title: Wnt to build a tube: contributions of Wnt signaling to epithelial tubulogenesis.
abstract: Epithelial tubes are crucial to the function of organ systems including the cardiovascular system, pulmonary system, gastrointestinal tract, reproductive organ systems, excretory system, and auditory system. Using a variety of animal model systems, recent studies have substantiated the role of Wnt signaling via the canonical/beta-catenin-mediated trajectory, the non-canonical Wnt trajectories, or both, in forming epithelial tubular tissues. This review focuses on the involvement of the Wnt pathways in the induction, specification, proliferation, and morphogenesis involved in tubulogenesis within tissues including the lungs, kidneys, ears, mammary glands, gut, and heart. The ultimate goal is to describe the developmental processes forming the various tubulogenic organ systems to determine the relationships between these processes.
authors.affiliation: Department of Biochemistry and Molecular Biology, The University of Texas M.D. Anderson Cancer Center, Houston, Texas 77030, USA. rkmiller@mdanderson.org
authors.forename: Rachel K
authors.initials: RK
authors.lastname: Miller
authors.forename: Pierre D
authors.initials: PD
authors.lastname: McCrea
mesh_terms: D000818:Animals; D002118:Calcium / Q000378:metabolism; D002319:Cardiovascular System / Q000196:embryology; D016764:Cell Polarity / Q000502:physiology; D007758:Ear, Inner / Q000196:embryology; D004848:Epithelium / Q000196:embryology*; D005260:Female; D041981:Gastrointestinal Tract / Q000196:embryology; D054262:Gastrulation / Q000502:physiology*; D007684:Kidney Tubules / Q000196:embryology; D008024:Ligands; D008321:Mammary Glands, Animal / Q000196:embryology; D023421:Models, Animal; D008954:Models, Biological; D009024:Morphogenesis; D054261:Neurulation / Q000502:physiology*; D012137:Respiratory System / Q000196:embryology; D015398:Signal Transduction / Q000502:physiology*; D051153:Wnt Proteins / Q000378:metabolism*; D051176:beta Catenin / Q000378:metabolism*
chemical_list: D008024:Ligands; D051153:Wnt Proteins; D051176:beta Catenin; D002118:Calcium
references.citation: Dev Dyn. 1999 Sep;216(1):45-58
references.pmid: 10474165
references.citation: Curr Biol. 2006 Oct 24;16(20):1986-97
references.pmid: 17055977
references.citation: Development. 1996 Dec;123:143-51
references.pmid: 9007236
references.citation: Dev Dyn. 2005 Apr;232(4):958-68
references.pmid: 15739222
references.citation: Mt Sinai J Med. 2006 Sep;73(5):738-50
references.pmid: 17008934
references.citation: Dev Cell. 2003 Jan;4(1):11-8
references.pmid: 12530959
references.citation: Nat Cell Biol. 2005 Jul;7(7):691-7
references.pmid: 15937478
references.citation: Organogenesis. 2008 Apr;4(2):116-22
references.pmid: 19279723
references.citation: Nat Genet. 2003 Aug;34(4):355-6
references.pmid: 12923538
references.citation: Dev Biol. 2007 Jun 1;306(1):121-33
references.pmid: 17433286
references.citation: J Biol Chem. 2003 Oct 10;278(41):40231-8
references.pmid: 12885771
references.citation: Nat Clin Pract Nephrol. 2006 Jan;2(1):40-55; quiz 55
references.pmid: 16932388
references.citation: Development. 2005 May;132(10):2273-85
references.pmid: 15829519
references.citation: Development. 1988 May;103(1):193-209
references.pmid: 3197629
references.citation: J Biol. 2004;3(3):11
references.pmid: 15186480
references.citation: Proc Natl Acad Sci U S A. 2003 Mar 18;100(6):3299-304
references.pmid: 12626757
references.citation: Development. 2008 Oct;135(20):3415-24
references.pmid: 18799542
references.citation: Zebrafish. 2009 Mar;6(1):29-40
references.pmid: 19292674
references.citation: Genes Dev. 2000 Apr 15;14(8):889-94
references.pmid: 10783160
references.citation: Development. 2004 Aug;131(16):4085-93
references.pmid: 15269167
references.citation: Nat Cell Biol. 2002 Jan;4(1):20-5
references.pmid: 11780127
references.citation: Dev Biol. 2003 Apr 1;256(1):18-33
references.pmid: 12654289
references.citation: J Biol Chem. 2002 Aug 16;277(33):29577-83
references.pmid: 12048202
references.citation: Cell. 2009 Apr 17;137(2):295-307
references.pmid: 19379695
references.citation: Genes Dev. 1990 Dec;4(12B):2319-32
references.pmid: 2279700
references.citation: J Neurosci. 2006 Feb 22;26(8):2147-56
references.pmid: 16495441
references.citation: Genes Dev. 2000 Mar 15;14(6):650-4
references.pmid: 10733525
references.citation: Curr Biol. 2005 Sep 20;15(18):1677-83
references.pmid: 16169491
references.citation: Development. 2005 Nov;132(21):4663-74
references.pmid: 16192304
references.citation: Development. 2008 Nov;135(22):3625-41
references.pmid: 18952908
references.citation: Dev Biol. 2002 Mar 1;243(1):1-19
references.pmid: 11846473
references.citation: Cell. 1982 Nov;31(1):99-109
references.pmid: 6297757
references.citation: Genes Dev. 2001 Feb 1;15(3):304-15
references.pmid: 11159911
references.citation: Genes Dev. 1998 Feb 15;12(4):449-55
references.pmid: 9472013
references.citation: Genes Dev. 2005 Jul 1;19(13):1612-23
references.pmid: 15961523
references.citation: Nature. 1994 Dec 15;372(6507):679-83
references.pmid: 7990960
references.citation: Development. 1998 Nov;125(21):4225-34
references.pmid: 9753677
references.citation: Development. 2009 Jan;136(1):161-71
references.pmid: 19060336
references.citation: Curr Opin Cell Biol. 2008 Apr;20(2):119-25
references.pmid: 18339531
references.citation: Proc Natl Acad Sci U S A. 2001 Dec 4;98(25):14487-92
references.pmid: 11717401
references.citation: Cell. 2007 Jun 15;129(6):1051-63
references.pmid: 17574020
references.citation: Development. 1994 Jun;120(6):1453-71
references.pmid: 8050356
references.citation: J Cell Biol. 1996 Jun;133(5):1123-37
references.pmid: 8655584
references.citation: J Cell Biol. 1996 Dec;135(5):1277-89
references.pmid: 8947551
references.citation: Development. 2008 Jul;135(13):2251-61
references.pmid: 18495817
references.citation: Development. 2007 Sep;134(17):3177-90
references.pmid: 17693601
references.citation: Development. 2005 Oct;132(20):4421-36
references.pmid: 16192308
references.citation: J Embryol Exp Morphol. 1985 Nov;89 Suppl:185-209
references.pmid: 3831213
references.citation: J Neurosci. 2006 May 10;26(19):5265-75
references.pmid: 16687519
references.citation: Curr Opin Cell Biol. 2005 Oct;17(5):533-41
references.pmid: 16099638
references.citation: Development. 2008 Nov;135(22):3719-29
references.pmid: 18927149
references.citation: Int J Dev Biol. 2001;45(1):225-7
references.pmid: 11291850
references.citation: Development. 2006 Mar;133(5):865-75
references.pmid: 16452098
references.citation: Proc Natl Acad Sci U S A. 2006 Dec 26;103(52):19812-7
references.pmid: 17170140
references.citation: Development. 2008 Mar;135(5):789-98
references.pmid: 18263841
references.citation: Curr Biol. 1999 Jul 1;9(13):695-8
references.pmid: 10395542
references.citation: Development. 1988 May;103(1):211-30
references.pmid: 3197630
references.citation: Proc Natl Acad Sci U S A. 1999 May 11;96(10):5522-7
references.pmid: 10318916
references.citation: Gastroenterology. 2007 Aug;133(2):529-38
references.pmid: 17681174
references.citation: Dev Biol. 2009 Feb 15;326(2):285-94
references.pmid: 19100728
references.citation: Nature. 2000 Sep 28;407(6803):530-5
references.pmid: 11029007
references.citation: Trends Cell Biol. 2003 Dec;13(12):615-21
references.pmid: 14624839
references.citation: Int J Dev Biol. 2007;51(6-7):535-47
references.pmid: 17891715
references.citation: Nature. 1997 May 15;387(6630):292-5
references.pmid: 9153394
references.citation: Development. 2000 Feb;127(3):457-67
references.pmid: 10631167
references.citation: Nat Genet. 2008 Jan;40(1):69-77
references.pmid: 18066062
references.citation: Cell Signal. 2007 Apr;19(4):659-71
references.pmid: 17188462
references.citation: Cell. 1990 Sep 21;62(6):1073-85
references.pmid: 2205396
references.citation: J Biol Chem. 2006 Nov 17;281(46):35081-7
references.pmid: 16973609
references.citation: Trends Genet. 2002 Sep;18(9):447-55
references.pmid: 12175805
references.citation: Nat Cell Biol. 2002 Aug;4(8):610-5
references.pmid: 12105418
references.citation: Exp Cell Res. 2004 Aug 15;298(2):369-87
references.pmid: 15265686
references.citation: Am J Physiol Renal Physiol. 2007 Aug;293(2):F494-500
references.pmid: 17494089
references.citation: Dev Biol. 1995 Aug;170(2):553-63
references.pmid: 7649383
references.citation: Development. 2007 Oct;134(20):3603-13
references.pmid: 17855428
references.citation: Dev Biol. 2002 Aug 1;248(1):13-28
references.pmid: 12142017
references.citation: Cell. 2005 Mar 25;120(6):857-71
references.pmid: 15797385
references.citation: J Embryol Exp Morphol. 1962 Mar;10:73-87
references.pmid: 14039372
references.citation: Dev Dyn. 2001 Sep;222(1):26-39
references.pmid: 11507767
references.citation: Dev Dyn. 2005 Mar;232(3):617-32
references.pmid: 15712279
references.citation: Cell. 2001 Dec 28;107(7):843-54
references.pmid: 11779461
references.citation: J Cell Biol. 2003 May 26;161(4):769-77
references.pmid: 12771126
references.citation: Cell. 2003 Jan 10;112(1):19-28
references.pmid: 12526790
references.citation: J Cell Biochem. 2006 Oct 1;99(2):647-64
references.pmid: 16791850
references.citation: Philos Trans R Soc Lond B Biol Sci. 2000 Jul 29;355(1399):897-922
references.pmid: 11128984
references.citation: Nat Rev Genet. 2007 Oct;8(10):791-802
references.pmid: 17878895
references.citation: J Clin Invest. 2007 Jul;117(7):1794-804
references.pmid: 17607356
references.citation: Oncogene. 1997 Oct;15(18):2133-44
references.pmid: 9393971
references.citation: Development. 2006 Feb;133(3):547-57
references.pmid: 16396908
references.citation: WormBook. 2005 Sep 26;:1-13
references.pmid: 18050409
references.citation: Dev Cell. 2005 Aug;9(2):283-92
references.pmid: 16054034
references.citation: Neuroscience. 2003;122(1):129-43
references.pmid: 14596855
references.citation: Dev Dyn. 2004 Feb;229(2):349-56
references.pmid: 14745960
references.citation: Proc Natl Acad Sci U S A. 2007 Jun 26;104(26):10894-9
references.pmid: 17576928
references.citation: Genesis. 2000 May;27(1):32-47
references.pmid: 10862153
references.citation: Pediatr Nephrol. 2007 Nov;22(11):1825-38
references.pmid: 17554566
references.citation: Nat Genet. 2007 Oct;39(10):1225-34
references.pmid: 17767158
references.citation: Proc Natl Acad Sci U S A. 2007 Jun 5;104(23):9685-90
references.pmid: 17522258
references.citation: Development. 2003 Jul;130(14):3175-85
references.pmid: 12783789
references.citation: Dev Biol. 2005 Jan 15;277(2):316-31
references.pmid: 15617677
references.citation: J Cell Biol. 2001 Apr 30;153(3):555-68
references.pmid: 11331306
references.citation: Development. 2006 May;133(9):1767-78
references.pmid: 16571627
references.citation: Dev Biol. 1997 Aug 15;188(2):189-204
references.pmid: 9268568
references.citation: Genesis. 2002 Apr;32(4):259-68
references.pmid: 11948913
references.citation: Annu Rev Cell Dev Biol. 1998;14:59-88
references.pmid: 9891778
references.citation: Hum Mol Genet. 2003 Jan 15;12(2):87-98
references.pmid: 12499390
references.citation: Pediatr Res. 2007 Apr;61(4):386-91
references.pmid: 17515859
references.citation: Trends Cell Biol. 1996 Aug;6(8):287-90
references.pmid: 15157435
references.citation: Oncogene. 2001 Sep 20;20(42):5972-81
references.pmid: 11593404
references.citation: Cell. 1992 May 1;69(3):385-7
references.pmid: 1581959
references.citation: Proc Natl Acad Sci U S A. 2007 May 29;104(22):9313-8
references.pmid: 17519333
references.citation: Dev Biol. 2006 Jul 1;295(1):219-31
references.pmid: 16678815
references.citation: Proc Natl Acad Sci U S A. 1999 May 25;96(11):6371-6
references.pmid: 10339594
references.citation: Development. 2008 May;135(9):1625-34
references.pmid: 18367557
references.citation: Curr Biol. 2003 Apr 15;13(8):674-9
references.pmid: 12699625
references.citation: EMBO Rep. 2002 Jan;3(1):69-75
references.pmid: 11751577
references.citation: Nature. 2009 Jan 22;457(7228):495-9
references.pmid: 19029882
references.citation: Nephrol Dial Transplant. 2002;17 Suppl 9:73-4
references.pmid: 12386296
references.citation: Gene Expr Patterns. 2008 May;8(5):297-306
references.pmid: 18346943
references.citation: Proc Natl Acad Sci U S A. 2007 Apr 10;104(15):6247-52
references.pmid: 17404238
references.citation: Cell. 1997 Aug 22;90(4):581-4
references.pmid: 9288737
references.citation: Dev Cell. 2001 Jul;1(1):93-101
references.pmid: 11703927
references.citation: Nat Genet. 1998 Aug;19(4):379-83
references.pmid: 9697701
references.citation: Kidney Int. 2006 Sep;70(5):854-64
references.pmid: 16816842
references.citation: PLoS Genet. 2008 Nov;4(11):e1000259
references.pmid: 19008950
references.citation: Trends Cardiovasc Med. 2006 Feb;16(2):38-45
references.pmid: 16473760
references.citation: Dev Biol. 2003 Jul 15;259(2):318-35
references.pmid: 12871704
references.citation: J Biol Chem. 2000 Apr 28;275(17):12701-11
references.pmid: 10777564
references.citation: Dev Biol. 2002 Aug 1;248(1):68-81
references.pmid: 12142021
references.citation: Mech Dev. 2001 Jul;105(1-2):181-4
references.pmid: 11429295
references.citation: Nature. 2006 Jan 12;439(7073):220-4
references.pmid: 16407953
references.citation: Mech Dev. 2001 Dec;109(2):437-40
references.pmid: 11731265
references.citation: Development. 2002 May;129(9):2087-98
references.pmid: 11959819
references.citation: Oncogene. 2006 Dec 4;25(57):7461-8
references.pmid: 17143290
references.citation: Dev Biol. 2007 Apr 1;304(1):127-40
references.pmid: 17240368
references.citation: Proc Natl Acad Sci U S A. 2004 Jan 6;101(1):266-71
references.pmid: 14695885
references.citation: Curr Opin Gastroenterol. 2007 Mar;23(2):111-4
references.pmid: 17268237
references.citation: Development. 2006 May;133(9):1611-24
references.pmid: 16613830
references.citation: Nature. 1999 Apr 1;398(6726):422-6
references.pmid: 10201372
references.citation: Genes Dev. 2002 Aug 15;16(16):2073-84
references.pmid: 12183362
references.citation: Dev Cell. 2005 Apr;8(4):611-22
references.pmid: 15809042
references.citation: Development. 2000 Jul;127(14):3091-100
references.pmid: 10862746
references.citation: Dev Biol. 2008 Sep 1;321(1):150-61
references.pmid: 18598690
references.citation: Pediatr Nephrol. 1999 Jun;13(5):454-9
references.pmid: 10412869
references.citation: Genes Dev. 2003 Jul 15;17(14):1709-13
references.pmid: 12865297
references.citation: Development. 2000 Oct;127(20):4433-42
references.pmid: 11003842
references.citation: Annu Rev Cell Dev Biol. 2005;21:155-76
references.pmid: 16212491
references.citation: Development. 2001 Jul;128(13):2581-92
references.pmid: 11493574
references.citation: Curr Biol. 2003 Apr 15;13(8):680-5
references.pmid: 12699626
references.citation: Mol Cell Neurosci. 2004 May;26(1):101-11
references.pmid: 15121182
references.citation: Circ Res. 2005 Feb 18;96(3):292-9
references.pmid: 15637299
references.citation: Genes Dev. 2004 Jun 15;18(12):1385-90
references.pmid: 15198980
references.citation: Nature. 2002 Aug 8;418(6898):636-41
references.pmid: 12167861
references.citation: Dev Dyn. 2008 Nov;237(11):3404-9
references.pmid: 18942153
references.citation: Trends Cell Biol. 2006 Dec;16(12):622-30
references.pmid: 17067797
references.citation: Int Rev Cytol. 2007;261:159-92
references.pmid: 17560282
references.citation: Development. 2008 Apr;135(7):1365-76
references.pmid: 18305003
references.citation: Dev Cell. 2008 Jun;14(6):954-61
references.pmid: 18539122
references.citation: Cancer Metastasis Rev. 1999;18(2):215-30
references.pmid: 10728985
references.citation: Cardiovasc Res. 2006 Nov 1;72(2):198-209
references.pmid: 16860783
references.citation: Curr Top Dev Biol. 1999;44:67-100
references.pmid: 9891877
references.citation: Hum Mol Genet. 2006 Oct 15;15 Spec No 2:R227-34
references.pmid: 16987888
references.citation: Nat Genet. 2005 Sep;37(9):980-5
references.pmid: 16116426
references.citation: Development. 2002 Oct;129(20):4831-42
references.pmid: 12361974
references.citation: Cell. 1998 Jul 10;94(1):109-18
references.pmid: 9674432
references.citation: Proc Natl Acad Sci U S A. 2007 May 29;104(22):9319-24
references.pmid: 17519332
references.citation: Development. 2007 Feb;134(4):647-58
references.pmid: 17259302
references.citation: Semin Cell Dev Biol. 2002 Jun;13(3):251-60
references.pmid: 12137734
references.citation: Genes Dev. 1998 Aug 15;12(16):2610-22
references.pmid: 9716412
references.citation: Development. 2005 Mar;132(6):1443-51
references.pmid: 15716339
references.citation: Growth Factors. 2005 Jun;23(2):111-6
references.pmid: 16019432
references.citation: Curr Biol. 2003 Jul 1;13(13):1129-33
references.pmid: 12842012
references.citation: Nat Rev Genet. 2007 May;8(5):368-81
references.pmid: 17387317
references.citation: Breast Cancer Res. 2009;11(2):R19
references.pmid: 19344510
references.citation: Nat Genet. 1997 Oct;17(2):179-81
references.pmid: 9326937
references.citation: Nature. 2003 May 8;423(6936):173-7
references.pmid: 12724779
references.citation: J Cell Sci. 2007 Jul 15;120(Pt 14):2402-12
references.pmid: 17606995
references.citation: Annu Rev Genet. 2008;42:517-40
references.pmid: 18710302
references.citation: Cell. 2009 Apr 3;137(1):32-45
references.pmid: 19345185
references.citation: Development. 2000 May;127(10):2227-38
references.pmid: 10769246
references.citation: Genes Dev. 2003 Jan 15;17(2):295-309
references.pmid: 12533515
references.citation: Int J Dev Biol. 2007;51(6-7):463-72
references.pmid: 17891709
references.citation: Mech Dev. 2009 Mar-Apr;126(3-4):142-59
references.pmid: 19100832
references.citation: Nature. 2000 May 4;405(6782):76-81
references.pmid: 10811221
references.citation: Curr Biol. 2006 Oct 24;16(20):R874-6
references.pmid: 17055968
references.citation: Mol Cell Biol. 2003 Jan;23(1):131-9
references.pmid: 12482967
references.citation: Dev Biol. 2005 Mar 1;279(1):179-92
references.pmid: 15708567
references.citation: Dev Biol. 2003 Jul 15;259(2):258-71
references.pmid: 12871700
references.citation: Cell. 2006 Apr 7;125(1):33-45
references.pmid: 16615888
references.citation: Dev Biol. 2003 Jun 15;258(2):406-18
references.pmid: 12798297
references.citation: Development. 2004 Oct;131(19):4819-29
references.pmid: 15342465
references.citation: Gastroenterology. 2005 Aug;129(2):626-38
references.pmid: 16083717
references.citation: Development. 2006 Jun;133(11):2095-104
references.pmid: 16672339
references.citation: Nat Genet. 2006 Mar;38(3):303-11
references.pmid: 16493421
references.citation: Dev Biol. 2002 Jul 1;247(1):165-81
references.pmid: 12074560
references.citation: Dev Cell. 2003 Sep;5(3):367-77
references.pmid: 12967557
references.citation: Development. 2001 May;128(9):1573-85
references.pmid: 11290296
references.citation: Development. 2002 Dec;129(24):5827-38
references.pmid: 12421720
references.citation: Nephron Exp Nephrol. 2005;100(1):e40-5
references.pmid: 15731568
references.citation: J Neurobiol. 2005 Sep 15;64(4):376-87
references.pmid: 16041754
references.citation: Curr Biol. 2002 Jun 4;12(11):876-84
references.pmid: 12062050
references.citation: Development. 2000 Oct;127(20):4407-17
references.pmid: 11003840
references.citation: Curr Biol. 2000 Aug 24;10(16):979-88
references.pmid: 10985385
references.citation: Proc Natl Acad Sci U S A. 2009 Mar 17;106(11):4290-5
references.pmid: 19237582
references.citation: Dev Cell. 2002 Jun;2(6):695-706
references.pmid: 12062082
references.citation: Genes Dev. 2009 Feb 1;23(3):265-77
references.pmid: 19204114
references.citation: Int J Dev Biol. 1999;43(5):381-95
references.pmid: 10535314
references.citation: J Neurobiol. 2005 Sep 15;64(4):446-57
references.pmid: 16041762
references.citation: Dev Cell. 2004 Mar;6(3):343-55
references.pmid: 15030758
references.citation: Curr Top Dev Biol. 2008;85:197-224
references.pmid: 19147007
references.citation: Nat Genet. 2008 Jul;40(7):871-9
references.pmid: 18552847
references.citation: Bioessays. 1992 Nov;14(11):735-41
references.pmid: 1365886
references.citation: Nature. 2000 May 4;405(6782):81-5
references.pmid: 10811222
references.citation: Development. 2003 Sep;130(17):4037-46
references.pmid: 12874125
references.citation: EMBO J. 2003 Sep 1;22(17):4409-20
references.pmid: 12941693
references.citation: EMBO J. 2002 Mar 1;21(5):976-85
references.pmid: 11867525
references.citation: Nature. 1997 Oct 30;389(6654):966-70
references.pmid: 9353119
references.citation: Dev Cell. 2007 Jul;13(1):10-3
references.pmid: 17609106
references.citation: Hum Mol Genet. 2001 Oct 15;10(22):2593-601
references.pmid: 11709546
references.citation: Cell. 2001 Apr 6;105(1):81-91
references.pmid: 11301004
references.citation: Organogenesis. 2008 Apr;4(2):87-91
references.pmid: 19279719
references.citation: Development. 2008 Oct;135(19):3185-90
references.pmid: 18715946
references.citation: Development. 2007 Jul;134(13):2533-9
references.pmid: 17537789
references.citation: Development. 2008 Jan;135(2):367-75
references.pmid: 18077588
references.citation: Nat Genet. 2005 May;37(5):537-43
references.pmid: 15852005
references.citation: Birth Defects Res C Embryo Today. 2003 Nov;69(4):318-24
references.pmid: 14745972
references.citation: Nature. 2005 Dec 8;438(7069):873-7
references.pmid: 16341017
references.citation: J Biol Chem. 1999 Jan 1;274(1):129-34
references.pmid: 9867820
references.citation: Development. 2007 Nov;134(21):3929-39
references.pmid: 17898001
references.citation: Nature. 2006 Aug 10;442(7103):688-91
references.pmid: 16799568
references.citation: Biochem J. 1998 Jan 15;329 ( Pt 2):209-23
references.pmid: 9425102
references.citation: Semin Cell Dev Biol. 2002 Jun;13(3):243-9
references.pmid: 12137733