Misfolded BRICHOS SP-C mutant proteins induce apoptosis via caspase-4- and cytochrome c-related mechanisms

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 293, Issue 3, 2007, Pages

  Mulugeta, Surafel ^a   Maguire, Jean Ann ^a   Newitt, Jennifer L ^a   Russo, Scott J ^a   Kotorashvili, Adam ^a   Beers, Michael F ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Endoplasmic reticulum stress; Misfolding proteins; Proteasome inhibition; Protein aggregation; Surfactant protein C

Indexed keywords

CASPASE 3; CASPASE 4; CYTOCHROME C; MEMBRANE PROTEIN; PROTEIN BRICHOS SP C; UNCLASSIFIED DRUG; X BOX BINDING PROTEIN 1;

APOPTOSIS; ARTICLE; CELL STRESS; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; EXON; GENE DELETION; HUMAN; HUMAN CELL; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEINASE INHIBITION;

ALTERNATIVE SPLICING; APOPTOSIS; CASPASES, INITIATOR; CELL LINE; CELL NUCLEUS; CYTOCHROMES C; CYTOSOL; DNA-BINDING PROTEINS; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; HUMANS; INCLUSION BODIES; MITOCHONDRIA; MUTANT PROTEINS; NUCLEAR PROTEINS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; PULMONARY SURFACTANT-ASSOCIATED PROTEIN C; SOLUBILITY; UBIQUITIN;

EID: 34548388834     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00025.2007     Document Type: Article

References (57)

1. Beers MF. Lung Surfactant: Cellular and Molecular Processing. Austin, TX: Landes, 1998.
2. Bence NF, Sampat RM, Kopito RR. Impairment of the ubiquitin-proteasome system by protein aggregation. Science 292: 1552-1555, 2001.
3. Brasch F, Griese M, Tredano M, Johnen G, Ochs M, Rieger C, Mulugeta S, Muller KM, Bahuau M, Beers MF. Interstitial lung disease in a baby with a de novo mutation in the SFTPC gene. Eur Respir J 24: 30-39, 2004.
4. Bridges JP, Wert SE, Nogee LM, Weaver TE. Expression of a human surfactant protein C mutation associated with interstitial lung disease disrupts lung development in transgenic mice. J Biol Chem 278: 52739-52746, 2003.
5. Bridges JP, Xu Y, Na CL, Wong HR, Weaver TE. Adaptation and increased susceptibility to infection associated with constitutive expression of misfolded SP-C. J Cell Biol 172: 395-407, 2006.
6. Cardinale A, Filesi I, Mattei S, Biocca S. Evidence for proteasome dysfunction in cytotoxicity mediated by anti-Ras intracellular antibodies. Eur J Biochem 270: 3389-3397, 2003.
7. Ciechanover A, Schwartz AL. Ubiquitin-mediated degradation of cellular proteins in health and disease. Hepatology 35: 3-6, 2002.
8. Conkright JJ, Bridges JP, Na CL, Voorhout WF, Trapnell B, Glasser SW, Weaver TE. Secretion of surfactant protein C, an integral membrane protein, requires the N-terminal propeptide. J Biol Chem 276: 14658-14664, 2001.
9. Dluhy RA, Shanmukh S, Leapard JB, Kruger P, Baatz JE. Deacylated pulmonary surfactant protein SP-C transforms from alpha-helical to amyloid fibril structure via a pH-dependent mechanism: an infrared structural investigation. Biophys J 85: 2417-2429, 2003.
10. Gilon T, Chomsky O, Kulka RG. Degradation signals for ubiquitin system proteolysis in Saccharomyces cerevisiae. EMBO J 17: 2759-2766, 1998.
11. Gustafsson M, Thyberg J, Naslund J, Eliasson E, Johansson J. Amyloid fibril formation by pulmonary surfactant protein C. FEBS Lett 464: 138-142, 1999.
12. Häcki J, Egger L, Monney L, Conus S, Rosse T, Fellay I, Borner C. Apoptotic crosstalk between the endoplasmic reticulum and mitochondria controlled by Bcl-2. Oncogene 19: 2286-2295, 2000.
13. Hitomi J, Katayama T, Eguchi Y, Kudo T, Taniguchi M, Koyama Y, Manabe T, Yamagishi S, Bando Y, Imaizumi K, Tsujimoto Y, Tohyama M. Involvement of caspase-4 in endoplasmic reticulum stress-induced apoptosis and Abeta-induced cell death. J Cell Biol 165: 347-356, 2004.
14. Iwawaki T, Akai R, Kohno K, Miura M. A transgenic mouse model for monitoring endoplasmic reticulum stress. Nat Med 10: 98-102, 2004.
15. Jensen TJ, Loo MA, Pind S, Williams DB, Goldberg AL, Riordan JR. Multiple proteolytic systems, including the proteasome, contribute to CFTR processing. Cell 83: 129-135, 1995.
16. Jimbo A, Fujita E, Kouroku Y, Ohnishi J, Inohara N, Kuida K, Sakamaki K, Yonehara S, Momoi T. ER stress induces caspase-8 activation, stimulating cytochrome c release and caspase-9 activation. Exp Cell Res 283: 156-166, 2003.
17. Johansson H, Nordling K, Weaver TE, Johansson J. The Brichos domain-containing C-terminal part of pro-surfactant protein C binds to an unfolded poly-Val transmembrane segment. J Biol Chem 281: 21032-21039, 2006.
18. Johansson J. Structure and properties of surfactant protein C. Biochim Biophys Acta 1408: 161-172, 1998.
19. 2-terminal flanking domain are cleaved in late compartments. Am J Respir Cell Mol Biol 24: 253-263, 2001.
20. Johnston JA, Ward CL, Kopito RR. Aggresomes: a cellular response to misfolded proteins. J Cell Biol 143: 1883-1898, 1998.
21. Kabore AF, Wang WJ, Russo SJ, Beers MF. Biosynthesis of surfactant protein C: characterization of aggresome formation by EGFP chimeras containing propeptide mutants lacking conserved cysteine residues. J Cell Sci 114: 293-302, 2001.
22. Kaufman RJ. Orchestrating the unfolded protein response in health and disease. J Clin Invest 110: 1389-1398, 2002.
23. Kiechle T, Dedeoglu A, Kubilus J, Kowall NW, Beal MF, Friedlander RM, Hersch SM, Ferrante RJ. Cytochrome c and caspase-9 expression in Huntington's disease. Neuromolecular Med 1: 183-195, 2002.
24. Kim HS, Lee JH, Lee JP, Kim EM, Chang KA, Park CH, Jeong SJ, Wittendorp MC, Seo JH, Choi SH, Suh YH. Amyloid beta peptide induces cytochrome c release from isolated mitochondria. Neuroreport 13: 1989-1993, 2002.
25. Kluck RM, Bossy-Wetzel E, Green DR, Newmeyer DD. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 275: 1132-1136, 1997.
26. Kopito RR. Aggresomes, inclusion bodies and protein aggregation. Trends Cell Biol 10: 524-530, 2000.
27. Kopito RR, Ron D. Conformational disease. Nat Cell Biol 2: E207-E209, 2000.
28. Lee AH, Iwakoshi NN, Glimcher LH. XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol Cell Biol 23: 7448-7459, 2003.
29. Li J, Hosia W, Hamvas A, Thyberg J, Jornvall H, Weaver TE, Johansson J. The N-terminal propeptide of lung surfactant protein C is necessary for biosynthesis and prevents unfolding of a metastable alpha-helix. J Mol Biol 338: 857-862, 2004.
30. Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M, Alnemri ES, Wang X. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91: 479-489, 1997.
31. Ma J, Lindquist S. Conversion of PrP to a self-perpetuating PrPSc-like conformation in the cytosol. Science 298: 1785-1788, 2002.
32. Mulugeta S, Beers MF. Processing of surfactant protein C requires a type II transmembrane topology directed by juxtamembrane positively charged residues. J Biol Chem 2003.
33. Mulugeta S, Nguyen V, Russo SJ, Muniswamy M, Beers MF. A surfactant protein C precursor protein BRICHOS domain mutation causes endoplasmic reticulum stress, proteasome dysfunction, and caspase 3 activation. Am J Respir Cell Mol Biol 32: 521-530, 2005.
34. Nakagawa T, Yuan J. Cross-talk between two cysteine protease families. Activation of caspase-12 by calpain in apoptosis. J Cell Biol 150: 887-894, 2000.
35. Nakagawa T, Zhu H, Morishima N, Li E, Xu J, Yankner BA, Yuan J. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 403: 98-103, 2000.
36. Nishitoh H, Matsuzawa A, Tobiume K, Saegusa K, Takeda K, Inoue K, Hori S, Kakizuka A, Ichijo H. ASK1 is essential for endoplasmic reticulum stress-induced neuronal cell death triggered by expanded polyglutamine repeats. Genes Dev 16: 1345-1355, 2002.
37. Nogee LM. Abnormal expression of surfactant protein C and lung disease. Am J Respir Cell Mol Biol 26: 641-644, 2002.
38. Nogee LM, Dunbar AE, III, Wert SE, Askin F, Hamvas A, Whitsett JA. A mutation in the surfactant protein C gene associated with familial interstitial lung disease. N Engl J Med 344: 573-579, 2001.
39. Obeng EA, Boise LH. Caspase-12 and caspase-4 are not required for caspase-dependent endoplasmic reticulum stress-induced apoptosis. J Biol Chem 280: 29578-29587, 2005.
40. Paquette JC, Guerin PJ, Gauthier ER. Rapid induction of the intrinsic apoptotic pathway by L-glutamine starvation. J Cell Physiol 202: 912-921, 2005.
41. Pastrana B, Mautone AJ, Mendelsohn R. Fourier transform infrared studies of secondary structure and orientation of pulmonary surfactant SP-C and its effect on the dynamic surface properties of phospholipids. Biochemistry 30: 10058-10064, 1991.
42. Petrucelli L, O'Farrell C, Lockhart PJ, Baptista M, Kehoe K, Vink L, Choi P, Wolozin B, Farrer M, Hardy J, Cookson MR. Parkin protects against the toxicity associated with mutant alpha-synuclein: proteasome dysfunction selectively affects catecholaminergic neurons. Neuron 36: 1007-1019, 2002.
43. Qiu JH, Asai A, Chi S, Saito N, Hamada H, Kirino T. Proteasome inhibitors induce cytochrome c-caspase-3-like protease-mediated apoptosis in cultured cortical neurons. J Neurosci 20: 259-265, 2000.
44. Rodrigues CM, Sola S, Brito MA, Brondino CD, Brites D, Moura JJ. Amyloid beta-peptide disrupts mitochondrial membrane lipid and protein structure: protective role of tauroursodeoxycholate. Biochem Biophys Res Commun 281: 468-474, 2001.
45. Rutkowski DT, Kaufman RJ. A trip to the ER: coping with stress. Trends Cell Biol 14: 20-28, 2004.
46. Sanchez-Pulido L, Devos D, Valencia A. BRICHOS: a conserved domain in proteins associated with dementia, respiratory distress and cancer. Trends Biochem Sci 27: 329-332, 2002.
47. Smith WW, Jiang H, Pei Z, Tanaka Y, Morita H, Sawa A, Dawson VL, Dawson TM, Ross CA. Endoplasmic reticulum stress and mitochondrial cell death pathways mediate A53T mutant alpha-synuclein-induced toxicity. Hum Mol Genet 14: 3801-3811, 2005.
48. Stevens PA, Pettenazzo A, Brasch F, Mulugeta S, Baritussio A, Ochs M, Morrison L, Russo SJ, Beers MF. Nonspecific interstitial pneumonia, alveolar proteinosis, and abnormal proprotein trafficking resulting from a spontaneous mutation in the surfactant protein C gene. Pediatr Res 57: 89-98, 2005.
49. Thomas AQ, Lane K, Phillips J, III, Prince M, Markin C, Speer M, Schwartz DA, Gaddipati R, Marney A, Johnson J, Roberts R, Haines J, Stahlman M, Loyd JE. Heterozygosity for a surfactant protein C gene mutation associated with usual interstitial pneumonitis and cellular nonspecific interstitial pneumonitis in one kindred. Am J Respir Crit Care Med 165: 1322-1328, 2002.
50. Wang WJ, Mulugeta S, Russo SJ, Beers MF. Deletion of exon 4 from human surfactant protein C results in aggresome formation and generation of a dominant negative. J Cell Sci 116: 683-692, 2003.
51. Wang WJ, Russo SJ, Mulugeta S, Beers MF. Biosynthesis of Surfactant Protein C (SP-C). Sorting of SP-C proprotein involves homomeric association via a signal anchor domain. J Biol Chem 277: 19929-19937, 2002.
52. Ward CL, Omura S, Kopito RR. Degradation of CFTR by the ubiquitin-proteasome pathway. Cell 83: 121-127, 1995.
53. Weaver TE. Synthesis, processing and secretion of surfactant proteins B and C. Biochim Biophys Acta 1408: 173-179, 1998.
54. Wojcik C. Regulation of apoptosis by the ubiquitin and proteasome pathway. J Cell Mol Med 6: 25-48, 2002.
55. Yankner BA, Dawes LR, Fisher S, Villa-Komaroff L, Oster-Granite ML, Neve RL. Neurotoxicity of a fragment of the amyloid precursor associated with Alzheimer's disease. Science 245: 417-420, 1989.
56. Yoneda T, Imaizumi K, Oono K, Yui D, Gomi F, Katayama T, Tohyama M. Activation of caspase-12, an endoplasmic reticulum (ER) resident caspase, through tumor necrosis factor receptor-associated factor 2-dependent mechanism in response to the ER stress. J Biol Chem 276: 13935-13940, 2001.
57. Zhang K, Kaufman RJ. The unfolded protein response: a stress signaling pathway critical for health and disease. Neurology 66: S102-S109, 2006.