The Drosophila neuromuscular junction: A model system for studying synaptic development and function

Annual Review of Neuroscience

Volumn 19, Issue , 1996, Pages 545-575

  Keshishian, Haig ^a   Broadie, Kendal ^b   Chiba, Akira ^c   Bate, Michael ^b  

^a YALE UNIVERSITY   (United States)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

axonogenesis; motoneurons; muscle; synaptic transmission; synaptogenesis

Indexed keywords

CELL ADHESION MOLECULE; CONNECTIN; TRANSCRIPTION FACTOR;

ANIMAL CELL; CELL ADHESION; CENTRAL NERVOUS SYSTEM; DROSOPHILA; EMBRYO; GENE EXPRESSION; GROWTH CONE; MOLECULAR GENETICS; MOTONEURON; MUSCLE DEVELOPMENT; NERVE CELL PLASTICITY; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; REVIEW; SYNAPTIC TRANSMISSION; SYNAPTOGENESIS;

EID: 0029926999     PISSN: 0147006X     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.ne.19.030196.002553     Document Type: Review

References (133)

1. Abmayr SM, Erickson MS, Bour BA. 1995. Embryonic development of the larval bodywall musculature of Drosophila melanogaster. Trends Genet. 11:153-59
2. Aceves-Pina EO, Booker R, Duerr JS, Livingstone MS, Quinn WG, et al. 1983. Learning and memory in Drosophila, studied with mutants. Cold Spring Harbor Symp. Quant. Biol. 48:831-40
3. Atwood HL, Govind CK, Wu C-F. 1993. Differential ultrastructure of synaptic terminals on ventral longitudinal abdominal muscles in Drosophila larvae. J. Neurobiol. 24:1008-24
4. Anderson MDS, Halpern ME, Keshishian H. 1988. Identification of the neuropeptide transmitter proctolin in Drosophila larvae: characterization of muscle fiber-specific neuromuscular endings. J. Neurosci. 8: 242-55
5. Baker R, Schubiger G. 1995. Ectoderm induces muscle-specific gene expression in Drosophila embryos. Development 121:387-98
6. Bate M. 1990. The embryonic development of larval muscle fibers in Drosophila. Development 110:791-804
7. Bate M. 1993. The mesoderm and its derivatives. See Bate & Martinez Arias 1993, pp. 1013-90
8. Bate CM, Martinez Arias A, eds. 1993. The Development of Drosophila melanogaster. New York: Cold Spring Harbor Press
9. Bate M, Rushton E. 1993. Myogenesis and muscle patterning in Drosophila. C. R. Acad. Sci. Ser. C 316:1047-61
10. Bate M, Rushton E, Frasch M. 1993. A dual requirement for neurogenic genes in Drosophila myogenesis. Development. pp. 149-61 (Suppl.)
11. Baylies MK, Martinez Arias AM, Bate M. 1995. wingless is required for the proper specification of a subset of muscle founder cells during Drosophila embryogenesis. Development. In press
12. Bentley D, O'Connor TP. 1994. Cytoskeletal events in growth cone steering. Curr. Opin. Neurobiol. 4:43-48
13. Bodmer R. 1993. The gene tinman is required for specification of the heart and visceral muscles in Drosophila. Development 118: 719-29
14. Bourgouin C, Lundgren SE, Thomas JB. 1992. apterous is a Drosophila LIM domain gene required for the development of a subset of embryonic muscles. Neuron 9:549-61
15. Brand AH, Perrimon N. 1993. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401-15
16. Broadie KS, Bate M. 1993a. Development of the embryonic neuromuscular synapse of Drosophila melanogaster. J. Neurosci. 13: 144-66
17. Broadie KS, Bate M. 1993b. Development of larval muscle properties in the embryonic myotubes of Drosophila melanogasler. J. Neurosci. 13:167-80
18. Broadie KS, Bate M. 1993c. Innervation directs receptor synthesis and localization in Drosophila embryo synaptogenesis. Nature 361: 350-53
19. Broadie K, Bate M. 1993d. Muscle development is independent of innervation during Drosophila embryogenesis. Development 119:533-43
20. Broadie K, Bate M. 1993e. Activity-dependent development of the neuromuscular synapse during Drosophila embryogenesis. Neuron 11:607-19
21. Broadie K, Bellen HJ, DiAntonio A, Littleton JT, Schwarz TL. 1994. Absence of synaptotagmin disrupts excitation-secretion coupling during synaptic transmission. Proc. Natl. Acad. Sci. USA 91:10727-31
22. Broadie K, Sink H, Van Vactor D, Fambrough D, Whitington PM, et al. 1993. From growth cone to synapse, the life history of the RP3 motor neuron. Development. pp. 227-38 (Suppl.)
23. Budnik V, Gorczyca M. 1992. SSB, an antigen that selectively labels morphologically distinct synaptic boutons at the Drosophila larval neuromuscular junction. J. Neurobiol. 23:1054-66
24. Budnik V, Zhong Y, Wu C-F. 1990. Morphological plasticity of motor axons in Drosophila mutants with altered excitability. J. Neurosci. 10:3754-68
25. Byers D. Davis RL, Kiger JA. 1981. Defect in cyclic AMP phosphodiesterase due to the dunce mutation of learning in Drosophila melanogaster. Nature 289:79-81
26. Callahan CA, Thomas JB. 1994. Tau-beta galactosidase, an axon-targeted fusion protein. Proc. Natl. Acad. Sci. USA 91:5972-76
27. Campos-Ortega JA. 1993. Early neurogenesis in Drosophila. See Bate & Martinez Arias 1993, pp. 1091-129
28. Campos-Ortega JA, Hanenstein V. 1985. The Embryonic Development of Drosophila melanogaster. Berlin/New York: Springer-Verlag. 227 pp.
29. Cantera R, Nässel DR. 1992. Segmental peptidergic innervation of abdominal targets in larval and adult dipteran insects revealed with an antiserum against leukokinin I. Cell. Tissue Res. 269:459-71
30. Carmena A, Bate M, Jimenez F. 1995. lethal of scute, a proneural gene is required for the specification of muscle progenitors during Drosophila embryogenesis. Genes Dev. In press
31. Cash S, Chiba A, Keshishian H. 1992. Alternate neuromuscular target selection following the loss of single muscle fibers in Drosophila. J. Neurosci. 12:2051-64
32. Chiba A, Hing H, Cash S, Keshishian H. 1993. The growth cone choices of Drosophila motoneurons in response to muscle fiber mismatch. J. Neurosci. 13:714-32
33. Chiba A, Snow P, Keshishian H, Hotta Y. 1995. Fasciclin III and a synaptic recognition molecule in Drosophila. Nature 374:166-68
34. Chu-LaGraff Q, Doe CQ. 1994. Neuroblast specification and formation regulated by wingless in the Drosophila CNS. Science 261:1594-97
35. Corbin V, Michelson AM, Abmayr SM, Neel V, Alcamo E, et al. 1991. A role for the Drosophila neurogenic genes in mesoderm differentiation. Cell 67:311-23
36. Crossley CA. 1978. The morphology and development of the Drosophila muscular system. In The Genetics and Biology of Drosophila, ed. M Ashburner, TRF Wright, 2b:499-560. New York: Academic
37. Currie DA, Truman JW, Burden SJ. 1995. Drosophila glutamate receptor RNA expression in embryonic and larval muscle fibers. Dev. Dyn. 203:311-16
38. Doe CQ. 1992. Molecular markers for identified neuroblasts and ganglion mother cells in the Drosophila central nervous system. Development 116:855-63
39. Doe CQ, Hiromi Y, Gehring WJ, Goodman CS. 1988. Expression and function of the segmentation gene fushi tarazu during Drosophila neurogenesis. Science 239:170-75
40. Doe CQ, Smouse D, Goodman CS. 1988. Control of neuronal fate by the Drosophila segmentation gene even-skipped. Nature 333: 376-78
41. Doe CQ, Technau GM. 1993. Identification and cell lineage of individual neural precursors in the Drosophila CNS. Trends Neurosci. 16:510-14
42. Dohrmann C, Azpiazu N, Frasch M. 1990 A new Drosophila homeobox gene is expressed in mesodermal precursor cells of distinct muscle fibers during embryogenesis. Genes Dev. 4:2098-111
43. Dudai Y, Jan YN, Byers D, Quinn WG, Benzer S. 1976. dunce, a mutant of Drosophila deficient in learning. Proc. Natl. Acad. Sci. USA 73:1684-88
44. Dudai Y, Zvi S. 1985. Multiple defects in the activity of adenylate cyclase from the Drosophila memory mutant rutabaga. J. Neurochem. 45:355-64
45. Epstein HF, Bernstein SI. 1992. Genetic approaches to understanding muscle development. Dev. Biol. 154:231-44
46. Falls DL, Harris DA, Johnson FA, Morgan MM, Corfas G, Fischbach GD. 1990. Mr 42,000 ARIA: a protein that may regulate the accumulation of acetylcholine receptors at developing chick neuromuscular junctions. Cold Spring Harbor Symp. Quant. Biol. 55: 397-406
47. Feany MB, Quinn WG. 1995. A neuropeptide gene defined by the Drosophila memory mutant amnesiac. Science 268:869-73
48. Fontaine B, Klarsfeld A, Hokfelt T, Changeux JP. 1986. Calcitonin gene-related peptide, a peptide present in spinal cord motoneurons, increases the number of acetylcholine receptors in primary cultures of chick embryo myotubes. Neurosci. Lett. 71:59-65
49. Fontaine B, Sassoon D, Buckingham M, Changeux JP. 1988. Detection of the nicotinic acetylcholine receptor alpha-subunit mRNA by in situ hybridization at neuromuscular junctions of 15-day-old chick striated muscles. EMBO J. 7:603-39
50. Frasch M. 1995. Induction of visceral and cardiac mesoderm by ectodermal Dpp in the early Drosophila embryo. Nature 374:464-67
51. Fujita SC, Zipursky SL, Benzer S, Ferrus A, Shotwell SL. 1982. Monoclonal antibodies against the Drosophila nervous system. Proc. Natl. Acad. Sci. USA 79:7929-33
52. Gho M. 1994. Voltage-clamp analysis of gap junctions between embryonic muscles of Drosophila. J. Physiol. 481:371-83
53. Giniger E, Jan LY, Jan YN. 1993. Specifying the path of the intersegmental nerve of the Drosophila embryo: a role for Delta and Notch. Development. 117:431-40
54. Goodman CS, Doe CQ. 1993. Embryonic development of the Drosophila central nervous system. See Bate & Martinez Arias 1993, pp. 1131-206
55. Gorczyca M, Augart C, Budnik V. 1993. Insulin-like receptor and insulin-like peptide are localized at neuromuscular junctions in Drosophila. J. Neurosci. 13:3692-704
56. Gorczyca MG, Phillis RW, Budnik V. 1994. The role of tinman, a mesodermal cell fate gene, in axon pathfinding during the development of the transverse nerve in Drosophila. Development 120:2143-52
57. Grenningloh G, Rehm EJ, Goodman CS. 1991. Genetic analysis of growth cone function in Drosophila: fasciclin II functions as a neuronal recognition molecule. Cell 67:45-57
58. Halfon M, Hashimoto C, Keshishian H. 1995. The Drosophila Toll gene functions zygotically and is necessary for proper motoneuron and muscle development. Dev. Biol. 169: 151-67
59. Hall ZW, Sanes JR. 1993. Synaptic structure and development: the neuromuscular junction. Cell 72:99-121
60. Halpern ME, Chiba A, Johansen J, Keshishian H. 1991. Growth cone behavior underlying the development of stereotypic synaptic connections in Drosophila embryos. J. Neurosci. 11:3227-38
61. Harrelson AL, Goodman CS. 1988. Growth cone guidance in insects: fasciclin II is a member of the immunoglobulin superfamily. Science 242:700-8
62. Harrison SD, Broadie K, van de Goor J, Rubin GM. 1994. Mutations in the Drosophila Rop gene suggest a function in general secretion and synaptic transmission. Neuron 13:555-66
63. Ho RK, Ball EE, Goodman CS. 1983. Muscle pioneers: large mesodermal cells that erect a scaffold for developing muscles and motoneurones in grasshopper embryos. Nature 301:66-69
64. Immergluck K, Lawrence PA, Bienz M. 1990. Induction across germ layers in Drosophila mediated by a genetic cascade. Cell 62:261-68
65. Ito K, Urban J, Technau GM. 1995. Distribution, classification, and development of Drosophila glial cells in the late embryonic and early larval nerve cord. Roux Arch. Dev. Biol. 204:284-307
66. Jacobs JR, Goodman CS. 1989. Embryonic development of axon pathways in the Drosophila CNS: II. Behavior of pioneer growth cones. J. Neurosci. 9:2412-24
67. Jan LY, Jan YN. 1976a. Properties of the larval neuromuscular junction in Drosophila melanogaster. J. Physiol. 262:189-214
68. Jan LY, Jan YN. 1976b. L-Glulamate as an excitatory transmitter at the Drosophila larval neuromuscular junction. J. Physiol. 262: 215-36
69. Jarecki J, Keshishian H. 1995. Role of neural activity during synaptogenesis in Drosophila. J. Neurosci. 15:8177-90
70. Jia X-X, Gorczyca M, Budnik V. 1993. Ultrastructure of neuromuscular junctions in Drosophila: Comparison of wild type and mutants with increased excitability. J. Neurobiol. 24:1025-44
71. Johansen J, Halpern ME, Johansen KM, Keshishian H. 1989a. Stereotypic morphology of glutamatergic synapses on identified muscle fiber cells of Drosophila larvae. J. Neurosci. 9:710-25
72. Johansen J, Halpern ME, Keshishian H. 1989b. Axonal guidance and the development of muscle fiber-specific innervation in Drosophila embryos. J. Neurosci. 9:4318-32
73. Kandel E, Abel T. 1995. Neuropeptides, adenylyl cyclase, and memory storage. Science 268:825-26
74. Kania A, Bellen HJ. 1995. Mutations in neuromusculin, a gene encoding a cell adhesion molecule, cause nervous system defects. Roux Arch. Dev. Biol. 204:259-270
75. Kania A, Han P-L, Kim Y-T, Bellen H. 1993. neuromusculin, a Drosophila gene expressed in peripheral neuronal precursors and muscles, encodes a cell adhesion molecule. Neuron 11:673-87
76. Keshishian H, Chang TN, Jarecki J. 1994. Precision and plasticity during Drosophila neuromuscular development. FASEB J. 8: 731-37
77. Keshishian H, Chiba A. 1993. Neuromuscular development in Drosophila: insights from single neurons and single genes. Trends Neurosci. 16:278-83
78. Keshishian H, Chiba A, Chang TN, Halfon M, Harkins EW, et al. 1993. The cellular mechanisms governing the development of synaptic connections in Drosophila melanogaster. J. Neurobiol. 24:767-87
79. Kidokoro Y, Nishikawa K. 1994. Miniature endplate currents at the newly formed neuromuscular junction in Drosophila embryos and larvae. Neurosci. Res. 19:143-54
80. Klämbt C, Goodman CS. 1991. The diversity and pattern of glia during axon pathway formation in the Drosophila embryo. Glia 4: 205-13
81. Kolodkin AL, Matthes DJ, Goodman CS. 1993. The semaphorin genes encode a family of transmembrane and secreted growth cone guidance molecules. Cell 75:1389-99
82. Kolodkin AL, Matthes DJ, O'Connor TP, Patel NH, Admon A, et al. 1992. Fasciclin IV: sequence, expression, and function during growth cone guidance in the grasshopper embryo. Neuron 9:831-45
83. Kurdyak P, Atwood HL, Steward BA, Wu CF. 1994. Differential physiology and morphology of motor axons to ventral longtidunal muscle in larval Drosophila. J. Comp. Neurol. 350:463-72
84. Landmesser L, Dahm L, Tang J, Rutishauser U. 1992. Polysialic acid as a regulator of intramuscular nerve branching during embryonic development. Neuron 4:655-67
85. Lawrence PA, Johnston P. 1986. The muscle patterns of a segment of Drosophila may be determined by neurons and not by contributing muscles. Cell 45:505-13
86. Lawrence PA, Johnston P, Vincent JP. 1994. Wingless can bring about a mesoderm-to-ectoderm induction in Drosophila embryos. Development 120:3355-59
87. Lilly B, Galewsky S, Firulli AB, Schulz RA, Olson EN. 1994. D-MEF2: a MADS box transcription factor expressed in differentiating mesoderm and muscle cell lineages during Drosophila embryogenesis. Proc. Natl. Acad. Sci. USA 91:5662-66
88. Lilly B, Zhao B, Ranganayakulu G, Paterson BM, Schulz RA, Olson EN. 1995. Requirement of MADS domain transcription factor D-MEF2 for muscle formation in Drosophila. Science 267:688-93
89. Lin DM, Fetter RD, Kopczynski C, Grenningloh G, Goodman CS. 1994. Genetic analysis of Fasciclin II in Drosophila: defasciculation, refasciculation, and altered fasciculation. Neuron 13:1055-69
90. Lin DM, Goodman CS. 1994. Ectopic and increased expression of fasciclin II alters motoneuron growth cone guidance. Neuron 13: 673-87
91. Litlleton JT, Stern M, Perin M, Bellen HJ. 1994. Calcium dependence of neurotransmitter release and rate of spontaneous vesicle fusions are altered in Drosophila synaptotagmin mutants. Proc. Natl. Acad. Sci USA 91: 10888-92
92. ++-activated neurotransmitter release. Cell 74:1125-34
93. Livingstone MS, Sziber PP, Quinn WG. 1984. Loss of calcium/calmodulin responsiveness in adenylate cyclase of rutabaga, a Drosophila learning mutant. Cell 37:205-15
94. Luo Y, Raible D, Raper JA. 1993. Collapsin: a protein in brain that induces the collapse and paralysis of neuronal growth cones. Cell 75: 217-27
95. Manning G, Krasnow M. 1993. Development of the Drosophila tracheal system. See Bate & Martinez Arias 1993, pp. 609-85
96. Martinez Arias A. 1993. Development and patterning of the larval epidermis of Drosophila. See Bate & Martinez Anas 1993, pp. 517-607
97. Matthes DJ, Sink H, Kolodkin AL, Goodman CS. 1995. Semaphorin II can function as a selective inhibitor of specific synaptic arborizations. Cell 81:631-39
98. McMahan U. 1990. The agrin hypothesis. Cold Spring Harbor Symp. Quant. Biol. 50:407-18
99. Merlie JP, Sanes JR. 1985. Concentration of acetylcholine receptor mRNA in synaptic regions of adult muscle fibres. Nature 317:66-68
100. Messersmith EK, Leonardo ED, Shatz CJ, Tessier-Lavigne M, Goodman CS, Kolodkin AL. 1995. Semaphorin III can function as a selective chemorepellant to pattern sensory projections in the spinal cord. Neuron 14: 949-59
101. Michelson AM, Abmayr SM, Bate M, Martinez Arias A, Maniatis T. 1990. Expression of a MyoD family member prefigures muscle pattern in Drosophila embryos. Genes Develop. 4:2086-97
102. Monastirioti M, Gorczyca M, Rapus J, Eckert M, White K, Budnik V. 1995. Octopamine immunoreactivity in the fruit fly Drosophila melanogaster. J. Comp. Neurol. 356: 275-87
103. New HV, Mudge AW. 1986. Calcitonin gene-related peptide regulates muscle acetylcholine receptor synthesis. Nature 323: 809-11
104. Nguyen HT, Bodmer R, Abmayr SM, McDermott JC, Spoerel NA. 1994. D-mef2: a Drosophila mesoderm-specific MADS box-containing gene with a biphasic expression profile during embryogenesis. Proc. Natl. Acad. Sci. USA 91:7520-24
105. Nose A, Mahajan VB, Goodman CS. 1992. Connectin: a homophilic cell adhesion molecule on a subset of muscles and motoneurons that innervate them in Drosophila. Cell 70: 553-67
106. Nose A, Takeichi M, Goodman CS. 1994. Ectopic expression of connectin reveals a repulsive function during growth cone guidance and synapse formation. Neuron 13:525-39
107. Nusse R, Varmus HE. 1992. Wnt genes. Cell 69:1073-87
108. Patel NH, Ball EE, Goodman CS. 1992. Changing role of even-skipped during the evolution of insect pattern formation. Nature 357:339-42
109. Paterson BM, Walldorf U, Eldridge J, Dübendorfer A, Frasch M, Gehring, WJ. 1991. The Drosophila homologue of vertebrate myogenic-determination genes encodes a transiently expressed nuclear protein marking primary myogenic cells. Proc. Natl. Acad. Sci. USA 88:3782-86
110. Rushton E, Drysdale R, Abmayr SM, Michelson AM, Bate M. 1995. Mutations in a novel gene, myoblast city, provide evidence in support of the founder cell hypothesis for Drosophila muscle development. Development 121:1979-88
111. Schulze KL, Broadie K, Perin MS, Bellen HJ. 1995. Genetic and electrophysiological studies of Drosophila syntaxin-1A demonstrate its role in nonneuronal secretion and neurotransmission. Cell 80:311-20
112. Schulze KL, Litlleton JT, Salzberg A, Halachmi N, Stern M, et al. 1994. rop, a Drosophila homolog of yeast Sec1 and vertebrate n-Sec1/Munc-18 proteins, is a negative regulator of neurotransmitter release in vivo. Neuron 13:1099-108
113. Seeger M, Tear G, Ferres-Marco D, Goodman CS. 1993. Mutations affecting growth cone guidance in Drosophila: genes necessary for guidance toward or away from the midline. Neuron 10:409-26
114. Serafini T, Kennedy TE, Galko MJ, Mirzayan C, Jessell TM, Tessier-Lavigne M. 1994. The netrins define a family of axon outgrowth-promoting proteins homologous to C. elegans UNC-6. Cell 78:409-24
115. Sink H, Goodman CS. 1994. Mutations in side-step lead to defects in pathfinding and synaptic specificity during the development of neuromuscular connectivity in Drosophila. Soc. Neurosci. Abstr. 20:1283.
116. Sink H, Whitington PM. 1991a. Location and connectivity of abdominal motoneurons in the embryo and larva of Drosophila melanogaster. J. Neurobiol. 22:298-311
117. Sink H, Whitington PM. 1991b. Pathfinding in the central nervous system and periphery by identified embryonic Drosophila motor axons. Development 112:307-16
118. Sink H, Whitington PM. 1991c. Early ablation of target muscles modulates the arborisation pattern of an identified embryonic Drosophila motor axon. Development 113:701-7
119. Snow PM, Bieber AJ, Goodman CS. 989. Fasciclin III: a novel homophilic adhesion molecule in Drosophila. Cell 59:313-23
120. Staehling-Hampton K, Hoffmann FM, Baylies MK, Rushton E, Bate M. 1994. dpp induces mesodermal gene expression in Drosophila. Nature 372:783-86
121. Sweeney ST, Broadie K, Keane J, Niemann H, O'Kane CJ. 1995. Targeted expression of tetanus toxin light chain in Drosophila specifically eliminates synaptic transmission and causes behavioral defects. Neuron 14: 341-51
122. Tang J, Landmesser L, Rutishauser U. 1992. Polysialic acid influences specific pathfinding by avian motoneurons. Neuron 8:1031-44
123. Taylor MV, Beatty KE, Hunter HK, Baylies MK. 1995. Drosophila MEF2 is regulated by twist and is expressed in both the primordia and differentiated cells of the embryonic somatic, visceral and heart musculature. Mech. Dev. 50:29-41
124. Truman JW, Bate M. 1988. Spatial and temporal patterns of neurogenesis in the central nervous system of Drosophila melanogaster. Dev. Biol. 125:145-57
125. Van Vactor D, Sink H, Fambrough D, Tsoo R, Goodman CS. 1993. Genes that control neuromuscular specificity in Drosophila. Cell 73:1137-54
126. Yin JC, Del Vecchio M, Zhou H, Tully T. 1995. CREB as a memory modulator: induced expression of a dCREB2 activator isoform enhances long-term memory in Drosophila. Cell 81:107-15
127. Yin JC, Wallach JS, Del Vecchio M, Wilder EL, Zhou H, et al. 1994. Induction of a dominant negative CREB transgene specifically blocks long-term memory in Drosophila. Cell 79:49-58
128. Younossi-Hartenstein A, Hartenstein V. 1993. The role of the tracheae and musculature during pathfinding of Drosophila embryonic sensory axons. Dev. Biol. 158:430-47
129. Zhong Y. 1995. Mediation of PACAP-like neuropeptide transmission by coactivation of Ras/Raf and cAMP signal transduction pathways in Drosophila. Nature 375:88-92
130. Zhong Y, Budnik V, Wu C-F. 1992. Synaptic plasticity in Drosophila memory and hyperexcitable mutants: role of cAMP cascade. J. Neurosci. 12:644-51
131. Zhong Y, Pena LA. 1995. A novel synaptic transmission mediated by a PACAP-like neuropeptide in Drosophila. Neuron 14:527-36
132. Zhong Y, Wu. 1991. Altered synaptic plasticity in Drosophila memory mutants with a defective cyclic AMP cascade. Science 251:198-201
133. Zinsmaier KE, Eberle KK, Buchner E, Walter N, Benzer S. 1994. Paralysis and early death in cysteine string protein mutants of Drosophila. Science 263:977-80