FABRY DISEASE: Phenotypic Spectrum Genotype/Phenotype Correlations Enzyme Replacement Therapy (ERT) R. J. Desnick, Ph.D., M.D.

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1 FABRY DISEASE: Phenotypic Spectrum Genotype/Phenotype Correlations Enzyme Replacement Therapy (ERT) R. J. Desnick, Ph.D., M.D. Director, International Center for Fabry Disease Dean for Genetic & Genomic Medicine Professor & Chair Emeritus Department of Genetics & Genomic Sciences Icahn School of Medicine at Mount Sinai, New York

2 FABRY DISEASE AN X-LINKED LYSOSOMAL STORAGE DISEASE α-galactosidase A Xq22.1 Human X Chromosome

3 FABRY DISEASE: X-LINKED INHERITANCE If Father Is Affected All Daughters Heterozygotes All Sons Unaffected If Mother Is Heterozygotes 50% Daughters Heterozygotes 50% Sons Unaffected

4 METABOLIC DEFECT IN FABRY DISEASE Globotriaosylceramide (GL-3, Gb3) Gal α β β Gal Glu Ceramide α-galactosidase A (α-gal A) Gal Gal Glu Ceramide Lactosylceramide (GL-2, Gb2)

5 PHENOTYPIC SPECTRUM OF FABRY DISEASE Affected Males Later-Onset Phenotypes: Cardiac Subtype Renal Subtype Classic Phenotype <1% Increasing α-gal A Activity >1% Classic Phenotype (Severe Disease) Later-Onset Phenotype Years

6 MAJOR EARLY SITES OF GL-3 ACCUMULATION Micro-Vascular Endothelium & Smooth Muscle: Ischemia & Occlusion: Acroparesthesias, Hypohidrosis, GI Pain, Angiokeratoma Cardiomyocytes: Early Diastolic Dysfunction > LVH & Mitral Insufficiency in Adolescents; Arrythmias Later Renal Endothelial,Podocytes & Tubular Cells: Microalbuminuria > Proteinuria; Isosthenuria, Sediment Inclusions

7 MANIFESTATIONS IN ADOLESCENTS & ADULTS Vascular Glycolipid Manifestations Deposition Skin Angiokeratoma Peripheral Nerves Acroparesthesias; Excruciating Pain Sweat Glands Hypohidrosis Intestine Abdominal Pain/Diarrhea Heart LVH, Myopathy, Arrythmias Brain TIAs, Strokes Kidney Renal Failure Average Age at Death ~40 Years

8 FABRY DISEASE: AGE AT DIALYSIS Thadhani et al., Kidney Int. 61:249, USRDS EDTA-ERA % Patie ents % Females 0 < Age (Years)

9 FABRY DISEASE: SURVIVAL ON DIALYSIS (USRSD ) Thadhani et al., Kid. Int. 61:249, 2002 Survival Distribution Function Non-DM Control Fabry Disease DM Control Time of Follow-Up (Years)

10 FABRY DISEASE: SURVIVAL AFTER RENAL TRANSPLANTATION Oto et al., Transplantation 69: , 2000 Fabry Disease (n = 93) Percent of Patie ents Alive Matched Control (n = 186) Months Post-Transplant

11 RENAL PATHOLOGY: STORAGE TO FIBROSIS Early Disease ESRD

12 KIDNEY DAMAGE STARTS IN FABRY CHILDREN EVEN BEFORE PROTEINURIA Gubler et al., Early Renal Changes in Hemizygous and Heterozygous Patients with Fabry Disease. Kidney Int 13: , 1978 Sheth et al., Early Renal Failure in Fabry s Disease. Am J Kidney Dis 2: , 1983 Tondel et al., Renal Biopsy Findings in Children and Adolescents with Fabry Disease and Minimal Albuminuria. Am J Kidney Dis 51: , 2008 Ramaswami et al., Assessment of Renal Pathology and Dysfunction In Children With Fabry Disease. Clin J Am Soc Nephrol 5: , 2010 Fogo et al., Scoring System for Renal Pathology in Fabry Disease: Report of the International Study Group of Fabry Nephropathy. Nephrol Dial Transplant 25: , 2010

13 KIDNEY DAMAGE STARTS IN FABRY CHILDREN EVEN BEFORE PROTEINURIA Najafian & Mauer, Quantitating Glomerular Endothelial Fenestration: An Unbiased Stereological Approach Am J Nephrol 33 (suppl 1):34-39, 2011 Najaflan et al., Progressive Podocyte Injury and GL-3 Accumulation in Young Patients with Fabry Disease Kidney Int 79: , 2011 Najafian et al., Renal Complications of Fabry Disease in Children. Pediatr Nephrol epub Aug 2012 Tondel et al., Agalsidase Benefits Renal Histology In Young Patients With Fabry Disease. J Am Soc Nephrol 24: , 2013

14 Naiafian et al., Pediatr Nephrol, Epub Aug 17, 2012 ELECTRON MICROGRAPH OF A GLOMERULUS FROM AN 11 YEAR OLD BOY WITH FABRY DISEASE The Patient Had Normal Glomerular Filtration Rate (GFR) and a Urine Protein/Creatinine Ratio of ~ 40 mg/g at Biopsy

15 PHENOTYPIC SPECTRUM OF FABRY DISEASE Later-Onset Phenotypes: Residual (>1%) α-gal A Activity; Missense Some Splicing Mutations; CRIM-Positive Most Lack Pain, Skin Lesions, Hypohidrosis, Eye Changes : Cardiac Subtype: No Vascular Endothelial GL-3 Accumulation Late-Onset: LVH, Myopathy, Arrhythmias, Proteinuria, Normal Renal Function for Age Renal Subtype:: Variable, but Late-Onset Renal Failure at 50-80s

16 RENAL PATHOLOGY Meehan et al., Am J Kidney Dis 43: , 2004 Classic Phenotype p.r227x 75 y/o Cardiac Later-Onset Phenotype p.n215s

17 ENZYMATIC DIAGNOSIS α-galactosidase A Activity Plasma Leukocytes α-gal Activity α-gal Activity

18 The New England Journal of Medicine 345: 9-16, 2001 Safety and Efficacy of Recombinant Human α-galactosidase A Replacement Therapy in Fabry Disease The International Fabry Disease Study Group Eng CM, Guffon N, Wilcox WR, Germain DP, Lee P, Waldeck S, Caplan L, Linthorst GA, and Desnick RJ Multinational, Multicenter, Randomized, Double-Blind, Placebo-Controlled Study: 8 Sites in 4 Countries 58 Classical Affected Patients: 56 M; 2 F Average Age: 30 yrs Dose: 1 mg/kg q 2 wk x11 Doses of Human α-gal A Produced in CHO Cells by Genzyme

19 % Zero-S Scores PRIMARY ENDPOINT RESULTS Renal Histology: Capillary Endothelium Clearance Double Blind P < (2x2 Chi Square) 20/29 69% 24/24 100% Extension Study 23/25 92% /29 0% Placebo Fabrazyme Week 20* PL / FZ FZ / FZ + 6 Months* *As Treated Population, Considered Equivalent to Intent-To-Treat

20 Am. J. Hum. Genet. 75:65-74, 2004 Long Term Safety and Efficacy of Enzyme Replacement Therapy for Fabry Disease Wilcox WR, Benikazemi M, Guffon N, Waldeck S, Lee P, Linthorst GA, Germain DP, and Desnick RJ The International Fabry Disease Study Group All 58 Patients from Phase 3 Continued in Extension Study Dose: 1 mg/kg q 2 wk of Fabrazyme After 30 to 36 Months of ERT: Sustained Capillary Endothelial GL-3 Clearance Plasma GL-3 Remained Normal Mean Serum Creatinine and Estimated GFR Remained Stable Infusion Associated Reactions Continued to Decreased with Time

21 J. Am. Soc. Nephrol., 18: , 2007 Sustained, Long-Term Renal Stabilization After 54 Months of Agalsidase Beta Therapy in Patients with Fabry Disease Germain DP, Waldek S, Banikazemi M, Bushinsky DA, Charrow J, Desnick RJ, Lee P, Loew T, Vedder AC, Abichandani R, Wlicox WR, Guffon N. The International Fabry Disease Study Group

22 PHASE 4 CLINICAL TRIAL Ann Intern Med. 146:77-86, 2007 Agalsidase-Beta Therapy for Advanced Fabry Disease: A Randomized Trial. Banikazemi M, Bultas J, Waldek S, Wilcox WR, Whitley CB, McDonald M, Finkel R,Packman S, Bichet DG, Warnock DG, and Desnick, RJ. Largest Randomized, Double-Blind, Placebo-Controlled Trial in Fabry Disease (n = 82) Narrow Inclusion Criteria: Mid to Moderate Renal Disease: Serum Creatinine 1.2 mg/dl to < 3.0 mg/dl Resulted in High Screening Failure (67&%) 252 Patients Screened at 41 Eligible Sites in 9 Countries

23 PRIMARY ENDPOINT - PROBABILITY OF AN EVENT Kaplan-Meier Analysis of Time to the First Occurrence of a Composite Event Risk Reduction 61% (p=0.034) Percen nt Placebo 44% Events 12/27 Patients Fabrazyme 28% Events 13/47 Patients Time in Study (Months)

24 SUMMARY: PHASE 4 CLINICAL TRIAL ERT IN ADVANCED DISEASE SLOWS CLINICAL PROGRESSION Fabrazyme Therapy Slowed the Rate of Clinical Progression as Manifested by Renal, Cardiac, and Cerebrovascular Outcomes in Patients with Advance Disease There was a 61% Risk Reduction for Events in Patients Treated with Fabrazyme (p = 0.034) Indicated Importance of Reducing Proteinuria with ACEi & ARBs Most Pronounced Effects Observed in Patients Who Had Less Advanced Disease, Emphasizing the Importance of Early Treatment

25 EFFECTS OF EARLY ERT & DOSE ON FABRY RENAL DISEASE & REVERSIBILITY Tøndel et al., J Am Soc Nephrol 24: , 2013 Compared α-gal A Dose & Cumulative Dose on Renal Biopsy Morphology Before & After 5 Yrs of ERT in 12 Patients (1F) from 7-33 Yrs (9<18 Yrs) 7 Patients on 0.2 mg/kg EOW, 2 on Varying Dose & 3 on 1 mg/kg EOW All Doses Cleared Glomerular Endothelial & Mesangial Cell Inclusions Podocyte GL-3 Clearance Was Highly Correlated with Cumulative Dose(p =0.002) There Was Essentially No GL3 Podocyte Clearance at 0.2 mg/kg EOW (7 Patients) Patients on 1 mg/kg EOW Cleared Podocyte & Tubular GL-3 Podocyte Clearance & Decreased Albumin/Creatinine Were Highly Correlated (p = ) The Current Study. Suggests Early Initiation of Treatment & the Use of Sufficiently High Enzyme Dose to Achieve Maximal Clearance of Kidney Cells

26 APPROVAL OF FABRAZYME FOR ENZYME REPLACEMENT THERAPY FOR FABRY DISEASE Country Dose Date (mg/kg) European Union 1.0 August, 2001 United States 1.0 April, 2003 Approved in Over 50 Countries

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