The Role of the Golgi-resident SPCA Ca²⁺/Mn²⁺ Pump in Ionic Homeostasis and Neural Function

Overview

Journal Neurochem Res

Specialties Chemistry
Neurology

Date 2011 Nov 16

PMID 22083668

Citations 18

Authors

Wenfang He

Zhiping Hu

Affiliations

Soon will be listed here.

Abstract

Recent evidence highlights the functional importance of the Golgi apparatus (GA) in neurological diseases. The functions of the mammalian GA, in addition to the processing and transport of cargo, also include ionic homeostasis. Besides Ca²⁺-release channels which serves GA as an agonist-sensitive intracellular Ca²⁺ store, and Ca²⁺-binding proteins, the GA contains Ca²⁺-uptake mechanisms consisting of the well-known sarco-endoplasmic reticulum Ca²⁺-transport ATPases and the much less characterized secretory-pathway Ca²⁺-transport ATPases (SPCA). SPCA can transport both Ca²⁺ and Mn²⁺ into the Golgi lumen and therefore is involved in the cytosolic and intra-Golgi Ca²⁺ and Mn²⁺ homeostasis. It has shown that both of the mRNA and protein of SPCAs are highly expressed in brain. In addition, brain is the region with the highest activity of SPCA isoforms, which may be related to the involvement of Ca²⁺ and Mn²⁺ homeostasis in neural functions. In this review, we compile some recent findings showing that the SPCA isoform plays a much more important role in intracellular ionic homeostasis than previously anticipated and illustrating the involvement of SPCA isoforms in certain neurophysiological or neuropathological process. We are interested in gaining insight into the intricate role of the SPCA pumps to explain the GA-specific functions in neurological disorders.

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References

Missiaen L, Vanoevelen J, Van Acker K, Raeymaekers L, Parys J, Callewaert G . Ca(2+) signals in Pmr1-GFP-expressing COS-1 cells with functional endoplasmic reticulum. Biochem Biophys Res Commun. 2002; 294(2):249-53. DOI: 10.1016/S0006-291X(02)00461-8. View

Rudolph H, Antebi A, Fink G, Buckley C, Dorman T, LeVitre J . The yeast secretory pathway is perturbed by mutations in PMR1, a member of a Ca2+ ATPase family. Cell. 1989; 58(1):133-45. DOI: 10.1016/0092-8674(89)90410-8. View

Mayuzumi N, Ikeda S, Kawada H, Fan P, Ogawa H . Effects of ultraviolet B irradiation, proinflammatory cytokines and raised extracellular calcium concentration on the expression of ATP2A2 and ATP2C1. Br J Dermatol. 2005; 152(4):697-701. DOI: 10.1111/j.1365-2133.2005.06383.x. View

Sepulveda M, Marcos D, Berrocal M, Raeymaekers L, Mata A, Wuytack F . Activity and localization of the secretory pathway Ca2+-ATPase isoform 1 (SPCA1) in different areas of the mouse brain during postnatal development. Mol Cell Neurosci. 2008; 38(4):461-73. DOI: 10.1016/j.mcn.2008.02.012. View

Missiaen L, Van Acker K, Van Baelen K, Raeymaekers L, Wuytack F, Parys J . Calcium release from the Golgi apparatus and the endoplasmic reticulum in HeLa cells stably expressing targeted aequorin to these compartments. Cell Calcium. 2004; 36(6):479-87. DOI: 10.1016/j.ceca.2004.04.007. View

Locke E, Bonilla M, Liang L, Takita Y, Cunningham K . A homolog of voltage-gated Ca(2+) channels stimulated by depletion of secretory Ca(2+) in yeast. Mol Cell Biol. 2000; 20(18):6686-94. PMC: 86178. DOI: 10.1128/MCB.20.18.6686-6694.2000. View

Wootton L, Argent C, Wheatley M, Michelangeli F . The expression, activity and localisation of the secretory pathway Ca2+ -ATPase (SPCA1) in different mammalian tissues. Biochim Biophys Acta. 2004; 1664(2):189-97. DOI: 10.1016/j.bbamem.2004.05.009. View

De Meis L, Vianna A . Energy interconversion by the Ca2+-dependent ATPase of the sarcoplasmic reticulum. Annu Rev Biochem. 1979; 48:275-92. DOI: 10.1146/annurev.bi.48.070179.001423. View

Yoshida M, Yamasaki K, Daiho T, Iizuka H, Suzuki H . ATP2C1 is specifically localized in the basal layer of normal epidermis and its depletion triggers keratinocyte differentiation. J Dermatol Sci. 2006; 43(1):21-33. DOI: 10.1016/j.jdermsci.2006.03.003. View

10.

Harper C, Wootton L, Michelangeli F, Lefievre L, Barratt C, Publicover S . Secretory pathway Ca(2+)-ATPase (SPCA1) Ca(2)+ pumps, not SERCAs, regulate complex [Ca(2+)](i) signals in human spermatozoa. J Cell Sci. 2005; 118(Pt 8):1673-85. DOI: 10.1242/jcs.02297. View

11.

Halachmi D, Eilam Y . Elevated cytosolic free Ca2+ concentrations and massive Ca2+ accumulation within vacuoles, in yeast mutant lacking PMR1, a homolog of Ca2+ -ATPase. FEBS Lett. 1996; 392(2):194-200. DOI: 10.1016/0014-5793(96)00799-5. View

12.

Dobson A, Erikson K, Aschner M . Manganese neurotoxicity. Ann N Y Acad Sci. 2004; 1012:115-28. DOI: 10.1196/annals.1306.009. View

13.

Gonatas N, Stieber A, Gonatas J . Fragmentation of the Golgi apparatus in neurodegenerative diseases and cell death. J Neurol Sci. 2006; 246(1-2):21-30. DOI: 10.1016/j.jns.2006.01.019. View

14.

Baron S, Vangheluwe P, Sepulveda M, Wuytack F, Raeymaekers L, Vanoevelen J . The secretory pathway Ca(2+)-ATPase 1 is associated with cholesterol-rich microdomains of human colon adenocarcinoma cells. Biochim Biophys Acta. 2010; 1798(8):1512-21. DOI: 10.1016/j.bbamem.2010.03.023. View

15.

SORIN A, Rosas G, Rao R . PMR1, a Ca2+-ATPase in yeast Golgi, has properties distinct from sarco/endoplasmic reticulum and plasma membrane calcium pumps. J Biol Chem. 1997; 272(15):9895-901. DOI: 10.1074/jbc.272.15.9895. View

16.

Wei Y, Marchi V, Wang R, Rao R . An N-terminal EF hand-like motif modulates ion transport by Pmr1, the yeast Golgi Ca(2+)/Mn(2+)-ATPase. Biochemistry. 1999; 38(44):14534-41. DOI: 10.1021/bi9911233. View

17.

Farina F, Uccelletti D, Goffrini P, Butow R, Abeijon C, Palleschi C . Alterations of O-glycosylation, cell wall, and mitochondrial metabolism in Kluyveromyces lactis cells defective in KlPmr1p, the Golgi Ca(2+)-ATPase. Biochem Biophys Res Commun. 2004; 318(4):1031-8. DOI: 10.1016/j.bbrc.2004.04.127. View

18.

Luk E, Culotta V . Manganese superoxide dismutase in Saccharomyces cerevisiae acquires its metal co-factor through a pathway involving the Nramp metal transporter, Smf2p. J Biol Chem. 2001; 276(50):47556-62. DOI: 10.1074/jbc.M108923200. View

19.

Reinhardt T, Horst R . Ca2+-ATPases and their expression in the mammary gland of pregnant and lactating rats. Am J Physiol. 1999; 276(4):C796-802. DOI: 10.1152/ajpcell.1999.276.4.C796. View

20.

Thackray A, Knight R, Haswell S, Bujdoso R, Brown D . Metal imbalance and compromised antioxidant function are early changes in prion disease. Biochem J. 2002; 362(Pt 1):253-8. PMC: 1222383. DOI: 10.1042/0264-6021:3620253. View