Current and future treatment approaches for Barth syndrome.
Acyltransferases
/ genetics
Animals
Barth Syndrome
/ genetics
Bezafibrate
/ therapeutic use
Cardiolipins
/ metabolism
Cardiomyopathies
/ metabolism
Clinical Trials as Topic
Enzyme Therapy
Genetic Therapy
Humans
Mice
Muscular Diseases
/ metabolism
Neutropenia
/ metabolism
Oligopeptides
/ therapeutic use
Peroxisome Proliferator-Activated Receptors
/ agonists
Barth syndrome
TAFAZZIN
cardiolipin
cardiomyopathy
Journal
Journal of inherited metabolic disease
ISSN: 1573-2665
Titre abrégé: J Inherit Metab Dis
Pays: United States
ID NLM: 7910918
Informations de publication
Date de publication:
01 2022
01 2022
Historique:
revised:
18
10
2021
received:
21
07
2021
accepted:
26
10
2021
pubmed:
30
10
2021
medline:
8
2
2022
entrez:
29
10
2021
Statut:
ppublish
Résumé
Barth Syndrome is an X-linked disorder of mitochondrial cardiolipin metabolism caused by pathogenic variants in TAFAZZIN with pleiotropic effects including cardiomyopathy, neutropenia, growth delay, and skeletal myopathy. Management requires a multidisciplinary approach to the organ-specific manifestations including specialists from cardiology, hematology, nutrition, physical therapy, genetics, and metabolism. Currently, treatment is centered on management of specific clinical features, and is not targeted toward remediating the underlying biochemical defect. However, two clinical trials have been recently undertaken which target the mitochondrial pathology of this disease: a study to examine the effects of elamipretide, a cardiolipin targeted agent, and a study to examine the effects of bezafibrate, a peroxisome proliferator-activated receptor (PPAR) agonist. Treatments to directly target the defective TAFAZZIN pathway are under development, including enzyme and gene therapies.
Substances chimiques
Cardiolipins
0
Oligopeptides
0
Peroxisome Proliferator-Activated Receptors
0
arginyl-2,'6'-dimethyltyrosyl-lysyl-phenylalaninamide
0
Acyltransferases
EC 2.3.-
TAFAZZIN protein, human
EC 2.3.1.-
Bezafibrate
Y9449Q51XH
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
17-28Informations de copyright
© 2021 SSIEM.
Références
Miller PC, Ren M, Schlame M, Toth MJ, Phoon CKL. A Bayesian analysis to determine the prevalence of Barth syndrome in the pediatric population. J Pediatr. 2020;217:139-144.
Barth PG, Scholte HR, Berden JA, et al. An X-linked mitochondrial disease affecting cardiac muscle, skeletal muscle and neutrophil leucocytes. J Neurol Sci. 1983;62:327-355.
Vreken P, Valianpour F, Nijtmans LG, et al. Defective remodeling of cardiolipin and phosphatidylglycerol in Barth syndrome. Biochem Biophys Res Commun. 2000;279:378-382.
Dudek J. Role of cardiolipin in mitochondrial signaling pathways. Front Cell Dev Biol. 2017;5:90.
Pfeiffer K, Gohil V, Stuart RA, et al. Cardiolipin stabilizes respiratory chain supercomplexes. J Biol Chem. 2003;278:52873-52880.
Chicco AJ, Sparagna GC. Role of cardiolipin alterations in mitochondrial dysfunction and disease. Am J Physiol Cell Physiol. 2007;292:C33-C44.
Paradies G, Paradies V, Ruggiero FM, Petrosillo G. Role of cardiolipin in mitochondrial function and dynamics in health and disease: molecular and pharmacological aspects. Cell. 2019;8:1-21.
Falabella M, Vernon HJ, Hanna MG, Claypool SM, Pitceathly RDS. Cardiolipin, mitochondria, and neurological disease. Trends Endocrinol Metab. 2021;32:224-237.
Xu Y, Malhotra A, Ren M, Schlame M. The enzymatic function of tafazzin. J Biol Chem. 2006;281:39217-39224.
Thompson WR, DeCroes B, McClellan R, et al. New targets for monitoring and therapy in Barth syndrome. Genet Med. 2016;18:1001-1010.
Houtkooper RH, Rodenburg RJ, Thiels C, et al. Cardiolipin and monolysocardiolipin analysis in fibroblasts, lymphocytes, and tissues using high-performance liquid chromatography-mass spectrometry as a diagnostic test for Barth syndrome. Anal Biochem. 2009;387:230-237.
McKenzie M, Lazarou M, Thorburn DR, Ryan MT. Mitochondrial respiratory chain supercomplexes are destabilized in Barth syndrome patients. J Mol Biol. 2006;361:462-469.
Liu X, Wang S, Guo X, et al. Increased reactive oxygen species-mediated Ca(2+)/calmodulin-dependent protein kinase II activation contributes to calcium handling abnormalities and impaired contraction in Barth syndrome. Circulation. 2021;143:1894-1911.
Le CH, Benage LG, Specht KS, et al. Tafazzin deficiency impairs CoA-dependent oxidative metabolism in cardiac mitochondria. J Biol Chem. 2020;295:12485-12497.
Raja V, Salsaa M, Joshi AS, et al. Cardiolipin-deficient cells depend on anaplerotic pathways to ameliorate defective TCA cycle function. Biochim Biophys Acta Mol Cell Biol Lipids. 2019;1864:654-661.
Ghosh S, Iadarola DM, Ball WB, Gohil VM. Mitochondrial dysfunctions in Barth syndrome. IUBMB Life. 2019;71:791-801.
Oemer G, Lackner K, Muigg K, et al. Molecular structural diversity of mitochondrial cardiolipins. Proc Natl Acad Sci U S A. 2018;115:4158-4163.
Oemer G, Koch J, Wohlfarter Y, et al. Phospholipid acyl chain diversity controls the tissue-specific assembly of mitochondrial cardiolipins. Cell Rep. 2020;30:4281-4291.
Orstavik KH, Orstavik RE, Naumova AK, et al. X chromosome inactivation in carriers of Barth syndrome. Am J Hum Genet. 1998;63:1457-1463.
Cosson L, Toutain A, Simard G, et al. Barth syndrome in a female patient. Mol Genet Metab. 2012;106:115-120.
Avdjieva-Tzavella DM, Todorova AP, Kathom HM, et al. Barth syndrome in male and female siblings caused by a novel mutation in the Taz gene. Genet Couns. 2016;27:495-501.
Roberts AE, Nixon C, Steward CG, et al. The Barth syndrome registry: distinguishing disease characteristics and growth data from a longitudinal study. Am J Med Genet A. 2012;158A:2726-2732.
Rigaud C, Lebre AS, Touraine R, et al. Natural history of Barth syndrome: a national cohort study of 22 patients. Orphanet J Rare Dis. 2013;8:70.
Kang SL, Forsey J, Dudley D, Steward CG, Tsai-Goodman B. Clinical characteristics and outcomes of cardiomyopathy in Barth syndrome: The UK experience. Pediatr Cardiol. 2016;37:167-176.
Ferreira C, Thompson R, Vernon H. Barth syndrome. In: Adam MP, Ardinger HH, Pagon RA, et al., eds. GeneReviews(R). Seattle, WA: University of Washington; 1993.
Spencer CT, Bryant RM, Day J, et al. Cardiac and clinical phenotype in Barth syndrome. Pediatrics. 2006;118:e337-e346.
Steward CG, Newbury-Ecob RA, Hastings R, et al. Barth syndrome: an X-linked cause of fetal cardiomyopathy and stillbirth. Prenat Diagn. 2010;30:970-976.
Marwick TH, Shah SJ, Thomas JD. Myocardial strain in the assessment of patients with heart failure: a review. JAMA Cardiol. 2019;4:287-294.
Pennell DJ, Baksi AJ, Prasad SK, et al. Review of journal of cardiovascular magnetic resonance 2015. J Cardiovasc Magn Reson. 2016;18:86.
Kantor PF, Lougheed J, Dancea A, et al. Presentation, diagnosis, and medical management of heart failure in children: Canadian cardiovascular society guidelines. Can J Cardiol. 2013;29:1535-1552.
Writing Committee M, Ommen SR, Mital S, et al. 2020 AHA/ACC guideline for the diagnosis and treatment of patients with hypertrophic cardiomyopathy: a report of the American College of Cardiology/American Heart Association Joint Committee on Clinical Practice Guidelines. J Thorac Cardiovasc Surg. 2021;162:e23-e106.
Jefferies JL, Wilkinson JD, Sleeper LA, et al. Cardiomyopathy phenotypes and outcomes for children with left ventricular myocardial noncompaction: results from the Pediatric Cardiomyopathy Registry. J Card Fail. 2015;21:877-884.
Reid Thompson W, Hornby B, Manuel R, et al. A phase 2/3 randomized clinical trial followed by an open-label extension to evaluate the effectiveness of elamipretide in Barth syndrome, a genetic disorder of mitochondrial cardiolipin metabolism. Genet Med. 2021;23:471-478.
Spencer CT, Byrne BJ, Gewitz MH, et al. Ventricular arrhythmia in the X-linked cardiomyopathy Barth syndrome. Pediatr Cardiol. 2005;26:632-637.
Bisignani A, De Bonis S, Mancuso L, Ceravolo G, Bisignani G. Implantable loop recorder in clinical practice. J Arrhythm. 2019;35:25-32.
Reynolds S, Kreider CM, Bendixen R. A mixed-methods investigation of sensory response patterns in Barth syndrome: a clinical phenotype? Am J Med Genet A. 2012;158A:1647-1653.
Yen TY, Hwu WL, Chien YH, et al. Acute metabolic decompensation and sudden death in Barth syndrome: report of a family and a literature review. Eur J Pediatr. 2008;167:941-944.
Donati MA, Malvagia S, Pasquini E, et al. Barth syndrome presenting with acute metabolic decompensation in the neonatal period. J Inherit Metab Dis. 2006;29:684.
Mejia EM, Zinko JC, Hauff KD, Xu FY, Ravandi A, Hatch GM. Glucose uptake and triacylglycerol synthesis are increased in Barth syndrome lymphoblasts. Lipids. 2017;52:161-165.
Cade WT, Spencer CT, Reeds DN, et al. Substrate metabolism during basal and hyperinsulinemic conditions in adolescents and young-adults with Barth syndrome. J Inherit Metab Dis. 2013;36:91-101.
Cade WT, Laforest R, Bohnert KL, et al. Myocardial glucose and fatty acid metabolism is altered and associated with lower cardiac function in young adults with Barth syndrome. J Nucl Cardiol. 2019;28:1649-1659.
Steward CG, Groves SJ, Taylor CT, et al. Neutropenia in Barth syndrome: characteristics, risks, and management. Curr Opin Hematol. 2019;26:6-15.
Finsterer J, Frank M. Haematological features in Barth syndrome. Curr Opin Hematol. 2013;20:36-40.
Dale DC, Bonilla MA, Davis MW, et al. A randomized controlled phase III trial of recombinant human granulocyte colony-stimulating factor (filgrastim) for treatment of severe chronic neutropenia. Blood. 1993;81:2496-2502.
Freedman MH, Bonilla MA, Fier C, et al. Myelodysplasia syndrome and acute myeloid leukemia in patients with congenital neutropenia receiving G-CSF therapy. Blood. 2000;96:429-436.
Li AM, Thyagu S, Maze D, et al. Prolonged granulocyte colony stimulating factor use in glycogen storage disease type 1b associated with acute myeloid leukemia and with shortened telomere length. Pediatr Hematol Oncol. 2018;35:45-51.
Hornby B, McClellan R, Buckley L, Carson K, Gooding T, Vernon HJ. Functional exercise capacity, strength, balance and motion reaction time in Barth syndrome. Orphanet J Rare Dis. 2019;14:37.
Spencer CT, Byrne BJ, Bryant RM, et al. Impaired cardiac reserve and severely diminished skeletal muscle O(2) utilization mediate exercise intolerance in Barth syndrome. Am J Physiol Heart Circ Physiol. 2011;301:H2122-H2129.
Cade WT, Reeds DN, Peterson LR, et al. Endurance exercise training in young adults with Barth syndrome: a pilot study. JIMD Rep. 2017;32:15-24.
Raches D, Mazzocco MM. Emergence and nature of mathematical difficulties in young children with Barth syndrome. J Dev Behav Pediatr. 2012;33:328-335.
Mazzocco MM, Kelley RI. Preliminary evidence for a cognitive phenotype in Barth syndrome. Am J Med Genet. 2001;102:372-378.
Mazzocco MM, Henry AE, Kelly RI. Barth syndrome is associated with a cognitive phenotype. J Dev Behav Pediatr. 2007;28:22-30.
Olivar-Villanueva M, Ren M, Phoon CKL. Neurological and psychological aspects of Barth syndrome: understanding their role and potential impact on quality of life. Mitochondrion. 2021. In Press.
Brady AN, Shehata BM, Fernhoff PM. X-linked fetal cardiomyopathy caused by a novel mutation in the TAZ gene. Prenat Diagn. 2006;26:462-465.
Vernon HJ, Sandlers Y, McClellan R, Kelley RI. Clinical laboratory studies in Barth syndrome. Mol Genet Metab. 2014;112:143-147.
Huhta JC, Pomerance HH, Barness EG. Clinicopathologic conference: Barth syndrome. Fetal Pediatr Pathol. 2005;24:239-254.
Tyagi S, Gupta P, Saini AS, Kaushal C, Sharma S. The peroxisome proliferator-activated receptor: a family of nuclear receptors role in various diseases. J Adv Pharm Technol Res. 2011;2:236-240.
Steele H, Gomez-Duran A, Pyle A, et al. Metabolic effects of bezafibrate in mitochondrial disease. EMBO Mol Med. 2020;12:e11589.
Orngreen MC, Madsen KL, Preisler N, Andersen G, Vissing J, Laforet P. Bezafibrate in skeletal muscle fatty acid oxidation disorders: a randomized clinical trial. Neurology. 2014;82:607-613.
Bonnefont JP, Bastin J, Laforet P, et al. Long-term follow-up of bezafibrate treatment in patients with the myopathic form of carnitine palmitoyltransferase 2 deficiency. Clin Pharmacol Ther. 2010;88:101-108.
Huang Y, Powers C, Moore V, et al. The PPAR pan-agonist bezafibrate ameliorates cardiomyopathy in a mouse model of Barth syndrome. Orphanet J Rare Dis. 2017;12:49.
Zegallai HM, Hatch GM. Barth syndrome: cardiolipin, cellular pathophysiology, management, and novel therapeutic targets. Mol Cell Biochem. 2021;476:1605-1629.
Dabner L, Pieles GE, Steward CG, et al. Treatment of Barth syndrome by cardiolipin manipulation (CARDIOMAN) with bezafibrate: protocol for a randomized placebo-controlled pilot trial conducted in the nationally commissioned Barth syndrome service. JMIR Res Protoc. 2021;10:e22533.
Allen ME, Pennington ER, Perry JB, et al. The cardiolipin-binding peptide elamipretide mitigates fragmentation of cristae networks following cardiac ischemia reperfusion in rats. Commun Biol. 2020;3:389.
Birk AV, Liu S, Soong Y, et al. The mitochondrial-targeted compound SS-31 re-energizes ischemic mitochondria by interacting with cardiolipin. J Am Soc Nephrol. 2013;24:1250-1261.
Birk AV, Chao WM, Bracken C, Warren JD, Szeto HH. Targeting mitochondrial cardiolipin and the cytochrome c/cardiolipin complex to promote electron transport and optimize mitochondrial ATP synthesis. Br J Pharmacol. 2014;171:2017-2028.
Ivanov AV, Bartosch B, Isaguliants MG. Oxidative stress in infection and consequent disease. Oxid Med Cell Longev. 2017;2017:3496043.
Wang D, Tai PWL, Gao G. Adeno-associated virus vector as a platform for gene therapy delivery. Nat Rev Drug Discov. 2019;18:358-378.
Mendell JR, Al-Zaidy S, Shell R, et al. Single-dose gene-replacement therapy for spinal muscular atrophy. N Engl J Med. 2017;377:1713-1722.
Maguire AM, Simonelli F, Pierce EA, et al. Safety and efficacy of gene transfer for Leber's congenital amaurosis. N Engl J Med. 2008;358:2240-2248.
Hastie E, Samulski RJ. Adeno-associated virus at 50: a golden anniversary of discovery, research, and gene therapy success: a personal perspective. Hum Gene Ther. 2015;26:257-265.
Wang PR, Xu M, Toffanin S, Li Y, Llovet JM, Russell DW. Induction of hepatocellular carcinoma by in vivo gene targeting. Proc Natl Acad Sci U S A. 2012;109:11264-11269.
Vandamme C, Adjali O, Mingozzi F. Unraveling the complex story of immune responses to AAV vectors trial after trial. Hum Gene Ther. 2017;28:1061-1074.
Hinderer C, Katz N, Buza EL, et al. Severe toxicity in nonhuman primates and piglets following high-dose intravenous administration of an adeno-associated virus vector expressing human SMN. Hum Gene Ther. 2018;29:285-298.
McCarty DM. Self-complementary AAV vectors; advances and applications. Mol Ther. 2008;16:1648-1656.
Wang S, Li Y, Xu Y, et al. AAV gene therapy prevents and reverses heart failure in a murine knockout model of Barth syndrome. Circ Res. 2020;126:1024-1039.
Wang G, McCain ML, Yang L, et al. Modeling the mitochondrial cardiomyopathy of Barth syndrome with induced pluripotent stem cell and heart-on-chip technologies. Nat Med. 2014;20:616-623.
Zincarelli C, Soltys S, Rengo G, Rabinowitz JE. Analysis of AAV serotypes 1-9 mediated gene expression and tropism in mice after systemic injection. Mol Ther. 2008;16:1073-1080.
Suzuki-Hatano S, Saha M, Rizzo SA, et al. AAV-mediated TAZ gene replacement restores mitochondrial and cardioskeletal function in Barth syndrome. Hum Gene Ther. 2019;30:139-154.
Ronzitti G, Gross DA, Mingozzi F. Human immune responses to adeno-associated virus (AAV) vectors. Front Immunol. 2020;11:670.
Wilson JM, Flotte TR. Moving forward after two deaths in a gene therapy trial of myotubular myopathy. Hum Gene Ther. 2020;31:695-696.
Leborgne C, Barbon E, Alexander JM, et al. IgG-cleaving endopeptidase enables in vivo gene therapy in the presence of anti-AAV neutralizing antibodies. Nat Med. 2020;26:1096-1101.
Elmore ZC, Oh DK, Simon KE, Fanous MM, Asokan A. Rescuing AAV gene transfer from neutralizing antibodies with an IgG-degrading enzyme. JCI Insight. 2020;5:5.
Ries M. Enzyme replacement therapy and beyond-in memoriam Roscoe O. Brady, M.D. (1923-2016). J Inherit Metab Dis. 2017;40:343-356.
Rapoport M, Saada A, Elpeleg O, Lorberboum-Galski H. TAT-mediated delivery of LAD restores pyruvate dehydrogenase complex activity in the mitochondria of patients with LAD deficiency. Mol Ther. 2008;16:691-697.
Marcus D, Lichtenstein M, Saada A, Lorberboum-Galski H. Replacement of the C6ORF66 assembly factor (NDUFAF4) restores complex I activity in patient cells. Mol Med. 2013;19:124-134.
Vyas PM, Tomamichel WJ, Pride PM, et al. A TAT-frataxin fusion protein increases lifespan and cardiac function in a conditional Friedreich's ataxia mouse model. Hum Mol Genet. 2012;21:1230-1247.
Dinca A, Chien WM, Chin MT. Intracellular delivery of proteins with cell-penetrating peptides for therapeutic uses in human disease. Int J Mol Sci. 2016;17:1-13.
Liou JS, Liu BR, Martin AL, Huang YW, Chiang HJ, Lee HJ. Protein transduction in human cells is enhanced by cell-penetrating peptides fused with an endosomolytic HA2 sequence. Peptides. 2012;37:273-284.
Li M, Tao Y, Shu Y, et al. Discovery and characterization of a peptide that enhances endosomal escape of delivered proteins in vitro and in vivo. J Am Chem Soc. 2015;137:14084-14093.
Schlame M, Acehan D, Berno B, et al. The physical state of lipid substrates provides transacylation specificity for tafazzin. Nat Chem Biol. 2012;8:862-869.
Schlame M, Xu Y, Ren M. The basis for acyl specificity in the tafazzin reaction. J Biol Chem. 2017;292:5499-5506.
Abe M, Hasegawa Y, Oku M, et al. Mechanism for remodeling of the acyl chain composition of cardiolipin catalyzed by Saccharomyces cerevisiae tafazzin. J Biol Chem. 2016;291:15491-15502.
Phoon CKL, Acehan D, Schlame M, et al. Tafazzin knockdown in mice leads to a developmental cardiomyopathy with early diastolic dysfunction preceding myocardial noncompaction. J Am Heart Assoc. 2012;1:e000455.
Soustek MS, Falk DJ, Mah CS, et al. Characterization of a transgenic short hairpin RNA-induced murine model of tafazzin deficiency. Hum Gene Ther. 2011;22:865-871.
Acehan D, Vaz F, Houtkooper RH, et al. Cardiac and skeletal muscle defects in a mouse model of human Barth syndrome. J Biol Chem. 2011;286:899-908.
Dinca AA, Chien WM, Chin MT. Identification of novel mitochondrial localization signals in human Tafazzin, the cause of the inherited cardiomyopathic disorder Barth syndrome. J Mol Cell Cardiol. 2018;114:83-92.
Gwaltney C, Stokes J, Aiudi A, et al. Development and content validity of the Barth syndrome symptom assessment (BTHS-SA) for adolescents and adults. Orphanet J Rare Dis. 2021;16:264.
Winhusen T. Not getting lost in translational science: a tool for navigating the pre-implementation phase of multi-site pharmacological clinical trials. Appl Clin Trials. 2014;23:36-39.