Types A and B Niemann-Pick disease

Molecular Genetics and Metabolism

Volumn 120, Issue 1-2, 2017, Pages 27-33

  Schuchman, Edward H ^a   Desnick, Robert J ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Acid sphingomyelinase; Enzyme Replacement Therapy; Mouse model; Niemann Pick; Sphingomyelin

Indexed keywords

SPHINGOMYELIN PHOSPHODIESTERASE; CHOLESTEROL; SPHINGOMYELIN PHOSPHODIESTERASE 1, HUMAN;

CHOLESTEROL TRANSPORT; CLINICAL FEATURE; DISEASE ACTIVITY; DISEASE COURSE; ENZYME REPLACEMENT; GENE MUTATION; GENOTYPE PHENOTYPE CORRELATION; HEPATOSPLENOMEGALY; HISTORY; HUMAN; MEDICAL HISTORY; MOLECULAR GENETICS; NIEMANN PICK DISEASE; NONHUMAN; ONSET AGE; PATHOLOGY; PRIORITY JOURNAL; REVIEW; ANIMAL; CLASSIFICATION; DEFICIENCY; FEMALE; GENETICS; MALE; METABOLISM; MUTATION;

AGE OF ONSET; ANIMALS; CHOLESTEROL; DISEASE PROGRESSION; FEMALE; HISTORY, 20TH CENTURY; HISTORY, 21ST CENTURY; HUMANS; MALE; MUTATION; NIEMANN-PICK DISEASES; SPHINGOMYELIN PHOSPHODIESTERASE;

EID: 85011265922     PISSN: 10967192     EISSN: 10967206     Source Type: Journal    
DOI: 10.1016/j.ymgme.2016.12.008     Document Type: Review

References (93)

1. [1] Niemann, A., Ein unbekanntes Krankheitsbild, Jahrb. Kinderheillkd, 79, 1914, 1.
2. [2] Pick, L., Uber die lipoidzellige splenohepatomegalie typus Niemann-Pick als stoffwechselerkrankung. Med. Klin., 23, 1927, 1483.
3. [3] Pick, L., Niemann-Pick's disease and other forms of so-called xanthomases. Am. J. Med. Sci., 185, 1933, 601.
4. [4] Pflander, U., La maladie de Niemann-Pick dans le cadre des lipoidoses. Schweiz. Med. Wochenschr., 1946, 76.
5. [5] Dusendschon, A., Deux cas familiaux de maladie de Niemann-Pick chez adulte. (Thesis), 1946, Faculte de Medicine, Geneva.
6. [6] Klenk, E., Uber die natur der phosphatide der milz bei Niemann-Pickchen Krankheit. Z. Physiol. Chem., 229, 1934, 151.
7. [7] Kanfer, J.N., Young, O.M., Shapiro, D., Brady, R.O., The metabolism of sphingomyelin. I. Purification and properties of a sphingomyelin-cleaving enzyme from rat liver tissue. J. Biol. Chem. 241 (1966), 1081–1084.
8. [8] Brady, R.O., Kanfer, J.N., Mock, M.B., Fredrickson, D.S., The metabolism of sphingomyelins. II. Evidence of an enzymatic deficiency in Niemann-Pick disease. Proc. Natl. Acad. Sci. U. S. A. 55 (1966), 366–369.
9. [9] Schneider, P.B., Kennedy, E.P., Sphingomyelinase in normal human spleens and in spleens from subjects with Niemann-Pick disease. J. Lipid Res. 8 (1967), 202–209.
10. [10] Kampine, J.P., Brady, R.O., Kanfer, J.N., Feld, M., Diagnosis of Gaucher's disease and Niemann-Pick disease with sample samples of venous blood. Science 155 (1967), 86–88.
11. [11] Pentchev, P.G., Gal, A.E., Boothe, A.D., Foukes, J., A lysosomal storage disorder in mice characterized by the accumulation of several sphingolipids. Birth Defects Orig. Artic. Ser. 16 (1980), 225–230.
12. [12] Pentchev, P.G., Boothe, A.D., Kruth, H.S., Weintroub, H., A genetic storage disease in BALB/C mice with a metabolic block in esterification of exogenous cholesterol. J. Biol. Chem. 259 (1984), 5784–5791.
13. [13] Pentchev, P.G., Comly, M.E., Kruth, H.S., Vanier, M.T., A defect in cholesterol esterification in Niemann-Pick disease (type C) patients. Proc. Natl. Acad. Sci. U. S. A. 82 (1985), 8257–8261.
14. [14] McGovern, M.M., Aron, A., Brodie, S.E., Desnick, R.J., Natural history of type A Niemann-Pick disease; possible endpoints for therapeutic trials. Neurology 66 (2006), 228–232.
15. [15] Schuchman, E.H., Desnick, R.J., Niemann-Pick disease type A and B: acid sphingomyelinase deficiencies. Scriver, C.R., Beaudet, A.L., Sly, W.S., (eds.) The Metabolic and Molecular Bases of Inherited Diseases, eighth ed., 2001, 3589–3610.
16. [16] Wasserstein, M.P., Desnick, R.J., Schuchman, E.H., Hossain, S., The natural history of type B Niemann-Pick disease: results from a 10-year longitudinal study. Pediatrics 114 (2004), e672–e677.
17. [17] McGovern, M.M., Wasserstein, M.P., Giugliani, R., Bembi, B., A prospective cross-sectional survey study of the natural history of Niemann-Pick disease type B. Pediatrics 122 (2008), e341–e349.
18. [18] Hollak, C.E., de Sonnaville, E.S., Cassiman, D., Linthorst, G.E., Groener, J.E., Morava, E., Wevers, R.A., Mannens, M., Aerts, J.M., Meersseman, W., Akkerman, E., Niezen-Koning, K.E., Mulder, M.F., Visser, G., Wiljburg, F.A., Lefeber, D., Poorthuis, B.J., Acid sphingomyelinase (ASM) deficiency patients in the Netherlands and Belgium: disease spectrum and natural course in attenuated patients. Mol. Genet. Metab. 107 (2012), 526–533.
19. [19] Pavlů-Pereira, H., Asfaw, B., Poupctová, H., Ledvinová, J., Sikora, J., Vanier, M.T., Sandhoff, K., Zeman, J., Novotná, Z., Chudoba, D., Elleder, M., Acid sphingomyelinase deficiency. Phenotype variability with prevalence of intermediate phenotype in a series of twenty-five Czech and Slovak patients. A multi-approach study. J. Inherit. Metab. Dis. 28 (2005), 203–207.
20. [20] Gal, A.E., Brady, R.O., Hibbert, S.R., A practical chromogenic procedure for the detection of homozygotes and heterozygous carriers of Niemann-Pick disease. N. Engl. J. Med. 293 (1975), 632–636.
21. [21] He, X., Chen, F., Dagan, A., Gatt, S., A fluorescence-based, high-performance liquid chromatographic assay to determine acid sphingomyelinase activity and diagnose types A and B Niemann-Pick disease. Anal. Biochem. 314 (2003), 116–120.
22. [22] Legnini, E., Orsini, J.J., Mühl, A., Johnson, B., Dajnoki, A., Bodamer, O.A., Analysis of acid sphingomyelinase activity in dried blood spots using tandem mass spectrometry. Ann. Lab. Med. 32:5 (2012), 319–323.
23. [23] Wasserstein, M.P., Larkin, A.E., Glass, R.B., Schuchman, E.H., Growth restriction in children with type B Niemann-Pick disease. J. Pediatr. 142 (2003), 424–442.
24. [24] Wasserstein, M., Godbold, J., McGovern, M.M., Skeletal manifestations in pediatric and adult patients with Niemann-Pick disease type B. J. Inherit. Metab. Dis. 36 (2013), 123–127.
25. [25] Isaelli, F., Rea, G., Cappabianca, S., Fabozzi, G., Adult onset pulmonary involvement in Niemann-Pick disease type B. Monaldi Arch. Chest Dis. 75 (2011), 235–240.
26. [26] Minai, O.A., Sullivan, E.J., Stoller, J.K., Pulmonary involvement in Niemann-Pick disease: case report and literature review. Respir. Med. 114 (2000), e672–e677.
27. [27] Wasserstein, M.P., Aron, A., Brodie, S.E., Simonaro, C., Acid sphingomyelinase deficiency: prevalence and characterization of an intermediate phenotype of Niemann-Pick disease. J. Pediatr. 149 (2006), 554–559.
28. [28] McGovern, M.M., Lippa, N., Bagiella, E., Schuchman, E.H., Morbidity and mortality in type B Niemann-Pick disease. Genet. Med. 15 (2013), 618–623.
29. [29] Cassiman, D., Packman, S., Bembi, B., Turkia, H.B., Al-Sayed, M., Schiff, M., Imrie, J., Mabe, P., Takahashi, T., Mengel, K.E., Giugliani, R., Cox, G.F., Cause of death in patients with chronic visceral and chronic neurovisceral acid sphingomyelinase deficiency (Niemann-Pick disease type B and B variant): literature review and report of new cases. Mol. Genet. Metab. 118 (2016), 206–213.
30. [30] Thurberg, B.L., Wasserstein, M.P., Schiano, T., O'Brien, F., Liver and skin histopathology in adults with acid sphingomyelinase deficiency (Niemann-Pick disease type B). Am. J. Surg. Pathol. 36 (2012), 1234–1246.
31. [31] Moles, A., Tarrats, N., Fernandez-Checa, J.C., Mari, M., Cathepsin, B., Overexpression due to acid sphingomyelinase ablation promotes liver fibrosis in Niemann-Pick disease. J. Biol. Chem. 287 (2012), 1178–1188.
32. [32] Dhami, R., He, X., Gordon, R.E., Schuchman, E.H., Analysis of the lung pathology and alveolar macrophage function in the acid sphingomyelinase-deficient mouse model of Niemann-Pick disease. Lab. Investig. 81 (2001), 987–999.
33. [33] Quinn, P.J., Sphingolipid symmetry governs membrane lipid raft structure. Biochim. Biophys. Acta 1838 (2014), 1922–1930.
34. [34] Jana, A., Pahan, K., Sphingolipids and multiple sclerosis. Neruomol. Med. 12 (2010), 351–361.
35. [35] Kirkegaard, T., Roth, A.G., Petersen, N.H., Mahalika, A.K., Hsp70 stabilizes lysosomes and reverts Niemann-Pick disease-associated lysosomal pathology. Nature 463 (2010), 549–553.
36. [36] Chuang, W.L., Pacheco, J., Cooper, S., McGovern, M.M., Lyso-sphingomyelin is elevated in dried blood spots of Niemann-Pick B patients. Mol. Genet. Metab. 111 (2014), 209–211.
37. [37] Henry, B., Ziobro, R., Becker, K.A., Kolesnick, R., Acid sphingomyelinase. Handb. Exp. Pharmacol. 215 (2013), 77–88.
38. [38] Schuchman, E.H., Acid sphingomyelinase, cell membranes and human disease: lessons from Niemann-Pick disease. FEBS Lett. 584 (2010), 1895–1900.
39. [39] Charruyer, A., Grazide, S., Bezombes, C., UV-C light induces raft-associated acid sphingomyelinase and JNK activation and translocation independently on a nuclear signal. J. Biol. Chem. 280 (2005), 19196–19204.
40. [40] Falcone, S., Perrotta, C., De Palma, C., Activation of acid sphingomyelinase and its inhibition by the nitric oxide/cyclic guanosine 3,5-monophosphate pathway: key events in Escherichia coli-elicited apoptosis of dendritic cells. J. Immunol. 173 (2004), 4452–4463.
41. [41] Buccinna, B., Piccinini, M., Prinetti, A., Scandroglio, F., Alterations of myelin-specific proteins and sphingolipids characterize the brains of acid sphingomyelinase-deficient mice, an animal model of Niemann-Pick disease type A. J. Neurochem. 109 (2009), 105–115.
42. [42] Scandroglio, F., Venkata, J.K., Loberto, N., Prioni, S., Lipid content of brain, brain membrane lipid domains, and neurons from acid sphingomyelinase deficient mice. J. Neurochem. 107 (2008), 329–338.
43. [43] Galvan, C., Camoletto, P.G., Cristofani, F., Van Veldhoven, P.P., Anomalous surface distribution of glycosyl phosphatidyl inositol-anchored proteins in neurons lacking acid sphingomyelinase. Mol. Biol. Cell 19 (2008), 509–522.
44. [44] Schissel, S.L., Jiang, X., Tweedie-Hardman, J., Jeong, T., Secretory sphingomyelinase, a product of the acid sphingomyelinase gene, can hydrolyze atherogenic lipoproteins at neutral pH. Implication for atherosclerotic lesion development. J. Biol. Chem. 273 (1998), 2738–2746.
45. [45] Castro, B.M., Prieto, M., Silva, L.C., Ceramide: a simple sphingolipid with unique biophysical properties. Prog. Lipid Res. 54C (2014), 53–67.
46. [46] Kornhuber, J., Muller, C.P., Becker, K.A., Reichel, M., The ceramide system as a novel antidepressant target. Trends Pharmacol. Sci. 35 (2014), 293–304.
47. [47] Larsen, P.J., Tennagels, N., On ceramides, other sphingolipids and impaired glucose homeostasis. Mol. Metab. 3 (2014), 252–260.
48. [48] Kosinska, M.K., Liebisch, G., Lochnit, G., Wilhelm, J., A lipidomic study of phospholipid classes and species in human synovial fluid. Arthritis Rheum. 65 (2013), 2323–2333.
49. [49] McGovern, M.M., Pohl-Worgall, T., Deckelbaum, R.J., Simpson, W., Mendelson, D., Desnick, R.J., Schuchman, E.H., Wasserstein, M.P., Lipid abnormalities in children with types A and B Niemann Pick disease. J. Pediatr. 145 (2004), 77–81.
50. [50] Ledesma, M.D., Prinetti, A., Sonnino, S., Schuchman, E.H., Brain pathology in Niemann-Pick disease type A: insights from the acid sphingomyelinase knockout mice. J. Neurochem. 116 (2011), 779–788.
51. [51] Schuchman, E.H., Levran, O., Pereira, L.V., Structural organization and complete nucleotide sequence of the gene encoding human acid sphingomyelinase (SMPD1). Genomics 12 (1992), 197–205.
52. [52] da Veiga Pereira, L., Desnick, R.J., Adler, D.A., Regional assignment of the human acid sphingomyelinase gene (SMPD1) by PCR analysis of somatic cell hybrids and in situ hybridization to 11p15.1–p15.4. Genomics 9 (1992), 229–234.
53. [53] Simonaro, C.M., Park, J.H., Eliyahu, E., Imprinting at the SMPD-1 gene: implications for acid sphingomyelinase- deficient Niemann-Pick disease. Am. J. Hum. Genet. 78 (2006), 79–84.
54. [54] Lee, C.Y., Krimbou, L., Vincent, J., Compound heterozygosity at the sphingomyelin phosphodiesterase-1 (SMPD1) gene is associated with low HDL cholesterol. Hum. Genet. 112 (2003), 552–562.
55. [55] Simonaro, C.M., Desnick, R.J., McGovern, M.M., The demographics and distribution of type B Niemann-Pick disease: novel mutations lead to new genotype/phenotype correlations. Am. J. Hum. Genet. 71 (2002), 1413–1419.
56. [56] Zampieri, S., Filocamo, M., Pianta, A., Lualdi, S., SMPD1 mutation update: database and comprehensive analysis of published and novel variants. Hum. Mutat. 37 (2016), 139–147.
57. [57] Wan, Q., Schuchman, E.H., A novel polymorphism in the human acid sphingomyelinase gene due to size variation of the signal peptide region. Biochim. Biophys. Acta 1270 (1995), 207–210.
58. [58] Foo, J.N., Liany, H., Bei, J.X., Liu, J., Rare lysosomal enzyme gene SMPD1 variant (p.R591C) associates with Parkinson's disease. Neurobiol. Aging, 34, 2013, 2890.
59. [59] Gan-Or, Z., Ozelius, L.J., Bar-Shira, A., Saunders-Pullman, R., The p.L302P mutation in the lysosomal gene SMPD1 is a risk factor for Parkinson disease. Neurology 80 (2013), 1606–1610.
60. [60] ACOG Committee on Genetics, ACOG Committee opinion no. 442: preconception and prenatal carrier screening for genetic diseases in individuals of Eastern European Jewish descent. Obstet. Gynecol. 114 (2009), 950–953.
61. [61] Acuña, M., Martínez, P., Moraga, C., He, X., Epidemiological clinical and biochemical characterization of the p.(Ala359Asp) SMPD1 variant causing Niemann-Pick disease type B. Eur. J. Hum. Genet. 24 (2016), 208–213.
62. [62] Gorelik, A., Illes, K., Heinz, L.X., Superti-Furga, G., Crystal structure of mammalian acid sphingomyelinase. Nat. Commun., 20(7), 2016, 12196.
63. [63] Xiong, Z.J., Huang, J., Poda, G., Pomès, R., Structure of human acid sphingomyelinase reveals the role of the saposin domain in activating substrate hydrolysis. J. Mol. Biol. 428 (2016), 3026–3042.
64. [64] Otterbach, B., Stoffel, W., Acid sphingomyelinase-deficient mice mimic the neurovisceral form of human lysosomal storage disease (Niemann-Pick disease). Cell 81 (1995), 1053–1061.
65. [65] Horinouchi, K., Erlich, S., Perl, D.P., Ferlinz, K., Acid sphingomyelinase deficient mice: a model of types A and B Niemann-Pick disease. Nat. Genet. 10 (1995), 288–293.
66. [66] Dhami, R., He, X., Schuchman, E.H., Gene expression analysis in acid sphingomyelinase deficient mice. Novel insights into disease pathogenesis and identification of potential bio-markers to monitor Niemann-Pick disease treatment. Mol. Ther. 13 (2005), 556–563.
67. [67] Brinkman, J., Wilburg, F.A., Hollak, C.E., Groener, J.E., Plasma chitotriosidase and CCL18: early biochemical surrogate markers in type B Niemann-Pick disease. J. Inherit. Metab. Dis. 28 (2005), 13–20.
68. [68] Utermohlen, O., Karow, U., Lohler, J., Severe impairment in early host defense against Listeria monocytogenes in mice deficient in acid sphingomyelinase. J. Immunol. 170 (2003), 2621–2628.
69. [69] Morita, Y., Perez, G.I., Paris, F., Oocyte apoptosis is suppressed by disruption of the acid sphingomyelinase gene or by sphingosine-1-phosphate therapy. Nat. Med. 6 (2000), 1109–1114.
70. [70] Marathe, S., Miranda, S.R., Devlin, C., Creation of a mouse model for non-neurological (type B) Niemann-Pick disease by stable, low level expression of lysosomal sphingomyelinase in the absence of secretory sphingomyelinase: relationship between brain intralysosomal enzyme activity and central nervous system function. Hum. Mol. Genet. 9 (2004), 1967–1976.
71. [71] Jones, I., He, X., Katouzian, F., Darroch, P.I., Characterization of common SMPD1 mutations causing types A and B Niemann-Pick disease and generation of mutation-specific mouse models. Mol. Genet. Metab. 95 (2008), 152–162.
72. [72] Victor, S., Coutler, J.B.S., Besley, G.T.N., Niemann-Pick disease type B: 16 year follow-up after allogenic bone marrow transplantation. J. Inherit. Metab. Dis. 26 (2003), 775–785.
73. [73] Miranda, S.R., Erlich, S., Friedrich, V.L. Jr., Biochemical, pathological, and clinical response to transplantation of normal bone marrow cells into acid sphingomyelinase deficient mice. Transplantation 65 (1998), 884–892.
74. [74] Jin, H.K., Schuchman, E.H., Combined bone marrow and intracerebral mesenchymal stem cell transplantation leads to synergistic visceral and neurological improvements in Niemann-Pick disease mice. Mol. Ther. 26 (2003), 775–785.
75. [75] Cerneca, F., Andolina, M., Simeone, R., Treatment of patients with Niemann-Pick disease using repeated amniotic epithelial cells implantation: correction of aggregation and coagulation abnormalities. Clin. Pediatr. 36 (1997), 141–146.
76. [76] Daloze, P., Delvin, E.E., Glorieux, F.H., Replacement therapy for inherited enzyme deficiency: liver orthotopic transplantation in Niemann-Pick disease type A. Am. J. Med. Genet. 1 (1977), 229–239.
77. [77] Scaggiante, B., Pineschi, A., Sustersich, M., Successful therapy of Niemann-Pick disease by implantation of human amniotic membrane. Transplantation 44 (1987), 59–61.
78. [78] Smanik, E.J., Tavill, A.S., Jacobs, G.H., Orthotopic liver transplantation in two adults with Niemann-Pick's and Gaucher's disease-implications for the treatment of inherited metabolic disease. Hepatology 17 (1993), 42–49.
79. [79] Coelho, G.R., Praciano, A.M., Rodrigues, J.P., Viana, C.F., Brandão, K.P., Valenca, J.T. Jr., Garcia, J.H., Liver transplantation in patients with Niemann-Pick disease-single-center experience. Transplant. Proc. 47 (2015), 2929–2931.
80. [80] Brady, R.O., Enzyme replacement for lysosomal diseases. Annu. Rev. Med. 57 (2006), 283–296.
81. [81] He, X., Miranda, S.R., Xiong, X., Characterization of human acid sphingomyelinase purified from the media of overexpressing Chinese hamster ovary cells. Biochim. Biophys. Acta 1432 (1999), 251–264.
82. [82] Miranda, S.R., He, X., Simonaro, C.M., Infusion of recombinant human acid sphingomyelinase into Niemann-Pick disease mice leads to visceral, but not neurological correction of the pathophysiology. FASEB J. 14 (2000), 1988–1995.
83. [83] Murray, J.M., Thompson, A.M., Vitsky, A., Hawes, M., Nonclinical safety assessment of recombinant human acid sphingomyelinase (rhASM) for the treatment of acid sphingomyelinase deficiency; the utility of animal models of disease in the toxicological evaluation of potential therapeutics. Mol. Genet. Metab. 114 (2015), 217–225.
84. [84] McGovern, M.M., Wasserstein, M.P., Kirmse, B., Duvall, W.L., Schiano, T., Thurberg, B.L., Richards, S., Cox, G.F., Novel first-dose adverse drug reactions during a phase I trial of olipudase alfa (recombinant human acid sphingomyelinase) in adults with Niemann-Pick disease type B (acid sphingomyelinase deficiency). Genet. Med. 18 (2016), 34–40.
85. [85] Wasserstein, M.P., Jones, S.A., Sora, H., Diaz, G.A., Successful within-patient dose escalation of olipudase alfa in acid sphingomyelinase deficiency. Mol. Genet. Metab. 116 (2015), 88–97.
86. [86] Wasserstein, M.P., Lachmann, R., Jouvin, M.H., Haney, J., Long-term Safety and Efficacy of Olipudase Alfa in Patients with Acid Sphingomyelinase Deficiency (ASMD). 2016 (Abstract LB-28, World symposium).
87. [87] https://clinicaltrials.gov/ct2/results?term=acid+sphingomyelinase&Search=Search.
88. [88] Miranda, S.R., Erlich, S., Friedrich, V.L., Gatt, S., Hematopoietic stem cell gene therapy leads to marked visceral organ improvements and a delayed onset of neurological abnormalities in the acid sphingomyelinase deficient mouse model of Niemann-Pick disease. Gene Ther. 7 (2000), 1768–1776.
89. [89] Barbon, C.M., Ziegler, R.J., Li, C., Armentano, D., AAV8-mediated hepatic expression of acid sphingomyelinase corrects the metabolic defect in the visceral organs of a mouse model of Niemann-Pick disease. Mol. Ther. 12 (2005), 431–440.
90. [90] Dodge, J.C., Clarke, J., Song, A., Bu, J., Gene transfer of human acid sphingomyelinase corrects neuropathology and motor deficits in a mouse model of Niemann-Pick disease. Proc. Natl. Acad. Sci. U. S. A. 102 (2005), 17822–17827.
91. [91] Dodge, J.C., Clarke, J., Treleaven, C.M., Taksir, T.V., Intracerebroventricular infusion of acid sphingomyelinase corrects CNS manifestations in a mouse model of Niemann-Pick A disease. Exp. Neurol. 215 (2009), 349–457.
92. [92] Arroyo, A.L., Camoletto, P.G., Morando, L., Sassoe-Pognetto, M., Pharmacological reversion of sphingomyelin-induced dendritic spine anomalies in a Niemann-Pick disease type A mouse model. EMBO Mol. Med. 6 (2014), 398–413.
93. [93] Germain, D.P., Hughes, D.A., Nicholls, K., Bichet, D.G., Treatment of Fabry's disease with the pharmacologic chaperone migalastat. N. Engl. J. Med. 11 (2016), 545–555.