Phagocyte-specific calcium-binding S100 proteins as clinical laboratory markers of inflammation

Clinica Chimica Acta

Volumn 344, Issue 1-2, 2004, Pages 37-51

  Foell, Dirk ^a   Frosch, Michael ^a   Sorg, Clemens ^a   Roth, Johannes ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

Calgranulins; Calprotectin; Inflammation; MRP; Phagocytes; RAGE; S100

Indexed keywords

ANTIBIOTIC AGENT; BIOLOGICAL MARKER; CALCIUM BINDING PROTEIN; IMMUNOGLOBULIN; METHOTREXATE; NONSTEROID ANTIINFLAMMATORY AGENT; PROTEIN S 100; PROTEIN S100 A12; PROTEIN S100 A8; PROTEIN S100 A9; STEROID; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ACUTE DISEASE; AUTOIMMUNE DISEASE; BACTERIAL INFECTION; CELL ACTIVATION; CHRONIC BRONCHITIS; CHRONIC DISEASE; CHRONIC LUNG DISEASE; CORRELATION ANALYSIS; CYSTIC FIBROSIS; DISEASE ACTIVITY; ENTERITIS; FECES; GASTROINTESTINAL SYMPTOM; HUMAN; IMMUNE SYSTEM; INFLAMMATION; NONHUMAN; PHAGOCYTE; PLASMA; PNEUMONIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN SECRETION; REVIEW; RHEUMATOID ARTHRITIS; SPUTUM; SYNOVIAL FLUID;

BIOLOGICAL MARKERS; CLINICAL CHEMISTRY TESTS; CLINICAL LABORATORY TECHNIQUES; HUMANS; INFLAMMATION; PHAGOCYTES; S100 PROTEINS;

EID: 2442443134     PISSN: 00098981     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cccn.2004.02.023     Document Type: Review

References (146)

1. Heizmann C.W. Calcium-binding proteins: basic concepts and clinical implications. Gen. Physiol. Biophys. 11:1992;411-425
2. Lagasse E., Clerc R.G. Cloning and expression of two human genes encoding calcium-binding proteins that are regulated during myeloid differentiation. Mol. Cell. Biol. 8:1988;2402-2410
3. Odink K., Cerletti N., Bruggen J., Clerc R.G., Tarcsay L., Zwadlo G., et al. Two calcium-binding proteins in infiltrate macrophages of rheumatoid arthritis. Nature. 330:1987;80-82
4. Zwadlo G., Bruggen J., Gerhards G., Schlegel R., Sorg C. Two calcium-binding proteins associated with specific stages of myeloid cell differentiation are expressed by subsets of macrophages in inflammatory tissues. Clin. Exp. Immunol. 72:1988;510-515
5. Dorin J.R., Novak M., Hill R.E., Brock D.J., Secher D.S., van Heyningen V. A clue to the basic defect in cystic fibrosis from cloning the CF antigen gene. Nature. 326:1987;614-617
6. Hofmann M.A., Drury S., Fu C., Qu W., Taguchi A., Lu Y., et al. RAGE mediates a novel proinflammatory axis: a central cell surface receptor for S100/calgranulin polypeptides. Cell. 97:1999;889-901
7. Srikrishna G., Panneerselvam K., Westphal V., Abraham V., Varki A., Freeze H.H. Two proteins modulating transendothelial migration of leukocytes recognize novel carboxylated glycans on endothelial cells. J. Immunol. 166:2001;4678-4688
8. Sander J., Fagerhol M.K., Bakken J.S., Dale I. Plasma levels of the leucocyte L1 protein in febrile conditions: relation to aetiology, number of leucocytes in blood, blood sedimentation reaction and C-reactive protein. Scand. J. Clin. Lab. Invest. 44:1984;357-362
9. Stockley R.A., Dale I., Hill S.L., Fagerhol M.K. Relationship of neutrophil cytoplasmic protein (L1) to acute and chronic lung disease. Scand. J. Clin. Lab. Invest. 44:1984;629-634
10. Moore B.W. A soluble protein characteristic of the nervous system. Biochem. Biophys. Res. Commun. 19:1965;739-744
11. Isobe T., Okuyama T. The amino-acid sequence of S-100 protein (PAP I-b protein) and its relation to the calcium-binding proteins. Eur. J. Biochem. 89:1978;379-388
12. Moroz O.V., Antson A.A., Grist S.J., Maitland N.J., Dodson G.G., Wilson K.S., et al. Structure of the human S100A12-copper complex: implications for host-parasite defence. Acta Crystallogr., D Biol. Crystallogr. 59:2003;859-867
13. 2+ binding on S100b protein. J. Biol. Chem. 261:1986;8192-8203
14. 2+ to human nuclear S100A2 and mutant proteins. J. Biol. Chem. 273:1998;18826-18834
15. Gottsch J.D., Eisinger S.W., Liu S.H., Scott A.L. Calgranulin C has filariacidal and filariastatic activity. Infect. Immun. 67:1999;6631-6636
16. Marenholz I., Heizmann C.W. S100A16, a ubiquitously expressed EF-hand protein which is up-regulated in tumors. Biochem. Biophys. Res. Commun. 313:2004;237-244
17. Wolf R., Mirmohammadsadegh A., Walz M., Lysa B., Tartler U., Remus R., et al. Molecular cloning and characterization of alternatively spliced mRNA isoforms from psoriatic skin encoding a novel member of the S100 family. FASEB J. 17:2003;1969-1971
18. Heizmann C.W., Fritz G., Schafer B.W. S100 proteins: structure, functions and pathology. Front. Biosci. 7:2002;d1356-d1368
19. Allore R., O'Hanlon D., Price R., Neilson K., Willard H.F., Cox D.R., et al. Gene encoding the beta subunit of S100 protein is on chromosome 21: implications for down syndrome. Science. 239:1988;1311-1313
20. Moroz O.V., Antson A.A., Dodson E.J., Burrell H.J., Grist S.J., Lloyd R.M., et al. The structure of S100A12 in a hexameric form and its proposed role in receptor signalling. Acta Crystallogr., D Biol. Crystallogr. 58:2002;407-413
21. Propper C., Huang X., Roth J., Sorg C., Nacken W. Analysis of the MRP8-MRP14 protein-protein interaction by the two-hybrid system suggests a prominent role of the C-terminal domain of S100 proteins in dimer formation. J. Biol. Chem. 274:1999;183-188
22. Strupat K., Rogniaux H., Van Dorsselaer A., Roth J., Vogl T. Calcium-induced noncovalently linked tetramers of MRP8 and MRP14 are confirmed by electrospray ionization-mass analysis. J. Am. Soc. Mass. Spectrom. 11:2000;780-788
23. Vogl T., Propper C., Hartmann M., Strey A., Strupat K., van den Bos C., et al. S100A12 is expressed exclusively by granulocytes and acts independently from MRP8 and MRP14. J. Biol. Chem. 274:1999;25291-25296
24. Arumugam T., Simeone D.M., Schmidt A.M., Logsdon C.D. S100P stimulates cell proliferation and survival via receptor for activated glycation end products (RAGE). J. Biol. Chem. 4(279):2003;5059-5065
25. Mikkelsen S.E., Novitskaya V., Kriajevska M., Berezin V., Bock E., Norrild B., et al. S100A12 protein is a strong inducer of neurite outgrowth from primary hippocampal neurons. J. Neurochem. 79:2001;767-776
26. Baudier J., Mochly-Rosen D., Newton A., Lee S.H., Koshland D.E. Jr., Cole R.D. Comparison of S100b protein with calmodulin: interactions with melittin and microtubule-associated tau proteins and inhibition of phosphorylation of tau proteins by protein kinase C. Biochemistry. 26:1987;2886-2893
27. Sorci G., Agneletti A.L., Bianchi R., Donato R. Association of S100B with intermediate filaments and microtubules in glial cells. Biochim. Biophys. Acta. 1448:1998;277-289
28. Adami C., Sorci G., Blasi E., Agneletti A.L., Bistoni F., Donato R. S100B expression in and effects on microglia. Glia. 33:2001;131-142
29. McAdory B.S., Van Eldik L.J., Norden J.J. S100B, a neurotropic protein that modulates neuronal protein phosphorylation, is upregulated during lesion-induced collateral sprouting and reactive synaptogenesis. Brain Res. 813:1998;211-217
30. Michetti F., Massaro A., Murazio M. The nervous system-specific S-100 antigen in cerebrospinal fluid of multiple sclerosis patients. Neurosci. Lett. 11:1979;171-175
31. Gazzolo D., Marinoni E., Di Iorio R., Bruschettini M., Kornacka M., Lituania M., et al. Measurement of urinary S100B protein concentrations for the early identification of brain damage in asphyxiated full-term infants. Arch. Pediatr. Adolesc. Med. 157:2003;1163-1168
32. Kleine T.O., Benes L., Zofel P. Studies of the brain specificity of S100B and neuron-specific enolase (NSE) in blood serum of acute care patients. Brain Res. Bull. 61:2003;265-279
33. Connolly E.S. Jr., Winfree C.J., Rampersad A., Sharma R., Mack W.J., Mocco J., et al. Serum S100B protein levels are correlated with subclinical neurocognitive declines after carotid endarterectomy. Neurosurgery. 49:2001;1076-1082
34. Li Y., Barger S.W., Liu L., Mrak R.E., Griffin W.S. S100beta induction of the proinflammatory cytokine interleukin-6 in neurons. J. Neurochem. 74:2000;143-150
35. Yan S.S., Wu Z.Y., Zhang H.P., Furtado G., Chen X., Yan S.F., et al. Suppression of experimental autoimmune encephalomyelitis by selective blockade of encephalitogenic T-cell infiltration of the central nervous system. Nat. Med. 9:2003;287-293
36. Michetti F., Gazzolo D. S100B testing in pregnancy. Clin. Chim. Acta. 335:2003;1-7
37. Bertsch T., Casarin W., Kretschmar M., Zimmer W., Walter S., Sommer C., et al. Protein S-100B: a serum marker for ischemic and infectious injury of cerebral tissue. Clin. Chem. Lab. Med. 39:2001;319-323
38. Regner A., Bianchini O., Jardim C., Menna-Barreto M. HTLV-I-associated myelopathy: are ferritin, S100beta protein, or guanine nucleotides CSF markers of disease? J. Neurovirol. 8:2002;64-67
39. Komada T., Araki R., Nakatani K., Yada I., Naka M., Tanaka T. Novel specific chemtactic receptor for S100L protein on guinea pig eosinophils. Biochem. Biophys. Res. Commun. 220:1996;871-874
40. Jinquan T., Vorum H., Larsen C.G., Madsen P., Rasmussen H.H., Gesser B., et al. Psoriasin: a novel chemotactic protein. J. Invest. Dermatol. 107:1996;5-10
41. Andersson K.B., Sletten K., Berntzen H.B., Dale I., Brandtzaeg P., Jellum E., et al. The leucocyte L1 protein: identity with the cystic fibrosis antigen and the calcium-binding MRP-8 and MRP-14 macrophage components. Scand. J. Immunol. 28:1988;241-245
42. Fagerhol M.K. Calprotectin, a faecal marker of organic gastrointestinal abnormality. Lancet. 356:2000;1783-1784
43. Steinbakk M., Naess-Andresen C.F., Lingaas E., Dale I., Brandtzaeg P., Fagerhol M.K. Antimicrobial actions of calcium binding leucocyte L1 protein, calprotectin. Lancet. 336:1990;763-765
44. Dale I., Fagerhol M.K., Naesgaard I. Purification and partial characterization of a highly immunogenic human leukocyte protein, the L1 antigen. Eur. J. Biochem. 134:1983;1-6
45. Edgeworth J., Gorman M., Bennett R., Freemont P., Hogg N. Identification of p8, 14 as a highly abundant heterodimeric calcium binding protein complex of myeloid cells. J. Biol. Chem. 266:1991;7706-7713
46. Roth J., Goebeler M., van den Bos C., Sorg C. Expression of calcium-binding proteins MRP8 and MRP14 is associated with distinct monocytic differentiation pathways in HL-60 cells. Biochem. Biophys. Res. Commun. 191:1993;565-570
47. Brandtzaeg P., Dale I., Fagerhol M.K. Distribution of a formalin-resistant myelomonocytic antigen (L1) in human tissues: II. Normal and aberrant occurrence in various epithelia. Am. J. Clin. Pathol. 87:1987;700-707
48. Hsieh H.L., Schafer B.W., Sasaki N., Heizmann C.W. Expression analysis of S100 proteins and RAGE in human tumors using tissue microarrays. Biochem. Biophys. Res. Commun. 307:2003;375-381
49. Frosch M., Vogl T., Waldherr R., Sorg C., Sunderkotter C., Roth J. Expression of MRP8 and MRP14 by macrophages is a marker for severe forms of glomerulonephritis. J. Leukoc. Biol. 75:2004;198-206
50. Goebeler M., Roth J., Burwinkel F., Vollmer E., Bocker W., Sorg C. Expression and complex formation of S100-like proteins MRP8 and MRP14 by macrophages during renal allograft rejection. Transplantation. 58:1994;355-361
51. Roth J., Burwinkel F., van den Bos C., Goebeler M., Vollmer E., Sorg C. MRP8 and MRP14, S-100-like proteins associated with myeloid differentiation, are translocated to plasma membrane and intermediate filaments in a calcium-dependent manner. Blood. 82:1993;1875-1883
52. Manitz M.P., Horst B., Seeliger S., Strey A., Skryabin B.V., Gunzer M., et al. Loss of S100A9 (MRP14) results in reduced interleukin-8-induced CD11b surface expression, a polarized microfilament system, and deminished responsiveness to chemoattractants in vitro. Mol. Cell. Biol. 23:2003;1034-1043
53. Doussiere J., Bouzidi F., Vignais P.V. The S100A8/A9 protein as a partner for the cytosolic factors of NADPH oxidase activation in neutrophils. Eur. J. Biochem. 269:2002;3246-3255
54. Kerkhoff C., Klempt M., Kaever V., Sorg C. The two calcium-binding proteins, S100A8 and S100A9, are involved in the metabolism of arachidonic acid in human neutrophils. J. Biol. Chem. 274:1999;32672-32679
55. Rammes A., Roth J., Goebeler M., Klempt M., Hartmann M., Sorg C. Myeloid-related protein (MRP) 8 and MRP14, calcium-binding proteins of the S100 family, are secreted by activated monocytes via a novel, tubulin-dependent pathway. J. Biol. Chem. 272:1997;9496-9502
56. Frosch M., Strey A., Vogl T., Wulffraat N.M., Kuis W., Sunderkotter C., et al. Myeloid-related proteins 8 and 14 are specifically secreted during interaction of phagocytes and activated endothelium and are useful markers for monitoring disease activity in pauciarticular-onset juvenile rheumatoid arthritis. Arthritis Rheum. 43:2000;628-637
57. Hitomi J., Yamaguchi K., Kikuchi Y., Kimura T., Maruyama K., Nagasaki K. A novel calcium-binding protein in amniotic fluid, CAAF1: its molecular cloning and tissue distribution. J. Cell Sci. 109:1996;805-815
58. Ilg E.C., Troxler H., Burgisser D.M., Kuster T., Markert M., Guignard F., et al. Amino acid sequence determination of human S100A12 (P6, calgranulin C, CGRP, CAAF1) by tandem mass spectrometry. Biochem. Biophys. Res. Commun. 225:1996;146-150
59. Wicki R., Marenholz I., Mischke D., Schafer B.W., Heizmann C.W. Characterization of the human S100A12 (calgranulin C, p6, CAAF1, CGRP) gene, a new member of the S100 gene cluster on chromosome 1q21. Cell Calcium. 20:1996;459-464
60. Hasegawa T., Kosaki A., Kimura T., Matsubara H., Mori Y., Okigaki M., et al. The regulation of EN-RAGE (S100A12) gene expression in human THP-1 macrophages. Atherosclerosis. 171:2003;211-218
61. Robinson M.J., Hogg N. A comparison of human S100A12 with MRP-14 (S100A9). Biochem. Biophys. Res. Commun. 275:2000;865-870
62. Yang Z., Tao T., Raftery M.J., Youssef P., Di Girolamo N., Geczy C.L. Proinflammatory properties of the human S100 protein S100A12. J. Leukoc. Biol. 69:2001;986-994
63. Foell D., Kucharzik T., Kraft M., Vogl T., Sorg C., Domschke W., et al. Neutrophil derived human S100A12 (EN-RAGE) is strongly expressed during chronic active inflammatory bowel disease. Gut. 52:2003;847-853
64. Boussac M., Garin J. Calcium-dependent secretion in human neutrophils: a proteomic approach. Electrophoresis. 21:2000;665-672
65. Schmidt A.M., Yan S.D., Yan S.F., Stern D.M. The multiligand receptor RAGE as a progression factor amplifying immune and inflammatory responses. J. Clin. Invest. 108:2001;949-955
66. Robinson M.J., Tessier P., Poulsom R., Hogg N. The S100 family heterodimer, MRP-8/14, binds with high affinity to heparin and heparan sulfate glycosaminoglycans on endothelial cells. J. Biol. Chem. 277:2002;3658-3665
67. Hofmann M.A., Drury S., Hudson B.I., Gleason M.R., Qu W., Lu Y., et al. RAGE and arthritis: the G82S polymorphism amplifies the inflammatory response. Genes Immun. 3:2002;123-135
68. Newton R.A., Hogg N. The human S100 protein MRP-14 is a novel activator of the beta 2 integrin Mac-1 on neutrophils. J. Immunol. 160:1998;1427-1435
69. Eue I., Pietz B., Storck J., Klempt M., Sorg C. Transendothelial migration of 27E10+ human monocytes. Int. Immunol. 12:2000;1593-1604
70. Miranda L.P., Tao T., Jones A., Chernushevich I., Standing K.G., Geczy C.L., et al. Total chemical synthesis and chemotactic activity of human S100A12 (EN-RAGE). FEBS Lett. 488:2001;85-90
71. Sohnle P.G., Hunter M.J., Hahn B., Chazin W.J. Zinc-reversible antimicrobial activity of recombinant calprotectin (migration inhibitory factor-related proteins 8 and 14). J. Infect. Dis. 182:2000;1272-1275
72. Seeliger S., Vogl T., Engels I.H., Schroder J.M., Sorg C., Sunderkotter C., et al. Expression of calcium-binding proteins MRP8 and MRP14 in inflammatory muscle diseases. Am. J. Pathol. 163:2003;947-956
73. Yui S., Nakatani Y., Mikami M. Calprotectin (S100A8/S100A9), an inflammatory protein complex from neutrophils with a broad apoptosis-inducing activity. Biol. Pharm. Bull. 26:2003;753-760
74. Sampson B., Fagerhol M.K., Sunderkotter C., Golden B.E., Richmond P., Klein N., et al. Hyperzincaemia and hypercalprotectinaemia: a new disorder of zinc metabolism. Lancet. 360:2002;1742-1745
75. Strasser F., Gowland P.L., Ruef C. Elevated serum macrophage inhibitory factor-related protein (MRP) 8/14 levels in advanced HIV infection and during disease exacerbation. J. Acquir. Immune Defic. Syndr. Human Retrovirol. 16:1997;230-238
76. Lugering N., Stoll R., Kucharzik T., Burmeister G., Sorg C., Domschke W. Serum 27E10 antigen: a new potential marker for staging HIV disease. Clin. Exp. Immunol. 101:1995;249-253
77. Kleinegger C.L., Stoeckel D.C., Kurago Z.B. A comparison of salivary calprotectin levels in subjects with and without oral candidiasis. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endo. 92:2001;62-67
78. Pechkovsky D.V., Zalutskaya O.M., Ivanov G.I., Misuno N.I. Calprotectin (MRP8/14 protein complex) release during mycobacterial infection in vitro and in vivo. FEMS Immunol. Med. Microbiol. 29:2000;27-33
79. Foell D., Seeliger S., Vogl T., Koch H.G., Maschek H., Harms E., et al. Expression of S100A12 (EN-RAGE) in cystic fibrosis. Thorax. 58:2003;613-617
80. Kane D., Roth J., Frosch M., Vogl T., Bresnihan B., FitzGerald O. Increased perivascular synovial membrane expression of myeloid-related proteins in psoriatic arthritis. Arthritis Rheum. 48:2003;1676-1685
81. Youssef P., Roth J., Frosch M., Costello P., Fitzgerald O., Sorg C., et al. Expression of myeloid related proteins (MRP) 8 and 14 and the MRP8/14 heterodimer in rheumatoid arthritis synovial membrane. J. Rheumatol. 26:1999;2523-2528
82. Berntzen H.B., Olmez U., Fagerhol M.K., Munthe E. The leukocyte protein L1 in plasma and synovial fluid from patients with rheumatoid arthritis and osteoarthritis. Scand. J. Rheumatol. 20:1991;74-82
83. Emery P., Lopez A.F., Burns G.F., Vadas M.A. Synovial fluid neutrophils of patients with rheumatoid arthritis have membrane antigen changes that reflect activation. Ann. Rheum. Dis. 47:1988;34-39
84. Wollheim F.A., Eberhardt K.B. The search for laboratory measures of outcome in rheumatoid arthritis. Bailliere's Clin. Rheumatol. 6:1992;69-93
85. Klimiuk P.A., Sierakowski S., Latosiewicz R., Cylwik J.P., Cylwik B., Skowronski J., et al. Soluble adhesion molecules (ICAM-1, VCAM-1, and E-selectin) and vascular endothelial growth factor (VEGF) in patients with distinct variants of rheumatoid synovitis. Ann. Rheum. Dis. 61:2002;804-809
86. Mangge H., Kenzian H., Gallistl S., Neuwirth G., Liebmann P., Kaulfersch W., et al. Serum cytokines in juvenile rheumatoid arthritis. Correlation with conventional inflammation parameters and clinical subtypes. Arthritis Rheum. 38:1995;211-220
87. Klimiuk P.A., Sierakowski S., Latosiewicz R., Cylwik J.P., Cylwik B., Skowronski J., et al. Circulating tumour necrosis factor alpha and soluble tumour necrosis factor receptors in patients with different patterns of rheumatoid synovitis. Ann. Rheum. Dis. 62:2003;472-475
88. Berntzen H.B., Munthe E., Fagerhol M.K. The major leukocyte protein L1 as an indicator of inflammatory joint disease. Scand. J. Rheumatol. Suppl. 76:1988;251-256
89. Berntzen H.B., Fagerhol M.K., Ostensen M., Mowinckel P., Hoyeraal H.M. The L1 protein as a new indicator of inflammatory activity in patients with juvenile rheumatoid arthritis. J. Rheumatol. 18:1991;133-138
90. Brun J.G., Haga H.J., Boe E., Kallay I., Lekven C., Berntzen H.B., et al. Calprotectin in patients with rheumatoid arthritis: relation to clinical and laboratory variables of disease activity. J. Rheumatol. 19:1992;859-862
91. Brun J.G., Jonsson R., Haga H.J. Measurement of plasma calprotectin as an indicator of arthritis and disease activity in patients with inflammatory rheumatic diseases. J. Rheumatol. 21:1994;733-738
92. Frosch M., Seeliger S., Wulffraat M., Kuis W., Vogl T., Viemann D., et al. Expression of myeloid related proteins 8 and 14 in systemic onset juvenile rheumatoid arthritis. Arthritis Rheum. 48:2003;2622-2626
93. Foell D., Frosch M., Schulze zur Wiesch A., Vogl T., Sorg C., Roth J. Methotrexate treatment in juvenile idiopathic arthritis: when is the right time to stop? Ann. Rheum. Dis. 63:2004;206-208
94. Wulffraat N.M., Haas P.J., Frosch M., De Kleer I.M., Vogl T., Brinkman D.M., et al. Myeloid related protein 8 and 14 secretion reflects phagocyte activation and correlates with disease activity in juvenile idiopathic arthritis treated with autologous stem cell transplantation. Ann. Rheum. Dis. 62:2003;236-241
95. Berntzen H.B., Munthe E., Fagerhol M.K. A longitudinal study of the leukocyte protein L1 as an indicator of disease activity in patients with rheumatoid arthritis. J. Rheumatol. 16:1989;1416-1420
96. Madland T.M., Hordvik M., Haga H.J., Jonsson R., Brun J.G. Leukocyte protein calprotectin and outcome in rheumatoid arthritis. A longitudinal study. Scand. J. Rheumatol. 31:2002;351-354
97. Hammer H.B., Kvien T.K., Glennas A., Melby K. A longitudinal study of calprotectin as an inflammatory marker in patients with reactive arthritis. Clin. Exp. Rheumatol. 13:1995;59-64
98. Sinz A., Bantscheff M., Mikkat S., Ringel B., Drynda S., Kekow J., et al. Mass spectrometric proteome analyses of synovial fluids and plasmas from patients suffering from rheumatoid arthritis and comparison to reactive arthritis or osteoarthritis. Electrophoresis. 23:2002;3445-3456
99. Rouleau P., Vandal K., Ryckman C., Poubelle P.E., Boivin A., Talbot M., et al. The calcium-binding protein S100A12 induces neutrophil adhesion, migration, and release from bone marrow in mouse at concentrations similar to those found in human inflammatory arthritis. Clin. Immunol. 107:2003;46-54
100. Foell D., Kane D., Bresnihan B., Vogl T., Nacken W., Sorg C., et al. Expression of the pro-inflammatory protein S100A12 (EN-RAGE) in rheumatoid and psoriatic arthritis. Rheumatology (Oxford). 42:2003;1383-1389
101. Foell D., Wittkowski H., Hammerschmidt I., Wulffraat N.M., Schmeling H., Frosch M., et al. Monitoring neutrophil activation in juvenile rheumatoid arthritis by S100A12 serum concentrations. Arthritis Rheum. 50:2004;1286-1295
102. Barthe C., Figarella C., Carrere J., Guy-Crotte O. Identification of 'cystic fibrosis protein' as a complex of two calcium-binding proteins present in human cells of myeloid origin. Biochim. Biophys. Acta. 1096:1991;175-177
103. Roth J., Teigelkamp S., Wilke M., Grun L., Tummler B., Sorg C. Complex pattern of the myelo-monocytic differentiation antigens MRP8 and MRP14 during chronic airway inflammation. Immunobiology. 186:1992;304-314
104. Renaud W., Merten M., Figarella C. Increased coexpression of CFTR and S100 calcium binding proteins MRP8 and MRP14 mRNAs in cystic fibrosis human tracheal gland cells. Biochem. Biophys. Res. Commun. 201:1994;1518-1525
105. Thomas G.R., Costelloe E.A., Lunn D.P., Stacey K.J., Delaney S.J., Passey R., et al. G551D cystic fibrosis mice exhibit abnormal regulation of inflammation in lungs and macrophages. J. Immunol. 164:2000;3870-3877
106. Cole A.M., Kim Y.H., Tahk S., Hong T., Weis P., Waring A.J., et al. Calcitermin, a novel antimicrobial peptide isolated from human airway secretions. FEBS Lett. 504:2001;5-10
107. Golden B.E., Clohessy P.A., Russell G., Fagerhol M.K. Calprotectin as a marker of inflammation in cystic fibrosis. Arch. Dis. Child. 74:1996;136-139
108. Clohessy P.A., Golden B.E. Elevated plasma levels of L1L and L1H in CF patients. Biochem. Soc. Trans. 24:1996;310S
109. Rugtveit J., Brandtzaeg P., Halstensen T.S., Fausa O., Scott H. Increased macrophage subset in inflammatory bowel disease: apparent recruitment from peripheral blood monocytes. Gut. 35:1994;669-674
110. Lugering N., Stoll R., Kucharzik T., Schmid K.W., Rohlmann G., Burmeister G., et al. Immunohistochemical distribution and serum levels of the Ca(2+)-binding proteins MRP8, MRP14 and their heterodimeric form MRP8/14 in Crohn's disease. Digestion. 56:1995;406-414
111. Schmid K.W., Lugering N., Stoll R., Brinkbaumer P., Winde G., Domschke W., et al. Immunohistochemical demonstration of the calcium-binding proteins MRP8 and MRP14 and their heterodimer (27E10 antigen) in Crohn's disease. Hum. Pathol. 26:1995;334-337
112. Costa F., Mumolo M.G., Bellini M., Romano M.R., Ceccarelli L., Arpe P., et al. Role of faecal calprotectin as non-invasive marker of intestinal inflammation. Dig. Liver Dis. 35:2003;642-647
113. Roseth A.G., Schmidt P.N., Fagerhol M.K. Correlation between faecal excretion of indium-111-labelled granulocytes and calprotectin, a granulocyte marker protein, in patients with inflammatory bowel disease. Scand. J. Gastroenterol. 34:1999;50-54
114. Tibble J.A., Sigthorsson G., Bridger S., Fagerhol M.K., Bjarnason I. Surrogate markers of intestinal inflammation are predictive of relapse in patients with inflammatory bowel disease. Gastroenterology. 119:2000;15-22
115. Tibble J.A., Sigthorsson G., Foster R., Forgacs I., Bjarnason I. Use of surrogate markers of inflammation and Rome criteria to distinguish organic from nonorganic intestinal disease. Gastroenterology. 123:2002;450-460
116. Summerton C.B., Longlands M.G., Wiener K., Shreeve D.R. Faecal calprotectin: a marker of inflammation throughout the intestinal tract. Eur. J. Gastroenterol. Hepatol. 14:2002;841-845
117. Aadland E., Fagerhol M.K. Faecal calprotectin: a marker of inflammation throughout the intestinal tract. Eur. J. Gastroenterol. Hepatol. 14:2002;823-825
118. Roseth A.G., Fagerhol M.K., Aadland E., Schjonsby H. Assessment of the neutrophil dominating protein calprotectin in feces. A methodologic study. Scand. J. Gastroenterol. 27:1992;793-798
119. Carroccio A., Iacono G., Cottone M., Di Prima L., Cartabellotta F., Cavataio F., et al. Diagnostic accuracy of fecal calprotectin assay in distinguishing organic causes of chronic diarrhea from irritable bowel syndrome: a prospective study in adults and children. Clin. Chem. 49:2003;861-867
120. Bunn S.K., Bisset W.M., Main M.J., Gray E.S., Olson S., Golden B.E. Fecal calprotectin: validation as a noninvasive measure of bowel inflammation in childhood inflammatory bowel disease. J. Pediatr. Gastroenterol. Nutr. 33:2001;14-22
121. Husebye E., Ton H., Johne B. Biological variability of fecal calprotectin in patients referred for colonoscopy without colonic inflammation or neoplasm. Am. J. Gastroenterol. 96:2001;2683-2687
122. Thjodleifsson B., Sigthorsson G., Cariglia N., Reynisdottir I., Gudbjartsson D.F., Kristjansson K., et al. Subclinical intestinal inflammation: an inherited abnormality in Crohn's disease relatives? Gastroenterology. 124:2003;1728-1737
123. Limburg P.J., Ahlquist D.A., Sandborn W.J., Mahoney D.W., Devens M.E., Harrington J.J., et al. Fecal calprotectin levels predict colorectal inflammation among patients with chronic diarrhea referred for colonoscopy. Am. J. Gastroenterol. 95:2000;2831-2837
124. Bunn S.K., Bisset W.M., Main M.J., Golden B.E. Fecal calprotectin as a measure of disease activity in childhood inflammatory bowel disease. J. Pediatr. Gastroenterol. Nutr. 32:2001;171-177
125. Carroll D., Corfield A., Spicer R., Cairns P. Faecal calprotectin concentrations and diagnosis of necrotising enterocolitis. Lancet. 361:2003;310-311
126. Olafsdottir E., Aksnes L., Fluge G., Berstad A. Faecal calprotectin levels in infants with infantile colic, healthy infants, children with inflammatory bowel disease, children with recurrent abdominal pain and healthy children. Acta Paediatr. 91:2002;45-50
127. Fagerberg U.L., Loof L., Merzoug R.D., Hansson L.O., Finkel Y. Fecal calprotectin levels in healthy children studied with an improved assay. J. Pediatr. Gastroenterol. Nutr. 37:2003;468-472
128. Nissen A.C., Van Gils C.E., Menheere P.P., Van Den Neucker A.M., Van Der Hoeven M.A., Forget P.P. Fecal calprotectin in healthy term and preterm infants. J. Pediatr. Gastroenterol. Nutr. 38:2004;107-108
129. Lugering N., Stoll R., Schmid K.W., Kucharzik T., Stein H., Burmeister G., et al. The myeloic related protein MRP8/14 (27E10 antigen)-usefulness as a potential marker for disease activity in ulcerative colitis and putative biological function. Eur. J. Clin. Invest. 25:1995;659-664
130. Kuruto R., Nozawa R., Takeishi K., Arai K., Yokota T., Takasaki Y. Myeloid calcium binding proteins: expression in the differentiated HL-60 cells and detection in sera of patients with connective tissue diseases. J. Biochem. (Tokyo). 108:1990;650-653
131. Haga H.J., Brun J.G., Berntzen H.B., Cervera R., Khamashta M., Hughes G.R. Calprotectin in patients with systemic lupus erythematosus: relation to clinical and laboratory parameters of disease activity. Lupus. 2:1993;47-50
132. Burkhardt K., Radespiel-Troger M., Rupprecht H.D., Goppelt-Struebe M., Riess R., Renders L., et al. An increase in myeloid-related protein serum levels precedes acute renal allograft rejection. J. Am. Soc. Nephrol. 12:2001;1947-1957
133. Kislinger T., Tanji N., Wendt T., Qu W., Lu Y., Ferran L.J. Jr., et al. Receptor for advanced glycation end products mediates inflammation and enhanced expression of tissue factor in vasculature of diabetic apolipoprotein E-null mice. Arterioscler. Thromb. Vasc. Biol. 21:2001;905-910
134. Foell D., Ichida F., Vogl T., Yu X., Chen R., Miyawaki T., et al. S100A12 (EN-RAGE) in monitoring Kawasaki disease. Lancet. 361:2003;1270-1272
135. Kristinsson J., Nygaard K., Aadland E., Barstad S., Sauar J., Hofstad B., et al. Screening of first degree relatives of patients operated for colorectal cancer: evaluation of fecal calprotectin vs. hemoccult II. Digestion. 64:2001;104-110
136. Gilbert J.A., Ahlquist D.A., Mahoney D.W., Zinsmeister A.R., Rubin J., Ellefson R.D. Fecal marker variability in colorectal cancer: calprotectin versus hemoglobin. Scand. J. Gastroenterol. 31:1996;1001-1005
137. Limburg P.J., Devens M.E., Harrington J.J., Diehl N.N., Mahoney D.W., Ahlquist D.A. Prospective evaluation of fecal calprotectin as a screening biomarker for colorectal neoplasia. Am. J. Gastroenterol. 98:2003;2299-2305
138. Tibble J.A., Sigthorsson G., Foster R., Scott D., Fagerhol M.K., Roseth A., et al. High prevalence of NSAID enteropathy as shown by a simple faecal test. Gut. 45:1999;362-366
139. Homann C., Garred P., Graudal N., Hasselqvist P., Christiansen M., Fagerhol M.K., et al. Plasma calprotectin: a new prognostic marker of survival in alcohol-induced cirrhosis. Hepatology. 21:1995;979-985
140. Berger D., Bolke E., Seidelmann M., Beger H.G. Time-scale of interleukin-6, myeloid related proteins (MRP), C reactive protein (CRP), and endotoxin plasma levels during the postoperative acute phase reaction. Shock. 7:1997;422-426
141. Beiche A., Konig H.H., Ebinger M., Matysiak-Klose D., Braun V., Leidl R. Costs of ambulant care for patients with inflammatory bowel disease in general practice. Z. Gastroenterol. 41:2003;527-536
142. Ward F.M., Bodger K., Daly M.J., Heatley R.V. Clinical economics review: medical management of inflammatory bowel disease. Aliment. Pharmacol. Ther. 13:1999;15-25
143. Murthy A.R., Lehrer R.I., Harwig S.S., Miyasaki K.T. In vitro candidastatic properties of the human neutrophil calprotectin complex. J. Immunol. 151:1993;6291-6301
144. Sohnle P.G., Collins-Lech C., Wiessner J.H. The zinc-reversible antimicrobial activity of neutrophil lysates and abscess fluid supernatants. J. Infect. Dis. 164:1991;137-142
145. Lusitani D., Malawista S.E., Montgomery R.R. Calprotectin, an abundant cytosolic protein from human polymorphonuclear leukocytes, inhibits the growth of Borrelia burgdorferi. Infect. Immun. 71:2003;4711-4716
146. Srikrishna G., Toomre D.K., Manzi A., Panneerselvam K., Freeze H.H., Varki A., et al. A novel anionic modification of N-glycans on mammalian endothelial cells is recognized by activated neutrophils and modulates acute inflammatory responses. J. Immunol. 166:2001;624-632