1932

Abstract

Cytoplasmic RNA localization is an evolutionarily ancient mechanism for producing cellular asymmetries. This review considers RNA localization in the context of animal development. Both mRNAs and non-protein-coding RNAs are localized in , , ascidian, zebrafish, and echinoderm oocytes and embryos, as well as in a variety of developing and differentiated polarized cells from yeast to mammals. Mechanisms used to transport and anchor RNAs in the cytoplasm include vectorial transport out of the nucleus, directed cytoplasmic transport in association with the cytoskeleton, and local entrapment at particular cytoplasmic sites. The majority of localized RNAs are targeted to particular cytoplasmic regions by -acting RNA elements; in mRNAs these are almost always in the 3′-untranslated region (UTR). A variety of -acting factors—many of them RNA-binding proteins—function in localization. Developmental functions of RNA localization have been defined in , , and . In , localized RNAs program the antero-posterior and dorso-ventral axes of the oocyte and embryo. In , localized RNAs may function in mesoderm induction as well as in dorso-ventral axis specification. Localized RNAs also program asymmetric cell fates during neurogenesis and yeast budding.

Loading

Article metrics loading...

/content/journals/10.1146/annurev.biochem.67.1.335
1998-07-01
2024-12-03
Loading full text...

Full text loading...

/deliver/fulltext/biochem/67/1/annurev.biochem.67.1.335.html?itemId=/content/journals/10.1146/annurev.biochem.67.1.335&mimeType=html&fmt=ahah

Literature Cited

  1. Lipshitz HD. ed 1995. Localized RNAs. Austin, TX: Landes/Springer-Verlag
  2. Meller VH, Wu K-H, Roman G, Kuroda MI, Davis RL. 1997. Cell 88:445–57 [Google Scholar]
  3. Herzing LB, Romer JT, Horn JM, Ashworth A. 1997. Nature 386:272–75 [Google Scholar]
  4. Penny GD, Kay GF, Sheardown SA, Rastan S, Brockdorff N. 1996. Nature 379:131–37 [Google Scholar]
  5. Rebagliati MR, Weeks DL, Harvey RP, Melton DA. 1985. Cell 42:769–77 [Google Scholar]
  6. Frigerio G, Burri M, Bopp D, Baumgartner S, Noll M. 1986. Cell 47:735–46 [Google Scholar]
  7. Berleth T, Burri M, Thoma G, Bopp D, Richstein S. et al. 1988. EMBO J. 7:1749–56 [Google Scholar]
  8. Frohnhöfer HG, Nüsslein-Volhard C. 1986. Nature 324:120–25 [Google Scholar]
  9. King RC. 1970. Ovarian Development in Drosophila melanogaster. New York: Academic
  10. McKearin D, Ohlstein B. 1995. Development 121:2937–47 [Google Scholar]
  11. Lin HF, Yue L, Spradling AC. 1994. Development 120:947–56 [Google Scholar]
  12. Lin HF, Spradling AC. 1995. Dev. Genet. 16:6–12 [Google Scholar]
  13. de Cuevas M, Lee JK, Spradling AC. 1996. Development 122:3959–68 [Google Scholar]
  14. Stephenson EC. 1995. See Ref. 1 63–76
  15. Cooley L, Theurkauf WE. 1994. Science 266:590–96 [Google Scholar]
  16. Ding D, Parkhurst SM, Lipshitz HD. 1993. Proc. Natl. Acad. Sci. USA 90:2512–16 [Google Scholar]
  17. Yue L, Spradling AC. 1992. Genes Dev. 6:2443–54 [Google Scholar]
  18. Mahone M, Saffman EE, Lasko PF. 1995. EMBO J. 14:2043–55 [Google Scholar]
  19. Suter B, Romberg LM, Steward R. 1989. Genes Dev. 3:1957–68 [Google Scholar]
  20. Mach JM, Lehmann R. 1997. Genes Dev. 11:423–35 [Google Scholar]
  21. Neuman-Silberberg FS, Schüpbach T. 1993. Cell 75:165–74 [Google Scholar]
  22. Cheung H-K, Serano TL, Cohen RS. 1992. Development 114:653–61 [Google Scholar]
  23. Lantz V, Ambrosio L, Schedl P. 1992. Development 115:75–88 [Google Scholar]
  24. Kim-Ha J, Smith JL, Macdonald PM. 1991. Cell 66:23–35 [Google Scholar]
  25. Ephrussi A, Dickinson LK, Lehmann R. 1991. Cell 66:37–50 [Google Scholar]
  26. Nakamura A, Amikura R, Mukai M, Kobayashi S, Lasko PF. 1996. Science 274:2075–79 [Google Scholar]
  27. Golumbeski GS, Bardsley A, Tax F, Boswell RE. 1991. Genes Dev. 5:2060–70 [Google Scholar]
  28. Wang C, Dickinson LK, Lehmann R. 1994. Dev. Dyn. 199:103–15 [Google Scholar]
  29. Tirronen M, Lahti V-P, Heino TI, Roos C. 1995. Mech. Dev. 52:65–75 [Google Scholar]
  30. Hales KH, Meredith JE, Storti RV. 1994. Dev. Biol. 165:639–53 [Google Scholar]
  31. Theurkauf WE. 1994. Dev. Biol. 165:352–60 [Google Scholar]
  32. St. Johnston D, Driever W, Berleth T, Richstein S, Nüsslein-Volhard C. 1989. Development 107(Suppl.):13–19 [Google Scholar]
  33. Karlin-McGinnes M, Serano TL, Cohen RS. 1996. Dev. Genet. 19:238–48 [Google Scholar]
  34. Roth S, Neuman-Silberberg FS, Barcelo G, Schüpbach T. 1995. Cell 81:967–78 [Google Scholar]
  35. González-Reyes A, Elliot H, Johnston DS. 1995. Nature 375:654–58 [Google Scholar]
  36. Clark IE, Jan LY, Jan YN. 1997. Development 124:461–70 [Google Scholar]
  37. Pokrywka N-J, Stephenson EC. 1995. Dev. Biol. 167:363–70 [Google Scholar]
  38. Lane ME, Kalderon D. 1994. Genes Dev. 8:2986–95 [Google Scholar]
  39. Ruohola H, Bremer KA, Baker D, Swedlow JR, Jan LY, Jan YN. 1991. Cell 66:433–49 [Google Scholar]
  40. Gillespie DE, Berg CA. 1995. Genes Dev. 9:2495–508 [Google Scholar]
  41. Clark I, Giniger E, Ruohola-Baker H, Jan LY, Jan YN. 1994. Curr. Biol. 4:289–300 [Google Scholar]
  42. González-Reyes A, Johnston DS. 1994. Science 266:639–41 [Google Scholar]
  43. Gavis ER, Curtis D, Lehmann R. 1996. Dev. Biol. 176:36–50 [Google Scholar]
  44. Zaccai M, Lipshitz HD. 1996. Dev. Genet. 19:249–57 [Google Scholar]
  45. Zaccai M, Lipshitz HD. 1996. Zygote 4:159–66 [Google Scholar]
  46. Deleted in proof
  47. Lasko PF. 1994. Molecular Genetics of Drosophila oogenesis. Austin, TX: Landes
  48. Mahajan-Miklos S, Cooley L. 1994. Cell 78:291–301 [Google Scholar]
  49. Cooley L, Verheyen E, Ayers K. 1992. Cell 69:173–84 [Google Scholar]
  50. Cant K, Knowles BA, Mooseker MS, Cooley L. 1994. J. Cell Biol. 125:369–80 [Google Scholar]
  51. Theurkauf WE, Smiley S, Wong ML, Alberts BM. 1992. Development 115:923–36 [Google Scholar]
  52. Theurkauf WE. 1994. Science 265:2093–96 [Google Scholar]
  53. Deleted in proof
  54. Karr TL, Alberts BM. 1986. J. Cell Biol. 102:1494–509 [Google Scholar]
  55. Sullivan W, Fogarty P, Theurkauf W. 1993. Development 118:1245–54 [Google Scholar]
  56. Wang C, Lehmann R. 1991. Cell 66:637–47 [Google Scholar]
  57. Jongens TA, Hay B, Jan LY, Jan YN. 1992. Cell 70:569–84 [Google Scholar]
  58. Foe VA, Alberts BM. 1983. J. Cell Sci. 61:31–70 [Google Scholar]
  59. Raff JW, Whitfield WGF, Glover DM. 1990. Development 110:1249–61 [Google Scholar]
  60. Dalby B, Glover DM. 1992. Development 115:989–97 [Google Scholar]
  61. Ding D, Lipshitz HD. 1993. Zygote 1:257–71 [Google Scholar]
  62. Whitfield WGF, Gonzalez C, Sanchez-Herrero E, Glover DM. 1989. Nature 338:337–40 [Google Scholar]
  63. Ding D, Parkhurst SM, Halsell SR, Lipshitz HD. 1993. Mol. Cell. Biol. 13:3773–81 [Google Scholar]
  64. Edgar BA, O'Dell GM, Schubiger G. 1987. Genes Dev. 1:1226–37 [Google Scholar]
  65. Davis I, Ish-Horowicz D. 1991. Cell 67:927–40 [Google Scholar]
  66. Gergen JP, Butler BA. 1988. Genes Dev. 2:1179–93 [Google Scholar]
  67. Tepass U, Speicher SA, Knust E. 1990. Cell 61:787–99 [Google Scholar]
  68. Baker NE. 1988. Dev. Biol. 125:96–108 [Google Scholar]
  69. Macdonald PM, Ingham PW, Struhl G. 1986. Cell 47:721–34 [Google Scholar]
  70. King ML. 1995. See Ref. 1 137–48
  71. Dumont JN. 1972. J. Morphol. 136:153–80 [Google Scholar]
  72. Gerhart J, Keller R. 1986. Annu. Rev. Cell Biol. 2:201–29 [Google Scholar]
  73. Gerhart J, Danilchik M, Doniach T, Roberts S, Rowning B, Stewart R. 1989. Development 107(Suppl.):37–51 [Google Scholar]
  74. Kloc M, Etkin LD. 1995. See Ref. 1 149–56
  75. Smith JL, Wilson JE, Macdonald PM. 1992. Cell 70:849–59 [Google Scholar]
  76. Ephrussi A, Lehmann R. 1992. Nature 358:387–92 [Google Scholar]
  77. Wylie CC, Heasman J, Snape A, O'Driscoll M, Holwill S. 1985. Dev. Biol. 112:66–72 [Google Scholar]
  78. Mosquera L, Forristall C, Zhou Y, King ML. 1993. Development 117:377–86 [Google Scholar]
  79. Zhou Y, King M-L. 1996. Development 122:2947–53 [Google Scholar]
  80. Wylie CC, Brown D, Godsave SF, Quarmby J, Heasman J. 1985. J. Embryol. Exp. Morphol. 89(Suppl.):1–15 [Google Scholar]
  81. Linnen JM, Bailey CP, Weeks DL. 1993. Gene 128:181–88 [Google Scholar]
  82. Weeks DL, Melton DA. 1987. Proc. Natl. Acad. Sci. USA 84:2798–802 [Google Scholar]
  83. Hudson JW, Alarcón VB, Elinson RP. 1996. Dev. Genet. 19:190–98 [Google Scholar]
  84. Otte AP, McGrew LL, Olate J, Nathanson NM, Moon RT. 1992. Development 116:141–46 [Google Scholar]
  85. Hinkley CS, Martin JF, Leibham D, Perry M. 1992. Mol. Cell. Biol. 12:638–49 [Google Scholar]
  86. Otte AP, Moon RT. 1992. Cell 68:1021–29 [Google Scholar]
  87. Kloc M, Reddy BA, Miller M, Eastman E, Etkin L. 1991. Mol. Reprod. Dev. 28:341–45 [Google Scholar]
  88. Reddy BA, Kloc M, Etkin LD. 1992. Mech. Dev. 39:1–8 [Google Scholar]
  89. Kloc M, Miller M, Carrasco A, Eastman E, Etkin L. 1989. Development 107:899–907 [Google Scholar]
  90. Kloc M, Etkin LD. 1995. Development 121:287–97 [Google Scholar]
  91. Stennard F, Carnac G, Gurdon JB. 1996. Development 122:4179–88 [Google Scholar]
  92. Zhang J, King M-L. 1996. Development 122:4119–29 [Google Scholar]
  93. Melton DA. 1987. Nature 328:80–82 [Google Scholar]
  94. Yisraeli JK, Sokol S, Melton DA. 1990. Development 108:289–98 [Google Scholar]
  95. Elinson RP, King M-L, Forristall C. 1993. Dev. Biol. 160:554–62 [Google Scholar]
  96. Pondel MD, King ML. 1988. Proc. Natl. Acad. Sci. USA 85:7612–16 [Google Scholar]
  97. Kloc M, Spohr G, Etkin LD. 1993. Science 262:1712–14 [Google Scholar]
  98. Ku M, Melton DA. 1993. Development 119:1161–73 [Google Scholar]
  99. Zhou Y, King ML. 1997. Dev. Biol. 179:173–83 [Google Scholar]
  100. Swalla BJ, Jeffery WR. 1996. Dev. Biol. 178:23–34 [Google Scholar]
  101. Swalla BJ, Jeffery WR. 1995. Dev. Biol. 170:353–64 [Google Scholar]
  102. Swalla BJ, Jeffrey WR. 1996. Dev. Genet. 19:258–67 [Google Scholar]
  103. Vlahou A, Gonzalez-Rimbau M, Flytzanis CN. 1996. Development 122:521–26 [Google Scholar]
  104. Steward O, Kleiman R, Banker G. 1995. See Ref. 1 235–55
  105. Van Minnen J. 1994. Histochem. J. 26:377–91 [Google Scholar]
  106. Garner CC, Tucker RP, Matus A. 1988. Nature 336:674–76 [Google Scholar]
  107. Tiedge H, Fremeau RT, Weinstock PH, Arancio O, Brosius J. 1991. Proc. Natl. Acad. Sci. USA 88:2093–97 [Google Scholar]
  108. Tiedge H, Chen W, Brosius J. 1993. J. Neurosci. 13:2382–90 [Google Scholar]
  109. Mayford M, Baranes D, Podsypanina K, Kandel ER. 1996. Proc. Natl. Acad. Sci. USA 93:13250–55 [Google Scholar]
  110. Furuichi T, Simon-Chazottes D, Fujino I, Yamada N. et al. 1993. Recept. Channels 1:11–24 [Google Scholar]
  111. Tiedge H, Zhou A, Thorn NA, Brosius J. 1993. J. Neurosci. 13:4214–19 [Google Scholar]
  112. Litman P, Barg J, Rindzoonski L, Ginzburg I. 1993. Neuron 10:627–38 [Google Scholar]
  113. Hannan AJ, Schevzov G, Gunning P, Jeffrey PL, Weinberger RP. 1995. Mol. Cell. Neurosci. 6:397–411 [Google Scholar]
  114. Murphy D, Levy A, Lightman S, Carter D. 1989. Proc. Natl. Acad. Sci. USA 86:9002–5 [Google Scholar]
  115. Jirikowski GF, Sanna PP, Bloom FE. 1990. Proc. Natl. Acad. Sci. USA 87:7400–4 [Google Scholar]
  116. Mohr E, Fehr S, Richter D. 1991. EMBO J. 10:2419–24 [Google Scholar]
  117. Mohr E, Richter D. 1992. Eur. J. Neurosci. 9:870–76 [Google Scholar]
  118. Ressler KJ, Sullivan SL, Buck LB. 1994. Cell 79:1245–55 [Google Scholar]
  119. Vassar R, Chao SK, Sitcheran R, Nuñez JM, Vosshall LB, Axel R. 1994. Cell 79:981–91 [Google Scholar]
  120. Trapp BD, Moench T, Pully M, Barbosa E, Tennekoon G, Griffin J. 1987. Proc. Natl. Acad. Sci. USA 84:7773–77 [Google Scholar]
  121. Colman DR, Kriebich G, Frey AB, Sabatini DD. 1982. J. Cell Biol. 95:598–608 [Google Scholar]
  122. Laitala-Leinonen T, Howell ML, Dean GE, Väänänen HK. 1996. Mol. Biol. Cell 7:129–42 [Google Scholar]
  123. Sundell CL, Singer RH. 1991. Science 253:1275–77 [Google Scholar]
  124. Lawrence JB, Singer RH. 1986. Cell 45:407–15 [Google Scholar]
  125. Cheng H, Bjerknes M. 1989. J. Mol. Biol. 210:541–49 [Google Scholar]
  126. Banerjee U, Renfranz PJ, Pollock JA, Benzer S. 1987. Cell 49:281–91 [Google Scholar]
  127. Li P, Yang XH, Wasser M, Cai Y, Chia W. 1997. Cell 90:437–47 [Google Scholar]
  128. Long RM, Singer RH, Meng XH, Gonzalez I, Nasmyth K, Jansen R-P. 1997. Science 277:383–87 [Google Scholar]
  129. Takizawa P, Sil A, Swedlow JR, Herskowitz I, Vale RD. 1997. Nature 389:90–93 [Google Scholar]
  130. Daneholt B. 1997. Cell 88:585–88 [Google Scholar]
  131. Francis-Lang H, Davis I, Ish-Horowicz D. 1996. EMBO J. 15:640–49 [Google Scholar]
  132. Kobayashi S, Okada M. 1990. Nucleic Acids Res. 18:4592 [Google Scholar]
  133. Kobayashi S, Okada M. 1989. Development 107:733–42 [Google Scholar]
  134. Kobayashi S, Amikura R, Okada M. 1993. Science 260:1521–24 [Google Scholar]
  135. Kobayashi S, Amikura R, Okada M. 1994. Int. J. Dev. Biol. 38:193–99 [Google Scholar]
  136. Kobayashi S, Amikura R, Nakamura A, Saito H, Okada M. 1995. Dev. Biol. 169:384–86 [Google Scholar]
  137. Ding D, Whittaker KL, Lipshitz HD. 1994. Dev. Biol. 163:503–15 [Google Scholar]
  138. Gottlieb E. 1990. Curr. Opin. Cell Biol. 2:1080–86 [Google Scholar]
  139. Gavis ER, Lehmann R. 1994. Nature 369:315–18 [Google Scholar]
  140. Dahanukar A, Wharton RP. 1996. Genes Dev. 10:2610–20 [Google Scholar]
  141. Smibert CA, Wilson JE, Kerr K, Macdonald PM. 1996. Genes Dev. 10:2600–9 [Google Scholar]
  142. Halsell SR, Lipshitz HD. 1995. See Ref. 1 9–39
  143. Deleted in proof
  144. Cooperstock RL, Lipshitz HD. 1998. Semin. Cell Dev. Biol. 8(6):541–49 [Google Scholar]
  145. Li MG, McGrail M, Serr M, Hays TS. 1994. J. Cell Sci. 126:1475–94 [Google Scholar]
  146. McGrail M, Hays TS. 1997. Development 124:2409–19 [Google Scholar]
  147. Pokrywka N-J, Stephenson EC. 1994. Dev. Biol. 166:210–19 [Google Scholar]
  148. Suter B, Steward R. 1991. Cell 67:917–26 [Google Scholar]
  149. Lantz V, Chang JS, Horabin JI, Bopp D, Schedl P. 1994. Genes Dev. 8:598–613 [Google Scholar]
  150. Pokrywka NJ, Stephenson EC. 1991. Development 113:55–66 [Google Scholar]
  151. Macdonald PM, Kerr K. 1997. RNA 3:1413–1420 [Google Scholar]
  152. Erdélyi M, Michon A-M, Guichet A, Glozter JB, Ephrussi A. 1995. Nature 377:524–27 [Google Scholar]
  153. Tetzlaff MT, Jäckle H, Pankratz MJ. 1996. EMBO J. 15:1247–54 [Google Scholar]
  154. Deshler JO, Highett MI, Schnapp BJ. 1997. Science 276:1128–31 [Google Scholar]
  155. Knowles RB, Sabry JH, Martone ME, Deerinck TJ, Ellisman MH. et al. 1996. J. Neurosci. 16:7812–20 [Google Scholar]
  156. Ainger K, Avossa D, Morgan F, Hill SJ, Barry C. et al. 1993. J. Cell Biol. 123:431–41 [Google Scholar]
  157. Behar L, Marx R, Sadot E, Barg J, Ginzburg I. 1995. Int. J. Dev. Neurosci. 13:113–27 [Google Scholar]
  158. Litman P, Behar L, Elisha Z, Yisraeli JK, Ginzburg I. 1996. Dev. Biol. 176:80–94 [Google Scholar]
  159. Glotzer JB, Saffrich R, Glotzer M, Ephrussi A. 1997. Curr. Biol. 7:326–37 [Google Scholar]
  160. Swan A, Suter B. 1996. Development 122:3577–86 [Google Scholar]
  161. Kloc M, Etkin LD. 1994. Science 265:1101–3 [Google Scholar]
  162. Wang SX, Hazelrigg T. 1994. Nature 369:400–3 [Google Scholar]
  163. Ferrandon D, Elphick L, Nüsslein-Volhard C, St. Johnston D. 1994. Cell 79:1221–32 [Google Scholar]
  164. Ferrandon D, Koch I, Westhof E, Nüsslein-Volhard C. 1997. EMBO J. 16:1751–58 [Google Scholar]
  165. Walter P, Johnson AE. 1994. Annu. Rev. Cell Biol. 10:87–119 [Google Scholar]
  166. Macdonald PM, Struhl G. 1988. Nature 336:595–98 [Google Scholar]
  167. Macdonald PM. 1990. Development 110:161–72 [Google Scholar]
  168. Kim-Ha J, Webster PJ, Smith JL, Macdonald PM. 1993. Development 119:169–78 [Google Scholar]
  169. Lantz V, Schedl P. 1994. Mol. Cell Biol. 14:2235–42 [Google Scholar]
  170. Mowry KL, Melton DA. 1992. Science 255:991–94 [Google Scholar]
  171. Kislauskis EH, Zhu X-C, Singer RH. 1994. J. Cell Biol. 127:441–51 [Google Scholar]
  172. Jackson RJ. 1993. Cell 74:9–14 [Google Scholar]
  173. Muslimov IA, Santi E, Homel P, Perini S, Higgins D, Tiedge H. 1997. J. Neurosci. 17:4722–33 [Google Scholar]
  174. Whittaker KL, Lipshitz HD. 1995. See Ref. 1 41–61
  175. Kislauskis EH, Li ZF, Singer RH, Taneja KL. 1993. J. Cell Biol. 123:165–72 [Google Scholar]
  176. Macdonald PM, Kerr K, Smith JL, Leask A. 1993. Development 118:1233–43 [Google Scholar]
  177. Macdonald PM, Leask A, Kerr K. 1995. Proc. Natl. Acad. Sci. USA 92:10787–91 [Google Scholar]
  178. St. Johnston D, Brown NH, Gall JG, Jantsch M. 1992. Proc. Natl. Acad. Sci. USA 89:10979–83 [Google Scholar]
  179. St. Johnston D, Beuchle D, Nüsslein-Volhard C. 1991. Cell 66:51–63 [Google Scholar]
  180. Ding D, Lipshitz HD. 1993. BioEssays 10:651–58 [Google Scholar]
  181. Serano T, Cohen R. 1995. Development 121:3809–18 [Google Scholar]
  182. Dalby B, Glover DM. 1993. EMBO J. 12:1219–27 [Google Scholar]
  183. Gautreau D, Cote CA, Mowry KL. 1997. Development 124:5013–20 [Google Scholar]
  184. Kim-Ha J, Kerr K, Macdonald PM. 1995. Cell 81:403–12 [Google Scholar]
  185. Gavis ER, Lunsford L, Bergsten SE, Lehmann R. 1996. Development 122:2791–800 [Google Scholar]
  186. Webster PJ, Liang L, Berg CA, Lasko P, Macdonald PM. 1997. Genes Dev. 11:2510–21 [Google Scholar]
  187. Yisraeli JK, Oberman F, Pressman Schwartz S, Havin L, Elisha Z. 1995. See Ref. 1 157–71
  188. Schüpbach T, Wieschaus E. 1986. Roux's Arch. Dev. Biol. 195:302–17 [Google Scholar]
  189. Frohnhöfer HG, Nüsslein-Volhard C. 1987. Genes Dev. 1:880–90 [Google Scholar]
  190. Rongo C, Gavis E, Lehmann R. 1995. Development 121:2737–46 [Google Scholar]
  191. Bandziulis R, Swanson MS, Dreyfuss G. 1989. Genes Dev. 3:431–37 [Google Scholar]
  192. Schüpbach T, Wieschaus E. 1991. Genetics 129:1119–36 [Google Scholar]
  193. Castrillon DH, Gönczy P, Alexander S, Rawson R, Eberhart CG. et al. 1993. Genetics 135:489–505 [Google Scholar]
  194. Lasko PF, Ashburner M. 1988. Nature 335:611–16 [Google Scholar]
  195. Hay B, Jan LY, Jan YN. 1988. Cell 55:577–87 [Google Scholar]
  196. Liang L, Diehl-Jones W, Lasko P. 1994. Development 120:1201–11 [Google Scholar]
  197. Schwartz SP, Aisenthal L, Elisha Z, Oberman F, Yisraeli JK. 1992. Proc. Natl. Acad. Sci. USA 89:11895–99 [Google Scholar]
  198. Perry-O'Keefe H, Kintner C, Yisraeli J, Melton DA. 1990. In In situ Hybridization and the Study of Development and Differentiation, ed. N Harris, D Wilkenson 115–30 Cambridge: Cambridge Univ. Press
  199. Elisha Z, Havin L, Ringel I, Yisraeli JK. 1995. EMBO J. 14:5109–14 [Google Scholar]
  200. Mowry KL. 1996. Proc. Natl. Acad. Sci. USA 93:14608–13 [Google Scholar]
  201. Marcey D, Watkins WS, Hazelrigg T. 1991. EMBO J. 10:4259–66 [Google Scholar]
  202. Macdonald PM, Luk SKS, Kilpatrick M. 1991. Genes Dev. 5:2455–66 [Google Scholar]
  203. Chao Y-C, Donahue KM, Pokrywka NJ, Stephenson EC. 1991. Dev. Genet. 12:333–41 [Google Scholar]
  204. Hegdé J, Stephenson EC. 1993. Development 119:457–70 [Google Scholar]
  205. Webster P, Suen J, Macdonald P. 1994. Development 120:2027–37 [Google Scholar]
  206. Lasko PF, Ashburner M. 1990. Genes Dev. 4:905–21 [Google Scholar]
  207. Hay B, Ackerman L, Barbel S, Jan LY, Jan YN. 1988. Development 103:625–40 [Google Scholar]
  208. Hay B, Jan LY, Jan YN. 1990. Development 109:425–33 [Google Scholar]
  209. Yoon C, Kawakami K, Hopkins N. 1997. Development 124:3157–66 [Google Scholar]
  210. Christerson LB, McKearin DM. 1994. Genes Dev. 8:614–28 [Google Scholar]
  211. Kelley RL. 1993. Genes Dev. 7:948–60 [Google Scholar]
  212. Serano TL, Karlin-McGinnes M, Cohen RS. 1995. Mech. Dev. 51:183–92 [Google Scholar]
  213. Prost E, Derychere F, Roos C, Haenlin M, Pantesco V, Mohier E. 1988. Genes Dev. 2:891–900 [Google Scholar]
  214. Wilson JE, Connell JE, Schlenker JD, Macdonald PM. 1996. Dev. Genet. 19:199–209 [Google Scholar]
  215. Rittenhouse KR, Berg CA. 1995. Development 121:3032–33 [Google Scholar]
  216. Wilson JE, Connell JE, Macdonald PM. 1996. Development 122:1631–39 [Google Scholar]
  217. St. Johnston D. 1995. Cell 81:161–70 [Google Scholar]
  218. Neuman-Silberberg FS, Schupbach T. 1994. Development 120:2457–63 [Google Scholar]
  219. Driever W, Nüsslein-Volhard C. 1988. Cell 54:83–93 [Google Scholar]
  220. Driever W, Nüsslein-Volhard C. 1988. Cell 54:95–104 [Google Scholar]
  221. Struhl G, Struhl K, Macdonald PM. 1989. Cell 57:1259–73 [Google Scholar]
  222. Driever W, Thoma G, Nüsslein-Volhard C. 1989. Nature 340:363–67 [Google Scholar]
  223. Driever W, Nüsslein-Volhard C. 1989. Nature 337:138–43 [Google Scholar]
  224. Driever W, Siegel V, Nüsslein-Volhard C. 1990. Development 109:811–20 [Google Scholar]
  225. Wharton RP, Struhl G. 1991. Cell 67:955–67 [Google Scholar]
  226. Rivera-Pomar R, Niessing D, Schmidt-Ott U, Gehring WJ, Jäckle H. 1996. Nature 379:746–49 [Google Scholar]
  227. Dubnau J, Struhl G. 1996. Nature 379:694–99 [Google Scholar]
  228. Mlodzik M, Fjose A, Gehring WJ. 1985. EMBO J. 4:2961–69 [Google Scholar]
  229. Macdonald PM, Struhl G. 1986. Nature 324:537–45 [Google Scholar]
  230. Lehmann R, Nüsslein-Volhard C. 1991. Developmen 112:679–93 [Google Scholar]
  231. Gavis ER, Lehmann R. 1992. Cell 71:301–13 [Google Scholar]
  232. Hülskamp M, Schröder C, Pfeifle C, Jäckle H, Tautz D. 1989. Nature 338:629–32 [Google Scholar]
  233. Irish V, Lehmann R, Akam M. 1989. Nature 338:646–48 [Google Scholar]
  234. Lehmann R, Nüsslein-Volhard C. 1987. Dev. Biol. 119:402–17 [Google Scholar]
  235. Tautz D, Lehmann R, Schnürch H, Schuh R, Seifert E. et al. 1987. Nature 327:383–89 [Google Scholar]
  236. Stanojevic D, Hoey T, Levine M. 1989. Nature 341:331–35 [Google Scholar]
  237. Lehmann R, Nüsslein-Volhard C. 1987. Nature 329:167–70 [Google Scholar]
  238. Lehmann R, Nüsslein-Volhard C. 1986. Cell 47:141–52 [Google Scholar]
  239. Jongens TA, Ackerman LD, Swedlow JR, Jan LY, Jan YN. 1994. Genes Dev. 8:2123–36 [Google Scholar]
  240. Kobayashi S, Yamada M, Asaoka M, Kitamura T. 1996. Nature 380:708–11 [Google Scholar]
  241. Thomsen GH, Melton DA. 1993. Cell 74:433–41 [Google Scholar]
  242. Dale L, Matthews G, Colman A. 1993. EMBO J. 12:4471–80 [Google Scholar]
  243. Kondaiah P, Sands M, Smith JM, Fields A, Roberts AB. et al. 1990. J. Biol. Chem. 265:1089–93 [Google Scholar]
  244. Doe CQ, Chu-LaGraff Q, Wright DM, Scott MP. 1991. Cell 65:451–64 [Google Scholar]
  245. Vaessin H, Grell E, Wolff E, Bier E, Jan LY, Jan YN. 1991. Cell 67:941–53 [Google Scholar]
  246. Hirata J, Nakagoshi H, Nabeshima Y-I, Matsuzuka F. 1995. Nature 377:627–30 [Google Scholar]
  247. Knoblich JA, Jan LY, Jan YN. 1995. Nature 377:624–27 [Google Scholar]
  248. Shen C-P, Jan LY, Jan YN. 1997. Cell 90:449–58 [Google Scholar]
  249. Jeffery WR, Tomlinson CR, Brodeur RD. 1983. Dev. Biol. 99:408–20 [Google Scholar]
  250. Macdonald PM. 1992. Development 114:221–32 [Google Scholar]
  251. Aït-Ahmed O, Thomas-Cavallin M, Rosset R. 1987. Dev. Biol. 122:153–62 [Google Scholar]
  252. Pomeroy ME, Lawrence JB, Singer RH, Billings-Gagliardi S. 1991. Dev. Biol. 143:58–67 [Google Scholar]
  253. Trembleau A, Calas A, Fèvre-Montange M. 1990. Mol. Brain Res. 8:37–45 [Google Scholar]
  254. Perry BA. 1988. Cell Differ. Dev. 25:99–108 [Google Scholar]
/content/journals/10.1146/annurev.biochem.67.1.335
Loading
/content/journals/10.1146/annurev.biochem.67.1.335
Loading

Data & Media loading...

  • Article Type: Introduction
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error