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Published in: World Journal of Pediatrics 4/2018

01-08-2018 | Review Article

Multifarious diagnostic possibilities of the S100 protein family: predominantly in pediatrics and neonatology

Authors: Anna Medkova, Josef Srovnal, Jarmila Potomkova, Jana Volejnikova, Vladimir Mihal

Published in: World Journal of Pediatrics | Issue 4/2018

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Abstract

Background

Numerous articles related to S100 proteins have been recently published. This review aims to introduce this large protein family and its importance in the diagnostics of many pathological conditions in children and adults.

Data sources

Based on original publications found in database systems, we summarize the current knowledge about the S100 protein group and highlight the most important proteins with focus on pediatric use.

Results

The S100 family is composed of Ca2+ and Zn2+ binding proteins, which are present only in vertebrates. Some of these proteins can be used as diagnostic markers in cardiology (S100A1, S100A12), oncology (S100A2, S100A5, S100A6, S100A14, S100A16, S100P, S100B), neurology (S100B), rheumatology (S100A8/A9, S100A4, S100A6, and S100A12), nephrology and infections (S100A8, S100A9, S100A8/A9, S100A12). The most useful S100 proteins in pediatrics are S100A8, S100A9, heterodimers S100A8/A9, S100B and S100A12.

Conclusions

The S100 family members are promising biomarkers and provide numerous possibilities for implementation into clinical practice to optimize the differential diagnostic process.
Literature
1.
go back to reference Schäfer BW, Heizmann CW. The S100 family of EF-hand calcium-binding proteins: functions and pathology. Trends Biochem Sci. 1996;21:134–40.CrossRefPubMed Schäfer BW, Heizmann CW. The S100 family of EF-hand calcium-binding proteins: functions and pathology. Trends Biochem Sci. 1996;21:134–40.CrossRefPubMed
2.
go back to reference Donato R. Intracellular and extracellular roles of S100 proteins. Microsc Res Tech. 2003;60:540–51.CrossRefPubMed Donato R. Intracellular and extracellular roles of S100 proteins. Microsc Res Tech. 2003;60:540–51.CrossRefPubMed
3.
go back to reference Baudier J, Glasser N, Gerard D. Ions binding to S100 proteins. I. Calcium- and zinc-binding properties of bovine brain S100αα, S100a (αβ), and S100b (ββ) protein: Zn2+ regulates Ca2+ binding on S100b protein. J Biol Chem. 1986;261:8192–203.PubMed Baudier J, Glasser N, Gerard D. Ions binding to S100 proteins. I. Calcium- and zinc-binding properties of bovine brain S100αα, S100a (αβ), and S100b (ββ) protein: Zn2+ regulates Ca2+ binding on S100b protein. J Biol Chem. 1986;261:8192–203.PubMed
5.
go back to reference Moore B. A soluble protein characteristic of the nervous system. Biochem Biophys Res Commun. 1965;19:739–44.CrossRefPubMed Moore B. A soluble protein characteristic of the nervous system. Biochem Biophys Res Commun. 1965;19:739–44.CrossRefPubMed
7.
go back to reference Li F, Men X, Zhang W. S100 protein in breast tumor. Indian J Cancer. 2014;51:67–71.CrossRef Li F, Men X, Zhang W. S100 protein in breast tumor. Indian J Cancer. 2014;51:67–71.CrossRef
8.
go back to reference Donato R. S100: a multigenic family of calcium-modulated proteins of the EF-hand type with intracellular and extracellular functional roles. Int J Biochem Cell Biol. 2001;33:637–68.CrossRefPubMed Donato R. S100: a multigenic family of calcium-modulated proteins of the EF-hand type with intracellular and extracellular functional roles. Int J Biochem Cell Biol. 2001;33:637–68.CrossRefPubMed
11.
go back to reference Boteanu RM, Suica VI, Uyy E, Ivan L, Dima SO, Popescu I, et al. Alarmins in chronic noncommunicable diseases: atherosclerosis, diabetes and cancer. J Proteom. 2016;153:21–9.CrossRef Boteanu RM, Suica VI, Uyy E, Ivan L, Dima SO, Popescu I, et al. Alarmins in chronic noncommunicable diseases: atherosclerosis, diabetes and cancer. J Proteom. 2016;153:21–9.CrossRef
12.
go back to reference Dmytriyeva O, Pankratova O, Owczarek S, Sonn K, Soroka V, Ridley CM, et al. The metastasis-promoting S100A4 protein confers neuroprotection in brain injury. Nat Commun. 2012;3:1197.CrossRefPubMed Dmytriyeva O, Pankratova O, Owczarek S, Sonn K, Soroka V, Ridley CM, et al. The metastasis-promoting S100A4 protein confers neuroprotection in brain injury. Nat Commun. 2012;3:1197.CrossRefPubMed
13.
go back to reference Willoughby KA, Kleindienst A, Müller C, Chen T, Muir JK, Ellis EF. S100B protein is released by in vitro trauma and reduces delayed neuronal injury. J Neurochem. 2004;91:1284–91.CrossRefPubMed Willoughby KA, Kleindienst A, Müller C, Chen T, Muir JK, Ellis EF. S100B protein is released by in vitro trauma and reduces delayed neuronal injury. J Neurochem. 2004;91:1284–91.CrossRefPubMed
14.
go back to reference Ellis EF, Willoughby KA, Sparks SA, Chen T. S100B protein is released from rat neonatal neurons, astrocytes, and microglia by in vitro trauma and anti-S100 increases trauma-induced delayed neuronal injury and negates the protective effect of exogenous S100B on neurons. J Neurochem. 2007;101:1463–70.CrossRefPubMed Ellis EF, Willoughby KA, Sparks SA, Chen T. S100B protein is released from rat neonatal neurons, astrocytes, and microglia by in vitro trauma and anti-S100 increases trauma-induced delayed neuronal injury and negates the protective effect of exogenous S100B on neurons. J Neurochem. 2007;101:1463–70.CrossRefPubMed
15.
go back to reference Sorci G, Giovannini G, Riuzzi F, Bonifazi P, Zelante T, Zagarella S, et al. The danger signal S100B integrates pathogen- and danger-sensing pathways to restrain inflammation. PLoS Pathog. 2011;7:e1001315.CrossRefPubMedPubMedCentral Sorci G, Giovannini G, Riuzzi F, Bonifazi P, Zelante T, Zagarella S, et al. The danger signal S100B integrates pathogen- and danger-sensing pathways to restrain inflammation. PLoS Pathog. 2011;7:e1001315.CrossRefPubMedPubMedCentral
16.
go back to reference Zhao J, Endoh I, Hsu K, Tedla N, Endoh Y, Geczy CL. S100A8 modulates mast cell function and suppresses eosinophil migration in acute asthma. Antioxid Redox Signal. 2011;14:1589–600.CrossRefPubMed Zhao J, Endoh I, Hsu K, Tedla N, Endoh Y, Geczy CL. S100A8 modulates mast cell function and suppresses eosinophil migration in acute asthma. Antioxid Redox Signal. 2011;14:1589–600.CrossRefPubMed
17.
go back to reference Caldwell RL, Opalenik SR, Davidson JM, Caprioli RM, Nanney LB. Tissue profiling MALDI mass spectrometry reveals prominent calcium-binding proteins in the proteome of regenerative MRL mouse wounds. Wound Repair Regen. 2008;16:442–9.CrossRefPubMedPubMedCentral Caldwell RL, Opalenik SR, Davidson JM, Caprioli RM, Nanney LB. Tissue profiling MALDI mass spectrometry reveals prominent calcium-binding proteins in the proteome of regenerative MRL mouse wounds. Wound Repair Regen. 2008;16:442–9.CrossRefPubMedPubMedCentral
18.
go back to reference Sroussi HY, Williams RL, Zhang QL, Villines D, Marucha PT. Ala42S100A8 ameliorates psychological-stress impaired cutaneous wound healing. Brain Behav Immun. 2009;23:755–9.CrossRefPubMedPubMedCentral Sroussi HY, Williams RL, Zhang QL, Villines D, Marucha PT. Ala42S100A8 ameliorates psychological-stress impaired cutaneous wound healing. Brain Behav Immun. 2009;23:755–9.CrossRefPubMedPubMedCentral
19.
go back to reference Anderberg SB, Luther T, Frithiof R. Physiological aspects of Toll-like receptor 4 activation in sepsis-induced acute kidney injury. Acta Physiol (Oxf). 2017;219:573–88.CrossRefPubMed Anderberg SB, Luther T, Frithiof R. Physiological aspects of Toll-like receptor 4 activation in sepsis-induced acute kidney injury. Acta Physiol (Oxf). 2017;219:573–88.CrossRefPubMed
20.
go back to reference Farina C, Theil D, Semlinger B, Hohlfeld R, Meinl E. Distinct responses to monocytes to Toll-like receptor ligands and inflammatory cytokines. Int Immunol. 2004;16:799–809.CrossRefPubMed Farina C, Theil D, Semlinger B, Hohlfeld R, Meinl E. Distinct responses to monocytes to Toll-like receptor ligands and inflammatory cytokines. Int Immunol. 2004;16:799–809.CrossRefPubMed
21.
go back to reference Hayashi F, Means TK, Luster AD. Toll-like receptors stimulate human neutrophil function. Blood. 2003;102:2660–9.CrossRefPubMed Hayashi F, Means TK, Luster AD. Toll-like receptors stimulate human neutrophil function. Blood. 2003;102:2660–9.CrossRefPubMed
22.
23.
go back to reference Ramasamy R, Yan SF, Herold K, Clynes R, Schmidt AM. Receptor for advanced glycation end products: fundamental roles in the inflammatory response: winding the way to the pathogenesis of endothelial dysfunction and atherosclerosis. Ann N Y Acadof Sci. 2008;1126:7–13.CrossRef Ramasamy R, Yan SF, Herold K, Clynes R, Schmidt AM. Receptor for advanced glycation end products: fundamental roles in the inflammatory response: winding the way to the pathogenesis of endothelial dysfunction and atherosclerosis. Ann N Y Acadof Sci. 2008;1126:7–13.CrossRef
24.
go back to reference Chavakis T, Bierhaus A, Nawroth PP. RAGE (receptor for advanced glycation end products): a central player in the inflammatory response. Microbes Infect. 2004;6:1219–25.CrossRefPubMed Chavakis T, Bierhaus A, Nawroth PP. RAGE (receptor for advanced glycation end products): a central player in the inflammatory response. Microbes Infect. 2004;6:1219–25.CrossRefPubMed
25.
go back to reference Sorci G, Riuzzi F, Giambanco I, Donato R. RAGE in tissue homeostasis, repair and regeneration. Biochim Biophys Acta. 2013;1833:101–9.CrossRefPubMed Sorci G, Riuzzi F, Giambanco I, Donato R. RAGE in tissue homeostasis, repair and regeneration. Biochim Biophys Acta. 2013;1833:101–9.CrossRefPubMed
26.
go back to reference Riuzzi F, Sorci G, Sagheddu R, Donato R. HMGB1–RAGE regulates muscle satellite cell homeostasis through p38-MAPK- and myogenin-dependent repression of Pax7 transcription. J Cell Sci. 2012;125:1440–54.CrossRefPubMed Riuzzi F, Sorci G, Sagheddu R, Donato R. HMGB1–RAGE regulates muscle satellite cell homeostasis through p38-MAPK- and myogenin-dependent repression of Pax7 transcription. J Cell Sci. 2012;125:1440–54.CrossRefPubMed
27.
go back to reference Brett W, Mandinova A, Remppis A, Sauder U, Rüter F, Heizmann CW, et al. Translocation of S100A1 calcium binding protein during heart surgery. Biochem Biophys Res Commun. 2001;284:698–703.CrossRefPubMed Brett W, Mandinova A, Remppis A, Sauder U, Rüter F, Heizmann CW, et al. Translocation of S100A1 calcium binding protein during heart surgery. Biochem Biophys Res Commun. 2001;284:698–703.CrossRefPubMed
28.
go back to reference Reppel M, Sasse P, Piekorz R, Tang M, Roell W, Duan Y, et al. S100A1 enhances the L-type Ca2+ current in embryonic mouse and neonatal rat ventricular cardiomyocytes. J Biol Chem. 2005;280:36019–28.CrossRefPubMed Reppel M, Sasse P, Piekorz R, Tang M, Roell W, Duan Y, et al. S100A1 enhances the L-type Ca2+ current in embryonic mouse and neonatal rat ventricular cardiomyocytes. J Biol Chem. 2005;280:36019–28.CrossRefPubMed
29.
go back to reference Most P, Seifert H, Gao E, Funakoshi H, Völkers M, Heierhorst J, et al. Cardiac S100A1 protein levels determine contractile performance and propensity toward heart failure after myocardial infarction. Circulation. 2006;114:1258–68.CrossRefPubMed Most P, Seifert H, Gao E, Funakoshi H, Völkers M, Heierhorst J, et al. Cardiac S100A1 protein levels determine contractile performance and propensity toward heart failure after myocardial infarction. Circulation. 2006;114:1258–68.CrossRefPubMed
30.
go back to reference Most P, Pleger ST, Völkers M, Heidt B, Boerries M, Weichenhan D, et al. Cardiac adenoviral S100A1 gene delivery rescues failing myocardium. J Clin Invest. 2004;114:1550–63.CrossRefPubMedPubMedCentral Most P, Pleger ST, Völkers M, Heidt B, Boerries M, Weichenhan D, et al. Cardiac adenoviral S100A1 gene delivery rescues failing myocardium. J Clin Invest. 2004;114:1550–63.CrossRefPubMedPubMedCentral
31.
go back to reference Averill MM, Kerkhoff C, Bornfeldt KE. S100A8 and S100A9 in cardiovascular biology and disease. Arterioscler Thromb Vasc Biol. 2012;32:223–9.CrossRefPubMed Averill MM, Kerkhoff C, Bornfeldt KE. S100A8 and S100A9 in cardiovascular biology and disease. Arterioscler Thromb Vasc Biol. 2012;32:223–9.CrossRefPubMed
32.
go back to reference Donato R, Sorci G, Giambanco I. S100A6 protein: functional roles. Cell Mol Life Sci. 2017;74:2749–60.CrossRefPubMed Donato R, Sorci G, Giambanco I. S100A6 protein: functional roles. Cell Mol Life Sci. 2017;74:2749–60.CrossRefPubMed
33.
go back to reference Petzold A, Keir G, Lim D, Smith M, Thompson EJ. Cerebrospinal fluid (CSF) and serum S100B: release and wash-out pattern. In Brain Res Bull. 2003;61:281–5.CrossRef Petzold A, Keir G, Lim D, Smith M, Thompson EJ. Cerebrospinal fluid (CSF) and serum S100B: release and wash-out pattern. In Brain Res Bull. 2003;61:281–5.CrossRef
34.
go back to reference Ghanem G, Loir B, Morandini R, Sales F, Lienard D, Eggermont A, et al. On the release and half-life of S100B protein in the peripheral blood of melanoma patients. Int J Cancer. 2001;94:586–90.CrossRefPubMed Ghanem G, Loir B, Morandini R, Sales F, Lienard D, Eggermont A, et al. On the release and half-life of S100B protein in the peripheral blood of melanoma patients. Int J Cancer. 2001;94:586–90.CrossRefPubMed
35.
36.
go back to reference Cervellin G, Benatti M, Carbucicchio A, Mattei L, Cerasti D, Aloe R, Lippi G. Serum levels of protein S100B predict intracranial lesions in mild head injury. Clin Biochem. 2012;45:408–11.CrossRefPubMed Cervellin G, Benatti M, Carbucicchio A, Mattei L, Cerasti D, Aloe R, Lippi G. Serum levels of protein S100B predict intracranial lesions in mild head injury. Clin Biochem. 2012;45:408–11.CrossRefPubMed
37.
go back to reference Abildtrup M, Kingsley GH, Scott DL. Calprotectin as a biomarker for rheumatoid arthritis: a systematic review. J Rheumatol. 2015;42:760–70.CrossRefPubMed Abildtrup M, Kingsley GH, Scott DL. Calprotectin as a biomarker for rheumatoid arthritis: a systematic review. J Rheumatol. 2015;42:760–70.CrossRefPubMed
38.
go back to reference Tantivitayakul P, Benjachat T, Somparn P, Leelahavanichkul A, Kittikovit V, Hirankarn N, et al. Elevated expressions of myeloid-related proteins-8 and -14 are danger biomarkers for lupus nephritis. Lupus. 2016;25:38–45.CrossRefPubMed Tantivitayakul P, Benjachat T, Somparn P, Leelahavanichkul A, Kittikovit V, Hirankarn N, et al. Elevated expressions of myeloid-related proteins-8 and -14 are danger biomarkers for lupus nephritis. Lupus. 2016;25:38–45.CrossRefPubMed
39.
go back to reference Winningham-Major F, Staecker JL, Barger SW, Coats S, Van Eldik LJ. Neurite extension and neuronal survival activities of recombinant S100 beta proteins that differ in the content and position of cysteine residues. J Cell Biol. 1989;109:3063–71.CrossRefPubMed Winningham-Major F, Staecker JL, Barger SW, Coats S, Van Eldik LJ. Neurite extension and neuronal survival activities of recombinant S100 beta proteins that differ in the content and position of cysteine residues. J Cell Biol. 1989;109:3063–71.CrossRefPubMed
40.
go back to reference Wang H, Zhang L, Zhang IY, Chen X, Da Fonseca A, Wu S, et al. S100B promotes glioma growth through chemoattraction of myeloid-derived macrophages. Clin Cancer Res. 2013;19:3764–75.CrossRefPubMedPubMedCentral Wang H, Zhang L, Zhang IY, Chen X, Da Fonseca A, Wu S, et al. S100B promotes glioma growth through chemoattraction of myeloid-derived macrophages. Clin Cancer Res. 2013;19:3764–75.CrossRefPubMedPubMedCentral
41.
go back to reference Hartman KG, McKnight LE, Liriano MA, Weber DJ. The evolution of S100B inhibitors for the treatment of malignant melanoma. Future Med Chem. 2013;5:97–109.CrossRefPubMedPubMedCentral Hartman KG, McKnight LE, Liriano MA, Weber DJ. The evolution of S100B inhibitors for the treatment of malignant melanoma. Future Med Chem. 2013;5:97–109.CrossRefPubMedPubMedCentral
42.
go back to reference Charmsaz S, Hughes É, Bane FT, Tibbitts P, McIlroy M, Byrne C, et al. S100β as a serum marker in endocrine resistant breast cancer. BMC Med. 2017;15:79. CrossRefPubMedPubMedCentral Charmsaz S, Hughes É, Bane FT, Tibbitts P, McIlroy M, Byrne C, et al. S100β as a serum marker in endocrine resistant breast cancer. BMC Med. 2017;15:79. CrossRefPubMedPubMedCentral
43.
go back to reference Gagnon A, Kim JH, Schorge JO, Ye B, Liu B, Hasselblatt K, et al. Use of a combination of approaches to identify and validate relevant tumor-associated antigens and their corresponding autoantibodies in ovarian cancer patients. Clin Cancer Res. 2008;14:764–71.CrossRefPubMed Gagnon A, Kim JH, Schorge JO, Ye B, Liu B, Hasselblatt K, et al. Use of a combination of approaches to identify and validate relevant tumor-associated antigens and their corresponding autoantibodies in ovarian cancer patients. Clin Cancer Res. 2008;14:764–71.CrossRefPubMed
44.
go back to reference Zhang H, Zhao Q, Chen Y, Wang Y, Gao S, Mao Y, et al. Selective expression of S100A7 in lung squamous cell carcinomas and large cell carcinomas but not in adenocarcinomas and small cell carcinomas. Thorax. 2008;63:352–9.CrossRefPubMed Zhang H, Zhao Q, Chen Y, Wang Y, Gao S, Mao Y, et al. Selective expression of S100A7 in lung squamous cell carcinomas and large cell carcinomas but not in adenocarcinomas and small cell carcinomas. Thorax. 2008;63:352–9.CrossRefPubMed
45.
go back to reference Liu Y, Tang W, Wang J, Xie L, Li T, He Y, et al. Clinicopathological and prognostic significance of S100A4 overexpression in colorectal cancer: a meta-analysis. Diagn Pathol. 2013;8:181.CrossRefPubMedPubMedCentral Liu Y, Tang W, Wang J, Xie L, Li T, He Y, et al. Clinicopathological and prognostic significance of S100A4 overexpression in colorectal cancer: a meta-analysis. Diagn Pathol. 2013;8:181.CrossRefPubMedPubMedCentral
46.
go back to reference Zhang L, Jiang H, Xu G, Wen H, Gu B, Liu J, et al. Proteins S100A8 and S100A9 are potential biomarkers for renal cell carcinoma in the early stages: results from a proteomic study integrated with bioinformatics analysis. Mol Med Rep. 2015;11:4093–100.CrossRefPubMedPubMedCentral Zhang L, Jiang H, Xu G, Wen H, Gu B, Liu J, et al. Proteins S100A8 and S100A9 are potential biomarkers for renal cell carcinoma in the early stages: results from a proteomic study integrated with bioinformatics analysis. Mol Med Rep. 2015;11:4093–100.CrossRefPubMedPubMedCentral
47.
go back to reference Kraakman MJ, Lee MK, Al-Sharea A, Dragoljevic D, Barret TJ, Montenont E. Neutrophil-derived S100 calcium-binding proteins A8/A9 promote reticulated thrombocytosis and atherogenesis in diabetes. J Clin Invest. 2017;127:2133–47.CrossRefPubMedPubMedCentral Kraakman MJ, Lee MK, Al-Sharea A, Dragoljevic D, Barret TJ, Montenont E. Neutrophil-derived S100 calcium-binding proteins A8/A9 promote reticulated thrombocytosis and atherogenesis in diabetes. J Clin Invest. 2017;127:2133–47.CrossRefPubMedPubMedCentral
48.
go back to reference Lee RH, Bergmeier W. Sugar makes neutrophils RAGE: linking diabetes-associated hyperglycemia to thrombocytosis and platelet reactivity. J Clin Invest. 2017;127:2040–3.CrossRefPubMedPubMedCentral Lee RH, Bergmeier W. Sugar makes neutrophils RAGE: linking diabetes-associated hyperglycemia to thrombocytosis and platelet reactivity. J Clin Invest. 2017;127:2040–3.CrossRefPubMedPubMedCentral
49.
go back to reference Krisp C, Jacobsen F, McKay MJ, Molloy MP, Steinstraesser L, Wolters DA. Proteome analysis reveals antiangiogenic environments in chronic wounds of diabetes mellitustype 2 patients. Proteomics. 2013;13:2670–81.CrossRefPubMed Krisp C, Jacobsen F, McKay MJ, Molloy MP, Steinstraesser L, Wolters DA. Proteome analysis reveals antiangiogenic environments in chronic wounds of diabetes mellitustype 2 patients. Proteomics. 2013;13:2670–81.CrossRefPubMed
50.
go back to reference Dhas B, Bha VT, Gane B. Role of calprotectin in infection and inflammation. Curr Pediatr Res. 2012;16:83–94. Dhas B, Bha VT, Gane B. Role of calprotectin in infection and inflammation. Curr Pediatr Res. 2012;16:83–94.
51.
go back to reference Fagerhol MK, Dale I, Andersson T. Release and quantitation of a leukocyte derived protein (L1). Scan J Haematol. 1980;24:393–8.CrossRef Fagerhol MK, Dale I, Andersson T. Release and quantitation of a leukocyte derived protein (L1). Scan J Haematol. 1980;24:393–8.CrossRef
52.
go back to reference Zwadlo G, Schlegel R, Sorg C. A monoclonal antibody to a subset of human monocytes found only in the peripheral blood and inflammatory tissues. J Immunol. 1986;137:512–8.PubMed Zwadlo G, Schlegel R, Sorg C. A monoclonal antibody to a subset of human monocytes found only in the peripheral blood and inflammatory tissues. J Immunol. 1986;137:512–8.PubMed
53.
go back to reference Dorin JR, Novak M, Hill RE, Brock DJ, Secher DS, van Heyningen V. A clue to the basic defect in cystic fibrosis from cloning the CF antigen gene. Nature. 1987;326:614–7.CrossRefPubMed Dorin JR, Novak M, Hill RE, Brock DJ, Secher DS, van Heyningen V. A clue to the basic defect in cystic fibrosis from cloning the CF antigen gene. Nature. 1987;326:614–7.CrossRefPubMed
54.
go back to reference Odink K, Cerletti N, Brüggen J, Clerc RG, Tarcsay L, Zwado G, et al. Two calcium-binding proteins in infiltrate macrophages of rheumatoid arthritis. Nature. 1987;330:80–2.CrossRefPubMed Odink K, Cerletti N, Brüggen J, Clerc RG, Tarcsay L, Zwado G, et al. Two calcium-binding proteins in infiltrate macrophages of rheumatoid arthritis. Nature. 1987;330:80–2.CrossRefPubMed
55.
go back to reference Andersson KB, Sletten K, Berntzen HB, 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. 1988;28:241–5.CrossRefPubMed Andersson KB, Sletten K, Berntzen HB, 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. 1988;28:241–5.CrossRefPubMed
56.
go back to reference Wilkinson MM, Busuttil A, Hayward C, Brock DJ, Dorin JR, van Heyningen V. Expression pattern of two related cystic fibrosis-associated calcium-binding proteins in normal and abnormal tissues. J Cell Sci. 1988;91:221–30.PubMed Wilkinson MM, Busuttil A, Hayward C, Brock DJ, Dorin JR, van Heyningen V. Expression pattern of two related cystic fibrosis-associated calcium-binding proteins in normal and abnormal tissues. J Cell Sci. 1988;91:221–30.PubMed
57.
go back to reference Hogg N, Allen C, Edgeworth J. Monoclonal antibody 5.5 reacts with p8,14, a myeloid molecule associated with some vascular endothelium. Eur J Immunol. 1989;19:1053–61.CrossRefPubMed Hogg N, Allen C, Edgeworth J. Monoclonal antibody 5.5 reacts with p8,14, a myeloid molecule associated with some vascular endothelium. Eur J Immunol. 1989;19:1053–61.CrossRefPubMed
58.
go back to reference Tobe T, Murakami K, Tomita M, Nozawa R. Amino acid sequences of 60B8 antigens induced in HL-60 cells by 1,25-dihydroxyvitamin D3. The antigens are identical with macrophage-related protein-14 and -8. Chem Pharm Bull (Tokyo). 1989;37:1576–80.CrossRef Tobe T, Murakami K, Tomita M, Nozawa R. Amino acid sequences of 60B8 antigens induced in HL-60 cells by 1,25-dihydroxyvitamin D3. The antigens are identical with macrophage-related protein-14 and -8. Chem Pharm Bull (Tokyo). 1989;37:1576–80.CrossRef
59.
go back to reference Steinbakk M, Naess-Andersen CF, Lingaas E, Dale I, Brandtzaeg P, Fagerhol MK. Antimicrobial actions of calcium binding leucocyte L1 protein, calprotectin. Lancet. 1990;336:763–5.CrossRefPubMed Steinbakk M, Naess-Andersen CF, Lingaas E, Dale I, Brandtzaeg P, Fagerhol MK. Antimicrobial actions of calcium binding leucocyte L1 protein, calprotectin. Lancet. 1990;336:763–5.CrossRefPubMed
60.
go back to reference Schafer BW, Wicki R, Engelkamp D, Mattei MG, Heizmann CW. Isolation of a YAC clone covering a cluster of nine S100 genes on human chromosome 1q21: rationale for a new nomenclature of the S100 calcium-binding protein family. Genomics. 1995;25:638–43.CrossRefPubMed Schafer BW, Wicki R, Engelkamp D, Mattei MG, Heizmann CW. Isolation of a YAC clone covering a cluster of nine S100 genes on human chromosome 1q21: rationale for a new nomenclature of the S100 calcium-binding protein family. Genomics. 1995;25:638–43.CrossRefPubMed
61.
go back to reference Stříž I, Trebichavský I. Calprotectin—a pleiotropic molecule in acute and chronic inflammation. Physiol Res. 2004;53:245–53.PubMed Stříž I, Trebichavský I. Calprotectin—a pleiotropic molecule in acute and chronic inflammation. Physiol Res. 2004;53:245–53.PubMed
62.
go back to reference Hessian PA, Edgeworth J, Hogg N. MRP-8 and MRP-14, two abundant Ca(2+)-binding proteins of neutrophils and monocytes. J Leukocy Biol. 1993;53:197–204.CrossRef Hessian PA, Edgeworth J, Hogg N. MRP-8 and MRP-14, two abundant Ca(2+)-binding proteins of neutrophils and monocytes. J Leukocy Biol. 1993;53:197–204.CrossRef
63.
go back to reference Vogl T, Ludwig S, Goebeler M, Strey A, Thorey IS, Reichelt R, et al. MRP8 and MRP14 control microtubule reorganization during transendothelial migration of phagocytes. Blood. 2004;104:4260–8.CrossRefPubMed Vogl T, Ludwig S, Goebeler M, Strey A, Thorey IS, Reichelt R, et al. MRP8 and MRP14 control microtubule reorganization during transendothelial migration of phagocytes. Blood. 2004;104:4260–8.CrossRefPubMed
64.
go back to reference Mariani A, Marsili M, Nozzi M, Faricelli R, Chiarelli F, Breda L. Serum calprotectin: review of its usefulness and validity in pediatric rheumatic diseases. Clin Exp Rheumatol. 2015;33:109–14.PubMed Mariani A, Marsili M, Nozzi M, Faricelli R, Chiarelli F, Breda L. Serum calprotectin: review of its usefulness and validity in pediatric rheumatic diseases. Clin Exp Rheumatol. 2015;33:109–14.PubMed
65.
go back to reference Krzesiek E. Fecal calprotectin as an activity marker of inflammatory bowel disease in children. Adv Clin Exp Med. 2015;24:815–22.CrossRefPubMed Krzesiek E. Fecal calprotectin as an activity marker of inflammatory bowel disease in children. Adv Clin Exp Med. 2015;24:815–22.CrossRefPubMed
66.
go back to reference van Rheenen PF, Van de Vijver E, Fidler V. Faecal calprotectin for screening of patients with suspected inflammatory bowel disease: diagnostic meta-analysis. BMJ. 2010;341:c3369.CrossRefPubMedPubMedCentral van Rheenen PF, Van de Vijver E, Fidler V. Faecal calprotectin for screening of patients with suspected inflammatory bowel disease: diagnostic meta-analysis. BMJ. 2010;341:c3369.CrossRefPubMedPubMedCentral
67.
go back to reference Van de Vijver E. Schreuder aB, Cnossen WR, Muller Kobold aC, van Rheenen PF. Safely ruling out inflammatory bowel disease in children and teenagers without referral for endoscopy. Arch Dis Child. 2012;97:1014–8.CrossRefPubMed Van de Vijver E. Schreuder aB, Cnossen WR, Muller Kobold aC, van Rheenen PF. Safely ruling out inflammatory bowel disease in children and teenagers without referral for endoscopy. Arch Dis Child. 2012;97:1014–8.CrossRefPubMed
68.
go back to reference Biskou O, Gardner-Medwin J, Mackinder M, Bertz M, Clark C, Svolos V, et al. Faecal calprotectin in treated and untreated children with coeliac disease and juvenile idiopathic arthritis. J Pediatr Gastroenterol Nutr. 2016;63:112–5.CrossRef Biskou O, Gardner-Medwin J, Mackinder M, Bertz M, Clark C, Svolos V, et al. Faecal calprotectin in treated and untreated children with coeliac disease and juvenile idiopathic arthritis. J Pediatr Gastroenterol Nutr. 2016;63:112–5.CrossRef
69.
go back to reference Cobanoglu N, Galip N, Dalkan C, Bahceciler NN. Leptin, ghrelin and calprotectin: inflammatory markers in childhood asthma? Multidiscip Respir Med. 2013;8:62.CrossRefPubMedPubMedCentral Cobanoglu N, Galip N, Dalkan C, Bahceciler NN. Leptin, ghrelin and calprotectin: inflammatory markers in childhood asthma? Multidiscip Respir Med. 2013;8:62.CrossRefPubMedPubMedCentral
70.
71.
go back to reference Gray RD, Imrie M, Boyd AC, Porteous D, Innes JA, Greening AP. Sputum and serum calprotectin are useful biomarkers during CF exacerbation. J Cyst Fibros. 2010;9:193–8.CrossRefPubMed Gray RD, Imrie M, Boyd AC, Porteous D, Innes JA, Greening AP. Sputum and serum calprotectin are useful biomarkers during CF exacerbation. J Cyst Fibros. 2010;9:193–8.CrossRefPubMed
72.
go back to reference Horsley AR, Davies JC, Gray RD, Macleod KA, Donovan J, Aziz ZA, et al. Changes in physiological, functional and structural markers of cystic fibrosis lung disease with treatment of a pulmonary exacerbation. Thorax. 2013;68:532–9. CrossRefPubMed Horsley AR, Davies JC, Gray RD, Macleod KA, Donovan J, Aziz ZA, et al. Changes in physiological, functional and structural markers of cystic fibrosis lung disease with treatment of a pulmonary exacerbation. Thorax. 2013;68:532–9. CrossRefPubMed
73.
go back to reference Anink J, Van Suijlekom-Smit LW, Otten MH, Prince FH, van Rossum MA, Dolman KM, et al. MRP8/14 serum levels as a predictor of response to starting and stopping anti-TNF treatment in juvenile idiopathic arthritis. Arthritis Res Ther. 2015;17:200.CrossRefPubMedPubMedCentral Anink J, Van Suijlekom-Smit LW, Otten MH, Prince FH, van Rossum MA, Dolman KM, et al. MRP8/14 serum levels as a predictor of response to starting and stopping anti-TNF treatment in juvenile idiopathic arthritis. Arthritis Res Ther. 2015;17:200.CrossRefPubMedPubMedCentral
74.
go back to reference Abe J, Jibiki T, Noma S, Nakajima T, Saito H, Terai M. Gene expression profiling of the effect of high-dose intravenous Ig in patients with Kawasaki disease. J Immunol. 2005;174:5837–45.CrossRefPubMed Abe J, Jibiki T, Noma S, Nakajima T, Saito H, Terai M. Gene expression profiling of the effect of high-dose intravenous Ig in patients with Kawasaki disease. J Immunol. 2005;174:5837–45.CrossRefPubMed
76.
go back to reference Chen O, Zhu XB, Ren P, Wang YB, Sun RP, Wei DE. Henoch Schonlein Purpura in children: clinical analysis of 120 cases. Afr Health Sci. 2013;13:94–9.PubMedPubMedCentral Chen O, Zhu XB, Ren P, Wang YB, Sun RP, Wei DE. Henoch Schonlein Purpura in children: clinical analysis of 120 cases. Afr Health Sci. 2013;13:94–9.PubMedPubMedCentral
77.
go back to reference Turnier JL, Fall N, Thornton S, Witte D, Bennett MR, Appenzeller S, et al. Urine S100 proteins as potential biomarkers of lupus nephritis activity. Arthritis Res Ther. 2017;19:242. CrossRefPubMedPubMedCentral Turnier JL, Fall N, Thornton S, Witte D, Bennett MR, Appenzeller S, et al. Urine S100 proteins as potential biomarkers of lupus nephritis activity. Arthritis Res Ther. 2017;19:242. CrossRefPubMedPubMedCentral
78.
go back to reference Pergialiotis V, Konstantopoulos P, Karampetsou N, Koutaki D, Gkioka E, Perrea DN, et al. Calprotectin levels in necrotizing enterocolitis: a systematic review of the literature. Inflammn Res. 2016;65:847–52.CrossRef Pergialiotis V, Konstantopoulos P, Karampetsou N, Koutaki D, Gkioka E, Perrea DN, et al. Calprotectin levels in necrotizing enterocolitis: a systematic review of the literature. Inflammn Res. 2016;65:847–52.CrossRef
79.
go back to reference Campeotto F, Baldassarre M, Butel MJ, Viallon V, Nganzali F, Soulaines P, et al. Fecal calprotectin: cutoff values for identifying intestinal distress in preterm infants. J Pediatr Gastroenterol Nutr. 2009;48:507–10.PubMed Campeotto F, Baldassarre M, Butel MJ, Viallon V, Nganzali F, Soulaines P, et al. Fecal calprotectin: cutoff values for identifying intestinal distress in preterm infants. J Pediatr Gastroenterol Nutr. 2009;48:507–10.PubMed
80.
go back to reference Yang Q, Smith PB, Goldberg RN, Cotton CM. Dynamic change of fecal calprotectin in very low birth weight infants during the first month of life. Neonatology. 2008;94:267–71.CrossRefPubMedPubMedCentral Yang Q, Smith PB, Goldberg RN, Cotton CM. Dynamic change of fecal calprotectin in very low birth weight infants during the first month of life. Neonatology. 2008;94:267–71.CrossRefPubMedPubMedCentral
81.
go back to reference Josefsson S, Bunn SK, Domellof M. Fecal calprotectin in very low birth weight infants. J Pediatr Gastroenterol Nutr. 2007;44:407–13.CrossRefPubMed Josefsson S, Bunn SK, Domellof M. Fecal calprotectin in very low birth weight infants. J Pediatr Gastroenterol Nutr. 2007;44:407–13.CrossRefPubMed
82.
go back to reference Zoppelli L, Güttel C, Bittrich HJ, Andrée C, Wirth S, Jenke A. Fecal calprotectin concentrations in premature infants have a lower limit and show postnatal and gestational age dependence. Neonatology. 2012;102:68–74.CrossRefPubMed Zoppelli L, Güttel C, Bittrich HJ, Andrée C, Wirth S, Jenke A. Fecal calprotectin concentrations in premature infants have a lower limit and show postnatal and gestational age dependence. Neonatology. 2012;102:68–74.CrossRefPubMed
83.
go back to reference Pietzsch J, Hoppmann S. Human S100A12: a novel key player in inflammation? Amino Acids. 2009;36:381–9.CrossRefPubMed Pietzsch J, Hoppmann S. Human S100A12: a novel key player in inflammation? Amino Acids. 2009;36:381–9.CrossRefPubMed
84.
go back to reference Guignard F, Mauel J, Markert M. Identification and characterization of a novel human neutrophil protein related to the S100 family. Biochemical J. 1995;309:395–401.CrossRef Guignard F, Mauel J, Markert M. Identification and characterization of a novel human neutrophil protein related to the S100 family. Biochemical J. 1995;309:395–401.CrossRef
85.
go back to reference Yang Z, Yan WX, Cai H, Tedla N, Armishaw C, Di Girolamo N, et al. S100A12 provokes mast cell activation: a potential amplification pathway in asthma and innate immunity. J Allergy Clin Immunol. 2007;119:106–14.CrossRefPubMed Yang Z, Yan WX, Cai H, Tedla N, Armishaw C, Di Girolamo N, et al. S100A12 provokes mast cell activation: a potential amplification pathway in asthma and innate immunity. J Allergy Clin Immunol. 2007;119:106–14.CrossRefPubMed
86.
go back to reference Yilmaz Y, Yonal O, Eren F, Atug O, Hamzaoglu HO. Serum levels of soluble receptor for advanced glycation endproducts (sRAGE) are higher in ulcerative colitis and correlate with disease activity. J Crohns Colitis. 2011;5:402–6.CrossRefPubMed Yilmaz Y, Yonal O, Eren F, Atug O, Hamzaoglu HO. Serum levels of soluble receptor for advanced glycation endproducts (sRAGE) are higher in ulcerative colitis and correlate with disease activity. J Crohns Colitis. 2011;5:402–6.CrossRefPubMed
87.
go back to reference Däbritz J, Foell D, Wirth S, Jenke A. Fecal S100A12: identifying intestinal distress in very-low-birth-weight infants. J Pediatr Gastroenterol Nutr. 2013;57:204–10.CrossRefPubMed Däbritz J, Foell D, Wirth S, Jenke A. Fecal S100A12: identifying intestinal distress in very-low-birth-weight infants. J Pediatr Gastroenterol Nutr. 2013;57:204–10.CrossRefPubMed
88.
go back to reference Däbritz J, Jenke A, Wirth S, Foell D. Fecal phagocyte-specific S100A12 for diagnosing necrotizing enterocolitis. J Pediatr. 2012;161:1059–64.CrossRefPubMed Däbritz J, Jenke A, Wirth S, Foell D. Fecal phagocyte-specific S100A12 for diagnosing necrotizing enterocolitis. J Pediatr. 2012;161:1059–64.CrossRefPubMed
89.
go back to reference Terrin G, Passariello A, Manguso F, Salvia G, Rapacciuolo L, Messina F, et al. Serum calprotectin: an antimicrobial peptide as a new marker for the diagnosis of sepsis in very low birth weight newborns. Clin Dev Immunol. 2011;2011:291085.CrossRefPubMedPubMedCentral Terrin G, Passariello A, Manguso F, Salvia G, Rapacciuolo L, Messina F, et al. Serum calprotectin: an antimicrobial peptide as a new marker for the diagnosis of sepsis in very low birth weight newborns. Clin Dev Immunol. 2011;2011:291085.CrossRefPubMedPubMedCentral
90.
go back to reference Abdel-Maaboud M, El-Mazary AA, Osman AM. Serum calprotectin as a diagnostic marker of late onset sepsis in full-term neonates. Egypt J Pediatr Allergy Immunol. 2012;10:19–24. Abdel-Maaboud M, El-Mazary AA, Osman AM. Serum calprotectin as a diagnostic marker of late onset sepsis in full-term neonates. Egypt J Pediatr Allergy Immunol. 2012;10:19–24.
91.
go back to reference Decembrino L, De Amici M, Pozzi M, De Silvestri A, Stronati M. Serum calprotectin: a potential biomarker for neonatal sepsis. J Immunol Res. 2015;2015:147973.CrossRefPubMedPubMedCentral Decembrino L, De Amici M, Pozzi M, De Silvestri A, Stronati M. Serum calprotectin: a potential biomarker for neonatal sepsis. J Immunol Res. 2015;2015:147973.CrossRefPubMedPubMedCentral
92.
go back to reference Avery GB, Fletcher MA, MacDonald MG. Neonatology: pathophysiology and management of the newborn. Philadelphia: Lippincott; 1994. Avery GB, Fletcher MA, MacDonald MG. Neonatology: pathophysiology and management of the newborn. Philadelphia: Lippincott; 1994.
93.
go back to reference Gazzolo D, Di Iorio R, Marioni E, Masetti P, Serra G, Giovannini L, et al. S100B protein is increased in asphyxiated term infants developing intraventricular hemorrhage. Crit Care Med. 2002;30:1356–60.CrossRefPubMed Gazzolo D, Di Iorio R, Marioni E, Masetti P, Serra G, Giovannini L, et al. S100B protein is increased in asphyxiated term infants developing intraventricular hemorrhage. Crit Care Med. 2002;30:1356–60.CrossRefPubMed
94.
go back to reference Gazzolo D, Bruschettini M, Lituania M, Serra G, Bonacci W, Michetti F. Increased urinary S100B protein as an early indicator of intraventricular hemorrhage in preterm infants: correlation with the grade of hemorrhage. Clin Chem. 2001;47:1836–8.PubMed Gazzolo D, Bruschettini M, Lituania M, Serra G, Bonacci W, Michetti F. Increased urinary S100B protein as an early indicator of intraventricular hemorrhage in preterm infants: correlation with the grade of hemorrhage. Clin Chem. 2001;47:1836–8.PubMed
95.
go back to reference Gazzolo D, Marinoni E, Di Iorio R, Bruschettini M, Kornacka M, Lituania M, et al. Urinary S100B protein measurements: a tool for the early identification of hypoxic-ischemic encephalopathy in asphyxiated full-term infants. Crit Care Med. 2004;32:131–6.CrossRefPubMed Gazzolo D, Marinoni E, Di Iorio R, Bruschettini M, Kornacka M, Lituania M, et al. Urinary S100B protein measurements: a tool for the early identification of hypoxic-ischemic encephalopathy in asphyxiated full-term infants. Crit Care Med. 2004;32:131–6.CrossRefPubMed
Metadata
Title
Multifarious diagnostic possibilities of the S100 protein family: predominantly in pediatrics and neonatology
Authors
Anna Medkova
Josef Srovnal
Jarmila Potomkova
Jana Volejnikova
Vladimir Mihal
Publication date
01-08-2018
Publisher
Childrens Hospital, Zhejiang University School of Medicine
Published in
World Journal of Pediatrics / Issue 4/2018
Print ISSN: 1708-8569
Electronic ISSN: 1867-0687
DOI
https://doi.org/10.1007/s12519-018-0163-5

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