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Proteomic Analysis Reveals PGAM1 Altering cis-9, trans-11 Conjugated Linoleic Acid Synthesis in Bovine Mammary Gland

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Lipids

Abstract

cis-9, trans-11 Conjugated linoleic acid (CLA) is one of the most extensively studied CLA isomers due to its multiple isomer-specific effects. However, the molecular mechanisms of cis-9,trans-11 CLA synthesis in ruminant mammary gland are still not clearly understood. This process may be mediated, to a certain extent, by trans-11 C18:1 regulated by stearoyl-CoA desaturase-1 (SCD1) and/or its syntrophic proteins. This study aimed to investigate the effects of TVA on SCD1-mediated cis-9,trans-11 CLA synthesis in MAC-T cells and its potential molecular mechanism. Results showed that trans-11 C18:1 was continually taken up and converted into cis-9,trans-11 CLA in MAC-T cells during the 4-h incubation of 50 μM trans-11 C18:1. SCD1 protein expression increased more than twofold at 2 h (P < 0.01) and 2.5 h (P < 0.05) before decreasing to less than half of the normal level at 4 h (P < 0.05). One up-regulated (RAS guanyl releasing protein 4 isoform 1 [RASGRP4]) and six down-regulated proteins (glucosamine-6-phosphate deaminase 1 [GNPDA1], triosephosphate isomerase [TPI1], phosphoglycerate mutase 1 [PGAM1], heat shock protein beta-1 [HSPB1], annexin A3 [ANXA3], thiopurine S-methyltransferase [TPMT]) were found in MAC-T cells treated with trans-11 C18:1. Of these seven identified proteins, the presence of GNPDA1 and PGAM1 was verified in several models. More trans-11 C18:1 was taken up after PGAM1 knockdown by small interfering RNA (siRNA). In conclusion, our data suggested that PGAM1 may have a negative relationship with SCD1 and seemed to be involved in cis-9, trans-11 CLA synthesis by facilitating the absorption of trans-11 C18:1 in the bovine mammary gland.

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Abbreviations

ANXA3:

Annexin A3

cis-9,trans-11 CLA:

cis-9, trans-11 conjugated linoleic acid

GNPDA1:

Glucosamine-6-phosphate deaminase 1

HSPB1:

Heat shock protein beta-1

MEC:

Milk epithelial cell

PGAM1:

Phosphoglycerate mutase 1

RASGRP4:

RAS guanyl releasing protein 4 isoform 1

SCD1:

Stearoyl-CoA desaturase 1

TPI1:

Triosephosphate isomerase

TPMT:

Thiopurine S-methyltransferase

TVA:

trans-11 C18:1

References

  1. Wang T, Lee HG (2015) Advances in research on cis-9,trans-11 conjugated linoleic acid: a major functional conjugated linoleic acid isomer. Crit Rev Food Sci 55(5):720–731

    Article  CAS  Google Scholar 

  2. Benjamin S, Spener F (2009) Conjugated linoleic acids as functional food: an insight into their health benefits. Nutr Metab 6:36

    Article  Google Scholar 

  3. Dhiman TR, Nam SH, Ure AL (2005) Factors affecting conjugated linoleic acid content in milk and meat. Crit Rev Food Sci 45:463–482

    Article  CAS  Google Scholar 

  4. Kay JK, Mackle TR, Auldist MJ, Thomson NA, Bauman DE (2004) Endogenous synthesis of cis-9,trans-11 conjugated linoleic acid in dairy cows fed fresh pasture. J Dairy Sci 87:369–378

    Article  CAS  PubMed  Google Scholar 

  5. Bauman DE, Baumgard LH, Corl BA, Griinari JM (2000) Biosynthesis of conjugated linoleic acid in ruminants. J Anim Sci 77:1–15

    Google Scholar 

  6. Lengi AJ, Corl BA (2007) Identification and characterization of a novel bovine stearoyl-CoA desaturase isoform with homology to human SCD5. Lipids 42:499–508

    Article  CAS  PubMed  Google Scholar 

  7. Jacobs AAA (2011) Nutritional regulation of stearoyl-CoA desaturase in the bovine mammary gland (PhD Thesis). Wageningen University, Wageningen

    Google Scholar 

  8. Wang T, Oh JJ, Lim JN, Hong JE, Kim JH, Kim JH, Kang HS, Choi YJ, Lee HG (2013) Effects of lactation stage and individual performance on milk cis-9,trans-11 conjugated linoleic acids content in dairy cows. Asian Austral J Anim 26:189–194

    Article  CAS  Google Scholar 

  9. Wang T, Lim JN, Bok JD, Kim JH, Kang SK, Lee SB, Hwang JH, Lee KH, Kang HS, Choi YJ, Kim EJ, Lee HG (2014) Association of protein expression in isolated milk epithelial cells and cis-9,trans-11 CLA concentrations in milk from dairy cows. J Sci Food Agr 94(9):1835–1843

    Article  CAS  Google Scholar 

  10. Liu G, Lynch JK, Freeman J, Liu B, Xin Z, Zhao H, Serby MD, Kym PR, Suhar TS, Smith HT, Cao N, Yang R, Janis RS, Krauser JA, Cepa SP, Beno DW, Sham HL, Collins CA, Surowy TK, Camp HS (2007) Discovery of potent, selective, orally bioavailable stearoyl-CoA desaturase one inhibitors. J Med Chem 50:3086–3100

    Article  CAS  PubMed  Google Scholar 

  11. Boutinaud M, Ben Chedly MH, Delamaire E, Guinard-Flament J (2008) Milking and feed restriction regulate transcripts of mammary epithelial cells purified from milk. J Dairy Sci 91:988–998

    Article  CAS  PubMed  Google Scholar 

  12. Wang T, Lee HG, Hwang JH, Oh JJ, Lim JN, Kang HS, Joo JK, Lee KS (2013) Myoglobin: an exogenous reference marker for proteomics analysis. Food Sci Biotechnol 22:393–398

    Article  CAS  Google Scholar 

  13. Mosley EE, Shafii B, Moate PJ, McGuire MA (2006) cis-9,trans-11 conjugated linoleic acid is synthesized directly from vaccenic acid in lactating dairy cattle. J Nutr 136:570–575

    CAS  PubMed  Google Scholar 

  14. Jin YC, Lee HG, Xu CX, Han JA, Choi SH, Song MK, Kim YJ, Lee KB, Kim SK, Kang HS, Cho BW, Shin TS, Choi YJ (2010) Proteomic analysis of endogenous conjugated linoleic acid biosynthesis in lactating rats and mouse mammary gland epithelia cells (HC11). Biochim Biophys Acta 1804(4):745–751

    Article  CAS  PubMed  Google Scholar 

  15. Lin XB, Loor JJ, Herbein JH (2004) trans10,cis12-18:2 is a more potent inhibitor of de novo fatty acid synthesis and desaturation than cis9, trans11-18:2 in the mammary gland of lactating mice. J Nutr 134:1362–1368

    CAS  PubMed  Google Scholar 

  16. Jin YC, Li ZH, Hong ZS, Xu CX, Han JA, Choi SH, Yin JL, Zhang QK, Lee KB, Kang SK, Song MK, Kim YJ, Kang HS, Choi YJ, Lee HG (2012) Conjugated linoleic acid synthesis-related protein proteasome subunit α 5 (PSMA5) is increased by vaccenic acid treatment in goat mammary tissue. J Dairy Sci 95(8):4286–4297

    Article  CAS  PubMed  Google Scholar 

  17. Yang Y, Li L, Wong GW, Krillis SA, Madhusudhan MS, Sali A, Stevens RL (2002) RasGRP4, a new mast cell-restricted Ras guanine nucleotide-releasing with calcium- and diacylglycerol-binding motifs. J Biol Chem 277:25756–25774

    Article  CAS  PubMed  Google Scholar 

  18. Nathanson NM (1990) G proteins and signal transduction. The Rockefeller University Press, New York

    Google Scholar 

  19. Neves SR, Ram PT, Iyengar R (2002) G protein pathways. Science 296:1636–1639

    Article  CAS  PubMed  Google Scholar 

  20. Comb DG, Roseman S (1958) Glucosamine metabolism. 4 glucosamine 6-phosphate deaminase. J Biol Chem 232:807–827

    CAS  PubMed  Google Scholar 

  21. Champe PC, Harve RA, Ferrier DR (2008) Biochemistry, 4th edn. Lippincott Williams & Wilkins, Philadelphia

    Google Scholar 

  22. Jogl G, Rozovsky S, McDermott AE, Tong L (2003) Optimal alignment for enzymatic proton transfer: structure of the Michaelis complex of triosephosphate isomerase at 1.2-A resolution. Proc Natl Acad Sci 100:50–55

    Article  PubMed Central  PubMed  Google Scholar 

  23. Seigle JL, Celotto AM, Palladino MJ (2008) Degradation of functional triose phosphate isomerase protein underlies sugarkill pathology. Genetics 179:855–862

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  24. Fothergill-Gilmore LA, Watson HC (1989) The phosphoglycerate mutases. Adv Enzymol Relat Areas Mol Biol 62:227–313

    CAS  PubMed  Google Scholar 

  25. Hallows WC, Yu W, Denu JM (2012) Regulation of glycolytic enzyme phosphoglycerate mutase-1 by Sirt1-mediated deacetylation. J Biol Chem 287:3850–3858

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  26. Ross TS, Tait JF, Majerus PW (1990) Identity of inositol 1,2-cyclic phosphate 2-phosphohydrolase with lipocortin III. Science 248:605–607

    Article  CAS  PubMed  Google Scholar 

  27. Park JE, Lee DH, Lee JA, Park SG, Kim NS, Park BC, Cho S (2005) Annexin A3 is a potential angiogenic mediator. Biochem Biophys Res Commun 337:1283–1287

    Article  CAS  PubMed  Google Scholar 

  28. Kim S, Ko J, Kim JH, Choi EC, Na DS (2001) Differential effects of annexins I, II, III, and V on cytosolic phospholipase A2 activity: specific interaction model. FEBS Letter 489:243–248

    Article  CAS  Google Scholar 

  29. Rothhut B (1997) Participation of annexins in protein phosphorylation. Cell Mol Life Sci 53:522–526

    Article  CAS  PubMed  Google Scholar 

  30. Ciocca DR, Oesterreich S, Chamness GC, MCGuire WL, Fuqua SAW (1993) Biological and clinical implications of heat shock protein 27000 (Hsp27): a review. J Natl Cancer Inst 85:1558–1570

    Article  CAS  PubMed  Google Scholar 

  31. Garrido C (2000) Size matters: of the small HSP27 and its large oligomers. Cell Death Differ 9:483–485

    Article  Google Scholar 

  32. Pandey P, Farber R, Nakazawa A, Kumar S, Bharti A, Nalin C, Weichselbaum R, Kufe D, Kharbanda S (2000) Hsp27 functions as a negative regulator of cytochrome c-dependent activation of procaspase-3. Oncogene 19:1975–1981

    Article  CAS  PubMed  Google Scholar 

  33. Paul C, Manero F, Gonin S, Kretz-Remy C, Virot S, Arrigo AP (2002) Hsp27 as a negative regulator of cytochrome c release. Mol Cell Biol 22:816–834

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  34. Das PM, Singal R (2004) DNA methylation and cancer. J Clin Oncol 22:4632–4642

    Article  CAS  PubMed  Google Scholar 

  35. Lee DY, Teyssier C, Strahl BD, Stallcup MR (2005) Role of protein methylation in regulation of transcription. Endocr Rev 26:147–170

    Article  CAS  PubMed  Google Scholar 

  36. Tai HL, Krynetski EY, Yates CR, Loennechen T, Fessing MY, Krynetskaia NF, Evans WE (1996) Thiopurine S-methyltransferase deficiency: two nucleotide transitions define the most prevalent mutant allele associated with loss of catalytic activity in Caucasians. Am J Hum Gen 58:694–702

    CAS  Google Scholar 

  37. Szumlanski CL, Weinshilboum RM (1995) Sulphasalazine inhibition of thiopurine methyltransferase: possible mechanism for interaction with 6-mercaptopurine and azathioprine. Brit J Clin Pharmacol 39:456–459

    Article  CAS  Google Scholar 

  38. Bolduc C, Larose M, Yoshioka M, Ye P, Belleau P, Labrie C, Morissette J, Raymond V, Labrie F, St-Amand J (2004) Effects of dihydrotestosterone on adipose tissue measured by serial analysis of gene expression. J Mol Endocrinol 33:429–444

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported by iPET (Korea Institute of Planning and Evaluation for Technology in Food, Agriculture, Forestry and Fisheries), Ministry of Agriculture, Food and Rural Affairs, Republic of Korea (Project No. 112027-01-1-SB010 and 313002-03-2-WT011) and project funding by the China Postdoctoral Science Foundation (Project No. 2014M550177).

Conflict of interest

There is no conflict of interest.

Author information

Authors and Affiliations

  1. College of Animal Science and Technology, Jilin Agricultural University, Changchun, 130118, Jilin Province, People’s Republic of China

    T. Wang

  2. Key Laboratory of Animal Nutrition and Feed Science of Jilin Province, Jilin Agricultural University, Changchun, 130118, Jilin Province, People’s Republic of China

    T. Wang

  3. Department of Animal Science and Technology, College of Animal Bioscience and Technology, Konkuk University, Seoul, 143-701, South Korea

    S. B. Lee, J. H. Hwang, J. N. Lim, U. S. Jung, M. J. Kim, J. S. Lee & H. G. Lee

  4. College of Natural Resources and Life Science, Pusan National University, Miryang, Gyeongnam-do, 627-706, South Korea

    H. S. Kang

  5. Department of Animal Science, Chungbuk National University, Cheongju, Chungcheongbuk-do, 361-763, South Korea

    S. H. Choi

  6. Lab of Animal Physiology, Graduate School of Agriculture Science, Tohoku University, Sendai, Miyagi-ken, 988-8555, Japan

    S. G. Roh

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  1. T. Wang
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Correspondence to H. G. Lee.

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Wang, T., Lee, S.B., Hwang, J.H. et al. Proteomic Analysis Reveals PGAM1 Altering cis-9, trans-11 Conjugated Linoleic Acid Synthesis in Bovine Mammary Gland. Lipids 50, 469–481 (2015). https://doi.org/10.1007/s11745-015-4009-9

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