Nutritional immunity: S100 proteins at the host-pathogen interface

Journal of Biological Chemistry

Volumn 290, Issue 31, 2015, Pages 18991-18998

  Zackular, Joseph P ^a   Chazin, Walter J ^a   Skaar, Eric P ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; MICROORGANISMS; PATHOGENS; PATTERN RECOGNITION;

ANTI-MICROBIAL PROPERTIES; BINDING PROTEINS; CELLULAR FUNCTION; IMMUNE RESPONSE; INFLAMMATORY RESPONSE; METAL SEQUESTRATION; MOLECULAR PATTERNS; PATTERN RECOGNITION RECEPTORS;

PROTEINS;

CALCIUM ION; COPPER; MANGANESE; PROTEIN S 100; ZINC ION;

DISEASE ASSOCIATION; HOST PATHOGEN INTERACTION; HUMAN; IMMUNE RESPONSE; IMMUNITY; IMMUNOREGULATION; INFECTION SENSITIVITY; INFLAMMATORY DISEASE; METAL BINDING; MOLECULAR BIOLOGY; NONHUMAN; NUTRITIONAL IMMUNITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REGULATORY MECHANISM; REVIEW; ANIMAL; BACTERIAL INFECTION; IMMUNOLOGY; INNATE IMMUNITY; PHYSIOLOGY;

ANIMALS; BACTERIAL INFECTIONS; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNITY, INNATE; S100 PROTEINS;

EID: 84940469864     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.R115.645085     Document Type: Review

References (82)

1. Donato, R., Cannon, B. R., Sorci, G., Riuzzi, F., Hsu, K., Weber, D. J., and Geczy, C. L. (2013) Functions of S100 proteins. Curr. Mol. Med. 13, 24-57
2. Marenholz, I., Heizmann, C. W., and Fritz, G. (2004) S100 proteins in mouse and man: From evolution to function and pathology (including an update of the nomenclature). Biochem. Biophys. Res. Commun. 322 1111-1122
3. Van Lent, P. L., Grevers, L. C., Schelbergen, R., Blom, A., Geurts, J., Sloetjes, A., Vogl, T., Roth, J., and Van Den Berg, W. B. (2010) S100A8 causes a shift to ward expression of activatory Fc- receptors on macrophages via Tolllike receptor 4 and regulates Fc- receptor expression in synovium during chronic experimental arthritis. Arthritis Rheum. 62, 3353-3364
4. Donato, R. (2003) Intracellular and extracellular roles of S100 proteins. Microsc. Res. Tech. 60, 540-551
5. Ravasi T. Hsu K. Goyette J. Schroder K. Yang Z. Rahimi F. Miranda L. P. Alewood P. F. Hume D. A.Geczy C. 2004 Probing the S100 protein family through genomic and functional analysis. Genomics 84 10-22
6. Heizmann, C. W., Fritz, G., and Schäfer, B. W. (2002) S100 proteins: Structure, functions and pathology. Front. Biosci. 7, d1356-d1368
7. Potts, B. C., Smith, J., Akke, M., Macke, T. J., Okazaki, K., Hidaka, H., Case, D. A., and Chaz in, W. J. (1995) The structure of calcyclin reveals a novel homodimeric fold for S100 Ca2-binding proteins. Nat. Struct. Biol. 2, 790-796
8. Bhattacharya, S., Bunick, C. G., and Chazin, W. J. (2004) Target selectivity in EF-hand calcium binding proteins. Biochim. Biophys. Acta 1742, 69-79
9. Santamaria-Kisiel, L., Rintala-Dempsey, A. C., and Shaw, G. S. (2006) Calcium-dependent and-independent interactions of the S100 protein family. Biochem. J. 396, 201-214
10. Foell, D., Wittkowski, H., Vogl, T., and Roth, J. (2007) S100 proteins expressed in phagocytes: A novel group of damage-associated molecular pattern molecules. J. Leukoc. Biol. 81, 28-37
11. Leclerc, E., Fritz, G., Vetter, S. W., and Heizmann, C. W. (2009) Binding of S100 proteins to RAGE: An update. Biochim. Biophys. Acta 1793, 993-1007
12. Damo, S. M., Kehl-Fie, T. E., Sugitani, N., Holt, M. E., Rathi, S., Murphy, W. J., Zhang, Y., Betz, C., Hench, L., Fritz, G., Skaar, E. P., and Chazin, W. J. ( 2013) Molecular basis for manganese sequestration by calprotectin and roles in the innate immune response to invading bacterial pathogens. Proc. Natl. Acad. Sci. U.S.A. 110, 3841-3846
13. Gaddy, J. A., Radin, J. N., Loh, J. T., Piazuelo, M. B., Kehl-Fie, T. E., Delgado, A. G., Ilca, F. T., Peek, R. M., Cover, T. L., Chazin, W. J., Skaar, E. P., and Scott Algood, H. M. (2014) The host protein calprotectin modulates the Helicobacter pylori cag type IV secretion system via zinc sequestration. PLoS Pathog. 10, e1004450
14. Hood, M. I., Mortensen, B. L., Moore, J. L., Zhang, Y., Kehl-Fie, T. E., Sugitani, N., Chazin, W. J., Caprioli, R. M., and Skaar, E. P. (2012) Identification of an Acinetobacter baumannii zinc acquisition system that facilitates resistance to calprotectin-mediated zinc sequestration. PLoS Pathog. 8, e1003068
15. Kehl-Fie, T. E., Chitayat, S., Hood, M. I., Damo, S., Restrepo, N., Garcia, C., Munro, K. A., Chazin, W. J., and Skaar, E. P. (2011) Nutrient metal sequestr ation by calprotectin inhibits bacterial superoxide defense, enhancing neutrophil killing of Staphylococcus aureus. Cell Host Microbe 10, 158-164
16. Kehl-Fie, T. E., Zhang, Y., Moore, J. L., Farrand, A. J., Hood, M. I., Rathi, S., Chazin, W. J., Caprioli, R. M., and Skaar, E. P. (2013) MntABC and MntH contribute to systemic Staphylococcus aureus infection by competing with calprotectin for nutrient manganese. Infect. Immun. 81, 3395-3405
17. Liu, J. Z., Jellbauer, S., Poe, A. J., Ton, V., Pesciaroli, M., Kehl-Fie, T. E., Restrepo, N. A., Hosking, M. P., Edwards, R. A., Battistoni, A., Pasquali, P., Lane, T. E., Chazin, W. J., Vogl, T., Roth, J., Skaar, E. P., and Raffatellu, M. (2012) Zinc sequestration by the neutrophil protein calprotectin enhances Salmonella growth in the inflamed gut. Cell Host Microbe 11, 227-239
18. Hunter, M. J., and Chazin, W. J. (1998) High level expression and dimer characterization of the S100 EF-hand proteins, migration inhibitory factor-related proteins 8 and 14. J. Biol. Chem. 273, 12427-12435
19. Pröpper, C., Huang, X., Roth, J., Sorg, C., and Nacken, W. (1999) 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, 183-188
20. Korndörfer, I. P., Brueckner, F., and Skerra, A. (2007) The crystal structure of the human (S100A8/S100A9)2 heterotetramer, calprotec tin, illustrates how conformational changes of interacting -helices can determine specific association of two EF-hand proteins. J. Mol. Biol. 370, 887-898
21. Brophy, M. B., Hayden, J. A., and Nolan, E. M. ( 2012) Calcium ion gradients modulate the zinc affinity and antibacterial activity of human calprotectin. J. Am. Chem. Soc. 134, 18089-18100
22. Hayden, J. A., Brophy, M. B., Cunden, L. S., and Nolan, E. M. (2013) High-affinity manganese coordination by human calprotectin is calciumdependent and requires the histidine-rich site formed at the dimer interface. J. Am. Chem. Soc. 135, 775-787
23. Brodersen , D. E., Nyborg, J., and Kjeldgaard, M. (1999) Zinc-binding site of an S100 protein revealed: Two crystal structures of Ca2-bound human psoriasin (S100A7) in the Zn2-loaded and Zn2-free states. Biochemistry 38, 1695-170 4
24. Moroz, O. V., Blagova, E. V., Wilkinson, A. J., Wilson, K. S., and Bronstein, I. B. (2009) The crystal structures of human S100A12 in apo form and in complex with zinc: New insights into S100A12 oligome risation. J. Mol. Biol. 391, 536-551
25. Donato, R. (2001) S100: A multigenic family of calcium-modulated proteins of the EF-hand type with intracellular and extracellular functional roles. Int. J. Biochem. Cell Biol. 33, 637-668
26. Lagasse, E., and Clerc, R. G. (1988) Cloning and expression of two human genes encoding calcium-binding proteins that are regulated during myeloid differentiation. Mol. Cell. Biol. 8, 2402-2410
27. Hsu K Champaiboon C. Guenther B. D. Sorenson B. S. Khammanivong A. Ross K. F. Geczy C. L. Herzberg M. C.(2009) Antiinfective protective properties of S100 calgranulins. Antiinflamm. Antiallergy Agents Med. Chem. 8 290-305
28. Clohessy, P. A., and Golden, B. E. (1995) Calprotectin- mediated zinc chelation as a biostatic mechanism in host defence. Scand. J. Immunol. 42, 551-556
29. Hessian, P. A., Edgeworth, J., and Hogg, N. (1993) MRP-8 and MRP-14, two abundant Ca2-binding proteins of neutrophils and monocytes. J. Leukoc. Biol. 53, 197-204
30. Stoll, S. W., Zhao, X., and Elder, J. T. (1998) EGF stimulates transcription of CaN19 (S100A2) in HaCaT keratinocytes. J. Invest. Dermatol. 111, 1092-1097
31. Nukui, T., Ehama, R., Sakaguchi, M., Sonegawa, H., Katagiri, C., Hibino, T., and Huh, N. H. (2008) S100A8/A9, a key mediator for positive feedback growth stimulation of normal human keratinocytes. J. Cell. Biochem. 104, 453-464
32. Goebeler, M., Roth, J., Van Den Bos, C., Ader, G., and Sorg, C. (1995) Increase of calcium levels in epithelial cells induces translo cation of calcium-binding proteins migration inhibitory factor-related protein 8 (MRP8) and MRP14 to keratin intermediate filaments. Biochem. J. 309, 419-424
33. Grimbaldeston, M. A., Geczy, C. L., Tedla, N., Finlay-Jones, J. J., and Hart, P. H. (2003) S100A8 induction in keratinocytes by ultravioletAirradiation is dependent on reactive oxygen intermediates. J. Invest. Dermatol. 121, 1168-1174
34. Mørk, G., Schjerven, H., Mangschau, L., Søyland, E., and Brandtzaeg, P. (2003) Proinflammatory cytokines upregulate expression of calprotectin (L1 protein, MRP-8/MRP-14) in cultured human keratinocytes. Br. J. Dermatol. 149, 484-491
35. Frosch, M., Strey, A., Vogl, T., Wulffraat, N. M., Kuis, W., Sunderkötter, C., Harms, E., Sorg, C., and Roth, J. (2000) Myeloid-related proteins 8 and 14 are specifically secreted duri ng interaction of phagocytes and activated endothelium and are useful markers for monitoring disease activity in pauciarticular-onset juvenile rheumatoid arthritis. Arthritis Rheum. 43, 628-637
36. Yang, Z., Tao, T., Raftery, M. J., Youssef, P., Di Girolamo, N., and Geczy, C. L. (2001) Proinflammatory properties of the human S100 protein S100A12. J. Leukoc. Biol. 69, 986-994
37. Yang, Z., Yan, W. X., Cai, H., Tedla, N., Armishaw, C., Di Girolamo, N., Wang, H. W., Hampartzoumian, T., Simpson, J. L., Gibson, P. G., Hunt, J., Hart, P., Hughes, J. M., Perry, M. A., Alewood, P. F., and Geczy, C. L. (2007) S100A12 provokes mast cell activation: A potential amplification pathway in asthma and innate immunity. J. Allergy Clin. Immunol. 119, 106-114
38. Rammes, A., Roth, J., Goebeler, M., Klempt, M., Hartmann, M., and Sorg, C. (1997) 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, 9496-9502
39. Urban, C. F., Ermert, D., Schmid, M., Abu-Abed, U., Goosmann, C., Nacken, W., Brinkmann, V., Jungblut, P. R., and Zychlinsky, A. (2009) Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans. PLoS Pathog. 5, e1000639
40. Voganatsi, A., Panyutich, A., Miyasaki, K. T., and Murthy, R. K. (2001) Mechanism of extracellular release of human neutrophil calprotectin complex. J. Leukoc. Biol. 70, 130-134
41. Gebhardt, C., Né meth, J., Angel, P., and Hess, J. (2006) S100A8 and S100A9 in inflammation and cancer. Biochem. Pharmacol. 72, 1622-1631
42. Gläser, R., Harder, J., Lange, H., Bartels, J., Christophers, E., and Schröder, J. M. (2005) Antimicrobial psoriasin (S100A7) protects human skin from Escherichia coli infection. Nat. Immunol. 6, 57-64
43. Vogl, T., Tenbrock, K., Ludwig, S., Leukert, N., Ehrhardt, C., Van Zoelen, M. A., Nacken, W., Foell, D., Van Der Poll, T., Sorg, C., and Roth, J. (2007) Mrp8 and Mrp14 are endogenous activators of Toll-like receptor 4, promoting lethal, endotoxin-induced shock. Nat. Med. 13, 1042-1049
44. Turovskaya, O., Foell, D., Sinha, P., Vogl, T., Newlin, R., Nayak, J., Nguyen, M., Olsson, A., Nawroth, P. P., Bierhaus, A., Varki, N., Kronenberg, M., Freeze, H. H., and Srikrishna, G. (2008) RAGE, carboxylated glycans and S100A8/A9 play essential roles in colitis-associated carcinogenesis. Carcinogenesis 29, 2035-2043
45. Schiopu, A., and Cotoi, O. S. (2013) S 100A8 and S100A9: DAMPs at the crossroads between innate immunity, traditional risk factors, and cardiovascular disease. Mediators Inflamm. 2013, 828354
46. Hofmann, M. A., Drury, S., Fu, C., Qu, W., Taguc hi, A., Lu, Y., Avila, C., Kambham, N., Bierhaus, A., Nawroth, P., Neurath, M. F., Slattery, T., Beach, D., McClary, J., Nagashima, M., Morser, J., Stern, D., and Schmidt, A. M. (1999) RAGE mediates a novel proinflammatory axis: A central cell surface receptor for S100/calgranulin polypeptides. Cell 97, 889-901
47. Ghavami, S., Rashedi, I., Dattilo, B. M., Eshraghi, M., Chazin, W. J., Hashemi, M., Wesselborg, S., Kerkhoff, C., and Los, M. (2008) S100A8/A9 at low concentration promotes tumor cell growth via RAGE ligation and MAP kinase-dependent pathway. J. Leukoc. Biol. 83, 1484-1492
48. Gebhardt C. Riehl A. Durchdewald M. Németh J. Fürstenberger G. Müller-Decker, K. Enk, A. Arnold, B. Bierhaus, A. Nawroth, P. P. Hess, J., Angel P.2008 RAGE signaling sustains inflammation and promotes tumor development. J. Exp. Med. 205 275-285
49. Sunahori, K., Yamamura, M., Yamana, J., Takasugi, K., Kawashima, M., Yamamoto, H., Chazin, W. J., Nakatani, Y., Yui, S., and Makino, H. (2006) The S100A8/A9 heterodimer amplifies proinflammatory cytokine production by macrophages via activation of nuclear factor -B and p38 mitogen-activated protein kinase in rheumatoid arthritis. Arthritis Res. Ther. 8, R69
50. Ryckman, C., Vandal, K., Rouleau, P., Talbot, M., and Tessier, P. A. (2003) Proinflammatory activities of S100: Proteins S100A8, S100A9, and S100A8/A9 induce neutrophil chemotaxis an d adhesion. J. Immunol. 170, 3233-3242
51. Lim, S. Y., Raftery, M., Cai, H., Hsu, K., Yan, W. X., Hseih, H. L., Watts, R. N., Richardson, D., Thomas, S., Perry, M., and Geczy, C. L. (2008) S-nitrosylated S100A8: Novel anti-inflammatory properties. J. Immunol. 181, 5627-5636
52. Goyette, J., and Geczy, C. L. (2011) Inflammation-associated S100 proteins: New mechanisms that regulate function. Amino acids 41, 821-842
53. Ghavami, S., Eshragi, M., Ande, S. R., Chazin, W. J., Klonisch, T., Halayko, A. J., McNeill, K. D., Hashemi, M., Kerkhoff, C., and Los, M. (20 10) S100A8/A9 induces autophagy and apoptosis via ROS-mediated crosstalk between mitochondria and lysosomes that involves BNIP3. Cell Res. 20, 314-331
54. Viemann, D., Barczyk, K., Vogl, T., Fischer, U., Sunderkötter, C., Schulze-Osthoff, K., and Roth, J. (2007) MRP8/MRP14 impairs endothelial integrity and induces a caspase-dependent and-independent cell death program. Blood 109, 2453-2460
55. Moroz, O. V., Burkitt, W., Wittkowski, H., He, W., Ianoul, A., Novitskaya, V., Xie, J., Polyakova, O., Lednev, I. K., Shekhtman, A., Derrick, P. J., Bjoerk, P., Foell, D., and Bronstei n, I. B. (2009) Both Ca2- and Zn2- are essential for S100A12 protein oligomerization and function. BMC Biochem. 10, 11
56. Wolf, R., Howard, O. M., Dong, H. F., Voscopoulos, C., Boeshans, K., Winston, J., Divi, R., Gunsior, M., Goldsmith, P., Ahvazi, B., Chavakis, T., Oppenheim, J. J., and Yuspa, S. H. (2008) Chemotactic activity of S100A7 (Psoriasin) is mediated by the receptor for advanced glycation end pr oducts and potentiates inflammation with highly homologous but functionally distinct S100A15. J. Immunol. 181, 1499-1506
57. Nakatani, Y., Yamazaki, M., Chazin, W. J., and Yui, S. (2005) Regulation of S100A8/A9 (calprotectin) binding to tumor cells by zinc ion and its implication for apoptosis-inducing activity. Mediators Inflamm. 2005, 280-292
58. Lügering, N., Stoll, R., Kucharzik, T., Schmid, K. W., Rohlmann, G., Burmeister, G., Sorg, C., and Domschke, W. (1995) Immunohistochemical distribution and serum levels of the Ca2-binding proteins MRP8, MRP14 and their heterodimeric form MRP8/14 in Crohn's disease. Digestion 56, 406-414
59. Salama, I., Malone, P. S., Mihaimeed, F., and Jones, J. L. (2008) A review of the S100 proteins in cancer. Eur. J. Surg. Oncol. 34, 357-364
60. Stulík , J., Osterreicher, J., Koupilová, K., Knízek, Macela, A., Bures, J., Jandík, P., Langr, F., Dedic, K., and Jungblut, P. R. (1999) The analysis of S100A9 and S100A8 expression in matched sets of macroscopicall y normal colon mucosa and colorectal carcinoma: The S100A9 and S100A8 positive cells underlie and invade tumor mass. Electrophoresis 20, 1047-1054
61. Emberley, E. D., Niu, Y., Njue, C., Kliewer, E. V., Murphy, L. C., and Watson, P. H. (2003) Psoriasin (S100A7) expression is associated with poor outcome in estrogen receptor-negative invasive breast cancer. Clin. Cancer Res. 9, 2627-2631
62. Broome, A. M., Ryan, D., and Eckert, R. L. (2003) S100 protein subcellular localization during epidermal differentiation and psoriasis. J. Histochem. Cytochem. 51, 675-685
63. Shang, J., Zhang, Z., Song, W., Zhou, B., Zhang, Y., Li, G., and Qiu, S. (2013) S100A10 as a novel biomarker in colorectal cancer. Tumour Biol. 34, 3785-3790
64. Konikoff, M. R., and Denson, L. A. (2006) Role of fecal calprote ctin as a biomarker of intestinal inflammation in inflammatory bowel disease. Inflamm. Bowel Dis. 12, 524-534
65. Hammer, H. B., Haavardsholm, E. A., and Kvien, T. K. (2008) Calprotectin (a major leucocyte protein) is associated with the levels of anti-CCP and rheumatoid factor in a longitudinal study of patients with very early rheumatoid arthritis. Scand. J. Rheumatol. 37, 179-1 82
66. Isidor, B., Poignant, S., Corradini, N., Fouassier, M., Quartier, P., Roth, J., and Picherot, G. (2009) Hyperzincemia and hypercalprotectinemia: Unsuccessful treatment with tacrolimus. Acta Paediatr. 98, 410-412
67. Vaos, G., Kostakis, I. D., Zavras, N., and Chatzemichael, A. (2013) The role of calprotectin in pediatric disease. Biomed Res. Int. 2013, 542363
68. Fessatou, S., Fagerhol, M. K., Roth, J., Stamoulakatou, A., Kitra, V., Hadarean, M., Paleologos, G., Chandrinou, H., Sampson, B., and Papassotiriou, I. (2005) Severe anemia and neutropenia associated with hyperzincemia and hypercalprotectinemia. J. Pediatr. Hematol. Oncol. 27, 477-480
69. Saito Y. Saito K. Hirano Y. Ikeya K. Suzuki H. Shishikura K. Manno S. Takakuwa Y. Nakagawa K. Iwasa A. Fujikawa S. Moriya M. Mizoguchi N. Golden B. E. and Osawa M.2002 Hyperzincemia with systemic inflammation: A heritable disorder of calprotectin metabolism with rheumatic manifestations? J. Pediatr. 140,267-269
70. Kehl-Fie, T. E., and Skaar, E. P. (2010) Nutritional immunity beyond iron: A role for manganese and zinc. Curr. Opin. Chem. Biol. 14, 218-224
71. Gagnon, D. M., Brophy, M. B., Bowman, S. E., Stich, T. A., Drennan, C. L., Britt, R. D., and Nolan, E. M. (2015) Manganese binding properties of human calprotectin under conditions of high and low calcium: X-ray crystallographic and advanced EPR spectroscopic analysis. J. Am. Chem. Soc. 137, 3004-3016
72. Moroz, O. V., Antson, A. A., Grist, S. J., Maitland, N. J., Dodson, G. G., Wilson, K. S., Lukanidin, E., and Bronstein, I. B. (2003) Structure of the human S100A12-copper complex: Implications for host- parasite defence. Acta Crystallogr. D Biol. Crystallogr. 59, 859-867
73. Lee, K. C., and Eckert, R. L. (2007) S100A7 (Psoriasin): Mechanism of antibacterial action in wounds. J. Invest. Dermatol. 127, 945-957
74. Cole, A. M., Kim, Y. H., Tahk, S., Hong, T., Weis, P., Waring, A. J., and Ganz, T. (2001) Calcitermin, a novel antimicrobial peptide isolated from human airway secretions. FEBS Lett. 504, 5-10
75. Lisher, J. P., and Giedroc, D. P. (2013) Manganese acquisition and homeostasis at the host-pathogen interface. Front. Cell. Infect. Microbiol. 3, 91
76. Kane, D., Roth, J., Frosch, M., Vogl, T., Bresnihan, B., and FitzGerald, O. (2003) Increased perivascular synovial membrane expression of myeloidrelated proteins in psoriatic arthritis. Arthritis Rheum. 48, 1676-1685
77. Haga, H. J., Brun, J. G., Berntzen, H. B., Cervera, R., Khamashta, M., and Hughes, G. R. (1993) Calprotectin in patients with systemic lupus erythematosus: Relation to clinical and laboratory parameters of disease activity. Lupus 2, 47-50
78. Pedersen, L., Nybo, M., Poulsen, M. K., Henriksen, J. E., Dahl, J., and Rasmussen, L. M. (2014) Plasma calprotectin and i ts association with cardiovascular disease manifestations, obesity and the metabolic syndrome in type 2 diabetes mellitus patients. BMC Cardiovasc. Disord. 14, 196
79. Tydé n, H., Lood, C., Gullstrand, B., Jönsen, A., Nived, O., Sturfelt, G., Truedsson, L., Ivars, F., Leanderson, T., and Bengtsson, A. A. (2013) Increased serum levels of S100A8/A9 and S100A12 are associated with cardiovascular disease in patients with inactive systemic lupus erythematosus. Rheumatology 52, 2048-2055
80. Reid, P. A., McAllister, D. A., Boyd, A. C., Innes, J. A., Porteous, D., Greening, A. P., and Gray, R. D. (2015) Measurement of ser um calprotectin in stable patients predicts exacerbation and lung function decline in cystic fibrosis. Am. J. Respir. Crit. Care Med. 191, 233-236
81. Zheng, Y., Niyonsaba, F., Ushio, H., Ikeda, S., Nagaoka, I., Okumura, K., and Ogawa, H. (2008) Microbicidal protein psoriasin is a multifunctional modulator of neutrophil activation. Immunology 124, 357-367
82. Eckert, R. L., Broome, A. M., Ruse, M., Robinson, N., Ryan, D., and Lee, K. (2004) S100 proteins in the epidermis. J. Invest. Dermatol. 123, 23-33