Pneumonectomy combined with SU5416 induces severe pulmonary hypertension in rats

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 310, Issue 11, 2016, Pages L1088-L1097

  Happe C M ^a   de Raaf, M A ^a   Rol, N ^a   Schalij, I ^a   Vonk Noordegraaf, A ^a   Westerhof, N ^a   Voelkel, N F ^b   de Man, F S ^a   Bogaard, H J ^a  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

Flow; Hypoxia; Pneumonectomy; Pulmonary hypertension; SU5416

Indexed keywords

CD20 ANTIGEN; CD68 ANTIGEN; CD8 ANTIGEN; SEMAXANIB; INDOLE DERIVATIVE; PYRROLE DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; B LYMPHOCYTE; BLOOD FLOW VELOCITY; CELL PROLIFERATION; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; HEART RIGHT VENTRICLE PRESSURE; HEART VENTRICLE CONTRACTILITY; HEMATOCRIT; HISTOPATHOLOGY; LUNG ALVEOLUS MACROPHAGE; LUNG BLOOD FLOW; LUNG BLOOD VESSEL; LUNG RESECTION; MALE; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; PULMONARY HYPERTENSION; RAT; SPRAGUE DAWLEY RAT; SYSTOLIC BLOOD PRESSURE; VASCULAR ENDOTHELIAL CELL; VASCULAR REMODELING; ANIMAL; BLOOD PRESSURE; DISEASE MODEL; HYPERTENSION, PULMONARY; PATHOLOGY;

ANIMALS; BLOOD PRESSURE; DISEASE MODELS, ANIMAL; HYPERTENSION, PULMONARY; INDOLES; MALE; PNEUMONECTOMY; PYRROLES; RATS, SPRAGUE-DAWLEY;

EID: 84984656697     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00023.2016     Document Type: Article

References (41)

1. Abe K, Toba M, Alzoubi A, Ito M, Fagan KA, Cool CD, Voelkel NF, McMurtry IF, Oka M. Formation of plexiform lesions in experimental severe pulmonary arterial hypertension. Circulation 121: 2747-2754, 2010.
2. Chemla D, Castelain V, Humbert M, Hébert JL, Simonneau G, Lecarpentier Y, Hervé P. New formula for predicting mean pulmonary artery pressure using systolic pulmonary artery pressure. Chest 126: 1313-1317, 2004.
3. Chiu JJ, Chien S. Effects of disturbed flow on vascular endothelium: pathophysiological basis and clinical perspectives. Physiol Rev 91: 327-387, 2011.
4. Coon BG, Baeyens N, Han J, Budatha M, Ross TD, Fang JS, Yun S, Thomas JL, Schwartz MA. Intramembrane binding of VE-cadherin to VEGFR2 and VEGFR3 assembles the endothelial mechanosensory complex. J Cell Biol 208: 975-986, 2015.
5. de Raaf MA, Schalij I, Gomez-Arroyo J, Rol N, Happé C, de Man FS, Vonk-Noordegraaf A, Westerhof N, Voelkel NF, Bogaard HJ. SuHx rat model: partly reversible pulmonary hypertension and progressive intima obstruction. Eur Respir J 44: 160-168, 2014.
6. Dickinson MG, Bartelds B, Borgdorff MAJ, Berger RMF. The role of disturbed blood flow in the development of pulmonary arterial hypertension: lessons from preclinical animal models. Am J Physiol Lung Cell Mol Physiol 305: L1-L14, 2013.
7. Dickinson MG, Bartelds B, Molema G, Borgdorff MA, Boersma B, Takens J, Weij M, Wichers P, Sietsma H, Berger RMF. Egr-1 expression during neointimal development in flow-associated pulmonary hypertension. Am J Pathol 179: 2199-2209, 2011.
8. Dorfmüller P, Chaumais MC, Giannakouli M, Durand-Gasselin I, Raymond N, Fadel E, Mercier O, Charlotte F, Montani D, Simonneau G, Humbert M, Perros F. Increased oxidative stress and severe arterial remodeling induced by permanent high-flow challenge in experimental pulmonary hypertension. Respir Res 12: 119, 2011.
9. Golpon HA, Fadok VA, Taraseviciene-Stewart L, Scerbavicius R, Sauer C, Welte T, Henson PM, Voelkel NF. Life after corpse engulfment: phagocytosis of apoptotic cells leads to VEGF secretion and cell growth. FASEB J 18: 1716-1718, 2004.
10. Guignabert C, Tu L, Le Hiress M, Ricard N, Sattler C, Seferian A, Huertas A, Humbert M, Montani D. Pathogenesis of pulmonary arterial hypertension: lessons from cancer. Eur Respir Rev 22: 543-551, 2013.
11. Handoko ML, de Man FS, Happé CM, Schalij I, Musters RJP, Westerhof N, Postmus PE, Paulus WJ, Laarse van der WJ, Vonk-Noordegraaf A. Opposite effects of training in rats with stable and progressive pulmonary hypertension. Circulation 120: 42-49, 2009.
12. Handoko ML, Schalij I, Kramer K, Sebkhi A, Postmus PE, van der Laarse WJ, Paulus WJ, Vonk-Noordegraaf A. A refined radio-telemetry technique to monitor right ventricle or pulmonary artery pressures in rats: a useful tool in pulmonary hypertension research. Pflügers Arch 455: 951-959, 2008.
13. Jones JE, Mendes L, Rudd MA, Russo G, Loscalzo J, Zhang YY. Serial noninvasive assessment of progressive pulmonary hypertension in a rat model. Am J Physiol Heart Circ Physiol 283: H364-H371, 2002.
14. Kasahara Y, Tuder RM, Taraseviciene-Stewart L, Le Cras TD, Abman S, Hirth PK, Waltenberger J, Voelkel NF. Inhibition of VEGF receptors causes lung cell apoptosis and emphysema. J Clin Invest 106: 1311-1319, 2000.
15. Kato Y, Iwase M, Kanazawa H, Kawata N, Yoshimori Y, Hashimoto K, Yokoi T, Noda A, Takagi K, Koike Y, Nishizawa T, Nishimura M, Yokota M. Progressive development of pulmonary hypertension leading to right ventricular hypertrophy assessed by echocardiography in rats. Exp Anim 52: 285-294, 2003.
16. Kim N, Voicu L, Hare GMT, Cheema-Dhadli S, Chong CK, Chan SKW, Bichet DG, Halperin ML, Mazer CD. Response of the renal inner medulla to hypoxia: possible defense mechanisms. Nephron Physiol 121: 1-7, 2012.
17. Li D, Fernandez LG, Dodd-o J, Langer J, Wang D, Laubach VE. Upregulation of hypoxia-induced mitogenic factor in compensatory lung growth after pneumonectomy. Am J Respir Cell Mol Biol 32: 185-191, 2005.
18. Li F, Xia W, Li A, Zhao C, Sun R. Long-term inhibition of Rho kinase with fasudil attenuates high flow induced pulmonary artery remodeling in rats. Pharmacol Res 55: 64-71, 2007.
19. Mizuno S, Farkas L, Husseini AA, Farkas D, Gomez-Arroyo J, Kraskauskas D, Nicolls MR, Cool CD, Bogaard HJ, Voelkel NF. Severe pulmonary arterial hypertension induced by SU5416 and ovalbumin immunization. Am J Respir Cell Mol Biol 47: 679-687, 2012.
20. Nicolls MR, Mizuno S, Taraseviciene-Stewart L, Farkas L, Drake JI, Al Husseini A, Gomez-Arroyo JG, Voelkel NF, Bogaard HJ. New models of pulmonary hypertension based on VEGF receptor blockade-induced endothelial cell apoptosis. Pulm Circ 2: 434-442, 2012.
21. Oka M, Homma N, Taraseviciene-Stewart L, Morris KG, Kraskauskas D, Burns N, Voelkel NF, McMurtry IF. Rho kinase-mediated vasoconstriction is important in severe occlusive pulmonary arterial hypertension in rats. Circ Res 100: 923-929, 2007.
22. Okada K, Tanaka Y, Bernstein M, Zhang W, Patterson GA, Botney MD. Pulmonary hemodynamics modify the rat pulmonary artery response to injury. A neointimal model of pulmonary hypertension. Am J Pathol 151: 1019-1025, 1997.
23. Plante E, Lachance D, Roussel E, Drolet MC, Arsenault M, Couet J. Impact of anesthesia on echocardiographic evaluation of systolic and diastolic function in rats. J Am Soc Echocardiogr 19: 1520-1525, 2006.
24. Rai PR, Cool CD, King JAC, Stevens T, Burns N, Winn RA, Kasper M, Voelkel NF. The cancer paradigm of severe pulmonary arterial hypertension. Am J Respir Crit Care Med 178: 558-564, 2008.
25. Ranchoux B, Antigny F, Rucker-Martin C, Hautefort A, Péchoux C, Bogaard HJ, Dorfmüller P, Remy S, Lecerf F, Planté S, Chat S, Fadel E, Houssaini A, Anegon I, Adnot S, Simonneau G, Humbert M, Cohen-Kaminsky S, Perros F. Endothelial-to-mesenchymal transition in pulmonary hypertension. Circulation 131: 1006-1018, 2015.
26. Rannels DE, Rannels SR. Compensatory growth of the lung following partial pneumonectomy. Exp Lung Res 14: 157-182, 1988.
27. Ravikumar P, Yilmaz C, Bellotto DJ, Dane DM, Estrera AS, Hsia CCW. Separating in vivo mechanical stimuli for postpneumonectomy compensation: imaging and ultrastructural assessment. J Appl Physiol 114: 961-970, 2013.
28. Sakao S, Tatsumi K. The effects of antiangiogenic compound SU5416 in a rat model of pulmonary arterial hypertension. Respiration 81: 253-261, 2011.
29. Selimovic N, Rundqvist B, Bergh CH, Andersson B, Petersson S, Johansson L, Bech-Hanssen O. Assessment of pulmonary vascular resistance by Doppler echocardiography in patients with pulmonary arterial hypertension. J Heart Lung Transplant 26: 927-934, 2007.
30. Simonneau G, Robbins IM, Beghetti M, Channick RN, Delcroix M, Denton CP, Elliott CG, Gaine SP, Gladwin MT, Jing ZC, Krowka MJ, Langleben D, Nakanishi N, Souza R. Updated clinical classification of pulmonary hypertension. J Am Coll Cardiol 54: S43-S54, 2009.
31. Szulcek R, Happé CM, Rol N, Fontijn RD, Dickhoff C, Hartemink KJ, Grünberg K, Tu L, Timens W, Nossent GD, Paul MA, Leyen TA, Horrevoets AJ, de Man FS, Guignabert C, Yu PB, Vonk-Noordegraaf A, van Nieuw Amerongen GP, Bogaard HJ. Delayed microvascular shear-adaptation in pulmonary arterial hypertension: role of PECAM-1 cleavage. Am J Respir Crit Care Med doi: 10.1164/rccm.201506-1231OC [Epub ahead of print
32. Tamosiuniene R, Nicolls MR. Regulatory T cells and pulmonary hypertension. Trends Cardiovasc Med 21: 166-171, 2011.
33. 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.
34. Taraseviciene-Stewart L, Nicolls MR, Kraskauskas D, Scerbavicius R, Burns N, Cool C, Wood K, Parr JE, Boackle SA, Voelkel NF. Absence of T cells confers increased pulmonary arterial hypertension and vascular remodeling. Am J Respir Crit Care Med 175: 1280-1289, 2007.
35. Toba M, Alzoubi A, O’Neill KD, Gairhe S, Matsumoto Y, Oshima K, Abe K, Oka M, McMurtry IF. Temporal hemodynamic and histological progression in Sugen5416/hypoxia/normoxia-exposed pulmonary arterial hypertensive rats. Am J Physiol Heart Circ Physiol 306: H243-H250, 2014.
36. Tzima E, Irani-Tehrani M, Kiosses WB, Dejana E, Schultz DA, Engelhardt B, Cao G, DeLisser H, Schwartz MA. A mechanosensory complex that mediates the endothelial cell response to fluid shear stress. Nature 437: 426-431, 2005.
37. van Albada ME, Bartelds B, Wijnberg H, Mohaupt S, Dickinson MG, Schoemaker RG, Kooi K, Gerbens F, Berger RMF. Gene expression profile in flow-associated pulmonary arterial hypertension with neointimal lesions. Am J Physiol Lung Cell Mol Physiol 298: L483-L491, 2010.
38. Voelkel NF, Gomez-Arroyo J, Abbate A, Bogaard HJ, Nicolls MR. Pathobiology of pulmonary arterial hypertension and right ventricular failure. Eur Respir J 40: 1555-1565, 2012.
39. Voelkel NF, Vandivier RW, Tuder RM. Vascular endothelial growth factor in the lung. Am J Physiol Lung Cell Mol Physiol 290: L209-L221, 2006.
40. Westerhof N, Stergiopulos N, Noble MIM. Snapshots of Hemodynamics: an Aid for Clinical Research and Graduate Education. Springer Science & Business Media, 2010.
41. White RJ, Meoli DF, Swarthout RF, Kallop DY, Galaria II, Harvey JL, Miller CM, Blaxall BC, Hall CM, Pierce RA, Cool CD, Taubman MB. Plexiform-like lesions and increased tissue factor expression in a rat model of severe pulmonary arterial hypertension. Am J Physiol Lung Cell Mol Physiol 293: L583-L590, 2007