Prognostic Impact of Jab1, p16, p21, p62, Ki67 and Skp2 in Soft Tissue Sarcomas

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Sorbye, Sveinung W ^a,b   Kilvaer, Thomas K ^b   Valkov, Andrej ^a,b   Donnem, Tom ^a,b   Smeland, Eivind ^a   Al Shibli, Khalid ^b,c   Bremnes, Roy M ^a,b   Busund, Lill Tove ^a,b  

^a UNIVERSITY HOSPITAL OF NORTH NORWAY   (Norway)

^b UNIVERSITY OF TROMSØ   (Norway)

^c NORDLAND HOSPITAL   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; BINDING PROTEIN; JAB1 PROTEIN; KI 67 ANTIGEN; PROTEIN P16; PROTEIN P21; PROTEIN P62; S PHASE KINASE ASSOCIATED PROTEIN 2; UNCLASSIFIED DRUG;

ADULT; AGED; ARTICLE; CANCER CHEMOTHERAPY; CANCER GRADING; CANCER PROGNOSIS; CANCER RADIOTHERAPY; CANCER SIZE; CANCER SURGERY; CANCER TISSUE; CONTROLLED STUDY; DISEASE SPECIFIC SURVIVAL; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MALE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; SEX DIFFERENCE; SOFT TISSUE SARCOMA; SURVIVAL TIME; TISSUE MICROARRAY;

ADOLESCENT; ADULT; AGED; CHILD, PRESCHOOL; CYCLIN-DEPENDENT KINASE INHIBITOR P16; CYCLIN-DEPENDENT KINASE INHIBITOR P21; FEMALE; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; KI-67 ANTIGEN; MALE; MIDDLE AGED; PEPTIDE HYDROLASES; PROGNOSIS; RNA-BINDING PROTEINS; S-PHASE KINASE-ASSOCIATED PROTEINS; SARCOMA; TISSUE ARRAY ANALYSIS; TUMOR MARKERS, BIOLOGICAL; YOUNG ADULT;

EID: 84867158968     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0047068     Document Type: Article

References (64)

1. Alamanda VK, Crosby SN, Archer KR, Song Y, Schwartz HS, et al. (2012) Primary excision compared with re-excision of extremity soft tissue sarcomas-is anything new? J Surg Oncol 105: 662-667. 10.1002/jso.23021 [doi].
2. Grobmyer SR, Maki RG, Demetri GD, Mazumdar M, Riedel E, et al. (2004) Neo-adjuvant chemotherapy for primary high-grade extremity soft tissue sarcoma. Ann Oncol 15: 1667-1672. 15/11/1667 [pii];10.1093/annonc/mdh431 [doi].
3. Dickinson IC, Whitwell DJ, Battistuta D, Thompson B, Strobel N, et al. (2006) Surgical margin and its influence on survival in soft tissue sarcoma. ANZ J Surg 76: 104-109.
4. Kiatisevi P, Asavamongkolkul A, Phimolsarnti R, Waikakul S, Benjarassamerote S, (2006) The outcomes and prognostic factors of patients with soft-tissue sarcoma. J Med Assoc Thai 89: 334-342.
5. Koea JB, Leung D, Lewis JJ, Brennan MF, (2003) Histopathologic type: an independent prognostic factor in primary soft tissue sarcoma of the extremity? Ann Surg Oncol 10: 432-440.
6. Mendenhall WM, Zlotecki RA, Hochwald SN, Hemming AW, Grobmyer SR, et al. (2005) Retroperitoneal soft tissue sarcoma. Cancer 104: 669-675.
7. Raney RB Jr, Crist WM, Maurer HM, Foulkes MA, (1983) Prognosis of children with soft tissue sarcoma who relapse after achieving a complete response. A report from the Intergroup Rhabdomyosarcoma Study I. Cancer 52: 44-50.
8. Yang RS, Lane JM, Eilber FR, Dorey FJ, al Shaikh R, et al. (1995) High grade soft tissue sarcoma of the flexor fossae. Size rather than compartmental status determine prognosis. Cancer 76: 1398-1405.
9. Zagars GK, Ballo MT, Pisters PW, Pollock RE, Patel SR, et al. (2003) Prognostic factors for disease-specific survival after first relapse of soft-tissue sarcoma: analysis of 402 patients with disease relapse after initial conservative surgery and radiotherapy. Int J Radiat Oncol Biol Phys 57: 739-747.
10. Claret FX, Hibi M, Dhut S, Toda T, Karin M (1996) A new group of conserved coactivators that increase the specificity of AP-1 transcription factors. Nature 383: 453-457. 10.1038/383453a0 [doi].
11. Ahn J, Hong SA, Lee SE, Kim J, Oh YS, et al. (2009) Cytoplasmic localization of Jab1 and p27 Kip1 might be associated with invasiveness of papillary thyroid carcinoma. Endocr J 56: 707-713. JST.JSTAGE/endocrj/K08E-372 [pii].
12. Tomoda K, Kubota Y, Kato J (1999) Degradation of the cyclin-dependent-kinase inhibitor p27Kip1 is instigated by Jab1. Nature 398: 160-165. 10.1038/18230 [doi].
13. Tomoda K, Kubota Y, Arata Y, Mori S, Maeda M, et al. (2002) The cytoplasmic shuttling and subsequent degradation of p27Kip1 mediated by Jab1/CSN5 and the COP9 signalosome complex. J Biol Chem 277: 2302-2310. 10.1074/jbc.M104431200 [doi];M104431200 [pii].
14. Esteva FJ, Sahin AA, Rassidakis GZ, Yuan LX, Smith TL, et al. (2003) Jun activation domain binding protein 1 expression is associated with low p27(Kip1)levels in node-negative breast cancer. Clin Cancer Res 9: 5652-5659.
15. Goto A, Niki T, Moriyama S, Funata N, Moriyama H, et al. (2004) Immunohistochemical study of Skp2 and Jab1, two key molecules in the degradation of P27, in lung adenocarcinoma. Pathol Int 54: 675-681. 10.1111/j.1440-1827.2004.01679.x [doi];PIN1679 [pii].
16. Korbonits M, Chahal HS, Kaltsas G, Jordan S, Urmanova Y, et al. (2002) Expression of phosphorylated p27(Kip1) protein and Jun activation domain-binding protein 1 in human pituitary tumors. J Clin Endocrinol Metab 87: 2635-2643.
17. Li W, Sanki A, Karim RZ, Thompson JF, Soon LC, et al. (2006) The role of cell cycle regulatory proteins in the pathogenesis of melanoma. Pathology 38: 287-301. U0L232825J282126 [pii];10.1080/00313020600817951 [doi].
18. Kamb A, Gruis NA, Weaver-Feldhaus J, Liu Q, Harshman K, et al. (1994) A cell cycle regulator potentially involved in genesis of many tumor types. Science 264: 436-440.
19. Caldas C, Hahn SA, da Costa LT, Redston MS, Schutte M, et al. (1994) Frequent somatic mutations and homozygous deletions of the p16 (MTS1) gene in pancreatic adenocarcinoma. Nat Genet 8: 27-32. 10.1038/ng0994-27 [doi].
20. Kim YT, Cho NH, Park SW, Kim JW (1998) Underexpression of cyclin-dependent kinase (CDK) inhibitors in cervical carcinoma. Gynecol Oncol 71: 38-45. S0090-8258(98)95134-4 [pii];10.1006/gyno.1998.5134 [doi].
21. Mori T, Miura K, Aoki T, Nishihira T, Mori S, et al. (1994) Frequent somatic mutation of the MTS1/CDK4I (multiple tumor suppressor/cyclin-dependent kinase 4 inhibitor) gene in esophageal squamous cell carcinoma. Cancer Res 54: 3396-3397.
22. Rocco JW, Sidransky D (2001) p16(MTS-1/CDKN2/INK4a) in cancer progression. Exp Cell Res 264: 42-55. 10.1006/excr.2000.5149 [doi];S0014-4827(00)95149-8 [pii].
23. van de Putte G, Holm R, Lie AK, Trope CG, Kristensen GB (2003) Expression of p27, p21, and p16 protein in early squamous cervical cancer and its relation to prognosis. Gynecol Oncol 89: 140-147. S0090825803000106 [pii].
24. Naini S, Etheridge KT, Adam SJ, Qualman SJ, Bentley RC, et al. (2008) Defining the cooperative genetic changes that temporally drive alveolar rhabdomyosarcoma. Cancer Res 68: 9583-9588. 68/23/9583 [pii];10.1158/0008-5472.CAN-07-6178 [doi].
25. Nishijo K, Chen QR, Zhang L, McCleish AT, Rodriguez A, et al. (2009) Credentialing a preclinical mouse model of alveolar rhabdomyosarcoma. Cancer Res 69: 2902-2911. 69/7/2902 [pii];10.1158/0008-5472.CAN-08-3723 [doi].
26. Dotto GP (2000) p21(WAF1/Cip1): more than a break to the cell cycle? Biochim Biophys Acta 1471: M43-M56. S0304-419X(00)00019-6 [pii].
27. Brown DC, Gatter KC, (1990) Monoclonal antibody Ki-67: its use in histopathology. Histopathology 17: 489-503.
28. Moscat J, Diaz-Meco MT, Wooten MW (2007) Signal integration and diversification through the p62 scaffold protein. Trends Biochem Sci 32: 95-100. S0968-0004(06)00327-6 [pii];10.1016/j.tibs.2006.12.002 [doi].
29. Duran A, Serrano M, Leitges M, Flores JM, Picard S, et al. (2004) The atypical PKC-interacting protein p62 is an important mediator of RANK-activated osteoclastogenesis. Dev Cell 6: 303-309. S1534580703004039 [pii].
30. Moscat J, Diaz-Meco MT, Albert A, Campuzano S (2006) Cell signaling and function organized by PB1 domain interactions. Mol Cell 23: 631-640. S1097-2765(06)00537-5 [pii];10.1016/j.molcel.2006.08.002 [doi].
31. Rodriguez A, Duran A, Selloum M, Champy MF, Diez-Guerra FJ, et al. (2006) Mature-onset obesity and insulin resistance in mice deficient in the signaling adapter p62. Cell Metab 3: 211-222. S1550-4131(06)00035-0 [pii];10.1016/j.cmet.2006.01.011 [doi].
32. Wang G, Chan CH, Gao Y, Lin HK (2011) Novel roles of Skp2 E3 ligase in cellular senescence, cancer progression, and metastasis. Chin J Cancer. cjc.011.10319 [pii];10.5732/cjc.011.10319 [doi].
33. Nocito A, Kononen J, Kallioniemi OP, Sauter G, (2001) Tissue microarrays (TMAs) for high-throughput molecular pathology research. Int J Cancer 94: 1-5.
34. Kallioniemi OP, Wagner U, Kononen J, Sauter G, (2001) Tissue microarray technology for high-throughput molecular profiling of cancer. Hum Mol Genet 10: 657-662.
35. Tsuchida R, Miyauchi J, Shen L, Takagi M, Tsunematsu Y, et al. (2002) Expression of cyclin-dependent kinase inhibitor p27/Kip1 and AP-1 coactivator p38/Jab1 correlates with differentiation of embryonal rhabdomyosarcoma. Jpn J Cancer Res 93: 1000-1006.
36. von Levetzow C, Jiang X, Gwye Y, von Levetzow G, Hung L, et al. (2011) Modeling initiation of Ewing sarcoma in human neural crest cells. PLoS One 6: e19305. 10.1371/journal.pone.0019305 [doi];PONE-D-11-01315 [pii].
37. Thway K, Flora R, Shah C, Olmos D, Fisher C (2012) Diagnostic utility of p16, CDK4, and MDM2 as an immunohistochemical panel in distinguishing well-differentiated and dedifferentiated liposarcomas from other adipocytic tumors. Am J Surg Pathol 36: 462-469. 10.1097/PAS.0b013e3182417330 [doi].
38. Hakverdi S, Gungoren A, Yaldiz M, Hakverdi AU, Toprak S, (2011) Immunohistochemical analysis of p16 expression in uterine smooth muscle tumors. Eur J Gynaecol Oncol 32: 513-515.
39. Karim RZ, Gerega SK, Yang YH, Spillane A, Carmalt H, et al. (2010) p16 and pRb immunohistochemical expression increases with increasing tumour grade in mammary phyllodes tumours. Histopathology 56: 868-875.
40. Maitra A, Roberts H, Weinberg AG, Geradts J (2001) AID-IJC1006>3.0.CO;2-V [pii].
41. Endo M, Kobayashi C, Setsu N, Takahashi Y, Kohashi K, et al. (2011) Prognostic significance of p14ARF, p15INK4b, and p16INK4a inactivation in malignant peripheral nerve sheath tumors. Clin Cancer Res 17: 3771-3782. 1078-0432.CCR-10-2393 [pii];10.1158/1078-0432.CCR-10-2393 [doi].
42. Bodner-Adler B, Bodner K, Czerwenka K, Kimberger O, Leodolter S, et al. (2005) Expression of p16 protein in patients with uterine smooth muscle tumors: an immunohistochemical analysis. Gynecol Oncol 96: 62-66. S0090-8258(04)00742-5 [pii];10.1016/j.ygyno.2004.09.026 [doi].
43. D'Angelo E, Espinosa I, Ali R, Gilks CB, Rijn M, et al. (2011) Uterine leiomyosarcomas: tumor size, mitotic index, and biomarkers Ki67, and Bcl-2 identify two groups with different prognosis. Gynecol Oncol 121: 328-333. S0090-8258(11)00065-5 [pii];10.1016/j.ygyno.2011.01.022 [doi].
44. Shim BY, Yoo J, Lee YS, Hong YS, Kim HK, et al. (2010) Prognostic role of Rb, p16, Cyclin D1 proteins in soft tissue sarcomas. Cancer Res Treat 42: 144-150. 10.4143/crt.2010.42.3.144 [doi].
45. Young NP, Crowley D, Jacks T (2011) Uncoupling cancer mutations reveals critical timing of p53 loss in sarcomagenesis. Cancer Res 71: 4040-4047. 0008-5472.CAN-10-4563 [pii];10.1158/0008-5472.CAN-10-4563 [doi].
46. Sabah M, Cummins R, Leader M, Kay E, (2007) Immunoreactivity of p53, Mdm2, p21(WAF1/CIP1) Bcl-2, and Bax in soft tissue sarcomas: correlation with histologic grade. Appl Immunohistochem Mol Morphol 15: 64-69.
47. Lopez-Guerrero JA, Machado I, Scotlandi K, Noguera R, Pellin A, et al. (2011) Clinicopathological significance of cell cycle regulation markers in a large series of genetically confirmed Ewing's sarcoma family of tumors. Int J Cancer 128: 1139-1150.
48. Leiser AL, Anderson SE, Nonaka D, Chuai S, Olshen AB, et al. (2006) Apoptotic and cell cycle regulatory markers in uterine leiomyosarcoma. Gynecol Oncol 101: 86-91. S0090-8258(05)00846-2 [pii];10.1016/j.ygyno.2005.09.055 [doi].
49. Rolland P, Madjd Z, Durrant L, Ellis IO, Layfield R, et al. (2007) The ubiquitin-binding protein p62 is expressed in breast cancers showing features of aggressive disease. Endocr Relat Cancer 14: 73-80. 14/1/73 [pii];10.1677/erc.1.01312 [doi].
50. Inoue D, Suzuki T, Mitsuishi Y, Miki Y, Suzuki S, et al. (2012) Accumulation of p62/SQSTM1 is associated with poor prognosis in patients with lung adenocarcinoma. Cancer Sci. 10.1111/j.1349-7006.2012.02216.x [doi].
51. Kitamura H, Torigoe T, Asanuma H, Hisasue SI, Suzuki K, et al. (2006) Cytosolic overexpression of p62 sequestosome 1 in neoplastic prostate tissue. Histopathology 48: 157-161. HIS2313 [pii];10.1111/j.1365-2559.2005.02313.x [doi].
52. Matsumoto K, Yamamoto J, Miura T, (1993) Lack of prognostic value of immunoreactivity for p62 oncoprotein in colorectal carcinoma. Int J Colorectal Dis 8: 103-105.
53. Huang HY, Kang HY, Li CF, Eng HL, Chou SC, et al. (2006) Skp2 overexpression is highly representative of intrinsic biological aggressiveness and independently associated with poor prognosis in primary localized myxofibrosarcomas. Clin Cancer Res 12: 487-498. 12/2/487 [pii];10.1158/1078-0432.CCR-05-1497 [doi].
54. Huang HY, Huang WW, Wu JM, Huang CK, Wang JW, et al. (2008) Flow cytometric analysis of DNA ploidy and S-phase fraction in primary localized myxofibrosarcoma: correlations with clinicopathological factors, Skp2 expression, and patient survival. Ann Surg Oncol 15: 2239-2249. 10.1245/s10434-008-9968-0 [doi].
55. Di VD, Demichelis F, Simonetti S, Pettinato G, Terracciano L, et al. (2008) Skp2 expression is associated with high risk and elevated Ki67 expression in gastrointestinal stromal tumours. BMC Cancer 8: 134. 1471-2407-8-134 [pii];10.1186/1471-2407-8-134 [doi].
56. Oliveira AM, Okuno SH, Nascimento AG, Lloyd RV, (2003) Skp2 protein expression in soft tissue sarcomas. J Clin Oncol 21: 722-727.
57. Valkov A, Sorbye S, Kilvaer TK, Donnem T, Smeland E, et al. (2011) Estrogen receptor and progesterone receptor are prognostic factors in soft tissue sarcomas. Int J Oncol 38: 1031-1040. 10.3892/ijo.2011.920 [doi].
58. Valkov A, Kilvaer TK, Sorbye SW, Donnem T, Smeland E, et al. (2011) The prognostic impact of Akt isoforms, PI3K and PTEN related to female steroid hormone receptors in soft tissue sarcomas. J Transl Med 9: 200. 1479-5876-9-200 [pii];10.1186/1479-5876-9-200 [doi].
59. Davidovich S, Ben-Izhak O, Shapira M, Futerman B, Hershko DD (2008) Over-expression of Skp2 is associated with resistance to preoperative doxorubicin-based chemotherapy in primary breast cancer. Breast Cancer Res 10: R63. bcr2122 [pii];10.1186/bcr2122 [doi].
60. Bhatt S, Xiao Z, Meng Z, Katzenellenbogen BS (2012) Phosphorylation by p38 mitogen-activated protein kinase promotes estrogen receptor alpha turnover and functional activity via the SCF(Skp2) proteasomal complex. Mol Cell Biol 32: 1928-1943. MCB.06561-11 [pii];10.1128/MCB.06561-11 [doi].
61. Umanskaya K, Radke S, Chander H, Monardo R, Xu X, et al. (2007) Skp2B stimulates mammary gland development by inhibiting REA, the repressor of the estrogen receptor. Mol Cell Biol 27: 7615-7622. MCB.01239-07 [pii];10.1128/MCB.01239-07 [doi].
62. Wang J, Han F, Wu J, Lee SW, Chan CH, et al. (2011) The role of Skp2 in hematopoietic stem cell quiescence, pool size, and self-renewal. Blood 118: 5429-5438. blood-2010-10-312785 [pii];10.1182/blood-2010-10-312785 [doi].
63. Wang Z, Gao D, Fukushima H, Inuzuka H, Liu P, et al. (2012) Skp2: a novel potential therapeutic target for prostate cancer. Biochim Biophys Acta 1825: 11-17. S0304-419X(11)00046-1 [pii];10.1016/j.bbcan.2011.09.002 [doi].
64. Wang Z, Fukushima H, Inuzuka H, Wan L, Liu P, et al. (2012) Skp2 is a promising therapeutic target in breast cancer. Front Oncol 1. 10.3389/fonc.2011.00057 [doi].