Co-expression of CD147 and GLUT-1 indicates radiation resistance and poor prognosis in cervical squamous cell carcinoma

International Journal of Clinical and Experimental Pathology

Volumn 7, Issue 4, 2014, Pages 1651-1666

  Huang, Xin Qiong ^a   Chen, Xiang ^a   Xie, Xiao Xue ^b   Zhou, Qin ^a   Li, Kai ^a   Li, Shan ^a   Shen, Liang Fang ^a   Su, Juan ^a  

^a CENTRAL SOUTH UNIVERSITY   (China)

^b HUNAN CANCER HOSPITAL   (China)

Author keywords

CD147; Cervical carcinoma; GLUT 1; Glycolysis; Immunohistochemistry; Radiation resistance

Indexed keywords

BSG PROTEIN, HUMAN; CD147 ANTIGEN; GLUCOSE TRANSPORTER 1; TUMOR MARKER;

ADULT; AGED; CARCINOMA, SQUAMOUS CELL; COHORT ANALYSIS; DISEASE FREE SURVIVAL; FEMALE; FOLLOW UP; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; MIDDLE AGED; MORTALITY; PROGNOSIS; RETROSPECTIVE STUDY; TREATMENT FAILURE; UTERINE CERVICAL NEOPLASMS; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; ANTIGENS, CD147; CARCINOMA, SQUAMOUS CELL; COHORT STUDIES; DISEASE-FREE SURVIVAL; FEMALE; FOLLOW-UP STUDIES; GENE EXPRESSION REGULATION, NEOPLASTIC; GLUCOSE TRANSPORTER TYPE 1; HUMANS; MIDDLE AGED; PROGNOSIS; RETROSPECTIVE STUDIES; TREATMENT FAILURE; TUMOR MARKERS, BIOLOGICAL; UTERINE CERVICAL NEOPLASMS;

EID: 84899553451     PISSN: None     EISSN: 19362625     Source Type: Journal    
DOI: None     Document Type: Article

References (85)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E and Forman D. Global cancer statistics. CA Cancer J Clin 2011; 61: 69-90.
2. Keys HM, Bundy BN, Stehman FB, Muderspach LI, Chafe WE, Suggs CL 3rd, Walker JL and Gersell D. Cisplatin, radiation, and adjuvant hysterectomy compared with radiation and adjuvant hysterectomy for bulky stage IB cervical carcinoma. N Engl J Med 1999; 340: 1154-1161.
3. Morris M, Eifel PJ, Lu J, Grigsby PW, Levenback C, Stevens RE, Rotman M, Gershenson DM and Mutch DG. Pelvic radiation with concurrent chemotherapy compared with pelvic and para-aortic radiation for high-risk cervical cancer. N Engl J Med 1999; 340: 1137-1143.
4. Rose PG, Bundy BN, Watkins EB, Thigpen JT, Deppe G, Maiman MA, Clarke-Pearson DL and Insalaco S. Concurrent cisplatin-based radio-therapy and chemotherapy for locally advanced cervical cancer. N Engl J Med 1999; 340: 1144-1153.
5. Kim TJ, Lee JW, Song SY, Choi JJ, Choi CH, Kim BG, Lee JH and Bae DS. Increased expression of pAKT is associated with radiation resistance in cervical cancer. Br J Cancer 2006; 94: 1678-1682.
6. Karar J and Maity A. Modulating the tumor microenvironment to increase radiation res-ponsiveness. Cancer Biol Ther 2009; 8: 1994-2001.
7. Wouters A, Pauwels B, Lardon F and Vermorken JB. Review: implications of in vitro research on the effect of radiotherapy and chemotherapy under hypoxic conditions. Oncologist 2007; 12: 690-712.
8. Rockwell S, Dobrucki IT, Kim EY, Marrison ST and Vu VT. Hypoxia and radiation therapy: past history, ongoing research, and future promise. Curr Mol Med 2009; 9: 442-458.
9. Sheehan JP, Shaffrey ME, Gupta B, Larner J, Rich JN and Park DM. Improving the radiosen-sitivity of radioresistant and hypoxic glioblas-toma. Future Oncol 2010; 6: 1591-1601.
10. Cohen-Jonathan Moyal E. [Angiogenic inhibi-tors and radiotherapy: from the concept to the clinical trial]. Cancer Radiother 2009; 13: 562-567.
11. Dewhirst MW, Cao Y and Moeller B. Cycling hypoxia and free radicals regulate angiogenesis and radiotherapy response. Nat Rev Cancer 2008; 8: 425-437.
12. Shimura T, Kakuda S, Ochiai Y, Nakagawa H, Kuwahara Y, Takai Y, Kobayashi J, Komatsu K and Fukumoto M. Acquired radioresistance of human tumor cells by DNA-PK/AKT/GSK3beta-mediated cyclin D1 overexpression. Oncogene 2010; 29: 4826-4837.
13. Ozeki M, Tamae D, Hou DX, Wang T, Lebon T, Spitz DR and Li JJ. Response of cyclin B1 to ionizing radiation: regulation by NF-kappaB and mitochondrial antioxidant enzyme MnSOD. Anticancer Res 2004; 24: 2657-2663.
14. He J, Li J, Ye C, Zhou L, Zhu J, Wang J, Mizota A, Furusawa Y and Zhou G. Cell cycle suspension: a novel process lurking in G(2) arrest. Cell Cycle 2011; 10: 1468-1476.
15. Parliament MB and Murray D. Single nucleotide polymorphisms of DNA repair genes as predic-tors of radioresponse. Semin Radiat Oncol 2010; 20: 232-240.
16. Smith J, Tho LM, Xu N and Gillespie DA. The ATM-Chk2 and ATR-Chk1 pathways in DNA damage signaling and cancer. Adv Cancer Res 2010; 108: 73-112.
17. Bolderson E, Richard DJ, Zhou BB and Khanna KK. Recent advances in cancer therapy tar-geting proteins involved in DNA double-strand break repair. Clin Cancer Res 2009; 15: 6314-6320.
18. Zhang L, Yang M, Bi N, Fang M, Sun T, Ji W, Tan W, Zhao L, Yu D, Lin D and Wang L. ATM polymorphisms are associated with risk of radiation-induced pneumonitis. Int J Radiat Oncol Biol Phys 2010; 77: 1360-1368.
19. Beskow C, Skikuniene J, Holgersson A, Nilsson B, Lewensohn R, Kanter L and Viktorsson K. Radioresistant cervical cancer shows upregu-lation of the NHEJ proteins DNA-PKcs, Ku70 and Ku86. Br J Cancer 2009; 101: 816-821.
20. Peltonen JK, Vahakangas KH, Helppi HM, Bloigu R, Paakko P and Turpeenniemi-Hujanen T. Specific TP53 mutations predict aggressive phenotype in head and neck squamous cell carcinoma: a retrospective archival study. Head Neck Oncol 2011; 3: 20.
21. Lehmann BD, McCubrey JA, Jefferson HS, Paine MS, Chappell WH and Terrian DM. A dominant role for p53-dependent cellular senescence in radiosensitization of human prostate cancer cells. Cell Cycle 2007; 6: 595-605.
22. Suzuki Y, Oka K, Yoshida D, Shirai K, Ohno T, Kato S, Tsujii H and Nakano T. Correlation between survivin expression and locoregional control in cervical squamous cell carcinomas treated with radiation therapy. Gynecol Oncol 2007; 104: 642-646.
23. Chu X, Chen L, Wang J, Guan X, Geng H, Zhang Q and Song H. SiRNA-mediated survivin inhibition enhances chemo-or radiosensivity of colorectal cancer cells in tumor-bearing nude mice. Hepatogastroenterology 2010; 57: 1445-1452.
24. Li HF, Kim JS and Waldman T. Radiation-induced Akt activation modulates radioresis-tance in human glioblastoma cells. Radiat Oncol 2009; 4: 43.
25. Mukherjee B, McEllin B, Camacho CV, Tomi-matsu N, Sirasanagandala S, Nannepaga S, Hatanpaa KJ, Mickey B, Madden C, Maher E, Boothman DA, Furnari F, Cavenee WK, Bachoo RM and Burma S. EGFRvIII and DNA double-strand break repair: a molecular mechanism for radioresistance in glioblastoma. Cancer Res 2009; 69: 4252-4259.
26. Bergkvist GT, Argyle DJ, Pang LY, Muirhead R and Yool DA. Studies on the inhibition of feline EGFR in squamous cell carcinoma: enhance-ment of radiosensitivity and rescue of resis-tance to small molecule inhibitors. Cancer Biol Ther 2011; 11: 927-937.
27. Baumann M, Krause M and Hill R. Exploring the role of cancer stem cells in radioresistance. Nat Rev Cancer 2008; 8: 545-554.
28. Kawano T, Akiyama M, Agawa-Ohta M, Mikami-Terao Y, Iwase S, Yanagisawa T, Ida H, Agata N and Yamada H. Histone deacetylase inhibitors valproic acid and depsipeptide sensitize retinoblastoma cells to radiotherapy by increasing H2AX phosphorylation and p53 acetylation-phosphorylation. Int J Oncol 2010; 37: 787-795.
29. Kim IA, Kim IH, Kim HJ, Chie EK and Kim JS. HDAC inhibitor-mediated radiosensitization in human carcinoma cells: a general phenome-non?. J Radiat Res 2010; 51: 257-263.
30. Quennet V, Yaromina A, Zips D, Rosner A, Walenta S, Baumann M and Mueller-Klieser W. Tumor lactate content predicts for response to fractionated irradiation of human squamous cell carcinomas in nude mice. Radiother Oncol 2006; 81: 130-135.
31. Sattler UG, Meyer SS, Quennet V, Hoerner C, Knoerzer H, Fabian C, Yaromina A, Zips D, Walenta S, Baumann M and Mueller-Klieser W. Glycolytic metabolism and tumour response to fractionated irradiation. Radiother Oncol 2010; 94: 102-109.
32. Sattler UG and Mueller-Klieser W. The anti-oxidant capacity of tumour glycolysis. Int J Radiat Biol 2009; 85: 963-971.
33. Trachootham D, Alexandre J and Huang P. Targeting cancer cells by ROS-mediated me-chanisms: a radical therapeutic approach?. Nat Rev Drug Discov 2009; 8: 579-591.
34. Cook JA, Gius D, Wink DA, Krishna MC, Russo A and Mitchell JB. Oxidative stress, redox, and the tumor microenvironment. Semin Radiat Oncol 2004; 14: 259-266.
35. Levy AG, Zage PE, Akers LJ, Ghisoli ML, Chen Z, Fang W, Kannan S, Graham T, Zeng L, Franklin AR, Huang P and Zweidler-McKay PA. The combination of the novel glycolysis inhibitor 3-BrOP and rapamycin is effective against neuroblastoma. Invest New Drugs 2012; 30: 191-199.
36. Liu Y, Cao Y, Zhang W, Bergmeier S, Qian Y, Akbar H, Colvin R, Ding J, Tong L, Wu S, Hines J and Chen X. A small-molecule inhibitor of glucose transporter 1 downregulates glycoly-sis, induces cell-cycle arrest, and inhibits cancer cell growth in vitro and in vivo. Mol Cancer Ther 2012; 11: 1672-1682.
37. Bui T and Thompson CB. Cancer's sweet tooth. Cancer Cell 2006; 9: 419-420.
38. Biswas C, Zhang Y, DeCastro R, Guo H, Nakamura T, Kataoka H and Nabeshima K. The human tumor cell-derived collagenase stimulatory factor (renamed EMMPRIN) is a member of the immunoglobulin superfamily. Cancer Res 1995; 55: 434-439.
39. Marieb EA, Zoltan-Jones A, Li R, Misra S, Ghatak S, Cao J, Zucker S and Toole BP. Emmprin promotes anchorage-independent growth in human mammary carcinoma cells by stimulating hyaluronan production. Cancer Res 2004; 64: 1229-1232.
40. Iacono KT, Brown AL, Greene MI and Saouaf SJ. CD147 immunoglobulin superfamily recep-tor function and role in pathology. Exp Mol Pathol 2007; 83: 283-295.
41. Nabeshima K, Iwasaki H, Koga K, Hojo H, Suzumiya J and Kikuchi M. Emmprin (basigin/CD147): matrix metalloproteinase modulator and multifunctional cell recognition molecule that plays a critical role in cancer progression. Pathol Int 2006; 56: 359-367.
42. Li R, Huang L, Guo H and Toole BP. Basigin (murine EMMPRIN) stimulates matrix metallo-proteinase production by fibroblasts. J Cell Physiol 2001; 186: 371-379.
43. Caudroy S, Polette M, Nawrocki-Raby B, Cao J, Toole BP, Zucker S and Birembaut P. EMMPRIN-mediated MMP regulation in tumor and endo-thelial cells. Clin Exp Metastasis 2002; 19: 697-702.
44. Sun J and Hemler ME. Regulation of MMP-1 and MMP-2 production through CD147/extra-cellular matrix metalloproteinase inducer interactions. Cancer Res 2001; 61: 2276-2281.
45. Tang Y, Nakada MT, Kesavan P, McCabe F, Millar H, Rafferty P, Bugelski P and Yan L. Extracellular matrix metalloproteinase inducer stimulates tumor angiogenesis by elevating vascular endothelial cell growth factor and matrix metalloproteinases. Cancer Res 2005; 65: 3193-3199.
46. Riethdorf S, Reimers N, Assmann V, Kornfeld JW, Terracciano L, Sauter G and Pantel K. High incidence of EMMPRIN expression in human tumors. Int J Cancer 2006; 119: 1800-1810.
47. Gabison EE, Hoang-Xuan T, Mauviel A and Menashi S. EMMPRIN/CD147, an MMP modu-lator in cancer, development and tissue repair. Biochimie 2005; 87: 361-368.
48. Sier CF, Zuidwijk K, Zijlmans HJ, Hanemaaijer R, Mulder-Stapel AA, Prins FA, Dreef EJ, Kenter GG, Fleuren GJ and Gorter A. EMMPRIN-induced MMP-2 activation cascade in human cervical squamous cell carcinoma. Int J Cancer 2006; 118: 2991-2998.
49. Ju XZ, Yang JM, Zhou XY, Li ZT and Wu XH. EMMPRIN expression as a prognostic factor in radiotherapy of cervical cancer. Clin Cancer Res 2008; 14: 494-501.
50. Baba M, Inoue M, Itoh K and Nishizawa Y. Blocking CD147 induces cell death in cancer cells through impairment of glycolytic energy metabolism. Biochem Biophys Res Commun 2008; 374: 111-116.
51. Su J, Chen X and Kanekura T. A CD147-targeting siRNA inhibits the proliferation, invasiveness, and VEGF production of human malignant melanoma cells by down-regulating glycolysis. Cancer Lett 2009; 273: 140-147.
52. Kirk P, Wilson MC, Heddle C, Brown MH, Barclay AN and Halestrap AP. CD147 is tightly associated with lactate transporters MCT1 and MCT4 and facilitates their cell surface expression. EMBO J 2000; 19: 3896-3904.
53. Yoshida S, Shibata M, Yamamoto S, Hagihara M, Asai N, Takahashi M, Mizutani S, Muramatsu T and Kadomatsu K. Homo-oligomer formation by basigin, an immunoglobulin superfamily member, via its N-terminal immunoglobulin domain. Eur J Biochem 2000; 267: 4372-4380.
54. Kennedy KM and Dewhirst MW. Tumor metabolism of lactate: the influence and therapeutic potential for MCT and CD147 regulation. Future Oncol 2010; 6: 127-148.
55. Kunkel M, Moergel M, Stockinger M, Jeong JH, Fritz G, Lehr HA and Whiteside TL. Overexpre-ssion of GLUT-1 is associated with resistance to radiotherapy and adverse prognosis in squamous cell carcinoma of the oral cavity. Oral Oncol 2007; 43: 796-803.
56. Macheda ML, Rogers S and Best JD. Molecular and cellular regulation of glucose transporter (GLUT) proteins in cancer. J Cell Physiol 2005; 202: 654-662.
57. Younes M, Brown RW, Stephenson M, Gondo M and Cagle PT. Overexpression of Glut1 and Glut3 in stage I nonsmall cell lung carcinoma is associated with poor survival. Cancer 1997; 80: 1046-1051.
58. Haber RS, Rathan A, Weiser KR, Pritsker A, Itzkowitz SH, Bodian C, Slater G, Weiss A and Burstein DE. GLUT1 glucose transporter expression in colorectal carcinoma: a marker for poor prognosis. Cancer 1998; 83: 34-40.
59. Cantuaria G, Fagotti A, Ferrandina G, Magal-haes A, Nadji M, Angioli R, Penalver M, Man-cuso S and Scambia G. GLUT-1 expression in ovarian carcinoma: association with survival and response to chemotherapy. Cancer 2001; 92: 1144-1150.
60. Kawamura T, Kusakabe T, Sugino T, Watanabe K, Fukuda T, Nashimoto A, Honma K and Suzuki T. Expression of glucose transporter-1 in human gastric carcinoma: association with tumor aggressiveness, metastasis, and patient survival. Cancer 2001; 92: 634-641.
61. Airley R, Loncaster J, Davidson S, Bromley M, Roberts S, Patterson A, Hunter R, Stratford I and West C. Glucose transporter glut-1 expression correlates with tumor hypoxia and predicts metastasis-free survival in advanced carcinoma of the cervix. Clin Cancer Res 2001; 7: 928-934.
62. Pedersen MW, Holm S, Lund EL, Hojgaard L and Kristjansen PE. Coregulation of glucose uptake and vascular endothelial growth factor (VEGF) in two small-cell lung cancer (SCLC) sublines in vivo and in vitro. Neoplasia 2001; 3: 80-87.
63. Tian L, Zhang Y, Chen Y, Cai M, Dong H and Xiong L. EMMPRIN is an independent negative prognostic factor for patients with astrocytic glioma. PLoS One 2013; 8: e58069.
64. Bachtiary B, Schindl M, Potter R, Dreier B, Knocke TH, Hainfellner JA, Horvat R and Birner P. Overexpression of hypoxia-inducible factor 1alpha indicates diminished response to radiotherapy and unfavorable prognosis in patients receiving radical radiotherapy for cervical cancer. Clin Cancer Res 2003; 9: 2234-2240.
65. Reimers N, Zafrakas K, Assmann V, Egen C, Riethdorf L, Riethdorf S, Berger J, Ebel S, Janicke F, Sauter G and Pantel K. Expression of extracellular matrix metalloproteases inducer on micrometastatic and primary mammary carcinoma cells. Clin Cancer Res 2004; 10: 3422-3428.
66. Tsai WC, Chao YC, Lee WH, Chen A, Sheu LF and Jin JS. Increasing EMMPRIN and matrip-tase expression in hepatocellular carcinoma: tissue microarray analysis of immunohistoche-mical scores with clinicopathological parame-ters. Histopathology 2006; 49: 388-395.
67. Zheng HC, Takahashi H, Murai Y, Cui ZG, Nomoto K, Miwa S, Tsuneyama K and Takano Y. Upregulated EMMPRIN/CD147 might contri-bute to growth and angiogenesis of gastric carcinoma: a good marker for local invasion and prognosis. Br J Cancer 2006; 95: 1371-1378.
68. Ishibashi Y, Matsumoto T, Niwa M, Suzuki Y, Omura N, Hanyu N, Nakada K, Yanaga K, Ya-mada K, Ohkawa K, Kawakami M and Urashi-ma M. CD147 and matrix metalloproteinase-2 protein expression as significant prognostic factors in esophageal squamous cell carcino-ma. Cancer 2004; 101: 1994-2000.
69. Jin JS, Yao CW, Loh SH, Cheng MF, Hsieh DS and Bai CY. Increasing expression of extracel-lular matrix metalloprotease inducer in ovary tumors: tissue microarray analysis of immuno-staining score with clinicopathological para-meters. Int J Gynecol Pathol 2006; 25: 140-146.
70. Sameshima T, Nabeshima K, Toole BP, Yoko-gami K, Okada Y, Goya T, Koono M and Waki-saka S. Expression of emmprin (CD147), a cell surface inducer of matrix metalloproteinases, in normal human brain and gliomas. Int J Cancer 2000; 88: 21-27.
71. Jiang JL, Zhou Q, Yu MK, Ho LS, Chen ZN and Chan HC. The involvement of HAb18G/CD147 in regulation of store-operated calcium entry and metastasis of human hepatoma cells. J Biol Chem 2001; 276: 46870-46877.
72. Bordador LC, Li X, Toole B, Chen B, Regezi J, Zardi L, Hu Y and Ramos DM. Expression of emmprin by oral squamous cell carcinoma. Int J Cancer 2000; 85: 347-352.
73. Kanekura T, Chen X and Kanzaki T. Basigin (CD147) is expressed on melanoma cells and induces tumor cell invasion by stimulating production of matrix metalloproteinases by fibroblasts. Int J Cancer 2002; 99: 520-528.
74. Du ZM, Hu CF, Shao Q, Huang MY, Kou CW, Zhu XF, Zeng YX and Shao JY. Upregulation of caveolin-1 and CD147 expression in nasopha-ryngeal carcinoma enhanced tumor cell mig-ration and correlated with poor prognosis of the patients. Int J Cancer 2009; 125: 1832-1841.
75. Pinheiro C, Longatto-Filho A, Pereira SM, Etlinger D, Moreira MA, Jube LF, Queiroz GS, Schmitt F and Baltazar F. Monocarboxylate transporters 1 and 4 are associated with CD147 in cervical carcinoma. Dis Markers 2009; 26: 97-103.
76. Adekola K, Rosen ST and Shanmugam M. Glucose transporters in cancer metabolism. Curr Opin Oncol 2012; 24: 650-654.
77. Liu TQ, Fan J, Zhou L and Zheng SS. Effects of suppressing glucose transporter-1 by an antisense oligodeoxynucleotide on the growth of human hepatocellular carcinoma cells. Hepatobiliary Pancreat Dis Int 2011; 10: 72-77.
78. Medina RA and Owen GI. Glucose transporters: expression, regulation and cancer. Biol Res 2002; 35: 9-26.
79. Szablewski L. Expression of glucose transport-ers in cancers. Biochim Biophys Acta 2013; 1835: 164-169.
80. Bartrons R and Caro J. Hypoxia, glucose meta-bolism and the Warburg's effect. J Bioenerg Biomembr 2007; 39: 223-229.
81. Meijer TW, Kaanders JH, Span PN and Bussink J. Targeting hypoxia, HIF-1, and tumor glucose metabolism to improve radiotherapy efficacy. Clin Cancer Res 2012; 18: 5585-5594.
82. Horsman MR. Measurement of tumor oxyge-nation. Int J Radiat Oncol Biol Phys 1998; 42: 701-704.
83. Vander Heiden MG, Cantley LC and Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 2009; 324: 1029-1033.
84. Leninger A, Nelson DL and Cox MM. Principles of biochemistry. Water: Its Effect on Dissolved Biomolecules. 2nd ed. New York: Worth Pub-lishers 1993; pp: 87.
85. Kim MK, Kim TJ, Sung CO, Choi CH, Lee JW, Kim BG and Bae DS. High expression of mTOR is associated with radiation resistance in cervical cancer. J Gynecol Oncol 2010; 21: 181-185.