Inactivation of ether lipid biosynthesis causes male infertility, defects in eye development and optic nerve hypoplasia in mice

Human Molecular Genetics

Volumn 12, Issue 15, 2003, Pages 1881-1895

  Rodemer, Claus ^a   Thai, Thanh Phuong ^b   Brugger, Britta ^a   Kaercher, Thomas ^c   Werner, Hauke ^d   Nave, Klaus Armin ^e   Wieland, Felix ^a   Gorgas, Karin ^a   Just, Wilhelm W ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^c KLINIKUM LUDWIGSHAFEN   (Germany)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACYLTRANSFERASE; CHOLESTEROL; CONNEXIN 43; CONTACTIN; DIHYDROXYACETONE PHOSPHATE ACYLTRANSFERASE; DOCOSAHEXAENOIC ACID; ETHER LIPID; FLOTILLIN 1; GAP JUNCTION PROTEIN; GLYCERONE PHOSPHATE O ACYLTRANSFERASE; GLYCERONE-PHOSPHATE O-ACYLTRANSFERASE; MEMBRANE PROTEIN; MYELIN; PLASMALOGEN; PRIMER DNA; UNCLASSIFIED DRUG; UNSATURATED FATTY ACID;

ANIMAL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; BIOSYNTHESIS; BRAIN; CATARACT; CELL COMPARTMENTALIZATION; CELL MEMBRANE; CHONDRODYSPLASIA PUNCTATA; COMPARATIVE STUDY; CONTROLLED STUDY; DISEASE MODEL; DOWN REGULATION; EMBRYO CELL; EYE MALFORMATION; FEMALE; FIBROBLAST; FLUORESCENT ANTIBODY TECHNIQUE; GENE DISRUPTION; GENE INACTIVATION; GENE SILENCING; GENE TARGETING; GENETIC IDENTIFICATION; GENETIC MARKER; GENETICS; HISTOLOGY; HUMAN; LENS; LIPID BRAIN LEVEL; LIPOGENESIS; MALE; MALE INFERTILITY; MASS SPECTROMETRY; METABOLISM; MOUSE; MOUSE MUTANT; NONHUMAN; OPTIC NERVE DISEASE; OPTIC NERVE HYPOPLASIA; PATHOGENESIS; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN FUNCTION; REVIEW; SPERMATOGENESIS;

ACYLTRANSFERASES; ANIMALS; BRAIN; CHONDRODYSPLASIA PUNCTATA, RHIZOMELIC; CONNEXIN 43; DISEASE MODELS, ANIMAL; DNA PRIMERS; DOCOSAHEXAENOIC ACIDS; FLUORESCENT ANTIBODY TECHNIQUE; GENE SILENCING; HISTOLOGICAL TECHNIQUES; HUMANS; INFERTILITY, MALE; MALE; MASS SPECTROMETRY; MEMBRANE MICRODOMAINS; MICE; OPTIC NERVE DISEASES; PLASMALOGENS; POLYMERASE CHAIN REACTION;

ANIMALIA; MAMMALIA;

EID: 0042131525     PISSN: 09646906     EISSN: None     Source Type: Journal    
DOI: 10.1093/hmg/ddg191     Document Type: Review

References (79)

1. Nagan, N. and Zoeller, R.A. (2001) Plasmalogens: biosynthesis and functions. Prog. Lipid Res., 40, 199-229.
2. Diagne, A., Fauvel, J., Record, M., Chap, H. and Douste-Blazy, L. (1984) Studies on ether phospholipids. II. Comparative composition of various tissues from human, rat and guinea pig. Biochim. Biophys. Acta, 793, 221-231.
3. Montrucchio, G., Alloatti, G. and Camussi, G. (2000) Role of platelet-activating factor in cardiovascular pathophysiology. Physiol. Rev., 80, 1669-1699.
4. Hooper, N.M. (1997) Glycosyl-phosphatidylinositol anchored membrane enzymes. Clin. Chim. Acta, 266, 3-12.
5. Chatterjee, S. and Mayor, S. (2001) The GPI-anchor and protein sorting. Cell Mol. Life Sci., 58, 1969-1987.
6. Vos, J.P., Lopes-Cardozo, M. and Gadella, B.M. (1994) Metabolic and functional aspects of sulfogalactolipids. Biochim. Biophys. Acta, 1211, 125-149.
7. Ishizuka, I. (1997) Chemistry and functional distribution of sulfoglycolipids. Prog. Lipid Res., 36, 245-319.
8. Hajra, A.K. (1995) Glycerolipid biosynthesis in peroxisomes (microbodies). Prog. Lipid Res., 34, 343-364.
9. Moser, H.W. (2000) Molecular genetics of peroxisomal disorders. Front. Biosci., 5, D298-306.
10. Subramani, S., Koller, A. and Snyder, W.B. (2000) Import of peroxisomal matrix and membrane proteins. A. Rev. Biochem., 69, 399-418.
11. Heikoop, J.C., van Roermund, C.W., Just, W.W., Ofman, R., Schutgens, R.B., Heymans, H.S., Wanders, R.J. and Tager, J.M. (1990) Rhizomelic chondrodysplasia punctata. Deficiency of 3-oxoacyl-coenzyme A thiolase in peroxisomes and impaired processing of the enzyme. J. Clin. Invest., 86, 126-130.
12. Thai, T.P., Rodemer, C., Jauch, A., Hunziker, A., Moser, A., Gorgas, K. and Just, W.W. (2001) Impaired membrane traffic in defective ether lipid biosynthesis. Hum. Mol. Genet., 10, 127-136.
13. Baes, M., Gressens, P., Baumgart, E., Carmeliet, P., Casteels, M., Fransen, M., Evrard, P., Fahimi, D., Declercq, P.E., Collen, D. et al. (1997) A mouse model for Zellweger syndrome. Nat. Genet., 17, 49-57.
14. Faust, P.L., Su, H.M., Moser, A. and Moser, H.W. (2001) The peroxisome deficient PEX2 Zellweger mouse: pathologic and biochemical correlates of lipid dysfunction. J. Mol. Neurosci., 16, 289-297; discussion 317-321.
15. Kunau, W.H. (2001) Peroxisomes: the extended shuttle to the peroxisome matrix. Curr. Biol., 11, R659-662.
16. Clayton, P.T., Eckhardt, S., Wilson, J., Hall, C.M., Yousuf, Y., Wanders, R.J. and Schutgens, R.B. (1994) Isolated dihydroxyacetonephosphate acyltransferase deficiency presenting with developmental delay. J. Inherit. Metab. Disord., 17, 533-540.
17. Hebestreit, H., Wanders, R.J., Schutgens, R.B., Espeel, M., Kerckaert, I., Roels, F., Schmausser, B., Schrod, L. and Marx, A. (1996) Isolated dihydroxyacetonephosphate-acyl-transferase deficiency in rhizomelic chondrodysplasia punctata: clinical presentation, metabolic and histological findings. Eur. J. Pediatr., 155, 1035-1039.
18. Elias, E.R., Mobassaleh, M., Hajra, A.K. and Moser, A.B. (1998) Developmental delay and growth failure caused by a peroxisomal disorder, dihydroxyacetorephosphate acyltransferase (DHAP-AT) deficiency. Am. J. Med. Genet., 80, 223-226.
19. Powers, J.M., Kenjarski, T.P., Moser, A.B. and Moser, H.W. (1999) Cerebellar atrophy in chronic rhizomelic chondrodysplasia punctata: a potential role for phytanic acid and calcium in the death of its Purkinje cells. Acta Neuropathol. (Berl.), 98, 129-134.
20. Wanders, R.J. (1999) Peroxisomal disorders: clinical, biochemical, and molecular aspects. Neurochem. Res., 24, 565-580.
21. de Vet, E.C, Ijlst, L., Oostheim, W, Dekker, C., Moser, H.W., van Den Bosch, H. and Wanders, R.J. (1999) Ether lipid biosynthesis: alkyl-dihydroxyacetonephosphate synthase protein deficiency leads to reduced dihydroxyacetonephosphate acyltransferase activities. J. Lipid Res., 40, 1998-2003.
22. Pike, L.J., Han, X., Chung, K.N. and Gross, R.W. (2002) Lipid rafts are enriched in arachidonic acid and plasmenylethanolamine and their composition is independent of caveolin-1 expression: a quantitative electrospray ionization/mass spectrometric analysis. Biochemistry, 41, 2075-2088.
23. Kokubo, H., Lemere, C.A. and Yamaguchi, H. (2000) Localization of flotillins in human brain and their accumulation with the progression of Alzheimer's disease pathology. Neurasci. Lett., 290, 93-96.
24. Bickel, P.E., Scherer, P.E., Schnitzer, J.E., Oh, R, Lisanti, M.P. and Lodish, H.F. (1997) Flotillin and epidermal surface antigen define a new family of caveolae-associated integral membrane proteins. J. Biol. Chem., 272, 13793-13802.
25. Kramer, E.M., Klein, C., Koch, T., Boytinck, M. and Trotter, J. (1999) Compartmentation of Fyn kinase with glycosylphosphatidylinositol-anchored molecules in oligodendrocytes facilitates kinase activation during myelination. J. Biol. Chem., 274, 29042-29049.
26. Boyle, M.E., Berglund, E.O., Murai, K.K., Weber, L., Peles, E. and Ranscht, B. (2001) Contactin orchestrates assembly of die septate-like junctions at the paranode in myelinated peripheral nerve. Neuron, 30, 385-397.
27. Goodenough, D.A., Goliger, J.A. and Paul, D.L. (1996) Connexins, connexons, and intercellular communication. A. Rev. Biochem., 65, 475-502.
28. Roscoe, W.A., Barr, K.J., Mhawi, A.A., Pomerantz, D.K. and Kidder, G.M. (2001) Failure of spermatogenesis in mice lacking connexin43. Biol. Reprod., 65, 829-838.
29. Girao, H. and Pereira, P. (2003) Phosphorylation of connexin 43 acts as a stimuli for proteasome-dependent degradation of the protein in lens epithelial cells. Mol. Vis., 9, 24-30.
30. Chang, B., Smith, R.S., Hawes, N.L., Anderson, M.G., Zabaleta, A., Savinova, O., Roderick, T.H., Heckenlively, J.R., Davisson, M.T. and John, S.W. (1999) Interacting loci cause severe iris atrophy and glaucoma in DBA/2J mice. Nat. Genet., 21, 405-409.
31. Ishii, S. and Shimizu, T. (2000) Platelet-activating factor (PAF) receptor and genetically engineered PAF receptor mutant mice. Prog. Lipid Res., 39, 41-82.
32. Martinez, M. and Mougan, I. (1999) Fatty acid composition of brain glycerophospholipids in peroxisomal disorders. Lipids, 34, 733-740.
33. Ford, D.A. and Gross, R.W. (1989) Plasmenylethanolamine is the major storage depot for arachidonic acid in rabbit vascular smooth muscle and is rapidly hydrolyzed after angiotensin II stimulation. Proc. Natl Acad. Sci. USA, 86, 3479-3483.
34. Nordoy, A., Marchioli, R., Amesen, H. and Videbaek, J. (2001) n-3 polyunsaturated fatty acids and cardiovascular diseases. Lipids, 36 (suppl.), S127-129.
35. Singh, N., Zoeller, R.A., Tykocinski, M.L., Lazarow, P.B. and Tartakoff, A.M. (1994) Addition of lipid substituents of mammalian protein glycosylphosphoinositol anchors. Mol. Cell. Biol., 14, 21-31.
36. Zoeller, R.A., Morand, O.H. and Raetz, C.R. (1988) A possible role for plasmalogens in protecting animal cells against photosensitized killing. J. Biol. Chem., 263, 11590-11596.
37. Jansen, G.A. and Wanders, R.J. (1997) Plasmalogens and oxidative stress: evidence against a major role of plasmalogens in protection against the superoxide anion radical. J. Inherit. Metab. Disord., 20, 85-94.
38. Wanders, R.J., Jansen, G.A., van Roermund, C.W., Denis, S., Schutgens, R.B. and Jakobs, B.S. (1996) Metabolic Aspects of Peroxisomal Disorders. New York Academy of Science, New York.
39. Brown, D.A. and London, E. (1998) Structure and origin of ordered lipid domains in biological membranes. J. Membr. Biol., 164, 103-114.
40. Ko, Y.G., Lee, J.S., Kang, Y.S., Ahn, J.H. and Seo, J.S. (1999) TNF-alpha-mediated apoptosis is initiated in caveolae-like domains. J. Immunol., 162, 7217-7223.
41. Cottin, V., Doan, J.E. and Riches, D.W. (2002) Restricted localization of the TNF receptor CD120a to lipid rafts: a novel role for the death domain. J. Immunol., 168, 4095-4102.
42. Razani, B., Zhang, X.L., Bitzer, M., von Gersdorff, G., Bottinger, E.P. and Lisanti, M.P. (2001) Caveolin-1 regulates transforming growth factor (TGF)-beta/SMAD signaling through an interaction with the TGF-beta type I receptor. J. Biol. Chem., 276, 6727-6738.
43. Mineo, C., Gill, G.N. and Anderson, R.G. (1999) Regulated migration of epidermal growth factor receptor from caveolae. J. Biol. Chem., 274, 30636-30643.
44. Davy, A., Feuerstein, C. and Robbins, S.M. (2000) Signaling within a caveolae-like membrane microdomain in human neuroblastoma cells in response to fibroblast growth factor. J. Neurochem., 74, 676-683.
45. Citores, L., Wesche, J., Kolpakova, E. and Olsnes, S. (1999) Uptake and intracellular transport of acidic fibroblast growth factor: evidence for free and cytoskeleton-anchored fibroblast growth factor receptors. Mol. Biol. Cell, 10, 3835-3848.
46. Nusrat, A., Parkos, C.A., Verkade, P., Foley, C.S., Liang, T.W., Innis-Whitehouse, W., Eastburn, K.K. and Madara, J.L. (2000) Tight junctions are membrane microdomains. J Cell Sci., 113 (Pt 10), 1771-1781.
47. Lee, N.P., Mruk, D., Lee, W.M. and Cheng, C.Y. (2003) Is the cadherin/ catenin complex a ftinctional unit of cell-cell actin-based adherens junctions in the rat testis? Biol. Reprod., 68, 489-508.
48. Faivre-Sarrailh, C., Gauthier, F., Denisenko-Nehrbass, N., Le Bivic, A., Rougon, G. and Girault, J.A. (2000) The glycosylphosphatidyl inositol-anchored adhesion molecule F3/contactin is required for surface transport of paranodin/contactin-associated protein (caspr). J. Cell Biol., 149, 491-502.
49. Schubert, A.L., Schubert, W., Spray, D.C. and Lisanti, M.P. (2002) Connexin family members target to lipid raft domains and interact with caveolin-1. Biochemistry, 41, 5754-5764.
50. Zhou, L., Kasperek, E.M. and Nicholson, B.J. (1999) Dissection of the molecular basis of pp60(v-src) induced gating of connexin 43 gap junction channels. J. Cell Biol., 144, 1033-1045.
51. Carystinos, G.D., Kandouz, M., Alaoui-Jamali, M.A. and Batist, G. (2003) Unexpected induction of the human connexin 43 promoter by the ras signaling pathway is mediated by a novel putative promoter sequence. Mol. Pharmac., 63, 821-831.
52. Jou, Y.S., Layhe, B., Matesic, D.F., Chang, C.C., de Feijter, A.W., Lockwood, L., Welsch, C.W., Klaunig, J.E. and Trosko, J.E. (1995) Inhibition of gap junctional intercellular communication and malignant transformation of rat liver epithelial cells by neu oncogene. Carcinogenesis, 16, 311-317.
53. Hossain, M.Z., Jagdale, A.B., Ao, P., Kazlauskas, A. and Boynton, A.L. (1999) Disruption of gap junctional communication by the platelet-derived growth factor is mediated via multiple signaling pathways. J. Biol. Chem., 274, 10489-10496.
54. Lau, A.F., Kurata, WE., Kanemitsu, M.Y, Loo, LW, Warn-Cramer, B.J., Eckhart, W. and Lampe, P.D. (1996) Regulation of connexin43 function by activated tyrosine protein kinases. J Bioenerg. Biomembr., 28, 359-368.
55. Munn, N.J., Amio, E., Liu, D., Zoeller, R.A. and Liscum, L. (2003) Deficiency in ethanolamine plasmalogen leads to altered cholesterol transport. J. Lipid Res., 44, 182-192.
56. Nwokoro, N.A., Wassif C.A. and Porter, F.D. (2001) Genetic disorders of cholesterol biosynthesis in mice and humans. Mol. Genet. Metab., 74, 105-119.
57. Bosio, A., Binczek, E. and Stoffel, W. (1996) Functional breakdown of the lipid bilayer of the myelin membrane in central and peripheral nervous system by disrupted galactocerebroside synthesis. Proc. Natl Acad. Sci. USA, 93, 13280-13285.
58. Coetzee, T., Fujita, N., Dupree, J., Shi, R., Blight, A., Suzuki, K. and Popko, B. (1996) Myelination in the absence of galactocerebroside and sulfatide: normal structure with abnormal function and regional instability. Cell, 86, 209-219.
59. Fujimoto, H., Tadano-Aritomi, K., Tokumasu, A., Ito, K., Hikita, T., Suzuki, K. and Ishizuka, I. (2000) Requirement of seminolipid in spermatogenesis revealed by UDP-galactose: ceramide galactosyltrans-ferase-deficient mice. J. Biol. Chem., 275, 22623-22626.
60. Honke, K., Hirahara, Y., Dupree, J., Suzuki, K., Popko, B., Fukushima, K., Fukushima, J., Nagasawa, T., Yoshida, N., Wada, Y. et al. (2002) Paranodal junction formation and spermatogenesis require sulfoglycolipids. Proc. Natl Acad. Sci. USA, 99, 4227-4232.
61. Takamiya, K., Yamamoto, A., Furukawa, K., Zhao, J., Fukumoto, S., Yamashiro, S., Okada, M., Haraguchi, M., Shin, M., Kishikawa, M. et al. (1998) Complex gangliosides are essential in spermatogenesis of mice: possible roles in the transport of testosterone. Proc. Natl Acad. Sci. USA, 95, 12147-12152.
62. White, T.W. (2002) Unique and redundant connexin contributions to lens development. Science, 295, 319-320.
63. Giepmans, B.N. and Moolenaar, W.H. (1998) The gap junction protein connixin43 interacts with the second PDZ domain of the zona occludens-1 protein. Curr. Biol., 8, 931-934.
64. Giepmans, B.N., Hengeveld, T., Postma, F.R. and Moolenaar, W.H. (2001) Interaction of c-Src with gap junction protein connexin-43. Role in the regulation of cell-cell communication. J. Biol. Chem., 276, 8544-8549.
65. Ai, Z., Fischer, A., Spray, D.C., Brown, A.M. and Fishman, G.I. (2000) Wnt-1 regulation of connexin43 in cardiac myocytes. J. Clin. Invest., 105, 161-171.
66. Colville, D.J. and Savige, J. (1997) Alport syndrome. A review of the ocular manifestations. Ophthal. Genet., 18, 161-173.
67. Chen, L., Miyamura, N., Ninomiya, Y. and Handa, J.T. (2003) Distribution of the collagen IV isoforms in human Bruch's membrane. Br. J. Ophthal., 87, 212-215.
68. Sin, M.K., Lee, W.M. and Cheng, C.Y. (2003) The interplay of collagen IV tumor necrosis factor-alpha, gelatinase B (matrix metalloprotease-9), and tissue inhibitor of metalloproteases-1 in the basal lamina regulates Sertoli cell-tight junction dynamics in the rat testis. Endocrinology, 144, 371-387.
69. Noble, M., Murray, K., Stroobant, P., Waterfield, M.D. and Riddle, P. (1988) Platelet-derived growth factor promotes division and motility and inhibits premature differentiation of the oligodendrocyte/type-2 astrocyte progenitor cell. Nature, 333, 560-562.
70. Baron, W., Decker, L., Colognato, H. and Fftench-Constant, C. (2003) Regulation of integrin growth factor interactions in oligodendrocytes by lipid raft microdomains. Curr. Biol., 13, 151-155.
71. Mariani, S., Basciani, S., Arizzi, M., Spera, G. and Gnessi, L. (2002) PDGF and the testis. Trends Endocrinol. Metab., 13, 11-17.
72. Fruttiger, M., Karlsson, L., Hall, A.C., Abramsson, A., Calvet, A.R., Bostrom, H., Willetts, K., Bertold, C.H., Heath, J.K., Betsholtz, C. et al. (1999) Defective oligodendrocyte development and severe hypomyelination in PDGF-A knockout mice. Development, 126, 457-467.
73. Westphal, C.H. and Leder, P. (1997) Transposon-generated 'knock-out' and 'knock-in' gene-targeting constructs for use in mice. Curr. Biol., 7, 530-533.
74. Forss-Petter, S., Werner, H., Berger, J., Lassmann, H., Molzer, B., Schwab, M.H., Bernheimer, H., Zimmermann, F. and Nave, K.A. (1997) Targeted inactivation of the X-linked adrenoleukodystrophy gene in mice. J. Neurosci. Res., 50, 829-843.
75. Thai, T.P., Heid, H., Rackwitz, H.R., Hunziker, A., Gorgas, K. and Just, W.W. (1997) Ether lipid biosynthesis: isolation and molecular characterization of human dihydroxyacetonephosphate acyltransferase. FEBS Lett., 420, 205-211.
76. Gkantiragas, I., Brugger, B., Stuven, E., Kaloyanova, D., Li, X.Y., Lohr, K., Lottspeich, F., Wieland, F.T. and Helms, J.B. (2001) Sphingomyelin-enriched microdomains at the Golgi complex. Mol. Biol. Cell, 12, 1819-1833.
77. Bligh, E.G. and Dyer, W.J. (1959) A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol., 37, 911-917.
78. Bragger, B., Erben, G., Sandhoff, R., Wieland, F.T. and Lehmann, W.D. (1997) Quantitative analysis of biological membrane lipids at the low picomole level by nano-electrospray ionization tandem mass spectrometry. Proc. Natl Acad. Sci. USA, 94, 2339-2244.
79. Gorgas, K. (1984) Peroxisomes in sebaceous glands. V. Complex peroxisomes in the mouse preputial gland: serial sectioning and three-dimensional reconstruction studies. Anat. Embryol. (Berl.), 169, 261-270.