Basigin mediates pulmonary hypertension by promoting inflammation and vascular smooth muscle cell proliferation

Circulation Research

Volumn 115, Issue 8, 2014, Pages 738-750

  Satoh, Kimio ^a   Satoh, Taijyu ^a   Kikuchi, Nobuhiro ^a   Omura, Junichi ^a   Kurosawa, Ryo ^a   Suzuki, Kota ^a   Sugimura, Koichiro ^a   Aoki, Tatsuo ^a   Nochioka, Kotaro ^a   Tatebe, Shunsuke ^a   Miyamichi Yamamoto, Saori ^a   Miura, Masanobu ^a   Shimizu, Toru ^a   Ikeda, Shohei ^a   Yaoita, Nobuhiro ^a   Fukumoto, Yoshihiro ^a   Minami, Tatsuro ^a   Miyata, Satoshi ^a   Nakamura, Kazufumi ^a   Ito, Hiroshi ^b   Kadomatsu, Kenji ^c   Shimokawa, Hiroaki ^a   more..

^a TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b OKAYAMA UNIVERSITY   (Japan)

^c NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Anoxia; Hypertension, pulmonary; Inflammation; Muscle, smooth, vascular; Oxidative stress; Pulmonary circulation

Indexed keywords

CD147 ANTIGEN; CYCLOPHILIN A; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PLATELET DERIVED GROWTH FACTOR BB; CHEMOKINE; CYTOKINE; MITOGEN ACTIVATED PROTEIN KINASE; SIGNAL PEPTIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME ACTIVATION; HEART RIGHT VENTRICLE HYPERTROPHY; INFLAMMATION; LUNG VASCULAR RESISTANCE; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PRIORITY JOURNAL; PULMONARY ARTERY; PULMONARY HYPERTENSION; SIGNAL TRANSDUCTION; SYSTOLIC BLOOD PRESSURE; VASCULAR SMOOTH MUSCLE; ANIMAL; ANOXIA; BLOOD; CELL CULTURE; CELL HYPOXIA; GENETICS; HUMAN; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; LUNG; METABOLISM; PATHOLOGY; SMOOTH MUSCLE FIBER; WESTERN BLOTTING;

ANIMALS; ANOXIA; ANTIGENS, CD147; BLOTTING, WESTERN; CELL HYPOXIA; CELL PROLIFERATION; CELLS, CULTURED; CHEMOKINES; CYCLOPHILIN A; CYTOKINES; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; HYPERTENSION, PULMONARY; IMMUNOHISTOCHEMISTRY; INFLAMMATION; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LUNG; MICE; MICE, KNOCKOUT; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; PULMONARY ARTERY;

EID: 84921817732     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.115.304563     Document Type: Article

References (65)

1. Michelakis ED. Pulmonary arterial hypertension: yesterday, today, tomorrow. Circ Res. 2014;115:109-114.
2. Rabinovitch M, Guignabert C, Humbert M, Nicolls MR. Inflammation and immunity in the pathogenesis of pulmonary arterial hypertension. Circ Res. 2014;115:165-175.
3. Lai YC, Potoka KC, Champion HC, Mora AL, Gladwin MT. Pulmonary arterial hypertension: the clinical syndrome. Circ Res. 2014;115:115-130.
4. Zamanian RT, Kudelko KT, Sung YK, de Jesus Perez V, Liu J, Spiekerkoetter E. Current clinical management of pulmonary arterial hypertension. Circ Res. 2014;115:131-147.
5. Paulin R, Michelakis ED. The metabolic theory of pulmonary arterial hypertension. Circ Res. 2014;115:148-164.
6. Ryan JJ, Archer SL. The right ventricle in pulmonary arterial hypertension: disorders of metabolism, angiogenesis and adrenergic signaling in right ventricular failure. Circ Res. 2014;115:176-188.
7. Stenmark KR, Fagan KA, Frid MG. Hypoxia-induced pulmonary vascular remodeling: cellular and molecular mechanisms. Circ Res. 2006;99:675-691.
8. Voelkel NF, Mizuno S, Bogaard HJ. The role of hypoxia in pulmonary vascular diseases: a perspective. Am J Physiol Lung Cell Mol Physiol. 2013;304:L457-L465.
9. Austin ED, Loyd JE. The genetics of pulmonary arterial hypertension. Circ Res. 2014;115:189-202.
10. Hansmann G, de Jesus Perez VA, Alastalo TP, Alvira CM, Guignabert C, Bekker JM, Schellong S, Urashima T, Wang L, Morrell NW, Rabinovitch M. An antiproliferative BMP-2/PPAR/apoE axis in human and murine SMCs and its role in pulmonary hypertension. J Clin Invest. 2008;118:1846-1857.
11. Tuder RM, Archer SL, Dorfmüller P, Erzurum SC, Guignabert C, Michelakis E, Rabinovitch M, Schermuly R, Stenmark KR, Morrell NW. Relevant issues in the pathology and pathobiology of pulmonary hypertension. J Am Coll Cardiol. 2013;62:D4-12.
12. de Frutos S, Spangler R, Alò D, Bosc LV. NFATc3 mediates chronic hypoxia-induced pulmonary arterial remodeling with alpha-actin up-regulation. J Biol Chem. 2007;282:15081-15089.
13. Satoh K, Kagaya Y, Nakano M, et al. Important role of endogenous erythropoietin system in recruitment of endothelial progenitor cells in hypoxia-induced pulmonary hypertension in mice. Circulation. 2006;113:1442-1450.
14. Satoh K, Fukumoto Y, Nakano M, Sugimura K, Nawata J, Demachi J, Karibe A, Kagaya Y, Ishii N, Sugamura K, Shimokawa H. Statin ameliorates hypoxia-induced pulmonary hypertension associated with down-regulated stromal cell-derived factor-1. Cardiovasc Res. 2009;81:226-234.
15. Shimizu T, Fukumoto Y, Tanaka S, Satoh K, Ikeda S, Shimokawa H. Crucial role of ROCK2 in vascular smooth muscle cells for hypoxia-induced pulmonary hypertension in mice. Arterioscler Thromb Vasc Biol. 2013;33:2780-2791.
16. Elias-Al-Mamun M, Satoh K, Tanaka S, Shimizu T, Nergui S, Miyata S, Fukumoto Y, Shimokawa H. Combination therapy with fasudil and sildenafil ameliorates monocrotaline-induced pulmonary hypertension and survival in rats. Circ J. 2014;78:967-976.
17. Ikeda S, Satoh K, Kikuchi N, Miyata S, Suzuki K, Omura J, Shimizu T, Kobayashi K, Kobayashi K, Fukumoto Y, Sakata Y, Shimokawa H. Crucial role of Rho-kinase in pressure overload-induced right ventricular hypertrophy and dysfunction in mice. Arterioscler Thromb Vasc Biol. 2014;34:1260-1271.
18. Satoh K, Matoba T, Suzuki J, O'Dell MR, Nigro P, Cui Z, Mohan A, Pan S, Li L, Jin ZG, Yan C, Abe J, Berk BC. Cyclophilin A mediates vascular remodeling by promoting inflammation and vascular smooth muscle cell proliferation. Circulation. 2008;117:3088-3098.
19. Jin ZG, Melaragno MG, Liao DF, Yan C, Haendeler J, Suh YA, Lambeth JD, Berk BC. Cyclophilin A is a secreted growth factor induced by oxidative stress. Circ Res. 2000;87:789-796.
20. Liao DF, Jin ZG, Baas AS, Daum G, Gygi SP, Aebersold R, Berk BC. Purification and identification of secreted oxidative stress-induced factors from vascular smooth muscle cells. J Biol Chem. 2000;275:189-196.
21. Satoh K, Fukumoto Y, Shimokawa H. Rho-kinase: important new therapeutic target in cardiovascular diseases. Am J Physiol Heart Circ Physiol. 2011;301:H287-H296.
22. Jin ZG, Lungu AO, Xie L, Wang M, Wong C, Berk BC. Cyclophilin A is a proinflammatory cytokine that activates endothelial cells. Arterioscler Thromb Vasc Biol. 2004;24:1186-1191.
23. Nigro P, Satoh K, O'Dell MR, Soe NN, Cui Z, Mohan A, Abe J, Alexis JD, Sparks JD, Berk BC. Cyclophilin A is an inflammatory mediator that promotes atherosclerosis in apolipoprotein E-deficient mice. J Exp Med. 2011;208:53-66.
24. Khromykh LM, Kulikova NL, Anfalova TV, Muranova TA, Abramov VM, Vasiliev AM, Khlebnikov VS, Kazansky DB. Cyclophilin A produced by thymocytes regulates the migration of murine bone marrow cells. Cell Immunol. 2007;249:46-53.
25. Yurchenko V, Zybarth G, O'Connor M, Dai WW, Franchin G, Hao T, Guo H, Hung HC, Toole B, Gallay P, Sherry B, Bukrinsky M. Active site residues of cyclophilin A are crucial for its signaling activity via CD147. J Biol Chem. 2002;277:22959-22965.
26. Miller LH, Ackerman HC, Su XZ, Wellems TE. Malaria biology and disease pathogenesis: insights for new treatments. Nat Med. 2013;19:156-167.
27. Igakura T, Kadomatsu K, Kaname T, Muramatsu H, Fan QW, Miyauchi T, Toyama Y, Kuno N, Yuasa S, Takahashi M, Senda T, Taguchi O, Yamamura K, Arimura K, Muramatsu T. A null mutation in basigin, an immunoglobulin superfamily member, indicates its important roles in peri-implantation development and spermatogenesis. Dev Biol. 1998;194:152-165.
28. Kuno N, Kadomatsu K, Fan QW, Hagihara M, Senda T, Mizutani S, Muramatsu T. Female sterility in mice lacking the basigin gene, which encodes a transmembrane glycoprotein belonging to the immunoglobulin superfamily. FEBS Lett. 1998;425:191-194.
29. Satoh K, Nigro P, Matoba T, O'Dell MR, Cui Z, Shi X, Mohan A, Yan C, Abe J, Illig KA, Berk BC. Cyclophilin A enhances vascular oxidative stress and the development of angiotensin II-induced aortic aneurysms. Nat Med. 2009;15:649-656.
30. Team RC. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. http://www.Rproject. org/. 2013. Accessed July 1, 2013.
31. Satoh K, Shimokawa H, Berk BC. Cyclophilin A: promising new target in cardiovascular therapy. Circ J. 2010;74:2249-2256.
32. Rabinovitch M. Molecular pathogenesis of pulmonary arterial hypertension. J Clin Invest. 2012;122:4306-4313.
33. Weng M, Baron DM, Bloch KD, Luster AD, Lee JJ, Medoff BD. Eosinophils are necessary for pulmonary arterial remodeling in a mouse model of eosinophilic inflammation-induced pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol. 2011;301:L927-L936.
34. Chen X, Su J, Chang J, Kanekura T, Li J, Kuang YH, Peng S, Yang F, Lu H, Zhang JL. Inhibition of CD147 gene expression via RNA interference reduces tumor cell proliferation, activation, adhesion, and migration activity in the human Jurkat T-lymphoma cell line. Cancer Invest. 2008;26:689-697.
35. Yeager ME, Frid MG, Stenmark KR. Progenitor cells in pulmonary vascular remodeling. Pulm Circ. 2011;1:3-16.
36. Undem C, Rios EJ, Maylor J, Shimoda LA. Endothelin-1 augments Na/ H exchange activity in murine pulmonary arterial smooth muscle cells via Rho kinase. PLoS One. 2012;7:e46303.
37. Levonen AL, Inkala M, Heikura T, Jauhiainen S, Jyrkkänen HK, Kansanen E, Määttä K, Romppanen E, Turunen P, Rutanen J, Ylä-Herttuala S. Nrf2 gene transfer induces antioxidant enzymes and suppresses smooth muscle cell growth in vitro and reduces oxidative stress in rabbit aorta in vivo. Arterioscler Thromb Vasc Biol. 2007;27:741-747.
38. Cheng C, Haasdijk RA, Tempel D, den Dekker WK, Chrifi I, Blonden LA, van de Kamp EH, de Boer M, Bürgisser PE, Noorderloos A, Rens JA, ten Hagen TL, Duckers HJ. PDGF-induced migration of vascular smooth muscle cells is inhibited by heme oxygenase-1 via VEGFR2 upregulation and subsequent assembly of inactive VEGFR2/PDGFR heterodimers. Arterioscler Thromb Vasc Biol. 2012;32:1289-1298.
39. Satoh K, Fukumoto Y, Sugimura K, et al. Plasma cyclophilin A is a novel biomarker for coronary artery disease. Circ J. 2013;77:447-455.
40. Yet SF, Perrella MA, Layne MD, Hsieh CM, Maemura K, Kobzik L, Wiesel P, Christou H, Kourembanas S, Lee ME. Hypoxia induces severe right ventricular dilatation and infarction in heme oxygenase-1 null mice. J Clin Invest. 1999;103:R23-R29.
41. Eba S, Hoshikawa Y, Moriguchi T, Mitsuishi Y, Satoh H, Ishida K, Watanabe T, Shimizu T, Shimokawa H, Okada Y, Yamamoto M, Kondo T. The nuclear factor erythroid 2-related factor 2 activator oltipraz attenuates chronic hypoxia-induced cardiopulmonary alterations in mice. Am J Respir Cell Mol Biol. 2013;49:324-333.
42. Seizer P, Schönberger T, Schött M, Lang MR, Langer HF, Bigalke B, Krämer BF, Borst O, Daub K, Heidenreich O, Schmidt R, Lindemann S, Herouy Y, Gawaz M, May AE. EMMPRIN and its ligand cyclophilin A regulate MT1-MMP, MMP-9 and M-CSF during foam cell formation. Atherosclerosis. 2010;209:51-57.
43. Seizer P, Ochmann C, Schönberger T, Zach S, Rose M, Borst O, Klingel K, Kandolf R, MacDonald HR, Nowak RA, Engelhardt S, Lang F, Gawaz M, May AE. Disrupting the EMMPRIN (CD147)-cyclophilin A interaction reduces infarct size and preserves systolic function after myocardial ischemia and reperfusion. Arterioscler Thromb Vasc Biol. 2011;31:1377-1386.
44. Venkatesan B, Valente AJ, Prabhu SD, Shanmugam P, Delafontaine P, Chandrasekar B. EMMPRIN activates multiple transcription factors in cardiomyocytes, and induces interleukin-18 expression via Rac1-dependent PI3K/Akt/IKK/NF-B andMKK7/JNK/AP-1 signaling. J Mol Cell Cardiol. 2010;49:655-663.
45. Venkatesan B, Valente AJ, Reddy VS, Siwik DA, Chandrasekar B. Resveratrol blocks interleukin-18-EMMPRIN cross-regulation and smooth muscle cell migration. Am J Physiol Heart Circ Physiol. 2009;297:H874-H886.
46. Suzuki J, Jin ZG, Meoli DF, Matoba T, Berk BC. Cyclophilin A is secreted by a vesicular pathway in vascular smooth muscle cells. Circ Res. 2006;98:811-817.
47. Shimokawa H, Takeshita A. Rho-kinase is an important therapeutic target in cardiovascular medicine. Arterioscler Thromb Vasc Biol. 2005;25:1767-1775.
48. Abe K, Shimokawa H, Morikawa K, Uwatoku T, Oi K, Matsumoto Y, Hattori T, Nakashima Y, Kaibuchi K, Sueishi K, Takeshit A. Long-term treatment with a Rho-kinase inhibitor improves monocrotaline-induced fatal pulmonary hypertension in rats. Circ Res. 2004;94:385-393.
49. Do e Z, Fukumoto Y, Takaki A, Tawara S, Ohashi J, Nakano M, Tada T, Saji K, Sugimura K, Fujita H, Hoshikawa Y, Nawata J, Kondo T, Shimokawa H. Evidence for Rho-kinase activation in patients with pulmonary arterial hypertension. Circ J. 2009;73:1731-1739.
50. Fukumoto Y, Yamada N, Matsubara H, et al. Double-blind, placebo-controlled clinical trial with a Rho-kinase inhibitor in pulmonary arterial hypertension. Circ J. 2013;77:2619-2625.
51. Janka JJ, Koita OA, Traoré B, Traoré JM, Mzayek F, Sachdev V, Wang X, Sanogo K, Sangaré L, Mendelsohn L, Masur H, Kato GJ, Gladwin MT, Krogstad DJ. Increased pulmonary pressures and myocardial wall stress in children with severe malaria. J Infect Dis. 2010;202:791-800.
52. Crosnier C, Bustamante LY, Bartholdson SJ, Bei AK, Theron M, Uchikawa M, Mboup S, Ndir O, Kwiatkowski DP, Duraisingh MT, Rayner JC, Wright GJ. Basigin is a receptor essential for erythrocyte invasion by Plasmodium falciparum. Nature. 2011;480:534-537.
53. Haug C, Lenz C, Díaz F, Bachem MG. Oxidized low-density lipoproteins stimulate extracellular matrix metalloproteinase Inducer (EMMPRIN) release by coronary smooth muscle cells. Arterioscler Thromb Vasc Biol. 2004;24:1823-1829.
54. Guo H, Majmudar G, Jensen TC, Biswas C, Toole BP, Gordon MK. Characterization of the gene for human EMMPRIN, a tumor cell surface inducer of matrix metalloproteinases. Gene. 1998;220:99-108.
55. Cracowski JL, Leuchte HH. The potential of biomarkers in pulmonary arterial hypertension. Am J Cardiol. 2012;110:32S-38S.
56. Weir EK, Archer SL. The role of redox changes in oxygen sensing. Respir Physiol Neurobiol. 2010;174:182-191.
57. Dromparis P, Paulin R, Sutendra G, Qi AC, Bonnet S, Michelakis ED. Uncoupling protein 2 deficiency mimics the effects of hypoxia and endoplasmic reticulum stress on mitochondria and triggers pseudohypoxic pulmonary vascular remodeling and pulmonary hypertension. Circ Res. 2013;113:126-136.
58. Kim YM, Barnes EA, Alvira CM, Ying L, Reddy S, Cornfield DN. Hypoxia-inducible factor-1 in pulmonary artery smooth muscle cells lowers vascular tone by decreasing myosin light chain phosphorylation. Circ Res. 2013;112:1230-1233.
59. Yamamura A, Yamamura H, Guo Q, Zimnicka AM, Wan J, Ko EA, Smith KA, Pohl NM, Song S, Zeifman A, Makino A, Yuan JX. Dihydropyridine Ca2+ channel blockers increase cytosolic [Ca2+] by activating Ca2+-sensing receptors in pulmonary arterial smooth muscle cells. Circ Res. 2013;112:640-650.
60. Svoboda LK, Reddie KG, Zhang L, Vesely ED, Williams ES, Schumacher SM, O'Connell RP, Shaw R, Day SM, Anumonwo JM, Carroll KS, Martens JR. Redox-sensitive sulfenic acid modification regulates surface expression of the cardiovascular voltage-gated potassium channel Kv1.5. Circ Res. 2012;111:842-853.
61. Matsuda S, Koyasu S. Regulation of MAPK signaling pathways through immunophilin-ligand complex. Curr Top Med Chem. 2003;3:1358-1367.
62. Bonnet S, Archer SL. Potassium channel diversity in the pulmonary arteries and pulmonary veins: implications for regulation of the pulmonary vasculature in health and during pulmonary hypertension. Pharmacol Ther. 2007;115:56-69.
63. Moudgil R, Michelakis ED, Archer SL. The role of K+ channels in determining pulmonary vascular tone, oxygen sensing, cell proliferation, and apoptosis: implications in hypoxic pulmonary vasoconstriction and pulmonary arterial hypertension. Microcirculation. 2006;13:615-632.
64. Bonnet S, Rochefort G, Sutendra G, Archer SL, Haromy A, Webster L, Hashimoto K, Bonnet SN, Michelakis ED. The nuclear factor of activated T cells in pulmonary arterial hypertension can be therapeutically targeted. Proc Natl Acad Sci USA. 2007;104:11418-11423.
65. Kato N, Yuzawa Y, Kosugi T, Hobo A, Sato W, Miwa Y, Sakamoto K, Matsuo S, Kadomatsu K. The E-selectin ligand basigin/CD147 is responsible for neutrophil recruitment in renal ischemia/reperfusion. J Am Soc Nephrol. 2009;20:1565-1576.