Identification of neutrophil gelatinase-associated lipocalin (NGAL) as a discriminatory marker of the hepatocyte-secreted protein response to IL-1β: A proteomic analysis

Biotechnology and Bioengineering

Volumn 91, Issue 4, 2005, Pages 502-515

  Jayaraman, Arul ^a,b,d   Roberts, Kristina A ^a,b   Yoon, Jeongah ^c   Yarmush, David M ^a,b   Duan, Xunbao ^a,b   Lee, Kyongbum ^c   Yarmush, Martin L ^a,b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c Tufts University   (United States)

^d Texas AandM University   (United States)

Author keywords

Hepatocytes, cytokines; NGAL; Proteomics; Secreted proteins

Indexed keywords

BIOLOGICAL ORGANS; ELECTROPHORESIS; IMMUNOLOGY; MULTIVARIABLE CONTROL SYSTEMS;

ACUTE PHASE RESPONSE (APR); INFLAMMATORY CYTOKINES; MULTIDIMENSIONAL SCALING (MDS); NEUTROPHIL GELATINASE-ASSOCIATED LIPOCALIN (NGAL);

PROTEINS;

CYTOKINE; INTERLEUKIN 1BETA; INTERLEUKIN 6; LIPOCALIN; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; UNCLASSIFIED DRUG;

ACUTE PHASE RESPONSE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; HEPATITIS; IMAGE ANALYSIS; LIVER CELL; LIVER INJURY; MALE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN SECRETION; PROTEIN SYNTHESIS; PROTEOMICS; RAT; STATISTICAL ANALYSIS; TWO DIMENSIONAL GEL ELECTROPHORESIS;

ACUTE-PHASE PROTEINS; AMINO ACID SEQUENCE; ANIMALS; BIOLOGICAL MARKERS; BLOOD PROTEINS; BLOTTING, WESTERN; DOSE-RESPONSE RELATIONSHIP, IMMUNOLOGIC; HEPATOCYTES; HUMANS; INTERLEUKIN-1; INTERLEUKIN-6; MALE; MOLECULAR SEQUENCE DATA; MULTIVARIATE ANALYSIS; PROTEOMICS; PROTO-ONCOGENE PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 23244465337     PISSN: 00063592     EISSN: None     Source Type: Journal    
DOI: 10.1002/bit.20535     Document Type: Article

References (59)

1. Ballmer PE, McNurlan MA, Grant I, Garlick PJ. 1995. Down-regulation of albumin synthesis in the rat by human recombinant interleukin-1b or turpentine in response to nutrients. JPEN 19:266-270.
2. Baue AE, Durham R, Faist E. 1998. Systemic inflammatory response syndrome (SIRS), multiple organ dysfunction syndrome (MODS), multiple organ failure (MOF): Are we winning the battle? Shock 10(2):79-89.
3. Baumann H, Gauldie J. 1994. The acute phase response. Immunol Today 15(2):74-80.
4. Baumann H, Prowse KR, Marinkovic S, Won KA, Jahreis GP. 1989. Stimulation of hepatic acute phase response by cytokines and glucocorticoids. Ann N Y Acad Sci 557:280-295, discussion 295-296.
5. Baumann H, Richards C, Gauldie J. 1987. Interaction among hepatocyte stimulating factors, interleulin 1, and glucocorticoids for regulation of acute phase plasma proteins in human hepatoma (HepG2) cells. J Immunol 139:4122-4128.
6. Bini L, Magi B, Marzocchi B, Cellesi C, Berti B, Raggiaschi R, Rossolini A, Pallini V. 1996. Two-dimensional electrophoretic patterns of acute-phase human serum in the course of bacterial and viral diseases. Electrophoresis 17:612-616.
7. Breiman L, Friedman JH. 1985. Estimating optimal transformations for multiple-regression and correlation. J Amer Stat Assoc 80:580-598.
8. Cannon JG, Friedberg JS, Gelfand JA, Tompkins RG, Burke JF, Dinarello CA. 1992. Circulating interleukin-1 beta and tumor necrosis factor-alpha concentrations after burn injury in humans. Crit Care Med 20(10): 1414-1419.
9. Cisowski J, Zarebski A, Koj A. 2002. IL-1-mediated inhibition of IL-6-induced STAT3 activation is modulated by IL-4, MAP kinase inhibitors and redox state of HepG2 cells. Folia Histochem Cytobiol 40:341-345.
10. Cooney RN, Yumet G. 2002. Cytokine signaling in sepsis: Redundancy, crosstalk, and regulatory mechanisms. Crit Care Med 30:262-263.
11. Cowland JB, Sorensen OE, Sehested M, Borregaard N. 2003. Neutrophil gelatinase-associated lipocalin is up-regulated in human epithelial cells by IL-1 beta, but not by TNF-alpha. J Immunol 171:6630-6639.
12. de Beaux AC, Goldie AS, Ross JA, Carter DC, Fearon KC. 1996. Serum concentrations of inflammatory mediators related to organ failure in patients with acute pancreatitis. Br J Surg 83(3):349-353.
13. Devireddy LR, Teodoro JG, Richard FA, Green MR. 2001. Induction of apoptosis by a secreted lipocalin that is transcriptionally regulated by IL-3 deprivation. Science 293:829-834.
14. Dillon WR, Goldstein M. 1984. Multivariate analysis: methods and applications. New York: Wiley.
15. Duan X, Yarmush DM, Berthiaume F, Jayaraman A, Yarmush ML. 2004a. A mouse serum two-dimensional gel map: Application to profiling burn injury and infection. Electrophoresis 25:3055-3065.
16. Duan X, Yarmush DM, Jayaraman A, Yarmush ML. 2004b. Dispensable role for interferon gamma in the burn-induced acute-phase response: A proteomic analysis. Proteomics 4:1830-1839.
17. Duan X, Yarmush DM, Berthiaume F, Jayaraman A, Yarmush ML. 2005. Evaluation of immunoprecipitation-based depletion of albumin for two-dimensional gel separation of normal and inflamed mouse plasma. Proteomics, in press.
18. Dunn JC, Tompkins RG, Yarmush ML. 1991. Long-term in vitro function of adult hepatocytes in a collagen sandwich configuration. Biotechnol Prog 7(3):237-245.
19. Dunn JC, Yarmush ML, Koebe HG, Tompkins RG. 1989. Hepatocyte function and extracellular matrix geometry: Long-term culture in a sandwich configuration. Faseb J 3(2):174-177.
20. Fadeel B. 2003. Programmed cell clearance. Cell Mol Life Sci 60:2575-2585.
21. Fey GH, Gauldie J. 1990. The acute phase response of the liver in inflammation. Prog Liver Dis 9:89-116.
22. Flower DR. 1994. The lipocalin protein family: A role in cell regulation. FEBS Lett 354:7-11.
23. Fouad FM, Mamer OA, Shahidi F. 1996. Biogenesis of hepatic acute-phase response to trauma. Med Hypotheses 47:157-177.
24. Friedman JH. 1984. A variable span smoother. Laboratory for Computational Statistics, Department of Statistics, Stanford University.
25. Gabay C, Kushner I. 1999. Acute-phase proteins and other systemic responses to inflammation. N Engl J Med 340(6):448-454.
26. Geiger T, Andus T, Klapproth J, Hirano T, Kishimoto T, Heinrich PC. 1988. Induction of rat acute-phase proteins by interleukin 6 in vivo. Eur J Immunol 18(5):717-721.
27. Gombart AF, Kwok SH, Anderson KL, Yamaguchi Y, Torbett BE, Koeffler HP. 2003. Regulation of neutrophil and eosinophil secondary granule gene expression by transcription factors C/EBP epsilon and PU.1. Blood 101:3265-3273.
28. Hack CE, De Groot ER, Felt-Bersma RJ, Nuijens JH, Strack Van Schijndel RJ, Eerenberg-Belmer AJ, Thijs LG, Aarden LA. 1989. Increased plasma levels of interleukin-6 in sepsis. Blood 74(5):1704-1710.
29. Herbomel P, Rollier A, Tronche F, Ott MO, Yaniv M, Weiss MC. 1989. The rat albumin promoter is composed of six distinct positive elements within 130 nucleotides. Mol Cell Biol 9:4750-4758.
30. Jayaraman A, Yarmush ML, Roth CM. 2000. Dynamics of gene expression in rat hepatocytes under stress. Metabolic Eng 2:1-13.
31. Kamezaki K, Shimoda K, Numata A, Aoki K, Kato K, Takase K, Nakajima H, Ihara K, Haro T, Ishikawa F. 2003. The lipocalin 24p3, which is an essential molecule in IL-3 withdrawal-induced apoptosis, is not involved in the G-CSF withdrawal-induced apoptosis. Eur J Haematol 71:412-417.
32. Kang YH, Berthiaume F, Yarmush ML. 2002. Long-term stable cultures of rat hepatocytes: An in vitro model to study acute and chronic hepatic inflammation. Tissue Eng 8:681-693.
33. Kennedy S. 2001. Proteomic profiling from human samples: The body fluid alternative. Toxicol Lett 120:379-384.
34. Kruskal JB. 1964. Multidimensional-scaling by optimizing goodness of fit to a nonmetric hypothesis. Psychometrika 29:1-27.
35. Kushner I. 1990. C-reactive protein and the acute-phase response. Hosp Pract (Off Ed) 25:13, 16, 21-28.
36. Lee K, Hwang D, Yokoyama T, Stephanopoulos G, Stephanopoulos GN, Yarmush ML. 2004. Identification of optimal classification functions for biological sample and state discrimination from metabolic profiling data. Bioinformatics 20:959-969.
37. Liu Q, Ryon J, Nilsen-Hamilton M. 1997. Uterocalin: A mouse acute phase protein expressed in the uterus around birth. Mol Reprod Dev 46:507-514.
38. Meheus LA, Fransen LM, Raymackers JG, Blockx HA, Van Beeumen JJ, Van Bun SM, Van de Voorde A. 1993. Identification by microsequencing of lipopolysaccharide-induced proteins secreted by mouse macrophages. J Immunol 151:1535-1547.
39. Miller I, Haynes P, Eberini I, Gemeiner M, Aebersold R, Gianazza E. 1999. Proteins of rat serum: III. Gender-related differences in protein concentration under baseline conditions and upon experimental inflammation as evaluated by two-dimensional electrophoresis. Electrophoresis 20:836-845.
40. Milosavljevic T, Lazic T, Uskokovic A, Petrovic M, Grigorov I. 2003. Expression of the rat liver haptoglobin gene is mediated by isoforms of C/EBPalpha, -beta and -delta proteins. Gen Physiol Biophys 22:181-190.
41. Moshage H. 1997. Cytokines and the hepatic acute phase response. J Pathol 181:257-266.
42. Nicola NA. 1994. Cytokine pleiotropy and redundancy: A view from the receptor. Stem cells 1:3-12.
43. Nilsen-Hamilton M, Liu Q, Ryon J, Bendickson L, Lepont P, Chang Q. 2003. Tissue involution and the acute phase response. Ann N Y Acad Sci 995:94-108.
44. Nishiura T, Nishimura T, deSerres S, Godfrey V, Bradham CA, Nakagawa T, Brenner DA, Meyer AA. 2000. Gene expression and cytokine and enzyme activation in the liver after a burn injury. J Burn Care Rehab 21:135-141.
45. Pajovic S, Jones VE, Prowse KR, Berger FG, Baumann H. 1994. Species-specific changes in regulatory elements of mouse haptoglobin genes. J Biol Chem 269:2215-2224.
46. Peng J, Gygi SP. 2001. Proteomics: The move to mixtures. J Mass Spectrom 36:1083-1091.
47. Pinilla JC, Hayes P, Laverty W, Arnold C, Laxdal V. 1998. The C-reactive protein to prealbumin ratio correlates with the severity of multiple organ dysfunction. Surgery 124(4):799-806.
48. Poli V, Ciliberto G. 1994. Transcriptional regulation of acute phase genes by IL-6 and related cytokines. In: Tronche F, Yaniv M, editors. Liver gene expression. New York: R. G. Landes Company, pp 131-151.
49. Prudhomme W, Daley GQ, Zandstra P, Lauffenburger DA. 2004. Multivariate proteomic analysis of murine embryonic stem cell self-renewal versus differentiation signaling. Proc Natl Acad Sci USA 101:2900-2905.
50. Rodriguez JL, Miller CG, Garner WL, Till GO, Guerrero P, Moore NP, Corridore M, Normolle DP, Smith DJ, Remick DG. 1993. Correlation of the local and systemic cytokine response with clinical outcome following thermal injury. J Trauma 34(5):684-694; discussion 694-695.
51. Roth CM, Kohen RL, Walton SP, Yarmush ML. 2001. Coupling of inflammatory cytokine signaling pathways probed by measurements of extracellular acidification rate. Biophys Chem 89:1-12.
52. Shevchenko A, Wilm M, Vorm O, Mann M. 1996. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 68:850-858.
53. Suire S, Stewart F, Beauchamp J, Kennedy MW. 2001. Uterocalin, a lipocalin provisioning the preattachment equine conceptus: Fatty acid and retinol binding properties, and structural characterization. Biochem J 356:369-376.
54. Takane Y, Young FW, Deleeuw J. 1977. Nonmetric individual-differences multidimensional-scaling-alternating least-squares method with optimal scaling features. Psychometrika 42:7-67.
55. Vemula M, Berthiaume F, Jayaraman A, Yarmush ML. 2004. Expression profiling analysis of the metabolic and inflammatory changes following burn injury in rats. Physiol Genomics 18:87-98.
56. Vorachek WR, Steppan CM, Lima M, Black H, Bhattacharya R, Wen P, Kajiyama Y, Locker J. 2000. Distant enhancers stimulate the albumin promoter through complex proximal binding sites. J Biol Chem 275: 29031-29041.
57. Xia C, Cheshire JK, Patel H, Woo P. 1997. Cross-talk between transcription factors NF-kappa B and C/EBP in the transcriptional regulation of genes. Int J Biochem Cell Biol 29(12): 1525-1539.
58. Xia Z-F, Coolbaugh MI, He F, Herndon DN, Papaconstantinou J. 1992. The effects of burn injury on the acute phase response. J Trauma 32:245-251.
59. Yarmush ML, Jayaraman A. 2002. Advances in proteomic technologies. Annu Rev Biomed Eng 4:349-373.