Increased expression of matrix metalloproteinase-1 in systemic vessels of preeclamptic women: A critical mediator of vascular dysfunction

American Journal of Pathology

Volumn 178, Issue 1, 2011, Pages 451-460

  Estrada Gutierrez, Guadalupe ^a,b   Cappello, Renato E ^a   Mishra, Nikita ^a   Romero, Roberto ^c,d,e   Strauss III, Jerome F ^a   Walsh, Scott W ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY MEDICAL CENTER   (United States)

^b INSTITUTO NACIONAL DE PERINATOLOGÍA   (Mexico)

^c EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^d HUTZEL HOSPITAL   (United States)

^e WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN; COLLAGEN TYPE 1; COLLAGEN TYPE 1ALPHA; INTERLEUKIN 8; INTERSTITIAL COLLAGENASE; PROTEINASE ACTIVATED RECEPTOR 1; REACTIVE OXYGEN METABOLITE; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ADULT; ARTICLE; BLOOD SAMPLING; BLOOD VESSEL; BLOOD VESSEL REACTIVITY; CELL ACTIVATION; CELL CULTURE; CHEMOTAXIS; CONTROLLED STUDY; CYTOKINE RELEASE; FEMALE; GENE EXPRESSION; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPERTENSION; MEDIATOR; NEUTROPHIL; OMENTUM; PREECLAMPSIA; PREGNANT WOMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SMOOTH MUSCLE FIBER; VASCULAR DISEASE; VASCULAR SMOOTH MUSCLE; VASOCONSTRICTION;

EID: 79251498302     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2010.11.003     Document Type: Article

References (59)

1. LaMarca BD, Ryan MJ, Gilbert JS, Murphy SR, Granger JP: Inflammatory cytokines in the pathophysiology of hypertension during pre-eclampsia. Curr Hypertens Rep 2007, 9:480-485
2. VanWijk MJ, Kublickiene K, Boer K, VanBavel E: Vascular function in preeclampsia. Cardiovasc Res 2000, 47:38-48
3. Flamant M, Placier S, Dubroca C, Esposito B, Lopes I, Chatziantoniou C, Tedgui A, Dussaule JC, Lehoux S: Role of matrix metalloproteinases in early hypertensive vascular remodeling. Hypertension 2007, 50:212-218
4. Lehoux S, Lemarie CA, Esposito B, Lijnen HR, Tedgui A: Pressure-induced matrix metalloproteinase-9 contributes to early hypertensive remodeling. Circulation 2004, 109:1041-1047 (Pubitemid 38282859)
5. Lehoux S, Castier Y, Tedgui A: Molecular mechanisms of the vascular responses to haemodynamic forces. J Intern Med 2006, 259:381-392
6. Leik CE, Walsh SW: Neutrophils infiltrate resistance-sized vessels of subcutaneous fat in women with preeclampsia. Hypertension 2004, 44:72-77
7. Shah TJ, Walsh SW: Activation of NF-kappaB and expression of COX-2 in association with neutrophil infiltration in systemic vascular tissue of women with preeclampsia. Am J Obstet Gynecol 2007, 196:48.e1-48.e8
8. Cadden KA, Walsh SW: Neutrophils, but not lymphocytes or monocytes, infiltrate maternal systemic vasculature in women with pre-eclampsia. Hypertens Pregnancy 2008, 27:396-405
9. Walsh SW: Maternal-placental interactions of oxidative stress and antioxidants in preeclampsia. Semin Reprod Endocrinol 1998, 16:93-104
10. Walsh SW, Vaughan JE, Wang Y, Roberts LJ 2nd: Placental isoprostane is significantly increased in preeclampsia. FASEB J 2000, 14:1289-1296
11. Smith JA: Neutrophils, host defense, and inflammation: a double-edged sword. J Leukoc Biol 1994, 56:672-686
12. Walsh SW: Obesity: a risk factor for preeclampsia. Trends Endocrinol Metab 2007, 18:365-370
13. Taniyama Y, Griendling KK: Reactive oxygen species in the vasculature: molecular and cellular mechanisms. Hypertension 2003, 42:1075-1081
14. Arenas IA, Xu Y, Lopez-Jaramillo P, Davidge ST: Angiotensin II-induced MMP-2 release from endothelial cells is mediated by TNF-alpha. Am J Physiol Cell Physiol 2004, 286:C779-C784
15. Moon SK, Cha BY, Kim CH: ERK1/2 mediates TNF-alpha-induced matrix metalloproteinase-9 expression in human vascular smooth muscle cells via the regulation of NF-kappaB and AP-1: involvement of the ras dependent pathway. J Cell Physiol 2004, 198:417-427
16. Lee SJ, Seo KW, Yun MR, Bae SS, Lee WS, Hong KW, Kim CD: 4-Hydroxynonenal enhances MMP-2 production in vascular smooth muscle cells via mitochondrial ROS-mediated activation of the Akt/ NF-kappaB signaling pathways. Free Radic Biol Med 2008, 45:1487-1492
17. Streuli C: Extracellular matrix remodelling and cellular differentiation. Curr Opin Cell Biol 1999, 11:634-640
18. Shapiro SD: Matrix metalloproteinase degradation of extracellular matrix: biological consequences. Curr Opin Cell Biol 1998, 10:602-608
19. Fernandez-Patron C, Radomski MW, Davidge ST: Vascular matrix metalloproteinase-2 cleaves big endothelin-1 yielding a novel vasoconstrictor. Circ Res 1999, 85:906-911
20. Fernandez-Patron C, Stewart KG, Zhang Y, Koivunen E, Radomski MW, Davidge ST: Vascular matrix metalloproteinase-2-dependent cleavage of calcitonin gene-related peptide promotes vasoconstriction. Circ Res 2000, 87:670-676
21. Sankaralingam S, Arenas IA, Lalu MM, Davidge ST: Preeclampsia: current understanding of the molecular basis of vascular dysfunction. Expert Rev Mol Med 2006, 8:1-20
22. Mellembakken JR, Aukrust P, Olafsen MK, Ueland T, Hestdal K, Videm V: Activation of leukocytes during the uteroplacental passage in preeclampsia. Hypertension 2002, 39:155-160
23. Saito S, Sakai M: Th1/Th2 balance in preeclampsia. J Reprod Immunol 2003, 59:161-173
24. Leik CE, Willey A, Graham MF, Walsh SW: Isolation and culture of arterial smooth muscle cells from human placenta. Hypertension 2004, 43:837-840
25. Forman HJ, Maiorino M, Ursini F: Signaling functions of reactive oxygen species. Biochemistry 2010, 49:835-842
26. Vaughan JE, Walsh SW, Ford GD: Thromboxane mediates neutrophil superoxide production in pregnancy. Am J Obstet Gynecol 2006, 195:1415-1420
27. Rosenfeldt MT, Valentino M, Labruzzo S, Scudder L, Pavlaki M, Cao J, Vacirca J, Bahou WF, Zucker S: The organomercurial 4-aminophenylmercuric acetate, independent of matrix metalloproteinases, induces dose-dependent activation/inhibition of platelet aggregation. Thromb Haemost 2005, 93:326-330
28. Gomez-Lopez N, Estrada-Gutierrez G, Jimenez-Zamudio L, Vega- Sanchez R, Vadillo-Ortega F: Fetal membranes exhibit selective leukocyte chemotaxic activity during human labor. J Reprod Immunol 2009, 80:122-131
29. Grab DJ, Nyarko E, Barat NC, Nikolskaia OV, Dumler JS: Anaplasma phagocytophilum-Borrelia burgdorferi coinfection enhances chemokine, cytokine, and matrix metalloprotease expression by human brain microvascular endothelial cells. Clin Vaccine Immunol 2007, 14:1420-1424
30. Sassi ML, Eriksen H, Risteli L, Niemi S, Mansell J, Gowen M, Risteli J: Immunochemical characterization of assay for carboxyterminal telopeptide of human type I collagen: loss of antigenicity by treatment with cathepsin K. Bone 2000, 26:367-373
31. Gaggar A, Jackson PL, Noerager BD, O'Reilly PJ, McQuaid DB, Rowe SM, Clancy JP, Blalock JE: A novel proteolytic cascade generates an extracellular matrix-derived chemoattractant in chronic neutrophilic inflammation. J Immunol 2008, 180:5662-5669
32. Riley DJ, Berg RA, Soltys RA, Kerr JS, Guss HN, Curran SF, Laskin DL: Neutrophil response following intratracheal instillation of collagen peptides into rat lungs. Exp Lung Res 1988, 14:549-563
33. Boire A, Covic L, Agarwal A, Jacques S, Sherifi S, Kuliopulos A: PAR1 is a matrix metalloprotease-1 receptor that promotes invasion and tumorigenesis of breast cancer cells. Cell 2005, 120:303-313
34. Leger AJ, Covic L, Kuliopulos A: Protease-activated receptors in cardiovascular diseases. Circulation 2006, 114:1070-1077
35. Erez O, Romero R, Kim SS, Kim JS, Kim YM, Wildman DE, Than NG, Mazaki-Tovi S, Gotsch F, Pineles B, Kusanovic JP, Espinoza J, Mittal P, Mazor M, Hassan SS, Kim CJ: Over-expression of the thrombin receptor (PAR-1) in the placenta in preeclampsia: a mechanism for the intersection of coagulation and inflammation. J Matern Fetal Neonatal Med 2008, 21:345-355
36. Martinez A, Oh HR, Unsworth EJ, Bregonzio C, Saavedra JM, Stetler- Stevenson WG, Cuttitta F: Matrix metalloproteinase-2 cleavage of adrenomedullin produces a vasoconstrictor out of a vasodilator. Biochem J 2004, 383:413-418
37. Ku DD, Dai J: Expression of thrombin receptors in human atherosclerotic coronary arteries leads to an exaggerated vasoconstrictory response in vitro. J Cardiovasc Pharmacol 1997, 30:649-657
38. Cicala C, Morello S, Santagada V, Caliendo G, Sorrentino L, Cirino G: Pharmacological dissection of vascular effects caused by activation of protease-activated receptors 1 and 2 in anesthetized rats. FASEB J 2001, 15:1433-1435
39. Strande JL, Hsu A, Su J, Fu X, Gross GJ, Baker JE: SCH 79797, a selective PAR1 antagonist, limits myocardial ischemia/reperfusion injury in rat hearts. Basic Res Cardiol 2007, 102:350-358
40. Bankowski E, Romanowicz L, Jaworski S: Collagen of umbilical cord arteries and its alterations in EPH-gestosis. J Perinat Med 1993, 21:491-498
41. Baumwell S, Karumanchi SA: Pre-eclampsia: clinical manifestations and molecular mechanisms. Nephron Clin Pract 2007, 106:c72-c81 (Pubitemid 46933395)
42. Hladunewich M, Karumanchi SA, Lafayette R: Pathophysiology of the clinical manifestations of preeclampsia. Clin J Am Soc Nephrol 2007, 2:543-549
43. Greer IA, Haddad NG, Dawes J, Johnstone FD, Calder AA: Neutrophil activation in pregnancy-induced hypertension. Br J Obstet Gynaecol 1989, 96:978-982
44. Gervasi MT, Chaiworapongsa T, Pacora P, Naccasha N, Yoon BH, Maymon E, Romero R: Phenotypic and metabolic characteristics of monocytes and granulocytes in preeclampsia. Am J Obstet Gynecol 2001, 185:792-797
45. Lee VM, Quinn PA, Jennings SC, Ng LL: Neutrophil activation and production of reactive oxygen species in pre-eclampsia. J Hypertens 2003, 21:395-402
46. Mellembakken JR, Aukrust P, Hestdal K, Ueland T, Abyholm T, Videm V: Chemokines and leukocyte activation in the fetal circulation during preeclampsia. Hypertension 2001, 38:394-398
47. Zhu Y, Hojo Y, Ikeda U, Takahashi M, Shimada K: Interaction between monocytes and vascular smooth muscle cells enhances matrix metalloproteinase- 1 production. J Cardiovasc Pharmacol 2000, 36:152-161
48. Vaughan JE, Walsh SW: Neutrophils from pregnant women produce thromboxane and tumor necrosis factor-alpha in response to linoleic acid and oxidative stress. Am J Obstet Gynecol 2005, 193:830-835
49. Rajagopalan S, Meng XP, Ramasamy S, Harrison DG, Galis ZS: Reactive oxygen species produced by macrophage-derived foam cells regulate the activity of vascular matrix metalloproteinases in vitro: implications for atherosclerotic plaque stability. J Clin Invest 1996, 98:2572-2579
50. Walsh SW: Plasma from preeclamptic women stimulates transendothelial migration of neutrophils. Reprod Sci 2009, 16:320-325
51. Schonbeck U, Brandt E, Petersen F, Flad HD, Loppnow H: IL-8 specifically binds to endothelial but not to smooth muscle cells. J Immunol 1995, 154:2375-2383
52. Faveeuw C, Preece G, Ager A: Transendothelial migration of lymphocytes across high endothelial venules into lymph nodes is affected by metalloproteinases. Blood 2001, 98:688-695
53. 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
54. Melnikova VO, Balasubramanian K, Villares GJ, Dobroff AS, Zigler M, Wang H, Petersson F, Price JE, Schroit A, Prieto VG, Hung MC, Bar-Eli M: Crosstalk between protease-activated receptor 1 and platelet-activating factor receptor regulates melanoma cell adhesion molecule (MCAM/MUC18) expression and melanoma metastasis. J Biol Chem 2009, 284:28845-28855
55. Coughlin SR: Thrombin signalling and protease-activated receptors. Nature 2000, 407:258-264
56. Derian CK, Maryanoff BE, Zhang HC, Andrade-Gordon P: Therapeutic potential of protease-activated receptor-1 antagonists. Expert Opin Investig Drugs 2003, 12:209-221
57. Nelken NA, Soifer SJ, O'Keefe J, Vu TK, Charo IF, Coughlin SR: Thrombin receptor expression in normal and atherosclerotic human arteries. J Clin Invest 1992, 90:1614-1621
58. Merchant SJ, Davidge ST: The role of matrix metalloproteinases in vascular function: implications for normal pregnancy and pre-eclampsia. Bjog 2004, 111:931-939
59. Magazine HI, Butt O, Yaghoutiel HR: Endothelin and nitric oxide release modulate aortic contraction to selected thrombin receptor agonists. Am J Physiol 1996, 270:C1815-C1818