A mouse model of harlequin ichthyosis delineates a key role for Abca12 in lipid homeostasis

PLoS Genetics

Volumn 4, Issue 9, 2008, Pages

  Smyth, Ian ^a,b   Hacking, Douglas F ^c,d   Hilton, Adrienne A ^c   Mukhamedova, Nigora ^e   Meikle, Peter J ^e   Ellis, Sarah ^f   Slattery, Keith ^c   Collinge, Janelle E ^c,g   De Graaf, Carolyn A ^c   Bahlo, Melanie ^d   Sviridov, Dmitri ^e   Kile, Benjamin T ^c   Hilton, Douglas J ^c  

^a MONASH UNIVERSITY   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^d ROYAL WOMEN'S HOSPITAL   (Australia)

^e BAKER IDI HEART AND DIABETES INSTITUTE   (Australia)

^f PETER MACCALLUM CANCER CENTRE   (Australia)

^g UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ABCA12 PROTEIN; SKIN LIPID; UNCLASSIFIED DRUG; ABCA12 PROTEIN, MOUSE; ETHYLNITROSOUREA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATHEROSCLEROSIS; CELL DIFFERENTIATION; CONTROLLED STUDY; FIBROBLAST; GENE MUTATION; HARLEQUIN ICHTHYOSIS; HISTOPATHOLOGY; HOMEOSTASIS; HYPERKERATOSIS; ICHTHYOSIS; IMMUNOHISTOCHEMISTRY; KERATINOCYTE; LAMELLAR BODY; LIPID METABOLISM; MOUSE; NONHUMAN; PHENOTYPE; SKIN WATER LOSS; TRANSMISSION ELECTRON MICROSCOPY; ANIMAL; C57BL MOUSE; DISEASE MODEL; EPIDERMIS; FEMALE; GENETICS; HUMAN; LAMELLAR ICHTHYOSIS; MALE; METABOLISM; MUTAGENESIS; PATHOPHYSIOLOGY; PRENATAL DEVELOPMENT; SKIN; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALIA;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL TRANSPORT; CELL DIFFERENTIATION; DISEASE MODELS, ANIMAL; EPIDERMIS; ETHYLNITROSOUREA; FEMALE; HOMEOSTASIS; HUMANS; ICHTHYOSIS, LAMELLAR; KERATINOCYTES; LIPID METABOLISM; MALE; MICE; MICE, INBRED C57BL; MUTAGENESIS; SKIN;

EID: 52949090042     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1000192     Document Type: Article

References (54)

1. Singh S, Bhura M, Maheshwari A, Kumar A, Singh CP, et al. (2001) Successful treatment of harlequin ichthyosis with acitretin. Int J Dermatol 40: 472-473.
2. Uitto J (2005) The gene family of ABC transporters-novel mutations, new phenotypes. Trends Mol Med 11: 341-343.
3. Elias P, Feingold KR, F M (2006) Epidermal lamellar body as a multifunctional secretory organelle; Elias P, Feingold KR, eds. New York: Taylor and Francis. 261-272 p.
4. Wertz PW, Downing DT (1987) Covalently bound omega-hydroxyacylsphingosine in the stratum corneum. Biochim Biophys Acta 917: 108-111.
5. Tybulewicz VL, Tremblay ML, LaMarca ME, Willemsen R, Stubblefield BK, et al. (1992) Animal model of Gaucher's disease from targeted disruption of the mouse glucocerebrosidase gene. Nature 357: 407-410.
6. Schmuth M, Man MQ, Weber F, Gao W, Feingold KR, et al. (2000) Permeability barrier disorder in Niemann-Pick disease: sphingomyelin-ceramide processing required for normal barrier homeostasis. J Invest Dermatol 115: 459-466.
7. Vielhaber G, Pfeiffer S, Brade L, Lindner B, Goldmann T, et al. (2001) Localization of ceramide and glucosylceramide in human epidermis by immunogold electron microscopy. J Invest Dermatol 117: 1126-1136.
8. Akiyama M, Sugiyama-Nakagiri Y, Sakai K, McMillan JR, Goto M, et al. (2005) Mutations in lipid transporter ABCA12 in harlequin ichthyosis and functional recovery by corrective gene transfer. J Clin Invest 115: 1777-1784.
9. Kelsell DP, Norgett EE, Unsworth H, Teh MT, Cullup T, et al. (2005) Mutations in ABCA12 underlie the severe congenital skin disease harlequin ichthyosis. Am J Hum Genet 76: 794-803.
10. Lefevre C, Audebert S, Jobard F, Bouadjar B, Lakhdar H, et al. (2003) Mutations in the transporter ABCA12 are associated with lamellar ichthyosis type 2. Hum Mol Genet 12: 2369-2378.
11. Sakai K, Akiyama M, Sugiyama-Nakagiri Y, McMillan JR, Sawamura D, et al. (2007) Localization of ABCA12 from Golgi apparatus to lamellar granules in human upper epidermal keratinocytes. Exp Dermatol 16: 920-926.
12. Akiyama M (2006) Pathomechanisms of harlequin ichthyosis and ABCA transporters in human diseases. Arch Dermatol 142: 914-918.
13. Bodzioch M, Orso E, Klucken J, Langmann T, Bottcher A, et al. (1999) The gene encoding ATP-binding cassette transporter 1 is mutated in Tangier disease. Nat Genet 22: 347-351.
14. Brooks-Wilson A, Marcil M, Clee SM, Zhang LH, Roomp K, et al. (1999) Mutations in ABC1 in Tangier disease and familial high-density lipoprotein deficiency. Nat Genet 22: 336-345.
15. Rust S, Rosier M, Funke H, Real J, Amoura Z, et al. (1999) Tangier disease is caused by mutations in the gene encoding ATP-binding cassette transporter 1. Nat Genet 22: 352-355.
16. Yanagi T, Akiyama M, Nishihara H, Sakai K, Nishie W, et al. (2008) Harlequin ichthyosis model mouse reveals alveolar collapse and severe fetal skin barrier defects. Hum Mol Genet.
17. Hardman MJ, Sisi P, Banbury DN, Byrne C (1998) Patterned acquisition of skin barrier function during development. Development 125: 1541-1552.
18. Dale BA, Holbrook KA, Fleckman P, Kimball JR, Brumbaugh S, et al. (1990) Heterogeneity in harlequin ichthyosis, an inborn error of epidermal keratinization: variable morphology and structural protein expression and a defect in lamellar granules. J Invest Dermatol 94: 6-18.
19. Yamanaka Y, Akiyama M, Sugiyama-Nakagiri Y, Sakai K, Goto M, et al. (2007) Expression of the keratinocyte lipid transporter ABCA12 in developing and reconstituted human epidermis. Am J Pathol 171: 43-52.
20. Hou SY, Mitra AK, White SH, Menon GK, Ghadially R, et al. (1991) Membrane structures in normal and essential fatty acid-deficient stratum corneum: characterization by ruthenium tetroxide staining and x-ray diffraction. J Invest Dermatol 96: 215-223.
21. Elias PM, Fartasch M, Crumrine D, Behne M, Uchida Y, et al. (2000) Origin of the corneocyte lipid envelope (CLE): observations in harlequin ichthyosis and cultured human keratinocytes. J Invest Dermatol 115: 765-769.
22. Buxman MM, Goodkin PE, Fahrenbach WH, Dimond RL (1979) Harlequin ichthyosis with epidermal lipid abnormality. Arch Dermatol 115: 189-193.
23. Fleck RM, Barnadas M, Schulz WW, Roberts LJ, Freeman RG (1989) Harlequin ichthyosis: an ultrastructural study. J Am Acad Dermatol 21: 999-1006.
24. Hashimoto K, De Dobbeleer G, Kanzaki T (1993) Electron microscopic studies of harlequin fetuses. Pediatr Dermatol 10: 214-223.
25. Milner ME, O'Guin WM, Holbrook KA, Dale BA (1992) Abnormal lamellar granules in harlequin ichthyosis. J Invest Dermatol 99: 824-829.
26. Akiyama M, Sakai K, Sugiyama-Nakagiri Y, Yamanaka Y, McMillan JR, et al. (2006) Compound heterozygous mutations including a de novo missense mutation in ABCA12 led to a case of harlequin ichthyosis with moderate clinical severity. J Invest Dermatol 126: 1518-1523.
27. Oram JF, Vaughan AM (2006) ATP-Binding cassette cholesterol transporters and cardiovascular disease. Circ Res 99: 1031-1043.
28. Jiang YJ, Lu B, Kim P, Paragh G, Schmitz G, et al. (2008) PPAR and LXR activators regulate ABCA12 expression in human keratinocytes. J Invest Dermatol 128: 104-109.
29. Sviridov D, Nestel PJ (2007) Genetic factors affecting HDL levels, structure, metabolism and function. Curr Opin Lipidol 18: 157-163.
30. Kile BT, Hilton DJ (2005) The art and design of genetic screens: mouse. Nat Rev Genet 6: 557-567.
31. Thomas AC, Cullup T, Norgett EE, Hill T, Barton S, et al. (2006) ABCA12 is the major harlequin ichthyosis gene. J Invest Dermatol 126: 2408-2413.
32. Hohl D, Huber M, Frenk E (1993) Analysis of the cornified cell envelope in lamellar ichthyosis. Arch Dermatol 129: 618-624.
33. Ishida-Yamamoto A, Iizuka H (1998) Structural organization of cornified cell envelopes and alterations in inherited skin disorders. Exp Dermatol 7: 1-10.
34. Albrecht C, Baynes K, Sardini A, Schepelmann S, Eden ER, et al. (2004) Two novel missense mutations in ABCA1 result in altered trafficking and cause severe autosomal recessive HDL deficiency. Biochim Biophys Acta 1689: 47-57.
35. Choi MY, Partridge AW, Daniels C, Du K, Lukacs GL, et al. (2005) Destabilization of the transmembrane domain induces misfolding in a phenotypic mutant of cystic fibrosis transmembrane conductance regulator. J Biol Chem 280: 4968-4974.
36. Gong X, Burbridge SM, Cowley EA, Linsdell P (2002) Molecular determinants of Au(CN)(2)(-) binding and permeability within the cystic fibrosis transmembrane conductance regulator Cl(-) channel pore. J Physiol 540: 39-47.
37. Rassner U, Feingold KR, Crumrine DA, Elias PM (1999) Coordinate assembly of lipids and enzyme proteins into epidermal lamellar bodies. Tissue Cell 31: 489-498.
38. Elias PM, Williams ML, Holleran WM, Jiang YJ, Schmuth M (2008) Pathogenesis of permeability barrier abnormalities in the ichthyoses: inherited disorders of lipid metabolism. J Lipid Res 49: 697-714.
39. Man MQ, Feingold KR, Elias PM (1993) Exogenous lipids influence permeability barrier recovery in acetone-treated murine skin. Arch Dermatol 129: 728-738.
40. Harris IR, Farrell AM, Grunfeld C, Holleran WM, Elias PM, et al. (1997) Permeability barrier disruption coordinately regulates mRNA levels for key enzymes of cholesterol, fatty acid, and ceramide synthesis in the epidermis. J Invest Dermatol 109: 783-787.
41. Holleran WM, Feingold KR, Man MQ, Gao WN, Lee JM, et al. (1991) Regulation of epidermal sphingolipid synthesis by permeability barrier function. J Lipid Res 32: 1151-1158.
42. Oram JF, Lawn RM (2001) ABCA1. The gatekeeper for eliminating excess tissue cholesterol. J Lipid Res 42: 1173-1179.
43. Cavelier C, Lorenzi I, Rohrer L, von Eckardstein A (2006) Lipid efflux by the ATP-binding cassette transporters ABCA1 and ABCG1. Biochim Biophys Acta 1761: 655-666.
44. Denis M, Haidar B, Marcil M, Bouvier M, Krimbou L, et al. (2004) Characterization of oligomeric human ATP binding cassette transporter A1. Potential implications for determining the structure of nascent high density lipoprotein particles. J Biol Chem 279: 41529-41536.
45. Singaraja RR, Brunham LR, Visscher H, Kastelein JJ, Hayden MR (2003) Efflux and atherosclerosis: the clinical and biochemical impact of variations in the ABCA1 gene. Arterioscler Thromb Vasc Biol 23: 1322-1332.
46. Dietrich W, Katz H, Lincoln SE, Shin HS, Friedman J, et al. (1992) A genetic map of the mouse suitable for typing intraspecific crosses. Genetics 131: 423-447.
47. Maatta A, DiColandrea T, Groot K, Watt FM (2001) Gene targeting of envoplakin, a cytoskeletal linker protein and precursor of the epidermal cornified envelope. Mol Cell Biol 21: 7047-7053.
48. Sybert VP, Dale BA, Holbrook KA (1985) Ichthyosis vulgaris: identification of a defect in synthesis of filaggrin correlated with an absence of keratohyaline granules. J Invest Dermatol 84: 191-194.
49. Talreja P, Kleene NK, Pickens WL, Wang TF, Kasting GB (2001) Visualization of the lipid barrier and measurement of lipid pathlength in human stratum corneum. AAPS PharmSci 3: E13.
50. Folch J, Lees M, Sloane Stanley GH (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226: 497-509.
51. Cavelier LB, Qiu Y, Bielicki JK, Afzal V, Cheng JF, et al. (2001) Regulation and activity of the human ABCA1 gene in transgenic mice. J Biol Chem 276: 18046-18051.
52. Sviridov D, Pyle LE, Fidge N (1996) Efflux of cellular cholesterol and phospholipid to apolipoprotein A-I mutants. J Biol Chem 271: 33277-33283.
53. Basu SK, Goldstein JL, Anderson GW, Brown MS (1976) Degradation of cationized low density lipoprotein and regulation of cholesterol metabolism in homozygous familial hypercholesterolemia fibroblasts. Proc Natl Acad Sci U S A 73: 3178-3182.
54. Sviridov D, Pyle LE, Jauhiainen M, Ehnholm C, Fidge NH (2000) Deletion of the propeptide of apolipoprotein A-I reduces protein expression but stimulates effective conversion of prebeta-high density lipoprotein to alpha-high density lipoprotein. J Lipid Res 41: 1872-1882.