Acid Sphingomyelinase Deficiency: A Clinical and Immunological Perspective

Carolina Pinto, Diana Sousa, Vladimir Ghilas, Andrea Dardis, Maurizio Scarpa, Maria Fatima Macedo, Carolina Pinto, Diana Sousa, Vladimir Ghilas, Andrea Dardis, Maurizio Scarpa, Maria Fatima Macedo

Abstract

Acid sphingomyelinase deficiency (ASMD) is a lysosomal storage disease caused by deficient activity of acid sphingomyelinase (ASM) enzyme, leading to the accumulation of varying degrees of sphingomyelin. Lipid storage leads to foam cell infiltration in tissues, and clinical features including hepatosplenomegaly, pulmonary insufficiency and in some cases central nervous system involvement. ASM enzyme replacement therapy is currently in clinical trial being the first treatment addressing the underlying pathology of the disease. Therefore, presently, it is critical to better comprehend ASMD to improve its diagnose and monitoring. Lung disease, including recurrent pulmonary infections, are common in ASMD patients. Along with lung disease, several immune system alterations have been described both in patients and in ASMD animal models, thus highlighting the role of ASM enzyme in the immune system. In this review, we summarized the pivotal roles of ASM in several immune system cells namely on macrophages, Natural Killer (NK) cells, NKT cells, B cells and T cells. In addition, an overview of diagnose, monitoring and treatment of ASMD is provided highlighting the new enzyme replacement therapy available.

Keywords: Niemann–Pick; acid sphingomyelinase deficiency; immune; lysosomal storage disease; sphingomyelinase.

Conflict of interest statement

M.F.M. received in the past a research grant from Sanofi-Genzyme. A.D. received travel grants and speaker fees from Sanofi-Genzyme and Takeda and has participated in advisory boards and received a research grant from Amicus. M.S. received research and honoraria for lecturing from Amicus, Alexion, Sanofi-Genzyme, Takeda, Orchard, Ultragenix Chiesi, Azafaros and Orphazyme. The remaining authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Differential diagnosis for ASMD.
Figure 2
Figure 2
Sphingomyelin regulates CD1d access to potentially agonistic lipids. (A) In the absence of sphingomyelin, lipid antigens are free to access CD1d present in antigen-presenting cells (APCs), binding to iNKT cell TCR and leading to cell activation. (B) In cases of ASM deficiency, excess sphingomyelin binds to CD1d on APCs, preventing the binding of lipid antigens, and, as a consequence, leads to impediment of iNKT cell activation.

References

    1. Schuchman E.H., Desnick R.J. Types A and B Niemann-Pick disease. Mol. Genet. Metab. 2017;120:27–33. doi: 10.1016/j.ymgme.2016.12.008.
    1. Brady R.O., Kanfer J.N., Mock M.B., Fredrickson D.S. The metabolism of sphingomyelin. II. Evidence of an enzymatic deficiency in Niemann-Pick diseae. Proc. Natl. Acad. Sci. USA. 1966;55:366–369. doi: 10.1073/pnas.55.2.366.
    1. Pentchev P.G., Comly M.E., Kruth H.S., Vanier M.T., Wenger D.A., Patel S., Brady R.O. A defect in cholesterol esterification in Niemann-Pick disease (type C) patients. Proc. Natl. Acad. Sci. USA. 1985;82:8247–8251. doi: 10.1073/pnas.82.23.8247.
    1. Platt F.M., d’Azzo A., Davidson B.L., Neufeld E.F., Tifft C.J. Lysosomal storage diseases. Nat. Rev. Dis. Primers. 2018;4:27. doi: 10.1038/s41572-018-0025-4.
    1. McGovern M.M., Aron A., Brodie S.E., Desnick R.J., Wasserstein M.P. Natural history of Type A Niemann-Pick disease: Possible endpoints for therapeutic trials. Neurology. 2006;66:228–232. doi: 10.1212/01.wnl.0000194208.08904.0c.
    1. Wasserstein M.P., Desnick R.J., Schuchman E.H., Hossain S., Wallenstein S., Lamm C., McGovern M.M. The natural history of type B Niemann-Pick disease: Results from a 10-year longitudinal study. Pediatrics. 2004;114:e672–e677. doi: 10.1542/peds.2004-0887.
    1. McGovern M.M., Avetisyan R., Sanson B.J., Lidove O. Disease manifestations and burden of illness in patients with acid sphingomyelinase deficiency (ASMD) Orphanet. J. Rare Dis. 2017;12:41. doi: 10.1186/s13023-017-0572-x.
    1. Sagaert X., Tousseyn T., De Hertogh G., Geboes K. Macrophage-related diseases of the gut: A pathologist’s perspective. Virchows Arch. 2012;460:555–567. doi: 10.1007/s00428-012-1244-9.
    1. McGovern M.M., Dionisi-Vici C., Giugliani R., Hwu P., Lidove O., Lukacs Z., Eugen Mengel K., Mistry P.K., Schuchman E.H., Wasserstein M.P. Consensus recommendation for a diagnostic guideline for acid sphingomyelinase deficiency. Genet. Med. 2017;19:967–974. doi: 10.1038/gim.2017.7.
    1. Nascimbeni F., Dionisi Vici C., Vespasiani Gentilucci U., Angelico F., Nobili V., Petta S., Valenti L., Committee A.R.D. AISF update on the diagnosis and management of adult-onset lysosomal storage diseases with hepatic involvement. Dig. Liver Dis. 2020;52:359–367. doi: 10.1016/j.dld.2019.12.005.
    1. Wasserstein M.P., Aron A., Brodie S.E., Simonaro C., Desnick R.J., McGovern M.M. Acid sphingomyelinase deficiency: Prevalence and characterization of an intermediate phenotype of Niemann-Pick disease. J. Pediatr. 2006;149:554–559. doi: 10.1016/j.jpeds.2006.06.034.
    1. Pavlů-Pereira H., Asfaw B., Poupctová H., Ledvinová J., Sikora J., Vanier M.T., Sandhoff K., Zeman J., Novotná Z., Chudoba D., et al. 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. 2005;28:203–227. doi: 10.1007/s10545-005-5671-5.
    1. Zampieri S., Filocamo M., Pianta A., Lualdi S., Gort L., Coll M.J., Sinnott R., Geberhiwot T., Bembi B., Dardis A. SMPD1 Mutation Update: Database and Comprehensive Analysis of Published and Novel Variants. Hum. Mutat. 2016;37:139–147. doi: 10.1002/humu.22923.
    1. Schuchman E.H., Miranda S.R. Niemann-Pick disease: Mutation update, genotype/phenotype correlations, and prospects for genetic testing. Genet. Test. 1997;1:13–19. doi: 10.1089/gte.1997.1.13.
    1. da Veiga Pereira L., Desnick R.J., Adler D.A., Disteche C.M., Schuchman E.H. 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. 1991;9:229–234. doi: 10.1016/0888-7543(91)90246-B.
    1. Simonaro C.M., Desnick R.J., McGovern M.M., Wasserstein M.P., Schuchman E.H. The demographics and distribution of type B Niemann-Pick disease: Novel mutations lead to new genotype/phenotype correlations. Am. J. Hum. Genet. 2002;71:1413–1419. doi: 10.1086/345074.
    1. Pittis M.G., Montalvo A.L., Miocic S., Martini C., Deganuto M., Candusso M., Ciana G., Bembi B. Identification of four novel mutations in the alpha glucosidase gene in five Italian patients with infantile onset glycogen storage disease type II. Am. J. Med. Genet. A. 2003;121A:225–230. doi: 10.1002/ajmg.a.20164.
    1. Dardis A., Zampieri S., Filocamo M., Burlina A., Bembi B., Pittis M.G. Functional in vitro characterization of 14 SMPD1 mutations identified in Italian patients affected by Niemann Pick Type B disease. Hum. Mutat. 2005;26:164. doi: 10.1002/humu.9353.
    1. Zhang H., Wang Y., Gong Z., Li X., Qiu W., Han L., Ye J., Gu X. Identification of a distinct mutation spectrum in the SMPD1 gene of Chinese patients with acid sphingomyelinase-deficient Niemann-Pick disease. Orphanet. J. Rare Dis. 2013;8:15. doi: 10.1186/1750-1172-8-15.
    1. 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. 1995;1270:207–210. doi: 10.1016/0925-4439(95)00050-E.
    1. Ricci V., Stroppiano M., Corsolini F., Di Rocco M., Parenti G., Regis S., Grossi S., Biancheri R., Mazzotti R., Filocamo M. Screening of 25 Italian patients with Niemann-Pick A reveals fourteen new mutations, one common and thirteen private, in SMPD1. Hum. Mutat. 2004;24:105. doi: 10.1002/humu.9258.
    1. Pittis M.G., Ricci V., Guerci V.I., Marcais C., Ciana G., Dardis A., Gerin F., Stroppiano M., Vanier M.T., Filocamo M., et al. Acid sphingomyelinase: Identification of nine novel mutations among Italian Niemann Pick type B patients and characterization of in vivo functional in-frame start codon. Hum. Mutat. 2004;24:186–187. doi: 10.1002/humu.9263.
    1. Rodriguez-Pascau L., Gort L., Schuchman E.H., Vilageliu L., Grinberg D., Chabas A. Identification and characterization of SMPD1 mutations causing Niemann-Pick types A and B in Spanish patients. Hum. Mutat. 2009;30:1117–1122. doi: 10.1002/humu.21018.
    1. Aykut A., Karaca E., Onay H., Ucar S.K., Coker M., Cogulu O., Ozkinay F. Analysis of the sphingomyelin phosphodiesterase 1 gene (SMPD1) in Turkish Niemann-Pick disease patients: Mutation profile and description of a novel mutation. Gene. 2013;526:484–486. doi: 10.1016/j.gene.2013.03.116.
    1. 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., et al. Acid sphingomyelinase (Asm) deficiency patients in The Netherlands and Belgium: Disease spectrum and natural course in attenuated patients. Mol. Genet. Metab. 2012;107:526–533. doi: 10.1016/j.ymgme.2012.06.015.
    1. Fernandez-Burriel M., Pena L., Ramos J.C., Cabrera J.C., Marti M., Rodriguez-Quinones F., Chabas A. The R608del mutation in the acid sphingomyelinase gene (SMPD1) is the most prevalent among patients from Gran Canaria Island with Niemann-Pick disease type B. Clin. Genet. 2003;63:235–236. doi: 10.1034/j.1399-0004.2003.00025.x.
    1. Mihaylova V., Hantke J., Sinigerska I., Cherninkova S., Raicheva M., Bouwer S., Tincheva R., Khuyomdziev D., Bertranpetit J., Chandler D., et al. Highly variable neural involvement in sphingomyelinase-deficient Niemann-Pick disease caused by an ancestral Gypsy mutation. Brain. 2007;130:1050–1061. doi: 10.1093/brain/awm026.
    1. Ferlinz K., Hurwitz R., Vielhaber G., Suzuki K., Sandhoff K. Occurrence of two molecular forms of human acid sphingomyelinase. Pt 3Biochem. J. 1994;301 ( Pt 3):855–862. doi: 10.1042/bj3010855.
    1. Simonaro C.M., Park J.-H., Eliyahu E., Shtraizent N., McGovern M.M., Schuchman E.H. Imprinting at the SMPD1 Locus: Implications for Acid Sphingomyelinase–Deficient Niemann-Pick Disease. Am. J. Hum. Genet. 2006;78:865–870. doi: 10.1086/503750.
    1. Tardy C., Codogno P., Autefage H., Levade T., Nathalie A. Lysosomes and lysosomal proteins in cancer cell death (new players of an old struggle) Biochim. Biophys. Acta. 2006;1765:101–125. doi: 10.1016/j.bbcan.2005.11.003.
    1. Schissel S.L., Schuchman E.H., Williams K.J., Tabas I. Zn2+-stimulated sphingomyelinase is secreted by many cell types and is a product of the acid sphingomyelinase gene. J. Biol. Chem. 1996;271:18431–18436. doi: 10.1074/jbc.271.31.18431.
    1. Schissel S.L., Keesler G.A., Schuchman E.H., Williams K.J., Tabas I. The cellular trafficking and zinc dependence of secretory and lysosomal sphingomyelinase, two products of the acid sphingomyelinase gene. J. Biol. Chem. 1998;273:18250–18259. doi: 10.1074/jbc.273.29.18250.
    1. Chung H.Y., Claus R.A. Keep Your Friends Close, but Your Enemies Closer: Role of Acid Sphingomyelinase During Infection and Host Response. Front. Med. (Lausanne) 2020;7:616500. doi: 10.3389/fmed.2020.616500.
    1. Rotolo J.A., Zhang J., Donepudi M., Lee H., Fuks Z., Kolesnick R. Caspase-dependent and -independent activation of acid sphingomyelinase signaling. J. Biol. Chem. 2005;280:26425–26434. doi: 10.1074/jbc.M414569200.
    1. Ponting C.P. Acid sphingomyelinase possesses a domain homologous to its activator proteins: Saposins B and D. Protein. Sci. 1994;3:359–361. doi: 10.1002/pro.5560030219.
    1. Linke T., Wilkening G., Lansmann S., Moczall H., Bartelsen O., Weisgerber J., Sandhoff K. Stimulation of acid sphingomyelinase activity by lysosomal lipids and sphingolipid activator proteins. Biol. Chem. 2001;382:283–290. doi: 10.1515/BC.2001.035.
    1. Kolter T., Sandhoff K. Principles of lysosomal membrane digestion: Stimulation of sphingolipid degradation by sphingolipid activator proteins and anionic lysosomal lipids. Annu. Rev. Cell Dev. Biol. 2005;21:81–103. doi: 10.1146/annurev.cellbio.21.122303.120013.
    1. Morimoto S., Martin B.M., Kishimoto Y., O’Brien J.S. Saposin D: A sphingomyelinase activator. Biochem. Biophys. Res. Commun. 1988;156:403–410. doi: 10.1016/S0006-291X(88)80855-6.
    1. Xiong Z.J., Huang J., Poda G., Pomes R., Prive G.G. Structure of Human Acid Sphingomyelinase Reveals the Role of the Saposin Domain in Activating Substrate Hydrolysis. J. Mol. Biol. 2016;428:3026–3042. doi: 10.1016/j.jmb.2016.06.012.
    1. Gorelik A., Illes K., Heinz L.X., Superti-Furga G., Nagar B. Crystal structure of mammalian acid sphingomyelinase. Nat. Commun. 2016;7:12196. doi: 10.1038/ncomms12196.
    1. Bai A., Guo Y. Acid sphingomyelinase mediates human CD4(+) T-cell signaling: Potential roles in T-cell responses and diseases. Cell Death Dis. 2017;8:e2963. doi: 10.1038/cddis.2017.360.
    1. Tawk C., Nigro G., Rodrigues Lopes I., Aguilar C., Lisowski C., Mano M., Sansonetti P., Vogel J., Eulalio A. Stress-induced host membrane remodeling protects from infection by non-motile bacterial pathogens. EMBO J. 2018;37:e98529. doi: 10.15252/embj.201798529.
    1. Melum E., Jiang X., Baker K.D., Macedo M.F., Fritsch J., Dowds C.M., Wang J., Pharo A., Kaser A., Tan C., et al. Control of CD1d-restricted antigen presentation and inflammation by sphingomyelin. Nat. Immunol. 2019;20:1644–1655. doi: 10.1038/s41590-019-0504-0.
    1. Henry B., Ziobro R., Becker K.A., Kolesnick R., Gulbins E. Acid sphingomyelinase. Handb. Exp. Pharmacol. 2013:77–88. doi: 10.1007/978-3-7091-1368-4_4.
    1. Park M.H., Jin H.K., Bae J.S. Potential therapeutic target for aging and age-related neurodegenerative diseases: The role of acid sphingomyelinase. Exp. Mol. Med. 2020;52:380–389. doi: 10.1038/s12276-020-0399-8.
    1. Perrotta C., Cervia D., De Palma C., Assi E., Pellegrino P., Bassi M.T., Clementi E. The emerging role of Acid Sphingomyelinase in autophagy. Apoptosis. 2015;20:635–644. doi: 10.1007/s10495-015-1101-9.
    1. Aldosari M.H., de Vries R.P., Rodriguez L.R., Hesen N.A., Beztsinna N., van Kuilenburg A.B.P., Hollak C.E.M., Schellekens H., Mastrobattista E. Liposome-targeted recombinant human acid sphingomyelinase: Production, formulation, and in vitro evaluation. Eur. J. Pharm. Biopharm. 2019;137:185–195. doi: 10.1016/j.ejpb.2019.02.019.
    1. Borie R., Crestani B., Guyard A., Lidove O. Interstitial lung disease in lysosomal storage disorders. Eur. Respir. Rev. 2021;30 doi: 10.1183/16000617.0363-2020.
    1. Sakata A., Ochiai T., Shimeno H., Hikishima S., Yokomatsu T., Shibuya S., Toda A., Eyanagi R., Soeda S. Acid sphingomyelinase inhibition suppresses lipopolysaccharide-mediated release of inflammatory cytokines from macrophages and protects against disease pathology in dextran sulphate sodium-induced colitis in mice. Immunology. 2007;122:54–64. doi: 10.1111/j.1365-2567.2007.02612.x.
    1. Jin J., Zhang X., Lu Z., Perry D.M., Li Y., Russo S.B., Cowart L.A., Hannun Y.A., Huang Y. Acid sphingomyelinase plays a key role in palmitic acid-amplified inflammatory signaling triggered by lipopolysaccharide at low concentrations in macrophages. Am. J. Physiol. Endocrinol. Metab. 2013;305:E853–E867. doi: 10.1152/ajpendo.00251.2013.
    1. Truman J.-P., Al Gadban M.M., Smith K.J., Jenkins R.W., Mayroo N., Virella G., Lopes-Virella M.F., Bielawska A., Hannun Y.A., Hammad S.M. Differential regulation of acid sphingomyelinase in macrophages stimulated with oxidized low-density lipoprotein (LDL) and oxidized LDL immune complexes: Role in phagocytosis and cytokine release. Immunology. 2012;136:30–45. doi: 10.1111/j.1365-2567.2012.03552.x.
    1. Peng H., Li C., Kadow S., Henry B.D., Steinmann J., Becker K.A., Riehle A., Beckmann N., Wilker B., Li P.L., et al. Acid sphingomyelinase inhibition protects mice from lung edema and lethal Staphylococcus aureus sepsis. J. Mol. Med. (Berl.) 2015;93:675–689. doi: 10.1007/s00109-014-1246-y.
    1. Xiang H., Jin S., Tan F., Xu Y., Lu Y., Wu T. Physiological functions and therapeutic applications of neutral sphingomyelinase and acid sphingomyelinase. Biomed. Pharm. 2021;139:111610. doi: 10.1016/j.biopha.2021.111610.
    1. Schramm M., Herz J., Haas A., Kronke M., Utermohlen O. Acid sphingomyelinase is required for efficient phago-lysosomal fusion. Cell Microbiol. 2008;10:1839–1853. doi: 10.1111/j.1462-5822.2008.01169.x.
    1. Utermöhlen O., Karow U., Löhler J., Krönke M. Severe impairment in early host defense against Listeria monocytogenes in mice deficient in acid sphingomyelinase. J. Immunol. 2003;170:2621–2628. doi: 10.4049/jimmunol.170.5.2621.
    1. Ghosh S., Bhattacharyya S., Das S., Raha S., Maulik N., Das D.K., Roy S., Majumdar S. Generation of ceramide in murine macrophages infected with Leishmania donovani alters macrophage signaling events and aids intracellular parasitic survival. Mol. Cell Biochem. 2001;223:47–60. doi: 10.1023/A:1017996609928.
    1. Steinbrecher U.P., Gómez-Muñoz A., Duronio V. Acid sphingomyelinase in macrophage apoptosis. Curr. Opin. Lipidol. 2004;15:531–537. doi: 10.1097/00041433-200410000-00006.
    1. Deigner H.P., Claus R., Bonaterra G.A., Gehrke C., Bibak N., Blaess M., Cantz M., Metz J., Kinscherf R. Ceramide induces aSMase expression: Implications for oxLDL-induced apoptosis. Faseb. J. 2001;15:807–814. doi: 10.1096/fj.15.3.807.
    1. Zhao M., Pan W., Shi R.Z., Bai Y.P., You B.Y., Zhang K., Fu Q.M., Schuchman E.H., He X.X., Zhang G.G. Acid Sphingomyelinase Mediates Oxidized-LDL Induced Apoptosis in Macrophage via Endoplasmic Reticulum Stress. J. Atheroscler Thromb. 2016;23:1111–1125. doi: 10.5551/jat.32383.
    1. Zhang Y., Li X., Carpinteiro A., Gulbins E. Acid sphingomyelinase amplifies redox signaling in Pseudomonas aeruginosa-induced macrophage apoptosis. J. Immunol. 2008;181:4247–4254. doi: 10.4049/jimmunol.181.6.4247.
    1. Diaz G.A., Jones S.A., Scarpa M., Mengel K.E., Giugliani R., Guffon N., Batsu I., Fraser P.A., Li J., Zhang Q., et al. One-year results of a clinical trial of olipudase alfa enzyme replacement therapy in pediatric patients with acid sphingomyelinase deficiency. Genet. Med. 2021;23:1543–1550. doi: 10.1038/s41436-021-01156-3.
    1. Eskes E.C.B., Sjouke B., Vaz F.M., Goorden S.M.I., van Kuilenburg A.B.P., Aerts J.M.F.G., Hollak C.E.M. Biochemical and imaging parameters in acid sphingomyelinase deficiency: Potential utility as biomarkers. Mol. Genet. Metab. 2020;130:16–26. doi: 10.1016/j.ymgme.2020.02.002.
    1. Pozo D., Valés-Gómez M., Mavaddat N., Williamson S.C., Chisholm S.E., Reyburn H. CD161 (human NKR-P1A) signaling in NK cells involves the activation of acid sphingomyelinase. J. Immunol. 2006;176:2397–2406. doi: 10.4049/jimmunol.176.4.2397.
    1. Taguchi Y., Kondo T., Watanabe M., Miyaji M., Umehara H., Kozutsumi Y., Okazaki T. Interleukin-2-induced survival of natural killer (NK) cells involving phosphatidylinositol-3 kinase-dependent reduction of ceramide through acid sphingomyelinase, sphingomyelin synthase, and glucosylceramide synthase. Blood. 2004;104:3285–3293. doi: 10.1182/blood-2004-03-0900.
    1. Taniguchi M., Ogiso H., Takeuchi T., Kitatani K., Umehara H., Okazaki T. Lysosomal ceramide generated by acid sphingomyelinase triggers cytosolic cathepsin B-mediated degradation of X-linked inhibitor of apoptosis protein in natural killer/T lymphoma cell apoptosis. Cell Death Dis. 2015;6:e1717. doi: 10.1038/cddis.2015.82.
    1. Grassme H., Jendrossek V., Bock J., Riehle A., Gulbins E. Ceramide-rich membrane rafts mediate CD40 clustering. J. Immunol. 2002;168:298–307. doi: 10.4049/jimmunol.168.1.298.
    1. Korthäuer U., Graf D., Mages H.W., Brière F., Padayachee M., Malcolm S., Ugazio A.G., Notarangelo L.D., Levinsky R.J., Kroczek R.A. Defective expression of T-cell CD40 ligand causes X-linked immunodeficiency with hyper-IgM. Nature. 1993;361:539–541. doi: 10.1038/361539a0.
    1. Allen R.C., Armitage R.J., Conley M.E., Rosenblatt H., Jenkins N.A., Copeland N.G., Bedell M.A., Edelhoff S., Disteche C.M., Simoneaux D.K., et al. CD40 Ligand Gene Defects Responsible for X-Linked Hyper-IgM Syndrome. Science. 1993;259:990–993. doi: 10.1126/science.7679801.
    1. Miller H., Castro-Gomes T., Corrotte M., Tam C., Maugel T.K., Andrews N.W., Song W. Lipid raft-dependent plasma membrane repair interferes with the activation of B lymphocytes. J. Cell Biol. 2015;211:1193–1205. doi: 10.1083/jcb.201505030.
    1. Canonico B., Cesarini E., Salucci S., Luchetti F., Falcieri E., Di Sario G., Palma F., Papa S. Defective Autophagy, Mitochondrial Clearance and Lipophagy in Niemann-Pick Type B Lymphocytes. PLoS ONE. 2016;11:e0165780. doi: 10.1371/journal.pone.0165780.
    1. Manjithaya R., Subramani S. Autophagy: A broad role in unconventional protein secretion? Trends Cell Biol. 2011;21:67–73. doi: 10.1016/j.tcb.2010.09.009.
    1. Hollmann C., Werner S., Avota E., Reuter D., Japtok L., Kleuser B., Gulbins E., Becker K.A., Schneider-Schaulies J., Beyersdorf N. Inhibition of Acid Sphingomyelinase Allows for Selective Targeting of CD4+ Conventional versus Foxp3+ Regulatory T Cells. J. Immunol. 2016;197:3130–3141. doi: 10.4049/jimmunol.1600691.
    1. Bai A., Kokkotou E., Zheng Y., Robson S.C. Role of acid sphingomyelinase bioactivity in human CD4+ T-cell activation and immune responses. Cell Death Dis. 2015;6:e1828. doi: 10.1038/cddis.2015.178.
    1. Hose M., Gunther A., Abberger H., Begum S., Korencak M., Becker K.A., Buer J., Westendorf A.M., Hansen W. T Cell-Specific Overexpression of Acid Sphingomyelinase Results in Elevated T Cell Activation and Reduced Parasitemia During Plasmodium yoelii Infection. Front. Immunol. 2019;10:1225. doi: 10.3389/fimmu.2019.01225.
    1. Boll S., Ziemann S., Ohl K., Klemm P., Rieg A.D., Gulbins E., Becker K.A., Kamler M., Wagner N., Uhlig S., et al. Acid sphingomyelinase regulates TH 2 cytokine release and bronchial asthma. Allergy. 2020;75:603–615. doi: 10.1111/all.14039.
    1. Meiners J., Palmieri V., Klopfleisch R., Ebel J.F., Japtok L., Schumacher F., Yusuf A.M., Becker K.A., Zoller J., Hose M., et al. Intestinal Acid Sphingomyelinase Protects From Severe Pathogen-Driven Colitis. Front. Immunol. 2019;10:1386. doi: 10.3389/fimmu.2019.01386.
    1. Zhou Y., Salker M.S., Walker B., Munzer P., Borst O., Gawaz M., Gulbins E., Singh Y., Lang F. Acid Sphingomyelinase (ASM) is a Negative Regulator of Regulatory T Cell (Treg) Development. Cell Physiol. Biochem. 2016;39:985–995. doi: 10.1159/000447806.
    1. Assi E., Cervia D., Bizzozero L., Capobianco A., Pambianco S., Morisi F., De Palma C., Moscheni C., Pellegrino P., Clementi E., et al. Modulation of Acid Sphingomyelinase in Melanoma Reprogrammes the Tumour Immune Microenvironment. Mediat. Inflamm. 2015;2015:370482. doi: 10.1155/2015/370482.
    1. Wiese T., Dennstadt F., Hollmann C., Stonawski S., Wurst C., Fink J., Gorte E., Mandasari P., Domschke K., Hommers L., et al. Inhibition of acid sphingomyelinase increases regulatory T cells in humans. Brain Commun. 2021;3:fcab020. doi: 10.1093/braincomms/fcab020.
    1. Tischner D., Theiss J., Karabinskaya A., van den Brandt J., Reichardt S.D., Karow U., Herold M.J., Luhder F., Utermohlen O., Reichardt H.M. Acid sphingomyelinase is required for protection of effector memory T cells against glucocorticoid-induced cell death. J. Immunol. 2011;187:4509–4516. doi: 10.4049/jimmunol.1100911.
    1. Stoffel B., Bauer P., Nix M., Deres K., Stoffel W. Ceramide-independent CD28 and TCR signaling but reduced IL-2 secretion in T cells of acid sphingomyelinase-deficient mice. Eur. J. Immunol. 1998;28:874–880. doi: 10.1002/(SICI)1521-4141(199803)28:03<874::AID-IMMU874>;2-T.
    1. Herz J., Pardo J., Kashkar H., Schramm M., Kuzmenkina E., Bos E., Wiegmann K., Wallich R., Peters P.J., Herzig S., et al. Acid sphingomyelinase is a key regulator of cytotoxic granule secretion by primary T lymphocytes. Nat. Immunol. 2009;10:761–768. doi: 10.1038/ni.1757.
    1. Hollmann C., Wiese T., Dennstädt F., Fink J., Schneider-Schaulies J., Beyersdorf N. Translational Approaches Targeting Ceramide Generation From Sphingomyelin in T Cells to Modulate Immunity in Humans. Front. Immunol. 2019;10:2363. doi: 10.3389/fimmu.2019.02363.
    1. Mori L., Lepore M., De Libero G. The Immunology of CD1- and MR1-Restricted T Cells. Annu. Rev. Immunol. 2016;34:479–510. doi: 10.1146/annurev-immunol-032414-112008.
    1. Pereira C.S., Macedo M.F. CD1-Restricted T Cells at the Crossroad of Innate and Adaptive Immunity. J. Immunol. Res. 2016;2016:2876275. doi: 10.1155/2016/2876275.
    1. Pereira C.S., Sa-Miranda C., De Libero G., Mori L., Macedo M.F. Globotriaosylceramide inhibits iNKT-cell activation in a CD1d-dependent manner. Eur. J. Immunol. 2016;46:147–153. doi: 10.1002/eji.201545725.
    1. Nieuwenhuis E.E., Matsumoto T., Exley M., Schleipman R.A., Glickman J., Bailey D.T., Corazza N., Colgan S.P., Onderdonk A.B., Blumberg R.S. CD1d-dependent macrophage-mediated clearance of Pseudomonas aeruginosa from lung. Nat. Med. 2002;8:588–593. doi: 10.1038/nm0602-588.
    1. Kinjo Y., Illarionov P., Vela J.L., Pei B., Girardi E., Li X., Li Y., Imamura M., Kaneko Y., Okawara A., et al. Invariant natural killer T cells recognize glycolipids from pathogenic Gram-positive bacteria. Nat. Immunol. 2011;12:966–974. doi: 10.1038/ni.2096.
    1. Gulhan B., Ozcelik U., Gurakan F., Gucer S., Orhan D., Cinel G., Yalcin E., Ersoz D.D., Kiper N., Yuce A., et al. Different features of lung involvement in Niemann-Pick disease and Gaucher disease. Respir. Med. 2012;106:1278–1285. doi: 10.1016/j.rmed.2012.06.014.
    1. McGovern M.M., Wasserstein M.P., Giugliani R., Bembi B., Vanier M.T., Mengel E., Brodie S.E., Mendelson D., Skloot G., Desnick R.J., et al. A prospective, cross-sectional survey study of the natural history of Niemann-Pick disease type B. Pediatrics. 2008;122:e341–e349. doi: 10.1542/peds.2007-3016.
    1. Guillemot N., Troadec C., de Villemeur T.B., Clément A., Fauroux B. Lung disease in Niemann-Pick disease. Pediatr. Pulmonol. 2007;42:1207–1214. doi: 10.1002/ppul.20725.
    1. Mendelson D.S., Wasserstein M.P., Desnick R.J., Glass R., Simpson W., Skloot G., Vanier M., Bembi B., Giugliani R., Mengel E., et al. Type B Niemann-Pick disease: Findings at chest radiography, thin-section CT, and pulmonary function testing. Radiology. 2006;238:339–345. doi: 10.1148/radiol.2381041696.
    1. von Ranke F.M., Pereira Freitas H.M., Mançano A.D., Rodrigues R.S., Hochhegger B., Escuissato D., Araujo Neto C.A., da Silva T.K., Marchiori E. Pulmonary Involvement in Niemann-Pick Disease: A State-of-the-Art Review. Lung. 2016;194:511–518. doi: 10.1007/s00408-016-9893-0.
    1. 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. Invest. 2001;81:987–999. doi: 10.1038/labinvest.3780311.
    1. MacFadden-Murphy E., Roussel L., Martel G., Bérubé J., Rousseau S. Decreasing SMPD1 activity in BEAS-2B bronchial airway epithelial cells results in increased NRF2 activity, cytokine synthesis and neutrophil recruitment. Biochem. Biophys. Res. Commun. 2017;482:645–650. doi: 10.1016/j.bbrc.2016.11.087.
    1. Grassme H., Jendrossek V., Riehle A., von Kurthy G., Berger J., Schwarz H., Weller M., Kolesnick R., Gulbins E. Host defense against Pseudomonas aeruginosa requires ceramide-rich membrane rafts. Nat. Med. 2003;9:322–330. doi: 10.1038/nm823.
    1. Jbeily N., Suckert I., Gonnert F.A., Acht B., Bockmeyer C.L., Grossmann S.D., Blaess M.F., Lueth A., Deigner H.P., Bauer M., et al. Hyperresponsiveness of mice deficient in plasma-secreted sphingomyelinase reveals its pivotal role in early phase of host response. J. Lipid. Res. 2013;54:410–424. doi: 10.1194/jlr.M031625.
    1. Wasserstein M., Dionisi-Vici C., Giugliani R., Hwu W.L., Lidove O., Lukacs Z., Mengel E., Mistry P.K., Schuchman E.H., McGovern M. Recommendations for clinical monitoring of patients with acid sphingomyelinase deficiency (ASMD) Mol. Genet. Metab. 2019;126:98–105. doi: 10.1016/j.ymgme.2018.11.014.
    1. 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. 2016;18:34–40. doi: 10.1038/gim.2015.24.
    1. Wasserstein M.P., Jones S.A., Soran H., Diaz G.A., Lippa N., Thurberg B.L., Culm-Merdek K., Shamiyeh E., Inguilizian H., Cox G.F., et al. Successful within-patient dose escalation of olipudase alfa in acid sphingomyelinase deficiency. Mol. Genet. Metab. 2015;116:88–97. doi: 10.1016/j.ymgme.2015.05.013.
    1. Thurberg B.L., Wasserstein M.P., Jones S.A., Schiano T.D., Cox G.F., Puga A.C. Clearance of Hepatic Sphingomyelin by Olipudase Alfa Is Associated With Improvement in Lipid Profiles in Acid Sphingomyelinase Deficiency. Am. J. Surg. Pathol. 2016;40:1232–1242. doi: 10.1097/PAS.0000000000000659.
    1. Wasserstein M.P., Diaz G.A., Lachmann R.H., Jouvin M.H., Nandy I., Ji A.J., Puga A.C. Olipudase alfa for treatment of acid sphingomyelinase deficiency (ASMD): Safety and efficacy in adults treated for 30 months. J. Inherit. Metab. Dis. 2018;41:829–838. doi: 10.1007/s10545-017-0123-6.
    1. Thurberg B.L., Diaz G.A., Lachmann R.H., Schiano T., Wasserstein M.P., Ji A.J., Zaher A., Peterschmitt M.J. Long-term efficacy of olipudase alfa in adults with acid sphingomyelinase deficiency (ASMD): Further clearance of hepatic sphingomyelin is associated with additional improvements in pro- and anti-atherogenic lipid profiles after 42 months of treatment. Mol. Genet. Metab. 2020;131:245–252. doi: 10.1016/j.ymgme.2020.06.010.

Source: PubMed

Sponzoři a spolupracovníci

Zdravotní podmínky

Drogové intervence

3
Předplatit