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Amino Acids

, Volume 41, Issue 4, pp 821–842 | Cite as

Inflammation-associated S100 proteins: new mechanisms that regulate function

  • Jesse Goyette
  • Carolyn L. GeczyEmail author
Review Article

Abstract

This review focuses on new aspects of extracellular roles of the calgranulins. S100A8, S100A9 and S100A12 are constitutively expressed in neutrophils and induced in several cell types. The S100A8 and S100A9 genes are regulated by pro- and anti-inflammatory mediators and their functions may depend on cell type, mediators within a particular inflammatory milieu, receptors involved in their recognition and their post-translational modification. The S100A8 gene induction in macrophages is dependent on IL-10 and potentiated by immunosuppressive agents. S100A8 and S100A9 are oxidized by peroxide, hypochlorite and nitric oxide (NO). HOCl generates intra-chain sulfinamide bonds; stronger oxidation promotes cross-linked forms that are seen in human atheroma. S100A8 is >200-fold more sensitive to oxidative cross-linking than low-density lipoprotein and may reduce oxidative damage. S100A8 and S100A9 can be S-nitrosylated. S100A8–SNO suppresses mast cell activation and inflammation in the microcirculation and may act as an NO transporter to regulate vessel tone in inflammatory lesions. S100A12 activates mast cells and is a monocyte and mast cell chemoattractant; a G-protein-coupled mechanism may be involved. Structure–function studies are discussed in relation to conservation and divergence of functions in S100A8. S100A12 induces cytokines in mast cells, but not monocytes/macrophages. It forms complexes with Zn2+ and, by chelating Zn2+, S100A12 significantly inhibits MMPs. Zn2+ in S100A12 complexes co-localize with MMP-9 in foam cells in atheroma. In summary, S100A12 has pro-inflammatory properties that are likely to be stable in an oxidative environment, because it lacks Cys and Met residues. Conversely, S100A8 and S100A9 oxidation and S-nitrosylation may have important protective mechanisms in inflammation.

Keywords

S100 Calgranulins S100A8 S100A9 S100A12 Inflammation Interleukin 10 

Abbreviations

RA

Rheumatoid arthritis

IBD

Inflammatory bowel disease

ROS

Reactive oxygen species

NO

Nitric oxide

TLR

Toll-like receptor

mS100A8

Murine S100A8

mS100A9

Murine S100A9

TNFα

Tumor necrosis factor α

TGFβ

Transforming growth factor β

IFN

Interferon

LPS

Lipopolysaccharide

IL

Interleukin

COX-2

Cyclo-oxygenase 2

cAMP

Cyclic adenosine monophosphate

MAP kinase

Mitogen-activated protein kinase

EC

Endothelial cells

FGF

Fibroblast growth factor

GC

Glucocorticoids

DEX

Dexamethasone

PPAR-γ

Peroxisome proliferator-activated receptor-γ

RAGE

Receptor for advanced glycation end products

NFκB

Nuclear factor κB

EN-RAGE

Extracellular newly identified RAGE-binding protein

AGE

Advanced glycation end products

MCP-1

Monocyte chemotactic protein 1

NIF

Neutrophil immobilizing factor

NADPH

Nicotinamide adenine dinucleotide phosphate

NMR

Nuclear magnetic resonance

MPO

Myeloperoxidase

MMP

Matrix metalloproteinase

Notes

Acknowledgments

The authors acknowledge the National Health and Medical Research Council of Australia for funding and members of the laboratory who contributed to the research discussed in this review, particularly Dr. Kenneth Hsu, Ms. Su Yin Lim, Dr. Zheng Yang, Dr. Weixing Yan and Dr. Mark Raftery and our long-term collaborator, Professor Paul Alewood.

References

  1. Adami C, Bianchi R, Pula G, Donato R (2004) S100B-stimulated NO production by BV-2 microglia is independent of RAGE transducing activity but dependent on RAGE extracellular domain. Biochim Biophys Acta 1742:169–177PubMedCrossRefGoogle Scholar
  2. Aguiar-Passeti T, Postol E, Sorg C, Mariano M (1997) Epithelioid cells from foreign-body granuloma selectively express the calcium-binding protein MRP-14, a novel down-regulatory molecule of macrophage activation. J Leukoc Biol 62:852–858PubMedGoogle Scholar
  3. Akiyama H, Ikeda K, Katoh M, McGeer EG, McGeer PL (1994) Expression of MRP14, 27E10, interferon-alpha and leukocyte common antigen by reactive microglia in postmortem human brain tissue. J Neuroimmunol 50:195–201PubMedCrossRefGoogle Scholar
  4. Akpek EK, Liu SH, Thompson R, Gottsch JD (2002) Identification of paramyosin as a binding protein for calgranulin C in experimental helminthic keratitis. Invest Ophthalmol Vis Sci 43:2677–2684PubMedGoogle Scholar
  5. Anceriz N, Vandal K, Tessier PA (2007) S100A9 mediates neutrophil adhesion to fibronectin through activation of beta2 integrins. Biochem Biophys Res Commun 354:84–89PubMedCrossRefGoogle Scholar
  6. Bai B, Yamamoto K, Sato H, Sugiura H, Tanaka T (2007) Complex regulation of S100A8 by IL-17, dexamethasone, IL-4 and IL-13 in HaCat cells (human keratinocyte cell line). J Dermatol Sci 47:259–262PubMedCrossRefGoogle Scholar
  7. Baldassarre ME, Altomare MA, Fanelli M, Carbone D, Di Bitonto G, Mautone A, Laforgia N (2007) Does calprotectin represent a regulatory factor in host defense or a drug target in inflammatory disease? Endocr Metab Immune Disord Drug Targets 7:1–5PubMedGoogle Scholar
  8. Basso D, Greco E, Fogar P, Pucci P, Flagiello A, Baldo G, Giunco S, Valerio A, Navaglia F, Zambon CF, Falda A, Pedrazzoli S, Plebani M (2006) Pancreatic cancer-derived S-100A8 N-terminal peptide: a diabetes cause? Clin Chim Acta 372:120–128PubMedCrossRefGoogle Scholar
  9. Bausinger H, Lipsker D, Ziylan U, Manie S, Briand JP, Cazenave JP, Muller S, Haeuw JF, Ravanat C, de la Salle H, Hanau D (2002) Endotoxin-free heat-shock protein 70 fails to induce APC activation. Eur J Immunol 32:3708–3713PubMedCrossRefGoogle Scholar
  10. Berntzen HB, Fagerhol MK (1988) L1, a major granulocyte protein: antigenic properties of its subunits. Scand J Clin Lab Invest 48:647–652PubMedCrossRefGoogle Scholar
  11. Bianchi R, Adami C, Giambanco I, Donato R (2007) S100B binding to RAGE in microglia stimulates COX-2 expression. J Leukoc Biol 81:108–118PubMedCrossRefGoogle Scholar
  12. Bianchi R, Giambanco I, Donato R (2008) S100B/RAGE-dependent activation of microglia via NF-kappaB and AP-1 Co-regulation of COX-2 expression by S100B, IL-1beta and TNF-alpha. Neurobiol Aging Google Scholar
  13. Bierhaus A, Humpert PM, Morcos M, Wendt T, Chavakis T, Arnold B, Stern DM, Nawroth PP (2005) Understanding RAGE, the receptor for advanced glycation end products. J Mol Med 83:876–886PubMedCrossRefGoogle Scholar
  14. Bischoff SC (2007) Role of mast cells in allergic and non-allergic immune responses: comparison of human and murine data. Nat Rev Immunol 7:93–104PubMedCrossRefGoogle Scholar
  15. Boyd JH, Kan B, Roberts H, Wang Y, Walley KR (2008) S100A8 and S100A9 mediate endotoxin-induced cardiomyocyte dysfunction via the receptor for advanced glycation end products. Circ Res 102:1239–1246PubMedCrossRefGoogle Scholar
  16. Bozinovski S, Cross M, Vlahos R, Jones JE, Hsuu K, Tessier PA, Reynolds EC, Hume DA, Hamilton JA, Geczy CL, Anderson GP (2005) S100A8 chemotactic protein is abundantly increased, but only a minor contributor to LPS-induced, steroid resistant neutrophilic lung inflammation in vivo. J Proteome Res 4:136–145PubMedCrossRefGoogle Scholar
  17. Brun JG, Haland G, Haga HJ, Fagerhol MK, Jonsson R (1995) Effects of calprotectin in avridine-induced arthritis. Apmis 103:233–240PubMedCrossRefGoogle Scholar
  18. Champaiboon C, Sappington KJ, Guenther BD, Ross KF, Herzberg MC (2009) Calprotectin S100A9 calcium-binding loops I and II are essential for keratinocyte resistance to bacterial invasion. J Biol Chem 284:7078–7090PubMedCrossRefGoogle Scholar
  19. Cole AM, Kim YH, Tahk S, Hong T, Weis P, Waring AJ, Ganz T (2001) Calcitermin, a novel antimicrobial peptide isolated from human airway secretions. FEBS Lett 504:5–10PubMedCrossRefGoogle Scholar
  20. Coleman N, Stanley MA (1994) Expression of the myelomonocytic antigens CD36 and L1 by keratinocytes in squamous intraepithelial lesions of the cervix. Hum Pathol 25:73–79PubMedCrossRefGoogle Scholar
  21. Cornish CJ, Devery JM, Poronnik P, Lackmann M, Cook DI, Geczy CL (1996) S100 protein CP-10 stimulates myeloid cell chemotaxis without activation. J Cell Physiol 166:427–437PubMedCrossRefGoogle Scholar
  22. Couper KN, Blount DG, Riley EM (2008) IL-10: the master regulator of immunity to infection. J Immunol 180:5771–5777PubMedGoogle Scholar
  23. Dale CS, Goncalves LR, Juliano L, Juliano MA, da Silva AM, Giorgi R (2004) The C-terminus of murine S100A9 inhibits hyperalgesia and edema induced by jararhagin. Peptides 25:81–89PubMedCrossRefGoogle Scholar
  24. Dale CS, Pagano Rde L, Paccola CC, Pinotti-Guirao T, Juliano MA, Juliano L, Giorgi R (2006) Effect of the C-terminus of murine S100A9 protein on experimental nociception. Peptides 27:2794–2802PubMedCrossRefGoogle Scholar
  25. Delabie J, de Wolf-Peeters C, van den Oord JJ, Desmet VJ (1990) Differential expression of the calcium-binding proteins MRP8 and MRP14 in granulomatous conditions: an immunohistochemical study. Clin Exp Immunol 81:123–126PubMedCrossRefGoogle Scholar
  26. Devery JM, King NJ, Geczy CL (1994) Acute inflammatory activity of the S100 protein CP-10. Activation of neutrophils in vivo and in vitro. J Immunol 152:1888–1897PubMedGoogle Scholar
  27. Donato R (2003) Intracellular and extracellular roles of S100 proteins. Microsc Res Tech 60:540–551PubMedCrossRefGoogle Scholar
  28. Eckert RL, Broome AM, Ruse M, Robinson N, Ryan D, Lee K (2004) S100 proteins in the epidermis. J Invest Dermatol 123:23–33PubMedCrossRefGoogle Scholar
  29. Edgeworth J, Gorman M, Bennett R, Freemont P, Hogg N (1991) Identification of p8, 14 as a highly abundant heterodimeric calcium binding protein complex of myeloid cells. J Biol Chem 266:7706–7713PubMedGoogle Scholar
  30. Ehlermann P, Eggers K, Bierhaus A, Most P, Weichenhan D, Greten J, Nawroth PP, Katus HA, Remppis A (2006) Increased proinflammatory endothelial response to S100A8/A9 after preactivation through advanced glycation end products. Cardiovasc Diabetol 5:6PubMedCrossRefGoogle Scholar
  31. Endoh Y, Chung YM, Clark IA, Geczy CL, Hsu K (2009) IL-10-dependent S100A8 gene induction in monocytes/macrophages by double-stranded RNA. J Immunol 182:2258–2268PubMedCrossRefGoogle Scholar
  32. Eue I, Langer C, Eckardstein A, Sorg C (2000a) Myeloid related protein (MRP) 14 expressing monocytes infiltrate atherosclerotic lesions of ApoE null mice. Atherosclerosis 151:593–597PubMedCrossRefGoogle Scholar
  33. Eue I, Pietz B, Storck J, Klempt M, Sorg C (2000b) Transendothelial migration of 27E10 + human monocytes. Int Immunol 12:1593–1604PubMedCrossRefGoogle Scholar
  34. Eversole LR, Miyasaki KT, Christensen RE (1992) The distribution of the antimicrobial protein, calprotectin, in normal oral keratinocytes. Arch Oral Biol 37:963–968PubMedCrossRefGoogle Scholar
  35. Eversole LR, Miyasaki KT, Christensen RE (1993) Keratinocyte expression of calprotectin in oral inflammatory mucosal diseases. J Oral Pathol Med 22:303–307PubMedCrossRefGoogle Scholar
  36. Foell D, Kucharzik T, Kraft M, Vogl T, Sorg C, Domschke W, Roth J (2003) Neutrophil derived human S100A12 (EN-RAGE) is strongly expressed during chronic active inflammatory bowel disease. Gut 52:847–853PubMedCrossRefGoogle Scholar
  37. Foell D, Frosch M, Sorg C, Roth J (2004a) Phagocyte-specific calcium-binding S100 proteins as clinical laboratory markers of inflammation. Clin Chim Acta 344:37–51PubMedCrossRefGoogle Scholar
  38. Foell D, Hernandez-Rodriguez J, Sanchez M, Vogl T, Cid MC, Roth J (2004b) Early recruitment of phagocytes contributes to the vascular inflammation of giant cell arteritis. J Pathol 204:311–316PubMedCrossRefGoogle Scholar
  39. Foell D, Wittkowski H, Vogl T, Roth J (2007) S100 proteins expressed in phagocytes: a novel group of damage-associated molecular pattern molecules. J Leukoc Biol 81:28–37PubMedCrossRefGoogle Scholar
  40. Foell D, Wittkowski H, Roth J (2009) Monitoring disease activity by stool analyses: from occult blood to molecular markers of intestinal inflammation and damage. Gut 58:859–868PubMedCrossRefGoogle Scholar
  41. Freemont P, Hogg N, Edgeworth J (1989) Sequence identity. Nature 339:516PubMedCrossRefGoogle Scholar
  42. Frosch M, Strey A, Vogl T, Wulffraat NM, Kuis W, Sunderkotter C, Harms E, Sorg C, Roth J (2000) 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 43:628–637PubMedCrossRefGoogle Scholar
  43. Fu X, Mueller DM, Heinecke JW (2002) Generation of intramolecular and intermolecular sulfenamides, sulfinamides, and sulfonamides by hypochlorous acid: a potential pathway for oxidative cross-linking of low-density lipoprotein by myeloperoxidase. Biochemistry 41:1293–1301PubMedCrossRefGoogle Scholar
  44. Gabrielsen TO, Dale I, Brandtzaeg P, Hoel PS, Fagerhol MK, Larsen TE, Thune PO (1986) Epidermal and dermal distribution of a myelomonocytic antigen (L1) shared by epithelial cells in various inflammatory skin diseases. J Am Acad Dermatol 15:173–179PubMedCrossRefGoogle Scholar
  45. Galli SJ, Nakae S, Tsai M (2005) Mast cells in the development of adaptive immune responses. Nat Immunol 6:135–142PubMedCrossRefGoogle Scholar
  46. Gao B, Tsan MF (2003a) Endotoxin contamination in recombinant human heat shock protein 70 (Hsp70) preparation is responsible for the induction of tumor necrosis factor alpha release by murine macrophages. J Biol Chem 278:174–179PubMedCrossRefGoogle Scholar
  47. Gao B, Tsan MF (2003b) Recombinant human heat shock protein 60 does not induce the release of tumor necrosis factor alpha from murine macrophages. J Biol Chem 278:22523–22529PubMedCrossRefGoogle Scholar
  48. Gebhardt C, Breitenbach U, Tuckermann JP, Dittrich BT, Richter KH, Angel P (2002) Calgranulins S100A8 and S100A9 are negatively regulated by glucocorticoids in a c-Fos-dependent manner and overexpressed throughout skin carcinogenesis. Oncogene 21:4266–4276PubMedCrossRefGoogle Scholar
  49. Gebhardt C, Nemeth J, Angel P, Hess J (2006) S100A8 and S100A9 in inflammation and cancer. Biochem Pharmacol 72:1622–1631PubMedCrossRefGoogle Scholar
  50. Geczy C (1996) Regulation and proinflammatory properties of the chemotactic protein, CP-10. Biochim Biophys Acta 1313:246–252PubMedCrossRefGoogle Scholar
  51. Ghavami S, Kerkhoff C, Los M, Hashemi M, Sorg C, Karami-Tehrani F (2004) Mechanism of apoptosis induced by S100A8/A9 in colon cancer cell lines: the role of ROS and the effect of metal ions. J Leukoc Biol 76:169–175PubMedCrossRefGoogle Scholar
  52. Ghavami S, Kerkhoff C, Chazin WJ, Kadkhoda K, Xiao W, Zuse A, Hashemi M, Eshraghi M, Schulze-Osthoff K, Klonisch T, Los M (2008a) S100A8/9 induces cell death via a novel, RAGE-independent pathway that involves selective release of Smac/DIABLO and Omi/HtrA2. Biochim Biophys Acta 1783:297–311PubMedCrossRefGoogle Scholar
  53. Ghavami S, Rashedi I, Dattilo BM, Eshraghi M, Chazin WJ, Hashemi M, Wesselborg S, Kerkhoff C, Los M (2008b) S100A8/A9 at low concentration promotes tumor cell growth via RAGE ligation and MAP kinase-dependent pathway. J Leukoc Biol 83:1484–1492PubMedCrossRefGoogle Scholar
  54. Glaser R, Harder J, Lange H, Bartels J, Christophers E, Schroder JM (2005) Antimicrobial psoriasin (S100A7) protects human skin from Escherichia coli infection. Nat Immunol 6:57–64PubMedCrossRefGoogle Scholar
  55. Goebeler M, Roth J, Burwinkel F, Vollmer E, Bocker W, Sorg C (1994) Expression and complex formation of S100-like proteins MRP8 and MRP14 by macrophages during renal allograft rejection. Transplantation 58:355–361PubMedGoogle Scholar
  56. Goetzl EJ, Austen KF (1972) A neutrophil-immobilizing factor derived from human leukocytes, I: generation and partial characterization. J Exp Med 136:1564–1580PubMedCrossRefGoogle Scholar
  57. Goetzl EJ, Gigli I, Wasserman S, Austen KF (1973) A neutrophil immobilizing factor derived from human leukocytes, II: specificity of action on polymorphonuclear leukocyte mobility. J Immunol 111:938–945PubMedGoogle Scholar
  58. Gordon S (2003) Alternative activation of macrophages. Nat Rev Immunol 3:23–35PubMedCrossRefGoogle Scholar
  59. Gottsch JD, Liu SH, Minkovitz JB, Goodman DF, Srinivasan M, Stark WJ (1995) Autoimmunity to a cornea-associated stromal antigen in patients with Mooren’s ulcer. Invest Ophthalmol Vis Sci 36:1541–1547PubMedGoogle Scholar
  60. Gottsch JD, Eisinger SW, Liu SH, Scott AL (1999a) Calgranulin C has filariacidal and filariastatic activity. Infect Immun 67:6631–6636PubMedGoogle Scholar
  61. Gottsch JD, Li Q, Ashraf F, O’Brien TP, Stark WJ, Liu SH (1999b) Cytokine-induced calgranulin C expression in keratocytes. Clin Immunol 91:34–40PubMedCrossRefGoogle Scholar
  62. Goyette J, Yan WX, Yamen E, Chung YM, Lim SY, Hsu K, Rahimi F, di Girolamo N, Song C, Jessup W, Kockx M, Bobryshev YV, Freedman SB, Geczy C (2009) Pleiotropic roles of S100A12 in coronary atherosclerotic plaque formation and rupture. J Immunol 183(1):593–603PubMedCrossRefGoogle Scholar
  63. Greenlee KJ, Corry DB, Engler DA, Matsunami RK, Tessier P, Cook RG, Werb Z, Kheradmand F (2006) Proteomic identification of in vivo substrates for matrix metalloproteinases 2 and 9 reveals a mechanism for resolution of inflammation. J Immunol 177:7312–7321PubMedGoogle Scholar
  64. Gribenko AV, Makhatadze GI (1998) Oligomerization and divalent ion binding properties of the S100P protein: a Ca2 +/Mg2 + -switch model. J Mol Biol 283:679–694PubMedCrossRefGoogle Scholar
  65. Grimbaldeston MA, Geczy CL, Tedla N, Finlay-Jones JJ, Hart PH (2003) S100A8 induction in keratinocytes by ultraviolet A irradiation is dependent on reactive oxygen intermediates. J Invest Dermatol 121:1168–1174PubMedCrossRefGoogle Scholar
  66. Guignard F, Mauel J, Markert M (1995) Identification and characterization of a novel human neutrophil protein related to the S100 family. Biochem J 309(Pt 2):395–401PubMedGoogle Scholar
  67. Gurish MF, Austen KF (2001) The diverse roles of mast cells. J Exp Med 194:F1–F5PubMedCrossRefGoogle Scholar
  68. Harrison CA, Raftery MJ, Walsh J, Alewood P, Iismaa SE, Thliveris S, Geczy CL (1999) Oxidation regulates the inflammatory properties of the murine S100 protein S100A8. J Biol Chem 274:8561–8569PubMedCrossRefGoogle Scholar
  69. Hasegawa T, Kosaki A, Kimura T, Matsubara H, Mori Y, Okigaki M, Masaki H, Toyoda N, Inoue-Shibata M, Kimura Y, Nishikawa M, Iwasaka T (2003) The regulation of EN-RAGE (S100A12) gene expression in human THP-1 macrophages. Atherosclerosis 171:211–218PubMedCrossRefGoogle Scholar
  70. Hayashi N, Kido J, Kido R, Wada C, Kataoka M, Shinohara Y, Nagata T (2007) Regulation of calprotectin expression by interleukin-1alpha and transforming growth factor-beta in human gingival keratinocytes. J Periodontal Res 42:1–7PubMedCrossRefGoogle Scholar
  71. Hazell LJ, Stocker R (1993) Oxidation of low-density lipoprotein with hypochlorite causes transformation of the lipoprotein into a high-uptake form for macrophages. Biochem J 290:165–172PubMedGoogle Scholar
  72. Hazell LJ, van den Berg JJ, Stocker R (1994) Oxidation of low-density lipoprotein by hypochlorite causes aggregation that is mediated by modification of lysine residues rather than lipid oxidation. Biochem J 302:297–304PubMedGoogle Scholar
  73. Healy AM, Pickard MD, Pradhan AD, Wang Y, Chen Z, Croce K, Sakuma M, Shi C, Zago AC, Garasic J, Damokosh AI, Dowie TL, Poisson L, Lillie J, Libby P, Ridker PM, Simon DI (2006) Platelet expression profiling and clinical validation of myeloid-related protein-14 as a novel determinant of cardiovascular events. Circulation 113:2278–2284PubMedCrossRefGoogle Scholar
  74. Heizmann CW, Cox JA (1998) New perspectives on S100 proteins: a multi-functional Ca(2 +)-, Zn(2 +)- and Cu(2 +)-binding protein family. Biometals 11:383–397PubMedCrossRefGoogle Scholar
  75. Heizmann CW, Fritz G, Schafer BW (2002) S100 proteins: structure, functions and pathology. Front Biosci 7:d1356–d1368PubMedCrossRefGoogle Scholar
  76. Hermani A, De Servi B, Medunjanin S, Tessier PA, Mayer D (2006) S100A8 and S100A9 activate MAP kinase and NF-kappaB signaling pathways and trigger translocation of RAGE in human prostate cancer cells. Exp Cell Res 312:184–197PubMedCrossRefGoogle Scholar
  77. Hess DT, Matsumoto A, Kim S-O, Marshall HE, Stamler JS (2005) Protein S-nitrosylation: purview and parameters. Nat Rev Mol Cell Biol 6:150–166PubMedCrossRefGoogle Scholar
  78. Hessian PA, Edgeworth J, Hogg N (1993) MRP-8 and MRP-14, two abundant Ca(2 +)-binding proteins of neutrophils and monocytes. J Leukoc Biol 53:197–204PubMedGoogle Scholar
  79. Hessian PA, Wilkinson L, Hogg N (1995) The S100 family protein MRP-14 (S100A9) has homology with the contact domain of high molecular weight kininogen. FEBS Lett 371:271–275PubMedCrossRefGoogle Scholar
  80. Hetland G, Talgo GJ, Fagerhol MK (1998) Chemotaxins C5a and fMLP induce release of calprotectin (leucocyte L1 protein) from polymorphonuclear cells in vitro. Mol Pathol 51:143–148PubMedCrossRefGoogle Scholar
  81. Hiratsuka S, Watanabe A, Aburatani H, Maru Y (2006) Tumour-mediated upregulation of chemoattractants and recruitment of myeloid cells predetermines lung metastasis. Nat Cell Biol 8:1369–1375PubMedCrossRefGoogle Scholar
  82. Hitomi J, Yamaguchi K, Kikuchi Y, Kimura T, Maruyama K, Nagasaki K (1996) A novel calcium-binding protein in amniotic fluid, CAAF1: its molecular cloning and tissue distribution. J Cell Sci 109(Pt 4):805–815PubMedGoogle Scholar
  83. Hitomi J, Kimura T, Kusumi E, Nakagawa S, Kuwabara S, Hatakeyama K, Yamaguchi K (1998) Novel S100 proteins in human esophageal epithelial cells: CAAF1 expression is associated with cell growth arrest. Arch Histol Cytol 61:163–178PubMedCrossRefGoogle Scholar
  84. Hobbs JA, May R, Tanousis K, McNeill E, Mathies M, Gebhardt C, Henderson R, Robinson MJ, Hogg N (2003) Myeloid cell function in MRP-14 (S100A9) null mice. Mol Cell Biol 23:2564–2576PubMedCrossRefGoogle Scholar
  85. Hofmann MA, Drury S, Fu C, Qu W, Taguchi A, Lu Y, Avila C, Kambham N, Bierhaus A, Nawroth P, Neurath MF, Slattery T, Beach D, McClary J, Nagashima M, Morser J, Stern D, Schmidt AM (1999) RAGE mediates a novel proinflammatory axis: a central cell surface receptor for S100/calgranulin polypeptides. Cell 97:889–901PubMedCrossRefGoogle Scholar
  86. Hogg N, Allen C, Edgeworth J (1989) Monoclonal antibody 5.5 reacts with p8, 14, a myeloid molecule associated with some vascular endothelium. Eur J Immunol 19:1053–1061PubMedCrossRefGoogle Scholar
  87. Hsu K, Passey RJ, Endoh Y, Rahimi F, Youssef P, Yen T, Geczy CL (2005) Regulation of S100A8 by glucocorticoids. J Immunol 174:2318–2326PubMedGoogle Scholar
  88. Hu SP, Harrison C, Xu K, Cornish CJ, Geczy CL (1996) Induction of the chemotactic S100 protein, CP-10, in monocyte/macrophages by lipopolysaccharide. Blood 87:3919–3928PubMedGoogle Scholar
  89. Hunter MJ, Chazin WJ (1998) High level expression and dimer characterization of the S100 EF-hand proteins, migration inhibitory factor-related proteins 8 and 14. J Biol Chem 273:12427–12435PubMedCrossRefGoogle Scholar
  90. Ikemoto M, Murayama H, Itoh H, Totani M, Fujita M (2007) Intrinsic function of S100A8/A9 complex as an anti-inflammatory protein in liver injury induced by lipopolysaccharide in rats. Clin Chim Acta 376:197–204PubMedCrossRefGoogle Scholar
  91. Isaksen B, Fagerhol MK (2001) Calprotectin inhibits matrix metalloproteinases by sequestration of zinc. Mol Pathol 54:289–292PubMedCrossRefGoogle Scholar
  92. Ishikawa K, Nakagawa A, Tanaka I, Suzuki M, Nishihira J (2000) The structure of human MRP8, a member of the S100 calcium-binding protein family, by MAD phasing at 1.9 A resolution. Acta Crystallogr D Biol Crystallogr 56:559–566PubMedCrossRefGoogle Scholar
  93. Jaffrey SR, Erdjument-Bromage H, Ferris CD, Tempst P, Snyder SH (2001) Protein S-nitrosylation: a physiological signal for neuronal nitric oxide. Nat Cell Biol 3:193–197PubMedCrossRefGoogle Scholar
  94. Jinquan T, Vorum H, Larsen CG, Madsen P, Rasmussen HH, Gesser B, Etzerodt M, Honore B, Celis JE, Thestrup-Pedersen K (1996) Psoriasin: a novel chemotactic protein. J Invest Dermatol 107:5–10PubMedCrossRefGoogle Scholar
  95. Kerkhoff C, Sorg C, Tandon NN, Nacken W (2001) Interaction of S100A8/S100A9-arachidonic acid complexes with the scavenger receptor CD36 may facilitate fatty acid uptake by endothelial cells. Biochemistry 40:241–248PubMedCrossRefGoogle Scholar
  96. Kerkhoff C, Hofmann HA, Vormoor J, Melkonyan H, Roth J, Sorg C, Klempt M (2002) Binding of two nuclear complexes to a novel regulatory element within the human S100A9 promoter drives the S100A9 gene expression. J Biol Chem 277:41879–41887PubMedCrossRefGoogle Scholar
  97. Kerkhoff C, Nacken W, Benedyk M, Dagher MC, Sopalla C, Doussiere J (2005) The arachidonic acid-binding protein S100A8/A9 promotes NADPH oxidase activation by interaction with p67phox and Rac-2. Faseb J 19:467–469PubMedGoogle Scholar
  98. Kido J, Hayashi N, Kataoka M, Nagata T (2005) Calprotectin expression in human monocytes: induction by porphyromonas gingivalis lipopolysaccharide, tumor necrosis factor-alpha, and interleukin-1beta. J Periodontol 76:437–442PubMedCrossRefGoogle Scholar
  99. Klebanoff SJ (2005) Myeloperoxidase: friend and foe. J Leukoc Biol 77:598–625PubMedCrossRefGoogle Scholar
  100. Kligman D, Hilt DC (1988) The S100 protein family. Trends Biochem Sci 13:437–443PubMedCrossRefGoogle Scholar
  101. Koike T, Harada N, Yoshida T, Morikawa M (1992) Regulation of myeloid-specific calcium binding protein synthesis by cytosolic protein kinase C. J Biochem (Tokyo) 112:624–630Google Scholar
  102. Komada T, Araki R, Nakatani K, Yada I, Naka M, Tanaka T (1996) Novel specific chemtactic receptor for S100L protein on guinea pig eosinophils. Biochem Biophys Res Commun 220:871–874PubMedCrossRefGoogle Scholar
  103. Korndorfer IP, Brueckner F, Skerra A (2007) The crystal structure of the human (S100A8/S100A9)2 heterotetramer, calprotectin, illustrates how conformational changes of interacting alpha-helices can determine specific association of two EF-hand proteins. J Mol Biol 370:887–898PubMedCrossRefGoogle Scholar
  104. Kube E, Becker T, Weber K, Gerke V (1992) Protein–protein interaction studied by site-directed mutagenesis: characterization of the annexin II-binding site on p11, a member of the S100 protein family. J Biol Chem 267:14175–14182PubMedGoogle Scholar
  105. Kumar A, Steinkasserer A, Berchtold S (2003) Interleukin-10 influences the expression of MRP8 and MRP14 in human dendritic cells. Int Arch Allergy Immunol 132:40–47PubMedCrossRefGoogle Scholar
  106. Lackmann M, Cornish CJ, Simpson RJ, Moritz RL, Geczy CL (1992) Purification and structural analysis of a murine chemotactic cytokine (CP-10) with sequence homology to S100 proteins. J Biol Chem 267:7499–7504PubMedGoogle Scholar
  107. Lackmann M, Rajasekariah P, Iismaa SE, Jones G, Cornish CJ, Hu S, Simpson RJ, Moritz RL, Geczy CL (1993) Identification of a chemotactic domain of the pro-inflammatory S100 protein CP-10. J Immunol 150:2981–2991PubMedGoogle Scholar
  108. Lagasse E, Clerc RG (1988) Cloning and expression of two human genes encoding calcium-binding proteins that are regulated during myeloid differentiation. Mol Cell Biol 8:2402–2410PubMedGoogle Scholar
  109. Lau D, Baldus S (2006) Myeloperoxidase and its contributory role in inflammatory vascular disease. Pharmacol Ther 111:16–26PubMedCrossRefGoogle Scholar
  110. Lau W, Devery JM, Geczy CL (1995) A chemotactic S100 peptide enhances scavenger receptor and Mac-1 expression and cholesteryl ester accumulation in murine peritoneal macrophages in vivo. J Clin Invest 95:1957–1965PubMedCrossRefGoogle Scholar
  111. Lazoura E, McLeish MJ, Aguilar MI (2000) Studies on the conformational properties of CP-10(42–55), the hinge region of CP-10, using circular dichroism and RP-HPLC. J Pept Res 55:411–418PubMedCrossRefGoogle Scholar
  112. Leach ST, Yang Z, Messina I, Song C, Geczy CL, Cunningham AM, Day AS (2007) Serum and mucosal S100 proteins, calprotectin (S100A8/S100A9) and S100A12, are elevated at diagnosis in children with inflammatory bowel disease. Scand J Gastroenterol 42:1321–1331PubMedCrossRefGoogle Scholar
  113. Leclerc E, Fritz G, Weibel M, Heizmann CW, Galichet A (2007) S100B and S100A6 differentially modulate cell survival by interacting with distinct RAGE (receptor for advanced glycation end products) immunoglobulin domains. J Biol Chem 282:31317–31331PubMedCrossRefGoogle Scholar
  114. Lee KC, Eckert RL (2007) S100A7 (Psoriasin)–mechanism of antibacterial action in wounds. J Invest Dermatol 127:945–957PubMedCrossRefGoogle Scholar
  115. Li J, Schmidt AM (1997) Characterization and functional analysis of the promoter of RAGE, the receptor for advanced glycation end products. J Biol Chem 272:16498–16506PubMedCrossRefGoogle Scholar
  116. Lim SY, Raftery M, Cai H, Hsu K, Yan WX, Hseih HL, Watts RN, Richardson D, Thomas S, Perry M, Geczy CL (2008) S-nitrosylated S100A8: novel anti-inflammatory properties. J Immunol 181:5627–5636PubMedGoogle Scholar
  117. Lim SY, Raftery MJ, Goyette J, Hsu K and Geczy CL (2009). Oxidative modifications of S100 proteins: functional regulation by redox. J Leukoc BiolGoogle Scholar
  118. Lusitani D, Malawista SE, Montgomery RR (2003) Calprotectin, an abundant cytosolic protein from human polymorphonuclear leukocytes, inhibits the growth of Borrelia burgdorferi. Infect Immun 71:4711–4716PubMedCrossRefGoogle Scholar
  119. Manitz MP, Horst B, Seeliger S, Strey A, Skryabin BV, Gunzer M, Frings W, Schonlau F, Roth J, Sorg C, Nacken W (2003) Loss of S100A9 (MRP14) results in reduced interleukin-8-induced CD11b surface expression, a polarized microfilament system, and diminished responsiveness to chemoattractants in vitro. Mol Cell Biol 23:1034–1043PubMedCrossRefGoogle Scholar
  120. McClintock KA, Shaw GS (2003) A novel S100 target conformation is revealed by the solution structure of the Ca2 + –S100B–TRTK-12 complex. J Biol Chem 278:6251–6257PubMedCrossRefGoogle Scholar
  121. McCormick MM, Rahimi F, Bobryshev YV, Gaus K, Zreiqat H, Cai H, Lord RS, Geczy CL (2005) S100A8 and S100A9 in human arterial wall. Implications for atherogenesis. J Biol Chem 280:41521–41529PubMedCrossRefGoogle Scholar
  122. McNeill E, Conway SJ, Roderick HL, Bootman MD, Hogg N (2007) Defective chemoattractant-induced calcium signalling in S100A9 null neutrophils. Cell Calcium 41:107–121PubMedCrossRefGoogle Scholar
  123. Mikkelsen SE, Novitskaya V, Kriajevska M, Berezin V, Bock E, Norrild B, Lukanidin E (2001) S100A12 protein is a strong inducer of neurite outgrowth from primary hippocampal neurons. J Neurochem 79:767–776PubMedCrossRefGoogle Scholar
  124. Miranda LP, Tao T, Jones A, Chernushevich I, Standing KG, Geczy CL, Alewood PF (2001) Total chemical synthesis and chemotactic activity of human S100A12 (EN-RAGE). FEBS Lett 488:85–90PubMedCrossRefGoogle Scholar
  125. Mirmohammadsadegh A, Tschakarjan E, Ljoljic A, Bohner K, Michel G, Ruzicka T, Goos M, Hengge UR (2000) Calgranulin C is overexpressed in lesional psoriasis. J Invest Dermatol 114:1207–1208PubMedCrossRefGoogle Scholar
  126. Mogensen TH (2009). Pathogen recognition and inflammatory signaling in innate immune defenses. Clin Microbiol Rev 22:240–273 (table of contents)Google Scholar
  127. Mork G, Schjerven H, Mangschau L, Soyland E, Brandtzaeg P (2003) Proinflammatory cytokines upregulate expression of calprotectin (L1 protein, MRP-8/MRP-14) in cultured human keratinocytes. Br J Dermatol 149:484–491PubMedCrossRefGoogle Scholar
  128. Moroz OV, Burkitt W, Wittkowski H, He W, Ianoul A, Novitskaya V, Xie J, Polyakova O, Lednev IK, Shekhtman A, Derrick PJ, Bjoerk P, Foell D, Bronstein IB (2009) Both Ca2 + and Zn2 + are essential for S100A12 protein -oligomerization and function. BMC Biochem 10:11PubMedCrossRefGoogle Scholar
  129. Murthy AR, Lehrer RI, Harwig SS, Miyasaki KT (1993) In vitro candidastatic properties of the human neutrophil calprotectin complex. J Immunol 151:6291–6301PubMedGoogle Scholar
  130. Nacken W, Roth J, Sorg C, Kerkhoff C (2003) S100A9/S100A8: myeloid representatives of the S100 protein family as prominent players in innate immunity. Microsc Res Tech 60:569–580PubMedCrossRefGoogle Scholar
  131. Nacken W, Mooren FC, Manitz MP, Bode G, Sorg C, Kerkhoff C (2005) S100A9 deficiency alters adenosine-5′******-triphosphate induced calcium signalling but does not generally interfere with calcium and zinc homeostasis in murine neutrophils. Int J Biochem Cell Biol 37:1241–1253PubMedCrossRefGoogle Scholar
  132. Newton RA, Hogg N (1998) The human S100 protein MRP-14 is a novel activator of the beta 2 integrin Mac-1 on neutrophils. J Immunol 160:1427–1435PubMedGoogle Scholar
  133. Nicholls SJ, Hazen SL (2005) Myeloperoxidase and cardiovascular disease. Arterioscler Thromb Vasc Biol 25:1102–1111PubMedCrossRefGoogle Scholar
  134. Nishimura F, Terranova VP, Sawa T, Murayama Y (1999) Migration inhibitory factor related protein-8 (MRP-8) is an autocrine chemotactic factor for periodontal ligament cells. J Dent Res 78:1251–1255PubMedCrossRefGoogle Scholar
  135. Odink K, Cerletti N, Bruggen J, Clerc RG, Tarcsay L, Zwadlo G, Gerhards G, Schlegel R, Sorg C (1987) Two calcium-binding proteins in infiltrate macrophages of rheumatoid arthritis. Nature 330:80–82PubMedCrossRefGoogle Scholar
  136. Orlova VV, Choi EY, Xie C, Chavakis E, Bierhaus A, Ihanus E, Ballantyne CM, Gahmberg CG, Bianchi ME, Nawroth PP, Chavakis T (2007) A novel pathway of HMGB1-mediated inflammatory cell recruitment that requires Mac-1-integrin. EMBO J 26:1129–1139PubMedCrossRefGoogle Scholar
  137. Otsuka K, Terasaki F, Ikemoto M, Fujita S, Tsukada B, Katashima T, Kanzaki Y, Sohmiya K, Kono T, Toko H, Fujita M, Kitaura Y (2009) Suppression of inflammation in rat autoimmune myocarditis by S100A8/A9 through modulation of the proinflammatory cytokine network. Eur J Heart Fail 11:229–237PubMedCrossRefGoogle Scholar
  138. Paccola CC, Gutierrez VP, Longo I, Juliano L, Juliano MA, Giorgi R (2008) Antinociceptive effect of the C-terminus of murine S100A9 protein on experimental neuropathic pain. Peptides 29:1806–1814PubMedCrossRefGoogle Scholar
  139. Pagano RL, Dias MA, Dale CS, Giorgi R (2002) Neutrophils and the calcium-binding protein MRP-14 mediate carrageenan-induced antinociception in mice. Mediators Inflamm 11:203–210PubMedCrossRefGoogle Scholar
  140. Pagano RL, Sampaio SC, Juliano L, Juliano MA, Giorgi R (2005) The C-terminus of murine S100A9 inhibits spreading and phagocytic activity of adherent peritoneal cells. Inflamm Res 54:204–210PubMedCrossRefGoogle Scholar
  141. Pagano RL, Mariano M, Giorgi R (2006) Neutrophilic cell-free exudate induces antinociception mediated by the protein S100A9. Mediators Inflamm 2006:36765PubMedCrossRefGoogle Scholar
  142. Pascual G, Glass CK (2006) Nuclear receptors versus inflammation: mechanisms of transrepression. Trends Endocrinol Metab 17:321–327PubMedCrossRefGoogle Scholar
  143. Passey RJ, Williams E, Lichanska AM, Wells C, Hu S, Geczy CL, Little MH, Hume DA (1999) A null mutation in the inflammation-associated S100 protein S100A8 causes early resorption of the mouse embryo. J Immunol 163:2209–2216PubMedGoogle Scholar
  144. Perez-Mato I, Castro C, Ruiz FA, Corrales FJ, Mato JM (1999) Methionine adenosyltransferase S-nitrosylation is regulated by the basic and acidic amino acids surrounding the target thiol. J Biol Chem 274:17075–17079PubMedCrossRefGoogle Scholar
  145. Petri B, Bixel MG (2006) Molecular events during leukocyte diapedesis. FEBS J 273:4399–4407PubMedCrossRefGoogle Scholar
  146. Petri B, Phillipson M, Kubes P (2008) The physiology of leukocyte recruitment: an in vivo perspective. J Immunol 180:6439–6446PubMedGoogle Scholar
  147. Petty HR, Kindzelskii AL, Adachi Y, Todd RF 3rd (1997) Ectodomain interactions of leukocyte integrins and pro-inflammatory GPI-linked membrane proteins. J Pharm Biomed Anal 15:1405–1416PubMedCrossRefGoogle Scholar
  148. Petty HR, Worth RG, Todd RF 3rd (2002) Interactions of integrins with their partner proteins in leukocyte membranes. Immunol Res 25:75–95PubMedCrossRefGoogle Scholar
  149. Propper C, Huang X, Roth J, Sorg C, 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 274:183–188PubMedCrossRefGoogle Scholar
  150. Raftery MJ, Geczy CL (2002) Electrospray low energy CID and MALDI PSD fragmentations of protonated sulfinamide cross-linked peptides. J Am Soc Mass Spectrom 13:709–718PubMedCrossRefGoogle Scholar
  151. Raftery MJ, Yang Z, Valenzuela SM, Geczy CL (2001) Novel intra- and inter-molecular sulfinamide bonds in S100A8 produced by hypochlorite oxidation. J Biol Chem 276:33393–33401PubMedCrossRefGoogle Scholar
  152. Rahimi F, Hsu K, Endoh Y, Geczy CL (2005) FGF-2, IL-1beta and TGF-beta regulate fibroblast expression of S100A8. Febs J 272:2811–2827PubMedCrossRefGoogle Scholar
  153. Rammes A, Roth J, Goebeler M, Klempt M, Hartmann M, 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 272:9496–9502PubMedCrossRefGoogle Scholar
  154. Raptis SZ, Pham CT (2005) Neutrophil-derived serine proteases in immune complex-mediated diseases. Immunol Res 32:211–215PubMedCrossRefGoogle Scholar
  155. Ravasi T, Hsu K, Goyette J, Schroder K, Yang Z, Rahimi F, Miranda LP, Alewood PF, Hume DA, Geczy C (2004) Probing the S100 protein family through genomic and functional analysis. Genomics 84:10–22PubMedCrossRefGoogle Scholar
  156. Reed RC, Berwin B, Baker JP, Nicchitta CV (2003) GRP94/gp96 elicits ERK activation in murine macrophages. A role for endotoxin contamination in NF-kappa B activation and nitric oxide production. J Biol Chem 278:31853–31860PubMedCrossRefGoogle Scholar
  157. Robinson MJ, Hogg N (2000) A comparison of human S100A12 with MRP-14 (S100A9). Biochem Biophys Res Commun 275:865–870PubMedCrossRefGoogle Scholar
  158. Robinson MJ, Tessier P, Poulsom R, Hogg N (2002) The S100 family heterodimer, MRP-8/14, binds with high affinity to heparin and heparan sulfate glycosaminoglycans on endothelial cells. J Biol Chem 277:3658–3665PubMedCrossRefGoogle Scholar
  159. Roth J, Vogl T, Sorg C, Sunderkotter C (2003) Phagocyte-specific S100 proteins: a novel group of proinflammatory molecules. Trends Immunol 24:155–158PubMedCrossRefGoogle Scholar
  160. Rouleau P, Vandal K, Ryckman C, Poubelle PE, Boivin A, Talbot M, Tessier PA (2003) 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 107:46–54PubMedCrossRefGoogle Scholar
  161. Ryckman C, McColl SR, Vandal K, de Medicis R, Lussier A, Poubelle PE, Tessier PA (2003a) Role of S100A8 and S100A9 in neutrophil recruitment in response to monosodium urate monohydrate crystals in the air-pouch model of acute gouty arthritis. Arthritis Rheum 48:2310–2320PubMedCrossRefGoogle Scholar
  162. Ryckman C, Vandal K, Rouleau P, Talbot M, Tessier PA (2003b) Proinflammatory activities of S100: proteins S100A8, S100A9, and S100A8/A9 induce neutrophil chemotaxis and adhesion. J Immunol 170:3233–3242PubMedGoogle Scholar
  163. Ryckman C, Gilbert C, de Medicis R, Lussier A, Vandal K, Tessier PA (2004) Monosodium urate monohydrate crystals induce the release of the proinflammatory protein S100A8/A9 from neutrophils. J Leukoc Biol 76:433–440PubMedCrossRefGoogle Scholar
  164. Sakaguchi T, Yan SF, Yan SD, Belov D, Rong LL, Sousa M, Andrassy M, Marso SP, Duda S, Arnold B, Liliensiek B, Nawroth PP, Stern DM, Schmidt AM, Naka Y (2003) Central role of RAGE-dependent neointimal expansion in arterial restenosis. J Clin Invest 111:959–972PubMedGoogle Scholar
  165. Salama I, Malone PS, Mihaimeed F, Jones JL (2008) A review of the S100 proteins in cancer. Eur J Surg Oncol 34:357–364PubMedGoogle Scholar
  166. Santhanagopalan V, Hahn BL, Sohnle PG (1995) Resistance of zinc-supplemented Candida albicans cells to the growth inhibitory effect of calprotectin. J Infect Dis 171:1289–1294PubMedCrossRefGoogle Scholar
  167. Schafer BW, Heizmann CW (1996) The S100 family of EF-hand calcium-binding proteins: functions and pathology. Trends Biochem Sci 21:134–140PubMedGoogle Scholar
  168. Schmidt AM, Yan SD, Yan SF, Stern DM (2001) The multiligand receptor RAGE as a progression factor amplifying immune and inflammatory responses. J Clin Invest 108:949–955PubMedGoogle Scholar
  169. Schnekenburger J, Schick V, Kruger B, Manitz MP, Sorg C, Nacken W, Kerkhoff C, Kahlert A, Mayerle J, Domschke W, Lerch MM (2008) The calcium binding protein S100A9 is essential for pancreatic leukocyte infiltration and induces disruption of cell–cell contacts. J Cell Physiol 216:558–567PubMedCrossRefGoogle Scholar
  170. Seemann J, Weber K, Gerke V (1996) Structural requirements for annexin I-S100C complex-formation. Biochem J 319(Pt 1):123–129PubMedGoogle Scholar
  171. Sellmayer A, Krane SM, Ouellette AJ, Bonventre JV (1992) 1 alpha, 25-(OH)2 vitamin D3 enhances expression of the genes encoding Ca(2 +)-binding proteins MRP-8 and MRP-14. Am J Physiol 262:C235–C242PubMedGoogle Scholar
  172. Shepherd CE, Goyette J, Utter V, Rahimi F, Yang Z, Geczy CL, Halliday GM (2006) Inflammatory S100A9 and S100A12 proteins in Alzheimer’s disease. Neurobiol Aging 27:1554–1563PubMedCrossRefGoogle Scholar
  173. Shibata F, Miyama K, Shinoda F, Mizumoto J, Takano K, Nakagawa H (2004) Fibroblast growth-stimulating activity of S100A9 (MRP-14). Eur J Biochem 271:2137–2143PubMedCrossRefGoogle Scholar
  174. Shibata F, Ito A, Ohkuma Y, Mitsui K (2005) Mitogenic activity of S100A9 (MRP-14). Biol Pharm Bull 28:2312–2314PubMedCrossRefGoogle Scholar
  175. Smith SP, Shaw GS (1998) A change-in-hand mechanism for S100 signalling. Biochem Cell Biol 76:324–333PubMedCrossRefGoogle Scholar
  176. Sohnle PG, Hunter MJ, Hahn B, Chazin WJ (2000) Zinc-reversible antimicrobial activity of recombinant calprotectin (migration inhibitory factor-related proteins 8 and 14). J Infect Dis 182:1272–1275PubMedCrossRefGoogle Scholar
  177. Sorci G, Riuzzi F, Agneletti AL, Marchetti C, Donato R (2003) S100B inhibits myogenic differentiation and myotube formation in a RAGE-independent manner. Mol Cell Biol 23:4870–4881PubMedCrossRefGoogle Scholar
  178. Sorci G, Riuzzi F, Agneletti AL, Marchetti C, Donato R (2004) S100B causes apoptosis in a myoblast cell line in a RAGE-independent manner. J Cell Physiol 199:274–283PubMedCrossRefGoogle Scholar
  179. Sperandio M (2006) Selectins and glycosyltransferases in leukocyte rolling in vivo. FEBS J 273:4377–4389PubMedCrossRefGoogle Scholar
  180. Srikrishna G, Panneerselvam K, Westphal V, Abraham V, Varki A, Freeze HH (2001) Two proteins modulating transendothelial migration of leukocytes recognize novel carboxylated glycans on endothelial cells. J Immunol 166:4678–4688PubMedGoogle Scholar
  181. Sroussi HY, Berline J, Dazin P, Green P, Palefsky JM (2006) S100A8 triggers oxidation-sensitive repulsion of neutrophils. J Dent Res 85:829–833PubMedCrossRefGoogle Scholar
  182. Sroussi HY, Berline J, Palefsky JM (2007) Oxidation of methionine 63 and 83 regulates the effect of S100A9 on the migration of neutrophils in vitro. J Leukoc Biol 81:818–824PubMedCrossRefGoogle Scholar
  183. Sroussi HY, Kohler GA, Agabian N, Villines D, Palefsky JM (2009) Substitution of methionine 63 or 83 in S100A9 and cysteine 42 in S100A8 abrogate the antifungal activities of S100A8/A9: potential role for oxidative regulation. FEMS Immunol Med Microbiol 55:55–61PubMedCrossRefGoogle Scholar
  184. Steinbakk M, Naess-Andresen CF, Lingaas E, Dale I, Brandtzaeg P, Fagerhol MK (1990) Antimicrobial actions of calcium binding leucocyte L1 protein, calprotectin. Lancet 336:763–765PubMedCrossRefGoogle Scholar
  185. Sunahori K, Yamamura M, Yamana J, Takasugi K, Kawashima M, Yamamoto H, Chazin WJ, Nakatani Y, Yui S, Makino H (2006) The S100A8/A9 heterodimer amplifies proinflammatory cytokine production by macrophages via activation of nuclear factor kappa B and p38 mitogen-activated protein kinase in rheumatoid arthritis. Arthritis Res Ther 8:R69PubMedCrossRefGoogle Scholar
  186. Suryono Kido J, Hayashi N, Kataoka M, Shinohara Y, Nagata T (2006) Norepinephrine stimulates calprotectin expression in human monocytic cells. J Periodontal Res 41:159–164PubMedCrossRefGoogle Scholar
  187. Terasaki F, Fujita M, Shimomura H, Tsukada B, Otsuka K, Katashima T, Ikemoto M, Kitaura Y (2007) Enhanced expression of myeloid-related protein complex (MRP8/14) in macrophages and multinucleated giant cells in granulomas of patients with active cardiac sarcoidosis. Circ J 71:1545–1550PubMedCrossRefGoogle Scholar
  188. Test S, Weiss SJ (1986) The generation and utilization of chlorinated oxidants by human neutrophils. Adv Free Radic Biol Med 2:91–116CrossRefGoogle Scholar
  189. Thorey IS, Roth J, Regenbogen J, Halle JP, Bittner M, Vogl T, Kaesler S, Bugnon P, Reitmaier B, Durka S, Graf A, Wockner M, Rieger N, Konstantinow A, Wolf E, Goppelt A, Werner S (2001) The Ca2 + -binding proteins S100A8 and S100A9 are encoded by novel injury-regulated genes. J Biol Chem 276:35818–35825PubMedCrossRefGoogle Scholar
  190. Tian J, Avalos AM, Mao SY, Chen B, Senthil K, Wu H, Parroche P, Drabic S, Golenbock D, Sirois C, Hua J, An LL, Audoly L, La Rosa G, Bierhaus A, Naworth P, Marshak-Rothstein A, Crow MK, Fitzgerald KA, Latz E, Kiener PA, Coyle AJ (2007) Toll-like receptor 9-dependent activation by DNA-containing immune complexes is mediated by HMGB1 and RAGE. Nat Immunol 8:487–496PubMedCrossRefGoogle Scholar
  191. Todd RF 3rd, Petty HR (1997) Beta 2 (CD11/CD18) integrins can serve as signaling partners for other leukocyte receptors. J Lab Clin Med 129:492–498PubMedCrossRefGoogle Scholar
  192. Tsan MF, Gao B (2004) Endogenous ligands of Toll-like receptors. J Leukoc Biol 76:514–519PubMedCrossRefGoogle Scholar
  193. Turovskaya O, Foell D, Sinha P, Vogl T, Newlin R, Nayak J, Nguyen M, Olsson A, Nawroth PP, Bierhaus A, Varki N, Kronenberg M, Freeze HH, Srikrishna G (2008) RAGE, carboxylated glycans and S100A8/A9 play essential roles in colitis-associated carcinogenesis. Carcinogenesis 29:2035–2043PubMedCrossRefGoogle Scholar
  194. van Lent PL, Grevers L, Blom AB, Sloetjes A, Mort JS, Vogl T, Nacken W, van den Berg WB and Roth J (2007) Myeloid related proteins S100A8/S100A9 regulate joint inflammation and cartilage destruction during antigen-induced arthritis. Ann Rheum DisGoogle Scholar
  195. Vandal K, Rouleau P, Boivin A, Ryckman C, Talbot M, Tessier PA (2003) Blockade of S100A8 and S100A9 suppresses neutrophil migration in response to lipopolysaccharide. J Immunol 171:2602–2609PubMedGoogle Scholar
  196. Viemann D, Strey A, Janning A, Jurk K, Klimmek K, Vogl T, Hirono K, Ichida F, Foell D, Kehrel B, Gerke V, Sorg C, Roth J (2005) Myeloid-related proteins 8 and 14 induce a specific inflammatory response in human microvascular endothelial cells. Blood 105:2955–2962PubMedCrossRefGoogle Scholar
  197. Viemann D, Barczyk K, Vogl T, Fischer U, Sunderkotter C, Schulze-Osthoff K, Roth J (2007) MRP8/MRP14 impairs endothelial integrity and induces a caspase-dependent and -independent cell death program. Blood 109:2453–2460PubMedCrossRefGoogle Scholar
  198. Voganatsi A, Panyutich A, Miyasaki KT, Murthy RK (2001) Mechanism of extracellular release of human neutrophil calprotectin complex. J Leukoc Biol 70:130–134PubMedGoogle Scholar
  199. Vogl T, Propper C, Hartmann M, Strey A, Strupat K, van den Bos C, Sorg C, Roth J (1999a) S100A12 is expressed exclusively by granulocytes and acts independently from MRP8 and MRP14. J Biol Chem 274:25291–25296PubMedCrossRefGoogle Scholar
  200. Vogl T, Roth J, Sorg C, Hillenkamp F, Strupat K (1999b) Calcium-induced noncovalently linked tetramers of MRP8 and MRP14 detected by ultraviolet matrix-assisted laser desorption/ionization mass spectrometry. J Am Soc Mass Spectrom 10:1124–1130PubMedCrossRefGoogle Scholar
  201. Vogl T, Ludwig S, Goebeler M, Strey A, Thorey IS, Reichelt R, Foell D, Gerke V, Manitz MP, Nacken W, Werner S, Sorg C, Roth J (2004) MRP8 and MRP14 control microtubule reorganization during transendothelial migration of phagocytes. Blood 104:4260–4268PubMedCrossRefGoogle Scholar
  202. Vogl T, Leukert N, Barczyk K, Strupat K, Roth J (2006) Biophysical characterization of S100A8 and S100A9 in the absence and presence of bivalent cations. Biochim Biophys Acta 1763:1298–1306PubMedCrossRefGoogle Scholar
  203. Vogl T, Tenbrock K, Ludwig S, Leukert N, Ehrhardt C, van Zoelen MA, Nacken W, Foell D, van der Poll T, Sorg C, Roth J (2007) Mrp8 and Mrp14 are endogenous activators of Toll-like receptor 4, promoting lethal, endotoxin-induced shock. Nat Med 13:1042–1049PubMedCrossRefGoogle Scholar
  204. Wilckens T (1995) Glucocorticoids and immune function: physiological relevance and pathogenic potential of hormonal dysfunction. Trends Pharmacol Sci 16:193–197PubMedCrossRefGoogle Scholar
  205. Wolf R, Howard OM, Dong HF, Voscopoulos C, Boeshans K, Winston J, Divi R, Gunsior M, Goldsmith P, Ahvazi B, Chavakis T, Oppenheim JJ, Yuspa SH (2008) Chemotactic activity of S100A7 (Psoriasin) is mediated by the receptor for advanced glycation end products and potentiates inflammation with highly homologous but functionally distinct S100A15. J Immunol 181:1499–1506PubMedGoogle Scholar
  206. Wu N, Davidson JM (2004) Migration inhibitory factor-related protein (MRP)8 and MRP14 are differentially expressed in free-electron laser and scalpel incisions. Wound Repair Regen 12:327–336PubMedCrossRefGoogle Scholar
  207. Xie J, Burz DS, He W, Bronstein IB, Lednev I, Shekhtman A (2007) Hexameric calgranulin C (S100A12) binds to the receptor for advanced glycated end products (RAGE) using symmetric hydrophobic target-binding patches. J Biol Chem 282:4218–4231PubMedCrossRefGoogle Scholar
  208. Xu K, Geczy CL (2000) IFN-gamma and TNF regulate macrophage expression of the chemotactic S100 protein S100A8. J Immunol 164:4916–4923PubMedGoogle Scholar
  209. Xu K, Yen T, Geczy CL (2001) Il-10 up-regulates macrophage expression of the S100 protein S100A8. J Immunol 166:6358–6366PubMedGoogle Scholar
  210. Yan WX, Armishaw C, Goyette J, Yang Z, Cai H, Alewood P, Geczy CL (2008) Mast cell and monocyte recruitment by S100A12 and its hinge domain. J Biol Chem 283:13035–13043PubMedCrossRefGoogle Scholar
  211. Yanamandra K, Alexeyev O, Zamotin V, Srivastava V, Shchukarev A, Brorsson AC, Tartaglia GG, Vogl T, Kayed R, Wingsle G, Olsson J, Dobson CM, Bergh A, Elgh F, Morozova-Roche LA (2009) Amyloid formation by the pro-inflammatory S100A8/A9 proteins in the ageing prostate. PLoS ONE 4:e5562PubMedCrossRefGoogle Scholar
  212. Yang Z, Tao T, Raftery MJ, Youssef P, Di Girolamo N, Geczy CL (2001) Proinflammatory properties of the human S100 protein S100A12. J Leukoc Biol 69:986–994PubMedGoogle Scholar
  213. Yang Z, Yan WX, Cai H, Tedla N, Armishaw C, Di Girolamo N, Wang HW, Hampartzoumian T, Simpson JL, Gibson PG, Hunt J, Hart P, Hughes JM, Perry MA, Alewood PF, Geczy CL (2007) S100A12 provokes mast cell activation: a potential amplification pathway in asthma and innate immunity. J Allergy Clin Immunol 119:106–114PubMedCrossRefGoogle Scholar
  214. Yen T, Harrison CA, Devery JM, Leong S, Iismaa SE, Yoshimura T, Geczy CL (1997) Induction of the S100 chemotactic protein, CP-10, in murine microvascular endothelial cells by proinflammatory stimuli. Blood 90:4812–4821PubMedGoogle Scholar
  215. Yong HY, Moon A (2007) Roles of calcium-binding proteins, S100A8 and S100A9, in invasive phenotype of human gastric cancer cells. Arch Pharm Res 30:75–81PubMedCrossRefGoogle Scholar
  216. Yui S, Mikami M, Yamazaki M (1995) Purification and characterization of the cytotoxic factor in rat peritoneal exudate cells: its identification as the calcium binding protein complex, calprotectin. J Leukoc Biol 58:307–316PubMedGoogle Scholar
  217. Yui S, Mikami M, Tsurumaki K, Yamazaki M (1997) Growth-inhibitory and apoptosis-inducing activities of calprotectin derived from inflammatory exudate cells on normal fibroblasts: regulation by metal ions. J Leukoc Biol 61:50–57PubMedGoogle Scholar
  218. Yui S, Nakatani Y, Hunter MJ, Chazin WJ, Yamazaki M (2002) Implication of extracellular zinc exclusion by recombinant human calprotectin (MRP8 and MRP14) from target cells in its apoptosis-inducing activity. Mediators Inflamm 11:165–172PubMedCrossRefGoogle Scholar
  219. Zimmer DB, Wright Sadosky P, Weber DJ (2003) Molecular mechanisms of S100–target protein interactions. Microsc Res Tech 60:552–559PubMedCrossRefGoogle Scholar
  220. Zreiqat H, Howlett CR, Gronthos S, Hume D, Geczy CL (2007) S100A8/S100A9 and their association with cartilage and bone. J Mol Histol 38:381–391PubMedCrossRefGoogle Scholar
  221. Zwadlo G, Bruggen J, Gerhards G, Schlegel R, Sorg C (1988) Two calcium-binding proteins associated with specific stages of myeloid cell differentiation are expressed by subsets of macrophages in inflammatory tissues. Clin Exp Immunol 72:510–515PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  1. 1.Centre for Infection and Inflammation Research, School of Medical SciencesUniversity of New South WalesSydneyAustralia

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