Enhancement of lung tumorigenesis in a Gprc5a Knockout mouse by chronic extrinsic airway inflammation

Molecular Cancer

Volumn 11, Issue , 2012, Pages

  Barta, Peter ^a   Van Pelt, Carolyn ^a   Men, Taoyan ^a   Dickey, Burton F ^a   Lotan, Reuben ^a   Moghaddam, Seyed Javad ^a  

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

Author keywords

COPD; Gpcr5a; Inflammation; Lung cancer; NTHi

Indexed keywords

CARCINOGEN; G PROTEIN COUPLED RECEPTOR KINASE 5; HYPOXIA INDUCIBLE FACTOR 1ALPHA; RETINOIC ACID INDUCIBLE PROTEIN I; 4 (METHYLNITROSAMINO) 1 (3 PYRIDYL) 1 BUTANONE; 4-(N-METHYL-N-NITROSAMINO)-1-(3-PYRIDYL)-1-BUTANONE; G PROTEIN COUPLED RECEPTOR; GPRC5A PROTEIN, MOUSE; NITROSAMINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARCINOGENESIS; CHRONIC INFLAMMATION; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; HAEMOPHILUS INFLUENZAE; INFLAMMATORY CELL; LUNG CANCER; MOUSE; NONHUMAN; TOBACCO; TUMOR PROMOTION; 129 MOUSE; ANIMAL; C57BL MOUSE; CELL TRANSFORMATION; CHEMICALLY INDUCED DISORDER; CHRONIC OBSTRUCTIVE LUNG DISEASE; DISEASE MODEL; GENETICS; HAEMOPHILUS INFECTION; LUNG; LUNG TUMOR; METABOLISM; MICROBIOLOGY; MOUSE MUTANT; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY;

BACTERIA (MICROORGANISMS); HAEMOPHILUS INFLUENZAE; MUS; NICOTIANA TABACUM;

ANIMALS; CELL TRANSFORMATION, NEOPLASTIC; DISEASE MODELS, ANIMAL; HAEMOPHILUS INFECTIONS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; LUNG; LUNG NEOPLASMS; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; NEOVASCULARIZATION, PATHOLOGIC; NITROSAMINES; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; RECEPTORS, G-PROTEIN-COUPLED;

EID: 84855577723     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-11-4     Document Type: Article

References (55)

1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ. Cancer statistics. CA Cancer J Clin 2009, 59:225-249. 10.3322/caac.20006, 19474385.
2. Stellman SD, Takezaki T, Wang L, Chen Y, Citron ML, Djordjevic MV, Harlap S, Muscat JE, Neugut AI, Wynder EL, et al. Smoking and lung cancer risk in American and Japanese men: an international case-control study. Cancer Epidemiol Biomarkers Prev 2001, 10:1193-1199.
3. Schottenfield D. Etiology and epidemiology of lung cancer. Lung cancer: Principles and Practice 2000, 367-388. Philadelphia: Lippincott, Williams and Wilkins, Pass HIMJBJDHTATMJD.
4. Mannino DM, Aguayo SM, Petty TL, Redd SC. Low lung function and incident lung cancer in the United States: data From the First National Health and Nutrition Examination Survey follow-up. Arch Intern Med 2003, 163:1475-1480. 10.1001/archinte.163.12.1475, 12824098.
5. Turner MC, Chen Y, Krewski D, Calle EE, Thun MJ. Chronic obstructive pulmonary disease is associated with lung cancer mortality in a prospective study of never smokers. Am J Respir Crit Care Med 2007, 176:285-290. 10.1164/rccm.200612-1792OC, 17478615.
6. Halbert RJ, Natoli JL, Gano A, Badamgarav E, Buist AS, Mannino DM. Global burden of COPD: systematic review and meta-analysis. Eur Respir J 2006, 28:523-532. 10.1183/09031936.06.00124605, 16611654.
7. Jeffery PK. Comparison of the structural and inflammatory features of COPD and asthma. Giles F. Filley Lecture. Chest 2000, 117:251S-260S. 10.1378/chest.117.5_suppl_1.251S, 10843939.
8. Shapiro SD. End-stage chronic obstructive pulmonary disease: the cigarette is burned out but inflammation rages on. Am J Respir Crit Care Med 2001, 164:339-340.
9. Moghaddam SJ, Clement CG, De la Garza MM, Zou X, Travis EL, Young HW, Evans CM, Tuvim MJ, Dickey BF. Haemophilus influenzae lysate induces aspects of the chronic obstructive pulmonary disease phenotype. Am J Respir Cell Mol Biol 2008, 38:629-638. 10.1165/rcmb.2007-0366OC, 2396243, 18096867.
10. King PT, Hutchinson PE, Johnson PD, Holmes PW, Freezer NJ, Holdsworth SR. Adaptive immunity to nontypeable Haemophilus influenzae. Am J Respir Crit Care Med 2003, 167:587-592. 10.1164/rccm.200207-728OC, 12433671.
11. Murphy TF. Haemophilus influenzae in chronic bronchitis. Semin Respir Infect 2000, 15:41-51. 10.1053/srin.2000.0150041, 10749549.
12. Sethi S, Murphy TF. Bacterial infection in chronic obstructive pulmonary disease in 2000: a state-of-the-art review. Clin Microbiol Rev 2001, 14:336-363. 10.1128/CMR.14.2.336-363.2001, 88978, 11292642.
13. Moghaddam SJ, Li H, Cho SN, Dishop MK, Wistuba II, Ji L, Kurie JM, Dickey BF, DeMayo FJ. Promotion of lung carcinogenesis by chronic obstructive pulmonary disease-like airway inflammation in a K-ras-induced mouse model. Am J Respir Cell Mol Biol 2009, 40:443-453. 2660561, 18927348.
14. Ochoa CE, Mirabolfathinejad SG, Ruiz VA, Evans SE, Gagea M, Evans CM, Dickey BF, Moghaddam SJ. Interleukin 6, but not T helper 2 cytokines, promotes lung carcinogenesis. Cancer Prev Res (Phila) 2011, 4:51-64.
15. Doris K, Karabela SP, Kairi CA, Simoes DC, Roussos C, Zakynthinos SG, Kalomenidis I, Blackwell TS, Stathopoulos GT. Allergic inflammation does not impact chemical-induced carcinogenesis in the lungs of mice. Respir Res 2010, 11:118. 10.1186/1465-9921-11-118, 2936383, 20796309.
16. Tao Q, Fujimoto J, Men T, Ye X, Deng J, Lacroix L, Clifford JL, Mao L, Van Pelt CS, Lee JJ, et al. Identification of the retinoic acid-inducible Gprc5a as a new lung tumor suppressor gene. J Natl Cancer Inst 2007, 99:1668-1682. 10.1093/jnci/djm208, 18000218.
17. Ribatti D, Crivellato E. Immune cells and angiogenesis. J Cell Mol Med 2009, 13:2822-2833. 10.1111/j.1582-4934.2009.00810.x, 19538473.
18. Semenza GL. Targeting HIF-1 for cancer therapy. Nat Rev Cancer 2003, 3:721-732. 10.1038/nrc1187, 13130303.
19. Imtiyaz HZ, Simon MC. Hypoxia-Inducible Factors as Essential Regulators of Inflammation. Curr Top Microbiol Immunol 2010,
20. Barnes PJ. New concepts in chronic obstructive pulmonary disease. Annu Rev Med 2003, 54:113-129. 10.1146/annurev.med.54.101601.152209, 12359824.
21. Dhala A, Pinsker K, Prezant DJ. Respiratory health consequences of environmental tobacco smoke. Med Clin North Am 2004, 88:1535-52. xi, 10.1016/j.mcna.2004.06.005, 15464112.
22. Philip M, Rowley DA, Schreiber H. Inflammation as a tumor promoter in cancer induction. Semin Cancer Biol 2004, 14:433-439. 10.1016/j.semcancer.2004.06.006, 15489136.
23. Borm PJ, Driscoll K. Particles, inflammation and respiratory tract carcinogenesis. Toxicol Lett 1996, 88:109-113.
24. Coussens LM, Werb Z. Inflammation and cancer. Nature 2002, 420:860-867. 10.1038/nature01322, 2803035, 12490959.
25. Lin EY, Pollard JW. Role of infiltrated leucocytes in tumour growth and spread. Br J Cancer 2004, 90:2053-2058. 10.1038/sj.bjc.6601705, 2410285, 15164120.
26. Balkwill F, Charles KA, Mantovani A. Smoldering and polarized inflammation in the initiation and promotion of malignant disease. Cancer Cell 2005, 7:211-217. 10.1016/j.ccr.2005.02.013, 15766659.
27. Deng J, Fujimoto J, Ye XF, Men TY, Van Pelt CS, Chen YL, Lin XF, Kadara H, Tao Q, Lotan D, et al. Knockout of the tumor suppressor gene Gprc5a in mice leads to NF-kappaB activation in airway epithelium and promotes lung inflammation and tumorigenesis. Cancer Prev Res (Phila) 2010, 3:424-437.
28. Fujimoto J, Kadara H, Men T, van Pelt C, Lotan D, Lotan R. Comparative functional genomics analysis of NNK tobacco-carcinogen induced lung adenocarcinoma development in Gprc5a-knockout mice. PLoS ONE 2010, 5:e11847. 10.1371/journal.pone.0011847, 2912294, 20686609.
29. Schuller HM. Mechanisms of smoking-related lung and pancreatic adenocarcinoma development. Nat Rev Cancer 2002, 2:455-463. 10.1038/nrc824, 12189387.
30. Rodenhuis S, Slebos RJ. The ras oncogenes in human lung cancer. Am Rev Respir Dis 1990, 142:S27-S30.
31. Bauer AK, Malkinson AM, Kleeberger SR. Susceptibility to neoplastic and non-neoplastic pulmonary diseases in mice: genetic similarities. Am J Physiol Lung Cell Mol Physiol 2004, 287:L685-L703. 10.1152/ajplung.00223.2003, 15355860.
32. Rehm S, Devor DE, Henneman JR, Ward JM. Origin of spontaneous and transplacentally induced mouse lung tumors from alveolar type II cells. Exp Lung Res 1991, 17:181-195. 10.3109/01902149109064410, 2050024.
33. Takahashi H, Ogata H, Nishigaki R, Broide DH, Karin M. Tobacco smoke promotes lung tumorigenesis by triggering IKKbeta- and JNK1-dependent inflammation. Cancer Cell 2010, 17:89-97. 10.1016/j.ccr.2009.12.008, 2818776, 20129250.
34. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell 2000, 100:57-70. 10.1016/S0092-8674(00)81683-9, 10647931.
35. Rius J, Guma M, Schachtrup C, Akassoglou K, Zinkernagel AS, Nizet V, Johnson RS, Haddad GG, Karin M. NF-kappaB links innate immunity to the hypoxic response through transcriptional regulation of HIF-1alpha. Nature 2008, 453:807-811. 10.1038/nature06905, 2669289, 18432192.
36. van Uden P, Kenneth NS, Rocha S. Regulation of hypoxia-inducible factor-1alpha by NF-kappaB. Biochem J 2008, 412:477-484. 10.1042/BJ20080476, 2474706, 18393939.
37. Shin DH, Li SH, Yang SW, Lee BL, Lee MK, Park JW. Inhibitor of nuclear factor-kappaB alpha derepresses hypoxia-inducible factor-1 during moderate hypoxia by sequestering factor inhibiting hypoxia-inducible factor from hypoxia-inducible factor 1alpha. FEBS J 2009, 276:3470-3480. 10.1111/j.1742-4658.2009.07069.x, 19456861.
38. Di Stefano A, Caramori G, Oates T, Capelli A, Lusuardi M, Gnemmi I, Ioli F, Chung KF, Donner CF, Barnes PJ, et al. Increased expression of nuclear factor-kappaB in bronchial biopsies from smokers and patients with COPD. Eur Respir J 2002, 20:556-563. 10.1183/09031936.02.00272002, 12358328.
39. Schabath MB, Delclos GL, Martynowicz MM, Greisinger AJ, Lu C, Wu X, Spitz MR. Opposing effects of emphysema, hay fever, and select genetic variants on lung cancer risk. Am J Epidemiol 2005, 161:412-422. 10.1093/aje/kwi063, 15718477.
40. Tang X, Liu D, Shishodia S, Ozburn N, Behrens C, Lee JJ, Hong WK, Aggarwal BB, Wistuba II. Nuclear factor-kappaB (NF-kappaB) is frequently expressed in lung cancer and preneoplastic lesions. Cancer 2006, 107:2637-2646. 10.1002/cncr.22315, 17078054.
41. Luo JL, Maeda S, Hsu LC, Yagita H, Karin M. Inhibition of NF-kappaB in cancer cells converts inflammation- induced tumor growth mediated by TNFalpha to TRAIL-mediated tumor regression. Cancer Cell 2004, 6:297-305. 10.1016/j.ccr.2004.08.012, 15380520.
42. Pikarsky E, Porat RM, Stein I, Abramovitch R, Amit S, Kasem S, Gutkovich-Pyest E, Urieli-Shoval S, Galun E, Ben Neriah Y. NF-kappaB functions as a tumour promoter in inflammation-associated cancer. Nature 2004, 431:461-466. 10.1038/nature02924, 15329734.
43. Greten FR, Eckmann L, Greten TF, Park JM, Li ZW, Egan LJ, Kagnoff MF, Karin M. IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer. Cell 2004, 118:285-296. 10.1016/j.cell.2004.07.013, 15294155.
44. Stathopoulos GT, Sherrill TP, Cheng DS, Scoggins RM, Han W, Polosukhin VV, Connelly L, Yull FE, Fingleton B, Blackwell TS. Epithelial NF-kappaB activation promotes urethane-induced lung carcinogenesis. Proc Natl Acad Sci USA 2007, 104:18514-18519. 10.1073/pnas.0705316104, 2141808, 18000061.
45. Meylan E, Dooley AL, Feldser DM, Shen L, Turk E, Ouyang C, Jacks T. Requirement for NF-kappaB signalling in a mouse model of lung adenocarcinoma. Nature 2009, 462:104-107. 10.1038/nature08462, 2780341, 19847165.
46. Moghaddam SJ, Barta P, Mirabolfathinejad SG, Ammar-Aouchiche Z, Garza NT, Vo TT, Newman RA, Aggarwal BB, Evans CM, Tuvim MJ, et al. Curcumin inhibits COPD-like airway inflammation and lung cancer progression in mice. Carcinogenesis 2009, 30:1949-1956. 10.1093/carcin/bgp229, 2783007, 19793800.
47. Chen Y, Thai P, Zhao YH, Ho YS, DeSouza MM, Wu R. Stimulation of airway mucin gene expression by interleukin (IL)-17 through IL-6 paracrine/autocrine loop. J Biol Chem 2003, 278:17036-17043. 10.1074/jbc.M210429200, 12624114.
48. Molet S, Hamid Q, Davoine F, Nutku E, Taha R, Page N, Olivenstein R, Elias J, Chakir J. IL-17 is increased in asthmatic airways and induces human bronchial fibroblasts to produce cytokines. J Allergy Clin Immunol 2001, 108:430-438. 10.1067/mai.2001.117929, 11544464.
49. Ye P, Rodriguez FH, Kanaly S, Stocking KL, Schurr J, Schwarzenberger P, Oliver P, Huang W, Zhang P, Zhang J, et al. Requirement of interleukin 17 receptor signaling for lung CXC chemokine and granulocyte colony-stimulating factor expression, neutrophil recruitment, and host defense. J Exp Med 2001, 194:519-527. 10.1084/jem.194.4.519, 2193502, 11514607.
50. Curtis JL, Freeman CM, Hogg JC. The immunopathogenesis of chronic obstructive pulmonary disease: insights from recent research. Proc Am Thorac Soc 2007, 4:512-521. 10.1513/pats.200701-002FM, 2365762,2365762, 17878463.
51. Di Stefano A, Caramori G, Gnemmi I, Contoli M, Vicari C, Capelli A, Magno F, D'Anna SE, Zanini A, Brun P, et al. T helper type 17-related cytokine expression is increased in the bronchial mucosa of stable chronic obstructive pulmonary disease patients. Clin Exp Immunol 2009, 157:316-324. 10.1111/j.1365-2249.2009.03965.x, 2730858, 19604272.
52. Bellocq A, Antoine M, Flahault A, Philippe C, Crestani B, Bernaudin JF, Mayaud C, Milleron B, Baud L, Cadranel J. Neutrophil alveolitis in bronchioloalveolar carcinoma: induction by tumor-derived interleukin-8 and relation to clinical outcome. Am J Pathol 1998, 152:83-92. 1858104, 9422526.
53. Redente EF, Orlicky DJ, Bouchard RJ, Malkinson AM. Tumor signaling to the bone marrow changes the phenotype of monocytes and pulmonary macrophages during urethane-induced primary lung tumorigenesis in A/J mice. Am J Pathol 2007, 170:693-708. 10.2353/ajpath.2007.060566, 1851863, 17255336.
54. Houghton AM, Rzymkiewicz DM, Ji H, Gregory AD, Egea EE, Metz HE, Stolz DB, Land SR, Marconcini LA, Kliment CR, et al. Neutrophil elastase-mediated degradation of IRS-1 accelerates lung tumor growth. Nat Med 2010, 16:219-223. 10.1038/nm.2084, 2821801, 20081861.
55. Nikitin AY, Alcaraz A, Anver MR, Bronson RT, Cardiff RD, Dixon D, Fraire AE, Gabrielson EW, Gunning WT, Haines DC, et al. Classification of proliferative pulmonary lesions of the mouse: recommendations of the mouse models of human cancers consortium. Cancer Res 2004, 64:2307-2316. 10.1158/0008-5472.CAN-03-3376, 15059877.