Endocrine aspects of organelle stress - cell non-autonomous signaling of mitochondria and the ER

Current Opinion in Cell Biology

Volumn 33, Issue , 2015, Pages 102-110

  Schinzel, Robert ^a   Dillin, Andrew ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ORGANELLE; CELL STRESS; ENDOCRINOLOGY; ENDOPLASMIC RETICULUM STRESS; HOMEOSTASIS; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE; ANIMAL; CYTOLOGY; ENDOPLASMIC RETICULUM; EUKARYOTIC CELL; HUMAN; LONGEVITY; METABOLISM;

EUKARYOTA;

ANIMALS; ENDOPLASMIC RETICULUM; EUKARYOTIC CELLS; HOMEOSTASIS; HUMANS; LONGEVITY; MITOCHONDRIA; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE;

EID: 84922459687     PISSN: 09550674     EISSN: 18790410     Source Type: Journal    
DOI: 10.1016/j.ceb.2015.01.006     Document Type: Review

References (117)

1. Lee J., Ozcan U. Unfolded protein response signaling and metabolic diseases. J Biol Chem 2014, 289:1203-1211.
2. Zhao L., Ackerman S.L. Endoplasmic reticulum stress in health and disease. Curr Opin Cell Biol 2006, 18:444-452.
3. Otsu M., Sitia R. Diseases originating from altered protein quality control in the endoplasmic reticulum. Curr Med Chem 2007, 14:1639-1652.
4. Wang S., Kaufman R.J. The impact of the unfolded protein response on human disease. J Cell Biol 2012, 197:857-867.
5. Powers E.T., et al. Biological and chemical approaches to diseases of proteostasis deficiency. Annu Rev Biochem 2009, 78:959-991.
6. Balch W.E., et al. Adapting proteostasis for disease intervention. Science 2008, 319:916-919.
7. Jovaisaite V., Mouchiroud L., Auwerx J. The mitochondrial unfolded protein response, a conserved stress response pathway with implications in health and disease. J Exp Biol 2014, 217(Pt 1):137-143.
8. Schumann W. Thermosensors in eubacteria: role and evolution. J Biosci 2007, 32:549-557.
9. Kultz D. Evolution of the cellular stress proteome: from monophyletic origin to ubiquitous function. J Exp Biol 2003, 206(Pt 18):3119-3124.
10. Hollien J. Evolution of the unfolded protein response. Biochim Biophys Acta 2013, 1833:2458-2463.
11. Akerfelt M., Morimoto R.I., Sistonen L. Heat shock factors: integrators of cell stress, development and lifespan. Nat Rev Mol Cell Biol 2010, 11:545-555.
12. Walter P., Ron D. The unfolded protein response: from stress pathway to homeostatic regulation. Science 2011, 334:1081-1086.
13. Haynes C.M., Ron D. The mitochondrial UPR - protecting organelle protein homeostasis. J Cell Sci 2010, 123(Pt 22):3849-3855.
14. Powers E.T., Balch W.E. Diversity in the origins of proteostasis networks - a driver for protein function in evolution. Nat Rev Mol Cell Biol 2013, 14:237-248.
15. Ron D., Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 2007, 8:519-529.
16. Pellegrino M.W., Nargund A.M., Haynes C.M. Signaling the mitochondrial unfolded protein response. Biochim Biophys Acta 2013, 1833:410-416.
17. Morley J.F., Morimoto R.I. Regulation of longevity in Caenorhabditis elegans by heat shock factor and molecular chaperones. Mol Biol Cell 2004, 15:657-664.
18. Kenyon C. The plasticity of aging: insights from long-lived mutants. Cell 2005, 120:449-460.
19. Taylor R.C., Dillin A. XBP-1 is a cell-nonautonomous regulator of stress resistance and longevity. Cell 2013, 153:1435-1447.
20. Jensen M.B., Jasper H. Mitochondrial proteostasis in the control of aging and longevity. Cell Metab 2014, 20:214-225.
21. Westendorp R.G., Kirkwood T.B. Human longevity at the cost of reproductive success. Nature 1998, 396:743-746.
22. Partridge L., Gems D., Withers D.J. Sex and death: what is the connection?. Cell 2005, 120:461-472.
23. Kirkwood T.B. Understanding the odd science of aging. Cell 2005, 120:437-447.
24. Durieux J., Wolff S., Dillin A. The cell-non-autonomous nature of electron transport chain-mediated longevity. Cell 2011, 144:79-91.
25. Prahlad V., Cornelius T., Morimoto R.I. Regulation of the cellular heat shock response in Caenorhabditis elegans by thermosensory neurons. Science 2008, 320:811-814.
26. Prahlad V., Morimoto R.I. Neuronal circuitry regulates the response of Caenorhabditis elegans to misfolded proteins. Proc Natl Acad Sci U S A 2011, 108:14204-14209.
27. Lee S.J., Kenyon C. Regulation of the longevity response to temperature by thermosensory neurons in Caenorhabditis elegans. Curr Biol 2009, 19:715-722.
28. van Oosten-Hawle P., Morimoto R.I. Transcellular chaperone signaling: an organismal strategy for integrated cell stress responses. J Exp Biol 2014, 217(Pt 1):129-136.
29. van Oosten-Hawle P., Morimoto R.I. Organismal proteostasis: role of cell-nonautonomous regulation and transcellular chaperone signaling. Genes Dev 2014, 28:1533-1543.
30. Braakman I., Bulleid N.J. Protein folding and modification in the mammalian endoplasmic reticulum. Annu Rev Biochem 2011, 80:71-99.
31. Ashby M.C., Tepikin A.V. ER calcium and the functions of intracellular organelles. Semin Cell Dev Biol 2001, 12:11-17.
32. Blom T., Somerharju P., Ikonen E. Synthesis and biosynthetic trafficking of membrane lipids. Cold Spring Harb Perspect Biol 2011, 3:a004713.
33. Rutkowski D.T., Hegde R.S. Regulation of basal cellular physiology by the homeostatic unfolded protein response. J Cell Biol 2010, 189:783-794.
34. Schroder M., Kaufman R.J. The mammalian unfolded protein response. Annu Rev Biochem 2005, 74:739-789.
35. Hetz C. The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat Rev Mol Cell Biol 2012, 13:89-102.
36. Park S.W., Ozcan U. Potential for therapeutic manipulation of the UPR in disease. Semin Immunopathol 2013, 35:351-373.
37. Kamimura D., Bevan M.J. Endoplasmic reticulum stress regulator XBP-1 contributes to effector CD8+ T cell differentiation during acute infection. J Immunol 2008, 181:5433-5441.
38. Richardson C.E., Kooistra T., Kim D.H. An essential role for XBP-1 in host protection against immune activation in C. elegans. Nature 2010, 463:1092-1095.
39. Reimold A.M., et al. Plasma cell differentiation requires the transcription factor XBP-1. Nature 2001, 412:300-307.
40. Iwakoshi N.N., et al. Plasma cell differentiation and the unfolded protein response intersect at the transcription factor XBP-1. Nat Immunol 2003, 4:321-329.
41. Souid S., Lepesant J.A., Yanicostas C. The xbp-1 gene is essential for development in Drosophila. Dev Genes Evol 2007, 217:159-167.
42. Reimold A.M., et al. An essential role in liver development for transcription factor XBP-1. Genes Dev 2000, 14:152-157.
43. Shen X., et al. Genetic interactions due to constitutive and inducible gene regulation mediated by the unfolded protein response in C. elegans. PLoS Genet 2005, 1:e37.
44. Harding H.P., et al. Diabetes mellitus and exocrine pancreatic dysfunction in perk-/- mice reveals a role for translational control in secretory cell survival. Mol Cell 2001, 7:1153-1163.
45. Gass J.N., et al. The unfolded protein response of B-lymphocytes: PERK-independent development of antibody-secreting cells. Mol Immunol 2008, 45:1035-1043.
46. Shaffer A.L., et al. XBP1, downstream of Blimp-1, expands the secretory apparatus and other organelles, and increases protein synthesis in plasma cell differentiation. Immunity 2004, 21:81-93.
47. Zhang P., et al. The PERK eukaryotic initiation factor 2 alpha kinase is required for the development of the skeletal system, postnatal growth, and the function and viability of the pancreas. Mol Cell Biol 2002, 22:3864-3874.
48. Wu J., et al. ATF6alpha optimizes long-term endoplasmic reticulum function to protect cells from chronic stress. Dev Cell 2007, 13:351-364.
49. Satpute-Krishnan P., et al. ER stress-induced clearance of misfolded GPI-anchored proteins via the secretory pathway. Cell 2014, 158:522-533.
50. Shoulders M.D., et al. Stress-independent activation of XBP1s and/or ATF6 reveals three functionally diverse ER proteostasis environments. Cell Rep 2013, 3:1279-1292.
51. Lee A.H., Iwakoshi N.N., Glimcher L.H. XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol Cell Biol 2003, 23:7448-7459.
52. Okada T., et al. Distinct roles of activating transcription factor 6 (ATF6) and double-stranded RNA-activated protein kinase-like endoplasmic reticulum kinase (PERK) in transcription during the mammalian unfolded protein response. Biochem J 2002, 366(Pt 2):585-594.
53. Hollien J., Weissman J.S. Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science 2006, 313:104-107.
54. Travers K.J., et al. Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 2000, 101:249-258.
55. Harding H.P., et al. Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol Cell 2000, 5:897-904.
56. Hegde R.S., Ploegh H.L. Quality and quantity control at the endoplasmic reticulum. Curr Opin Cell Biol 2010, 22:437-446.
57. Yamamoto K., et al. Differential contributions of ATF6 and XBP1 to the activation of endoplasmic reticulum stress-responsive cis-acting elements ERSE, UPRE and ERSE-II. J Biochem 2004, 136:343-350.
58. Yamamoto K., et al. Transcriptional induction of mammalian ER quality control proteins is mediated by single or combined action of ATF6alpha and XBP1. Dev Cell 2007, 13:365-376.
59. Ryno L.M., Wiseman R.L., Kelly J.W. Targeting unfolded protein response signaling pathways to ameliorate protein misfolding diseases. Curr Opin Chem Biol 2013, 17:346-352.
60. Henis-Korenblit S., et al. Insulin/IGF-1 signaling mutants reprogram ER stress response regulators to promote longevity. Proc Natl Acad Sci U S A 2010, 107:9730-9735.
61. Berlett B.S., Stadtman E.R. Protein oxidation in aging, disease, and oxidative stress. J Biol Chem 1997, 272:20313-20316.
62. Soskic V., Groebe K., Schrattenholz A. Nonenzymatic posttranslational protein modifications in ageing. Exp Gerontol 2008, 43:247-257.
63. David D.C., et al. Widespread protein aggregation as an inherent part of aging in C. elegans. PLoS Biol 2010, 8:e1000450.
64. Ben-Zvi A., Miller E.A., Morimoto R.I. Collapse of proteostasis represents an early molecular event in Caenorhabditis elegans aging. Proc Natl Acad Sci U S A 2009, 106:14914-14919.
65. Zinszner H., et al. CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev 1998, 12:982-995.
66. Lerner A.G., et al. IRE1alpha induces thioredoxin-interacting protein to activate the NLRP3 inflammasome and promote programmed cell death under irremediable ER stress. Cell Metab 2012, 16:250-264.
67. Upton J.P., et al. IRE1alpha cleaves select microRNAs during ER stress to derepress translation of proapoptotic caspase-2. Science 2012, 338:818-822.
68. Lin W., Popko B. Endoplasmic reticulum stress in disorders of myelinating cells. Nat Neurosci 2009, 12:379-385.
69. Han D., et al. IRE1alpha kinase activation modes control alternate endoribonuclease outputs to determine divergent cell fates. Cell 2009, 138:562-575.
70. Skalet A.H., et al. Rapid B cell receptor-induced unfolded protein response in nonsecretory B cells correlates with pro- versus antiapoptotic cell fate. J Biol Chem 2005, 280:39762-39771.
71. Woo C.W., et al. Adaptive suppression of the ATF4-CHOP branch of the unfolded protein response by Toll-like receptor signalling. Nat Cell Biol 2009, 11:1473-1480.
72. Sun J., et al. Neuronal GPCR controls innate immunity by regulating noncanonical unfolded protein response genes. Science 2011, 332:729-732.
73. Sun J., Liu Y., Aballay A. Organismal regulation of XBP-1-mediated unfolded protein response during development and immune activation. EMBO Rep 2012, 13:855-860.
74. Christis C., et al. Regulated increase in folding capacity prevents unfolded protein stress in the ER. J Cell Sci 2010, 123(Pt 5):787-794.
75. Mahadevan N.R., et al. Transmission of endoplasmic reticulum stress and pro-inflammation from tumor cells to myeloid cells. Proc Natl Acad Sci U S A 2011, 108:6561-6566.
76. Cullen S.J., Fatemie S., Ladiges W. Breast tumor cells primed by endoplasmic reticulum stress remodel macrophage phenotype. Am J Cancer Res 2013, 3:196-210.
77. Mahadevan N.R., et al. Cell-extrinsic effects of tumor ER stress imprint myeloid dendritic cells and impair CD8(+) T cell priming. PLoS ONE 2012, 7:e51845.
78. Taylor R.C., Berendzen K.M., Dillin A. Systemic stress signalling: understanding the cell non-autonomous control of proteostasis. Nat Rev Mol Cell Biol 2014, 15:211-217.
79. Madison J.M., Nurrish S., Kaplan J.M. UNC-13 interaction with syntaxin is required for synaptic transmission. Curr Biol 2005, 15:2236-2242.
80. Speese S., et al. UNC-31 (CAPS) is required for dense-core vesicle but not synaptic vesicle exocytosis in Caenorhabditis elegans. J Neurosci 2007, 27:6150-6162.
81. Williams K.W., et al. Xbp1s in Pomc neurons connects ER stress with energy balance and glucose homeostasis. Cell Metab 2014, 20:471-482.
82. Salway J.G. Metabolism at a Glance 1994, 95. Blackwell Scientific Publications, Oxford/Boston.
83. Dolezal P., et al. Evolution of the molecular machines for protein import into mitochondria. Science 2006, 313:314-318.
84. Allen J.F. Control of gene expression by redox potential and the requirement for chloroplast and mitochondrial genomes. J Theor Biol 1993, 165:609-631.
85. Allen J.F. The function of genomes in bioenergetic organelles. Philos Trans R Soc Lond B: Biol Sci 2003, 358:19-37. discussion 37-38.
86. Lane N., Martin W. The energetics of genome complexity. Nature 2010, 467:929-934.
87. Martinus R.D., et al. Selective induction of mitochondrial chaperones in response to loss of the mitochondrial genome. Eur J Biochem 1996, 240:98-103.
88. Zhao Q., et al. A mitochondrial specific stress response in mammalian cells. EMBO J 2002, 21:4411-4419.
89. Yoneda T., et al. Compartment-specific perturbation of protein handling activates genes encoding mitochondrial chaperones. J Cell Sci 2004, 117(Pt 18):4055-4066.
90. Benedetti C., et al. Ubiquitin-like protein 5 positively regulates chaperone gene expression in the mitochondrial unfolded protein response. Genetics 2006, 174:229-239.
91. Houtkooper R.H., et al. Mitonuclear protein imbalance as a conserved longevity mechanism. Nature 2013, 497:451-457.
92. Mouchiroud L., et al. The NAD(+)/sirtuin pathway modulates longevity through activation of mitochondrial UPR and FOXO signaling. Cell 2013, 154:430-441.
93. Melo J.A., Ruvkun G. Inactivation of conserved C. elegans genes engages pathogen- and xenobiotic-associated defenses. Cell 2012, 149:452-466.
94. Nargund A.M., et al. Mitochondrial import efficiency of ATFS-1 regulates mitochondrial UPR activation. Science 2012, 337:587-590.
95. Haynes C.M., et al. The matrix peptide exporter HAF-1 signals a mitochondrial UPR by activating the transcription factor ZC376.7 in C. elegans. Mol Cell 2010, 37:529-540.
96. Schleyer M., Schmidt B., Neupert W. Requirement of a membrane potential for the posttranslational transfer of proteins into mitochondria. Eur J Biochem 1982, 125:109-116.
97. Kornmann B. Quality control in mitochondria: use it, break it, fix it, trash it. F1000Prime Rep 2014, 6:15.
98. Martin J., Mahlke K., Pfanner N. Role of an energized inner membrane in mitochondrial protein import. Delta psi drives the movement of presequences. J Biol Chem 1991, 266:18051-18057.
99. Haynes C.M., et al. ClpP mediates activation of a mitochondrial unfolded protein response in C. elegans. Dev Cell 2007, 13:467-480.
100. Aldridge J.E., Horibe T., Hoogenraad N.J. Discovery of genes activated by the mitochondrial unfolded protein response (mtUPR) and cognate promoter elements. PLoS ONE 2007, 2:pe874.
101. Feng J., Bussiere F., Hekimi S. Mitochondrial electron transport is a key determinant of life span in Caenorhabditis elegans. Dev Cell 2001, 1:633-644.
102. Dillin A., et al. Rates of behavior and aging specified by mitochondrial function during development. Science 2002, 298:2398-2401.
103. Lee S.S., et al. A systematic RNAi screen identifies a critical role for mitochondria in C. elegans longevity. Nat Genet 2003, 33:40-48.
104. Copeland J.M., et al. Extension of Drosophila life span by RNAi of the mitochondrial respiratory chain. Curr Biol 2009, 19:1591-1598.
105. Liu X., et al. Evolutionary conservation of the clk-1-dependent mechanism of longevity: loss of mclk1 increases cellular fitness and lifespan in mice. Genes Dev 2005, 19:2424-2434.
106. Owusu-Ansah E., Song W., Perrimon N. Muscle mitohormesis promotes longevity via systemic repression of insulin signaling. Cell 2013, 155:699-712.
107. Barbour J.A., Turner N. Mitochondrial stress signaling promotes cellular adaptations. Int J Cell Biol 2014, 2014:p156020.
108. Lee C., Yen K., Cohen P. Humanin: a harbinger of mitochondrial-derived peptides?. Trends Endocrinol Metab 2013, 24:222-228.
109. Tajima H., et al. Evidence for in vivo production of humanin peptide, a neuroprotective factor against Alzheimer's disease-related insults. Neurosci Lett 2002, 324:227-231.
110. Yen K., et al. The emerging role of the mitochondrial-derived peptide humanin in stress resistance. J Mol Endocrinol 2013, 50:R11-R19.
111. Hashimoto Y., et al. Detailed characterization of neuroprotection by a rescue factor humanin against various Alzheimer's disease-relevant insults. J Neurosci 2001, 21:9235-9245.
112. Kim K.H., et al. Autophagy deficiency leads to protection from obesity and insulin resistance by inducing Fgf21 as a mitokine. Nat Med 2013, 19:83-92.
113. Tyynismaa H., et al. Mitochondrial myopathy induces a starvation-like response. Hum Mol Genet 2010, 19:3948-3958.
114. Suomalainen A., et al. FGF-21 as a biomarker for muscle-manifesting mitochondrial respiratory chain deficiencies: a diagnostic study. Lancet Neurol 2011, 10:806-818.
115. Fu S., et al. Aberrant lipid metabolism disrupts calcium homeostasis causing liver endoplasmic reticulum stress in obesity. Nature 2011, 473:528-531.
116. Ozcan U., et al. Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 2006, 313:1137-1140.
117. Shore G.C., Papa F.R., Oakes S.A. Signaling cell death from the endoplasmic reticulum stress response. Curr Opin Cell Biol 2011, 23:143-149.