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Published in: Surgery Today 2/2014

01-02-2014 | Original Article

Increase of bone morphogenetic protein-7 expressing pulmonary resident cells in pneumonectomized rats

Authors: Taro Ohba, Hironobu Wada, Ichiro Yoshino, Shigetoshi Yoshida, Tetsuzo Tagawa, Fumihiro Shoji, Koji Yamazaki, Yoshihiko Maehara

Published in: Surgery Today | Issue 2/2014

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Abstract

Purpose

Compensatory lung growth (CLG) is recognized in rodents subjected to major pulmonary resection; however, the source of cells constituting regenerated tissues during the CLG is still unknown. We investigated the differentiation of lung resident cells and the participation of bone marrow (BM)-derived cells in the remnant lung of pneumonectomized rats.

Methods

After left pneumonectomy, the right remnant lung of Wistar rats was subjected to morphologic and molecular experiments at several time points. We studied the expression of bone morphogenic protein 7 (BMP-7), an accelerator of epithelial differentiation, based on the gene expression profile data of the remnant lung. Next, we evaluated the presence of GFP-positive cells in the remnant lung of Wistar rats that had received BM transplantation from green fluorescent protein (GFP) gene-transgenic Wistar rats prior to left pneumonectomy.

Results

We observed progression of emphysematous change, modulation of gene expression profile, and proliferating cellular nuclear antigen-positive cells in the alveoli of the remnant lungs. BMP-7 protein positive cells were detected in the alveolar septa, which increased significantly over time with the progression of emphysematous change. No bone marrow-derived cells were detected in the right remnant lung of the GFP-BM transferred rats by fluorescence microscopy, immunohistochemistry, or polymerase chain reaction at any time.

Conclusion

Lung resident cells appear to contribute to CLG, possibly via a trans-differentiation pathway.
Literature
1.
go back to reference Brown LM, Rannels SR, Rannels DE. Implications of post-pneumonectomy compensatory lung growth in pulmonary physiology and disease. Respir Res. 2001;2(6):340–7.PubMedCentralPubMedCrossRef Brown LM, Rannels SR, Rannels DE. Implications of post-pneumonectomy compensatory lung growth in pulmonary physiology and disease. Respir Res. 2001;2(6):340–7.PubMedCentralPubMedCrossRef
2.
go back to reference Wada H, Yoshida S, Suzuki H, Sakairi Y, Mizobuchi T, Komura D, et al. Transplantation of type II cells stimulates lung regeneration during compensatory lung growth in adult rats. J Thorac Cardiovasc Surg. 2012;143(3):711–9.PubMedCrossRef Wada H, Yoshida S, Suzuki H, Sakairi Y, Mizobuchi T, Komura D, et al. Transplantation of type II cells stimulates lung regeneration during compensatory lung growth in adult rats. J Thorac Cardiovasc Surg. 2012;143(3):711–9.PubMedCrossRef
3.
4.
go back to reference Wirtz HR, Dobbs LG. The effects of mechanical forces on lung functions. Respir Physiol. 2000;119(1):1–17. Wirtz HR, Dobbs LG. The effects of mechanical forces on lung functions. Respir Physiol. 2000;119(1):1–17.
5.
go back to reference Blau HM, Brazelton TR, Weimann JM. The evolving concept of a stem cell: entity or function? Cell. 2001;105(7):829–41.PubMedCrossRef Blau HM, Brazelton TR, Weimann JM. The evolving concept of a stem cell: entity or function? Cell. 2001;105(7):829–41.PubMedCrossRef
6.
go back to reference Ferrari G, Cusella-De Angelis G, Coletta M, Paolucci E, Stornaiuolo A, Cossu G, et al. Muscle regeneration by bone marrow-derived myogenic progenitors. Science. 1998;279(5356):1528–30.PubMedCrossRef Ferrari G, Cusella-De Angelis G, Coletta M, Paolucci E, Stornaiuolo A, Cossu G, et al. Muscle regeneration by bone marrow-derived myogenic progenitors. Science. 1998;279(5356):1528–30.PubMedCrossRef
7.
go back to reference Orlic D, Kajstura J, Chimenti S, Jakoniuk I, Anderson SM, Li B, et al. Bone marrow cells regenerate infarcted myocardium. Nature. 2001;410(6829):701–5.PubMedCrossRef Orlic D, Kajstura J, Chimenti S, Jakoniuk I, Anderson SM, Li B, et al. Bone marrow cells regenerate infarcted myocardium. Nature. 2001;410(6829):701–5.PubMedCrossRef
8.
go back to reference Lagasse E, Connors H, Al-Dhalimy M, Reitsma M, Dohse M, Osborne L, et al. Purified hematopoietic stem cells can differentiate into hepatocytes in vivo. Nat Med. 2000;6(11):1229–34.PubMedCrossRef Lagasse E, Connors H, Al-Dhalimy M, Reitsma M, Dohse M, Osborne L, et al. Purified hematopoietic stem cells can differentiate into hepatocytes in vivo. Nat Med. 2000;6(11):1229–34.PubMedCrossRef
9.
go back to reference Krause DS, Theise ND, Collector MI, Henegariu O, Hwang S, Gardner R, et al. Multi-organ, multi-lineage engraftment by a single bone marrow-derived stem cell. Cell. 2001;105(3):369–77.PubMedCrossRef Krause DS, Theise ND, Collector MI, Henegariu O, Hwang S, Gardner R, et al. Multi-organ, multi-lineage engraftment by a single bone marrow-derived stem cell. Cell. 2001;105(3):369–77.PubMedCrossRef
10.
go back to reference Kotton DN, Ma BY, Cardoso WV, Sanderson EA, Summer RS, Williams MC, et al. Bone marrow-derived cells as progenitors of lung alveolar epithelium. Development. 2001;128(24):5181–8.PubMed Kotton DN, Ma BY, Cardoso WV, Sanderson EA, Summer RS, Williams MC, et al. Bone marrow-derived cells as progenitors of lung alveolar epithelium. Development. 2001;128(24):5181–8.PubMed
11.
go back to reference Ishizawa K, Kubo H, Yamada M, Kobayashi S, Numasaki M, Ueda S, et al. Bone marrow-derived cells contribute to lung regeneration after elastase-induced pulmonary emphysema. FEBS Lett. 2004;556(13):249–52.PubMedCrossRef Ishizawa K, Kubo H, Yamada M, Kobayashi S, Numasaki M, Ueda S, et al. Bone marrow-derived cells contribute to lung regeneration after elastase-induced pulmonary emphysema. FEBS Lett. 2004;556(13):249–52.PubMedCrossRef
12.
go back to reference Lee JM, Dedhar S, Kalluri R, Thompson EW. The epithelial-mesenchymal transition: new insights in signaling, development, and disease. J Cell Biol. 2006;172(7):973–81.PubMedCrossRef Lee JM, Dedhar S, Kalluri R, Thompson EW. The epithelial-mesenchymal transition: new insights in signaling, development, and disease. J Cell Biol. 2006;172(7):973–81.PubMedCrossRef
13.
14.
go back to reference Kalluri R, Neilson EG. Epithelial-mesenchymal transition and its implications for fibrosis. J Clin Invest. 2003;112(12):1776–84.PubMedCentralPubMed Kalluri R, Neilson EG. Epithelial-mesenchymal transition and its implications for fibrosis. J Clin Invest. 2003;112(12):1776–84.PubMedCentralPubMed
15.
go back to reference Thiery JP. Epithelial-mesenchymal transitions in tumour progression. Nature Rev Cancer. 2002;2(6):442–54.CrossRef Thiery JP. Epithelial-mesenchymal transitions in tumour progression. Nature Rev Cancer. 2002;2(6):442–54.CrossRef
16.
go back to reference Zeisberg M, Shah AA, Kalluri R. Bone morphogenic protein-7 induces mesenchymal to epithelial transition in adult renal fibroblasts and facilitates regeneration of injured kidney. J Biol Chem. 2005;280(9):8094–100.PubMedCrossRef Zeisberg M, Shah AA, Kalluri R. Bone morphogenic protein-7 induces mesenchymal to epithelial transition in adult renal fibroblasts and facilitates regeneration of injured kidney. J Biol Chem. 2005;280(9):8094–100.PubMedCrossRef
17.
go back to reference Izumi N, Mizuguchi S, Inagaki Y, Saika S, Kawada N, Nakajima Y, et al. BMP-7 opposes TGF-beta1-mediated collagen induction in mouse pulmonary myofibroblasts through Id2. Am J Physiol Lung Cell Mol Physiol. 2006;290(1):L120–6.PubMedCrossRef Izumi N, Mizuguchi S, Inagaki Y, Saika S, Kawada N, Nakajima Y, et al. BMP-7 opposes TGF-beta1-mediated collagen induction in mouse pulmonary myofibroblasts through Id2. Am J Physiol Lung Cell Mol Physiol. 2006;290(1):L120–6.PubMedCrossRef
18.
go back to reference Myllarniemi M, Lindholm P, Ryynanen MJ, Kliment CR, Salmenkivi K, Keski-Oja J, et al. Gremlin-mediated decrease in bone morphogenic protein signaling promotes pulmonary fibrosis. Am J Respir Crit Care Med. 2008;177(3):321–9.PubMedCrossRef Myllarniemi M, Lindholm P, Ryynanen MJ, Kliment CR, Salmenkivi K, Keski-Oja J, et al. Gremlin-mediated decrease in bone morphogenic protein signaling promotes pulmonary fibrosis. Am J Respir Crit Care Med. 2008;177(3):321–9.PubMedCrossRef
19.
go back to reference Frenckner B, Freyschuss U. Pulmonary function after lobectomy for congenital lobar emphysema and congenital cystic adenomatoid malformation. A follow-up study. Scand J Thorac Cardiovasc Surg. 1982;16(3):293–8.PubMedCrossRef Frenckner B, Freyschuss U. Pulmonary function after lobectomy for congenital lobar emphysema and congenital cystic adenomatoid malformation. A follow-up study. Scand J Thorac Cardiovasc Surg. 1982;16(3):293–8.PubMedCrossRef
20.
go back to reference Nakajima C, Kijimoto C, Yokoyama Y, Miyakawa T, Tsuchiya Y, Kuroda T, et al. Longitudinal follow-up of pulmonary function after lobectomy in childhood—factors affecting lung growth. Pediatr Surg Int. 1998;13(5–6):341–5.PubMedCrossRef Nakajima C, Kijimoto C, Yokoyama Y, Miyakawa T, Tsuchiya Y, Kuroda T, et al. Longitudinal follow-up of pulmonary function after lobectomy in childhood—factors affecting lung growth. Pediatr Surg Int. 1998;13(5–6):341–5.PubMedCrossRef
21.
go back to reference McBride JT, Wohl ME, Strieder DJ, Jackson AC, Morton JR, Zwerdling RG, et al. Lung growth and airway function after lobectomy in infancy for congenital lobar emphysema. J Clin Invest. 1980;66(5):962–70.PubMedCentralPubMedCrossRef McBride JT, Wohl ME, Strieder DJ, Jackson AC, Morton JR, Zwerdling RG, et al. Lung growth and airway function after lobectomy in infancy for congenital lobar emphysema. J Clin Invest. 1980;66(5):962–70.PubMedCentralPubMedCrossRef
22.
go back to reference McAnulty RJ, Staple LH, Guerreiro D, Laurent GJ. Extensive changes in ccollagen synthesis and degradation during compensatory lung growth. Am J Physiol. 1988; 255(6Pt1): C754–9. McAnulty RJ, Staple LH, Guerreiro D, Laurent GJ. Extensive changes in ccollagen synthesis and degradation during compensatory lung growth. Am J Physiol. 1988; 255(6Pt1): C754–9.
23.
go back to reference Koh DW, Roby JD, Starcher B, Senior RM, Pierce RA. Postpneumonectomy lung growth: a model of reinitiation of tropoelastin and type I collagen production in a normal pattern in adult rat lung. Am J Respir Cell Mol Biol. 1996;15(5):611–23.PubMedCrossRef Koh DW, Roby JD, Starcher B, Senior RM, Pierce RA. Postpneumonectomy lung growth: a model of reinitiation of tropoelastin and type I collagen production in a normal pattern in adult rat lung. Am J Respir Cell Mol Biol. 1996;15(5):611–23.PubMedCrossRef
24.
go back to reference Tronc F, Gregoire J, Leblanc P, Deslauriers J. Physiologic consequences of pneumonectomy. Consequences on the pulmonary function. Chest Surg Clin N Am. 1999;9(2):459–73, xii–xiii. Tronc F, Gregoire J, Leblanc P, Deslauriers J. Physiologic consequences of pneumonectomy. Consequences on the pulmonary function. Chest Surg Clin N Am. 1999;9(2):459–73, xii–xiii.
25.
go back to reference Edwards YS. Stretch stimulation: its effects on alveolar type II cell function in the lung. Comp Biochem Physiol A: Mol Integr Physiol. 2001;129(1):245–60.CrossRef Edwards YS. Stretch stimulation: its effects on alveolar type II cell function in the lung. Comp Biochem Physiol A: Mol Integr Physiol. 2001;129(1):245–60.CrossRef
26.
go back to reference Sanchez-Esteban J, Wang Y, Gruppuso PA, Rubin LP. Mechanical stretch induces fetal type II cell differentiation via an epidermal growth factor receptor-extracellular-regulated protein kinase signaling pathway. Am J Res Cell Mol Biol. 2004;30(1):76–83.CrossRef Sanchez-Esteban J, Wang Y, Gruppuso PA, Rubin LP. Mechanical stretch induces fetal type II cell differentiation via an epidermal growth factor receptor-extracellular-regulated protein kinase signaling pathway. Am J Res Cell Mol Biol. 2004;30(1):76–83.CrossRef
27.
go back to reference Sakamaki Y, Matsumoto K, Mizuno S, Miyoshi S, Matsuda H, Nakamura T. Hepatocyte growth factor stimulates proliferation of respiratory epithelial cells during postpneumonectomy compensatory lung growth in mice. Am J Res Cell Mol Biol. 2002;26(5):525–33.CrossRef Sakamaki Y, Matsumoto K, Mizuno S, Miyoshi S, Matsuda H, Nakamura T. Hepatocyte growth factor stimulates proliferation of respiratory epithelial cells during postpneumonectomy compensatory lung growth in mice. Am J Res Cell Mol Biol. 2002;26(5):525–33.CrossRef
28.
go back to reference Massaro D, Massaro GD. Invited Review: pulmonary alveoli: formation, the “call for oxygen”, and other regulators. Am J Physiol Lung Cell Mol Physiol. 2002;282(3):L345–58.PubMed Massaro D, Massaro GD. Invited Review: pulmonary alveoli: formation, the “call for oxygen”, and other regulators. Am J Physiol Lung Cell Mol Physiol. 2002;282(3):L345–58.PubMed
29.
30.
go back to reference Ozkaynak E, Rueger DC, Drier EA, Corbett C, Ridge RJ, Sampath TK, et al. OP-1 cDNA encodes an osteogenic protein in the TGF-beta family. EMBO J. 1990;9(7):2085–93.PubMed Ozkaynak E, Rueger DC, Drier EA, Corbett C, Ridge RJ, Sampath TK, et al. OP-1 cDNA encodes an osteogenic protein in the TGF-beta family. EMBO J. 1990;9(7):2085–93.PubMed
31.
go back to reference Lyons KM, Hogan BL, Robertson EJ. Colocalization of BMP 7 and BMP 2 RNAs suggests that these factors cooperatively mediate tissue interactions during murine development. Mech Dev. 1995;50(1):71–83.PubMedCrossRef Lyons KM, Hogan BL, Robertson EJ. Colocalization of BMP 7 and BMP 2 RNAs suggests that these factors cooperatively mediate tissue interactions during murine development. Mech Dev. 1995;50(1):71–83.PubMedCrossRef
32.
go back to reference Dudley AT, Lyons KM, Robertson EJ. A requirement for bone morphogenetic protein-7 during development of the mammalian kidney and eye. Genes Dev. 1995;9(2):2795–807.PubMedCrossRef Dudley AT, Lyons KM, Robertson EJ. A requirement for bone morphogenetic protein-7 during development of the mammalian kidney and eye. Genes Dev. 1995;9(2):2795–807.PubMedCrossRef
33.
go back to reference Luo G, Hofmann C, Bronckers AL, Sohocki M, Bradley A, Karsenty G. BMP-7 is an inducer of nephrogenesis, and is also required for eye development and skeletal patterning. Genes Dev. 1995;9(22):2808–20.PubMedCrossRef Luo G, Hofmann C, Bronckers AL, Sohocki M, Bradley A, Karsenty G. BMP-7 is an inducer of nephrogenesis, and is also required for eye development and skeletal patterning. Genes Dev. 1995;9(22):2808–20.PubMedCrossRef
34.
go back to reference Zeisberg EM, Tarnavski O, Zeisberg M, Dorfman AL, McMullen JR, Gustafsson E, et al. Endothelial-to-mesenchymal transition contributes to cardiac fibrosis. Nat Med. 2007;13(8):952–61.PubMedCrossRef Zeisberg EM, Tarnavski O, Zeisberg M, Dorfman AL, McMullen JR, Gustafsson E, et al. Endothelial-to-mesenchymal transition contributes to cardiac fibrosis. Nat Med. 2007;13(8):952–61.PubMedCrossRef
35.
go back to reference Miyazawa K, Shinozaki M, Hara T, Furuya T, Miyazono K. Two major Smad pathways in TGF-beta superfamily signalling. Genes Cells. 2002;7(12):1191–204.PubMedCrossRef Miyazawa K, Shinozaki M, Hara T, Furuya T, Miyazono K. Two major Smad pathways in TGF-beta superfamily signalling. Genes Cells. 2002;7(12):1191–204.PubMedCrossRef
36.
go back to reference Zwijsen A, Verschueren K, Huylebroeck D. New intracellular components of bone morphogenetic protein/Smad signaling cascades. FEBS Lett. 2003;546(1):133–9.PubMedCrossRef Zwijsen A, Verschueren K, Huylebroeck D. New intracellular components of bone morphogenetic protein/Smad signaling cascades. FEBS Lett. 2003;546(1):133–9.PubMedCrossRef
38.
go back to reference Reddy R, Buckley S, Doerken M, Barsky L, Weinberg K, Anderson KD, et al. Isolation of a putative progenitor subpopulation of alveolar epithelial type 2 cells. Am J Physiol Lung Cell Mol Physiol. 2004;286(3):L658–67.PubMedCrossRef Reddy R, Buckley S, Doerken M, Barsky L, Weinberg K, Anderson KD, et al. Isolation of a putative progenitor subpopulation of alveolar epithelial type 2 cells. Am J Physiol Lung Cell Mol Physiol. 2004;286(3):L658–67.PubMedCrossRef
Metadata
Title
Increase of bone morphogenetic protein-7 expressing pulmonary resident cells in pneumonectomized rats
Authors
Taro Ohba
Hironobu Wada
Ichiro Yoshino
Shigetoshi Yoshida
Tetsuzo Tagawa
Fumihiro Shoji
Koji Yamazaki
Yoshihiko Maehara
Publication date
01-02-2014
Publisher
Springer Japan
Published in
Surgery Today / Issue 2/2014
Print ISSN: 0941-1291
Electronic ISSN: 1436-2813
DOI
https://doi.org/10.1007/s00595-013-0604-7

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