MMP-2 is localized to the mitochondria-associated membrane of the heart

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 306, Issue 5, 2014, Pages

  Hughes, Bryan G ^a   Fan, Xiaohu ^a   Cho, Woo Jung ^a   Schulz, Richard ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Calreticulin; Matrix metalloproteinase 2; Mitochondria; Mitochondria associated membrane

Indexed keywords

CALRETICULIN; GELATINASE A; GELATINASE B; INTERSTITIAL COLLAGENASE; MITOCHONDRIAL PROTEIN; CALRETICULIN, HUMAN; HYBRID PROTEIN; MMP2 PROTEIN, MOUSE; MMP2 PROTEIN, RAT;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CALCIUM SIGNALING; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENZYME ACTIVITY; HEART MITOCHONDRION; HEART MUSCLE CELL; HEART MUSCLE FIBER MEMBRANE; HEART PROTECTION; IMMUNOGOLD ELECTRON MICROSCOPY; IN VITRO STUDY; INTRACELLULAR SPACE; ISCHEMIC PRECONDITIONING; MALE; MITOCHONDRIA ASSOCIATED MEMBRANE; MUSCLE FIBRIL; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEGRADATION; RAT; REPERFUSION INJURY; ANIMAL; C57BL MOUSE; CELL LINE; ENDOPLASMIC RETICULUM; ENZYMOLOGY; GENETIC TRANSFECTION; GENETICS; INTRACELLULAR MEMBRANE; KNOCKOUT MOUSE; METABOLISM; MITOCHONDRIA-ASSOCIATED MEMBRANE; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; MOUSE; SPRAGUE DAWLEY RAT; ULTRASTRUCTURE;

CALRETICULIN; MATRIX METALLOPROTEINASE 2; MITOCHONDRIA; MITOCHONDRIA-ASSOCIATED MEMBRANE;

ANIMALS; CALCIUM SIGNALING; CALRETICULIN; CELL LINE; ENDOPLASMIC RETICULUM; INTRACELLULAR MEMBRANES; MALE; MATRIX METALLOPROTEINASE 2; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIA, HEART; MITOCHONDRIAL MEMBRANES; MYOCYTES, CARDIAC; PROTEOLYSIS; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT FUSION PROTEINS; TRANSFECTION;

EID: 84899417766     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00909.2013     Document Type: Article

References (48)

1. Ali MA, Cho WJ, Hudson B, Kassiri Z, Granzier H, Schulz R. Titin is a target of matrix metalloproteinase-2. Circulation 122: 2039-2047, 2010.
2. Ali MA, Chow AK, Kandasamy AD, Fan X, West LJ, Crawford BD, Simmen T, Schulz R. Mechanisms of cytosolic targeting of matrix metalloproteinase-2. J Cell Physiol 227: 3397-3404, 2012.
3. Area-Gomez E, de Groof AJ, Boldogh I, Bird TD, Gibson GE, Koehler CM, Yu WH, Duff KE, Yaffe MP, Pon LA, Schon EA. Presenilins are enriched in endoplasmic reticulum membranes associated with mitochondria. Am J Pathol 175: 1810-1816, 2009.
4. Arnaudeau S, Frieden M, Nakamura K, Castelbou C, Michalak M, Demaurex N. Calreticulin differentially modulates calcium uptake and release in the endoplasmic reticulum and mitochondria. J Biol Chem 277: 46696-46705, 2002.
5. Berman B, Perez OA, Zell D. Update on rosacea and anti-inflammatorydose doxycycline. Drugs Today (Barc) 43: 27-34, 2007.
6. Caton J, Ryan ME. Clinical studies on the management of periodontal diseases utilizing subantimicrobial dose doxycycline (SDD). Pharmacol Res 63: 114-120, 2011.
7. Cauwe B, Opdenakker G. Intracellular substrate cleavage: a novel dimension in the biochemistry, biology and pathology of matrix metalloproteinases. Crit Rev Biochem Mol Biol 45: 351-423, 2010.
8. Cheung PY, Sawicki G, Wozniak M, Wang W, Radomski MW, Schulz R. Matrix metalloproteinase-2 contributes to ischemia-reperfusion injury in the heart. Circulation 101: 1833-1839, 2000.
9. Claros MG, Vincens P. Computational method to predict mitochondrially imported proteins and their targeting sequences. Eur J Biochem 241: 779-786, 1996.
10. Claycomb WC, Lanson NA, Stallworth BS, Egeland DB, Delcarpio JB, Bahinski A, Izzo NJ. HL-1 cells: a cardiac muscle cell line that contracts and retains phenotypic characteristics of the adult cardiomyocyte. Proc Natl Acad Sci USA 95: 2979-2984, 1998.
11. Coussens LM, Fingleton B, Matrisian LM. Matrix metalloproteinase inhibitors and cancer: trials and tribulations. Science 295: 2387-2392, 2002.
12. Csordás G, Renken C, Várnai P, Walter L, Weaver D, Buttle KF, Balla T, Mannella CA, Hajnóczky G. Structural and functional features and significance of the physical linkage between ER and mitochondria. J Cell Biol 174: 915-921, 2006.
13. Dean RA, Overall CM. Proteomics discovery of metalloproteinase substrates in the cellular context by iTRAQ labeling reveals a diverse MMP-2 substrate degradome. Mol Cell Proteomics 6: 611-623, 2007.
14. Dormán G, Cseh S, Hajdú I, Barna L, Kónya D, Kupai K, Kovács L, Ferdinandy P. Matrix metalloproteinase inhibitors. Drugs 70: 949-964, 2010.
15. Emanuelsson O, Nielsen H, Brunak S, von Heijne G. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300: 1005-1016, 2000.
16. Fingleton B. MMP inhibitor clinical trials-the past, present, and future. In: The Cancer Degradome, edited by Edwards D, Høyer-Hansen G, Blasi F, and Sloane B. New York: Springer, 2008, p. 759-785.
17. Fingleton B. MMPs as therapeutic targets-still a viable option? Semin Cell Dev Biol 19: 61-68, 2008.
18. Gabaldón T. Computational approaches for the prediction of protein function in the mitochondrion. Am J Physiol Cell Physiol 291: C1121-C1128, 2006.
19. Hughes BG, Hekimi S. A mild impairment of mitochondrial electron transport has sex-specific effects on lifespan and aging in mice. PLoS One 6: e26116, 2011.
20. Ilkow CS, Weckbecker D, Cho WJ, Meier S, Beatch MD, Goping IS, Herrmann JM, Hobman TC. The rubella virus capsid protein inhibits mitochondrial import. J Virol 84: 119-130, 2010.
21. Itoh T, Ikeda T, Gomi H, Nakao S, Suzuki T, Itohara S. Unaltered secretion of β-amyloid precursor protein in gelatinase A (matrix metalloproteinase 2)-deficient mice. J Biol Chem 272: 22389-22392, 1997.
22. Jacob-Ferreira AL, Kondo MY, Baral PK, James MN, Holt A, Fan X, Schulz R. Phosphorylation status of 72 kDa MMP-2 determines its structure and activity in response to peroxynitrite. PLoS One 8: e71794, 2013.
23. Jia L, Xu M, Zhen W, Shen X, Zhu Y, Wang W, Wang X. Novel anti-oxidative role of calreticulin in protecting A549 human type II alveolar epithelial cells against hypoxic injury. Am J Physiol Cell Physiol 294: C47-C55, 2008.
24. Koo BH, Kim YH, Han JH, Kim DS. Dimerization of matrix metalloproteinase-2 (MMP-2): functional implication in MMP-2 activation. J Biol Chem 287: 22643-22653, 2012.
25. Kowluru RA, Mohammad G, dos Santos JM, Zhong Q. Abrogation of MMP-9 gene protects against the development of retinopathy in diabetic mice by preventing mitochondrial damage. Diabetes 60: 3023-3033, 2011.
26. Kumar M, Verma R, Raghava GPS. Prediction of mitochondrial proteins using support vector machine and hidden Markov model. J Biol Chem 281: 5357-5363, 2006.
27. Limb GA, Matter K, Murphy G, Cambrey AD, Bishop PN, Morris GE, Khaw PT. Matrix metalloproteinase-1 associates with intracellular organelles and confers resistance to lamin A/C degradation during apoptosis. Am J Pathol 166: 1555-1563, 2005.
28. Liu X, Xu F, Fu Y, Liu F, Sun S, Wu X. Calreticulin induces delayed cardioprotection through mitogen-activated protein kinases. Proteomics 6: 3792-3800, 2006.
29. Lovett DH, Mahimkar R, Raffai RL, Cape L, Maklashina E, Cecchini G, Karliner JS. A novel intracellular isoform of matrix metalloproteinase-2 induced by oxidative stress activates innate immunity. PLoS One 7: e34177, 2012.
30. Lovett DH, Mahimkar R, Raffai RL, Cape L, Zhu BQ, Jin ZQ, Baker AJ, Karliner JS. N-terminal truncated intracellular matrix metalloproteinase-2 induces cardiomyocyte hypertrophy, inflammation and systolic heart failure. PLoS One 8: e68154, 2013.
31. Michalak M, Groenendyk J, Szabo E, Gold LI, Opas M. Calreticulin, a multi-process calcium-buffering chaperone of the endoplasmic reticulum. Biochem J 417: 651-666, 2009.
32. Mickelson JR, Greaser ML, Marsh BB. Purification of skeletal-muscle mitochondria by density-gradient centrifugation with Percoll. Anal Biochem 109: 255-260, 1980.
33. Mohammad G, Kowluru RA. Novel role of mitochondrial matrix metalloproteinase-2 in the development of diabetic retinopathy. Invest Ophthalml Vis Sci 52: 3832-3841, 2011.
34. Moshal KS, Tipparaju SM, Vacek TP, Kumar M, Singh M, Frank IE, Patibandla PK, Tyagi N, Rai J, Metreveli N, Rodriguez WE, Tseng MT, Tyagi SC. Mitochondrial matrix metalloproteinase activation decreases myocyte contractility in hyperhomocysteinemia. Am J Physiol Heart Circ Physiol 295: H890-H897, 2008.
35. Murphy E, Steenbergen C. Mechanisms underlying acute protection from cardiac ischemia-reperfusion injury. Physiol Rev 88: 581-609, 2008.
36. Pacher P, Beckman JS, Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol Rev 87: 315-424, 2007.
37. Raturi A, Simmen T. Where the endoplasmic reticulum and the mitochondrion tie the knot: the mitochondria-associated membrane (MAM). Biochim Biophys Acta 1833: 213-224, 2013.
38. Santos JM, Tewari S, Lin JY, Kowluru RA. Interrelationship between activation of matrix metalloproteinases and mitochondrial dysfunction in the development of diabetic retinopathy. Biochem Biophys Res Commun 438: 760-764, 2013.
39. Sawicki G, Leon H, Sawicka J, Sariahmetoglu M, Schulze CJ, Scott PG, Szczesna-Cordary D, Schulz R. Degradation of myosin light chain in isolated rat hearts subjected to ischemia-reperfusion injury. Circulation 112: 544-552, 2005.
40. Schulz R. Intracellular targets of matrix metalloproteinase-2 in cardiac disease: rationale and therapeutic approaches. Annu Rev Pharmacoly Toxicol 47: 211-242, 2007.
41. Small I, Peeters N, Legeai F, Lurin C. Predotar: a tool for rapidly screening proteomes for N-terminal targeting sequences. Proteomics 4: 1581-1590, 2004.
42. Sung MM, Schulz CG, Wang W, Sawicki G, Bautista-López NL, Schulz R. Matrix metalloproteinase-2 degrades the cytoskeletal protein α-actinin in peroxynitrite mediated myocardial injury. J Mol Cell Cardiol 43: 429-436, 2007.
43. Vacek TP, Metreveli N, Tyagi N, Vacek JC, Pagni S, Tyagi SC. Electrical stimulation of cardiomyocytes activates mitochondrial matrix metalloproteinase causing electrical remodeling. Biochem Biophys Res Commun 404: 762-766, 2011.
44. Viappiani S, Nicolescu AC, Holt A, Sawicki G, Crawford BD, León H, van Mulligen T, Schulz R. Activation and modulation of 72 kDa matrix metalloproteinase-2 by peroxynitrite and glutathione. Biochem Pharmacol 77: 826-834, 2009.
45. Wang W, Schulze CJ, Suarez-Pinzon WL, Dyck JR, Sawicki G, Schulz R. Intracellular action of matrix metalloproteinase-2 accounts for acute myocardial ischemia and reperfusion injury. Circulation 106: 1543-1549, 2002.
46. Wu X, Liu X, Zhu X, Tang C. Hypoxic preconditioning induces delayed cardioprotection through p38 MAPK-mediated calreticulin upregulation. Shock 27: 572-577, 2007.
47. Yu CS, Chen YC, Lu CH, Hwang JK. Prediction of protein subcellular localization. Proteins 64: 643-651, 2006.
48. Zhou HZ, Ma X, Gray MO, Zhu BQ, Nguyen AP, Baker AJ, Simonis U, Cecchini G, Lovett DH, Karliner JS. Transgenic MMP-2 expression induces latent cardiac mitochondrial dysfunction. Biochem Biophys Res Commun 358: 189-195, 2007.