Kinetics of lipogenic genes expression in milk purified mammary epithelial cells (MEC) across lactation and their correlation with milk and fat yield in buffalo

Research in Veterinary Science

Volumn 99, Issue , 2015, Pages 129-136

  Yadav, Poonam ^a,b   Kumar, Parveen ^c   Mukesh, Manishi ^a   Kataria, R S ^a   Yadav, Anita ^d   Mohanty, A K ^c   Mishra, B P ^a  

^a NATIONAL BUREAU OF ANIMAL GENETIC RESOURCES   (India)

^b DEPARTMENT OF SCIENCE AND TECHNOLOGY   (India)

^c NATIONAL DAIRY RESEARCH INSTITUTE   (India)

^d KURUKSHETRA UNIVERSITY   (India)

Author keywords

Buffalo; Lactation; Lipogenic genes; Mammary epithelial cells; Milk fat

Indexed keywords

3 HYDROXYBUTYRATE DEHYDROGENASE; BREAST CANCER RESISTANCE PROTEIN; LIPOPROTEIN LIPASE; MILK FAT; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; FAT;

3 HYDROXYBUTYRATE DEHYDROGENASE GENE; ACETYL COA CARBOXYLASE ALPHA GENE; ACYL COA SYNTHETASE SHORT CHAIN FAMILY MAMBER 2 GENE; AGRICULTURAL PARAMETERS; ANIMAL CELL; ARTICLE; ATP BINDING CASSETTE SUBFAMILY G MEMBER 2 GENE; BREAST EPITHELIUM CELL; BUFFALO; CONTROLLED STUDY; FAT YIELD; FEMALE; GENE; GENE EXPRESSION; LACTATION; LIPIN1 GENE; LIPOPROTEIN LIPASE GENE; MILK YIELD; NONHUMAN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA GENE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA GENE; STEROL REGULATORY ELEMENT BINDING TRANSCRIPTION FACTOR 1 GENE; STEROYL COA DESATURASE GENE; ANIMAL; CHEMISTRY; EPITHELIUM CELL; GENETICS; KINETICS; METABOLISM; MILK; PHYSIOLOGY; UDDER;

ANIMALS; BUFFALOES; EPITHELIAL CELLS; FATS; FEMALE; GENE EXPRESSION; KINETICS; LACTATION; MAMMARY GLANDS, ANIMAL; MILK;

EID: 84925245878     PISSN: 00345288     EISSN: 15322661     Source Type: Journal    
DOI: 10.1016/j.rvsc.2015.01.003     Document Type: Article

References (77)

1. Abu-Elheiga L., Almarza-Ortega D.B., Baldini A., Wakil S.J. Human acetyl-CoA carboxylase 2. Molecular cloning, characterization, chromosomal mapping, and evidence for two isoforms. Journal of Biological Chemistry 1997, 272:10669-10677.
2. Annen E.L., Stiening C.M., Crooker B.A., Fitzgerald A.C., Collier R.J. Effect of continuous milking and prostaglandin E2 on milk production and mammary epithelial cell turnover, ultrastructure, and gene expression. Journal of Animal Science 2008, 86:1132-1144.
3. Annison E.F. Metabolic utilization by the ruminant mammary gland. Biochemistry of Lactation 1983, 399-436. Elsevier Science Publishers, Amsterdam and New York. T.B. Mepham (Ed.).
4. Aoyama T., Peters J.M., Iritani N., Nakajima T., Furihata K., Hashimoto T., et al. Altered constitutive expression of fatty acid-metabolizing enzymes in mice lacking the peroxisome proliferator-activated receptor alpha (PPARalpha). Journal of Biological Chemistry 1998, 273:5678-5684.
5. Barry J.M., Bartley W., Linzell J.L., Robinson D.S. The uptake from the blood of triglyceride fatty acids of chylomicra and low-density lipoproteins by the mammary gland of the goat. The Biochemical Journal 1963, 89:6-11.
6. Bauchart D. Lipid absorption and transport in ruminants. Journal of Dairy Science 1993, 76:3864-3881.
7. Bauman D.E., Davis C.L. Biosynthesis of milk fat in lactation. A Comprehensive Treatise 1974, 31-75. Academic Press, New York. B.L.L.V.R. Smith (Ed.).
8. Bauman D.E., Mather I.H., Wall R.J., Lock A.L. Major advances associated with the biosynthesis of milk. Journal of Dairy Science 2006, 89:1235-1243.
9. Bengoechea-Alonso M.T., Ericsson J. SREBP in signal transduction: cholesterol metabolism and beyond. Current Opinion in Cell Biology 2007, 19:215-222.
10. Bionaz M., Loor J.J. Gene networks driving bovine milk fat synthesis during the lactation cycle. BMC Genomics 2008, 9:366.
11. Bionaz M., Rodriguez-Zas S.L., Everts R.E., Lewin H.A., Loor J.J. MammOmicsTM: transcript profiling of the mammary gland during the lactation cycle in Holstein cows. Journal of Dairy Science 2007, 272. ADSA-PSA-ASAS-AMPA Joint Annual Meeting.
12. Boutinaud M., Ben Chedly M.H., Delamaire E., Guinard-Flament J. Milking and feed restriction regulate transcripts of mammary epithelial cells purified from milk. Journal of Dairy Science 2008, 91:988-998.
13. Braun J.E., Severson D.L. Regulation of the synthesis, processing and translocation of lipoprotein lipase. The Biochemical Journal 1992, 287(Pt 2):337-347.
14. Brown M.S., Goldstein J.L. The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell 1997, 89:331-340.
15. Camps L., Reina M., Llobera M., Bengtsson-Olivecrona G., Olivecrona T., Vilaro S. Lipoprotein lipase in lungs, spleen, and liver: synthesis and distribution. Journal of Lipid Research 1991, 32:1877-1888.
16. Cohen-Zinder M., Seroussi E., Larkin D.M., Loor J.J., Everts-van der Wind A., Lee J.H., et al. Identification of a missense mutation in the bovine ABCG2 gene with a major effect on the QTL on chromosome 6 affecting milk yield and composition in Holstein cattle. Genome Research 2005, 15:936-944.
17. Desvergne B., Wahli W. Peroxisome proliferator-activated receptors: nuclear control of metabolism. Endocrine Reviews 1999, 20:649-688.
18. Doolittle M.H., Ben-Zeev O. Immunodetection of lipoprotein lipase: antibody production, immunoprecipitation, and western blotting techniques. Methods in Molecular Biology 1999, 109:215-237.
19. Dreyer C., Keller H., Mahfoudi A., Laudet V., Krey G., Wahli W. Positive regulation of the peroxisomal beta-oxidation pathway by fatty acids through activation of peroxisome proliferator-activated receptors (PPAR). Biology of the Cell 1993, 77:67-76.
20. Du X., Kristiana I., Wong J., Brown A.J. Involvement of Akt in ER-to-Golgi transport of SCAP/SREBP: a link between a key cell proliferative pathway and membrane synthesis. Molecular Biology of the Cell 2006, 17:2735-2745.
21. Eberle D., Hegarty B., Bossard P., Ferre P., Foufelle F. SREBP transcription factors: master regulators of lipid homeostasis. Biochimie 2004, 86:839-848.
22. Ejendal K.F., Hrycyna C.A. Multidrug resistance and cancer: the role of the human ABC transporter ABCG2. Current Protein & Peptide Science 2002, 3:503-511.
23. Enoch H.G., Catala A., Strittmatter P. Mechanism of rat liver microsomal stearyl-CoA desaturase. Studies of the substrate specificity, enzyme-substrate interactions, and the function of lipid. Journal of Biological Chemistry 1976, 251:5095-5103.
24. Farke C., Meyer H.H., Bruckmaier R.M., Albrecht C. Differential expression of ABC transporters and their regulatory genes during lactation and dry period in bovine mammary tissue. Journal of Dairy Research 2008, 75:406-414.
25. Finck B.N., Gropler M.C., Chen Z., Leone T.C., Croce M.A., Harris T.E., et al. Lipin 1 is an inducible amplifier of the hepatic PGC-1alpha/PPARalpha regulatory pathway. Cell Metabolism 2006, 4:199-210.
26. Glascock R.F., Welch V.A. Contribution of the fatty acids of three low density serum lipoproteins to bovine milk fat. Journal of Dairy Science 1974, 57:1364-1370.
27. Gottesman M.M., Fojo T., Bates S.E. Multidrug resistance in cancer: role of ATP-dependent transporters. Nature Reviews. Cancer 2002, 2:48-58.
28. Guerre-Millo M., Gervois P., Raspe E., Madsen L., Poulain P., Derudas B., et al. Peroxisome proliferator-activated receptor alpha activators improve insulin sensitivity and reduce adiposity. Journal of Biological Chemistry 2000, 275:16638-16642.
29. Hamosh M., Clary T.R., Chernick S.S., Scow R.O. Lipoprotein lipase activity of adipose and mammary tissue and plasma triglyceride in pregnant and lactating rats. Biochimica et Biophysica Acta 1970, 210:473-482.
30. Han L.Q., Li H.J., Wang Y.Y., Zhu H.S., Wang L.F., Guo Y.J., et al. mRNA abundance and expression of SLC27A, ACC, SCD, FADS, LPIN, INSIG, and PPARGC1 gene isoforms in mouse mammary glands during the lactation cycle. Genetics and Molecular Research 2010, 9:1250-1257.
31. Horton J.D., Shah N.A., Warrington J.A., Anderson N.N., Park S.W., Brown M.S., et al. Combined analysis of oligonucleotide microarray data from transgenic and knockout mice identifies direct SREBP target genes. Proceedings of the National Academy of Sciences 2003, 100:12027-12032.
32. Jiang Y.J., Feingold K.R. The expression and regulation of enzymes mediating the biosynthesis of triglycerides and phospholipids in keratinocytes/epidermis. Dermato-Endocrinology 2011, 3:70-76.
33. Jones A.B. Peroxisome proliferator-activated receptor (PPAR) modulators: diabetes and beyond. Medicinal Research Reviews 2001, 21:540-552.
34. Jones D.H. The mitochondria of the mammary parenchymal cell in relation to pregnancy-lactation cycle. Lactation: A Comprehensive Treatise 1974, 503-512. Academic Press, New York. B.L.L.V.R. Smith (Ed.).
35. Jonker J.W., Merino G., Musters S., van Herwaarden A.E., Bolscher E., Wagenaar E., et al. The breast cancer resistance protein BCRP (ABCG2) concentrates drugs and carcinogenic xenotoxins into milk. Nature Medicine 2005, 11:127-129.
36. Kadegowda A.K.G., Bionaz M., Piperova L.S., Erdman R.A., Loor J.J. Lipogenic gene expression in MAC-T cells is affected differently by fatty acids and enhanced by PPAR-gamma activation. Journal of Dairy Science 2008, 91(Suppl. 1):678-688. ADSA-PSA-ASAS-AMPA Joint Annual Meeting: 2008.
37. Kasturi R., Joshi V.C. Hormonal regulation of stearoyl coenzyme A desaturase activity and lipogenesis during adipose conversion of 3T3-L1 cells. Journal of Biological Chemistry 1982, 257:12224-12230.
38. Keenan T.W., Mather I.H. Intracellular origin of milk fat globules and the nature of the milk fat globule membrane. Advanced Dairy Chemistry: Lipids 2006, 137-171. Springer, New York. P.F. Fox, P.L.H. McSweeney (Eds.).
39. Kersten S., Wahli W. Peroxisome proliferator activated receptor agonists. New Approaches to Drug Development 2000, 141-151. Birkhauser Verlag, Basel, Switzerland. P. Jolles (Ed.).
40. Khalil M.B., Blais A., Figeys D., Yao Z. Lipin - the bridge between hepatic glycerolipid biosynthesis and lipoprotein metabolism. Biochimica et Biophysica Acta 2010, 1801:1249-1259.
41. Kinsella J.E. Stearic acid metabolism by mammary cells. Journal of Dairy Science 1970, 53:1757-1765.
42. Kinsella J.E. Stearyl CoA as a precursor of oleic acid and glycerolipids in mammary microsomes from lactating bovine: possible regulatory step in milk triglyceride synthesis. Lipids 1972, 7:349-355.
43. Komisarek J., Dorynek Z. Effect of ABCG2, PPARGC1A, OLR1 and SCD1 gene polymorphism on estimated breeding values for functional and production traits in Polish Holstein-Friesian bulls. Journal of Applied Genetics 2009, 50:125-132.
44. Kronfeld D.S., Raggi F., Ramberg C.F. Mammary blood flow and ketone body metabolism in normal, fasted, and ketotic cows. American Journal of Physiology 1968, 215:218-227.
45. Kumar S., Lakshmanan S., Shaw J.C. beta-Hydroxybutyrate and acetate metabolism of the perfused bovine udder. Journal of Biological Chemistry 1959, 234:754-757.
46. Lee C.H., Olson P., Evans R.M. Minireview: lipid metabolism, metabolic diseases, and peroxisome proliferator-activated receptors. Endocrinology 2003, 144:2201-2207.
47. Leone T.C., Weinheimer C.J., Kelly D.P. A critical role for the peroxisome proliferator-activated receptor alpha (PPARalpha) in the cellular fasting response: the PPARalpha-null mouse as a model of fatty acid oxidation disorders. Proceedings of the National Academy of Sciences of the United States of America 1999, 96:7473-7478.
48. Liang H., Ward W.F. PGC-1alpha: a key regulator of energy metabolism. Advances in Physiology Education 2006, 30:145-151.
49. Litman T., Brangi M., Hudson E., Fetsch P., Abati A., Ross D.D., et al. The multidrug-resistant phenotype associated with overexpression of the new ABC half-transporter, MXR (ABCG2). Journal of Cell Science 2000, 113(Pt 11):2011-2021.
50. Lopez-Casillas F., Ponce-Castaneda M.V., Kim K.H. In vivo regulation of the activity of the two promoters of the rat acetyl coenzyme-A carboxylase gene. Endocrinology 1991, 129:1049-1058.
51. Luong A., Hannah V.C., Brown M.S., Goldstein J.L. Molecular characterization of human acetyl-CoA synthetase, an enzyme regulated by sterol regulatory element-binding proteins. Journal of Biological Chemistry 2000, 275:26458-26466.
52. Mackall J.C., Lane M.D. Changes in mammary-gland acetyl-coenzyme A carboxylase associated with lactogenic differentiation. Biochemical Journal 1977, 162:635-642.
53. McCarthy R.D., Patton S. Cholesterol esters and the synthesis of milk fat. Biochimica et Biophysica Acta 1963, 70:102-103.
54. Mead J.R., Irvine S.A., Ramji D.P. Lipoprotein lipase: structure, function, regulation, and role in disease. Journal of Molecular Medicine 2002, 80:753-769.
55. Mellenberger R.W., Bauman D.E., Nelson D.R. Metabolic adaptations during lactogenesis. Fatty acid and lactose synthesis in cow mammary tissue. Biochemical Journal 1973, 136:741-748.
56. Miyazaki M., Nitambi J.M. Fatty acid desaturation and elongation in mammals. Biochemistry of Lipids, Lipoproteins and Membranes 2008, 191-211. Elsevier, Amsterdam. D.E. Vance, J.E. Vance (Eds.).
57. Olsen H.G., Nilsen H., Hayes B., Berg P.R., Svendsen M., Lien S., et al. Genetic support for a quantitative trait nucleotide in the ABCG2 gene affecting milk composition of dairy cattle. BMC Genetics 2007, 8:32.
58. Page M.A., Williamson D.H. Lactating mammary gland of the rat: a potential major site of ketone-body utilization. Biochemical Journal 1972, 128:459-460.
59. Palmquist D.L. Milk fat: origin of fatty acids and influence of nutritional factors thereon. Advanced Chemistry: Lipids 2006, 43-92. Springer, New York. P.F. Fox, P.L.H. McSweeney (Eds.).
60. Palmquist D.L., Davis C.L., Brown R.E., Sachan D.S. Availability and metabolism of various substrates in ruminants. V. Entry rate into the body and incorporation into milk fat of d(-)β-hydroxybutyrate. Journal of Dairy Science 1969, 52:633-638.
61. Peters J.M., Hennuyer N., Staels B., Fruchart J.C., Fievet C., Gonzalez F.J., et al. Alterations in lipoprotein metabolism in peroxisome proliferator-activated receptor alpha-deficient mice. Journal of Biological Chemistry 1997, 272:27307-27312.
62. Raphael B.C., Dimick P.S., Puppione D.L. Lipid characterization of bovine serum lipoproteins throughout gestation and lactation. Journal of Dairy Science 1973, 56:1025-1032.
63. Reue K., Zhang P. The lipin protein family: dual roles in lipid biosynthesis and gene expression. FEBS Letters 2008, 582:90-96.
64. Schmitz G., Langmann T. Transcriptional regulatory networks in lipid metabolism control ABCA1 expression. Biochimica et Biophysica Acta 2005, 1735:1-19.
65. Shaw J.C., Knodt C.B. The utilization of β-hydroxybutyric acid by the lactating mammary gland. Journal of Biological Chemistry 1941, 138:287-292.
66. Sher T., Yi H.F., McBride O.W., Gonzalez F.J. cDNA cloning, chromosomal mapping, and functional characterization of the human peroxisome proliferator activated receptor. Biochemistry 1993, 32:5598-5604.
67. Strittmatter P., Spatz L., Corcoran D., Rogers M.J., Setlow B., Redline R. Purification and properties of rat liver microsomal stearyl coenzyme A desaturase. Proceedings of the National Academy of Sciences of the United States of America 1974, 71:4565-4569.
68. Sundqvist A., Bengoechea-Alonso M.T., Ye X., Lukiyanchuk V., Jin J., Harper J.W., et al. Control of lipid metabolism by phosphorylation-dependent degradation of the SREBP family of transcription factors by SCF(Fbw7). Cell Metabolism 2005, 1:379-391.
69. Takeuchi K., Reue K. Biochemistry, physiology, and genetics of GPAT, AGPAT, and lipin enzymes in triglyceride synthesis. American Journal of Physiology. Endocrinology and Metabolism 2009, 296:E1195-E1209.
70. Tantia M.S., Vijh R.K., Mishra B.P., Mishra B., Kumar S.T., Sodhi M. DGAT1 and ABCG2 polymorphism in Indian cattle (Bos indicus) and buffalo (Bubalus bubalis) breeds. BMC Veterinary Research 2006, 2:32.
71. Tocher D.R., Leaver M.J., Hodgson P.A. Recent advances in the biochemistry and molecular biology of fatty acyl desaturases. Progress in Lipid Research 1998, 37:73-117.
72. Uchide T., Onda K., Bonkobara M., Thongsong B., Matsuki N., Inaba M., et al. Utilization of intestinal triglyceride-rich lipoproteins in mammary gland of cows. Journal of Veterinary Medical Science 1999, 61:1143-1146.
73. van Herwaarden A.E., Wagenaar E., Merino G., Jonker J.W., Rosing H., Beijnen J.H., et al. Multidrug transporter ABCG2/breast cancer resistance protein secretes riboflavin (vitamin B2) into milk. Molecular and Cellular Biology 2007, 27:1247-1253.
74. Wei Y., Ma Y., Zhao Q., Ren Z., Li Y., Hou T., et al. New use for an old drug: inhibiting ABCG2 with sorafenib. Molecular Cancer Therapeutics 2012, 11:1693-1702.
75. Willson T.M., Brown P.J., Sternbach D.D., Henke B.R. The PPARs: from orphan receptors to drug discovery. Journal of Medicinal Chemistry 2000, 43:527-550.
76. Yadav P., Singh D.D., Mukesh M., Kataria R.S., Yadav A., Mohanty A.K., et al. Identification of suitable housekeeping genes for expression analysis in mammary epithelial cells of buffalo (Bubalus bubalis) during lactation cycle. Livestock Science 2012, 142:72-76.
77. Yadav P., Singh D.D., Mukesh M., Kataria R.S., Yadav A., Mohanty A.K., et al. Expression profiling of glucose transporter 1 (GLUT1) and apoptotic genes (BAX and BCL2) in milk enriched mammary epithelial cells (MEC) in riverine buffalo during lactation. Animal Biotechnology 2014, 25:151-159.