The reorganization of epithelial sheets into tubes is a fundamental process in the formation of many organs, such as the lungs, kidneys, gut, and neural tube. This process involves the patterning of distinct cell types and the coordination of those cells during the shape changes and rearrangements that produce the tube. A better understanding of the cellular and genetic mechanisms that regulate tube formation is necessary for tissue engineers to develop functional organs in vitro. The Drosophila egg chamber has emerged as an outstanding model for studying tubulogenesis. Synthesis of the dorsal respiratory appendages by the follicular epithelium resembles primary neurulation in vertebrates. This review summarizes work on the patterning and morphogenesis of the dorsal-appendage tubes and highlights key areas where mathematical modeling could contribute to our understanding of these processes.
HwangN.S., VargheseS., ElisseeffJ.Controlled differentiation of stem cells. Adv Drug Deliv Rev, 60:199. 2008.
3.
ParkH., CannizzaroC., Vunjak-NovakovicG., LangerR., VacantiC.A., FarokhzadO.C.Nanofabrication and microfabrication of functional materials for tissue engineering. Tissue Eng, 13:1867. 2007.
4.
HumesH.D., BuffingtonD.A., MacKayS.M., FunkeA.J., WeitzelW.F.Replacement of renal function in uremic animals with a tissue-engineered kidney. Nat Biotechnol, 17:451. 1999.
5.
MinuthW.W., SorokinL., SchumacherK.Generation of renal tubules at the interface of an artificial interstitium. Cell Physiol Biochem, 14:387. 2004.
6.
HeberS., DenkL., HuK., MinuthW.W.Modulating the development of renal tubules growing in serum-free culture medium at an artificial interstitium. Tissue Eng, 13:281. 2007.
KuboH., ShimizuT., YamatoM., FujimotoT., OkanoT.Creation of myocardial tubes using cardiomyocyte sheets and an in vitro cell sheet-wrapping device. Biomaterials, 28:3508. 2007.
9.
FranchiniJ.L., PropstJ.T., ComerG.R., YostM.J.Novel tissue engineered tubular heart tissue for in vitro pharmaceutical toxicity testing. Microsc Microanal, 13:267. 2007.
10.
OttH.C., MatthiesenT.S., GohS., BlackL.D., KrenS.M., NetoffT.I., TaylorD.A.Perfusion-decellularized matrix: using nature's platform to engineer a bioartificial heart. Nat Med, 14:213. 2008.
11.
ParenteauN.L., RosenbergL., Hardin-YoungJ.The engineering of tissues using progenitor cells. Curr Top Dev Biol, 64:101. 2004.
12.
BeckerC., JakseG.Stem cells for regeneration of urological structures. Eur Urol, 51:1217. 2007.
13.
KurosawaH.Methods for inducing embryoid body formation: in vitro differentiation system of embryonic stem cells. J Biosci Bioeng, 103:389. 2007.
14.
LubarskyB., KrasnowM.A.Tube morphogenesis: making and shaping biological tubes. Cell, 112:19. 2003.
15.
LoweryL., SiveH.Strategies of vertebrate neurulation and a re-evaluation of teleost neural tube formation. Mech Dev, 121:1189. 2004.
16.
SweetonD., ParksS., CostaM., WieschausU.Gastrulation in Drosophila: the formation of the ventral furrow and posterior midgut invaginations. Development, 112:775. 1991.
SchüpbachT.Germ line and soma cooperate during oogenesis to establish the dorsoventral pattern of egg shell and embryo in Drosophila melanogaster. Cell, 49:699. 1987.
24.
TwomblyV., BlackmanB.K., JinH., GraffJ.M., PadgettR.W., GelbartW.M.The TGF-beta signaling pathway is essential for Drosophila oogenesis. Development, 122:1555. 1996.
25.
XieT., SpradlingA.C.Decapentaplegic is essential for the maintenance and division of germline stem cells in the Drosophila ovary. Cell, 94:251. 1998.
26.
DuchekP., RØrthP.Guidance of cell migration by EGF receptor signaling during Drosophila oogenesis. Science, 291:131. 2001.
27.
McDonaldJ.A., PinheiroE.M., KadlecL., SchüpbachT., MontellD.J.Multiple EGFR ligands participate in guiding migrating border cells. Dev Biol, 296:94. 2006.
28.
GilboaL., LehmannR.Soma-germline interactions coordinate homeostasis and growth in the Drosophila gonad. Nature, 443:97. 2006.
29.
ShiloB.Z.Signaling by the Drosophila epidermal growth factor receptor pathway during development. Exp Cell Res, 284:140. 2003.
30.
AffolterM., BaslerK.The Decapentaplegic morphogen gradient: from pattern formation to growth regulation. Nat Rev Genet, 8:663. 2007.
31.
SpradlingA.C.BateM., Martinez-AriasA.Developmental genetics of oogenesis. The Development of Drosophila melanogaster, Vol. 1. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, 1993; 1–70.
32.
Mahajan-MiklosS., CooleyL.Intercellular cytoplasm transport during Drosophila oogenesis. Dev Biol, 165:336. 1994.
33.
RayR.P., SchüpbachT.Intercellular signaling and the polarization of body axes during Drosophila oogenesis. Genes Dev, 10:1711. 1996.
34.
RothS.The origin of dorsoventral polarity in Drosophila. Philos Trans R Soc Lond B Biol Sci, 358:1317. 2003.
35.
LeMosyE.K.Pattern formation: the eggshell holds the cue. Curr Biol, 13:R508. 2003.
36.
WaringG.L.Morphogenesis of the eggshell in Drosophila. Int Rev Cytol, 198:67. 2000.
37.
DobensL.L., RafteryL.A.Integration of epithelial patterning and morphogenesis in Drosophila ovarian follicle cells. Dev Dyn, 218:80. 2000.
38.
DormanJ.B., JamesK.E., FraserS.E., KiehartD.P., BergC.A.bullwinkle is required for epithelial morphogenesis during Drosophila oogenesis. Dev Biol, 267:320. 2004.
39.
Neuman-SilberbergF.S., SchüpbachT.Dorsoventral axis formation in Drosophila depends on the correct dosage of the gene gurken. Development, 120:2457. 1994.
40.
DengW.M., BownesM.Two signalling pathways specify localized expression of the Broad-Complex in Drosophila eggshell patterning and morphogenesis. Development, 124:4639. 1997.
41.
DobensL.L., PetersonJ.S., TreismanJ., RafteryL.A.Drosophila bunched integrates opposing DPP and EGF signals to set the operculum boundary. Development, 127:745. 2000.
42.
PeriF., RothS.Combined activities of Gurken and Decapentaplegic specify dorsal chorion structures of the Drosophila egg. Development, 127:841. 2000.
43.
ShravageB.V., AltmannG., TechnauM., RothS.The role of DPP and its inhibitors during eggshell patterning in Drosophila. Development, 134:2261. 2007.
44.
MorimotoA.M., JordanK.C., TietzeK., BrittonJ.S., O′NeillE.M., Ruohola-BakerH.Pointed, an ETS domain transcription factor, negatively regulates the EGF receptor pathway in Drosophila oogenesis. Development, 122:3745. 1996.
45.
WassermanJ.D., FreemanM.An autoregulatory cascade of EGF receptor signaling patterns the Drosophila egg. Cell, 95:355. 1998.
46.
SapirA., SchweitzerR., ShiloB.Z.Sequential activation of the EGF receptor pathway during Drosophila oogenesis establishes the dorsoventral axis. Development, 125:191. 1998.
47.
PeriF., BökelC., RothS.Local Gurken signaling and dynamic MAPK activation during Drosophila oogenesis. Mech Dev, 81:75. 1999.
48.
ChenY.and Schüpbach, T. The role of brinker in eggshell patterning. Mech Dev, 123:395. 2006.
49.
YakobyN., LembongJ., SchüpbachT., ShvartsmanS.Y.Drosophila eggshell is patterned by sequential action of feedforward and feedback loops. Development, 135:343. 2008.
50.
WardE.J., BergC.A.Juxtaposition between two cell types is necessary for dorsal appendage tube formation. Mech Dev, 122:241. 2005.
51.
WardE.J., ZhouX., RiddifordL.M., BergC.A., Ruohola-BakerH.Border of Notch activity establishes a boundary between the two dorsal appendage tube cell types. Dev Biol, 297:461. 2006.
52.
ShvartsmanS.Y., MuratovC.B., LauffenburgerD.A.Modeling and computational analysis of EGF receptor-mediated cell communication in Drosophila oogenesis. Development, 129:2577. 2002.
53.
GoentoroL.A., ReevesG.T., KowalC.P., MartinelliL., SchüpbachT., ShvartsmanS.Y.Quantifying the Gurken morphogen gradient in Drosophila oogenesis. Dev Cell, 11:263. 2006.
54.
ZegersM., O′BrienL., YuW., DattaA., MostovK.Epithelial polarity and tubulogenesis in vitro. Trends Cell Biol, 13:169. 2003.
55.
NelsonW.Tube morphogenesis: closure, but many openings remain. Trends Cell Biol, 13:615. 2003.
56.
AffolterM., BellusciS., ItohN., ShiloB., ThieryJ.P., WerbZ.Tube or not tube: remodeling epithelial tissues by branching morphogenesis. Dev Cell, 4:11. 2003.
57.
BeitelG.J., KrasnowM.A.Genetic control of epithelial tube size in the Drosophila tracheal system. Development, 127:3271. 2000.
58.
GhabrialA.S., KrasnowM.A.Social interactions among epithelial cells during tracheal branching morphogenesis. Nature, 441:746. 2006.
59.
EdwardsK.A., KiehartD.P.Drosophila nonmuscle myosin II has multiple essential roles in imaginal disc and egg chamber morphogenesis. Development, 122:1499. 1996.
NezisI.P., StravopodisD.J., PapassideriI., Robert-NicoudM., MargaritisL.H.Dynamics of apoptosis in the ovarian follicle cells during the late stages of Drosophila oogenesis. Cell Tissue Res, 307:401. 2002.
62.
OdellG.M., OsterG., AlberchP., BurnsideB.The mechanical basis of morphogenesis. I. Epithelial folding and invagination. Dev Biol, 85:446. 1981.
63.
PilotF., LecuitT.Compartmentalized morphogenesis in epithelia: from cell to tissue shape. Dev Dyn, 232:685. 2005.
64.
SnowP.M., BieberA.J., GoodmanC.S.Fasciclin III: a novel homophilic adhesion molecule in Drosophila. Cell, 59:313. 1989.
65.
RittenhouseK.R., BergC.A.Mutations in the Drosophila gene bullwinkle cause the formation of abnormal eggshell structures and bicaudal embryos. Development, 121:3023. 1995.
66.
TranD.H., BergC.A.bullwinkle and shark regulate dorsal-appendage morphogenesis in Drosophila oogenesis. Development, 130:6273. 2003.
67.
KerszbergM., ChangeuxJ.A simple molecular model of neurulation. BioEssays, 20:758. 1998.
68.
ZajacM., JonesG.L., GlazierJ.A.Model of convergent extension in animal morphogenesis. Phys Rev Lett, 85:2022. 2000.
69.
ZajacM., JonesG.L., GlazierJ.A.Simulating convergent extension by way of anisotropic differential adhesion. J Theor Biol, 222:247. 2003.
70.
JamesK.E., BergC.A.Temporal comparison of Broad-Complex expression during eggshell-appendage patterning and morphogenesis in two Drosophila species with different eggshell-appendage numbers. Gene Expr Patterns, 3:629. 2003.
