Tracheal dysplasia precedes bronchial dysplasia in mouse model of N-nitroso trischloroethylurea induced squamous cell lung cancer

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Ghosh, Moumita ^a   Dwyer Nield, Lori D ^b   Kwon, Jennifer B ^a   Barthel, Lea ^a   Janssen, William J ^a   Merrick, Daniel T ^d   Keith, Robert L ^c  

^a DEPARTMENT OF MEDICINE   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

^d UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLATED TUBULIN; CLUB CELL SECRETORY PROTEIN; CYTOKERATIN 14; CYTOKERATIN 5; INVOLUCRIN; N NITROSO TRIS CHLOROETHYLUREA; NITROSOUREA DERIVATIVE; PROTEIN P63; SECRETORY PROTEIN; TUBULIN; UNCLASSIFIED DRUG; CARMUSTINE; N-NITROSO-TRIS-CHLOROETHYLUREA; TUMOR MARKER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASAL CELL; BRONCHIAL DYSPLASIA; BRONCHUS MUCOSA; CELL PROLIFERATION; CILIATED EPITHELIUM CELL; CONTROLLED STUDY; DYSPLASIA; EPITHELIUM CELL; FEMALE; HISTOPATHOLOGY; LUNG DYSPLASIA; METAPLASIA; MITOSIS INDEX; MOUSE; NONHUMAN; SQUAMOUS CELL LUNG CARCINOMA; TRACHEA MUCOSA; TRACHEAL DYSPLASIA; ANALOGS AND DERIVATIVES; ANIMAL; BRONCHUS; CANCER GRADING; CELL TRANSFORMATION; CHEMICALLY INDUCED; DISEASE MODEL; LUNG TUMOR; METABOLISM; PATHOLOGY; RESPIRATORY TRACT MUCOSA; SQUAMOUS CELL CARCINOMA; TRACHEA;

MUS;

ANIMALS; BIOMARKERS, TUMOR; BRONCHI; CARCINOMA, SQUAMOUS CELL; CARMUSTINE; CELL TRANSFORMATION, NEOPLASTIC; DISEASE MODELS, ANIMAL; FEMALE; LUNG NEOPLASMS; MICE; MITOTIC INDEX; NEOPLASM GRADING; RESPIRATORY MUCOSA; TRACHEA;

EID: 84929452726     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0122823     Document Type: Article

References (40)

1. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J Clin. 2013; 63(1):11-30. doi: 10.3322/caac.21166 PMID: 23335087
2. Banerjee AK. Preinvasive lesions of the bronchus. J Thorac Oncol. 2009; 4(4):545-51. doi: 10.1097/ JTO.0b013e31819667bd PMID: 19279508
3. Nicholson AG, Perry LJ, Cury PM, Jackson P, McCormick CM, Corrin B, et al. Reproducibility of the WHO/IASLC grading system for pre-invasive squamous lesions of the bronchus: a study of inter-observer and intra-observer variation. Histopathology. 2001; 38(3):202-8. PMID: 11260299
4. Kelly K, Kittelson J, Franklin WA, Kennedy TC, Klein CE, Keith RL, et al. A randomized phase II chemoprevention trial of 13-CIS retinoic acid with or without alpha tocopherol or observation in subjects at high risk for lung cancer. Cancer Prev Res (Phila). 2009; 2(5):440-9. doi: 10.1158/1940-6207.CAPR-08-0136 PMID: 19401528
5. Lam S, McWilliams A, LeRiche J, MacAulay C, Wattenberg L, Szabo E. A phase I study of myo-inositol for lung cancer chemoprevention. Cancer Epidemiol Biomarkers Prev. 2006; 15(8):1526-31. PMID: 16896044
6. Hudish TM, Opincariu LI, Mozer AB, Johnson MS, Cleaver TG, Malkoski SP, et al. N-nitroso-tris-chloroethylurea induces premalignant squamous dysplasia in mice. Cancer Prev Res (Phila). 2011; 5(2):283-9.
7. Evans MJ, Fanucchi MV, Baker GL, Van Winkle LS, Pantle LM, Nishio SJ, et al. The remodelled tracheal basement membrane zone of infant rhesus monkeys after 6 months of recovery. Clin Exp Allergy. 2004; 34(7):1131-6. PMID: 15248862
8. Rehm S, Lijinsky W, Singh G, Katyal SL. Mouse bronchiolar cell carcinogenesis. Histologic characterization and expression of Clara cell antigen in lesions induced by N-nitrosobis-(2-chloroethyl) ureas. Am J Pathol. 1991; 139(2):413-22. PMID: 1651059
9. Wang Y, Zhang Z, Yan Y, Lemon WJ, LaRegina M, Morrison C, et al. A chemically induced model for squamous cell carcinoma of the lung in mice: histopathology and strain susceptibility. Cancer Res. 2004; 64(5):1647-54. PMID: 14996723
10. Ji H, Ramsey MR, Hayes DN, Fan C, McNamara K, Kozlowski P, et al. LKB1 modulates lung cancer differentiation and metastasis. Nature. 2007; 448(7155):807-10. PMID: 17676035
11. Xiao Z, Jiang Q, Willette-Brown J, Xi S, Zhu F, Burkett S, et al. The pivotal role of IKKalpha in the development of spontaneous lung squamous cell carcinomas. Cancer Cell. 2013; 23(4):527-40. doi: 10.1016/j.ccr.2013.03.009 PMID: 23597566
12. Rackley CR, Stripp BR. Building and maintaining the epithelium of the lung. J Clin Invest. 2012; 122(8):2724-30. doi: 10.1172/JCI60519 PMID: 22850882
13. Rock JR, Randell SH, Hogan BL. Airway basal stem cells: a perspective on their roles in epithelial homeostasis and remodeling. Dis Model Mech. 2010; 3(9-10):545-56. doi: 10.1242/dmm.004598 PMID: 20442204
14. Rock JR, Hogan BL. Epithelial Progenitor Cells in Lung Development, Maintenance, Repair, and Disease. Annu Rev Cell Dev Biol. 2011; 27:493-512. doi: 10.1146/annurev-cellbio-100109-104040 PMID: 21639799
15. Cole BB, Smith RW, Jenkins KM, Graham BB, Reynolds PR, Reynolds SD. Tracheal Basal Cells. A Facultative Progenitor Cell Pool. Am J Pathol. 2010; 177(4):2145.
16. Van Winkle LS, Fanucchi MV, Miller LA, Baker GL, Gershwin LJ, Schelegle ES, et al. Epithelial cell distribution and abundance in rhesus monkey airways during postnatal lung growth and development. J Appl Physiol. 2004; 97(6):2355-63; discussion 4. PMID: 15298983
17. Hsia CC, Hyde DM, Ochs M, Weibel ER. An official research policy statement of the American Thoracic Society/European Respiratory Society: standards for quantitative assessment of lung structure. Am J Respir Crit Care Med. 2010; 181(4):394-418. doi: 10.1164/rccm.200809-1522ST PMID: 20130146
18. Rock JR, Onaitis MW, Rawlins EL, Lu Y, Clark CP, Xue Y, et al. Basal cells as stem cells of the mouse trachea and human airway epithelium. Proc Natl Acad Sci U S A. 2009; 106(31):12771-5. doi: 10.1073/pnas.0906850106 PMID: 19625615
19. Jetten AM. Multistep process of squamous differentiation in tracheobronchial epithelial cells in vitro: analogy with epidermal differentiation. Environ Health Perspect. 1989; 80:149-60. PMID: 2647475
20. Ishida-Yamamoto A, Iizuka H. Structural organization of cornified cell envelopes and alterations in inherited skin disorders. Exp Dermatol. 1998; 7(1):1-10. PMID: 9517915
21. Brechbuhl HM, Ghosh M, Smith MK, Smith RW, Li B, Hicks DA, et al. beta-catenin dosage is a critical determinant of tracheal basal cell fate determination. Am J Pathol. 2011; 179(1):367-79. doi: 10.1016/j.ajpath.2011.03.016 PMID: 21703416
22. Ghosh M, Brechbuhl HM, Smith RW, Li B, Hicks DA, Titchner T, et al. Context-dependent differentiation of multipotential keratin 14-expressing tracheal Basal cells. Am J Respir Cell Mol Biol. 2011; 45(2):403-10. doi: 10.1165/rcmb.2010-0283OC PMID: 21131447
23. Merrick DT, Kittelson J, Winterhalder R, Kotantoulas G, Ingeberg S, Keith RL, et al. Analysis of c-ErbB1/epidermal growth factor receptor and c-ErbB2/HER-2 expression in bronchial dysplasia: evaluation of potential targets for chemoprevention of lung cancer. Clin Cancer Res. 2006; 12(7 Pt 1):2281-8. PMID: 16609045
24. Miller YE, Blatchford P, Hyun DS, Keith RL, Kennedy TC, Wolf H, et al. Bronchial epithelial ki-67 index is related to histology, smoking, and gender, but not lung cancer or chronic obstructive pulmonary disease. Cancer Epidemiol Biomarkers Prev. 2007; 16(11):2425-31. PMID: 18006932
25. Rawlins EL, Hogan BL. Ciliated epithelial cell lifespan in the mouse trachea and lung. Am J Physiol Lung Cell Mol Physiol. 2008; 295(1):L231-4. doi: 10.1152/ajplung.90209.2008 PMID: 18487354
26. Rawlins EL, Hogan BL. Epithelial stem cells of the lung: privileged few or opportunities for many? Development. 2006; 133(13):2455-65. PMID: 16735479
27. Rawlins EL, Ostrowski LE, Randell SH, Hogan BL. Lung development and repair: Contribution of the ciliated lineage. Proc Natl Acad Sci U S A. 2006; 104(2):410-7. PMID: 17194755
28. Hong KU, Reynolds SD, Watkins S, Fuchs E, Stripp BR. Basal cells are a multipotent progenitor capable of renewing the bronchial epithelium. Am J Pathol. 2004; 164(2):577-88. PMID: 14742263
29. Rawlins EL, Okubo T, Xue Y, Brass DM, Auten RL, Hasegawa H, et al. The role of Scgb1a1+ Clara cells in the long-term maintenance and repair of lung airway, but not alveolar, epithelium. Cell Stem Cell. 2009; 4(6):525-34. doi: 10.1016/j.stem.2009.04.002 PMID: 19497281
30. Reynolds SD, Malkinson AM. Clara cell: Progenitor for the bronchiolar epithelium. Int J Biochem Cell Biol. 2010; 42(1):1-4. doi: 10.1016/j.biocel.2009.09.002 PMID: 19747565
31. Kumar PA, Hu Y, Yamamoto Y, Hoe NB, Wei TS, Mu D, et al. Distal airway stem cells yield alveoli in vitro and during lung regeneration following H1N1 influenza infection. Cell. 2011; 147(3):525-38. doi: 10.1016/j.cell.2011.10.001 PMID: 22036562
32. Ooi AT, Mah V, Nickerson DW, Gilbert JL, Ha VL, Hegab AE, et al. Presence of a putative tumor-initiating progenitor cell population predicts poor prognosis in smokers with non-small cell lung cancer. Cancer Res. 2010; 70(16):6639-48. doi: 10.1158/0008-5472.CAN-10-0455 PMID: 20710044
33. Dakir EL, Feigenbaum L, Linnoila RI. Constitutive expression of human keratin 14 gene in mouse lung induces premalignant lesions and squamous differentiation. Carcinogenesis. 2008; 29(12):2377-84. doi: 10.1093/carcin/bgn190 PMID: 18701433
34. Alam H, Sehgal L, Kundu ST, Dalal SN, Vaidya MM. Novel function of keratins 5 and 14 in proliferation and differentiation of stratified epithelial cells. Mol Biol Cell. 2011; 22(21):4068-78. doi: 10.1091/mbc.E10-08-0703 PMID: 21900500
35. Zuo W, Zhang T, Wu DZ, Guan SP, Liew A, Yamamoto Y, et al. p63Krt5 distal airway stem cells are essential for lung regeneration. Nature. 2015; 517(7536):616-20. doi: 10.1038/nature13903 PMID: 25383540
36. Ghosh M, Ahmad S, Jian A, Li B, Smith RW, Helm KM, et al. Human tracheobronchial basal cells. Normal versus remodeling/repairing phenotypes in vivo and in vitro. Am J Respir Cell Mol Biol. 2013; 49(6):1127-34. doi: 10.1165/rcmb.2013-0049OC PMID: 23927678
37. Ghosh M, Smith RW, Runkle CM, Hicks DA, Helm KM, Reynolds SD. Regulation of trachebronchial tissue-specific stem cell pool size. Stem Cells. 2013; 31(12):2767-78. doi: 10.1002/stem.1440 PMID: 23712882
38. Khojasteh M, Buys TP, LeRiche J, Lam S, Guillaud M, MacAulay C. A framework for quantitative assessment of Ki67 distribution in preneoplastic bronchial epithelial lesions. Anal Quant Cytol Histol. 2012; 34(3):120-38. PMID: 23016458
39. Hong KU, Reynolds SD, Watkins S, Fuchs E, Stripp BR. In vivo differentiation potential of tracheal basal cells: Evidence for multipotent and unipotent subpopulations. Am J Physiol Lung Cell Mol Physiol. 2003; 286(4):L643-9. PMID: 12871857
40. Ghosh M, Helm KM, Smith RW, Giordanengo MS, Li B, Shen H, et al. A single cell functions as a tissue-specific stem cell and the in vitro niche-forming cell. Am J Respir Cell Mol Biol. 2011; 45(3):459-69. doi: 10.1165/rcmb.2010-0314OC PMID: 21131442