Division of Life Science
 
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Andrew L. MILLER

PhD Dundee
Professor

Email: almiller@ust.hk

Homepage of Dr. Miller's research lab

Research Interests
Investigating the role played by calcium ions in the signal transduction pathways orchestrating embryonic development.

Calcium signaling is studied through the use of aequorins, a group of bioluminescent proteins. They can either be microinjected or transfected into cells, without disturbing function or development. The pattern of luminescence that is emitted by an aequorin-loaded cell, tissue or embryo, reveals changing patterns and levels of free calcium. Dr Miller is currently studying the role of calcium signaling in fertilization, segregation, cytokinesis, gastrulation and segmentation in zebrafish, and in neural induction in Xenopus. His work also focuses on exploring the calcium-sensitive target elements interacting with both intracellular and intercellular calcium signals - such as cytoskeletal components, morphogenic protein secretions, and localized developmental gene expression via calcium-sensitive transcription factors. A second area of interest is to elucidate the structures and mechanisms of activation of receptor-activated calcium channels in the plasma membrane of non-excitable animal cells. This is being done by targeting aequorins to specific compartments and locations within cells. A third area of research is the development of microscopy and image processing techniques required to collect and visualize ultra-low levels of photon emission from living cells and embryos.

Representative Publications

  1. Kelu, J.J., Webb, S.E., Parrington, J., Galione, A. and Miller, A.L. (2017). Ca2+ release via two-pore channel type 2 (TPC2) is required for slow muscle cell myofibrillogenesis and myotomal patterning in intact zebrafish embryos. Dev. Biol. 425:109-129.

  2. Li W.M., Chan, C.M., Miller, A.L. and Lee, C.H. (2017). Dual functional roles of molecular beacon: a microRNA detector and inhibitor. J. Biol. Chem. Doi: 10.1074/jbc.M116.765776.

  3. Webb, S.E. and Miller, A.L. (2017). Ca2+ signalling and membrane dynamics during cytokinesis in animal cells. Invited Chapter for: Membrane Dynamics and Ca2+ Signalling (Springer) - submitted.

  4. Hao, B., Wei, W., Webb, S.E., Miller, A.L., and Yue, J. (2017). The role of Ca2+ signaling in the differentiation of embryonic stem cells (ESCs) into cardiomyocytes. Frontiers in Stem Cell and Regenerative Medicine Research Vol 4. Doi: 10.2174/97816810843501170401.

  5. Chan, C.M., Aw, J.T.M., Webb, S.E., Miller, A.L. (2016). SOCE proteins, STIM1 and Orai1, are localized to the cleavage furrow during cytokinesis of the first and second cell division cycles in zebrafish embryos. Zygote 24:880-889.

  6. Chan, H.Y.S., Cheung, M.C., Gao, Y., Miller, A.L., and Webb, S.E. (2016). Expression and reconstitution of the bioluminescent Ca2+ reporter aequorin in human embryonic stem cells, and exploration of the presence of functional IP3 and ryanodine receptors during the early stages of their differentiation into cardiomyocytes. SCIENCE CHINA Life Sciences doi: 10.1007/s11427-016-5094-6.

  7. Leclerc, C., Haeich, J., Aulestia, F.J., Kilhoffer, M.-C., Miller, A.L., Néant, I., Webb, S.E., Schaeffer, E., Junier, M.-P., Chneiweiss, H., and Moreau, M. (2016). Calcium signaling orchestrates glioblastoma development: Facts and conjectures. Biochim. Biophys. Acta Mol. Cell Res. 1863: 1447-1459.

  8. Hao, B., Webb, S.E., Miller, A.L., and Yue, J. (2016). The role of Ca2+ signaling on the self-renewal and neural differentiation of embryonic stem cells (ESCs). Cell Calcium 59: 67-74.

  9. Chan, C.M., Chen, Y., Hung, T.S., Miller, A.L. and Webb, S.E. (2015). Inhibition of SOCE disrupts cytokinesis in zebrafish embryos via inhibition of cleavage furrow deepening. Int. J. Dev. Biol. 59: 289-301.

  10. Kelu, J.K., Chan, H.L.H., Webb, S.E., Cheng, A.H.H., Ruas, M., Parrington, J., Galione A., and Miller, A.L. (2015). Two-pore channel 2 activity is required for slow muscle cell-generated Ca2+ signaling during myogenesis in intact zebrafish. Int. J. Dev. Biol. 59: 313-325.

  11. Moreau, M., Néant, I., Webb, S.E., Miller, A.L., Riou, J.-F., Leclerc, C. (2015). Ca2+ coding and decoding strategies for the specification or neural and renal precursor cells during development. Cell Calcium. 59: 75-83.

  12. Chan, H.Y.S., Keung, W., Li, R.A., Miller, A.L. and Webb, S.E. (2015) Morphometric analysis of human embryonic stem cell-derived ventricular cardiomyocytes: Determining the maturation state of a population by quantifying parameters in individual cells. Stem Cells Int. Article ID 586908, 13 pages, doi:10.1155/2015/586908.

  13. Barnes, M., van Rensburg, G., Li, W.-M., Mehmood, K., Mackedenski, S., Chan, C.-M., King, D.T., Miller, A.L. and Lee, C.H. (2015) Molecular insights into the coding region determinant-binding protein-RNA interaction through site-directed mutagenesis in the heterogeneous nuclear ribonucleoprotein-K-homology domains. J. Biol. Chem. 290:625-639.

  14. Webb, S.E., Goulet, C., Chan, C.M., Yuen, Y.F., and Miller, A.L. (2014). Biphasic assembly of the contractile apparatus during the first two cell division cycles in zebrafish embryos. Zygote. 22:218-228.

  15. Webb, S.E., Karplus, E. and Miller A.L. (2014). Retrospective on the development of aequorin and aequorin-based imaging to visualize changes in intracellular free [Ca2+]. Mol. Reprod. Devel. DOI 10.1002/mrd.22298.

  16. Webb, S.E., and Miller A.L. (2013). Calcium signaling in extra-embryonic domains during early teleost development. International Review of Cell and Molecular Biology.304:369-418.

  17. Yuen, Y.F., Webb, S.E., Chan, C.M., Thisse, B., Thisse, C and Miller, A.L. (2013). Characterization of Ca2+ signaling in the external yolk syncytial layer during the late blastula and early gastrula periods of zebrafish development. Biochim. Biophys. Acta 1833: 1641-1656.

  18. Webb, S.E., Chan C.M. and Miller A.L. (2013). Introduction of aequorin into zebrafish embryos for recording Ca2+ signaling during the first 48 h of development. Cold Spring Harb. Protoc. doi:10.1101/pdb.top066316.

  19. Webb, S.E. and Miller, A.L. (2013). Microinjecting holo-aequorin into dechorionated and intact zebrafish embryos. Cold Spring Harb. Protoc. doi:10.1101/pdb.prot072967.

  20. Chan, C.M., Miller, A.L. and Webb, S.E. (2013). Reconstitution of holo-aequorin with apoaequorin mRNA and coelenterazine in zebrafish embryos. Cold Spring Harb. Protoc. doi:10.1101/pdb.prot072975

  21. Webb, S.E., and Miller, A.L. (2012). Ca2+ signaling during activation and fertilization in the eggs of teleost fish. Cell Calcium. 53: 24-31.

  22. Webb, S.E., and Miller, A.L. (2012). Aequorin-based genetic approaches to visualize Ca2+ signaling in developing animal systems. Biochim. Biophys. Acta 1820: 1160-1168.

  23. Webb, S.E., Cheung, C.Y., Chan C.M., Love, D.R. and Miller, A.L. (2012). Application of complementary luminescent and fluorescent imaging techniques to visualize nuclear and cytoplasmic Ca2+ signaling during the in vivo differentiation of slow muscle cells in zebrafish embryos under normal and dystrophic conditions. Clin. Expt. Pharm. Physiol. 39: 78-86.

  24. Webb, S.E., Cheung, C.Y., Love, D., and Miller, A.L. (2011). The application of complementary luminescent and fluorescent imaging techniques to visualize nuclear and cytoplasmic Ca2+-signaling during the in vivo differentiation of slow muscle cells in zebrafish embryos under normal and dystrophic conditions. Proceedings of the Australian Physiological Society 42: 29-40.

  25. Zhang, J., Webb, S.E. Ma, L.H., Chan, C.M. & Miller, A.L. (2011). Necessary role for intracellular Ca2+ transients in initiating the apical-basolateral thinning of enveloping layer cells during the early blastula period of zebrafish development. Dev. Growth Diff. 53:679-696.

  26. Cheung, C.Y., Webb, S.E., Love, D.R. & Miller, A.L. (2011). Visualization, characterization and modulation of Calcium signaling during the development of slow muscle cells in intact zebrafish embryos. Int.J.Dev.Biol. 55:153-174.

  27. Mei, W., Marlow, F., Lee, K.W., Miller, A.L., and Mullins, M.C. (2009). hnRNP I/brom bones is required for calcium-mediated egg activation in the zebrafish. Development  136:3007-3017.

  28. Leung, C.F., Miller, A.L., Korzh, V. and Webb, S.E. (2009). Visualization of stochastic Ca2+ signals in the formed somites during the early Segmentation Period in intact, normally developing zebrafish embryos. Dev Growth Differ. 51:617-637.

  29. Ma, O., Webb, S.E., Chan, C.M., Zhang, J. and Miller, A.L. (2009). Establishment of a transitory dorsal-biased window of localized Ca2+ signaling in the superficial epithelium following the mid-blastula transition in zebrafish embryos Dev. Biol. 327: 143-157.

  30. Lam, P.Y., Webb, S.E., Leclerc, C., Moreau, M. and Miller, A.L. (2009). Inhibition of stored Ca2+ release disrupts convergence-related cell movements in the lateral intermediate mesoderm resulting in abnormal positioning and morphology of the pronephric anlagen in intact zebrafish embryos. Dev. Growth Differ. 51: 429-442.

  31. Moreau, M., Webb, S.E., Neant, I., Miller, A.L. and Leclerc, C. (2009). Calcium signaling and cell fate determination during neural induction in amphibian embryos. Handbook of Neurochem. Mol. Neurobiol (Ed. K. Mikoshiba). Ch. 1 pp. 3-13. Springer Science+Business Media, LLC.

  32. Leclerc, C., Webb, S.E., Miller, A.L. and Moreau, M. (2008). An increase in intracellular Ca2+ is involved in pronephric tubule differentiation in the amphibian Xenopus laevis. Dev. Biol. 321: 357-367.

  33. Li, W.M., Webb, S.E., Chan, C.M. and Miller, A.L. (2008). Multiple roles of the furrow deepening Ca2+ transient during cytokinesis in zebrafish embryos. Dev. Biol. 316: 228-248.

  34. Webb, S.E., Li, W.M. and Miller, A.L. (2008). Calcium signalling during the cleavage period of zebrafish development. Phil. Trans. R. Soc. B 363: 1363-1369.

  35. Moreau, M., Neant, I., Webb, S.E., Miller, A.L. and Leclerc, C. (2008). Calcium signalling during neural induction in Xenopus laevis embryos. Phil. Trans. R. Soc. B 363: 1371-1375.

  36. Webb, S.E. and Miller, A.L. (2007). Ca2+ signaling during embryonic cytokinesis in animal systems. In: New Comprehensive Biochemistry vol 41: Calcium. A Matter of Life or Death. (Eds, J. Krebs, & M. Michalak). Elsevier. Ch 17. pp. 445-470.

  37. Webb, S.E. and Miller, A.L. (2007). Ca2+ signaling and early embryonic patterning during zebrafish development. Proc. Aus. Physiol. Soc. 38: 43-51.

  38. Webb, S.E. and Miller, A.L. (2006). Ca2+ signaling and early embryonic patterning during the Blastula and Gastrula Periods of Zebrafish and Xenopus development. Biochim. Biophys. Acta 1763: 1192-1208.

  39. Leclerc, C., Neant, I., Webb, S.E., Miller, A.L. and Moreau, M. (2006). Calcium transients and calcium signalling during early neurogenesis in the amphibian embryo Xenopus laevis. Biochim. Biophys. Acta 1763: 1184-1191.

  40. Montaville, P., Dai, Y., Cheung, C.Y., Giller, K., Becker, S., Michalak, M., Webb, S.E., Miller, A.L. and Krebs, J. (2006). Nuclear translocation of the calcium-binding protein ALG-2 induced by the RNA-binding protein RBM22. Biochim. Biophys. Acta 1763: 1335-1343.

  41. Li, W.M., Webb, S.E., Lee, K.W. and Miller, A.L. (2006). Recruitment and SNARE-mediated fusion of vesicles in furrow membrane remodeling during cytokinesis in zebrafish embryos. Exp. Cell. Res. 312: 3260-3275.

  42. Webb, S.E. and Miller, A.L. (2006). Ca2+ signaling during vertebrate somitogenesis. Acta Pharmacol. Sinica. 27:781-790.

  43. Cheung, Y.C., Webb, S.E., and Miller, A.L. (2006). Transient expression of apoaequorin in zebrafish embryos: extending the ability to image calcium transients during later states of development. Int. J. Dev. Biol. 50:561-569.

  44. Lee, K.W., Webb, S.E. and Miller A.L. (2006). Requirement for a localized IP3R generated Ca2+ transient during the furrow positioning process in zebrafish zygotes. Zygote 14:143-155.

  45. Dodd, A., Greenwood, D.R., Miller, A.L. Webb, S.E., Chambers, S.P., Copp, B.R. and Love, D.R. (2006). Zebrafish: At the nexus of functional and chemical genomics. Biotech. Gen. Eng. Rev. 22:77-99.

  46. Webb, S.E., Moreau, M., Leclerc, C. and Miller, A.L. (2005). Calcium transients and neural induction in vertebrates. Cell Calcium. 37: 375-385.

  47. Lee, K.W., Ho, S.M., Wong, C.H., Webb, S.E. and Miller, A.L. (2004) Characterization of Mid-Spindle Microtubules during Furrow Positioning in Early Cleavage Period Zebrafish Embryos. Zygote 12: 221-230.

  48. Cheng, J.C., Miller, A.L., and Webb, S.E. (2004). Organisation and function of microfilaments during late epiboly in zebrafish embryos. Developmental Dynamics 231: 313-323.

  49. Chan, C., Harland, M.L., Webb, S.E., Miller, A.L. and Barritt, G.J. (2004). Evidence that Ca2+ inflow through liver cell store-operated Ca2+ channels does not require the thapsigargin-sensitive endoplasmic reticulum (Ca2+ + Mg2+)ATP-ase. Cell Calcium 35: 317-331.

  50. Lee, K.W., Webb, S.E., and Miller, A.L. (2003). Ca2+ released via IP3 receptors is required for furrow deepening during cytokinesis in zebrafish embryos. Int. J. Dev. Biol. 47: 411-421.

  51. Leclerc, C., Lee, M., Webb, S.E., Moreau, M., and Miller, A.L. (2003). Calcium transients triggered by planar signals induce the expression of Zic3 during neural induction in Xenopus. Developmental Biology 261(2): 381-390.

  52. Webb, S.E., and Miller, A.L. (2003). Calcium signalling during embryonic development. Nature Reviews Molecular Cell Biology 4: 539-551.

  53. Webb, S.E., and Miller, A.L. (2003). Imaging intercellular calcium waves during late epiboly in intact zebrafish embryos. Zygote 11(2): 175-182.

  54. Webb, S.E., Moreau, M., Leclerc, C. and Miller, A.L. (2001) Calcium in development: from ion transients to gene expression. Bioessays 23(4):372-374.

  55. Leclerc, C., Webb, S.E., Daguzan, C., Moreau, M. and Miller, A.L. (2000) Imaging patterns of calcium transients during neural induction in Xenopus laevis embryos. J. Cell Sci. 113:3519-3529.

  56. Webb, S.E. and Miller, A.L. (2000) Calcium signalling during zebrafish embryonic development. Bioessays 22(2):113-123.

  57. Leung, C.F., Webb, S.E. and Miller, A.L. (2000) On the mechanism of ooplasmic segregation in single-cell zebrafish embryos. Dev. Growth & Diff. 42:29-40.

  58. Fluck, R.A., Abraham, V., Miller, A.L. and Galione, A. (1999) Microinjection of cyclic ADP-ribose triggers a wave of Ca2+ release and exocytosis of cortical alveoli in medaka eggs. Zygote 7:285-292.

  59. Lee, K.W., Webb, S.E. and Miller, A.L. (1999) A wave of free cytosolic calcium traverses zebrafish eggs on activation. Dev. Biol. 214:168-180.

  60. Gilland, E., Miller, A.L., Karplus, E., Baker, R. and Webb, S.E. (1999) Imaging of multicellular large-scale rhythmic calcium waves during zebrafish gastrulation. P.N.A.S. 96:157-161.

  61. Webb, S.E., Lee, K.W., Karplus, E. and Miller, A.L. (1997) Localized calcium transients accompany furrow positioning, propagation, and deepening during the early cleavage period of zebrafish embryos. Dev. Biol. 192:78-92.

  62. Eckberg, W.R. and Miller, A.L. (1995) Propagated and non-propagated calcium transients during egg activation in the annelid Chaetopterus. Dev. Biol. 172:654-664.

  63. Cubitt, A.B., Firtel, R.A., Fischer, G., Jaffe, L.F., Karplus, E. and Miller, A.L. (1995) Patterns of free calcium in developing Dictyostelium. Development 121:2291-2301.

  64. Miller, A.L. , Karplus, E. and Jaffe, L.F. (1994) Use of aequorin for [Ca2+]i imaging. Chapter 13. In: Methods in Cell Biology Volume 40: A Practical Guide to the Study of Ca2+ in Living Cells (ed. R. Nuccitelli), pp. 305-338. Academic Press.

  65. Miller, A.L. , Fluck, R.A., McLaughlin, J.A. and Jaffe, L.F. (1993) Calcium buffer injections inhibit cytokinesis in Xenopus eggs. J. Cell Science. 106:523-534.

  66. Fluck, R.A., Miller, A.L. and Jaffe, L.F. (1991) Slow calcium waves accompany cytokinesis in medaka fish eggs. J. Cell Biol. 115:1259-1265.

 

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