Leukocyte calpain deficiency reduces Angiotensin II-induced inflammation and atherosclerosis but not abdominal aortic aneurysms in mice

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 36, Issue 5, 2016, Pages 835-845

  Howatt, Deborah A ^a   Balakrishnan, Anju ^a   Moorleghen, Jessica J ^a   Muniappan, Latha ^a   Rateri, Debra L ^a   Uchida, Haruhito A ^b   Takano, Jiro ^c   Saido, Takaomi C ^c   Chishti, Athar H ^d   Baud, Laurent ^e   Subramanian, Venkateswaran ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b OKAYAMA UNIVERSITY   (Japan)

^c RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

^d TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e INSERM   (France)

Author keywords

angiotensin II; atherosclerosis; calpain; inflammation; macrophages

Indexed keywords

ANGIOTENSIN II; CALPAIN; CALPAIN 1; CALPAIN 2; CALPASTATIN; CALCIUM BINDING PROTEIN; CAPN1 PROTEIN, MOUSE; CAPN2 PROTEIN, MOUSE; CYSTEINE PROTEINASE INHIBITOR; LOW DENSITY LIPOPROTEIN RECEPTOR;

ABDOMINAL AORTA ANEURYSM; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA ARCH; AORTA ATHEROSCLEROSIS; ARTICLE; BONE MARROW DERIVED MACROPHAGE; CELL ADHESION; CONTROLLED STUDY; DISEASE ASSOCIATION; GENE OVEREXPRESSION; HYPERCHOLESTEROLEMIA; IN VITRO STUDY; INFLAMMATION; LEUKOCYTE; MACROPHAGE MIGRATION INHIBITION; MALE; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPLEEN; ANIMAL; AORTIC ANEURYSM, ABDOMINAL; ATHEROSCLEROSIS; BONE MARROW TRANSPLANTATION; C57BL MOUSE; CELL CULTURE; CELL MOTION; CHEMICALLY INDUCED; COCULTURE; DEFICIENCY; DISEASE MODEL; DRUG EFFECTS; ENDOTHELIUM CELL; ENZYMOLOGY; GENETIC PREDISPOSITION; GENETICS; KNOCKOUT MOUSE; LIPID DIET; MACROPHAGE; METABOLISM; PHENOTYPE; TRANSGENIC MOUSE; WHOLE BODY RADIATION;

ANGIOTENSIN II; ANIMALS; AORTIC ANEURYSM, ABDOMINAL; ATHEROSCLEROSIS; BONE MARROW TRANSPLANTATION; CALCIUM-BINDING PROTEINS; CALPAIN; CELL ADHESION; CELL MOVEMENT; CELLS, CULTURED; COCULTURE TECHNIQUES; CYSTEINE PROTEINASE INHIBITORS; DIET, HIGH-FAT; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; GENETIC PREDISPOSITION TO DISEASE; INFLAMMATION; LEUKOCYTES; MACROPHAGES; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; PHENOTYPE; RECEPTORS, LDL; WHOLE-BODY IRRADIATION;

EID: 84960379159     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.116.307285     Document Type: Article

References (43)

1. Daugherty A, Rateri DL, Lu H, Inagami T, Cassis LA, Hypercholesterolemia stimulates angiotensin peptide synthesis and contributes to atherosclerosis through the AT1A receptor. Circulation 2004 110 3849 3857. doi: 10.1161/01.CIR.0000150540.54220.C4
2. Daugherty A, Manning MW, Cassis LA, Angiotensin II promotes atherosclerotic lesions and aneurysms in apolipoprotein E-deficient mice. J Clin Invest 2000 105 1605 1612. doi: 10.1172/JCI7818
3. Saraff K, Babamusta F, Cassis LA, Daugherty A, Aortic dissection precedes formation of aneurysms and atherosclerosis in angiotensin II-infused, apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 2003 23 1621 1626. doi: 10.1161/01.ATV.0000085631.76095.64
4. Cassis LA, Rateri DL, Lu H, Daugherty A, Bone marrow transplantation reveals that recipient AT1a receptors are required to initiate angiotensin II-induced atherosclerosis and aneurysms. Arterioscler Thromb Vasc Biol 2007 27 380 386. doi: 10.1161/01.ATV.0000254680.71485.92
5. Goll DE, Thompson VF, Li H, Wei W, Cong J, The calpain system. Physiol Rev 2003 83 731 801. doi: 10.1152/physrev.00029.2002
6. Sato K, Minegishi S, Takano J, Plattner F, Saito T, Asada A, Kawahara H, Iwata N, Saido TC, Hisanaga S, Calpastatin, an endogenous calpain-inhibitor protein, regulates the cleavage of the Cdk5 activator p35 to p25. J Neurochem 2011 117 504 515. doi: 10.1111/j.1471-4159.2011.07222.x
7. Smolock AR, Mishra G, Eguchi K, Eguchi S, Scalia R, Protein kinase C upregulates intercellular adhesion molecule-1 and leukocyte-endothelium interactions in hyperglycemia via activation of endothelial expressed calpain. Arterioscler Thromb Vasc Biol 2011 31 289 296. doi: 10.1161/ATVBAHA.110.217901
8. Bate N, Gingras AR, Bachir A, Horwitz R, Ye F, Patel B, Goult BT, Critchley DR, Talin contains a C-Terminal calpain2 cleavage site important in focal adhesion dynamics. PLoS One 2012 7 e34461. doi: 10.1371/journal.pone.0034461
9. Kobeissy FH, Liu MC, Yang Z, Zhang Z, Zheng W, Glushakova O, Mondello S, Anagli J, Hayes RL, Wang KK, Degradation of βII-Spectrin Protein by Calpain-2 and Caspase-3 Under Neurotoxic and Traumatic Brain Injury Conditions. Mol Neurobiol 2015 52 696 709. doi: 10.1007/s12035-014-8898-z
10. Hirai S, Kawasaki H, Yaniv M, Suzuki K, Degradation of transcription factors, c-Jun and c-Fos, by calpain. FEBS Lett 1991 287 57 61
11. Carillo S, Pariat M, Steff AM, Roux P, Etienne-Julan M, Lorca T, Piechaczyk M, Differential sensitivity of FOS and JUN family members to calpains. Oncogene 1994 9 1679 1689
12. Fenouille N, Grosso S, Yunchao S, Mary D, Pontier-Bres R, Imbert V, Czerucka D, Caroli-Bosc FX, Peyron JF, Lagadec P, Calpain 2-dependent IκBα degradation mediates CPT-11 secondary resistance in colorectal cancer xenografts. J Pathol 2012 227 118 129. doi: 10.1002/path.3034
13. Kerbiriou M, Teng L, Benz N, Trouvé P, Férec C, The calpain, caspase 12, caspase 3 cascade leading to apoptosis is altered in F508del-CFTR expressing cells. PLoS One 2009 4 e8436. doi: 10.1371/journal.pone.0008436
14. Wolf BB, Goldstein JC, Stennicke HR, Beere H, Amarante-Mendes GP, Salvesen GS, Green DR, Calpain functions in a caspase-independent manner to promote apoptosis-like events during platelet activation. Blood 1999 94 1683 1692
15. Ma J, Wei M, Wang Q, Li J, Wang H, Liu W, Lacefield JC, Greer PA, Karmazyn M, Fan GC, Peng T, Deficiency of Capn4 gene inhibits nuclear factor-κB (NF-κB) protein signaling/inflammation and reduces remodeling after myocardial infarction. J Biol Chem 2012 287 27480 27489. doi: 10.1074/jbc.M112.358929
16. Wendt A, Thompson VF, Goll DE, Interaction of calpastatin with calpain: a review. Biol Chem 2004 385 465 472. doi: 10.1515/BC.2004.054
17. Huang Z, Hoffmann FW, Norton RL, Hashimoto AC, Hoffmann PR, Selenoprotein K is a novel target of m-calpain, and cleavage is regulated by Toll-like receptor-induced calpastatin in macrophages. J Biol Chem 2011 286 34830 34838. doi: 10.1074/jbc.M111.265520
18. Scalia R, Gong Y, Berzins B, Freund B, Feather D, Landesberg G, Mishra G, A novel role for calpain in the endothelial dysfunction induced by activation of angiotensin II type 1 receptor signaling. Circ Res 2011 108 1102 1111. doi: 10.1161/CIRCRESAHA.110.229393
19. Letavernier E, Perez J, Bellocq A, Mesnard L, de Castro Keller A, Haymann JP, Baud L, Targeting the calpain/calpastatin system as a new strategy to prevent cardiovascular remodeling in angiotensin II-induced hypertension. Circ Res 2008 102 720 728. doi: 10.1161/CIRCRESAHA.107.160077
20. Subramanian V, Uchida HA, Ijaz T, Moorleghen JJ, Howatt DA, Balakrishnan A, Calpain inhibition attenuates angiotensin II-induced abdominal aortic aneurysms and atherosclerosis in low-density lipoprotein receptor-deficient mice. J Cardiovasc Pharmacol 2012 59 66 76. doi: 10.1097/FJC.0b013e318235d5ea
21. Subramanian V, Moorleghen JJ, Balakrishnan A, Howatt DA, Chishti AH, Uchida HA, Calpain-2 compensation promotes angiotensin II-induced ascending and abdominal aortic aneurysms in calpain-1 deficient mice. PLoS One 2013 8 e72214. doi: 10.1371/journal.pone.0072214
22. Takano J, Mihira N, Fujioka R, Hosoki E, Chishti AH, Saido TC, Vital role of the calpain-calpastatin system for placental-integrity-dependent embryonic survival. Mol Cell Biol 2011 31 4097 4106. doi: 10.1128/MCB.05189-11
23. Kanters E, Pasparakis M, Gijbels MJ, Vergouwe MN, Partouns-Hendriks I, Fijneman RJ, Clausen BE, Förster I, Kockx MM, Rajewsky K, Kraal G, Hofker MH, de Winther MP, Inhibition of NF-kappaB activation in macrophages increases atherosclerosis in LDL receptor-deficient mice. J Clin Invest 2003 112 1176 1185. doi: 10.1172/JCI18580
24. Park SH, Sui Y, Gizard F, Xu J, Rios-Pilier J, Helsley RN, Han SS, Zhou C, Myeloid-specific IκB kinase β deficiency decreases atherosclerosis in low-density lipoprotein receptor-deficient mice. Arterioscler Thromb Vasc Biol 2012 32 2869 2876. doi: 10.1161/ATVBAHA.112.254573
25. Perkins ND, Integrating cell-signalling pathways with NF-kappaB and IKK function. Nat Rev Mol Cell Biol 2007 8 49 62. doi: 10.1038/nrm2083
26. Shumway SD, Maki M, Miyamoto S, The PEST domain of IkappaBalpha is necessary and sufficient for in vitro degradation by mu-calpain. J Biol Chem 1999 274 30874 30881
27. Huang Z, Rose AH, Hoffmann FW, Hashimoto AS, Bertino P, Denk T, Takano J, Iwata N, Saido TC, Hoffmann PR, Calpastatin prevents NF-κB-mediated hyperactivation of macrophages and attenuates colitis. J Immunol 2013 191 3778 3788. doi: 10.4049/jimmunol.1300972
28. Chen F, Demers LM, Vallyathan V, Lu Y, Castranova V, Shi X, Impairment of NF-kappaB activation and modulation of gene expression by calpastatin. Am J Physiol Cell Physiol 2000 279 C709 C716
29. Cassis LA, Gupte M, Thayer S, Zhang X, Charnigo R, Howatt DA, Rateri DL, Daugherty A, ANG II infusion promotes abdominal aortic aneurysms independent of increased blood pressure in hypercholesterolemic mice. Am J Physiol Heart Circ Physiol 2009 296 H1660 H1665. doi: 10.1152/ajpheart.00028.2009
30. Westerterp M, Murphy AJ, Wang M, Deficiency of ATP-binding cassette transporters A1 and G1 in macrophages increases inflammation and accelerates atherosclerosis in mice. Circ Res 2013 112 1456 1465. doi: 10.1161/CIRCRESAHA.113.301086
31. Yvan-Charvet L, Ranalletta M, Wang N, Han S, Terasaka N, Li R, Welch C, Tall AR, Combined deficiency of ABCA1 and ABCG1 promotes foam cell accumulation and accelerates atherosclerosis in mice. J Clin Invest 2007 117 3900 3908. doi: 10.1172/JCI33372
32. Aiello RJ, Brees D, Bourassa PA, Royer L, Lindsey S, Coskran T, Haghpassand M, Francone OL, Increased atherosclerosis in hyperlipidemic mice with inactivation of ABCA1 in macrophages. Arterioscler Thromb Vasc Biol 2002 22 630 637
33. Yokoyama S, Arakawa R, Wu CA, Iwamoto N, Lu R, Tsujita M, Abe-Dohmae S, Calpain-mediated ABCA1 degradation: post-Translational regulation of ABCA1 for HDL biogenesis. Biochim Biophys Acta 2012 1821 547 551. doi: 10.1016/j.bbalip.2011.07.017
34. Wang N, Chen W, Linsel-Nitschke P, Martinez LO, Agerholm-Larsen B, Silver DL, Tall AR, A PEST sequence in ABCA1 regulates degradation by calpain protease and stabilization of ABCA1 by apoA-I. J Clin Invest 2003 111 99 107. doi: 10.1172/JCI16808
35. Martinez LO, Agerholm-Larsen B, Wang N, Chen W, Tall AR, Phosphorylation of a pest sequence in ABCA1 promotes calpain degradation and is reversed by ApoA-I. J Biol Chem 2003 278 37368 37374. doi: 10.1074/jbc.M307161200
36. Libby P, Inflammation in atherosclerosis. Nature 2002 420 868 874. doi: 10.1038/nature01323
37. Potteaux S, Gautier EL, Hutchison SB, van Rooijen N, Rader DJ, Thomas MJ, Sorci-Thomas MG, Randolph GJ, Suppressed monocyte recruitment drives macrophage removal from atherosclerotic plaques of Apoe-/-mice during disease regression. J Clin Invest 2011 121 2025 2036. doi: 10.1172/JCI43802
38. Donadelli R, Abbate M, Zanchi C, Corna D, Tomasoni S, Benigni A, Remuzzi G, Zoja C, Protein traffic activates NF-kB gene signaling and promotes MCP-1-dependent interstitial inflammation. Am J Kidney Dis 2000 36 1226 1241. doi: 10.1053/ajkd.2000.19838
39. Rego D, Kumar A, Nilchi L, Wright K, Huang S, Kozlowski M, IL-6 production is positively regulated by two distinct Src homology domain 2-containing tyrosine phosphatase-1 (SHP-1)-dependent CCAAT/enhancer-binding protein β and NF-κB pathways and an SHP-1-independent NF-κB pathway in lipopolysaccharide-stimulated bone marrow-derived macrophages. J Immunol 2011 186 5443 5456. doi: 10.4049/jimmunol.1003551
40. Daugherty A, Rateri DL, Charo IF, Owens AP, Howatt DA, Cassis LA, Angiotensin II infusion promotes ascending aortic aneurysms: attenuation by CCR2 deficiency in apoE-/-mice. Clin Sci (Lond) 2010 118 681 689. doi: 10.1042/CS20090372
41. Wang Q, Ren J, Morgan S, Liu Z, Dou C, Liu B, Monocyte chemoattractant protein-1 (MCP-1) regulates macrophage cytotoxicity in abdominal aortic aneurysm. PLoS One 2014 9 e92053. doi: 10.1371/journal.pone.0092053
42. Gu L, Okada Y, Clinton SK, Gerard C, Sukhova GK, Libby P, Rollins BJ, Absence of monocyte chemoattractant protein-1 reduces atherosclerosis in low density lipoprotein receptor-deficient mice. Mol Cell 1998 2 275 281
43. Tieu BC, Lee C, Sun H, Lejeune W, Recinos A III, Ju X, Spratt H, Guo DC, Milewicz D, Tilton RG, Brasier AR, An adventitial IL-6/MCP1 amplification loop accelerates macrophage-mediated vascular inflammation leading to aortic dissection in mice. J Clin Invest 2009 119 3637 3651. doi: 10.1172/JCI38308