Display options
Share it on

Oncogenesis. 2020 Sep 18;9(9):83. doi: 10.1038/s41389-020-00266-y.

The membrane-associated form of cyclin D1 enhances cellular invasion.

Oncogenesis

Ke Chen, Xuanmao Jiao, Anthony Ashton, Agnese Di Rocco, Timothy G Pestell, Yunguang Sun, Jun Zhao, Mathew C Casimiro, Zhiping Li, Michael P Lisanti, Peter A McCue, Duanwen Shen, Samuel Achilefu, Hallgeir Rui, Richard G Pestell

Affiliations

  1. Department of Cancer Biology, Thomas Jefferson University, Philadelphia, PA, 19107, USA.
  2. Pennsylvania Cancer and Regenerative Medicine Research Center, Baruch S. Blumberg Institute, Pennsylvania Biotechnology Center, Wynnewood, PA, 19096, USA.
  3. Department of Pathology, Medical College of Wisconsin, Milwaukee, WI, 53226, USA.
  4. Dept of Science and Math, Abraham Baldwin Agricultural college, Tifton, GA, 31794, Georgia.
  5. Biomedical Research Centre (BRC), Translational Medicine, School of Environment and Life Sciences, University of Salford, Manchester, United Kingdom.
  6. Department of Pathology, Anatomy and Cell Biology, Sidney Kimmel Cancer Center, Thomas Jefferson University, Philadelphia, PA, 19107, USA.
  7. Departments of Biomedical Engineering, Washington University, St. Louis, MO, 63110, USA.
  8. Departments of Radiology, Washington University, St. Louis, MO, 63110, USA.
  9. Departments of Biochemistry & Molecular Biophysics, Washington University, St. Louis, MO, 63110, USA.
  10. Pennsylvania Cancer and Regenerative Medicine Research Center, Baruch S. Blumberg Institute, Pennsylvania Biotechnology Center, Wynnewood, PA, 19096, USA. [email protected].
  11. The Wistar Cancer Center, Wistar Institute, Philadelphia, PA, 19104, USA. [email protected].

PMID: 32948740 PMCID: PMC7501870 DOI: 10.1038/s41389-020-00266-y

Abstract

The essential G

References

  1. Hanahan, D. & Weinberg, R. A. Hallmarks of cancer: the next generation. Cell 144, 646–674 (2011). - PubMed
  2. Hassaan, S. H. et al. Assessment of cognitive functions and psychiatric symptoms in hepatitis C patients receiving pegylated interferon alpha and ribavirin: a prospective cohort study. Int J. Psychiatry Med. 54, 424–440 (2019). - PubMed
  3. Sherr, C. J. G1 phase progression: cycling on cue. Cell 79, 551–555 (1994). - PubMed
  4. Hinds, P. W., Dowdy, S. F., Eaton, E. N., Arnold, A. & Weinberg, R. A. Function of a human cyclin gene as an oncogene. Proc. Natl Acad. Sci. USA 91, 709–713 (1994). - PubMed
  5. Lee, R. J. et al. Cyclin D1 is required for transformation by activated Neu and is induced through an E2F-dependent signaling pathway. Mol. Cell Biol. 20, 672–683 (2000). - PubMed
  6. Yu, B., Lane, M. E., Pestell, R. G., Albanese, C. & Wadler, S. Downregulation of cyclin D1 alters cdk 4- and cdk 2-specific phosphorylation of retinoblastoma protein. Mol. Cell Biol. Res. Commun. 3, 352–359 (2000). - PubMed
  7. Hulit, J. et al. Cyclin D1 genetic heterozygosity regulates colonic epithelial cell differentiation and tumor number in ApcMin mice. Mol. Cell Biol. 24, 7598–7611 (2004). - PubMed
  8. Robles, A. I. et al. Reduced skin tumor development in cyclin D1-deficient mice highlights the oncogenic ras pathway in vivo. Genes Dev. 12, 2469–2474 (1998). - PubMed
  9. Sicinski, P. et al. Cyclin D1 provides a link between development and oncogenesis in the retina and breast. Cell 82, 621–630 (1995). - PubMed
  10. Casimiro, M. C. et al. ChIP sequencing of cyclin D1 reveals a transcriptional role in chromosomal instability in mice. J. Clin. Investig. 122, 833–843 (2012). - PubMed
  11. Wang, T. C. et al. Mammary hyperplasia and carcinoma in MMTV-cyclin D1 transgenic mice. Nature 369, 669–671 (1994). - PubMed
  12. Drobnjak, M., Osman, I., Scher, H. I., Fazzari, M. & Cordon-Cardo, C. Overexpression of cyclin D1 is associated with metastatic prostate cancer to bone. Clin. Cancer Res. 6, 1891–1895 (2000). - PubMed
  13. Hou, X. et al. Cyclin D1 expression predicts postoperative distant metastasis and survival in resectable esophageal squamous cell carcinoma. Oncotarget 7, 31088–31096 (2016). - PubMed
  14. Huang, H., Hu, Y. D., Li, N. & Zhu, Y. Inhibition of tumor growth and metastasis by non-small cell lung cancer cells transfected with cyclin D1-targeted siRNA. Oligonucleotides 19, 151–162 (2009). - PubMed
  15. Noorlag, R. et al. Amplification and protein overexpression of cyclin D1: predictor of occult nodal metastasis in early oral cancer. Head Neck 39, 326–333 (2017). - PubMed
  16. Borlakoglu, J. T., Stegeman, J. & Dils, R. R. Induction of hepatic cytochrome P-450IA1 in pigeons treated in vivo with Aroclor 1254, a commercial mixture of polychlorinated biphenyls (PCBs). Comp. Biochem. Physiol. C 99, 279–286 (1991). - PubMed
  17. Sumrejkanchanakij, P., Tamamori-Adachi, M., Matsunaga, Y., Eto, K. & Ikeda, M. A. Role of cyclin D1 cytoplasmic sequestration in the survival of postmitotic neurons. Oncogene 22, 8723–8730 (2003). - PubMed
  18. Tamamori-Adachi, M. et al. Critical role of cyclin D1 nuclear import in cardiomyocyte proliferation. Circ. Res. 92, e12–19 (2003). - PubMed
  19. Jaumot, M., Estanyol, J. M., Serratosa, J., Agell, N. & Bachs, O. Activation of cdk4 and cdk2 during rat liver regeneration is associated with intranuclear rearrangements of cyclin-cdk complexes. Hepatology 29, 385–395 (1999). - PubMed
  20. Alhaja, E. et al. Anti-migratory and anti-angiogenic effect of p16: a novel localization at membrane ruffles and lamellipodia in endothelial cells. Angiogenesis 7, 323–333 (2004). - PubMed
  21. Fuste, N. P. et al. Cytoplasmic cyclin D1 regulates cell invasion and metastasis through the phosphorylation of paxillin. Nat. Commun. 7, 11581 (2016). - PubMed
  22. Nebot-Cegarra, J. & Domenech-Mateu, J. M. Association of tracheoesophageal anomalies with visceral and parietal malformations in a human embryo (Carnegie stage 21). Teratology 39, 11–17 (1989). - PubMed
  23. Meng, H. et al. PACSIN 2 represses cellular migration through direct association with cyclin D1 but not its alternate splice form cyclin D1b. Cell Cycle 10, 73–81 (2011). - PubMed
  24. Zhong, Z. et al. Cyclin D1/cyclin-dependent kinase 4 interacts with filamin A and affects the migration and invasion potential of breast cancer cells. Cancer Res. 70, 2105–2114 (2010). - PubMed
  25. Fahraeus, R. & Lane, D. P. The p16(INK4a) tumour suppressor protein inhibits alphavbeta3 integrin-mediated cell spreading on vitronectin by blocking PKC-dependent localization of alphavbeta3 to focal contacts. EMBO J. 18, 2106–2118 (1999). - PubMed
  26. Li, Z. et al. Cyclin D1 regulates cellular migration through the inhibition of thrombospondin 1 and ROCK signaling. Mol. Cell Biol. 26, 4240–4256 (2006). - PubMed
  27. Li, Z., Wang, C., Prendergast, G. C. & Pestell, R. G. Cyclin D1 functions in cell migration. Cell Cycle 5, 2440–2442 (2006). - PubMed
  28. Neumeister, P. et al. Cyclin D1 governs adhesion and motility of macrophages. Mol. Biol. Cell 14, 2005–2015 (2003). - PubMed
  29. Dunbar, L. A. & Caplan, M. J. Ion pumps in polarized cells: sorting and regulation of the Na+, K+- and H+, K+-ATPases. J. Biol. Chem. 276, 29617–29620 (2001). - PubMed
  30. Casimiro, M. C. et al. Cyclin D1 promotes androgen-dependent DNA damage repair in prostate cancer cells. Cancer Res 76, 329–338 (2016). - PubMed
  31. Li, Z. et al. Alternative cyclin D1 splice forms differentially regulate the DNA damage response. Cancer Res. 70, 8802–8811 (2010). - PubMed
  32. Li, Z. et al. Cyclin D1 integrates estrogen-mediated DNA damage repair signaling. Cancer Res. 74, 3959–3970 (2014). - PubMed
  33. Soutoglou, E. & Misteli, T. Activation of the cellular DNA damage response in the absence of DNA lesions. Science 320, 1507–1510 (2008). - PubMed
  34. Razandi, M. et al. Identification of a structural determinant necessary for the localization and function of estrogen receptor alpha at the plasma membrane. Mol. Cell Biol. 23, 1633–1646 (2003). - PubMed
  35. Coumans, J. V. et al. Green fluorescent protein expression triggers proteome changes in breast cancer cells. Exp. Cell Res. 320, 33–45 (2014). - PubMed
  36. Wang, C. et al. Cyclin D1 repression of peroxisome proliferator-activated receptor gamma expression and transactivation. Mol. Cell Biol. 23, 6159–6173 (2003). - PubMed
  37. Levin, E. R. Minireview: extranuclear steroid receptors: roles in modulation of cell functions. Mol. Endocrinol. 25, 377–384 (2011). - PubMed
  38. Di Sante, G., Di Rocco, A., Pupo, C., Casimiro, M. C. & Pestell, R. G. Hormone-induced DNA damage response and repair mediated by cyclin D1 in breast and prostate cancer. Oncotarget 8, 81803–81812 (2017). - PubMed
  39. Dibble, C. C. & Cantley, L. C. Regulation of mTORC1 by PI3K signaling. Trends Cell Biol. 25, 545–555 (2015). - PubMed
  40. Hresko, R. C. & Mueckler, M. mTOR.RICTOR is the Ser473 kinase for Akt/protein kinase B in 3T3-L1 adipocytes. J. Biol. Chem. 280, 40406–40416 (2005). - PubMed
  41. Harrington, W. R. et al. Estrogen dendrimer conjugates that preferentially activate extranuclear, nongenomic versus genomic pathways of estrogen action. Mol. Endocrinol. 20, 491–502 (2006). - PubMed
  42. Madak-Erdogan, Z. et al. Nuclear and extranuclear pathway inputs in the regulation of global gene expression by estrogen receptors. Mol. Endocrinol. 22, 2116–2127 (2008). - PubMed
  43. Li, Z. et al. Cyclin D1 induction of cellular migration requires p27(KIP1). Cancer Res. 66, 9986–9994 (2006). - PubMed
  44. Li, Z. et al. Alternate cyclin D1 mRNA splicing modulates p27KIP1 binding and cell migration. J. Biol. Chem. 283, 7007–7015 (2008). - PubMed
  45. Martelli, A. M. et al. The emerging multiple roles of nuclear Akt. Biochim. Biophys. Acta 1823, 2168–2178 (2012). - PubMed
  46. Shen, D. et al. Dual fluorescent molecular substrates selectively report the activation, sustainability and reversibility of cellular PKB/Akt activity. Sci. Rep. 3, 1697 (2013). - PubMed
  47. Lawson, C. D. & Ridley, A. J. Rho GTPase signaling complexes in cell migration and invasion. J. Cell Biol. 217, 447–457 (2018). - PubMed
  48. Pestell, R. G. New roles of cyclin D1. Am. J. Pathol. 183, 3–9 (2013). - PubMed
  49. Gordon, B. S. et al. RhoA modulates signaling through the mechanistic target of rapamycin complex 1 (mTORC1) in mammalian cells. Cell Signal. 26, 461–467 (2014). - PubMed
  50. Jirawatnotai, S. et al. A function for cyclin D1 in DNA repair uncovered by protein interactome analyses in human cancers. Nature 474, 230–234 (2011). - PubMed
  51. de Kreuk, B. J. et al. The F-BAR domain protein PACSIN2 associates with Rac1 and regulates cell spreading and migration. J. Cell Sci. 124, 2375–2388 (2011). - PubMed
  52. de Kreuk, B. J., Anthony, E. C., Geerts, D. & Hordijk, P. L. The F-BAR protein PACSIN2 regulates epidermal growth factor receptor internalization. J. Biol. Chem. 287, 43438–43453 (2012). - PubMed
  53. Giridharan, S. S., Cai, B., Vitale, N., Naslavsky, N. & Caplan, S. Cooperation of MICAL-L1, syndapin2, and phosphatidic acid in tubular recycling endosome biogenesis. Mol. Biol. Cell 24, 1776–1790 (2013). S1771-1715. - PubMed
  54. Senju, Y., Itoh, Y., Takano, K., Hamada, S. & Suetsugu, S. Essential role of PACSIN2/syndapin-II in caveolae membrane sculpting. J. Cell Sci. 124, 2032–2040 (2011). - PubMed
  55. Hers, I., Vincent, E. E. & Tavare, J. M. Akt signalling in health and disease. Cell Signal. 23, 1515–1527 (2011). - PubMed
  56. Ju, X. et al. Akt1 governs breast cancer progression in vivo. Proc. Natl Acad. Sci. USA 104, 7438–7443 (2007). - PubMed
  57. Castoria, G. et al. PI3-kinase in concert with Src promotes the S-phase entry of oestradiol-stimulated MCF-7 cells. EMBO J. 20, 6050–6059 (2001). - PubMed
  58. Pedram, A., Razandi, M., Evinger, A. J., Lee, E. & Levin, E. R. Estrogen inhibits ATR signaling to cell cycle checkpoints and DNA repair. Mol. Biol. Cell 20, 3374–3389 (2009). - PubMed
  59. Bjornstrom, L. & Sjoberg, M. Mechanisms of estrogen receptor signaling: convergence of genomic and nongenomic actions on target genes. Mol. Endocrinol. 19, 833–842 (2005). - PubMed
  60. Simoncini, T. et al. Interaction of oestrogen receptor with the regulatory subunit of phosphatidylinositol-3-OH kinase. Nature 407, 538–541 (2000). - PubMed
  61. Song, R. X., Zhang, Z. & Santen, R. J. Estrogen rapid action via protein complex formation involving ERalpha and Src. Trends Endocrinol. Metab. 16, 347–353 (2005). - PubMed
  62. Levin, E. R. & Pietras, R. J. Estrogen receptors outside the nucleus in breast cancer. Breast Cancer Res. Treat. 108, 351–361 (2008). - PubMed
  63. Casimiro, M. C. et al. Cyclin D1 determines estrogen signaling in the mammary gland in vivo. Mol. Endocrinol. 27, 1415–1428 (2013). - PubMed
  64. Body, S. et al. Cytoplasmic cyclin D1 controls the migration and invasiveness of mantle lymphoma cells. Sci. Rep. 7, 13946 (2017). - PubMed
  65. Baker, G. L., Landis, M. W. & Hinds, P. W. Multiple functions of D-type cyclins can antagonize pRb-mediated suppression of proliferation. Cell Cycle 4, 330–338 (2005). - PubMed
  66. Su, L. F., Knoblauch, R. & Garabedian, M. J. Rho GTPases as modulators of the estrogen receptor transcriptional response. J. Biol. Chem. 276, 3231–3237 (2001). - PubMed
  67. Takahashi, K. et al. Estrogen induces neurite outgrowth via Rho family GTPases in neuroblastoma cells. Mol. Cell Neurosci. 48, 217–224 (2011). - PubMed
  68. Poulard, C. et al. Oestrogen non-genomic signalling is activated in tamoxifen-resistant breast cancer. Int J. Mol. Sci. 20, 2773 (2019). - PubMed
  69. Alt, J. R., Cleveland, J. L., Hannink, M. & Diehl, J. A. Phosphorylation-dependent regulation of cyclin D1 nuclear export and cyclin D1-dependent cellular transformation. Genes Dev. 14, 3102–3114 (2000). - PubMed
  70. Gladden, A. B., Woolery, R., Aggarwal, P., Wasik, M. A. & Diehl, J. A. Expression of constitutively nuclear cyclin D1 in murine lymphocytes induces B-cell lymphoma. Oncogene 25, 998–1007 (2006). - PubMed
  71. Lin, D. I. et al. Disruption of cyclin D1 nuclear export and proteolysis accelerates mammary carcinogenesis. Oncogene 27, 1231–1242 (2008). - PubMed
  72. Brown, J. R. et al. Fos family members induce cell cycle entry by activating cyclin D1. Mol. Cell Biol. 18, 5609–5619 (1998). - PubMed
  73. Soderberg, O. et al. Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat. Methods 3, 995–1000 (2006). - PubMed
  74. Poulard, C. et al. Activation of rapid oestrogen signalling in aggressive human breast cancers. EMBO Mol. Med. 4, 1200–1213 (2012). - PubMed
  75. Poulard, C., Rambaud, J., Le Romancer, M. & Corbo, L. Proximity ligation assay to detect and localize the interactions of ERalpha with PI3-K and Src in breast cancer cells and tumor samples. Methods Mol. Biol. 1204, 135–143 (2014). - PubMed
  76. Albanese, C. et al. Activation of the cyclin D1 gene by the E1A-associated protein p300 through AP-1 inhibits cellular apoptosis. J. Biol. Chem. 274, 34186–34195 (1999). - PubMed
  77. Jiao, X. et al. Disruption of c-Jun reduces cellular migration and invasion through inhibition of c-Src and hyperactivation of ROCK II kinase. Mol. Biol. Cell 19, 1378–1390 (2008). - PubMed
  78. Lam, A. J. et al. Improving FRET dynamic range with bright green and red fluorescent proteins. Nat. Methods 9, 1005–1012 (2012). - PubMed
  79. Yoshizaki, H. et al. Activity of Rho-family GTPases during cell division as visualized with FRET-based probes. J. Cell Biol. 162, 223–232 (2003). - PubMed
  80. Jiao, X., Zhang, N., Xu, X., Oppenheim, J. J. & Jin, T. Ligand-induced partitioning of human CXCR1 chemokine receptors with lipid raft microenvironments facilitates G-protein-dependent signaling. Mol. Cell Biol. 25, 5752–5762 (2005). - PubMed
  81. Jiao, X. et al. CCR5 governs DNA damage repair and breast cancer stem cell expansion. Cancer Res. 78, 1657–1671 (2018). - PubMed
  82. Peck, A. R. et al. Validation of tumor protein marker quantification by two independent automated immunofluorescence image analysis platforms. Mod. Pathol. 29, 1143–1154 (2016). - PubMed
  83. Pestell, T. G. et al. Stromal cyclin D1 promotes heterotypic immune signaling and breast cancer growth. Oncotarget 8, 81754–81775 (2017). - PubMed

Publication Types

Grant support