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Metabolism of sn-1(3)-Monoacylglycerol and sn-2-Monoacylglycerol in Caecal Enterocytes and Hepatocytes of Brown Trout (Salmo trutta)

  • Original Article
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Lipids

Abstract

sn-2-Monoacylglycerol (2-MAG) and sn-1(3)-monoacylglycerol [1(3)-MAG] are important but yet little studied intermediates in lipid metabolism. The current study compared the metabolic fate of 2-MAG and 1(3)-MAG in isolated caecal enterocytes and hepatocytes of brown trout (Salmo trutta). 1(3)-Oleoyl [9,10-3H(N)]-glycerol and 2-Oleoyl [9,10-3H(N)]-glycerol were prepared by pancreatic lipase digestion of triolein [9,10-3H(N)]. The 1(3)-MAG and 2-MAG were efficiently absorbed by enterocytes and hepatocytes at similar rates. The 2-MAG was quickly resynthesized into TAG through the monoacylglycerol acyltransferase (EC: 2.3.1.22, MGAT) pathway in both tissues, whereas 1(3)-MAG was processed into TAG and phospholipids at a much slower rate, suggesting 2-MAG was the preferred substrates for MGAT. Further analysis showed that 1(3)-MAG was synthesized into 1,3-DAG, but there were no accumulation of 1,3-DAG in either enterocytes or hepatocytes, which contrasts that of mammalian studies. Some of the 1(3)-MAG may be acylated to 1,2(2,3)-DAG and then utilized for TAG synthesis. Alternatively, 1(3)-MAG can be hydrolyzed to free fatty acid and glycerol, and re-synthesized into TAG through the glycerol-3-phosphate (Gro-3-P) pathway. The overall data suggested that the limiting step of the intracellular 1(3)-MAG metabolism is the conversion of 1(3)-MAG itself.

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Abbreviations

1(3)-MAG:

sn-1(3)-Monoacylglycerol

1,2(2,3)-DAG:

sn-1,2(2,3)-Diacylglycerol

1,3-DAG:

sn-1,3-Diacylglycerol

1-MAG:

sn-1-Monoacylglycerol

2-MAG:

sn-2-Monoacylglycerol

BSDL:

Bile salt-dependent lipase

DAG:

Diacylglycerol(s)

DGAT:

Diacylglycerol acyltransferase

FAF-BSA:

Fatty acid free bovine serum albumin

FFA:

Unesterified fatty acids

Gro-3-P:

Glycerol-3-phosphate

HBSS:

Hank’s balanced salt solution

HPTLC:

High performance thin layer chromatography

lysoPtdOH:

Lysophosphatidic acid

MAG:

Monoacylglycerol(s)

MEM:

Minimum essential medium

MGAT:

Monoacylglycerol acyltransferase

MGL:

Monoacylglycerol lipase

MS222:

Tricaine methanesulfonate

PtdCho:

Phosphatidylcholine

PtdEtn:

Phosphatidylethanolamine

PtdIns:

Phosphatidylinositol

PtdOH:

Phosphatidic acid

PtdSer:

Phosphatidylserine

TAG:

Triacylglycerol(s)

References

  1. Decaro A, Figarella C, Amic J, Michel R, Guy O (1977) Human pancreatic lipase—glycoprotein. Biochim Biophys Acta 490:411–419

    Article  CAS  Google Scholar 

  2. Mattson FH, Volpenhein RA (1964) The digestion and absorption of triglycerides. J Biol Chem 239:2772–2777

    CAS  PubMed  Google Scholar 

  3. Mattson FH, Volpenhein RA (1968) Hydrolysis of primary and secondary esters of glycerol by pancreatic juice. J Lipid Res 9:79–84

    CAS  PubMed  Google Scholar 

  4. Wang CS, Kuksis A, Manganaro F, Myher JJ, Downs D, Bass HB (1983) Studies on the substrate specificity of purified human milk bile salt-activated lipase. J Biol Chem 258:9197–9202

    CAS  PubMed  Google Scholar 

  5. Lombardo D (2001) Bile salt-dependent lipase: its pathophysiological implications. BBA-Mol Cell Biol Lipids 1533:1–28

    Article  CAS  Google Scholar 

  6. Olsen RE, Ringø E (1997) Lipid digestibility in fish: a review. Recent Res Dev Lipid Res 1:199–265

    CAS  Google Scholar 

  7. Tocher DR, Sargent JR (1984) Studies on triacylglycerol, wax ester and sterol ester hydrolases in intestinal ceca of rainbow trout (Salmo gairdneri) fed diets rich in triacylglycerols and wax esters. Comp Biochem Physio 77:561–571

    Google Scholar 

  8. Iijima N, Tanaka S, Ota Y (1998) Purification and characterization of bile salt-activated lipase from the hepatopancreas of red sea bream, Pagrus major. Fish Physiol Biochem 18:59–69

    Article  CAS  Google Scholar 

  9. Bogevik AS, Tocher DR, Waagbo R, Olsen RE (2008) Triacylglycerol-, wax ester- and sterol ester-hydrolases in midgut of Atlantic salmon (Salmo salar). Aquac Nutr 14:93–98

    Article  CAS  Google Scholar 

  10. Bogevik AS, Oxley A, Olsen RE (2008) Hydrolysis of acyl-homogeneous and fish oil triacylglycerols using desalted midgut extract from Atlantic salmon, Salmo salar. Lipids 43:655–662

    Article  CAS  PubMed  Google Scholar 

  11. Gjellesvik DR (1991) Fatty acid specificity of bile salt-dependent lipase enzyme recognition and super-substrate effects. Biochim Biophys Acta 1086:167–172

    Article  CAS  PubMed  Google Scholar 

  12. Gjellesvik DR, Lombardo D, Walther BT (1992) Pancreatic bile salt dependent lipase from cod (Gadus morhua) purification and properties. Biochim Biophys Acta 1124:123–134

    Article  CAS  PubMed  Google Scholar 

  13. Lehner R, Kuksis A (1996) Biosynthesis of triacylglycerols. Prog Lipid Res 35:169–201

    Article  CAS  PubMed  Google Scholar 

  14. Oxley A, Torstensen BE, Rustan AC, Olsen RE (2005) Enzyme activities of intestinal triacylglycerol and phosphatidylcholine biosynthesis in Atlantic salmon (Salmo salar L.). Comp Biochem Physiol B-Biochem Mol Biol 141:77–87

    Article  PubMed  Google Scholar 

  15. Oxley A, Jutfelt F, Sundell K, Olsen RE (2007) Sn-2-monoacylglycerol, not glycerol, is preferentially utilised for triacylglycerol and phosphatidylcholine biosynthesis in Atlantic salmon (Salmo salar L.) intestine. Comp Biochem Physiol B-Biochem Mol Biol 146:115–123

    Article  PubMed  Google Scholar 

  16. Caballero MJ, Gallardo G, Robaina L, Montero D, Fernandez A, Izquierdo M (2006) Vegetable lipid sources affect in vitro biosynthesis of triacylglycerols and phospholipids in the intestine of sea bream (Sparus aurata). Br J Nutr 95:448–454

    Article  CAS  PubMed  Google Scholar 

  17. Li KS, Olsen RE, Ostensen MA, Altin D, Kjorsvik E, Olsen Y (2016) Atlantic cod (Gadus morhua) larvae can biosynthesis phospholipid de novo from 2-oleoyl-glycerol and glycerol precursors. Fish Physiol Biochem 42:137–147

    Article  CAS  PubMed  Google Scholar 

  18. Senior JR, Isselbacher KJ (1963) Demonstration of an intestinal monoglyceride lipase: an enzyme with a possible role in the intracellular completion of fat digestion. J Clin Invest 42:187–195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. De Jong B, Hülsmann W (1978) Monoacylglycerol hydrolase activity of isolated rat small intestinal epithelial cells. BBA-Lipid Lipid Metab 528:36–46

    Article  Google Scholar 

  20. Yen CLE, Farese RV (2003) MGAT2, a monoacylglycerol acyltransferase expressed in the small intestine. J Biol Chem 278:18532–18537

    Article  CAS  PubMed  Google Scholar 

  21. Cao JS, Lockwood J, Burn P, Shi YG (2003) Cloning and functional characterization of a mouse intestinal Acyl-CoA: monoacylglycerol acyltransferase, MGAT2. J Biol Chem 278:13860–13866

    Article  CAS  PubMed  Google Scholar 

  22. Kondo H, Hase T, Murase T, Tokimitsu I (2003) Digestion and assimilation features of dietary DAG in the rat small intestine. Lipids 38:25–30

    Article  CAS  PubMed  Google Scholar 

  23. Murase T, Aoki M, Wakisaka T, Hase T, Tokimitsu I (2002) Anti-obesity effect of dietary diacylglycerol in C57BL/6 J mice: dietary diacylglycerol stimulates intestinal lipid metabolism. J Lipid Res 43:1312–1319

    CAS  PubMed  Google Scholar 

  24. Hibi M, Takase H, Meguro S, Tokimitsu I (2009) The effects of diacylglycerol oil on fat oxidation and energy expenditure in humans and animals. BioFactors 35:175–177

    Article  CAS  PubMed  Google Scholar 

  25. Tocher DR, Fonseca-Madrigal J, Bell JG, Dick JR, Henderson RJ, Sargent JR (2002) Effects of diets containing linseed oil on fatty acid desaturation and oxidation in hepatocytes and intestinal enterocytes in Atlantic salmon (Salmo salar). Fish Physiol Biochem 26:157–170

    Article  CAS  Google Scholar 

  26. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265–275

    CAS  PubMed  Google Scholar 

  27. Myher J, Kuksis A (1979) Stereospecific analysis of triacylglycerols via racemic phosphatidylcholines and phospholipase C. Can J Biochem 57:117–124

    Article  CAS  PubMed  Google Scholar 

  28. Thomas A III, Scharoun J, Ralston H (1965) Quantitative estimation of isomeric monoglycerides by thin-layer chromatography. J Am Oil Chem Soc 42:789–792

    Article  CAS  Google Scholar 

  29. Christie W (2003) Lipid analysis, isolation, separation and structural analysis of lipids. J Barnes and Associates, Dundee

    Google Scholar 

  30. Folch J, Lees M, Stanley GHS (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226:497–509

    CAS  PubMed  Google Scholar 

  31. Olsen RE, Henderson RJ (1989) The rapid analysis of neutral and polar marine lipids using double-development HPTLC and scanning densitometry. J Exp Mar Biol Ecol 129:189–197

    Article  CAS  Google Scholar 

  32. Ho SY, Delgado L, Storch J (2002) Monoacylglycerol metabolism in human intestinal Caco-2 cells—evidence for metabolic compartmentation and hydrolysis. J Biol Chem 277:1816–1823

    Article  CAS  PubMed  Google Scholar 

  33. Oxley A, Tocher DR, Torstensen BE, Olsen RE (2005) Fatty acid utilisation and metabolism in caecal enterocytes of rainbow trout (Oncorhynchus mykiss) fed dietary fish or copepod oil. BBA-Mol Cell Biol Lipids 1737:119–129

    Article  CAS  Google Scholar 

  34. Diaz-Lopez M, Perez MJ, Acosta NG, Jerez S, Dorta-Guerra R, Tocher DR, Lorenzo A, Rodriguez C (2010) Effects of dietary fish oil substitution by Echium oil on enterocyte and hepatocyte lipid metabolism of gilthead seabream (Sparus aurata L.). Comp Biochem Physiol B-Biochem Mol Biol 155:371–379

    Article  PubMed  Google Scholar 

  35. Hiramine Y, Emoto H, Takasuga S, Hiramatsu R (2010) Novel acyl-coenzyme A: monoacylglycerol acyltransferase plays an important role in hepatic triacylglycerol secretion. J Lipid Res 51:1424–1431

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Young SG, Zechner R (2013) Biochemistry and pathophysiology of intravascular and intracellular lipolysis. Genes Dev 27:459–484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Chon SH, Zhou YX, Dixon JL, Storch J (2007) Intestinal monoacylglycerol metabolism: developmental and nutritional regulation of monoacylglycerol lipase and monoacylglycerol acyltransferase. J Biol Chem 282:33346–33357

    Article  CAS  PubMed  Google Scholar 

  38. Duncan M, Thomas AD, Cluny NL, Patel A, Patel KD, Lutz B, Piomelli D, Alexander SP, Sharkey KA (2008) Distribution and function of monoacylglycerol lipase in the gastrointestinal tract. Am J Physiol Gastrointest Liver Physiol 295:G1255–G1265

    Article  CAS  PubMed  Google Scholar 

  39. Tornqvist H, Belfrage P (1976) Purification and some properties of a monoacylglycerol-hydrolyzing enzyme of rat adipose tissue. J Biol Chem 251:813–819

    CAS  PubMed  Google Scholar 

  40. Sun J, Ji H, Li XX, Shi XC, Du ZY, Chen LQ (2016) Lipolytic enzymes involving lipolysis in Teleost: synteny, structure, tissue distribution, and expression in grass carp (Ctenopharyngodon idella). Comp Biochem Physiol B Biochem Mol Biol 198:110–118

    Article  CAS  PubMed  Google Scholar 

  41. Lehner R, Kuksis A, Itabashi Y (1993) Stereospecificity of monoacylglycerol and diacylglycerol acyltransferases from rat intestine as determined by chiral phase high-performance liquid chromatography. Lipids 28:29–34

    Article  CAS  PubMed  Google Scholar 

  42. Brown JL, Johnston JM (1964) The mechanism of intestinal utilization of monoglycerides. BBA-Lipid Lipid Metab 84:264–274

    CAS  Google Scholar 

  43. Pieringer RA, Hokin LE (1962) Biosynthesis of lysophosphatidic acid from monoglyceride and adenosine triphosphate. J Biol Chem 237:653–658

    CAS  PubMed  Google Scholar 

  44. Wiggins D, Gibbons GF (1992) The lipolysis/esterification cycle of hepatic triacylglycerol. Its role in the secretion of very-low-density lipoprotein and its response to hormones and sulphonylureas. Biochem J 284(Pt 2):457–462

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by the Norwegian Research Council (Grant No. 245327). The authors wish to thank the staff at NTNU Sealab for excellent technical assistance.

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Correspondence to Keshuai Li.

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Li, K., Olsen, R.E. Metabolism of sn-1(3)-Monoacylglycerol and sn-2-Monoacylglycerol in Caecal Enterocytes and Hepatocytes of Brown Trout (Salmo trutta). Lipids 52, 61–71 (2017). https://doi.org/10.1007/s11745-016-4215-0

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  • DOI: https://doi.org/10.1007/s11745-016-4215-0

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