Reduction of microtubule catastrophe events by LIS1, platelet-activating factor acetylhydrolase subunit (original) (raw)

Abstract

Forming the structure of the human brain involves extensive neuronal migration, a process dependent on cytoskeletal rearrangement. Neuronal migration is believed to be disrupted in patients exhibiting the developmental brain malformation lissencephaly. Previous studies have shown that LIS1, the defective gene found in patients with lissencephaly, is a subunit of the platelet-activating factor acetylhydrolase. Our results indicated that LIS1 has an additional function. By interacting with tubulin it suppresses microtubule dynamics. We detected LIS1 interaction with microtubules by immunostaining and co-assembly. LIS1-tubulin interactions were assayed by co-immunoprecipitation and by surface plasmon resonance changes. Microtubule dynamic measurements in vitro indicated that physiological concentrations of LIS1 indeed reduced microtubule catastrophe events, thereby resulting in a net increase in the maximum length of the microtubules. Furthermore, the LIS1 protein concentration in the brain, measured by quantitative Western blots, is high and is approximately one-fifth of the concentration of brain tubulin. Our new findings show that LIS1 is a protein exhibiting several cellular interactions, and the interaction with the cytoskeleton may prove to be the mode of transducing a signal generated by platelet-activating factor. We postulate that the LIS1-cytoskeletal interaction is important for neuronal migration, a process that is defective in lissencephaly patients.

Full Text

The Full Text of this article is available as a PDF (358.4 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Albrecht U., Abu-Issa R., Rätz B., Hattori M., Aoki J., Arai H., Inoue K., Eichele G. Platelet-activating factor acetylhydrolase expression and activity suggest a link between neuronal migration and platelet-activating factor. Dev Biol. 1996 Dec 15;180(2):579–593. doi: 10.1006/dbio.1996.0330. [DOI] [PubMed] [Google Scholar]
  2. Avila J. Microtubule functions. Life Sci. 1992;50(5):327–334. doi: 10.1016/0024-3205(92)90433-p. [DOI] [PubMed] [Google Scholar]
  3. Barth P. G. Disorders of neuronal migration. Can J Neurol Sci. 1987 Feb;14(1):1–16. doi: 10.1017/s031716710002610x. [DOI] [PubMed] [Google Scholar]
  4. Bazan N. G., Allan G., Rodriguez de Turco E. B. Role of phospholipase A2 and membrane-derived lipid second messengers in membrane function and transcriptional activation of genes: implications in cerebral ischemia and neuronal excitability. Prog Brain Res. 1993;96:247–257. doi: 10.1016/s0079-6123(08)63271-9. [DOI] [PubMed] [Google Scholar]
  5. Belmont L. D., Mitchison T. J. Identification of a protein that interacts with tubulin dimers and increases the catastrophe rate of microtubules. Cell. 1996 Feb 23;84(4):623–631. doi: 10.1016/s0092-8674(00)81037-5. [DOI] [PubMed] [Google Scholar]
  6. Bito H., Nakamura M., Honda Z., Izumi T., Iwatsubo T., Seyama Y., Ogura A., Kudo Y., Shimizu T. Platelet-activating factor (PAF) receptor in rat brain: PAF mobilizes intracellular Ca2+ in hippocampal neurons. Neuron. 1992 Aug;9(2):285–294. doi: 10.1016/0896-6273(92)90167-c. [DOI] [PubMed] [Google Scholar]
  7. Bré M. H., Karsenti E. Effects of brain microtubule-associated proteins on microtubule dynamics and the nucleating activity of centrosomes. Cell Motil Cytoskeleton. 1990;15(2):88–98. doi: 10.1002/cm.970150205. [DOI] [PubMed] [Google Scholar]
  8. Carminati J. L., Stearns T. Microtubules orient the mitotic spindle in yeast through dynein-dependent interactions with the cell cortex. J Cell Biol. 1997 Aug 11;138(3):629–641. doi: 10.1083/jcb.138.3.629. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cleveland D. W., Hwo S. Y., Kirschner M. W. Physical and chemical properties of purified tau factor and the role of tau in microtubule assembly. J Mol Biol. 1977 Oct 25;116(2):227–247. doi: 10.1016/0022-2836(77)90214-5. [DOI] [PubMed] [Google Scholar]
  10. Cleveland D. W., Hwo S. Y., Kirschner M. W. Purification of tau, a microtubule-associated protein that induces assembly of microtubules from purified tubulin. J Mol Biol. 1977 Oct 25;116(2):207–225. doi: 10.1016/0022-2836(77)90213-3. [DOI] [PubMed] [Google Scholar]
  11. Condeelis J. Elongation factor 1 alpha, translation and the cytoskeleton. Trends Biochem Sci. 1995 May;20(5):169–170. doi: 10.1016/s0968-0004(00)88998-7. [DOI] [PubMed] [Google Scholar]
  12. Drubin D., Kobayashi S., Kellogg D., Kirschner M. Regulation of microtubule protein levels during cellular morphogenesis in nerve growth factor-treated PC12 cells. J Cell Biol. 1988 May;106(5):1583–1591. doi: 10.1083/jcb.106.5.1583. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Edelmann W., Zervas M., Costello P., Roback L., Fischer I., Hammarback J. A., Cowan N., Davies P., Wainer B., Kucherlapati R. Neuronal abnormalities in microtubule-associated protein 1B mutant mice. Proc Natl Acad Sci U S A. 1996 Feb 6;93(3):1270–1275. doi: 10.1073/pnas.93.3.1270. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Fygenson DK, Braun E, Libchaber A. Phase diagram of microtubules. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics. 1994 Aug;50(2):1579–1588. doi: 10.1103/physreve.50.1579. [DOI] [PubMed] [Google Scholar]
  15. Fägerstam L. G., Frostell-Karlsson A., Karlsson R., Persson B., Rönnberg I. Biospecific interaction analysis using surface plasmon resonance detection applied to kinetic, binding site and concentration analysis. J Chromatogr. 1992 Apr 24;597(1-2):397–410. doi: 10.1016/0021-9673(92)80137-j. [DOI] [PubMed] [Google Scholar]
  16. Garcia-Higuera I., Fenoglio J., Li Y., Lewis C., Panchenko M. P., Reiner O., Smith T. F., Neer E. J. Folding of proteins with WD-repeats: comparison of six members of the WD-repeat superfamily to the G protein beta subunit. Biochemistry. 1996 Nov 5;35(44):13985–13994. doi: 10.1021/bi9612879. [DOI] [PubMed] [Google Scholar]
  17. Geiser J. R., Schott E. J., Kingsbury T. J., Cole N. B., Totis L. J., Bhattacharyya G., He L., Hoyt M. A. Saccharomyces cerevisiae genes required in the absence of the CIN8-encoded spindle motor act in functionally diverse mitotic pathways. Mol Biol Cell. 1997 Jun;8(6):1035–1050. doi: 10.1091/mbc.8.6.1035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Gordon-Weeks P. R. Control of microtubule assembly in growth cones. J Cell Sci Suppl. 1991;15:45–49. doi: 10.1242/jcs.1991.supplement_15.7. [DOI] [PubMed] [Google Scholar]
  19. Hanahan D. J. Platelet activating factor: a biologically active phosphoglyceride. Annu Rev Biochem. 1986;55:483–509. doi: 10.1146/annurev.bi.55.070186.002411. [DOI] [PubMed] [Google Scholar]
  20. Harada A., Oguchi K., Okabe S., Kuno J., Terada S., Ohshima T., Sato-Yoshitake R., Takei Y., Noda T., Hirokawa N. Altered microtubule organization in small-calibre axons of mice lacking tau protein. Nature. 1994 Jun 9;369(6480):488–491. doi: 10.1038/369488a0. [DOI] [PubMed] [Google Scholar]
  21. Hatta S., Ozawa H., Saito T., Ohshika H. Participation of tubulin in the stimulatory regulation of adenylyl cyclase in rat cerebral cortex membranes. J Neurochem. 1995 Mar;64(3):1343–1350. doi: 10.1046/j.1471-4159.1995.64031343.x. [DOI] [PubMed] [Google Scholar]
  22. Hattori M., Adachi H., Tsujimoto M., Arai H., Inoue K. Miller-Dieker lissencephaly gene encodes a subunit of brain platelet-activating factor acetylhydrolase [corrected]. Nature. 1994 Jul 21;370(6486):216–218. doi: 10.1038/370216a0. [DOI] [PubMed] [Google Scholar]
  23. Ho Y. S., Swenson L., Derewenda U., Serre L., Wei Y., Dauter Z., Hattori M., Adachi T., Aoki J., Arai H. Brain acetylhydrolase that inactivates platelet-activating factor is a G-protein-like trimer. Nature. 1997 Jan 2;385(6611):89–93. doi: 10.1038/385089a0. [DOI] [PubMed] [Google Scholar]
  24. Horio T., Hotani H. Visualization of the dynamic instability of individual microtubules by dark-field microscopy. Nature. 1986 Jun 5;321(6070):605–607. doi: 10.1038/321605a0. [DOI] [PubMed] [Google Scholar]
  25. Huttenlocher A., Sandborg R. R., Horwitz A. F. Adhesion in cell migration. Curr Opin Cell Biol. 1995 Oct;7(5):697–706. doi: 10.1016/0955-0674(95)80112-x. [DOI] [PubMed] [Google Scholar]
  26. Kapeller R., Chakrabarti R., Cantley L., Fay F., Corvera S. Internalization of activated platelet-derived growth factor receptor-phosphatidylinositol-3' kinase complexes: potential interactions with the microtubule cytoskeleton. Mol Cell Biol. 1993 Oct;13(10):6052–6063. doi: 10.1128/mcb.13.10.6052. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Kato K., Clark G. D., Bazan N. G., Zorumski C. F. Platelet-activating factor as a potential retrograde messenger in CA1 hippocampal long-term potentiation. Nature. 1994 Jan 13;367(6459):175–179. doi: 10.1038/367175a0. [DOI] [PubMed] [Google Scholar]
  28. Kiley S. C., Parker P. J. Differential localization of protein kinase C isozymes in U937 cells: evidence for distinct isozyme functions during monocyte differentiation. J Cell Sci. 1995 Mar;108(Pt 3):1003–1016. doi: 10.1242/jcs.108.3.1003. [DOI] [PubMed] [Google Scholar]
  29. Kornecki E., Ehrlich Y. H. Neuroregulatory and neuropathological actions of the ether-phospholipid platelet-activating factor. Science. 1988 Jun 24;240(4860):1792–1794. doi: 10.1126/science.3381103. [DOI] [PubMed] [Google Scholar]
  30. Lehrich R. W., Forrest J. N., Jr Protein kinase C zeta is associated with the mitotic apparatus in primary cell cultures of the shark rectal gland. J Biol Chem. 1994 Dec 23;269(51):32446–32450. [PubMed] [Google Scholar]
  31. Letourneau P. C., Ressler A. H. Inhibition of neurite initiation and growth by taxol. J Cell Biol. 1984 Apr;98(4):1355–1362. doi: 10.1083/jcb.98.4.1355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Lo Nigro C., Chong C. S., Smith A. C., Dobyns W. B., Carrozzo R., Ledbetter D. H. Point mutations and an intragenic deletion in LIS1, the lissencephaly causative gene in isolated lissencephaly sequence and Miller-Dieker syndrome. Hum Mol Genet. 1997 Feb;6(2):157–164. doi: 10.1093/hmg/6.2.157. [DOI] [PubMed] [Google Scholar]
  33. Maccioni R. B., Cambiazo V. Role of microtubule-associated proteins in the control of microtubule assembly. Physiol Rev. 1995 Oct;75(4):835–864. doi: 10.1152/physrev.1995.75.4.835. [DOI] [PubMed] [Google Scholar]
  34. Malmqvist M. Biospecific interaction analysis using biosensor technology. Nature. 1993 Jan 14;361(6408):186–187. doi: 10.1038/361186a0. [DOI] [PubMed] [Google Scholar]
  35. Mandelkow E., Mandelkow E. M. Microtubules and microtubule-associated proteins. Curr Opin Cell Biol. 1995 Feb;7(1):72–81. doi: 10.1016/0955-0674(95)80047-6. [DOI] [PubMed] [Google Scholar]
  36. Mitchison T., Kirschner M. Dynamic instability of microtubule growth. Nature. 1984 Nov 15;312(5991):237–242. doi: 10.1038/312237a0. [DOI] [PubMed] [Google Scholar]
  37. Mitchison T., Kirschner M. Microtubule assembly nucleated by isolated centrosomes. Nature. 1984 Nov 15;312(5991):232–237. doi: 10.1038/312232a0. [DOI] [PubMed] [Google Scholar]
  38. Mizuguchi M., Takashima S., Kakita A., Yamada M., Ikeda K. Lissencephaly gene product. Localization in the central nervous system and loss of immunoreactivity in Miller-Dieker syndrome. Am J Pathol. 1995 Oct;147(4):1142–1151. [PMC free article] [PubMed] [Google Scholar]
  39. Neer E. J., Schmidt C. J., Nambudripad R., Smith T. F. The ancient regulatory-protein family of WD-repeat proteins. Nature. 1994 Sep 22;371(6495):297–300. doi: 10.1038/371297a0. [DOI] [PubMed] [Google Scholar]
  40. Panda D., Goode B. L., Feinstein S. C., Wilson L. Kinetic stabilization of microtubule dynamics at steady state by tau and microtubule-binding domains of tau. Biochemistry. 1995 Sep 5;34(35):11117–11127. doi: 10.1021/bi00035a017. [DOI] [PubMed] [Google Scholar]
  41. Raghavan M., Bjorkman P. J. BIAcore: a microchip-based system for analyzing the formation of macromolecular complexes. Structure. 1995 Apr 15;3(4):331–333. doi: 10.1016/s0969-2126(01)00164-2. [DOI] [PubMed] [Google Scholar]
  42. Rakic P., Cameron R. S., Komuro H. Recognition, adhesion, transmembrane signaling and cell motility in guided neuronal migration. Curr Opin Neurobiol. 1994 Feb;4(1):63–69. doi: 10.1016/0959-4388(94)90033-7. [DOI] [PubMed] [Google Scholar]
  43. Reiner O., Albrecht U., Gordon M., Chianese K. A., Wong C., Gal-Gerber O., Sapir T., Siracusa L. D., Buchberg A. M., Caskey C. T. Lissencephaly gene (LIS1) expression in the CNS suggests a role in neuronal migration. J Neurosci. 1995 May;15(5 Pt 2):3730–3738. doi: 10.1523/JNEUROSCI.15-05-03730.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Reiner O., Carrozzo R., Shen Y., Wehnert M., Faustinella F., Dobyns W. B., Caskey C. T., Ledbetter D. H. Isolation of a Miller-Dieker lissencephaly gene containing G protein beta-subunit-like repeats. Nature. 1993 Aug 19;364(6439):717–721. doi: 10.1038/364717a0. [DOI] [PubMed] [Google Scholar]
  45. Reszka A. A., Seger R., Diltz C. D., Krebs E. G., Fischer E. H. Association of mitogen-activated protein kinase with the microtubule cytoskeleton. Proc Natl Acad Sci U S A. 1995 Sep 12;92(19):8881–8885. doi: 10.1073/pnas.92.19.8881. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Roychowdhury S., Rasenick M. M. Tubulin-G protein association stabilizes GTP binding and activates GTPase: cytoskeletal participation in neuronal signal transduction. Biochemistry. 1994 Aug 16;33(32):9800–9805. doi: 10.1021/bi00198a052. [DOI] [PubMed] [Google Scholar]
  47. Schwarz A., Futerman A. H. The localization of gangliosides in neurons of the central nervous system: the use of anti-ganglioside antibodies. Biochim Biophys Acta. 1996 Oct 29;1286(3):247–267. doi: 10.1016/s0304-4157(96)00011-1. [DOI] [PubMed] [Google Scholar]
  48. Shiina N., Gotoh Y., Kubomura N., Iwamatsu A., Nishida E. Microtubule severing by elongation factor 1 alpha. Science. 1994 Oct 14;266(5183):282–285. doi: 10.1126/science.7939665. [DOI] [PubMed] [Google Scholar]
  49. Tanaka E., Sabry J. Making the connection: cytoskeletal rearrangements during growth cone guidance. Cell. 1995 Oct 20;83(2):171–176. doi: 10.1016/0092-8674(95)90158-2. [DOI] [PubMed] [Google Scholar]
  50. Vallee R. B. Reversible assembly purification of microtubules without assembly-promoting agents and further purification of tubulin, microtubule-associated proteins, and MAP fragments. Methods Enzymol. 1986;134:89–104. doi: 10.1016/0076-6879(86)34078-3. [DOI] [PubMed] [Google Scholar]
  51. Walker R. A., O'Brien E. T., Pryer N. K., Soboeiro M. F., Voter W. A., Erickson H. P., Salmon E. D. Dynamic instability of individual microtubules analyzed by video light microscopy: rate constants and transition frequencies. J Cell Biol. 1988 Oct;107(4):1437–1448. doi: 10.1083/jcb.107.4.1437. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Wang N., Yan K., Rasenick M. M. Tubulin binds specifically to the signal-transducing proteins, Gs alpha and Gi alpha 1. J Biol Chem. 1990 Jan 25;265(3):1239–1242. [PubMed] [Google Scholar]
  53. Willins D. A., Xiang X., Morris N. R. An alpha tubulin mutation suppresses nuclear migration mutations in Aspergillus nidulans. Genetics. 1995 Dec;141(4):1287–1298. doi: 10.1093/genetics/141.4.1287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Xiang X., Osmani A. H., Osmani S. A., Xin M., Morris N. R. NudF, a nuclear migration gene in Aspergillus nidulans, is similar to the human LIS-1 gene required for neuronal migration. Mol Biol Cell. 1995 Mar;6(3):297–310. doi: 10.1091/mbc.6.3.297. [DOI] [PMC free article] [PubMed] [Google Scholar]