Global loss of a nuclear lamina component, lamin A/C, and LINC complex components SUN1, SUN2, and nesprin-2 in breast cancer

Cancer Medicine

Volumn 4, Issue 10, 2015, Pages 1547-1557

  Matsumoto, Ayaka ^a   Hieda, Miki ^a   Yokoyama, Yuhki ^a   Nishioka, Yu ^a,b   Yoshidome, Katsuhide ^c   Tsujimoto, Masahiko ^c   Matsuura, Nariaki ^a  

^a OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b 1 5 5 Minatojima Minamimachi   (Japan)

^c OSAKA POLICE HOSPITAL   (Japan)

Author keywords

Breast cancer; Lamin A C; LINC complex; Nesprin 2; SUN1 2

Indexed keywords

CELL PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR 2; LAMININ; MESSENGER RNA; NESPRIN 2; PROTEIN SUN1; PROTEIN SUN2; UNCLASSIFIED DRUG; ACTIN BINDING PROTEIN; ERBB2 PROTEIN, HUMAN; KI 67 ANTIGEN; LAMIN A; LMNA PROTEIN, HUMAN; MEMBRANE PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; NERVE PROTEIN; NUCLEAR PROTEIN; SIGNAL PEPTIDE; SUN1 PROTEIN, HUMAN; SUN2 PROTEIN, HUMAN; SYNE2 PROTEIN, HUMAN;

ARTICLE; BREAST CANCER; CANCER CELL; CANCER GROWTH; CANCER RECURRENCE; CANCER SURVIVAL; CELL LOSS; CONTROLLED STUDY; DISEASE FREE SURVIVAL; EPITHELIUM CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; NUCLEAR LAMINA; OVERALL SURVIVAL; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; TUMOR CLASSIFICATION; BREAST TUMOR; CLASSIFICATION; DOWN REGULATION; FEMALE; MCF-7 CELL LINE; METABOLISM; PATHOLOGY; TUMOR RECURRENCE;

BREAST NEOPLASMS; DOWN-REGULATION; FEMALE; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; KI-67 ANTIGEN; LAMIN TYPE A; MCF-7 CELLS; MEMBRANE PROTEINS; MICROFILAMENT PROTEINS; MICROTUBULE-ASSOCIATED PROTEINS; NEOPLASM RECURRENCE, LOCAL; NERVE TISSUE PROTEINS; NUCLEAR LAMINA; NUCLEAR PROTEINS; RECEPTOR, ERBB-2;

EID: 84949580921     PISSN: None     EISSN: 20457634     Source Type: Journal    
DOI: 10.1002/cam4.495     Document Type: Article

References (37)

1. Zink, D., A. H. Fischer, and J. A. Nickerson. 2004. Nuclear structure in cancer cells. Nat. Rev. Cancer 4:677-687.
2. Chow, K. H., R. E. Factor, and K. S. Ullman. 2012. The nuclear envelope environment and its cancer connections. Nat. Rev. Cancer 12:196-209.
3. Crisp, M., Q. Liu, K. Roux, J. B. Rattner, C. Shanahan, B. Burke, et al. 2006. Coupling of the nucleus and cytoplasm: role of the LINC complex. J. Cell Biol. 172:41-53.
4. Isermann, P., and J. Lammerding. 2013. Nuclear mechanics and mechanotransduction in health and disease. Curr. Biol. 23:R1113-R1121.
5. Khatau, S. B., C. M. Hale, P. J. Stewart-Hutchinson, M. S. Patel, C. L. Stewart, P. C. Searson, et al. 2009. A perinuclear actin cap regulates nuclear shape. Proc. Natl Acad. Sci. USA 106:19017-19022.
6. Meinke, P., T. D. Nguyen, and M. S. Wehnert. 2011. The LINC complex and human disease. Biochem. Soc. Trans. 39:1693-1697.
7. Wu, Z., L. Wu, D. Weng, D. Xu, J. Geng, and F. Zhao. 2009. Reduced expression of lamin A/C correlates with poor histological differentiation and prognosis in primary gastric carcinoma. J. Exp. Clin. Cancer Res. 28:8. doi:10.1186/1756-9966-28-8
8. Broers, J. L., Y. Raymond, M. K. Rot, H. Kuijpers, S. S. Wagenaar, and F. C. Ramaekers. 1993. Nuclear A-type lamins are differentially expressed in human lung cancer subtypes. Am. J. Pathol. 143:211-220.
9. Stadelmann, B., E. Khandjian, A. Hirt, A. Lüthy, R. Weil, and H. P. Wagner. 1990. Repression of nuclear lamin A and C gene expression in human acute lymphoblastic leukemia and non-Hodgkin's lymphoma cells. Leuk. Res. 14:815-821.
10. Agrelo, R., F. Setien, J. Espada, M. J. Artiga, M. Rodriguez, A. Pérez-Rosado, et al. 2005. Inactivation of the lamin A/C gene by CpG island promoter hypermethylation in hematologic malignancies, and its association with poor survival in nodal diffuse large B-cell lymphoma. J. Clin. Oncol. 23:3940-3947.
11. Capo-chichi, C. D., K. Q. Cai, F. Simpkins, P. Ganjei-Azar, A. K. Godwin, and X. X. Xu. 2011. Nuclear envelope structural defects cause chromosomal numerical instability and aneuploidy in ovarian cancer. BMC Med. 9:28. doi:10.1186/1741-7015-9-28
12. Capo-chichi, C. D., K. Q. Cai, J. Smedberg, P. Ganjei-Azar, A. K. Godwin, and X. X. Xu. 2011. Loss of A-type lamin expression compromises nuclear envelope integrity in breast cancer. Chin. J. Cancer 30:415-425.
13. Wazir, U., M. H. Ahmed, J. M. Bridger, A. Harvey, W. G. Jiang, Sharma, A. K. et al. 2013. The clinicopathological significance of lamin A/C, lamin B1 and lamin B receptor mRNA expression in human breast cancer. Cell. Mol. Biol. Lett. 18:595-611.
14. Hudson, M. E., I. Pozdnyakova, K. Haines, G. Mor, and M. Snyder. 2007. Identification of differentially expressed proteins in ovarian cancer using high-density protein microarrays. Proc. Natl Acad. Sci. USA 104:17494-17499.
15. Willis, N. D., T. R. Cox, S. F. Rahman-Casans, K. Smits, S. A. Przyborski, et al. 2008. Lamin A/C is a risk biomarker in colorectal cancer. PLoS ONE 3:e2988. doi:10.1371/journal.pone.0002988
16. Kong, L., G. Schäfer, H. Bu, Y. Zhang, Y. Zhang, and H. Klocker. 2012. Lamin A/C protein is overexpressed in tissue-invading prostate cancer and promotes prostate cancer cell growth, migration and invasion through the PI3K/AKT/PTEN pathway. Carcinogenesis 33:751-759.
17. Tilli, C. M., F. C. Ramaekers, J. L. Broers, C. J. Hutchison, and H. A. Neumann. 2003. Lamin expression in normal human skin, actinic keratosis, squamous cell carcinoma and basal cell carcinoma. Br. J. Dermatol. 148:102-109.
18. Venables, R. S., S. McLean, D. Luny, E. Moteleb, S. Morley, et al. 2001. Expression of individual lamins in basal cell carcinomas of the skin. Br. J. Cancer 84:512-519.
19. Mattout, A., T. Dechat, S. A. Adam, R. D. Goldman, and Y. Gruenbaum. 2006. Nuclear lamins, diseases and aging. Curr. Opin. Cell Biol. 18:335-341.
20. Gruenbaum, Y., A. Margalit, R. D. Goldman, D. K. Shumaker, and K. L. Wilson. 2005. The nuclear lamina comes of age. Nat. Rev. Mol. Cell Biol. 6:21-31.
21. Mekhail, K., J. Seebacher, S. P. Gygi, and D. Moazed. 2008. Role for perinuclear chromosome tethering in maintenance of genome stability. Nature 456:667-670.
22. Crabbe, L., A. J. Cesare, J. M. Kasuboski, J. A. Fitzpatrick, and J. Karlseder. 2012. Human telomeres are tethered to the nuclear envelope during postmitotic nuclear assembly. Cell Rep. 2:1521-1529.
23. Yokoyama, Y., M. Hieda, Y. Nishioka, A. Matsumoto, S. Higashi, et al. 2013. Cancer-associated upregulation of histone H3 lysine 9 trimethylation promotes cell motility in vitro and drives tumor formation in vivo. Cancer Sci. 104:889-895.
24. Yokoyama, Y., A. Matsumoto, M. Hieda, Y. Shinchi, E. Ogihara, M. Hamada, et al. 2014. Loss of histone H4K20 trimethylation predicts poor prognosis in breast cancer and is associated with invasive activity. Breast Cancer Res. 16:R66. doi:10.1186/bcr3681
25. Tanaka, H., Y. Nishioka, Y. Yokoyama, S. Higashiyama, N. Matsuura, et al. 2012. Nuclear envelope-localized EGF family protein amphiregulin activates breast cancer cell migration in an EGF-like domain independent manner. Biochem. Biophys. Res. Commun. 420:721-726.
26. Starr, D. A., and M. Han. 2003. ANChors away: an actin based mechanism of nuclear positioning. J. Cell Sci. 116(Pt. 2):211-216.
27. Houben, F., F. C. Ramaekers, L. H. Snoeckx, and J. L. Broers. 2007. Role of nuclear lamina-cytoskeleton interactions in the maintenance of cellular strength. Biochim. Biophys. Acta 1773:675-686.
28. Stewart-Hutchinson, P. J., C. M. Hale, D. Wirtz, and D. Hodzic. 2008. Structural requirements for the assembly of LINC complexes and their function in cellular mechanical stiffness. Exp. Cell Res. 314:1892-1905.
29. van Steensel, B., and J. Kind. 2014. Stochastic genome-nuclear lamina interactions: modulating roles of Lamin A and BAF. Nucleus 5:124-130.
30. Lund, E., A. R. Oldenburg, E. Delbarre, C. T. Freberg, I. Duband-Goulet, et al. 2013. Lamin A/C-promoter interactions specify chromatin state-dependent transcription outcomes. Genome Res. 23:1580-1589.
31. Yang, W., H. Zheng, Y. Wang, F. Lian, Z. Hu, and S. Xue. 2013. Nesprin-1 plays an important role in the proliferation and apoptosis of mesenchymal stem cells. Int. J. Mol. Med. 32:805-812.
32. Warren, D. T., T. Tajsic, J. A. Mellad, R. Searles, Q. Zhang, and C. M. Shanahan. 2010. Novel nuclear nesprin-2 variants tether active extracellular signal-regulated MAPK1 and MAPK2 at promyelocytic leukemia protein nuclear bodies and act to regulate smooth muscle cellproliferation. J. Biol. Chem. 285:1311-1320.
33. Rashmi, R. N., B. Eckes, G. Glöckner, M. Groth, S. Neumann, J. Gloy, et al. 2012. The nuclear envelope protein Nesprin-2 has roles in cellproliferation and differentiation during wound healing. Nucleus 3:172-186.
34. Lei, K., X. Zhu, R. Xu, C. Shao, T. Xu, et al. 2012. Inner nuclear envelope proteins SUN1 and SUN2 play a prominent role in the DNA damage response. Curr. Biol. 22:1609-1615.
35. Oza, P., S. L. Jaspersen, A. Miele, J. Dekker, and C. L. Peterson. 2009. Mechanisms that regulate localization of a DNA double-strand break to the nuclear periphery. Genes Dev. 23:912-927.
36. Horn, H. F., D. I. Kim, G. D. Wright, E. S. Wong, C. L. Stewart, B. Burke, et al. 2013. A mammalian KASH domain protein coupling meiotic chromosomes to the cytoskeleton. J. Cell Biol. 202:1023-1039.
37. Chen, C. Y., Y. H. Chi, R. A. Mutalif, M. F. Starost, T. G. Myers, et al. 2012. Accumulation of the inner nuclear envelope protein Sun1 is pathogenic in progeric and dystrophic laminopathies. Cell 27:565-577.