The effect of serum withdrawal on the protein profile of quiescent human dermal fibroblasts in primary cell culture

Proteomics

Volumn 8, Issue 1, 2008, Pages 66-82

  Boraldi, Federica ^a   Annovi, Giulia ^a   Paolinelli Devincenzi, Chiara ^a   Tiozzo, Roberta ^a   Quaglino, Daniela ^a,b  

^a UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^b Department of Biomedical Sciences ^*  (Italy)

Author keywords

Dermal fibroblasts; Primary cell culture; ROS production; Serum withdrawal

Indexed keywords

ELASTIN; HYDROETHIDINE; PROTEIN; PROTEOME; REACTIVE OXYGEN METABOLITE;

ADULT; ARTICLE; CELL COUNT; CELL CULTURE; CELL FUNCTION; CELL GROWTH; CELL METABOLISM; CELL STRUCTURE; CELL VIABILITY; CHEMICAL ANALYSIS; COLORIMETRY; CONTROLLED STUDY; CYTOSKELETON; ENVIRONMENTAL CHANGE; FEMALE; GLYCOLYSIS; HUMAN; HUMAN CELL; HUMAN TISSUE; MASS SPECTROMETRY; MESENCHYME CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; SERUM; SKIN FIBROBLAST; STRESS;

ADULT; AMINO ACID SEQUENCE; CELL CULTURE TECHNIQUES; CELLS, CULTURED; FEMALE; FIBROBLASTS; G0 PHASE; HUMANS; MOLECULAR SEQUENCE DATA; PROTEINS; PROTEOME; SERUM; SKIN;

EID: 38149045837     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.200700833     Document Type: Article

References (76)

1. Chang, H. Y., Sneddon, J. B., Alizadeh, A. A., Sood, R. et al., Gene expression signature of fibroblast serum response predicts human cancer progression: Similarities between tumors and wounds. PLoS Biol. 2004, 2, E7.
2. Iyer, V. R., Eisen, M. B., Ross, D. T., Schuler, G. et al., The transcriptional program in the response of human fibroblasts to serum. Science 1999, 283, 83-87.
3. Gos, M., Miloszewska, J., Swoboda, P., Trembacz, H. et al., Cellular quiescence induced by contact inhibition or serum withdrawal in C3H10T1/2 cells. Cell Prolif. 2005, 38, 107-116.
4. Simm, A., Bertsch, G., Frank, H., Zimmermann, U. et al., Cell death of AKR-2B fibroblasts after serum removal: A process between apoptosis and necrosis. J. Cell Sci. 1997, 110, 819-828.
5. Leicht, M., Briest, W., Holzl, A., Zimmer, H. G., Serum depletion induces cell loss of rat cardiac fibroblasts and increased expression of extracellular matrix proteins in surviving cells. Cardiovasc. Res. 2001, 52, 429-437.
6. Leicht, M., Marx, G., Karbach, D., Gekle, M. et al., Mechanism of cell death of rat cardiac fibroblasts induced by serum depletion. Mol. Cell. Biochem. 2003, 251, 119-126.
7. Kalckar, H. M., Ullrey, D. B., Laursen, R. A., Effects of combined glutamine and serum deprivation on glucose control of hexose transport in mammalian fibroblast cultures. Proc. Natl. Acad. Sci. USA 1980, 77, 5958-5961.
8. Tamm, I., Kikuchi, T., Krueger, J., Murphy, J. S., Dissociation between early loss of actin fibres and subsequent cell death in serum-deprived quiescent Balb/c-3T3 cells. Cell. Signal. 1992, 4, 675-686.
9. Paddenberg, R., Loos, S., Schoneberger, H. J., Wulf, S. et al., Serum withdrawal induces a redistribution of intracellular gelsolin towards F-actin in NIH 3T3 fibroblasts preceding apoptotic cell death. Eur. J. Cell Biol. 2001, 80, 366-378.
10. Rittié, L., Fisher, G. J., Isolation and culture of skin fibroblasts. Methods Mol. Med. 2005, 117, 83-98.
11. Everts, V., van der Zee, E., Creemers, L., Beertsen, W., Phagocytosis and intracellular digestion of collagen, its role in turnover and remodelling. Histochem. J. 1996, 28, 229-245.
12. Meyyappan, M., Wheaton, K., Riabowol, K. T., Decreased expression and activity of the immediate-early growth response (Egr-1) gene product during cellular senescence. J. Cell Physiol. 1999, 179, 29-39.
13. Bradford, M. M., A rapid and sensitive method forthe quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72, 248-254.
14. Bjellqvist, B., Pasquali, C., Ravier, F., Sanchez, J. C. et al., A nonlinear wide-range immobilized pH gradient for two-dimensional electrophoresis and its definition in a relevant pH scale. Electrophoresis 1993, 14, 1357-1365.
15. Hochstrasser, D. F., Patchomik, A., Merril, C. R., Development of Polyacrylamide gels that improve the separation of proteins and their detection by silver staining. Anal. Biochem. 1988, 173, 412-423.
16. Shevchenko, A., Wilm, M., Vorm, O., Mann, M., Mass spectrometry sequencing of proteins silver-stained Polyacrylamide gels. Anal. Chem. 1996, 68, 850-858.
17. Gharahdaghi, F., Weinberg, C. R., Meagher, D. A., Imai, B. S. et al., Mass spectrometry identification of proteins from silver-stained Polyacrylamide gel: A method forthe removal of silver ions to enhance sensitivity. Electrophoresis 1999, 20, 601-605.
18. Honore, B., Ostergaard, M., Vorum, H., Functional genomics studied by proteomics. Bioessays 2004, 26, 901-915.
19. Molloy, M. P., Brzezinski, E. E., Hang, J., McDowell, M. T. et al., Overcoming technical variation and biological variation in quantitative proteomics. Proteomics 2003, 3, 1912-1919.
20. Pardo, M., Garcia, A., Thomas, B., Pineiro, A. et al., Proteome analysis of a human uveal melanoma primary cell culture by 2-DE and MS. Proteomics 2005, 5, 4980-4993.
21. Pucci-Minafra, I., Cancemi, P., Fontana, S., Minafra, L. et al., Expanding the protein catalogue in the proteome reference map of human breast cancer cells. Proteomics 2006, 6, 2609-2625.
22. Honn, K. V., Singley, J. A., Chavin, W., Fetal bovine serum: A multivariate standard. Proc. Soc. Exp. Biol. Med. 1975, 149, 344-347.
23. Liu, H., Adler, A. S., Segal, E., Chang, H. Y., A transcriptional program mediating entry into cellular quiescence. PLoS Genet. 2007, 3, e91.
24. Khalifa, A., Chion, T., Quiang, H., Agarwal, N., Cooper, N. G., Microarray reveals complement components are regulated in the serum-deprived rat retinal ganglion cell line. Mol. Vis. 2007, 13, 293-308.
25. Kulkarni, G. V., McCulloch, C. A., Serum deprivation induces apoptotic cell death in a subset of Balb/c 3T3 fibroblasts. J. Cell Sci. 1994, 107, 1169-1179.
26. Flora, S. J., Role of free radicals and antioxidants in health and disease. Cell. Mol. Biol. 2007, 53, 1-2.
27. Yim, M. B., Yim, H. S., Lee, C., Kang, S. O. et al., Protein glycation: Creation of catalytic sites for free radical generation. Ann. NY Acad. Sci. 2001, 928, 48-53.
28. Brownlee, M., Biochemistry and molecular cell biology of diabetic complications. Nature 2001, 414, 813-820.
29. Masoro, E. J., Possible mechanisms underlying the antiaging actions of caloric restriction. Toxicol. Pathol. 1996, 24, 738-741.
30. Maestre, I., Jordan, J., Calvo, S., Reig, J. A. et al., Mitochondrial dysfunction is involved in apoptosis induced by serum withdrawal and fatty acids in the beta-cell line INS-1. Endocrinology 2003, 144, 335-345.
31. Zhang, Y., Fong, C. C., Wong, M. S., Tzang, C. H. et al., Molecular mechanisms of survival and apoptosis in RAW 264.7 macrophages under oxidative stress. Apoptosis 2005, 10, 545-556.
32. Pereira, C., Santos, M. S., Oliveira, C. I., Involvement of oxidative stress on the impairment of energy metabolism induced by A beta peptides on PC12 cells: protection by antioxidants. Neurobiol. Dis. 1999, 6, 209-219.
33. Cabiscol, E., Piulats, E., Echave, P., Herrero, E., Ros, J., Oxidative stress promotes specific protein damage in Saccharomyces cerevisiae. J. Biol. Chem. 2000, 275, 27393-27398.
34. Shenton, D., Grant, C. M., Protein S-thiolation targets glycolysis and protein synthesis in response to oxidative stress in the yeast Saccharomyces cerevisiae. Biochem. J. 2003, 374, 513-519.
35. Hunt, N. D., Hyun, D. H., Allard, J. S., Minor, R. K. et al., Bioenergetics of aging and calorie restriction. Ageing Res. Rev. 2006, 5, 125-143.
36. Wlaschek, M., Tantcheva-Poór, I., Naderi, L., Ma, W. et al., Solar UV irradiation and dermal photoaging. J. Photochem. Photobiol. B 2001, 63, 41-51.
37. Kawaguchi, Y., Tanaka, H., Okada, T., Konishi, H. et al., Effect of reactive oxygen species on the elastin mRNA expression in cultured human dermal fibroblasts. Free Radic. Biol. Med. 1997, 23, 162-165.
38. Hayashi, A., Ryu, A., Suzuki, T., Kawada, A., Tajima, S., In vitro degradation of tropoelastin by reactive oxygen species. Arch. Dermatol. Res. 1998, 290, 497-500.
39. Wachi, H., Seyama, Y., Yamashita, S., Tajima, S., Cell cycle-dependent regulation of elastin gene in cultured chick vascular smooth-muscle cells. Biochem. J. 1995, 309, 575-579.
40. Kiningham, K. K., St. Clair, D. R., Overexpression of manganese superoxide dismutase selectively modulates the activity of Jun-associated transcription factors in fibrosarcoma cells. Cancer Res. 1997, 57, 5265-5271.
41. Simon, V. R., Swayne, T. C., Pon, L. A., Actin-dependent mitochondrial motility in mitotic yeast and cell-free systems: Identification of a motor activity on the mitochondrial surface. J. Cell Biol. 1995, 130, 345-354.
42. Cavelier, G., Theory of malignant cell transformation by superoxide fate coupled with cytoskeletal electron-transport and electron-transfer. Med. Hypotheses 2000, 54, 95-98.
43. Davis-Smyth, T., Duncan, R. C., Zheng, T., Michelotti, G. et al., The far upstream element-binding proteins comprise an ancient family of single-strand DNA-binding transactivators. J. Biol. Chem. 1996, 271, 31679-31687.
44. Dalle-Donne, I., Rossi, R., Milzani, A., Di-Simplicio, P., Colombo, R., The actin cytoskeleton response to oxidants: from small heat shock protein phosphorylation to changes in the redox state of actin itself. Free Radic. Biol. Med. 2001, 31, 1624-1632.
45. Kaur, I. P., Geetha, T., Screening methods for antioxidants-a review. Mini Rev. Med. Chem. 2006, 6, 305-312.
46. Gerke, V., Moss, S. E., Annexins: From structure to function. Physiol. Rev. 2002, 82, 331-371.
47. Van-Gansen, P., Siebertz, B., Capone, B., Malherbe, L., Relationships between cytoplasmic microtubular complex, DNA synthesis and cell morphology in mouse embryonic fibroblasts (effects of age, serum deprivation, aphidicolin, cytochalasin B and colchicine). Biol. Cell. 1984, 52, 161-174.
48. Wang, E., Gundersen, D., Increased organization of cytoskeleton accompanying the aging of human fibroblasts In vitro. Exp. Cell Res. 1984, 154, 191-202.
49. Chaponnier, C., Gabbiani, G., Pathological situations characterized by altered actin isoform expression. J. Pathol. 2004, 204, 386-395.
50. Schmittgen, T. D., Zakrajsek, B. A., Effect of experimental treatment on housekeeping gene expression: validation by real-time, quantitative RT-PCR. J. Biochem. Biophys. Methods 2000, 46, 69-81.
51. Hotulainen, P., Paunola, E., Vartiainen, M. K., Lappalainen, P., Actin-depolymerizing factor and cofilin-1 play overlapping roles in promoting rapid F-actin depolymerization in mammalian nonmuscle cells. Mol. Biol. Cell 2005, 16, 649-664.
52. Ono, S., Mechanism of depolymerization and severing of actin filaments and its significance in cytoskeletal dynamics. Int. Rev. Cytol. 2007, 258, 1-82.
53. Bamburg, J. R., Wiggan, O. P., ADF/cofilin and actin dynamics in disease. Trends Cell Biol. 2002, 12, 598-605.
54. Wiesner, S., Legate, K. R., Fassler, R., Integrin-actin interactions. Cell. Mol. Life Sci. 2005, 62, 1081-1099.
55. Nair, R. R., Solway, J., Boyd, D. D., Expression cloning identifies transgelin (SM22) as a novel repressor of 92-kDa type IV collagenase (MMP-9) expression. J. Biol. Chem. 2006, 281, 26424-26436.
56. Uemura, S., Matsushita, H., Li, W., Glassford, A. J. et al., Diabetes mellitus enhances vascular matrix metalloproteinase activity: Role of oxidative stress. Circ. Res. 2001, 88, 1291-1298.
57. Kameda, K., Matsunaga, T., Abe, N., Hanada, H. et al., Correlation of oxidative stress with activity of matrix metalloproteinase in patients with coronary artery disease. Possible role for left ventricular remodelling. Eur. Heart J. 2003, 24, 2180-2185.
58. Roberts, C. K., Won, D., Pruthi, S., Kurtovic, S. et al., Effect of a short-term diet and exercise intervention on oxidative stress, inflammation, MMP-9, and monocyte chemotactic activity in men with metabolic syndrome factors. J. Appl. Physiol. 2006, 100, 1657-65.
59. Siwik, D. A., Pagano, P. J., Colucci, W. S., Oxidative stress regulates collagen synthesis and matrix metalloproteinase activity in cardiac fibroblasts. Am. J. Physiol. Cell Physiol. 2001, 280, C53-C60.
60. Hayes, M. J., Shao, D., Bailly, M., Moss, S. E., Regulation of actin dynamics by annexin 2. EMBO J. 2006, 25, 1816-1826.
61. Boraldi, F., Bini, L., Liberatori, S. et al., Proteome analysis of dermal fibroblasts cultured In vitro from human healthy subjects of different ages. Proteomics 2003, 3, 917-929.
62. Chasserot-Golaz, S., Vitale, N., Umbrecht-Jenck, E., Knight, D. et al., Annexin 2 promotes the formation of lipid microdomains required for calcium-regulated exocytosis of dense-core vesicles. Mol. Biol. Cell 2005, 16, 1108-1119.
63. Wheatley, D. N., Yin, Z., Degradation of intracellular endogenous proteins following serum deprivation in mammalian cell cultures: theoretical considerations of the role of very-fast turnover proteins in growth regulation. Acta Biol. Hung. 1991, 42, 161-174.
64. Cavallius, J., Rattan, S. I., Clark, B. F., Changes in activity and amount of active elongation factor 1 alpha in aging and immortal human fibroblast cultures. Exp. Gerontol. 1986, 21, 149-157.
65. Talapatra, S., Wagner, J. D., Thompson, C. B., Elongation factor-1 alpha is a selective regulator of growth factor withdrawal and ER stress-induced apoptosis. Cell Death Differ. 2002, 9, 856-861.
66. Ma, Y., Hendershot, L. M., The unfolding tale of the unfolded protein response. Cell 2001, 107, 827-830.
67. Fuertes, G., Martin De Llano, J. J., Villarroya, A., Rivett, A. J. et al., Changes in the proteolytic activities of proteasomes and lysosomes in human fibroblasts produced by serum withdrawal, amino-acid deprivation and confluent conditions. Biochem. J. 2003, 375, 75-86.
68. Tessari, P., Puricelli, L., Iori, E., Arrigoni, G. et al., Altered chaperone and protein turnover regulators expression in cultured skin fibroblasts from type 1 diabetes mellitus with nephropathy. J. Proteome Res. 2007, 6, 976-986.
69. Hawkes, C., Kabogo, D., Amritral, A., Kar, S., Up-regulation of cation-independent mannose 6-phosphate receptor and endosomal-lysosomal markers in surviving neurons after 192-IgG-saporin administrations into the adult rat brain. Am. J. Pathol. 2006, 169, 1140-1154.
70. Ellgaard, L., Helenius, A., Quality control in the endoplasmic reticulum. Nat. Rev. Mol. Cell. Biol. 2003, 4, 181-191.
71. Cribb, A. E., Peyrou, M., Muruganandan, S., Schneider, L., The endoplasmic reticulum in xenobiotic toxicity. Drug Metab. Rev. 2005, 37, 405-442.
72. Nguyen, T. O., Capra, J. D., Sontheimer, R. D., Calreticulin is transcriptionally upregulated by heat shock, calcium and heavy metals. Mol. Immunol. 1996, 33, 379-386.
73. Llewellyn, D. H., Roderick, H. L., Overexpression of calreticulin fails to abolish its induction by perturbation of normal ER function. Biochem. Cell Biol. 1998, 76, 875-880.
74. Rabek, J. P., Boylston, W. H., Papaconstantinou, J., Carbonylation of ER chaperone proteins in aged mouse liver. Biochem. Biophys. Res. Commun. 2003, 305, 566-572.
75. Kageyama, K., Ihara, Y., Goto, S., Urata, Y. et al., Overexpression of calreticulin modulates protein kinase B/Akt signaling to promote apoptosis during cardiac differentiation of cardiomyoblast H9c2 cells. J. Biol. Chem. 2002, 277, 19255-19264.
76. Tresini, M., Lorenzini, A., Frisoni, L., Allen, R. G., Cristofalo, V. J., Lack of Elk-1 phosphorylation and dysregulation of the extracellular regulated kinase signaling pathway in senescent human fibroblast. Exp. Cell. Res. 2001, 269, 287-300.