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DOI: 10.1055/s-0037-1603803
Pediatric Sepsis: Genetic Considerations
Publication History
22 February 2017
05 April 2017
Publication Date:
26 July 2017 (online)
Abstract
The mortality of childhood sepsis continues to be rather high. When it comes to prevention and adequate therapy, individual differences and genetic alterations are becoming more and more important. These may affect molecules involved in pathogen recognition (e.g., lipopolysaccharide-binding protein, mannose-binding lectin, bactericidal/permeability-increasing protein, Toll-like receptors), signal transduction pathways (e.g., cRel), proinflammatory (e.g., tumor necrosis factor-α, interleukin-1 [IL-1], IL-6, IL-8) as well as anti-inflammatory cytokines (e.g., IL-4, IL-10, IL-1 receptor antagonist), members of the coagulation cascade, and other molecules active in the process of systemic inflammatory response syndrome (e.g., heat shock proteins, complement system). The most common genetic polymorphisms are the so-called single-nucleotide polymorphisms, which entail the change of a single base. Genetic mutations have an impact on susceptibility, severity, and outcome of sepsis. Understanding such mutations may improve treatment efficiency; although there is a considerably limited choice of causal treatments today, they may become available upon future developments in genetic therapy.
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References
- 1 Wright SD, Ramos RA, Tobias PS, Ulevitch RJ, Mathison JC. CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS binding protein. Science 1990; 249 (4975): 1431-1433
- 2 Fenton MJ, Golenbock DT. LPS-binding proteins and receptors. J Leukoc Biol 1998; 64 (01) 25-32
- 3 Zeng L, Gu W, Zhang AQ. , et al. A functional variant of lipopolysaccharide binding protein predisposes to sepsis and organ dysfunction in patients with major trauma. Ann Surg 2012; 255 (01) 147-157
- 4 Calafat J, Janssen H, Tool A. , et al. The bactericidal/permeability-increasing protein (BPI) is present in specific granules of human eosinophils. Blood 1998; 91 (12) 4770-4775
- 5 Mannion BA, Weiss J, Elsbach P. Separation of sublethal and lethal effects of the bactericidal/permeability increasing protein on Escherichia coli. J Clin Invest 1990; 85 (03) 853-860
- 6 Marra MN, Wilde CG, Griffith JE, Snable JL, Scott RW. Bactericidal/permeability-increasing protein has endotoxin-neutralizing activity. J Immunol 1990; 144 (02) 662-666
- 7 Iovine NM, Elsbach P, Weiss J. An opsonic function of the neutrophil bactericidal/permeability-increasing protein depends on both its N- and C-terminal domains. Proc Natl Acad Sci U S A 1997; 94 (20) 10973-10978
- 8 Hubacek JA, Büchler C, Aslanidis C, Schmitz G. The genomic organization of the genes for human lipopolysaccharide binding protein (LBP) and bactericidal permeability increasing protein (BPI) is highly conserved. Biochem Biophys Res Commun 1997; 236 (02) 427-430
- 9 Michalek J, Svetlikova P, Fedora M. , et al. Bactericidal permeability increasing protein gene variants in children with sepsis. Intensive Care Med 2007; 33 (12) 2158-2164
- 10 Kufer TA, Banks DJ, Philpott DJ. Innate immune sensing of microbes by Nod proteins. Ann N Y Acad Sci 2006; 1072: 19-27
- 11 Ogura Y, Bonen DK, Inohara N. , et al. A frameshift mutation in NOD2 associated with susceptibility to Crohn's disease. Nature 2001; 411 (6837): 603-606
- 12 Tsujimoto H, Ono S, Efron PA, Scumpia PO, Moldawer LL, Mochizuki H. Role of Toll-like receptors in the development of sepsis. Shock 2008; 29 (03) 315-321
- 13 Medzhitov R. Toll-like receptors and innate immunity. Nat Rev Immunol 2001; 1 (02) 135-145
- 14 Seabury CM, Cargill EJ, Womack JE. Sequence variability and protein domain architectures for bovine Toll-like receptors 1, 5, and 10. Genomics 2007; 90 (04) 502-515
- 15 Wurfel MM, Gordon AC, Holden TD. , et al. Toll-like receptor 1 polymorphisms affect innate immune responses and outcomes in sepsis. Am J Respir Crit Care Med 2008; 178 (07) 710-720
- 16 Johnson CM, Lyle EA, Omueti KO. , et al. Cutting edge: a common polymorphism impairs cell surface trafficking and functional responses of TLR1 but protects against leprosy. J Immunol 2007; 178 (12) 7520-7524
- 17 Whitmore LC, Hook JS, Philiph AR. , et al. A Common genetic variant in TLR1 enhances human neutrophil priming and impacts length of intensive care stay in pediatric sepsis. J Immunol 2016; 196 (03) 1376-1386
- 18 Smith Jr MF, Mitchell A, Li G. , et al. Toll-like receptor (TLR) 2 and TLR5, but not TLR4, are required for Helicobacter pylori-induced NF-κ B activation and chemokine expression by epithelial cells. J Biol Chem 2003; 278 (35) 32552-32560
- 19 Xiong Y, Song C, Snyder GA, Sundberg EJ, Medvedev AE. R753Q polymorphism inhibits Toll-like receptor (TLR) 2 tyrosine phosphorylation, dimerization with TLR6, and recruitment of myeloid differentiation primary response protein 88. J Biol Chem 2012; 287 (45) 38327-38337
- 20 Lorenz E, Mira JP, Cornish KL, Arbour NC, Schwartz DA. A novel polymorphism in the toll-like receptor 2 gene and its potential association with staphylococcal infection. Infect Immun 2000; 68 (11) 6398-6401
- 21 Gao JW, Zhang AQ, Wang X. , et al. Association between the TLR2 Arg753Gln polymorphism and the risk of sepsis: a meta-analysis. Crit Care 2015; 19: 416 . Doi: 10.1186/s13054-015-1130-3
- 22 Lorenz E, Mira JP, Frees KL, Schwartz DA. Relevance of mutations in the TLR4 receptor in patients with gram-negative septic shock. Arch Intern Med 2002; 162 (09) 1028-1032
- 23 Jessen KM, Lindboe SB, Petersen AL, Eugen-Olsen J, Benfield T. Common TNF-alpha, IL-1 beta, PAI-1, uPA, CD14 and TLR4 polymorphisms are not associated with disease severity or outcome from Gram negative sepsis. BMC Infect Dis 2007; 7: 108 . Doi: 10.1186/1471-2334-7-108
- 24 Ferwerda B, McCall MB, Alonso S. , et al. TLR4 polymorphisms, infectious diseases, and evolutionary pressure during migration of modern humans. Proc Natl Acad Sci U S A 2007; 104 (42) 16645-16650
- 25 Ferwerda B, McCall MB, Verheijen K. , et al. Functional consequences of toll-like receptor 4 polymorphisms. Mol Med 2008; 14 (5-6): 346-352
- 26 Chantratita N, Tandhavanant S, Seal S. , et al. TLR4 genetic variation is associated with inflammatory responses in Gram-positive sepsis. Clin Microbiol Infect 2017; 23 (01) 47.e1-47.e10
- 27 Mansur A, von Gruben L, Popov AF. , et al. The regulatory toll-like receptor 4 genetic polymorphism rs11536889 is associated with renal, coagulation and hepatic organ failure in sepsis patients. J Transl Med 2014; 12: 177 . Doi: 10.1186/1479-5876-12-177
- 28 Lin J, Yao YM, Yu Y. , et al. Effects of CD14-159 C/T polymorphism on CD14 expression and the balance between proinflammatory and anti-inflammatory cytokines in whole blood culture. Shock 2007; 28 (02) 148-153
- 29 Burgmann H, Winkler S, Locker GJ. , et al. Increased serum concentration of soluble CD14 is a prognostic marker in gram-positive sepsis. Clin Immunol Immunopathol 1996; 80 (3 Pt 1): 307-310
- 30 Landmann R, Zimmerli W, Sansano S. , et al. Increased circulating soluble CD14 is associated with high mortality in gram-negative septic shock. J Infect Dis 1995; 171 (03) 639-644
- 31 Gu W, Dong H, Jiang DP. , et al. Functional significance of CD14 promoter polymorphisms and their clinical relevance in a Chinese Han population. Crit Care Med 2008; 36 (08) 2274-2280
- 32 Zhang AQ, Yue CL, Gu W, Du J, Wang HY, Jiang J. Association between CD14 promoter −159C/T polymorphism and the risk of sepsis and mortality: a systematic review and meta-analysis. PLoS One 2013; 8 (08) e71237 . Doi: 10.1371/journal.pone.0071237
- 33 Turner MW. Mannose-binding lectin: the pluripotent molecule of the innate immune system. Immunol Today 1996; 17 (11) 532-540
- 34 Steffensen R, Thiel S, Varming K, Jersild C, Jensenius JC. Detection of structural gene mutations and promoter polymorphisms in the mannan-binding lectin (MBL) gene by polymerase chain reaction with sequence-specific primers. J Immunol Methods 2000; 241 (1-2): 33-42
- 35 Madsen HO, Garred P, Thiel S. , et al. Interplay between promoter and structural gene variants control basal serum level of mannan-binding protein. J Immunol 1995; 155 (06) 3013-3020
- 36 Hibberd ML, Sumiya M, Summerfield JA, Booy R, Levin M. ; Meningococcal Research Group. Association of variants of the gene for mannose-binding lectin with susceptibility to meningococcal disease. Lancet 1999; 353 (9158): 1049-1053
- 37 Summerfield JA, Sumiya M, Levin M, Turner MW. Association of mutations in mannose binding protein gene with childhood infection in consecutive hospital series. BMJ 1997; 314 (7089): 1229-1232
- 38 Lawrence T. The nuclear factor NF-kappaB pathway in inflammation. Cold Spring Harb Perspect Biol 2009; 1 (06) a001651 . Doi: 10.1101/cshperspect.a001651
- 39 Toubiana J, Courtine E, Tores F. , et al. Association of REL polymorphisms and outcome of patients with septic shock. Ann Intensive Care 2016; 6 (01) 28 . Doi: 10.1186/s13613-016-0130-z
- 40 Gordon AC, Lagan AL, Aganna E. , et al. TNF and TNFR polymorphisms in severe sepsis and septic shock: a prospective multicentre study. Genes Immun 2004; 5 (08) 631-640
- 41 Dahmer MK, Randolph A, Vitali S, Quasney MW. Genetic polymorphisms in sepsis. Pediatr Crit Care Med 2005; 6 (3, Suppl): S61-S73
- 42 Wilson AG, de Vries N, Pociot F, di Giovine FS, van der Putte LB, Duff GW. An allelic polymorphism within the human tumor necrosis factor alpha promoter region is strongly associated with HLA A1, B8, and DR3 alleles. J Exp Med 1993; 177 (02) 557-560
- 43 Wilson AG, Symons JA, McDowell TL, McDevitt HO, Duff GW. Effects of a polymorphism in the human tumor necrosis factor alpha promoter on transcriptional activation. Proc Natl Acad Sci U S A 1997; 94 (07) 3195-3199
- 44 Teuffel O, Ethier MC, Beyene J, Sung L. Association between tumor necrosis factor-alpha promoter -308 A/G polymorphism and susceptibility to sepsis and sepsis mortality: a systematic review and meta-analysis. Crit Care Med 2010; 38 (01) 276-282
- 45 Kaluza W, Reuss E, Grossmann S. , et al. Different transcriptional activity and in vitro TNF-alpha production in psoriasis patients carrying the TNF-alpha 238A promoter polymorphism. J Invest Dermatol 2000; 114 (06) 1180-1183
- 46 McArthur JA, Zhang Q, Quasney MW. Association between the A/A genotype at the lymphotoxin-alpha+250 site and increased mortality in children with positive blood cultures. Pediatr Crit Care Med 2002; 3 (04) 341-344
- 47 Kurt AN, Aygun AD, Godekmerdan A, Kurt A, Dogan Y, Yilmaz E. Serum IL-1beta, IL-6, IL-8, and TNF-alpha levels in early diagnosis and management of neonatal sepsis. Mediators Inflamm 2007; 2007: 31397
- 48 Fida NM, Al-Mughales J, Farouq M. Interleukin-1alpha, interleukin-6 and tumor necrosis factor-alpha levels in children with sepsis and meningitis. Pediatr Int 2006; 48 (02) 118-124
- 49 Pruitt JH, Copeland III EM, Moldawer LL. Interleukin-1 and interleukin-1 antagonism in sepsis, systemic inflammatory response syndrome, and septic shock. Shock 1995; 3 (04) 235-251
- 50 Dinarello CA. Biologic basis for interleukin-1 in disease. Blood 1996; 87 (06) 2095-2147
- 51 Zhang AQ, Pan W, Gao JW. , et al. Associations between interleukin-1 gene polymorphisms and sepsis risk: a meta-analysis. BMC Med Genet 2014; 15: 8 . Doi: 10.1155/2007/31397
- 52 Shirodaria S, Smith J, McKay IJ, Kennett CN, Hughes FJ. Polymorphisms in the IL-1A gene are correlated with levels of interleukin-1alpha protein in gingival crevicular fluid of teeth with severe periodontal disease. J Dent Res 2000; 79 (11) 1864-1869
- 53 Pociot F, Mølvig J, Wogensen L, Worsaae H, Nerup J. A TaqI polymorphism in the human interleukin-1 beta (IL-1 beta) gene correlates with IL-1 beta secretion in vitro. Eur J Clin Invest 1992; 22 (06) 396-402
- 54 Hack CE, De Groot ER, Felt-Bersma RJ. , et al. Increased plasma levels of interleukin-6 in sepsis. Blood 1989; 74 (05) 1704-1710
- 55 Waage A, Brandtzaeg P, Halstensen A, Kierulf P, Espevik T. The complex pattern of cytokines in serum from patients with meningococcal septic shock. Association between interleukin 6, interleukin 1, and fatal outcome. J Exp Med 1989; 169 (01) 333-338
- 56 Fishman D, Faulds G, Jeffery R. , et al. The effect of novel polymorphisms in the interleukin-6 (IL-6) gene on IL-6 transcription and plasma IL-6 levels, and an association with systemic-onset juvenile chronic arthritis. J Clin Invest 1998; 102 (07) 1369-1376
- 57 Kilpinen S, Hulkkonen J, Wang XY, Hurme M. The promoter polymorphism of the interleukin-6 gene regulates interleukin-6 production in neonates but not in adults. Eur Cytokine Netw 2001; 12 (01) 62-68
- 58 Haddy N, Sass C, Maumus S. , et al. Biological variations, genetic polymorphisms and familial resemblance of TNF-alpha and IL-6 concentrations: STANISLAS cohort. Eur J Hum Genet 2005; 13 (01) 109-117
- 59 Bennermo M, Held C, Stemme S. , et al. Genetic predisposition of the interleukin-6 response to inflammation: implications for a variety of major diseases?. Clin Chem 2004; 50 (11) 2136-2140
- 60 Schlüter B, Raufhake C, Erren M. , et al. Effect of the interleukin-6 promoter polymorphism (-174 G/C) on the incidence and outcome of sepsis. Crit Care Med 2002; 30 (01) 32-37
- 61 Michalek J, Svetlikova P, Fedora M. , et al. Interleukin-6 gene variants and the risk of sepsis development in children. Hum Immunol 2007; 68 (09) 756-760
- 62 Sutherland AM, Walley KR, Manocha S, Russell JA. The association of interleukin 6 haplotype clades with mortality in critically ill adults. Arch Intern Med 2005; 165 (01) 75-82
- 63 Miyoshi T, Yamashita K, Arai T, Yamamoto K, Mizugishi K, Uchiyama T. The role of endothelial interleukin-8/NADPH oxidase 1 axis in sepsis. Immunology 2010; 131 (03) 331-339
- 64 Mera S, Tatulescu D, Cismaru C. , et al. Multiplex cytokine profiling in patients with sepsis. APMIS 2011; 119 (02) 155-163
- 65 Esposito S, Zampiero A, Pugni L. , et al. Genetic polymorphisms and sepsis in premature neonates. PLoS One 2014; 9 (07) e101248 . Doi: 10.1371/journal.pone.0101248
- 66 Hillian AD, Londono D, Dunn JM. , et al; CF Gene Modifier Study Group. Modulation of cystic fibrosis lung disease by variants in interleukin-8. Genes Immun 2008; 9 (06) 501-508
- 67 Wacharasint P, Nakada TA, Boyd JH, Russell JA, Walley KR. AA genotype of IL-8 -251A/T is associated with low PaO(2)/FiO(2) in critically ill patients and with increased IL-8 expression. Respirology 2012; 17 (08) 1253-1260
- 68 Hull J, Thomson A, Kwiatkowski D. Association of respiratory syncytial virus bronchiolitis with the interleukin 8 gene region in UK families. Thorax 2000; 55 (12) 1023-1027
- 69 Hu D, Wang H, Huang X. , et al. Investigation of association between IL-8 serum levels and IL8 polymorphisms in Chinese patients with sepsis. Gene 2016; 594 (01) 165-170
- 70 Schoenborn JR, Wilson CB. Regulation of interferon-gamma during innate and adaptive immune responses. Adv Immunol 2007; 96: 41-101
- 71 Wang D, Zhong X, Huang D. , et al. Functional polymorphisms of interferon-gamma affect pneumonia-induced sepsis. PLoS One 2014; 9 (01) e87049 . Doi: 10.1371/journal.pone.0087049
- 72 Wang H, Bloom O, Zhang M. , et al. HMG-1 as a late mediator of endotoxin lethality in mice. Science 1999; 285 (5425): 248-251
- 73 Scaffidi P, Misteli T, Bianchi ME. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 2002; 418 (6894): 191-195
- 74 Palumbo R, Bianchi ME. High mobility group box 1 protein, a cue for stem cell recruitment. Biochem Pharmacol 2004; 68 (06) 1165-1170
- 75 Kornblit B, Munthe-Fog L, Madsen HO, Strøm J, Vindeløv L, Garred P. Association of HMGB1 polymorphisms with outcome in patients with systemic inflammatory response syndrome. Crit Care 2008; 12 (03) R83 . Doi: 10.1186/cc6935
- 76 Lee K, Chang Y, Song K. , et al. Associations between Single Nucleotide Polymorphisms of High Mobility Group Box 1 Protein and Clinical Outcomes in Korean Sepsis Patients. Yonsei Med J 2016; 57 (01) 111-117
- 77 Vamvakopoulos JE, Taylor CJ, Morris-Stiff GJ, Green C, Metcalfe S. The interleukin-1 receptor antagonist gene: a single-copy variant of the intron 2 variable number tandem repeat (VNTR) polymorphism. Eur J Immunogenet 2002; 29 (04) 337-340
- 78 Witkin SS, Gerber S, Ledger WJ. Influence of interleukin-1 receptor antagonist gene polymorphism on disease. Clin Infect Dis 2002; 34 (02) 204-209
- 79 Lim WY, Chen Y, Ali SM. , et al. Polymorphisms in inflammatory pathway genes, host factors and lung cancer risk in Chinese female never-smokers. Carcinogenesis 2011; 32 (04) 522-529
- 80 Arnalich F, López-Maderuelo D, Codoceo R. , et al. Interleukin-1 receptor antagonist gene polymorphism and mortality in patients with severe sepsis. Clin Exp Immunol 2002; 127 (02) 331-336
- 81 Zanotti S, Kumar A, Kumar A. Cytokine modulation in sepsis and septic shock. Expert Opin Investig Drugs 2002; 11 (08) 1061-1075
- 82 Gibson AW, Edberg JC, Wu J, Westendorp RG, Huizinga TW, Kimberly RP. Novel single nucleotide polymorphisms in the distal IL-10 promoter affect IL-10 production and enhance the risk of systemic lupus erythematosus. J Immunol 2001; 166 (06) 3915-3922
- 83 Stanilova SA, Miteva LD, Karakolev ZT, Stefanov CS. Interleukin-10-1082 promoter polymorphism in association with cytokine production and sepsis susceptibility. Intensive Care Med 2006; 32: 260-266
- 84 Shu Q, Fang X, Chen Q, Stuber F. IL-10 polymorphism is associated with increased incidence of severe sepsis. Chin Med J (Engl) 2003; 116 (11) 1756-1759
- 85 Mosnier LO, Zlokovic BV, Griffin JH. The cytoprotective protein C pathway. Blood 2007; 109 (08) 3161-3172
- 86 Scopes D, Berg LP, Krawczak M, Kakkar VV, Cooper DN. Polymorphic variation in the human protein C (PROC) gene promoter can influence transcriptional efficiency in vitro. Blood Coagul Fibrinolysis 1995; 6 (04) 317-321
- 87 Spek CA, Greengard JS, Griffin JH, Bertina RM, Reitsma PH. Two mutations in the promoter region of the human protein C gene both cause type I protein C deficiency by disruption of two HNF-3 binding sites. J Biol Chem 1995; a 270 (41) 24216-24221
- 88 Annane D, Bellissant E, Cavaillon JM. Septic shock. Lancet 2005; 365 (9453): 63-78
- 89 Binder A, Endler G, Rieger S. , et al; Central European Meningococcal Genetic Study Group. Protein C promoter polymorphisms associate with sepsis in children with systemic meningococcemia. Hum Genet 2007; 122 (02) 183-190
- 90 Walley KR, Russell JA. Protein C -1641 AA is associated with decreased survival and more organ dysfunction in severe sepsis. Crit Care Med 2007; 35 (01) 12-17
- 91 Eriksson P, Kallin B, van 't Hooft FM, Båvenholm P, Hamsten A. Allele-specific increase in basal transcription of the plasminogen-activator inhibitor 1 gene is associated with myocardial infarction. Proc Natl Acad Sci U S A 1995; 92 (06) 1851-1855
- 92 Hermans PW, Hibberd ML, Booy R. , et al; Meningococcal Research Group. 4G/5G promoter polymorphism in the plasminogen-activator-inhibitor-1 gene and outcome of meningococcal disease. Lancet 1999; 354 (9178): 556-560
- 93 Binder A, Endler G, Müller M, Mannhalter C, Zenz W. ; European Meningococcal Study Group. 4G4G genotype of the plasminogen activator inhibitor-1 promoter polymorphism associates with disseminated intravascular coagulation in children with systemic meningococcemia. J Thromb Haemost 2007; 5 (10) 2049-2054
- 94 Madách K, Aladzsity I, Szilágyi A. , et al. 4G/5G polymorphism of PAI-1 gene is associated with multiple organ dysfunction and septic shock in pneumonia induced severe sepsis: prospective, observational, genetic study. Crit Care 2010; 14 (02) R79 . Doi: 10.1186/cc8992
- 95 Zenz W, Zoehrer B, Levin M. , et al; International Paediatric Meningococcal Thrombolysis Study Group. Use of recombinant tissue plasminogen activator in children with meningococcal purpura fulminans: a retrospective study. Crit Care Med 2004; 32 (08) 1777-1780
- 96 Zenz W, Muntean W, Zobel G, Grubbauer HM, Gallistl S. Treatment of fulminant meningococcemia with recombinant tissue plasminogen activator. Thromb Haemost 1995; 74 (02) 802-803
- 97 Bernard GR, Vincent JL, Laterre PF. , et al; Recombinant human protein C Worldwide Evaluation in Severe Sepsis (PROWESS) study group. Efficacy and safety of recombinant human activated protein C for severe sepsis. N Engl J Med 2001; 344 (10) 699-709
- 98 Sakata Y, Loskutoff DJ, Gladson CL, Hekman CM, Griffin JH. Mechanism of protein C-dependent clot lysis: role of plasminogen activator inhibitor. Blood 1986; 68 (06) 1218-1223
- 99 Green FR. Fibrinogen polymorphisms and atherothrombotic disease. Ann N Y Acad Sci 2001; 936: 549-559
- 100 Brull DJ, Dhamrait S, Moulding R. , et al. The effect of fibrinogen genotype on fibrinogen levels after strenuous physical exercise. Thromb Haemost 2002; 87 (01) 37-41
- 101 Iso H, Folsom AR, Winkelmann JC. , et al. Polymorphisms of the beta fibrinogen gene and plasma fibrinogen concentration in Caucasian and Japanese population samples. Thromb Haemost 1995; 73 (01) 106-111
- 102 van't Hooft FM, von Bahr SJ, Silveira A, Iliadou A, Eriksson P, Hamsten A. Two common, functional polymorphisms in the promoter region of the beta-fibrinogen gene contribute to regulation of plasma fibrinogen concentration. Arterioscler Thromb Vasc Biol 1999; 19 (12) 3063-3070
- 103 Skogen WF, Senior RM, Griffin GL, Wilner GD. Fibrinogen-derived peptide B beta 1-42 is a multidomained neutrophil chemoattractant. Blood 1988; 71 (05) 1475-1479
- 104 Leavell KJ, Peterson MW, Gross TJ. The role of fibrin degradation products in neutrophil recruitment to the lung. Am J Respir Cell Mol Biol 1996; 14 (01) 53-60
- 105 Kuhns DB, Nelson EL, Alvord WG, Gallin JI. Fibrinogen induces IL-8 synthesis in human neutrophils stimulated with formyl-methionyl-leucyl-phenylalanine or leukotriene B(4). J Immunol 2001; 167 (05) 2869-2878
- 106 Rubel C, Fernández GC, Dran G, Bompadre MB, Isturiz MA, Palermo MS. Fibrinogen promotes neutrophil activation and delays apoptosis. J Immunol 2001; 166 (03) 2002-2010
- 107 Rubel C, Gómez S, Fernández GC, Isturiz MA, Caamaño J, Palermo MS. Fibrinogen-CD11b/CD18 interaction activates the NF-kappa B pathway and delays apoptosis in human neutrophils. Eur J Immunol 2003; 33 (05) 1429-1438
- 108 van Sorge NM, van der Pol WL, van de Winkel JG. FcgammaR polymorphisms: implications for function, disease susceptibility and immunotherapy. Tissue Antigens 2003; 61 (03) 189-202
- 109 Warmerdam PA, van de Winkel JG, Vlug A, Westerdaal NA, Capel PJ. A single amino acid in the second Ig-like domain of the human Fc gamma receptor II is critical for human IgG2 binding. J Immunol 1991; 147 (04) 1338-1343
- 110 Salmon JE, Edberg JC, Brogle NL, Kimberly RP. Allelic polymorphisms of human Fc gamma receptor IIA and Fc gamma receptor IIIB. Independent mechanisms for differences in human phagocyte function. J Clin Invest 1992; 89 (04) 1274-1281
- 111 Sanders LA, Feldman RG, Voorhorst-Ogink MM. , et al. Human immunoglobulin G (IgG) Fc receptor IIA (CD32) polymorphism and IgG2-mediated bacterial phagocytosis by neutrophils. Infect Immun 1995; 63 (01) 73-81
- 112 Herman DJ, Hamilton RG, Barington T. , et al. Quantitation of human IgG subclass antibodies to Haemophilus influenzae type b capsular polysaccharide. Results of an international collaborative study using enzyme immunoassay methodology. J Immunol Methods 1992; 148: 101-114
- 113 Siber GR, Schur PH, Aisenberg AC, Weitzman SA, Schiffman G. Correlation between serum IgG-2 concentrations and the antibody response to bacterial polysaccharide antigens. N Engl J Med 1980; 303 (04) 178-182
- 114 Wu J, Edberg JC, Redecha PB. , et al. A novel polymorphism of FcgammaRIIIa (CD16) alters receptor function and predisposes to autoimmune disease. J Clin Invest 1997; 100 (05) 1059-1070
- 115 Koene HR, Kleijer M, Algra J, Roos D, von dem Borne AE, de Haas M. Fc gammaRIIIa-158V/F polymorphism influences the binding of IgG by natural killer cell Fc gammaRIIIa, independently of the Fc gammaRIIIa-48L/R/H phenotype. Blood 1997; 90 (03) 1109-1114
- 116 Huizinga TW, Kleijer M, Tetteroo PA, Roos D, von dem Borne AE. Biallelic neutrophil Na-antigen system is associated with a polymorphism on the phospho-inositol-linked Fc gamma receptor III (CD16). Blood 1990; 75 (01) 213-217
- 117 Salmon JE, Edberg JC, Kimberly RP. Fc gamma receptor III on human neutrophils. Allelic variants have functionally distinct capacities. J Clin Invest 1990; 85 (04) 1287-1295
- 118 Salmon JE, Millard SS, Brogle NL, Kimberly RP. Fc gamma receptor IIIb enhances Fc gamma receptor IIa function in an oxidant-dependent and allele-sensitive manner. J Clin Invest 1995; 95 (06) 2877-2885
- 119 Fijen CA, Bredius RG, Kuijper EJ. Polymorphism of IgG Fc receptors in meningococcal disease. Ann Intern Med 1993; 119 (7 Pt 1): 636
- 120 Bredius RG, Derkx BH, Fijen CA. , et al. Fc gamma receptor IIa (CD32) polymorphism in fulminant meningococcal septic shock in children. J Infect Dis 1994; 170 (04) 848-853
- 121 Platonov AE, Shipulin GA, Vershinina IV, Dankert J, van de Winkel JG, Kuijper EJ. Association of human Fc gamma RIIa (CD32) polymorphism with susceptibility to and severity of meningococcal disease. Clin Infect Dis 1998; 27 (04) 746-750
- 122 Platonov AE, Kuijper EJ, Vershinina IV. , et al. Meningococcal disease and polymorphism of FcgammaRIIa (CD32) in late complement component-deficient individuals. Clin Exp Immunol 1998; 111 (01) 97-101
- 123 Domingo P, Muñiz-Diaz E, Baraldès MA. , et al. Associations between Fc gamma receptor IIA polymorphisms and the risk and prognosis of meningococcal disease. Am J Med 2002; 112 (01) 19-25
- 124 van der Pol WL, Huizinga TW, Vidarsson G. , et al. Relevance of Fcgamma receptor and interleukin-10 polymorphisms for meningococcal disease. J Infect Dis 2001; 184 (12) 1548-1555
- 125 Janeway CA. The complement system and innate immunity. In: Immunobiology: The Immune System in Health and Disease. Janeway CA, Travers P, Walport M, Schlomchik M. , eds. New York, NY: Garland Science; 2001
- 126 Abbas AK, Lichtman AH, Pillai S. Cellular and Molecular Immunology. 6th ed. Philadelphia, PA: Elsevier; 2010: 272-288
- 127 Holers VM. The spectrum of complement alternative pathway-mediated diseases. Immunol Rev 2008; 223: 300-316
- 128 Rodríguez de Córdoba S, Esparza-Gordillo J, Goicoechea de Jorge E, Lopez-Trascasa M, Sánchez-Corral P. The human complement factor H: functional roles, genetic variations and disease associations. Mol Immunol 2004; 41 (04) 355-367
- 129 Agbeko RS, Fidler KJ, Allen ML, Wilson P, Klein NJ, Peters MJ. Genetic variability in complement activation modulates the systemic inflammatory response syndrome in children. Pediatr Crit Care Med 2010; 11 (05) 561-567
- 130 Haralambous E, Dolly SO, Hibberd ML. , et al. Factor H, a regulator of complement activity, is a major determinant of meningococcal disease susceptibility in UK Caucasian patients. Scand J Infect Dis 2006; 38 (09) 764-771
- 131 Calandra T, Roger T. Macrophage migration inhibitory factor: a regulator of innate immunity. Nat Rev Immunol 2003; 3 (10) 791-800
- 132 Barret J. Basic Immunology and its Medical Application. 2nd ed. St. Louis, MO: C.V. Mosby; 1980
- 133 Larson DF, Horak K. Macrophage migration inhibitory factor: controller of systemic inflammation. Crit Care 2006; 10 (02) 138 . Doi: 10.1186/cc4899
- 134 Savva A, Brouwer MC, Roger T. , et al. Functional polymorphisms of macrophage migration inhibitory factor as predictors of morbidity and mortality of pneumococcal meningitis. Proc Natl Acad Sci U S A 2016; 113 (13) 3597-3602
- 135 Lehmann LE, Book M, Hartmann W. , et al. A MIF haplotype is associated with the outcome of patients with severe sepsis: a case control study. J Transl Med 2009; 7: 100
- 136 Yende S, Angus DC, Kong L. , et al. The influence of macrophage migration inhibitory factor gene polymorphisms on outcome from community-acquired pneumonia. FASEB J 2009; 23 (08) 2403-2411
- 137 Renner P, Roger T, Bochud PY. , et al. A functional microsatellite of the macrophage migration inhibitory factor gene associated with meningococcal disease. FASEB J 2012; 26 (02) 907-916
- 138 Brouwer MC, de Gans J, Heckenberg SG, Zwinderman AH, van der Poll T, van de Beek D. Host genetic susceptibility to pneumococcal and meningococcal disease: a systematic review and meta-analysis. Lancet Infect Dis 2009; 9 (01) 31-44
- 139 Bochud PY, Bochud M, Telenti A, Calandra T. Innate immunogenetics: a tool for exploring new frontiers of host defence. Lancet Infect Dis 2007; 7 (08) 531-542
- 140 Chapman SJ, Hill AV. Human genetic susceptibility to infectious disease. Nat Rev Genet 2012; 13 (03) 175-188
- 141 Lehmann LE, Book M, Hartmann W. , et al. A MIF haplotype is associated with the outcome of patients with severe sepsis: a case control study. J Transl Med 2009; 7: 100 . Doi: 10.1186/1479-5876-7-100
- 142 De Maio A. Heat shock proteins: facts, thoughts, and dreams. Shock 1999; 11 (01) 1-12
- 143 Schröder O, Schulte KM, Ostermann P, Röher HD, Ekkernkamp A, Laun RA. Heat shock protein 70 genotypes HSPA1B and HSPA1L influence cytokine concentrations and interfere with outcome after major injury. Crit Care Med 2003; 31 (01) 73-79
- 144 Waterer GW, ElBahlawan L, Quasney MW, Zhang Q, Kessler LA, Wunderink RG. Heat shock protein 70-2+1267 AA homozygotes have an increased risk of septic shock in adults with community-acquired pneumonia. Crit Care Med 2003; 31 (05) 1367-1372
- 145 Temple SE, Cheong KY, Ardlie KG, Sayer D, Waterer GW. The septic shock associated HSPA1B1267 polymorphism influences production of HSPA1A and HSPA1B. Intensive Care Med 2004; 30 (09) 1761-1767
- 146 Schroeder S, Reck M, Hoeft A, Stüber F. Analysis of two human leukocyte antigen-linked polymorphic heat shock protein 70 genes in patients with severe sepsis. Crit Care Med 1999; 27 (07) 1265-1270
- 147 Tran CT, Leiper JM, Vallance P. The DDAH/ADMA/NOS pathway. Atheroscler Suppl 2003; 4 (04) 33-40
- 148 O'Dwyer MJ, Dempsey F, Crowley V, Kelleher DP, McManus R, Ryan T. Septic shock is correlated with asymmetrical dimethyl arginine levels, which may be influenced by a polymorphism in the dimethylarginine dimethylaminohydrolase II gene: a prospective observational study. Crit Care 2006; 10 (05) R139 . Doi: 10.1186/cc5053
- 149 Ryan R, Thornton J, Duggan E. , et al. Gene polymorphism and requirement for vasopressor infusion after cardiac surgery. Ann Thorac Surg 2006; 82 (03) 895-901
- 150 Bai Y, Chen J, Sun K, Xin Y, Liu J, Hui R. Common genetic variation in DDAH2 is associated with intracerebral haemorrhage in a Chinese population: a multi-centre case-control study in China. Clin Sci (Lond) 2009; 117 (07) 273-279
- 151 Maas R, Erdmann J, Lüneburg N. , et al. Polymorphisms in the promoter region of the dimethylarginine dimethylaminohydrolase 2 gene are associated with prevalence of hypertension. Pharmacol Res 2009; 60 (06) 488-493
- 152 Weiss SL, Yu M, Jennings L, Haymond S, Zhang G, Wainwright MS. Pilot study of the association of the DDAH2 -449G polymorphism with asymmetric dimethylarginine and hemodynamic shock in pediatric sepsis. PLoS One 2012; 7 (03) e33355 . Doi: 10.1371/journal.pone.0033355