Identification of the retinoic acid-inducible Gprc5a as a new lung tumor suppressor gene

Journal of the National Cancer Institute

Volumn 99, Issue 22, 2007, Pages 1668-1682

  Tao, Qingguo ^a   Fujimoto, Junya ^a   Men, Taoyan ^a   Ye, Xiaofeng ^a   Deng, Jiong ^a   Lacroix, Ludovic ^a   Clifford, John L ^a   Mao, Li ^a   Van Pelt, Carolyn S ^a   Lee, J Jack ^a   Lotan, Dafna ^a   Lotan, Reuben ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

G PROTEIN COUPLED RECEPTOR C 5A; K RAS PROTEIN; TUMOR SUPPRESSOR PROTEIN; G PROTEIN COUPLED RECEPTOR; GPRC5A PROTEIN, HUMAN; MESSENGER RNA; TUMOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CARCINOMA CELL; CELL GROWTH; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GENE DELETION; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE FUNCTION; GENE MUTATION; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; LUNG ADENOCARCINOMA; LUNG CARCINOMA; LUNG NON SMALL CELL CANCER; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR GROWTH; TUMOR SUPPRESSOR GENE; ADENOCARCINOMA; ANIMAL; CANCER STEM CELL; CELL TRANSFORMATION; CHEMISTRY; COMPARATIVE STUDY; DISEASE MODEL; DRUG SCREENING; EMBRYONIC STEM CELL; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; GENETIC PREDISPOSITION; GENETIC TRANSFECTION; GENETICS; HOMOZYGOTE; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; ISOLATION AND PURIFICATION; LUNG; LUNG TUMOR; MOUSE MUTANT; MUTATION; NORTHERN BLOTTING; ONCOGENE RAS; PATHOLOGY; PROTEIN MICROARRAY; RESPIRATORY TRACT MUCOSA; SMALL CELL CARCINOMA; TUMOR CELL LINE;

ADENOCARCINOMA; ANIMALS; BLOTTING, NORTHERN; CARCINOMA, NON-SMALL-CELL LUNG; CARCINOMA, SMALL CELL; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; DISEASE MODELS, ANIMAL; EMBRYONIC STEM CELLS; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, RAS; GENES, TUMOR SUPPRESSOR; GENETIC PREDISPOSITION TO DISEASE; HOMOZYGOTE; HUMANS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LUNG; LUNG NEOPLASMS; MICE; MICE, KNOCKOUT; MUTATION; NEOPLASM PROTEINS; NEOPLASTIC STEM CELLS; PHENOTYPE; PROTEIN ARRAY ANALYSIS; RECEPTORS, G-PROTEIN-COUPLED; RESPIRATORY MUCOSA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TRANSFECTION; TUMOR STEM CELL ASSAY;

EID: 38449112841     PISSN: 00278874     EISSN: 14602105     Source Type: Journal    
DOI: 10.1093/jnci/djm208     Document Type: Article

References (61)

1. Love JM, Gudas LJ. Vitamin A, differentiation and cancer. Curr Opin Cell Biol 1994;6:825-31.
2. Sun SY, Lotan R. Retinoids and their receptors in cancer development and chemoprevention. Crit Rev Oncol Hematol 2002;41:41-55.
3. Dragnev KH, Petty WJ, Ma Y, Rigas JR, Dmitrovsky E. Nonclassical retinoids and lung carcinogenesis. Clin Lung Cancer 2005;6:237-44.
4. Bastien J, Rochette-Egly C. Nuclear retinoid receptors and the transcription of retinoid-target genes. Gene 2004;328:1-16.
5. Mark M, Chambon P. Functions of RARs and RXRs in vivo: genetic dissection of the retinoid signaling pathway. Pure Appl Chem 2003;75:1709-32.
6. Cheng Y, Lotan R. Molecular cloning and characterization of a novel retinoic acid-inducible gene that encodes a putative G protein-coupled receptor. J Biol Chem 1998;273:35008-15.
7. Recasens M, Guiramand J, Aimar R, Abdulkarim A, Barbanel G. Metabotropic glutamate receptors as drug targets. Curr Drug Targets 2007;8:651-81.
8. Tao Q, Cheng Y, Clifford J, Lotan R. Characterization of the murine orphan G-protein-coupled receptor gene Rai3 and its regulation by retinoic acid. Genomics 2004;83:270-80.
9. Robbins MJ, Michalovich D, Hill J, Calver AR, Medhurst AD, Gloger I, et al. Molecular cloning and characterization of two novel retinoic acid-inducible orphan G-protein-coupled receptors (GPRC5B and GPRC5C). Genomics 2000;67:8-18.
10. Brauner-Osborne H, Jensen A, Sheppard PO, Brodin B, Krogsgaard-Larsen P, O'Hara P. Cloning and characterization of a human orphan family C G-protein coupled receptor GPRC5D. Biochim Biophys Acta 2001;1518:237-48.
11. Inoue S, Nambu T, Shimomura T. The RAIG family member, GPRC5D, is associated with hard-keratinized structures. J Invest Dermatol 2004;122:565-73.
12. Cheng Y, Lotan D, Lotan R. Molecular cloning of mRAIG1, a mouse homologous cDNA for human RAIG1, and its expression during ATRA-induced differentiation of P19 embryonic carcinoma cells. Proc Am Assoc Cancer Res 1999;40:308.
13. Tao Q, Lotan D, Lotan R. Molecular cloning of two novel murine retinoic acid-inducible orphan G-protein-coupled receptors (mGPRC5B and mGPRC5C), their expression in adult mouse tissues and embryos, and their induction by retinoic acid during embryonal carcinoma cell differentiation. Proc Am Assoc Cancer Res 2005;46:987.
14. Cheah SS, Behringer RR. Contemporary gene targeting strategies for the novice. Mol Biotechnol 2001;19:297-304.
15. Wurst W, Joyner AL. Production of targeted embryonic stem cell clones. In: Joyner AL, editors. Gene targeting, a practical approach. Oxford (U.K): Oxford University Press; 1993. p. 33-61.
16. Xu XC, Clifford JL, Hong WK, Lotan R. Detection of nuclear retinoic acid receptor mRNAs in histological tissue sections using non-radioactive in situ hybridization histochemistry. Diagn Mol Pathol 1994;3:122-31.
17. Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JD, Simith JA, et al., editors. Current protocols in molecular biology. New York (NY): John Wiley & Sons Inc.; 2006.
18. Boorman GA, Herbert RA. Alveolar/bronchiolar hyperplasia, adenoma, and carcinoma, lung, rat. In: Jones TC, Dungworth DL, Mohr U, editors. Respiratory system. Ilsi monographs on pathology of laboratory animals. Berlin (Germany): Springer; 1996. p. 174-83.
19. Nikitin AY, Alcaraz A, Anver MR, Bronson RT, Cardiff RD, Dixon D, et al. Classification of proliferative pulmonary lesions of the mouse: recommendations of the mouse models of human cancers consortium. Cancer Res 2004;64:2307-16.
20. Chakravarti N, Mathur M, Bahadur S, Shukla NK, Rochette-Egly C, Ralhan R. Expression of RAR alpha and RAR beta in human oral potentially malignant and neoplastic lesions. Int J Cancer 2001;91:27-31.
21. Jang SJ, Soria JC, Wang L, Hassan KA, Morice RC, Walsh GL, et al. Activation of melanoma tumor antigens occurs early in lung carcinogenesis. Cancer Res 2001;61:7959-63.
22. Bhattacharjee A, Richards WG, Staunton J, Li C, Monti S, Vasa P, et al. Classification of human lung carcinomas by mRNA expression profiling reveals distinct adenocarcinoma subclasses. Proc Natl Acad Sci U S A 2001;98:13790-5. Supporting information available at http://www.pnas.org. [Last accessed: October 12, 2007.].
23. Graham FL, Smiley J, Russell WC, Nairn R. Characteristics of a human cell line transformed by DNA from human adenovirus type 5. J Gen Virol 1977;36:59-74.
24. Xu L, Schantz SP, Edelstein D, Sacks PG. A simplified method for the routine culture of normal oral epithelial (NOE) cells from upper aerodigestive tract mucosa. Methods Cell Sci 1996;18:31-9.
25. Smyth GK. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 2004;3:Article 3. Available at http://www.bepress.com/sagmb/vol3/iss1/art3. [Last accessed: October 12, 2007.].
26. The R Project for Statistical Computing. Available at: http://www.r-project.org/. [Last accessed: October 12, 2007.].
27. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 1995;57:289-300.
28. Donehower LA, Harvey M, Slagle BL, McArthur MJ, Montgomery CA, Butel JS, et al. Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 1992;356:215-21.
29. Tao Q, Lotan R. Spontaneous development of lung cancers in mice with deleted retinoic acid-inducible orphan G-protein coupled receptor gene RAI3. Proc Am Assoc Cancer Res 2004;45:876.
30. Xu J, Tian J, Shapiro SD. Normal lung development in RAIG1-deficient mice despite unique lung epithelium-specific expression. Am J Respir Cell Mol Biol 2005;32:381-7.
31. Belinsky SA, Devereux TR, Foley JF, Maronpot RR, Anderson MW. Role of the alveolar type II cell in the development and progression of pulmonary tumors induced by 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone in the A/J mouse. Cancer Res 1992;52:3164-73.
32. Sjoblom T, Jones S, Wood LD, Parsons DW, Lin J, Barber T, et al. The consensus coding sequences of human breast and colorectal cancers. Science 2006;314:268-74.
33. 6-methylguanine DNA adduct levels and Ki-ras activation in lung tumors from resistant and susceptible mouse strains. Mol Carcinog 1993;8:177-85.
34. Jackson EL, Willis N, Mercer K, Bronson RT, Crowley D, Montoya R, et al. Analysis of lung tumor initiation and progression using conditional expression of oncogenic K-ras. Genes Dev 2001;15:3243-8.
35. Malkinson AM. The genetic basis of susceptibility to lung tumors in mice. Toxicology 1989;54:241-71.
36. You M, Candrian U, Maronpot RR, Stoner GD, Anderson MW. Activation of the Ki-ras protooncogene in spontaneously occurring and chemically induced lung tumors of the strain A mouse. Proc Natl Acad Sci U S A 1989;86:3070-4.
37. Kim CF, Jackson EL, Kirsch DG, Grimm J, Shaw AT, Lane K, et al. Mouse models of human non-small-cell lung cancer: raising the bar. Cold Spring Harb Symp Quant Biol 2005;70:241-50.
38. Ji H, Li D, Chen L, Shimamura T, Kobayashi S, McNamara K, et al. The impact of human EGFR kinase domain mutations on lung tumorigenesis and in vivo sensitivity to EGFR-targeted therapies. Cancer Cell 2006;9:485-95.
39. Herzig M, Christofori G. Recent advances in cancer research: mouse models of tumorigenesis. Biochim Biophys Acta 2002;1602:97-113.
40. Kwak I, Tsai SY, DeMayo FJ. Genetically engineered mouse models for lung cancer. Annu Rev Physiol 2004;66:647-63.
41. Meuwissen R, Berns A. Mouse models for human lung cancer. Genes Dev 2005;19:643-64.
42. Whitsett JA, Glasser SW, Tichelaar JW, Perl AK, Clark JC, Wert SE. Transgenic models for study of lung morphogenesis and repair: Parker B. Francis lecture. Chest 2001;120:275-30.
43. Xian J, Clark KJ, Fordham R, Pannell R, Rabbitts TH, Rabbitts PH. Inadequate lung development and bronchial hyperplasia in mice with a targeted deletion in the Dutt1/Robo1 gene. Proc Natl Acad Sci U S A 2001;98:15062-6.
44. Xian J, Aitchison A, Bobrow L, Corbett G, Pannell R, Rabbitts T, et al. Targeted disruption of the 3p12 gene, Dutt1/Robo1, predisposes mice to lung adenocarcinomas and lymphomas with methylation of the gene promoter. Cancer Res 2004;64:6432-7.
45. Yang Y, Zhang Z, Mukherjee AB, Linnoila RI. Increased susceptibility of mice lacking Clara cell 10-kDa protein to lung tumorigenesis by 4 (methyl-nitrosamino)-1-(3-pyridyl)-1-butanone, a potent carcinogen in cigarette smoke. J Biol Chem 2004;279:29336-40.
46. Takeuchi S, Mori N, Koike M, Slater J, Park S, Miller CW, et al. Frequent loss of heterozygosity in region of the KIP1 locus in non-small cell lung cancer: evidence for a new tumor suppressor gene on the short arm of chromosome 12. Cancer Res 1996;56:738-40.
47. Grepmeier U, Dietmaier W, Merk J, Wild PJ, Obermann EC, Pfeifer M, et al. Deletions at chromosome 2q and 12p are early and frequent molecular alterations in bronchial epithelium and NSCLC of long-term smokers. Int J Oncol 2005;27:481-8.
48. Agathanggelou A, Dallol A, Zochbauer-Muller S, Morrissey C, Honorio S, Hesson L, et al. Epigenetic inactivation of the candidate 3p21.3 suppressor gene BLU in human cancers. Oncogene 2003;22:1580-8.
49. Gery S, Komatsu N, Kawamata N, Miller CW, Desmond J, Virk RK, et al. Epigenetic silencing of the candidate tumor suppressor gene Per1 in non-small cell lung cancer. Clin Cancer Res 2007;13:1399-404.
50. Dorsam RT, Gutkind JS. G-protein-coupled receptors and cancer. Nat Rev Cancer 2007;7:79-94.
51. Ohtaki T, Shintani Y, Honda S, Matsumoto H, Hori A, Kanehashi K, et al. Metastasis suppressor gene KiSS-1 encodes peptide ligand of a G-protein-coupled receptor. Nature 2001;411:613-7.
52. Sanchez T, Thangada S, Wu MT, Kontos CD, Wu D, Wu H, et al. PTEN as an effector in the signaling of antimigratory G protein-coupled receptor. Proc Natl Acad Sci U S A 2005;102:4312-7.
53. Freedman VH, Shin SI. Cellular tumorigenicity in nude mice: correlation with cell growth in semi-solid medium. Cell 1974;3:355-9.
54. Reddig PJ, Juliano RL. Clinging to life: cell to matrix adhesion and cell survival. Cancer Metastasis Rev 2005;24:425-39.
55. Quinlan KG, Verger A, Yaswen P, Crossley M. Amplification of zinc finger gene 217 (ZNF217) and cancer: when good fingers go bad. Biochim Biophys Acta 2007;1775:333-40.
56. Krig SR, Jin VX, Bieda MC, O'geen H, Yaswen P, Green R, et al. Identification of genes directly regulated by the oncogene ZNF217 using ChIP-chip assays. J Biol Chem 2007;282:9703-12.
57. Harada Y, Yokota C, Habas R, Slusarski DC, He X. Retinoic acid-inducible G protein-coupled receptors bind to frizzled receptors and may activate non-canonical Wnt signaling. Biochem Biophys Res Commun 2007;358:968-75.
58. Olson DJ, Gibo DM. Antisense wnt-5a mimics wnt-1-mediated C57MG mammary epithelial cell transformation. Exp Cell Res 1998;241:134-41.
59. Topol L, Jiang X, Choi H, Garrett-Beal L, Carolan P, Yang Y. Wnt-5a inhibits the canonical Wnt pathway by promoting GSK-3 independent β-catenin degradation. J Cell Biol 2003;162:899-908.
60. Bond RA, Ijzerman AP. Recent developments in constitutive receptor activity and inverse agonism, and their potential for GPCR drug discovery. Trends Pharmacol Sci 2006;27:92-6.
61. Wu Q, Ding W, Mirza A, Van Arsdale T, Wei I, Bishop WR, et al. Integrative genomics revealed RAI3 is a cell growth-promoting gene and a novel P53 transcriptional target. J Biol Chem 2005;280:12935-43.