Preclinical anatomical, molecular, and functional imaging of the lung with multiple modalities

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 306, Issue 10, 2014, Pages

  Gammon, Seth T ^a   Foje, Nathan ^b   Brewer, Elizabeth M ^c   Owers, Elizabeth ^b   Downs, Charles A ^d   Budde, Matthew D ^e   Leevy, W Matthew ^b   Helms, My N ^c  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b Department of Biological Sciences Notre Dame Integrated Imaging Facility   (United States)

^c EMORY UNIVERSITY   (United States)

^d EMORY UNIVERSITY   (United States)

^e MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

Epithelial sodium channels (ENaC) and fluid clearance; Image molecular events in vivo; Noninvasive lung imaging; PAO P1 lux bioluminescence; PET SPECT CT

Indexed keywords

BIOLUMINESCENCE; COMPUTER ASSISTED TOMOGRAPHY; FLUORESCENCE IMAGING; HUMAN; LUNG; LUNG DISEASE; MOLECULAR IMAGING; MULTIMODAL IMAGING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; REVIEW; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY; X RAY; ANIMAL; LUNG DISEASES; PATHOLOGY; RADIOGRAPHY;

ANIMALS; HUMANS; LUNG; LUNG DISEASES; MAGNETIC RESONANCE IMAGING; OPTICAL IMAGING; POSITRON-EMISSION TOMOGRAPHY; TOMOGRAPHY, X-RAY COMPUTED;

EID: 84900823117     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00007.2014     Document Type: Review

References (163)

1. Abascal JF, Aguirre J, Chamorro-Servent J, Schweiger M, Arridge S, Ripoll J, Vaquero JJ, Desco M. Influence of absorption and scattering on the quantification of fluorescence diffuse optical tomography using normalized data. J Biomed Opt 17: 036013, 2012.
2. Aghi M, Hochberg F, Breakefield XO. Prodrug activation enzymes in cancer gene therapy. J Gene Med 2: 148-164, 2000.
3. Akhavan Sharif MR, Lam WW, Ouriadov AV, Holdsworth DW, Santyr GE. Comparison of hyperpolarized 3He MRI rat lung volume measurement with micro-computed tomography. NMR Biomed 23: 359-367, 2010.
4. Alauddin MM, Gelovani JG. Pyrimidine nucleosides in molecular PET imaging of tumor proliferation. Curr Med Chem 17: 1010-1029, 2010.
5. Alauddin MM, Shahinian A, Gordon EM, Bading JR, Conti PS. Preclinical evaluation of the penciclovir analog 9-(4-[18F]fluoro-3-hydroxymethylbutyl) guanine for in vivo measurement of suicide gene expression with PET. J Nucl Med 42: 1682-1690, 2001.
6. Albert MS, Cates GD, Driehuys B, Happer W, Saam B, Springer CS Jr, Wishnia A. Biological magnetic resonance imaging using laserpolarized 129Xe. Nature 370: 199-201, 1994.
7. Alshoukr F, Prignon A, Brans L, Jallane A, Mendes S, Talbot JN, Tourwe D, Barbet J, Gruaz-Guyon A. Novel DOTA-neurotensin analogues for 111In scintigraphy and 68Ga PET imaging of neurotensin receptor-positive tumors. Bioconjug Chem 22: 1374-1385, 2011.
8. Ambrosini V, Nanni C, Pettinato C, Fini M, D'Errico A, Trepidi S, Spinelli A, Al-Nahhas A, Rubello D, Zompatori M, Fabbri M, Franchi R, Fanti S. Assessment of a chemically induced model of lung squamous cell carcinoma in mice by 18F-FDG small-animal PET. Nucl Med Commun 28: 647-652, 2007.
9. Ando Y, Niwa K, Yamada N, Enomoto T, Irie T, Kubota H, Ohmiya Y, Akiyama H. Firefly bioluminescence quantum yield and colour change by pH-sensitive green emission. Nature Photonics 2: 44-47, 2008.
10. Armitage SE, Pollmann SI, Detombe SA, Drangova M. Least-error projection sorting to optimize retrospectively gated cardiac micro-CT of free-breathing mice. Med Phys 39: 1452-1461, 2012.
11. Artaechevarria X, Blanco D, de Biurrun G, Ceresa M, Perez-Martin D, Bastarrika G, de Torres JP, Zulueta JJ, Montuenga LM, Ortizde-Solorzano C, Munoz-Barrutia A. Evaluation of micro-CT for emphysema assessment in mice: comparison with non-radiological techniques. Eur Radiol 21: 954-962, 2011.
12. Artaechevarria X, Blanco D, Perez-Martin D, de Biurrun G, Montuenga LM, de Torres JP, Zulueta JJ, Bastarrika G, Munoz-Barrutia A, Ortiz-de-Solorzano C. Longitudinal study of a mouse model of chronic pulmonary inflammation using breath hold gated micro-CT. Eur Radiol 20: 2600-2608, 2010.
13. Awadh N, Muller NL, Park CS, Abboud RT, FitzGerald JM. Airway wall thickness in patients with near fatal asthma and control groups: assessment with high resolution computed tomographic scanning. Thorax 53: 248-253, 1998.
14. Badea CT, Guo X, Clark D, Johnston SM, Marshall CD, Piantadosi CA. Dual-energy micro-CT of the rodent lung. Am J Physiol Lung Cell Mol Physiol 302: L1088-L1097, 2012.
15. Bakhtiar R. Biomarkers in drug discovery and development. J Pharmacol Toxicol Methods 57: 85-91, 2008.
16. Beckmann N, Laurent D, Tigani B, Panizzutti R, Rudin M. Magnetic resonance imaging in drug discovery: lessons from disease areas. Drug Discov Today 9: 35-42, 2004.
17. Beckmann N, Tigani B, Ekatodramis D, Borer R, Mazzoni L, Fozard JR. Pulmonary edema induced by allergen challenge in the rat: noninvasive assessment by magnetic resonance imaging. Magn Reson Med 45: 88-95, 2001.
18. Bell LC, Johnson KM, Fain SB, Wentland A, Drees R, Johnson RA, Bauman G, Francois CJ, Nagle SK. Simultaneous MRI of lung structure and perfusion in a single breathhold. J Magn Reson Imaging 2013 Dec 20. doi: 10.1002/jmri.24520. [Epub ahead of print]
19. Belur LR, Podetz-Pedersen K, Frandsen J, McIvor RS. Lung-directed gene therapy in mice using the nonviral Sleeping Beauty transposon system. Nat Protoc 2: 3146-3152, 2007.
20. Bennett WD. Effect of beta-adrenergic agonists on mucociliary clearance. J Allergy Clin Immunol 110: S291-S297, 2002.
21. Berezin MY, Achilefu S. Fluorescence lifetime measurements and biological imaging. Chem Rev 110: 2641-2684, 2010.
22. Bottiroli G, Croce AC. Autofluorescence spectroscopy of cells and tissues as a tool for biomedical diagnosis. Photochem Photobiol Sci 3: 189-210, 2004.
23. Branca RT, Cleveland ZI, Fubara B, Kumar CS, Maronpot RR, Leuschner C, Warren WS, Driehuys B. Molecular MRI for sensitive and specific detection of lung metastases. Proc Natl Acad Sci USA 107: 3693-3697, 2010.
24. Branchini BR, Ablamsky DM, Murtiashaw MH, Uzasci L, Fraga H, Southworth TL. Thermostable red and green light-producing firefly luciferase mutants for bioluminescent reporter applications. Anal Biochem 361: 253-262, 2007.
25. Caravan P, Yang Y, Zachariah R, Schmitt A, Mino-Kenudson M, Chen HH, Sosnovik DE, Dai G, Fuchs BC, Lanuti M. Molecular magnetic resonance imaging of pulmonary fibrosis in mice. Am J Respir Cell Mol Biol 49: 1120-1126, 2013.
26. Carlon M, Toelen J, Van der Perren A, Vandenberghe LH, Reumers V, Sbragia L, Gijsbers R, Baekelandt V, Himmelreich U, Wilson JM, Deprest J, Debyser Z. Efficient gene transfer into the mouse lung by fetal intratracheal injection of rAAV2/6.2. Mol Ther 18: 2130-2138, 2010.
27. Chang CH, Wang HE, Wu SY, Fan KH, Tsai TH, Lee TW, Chang SR, Liu RS, Chen CF, Chen CH, Fu YK. Comparative evaluation of FET and FDG for differentiating lung carcinoma from inflammation in mice. Anticancer Res 26: 917-925, 2006.
28. Chapman SE, Diener JM, Sasser TA, Correcher C, Gonzalez AJ, Avermaete TV, Leevy WM. Dual tracer imaging of SPECT and PET probes in living mice using a sequential protocol. Am J Nucl Med Mol Imaging 2: 405-414, 2012.
29. Chen BT, Brau AC, Johnson GA. Measurement of regional lung function in rats using hyperpolarized 3helium dynamic MRI. Magn Reson Med 49: 78-88, 2003.
30. Chen DL, Bedient TJ, Kozlowski J, Rosenbluth DB, Isakow W, Ferkol TW, Thomas B, Mintun MA, Schuster DP, Walter MJ. [18F]fluorodeoxyglucose positron emission tomography for lung antiinflammatory response evaluation. Am J Respir Crit Care Med 180: 533-539, 2009.
31. Chen DL, Schuster DP. Positron emission tomography with [18F]fluorodeoxyglucose to evaluate neutrophil kinetics during acute lung injury. Am J Physiol Lung Cell Mol Physiol 286: L834-L840, 2004.
32. Chen K, Conti PS. Target-specific delivery of peptide-based probes for PET imaging. Adv Drug Deliv Rev 62: 1005-1022, 2010.
33. Chen XJ, Hedlund LW, Moller HE, Chawla MS, Maronpot RR, Johnson GA. Detection of emphysema in rat lungs by using magnetic resonance measurements of 3He diffusion. Proc Natl Acad Sci USA 97: 11478-11481, 2000.
34. Cherry SR. In vivo molecular and genomic imaging: new challenges for imaging physics. Phys Med Biol 49: R13-R48, 2004.
35. Cherry SR. Multimodality in vivo imaging systems: twice the power or double the trouble? Annu Rev Biomed Eng 8: 35-62, 2006.
36. Cherry SR. Multimodality imaging: beyond PET/CT and SPECT/CT. Semin Nucl Med 39: 348-353, 2009.
37. Church JE, Fulton D. Differences in eNOS activity because of subcellular localization are dictated by phosphorylation state rather than the local calcium environment. J Biol Chem 281: 1477-1488, 2006.
38. Contag CH, Bachmann MH. Advances in in vivo bioluminescence imaging of gene expression. Annu Rev Biomed Eng 4: 235-260, 2002.
39. Contag CH, Spilman SD, Contag PR, Oshiro M, Eames B, Dennery P, Stevenson DK, Benaron DA. Visualizing gene expression in living mammals using a bioluminescent reporter. Photochem Photobiol 66: 523-531, 1997.
40. Conti E, Franks NP, Brick P. Crystal structure of firefly luciferase throws light on a superfamily of adenylate-forming enzymes. Structure 4: 287-298, 1996.
41. Counter WB, Wang IQ, Farncombe TH, Labiris NR. Airway and pulmonary vascular measurements using contrast-enhanced micro-CT in rodents. Am J Physiol Lung Cell Mol Physiol 304: L831-L843, 2013.
42. D'Ambrosio D, Zagni F, Spinelli AE, Marengo M. Attenuation correction for small animal PET images: a comparison of two methods. Comput Math Methods Med 2013: 103476, 2013.
43. Dahan M, Laurence T, Pinaud F, Chemla DS, Alivisatos AP, Sauer M, Weiss S. Time-gated biological imaging by use of colloidal quantum dots. Opt Lett 26: 825-827, 2001.
44. Damron FH, McKenney ES, Schweizer HP, Goldberg JB. Construction of a broad-host-range Tn7-based vector for single-copy P(BAD)-controlled gene expression in gram-negative bacteria. Appl Environ Microbiol 79: 718-721, 2013.
45. Davison CA, Durbin SM, Thau MR, Zellmer VR, Chapman SE, Diener J, Wathen C, Leevy WM, Schafer ZT. Antioxidant enzymes mediate survival of breast cancer cells deprived of extracellular matrix. Cancer Res 73: 3704-3715, 2013.
46. Davison CA, Chapman SE, Sasser TA, Wathen C, Diener J, Schafer ZT, Leevy WM. Multimodal optical, X-ray CT, and SPECT imaging of a mouse model of breast cancer lung metastasis. Curr Mol Med 13: 368-376, 2013.
47. De Langhe E, Vande Velde G, Hostens J, Himmelreich U, Nemery B, Luyten FP, Vanoirbeek J, Lories RJ. Quantification of lung fibrosis and emphysema in mice using automated micro-computed tomography. PLoS One 7: e43123, 2012.
48. De Langhe E, Vande Velde G, Hostens J, Himmelreich U, Nemery B, Luyten FP, Vanoirbeek J, Lories RJ. Quantification of lung fibrosis and emphysema in mice using automated micro-computed tomography. PLoS One 7: e43123, 2012.
49. Dikalov S, Griendling KK, Harrison DG. Measurement of reactive oxygen species in cardiovascular studies. Hypertension 49: 717-727, 2007.
50. Downs CA, Helms MN. Regulation of ion transport by oxidants. Am J Physiol Lung Cell Mol Physiol 305: L595-L603, 2013.
51. Downs CA, Kriener LH, Yu L, Eaton DC, Jain L, Helms MN. β-Adrenergic agonists differentially regulate highly selective and nonselective epithelial sodium channels to promote alveolar fluid clearance in vivo. Am J Physiol Lung Cell Mol Physiol 302: L1167-L1178, 2012.
52. Downs CA, Kumar A, Kreiner LH, Johnson NM, Helms MN. H2O2 regulates lung ENaC via ubiquitin-like protein Nedd8. J Biol Chem 288: 8136-8145, 2013.
53. Egger C, Cannet C, Gerard C, Jarman E, Jarai G, Feige A, Suply T, Micard A, Dunbar A, Tigani B, Beckmann N. Administration of bleomycin via the oropharyngeal aspiration route leads to sustained lung fibrosis in mice and rats as quantified by UTE-MRI and histology. PLoS One 8: e63432, 2013.
54. Farncombe TH. Software-based respiratory gating for small animal conebeam CT. Med Phys 35: 1785-1792, 2008.
55. Floyd E, McShane TM. Development and use of biomarkers in oncology drug development. Toxicol Pathol 32, Suppl 1: 106-115, 2004.
56. Foster WM, Wagner EM. Bronchial edema alters 99mTc-DTPA clearance from the airway surface in sheep. J Appl Physiol 91: 2567-2573, 2001.
57. Fox MS, Ouriadov A, Santyr GE. Comparison of hyperpolarized He and Xe MRI for the measurement of absolute ventilated lung volume in rats. Magn Reson Med 2013 May 6. doi: 10.1002/mrm.24746. [Epub ahead of print]
58. Franc BL, Acton PD, Mari C, Hasegawa BH. Small-animal SPECT and SPECT/CT: important tools for preclinical investigation. J Nucl Med 49: 1651-1663, 2008.
59. Francis KP, Yu J, Bellinger-Kawahara C, Joh D, Hawkinson MJ, Xiao G, Purchio TF, Caparon MG, Lipsitch M, Contag PR. Visualizing pneumococcal infections in the lungs of live mice using bioluminescent Streptococcus pneumoniae transformed with a novel grampositive lux transposon. Infect Immun 69: 3350-3358, 2001.
60. Gammon ST, Leevy WM, Gross S, Gokel GW, Piwnica-Worms D. Spectral unmixing of multicolored bioluminescence emitted from heterogeneous biological sources. Anal Chem 78: 1520-1527, 2006.
61. Gao X, Cui Y, Levenson RM, Chung LW, Nie S. In vivo cancer targeting and imaging with semiconductor quantum dots. Nat Biotechnol 22: 969-976, 2004.
62. Goodson P, Kumar A, Jain L, Kundu K, Murthy N, Koval M, Helms MN. Nadph oxidase regulates alveolar epithelial sodium channel activity and lung fluid balance in vivo via O2-signaling. Am J Physiol Lung Cell Mol Physiol 302: L410-L419, 2012.
63. Gould SJ, Subramani S. Firefly luciferase as a tool in molecular and cell biology. Anal Biochem 175: 5-13, 1988.
64. Gross S, Abraham U, Prior JL, Herzog ED, Piwnica-Worms D. Continuous delivery of D-luciferin by implanted micro-osmotic pumps enables true real-time bioluminescence imaging of luciferase activity in vivo. Mol Imaging 6: 121-130, 2007.
65. Gross S, Piwnica-Worms D. Real-time imaging of ligand-induced IKK activation in intact cells and in living mice. Nat Methods 2: 607-614, 2005.
66. Gu L, Hall DJ, Qin Z, Anglin E, Joo J, Mooney DJ, Howell SB, Sailor MJ. In vivo time-gated fluorescence imaging with biodegradable luminescent porous silicon nanoparticles. Nat Commun 4: 2326, 2013.
67. Hardwick MJ, Chen MK, Baidoo K, Pomper MG, Guilarte TR. In vivo imaging of peripheral benzodiazepine receptors in mouse lungs: a biomarker of inflammation. Mol Imaging 4: 432-438, 2005.
68. Hasegawa BH, Iwata K, Wong KH, Wu MC, Da Silva AJ, Tang HR, Barber WC, Hwang AH, Sakdinawat AE. Dual-modality imaging of function and physiology. Acad Radiol 9: 1305-1321, 2002.
69. Hatori A, Yui J, Yamasaki T, Xie L, Kumata K, Fujinaga M, Yoshida Y, Ogawa M, Nengaki N, Kawamura K, Fukumura T, Zhang MR. PET imaging of lung inflammation with [18F]FEDAC, a radioligand for translocator protein (18 kDa). PLoS One 7: e45065, 2012.
70. Hayakawa T, Mutoh M, Imai T, Tsuta K, Yanaka A, Fujii H, Yoshimoto M. SPECT/CT of lung nodules using 111In-DOTA-c(RGDfK) in a mouse lung carcinogenesis model. Ann Nucl Med 27: 640-647, 2013.
71. Hedlund LW, Johnson GA. Mechanical ventilation for imaging the small animal lung. ILAR J 43: 159-174, 2002.
72. Helms MN, Torres-Gonzalez E, Goodson P, Rojas M. Direct tracheal instillation of solutes into mouse lung. J Vis Exp 42: 1942, 2010.
73. Hori Y, Takasuka N, Mutoh M, Kitahashi T, Kojima S, Imaida K, Suzuki M, Kohara K, Yamamoto S, Moriyama N, Sugimura T, Wakabayashi K. Periodic analysis of urethane-induced pulmonary tumors in living A/J mice by respiration-gated X-ray microcomputed tomography. Cancer Sci 99: 1774-1777, 2008.
74. Iyer M, Berenji M, Templeton NS, Gambhir SS. Noninvasive imaging of cationic lipid-mediated delivery of optical and PET reporter genes in living mice. Mol Ther 6: 555-562, 2002.
75. Jenkins DE, Oei Y, Hornig YS, Yu SF, Dusich J, Purchio T, Contag PR. Bioluminescent imaging (BLI) to improve and refine traditional murine models of tumor growth and metastasis. Clin Exp Metastasis 20: 733-744, 2003.
76. Jobse BN, Johnson JR, Farncombe TH, Labiris R, Walker TD, Goncharova S, Jordana M. Evaluation of allergic lung inflammation by computed tomography in a rat model in vivo. Eur Respir J 33: 1437-1447, 2009.
77. Jobse BN, Rhem RG, Wang IQ, Counter WB, Stampfli MR, Labiris NR. Detection of lung dysfunction using ventilation and perfusion SPECT in a mouse model of chronic cigarette smoke exposure. J Nucl Med 54: 616-623, 2013.
78. Johnson EM, Price RE, Kurie JM, Rivera BS, Cody DD. A new method for respiratory gating during microcomputed tomography of lung in mice. J Am Assoc Lab Anim Sci 47: 46-56, 2008.
79. Johnson GA, Cofer GP, Hedlund LW, Maronpot RR, Suddarth SA. Registered 1H and 2He magnetic resonance microscopy of the lung. Magn Reson Med 45: 365-370, 2001.
80. Jones HA, Cadwallader KA, White JF, Uddin M, Peters AM, Chilvers ER. Dissociation between respiratory burst activity and deoxyglucose uptake in human neutrophil granulocytes: implications for interpretation of 18F-FDG PET images. J Nucl Med 43: 652-657, 2002.
81. Jones HA, Clark RJ, Rhodes CG, Schofield JB, Krausz T, Haslett C. In vivo measurement of neutrophil activity in experimental lung inflammation. Am J Respir Crit Care Med 149: 1635-1639, 1994.
82. Kazzaz JA, Strayer MS, Wu J, Malone DJ, Koo HC, Shaffer TH, Davis JM, Strayer DS, Wolfson MR. Perfluorochemical liquid-adenovirus suspensions enhance gene delivery to the distal lung. Pulm Med 2011: 918036, 2011.
83. Kitchen MJ, Lewis RA, Yagi N, Uesugi K, Paganin D, Hooper SB, Adams G, Jureczek S, Singh J, Christensen CR, Hufton AP, Hall CJ, Cheung KC, Pavlov KM. Phase contrast X-ray imaging of mice and rabbit lungs: a comparative study. Br J Radiol 78: 1018-1027, 2005.
84. Kitchen MJ, Paganin D, Lewis RA, Yagi N, Uesugi K, Mudie ST. On the origin of speckle in x-ray phase contrast images of lung tissue. Phys Med Biol 49: 4335-4348, 2004.
85. Kitchen M, Paganin D, Lewis R, Yagi N, Uesugi K. Analysis of speckle patterns in phase-contrast images of lung tissue. Nucl Instrum Meth A 548: 240-246, 2005.
86. Kobayashi S, Fujinawa R, Ota F, Kobayashi S, Angata T, Ueno M, Maeno T, Kitazume S, Yoshida K, Ishii T, Gao C, Ohtsubo K, Yamaguchi Y, Betsuyaku T, Kida K, Taniguchi N. A single dose of lipopolysaccharide into mice with emphysema mimics human chronic obstructive pulmonary disease exacerbation as assessed by micro-computed tomography. Am J Respir Cell Mol Biol 49: 971-977, 2013.
87. Kocher B, Piwnica-Worms D. Illuminating cancer systems with genetically engineered mouse models and coupled luciferase reporters in vivo. Cancer Discov 3: 616-629, 2013.
88. Kundu K, Knight SF, Willett N, Lee S, Taylor WR, Murthy N. Hydrocyanines: a class of fluorescent sensors that can image reactive oxygen species in cell culture, tissue, and in vivo. Angew Chem Int Ed Engl 48: 299-303, 2009.
89. Lam WW, Holdsworth DW, Du LY, Drangova M, McCormack DG, Santyr GE. Micro-CT imaging of rat lung ventilation using continuous image acquisition during xenon gas contrast enhancement. J Appl Physiol 103: 1848-1856, 2007.
90. Lang TF, Hasegawa BH, Liew SC, Brown JK, Blankespoor SC, Reilly SM, Gingold EL, Cann CE. Description of a prototype emissiontransmission computed tomography imaging system. J Nucl Med 33: 1881-1887, 1992.
91. Lederlin M, Ozier A, Dournes G, Ousova O, Girodet PO, Begueret H, Marthan R, Montaudon M, Laurent F, Berger P. In vivo micro-CT assessment of airway remodeling in a flexible OVA-sensitized murine model of asthma. PLoS One 7: e48493, 2012.
92. Lederlin M, Ozier A, Montaudon M, Begueret H, Ousova O, Marthan R, Berger P, Laurent F. Airway remodeling in a mouse asthma model assessed by in-vivo respiratory-gated micro-computed tomography. Eur Radiol 20: 128-137, 2010.
93. Lee HH, Chen JC. Investigation of attenuation correction for small animal single photon emission computed tomography. Comput Math Methods Med 430276, 2013.
94. Lee HW, Jeon YH, Hwang MH, Kim JE, Park TI, Ha JH, Lee SW, Ahn BC, Lee J. Dual reporter gene imaging for tracking macrophage migration using the human sodium iodide symporter and an enhanced firefly luciferase in a murine inflammation model. Mol Imaging Biol 15: 703-712, 2013.
95. Lewis RA, Yagi N, Kitchen MJ, Morgan MJ, Paganin D, Siu KK, Pavlov K, Williams I, Uesugi K, Wallace MJ, Hall CJ, Whitley J, Hooper SB. Dynamic imaging of the lungs using x-ray phase contrast. Phys Med Biol 50: 5031-5040, 2005.
96. Liew SC, Hasegawa BH. Noise, resolution, and sensitivity considerations in the design of a single-slice emission-transmission computed tomographic system. Med Phys 18: 1002-1015, 1991.
97. Luangsay S, Wittamer V, Bondue B, De Henau O, Rouger L, Brait M, Franssen JD, de Nadai P, Huaux F, Parmentier M. Mouse ChemR23 is expressed in dendritic cell subsets and macrophages, and mediates an anti-inflammatory activity of chemerin in a lung disease model. J Immunol 183: 6489-6499, 2009.
98. Luker GD, Sharma V, Pica CM, Dahlheimer JL, Li W, Ochesky J, Ryan CE, Piwnica-Worms H, Piwnica-Worms D. Noninvasive imaging of protein-protein interactions in living animals. Proc Natl Acad Sci USA 99: 6961-6966, 2002.
99. Matute-Bello G, Downey G, Moore BB, Groshong SD, Matthay MA, Slutsky AS, Kuebler WM. An official American Thoracic Society workshop report: features and measurements of experimental acute lung injury in animals. Am J Respir Cell Mol Biol 44: 725-738, 2011.
100. Mclean AN, Sproule MW, Cowan MD, Thomson NC. High resolution computed tomography in asthma. Thorax 53: 308-314, 1998.
101. Meighen EA. Molecular biology of bacterial bioluminescence. Microbiol Rev 55: 123-142, 1991.
102. Mistry NN, Pollaro J, Song J, De LM, Johnson GA. Pulmonary perfusion imaging in the rodent lung using dynamic contrast-enhanced MRI. Magn Reson Med 59: 289-297, 2008.
103. Mizgerd JP, Skerrett SJ. Animal models of human pneumonia. Am J Physiol Lung Cell Mol Physiol 294: L387-L398, 2008.
104. Mora AL, LaVoy J, McKean M, Stecenko A, Brigham KL, Parker R, Rojas M. Prevention of NF-κB activation in vivo by a cell-permeable NF-κB inhibitor peptide. Am J Physiol Lung Cell Mol Physiol 289: L536-L544, 2005.
105. Namati E, Thiesse J, Sieren JC, Ross A, Hoffman EA, McLennan G. Longitudinal assessment of lung cancer progression in the mouse using in vivo micro-CT imaging. Med Phys 37: 4793-4805, 2010.
106. Narayanan M, Owers-Bradley J, Beardsmore CS, Mada M, Ball I, Garipov R, Panesar KS, Kuehni CE, Spycher BD, Williams SE, Silverman M. Alveolarization continues during childhood and adolescence: new evidence from helium-3 magnetic resonance. Am J Respir Crit Care Med 185: 186-191, 2012.
107. Niu G, Krager KJ, Graham MM, Hichwa RD, Domann FE. Noninvasive radiological imaging of pulmonary gene transfer and expression using the human sodium iodide symporter. Eur J Nucl Med Mol Imaging 32: 534-540, 2005.
108. O'Neill K, Venegas JG, Richter T, Harris RS, Layfield JD, Musch G, Winkler T, Melo MF. Modeling kinetics of infused 13NN-saline in acute lung injury. J Appl Physiol 95: 2471-2484, 2003.
109. Orndorff RL, Hong N, Yu K, Feinstein SI, Zern BJ, Fisher AB, Muzykantov VR, Chatterjee S. NOX2 in lung inflammation: quantum dot based in situ imaging of NOX2-mediated expression of vascular cell adhesion molecule-1. Am J Physiol Lung Cell Mol Physiol 306: L260-L268, 2014.
110. Overhage J, Lewenza S, Marr AK, Hancock RE. Identification of genes involved in swarming motility using a Pseudomonas aeruginosa PAO1 mini-Tn5-lux mutant library. J Bacteriol 189: 2164-2169, 2007.
111. Paulus MJ, Gleason SS, Kennel SJ, Hunsicker PR, Johnson DK. High resolution X-ray computed tomography: an emerging tool for small animal cancer research. Neoplasia 2: 62-70, 2000.
112. Peces-Barba G, Ruiz-Cabello J, Cremillieux Y, Rodriguez I, Dupuich D, Callot V, Ortega M, Rubio Arbo ML, Cortijo M, Gonzalez-Mangado N. Helium-3 MRI diffusion coefficient: correlation to morphometry in a model of mild emphysema. Eur Respir J 22: 14-19, 2003.
113. Petrik M, Haas H, Dobrozemsky G, Lass-Florl C, Helbok A, Blatzer M, Dietrich H, Decristoforo C. 68Ga-siderophores for PET imaging of invasive pulmonary aspergillosis: proof of principle. J Nucl Med 51: 639-645, 2010.
114. Petrik M, Haas H, Schrettl M, Helbok A, Blatzer M, Decristoforo C. In vitro and in vivo evaluation of selected 68Ga-siderophores for infection imaging. Nucl Med Biol 39: 361-369, 2012.
115. Postnov AA, Meurrens K, Weiler H, Van Dyck D, Xu H, Terpstra P, De Clerck NM. In vivo assessment of emphysema in mice by high resolution X-ray microtomography. J Microsc 220: 70-75, 2005.
116. Prasad MN, Brown MS, Ahmad S, Abtin F, Allen J, da Costa I, Kim HJ, McNitt-Gray MF, Goldin JG. Automatic segmentation of lung parenchyma in the presence of diseases based on curvature of ribs. Acad Radiol 15: 1173-1180, 2008.
117. Prescher JA, Contag CH. Guided by the light: visualizing biomolecular processes in living animals with bioluminescence. Curr Opin Chem Biol 14: 80-89, 2010.
118. Pu J, Roos J, Yi CA, Napel S, Rubin GD, Paik DS. Adaptive border marching algorithm: automatic lung segmentation on chest CT images. Comput Med Imaging Graph 32: 452-462, 2008.
119. Qian F, Deng J, Gantner BN, Flavell RA, Dong C, Christman JW, Ye RD. Map kinase phosphatase 5 protects against sepsis-induced acute lung injury. Am J Physiol Lung Cell Mol Physiol 302: L866-L874, 2012.
120. Rab A, Rowe SM, Raju SV, Bebok Z, Matalon S, Collawn JF. Cigarette smoke and CFTR: implications in the pathogenesis of COPD. Am J Physiol Lung Cell Mol Physiol 305: L530-L541, 2013.
121. Radotic K, Radenovic C, Jeremic M. Spontaneous ultraweak bioluminescence in plants: origin, mechanisms and properties. Gen Physiol Biophys 17: 289-308, 1998.
122. Ramirez MP, Sigaloff KC, Kubatina LV, Donahue MA, Venkatesh AK, Albert MS. Physiological response of rats to delivery of helium and xenon: implications for hyperpolarized noble gas imaging. NMR Biomed 13: 253-264, 2000.
123. Rao J, Dragulescu-Andrasi A, Yao H. Fluorescence imaging in vivo: recent advances. Curr Opin Biotechnol 18: 17-25, 2007.
124. Reidy MF, Wright JR. Surfactant protein A enhances apoptotic cell uptake and TGF-beta1 release by inflammatory alveolar macrophages. Am J Physiol Lung Cell Mol Physiol 285: L854-L861, 2003.
125. Richard JC, Zhou Z, Ponde DE, Dence CS, Factor P, Reynolds PN, Luker GD, Sharma V, Ferkol T, Piwnica-Worms D, Schuster DP. Imaging pulmonary gene expression with positron emission tomography. Am J Respir Crit Care Med 167: 1257-1263, 2003.
126. Ritman EL. Current status of developments and applications of micro-CT. Annu Rev Biomed Eng 13: 531-552, 2011.
127. Rodrigues TB, Serrao EM, Kennedy BW, Hu DE, Kettunen MI, Brindle KM. Magnetic resonance imaging of tumor glycolysis using hyperpolarized C-labeled glucose. Nat Med 20: 93-97, 2013.
128. Rogers CS, Abraham WM, Brogden KA, Engelhardt JF, Fisher JT, McCray PB Jr, McLennan G, Meyerholz DK, Namati E, Ostedgaard LS, Prather RS, Sabater JR, Stoltz DA, Zabner J, Welsh MJ. The porcine lung as a potential model for cystic fibrosis. Am J Physiol Lung Cell Mol Physiol 295: L240-L263, 2008.
129. Salerno M, Altes TA, Brookeman JR, de Lange EE, Mugler JP. Dynamic spiral MRI of pulmonary gas flow using hyperpolarized 3He: preliminary studies in healthy and diseased lungs. Magn Reson Med 46: 667-677, 2001.
130. Sanchez F, Orero A, Soriano A, Correcher C, Conde P, Gonzalez A, Hernandez L, Moliner L, Rodriguez-Alvarez MJ, Vidal LF, Benlloch JM, Chapman SE, Leevy WM. ALBIRA: a small animal PETSPECTCT imaging system. Med Phys 40: 051906, 2013.
131. 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 76: 1036-1047, 2008.
132. Schagat TL, Wofford JA, Greene KE, Wright JR. Surfactant protein A differentially regulates peripheral and inflammatory neutrophil chemotaxis. Am J Physiol Lung Cell Mol Physiol 284: L140-L147, 2003.
133. Schuster DP, Brody SL, Zhou Z, Bernstein M, Arch R, Link D, Mueckler M. Regulation of lipopolysaccharide-induced increases in neutrophil glucose uptake. Am J Physiol Lung Cell Mol Physiol 292: L845-L851, 2007.
134. Schuster DP, Kozlowski J, Hogue L. Imaging lung inflammation in a murine model of Pseudomonas infection: a positron emission tomography study. Exp Lung Res 29: 45-57, 2003.
135. Sen SK, Jin X, Holzner C, Narayanan S, Liu B, Wang D, Agah M, Wang L, Yu H, Wang G. Experimental studies on few-view reconstruction for high-resolution micro-CT. J Xray Sci Technol 21: 25-42, 2013.
136. Shaner NC, Steinbach PA, Tsien RY. A guide to choosing fluorescent proteins. Nat Methods 2: 905-909, 2005.
137. Signore A, Mather SJ, Piaggio G, Malviya G, Dierckx RA. Molecular imaging of inflammation/infection: nuclear medicine and optical imaging agents and methods. Chem Rev 110: 3112-3145, 2010.
138. Slavinsky AA. Index of phagocyte activation based on luminescence of dehydrogenase coenzymes. Folia Haematol Int Mag Klin Morphol Blutforsch 117: 365-368, 1990.
139. Sluimer I, Prokop M, van Ginneken B. Toward automated segmentation of the pathological lung in CT. IEEE Trans Med Imaging 24: 1025-1038, 2005.
140. Sundram FX. Clinical studies of alveolar-capillary permeability using technetium-99m DTPA aerosol. Ann Nucl Med 9: 171-178, 1995.
141. Sundram FX, Lee ST. Radionuclide lung scanning in the management of respiratory burns. Ann Acad Med Singapore 21: 630-634, 1992.
142. Takahashi M, Togao O, Obara M, van Cauteren M, Ohno Y, Doi S, Kuro-o M, Malloy C, Hsia CC, Dimitrov I. Ultra-short echo time (UTE) MR imaging of the lung: comparison between normal and emphysematous lungs in mutant mice. J Magn Reson Imaging 32: 326-333, 2010.
143. Takemura Y, Helms MN, Eaton AF, Self J, Ramosevac S, Jain L, Bao HF, Eaton DC. Cholinergic regulation of epithelial sodium channels in rat alveolar type 2 epithelial cells. Am J Physiol Lung Cell Mol Physiol 304: L428-L437, 2013.
144. Taschereau R, Chow PL, Chatziioannou AF. Monte carlo simulations of dose from microCT imaging procedures in a realistic mouse phantom. Med Phys 33: 216-224, 2006.
145. Thind K, Chen A, Friesen-Waldner L, Ouriadov A, Scholl TJ, Fox M, Wong E, Vandyk J, Hope A, Santyr G. Detection of radiationinduced lung injury using hyperpolarized 13C magnetic resonance spectroscopy and imaging. Magn Reson Med 70: 601-609, 2013.
146. Thind K, Jensen MD, Hegarty E, Chen AP, Lim H, Martinez-Santiesteban F, Van Dyk J, Wong E, Scholl TJ, Santyr GE. Mapping metabolic changes associated with early Radiation Induced Lung Injury post conformal radiotherapy using hyperpolarized C-pyruvate Magnetic Resonance Spectroscopic Imaging. Radiother Oncol 110: 317-322, 2014.
147. Tigani B, Schaeublin E, Sugar R, Jackson AD, Fozard JR, Beckmann N. Pulmonary inflammation monitored noninvasively by MRI in freely breathing rats. Biochem Biophys Res Commun 292: 216-221, 2002.
148. Turi GJ, Ellis R, Wattie JN, Labiris NR, Inman MD. The effects of inhaled house dust mite on airway barrier function and sensitivity to inhaled methacholine in mice. Am J Physiol Lung Cell Mol Physiol 300: L185-L190, 2011.
149. van Rikxoort EM, de Hoop B, Viergever MA, Prokop M, van Ginneken B. Automatic lung segmentation from thoracic computed tomography scans using a hybrid approach with error detection. Med Phys 36: 2934-2947, 2009.
150. van Rikxoort EM, van Ginneken B. Automated segmentation of pulmonary structures in thoracic computed tomography scans: a review. Phys Med Biol 58: R187-R220, 2013.
151. Vasilescu DM, Gao Z, Saha PK, Yin L, Wang G, Haefeli-Bleuer B, Ochs M, Weibel ER, Hoffman EA. Assessment of morphometry of pulmonary acini in mouse lungs by nondestructive imaging using multiscale microcomputed tomography. Proc Natl Acad Sci USA 109: 17105-17110, 2012.
152. Venegas J, Winkler T, Harris RS. Lung physiology and aerosol deposition imaged with positron emission tomography. J Aerosol Med Pulm Drug Deliv 26: 1-8, 2013.
153. Virostko J, Chen Z, Fowler M, Poffenberger G, Powers AC, Jansen ED. Factors influencing quantification of in vivo bioluminescence imaging: application to assessment of pancreatic islet transplants. Mol Imaging 3: 333-342, 2004.
154. Wellman TJ, Winkler T, Costa EL, Musch G, Harris RS, Venegas JG, Melo MF. Measurement of regional specific lung volume change using respiratory-gated PET of inhaled 13N-nitrogen. J Nucl Med 51: 646-653, 2010.
155. Willekens I, Buls N, Lahoutte T, Baeyens L, Vanhove C, Caveliers V, Deklerck R, Bossuyt A, de Mey J. Evaluation of the radiation dose in micro-CT with optimization of the scan protocol. Contrast Media Mol Imaging 5: 201-207, 2010.
156. Williams AE, Chambers RC. The mercurial nature of neutrophils: still an enigma in ARDS? Am J Physiol Lung Cell Mol Physiol 306: L217-L230, 2014.
157. Xiang JJ, Tang JQ, Zhu SG, Nie XM, Lu HB, Shen SR, Li XL, Tang K, Zhou M, Li GY. IONP-PLL: a novel non-viral vector for efficient gene delivery. J Gene Med 5: 803-817, 2003.
158. Xu T, Ducote JL, Wong JT, Molloi S. Dynamic dual-energy chest radiography: a potential tool for lung tissue motion monitoring and kinetic study. Phys Med Biol 56: 1191-1205, 2011.
159. Yaghoubi S, Barrio JR, Dahlbom M, Iyer M, Namavari M, Satyamurthy N, Goldman R, Herschman HR, Phelps ME, Gambhir SS. Human pharmacokinetic and dosimetry studies of [18F]FHBG: a reporter probe for imaging herpes simplex virus type-1 thymidine kinase reporter gene expression. J Nucl Med 42: 1225-1234, 2001.
160. Yaghoubi SS, Gambhir SS. PET imaging of herpes simplex virus type 1 thymidine kinase (HSV1-tk) or mutant HSV1-sr39tk reporter gene expression in mice and humans using [18F]FHBG. Nat Protoc 1: 3069-3075, 2006.
161. Yao R, Lecomte R, Crawford ES. Small-animal PET: what is it, and why do we need it? J Nucl Med Technol 40: 157-165, 2012.
162. Ziady AG, Kotlarchyk M, Bryant L, McShane M, Lee Z. Bioluminescent imaging of reporter gene expression in the lungs of wildtype and model mice following the administration of PEG-stabilized DNA nanoparticles. Microsc Res Tech 73: 918-928, 2010.
163. Zurek M, Cremillieux Y. MRI of the lung: non-invasive protocols and applications to small animal models of lung disease. Methods Mol Biol 771: 459-474, 2011.