Fatty diabetic lung: Altered alveolar structure and surfactant protein expression

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 298, Issue 3, 2010, Pages

  Foster, David J ^a   Ravikumar, Priya ^a   Bellotto, Dennis J ^a   Unger, Roger H ^a   Hsia, Connie C W ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Collagen; Diabetes mellitus; Lipid deposition; Lung morphometry; Surfactant associated proteins

Indexed keywords

SURFACTANT PROTEIN A; SURFACTANT PROTEIN C; TRIACYLGLYCEROL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ULTRASTRUCTURE; CONTROLLED STUDY; HYPERGLYCEMIA; LAMELLAR BODY; LIPID STORAGE; LUNG ALVEOLUS CELL; LUNG ALVEOLUS MACROPHAGE; LUNG DISEASE; LUNG PARENCHYMA; MALE; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; ZUCKER DIABETIC FATTY RAT;

AGING; ANIMALS; DIABETES MELLITUS, EXPERIMENTAL; OBESITY; ORGAN SIZE; PULMONARY ALVEOLI; PULMONARY SURFACTANTS; RATS; RATS, ZUCKER; SURFACE PROPERTIES; THINNESS; TRIGLYCERIDES;

EID: 77249106524     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00041.2009     Document Type: Article

References (79)

1. Angermuller S, Fahimi HD. Imidazole-buffered osmium tetroxide: an excellent stain for visualization of lipids in transmission electron microscopy. Histochem J 14: 823-835, 1982.
2. Beers MF, Mulugeta S. Surfactant protein C biosynthesis and its emerging role in conformational lung disease. Annu Rev Physiol 67: 663-696, 2005.
3. Beers MF, Wali A, Eckenhoff MF, Feinstein SI, Fisher JH, Fisher AB. An antibody with specificity for surfactant protein C precursors: identification of pro-SP-C in rat lung. Am J Respir Cell Mol Biol 7: 368-378, 1992.
4. Boehme DS, Roberts CM, Bessman SP. High-performance liquid chromatographic analysis of lung phospholipids and their precursors in the offspring of diabetic rats. Biochem Med Metab Biol 44: 29-36, 1990.
5. Boulbou MS, Gourgoulianis KI, Krommydas GC, Klisiaris VK, Arseniou AA, Dafopoulos KC, Molyvdas PA. Diabetes mellitus vs. Raynaud disease: different lung vascular bed disorders. Arch Med Res 33: 531-535, 2002.
6. Bourbon JR, Pignol B, Marin L, Rieutort M, Tordet C. Maturation of fetal rat lung in diabetic pregnancies of graduated severity. Diabetes 34: 734-743, 1985.
7. Bridges JP, Davis HW, Damodarasamy M, Kuroki Y, Howles G, Hui DY, McCormack FX. Pulmonary surfactant proteins A and D are potent endogenous inhibitors of lipid peroxidation and oxidative cellular injury. J Biol Chem 275: 38848-38855, 2000.
8. Brown LA, Longmore WJ. Altered phospholipid secretion in type II pneumocytes isolated from streptozotocin-diabetic rats. Biochim Biophys Acta 878: 258-265, 1986.
9. Brownlee M, Vlassara H, Cerami A. Nonenzymatic glycosylation and the pathogenesis of diabetic complications. Ann Intern Med 101: 527-537, 1984.
10. Burbach JA, Waltz WF, Goodman BE, Schlenker EH. Structural abnormalities underlying alveolar hypoventilation and fluid imbalance in the dystrophic hamster lung. Anat Rec 256: 321-333, 1999.
11. Burri PH, Dbaly J, Weibel ER. The postnatal growth of the rat lung. I. Morphometry. Anat Rec 178: 711-730, 1974.
12. Chance WW, Rhee C, Yilmaz C, Dane DM, Pruneda ML, Raskin P, Hsia CC. Diminished alveolar microvascular reserves in type 2 diabetes reflect systemic microangiopathy. Diabetes Care 31: 1596-1601, 2008.
13. Clark JB, Palmer CJ, Shaw WN. The diabetic Zucker fatty rat. Proc Soc Exp Biol Med 173: 68-75, 1983.
14. Eriksson U, Tydén O, Berne C. Glycogen content and lipid biosynthesis in the lungs of fetuses of diabetic rats. Biol Res Pregnancy Perinatol 4: 103-106, 1983.
15. Farkas GA, Schlenker EH. Pulmonary ventilation and mechanics in morbidly obese Zucker rats. Am J Respir Crit Care Med 150: 356-362, 1994.
16. Fernandez-Real JM, Chico B, Shiratori M, Nara Y, Takahashi H, Ricart W. Circulating surfactant protein A (SP-A), a marker of lung injury, is associated with insulin resistance. Diabetes Care 31: 958-963, 2008.
17. Foster DJ, Yan X, Bellotto DJ, Moe OW, Hagler HK, Estrera AS, Hsia CC. Expression of epidermal growth factor and surfactant proteins during postnatal and compensatory lung growth. Am J Physiol Lung Cell Mol Physiol 283: L981-L990, 2002.
18. Gewolb IH, Barrett C, Wilson CM, Warshaw JB. Delay in pulmonary glycogen degradation in fetuses of streptozotocin diabetic rats. Pediatr Res 16: 869-873, 1982.
19. Guazzi M, Brambilla R, De Vita S, Guazzi MD. Diabetes worsens pulmonary diffusion in heart failure, and insulin counteracts this effect. Am J Respir Crit Care Med 166: 978-982, 2002.
20. Guttentag SH, Phelps DS, Stenzel W, Warshaw JB, Floros J. Surfactant protein A expression is delayed in fetuses of streptozotocin-treated rats. Am J Physiol Lung Cell Mol Physiol 262: L489-L494, 1992.
21. Guttentag SH, Phelps DS, Warshaw JB, Floros J. Delayed hydrophobic surfactant protein (SP-B, SP-C) expression in fetuses of streptozotocintreated rats. Am J Respir Cell Mol Biol 7: 190-197, 1992.
22. Hsia CC, Carbayo JJ, Yan X, Bellotto DJ. Enhanced alveolar growth and remodeling in Guinea pigs raised at high altitude. Respir Physiol Neurobiol 147: 105-115, 2005.
23. Hsia CC, Raskin P. Lung function changes related to diabetes mellitus. Diabetes Technol Ther 9, Suppl 1: S73-S82, 2007.
24. Hsia CC, Raskin P. The diabetic lung: relevance of alveolar microangiopathy for the use of inhaled insulin. Am J Med 118: 205-211, 2005.
25. Hsia CC, Chuong CJ, Johnson RL Jr. Critique of the conceptual basis of diffusing capacity estimates: a finite element analysis. J Appl Physiol 79: 1039-1047, 1995.
26. Iida M, Murakami T, Ishida K, Mizuno A, Kuwajima M, Shima K. Substitution at codon 269 (glutamine - proline) of the leptin receptor (OB-R) cDNA is the only mutation found in the Zucker fatty (fa/fa) rat. Biochem Biophys Res Commun 224: 597-604, 1996.
27. Inselman LS, Chander A, Spitzer AR. Diminished lung compliance and elevated surfactant lipids and proteins in nutritionally obese young rats. Lung 182: 101-117, 2004.
28. Inselman LS, Padilla-Burgos LB, Teichberg S, Spencer H. Alveolar enlargement in obesity-induced hyperplastic lung growth. J Appl Physiol 65: 2291-2296, 1988.
29. Inselman LS, Wapnir RA, Spencer H. Obesity-induced hyperplastic lung growth. Am Rev Respir Dis 135: 613-616, 1987.
30. Islam KN, Mendelson CR. Potential role of nuclear factor kappaB and reactive oxygen species in cAMP and cytokine regulation of surfactant protein-A gene expression in lung type II cells. Mol Endocrinol 16: 1428-1440, 2002.
31. Kida K, Utsuyama M, Takizawa T, Thurlbeck WM. Changes in lung morphologic features and elasticity caused by streptozotocin-induced diabetes mellitus in growing rats. Am Rev Respir Dis 128: 125-131, 1983.
32. Kodolova IM, Lysenko LV, Saltykov BB. [Changes in the lungs in diabetes mellitus]. Arkh Patol 44: 35-40, 1982.
33. Lee Y, Hirose H, Ohneda M, Johnson JH, McGarry JD, Unger RH. Beta-cell lipotoxicity in the pathogenesis of non-insulin-dependent diabetes mellitus of obese rats: impairment in adipocyte-beta-cell relationships. Proc Natl Acad Sci USA 91: 10878-10882, 1994.
34. Leone N, Courbon D, Thomas F, Bean K, Jego B, Leynaert B, Guize L, Zureik M. Lung function impairment and metabolic syndrome: the critical role of abdominal obesity. Am J Respir Crit Care Med 179: 509-516, 2009.
35. Lin CC, Chang CT, Li TC, Kao A. Objective evidence of impairment of alveolar integrity in patients with non-insulin-dependent diabetes mellitus using radionuclide inhalation lung scan. Lung 180: 181-186, 2002.
36. Maiolo C, Mohamed EI, Di DN, Pepe M, Perriello G, De LA. Body composition and pulmonary function in obese type 2 diabetic women. Diabetes Nutr Metab 15: 20-25, 2002.
37. Marvisi M, Bartolini L, del Borrello P, Brianti M, Marani G, Guariglia A, Cuomo A. Pulmonary function in non-insulin-dependent diabetes mellitus. Respiration 68: 268-272, 2001.
38. Massaro GD, Massaro D. Postnatal lung growth: evidence that the gas-exchange region grows fastest at the periphery. Am J Physiol Lung Cell Mol Physiol 265: L319-L322, 1993.
39. Moglia BB, Phelps DS. Changes in surfactant protein A mRNA levels in a rat model of insulin-treated diabetic pregnancy. Pediatr Res 39: 241-247, 1996.
40. Moore TR. A comparison of amniotic fluid fetal pulmonary phospholipids in normal and diabetic pregnancy. Am J Obstet Gynecol 186: 641-650, 2002.
41. Niranjan V, McBrayer DG, Ramirez LC, Raskin P, Hsia CC. Glycemic control and cardiopulmonary function in patients with insulin-dependent diabetes mellitus. Am J Med 103: 504-513, 1997.
42. Ofulue AF, Kida K, Thurlbeck WM. Experimental diabetes and the lung. I. Changes in growth, morphometry, and biochemistry. Am Rev Respir Dis 137: 162-166, 1988.
43. Ofulue AF, Thurlbeck WM. Experimental diabetes and the lung. II. In vivo connective tissue metabolism. Am Rev Respir Dis 138: 284-289, 1988.
44. Ohneda M, Inman LR, Unger RH. Caloric restriction in obese prediabetic rats prevents beta-cell depletion, loss of beta-cell GLUT 2 and glucose incompetence. Diabetologia 38: 173-179, 1995.
45. Orci L, Ravazzola M, Baetens D, Inman L, Amherdt M, Peterson RG, Newgard CB, Johnson JH, Unger RH. Evidence that down-regulation of beta-cell glucose transporters in non-insulin-dependent diabetes may be the cause of diabetic hyperglycemia. Proc Natl Acad Sci USA 87: 9953-9957, 1990.
46. Ozsahin K, Tugrul A, Mert S, Yuksel M, Tugrul G. Evaluation of pulmonary alveolo-capillary permeability in Type 2 diabetes mellitus: using technetium 99mTc-DTPA aerosol scintigraphy and carbon monoxide diffusion capacity. J Diabetes Complications 20: 205-209, 2006.
47. Phillips MS, Liu Q, Hammond HA, Dugan V, Hey PJ, Caskey CJ, Hess JF. Leptin receptor missense mutation in the fatty Zucker rat. Nat Genet 13: 18-19, 1996.
48. Piper JM, Xenakis EM, Langer O. Delayed appearance of pulmonary maturation markers is associated with poor glucose control in diabetic pregnancies. J Matern Fetal Med 7: 148-153, 1998.
49. Plopper CG, Morishige WK. Alterations in granular (type II) pneumocyte ultrastructure by streptozotocin-induced diabetes in the rat. Lab Invest 38: 143-148, 1978.
50. Popov D, Hasu M, Costache G, Stern D, Simionescu M. Capillary and aortic endothelia interact in situ with nonenzymatically glycated albumin and develop specific alterations in early experimental diabetes. Acta Diabetol 34: 285-293, 1997.
51. Popov D, Simionescu M. Alterations of lung structure in experimental diabetes, and diabetes associated with hyperlipidaemia in hamsters. Eur Respir J 10: 1850-1858, 1997.
52. Ramirez LC, Dal Nogare A, Hsia C, Arauz C, Butt I, Strowig SM, Schnurr-Breen L, Raskin P. Relationship between diabetes control and pulmonary function in insulin-dependent diabetes mellitus. Am J Med 91: 371-376, 1991.
53. Reinila A, Akerblom HK, Koivisto VA. The influence of insulin on the lipids in the pulmonary artery and the lungs of severely diabetic rats. A histochemical and chemical study. Diabetologia 16: 59-64, 1979.
54. Reinila A, Koivisto VA, Akerblom HK. Lipids in the pulmonary artery and the lungs of severely diabetic rats. A histochemical and chemical study. Diabetologia 13: 305-310, 1977.
55. Sandler M, Bunn AE, Stewart RI. Cross-section study of pulmonary function in patients with insulin-dependent diabetes mellitus. Am Rev Respir Dis 135: 223-229, 1987.
56. Schellhase DE, Emrie PA, Fisher JH, Shannon JM. Ontogeny of surfactant apoproteins in the rat. Pediatr Res 26: 167-174, 1989.
57. Schuyler MR, Niewoehner DE, Inkley SR, Kohn R. Abnormal lung elasticity in juvenile diabetes mellitus. Am Rev Respir Dis 113: 37-41, 1976.
58. Shimabukuro M, Koyama K, Chen G, Wang MY, Trieu F, Lee Y, Newgard CB, Unger RH. Direct antidiabetic effect of leptin through triglyceride depletion of tissues. Proc Natl Acad Sci USA 94: 4637-4641, 1997.
59. Shimabukuro M, Zhou YT, Levi M, Unger RH. Fatty acid-induced beta cell apoptosis: a link between obesity and diabetes. Proc Natl Acad Sci USA 95: 2498-2502, 1998.
60. Singh M, Feigelson M. Effects of maternal diabetes on the levels, synthetic rates and activities of synthetic enzymes of surface-active phospholipids in perinatal rat lung. Biochim Biophys Acta 753: 53-59, 1983.
61. Sugahara K, Ezaki K, Kaneko T, Morioka T, Maeda H. Studies of the lungs in diabetes mellitus. II. Phospholipid analyses on the surfactant from broncho-alveolar lavage fluid of alloxan-induced diabetic rats. Biochem Biophys Res Commun 98: 163-168, 1981.
62. Sugahara K, Iyama K, Sano K, Morioka T. Differential expressions of surfactant protein SP-A, SP-B, and SP-C mRNAs in rats with streptozotocin-induced diabetes demonstrated by in situ hybridization. Am J Respir Cell Mol Biol 11: 397-404, 1994.
63. Sugahara K, Iyama K, Sano K, Morioka T. Overexpression of pulmonary surfactant apoprotein A mRNA in alveolar type II cells and nonciliated bronchiolar (Clara) epithelial cells in streptozotocin-induced diabetic rats demonstrated by in situ hybridization. Am J Respir Cell Mol Biol 6: 307-314, 1992.
64. Sugahara K, Ushijima K, Morioka T, Usuku G. Studies of the lung in diabetes mellitus. I. Ultrastructural studies of the lungs in alloxan-induced diabetic rats. Virchows Arch A Pathol Anat Histol 390: 313-324, 1981.
65. Tsai MY, Shultz EK, Williams PP, Bendel R, Butler J, Farb H, Wager G, Knox EG, Julian T, Thompson TR. Assay of disaturated phosphatidylcholine in amniotic fluid as a test of fetal lung maturity: experience with 2000 analyses. Clin Chem 33: 1648-1651, 1987.
66. Tyden O, Berne C, Eriksson U. Lung maturation in fetuses of diabetic rats. Pediatr Res 14: 1192-1195, 1980.
67. Uhal BD, Longmore WJ. Altered phospholipid biosynthesis in type II pneumocytes isolated from streptozotocin-diabetic rats. Biochim Biophys Acta 878: 266-272, 1986.
68. Unger RH. How obesity causes diabetes in Zucker diabetic fatty rats. Trends Endocrinol Metab 8: 276-282, 1997.
69. Unger RH. Lipotoxic diseases. Annu Rev Med 53: 319-336, 2002.
70. Unger RH. Lipotoxicity in the pathogenesis of obesity-dependent NIDDM. Genetic and clinical implications. Diabetes 44: 863-870, 1995.
71. Unger RH, Orci L. Diseases of liporegulation: new perspective on obesity and related disorders. FASEB J 15: 312-321, 2001.
72. Vracko R, Thorning D, Huang TW. Basal lamina of alveolar epithelium and capillaries: quantitative changes with aging and in diabetes mellitus. Am Rev Respir Dis 120: 973-983, 1979.
73. Watanabe K, Senju S, Toyoshima H, Yoshida M. Thickness of the basement membrane of bronchial epithelial cells in lung diseases as determined by transbronchial biopsy. Respir Med 91: 406-410, 1997.
74. Weaver TE, Hull WM, Ross GF, Whitsett JA. Intracellular and oligomeric forms of surfactant-associated apolipoproteins(s) A in the rat. Biochim Biophys Acta 827: 260-267, 1985.
75. Weibel ER. Morphometric and stereological methods in respiratory physiology, including fixation techniques. In: Techniques in the Life Sciences: Respiratory Physiology, edited by Otis AB. County Clare, Ireland: Elsevier, 1984, p. 1-35.
76. Weibel ER, Federspiel WJ, Fryder-Doffey F, Hsia CC, König M, Stalder-Navarro V, Vock R. Morphometric model for pulmonary diffusing capacity. I. Membrane diffusing capacity. Respir Physiol 93: 125-149, 1993.
77. Weynand B, Jonckheere A, Frans A, Rahier J. Diabetes mellitus induces a thickening of the pulmonary basal lamina. Respiration 66: 14-19, 1999.
78. Yan X, Polo Carbayo JJ, Weibel ER, Hsia CC. Variation of lung volume after fixation when measured by immersion or Cavalieri method. Am J Physiol Lung Cell Mol Physiol 284: L242-L245, 2003.
79. Ylinen K. High maternal levels of hemoglobin A1c associated with delayed fetal lung maturation in insulin-dependent diabetic pregnancies. Acta Obstet Gynecol Scand 66: 263-266, 1987.