A thrombospondin-dependent pathway for a protective ER stress response

Cell

Volumn 149, Issue 6, 2012, Pages 1257-1268

  Lynch, Jeffrey M ^a   Maillet, Marjorie ^a   Vanhoutte, Davy ^a   Schloemer, Aryn ^a   Sargent, Michelle A ^a,b   Blair, N Scott ^a   Lynch, Kaari A ^a   Okada, Tetsuya ^c   Aronow, Bruce J ^a   Osinska, Hanna ^a   Prywes, Ron ^d   Lorenz, John N ^a   Mori, Kazutoshi ^c   Lawler, Jack ^e   Robbins, Jeffrey ^a   Molkentin, Jeffery D ^a,b  

^a UNIVERSITY OF CINCINNATI   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c KYOTO UNIVERSITY   (Japan)

^d Och Spine at New York Presbyterian Hospitals   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; ACTIVATING TRANSCRIPTION FACTOR 6 ALPHA; DOXYCYCLINE; HEAT SHOCK PROTEIN; PLASMA PROTEIN; TETRACYCLINE; THROMBOSPONDIN; THROMBOSPONDIN 4; TUNICAMYCIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL EXPANSION; CELL FUNCTION; CELL VACUOLE; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; EFFECTOR CELL; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; GENE DELETION; GENE OVEREXPRESSION; HEART; HEART MUSCLE INJURY; HEART PROTECTION; HUMAN; HUMAN CELL; MALADJUSTMENT; MEDIATOR; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; TRANSGENIC ANIMAL;

MUS; MUS MUSCULUS;

EID: 84861996364     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2012.03.050     Document Type: Article

References (63)

1. Y. Adachi, K. Yamamoto, T. Okada, H. Yoshida, A. Harada, and K. Mori ATF6 is a transcription factor specializing in the regulation of quality control proteins in the endoplasmic reticulum Cell Struct. Funct. 33 2008 75 89
2. P.J. Belmont, A. Tadimalla, W.J. Chen, J.J. Martindale, D.J. Thuerauf, M. Marcinko, N. Gude, M.A. Sussman, and C.C. Glembotski Coordination of growth and endoplasmic reticulum stress signaling by regulator of calcineurin 1 (RCAN1), a novel ATF6-inducible gene J. Biol. Chem. 283 2008 14012 14021
3. A. Beskow, K.B. Grimberg, L.C. Bott, F.A. Salomons, N.P. Dantuma, and P. Young A conserved unfoldase activity for the p97 AAA-ATPase in proteasomal degradation J. Mol. Biol. 394 2009 732 746
4. H. Bommiasamy, S.H. Back, P. Fagone, K. Lee, S. Meshinchi, E. Vink, R. Sriburi, M. Frank, S. Jackowski, R.J. Kaufman, and J.W. Brewer ATF6alpha induces XBP1-independent expansion of the endoplasmic reticulum J. Cell Sci. 122 2009 1626 1636
5. M.D. Briggs, S.M. Hoffman, L.M. King, A.S. Olsen, H. Mohrenweiser, J.G. Leroy, G.R. Mortier, D.L. Rimoin, R.S. Lachman, and E.S. Gaines Pseudoachondroplasia and multiple epiphyseal dysplasia due to mutations in the cartilage oligomeric matrix protein gene Nat. Genet. 10 1995 330 336
6. F.H. Chen, M.E. Herndon, N. Patel, J.T. Hecht, R.S. Tuan, and J. Lawler Interaction of cartilage oligomeric matrix protein/thrombospondin 5 with aggrecan J. Biol. Chem. 282 2007 24591 24598
7. Y.-W. Chen, P. Zhao, R. Borup, and E.P. Hoffman Expression profiling in the muscular dystrophies: identification of novel aspects of molecular pathophysiology J. Cell Biol. 151 2000 1321 1336
8. O.H. Cingolani, J.A. Kirk, K. Seo, N. Koitabashi, D.I. Lee, G. Ramirez-Correa, D. Bedja, A.S. Barth, A.L. Moens, and D.A. Kass Thrombospondin-4 is required for stretch-mediated contractility augmentation in cardiac muscle Circ. Res. 109 2011 1410 1414
9. A.R. Cook, S.C. Bardswell, S. Pretheshan, K. Dighe, G.S. Kanaganayagam, R.I. Jabr, S. Merkle, M.S. Marber, S. Engelhardt, and M. Avkiran Paradoxical resistance to myocardial ischemia and age-related cardiomyopathy in NHE1 transgenic mice: a role for ER stress? J. Mol. Cell. Cardiol. 46 2009 225 233
10. E. Délot, L.M. King, M.D. Briggs, W.R. Wilcox, and D.H. Cohn Trinucleotide expansion mutations in the cartilage oligomeric matrix protein (COMP) gene Hum. Mol. Genet. 8 1999 123 128
11. N.G. Frangogiannis, G. Ren, O. Dewald, P. Zymek, S. Haudek, A. Koerting, K. Winkelmann, L.H. Michael, J. Lawler, and M.L. Entman Critical role of endogenous thrombospondin-1 in preventing expansion of healing myocardial infarcts Circulation 111 2005 2935 2942
12. A. Gabrielsen, P.R. Lawler, W. Yongzhong, D. Steinbrüchel, D. Blagoja, G. Paulsson-Berne, J. Kastrup, and G.K. Hansson Gene expression signals involved in ischemic injury, extracellular matrix composition and fibrosis defined by global mRNA profiling of the human left ventricular myocardium J. Mol. Cell. Cardiol. 42 2007 870 883
13. C.C. Glembotski Endoplasmic reticulum stress in the heart Circ. Res. 101 2007 975 984
14. S.A. Greco, J. Chia, K.J. Inglis, S.J. Cozzi, I. Ramsnes, R.L. Buttenshaw, K.J. Spring, G.M. Boyle, D.L. Worthley, B.A. Leggett, and V.L. Whitehall Thrombospondin-4 is a putative tumour-suppressor gene in colorectal cancer that exhibits age-related methylation BMC Cancer 10 2010 494
15. H. Hamada, M. Suzuki, S. Yuasa, N. Mimura, N. Shinozuka, Y. Takada, M. Suzuki, T. Nishino, H. Nakaya, H. Koseki, and T. Aoe Dilated cardiomyopathy caused by aberrant endoplasmic reticulum quality control in mutant KDEL receptor transgenic mice Mol. Cell. Biol. 24 2004 8007 8017
16. Y. Hashimoto, T. Tomiyama, Y. Yamano, and H. Mori Mutation (D472Y) in the type 3 repeat domain of cartilage oligomeric matrix protein affects its early vesicle trafficking in endoplasmic reticulum and induces apoptosis Am. J. Pathol. 163 2003 101 110
17. N. Hauser, M. Paulsson, A.A. Kale, and P.E. DiCesare Tendon extracellular matrix contains pentameric thrombospondin-4 (TSP-4) FEBS Lett. 368 1995 307 310
18. J.T. Hecht, M. Deere, E. Putnam, W. Cole, B. Vertel, H. Chen, and J. Lawler Characterization of cartilage oligomeric matrix protein (COMP) in human normal and pseudoachondroplasia musculoskeletal tissues Matrix Biol. 17 1998 269 278
19. J.T. Hecht, E. Hayes, M. Snuggs, G. Decker, D. Montufar-Solis, K. Doege, F. Mwalle, R. Poole, J. Stevens, and P.J. Duke Calreticulin, PDI, Grp94 and BiP chaperone proteins are associated with retained COMP in pseudoachondroplasia chondrocytes Matrix Biol. 20 2001 251 262
20. J.T. Hecht, L.D. Nelson, E. Crowder, Y. Wang, F.F. Elder, W.R. Harrison, C.A. Francomano, C.K. Prange, G.G. Lennon, M. Deere, and J. Lawler Mutations in exon 17B of cartilage oligomeric matrix protein (COMP) cause pseudoachondroplasia Nat. Genet. 10 1995 325 329
21. M. Kaneko, H. Koike, R. Saito, Y. Kitamura, Y. Okuma, and Y. Nomura Loss of HRD1-mediated protein degradation causes amyloid precursor protein accumulation and amyloid-beta generation J. Neurosci. 30 2010 3924 3932
22. S. Kazerounian, K.O. Yee, and J. Lawler Thrombospondins in cancer Cell. Mol. Life Sci. 65 2008 700 712
23. M. Kerbiriou, M.A. Le Drévo, C. Férec, and P. Trouvé Coupling cystic fibrosis to endoplasmic reticulum stress: Differential role of Grp78 and ATF6 Biochim. Biophys. Acta 1772 2007 1236 1249
24. G. Kuznetsov, L.B. Chen, and S.K. Nigam Multiple molecular chaperones complex with misfolded large oligomeric glycoproteins in the endoplasmic reticulum J. Biol. Chem. 272 1997 3057 3063
25. J. Lawler, M. Duquette, C.A. Whittaker, J.C. Adams, K. McHenry, and D.W. DeSimone Identification and characterization of thrombospondin-4, a new member of the thrombospondin gene family J. Cell Biol. 120 1993 1059 1067
26. J. Lawler, K. McHenry, M. Duquette, and L. Derick Characterization of human thrombospondin-4 J. Biol. Chem. 270 1995 2809 2814
27. J.J. Martindale, R. Fernandez, D. Thuerauf, R. Whittaker, N. Gude, M.A. Sussman, and C.C. Glembotski Endoplasmic reticulum stress gene induction and protection from ischemia/reperfusion injury in the hearts of transgenic mice with a tamoxifen-regulated form of ATF6 Circ. Res. 98 2006 1186 1193
28. E. Mustonen, J. Aro, J. Puhakka, M. Ilves, Y. Soini, H. Leskinen, H. Ruskoaho, and J. Rysä Thrombospondin-4 expression is rapidly upregulated by cardiac overload Biochem. Biophys. Res. Commun. 373 2008 186 191
29. T. Okada, K. Haze, S. Nadanaka, H. Yoshida, N.G. Seidah, Y. Hirano, R. Sato, M. Negishi, and K. Mori A serine protease inhibitor prevents endoplasmic reticulum stress-induced cleavage but not transport of the membrane-bound transcription factor ATF6 J. Biol. Chem. 278 2003 31024 31032
30. D. Prabakaran, P.S. Kim, V.M. Dixit, and P. Arvan Oligomeric assembly of thrombospondin in the endoplasmic reticulum of thyroid epithelial cells Eur. J. Cell Biol. 70 1996 134 141
31. A. Sanbe, J. Gulick, M.C. Hanks, Q. Liang, H. Osinska, and J. Robbins Reengineering inducible cardiac-specific transgenesis with an attenuated myosin heavy chain promoter Circ. Res. 92 2003 609 616
32. M.W. Schellings, G.C. van Almen, E.H. Sage, and S. Heymans Thrombospondins in the heart: potential functions in cardiac remodeling J Cell Commun Signal 3 2009 201 213
33. B. Schroen, S. Heymans, U. Sharma, W.M. Blankesteijn, S. Pokharel, J.P. Cleutjens, J.G. Porter, C.T. Evelo, R. Duisters, and R.E. van Leeuwen Thrombospondin-2 is essential for myocardial matrix integrity: increased expression identifies failure-prone cardiac hypertrophy Circ. Res. 95 2004 515 522
34. F. Södersten, S. Ekman, A. Niehoff, F. Zaucke, D. Heinegård, and K. Hultenby Ultrastructural immunolocalization of cartilage oligomeric matrix protein, thrombospondin-4, and collagen fibril size in rodent achilles tendon in relation to exercise Connect. Tissue Res. 48 2007 254 262
35. O.I. Stenina, E.J. Topol, and E.F. Plow Thrombospondins, their polymorphisms, and cardiovascular disease Arterioscler. Thromb. Vasc. Biol. 27 2007 1886 1894
36. M. Swinnen, D. Vanhoutte, G.C. Van Almen, N. Hamdani, M.W. Schellings, J. D'hooge, J. Van der Velden, M.S. Weaver, E.H. Sage, and P. Bornstein Absence of thrombospondin-2 causes age-related dilated cardiomyopathy Circulation 120 2009 1585 1597
37. D. Veliceasa, M. Ivanovic, F.T.-S. Hoepfner, P. Thumbikat, O.V. Volpert, and N.D. Smith Transient potential receptor channel 4 controls thrombospondin-1 secretion and angiogenesis in renal cell carcinoma FEBS J. 274 2007 6365 6377
38. J. Vranka, A. Mokashi, D.R. Keene, S. Tufa, G. Corson, M. Sussman, W.A. Horton, K. Maddox, L. Sakai, and H.P. Bächinger Selective intracellular retention of extracellular matrix proteins and chaperones associated with pseudoachondroplasia Matrix Biol. 20 2001 439 450
39. X. Wang, and J. Robbins Heart failure and protein quality control Circ. Res. 99 2006 1315 1328
40. X. Wang, H. Osinska, G.W. Dorn 2nd, M. Nieman, J.N. Lorenz, A.M. Gerdes, S. Witt, T. Kimball, J. Gulick, and J. Robbins Mouse model of desmin-related cardiomyopathy Circulation 103 2001 2402 2407
41. X. Wang, H. Osinska, R. Klevitsky, A.M. Gerdes, M. Nieman, J. Lorenz, T. Hewett, and J. Robbins Expression of R120G-alphaB-crystallin causes aberrant desmin and alphaB-crystallin aggregation and cardiomyopathy in mice Circ. Res. 89 2001 84 91
42. J. Xu, G. Wang, Y. Wang, Q. Liu, W. Xu, Y. Tan, and L. Cai Diabetes- and angiotensin II-induced cardiac endoplasmic reticulum stress and cell death: metallothionein protection J. Cell. Mol. Med. 13 8A 2009 1499 1512
43. K. Zhang, and R.J. Kaufman From endoplasmic-reticulum stress to the inflammatory response Nature 454 2008 455 462
44. Arber, S.; Hunter, J.J.; Ross, J.; Jr.; Hongo, M.; Sansig, G.; Borg, J.; Perriard, J.C.; Chien, K.R.; and Caroni, P. (1997). MLP-deficient mice exhibit a disruption of cardiac cytoarchitectural organization, dilated cardiomyopathy, and heart failure. Cell 88, 393-403.
45. Braz, J.C.; Gregory, K.; Pathak, A.; Zhao, W.; Sahin, B.; Klevitsky, R.; Kimball, T.F.; Lorenz, J.N.; Nairn, A.C.; Liggett, S.B.; et al. (2004). PKC-alpha regulates cardiac contractility and propensity toward heart failure. Nat. Med. 10, 248-254.
46. Chen, X.; Shen, J.; and Prywes, R. (2002). The luminal domain of ATF6 senses endoplasmic reticulum (ER) stress and causes translocation of ATF6 from the ER to the Golgi. J. Biol. Chem. 277, 13045-13052.
47. De Windt, L.J.; Lim, H.W.; Haq, S.; Force, T.; and Molkentin, J.D. (2000). Calcineurin promotes protein kinase C and c-Jun NH2-terminal kinase activation in the heart. Cross-talk between cardiac hypertrophic signaling pathways. J. Biol. Chem. 275, 13571-13579.
48. Fewell, J.G.; Osinska, H.; Klevitsky, R.; Ng, W.; Sfyris, G.; Bahrehmand, F.; and Robbins, J. (1997). A treadmill exercise regimen for identifying cardiovascular phenotypes in transgenic mice. Am. J. Physiol. 273, H1595-H1605.
49. Goonasekera, S.A.; Lam, C.K.; Millay, D.P.; Sargent, M.A.; Hajjar, R.J.; Kranias, E.G.; and Molkentin, J.D. (2011). Mitigation of muscular dystrophy in mice by SERCA overexpression in skeletal muscle. J. Clin. Invest. 121, 1044-1052.
50. Kaiser, R.A.; Lyons, J.M.; Duffy, J.Y.; Wagner, C.J.; McLean, K.M.; O'Neill, T.P.; Pearl, J.M.; and Molkentin, J.D. (2005). Inhibition of p38 reduces myocardial infarction injury in the mouse but not pig after ischemia-reperfusion. Am. J. Physiol. Heart Circ. Physiol. 289, H2747-H2751.
51. Maillet, M.; Davis, J.; Auger-Messier, M.; York, A.; Osinska, H.; Piquereau, J.; Lorenz, J.N.; Robbins, J.; Ventura-Clapier, R.; and Molkentin, J.D. (2010). Heart-specific deletion of CnB1 reveals multiple mechanisms whereby calcineurin regulates cardiac growth and function. J. Biol. Chem. 285, 6716-6724.
52. Molkentin, J.D.; Lu, J.R.; Antos, C.L.; Markham, B.; Richardson, J.; Robbins, J.; Grant, S.R.; and Olson, E.N. (1998). A calcineurin-dependent transcriptional pathway for cardiac hypertrophy. Cell 93, 215-228.
53. Oka, T.; Maillet, M.; Watt, A.J.; Schwartz, R.J.; Aronow, B.J.; Duncan, S.A.; and Molkentin, J.D. (2006). Cardiac-specific deletion of Gata4 reveals its requirement for hypertrophy, compensation, and myocyte viability. Circ. Res. 98, 837-845.
54. Okada, T.; Haze, K.; Nadanaka, S.; Yoshida, H.; Seidah, N.G.; Hirano, Y.; Sato, R.; Negishi, M.; and Mori, K. (2003). A serine protease inhibitor prevents endoplasmic reticulum stress-induced cleavage but not transport of the membrane-bound transcription factor ATF6. J. Biol. Chem. 278, 31024-31032.
55. Sanbe, A.; Gulick, J.; Hanks, M.C.; Liang, Q.; Osinska, H.; and Robbins, J. (2003). Reengineering inducible cardiac-specific transgenesis with an attenuated myosin heavy chain promoter. Circ. Res. 92, 609-616.
56. Shen, J.; Chen, X.; Hendershot, L.; and Prywes, R. (2002). ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of Golgi localization signals. Dev. Cell 3, 99-111.
57. Wang, X.; Osinska, H.; Dorn, G.W.; 2nd, Nieman, M.; Lorenz, J.N.; Gerdes, A.M.; Witt, S.; Kimball, T.; Gulick, J.; and Robbins, J. (2001a). Mouse model of desmin-related cardiomyopathy. Circulation 103, 2402-2407.
58. Wang, X.; Osinska, H.; Klevitsky, R.; Gerdes, A.M.; Nieman, M.; Lorenz, J.; Hewett, T.; and Robbins, J. (2001b). Expression of R120G-alphaB-crystallin causes aberrant desmin and alphaB-crystallin aggregation and cardiomyopathy in mice. Circ. Res. 89, 84-91.
59. Waser, M.; Mesaeli, N.; Spencer, C.; and Michalak, M. (1997). Regulation of calreticulin gene expression by calcium. J. Cell Biol. 138, 547-557.
60. Wilkins, B.J.; Dai, Y.S.; Bueno, O.F.; Parsons, S.A.; Xu, J.; Plank, D.M.; Jones, F.; Kimball, T.R.; and Molkentin, J.D. (2004). Calcineurin/NFAT coupling participates in pathological, but not physiological, cardiac hypertrophy. Circ. Res. 94, 110-118.
61. Woods, A.E.; and Ellis, R.C. (1994). Laboratory Histopathology: A Complete Reference (New York: Churchill Livingstone Publishers), pp. 7.1-13.
62. Xu, J.; Gong, N.L.; Bodi, I.; Aronow, B.J.; Backx, P.H.; and Molkentin, J.D. (2006). Myocyte enhancer factors 2A and 2C induce dilated cardiomyopathy in transgenic mice. J. Biol. Chem. 281, 9152-9162.
63. Yamamoto, K.; Sato, T.; Matsui, T.; Sato, M.; Okada, T.; Yoshida, H.; Harada, A.; and Mori, K. (2007). Transcriptional induction of mammalian ER quality control proteins is mediated by single or combined action of ATF6α and XBP1. Dev. Cell 13, 365-376.