Secretory pathway stress responses as possible mechanisms of disease involving Golgi Ca2+ pump dysfunction

BioFactors

Volumn 37, Issue 3, 2011, Pages 150-158

  Shull, Gary E ^a   Miller, Marian L ^a   Prasad, Vikram ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

Acantholysis; Cornification; Darier disease; Endoplasmic reticulum stress; Golgi stress; Secretory pathway stress; Unfolded protein response

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATASE (CALCIUM); PROTEIN SPCA1; PROTEIN SPCA2; UNCLASSIFIED DRUG;

ATP2C1 GENE; CELLULAR STRESS RESPONSE; DARIER DISEASE; ENDOPLASMIC RETICULUM STRESS; GENE; GENE MUTATION; GOLGI COMPLEX; HAPLOINSUFFICIENCY; HUMAN; MAMMAL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REVIEW; YEAST;

ANIMALS; CALCIUM; CALCIUM-TRANSPORTING ATPASES; DARIER DISEASE; ENDOPLASMIC RETICULUM; GOLGI APPARATUS; HUMANS; SECRETORY PATHWAY;

MAMMALIA; MUS;

EID: 79959497957     PISSN: 09516433     EISSN: 18728081     Source Type: Journal    
DOI: 10.1002/biof.141     Document Type: Review

References (113)

1. Brini, M. and Carafoli, E. (2009) Calcium pumps in health and disease. Physiol. Rev. 89, 1341-1378.
2. 2+ pumps: structural diversity as the basis for functional versatility. Biochem. Soc. Trans. 35, 919-922.
3. 2+-ATPase: design of a perfect chemi-osmotic pump. Q. Rev. Biophys. 1, 1-66.
4. 2+ ATPase pump expression and its relevance to cardiac muscle physiology and pathology. Cardiovasc. Res. 77, 265-273.
5. Hu, Z., Bonifas, J. M., Beech, J., Bench, G., Shigihara, T., Ogawa, H., Ikeda, S., Mauro, T., and Epstein, E. H. Jr. (2000) Mutations in ATP2C1, encoding a calcium pump, cause Hailey-Hailey disease. Nat. Genet. 24, 61-65.
6. 2+ pump. Hum. Mol. Genet. 9, 1131-1140.
7. 2+ pump, cause Darier disease. Nat. Genet. 21, 271-277.
8. 2+ pump. J. Biol. Chem. 276, 26737-26740.
9. 2+ pump, predisposes mice to squamous cell tumors via a novel mode of cancer susceptibility. Cancer Res. 65, 8655-8661.
10. 2+ ATPase 2 heterozygote mice keratinocytes. Prog. Biophys. Mol. Biol. 103, 81-87.
11. 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.
12. Wuytack, F., Raeymaekers, L., and Missiaen, L. (2002) Molecular physiology of the SERCA and SPCA pumps. Cell Calcium 32, 279-305.
13. 2+ pumps in the Golgi apparatus. Biochim. Biophys. Acta 1742, 103-112.
14. Missiaen, L., Raeymaekers, L., Dode, L., Vanoevelen, J., Van Baelen, K., Parys, J. B., Callewaert, G., De Smedt, H., Segaert, S., and Wuytack, F. (2004) SPCA1 pumps and Hailey-Hailey disease. Biochem. Biophys. Res. Commun. 322, 1204-1213.
15. Missiaen, L., Dode, L., Vanoevelen, J., Raeymaekers, L., and Wuytack, F. (2007) Calcium in the Golgi apparatus. Cell Calcium 41, 405-416.
16. Baumrucker, C. R. and Keenan, T. W. (1975) Membranes of mammary gland. X. Adenosine triphosphate dependent calcium accumulation by Golgi apparatus rich fractions from bovine mammary gland. Exp. Cell Res. 90, 253-260.
17. Neville, M. C., Selker, F., Semple, K., and Watters, C. (1981) ATP-dependent calcium transport by a Golgi-enriched membrane fraction from mouse mammary gland. J. Membr. Biol. 61, 97-105.
18. West, D. W. (1981) Energy-dependent calcium sequestration activity in a Golgi apparatus fraction derived from lactating rat mammary glands. Biochim. Biophys. Acta 673, 374-386.
19. 2+-dependent ATP hydrolysis by Golgi vesicles from lactating rat mammary glands. Biochem. J. 226, 741-748.
20. 2+-stimulated adenosine triphosphatase in Golgi-enriched membranes of lactating murine mammary tissue. Biochem. J. 224, 39-45.
21. 2+ ATPase family. Cell 58, 133-145.
22. Gunteski-Hamblin, A. M., Clarke, D. M., and Shull, G. E. (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.
23. Van Baelen, K., Vanoevelen, J., Missiaen, L., Raeymaekers, L., and 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.
24. 2+-ATPase, hSPCA2, has unusual properties and is expressed in the brain. J. Biol. Chem. 280, 11608-11614.
25. 2+ ions. J. Biol. Chem. 280, 22800-22808.
26. 2+ required for glycosylation, sorting, and endoplasmic reticulum-associated protein degradation. Mol. Biol. Cell. 9, 1149-1162.
27. 2+ stores. J. Invest. Dermatol. 121, 688-694.
28. 2+ accumulation in the Golgi apparatus of HeLa cells assessed via RNA-mediated interference. Biochem. Biophys. Res. Commun. 306, 430-436.
29. Faddy, H. M., Smart, C. E., Xu, R., Lee, G. Y., Kenny, P. A., Feng, M., Rao, R., Brown, M. A., Bissell, M. J., Roberts-Thomson, S. J., and Monteith, G. R. (2008) Localization of plasma membrane and secretory calcium pumps in the mammary gland. Biochem. Biophys. Res. Commun. 369, 977-981.
30. 2+-ATPases. Biochem. Biophys. Res. Commun. 378, 99-102.
31. 2+-transporting ATPase. J. Bacteriol. 176, 4430-4436.
32. Mills, R. F., Doherty, M. L., López-Marqués, R. L., Weimar, T., Dupree, P., Palmgren, M. G., Pittman, J. K., and Williams, L. E. (2008) ECA3, a Golgi-localized P2A-type ATPase, plays a crucial role in manganese nutrition in Arabidopsis. Plant Physiol. 146, 116-128.
33. 2+ store. Cell Calcium 35, 115-121.
34. Mandal, D., Woolf, T. B., and 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.
35. 2+-ATPase (SERCA) 1 isoforms by steady-state and transient kinetic analyses. J. Biol. Chem. 280, 39124-39134.
36. 2+-ATPase (SPCA) 1 and 2 isoenzymes by steady-state and transient kinetic analyses. J. Biol. Chem. 281, 3182-3189.
37. 2+ homeostasis of the trans-Golgi compartment. Proc. Natl. Acad. Sci. USA 107, 9198-9203.
38. 2+-ATPase homologue, PMR1, is required for normal Golgi function and localizes in a novel Golgi-like distribution. Mol. Biol. Cell. 3, 633-654.
39. Lapinskas, P. J., Cunningham, K. W., Liu, X. F., Fink, G. R., and Culotta, V. C. (1995) Mutations in PMR1 suppress oxidative damage in yeast cells lacking superoxide dismutase. Mol. Cell. Biol. 15, 1382-1388.
40. 2+ pump and intracellular membrane trafficking. Traffic 11, 1315-1333.
41. Ramos-Castañeda, J., Park, Y. N., Liu, M., Hauser, K., Rudolph, H., Shull, G. E., Jonkman, M. F., Mori, K., Ikeda, S., Ogawa, H., and 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.
42. 2+ homeostasis in the Golgi and disturbs neural polarity. J. Neurosci. 29, 12174-12182.
43. Varki, A. (1998) Factors controlling the glycosylation potential of the Golgi apparatus. Trends Cell Biol. 8, 34-40.
44. 2+-ATPase SPCA1. Cell Calcium 34, 157-162.
45. i signals in human spermatozoa. J. Cell Sci. 118, 1673-1685.
46. 2+ response and cell viability in Darier disease. J. Cell Sci. 119, 671-679.
47. 2+ ATPase 1 (SPCA1) in A7r5 vascular smooth muscle cells cultured at different glucose concentrations. Biosci. Rep. 29, 397-404.
48. 2+ signaling during chemokinesis of human neutrophil granulocytes. Biochim. Biophys. Acta 1793, 1041-1049.
49. 2+ from the Golgi apparatus. Exp. Cell Res. 316, 2071-2086.
50. Copp, A. J. (1995) Death before birth: clues from gene knockouts and mutations. Trends Genet. 11, 87-93.
51. Ybot-Gonzalez, P., Cogram, P., Gerrelli, D., and Copp, A. J. (2002) Sonic hedgehog and the molecular regulation of mouse neural tube closure. Development 129, 2507-2517.
52. Copp, A. J. (2005) Neurulation in the cranial region-normal and abnormal. J. Anat. 207, 623-635.
53. Dolman, N. J. and Tepikin, A. V. (2006) Calcium gradients and the Golgi. Cell Calcium 40, 505-512.
54. 2+ release. J. Biol. Chem. 268, 23601-23610.
55. Marutani, T., Yamamoto, A., Nagai, N., Kubota, H., and Nagata, K. (2004) Accumulation of type IV collagen in dilated ER leads to apoptosis in Hsp47-knockout mouse embryos via induction of CHOP. J. Cell Sci. 117, 5913-5922.
56. Schröder, M. and Kaufman, R. J. (2005) The mammalian unfolded protein response. Annu. Rev. Biochem. 74, 739-789.
57. Yamamoto, K., Takahara, K., Oyadomari, S., Okada, T., Sato, T., Harada, A., and Mori, K. (2010) Induction of liver steatosis and lipid droplet formation in ATF6α-knockout mice burdened with pharmacological endoplasmic reticulum stress. Mol. Biol. Cell. 21, 2975-2986.
58. Orsó, E., Broccardo, C., Kaminski, W. E., Böttcher, A., Liebisch, G., Drobnik, W., Götz, A., Chambenoit, O., Diederich, W., Langmann, T., Spruss, T., Luciani, M. F., Rothe, G., Lackner, K. J., Chimini, G., and Schmitz, G. (2000) Transport of lipids from golgi to plasma membrane is defective in tangier disease patients and Abc1-deficient mice. Nat. Genet. 24, 192-196.
59. Hicks, S. W. and Machamer, C. E. (2005) Golgi structure in stress sensing and apoptosis. Biochim. Biophys. Acta 1744, 406-414.
60. Yoshida, H. (2009) ER stress response, peroxisome proliferation, mitochondrial unfolded protein response and Golgi stress response. IUBMB Life 61, 871-879.
61. Federovitch, C. M., Ron, D., and Hampton, R. Y. (2005) The dynamic ER: experimental approaches and current questions. Curr. Opin. Cell Biol. 17, 409-414.
62. Sriburi, R., Bommiasamy, H., Buldak, G. L., Robbins, G. R., Frank, M., Jackowski, S., and Brewer, J. W. (2007) Coordinate regulation of phospholipid biosynthesis and secretory pathway gene expression in XBP-1(S)-induced endoplasmic reticulum biogenesis. J. Biol. Chem. 282, 7024-7034.
63. Sriburi, R., Jackowski, S., Mori, K., and Brewer, J. W. (2004) XBP1: a link between the unfolded protein response, lipid biosynthesis, and biogenesis of the endoplasmic reticulum. J. Cell Biol. 167, 35-41.
64. Tigges, M. and Fussenegger, M. (2006) Xbp1-based engineering of secretory capacity enhances the productivity of Chinese hamster ovary cells. Metab. Eng. 8, 264-272.
65. Foggia, L. and Hovnanian, A. (2004) Calcium pump disorders of the skin. Am. J. Med. Genet. C Semin. Med. Genet. 131C, 20-31.
66. Dhitavat, J., Fairclough, R. J., Hovnanian, A., and Burge, S. M. (2004) Calcium pumps and keratinocytes: lessons from Darier's disease and Hailey-Hailey disease. Br. J. Dermatol. 150, 821-828.
67. Hovnanian, A. (2004) Darier's disease: from dyskeratosis to endoplasmic reticulum calcium ATPase deficiency. Biochem. Biophys. Res. Commun. 322, 1237-1244.
68. Szigeti, R. and Kellermayer, R. (2006) Autosomal-dominant calcium ATPase disorders. J. Invest. Dermatol. 126, 2370-2376.
69. Wilgram, G. F., Caulfield, J. B., and Lever, W. F. (1962) An electron-microscopic study of acantholysis and dyskeratosis in Hailey and Hailey's disease. J. Invest. Dermatol. 39, 373-381.
70. Caulfield, J. B and Wilgram, G. F. (1963) An electron-microscope study of dyskeratosis and acantholysis in Darier's disease. J. Invest. Dermatol. 41, 57-65.
71. Wilgram, G. F. and Weinstock, A. (1966) Advances in genetic dermatology. Dyskeratosis, acantholysis, and hyperkeratosis, with a note on the specific role of desmosomes and keratinosomes in the formation of the horny layer. Arch. Dermatol. 94, 456-479.
72. Gottlieb, S. K. and Lutzner, M. A. (1970) Hailey-Hailey disease-an electron microscopic study. J. Invest. Dermatol. 54, 368-376.
73. Gottlieb, S. K. and Lutzner, M. A. (1973) Darier's disease. An electron microscopic study. Arch. Dermatol. 107, 225-230.
74. Hashimoto, K., Fujiwara, K., Tada, J., Harada, M., Setoyama, M., and Eto, H. (1995) Desmosomal dissolution in Grover's disease, Hailey-Hailey's disease and Darier's disease. J. Cutan. Pathol. 22, 488-501.
75. Burge, S. M and Schomberg, K. H. (1992) Adhesion molecules and related proteins in Darier's disease and Hailey-Hailey disease. Br. J. Dermatol. 127, 335-343.
76. Metze, D., Hamm, H., Schorat, A., and Luger, T. (1996) Involvement of the adherens junction-actin filament system in acantholytic dyskeratosis of Hailey-Hailey disease. A histological, ultrastructural, and histochemical study of lesional and non-lesional skin. J. Cutan. Pathol. 23, 211-222.
77. von Felbert, V., Hampl, M., Talhari, C., Engers, R., and Megahed, M. (2010) Squamous cell carcinoma arising from a localized vulval lesion of Hailey-Hailey disease after tacrolimus therapy. Am. J. Obstet. Gynecol. 203, e5-7.
78. Matsui, K., Makino, T., Nakano, H., Furuichi, M., Sawamura, D., and Shimizu, T. (2009) Squamous cell carcinoma arising from Darier's disease. Clin. Exp. Dermatol. 34, e1015-1016.
79. 2+ ATPase type 2 downregulated in human oral squamous cell carcinoma. Int. J. Cancer 110, 225-231.
80. 2+/serum induction and UVB radiation in Hailey-Hailey keratinocytes. J. Invest. Dermatol. 114, 1058-1061.
81. Onozuka, T., Sawamura, D., Goto, M., Yokota, K., and Shimizu, H. (2006) Possible role of endoplasmic reticulum stress in the pathogenesis of Darier's disease. J. Dermatol. Sci. 41, 217-220.
82. Marciniak, S. J. and Ron, D. (2006) Endoplasmic reticulum stress signaling in disease. Physiol. Rev. 86, 1133-1149.
83. Kim, I., Xu, W., and Reed, J. C. (2008) Cell death and endoplasmic reticulum stress: disease relevance and therapeutic opportunities. Nat. Rev. Drug Discov. 7, 1013-1030.
84. Hosoi, T. and Ozawa, K. (2010) Endoplasmic reticulum stress in disease: mechanisms and therapeutic opportunities. Clin. Sci. (Lond). 118, 19-29.
85. Salminen, A., Kauppinen, A., Suuronen, T., Kaarniranta, K., and Ojala, J. (2009) ER stress in Alzheimer's disease: a novel neuronal trigger for inflammation and Alzheimer's pathology. J. Neuroinflammation 6, 41. DOI: 10.1186/1742-2094-6-41.
86. Nassif, M., Matus, S., Castillo, K., and Hetz, C. (2010) Amyotrophic lateral sclerosis pathogenesis: a journey through the secretory pathway. Antioxid. Redox Signal. 13, 1955-1989.
87. Minamino, T. and Kitakaze, M. (2010) ER stress in cardiovascular disease. J. Mol. Cell. Cardiol. 48, 1105-1110.
88. Tabas, I. (2010) The role of endoplasmic reticulum stress in the progression of atherosclerosis. Circ. Res. 107, 839-850.
89. Thomas, S. E., Dalton, L. E., Daly, M. L., Malzer, E., Marciniak, S. J. (2010) Diabetes as a disease of endoplasmic reticulum stress. Diabetes Metab. Res. Rev. 26, 611-621.
90. Ozcan, L., Ergin, A. S., Lu, A., Chung, J., Sarkar, S., Nie, D., Myers, M. G. Jr, and Ozcan, U. (2009) Endoplasmic reticulum stress plays a central role in development of leptin resistance. Cell Metab. 9, 35-51.
91. McGuckin, M. A., Eri, R. D., Das, I., Lourie, R., and Florin, T. H. (2010) ER stress and the unfolded protein response in intestinal inflammation. Am. J. Physiol. Gastrointest. Liver Physiol. 298, G820-G832.
92. Dickhout, J. G. and Krepinsky, J. C. (2009) Endoplasmic reticulum stress and renal disease. Antioxid. Redox Signal. 11, 2341-2352.
93. Malhotra, D., Thimmulappa, R., Vij, N., Navas-Acien, A., Sussan, T., Merali, S., Zhang, L., Kelsen, S. G., Myers, A., Wise, R., Tuder, R., and Biswal, S. (2009) Heightened endoplasmic reticulum stress in the lungs of patients with chronic obstructive pulmonary disease: the role of Nrf2-regulated proteasomal activity. Am. J. Respir. Crit. Care Med. 180, 1196-1207.
94. Henriques-Pons, A. and Nagaraju, K. (2009) Nonimmune mechanisms of muscle damage in myositis: role of the endoplasmic reticulum stress response and autophagy in the disease pathogenesis. Curr. Opin. Rheumatol. 21, 581-587.
95. Ma, Y. and Hendershot, L. M. (2004) The role of the unfolded protein response in tumour development: friend or foe? Nat. Rev. Cancer. 4, 966-977.
96. Healy, S. J., Gorman, A. M., Mousavi-Shafaei, P., Gupta, S., and Samali, A. (2009) Targeting the endoplasmic reticulum-stress response as an anticancer strategy. Eur. J. Pharmacol. 625, 234-246.
97. Rutkowski, D. T. and Kaufman, R. J. (2007) That which does not kill me makes me stronger: adapting to chronic ER stress. Trends Biochem. Sci. 32, 469-476.
98. Rutkowski, D. T., Arnold, S. M., Miller, C. N., Wu, J., Li, J., Gunnison, K. M., Mori, K., Sadighi Akha, A. A., Raden, D., and Kaufman, R. J. (2006) Adaptation to ER stress is mediated by differential stabilities of pro-survival and pro-apoptotic mRNAs and proteins. PLoS Biol. 4, e374. DOI: 10.1371/journal.pbio.0040374.
99. Maag, R. S., Hicks, S. W., and Machamer, C. E. (2003) Death from within: apoptosis and the secretory pathway. Curr. Opin. Cell Biol. 15, 456-461.
100. Wlodkowic, D., Skommer, J., McGuinness, D., Hillier, C., and Darzynkiewicz, Z. (2009) ER-Golgi network-a future target for anti-cancer therapy. Leuk. Res. 33, 1440-1447.
101. Candi, E., Schmidt, R., and Melino, G. (2005) The cornified envelope: a model of cell death in the skin. Nat. Rev. Mol. Cell Biol. 6, 328-340.
102. Raj, D., Brash, D. E., and Grossman, D. (2006) Keratinocyte apoptosis in epidermal development and disease. J. Invest. Dermatol. 126, 243-257.
103. Lippens, S., Hoste, E., Vandenabeele, P., Agostinis, P., and Declercq, W. (2009) Cell death in the skin. Apoptosis 14, 549-569.
104. Lee, A. H., Chu, G. C., Iwakoshi, N. N., Glimcher, L. H. (2005) XBP-1 is required for biogenesis of cellular secretory machinery of exocrine glands. EMBO J. 24, 4368-4380.
105. Ma, Y., Shimizu, Y., Mann, M. J., Jin, Y., and Hendershot, L. M. (2010) Plasma cell differentiation initiates a limited ER stress response by specifically suppressing the PERK-dependent branch of the unfolded protein response. Cell Stress Chaperones 15, 281-293.
106. Firtina, Z. and Duncan, M. K. (2010) Unfolded protein response (UPR) is activated during normal lens development. Gene Expr. Patterns, in press.
107. Sugiura, K., Muro, Y., Futamura, K., Matsumoto, K., Hashimoto, N., Nishizawa, Y., Nagasaka, T., Saito, H., Tomita, Y., and Usukura, J. (2009) The unfolded protein response is activated in differentiating epidermal keratinocytes. J. Invest. Dermatol. 129, 2126-2135.
108. Weil, M., Raff, M. C., and Braga, V. M. (1999) Caspase activation in the terminal differentiation of human epidermal keratinocytes. Curr. Biol. 9, 361-364.
109. Chaturvedi, V., Sitailo, L. A., Bodner, B., Denning, M. F., and Nickoloff, B. J. (2006) Defining the caspase-containing apoptotic machinery contributing to cornification in human epidermal equivalents. Exp. Dermatol. 15, 14-22.
110. Weiske, J., Schöneberg, T., Schröder, W., Hatzfeld, M., Tauber, R., and Huber, O. (2001) The fate of desmosomal proteins in apoptotic cells. J. Biol. Chem. 276, 41175-41181.
111. Aho, S. (2004) Plakin proteins are coordinately cleaved during apoptosis but preferentially through the action of different caspases. Exp. Dermatol. 13, 700-707.
112. Gniadecki, R., Jemec, G. B., Thomsen, B. M., and Hansen, M. (1998) Relationship between keratinocyte adhesion and death: anoikis in acantholytic diseases. Arch. Dermatol Res. 290, 528-532.
113. Pasmatzi, E., Badavanis, G., Monastirli, A., and Tsambaos, D. (2007) Reduced expression of the antiapoptotic proteins of Bcl-2 gene family in the lesional epidermis of patients with Darier's disease. J. Cutan. Pathol. 34, 234-238.