A calcium-dependent protease as a potential therapeutic target for Wolfram syndrome

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 49, 2014, Pages E5292-E5301

  Lu, Simin ^a,b   Kanekura, Kohsuke ^a   Hara, Takashi ^a   Mahadevan, Jana ^a   Spears, Larry D ^a   Oslowski, Christine M ^c   Martinez, Rita ^a   Yamazaki Inoue, Mayu ^d   Toyoda, Masashi ^d   Neilson, Amber ^a   Blanner, Patrick ^a   Brown, Cris M ^a   Semenkovich, Clay F ^a   Marshall, Bess A ^a   Hershey, Tamara ^a   Umezawa, Akihiro ^d   Greer, Peter A ^e   Urano, Fumihiko ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^c BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d NATIONAL CENTER FOR CHILD HEALTH AND DEVELOPMENT   (Japan)

^e QUEEN S UNIVERSITY   (Canada)

Author keywords

Diabetes; Endoplasmic reticulum; Neurodegeneration; Treatment; Wolfram syndrome

Indexed keywords

CALCIUM; CALPAIN 2; CALPAIN INHIBITOR III; CALPASTATIN; DANTROLENE; DOCOSAHEXAENOIC ACID; GLUCAGON LIKE PEPTIDE 1; N (2 CYCLOHEXYLOXY 4 NITROPHENYL)METHANESULFONAMIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; PIOGLITAZONE; UNCLASSIFIED DRUG; CALPAIN; CAPN2 PROTEIN, HUMAN; CAPNS1 PROTEIN, HUMAN; MEMBRANE PROTEIN; PROTEIN BINDING; WOLFRAMIN PROTEIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CALCIUM SIGNALING; CELL PROTECTION; CONTROLLED STUDY; DRUG TARGETING; EMBRYO; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; GENE; GENE ACTIVATION; GENE CONTROL; HUMAN; HUMAN CELL; KNOCKOUT MOUSE; LOSS OF FUNCTION MUTATION; MOUSE; NEURAL STEM CELL; NEUROPROTECTION; NONHUMAN; PLURIPOTENT STEM CELL; WOLFRAM SYNDROME; WOLFRAM SYNDROME 1 GENE; WOLFRAM SYNDROME 2 GENE; ADOLESCENT; ADULT; ANIMAL; CELL DEATH; CELL LINE; CHILD; CYTOLOGY; ENDOPLASMIC RETICULUM; FEMALE; FIBROBLAST; GENETICS; HEK293 CELL LINE; MALE; METABOLISM; MUTATION; NEWBORN; PATHOLOGY; RAT;

ADOLESCENT; ADULT; ANIMALS; CALCIUM; CALPAIN; CELL DEATH; CELL LINE; CHILD; DANTROLENE; ENDOPLASMIC RETICULUM; FEMALE; FIBROBLASTS; HEK293 CELLS; HUMANS; INDUCED PLURIPOTENT STEM CELLS; INFANT, NEWBORN; MALE; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; MUTATION; NEURAL STEM CELLS; PROTEIN BINDING; RATS; WOLFRAM SYNDROME;

EID: 84916199287     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1421055111     Document Type: Article

References (48)

1. Ron D, Walter P (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8(7):519-529.
2. Tabas I, Ron D (2011) Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat Cell Biol 13(3):184-190.
3. Hetz C, Chevet E, Harding HP (2013) Targeting the unfolded protein response in disease. Nat Rev Drug Discov 12(9):703-719.
4. Wang S, Kaufman RJ (2012) The impact of the unfolded protein response on human disease. J Cell Biol 197(7):857-867.
5. Fonseca SG, et al. (2005) WFS1 is a novel component of the unfolded protein response and maintains homeostasis of the endoplasmic reticulum in pancreatic beta-cells. J Biol Chem 280(47):39609-39615.
6. Fonseca SG, et al. (2010) Wolfram syndrome 1 gene negatively regulates ER stress signaling in rodent and human cells. J Clin Invest 120(3):744-755.
7. Barrett TG, Bundey SE, Macleod AF (1995) Neurodegeneration and diabetes: UK nationwide study of Wolfram (DIDMOAD) syndrome. Lancet 346(8988):1458-1463.
8. Wolfram DJ, Wagener HP (1938) Diabetes mellitus and simple optic atrophy among siblings: Report of four cases. Mayo Clin Proc 1:715-718.
9. Urano F (2014) Diabetes: Targeting endoplasmic reticulum to combat juvenile diabetes. Nat Rev Endocrinol 10(3):129-130.
10. Hershey T, et al.; Washington University Wolfram Study Group (2012) Early brain vulnerability in Wolfram syndrome. PLoS ONE 7(7):e40604.
11. Marshall BA, et al.; Washington University Wolfram Study Group (2013) Phenotypic characteristics of early Wolfram syndrome. Orphanet J Rare Dis 8(1):64.
12. Inoue H, et al. (1998) A gene encoding a transmembrane protein is mutated in patients with diabetes mellitus and optic atrophy (Wolfram syndrome). Nat Genet 20(2):143-148.
13. Amr S, et al. (2007) A homozygous mutation in a novel zinc-finger protein, ERIS, is responsible for Wolfram syndrome 2. Am J Hum Genet 81(4):673-683.
14. Chen YF, et al. (2009) Cisd2 deficiency drives premature aging and causes mitochondria-mediated defects in mice. Genes Dev 23(10):1183-1194.
15. Wiley SE, et al. (2013) Wolfram Syndrome protein, Miner1, regulates sulphydryl redox status, the unfolded protein response, and Ca2+ homeostasis. EMBO Mol Med 5(6):904-918.
16. Shang L, et al. (2014) innodatabeta-cell dysfunction due to increased ER stress in a stem cell model of Wolfram syndrome. Diabetes 63(3):923-933.
17. Sandhu MS, et al. (2007) Common variants in WFS1 confer risk of type 2 diabetes. Nat Genet 39(8):951-953.
18. Bonnycastle LL, et al. (2013) Autosomal dominant diabetes arising from a Wolfram syndrome 1 mutation. Diabetes 62(11):3943-3950.
19. Goll DE, Thompson VF, Li H, Wei W, Cong J (2003) The calpain system. Physiol Rev 83(3):731-801.
20. Tan Y, et al. (2006) Ubiquitous calpains promote caspase-12 and JNK activation during endoplasmic reticulum stress-induced apoptosis. J Biol Chem 281(23):16016-16024.
21. Tan Y, Wu C, De Veyra T, Greer PA (2006) Ubiquitous calpains promote both apoptosis and survival signals in response to different cell death stimuli. J Biol Chem 281(26):17689-17698.
22. Nakagawa T, Yuan J (2000) Cross-talk between two cysteine protease families. Activation of caspase-12 by calpain in apoptosis. J Cell Biol 150(4):887-894.
23. Cui W, et al. (2013) Free fatty acid induces endoplasmic reticulum stress and apoptosis of β-cells by Ca2+/calpain-2 pathways. PLoS ONE 8(3):e59921.
24. Huang CJ, et al. (2010) Calcium-activated calpain-2 is a mediator of beta cell dysfunction and apoptosis in type 2 diabetes. J Biol Chem 285(1):339-348.
25. Barrett TG, Bundey SE (1997) Wolfram (DIDMOAD) syndrome. J Med Genet 34(10):838-841.
26. Liu MC, et al. (2006) Comparing calpain- and caspase-3-mediated degradation patterns in traumatic brain injury by differential proteome analysis. Biochem J 394(Pt 3):715-725.
27. Hara T, et al. (2014) Calcium efflux from the endoplasmic reticulum leads to innodatabeta-cell death. Endocrinology 155(3):758-768.
28. Takei D, et al. (2006) WFS1 protein modulates the free Ca(2+) concentration in the endoplasmic reticulum. FEBS Lett 580(24):5635-5640.
29. Liu MC, et al. (2006) Extensive degradation of myelin basic protein isoforms by calpain following traumatic brain injury. J Neurochem 98(3):700-712.
30. Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126(4):663-676.
31. Yusta B, et al. (2006) GLP-1 receptor activation improves beta cell function and survival following induction of endoplasmic reticulum stress. Cell Metab 4(5):391-406.
32. Akiyama M, et al. (2009) Increased insulin demand promotes while pioglitazone prevents pancreatic beta cell apoptosis in Wfs1 knockout mice. Diabetologia 52(4):653-663.
33. Bachar-Wikstrom E, et al. (2013) Stimulation of autophagy improves endoplasmic reticulum stress-induced diabetes. Diabetes 62(4):1227-1237.
34. Dykes MH (1975) Evaluation of a muscle relaxant: Dantrolene sodium (Dantrium). JAMA 231(8):862-864.
35. Wei H, Perry DC (1996) Dantrolene is cytoprotective in two models of neuronal cell death. J Neurochem 67(6):2390-2398.
36. Luciani DS, et al. (2009) Roles of IP3R and RyR Ca2+ channels in endoplasmic reticulum stress and beta-cell death. Diabetes 58(2):422-432.
37. Hotamisligil GS (2010) Endoplasmic reticulum stress and atherosclerosis. Nat Med 16(4):396-399.
38. Hotamisligil GS (2010) Endoplasmic reticulum stress and the inflammatory basis of metabolic disease. Cell 140(6):900-917.
39. Ozcan L, Tabas I (2012) Role of endoplasmic reticulum stress in metabolic disease and other disorders. Annu Rev Med 63:317-328.
40. Riggs AC, et al. (2005) Mice conditionally lacking the Wolfram gene in pancreatic islet beta cells exhibit diabetes as a result of enhanced endoplasmic reticulum stress and apoptosis. Diabetologia 48(11):2313-2321.
41. Ishihara H, et al. (2004) Disruption of the WFS1 gene in mice causes progressive beta-cell loss and impaired stimulus-secretion coupling in insulin secretion. Hum Mol Genet 13(11):1159-1170.
42. Zatyka M, et al. (2008) Sodium-potassium ATPase 1 subunit is a molecular partner of Wolframin, an endoplasmic reticulum protein involved in ER stress. Hum Mol Genet 17(2):190-200.
43. Chang NC, Nguyen M, Germain M, Shore GC (2010) Antagonism of Beclin 1-dependent autophagy by BCL-2 at the endoplasmic reticulum requires NAF-1. EMBO J 29(3):606-618.
44. Dutt P, et al. (2006) m-Calpain is required for preimplantation embryonic development in mice. BMC Dev Biol 6:3.
45. Arya VB, Mohammed Z, Blankenstein O, De Lonlay P, Hussain K (2014) Hyperinsulinaemic hypoglycaemia. Hormone Metabolic Res 46(3):157-170.
46. Shah P, Demirbilek H, Hussain K (2014) Persistent hyperinsulinaemic hypoglycaemia in infancy. Semin Pediatr Surg 23(2):76-82.
47. Krause T, Gerbershagen MU, Fiege M, Weisshorn R, Wappler F (2004) Dantrolene - a review of its pharmacology, therapeutic use and new developments. Anaesthesia 59(4):364-373.
48. Chakroborty S, et al. (2012) Stabilizing ER Ca2+ channel function as an early preventative strategy for Alzheimer's disease. PLoS ONE 7(12):e52056.