全部 标题 作者
关键词 摘要

OALib Journal期刊
ISSN: 2333-9721
费用:99美元

查看量下载量

相关文章

更多...
PLOS ONE  2013 

A Novel Role for Lh3 Dependent ECM Modifications during Neural Crest Cell Migration in Zebrafish

DOI: 10.1371/journal.pone.0054609

Full-Text   Cite this paper   Add to My Lib

Abstract:

During vertebrate development, trunk neural crest cells delaminate along the entire length of the dorsal neural tube and initially migrate as a non-segmented sheet. As they enter the somites, neural crest cells rearrange into spatially restricted segmental streams. Extracellular matrix components are likely to play critical roles in this transition from a sheet-like to a stream-like mode of migration, yet the extracellular matrix components and their modifying enzymes critical for this transition are largely unknown. Here, we identified the glycosyltransferase Lh3, known to modify extracellular matrix components, and its presumptive substrate Collagen18A1, to provide extrinsic signals critical for neural crest cells to transition from a sheet-like migration behavior to migrating as a segmental stream. Using live cell imaging we show that in lh3 null mutants, neural crest cells fail to transition from a sheet to a stream, and that they consequently enter the somites as multiple streams, or stall shortly after entering the somites. Moreover, we demonstrate that transgenic expression of lh3 in a small subset of somitic cells adjacent to where neural crest cells switch from sheet to stream migration restores segmental neural crest cell migration. Finally, we show that knockdown of the presumptive Lh3 substrate Collagen18A1 recapitulates the neural crest cell migration defects observed in lh3 mutants, consistent with the notion that Lh3 exerts its effect on neural crest cell migration by regulating post-translational modifications of Collagen18A1. Together these data suggest that Lh3–Collagen18A1 dependent ECM modifications regulate the transition of trunk neural crest cells from a non-segmental sheet like migration mode to a segmental stream migration mode.

References

[1]  Krull CE (2010) Neural crest cells and motor axons in avians: Common and distinct migratory molecules. Cell Adh Migr 4.
[2]  Erickson CA (1985) Control of neural crest cell dispersion in the trunk of the avian embryo. Dev Biol 111: 138–157.
[3]  Erickson CA, Weston JA (1983) An SEM analysis of neural crest migration in the mouse. J Embryol Exp Morphol 74: 97–118.
[4]  Loring JF, Erickson CA (1987) Neural crest cell migratory pathways in the trunk of the chick embryo. Dev Biol 121: 220–236.
[5]  Bronner-Fraser M (1986) Analysis of the early stages of trunk neural crest migration in avian embryos using monoclonal antibody HNK-1. Dev Biol 115: 44–55.
[6]  Rickmann M, Fawcett JW, Keynes RJ (1985) The migration of neural crest cells and the growth of motor axons through the rostral half of the chick somite. J Embryol Exp Morphol 90: 437–455.
[7]  Serbedzija GN, Fraser SE, Bronner-Fraser M (1990) Pathways of trunk neural crest cell migration in the mouse embryo as revealed by vital dye labelling. Development 108: 605–612.
[8]  Banerjee S, Gordon L, Donn TM, Berti C, Moens CB, et al. (2011) A novel role for MuSK and non-canonical Wnt signaling during segmental neural crest cell migration. Development 138: 3287–3296.
[9]  Bronner-Fraser M, Stern C (1991) Effects of mesodermal tissues on avian neural crest cell migration. Dev Biol 143: 213–217.
[10]  Kalcheim C, Teillet MA (1989) Consequences of somite manipulation on the pattern of dorsal root ganglion development. Development 106: 85–93.
[11]  Krull CE, Lansford R, Gale NW, Collazo A, Marcelle C, et al. (1997) Interactions of Eph-related receptors and ligands confer rostrocaudal pattern to trunk neural crest migration. Curr Biol 7: 571–580.
[12]  McLennan R, Krull CE (2002) Ephrin-as cooperate with EphA4 to promote trunk neural crest migration. Gene Expr 10: 295–305.
[13]  Santiago A, Erickson CA (2002) Ephrin-B ligands play a dual role in the control of neural crest cell migration. Development 129: 3621–3632.
[14]  Roffers-Agarwal J, Gammill LS (2009) Neuropilin receptors guide distinct phases of sensory and motor neuronal segmentation. Development 136: 1879–1888.
[15]  Schwarz Q, Maden CH, Davidson K, Ruhrberg C (2009) Neuropilin-mediated neural crest cell guidance is essential to organise sensory neurons into segmented dorsal root ganglia. Development 136: 1785–1789.
[16]  Schwarz Q, Maden CH, Vieira JM, Ruhrberg C (2009) Neuropilin 1 signaling guides neural crest cells to coordinate pathway choice with cell specification. Proc Natl Acad Sci U S A 106: 6164–6169.
[17]  Perris R, Perissinotto D (2000) Role of the extracellular matrix during neural crest cell migration. Mech Dev 95: 3–21.
[18]  Halloran MC, Berndt JD (2003) Current progress in neural crest cell motility and migration and future prospects for the zebrafish model system. Dev Dyn 228: 497–513.
[19]  Eisen JS, Weston JA (1993) Development of the neural crest in the zebrafish. Dev Biol 159: 50–59.
[20]  Raible DW, Wood A, Hodsdon W, Henion PD, Weston JA, et al. (1992) Segregation and early dispersal of neural crest cells in the embryonic zebrafish. Dev Dyn 195: 29–42.
[21]  Kivirikko KI, Pihlajaniemi T (1998) Collagen hydroxylases and the protein disulfide isomerase subunit of prolyl 4-hydroxylases. Adv Enzymol Relat Areas Mol Biol 72: 325–398.
[22]  Bronner-Fraser M (1994) Neural crest cell formation and migration in the developing embryo. Faseb J 8: 699–706.
[23]  Pike SH, Melancon EF, Eisen JS (1992) Pathfinding by zebrafish motoneurons in the absence of normal pioneer axons. Development 114: 825–831.
[24]  Zeller J, Granato M (1999) The zebrafish diwanka gene controls an early step of motor growth cone migration. Development 126: 3461–3472.
[25]  Schneider VA, Granato M (2006) The myotomal diwanka (lh3) glycosyltransferase and type XVIII collagen are critical for motor growth cone migration. Neuron 50: 683–695.
[26]  Honjo Y, Eisen JS (2005) Slow muscle regulates the pattern of trunk neural crest migration in zebrafish. Development 132: 4461–4470.
[27]  Elworthy S, Lister JA, Carney TJ, Raible DW, Kelsh RN (2003) Transcriptional regulation of mitfa accounts for the sox10 requirement in zebrafish melanophore development. Development 130: 2809–2818.
[28]  Glasgow E, Tomarev SI (1998) Restricted expression of the homeobox gene prox 1 in developing zebrafish. Mech Dev 76: 175–178.
[29]  Roy S, Wolff C, Ingham PW (2001) The u-boot mutation identifies a Hedgehog-regulated myogenic switch for fiber-type diversification in the zebrafish embryo. Genes Dev 15: 1563–1576.
[30]  Elamaa H, Peterson J, Pihlajaniemi T, Destree O (2002) Cloning of three variants of type XVIII collagen and their expression patterns during Xenopus laevis development. Mech Dev 114: 109–113.
[31]  Ackley BD, Crew JR, Elamaa H, Pihlajaniemi T, Kuo CJ, et al. (2001) The NC1/endostatin domain of Caenorhabditis elegans type XVIII collagen affects cell migration and axon guidance. J Cell Biol 152: 1219–1232.
[32]  Meyer F, Moussian B (2009) Drosophila multiplexin (Dmp) modulates motor axon pathfinding accuracy. Dev Growth Differ 51: 483–498.
[33]  Salo AM, Wang C, Sipila L, Sormunen R, Vapola M, et al. (2006) Lysyl hydroxylase 3 (LH3) modifies proteins in the extracellular space, a novel mechanism for matrix remodeling. J Cell Physiol 207: 644–653.
[34]  Myllyla R, Wang C, Heikkinen J, Juffer A, Lampela O, et al. (2007) Expanding the lysyl hydroxylase toolbox: new insights into the localization and activities of lysyl hydroxylase 3 (LH3). J Cell Physiol 212: 323–329.
[35]  Myllyharju J, Kivirikko KI (2004) Collagens, modifying enzymes and their mutations in humans, flies and worms. Trends Genet 20: 33–43.
[36]  Tucker RP, Hagios C, Chiquet-Ehrismann R, Lawler J, Hall RJ, et al. (1999) Thrombospondin-1 and neural crest cell migration. Dev Dyn 214: 312–322.
[37]  Risteli M, Ruotsalainen H, Salo AM, Sormunen R, Sipila L, et al. (2009) Reduction of lysyl hydroxylase 3 causes deleterious changes in the deposition and organization of extracellular matrix. J Biol Chem 284: 28204–28211.
[38]  Mullins MC, Hammerschmidt M, Haffter P, Nusslein-Volhard C (1994) Large-scale mutagenesis in the zebrafish: in search of genes controlling development in a vertebrate. Curr Biol 4: 189–202.
[39]  van Eeden FJ, Granato M, Schach U, Brand M, Furutani-Seiki M, et al. (1996) Mutations affecting somite formation and patterning in the zebrafish, Danio rerio. Development 123: 153–164.
[40]  Flanagan-Steet H, Fox MA, Meyer D, Sanes JR (2005) Neuromuscular synapses can form in vivo by incorporation of initially aneural postsynaptic specializations. Development 132: 4471–4481.
[41]  Kirby BB, Takada N, Latimer AJ, Shin J, Carney TJ, et al. (2006) In vivo time-lapse imaging shows dynamic oligodendrocyte progenitor behavior during zebrafish development. Nat Neurosci 9: 1506–1511.
[42]  Jing L, Lefebvre JL, Gordon LR, Granato M (2009) Wnt signals organize synaptic prepattern and axon guidance through the zebrafish unplugged/MuSK receptor. Neuron 61: 721–733.
[43]  Zeller J, Schneider V, Malayaman S, Higashijima S, Okamoto H, et al. (2002) Migration of zebrafish spinal motor nerves into the periphery requires multiple myotome-derived cues. Dev Biol 252: 241–256.
[44]  Trevarrow B, Marks DL, Kimmel CB (1990) Organization of hindbrain segments in the zebrafish embryo. Neuron 4: 669–679.
[45]  Luo R, An M, Arduini BL, Henion PD (2001) Specific pan-neural crest expression of zebrafish Crestin throughout embryonic development. Dev Dyn 220: 169–174.

Full-Text

Contact Us

service@oalib.com

QQ:3279437679

WhatsApp +8615387084133