The lung alveolar lipofibroblast: An evolutionary strategy against neonatal hyperoxic lung injury

Antioxidants and Redox Signaling

Volumn 21, Issue 13, 2014, Pages 1893-1904

  Rehan, Virender K ^a   Torday, John S ^a  

^a HARBOR UCLA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIOXIDANT; LUNG SURFACTANT; OXYGEN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA AGONIST; REACTIVE OXYGEN METABOLITE;

CELL DIFFERENTIATION; CELL TRANSDIFFERENTIATION; CHRONIC LUNG DISEASE; CYTOLOGY; EPITHELIAL MESENCHYMAL TRANSITION; EVOLUTION; HOMEOSTASIS; HUMAN; HYPEROXIA; LUNG; LUNG ALVEOLAR LIPOFIBROBLAST; LUNG DEVELOPMENT; LUNG DYSPLASIA; LUNG FIBROBLAST; LUNG INJURY; MAMMAL; NEONATAL HYPEROXIC LUNG INJURY; NEWBORN DISEASE; NONHUMAN; OXOTRAUMA; PATHOGENESIS; PEROXISOME; PHYLOGENY; POSITIVE END EXPIRATORY PRESSURE; PREMATURITY; RESPIRATORY DISTRESS SYNDROME; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; FIBROBLAST; LUNG ALVEOLUS; NEWBORN; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

VERTEBRATA;

ANIMALS; ANIMALS, NEWBORN; FIBROBLASTS; HUMANS; HYPEROXIA; INFANT, NEWBORN; PULMONARY ALVEOLI;

EID: 84911863104     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2013.5793     Document Type: Review

References (101)

1. Awonusonu F, Srinivasan S, Strange J, Al-Jumaily W, and Bruce MC. Developmental shift in the relative percentages of lung fibroblast subsets: role of apoptosis postseptation. Am J Physiol 277: L848-L859, 1999.
2. Baerends RJ, Rasmussen SW, Hilbrands RE, van der HM, Faber KN, Reuvekamp PT, Kiel JA, Cregg JM, van der KIJ, and Veenhuis M. The Hansenula polymorpha PER9 gene encodes a peroxisomal membrane protein essential for peroxisome assembly and integrity. J Biol Chem 271: 8887-8894, 1996.
3. Bancalari E, Claure N, and Sosenko IR. Bronchopulmonary dysplasia: changes in pathogenesis, epidemiology and definition. Semin Neonatol 8: 63-71, 2003.
4. Baumgart F, Ospina OL, Mingarro I, Rodriguez-Crespo I, and Perez-Gil J. Palmitoylation of pulmonary surfactant protein SP-C is critical for its functional cooperation with SP-B to sustain compression/expansion dynamics in cholesterol-containing surfactant films. Biophys J 99: 3234-3243, 2010.
5. Behrendtsen O, Alexander CM, and Werb Z. Cooperative interactions between extracellular matrix, integrins and parathyroid hormone-related peptide regulate parietal endoderm differentiation in mouse embryos. Development 121: 4137-4148, 1995.
6. Berner RA. Phanerozoic atmospheric oxygen: new results using the GEOCARBSULF model. Am J Sci 309: 603-606, 2009.
7. Besnard V, Wert SE, Stahlman MT, Postle AD, Xu Y, Ikegami M, and Whitsett JA. Deletion of Scap in alveolar type II cells influences lung lipid homeostasis and identifies a compensatory role for pulmonary lipofibroblasts. J Biol Chem 284: 4018-4030, 2009.
8. Bland RD, Xu L, Ertsey R, Rabinovitch M, Albertine KH, Wynn KA, Kumar VH, Ryan RM, Swartz DD, Csiszar K, and Fong KS. Dysregulation of pulmonary elastin synthesis and assembly in preterm lambs with chronic lung disease. Am J Physiol Lung Cell Mol Physiol 292: L1370-L1384, 2007.
9. Bolte K, Gruenheit N, Felsner G, Sommer MS, Maier UG, and Hempel F. Making new out of old: recycling and modification of an ancient protein translocation system during eukaryotic evolution. Mechanistic comparison and phylogenetic analysis of ERAD, SELMA and the peroxisomal importomer. Bioessays 33: 368-376, 2011.
10. Boros LG, Torday JS, Paul Lee WN, and Rehan VK. Oxygen-induced metabolic changes and transdifferentiation in immature fetal rat lung lipofibroblasts. Mol Genet Metab 77: 230-236, 2002.
11. Brody JS and Vaccaro C. Postnatal formation of alveoli: interstitial events and physiologic consequences. Fed Proc 38: 215-223, 1979.
12. Buczynski BW, Maduekwe ET, and O'Reilly MA. The role of hyperoxia in the pathogenesis of experimental Bronchopulmonary Dysplasia. Semin Perinatol 37: 69-78, 2013.
13. Cairns-Smith AG. Seven Clues to the Origin of Life. Cambridge, United Kingdom: Cambridge University Press, 1985.
14. Carlo WA. Gentle ventilation: the new evidence from the SUPPORT, COIN, VON, CURPAP, Colombian Network, and Neocosur Network trials. Early Hum Dev 88 Suppl 2: S81-S83, 2012.
15. Cerny L, Torday JS, and Rehan VK. Prevention and treatment of bronchopulmonary dysplasia: contemporary status and future outlook. Lung 186: 75-89, 2008.
16. Chapman MJ and Margulis L. Morphogenesis by symbiogenesis. Int Microbiol 1: 319-326, 1998.
17. Chen HL, Demiralp B, Schneider A, Koh AJ, Silve C, Wang CY, and McCauley LK. Parathyroid hormone and parathyroid hormone-related protein exert both pro- and anti-apoptotic effects in mesenchymal cells. J Biol Chem 277: 19374-19381, 2002.
18. Choi CW. Lung interstitial cells during alveolarization. Korean J Pediatr 53: 979-984, 2010.
19. Csete M, Walikonis J, Slawny N, Wei Y, Korsnes S, Doyle JC, and Wold B. Oxygen-mediated regulation of skeletal muscle satellite cell proliferation and adipogenesis in culture. J Cell Physiol 189: 189-196, 2001.
20. Cucoranu I, Clempus R, Dikalova A, Phelan PJ, Ariyan S, Dikalov S, and Sorescu D. NAD(P)H oxidase 4 mediates transforming growth factor-beta1-induced differentiation of cardiac fibroblasts into myofibroblasts. Circ Res 97: 900-907, 2005.
21. Dasgupta C, Sakurai R, Wang Y, Guo P, Ambalavanan N, Torday JS, and Rehan VK. Hyperoxia-induced neonatal rat lung injury involves activation of TGF-{beta} and Wnt signaling and is protected by rosiglitazone. Am J Physiol Lung Cell Mol Physiol 296: L1031-L1041, 2009.
22. Davis JM. Role of oxidant injury in the pathogenesis of neonatal lung disease. Acta Paediatr Suppl 91: 23-25, 2002.
23. de Duve D. The peroxisome: a new cytoplasmic organelle. Proc R Soc Lond B Biol Sci 173: 71-83, 1969.
24. de Duve D. Peroxisomes and related particles in historical perspective. Ann N Y Acad Sci 386: 1-4, 1982.
25. del Rio LA, Palma JM, Sandalio LM, Corpas FJ, Pastori GM, Bueno P, and Lopez-Huertas E. Peroxisomes as a source of superoxide and hydrogen peroxide in stressed plants. Biochem Soc Trans 24: 434-438, 1996.
26. Diamond AG, Gonterman RM, Anderson AL, Menon K, Offutt CD, Weaver CH, Philbrick WM, and Foley J. Parathyroid hormone hormone-related protein and the PTH receptor regulate angiogenesis of the skin. J Invest Dermatol 126: 2127-2134, 2006.
27. Dreyer C, Krey G, Keller H, Givel F, Helftenbein G, and Wahli W. Control of the peroxisomal beta-oxidation pathway by a novel family of nuclear hormone receptors. Cell 68: 879-887, 1992.
28. Frank L, Bucher JR, and Roberts RJ. Oxygen toxicity in neonatal and adult animals of various species. J Appl Physiol Respir Environ Exerc Physiol 45: 699-704, 1978.
29. Frank L and Groseclose EE. Preparation for birth into an O2-rich environment: the antioxidant enzymes in the developing rabbit lung. Pediatr Res 18: 240-244, 1984.
30. Frank L, Lewis PL, and Sosenko IR. Dexamethasone stimulation of fetal rat lung antioxidant enzyme activity in parallel with surfactant stimulation. Pediatrics 75: 569-574, 1985.
31. Gabaldon T. Peroxisome diversity and evolution. Philos Trans R Soc Lond B Biol Sci 365: 765-773, 2010.
32. Gray C, Bratt D, Lees J, daCosta M, Plant K, Watson OJ, Solaymani-Kohal S, Tazzyman S, Serbanovic-Canic J, Crossman DC, Keavney BD, Haase A, McMahon K, Gering M, Roehl H, Evans PC, and Chico TJ. Loss of function of parathyroid hormone receptor 1 induces Notch-dependent aortic defects during zebrafish vascular development. Arterioscler Thromb Vasc Biol 33: 1257-1263, 2013.
33. Gregory GA, Kitterman JA, Phibbs RH, Tooley WH, and Hamilton WK. Treatment of the idiopathic respiratorydistress syndrome with continuous positive airway pressure. N Engl J Med 284: 1333-1340, 1971.
34. Hernandez-Garcia D, Wood CD, Castro-Obregon S, and Covarrubias L. Reactive oxygen species: a radical role in development? Free Radic Biol Med 49: 130-143, 2010.
35. Ho YS. Transgenic and knockout models for studying the role of lung antioxidant enzymes in defense against hyperoxia. Am J Respir Crit Care Med 166: S51-S56, 2002.
36. Ho YS, Gargano M, Cao J, Bronson RT, Heimler I, and Hutz RJ. Reduced fertility in female mice lacking copperzinc superoxide dismutase. J Biol Chem 273: 7765-7769, 1998.
37. Ho YS, Magnenat JL, Bronson RT, Cao J, Gargano M, Sugawara M, and Funk CD. Mice deficient in cellular glutathione peroxidase develop normally and show no increased sensitivity to hyperoxia. J Biol Chem 272: 16644-16651, 1997.
38. Ho YS, Vincent R, Dey MS, Slot JW, and Crapo JD. Transgenic models for the study of lung antioxidant defense: enhanced manganese-containing superoxide dismutase activity gives partial protection to B6C3 hybrid mice exposed to hyperoxia. Am J Respir Cell Mol Biol 18: 538-547, 1998.
39. Hu E, Tontonoz P, and Spiegelman BM. Transdifferentiation of myoblasts by the adipogenic transcription factors PPAR gamma and C/EBP alpha. Proc Natl Acad Sci U S A 92: 9856-9860, 1995.
40. Isowa S, Shimo T, Ibaragi S, Kurio N, Okui T, Matsubara K, Hassan NM, Kishimoto K, and Sasaki A. PTHrP regulates angiogenesis and bone resorption via VEGF expression. Anticancer Res 30: 2755-2767, 2010.
41. Jobe AJ. The new BPD: an arrest of lung development. Pediatr Res 46: 641-643, 1999.
42. Kawahara T and Lambeth JD. Molecular evolution of Phox-related regulatory subunits for NADPH oxidase enzymes. BMC Evol Biol 7: 178, 2007.
43. Kersten S, Desvergne B, and Wahli W. Roles of PPARs in health and disease. Nature 405: 421-424, 2000.
44. Kumar L, Panda RP, Hyder I, Yadav VP, Sastry KV, Sharma GT, Mahapatra RK, Bag S, Bhure SK, Das GK, Mitra A, and Sarkar M. Expression of leptin and its receptor in corpus luteum during estrous cycle in buffalo (Bubalus bubalis). Anim Reprod Sci 135: 8-17, 2012.
45. Kunau WH. Peroxisome biogenesis: end of the debate. Curr Biol 15: R774-R776, 2005.
46. Lau MJ and Keough KM. Lipid composition of lung and lung lavage fluid from map turtles (Malaclemys geographica) maintained at different environmental temperatures. Can J Biochem 59: 208-219, 1981.
47. Leon S, Goodman JM, and Subramani S. Uniqueness of the mechanism of protein import into the peroxisome matrix: transport of folded, co-factor-bound and oligomeric proteins by shuttling receptors. Biochim Biophys Acta 1763: 1552-1564, 2006.
48. Liu J, Sakurai R, O'Roark EM, Kenyon NJ, Torday JS, and Rehan VK. PPARgamma agonist rosiglitazone prevents perinatal nicotine exposure-induced asthma in rat offspring. Am J Physiol Lung Cell Mol Physiol 300: L710-L717, 2011.
49. Longo D, Fauci A, Kasper D, Hauser S, Jameson L, and Loscalzo J. Harrison's Principles of Internal Medicine. New York, NY: McGraw-Hill, 2012.
50. Maksvytis HJ, Vaccaro C, and Brody JS. Isolation and characterization of the lipid-containing interstitial cell from the developing rat lung. Lab Invest 45: 248-259, 1981.
51. Masood A, Belcastro R, Li J, Kantores C, Jankov RP, and Tanswell AK. A peroxynitrite decomposition catalyst prevents 60% O2-mediated rat chronic neonatal lung injury. Free Radic Biol Med 49: 1182-1191, 2010.
52. McElroy MC, Postle AD, and Kelly FJ. Catalase, superoxide dismutase and glutathione peroxidase activities of lung and liver during human development. Biochim Biophys Acta 1117: 153-158, 1992.
53. McGowan SE and Torday JS. The pulmonary lipofibroblast (lipid interstitial cell) and its contributions to alveolar development. Annu Rev Physiol 59: 43-62, 1997.
54. Mezentseva NV, Kumaratilake JS, and Newman SA. The brown adipocyte differentiation pathway in birds: an evolutionary road not taken. BMC Biol 6: 17, 2008.
55. Northway WH Jr., Rosan RC, and Porter DY. Pulmonary disease following respirator therapy of hyaline-membrane disease. Bronchopulmonary dysplasia. N Engl J Med 276: 357-368, 1967.
56. Phan SH. Genesis of the myofibroblast in lung injury and fibrosis. Proc Am Thorac Soc 9: 148-152, 2012.
57. Reddy RC, Rehan VK, Roman J, and Sime PJ. PPARs: Regulators and Translational Targets in the Lung. PPAR Res 2012: 342924, 2012.
58. Rehan V and Torday J. Hyperoxia augments pulmonary lipofibroblast-to-myofibroblast transdifferentiation. Cell Biochem Biophys 38: 239-250, 2003.
59. Rehan VK. Prevention of bronchopulmonary dysplasia: finally, something that works. Indian J Pediatr 73: 1027-1032, 2006.
60. Rehan VK, Dargan-Batra SK, Wang Y, Cerny L, Sakurai R, Santos J, Beloosesky R, Gayle D, and Torday JS. A paradoxical temporal response of the PTHrP/PPARgamma signaling pathway to lipopolysaccharide in an in vitro model of the developing rat lung. Am J Physiol Lung Cell Mol Physiol 293: L182-L190, 2007.
61. Rehan VK, Sakurai R, Corral J, Krebs M, Ibe B, Ihida-Stansbury K, and Torday JS. Antenatally administered PPAR-gamma agonist rosiglitazone prevents hyperoxiainduced neonatal rat lung injury. Am J Physiol Lung Cell Mol Physiol 299: L672-L680, 2010.
62. Rehan VK, Sakurai R, Wang Y, Santos J, Huynh K, and Torday JS. Reversal of nicotine-induced alveolar lipofibroblast- to-myofibroblast transdifferentiation by stimulants of parathyroid hormone-related protein signaling. Lung 185: 151-159, 2007.
63. Rehan VK, Sugano S, Wang Y, Santos J, Romero S, Dasgupta C, Keane MP, Stahlman MT, and Torday JS. Evidence for the presence of lipofibroblasts in human lung. Exp Lung Res 32: 379-393, 2006.
64. Rehan VK and Torday JS. Exploiting the PTHrP signaling pathway to treat chronic lung disease. Drugs Today (Barc) 43: 317-331, 2007.
65. Rehan VK, Wang Y, Patel S, Santos J, and Torday JS. Rosiglitazone, a peroxisome proliferator-activated receptorgamma agonist, prevents hyperoxia-induced neonatal rat lung injury in vivo. Pediatr Pulmonol 41: 558-569, 2006.
66. Rehan VK, Wang Y, Sugano S, Romero S, Chen X, Santos J, Khazanchi A, and Torday JS. Mechanism of nicotine-induced pulmonary fibroblast transdifferentiation. Am J Physiol Lung Cell Mol Physiol 289: L667- L676, 2005.
67. Rehan VK, Wang Y, Sugano S, Santos J, Patel S, Sakurai R, Boros LG, Lee WP, and Torday JS. In utero nicotine exposure alters fetal rat lung alveolar type II cell proliferation, differentiation, and metabolism. Am J Physiol Lung Cell Mol Physiol 292: L323-L333, 2007.
68. Romer AS. Man and the Vertebrates, Vol. 1. Harmondsworth, GB: Penguin, 1954.
69. Rook D, Schierbeek H, van der Eijk AC, Longini M, Buonocore G, Vento M, van Goudoever JB, and Vermeulen MJ. Resuscitation of very preterm infants with 30% vs. 65% oxygen at birth: study protocol for a randomized controlled trial. Trials 13: 65, 2012.
70. Ross SE, Hemati N, Longo KA, Bennett CN, Lucas PC, Erickson RL, and MacDougald OA. Inhibition of adipogenesis by Wnt signaling. Science 289: 950-953, 2000.
71. Saugstad OD. Oxidative stress in the newborn - a 30-year perspective. Biol Neonate 88: 228-236, 2005.
72. Sosenko IR, Innis SM, and Frank L. Polyunsaturated fatty acids and protection of newborn rats from oxygen toxicity. J Pediatr 112: 630-637, 1988.
73. Sosenko IR, Innis SM, and Frank L. Menhaden fish oil, n- 3 polyunsaturated fatty acids, and protection of newborn rats from oxygen toxicity. Pediatr Res 25: 399-404, 1989.
74. Sosenko IR, Innis SM, and Frank L. Intralipid increases lung polyunsaturated fatty acids and protects newborn rats from oxygen toxicity. Pediatr Res 30: 413-417, 1991.
75. Sosenko IR, Nielsen HC, and Frank L. Lack of sex differences in antioxidant enzyme development in the fetal rabbit lung. Pediatr Res 26: 16-19, 1989.
76. Sumimoto H. Structure, regulation and evolution of Noxfamily NADPH oxidases that produce reactive oxygen species. FEBS J 275: 3249-3277, 2008.
77. Titorenko VI and Mullen RT. Peroxisome biogenesis: the peroxisomal endomembrane system and the role of the ER. J Cell Biol 174: 11-17, 2006.
78. Torday J, Hua J, and Slavin R. Metabolism and fate of neutral lipids of fetal lung fibroblast origin. Biochim Biophys Acta 1254: 198-206, 1995.
79. Torday J and Rehan V. Neutral lipid trafficking regulates alveolar type II cell surfactant phospholipid and surfactant protein expression. Exp Lung Res 37: 376-386, 2011.
80. Torday JS and Rehan VK. Stretch-stimulated surfactant synthesis is coordinated by the paracrine actions of PTHrP and leptin. Am J Physiol Lung Cell Mol Physiol 283: L130-L135, 2002.
81. Torday JS and Rehan VK. Deconvoluting lung evolution using functional/comparative genomics. Am J Respir Cell Mol Biol 31: 8-12, 2004.
82. Torday JS and Rehan VK. Developmental cell/molecular biologic approach to the etiology and treatment of bronchopulmonary dysplasia. Pediatr Res 62: 2-7, 2007.
83. Torday JS and Rehan VK. The evolutionary continuum from lung development to homeostasis and repair. Am J Physiol Lung Cell Mol Physiol 292: L608-L611, 2007.
84. Torday JS and Rehan VK. Cell-cell signaling drives the evolution of complex traits: introduction-lung evo-devo. Integr Comp Biol 49: 142-154, 2009.
85. Torday JS and Rehan VK. Lung evolution as a cipher for physiology. Physiol Genomics 38: 1-6, 2009.
86. Torday JS and Rehan VK. A cell-molecular approach predicts vertebrate evolution. Mol Biol Evol 28: 2973-2981, 2011.
87. Torday JS and Rehan VK. Evolutionary Biology, Cell-Cell Communication and Complex Disease. Hoboken, NJ: Wiley, 2012.
88. Torday JS and Rehan VK, Hicks JW, Wang T, Maina J, Weibel ER, Hsia CC, Sommer RJ, Perry SF. Deconvoluting lung evolution: from phenotypes to gene regulatory networks. Integr Comp Biol 47: 601-609, 2007.
89. Torday JS, Sun H, Wang L, Torres E, Sunday ME, and Rubin LP. Leptin mediates the parathyroid hormonerelated protein paracrine stimulation of fetal lung maturation. Am J Physiol Lung Cell Mol Physiol 282: L405-L410, 2002.
90. Torday JS, Torday DP, Gutnick J, Qin J, and Rehan V. Biologic role of fetal lung fibroblast triglycerides as antioxidants. Pediatr Res 49: 843-849, 2001.
91. Torday JS, Torres E, and Rehan VK. The role of fibroblast transdifferentiation in lung epithelial cell proliferation, differentiation, and repair in vitro. Pediatr Pathol Mol Med 22: 189-207, 2003.
92. Tordet C, Marin L, and Dameron F. Pulmonary di-andtriacylglycerols during the perinatal development of the rat. Experientia 37: 333-334, 1981.
93. Truong TH and Carroll KS. Redox regulation of epidermal growth factor receptor signaling through cysteine oxidation. Biochemistry 51: 9954-9965, 2012.
94. Vaccaro C and Brody JS. Ultrastructure of developing alveoli. I. The role of the interstitial fibroblast. Anat Rec 192: 467-479, 1978.
95. Wang Y, Santos J, Sakurai R, Shin E, Cerny L, Torday JS, and Rehan VK. Peroxisome proliferator-activated receptor gamma agonists enhance lung maturation in a neonatal rat model. Pediatr Res 65: 150-155, 2009.
96. West JB. Respiratory Physiology: The Essentials. Baltimore, MD: Lippincott, Williams and Wilkins, 2012.
97. Whyte LL. Internal Factors in Evolution. New York, NY: George Braziler, 1968.
98. Wilson TM, Brown PJ, Sternbach DD, and Henke BR. The PPARs: from orphan receptors to drug discovery. J Med Chem 43: 527-550, 2000.
99. Williams GC. Pleiotropy, natural selection, and the evolution of senescence. Evolution 11: 398-411, 1957.
100. Wlodarski K and Wlodarski P. Leptin as a modulator of osteogenesis. Ortop Traumatol Rehabil 11: 1-6, 2009.
101. Yam J, Frank L, and Roberts RJ. Age-related development of pulmonary antioxidant enzymes in the rat. Proc Soc Exp Biol Med 157: 293-296, 1978.