The Endoplasmic Reticulum and the Cellular Reticular Network

  • Luis B. Agellon
  • Marek Michalak
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 981)


The endoplasmic reticulum and the other organelles of the eukaryotic cell are membrane-bound structures that carry out specialized functions. In this chapter, we discuss strategies that the cell has adopted to link and coordinate the different activities occurring within its various organelles as the cell carries out its physiological role.


Calcium signaling Cell stress Cellular reticular network Homeostasis Membrane contact sites 



activating transcription factor 6


immunoglobulin binding protein


endoplasmic reticulum


ER-associated degradation


ER-mitochondria encounter structure


glucose regulated protein


heat shock protein




serine/threonine-protein kinase/endoribonuclease inositol-requiring enzyme


Ca2+ release-activated Ca2+ channel


dsRNA-activated protein kinase-like ER kinase


protein disulfide isomerase


rough ER


SOCE-associated regulatory factor


SREBP cleavage activating protein


smooth ER


sarcoplasmic/endoplasmic reticulum Ca2+-ATPase


store-operated Ca2+ entry


sarcoplasmic reticulum


sterol-response element-binding protein


stromal-interacting molecule


ryanodine receptor


unfolded protein response


X-box binding protein 1



Research in our laboratories is supported by grants from the Canadian Institutes of Health Research grants MOP-15291, MOP-15415, MOP-86750 and PS-153325.

Conflict of Interest

The authors declare no conflict of interest.


  1. 1.
    Hebert DN, Molinari M (2007) In and out of the ER: protein folding, quality control, degradation, and related human diseases. Physiol Rev 87:1377–1408CrossRefPubMedGoogle Scholar
  2. 2.
    Krebs J, Agellon LB, Michalak M (2015) Ca2+ homeostasis and endoplasmic reticulum (ER) stress: an integrated view of calcium signaling. Biochem Biophys Res Commun 460:114–121CrossRefPubMedGoogle Scholar
  3. 3.
    McCaffrey K, Braakman I (2016) Protein quality control at the endoplasmic reticulum. Essays Biochem 60:227–235CrossRefPubMedGoogle Scholar
  4. 4.
    Coe H, Michalak M (2009) Calcium binding chaperones of the endoplasmic reticulum. Gen Physiol Biophys 28 Spec No Focus:F96–F103Google Scholar
  5. 5.
    Bose D, Chakrabarti A (2017) Substrate specificity in the context of molecular chaperones. IUBMB Life 69(9):647–659CrossRefPubMedGoogle Scholar
  6. 6.
    Horowitz S, Koldewey P, Stull F, Bardwell JC (2017) Folding while bound to chaperones. Curr Opin Struct Biol 48:1–5CrossRefPubMedGoogle Scholar
  7. 7.
    Caramelo JJ, Parodi AJ (2015) A sweet code for glycoprotein folding. FEBS Lett 589:3379–3387CrossRefPubMedGoogle Scholar
  8. 8.
    Baiceanu A, Mesdom P, Lagouge M, Foufelle F (2016) Endoplasmic reticulum proteostasis in hepatic steatosis. Nat Rev Endocrinol 12:710–722CrossRefPubMedGoogle Scholar
  9. 9.
    Horton JD, Goldstein JL, Brown MS (2002) SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver. J Clin Invest 109:1125–1131CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Vincenz-Donnelly L, Hipp MS (2017) The endoplasmic reticulum: a hub of protein quality control in health and disease. Free Radic Biol Med 108:383–393CrossRefPubMedGoogle Scholar
  11. 11.
    Volpi VG, Touvier T, D’Antonio M (2016) Endoplasmic reticulum protein quality control failure in myelin disorders. Front Mol Neurosci 9:162PubMedGoogle Scholar
  12. 12.
    Berridge MJ (2016) The inositol trisphosphate/calcium signaling pathway in health and disease. Physiol Rev 96:1261–1296CrossRefPubMedGoogle Scholar
  13. 13.
    Soboloff J, Rothberg BS, Madesh M, Gill DL (2012) STIM proteins: dynamic calcium signal transducers. Nat Rev Mol Cell Biol 13:549–565CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Groenendyk J, Agellon LB, Michalak M (2013) Coping with endoplasmic reticulum stress in the cardiovascular system. Annu Rev Physiol 75:49–67CrossRefPubMedGoogle Scholar
  15. 15.
    Hetz C, Chevet E, Oakes SA (2015) Proteostasis control by the unfolded protein response. Nat Cell Biol 17:829–838CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    D’Amico D, Sorrentino V, Auwerx J (2017) Cytosolic proteostasis networks of the mitochondrial stress response. Trends Biochem Sci 42(9):712–725CrossRefPubMedGoogle Scholar
  17. 17.
    Dicks N, Gutierrez K, Michalak M, Bordignon V, Agellon LB (2015) Endoplasmic reticulum stress, genome damage, and cancer. Front Oncol 5:11CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Jovaisaite V, Auwerx J (2015) The mitochondrial unfolded protein response-synchronizing genomes. Curr Opin Cell Biol 33:74–81CrossRefPubMedGoogle Scholar
  19. 19.
    Stepien KM, Heaton R, Rankin S, Murphy A, Bentley J, Sexton D, Hargreaves IP (2017) Evidence of oxidative stress and secondary mitochondrial dysfunction in metabolic and non-metabolic disorders. J Clin Med 6(7):E71CrossRefPubMedGoogle Scholar
  20. 20.
    Szymanski J, Janikiewicz J, Michalska B, Patalas-Krawczyk P, Perrone M, Ziolkowski W, Duszynski J, Pinton P, Dobrzyn A, Wieckowski MR (2017) Interaction of mitochondria with the endoplasmic reticulum and plasma membrane in calcium homeostasis, lipid trafficking and mitochondrial structure. Int J Mol Sci 18(7):E1576CrossRefPubMedGoogle Scholar
  21. 21.
    Baumann O, Walz B (2001) Endoplasmic reticulum of animal cells and its organization into structural and functional domains. Int Rev Cytol 205:149–214CrossRefPubMedGoogle Scholar
  22. 22.
    Corbett EF, Michalak M (2000) Calcium, a signaling molecule in the endoplasmic reticulum? Trends Biochem Sci 25:307–311CrossRefPubMedGoogle Scholar
  23. 23.
    High S, Lecomte FJ, Russell SJ, Abell BM, Oliver JD (2000) Glycoprotein folding in the endoplasmic reticulum: a tale of three chaperones? FEBS Lett 476:38–41CrossRefPubMedGoogle Scholar
  24. 24.
    Jakob CA, Chevet E, Thomas DY, Bergeron JJ (2001) Lectins of the ER quality control machinery. Results Probl Cell Differ 33:1–17CrossRefPubMedGoogle Scholar
  25. 25.
    Molinari M, Helenius A (2000) Chaperone selection during glycoprotein translocation into the endoplasmic reticulum. Science 288:331–333CrossRefPubMedGoogle Scholar
  26. 26.
    Nakamura K, Zuppini A, Arnaudeau S, Lynch J, Ahsan I, Krause R, Papp S, De Smedt H, Parys JB, Müller-Esterl W, Lew DP, Krause K-H, Demaurex N, Opas M, Michalak M (2001) Functional specialization of calreticulin domains. J Cell Biol 154:961–972CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Lievremont JP, Rizzuto R, Hendershot L, Meldolesi J (1997) BiP, a major chaperone protein of the endoplasmic reticulum lumen, plays a direct and important role in the storage of the rapidly exchanging pool of Ca2+. J Biol Chem 272:30873–33089CrossRefPubMedGoogle Scholar
  28. 28.
    Van PN, Peter F, Soling H-D (1989) Four intracisternal calcium-binding glycoproteins from rat liver microsomes with high affinity for calcium. No indication for calsequestrin-like proteins in inositol 1,4,5-trisphosphate-sensitive calcium sequestering rat liver vesicles. J Biol Chem 264:17494–17501PubMedGoogle Scholar
  29. 29.
    Waser M, Mesaeli N, Spencer C, Michalak M (1997) Regulation of calreticulin gene expression by calcium. J Cell Biol 138:547–557CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Lebeche D, Lucero HA, Kaminer B (1994) Calcium binding properties of rabbit liver protein disulfide isomerase. Biochem Biophys Res Commun 202:556–561CrossRefPubMedGoogle Scholar
  31. 31.
    Lucero HA, Kaminer B (1999) The role of calcium on the activity of ERcalcistorin/protein-disulfide isomerase and the significance of the C-terminal and its calcium binding. A comparison with mammalian protein-disulfide isomerase. J Biol Chem 274:3243–3251CrossRefPubMedGoogle Scholar
  32. 32.
    Lucero HA, Lebeche D, Kaminer B (1998) ERcalcistorin/protein-disulfide isomerase acts as a calcium storage protein in the endoplasmic reticulum of a living cell. Comparison with calreticulin and calsequestrin. J Biol Chem 273:9857–9863CrossRefPubMedGoogle Scholar
  33. 33.
    Faggioni M, Knollmann BC (2012) Calsequestrin 2 and arrhythmias. Am J Physiol Heart Circ Physiol 302:H1250–H1260CrossRefPubMedGoogle Scholar
  34. 34.
    Lee D, Michalak M (2010) Membrane associated Ca2+ buffers in the heart. BMB Rep 43:151–157CrossRefPubMedGoogle Scholar
  35. 35.
    Bhardwaj R, Hediger MA, Demaurex N (2016) Redox modulation of STIM-ORAI signaling. Cell Calcium 60:142–152CrossRefPubMedGoogle Scholar
  36. 36.
    Saheki Y, De Camilli P (2017) Endoplasmic reticulum-plasma membrane contact sites. Annu Rev Biochem 86:659–684CrossRefPubMedGoogle Scholar
  37. 37.
    Zhou Y, Cai X, Nwokonko RM, Loktionova NA, Wang Y, Gill DL (2017) The STIM-Orai coupling interface and gating of the Orai1 channel. Cell Calcium 63:8–13CrossRefPubMedGoogle Scholar
  38. 38.
    Takemura H, Putney JW Jr (1989) Capacitative calcium entry in parotid acinar cells. Biochem J 258:409–412CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Delpire E (2016) STIM and Orai proteins in calcium signaling: an AJP-cell physiology series of themed reviews. Am J Physiol Cell Physiol 310:C401CrossRefPubMedGoogle Scholar
  40. 40.
    Tanwar J, Motiani RK (2017) Role of SOCE architects STIM and Orai proteins in cell death. Cell Calcium
  41. 41.
    Brandman O, Liou J, Park WS, Meyer T (2007) STIM2 is a feedback regulator that stabilizes basal cytosolic and endoplasmic reticulum Ca2+ levels. Cell 131:1327–1339CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Kawasaki H, Kretsinger RH (2017) Structural and functional diversity of EF-hand proteins: Evolutionary perspectives. Protein Sci 26(10):1898–1920CrossRefPubMedGoogle Scholar
  43. 43.
    Hou X, Pedi L, Diver MM, Long SB (2012) Crystal structure of the calcium release-activated calcium channel Orai. Science 338:1308–1313CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    DeHaven WI, Smyth JT, Boyles RR, Putney JW Jr (2007) Calcium inhibition and calcium potentiation of Orai1, Orai2, and Orai3 calcium release-activated calcium channels. J Biol Chem 282:17548–17556CrossRefPubMedGoogle Scholar
  45. 45.
    Gonzalez-Cobos JC, Zhang X, Zhang W, Ruhle B, Motiani RK, Schindl R, Muik M, Spinelli AM, Bisaillon JM, Shinde AV, Fahrner M, Singer HA, Matrougui K, Barroso M, Romanin C, Trebak M (2013) Store-independent Orai1/3 channels activated by intracrine leukotriene C4: role in neointimal hyperplasia. Circ Res 112:1013–1025CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Thompson JL, Shuttleworth TJ (2013) Exploring the unique features of the ARC channel, a store-independent Orai channel. Channels (Austin) 7:364–373CrossRefGoogle Scholar
  47. 47.
    Zhang W, Zhang X, Gonzalez-Cobos JC, Stolwijk JA, Matrougui K, Trebak M (2015) Leukotriene-C4 synthase, a critical enzyme in the activation of store-independent Orai1/Orai3 channels, is required for neointimal hyperplasia. J Biol Chem 290:5015–5027CrossRefPubMedGoogle Scholar
  48. 48.
    Prins D, Groenendyk J, Touret N, Michalak M (2011) Modulation of STIM1 and capacitative Ca2+ entry by the endoplasmic reticulum luminal oxidoreductase ERp57. EMBO Rep 12:1182–1188CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Li Y, Camacho P (2004) Ca2+-dependent redox modulation of SERCA 2b by ERp57. J Cell Biol 164:35–46CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Ellgaard L, McCaul N, Chatsisvili A, Braakman I (2016) Co- and post-translational protein folding in the ER. Traffic 17:615–638CrossRefPubMedGoogle Scholar
  51. 51.
    Jung J, Michalak M, Agellon LB (2017) Endoplasmic reticulum malfunction in the nervous system. Front Neurosci 11:220CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Balchin D, Hayer-Hartl M, Hartl FU (2016) In vivo aspects of protein folding and quality control. Science 353:aac4354CrossRefPubMedGoogle Scholar
  53. 53.
    Bernasconi R, Molinari M (2011) ERAD and ERAD tuning: disposal of cargo and of ERAD regulators from the mammalian ER. Curr Opin Cell Biol 23:176–183CrossRefPubMedGoogle Scholar
  54. 54.
    Qi L, Tsai B, Arvan P (2017) New insights into the physiological role of endoplasmic reticulum-associated degradation. Trends Cell Biol 27:430–440CrossRefPubMedGoogle Scholar
  55. 55.
    Grek C, Townsend DM (2014) Protein disulfide isomerase superfamily in disease and the regulation of apoptosis. Endoplasmic Reticul Stress Dis 1:4–17Google Scholar
  56. 56.
    Parakh S, Atkin JD (2015) Novel roles for protein disulphide isomerase in disease states: a double edged sword? Front Cell Dev Biol 3:30CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Trombetta ES, Parodi AJ (2003) Quality control and protein folding in the secretory pathway. Annu Rev Cell Dev Biol 19:649–676CrossRefPubMedGoogle Scholar
  58. 58.
    Carafoli E, Krebs J (2016) Why calcium? How calcium became the best communicator. J Biol Chem 291:20849–20857CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Gidalevitz T, Prahlad V, Morimoto RI (2011) The stress of protein misfolding: from single cells to multicellular organisms. Cold Spring Harb Perspect Biol 3(6):a009704CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Wang M, Kaufman RJ (2014) The impact of the endoplasmic reticulum protein-folding environment on cancer development. Nat Rev Cancer 14:581–597CrossRefPubMedGoogle Scholar
  61. 61.
    Nakka VP, Prakash-babu P, Vemuganti R (2016) Crosstalk between endoplasmic reticulum stress, oxidative stress, and autophagy: potential therapeutic targets for acute CNS injuries. Mol Neurobiol 53:532–544CrossRefPubMedGoogle Scholar
  62. 62.
    Zhang C, Syed TW, Liu R, Yu J (2017) Role of endoplasmic reticulum stress, autophagy, and inflammation in cardiovascular disease. Front Cardiovasc Med 4:29CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Kaur J, Debnath J (2015) Autophagy at the crossroads of catabolism and anabolism. Nat Rev Mol Cell Biol 16:461–472CrossRefPubMedGoogle Scholar
  64. 64.
    Groenendyk J, Peng Z, Dudek E, Fan X, Mizianty MJ, Dufey E, Urra H, Sepulveda D, Rojas-Rivera D, Lim Y, Kim do H, Baretta K, Srikanth S, Gwack Y, Ahnn J, Kaufman RJ, Lee SK, Hetz C, Kurgan L, Michalak M (2014) Interplay between the oxidoreductase PDIA6 and microRNA-322 controls the response to disrupted endoplasmic reticulum calcium homeostasis. Sci Signal 7:ra54CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Leung AK, Sharp PA (2010) MicroRNA functions in stress responses. Mol Cell 40:205–215CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Hong M, Luo S, Baumeister P, Huang JM, Gogia RK, Li M, Lee AS (2004) Underglycosylation of ATF6 as a novel sensing mechanism for activation of the unfolded protein response. J Biol Chem 279:11354–11363CrossRefPubMedGoogle Scholar
  67. 67.
    Higa A, Taouji S, Lhomond S, Jensen D, Fernandez-Zapico ME, Simpson JC, Pasquet JM, Schekman R, Chevet E (2014) Endoplasmic reticulum stress-activated transcription factor ATF6alpha requires the disulfide isomerase PDIA5 to modulate chemoresistance. Mol Cell Biol 34:1839–1849CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Eletto D, Eletto D, Dersh D, Gidalevitz T, Argon Y (2014) Protein disulfide isomerase A6 controls the decay of IRE1alpha signaling via disulfide-dependent association. Mol Cell 53:562–576CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Khan S, Greco D, Michailidou K, Milne RL, Muranen TA, Heikkinen T, Aaltonen K, Dennis J, Bolla MK, Liu J, Hall P, Irwanto A, Humphreys K, Li J, Czene K, Chang-Claude J, Hein R, Rudolph A, Seibold P, Flesch-Janys D, Fletcher O, Peto J, dos Santos Silva I, Johnson N, Gibson L, Aitken Z, Hopper JL, Tsimiklis H, Bui M, Makalic E, Schmidt DF, Southey MC, Apicella C, Stone J, Waisfisz Q, Meijers-Heijboer H, Adank MA, van der Luijt RB, Meindl A, Schmutzler RK, Muller-Myhsok B, Lichtner P, Turnbull C, Rahman N, Chanock SJ, Hunter DJ, Cox A, Cross SS, Reed MW, Schmidt MK, Broeks A, Van't Veer LJ, Hogervorst FB, Fasching PA, Schrauder MG, Ekici AB, Beckmann MW, Bojesen SE, Nordestgaard BG, Nielsen SF, Flyger H, Benitez J, Zamora PM, Perez JI, Haiman CA, Henderson BE, Schumacher F, Le Marchand L, Pharoah PD, Dunning AM, Shah M, Luben R, Brown J, Couch FJ, Wang X, Vachon C, Olson JE, Lambrechts D, Moisse M, Paridaens R, Christiaens MR, Guenel P, Truong T, Laurent-Puig P, Mulot C, Marme F, Burwinkel B, Schneeweiss A, Sohn C, Sawyer EJ, Tomlinson I, Kerin MJ, Miller N, Andrulis IL, Knight JA, Tchatchou S, Mulligan AM, Dork T, Bogdanova NV, Antonenkova NN et al (2014) MicroRNA related polymorphisms and breast cancer risk. PLoS One 9:e109973CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    McMahon M, Samali A, Chevet E (2017) Regulation of the unfolded protein response by non-coding RNA. Am J Physiol Cell Physiol 313(3):C243–C254CrossRefPubMedGoogle Scholar
  71. 71.
    van Meer G, Voelker DR, Feigenson GW (2008) Membrane lipids: where they are and how they behave. Nat Rev Mol Cell Biol 9:112–124CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Chernomordik LV, Kozlov MM (2008) Mechanics of membrane fusion. Nat Struct Mol Biol 15:675–683CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Kannan M, Lahiri S, Liu LK, Choudhary V, Prinz WA (2017) Phosphatidylserine synthesis at membrane contact sites promotes its transport out of the ER. J Lipid Res 58:553–562CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Cerqueira NM, Oliveira EF, Gesto DS, Santos-Martins D, Moreira C, Moorthy HN, Ramos MJ, Fernandes PA (2016) Cholesterol biosynthesis: a mechanistic overview. Biochemistry 55:5483–5506CrossRefPubMedGoogle Scholar
  75. 75.
    Kovacs WJ, Olivier LM, Krisans SK (2002) Central role of peroxisomes in isoprenoid biosynthesis. Prog Lipid Res 41:369–391CrossRefPubMedGoogle Scholar
  76. 76.
    Agellon LB (2008) Metabolism and function of bile acids. In: Vance DE, Vance JE (eds) Biochemistry of lipids, lipoproteins and membranes, 5th edn. Elsevier, AmsterdamGoogle Scholar
  77. 77.
    Miller WL (2013) Steroid hormone synthesis in mitochondria. Mol Cell Endocrinol 379:62–73CrossRefPubMedGoogle Scholar
  78. 78.
    Fleet JC (2017) The role of vitamin D in the endocrinology controlling calcium homeostasis. Mol Cell Endocrinol 453:36–45CrossRefPubMedGoogle Scholar
  79. 79.
    Vega H, Agellon LB, Michalak M (2016) The rise of proteostasis promoters. IUBMB Life 68:943–954CrossRefPubMedGoogle Scholar
  80. 80.
    Norimatsu Y, Hasegawa K, Shimizu N, Toyoshima C (2017) Protein-phospholipid interplay revealed with crystals of a calcium pump. Nature 545:193–198CrossRefPubMedGoogle Scholar
  81. 81.
    Sriburi R, Jackowski S, Mori K, Brewer JW (2004) XBP1: a link between the unfolded protein response, lipid biosynthesis, and biogenesis of the endoplasmic reticulum. J Cell Biol 167:35–41CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Bommiasamy H, Back SH, Fagone P, Lee K, Meshinchi S, Vink E, Sriburi R, Frank M, Jackowski S, Kaufman RJ, Brewer JW (2009) ATF6alpha induces XBP1-independent expansion of the endoplasmic reticulum. J Cell Sci 122:1626–1636CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Wang WA, Liu WX, Durnaoglu S, Lee SK, Lian J, Lehner R, Ahnn J, Agellon LB, Michalak M (2017) Loss of calreticulin uncovers a critical role for calcium in regulating cellular lipid homeostasis. Sci Rep 7:5941CrossRefPubMedPubMedCentralGoogle Scholar
  84. 84.
    Brown MS, Goldstein JL (1997) The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell 89:331–340CrossRefPubMedGoogle Scholar
  85. 85.
    Shimano H (2001) Sterol regulatory element-binding proteins (SREBPs): transcriptional regulators of lipid synthetic genes. Prog Lipid Res 40:439–452CrossRefPubMedGoogle Scholar
  86. 86.
    Radhakrishnan A, Goldstein JL, McDonald JG, Brown MS (2008) Switch-like control of SREBP-2 transport triggered by small changes in ER cholesterol: a delicate balance. Cell Metab 8:512–521CrossRefPubMedPubMedCentralGoogle Scholar
  87. 87.
    Barneda D, Christian M (2017) Lipid droplet growth: regulation of a dynamic organelle. Curr Opin Cell Biol 47:9–15CrossRefPubMedGoogle Scholar
  88. 88.
    Daniele T, Schiaffino MV (2014) Organelle biogenesis and interorganellar connections: Better in contact than in isolation. Commun Integr Biol 7:e29587CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    Filadi R, Pozzan T (2015) Generation and functions of second messengers microdomains. Cell Calcium 58:405–414CrossRefPubMedGoogle Scholar
  90. 90.
    Joshi AS, Zhang H, Prinz WA (2017) Organelle biogenesis in the endoplasmic reticulum. Nat Cell Biol 19:876–882CrossRefPubMedGoogle Scholar
  91. 91.
    Nunes-Hasler P, Demaurex N (2017) The ER phagosome connection in the era of membrane contact sites. Biochim Biophys Acta 1864:1513–1524CrossRefPubMedGoogle Scholar
  92. 92.
    Penny CJ, Kilpatrick BS, Eden ER, Patel S (2015) Coupling acidic organelles with the ER through Ca2+ microdomains at membrane contact sites. Cell Calcium 58:387–396CrossRefPubMedGoogle Scholar
  93. 93.
    Phillips MJ, Voeltz GK (2016) Structure and function of ER membrane contact sites with other organelles. Nat Rev Mol Cell Biol 17:69–82CrossRefPubMedGoogle Scholar
  94. 94.
    Prinz WA (2014) Bridging the gap: membrane contact sites in signaling, metabolism, and organelle dynamics. J Cell Biol 205:759–769CrossRefPubMedPubMedCentralGoogle Scholar
  95. 95.
    Prudent J, McBride HM (2017) The mitochondria-endoplasmic reticulum contact sites: a signalling platform for cell death. Curr Opin Cell Biol 47:52–63CrossRefPubMedGoogle Scholar
  96. 96.
    Helle SC, Kanfer G, Kolar K, Lang A, Michel AH, Kornmann B (2013) Organization and function of membrane contact sites. Biochim Biophys Acta 1833:2526–2541CrossRefPubMedGoogle Scholar
  97. 97.
    Orci L, Ravazzola M, Le Coadic M, Shen WW, Demaurex N, Cosson P (2009) From the Cover: STIM1-induced precortical and cortical subdomains of the endoplasmic reticulum. Proc Natl Acad Sci U S A 106:19358–19362CrossRefPubMedPubMedCentralGoogle Scholar
  98. 98.
    Jain A, Holthuis JCM (2017) Membrane contact sites, ancient and central hubs of cellular lipid logistics. Biochim Biophys Acta 1864:1450–1458CrossRefPubMedGoogle Scholar
  99. 99.
    Chiapparino A, Maeda K, Turei D, Saez-Rodriguez J, Gavin AC (2016) The orchestra of lipid-transfer proteins at the crossroads between metabolism and signaling. Prog Lipid Res 61:30–39CrossRefPubMedGoogle Scholar
  100. 100.
    Lang A, John Peter AT, Kornmann B (2015) ER-mitochondria contact sites in yeast: beyond the myths of ERMES. Curr Opin Cell Biol 35:7–12CrossRefPubMedGoogle Scholar
  101. 101.
    Levine TP, Patel S (2016) Signalling at membrane contact sites: two membranes come together to handle second messengers. Curr Opin Cell Biol 39:77–83CrossRefPubMedGoogle Scholar
  102. 102.
    Vance JE (1990) Phospholipid synthesis in a membrane fraction associated with mitochondria. J Biol Chem 265:7248–7256PubMedGoogle Scholar
  103. 103.
    Raturi A, Simmen T (2013) Where the endoplasmic reticulum and the mitochondrion tie the knot: the mitochondria-associated membrane (MAM). Biochim Biophys Acta 1833:213–224CrossRefPubMedGoogle Scholar
  104. 104.
    Wong LH, Levine TP (2016) Lipid transfer proteins do their thing anchored at membrane contact sites… but what is their thing? Biochem Soc Trans 44:517–527CrossRefPubMedGoogle Scholar
  105. 105.
    Michel AH, Kornmann B (2012) The ERMES complex and ER-mitochondria connections. Biochem Soc Trans 40:445–450CrossRefPubMedGoogle Scholar
  106. 106.
    Barone V, Randazzo D, Del Re V, Sorrentino V, Rossi D (2015) Organization of junctional sarcoplasmic reticulum proteins in skeletal muscle fibers. J Muscle Res Cell Motil 36:501–515CrossRefPubMedGoogle Scholar
  107. 107.
    Landstrom AP, Beavers DL, Wehrens XH (2014) The junctophilin family of proteins: from bench to bedside. Trends Mol Med 20:353–362CrossRefPubMedPubMedCentralGoogle Scholar
  108. 108.
    Louch WE, Nattel S (2017) T-tubular collagen: a new player in mechanosensing and disease? Cardiovasc Res 113(8):839–840CrossRefPubMedGoogle Scholar
  109. 109.
    Manfra O, Frisk M, Louch WE (2017) Regulation of cardiomyocyte T-tubular structure: opportunities for therapy. Curr Heart Fail Rep 14:167–178CrossRefPubMedPubMedCentralGoogle Scholar
  110. 110.
    Eisner DA, Caldwell JL, Kistamas K, Trafford AW (2017) Calcium and excitation-contraction coupling in the heart. Circ Res 121:181–195CrossRefPubMedPubMedCentralGoogle Scholar
  111. 111.
    De Stefani D, Rizzuto R, Pozzan T (2016) Enjoy the trip: calcium in mitochondria back and forth. Annu Rev Biochem 85:161–192CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2017

Authors and Affiliations

  1. 1.School of Human NutritionMcGill UniversitySte. Anne de BellevueCanada
  2. 2.Department of BiochemistryUniversity of AlbertaEdmontonCanada

Personalised recommendations