The cancer paradigm of severe pulmonary arterial hypertension

American Journal of Respiratory and Critical Care Medicine

Volumn 178, Issue 6, 2008, Pages 558-564

  Rai, Pradeep R ^a   Cool, Carlyne D ^a   King, Judy A C ^b   Stevens, Troy ^b   Burns, Nana ^a   Winn, Robert A ^a   Kasper, Michael ^c   Voelkel, Norbert F ^d  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF SOUTH ALABAMA COLLEGE OF MEDICINE   (United States)

^c DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^d VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

Angiogenesis; Cancer; Plexiform lesions; Pulmonary arterial hypertension

Indexed keywords

ACTIVATED LEUKOCYTE CELL ADHESION MOLECULE; CAVEOLIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; NITRIC OXIDE SYNTHASE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROTEIN P27; STEM CELL FACTOR; TRANSCRIPTION FACTOR NFAT; VASCULOTROPIN; VASCULOTROPIN RECEPTOR; WNT PROTEIN;

ANGIOGENESIS; ANTIANGIOGENIC ACTIVITY; ARTERY INTIMA PROLIFERATION; AUTOIMMUNE THYROIDITIS; AUTOIMMUNITY; B LYMPHOCYTE ACTIVATION; CANCER EPIDEMIOLOGY; CANCER GROWTH; CANCER INVASION; CHANNELOPATHY; COLON ADENOCARCINOMA; DENDRITIC CELL; DISEASE ASSOCIATION; DISEASE CLASSIFICATION; DISEASE SEVERITY; ENDOTHELIUM CELL; EPIGENETICS; GENETIC SUSCEPTIBILITY; HUMAN; LIVER CELL CARCINOMA; LUNG VASOCONSTRICTION; NEOPLASM; NONHUMAN; PATHOGENESIS; PATHOPHYSIOLOGY; PRIMARY SCLEROSING CHOLANGITIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PULMONARY ARTERY; PULMONARY HYPERTENSION; REGULATORY T LYMPHOCYTE; REVIEW; SMOOTH MUSCLE FIBER; T LYMPHOCYTE ACTIVATION; THYROID CANCER; TUMOR SUPPRESSOR GENE; ULCERATIVE COLITIS;

CELL PROLIFERATION; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION; HUMANS; HYPERTENSION, PULMONARY; IMMUNOHISTOCHEMISTRY; NEOPLASMS; PULMONARY ARTERY; TERMINOLOGY AS TOPIC; VASOCONSTRICTION; WNT PROTEINS;

EID: 51849167730     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.200709-1369PP     Document Type: Review

References (77)

1. Simonneau G, Galiè N, Rubin LJ, Langleben D, Seeger W, Domenighetti G, Gibbs S, Lebrec D, Speich R, Beghetti M, et al. Clinical classification of pulmonary hypertension. J Am Coll Cardiol 2004;43(12, Suppl S):5S-12S.
2. McLaughlin VV, Shillington A, Rich S. Survival in primary pulmonary hypertension: the impact of epoprostenol therapy. Circulation 2002;106:1477-1482.
3. Galiè N, Ghofrani HA, Torbicki A, Barst RJ, Rubin LJ, Badesch D, Fleming T, Parpia T, Burgess G, Branzi A, et al. Sildenafil citrate therapy for pulmonary arterial hypertension. N Engl J Med 2005;353:2148-2157. [Published erratum appears in N Engl J Med 2006;354:2400-2401.]
4. Shapiro B, Nishimura RA, McGoon MD, Redfield MM. Diagnostic dilemmas: diastolic heart failure causing pulmonary hypertension and pulmonary hypertension causing diastolic dysfunction. Advances in Pulmonary Hypertension 2006;5:13-20.
5. Nicolls MR, Taraseviciene-Stewart L, Rai PR, Badesch DB, Voelkel NF. Autoimmunity and pulmonary hypertension: a perspective. Eur Respir J 2005;26:1110-1118.
6. Tuder RM, Groves B, Badesch DB, Voelkel NF. Exuberant endothelial cell growth and elements of inflammation are present in plexiform lesions of pulmonary hypertension. Am J Pathol 1994;144:275-285.
7. Tuder RM, Cool CD, Yeager ME, Taraseviciene-Stewart L, Bull TM, Voelkel NF. The pathobiology of pulmonary hypertension. Clin Chest Med 2001;22:405-418.
8. Cool CD, Stewart JS, Werahera P, Miller GJ, Williams RL, Voelkel NF, Tuder RM. Three-dimensional reconstruction of pulmonary arteries in plexiform pulmonary hypertension using cell-specific markers: evidence for a dynamic and heterogeneous process of pulmonary endothelial cell growth. Am J Pathol 1999;155:411-419.
9. Dresdale DT, Michtom RJ, Schultz M. Recent studies in primary pulmonary hypertension, including pharmacodynamic observations on pulmonary vascular resistance. Bull NY Acad Med 1954;30:195-207.
10. Rubin LJ. Primary pulmonary hypertension. Chest 1993;104:236-250.
11. Wagenvoort CA. Vasoconstrictive primary pulmonary hypertension and pulmonary veno-occlusive disease. Cardiovasc Clin 1972;4:97-113.
12. Davies P, Reid L. Hypoxic remodeling of the rat pulmonary arterial microcirculation assessed by microdissection. J Appl Physiol 1991;71:1886-1891.
13. Schermuly RT, Dony E, Ghofrani HA, Pullamsetti S, Savai R, Roth M, Sydykov A, Lai YJ, Weissmann N, Seeger W, et al. Reversal of experimental pulmonary hypertension by PDGF inhibition. J Clin Invest 2005;115:2811-2821.
14. Merklinger SL, Jones PL, Martinez EC, Rabinovitch M. Epidermal growth factor receptor blockade mediates smooth muscle cell apoptosis and improves survival in rats with pulmonary hypertension. Circulation 2005;112:423-431.
15. Crossno JT Jr, Garat CV, Reusch JE, Morris KG, Dempsey EC, McMurtry IF, Stenmark KR, Klemm DJ. Rosiglitazone attenuates hypoxia-induced pulmonary arterial remodeling. Am J Physiol Lung Cell Mol Physiol 2007;292:L885-L897.
16. Campian ME, Hardziyenka M, Michel MC, Tan HL. How valid are animal models to evaluate treatments for pulmonary hypertension? Naunyn Schmiedebergs Arch Pharmacol 2006;373:391-400.
17. Paddenberg R, Stieger P, von Lilien AL, Faulhammer P, Goldenberg A, Tillmanns HH, Kummer W, Braun-Dullaeus RC. Rapamycin attenuates hypoxia-induced pulmonary vascular remodeling and right ventricular hypertrophy in mice. Respir Res 2007;8:15.
18. Rich S, Kaufmann E, Levy PS. The effect of high doses of calcium-channel blockers on survival in primary pulmonary hypertension. N Engl J Med 1992;327:76-81.
19. Sitbon O, Humbert M, Jais X, Ioos V, Hamid AM, Provencher S, Garcia G, Parent F, Herve P, Simonneau G. Long-term response to calcium channel blockers in idiopathic pulmonary arterial hypertension. Circulation 2005;111:3105-3111.
20. Yeager ME, Halley GR, Golpon HA, Voelkel NF, Tuder RM. Microsatellite instability of endothelial cell growth and apoptosis genes within plexiform lesions in primary pulmonary hypertension. Circ Res 2001;88:E2-E11.
21. Ivy DD, McMurtry IF, Colvin K, Imamura M, Oka M, Lee DS, Gebb S, Jones PL. Development of occlusive neointimal lesions in distal pulmonary arteries of endothelin B receptor-deficient rats: a new model of severe pulmonary arterial hypertension. Circulation 2005;111:2988-2996.
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 1997;151:1019-1025.
23. Cool CD, Rai PR, Yeager ME, Hernandez-Saavedra D, Serls AE, Bull TM, Geraci MW, Brown KK, Routes JM, Tuder RM, et al. Expression of human herpes virus 8 in primary pulmonary hypertension. N Engl J Med 2003;349:1113-1122.
24. Ameshima S, Golpon H, Cool CD, Chan D, Vandivier RW, Gardai SJ, Wick M, Nemenoff RA, Geraci MW, Voelkel NF. Peroxisome proliferator-activated receptor gamma (PPARgamma) expression is decreased in pulmonary hypertension and affects endothelial cell growth. Circ Res 2003;92:1162-1169.
25. Achcar RO, Demura Y, Rai PR, Taraseviciene-Stewart L, Kasper M, Voelkel NF, Cool CD. Loss of caveolin and heme oxygenase expression in severe pulmonary hypertension. Chest 2006;129:696-705.
26. Murray F, Patel HH, Suda RY, Zhang S, Thistlethwaite PA, Yuan JX, Insel PA. Expression and activity of cAMP phosphodiesterase isoforms in pulmonary artery smooth muscle cells from patients with pulmonary hypertension: role for PDE1. Am J Physiol Lung Cell Mol Physiol 2007;292:L294-L303.
27. Masri FA, Xu W, Comhair SA, Asosingh K, Koo M, Vasanji A, Drazba J, Anand-Apte B, Erzurum SC. Hyperproliferative apoptosis-resistant endothelial cells in idiopathic pulmonary arterial hypertension. Am J Physiol Lung Cell Mol Physiol 2007;293:L548-L554.
28. Yuan JX, Aldinger AM, Juhaszova M, Wang J, Conte JV Jr, Gaine SP, Orens JB, Rubin LJ. Dysfunctional voltage-gated K+ channels in pulmonary artery smooth muscle cells of patients with primary pulmonary hypertension. Circulation 1998;98:1400-1406.
29. Sakao S, Taraseviciene-Stewart L, Lee JD, Wood K, Cool CD, Voelkel NF. Initial apoptosis is followed by increased proliferation of apoptosis-resistant endothelial cells. FASEB J 2005;19:1178-1180.
30. Yoder MC, Mead LE, Prater D, Krier TR, Mroueh KN, Li F, Krasich R, Temm CJ, Prchal JT, Ingram DA. Redefining endothelial progenitor cells via clonal analysis and hematopoietic stem/progenitor cell principals. Blood 2007;109:1801-1809.
31. Sahara M, Sata M, Morita T, Nakamura K, Hirata Y, Nagai R. Diverse contribution of bone marrow-derived cells to vascular remodeling associated with pulmonary arterial hypertension and arterial neointimal formation. Circulation 2007;115:509-517.
32. Steinman RM, Banchereau J. Taking dendritic cells into medicine. Nature 2007;449:419-426.
33. 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 2007;175:1280-1289.
34. Cool CD, Groshong SD, Oakey J, Voelkel NF. Pulmonary hypertension: cellular and molecular mechanisms. Chest 2005;128:565S-571S.
35. Voelkel NF, Cool C, Lee SD, Wright L, Geraci MW, Tuder RM. Primary pulmonary hypertension between inflammation and cancer. Chest 1998;114:225S-230S.
36. Hanahan D, Weinberg R. The hallmarks of cancer. Cell 2000;100:57-70.
37. Levy M, Maurey C, Celermajer DS, Vouhe PR, Danel C, Bonnet D, Israel-Biet D. Impaired apoptosis of pulmonary endothelial cells is associated with intimal proliferation and irreversibility of pulmonary hypertension in congenital heart disease. J Am Coll Cardiol 2007;49:803-810.
38. McMurtry MS, Archer SL, Altieri DC, Bonnet S, Haromy A, Harry G, Bonnet S, Puttagunta L, Michelakis ED. Gene therapy targeting survivin selectively induces pulmonary vascular apoptosis and reverses pulmonary arterial hypertension. J Clin Invest 2005;115:1479-1491.
39. Norton L, Massague J. Is cancer a disease of self-seeding? Nat Med 2006;12:875-878.
40. Tuder RM, Cool CD, Geraci MW, Wang J, Abman SH, Wright L, Badesch D, Voelkel NF. Prostacyclin synthase expression is decreased in lungs from patients with severe pulmonary hypertension. Am J Respir Crit Care Med 1999;159:1925-1932.
41. Richter A, Yeager ME, Zaiman A, Cool CD, Voelkel NF, Tuder RM. Impaired transforming growth factor-β signaling in idiopathic pulmonary arterial hypertension. Am J Respir Crit Care Med 2004;170:1340-1348.
42. King JA, Ofori-Acquah SF, Stevens T, Al-Mehdi AB, Fodstad O, Jiang WG. Activated leukocyte cell adhesion molecule in breast cancer: prognostic indicator. Breast Cancer Res 2004;6:R478-R487.
43. Xu W, Koeck T, Lara AR, Neumann D, DiFilippo FP, Koo M, Janocha AJ, Masri FA, Arroliga AC, Jennings C, et al. Alterations of cellular bioenergetics in pulmonary artery endothelial cells. Proc Natl Acad Sci USA 2007;104:1342-1347.
44. Sundberg C, Nagy JA, Brown LF, Feng D, Eckelhoefer IA, Manseau EJ, Dvorak AM, Dvorak HF. Glomeruloid microvascular proliferation follows adenoviral vascular permeability factor/vascular endothelial growth factor-164 gene delivery. Am J Pathol 2001;158:1145-1160.
45. McDonald DM, Baluk P. Imaging of angiogenesis in inflamed airways and tumors: newly formed blood vessels are not alike and may be wildly abnormal: Parker B. Francis lecture. Chest 2005;128:602S-608S.
46. Perros F, Dorfmuller P, Souza R, Durand-Gasselin I, Mussot S, Mazmanian M, Herve P, Emilie D, Simonneau G, Humbert M. Dendritic cell recruitment in lesions of human and experimental pulmonary hypertension. Eur Respir J 2007;29:462-468.
47. Heissig B, Rafii S, Akiyama H, Ohki Y, Sato Y, Rafael T, Zhu Z, Hicklin DJ, Okumura K, Ogawa H, et al. Low-dose irradiation promotes tissue revascularization through VEGF release from mast cells and MMP-9-mediated progenitor cell mobilization. J Exp Med 2005;202:739-750.
48. Gao J, Dennis JE, Muzic RF, Lundberg M, Caplan AI. The dynamic in vivo distribution of bone marrow-derived mesenchymal stem cells after infusion. Cells Tissues Organs. 2001;169:12-20.
49. Kraitchman DL, Tatsumi M, Gilson WD, Ishimori T, Kedziorek D, Walczak P, Segars WP, Chen HH, Fritgges D, Izbudak I, et al. Dynamic imaging of allogeneic mesenchymal stem cells trafficking to myocardial infarction. Circulation. 2005;112:1451-1461.
50. Scadden DT. The stem-cell niche as an entity of action. Nature 2006;441:1075-1079.
51. Fokas E, Engenhart-Cabillic R, Daniilidis K, Rose F, An HX. Metastasis: the seed and soil theory gains identity. Cancer Metastasis Rev 2007;26:705-715.
52. INK4A in human endometrial adenocarcinoma. Exp Oncol 2006;28:152-155.
53. ARF gene hypermethylation in human colon cancer. Pathol Res Pract 2006;202:415-424.
54. Archer SL, Huang JM, Hampl V, Nelson DP, Shultz PJ, Weir EK. Nitric oxide and cGMP cause vasorelaxation by activation of a charybdotoxin-sensitive K channel by cGMP-dependent protein kinase. Proc Natl Acad Sci USA 1994;91:7583-7587.
55. Ekhterae D, Platoshyn O, Krick S, Yu Y, McDaniel SS, Yuan JX. Bcl-2 decreases voltage-gated K+ channel activity and enhances survival in vascular smooth muscle cells. Am J Physiol Cell Physiol 2001;281:C157-C165.
56. + channels before inducing apoptosis. Am J Physiol Cell Physiol 2002;283:C1298-C1305.
57. K(V) and enhances apoptosis. Am J Physiol Cell Physiol 2004;287:C715-C722.
58. McMurtry MS, Bonnet S, Wu X, Dyck JR, Haromy A, Hashimoto K, Michelakis ED. Dichloroacetate prevents and reverses pulmonary hypertension by inducing pulmonary artery smooth muscle cell apoptosis. Circ Res 2004;95:830-840.
59. Pardo LA. Voltage-gated potassium channels in cell proliferation. Physiology (Bethesda) 2004;19:285-292.
60. Stühmer W, Alves F, Hartung F, Zientkowska M, Pardo LA. Potassium channels as tumour markers. FEBS Lett 2006;580:2850-2852.
61. + channel axis is suppressed in cancer and its normalization promotes apoptosis and inhibits cancer growth. Cancer Cell 2007;11:37-51.
62. 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 U S A 2007;104:11418-11423.
63. O'Byrne KJ, Dalgleish AG, Browning MJ, Steward WP, Harris AL. The relationship between angiogenesis and the immune response in carcinogenesis and the progression of malignant disease. Eur J Cancer 2000;36:151-169.
64. - lymphocytes is thymus and proliferation independent. Cancer Res 2006;66:4488-4495.
65. Ulrich S, Nicolls MR, Taraseviciene L, Speich R, Voelkel N. Increased regulatory and decreased CD8+ cytotoxic T cells in the blood of patients with idiopathic pulmonary arterial hypertension. Respiration 2008;75:272-280.
66. Aldred MA, Vijayakrishnan J, James V, Soubrier F, Gomez-Sanchez MA, Martensson G, Galie N, Manes A, Corris P, Simonneau G, et al. BMPR2 gene rearrangements account for a significant proportion of mutations in familial and idiopathic pulmonary arterial hypertension. Hum Mutat 2006;27:212-213.
67. WAF1 stabilization and modulated by RAS/ERK. Cell Signal 2007;19:1465-1472.
68. Katoh M. Networking of WNT, FGF, Notch, BMP, and Hedgehog signaling pathways during carcinogenesis. Stem Cell Rev 2007;3:30-38.
69. Ye L, Lewis-Russell JM, Kyanaston HG, Jiang WG. Bone morphogenetic proteins and their receptor signaling in prostate cancer. Histol Histopathol 2007;22:1129-1147.
70. Morrell NW, Yang X, Upton PD, Jourdan KB, Morgan N, Sheares KK, Trembath RC. Altered growth responses of pulmonary artery smooth muscle cells from patients with primary pulmonary hypertension to transforming growth factor-B1 and bone morphogenetic proteins. Circulation 2001;104:790-795.
71. Jeffery TK, Upton PD, Trembath RC, Morrell NW. BMP4 inhibits proliferation and prmotes myocyte differentiation of lung fiborblasts via Smad1 and JNK pathways. Am J Physiol Lung Cell Mol Physiol 2005;288:L370-L378.
72. Ihida-Stansbury K, McKean DM, Lane KB, Loyd JE, Wheeler LA, Morrell NW, Jones PL. Tenascin-C is induced by mutated BMP type II receptors in familial forms of pulmonary arterial hypertension. Am J Physiol Lung Cell Mol Physiol 2006;291:L694-L702.
73. Voelkel NF, Nicolls MR. The central role of endothelial cells in severe angioproliferative pulmonary hypertension. In: Aird WC, editor. Endothelial biomedicine. New York: Cambridge University Press; 2000. pp. 1193-1198.
74. 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 2007;175:1280-1289.
75. Benekli M, Baer MR, Baumann H, Wetzler M. Signal transducer and activator of transcription proteins in leukemias. Blood 2003;101:2940-2954.
76. Kawamura C, Kizaki M, Yamato K, Uchida H, Fukuchi Y, Hattori Y, Koseki T, Nishihara T, Ikeda Y. Bone morphogenetic protein-2 induces apoptosis in human myeloma cells with modulation of STAT3. Blood 2000;96:2005-2011.
77. Pepper MS. Transforming growth factor-beta: vasculogenesis, angiogenesis, and vessel wall integrity. Cytokine Growth Factor Rev 1997;8:21-43.