Sustained hypoxia leads to the emergence of cells with enhanced growth, migratory, and promitogenic potentials within the distal pulmonary artery wall

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 297, Issue 6, 2009, Pages

  Frid, Maria G ^a   Li, Min ^a   Gnanasekharan, Meena ^a   Burke, Danielle L ^a   Fragoso, Miguel ^a   Strassheim, Derek ^a   Sylman, Joanna L ^a   Stenmark, Kurt R ^a  

^a Children's Hospital Colorado   (United States)

Author keywords

Inflammation; Progenitor cells; Pulmonary hypertension; S100A4; Vascular remodeling

Indexed keywords

5' NUCLEOTIDASE; ALPHA SMOOTH MUSCLE ACTIN; CALVASCULIN; CD11B ANTIGEN; CD14 ANTIGEN; CD34 ANTIGEN; CD45 ANTIGEN; CELL MARKER; INTERLEUKIN 6; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; PROCOLLAGEN; STEM CELL FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERY WALL; ARTICLE; CALF (MAMMAL); CELL GROWTH; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CELL STRUCTURE; CONTROLLED STUDY; FIBROBLAST; HYPOXIA; IN VIVO STUDY; MESENCHYME CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PULMONARY ARTERY; PULMONARY HYPERTENSION; SMOOTH MUSCLE FIBER;

ANIMALS; ANOXIA; AUTOCRINE COMMUNICATION; BIOLOGICAL MARKERS; CATTLE; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; CHEMOKINE CXCL12; CULTURE MEDIA; GENE EXPRESSION REGULATION; HYPERTENSION, PULMONARY; INFLAMMATION MEDIATORS; MITOGENS; PARACRINE COMMUNICATION; PHENOTYPE; PLATELET-DERIVED GROWTH FACTOR; PULMONARY ARTERY; RECEPTORS, IMMUNOLOGIC; RNA, MESSENGER; S100 PROTEINS;

EID: 71949097961     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.90611.2008     Document Type: Article

References (81)

1. Arciniegas E, Frid MG, Douglas IS, Stenmark KR. Perspectives on endothelial-to-mesenchymal transition: potential contribution to vascular remodeling in chronic pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol 293: L1-L8, 2007.
2. Asosingh K, Aldred MA, Vasanji A, Drazba J, Sharp J, Farver C, Comhair SA, Xu W, Licina L, Huang L, Anand-Apte B, Yoder MC, Tuder RM, Erzurum SC. Circulating angiogenic precursors in idiopathic pulmonary arterial hypertension. Am J Pathol 172: 615-627, 2008. (Pubitemid 351354535)
3. Ball SG, Shuttleworth CA, Kielty CM. Mesenchymal stem cells and neovascularization: role of platelet-derived growth factor receptors. J Cell Mol Med 11: 1012-1030, 2007.
4. Bellini A, Mattoli S. The role of the fibrocyte, a bone marrow-derived mesenchymal progenitor, in reactive and reparative fibroses. Lab Invest 87: 858-870, 2007. (Pubitemid 47267815)
5. Brisset AC, Hao H, Camenzind E, Bacchetta M, Geinoz A, Sanchez JC, Chaponnier C, Gabbiani G, Bochaton-Piallat ML. Intimal smooth muscle cells of porcine and human coronary artery express S100A4, a marker of the rhomboid phenotype in vitro. Circ Res 100: 1055-1062, 2007.
6. Caplice NM, Bunch TJ, Stalboerger PG, Wang S, Simper D, Miller DV, Russell SJ, Litzow MR, Edwards WD. Smooth muscle cells in human coronary atherosclerosis can originate from cells administered at marrow transplantation. Proc Natl Acad Sci USA 100: 4754-4759, 2003.
7. Ceradini DJ, Kulkarni AR, Callaghan MJ, Tepper OM, Bastidas N, Kleinman ME, Capla JM, Galiano RD, Levine JP, Gurtner GC. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat Med 10: 858-864, 2004. (Pubitemid 39070860)
8. Chang JS, Wendt T, Qu W, Kong L, Zou YS, Schmidt AM, Yan SF. Oxygen deprivation triggers upregulation of early growth response-1 by the receptor for advanced glycation end products. Circ Res 102: 905-913, 2008. (Pubitemid 351591549)
9. Davie NJ, Crossno JT Jr, Frid MG, Hofmeister SE, Reeves JT, Hyde DM, Carpenter TC, Brunetti JA, McNiece IK, Stenmark KR. Hypoxia-induced pulmonary artery adventitial remodeling and neovascularization: contribution of progenitor cells. Am J Physiol Lung Cell Mol Physiol 286: L668-L678, 2004.
10. Dolgachev VA, Ullenbruch MR, Lukacs NW, Phan SH. Role of stem cell factor and bone marrow-derived fibroblasts in airway remodeling. Am J Pathol 174: 390-400, 2009.
11. Donato R. RAGE: a single receptor for several ligands and different cellular responses: the case of certain S100 proteins. Curr Mol Med 7: 711-724, 2007.
12. Eddahibi S, Guignabert C, Barlier-Mur AM, Dewachter L, Fadel E, Dartevelle P, Humbert M, Simonneau G, Hanoun N, Saurini F, Hamon M, Adnot S. Cross talk between endothelial and smooth muscle cells in pulmonary hypertension: critical role for serotonin-induced smooth muscle hyperplasia. Circulation 113: 1857-1864, 2006.
13. Ergun S, Tilki D, Hohn HP, Gehling U, Kilic N. Potential implications of vascular wall resident endothelial progenitor cells. Thromb Haemost 98: 930-939, 2007. (Pubitemid 350091120)
14. Farmer DG, Kennedy S. RAGE, vascular tone and vascular disease. Pharmacol Ther 124: 185-194, 2009.
15. Frid MG, Aldashev AA, Dempsey EC, Stenmark KR. Smooth muscle cells isolated from discrete compartments of the mature vascular media exhibit unique phenotypes and distinct growth capabilities. Circ Res 81: 940-952, 1997.
16. Frid MG, Aldashev AA, Nemenoff RA, Higashito R, Westcott JY, Stenmark KR. Subendothelial cells from normal bovine arteries exhibit autonomous growth and constitutively activated intracellular signaling. Arterioscler Thromb Vasc Biol 19: 2884-2893, 1999. (Pubitemid 30029814)
17. Frid MG, Brunetti JA, Burke DL, Carpenter TC, Davie NJ, Reeves JT, Roedersheimer MT, van Rooijen N, Stenmark KR. Hypoxia-induced pulmonary vascular remodeling requires recruitment of circulating mesenchymal precursors of a monocyte/macrophage lineage. Am J Pathol 168: 659-669, 2006.
18. Frid MG, Moiseeva EP, Stenmark KR. Multiple phenotypically distinct smooth muscle cell populations exist in the adult and developing bovine pulmonary arterial media in vivo. Circ Res 75: 669-681, 1994.
19. Gao XN, Tang SQ, Zhang XF. S100A4 antisense oligodeoxynucleotide suppresses invasive potential of neuroblastoma cells. J Ped Surg 40: 648-652, 2005. (Pubitemid 40504008)
20. Goumans MJ, van Zonneveld AJ, ten Dijke P. Transforming growth factor beta-induced endothelial-to-mesenchymal transition: a switch to cardiac fibrosis? Trends Cardiovasc Med 18: 293-298, 2008.
21. Greenway S, van Suylen RJ, Du Marchie Sarvaas G, Kwan E, Ambartsumian N, Lukanidin E, Rabinovitch M. S100A4/Mts1 produces murine pulmonary artery changes resembling plexogenic arteriopathy and is increased in human plexogenic arteriopathy. Am J Pathol 164: 253-262, 2004.
22. Hall SM, Brogan P, Haworth SG, Klein N. Contribution of inflammation to the pathology of idiopathic pulmonary arterial hypertension in children. Thorax 64: 778-783, 2009.
23. Hassoun PM, Mouthon L, Barbera JA, Eddahibi S, Flores SC, Grimminger F, Jones PL, Maitland ML, Michelakis ED, Morrell NW, Newman JH, Rabinovitch M, Schermuly R, Stenmark KR, Voelkel NF, Yuan JX, Humbert M. Inflammation, growth factors, and pulmonary vascular remodeling. J Am Coll Cardiol 54: S10-S19, 2009.
24. Hayashida K, Fujita J, Miyake Y, Kawada H, Ando K, Ogawa S, Fukuda K. Bone marrow-derived cells contribute to pulmonary vascular remodeling in hypoxia-induced pulmonary hypertension. Chest 127: 1793-1798, 2005. (Pubitemid 46218809)
25. Heizmann CW, Ackermann GE, Galichet A. Pathologies involving the S100 proteins and RAGE. Subcell Biochem 45: 93-138, 2007.
26. Hinz B, Phan SH, Thannickal VJ, Galli A, Bochaton-Piallat ML, Gabbiani G. The myofibroblast: one function, multiple origins. Am J Pathol 170: 1807-1816, 2007.
27. Hiwatashi K, Ueno S, Kubo F, Sakoda M, Tateno T, Hayashi T, Abeyama K, Natsugoe S. Relevance of apoptosis and tolerance to hypoxic stress in cells transfected with receptor for advanced glycation end products (RAGE). Anticancer Res 29: 1287-1294, 2009.
28. Hu Y, Zhang Z, Torsney E, Afzal AR, Davison F, Metzler B, Xu Q. Abundant progenitor cells in the adventitia contribute to atherosclerosis of vein grafts in ApoE-deficient mice. J Clin Invest 113: 1258-1265, 2004. (Pubitemid 39069924)
29. Humbert M, Morrell NW, Archer SL, Stenmark KR, MacLean MR, Lang IM, Christman BW, Weir EK, Eickelberg O, Voelkel NF, Rabinovitch M. Cellular and molecular pathobiology of pulmonary arterial hypertension. J Am Coll Cardiol 43: 13S-24S, 2004.
30. Iyer SS, Rojas M. Anti-inflammatory effects of mesenchymal stem cells: novel concept for future therapies. Expert Opin Biol Ther 8: 569-581, 2008.
31. Jeffery TK, Morrell NW. Molecular and cellular basis of pulmonary vascular remodeling in pulmonary hypertension. Prog Cardiovasc Dis 45: 173-202, 2002. (Pubitemid 36139815)
32. Jones R, Jacobson M, Steudel W. α-Smooth-muscle actin and microvascular precursor smooth-muscle cells in pulmonary hypertension. Am J Respir Cell Mol Biol 20: 582-594, 1999. (Pubitemid 129495646)
33. Jovin TM, Morris SJ, Striker G, Schultens HA, Digweed M, Arndt-Jovin DJ. Automatic sizing and separation of particles by ratios of light scattering intensities. J Histochem Cytochem 24: 269-283, 1976.
34. Kaplan-Albuquerque N, Bogaert YE, Van Putten V, Weiser-Evans MC, Nemenoff RA. Patterns of gene expression differentially regulated by platelet-derived growth factor and hypertrophic stimuli in vascular smooth muscle cells: markers for phenotypic modulation and response to injury. J Biol Chem 280: 19966-19976, 2005. (Pubitemid 41379525)
35. Lantz MS, Ciborowski P. Zymographic techniques for detection and characterization of microbial proteases. Methods Enzymol 235: 563-594, 1994.
36. Lawrie A, Spiekerkoetter E, Martinez EC, Ambartsumian N, Sheward WJ, MacLean MR, Harmar AJ, Schmidt AM, Lukanidin E, Rabinovitch M. Interdependent serotonin transporter and receptor pathways regulate S100A4/Mts1, a gene associated with pulmonary vascular disease. Circ Res 97: 227-235, 2005. (Pubitemid 41105448)
37. Liao SH, Zhao XY, Han YH, Zhang J, Wang LS, Xia L, Zhao KW, Zheng Y, Guo M, Chen GQ. Proteomics-based identification of two novel direct targets of hypoxia-inducible factor-1 and their potential roles in migration/invasion of cancer cells. Proteomics 9: 3901-3912, 2009.
38. Majka SM, Skokan M, Wheeler L, Harral J, Gladson S, Burnham E, Loyd JE, Stenmark KR, Varella-Garcia M, West J. Evidence for cell fusion is absent in vascular lesions associated with pulmonary arterial hypertension. Am J Physiol Lung Cell Mol Physiol 295: L1028-L1039, 2008.
39. 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 293: L548-L554, 2007.
40. Merklinger SL, Wagner RA, Spiekerkoetter E, Hinek A, Knutsen RH, Kabir MG, Desai K, Hacker S, Wang L, Cann GM, Ambartsumian NS, Lukanidin E, Bernstein D, Husain M, Mecham RP, Starcher B, Yanagisawa H, Rabinovitch M. Increased fibulin-5 and elastin in S100A4/Mts1 mice with pulmonary hypertension. Circ Res 97: 596-604, 2005.
41. Metharom P, Caplice NM. Vascular disease: a new progenitor biology. Curr Vasc Pharmacol 5: 61-68, 2007.
42. Morrell NW, Adnot S, Archer SL, Dupuis J, Jones PL, MacLean MR, McMurtry IF, Stenmark KR, Thistlethwaite PA, Weissmann N, Yuan JX, Weir EK. Cellular and molecular basis of pulmonary arterial hypertension. J Am Coll Cardiol 54: S20-S31, 2009.
43. Mourani PM, Garl PJ, Wenzlau JM, Carpenter TC, Stenmark KR, Weiser-Evans MC. Unique, highly proliferative growth phenotype expressed by embryonic and neointimal smooth muscle cells is driven by constitutive Akt, mTOR, and p70S6K signaling and is actively repressed by PTEN. Circulation 109: 1299-1306, 2004.
44. Nemenoff RA, Simpson PA, Furgeson SB, Kaplan-Albuquerque N, Crossno J, Garl PJ, Cooper J, Weiser-Evans MC. Targeted deletion of PTEN in smooth muscle cells results in vascular remodeling and recruitment of progenitor cells through induction of stromal cell-derived factor-1alpha. Circ Res 102: 1036-1045, 2008. (Pubitemid 351667857)
45. Oslejskova L, Grigorian M, Gay S, Neidhart M, Senolt L. The metastasis associated protein S100A4: a potential novel link to inflammation and consequent aggressive behaviour of rheumatoid arthritis synovial fibroblasts. Ann Rheumatic Dis 67: 1499-1504, 2008.
46. Ostman A. PDGF receptors-mediators of autocrine tumor growth and regulators of tumor vasculature and stroma. Cytokine Growth Factor Rev 15: 275-286, 2004. (Pubitemid 38781051)
47. Passman JN, Dong XR, Wu SP, Maguire CT, Hogan KA, Bautch VL, Majesky MW. A sonic hedgehog signaling domain in the arterial adventitia supports resident Sca1 smooth muscle progenitor cells. Proc Natl Acad Sci USA 105: 9349-9354, 2008.
48. Peinado VI, Pizarro S, Barbera JA. Pulmonary vascular involvement in COPD. Chest 134: 808-814, 2008.
49. Peinado VI, Ramirez J, Roca J, Rodriguez-Roisin R, Barbera JA. Identification of vascular progenitor cells in pulmonary arteries of patients with chronic obstructive pulmonary disease. Am J Respir Cell Mol Biol 34: 257-263, 2006. (Pubitemid 43320706)
50. Prockop DJ. "Stemness" does not explain the repair of many tissues by mesenchymal stem/multipotent stromal cells (MSCs). Clin Pharmacol Ther 82: 241-243, 2007.
51. Quan TE, Cowper SE, Bucala R. The role of circulating fibrocytes in fibrosis. Curr Rheumatol Rep 8: 145-150, 2006.
52. Ross JJ, Hong Z, Willenbring B, Zeng L, Isenberg B, Lee EH, Reyes M, Keirstead SA, Weir EK, Tranquillo RT, Verfaillie CM. Cytokine-induced differentiation of multipotent adult progenitor cells into functional smooth muscle cells. J Clin Invest 116: 3139-3149, 2006.
53. Rozen S, Skaletsky H. Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132: 365-386, 2000.
54. Saleem M, Kweon MH, Johnson JJ, Adhami VM, Elcheva I, Khan N, Bin Hafeez B, Bhat KM, Sarfaraz S, Reagan-Shaw S, Spiegelman VS, Setaluri V, Mukhtar H. S100A4 accelerates tumorigenesis and invasion of human prostate cancer through the transcriptional regulation of matrix metalloproteinase 9. Proc Natl Acad Sci USA 103: 14825-14830, 2006.
55. Samolov B, Steen B, Seregard S, van der Ploeg I, Montan P, Kvanta A. Delayed inflammation-associated corneal neovascularization in MMP-2-deficient mice. Exp Eye Res 80: 159-166, 2005.
56. Sartore S, Chiavegato A, Faggin E, Franch R, Puato M, Ausoni S, Pauletto P. Contribution of adventitial fibroblasts to neointima formation and vascular remodeling: from innocent bystander to active participant. Circ Res 89: 1111-1121, 2001.
57. Sata M, Saiura A, Kunisato A, Tojo A, Okada S, Tokuhisa T, Hirai H, Makuuchi M, Hirata Y, Nagai R. Hematopoietic stem cells differentiate into vascular cells that participate in the pathogenesis of atherosclerosis. Nat Med 8: 403-409, 2002.
58. 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. Cardiovas Res 81: 226-234, 2009.
59. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nature Protocols 3: 1101-1108, 2008. (Pubitemid 351818697)
60. Shi Y, O'Brien JE Jr, Ala-Kokko L, Chung W, Mannion JD, Zalewski A. Origin of extracellular matrix synthesis during coronary repair. Circulation 95: 997-1006, 1997. (Pubitemid 27091546)
61. Shimizu K, Sugiyama S, Aikawa M, Fukumoto Y, Rabkin E, Libby P, Mitchell RN. Host bone-marrow cells are a source of donor intimal smooth-muscle-like cells in murine aortic transplant arteriopathy. Nat Med 7: 738-741, 2001. (Pubitemid 32588032)
62. Sobin SS, Tremer HM, Hardy JD, Chiodi HP. Changes in arteriole in acute and chronic hypoxic pulmonary hypertension and recovery in rat. J Appl Physiol 55: 1445-1455, 1983.
63. Spees JL, Whitney MJ, Sullivan DE, Lasky JA, Laboy M, Ylostalo J, Prockop DJ. Bone marrow progenitor cells contribute to repair and remodeling of the lung and heart in a rat model of progressive pulmonary hypertension. FASEB J 22: 1226-1236, 2008.
64. Stenmark KR, Fagan KA, Frid MG. Hypoxia-induced pulmonary vascular remodeling: cellular and molecular mechanisms. Circ Res 99: 675-691, 2006. (Pubitemid 44498302)
65. Stenmark KR, Fasules J, Hyde DM, Voelkel NF, Henson J, Tucker A, Wilson H, Reeves JT. Severe pulmonary hypertension and arterial adventitial changes in newborn calves at 4,300 m. J Appl Physiol 62: 821-830, 1987.
66. Stenmark KR, Orton EC, Reeves JT, Voelkel NF, Crouch EC, Parks WC, Mecham RP. Vascular remodeling in neonatal pulmonary hypertension. Role of the smooth muscle cell. Chest 93: 127S-133S, 1988.
67. Stiebellehner L, Frid MG, Reeves JT, Low RB, Gnanasekharan M, Stenmark KR. Bovine distal pulmonary arterial media is composed of a uniform population of well-differentiated smooth muscle cells with low proliferative capabilities. Am J Physiol Lung Cell Mol Physiol 285: L819-L828, 2003.
68. Strieter RM, Keeley EC, Hughes MA, Burdick MD, Mehrad B. The role of circulating mesenchymal progenitor cells (fibrocytes) in the pathogenesis of pulmonary fibrosis. J Leukocyte Biol. In press.
69. Takenaga K, Kozlova EN. Role of intracellular S100A4 for migration of rat astrocytes. Glia 53: 313-321, 2006.
70. Tanaka K, Sata M, Hirata Y, Nagai R. Diverse contribution of bone marrow cells to neointimal hyperplasia after mechanical vascular injuries. Circ Res 93: 783-790, 2003. (Pubitemid 37288674)
71. Tarabykina S, Griffiths TR, Tulchinsky E, Mellon JK, Bronstein IB, Kriajevska M. Metastasis-associated protein S100A4: spotlight on its role in cell migration. Curr Cancer Drug Targets 7: 217-228, 2007. (Pubitemid 46699073)
72. Tolboom TC, Huizinga TW. In vitro matrigel fibroblast invasion assay. Methods Mol Med 135: 413-421, 2007.
73. Tuder RM, Marecki JC, Richter A, Fijalkowska I, Flores S. Pathology of pulmonary hypertension. Clin Chest Med 28: 23-42, 2007.
74. Tuder RM, Yun JH, Bhunia A, Fijalkowska I. Hypoxia and chronic lung disease. J Mol Med 85: 1317-1324, 2007.
75. Varcoe RL, Mikhail M, Guiffre AK, Pennings G, Vicaretti M, Hawthorne WJ, Fletcher JP, Medbury HJ. The role of the fibrocyte in intimal hyperplasia. J Thromb Haemost 4: 1125-1133, 2006.
76. Weiser-Evans MC, Quinn BE, Burkard MR, Stenmark KR. Transient reexpression of an embryonic autonomous growth phenotype by adult carotid artery smooth muscle cells after vascular injury. J Cell Physiol 182: 12-23, 2000.
77. Weiser-Evans MC, Schwartz PE, Grieshaber NA, Quinn BE, Grieshaber SS, Belknap JK, Mourani PM, Majack RA, Stenmark KR. Novel embryonic genes are preferentially expressed by autonomously replicating rat embryonic and neointimal smooth muscle cells. Circ Res 87: 608-615, 2000.
78. Xaymardan M, Cimini M, Fazel S, Weisel RD, Lu WY, Martin U, Harvey RP, Li RK. c-Kit function is necessary for in vitro myogenic differentiation of bone marrow hematopoietic cells. Stem Cells 27: 1911-1920, 2009.
79. Young KC, Torres E, Hatzistergos KE, Hehre D, Suguihara C, Hare JM. Inhibition of the SDF-1/CXCR4 axis attenuates neonatal hypoxia-induced pulmonary hypertension. Circ Res 104: 1293-1301, 2009.
80. Zalewski A, Shi Y. Vascular myofibroblasts. Lessons from coronary repair and remodeling. Arterioscler Thromb Vasc Biol 17: 417-422, 1997. (Pubitemid 27133129)
81. Zengin E, Chalajour F, Gehling UM, Ito WD, Treede H, Lauke H, Weil J, Reichenspurner H, Kilic N, Ergun S. Vascular wall resident progenitor cells: a source for postnatal vasculogenesis. Development 133: 1543-1551, 2006. (Pubitemid 43732967)