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  2012 

Regulation of Motility of Myogenic Cells in Filling Limb Muscle Anlagen by Pitx2

DOI: 10.1371/journal.pone.0035822

Full-Text   Cite this paper   Add to My Lib

Abstract:

Cells of the ventrolateral dermomyotome delaminate and migrate into the limb buds where they give rise to all muscles of the limbs. The migratory cells proliferate and form myoblasts, which withdraw from the cell cycle to become terminally differentiated myocytes. The myogenic lineage colonizes pre-patterned regions to form muscle anlagen as muscle fibers are assembled. The regulatory mechanisms that control the later steps of this myogenic program are not well understood. The homeodomain transcription factor Pitx2 is expressed specifically in the muscle lineage from the migration of precursors to adult muscle. Ablation of Pitx2 results in distortion, rather than loss, of limb muscle anlagen, suggesting that its function becomes critical during the colonization of, and/or fiber assembly in, the anlagen. Microarrays were used to identify changes in gene expression in flow-sorted migratory muscle precursors, labeled by Lbx1EGFP/+, which resulted from the loss of Pitx2. Very few genes showed changes in expression. Many small-fold, yet significant, changes were observed in genes encoding cytoskeletal and adhesion proteins which play a role in cell motility. Myogenic cells from genetically-tagged mice were cultured and subjected to live cell-tracking analysis using time-lapse imaging. Myogenic cells lacking Pitx2 were smaller, more symmetrical, and had more actin bundling. They also migrated about half of the total distance and velocity. Decreased motility may prevent myogenic cells from filling pre-patterned regions of the limb bud in a timely manner. Altered shape may prevent proper assembly of higher-order fibers within anlagen. Pitx2 therefore appears to regulate muscle anlagen development by appropriately balancing expression of cytoskeletal and adhesion molecules.

References

[1]  Tremblay P, Dietrich S, Mericskay M, Schubert FR, Li Z, et al. (1998) A crucial role for Pax3 in the development of the hypaxial musculature and the long-range migration of muscle precursors. Dev Biol 203: 49–61.
[2]  Venters SJ, Argent RE, Deegan FM, Perez-Baron G, Wong TS, et al. (2004) Precocious terminal differentiation of premigratory limb muscle precursor cells requires positive signalling. Dev Dyn 229: 591–599.
[3]  Bladt F, Riethmacher D, Isenmann S, Aguzzi A, Birchmeier C (1995) Essential role for the c-met receptor in the migration of myogenic precursor cells into the limb bud. Nature 376: 768–771.
[4]  Dietrich S, Abou-Rebyeh F, Brohmann H, Bladt F, Sonnenberg-Riethmacher E, et al. (1999) The role of SF/HGF and c-Met in the development of skeletal muscle. Development 126: 1621–1629.
[5]  Hayashi K, Ozawa E (1995) Myogenic cell migration from somites is induced by tissue contact with medial region of the presumptive limb mesoderm in chick embryos. Development 121: 661–669.
[6]  Gross MK, Moran-Rivard L, Velasquez T, Nakatsu MN, Jagla K, et al. (2000) Lbx1 is required for muscle precursor migration along a lateral pathway into the limb. Development 127: 413–424.
[7]  Goulding M, Lumsden A, Paquette AJ (1994) Regulation of Pax-3 expression in the dermomyotome and its role in muscle development. Development 120: 957–971.
[8]  Bober E, Franz T, Arnold HH, Gruss P, Tremblay P (1994) Pax-3 is required for the development of limb muscles: a possible role for the migration of dermomyotomal muscle progenitor cells. Development 120: 603–612.
[9]  Mennerich D, Schafer K, Braun T (1998) Pax-3 is necessary but not sufficient for lbx1 expression in myogenic precursor cells of the limb. Mech Dev 73: 147–158.
[10]  Schafer K, Braun T (1999) Early specification of limb muscle precursor cells by the homeobox gene Lbx1h. Nature Genetics 23: 213–216.
[11]  Gurdon JB (1988) A community effect in animal development. Nature 336: 772–774.
[12]  Hynes RO (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110: 673–687.
[13]  Zaidel-Bar R, Milo R, Kam Z, Geiger B (2007) A paxillin tyrosine phosphorylation switch regulates the assembly and form of cell-matrix adhesions. J Cell Sci 120: 137–148.
[14]  Otey CA, Carpen O (2004) Alpha-actinin revisited: a fresh look at an old player. Cell Motil Cytoskeleton 58: 104–111.
[15]  Campbell ID, Ginsberg MH (2004) The talin-tail interaction places integrin activation on FERM ground. Trends Biochem Sci 29: 429–435.
[16]  Ziegler WH, Liddington RC, Critchley DR (2006) The structure and regulation of vinculin. Trends Cell Biol 16: 453–460.
[17]  Amano M, Chihara K, Kimura K, Fukata Y, Nakamura N, et al. (1997) Formation of actin stress fibers and focal adhesions enhanced by Rho-kinase. Science 275: 1308–1311.
[18]  Shih HP, Gross MK, Kioussi C (2007) Cranial muscle defects of Pitx2 mutants result from specification defects in the first branchial arch. Proc Natl Acad Sci U S A 104: 5907–5912.
[19]  Shih HP, Gross MK, Kioussi C (2007) Expression pattern of the homeodomain transcription factor Pitx2 during muscle development. Gene Expr Patterns 7: 441–451.
[20]  Shih HP, Gross MK, Kioussi C (2008) Muscle development: forming the head and trunk muscles. Acta Histochem 110: 97–108.
[21]  Lu MF, Pressman C, Dyer R, Johnson RL, Martin JF (1999) Function of Rieger syndrome gene in left-right asymmetry and craniofacial development. Nature 401: 276–278.
[22]  Lin CR, Kioussi C, O'Connell S, Briata P, Szeto D, et al. (1999) Pitx2 regulates lung asymmetry, cardiac positioning and pituitary and tooth morphogenesis. Nature 401: 279–282.
[23]  Gage PJ, Suh H, Camper SA (1999) Dosage requirement of Pitx2 for development of multiple organs. Development 126: 4643–4651.
[24]  Kitamura K, Miura H, Miyagawa-Tomita S, Yanazawa M, Katoh-Fukui Y, et al. (1999) Mouse Pitx2 deficiency leads to anomalies of the ventral body wall, heart, extra- and periocular mesoderm and right pulmonary isomerism. Development 126: 5749–5758.
[25]  Kioussi C, Briata P, Baek SH, Rose DW, Hamblet NS, et al. (2002) Identification of a Wnt/Dvl/beta-Catenin –> Pitx2 pathway mediating cell-type-specific proliferation during development. Cell 111: 673–685.
[26]  Hilton T, Gross MK, Kioussi C (2010) Pitx2-dependent occupancy by histone deacetylases is associated with T-box gene regulation in mammalian abdominal tissue. J Biol Chem 285: 11129–11142.
[27]  Bershadsky A, Chausovsky A, Becker E, Lyubimova A, Geiger B (1996) Involvement of microtubules in the control of adhesion-dependent signal transduction. Curr Biol 6: 1279–1289.
[28]  Gu J, Tamura M, Pankov R, Danen EH, Takino T, et al. (1999) Shc and FAK differentially regulate cell motility and directionality modulated by PTEN. Journal of Cell Biology 146: 389–403.
[29]  Gail M (1973) Time lapse studies on the motility of fibroblasts in tissue culture. Ciba Found Symp 14: 287–310.
[30]  Locascio A, Nieto MA (2001) Cell movements during vertebrate development: integrated tissue behaviour versus individual cell migration. Curr Opin Genet Dev 11: 464–469.
[31]  Carlier MF, Le Clainche C, Wiesner S, Pantaloni D (2003) Actin-based motility: from molecules to movement. Bioessays 25: 336–345.
[32]  Bandman E (1992) Contractile protein isoforms in muscle development. Dev Biol 154: 273–283.
[33]  Hayward LJ, Zhu YY, Schwartz RJ (1988) Cellular localization of muscle and nonmuscle actin mRNAs in chicken primary myogenic cultures: the induction of alpha-skeletal actin mRNA is regulated independently of alpha-cardiac actin gene expression. Journal of Cell Biology 106: 2077–2086.
[34]  Gunning PW, Ferguson V, Brennan KJ, Hardeman EC (2001) Alpha-skeletal actin induces a subset of muscle genes independently of muscle differentiation and withdrawal from the cell cycle. J Cell Sci 114: 513–524.
[35]  Jain MK, Kashiki S, Hsieh CM, Layne MD, Yet SF, et al. (1998) Embryonic expression suggests an important role for CRP2/SmLIM in the developing cardiovascular system. Circ Res 83: 980–985.
[36]  Lilly B, Clark KA, Yoshigi M, Pronovost S, Wu ML, et al. (2010) Loss of the serum response factor cofactor, cysteine-rich protein 1, attenuates neointima formation in the mouse. Arterioscler Thromb Vasc Biol 30: 694–701.
[37]  Wei Q, Adelstein RS (2002) Pitx2a expression alters actin-myosin cytoskeleton and migration of HeLa cells through Rho GTPase signaling. Molecular Biology of the Cell 13: 683–697.
[38]  Small JV, Geiger B, Kaverina I, Bershadsky A (2002) How do microtubules guide migrating cells? Nat Rev Mol Cell Biol 3: 957–964.
[39]  Blaxall BC, Spang R, Rockman HA, Koch WJ (2003) Differential myocardial gene expression in the development and rescue of murine heart failure. Physiol Genomics 15: 105–114.
[40]  Gertler FB, Niebuhr K, Reinhard M, Wehland J, Soriano P (1996) Mena, a relative of VASP and Drosophila Enabled, is implicated in the control of microfilament dynamics. Cell 87: 227–239.
[41]  Barzik M, Kotova TI, Higgs HN, Hazelwood L, Hanein D, et al. (2005) Ena/VASP proteins enhance actin polymerization in the presence of barbed end capping proteins. J Biol Chem 280: 28653–28662.
[42]  Mikhailov A, Gundersen GG (1998) Relationship between microtubule dynamics and lamellipodium formation revealed by direct imaging of microtubules in cells treated with nocodazole or taxol. Cell Motil Cytoskeleton 41: 325–340.
[43]  Al-Bassam J, Ozer RS, Safer D, Halpain S, Milligan RA (2002) MAP2 and tau bind longitudinally along the outer ridges of microtubule protofilaments. Journal of Cell Biology 157: 1187–1196.
[44]  Daub H, Gevaert K, Vandekerckhove J, Sobel A, Hall A (2001) Rac/Cdc42 and p65PAK regulate the microtubule-destabilizing protein stathmin through phosphorylation at serine 16. J Biol Chem 276: 1677–1680.
[45]  Jourdain L, Curmi P, Sobel A, Pantaloni D, Carlier MF (1997) Stathmin: a tubulin-sequestering protein which forms a ternary T2S complex with two tubulin molecules. Biochemistry 36: 10817–10821.
[46]  Bugnard E, Zaal KJ, Ralston E (2005) Reorganization of microtubule nucleation during muscle differentiation. Cell Motil Cytoskeleton 60: 1–13.
[47]  Takada F, Vander Woude DL, Tong HQ, Thompson TG, Watkins SC, et al. (2001) Myozenin: an alpha-actinin- and gamma-filamin-binding protein of skeletal muscle Z lines. Proc Natl Acad Sci U S A 98: 1595–1600.
[48]  Cox D, Brennan M, Moran N (2010) Integrins as therapeutic targets: lessons and opportunities. Nat Rev Drug Discov 9: 804–820.
[49]  Hynes RO (1992) Integrins: versatility, modulation, and signaling in cell adhesion. Cell 69: 11–25.
[50]  Disatnik MH, Rando TA (1999) Integrin-mediated muscle cell spreading. The role of protein kinase c in outside-in and inside-out signaling and evidence of integrin cross-talk. J Biol Chem 274: 32486–32492.
[51]  Kornberg L, Earp HS, Parsons JT, Schaller M, Juliano RL (1992) Cell adhesion or integrin clustering increases phosphorylation of a focal adhesion-associated tyrosine kinase. J Biol Chem 267: 23439–23442.
[52]  Kim CW, Goldberger OA, Gallo RL, Bernfield M (1994) Members of the syndecan family of heparan sulfate proteoglycans are expressed in distinct cell-, tissue-, and development-specific patterns. Molecular Biology of the Cell 5: 797–805.
[53]  Couchman JR (2003) Syndecans: proteoglycan regulators of cell-surface microdomains? Nat Rev Mol Cell Biol 4: 926–937.
[54]  Dovas A, Yoneda A, Couchman JR (2006) PKCbeta-dependent activation of RhoA by syndecan-4 during focal adhesion formation. J Cell Sci 119: 2837–2846.
[55]  Bass MD, Roach KA, Morgan MR, Mostafavi-Pour Z, Schoen T, et al. (2007) Syndecan-4-dependent Rac1 regulation determines directional migration in response to the extracellular matrix. Journal of Cell Biology 177: 527–538.
[56]  Howe AK, Baldor LC, Hogan BP (2005) Spatial regulation of the cAMP-dependent protein kinase during chemotactic cell migration. Proc Natl Acad Sci U S A 102: 14320–14325.
[57]  Feoktistov I, Goldstein AE, Biaggioni I (2000) Cyclic AMP and protein kinase A stimulate Cdc42: role of A(2) adenosine receptors in human mast cells. Mol Pharmacol 58: 903–910.
[58]  Arthur WT, Noren NK, Burridge K (2002) Regulation of Rho family GTPases by cell-cell and cell-matrix adhesion. Biol Res 35: 239–246.
[59]  Oude Weernink PA, Schmidt M, Jakobs KH (2004) Regulation and cellular roles of phosphoinositide 5-kinases. Eur J Pharmacol 500: 87–99.
[60]  Franco SJ, Huttenlocher A (2005) Regulating cell migration: calpains make the cut. J Cell Sci 118: 3829–3838.
[61]  Engleka KA, Gitler AD, Zhang M, Zhou DD, High FA, et al. (2005) Insertion of Cre into the Pax3 locus creates a new allele of Splotch and identifies unexpected Pax3 derivatives. Dev Biol 280: 396–406.
[62]  Mao X, Fujiwara Y, Chapdelaine A, Yang H, Orkin SH (2001) Activation of EGFP expression by Cre-mediated excision in a new ROSA26 reporter mouse strain. Blood 97: 324–326.
[63]  Kioussi C, Gross MK (2008) How to build transcriptional network models of mammalian pattern formation. PLoS One 3: e2179.
[64]  Edgar R, Domrachev M, Lash AE (2002) Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30: 207–210.
[65]  Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, et al. (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13: 2498–2504.
[66]  Sassoon DA, Garner I, Buckingham M (1988) Transcripts of alpha-cardiac and alpha-skeletal actins are early markers for myogenesis in the mouse embryo. Development 104: 155–164.
[67]  Reinhard M, Jarchau T, Walter U (2001) Actin-based motility: stop and go with Ena/VASP proteins. Trends Biochem Sci 26: 243–249.
[68]  Kim E, Waters SH, Hake LE, Hecht NB (1989) Identification and developmental expression of a smooth-muscle gamma-actin in postmeiotic male germ cells of mice. Molecular and Cellular Biology 9: 1875–1881.
[69]  Jin L, Yoshida T, Ho R, Owens GK, Somlyo AV (2009) The actin-associated protein Palladin is required for development of normal contractile properties of smooth muscle cells derived from embryoid bodies. J Biol Chem 284: 2121–2130.
[70]  Dixson JD, Forstner MJ, Garcia DM (2003) The alpha-actinin gene family: a revised classification. J Mol Evol 56: 1–10.
[71]  Miyasaka KY, Kida YS, Sato T, Minami M, Ogura T (2007) Csrp1 regulates dynamic cell movements of the mesendoderm and cardiac mesoderm through interactions with Dishevelled and Diversin. Proc Natl Acad Sci U S A 104: 11274–11279.
[72]  Wang S, Yu WM, Zhang W, McCrae KR, Neel BG, et al. (2009) Noonan syndrome/leukemia-associated gain-of-function mutations in SHP-2 phosphatase (PTPN11) enhance cell migration and angiogenesis. J Biol Chem 284: 913–920.
[73]  Schevzov G, Fath T, Vrhovski B, Vlahovich N, Rajan S, et al. (2008) Divergent regulation of the sarcomere and the cytoskeleton. J Biol Chem 283: 275–283.
[74]  Hubberstey AV, Mottillo EP (2002) Cyclase-associated proteins: CAPacity for linking signal transduction and actin polymerization. FASEB J 16: 487–499.
[75]  Schmetsdorf S, Arnold E, Holzer M, Arendt T, Gartner U (2009) A putative role for cell cycle-related proteins in microtubule-based neuroplasticity. Eur J Neurosci 29: 1096–1107.
[76]  Kamath K, Oroudjev E, Jordan MA (2010) Determination of microtubule dynamic instability in living cells. Methods Cell Biol 97: 1–14.
[77]  Lee C, Scherr HM, Wallingford JB (2007) Shroom family proteins regulate gamma-tubulin distribution and microtubule architecture during epithelial cell shape change. Development 134: 1431–1441.
[78]  Lewis SA, Lee MG, Cowan NJ (1985) Five mouse tubulin isotypes and their regulated expression during development. Journal of Cell Biology 101: 852–861.
[79]  Wang D, Villasante A, Lewis SA, Cowan NJ (1986) The mammalian beta-tubulin repertoire: hematopoietic expression of a novel, heterologous beta-tubulin isotype. Journal of Cell Biology 103: 1903–1910.
[80]  Tachikawa K, Sasaki S, Maeda T, Nakajima K (2008) Identification of molecules preferentially expressed beneath the marginal zone in the developing cerebral cortex. Neurosci Res 60: 135–146.
[81]  Zilberman Y, Ballestrem C, Carramusa L, Mazitschek R, Khochbin S, et al. (2009) Regulation of microtubule dynamics by inhibition of the tubulin deacetylase HDAC6. J Cell Sci 122: 3531–3541.
[82]  Frey N, Richardson JA, Olson EN (2000) Calsarcins, a novel family of sarcomeric calcineurin-binding proteins. Proc Natl Acad Sci U S A 97: 14632–14637.
[83]  Leu SJ, Liu Y, Chen N, Chen CC, Lam SC, et al. (2003) Identification of a novel integrin alpha 6 beta 1 binding site in the angiogenic inducer CCN1 (CYR61). J Biol Chem 278: 33801–33808.
[84]  Jungers KA, Le Goff C, Somerville RP, Apte SS (2005) Adamts9 is widely expressed during mouse embryo development. Gene Expr Patterns 5: 609–617.
[85]  Hu M, Sun XJ, Zhang YL, Kuang Y, Hu CQ, et al. (2010) Histone H3 lysine 36 methyltransferase Hypb/Setd2 is required for embryonic vascular remodeling. Proc Natl Acad Sci U S A 107: 2956–2961.
[86]  Zhang HY, Timpl R, Sasaki T, Chu ML, Ekblom P (1996) Fibulin-1 and fibulin-2 expression during organogenesis in the developing mouse embryo. Dev Dyn 205: 348–364.
[87]  Gersdorff N, Muller M, Schall A, Miosge N (2006) Secreted modular calcium-binding protein-1 localization during mouse embryogenesis. Histochem Cell Biol 126: 705–712.
[88]  Nelson WJ, Lazarides E (1985) Posttranslational control of membrane-skeleton (ankyrin and alpha beta-spectrin) assembly in early myogenesis. Journal of Cell Biology 100: 1726–1735.
[89]  Nagae S, Tanoue T, Takeichi M (2007) Temporal and spatial expression profiles of the Fat3 protein, a giant cadherin molecule, during mouse development. Dev Dyn 236: 534–543.
[90]  Kawai J, Shinagawa A, Shibata K, Yoshino M, Itoh M, et al. (2001) Functional annotation of a full-length mouse cDNA collection. Nature 409: 685–690.
[91]  Sutherland AE, Sanderson RD, Mayes M, Seibert M, Calarco PG, et al. (1991) Expression of syndecan, a putative low affinity fibroblast growth factor receptor, in the early mouse embryo. Development 113: 339–351.
[92]  David G, Bai XM, Van der Schueren B, Marynen P, Cassiman JJ, et al. (1993) Spatial and temporal changes in the expression of fibroglycan (syndecan-2) during mouse embryonic development. Development 119: 841–854.
[93]  Yagami-Hiromasa T, Sato T, Kurisaki T, Kamijo K, Nabeshima Y, et al. (1995) A metalloprotease-disintegrin participating in myoblast fusion. Nature 377: 652–656.
[94]  Abreu JG, Ketpura NI, Reversade B, De Robertis EM (2002) Connective-tissue growth factor (CTGF) modulates cell signalling by BMP and TGF-beta. Nat Cell Biol 4: 599–604.
[95]  Saba JD, Hla T (2004) Point-counterpoint of sphingosine 1-phosphate metabolism. Circ Res 94: 724–734.
[96]  Mandicourt G, Iden S, Ebnet K, Aurrand-Lions M, Imhof BA (2007) JAM-C regulates tight junctions and integrin-mediated cell adhesion and migration. J Biol Chem 282: 1830–1837.
[97]  Holaska JM, Rais-Bahrami S, Wilson KL (2006) Lmo7 is an emerin-binding protein that regulates the transcription of emerin and many other muscle-relevant genes. Hum Mol Genet 15: 3459–3472.
[98]  Ruan K, Bao S, Ouyang G (2009) The multifaceted role of periostin in tumorigenesis. Cell Mol Life Sci 66: 2219–2230.
[99]  Garcia-Espana A, Chung PJ, Sarkar IN, Stiner E, Sun TT, et al. (2008) Appearance of new tetraspanin genes during vertebrate evolution. Genomics 91: 326–334.
[100]  Singh IS, Luo ZJ, Eng A, Erlichman J (1991) Molecular cloning and characterization of the promoter region of the mouse regulatory subunit RII beta of type II cAMP-dependent protein kinase. Biochem Biophys Res Commun 178: 221–226.
[101]  Dong LQ, Zhang RB, Langlais P, He H, Clark M, et al. (1999) Primary structure, tissue distribution, and expression of mouse phosphoinositide-dependent protein kinase-1, a protein kinase that phosphorylates and activates protein kinase Czeta. J Biol Chem 274: 8117–8122.

Full-Text

Contact Us

service@oalib.com

QQ:3279437679

WhatsApp +8615387084133