Tissue optical clearing, three-dimensional imaging, and computer morphometry in whole mouse lungs and human airways

American Journal of Respiratory Cell and Molecular Biology

Volumn 51, Issue 1, 2014, Pages 43-55

  Scott, Gregory D ^a   Blum, Emily D ^a   Fryer, Allison D ^a   Jacoby, David B ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Clearing; Modeling; Morphometry; Nerve; Visceral pleura

Indexed keywords

EPITOPE;

AIRWAY; ANIMAL TISSUE; ARTICLE; COMPUTER PROGRAM; GANGLION; HUMAN; HUMAN TISSUE; LUNG; LUNG INNERVATION; MORPHOMETRICS; MOUSE; NERVE; NONHUMAN; THREE DIMENSIONAL IMAGING; TISSUE AND ORGAN PREPARATION AND CULTURE; TISSUE OPTICAL CLEARING; TRACHEA;

CLEARING; MODELING; MORPHOMETRY; NERVE; VISCERAL PLEURA;

ADULT; ANIMALS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; IMAGING, THREE-DIMENSIONAL; LUNG; MICE; MICE, INBRED C57BL; NERVOUS SYSTEM; OPTICAL IMAGING; RESPIRATORY SYSTEM;

EID: 84903738575     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2013-0284OC     Document Type: Article

References (44)

1. Muhlfeld C, Graulich T, Das SK, Krasteva G, Wessels L, Ruppert C, Kummer W, Hofler G. Tracheal innervation and alveolar epithelial type II cell lamellar bodies are reduced in the cancer cachectic mouse. Am J Respir Crit Care Med 2012 [accessed 2013 Oct 1]. Available from: http://www.atsjournals.org/doi/abs/10. 1164/ajrccmconference.2012.185.1-MeetingAbstracts.A3552
2. O'Connell F, Springall DR, Moradoghli-Haftvani A, Krausz T, Price D, Fuller RW, Polak JM, Pride NB. Abnormal intraepithelial airway nerves in persistent unexplained cough? Am J Respir Crit Care Med 1995;152:2068-2075.
3. Scott GD, Fryer AD. Role of parasympathetic nerves and muscarinic receptors in allergy and asthma. Chem Immunol Allergy 2012;98:48-69.
4. Ollerenshaw SL, Jarvis D, Sullivan CE, Woolcock AJ. Substance P immunoreactive nerves in airways from asthmatics and nonasthmatics. Eur Respir J 1991;4:673-682.
5. Howarth PH, Springall DR, Redington AE, Djukanovic R, Holgate ST, Polak JM. Neuropeptide-containing nerves in endobronchial biopsies from asthmatic and nonasthmatic subjects. Am J Respir Cell Mol Biol 1995;13:288-296.
6. Goldie RG, Fernandes LB, Rigsby PJ, Pudney CJ, Spalding LJ, O 'Connor BJ, Page CP. Airway structure: a role for confocal microscopy? Pulm Pharmacol Ther 1998;11:349-354. (Pubitemid 29204272)
7. Dunnill MS. The pathology of asthma, with special reference to changes in the bronchial mucosa. J Clin Pathol 1960;13:27-33.
8. de Lange EE, Altes TA, Patrie JT, Parmar J, Brookeman JR, Mugler JP III, Platts-Mills TA. The variability of regional air flow obstruction within the lungs of patients with asthma: assessment with hyperpolarized helium-3 magnetic resonance imaging. J Allergy Clin Immunol 2007;119:1072-1078. (Pubitemid 46667159)
9. Turnbull DH, Mori S. MRI in mouse developmental biology. NMR Biomed 2007;20:265-274. (Pubitemid 46824529)
10. Thiesse J, Namati E, Sieren JC, Smith AR, Reinhardt JM, Hoffman EA, McLennan G. Lung structure phenotype variation in inbred mouse strains revealed through in vivo micro-CT imaging. J Appl Physiol (1985) 2010;109:1960-1968.
11. Cavanaugh D, Johnson E, Price RE, Kurie J, Travis EL, Cody DD. In vivo respiratory-gated micro-CT imaging in small-animal oncology models. Mol Imaging 2004;3:55-62.
12. Badea CT, Athreya KK, Espinosa G, Clark D, Ghafoori AP, Li Y, Kirsch DG, Johnson GA, Annapragada A, Ghaghada KB. Computed tomography imaging of primary lung cancer in mice using a liposomal-iodinated contrast agent. PLoS ONE 2012;7:e34496.
13. 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 2012;109:17105-17110.
14. Hyde DM, Harkema JR, Tyler NK, Plopper CG. Design-based sampling and quantitation of the respiratory airways. Toxicol Pathol 2006;34:286-295.
15. Scott GD, Fryer AD, Jacoby DB. Quantifying nerve architecture in murine and human airways using three-dimensional computational mapping. Am J Respir Cell Mol Biol 2013;48:10-16.
16. Mühlfeld C, Papadakis T, Krasteva G, Nyengaard JR, Hahn U, Kummer W. An unbiased stereological method for efficiently quantifying the innervation of the heart and other organs based on total length estimations. J Appl Physiol (1985) 2010;108:1402-1409.
17. Kuhn C. Biotin stores in rodent lungs: localization to Clara and type II alveolar cells. Exp Lung Res 1988;14:527-536.
18. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods 2012;9:676-682.
19. Madl P, Hofmann W, Oldham MJ, Asgharian B. Stochastic morphometric model of the BALB/c mouse lung. Anat Rec (Hoboken) 2010;293:1766-1775.
20. Larson SD, Schelegle ES, Hyde DM, Plopper CG. The three-dimensional distribution of nerves along the entire intrapulmonary airway tree of the adult rat and the anatomical relationship between nerves and neuroepithelial bodies. Am J Respir Cell Mol Biol 2003;28:592-599. (Pubitemid 36543406)
21. Barnes PJ, Chung KF, Page CP. In flammatory mediators of asthma: an update. Pharmacol Rev 1998;50:515-596.
22. Baker DG, McDonald DM, Basbaum CB, Mitchell RA. The architecture of nerves and ganglia of the ferret trachea as revealed by acetylcholinesterase histochemistry. J Comp Neurol 1986;246:513-526. (Pubitemid 16079513)
23. Larsell O. The ganglia, plexuses, and nerve-terminations of the mammalian lung and pleura pulmonalis. J Comp Neurol 1922;35:97-132.
24. Pintelon I, Brouns I, De Proost I, Van Meir F, Timmermans JP, Adriaensen D. Sensory receptors in the visceral pleura: neurochemical coding and live staining in whole mounts. Am J Respir Cell Mol Biol 2007;36:541-551. (Pubitemid 46676713)
25. Blake K, Teague WG. Gastroesophageal reflux disease and childhood asthma. Curr Opin Pulm Med 2013;19:24-29.
26. Carr S, Watson W. Eosinophilic esophagitis. Allergy Asthma Clin Immunol 2011;7(Suppl):S8.
27. Harer KN, Enders FT, Lim KG, Alexander JA, Katzka DA. An allergic phenotype and the use of steroid inhalers predict eosinophilic oesophagitis in patients with asthma. Aliment Pharmacol Ther 2013;37:107-113.
28. Canning BJ. Reflex regulation of airway smooth muscle tone. J Appl Physiol (1985) 2006;101:971-985.
29. Joos GF, Germonpré PR, Pauwels RA. Neural mechanisms in asthma. Clin Exp Allergy 2000;30:60-65. (Pubitemid 30341381)
30. Wu M, Majewski M, Wojtkiewicz J, Vanderwinden JM, Adriaensen D, Timmermans JP. Anatomical and neurochemical features of the extrinsic and intrinsic innervation of the striated muscle in the porcine esophagus: evidence for regional and species differences. Cell Tissue Res 2003;311:289-297. (Pubitemid 36459668)
31. McLaughlin AI. Nerves and nerve endings in the visceral pleura of the cat. J Physiol 1933;80:101-104.
32. Chung K, Wallace J, Kim SY, Kalyanasundaram S, Andalman AS, Davidson TJ, Mirzabekov JJ, Zalocusky KA, Mattis J, Denisin AK, et al. Structural and molecular interrogation of intact biological systems. Nature 2013;497:332-337.
33. Yokomizo T, Ng CE, Osato M, Dzierzak E. Three-dimensional imaging of whole midgestation murine embryos shows an intravascular localization for all hematopoietic clusters. Blood 2011;117:6132-6134.
34. Oldham MJ, Robinson RJ. Predicted tracheobronchial and pulmonary deposition in a murine asthma model. Anat Rec (Hoboken) 2007;290:1309-1314. (Pubitemid 47573202)
35. Chaturvedi A, Lee Z. Three-dimensional segmentation and skeletonization to build an airway tree data structure for small animals. Phys Med Biol 2005;50:1405-1419. (Pubitemid 40524533)
36. Komatsu T, Yamamoto M, Shimokata K, Nagura H. Distribution of substance P-immunoreactive and calcitonin gene-related peptide-immunoreactive nerves in normal human lungs. Int Arch Allergy Appl Immunol 1991;95:23-28.
37. Laitinen LA, Laitinen A, Panula PA, Partanen M, Tervo K, Tervo T. Immunohistochemical demonstration of substance P in the lower respiratory tract of the rabbit and not of man. Thorax 1983;38:531-536. (Pubitemid 13030338)
38. Dey RD, Altemus JB, Rodd A, Mayer B, Said SI, Coburn RF. Neurochemical characterization of intrinsic neurons in ferret tracheal plexus. Am J Respir Cell Mol Biol 1996;14:207-216. (Pubitemid 126439813)
39. Wu ZX, Barker JS, Batchelor TP, Dey RD. Interleukin (IL)-1 regulates ozone-enhanced tracheal smooth muscle responsiveness by increasing substance P (SP) production in intrinsic airway neurons of ferret. Respir Physiol Neurobiol 2008;164:300-311.
40. Iwadare T, Mori H, Ishiguro K, Takeishi M. Dimensional changes of tissues in the course of processing. J Microsc 1984;136:323-327. (Pubitemid 15175730)
41. Dorph-Petersen KA, Nyengaard JR, Gundersen HJ. Tissue shrinkage and unbiased stereological estimation of particle number and size. J Microsc 2001;204:232-246. (Pubitemid 34075121)
42. Hama H, Kurokawa H, Kawano H, Ando R, Shimogori T, Noda H, Fukami K, Sakaue-Sawano A, Miyawaki A. Scale: a chemical approach for fluorescence imaging and reconstruction of transparent mouse brain. Nat Neurosci 2011;14:1481-1488.
43. Pritchard S, Wick HC, Slonim DK, Johnson KL, Bianchi DW. Comprehensive analysis of genes expressed by rare microchimeric fetal cells in the maternal mouse lung. Biol Reprod 2012;87:42.
44. Provenzano PP, Eliceiri KW, Keely PJ. Multiphoton microscopy and fluorescence lifetime imaging microscopy (FLIM) to monitor metastasis and the tumor microenvironment. Clin Exp Metastasis 2009;26:357-370.