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Centrosomes in Branching Morphogenesis

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The Golgi Apparatus and Centriole

Part of the book series: Results and Problems in Cell Differentiation ((RESULTS,volume 67))

Abstract

The centrosome, a major microtubule organizer, has important functions in regulating the cytoskeleton as well as the position of cellular structures and orientation of cells within tissues. The centrosome serves as the main cytoskeleton-organizing centre in the cell and is the classical site of microtubule nucleation and anchoring. For these reasons, centrosomes play a very important role in morphogenesis, not just in the early stages of cell divisions but also in the later stages of organogenesis. Many organs such as lung, kidney and blood vessels develop from epithelial tubes that branch into complex networks. Cells in the nervous system also form highly branched structures in order to build complex neuronal networks. During branching morphogenesis, cells have to rearrange within tissues though multicellular branching or through subcellular branching, also known as single-cell branching. For highly branched structures to be formed during embryonic development, the cytoskeleton needs to be extensively remodelled. The centrosome has been shown to play an important role during these events.

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References

  • Affolter M, Caussinus E (2008) Tracheal branching morphogenesis in Drosophila: new insights into cell behaviour and organ architecture. Development 135:2055–2064

    Article  CAS  Google Scholar 

  • Ahmad FJ, Baas PW (1995) Microtubules released from the neuronal centrosome are transported into the axon. J Cell Sci 108 (Pt 8):2761–2769

    Google Scholar 

  • Ahmad FJ, Echeverri CJ, Vallee RB, Baas PW (1998) Cytoplasmic dynein and dynactin are required for the transport of microtubules into the axon. J Cell Biol 140:391–401

    Article  CAS  Google Scholar 

  • Andersen EF, Halloran MC (2012) Centrosome movements in vivo correlate with specific neurite formation downstream of LIM homeodomain transcription factor activity. Development 139:3590–3599

    Article  CAS  Google Scholar 

  • Avidor-Reiss T, Gopalakrishnan J (2013) Building a centriole. Curr Opin Cell Biol 25:72–77

    Article  CAS  Google Scholar 

  • Aydogan V, Lenard A, Denes AS, Sauteur L, Belting H-G, Affolter M (2015) Endothelial cell division in angiogenic sprouts of differing cellular architecture. Biology Open 4:1259–1269

    Article  CAS  Google Scholar 

  • Baas PW, Rao AN, Matamoros AJ, Leo L (2016) Stability properties of neuronal microtubules. Cytoskeleton (Hoboken) 73:442–460

    Article  CAS  Google Scholar 

  • Barker AR, Mcintosh KV, Dawe HR (2016) Centrosome positioning in non-dividing cells. Protoplasma 253:1007–1021

    Article  Google Scholar 

  • Battini L, Macip S, Fedorova E, Dikman S, Somlo S, Montagna C, Gusella GL (2008) Loss of polycystin-1 causes centrosome amplification and genomic instability. Hum Mol Genet 17:2819–2833

    Article  CAS  Google Scholar 

  • Bonini SA, Mastinu A, Ferrari-Toninelli G, Memo M (2017) Potential role of microtubule stabilizing agents in neurodevelopmental disorders. Int J Mol Sci 18(8). https://doi.org/10.3390/ijms18081627

    Article  Google Scholar 

  • Brodu V, Baffet AD, Le Droguen P-M, Casanova J, Guichet A (2010) A developmentally regulated two-step process generates a noncentrosomal microtubule network in Drosophila tracheal cells. Dev Cell 18:790–801

    Article  CAS  Google Scholar 

  • Conde C, Cáceres A (2009) Microtubule assembly, organization and dynamics in axons and dendrites. Nat Rev Neurosci 10:319–332

    Article  CAS  Google Scholar 

  • Corthesy-Theulaz I, Pauloin A, Pfeffer SR (1992) Cytoplasmic dynein participates in the centrosomal localization of the Golgi complex. J Cell Biol 118:1333–1345

    Article  CAS  Google Scholar 

  • Craig AM, Banker G (1994) Neuronal polarity. Annu Rev Neurosci 17:267–310

    Article  CAS  Google Scholar 

  • Davis GE, Koh W, Stratman AN (2007) Mechanisms controlling human endothelial lumen formation and tube assembly in three-dimensional extracellular matrices. Birth Defects Res C Embryo Today 81:270–285

    Article  CAS  Google Scholar 

  • De Anda FC, Pollarolo G, Da Silva JS, Camoletto PG, Feiguin F, Dotti CG (2005) Centrosome localization determines neuronal polarity. Nature 436:704–708

    Article  Google Scholar 

  • Delandre C, Amikura R, Moore AW (2016) Microtubule nucleation and organization in dendrites. Cell Cycle 15:1685–1692

    Article  CAS  Google Scholar 

  • Diaz-Corrales FJ, Asanuma M, Miyazaki I, Miyoshi K, Ogawa N (2005) Rotenone induces aggregation of gamma-tubulin protein and subsequent disorganization of the centrosome: relevance to formation of inclusion bodies and neurodegeneration. Neuroscience 133:117–135

    Article  CAS  Google Scholar 

  • Dionne LK, Shim K, Hoshi M, Cheng T, Wang J, Marthiens V, Knoten A, Basto R, Jain S, Mahjoub MR (2018) Centrosome amplification disrupts renal development and causes cystogenesis. J Cell Biol 217:2485–2501

    Article  CAS  Google Scholar 

  • Fischer E, Legue E, Doyen A, Nato F, Nicolas J-F, Torres V, Yaniv M, Pontoglio M (2006) Defective planar cell polarity in polycystic kidney disease. Nat Genet 38:21–23

    Article  CAS  Google Scholar 

  • Gervais L, Casanova J (2010) In vivo coupling of cell elongation and lumen formation in a single cell. Curr Biol 20:359–366

    Article  CAS  Google Scholar 

  • Ghabrial A, Luschnig S, Metzstein M, Krasnow M (2003) Branching morphogenesis of the Drosophila tracheal system. Annu Rev Cell Dev Biol 19:623–647

    Article  CAS  Google Scholar 

  • Gierke S, Wittmann T (2012) EB1-recruited microtubule +TIP complexes coordinate protrusion dynamics during 3D epithelial remodeling. Curr Biol 22:753–762

    Article  CAS  Google Scholar 

  • Godinho SA, Picone R, Burute M, Dagher R, Su Y, Leung CT, Polyak K, Brugge JS, Théry M, Pellman D (2014) Oncogene-like induction of cellular invasion from centrosome amplification. Nature 510(7503):167–171

    Article  CAS  Google Scholar 

  • Hames RS, Crookes RE, Straatman KR, Merdes A, Hayes MJ, Faragher AJ, Fry AM (2005) Dynamic recruitment of Nek2 kinase to the centrosome involves microtubules, PCM-1, and localized proteasomal degradation. Mol Biol Cell 16:1711–1724

    Article  CAS  Google Scholar 

  • Hayashi S, Kondo T (2018) Development and function of the Drosophila tracheal system. Genetics 209:367–380

    Article  CAS  Google Scholar 

  • Higginbotham HR, Gleeson JG (2007) The centrosome in neuronal development. Trends Neurosci 30:276–283

    Article  CAS  Google Scholar 

  • Jayanandanan N, Mathew R, Leptin M (2014) Guidance of subcellular tubulogenesis by actin under the control of a synaptotagmin-like protein and Moesin. Nat Commun 5:3036

    Article  CAS  Google Scholar 

  • Jing Z, Yin H, Wang P, Gao J, Yuan L (2016) Centlein, a novel microtubule-associated protein stabilizing microtubules and involved in neurite formation. Biochem Biophys Res Commun 472:360–365

    Article  CAS  Google Scholar 

  • Kapitein LC, Hoogenraad CC (2015) Building the neuronal microtubule cytoskeleton. Neuron 87:492–506

    Article  CAS  Google Scholar 

  • Kim A, Puram S, Bilimoria P, Ikeuchi Y, Keough S, Wong M, Rowitch D, Bonni A (2009) A centrosomal Cdc20-Apc pathway controls dendrite morphogenesis in postmitotic neurons. Cell 136:322–336

    Article  CAS  Google Scholar 

  • Klämbt C, Glazer L, Shilo BZ (1992) Breathless, a Drosophila FGF receptor homolog, is essential for migration of tracheal and specific midline glial cells. Genes Dev 6:1668–1678

    Article  Google Scholar 

  • Kotini MP, Mäe MA, Belting H-G, Betsholtz C, Affolter M (2018) Sprouting and anastomosis in the Drosophila trachea and the vertebrate vasculature: similarities and differences in cell behaviour. Vascular pharmacol 112:8–16

    Article  Google Scholar 

  • Kuijpers M, Hoogenraad CC (2011) Centrosomes, microtubules and neuronal development. Mol Cell Neurosci 48(4):349–358

    Article  CAS  Google Scholar 

  • Kushner EJ, Ferro LS, Liu J-Y, Durrant JR, Rogers SL, Dudley AC, Bautch VL (2014) Excess centrosomes disrupt endothelial cell migration via centrosome scattering. J Cell Biol 206:257–272

    Article  CAS  Google Scholar 

  • Kushner EJ, Ferro LS, Yu Z, Bautch VL (2016) Excess centrosomes perturb dynamic endothelial cell repolarization during blood vessel formation. Mol Biol Cell 27:1911–1920

    Article  CAS  Google Scholar 

  • Lee T, Hacohen N, Krasnow M, Montell DJ (1996) Regulated breathless receptor tyrosine kinase activity required to pattern cell migration and branching in the Drosophila tracheal system. Genes Dev 10:2912–2921

    Article  CAS  Google Scholar 

  • Luxton GWG, Gundersen GG (2011) Orientation and function of the nuclear-centrosomal axis during cell migration. Curr Opin Cell Biol 23:579–588

    Article  CAS  Google Scholar 

  • Madero-Perez J, Fdez E, Fernandez B, Lara Ordonez AJ, Blanca Ramirez M, Gomez-Suaga P, Waschbusch D, Lobbestael E, Baekelandt V, Nairn AC, Ruiz-Martinez J, Aiastui A, Lopez De Munain A, Lis P, Comptdaer T, Taymans JM, Chartier-Harlin MC, Beilina A, Gonnelli A, Cookson MR, Greggio E, Hilfiker S (2018) Parkinson disease-associated mutations in LRRK2 cause centrosomal defects via Rab8a phosphorylation. Mol Neurodegener 13:3

    Article  Google Scholar 

  • Makanya AN, Hlushchuk R, Djonov VG (2009) Intussusceptive angiogenesis and its role in vascular morphogenesis, patterning, and remodeling. Angiogenesis 12:113–123

    Article  CAS  Google Scholar 

  • Manning G, Krasnow MA (1993) Development of the Drosophila tracheal system. In: Bate M, Martínez-Arias A (eds) The development of Drosophila melanogaster. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY

    Google Scholar 

  • Martin M, Veloso A, Wu J, Katrukha EA, Akhmanova A (2018) Control of endothelial cell polarity and sprouting angiogenesis by non-centrosomal microtubules. eLife 7:R162

    Google Scholar 

  • Nguyen MM, Stone MC, Rolls MM (2011) Microtubules are organized independently of the centrosome in Drosophila neurons. Neural Dev 6:38

    Article  CAS  Google Scholar 

  • Nguyen MM, Mccracken CJ, Milner ES, Goetschius DJ, Weiner AT, Long MK, Michael NL, Munro S, Rolls MM (2014) Gamma-tubulin controls neuronal microtubule polarity independently of Golgi outposts. Mol Biol Cell 25:2039–2050

    Article  Google Scholar 

  • Nishimura M, Inoue Y, Hayashi S (2007) A wave of EGFR signaling determines cell alignment and intercalation in the Drosophila tracheal placode. Development 134:4273–4282

    Article  CAS  Google Scholar 

  • Ochoa-Espinosa A, Affolter M (2012) Branching morphogenesis: from cells to organs and back. Cold Spring Harb Perspect Biol 4(10). https://doi.org/10.1101/cshperspect.a008243

    Article  Google Scholar 

  • Ogura Y, Wen FL, Sami MM, Shibata T, Hayashi S (2018) A switch-like activation relay of EGFR-ERK signaling regulates a wave of cellular contractility for epithelial invagination. Dev Cell 46:162–172 e5

    Article  CAS  Google Scholar 

  • Ori-Mckenney KM, Jan LY, Jan Y-N (2012) Golgi outposts shape dendrite morphology by functioning as sites of acentrosomal microtubule nucleation in neurons. Neuron 76:921–930

    Article  CAS  Google Scholar 

  • Petry S, Vale RD (2015) Microtubule nucleation at the centrosome and beyond. Nat Cell Biol 17:1089–1093

    Article  CAS  Google Scholar 

  • Puram SV, Kim AH, Park H-Y, Anckar J, Bonni A (2013) The ubiquitin receptor S5a/Rpn10 links centrosomal proteasomes with dendrite development in the mammalian brain. Cell Rep 4(1):19–30

    Article  CAS  Google Scholar 

  • Ricolo D, Deligiannaki M, Casanova J, Araújo SJ (2016) Centrosome amplification increases single-cell branching in post-mitotic cells. Curr Biol 26:2805–2813

    Article  CAS  Google Scholar 

  • Rodríguez-Fraticelli AE, Auzan M, Alonso MA, Bornens M, Martín-Belmonte F (2012) Cell confinement controls centrosome positioning and lumen initiation during epithelial morphogenesis. J Cell Biol 198:1011–1023

    Article  Google Scholar 

  • Sanchez-Huertas C, Luders J (2015) The augmin connection in the geometry of microtubule networks. Curr Biol 25:R294–R299

    Article  CAS  Google Scholar 

  • Sanchez-Huertas C, Freixo F, Viais R, Lacasa C, Soriano E, Luders J (2016) Non-centrosomal nucleation mediated by augmin organizes microtubules in post-mitotic neurons and controls axonal microtubule polarity. Nat Commun 7:12187

    Article  CAS  Google Scholar 

  • Sanders AA, Kaverina I (2015) Nucleation and dynamics of Golgi-derived microtubules. Front Neurosci 9:431

    Article  Google Scholar 

  • Schnatwinkel C, Niswander L (2012) Nubp1 is required for lung branching morphogenesis and distal progenitor cell survival in mice. PLoS One 7:e44871

    Article  CAS  Google Scholar 

  • Schottenfeld-Roames J, Ghabrial AS (2012) Whacked and Rab35 polarize dynein-motor-complex-dependent seamless tube growth. Nat Cell Biol 14(4):386–393

    Article  CAS  Google Scholar 

  • Schottenfeld-Roames J, Rosa JB, Ghabrial AS (2014) Seamless tube shape is constrained by endocytosis-dependent regulation of active moesin. Curr Biol 24:1756–1764

    Article  CAS  Google Scholar 

  • Sharp DJ, Yu W, Baas PW (1995) Transport of dendritic microtubules establishes their nonuniform polarity orientation. J Cell Biol 130:93–103

    Article  CAS  Google Scholar 

  • Sigurbjörnsdóttir S, Mathew R, Leptin M (2014) Molecular mechanisms of de novo lumen formation. Nat Rev Mol Cell Biol 15:665–676

    Article  Google Scholar 

  • Stiess M, Maghelli N, Kapitein LC, Gomis-Rüth S, Wilsch-Bräuninger M, Hoogenraad CC, Tolić-Nørrelykke IM, Bradke F (2010) Axon extension occurs independently of centrosomal microtubule nucleation. Science 327:704–707

    Article  CAS  Google Scholar 

  • Sutherland D, Samakovlis C, Krasnow MA (1996) Branchless encodes a Drosophila FGF homolog that controls tracheal cell migration and the pattern of branching. Cell 87:1091–1101

    Article  CAS  Google Scholar 

  • Tang N, Marshall WF (2012) Centrosome positioning in vertebrate development. J Cell Sci 125:4951–4961

    Article  CAS  Google Scholar 

  • Tang N, Marshall WF, McMahon M, Metzger RJ, Martin GR (2011) Control of mitotic spindle angle by the RAS-regulated ERK1/2 pathway determines lung tube shape. Science 333(6040):342–345. https://doi.org/10.1126/science.1204831

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yalgin C, Ebrahimi S, Delandre C, Yoong LF, Akimoto S, Tran H, Amikura R, Spokony R, Torben-Nielsen B, White KP, Moore AW (2015) Centrosomin represses dendrite branching by orienting microtubule nucleation. Nat Neurosci 18:1437–1445

    Article  CAS  Google Scholar 

  • Yu W, Qiang L, Solowska JM, Karabay A, Korulu S, Baas PW (2008) The microtubule-severing proteins spastin and katanin participate differently in the formation of axonal branches. Mol Biol Cell 19:1485–1498

    Article  CAS  Google Scholar 

  • Zeng G, Taylor SM, Mccolm JR, Kappas NC, Kearney JB, Williams LH, Hartnett ME, Bautch VL (2007) Orientation of endothelial cell division is regulated by VEGF signaling during blood vessel formation. Blood 109:1345–1352

    Article  CAS  Google Scholar 

  • Zmuda JF, Rivas RJ (1998) The Golgi apparatus and the centrosome are localized to the sites of newly emerging axons in cerebellar granule neurons in vitro. Cell Motil Cytoskeleton 41:18–38

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Genetics, Microbiology and Statistics, School of Biology, University of Barcelona, Barcelona, Spain

    Sofia J. Araújo

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  1. Sofia J. Araújo
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Correspondence to Sofia J. Araújo .

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  1. Department of Surgery, Houston Methodist Hospital, Houston, TX, USA

    Malgorzata Kloc

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Araújo, S.J. (2019). Centrosomes in Branching Morphogenesis. In: Kloc, M. (eds) The Golgi Apparatus and Centriole. Results and Problems in Cell Differentiation, vol 67. Springer, Cham. https://doi.org/10.1007/978-3-030-23173-6_13

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