Micro-scale chromophore-assisted laser inactivation of nerve growth cone proteins

Microscopy Research and Technique

Volumn 48, Issue 2, 2000, Pages 97-106

  Buchstaller, Andrea ^a   Jay, Daniel G ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

CALI; Filopodia; Growth cone motility; Lamellipodia; Loss of function

Indexed keywords

CELL MEMBRANES; CELL SIGNALING; CHROMOPHORES; MOLECULES;

CALI; CELL SURFACE RECEPTORS; DIRECTED GROWTH; FILOPODIUM; GROWTH CONE MOTILITY; GROWTH CONES; LAMELLIPODIA; LOSS OF FUNCTION; NERVE-GROWTH CONE; RECEPTOR SIGNALING;

PROTEINS;

NERVE PROTEIN;

ARTICLE; CELL MOTILITY; CHROMATOPHORE; CYTOSKELETON; GENE FUNCTION; GENE INACTIVATION; GENE LOCATION; GENE LOSS; LASER; NERVE FIBER GROWTH; PRIORITY JOURNAL;

EID: 0034650664     PISSN: 1059910X     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-0029(20000115)48:2<97::AID-JEMT5>3.0.CO;2-G     Document Type: Article

References (108)

1. Aigner L, Caroni P. 1993. Depletion of 43-kD growth-associated protein in primary sensory neurons leads to diminished formation and spreading of growth cones. J Cell Biol 123:417-429.
2. Aigner L, Caroni P. 1995. Absence of persistent spreading, branching, adhesion in GAP-43-depleted growth cones. J Cell Biol 128:647-660.
3. Aigner L, Arber S, Kapfhammer JP, Laux T, Schneider C, Botteri F, Brenner HR, Caroni P. 1995. Overexpression of the neural growth-associated protein GAP-43 induces nerve sprouting in the adult nervous system of transgenic mice. Cell 83:269-278.
4. Algrain M, Turunen O, Vaheri A, Louvard D, Arpin M. 1993. Ezrin contains cytoskeleton and membrane binding domains accounting for its proposed role as a membrane-cytoskeletal linker. J Cell Biol 120:129-139.
5. Atashi JR, Klinz SG, Ingraham CA, Matten WT, Schachner M, Maness PF. 1992. Neural cell adhesion molecules modulate tyrosine phosphorylation of tubulin in nerve growth cone membranes. Neuron 8:831-842.
6. Beermann AE, Jay DG. 1994. Chromophore-assisted laser inactivation of cellular proteins. Methods Cell Biol 44:715-732.
7. Bixby JL, Bookman RJ. 1996. Intracellular mechanisms of axon growth induction by CAMs and integrins: some unresolved issues. Perspect Dev Neurobiol 4:147-156.
8. Bray D. 1989. Growth cone formation and navigation: axonal growth. Curr Opin Cell Biol 1:87-90.
9. Bridgman PC, Dailey ME. 1989. The organization of myosin and actin in rapid frozen nerve growth cones. J Cell Biol 108:95-109.
10. Brittis PA, Lemmon V, Rutishauser U, Silver J. 1995. Unique changes of ganglion cell growth cone behavior following cell adhesion molecule perturbations: a time-lapse study of the living retina. Mol Cell Neurosci 6:433-449.
11. Brugge JS, Cotton PC, Queral AE, Barrett JN, Nonner D, Keane RW. 1985. Neurones express high levels of a structurally modified, activated form of pp60c-src. Nature 316:554-557.
12. Burden-Gulley SM, Pendergast M, Lemmon V. 1997. The role of cell adhesion molecule L1 in axonal extension, growth cone motility, signal transduction. Cell Tissue Res 290:415-422.
13. Burridge K, Fath K. 1989. Focal contacts: transmembrane links between the extracellular matrix and the cytoskeleton. Bioessays 10:104-108.
14. Castelo L, Jay DG. 1999. Radixin is involved in lamellipodial stability during nerve growth cone motility. Mol Biol Cell 10:1511-1520.
15. Chang HY, Takei K, Sydor AM, Born T, Rusnak F, Jay DG. 1995. Asymmetric retraction of growth cone filopodia following focal inactivation of calcineurin. Nature 376:686-690.
16. Cleveland DW, Hwo SY, Kirschner MW. 1977. Physical and chemical properties of purified tau factor and the role of tau in microtubule assembly. J Mol Biol 116:227-247.
17. Cohen NR, Taylor JS, Scott LB, Guillery RW, Soriano P, Furley AJ. 1998. Errors in corticospinal axon guidance in mice lacking the neural cell adhesion molecule L1. Curr Biol 8:26-33.
18. Cotton PC, Brugge JS. 1983. Neural tissues express high levels of the cellular src gene product pp60c-src. Mol Cell Biol 3:1157-1162.
19. Cremer H, Lange R, Christoph A, Plomann M, Vopper G, Roes J, Brown R, Baldwin S, Kraemer P, Scheff S, et al. 1994. Inactivation of the N-CAM gene in mice results in size reduction of the olfactory bulb and deficits in spatial learning. Nature 367:455-459.
20. Dahme M, Bartsch U, Martini R, Anliker B, Schachner M, Mantei N. 1997. Disruption of the mouse L1 gene leads to malformations of the nervous system. Nat Genet 17:346-349.
21. Davis JQ, Bennett V. 1994. Ankyrin binding activity shared by the neurofascin/L1 /NrCAM family of nervous system cell adhesion molecules. J Biol Chem 69:27163-27166.
22. Diamond P, Mallavarapu A, Schnipper J, Booth J, Park L, O'Connor TP, Jay DG. 1993. Fasciclin I and II have distinct roles in the development of grasshopper pioneer neurons. Neuron 11:409-421.
23. Doherty P, Walsh FS. 1994. Signal transduction events underlying neurite outgrowth stimulated by cell adhesion molecules. Curr Opin Neurobiol 4:49-55.
24. Doherty P, Walsh FS. 1996. CAM-FGF receptor interactions: a model for axonal growth. Mol Cell Neurosci 8:99-111.
25. Doherty P, Fruns M, Seaton P, Dickson G, Barton CH, Sears TA, Walsh FS. 1990. A threshold effect of the major isoforms of NCAM on neurite outgrowth. Nature 343:464-466.
26. Edelmann W, Zervas M, Costello P, Roback L, Fisher I, Hammarback JA, Cowan N, Davies P, Wainer B, Kucherlapati R. 1996. Neuronal abnormalities in microtubule-associated protein 1B mutant mice. Proc Natl Acad Sci U S A 93:1270-1275.
27. Evans LL, Hammer J, Bridgman PC. 1997. Subcellular localization of myosin V in nerve growth cones and outgrowth from dilute-lethal neurons. J Cell Sci 110:439-449.
28. Feil R, Brocard J, Mascrez B, LeMeur M, Metzger D, Chambon P. 1996. Ligand-activated site-specific recombination in mice. Proc Natl Acad Sci U S A 93:10887-10890.
29. Forscher P, Smith SJ. 1988. Actions of cytochalasins on the organization of actin filaments and microtubules in a neuronal growth cone. J Cell Biol 107:1505-1516.
30. Goldberg DJ, Burmeister DW. 1986. Stages in axon formation: observations of growth of Aplysia axons in culture using video-enhanced contrast-differential interference contrast microscopy. J Cell Biol 103:1921-1931.
31. Goldberg DJ, Wu DY. 1996. Tyrosine phosphorylation and protrusive structures of the growth cone. Perspect Dev Neurobiol 4:183-192.
32. Grant SG, Karl KA, Kiebler MA, Kandel ER. 1995. Focal adhesion kinase in the brain: novel subcellular localization and specific regulation by Fyn tyrosine kinase in mutant mice. Genes Dev 9:1909-1921.
33. Harada A, Oguchi K, Okabe S, Kuno J, Terada S, Ohshima T, Sato-Yoshitake R, Takei Y, Noda T, Hirokawa N. 1994. Altered microtubule organization in small-calibre axons of mice lacking tau protein. Nature 369:488-491.
34. Henkemeyer M, Orioli D, Henderson JT, Saxton TM, Roder J, Pawson T, Klein R. 1996. Nuk controls pathfinding of commissural axons in the mammalian central nervous system. Cell 86:35-46.
35. Hoffman KB. 1998. The relationship between adhesion molecules and neuronal plasticity. Cell Mol Neurobiol 18:461-475.
36. c-src but not p59 is a negative regulator of neurite outgrowth in chick sensory neurons. J Neurosci (in press).
37. Holtmaat AJ, Oestreicher AB, Gispen WH, Verhaagen J. 1998. Manipulation of gene expression in the mammalian nervous system: application in the study of neurite outgrowth and neuroregeneration-related proteins. Brain Res Brain Res Rev 26:43-71.
38. Honig MG, Rutishauser US. 1996. Changes in the segmental pattern of sensory neuron projections in the chick hindlimb under conditions of altered cell adhesion molecule function. Dev Biol 175:325-337.
39. Honig MG, Petersen GG, Rutishauser US, Camilli SJ. 1998a. In vitro studies of growth cone behavior support a role for fasciculation mediated by cell adhesion molecules in sensory axon guidance during development. Dev Biol 204:317-326.
40. Honig MG, Frase PA, Camilli SJ. 1998b. The spatial relationships among cutaneous, muscle sensory and motoneuron axons during development of the chick hindlimb. Development 125:995-1004.
41. Ignelzi MA Jr, Miller DR, Soriano P, Maness PF. 1994. Impaired neurite outgrowth of src-minus cerebellar neurons on the cell adhesion molecule L1. Neuron 12:873-84.
42. Jay DG. 1988. Selective destruction of protein function by chromophore-assisted laser inactivation. Proc Natl Acad Sci USA 85:5454-5458.
43. Jay DG. 1996. Molecular mechanisms of directed growth cone motility. Perspect Dev Neurobiol 4:137-145.
44. Jay DG. 1999. Chromophore-assisted laser inactivation (CALI) to elucidate cellular mechanisms of cancer. Biochem Biophys Acta 1424:1139-1148.
45. Jay DG, Keshishian H. 1990. Laser inactivation of fasciclin I disrupts axon adhesion of grasshopper pioneer neurons. Nature 348:548-550.
46. Kamiguchi H, Hlavin ML, Lemmon V. 1998. Role of L1 in neural development: what the knockouts tell us. Mol Cell Neurosci 12: 48-55.
47. Kater SB, Rehder V. 1995. The sensory-motor role of growth cone filopodia. Curr Opin Neurobiol 5:68-74.
48. Kramer I, Hall H, Bleistein U, Schachner M. 1997. Developmentally regulated masking of an intracellular epitope of the 180 kDa isoform of the neural cell adhesion molecule NCAM. J Neurosci Res 49:161-175
49. Kruger K, Tam AS, Lu C, Sretavan DW. 1998. Retinal ganglion cell axon progression from the optic chiasm to initiate optic tract development requires cell autonomous function of GAP-43. J Neurosci 18:5692-5705.
50. Kuhn TB, Brown MD, Bamburg JR. 1998. Rac1-dependent actin filament organization in growth cones is necessary for beta1-integrin-mediated advance but not for growth on poly-D-lysine. J Neurobiol 37:524-540.
51. Kuhn TB, Brown MD, Wilcox CL, Raper JA, Bamburg JR. 1999. Myelin and collapsin-1 induce motor neuron growth cone collapse through different pathways: inhibition of collapse by opposing mutants of rac1. J Neurosci 19:1965-1975.
52. Lagenaur C, Lemmon V. 1987. An L1-like molecule, the 8D9 antigen, is a potent substrate for neurite extension. Proc Natl Acad Sci U S A 84:7753-7757.
53. Lamb RF, Ozanne BW, Roy C, McGarry L, Stipp C, Mangeat P, Jay DG. 1997. Essential functions of ezrin in maintenance of cell shape and lamellipodial extension in normal and transformed fibroblasts. Curr Biol 7:682-688.
54. Landmesser L, Dahm L, Schultz K, Rutishauser U. 1988. Distinct roles for adhesion molecules during innervation of embryonic chick muscle. Dev Biol 130:645-670.
55. Lemmon V, Farr KL, Lagenaur C. 1989. L1-mediated axon outgrowth occurs via homophilic binding mechanism. Neuron 6;1597-1603.
56. Letourneau PC. 1996. The cytoskeleton in nerve growth cone motility and axonal pathfinding. Perspect Dev Neurobiol 4:111-123.
57. Letourneau PC, Shattuck TA. 1989. Distribution and possible interactions of actin-associated proteins and cell adhesion molecules of nerve growth cones. Development 105:505-519.
58. Letourneau PC, Snow DM, Gomez TM. 1994. Regulation of growth cone motility by substratum bound molecules and cytoplasmic [Ca2+]. Prog Brain Res 103:85-98.
59. Liao JC, Roider J, Jay DG. 1994. Chromophore-assisted laser inactivation of proteins is mediated by the photogeneration of free radicals. Proc Natl Acad Sci USA 91:2659-2663.
60. Liao JC, Berg LJ, Jay DG. 1995. Chromophore-assisted laser inactivation of subunits of the T-cell receptor in living cells is spatially restricted. Photochem Photobiol 62:923-929.
61. Lin CH, Forscher P. 1993. Cytoskeletal remodeling during growth cone-target interactions. J Cell Biol 121:1369-1383.
62. Lin CH, Espreafico EM, Mooseker MS, Forscher P. 1996. Myosin drives retrograde F-actin flow in neuronal growth cones. Neuron 16:769-782.
63. Linden KG, Liao JC, Jay DG. 1992. Spatial specificity of chromophore assisted laser inactivation of protein function. Biophys J 61:956-962.
64. Lipsich LA, Lewis AJ, Brugge JS. 1983. Isolation of monoclonal antibodies that recognize the transforming proteins of avian sarcoma viruses. J Virol 48:352-360.
65. Liu CA, Lee G, Jay DG. 1999. Tau is required for neurite outgrowth and growth cone motility of chick sensory neurons. Cell Motil Cytoskeleton (in press).
66. Luo L, Liao YJ, Jan LY, Jan YN. 1994. Distinct morphogenetic functions of similar small GTPases: Drosophila Drac1 is involved in axonal outgrowth and myoblast fusion. Genes Dev 8:1787-802.
67. Mack TGA, Koester, M, Pollerberg GE. 1999. The microtubule-associated protein MAP1B is involved in local stabilization of turning growth cones. Mol Cell Neurosci (in press).
68. Matten WT, Aubry M, West J, Maness PF. 1990. Tubulin is phosphorylated at tyrosine by pp60c-src in nerve growth cone membranes. J Cell Biol 111:1959-1970.
69. McFarlane S, Cornel E, Amaya E, Holt CE. 1996. Inhibition of FGF receptor activity in retinal ganglion cell axons causes errors in target recognition. Neuron 17:245-254.
70. Mitchison T, Kirschner M. 1988. Cytoskeletal dynamics and nerve growth. Neuron 1:761-772.
71. Mochly-Rosen, D, L.M. Kauvar. 1998. Modulating protein kinase C signal transduction. Adv Pharmacol 44:91-145.
72. Moos M, Tacke R, Scherer H, Teplow D, Fruh K, Schachner M. 1988. Neural adhesion molecule L1 as a member of the immunoglobulin superfamily with binding domains similar to fibronectin. Nature 334:701-703.
73. Mueller BK. 1999. Growth cone guidance: first steps towards a deeper understanding. Annu Rev Neurosci 22:351-388.
74. Muller BK, Bonhoeffer F. 1995. Molecular inactivation. Spatially and temporally defined molecular knockouts. Curr Biol 5:1255-1256.
75. Muller BK, Jay DG, Bonhoeffer F. 1996. Chromophore-assisted laser inactivation of a repulsive axonal guidance molecule. Curr Biol 6:1497-1502.
76. Murray BA, Hemperly JJ, Prediger EA, Edelman GM, Cunningham BA. 1986. Alternatively spliced mRNAs code for different polypeptide chains of the chicken neural cell adhesion molecule (N-CAM). J Cell Biol 102:189-193.
77. Pollerberg GE, Beck-Sickingen A. 1993. A functional role for the middle extracellular region of the neural cell adhesion molecule (NCAM) in axonal fasciculation and orientation. Dev Biol 56:324-340.
78. Rutishauser U, Gall WE, Edelman GM. 1978. Adhesion among neural cells of the chick embryo. IV. Role of the cell surface molecule CAM in the formation of neurite bundles in cultures of spinal ganglia. J Cell Biol 79:382-393.
79. Sattilaro RF, Dentier WL, LeCluyse EL. 1981. Microtubule-associated-proteins (MAPs) and the organization of actin filaments in vitro. J Cell Biol 90:467-473.
80. Schmucker D, Su AL, Beermann A, Jackle H, Jay DG. 1994. Chromophore-assisted laser inactivation of patched protein switches cell fate in the larval visual system of Drosophila. Proc Natl Acad Sci USA 91:2664-2668.
81. Schroder R, Jay DG, Tautz D. 1999. Elimination of EVE protein by CALI in the short germ band insect Tribolium suggests a conserved pair-rule function for even skipped. Mech Dev 80:191-195.
82. Schroeder R, Tautz D, Jay DG. 1996. Chromophore assisted laser inactivation of even skipped in Drosophila phenocopies genetic loss of function. Dev Genes Eval 206:86-88.
83. Selden SC, Pollard TD. 1983. Phosphorylation of microtubule-associated proteins regulates their interaction with actin filaments. J Biol Chem 258:7064-7071.
84. Shah EM, Jay DG. 1993. Methods for ablating neurons. Curr Opin Neurobiol 3:738-742.
85. Song HJ, Ming GL, Poo MM. 1997. C-AMP-induced switching in turning direction of nerve growth cones. Nature 388:275-279.
86. Soriano P, Montgomery C, Geske R, Bradley A. 1991. Targeted disruption of the c-src proto-oncogene leads to osteopetrosis in mice. Cell 64:693-702.
87. Stoeckli ET, Landmesser LT. 1995. Axonin-1, Nr-CAM, Ng-CAM play different roles in the in vivo guidance of chick commissural neurons. Neuron 14:1165-1179.
88. Stoeckli ET, Sonderegger P, Pollerberg GE, Landmesser LT. 1997. Interference with axonin-1 and NrCAM interactions unmasks a floor-plate activity inhibitory for commissural axons. Neuron 18:209-221.
89. Strittmatter SM, Fankhauser C, Huang PL, Mashimo H, Fishman MC. 1995. Neuronal pathfinding is abnormal in mice lacking the neuronal growth cone protein GAP-43. Cell 80:445-452.
90. Sydor AM, Su AL, Wang FS, Xu A, Jay DG. 1996. Talin and vinculin play distinct roles in filopodial motility in the neuronal growth cone. J Cell Biol 134:1197-1207.
91. Tabb JS, Molyneaux BJ, Cohen DL, Kuznetsov SA, Langford GM. 1998. Transport of ER vesicles on actin filaments in neurons by myosin V. J Cell Sci 111:3221-3234.
92. Takei Y, Kondo S, Kanada A, Themata S, Noda T, Hirokawa N. 1997. Delayed development of nervous system in mice homozygous for disrupted microtubule-associated protein 1B (MAP1B) gene. J Cell Biol 137:1615-1626.
93. Takei K, Shin RM, Inoue T, Kato K, Mikoshiba K. 1998a. Regulation of nerve growth mediated by inositol 1,4,5-trisphosphate receptors in growth cones. Science 282:1705-1708.
94. Takei Y, Junlin T, Harada A, Inomata-Terada S, Hirokawa N. 1998b. Abnormal development of nervous system in mice lacking tau and MAP1B. Mol Biol Cell 9:394a.
95. Takei K, Chan TA, Wang FS, Deng H, Rutishauser U, Jay DG. 1999. The neural cell adhesion molecules L1 and NCAM-180 act in different steps of neurite outgrowth. J Neurosci (in press). Tanaka E, Sabry J. 1995. Making the connection: cytoskeletal rearrangements during growth cone guidance. Cell 83:171-176.
96. Takei K, Chan TA, Wang FS, Deng H, Rutishauser U, Jay DG. 1999. The neural cell adhesion molecules L1 and NCAM-180 act in different steps of neurite outgrowth. J Neurosci (in press). Tanaka E, Sabry J. 1995. Making the connection: cytoskeletal rearrangements during growth cone guidance. Cell 83:171-176.
97. Tanaka E, Kirschner MW. 1995. The role of microtubules in growth cone turning at substrate boundaries. J Cell Biol 128:127-137.
98. Tsukita S, Yonemura S. 1997. ERM proteins: head-to-tail regulation of actin-plasma membrane interaction. Trends Biochem Sci 22:53-58.
99. Tsukita S, Oishi K, Sato N, Sagara J, Kawai A. 1994. ERM family members as molecular linkers between the cell surface glycoprotein CD44 and actin-based cytoskeletons. J Cell Biol 126:391-401.
100. Wagner MC, Barylko B, Albanesi JP. 1992. Tissue distribution and subcellular localization of mammalian myosin I. J Cell Biol 119:163-170.
101. Wang FS, Jay DG. 1996. Chromophore-assisted laser inactivation (CALI): probing protein function in situ with a high degree of spatial and temporal resultion. Trends Cell Biol 6:442-445.
102. Wang FS, Wolenski JS, Cheney RE, Mooseker MS, Jay DG. 1996. Function of myosin-V in filopodial extension of neuronal growth cones. Science 273:660-663.
103. Williams AF, Barclay AN. 1988. The immunoglobulin superfamily: domains for cell surface recognition. Annu Rev Immunol 6:381-405.
104. Williams EJ, Furness J, Walsh FS, Doherty P. 1994. Characterization of the second messenger pathway underlying neurite outgrowth stimulated by FGF. Development 120:1685-1693.
105. Worley TL, Holt CE. 1996. Expression and herbimycin A-sensitive localization of pp125FAK in retinal growth cones. Neuroreport 7:1133-1137.
106. Wu X, Bowers B, Wei Q, Kocher B, Hammer JA 3rd. 1997. Myosin V associates with melanosomes in mouse melanocytes: evidence that myosin V is an organelle motor. J Cell Sci 110:847-859.
107. Wylie SR, Wu PJ, Patel H, Chantler PD. 1998. A conventional myosin motor drives neurite outgrowth. Proc Natl Acad Sci U S A 95:12967-12972.
108. Yamada, K.M., B.S. Spooner, N.K. Wessells. 1971. Ultrastructure and function of growth cones and axons of cultured nerve cells. J Cell Biol 49:614-635.