LC-MS/MS analysis of visceral and subcutaneous adipose tissue proteomes in young goats with focus on innate immunity and inflammation related proteins

Journal of Proteomics

Volumn 108, Issue , 2014, Pages 295-305

  Restelli, Laura ^a   Codrea, Marius Cosmin ^b   Savoini, Giovanni ^a   Ceciliani, Fabrizio ^a   Bendixen, Emoke ^c  

^a UNIVERSITY OF MILAN   (Italy)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c AARHUS UNIVERSITY   (Denmark)

Author keywords

Adipokines; Goat; LC MS MS; Subcutaneous adipose tissue; Visceral adipose tissue

Indexed keywords

ADIPOCYTOKINE; PROTEOME;

ANIMAL WELFARE; ARTICLE; BODY FAT; CLUSTER ANALYSIS; FARM ANIMAL; GOAT; INFLAMMATION; INNATE IMMUNITY; INTRAABDOMINAL FAT; LIQUID CHROMATOGRAPHY; METABOLISM; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SUBCUTANEOUS FAT; TANDEM MASS SPECTROMETRY; ANIMAL; BIOSYNTHESIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; HUMAN; IMMUNOLOGY; MASS SPECTROMETRY; MOUSE; PHYSIOLOGY; PROCEDURES; PROTEIN DATABASE; RAT;

ANIMALS; CHROMATOGRAPHY, LIQUID; DATABASES, PROTEIN; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GOATS; HUMANS; IMMUNITY, INNATE; INFLAMMATION; INTRA-ABDOMINAL FAT; MASS SPECTROMETRY; MICE; PROTEOME; RATS; SUBCUTANEOUS FAT;

EID: 84902602457     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2014.05.027     Document Type: Article

References (73)

1. Zhang Y., Proenca R., Maffei M., Barone M., Leopold L., Friedman J.M. Positional cloning of the mouse obese gene and its human homologue. Nature Dec 1994, 372(6505):425-432.
2. Lehr S., Hartwig S., Sell H. Adipokines: a treasure trove for the discovery of biomarkers for metabolic disorders. Proteomics Clin Appl Jan 2012, 6(1-2):91-101.
3. Frühbeck G., Gómez-Ambrosi J., Muruzábal F.J., Burrell M.A. The adipocyte: a model for integration of endocrine and metabolic signaling in energy metabolism regulation. Am J Physiol Endocrinol Metab Jun 2001, 280(6):E827-E847.
4. Peinado J.R., Jimenez-Gomez Y., Pulido M.R., Ortega-Bellido M., Diaz-Lopez C., Padillo F.J., et al. The stromal-vascular fraction of adipose tissue contributes to major differences between subcutaneous and visceral fat depots. Proteomics Sep 2010, 10(18):3356-3366.
5. Kershaw E.E., Flier J.S. Adipose tissue as an endocrine organ. J Clin Endocrinol Metab Jun 2004, 89(6):2548-2556.
6. Votruba S.B., Jensen M.D. Regional fat deposition as a factor in FFA metabolism. Annu Rev Nutr Aug 2007, 27:149-163.
7. O'Rourke R.W., Metcalf M.D., White A.E., Madala A., Winters B.R., Maizlin I.I., et al. Depot-specific differences in inflammatory mediators and a role for NK cells and IFN-gamma in inflammation in human adipose tissue. Int J Obes (Lond) Sep 2009, 33(9):978-990.
8. Hocking S.L., Wu L.E., Guilhaus M., Chisholm D.J., James D.E. Intrinsic depot-specific differences in the secretome of adipose tissue, preadipocytes, and adipose tissue-derived microvascular endothelial cells. Diabetes Dec 2010, 59(12):3008-3016.
9. Roca-Rivada A., Alonso J., Al-Massadi O., Castelao C., Peinado J.R., Seoane L.M., et al. Secretome analysis of rat adipose tissues shows location-specific roles for each depot type. J Proteomics Jun 2011, 74(7):1068-1079.
10. Mukesh M., Bionaz M., Graugnard D.E., Drackley J.K., Loor J.J. Adipose tissue depots of Holstein cows are immune responsive: inflammatory gene expression in vitro. Domest Anim Endocrinol Apr 2010, 38(3):168-178.
11. Lemor A., Mielenz M., Altmann M., von Borell E., Sauerwein H. mRNA abundance of adiponectin and its receptors, leptin and visfatin and of G-protein coupled receptor 41 in five different fat depots from sheep. J Anim Physiol Anim Nutr (Berl) Oct 2010, 94(5):e96-e101.
12. Rajesh R.V., Heo G.N., Park M.R., Nam J.S., Kim N.K., Yoon D., et al. Proteomic analysis of bovine omental, subcutaneous and intramuscular preadipocytes during in vitro adipogenic differentiation. Comp Biochem Physiol Part D Genomics Proteomics Sep 2010, 5(3):234-244.
13. Taga H., Chilliard Y., Picard B., Zingaretti M.C., Bonnet M. Foetal bovine intermuscular adipose tissue exhibits histological and metabolic features of brown and white adipocytes during the last third of pregnancy. Animal Apr 2012, 6(4):641-649.
14. Zhang Q., Lee H.G., Han J.A., Kim E.B., Kang S.K., Yin J., et al. Differentially expressed proteins during fat accumulation in bovine skeletal muscle. Meat Sci Nov 2010, 86(3):814-820.
15. Danielsen M., Pedersen L.J., Bendixen E. An in vivo characterization of colostrum protein uptake in porcine gut during early lactation. J Proteomics Jan 2011, 74(1):101-109.
16. Elias J.E., Gygi S.P. Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat Methods Mar 2007, 4(3):207-214.
17. Chong P.K., Gan C.S., Pham T.K., Wright P.C. Isobaric tags for relative and absolute quantitation (iTRAQ) reproducibility: implication of multiple injections. J Proteome Res May 2006, 5(5):1232-1240.
18. Ward J.H. Hierarchical grouping to optimize an objective function. J Am Stat Assoc Mar 1963, 58(301):236-244.
19. Conesa A., Götz S., García-Gómez J.M., Terol J., Talón M., Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics Sep 2005, 21(18):3674-3676.
20. Thomas P.D., Campbell M.J., Kejariwal A., Mi H., Karlak B., Daverman R., et al. PANTHER: a library of protein families and subfamilies indexed by function. Genome Res Sep 2003, 13(9):2129-2141.
21. Dilda F., Pisani L.F., Rahman M.M., Modina S., Tessaro I., Sartorelli P., et al. Distribution of acute phase proteins in the bovine forestomachs and abomasum. Vet J Apr 2012, 192(1):101-105.
22. Sejersen H., Sørensen M.T., Larsen T., Bendixen E., Ingvartsen K.L. Liver protein expression in dairy cows with high liver triglycerides in early lactation. J Dairy Sci May 2012, 95(5):2409-2421.
23. Hornshøj H., Bendixen E., Conley L.N., Andersen P.K., Hedegaard J., Panitz F., et al. Transcriptomic and proteomic profiling of two porcine tissues using high-throughput technologies. BMC Genomics Jan 2009, 10:30.
24. Bueno A.A., Oyama L.M., de Oliveira C., Pisani L.P., Ribeiro E.B., Silveira V.L. Oller do Nascimento CM. Effects of different fatty acids and dietary lipids on adiponectin gene expression in 3T3-L1 cells and C57BL/6J mice adipose tissue. Pflugers Arch Jan 2008, 455(4):701-709.
25. Pérez-Pérez R., Ortega-Delgado F.J., García-Santos E., López J.A., Camafeita E., Ricart W., et al. Differential proteomics of omental and subcutaneous adipose tissue reflects their unalike biochemical and metabolic properties. J Proteome Res Apr 2009, 8(4):1682-1693.
26. Faulconnier Y., Chilliard Y., Torbati M.B., Leroux C. The transcriptomic profiles of adipose tissues are modified by feed deprivation in lactating goats. Comp Biochem Physiol Part D Genomics Proteomics Jun 2011, 6(2):139-149.
27. Griffin T.J., Gygi S.P., Ideker T., Rist B., Eng J., Hood L., et al. Complementary profiling of gene expression at the transcriptome and proteome levels in Saccharomyces cerevisiae. Mol Cell Proteomics Apr 2002, 1(4):323-333.
28. Takenouchi T., Miyashita N., Ozutsumi K., Rose M.T., Aso H. Role of caveolin-1 and cytoskeletal proteins, actin and vimentin, in adipogenesis of bovine intramuscular preadipocyte cells. Cell Biol Int 2004, 28(8-9):615-623.
29. Zhao Y.M., Basu U., Dodson M.V., Basarb J.A., Guan le L. Proteome differences associated with fat accumulation in bovine subcutaneous adipose tissues. Proteome Sci Mar 2010, 18:8-14.
30. Furukawa S., Fujita T., Shimabukuro M., Iwaki M., Yamada Y., Nakajima Y., et al. Increased oxidative stress in obesity and its impact on metabolic syndrome. J Clin Invest Dec 2004, 114(12):1752-1761.
31. Pessler-Cohen D., Pekala P.H., Kovsan J., Bloch-Damti A., Rudich A., Bashan N. GLUT4 repression in response to oxidative stress is associated with reciprocal alterations in C/EBP alpha and delta isoforms in 3T3-L1 adipocytes. Arch Physiol Biochem Feb 2006, 112(1):3-12.
32. Prabakaran S., Wengenroth M., Lockstone H.E., Lilley K., Leweke F.M., Bahn S. 2-D DIGE analysis of liver and red blood cells provides further evidence for oxidative stress in schizophrenia. J Proteome Res Jan 2007, 6(1):141-149.
33. Young J.C., Agashe V.R., Siegers K., Hartl F.U. Pathways of chaperone-mediated protein folding in the cytosol. Nat Rev Mol Cell Biol Oct 2004, 5(10):781-791.
34. DeLany J.P., Floyd Z.E., Zvonic S., Smith A., Gravois A., Reiners E., et al. Proteomic analysis of primary cultures of human adipose-derived stem cells: modulation by adipogenesis. Mol Cell Proteomics Jun 2005, 4(6):731-740.
35. Rhee S.G., Woo H.A., Kil I.S., Bae S.H. Peroxiredoxin functions as a peroxidase and a regulator and sensor of local peroxides. J Biol Chem Feb 2012, 287(7):4403-4410.
36. Edgar R.S., Green E.W., Zhao Y., van Ooijen G., Olmedo M., Qin X., et al. Peroxiredoxins are conserved markers of circadian rhythms. Nature May 2012, 485(7399):459-464.
37. Desruisseaux M.S., Nagajyothi, Trujillo M.E., Tanowitz H.B., Scherer P.E. Adipocyte, adipose tissue, and infectious disease. Infect Immun Mar 2007, 75(3):1066-1078.
38. Akter S.H., Häussler S., Germeroth D., von Soosten D., Dänicke S., Südekum K.H., et al. Immunohistochemical characterization of phagocytic immune cell infiltration into different adipose tissue depots of dairy cows during early lactation. J Dairy Sci Jun 2012, 95(6):3032-3044.
39. Faber D.R., de Groot P.G., Visseren F.L. Role of adipose tissue in haemostasis, coagulation and fibrinolysis. Obes Rev Sep 2009, 10(5):554-563.
40. Pérez-Pérez R., García-Santos E., Ortega-Delgado F.J., López J.A., Camafeita E., Ricart W., et al. Attenuated metabolism is a hallmark of obesity as revealed by comparative proteomic analysis of human omental adipose tissue. J Proteomics Jan 2012, 75(3):783-795.
41. Insenser M., Montes-Nieto R., Vilarrasa N., Lecube A., Simó R., Vendrell J., et al. A nontargeted proteomic approach to the study of visceral and subcutaneous adipose tissue in human obesity. Mol Cell Endocrinol Nov 2012, 363(1-2):10-19.
42. Abe K.C., da Silva Mori M.A., Pesquero J.B. Leptin deficiency leads to the regulation of kinin receptors expression in mice. Regul Pept Feb 2007, 138(2-3):56-58.
43. Schlesinger J.B., van Harmelen V., Alberti-Huber C.E., Hauner H. Albumin inhibits adipogenesis and stimulates cytokine release from human adipocytes. Am J Physiol Cell Physiol Jul 2006, 291(1):C27-C33.
44. Li A., Mo D., Zhao X., Jiang W., Cong P., He Z., et al. Comparison of the longissimus muscle proteome between obese and lean pigs at 180days. Mamm Genome Feb 2013, 24(1-2):72-79.
45. Lehr S., Hartwig S., Lamers D., Famulla S., Müller S., Hanisch F.G., et al. Identification and validation of novel adipokines released from primary human adipocytes. Mol Cell Proteomics Jan 2012, 11(1). [M111.010504].
46. Dahlman I., Elsen M., Tennagels N., Korn M., Brockmann B., Sell H., et al. Functional annotation of the human fat cell secretome. Arch Physiol Biochem Jul 2012, 118(3):84-91.
47. Schattner M., Rabinovich G.A. Galectins: new agonists of platelet activation. Biol Chem Jul 2013, 394(7):857-863.
48. Camby I., Le Mercier M., Lefranc F., Kiss R. Galectin-1: a small protein with major functions. Glycobiology Nov 2006, 16(11):137R-157R.
49. Kiwaki K., Novak C.M., Hsu D.K., Liu F.T., Levine J.A. Galectin-3 stimulates preadipocyte proliferation and is up-regulated in growing adipose tissue. Obesity (Silver Spring) Jan 2007, 15(1):32-39.
50. Ahmed M., Neville M.J., Edelmann M.J., Kessler B.M., Karpe F. Proteomic analysis of human adipose tissue after rosiglitazone treatment shows coordinated changes to promote glucose uptake. Obesity (Silver Spring) Jan 2010, 18(1):27-34.
51. Ceciliani F., Ceron J.J., Eckersall P.D., Sauerwein H. Acute phase proteins in ruminants. J Proteomics Jul 2012, 75(14):4207-4231.
52. Saremi B., Al-Dawood A., Winand S., Müller U., Pappritz J., von Soosten D., et al. Bovine haptoglobin as an adipokine: serum concentrations and tissue expression in dairy cows receiving a conjugated linoleic acids supplement throughout lactation. Vet Immunol Immunopathol May 2012, 146(3-4):201-211.
53. Berg L.C., Thomsen P.D., Andersen P.H., Jensen H.E., Jacobsen S. Serum amyloid A is expressed in histologically normal tissues from horses and cattle. Vet Immunol Immunopathol Nov 2011, 144(1-2):155-159.
54. Rødgaard T., Stagsted J., Christoffersen B.Ø., Cirera S., Moesgaard S.G., Sturek M., et al. Orosomucoid expression profiles in liver, adipose tissues and serum of lean and obese domestic pigs, Göttingen minipigs and Ossabaw minipigs. Vet Immunol Immunopathol Feb 2013, 151(3-4):325-330.
55. Hermsdorff H.H., Volp A.C., Puchau B., Barbosa K.B., Zulet M.A., Bressan J., et al. Contribution of gender and body fat distribution to inflammatory marker concentrations in apparently healthy young adults. Inflamm Res May 2012, 61(5):427-435.
56. Pini M., Rhodes D.H., Fantuzzi G. Hematological and acute-phase responses to diet-induced obesity in IL-6 KO mice. Cytokine Dec 2011, 56(3):708-716.
57. Chen K., Chen S., Huang C., Cheng H., Zhou R. TCTP increases stability of hypoxia-inducible factor 1α by interaction with and degradation of the tumour suppressor VHL. Biol Cell May 2013, 105(5):208-218.
58. Jin Y.C., Li Z.H., Hong Z.S., Xu C.X., Han J.A., Choi S.H., et al. Conjugated linoleic acid synthesis-related protein proteasome subunit α 5 (PSMA5) is increased by vaccenic acid treatment in goat mammary tissue. J Dairy Sci Aug 2012, 95(8):4286-4297.
59. Im J.Y., Lee K.W., Junn E., Mouradian M.M. DJ-1 protects against oxidative damage by regulating the thioredoxin/ASK1 complex. Neurosci Res Jul 2010, 67(3):203-208.
60. Diandong H., Kefeng S., Weixin F., Zaifu L. Proteomic analysis of NK92-MI cells activated by neuropeptide substance P. Neuropeptides Jun 2013, 47(3):157-162.
61. Pemberton A.D., Brown J.K., Craig N.M., Pate J., McLean K., Inglis N.F., et al. Changes in protein expression in the sheep abomasum following trickle infection with Teladorsagia circumcincta. Parasitology Mar 2012, 139(3):375-385.
62. Das S.K., Sharma N.K., Hasstedt S.J., Mondal A.K., Ma L., Langberg K.A., et al. An integrative genomics approach identifies activation of thioredoxin/thioredoxin reductase-1-mediated oxidative stress defense pathway and inhibition of angiogenesis in obese nondiabetic human subjects. J Clin Endocrinol Metab Aug 2011, 96(8):E1308-E1313.
63. Joo J.I., Oh T.S., Kim D.H., Choi D.K., Wang X., Choi J.W., et al. Differential expression of adipose tissue proteins between obesity-susceptible and -resistant rats fed a high-fat diet. Proteomics Apr 2011, 11(8):1429-1448.
64. Pérez-Pérez R., López J.A., García-Santos E., Camafeita E., Gómez-Serrano M., Ortega-Delgado F.J., et al. Uncovering suitable reference proteins for expression studies in human adipose tissue with relevance to obesity. PLoS One Jan 2012, 7(1):e30326.
65. Aminlari L., Tavana M., Kazemipour N. Rhodanese distribution in different tissues of rabbits. Comp Clin Pathol Jun 2013, 1-4. [in press]. 10.1007/s00580-013-1772-y.
66. Ousman S.S., Tomooka B.H., van Noort J.M., Wawrousek E.F., O'Connor K.C., Hafler D.A., et al. Protective and therapeutic role for alphaB-crystallin in autoimmune demyelination. Nature Jul 2007, 448(7152):474-479.
67. Lavatelli F., Perlman D.H., Spencer B., Prokaeva T., McComb M.E., Théberge R., et al. Amyloidogenic and associated proteins in systemic amyloidosis proteome of adipose tissue. Mol Cell Proteomics Aug 2008, 7(8):1570-1583.
68. Shao W., Zhang S.Z., Tang M., Zhang X.H., Zhou Z., Yin Y.Q., et al. Suppression of neuroinflammation by astrocytic dopamine D2 receptors via αB-crystallin. Nature Feb 2013, 494(7435):90-94.
69. Dubin R.A., Wawrousek E.F., Piatigorsky J. Expression of the murine αB-Crystallin gene is not restricted to the lens. Mol Cell Biol Mar 1989, 9(3):1083-1091.
70. Kumar P.A., Haseeb A., Suryanarayana P., Ehtesham N.Z., Reddy G.B. Elevated expression of alphaA- and alphaB-crystallins in streptozotocin-induced diabetic rat. Arch Biochem Biophys Dec 2005, 444(2):77-83.
71. Valle A., Sastre-Serra J., Roca P., Oliver J. Modulation of white adipose tissue proteome by aging and calorie restriction. Aging Cell Oct 2010, 9(5):882-894.
72. Ni Y., Ji C., Wang B., Qiu J., Wang J., Guo X. A Novel pro-adipogenesis factor abundant in adipose tissues and over-expressed in obesity acts upstream of PPARγ and C/EBPα. J Bioenerg Biomembr Jun 2013, 45(3):219-228.
73. Vizcaino J.A., CÔté R.G., Csordas A., Dianes J.A., Fabregat A., Foster J.M., et al. The Proteomics Identifications (PRIDE) database and associated tools: status in 2013. Nucleic Acids Res Jan 2013, 41(D1):D1063-D1069.