development · patterns: a test of the differential adhesion hypothesis 37 hanneman, e., trevarrow,...

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Development Volume 103 1988 Editor in Chief Chris Wylie (London) UK Editors Richard Gardner (Oxford) Mike Gaze (Edinburgh) Peter Lawrence (Cambridge) Keith Roberts (Norwich) Hugh Woodland (Warwick) USA Editors Richard Hynes (MIT) Doug Melton (Harvard) Editorial Advisory Board Eileen Adamson (La Jolla, California) Michael Akam (Cambridge) Jonathan Bard (Edinburgh) Michael Bate (Cambridge) Rosa Beddington (Oxford) Ruth Bellairs (London) Mary Bownes (Edinburgh) David Cockcroft (Oxford) Jack Cohen (Birmingham) Alan Colman (Warwick) Alun Davies (London) John Ellis (Warwick) Chris Ford (Sussex) Michael Freeling (Berkeley, California) David Garrod (Southampton) Walter Gehring (Basel) John Gerhart (Berkeley, California) Peter Goodfellow (ICRF London) John Gurdon (Cambridge) John Heath (Oxford) Brigid Hogan (London) Nigel Holder (London) Robert Horvitz (MIT) Herbert Jackie (Tubingen) Rudolph Jaenisch (MIT) William Jeffery (Austin, Texas) Martin Johnson (Cambridge) Elizabeth Jones (Warwick) Klaus Kalthoff (Austin, Texas) Matthew Kaufman (Edinburgh) Michael Keating (London) Judith Kimble (Wisconsin) Klaus Kratochwil (Salzburg) Mary Lyon (Didcot) Gail Martin (UCSF) Rolf Nothiger (Zurich) Bjorn Olsen (Harvard) Scott Poethig (Pennsylvania) Martin Raff (London) Beverley Randle (Bristol) Janet Rossant (Toronto) Joan Ruderman (Duke, N. Carolina) Matthew Scott (Boulder, Colorado) Peter Shelton (Leicester) Richard Skaer (Cambridge) Jonathan Slack (Oxford) Jim Smith (London) Gary Struhl (Columbia Univ., NY) Chris Summerville (Michigan) Masatoshi Takeichi (Kyoto) Peter Thorogood (Southampton) John Tucker (St Andrews) Richard Whittaker (Woods Hole) Jeff Williams (ICRF South Mimms) Published by The Company of Biologists Limited, Cambridge

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Page 1: Development · patterns: a test of the differential adhesion hypothesis 37 Hanneman, E., Trevarrow, B., Metcalfe, W. K., Kimmel, C. B. and Westerfield, M. Segmental pattern of development

DevelopmentVolume 103 1988

Editor in ChiefChris Wylie (London)

UK EditorsRichard Gardner (Oxford)

Mike Gaze (Edinburgh)Peter Lawrence (Cambridge)

Keith Roberts (Norwich)Hugh Woodland (Warwick)

USA EditorsRichard Hynes (MIT)Doug Melton (Harvard)

Editorial Advisory BoardEileen Adamson (La Jolla, California)

Michael Akam (Cambridge)Jonathan Bard (Edinburgh)Michael Bate (Cambridge)Rosa Beddington (Oxford)

Ruth Bellairs (London)Mary Bownes (Edinburgh)David Cockcroft (Oxford)Jack Cohen (Birmingham)

Alan Colman (Warwick)Alun Davies (London)

John Ellis (Warwick)Chris Ford (Sussex)

Michael Freeling (Berkeley, California)David Garrod (Southampton)

Walter Gehring (Basel)John Gerhart (Berkeley, California)

Peter Goodfellow (ICRF London)John Gurdon (Cambridge)

John Heath (Oxford)Brigid Hogan (London)Nigel Holder (London)Robert Horvitz (MIT)

Herbert Jackie (Tubingen)Rudolph Jaenisch (MIT)

William Jeffery (Austin, Texas)Martin Johnson (Cambridge)

Elizabeth Jones (Warwick)Klaus Kalthoff (Austin, Texas)Matthew Kaufman (Edinburgh)Michael Keating (London)Judith Kimble (Wisconsin)Klaus Kratochwil (Salzburg)Mary Lyon (Didcot)Gail Martin (UCSF)Rolf Nothiger (Zurich)Bjorn Olsen (Harvard)Scott Poethig (Pennsylvania)Martin Raff (London)Beverley Randle (Bristol)Janet Rossant (Toronto)Joan Ruderman (Duke, N. Carolina)Matthew Scott (Boulder, Colorado)Peter Shelton (Leicester)Richard Skaer (Cambridge)Jonathan Slack (Oxford)Jim Smith (London)Gary Struhl (Columbia Univ., NY)Chris Summerville (Michigan)Masatoshi Takeichi (Kyoto)Peter Thorogood (Southampton)John Tucker (St Andrews)Richard Whittaker (Woods Hole)Jeff Williams (ICRF South Mimms)

Published by The Company of Biologists Limited, Cambridge

Page 2: Development · patterns: a test of the differential adhesion hypothesis 37 Hanneman, E., Trevarrow, B., Metcalfe, W. K., Kimmel, C. B. and Westerfield, M. Segmental pattern of development

Typeset, Printed and Published byThe Company of Biologists Limited

Department of Zoology, University of Cambridge, Downing Street,Cambridge CB2 3EJ

© The Company of Biologists Limited 1988

Page 3: Development · patterns: a test of the differential adhesion hypothesis 37 Hanneman, E., Trevarrow, B., Metcalfe, W. K., Kimmel, C. B. and Westerfield, M. Segmental pattern of development

Contents

Volume 103 1988

ESSAY IN DEVELOPMENTWilliams, J. G.The role of diffusible molecules in regulating thecellular differentiation of Dictyosteliumdiscoideum

CONTRIBUTED PAPERSWatanabe, K., Aoyama, H., Tamamaki, N.,Sonomura, T., Okada, T. S., Eguchi, G.and Nojyo, Y.An embryonic pineal body as a multipotentsystem in cell differentiation 17

Hayashi, M., Ninomiya, Y., Hayashi, K.,Linsenmayer, T. F., Olsen, B. R.and Trelstad, R. L.Secretion of collagen types I and II by epithelialand endothelial cells in the developing chickcornea demonstrated by in situ hybridization andimmunohistochemistry 27

Thomas, W. A. and Yancey, J.Can retinal mechanisms determine cell-sortingpatterns: a test of the differential adhesionhypothesis 37

Hanneman, E., Trevarrow, B., Metcalfe, W. K.,Kimmel, C. B. and Westerfield, M.Segmental pattern of development of thehindbrain and spinal cord of the zebrafishembryo 49

Krone, P. H. and Heikkila, J. J.Analysis of hsp 30, hsp 70 and ubiquitin geneexpression in Xenopus laevis tadpoles 59

Bagnall, K. M., Higgins, S. J.and Sanders, E. J.The contribution made by a single somite to thevertebral column: experimental evidence insupport of resegmentation using the chick-quailchimaera model 69

Repressa, J. J., Miner, C , Barbosa, E.and Giraldez, F.Bombesin and other growth factors activate cellproliferation in chick embryo otic vesicles inculture 87

Stirling, R. V. and Summerbell, D.Specific guidance of motor axons to duplicatedmuscles in the developing amniote limb 97

Devlin, C. J., Brickell, P. M., Taylor, E. R.,Hornbruch, A., Craig, R. K. and Wolpert, L.In situ hybridization reveals differential spatialdistribution of mRNAs for type I and type IIcollagen in the chick limb bud 111

Bownes, M., Scott, A. and Shin-as, A.Dietary components modulate yolk protein genetranscription in Drosophila melanogaster 119

Howlett, S. K., Barton, S. C , Norris, M. L.and Surani, M. A. H.Nuclear and cytoplasmic localization of newlysynthesized proteins in the early mouse embryo 129

Gaunt, S. J.Mouse homeobox gene transcripts occupydifferent but overlapping domains in embryonicgerm layers and organs: a comparison of Hox-3.1 and Hox-1.5 135

Piovant, M. and Lena, P.Membrane glycoproteins immunologicallyrelated to the human insulin receptor areassociated with presumptive neuronal territoriesand developing neurones in Drosophilamelanogaster 145

Martinez Arias, A., Baker, N. E.and Ingham, P. W.Role of segment polarity genes in the definitionand maintenance of cell states in the Drosophilaembryo 157

Surani, M. A., Barton, S. C , Howlett, S. K.and Norris, M. L.Influence of chromosomal determinants ondevelopment of androgenetic andparthenogenetic cells 171

Chau, M. F. and Ng, S. F.Interspecific micronuclear transplantation inParamecium: nucleogenesis and stomatogenesisin asexual and sexual reproduction 179

Keller, R. and Danilchik, M.Regional expression, pattern and timing ofconvergence and extension during gastrulationof Xenopus laevis 193

Page 4: Development · patterns: a test of the differential adhesion hypothesis 37 Hanneman, E., Trevarrow, B., Metcalfe, W. K., Kimmel, C. B. and Westerfield, M. Segmental pattern of development

Contents

Hardin, J. and Keller, R.The behaviour and function of bottle cellsduring gastrulation of Xenopus laevis 211

ESSAY IN DEVELOPMENTDecker, G. L. and Lennarz, W. J.Skeletogenesis in the sea urchin embryo 231

CONTRIBUTED PAPERSKolberg, K. J. S. and Martin, V. J.Morphological, cytochemical andneuropharmacological evidence for the presenceof catecholamines in hydrozoan planulae 249

Fukuda, Y., Masuda, Y., Kishi, J.-L,Hashimoto, Y., Hayakawa, T., Nogawa, H.and Nakanishi, Y.The role of interstitial collagens in cleftformation of mouse embryonic submandibulargland during initial branching 259

Sharpe, C. R.Developmental expression of a neurofilament-Mand two vimentin-like genes in Xenopus laevis 269

Tang, P., Sharpe, C. R., Mohun, T. J.and Wylie, C. C.Vimentin expression in oocytes, eggs and earlyembryos of Xenopus laevis 279

Baker, N. E.Localization of transcripts from the winglessgene in whole Drosophila embryos 289

Urven, L. E., Erickson, C. A., Abbott, U. K.and McCarrey, J. R.Analysis of germ line development in the chickembryo using an anti-mouse EC cell antibody 299

Wray, G. A. and McClay, D. R.The origin of spicule-forming cells in a'primitive' sea urchin (Eucidaris tribuloides)which appears to lack primary mesenchyme cells 305

Hardin, J.The role of secondary mesenchyme cells duringsea urchin gastrulation studied by laserablation 317

Duband, J.-L., Volberg, T., Sabanay, I.,Thiery, J. P. and Geiger, B.Spatial and temporal distribution of theadherens-junction-associated adhesion moleculeA-CAM during avian embryogenesis 325

Tsuchimori, N., Miyashiro, S., Shibai, H.and Ikegami, S.Adenosine induces dormancy in starfishblastulae 345

Pickering, S. J., Maro, B., Johnson, M. H.and Skepper, J. N.The influence of cell contact on the division ofmouse 8-cell blastomeres 353

Wilson, S., Jesani, M. and Holder, N.Reformation of specific neuromuscularconnections during axolotl limb regeneration:evidence that the first contacts are correct 365

Tam, P. P. L.The allocation of cells in the presomiticmesodenn during somite segmentation in themouse embryo 379

Simpson, P., El Messal, M., Moscoso delPrado, J. and Ripoll, P.Stripes of positional homologies across the wingblade of Drosophila melanogaster 391

Stuart, G. W., McMurray, J. V.and Westerfield, M.Replication, integration and stable germ-linetransmission of foreign sequences injected intoearly zebrafish embryos 403

ESSAY IN DEVELOPMENTKeynes, R. J. and Stern, C. D.Mechanisms of vertebrate segmentation 413

CONTRIBUTED PAPERSJaffredo, T., Horwitz, A. F., Buck, C. A.,Rong, P. M. and Dieterlen-Lievre, F.Myoblast migration specifically inhibited in thechick embryo by grafted CSAT hybridoma cellssecreting an anti-integrin antibody 431

Roberts, A., Dale, N., Ottersen, O. P.and Stonn-Mathisen, J.Development and characterization ofcommissural interneurones in the spinal cord ofXenopus laevis embryos revealed by antibodiesto glycine 447

Kay, B. K., Schwartz, L. M., Rutishauser, U.,Qiu, T. H. and Peng, H. B.Patterns of N-CAM expression duringmyogenesis in Xenopus laevis 463

Thaller, C. and Eichele, G.Characterization of retinoid metabolism in thedeveloping chick limb bud 473

Link, C. D., Ehrenfels, C. W. and Wood, W. B.Mutant expression of male copulatory bursasurface markers in Caenorhabditis elegans 485

Page 5: Development · patterns: a test of the differential adhesion hypothesis 37 Hanneman, E., Trevarrow, B., Metcalfe, W. K., Kimmel, C. B. and Westerfield, M. Segmental pattern of development

Contents

Stylianopoulou, F., Efstratiadis, A., Herbert, J.and Pintar, J.Pattern of the insulin-like growth factor II geneexpression during rat embryogenesis 497

Ressom, R. E. and Dixon, K. E.Relocation and reorganization of germ plasm inXenopus embryos after fertilization 507

Early, A. E. and Williams, J. G.A Dictyostelium prespore-specific gene istranscriptionally repressed by DIF in vitro 519

Fleig, R. and Sander, K.Honeybee morphogenesis: embryonic cellmovements that shape the larval body 525

Ken-, J. B. and Knell, C. M.The fate of fetal Leydig cells during thedevelopment of the fetal and postnatal rat testis 535

Rohrer, H., Hofer, M., Hellweg, R.,Korsching, S., Stehle, A. D., Saadat, S.and Thoenen, H.Antibodies against mouse nerve growth factorinterfere in vivo with the development of aviansensory and sympathetic neurones 545

Hutchison, C. J., Cox, R. and Ford, C. C.The control of DNA replication in a cell-freeextract that recapitulates a basic cell cycle invitro 553

Fekete, D. M. and Brockes, J. P.Evidence that the nerve controls molecularidentity of progenitor cells for limb regeneration 567

Picard, A., Labbe, J.-C. and Dor6e, M.Normal embryogenesis occurs in starfish eggsinduced to mature by microinjection ofcytoplasm containing maturation-promotingfactor (MPF) 575

Slack, J. M. W., Isaacs, H. V.and Darlington, B. G.Inductive effects of fibroblast growth factor andlithium ion on Xenopus blastula ectoderm 581

Smith, J. C , Yaqoob, M. and Symes, K.Purification, partial characterization andbiological effects of the XTC mesoderm-inducing factor 591

Falzon, M. and Chung, S. Y.The expression of rat homeobox-containinggenes is developmentally regulated and tissuespecific

Wang, M., van Driel, R. and Schaap, P.Cyclic AMP-phosphodiesterase inducesdedifferentiation of prespore cells inDictyostelium discoideum slugs: evidence thatcyclic AMP is the morphogenetic signal forprespore differentiation

BOOKS IN DEVELOPMENT

611

619

Hay, B., Ackerman, L., Barbel, S., Jan, L. Y.and Jan, Y. N.Identification of a component of DrosophUapolar granules 625

Carrino, D. A., Oron, U., Pechak, D. G.and Caplan, A. I.Reinitiation of chondroitin sulphateproteoglycan synthesis in regenerating skeletalmuscle 641

Schiavone, F. M.Microamputation of somatic embryos of thedomestic carrot reveals apical control of axiselongation and root regeneration 657

Racusen, R. H. and Schiavone, F. M.Detection of spatially- and stage-specificproteins in extracts from single embryos of thedomesticated carrot 665

Kellogg, D. R., Mitchison, T. J.and Alberts, B. M.Behaviour of microtubules and actin filaments inliving DrosophUa embryos 675

Martins-Green, M.Origin of the dorsal surface of the neural tubeby progressive delamination of epidermalectoderm and neuroepithelium: implications forneurulation and neural tube defects 687

Toussaint, N. and French, V.The formation of pattern on the wing of themoth, Ephestia kuhniella 707

601

Stevens, M. E., Maidens, P. M.,Robinson, E. S., Vandeberg, J. L.,Pedersen, R. A. and Monk, M.DNA methylation in the developing marsupialembryo 719

Hayashi, K., Yasugi, S. and Mizuno, T.Pepsinogen gene transcription induced inheterologous epithelial-mesenchymalrecombinations of chicken endoderms andglandular stomach mesenchyme 725

Page 6: Development · patterns: a test of the differential adhesion hypothesis 37 Hanneman, E., Trevarrow, B., Metcalfe, W. K., Kimmel, C. B. and Westerfield, M. Segmental pattern of development

Contents

Dura, J.-M. and Ingham, P.Tissue- and stage-specific control of homeoticand segmentation gene expression in Drosophilaembryos by the polyhomeotic gene 733

Epperlein, H. H., Halfter, W. and Tucker, R. P.The distribution of fibronectin and tenascinalong the migratory pathways of the neural crestin the trunk of amphibian embryos 743

Ripoll, P., El Messel, M., Laran, E.and Simpson, P.A gradient of affinities for sensory bristlesacross the wing blade of Drosophila melanogaster 757

Guthrie, S., Turin, L. and Warner, A.Patterns of junctional communication duringdevelopment of the early amphibian embryo

Schmidt, G. H., Winton, D. J.and Ponder, B. A. J.Development of the pattern of cell renewal inthe crypt-villus unit of chimaeric mouse smallintestine

Plickert, G. and Kroiher, M.Proliferation kinetics and cell lineages can bestudied in whole mounts and macerates bymeans of BrdU/anti-BrdU technique

Plickert, G., Kroiher, M. and Munck, A.Cell proliferation and early differentiationduring embryonic development andmetamorphosis of Hydractinia echinata

Index of Authors and Titles

785

791

769 Subject Index

795

805

809

Page 7: Development · patterns: a test of the differential adhesion hypothesis 37 Hanneman, E., Trevarrow, B., Metcalfe, W. K., Kimmel, C. B. and Westerfield, M. Segmental pattern of development

Information about the journalDEVELOPMENT (ISSN 0950-1991) is a continuation of Journal of Embryology and Experimental Morphology (ISSN 0022-0752).

The aim of DEVELOPMENT is to act as a forum for allresearch that offers a genuine insight into mechanisms ofdevelopment. Manuscripts will be considered primarilywith respect to this aim.

Studies on both plant and animal development arewelcome and can be focused upon any aspect of thedevelopmental process, at all levels of biological organ-ization from the molecular and cellular to the tissuelevels.

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Subscription ratesDEVELOPMENT in 1988 will have 12 normal issues and2 casebound supplements. The 12 normal issues will bein the form of 3 volumes (102, 103, 104) each of 4 parts.In 1988 the Supplements will be Craniofacial Develop-ment, edited by Peter Thorogood & Cheryll Tickle, andMechanisms of Segmentation edited by Vernon French,Phil Ingham and Jonathan Cooke. The prices for 1988are £280.00 (UK) US$620.00 (USA and Canada)£355.00 (Japan) £325.00 (Rest of World). There arereduced subscriptions for members of the BSCB, BSDBand SEB (£40, $85) and for individual use only (£55,$90). These prices include postage and packing. Ordersfor 1988, which can be in £ Sterling/Dollars or Access-/Visa credit cards, should be sent to The BiochemicalSociety Book Depot, PO Box 32, Commerce Way,Colchester, CO2 8HP, UK or to your normal agent orbookseller. Orders must be accompanied by payment.Copies of the journal for subscribers in the USA andCanada are sent by air to New Jersey for delivery withthe minimum delay (second class postage paid atRahway, NJ and at additional mailing offices).

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Page 8: Development · patterns: a test of the differential adhesion hypothesis 37 Hanneman, E., Trevarrow, B., Metcalfe, W. K., Kimmel, C. B. and Westerfield, M. Segmental pattern of development

Information for contributors

1 Manuscripts can be sent to any editor or toThe Editorial Office, DEVELOPMENT, Dept ofZoology, Downing St, Cambridge CB2 3EJ, UK.USA papers should be sent direct to one of the USAeditors: Dr D. Melton, Department of Biochemistryand Molecular Biology, Harvard University, 7Divinity Avenue, Cambridge, MA 02138, USA orDr R. O. Hynes, Center for Cancer Research,Department of Biology, Massachusetts Institute ofTechnology, Cambridge, MA 02139, USA.

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of the Drosophila abdomen: the epidermis, oeno-cytes and ventral muscles. /. Embryol. exp. Morph.72, 197-208.

ROSSANT, J. (1977). Cell commitment in early rodentdevelopment. In Development in Mammals, vol. 2(ed. M. H. Johnson), pp. 119-150. Amsterdam:North Holland.

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Page 9: Development · patterns: a test of the differential adhesion hypothesis 37 Hanneman, E., Trevarrow, B., Metcalfe, W. K., Kimmel, C. B. and Westerfield, M. Segmental pattern of development

ContentsVolume 103 (4) 1988

BOOKS IN DEVELOPMENT 619

Hay, B., Ackerman, L, Barbel, S., Jan, L. Y.and Jan, Y. N.Identification of a component of Drosophilapolar granules 625

Carrino, D. A., Oron, U., Pechak, D. G.and Caplan, A. I.Reinitiation of chondroitin sulphate proteoglycansynthesis in regenerating skeletal muscle 641

Schiavone, F. M.Microamputation of somatic embryos of thedomestic carrot reveals apical control of axiselongation and root regeneration 657

Racusen, R. H. and Schiavone, F. M.Detection of spatially- and stage-specificproteins in extracts from single embryos of thedomesticated carrot 665

Kellogg, D. R., Mitchison, T. J.and Alberts, B. M.Behaviour of microtubules and actin filaments inliving Drosophila embryos 675

Martins-Green, M.Origin of the dorsal surface of the neural tubeby progressive delamination of epidermalectoderm and neuroepithelium: implications forneurulation and neural tube defects 687

Toussaint, N. and French, V.The formation of pattern on the wing of themoth, Ephestia kuhniella 707

Stevens, M. E., Maidens, P. M.,Robinson, E. S., Vandeberg, J. L.,Pedersen, R. A. and Monk, M.DNA methylation in the developing marsupialembryo 719

Hayashi, K., Yasugi, S. and Mizuno, T.Pepsinogen gene transcription induced inheterologous epithelial-mesenchymalrecombinations of chicken endoderms andglandular stomach mesenchyme 725

Dura, J.-M. and Ingham, P.Tissue- and stage-specific control of homeoticand segmentation gene expression inDrosophila embryos by the polyhomeotic gene 733

Epperlein, H. H., Halfter, W.and Tucker, R. P.The distribution of fibronectin and tenascinalong the migratory pathways of the neuralcrest in the trunk of amphibian embryos 743

Ripoll. P., El Messel, M., Laran, E.and Simpson, P.A gradient of affinities for sensory bristlesacross the wing blade of Drosophilamelanogaster 757

Guthrie, S., Turin, L. and Warner, A.Patterns of junctional communication duringdevelopment of the early amphibian embryo 769

Schmidt, G. H., Winton, D. J.and Ponder, B. A. J.Development of the pattern of cell renewal inthe crypt—villus unit of chimaeric mouse smallintestine 785

Plickert, G. and Kroiher. M.Proliferation kinetics and cell lineages can bestudied in whole mounts and macerates bymeans of BrdU anti-BrdU technique 791

Plickert, G., Kroiher, M. and Munck, A.Cell proliferation and early differentiation duringembryonic development and metamorphosis ofHydractinia echinata ' 795

Index of Authors and Titles 805

Subject Index 809

The Company of Biologists LimitedDepartment of Zoology, University of Cambridge, Downing Street. Cambridge CB2 3EJISSN: 0950-1991(c) The Company of Biologists Limited 1988