral and central nervous system diseases after allogeneic hematopoietic stem cell transplantation. Sci Rep 11: 8527. 9 Hahn T, McCarthy PL Jr, Hassebroek A, Bredeson C, Gajewski JL, et al. (2013) Significant improvement in survival after allogeneic hematopoietic cell transplantation during a period of significantly increased use, older recipient age, and use of unrelated donors. J Clin Oncol 31: 2437–2449. 23 Björk E, Velloso LA, Kämpe O, Karlsson FA (1994) GAD autoantibodies in IDDM, stiff-man syndrome, and autoimmune polyendocrine syndrome type I recognize different epitopes. Diabetes 43: 161–165. 13 Disserol CCD, Kowacs DP, Nabhan SK, Teive HAG, Kowacs PA (2023) Case report: successful autologous hematopoietic stem cell transplantation in a patient with GAD antibody-spectrum disorder with rapidly progressive dementia. Front Neurol 14: 1254981. 22 Daw K, Ujihara N, Atkinson M, Powers AC (1996) Glutamic acid decarboxylase autoantibodies in stiff-man syndrome and insulin-dependent diabetes mellitus exhibit similarities and differences in epitope recognition. J Immunol 156: 818–825. 30 McKeon A, Robinson MT, McEvoy KM, Matsumoto JY, Lennon VA, et al. (2012) Stiff-man syndrome and variants: clinical course, treatments, and outcomes. Arch Neurol 69: 230–238. 11 Dalakas MC, Li M, Fujii M, Jacobowitz DM (2001) Stiff person syndrome: quantification, specificity, and intrathecal synthesis of GAD65 antibodies. Neurology 57: 780–784. 29 Lee YY, Chen IW, Chen ST, Wang CC (2019) Association of stiff-person syndrome with autoimmune endocrine diseases. World J Clin Cases 7: 2942–2952. 22 23 24 25 26 27 28 29 30 31 10 32 11 33 12 13 14 15 16 17 18 19 1 2 3 4 5 6 7 8 9 20 21 |
| References_xml | – reference: 28 Rathore GS, Leung KS, Muscal E (2015) Autoimmune encephalitis following bone marrow transplantation. Pediatr Neurol 53: 253–256. – reference: 7 Heneberg P (2023) Diabetes in stiff-person syndrome. Trends Endocrinol Metab 34: 640–651. – reference: 3 Kawasaki E (2014) Type 1 diabetes and autoimmunity. Clin Pediatr Endocrinol 23: 99–105. – reference: 13 Disserol CCD, Kowacs DP, Nabhan SK, Teive HAG, Kowacs PA (2023) Case report: successful autologous hematopoietic stem cell transplantation in a patient with GAD antibody-spectrum disorder with rapidly progressive dementia. Front Neurol 14: 1254981. – reference: 27 Sequeira M, Lobo GG, Ferro M, Capela C (2024) Relapsing remitting encephalomyelitis with glutamic acid decarboxylase antibodies following autologous haematopoietic stem cell transplantation-coincidence or consequence? Neurol Sci 45: 813–815. – reference: 30 McKeon A, Robinson MT, McEvoy KM, Matsumoto JY, Lennon VA, et al. (2012) Stiff-man syndrome and variants: clinical course, treatments, and outcomes. Arch Neurol 69: 230–238. – reference: 22 Daw K, Ujihara N, Atkinson M, Powers AC (1996) Glutamic acid decarboxylase autoantibodies in stiff-man syndrome and insulin-dependent diabetes mellitus exhibit similarities and differences in epitope recognition. J Immunol 156: 818–825. – reference: 25 Shargian-Alon L, Raanani P, Rozovski U, Siegal T, Yust-Katz S, et al. (2019) Immune mediated cerebellar ataxia: an unknown manifestation of graft-versus-host disease. Acta Haematol 141: 19–22. – reference: 11 Dalakas MC, Li M, Fujii M, Jacobowitz DM (2001) Stiff person syndrome: quantification, specificity, and intrathecal synthesis of GAD65 antibodies. Neurology 57: 780–784. – reference: 5 Dalakas MC (2022) Stiff-person Syndrome and GAD Antibody-spectrum disorders: GABAergic neuronal excitability, immunopathogenesis and update on antibody therapies. Neurotherapeutics 19: 832–847. – reference: 16 Muñoz-Lopetegi A, de Bruijn M, Boukhrissi S, Bastiaansen AEM, Nagtzaam MMP, et al. (2020) Neurologic syndromes related to anti-GAD65: clinical and serologic response to treatment. Neurol Neuroimmunol Neuroinflamm 7: e696. – reference: 4 Solimena M, Folli F, Denis-Donini S, Comi GC, Pozza G, et al. (1988) Autoantibodies to glutamic acid decarboxylase in a patient with stiff-man syndrome, epilepsy, and type I diabetes mellitus. N Engl J Med 318: 1012–1020. – reference: 32 Martino G, Grimaldi LM, Bazzigaluppi E, Passini N, Sinigaglia F, et al. (1996) The insulin-dependent diabetes mellitus-associated ICA 105 autoantigen in stiff-man syndrome patients. J Neuroimmunol 69: 129–134. – reference: 1 Gagnon MM, Savard M (2016) Limbic encephalitis associated with GAD65 antibodies: brief review of the relevant literature. 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(1994) Antibodies to islet 37k antigen, but not to glutamate decarboxylase, discriminate rapid progression to IDDM in endocrine autoimmunity. Diabetes 43: 1254–1259. – reference: 2 Wendt A, Birnir B, Buschard K, Gromada J, Salehi A, et al. (2004) Glucose inhibition of glucagon secretion from rat alpha-cells is mediated by GABA released from neighboring beta-cells. Diabetes 53: 1038–1045. – reference: 24 Clow EC, Couban S, Grant IA (2008) Stiff-person syndrome associated with multiple myeloma following autologous bone marrow transplantation. Muscle Nerve 38: 1649–1652. – reference: 15 Madlener M, Strippel C, Thaler FS, Doppler K, Wandinger KP, et al. (2023) Glutamic acid decarboxylase antibody-associated neurological syndromes: clinical and antibody characteristics and therapy response. J Neurol Sci 445: 120540. – reference: 18 Teshima T, Boelens JJ, Matsuoka KI (2023) Novel insights into GVHD and immune reconstitution after allogeneic hematopoietic cell transplantation. 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| Title | Glutamic acid decarboxylase antibody-spectrum disorders and type 1 diabetes mellitus in a patient following allogenic hematopoietic cell transplantation with review of literature |
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