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On the role of sulfolipids in mammalian metabolism

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Summary

Sulfolipids of mammalian origin include sulfosphingolipids, sulfoglycerolipids and steroid sulfates. Sulfosphingolipids (sulfogalactosylceramide) may be involved in sodium transport, interaction of opiates with their receptors, activation of oxygen radical generating system, and blood coagulation Factor XII. Sulfoglycerolipids and steroid sulfates may be involved in spermatogenesis and sperm capacitation.

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References

  1. Farooqui AA: Metabolism and role of sulfolipids in mammalian tissues. Int J Biochem 9:709–716, 1978.

    Google Scholar 

  2. Radin NS: Sulfatides. In: Lajtha A(ed), Handbook of Neurochemistry 3, 2nd ed. Plenum Press, New York, 1983, pp 163–177.

    Google Scholar 

  3. Schachter H, Roseman S: Mammalian glycosyltransferases: their role in the synthesis and function of complex carbohydrates and glycolipids. In: Lennarz WJ (ed), Biochemistry Glycoproteins and Proteoglycans. Plenum Publishing Corp, New York, 1980, pp 85–160.

    Google Scholar 

  4. Fleischer B, Zambrano F: Golgi apparatus of rat kidney: role in sulphatide formation. J Biol Chem 249:5995–6003, 1974.

    Google Scholar 

  5. Tennekoon G, Zaruba M, Wolinsky J: Topography of cerebroside sulfotransferase in Golgi-enriched vesicles from rat brain. J Cell Biol 97:1107–1112, 1983.

    Google Scholar 

  6. Young RW: The role of the Golgi complex in sulfate metabolism. J Cell Biol 57:175–189, 1973.

    Google Scholar 

  7. Aruna RM, Basu D: Glycolipid metabolism in tumors of central nervous system. Ind J Biochem Biophys 13:158–160, 1978.

    Google Scholar 

  8. Hakomori S-I: Glycolipids — their chemical pattern, synthesis and degradation in normal and tumor cells. In: Wood R (ed), Tumor Lipids: Biochemistry and Metabolism. Americal Oil Chemist Society Press, Champaign, Illinois, 1973, pp 269–294.

    Google Scholar 

  9. Farooqui AA, Mandel P: Recent developments in the biochemistry of globoid and metachromatic leucodystrophies. Biomedicine 26:232–236, 1977.

    Google Scholar 

  10. Dulaney JT, Moser HW: Sulfatide lipidosis: metachromatic leukodystrophy. In: Stanbury JB, Wyngaarden JB, Fredrickson DS (eds), Metabolic Basis of Inherited Diseases. McGraw-Hill, New York, 1978, pp 770–809.

    Google Scholar 

  11. Herschkowitz N, McKhann GM, Saxena S, Shooter EM, Herndon R: Synthesis of sulfatide-containing lipoprotein in rat brain. J Neurochem 16:1049–1057, 1969.

    Google Scholar 

  12. Jungalwala FB: Synthesis and turnover of cerebroside sulfate of myelin in adult and developing rat brain. J Lipid Res 15:114–123, 1974.

    Google Scholar 

  13. Mehl E, Jatzkewitz H: Cerebroside 3-sulphate as a physiological substrate for arylsulphatase A. Biochim Biophys Acta 151:619–627, 1968.

    Google Scholar 

  14. Farooqui AA, Bachhawat BK: Enzymatic desulphation of cerebroside 3-sulphate by chicken brain arylsulphatase A J Neurochem 20:889–891, 1973.

    Google Scholar 

  15. Farooqui AA: Purification and properties of arylsulphatase A from human placenta. Archs Int Physiol Biochim 84: 479–492, 1976.

    Google Scholar 

  16. Jerfy A, Roy AB: Comparison of the arylsulphatase and cerebroside sulphatase activities of sulphatase A. Biochim Biophys Acta 293:178–190, 1973.

    Google Scholar 

  17. London Y, Vossenberg FGA: Specific interaction of central nervous system myelin basic protein with lipids. Biochim Biophys Acta 478:478–490, 1973.

    Google Scholar 

  18. London Y, Demel RA, Geurts Van Kessel WSM, Vossenberg FGA, Van Deenen LLM: The protection of A1 myelin basic protein against the action of proteolytic enzymes after interaction of the protein with lipids at the air-water interface. Biochim Biophys Acta 311:520–530, 1973.

    Google Scholar 

  19. Davison AN, Gregson NA: The physiological role of cerebron sulfuric acid in the brain. Biochem J 85:558–568, 1962.

    Google Scholar 

  20. Pritchard ET: Variation in sulfolipid metabolism during early growth in some rat tissues. Int J Biochem 6:353–359, 1975.

    Google Scholar 

  21. Kornblatt MJ, Schachter H, Murray RK: Partial characterization of a novel glycerogalactolipid from rat testis. Biochem Biophys Res Common 48:1489–1494, 1972.

    Google Scholar 

  22. Ishizuka I, Suzuki M, Yamakawa T: Isolation and characterization of a novel sulphoglycolipid, seminolipid, from boar testis and spermatozoa. J Biochem (Tokyo) 73:77–87, 1973.

    Google Scholar 

  23. Kornblatt MJ, Knapp A, Levine M, Schachter H, Murray RK: Studies on the structure and formation during spermatogenesis of sulphoglycerogalactolipid of rat testis. Can J Biochem 52:689–697, 1974.

    Google Scholar 

  24. Levine M, Kornblatt MJ, Murray RK: Isolation and partial characterization of a sulphogalactoglycolipid from rat brain. Can J Biochem 53:679–689, 1975.

    Google Scholar 

  25. Pieringer J, Subba Rao G, Mandel P,Pieringer RA: The association of the sulfogalactosylglycerolipid of rat brain with myelination. Biochem J 166:421–428, 1977.

    Google Scholar 

  26. Ishizuka I, Inomata M, Ueno K, Yamakawa T: Sulphated glyceroglycolipid in rat brain. Structure, sulphation in vivo and accumulation in whole brain during development. J Biol Chem 253:898–907, 1978.

    Google Scholar 

  27. Burkart T, Caimi L, Herschkowitz H, Wiesmann UN: Metabolism of sulfogalactosylglycerolipids in the myelinating mouse brain. Develop. Biol. 98:182–186, 1983.

    Google Scholar 

  28. Green JP, Robinson Jr. JD, Day M: Interaction between cerebroside sulfate and amines. J Pharmacol Exp Therap 131:12–17, 1961.

    Google Scholar 

  29. Alam T, Cherian R, Balasubramanian AS: An in vitro study of the binding of histamine to brain glycolipids. Ind J Biochem Biophys 15:49–53, 1978.

    Google Scholar 

  30. Abramson MB, Katzman R, Curci R, Wilson CE: The reactions of sulfatide with metallic cations in aqueous systems. Biochemistry 6:295–301, 1967.

    Google Scholar 

  31. Leitch GJ, Horrocks LA, Samorajski T: Effects of cations on isolated bovine optic nerve myelin. J Neurochem 16: 1347–1354, 1969.

    Google Scholar 

  32. Lowney LI, Schultz K, Lowery PJ, Goldstein A: Science 183:749–753, 1974.

    Google Scholar 

  33. Cho TM, Cho JS, Loh HH: Cerebroside sulphate redistribution induced by cation opiate or phosphatidyl serine. Life Sci 19:117–124, 1976.

    Google Scholar 

  34. Loh HH, Law PY, Ostwald T, Cho TM, Way EL: Possible involvement of cerebroside sulphate in opiate receptor binding. Fed Proc Fed Am See Exp Biol 37:147–152, 1978.

    Google Scholar 

  35. Law PY, Fischer G, Loh HH, Herz A: Inhibition of specific opiate binding to synaptic membrane by cerebroside sulfatase. Biochem Pharmacol 28:2557–2562, 1979.

    Google Scholar 

  36. Garzon J, Jen MF, Lee NM: Differential modification of opiate receptor activity by arylsulfatase treatment. Biochem Pharmacol 32:1523–1528, 1983.

    Google Scholar 

  37. Craves FB, Zalc B, Leybin L, Baumann N, Loh HH: Antibodies to cerebroside sulfate inhibit the effects of morphine and /gb-endorphin. Science 207:75–76, 1979.

    Google Scholar 

  38. Dennis SG: Peptides, opiate receptors and cerebroside sulfate: a hypothesis. Prog Neuro-psychopharmacol 4:111–122, 1980.

    Google Scholar 

  39. McLawhon RW, Schoon GS, Dawson G: Glycolipids and opiate action. Eur J Cell Biol 25:353–358, 1981.

    Google Scholar 

  40. Dawson G, Kernes SM, Miller RJ, Wainer B: Evidence for the noninvolvement of sulfogalactosylceramide in the enkephalin (opiate) receptor. J Biol Chem 253:7999–8001, 1978.

    Google Scholar 

  41. Ebadi M, Chweh A: Inhibition by arylsulfatase A of Na-independent [3H]-GABA and [3H]muscimol binding to bovine cerebellar synaptic membranes. Neuropharmacology 19: 1105–1111, 1980.

    Google Scholar 

  42. Chweh AY, Leslie SW: Enhancement by sulfatides of Na+-independent [3H]GABA binding in mouse brain. Biochem Biophys Res Common 112:827–832, 1983.

    Google Scholar 

  43. Karlsson KA, Samuelsson BE, Steen GO: The sphingolipid composition of bovine kidney cortex. Medulla and papilla. Biochem Biophys Acta 316:317–335, 1973.

    Google Scholar 

  44. Samuelsson BE: Regional distribution of glycosylceramidesulfates in human kidney. Lipids 17:160–165, 1982.

    Google Scholar 

  45. Karlsson KA, Samuelsson BE, Steen GO: The lipid composition and Na+-K+-dependent ATPase activity of the salt gland of eider duck and herring gull. Eur J Biochem 46:243–258, 1974.

    Google Scholar 

  46. Karlsson KA, Samuelsson BE, Steen GO: The lipid composition of the salt (rectal) gland of spiny dog fish. Biochim Biophys Acta 337:356–376, 1974.

    Google Scholar 

  47. Hansson GC, Heilbronn E, Karlsson KA, Samuelsson BE: The lipid composition of the electric organ of the ray, Torpedo marmorata, with specific reference to sulfatides and Na++K-ATPase. J Lipid Res 20:509–518, 1979.

    Google Scholar 

  48. Gonzalez M, Morales M, Zambrano F: Sulfatide content and (Na+, K+)-ATPase activity of skin and gill during larval development of the chilean frog, Calyptocephalella caudiverbera. J Membrane Biol 51:347–359, 1979.

    Google Scholar 

  49. Gonzalez E, Zambrano F: Possible role of sulfatide in the K+-activated phosphatase activity. Biochim Biophys Acta 728:66–72, 1983.

    Google Scholar 

  50. Umeda T, Egawa K, Nagai Y: Enhancement of sulphatide metabolism in the hypertrophied kidney of C3H/HC mouse with reference to Na+, K+-dependent ATPase. Jpn J Exp Med 46:87–94, 1976.

    Google Scholar 

  51. Bently JP, Feeney L, Hanson AN, Mixon RN: Sulphated glycolipids in ciliary body epithelium. Invest Ophthalmol 15:575–579, 1976.

    Google Scholar 

  52. Helwig JJ, Pieringer J, Sarlieve LL, Farooqui AA, Rebel G, Mandel P, Pieringer RA: Cellular localization of Na+, K+-dependent ATPase and the enzymes of sulfolipid metabolism in rabbit kidney. Adv Exp Biol Med 101:641–648, 1978.

    Google Scholar 

  53. Zalc B, Helwig JJ, Ghandour MS, Sarlieve L: Sulfatide in the kidney: How is this lipid involved in sodium chloride transport. FEBS Lett 92:92–96, 1978.

    Google Scholar 

  54. Zwingelstein G, Portoukalian J, Rebel G, Brichon G: Gill sulfolipid synthesis and seawater adaptation in euryhalion fish Anguilla anguilla. Comp. Biochem. Physiol 6513: 555–558, 1980.

    Google Scholar 

  55. Hansson GC, Karlsson KA, Samuelsson BE: The identification of sulphtides in human erythrocyte membrane and their relation to Na+, K+-dependent ATPase. J Biochem (Tokyo) 83:813–819, 1978.

    Google Scholar 

  56. Bleau G, Bodley FH, Longpre J, Chapdelaine A, Roberts KD: Cholesterol sulphate: Occurrence and possible biological function as an amphipathic lipid in the membrane of human erythrocyte. Biochim Biophys Acta 352:1–9, 1974.

    Google Scholar 

  57. Lalumiere G, Bleau G, Chapdelaine A, Roberts K D: Cholesteryl sulphate and sterol sulphatase in the human reproductive tract. Steroid 27:247–260, 1976.

    Google Scholar 

  58. Legault Y, Bouthillier M, Bleau G, Chapdelaine A, Roberts KD: The sterol and sterol sulfate content of the male hamster reproductive tract. Biol Reprod 20:1213–1219, 1979.

    Google Scholar 

  59. Bleau G, VandenHeuvel WJA, Anderson OF, Gwatkin RBL: Desmosteryl sulfate of hamster spermatozoa, a potent inhibitor of capacitation in vitro. J Reprod Fertil 43: 175–178, 1975.

    Google Scholar 

  60. Farooqui AA, Biochemistry of sperm capacitation. Int J Biochem 15:463–468, 1983.

    Google Scholar 

  61. Bruck PJ, Zimmerman RE: The inhibition of acrosin by sterol sulfates. J Reprod Fertil 58:121–125, 1980.

    Google Scholar 

  62. McRorie RA, William WL: Biochemistry of mammalian fertilization. Ann Rev Biochem 43:777–803, 1974.

    Google Scholar 

  63. Farooqui AA, Srivastava PN: Isolation, characterization and the role of rabbit testicular arylsulfatase A in fertilization. Biochem J 181:331–337, 1979.

    Google Scholar 

  64. Go KJ, Wolf DP: The role of sterols in sperm capacitation. Adv Lipid Res 20:317–330, 1983.

    Google Scholar 

  65. Griffin JH: The role of surface in the surface-dependent activation of Hageman factor (factor XII). Proc Natl Acad Sci U.S.A. 75:1998–2002, 1978.

    Google Scholar 

  66. Fujikawa K, Heimark RL, Kurachi K, Davie EW: Mechanisms of activation of bovine factor XI by factor XII and factor XIIa. Biochemistry 19:1322–1330, 1980.

    Google Scholar 

  67. Griffin JH, Cochrane CG: Mechanism for involvement of high molecular weight kininogen in surface-dependent reactions of Hageman factor (coagulation factor XII). Proc Natl Acad Sci USA 73: 2554–2559, 1976.

    Google Scholar 

  68. Tans G, Griffin JH: Properties of sulfatides in factor — XII — dependent contact activation. Blood 59:69–75, 1982.

    Google Scholar 

  69. Tans G, Roling J, Griffin JH: Sulfatide-dependent autoactivation of human blood coagulation factor XII (Hageman factor). J Biol Chem 258:8215–8222, 1983.

    Google Scholar 

  70. Espana F, Ratnoff OD: Activation of Hageman factor (factor XII) by sulfatides and other agents in the absence of plasma proteases. J Lab Clin Med 102:31–45, 1983.

    Google Scholar 

  71. Kakinuma K, Yamaguchi T, Suzuki H, Nagai Y: Sulfatide activation of the oxygen radical generating system of leukocytes. FEBS Lett 145:16–20, 1982.

    Google Scholar 

  72. Nagai Y, Osanai T, Yamaguchi T, Kakinuma K: Sulfatides in demyelination: their possible relation to the membrane-hazardous activity oxygen-generating system of leukocytes. In: Battistin A, Hashim G, Lajtha A (eds), Clinical and Biological Aspects of Peripheral Nerve Diseases. Alan R. Liss, Inc, New York, 1983, pp 235–245.

    Google Scholar 

  73. Paterson PY: Experimental autoimmune (allergic) encephalomyelitis: induction, pathogenesis and suppression. In: Meischer PE, Muller-Eberhard HJ (eds), Textbook of Immunopathology, 2nd ed, Vol 1. Grune and Stratton, New York, 1976, pp 179–213.

    Google Scholar 

  74. Slomiany BL, Slomiany A: Isolation and characterization of the sulphated neolactotetraosylceramide from hog gastric mucosa. J Biol Chem 253:3517–3520, 1978.

    Google Scholar 

  75. Slomiany A, Kojima K, Banas-Gruszka Z, Slomiany BL: Structure of a novel sulfated sialoglycosphingolipid from bovine gastric mucosa. Biochem Biophys Res Commun 100: 778–784, 1981.

    Google Scholar 

  76. Slomiany BL, Kojima K, Banas-Gruszka Z, Murty KLN, Galicki NI, Slomiany A: Characterization of the sulfated monosialosyltriglycosylceramide from bovine gastric mucosa. Eur J Biochem 119:647–650, 1981.

    Google Scholar 

  77. Martin F, Vuez JL, Berard A, Andre C, Lambert R: A study of the mechanisms of inhibition of peptic proteolysis by a sulfated polysaccharide. Digestion 1:165–174, 1968.

    Google Scholar 

  78. Tadono K, Ishizuka I: Isolation and partial characterization of a novel sulfoglycosphingolipid and ganglioside GM4 from rat kidney. Biochem Biophys Res Commun 97:126–132, 1980.

    Google Scholar 

  79. Tadano K, Ishizuka I: Isolation and partial characterization of a novel disulfoglycosphingolipid from rat kidney. Biochem Biophys Res Commun 103:1006–1013, 1981.

    Google Scholar 

  80. Goren MB, Hart PD, Young MR, Armstrong JA: Prevention of phagosome-lysosome fusion in cultured macrophages by sulfatides of Mycobacterium tuberculosis. Proc Natl Acad Sci USA 73:2510–2514, 1976.

    Google Scholar 

  81. Eto Y, Wiesmann U, Herschkowitz N: Sulfogalactosylsphingosine sulfatase. Characteristics of the enzyme and its deficiency in metachromatic leukodystrophy in human cultured skin fibroblasts. J Biol Chem 249:4955–4960, 1974.

    Google Scholar 

  82. Dreyfus H, Pieringer JA, Farooqui AA, Harth S, Rebel G, Sarlieve LL: Sulfolipid metabolism in developing chicken retina. J Neurochem 30:167–174, 1978.

    Google Scholar 

  83. Martensson E: Sulfatides of human kidney: isolation, identification and fatty acid composition. Biochim Biophys Acta 11:521–531, 1966.

    Google Scholar 

  84. Slomiany A, Smith FB, Slomiany BL: Isolation and characterization of sulfated glyceroglucolipid from alveolar lavage of rabbit. Eur J Biochem 98:47–51, 1979.

    Google Scholar 

  85. Moser HW, Moser AB, Orr JC: Preliminary observations on the occurrence of cholesterol sulfate in man. Biochim Biophys Acta 116:146–155, 1966.

    Google Scholar 

  86. Iwamori M, Moser HW, Kishimoto Y: Cholesterol sulfate in rat tissues — tissue distribution, developmental changes and brain subcellular localization. Biochim Biophys Acta 441: 268–279, 1976.

    Google Scholar 

  87. Farooqui AA, Rebel A, Mandel P: Sulfatide metabolism in brain. Life Sci 20:569–584, 1977.

    Google Scholar 

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Farooqui, A.A., Horrocks, L.A. On the role of sulfolipids in mammalian metabolism. Mol Cell Biochem 66, 87–95 (1985). https://doi.org/10.1007/BF00231827

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