Hormone-sensitive lipase deficiency disturbs the fatty acid composition of mouse testis

Prostaglandins Leukotrienes and Essential Fatty Acids

Volumn 88, Issue 3, 2013, Pages 227-233

  Casado, M E ^a,b   Pastor, O ^a   Mariscal, P ^a   Canfran Duque A ^a   Martinez Botas J ^a,b   Kraemer, F B ^c   Lasuncion M A ^a,b,d   Martin Hidalgo A ^a,b   Busto, R ^a,b  

^a HOSPITAL RAMÓN Y CAJAL   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c STANFORD UNIVERSITY   (United States)

^d UNIVERSITY OF ALCALÁ   (Spain)

Author keywords

Fatty acid; Hormone sensitive lipase; Plasmalogen; PUFA; Sterility; Testis

Indexed keywords

5,8,11 ICOSATRIENOIC ACID; ACYL COENZYME A DESATURASE 1; DOCOSAHEXAENOIC ACID; HORMONE SENSITIVE LIPASE; LINOLENIC ACID; MESSENGER RNA; MONOUNSATURATED FATTY ACID; OMEGA 3 FATTY ACID; OMEGA 6 FATTY ACID; PLASMALOGEN; POLYUNSATURATED FATTY ACID;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELOVL2 GENE; ENZYME DEFICIENCY; FADS1 GENE; FADS2 GENE; FATTY ACID METABOLISM; GENE; GENE EXPRESSION; KNOCKOUT MOUSE; LIPID COMPOSITION; MALE; MALE INFERTILITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEAROYL COA DESATURASE 1 GENE; TESTIS; TISSUE LEVEL;

ACETYLTRANSFERASES; ANIMALS; FATTY ACID DESATURASES; FATTY ACID SYNTHETASE COMPLEX; FATTY ACIDS, ESSENTIAL; GENE EXPRESSION; INFERTILITY, MALE; LIPID METABOLISM; MALE; MICE; MICE, KNOCKOUT; MYOCARDIUM; ORGAN SPECIFICITY; PLASMALOGENS; RNA, MESSENGER; SPERMATOGENESIS; STEROL ESTERASE; TESTIS;

ANIMALIA; MUS;

EID: 84875402335     PISSN: 09523278     EISSN: 15322823     Source Type: Journal    
DOI: 10.1016/j.plefa.2012.12.005     Document Type: Article

References (50)

1. Ahluwalia B., Holman R.T. Fatty acid composition of lipids of bull, boar, rabbit and human semen. J. Reprod. Fertil. 1969, 18:431-437.
2. Chanmugam P.S., Boudreau M.D., Hwang D.H. Dietary (n-3) fatty acids alter fatty acid composition and prostaglandin synthesis in rat testis. J. Nutr. 1991, 121:1173-1178.
3. Nissen H.P., Heinze I., Kreysel H.W., Schirren C. Fatty acid composition of neutral lipids of human semen. Andrologia 1978, 10:390-392.
4. Furland N.E., Zanetti S.R., Oresti G.M., Maldonado E.N., Aveldano M.I. Ceramides and sphingomyelins with high proportions of very long-chain polyunsaturated fatty acids in mammalian germ cells. J. Biol. Chem. 2007, 282:18141-18150.
5. Roqueta-Rivera M., Stroud C.K., Haschek W.M., Akare S.J., Segre M., Brush R.S., Agbaga M.P., Anderson R.E., Hess R.A., Nakamura M.T. Docosahexaenoic acid supplementation fully restores fertility and spermatogenesis in male delta-6 desaturase-null mice. J. Lipid Res. 2011, 51:360-367.
6. Kraemer F.B., Shen W.J. Hormone-sensitive lipase: control of intracellular tri-(di-)acylglycerol and cholesteryl ester hydrolysis. J. Lipid Res. 2002, 43:1585-1594.
7. Blaise R., Guillaudeux T., Tavernier G., Daegelen D., Evrard B., Mairal A., Holm C., Jegou B., Langin D. Testis hormone-sensitive lipase expression in spermatids is governed by a short promoter in transgenic mice. J. Biol. Chem. 2001, 276:5109-5115.
8. Holst L.S., Hoffmann A.M., Mulder H., Sundler F., Holm C., Bergh A., Fredrikson G. Localization of hormone-sensitive lipase to rat sertoli cells and its expression in developing and degenerating testes. FEBS Lett. 1994, 355:125-130.
9. Holst L.S., Langin D., Mulder H., Laurell H., Grober J., Bergh A., Mohrenweiser H.W., Edgren G., Holm C. Molecular cloning, genomic organization, and expression of a testicular isoform of hormone-sensitive lipase. Genomics 1996, 35:441-447.
10. Mairal A., Melaine N., Laurell H., Grober J., Holst L.S., Guillaudeux T., Holm C., Jegou B., Langin D. Characterization of a novel testicular form of human hormone-sensitive lipase. Biochem. Biophys. Res. Commun. 2002, 291:286-290.
11. Arenas M.I., Lobo M.V., Caso E., Huerta L., Paniagua R., Martin-Hidalgo M.A. Normal and pathological human testes express hormone-sensitive lipase and the lipid receptors cla-1/sr-bi and cd36. Hum. Pathol. 2004, 35:34-42.
12. Osuga J., Ishibashi S., Oka T., Yagyu H., Tozawa R., Fujimoto A., Shionoiri F., Yahagi N., Kraemer F.B., Tsutsumi O., Yamada N. Targeted disruption of hormone-sensitive lipase results in male sterility and adipocyte hypertrophy, but not in obesity. Proc. Natl. Acad. Sci. U S A 2000, 97:787-792.
13. Chung S., Wang S.P., Pan L., Mitchell G., Trasler J., Hermo L. Infertility and testicular defects in hormone-sensitive lipase-deficient mice. Endocrinology 2001, 142:4272-4281.
14. Fernandez C., Lindholm M., Krogh M., Lucas S., Larsson S., Osmark P., Berger K., Boren J., Fielding B., Frayn K., Holm C. Disturbed cholesterol homeostasis in hormone-sensitive lipase-null mice. Am. J. Physiol. Endocrinol. Metab. 2008, 295:E820-831.
15. Guillou H., Zadravec D., Martin P.G., Jacobsson A. The key roles of elongases and desaturases in mammalian fatty acid metabolism: insights from transgenic mice. Prog. Lipid Res. 2010, 49:186-199.
16. Engster H.M., Carew L.B., Cunningham F.J. Effects of an essential fatty acid deficiency, pair-feeding and level of dietary corn oil on the hypothalamic-pituitary-gonadal axis and other physiological parameters in the male chicken. J. Nutr 1978, 108:889-900.
17. Marzouki Z.M., Coniglio J.G. Effect of essential fatty acid deficiency on lipids of rat sertoli and germinal cells. Biol. Reprod 1982, 27:312-315.
18. Saether T., Tran T.N., Rootwelt H., Grav H.J., Christophersen B.O., Haugen T.B. Essential fatty acid deficiency induces fatty acid desaturase expression in rat epididymis, but not in testis. Reproduction 2007, 133:467-477.
19. Zadravec D., Tvrdik P., Guillou H., Haslam R., Kobayashi T., Napier J.A., Capecchi M.R., Jacobsson A. Elovl2 controls the level of n-6 28:5 and 30:5 fatty acids in testis, a prerequisite for male fertility and sperm maturation in mice. J. Lipid Res. 2011, 52:245-255.
20. Fan Y.Y., Monk J.M., Hou T.Y., Callway E., Vincent L., Weeks B., Yang P., Chapkin R.S. Characterization of an arachidonic acid-deficient (Fads1 knockout) mouse model. J. Lipid Res. 2011, 53:1287-1295.
21. Folch J., Lees M., Stanley G.H.Sloane A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem 1957, 226:497-509.
22. Lepage G., Roy C.C. Direct transesterification of all classes of lipids in a one-step reaction. J. Lipid Res. 1986, 27:114-120.
23. Abu E.O., Oluwatowoju I. Omega-3 index determined by gas chromatography with electron impact mass spectrometry. Prostaglandins Leukot. Essent. Fatty Acids 2009, 80:189-194.
24. Lessig J., Fuchs B. Plasmalogens in biological systems: their role in oxidative processes in biological membranes, their contribution to pathological processes and aging and plasmalogen analysis. Curr. Med. Chem 2009, 16:2021-2041.
25. Ayala S., Brenner R.R., Dumm C.G. Effect of polyunsaturated fatty acids of the alpha-linolenic series on the development of rat testicles. Lipids 1977, 12:1017-1024.
26. Coniglio J.G. Testicular lipids. Prog. Lipid Res. 1994, 33:387-401.
27. Retterstol K., Haugen T.B., Christophersen B.O. The pathway from arachidonic to docosapentaenoic acid (20:4n-6 to 22:5n-6) and from eicosapentaenoic to docosahexaenoic acid (20:5n-3 to 22:6n-3) studied in testicular cells from immature rats. Biochim. Biophys. Acta 2000, 1483:119-131.
28. Peluffo R.O., Ayala S., Brenner R.R. Metabolism of fatty acids of the linoleic acid series in testicles of diabetic rats. Am. J. Physiol. 1970, 218:669-673.
29. Stroud C.K., Nara T.Y., Roqueta-Rivera M., Radlowski E.C., Lawrence P., Zhang Y., Cho B.H., Segre M., Hess R.A., Brenna J.T., Haschek W.M., Nakamura M.T. Disruption of fads2 gene in mice impairs male reproduction and causes dermal and intestinal ulceration. J. Lipid Res. 2009, 50:1870-1880.
30. Haemmerle G., Zimmermann R., Hayn M., Theussl C., Waeg G., Wagner E., Sattler W., Magin T.M., Wagner E.F., Zechner R. Hormone-sensitive lipase deficiency in mice causes diglyceride accumulation in adipose tissue, muscle, and testis. J. Biol. Chem. 2002, 277:4806-4815.
31. Fernandez C., Schuhmann K., Herzog R., Fielding B., Frayn K., Shevchenko A., James P., Holm C., Strom K. Altered desaturation and elongation of fatty acids in hormone-sensitive lipase null mice. PLoS One 2011, 6:e21603.
32. Cao H., Gerhold K., Mayers J.R., Wiest M.M., Watkins S.M., Hotamisligil G.S. Identification of a lipokine, a lipid hormone linking adipose tissue to systemic metabolism. Cell 2008, 134:933-944.
33. Ntambi J.M. Regulation of stearoyl-coa desaturase by polyunsaturated fatty acids and cholesterol. J. Lipid Res 1999, 40:1549-1558.
34. Cho H.P., Nakamura M.T., Clarke S.D. Cloning, expression, and nutritional regulation of the mammalian delta-6 desaturase. J. Biol. Chem. 1999, 274:471-477.
35. Igarashi M., Ma K., Chang L., Bell J.M., Rapoport S.I. Dietary n-3 pufa deprivation for 15 weeks upregulates elongase and desaturase expression in rat liver but not brain. J. Lipid Res. 2007, 48:2463-2470.
36. Cho H.P., Nakamura M., Clarke S.D. Cloning, expression, and fatty acid regulation of the human delta-5 desaturase. J. Biol. Chem. 1999, 274:37335-37339.
37. Wang Y., Botolin D., Christian B., Busik J., Xu J., Jump D.B. Tissue-specific, nutritional, and developmental regulation of rat fatty acid elongases. J. Lipid Res. 2005, 46:706-715.
38. Holman R.T. The ratio of trienoic: tetraenoic acids in tissue lipids as a measure of essential fatty acid requirement. J. Nutr. 1960, 70:405-410.
39. Neely J.R., Morgan H.E. Relationship between carbohydrate and lipid metabolism and the energy balance of heart muscle. Annu. Rev. Physiol. 1974, 36:413-459.
40. Haemmerle G., Zimmermann R., Strauss J.G., Kratky D., Riederer M., Knipping G., Zechner R. Hormone-sensitive lipase deficiency in mice changes the plasma lipid profile by affecting the tissue-specific expression pattern of lipoprotein lipase in adipose tissue and muscle. J. Biol. Chem 2002, 277:12946-12952.
41. Okazaki H., Osuga J., Tamura Y., Yahagi N., Tomita S., Shionoiri F., Iizuka Y., Ohashi K., Harada K., Kimura S., Gotoda T., Shimano H., Yamada N., Ishibashi S. Lipolysis in the absence of hormone-sensitive lipase: evidence for a common mechanism regulating distinct lipases. Diabetes 2002, 51:3368-3375.
42. Isensee H., Jacob R. Differential effects of various oil diets on the risk of cardiac arrhythmias in rats. J. Cardiovasc. Risk 1994, 1:353-359.
43. Skuladottir G.V., Schioth H.B., Gudbjarnason S. Polyunsaturated fatty acids in heart muscle and alpha 1-adrenoceptor binding properties. Biochim. Biophys. Acta 1993, 1178:49-54.
44. Raclot T., Holm C., Langin D. Fatty acid specificity of hormone-sensitive lipase, implication in the selective hydrolysis of triacylglycerols. J. Lipid Res. 2001, 42:2049-2057.
45. Raclot T., Holm C., Langin D. A role for hormone-sensitive lipase in the selective mobilization of adipose tissue fatty acids. Biochim. Biophys. Acta 2001, 1532:88-96.
46. Strom K., Gundersen T.E., Hansson O., Lucas S., Fernandez C., Blomhoff R., Holm C. Hormone-sensitive lipase (HSL) is also a retinyl ester hydrolase: evidence from mice lacking hsl. Faseb J 2009, 23:2307-2316.
47. Thai T.P., Rodemer C., Jauch A., Hunziker A., Moser A., Gorgas K., Just W.W. Impaired membrane traffic in defective ether lipid biosynthesis. Hum. Mol. Genet. 2001, 10:127-136.
48. Munn N.J., Arnio E., Liu D., Zoeller R.A., Liscum L. Deficiency in ethanolamine plasmalogen leads to altered cholesterol transport. J. Lipid Res. 2003, 44:182-192.
49. Mankidy R., Ahiahonu P.W., Ma H., Jayasinghe D., Ritchie S.A., Khan M.A., Su-Myat K.K., Wood P.L., Goodenowe D.B. Membrane plasmalogen composition and cellular cholesterol regulation: a structure activity study. Lipids Health Dis. 2010, 9:62.
50. Pietilainen K.H., Rog T., Seppanen-Laakso T., Virtue S., Gopalacharyulu P., Tang J., Rodriguez-Cuenca S., Maciejewski A., Naukkarinen J., Ruskeepaa A.L., Niemela P.S., Yetukuri L., Tan C.Y., Velagapudi V., Castillo S., Nygren H., Hyotylainen T., Rissanen A., Kaprio J., Yki-Jarvinen H., Vattulainen I., Vidal-Puig A., Oresic M. Association of lipidome remodeling in the adipocyte membrane with acquired obesity in humans. PLoS Biol. 2011, 9(6):e1000623.