Birt-Hogg-Dubé renal tumors are genetically distinct from other renal neoplasias and are associated with up-regulation of mitochondrial gene expression

BMC Medical Genomics

Volumn 3, Issue , 2010, Pages

  Klomp, Jeff A ^a   Petillo, David ^a   Niemi, Natalie M ^a   Dykema, Karl J ^a   Chen, Jindong ^a   Yang, Ximing J ^b   Sääf, Annika ^c   Zickert, Peter ^c   Aly, Markus ^d   Bergerheim, Ulf ^d   Nordenskjöld, Magnus ^c   Gad, Sophie ^e   Giraud, Sophie ^f,g   Denoux, Yves ^h   Yonneau, Laurent ^h   Méjean, Arnaud ^g,i   Vasiliu, Viorel ^g,i   Richard, Stéphane ^e   MacKeigan, Jeffrey P ^a   Teh, Bin T ^a,j   Furge, Kyle A ^a   more..

^a VAN ANDEL RESEARCH INSTITUTE   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^d DANDERYD HOSPITAL   (Sweden)

^e INSTITUT GUSTAVE ROUSSY   (France)

^f EDOUARD HERRIOT HOSPITAL   (France)

^g BICÊTRE HOSPITAL   (France)

^h FOCH HOSPITAL   (France)

ⁱ HÔPITAL NECKER ENFANTS MALADES   (France)

^j DIVISION OF MEDICAL ONCOLOGY   (Singapore)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CADHERIN; CADHERIN 19; DNA; ESTRONE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; LEUCINE RICH REPEAT TRANSMEMBRANE NEURONAL 4 PROTEIN; MEMBRANE PROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; RGS PROTEIN; RGS20 PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR A; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; HEAT SHOCK PROTEIN; MITOCHONDRIAL PROTEIN; PPARGC1A PROTEIN, HUMAN; TFAM PROTEIN, HUMAN;

ARTICLE; BIRT HOGG DUBE SYNDROME; CHROMOSOME ANALYSIS; CONTROLLED STUDY; DNA SEQUENCE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE MUTATION; GENETIC DIFFERENCE; HUMAN; HUMAN CELL; HUMAN TISSUE; KIDNEY CANCER; MITOCHONDRIAL GENE; OXIDATIVE PHOSPHORYLATION; PHENOTYPE; PRIORITY JOURNAL; PROTEIN INTERACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UPREGULATION; GENETICS; KIDNEY CARCINOMA; KIDNEY TUMOR; METABOLISM; ONCOCYTOMA;

ADENOMA, OXYPHILIC; BIRT-HOGG-DUBE SYNDROME; CARCINOMA, RENAL CELL; DNA-BINDING PROTEINS; ESTRONE; GENES, MITOCHONDRIAL; HEAT-SHOCK PROTEINS; HUMANS; KIDNEY NEOPLASMS; MITOCHONDRIAL PROTEINS; OXIDATIVE PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; UP-REGULATION;

EID: 78650118680     PISSN: None     EISSN: 17558794     Source Type: Journal    
DOI: 10.1186/1755-8794-3-59     Document Type: Article

References (68)

1. WHO International Histological Classification of Tumors. FK Mostofi CJ Davis, Berlin: Springer 1998
2. Molecular differential pathology of renal cell tumours. G Kovacs, Histopathology 1993 22 1 8 10.1111/j.1365-2559.1993.tb00061.x 8436337 (Pubitemid 23043987)
3. Gene expression patterns in renal cell carcinoma assessed by complementary DNA microarray. JP Higgins R Shinghal H Gill JH Reese M Terris RJ Cohen M Fero JR Pollack M Van De Rijn JD Brooks, Am J Pathol 2003 162 3 925 932 12598325
4. Molecular subclassification of kidney tumors and the discovery of new diagnostic markers. M Takahashi XJ Yang J Sugimura J Backdahl M Tretiakova CN Qian SG Gray R Knapp J Anema R Kahnoski,, et al. Oncogene 2003 22 43 6810 6818 10.1038/sj.onc.1206869 14555994
5. Molecular pathology of renal oncocytoma: a review. MV Yusenko, Int J Urol 17 7 602 612 10.1111/j.1442-2042.2010.02574.x 20590944
6. Molecular pathology of chromophobe renal cell carcinoma: a review. MV Yusenko, Int J Urol 17 7 592 600 10.1111/j.1442-2042.2010.02558.x 20590942
7. Renal oncocytoma: a clinicopathological analysis of 45 consecutive cases. T Gudbjartsson S Hardarson V Petursdottir A Thoroddsen J Magnusson GV Einarsson, BJU Int 2005 96 9 1275 1279 10.1111/j.1464-410X.2005.05827.x 16287444
8. Identification of the genes for kidney cancer: opportunity for disease-specific targeted therapeutics. WM Linehan PA Pinto R Srinivasan M Merino P Choyke L Choyke J Coleman J Toro G Glenn C Vocke,, et al. Clin Cancer Res 2007 13 2 Pt 2 671s 679s 10.1158/1078-0432.CCR-06-1870 17255292
9. The von Hippel-Lindau tumor suppressor protein and clear cell renal carcinoma. WG Kaelin, Clin Cancer Res 2007 13 680 684 10.1158/1078-0432.CCR-06- 1865
10. Improved identification of von Hippel-Lindau gene alterations in clear cell renal tumors. ML Nickerson E Jaeger Y Shi JA Durocher S Mahurkar D Zaridze V Matveev V Janout H Kollarova V Bencko,, et al. Clin Cancer Res 2008 14 15 4726 4734 10.1158/1078-0432.CCR-07-4921 18676741
11. Birt-Hogg-Dube syndrome: diagnosis and management. FH Menko MA van Steensel S Giraud L Friis-Hansen S Richard S Ungari M Nordenskjold TV Hansen J Solly ER Maher, Lancet Oncol 2009 10 12 1199 1206 10.1016/S1470-2045(09)70188-3 19959076
12. BHD mutations, clinical and molecular genetic investigations of Birt-Hogg-Dube syndrome: a new series of 50 families and a review of published reports. JR Toro MH Wei GM Glenn M Weinreich O Toure C Vocke M Turner P Choyke MJ Merino PA Pinto,, et al. J Med Genet 2008 45 6 321 331 10.1136/jmg.2007. 054304 18234728
13. Mutations in a novel gene lead to kidney tumors, lung wall defects, and benign tumors of the hair follicle in patients with the Birt-Hogg-Dube syndrome. ML Nickerson MB Warren JR Toro V Matrosova G Glenn ML Turner P Duray M Merino P Choyke CP Pavlovich,, et al. Cancer Cell 2002 2 2 157 164 10.1016/S1535- 6108(02)00104-6 12204536
14. Renal tumors in the Birt-Hogg-Dube syndrome. CP Pavlovich MM Walther RA Eyler SM Hewitt B Zbar WM Linehan MJ Merino, Am J Surg Pathol 2002 26 12 1542 1552 10.1097/00000478-200212000-00002 12459621
15. Birt-Hogg-Dube syndrome: clinicopathologic findings and genetic alterations. BP Adley ND Smith R Nayar XJ Yang, Arch Pathol Lab Med 2006 130 12 1865 1870 17149965
16. Inactivation of BHD in sporadic renal tumors. SK Khoo K Kahnoski J Sugimura D Petillo J Chen K Shockley J Ludlow R Knapp S Giraud S Richard,, et al. Cancer Res 2003 63 15 4583 4587 12907635
17. Mutations in BHD and TP53 genes, but not in HNF1beta gene, in a large series of sporadic chromophobe renal cell carcinoma. S Gad SH Lefevre SK Khoo S Giraud A Vieillefond V Vasiliu S Ferlicot V Molinie Y Denoux N Thiounn,, et al. Br J Cancer 2007 96 2 336 340 10.1038/sj.bjc.6603492 17133269
18. Transgenic rescue from embryonic lethality and renal carcinogenesis in the Nihon rat model by introduction of a wild-type Bhd gene. Y Togashi T Kobayashi S Momose M Ueda K Okimoto O Hino, Oncogene 2006 25 20 2885 2889 10.1038/sj.onc.1209317 16369488
19. High frequency of somatic frameshift BHD gene mutations in Birt-Hogg-Dube-associated renal tumors. CD Vocke Y Yang CP Pavlovich LS Schmidt ML Nickerson CA Torres-Cabala MJ Merino MM Walther B Zbar WM Linehan, J Natl Cancer Inst 2005 97 12 931 935 10.1093/jnci/dji154 15956655
20. Folliculin encoded by the BHD gene interacts with a binding protein, FNIP1, and AMPK, and is involved in AMPK and mTOR signaling. M Baba SB Hong N Sharma MB Warren ML Nickerson A Iwamatsu D Esposito WK Gillette RF Hopkins JL Hartley,, et al. Proc Natl Acad Sci USA 2006 103 42 15552 15557 10.1073/pnas.0603781103 17028174
21. The role of the Birt-Hogg-Dube protein in mTOR activation and renal tumorigenesis. TR Hartman E Nicolas A Klein-Szanto T Al-Saleem TP Cash MC Simon EP Henske, Oncogene 2009 28 13 1594 1604 10.1038/onc.2009.14 19234517
22. Homozygous loss of BHD causes early embryonic lethality and kidney tumor development with activation of mTORC1 and mTORC2. Y Hasumi M Baba R Ajima H Hasumi VA Valera ME Klein DC Haines MJ Merino SB Hong TP Yamaguchi,, et al. Proc Natl Acad Sci USA 2009 106 44 18722 18727 10.1073/pnas.0908853106 19850877
23. Identification and characterization of a novel folliculin-interacting protein FNIP2. H Hasumi M Baba SB Hong Y Hasumi Y Huang M Yao VA Valera WM Linehan LS Schmidt, Gene 2008 415 1-2 60 67 10.1016/j.gene.2008.02.022 18403135
24. Interaction of folliculin (Birt-Hogg-Dube gene product) with a novel Fnip1-like (FnipL/Fnip2) protein. Y Takagi T Kobayashi M Shiono L Wang X Piao G Sun D Zhang M Abe Y Hagiwara K Takahashi,, et al. Oncogene 2008 27 40 5339 5347 10.1038/onc.2008.261 18663353
25. Molecular classification of renal tumors by gene expression profiling. AN Schuetz Q Yin-Goen MB Amin CS Moreno C Cohen CD Hornsby WL Yang JA Petros MM Issa JG Pattaras,, et al. J Mol Diagn 2005 7 2 206 218 15858144
26. Loss of complex I due to mitochondrial DNA mutations in renal oncocytoma. JA Mayr D Meierhofer F Zimmermann R Feichtinger C Kogler M Ratschek N Schmeller W Sperl B Kofler, Clin Cancer Res 2008 14 8 2270 2275 10.1158/1078-0432.CCR-07- 4131 18413815
27. Clonal expansion of mutated mitochondrial DNA is associated with tumor formation and complex I deficiency in the benign renal oncocytoma. G Gasparre E Hervouet E de Laplanche J Demont LF Pennisi M Colombel F Mege-Lechevallier JY Scoazec E Bonora R Smeets,, et al. Hum Mol Genet 2008 17 7 986 995 10.1093/hmg/ddm371 18156159
28. Mitochondrial and chromosomal DNA alterations in human chromophobe renal cell carcinomas. A Kovacs S Storkel W Thoenes G Kovacs, J Pathol 1992 167 3 273 277 10.1002/path.1711670303 1381433
29. Alteration of mitochondrial DNA in human oncocytomas. C Welter G Kovacs G Seitz N Blin, Genes Chromosomes Cancer 1989 1 1 79 82 10.1002/gcc.2870010112 2487148
30. Analysis of differentially expressed mitochondrial proteins in chromophobe renal cell carcinomas and renal oncocytomas by 2-D gel electrophoresis. MV Yusenko T Ruppert G Kovacs, Int J Biol Sci 6 3 213 224 20440404
31. Identification and characterization of Birt-Hogg-Dube associated renal carcinoma. T Murakami F Sano Y Huang A Komiya M Baba Y Osada Y Nagashima K Kondo N Nakaigawa T Miura,, et al. J Pathol 2007 211 5 524 531 10.1002/path.2139 17323425
32. A molecular classification of papillary renal cell carcinoma. XJ Yang MH Tan HL Kim JA Ditlev MW Betten CE Png EJ Kort K Futami KA Furge M Takahashi,, et al. Cancer Res 2005 65 13 5628 5637 10.1158/0008-5472.CAN-05-0533 15994935
33. Clinical and genetic studies of Birt-Hogg-Dube syndrome. SK Khoo S Giraud K Kahnoski J Chen O Motorna R Nickolov O Binet D Lambert J Friedel R Levy,, et al. J Med Genet 2002 39 12 906 912 10.1136/jmg.39.12.906 12471204
34. R: A language for data analysis and graphics. R Ihaka R Gentleman, J Comput Graph Stat 1996 5 299 314 10.2307/1390807
35. Bioconductor: open software development for computational biology and bioinformatics. RC Gentleman VJ Carey DM Bates B Bolstad M Dettling S Dudoit B Ellis L Gautier Y Ge J Gentry,, et al. Genome Biol 2004 5 80 10.1186/gb-2004-5-10-r80 15461798
36. Evolving gene/transcript definitions significantly alter the interpretation of GeneChip data. M Dai P Wang AD Boyd G Kostov B Athey EG Jones WE Bunney RM Myers TP Speed H Akil,, et al. Nucleic Acids Res 2005 33 20 175 10.1093/nar/gni179 16284200
37. PerlPrimer: cross-platform, graphical primer design for standard, bisulphite and real-time PCR. OJ Marshall, Bioinformatics 2004 20 15 2471 2472 10.1093/bioinformatics/bth254 15073005
38. Pvclust: an R package for assessing the uncertainty in hierarchical clustering. R Suzuki H Shimodaira, Bioinformatics 2006 22 12 1540 1542 10.1093/bioinformatics/btl117 16595560
39. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. GK Smyth, Stat Appl Genet Mol Biol 2004 3 rticle3 16646809
40. Comparison of array-based comparative genomic hybridization with gene expression-based regional expression biases to identify genetic abnormalities in hepatocellular carcinoma. KA Furge KJ Dykema C Ho X Chen, BMC Genomics 2005 6 1 67 10.1186/1471-2164-6-67 15882461
41. Detection of DNA copy number changes and oncogenic signaling abnormalities from gene expression data reveals MYC activation in high-grade papillary renal cell carcinoma. KA Furge J Chen J Koeman P Swiatek K Dykema K Lucin R Kahnoski XJ Yang BT Teh, Cancer Res 2007 67 7 3171 3176 10.1158/0008-5472.CAN-06-4571 17409424
42. Parvalbumin is constantly expressed in chromophobe renal carcinoma. G Martignoni M Pea M Chilosi M Brunelli A Scarpa C Colato R Tardanico G Zamboni F Bonetti, Mod Pathol 2001 14 8 760 767 10.1038/modpathol.3880386 11504835
43. Patterns of gene expression and copy-number alterations in von-hippel lindau disease-associated and sporadic clear cell carcinoma of the kidney. R Beroukhim JP Brunet A Di Napoli KD Mertz A Seeley MM Pires D Linhart RA Worrell H Moch MA Rubin,, et al. Cancer Res 2009 69 11 4674 4681 10.1158/0008-5472.CAN- 09-0146 19470766
44. Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer. SA Tomlins DR Rhodes S Perner SM Dhanasekaran R Mehra XW Sun S Varambally X Cao J Tchinda R Kuefer,, et al. Science 2005 310 5748 644 648 10.1126/science.1117679 16254181
45. Prediction of chromosomal aneuploidy from gene expression data. L Hertzberg DR Betts SC Raimondi BW Schafer DA Notterman E Domany S Izraeli, Genes Chromosomes Cancer 2006 46 1 75 86 10.1002/gcc.20391
46. High Incidence of Chromosome 1 Abnormalities in a Series of 27 Renal Oncocytomas: Cytogenetic and Fluorecence In Situ Hybridzation Studies. GP Paner V Lindgren MS Jacobson K Harrison Y Cao SC Campbell RC Flanigan MM Picken, Arch Path Lab Medicine 2006 131 81 85
47. Somatic pairing of chromosome 19 in renal oncocytoma is associated with deregulated EGLN2-mediated oxygen sensing response. JM Koeman RC Russell MH Tan D Petillo M Westphal K Koelzer JL Metcalf Z Zhang KJ Dykema HL Houseman,, et al. PLoS Genet 2008 4 1000176 10.1371/journal.pgen.1000176 18773095
48. Familial and sporadic renal oncocytomas - a comparative molecular-genetic analysis. K Junker G Weirich P Moravek M Podhola B Ilse A Hartmann J Schubert, Eur Urol 2001 40 3 330 336 10.1159/000049795 11684851
49. The UOK 257 cell line: a novel model for studies of the human Birt-Hogg-Dube gene pathway. Y Yang HM Padilla-Nash MA Vira MS Abu-Asab D Val R Worrell M Tsokos MJ Merino CP Pavlovich T Ried,, et al. Cancer Genet Cytogenet 2008 180 2 100 109 10.1016/j.cancergencyto.2007.10.010 18206534
50. Fine mapping of the human renal oncocytoma-associated translocation (5;11)(q35;q13) breakpoint. RJ Sinke T Dijkhuizen B Janssen D Olde Weghuis G Merkx E van den Berg E Schuuring AM Meloni B de Jong A Geurts van Kessel, Cancer Genet Cytogenet 1997 96 2 95 101 10.1016/S0165-4608(96)00250-6 9216713
51. Identification of deregulated oncogenic pathways in renal cell carcinoma: an integrated oncogenomic approach based on gene expression profiling. KA Furge MH Tan K Dykema E Kort W Stadler X Yao M Zhou BT Teh, Oncogene 2007 26 9 1346 1350 10.1038/sj.onc.1210256 17322920
52. The E2F3-Oncomir-1 axis is activated in Wilms' tumor. EJ Kort L Farber M Tretiakova D Petillo KA Furge XJ Yang A Cornelius BT Teh, Cancer Res 2008 68 11 4034 4038 10.1158/0008-5472.CAN-08-0592 18519660
53. Activation of the PI3K/AKT pathway induces urothelial carcinoma of the renal pelvis: identification in human tumors and confirmation in animal models. CN Qian KA Furge J Knol D Huang J Chen KJ Dykema EJ Kort A Massie SK Khoo K Vanden Beldt,, et al. Cancer Res 2009 69 21 8256 8264 10.1158/0008-5472.CAN-09- 1689 19843858
54. Gene expression profiling separates chromophobe renal cell carcinoma from oncocytoma and identifies vesicular transport and cell junction proteins as differentially expressed genes. S Rohan JJ Tu J Kao P Mukherjee F Campagne XK Zhou E Hyjek MA Alonso YT Chen, Clin Cancer Res 2006 12 23 6937 6945 10.1158/1078-0432.CCR-06-1268 17145811
55. PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. VK Mootha CM Lindgren KF Eriksson A Subramanian S Sihag J Lehar P Puigserver E Carlsson M Ridderstrale E Laurila,, et al. Nat Genet 2003 34 3 267 273 10.1038/ng1180 12808457
56. Transcriptional paradigms in mammalian mitochondrial biogenesis and function. RC Scarpulla, Physiol Rev 2008 88 2 611 638 10.1152/physrev.00025.2007 18391175
57. Transcriptional control of mitochondrial biogenesis and function. MB Hock A Kralli, Annu Rev Physiol 2009 71 177 203 10.1146/annurev.physiol.010908. 163119 19575678
58. Transcriptional control of mitochondrial biogenesis: the central role of PGC-1alpha. R Ventura-Clapier A Garnier V Veksler, Cardiovasc Res 2008 79 2 208 217 10.1093/cvr/cvn098 18430751
59. Receptor-selective coactivators as tools to define the biology of specific receptor-coactivator pairs. S Gaillard LL Grasfeder CL Haeffele EK Lobenhofer TM Chu R Wolfinger D Kazmin TR Koves DM Muoio CY Chang,, et al. Mol Cell 2006 24 5 797 803 10.1016/j.molcel.2006.10.012 17157261
60. EEDA: a protein associated with an early stage of stratified epithelial differentiation. L Sun DG Ryan M Zhou TT Sun RM Lavker, J Cell Physiol 2006 206 1 103 111 10.1002/jcp.20433 15920738
61. Kidney-targeted Birt-Hogg-Dube gene inactivation in a mouse model: Erk1/2 and Akt-mTOR activation, cell hyperproliferation, and polycystic kidneys. M Baba M Furihata SB Hong L Tessarollo DC Haines E Southon V Patel P Igarashi WG Alvord R Leighty,, et al. J Natl Cancer Inst 2008 100 2 140 154 10.1093/jnci/djm288 18182616
62. Deficiency of FLCN in mouse kidney led to development of polycystic kidneys and renal neoplasia. J Chen K Futami D Petillo J Peng P Wang J Knol Y Li SK Khoo D Huang CN Qian,, et al. PLoS ONE 2008 3 10 3581 10.1371/journal.pone. 0003581 18974783
63. mTOR controls mitochondrial oxidative function through a YY1-PGC-1alpha transcriptional complex. JT Cunningham JT Rodgers DH Arlow F Vazquez VK Mootha P Puigserver, Nature 2007 450 7170 736 740 10.1038/nature06322 18046414
64. Chromophobe renal cell carcinoma: histomorphologic characteristics and evaluation of conventional pathologic prognostic parameters in 145 cases. MB Amin GP Paner I Alvarado-Cabrero AN Young HJ Stricker RH Lyles H Moch, Am J Surg Pathol 2008 32 12 1822 1834 10.1097/PAS.0b013e3181831e68 18813125
65. Defective oxidative phosphorylation in thyroid oncocytic carcinoma is associated with pathogenic mitochondrial DNA mutations affecting complexes I and III. E Bonora AM Porcelli G Gasparre A Biondi A Ghelli V Carelli A Baracca G Tallini A Martinuzzi G Lenaz,, et al. Cancer Res 2006 66 12 6087 6096 10.1158/0008-5472.CAN-06-0171 16778181
66. PGC-1-related coactivator and targets are upregulated in thyroid oncocytoma. F Savagner D Mirebeau C Jacques S Guyetant C Morgan B Franc P Reynier Y Malthiery, Biochem Biophys Res Commun 2003 310 3 779 784 10.1016/j.bbrc.2003.09.076 14550271
67. Mitochondrial DNA expression in mitochondrial myopathies and coordinated expression of nuclear genes involved in ATP production. A Heddi P Lestienne DC Wallace G Stepien, J Biol Chem 1993 268 16 12156 12163 8505336
68. PGC-1alpha/beta upregulation is associated with improved oxidative phosphorylation in cells harboring nonsense mtDNA mutations. S Srivastava JN Barrett CT Moraes, Hum Mol Genet 2007 16 8 993 1005 10.1093/hmg/ddm045 17341490