CD36 Is a Matrix Metalloproteinase-9 Substrate That Stimulates Neutrophil Apoptosis and Removal during Cardiac Remodeling

Circulation: Cardiovascular Genetics

Volumn 9, Issue 1, 2016, Pages 14-25

  Deleon Pennell, Kristine Y ^a,b   Tian, Yuan ^a,b   Zhang, Bai ^d   Cates, Courtney A ^a,b   Iyer, Rugmani Padmanabhan ^a,b   Cannon, Presley ^a,b   Shah, Punit ^d   Aiyetan, Paul ^d   Halade, Ganesh V ^e   Ma, Yonggang ^a   Flynn, Elizabeth ^a,b   Zhang, Zhen ^d   Jin, Yu Fang ^b,c   Zhang, Hui ^d   Lindsey, Merry L ^a,b,f  

^a UNIVERSITY OF MISSISSIPPI SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MISSISSIPPI MEDICAL CENTER   (United States)

^c The University of Texas at San Antonio   (United States)

^d JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e University of Alabama at Birmingham and Birmingham Veterans Affairs Medical Center   (United States)

^f G V SONNY MONTGOMERY VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

extracellular matrix; immunoblotting; infarction; inflammation; myocardial; proteomics

Indexed keywords

CD36 ANTIGEN; GELATINASE B; MMP9 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CARTILAGE; CELL ISOLATION; CONTROLLED STUDY; DOWN REGULATION; FEMALE; GENE DELETION; HEART INFARCTION; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IN VITRO STUDY; IN VIVO STUDY; MACROPHAGE; MALE; MOUSE; NEUTROPHIL; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEOMICS; UPREGULATION; ANIMAL; BIOSYNTHESIS; CARDIAC MUSCLE CELL; GENE EXPRESSION REGULATION; GENETICS; HEART VENTRICLE; METABOLISM; MUTANT MOUSE STRAIN; PATHOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; ANTIGENS, CD36; APOPTOSIS; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HEART VENTRICLES; MALE; MATRIX METALLOPROTEINASE 9; MICE; MICE, MUTANT STRAINS; MYOCARDIAL INFARCTION; MYOCYTES, CARDIAC; NEUTROPHILS; PROTEOLYSIS; SIGNAL TRANSDUCTION;

EID: 84959563258     PISSN: 1942325X     EISSN: 19423268     Source Type: Journal    
DOI: 10.1161/CIRCGENETICS.115.001249     Document Type: Article

References (48)

1. Roger VL, Go AS, Lloyd-Jones DM, Benjamin EJ, Berry JD, Borden WB, American Heart Association Statistics Committee and Stroke Statistics Subcommittee Heart disease and stroke statistics-2012 update: a report from the American Heart Association. Circulation 2012 125 e2 e220. doi: 10.1161/CIR.0b013e31823ac046.
2. Jourdan-Lesaux C, Zhang J, Lindsey ML., Extracellular matrix roles during cardiac repair. Life Sci 2010 87 391 400. doi: 10.1016/j.lfs.2010.07.010.
3. Zamilpa R, Zhang J, Chiao YA, de Castro Brás LE, Halade GV, Ma Y, Cardiac wound healing post-myocardial infarction: a novel method to target extracellular matrix remodeling in the left ventricle. Methods Mol Biol 2013 1037 313 324. doi: 10.1007/978-1-62703-505-7-18.
4. Lindsey ML., MMP induction and inhibition in myocardial infarction. Heart Fail Rev 2004 9 7 19. doi: 10.1023/B:HREV.0000011390.44039.b7.
5. Van Lint P, Libert C., Chemokine and cytokine processing by matrix metalloproteinases and its effect on leukocyte migration and inflammation. J Leukoc Biol 2007 82 1375 1381. doi: 10.1189/jlb.0607338.
6. Ducharme A, Frantz S, Aikawa M, Rabkin E, Lindsey M, Rohde LE, Targeted deletion of matrix metalloproteinase-9 attenuates left ventricular enlargement and collagen accumulation after experimental myocardial infarction. J Clin Invest 2000 106 55 62. doi: 10.1172/JCI8768.
7. Tao ZY, Cavasin MA, Yang F, Liu YH, Yang XP., Temporal changes in matrix metalloproteinase expression and inflammatory response associated with cardiac rupture after myocardial infarction in mice. Life Sci 2004 74 1561 1572
8. Heymans S, Luttun A, Nuyens D, Theilmeier G, Creemers E, Moons L, Inhibition of plasminogen activators or matrix metalloproteinases prevents cardiac rupture but impairs therapeutic angiogenesis and causes cardiac failure. Nat Med 1999 5 1135 1142. doi: 10.1038/13459.
9. Zamilpa R, Lopez EF, Chiao YA, Dai Q, Escobar GP, Hakala K, Proteomic analysis identifies in vivo candidate matrix metalloproteinase-9 substrates in the left ventricle post-myocardial infarction. Proteomics 2010 10 2214 2223. doi: 10.1002/pmic.200900587.
10. Zitka O, Kukacka J, Krizkova S, Huska D, Adam V, Masarik M, Matrix metalloproteinases. Curr Med Chem 2010 17 3751 3768
11. Lindsey ML, Escobar GP, Dobrucki LW, Goshorn DK, Bouges S, Mingoia JT, Matrix metalloproteinase-9 gene deletion facilitates angiogenesis after myocardial infarction. Am J Physiol Heart Circ Physiol 2006 290 H232 H239. doi: 10.1152/ajpheart.00457.2005.
12. Vu TH, Shipley JM, Bergers G, Berger JE, Helms JA, Hanahan D, MMP-9/gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes. Cell 1998 93 411 422
13. de Castro Brás LE, Ramirez TA, DeLeon-Pennell KY, Chiao YA, Ma Y, Dai Q, Texas 3-step decellularization protocol: looking at the cardiac extracellular matrix. J Proteomics 2013 86 43 52. doi: 10.1016/j.jprot.2013.05.004.
14. Zhang H, Li XJ, Martin DB, Aebersold R., Identification and quantification of N-linked glycoproteins using hydrazide chemistry, stable isotope labeling and mass spectrometry. Nat Biotechnol 2003 21 660 666. doi: 10.1038/nbt827.
15. Tian Y, Zhou Y, Elliott S, Aebersold R, Zhang H., Solid-phase extraction of N-linked glycopeptides. Nat Protoc 2007 2 334 339. doi: 10.1038/nprot.2007.42.
16. Zhou Y, Aebersold R, Zhang H., Isolation of N-linked glycopeptides from plasma. Anal Chem 2007 79 5826 5837. doi: 10.1021/ac0623181.
17. Palmisano G, Melo-Braga MN, Engholm-Keller K, Parker BL, Larsen MR., Chemical deamidation: a common pitfall in large-scale N-linked glycoproteomic mass spectrometry-based analyses. J Proteome Res 2012 11 1949 1957. doi: 10.1021/pr2011268.
18. Wright HT., Nonenzymatic deamidation of asparaginyl and glutaminyl residues in proteins. Crit Rev Biochem Mol Biol 1991 26 1 52. doi: 10.3109/10409239109081719.
19. Vizcaíno JA, Deutsch EW, Wang R, Csordas A, Reisinger F, Ríos D, ProteomeXchange provides globally coordinated proteomics data submission and dissemination. Nat Biotechnol 2014 32 223 226. doi: 10.1038/nbt.2839.
20. Huang da W, Sherman BT, Lempicki RA., Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009 4 44 57. doi: 10.1038/nprot.2008.211.
21. Huang W, Kim J, Jha S, Aboul-ela F., A mechanism for S-adenosyl methionine assisted formation of a riboswitch conformation: a small molecule with a strong arm. Nucleic Acids Res 2009 37 6528 6539. doi: 10.1093/nar/gkp664.
22. Salwinski L, Miller CS, Smith AJ, Pettit FK, Bowie JU, Eisenberg D., The Database of Interacting Proteins: 2004 update. Nucleic Acids Res 2004 32 database issue D449 D451. doi: 10.1093/nar/gkh086.
23. Jensen LJ, Kuhn M, Stark M, Chaffron S, Creevey C, Muller J, STRING 8-a global view on proteins and their functional interactions in 630 organisms. Nucleic Acids Res 2009 37 database issue D412 D416. doi: 10.1093/nar/gkn760.
24. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 2003 13 2498 2504. doi: 10.1101/gr.1239303.
25. Deleon-Pennell KY, de Castro Brás LE, Lindsey ML., Circulating Porphyromonas gingivalis lipopolysaccharide resets cardiac homeostasis in mice through a matrix metalloproteinase-9-dependent mechanism. Physiol Rep 2013 1 e00079. doi: 10.1002/phy2.79.
26. DeLeon-Pennell KY, de Castro Brás LE, Iyer RP, Bratton DR, Jin YF, Ripplinger CM, P. gingivalis lipopolysaccharide intensifies inflammation post-myocardial infarction through matrix metalloproteinase-9. J Mol Cell Cardiol 2014 76 218 226. doi: 10.1016/j.yjmcc.2014.09.007.
27. Iyer RP, Patterson NL, Zouein FA, Ma Y, Dive V, de Castro Brás LE, Early matrix metalloproteinase-12 inhibition worsens post-myocardial infarction cardiac dysfunction by delaying inflammation resolution. Int J Cardiol 2015 185 198 208. doi: 10.1016/j.ijcard.2015.03.054.
28. Zamilpa R, Kanakia R, Cigarroa J IV, Dai Q, Escobar GP, Martinez H, CC chemokine receptor 5 deletion impairs macrophage activation and induces adverse remodeling following myocardial infarction. Am J Physiol Heart Circ Physiol 2011 300 H1418 H1426. doi: 10.1152/ajpheart.01002.2010.
29. Oh H, Siano B, Diamond S., Neutrophil isolation protocol. J Vis Exp 2008 17 745
30. Qin L, Kim E, Ratan R, Lee FS, Cho S., Genetic variant of BDNF (Val66Met) polymorphism attenuates stroke-induced angiogenic responses by enhancing anti-angiogenic mediator CD36 expression. J Neurosci 2011 31 775 783. doi: 10.1523/JNEUROSCI.4547-10.2011.
31. Seftor RE, Seftor EA, Stetler-Stevenson WG, Hendrix MJ., The 72 kDa type IV collagenase is modulated via differential expression of alpha v beta 3 and alpha 5 beta 1 integrins during human melanoma cell invasion. Cancer Res 1993 53 3411 3415
32. Swerlick RA, Lee KH, Wick TM, Lawley TJ., Human dermal microvascular endothelial but not human umbilical vein endothelial cells express CD36 in vivo and in vitro. J Immunol 1992 148 78 83
33. Fadok VA, Warner ML, Bratton DL, Henson PM., CD36 is required for phagocytosis of apoptotic cells by human macrophages that use either a phosphatidylserine receptor or the vitronectin receptor (alpha v beta 3). J Immunol 1998 161 6250 6257
34. Ma Y, Yabluchanskiy A, Lindsey ML., Neutrophil roles in left ventricular remodeling following myocardial infarction. Fibrogenesis Tissue Repair 2013 6 11. doi: 10.1186/1755-1536-6-11.
35. Bratton DL, Henson PM., Neutrophil clearance: when the party is over, clean-up begins. Trends Immunol 2011 32 350 357. doi: 10.1016/j.it.2011.04.009.
36. Loison F, Zhu H, Karatepe K, Kasorn A, Liu P, Ye K, Proteinase 3-dependent caspase-3 cleavage modulates neutrophil death and inflammation. J Clin Invest 2014 124 4445 4458. doi: 10.1172/JCI76246.
37. Savill J, Hogg N, Ren Y, Haslett C., Thrombospondin cooperates with CD36 and the vitronectin receptor in macrophage recognition of neutrophils undergoing apoptosis. J Clin Invest 1992 90 1513 1522. doi: 10.1172/JCI116019.
38. Cheah FC, Hampton MB, Darlow BA, Winterbourn CC, Vissers MC., Detection of apoptosis by caspase-3 activation in tracheal aspirate neutrophils from premature infants: relationship with NF-kappaB activation. J Leukoc Biol 2005 77 432 437. doi: 10.1189/jlb.0904520.
39. Kirschnek S, Vier J, Gautam S, Frankenberg T, Rangelova S, Eitz-Ferrer P, Molecular analysis of neutrophil spontaneous apoptosis reveals a strong role for the pro-apoptotic BH3-only protein Noxa. Cell Death Differ 2011 18 1805 1814. doi: 10.1038/cdd.2011.69.
40. Frumento G, Ottonello L, Bertolotto M, Franchello S, Melioli G, Dallegri F., Spontaneous apoptosis in neutrophils is associated with downregulation of HLA Class I and is prevented by ligation of Class I. J Leukoc Biol 2000 68 873 880
41. Savill JS, Wyllie AH, Henson JE, Walport MJ, Henson PM, Haslett C., Macrophage phagocytosis of aging neutrophils in inflammation. Programmed cell death in the neutrophil leads to its recognition by macrophages. J Clin Invest 1989 83 865 875. doi: 10.1172/JCI113970.
42. Akgul C, Moulding DA, Edwards SW., Molecular control of neutrophil apoptosis. FEBS Lett 2001 487 318 322
43. Irie H, Krukenkamp IB, Brinkmann JF, Gaudette GR, Saltman AE, Jou W, Myocardial recovery from ischemia is impaired in CD36-null mice and restored by myocyte CD36 expression or medium-chain fatty acids. Proc Natl Acad Sci USA 2003 100 6819 6824. doi: 10.1073/pnas.1132094100.
44. Patterson NL, Iyer RP, de Castro Brás LE, Li Y, Andrews TG, Aune GJ, Using proteomics to uncover extracellular matrix interactions during cardiac remodeling. Proteomics Clin Appl 2013 7 516 527. doi: 10.1002/prca.201200100.
45. Bonen A, Tandon NN, Glatz JF, Luiken JJ, Heigenhauser GJ., The fatty acid transporter FAT/CD36 is upregulated in subcutaneous and visceral adipose tissues in human obesity and type 2 diabetes. Int J Obes (Lond) 2006 30 877 883. doi: 10.1038/sj.ijo.0803212.
46. Fadok VA, Bratton DL, Konowal A, Freed PW, Westcott JY, Henson PM., Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-beta, PGE2, and PAF. J Clin Invest 1998 101 890 898. doi: 10.1172/JCI1112.
47. Hudson MP, Armstrong PW, Ruzyllo W, Brum J, Cusmano L, Krzeski P, Effects of selective matrix metalloproteinase inhibitor (PG-116800) to prevent ventricular remodeling after myocardial infarction: results of the PREMIER (Prevention of Myocardial Infarction Early Remodeling) trial. J Am Coll Cardiol 2006 48 15 20. doi: 10.1016/j.jacc.2006.02.055.
48. Benites-Zapata VA, Hernandez AV, Nagarajan V, Cauthen CA, Starling RC, Tang WH., Usefulness of neutrophil-to-lymphocyte ratio in risk stratification of patients with advanced heart failure. Am J Cardiol 2015 115 57 61. doi: 10.1016/j.amjcard.2014.10.008.