Gene Expression-Based Classifiers Identify Staphylococcus aureus Infection in Mice and Humans

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Ahn, Sun Hee ^a   Tsalik, Ephraim L ^a,b   Cyr, Derek D ^c   Zhang, Yurong ^a   van Velkinburgh, Jennifer C ^d   Langley, Raymond J ^e   Glickman, Seth W ^f   Cairns, Charles B ^f   Zaas, Aimee K ^a,c   Rivers, Emanuel P ^g   Otero, Ronny M ^g   Veldman, Tim ^c   Kingsmore, Stephen F ^h   Lucas, Joseph ^c   Woods, Christopher W ^a,b,c   Ginsburg, Geoffrey S ^c   Fowler, Vance G ^a,c,i  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b DURHAM VA MEDICAL CENTER   (United States)

^c DUKE UNIVERSITY   (United States)

^d Van Velkinburgh Initiative for Collaboratory BioMedical Research   (United States)

^e LOVELACE RESPIRATORY RESEARCH INSTITUTE   (United States)

^f UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^g WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^h CHILDREN S MERCY HOSPITAL   (United States)

ⁱ DUKE CLINICAL RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL STRAIN; BAYESIAN LEARNING; BLOODSTREAM INFECTION; CLASSIFIER; COHORT ANALYSIS; CONTROLLED STUDY; DIAGNOSTIC ACCURACY; DIAGNOSTIC TEST; DIFFERENTIAL DIAGNOSIS; DISEASE CLASSIFICATION; ESCHERICHIA COLI INFECTION; FEMALE; GENE EXPRESSION; HUMAN; MAJOR CLINICAL STUDY; MALE; MOUSE; MOUSE STRAIN; NONHUMAN; NUCLEOTIDE SEQUENCE; OUTBRED STRAIN; PROCESS MODEL; QUANTITATIVE ANALYSIS; REGRESSION ANALYSIS; SEPSIS; STAPHYLOCOCCUS INFECTION; THEORY VALIDATION;

ADULT; AGED; AGED, 80 AND OVER; ANIMALS; ANTI-BACTERIAL AGENTS; GENE EXPRESSION PROFILING; HOST-PATHOGEN INTERACTIONS; HUMANS; MICE; MICE, 129 STRAIN; MICE, INBRED BALB C; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, INBRED NOD; MICE, INBRED STRAINS; MIDDLE AGED; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY; SEPSIS; SPECIES SPECIFICITY; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; YOUNG ADULT;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; MURINAE; MUS; STAPHYLOCOCCUS AUREUS;

EID: 84872175208     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0048979     Document Type: Article

References (73)

1. Klein E, Smith DL, Laxminarayan R, (2007) Hospitalizations and deaths caused by methicillin-resistant Staphylococcus aureus, United States, 1999-2005. Emerg Infect Dis 13: 1840-1846.
2. Martin GS, Mannino DM, Eaton S, Moss M, (2003) The epidemiology of sepsis in the United States from 1979 through 2000. N Engl J Med 348: 1546-1554.
3. Lee A, Mirrett S, Reller LB, Weinstein MP, (2007) Detection of bloodstream infections in adults: how many blood cultures are needed? J Clin Microbiol 45: 3546-3548.
4. Kollef MH, Sherman G, Ward S, Fraser VJ, (1999) Inadequate antimicrobial treatment of infections: a risk factor for hospital mortality among critically ill patients. Chest 115: 462-474.
5. Kumar A, Ellis P, Arabi Y, Roberts D, Light B, et al. (2009) Initiation of inappropriate antimicrobial therapy results in a fivefold reduction of survival in human septic shock. Chest 136: 1237-1248.
6. Kim JH, Gallis HA, (1989) Observations on spiraling empiricism: its causes, allure, and perils, with particular reference to antibiotic therapy. Am J Med 87: 201-206.
7. Boucher HW, Talbot GH, Bradley JS, Edwards JE, Gilbert D, et al. (2009) Bad bugs, no drugs: no ESKAPE! An update from the Infectious Diseases Society of America. Clin Infect Dis 48: 1-12.
8. Feezor RJ, Oberholzer C, Baker HV, Novick D, Rubinstein M, et al. (2003) Molecular characterization of the acute inflammatory response to infections with gram-negative versus gram-positive bacteria. Infect Immun 71: 5803-5813.
9. Yu SL, Chen HW, Yang PC, Peck K, Tsai MH, et al. (2004) Differential gene expression in gram-negative and gram-positive sepsis. Am J Respir Crit Care Med 169: 1135-1143.
10. Ramilo O, Allman W, Chung W, Mejias A, Ardura M, et al. (2007) Gene expression patterns in blood leukocytes discriminate patients with acute infections. Blood 109: 2066-2077.
11. Takeuchi O, Hoshino K, Kawai T, Sanjo H, Takada H, et al. (1999) Differential roles of TLR2 and TLR4 in recognition of gram-negative and gram-positive bacterial cell wall components. Immunity 11: 443-451.
12. Dziarski R, Wang Q, Miyake K, Kirschning CJ, Gupta D, (2001) MD-2 enables Toll-like receptor 2 (TLR2)-mediated responses to lipopolysaccharide and enhances TLR2-mediated responses to Gram-positive and Gram-negative bacteria and their cell wall components. J Immunol 166: 1938-1944.
13. Cross ML, Ganner A, Teilab D, Fray LM, (2004) Patterns of cytokine induction by gram-positive and gram-negative probiotic bacteria. FEMS Immunol Med Microbiol 42: 173-180.
14. Hessle CC, Andersson B, Wold AE, (2005) Gram-positive and Gram-negative bacteria elicit different patterns of pro-inflammatory cytokines in human monocytes. Cytokine 30: 311-318.
15. Zaas AK, Chen M, Varkey J, Veldman T, Hero AO 3rd, et al (2009) Gene expression signatures diagnose influenza and other symptomatic respiratory viral infections in humans. Cell Host Microbe 6: 207-217.
16. Kawada J, Kimura H, Kamachi Y, Nishikawa K, Taniguchi M, et al. (2006) Analysis of gene-expression profiles by oligonucleotide microarray in children with influenza. J Gen Virol 87: 1677-1683.
17. Ng HH, Frantz CE, Rausch L, Fairchild DC, Shimon J, et al. (2005) Gene expression profiling of mouse host response to Listeria monocytogenes infection. Genomics 86: 657-667.
18. Ardura MI, Banchereau R, Mejias A, Di Pucchio T, Glaser C, et al. (2009) Enhanced monocyte response and decreased central memory T cells in children with invasive Staphylococcus aureus infections. PLoS One 4: e5446.
19. Zaas AK, Aziz H, Lucas J, Perfect JR, Ginsburg GS, (2010) Blood gene expression signatures predict invasive candidiasis. Sci Transl Med 2: 21ra17.
20. Kim HS, Choi EH, Khan J, Roilides E, Francesconi A, et al. (2005) Expression of genes encoding innate host defense molecules in normal human monocytes in response to Candida albicans. Infect Immun 73: 3714-3724.
21. McDunn JE, Husain KD, Polpitiya AD, Burykin A, Ruan J, et al. (2008) Plasticity of the systemic inflammatory response to acute infection during critical illness: development of the riboleukogram. PLoS One 3: e1564.
22. Chaussabel D, Quinn C, Shen J, Patel P, Glaser C, et al. (2008) A modular analysis framework for blood genomics studies: application to systemic lupus erythematosus. Immunity 29: 150-164.
23. Timofeeva AV, Goriunova LE, Khaspekov GL, Il'inskaia OP, Sirotkin VN, et al. (2009) [Comparative transcriptome analysis of human aorta atherosclerotic lesions and peripheral blood leukocytes from essential hypertension patients]. Kardiologiia 49: 27-38.
24. Dressman HK, Muramoto GG, Chao NJ, Meadows S, Marshall D, et al. (2007) Gene expression signatures that predict radiation exposure in mice and humans. PLoS Med 4: e106.
25. Rice KC, Firek BA, Nelson JB, Yang SJ, Patton TG, et al. (2003) The Staphylococcus aureus cidAB operon: evaluation of its role in regulation of murein hydrolase activity and penicillin tolerance. J Bacteriol 185: 2635-2643.
26. Miller RL, Ramsey GA, Krenitsky TA, Elion GB, (1972) Guanine phosphoribosyltransferase from Escherichia coli, specificity and properties. Biochemistry 11: 4723-4731.
27. Glickman SW, Cairns CB, Otero RM, Woods CW, Tsalik EL, et al. (2010) Disease progression in hemodynamically stable patients presenting to the emergency department with sepsis. Acad Emerg Med 17: 383-390.
28. Tsalik EL, Jones D, Nicholson B, Waring L, Liesenfeld O, et al. (2010) Multiplex PCR to diagnose bloodstream infections in patients admitted from the emergency department with sepsis. J Clin Microbiol 48: 26-33.
29. Bone RC, Balk RA, Cerra FB, Dellinger RP, Fein AM, et al. (1992) Definitions for sepsis and organ failure and guidelines for the use of innovative therapies in sepsis. The ACCP/SCCM Consensus Conference Committee. American College of Chest Physicians/Society of Critical Care Medicine. Chest 101: 1644-1655.
30. Voora D, Ortel TL, Lucas JE, Chi JT, Becker RC, et al. (2010) Abstract 16293: A Whole Blood RNA Signature Accurately Classifies Multiple Measures of Platelet Function on Aspirin in Healthy Volunteers and Highlights a Common Underlying Pathway. Circulation 122: A16293.
31. Carvalho CM, Chang J, Lucas JE, Nevins JR, Wang QL, et al. (2008) High-Dimensional Sparse Factor Modeling: Applications in Gene Expression Genomics. Journal of the American Statistical Association 103: 1438-1456.
32. Wang Q, Carvalho C, Lucas JE, West M, (2007) BFRM: Bayesian factor regression modeling. Bulletin of the International Society of Bayesian Analysis 14: 4-5.
33. Hans C, Dobra A, West M, (2007) Shotgun Stochastic search for "Large p" regression. Journal of the American Statistical Association 102: 507-516.
34. Raftery AE, Madigan D, Hoeting JA, (1997) Bayesian model averaging for linear regression models. Journal of the American Statistical Association 92: 179-191.
35. Chang JT, Carvalho C, Mori S, Bild AH, Gatza ML, et al. (2009) A genomic strategy to elucidate modules of oncogenic pathway signaling networks. Mol Cell 34: 104-114.
36. Chen M, Carlson D, Zaas A, Woods CW, Ginsburg GS, et al. (2011) Detection of viruses via statistical gene expression analysis. IEEE Trans Biomed Eng 58: 468-479.
37. Chen M, Zaas A, Woods CW, Ginsburg GS, Lucas JE, et al. (2011) Predicting Viral Infection from High-Dimensional Biomarker Trajectories. Journal of the American Statistical Association In Press.
38. Cyr DD, Lucas JE, Thompson JW, Patel K, Clark PJ, et al. (2011) Characterization of serum proteins associated with IL28B genotype among patients with chronic hepatitis C. PLoS One. 6: e21854.
39. Lucas J, Carvalho C, West M (2009) A bayesian analysis strategy for cross-study translation of gene expression biomarkers. Stat Appl Genet Mol Biol 8: Article 11.
40. Lucas JE, Kung HN, Chi JT, (2010) Latent factor analysis to discover pathway-associated putative segmental aneuploidies in human cancers. PLoS Comput Biol 6: e1000920.
41. Meadows SK, Dressman HK, Daher P, Himburg H, Russell JL, et al. (2010) Diagnosis of partial body radiation exposure in mice using peripheral blood gene expression profiles. PLoS One 5: e11535.
42. Merl D, Lucas JE, Nevins JR, Shen H, West M (2009) Trans-study Projection of Genomic Biomarkers in Analysis of Oncogene Deregulation and Breast Cancer. In: O'Hagan T, West M, editors. The Oxford Handbook of Applied Bayesian Analysis.
43. Ahn SH, Deshmukh H, Johnson N, Cowell LG, Rude TH, et al. (2010) Two genes on A/J chromosome 18 are associated with susceptibility to Staphylococcus aureus infection by combined microarray and QTL analyses. PLoS Pathog 6: e1001088.
44. von Kockritz-Blickwede M, Rohde M, Oehmcke S, Miller LS, Cheung AL, et al. (2008) Immunological mechanisms underlying the genetic predisposition to severe Staphylococcus aureus infection in the mouse model. Am J Pathol 173: 1657-1668.
45. Downey T, (2006) Analysis of a multifactor microarray study using Partek genomics solution. Methods Enzymol 411: 256-270.
46. Thakker M, Park JS, Carey V, Lee JC, (1998) Staphylococcus aureus serotype 5 capsular polysaccharide is antiphagocytic and enhances bacterial virulence in a murine bacteremia model. Infect Immun 66: 5183-5189.
47. Xu W-F, Andersen H, Whitmore TE, Presnell SR, Yee DP, et al. (1998) Cloning and characterization of human protease-activated receptor 4. Proceedings of the National Academy of Sciences 95: 6642-6646.
48. Mueller A, O'Rourke J, Grimm J, Guillemin K, Dixon MF, et al. (2003) Distinct gene expression profiles characterize the histopathological stages of disease in Helicobacter-induced mucosa-associated lymphoid tissue lymphoma. Proc Natl Acad Sci U S A 100: 1292-1297.
49. Zhang H, Su YA, Hu P, Yang J, Zheng B, et al. (2006) Signature patterns revealed by microarray analyses of mice infected with influenza virus A and Streptococcus pneumoniae. Microbes Infect 8: 2172-2185.
50. Desai KV, Kavanaugh CJ, Calvo A, Green JE, (2002) Chipping away at breast cancer: insights from microarray studies of human and mouse mammary cancer. Endocr Relat Cancer 9: 207-220.
51. Larsson O, Scheele C, Liang Z, Moll J, Karlsson C, et al. (2004) Kinetics of senescence-associated changes of gene expression in an epithelial, temperature-sensitive SV40 large T antigen model. Cancer Res 64: 482-489.
52. Weindruch R, Kayo T, Lee CK, Prolla TA, (2001) Microarray profiling of gene expression in aging and its alteration by caloric restriction in mice. J Nutr 131: 918S-923S.
53. Wennmalm K, Wahlestedt C, Larsson O, (2005) The expression signature of in vitro senescence resembles mouse but not human aging. Genome Biol 6: R109.
54. Lytkin NI, McVoy L, Weitkamp JH, Aliferis CF, Statnikov A, (2011) Expanding the understanding of biases in development of clinical-grade molecular signatures: a case study in acute respiratory viral infections. PLoS One 6: e20662.
55. Nau GJ, Schlesinger A, Richmond JF, Young RA, (2003) Cumulative Toll-like receptor activation in human macrophages treated with whole bacteria. J Immunol 170: 5203-5209.
56. Boldrick JC, Alizadeh AA, Diehn M, Dudoit S, Liu CL, et al. (2002) Stereotyped and specific gene expression programs in human innate immune responses to bacteria. Proc Natl Acad Sci U S A 99: 972-977.
57. Tang BM, McLean AS, Dawes IW, Huang SJ, Cowley MJ, et al. (2008) Gene-expression profiling of gram-positive and gram-negative sepsis in critically ill patients. Crit Care Med. 1125-1128.
58. Sriskandan S, Cohen J, (1999) Gram-positive sepsis. Mechanisms and differences from gram-negative sepsis. Infect Dis Clin North Am 13: 397-412.
59. He M, Mangiameli DP, Kachala S, Hunter K, Gillespie J, et al. (2010) Expression signature developed from a complex series of mouse models accurately predicts human breast cancer survival. Clin Cancer Res 16: 249-259.
60. Labreche HG, Nevins JR, Huang E, (2011) Integrating factor analysis and a transgenic mouse model to reveal a peripheral blood predictor of breast tumors. BMC Med Genomics 4: 61.
61. Deitch EA, (1998) Animal models of sepsis and shock: a review and lessons learned. Shock 9: 1-11.
62. Dyson A, Singer M, (2009) Animal models of sepsis: why does preclinical efficacy fail to translate to the clinical setting? Crit Care Med 37: S30-37.
63. Esmon CT, (2004) Why do animal models (sometimes) fail to mimic human sepsis? Crit Care Med 32: S219-222.
64. Unsinger J, McDonough JS, Shultz LD, Ferguson TA, Hotchkiss RS, (2009) Sepsis-induced human lymphocyte apoptosis and cytokine production in "humanized" mice. J Leukoc Biol 86: 219-227.
65. Zeni F, Freeman B, Natanson C, (1997) Anti-inflammatory therapies to treat sepsis and septic shock: a reassessment. Crit Care Med 25: 1095-1100.
66. Mohler KM, Torrance DS, Smith CA, Goodwin RG, Stremler KE, et al. (1993) Soluble tumor necrosis factor (TNF) receptors are effective therapeutic agents in lethal endotoxemia and function simultaneously as both TNF carriers and TNF antagonists. J Immunol 151: 1548-1561.
67. Fisher CJ Jr, Agosti JM, Opal SM, Lowry SF, Balk RA, et al. (1996) Treatment of septic shock with the tumor necrosis factor receptor:Fc fusion protein. The Soluble TNF Receptor Sepsis Study Group. N Engl J Med 334: 1697-1702.
68. Mestas J, Hughes CC, (2004) Of mice and not men: differences between mouse and human immunology. J Immunol 172: 2731-2738.
69. von Bernuth H, Picard C, Jin Z, Pankla R, Xiao H, et al. (2008) Pyogenic bacterial infections in humans with MyD88 deficiency. Science 321: 691-696.
70. Shanley TP, Cvijanovich N, Lin R, Allen GL, Thomas NJ, et al. (2007) Genome-level longitudinal expression of signaling pathways and gene networks in pediatric septic shock. Mol Med 13: 495-508.
71. Berry MP, Graham CM, McNab FW, Xu Z, Bloch SA, et al. (2010) An interferon-inducible neutrophil-driven blood transcriptional signature in human tuberculosis. Nature 466: 973-977.
72. Chin CY, Monack DM, Nathan S, (2010) Genome wide transcriptome profiling of a murine acute melioidosis model reveals new insights into how Burkholderia pseudomallei overcomes host innate immunity. BMC Genomics 11: 672.
73. Pankla R, Buddhisa S, Berry M, Blankenship DM, Bancroft GJ, et al. (2009) Genomic transcriptional profiling identifies a candidate blood biomarker signature for the diagnosis of septicemic melioidosis. Genome Biol 10: R127.