Proteomic profiling of high glucose primed monocytes identifies cyclophilin A as a potential secretory marker of inflammation in type 2 diabetes

Proteomics

Volumn 12, Issue 18, 2012, Pages 2808-2821

  Ramachandran, Surya ^a   Venugopal, Anila ^a   Sathisha, K ^b   Reshmi, G ^a   Charles, Sona ^a   Divya, G ^a   Pratap Chandran, N S ^c   Mullassari, Ajit ^d   Pillai, M Radhakrishna ^a   Kartha, C C ^a  

^a RAJIV GANDHI CENTRE FOR BIOTECHNOLOGY   (India)

^b INDIAN INSTITUTE OF SCIENCE   (India)

^c Indian Institute of Diabetes   (India)

^d MADRAS MEDICAL MISSION HOSPITAL   (India)

Author keywords

Cell biology; Hyperglycemia; Monocytes; Type 2 diabetes mellitus

Indexed keywords

CALGRANULIN; CALRETICULIN; CYCLOPHILIN A; FRUCTOSE BISPHOSPHATE ALDOLASE; GLUCOSE; IMMUNOPHILIN; ISOMERASE; MESSENGER RNA; PROHIBITIN;

ADULT; ARTICLE; ATHEROSCLEROSIS; AUTOCRINE EFFECT; BIOINFORMATICS; CELL ACTIVATION; CELL DIFFERENTIATION; CLINICAL ARTICLE; CONTROLLED STUDY; CORONARY ARTERY DISEASE; DISEASE COURSE; DOSE RESPONSE; DOWN REGULATION; ELECTROSPRAY MASS SPECTROMETRY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOBLOTTING; INFLAMMATION; LIQUID CHROMATOGRAPHY; MALE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MONOCYTE; NON INSULIN DEPENDENT DIABETES MELLITUS; NUCLEOTIDE SEQUENCE; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEOMICS; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TWO DIMENSIONAL ELECTROPHORESIS; WESTERN BLOTTING;

CELL LINE; CELLS, CULTURED; CYCLOPHILIN A; DIABETES MELLITUS, TYPE 2; FEMALE; GENE EXPRESSION REGULATION; GLUCOSE; HUMANS; INFLAMMATION; MALE; MIDDLE AGED; MONOCYTES; PROTEOME; PROTEOMICS; RNA, MESSENGER; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 84866156188     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201100586     Document Type: Article

References (56)

1. Kaiser, N., Yuli, M., Uckaya, G., Oprescu, A. I. et al., Dynamic changes in beta-cell mass and pancreatic insulin during the evolution of nutrition-dependent diabetes in Psammomys obesus: impact of glycemic control. Diabetes 2005, 54, 138-145.
2. Nesher, R., Gross, D. J., Donath, M. Y., Cerasi, E. et al., Interaction between genetic and dietary factors determines beta-cell function in Psammomys obesus, an animal model of type 2 diabetes. Diabetes 1999, 48, 731-737.
3. Sela-Brown, A., Silver, J., Brewer, G., Naveh-Many, T. et al., Identification of AUF1 as a parathyroid hormone mRNA 3'-untranslated region-binding protein that determines parathyroid hormone mRNA stability. J. Biol. Chem. 2000, 275, 7424-7429.
4. Sasson, S., Kaiser, N., Dan-Goor, M., Oron, R. et al., Substrate autoregulation of glucose transport: hexose 6-phosphate mediates the cellular distribution of glucose transporters. Diabetologia 1997, 4, 30-39.
5. Langdown, M. L., Holness, M. J., Sugden, M. C., Effects of prenatal glucocorticoid exposure on cardiac calreticulin and calsequestrin protein expression during early development and in adulthood. Biochem. J. 2003, 371, 61-69.
6. Alpert, E., Gruzman, A., Totary, H., Kaiser, N. et al., A natural protective mechanism against hyperglycaemia in vascular endothelial and smooth-muscle cells: role of glucose and 12-hydroxyeicosatetraenoic acid. Biochem. J. 2002, 362, 413-422.
7. Narkunaraja, S., Reddy, M. A., Guha, M., Natarajan, R., High glucose-induced expression of proinflammatory cytokine and chemokine genes in monocytic cells. Diabetes 2003, 52, 1256-1264.
8. Hu, S., Arellano, M., Boontheung, P., Wang, J. et al., Salivary proteomics for oral cancer biomarker discovery. Clin. Cancer Res. 2008, 14, 6246-6252.
9. Rifai, N., Gillette, M. A., Carr, S. A., Protein biomarker discovery and validation: the long and uncertain path to clinical utility. Nat. Biotechnol. 2006, 24, 971-983.
10. Karagiannis, G. S., Pavlou, M. P., Diamandis, E. P., Cancer secretomics reveal pathophysiological pathways in cancer molecular oncology. Mol. Oncol. 2010, 4, 496-510.
11. Kristensen, D. B., Brond, J. C., Nielsen, P. A., Andersen, J. R. et al., Experimental Peptide Identification Repository (EPIR): an integrated peptide-centric platform for validation and mining of tandem mass spectrometry data. Mol. Cell Proteomics 2004, 3, 1023-1038.
12. Gotz, S., Garcia-Gomez, J. M., Terol, J., Williams, T. D. et al., High-throughput functional annotation and data mining with the Blast2GO suite. Nucl. Acids Res. 2008, 36, 3420-3435.
13. Vizcaíno, J. A., Côté, R., Reisinger, F., Foster, J. M. et al., A guide to the Proteomics Identifications Database proteomics data repository. Proteomics 2009, 18, 4276-4283.
14. Maere, S., Heymans, K., Kuiper, M., BiNGO: a cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 2005, 21, 3448-3449.
15. Shannon, P., Markiel, A., Ozier, O., Baliga, NS. et al., Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003, 13, 2498-2504.
16. Petersen, T. N., Brunak, S., von Heijne, G., Nielsen, H., SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat. Met. 2011, 8, 785-786.
17. Bendtsen, J. D., Jensen, L. J., Blom, N., von Heijne, G. et al., Feature based prediction of non-classical and leaderless protein secretion. Protein Eng. Des. Sel. 2004, 17, 349-356.
18. Ralhan, R., Masui, O., Desouza, L. V., Matta, A. et al., Identification of proteins secreted by head and neck cancer cell lines using LC-MS/MS: strategy for discovery of candidate serological biomarkers. Proteomics 2011, 11, 2363-2376.
19. Baynes, J. W., Role of oxidative stress in development of complications in diabetes. Diabetes 1991, 40, 405-412.
20. Giugliano, D., Ceriello, A., Paolisso, G., Oxidative stress and diabetic vascular complications. Diabetes Care 1996, 19, 257-267.
21. Brownlee, M., Cerami, A., Vlassara, H., Advanced glycosylation endproducts in tissue and the biochemical basis of diabetic complications. N. Engl. J. Med. 1988, 318, 1315-1321.
22. Schmidt, A. M., Hori, O., Brett, J., Yan, S. D., Cellular receptors for advanced glycosylation end products: implication for induction of oxidant stress and cellular dysfunction in the pathogenesis of vascular lesions. Arterioscler. Throm. 1994, 14, 1521-1528.
23. Hotta, N., New approaches for treatment in diabetes: aldose reductase inhibitors. Biomed. Pharmacother. 1995, 49, 232-243.
24. Ido, Y., Kilo, C., Williamson, J. R., Cytosolic NADH/NAD, free radicals, and vascular dysfunction in early diabetes mellitus. Diabetologia 1997, 40, S115-S117.
25. Baynes, J. W., Thorpe, S. R., Role of oxidative stress in diabetic complications: a new perspective on an old paradigm. Diabetes 1999, 48, 1-9.
26. Gerrity, R. G., Transition of blood borne monocytes into foam cells in fatty lesions. Am. J. Pathol. 1981, 103, 181-190.
27. Tsao, P. S., Niebauer, J., Buitrago, R., Lin, P. S. et al., Interaction of diabetes and hypertension on determinants of endothelial adhesiveness. Arterioscler. Thromb. Vasc. Biol. 1998, 18, 947-953.
28. Kunt, T., Forst, T., Fruh, B., Flohr, T. et al., Binding of monocytes from normolipidemic hyperglycemic patients with type 1 diabetes to endothelial cells is increased in vitro. Exp. Clin. Endocrinol. Diabetes 1999, 107, 52-256.
29. Hryniewicz-Jankowska, A., Choudhary, P. K., Goodman, S. R., Variation in the monocyte proteome. Exp. Biol. Med. 2007, 232, 967-976.
30. Lawlor, K., Nazarian, A., Lacomis, L., Tempst, P. et al., Pathway-based biomarker search by high-throughput proteomics profiling of secretomes. J. Proteome Res. 2009, 8, 1489-1503.
31. Totary-Jain, H., Naveh-Many, T., Riahi, Y., Kaiser, N. et al., Calreticulin destabilizes glucose transporter-1 mRNA in vascular endothelial and smooth muscle cells under high-glucose conditions. Circ. Res. 2005, 97, 1001-1008.
32. Coppolino, M. G., Dedhar, S., Calreticulin. Int. J. Biochem. Cell Biol. 1998, 30, 553-558.
33. Burns, K., Duggan, B., Atkinson, E. A., Famulski, K. S. et al., Modulation of gene expression by calreticulin binding to the glucocorticoid receptor. Nature 1994, 367, 476-480.
34. Michalak, M., Corbett, E. F., Mesaeli, N., Nakamura, K. et al., Calreticulin:one protein, one gene, many functions. Biochem. J. 1999, 344, 281-292.
35. Hink, U., Li, H., Mollnau, H., Oelze, M. et al., Mechanisms underlying endothelial dysfunction in diabetes mellitus. Circ. Res. 2001, 88, e14-e22.
36. Healy, A. M., Pickard, M. D., Pradhan, A. D., Wang, Y. et al., Platelet expression profiling and clinical validation of myeloid-related protein-14 as a novel determinant of cardiovascular events. Circulation 2006, 113, 2278-2284.
37. Vogl, T., Tenbrock, K., Ludwig, S., Leukert, N. et al., Mrp8 and Mrp14 are endogenous activators of Toll-like receptor 4, promoting lethal, endotoxin-induced shock. Nat. Med. 2007, 13, 1042-1049.
38. Boyd, J. H., Kan, B., Roberts, H., Wang, Y. et al., S100A8 and S100A9 mediate endotoxin- induced cardiomyocyte dysfunction via the receptor for advanced glycation end products. Circ. Res. 2008, 102, 1239-1246.
39. Hobbs, J. A., May, R., Tanousis, K., McNeill, E. et al., Myeloid cell function in MRP-14 (S100A9) null mice. Mol. Cell Biol. 2003, 23, 2564-2576.
40. Vogl, T., Ludwig, S., Goebeler, M., Strey, A. et al., MRP8 and MRP14 control microtubule reorganization during transendothelial migration of phagocytes. Blood 2004, 104(13), 4260-4268.
41. Bouma, G., Lam-Tse, W. K., Wierenga-Wolf, A. F., Drexhage, H. A. et al., Increased serum levels of MRP-8/14 in type 1 diabetes induce an increased expression of CD11b and an enhanced adhesion of circulating monocytes to fibronectin. Diabetes 2004, 53, 1979-1986.
42. Nijtmans, L. G., de Jong, L., Artal, S. M., Coates, P. J. et al., Prohibitins act as a membrane-bound chaperone for the stabilization of mitochondrial proteins. EMBO J. 2000, 19, 2444-2451.
43. Coates, P. J., Jamieson, D. J., Smart, K., Prescott, A. R. et al., The prohibitin family of mitochondrial proteins regulate replicative lifespan. Curr. Biol. 1997, 7, 607-610.
44. Back, J. W., Sanz, M. A., De Jong, L., De Koning, L. J. et al., A structure for the yeast prohibitin complex: Structure prediction and evidence from chemical crosslinking and mass spectrometry. Protein Sci. 2002, 11, 2471-2478.
45. Lott, J. A., Landesman, P. W., The enzymology of skeletal muscle disorders. Crit. Rev. Clin. Lab. Sci. 1984, 20, 153-190.
46. Nozaki, K., Pestronk, A., High aldolase with normal creatine kinase in serum predicts a myopathy with perimysial pathology. J. Neurol. Neurosurg. Psychiat. 2009, 80, 904-909.
47. Jose, J., Zamorano-León J. J., Modrego, J., Mateos-Cáceres, P. J. et al., A Proteomic approach to determine changes in proteins involved in the myocardial metabolism in left ventricles of spontaneously hypertensive rats. Cell Physiol. Biochem. 2010, 25, 347-358.
48. Sherry, B., Yarlett, N., Strupp, A., Cerami, A., Identification of cyclophilin as a proinflammatory secretory product of lipopolysaccharide-activated macrophages. Proc. Natl. Acad. Sci. USA 1992, 89, 3511-3515.
49. Xu, Q., Leiva, M. C., Fischkoff, S. A., Handschumacher, R. E. et al., Leukocyte chemotactic activity of cyclophilin. J. Biol. Chem. 1992, 267, 11968-11971.
50. Allain, F., Vanpouille, C., Carpentier, M., Slomianny, M. C. et al., Interaction with glycosaminoglycans is required for cyclophilin B to trigger integrin-mediated adhesion of peripheral blood T lymphocytes to extracellular matrix. Proc. Natl. Acad. Sci. USA 2002, 26, 2714-2719.
51. Suzuki, J., Jin, Z. G., Meoli, D. F., Matoba, T. et al., Cyclophilin A is secreted by a vesicular pathway in vascular smooth muscle cells. Circ. Res. 2006, 98, 811-817.
52. Billich, A., Winkler, G., Aschauer, H., Rot, A. et al., Presence of cyclophilin A in synovial fluids of patients with rheumatoid arthritis. J. Exp. Med. 1997, 185, 975-980.
53. Jin, Z. G., Lungu, A. O., Xie, L., Wang, M. et al., Cyclophilin A is a proinflammatory cytokine that activates endothelial cells. Arterioscler. Thromb. Vasc. Biol. 2004, 24, 1186-1191.
54. Nigro, P., Satoh, K., O'Dell, M. R., Soe, N. N. et al., Cyclophilin A is an inflammatory mediator that promotes atherosclerosis in apolipoprotein E-deficient mice. Exp. Med. 2011, 208, 53-66.
55. Yuan, W., Ge, H., He, B., Pro-inflammatory activities induced by CyPA-EMMPRIN interaction in monocytes. Atherosclerosis 2010, 213, 415-421.
56. Satoh, K., Nigro, P., Berk, B. C., Oxidative stress and vascular smooth muscle cell growth: a mechanistic linkage by cyclophilin A. Antioxid. Redox. Signal. 2010, 12, 675-682.