Cell Biology ~ Proteomics & Calcium Biology
Personnel
1. Our Biology
2. Our Research Technologies
3. Independent Publications
1. Our Biology
Cell Signalling
The mechanisms used to relay messages within cells are of intense biomedical interest. Complex signalling pathways underlie normal development and health of cells. Many diseases are associated with cell-signalling anomalies. Numerous drugs target the principal signalling effectors, calcium and protein phosphorylation.
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Calcium biology
Calcium has many roles inside and outside cells necessitating strict regulation at different concentrations in various locations. Calcium signals are transmitted through cells as transient increases of calcium which normally is kept at a very low concentration in the cytosol (cellular fluid). Cellular toxicity arises if these calcium elevations are too large or frequent (calcium cytotoxicity). It is clear that excess calcium can lead to cell death but disease-related disruptions of calcium signalling are not well understood.
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Dental enamel cells
We initiated investigations of calcium handling in enamel cells questioning how they make such a highly-calcified product (tooth enamel is 40% calcium) without suffering the cytotoxic effects of excess intracellular calcium. Of broader biomedical value, this research model comprises epithelial cells that have an informatively elongate morphology and undergo functionally-distinct phases of development linked to production of a hypermineralized extracellular matrix. Dentally, these cells are also central to the understanding of enamel mineralization and associated developmental defects; more information ![]()
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Current research focus
- calcium handling and avoidance of calcium cytotoxicity during mineralization of enamel
- cause, treatment and prevention of enamel defects, particularly idiopathic Molar Hypomineralisation
- function of calbindins (calcium-binding proteins) in health and disease
- role of ERp29 (a novel protein in the Endoplasmic Reticulum) in ER pathobiology
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2. Our Research Technologies
Molecular and cellular biology
We are using a broad range of experimental approaches from the DNA level (eg cDNA cloning, qPCR) through protein (eg 2-D gels, recombinant protein engineering), cellular (eg confocal and transmission electron microscopy) and physiological levels (eg knockout mouse characterisation).
Proteomics and protein biochemistry
Our speciality is microscale protein biochemistry, a challenging area necessitated by the scarcity of enamel cells. Approaches include mass spectrometry, Edman analysis, amino acid composition, gel electrophoresis and the purification, biophysical and functional analysis of proteins.
An online database (ToothPrint) of dental proteins in rat has been established.

Hard tissue microanalysis
We phenotypically characterise mouse and rat teeth using a variety of approaches including polarised light and scanning electron microscopy, histology, micro-CT and microradiography, microhardness and quantitative fracture analysis.
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3. Independent Publications
A. Enamel cell biology – how is bulk calcium handled safely?
Calcium plays numerous key roles in cells from their birth through to their death. Consequently there is much medical interest in manipulating calcium-dependent activities, for example to help keep damaged cells alive in neurodegenerative diseases or hastening the death of renegade cells in cancer. Enamel-forming cells hold interest in this regard as a calcium-savvy cell type that handles a lot of calcium (for mineralisation of dental enamel) without succumbing to the potentially cytotoxic effects of excessive intracellular calcium. To learn how enamel cells survive such a calcium onslaught, we developed microscale proteomic approaches and characterised enamel epithelial cells from developing teeth in neonatal rats and mice. This information was used to investigate the mechanistic basis of calcium transport across enamel cells. Our findings contradicted the classical "calcium ferry" dogma and led to development of a new paradigm for transcellular calcium transport that we've named "calcium transcytosis". Increasingly it appears this organelle-based mechanism could be more generally applicable across biology.
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Hubbard, M.J., McHugh, N.J. and Mangum, J.E. (2011) Exclusion of all three calbindins from a calcium-ferry role in rat enamel cells. Eur. J. Oral Sci. 119 (Suppl. 1), 112-119 (PMID: 22243236)
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Lacruz, R.S., Smith, C.E., Chen, Y., Hubbard, M.J., Hacia, J.G., and Paine, M.L. (2011) Gene expression analysis of early and late maturation stage rat enamel organ. Eur. J. Oral Sci. (119 (Suppl. 1), 149-157 (PMID: 21809343)
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Lacruz, R.S., Smith, C.E., Bringas, P., Chen, Y.B., Smith, S.M., Snead, M.L., Kurtz, I., Hacia, J.G., Hubbard, M.J. and Paine, M.L. (2012) Identification of novel candidate genes involved in mineralization of dental enamel by genome-wide transcript profiling. J. Cell Physiol. 227, 2264-2275 (PMID: 21809343)
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Mangum, J.E., Kon, J.C., Hubbard, M.J. (2010) Proteomic analysis of dental tissue microsamples. Methods Mol. Biol. 666, 309-325 (PMID: 20717792)
Mangum, J.E., Veith, P.D., Reynolds, E.C. and Hubbard, M.J. (2006) Towards second-generation proteome analysis of murine enamel-forming cells. Eur. J. Oral Sci. 114, 259-265 (PMID: 16674695) - Turnbull, C.I., Looi, K., Mangum, J.E., Meyer, M., Sayer, R.J. and Hubbard, M.J. (2004) Calbindin-independence of calcium transport in developing teeth contradicts the calcium-ferry dogma. J. Biol. Chem. 279, 55850-55854 (PMID: 15494408)
- Hubbard, M.J. and Kon, J.C. (2002) Proteomic analysis of dental tissues. J. Chromatogr. B, 771, 211-220 (PMID: 12016000)
- Franklin, I.K., Winz, R.A. and Hubbard, M.J. (2001) Endoplasmic reticulum Ca2+-ATPase pump is up-regulated in calcium-transporting dental enamel cells: A non-housekeeping role for SERCA2b. Biochem. J., 358, 217-224 (PMID: 11485570)
- Hubbard, M.J., Faught, M.J., Carlisle, B.H. and Stockwell, P.A. (2001) ToothPrint, a proteomic database for dental tissues. Proteomics 1, 132-135 (PMID: 11680893)
- Hubbard, M.J. (2000) Calcium transport across the dental enamel epithelium. Crit. Rev. Oral Biol. Med., 11, 437-466 (PMID: 11132765)
- Hubbard, M.J. (1998) Proteomic analysis of enamel cells from developing rat teeth. Big returns from a small tissue. Electrophoresis, 19, 1891-1900 (PMID: 9740049)
- Hubbard, M.J. (1998) Enamel cell biology. Towards a comprehensive biochemical understanding. Conn. Tissue Res., 39, 17-32 (PMID: 11063013)
- Hubbard, M.J. (1996) Abundant calcium homeostasis machinery in rat dental enamel cells. Up-regulation of calcium store proteins during enamel hypermineralization implicates the endoplasmic reticulum in calcium transcytosis. Eur. J. Biochem., 239, 611-623 (PMID: 877470)
- Hubbard, M.J. (1995) Calbindin28kDa and calmodulin are hyperabundant in rat dental enamel cells. Identification of the protein phosphatase calcineurin as a principal calmodulin target and of a secretion-related role for calbindin28kDa. Eur. J. Biochem., 230, 68-79 (PMID: 7601126)
B. Enamel defects - can they be prevented?
Developmental defects of enamel are costly to patients and society. Many of these dental defects may become preventable if a better understanding of their causes and pathologies can be gained. Recently we assembled a multidisciplinary team to investigate a common dental defect, termed Molar Hypomineralization, which manifests as soft, porous (chalky) enamel – this congenital defect affects 'six-year-old molars' in over 10% of otherwise healthy children, causing life-long risk of pain, dental caries and perhaps tooth loss in severe cases. Our initial proteomics investigation provided intriguing insights to the nature and possible cause of Molar Hypomineralization, and so suggests novel avenues for basic research and clinical development.
- Mangum, J.E., Crombie, F.A., Kilpatrick, N., Manton, D.J. and Hubbard, M.J. (2010) Surface integrity governs the proteome of hypomineralized enamel. J. Dent. Res. 89, 1160-1165 (PMID: 20651090)
C. Calbindins - what do they do?
Our cells contain numerous proteins thought to bind calcium as their primary role. Many of these calcium-binding proteins play pivotal roles in cell signalling, regulation and structure, making them attractive targets for therapeutic intervention in multiple diseases including cancer and neurodegeneration. However, for such applications to be fully effective, better understanding is needed about the functions of these calcium-binding proteins at individual and collective levels. Calbindins comprise three types of calcium-binding protein (calbindin-28kDa, calbindin-9kDa, calretinin) that have long been regarded as mobile calcium buffers in the cytosol and consequently are widely investigated as potential targets in calcium transport and neurodegeneration. Our investigations have contradicted this view and instead pointed to calbindins having a role that involves interactions with other proteins. These findings, which lead us to contemplate an alternative role in cell signalling, hold fundamental significance for medical targeting of calbindins.
- Hubbard, M.J., McHugh, N.J. and Mangum, J.E. (2011) Exclusion of all three calbindins from a calcium-ferry role in rat enamel cells. Eur. J. Oral Sci. 119 (Suppl. 1), 112-119 (PMID: 22243236)
- Turnbull, C.I., Looi, K., Mangum, J.E., Meyer, M., Sayer, R.J. and Hubbard, M.J. (2004) Calbindin-independence of calcium transport in developing teeth contradicts the calcium-ferry dogma. J. Biol. Chem. 279, 55850-55854 (PMID: 15494408)
- Sayer, R.J., Turnbull, C.I. and Hubbard, M.J. (2000) Calbindin28kDa is specifically associated with extra-nuclear constituents of the dense particulate fraction. Cell Tiss. Res., 302, 171-180 (PMID: 11131128)
- Hubbard, M.J. and McHugh, N.J. (1995) Calbindin28kDa and calbindin30kDa (calretinin) are substantially localised in the particulate fraction of rat brain. FEBS Lett., 374, 333-337 (PMID: 7589565)
- Hubbard, M.J. (1995) Calbindin28kDa and calmodulin are hyperabundant in rat dental enamel cells. Identification of the protein phosphatase calcineurin as a principal calmodulin target and of a secretion-related role for calbindin28kDa. Eur. J. Biochem., 230, 68-79 (PMID: 7601126)
- Hubbard, M.J. and Carne, A. (1994) Differential feeding-related regulation of ubiquitin and calbindin9kDa in rat duodenum. Biochim. Biophys. Acta, 1200, 191-6 (PMID: 8031840)
- Hubbard, M.J. (1993) Rapid purification and direct microassay of calbindin9kDa utilizing its solubility in perchloric acid. Biochem. J. 293, 223-7 (PMID: 8392333)
D. ERp29 – what does it do?
The Endoplasmic Reticulum (ER) plays several critical roles in cell biology including the production of secretory proteins and the safe storage of calcium inside cells. Numerous proteins reside in the ER and so hold medical importance as potential therapeutic targets for the many diseases associated with ER dysfunction (e.g. cystic fibrosis, type 2 diabetes, cancer). However, much needs to be learned about these ER residents both in terms of their individual functions and how they work together as the 'ER machinery'. We discovered ERp29 during proteomic analysis of rat enamel cells, leading to the naming and first description of this ubiquitous ER resident in 1997. The challenge since has been to figure out the functional role of ERp29, bioinformatics having offered only limited insight. In a series of pioneering studies, we've gathered a variety of clues that collectively point to a novel "housekeeping" role of general importance, probably as a new type of chaperone. Now linked to a broad array of physiological processes and diseases including cancer, ERp29 holds broad potential as a medical target.
- Suaud, L., Miller, K., Alvey, L., Yan, W., Robay, A., Kebler, C., Kreindler, J.L., Guttentag, S., Hubbard, M.J., Rubenstein, R.C. (2011) ERp29 Regulates {Delta}F508 and Wild-type Cystic Fibrosis Transmembrane Conductance Regulator (CFTR) Trafficking to the Plasma Membrane in Cystic Fibrosis (CF) and Non-CF Epithelial Cells. J. Biol. Chem. 286, 21239-21253 (PMID: 21525008)
- Das, S., Smith, T.D., Sarma, J.D., Ritzenthaler, J.D., Maza, J., Kaplan, B.E., Cunningham, L.A., Suaud, L., Hubbard, M.J., Rubenstein, R.C., and Koval, M (2009) ERp29 restricts Connexin43 oligomerization in the endoplasmic reticulum. Mol. Biol. Cell 20, 2593-2604 (PMID: 19321666)
- Shnyder, S.D., Mangum, J.E. and Hubbard, M.J. (2008) Triplex profiling of functionally distinct chaperones (ERp29/PDI/BiP) reveals marked heterogeneity of the endoplasmic reticulum proteome in cancer. J. Proteome Res. 7, 3364-3372 (PMID: 18598068)
- Hermann, V.M., Cutfield, J.F. and Hubbard, M.J. (2005) Biophysical characterization of ERp29: evidence for a key structural role of Cysteine-125. J. Biol. Chem. 280, 13529-13537 (PMID: 15572350)
- Hubbard, M.J., Mangum, J.E. and McHugh, N.J. (2004) Purification and biochemical characterisation of native ERp29 from rat liver. Biochem. J. 383, 589-598 (PMID: 15500441)
- Macleod, J.C., Sayer, R.J., Lucocq, J.M., and Hubbard, M.J. (2004) ERp29, a general endoplasmic reticulum marker, is highly expressed throughout the brain. J. Comp. Neurol. 477, 29-42 (PMID: 15281078)
- Shnyder, S.D. and Hubbard, M.J. (2002) ERp29 is a ubiquitous resident of the endoplasmic reticulum with a distinct role in secretory protein production. J. Histochem. Cytochem., 50, 557-566 (PMID: 11897809)
- Hubbard, M.J. (2002) Functional proteomics. The goalposts are moving. Proteomics, 2, 1069-1078 (PMID: 12362325)
- Hubbard, M.J., McHugh, N.J. and Carne, D.L. (2000) Isolation of ERp29, a novel endoplasmic reticulum protein, from rat enamel cells: Evidence for a unique role in secretory-protein synthesis. Eur. J. Biochem., 267, 1945-1957 (PMID: 10727933)
- Hubbard, M.J. and McHugh, N.J. (2000) Human ERp29: Isolation, primary structural characterisation and two-dimensional gel mapping. Electrophoresis, 21, 3785-379 (PMID: 11271497)
- Demmer, J., Zhou, C.M. and Hubbard, M.J. (1997) Molecular cloning of ERp29, a novel and widely expressed resident of the endoplasmic reticulum. FEBS Lett., 402, 145-150 (PMID: 9037184)
E. Other reports and articles
- Hubbard, M.J. (2006) Editorial – Hierarchical protein identifications and assignments. J. Proteome Res. 5, 733 (PMID: 16625735)
- Mangum, J.E., Farlie, P.G. and Hubbard, M.J. (2005) Proteomic profiling of facial development in chick embryos. Proteomics 5, 2542-2550 (PMID: 15912509)
- Piotte, C.P., Marshall, C.J., Hubbard, M.J., Collet, C. and Grigor, M.R. (1997) Lysozyme and a-lactalbumin from the milk of a marsupial, the common brush-tailed possum (Trichosurus vulpecula). Biochim. Biophys. Acta, 1336, 235-242 (PMID: 9305795)
- Hubbard, M.J. and McHugh, N.J. (1996) Mitochondrial ATP synthase F1-b-subunit is a calcium-binding protein. FEBS Lett., 391, 323-329 (PMID: 8764999)
- Bird, S.D., Walker, R.J. and Hubbard, M.J. (1994) Altered free calcium transients in pig kidney cells (LLC-PK1) cultured with penicillin/streptomycin. In Vitro Cell Dev. Biol. Anim., 30A, 420-4 (PMID: 7952510)
- Hubbard, M.J. and Cohen, P. (1993) On target with a new mechanism for the regulation of protein phosphorylation. Trends Biochem. Sci 18, 172-7 (PMID: 8392229)
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