Reversible remodeling of lung tissue during hibernation in the Syrian hamster

Journal of Experimental Biology

Volumn 214, Issue 8, 2011, Pages 1276-1282

  Talaei, Fatemeh ^a   Hylkema, MacHteld N ^a   Bouma, Hjalmar R ^a   Boerema, Ate S ^b   Strijkstra, Arjen M ^a,b   Henning, Rob H ^a   Schmidt, Martina ^b  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

Hibernation; Hypothermia; Lung; Mesocricetus auratus.; Remodeling; Torpor

Indexed keywords

CAVEOLIN 1; COLLAGEN; EPIDERMAL GROWTH FACTOR RECEPTOR;

AIRWAY REMODELING; ANIMAL; ARTICLE; FEMALE; HAMSTER; HIBERNATION; HISTOLOGY; HUMAN; LUNG; LUNG DISEASE; MALE; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SYRIAN HAMSTER;

AIRWAY REMODELING; ANIMALS; CAVEOLIN 1; COLLAGEN; CRICETINAE; FEMALE; HIBERNATION; HUMANS; LUNG; LUNG DISEASES; MALE; MESOCRICETUS; RECEPTOR, EPIDERMAL GROWTH FACTOR;

CRICETINAE; MESOCRICETUS AURATUS; RODENTIA;

EID: 79954999807     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.052704     Document Type: Article

References (56)

1. Arai, S., Hanaya, T., Sakurai, T., Ikeda, M. and Kurimoto, M. (2005). A novel phenomenon predicting the entry into a state of hibernation in Syrian hamsters (Mesocricetus auratus). J. Vet. Med. Sci. 67, 215-217. (Pubitemid 41380457)
2. Barnes, P. J., Thomson, N. C., Rennard, S. I. and Drazen, J. M. (2002). Asthma and COPD basic mechanisms and clinical management. San Diego, CA: Elsevier Science.
3. Blacquiere, M. J., Timens, W., Melgert, B. N., Geerlings, M., Postma, D. S. and Hylkema, M. N. (2009). Maternal smoking during pregnancy induces airway remodelling in mice offspring. Eur. Respir. J. 33, 1133-1140.
4. Bottoms, S. E., Howell, J. E., Reinhardt, A. K., Evans, I. C. and McAnulty, R. J. (2010). TGF-beta isoform specific regulation of airway inflammation and remodelling in a murine model of asthma. PLoS One 5, e9674.
5. Bougault, V., Turmel, J., St-Laurent, J., Bertrand, M. and Boulet, L. P. (2009). Asthma, airway inflammation and epithelial damage in swimmers and cold-air athletes. Eur. Respir. J. 33, 740-746.
6. Bouma, H. R., Carey, H. V. and Kroese, F. G. M. (2010). Hibernation: the immune system at rest? J. Leukoc. Biol. 88, 619-624.
7. Bradford, M. M. (1976). Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Anal. Biochem. 72, 248-254.
8. Brilla, C. G., Zhou, G. P., Matsubara, L. and Weber, K. T. (1994). Collagenmetabolism in cultured adult-rat cardiac fibroblasts - response to angiotensin-II and aldosterone. J. Mol. Cell. Cardiol. 26, 809-820. (Pubitemid 24223231)
9. Burgel, P. R. and Nadel, J. A. (2004). Roles of epidermal growth factor receptor activation in epithelial cell repair and mucin production in airway epithelium. Thorax 59, 992-996. (Pubitemid 39490787)
10. Carey, H. V., Andrews, M. T. and Martin, S. L. (2003). Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature. Physiol. Rev. 83, 1153-1181. (Pubitemid 37222270)
11. Cho, H. Y., Reddy, S. P. M., Yamamoto, M. and Kleeberger, S. R. (2004a). The transcription factor NRF2 protects against pulmonary fibrosis. FASEB J. 18, 1258-1260. (Pubitemid 39561569)
12. Cho, J. Y., Miller, M., Baek, K. J., Han, J. W., Nayar, J., Lee, S. Y., McElwain, K., McElwain, S., Friedman, S. and Broide, D. H. (2004b). Inhibition of airway remodeling in IL-5-deficient mice. J. Clin. Invest. 113, 551-560. (Pubitemid 38542504)
13. Daniels, C. B., Lopatko, O. V. and Orgeig, S. (1998). Evolution of surface activity related functions of vertebrate pulmonary surfactant. Clin. Exp. Pharmacol. Physiol. 25, 716-721. (Pubitemid 28399070)
14. Dausmann, K. H., Glos, J., Ganzhorn, J. U. and Heldmaier, G. (2004). Physiology: hibernation in a tropical primate. Nature 429, 825-826.
15. Dekkers, B. G. J., Maarsingh, H., Meurs, H. and Gosens, R. (2009). Airway structural components drive airway smooth muscle remodeling in asthma. Proc. Am. Thorac. Soc. 6, 683-692.
16. Elias, J. A., Zhu, Z., Chupp, G. and Homer, R. J. (1999). Airway remodeling in asthma. J. Clin. Invest. 104, 1001-1006.
17. Faridy, E. E. (1970). Effect of food and water deprivation on surface activity of lungs of rats. J. Appl. Physiol. 29, 493-498.
18. Geiser, F. (2004). Metabolic rate and body temperature reduction during hibernation and daily torpor. Annu. Rev. Physiol. 66, 239-274. (Pubitemid 40614445)
19. Henning, R. H., Deelman, L. E., Hut, R. A., Van der Zee, E. A., Buikema, H., Nelemans, S. A., Lip, H., De Zeeuw, D., Daan, S. and Epema, A. H. (2002). Normalization of aortic function during arousal episodes in the hibernating ground squirrel. Life Sci. 70, 2071-2083. (Pubitemid 34215132)
20. Hocher, B., George, I., Rebstock, J., Bauch, A., Schwarz, A., Neumayer, H. H. and Bauer, C. (1999). Endothelin system-dependent cardiac remodeling in renovascular hypertension. Hypertension 33, 816-822. (Pubitemid 29140440)
21. Holgate, S. T. (2008). The airway epithelium is central to the pathogenesis of asthma. Allergol. Int. 57, 1-10. (Pubitemid 351413241)
22. Igarashi, J., Shoji, K., Hashimoto, T., Moriue, T., Yoneda, K., Takamura, T., Yamashita, T., Kubota, Y. and Kosaka, H. (2009). Transforming growth factor-{beta}1 downregulates caveolin-1 expression and enhances sphingosine 1-phosphate signaling in cultured vascular endothelial cells. Am. J. Physiol. Cell Physiol. 297, C1263-C1274.
23. Jasmin, J. F., Mercier, I., Hnasko, R., Cheung, M. W. C., Tanowitz, H. B., Dupuis, J. and Lisanti, M. P. (2004). Lung remodeling and pulmonary hypertension after myocardial infarction: pathogenic role of reduced caveolin expression. Cardiovasc. Res. 63, 747-755. (Pubitemid 39078689)
24. Jimenez, W., Pares, A., Caballeria, J., Heredia, D., Bruguera, M., Torres, M., Rojkind, M. and Rodes, J. (1985). Measurement of fibrosis in needle liver biopsiesevaluation of a colorimetric method. Hepatology 5, 815-818. (Pubitemid 15236626)
25. Johnson, P. R. A., Burgess, J. K., Underwood, P. A., Au, W., Poniris, M. H., Tamm, M., Ge, Q. and Black, J. L. (2004). Extracellular matrix proteins modulate asthmatic airway smooth muscle cell proliferation via an autocrine mechanism. J. Allergy Clin. Immunol. 113, 690-696. (Pubitemid 38530425)
26. Karjalainen, E. M., Laitinen, A., Sue-Chu, M., Altraja, A., Bjermer, L. and Laitinen, L. A. (2000). Evidence of airway inflammation and remodeling in ski athletes with and without bronchial hyperresponsiveness to methacholine. Am. J. Respir. Crit. Care Med. 161, 2086-2091. (Pubitemid 30418154)
27. Kortner, G. and Geiser, F. (2000). The temporal organization of daily torpor and hibernation: circadian and circannual rhythms. Chronobiol. Int. 17, 103-128. (Pubitemid 30176701)
28. Kramer, E. L., Mushaben, E. M., Pastura, P. A., Acciani, T. H., Deutsch, G. H., Khurana Hershey, G. K., Korfhagen, T. R., Hardie, W. D., Whitsett, J. A. and Le Cras, T. D. (2009). Egr-1 suppresses EGFR-mediated airway hyperresponsiveness and lung remodeling in mice. Am. J. Respir. Cell Mol. Biol. 41, 415-425.
29. Kuba, K., Imai, Y. and Penninger, J. M. (2006). Angiotensin-converting enzyme 2 in lung diseases. Curr. Opin. Pharmacol. 6, 271-276. (Pubitemid 43670913)
30. LeCras, T. D. (2009). Remodeling in the developing lung - role for the EGF receptor. FASEB J. 23, 10.
31. Le Lay, S. and Kurzchalia, T. V. (2005). Getting rid of caveolins: phenotypes of caveolin-deficient animals. Biochim. Biophys. Acta Mol. Cell Res. 1746, 322-333. (Pubitemid 41815026)
32. Le Saux, C. J., Teeters, K., Miyasato, S. K., Hoffmann, P. R., Bollt, O., Douet, V., Shohet, R. V., Broide, D. H. and Tam, E. K. (2008a). Down-regulation of caveolin-1, an inhibitor of transforming growth factor-beta signaling, in acute allergen-induced airway remodeling. J. Biol. Chem. 283, 5760-5768.
33. Le Saux, C. J., Teeters, K., Miyasato, S. K., Hoffmann, P. R., Bollt, O., Douet, V., Shohet, R. V., Broide, D. H. and Tam, E. K. (2008b). Down-regulation of caveolin-1, an inhibitor of transforming growth factor-beta signaling, in acute allergen-induced airway remodeling. J. Biol. Chem. 283, 5760-5768.
34. Meijering, B. D., van der Wouden, E. A., Pelgrom, V., Henning, R. H., Sharma, K. and Deelman, L. E. (2009). TGF-beta inhibits Ang II-induced MAPK p44/42 signaling in vascular smooth muscle cells by Ang II type 1 receptor downregulation. J. Vasc. Res. 46, 459-468.
35. Melling, J. and Keough, K. M. W. (1981). Major phospholipids of the lung and lung lavage fluid from warm and cold acclimated Richardson's ground squirrels (Spermophilus richardsoni). Comp. Biochem. Physiol. 69B, 797-802.
36. Murata, H., Zhou, L., Ochoa, S., Hasan, A., Badiavas, E. and Falanga, V. (1997). TGF-[beta]3 stimulates and regulates collagen synthesis through TGF-[beta]1-dependent and independent mechanisms. J. Invest. Dermatol. 108, 258-262. (Pubitemid 27116220)
37. Nadel, J. A. (2001). Role of epidermal growth factor receptor activation in regulating mucin synthesis. Respir. Res. 2, 85-89. (Pubitemid 34187912)
38. Navarro, A., Nand-Apte, B. and Parat, M. O. (2004). A role for caveolae in cell migration. FASEB J. 18, 1801-1811. (Pubitemid 39602266)
39. Norkin, L. and Kuksin, D. (2005). The caveolae-mediated sv40 entry pathway bypasses the golgi complex en route to the endoplasmic reticulum. Virol. J. 2, 38.
40. Ormond, C. J., Orgeig, S., Daniels, C. B. and Milsom, W. K. (2003a). Thermal acclimation of surfactant secretion and its regulation by adrenergic and cholinergic agonists in type II cells isolated from warm-active and torpid golden-mantled ground squirrels, Spermophilus lateralis. J. Exp. Biol. 206, 3031-3041. (Pubitemid 37073839)
41. Ormond, C. J., Orgeig, S., Daniels, C. B. and Milsom, W. K. (2003b). Thermal acclimation of surfactant secretion and its regulation by adrenergic and cholinergic agonists in type II cells isolated from warm-active and torpid golden-mantled ground squirrels, Spermophilus lateralis. J. Exp. Biol. 206, 3031-3041. (Pubitemid 37073839)
42. Ramos-Barbon, D., Ludwig, M. S. and Martin, J. G. (2004). Airway remodeling -lessons from animal models. Clin. Rev. Allergy Immunol. 27, 3-21. (Pubitemid 39274066)
43. Razani, B., Engelman, J. A., Wang, X. B., Schubert, W., Zhang, X. L., Marks, C. B., Macaluso, F., Russell, R. G., Li, M. M., Pestell, R. G., et al. (2001). Caveolin-1 null mice are viable but show evidence of hyperproliferative and vascular abnormalities. J. Biol. Chem. 276, 38121-38138.
44. Rubin, I. B., Gill, B. E., Guerin, M. R., Kendrick, J. and Nettesheim, P. (1978). Correlation of respiratory parameters in hamsters with the lung deposition of radiolabeled cigarette smoke. Environ. Res. 16, 70-76. (Pubitemid 8369418)
45. Sahebjami, H. (1993). Nutrition and lung structure and function. Exp. Lung Res. 19, 105-124. (Pubitemid 23114015)
46. Sandovici, M., Henning, R. H., Hut, R. A., Strijkstra, A. M., Epema, A. H., van Goor, H. and Deelman, L. E. (2004). Differential regulation of glomerular and interstitial endothelial nitric oxide synthase expression in the kidney of hibernating ground squirrel. Nitric Oxide 11, 194-200. (Pubitemid 39371097)
47. Sarin, S., Undem, B., Sanico, A. and Togias, A. (2006). The role of the nervous system in rhinitis. J. Allergy Clin. Immunol. 118, 999-1016.
48. Shao, C. X., Liu, Y. T., Ruan, H. Q., Li, Y., Wang, H. F., Kohl, F., Goropashnaya, A. V., Fedorov, V. B., Zeng, R., Barnes, B. M. et al. (2010). Shotgun proteomics analysis of hibernating arctic ground squirrels. Mol. Cell. Proteomics 9, 313-326.
49. Shephard, R. J. (2004). Does cold air damage the lungs of winter athletes? Curr. Sports Med. Rep. 3, 289-291.
50. Simons, K. and Ikonen, E. (1997). Functional rafts in cell membranes. Nature 387, 569-572. (Pubitemid 27248754)
51. Storey, K. B. (2010). Out cold: biochemical regulation of mammalian hibernation - a mini-review. Gerontology 56, 220-230.
52. Sue-Chu, M., Larsson, L., Moen, T., Rennard, S. I. and Bjermer, L. (1999). Bronchoscopy and bronchoalveolar lavage findings in cross-country skiers with and without "ski asthma". Eur. Respir. J. 13, 626-632. (Pubitemid 29180177)
53. Ten Hacken, N. H. T., Postma, D. S. and Timens, W. (2003). Airway remodeling and long-term decline in lung function in asthma. Curr. Opin. Pulm. Med. 9, 9-14. (Pubitemid 35440964)
54. Velickovska, V., Lloyd, B. P., Qureshi, S. and van Breukelen, F. (2005). Proteolysis is depressed during torpor in hibernators at the level of the 20S core protease. J. Comp. Physiol. B Biochem. Syst. Environ. Physiol. 175, 329-335. (Pubitemid 40938472)
55. Vignola, A. M., Mirabella, F., Costanzo, G., Di Giorgi, R., Gjomarkaj, M., Bellia, V. and Bonsignore, G. (2003). Airway remodeling in asthma. Chest 123, 417S-422S. (Pubitemid 36315442)
56. Zancanaro, C., Malatesta, M., Mannello, F., Vogel, P. and Fakan, S. (1999). The kidney during hibernation and arousal from hibernation. A natural model of organ preservation during cold ischaemia and reperfusion. Nephrol. Dial. Transplant. 14, 1982-1990. (Pubitemid 29358898)