Inducible knockout of twist1 in young and adult mice prolongs hair growth cycle and has mild effects on general health, supporting twist1 as a preferential cancer target

American Journal of Pathology

Volumn 183, Issue 4, 2013, Pages 1281-1292

  Xu, Yan ^a,b   Xu, Yixiang ^a,c   Liao, Lan ^a   Zhou, Niya ^a   Theissen, Sarah M ^a   Liao, Xin Hua ^a   Nguyen, Hoang ^d   Ludwig, Thomas ^a   Qin, Li ^a   Martinez, Jarrod D ^b   Jiang, Jun ^a   Xu, Jianming ^a,e  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b THIRD MILITARY MEDICAL UNIVERSITY   (China)

^c UNIVERSITY OF TEXAS   (United States)

^d THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

^e SOUTHWEST MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

TAMOXIFEN; TRANSCRIPTION FACTOR; TWIST1 PROTEIN; UNCLASSIFIED DRUG; VIMENTIN;

ADULT ANIMAL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD PRESSURE; CONTROLLED STUDY; FEMALE; GENE DELETION; GENE EXPRESSION; GENE INACTIVATION; GENE TARGETING; HAIR FOLLICLE; HAIR GROWTH; HEART RATE; JUVENILE ANIMAL; MALE; MAMMARY GLAND; MORPHOGENESIS; MOUSE; NEOPLASM; NONHUMAN; PRIORITY JOURNAL; WEIGHT GAIN;

AGING; ANIMALS; FEMALE; HAIR FOLLICLE; HEALTH; MALE; MAMMARY GLANDS, ANIMAL; MICE; MICE, KNOCKOUT; MORPHOGENESIS; NEOPLASMS; NUCLEAR PROTEINS; ORGAN SPECIFICITY; TWIST TRANSCRIPTION FACTOR;

EID: 84884562451     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2013.06.021     Document Type: Article

References (70)

1. B. Thisse, M. el Messal, and F. Perrin-Schmitt The twist gene: isolation of a Drosophila zygotic gene necessary for the establishment of dorsoventral pattern Nucleic Acids Res 15 1987 3439 3453
2. Q. Qin, Y. Xu, T. He, C. Qin, and J. Xu Normal and disease-related biological functions of Twist1 and underlying molecular mechanisms Cell Res 22 2012 90 106
3. Y.N. Jan, and L.Y. Jan HLH proteins, fly neurogenesis, and vertebrate myogenesis Cell 75 1993 827 830
4. C. Wolf, C. Thisse, C. Stoetzel, B. Thisse, P. Gerlinger, and F. Perrin-Schmitt The M-twist gene of Mus is expressed in subsets of mesodermal cells and is closely related to the Xenopus X-twi and the Drosophila twist genes Dev Biol 143 1991 363 373
5. E.M. Füchtbauer Expression of M-twist during postimplantation development of the mouse Dev Dyn 204 1995 316 322
6. C. Stoetzel, B. Weber, P. Bourgeois, A.L. Bolcato-Bellemin, and F. Perrin-Schmitt Dorso-ventral and rostro-caudal sequential expression of M-twist in the postimplantation murine embryo Mech Dev 51 1995 251 263
7. I. Gitelman Twist protein in mouse embryogenesis Dev Biol 189 1997 205 214
8. N. Figeac, M. Daczewska, C. Marcelle, and K. Jagla Muscle stem cells and model systems for their investigation Dev Dyn 236 2007 3332 3342
9. P. Zhao, and E.P. Hoffman Embryonic myogenesis pathways in muscle regeneration Dev Dyn 229 2004 380 392
10. S.S. Murray, C.A. Glackin, K.A. Winters, D. Gazit, A.J. Kahn, and E.J. Murray Expression of helix-loop-helix regulatory genes during differentiation of mouse osteoblastic cells J Bone Miner Res 7 1992 1131 1138
11. D. Pan, M. Fujimoto, A. Lopes, and Y.X. Wang Twist-1 is a PPARdelta-inducible, negative-feedback regulator of PGC-1alpha in brown fat metabolism Cell 137 2009 73 86
12. A.T. Pettersson, J. Laurencikiene, N. Mejhert, E. Näslund, A. Bouloumié, I. Dahlman, P. Arner, and M. Rydén A possible inflammatory role of twist1 in human white adipocytes Diabetes 59 2010 564 571
13. W. Reardon, and R.M. Winter Saethre-Chotzen syndrome J Med Genet 31 1994 393 396
14. V. el Ghouzzi, M. Le Merrer, F. Perrin-Schmitt, E. Lajeunie, P. Benit, D. Renier, P. Bourgeois, A.L. Bolcato-Bellemin, A. Munnich, and J. Bonaventure Mutations of the TWIST gene in the Saethre-Chotzen syndrome Nat Genet 15 1997 42 46
15. I. Krebs, I. Weis, M. Hudler, J.M. Rommens, H. Roth, S.W. Scherer, L.C. Tsui, E.M. Füchtbauer, K.H. Grzeschik, K. Tsuji, and J. Kunz Translocation breakpoint maps 5 kb 3′ from TWIST in a patient affected with Saethre-Chotzen syndrome Hum Mol Genet 6 1997 1079 1086
16. K.W. Gripp, E.H. Zackai, and C.A. Stolle Mutations in the human TWIST gene [Erratum appeared in Hum Mutat 2000, 15:479] Hum Mutat 15 2000 150 155
17. C.S. Rose, P. Patel, W. Reardon, S. Malcolm, and R.M. Winter The TWIST gene, although not disrupted in Saethre-Chotzen patients with apparently balanced translocations of 7p21, is mutated in familial and sporadic cases Hum Mol Genet 6 1997 1369 1373
18. T.D. Howard, W.A. Paznekas, E.D. Green, L.C. Chiang, N. Ma, R.I. Ortiz de Luna, C. Garcia Delgado, M. Gonzalez-Ramos, A.D. Kline, and E.W. Jabs Mutations in TWIST, a basic helix-loop-helix transcription factor, in Saethre-Chotzen syndrome Nat Genet 15 1997 36 41
19. Z.F. Chen, and R.R. Behringer Twist is required in head mesenchyme for cranial neural tube morphogenesis Genes Dev 9 1995 686 699
20. P. Bourgeois, A.L. Bolcato-Bellemin, J.M. Danse, A. Bloch-Zupan, K. Yoshiba, C. Stoetzel, and F. Perrin-Schmitt The variable expressivity and incomplete penetrance of the twist-null heterozygous mouse phenotype resemble those of human Saethre-Chotzen syndrome Hum Mol Genet 7 1998 945 957
21. P. Bialek, B. Kern, X. Yang, M. Schrock, D. Sosic, N. Hong, H. Wu, K. Yu, D.M. Ornitz, E.N. Olson, M.J. Justice, and G. Karsenty A twist code determines the onset of osteoblast differentiation Dev Cell 6 2004 423 435
22. K. Soo, M.P. O'Rourke, P.L. Khoo, K.A. Steiner, N. Wong, R.R. Behringer, and P.P. Tam Twist function is required for the morphogenesis of the cephalic neural tube and the differentiation of the cranial neural crest cells in the mouse embryo Dev Biol 247 2002 251 270
23. J. Yang, S.A. Mani, J.L. Donaher, S. Ramaswamy, R.A. Itzykson, C. Come, P. Savagner, I. Gitelman, A. Richardson, and R.A. Weinberg Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis Cell 117 2004 927 939
24. W.K. Kwok, M.T. Ling, T.W. Lee, T.C. Lau, C. Zhou, X. Zhang, C.W. Chua, K.W. Chan, F.L. Chan, C. Glackin, Y.C. Wong, and X. Wang Up-regulation of TWIST in prostate cancer and its implication as a therapeutic target Cancer Res 65 2005 5153 5162
25. H.F. Yuen, C.W. Chua, Y.P. Chan, Y.C. Wong, X. Wang, and K.W. Chan Significance of TWIST and E-cadherin expression in the metastatic progression of prostatic cancer Histopathology 50 2007 648 658
26. G.Q. Luo, J.H. Li, J.F. Wen, Y.H. Zhou, Y.B. Hu, and J.H. Zhou Effect and mechanism of the Twist gene on invasion and metastasis of gastric carcinoma cells World J Gastroenterol 14 2008 2487 2493
27. M.Y. Feng, K. Wang, H.T. Song, H.W. Yu, Y. Qin, Q.T. Shi, and J.S. Geng Metastasis-induction and apoptosis-protection by TWIST in gastric cancer cells Clin Exp Metastasis 26 2009 1013 1023
28. T.K. Lee, R.T. Poon, A.P. Yuen, M.T. Ling, W.K. Kwok, X.H. Wang, Y.C. Wong, X.Y. Guan, K. Man, K.L. Chau, and S.T. Fan Twist overexpression correlates with hepatocellular carcinoma metastasis through induction of epithelial-mesenchymal transition Clin Cancer Res 12 2006 5369 5376
29. M.H. Yang, C.L. Chen, G.Y. Chau, S.H. Chiou, C.W. Su, T.Y. Chou, W.L. Peng, and J.C. Wu Comprehensive analysis of the independent effect of Twist and Snail in promoting metastasis of hepatocellular carcinoma Hepatology 50 2009 1464 1474
30. Z. Zhang, D. Xie, X. Li, Y.C. Wong, D. Xin, X.Y. Guan, C.W. Chua, S.C. Leung, Y. Na, and X. Wang Significance of TWIST expression and its association with E-cadherin in bladder cancer Hum Pathol 38 2007 598 606
31. H. Wallerand, G. Robert, G. Pasticier, A. Ravaud, P. Ballanger, R.E. Reiter, and J.M. Ferrière The epithelial-mesenchymal transition-inducing factor TWIST is an attractive target in advanced and/or metastatic bladder and prostate cancers Urol Oncol 28 2010 473 479
32. K. Sasaki, S. Natsugoe, S. Ishigami, M. Matsumoto, H. Okumura, T. Setoyama, Y. Uchikado, Y. Kita, K. Tamotsu, A. Sakamoto, T. Owaki, and T. Aikou Significance of Twist expression and its association with E-cadherin in esophageal squamous cell carcinoma J Exp Clin Cancer Res 28 2009 158
33. H.F. Yuen, Y.P. Chan, M.L. Wong, W.K. Kwok, K.K. Chan, P.Y. Lee, G. Srivastava, S.Y. Law, Y.C. Wong, X. Wang, and K.W. Chan Upregulation of Twist in oesophageal squamous cell carcinoma is associated with neoplastic transformation and distant metastasis J Clin Pathol 60 2007 510 514
34. K. Satoh, S. Hamada, K. Kimura, A. Kanno, M. Hirota, J. Umino, W. Fujibuchi, A. Masamune, N. Tanaka, K. Miura, S. Egawa, F. Motoi, M. Unno, B.K. Vonderhaar, and T. Shimosegawa Up-regulation of MSX2 enhances the malignant phenotype and is associated with twist 1 expression in human pancreatic cancer cells Am J Pathol 172 2008 926 939
35. R. Maestro, A.P. Dei Tos, Y. Hamamori, S. Krasnokutsky, V. Sartorelli, L. Kedes, C. Doglioni, D.H. Beach, and G.J. Hannon Twist is a potential oncogene that inhibits apoptosis Genes Dev 13 1999 2207 2217
36. S. Valsesia-Wittmann, M. Magdeleine, S. Dupasquier, E. Garin, A.C. Jallas, V. Combaret, A. Krause, P. Leissner, and A. Puisieux Oncogenic cooperation between H-Twist and N-Myc overrides failsafe programs in cancer cells Cancer Cell 6 2004 625 630
37. S. Ansieau, J. Bastid, A. Doreau, A.P. Morel, B.P. Bouchet, C. Thomas, F. Fauvet, I. Puisieux, C. Doglioni, S. Piccinin, R. Maestro, T. Voeltzel, A. Selmi, S. Valsesia-Wittmann, C. Caron de Fromentel, and A. Puisieux Induction of EMT by twist proteins as a collateral effect of tumor-promoting inactivation of premature senescence Cancer Cell 14 2008 79 89
38. Q.Q. Li, J.D. Xu, W.J. Wang, X.X. Cao, Q. Chen, F. Tang, Z.Q. Chen, X.P. Liu, and Z.D. Xu Twist1-mediated adriamycin-induced epithelial-mesenchymal transition relates to multidrug resistance and invasive potential in breast cancer cells Clin Cancer Res 15 2009 2657 2665
39. G.Z. Cheng, J. Chan, Q. Wang, W. Zhang, C.D. Sun, and L.H. Wang Twist transcriptionally up-regulates AKT2 in breast cancer cells leading to increased migration, invasion, and resistance to paclitaxel Cancer Res 67 2007 1979 1987
40. S.A. Mani, W. Guo, M.J. Liao, E.N. Eaton, A. Ayyanan, A.Y. Zhou, M. Brooks, F. Reinhard, C.C. Zhang, M. Shipitsin, L.L. Campbell, K. Polyak, C. Brisken, J. Yang, and R.A. Weinberg The epithelial-mesenchymal transition generates cells with properties of stem cells Cell 133 2008 704 715
41. F. Vesuna, A. Lisok, B. Kimble, and V. Raman Twist modulates breast cancer stem cells by transcriptional regulation of CD24 expression Neoplasia 11 2009 1318 1328
42. V.L. Battula, K.W. Evans, B.G. Hollier, Y. Shi, F.C. Marini, A. Ayyanan, R.Y. Wang, C. Brisken, R. Guerra, M. Andreeff, and S.A. Mani Epithelial-mesenchymal transition-derived cells exhibit multilineage differentiation potential similar to mesenchymal stem cells Stem Cells 28 2010 1435 1445
43. A. Puisieux, S. Valsesia-Wittmann, and S. Ansieau A twist for survival and cancer progression Br J Cancer 94 2006 13 17
44. A.B. Firulli, and S.J. Conway Phosphoregulation of Twist1 provides a mechanism of cell fate control Curr Med Chem 15 2008 2641 2647
45. L. Qin, Z. Liu, H. Chen, and J. Xu The steroid receptor coactivator-1 regulates twist expression and promotes breast cancer metastasis Cancer Res 69 2009 3819 3827
46. J. Fu, L. Qin, T. He, J. Qin, J. Hong, J. Wong, L. Liao, and J. Xu The TWIST/Mi2/NuRD protein complex and its essential role in cancer metastasis Cell Res 21 2011 275 289
47. A.E. Vernon, and C. LaBonne Tumor metastasis: a new twist on epithelial-mesenchymal transitions Curr Biol 14 2004 R719 R721
48. F. Karreth, and D.A. Tuveson Twist induces an epithelial-mesenchymal transition to facilitate tumor metastasis Cancer Biol Ther 3 2004 1058 1059
49. M.H. Yang, M.Z. Wu, S.H. Chiou, P.M. Chen, S.Y. Chang, C.J. Liu, S.C. Teng, and K.J. Wu Direct regulation of TWIST by HIF-1alpha promotes metastasis Nat Cell Biol 10 2008 295 305
50. J. Fu, L. Zhang, T. He, X. Xiao, X. Liu, L. Wang, L. Yang, M. Yang, T. Zhang, R. Chen, and J. Xu TWIST represses estrogen receptor-alpha expression by recruiting the NuRD protein complex in breast cancer cells Int J Biol Sci 8 2012 522 532
51. M.H. Yang, D.S. Hsu, H.W. Wang, H.J. Wang, H.Y. Lan, W.H. Yang, C.H. Huang, S.Y. Kao, C.H. Tzeng, S.K. Tai, S.Y. Chang, O.K. Lee, and K.J. Wu Bmi1 is essential in Twist1-induced epithelial-mesenchymal transition Nat Cell Biol 12 2010 982 992
52. J. Kalra, B.W. Sutherland, A.L. Stratford, W. Dragowska, K.A. Gelmon, S. Dedhar, S.E. Dunn, and M.B. Bally Suppression of Her2/neu expression through ILK inhibition is regulated by a pathway involving TWIST and YB-1 Oncogene 29 2010 6343 6356
53. M.A. Eckert, T.M. Lwin, A.T. Chang, J. Kim, E. Danis, L. Ohno-Machado, and J. Yang Twist1-induced invadopodia formation promotes tumor metastasis Cancer Cell 19 2011 372 386
54. J.H. Tsai, J.L. Donaher, D.A. Murphy, S. Chau, and J. Yang Spatiotemporal regulation of epithelial-mesenchymal transition is essential for squamous cell carcinoma metastasis Cancer Cell 22 2012 725 736
55. S.Q. Kuang, L. Liao, H. Zhang, A.V. Lee, B.W. O'Malley, and J. Xu AIB1/SRC-3 deficiency affects insulin-like growth factor I signaling pathway and suppresses v-Ha-ras-induced breast cancer initiation and progression in mice Cancer Res 64 2004 1875 1885
56. Y.T. Chen, P.O. Akinwunmi, J.M. Deng, O.H. Tam, and R.R. Behringer Generation of a Twist1 conditional null allele in the mouse Genesis 45 2007 588 592
57. K. Guo, J.E. McMinn, T. Ludwig, Y.H. Yu, G. Yang, L. Chen, D. Loh, C. Li, S. Chua Jr., and Y. Zhang Disruption of peripheral leptin signaling in mice results in hyperleptinemia without associated metabolic abnormalities Endocrinology 148 2007 3987 3997
58. Z. Liu, S. Zhou, L. Liao, X. Chen, M. Meistrich, and J. Xu Jmjd1a demethylase-regulated histone modification is essential for cAMP-response element modulator-regulated gene expression and spermatogenesis J Biol Chem 285 2010 2758 2770
59. J. Xu, L. Liao, G. Ning, H. Yoshida-Komiya, C. Deng, and B.W. O'Malley The steroid receptor coactivator SRC-3 (p/CIP/RAC3/AIB1/ACTR/TRAM-1) is required for normal growth, puberty, female reproductive function, and mammary gland development Proc Natl Acad Sci USA 97 2000 6379 6384
60. S. Itzkovitz, I.C. Blat, T. Jacks, H. Clevers, and A. van Oudenaarden Optimality in the development of intestinal crypts Cell 148 2012 608 619
61. M.H. Ross, G.I. Kaye, and W. Pawlina Histology: a text and atlas: with correlated cell and molecular biology ed 4 2003 Lippincott Williams & Wilkins Hagerstown, MD
62. K.K. Lin, D. Chudova, G.W. Hatfield, P. Smyth, and B. Andersen Identification of hair cycle-associated genes from time-course gene expression profile data by using replicate variance Proc Natl Acad Sci USA 101 2004 15955 15960
63. T. Matsuzaki, and K. Yoshizato Role of hair papilla cells on induction and regeneration processes of hair follicles Wound Repair Regen 6 1998 524 530
64. J. Yang, S.A. Mani, and R.A. Weinberg Exploring a new twist on tumor metastasis Cancer Res 66 2006 4549 4552
65. E. Fuchs, B.J. Merrill, C. Jamora, and R. DasGupta At the roots of a never-ending cycle Dev Cell 1 2001 13 25
66. K.S. Stenn, and R. Paus Controls of hair follicle cycling Physiol Rev 81 2001 449 494
67. M. Rendl, L. Lewis, and E. Fuchs Molecular dissection of mesenchymal-epithelial interactions in the hair follicle PLoS Biol 3 2005 e331
68. F.A. Pereira, Y. Qiu, G. Zhou, M.J. Tsai, and S.Y. Tsai The orphan nuclear receptor COUP-TFII is required for angiogenesis and heart development Genes Dev 13 1999 1037 1049
69. J. Qin, S.P. Wu, C.J. Creighton, F. Dai, X. Xie, C.M. Cheng, A. Frolov, G. Ayala, X. Lin, X.H. Feng, M.M. Ittmann, S.J. Tsai, M.J. Tsai, and S.Y. Tsai COUP-TFII inhibits TGF-beta-induced growth barrier to promote prostate tumorigenesis Nature 493 2013 236 240
70. J. Qin, M.J. Tsai, and S.Y. Tsai Essential roles of COUP-TFII in Leydig cell differentiation and male fertility PLoS One 3 2008 e3285