Functional genomics identifies novel genes essential for clear cell renal cell carcinoma tumor cell proliferation and migration

Oncotarget

Volumn 5, Issue 14, 2014, Pages 5320-5334

  von Roemeling, Christina A ^a   Marlow, Laura A ^a   Radisky, Derek C ^a   Rohl, Austin ^a   Larsen, Hege Ekeberg ^a   Wei, Johnny ^a   Sasinowska, Heather ^b   Zhu, Heng ^d   Drake, Richard ^c   Sasinowski, Maciek ^b   Tun, Han W ^a   Copland, John A ^a  

^a MAYO CLINIC   (United States)

^b Incogen Inc ^*  (United States)

^c MUSC Proteomics Center   (United States)

^d JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Gene array; Metastasis; Renal cell carcinoma; Therapeutic targets

Indexed keywords

ARTICLE; CANCER CELL LINE; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; FUNCTIONAL GENOMICS; GENE IDENTIFICATION; GENE OVEREXPRESSION; GENETIC ASSOCIATION; GENETIC SCREENING; GENETIC TRANSCRIPTION; HUMAN; HUMAN TISSUE; KIDNEY CARCINOMA; LENTIVIRINAE; NUCLEOTIDE SEQUENCE; TUMOR CELL; TUMOR INVASION; CELL MOTION; GENE EXPRESSION PROFILING; GENETICS; GENOMICS; HIGH THROUGHPUT SEQUENCING; KIDNEY TUMOR; PATHOLOGY; PROCEDURES; TUMOR CELL LINE;

CARCINOMA, RENAL CELL; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; DOWN-REGULATION; GENE EXPRESSION PROFILING; GENOMICS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; KIDNEY NEOPLASMS;

EID: 84906236213     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2097     Document Type: Article

References (64)

1. Siegel R, Naishadham D and Jemal A. Cancer statistics, 2013. CA Cancer J Clin. 2013; 63(1):11-30.
2. Lam JS, Shvarts O and Pantuck AJ. Changing concepts in the surgical management of renal cell carcinoma. Eur Urol. 2004; 45(6):692-705.
3. Haddad H and Rini BI. Current treatment considerations in metastatic renal cell carcinoma. Curr Treat Options Oncol. 2012; 13(2):212-229.
4. Cohen HT and McGovern FJ. Renal-cell carcinoma. N Engl J Med. 2005; 353(23):2477-2490.
5. Mulders P, Figlin R, deKernion JB, Wiltrout R, Linehan M, Parkinson D, deWolf W and Belldegrun A. Renal cell carcinoma: recent progress and future directions. Cancer Res. 1997; 57(22):5189-5195.
6. Motzer RJ, Bacik J and Mazumdar M. Prognostic factors for survival of patients with stage IV renal cell carcinoma: memorial sloan-kettering cancer center experience. Clin Cancer Res. 2004; 10(18 Pt 2):6302S-6303S.
7. Coppin C, Kollmannsberger C, Le L, Porzsolt F and Wilt TJ. Targeted therapy for advanced renal cell cancer (RCC): a Cochrane systematic review of published randomised trials. BJU Int. 2011; 108(10):1556-1563.
8. Finley DS, Pantuck AJ and Belldegrun AS. Tumor biology and prognostic factors in renal cell carcinoma. Oncologist. 2011; 16 Suppl 2:4-13.
9. Jonasch E, Futreal PA, Davis IJ, Bailey ST, Kim WY, Brugarolas J, Giaccia AJ, Kurban G, Pause A, Frydman J, Zurita AJ, Rini BI, Sharma P, Atkins MB, Walker CL and Rathmell WK. State of the science: an update on renal cell carcinoma. Mol Cancer Res. 2012; 10(7):859-880.
10. Tang SW, Chang WH, Su YC, Chen YC, Lai YH, Wu PT, Hsu CI, Lin WC, Lai MK and Lin JY. MYC pathway is activated in clear cell renal cell carcinoma and essential for proliferation of clear cell renal cell carcinoma cells. Cancer Lett. 2009; 273(1):35-43.
11. Malo N, Hanley JA, Cerquozzi S, Pelletier J and Nadon R. Statistical practice in high-throughput screening data analysis. Nat Biotechnol. 2006; 24(2):167-175.
12. Ooi A, Wong JC, Petillo D, Roossien D, Perrier-Trudova V, Whitten D, Min BW, Tan MH, Zhang Z, Yang XJ, Zhou M, Gardie B, Molinie V, Richard S, Tan PH, Teh BT, et al. An antioxidant response phenotype shared between hereditary and sporadic type 2 papillary renal cell carcinoma. Cancer Cell. 2011; 20(4):511-523.
13. Kort EJ, Farber L, Tretiakova M, Petillo D, Furge KA, Yang XJ, Cornelius A and Teh BT. The E2F3-Oncomir-1 axis is activated in Wilms' tumor. Cancer Res. 2008; 68(11):4034-4038.
14. Qian CN, Huang D, Wondergem B and Teh BT. Complexity of tumor vasculature in clear cell renal cell carcinoma. Cancer. 2009; 115(10 Suppl):2282-2289.
15. Daurkin I, Eruslanov E, Stoffs T, Perrin GQ, Algood C, Gilbert SM, Rosser CJ, Su LM, Vieweg J and Kusmartsev S. Tumor-associated macrophages mediate immunosuppression in the renal cancer microenvironment by activating the 15-lipoxygenase-2 pathway. Cancer Res. 2011; 71(20):6400-6409.
16. Fujita Y, Mimata H, Nasu N, Nomura T, Nomura Y and Nakagawa M. Involvement of adrenomedullin induced by hypoxia in angiogenesis in human renal cell carcinoma. Int J Urol. 2002; 9(6):285-295.
17. Verine J, Lehmann-Che J, Soliman H, Feugeas JP, Vidal JS, Mongiat-Artus P, Belhadj S, Philippe J, Lesage M, Wittmer E, Chanel S, Couvelard A, Ferlicot S, Rioux-Leclercq N, Vignaud JM, Janin A, et al. Determination of angptl4 mRNA as a diagnostic marker of primary and metastatic clear cell renal-cell carcinoma. PLoS One. 2010; 5(4):e10421.
18. Le Jan S, Amy C, Cazes A, Monnot C, Lamande N, Favier J, Philippe J, Sibony M, Gasc JM, Corvol P and Germain S. Angiopoietin-like 4 is a proangiogenic factor produced during ischemia and in conventional renal cell carcinoma. Am J Pathol. 2003; 162(5):1521-1528.
19. Minner S, Rump D, Tennstedt P, Simon R, Burandt E, Terracciano L, Moch H, Wilczak W, Bokemeyer C, Fisch M, Sauter G and Eichelberg C. Epidermal growth factor receptor protein expression and genomic alterations in renal cell carcinoma. Cancer. 2012; 118(5):1268-1275.
20. De Luca A, Carotenuto A, Rachiglio A, Gallo M, Maiello MR, Aldinucci D, Pinto A and Normanno N. The role of the EGFR signaling in tumor microenvironment. J Cell Physiol. 2008; 214(3):559-567.
21. Pflug BR, Zheng H, Udan MS, D'Antonio JM, Marshall FF, Brooks JD and Nelson JB. Endothelin-1 promotes cell survival in renal cell carcinoma through the ET(A) receptor. Cancer Lett. 2007; 246(1-2):139-148.
22. Gonzalez AM, Gonzales M, Herron GS, Nagavarapu U, Hopkinson SB, Tsuruta D and Jones JC. Complex interactions between the laminin alpha 4 subunit and integrins regulate endothelial cell behavior in vitro and angiogenesis in vivo. Proc Natl Acad Sci U S A. 2002; 99(25):16075-16080.
23. Vainionpaa N, Lehto VP, Tryggvason K and Virtanen I. Alpha4 chain laminins are widely expressed in renal cell carcinomas and have a de-adhesive function. Lab Invest. 2007; 87(8):780-791.
24. Smallridge RC, Copland JA, Brose MS, Wadsworth JT, Houvras Y, Menefee ME, Bible KC, Shah MH, Gramza AW, Klopper JP, Marlow LA, Heckman MG and Von Roemeling R. Efatutazone, an oral PPAR-gamma agonist, in combination with paclitaxel in anaplastic thyroid cancer: results of a multicenter phase 1 trial. J Clin Endocrinol Metab. 2013; 98(6):2392-2400.
25. Mohamed AJ, Yu L, Backesjo CM, Vargas L, Faryal R, Aints A, Christensson B, Berglof A, Vihinen M, Nore BF and Smith CI. Bruton's tyrosine kinase (Btk): function, regulation, and transformation with special emphasis on the PH domain. Immunol Rev. 2009; 228(1):58-73.
26. Behbahani TE, Thierse C, Baumann C, Holl D, Bastian PJ, von Ruecker A, Muller SC, Ellinger J and Hauser S. Tyrosine kinase expression profile in clear cell renal cell carcinoma. World J Urol. 2012; 30(4):559-565.
27. Nam JS, Hirohashi S and Wakefield LM. Dysadherin: a new player in cancer progression. Cancer Lett. 2007; 255(2):161-169.
28. Ino Y, Gotoh M, Sakamoto M, Tsukagoshi K and Hirohashi S. Dysadherin, a cancer-associated cell membrane glycoprotein, down-regulates E-cadherin and promotes metastasis. Proc Natl Acad Sci U S A. 2002; 99(1):365-370.
29. Schuler Y, Lee-Thedieck C, Geiger K, Kaiser T, Ino Y, Aicher WK and Klein G. Osteoblast-secreted factors enhance the expression of dysadherin and CCL2-dependent migration of renal carcinoma cells. Int J Cancer. 2012; 130(2):288-299.
30. Berx G and van Roy F. Involvement of members of the cadherin superfamily in cancer. Cold Spring Harb Perspect Biol. 2009; 1(6):a003129.
31. Therrien M, Chang HC, Solomon NM, Karim FD, Wassarman DA and Rubin GM. KSR, a novel protein kinase required for RAS signal transduction. Cell. 1995; 83(6):879-888.
32. Llobet D, Eritja N, Domingo M, Bergada L, Mirantes C, Santacana M, Pallares J, Macia A, Yeramian A, Encinas M, Moreno-Bueno G, Palacios J, Lewis RE, Matias-Guiu X and Dolcet X. KSR1 is overexpressed in endometrial carcinoma and regulates proliferation and TRAIL-induced apoptosis by modulating FLIP levels. Am J Pathol. 2011; 178(4):1529-1543.
33. Fisher KW, Das B, Kortum RL, Chaika OV and Lewis RE. Kinase suppressor of ras 1 (KSR1) regulates PGC1alpha and estrogen-related receptor alpha to promote oncogenic Ras-dependent anchorage-independent growth. Mol Cell Biol. 2011; 31(12):2453-2461.
34. van der Slot AJ, Zuurmond AM, Bardoel AF, Wijmenga C, Pruijs HE, Sillence DO, Brinckmann J, Abraham DJ, Black CM, Verzijl N, DeGroot J, Hanemaaijer R, TeKoppele JM, Huizinga TW and Bank RA. Identification of PLOD2 as telopeptide lysyl hydroxylase, an important enzyme in fibrosis. J Biol Chem. 2003; 278(42):40967-40972.
35. Gilkes DM, Bajpai S, Wong CC, Chaturvedi P, Hubbi ME, Wirtz D and Semenza GL. Procollagen lysyl hydroxylase 2 is essential for hypoxia-induced breast cancer metastasis. Mol Cancer Res. 2013; 11(5):456-466.
36. Tanaka T, Yamaguchi J, Shoji K and Nangaku M. Anthracycline inhibits recruitment of hypoxia-inducible transcription factors and suppresses tumor cell migration and cardiac angiogenic response in the host. J Biol Chem. 2012; 287(42):34866-34882.
37. Tang SW, Yang TC, Lin WC, Chang WH, Wang CC, Lai MK and Lin JY. Nicotinamide N-methyltransferase induces cellular invasion through activating matrix metalloproteinase-2 expression in clear cell renal cell carcinoma cells. Carcinogenesis. 2011; 32(2):138-145.
38. Yoshino H, Enokida H, Itesako T, Tatarano S, Kinoshita T, Fuse M, Kojima S, Nakagawa M and Seki N. Epithelial-mesenchymal transition-related microRNA-200s regulate molecular targets and pathways in renal cell carcinoma. J Hum Genet. 2013; 58(8):508-516.
39. Chedotal A, Kerjan G and Moreau-Fauvarque C. The brain within the tumor: new roles for axon guidance molecules in cancers. Cell Death Differ. 2005; 12(8):1044-1056.
40. Dhanabal M, Wu F, Alvarez E, McQueeney KD, Jeffers M, MacDougall J, Boldog FL, Hackett C, Shenoy S, Khramtsov N, Weiner J, Lichenstein HS and LaRochelle WJ. Recombinant semaphorin 6A-1 ectodomain inhibits in vivo growth factor and tumor cell line-induced angiogenesis. Cancer Biol Ther. 2005; 4(6):659-668.
41. Fu L, Wang G, Shevchuk MM, Nanus DM and Gudas LJ. Activation of HIF2alpha in kidney proximal tubule cells causes abnormal glycogen deposition but not tumorigenesis. Cancer Res. 2013; 73(9):2916-2925.
42. Yano Y, Hayashi Y, Sano K, Shinmaru H, Kuroda Y, Yokozaki H, Yoon S and Kasuga M. Expression and localization of ecto-nucleotide pyrophosphatase/phosphodiesterase I-3 (E-NPP3/CD203c/PD-I beta/B10/gp130RB13-6) in human colon carcinoma. Int J Mol Med. 2003; 12(5):763-766.
43. Yano Y, Hayashi Y, Sano K, Nagano H, Nakaji M, Seo Y, Ninomiya T, Yoon S, Yokozaki H and Kasuga M. Expression and localization of ecto-nucleotide pyrophosphatase/phosphodiesterase I-1 (E-NPP1/PC-1) and-3 (E-NPP3/CD203c/PD-Ibeta/B10/gp130(RB13-6)) in inflammatory and neoplastic bile duct diseases. Cancer Lett. 2004; 207(2):139-147.
44. Fluge O, Bruland O, Akslen LA, Lillehaug JR and Varhaug JE. Gene expression in poorly differentiated papillary thyroid carcinomas. Thyroid. 2006; 16(2):161-175.
45. Furge KA, Tan MH, Dykema K, Kort E, Stadler W, Yao X, Zhou M and Teh BT. Identification of deregulated oncogenic pathways in renal cell carcinoma: an integrated oncogenomic approach based on gene expression profiling. Oncogene. 2007; 26(9):1346-1350.
46. Safarinejad MR. Insulin-like growth factor binding protein-3 (IGFBP-3) gene variants are associated with renal cell carcinoma. BJU Int. 2011; 108(5):762-770.
47. Xian L, Wu X, Pang L, Lou M, Rosen CJ, Qiu T, Crane J, Frassica F, Zhang L, Rodriguez JP, Xiaofeng J, Shoshana Y, Shouhong X, Argiris E, Mei W and Xu C. Matrix IGF-1 maintains bone mass by activation of mTOR in mesenchymal stem cells. Nat Med. 2012; 18(7):1095-1101.
48. Shoji S, Tang XY, Umemura S, Itoh J, Takekoshi S, Shima M, Usui Y, Nagata Y, Uchida T, Osamura RY and Terachi T. Metastin inhibits migration and invasion of renal cell carcinoma with overexpression of metastin receptor. Eur Urol. 2009; 55(2):441-449.
49. Yoshioka K, Ohno Y, Horiguchi Y, Ozu C, Namiki K and Tachibana M. Effects of a KiSS-1 peptide, a metastasis suppressor gene, on the invasive ability of renal cell carcinoma cells through a modulation of a matrix metalloproteinase 2 expression. Life Sci. 2008; 83(9-10):332-338.
50. Cvetkovic D, Babwah AV and Bhattacharya M. Kisspeptin/KISS1R System in Breast Cancer. J Cancer. 2013; 4(8):653-661.
51. Takai N, Ueda T, Nasu K, Yamashita S, Toyofuku M and Narahara H. Targeting calcium/calmodulin-dependence kinase I and II as a potential anti-proliferation remedy for endometrial carcinomas. Cancer Lett. 2009; 277(2):235-243.
52. Colomer J and Means AR. Physiological roles of the Ca2+/CaM-dependent protein kinase cascade in health and disease. Subcell Biochem. 2007; 45:169-214.
53. Marshall JL and Crosbie-Watson RH. Sarcospan: a small protein with large potential for Duchenne muscular dystrophy. Skelet Muscle. 2013; 3(1):1.
54. Falvella FS, Colombo F, Spinola M, Campiglio M, Pastorino U and Dragani TA. BHLHB3: a candidate tumor suppressor in lung cancer. Oncogene. 2008; 27(26):3761-3764.
55. Reinhold WC, Reimers MA, Lorenzi P, Ho J, Shankavaram UT, Ziegler MS, Bussey KJ, Nishizuka S, Ikediobi O, Pommier YG and Weinstein JN. Multifactorial regulation of E-cadherin expression: an integrative study. Mol Cancer Ther. 2010; 9(1):1-16.
56. Krause M, Dent EW, Bear JE, Loureiro JJ and Gertler FB. Ena/VASP proteins: regulators of the actin cytoskeleton and cell migration. Annu Rev Cell Dev Biol. 2003; 19:541-564.
57. Baldewijns MM, Thijssen VL, Van den Eynden GG, Van Laere SJ, Bluekens AM, Roskams T, van Poppel H, De Bruine AP, Griffioen AW and Vermeulen PB. High-grade clear cell renal cell carcinoma has a higher angiogenic activity than low-grade renal cell carcinoma based on histomorphological quantification and qRT-PCR mRNA expression profile. Br J Cancer. 2007; 96(12):1888-1895.
58. Cooper SJ, von Roemeling CA, Kang KH, Marlow LA, Grebe SK, Menefee ME, Tun HW, Colon-Otero G, Perez EA and Copland JA. Reexpression of tumor suppressor, sFRP1, leads to antitumor synergy of combined HDAC and methyltransferase inhibitors in chemoresistant cancers. Mol Cancer Ther. 2012; 11(10):2105-2115.
59. Grossman HB, Wedemeyer G and Ren LQ. Human renal carcinoma: characterization of five new cell lines. J Surg Oncol. 1985; 28(3):237-244.
60. Tun HW, Marlow LA, von Roemeling CA, Cooper SJ, Kreinest P, Wu K, Luxon BA, Sinha M, Anastasiadis PZ and Copland JA. Pathway signature and cellular differentiation in clear cell renal cell carcinoma. PLoS One. 2010; 5(5):e10696.
61. Kupershmidt I, Su QJ, Grewal A, Sundaresh S, Halperin I, Flynn J, Shekar M, Wang H, Park J, Cui W, Wall GD, Wisotzkey R, Alag S, Akhtari S and Ronaghi M. Ontology-based meta-analysis of global collections of high-throughput public data. PLoS One. 2010; 5(9).
62. Makarenkov V, Kevorkov D, Zentilli P, Gagarin A, Malo N and Nadon R. HTS-Corrector: software for the statistical analysis and correction of experimental high-throughput screening data. Bioinformatics. 2006; 22(11):1408-1409.
63. Schmittgen TD and Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc. 2008; 3(6):1101-1108.
64. Storz P, Doppler H, Copland JA, Simpson KJ and Toker A. FOXO3a promotes tumor cell invasion through the induction of matrix metalloproteinases. Mol Cell Biol. 2009; 29(18):4906-4917.