Imaging Mass Spectrometry Visualizes Ceramides and the Pathogenesis of Dorfman-Chanarin Syndrome Due to Ceramide Metabolic Abnormality in the Skin

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Goto Inoue, Naoko ^a   Hayasaka, Takahiro ^a   Zaima, Nobuhiro ^b   Nakajima, Kimiko ^c   Holleran, Walter M ^d   Sano, Shigetoshi ^c   Uchida, Yoshikazu ^d   Setou, Mitsutoshi ^a  

^a HAMAMATSU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b KINKI UNIVERSITY   (Japan)

^c KOCHI MEDICAL SCHOOL   (Japan)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CERAMIDE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL LABELING; CLINICAL ASSESSMENT; CONTROLLED STUDY; DISORDERS OF LIPID METABOLISM; DORFMAN CHANARIN SYNDROME; HUMAN; HUMAN TISSUE; ICHTHYOSIS; IMAGE ANALYSIS; IMAGING MASS SPECTROMETRY; LIPID ANALYSIS; LIPID COMPOSITION; LIPIDOSIS; MASS SPECTROMETRY; MOUSE; NONHUMAN; PATHOGENESIS; PERMEABILITY BARRIER; PROTEIN LOCALIZATION; SKIN FLAP SURVIVAL; SKIN WATER LOSS; STRATUM CORNEUM;

ANIMALS; CERAMIDES; DIAGNOSTIC IMAGING; HUMANS; ICHTHYOSIFORM ERYTHRODERMA, CONGENITAL; IONS; LIPID METABOLISM, INBORN ERRORS; LIPIDS; MASS SPECTROMETRY; MICE; MOLECULAR IMAGING; MUSCULAR DISEASES; PHOSPHATIDYLCHOLINES; PHOSPHORIC MONOESTER HYDROLASES; SKIN;

MAMMALIA;

EID: 84869205471     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0049519     Document Type: Article

References (49)

1. Shimma S, Sugiura Y, Hayasaka T, Zaima N, Matsumoto M, et al. (2008) Mass imaging and identification of biomolecules with MALDI-QIT-TOF-based system. Anal Chem. 80: 878-885.
2. Hayasaka T, Goto-Inoue N, Sugiura Y, Zaima N, Nakanishi H, et al. (2008) Matrix-assisted laser desorption/ionization quadrupole ion trap time-of-flight (MALDI-QIT-TOF)-based imaging mass spectrometry reveals a layered distribution of phospholipid molecular species in the mouse retina. Rapid Commun Mass Spectrom. 22: 3415-3426.
3. Cornett DS, Reyzer ML, Chaurand P, Caprioli RM, (2007) MALDI imaging mass spectrometry: molecular snapshots of biochemical systems. Nat Methods. 4: 828-833.
4. Yao I, Takagi H, Ageta H, Kahyo T, Sato S, et al. (2007) SCRAPPER-dependent ubiquitination of active zone protein RIM1 regulates synaptic vesicle release. Cell. 130: 943-957.
5. Morita Y, Ikegami K, Goto-Inoue N, Hayasaka T, Zaima N, et al. (2010) Imaging mass spectrometry of gastric carcinoma in formalin-fixed paraffin-embedded tissue microarray. Cancer Sci. 101: 267-273.
6. Hayasaka T, Goto-Inoue N, Zaima N, Kimura Y, Setou M, (2009) Organ-specific distributions of lysophosphatidylcholine and triacylglycerol in mouse embryo. Lipids. 44: 837-848.
7. Goto-Inoue N, Setou M, Zaima N, (2010) Visualization of spatial distribution of gamma-aminobutyric acid in eggplant (Solanum melongena) by matrix-assisted laser desorption/ionization imaging mass spectrometry. Anal Sci. 26: 821-825.
8. Zaima N, Hayasaka T, Goto-Inoue N, Setou M, (2009) Imaging of metabolites by MALDI mass spectrometry. J Oleo Sci. 58: 415-419.
9. Sugiura Y, Konishi Y, Zaima N, Kajihara S, Nakanishi H, et al. (2009) Visualization of the cell-selective distribution of PUFA-containing phosphatidylcholines in mouse brain by imaging mass spectrometry. J Lipid Res. 50: 1776-1788.
10. Spengler B, Hubert M, (2002) Scanning microprobe matrix-assisted laser desorption ionization (SMALDI) mass spectrometry: instrumentation for sub-micrometer resolved LDI and MALDI surface analysis. J Am Soc Mass Spectrom. 13: 735-748.
11. Yang J, Caprioli RM, (2011) Matrix sublimation/recrystallization for imaging proteins by mass spectrometry at high spatial resolution. Anal Chem. 83: 5728-5734.
12. Spraggins JM, Caprioli RM, (2011) High-speed maldi-tof imaging mass spectrometry: rapid ion image acquisition and considerations for next generation instrumentation. J Am Soc Mass Spectrom. 22: 1022-1031.
13. Hankin JA, Farias SE, Barkley RM, Heidenreich K, Frey LC, et al. (2011) MALDI Mass Spectrometric Imaging of Lipids in Rat Brain Injury Models. J Am Soc Mass Spectrom. 22: 1014-1021.
14. Deutskens F, Yang J, Caprioli RM, (2011) High spatial resolution imaging mass spectrometry and classical histology on a single tissue section. J Mass Spectrom. 46: 568-571.
15. Harada T, Yuba-Kubo A, Sugiura Y, Zaima N, Hayasaka T, et al. (2009) Visualization of volatile substances in different organelles with an atmospheric-pressure mass microscope. Anal Chem. 81: 9153-9157.
16. Pettus BJ, Bielawska A, Subramanian P, Wijesinghe DS, Maceyka M, et al. (2004) Ceramide 1-phosphate is a direct activator of cytosolic phospholipase A2. J Biol Chem. 279: 11320-11326.
17. Ponec M, Weerheim A, Kempenaar J, Mommaas AM, Nugteren DH, (1988) Lipid composition of cultured human keratinocytes in relation to their differentiation. J Lipid Res. 29: 949-961.
18. Wertz PW, Downing DT, (1982) Glycolipids in mammalian epidermis: structure and function in the water barrier. Science. 217: 1261-1262.
19. Holleran WM, Takagi Y, Menon GK, Legler G, Feingold KR, et al. (1993) Processing of Epidermal Glucosylceramides Is Required for Optimal Mammalian Cutaneous Permeability Barrier Function. J Clin Invest. 91: 1656-1664.
20. Holleran WM, Ginns EI, Menon GK, Grundmann JU, Fartasch M, et al. (1994) Consequences of Beta-Glucocerebrosidase Deficiency in Epidermis- Ultrastructure and Permeability Barrier Alterations in Gaucher Disease. J Clin Invest. 93: 1756-1764.
21. Elias PM, Menon GK, (1991) Structural and lipid biochemical correlates of the epidermal permeability barrier. Adv Lipid Res. 24: 1-26.
22. 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.
23. Jensen JM, Schutze S, Forl M, Kronke M, Proksch E, (1999) Roles for tumor necrosis factor receptor p55 and sphingomyelinase in repairing the cutaneous permeability barrier. J Clin Invest. 104: 1761-1770.
24. Bouwstra JA, Gooris GS, Dubbelaar FE, Weerheim AM, Ijzerman AP, et al. (1998) Role of ceramide 1 in the molecular organization of the stratum corneum lipids. J Lipid Res. 39: 186-196.
25. Paige DG, Morse-Fisher N, Harper JI, (1994) Quantification of stratum corneum ceramides and lipid envelope ceramides in the hereditary ichthyoses. Br J Dermatol. 131: 23-27.
26. Motta S, Monti M, Sesana S, Caputo R, Carelli S, et al. (1993) Ceramide composition of the psoriatic scale. Biochim Biophys Acta. 1182: 147-151.
27. Imokawa G, Abe A, Jin K, Higaki Y, Kawashima M, et al. (1991) Decreased level of ceramides in stratum corneum of atopic dermatitis: an etiologic factor in atopic dry skin? J Invest Dermatol. 96: 523-526.
28. Bleck O, Abeck D, Ring J, Hoppe U, Vietzke JP, et al. (1999) Two ceramide subfractions detectable in Cer(AS) position by HPTLC in skin surface lipids of non-lesional skin of atopic eczema. Journal of Investigative Dermatology. 113: 894-900.
29. Preiss JE, Loomis CR, Bell RM, Niedel JE, (1987) Quantitative measurement of sn-1,2-diacylglycerols. Methods Enzymol. 141: 294-300.
30. Gorska M, Dobrzyn A, Zendzian-Piotrowska M, Namiot Z, (2002) Concentration and composition of free ceramides in human plasma. Horm Metab Res. 34: 466-468.
31. Yano M, Kishida E, Muneyuki Y, Masuzawa Y, (1998) Quantitative analysis of ceramide molecular species by high performance liquid chromatography. J Lipid Res. 39: 2091-2098.
32. Dobrzyn A, Gorski J, (2002) Ceramides and sphingomyelins in skeletal muscles of the rat: content and composition. Effect of prolonged exercise. Am J Physiol Endocrinol Metab. 282: E277-285.
33. Kasumov T, Huang H, Chung YM, Zhang R, McCullough AJ, et al. (2010) Quantification of ceramide species in biological samples by liquid chromatography electrospray ionization tandem mass spectrometry. Anal Biochem.
34. Farwanah H, Pierstorff B, Schmelzer CE, Raith K, Neubert RH, et al. (2007) Separation and mass spectrometric characterization of covalently bound skin ceramides using LC/APCI-MS and Nano-ESI-MS/MS. J Chromatogr B Analyt Technol Biomed Life Sci. 852: 562-570.
35. Tserng KY, Griffin R, (2003) Quantitation and molecular species determination of diacylglycerols, phosphatidylcholines, ceramides, and sphingomyelins with gas chromatography. Anal Biochem. 323: 84-93.
36. Hart PJ, Francese S, Claude E, Woodroofe MN, Clench MR, (2011) MALDI-MS imaging of lipids in ex vivo human skin. Anal Bioanal Chem. 401: 115-125.
37. Uchida Y, Visireddy V, Gooris G, Alderson NI, Brown J, et al. (2008) ELOVL4 is required to generate epidermal-unique omega-O-(acyl)ceramides that form two structures critical for the epidermal permeability barrier. Journal of Investigative Dermatology. 128: S92-S92.
38. 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.
39. Munoz-Garcia A, Ro J, Brown JC, Williams JB, (2006) Identification of complex mixtures of sphingolipids in the stratum corneum by reversed-phase high-performance liquid chromatography and atmospheric pressure photospray ionization mass spectrometry. J Chromatogr A. 1133: 58-68.
40. Holleran WM, Takagi Y, Uchida Y, (2006) Epidermal sphingolipids: metabolism, function, and roles in skin disorders. Febs Lett. 580: 5456-5466.
41. Kobayashi Y, Hayasaka T, Setou M, Itoh H, Kanayama N, (2010) Comparison of phospholipid molecular species between terminal and stem villi of human term placenta by imaging mass spectrometry. Placenta. 31: 245-248.
42. Nakamura K, Suzuki Y, Goto-Inoue N, Yoshida-Noro C, Suzuki A, (2006) Structural characterization of neutral glycosphingolipids by thin-layer chromatography coupled to matrix-assisted laser desorption/ionization quadrupole ion trap time-of-flight MS/MS. Anal Chem. 78: 5736-5743.
43. Zaima N, Goto-Inoue N, Hayasaka T, Setou M, (2010) Application of imaging mass spectrometry for the analysis of Oryza sativa rice. Rapid Commun Mass Spectrom. 24: 2723-2729.
44. Uchida Y, Cho Y, Moradian S, Kim J, Nakajima K, et al. (2010) Neutral lipid storage leads to acylceramide deficiency, likely contributing to the pathogenesis of Dorfman-Chanarin syndrome. J Invest Dermatol. 130: 2497-2499.
45. Laiko VV, Baldwin MA, Burlingame AL, (2000) Atmospheric pressure matrix-assisted laser desorption/ionization mass spectrometry. Anal Chem. 72: 652-657.
46. Vietzke JP, Brandt O, Abeck D, Rapp C, Strassner M, et al. (2001) Comparative investigation of human stratum corneum ceramides. Lipids. 36: 299-304.
47. Hamanaka S, Nakazawa S, Yamanaka M, Uchida Y, Otsuka F, (2005) Glucosylceramide accumulates preferentially in lamellar bodies in differentiated keratinocytes. Br J Dermatol. 152: 426-434.
48. Radner FP, Streith IE, Schoiswohl G, Schweiger M, Kumari M, et al. (2010) Growth retardation, impaired triacylglycerol catabolism, hepatic steatosis, and lethal skin barrier defect in mice lacking comparative gene identification-58 (CGI-58). J Biol Chem. 285: 7300-7311.
49. Demerjian M, Crumrine DA, Milstone LM, Williams ML, Elias PM, (2006) Barrier dysfunction and pathogenesis of neutral lipid storage disease with ichthyosis (Chanarin-Dorfman syndrome). J Invest Dermatol. 126: 2032-2038.