Elevated HMGA2 expression is associated with cancer aggressiveness and predicts poor outcome in breast cancer

Cancer Letters

Volumn 376, Issue 2, 2016, Pages 284-292

  Wu, Jingjing ^a   Zhang, Shizhen ^a   Shan, Jinlan ^a   Hu, Zujian ^b   Liu, Xiyong ^c   Chen, Lirong ^a   Ren, Xingchang ^b   Yao, Lifang ^a   Sheng, Hongqiang ^a   Li, Ling ^d   Ann, David ^d   Yen, Yun ^e   Wang, Jian ^a   Wang, Xiaochen ^a  

^a ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b Hangzhou Traditional Chinese Medicine Hospital   (China)

^c Biomarker Development   (United States)

^d CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^e TAIPEI MEDICAL UNIVERSITY   (Taiwan)

Author keywords

Breast cancer; High mobility group AT hook 2; Prognostic biomarker; Tumor progression

Indexed keywords

BIOLOGICAL MARKER; PROTEIN P53; HIGH MOBILITY GROUP A2 PROTEIN; TP53 PROTEIN, HUMAN; TUMOR MARKER;

ADULT; ARTICLE; BREAST CANCER; BREAST CANCER CELL LINE; CANCER GRADING; CANCER STAGING; CANCER SURVIVAL; CELL INVASION; CELL MIGRATION; COHORT ANALYSIS; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; GENETIC ASSOCIATION; HMGA2 GENE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; ONCOGENE; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; TRIPLE NEGATIVE BREAST CANCER; BREAST TUMOR; CELL MOTION; CELL PROLIFERATION; GENE EXPRESSION PROFILING; GENETIC PREDISPOSITION; GENETIC TRANSFECTION; GENETICS; KAPLAN MEIER METHOD; MCF-7 CELL LINE; METABOLISM; MIDDLE AGED; MORTALITY; PATHOLOGY; PHOSPHORYLATION; PREDICTIVE VALUE; PROPORTIONAL HAZARDS MODEL; REPRODUCIBILITY; RISK FACTOR; TIME FACTOR; TREATMENT OUTCOME; TUMOR INVASION; UPREGULATION; VALIDATION STUDY;

BIOMARKERS, TUMOR; BREAST NEOPLASMS; CELL MOVEMENT; CELL PROLIFERATION; FEMALE; GENE EXPRESSION PROFILING; GENETIC PREDISPOSITION TO DISEASE; HMGA2 PROTEIN; HUMANS; IMMUNOHISTOCHEMISTRY; KAPLAN-MEIER ESTIMATE; MCF-7 CELLS; MIDDLE AGED; NEOPLASM GRADING; NEOPLASM INVASIVENESS; PHENOTYPE; PHOSPHORYLATION; PREDICTIVE VALUE OF TESTS; PROPORTIONAL HAZARDS MODELS; REPRODUCIBILITY OF RESULTS; RISK FACTORS; TIME FACTORS; TRANSFECTION; TREATMENT OUTCOME; TUMOR SUPPRESSOR PROTEIN P53; UP-REGULATION;

EID: 84963610832     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2016.04.005     Document Type: Article

References (47)

1. Siegel R.L., Miller K.D., Jemal A. Cancer statistics, 2015. CA Cancer J. Clin 2015, 65:5-29.
2. Berry D.A., Cronin K.A., Plevritis S.K., Fryback D.G., Clarke L., Zelen M., et al. Effect of screening and adjuvant therapy on mortality from breast cancer. N. Engl. J. Med 2005, 353:1784-1792.
3. Fadoukhair Z., Zardavas D., Chad M.A., Goulioti T., Aftimos P., Piccart M. Evaluation of targeted therapies in advanced breast cancer: the need for large-scale molecular screening and transformative clinical trial designs. Oncogene 2015, 10.1038/onc.2015.249.
4. Fusco A., Fedele M. Roles of HMGA proteins in cancer. Nat. Rev. Cancer 2007, 7:899-910.
5. Young A.R., Narita M. Oncogenic HMGA2: short or small?. Genes Dev 2007, 21:1005-1009.
6. Hammond S.M., Sharpless N.E. HMGA2, microRNAs, and stem cell aging. Cell 2008, 135:1013-1016.
7. Zhou X., Benson K.F., Ashar H.R., Chada K. Mutation responsible for the mouse pygmy phenotype in the developmentally regulated factor HMGI-C. Nature 1995, 376:771-774.
8. Li A.Y., Boo L.M., Wang S.Y., Lin H.H., Wang C.C., Yen Y., et al. Suppression of nonhomologous end joining repair by overexpression of HMGA2. Cancer Res 2009, 69:5699-5706.
9. Summer H., Li O., Bao Q., Zhan L., Peter S., Sathiyanathan P., et al. HMGA2 exhibits dRP/AP site cleavage activity and protects cancer cells from DNA-damage-induced cytotoxicity during chemotherapy. Nucleic Acids Res 2009, 37:4371-4384.
10. Singh I., Ozturk N., Cordero J., Mehta A., Hasan D., Cosentino C., et al. High mobility group protein-mediated transcription requires DNA damage marker gamma-H2AX. Cell Res 2015, 25:837-850.
11. Natarajan S., Hombach-Klonisch S., Droge P., Klonisch T. HMGA2 inhibits apoptosis through interaction with ATR-CHK1 signaling complex in human cancer cells. Neoplasia 2013, 15:263-280.
12. Wend P., Runke S., Wend K., Anchondo B., Yesayan M., Jardon M., et al. WNT10B/beta-catenin signalling induces HMGA2 and proliferation in metastatic triple-negative breast cancer. EMBO Mol. Med 2013, 5:264-279.
13. Li Y., Peng L., Seto E. Histone deacetylase 10 regulates the cell cycle G2/M phase transition via a novel Let-7-HMGA2-Cyclin A2 pathway. Mol. Cell. Biol 2015, 35:3547-3565.
14. Narita M., Krizhanovsky V., Nunez S., Chicas A., Hearn S.A., Myers M.P., et al. A novel role for high-mobility group a proteins in cellular senescence and heterochromatin formation. Cell 2006, 126:503-514.
15. Wu J., Liu Z., Shao C., Gong Y., Hernando E., Lee P., et al. HMGA2 overexpression-induced ovarian surface epithelial transformation is mediated through regulation of EMT genes. Cancer Res 2011, 71:349-359.
16. Tan E.J., Kahata K., Idas O., Thuault S., Heldin C.H., Moustakas A. The high mobility group A2 protein epigenetically silences the Cdh1 gene during epithelial-to-mesenchymal transition. Nucleic Acids Res 2015, 43:162-178.
17. Morishita A., Zaidi M.R., Mitoro A., Sankarasharma D., Szabolcs M., Okada Y., et al. HMGA2 is a driver of tumor metastasis. Cancer Res 2013, 73:4289-4299.
18. Li A.Y., Lin H.H., Kuo C.Y., Shih H.M., Wang C.C., Yen Y., et al. High-mobility group A2 protein modulates hTERT transcription to promote tumorigenesis. Mol. Cell. Biol 2011, 31:2605-2617.
19. Wang X., Liu X., Li A.Y., Chen L., Lai L., Lin H.H., et al. Overexpression of HMGA2 promotes metastasis and impacts survival of colorectal cancers. Clin. Cancer Res 2011, 17:2570-2580.
20. Piscuoglio S., Zlobec I., Pallante P., Sepe R., Esposito F., Zimmermann A., et al. HMGA1 and HMGA2 protein expression correlates with advanced tumour grade and lymph node metastasis in pancreatic adenocarcinoma. Histopathology 2012, 60:397-404.
21. Chang K.P., Lin S.J., Liu S.C., Yi J.S., Chien K.Y., Chi L.M., et al. Low-molecular-mass secretome profiling identifies HMGA2 and MIF as prognostic biomarkers for oral cavity squamous cell carcinoma. Sci. Rep 2015, 5:11689.
22. Saada-Bouzid E., Burel-Vandenbos F., Ranchere-Vince D., Birtwisle-Peyrottes I., Chetaille B., Bouvier C., et al. Prognostic value of HMGA2, CDK4, and JUN amplification in well-differentiated and dedifferentiated liposarcomas. Mod. Pathol 2015, 28:1404-1414.
23. Sun M., Gomes S., Chen P., Frankenberger C.A., Sankarasharma D., Chung C.H., et al. RKIP and HMGA2 regulate breast tumor survival and metastasis through lysyl oxidase and syndecan-2. Oncogene 2014, 33:3528-3537.
24. Boo L.M., Lin H.H., Chung V., Zhou B., Louie S.G., O'Reilly M.A., et al. High mobility group A2 potentiates genotoxic stress in part through the modulation of basal and DNA damage-dependent phosphatidylinositol 3-kinase-related protein kinase activation. Cancer Res 2005, 65:6622-6630.
25. Langelotz C., Schmid P., Jakob C., Heider U., Wernecke K.D., Possinger K., et al. Expression of high-mobility-group-protein HMGI-C mRNA in the peripheral blood is an independent poor prognostic indicator for survival in metastatic breast cancer. Br. J. Cancer 2003, 88:1406-1410.
26. Wu J., Lai M., Shao C., Wang J., Wei J.J. STC2 overexpression mediated by HMGA2 is a biomarker for aggressiveness of high-grade serous ovarian cancer. Oncol. Rep 2015, 34:1494-1502.
27. Desmedt C., Piette F., Loi S., Wang Y., Lallemand F., Haibe-Kains B., et al. Strong time dependence of the 76-gene prognostic signature for node-negative breast cancer patients in the TRANSBIG multicenter independent validation series. Clin. Cancer Res 2007, 13:3207-3214.
28. Smeds J., Miller L.D., Bjohle J., Hall P., Klaar S., Liu E.T., et al. Gene profile and response to treatment. Ann. Oncol 2005, 16(Suppl. 2):ii195-ii202.
29. van de Vijver M.J., He Y.D., van't Veer L.J., Dai H., Hart A.A., Voskuil D.W., et al. A gene-expression signature as a predictor of survival in breast cancer. N. Engl. J. Med 2002, 347:1999-2009.
30. Ivshina A.V., George J., Senko O., Mow B., Putti T.C., Smeds J., et al. Genetic reclassification of histologic grade delineates new clinical subtypes of breast cancer. Cancer Res 2006, 66:10292-10301.
31. Wang Y., Klijn J.G., Zhang Y., Sieuwerts A.M., Look M.P., Yang F., et al. Gene-expression profiles to predict distant metastasis of lymph-node-negative primary breast cancer. Lancet 2005, 365:671-679.
32. Zhang H., Liu X., Warden C.D., Huang Y., Loera S., Xue L., et al. Prognostic and therapeutic significance of ribonucleotide reductase small subunit M2 in estrogen-negative breast cancers. BMC Cancer 2014, 14:664.
33. Irizarry R.A., Wang C., Zhou Y., Speed T.P. Gene set enrichment analysis made simple. Stat. Methods Med. Res 2009, 18:565-575.
34. Madison B.B., Jeganathan A.N., Mizuno R., Winslow M.M., Castells A., Cuatrecasas M., et al. Let-7 represses carcinogenesis and a stem cell phenotype in the intestine via regulation of Hmga2. PLoS Genet 2015, 11:e1005408.
35. Yu K.R., Shin J.H., Kim J.J., Koog M.G., Lee J.Y., Choi S.W., et al. Rapid and efficient direct conversion of human adult somatic cells into neural stem cells by HMGA2/let-7b. Cell Rep 2015, pii: S2211-1247(14)01067-5.
36. Chien C.S., Wang M.L., Chu P.Y., Chang Y.L., Liu W.H., Yu C.C., et al. Lin28B/Let-7 regulates expression of Oct4 and Sox2 and reprograms oral squamous cell carcinoma cells to a stem-like state. Cancer Res 2015, 75:2553-2565.
37. Alam M., Ahmad R., Rajabi H., Kufe D. MUC1-C induces the LIN28B→LET-7→HMGA2 axis to regulate self-renewal in NSCLC. Mol. Cancer Res 2015, 13:449-460.
38. Parameswaran S., Xia X., Hegde G., Ahmad I. Hmga2 regulates self-renewal of retinal progenitors. Development 2014, 141:4087-4097.
39. Nishino J., Kim I., Chada K., Morrison S.J. Hmga2 promotes neural stem cell self-renewal in young but not old mice by reducing p16Ink4a and p19Arf Expression. Cell 2008, 135:227-239.
40. Ding X., Wang Y., Ma X., Guo H., Yan X., Chi Q., et al. Expression of HMGA2 in bladder cancer and its association with epithelial-to-mesenchymal transition. Cell Prolif 2014, 47:146-151.
41. Wu J., Li S., Jia W., Deng H., Chen K., Zhu L., et al. Reduced Let-7a is associated with chemoresistance in primary breast cancer. PLoS ONE 2015, 10. e0133643.
42. Gyorffy B., Surowiak P., Kiesslich O., Denkert C., Schafer R., Dietel M., et al. Gene expression profiling of 30 cancer cell lines predicts resistance towards 11 anticancer drugs at clinically achieved concentrations. Int. J. Cancer 2006, 118:1699-1712.
43. Yu H., Lim H.H., Tjokro N.O., Sathiyanathan P., Natarajan S., Chew T.W., et al. Chaperoning HMGA2 protein protects stalled replication forks in stem and cancer cells. Cell Rep 2014, 6:684-697.
44. Palmieri D., Valentino T., D'Angelo D., De Martino I., Postiglione I., Pacelli R., et al. HMGA proteins promote ATM expression and enhance cancer cell resistance to genotoxic agents. Oncogene 2011, 30:3024-3035.
45. Deschoemaeker S., Di Conza G., Lilla S., Martin-Perez R., Mennerich D., Boon L., et al. PHD1 regulates p53-mediated colorectal cancer chemoresistance. EMBO Mol. Med 2015, 7:1350-1365.
46. Al Rashid S.T., Dellaire G., Cuddihy A., Jalali F., Vaid M., Coackley C., et al. Evidence for the direct binding of phosphorylated p53 to sites of DNA breaks in vivo. Cancer Res 2005, 65:10810-10821.
47. Wei J.J., Wu J., Luan C., Yeldandi A., Lee P., Keh P., et al. HMGA2: a potential biomarker complement to P53 for detection of early-stage high-grade papillary serous carcinoma in fallopian tubes. Am. J. Surg. Pathol 2010, 34:18-26.