Advertisement

Dietary uptake of omega-3 fatty acids in mouse tissue studied by time-of-flight secondary ion mass spectrometry (TOF-SIMS)

Abstract

Dietary intake of omega-3 fatty acids is associated with considerable health benefits, including the prevention of metabolic disorders such as cardiovascular disease and type 2 diabetes. Furthermore, incorporation of the main omega-3 fatty acids, eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA), at the systemic level has been found to be more efficient when these fatty acids are supplied in the form of marine phospholipids compared to triglycerides. In this work, the uptake of omega-3 fatty acids and their incorporation in specific lipids were studied in adipose, skeletal muscle, and liver tissues of mice given high-fat diets with or without omega-3 supplements in the form of phospholipids or triglycerides using time-of-flight secondary ion mass spectrometry (TOF-SIMS). The results demonstrate significant uptake of EPA and DHA, and the incorporation of these fatty acids in specific lipid molecules, in all three tissue types in response to the dietary omega-3 supplements. Moreover, the results indicate reduced concentrations of arachidonic acid (AA) and depletion of lipids containing AA in tissue samples from mice given supplementary omega-3, as compared to the control mice. The effect on the lipid composition, in particular the DHA uptake and AA depletion, was found to be significantly stronger when the omega-3 supplement was supplied in the form of phospholipids, as compared to triglycerides. TOF-SIMS was found to be a useful technique for screening the lipid composition and simultaneously obtaining the spatial distributions of various lipid classes on tissue surfaces.

Lipid-specific analysis of TOF-SIMS spectra was used to study dietary uptake of omega-3 fatty acids in mouse adipose, muscle and liver tissue. Ion images shows the lateral distribution of molecular species, herephosphocholine (red), protein fragment (green) and diacylglycerol (blue), on the tissue surfaces

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. 1.

    Bich C, Touboul D, Brunelle A (2014) Mass Spectrom Rev 33:442–451

  2. 2.

    Fletcher JS, Vickerman JC (2013) Anal Chem 85:610–639

  3. 3.

    Kraft ML, Klitzing HA (2014) Biochim Biophys Acta Mol Cell Biol Lipids 1841:1108–1119

  4. 4.

    Passarelli MK, Winograd N (2011) Biochim Biophys Acta Mol Cell Biol Lipids 1811:976–990

  5. 5.

    Carlred L, Gunnarsson A, Sole-Domenech S, Johansson B, Vukojevic V, Terenius L, Codita A, Winblad B, Schalling M, Hook F, Sjovall P (2014) J Am Chem Soc 136:9973–9981

  6. 6.

    Lazar AN, Bich C, Panchal M, Desbenoit N, Petit VW, Touboul D, Dauphinot L, Marquer C, Laprevote O, Brunelle A, Duyckaerts C (2013) Acta Neuropathol 125:133–144

  7. 7.

    Sole-Domenech S, Sjovall P, Vukojevic V, Fernando R, Codita A, Salve S, Bogdanovic N, Mohammed AH, Hammarstrom P, Nilsson KPR, LaFerla FM, Jacob S, Berggren PO, Gimenez-Llort L, Schalling M, Terenius L, Johansson B (2013) Acta Neuropathol 125:145–157

  8. 8.

    Hanrieder J, Ewing AG (2014) Scientific reports 4

  9. 9.

    Desbenoit N, Saussereau E, Bich C, Bourderioux M, Fritsch J, Edelman A, Brunelle A, Ollero M (2014) Int J Biochem Cell Biol 52:77–82

  10. 10.

    Debois D, Bralet MP, Le Naour F, Brunelle A, Laprevote O (2009) Anal Chem 81:2823–2831

  11. 11.

    Sjovall P, Johansson B, Belazi D, Stenvinkel P, Lindholm B, Lausmaa J, Schalling M (2008) Appl Surf Sci 255:1177–1180

  12. 12.

    Sjovall P, Greve TM, Clausen SK, Moller K, Eirefelt S, Johansson B, Nielsen KT (2014) Anal Chem 86:3443–3452

  13. 13.

    Hanrieder J, Gerber L, Sandelius AP, Brittebo EB, Ewing AG, Karlsson O (2014) ACS Chem Neurosci 5:568–575

  14. 14.

    Kurczy ME, Piehowski PD, Van Bell CT, Heien ML, Winograd N, Ewing AG (2010) Proc Natl Acad Sci U S A 107:2751–2756

  15. 15.

    Seyer A, Cantiello M, Bertrand-Michel J, Roques V, Nauze M, Bezirard V, Collet X, Touboul D, Brunelle A, Comera C (2013) Plos One 8

  16. 16.

    Tian H, Fletcher JS, Thuret R, Henderson A, Papalopulu N, Vickerman JC, Lockyer NP (2014) J Lipid Res 55

  17. 17.

    Bich C, Havelund R, Moellers R, Touboul D, Kollmer F, Niehuis E, Gilmore IS, Brunelle A (2013) Anal Chem 85:7745–7752

  18. 18.

    Fletcher JS, Vickerman JC (2010) Anal Bioanal Chem 396:85–104

  19. 19.

    Rabbani S, Barber AM, Fletcher JS, Lockyer NP, Vickerman JC (2011) Anal Chem 83:3793–3800

  20. 20.

    Han XL, Yang K, Gross RW (2012) Mass Spectrom Rev 31:134–178

  21. 21.

    Kawashima T, Kurosawa T, Aoyagi S, Sheraz S, Fletcher JS, Futigami M, Lockyer NP, Vickerman JC (2014) Surf Interface Anal 46:92–95

  22. 22.

    Kopelman PG (2000) Nature 404:635–643

  23. 23.

    Bilato C (2013) Aging Clin Exp Res 25:357–363

  24. 24.

    Mozaffarian D, Rimm EB (2006) JAMA 296:1885–1899

  25. 25.

    Sell H, Habich C, Eckel J (2012) Nat Rev Endocrinol 8:709–716

  26. 26.

    Van Gaal LF, Mertens IL, De Block CE (2006) Nature 444:875–880

  27. 27.

    Flachs P, Mohamed-Ali V, Horakova O, Rossmeisl M, Hosseinzadeh-Attar MJ, Hensler M, Ruzickova J, Kopecky J (2006) Diabetologia 49:394–397

  28. 28.

    Jelenik T, Rossmeisl M, Kuda O, Jilkova ZM, Medrikova D, Kus V, Hensler M, Janovska P, Miksik I, Baranowski M, Gorski J, Hebrard S, Jensen TE, Flachs P, Hawley S, Viollet B, Kopecky J (2010) Diabetes 59:2737–2746

  29. 29.

    Rossmeisl M, Jelenik T, Jilkova Z, Slamova K, Kus V, Hensler M, Medrikova D, Povysil C, Flachs P, Mohamed-Ali V, Bryhn M, Berge K, Holmeide AK, Kopecky J (2009) Obesity (Silver Spring) 17:1023–1031

  30. 30.

    Rossmeisl M, Jilkova ZM, Kuda O, Jelenik T, Medrikova D, Stankova B, Kristinsson B, Haraldsson GG, Svensen H, Stoknes I, Sjovall P, Magnusson Y, Balvers MGJ, Verhoeckx KCM, Tvrzicka E, Bryhn M, Kopecky J (2012) Plos One 7

  31. 31.

    Rossmeisl M, Medrikova D, van Schothorst EM, Pavlisova J, Kuda O, Hensler M, Bardova K, Flachs P, Stankova B, Vecka M, Tvrzicka E, Zak A, Keijer J, Kopecky J (2014) Biochim Biophys Acta 1841:267–278

  32. 32.

    Ruzickova J, Rossmeisl M, Prazak T, Flachs P, Sponarova J, Veck M, Tvrzicka E, Bryhn M, Kopecky J (2004) Lipids 39:1177–1185

  33. 33.

    Storlien LH, Kraegen EW, Chisholm DJ, Ford GL, Bruce DG, Pascoe WS (1987) Science 237:885–888

  34. 34.

    Todoric J, Loffler M, Huber J, Bilban M, Reimers M, Kadl A, Zeyda M, Waldhausl W, Stulnig TM (2006) Diabetologia 49:2109–2119

  35. 35.

    Flachs P, Rossmeisl M, Kopecky J (2014) Physiol Res 63(Suppl 1):S93–S118

  36. 36.

    Sampath H, Ntambi JM (2005) Annu Rev Nutr 25:317–340

  37. 37.

    Sanderson LM, de Groot PJ, Hooiveld GJ, Koppen A, Kalkhoven E, Muller M, Kersten S (2008) PLoS One 3:e1681

  38. 38.

    Flachs P, Rossmeisl M, Bryhn M, Kopecky J (2009) Clin Sci (Lond) 116:1–16

  39. 39.

    Banni S, Di Marzo V (2010) Mol Nutr Food Res 54:82–92

  40. 40.

    Serhan CN (2014) Nature 510:92–101

  41. 41.

    Maki KC, Reeves MS, Farmer M, Griinari M, Berge K, Vik H, Hubacher R, Rains TM (2009) Nutr Res 29:609–615

  42. 42.

    Schuchardt JP, Hahn A (2013) Prostaglandins Leukot Essent Fat Acids 89:1–8

  43. 43.

    Ulven SM, Kirkhus B, Lamglait A, Basu S, Elind E, Haider T, Berge K, Vik H, Pedersen JI (2011) Lipids 46:37–46

  44. 44.

    Sjovall P, Johansson B, Lausmaa J (2006) Appl Surf Sci 252:6966–6974

  45. 45.

    Schuchardt JP, Schneider I, Meyer H, Neubronner J, von Schacky C, Hahn A (2011) Lipids Health Dis 10:145

  46. 46.

    Bluher M, Engeli S, Kloting N, Berndt J, Fasshauer M, Batkai S, Pacher P, Schon MR, Jordan J, Stumvoll M (2006) Diabetes 55:3053–3060

  47. 47.

    Di Marzo V (2008) Diabetologia 51:1356–1367

  48. 48.

    Alvheim AR, Malde MK, Osei-Hyiaman D, Lin YH, Pawlosky RJ, Madsen L, Kristiansen K, Froyland L, Hibbeln JR (2012) Obesity (Silver Spring) 20:1984–1994

  49. 49.

    Osei-Hyiaman D, Liu J, Zhou L, Godlewski G, Harvey-White J, Jeong WI, Batkai S, Marsicano G, Lutz B, Buettner C, Kunos G (2008) J Clin Invest 118:3160–3169

  50. 50.

    Kuda O, Jelenik T, Jilkova Z, Flachs P, Rossmeisl M, Hensler M, Kazdova L, Ogston N, Baranowski M, Gorski J, Janovska P, Kus V, Polak J, Mohamed-Ali V, Burcelin R, Cinti S, Bryhn M, Kopecky J (2009) Diabetologia 52:941–951

  51. 51.

    Storlien LH, Jenkins AB, Chisholm DJ, Pascoe WS, Khouri S, Kraegen EW (1991) Diabetes 40:280–289

Download references

Acknowledgments

We are grateful to Ylva Magnusson for assistance in the preparation of tissue sections. This study was supported by grants from the Czech Science Foundation (14-09347S, to M.R.) and VINNOVA Swedish Governmental Agency for Innovation Systems (P.S.).

Author information

Correspondence to Peter Sjövall.

Additional information

Published in the topical collection Lipidomics with guest editor Michal Holčapek.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 2.78 mb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Sjövall, P., Rossmeisl, M., Hanrieder, J. et al. Dietary uptake of omega-3 fatty acids in mouse tissue studied by time-of-flight secondary ion mass spectrometry (TOF-SIMS). Anal Bioanal Chem 407, 5101–5111 (2015). https://doi.org/10.1007/s00216-015-8515-7

Download citation

Keywords

  • Omega-3
  • TOF-SIMS
  • Mouse tissue
  • Lipids
  • Imaging
  • PCA