Identification of novel human adipocyte secreted proteins by using SGBS cells

Journal of Proteome Research

Volumn 9, Issue 10, 2010, Pages 5389-5401

  Rosenow, Anja ^a   Arrey, Tabiwang N ^b   Bouwman, Freek G ^a   Noben, Jean Paul ^c   Wabitsch, Martin ^d   Mariman, Edwin C M ^a   Karas, Michael ^b   Renes, Johan ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b GOETHE UNIVERSITY   (Germany)

^c HASSELT UNIVERSITY   (Belgium)

^d UNIVERSITY OF ULM   (Germany)

Author keywords

2D MS MS; off line LC MS MS; secretion; SGBS (pre)adipocyte

Indexed keywords

ADIPOCYTOKINE; BREFELDIN A;

ADIPOCYTE; ARTICLE; CELL DIFFERENTIATION; CELL STRAIN; CONTROLLED STUDY; ELECTROSPRAY MASS SPECTROMETRY; ENDOPLASMIC RETICULUM; GOLGI COMPLEX; HUMAN; HUMAN CELL; LIQUID CHROMATOGRAPHY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN SECRETION; SIMPSON GOLABI BEHMEL SYNDROME; SIMPSON GOLABI BEHMEL SYNDROME CELL; TANDEM MASS SPECTROMETRY; TWO DIMENSIONAL GEL ELECTROPHORESIS; UNINDEXED SEQUENCE;

ADIPOCYTES; CELLS, CULTURED; CHROMATOGRAPHY, LIQUID; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; GROWTH DISORDERS; HUMANS; PROTEINS; PROTEOMICS; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; SYNDROME;

EID: 77957362619     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr100621g     Document Type: Article

References (62)

1. Dixon, J. B. The effect of obesity on health outcomes Mol. Cell. Endocrinol. 2010, 316 (2) 104-8
2. Runge, C. F. Economic consequences of the obese Diabetes 2007, 56 (11) 2668-72
3. Wang, Y.; Beydoun, M. A.; Liang, L.; Caballero, B.; Kumanyika, S. K. Will all Americans become overweight or obese? estimating the progression and cost of the US obesity epidemic Obesity (Silver Spring) 2008, 16 (10) 2323-30
4. Diamanti-Kandarakis, E.; Palioura, E.; Kandarakis, S. A.; Koutsilieris, M. The Impact of Endocrine Disruptors on Endocrine Targets Horm. Metab. Res. 2010, 42 (8) 543-52
5. Gregoire, F. M. Adipocyte differentiation: from fibroblast to endocrine cell Exp. Biol. Med. (Maywood) 2001, 226 (11) 997-1002
6. Goossens, G. H. The role of adipose tissue dysfunction in the pathogenesis of obesity-related insulin resistance Physiol. Behav. 2008, 94 (2) 206-18
7. Mohamed-Ali, V.; Pinkney, J. H.; Coppack, S. W. Adipose tissue as an endocrine and paracrine organ Int. J. Obes. Relat. Metab. Disord. 1998, 22 (12) 1145-58
8. Wang, P.; Mariman, E.; Keijer, J.; Bouwman, F.; Noben, J. P.; Robben, J.; Renes, J. Profiling of the secreted proteins during 3T3-L1 adipocyte differentiation leads to the identification of novel adipokines Cell. Mol. Life Sci. 2004, 61 (18) 2405-17
9. Chen, H.; Charlat, O.; Tartaglia, L. A.; Woolf, E. A.; Weng, X.; Ellis, S. J.; Lakey, N. D.; Culpepper, J.; Moore, K. J.; Breitbart, R. E.; Duyk, G. M.; Tepper, R. I.; Morgenstern, J. P. Evidence that the diabetes gene encodes the leptin receptor: identification of a mutation in the leptin receptor gene in db/db mice Cell 1996, 84 (3) 491-5
10. Himms-Hagen, J. Physiological roles of the leptin endocrine system: differences between mice and humans Crit. Rev. Clin. Lab. Sci. 1999, 36 (6) 575-655
11. Kadowaki, T.; Yamauchi, T. Adiponectin and adiponectin receptors Endocr. Rev. 2005, 26 (3) 439-51
12. Patel, L.; Buckels, A. C.; Kinghorn, I. J.; Murdock, P. R.; Holbrook, J. D.; Plumpton, C.; Macphee, C. H.; Smith, S. A. Resistin is expressed in human macrophages and directly regulated by PPAR gamma activators Biochem. Biophys. Res. Commun. 2003, 300 (2) 472-6
13. Rosen, B. S.; Cook, K. S.; Yaglom, J.; Groves, D. L.; Volanakis, J. E.; Damm, D.; White, T.; Spiegelman, B. M. Adipsin and complement factor D activity: an immune-related defect in obesity Science 1989, 244 (4911) 1483-7
14. Steppan, C. M.; Bailey, S. T.; Bhat, S.; Brown, E. J.; Banerjee, R. R.; Wright, C. M.; Patel, H. R.; Ahima, R. S.; Lazar, M. A. The hormone resistin links obesity to diabetes Nature 2001, 409 (6818) 307-12
15. Wang, P.; Mariman, E.; Renes, J.; Keijer, J. The secretory function of adipocytes in the physiology of white adipose tissue J. Cell Physiol. 2008, 216 (1) 3-13
16. Wabitsch, M.; Brenner, R. E.; Melzner, I.; Braun, M.; Moller, P.; Heinze, E.; Debatin, K. M.; Hauner, H. Characterization of a human preadipocyte cell strain with high capacity for adipose differentiation Int. J. Obes. Relat. Metab. Disord. 2001, 25 (1) 8-15
17. Nickel, W. The mystery of nonclassical protein secretion. A current view on cargo proteins and potential export routes Eur. J. Biochem. 2003, 270 (10) 2109-19
18. Orci, L.; Tagaya, M.; Amherdt, M.; Perrelet, A.; Donaldson, J. G.; Lippincott-Schwartz, J.; Klausner, R. D.; Rothman, J. E.; Brefeldin, A. a drug that blocks secretion, prevents the assembly of non-clathrin-coated buds on Golgi cisternae Cell 1991, 64 (6) 1183-95
19. Bouwman, F.; Renes, J.; Mariman, E. A combination of protein profiling and isotopomer analysis using matrix-assisted laser desorption/ionization-time of flight mass spectrometry reveals an active metabolism of the extracellular matrix of 3T3-L1 adipocytes Proteomics 2004, 4 (12) 3855-63
20. Cranenburg, E. C.; Vermeer, C.; Koos, R.; Boumans, M. L.; Hackeng, T. M.; Bouwman, F. G.; Kwaijtaal, M.; Brandenburg, V. M.; Ketteler, M.; Schurgers, L. J. The circulating inactive form of matrix Gla Protein (ucMGP) as a biomarker for cardiovascular calcification J. Vasc. Res. 2008, 45 (5) 427-36
21. Dumont, D.; Noben, J. P.; Moreels, M.; Vanderlocht, J.; Hellings, N.; Vandenabeele, F.; Lambrichts, I.; Stinissen, P.; Robben, J. Characterization of mature rat oligodendrocytes: a proteomic approach J. Neurochem. 2007, 102 (2) 562-76
22. Alvarez-Llamas, G.; Szalowska, E.; de Vries, M. P.; Weening, D.; Landman, K.; Hoek, A.; Wolffenbuttel, B. H.; Roelofsen, H.; Vonk, R. J. Characterization of the human visceral adipose tissue secretome Mol. Cell. Proteomics 2007, 6 (4) 589-600
23. Roelofsen, H.; Dijkstra, M.; Weening, D.; de Vries, M. P.; Hoek, A.; Vonk, R. J. Comparison of isotope-labeled amino acid incorporation rates (CILAIR) provides a quantitative method to study tissue secretomes Mol. Cell. Proteomics 2009, 8 (2) 316-24
24. Chiellini, C.; Cochet, O.; Negroni, L.; Samson, M.; Poggi, M.; Ailhaud, G.; Alessi, M. C.; Dani, C.; Amri, E. Z. Characterization of human mesenchymal stem cell secretome at early steps of adipocyte and osteoblast differentiation BMC Mol. Biol. 2008, 9, 26
25. Sell, H.; Dietze-Schroeder, D.; Eckardt, K.; Eckel, J. Cytokine secretion by human adipocytes is differentially regulated by adiponectin, AICAR and troglitazone Biochem. Biophys. Res. Commun. 2006, 343 (3) 700-6
26. Zvonic, S.; Lefevre, M.; Kilroy, G.; Floyd, Z. E.; DeLany, J. P.; Kheterpal, I.; Gravois, A.; Dow, R.; White, A.; Wu, X.; Gimble, J. M. Secretome of primary cultures of human adipose-derived stem cells: modulation of serpins by adipogenesis Mol. Cell. Proteomics 2007, 6 (1) 18-28
27. Aoki, N.; Jin-no, S.; Nakagawa, Y.; Asai, N.; Arakawa, E.; Tamura, N.; Tamura, T.; Matsuda, T. Identification and characterization of microvesicles secreted by 3T3-L1 adipocytes: redox- and hormone-dependent induction of milk fat globule-epidermal growth factor 8-associated microvesicles Endocrinology 2007, 148 (8) 3850-62
28. Chen, X.; Cushman, S. W.; Pannell, L. K.; Hess, S. Quantitative proteomic analysis of the secretory proteins from rat adipose cells using a 2D liquid chromatography-MS/MS approach J. Proteome Res. 2005, 4 (2) 570-7
29. Kratchmarova, I.; Kalume, D. E.; Blagoev, B.; Scherer, P. E.; Podtelejnikov, A. V.; Molina, H.; Bickel, P. E.; Andersen, J. S.; Fernandez, M. M.; Bunkenborg, J.; Roepstorff, P.; Kristiansen, K.; Lodish, H. F.; Mann, M.; Pandey, A. A proteomic approach for identification of secreted proteins during the differentiation of 3T3-L1 preadipocytes to adipocytes Mol. Cell. Proteomics 2002, 1 (3) 213-22
30. Lim, J. M.; Sherling, D.; Teo, C. F.; Hausman, D. B.; Lin, D.; Wells, L. Defining the regulated secreted proteome of rodent adipocytes upon the induction of insulin resistance J. Proteome Res. 2008, 7 (3) 1251-63
31. Molina, H.; Yang, Y.; Ruch, T.; Kim, J. W.; Mortensen, P.; Otto, T.; Nalli, A.; Tang, Q. Q.; Lane, M. D.; Chaerkady, R.; Pandey, A. Temporal profiling of the adipocyte proteome during differentiation using a five-plex SILAC based strategy J. Proteome Res. 2009, 8 (1) 48-58
32. Hossner, K. L.; Yemm, R.; Vierck, J.; Dodson, M. V. Insulin-like growth factor (IGF)-I and -II and IGFBP secretion by ovine satellite cell strains grown alone or in coculture with 3T3-L1 preadipocytes In Vitro Cell Dev. Biol. Anim. 1997, 33 (10) 791-5
33. Wabitsch, M.; Heinze, E.; Debatin, K. M.; Blum, W. F. IGF-I- and IGFBP-3-expression in cultured human preadipocytes and adipocytes Horm. Metab. Res. 2000, 32 (11-12) 555-9
34. Baxter, R. C.; Twigg, S. M. Actions of IGF binding proteins and related proteins in adipose tissue Trends Endocrinol. Metab. 2009, 20 (10) 499-505
35. Hausman, G. J.; Poulos, S. P.; Richardson, R. L.; Barb, C. R.; Andacht, T.; Kirk, H. C.; Mynatt, R. L. Secreted proteins and genes in fetal and neonatal pig adipose tissue and stromal-vascular cells J. Anim. Sci. 2006, 84 (7) 1666-81
36. Kallio, P.; Tolppanen, A. M.; Kolehmainen, M.; Poutanen, K.; Lindstrom, J.; Tuomilehto, J.; Kuulasmaa, T.; Kuusisto, J.; Pulkkinen, L.; Uusitupa, M. Association of sequence variations in the gene encoding insulin-like growth factor binding protein 5 with adiponectin Int. J. Obes. (London) 2009, 33 (1) 80-8
37. Fischer-Posovszky, P.; Newell, F. S.; Wabitsch, M.; Tornqvist, H. E. Human SGBS Cells-a Unique Tool for Studies of Human Fat Cell Biology Obes. Facts 2008, 1 (4) 184-189
38. Hauner, H. Secretory factors from human adipose tissue and their functional role Proc. Nutr. Soc. 2005, 64 (2) 163-9
39. Karastergiou, K.; Mohamed-Ali, V. The autocrine and paracrine roles of adipokines Mol. Cell. Endocrinol. 2010, 318 (1-2) 69-78
40. Trayhurn, P.; Bing, C.; Wood, I. S. Adipose tissue and adipokines - energy regulation from the human perspective J. Nutr. 2006, 136 (7 Suppl) 1935S-1939S
41. Vazquez-Vela, M. E.; Torres, N.; Tovar, A. R. White adipose tissue as endocrine organ and its role in obesity Arch. Med. Res. 2008, 39 (8) 715-28
42. Fain, J. N. Release of interleukins and other inflammatory cytokines by human adipose tissue is enhanced in obesity and primarily due to the nonfat cells Vitam. Horm. 2006, 74, 443-77
43. Mariman, E. C.; Wang, P. Adipocyte extracellular matrix composition, dynamics and role in obesity Cell. Mol. Life Sci. 2010, 67 (8) 1277-92
44. Wang, P.; Bouwman, F. G.; Mariman, E. C. Generally detected proteins in comparative proteomics - a matter of cellular stress response Proteomics 2009, 9 (11) 2955-66
45. Rand, J. H.; Wu, X. X.; Quinn, A. S.; Taatjes, D. J. Resistance to annexin A5 anticoagulant activity: a thrombogenic mechanism for the antiphospholipid syndrome Lupus 2008, 17 (10) 922-30
46. Urso, B.; Niesler, C. U.; ORahilly, S.; Siddle, K. Comparison of anti-apoptotic signalling by the insulin receptor and IGF-I receptor in preadipocytes and adipocytes Cell Signal. 2001, 13 (4) 279-85
47. Fink, S. L.; Cookson, B. T. Apoptosis, pyroptosis, and necrosis: mechanistic description of dead and dying eukaryotic cells Infect. Immun. 2005, 73 (4) 1907-16
48. Jin, Z. G.; Melaragno, M. G.; Liao, D. F.; Yan, C.; Haendeler, J.; Suh, Y. A.; Lambeth, J. D.; Berk, B. C. Cyclophilin A is a secreted growth factor induced by oxidative stress Circ. Res. 2000, 87 (9) 789-96
49. Jin, Z.-G.; Lungu, A. O.; Xie, L.; Wang, M.; Wong, C.; Berk, B. C. Cyclophilin A Is a Proinflammatory Cytokine that Activates Endothelial Cells Arterioscler. Thromb. Vasc. Biol. 2004, 24 (7) 1186-1191
50. Sherry, B.; Yarlett, N.; Strupp, A.; Cerami, A. Identification of cyclophilin as a proinflammatory secretory product of lipopolysaccharide- activated macrophages Proc. Natl. Acad. Sci. U.S.A. 1992, 89 (8) 3511-5
51. Suzuki, J.; Jin, Z.-G.; Meoli, D. F.; Matoba, T.; Berk, B. C. Cyclophilin A Is Secreted by a Vesicular Pathway in Vascular Smooth Muscle Cells Circ. Res. 2006, 98 (6) 811-817
52. Tanaka, K.; Arao, T.; Maegawa, M.; Matsumoto, K.; Kaneda, H.; Kudo, K.; Fujita, Y.; Yokote, H.; Yanagihara, K.; Yamada, Y.; Okamoto, I.; Nakagawa, K.; Nishio, K. SRPX2 is overexpressed in gastric cancer and promotes cellular migration and adhesion Int. J. Cancer 2009, 124 (5) 1072-80
53. Kinseth, M. A.; Anjard, C.; Fuller, D.; Guizzunti, G.; Loomis, W. F.; Malhotra, V. The Golgi-associated protein GRASP is required for unconventional protein secretion during development Cell 2007, 130 (3) 524-34
54. Ejaz, A.; Wu, D.; Kwan, P.; Meydani, M. Curcumin inhibits adipogenesis in 3T3-L1 adipocytes and angiogenesis and obesity in C57/BL mice J. Nutr. 2009, 139 (5) 919-25
55. Zhou, X. R.; Sun, C. H.; Liu, J. R.; Zhao, D. Dietary conjugated linoleic acid increases PPAR gamma gene expression in adipose tissue of obese rat, and improves insulin resistance Growth Horm. IGF Res. 2008, 18 (5) 361-8
56. Dahlman, I.; Eriksson, P.; Kaaman, M.; Jiao, H.; Lindgren, C. M.; Kere, J.; Arner, P. alpha2-Heremans-Schmid glycoprotein gene polymorphisms are associated with adipocyte insulin action Diabetologia 2004, 47 (11) 1974-9
57. Ix, J. H.; Sharma, K. Mechanisms linking obesity, chronic kidney disease, and fatty liver disease: the roles of fetuin-A, adiponectin, and AMPK J. Am. Soc. Nephrol. 2010, 21 (3) 406-12
58. Decitre, M.; Gleyzal, C.; Raccurt, M.; Peyrol, S.; Aubert-Foucher, E.; Csiszar, K.; Sommer, P. Lysyl oxidase-like protein localizes to sites of de novo fibrinogenesis in fibrosis and in the early stromal reaction of ductal breast carcinomas Lab. Invest. 1998, 78 (2) 143-51
59. Gettins, P. G. Serpin structure, mechanism, and function Chem. Rev. 2002, 102 (12) 4751-804
60. Silverman, G. A.; Bird, P. I.; Carrell, R. W.; Church, F. C.; Coughlin, P. B.; Gettins, P. G.; Irving, J. A.; Lomas, D. A.; Luke, C. J.; Moyer, R. W.; Pemberton, P. A.; Remold-ODonnell, E.; Salvesen, G. S.; Travis, J.; Whisstock, J. C. The serpins are an expanding superfamily of structurally similar but functionally diverse proteins. Evolution, mechanism of inhibition, novel functions, and a revised nomenclature J. Biol. Chem. 2001, 276 (36) 33293-6
61. Nagasawa, A.; Kubota, R.; Imamura, Y.; Nagamine, K.; Wang, Y.; Asakawa, S.; Kudoh, J.; Minoshima, S.; Mashima, Y.; Oguchi, Y.; Shimizu, N. Cloning of the cDNA for a new member of the immunoglobulin superfamily (ISLR) containing leucine-rich repeat (LRR) Genomics 1997, 44 (3) 273-9
62. Wu, M.; Gan, K.; Huang, C.; Tang, Y.; Chen, Q.; Tang, K.; Li, X.; Shen, S.; Li, G. LRRC4 controls in vitro invasion of glioblastoma cells through inhibiting RPTP-zeta expression J. Neurooncol. 2006, 80 (2) 133-42