Bone marrow-derived angiogenic cells restore lung alveolar and vascular structure after neonatal hyperoxia in infant mice

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 298, Issue 3, 2010, Pages

  Balasubramaniam, Vivek ^a   Ryan, Sharon L ^a   Seedorf, Gregory J ^a   Roth, Emily V ^a   Heumann, Thatcher R ^a   Yoder, Mervin C ^b   Ingram, David A ^b   Hogan, Christopher J ^a   Markham, Neil E ^a   Abman, Steven H ^a  

^a CHILDREN S HOSPITAL COLORADO   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Alveolar type 2 cell; Bronchopulmonary dysplasia; Endothelial cell; Oxygen; Stem cell

Indexed keywords

ANGIOPOIETIN RECEPTOR; GREEN FLUORESCENT PROTEIN; OXYGEN;

AMBIENT AIR; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BONE MARROW CELL; CELL GROWTH; CELL POPULATION; COCULTURE; CONTROLLED STUDY; HYPEROXIA; IN VITRO STUDY; LUNG ALVEOLUS; LUNG ALVEOLUS CELL; LUNG BLOOD VESSEL; LUNG CIRCULATION; LUNG STRUCTURE; MOUSE; MYELOID PROGENITOR CELL; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; ANIMALS, NEWBORN; BONE MARROW CELLS; CELL PROLIFERATION; COLONY-FORMING UNITS ASSAY; ENDOTHELIAL CELLS; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; HYPEROXIA; MICE; NEOVASCULARIZATION, PHYSIOLOGIC; PHENOTYPE; PULMONARY ALVEOLI; TIME FACTORS;

EID: 77249157301     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00089.2009     Document Type: Article

References (68)

1. Abe S, Boyer C, Liu X, Wen FQ, Kobayashi T, Fang Q, Wang X, Hashimoto M, Sharp JG, Rennard SI. Cells derived from the circulation contribute to the repair of lung injury. Am J Respir Crit Care Med 170: 1158-1163, 2004.
2. Abman S. Pulmonary hypertension in chronic lung disease of infancy: pathogenesis, pathophysiology, and treatment. In: Chronic Lung Disease in Early Infancy, edited by Bland RD and Coalson JJ. New York: Dekker, 1999, p. 619-668.
3. Anghelina M, Krishnan P, Moldovan L, Moldovan NI. Monocytes/macrophages cooperate with progenitor cells during neovascularization and tissue repair: conversion of cell columns into fibrovascular bundles. Am J Pathol 168: 529-541, 2006.
4. Asahara T, Masuda H, Takahashi T, Kalka C, Pastore C, Silver M, Kearne M, Magner M, Isner JM. Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res 85: 221-228, 1999.
5. Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, Witzenbichler B, Schatteman G, Isner JM. Isolation of putative progenitor endothelial cells for angiogenesis. Science 275: 964-967, 1997.
6. Balasubramaniam V, Le Cras TD, Ivy DD, Grover TR, Kinsella JP, Abman SH. Role of platelet-derived growth factor in vascular remodeling during pulmonary hypertension in the ovine fetus. Am J Physiol Lung Cell Mol Physiol 284: L826-L833, 2003.
7. Balasubramaniam V, Maxey AM, Morgan DB, Markham NE, Abman SH. Inhaled NO restores lung structure in eNOS deficient mice recovering from neonatal hypoxia. Am J Physiol Lung Cell Mol Physiol 291: L119-L127, 2006.
8. Balasubramaniam V, Mervis CF, Maxey AM, Markham NE, Abman SH. Hyperoxia reduces bone marrow, circulating, and lung endothelial progenitor cells in the developing lung: implications for the pathogenesis of bronchopulmonary dysplasia. Am J Physiol Lung Cell Mol Physiol 292: L1073-L1084, 2007.
9. Balasubramaniam V, Tang JR, Maxey A, Plopper CG, Abman SH. Mild hypoxia impairs alveolarization in the endothelial nitric oxide synthase-deficient mouse. Am J Physiol Lung Cell Mol Physiol 284: L964-L971, 2003.
10. Bronte V, Apolloni E, Cabrelle A, Ronca R, Serafini P, Zamboni P, Restifo NP, Zanovello P. Identification of a CD11b(+)/Gr-1(+)/CD31(+) myeloid progenitor capable of activating or suppressing CD8(+) T cells. Blood 96: 3838-3846, 2000.
11. Cantor JO, Keller S, Cerreta JM, Manahan J, Evans HE, Turino GM. The effect of 60% oxygen on air-space enlargement and cross-linked elastin synthesis in hamsters with elastase-induced emphysema. Am Rev Respir Dis 142: 668-673, 1990.
12. Chang JC, Summer R, Sun X, Fitzsimmons K, Fine A. Evidence that bone marrow cells do not contribute to the alveolar epithelium. Am J Respir Cell Mol Biol 33: 335-342, 2005.
13. Coalson JJ. Pathology of chronic lung disease of early infancy. In: Chronic Lung Disease in Early Infancy, edited by Bland RD and Coalson JJ. New York: Dekker, 1999, p. 85-124.
14. Cooney TP, Thurlbeck WM. The radial alveolar count method of Emery and Mithal: a reappraisal 2-intrauterine and early postnatal lung growth. Thorax 37: 580-583, 1982.
15. Dauger S, Ferkdadji L, Saumon G, Vardon G, Peuchmaur M, Gaultier C, Gallego J. Neonatal exposure to 65% oxygen durably impairs lung architecture and breathing pattern in adult mice. Chest 123: 530-538, 2003.
16. De Palma M, Venneri MA, Galli R, Sergi Sergi L, Politi LS, Sampaolesi M, Naldini L. Tie2 identifies a hematopoietic lineage of proangiogenic monocytes required for tumor vessel formation and a mesenchymal population of pericyte progenitors. Cancer Cell 8: 211-226, 2005.
17. Dong QG, Bernasconi S, Lostaglio S, De Calmanovici RW, Martin-Padura I, Breviario F, Garlanda C, Ramponi S, Mantovani A, Vecchi A. A general strategy for isolation of endothelial cells from murine tissues. Characterization of two endothelial cell lines from the murine lung and subcutaneous sponge implants. Arterioscler Thromb Vasc Biol 17: 1599-1604, 1997.
18. Frank L. Developmental aspects of experimental pulmonary oxygen toxicity. Free Radic Biol Med 11: 463-494, 1991.
19. Frank L. Hyperoxic inhibition of newborn rat lung development: protection by deferoxamine. Free Radic Biol Med 11: 341-348, 1991.
20. Frank L, Bucher JR, Roberts RJ. Oxygen toxicity in neonatal and adult animals of various species. J Appl Physiol 45: 699-704, 1978.
21. Giangreco A, Reynolds SD, Stripp BR. Terminal bronchioles harbor a unique airway stem cell population that localizes to the bronchoalveolar duct junction. Am J Pathol 161: 173-182, 2002.
22. Gordon S, Taylor PR. Monocyte and macrophage heterogeneity. Nat Rev Immunol 5: 953-964, 2005.
23. Han RN, Buch S, Tseu I, Young J, Christie NA, Frndova H, Lye SJ, Post M, Tanswell AK. Changes in structure, mechanics, and insulin-like growth factor-related gene expression in the lungs of newborn rats exposed to air or 60% oxygen. Pediatr Res 39: 921-929, 1996.
24. Harris RG, Herzog EL, Bruscia EM, Grove JE, Van Arnam JS, Krause DS. Lack of a fusion requirement for development of bone marrow-derived epithelia. Science 305: 90-93, 2004.
25. Hatzopoulos AK, Folkman J, Vasile E, Eiselen GK, Rosenberg RD. Isolation and characterization of endothelial progenitor cells from mouse embryos. Development 125: 1457-1468, 1998.
26. Hong KU, Reynolds SD, Giangreco A, Hurley CM, Stripp BR. Clara cell secretory protein-expressing cells of the airway neuroepithelial body microenvironment include a label-retaining subset and are critical for epithelial renewal after progenitor cell depletion. Am J Respir Cell Mol Biol 24: 671-681, 2001.
27. Hong KU, Reynolds SD, Watkins S, Fuchs E, Stripp BR. Basal cells are a multipotent progenitor capable of renewing the bronchial epithelium. Am J Pathol 164: 577-588, 2004.
28. Husain AN, Siddiqui NH, Stocker JT. Pathology of arrested acinar development in postsurfactant bronchopulmonary dysplasia. Hum Pathol 29: 710-717, 1998.
29. Jackson L, Jones DR, Scotting P, Sottile V. Adult mesenchymal stem cells: differentiation potential and therapeutic applications. J Postgrad Med 53: 121-127, 2007.
30. Jakkula M, Le Cras TD, Gebb S, Hirth KP, Tuder RM, Voelkel NF, Abman SH. Inhibition of angiogenesis decreases alveolarization in the developing rat lung. Am J Physiol Lung Cell Mol Physiol 279: L600-L607, 2000.
31. Jobe AH. The new BPD: an arrest of lung development. Pediatr Res 46: 641-643, 1999.
32. Jobe AH, Bancalari E. Bronchopulmonary dysplasia. Am J Respir Crit Care Med 163: 1723-1729, 2001.
33. Kalka C, Tehrani H, Laudenberg B, Vale PR, Isner JM, Asahara T, Symes JF. VEGF gene transfer mobilizes endothelial progenitor cells in patients with inoperable coronary disease. Ann Thorac Surg 70: 829-834, 2000.
34. Kocher AA, Schuster MD, Szabolcs MJ, Takuma S, Burkhoff D, Wang J, Homma S, Edwards NM, Itescu S. Neovascularization of ischemic myocardium by human bone-marrow-derived angioblasts prevents cardiomyocyte apoptosis, reduces remodeling and improves cardiac function. Nat Med 7: 430-436, 2001.
35. Kotton DN, Fabian AJ, Mulligan RC. Failure of bone marrow to reconstitute lung epithelium. Am J Respir Cell Mol Biol 33: 328-334, 2005.
36. Krause DS, Theise ND, Collector MI, Henegariu O, Hwang S, Gardner R, Neutzel S, Sharkis SJ. Multi-organ, multi-lineage engraftment by a single bone marrow-derived stem cell. Cell 105: 369-377, 2001.
37. Kunig AM, Balasubramaniam V, Markham NE, Morgan D, Montgomery G, Grover TR, Abman SH. Recombinant human VEGF treatment enhances alveolarization after hyperoxic lung injury in neonatal rats. Am J Physiol Lung Cell Mol Physiol 289: L529-L535, 2005.
38. Kunig AM, Balasubramaniam V, Markham NE, Seedorf G, Gien J, Abman SH. Recombinant human VEGF treatment transiently increases lung edema but enhances lung structure after neonatal hyperoxia. Am J Physiol Lung Cell Mol Physiol 291: L1068-L1078, 2006.
39. Le Cras TD, Markham NE, Tuder RM, Voelkel NF, Abman SH. Treatment of newborn rats with a VEGF receptor inhibitor causes pulmonary hypertension and abnormal lung structure. Am J Physiol Lung Cell Mol Physiol 283: L555-L562, 2002.
40. Lin YJ, Markham NE, Balasubramaniam V, Tang JR, Maxey A, Kinsella JP, Abman SH. Inhaled nitric oxide enhances distal lung growth after exposure to hyperoxia in neonatal rats. Pediatr Res 58: 22-29, 2005.
41. Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, Locati M. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol 25: 677-686, 2004.
42. Mason RJ, Williams MC. Type II alveolar cell. Defender of the alveolus. Am Rev Respir Dis 115: 81-91, 1977.
43. Massaro GD, Olivier J, Massaro D. Short-term perinatal 10% O2 alters postnatal development of lung alveoli. Am J Physiol Lung Cell Mol Physiol 257: L221-L225, 1989.
44. Northway WH Jr, Rosan RC, Porter DY. Pulmonary disease following respirator therapy of hyaline-membrane disease. Bronchopulmonary dysplasia. N Engl J Med 276: 357-368, 1967.
45. Peake JL, Reynolds SD, Stripp BR, Stephens KE, Pinkerton KE. Alteration of pulmonary neuroendocrine cells during epithelial repair of naphthalene-induced airway injury. Am J Pathol 156: 279-286, 2000.
46. Reynolds SD, Giangreco A, Power JH, Stripp BR. Neuroepithelial bodies of pulmonary airways serve as a reservoir of progenitor cells capable of epithelial regeneration. Am J Pathol 156: 269-278, 2000.
47. Roberts RJ, Weesner KM, Bucher JR. Oxygen-induced alterations in lung vascular development in the newborn rat. Pediatr Res 17: 368-375, 1983.
48. Shaffer SG, O'Neill D, Bradt SK, Thibeault DW. Chronic vascular pulmonary dysplasia associated with neonatal hyperoxia exposure in the rat. Pediatr Res 21: 14-20, 1987.
49. Sica A, Schioppa T, Mantovani A, Allavena P. Tumour-associated macrophages are a distinct M2 polarised population promoting tumour progression: potential targets of anti-cancer therapy. Eur J Cancer 42: 717-727, 2006.
50. Sobonya RE, Logvinoff MM, Taussig LM, Theriault A. Morphometric analysis of the lung in prolonged bronchopulmonary dysplasia. Pediatr Res 16: 969-972, 1982.
51. Stocker JT. Pathologic features of long-standing "healed" bronchopulmonary dysplasia: a study of 28 3- to 40-month-old infants. Hum Pathol 17: 943-961, 1986.
52. Tang, Jr, Le Cras TD, Morris KG Jr, Abman SH. Brief perinatal hypoxia increases severity of pulmonary hypertension after reexposure to hypoxia in infant rats. Am J Physiol Lung Cell Mol Physiol 278: L356-L364, 2000.
53. Tang Y, Yasuhara T, Hara K, Matsukawa N, Maki M, Yu G, Xu L, Hess DC, Borlongan CV. Transplantation of bone marrow-derived stem cells: a promising therapy for stroke. Cell Transplant 16: 159-169, 2007.
54. Uhal BD. Cell cycle kinetics in the alveolar epithelium. Am J Physiol Lung Cell Mol Physiol 272: L1031-L1045, 1997.
55. Van Ginderachter JA, Meerschaut S, Liu Y, Brys L, De Groeve K, Hassanzadeh Ghassabeh G, Raes G, De Baetselier P. Peroxisome proliferator-activated receptor gamma (PPARgamma) ligands reverse CTL suppression by alternatively activated (M2) macrophages in cancer. Blood 108: 525-535, 2006.
56. Van Ginderachter JA, Movahedi K, Hassanzadeh Ghassabeh G, Meerschaut S, Beschin A, Raes G, De Baetselier P. Classical and alternative activation of mononuclear phagocytes: picking the best of both worlds for tumor promotion. Immunobiology 211: 487-501, 2006.
57. Venneri MA, De Palma M, Ponzoni M, Pucci F, Scielzo C, Zonari E, Mazzieri R, Doglioni C, Naldini L. Identification of proangiogenic TIE2-expressing monocytes (TEMs) in human peripheral blood and cancer. Blood 109: 5276-5285, 2007.
58. Wagers AJ, Sherwood RI, Christensen JL, Weissman IL. Little evidence for developmental plasticity of adult hematopoietic stem cells. Science 297: 2256-2259, 2002.
59. Wang X, Willenbring H, Akkari Y, Torimaru Y, Foster M, Al-Dhalimy M, Lagasse E, Finegold M, Olson S, Grompe M. Cell fusion is the principal source of bone-marrow-derived hepatocytes. Nature 422: 897-901, 2003.
60. Wang XJ, Li QP. The roles of mesenchymal stem cells (MSCs) therapy in ischemic heart diseases. Biochem Biophys Res Commun 359: 189-193, 2007.
61. Warner BB, Stuart LA, Papes RA, Wispe JR. Functional and pathological effects of prolonged hyperoxia in neonatal mice. Am J Physiol Lung Cell Mol Physiol 275: L110-L117, 1998.
62. Wilborn AM, Evers LB, Canada AT. Oxygen toxicity to the developing lung of the mouse: role of reactive oxygen species. Pediatr Res 40: 225-232, 1996.
63. Wilson WL, Mullen M, Olley PM, Rabinovitch M. Hyperoxia-induced pulmonary vascular and lung abnormalities in young rats and potential for recovery. Pediatr Res 19: 1059-1067, 1985.
64. Xu F, Fok TF, Yin J. Hyperoxia-induced lung injury in premature rat: description of a suitable model for the study of lung diseases in newborns. Chin Med J (Engl) 111: 619-624, 1998.
65. Yam J, Frank L, Roberts RJ. Oxygen toxicity: comparison of lung biochemical responses in neonatal and adult rats. Pediatr Res 12: 115-119, 1978.
66. Yamada M, Kubo H, Kobayashi S, Ishizawa K, Numasaki M, Ueda S, Suzuki T, Sasaki H. Bone marrow-derived progenitor cells are important for lung repair after lipopolysaccharide-induced lung injury. J Immunol 172: 1266-1272, 2004.
67. 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 109: 1801-1809, 2007.
68. Zhang ZG, Zhang L, Jiang Q, Chopp M. Bone marrow-derived endothelial progenitor cells participate in cerebral neovascularization after focal cerebral ischemia in the adult mouse. Circ Res 90: 284 -288, 2002