Noncanonical NOTCH signaling limits self-renewal of human epithelial and induced pluripotent stem cells through ROCK activation

Molecular and Cellular Biology

Volumn 33, Issue 22, 2013, Pages 4434-4447

  Yugawa, Takashi ^a   Nishino, Koichiro ^b   Ohno, Shin Ichi ^a   Nakahara, Tomomi ^a   Fujita, Masatoshi ^c   Goshima, Naoki ^d   Umezawa, Akihiro ^e   Kiyono, Tohru ^a  

^a NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

^b UNIVERSITY OF MIYAZAKI   (Japan)

^c KYUSHU UNIVERSITY   (Japan)

^d NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

^e NATIONAL CENTER FOR CHILD HEALTH AND DEVELOPMENT   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; NOTCH1 RECEPTOR; RHO KINASE;

ARTICLE; CELL DIFFERENTIATION; CELL GROWTH; CELL RENEWAL; CLONOGENESIS; CONTROLLED STUDY; EPITHELIUM CELL; HUMAN; HUMAN CELL; KERATINOCYTE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ADULT; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; ENZYME ACTIVATION; FEMALE; GENE EXPRESSION; GENE KNOCKDOWN TECHNIQUES; HUMANS; INDUCED PLURIPOTENT STEM CELLS; KERATINOCYTES; RECEPTOR, NOTCH1; RHO-ASSOCIATED KINASES; SIGNAL TRANSDUCTION;

EID: 84887006066     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00577-13     Document Type: Article

References (74)

1. Lai EC. 2004. Notch signaling: control of cell communication and cell fate. Development 131:965-973.
2. Bray SJ. 2006. Notch signalling: a simple pathway becomes complex. Nat. Rev. Mol. Cell Biol. 7:678-689.
3. Kopan R, Ilagan MX. 2009. The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 137:216-233.
4. Roy M, Pear WS, Aster JC. 2007. The multifaceted role of Notch in cancer. Curr. Opin. Genet. Dev. 17:52-59.
5. Koch U, Radtke F. 2007. Notch and cancer: a double-edged sword. Cell. Mol. Life Sci. 64:2746-2762.
6. Talora C, Campese AF, Bellavia D, Felli MP, Vacca A, Gulino A, Screpanti I. 2008. Notch signaling and diseases: an evolutionary journey from a simple beginning to complex outcomes. Biochim. Biophys. Acta 1782:489-497.
7. South AP, Cho RJ, Aster JC. 2012. The double-edged sword of Notch signaling in cancer. Semin. Cell Dev. Biol. 23:458-464.
8. Watt FM, Estrach S, Ambler CA. 2008. Epidermal Notch signalling: differentiation, cancer and adhesion. Curr. Opin. Cell Biol. 20:171-179.
9. Dotto GP. 2009. Crosstalk of Notch with p53 and p63 in cancer growth control. Nat. Rev. Cancer 9:587-595.
10. Tan MJ, White EA, Sowa ME, Harper JW, Aster JC, Howley PM. 2012. Cutaneous beta-human papillomavirus E6 proteins bind Mastermindlike coactivators and repress Notch signaling. Proc. Natl. Acad. Sci. U. S. A. 109:E1473-E1480.
11. Lowell S, Jones P, Le Roux I, Dunne J, Watt FM. 2000. Stimulation of human epidermal differentiation by delta-notch signalling at the boundaries of stem-cell clusters. Curr. Biol. 10:491-500.
12. Nicolas M, Wolfer A, Raj K, Kummer JA, Mill P, van Noort M, Hui CC, Clevers H, Dotto GP, Radtke F. 2003. Notch1 functions as a tumor suppressor in mouse skin. Nat. Genet. 33:416-421.
13. Kolly C, Suter MM, Muller EJ. 2005. Proliferation, cell cycle exit, and onset of terminal differentiation in cultured keratinocytes: preprogrammed pathways in control of C-Myc and Notch1 prevail over extracellular calcium signals. J. Invest. Dermatol. 124:1014-1025.
14. Yugawa T, Handa K, Narisawa-Saito M, Ohno S, Fujita M, Kiyono T. 2007. Regulation of Notch1 gene expression by p53 in epithelial cells. Mol. Cell. Biol. 27:3732-3742.
15. Miller AC, Lyons EL, Herman TG. 2009. cis-inhibition of Notch by endogenous Delta biases the outcome of lateral inhibition. Curr. Biol. 19:1378-1383.
16. Fleming RJ, Hori K, Sen A, Filloramo GV, Langer JM, Obar RA, Artavanis-Tsakonas S, Maharaj-Best AC. 2013. An extracellular region of Serrate is essential for ligand-induced cis-inhibition of Notch signaling. Development 140:2039-2049.
17. Sprinzak D, Lakhanpal A, Lebon L, Santat LA, Fontes ME, Anderson GA, Garcia-Ojalvo J, Elowitz MB. 2010. cis-interactions between Notch and Delta generate mutually exclusive signalling states. Nature 465:86-90.
18. Yugawa T, Narisawa-Saito M, Yoshimatsu Y, Haga K, Ohno S, Egawa N, Fujita M, Kiyono T. 2010. DeltaNp63alpha repression of the Notch1 gene supports the proliferative capacity of normal human keratinocytes and cervical cancer cells. Cancer Res. 70:4034-4044.
19. Mills AA, Zheng B, Wang XJ, Vogel H, Roop DR, Bradley A. 1999. p63 is a p53 homologue required for limb and epidermal morphogenesis. Nature 398:708-713.
20. Yang A, Schweitzer R, Sun D, Kaghad M, Walker N, Bronson RT, Tabin C, Sharpe A, Caput D, Crum C, McKeon F. 1999. p63 is essential for regenerative proliferation in limb, craniofacial and epithelial development. Nature 398:714-718.
21. Nguyen BC, Lefort K, Mandinova A, Antonini D, Devgan V, Della Gatta G, Koster MI, Zhang Z, Wang J, Tommasi di Vignano A, Kitajewski J, Chiorino G, Roop DR, Missero C, Dotto GP. 2006. Cross-regulation between Notch and p63 in keratinocyte commitment to differentiation. Genes Dev. 20:1028-1042.
22. Yi R, Poy MN, Stoffel M, Fuchs E. 2008. A skin microRNA promotes differentiation by repressing 'stemness'. Nature 452:225-229.
23. Lena AM, Shalom-Feuerstein R, Rivetti di Val Cervo P, Aberdam D, Knight RA, Melino G, Candi E. 2008. miR-203 represses 'stemness' by repressing DeltaNp63. Cell Death Differ. 15:1187-1195.
24. Melino G, Gallagher E, Aqeilan RI, Knight R, Peschiaroli A, Rossi M, Scialpi F, Malatesta M, Zocchi L, Browne G, Ciechanover A, Bernassola F. 2008. Itch: a HECT-type E3 ligase regulating immunity, skin and cancer. Cell Death Differ. 15:1103-1112.
25. Rand MD, Grimm LM, Artavanis-Tsakonas S, Patriub V, Blacklow SC, Sklar J, Aster JC. 2000. Calcium depletion dissociates and activates heterodimeric notch receptors. Mol. Cell. Biol. 20:1825-1835.
26. Gupta-Rossi N, Le Bail O, Gonen H, Brou C, Logeat F, Six E, Ciechanover A, Israel A. 2001. Functional interaction between SEL-10, an F-box protein, and the nuclear form of activated Notch1 receptor. J. Biol. Chem. 276:34371-34378.
27. Krejci A, Bray S. 2007. Notch activation stimulates transient and selective binding of Su(H)/CSL to target enhancers. Genes Dev. 21:1322-1327.
28. van Tetering G, van Diest P, Verlaan I, van der Wall E, Kopan R, Vooijs M. 2009. Metalloprotease ADAM10 is required for Notch1 site 2 cleavage. J. Biol. Chem. 284:31018-31027.
29. Perumalsamy LR, Marcel N, Kulkarni S, Radtke F, Sarin A. 2012. Distinct spatial and molecular features of notch pathway assembly in regulatory T cells. Sci. Signal. 5:ra53. doi:10.1126/scisignal.2002859.
30. Sanalkumar R, Dhanesh SB, James J. 2010. Non-canonical activation of Notch signaling/target genes in vertebrates. Cell. Mol. Life Sci. 67:2957- 2968.
31. Andersen P, Uosaki H, Shenje LT, Kwon C. 2012. Non-canonical Notch signaling: emerging role and mechanism. Trends Cell Biol. 22:257-265.
32. Jaffe AB, Hall A. 2005. Rho GTPases: biochemistry and biology. Annu. Rev. Cell Dev. Biol. 21:247-269.
33. Riento K, Ridley AJ. 2003. Rocks: multifunctional kinases in cell behaviour. Nat. Rev. Mol. Cell Biol. 4:446-456.
34. Narumiya S, Tanji M, Ishizaki T. 2009. Rho signaling, ROCK and mDia1, in transformation, metastasis and invasion. Cancer Metastasis Rev. 28:65-76.
35. McMullan R, Lax S, Robertson VH, Radford DJ, Broad S, Watt FM, Rowles A, Croft DR, Olson MF, Hotchin NA. 2003. Keratinocyte differentiation is regulated by the Rho and ROCK signaling pathway. Curr. Biol. 13:2185-2189.
36. Liebig T, Erasmus J, Kalaji R, Davies D, Loirand G, Ridley A, Braga VM. 2009. RhoE Is required for keratinocyte differentiation and stratification. Mol. Biol. Cell 20:452-463.
37. Chapman S, Liu X, Meyers C, Schlegel R, McBride AA. 2010. Human keratinocytes are efficiently immortalized by a Rho kinase inhibitor. J. Clin. Invest. 120:2619-2626.
38. Liu X, Ory V, Chapman S, Yuan H, Albanese C, Kallakury B, Timofeeva OA, Nealon C, Dakic A, Simic V, Haddad BR, Rhim JS, Dritschilo A, Riegel A, McBride A, Schlegel R. 2012. ROCK inhibitor and feeder cells induce the conditional reprogramming of epithelial cells. Am. J. Pathol. 180:599-607.
39. Watanabe K, Ueno M, Kamiya D, Nishiyama A, Matsumura M, Wataya T, Takahashi JB, Nishikawa S, Muguruma K, Sasai Y. 2007. A ROCK inhibitor permits survival of dissociated human embryonic stem cells. Nat. Biotechnol. 25:681-686.
40. Chen G, Hou Z, Gulbranson DR, Thomson JA. 2010. Actin-myosin contractility is responsible for the reduced viability of dissociated human embryonic stem cells. Cell Stem Cell 7:240-248.
41. Ohgushi M, Matsumura M, Eiraku M, Murakami K, Aramaki T, Nishiyama A, Muguruma K, Nakano T, Suga H, Ueno M, Ishizaki T, Suemori H, Narumiya S, Niwa H, Sasai Y. 2010. Molecular pathway and cell state responsible for dissociation-induced apoptosis in human pluripotent stem cells. Cell Stem Cell 7:225-239.
42. Ohgushi M, Sasai Y. 2011. Lonely death dance of human pluripotent stem cells: ROCKing between metastable cell states. Trends Cell Biol. 21: 274-282.
43. Jacobs JP, Jones CM, Baille JP. 1970. Characteristics of a human diploid cell designated MRC-5. Nature 227:168-170.
44. Cui CH, Uyama T, Miyado K, Terai M, Kyo S, Kiyono T, Umezawa A. 2007. Menstrual blood-derived cells confer human dystrophin expression in the murine model of Duchenne muscular dystrophy via cell fusion and myogenic transdifferentiation. Mol. Biol. Cell 18:1586-1594.
45. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S. 2007. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131:861-872.
46. Nishino K, Toyoda M, Yamazaki-Inoue M, Makino H, Fukawatase Y, Chikazawa E, Takahashi Y, Miyagawa Y, Okita H, Kiyokawa N, Akutsu H, Umezawa A. 2010. Defining hypo-methylated regions of stem cellspecific promoters in human iPS cells derived from extra-embryonic amnions and lung fibroblasts. PLoS One 5:e13017. doi:10.1371/journal.pone .0013017.
47. Nishino K, Toyoda M, Yamazaki-Inoue M, Fukawatase Y, Chikazawa E, Sakaguchi H, Akutsu H, Umezawa A. 2011. DNA methylation dynamics in human induced pluripotent stem cells over time. PLoS Genet. 7:e1002085. doi:10.1371/journal.pgen.1002085.
48. Weng AP, Nam Y, Wolfe MS, Pear WS, Griffin JD, Blacklow SC, Aster JC. 2003. Growth suppression of pre-T acute lymphoblastic leukemia cells by inhibition of notch signaling. Mol. Cell. Biol. 23:655-664.
49. Mandinova A, Lefort K, Tommasi di Vignano A, Stonely W, Ostano P, Chiorino G, Iwaki H, Nakanishi J, Dotto GP. 2008. The FoxO3a gene is a key negative target of canonical Notch signalling in the keratinocyte UVB response. EMBO J. 27:1243-1254.
50. Narisawa-Saito M, Yoshimatsu Y, Ohno S, Yugawa T, Egawa N, Fujita M, Hirohashi S, Kiyono T. 2008. An in vitro multistep carcinogenesis model for human cervical cancer. Cancer Res. 68:5699-5705.
51. Ongusaha PP, Kim HG, Boswell SA, Ridley AJ, Der CJ, Dotto GP, Kim YB, Aaronson SA, Lee SW. 2006. RhoE is a pro-survival p53 target gene that inhibits ROCK I-mediated apoptosis in response to genotoxic stress. Curr. Biol. 16:2466-2472.
52. Wong CC, Wong CM, Tung EK, Man K, Ng IO. 2009. Rho-kinase 2 is frequently overexpressed in hepatocellular carcinoma and involved in tumor invasion. Hepatology 49:1583-1594.
53. Weng AP, Ferrando AA, Lee W, Morris JPT Silverman LB, Sanchez-Irizarry C, Blacklow SC, Look AT, Aster JC. 2004. Activating mutations of NOTCH1 in human T cell acute lymphoblastic leukemia. Science 306: 269-271.
54. Coleman ML, Sahai EA, Yeo M, Bosch M, Dewar A, Olson MF. 2001. Membrane blebbing during apoptosis results from caspase-mediated activation of ROCK I. Nat. Cell Biol. 3:339-345.
55. Sebbagh M, Renvoize C, Hamelin J, Riche N, Bertoglio J, Breard J. 2001. Caspase-3-mediated cleavage of ROCK I induces MLC phosphorylation and apoptotic membrane blebbing. Nat. Cell Biol. 3:346-352.
56. Lefort K, Mandinova A, Ostano P, Kolev V, Calpini V, Kolfschoten I, Devgan V, Lieb J, Raffoul W, Hohl D, Neel V, Garlick J, Chiorino G, Dotto GP. 2007. Notch1 is a p53 target gene involved in human keratinocyte tumor suppression through negative regulation of ROCK1/2 and MRCKalpha kinases. Genes Dev. 21:562-577.
57. Ronchini C, Capobianco AJ. 2000. Notch(ic)-ER chimeras display hormone-dependent transformation, nuclear accumulation, phosphorylation and CBF1 activation. Oncogene 19:3914-3924.
58. Krawetz RJ, Li X, Rancourt DE. 2009. Human embryonic stem cells: caught between aROCKinhibitor and a hard place. Bioessays 31:336-343.
59. Chang J, Xie M, Shah VR, Schneider MD, Entman ML, Wei L, Schwartz RJ. 2006. Activation of Rho-associated coiled-coil protein kinase 1 (ROCK-1) by caspase-3 cleavage plays an essential role in cardiac myocyte apoptosis. Proc. Natl. Acad. Sci. U. S. A. 103:14495-14500.
60. Yatim A, Benne C, Sobhian B, Laurent-Chabalier S, Deas O, Judde JG, Lelievre JD, Levy Y, Benkirane M. 2012. NOTCH1 nuclear interactome reveals key regulators of its transcriptional activity and oncogenic function. Mol. Cell 48:445-458.
61. Yi CH, Yuan J. 2009. The Jekyll and Hyde functions of caspases. Dev. Cell 16:21-34.
62. Okuyama R, Nguyen BC, Talora C, Ogawa E, Tommasi di Vignano A, Lioumi M, Chiorino G, Tagami H, Woo M, Dotto GP. 2004. High commitment of embryonic keratinocytes to terminal differentiation through a Notch1-caspase 3 regulatory mechanism. Dev. Cell 6:551-562.
63. Lee P, Lee DJ, Chan C, Chen SW, Ch'en I, Jamora C. 2009. Dynamic expression of epidermal caspase 8 simulates a wound healing response. Nature 458:519-523.
64. Blanpain C, Fuchs E. 2009. Epidermal homeostasis: a balancing act of stem cells in the skin. Nat. Rev. Mol. Cell Biol. 10:207-217.
65. Carroll DK, Carroll JS, Leong CO, Cheng F, Brown M, Mills AA, Brugge JS, Ellisen LW. 2006. p63 regulates an adhesion programme and cell survival in epithelial cells. Nat. Cell Biol. 8:551-561.
66. Melino G. 2011. p63 is a suppressor of tumorigenesis and metastasis interacting with mutant p53. Cell Death Differ. 18:1487-1499.
67. Thumkeo D, Keel J, Ishizaki T, Hirose M, Nonomura K, Oshima H, Oshima M, Taketo MM, Narumiya S. 2003. Targeted disruption of the mouse rho-associated kinase 2 gene results in intrauterine growth retardation and fetal death. Mol. Cell. Biol. 23:5043-5055.
68. Shimizu Y, Thumkeo D, Keel J, Ishizaki T, Oshima H, Oshima M, Noda Y, Matsumura F, Taketo MM, Narumiya S. 2005. ROCK-I regulates closure of the eyelids and ventral body wall by inducing assembly of actomyosin bundles. J. Cell Biol. 168:941-953.
69. Lock FE, Hotchin NA. 2009. Distinct roles for ROCK1 and ROCK2 in the regulation of keratinocyte differentiation. PLoS One 4:e8190. doi:10.1371 /journal.pone.0008190.
70. Grossi M, Hiou-Feige A, Tommasi Di Vignano A, Calautti E, Ostano P, Lee S, Chiorino G, Dotto GP. 2005. Negative control of keratinocyte differentiation by Rho/CRIK signaling coupled with up-regulation of KyoT1/2 (FHL1) expression. Proc. Natl. Acad. Sci. U. S. A. 102:11313-1318.
71. Zheng S, Huang J, Zhou K, Zhang C, Xiang Q, Tan Z, Wang T, Fu X. 2011. 17beta-Estradiol enhances breast cancer cell motility and invasion via extra-nuclear activation of actin-binding protein ezrin. PLoS One 6:e22439. doi:10.1371/journal.pone.0022439.
72. Vega FM, Fruhwirth G, Ng T, Ridley AJ. 2011. RhoA and RhoC have distinct roles in migration and invasion by acting through different targets. J. Cell Biol. 193:655-665.
73. Zhang YM, Bo J, Taffet GE, Chang J, Shi J, Reddy AK, Michael LH, Schneider MD, Entman ML, Schwartz RJ, Wei L. 2006. Targeted deletion of ROCK1 protects the heart against pressure overload by inhibiting reactive fibrosis. FASEB J. 20:916-925.
74. Lee DH, Shi J, Jeoung NH, Kim MS, Zabolotny JM, Lee SW, White MF, Wei L, Kim YB. 2009. Targeted disruption of ROCK1 causes insulin resistance in vivo. J. Biol. Chem. 284:11776-11780.