Matrix metalloproteinase-3 is activated by HtrA2/Omi in dopaminergic cells: Relevance to Parkinson's disease

Neurochemistry International

Volumn 60, Issue 3, 2012, Pages 249-256

  Shin, Eun Jung ^a   Kim, Eun Mee ^a,c   Lee, Ji Ae ^a   Rhim, Hyangshuk ^b   Hwang, Onyou ^a  

^a University of Ulsan College of Medicine   (South Korea)

^b The Catholic University of Korea   (South Korea)

^c Korea Nazarene University   (South Korea)

Author keywords

Dopaminergic neuron; HtrA2 Omi; Mitochondria; MMP 3; Parkinson's disease

Indexed keywords

RECOMBINANT ENZYME; ROTENONE; SERINE PROTEINASE OMI; SMALL INTERFERING RNA; STROMELYSIN;

ANIMAL CELL; ARTICLE; CELL DEATH; CELL STRESS; CONTROLLED STUDY; DISEASE ASSOCIATION; DOPAMINERGIC NERVE CELL; ENZYME ACTIVATION; ENZYME ACTIVITY; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN CLEAVAGE;

BLOTTING, WESTERN; CELL DEATH; CYTOSOL; DOPAMINERGIC NEURONS; ENZYME ACTIVATION; HUMANS; IMMUNOHISTOCHEMISTRY; L-LACTATE DEHYDROGENASE; MATRIX METALLOPROTEINASE 3; MITOCHONDRIA; NERVE TISSUE PROTEINS; PARKINSON DISEASE; REAL-TIME POLYMERASE CHAIN REACTION; RNA; RNA, SMALL INTERFERING; RNA-BINDING PROTEINS; ROTENONE; SILVER STAINING; SUBCELLULAR FRACTIONS; TRANSFECTION; UNCOUPLING AGENTS; X-LINKED INHIBITOR OF APOPTOSIS PROTEIN;

EID: 84862777355     PISSN: 01970186     EISSN: 18729754     Source Type: Journal    
DOI: 10.1016/j.neuint.2012.01.001     Document Type: Article

References (50)

1. J. Althaus, M.D. Siegelin, F. Dehghani, L. Cilenti, A.S. Zervos, and A. Rami The serine protease Omi/HtrA2 is involved in XIAP cleavage and in neuronal cell death following focal cerebral ischemia/reperfusion Neurochem. Int. 50 2007 172 180 (Pubitemid 44895360)
2. D.M. Arduíno, A.R. Esteves, S.M. Cardoso, and C.R. Oliveira Endoplasmic reticulum and mitochondria interplay mediates apoptotic cell death: relevance to Parkinson's disease Neurochem. Int. 55 2009 341 348
3. R. Banerjee, A.A. Starkov, M.F. Beal, and B. Thomas Mitochondrial dysfunction in the limelight of Parkinson's disease pathogenesis Biochim. Biophys. Acta 1792 2009 651 663
4. R. Betarbet, T.B. Sherer, G. MacKenzie, M. Garcia-Osuna, A.V. Panov, and J.T. Greenamyre Chronic systemic pesticide exposure reproduces features of Parkinson's disease Nat. Neurosci. 3 2000 1301 1306
5. R. Betarbet, T.B. Sherer, and J.T. Greenamyre Animal models of Parkinson's disease Bioessays 24 2002 308 318 (Pubitemid 34305686)
6. M.S. Bhuiyan, and K. Fukunaga Inhibition of HtrA2/Omi ameliorates heart dysfunction following ischemia/reperfusion injury in rat heart in vivo Eur. J. Pharmacol. 557 2007 168 177 (Pubitemid 46186288)
7. Y. Cho, H.J. Son, E.M. Kim, J.H. Choi, S.T. Kim, I.J. Ji, D.H. Choi, T.H. Joh, Y.S. Kim, and O. Hwang Doxycycline is neuroprotective against nigral dopaminergic degeneration by a dual mechanism involving MMP-3 Neurotox. Res. 16 2009 361 371
8. D.H. Choi, O. Hwang, K.H. Lee, J. Lee, M.F. Beal, and Y.S. Kim DJ-1 cleavage by matrix metalloproteinase-3 mediates oxidative stress-induced dopaminergic cell death Antioxid. Redox. Signal 14 2011 2137 2150
9. D.H. Choi, E.M. Kim, H.J. Son, T.H. Joh, Y.S. Kim, D. Kim, M.F. Beal, and O. Hwang A novel intracellular role of matrix metalloproteinase-3 during apoptosis of dopaminergic cells J. Neurochem. 106 2008 405 415 (Pubitemid 351840221)
10. H.J. Choi, Y.J. Jang, H.J. Kim, and O. Hwang Tetrahydrobiopterin is released from and causes preferential death of catecholaminergic cells by oxidative stress Mol. Pharmacol. 58 2000 633 640
11. H.J. Choi, S.W. Kim, S.Y. Lee, and O. Hwang Dopamine-dependent cytotoxicity of tetrahydrobiopterin: a possible mechanism for selective neurodegeneration in Parkinson's disease J. Neurochem. 86 2003 143 152 (Pubitemid 36753855)
12. L. Cilenti, Y. Lee, S. Hess, S. Srinivasula, K.M. Park, D. Junqueira, H. Davis, J.V. Bonventre, E.S. Alnemri, and A.S. Zervos Characterization of a novel and specific inhibitor for the pro-apoptotic protease Omi/HtrA2 J. Biol. Chem. 278 2003 11489 11494 (Pubitemid 36792709)
13. L. Cilenti, M.M. Soundarapandrian, and G.A. Kyriasis Regulation of HAX-1 anti-apoptotic protein by Omi/HtrA2 protease during cell death J. Biol. Chem. 279 2004 50295 50301 (Pubitemid 39577845)
14. F.J. Descamps, E. Martens, F. Ballaux, K. Geboes, and G. Opdenakker In vivo activation of gelatinase B/MMP-9 by trypsin in acute pancreatitis is a permissive factor in streptozotocin-induced diabetes J. Pathol. 204 2004 555 561 (Pubitemid 39585954)
15. F.J. Diaz-Corrales, M. Asanuma, I. Miyazaki, K. Miyoshi, N. Hattori, and N. Ogawa Dopamine induces supernumerary centrosomes and subsequent cell death through Cdk2 up-regulation in dopaminergic neuronal cells Neurotox. Res. 14 2008 295 305
16. C. Han, M.K. Nam, H.J. Park, Y.M. Seong, S. Kang, and H. Rhim Tunicamycin-induced ER stress upregulates the expression of mitochondrial HtrA2 and promotes apoptosis through the cytosolic release of HtrA2 J. Microbiol. Biotechnol. 18 2008 1197 1202
17. J.M. Han, Y.J. Lee, S.Y. Lee, E.M. Kim, Y. Moon, H.W. Kim, and O. Hwang Protective effect of sulforaphane against dopaminergic cell death J. Pharmacol. Exp. Ther. 321 2007 249 256 (Pubitemid 46456990)
18. R. Hedge, S.M. Srinivasula, and Z.J. Zhang Identification of Omi/HtrA2 as a mitochondrial apoptotic serine protease that disrupts inhibitors of apoptosis protein-caspase interaction J. Biol. Chem. 277 2002 432 438 (Pubitemid 34952076)
19. O. Hwang, G. Kim, Y.J. Jang, S.W. Kim, G. Choi, H.J. Choi, S.Y. Jeon, D.G. Lee, and J.D. Lee Synthetic phytoceramides induce apoptosis with higher potency than ceramides Mol. Pharmacol. 59 2001 1249 1255 (Pubitemid 32381605)
20. Y. Irie, M. Saeki, H. Tanaka, Y. Kanemura, S. Otake, Y. Ozono, T. Nagai, Y. Kondo, K. Kudo, Y. Kamisaki, N. Miki, and E. Taira Methamphetamine induces endoplasmic reticulum stress related gene CHOP/Gadd153/ddit3 in dopaminergic cells Cell Tissue Res. 345 2011 231 241
21. S. Jin, M. Kalkum, and M. Overholtzer CIAP1 and the serine protease HtrA2 are involved in a novel p53-dependent apoptosis pathway in mammals Genes Dev. 17 2003 359 367 (Pubitemid 36182195)
22. J.M. Jones, R.L. Albin, E.L. Feldman, K. Simin, T.G. Schuster, W.A. Dunnick, J.T. Collins, C.E. Chrisp, B.A. Taylor, and M.H. Meisler Mnd2: A new mouse model of inherited motor neuron disease Genomics 16 1993 669 677 (Pubitemid 23183487)
23. J.M. Jones, P. Datta, and S.M. Srinivasula Loss of Omi mitochondrial protease activity causes the neuromuscular disorder of mnd2 mutant mice Nature 425 2003 721 727 (Pubitemid 37314315)
24. E.M. Kim, and O. Hwang Role of matrix metalloproteinase-3 in neurodegeneration J. Neurochem. 116 2011 22 32
25. E.M. Kim, E.J. Shin, J.H. Choi, H.J. Son, I.S. Park, T.H. Joh, and O. Hwang Matrix metalloproteinase-3 is increased and participates in neuronal apoptotic signaling downstream of caspase-12 during endoplasmic reticulum stress J. Biol. Chem. 285 2010 16444 16452
26. Y.S. Kim, D.H. Choi, M.L. Block, S. Lorenzl, L. Yang, Y.J. Kim, S. Sugama, B.P. Cho, O. Hwang, S.E. Browne, S.Y. Kim, J.S. Hong, M.F. Beal, and T.H. Joh A pivotal role of matrix metalloproteinase-3 activity in dopaminergic neuronal degeneration via microglial activation FASEB J. 21 2007 179 187 (Pubitemid 46052555)
27. Y.S. Kim, S.S. Kim, J.J. Cho, D.H. Choi, O. Hwang, D.H. Shin, H.S. Chun, M.F. Beal, and T.H. Joh Matrix metalloproteinase-3: a novel signaling proteinase from apoptotic neuronal cells that activates microglia J. Neurosci. 25 2005 3701 3711
28. K. Kishi, M. Muramatsu, D. Jin, K. Furubayashi, S. Takai, H. Tamai, and M. Miyazaki The effects of chymase on matrix metalloproteinase-2 activation in neointimal hyperplasia after balloon injury in dogs Hypertens. Res. 30 2007 77 83
29. S. Krick, S. Shi, and W. Ju Mpv17l protects against mitochondrial oxidative stress and apoptosis by activation of Omi/Htra2 protease Proc. Natl. Acad. Sci. USA 105 2008 14106 141 11
30. J. Levin, A. Giese, K. Boetzel, L. Israel, T. Hogen, G. Nubling, H. Kretzschmar, and S. Lorenzl Increased a-synuclein aggregation following limited cleavage by certain matrix metalloproteinases Exp. Neurol. 215 2009 201 208
31. R.I. Lindstad, I. Sylte, S.O. Mikalsen, P.O. Seglen, E. Berg, and J.O. Winberg Pancreatic trypsin activates human promatrix metalloproteinase-2 J. Mol. Biol. 350 2005 682 698 (Pubitemid 40848667)
32. H.R. Liu, E. Gao, A. Hu, L. Tao, Y. Qu, P. Most, W.J. Koch, T.A. Christopher, B.L. Lopez, and E.S. Alnemri Role of Omi/HtrA2 in apoptotic cell ceath after myocardial ischemia and reperfusion Circulation 111 2005 90 96 (Pubitemid 40070849)
33. M.J. Liu, M.L. Liu, and Y.F. Shen Transgenic mice with neuron-specific overexpression of HtrA2/Omi suggests a neuroprotective role for HtrA2/Omi Biochem. Biophys. Res. Commun. 362 2007 295 300
34. L.M. Martins, I. Iaccarino, T. Tenev, S. Gschmeissner, N.F. Totty, N.R. Lemoine, J. Savopoulos, C.W. Gray, C.L. Creasy, and C. Dingwall The serine protease Omi/HtrA2 regulates apoptosis by binding XIAP through a reaper-like motif J. Biol. Chem. 277 2002 439 444 (Pubitemid 34952077)
35. L.M. Martins, A. Morrison, and K. Klupsch Neuroprotective role of the reaper-realated serine protease HtrA2/Omi revealed by targeted deletion in mice Mol. Cell. Biol. 24 2004 9848 9862 (Pubitemid 39458812)
36. M. Marabese, M. Mazzoletti, F. Vikhanskaya, and M. Broggini HtrA2 enhances the apoptotic functions of p73 on bax Cell Death Differ. 15 2008 849 858 (Pubitemid 351524427)
37. N. Moisoi, K. Klupsch, V. Fedele, P. East, S. Sharma, A. Renton, H. Plun-Favreau, R.E. Edwards, P. Teismann, M.D. Esposti, A.D. Morrison, N.W. Wood, J. Downward, and L.M. Martins Mitochondrial dysfunction triggered by loss of HtrA2 results in the activation of a brain-specific transcriptional stress response Cell Death Differ. 16 2009 449 464
38. H.M. Park, G.Y. Kim, M.K. Nam, G.H. Seong, C. Han, K.C. Chung, S. Kang, and H. Rhim The serine protease HtrA2/Omi cleaves Parkin and irreversibly inactivates its E3 ubiquitin ligase activity Biochem. Biophys. Res. Commun. 387 2009 537 542
39. H.J. Park, S.S. Kim, Y.M. Seong, K.H. Kim, H.G. Goo, E.J. Yoon, D.S. Min, S. Kang, and H. Rhim Beta-amyloid precursor protein is a direct cleavage target of HtrA2 serine protease. Implications for the physiological function of HtrA2 in the mitochondria J. Biol. Chem. 281 2006 34277 34287 (Pubitemid 46036636)
40. A. Rami, M. Kim, and J. Niquet Translocation of the serine protease Omi/HtrA2 from mitochondria into the cytosol upon seizure-induced hippocampal injury in the neonatal rat brain Neurochem. Res. 35 2010 2199 2207
41. W.B. Saunders, K.J. Bayless, and G.E. Davis MMP-1 activation by serine proteases and MMP-10 induces human capillary tubular network collapse and regression in 3D collagen matrices J. Cell Sci. 118 2005 2325 2340 (Pubitemid 40872853)
42. A.H. Schapira Mitochondria in the aetiology and pathogenesis of Parkinson's disease Lancet Neurol. 7 2008 97 109 (Pubitemid 350251942)
43. Y.M. Seong, H.J. Park, G.H. Seong, J.Y. Choi, S.J. Yoon, B.R. Min, S. Kang, and H. Rhim N-terminal truncation circumvents proteolytic degradation of the human HtrA2/Omi serine protease in Escherichia coli: rapid purification of a proteolytically active HtrA2/Omi Protein Expression Purif. 33 2004 200 208 (Pubitemid 38161985)
44. K.M. Strauss, L.M. Martins, H. Plun-Favreau, F.P. Marx, S. Kautzmann, D. Berg, T. Gasser, Z. Wszolek, T. Muller, A. Bornemann, H. Wolburg, J. Downward, O. Riess, J.B. Schulz, and R. Kruger Loss of function mutations in the gene encoding Omi/HtrA2 in Parkinson's disease Hum. Mol. Genet. 14 2005 2099 2111 (Pubitemid 41418010)
45. J.Y. Sung, S.M. Park, C.H. Lee, J.W. Um, H.J. Lee, J. Kim, Y.J. Oh, S.T. Lee, S.R. Paik, and K.C. Chung Proteolytic cleavage of extracellular secreted {alpha}-synuclein via matrix metalloproteinases J. Biol. Chem. 280 2005 25216 25224 (Pubitemid 40934615)
46. E. Tchougounova, A. Lundequist, I. Fajardo, J.O. Winberg, M. Abrink, and G. Pejler A key role for mast cell chymase in the activation of pro-matrix metalloprotease-9 and pro-matrix metalloprotease-2 J. Biol. Chem. 280 2005 9291 9296 (Pubitemid 40409621)
47. A. Trencia, F. Fiory, M.A. Maitan, P. Vito, A.P. Barbagallo, A. Perfetti, C. Miele, P. Hungaro, F. Oriente, and L. Cilenti Omi/HtrA2 promotes cell death by binding and degrading the anti-apoptotic protein ped/pea-15 J. Biol. Chem. 279 2004 46566 46572 (Pubitemid 39518301)
48. G. van Loo, M. van Gurp, B. Depuydt, S.M. Srinivasula, I. Rodriguez, E.S. Alnemri, K. Gevaert, J. Vandekerckhove, W. Declercq, and P. Vandenabeele The serine protease Omi/HtrA2 is released from mitochondria during apoptosis: Omi interacts with caspase-inhibitor XIAP and induces enhanced caspase activity Cell Death Differ. 9 2002 20 26 (Pubitemid 34071990)
49. L. Vande Walle, E. Wirawan, M. Lamkanfi, N. Festjens, J. Verspurten, X. Saelens, T. Vanden Berghe, and P. Vandenabeele The mitochondrial serine protease HtrA2/Omi cleaves RIP1 during apoptosis of Ba/F3 cells induced by growth factor withdrawal Cell Res. 20 2010 421 433
50. A.M. Verhagen, J. Silke, P.G. Ekert, M. Pakushi, H. Kaufmann, L.M. Connolly, C.L. Day, A. Tikoo, R. Burke, and C. Wrobel HtrA2 promotes cell death through its serine protease activity and its ability to antagonize inhibitor of apoptosis proteins J. Biol. Chem. 277 2002 445 454 (Pubitemid 34952078)