Comparative 2D-DIGE proteomic analysis of bovine mammary epithelial cells during lactation reveals protein signatures for lactation persistency and milk yield

PLoS ONE

Volumn 9, Issue 8, 2014, Pages

  Janjanam, Jagadeesh ^a,d   Singh, Surender ^a   Jena, Manoj K ^a   Varshney, Nishant ^a   Kola, Srujana ^b   Kumar, Sudarshan ^a   Kaushik, Jai K ^a   Grover, Sunita ^a   Dang, Ajay K ^a   Mukesh, Manishi ^c   Prakash, B S ^a   Mohanty, Ashok K ^a  

^a NATIONAL DAIRY RESEARCH INSTITUTE   (India)

^b ALL INDIA INSTITUTE OF MEDICAL SCIENCES   (India)

^c NATIONAL BUREAU OF ANIMAL GENETIC RESOURCES   (India)

^d UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA LACTALBUMIN; BETA ACTIN; BETA CASEIN; CD19 ANTIGEN; CD4 ANTIGEN; CD45 ANTIGEN; CYTOKERATIN 8; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INSULIN; INTERLEUKIN 8; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SMOOTH MUSCLE ACTIN; MILK PROTEIN;

ANIMAL CELL; ARTICLE; BIOINFORMATICS; BREAST EPITHELIUM; CATTLE; CONTROLLED STUDY; ELECTROSPRAY MASS SPECTROMETRY; FEMALE; LACTATION; MASS SPECTROMETRY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; METABOLISM; MILK PRODUCTION; MILK YIELD; NONHUMAN; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEOMICS; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY; TWO DIMENSIONAL DIFFERENCE GEL ELECTROPHORESIS; UPREGULATION; ANIMAL; BOVINAE; CLUSTER ANALYSIS; COMPARATIVE STUDY; GENE EXPRESSION PROFILING; GENETICS; MILK; PRINCIPAL COMPONENT ANALYSIS; UDDER;

ANIMALS; CATTLE; CLUSTER ANALYSIS; FEMALE; GENE EXPRESSION PROFILING; LACTATION; MAMMARY GLANDS, ANIMAL; MILK; MILK PROTEINS; PRINCIPAL COMPONENT ANALYSIS; PROTEOMICS; TWO-DIMENSIONAL DIFFERENCE GEL ELECTROPHORESIS;

EID: 84905851903     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0102515     Document Type: Article

References (67)

1. McManaman JL, Neville MC (2003) Mammary physiology and milk secretion. Advanced Drug Delivery Reviews 55: 629-641. (Pubitemid 36428676)
2. Hadsell DL (2003) The insulin-like growth factor system in normal mammary gland function. Breast Disease 17: 3-14.
3. Grossman M, Koops W (2003) Modeling extended lactation curves of dairy cattle: A biological basis for the multiphasic approach. Journal of Dairy Science 86: 988-998. (Pubitemid 39067122)
4. Vetharaniam I, Davis S, Soboleva T, Shorten P, Wake G (2003) Modeling the interaction of milking frequency and nutrition on mammary gland growth and lactation. Journal of Dairy Science 86: 1987-1996. (Pubitemid 39067060)
5. Knight C, Wilde C (1987) Mammary growth during lactation: implications for increasing milk yield. J Dairy Sci 70: 1991-2000.
6. Neville M, Peaker M (1981) Ionized calcium in milk and the integrity of the mammary epithelium in the goat. The Journal of Physiology 313: 561-570. (Pubitemid 11125593)
7. Stelwagen K, Davis S, Farr V, Prosser C, Sherlock R (1994) Mammary epithelial cell tight junction integrity and mammary blood flow during an extended milking interval in goats. Journal of Dairy Science 77: 426-432.
8. Stelwagen K, Farr VC, Davis SR, Prosser CG (1995) EGTA-induced disruption of epithelial cell tight junctions in the lactating caprine mammary gland. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology 269: R848-R855.
9. Hadsell DL, Torres D, George J, Capuco AV, Ellis SE, et al. (2006) Changes in secretory cell turnover, and mitochondrial oxidative damage in the mouse mammary gland during a single prolonged lactation cycle suggest the possibility of accelerated cellular aging. Experimental Gerontology 41: 271-281.
10. Neville MC, Allen JC, Archer PC, Casey CE, Seacat J, et al. (1991) Studies in human lactation: milk volume and nutrient composition during weaning and lactogenesis. The American Journal of Clinical Nutrition 54: 81-92. (Pubitemid 21898920)
11. Hadsell D, George J, Torres D (2007) The declining phase of lactation: Peripheral or central, programmed or pathological? Journal of Mammary Gland Biology and Neoplasia 12: 59-70. (Pubitemid 46394926)
12. Lewallen LP, Dick MJ, Flowers J, Powell W, Zickefoose KT, et al. (2006) Breastfeeding support and early cessation. Journal of Obstetric, Gynecologic, & Neonatal Nursing 35: 166-172.
13. Janjanam J, Jamwal M, Singh S, Kumar S, Panigrahi AK, et al. (2013) Proteome Analysis of Functionally Differentiated Bovine (Bos indicus) Mammary Epithelial Cells isolated from Milk. Proteomics 13: 3189-3204.
14. O'Donnell R, Holland J, Deeth H, Alewood P (2004) Milk proteomics. International Dairy Journal 14: 1013-1023. (Pubitemid 39239301)
15. Roncada P, Piras C, Soggiu A, Turk R, Urbani A, et al. (2012) Farm animal milk proteomics. Journal of proteomics 75: 4259-4274.
16. Gade D, Thiermann J, Markowsky D, Rabus R (2003) Evaluation of two-dimensional difference gel electrophoresis for protein profiling. Journal of Molecular Microbiology and Biotechnology 5: 240-251.
17. Tonge R, Shaw J, Middleton B, Rowlinson R, Rayner S, et al. (2001) Validation and development of fluorescence two-dimensional differential gel electrophoresis proteomics technology. Proteomics 1: 377-396. (Pubitemid 33585112)
18. Unlu M, Morgan ME, Minden JS (1997) Difference gel electrophoresis: A single gel method for detecting changes in protein extracts. Electrophoresis 18: 2071-2077. (Pubitemid 27501267)
19. Von Eggeling F, Gawriljuk A, Fiedler W, Ernst G, Claussen U, et al. (2001) Fluorescent dual colour 2D-protein gel electrophoresis for rapid detection of differences in protein pattern with standard image analysis software. International Journal of Molecular Medicine 8: 373-377.
20. 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. (Pubitemid 351456312)
21. Alcorn J, Lu X, Moscow JA, McNamara PJ (2002) Transporter gene expression in lactating and nonlactating human mammary epithelial cells using real-time reverse transcription-polymerase chain reaction. J Pharmacol Exp Ther 303: 487-496. (Pubitemid 35231217)
22. Bringans S, Eriksen S, Kendrick T, Gopalakrishnakone P, Livk A, et al. (2008) Proteomic analysis of the venom of Heterometrus longimanus (Asian black scorpion). Proteomics 8: 1081-1096. (Pubitemid 351441446)
23. Janjanam J, Singh S, Choudhary S, Pradeep MA, Kumar S, et al. (2012) Molecular cloning, sequence characterization and heterologous expression of buffalo (Bubalus bubalis) oviduct-specific glycoprotein in E. coli. Molecular Biology Reports 39: 10031-10043.
24. Friedman DB, Wang SE, Whitwell CW, Caprioli RM, Arteaga CL (2007) Multivariable Difference Gel Electrophoresis and Mass Spectrometry A Case Study on Transforming Growth Factor-β and ERBB2 Signaling. Molecular & Cellular Proteomics 6: 150-169. (Pubitemid 46152700)
25. Boguth G, Harder A, Scheibe B, Wildgruber R, Weiss W (2000) The current state of two-dimensional electrophoresis with immobilized pH gradients. Electrophoresis 21: 1037-1053. (Pubitemid 30230771)
26. Tucker H (1969) Factors affecting mammary gland cell numbers. Journal of Dairy Science 52: 720-729.
27. Lemay D, Lynn D, Martin W, Neville M, Casey T, et al. (2009) The bovine lactation genome: insights into the evolution of mammalian milk. Genome Biol 10: R43.
28. Lemay DG, Neville MC, Rudolph MC, Pollard KS, German JB (2007) Gene regulatory networks in lactation: identification of global principles using bioinformatics. BMC Systems Biology 1: 56.
29. Liang P, MacRae T (1997) Molecular chaperones and the cytoskeleton. Journal of Cell Science 110: 1431-1440. (Pubitemid 27326662)
30. Hofer D, Jons T, Kraemer J, Drenckhahn D (1998) From cytoskeleton to polarity and chemoreception in the gut epithelium. Ann N Y Acad Sci 859: 75-84. (Pubitemid 29021007)
31. Wodarz A (2002) Establishing cell polarity in development. Nat Cell Biol 4: E39-44.
32. Sun HQ, Yamamoto M, Mejillano M, Yin HL (1999) Gelsolin, a multifunctional actin regulatory protein. Journal of Biological Chemistry 274: 33179-33182. (Pubitemid 129511609)
33. Witke W, Sharpe AH, Hartwig JH, Azuma T, Stossel TP, et al. (1995) Hemostatic, inflammatory, and fibroblast responses are blunted in mice lacking gelsolin. Cell 81: 41-51.
34. Crowley MR, Head KL, Kwiatkowski DJ, Asch HL, Asch BB (2000) The mouse mammary gland requires the actin-binding protein gelsolin for proper ductal morphogenesis. Developmental Biology 225: 407-423.
35. Chen P, Murphy-Ullrich JE, Wells A (1996) A role for gelsolin in actuating epidermal growth factor receptor-mediated cell motility. The Journal of Cell Biology 134: 689-698. (Pubitemid 26269141)
36. Hennighausen L, Robinson GW (2001) Signaling pathways in mammary gland development. Developmental Cell 1: 467-475. (Pubitemid 33586099)
37. Hennighausen L, Robinson GW (2005) Information networks in the mammary gland. Nature Reviews Molecular Cell Biology 6: 715-725. (Pubitemid 41742795)
38. Hershko A, Ciechanover A (1998) The ubiquitin system. Annual Review of Biochemistry 67: 425-479. (Pubitemid 28411135)
39. Hershko A (1997) Roles of ubiquitin-mediated proteolysis in cell cycle control. Current Opinion in Cell Biology 9: 788-799.
40. King RW, Deshaies RJ, Peters J-M, Kirschner MW (1996) How proteolysis drives the cell cycle. Science 274: 1652-1659. (Pubitemid 26414887)
41. Pagano M (1997) Cell cycle regulation by the ubiquitin pathway. The FASEB Journal 11: 1067-1075.
42. Gerke V, Moss SE (2002) Annexins: from structure to function. Physiological Reviews 82: 331-371. (Pubitemid 34654456)
43. Schlaepfer DD, Haigler HT (1990) Expression of annexins as a function of cellular growth state. The Journal of Cell Biology 111: 229-238.
44. Burgoyne RD (1988) Calpactin in exocytosis? Nature 331: 20-20.
45. Hong K, Düzgüneş N, Papahadjopoulos D (1981) Role of synexin in membrane fusion. Enhancement of calcium-dependent fusion of phospholipid vesicles. Journal of Biological Chemistry 256: 3641-3644.
46. Reinhardt TA, Lippolis JD, Nonnecke BJ, Sacco RE (2012) Bovine milk exosome proteome. Journal of Proteomics 75: 1486-1492.
47. Frey BM, Reber BF, Vishwanath BS, Escher G, Frey FJ (1999) Annexin I modulates cell functions by controlling intracellular calcium release. The FASEB Journal 13: 2235-2245.
48. Huntington JA, Read RJ, Carrell RW (2000) Structure of a serpin - protease complex shows inhibition by deformation. Nature 407: 923-926.
49. Silverman GA, Bird PI, Carrell RW, Church FC, Coughlin PB, et al. (2001) The serpins are an expanding superfamily of structurally similar but functionally diverse proteins evolution, mechanism of inhibition, novel functions, and a revised nomenclature. Journal of Biological Chemistry 276: 33293-33296.
50. Turk R, Piras C, Kovačić M, Samardžija M, Ahmed H, et al. (2012) Proteomics of inflammatory and oxidative stress response in cows with subclinical and clinical mastitis. Journal of proteomics 75: 4412-4428.
51. Taylor MR, Couto JR, Scallan CD, Ceriani RL, Peterson JA (1997) Lactadherin (formerly BA46), a membrane-associated glycoprotein expressed in human milk and breast carcinomas, promotes Arg-Gly-Asp (RGD)-dependent cell adhesion. DNA and cell biology 16: 861-869. (Pubitemid 27332695)
52. Li N, Zhang Y, Naylor MJ, Schatzmann F, Maurer F, et al. (2005) β1 integrins regulate mammary gland proliferation and maintain the integrity of mammary alveoli. The EMBO journal 24: 1942-1953. (Pubitemid 40896166)
53. Donato R (2003) Intracellular and extracellular roles of S100 proteins. Microscopy research and technique 60: 540-551.
54. Rosfjord EC, Dickson RB (1999) Growth factors, apoptosis, and survival of mammary epithelial cells. Journal of mammary gland biology and neoplasia 4: 229-237.
55. Burgoyne R, Geisow M (1989) The annexin family of calcium-binding proteins: Review article. Cell calcium 10: 1-10. (Pubitemid 19050291)
56. Oliver CH, Watson CJ (2013) Making milk: A new link between STAT5 and Akt1. JAK-STAT 2: 0-1.
57. Anderson SM, Rudolph MC, McManaman JL, Neville MC (2007) Secretory activation in the mammary gland: it's not just about milk protein synthesis. Breast Cancer Res 9: 204-217.
58. Proud C (2007) Signalling to translation: how signal transduction pathways control the protein synthetic machinery. Biochem J 403: 217-234.
59. Bionaz M, Loor JJ (2011) Gene networks driving bovine mammary protein synthesis during the lactation cycle. Bioinformatics and biology insights 5: 83.
60. Clarkson RW, Watson CJ (1999) NF-kappaB and apoptosis in mammary epithelial cells. Journal of Mammary Gland Biology and Neoplasia 4: 165-175.
61. Brantley DM, Yull FE, Muraoka RS, Hicks DJ, Cook CM, et al. (2000) Dynamic expression and activity of NF-κB during post-natal mammary gland morphogenesis. Mechanisms of development 97: 149-155.
62. Connelly L, Barham W, Pigg R, Saint-Jean L, Sherrill T, et al. (2010) Activation of nuclear factor kappa B in mammary epithelium promotes milk loss during mammary development and infection. Journal of Cellular Physiology 222: 73-81.
63. Karin M, Ben-Neriah Y (2000) Phosphorylation meets ubiquitination: the control of NF-κB activity. Annual Review of Immunology 18: 621-663. (Pubitemid 30365393)
64. Johnson GL, Lapadat R (2002) Mitogen-activated protein kinase pathways mediated by ERK, JNK, and p38 protein kinases. Science 298: 1911-1912. (Pubitemid 35425238)
65. Pearson G, Robinson F, Gibson TB, Xu B-e, Karandikar M, et al. (2001) Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocrine Reviews 22: 153-183. (Pubitemid 32458157)
66. Lemay DG, Ballard OA, Hughes MA, Morrow AL, Horseman ND, et al. (2013) RNA sequencing of the human milk fat layer transcriptome reveals distinct gene expression profiles at three stages of lactation. PloS one 8: e67531.
67. Mi H, Muruganujan A, Thomas PD (2013) PANTHER in 2013: modeling the evolution of gene function, and other gene attributes, in the context of phylogenetic trees. Nucleic Acids Research 41: D377-D386.