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International Journal of Cell Biology
Volume 2014, Article ID 308535, 10 pages
http://dx.doi.org/10.1155/2014/308535
Review Article

Small G Proteins Dexras1 and RHES and Their Role in Pathophysiological Processes

Department of Biotechnology, Graphic Era University, Dehradun, Uttarakhand 248002, India

Received 25 October 2013; Accepted 18 February 2014; Published 20 March 2014

Academic Editor: J. R. Davie

Copyright © 2014 Ashish Thapliyal et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. D. S. Goodsell, “The molecular perspective: the ras oncogene,” The Oncologist, vol. 4, no. 3, pp. 263–264, 1999. View at Google Scholar · View at Scopus
  2. J. L. Bos, “Ras oncogenes in human cancer: a review,” Cancer Research, vol. 49, no. 17, pp. 4682–4689, 1989. View at Google Scholar · View at Scopus
  3. K. Wennerberg, K. L. Rossman, and C. J. Der, “The Ras superfamily at a glance,” Journal of Cell Science, vol. 118, part 5, pp. 843–846, 2005. View at Publisher · View at Google Scholar · View at Scopus
  4. R. J. Kemppainen and E. N. Behrend, “Dexamethasone rapidly induces a novel ras superfamily member-related gene in AtT-20 cells,” Journal of Biological Chemistry, vol. 273, no. 6, pp. 3129–3131, 1998. View at Publisher · View at Google Scholar · View at Scopus
  5. P. Agretti, G. de Marco, A. Pinchera, P. Vitti, J. Bernal, and M. Tonacchera, “Ras homolog enriched in striatum inhibits the functional activity of wild type thyrotropin, follicle-stimulating hormone, luteinizing hormone receptors and activating thyrotropin receptor mutations by altering their expression in COS-7 cells,” Journal of Endocrinological Investigation, vol. 30, no. 4, pp. 279–284, 2007. View at Google Scholar · View at Scopus
  6. P. Vargiu, B. Morte, J. Manzano et al., “Thyroid hormone regulation of rhes, a novel Ras homolog gene expressed in the striatum,” Molecular Brain Research, vol. 94, no. 1-2, pp. 1–8, 2001. View at Publisher · View at Google Scholar · View at Scopus
  7. J. Bernal and A. Guadaño-Ferraz, “Thyroid hormone and the development of the brain,” Current Opinion in Endocrinology and Diabetes, vol. 5, no. 4, pp. 296–302, 1998. View at Google Scholar · View at Scopus
  8. P. Vargiu, R. de Abajo, J. A. Garcia-Ranea et al., “The small GTP-binding protein, Rhes, regulates signal transduction from G protein-coupled receptors,” Oncogene, vol. 23, no. 2, pp. 559–568, 2004. View at Publisher · View at Google Scholar · View at Scopus
  9. T. E. Graham, T. A. Key, K. Kilpatrick, and R. I. Dorin, “Dexras1/AGS-1, a steroid hormone-induced guanosine triphosphate-binding protein, inhibits 3′,5′-cyclic adenosine monophosphate-stimulated secretion in AtT-20 corticotroph cells,” Endocrinology, vol. 142, no. 6, pp. 2631–2640, 2001. View at Publisher · View at Google Scholar · View at Scopus
  10. A. Thapliyal, R. A. Bannister, C. Hanks, and B. A. Adams, “The monomeric G proteins AGS1 and Rhes selectively influence Gαi-dependent signaling to modulate N-type (CaV2.2) calcium channels,” American Journal of Physiology—Cell Physiology, vol. 295, no. 5, pp. C1417–C1426, 2008. View at Publisher · View at Google Scholar · View at Scopus
  11. G. F. Ball and J. Balthazart, “Hormonal regulation of brain circuits mediating male sexual behavior in birds,” Physiology & Behavior, vol. 83, no. 2, pp. 329–346, 2004. View at Publisher · View at Google Scholar · View at Scopus
  12. M. F. McGrath, T. Ogawa, and A. J. de Bold, “Ras dexamethasone-induced protein 1 is a modulator of hormone secretion in the volume overloaded heart,” American Journal of Physiology—Heart and Circulatory Physiology, vol. 302, no. 9, pp. H1826–H1837, 2012. View at Publisher · View at Google Scholar · View at Scopus
  13. S. Subramaniam and S. H. Snyder, “Huntington's disease is a disorder of the corpus striatum: focus on Rhes (Ras homologue enriched in the striatum),” Neuropharmacology, vol. 60, no. 7-8, pp. 1187–1192, 2011. View at Publisher · View at Google Scholar · View at Scopus
  14. G. Vaidyanathan, M. J. Cismowski, G. Wang, T. S. Vincent, K. D. Brown, and S. M. Lanier, “The Ras-related protein AGS1/RASD1 suppresses cell growth,” Oncogene, vol. 23, no. 34, pp. 5858–5863, 2004. View at Publisher · View at Google Scholar · View at Scopus
  15. B. St. Croix, C. Rago, V. Velculescu et al., “Genes expressed in human tumor endothelium,” Science, vol. 289, no. 5482, pp. 1197–1202, 2000. View at Publisher · View at Google Scholar · View at Scopus
  16. J. Bernal and P. Crespo, “Analysis of Rhes activation state and effector function,” Methods in Enzymology, vol. 407, pp. 535–542, 2005. View at Publisher · View at Google Scholar · View at Scopus
  17. Y. Tu and C. Wu, “Cloning, expression and characterization of a novel human Ras-related protein that is regulated by glucocorticoid hormone,” Biochimica et Biophysica Acta—Gene Structure and Expression, vol. 1489, no. 2-3, pp. 452–456, 1999. View at Publisher · View at Google Scholar · View at Scopus
  18. R. J. Kemppainen, E. Cox, E. N. Behrend, M. D. Brogan, and J. M. Ammons, “Identification of a glucocorticoid response element in the 3′-flanking region of the human Dexras1 gene,” Biochimica et Biophysica Acta—Gene Structure and Expression, vol. 1627, no. 2-3, pp. 85–89, 2003. View at Publisher · View at Google Scholar · View at Scopus
  19. M. Fang, S. R. Jaffrey, A. Sawa, K. Ye, X. Luo, and S. H. Snyder, “Dexras1: a G protein specifically coupled to neuronal nitric oxide synthase via CAPON,” Neuron, vol. 28, no. 1, pp. 183–193, 2000. View at Google Scholar · View at Scopus
  20. S. M. Lanier, A. M. Struckhoff, and M. J. Cismowski, “Ags1,” UCSD Nature Molecule Pages, 2007. View at Publisher · View at Google Scholar
  21. H. R. Bourne, D. A. Sanders, and F. McCormick, “The GTPase superfamily: a conserved switch for diverse cell functions,” Nature, vol. 348, no. 6297, pp. 125–132, 1990. View at Publisher · View at Google Scholar · View at Scopus
  22. H. R. Bourne, D. A. Sanders, and F. McCormick, “The GTPase superfamily: conserved structure and molecular mechanism,” Nature, vol. 349, no. 6305, pp. 117–127, 1991. View at Publisher · View at Google Scholar · View at Scopus
  23. P. F. W. Stouten, C. Sander, A. Wittinghofer, and A. Valencia, “How does the switch II region of G-domains work?” FEBS Letters, vol. 320, no. 1, pp. 1–6, 1993. View at Publisher · View at Google Scholar · View at Scopus
  24. A. Valencia, P. Chardin, A. Wittinghofer, and C. Sander, “The ras protein family: evolutionary tree and role of conserved amino acids,” Biochemistry, vol. 30, no. 19, pp. 4637–4648, 1991. View at Google Scholar · View at Scopus
  25. K. del Villar, D. Dorin, I. Sattler et al., “C-terminal motifs found in Ras-superfamily G-proteins: CAAX and C-seven motifs,” Biochemical Society Transactions, vol. 24, no. 3, pp. 709–713, 1996. View at Google Scholar · View at Scopus
  26. P. J. Casey and M. C. Seabra, “Protein prenyltransferases,” Journal of Biological Chemistry, vol. 271, no. 10, pp. 5289–5292, 1996. View at Publisher · View at Google Scholar · View at Scopus
  27. M. J. Cismowski, C. Ma, C. Ribas et al., “Activation of heterotrimeric G-protein signaling by a Ras-related protein: implications for signal integration,” The Journal of Biological Chemistry, vol. 275, no. 31, pp. 23421–23424, 2000. View at Publisher · View at Google Scholar · View at Scopus
  28. T. E. Graham, E. R. Prossnitz, and R. I. Dorin, “Dexras1/AGS-1 inhibits signal transduction from the Gi-coupled formyl peptide receptor to Erk-1/2 MAP kinases,” The Journal of Biological Chemistry, vol. 277, no. 13, pp. 10876–10882, 2002. View at Publisher · View at Google Scholar · View at Scopus
  29. T. E. Graham, Z. Qiao, and R. I. Dorin, “Dexras1 inhibits adenylyl cyclase,” Biochemical and Biophysical Research Communications, vol. 316, no. 2, pp. 307–312, 2004. View at Publisher · View at Google Scholar · View at Scopus
  30. A. Takesono, M. W. Nowak, M. Cismowski, E. Duzic, and S. M. Lanier, “Activator of G-protein signaling 1 blocks GIRK channel activation by a G-protein-coupled receptor: apparent disruption of receptor signaling complexes,” The Journal of Biological Chemistry, vol. 277, no. 16, pp. 13827–13830, 2002. View at Publisher · View at Google Scholar · View at Scopus
  31. C. H. Nguyen and V. J. Watts, “Dexamethasone-induced Ras protein 1 negatively regulates protein kinase C δ: implications for adenylyl cyclase 2 signaling,” Molecular Pharmacology, vol. 69, no. 5, pp. 1763–1771, 2006. View at Publisher · View at Google Scholar · View at Scopus
  32. C. H. Nguyen and V. J. Watts, “Dexras1 blocks receptor-mediated heterologous sensitization of adenylyl cyclase 1,” Biochemical and Biophysical Research Communications, vol. 332, no. 3, pp. 913–920, 2005. View at Publisher · View at Google Scholar · View at Scopus
  33. J. D. Falk, P. Vargiu, P. E. Foye et al., “Rhes: a striatal-specific Ras homolog related to Dexras1,” Journal of Neuroscience Research, vol. 57, no. 6, pp. 782–788, 1999. View at Google Scholar
  34. D. Spano, I. Branchi, A. Rosica et al., “Rhes is involved in striatal function,” Molecular and Cellular Biology, vol. 24, no. 13, pp. 5788–5796, 2004. View at Publisher · View at Google Scholar · View at Scopus
  35. S. L. F. Chan, L. K. Monks, H. Gao, P. Deaville, and N. G. Morgan, “Identification of the monomeric G-protein, Rhes, as an efaroxan-regulated protein in the pancreatic β-cell,” British Journal of Pharmacology, vol. 136, no. 1, pp. 31–36, 2002. View at Google Scholar · View at Scopus
  36. S. C. Boyages and J.-P. Halpern, “Endemic cretinism: toward a unifying hypothesis,” Thyroid, vol. 3, no. 1, pp. 59–69, 1993. View at Google Scholar · View at Scopus
  37. G. R. DeLong, J. B. Stanbury, and R. Fierro-Benitez, “Neurological signs in congenital iodine-deficiency disorder (endemic cretinism),” Developmental Medicine and Child Neurology, vol. 27, no. 3, pp. 317–324, 1985. View at Google Scholar · View at Scopus
  38. T. Ma, Z. C. Lian, S. P. Qi, E. R. Heinz, and G. R. DeLong, “Magnetic resonance imaging of brain and the neuromotor disorder in endemic cretinism,” Annals of Neurology, vol. 34, no. 1, pp. 91–94, 1993. View at Google Scholar · View at Scopus
  39. H.-Y. M. Cheng and K. Obrietan, “Dexras1: shaping the responsiveness of the circadian clock,” Seminars in Cell and Developmental Biology, vol. 17, no. 3, pp. 345–351, 2006. View at Publisher · View at Google Scholar · View at Scopus
  40. C. Hill, A. Goddard, G. Ladds, and J. Davey, “The cationic region of Rhes mediates its interactions with specific Gβ subunits,” Cellular Physiology and Biochemistry, vol. 23, no. 1–3, pp. 1–8, 2009. View at Publisher · View at Google Scholar · View at Scopus
  41. C. Lellis-Santos, L. H. Sakamoto, C. R. Bromati et al., “The regulation of rasd1 expression by glucocorticoids and prolactin controls peri-partum-maternal insulin secretion,” Endocrinology, vol. 153, no. 8, pp. 3668–3678, 2012. View at Publisher · View at Google Scholar
  42. J. Manzano, B. Morte, T. S. Scanlan, and J. Bernal, “Differential effects of triiodothyronine and the thyroid hormone receptor β-specific agonist GC-1 on thyroid hormone target genes in the brain,” Endocrinology, vol. 144, no. 12, pp. 5480–5487, 2003. View at Publisher · View at Google Scholar · View at Scopus
  43. J. Vallortigara, S. Alfos, J. Micheau, P. Higueret, and V. Enderlin, “T3 administration in adult hypothyroid mice modulates expression of proteins involved in striatal synaptic plasticity and improves motor behavior,” Neurobiology of Disease, vol. 31, no. 3, pp. 378–385, 2008. View at Publisher · View at Google Scholar · View at Scopus
  44. J. Narayana and T. E. Porter, “Effects of chicken dexamethasone-induced Ras-related 1(cDexras1) on growth hormone (GH) gene expression in embryonic pituitary cells,” 2009, College Park, Md, USA, University of Maryland.
  45. S. Subramaniam, R. G. Mealer, K. M. Sixt, R. K. Barrow, A. Usiello, and S. H. Snyder, “Rhes, a physiologic regulator of sumoylation, enhances cross-sumoylation between the basic sumoylation enzymes E1 and Ubc9,” The Journal of Biological Chemistry, vol. 285, no. 27, pp. 20428–20432, 2010. View at Publisher · View at Google Scholar · View at Scopus
  46. S. Subramaniam, K. M. Sixt, R. Barrow, and S. H. Snyder, “Rhes, a striatal specific protein, mediates mutant-huntingtin cytotoxicity,” Science, vol. 324, no. 5932, pp. 1327–1330, 2009. View at Publisher · View at Google Scholar · View at Scopus
  47. L. M. Harrison, “Rhes: a GTP-binding protein integral to striatal physiology and pathology,” Cellular and Molecular Neurobiology, vol. 32, no. 6, pp. 907–918, 2012. View at Publisher · View at Google Scholar · View at Scopus
  48. H.-Y. M. Cheng, K. Obrietan, S. W. Cain et al., “Dexras1 potentiates photic and suppresses nonphotic responses of the circadian clock,” Neuron, vol. 43, no. 5, pp. 715–728, 2004. View at Publisher · View at Google Scholar · View at Scopus
  49. J. R. Gerstner, W. M. Vander Heyden, T. M. LaVaute, and C. F. Landry, “Profiles of novel diurnally regulated genes in mouse hypothalamus: expression analysis of the cysteine and histidine-rich domain-containing, zinc-binding protein 1, the fatty acid-binding protein 7 and the GTPase, ras-like family member 11b,” Neuroscience, vol. 139, no. 4, pp. 1435–1448, 2006. View at Publisher · View at Google Scholar · View at Scopus
  50. H. Takahashi, N. Umeda, Y. Tsutsumi et al., “Mouse dexamethasone-induced RAS protein 1 gene is expressed in a circadian rhythmic manner in the suprachiasmatic nucleus,” Molecular Brain Research, vol. 110, no. 1, pp. 1–6, 2003. View at Publisher · View at Google Scholar · View at Scopus
  51. A. Chandola-Saklani, A. Thapliyal, K. Negi, S. C. Diyundi, and B. Choudhary, “Daily increments of light hours near vernal equinox synchronize circannual testicular cycle of tropical spotted munia,” Chronobiology International, vol. 21, no. 4-5, pp. 553–569, 2004. View at Publisher · View at Google Scholar · View at Scopus
  52. A. Chandola and V. K. Pathak, “Restricted food intake and annual thyroid cycle of spotted munia,” General and Comparative Endocrinology, vol. 42, no. 1, pp. 39–46, 1980. View at Google Scholar · View at Scopus
  53. P. Bouchard-Cannon and H. M. Cheng, “Scheduled feeding alters the timing of the suprachiasmatic nucleus circadian clock in Dexras1-deficient mice,” Chronobiology International, vol. 29, no. 8, pp. 965–981, 2012. View at Publisher · View at Google Scholar
  54. R. Dubruille and P. Emery, “A plastic clock: how circadian rhythms respond to environmental cues in drosophila,” Molecular Neurobiology, vol. 38, no. 2, pp. 129–145, 2008. View at Publisher · View at Google Scholar · View at Scopus
  55. C. Helfrich-Förster, C. Winter, A. Hofbauer, J. C. Hall, and R. Stanewsky, “The circadian clock of fruit flies is blind after elimination of all known photoreceptors,” Neuron, vol. 30, no. 1, pp. 249–261, 2001. View at Publisher · View at Google Scholar · View at Scopus
  56. S. Hattar, R. J. Lucas, N. Mrosovsky et al., “Melanopsin and rod-cone photoreceptive systems account for all major accessory visual functions in mice,” Nature, vol. 424, no. 6944, pp. 76–81, 2003. View at Google Scholar · View at Scopus
  57. S. Panda, I. Provencio, D. C. Tu et al., “Melanopsin is required for non-image-forming photic responses in blind mice,” Science, vol. 301, no. 5632, pp. 525–527, 2003. View at Publisher · View at Google Scholar · View at Scopus
  58. P. V. Agostino, M. E. Harrington, M. R. Ralph, and D. A. Golombek, “Casein kinase-1-epsilon (CK1ε) and circadian photic responses in hamsters,” Chronobiology International, vol. 26, no. 1, pp. 126–133, 2009. View at Publisher · View at Google Scholar · View at Scopus
  59. M. D. Brogan, E. N. Behrend, and R. J. Kemppainen, “Regulation of Dexras1 expression by endogenous steroids,” Neuroendocrinology, vol. 74, no. 4, pp. 244–250, 2001. View at Publisher · View at Google Scholar · View at Scopus
  60. R. Dallmann and N. Mrosovsky, “Non-photic phase resetting of Dexras1 deficient mice: a more complicated story,” Behavioural Brain Research, vol. 180, no. 2, pp. 197–202, 2007. View at Publisher · View at Google Scholar · View at Scopus
  61. X. Li, C. Cheng, M. Fei et al., “Spatiotemporal expression of Dexras1 after spinal cord transection in rats,” Cellular and Molecular Neurobiology, vol. 28, no. 3, pp. 371–388, 2008. View at Publisher · View at Google Scholar · View at Scopus
  62. A. Shen, M. Chen, S. Niu et al., “Changes in mRNA for CAPON and Dexras1 in adult rat following sciatic nerve transection,” Journal of Chemical Neuroanatomy, vol. 35, no. 1, pp. 85–93, 2008. View at Publisher · View at Google Scholar · View at Scopus
  63. H.-Y. M. Cheng, H. Dziema, J. Papp et al., “The molecular gatekeeper Dexras1 sculpts the photic responsiveness of the mammalian circadian clock,” The Journal of Neuroscience, vol. 26, no. 50, pp. 12984–12995, 2006. View at Publisher · View at Google Scholar · View at Scopus
  64. M. J. Cismowski, A. Takesono, C. Ma et al., “Genetic screens in yeast to identify mammalian nonreceptor modulators of G-protein signaling,” Nature Biotechnology, vol. 17, no. 9, pp. 878–883, 1999. View at Publisher · View at Google Scholar · View at Scopus
  65. S. R. Jaffrey, A. M. Snowman, M. J. L. Eliasson, N. A. Cohen, and S. H. Snyder, “CAPON: a protein associated with neuronal nitric oxide synthase that regulates its interactions with PSD95,” Neuron, vol. 20, no. 1, pp. 115–124, 1998. View at Publisher · View at Google Scholar · View at Scopus
  66. S. A. Ong, J. J. Tan, W. L. Tew, and K.-S. Chen, “Rasd1 modulates the coactivator function of NonO in the cyclic AMP pathway,” PLoS ONE, vol. 6, no. 9, Article ID e24401, 2011. View at Publisher · View at Google Scholar · View at Scopus
  67. Y.-S. Yang, J. H. Hanke, L. Carayannopoulos, C. M. Craft, J. D. Capra, and P. W. Tucker, “NonO, a non-POU-domain-containing, octamer-binding protein, is the mammalian homolog of Drosophila nonAdiss,” Molecular and Cellular Biology, vol. 13, no. 9, pp. 5593–5603, 1993. View at Google Scholar · View at Scopus
  68. M. Mathur, P. W. Tucker, and H. H. Samuels, “PSF is a novel corepressor that mediates its effect through Sin3A and the DNA binding domain of nuclear hormone receptors,” Molecular and Cellular Biology, vol. 21, no. 7, pp. 2298–2311, 2001. View at Publisher · View at Google Scholar · View at Scopus
  69. A. L. Amelio, L. J. Miraglia, J. J. Conkright et al., “A coactivator trap identifies NONO (p54nrb) as a component of the cAMP-signaling pathway,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 51, pp. 20314–20319, 2007. View at Publisher · View at Google Scholar · View at Scopus
  70. M. B. Sewer, V. Q. Nguyen, C.-J. Huang, P. W. Tucker, N. Kagawa, and M. R. Waterman, “Transcriptional activation of human CYP17 in H295R adrenocortical cells depends on complex formation among p54nrb/NonO, protein-associated splicing factor, and SF-1, a complex that also participates in repression of transcription,” Endocrinology, vol. 143, no. 4, pp. 1280–1290, 2002. View at Publisher · View at Google Scholar · View at Scopus
  71. C. Zhang, M.-X. Zhang, Y. H. Shen et al., “Role of NonO-histone interaction in TNFα-suppressed Prolyl-4-hydroxylase α1,” Biochimica et Biophysica Acta—Molecular Cell Research, vol. 1783, no. 8, pp. 1517–1528, 2008. View at Publisher · View at Google Scholar · View at Scopus
  72. C. D. Boethel, “Sleep and the endocrine system: new associations to old diseases,” Current Opinion in Pulmonary Medicine, vol. 8, no. 6, pp. 502–505, 2002. View at Publisher · View at Google Scholar · View at Scopus
  73. F. W. Turek, C. Joshu, A. Kohsaka et al., “Obesity and metabolic syndrome in circadian clock mutant nice,” Science, vol. 308, no. 5724, pp. 1043–1045, 2005. View at Publisher · View at Google Scholar · View at Scopus
  74. J. Hansen, “Light at night, shiftwork, and breast cancer risk,” Journal of the National Cancer Institute, vol. 93, no. 20, pp. 1513–1515, 2001. View at Google Scholar · View at Scopus
  75. D. E. Blask, “Melatonin, sleep disturbance and cancer risk,” Sleep Medicine Reviews, vol. 13, no. 4, pp. 257–264, 2009. View at Publisher · View at Google Scholar · View at Scopus
  76. G. C. Quintero, D. Spano, G. J. LaHoste, and L. M. Harrison, “The Ras homolog Rhes affects dopamine D1 and D2 receptor-mediated behavior in mice,” NeuroReport, vol. 19, no. 16, pp. 1563–1566, 2008. View at Publisher · View at Google Scholar · View at Scopus
  77. G. C. Quintero and D. Spano, “Exploration of sex differences in Rhes effects in dopamine mediated behaviors,” Neuropsychiatric Disease and Treatment, vol. 7, no. 1, pp. 697–706, 2011. View at Google Scholar · View at Scopus
  78. L. M. Harrison and Y. He, “Rhes and AGS1/Dexras1 affect signaling by dopamine D1 receptors through adenylyl cyclase,” Journal of Neuroscience Research, vol. 89, no. 6, pp. 874–882, 2011. View at Publisher · View at Google Scholar · View at Scopus
  79. M. Schwendt and J. F. McGinty, “Amphetamine up-regulates AGS1 mRNA and protein levels in rat frontal cortex: the role of dopamine and glucocorticoid receptors,” Neuroscience, vol. 168, no. 1, pp. 96–107, 2010. View at Publisher · View at Google Scholar · View at Scopus
  80. M. L. Hard, M. Abdolell, B. H. Robinson, and G. Koren, “Gene-expression analysis after alcohol exposure in the developing mouse,” Journal of Laboratory and Clinical Medicine, vol. 145, no. 1, pp. 47–54, 2005. View at Publisher · View at Google Scholar · View at Scopus
  81. J. Tian, Y. X. Duan, C. Y. Bei, and J. Chen, “Calycosin induces apoptosis by upregulation of RASD1 in human breast cancer cells MCF-7,” Hormone and Metabolic Research, vol. 45, no. 8, pp. 593–598, 2013. View at Publisher · View at Google Scholar