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Development Genes and Evolution

, Volume 214, Issue 2, pp 64–71 | Cite as

An enhancer-trap LacZ transgene reveals a distinct expression pattern of Kinesin family 26B in mouse embryos

  • Yusuke Marikawa
  • Toko C. Fujita
  • Vernadeth B. Alarcón
Short Communication

Abstract

The enhancer-trap system is a useful tool to uncover genes that exhibit a unique tissue-specific expression. Here, we established a transgenic mouse line in which the reporter gene LacZ was specifically expressed in the developing limbs and face in the embryo. To identify the endogenous genes that are controlled by the limb- and face-specific enhancers, we pinpointed the integration site of the transgene, and analyzed the expression pattern of the genes that were located near the integration site. We found that the gene encoding KIF26B, a member of the kinesin superfamily, was preferentially expressed in the limb buds, face, and somite derivatives. Moreover, while a 7.5-kb mRNA was the major Kif26B transcript in the embryo, it was absent in many adult tissues. These results imply that KIF26B may play a role in embryogenesis, specifically in the development of limbs, face, and somites.

Keywords

Mouse embryo Kinesin Enhancer-trap Limb Face 

Notes

Acknowledgements

We give special thanks to S. Lozanoff and M. Kuroyama for helping us with the Celera Genome Database. We are grateful to the staff of the University of Hawaii Laboratory Animal Service and Molecular Biology Core Facility and the members of the Institute for Biogenesis Research for their support. We thank former students, Jessica Hui and James Howard, who participated in the early stage of this project. This work was funded by the Victoria S. and Bradley L. Geist Foundation (20030540) to V.B.A., and the Harold K.L. Castle Foundation and National Institute of Health (HD040208) to Y.M.

References

  1. Alarcón VB, Marikawa Y (2003) Deviation of the blastocyst axis from the first cleavage plane does not affect the quality of mouse postimplantation development. Biol Reprod 69:1208–1212PubMedGoogle Scholar
  2. Aoto K, Nishimura T, Eto K, Motoyama J (2002) Mouse GLI3 regulates Fgf8 expression and apoptosis in the developing neural tube, face, and limb bud. Dev Biol 251:320–332CrossRefPubMedGoogle Scholar
  3. Baskar JF, Smith PP, Ciment GS, Hoffmann S, Tucker C, Tenney DJ, Colberg-Poley AM, Nelson JA, Ghazal P (1996) Developmental analysis of the cytomegalovirus enhancer in transgenic animals. J Virol 70:3215–3226PubMedGoogle Scholar
  4. Chiang C, Litingtung Y, Harris MP, Simandl BK, Li Y, Beachy PA, Fallon JF (2001) Manifestation of the limb prepattern: limb development in the absence of Sonic hedgehog function. Dev Biol 236:421–435CrossRefPubMedGoogle Scholar
  5. Gibson-Brown JJ, Agulnik SI, Chapman DL, Alexiou M, Garvey N, Silver LM, Papaioannou VE (1996) Evidence of a role for T-box genes in the evolution of limb morphogenesis and the specification of forelimb/hindlimb identity. Mech Dev 56:93–101PubMedGoogle Scholar
  6. Guigo R, Dermitzakis ET, Agarwal P, Ponting CP, Parra G, Reymond A, Abril JF, Keibler E, Lyle R, Ucla C, Antonarakis SE, Brent MR (2003) Comparison of mouse and human genomes followed by experimental verification yields an estimated 1,019 additional genes. Proc Natl Acad Sci USA 100:1140–1145CrossRefPubMedGoogle Scholar
  7. Hogan B, Beddington R, Costantini F, Lacy E (1994) Manipulating the mouse embryo, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y., pp 373Google Scholar
  8. Hu D, Helms JA (1999) The role of sonic hedgehog in normal and abnormal craniofacial morphogenesis. Development 126:4873–4884PubMedGoogle Scholar
  9. Kawai J, Shinagawa A, Shibata K, Yoshino M, Itoh M, Ishii Y, Arakawa T, Hara A, Fukunishi Y, Konno H, et al (2001) Functional annotation of a full-length mouse cDNA collection. Nature 409:685–690CrossRefPubMedGoogle Scholar
  10. Kothary R, Barton SC, Franz T, Norris ML, Hettle S, Surani MA (1991) Unusual cell specific expression of a major human cytomegalovirus immediate early gene promoter-lacZ hybrid gene in transgenic mouse embryos. Mech Dev 35:25–31CrossRefPubMedGoogle Scholar
  11. Kruger M, Mennerich D, Fees S, Schafer R, Mundlos S, Braun T (2001) Sonic hedgehog is a survival factor for hypaxial muscles during mouse development. Development 128:743–752PubMedGoogle Scholar
  12. Kuratani S, Martin JF, Wawersik S, Lilly B, Eichele G, Olson EN (1994) The expression pattern of the chick homeobox gene gMHox suggests a role in patterning of the limbs and face and in compartmentalization of somites. Dev Biol 161:357–369CrossRefPubMedGoogle Scholar
  13. Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, Baldwin J, Devon K, Dewar K, Doyle M, FitzHugh W, et al (2001) Initial sequencing and analysis of the human genome. Nature 409:860–921PubMedGoogle Scholar
  14. Lu MF, Cheng HT, Lacy AR, Kern MJ, Argao EA, Potter SS, Olson EN, Martin JF (1999) Paired-related homeobox genes cooperate in handplate and hindlimb zeugopod morphogenesis. Dev Biol 205:145–157CrossRefPubMedGoogle Scholar
  15. Mahmood R, Bresnick J, Hornbruch A, Mahony C, Morton N, Colquhoun K, Martin P, Lumsden A, Dickson C, Mason I (1995) A role for FGF-8 in the initiation and maintenance of vertebrate limb bud outgrowth. Curr Biol 5:797–806PubMedGoogle Scholar
  16. McPherson JD, Marra M, Hillier L, Waterston RH, Chinwalla A, Wallis J, Sekhon M, Wylie K, Mardis ER, Wilson RK, et al (2001) A physical map of the human genome. Nature 409:934–941PubMedGoogle Scholar
  17. Miki H, Setou M, Kaneshiro K, Hirokawa N (2001) All kinesin superfamily protein, KIF, genes in mouse and human. Proc Natl Acad Sci USA 98:7004–7011CrossRefPubMedGoogle Scholar
  18. Nybakken K, Perrimon N (2002) Hedgehog signal transduction: recent findings. Curr Opin Genet Dev 12:503–511CrossRefPubMedGoogle Scholar
  19. O’Kane CJ, Gehring WJ (1987) Detection in situ of genomic regulatory elements in Drosophila. Proc Natl Acad Sci USA 84:9123–9127PubMedGoogle Scholar
  20. Perry AC, Wakayama T, Kishikawa H, Kasai T, Okabe M, Toyoda Y, Yanagimachi R (1998) Mammalian transgenesis by intracytoplasmic sperm injection. Science 284:1180–1183CrossRefGoogle Scholar
  21. Riddle RD, Johnson RL, Laufer E, Tabin C (1993) Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 75:1401–1416PubMedGoogle Scholar
  22. Robbins DJ, Nybakken KE, Kobayashi R, Sisson JC, Bishop JM, Therond PP (1997) Hedgehog elicits signal transduction by means of a large complex containing the kinesin-related protein Costal2. Cell 90:225–234PubMedGoogle Scholar
  23. Rodriguez-Esteban C, Tsukui T, Yonei S, Magallon J, Tamura K, Izpisua-Belmonte JC (1999) The T-box genes Tbx4 and Tbx5 regulate limb outgrowth and identity. Nature 398:814–818PubMedGoogle Scholar
  24. Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y., pp 8.84Google Scholar
  25. Sisson JC, Ho KS, Suyama K, Scott MP (1997) Costal2, a novel kinesin-related protein in the Hedgehog signaling pathway. Cell 90:235–245PubMedGoogle Scholar
  26. Stanford WL, Cohn JB, Cordes SP (2001) Gene-trap mutagenesis: past, present and beyond. Nat Rev Genet 2:756–768CrossRefPubMedGoogle Scholar
  27. Vale RD (2003) The molecular motor toolbox for intracellular transport. Cell 112:467–480PubMedGoogle Scholar
  28. von Melchner H, Reddy S, Ruley HE (1990) Isolation of cellular promoters by using a retrovirus promoter trap. Proc Natl Acad Sci USA 87:3733–3737PubMedGoogle Scholar
  29. Wang G, Amanai K, Wang B, Jiang J (2000) Interactions with Costal2 and Suppressor of fused regulate nuclear translocation and activity of Cubitus interruptus. Genes Dev 14:2893-2905CrossRefPubMedGoogle Scholar
  30. Waterston RH, Lindblad-Toh K, Birney E, Rogers J, Abril JF, Agarwal P, Ainscough R, Alexandersson M, An P, Antonarakis SE, et al (2002) Initial sequencing and comparative analysis of the mouse genome. Nature 420:520–562CrossRefPubMedGoogle Scholar
  31. Wilkinson DG, Nieto MA (1993) Detection of messenger RNA by in situ hybridization to tissue sections and whole mounts. Methods Enzymol 225:361–373PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • Yusuke Marikawa
    • 1
  • Toko C. Fujita
    • 1
  • Vernadeth B. Alarcón
    • 1
  1. 1.Institute for Biogenesis Research, Department of Anatomy and Reproductive Biology, John A. Burns School of MedicineUniversity of HawaiiHonoluluUSA

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