Inflammation, endothelial injury, and persistent pulmonary hypertension in heterozygous BMPR2-mutant mice (American Journal of Physiology - Heart and Circulatory Physiology (2008) 295, (H677-H690) DOI: 10.1152/ajpheart.91519.2007);Inflammation, endothelial injury, and persistent pulmonary hypertension in heterozygous BMPR2-mutant mice

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 295, Issue 2, 2008, Pages

  Song, Yanli ^a   Coleman, Laura ^a   Shi, Jianru ^a   Beppu, Hideyuki ^b   Sato, Kaori ^c   Walsh, Kenneth ^c   Loscalzo, Joseph ^a   Zhang, Ying Yi ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Heterozygous bone morphogenetic protein receptor 2 knockout mice

Indexed keywords

ADENOVIRUS VECTOR; ARACHIDONATE 5 LIPOXYGENASE; BONE MORPHOGENETIC PROTEIN RECEPTOR 1; BONE MORPHOGENETIC PROTEIN RECEPTOR 2; CHEMOKINE RECEPTOR CX3CR1; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MONOCROTALINE; BIOLOGICAL MARKER; BMPR2 PROTEIN, MOUSE; CHEMOKINE; MESSENGER RNA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERIAL WALL THICKENING; ARTICLE; BMPR2 GENE; CONTROLLED STUDY; ENDOTHELIUM INJURY; FEMALE; GENE; GENE MUTATION; GENETIC TRAIT; HEART RIGHT VENTRICLE; HETEROZYGOSITY; IDIOPATHIC DISEASE; INFLAMMATION; LYMPHOCYTIC INFILTRATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PULMONARY HYPERTENSION; SYSTOLIC BLOOD PRESSURE; ANIMAL; APOPTOSIS; B LYMPHOCYTE; C57BL MOUSE; CHEMICALLY INDUCED DISORDER; DISEASE MODEL; GENETIC TRANSDUCTION; GENETICS; HEART RIGHT VENTRICLE FUNCTION; HETEROZYGOTE; LUNG; MACROPHAGE; METABOLISM; MUTATION; PATHOLOGY; PRESSURE; PULMONARY ARTERY; T LYMPHOCYTE; TIME; TRANSGENIC MOUSE; VASCULAR ENDOTHELIUM;

ANIMALS; APOPTOSIS; ARACHIDONATE 5-LIPOXYGENASE; B-LYMPHOCYTES; BIOLOGICAL MARKERS; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE II; CHEMOKINES; DISEASE MODELS, ANIMAL; ENDOTHELIUM, VASCULAR; HETEROZYGOTE; HYPERTENSION, PULMONARY; INFLAMMATION; LUNG; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MONOCROTALINE; MUTATION; PRESSURE; PULMONARY ARTERY; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; RNA, MESSENGER; T-LYMPHOCYTES; TIME FACTORS; TRANSDUCTION, GENETIC; VENTRICULAR FUNCTION, RIGHT;

EID: 52449108680     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.zh4-9060-corr.2009     Document Type: Erratum

References (53)

1. Aldred MA, Vijayakrishnan J, James V, Soubrier F, Gomez-Sanchez MA, Martensson G, Galie N, Manes A, Corris P, Simonneau G, Humbert M, Morrell NW, Trembath RC. BMPR2 gene rearrangements account for a significant proportion of mutations in familial and idiopathic pulmonary arterial hypertension. Hum Mutat 27: 212-213, 2006.
2. Astorga J, Carlsson P. Hedgehog induction of murine vasculogenesis is mediated by Foxf1 and Bmp4. Development 134: 3753-3761, 2007.
3. Atkinson C, Stewart S, Upton PD, Machado R, Thomson JR, Trembath RC, Morrell NW. Primary pulmonary hypertension is associated with reduced pulmonary vascular expression of type II bone morphogenetic protein receptor. Circulation 105: 1672-1678, 2002.
4. Beppu H, Kawabata M, Hamamoto T, Chytil A, Minowa O, Noda T, Miyazono K. BMP type II receptor is required for gastrulation and early development of mouse embryos. Dev Biol 221: 249-258, 2000.
5. Bouletreau PJ, Warren SM, Spector JA, Peled ZM, Gerrets RP, Greenwald JA, Longaker MT. Hypoxia and VEGF up-regulate BMP-2 mRNA and protein expression in microvascular endothelial cells: implications for fracture healing. Plast Reconstr Surg 109: 2384-2397, 2002.
6. Campbell AI, Zhao Y, Sandhu R, Stewart DJ. Cell-based gene transfer of vascular endothelial growth factor attenuates monocrotaline-induced pulmonary hypertension. Circulation 104: 2242-2248, 2001.
7. Cejalvo T, Sacedon R, Hernandez-Lopez C, Diez B, Gutierrez-Frias C, Valencia J, Zapata AG, Varas A, Vicente A. Bone morphogenetic protein-2/4 signalling pathway components are expressed in the human thymus and inhibit early T-cell development. Immunology 121: 94-104, 2007.
8. Csiszar A, Ahmad M, Smith KE, Labinskyy N, Gao Q, Kaley G, Edwards JG, Wolin MS, Ungvari Z. Bone morphogenetic protein-2 induces proinflammatory endothelial phenotype. Am J Pathol 168: 629-638, 2006.
9. Deckers MM, van Bezooijen RL, van der Horst G, Hoogendam J, van Der Bent C, Papapoulos SE, Lowik CW. Bone morphogenetic proteins stimulate angiogenesis through osteoblast-derived vascular endothelial growth factor A. Endocrinology 143: 1545-1553, 2002.
10. Deng Z, Morse JH, Slager SL, Cuervo N, Moore KJ, Venetos G, Kalachikov S, Cayanis E, Fischer SG, Barst RJ, Hodge SE, Knowles JA. Familial primary pulmonary hypertension (gene PPH1) is caused by mutations in the bone morphogenetic protein receptor-II gene. Am J Hum Genet 67: 737-744, 2000.
11. Dorner BG, Scheffold A, Rolph MS, Huser MB, Kaufmann SH, Radbruch A, Flesch IE, Kroczek RA. MIP-1alpha, MIP-1beta, RANTES, and ATAC/lymphotactin function together with IFN-gamma as type 1 cytokines. Proc Natl Acad Sci USA 99: 6181-6186, 2002.
12. Ferkowicz MJ, Yoder MC. Blood island formation: longstanding observations and modern interpretations. Exp Hematol 33: 1041-1047, 2005.
13. Fischer S, Maclean AA, Liu M, Cardella JA, Slutsky AS, Suga M, Moreira JF, Keshavjee S. Dynamic changes in apoptotic and necrotic cell death correlate with severity of ischemia-reperfusion injury in lung transplantation. Am J Respir Crit Care Med 162: 1932-1939, 2000.
14. Haynes T, Gutierrez C, Aycinena JC, Tsonis PA, Del Rio-Tsonis K. BMP signaling mediates stem/progenitor cell-induced retina regeneration. Proc Natl Acad Sci USA 104: 20380-20385, 2007.
15. Hofer-Warbinek R, Schmid JA, Stehlik C, Binder BR, Lipp J, de Martin R. Activation of NF-kappa B by XIAP, the X chromosome-linked inhibitor of apoptosis, in endothelial cells involves TAK1. J Biol Chem 275: 22064-22068, 2000.
16. Hsieh PC, Kenagy RD, Mulvihill ER, Jeanette JP, Wang X, Chang CM, Yao Z, Ruzzo WL, Justice S, Hudkins KL, Alpers CE, Berceli S, Clowes AW. Bone morphogenetic protein 4: potential regulator of shear stress-induced graft neointimal atrophy. J Vasc Surg 43: 150-158, 2006.
17. Jones JE, Walker JL, Song Y, Weiss N, Cardoso WV, Tuder RM, Loscalzo J, Zhang YY. Effect of 5-lipoxygenase on the development of pulmonary hypertension in rats. Am J Physiol Heart Circ Physiol 286: H1775-H1784, 2004.
18. Kennedy M, D'Souza SL, Lynch-Kattman M, Schwantz S, Keller G. Development of the hemangioblast defines the onset of hematopoiesis in human ES cell differentiation cultures. Blood 109: 2679-2687, 2007.
19. Kersten C, Dosen G, Myklebust JH, Sivertsen EA, Hystad ME, Smeland EB, Rian E. BMP-6 inhibits human bone marrow B lymphopoiesis-upregulation of Id1 and Id3. Exp Hematol 34: 72-81, 2006.
20. Lane KB, Machado RD, Pauciulo MW, Thomson JR, Phillips JA, 3rd Loyd JE, Nichols WC, Trembath RC. Heterozygous germline mutations in BMPR2, encoding a TGF-beta receptor, cause familial primary pulmonary hypertension. Int PPH Consort Nat Genet 26: 81-84, 2000.
21. Langenfeld EM, Langenfeld J. Bone morphogenetic protein-2 stimulates angiogenesis in developing tumors. Mol Cancer Res 2: 141-149, 2004.
22. Larsson J, Karlsson S. The role of Smad signaling in hematopoiesis. Oncogene 24: 5676-5692, 2005.
23. Liu D, Wang J, Kinzel B, Mueller M, Mao X, Valdez R, Liu Y, Li E. Dosage-dependent requirement of BMP type II receptor for maintenance of vascular integrity. Blood 110: 1502-1510, 2007.
24. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408, 2001.
25. Long L, MacLean MR, Jeffery TK, Morecroft I, Yang X, Rudarakanchana N, Southwood M, James V, Trembath RC, Morrell NW. Serotonin increases susceptibility to pulmonary hypertension in BMPR2-deficient mice. Circ Res 98: 818-827, 2006.
26. Lu M, Lin SC, Huang Y, Kang YJ, Rich R, Lo YC, Myszka D, Han J, Wu H. XIAP induces NF-kappaB activation via the BIR1/TAB1 interaction and BIR1 dimerization. Mol Cell 26: 689-702, 2007.
27. Lyden D, Hattori K, Dias S, Costa C, Blaikie P, Butros L, Chadburn A, Heissig B, Marks W, Witte L, Wu Y, Hicklin D, Zhu Z, Hackett NR, Crystal RG, Moore MA, Hajjar KA, Manova K, Benezra R, Rafii S. Impaired recruitment of bone-marrow-derived endothelial and hematopoietic precursor cells blocks tumor angiogenesis and growth. Nat Med 7: 1194-1201, 2001.
28. Lyden D, Young AZ, Zagzag D, Yan W, Gerald W, O'Reilly R, Bader BL, Hynes RO, Zhuang Y, Manova K, Benezra R. Id1 and Id3 are required for neurogenesis, angiogenesis and vascularization of tumour xenografts. Nature 401: 670-677, 1999.
29. Miyazono K, Maeda S, Imamura T. BMP receptor signaling: transcriptional targets, regulation of signals, and signaling cross-talk. Cytokine Growth Factor Rev 16: 251-263, 2005.
30. Molteni A, Ward WF, Ts'ao CH, Solliday NH. Monocrotaline pneumotoxicity in mice. Virchows Arch B Cell Pathol Incl Mol Pathol 57: 149-155, 1989.
31. Morty RE, Nejman B, Kwapiszewska G, Hecker M, Zakrzewicz A, Kouri FM, Peters DM, Dumitrascu R, Seeger W, Knaus P, Schermuly RT, Eickelberg O. Dysregulated bone morphogenetic protein signaling in monocrotaline-induced pulmonary arterial hypertension. Arterioscler Thromb Vasc Biol 27: 1072-1078, 2007.
32. Newman JH, Wheeler L, Lane KB, Loyd E, Gaddipati R, Phillips JA, 3rd, Loyd JE. Mutation in the gene for bone morphogenetic protein receptor II as a cause of primary pulmonary hypertension in a large kindred. N Engl J Med 345: 319-324, 2001.
33. Nohe A, Hassel S, Ehrlich M, Neubauer F, Sebald W, Henis YI, Knaus P. The mode of bone morphogenetic protein (BMP) receptor oligomerization determines different BMP-2 signaling pathways. J Biol Chem 277: 5330-5338, 2002.
34. Park C, Afrikanova I, Chung YS, Zhang WJ, Arentson E, Fong Gh G, Rosendahl A, Choi K. A hierarchical order of factors in the generation of FLK1- and SCL-expressing hematopoietic and endothelial progenitors from embryonic stem cells. Development 131: 2749-2762, 2004.
35. Raida M, Clement JH, Leek RD, Ameri K, Bicknell R, Niederwieser D, Harris AL. Bone morphogenetic protein 2 (BMP-2) and induction of tumor angiogenesis. J Cancer Res Clin Oncol 131: 741-750, 2005.
36. Ramoshebi LN, Ripamonti U. Osteogenic protein-1, a bone morphogenetic protein, induces angiogenesis in the chick chorioallantoic membrane and synergizes with basic fibroblast growth factor and transforming growth factor-beta1. Anat Rec 259: 97-107, 2000.
37. Roth RA, Ganey PE. Arachidonic acid metabolites and the mechanisms of monocrotaline pneumotoxicity. Am Rev Respir Dis 136: 762-765, 1987.
38. Rothhammer T, Bataille F, Spruss T, Eissner G, Bosserhoff AK. Functional implication of BMP4 expression on angiogenesis in malignant melanoma. Oncogene 26: 4158-4170, 2007.
39. Schultze AE, Roth RA. Chronic pulmonary hypertension - the monocrotaline model and involvement of the hemostatic system. J Toxicol Environ Health B Crit Rev 1: 271-346, 1998.
40. Song Y, Jones JE, Beppu H, Keaney JF Jr, Loscalzo J, Zhang YY. Increased susceptibility to pulmonary hypertension in heterozygous BMPR2-mutant mice. Circulation 112: 553-562, 2005.
41. Sorescu GP, Sykes M, Weiss D, Platt MO, Saha A, Hwang J, Boyd N, Boo YC, Vega JD, Taylor WR, Jo H. Bone morphogenic protein 4 produced in endothelial cells by oscillatory shear stress stimulates an inflammatory response. J Biol Chem 278: 31128-31135, 2003.
42. Stenmark KR, Morganroth ML, Remigio LK, Voelkel NF, Murphy RC, Henson PM, Mathias MM, Reeves JT. Alveolar inflammation and arachidonate metabolism in monocrotaline-induced pulmonary hypertension. Am J Physiol Heart Circ Physiol 248: H859-H866, 1985.
43. Taraseviciene-Stewart L, Kasahara Y, Alger L, Hirth P, Mc Mahon G, Waltenberger J, Voelkel NF, Tuder RM. Inhibition of the VEGF receptor 2 combined with chronic hypoxia causes cell death-dependent pulmonary endothelial cell proliferation and severe pulmonary hypertension. FASEB J 15: 427-438, 2001.
44. Teichert-Kuliszewska K, Kutryk MJ, Kuliszewski MA, Karoubi G, Courtman DW, Zucco L, Granton J, Stewart DJ. Bone morphogenetic protein receptor-2 signaling promotes pulmonary arterial endothelial cell survival: implications for loss-of-function mutations in the pathogenesis of pulmonary hypertension. Circ Res 98: 209-217, 2006.
45. ten Dijke P, Korchynskyi O, Valdimarsdottir G, Goumans MJ. Controlling cell fate by bone morphogenetic protein receptors. Mol Cell Endocrinol 211: 105-113, 2003.
46. Thomson JR, Machado RD, Pauciulo MW, Morgan NV, Humbert M, Elliott GC, Ward K, Yacoub M, Mikhail G, Rogers P, Newman J, Wheeler L, Higenbottam T, Gibbs JS, Egan J, Crozier A, Peacock A, Allcock R, Corris P, Loyd JE, Trembath RC, Nichols WC. Sporadic primary pulmonary hypertension is associated with germline mutations of the gene encoding BMPR-II, a receptor member of the TGF-beta family. J Med Genet 37: 741-745, 2000.
47. Tuder RM, Voelkel NF. Pulmonary hypertension and inflammation. J Lab Clin Med 132: 16-24, 1998.
48. Umehara H, Bloom ET, Okazaki T, Nagano Y, Yoshie O, Imai T. Fractalkine in vascular biology: from basic research to clinical disease. Arterioscler Thromb Vasc Biol 24: 34-40, 2004.
49. Ungvari Z, Csiszar A, Edwards JG, Kaminski PM, Wolin MS, Kaley G, Koller A. Increased superoxide production in coronary arteries in hyperhomocysteinemia: role of tumor necrosis factor-alpha, NAD(P)H oxidase, and inducible nitric oxide synthase. Arterioscler Thromb Vasc Biol 23: 418-424, 2003.
50. Valdimarsdottir G, Goumans MJ, Rosendahl A, Brugman M, Itoh S, Lebrin F, Sideras P, ten Dijke P. Stimulation of Id1 expression by bone morphogenetic protein is sufficient and necessary for bone morphogenetic protein-induced activation of endothelial cells. Circulation 106: 2263-2270, 2002.
51. West J, Fagan K, Steudel W, Fouty B, Lane K, Harral J, Hoedt-Miller M, Tada Y, Ozimek J, Tuder R, Rodman DM. Pulmonary hypertension in transgenic mice expressing a dominant-negative BMPRII gene in smooth muscle. Circ Res 94: 1109-1114, 2004.
52. Yamaguchi K, Nagai S, Ninomiya-Tsuji J, Nishita M, Tamai K, Irie K, Ueno N, Nishida E, Shibuya H, Matsumoto K. XIAP, a cellular member of the inhibitor of apoptosis protein family, links the receptors to TAB1-TAK1 in the BMP signaling pathway. Embo J 18: 179-187, 1999.
53. Zhao YD, Campbell AI, Robb M, Ng D, Stewart DJ. Protective role of angiopoietin-1 in experimental pulmonary hypertension. Circ Res 92: 984-991, 2003.