The role of endogenous H2S formation in reversible remodeling of lung tissue during hibernation in the Syrian hamster

Journal of Experimental Biology

Volumn 215, Issue 16, 2012, Pages 2912-2919

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

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

Collagen; Cystathionine beta synthase; Hibernation; Hydrogen sulfide; Lung remodeling; Mesocricetus auratus

Indexed keywords

BIOLOGICAL MARKER; COLLAGEN; CYSTATHIONINE BETA SYNTHASE; DIPEPTIDYL CARBOXYPEPTIDASE; GELATINASE; HYDROGEN SULFIDE; HYDROXYPROLINE; MATRIX METALLOPROTEINASE; SCLEROPROTEIN;

AIRWAY REMODELING; ANIMAL; ARTICLE; BIOLOGICAL MODEL; ENZYMOLOGY; FEMALE; HAMSTER; HIBERNATION; INFLAMMATION; LUNG; MALE; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SYRIAN HAMSTER;

AIRWAY REMODELING; ANIMALS; BIOLOGICAL MARKERS; COLLAGEN; CRICETINAE; CYSTATHIONINE BETA-SYNTHASE; EXTRACELLULAR MATRIX PROTEINS; FEMALE; GELATINASES; HIBERNATION; HYDROGEN SULFIDE; HYDROXYPROLINE; INFLAMMATION; LUNG; MALE; MATRIX METALLOPROTEINASES; MESOCRICETUS; MODELS, BIOLOGICAL; PEPTIDYL-DIPEPTIDASE A;

ANIMALIA; CRICETINAE; MAMMALIA; MESOCRICETUS AURATUS;

EID: 84864366026     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.067363     Document Type: Article

References (50)

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. and Thomson, N. C. Rennard and S. I. and Drazen J. M. (2002). Asthma and COPD: Basic Mechanisms and Clinical Management. San Diego, CA: Elsevier Science.
3. Bhatia, M., Sidhapuriwala, J. N., Sparatore, A. and Moore, P. K. (2008). Treatment with H2S-releasing diclofenac protects mice against acute pancreatitis-associated lung injury. Shock 29, 84-88.
4. Bouma, H. R., Kroese, F. G. M., Kok, J. W., Talaei, F., Boerema, A. S., Herwig, A., Draghiciu, O., van Buiten, A., Epema, A. H., van Dam, A. et al. (2011). Low body temperature governs the decline of circulating lymphocytes during hibernation through sphingosine-1-phosphate. Proc. Natl. Acad. Sci. USA 108, 2052-2057.
5. Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
6. Carey, H. V., Frank, C. L. and Seifert, J. P. (2000). Hibernation induces oxidative stress and activation of NK-kappaB in ground squirrel intestine. J. Comp. Physiol. B 170, 551-559.
7. 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)
8. Chung, L., Dinakarpandian, D., Yoshida, N., Lauer-Fields, J. L., Fields, G. B., Visse, R. and Nagase, H. (2004). Collagenase unwinds triple-helical collagen prior to peptide bond hydrolysis. EMBO J. 23, 3020-3030. (Pubitemid 39093596)
9. Conroy, J. M. and Lai, C. Y. (1978). A rapid and sensitive fluorescence assay for angiotensin-converting enzyme. Anal. Biochem. 87, 556-561. (Pubitemid 9066625)
10. Corbel, M., Boichot, E. and Lagente, V. (2000). Role of gelatinases MMP-2 and MMP-9 in tissue remodeling following acute lung injury. Braz. J. Med. Biol. Res. 33, 749-754.
11. Demedts, I. K., Brusselle, G. G., Bracke, K. R., Vermaelen, K. Y. and Pauwels, R. A. (2005). Matrix metalloproteinases in asthma and COPD. Curr. Opin. Pharmacol. 5, 257-263. (Pubitemid 40674248)
12. Di Stefano, A., Caramori, G., Oates, T., Capelli, A., Lusuardi, M., Gnemmi, I., Ioli, F., Chung, K. F., Donner, C. F., Barnes, P. J. et al. (2002). Increased expression of nuclear factor-kappaB in bronchial biopsies from smokers and patients with COPD. Eur. Respir. J. 20, 556-563.
13. Elvert, R. and Heldmaier, G. (2005). Cardiorespiratory and metabolic reactions during entrance into torpor in dormice, Glis glis. J. Exp. Biol. 208, 1373-1383. (Pubitemid 40564571)
14. Esechie, A., Kiss, L., Olah, G., Horvath, E. M., Hawkins, H., Szabo, C. and Traber, D. L. (2008). Protective effect of hydrogen sulfide in a murine model of acute lung injury induced by combined burn and smoke inhalation. Clin. Sci. 115, 91-97.
15. Greenlee, K. J., Werb, Z. and Kheradmand, F. (2007). Matrix metalloproteinases in lung: multiple, multifarious, and multifaceted. Physiol. Rev. 87, 69-98. (Pubitemid 46209991)
16. 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)
17. Hongfang, J., Cong, B., Zhao, B., Zhang, C., Liu, X., Zhou, W., Shi, Y., Tang, C. and Junbao, D. (2006). Effects of hydrogen sulfide on hypoxic pulmonary vascular structural remodeling. Life Sci. 78, 1299-1309. (Pubitemid 43199950)
18. Isaksen, B. and Fagerhol, M. K. (2001). Calprotectin inhibits matrix metalloproteinases by sequestration of zinc. J. Clin. Pathol. Mol. Pathol. 54, 289-292. (Pubitemid 32928253)
19. Ji, Y., Pang, Q. F., Xu, G., Wang, L., Wang, J. K. and Zeng, Y. M. (2008). Exogenous hydrogen sulfide postconditioning protects isolated rat hearts against ischemia-reperfusion injury. Eur. J. Pharmacol. 587, 1-7.
20. Jimenez, W., Parés, A., Caballeria, J., Heredia, D., Bruguera, M., Torres, M., Rojkind, M. and Rodés, J. (1985). Measurement of fibrosis in needle liver biopsies: evaluation of a colorimetric method. Hepatology 5, 815-818. (Pubitemid 15236626)
21. Junqueira, L. C. U., Bignolas, G. and Brentani, R. R. (1979). A simple and sensitive method for the quantitative estimation of collagen. Anal. Biochem. 94, 96-99. (Pubitemid 9170209)
22. Körtner, G. and Geiser, F. (2000). The temporal organization of daily torpor and hibernation: circadian and circannual rhythms. Chronobiol. Int. 17, 103-128. (Pubitemid 30176701)
23. Kuba, K., Imai, Y. and Penninger, J. M. (2006). Angiotensin-converting enzyme 2 in lung diseases. Curr. Opin. Pharmacol. 6, 271-276. (Pubitemid 43670913)
24. Laggner, H., Hermann, M., Esterbauer, H., Muellner, M. K., Exner, M., Gmeiner, B. M. and Kapiotis, S. (2007). The novel gaseous vasorelaxant hydrogen sulfide inhibits angiotensin-converting enzyme activity of endothelial cells. J. Hypertens. 25, 2100-2104. (Pubitemid 47476307)
25. Lancaster, L. H., Christman, J. W., Blackwell, T. R., Koay, M. A. and Blackwell, T. S. (2001). Suppression of lung inflammation in rats by prevention of NF-kB activation in the liver. Inflammation 25, 25-31. (Pubitemid 32225479)
26. Lechner, A. J. (1985). Pulmonary design in a microchiropteran bat (Pipistrellus subflavus) during hibernation. Respir. Physiol. 59, 301-312. (Pubitemid 15122800)
27. Li, L., Rossoni, G., Sparatore, A., Lee, L. C., Del Soldato, P. and Moore, P. K. (2007). Anti-inflammatory and gastrointestinal effects of a novel diclofenac derivative. Free Radic. Biol. Med. 42, 706-719. (Pubitemid 46205152)
28. Li, X., Jin, H., Bin, G., Wang, L., Tang, C. and Du, J. (2009). Endogenous hydrogen sulfide regulates pulmonary artery collagen remodeling in rats with high pulmonary blood flow. Exp. Biol. Med. 234, 504-512.
29. Li, Z., Wang, Y., Xie, Y., Yang, Z. and Zhang, T. (2011). Protective effects of exogenous hydrogen sulfide on neurons of hippocampus in a rat model of brain ischemia. Neurochem. Res. 36, 1840-1849.
30. Lohuis, T. D., Beck, T. D. I. and Harlow, H. J. (2005). Hibernating black bears have blood chemistry and plasma amino acid profiles that are indicative of long-term adaptive fasting. Can. J. Zool. 83, 1257-1263. (Pubitemid 41712790)
31. Morin, P., Jr and Storey, K. B. (2009). Mammalian hibernation: differential gene expression and novel application of epigenetic controls. Int. J. Dev. Biol. 53, 433-442.
32. Nowell, M. M., Choi, H. and Rourke, B. C. (2011). Muscle plasticity in hibernating ground squirrels (Spermophilus lateralis) is induced by seasonal, but not lowtemperature, mechanisms. J. Comp. Physiol. B 181, 147-164.
33. Okamoto, I., Kayano, T., Hanaya, T., Arai, S., Ikeda, M. and Kurimoto, M. (2006). Up-regulation of an extracellular superoxide dismutase-like activity in hibernating hamsters subjected to oxidative stress in mid-to late arousal from torpor. Comp. Biochem. Physiol. 144C, 47-56. (Pubitemid 44301959)
34. Qu, K., Chen, C. P., Halliwell, B., Moore, P. K. and Wong, P. T. (2006). Hydrogen sulfide is a mediator of cerebral ischemic damage. Stroke 37, 889-893. (Pubitemid 43731927)
35. Redington, A. E. (2000). Fibrosis and airway remodelling. Clin. Exp. Allergy 30, 42-45.
36. Talaei, F., Bouma, H. R., Van der Graaf, A. C., Strijkstra, A. M., Schmidt, M. and Henning, R. H. (2011a). Serotonin and dopamine protect from hypothermia/rewarming damage through the CBS/H2S pathway. PLoS ONE 6, e22568.
37. Talaei, F., Hylkema, M. N., Bouma, H. R., Boerema, A. S., Strijkstra, A. M., Henning, R. H. and Schmidt, M. (2011b). Reversible remodeling of lung tissue during hibernation in the Syrian hamster. J. Exp. Biol. 214, 1276-1282.
38. Uitto, V. J. and Larjava, H. (1991). Extracellular matrix molecules and their receptors: an overview with special emphasis on periodontal tissues. Crit. Rev. Oral Biol. Med. 2, 323-354.
39. Van Raemdonck, D. (2010). Thoracic organs: current preservation technology and future prospects; part 1: lung. Curr. Opin. Organ Transplant. 15, 150-155.
40. von der Ohe, C. G., Darian-Smith, C., Garner, C. C. and Heller, H. C. (2006). Ubiquitous and temperature-dependent neural plasticity in hibernators. J. Neurosci. 26, 10590-10598. (Pubitemid 44564611)
41. Walter, M. J., Morton, J. D., Kajiwara, N., Agapov, E. and Holtzman, M. J. (2002). Viral induction of a chronic asthma phenotype and genetic segregation from the acute response. J. Clin. Invest. 110, 165-175. (Pubitemid 34787353)
42. Weekley, L. B. (1995). Tissue and plasma peptidase activity is altered during hypothermic hibernation in the 13 lined ground squirrel (Spermophilus tridecemlineatus). Physiol. Behav. 57, 595-598.
43. Wester, K., Asplund, A., Bäckvall, H., Micke, P., Derveniece, A., Hartmane, I., Malmström, P. U. and Pontén, F. (2003). Zinc-based fixative improves preservation of genomic DNA and proteins in histoprocessing of human tissues. Lab. Invest. 83, 889-899. (Pubitemid 36723698)
44. Xiaohui, L., Junbao, D., Lin, S., Jian, L., Xiuying, T., Jianguang, Q., Bing, W., Hongfang, J. and Chaoshu, T. (2005). Down-regulation of endogenous hydrogen sulfide pathway in pulmonary hypertension and pulmonary vascular structural remodeling induced by high pulmonary blood flow in rats. Circ. J. 69, 1418-1424. (Pubitemid 41560825)
45. 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)
46. Zhang, C. Y., Du, J. B., Yan, H. and Tang, C. S. (2005). Effect of a new gasotransmitter, hydrogen sulfide, on collagen remodeling of pulmonary artery under hypoxia. Zhonghua Jie He He Hu Xi Za Zhi 28, 448-452. (Pubitemid 44785196)
47. Zhang, H., Zhi, L., Moochhala, S., Moore, P. K. and Bhatia, M. (2007a). Hydrogen sulfide acts as an inflammatory mediator in cecal ligation and puncture-induced sepsis in mice by upregulating the production of cytokines and chemokines via NFkappaB. Am. J. Physiol. 292, L960-L971. (Pubitemid 46608243)
48. Zhang, H., Zhi, L., Moochhala, S. M., Moore, P. K. and Bhatia, M. (2007b). Endogenous hydrogen sulfide regulates leukocyte trafficking in cecal ligation and puncture-induced sepsis. J. Leukoc. Biol. 82, 894-905. (Pubitemid 47511050)
49. Zhang, H., Moochhala, S. M. and Bhatia, M. (2008). Endogenous hydrogen sulfide regulates inflammatory response by activating the ERK pathway in polymicrobial sepsis. J. Immunol. 181, 4320-4331.
50. Zola, H., Melo, J. V., Zowtyj, H. N., Nikoloutsopoulos, A. and Skinner, J. (1990). The leukocyte-common antigen (CD45) complex and B-lymphocyte activation. Hum. Immunol. 27, 368-377. (Pubitemid 20106369)