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http://dx.doi.org/10.5713/ajas.2011.10110

Proteomic Functional Characterization of Bovine Stromal Vascular Cells from Omental, Subcutaneous and Intramuscular Adipose Depots  

Rajesh, Ramanna Valmiki (Division of Animal Genomics and Bioinformatics, National Institute of Animal Science, Rural Development Administration)
Kim, Seong-Kon (Division of Animal Genomics and Bioinformatics, National Institute of Animal Science, Rural Development Administration)
Park, Mi-Rim (Division of Animal Genomics and Bioinformatics, National Institute of Animal Science, Rural Development Administration)
Nam, Jin-Seon (Division of Animal Genomics and Bioinformatics, National Institute of Animal Science, Rural Development Administration)
Kim, Nam-Kuk (Division of Animal Genomics and Bioinformatics, National Institute of Animal Science, Rural Development Administration)
Kwon, Seulemina (Division of Animal Genomics and Bioinformatics, National Institute of Animal Science, Rural Development Administration)
Yoon, Du-Hak (Division of Animal Genomics and Bioinformatics, National Institute of Animal Science, Rural Development Administration)
Kim, Tae-Hun (Division of Animal Genomics and Bioinformatics, National Institute of Animal Science, Rural Development Administration)
Lee, Hyun-Jeong (Division of Animal Genomics and Bioinformatics, National Institute of Animal Science, Rural Development Administration)
Publication Information
Asian-Australasian Journal of Animal Sciences / v.24, no.1, 2011 , pp. 110-124 More about this Journal
Abstract
Anatomically separate fat depots differ in size, function, and contribution to pathological states such as the metabolic syndrome. We isolated pre-adipocytes from different adipose depots, omental, subcutaneous and intramuscular, of beef cattle, and cultured in vitro to determine the basis for the variations and attribute these variations to the inherent properties of adipocyte progenitors. The proliferating cells from all depots before the confluence were harvested and the proteome was analyzed by a functional proteomic approach, involving 2-DE and MALDI-TOF/TOF. More than 252 protein spots were identified, selected and analyzed by Image Master (ver 7.0) and MALDI-TOF/TOF. Further, our analysis showed that there were specific differences in proteome expression patterns among proliferating precursor cells from the three depots. Sixteen proteins were found to be differentially expressed and these were identified as proteins involved in cellular processes, heat shock/chaperones, redox proteins, cytoskeletal proteins and metabolic enzymes. The results also enabled us to understand the basic roles of these proteins in different inherent properties exhibited by adipose tissue depots.
Keywords
2-DE; Stromal Vascular Cells; Adipose Depot; Proteome;
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1 Kirkland, J. and P. M. Harris. 1980. Changes in adipose tissue of the rat due to early under nutrition followed by rehabilitation. 3. Changes in cell replication studies with tritiated thymidine. Br. J. Nutr. 43:33-43.   DOI   ScienceOn
2 Kirkland, J. L. and E. M. Dax. 1984. Adipose hormone responsiveness and aging in the rat. J. Am. Geriatr. Soc. 32:1219-228.
3 Kirkland, J. L., C. H. Hollenberg and W. S. Gillon. 1996. Effects of fat depot site on differentiation-dependent gene expression in rat preadipocytes. Int. J. Obes. 20:S102-S107.
4 Kirkland, J. L., C. H. Hollenberg, W. Gillon and S. Kindler. 1992. Effect of hypophysectomy on rat preadipocyte replication and differentiation. Endocrinology 131:2769-2773.   DOI   ScienceOn
5 Kirkland, J. L., P. Cummins, C. Steppan, D. E. Dobson and M. H. Cladaras. 1997. Decreasing preadipocyte differentiation capacity with aging is associated with blunted expression of the transcription factor, CCAAT enhancer binding protein ${\alpha}$. Obes. Res. 5 (Suppl 1):22S.
6 Kumar, M. S., P. Y. Reddy, P. A. Kumar, I. Surolia and G. B. Reddy. 2004. Effect of dicarbonyl-induced browning on ${\alpha}-crystallin$ chaperone like activity: physiological significance and caveats of in vitro aggregation assays. Biochem. J. 379:273-282.   DOI   ScienceOn
7 Kurucz, I., A. Morva, A. Vaag, K. Eriksson, X. Huang, L. Group and L. Koranyi. 2002. Decreased expression of heat shock protein 72 in skeletal muscle of patients with type 2 diabetes correlates with insulin resistance. Diabetes 51:1102-1109.   DOI   ScienceOn
8 Hartman, A. D. 1985. Adipocyte fatty acid mobilization in vivo: effects of age and anatomical location. Lipids 20:255-261.   DOI
9 Hauner, H. and G. Entenmann. 1991. Regional variation of adipose differentiation in cultured stromal-vascular cells from the abdominal and femoral adipose tissue of obese women. Int. J. Obes. 15:121-126.
10 Hausman, D. B., M. DiGirolamo, T. J. Bartness, G. J. Hausman and R. J. Martin. 2001. The biology of white adipocyte proliferation. Obes. Rev. 2:239-254.   DOI   ScienceOn
11 Hellmann, U., C. Wemstedt, J. Gonez and C. H. Heldin. 1995. Improvement of an "In-gel" digestion procedure for the micropreparation of internal protein fragments for amino acid sequencing. Anal. Biochem. 224:451-455.   DOI   ScienceOn
12 Hoehn, B., M. A. Yenari, R. M. Sapolsky and G. K. Steinberg. 2003. Glutathione peroxidase overexpression inhibits cytochrome c release and proapoptotic mediators to protect neurons from experimental stroke. Stroke. 34:2489-2449.   DOI   ScienceOn
13 Hube, F., U. Lietz, M. Igel, P. B. Jensen, H. Tornqvist, H. G. Joost and H. Hauner. 1996. Difference in leptin mRNA levels between omental and subcutaneous abdominal adipose tissue from obese humans. Horm. Metab. Res. 28:690-693.   DOI   ScienceOn
14 James, P., Z. DeLany, E. Floyd, S. Zvonic, A. Gravois, E. Reiners, X. Wu, G. Kilroy, M. Lefevre and J. M. Gimble. 2005. Proteomic analysis of primary cultures of human adipose-derived stem cells. Mol. Cell. Proteomics 4:731-740.   DOI   ScienceOn
15 Jin, D. Y., H. Z. Chae, S. G. Rhee and K. T. Jeang. 1997. Regulatory role for a novel human thioredoxin peroxidase in $NF-{\kappa}B$ activation. J. Biol. Chem. 272:30952-30961.   DOI   ScienceOn
16 Dubios, T., J. P. Mira, D. Feliers, E. Solito, F. Russo-Marie and J. P. Oudinet. 1998. Annexin V inhibits protein kinase C activity via a mechanism of phospholipid sequestration. Biochem. J. 330:1277-1282.
17 Fried, S. K., C. D. Russell, N. L. Grauso and R. E. Brolin. 1993. Lipoprotein lipase regulation by insulin and glucocorticoid in subcutaneous and omental adipose tissues of obese women and men. J. Clin. Invest. 92:2191-2198.   DOI   ScienceOn
18 Edens, N. K., S. K. Fried, J. G. Kral, J. Hirsch and R. L. Leibel. 1993. In vitro lipid synthesis in human adipose tissue from three abdominal sites. Am. J. Physiol. Endocrinol. Metab. 265: E374-E379.
19 Fasshauera, M., J. Kleinb, S. Neumanna, M. Eszlingera and R. Paschke. 2002. Hormonal regulation of adiponectin gene expression in 3T3-L1 adipocytes. Biochem. Biophys. Res. Commun. 290:1084-1089.   DOI   ScienceOn
20 Fleming, I., S. J. MacKenzie, R. G. Vernon, N. G. Anderson, M. D. Houslay and E. Kilgour. 1999. Protein kinase C isoform play differential roles in the regulation of adipocyte differentiation. Biochem. J. 333:719-727.
21 Gao, G. and G. Serrero. 1990. Phospholipase $A_2$ is a differentiation-dependent enzymatic activity for adipogenic cell line and adipocyte precursors in primary culture. J. Biol. Chem. 265:2431-2434.
22 Gregoire, F., G. Todoroff, N. Hauser and C. Remacle. 1990. The stromal vascular fraction of rat inguinal and epididymal adipose tissue and the adipoconversion of fat cell precursors in primary culture. Biol. Cell. 69:215-222.   DOI   ScienceOn
23 Hache, R. J., R. Tse, T. Reich, J. G. Savory and Y. A. Lefebure. 1999. Nucleocytoplasmic trafficking of steroid-free glucocorticoid receptor. J. Biol. Chem. 274:1432-1439.   DOI   ScienceOn
24 Cornelius, P., O. A. MacDougald and M. D. Lane. 1994. Regulation of adipocyte development. Annu. Rev. Nutr. 14:99-129.   DOI   ScienceOn
25 Choi, K. C., S. G. Roh, D. Hishikawa, H. Miyahara, M. Kuno, H. Tsuzuki, A. Tomimatsu, Y. H. Hong, K. K. Cho, K. H. Han and S. Sasaki. 2003. Differential expression of the nonmuscle-type cofilin gene between subcutaneous and visceral adipose tissue. Biosci. Biotechnol. Biochem. 67:2262-2265.   DOI   ScienceOn
26 Chouchane, L., J. Danguir, C. Beji, K. Bouassida, L. Camoin, H. Sfar, S. Gabbouj and A. D. Strosberg. 2001. Genetic variation in the stress protein hsp70-2 gene is highly associated with obesity. Int. J. Obes. Relat. Metab. Disord. 25:462-466.   DOI   ScienceOn
27 Cianzio, D., D. G. Topel, G. Whitehurst, D. C. Beitz and H. L. Slef. 1982. Adipose tissue growth in cattle representing two frame sizes: Distribution among depots. J. Anim. Sci. 55:305-312.
28 Cryer, A., S. E. Williams and J. Cryer. 1992. Dietary and other factors involved in the proliferation, determination and differentiation of adipocyte precursor cells. Proc. Nutr. Soc. 51:379-385.   DOI   ScienceOn
29 Cryer, J., B. G. Woodhead and A. Cryer. 1987. The isolation and characterization of a putative adipocyte precursor cell type from the white adipose tissue of the chicken (Gallus domesticus). Comp. Biochem. Physiol. 86A:515-520.
30 Darlington, G. J., S. E. Ross and O. A. MacDougald. 1998. The role of C/EBP genes in adipocyte differentiation. J. Biol. Chem. 273:30057-30060.   DOI
31 Djian, P., D. A. K. Roncari and C. H. Hollenberg. 1993. Influence of anatomic site and age on the replication and differentiation of rat adipocyte precursors in culture. J. Clin. Invest. 72:1200-1208.
32 Ahmed, M. and P. Bergsten. 2005. Glucose-induced changes of multiple mouse islet proteins analysed by two-dimensional gel electrophoresis and mass spectrometry. Diabetologica 48:477-485.   DOI
33 Aboulaich, N., J. P. Vainonen, P. Stralfors and A. V. Vener. 2004. Vectorial proteomics reveal targeting, phosphorylation and specific fragmentation of PTRF (polymerase I and transcript release factor) at the surface of caveolae in human adipocytes. Biochem. J. 383:237-248.   DOI   ScienceOn
34 Adachi, J., C. Kumar, Y. Zhang and M. Mann. 2007. In-depth analysis of the adipocyte proteome by mass spectrometry and bioinformatics. Mol. Cell Proteomics 6:1257-1273.   DOI   ScienceOn
35 Adams, M., M. J. Reginato, D. Shao, M. A. Lazar and V. Krishna Chatterjee. 1997. Transcriptional activation by peroxisome proliferator-activated receptor is inhibited by phosphorylation at a consensus mitogen-activated protein kinase site. J. Biol. Chem. 272:5128-5132.   DOI   ScienceOn
36 Arner, P. 1997. Regional adiposity in man. J. Endocrinol. 155:191-192.   DOI   ScienceOn
37 Barcelo-Batllori, S. and R. Gomis. 2009. Proteomics in obesity. Proteomics Clin. Appl. 3:263-278.   DOI
38 Caserta, F., T. Tchkonia, V. Civelekm, M. Prentki, N. F. Brown, J. D. McGarry, R. A. Forse, B. E. Corkey, J. A. Hamilton and J. L. Kirkland. 2001. Fat depot origin affects fatty acid handling in cultured rat and human preadipocytes. Am. J. Physiol. Endocrinol. Metab. 280:E238-E247.
39 Cherian, M. and E. C. Abraham. 1995. Diabetes affects ${\alpha}-crystallin$ chaperone function. Biochem. Biophys. Res. Commun. 212:184-189.   DOI   ScienceOn
40 Webb, P. R., Doyle and C. N. G. Anderson. 2003. Protein kinase $C-{\varepsilon}$ promotes adipogenic commitment and is essential for terminal differentiation of 3T3-F442A preadipocytes. Cell. Mol. Life. Sci. 60:1504-1512.   DOI
41 Weil, C., N. Sabin, J. Bugeon, G. Paboeuf and F. Lefevre. 2009. Differentially expressed proteins in rainbow trout adipocytes isolated from visceral and subcutaneous tissues. Comp. Biochem. Physiol. Part D Genomics Proteomics 4:235-241.   DOI   ScienceOn
42 Yeh, W. C., T. K. Li, B. E. Bierer and S. L. McKnight. 1995. Identification and characterization of an immunophilin expressed during the clonal expansion phase of adipocyte differentiation. Proc. Natl. Acad. Sci. USA 92:11081-11085.   DOI   ScienceOn
43 Shi, Y., K. Porter, N. Parameswaran and H. K. Bae. 2009. Role of GRP78/BiP degradation and ER stress in deoxynivalenolinduced interleukin-6 upregulation in the macrophage. Toxicol. Sci. 109:247-255.   DOI   ScienceOn
44 Young, J. C., V. R. Agashe, K. Siegers and F. U. Hartl. 2005. Pathways of chaperone-mediated protein folding in the cytosol. Nat. Rev. Mol. Cell. Biol. 5:781-791.
45 Ziouzenkova, O., G. Orasanu, M. Sharlach, T. E Akiyama, J. P. Berger, J. Viereck, J. A. Hamilton, G. Tang, G. G. Dolnikowski, S. Vogel, G. Duester and J. Plutzky. 2007. Retinaldehyde represses adipogenesis and diet-induced obesity. Nat. Med. 13:695-702.   DOI   ScienceOn
46 Zouari Bouassida, K., L. Chouchane, K. Jellouli, S. Cherif, S. Haddada, S. Gabboujb and J. Danguir. 2004. Polymorphism of stress protein HSP70-2 gene in Tunisians: susceptibility implications in type 2 diabetes and obesity. Diabetes Metab. 30:175-180.   DOI   ScienceOn
47 Smyth, M. J., R. L. Sparks and W. Wharton. 1993. Proadipocyte cell lines: models of cellular proliferation and differentiation. J. Cell. Sci. 106:1-9.
48 Takenouchi, T., N. Miyashita, K. Ozutsumi, M. T. Rose and H. Aso. 2004. Role of caveolin-1 and cytoskeletal proteins, actin and vimentinm in adipogenesis of bovine intramuscular preadipocytes cells. Cell Biol. Int. 28:615-623.   DOI   ScienceOn
49 Van Harmelen, V., K. Rohrig and H. Hauner. 2004. Comparison of proliferation and differentiation capacity of human adipocyte precursor cells from omental and subcutaneous adipose tissue depot of obese subjects. Metab. Clin. Exp. 53:632-637.   DOI   ScienceOn
50 Tchkonia, T., N. Giorgadze, T. Pirtskhalava, Y. Tchoukalova, I. Karagiannides and R. A. Forse. 2002. Fat depot origin affects adipogenesis in primary cultured and cloned human preadipocytes. Am. J. Physiol. Regul. Integr. Comp. Physiol. 282:R1286-1296.
51 Villani, P., P. L. Altavista, L. Castaldi, G. Leter and E. Cordelli. 2000. Analysis of DNA oxidative damage related to cell proliferation. Mutat. Res. 464:229-237.   DOI   ScienceOn
52 Wadhwa, R., S. Takano, M. Robert, A. Yoshida, H. Nomura, R. R. Reddel, Y. Mitusui and S. C. Kaul. 1998. Inactivation of tumor suppressor p53 by mot-2, a hsp70 family member. J. Biol. Chem. 273:29586-29591.   DOI
53 Wang, P., F. G. Bouwman and E. C. Mariman. 2009. Generally detected proteins in comparative proteomics-a matter of cellular stress response? Proteomics 9:2955-2966.   DOI   ScienceOn
54 Rahman, A., S. G. Kumar, S. W. Kim, H. J. Hwang, M. B. Yu, S. K. Lee, H. S. Hwang, Y. H. Shon, K. S. Nam and J. W. Yun. 2008. Proteomic analysis for inhibitory effect of chitosan oligosaccharides on 3T3-L1 adipocyte differentiation. Proteomics 8:569-581.   DOI   ScienceOn
55 Ramsay, T. G., S. V. Rao and C. K. Wolverton. 1993. In vitro systems for the analysis of the development of adipose tissue in domestic animals. J. Nutr. 122:806-817.
56 Rane, M. J., Y. Pan, S. Singh, D. W. Powell, R. Wu, T. Cummins, Q. Chen, K. R. McLeish and J. B. Klein. 2003. Heat shock protein 27 controls apoptosis by regulating Akt activation. J. Biol. Chem. 278:27828-27835.   DOI   ScienceOn
57 Sha, H., Y. He, H. Chen, C. Wang, A. Zenno, H. Shi, X. Yang, X. Zhang and L. Qi. 2009. The IRE1a-XBP1 pathway of the unfolded protein response is required for adipogenesis. Cell Metab. 9:556-564.   DOI   ScienceOn
58 Renes, J., F. Bouwman, J. P. Noben, C. Evelo, J. Robben and E. Mariman. 2005. Protein profiling of 3T3-L1 adipocyte differentiation and (tumor necrosis factor alpha-mediated) starvation. Cell. Mol. Life Sci. 62:492-503.   DOI
59 Samulin, J., S. Lien, E. Grindflek, I. Berget, B. Ruyter and H. Sundvold. 2008. Depot specific differences during adipogenesis of porcine stromal-vascular cells. Cell Biol. Int. 32:525-531.   DOI   ScienceOn
60 Sezen, D., A. Bongiovanni, S. Gelber, U. Perni, J. Hutson, D. Skupski and S. Witkin. 2009. Gelsolin down-regulates lipopolysaccharide-inducedintraamniotic tumor necrosis factor-α production in the midtrimester of pregnancy. Am. J. Obstet. Gynecol. 200:191-192.
61 Shan, Y., T. L. Yang, R. Mestril and P. H. Wang. 2003. Hsp10 and Hsp60 suppress ubiquitination of insulin-like growth factor-1 receptor and augment insulin-like growth factor-1 receptor signaling in cardiac muscle. J. Biol. Chem. 278:45492-45498.   DOI   ScienceOn
62 Niesler, C. U., K. Siddle and B. Prins. 1998. Human preadipocytes displays a depot-specific susceptibility to apoptosis. Diabetes 47:1365-1368.   DOI   ScienceOn
63 Niesler, C. U., K. Siddle and J. B. Prins. 1998. Human preadipocytes display a depot-specific susceptibility to apoptosis. Diabetes 47:1365-1368.   DOI   ScienceOn
64 Novakofski, J. and C. Y. Hu. 1987. Culture of isolated adipose tissue cells. J. Anim. Sci. 65:12-24.
65 Petrak, J., R. Ivanek, O. Toman, R. Cmejla, J. Cmejlova, D. Vyoral, J. Zivny, C. D. Vulpe, Deja vu in proteomics. 2008. A hit parade of repeatedly identified differentially expressed proteins. Proteomics 8:1744-1749.   DOI   ScienceOn
66 Ozcan, U., Q. Cao, E. Yilmaz, A. H. Lee, N.N. Iwakoshi, E. Ozdelen, G. Tuncman, C. Gorgun, L. H. Glimcher and G. S. Hotamisligil. 2004. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 306:457-461.   DOI   ScienceOn
67 Pan, L., P. C. L. Beverley and P. G. Isaacson. 1991. Lactate dehydrogenase (LDH) isoenzymes and proliferative activity of lymphoid cells - an immunocytochemical study. Clin. Exp. Immunol. 86:240-245.
68 Perez-Perez, R., F. J. Ortega-Delgado, E. Garcia-Santos, J. A. Lopez, E. Camafeita, W. Ricart, J. M. Fernandez-Real and B. Peral. 2009. Differential proteomics of omental and subcutaneous adipose tissue reflects their unalike biochemical and metabolic properties. J. Proteome Res. 8:1682-1693.   DOI   ScienceOn
69 Prins, J. B. and S. O'Rahilly. 1997. Regulation of adipose cell number in man. Clin. Sci. 92:3-11.
70 Prosperi, M. T., D. Ferbus, D. Rouillard and G. Goubin. 1998. The pag gene product, a physiological inhibitor of c-abl tyrosine kinase, is overexpressed in cells entering S phase and by contact with agents including oxidative stress. FEBS Lett. 423:39-44.   DOI   ScienceOn
71 Lacasa, D., E. Garcia, B. Agli and Y. Giudicelli. 1997. Control of rat preadipocytes adipose conversion by ovarian status: regional specificity and possible involvement of the mitogenactivated protein kinase-dependent and c-fos signaling pathways. Endocrinology 138:2729-2734.   DOI   ScienceOn
72 Luegmayr, E., F. Varga, T. Frank, P. Roschger and K. Klaushofer. 1996. Effects of triiodothyronine on morphology, growth behavior, and the actin cytoskeleton in mouse osteoblastic cells (MC3T3-E1). Bone 18:591-599.   DOI   ScienceOn
73 Landry, F., C. R. Lombardo and J. W. Smith. 2000. A method for application of samples to Matrix-Assisted Laser Desorption Ionization Time-of-Flight targets that enhances peptide detection. Anal. Biochem. 279:1-8.   DOI   ScienceOn
74 Litthauer, D. and G. Serrero. 1992. The primary culture of mouse adipocyte precursor cells in defined medium. Comp. Biochem. Physiol. A Comp. Physiol. 101:59-64.   DOI   ScienceOn
75 Loffler, G. and H. Hauner. 1987. Adipose tissue development: the role of precursor cells and adipogenic factors. Part II. The regulation of the adipogenic conversion by hormones and serum factors. Klin. Wochenschr. 65:812-817.   DOI
76 Mayr, M., R. Siow, Y. L. Chung, U. Mayr, J. R. Griffiths and Q. Xu. 2004. Proteomic and metabolomic analysis of vascular smooth muscle cells. Circ. Res. 94:e87-e96.   DOI   ScienceOn
77 McBeath, R., D. M. Pirone, C. M. Nelson, K. Bhadriraju and C. S. Chen. 2004. Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev. Cell 6:483-495.   DOI   ScienceOn
78 Mira, J. P., T. Dubois, J. P. Oudinet, S. Lukowski, F. Russo-Marie and B. Geny. 1997. Inhibition of cytosolic phospholipase $A_2$ by Annexin V in differentiated permeabilized HL-60 cells. J. Biol. Chem. 272:10474-10482.   DOI   ScienceOn
79 Kaul, S. C., R. R. Reddel, Y. Mitsui and R. Wadhwa. 2001. An N-terminal region of mot-2 binds to p53 in vitro. Neoplasia 3:110-114.   DOI