Skip to main content

Advertisement

Log in

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

  • Overview
  • Published:
Neurochemical Research Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Maag RS, Hicks SW, Machamer CE (2003) Death from within: apoptosis and the secretory pathway. Curr Opin Cell Biol 15:456–461

    PubMed  CAS  Google Scholar 

  2. Hicks SW, Machamer CE (2005) Golgi structure in stress sensing and apoptosis. Biochim Biophys Acta 1744:406–414

    PubMed  CAS  Google Scholar 

  3. Jiang Z, Hu Z, Zeng L, Lu W, Zhang H, Li T, Xiao H (2011) The role of the Golgi apparatus in oxidative stress: is this organelle less significant than mitochondria? Free Radic Biol Med 50:907–917

    PubMed  CAS  Google Scholar 

  4. Rudolph HK, Antebi A, Fink GR, Buckley CM, Dorman TE, LeVitre J, Davidow LS, Mao JI, Moir DT (1989) The yeast secretory pathway is perturbed by mutations in PMR1, a member of a Ca2+ ATPase family. Cell 58:133–145

    PubMed  CAS  Google Scholar 

  5. Hu Z, Bonifas JM, Beech J, Bench G, Shigihara T, Ogawa H, Ikeda S, Mauro T, Epstein EJ (2000) Mutations in ATP2C1, encoding a calcium pump, cause Hailey–Hailey disease. Nat Genet 24:61–65

    PubMed  CAS  Google Scholar 

  6. Sudbrak R, Brown J, Dobson-Stone C, Carter S, Ramser J, White J, Healy E, Dissanayake M, Larregue M, Perrussel M, Lehrach H, Munro CS, Strachan T, Burge S, Hovnanian A, Monaco AP (2000) Hailey–Hailey disease is caused by mutations in ATP2C1 encoding a novel Ca(2+) pump. Hum Mol Genet 9:1131–1140

    PubMed  CAS  Google Scholar 

  7. Xiang M, Mohamalawari D, Rao R (2005) A novel isoform of the secretory pathway Ca2+, Mn(2+)-ATPase, hSPCA2, has unusual properties and is expressed in the brain. J Biol Chem 280:11608–11614

    PubMed  CAS  Google Scholar 

  8. Uccelletti D, Farina F, Pinton P, Goffrini P, Mancini P, Talora C, Rizzuto R, Palleschi C (2005) The Golgi Ca2+-ATPase KlPmr1p function is required for oxidative stress response by controlling the expression of the heat-shock element HSP60 in Kluyveromyces lactis. Mol Biol Cell 16:4636–4647

    PubMed  CAS  Google Scholar 

  9. Wootton LL, Argent CC, Wheatley M, Michelangeli F (2004) The expression, activity and localisation of the secretory pathway Ca2+-ATPase (SPCA1) in different mammalian tissues. Biochim Biophys Acta 1664:189–197

    PubMed  CAS  Google Scholar 

  10. Ton VK, Mandal D, Vahadji C, Rao R (2002) Functional expression in yeast of the human secretory pathway Ca(2+), Mn(2+)-ATPase defective in Hailey–Hailey disease. J Biol Chem 277:6422–6427

    PubMed  CAS  Google Scholar 

  11. Wei Y, Chen J, Rosas G, Tompkins DA, Holt PA, Rao R (2000) Phenotypic screening of mutations in Pmr1, the yeast secretory pathway Ca2+/Mn2+-ATPase, reveals residues critical for ion selectivity and transport. J Biol Chem 275:23927–23932

    PubMed  CAS  Google Scholar 

  12. Yu M, Zhong L, Rishi AK, Khadeer M, Inesi G, Hussain A (1998) Specific substitutions at amino acid 256 of the sarcoplasmic/endoplasmic reticulum Ca2+transport ATPase mediate resistance to thapsigargin in thapsigargin-resistant hamster cells. J Biol Chem 273:3542–3546

    PubMed  CAS  Google Scholar 

  13. Wei Y, Marchi V, Wang R, Rao R (1999) An N-terminal EF hand-like motif modulates ion transport by Pmr1, the yeast Golgi Ca(2+)/Mn(2+)-ATPase. Biochemistry 38:14534–14541

    PubMed  CAS  Google Scholar 

  14. Huster D, Lutsenko S (2003) The distinct roles of the N-terminal copper-binding sites in regulation of catalytic activity of the Wilson’s disease protein. J Biol Chem 278:32212–32218

    PubMed  CAS  Google Scholar 

  15. Van Baelen K, Vanoevelen J, Missiaen L, Raeymaekers L, Wuytack F (2001) The Golgi PMR1 P-type ATPase of Caenorhabditis elegans. Identification of the gene and demonstration of calcium and manganese transport. J Biol Chem 276:10683–10691

    PubMed  Google Scholar 

  16. Mandal D, Woolf TB, Rao R (2000) Manganese selectivity of pmr1, the yeast secretory pathway ion pump, is defined by residue gln783 in transmembrane segment 6. Residue Asp778 is essential for cation transport. J Biol Chem 275:23933–23938

    PubMed  CAS  Google Scholar 

  17. Mandal D, Rulli SJ, Rao R (2003) Packing interactions between transmembrane helices alter ion selectivity of the yeast Golgi Ca2+/Mn2+-ATPase PMR1. J Biol Chem 278:35292–35298

    PubMed  CAS  Google Scholar 

  18. Fairclough RJ, Dode L, Vanoevelen J, Andersen JP, Missiaen L, Raeymaekers L, Wuytack F, Hovnanian A (2003) Effect of Hailey–Hailey Disease mutations on the function of a new variant of human secretory pathway Ca2+/Mn2+-ATPase (hSPCA1). J Biol Chem 278:24721–24730

    PubMed  CAS  Google Scholar 

  19. Mukhopadhyay S, Linstedt AD (2011) Identification of a gain-of-function mutation in a Golgi P-type ATPase that enhances Mn2+ efflux and protects against toxicity. Proc Natl Acad Sci USA 108:858–863

    PubMed  CAS  Google Scholar 

  20. Dode L, Andersen JP, Raeymaekers L, Missiaen L, Vilsen B, Wuytack F (2005) Functional comparison between secretory pathway Ca2+/Mn2+-ATPase (SPCA) 1 and sarcoplasmic reticulum Ca2+-ATPase (SERCA) 1 isoforms by steady-state and transient kinetic analyses. J Biol Chem 280:39124–39134

    PubMed  CAS  Google Scholar 

  21. Dode L, Andersen JP, Vanoevelen J, Raeymaekers L, Missiaen L, Vilsen B, Wuytack F (2006) Dissection of the functional differences between human secretory pathway Ca2+/Mn2+-ATPase (SPCA) 1 and 2 isoenzymes by steady-state and transient kinetic analyses. J Biol Chem 281:3182–3189

    PubMed  CAS  Google Scholar 

  22. Sepulveda MR, Berrocal M, Marcos D, Wuytack F, Mata AM (2007) Functional and immunocytochemical evidence for the expression and localization of the secretory pathway Ca2+-ATPase isoform 1 (SPCA1) in cerebellum relative to other Ca2+ pumps. J Neurochem 103:1009–1018

    PubMed  CAS  Google Scholar 

  23. Sepulveda MR, Marcos D, Berrocal M, Raeymaekers L, Mata AM, Wuytack F (2008) 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 38:461–473

    PubMed  CAS  Google Scholar 

  24. Sorin A, Rosas G, Rao R (1997) PMR1, a Ca2+-ATPase in yeast Golgi, has properties distinct from sarco/endoplasmic reticulum and plasma membrane calcium pumps. J Biol Chem 272:9895–9901

    PubMed  CAS  Google Scholar 

  25. Vanoevelen J, Dode L, Van Baelen K, Fairclough RJ, Missiaen L, Raeymaekers L, Wuytack F (2005) The secretory pathway Ca2+/Mn2+-ATPase 2 is a Golgi-localized pump with high affinity for Ca2+ ions. J Biol Chem 280:22800–22808

    PubMed  CAS  Google Scholar 

  26. Sagara Y, Inesi G (1991) Inhibition of the sarcoplasmic reticulum Ca2+ transport ATPase by thapsigargin at subnanomolar concentrations. J Biol Chem 266:13503–13506

    PubMed  CAS  Google Scholar 

  27. de Meis L, Vianna AL (1979) Energy interconversion by the Ca2+-dependent ATPase of the sarcoplasmic reticulum. Annu Rev Biochem 48:275–292

    PubMed  Google Scholar 

  28. Reinhardt TA, Horst RL, Waters WR (2004) Characterization of Cos-7 cells overexpressing the rat secretory pathway Ca2+-ATPase. Am J Physiol Cell Physiol 286:C164–C169

    PubMed  CAS  Google Scholar 

  29. Vanoevelen J, Raeymaekers L, Dode L, Parys JB, De Smedt H, Callewaert G, Wuytack F, Missiaen L (2005) Cytosolic Ca2+signals depending on the functional state of the Golgi in HeLa cells. Cell Calcium 38:489–495

    PubMed  CAS  Google Scholar 

  30. Sepulveda MR, Vanoevelen J, Raeymaekers L, Mata AM, Wuytack F (2009) Silencing the SPCA1 (secretory pathway Ca2+-ATPase isoform 1) impairs Ca2+ homeostasis in the Golgi and disturbs neural polarity. J Neurosci 29:12174–12182

    PubMed  CAS  Google Scholar 

  31. Mitchell KJ, Tsuboi T, Rutter GA (2004) Role for plasma membrane-related Ca2+-ATPase-1 (ATP2C1) in pancreatic beta-cell Ca2+ homeostasis revealed by RNA silencing. Diabetes 53:393–400

    PubMed  CAS  Google Scholar 

  32. Micaroni M, Perinetti G, Berrie CP, Mironov AA (2010) The SPCA1 Ca2+ pump and intracellular membrane trafficking. Traffic 11:1315–1333

    PubMed  CAS  Google Scholar 

  33. Behne MJ, Tu CL, Aronchik I, Epstein E, Bench G, Bikle DD, Pozzan T, Mauro TM (2003) Human keratinocyte ATP2C1 localizes to the Golgi and controls Golgi Ca2+ stores. J Invest Dermatol 121:688–694

    PubMed  CAS  Google Scholar 

  34. Harper C, Wootton L, Michelangeli F, Lefievre L, Barratt C, Publicover S (2005) Secretory pathway Ca(2+)-ATPase (SPCA1) Ca(2)+ pumps, not SERCAs, regulate complex [Ca(2+)](i) signals in human spermatozoa. J Cell Sci 118:1673–1685

    PubMed  CAS  Google Scholar 

  35. Southall TD, Terhzaz S, Cabrero P, Chintapalli VR, Evans JM, Dow JA, Davies SA (2006) Novel subcellular locations and functions for secretory pathway Ca2+/Mn2+-ATPases. Physiol Genomics 26:35–45

    PubMed  CAS  Google Scholar 

  36. Baron S, Struyf S, Wuytack F, Van Damme J, Missiaen L, Raeymaekers L, Vanoevelen J (2009) Contribution of intracellular Ca2+ stores to Ca2+ signaling during chemokinesis of human neutrophil granulocytes. Biochim Biophys Acta 1793:1041–1049

    PubMed  CAS  Google Scholar 

  37. Faddy HM, Smart CE, Xu R, Lee GY, Kenny PA, Feng M, Rao R, Brown MA, Bissell MJ, Roberts-Thomson SJ, Monteith GR (2008) Localization of plasma membrane and secretory calcium pumps in the mammary gland. Biochem Biophys Res Commun 369:977–981

    PubMed  CAS  Google Scholar 

  38. Van Baelen K, Vanoevelen J, Callewaert G, Parys JB, De Smedt H, Raeymaekers L, Rizzuto R, Missiaen L, Wuytack F (2003) The contribution of the SPCA1 Ca2+ pump to the Ca2+ accumulation in the Golgi apparatus of HeLa cells assessed via RNA-mediated interference. Biochem Biophys Res Commun 306:430–436

    PubMed  Google Scholar 

  39. Lissandron V, Podini P, Pizzo P, Pozzan T (2010) Unique characteristics of Ca2+ homeostasis of the trans-Golgi compartment. Proc Natl Acad Sci USA 107:9198–9203

    PubMed  CAS  Google Scholar 

  40. Reinhardt TA, Filoteo AG, Penniston JT, Horst RL (2000) Ca(2+)-ATPase protein expression in mammary tissue. Am J Physiol Cell Physiol 279:C1595–C1602

    PubMed  CAS  Google Scholar 

  41. Reinhardt TA, Horst RL (1999) Ca2+-ATPases and their expression in the mammary gland of pregnant and lactating rats. Am J Physiol 276:C796–C802

    PubMed  CAS  Google Scholar 

  42. Rojas P, Surroca A, Orellana A, Wolff D (2000) Kinetic characterization of calcium uptake by the rat liver Golgi apparatus. Cell Biol Int 24:229–233

    PubMed  CAS  Google Scholar 

  43. Taylor RS, Jones SM, Dahl RH, Nordeen MH, Howell KE (1997) Characterization of the Golgi complex cleared of proteins in transit and examination of calcium uptake activities. Mol Biol Cell 8:1911–1931

    PubMed  CAS  Google Scholar 

  44. Lin P, Yao Y, Hofmeister R, Tsien RY, Farquhar MG (1999) Overexpression of CALNUC (nucleobindin) increases agonist and thapsigargin releasable Ca2+ storage in the Golgi. J Cell Biol 145:279–289

    PubMed  CAS  Google Scholar 

  45. Pinton P, Pozzan T, Rizzuto R (1998) The Golgi apparatus is an inositol 1, 4, 5-trisphosphate-sensitive Ca2+ store, with functional properties distinct from those of the endoplasmic reticulum. EMBO J 17:5298–5308

    PubMed  CAS  Google Scholar 

  46. Surroca A, Wolff D (2000) Inositol 1, 4, 5-trisphosphate but not ryanodine-receptor agonists induces calcium release from rat liver Golgi apparatus membrane vesicles. J Membr Biol 177:243–249

    PubMed  CAS  Google Scholar 

  47. Missiaen L, Van Acker K, Van Baelen K, Raeymaekers L, Wuytack F, Parys JB, De Smedt H, Vanoevelen J, Dode L, Rizzuto R, Callewaert G (2004) Calcium release from the Golgi apparatus and the endoplasmic reticulum in HeLa cells stably expressing targeted aequorin to these compartments. Cell Calcium 36:479–487

    PubMed  CAS  Google Scholar 

  48. Vanoevelen J, Raeymaekers L, Parys JB, De Smedt H, Van Baelen K, Callewaert G, Wuytack F, Missiaen L (2004) Inositol trisphosphate producing agonists do not mobilize the thapsigargin-insensitive part of the endoplasmic-reticulum and Golgi Ca2+ store. Cell Calcium 35:115–121

    PubMed  CAS  Google Scholar 

  49. Locke EG, Bonilla M, Liang L, Takita Y, Cunningham KW (2000) A homolog of voltage-gated Ca(2+) channels stimulated by depletion of secretory Ca(2+) in yeast. Mol Cell Biol 20:6686–6694

    PubMed  CAS  Google Scholar 

  50. Missiaen L, Vanoevelen J, Van Acker K, Raeymaekers L, Parys JB, Callewaert G, Wuytack F, De Smedt H (2002) Ca(2+) signals in Pmr1-GFP-expressing COS-1 cells with functional endoplasmic reticulum. Biochem Biophys Res Commun 294:249–253

    PubMed  CAS  Google Scholar 

  51. Halachmi D, Eilam Y (1996) Elevated cytosolic free Ca2+ concentrations and massive Ca2+ accumulation within vacuoles, in yeast mutant lacking PMR1, a homolog of Ca2+-ATPase. FEBS Lett 392:194–200

    PubMed  CAS  Google Scholar 

  52. Callewaert G, Parys JB, De Smedt H, Raeymaekers L, Wuytack F, Vanoevelen J, Van Baelen K, Simoni A, Rizzuto R, Missiaen L (2003) Similar Ca(2+)-signaling properties in keratinocytes and in COS-1 cells overexpressing the secretory-pathway Ca(2+)-ATPase SPCA1. Cell Calcium 34:157–162

    PubMed  CAS  Google Scholar 

  53. Missiaen L, Van Acker K, Parys JB, De Smedt H, Van Baelen K, Weidema AF, Vanoevelen J, Raeymaekers L, Renders J, Callewaert G, Rizzuto R, Wuytack F (2001) Baseline cytosolic Ca2+ oscillations derived from a non-endoplasmic reticulum Ca2+ store. J Biol Chem 276:39161–39170

    PubMed  CAS  Google Scholar 

  54. Lai P, Michelangeli F (2009) Changes in expression and activity of the secretory pathway Ca2+ ATPase 1 (SPCA1) in A7r5 vascular smooth muscle cells cultured at different glucose concentrations. Biosci Rep 29:397–404

    PubMed  CAS  Google Scholar 

  55. Ramos-Castaneda J, Park YN, Liu M, Hauser K, Rudolph H, Shull GE, Jonkman MF, Mori K, Ikeda S, Ogawa H, Arvan P (2005) Deficiency of ATP2C1, a Golgi ion pump, induces secretory pathway defects in endoplasmic reticulum (ER)-associated degradation and sensitivity to ER stress. J Biol Chem 280:9467–9473

    PubMed  CAS  Google Scholar 

  56. Kawada H, Nishiyama C, Takagi A, Tokura T, Nakano N, Maeda K, Mayuzumi N, Ikeda S, Okumura K, Ogawa H (2005) Transcriptional regulation of ATP2C1 gene by Sp1 and YY1 and reduced function of its promoter in Hailey–Hailey disease keratinocytes. J Invest Dermatol 124:1206–1214

    PubMed  CAS  Google Scholar 

  57. Mayuzumi N, Ikeda S, Kawada H, Fan PS, Ogawa H (2005) Effects of ultraviolet B irradiation, proinflammatory cytokines and raised extracellular calcium concentration on the expression of ATP2A2 and ATP2C1. Br J Dermatol 152:697–701

    PubMed  CAS  Google Scholar 

  58. Yoshida M, Yamasaki K, Daiho T, Iizuka H, Suzuki H (2006) ATP2C1 is specifically localized in the basal layer of normal epidermis and its depletion triggers keratinocyte differentiation. J Dermatol Sci 43:21–33

    PubMed  CAS  Google Scholar 

  59. Squier TC, Bigelow DJ (2000) Protein oxidation and age-dependent alterations in calcium homeostasis. Front Biosci 5:D504–D526

    PubMed  CAS  Google Scholar 

  60. Grice DM, Vetter I, Faddy HM, Kenny PA, Roberts-Thomson SJ, Monteith GR (2010) Golgi calcium pump secretory pathway calcium ATPase 1 (SPCA1) is a key regulator of insulin-like growth factor receptor (IGF1R) processing in the basal-like breast cancer cell line MDA-MB-231. J Biol Chem 285:37458–37466

    PubMed  CAS  Google Scholar 

  61. Vashist S, Frank CG, Jakob CA, Ng DT (2002) Two distinctly localized p-type ATPases collaborate to maintain organelle homeostasis required for glycoprotein processing and quality control. Mol Biol Cell 13:3955–3966

    PubMed  CAS  Google Scholar 

  62. Durr G, Strayle J, Plemper R, Elbs S, Klee SK, Catty P, Wolf DH, Rudolph HK (1998) The medial-Golgi ion pump Pmr1 supplies the yeast secretory pathway with Ca2+ and Mn2+ required for glycosylation, sorting, and endoplasmic reticulum-associated protein degradation. Mol Biol Cell 9:1149–1162

    PubMed  CAS  Google Scholar 

  63. Farina F, Uccelletti D, Goffrini P, Butow RA, Abeijon C, Palleschi C (2004) 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 318:1031–1038

    PubMed  CAS  Google Scholar 

  64. Cabiscol E, Belli G, Tamarit J, Echave P, Herrero E, Ros J (2002) Mitochondrial Hsp60, resistance to oxidative stress, and the labile iron pool are closely connected in Saccharomyces cerevisiae. J Biol Chem 277:44531–44538

    PubMed  CAS  Google Scholar 

  65. Okunade GW, Miller ML, Azhar M, Andringa A, Sanford LP, Doetschman T, Prasad V, Shull GE (2007) Loss of the Atp2c1 secretory pathway Ca(2+)-ATPase (SPCA1) in mice causes Golgi stress, apoptosis, and midgestational death in homozygous embryos and squamous cell tumors in adult heterozygotes. J Biol Chem 282:26517–26527

    PubMed  CAS  Google Scholar 

  66. Hearn AS, Stroupe ME, Cabelli DE, Lepock JR, Tainer JA, Nick HS, Silverman DN (2001) Kinetic analysis of product inhibition in human manganese superoxide dismutase. Biochemistry 40:12051–12058

    PubMed  CAS  Google Scholar 

  67. Cottrell GS, Hooper NM, Turner AJ (2000) Cloning, expression, and characterization of human cytosolic aminopeptidase P: a single manganese(II)-dependent enzyme. Biochemistry 39:15121–15128

    PubMed  CAS  Google Scholar 

  68. Golub MS, Hogrefe CE, Germann SL, Tran TT, Beard JL, Crinella FM, Lonnerdal B (2005) Neurobehavioral evaluation of rhesus monkey infants fed cow’s milk formula, soy formula, or soy formula with added manganese. Neurotoxicol Teratol 27:615–627

    PubMed  CAS  Google Scholar 

  69. Dobson AW, Erikson KM, Aschner M (2004) Manganese neurotoxicity. Ann NY Acad Sci 1012:115–128

    PubMed  CAS  Google Scholar 

  70. Hirata Y (2002) Manganese-induced apoptosis in PC12 cells. Neurotoxicol Teratol 24:639–653

    PubMed  CAS  Google Scholar 

  71. Milatovic D, Zaja-Milatovic S, Gupta RC, Yu Y, Aschner M (2009) Oxidative damage and neurodegeneration in manganese-induced neurotoxicity. Toxicol Appl Pharmacol 240:219–225

    PubMed  CAS  Google Scholar 

  72. Hirata Y, Kiuchi K, Nagatsu T (2001) Manganese mimics the action of 1-methyl-4-phenylpyridinium ion, a dopaminergic neurotoxin, in rat striatal tissue slices. Neurosci Lett 311:53–56

    PubMed  CAS  Google Scholar 

  73. Aschner M, Guilarte TR, Schneider JS, Zheng W (2007) Manganese: recent advances in understanding its transport and neurotoxicity. Toxicol Appl Pharmacol 221:131–147

    PubMed  CAS  Google Scholar 

  74. Fong CS, Wu RM, Shieh JC, Chao YT, Fu YP, Kuao CL, Cheng CW (2007) Pesticide exposure on southwestern Taiwanese with MnSOD and NQO1 polymorphisms is associated with increased risk of Parkinson’s disease. Clinica Chimica Acta 378:136–141

    CAS  Google Scholar 

  75. Olanow CW (2004) Manganese-induced parkinsonism and Parkinson’s disease. Ann NY Acad Sci 1012:209–223

    PubMed  CAS  Google Scholar 

  76. Hitzeroth A, Niehaus DJ, Koen L, Botes WC, Deleuze JF, Warnich L (2007) Association between the MnSOD Ala-9Val polymorphism and development of schizophrenia and abnormal involuntary movements in the Xhosa population. Prog Neuropsychopharmacol Biol Psychiatry 31:664–672

    PubMed  CAS  Google Scholar 

  77. Thackray AM, Knight R, Haswell SJ, Bujdoso R, Brown DR (2002) Metal imbalance and compromised antioxidant function are early changes in prion disease. Biochem J 362:253–258

    PubMed  CAS  Google Scholar 

  78. Towler MC, Prescott AR, James J, Lucocq JM, Ponnambalam S (2000) The manganese cation disrupts membrane dynamics along the secretory pathway. Exp Cell Res 259:167–179

    PubMed  CAS  Google Scholar 

  79. Bolton EC, Mildvan AS, Boeke JD (2002) Inhibition of reverse transcription in vivo by elevated manganese ion concentration. Molecular Cell 9:879–889

    PubMed  CAS  Google Scholar 

  80. Erikson KM, Aschner M (2003) Manganese neurotoxicity and glutamate-GABA interaction. Neurochem Int 43:475–480

    PubMed  CAS  Google Scholar 

  81. Zhang S, Fu J, Zhou Z (2005) Changes in the brain mitochondrial proteome of male Sprague-Dawley rats treated with manganese chloride. Toxicol Appl Pharmacol 202:13–17

    PubMed  CAS  Google Scholar 

  82. Leitch S, Feng M, Muend S, Braiterman LT, Hubbard AL, Rao R (2011) Vesicular distribution of secretory pathway Ca(2)+-ATPase isoform 1 and a role in manganese detoxification in liver-derived polarized cells. Biometals 24:159–170

    PubMed  CAS  Google Scholar 

  83. Burkhard PR, Delavelle J, Du Pasquier R, Spahr L (2003) Chronic parkinsonism associated with cirrhosis: a distinct subset of acquired hepatocerebral degeneration. Arch Neurol 60:521–528

    PubMed  Google Scholar 

  84. Aggarwal A, Vaidya S, Shah S, Singh J, Desai S, Bhatt M (2006) Reversible Parkinsonism and T1W pallidal hyperintensities in acute liver failure. Mov Disord 21:1986–1990

    PubMed  Google Scholar 

  85. Gunter TE, Gavin CE, Aschner M, Gunter KK (2006) Speciation of manganese in cells and mitochondria: a search for the proximal cause of manganese neurotoxicity. Neurotoxicology 27:765–776

    PubMed  CAS  Google Scholar 

  86. Bae JH, Jang BC, Suh SI, Ha E, Baik HH, Kim SS, Lee MY, Shin DH (2006) Manganese induces inducible nitric oxide synthase (iNOS) expression via activation of both MAP kinase and PI3K/Akt pathways in BV2 microglial cells. Neurosci Lett 398:151–154

    PubMed  CAS  Google Scholar 

  87. Prabhakaran K, Ghosh D, Chapman GD, Gunasekar PG (2008) Molecular mechanism of manganese exposure-induced dopaminergic toxicity. Brain Res Bull 76:361–367

    PubMed  CAS  Google Scholar 

  88. Liu X, Sullivan KA, Madl JE, Legare M, Tjalkens RB (2006) Manganese-induced neurotoxicity: the role of astroglial-derived nitric oxide in striatal interneuron degeneration. Toxicol Sci 91:521–531

    PubMed  CAS  Google Scholar 

  89. Ramesh GT, Ghosh D, Gunasekar PG (2002) Activation of early signaling transcription factor, NF-kappaB following low-level manganese exposure. Toxicol Lett 136:151–158

    PubMed  CAS  Google Scholar 

  90. Wise K, Manna S, Barr J, Gunasekar P, Ramesh G (2004) Activation of activator protein-1 DNA binding activity due to low level manganese exposure in pheochromocytoma cells. Toxicol Lett 147:237–244

    PubMed  CAS  Google Scholar 

  91. Sanchez RJ, Srinivasan C, Munroe WH, Wallace MA, Martins J, Kao TY, Le K, Gralla EB, Valentine JS (2005) Exogenous manganous ion at millimolar levels rescues all known dioxygen-sensitive phenotypes of yeast lacking CuZnSOD. J Biol Inorg Chem 10:913–923

    PubMed  CAS  Google Scholar 

  92. Luk EE, Culotta VC (2001) Manganese superoxide dismutase in Saccharomyces cerevisiae acquires its metal co-factor through a pathway involving the Nramp metal transporter, Smf2p. J Biol Chem 276:47556–47562

    PubMed  CAS  Google Scholar 

  93. Lapinskas PJ, Cunningham KW, Liu XF, Fink GR, Culotta VC (1995) Mutations in PMR1 suppress oxidative damage in yeast cells lacking superoxide dismutase. Mol Cell Biol 15:1382–1388

    PubMed  CAS  Google Scholar 

  94. Cho JH, Ko KM, Singaravelu G, Ahnn J (2005) Caenorhabditis elegans PMR1, a P-type calcium ATPase, is important for calcium/manganese homeostasis and oxidative stress response. FEBS Lett 579:778–782

    PubMed  CAS  Google Scholar 

  95. Gunteski-Hamblin AM, Clarke DM, Shull GE (1992) Molecular cloning and tissue distribution of alternatively spliced mRNAs encoding possible mammalian homologues of the yeast secretory pathway calcium pump. Biochemistry 31:7600–7608

    PubMed  CAS  Google Scholar 

  96. Murin R, Verleysdonk S, Raeymaekers L, Kaplan P, Lehotsky J (2006) Distribution of secretory pathway Ca2+ ATPase (SPCA1) in neuronal and glial cell cultures. Cell Mol Neurobiol 26:1355–1365

    PubMed  CAS  Google Scholar 

  97. Baron S, Vangheluwe P, Sepulveda MR, Wuytack F, Raeymaekers L, Vanoevelen J (2010) The secretory pathway Ca(2+)-ATPase 1 is associated with cholesterol-rich microdomains of human colon adenocarcinoma cells. Biochim Biophys Acta 1798:1512–1521

    PubMed  CAS  Google Scholar 

  98. Dolman NJ, Tepikin AV (2006) Calcium gradients and the Golgi. Cell Calcium 40:505–512

    PubMed  CAS  Google Scholar 

  99. Evanko DS, Zhang Q, Zorec R, Haydon PG (2004) Defining pathways of loss and secretion of chemical messengers from astrocytes. Glia 47:233–240

    PubMed  Google Scholar 

  100. Volterra A, Meldolesi J (2005) Astrocytes, from brain glue to communication elements: the revolution continues. Nat Rev Neurosci 6:626–640

    PubMed  CAS  Google Scholar 

  101. Mitchell KJ, Pinton P, Varadi A, Tacchetti C, Ainscow EK, Pozzan T, Rizzuto R, Rutter GA (2001) Dense core secretory vesicles revealed as a dynamic Ca(2+) store in neuroendocrine cells with a vesicle-associated membrane protein aequorin chimaera. J Cell Biol 155:41–51

    PubMed  CAS  Google Scholar 

  102. Lohmann C (2009) Calcium signaling and the development of specific neuronal connections. Prog Brain Res 175:443–452

    PubMed  Google Scholar 

  103. Horton AC, Racz B, Monson EE, Lin AL, Weinberg RJ, Ehlers MD (2005) Polarized secretory trafficking directs cargo for asymmetric dendrite growth and morphogenesis. Neuron 48:757–771

    PubMed  CAS  Google Scholar 

  104. Chua CE, Tang BL (2008) Syntaxin 16 is enriched in neuronal dendrites and may have a role in neurite outgrowth. Mol Membr Biol 25:35–45

    PubMed  CAS  Google Scholar 

  105. Yin DM, Huang YH, Zhu YB, Wang Y (2008) Both the establishment and maintenance of neuronal polarity require the activity of protein kinase D in the Golgi apparatus. J Neurosci 28:8832–8843

    PubMed  CAS  Google Scholar 

  106. Sytnyk V, Leshchyns’Ka I, Dityatev A, Schachner M (2004) Trans-Golgi network delivery of synaptic proteins in synaptogenesis. J Cell Sci 117:381–388

    PubMed  CAS  Google Scholar 

  107. Copp AJ (2005) Neurulation in the cranial region–normal and abnormal. J Anat 207:623–635

    PubMed  Google Scholar 

  108. Parsons JT, Churn SB, DeLorenzo RJ (1997) Ischemia-induced inhibition of calcium uptake into rat brain microsomes mediated by Mg2+/Ca2+ ATPase. J Neurochem 68:1124–1134

    PubMed  CAS  Google Scholar 

  109. Parsons JT, Churn SB, DeLorenzo RJ (1999) Global ischemia-induced inhibition of the coupling ratio of calcium uptake and ATP hydrolysis by rat whole brain microsomal Mg(2+)/Ca(2+) ATPase. Brain Res 834:32–41

    PubMed  CAS  Google Scholar 

  110. Pavlikova M, Tatarkova Z, Sivonova M, Kaplan P, Krizanova O, Lehotsky J (2009) Alterations induced by ischemic preconditioning on secretory pathways Ca2+-ATPase (SPCA) gene expression and oxidative damage after global cerebral ischemia/reperfusion in rats. Cell Mol Neurobiol 29:909–916

    PubMed  CAS  Google Scholar 

  111. Gonatas NK, Stieber A, Gonatas JO (2006) Fragmentation of the Golgi apparatus in neurodegenerative diseases and cell death. J Neurol Sci 246:21–30

    PubMed  CAS  Google Scholar 

  112. LaFerla FM (2002) Calcium dyshomeostasis and intracellular signalling in Alzheimer’s disease. Nat Rev Neurosci 3:862–872

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the Undergraduate Creative Program of Central South University (No. 081053358), the Education Expenditure of Hunan Province Provincial Finance Department (No. 2010163), and the Key Frontier Research Project of Central South University (from 2010 to 2011).

Conflict of interest

There are no conflicts of interest. All authors report no disclosures.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zhiping Hu.

Rights and permissions

Reprints and permissions

About this article

Cite this article

He, W., Hu, Z. The Role of the Golgi-Resident SPCA Ca2+/Mn2+ Pump in Ionic Homeostasis and Neural Function. Neurochem Res 37, 455–468 (2012). https://doi.org/10.1007/s11064-011-0644-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11064-011-0644-6

Keywords

Navigation