Noninvasive biophotonic imaging for studies of infectious disease

Abstract

According to World Health Organization estimates, infectious organisms are responsible for approximately one in four deaths worldwide. Animal models play an essential role in the development of vaccines and therapeutic agents but large numbers of animals are required to obtain quantitative microbiological data by tissue sampling. Biophotonic imaging (BPI) is a highly sensitive, nontoxic technique based on the detection of visible light, produced by luciferase-catalysed reactions (bioluminescence) or by excitation of fluorescent molecules, using sensitive photon detectors. The development of bioluminescent/fluorescent microorganisms therefore allows the real-time noninvasive detection of microorganisms within intact living animals. Multiple imaging of the same animal throughout an experiment allows disease progression to be followed with extreme accuracy, reducing the number of animals required to yield statistically meaningful data. In the study of infectious disease, the use of BPI is becoming widespread due to the novel insights it can provide into established models, as well as the impact of the technique on two of the guiding principles of using animals in research, namely reduction and refinement. Here, we review the technology of BPI, from the instrumentation through to the generation of a photonic signal, and illustrate how the technique is shedding light on infection dynamics in vivo.

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     Not in our library10.1016/j.chom.2008.12.013

102. 102.

     Hyland KV, Asfaw SH, Olson CL, Daniels MD, Engman DM. Bioluminescent imaging of Trypanosoma cruzi infection. Int J Parasitol. 2008;38:1391-1400.

     Not in our library10.1016/j.ijpara.2008.04.002

103. 103.

     Inoue Y, Izawa K, Kiryu S, Tojo A, Ohtomo K. Diet and abdominal autofluorescence detected by in vivo fluorescence imaging of living mice. Mol Imaging. 2008;7:21-27.

     Not in our library

104. 104.

     Jawhara S, Mordon S. In vivo imaging of bioluminescent Escherichia coli in a cutaneous wound infection model for evaluation of an antibiotic therapy. Antimicrob Agents Ch. 2004;48:3436-3441.

     Not in our library10.1128/aac.48.9.3436-3441.2004

105. 105.

     Jawhara S, Mordon S. Monitoring of bactericidal action of laser by in vivo imaging of bioluminescent E. coli in a cutaneous wound infection. Laser Med Sci. 2006;21:153-159.

     Not in our library10.1007/s10103-006-0388-8

106. 106.

     Jia Q, Freeman ML, Yager EJ, et al. Induction of protective immunity against murine gammaherpesvirus-68 infection in the absence of viral latency. J Virol. 2010;84:2453-2465.

     Not in our library10.1128/jvi.01543-09

107. 107.

     Johnson FH, Flagler EA, Simpson R, Mc GK. The inhibition of bacterial luminescence by a homologous series of carbamates. J Cell Physiol. 1951;37:1-13.

     Not in our library10.1002/jcp.1030370102

108. 108.

     Jones SA, Chowdhury FZ, Fabich AJ, et al. Respiration of Escherichia coli in the mouse intestine. Infect Immun. 2007;75:4891-4899.

     Not in our library10.1128/iai.00484-07

109. 109.

     Jurcisek JA, Bookwalter JE, Baker BD, Fernandez S, Novotny LA, Munson RS, Bakaletz LO. The PilA protein of non-typeable Haemophilus influenzae plays a role in biofilm formation, adherence to epithelial cells and colonization of the mammalian upper respiratory tract. Mol Microbiol. 2007;65:1288-1299.

     Not in our library10.1111/j.1365-2958.2007.05864.x

110. 110.

     Kadurugamuwa JL, Sin L, Albert E, et al. Direct continuous method for monitoring biofilm infection in a mouse model. Infect Immun. 2003a;71:882-890.

     Not in our library10.1128/iai.71.2.882-890.2003

111. 111.

     Kadurugamuwa JL, Sin LV, Yu J, Francis KP, Kimura R, Purchio T, Contag PR. Rapid direct method for monitoring antibiotics in a mouse model of bacterial biofilm infection. Antimicrob Agents Ch. 2003b;47:3130-3137.

     Not in our library10.1128/aac.47.10.3130-3137.2003

112. 112.

     Kadurugamuwa JL, Sin LV, Yu J, Francis KP, Purchio TF, Contag PR. Noninvasive optical imaging method to evaluate postantibiotic effects on biofilm infection in vivo. Antimicrob Agents Ch. 2004;48:2283-2287.

     Not in our library10.1128/aac.48.6.2283-2287.2004

113. 113.

     Kadurugamuwa JL, Modi K, Coquoz O, Rice B, Smith S, Contag PR, Purchio T. Reduction of astrogliosis by early treatment of pneumococcal meningitis measured by simultaneous imaging, in vivo, of the pathogen and host response. Infect Immun. 2005a;73:7836-7843.

     Not in our library10.1128/iai.73.12.7836-7843.2005

114. 114.

     Kadurugamuwa JL, Modi K, Yu J, Francis KP, Purchio T, Contag PR. Noninvasive biophotonic imaging for monitoring of catheter-associated urinary tract infections and therapy in mice. Infect Immun. 2005b;73:3878-3887.

     Not in our library10.1128/iai.73.7.3878-3887.2005

115. 115.

     Kadurugamuwa JL, Modi K, Yu J, et al. Noninvasive monitoring of pneumococcal meningitis and evaluation of treatment efficacy in an experimental mouse model. Mol Imaging. 2005c;4:137-142.

     Not in our library10.1177/13505068211024891

116. 116.

     Karabiyik L, Turkan H, Ozisik T, Saracli MA, Haznedaroglu T. Effects of sevoflurane and/or nitrous oxide on bacterial growth in in vitro culture conditions. J Anesth. 2007;21:436-438.

     Not in our library10.1007/s00540-007-0520-3

117. 117.

     Karlstrom A, Boyd KL, English BK, McCullers JA. Treatment with protein synthesis inhibitors improves outcomes of secondary bacterial pneumonia after influenza. J Infect Dis. 2009;199:311-319.

     Not in our library10.1086/596051

118. 118.

     Karsi A, Menanteau-Ledouble S, Lawrence ML. Development of bioluminescent Edwardsiella ictaluri for noninvasive disease monitoring. FEMS Microbiol Lett. 2006;260:216-223.

     Not in our library10.1111/j.1574-6968.2006.00310.x

119. 119.

     Kheirolomoom A, Kruse DE, Qin S, et al. Enhanced in vivo bioluminescence imaging using liposomal luciferin delivery system. J Control Release. 2010;141:128-136.

     Not in our library10.1016/j.jconrel.2009.08.029

120. 120.

     Kirby AC, Beattie L, Maroof A, van Rooijen N, Kaye PM. SIGNR1-negative red pulp macrophages protect against acute streptococcal sepsis after Leishmania donovani-induced loss of marginal zone macrophages. Am J Pathol. 2009;175:1107-1115.

     Not in our library10.2353/ajpath.2009.090258

121. 121.

     Kong Y, Subbian S, Cirillo SL, Cirillo JD. Application of optical imaging to study of extrapulmonary spread by tuberculosis. Tuberculosis (Edinburgh). 2009;89(suppl 1):S15-S17.

     Not in our library10.1016/s1472-9792(09)70006-x

122. 122.

     Kong Y, Yao H, Ren H, et al. Imaging tuberculosis with endogenous beta-lactamase reporter enzyme fluorescence in live mice. P Natl Acad Sci USA. 2010;107:12239-12244.

     Not in our library10.1073/pnas.1000643107

123. 123.

     Krautz-Peterson G, Ndegwa D, Vasquez K, Korideck H, Zhang J, Peterson JD, Skelly PJ. Imaging schistosomes in vivo. Faseb J. 2009;23:2673-2680.

     Not in our library10.1096/fj.08-127738

124. 124.

     Kredel S, Nienhaus K, Oswald F, et al. Optimized and far-red-emitting variants of fluorescent protein eqFP611. Chem Biol. 2008;15:224-233.

     Not in our library10.1016/j.chembiol.2008.02.008

125. 125.
     mRuby, a Bright Monomeric Red Fluorescent Protein for Labeling of Subcellular Structures · 2009

     No notice
126. 126.

     Krug A, Luker GD, Barchet W, Leib DA, Akira S, Colonna M. Herpes simplex virus type 1 activates murine natural interferon-producing cells through toll-like receptor 9. Blood. 2004;103:1433-1437.

     Not in our library10.1182/blood-2003-08-2674

127. 127.

     Kuklin NA, Pancari GD, Tobery TW, et al. Real-time monitoring of bacterial infection in vivo: development of bioluminescent staphylococcal foreign-body and deep-thigh-wound mouse infection models. Antimicrob Agents Ch. 2003;47:2740-2748.

     Not in our library10.1128/aac.47.9.2740-2748.2003

128. 128.

     Kuo C, Coquoz O, Troy TL, Xu H, Rice BW. Three-dimensional reconstruction of in vivo bioluminescent sources based on multispectral imaging. J Biomed Opt. 2007;12:024007.

     Not in our library10.1117/1.2717898

129. 129.

     Lambert H, Hitziger N, Dellacasa I, Svensson M, Barragan A. Induction of dendritic cell migration upon Toxoplasma gondii infection potentiates parasite dissemination. Cell Microbiol. 2006;8:1611-1623.

     Not in our library10.1111/j.1462-5822.2006.00735.x

130. 130.

     Lane MC, Alteri CJ, Smith SN, Mobley HL. Expression of flagella is coincident with uropathogenic Escherichia coli ascension to the upper urinary tract. P Natl Acad Sci USA. 2007;104:16669-16674.

     Not in our library10.1073/pnas.0607898104

131. 131.

     Lang T, Goyard S, Lebastard M, Milon G. Bioluminescent Leishmania expressing luciferase for rapid and high throughput screening of drugs acting on amastigote-harbouring macrophages and for quantitative real-time monitoring of parasitism features in living mice. Cell Microbiol. 2005;7:383-392.

     Not in our library10.1111/j.1462-5822.2004.00468.x

132. 132.

     Lecoeur H, Buffet P, Morizot G, Goyard S, Guigon G, Milon G, Lang T. Optimization of topical therapy for Leishmania major localized cutaneous leishmaniasis using a reliable C57BL/6 model. PLoS Negl Trop Dis. 2007;1:e34.

     Not in our library10.1371/journal.pntd.0000034

133. 133.

     Lecoeur H, Buffet PA, Milon G, Lang T. Early curative applications of aminoglycosides (WR279396) on experimental Leishmania major-loaded cutaneous site do not impair the acquisition of immunity. Antimicrob Agents Ch. 2010;54:984-990.

     Not in our library10.1128/aac.01310-09

134. 134.

     Leevy WM, Gammon ST, Jiang H, et al. Optical imaging of bacterial infection in living mice using a fluorescent near-infrared molecular probe. J Am Chem Soc. 2006;128:16476-16477.

     Not in our library10.1021/ja0665592

135. 135.

     Leevy WM, Gammon ST, Johnson JR, et al. Noninvasive optical imaging of Staphylococcus aureus bacterial infection in living mice using a Bis-dipicolylamine-Zinc(II) affinity group conjugated to a near-infrared fluorophore. Bioconjugate Chem. 2008a;19:686-692.

     Not in our library10.1021/bc700376v

136. 136.

     Leevy WM, Lambert TN, Johnson JR, Morris J, Smith BD. Quantum dot probes for bacteria distinguish Escherichia coli mutants and permit in vivo imaging. Chem Commun (Cambridge). 2008b;20:2331-2333.

     Not in our library10.1039/b803590c

137. 137.

     Levine MM, Black RE, Lanata C. Precise estimation of the numbers of chronic carriers of Salmonella typhi in Santiago, Chile, an endemic area. J Infect Dis. 1982;146:724-726.

     Not in our library10.1093/infdis/146.6.724

138. 138.

     Li L, Fei Z, Ren J, et al. Functional imaging of interleukin 1 beta expression in inflammatory process using bioluminescence imaging in transgenic mice. BMC Immunol. 2008;9:49.

     Not in our library10.1186/1471-2172-9-49

139. 139.

     Lipshutz GS, Gruber CA, Cao Y, Hardy J, Contag CH, Gaensler KM. In utero delivery of adeno-associated viral vectors: intraperitoneal gene transfer produces long-term expression. Mol Ther. 2001;3:284-292.

     Not in our library10.1006/mthe.2001.0267

140. 140.

     Loening AM, Fenn TD, Wu AM, Gambhir SS. Consensus guided mutagenesis of Renilla luciferase yields enhanced stability and light output. Protein Eng Des Sel. 2006;19:391-400.

     Not in our library10.1093/protein/gzl023

141. 141.

     Loving CL, Khurana T, Osorio M, Lee GM, Kelly VK, Stibitz S, Merkel TJ. Role of anthrax toxins in dissemination, disease progression, and induction of protective adaptive immunity in the mouse aerosol challenge model. Infect Immun. 2009;77:255-265.

     Not in our library10.1128/iai.00633-08

142. 142.

     Luker GD, Leib DA. Luciferase real-time bioluminescence imaging for the study of viral pathogenesis. Methods Mol Biol. 2005;292:285-296.

     Not in our library10.1385/1-59259-848-x:285

143. 143.

     Luker GD, Bardill JP, Prior JL, Pica CM, Piwnica-Worms D, Leib DA. Noninvasive bioluminescence imaging of herpes simplex virus type 1 infection and therapy in living mice. J Virol. 2002;76:12149-12161.

     Not in our library10.1128/jvi.76.23.12149-12161.2002

144. 144.

     Luker GD, Prior JL, Song J, Pica CM, Leib DA. Bioluminescence imaging reveals systemic dissemination of herpes simplex virus type 1 in the absence of interferon receptors. J Virol. 2003;77:11082-11093.

     Not in our library10.1128/jvi.77.20.11082-11093.2003

145. 145.

     Luker KE, Luker GD. Bioluminescence imaging of reporter mice for studies of infection and inflammation. Antiviral Res. 2010;86:93-100.

     Not in our library10.1016/j.antiviral.2010.02.002

146. 146.

     Luker KE, Hutchens M, Schultz T, Pekosz A, Luker GD. Bioluminescence imaging of vaccinia virus: effects of interferon on viral replication and spread. Virology. 2005;341:284-300.

     Not in our library10.1016/j.virol.2005.06.049

147. 147.

     Luker KE, Schultz T, Romine J, Leib DA, Luker GD. Transgenic reporter mouse for bioluminescence imaging of herpes simplex virus 1 infection in living mice. Virology. 2006;347:286-295.

     Not in our library10.1016/j.virol.2005.12.016

148. 148.

     Malley R, Henneke P, Morse SC, et al. Recognition of pneumolysin by Toll-like receptor 4 confers resistance to pneumococcal infection. P Natl Acad Sci USA. 2003;100:1966-1971.

     Not in our library10.1073/pnas.0435928100

149. 149.

     Mason KM, Munson RS, Bakaletz LO. Nontypeable Haemophilus influenzae gene expression induced in vivo in a chinchilla model of otitis media. Infect Immun. 2003;71:3454-3462.

     Not in our library10.1128/iai.71.6.3454-3462.2003

150. 150.

     Mason KM, Munson RS, Bakaletz LO. A mutation in the sap operon attenuates survival of nontypeable Haemophilus influenzae in a chinchilla model of otitis media. Infect Immun. 2005;73:599-608.

     Not in our library10.1128/iai.73.1.599-608.2005

151. 151.

     McCullers JA, Bartmess KC. Role of neuraminidase in lethal synergism between influenza virus and Streptococcus pneumoniae. J Infect Dis. 2003;187:1000-1009.

     Not in our library10.1086/368163

152. 152.

     McCullers JA, Karlstrom A, Iverson AR, Loeffler JM, Fischetti VA. Novel strategy to prevent otitis media caused by colonizing Streptococcus pneumoniae. PLoS Pathog. 2007;3:e28.

     Not in our library10.1371/journal.ppat.0030028

153. 153.

     Medarova Z, Rashkovetsky L, Pantazopoulos P, Moore A. Multiparametric monitoring of tumor response to chemotherapy by noninvasive imaging. Cancer Res. 2009;69:1182-1189.

     Not in our library10.1158/0008-5472.can-08-2001

154. 154.

     Mehta SR, Huang R, Yang M, et al. Real-time in vivo green fluorescent protein imaging of a murine leishmaniasis model as a new tool for Leishmania vaccine and drug discovery. Clin Vaccine Immunol. 2008;15:1764-1770.

     Not in our library10.1128/cvi.00270-08

155. 155.

     Merzlyak EM, Goedhart J, Shcherbo D, et al. Bright monomeric red fluorescent protein with an extended fluorescence lifetime. Nat Methods. 2007;4:555-557.

     Not in our library10.1038/nmeth1062

156. 156.

     Mesak LR, Yim G, Davies J. Improved lux reporters for use in Staphylococcus aureus. Plasmid. 2009;61:182-187.

     Not in our library10.1016/j.plasmid.2009.01.003

157. 157.

     Milho R, Smith CM, Marques S, et al. In vivo imaging of murid herpesvirus-4 infection. J Gen Virol. 2009;90:21-32.

     Not in our library10.1099/vir.0.006569-0

158. 158.

     Mishin AS, Subach FV, Yampolsky IV, King W, Lukyanov KA, Verkhusha VV. The first mutant of the Aequorea victoria green fluorescent protein that forms a red chromophore. Biochemistry. 2008;47:4666-4673.

     Not in our library10.1021/bi702130s

159. 159.

     Miyahira AK, Shahangian A, Hwang S, Sun R, Cheng G. TANK-binding kinase-1 plays an important role during in vitro and in vivo type I IFN responses to DNA virus infections. J Immunol. 2009;182:2248-2257.

     Not in our library10.4049/jimmunol.0802466

160. 160.

     Molliex S, Montravers P, Dureuil B, Desmonts JM. Halogenated anesthetics inhibit Pseudomonas aeruginosa growth in culture conditions reproducing the alveolar environment. Anesth Analg. 1998;86:1075-1078.

     Not in our library10.1097/00000539-199805000-00033

161. 161.

     Monack DM, Bouley DM, Falkow S. Salmonella typhimurium persists within macrophages in the mesenteric lymph nodes of chronically infected Nramp1+/+ mice and can be reactivated by IFNgamma neutralization. J Exp Med. 2004;199:231-241.

     Not in our library10.1084/jem.20031319

162. 162.

     Mook-Kanamori BB, Rouse MS, Kang CI, van de Beek D, Steckelberg JM, Patel R. Daptomycin in experimental murine pneumococcal meningitis. BMC Infect Dis. 2009;9:50.

     Not in our library10.1186/1471-2334-9-50

163. 163.

     Mortin LI, Li T, Van Praagh AD, Zhang S, Zhang XX, Alder JD. Rapid bactericidal activity of daptomycin against methicillin-resistant and methicillin-susceptible Staphylococcus aureus peritonitis in mice as measured with bioluminescent bacteria. Antimicrob Agents Ch. 2007;51:1787-1794.

     Not in our library10.1128/aac.00738-06

164. 164.

     Novotny LA, Mason KM, Bakaletz LO. Development of a chinchilla model to allow direct, continuous, biophotonic imaging of bioluminescent nontypeable Haemophilus influenzae during experimental otitis media. Infect Immun. 2005;73:609-611.

     Not in our library10.1128/iai.73.1.609-611.2005

165. 165.

     Ntziachristos V. Fluorescence molecular imaging. Annu Rev Biomed Eng. 2006;8:1-33.

     Not in our library10.1146/annurev.bioeng.8.061505.095831

166. 166.

     Ntziachristos V, Ripoll J, Wang LV, Weissleder R. Looking and listening to light: the evolution of whole-body photonic imaging. Nat Biotechnol. 2005;23:313-320.

     Not in our library10.1038/nbt1074

167. 167.

     Orihuela CJ, Gao G, McGee M, Yu J, Francis KP, Tuomanen E. Organ-specific models of Streptococcus pneumoniae disease. Scand J Infect Dis. 2003;35:647-652.

     Not in our library10.1080/00365540310015854

168. 168.

     Orihuela CJ, Gao G, Francis KP, Yu J, Tuomanen EI. Tissue-specific contributions of pneumococcal virulence factors to pathogenesis. J Infect Dis. 2004;190:1661-1669.

     Not in our library10.1086/424596

169. 169.

     Owen SJ, Batzloff M, Chehrehasa F, et al. Nasal-associated lymphoid tissue and olfactory epithelium as portals of entry for Burkholderia pseudomallei in murine melioidosis. J Infect Dis. 2009;199:1761-1770.

     Not in our library10.1086/599210

170. 170.

     Pakhomov AA, Martynov VI. GFP family: structural insights into spectral tuning. Chem Biol. 2008;15:755-764.

     Not in our library10.1016/j.chembiol.2008.07.009

171. 171.

     Park HS, Francis KP, Yu J, Cleary PP. Membranous cells in nasal-associated lymphoid tissue: a portal of entry for the respiratory mucosal pathogen group A streptococcus. J Immunol. 2003;171:2532-2537.

     Not in our library10.4049/jimmunol.171.5.2532

172. 172.

     Pichler A, Prior JL, Piwnica-Worms D. Imaging reversal of multidrug resistance in living mice with bioluminescence: MDR1 P-glycoprotein transports coelenterazine. P Natl Acad Sci USA. 2004;101:1702-1707.

     Not in our library10.1073/pnas.0304326101

173. 173.
     Visualisation and Quantitative Analysis of the Rodent Malaria Liver Stage by Real Time Imaging · 2009

     No notice
174. 174.

     Qazi SN, Counil E, Morrissey J, et al. agr expression precedes escape of internalized Staphylococcus aureus from the host endosome. Infect Immun. 2001;69:7074-7082.

     Not in our library10.1128/iai.69.11.7074-7082.2001

175. 175.

     Rabinovich BA, Ye Y, Etto T, et al. Visualizing fewer than 10 mouse T cells with an enhanced firefly luciferase in immunocompetent mouse models of cancer. P Natl Acad Sci USA. 2008;105:14342-14346.

     Not in our library10.1073/pnas.0804105105

176. 176.

     Radhakrishnan GK, Yu Q, Harms JS, Splitter GA. Brucella TIR domain-containing protein mimics properties of the Toll-like receptor adaptor protein TIRAP. J Biol Chem. 2009;284:9892-9898.

     Not in our library10.1074/jbc.m805458200

177. 177.

     Rajashekara G, Glover DA, Krepps M, Splitter GA. Temporal analysis of pathogenic events in virulent and avirulent Brucella melitensis infections. Cell Microbiol. 2005;7:1459-1473.

     Not in our library10.1111/j.1462-5822.2005.00570.x

178. 178.

     Rajashekara G, Glover DA, Banai M, O'Callaghan D, Splitter GA. Attenuated bioluminescent Brucella melitensis mutants GR019 (virB4), GR024 (galE), and GR026 (BMEI1090-BMEI1091) confer protection in mice. Infect Immun. 2006;74:2925-2936.

     Not in our library10.1128/iai.74.5.2925-2936.2006

179. 179.

     Ramphal R, Balloy V, Jyot J, Verma A, Si-Tahar M, Chignard M. Control of Pseudomonas aeruginosa in the lung requires the recognition of either lipopolysaccharide or flagellin. J Immunol. 2008;181:586-592.

     Not in our library10.4049/jimmunol.181.1.586

180. 180.

     Rehemtulla A, Hall DE, Stegman LD, et al. Molecular imaging of gene expression and efficacy following adenoviral-mediated brain tumor gene therapy. Mol Imaging. 2002;1:43-55.

     Not in our library10.1162/15353500200200005

181. 181.

     Remington SJ. Fluorescent proteins: maturation, photochemistry and photophysics. Curr Opin Struc Biol. 2006;16:714-721.

     Not in our library10.1016/j.sbi.2006.10.001

182. 182.

     Rice BW, Cable MD, Nelson MB. In vivo imaging of light-emitting probes. J Biomed Opt. 2001;6:432-440.

     Not in our library10.1117/1.1413210

183. 183.

     Riedel CU, Casey PG, Mulcahy H, O'Gara F, Gahan CG, Hill C. Construction of p16Slux, a novel vector for improved bioluminescent labeling of gram-negative bacteria. Appl Environ Microb. 2007a;73:7092-7095.

     Not in our library10.1128/aem.01394-07

184. 184.

     Riedel CU, Monk IR, Casey PG, et al. Improved luciferase tagging system for Listeria monocytogenes allows real-time monitoring in vivo and in vitro. Appl Environ Microb. 2007b;73:3091-3094.

     Not in our library10.1128/aem.02940-06

185. 185.

     Riedel CU, Monk IR, Casey PG, Waidmann MS, Gahan CG, Hill C. AgrD-dependent quorum sensing affects biofilm formation, invasion, virulence and global gene expression profiles in Listeria monocytogenes. Mol Microbiol. 2009;71:1177-1189.

     Not in our library10.1111/j.1365-2958.2008.06589.x

186. 186.

     Ripoll J, Ntziachristos V. Iterative boundary method for diffuse optical tomography. J Opt Soc Am A. 2003;20:1103-1110.

     Not in our library10.1364/josaa.20.001103

187. 187.

     Ripoll J, Schulz RB, Ntziachristos V. Free-space propagation of diffuse light: theory and experiments. Phys Rev Lett. 2003;91:103901.

     Not in our library10.1103/physrevlett.91.103901

188. 188.

     Rivera R, Hutchens M, Luker KE, Sonstein J, Curtis JL, Luker GD. Murine alveolar macrophages limit replication of vaccinia virus. Virology. 2007;363:48-58.

     Not in our library10.1016/j.virol.2007.01.033

189. 189.

     Rocchetta HL, Boylan CJ, Foley JW, et al. Validation of a noninvasive, real-time imaging technology using bioluminescent Escherichia coli in the neutropenic mouse thigh model of infection. Antimicrob Agents Ch. 2001;45:129-137.

     Not in our library10.1128/aac.45.1.129-137.2001

190. 190.

     Saeij JP, Boyle JP, Grigg ME, Arrizabalaga G, Boothroyd JC. Bioluminescence imaging of Toxoplasma gondii infection in living mice reveals dramatic differences between strains. Infect Immun. 2005;73:695-702.

     Not in our library10.1128/iai.73.2.695-702.2005

191. 191.

     Sanz P, Teel LD, Alem F, Carvalho HM, Darnell SC, O'Brien AD. Detection of Bacillus anthracis spore germination in vivo by bioluminescence imaging. Infect Immun. 2008;76:1036-1047.

     Not in our library10.1128/iai.00985-07

192. 192.

     Sedgley C, Applegate B, Nagel A, Hall D. Real-time imaging and quantification of bioluminescent bacteria in root canals in vitro. J Endodont. 2004;30:893-898.

     Not in our library10.1097/01.don.0000132299.02265.6c

193. 193.

     Sedgley CM, Nagel AC, Hall D, Applegate B. Influence of irrigant needle depth in removing bioluminescent bacteria inoculated into instrumented root canals using real-time imaging in vitro. Int Endod J. 2005;38:97-104.

     Not in our library10.1111/j.1365-2591.2004.00906.x

194. 194.

     Shaner NC, Campbell RE, Steinbach PA, Giepmans BN, Palmer AE, Tsien RY. Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol. 2004;22:1567-1572.

     Not in our library10.1038/nbt1037

195. 195.

     Shaner NC, Steinbach PA, Tsien RY. A guide to choosing fluorescent proteins. Nat Methods. 2005;2:905-909.

     Not in our library10.1038/nmeth819

196. 196.

     Shaner NC, Patterson GH, Davidson MW. Advances in fluorescent protein technology. J Cell Sci. 2007;120:4247-4260.

     Not in our library10.1242/jcs.005801

197. 197.

     Shaner NC, Lin MZ, McKeown MR, Steinbach PA, Hazelwood KL, Davidson MW, Tsien RY. Improving the photostability of bright monomeric orange and red fluorescent proteins. Nat Methods. 2008;5:545-551.

     Not in our library10.1038/nmeth.1209

198. 198.

     Sharma PK, Engels E, Van Oeveren W, et al. Spatiotemporal progression of localized bacterial peritonitis before and after open abdomen lavage monitored by in vivo bioluminescent imaging. Surgery. 2010;147:89-97.

     Not in our library10.1016/j.surg.2009.05.016

199. 199.

     Shcherbo D, Merzlyak EM, Chepurnykh TV, et al. Bright far-red fluorescent protein for whole-body imaging. Nat Methods. 2007;4:741-746.

     Not in our library10.1038/nmeth1083

200. 200.

     Shcherbo D, Murphy CS, Ermakova GV, et al. Far-red fluorescent tags for protein imaging in living tissues. Biochem J. 2009;418:567-574.

     Not in our library10.1042/bj20081949

201. 201.

     Shimomura O. The discovery of aequorin and green fluorescent protein. J Microsc. 2005;217:1-15.

     Not in our library10.1111/j.0022-2720.2005.01441.x

202. 202.

     Shimomura O, Teranishi K. Light-emitters involved in the luminescence of coelenterazine. Luminescence. 2000;15:51-58.

     Not in our library10.1002/(sici)1522-7243(200001/02)15:1<51::aid-bio555>3.0.co;2-j

203. 203.

     Shimomura O, Johnson FH, Saiga Y. Extraction, purification and properties of aequorin, a bioluminescent protein from the luminous hydromedusan, Aequorea. J Cell Compar Physl. 1962;59:223-239.

     Not in our library10.1002/jcp.1030590302

204. 204.

     Shimomura O, Masugi T, Johnson FH, Haneda Y. Properties and reaction mechanism of the bioluminescence system of the deep-sea shrimp Oplophorus gracilorostris. Biochemistry. 1978;17:994-998.

     Not in our library10.1021/bi00599a008

205. 205.

     Shkrob MA, Yanushevich YG, Chudakov DM, et al. Far-red fluorescent proteins evolved from a blue chromoprotein from Actinia equina. Biochem J. 2005;392:649-654.

     Not in our library10.1042/bj20051314

206. 206.

     Shu X, Royant A, Lin MZ, Aguilera TA, Lev-Ram V, Steinbach PA, Tsien RY. Mammalian expression of infrared fluorescent proteins engineered from a bacterial phytochrome. Science. 2009;324:804-807.

     Not in our library10.1126/science.1168683

207. 207.

     Sjolinder H, Jonsson AB. Imaging of disease dynamics during meningococcal sepsis. PLoS ONE. 2007;2:e241.

     Not in our library10.1371/journal.pone.0000241

208. 208.

     So MK, Loening AM, Gambhir SS, Rao J. Creating self-illuminating quantum dot conjugates. Nat Protoc. 2006a;1:1160-1164.

     Not in our library10.1038/nprot.2006.162

209. 209.

     So MK, Xu C, Loening AM, Gambhir SS, Rao J. Self-illuminating quantum dot conjugates for in vivo imaging. Nat Biotechnol. 2006b;24:339-343.

     Not in our library10.1038/nbt1188

210. 210.

     Spaccapelo R, Janse CJ, Caterbi S, et al. Plasmepsin 4-deficient Plasmodium berghei are virulence attenuated and induce protective immunity against experimental malaria. Am J Pathol. 2010;176:205-217.

     Not in our library10.2353/ajpath.2010.090504

211. 211.

     Steinhuber A, Landmann R, Goerke C, Wolz C, Fluckiger U. Bioluminescence imaging to study the promoter activity of hla of Staphylococcus aureus in vitro and in vivo. Int J Med Microbiol. 2008;298:599-605.

     Not in our library10.1016/j.ijmm.2007.09.008

212. 212.

     Symonds EL, Riedel CU, O'Mahony D, Lapthorne S, O'Mahony L, Shanahan F. Involvement of T helper type 17 and regulatory T cell activity in Citrobacter rodentium invasion and inflammatory damage. Clin Exp Immunol. 2009;157:148-154.

     Not in our library10.1111/j.1365-2249.2009.03934.x

213. 213.

     Szittner R, Meighen E. Nucleotide sequence, expression, and properties of luciferase coded by lux genes from a terrestrial bacterium. J Biol Chem. 1990;265:16581-16587.

     Not in our library

214. 214.

     Talaat AM, Lyons R, Howard ST, Johnston SA. The temporal expression profile of Mycobacterium tuberculosis infection in mice. P Natl Acad Sci USA. 2004;101:4602-4607.

     Not in our library10.1073/pnas.0306023101

215. 215.

     Tamagnini I, Guglielmetti S, Mora D, Parini C, Canzi E, Karp M. Generation and comparison of bioluminescent and fluorescent Bacillus licheniformis. Curr Microbiol. 2008;57:245-250.

     Not in our library10.1007/s00284-008-9184-y

216. 216.

     Tannous BA, Kim DE, Fernandez JL, Weissleder R, Breakefield XO. Codon-optimized Gaussia luciferase cDNA for mammalian gene expression in culture and in vivo. Mol Ther. 2005;11:435-443.

     Not in our library10.1016/j.ymthe.2004.10.016

217. 217.

     Tarantal AF, Lee CC, Jimenez DF, Cherry SR. Fetal gene transfer using lentiviral vectors: in vivo detection of gene expression by microPET and optical imaging in fetal and infant monkeys. Hum Gene Ther. 2006;17:1254-1261.

     Not in our library10.1089/hum.2006.17.1254

218. 218.

     Taroni P, Pifferi A, Torricelli A, Comelli D, Cubeddu R. In vivo absorption and scattering spectroscopy of biological tissues. Photochem Photobio S. 2003;2:124-129.

     Not in our library10.1039/b209651j

219. 219.

     Thomson CM, Herring PJ, Campbell AK. The widespread occurrence and tissue distribution of the imidazolopyrazine luciferins. J Biolum Chemilum. 1997;12:87-91.

     Not in our library10.1002/(sici)1099-1271(199703/04)12:2<87::aid-bio438>3.0.co;2-8

220. 220.

     Troy T, Jekic-McMullen D, Sambucetti L, Rice B. Quantitative comparison of the sensitivity of detection of fluorescent and bioluminescent reporters in animal models. Mol Imaging. 2004;3:9-23.

     Not in our library10.1162/15353500200403196

221. 221.

     Trull FL, Rich BA. More regulation of rodents. Science. 1999;284:1463.

     Not in our library10.1126/science.284.5419.1463

222. 222.

     Tseng JC, Levin B, Hurtado A, et al. Systemic tumor targeting and killing by Sindbis viral vectors. Nat Biotechnol. 2004;22:70-77.

     Not in our library10.1038/nbt917

223. 223.

     Turner GM, Zacharakis G, Soubret A, Ripoll J, Ntziachristos V. Complete-angle projection diffuse optical tomography by use of early photons. Opt Lett. 2005;30:409-411.

     Not in our library10.1364/ol.30.000409

224. 224.

     2009.

     Not in our library

225. 225.

     Unge A, Tombolini R, Molbak L, Jansson JK. Simultaneous monitoring of cell number and metabolic activity of specific bacterial populations with a dual gfp-luxAB marker system. Appl Environ Microb. 1999;65:813-821.

     Not in our library10.1128/aem.65.2.813-821.1999

226. 226.
     Preclinical assessment of the treatment of second-stage African trypanosomiasis with cordycepin and deoxycoformycin. · 2009

     Not checked
227. 227.

     Vuong C, Kocianova S, Yu J, Kadurugamuwa JL, Otto M. Development of real-time in vivo imaging of device-related Staphylococcus epidermidis infection in mice and influence of animal immune status on susceptibility to infection. J Infect Dis. 2008;198:258-261.

     Not in our library10.1086/589307

228. 228.

     Vyas A, Kim SK, Giacomini N, Boothroyd JC, Sapolsky RM. Behavioral changes induced by Toxoplasma infection of rodents are highly specific to aversion of cat odors. P Natl Acad Sci USA. 2007;104:6442-6447.

     Not in our library10.1073/pnas.0608310104

229. 229.

     Wang G, Li Y, Jiang M. Uniqueness theorems in bioluminescence tomography. Med Phys. 2004a;31:2289-2299.

     Not in our library10.1118/1.1766420

230. 230.

     Wang L, Jackson WC, Steinbach PA, Tsien RY. Evolution of new nonantibody proteins via iterative somatic hypermutation. P Natl Acad Sci USA. 2004b;101:16745-16749.

     Not in our library10.1073/pnas.0407752101

231. 231.

     Weissleder R, Ntziachristos V. Shedding light onto live molecular targets. Nat Med. 2003;9:123-128.

     Not in our library10.1038/nm0103-123

232. 232.

     Welch WD. Effect of enflurane, isoflurane, and nitrous oxide on the microbicidal activity of human polymorphonuclear leukocytes. Anesthesiology. 1984;61:188-192.

     Not in our library10.1097/00000542-198408000-00012

233. 233.

     White DC, Dundas CR. Effect of anaesthetics on emission of light by luminous bacteria. Nature. 1970;226:456-458.

     Not in our library10.1038/226456a0

234. 234.

     Wiedenmann J, Schenk A, Rocker C, Girod A, Spindler KD, Nienhaus GU. A far-red fluorescent protein with fast maturation and reduced oligomerization tendency from Entacmaea quadricolor (Anthozoa, Actinaria). P Natl Acad Sci USA. 2002;99:11646-11651.

     Not in our library10.1073/pnas.182157199

235. 235.

     Wiles S. The influence of anaesthesia on bioluminescence imaging of infection. Luminescence. 2010;25:167-168.

     Not in our library

236. 236.

     Wiles S, Clare S, Harker J, Huett A, Young D, Dougan G, Frankel G. Organ specificity, colonization and clearance dynamics in vivo following oral challenges with the murine pathogen Citrobacter rodentium. Cell Microbiol. 2004;6:963-972.

     Not in our library10.1111/j.1462-5822.2004.00414.x

237. 237.

     Wiles S, Dougan G, Frankel G. Emergence of a ‘hyperinfectious’ bacterial state after passage of Citrobacter rodentium through the host gastrointestinal tract. Cell Microbiol. 2005a;7:1163-1172.

     Not in our library10.1111/j.1462-5822.2005.00544.x

238. 238.

     Wiles S, Ferguson K, Stefanidou M, Young DB, Robertson BD. Alternative luciferase for monitoring bacterial cells under adverse conditions. Appl Environ Microb. 2005b;71:3427-3432.

     Not in our library10.1128/aem.71.7.3427-3432.2005

239. 239.

     Wiles S, Hanage WP, Frankel G, Robertson B. Modelling infectious disease – time to think outside the box? Nat Rev Microbiol. 2006a;4:307-312.

     Not in our library10.1038/nrmicro1386

240. 240.

     Wiles S, Pickard KM, Peng K, MacDonald TT, Frankel G. In vivo bioluminescence imaging of the murine pathogen Citrobacter rodentium. Infect Immun. 2006b;74:5391-5396.

     Not in our library10.1128/iai.00848-06

241. 241.

     Wiles S, Crepin VF, Childs G, Frankel G, Kerton A. Use of biophotonic imaging as a training aid for administration of substances in laboratory rodents. Lab Anim. 2007;41:321-328.

     Not in our library10.1258/002367707781282785

242. 242.

     Wiles S, Robertson BD, Frankel G, Kerton A. Bioluminescent monitoring of in vivo colonization and clearance dynamics by light-emitting bacteria. Method Mol Biol. 2009;574:137-153.

     Not in our library10.1007/978-1-60327-321-3_12

243. 243.

     Winson MK, Swift S, Hill PJ, et al. Engineering the luxCDABE genes from Photorhabdus luminescens to provide a bioluminescent reporter for constitutive and promoter probe plasmids and mini-Tn5 constructs. FEMS Microbiol Lett. 1998;163:193-202.

     Not in our library10.1111/j.1574-6968.1998.tb13045.x

244. 244.

     Wood KV, Lam YA, Seliger HH, McElroy WD. Complementary DNA coding click beetle luciferases can elicit bioluminescence of different colors. Science. 1989;244:700-702.

     Not in our library10.1126/science.2655091

245. 245.

     Wright JS, Jin R, Novick RP. Transient interference with staphylococcal quorum sensing blocks abscess formation. P Natl Acad Sci USA. 2005;102:1691-1696.

     Not in our library10.1073/pnas.0407661102

246. 246.

     Xiong YQ, Willard J, Kadurugamuwa JL, Yu J, Francis KP, Bayer AS. Real-time in vivo bioluminescent imaging for evaluating the efficacy of antibiotics in a rat Staphylococcus aureus endocarditis model. Antimicrob Agents Ch. 2005;49:380-387.

     Not in our library10.1128/aac.49.1.380-387.2005

247. 247.

     Yu J, Wu J, Francis KP, Purchio TF, Kadurugamuwa JL. Monitoring in vivo fitness of rifampicin-resistant Staphylococcus aureus mutants in a mouse biofilm infection model. J Antimicrob Chemoth. 2005;55:528-534.

     Not in our library10.1093/jac/dki053

248. 248.

     Zacharakis G, Kambara H, Shih H, et al. Volumetric tomography of fluorescent proteins through small animals in vivo. P Natl Acad Sci USA. 2005a;102:18252-18257.

     Not in our library10.1073/pnas.0504628102

249. 249.

     Zacharakis G, Ripoll J, Weissleder R, Ntziachristos V. Fluorescent protein tomography scanner for small animal imaging. IEEE Trans Med Imaging. 2005b;24:878-885.

     Not in our library10.1109/tmi.2004.843254

250. 250.

     Zhang N, Weber A, Li B, Lyons R, Contag PR, Purchio AF, West DB. An inducible nitric oxide synthase-luciferase reporter system for in vivo testing of anti-inflammatory compounds in transgenic mice. J Immunol. 2003;170:6307-6319.

     Not in our library10.4049/jimmunol.170.12.6307

251. 251.

     Zhang Z, Rowe J, Wang W, Sommer M, Arvin A, Moffat J, Zhu H. Genetic analysis of varicella-zoster virus ORF0 to ORF4 by use of a novel luciferase bacterial artificial chromosome system. J Virol. 2007;81:9024-9033.

     Not in our library10.1128/jvi.02666-06

252. 252.

     Zhao H, Doyle TC, Coquoz O, Kalish F, Rice BW, Contag CH. Emission spectra of bioluminescent reporters and interaction with mammalian tissue determine the sensitivity of detection in vivo. J Biomed Opt. 2005a;10:41210.

     Not in our library10.1117/1.2032388

253. 253.

     Zhao M, Yang M, Baranov E, Wang X, Penman S, Moossa AR, Hoffman RM. Spatial–temporal imaging of bacterial infection and antibiotic response in intact animals. P Natl Acad Sci USA. 2001;98:9814-9818.

     Not in our library10.1073/pnas.161275798

254. 254.

     Zhao M, Yang M, Li XM, et al. Tumor-targeting bacterial therapy with amino acid auxotrophs of GFP-expressing Salmonella typhimurium. P Natl Acad Sci USA. 2005b;102:755-760.

     Not in our library10.1073/pnas.0408422102

255. 255.

     Zhao M, Geller J, Ma H, Yang M, Penman S, Hoffman RM. Monotherapy with a tumor-targeting mutant of Salmonella typhimurium cures orthotopic metastatic mouse models of human prostate cancer. P Natl Acad Sci USA. 2007;104:10170-10174.

     Not in our library10.1073/pnas.0703867104

256. 256.

     Zonios G, Bykowski J, Kollias N. Skin melanin, hemoglobin, and light scattering properties can be quantitatively assessed in vivo using diffuse reflectance spectroscopy. J Invest Dermatol. 2001;117:1452-1457.

     Not in our library10.1046/j.0022-202x.2001.01577.x

Cited by papers we hold 2

• Molecular insights into probiotic mechanisms of action employed against intestinal pathogenic bacteria · 2020
  No notice
• Neutrophil-derived IL-1β Is Sufficient for Abscess Formation in Immunity against Staphylococcus aureus in Mice · 2012
  No notice

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