Systemic ceramide accumulation leads to severe and varied pathological consequences

EMBO Molecular Medicine

Volumn 5, Issue 6, 2013, Pages 827-842

  Alayoubi, Abdulfatah M ^a,b   Wang, James C M ^c   Au, Bryan C Y ^c   Carpentier, Stéphane ^d   Garcia, Virginie ^d   Dworski, Shaalee ^a   El Ghamrasni, Samah ^c   Kirouac, Kevin N ^c   Exertier, Mathilde J ^c   Xiong, Zi Jian ^a   Privé, Gilbert G ^a,c   Simonaro, Calogera M ^e   Casas, Josefina ^f   Fabrias, Gemma ^f   Schuchman, Edward H ^e   Turner, Patricia V ^g   Hakem, Razqallah ^a,c   Levade, Thierry ^d,h   Medin, Jeffrey A ^a,c  

^a UNIVERSITY OF TORONTO   (Canada)

^b TAIBAH UNIVERSITY   (Saudi Arabia)

^c UNIVERSITY HEALTH NETWORK   (Canada)

^d CANCER RESEARCH CENTER OF TOULOUSE   (France)

^e MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^f INSTITUTE OF ADVANCED CHEMISTRY OF CATALONIA IQAC CSIC   (Spain)

^g UNIVERSITY OF GUELPH   (Canada)

^h TOULOUSE UNIVERSITY HOSPITAL   (France)

Author keywords

Acid ceramidase; Farber disease; Lysosomal storage disorders; MCP 1

Indexed keywords

ACID CERAMIDASE; CERAMIDE; LENTIVIRUS VECTOR; LIPID; LIPOSOME; LYSOSOME ENZYME; MONOCYTE CHEMOTACTIC PROTEIN 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN TISSUE; CELL INFILTRATION; CELL SURVIVAL; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE SEVERITY; EMBRYO; ENZYME ACTIVITY; ENZYME DEFICIENCY; EOSINOPHIL COUNT; FARBER DISEASE; FEMALE; GENE MUTATION; GENE REPLACEMENT THERAPY; GENE TARGETING; GROWTH RETARDATION; HISTIOCYTE; HISTOPATHOLOGY; HOMOZYGOSITY; LEUKOCYTE; LIFESPAN; LIPID METABOLISM; LIVER; MACROPHAGE; MALE; MONOCYTE; MOUSE; NEUTROPHIL COUNT; NONHUMAN; OVARY; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SINGLE NUCLEOTIDE POLYMORPHISM; SPLEEN; THYMUS;

ACID CERAMIDASE; ANIMALS; CELLS, CULTURED; CERAMIDES; CHEMOKINE CCL2; DISEASE MODELS, ANIMAL; EMBRYONIC STEM CELLS; FARBER LIPOGRANULOMATOSIS; FEMALE; GENE KNOCK-IN TECHNIQUES; GENETIC VECTORS; HOMOZYGOTE; HUMANS; LENTIVIRUS; MACROPHAGES; MICE; MUTATION; PHENOTYPE;

EID: 84878688969     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.1002/emmm.201202301     Document Type: Article

References (50)

1. Amarnath S, Mangus CW, Wang JC, Wei F, He A, Kapoor V, Foley JE, Massey PR, Felizardo TC, Riley JL, et al (2011) The PDL1-PD1 axis converts human TH1 cells into regulatory T cells. Sci Transl Med 3: 111ra120
2. Antonarakis SE, Valle D, Moser HW, Moser A, Qualman SJ, Zinkham WH (1984) Phenotypic variability in siblings with Farber disease. J Pediatr 104: 406-409
3. Bar J, Linke T, Ferlinz K, Neumann U, Schuchman EH, Sandhoff K (2001) Molecular analysis of acid ceramidase deficiency in patients with Farber disease. Hum Mutat 17: 199-209
4. Beckham TH, Lu P, Cheng JC, Zhao D, Turner LS, Zhang X, Hoffman S, Armeson KE, Liu A, Marrison T, et al (2012) Acid ceramidase-mediated production of sphingosine 1-phosphate promotes prostate cancer invasion through upregulation of cathepsin B. Int J Cancer 131: 2034-2043
5. Bielawska A, Perry DK, Hannun YA (2001) Determination of ceramides and diglycerides by the diglyceride kinase assay. Anal Biochem 298: 141-150
6. Bokhove M, Yoshida H, Hensgens CM, van der Laan JM, Sutherland JD, Dijkstra BW (2010) Structures of an isopenicillin N converting Ntn-hydrolase reveal different catalytic roles for the active site residues of precursor and mature enzyme. Structure 18: 301-308
7. Boring L, Gosling J, Cleary M, Charo IF (1998) Decreased lesion formation in CCR2-/- mice reveals a role for chemokines in the initiation of atherosclerosis. Nature 394: 894-897
8. Burek C, Roth J, Koch HG, Harzer K, Los M, Schulze-Osthoff K (2001) The role of ceramide in receptor- and stress-induced apoptosis studied in acidic ceramidase-deficient Farber disease cells. Oncogene 20: 6493-6502
9. Cvitanovic-Sojat L, Gjergja Juraski R, Sabourdy F, Fensom AH, Fumic K, Paschke E, Levade T (2011) Farber lipogranulomatosis type 1 - late presentation and early death in a Croatian boy with a novel homozygous ASAH1 mutation. Eur J Paediatr Neurol 15: 171-173
10. Ehlert K, Frosch M, Fehse N, Zander A, Roth J, Vormoor J (2007) Farber disease: clinical presentation, pathogenesis and a new approach to treatment. Pediatr Rheumatol Online J 5: 15-21
11. Ehlert K, Roth J, Frosch M, Fehse N, Zander N, Vormoor J (2006) Farber's disease without central nervous system involvement: bone-marrow transplantation provides a promising new approach. Ann Rheum Dis 65: 1665-1666
12. Eliyahu E, Park JH, Shtraizent N, He X, Schuchman EH (2007) Acid ceramidase is a novel factor required for early embryo survival. FASEB J 21: 1403-1409
13. Eliyahu E, Shtraizent N, Shalgi R, Schuchman EH (2012) Construction of conditional acid ceramidase knockout mice and in vivo effects on oocyte development and fertility. Cell Physiol Biochem 30: 735-748
14. Fuentes ME, Durham SK, Swerdel MR, Lewin AC, Barton DS, Megill JR, Bravo R, Lira SA (1995) Controlled recruitment of monocytes and macrophages to specific organs through transgenic expression of monocyte chemoattractant protein-1. J Immunol 155: 5769-5776
15. Haraoka G, Muraoka M, Yoshioka N, Wakami S, Hayashi I (1997) First case of surgical treatment of Farber's disease. Ann Plast Surg 39: 405-410
16. Kanamori H, Matsubara T, Mima A, Sumi E, Nagai K, Takahashi T, Abe H, Iehara N, Fukatsu A, Okamoto H, et al (2007) Inhibition of MCP-1/CCR2 pathway ameliorates the development of diabetic nephropathy. Biochem Biophys Res Commun 360: 772-777
17. Kanda H, Tateya S, Tamori Y, Kotani K, Hiasa K, Kitazawa R, Kitazawa S, Miyachi H, Maeda S, Egashira K, et al (2006) MCP-1 contributes to macrophage infiltration into adipose tissue, insulin resistance, and hepatic steatosis in obesity. J Clin Invest 116: 1494-1505
18. Kolesnick R (2002) The therapeutic potential of modulating the ceramide/sphingomyelin pathway. J Clin Invest 110: 3-8
19. Levade T, Leruth M, Graber D, Moisand A, Vermeersch S, Salvayre R, Courtoy PJ (1996) In situ assay of acid sphingomyelinase and ceramidase based on LDL-mediated lysosomal targeting of ceramide-labeled sphingomyelin. J Lipid Res 37: 2525-2538
20. Levade T, Moser HW, Fensom AH, Harzer K, Moser AB, Salvayre R (1995) Neurodegenerative course in ceramidase deficiency (Farber disease) correlates with the residual lysosomal ceramide turnover in cultured living patient cells. J Neurol Sci 134: 108-114
21. Levade T, Sandhoff K, Schulze H, Medin JA (2009) Acid ceramidase deficiency: Farber lipogranulomatosis. In Scriver's OMMBID (Online Metabolic and Molecular Bases of Inherited Disease), Valle D, Beaudet AL, Vogelstein B, Kinzler KW, Antonarakis SE, Ballabio A (eds), New York: McGraw-Hill
22. Li CM, Park JH, He X, Levy B, Chen F, Arai K, Adler DA, Disteche CM, Koch J, Sandhoff K, et al (1999) The human acid ceramidase gene (ASAH): structure, chromosomal location, mutation analysis, and expression. Genomics 62: 223-231
23. Li CM, Park JH, Simonaro CM, He X, Gordon RE, Friedman AH, Ehleiter D, Paris F, Manova K, Hepbildikler S, et al (2002) Insertional mutagenesis of the mouse acid ceramidase gene leads to early embryonic lethality in homozygotes and progressive lipid storage disease in heterozygotes. Genomics 79: 218-224
24. Loughran TP, Wang HG (2011) Editorial [hot topic: Therapeutic targeting of the sphingolipid "biostat" in hematologic malignancies (guest editors: Thomas P. Loughran and Hong-Gang Wang). Anticancer Agents Med Chem 11: 780-781
25. Lucki NC, Sewer MB (2011) Genistein stimulates MCF-7 breast cancer cell growth by inducing acid ceramidase (ASAH1) gene expression. J Biol Chem 286: 19399-19409
26. Maceyka M, Harikumar KB, Milstien S, Spiegel S (2012) Sphingosine-1-phosphate signaling and its role in disease. Trends Cell Biol 22: 50-60
27. Medin JA, Takenaka T, Carpentier S, Garcia V, Basile JP, Segui B, Andrieu-Abadie N, Auge N, Salvayre R, Levade T (1999) Retrovirus-mediated correction of the metabolic defect in cultured Farber disease cells. Hum Gene Ther 10: 1321-1329
28. Mitsutake S, Date T, Yokota H, Sugiura M, Kohama T, Igarashi Y (2012) Ceramide kinase deficiency improves diet-induced obesity and insulin resistance. FEBS Lett 586: 1300-1305
29. Moser HW, Moser AB, Chen WW, Schram AW (1989) Ceramidase deficiency: Farber lipogranulomatosis, In: The Metabolic Basis of Inherited Disease, Vol. II, 6th edition, Scriver CR, Beaudet AL, Sly WS, Valle D (eds) pp. 1645-1654 New York: McGraw-Hill
30. Munoz-Olaya JM, Matabosch X, Bedia C, Egido-Gabas M, Casas J, Llebaria A, Delgado A, Fabrias G (2008) Synthesis and biological activity of a novel inhibitor of dihydroceramide desaturase. ChemMedChem 3: 946-953
31. Nagy A, Gertsensten M, Vintersten K, Behringer R (2003) Manipulating the Mouse Embryo; A Laboratory manual, 3rd edition, New York: Cold Spring Harbor Press, Cold Spring Harbor
32. Ogretmen B, Hannun YA (2004) Biologically active sphingolipids in cancer pathogenesis and treatment. Nat Rev Cancer 4: 604-616
33. Park JH, Schuchman EH (2006) Acid ceramidase and human disease. Biochim Biophys Acta 1758: 2133-2138
34. Pellissier JF, Berard-Badier M, Pinsard N (1986) Farber's disease in two siblings, sural nerve and subcutaneous biopsies by light and electron microscopy. Acta Neuropathol 72: 178-188
35. Popovic K, Prive GG (2008) Structures of the human ceramide activator protein saposin D. Acta Crystallogr D Biol Crystallogr 64: 589-594
36. Qualman SJ, Moser HW, Valle D, Moser AE, Antonarakis SE, Boitnott JK, Zinkham WH (1987) Farber disease: pathologic diagnosis in sibs with phenotypic variability. Am J Med Genet 3: 233-241
37. Ramsubir S, Nonaka T, Girbes CB, Carpentier S, Levade T, Medin JA (2008) In vivo delivery of human acid ceramidase via cord blood transplantation and direct injection of lentivirus as novel treatment approaches for Farber disease. Mol Genet Metab 95: 133-141
38. Rutledge BJ, Rayburn H, Rosenberg R, North RJ, Gladue RP, Corless CL, Rollins BJ (1995) High level monocyte chemoattractant protein-1 expression in transgenic mice increases their susceptibility to intracellular pathogens. J Immunol 155: 4838-4843
39. Samad F, Hester KD, Yang G, Hannun YA, Bielawski J (2006) Altered adipose and plasma sphingolipid metabolism in obesity: a potential mechanism for cardiovascular and metabolic risk. Diabetes 55: 2579-2587
40. Sands MS, Barker JE (1999) Percutaneous intravenous injection in neonatal mice. Lab Anim Sci 49: 328-330
41. Shtraizent N, Eliyahu E, Park JH, He X, Shalgi R, Schuchman EH (2008) Autoproteolytic cleavage and activation of human acid ceramidase. J Biol Chem 283: 11253-11259
42. Sugita M, Dulaney JT, Moser HW (1972) Ceramidase deficiency in Farber's disease (lipogranulomatosis). Science 178: 1100-1102
43. Theunissen JW, Petrini JH (2006) Methods for studying the cellular response to DNA damage: influence of the Mre11 complex on chromosome metabolism. Methods Enzymol 409: 251-284
44. Walia JS, Neschadim A, Lopez-Perez O, Alayoubi A, Fan X, Carpentier S, Madden M, Lee CJ, Cheung F, Jaffray DA, et al (2011) Autologous transplantation of lentivector/acid ceramidase-transduced hematopoietic cells in nonhuman primates. Hum Gene Ther 22: 679-687
45. Yang G, Badeanlou L, Bielawski J, Roberts AJ, Hannun YA, Samad F (2009) Central role of ceramide biosynthesis in body weight regulation, energy metabolism, and the metabolic syndrome. Am J Physiol Endocrinol Metab 297: E211- E224
46. Yeager AM, Uhas KA, Coles CD, Davis PC, Krause WL, Moser HW (2000) Bone marrow transplantation for infantile ceramidase deficiency (Farber disease). Bone Marrow Transplant 26: 357-363
47. Yoshimitsu M, Sato T, Tao K, Walia JS, Rasaiah VI, Sleep GT, Murray GJ, Poeppl AG, Underwood J, West L, et al (2004) Bioluminescent imaging of a marking transgene and correction of Fabry mice by neonatal injection of recombinant lentiviral vectors. Proc Natl Acad Sci USA 101: 16909-16914
48. Zarbin MA, Green WR, Moser HW, Morton SJ (1985) Farber's disease. Light and electron microscopic study of the eye. Arch Ophthalmol 103: 73-80
49. Zhang Y (2008) I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 9: 40-47
50. Zhang Z, Mandal AK, Mital A, Popescu N, Zimonjic D, Moser A, Moser H, Mukherjee AB (2000) Human acid ceramidase gene: novel mutations in Farber disease. Mol Genet Metab 70: 301-309