Proteome analysis of functionally differentiated bovine (Bos indicus) mammary epithelial cells isolated from milk

Proteomics

Volumn 13, Issue 21, 2013, Pages 3189-3204

  Janjanam, Jagadeesh ^a,f   Jamwal, Manu ^a   Singh, Surender ^a   Kumar, Saravanan ^b   Panigrahi, Aswini K ^c   Hariprasad, Gururao ^d   Jena, Manoj K ^a   Anand, Vijay ^a   Kumar, Sudarshan ^a   Kaushik, Jai K ^a   Dang, Ajay K ^a   Mukesh, Manishi ^e   Mishra, Bishnu P ^e   Srinivasan, Alagiri ^d   Reddy, Vanga S ^b   Mohanty, Ashok K ^a  

^a NATIONAL DAIRY RESEARCH INSTITUTE   (India)

^b INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY ICGEB   (India)

^c KING ABDULLAH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Saudi Arabia)

^d ALL INDIA INSTITUTE OF MEDICAL SCIENCES   (India)

^e NATIONAL BUREAU OF ANIMAL GENETIC RESOURCES   (India)

^f MICHIGAN TECHNOLOGICAL UNIVERSITY   (United States)

Author keywords

Animal proteomics; Bovine; Lactation; MEC; Milk

Indexed keywords

PROTEIN; PROTEOME;

ANIMAL CELL; ARTICLE; BIOINFORMATICS; BOS INDICUS; BREAST EPITHELIUM; BREAST MILK; CONTROLLED STUDY; IMMUNOMAGNETIC SEPARATION; LACTATION; LIQUID CHROMATOGRAPHY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEOMICS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TANDEM MASS SPECTROMETRY; TWO DIMENSIONAL ELECTROPHORESIS; WESTERN BLOTTING;

ANIMAL PROTEOMICS; BOVINE; LACTATION; MEC; MILK;

ANIMALS; CATTLE; EPITHELIAL CELLS; FEMALE; LACTATION; MAMMARY GLANDS, ANIMAL; METABOLIC NETWORKS AND PATHWAYS; MILK; PROTEIN INTERACTION MAPS; PROTEINS; PROTEOME;

EID: 84887104005     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201300031     Document Type: Article

References (81)

1. Singh, K., Erdman, R. A., Swanson, K. M., Molenaar, A. J. et al., Epigenetic regulation of milk production in dairy cows. J. Mammary Gland Biol. Neoplasia 2010, 15, 101-112.
2. Nandi, S., Endocrine control of mammary gland development and function in the C3H/He Crgl mouse. J. Natl. Cancer Inst. 1958, 21, 1039-1063.
3. Knight, C., Wilde, C., Mammary growth during lactation: implications for increasing milk yield. J. Dairy Sci. 1987, 70, 1991-2000.
4. Elsik, C. G., Tellam, R. L., Worley, K. C., Gibbs, R. A. et al., The genome sequence of taurine cattle: a window to ruminant biology and evolution. Science 2009, 324, 522-528.
5. Lemay, D., Lynn, D., Martin, W., Neville, M. et al., The bovine lactation genome: insights into the evolution of mammalian milk. Genom. Biol. 2009, 10, R43.1.
6. Tellam, R. L., Lemay, D. G., Van Tassell, C. P., Lewin, H. A. et al., Unlocking the bovine genome. BMC Genomics 2009, 10, 193-193.
7. Finucane, K. A., McFadden, T. B., Bond, J. P., Kennelly, J. J., Zhao, F.-Q., Onset of lactation in the bovine mammary gland: gene expression profiling indicates a strong inhibition of gene expression in cell proliferation. Funct. Integr. Genomics 2008, 8, 251-264.
8. Suchyta, S. P., Sipkovsky, S., Halgren, R. G., Kruska, R. et al., Bovine mammary gene expression profiling using a cDNA microarray enhanced for mammary-specific transcripts. Physiol. Genomics 2003, 16, 8-18.
9. Singh, K., Davis, S. R., Dobson, J. M., Molenaar, A. J. et al., cDNA microarray analysis reveals that antioxidant and immune genes are upregulated during involution of the bovine mammary gland. J. Dairy Sci. 2008, 91, 2236-2246.
10. Connor, E. E., Siferd, S., Elsasser, T. H., Evock-Clover, C. M. et al., Effects of increased milking frequency on gene expression in the bovine mammary gland. BMC Genomics 2008, 9, 362-362.
11. Bendixen, E., Danielsen, M., Hollung, K., Gianazza, E., Miller, I., Farm animal proteomics-A review. J. Proteomics 2011, 74, 282-293.
12. Jacobs, J. M., Mottaz, H. M., Yu, L.-R., Anderson, D. J. et al., Multidimensional proteome analysis of human mammary epithelial cells. J. Proteome Res. 2004, 3, 68-75.
13. Davies, C. R., Morris, J. S., Griffiths, M. R., Page, M. J. et al., Proteomic analysis of the mouse mammary gland is a powerful tool to identify novel proteins that are differentially expressed during mammary development. Proteomics 2006, 6, 5694-5704.
14. Wu, C. C., Howell, K. E., Neville, M. C., Yates, J. R., McManaman, J. L., Proteomics reveal a link between the endoplasmic reticulum and lipid secretory mechanisms in mammary epithelial cells. Electrophoresis 2000, 21, 3470-3482.
15. Boutinaud, M., Rulquin, H., Keisler, D. H., Djiane, J., Jammes, H., Use of somatic cells from goat milk for dynamic studies of gene expression in the mammary gland. J. Anim. Sci. 2002, 80, 1258-1269.
16. Boutinaud, M., Ben Chedly, M. H., Delamaire, E., Guinard-Flament, J., Milking and feed restriction regulate transcripts of mammary epithelial cells purified from milk. J. Dairy Sci. 2008, 91, 988-998.
17. Alcorn, J., Lu, X., Moscow, J. A., McNamara, P. J., Transporter gene expression in lactating and nonlactating human mammary epithelial cells using real-time reverse transcription-polymerase chain reaction. J. Pharmacol. Exp. Ther. 2002, 303, 487-496.
18. Hayashi, A. A., Nones, K., Roy, N. C., McNabb, W. C. et al., Initiation and elongation steps of mRNA translation are involved in the increase in milk protein yield caused by growth hormone administration during lactation. J. Dairy Sci. 2009, 92, 1889-1899.
19. Murrieta, C. M., Hess, B. W., Scholljegerdes, E. J., Engle, T. E. et al., Evaluation of milk somatic cells as a source of mRNA for study of lipogenesis in the mammary gland of lactating beef cows supplemented with dietary high-linoleate safflower seeds. J. Anim. Sci. 2006, 84, 2399-2405.
20. Bini, L., Magi, B., Marzocchi, B., Arcuri, F. et al., Protein expression profiles in human breast ductal carcinoma and histologically normal tissue. Electrophoresis 1997, 18, 2832-2841.
21. Vercoutter-Edouart, A. S., Lemoine, J., Le Bourhis, X., Louis, H. et al., Proteomic analysis reveals that 14-3-3sigma is down-regulated in human breast cancer cells. Cancer Res. 2001, 61, 76-80.
22. Desrivieres, S., Kuhn, K., Muller, J., Glaser, M. et al., Comparison of the nuclear proteomes of mammary epithelial cells at different stages of functional differentiation. Proteomics 2007, 7, 2019-2037.
23. Desrivières, S., Prinz, T., Laria, N. C. P., Meyer, M. et al., Comparative proteomic analysis of proliferating and functionally differentiated mammary epithelial cells. Mol. Cell Proteomics 2003, 2, 1039-1054.
24. Beddek, A. J., Rawson, P., Peng, L., Snell, R. et al., Profiling the metabolic proteome of bovine mammary tissue. Proteomics 2008, 8, 1502-1515.
25. Dang, A., Kapila, S., Tomar, P., Singh, C., Immunity of the buffalo mammary gland during different physiological stages. Asian Austral. J. Anim. 2007, 20, 1174-1181.
26. De, K., Mukherjee, J., Prasad, S., Dang, A., Effect of different physiological stages and managemental practices on milk somatic cell counts of Murrah buffaloes. Buffalo Bull. 2011, 30, 72-99.
27. German, T., Barash, I., Characterization of an epithelial cell line from bovine mammary gland. In Vitro Cell Dev-An. 2002, 38, 282-292.
28. Jones, J. C., Green, K. J., Intermediate filament plasma membrane interactions. Curr. Opin. Cell Biol. 1991, 3, 127-132.
29. Georgatos, S. D., Maison, C., Integration of intermediate filaments into cellular organelles. Int. Rev. Cytol. 1996, 164, 91-138.
30. Mikaelian, I., Hovick, M., Silva, K. A., Burzenski, L. M. et al., Expression of terminal differentiation proteins defines stages of mouse mammary gland development. Vet. Pathol. 2006, 43, 36-49.
31. Maningat, P. D., Sen, P., Rijnkels, M., Sunehag, A. L. et al., Gene expression in the human mammary epithelium during lactation: the milk fat globule transcriptome. Physiol. Genomics 2009, 37, 12-22.
32. Wang, Z., Luo, J., Wang, W., Zhao, W., Lin, X., Characterization and culture of isolated primary dairy goat mammary gland epithelial cells. Sheng Wu Gong Cheng Xue Bao 2010, 26, 1123-1127.
33. Deugnier, M. A., Moiseyeva, E. P., Thiery, J. P., Glukhova, M., Myoepithelial cell differentiation in the developing mammary gland: progressive acquisition of smooth muscle phenotype. Dev. Dyn. 1995, 204, 107-117.
34. Li, N., Goodall, A. H., Hjemdahl, P., Efficient flow cytometric assay for platelet-leukocyte aggregates in whole blood using fluorescence signal triggering. Cytometry 1999, 35, 154-161.
35. Hussain, T., Kotnis, A., Sarin, R., Mulherkar, R., Establishment & characterization of lymphoblastoid cell lines from patients with multiple primary neoplasms in the upper aero-digestive tract & healthy individuals. Indian J. Med. Res. 2012, 135, 820-829.
36. Murray, S. M., Picker, L. J., Axthelm, M. K., Linial, M. L., Expanded tissue targets for foamy virus replication with simian immunodeficiency virus-induced immunosuppression. J. Virol. 2006, 80, 663-670.
37. Lau, S. K., Chu, P. G., Weiss, L. M., CD163 A specific marker of macrophages in paraffin-embedded tissue samples. Am. J. Clin. Pathol. 2004, 122, 794-801.
38. Lawson, N. D., Berliner, N., Representational difference analysis of a committed myeloid progenitor cell line reveals evidence for bilineage potential. Proc. Natl. Acad. Sci. USA 1998, 95, 10129-10133.
39. Yadav, P., Deepak Singh, D., Mukesh, M., Kataria, R. et al., Identification of suitable housekeeping genes for expression analysis in mammary epithelial cells of buffalo (Bubalus bubalis) during lactation cycle. Livest Sci. 2012, 147, 72-76.
40. Rozen, S., Skaletsky, H., Primer3 on the WWW for general users and for biologist programmers. Methods Mol. Biol. 2000, 132, 365-386.
41. Viturro, E., Koenning, M., Kroemer, A., Schlamberger, G. et al., Cholesterol synthesis in the lactating cow: induced expression of candidate genes. J. Steroid Biochem. Mol. Biol. 2009, 115, 62-67.
42. Xie, X., Yi, Z., Bowen, B., Wolf, C. et al., Characterization of the human adipocyte proteome and reproducibility of protein abundance by one-dimensional gel electrophoresis and HPLC- ESI- MS/MS. J. Proteome Res. 2010, 9, 4521-4534.
43. Shevchenko, A., Tomas, H., Havlis, J., Olsen, J. V., Mann, M., In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat. Protoc. 2006, 1, 2856-2860.
44. Ranjan, R., Chugh, M., Kumar, S., Singh, S. et al., Proteome analysis reveals a large merozoite surface protein-1 associated complex on the Plasmodium falciparum merozoite surface. J. Proteome Res. 2011, 10, 680-691.
45. Agrawal, P., Kumar, S., Das, H. R., Mass spectrometric characterization of isoform variants of peanut (Arachis hypogaea) stem lectin (SL-I). J. Proteomics 2010, 73, 1573-1586.
46. Panigrahi, A. K., Ogata, Y., Zikova, A., Anupama, A. et al., A comprehensive analysis of Trypanosoma brucei mitochondrial proteome. Proteomics 2009, 9, 434-450.
47. Keller, A., Nesvizhskii, A. I., Kolker, E., Aebersold, R., Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal. Chem. 2002, 74, 5383-5392.
48. Nesvizhskii, A. I., Keller, A., Kolker, E., Aebersold, R., A statistical model for identifying proteins by tandem mass spectrometry. Anal. Chem. 2003, 75, 4646-4658.
49. Nikitin, A., Egorov, S., Daraselia, N., Mazo, I., Pathway studio-the analysis and navigation of molecular networks. Bioinformatics 2003, 19, 2155-2157.
50. Dimmer, E. C., Huntley, R. P., Alam-Faruque, Y., Sawford, T. et al., The UniProt-GO annotation database in 2011. Nucleic Acids Res. 2012, 40, D565-D570.
51. Boutinaud, M., Jammes, H., Potential uses of milk epithelial cells: a review. Reprod. Nutr. Dev. 2002, 42, 133-147.
52. Gomm, J. J., Browne, P. J., Coope, R. C., Liu, Q. Y. et al., Isolation of pure populations of epithelial and myoepithelial cells from the normal human mammary gland using immunomagnetic separation with Dynabeads. Anal. Biochem. 1995, 226, 91-99.
53. Varshney, N., Mohanty, A. K., Kumar, S., Kaushik, J. K. et al., Selection of suitable reference genes for quantitative gene expression studies in milk somatic cells of lactating cows (Bos indicus). J. Dairy Sci. 2012, 95, 2935-2945.
54. Bougarn, S., Cunha, P., Gilbert, F. B., Harmache, A. et al., Staphylococcal-associated molecular patterns enhance expression of immune defense genes induced by IL-17 in mammary epithelial cells. Cytokine 2011, 56, 749-759.
55. Bartek, J., Durban, E., Hallowes, R., Taylor-Papadimitriou, J., A subclass of luminal epithelial cells in the human mammary gland, defined by antibodies to cytokeratins. J. Cell Sci. 1985, 75, 17-33.
56. Swallow, D. M., Gendler, S., Griffiths, B., Kearney, A. et al., The hypervariable gene locus PUM, which codes for the tumour associated epithelial mucins, is located on chromosome 1, within the region 1q21-24. Ann. Hum. Genet. 1987, 51, 289-294.
57. Hahm, H. A., Ip, M. M., Darcy, K., Black, J. D. et al., Primary culture of normal rat mammary epithelial cells within a basement membrane matrix. II. Functional differentiation under serum-free conditions. In Vitro Cell Dev. Biol. 1990, 26, 803-814.
58. Levine, J. F., Stockdale, F. E., Cell-cell interactions promote mammary epithelial cell differentiation. J. Cell Biol. 1985, 100, 1415-1422.
59. Tomazella, G. G., da Silva, I., Laure, H. J., Rosa, J. C. et al., Proteomic analysis of total cellular proteins of human neutrophils. Proteome Sci. 2009, 7, 32-32.
60. Anand, V., Dogra, N., Singh, S., Kumar, S. N. et al., Establishment and characterization of a buffalo (Bubalus bubalis) mammary epithelial cell line. PLoS ONE 2012, 7, e40469.
61. Aoki, N., Regulation and functional relevance of milk fat globules and their components in the mammary gland. Biosci. Biotechnol. Biochem. 2006, 70, 2019-2027.
62. Huynh, H. T., Robitaille, G., Turner, J. D., Establishment of bovine mammary epithelial cells (MAC-T): an in vitro model for bovine lactation. Exp. Cell Res. 1991, 197, 191-199.
63. Addis, M. F., Pisanu, S., Ghisaura, S., Pagnozzi, D. et al., Proteomics and pathway analyses of the milk fat globule in sheep naturally infected by Mycoplasma agalactiae provide indications of the in vivo response of the mammary epithelium to bacterial infection. Infect. Immun. 2011, 79, 3833-3845.
64. Reinhardt, T. A., Lippolis, J. D., Bovine milk fat globule membrane proteome. J. Dairy Res. 2006, 73, 406-416.
65. Vanderghem, C., Blecker, C., Danthine, S., Deroanne, C. et al., Proteome analysis of the bovine milk fat globule: enhancement of membrane purification. Int. Dairy J. 2008, 18, 885-893.
66. Jessani, N., Humphrey, M., McDonald, W. H., Niessen, S. et al., Carcinoma and stromal enzyme activity profiles associated with breast tumor growth in vivo. Proc. Natl. Acad. Sci. USA 2004, 101, 13756-13761.
67. Scrutton, M. C., Utter, M. F., The regulation of glycolysis and gluconeogenesis in animal tissues. Annu. Rev. Biochem. 1968, 37, 249-302.
68. Betancourt, A. M., Mobley, J. A., Russo, J., Lamartiniere, C. A., Proteomic analysis in mammary glands of rat offspring exposed in utero to bisphenol A. J. Proteomics 2010, 73, 1241-1253.
69. Moreira, J. M. A., Cabezon, T., Gromova, I., Gromov, P. et al., Tissue proteomics of the human mammary gland: towards an abridged definition of the molecular phenotypes underlying epithelial normalcy. Mol. Oncol. 2010, 4, 539-561.
70. Lindahl, R., Aldehyde dehydrogenases and their role in carcinogenesis. Crit. Rev. Biochem. Mol. Biol. 1992, 27, 283-335.
71. Dräger, U. C., Wagner, E., McCaffery, P., Aldehyde dehydrogenases in the generation of retinoic acid in the developing vertebrate: a central role of the eye. J. Nutr. 1998, 128, 463S-466S.
72. Hofer, D., Jons, T., Kraemer, J., Drenckhahn, D., From cytoskeleton to polarity and chemoreception in the gut epithelium. Ann. NY Acad. Sci. 1998, 859, 75-84.
73. Chanat, E., Martin, P., Ollivier-Bousquet, M., Alpha(S1)-casein is required for the efficient transport of beta- and kappa-casein from the endoplasmic reticulum to the Golgi apparatus of mammary epithelial cells. J. Cell Sci. 1999, 112(Pt 19), 3399-3412.
74. Shekar, P. C., Goel, S., Rani, S. D. S., Sarathi, D. P. et al., Kappa-casein-deficient mice fail to lactate. Proc. Natl. Acad. Sci. USA 2006, 103, 8000-8005.
75. Grewal, T., Enrich, C., Annexins-modulators of EGF receptor signalling and trafficking. Cell. Signal. 2009, 21, 847-858.
76. Monastyrskaya, K., Babiychuk, E. B., Draeger, A., The annexins: spatial and temporal coordination of signaling events during cellular stress. Cell Mol. Life Sci. 2009, 66, 2623-2642.
77. Gerke, V., Moss, S. E., Annexins: from structure to function. Physiol. Rev. 2002, 82, 331-371.
78. Schlaepfer, D. D., Haigler, H. T., Expression of annexins as a function of cellular growth state. J. Cell Biol. 1990, 111, 229-238.
79. Burgoyne, R. D., Calpactin in exocytosis? Nature 1988, 331, 20-20.
80. Hong, K., Düzgüneş, N., Papahadjopoulos, D., Role of synexin in membrane fusion. Enhancement of calcium-dependent fusion of phospholipid vesicles. J. Biol. Chem. 1981, 256, 3641-3644.
81. Gill, J. J., Sabour, P. M., Gong, J., Yu, H. et al., Characterization of bacterial populations recovered from the teat canals of lactating dairy and beef cattle by 16S rRNA gene sequence analysis. FEMS Microbiol. Ecol. 2006, 56, 471-481.