Partial loss of Smad signaling during in vitro progression of HPV16-immortalized human keratinocytes

BMC Cancer

Volumn 13, Issue , 2013, Pages

  Altomare, Diego ^a   Velidandla, Rupa ^a   Pirisi, Lucia ^b   Creek, Kim E ^a  

^a UNIVERSITY OF SOUTH CAROLINA   (United States)

^b UNIVERSITY OF SOUTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

HPV mediated transformation; Human keratinocytes; Smads; TGF signaling

Indexed keywords

LUCIFERASE; SMAD PROTEIN; SMAD2 PROTEIN; SMAD3 PROTEIN; SMAD4 PROTEIN; SMAD7 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1;

ARTICLE; CELL IMMORTALIZATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN PAPILLOMAVIRUS TYPE 16; HUMAN TISSUE; IMMUNOFLUORESCENCE TEST; IN VITRO STUDY; INTRACELLULAR SIGNALING; KERATINOCYTE; MALE; NEWBORN; NUCLEAR LOCALIZATION SIGNAL; PAPILLOMAVIRUS INFECTION; PROTEIN DEFECT; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; WESTERN BLOTTING;

CELL LINE, TRANSFORMED; CELL NUCLEUS; HUMAN PAPILLOMAVIRUS 16; HUMANS; KERATINOCYTES; PHOSPHORYLATION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; SMAD PROTEINS; SMAD2 PROTEIN; SMAD3 PROTEIN; SMAD4 PROTEIN; SMAD7 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84884183730     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-13-424     Document Type: Article

References (44)

1. Padua D, Massague J. Roles of TGFbeta in metastasis. Cell Res 2009, 19:89-102. 10.1038/cr.2008.316, 19050696.
2. Huang SS, Huang JS. TGF-beta control of cell proliferation. J Cell Biochem 2005, 96:447-462. 10.1002/jcb.20558, 16088940.
3. Massague J, Gomis RR. The logic of TGFbeta signaling. FEBS Lett 2006, 580:2811-2820. 10.1016/j.febslet.2006.04.033, 16678165.
4. Moustakas A, Pardali K, Gaal A, Heldin CH. Mechanisms of TGF-beta signaling in regulation of cell growth and differentiation. Immunol Lett 2002, 82:85-91. 10.1016/S0165-2478(02)00023-8, 12008039.
5. Rahimi RA, Leof EB. TGF-beta signaling: a tale of two responses. J Cell Biochem 2007, 102:593-608. 10.1002/jcb.21501, 17729308.
6. Datto MB, Frederick JP, Pan L, Borton AJ, Zhuang Y, Wang XF. Targeted disruption of Smad3 reveals an essential role in transforming growth factor beta-mediated signal transduction. Mol Cell Biol 1999, 19:2495-2504. 84042, 10082515.
7. Shi Y, Massague J. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 2003, 113:685-700. 10.1016/S0092-8674(03)00432-X, 12809600.
8. Massague J, Seoane J, Wotton D. Smad transcription factors. Genes Dev 2005, 19:2783-2810. 10.1101/gad.1350705, 16322555.
9. Feng XH, Derynck R. Specificity and versatility in tgf-beta signaling through smads. Annu Rev Cell Dev Biol 2005, 21:659-693. 10.1146/annurev.cellbio.21.022404.142018, 16212511.
10. Mehra A, Wrana JL. TGF-beta and the smad signal transduction pathway. Biochem Cell Biol 2002, 80:605-622. 10.1139/o02-161, 12440701.
11. Nakao A, Imamura T, Souchelnytskyi S, Kawabata M, Ishisaki A, Oeda E, Tamaki K, Hanai J, Heldin CH, Miyazono K, Ten Dijke P. TGF-beta receptor-mediated signalling through Smad2, Smad3 and Smad4. EMBO J 1997, 16:5353-5362. 10.1093/emboj/16.17.5353, 1170167, 9311995.
12. Jakowlew SB. Transforming growth factor-beta in cancer and metastasis. Cancer Metastasis Rev 2006, 25:435-457. 10.1007/s10555-006-9006-2, 16951986.
13. Pardali K, Moustakas A. Actions of TGF-beta as tumor suppressor and pro-metastatic factor in human cancer. Biochim Biophys Acta 2007, 1775:21-62.
14. Levy L, Hill CS. Alterations in components of the TGF-beta superfamily signaling pathways in human cancer. Cytokine Growth Factor Rev 2006, 17:41-58. 10.1016/j.cytogfr.2005.09.009, 16310402.
15. Maliekal TT, Antony ML, Nair A, Paulmurugan R, Karunagaran D. Loss of expression, and mutations of smad 2 and smad 4 in human cervical cancer. Oncogene 2003, 22:4889-4897. 10.1038/sj.onc.1206806, 12894231.
16. Pirisi L, Creek KE, Doniger J, DiPaolo JA. Continuous cell lines with altered growth and differentiation properties originate after transfection of human keratinocytes with human papillomavirus type 16 DNA. Carcinogenesis 1988, 9:1573-1579. 10.1093/carcin/9.9.1573, 2457456.
17. Creek KE, Jenkins GR, Khan MA, Batova A, Hodam JR, Tolleson WH, Pirisi L. Retinoic acid suppresses human papillomavirus type 16 (HPV16)-mediated transformation of human keratinocytes and inhibits the expression of the HPV16 oncogenes. Adv Exp Med Biol 1994, 354:19-35.
18. Creek KE, Geslani G, Batova A, Pirisi L. Progressive loss of sensitivity to growth control by retinoic acid and transforming growth factor-beta at late stages of human papillomavirus type 16-initiated transformation of human keratinocytes. Adv Exp Med Biol 1995, 375:117-135.
19. DiPaolo JA, Woodworth CD, Popescu NC, Notario V, Doniger J. Induction of human cervical squamous cell carcinoma by sequential transfection with human papillomavirus 16 DNA and viral Harvey ras. Oncogene 1989, 4:395-399.
20. DiPaolo JA, Woodworth CD, Popescu NC, Koval DL, Lopez JV, Doniger J. HSV-2-induced tumorigenicity in HPV16-immortalized human genital keratinocytes. Virology 1990, 177:777-779. 10.1016/0042-6822(90)90548-6, 2164733.
21. Borger DR, Mi Y, Geslani G, Zyzak LL, Batova A, Engin TS, Pirisi L, Creek KE. Retinoic acid resistance at late stages of human papillomavirus type 16-mediated transformation of human keratinocytes arises despite intact retinoid signaling and is due to a loss of sensitivity to transforming growth factor-beta. Virology 2000, 270:397-407. 10.1006/viro.2000.0282, 10792999.
22. Braun L, Durst M, Mikumo R, Gruppuso P. Differential response of nontumorigenic and tumorigenic human papillomavirus type 16-positive epithelial cells to transforming growth factor beta 1. Cancer Res 1990, 50:7324-7332.
23. Hasskarl J, Butz K, Whitaker N, Ullmann A, Durst M, Hoppe-Seyler F. Differential cell cycle response of nontumorigenic and tumorigenic human papillomavirus-positive keratinocytes towards transforming growth factor-beta1. J Mol Med 2000, 78:94-101. 10.1007/s001090000083, 10794545.
24. Mi Y, Borger DR, Fernandes PR, Pirisi L, Creek KE. Loss of transforming growth factor-beta (TGF-beta) receptor type I mediates TGF-beta resistance in human papillomavirus type 16-transformed human keratinocytes at late stages of in vitro progression. Virology 2000, 270:408-416. 10.1006/viro.2000.0283, 10793000.
25. Hypes MK, Pirisi L, Creek KE. Mechanisms of decreased expression of transforming growth factor-beta receptor type I at late stages of HPV16-mediated transformation. Cancer Lett 2009, 282:177-186. 10.1016/j.canlet.2009.03.014, 2710415, 19344999.
26. Pirisi L, Yasumoto S, Feller M, Doniger J, DiPaolo JA. Transformation of human fibroblasts and keratinocytes with human papillomavirus type 16 DNA. J Virol 1987, 61:1061-1066. 254063, 2434663.
27. Souchelnytskyi S, Tamaki K, Engstrom U, Wernstedt C, Ten Dijke P, Heldin CH. Phosphorylation of Ser465 and Ser467 in the C terminus of Smad2 mediates interaction with Smad4 and is required for transforming growth factor-beta signaling. J Biol Chem 1997, 272:28107-28115. 10.1074/jbc.272.44.28107, 9346966.
28. Schneider CA, Rasband WS, Eliceiri KW. NIH image to ImageJ: 25 years of image analysis. Nat Methods 2012, 9:671-675. 10.1038/nmeth.2089, 22930834.
29. Ki KD, Tong SY, Huh CY, Lee JM, Lee SK, Chi SG. Expression and mutational analysis of TGF-beta/smads signaling in human cervical cancers. J Gynecol Oncol 2009, 20:117-121. 10.3802/jgo.2009.20.2.117, 2704993, 19590724.
30. Kloth JN, Kenter GG, Spijker HS, Uljee S, Corver WE, Jordanova ES, Fleuren GJ, Gorter A. Expression of Smad2 and Smad4 in cervical cancer: absent nuclear Smad4 expression correlates with poor survival. Mod Pathol 2008, 21:866-875. 10.1038/modpathol.2008.62, 18425078.
31. Ku JL, Park SH, Yoon KA, Shin YK, Kim KH, Choi JS, Kang HC, Kim IJ, Han IO, Park JG. Genetic alterations of the TGF-beta signaling pathway in colorectal cancer cell lines: a novel mutation in Smad3 associated with the inactivation of TGF-beta-induced transcriptional activation. Cancer Lett 2007, 247:283-292. 10.1016/j.canlet.2006.05.008, 16828225.
32. Wolfraim LA, Fernandez TM, Mamura M, Fuller WL, Kumar R, Cole DE, Byfield S, Felici A, Flanders KC, Walz TM, et al. Loss of Smad3 in acute T-cell lymphoblastic leukemia. N Engl J Med 2004, 351:552-559. 10.1056/NEJMoa031197, 15295048.
33. Sodir NM, Chen X, Park R, Nickel AE, Conti PS, Moats R, Bading JR, Shibata D, Laird PW. Smad3 deficiency promotes tumorigenesis in the distal colon of ApcMin/+ mice. Cancer Res 2006, 66:8430-8438. 10.1158/0008-5472.CAN-06-1437, 16951153.
34. Maggio-Price L, Treuting P, Zeng W, Tsang M, Bielefeldt-Ohmann H, Iritani BM. Helicobacter infection is required for inflammation and colon cancer in SMAD3-deficient mice. Cancer Res 2006, 66:828-838. 10.1158/0008-5472.CAN-05-2448, 16424015.
35. Yang YA, Zhang GM, Feigenbaum L, Zhang YE. Smad3 reduces susceptibility to hepatocarcinoma by sensitizing hepatocytes to apoptosis through downregulation of Bcl-2. Cancer Cell 2006, 9:445-457. 10.1016/j.ccr.2006.04.025, 2708973, 16766264.
36. Hahn SA, Schutte M, Hoque AT, Moskaluk CA, Da Costa LT, Rozenblum E, Weinstein CL, Fischer A, Yeo CJ, Hruban RH, Kern SE. DPC4, a candidate tumor suppressor gene at human chromosome 18q21.1. Science 1996, 271:350-353. 10.1126/science.271.5247.350, 8553070.
37. Lee S, Cho YS, Shim C, Kim J, Choi J, Oh S, Zhang W, Lee J. Aberrant expression of Smad4 results in resistance against the growth-inhibitory effect of transforming growth factor-beta in the SiHa human cervical carcinoma cell line. Int J Cancer 2001, 94:500-507. 10.1002/ijc.1494, 11745435.
38. Kleeff J, Ishiwata T, Maruyama H, Friess H, Truong P, Buchler MW, Falb D, Korc M. The TGF-beta signaling inhibitor Smad7 enhances tumorigenicity in pancreatic cancer. Oncogene 1999, 18:5363-5372. 10.1038/sj.onc.1202909, 10498890.
39. Liu X, Lee J, Cooley M, Bhogte E, Hartley S, Glick A. Smad7 but not Smad6 cooperates with oncogenic ras to cause malignant conversion in a mouse model for squamous cell carcinoma. Cancer Res 2003, 63:7760-7768.
40. Wu RY, Zhang Y, Feng XH, Derynck R. Heteromeric and homomeric interactions correlate with signaling activity and functional cooperativity of Smad3 and Smad4/DPC4. Mol Cell Biol 1997, 17:2521-2528. 232101, 9111321.
41. Inman GJ, Nicolas FJ, Hill CS. Nucleocytoplasmic shuttling of smads 2, 3, and 4 permits sensing of TGF-beta receptor activity. Mol Cell 2002, 10:283-294. 10.1016/S1097-2765(02)00585-3, 12191474.
42. Nicolas FJ, Hill CS. Attenuation of the TGF-beta-smad signaling pathway in pancreatic tumor cells confers resistance to TGF-beta-induced growth arrest. Oncogene 2003, 22:3698-3711. 10.1038/sj.onc.1206420, 12802277.
43. Dai JL, Turnacioglu KK, Schutte M, Sugar AY, Kern SE. Dpc4 transcriptional activation and dysfunction in cancer cells. Cancer Res 1998, 58:4592-4597.
44. Wan F, Miao X, Quraishi I, Kennedy V, Creek KE, Pirisi-Creek L. Gene expression changes during HPV-mediated carcinogenesis: a comparison between an in vitro cell model and cervical cancer. Int J Cancer 2008, 123:32-40. 10.1002/ijc.23463, 2872618, 18398830.