Canonical Notch signaling in the developing lung is required for determination of arterial smooth muscle cells and selection of Clara versus ciliated cell fate

被引:178
作者
Morimoto, Mitsuru [1 ,2 ]
Liu, Zhenyi [1 ,2 ]
Cheng, Hui-Teng [3 ,4 ]
Winters, Niki [5 ,6 ]
Bader, David [5 ,6 ]
Kopan, Raphael [1 ,2 ]
机构
[1] Washington Univ, Sch Med, Dept Dev Biol, St Louis, MO 63110 USA
[2] Washington Univ, Sch Med, Div Dermatol, St Louis, MO 63110 USA
[3] Natl Taiwan Univ Hosp, Taipei, Taiwan
[4] Far Eastern Mem Hosp, Dept Internal Med, Taipei, Taiwan
[5] Vanderbilt Univ, Med Ctr, Dept Med, Nashville, TN 37232 USA
[6] Vanderbilt Univ, Med Ctr, Program Dev Biol, Stahlman Cardiovasc Res Labs, Nashville, TN 37232 USA
关键词
Notch; Lung; Clara cells; Ciliated cells; Arterial vascular smooth muscle cells; RBP-J; MESENCHYMAL TRANSITION; PROGENITOR CELLS; HES1; EXPRESSION; HAIR FOLLICLE; BASAL-CELLS; STEM-CELLS; IN-VIVO; DIFFERENTIATION; ACTIVATION;
D O I
10.1242/jcs.058669
中图分类号
Q2 [细胞生物学];
学科分类号
071009 ; 090102 ;
摘要
Lung development is the result of complex interactions between four tissues: epithelium, mesenchyme, mesothelium and endothelium. We marked the lineages experiencing Notch1 activation in these four cellular compartments during lung development and complemented this analysis by comparing the cell fate choices made in the absence of RBPj kappa, the essential DNA binding partner of all Notch receptors. In the mesenchyme, RBPj kappa was required for the recruitment and specification of arterial vascular smooth muscle cells (vSMC) and for regulating mesothelial epithelial-mesenchymal transition (EMT), but no adverse affects were observed in mice lacking mesenchymal RBPj kappa. We provide indirect evidence that this is due to vSMC rescue by endothelial-mesenchymal transition (EnMT). In the epithelium, we show that Notch1 activation was most probably induced by Foxj1-expressing cells, which suggests that Notch1-mediated lateral inhibition regulates the selection of Clara cells at the expense of ciliated cells. Unexpectedly, and in contrast to Pofut1-null epithelium, Hes1 expression was only marginally reduced in RBPj kappa-null epithelium, with a corresponding minimal effect on pulmonary neuroendocrine cell fate selection. Collectively, the primary roles for canonical Notch signaling in lung development are in selection of Clara cell fate and in vSMC recruitment. These analyses suggest that the impact of gamma-secretase inhibitors on branching in vitro reflect a non-cell autonomous contribution from endothelial or vSMC-derived signals.
引用
收藏
页码:213 / 224
页数:12
相关论文
共 72 条
[1]   Role of platelet-derived growth factors in physiology and medicine [J].
Andrae, Johanna ;
Gallini, Radiosa ;
Betsholtz, Christer .
GENES & DEVELOPMENT, 2008, 22 (10) :1276-1312
[2]   Perspectives on endothelial-to-mesenchymal transition: potential contribution to vascular remodeling in chronic pulmonary hypertension [J].
Arciniegas, Enrique ;
Frid, Maria G. ;
Douglas, Ivor S. ;
Stenmark, Kurt R. .
AMERICAN JOURNAL OF PHYSIOLOGY-LUNG CELLULAR AND MOLECULAR PHYSIOLOGY, 2007, 293 (01) :L1-L8
[3]   PTF1 is an organ-specific and notch-independent basic helix-loop-helix complex containing the mammalian suppressor of hairless (RBP-J) or its paralogue, RBP-L [J].
Beres, TM ;
Masui, T ;
Swift, GH ;
Shi, L ;
Henke, RM ;
MacDonald, RJ .
MOLECULAR AND CELLULAR BIOLOGY, 2006, 26 (01) :117-130
[4]   A myocardial lineage derives from Tbx18 epicardial cells [J].
Cai, Chen-Leng ;
Martin, Jody C. ;
Sun, Yunfu ;
Cui, Li ;
Wang, Lianchun ;
Ouyang, Kunfu ;
Yang, Lei ;
Bu, Lei ;
Liang, Xingqun ;
Zhang, Xiaoxue ;
Stallcup, William B. ;
Denton, Christopher P. ;
McCulloch, Andrew ;
Chen, Ju ;
Evans, Sylvia M. .
NATURE, 2008, 454 (7200) :104-U4
[5]   Regulation of early lung morphogenesis:: questions, facts and controversies [J].
Cardoso, WV ;
Lü, JN .
DEVELOPMENT, 2006, 133 (09) :1611-1624
[6]  
Chen CL, 2006, CIRCULATION, V114, P1
[7]  
CONLON RA, 1995, DEVELOPMENT, V121, P1533
[8]  
Deblandre GA, 1999, DEVELOPMENT, V126, P4715
[9]   Jagged1-selective notch signaling induces smooth muscle differentiation via a RBP-Jκ-dependent pathway [J].
Doi, Hiroshi ;
Iso, Tatsuya ;
Sato, Hiroko ;
Yamazaki, Miki ;
Matsui, Hiroki ;
Tanaka, Toru ;
Manabe, Ichiro ;
Arai, Masashi ;
Nagai, Ryozo ;
Kurabayashi, Masahiko .
JOURNAL OF BIOLOGICAL CHEMISTRY, 2006, 281 (39) :28555-28564
[10]   Jagged 1 is a β-catenin target gene required for ectopic hair follicle formation in adult epidermis [J].
Estrach, Soline ;
Ambler, Carrie A. ;
Lo Celso, Cristina ;
Hozumi, Katsuto ;
Watt, Fiona M. .
DEVELOPMENT, 2006, 133 (22) :4427-4438