Identification of an Invariant Response: Stable Contact with Schwann Cells Induces Veil Extension in Sensory Growth Cones

Growth cones sense cues by filopodial contact, but how their motility is altered by contact remains unclear. Although contact could alter motile dynamics in complex ways, our analysis shows that stable contact with Schwann cells induces motility changes that are remarkably discrete and invariant. Filopodial contact invariably induces local veil extension. Even when contacts are brief, veils always extend before the filopodia retract. Contact at filopodial tips suffices for induction. Moreover, veils extend significantly sooner than on filopodia contacting laminin, which often detach without extending veils. The overall behavioral responses of the growth cone, such as increased area and turning, result from integrating multiple discrete responses. Cycles of veil induction enlarge the growth cone and often lead it onto the cell. Invariant veil induction is abolished by blocking N-cadherin signaling. We propose an axonal guidance model in which different guidance cues act by inducing different but discrete and invariant responses.

[1]  Karthryn W. Tonsey,et al.  Cells and cell‐interactions that guide motor axons in the developing chick embryo , 1991 .

[2]  M. Schachner,et al.  Studies of adhesion molecules mediating interactions between cells of peripheral nervous system indicate a major role for L1 in mediating sensory neuron growth on Schwann cells in culture , 1988, The Journal of cell biology.

[3]  C. Shatz,et al.  Developmental mechanisms that generate precise patterns of neuronal connectivity , 1993, Cell.

[4]  P. Forscher Calcium and polyphosphoinositide control of cytoskeletal dynamics , 1989, Trends in Neurosciences.

[5]  M. Takeichi,et al.  Expression of N-cadherin adhesion molecules associated with early morphogenetic events in chick development , 1986, Nature.

[6]  Mu-ming Poo,et al.  cAMP-induced switching in turning direction of nerve growth cones , 1997, Nature.

[7]  Mu-ming Poo,et al.  cAMP-Dependent Growth Cone Guidance by Netrin-1 , 1997, Neuron.

[8]  R. W. Gundersen,et al.  Response of sensory neurites and growth cones to patterned substrata of laminin and fibronectin in vitro. , 1987, Developmental biology.

[9]  S. B. Kater,et al.  Interactive effects of serotonin and acetylcholine on neurite elongation , 1988, Neuron.

[10]  Daniel J. Goldberg,et al.  Looking into growth cones , 1989, Trends in Neurosciences.

[11]  A. Gilman,et al.  G proteins: transducers of receptor-generated signals. , 1987, Annual review of biochemistry.

[12]  Kathryn W. Tosney Cells and cell-interactions that guide motor axons in the developing chick embryo. , 1991, BioEssays : news and reviews in molecular, cellular and developmental biology.

[13]  D. Goldberg,et al.  Stages in axon formation: observations of growth of Aplysia axons in culture using video-enhanced contrast-differential interference contrast microscopy , 1986, The Journal of cell biology.

[14]  W. Thompson,et al.  Nerve sprouting in muscle is induced and guided by processes extended by schwann cells , 1995, Neuron.

[15]  Jinhong Fan,et al.  Localized collapsing cues can steer growth cones without inducing their full collapse , 1995, Neuron.

[16]  Z. Werb,et al.  Reorganization of polymerized actin: a possible trigger for induction of procollagenase in fibroblasts cultured in and on collagen gels , 1986, The Journal of cell biology.

[17]  Kathryn W. Tosney,et al.  Contact-mediated mechanisms of motor axon segmentation , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[18]  T. Gómez,et al.  Filopodia initiate choices made by sensory neuron growth cones at laminin/fibronectin borders in vitro , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  P Z Myers,et al.  Growth cone dynamics during the migration of an identified commissural growth cone , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  D. Bentley,et al.  Disoriented pathfinding by pioneer neurone growth cones deprived of filopodia by cytochalasin treatment , 1986, Nature.

[21]  S. Skaper,et al.  Selective survival of neurons from chick embryo sensory ganglionic dissociates utilizing serum-free supplemented medium. , 1980, Experimental cell research.

[22]  M. Steketee,et al.  Contact with Isolated Sclerotome Cells Steers Sensory Growth Cones by Altering Distinct Elements of Extension , 1999, The Journal of Neuroscience.

[23]  W. Thompson,et al.  Schwann cell processes guide regeneration of peripheral axons , 1995, Neuron.

[24]  M. Hollyday,et al.  The location and distribution of neural crest-derived Schwann cells in developing peripheral nerves in the chick forelimb. , 1992, Developmental biology.

[25]  L. Greene,et al.  Growth cone configuration and advance: a time-lapse study using video- enhanced differential interference contrast microscopy , 1988, Journal of Neuroscience.

[26]  D. Bentley,et al.  Pioneer growth cone steering decisions mediated by single filopodial contacts in situ , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  E. Neer,et al.  G0 is a major growth cone protein subject to regulation by GAP-43 , 1990, Nature.

[28]  A. Lander,et al.  Relationship between neuronal migration and cell-substratum adhesion: laminin and merosin promote olfactory neuronal migration but are anti- adhesive , 1991, The Journal of cell biology.

[29]  M. Lohse,et al.  Neural cell adhesion molecules influence second messenger systems , 1989, Neuron.

[30]  E. Frank,et al.  P0 is an early marker of the schwann cell lineage in chickens , 1991, Neuron.

[31]  R. Keynes,et al.  Segmentation in the vertebrate nervous system , 1984, Nature.

[32]  J. Bixby,et al.  Identification of the major proteins that promote neuronal process outgrowth on Schwann cells in vitro , 1988, The Journal of cell biology.

[33]  Viktor Hamburger,et al.  A series of normal stages in the development of the chick embryo , 1992, Journal of morphology.

[34]  James Q. Zheng,et al.  cAMP-Mediated Regulation of Neurotrophin-Induced Collapse of Nerve Growth Cones , 1998, The Journal of Neuroscience.

[35]  L. Marsh,et al.  Growth of neurites without filopodial or lamellipodial activity in the presence of cytochalasin B , 1984, The Journal of cell biology.

[36]  L Erskine,et al.  Integrated interactions between chondroitin sulphate proteoglycans and weak dc electric fields regulate nerve growth cone guidance in vitro. , 1997, Journal of cell science.

[37]  David W. Sretavan,et al.  Time-lapse video analysis of retinal ganglion cell axon pathfinding at the mammalian optic chiasm: Growth cone guidance using intrinsic chiasm cues , 1993, Neuron.

[38]  D. Jackson Structure–function relationships in eukaryotic nuclei , 1991, BioEssays : news and reviews in molecular, cellular and developmental biology.

[39]  M. Takeichi,et al.  Nerve growth cone migration onto Schwann cells involves the calcium-dependent adhesion molecule, N-cadherin. , 1990, Developmental biology.

[40]  D. Bentley,et al.  Pioneer growth cone morphologies reveal proximal increases in substrate affinity within leg segments of grasshopper embryos , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[41]  M. Fishman,et al.  The neuronal growth cone as a specialized transduction system , 1991, BioEssays : news and reviews in molecular, cellular and developmental biology.

[42]  S. M. Burden-Gulley,et al.  Growth cones are actively influenced by substrate-bound adhesion molecules , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[43]  D. Burmeister,et al.  Micropruning: the mechanism of turning of Aplysia growth cones at substrate borders in vitro , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.