title: Anion translocation through an Slc26 transporter mediates lumen expansion during tubulogenesis.
abstract: Lumen formation is a critical event in biological tube formation, yet its molecular mechanisms remain poorly understood. Specifically, how lumen expansion is coordinated with other processes of tubulogenesis is not well known, and the role of membrane transporters in tubulogenesis during development has not been adequately addressed. Here we identify a solute carrier 26 (Slc26) family protein as an essential regulator of tubulogenesis using the notochord of the invertebrate chordate Ciona intestinalis as a model. Ci-Slc26aα is indispensable for lumen formation and expansion, but not for apical/luminal membrane formation and lumen connection. Ci-Slc26aα acts as an anion transporter, mediating the electrogenic exchange of sulfate or oxalate for chloride or bicarbonate and electroneutral chloride:bicarbonate exchange. Mutant rescue assays show that this transport activity is essential for Ci-Slc26aα's in vivo function. Our work reveals the consequences and relationships of several key processes in lumen formation, and establishes an in vivo assay for studying the molecular basis of the transport properties of SLC26 family transporters and their related diseases.
authors: Sars International Centre for Marine Molecular Biology, University of Bergen, 5008 Bergen, Norway.
authors: Wei
authors: W
authors: Deng
authors: Florian
authors: F
authors: Nies
authors: Anja
authors: A
authors: Feuer
authors: Ivana
authors: I
authors: Bocina
authors: Dominik
authors: D
authors: Oliver
authors: Di
authors: D
authors: Jiang
mesh_terms: D000595:Amino Acid Sequence; D000818:Animals; D027963:Chloride-Bicarbonate Antiporters / Q000737:chemistry / Q000235:genetics / Q000378:metabolism*; D002938:Ciona intestinalis / Q000196:embryology* / Q000235:genetics / Q000378:metabolism*; D004563:Electrochemistry; D046529:Microscopy, Electron, Transmission; D008954:Models, Biological; D008969:Molecular Sequence Data; D050505:Mutant Proteins / Q000235:genetics / Q000378:metabolism; D009672:Notochord / Q000196:embryology / Q000378:metabolism / Q000648:ultrastructure; D010802:Phylogeny; D017434:Protein Structure, Tertiary; D017386:Sequence Homology, Amino Acid
chemical_list: D027963:Chloride-Bicarbonate Antiporters; D050505:Mutant Proteins
references: Curr Biol. 2011 Nov 22;21(22):1942-8
references: 22079115
references: Cell Physiol Biochem. 2011;28(3):527-34
references: 22116367
references: Dev Biol. 2009 Jun 15;330(2):237-49
references: 19324030
references: Nat Rev Mol Cell Biol. 2008 Nov;9(11):887-901
references: 18946477
references: Biophys J. 2006 Jun 1;90(11):4035-45
references: 16565043
references: Development. 2007 Jan;134(1):147-55
references: 17164420
references: Pediatr Res. 2002 Apr;51(4):479-84
references: 11919333
references: Dev Growth Differ. 1999 Dec;41(6):657-64
references: 10646795
references: J Biol Chem. 1996 Aug 2;271(31):18456-64
references: 8702490
references: Curr Med Chem. 2005;12(4):385-96
references: 15720248
references: J Clin Endocrinol Metab. 2002 Apr;87(4):1778-84
references: 11932316
references: J Physiol. 2012 Jan 15;590(2):259-72
references: 22063625
references: J Cell Biol. 1982 Oct;95(1):189-96
references: 6815204
references: Pflugers Arch. 2004 Feb;447(5):710-21
references: 12759755
references: Methods Enzymol. 1990;192:38-81
references: 2074799
references: Proc Natl Acad Sci U S A. 2007 May 1;104(18):7693-8
references: 17442754
references: Mech Dev. 1995 May;51(1):115-26
references: 7669687
references: Hum Mol Genet. 1998 Jul;7(7):1105-12
references: 9618167
references: Hum Mutat. 2001 May;17(5):403-11
references: 11317356
references: Cell. 2003 Jan 10;112(1):19-28
references: 12526790
references: EMBO J. 2011 Jun 24;30(14):2793-804
references: 21701557
references: Cold Spring Harb Protoc. 2009 Dec;2009(12):pdb.prot5345
references: 20150092
references: J Gen Physiol. 2011 Feb;137(2):239-51
references: 21282402
references: J Cell Biol. 2004 Jan 19;164(2):313-23
references: 14734539
references: Dev Dyn. 2007 Jul;236(7):1748-57
references: 17497687
references: Curr Biol. 2011 Feb 8;21(3):R126-36
references: 21300279
references: Physiology (Bethesda). 2008 Apr;23:104-14
references: 18400693
references: J Physiol. 2009 May 15;587(Pt 10):2179-85
references: 19015189
references: Nature. 2000 May 11;405(6783):149-55
references: 10821263
references: Cold Spring Harb Protoc. 2009 Dec;2009(12):pdb.prot5347
references: 20150094
references: J Med Genet. 2003 Apr;40(4):242-8
references: 12676893
references: Annu Rev Neurosci. 2004;27:453-85
references: 15217340
references: Dev Biol. 2008 Apr 15;316(2):312-22
references: 18342303
references: Nat Cell Biol. 2007 Aug;9(8):954-60
references: 17632505
references: J Biol Chem. 1994 Jan 28;269(4):3017-21
references: 8300633
references: Proc Natl Acad Sci U S A. 1998 May 26;95(11):5857-64
references: 9600884
references: Hum Mol Genet. 1998 Jul;7(7):1099-104
references: 9618166