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Aquaporin-1: a potential membrane channel for facilitating the adaptability of rabbit nucleus pulposus cells to an extracellular matrix environment

  • Original article
  • Published:
Journal of Orthopaedic Science

Abstract

Background

During the process of degenerative aging of the intervertebral disc (IVD), the extracellular matrix (ECM) environment changes, with osmolarity and oxygen (O2) concentration important components of such changes. The IVD cells respond to maintain the homeostasis and function of the IVD by several mechanisms. Aquaporin-1 (AQP-1) is a transmembrane channel protein that is permeable to water and O2, which prevents rapid volume deformation under osmotic stress and facilitates O2 diffusion across the plasma membrane. One hypothesis is that AQP-1 has potential roles in aging degeneration of IVDs.

Methods

In this study, AQP-1 expression levels were investigated in aging rabbit nucleus pulposus (NP) cells using immunohistochemistry and Western blotting in vivo, and different osmolarities and O2 concentrations in vitro by quantitative real-time PCR.

Results

The results showed that AQP-1 was expressed at different levels in aging rabbit’s NPs and AQP-1 was regulated by the NP cells in different ECM environmental conditions. AQP-1 was downregulated under hypo-osmotic stress to prevent rapid swelling deformation and was upregulated under hypoxic stress to facilitate O2 utilization.

Conclusion

It is suggested that AQP-1 may reflect the status of aged IVDs and have a potential role in reflecting the adaptability of NP cells under different adverse ECM environments in aging degenerated IVDs.

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References

  1. Urban JP, Smith S, Fairbank JC. Nutrition of the intervertebral disc. Spine. 2004;29:2700–9.

    Article  PubMed  Google Scholar 

  2. Urban JP, Marouda A. The measurement of fixed charge density in the intervertebral disc. Biochim Biophys Acta. 1979;586:166–78.

    CAS  Google Scholar 

  3. Tran ND, Kim S, Vincent HK, Rodriguez A, Hinton DR, Bullock MR, Young HF. Aquaporin-1-mediated cerebral edema following traumatic brain injury: effects of acidosis and corticosteroid administration. J Neurosurg. 2010;112:1095–104.

    Article  PubMed  CAS  Google Scholar 

  4. Nesic O, Lee J, Unabia GC, Johnson K, Ye Z, Vergara L, Hulsebosch CE, Perez-Polo JR. Aquaporin 1—a novel player in spinal cord injury. J Neurochem. 2008;105:628–40.

    Article  PubMed  CAS  Google Scholar 

  5. Xiong X, Miao J, Xi Z, Zhang H, Han B, Hu Y. Regulatory effect of dexamethasone on aquaporin-1 expression in cultured bovine trabecular meshwork cells. J Huazhong Univ Sci Technol Med Sci. 2005;25:735–7.

    Article  PubMed  CAS  Google Scholar 

  6. Sonoda H, Yokota-Ikeda N, Oshikawa S, Kanno Y, Yoshinaga K, Uchida K, Ueda Y, Kimiya K, Uezono S, Ueda A, Ito K, Ikeda M. Decreased abundance of urinary exosomal aquaporin-1 in renal ischemia-reperfusion injury. Am J Physiol Renal Physiol. 2009;297:F1006–16.

    Article  PubMed  CAS  Google Scholar 

  7. Trujillo E, González T, Marín R, Martín-Vasallo P, Marples D, Mobasheri A. Human articular chondrocytes, synoviocytes and synovial microvessels express aquaporin water channels; upregulation of AQP1 in rheumatoid arthritis. Histol Histopathol. 2004;19:435–44.

    PubMed  CAS  Google Scholar 

  8. Mobasheri A, Moskaluk CA, Marples D, Shakibaei M. Expression of aquaporin 1 (AQP1) in human synovitis. Ann Anat. 2010;192:116–21.

    Article  PubMed  Google Scholar 

  9. Mobasheri A, Marples D. Expression of the AQP-1 water channel in normal human tissues: a semiquantitative study using tissue microarray technology. Am J Physiol Cell Physiol. 2004;286:C529–37.

    Article  PubMed  CAS  Google Scholar 

  10. Richardson SM, Knowles R, Marples D, Hoyland JA, Mobasheri A. Aquaporin expression in the human intervertebral disc. J Mol Histol. 2008;39:303–9.

    Article  PubMed  CAS  Google Scholar 

  11. Leung VY, Hung SC, Li LC, Wu EX, Luk KD, Chan D, Cheung KM. Age-related degeneration of lumbar intervertebral discs in rabbits revealed by deuterium oxide-assisted MRI. Osteoarthr Cartil. 2008;16:1312–8.

    Article  PubMed  CAS  Google Scholar 

  12. Sowa G, Vadalà G, Studer R, Kompel J, Iucu C, Georgescu H, Gilbertson L, Kang J. Characterization of intervertebral disc aging: longitudinal analysis of a rabbit model by magnetic resonance imaging, histology, and gene expression. Spine. 2008;33:1821–8.

    Article  PubMed  Google Scholar 

  13. Gan JC, Ducheyne P, Vresilovic EJ, Shapiro IM. Intervertebral disc tissue engineering II: cultures of nucleus pulposus cells. Clin Orthop Relat Res. 2003;411:315–24.

    Article  PubMed  Google Scholar 

  14. Bibby SR, Urban JP. Effect of nutrient deprivation on the viability of intervertebral disc cells. Eur Spine J. 2004;13:695–701.

    Article  PubMed  CAS  Google Scholar 

  15. Boyd LM, Richardson WJ, Chen J, Kraus VB, Tewari A, Setton LA. Osmolarity regulates gene expression in intervertebral disc cells determined by gene array and real-time quantitative RT-PCR. Ann Biomed Eng. 2005;33:1071–7.

    Article  PubMed  Google Scholar 

  16. Xia M, Zhu Y. Expression of integrin subunits in the herniated intervertebral disc. Connect Tissue Res. 2008;49:464–9.

    Article  PubMed  CAS  Google Scholar 

  17. Boos N, Weissbach S, Rohrbach H, Weiler C, Spratt KF, Nerlich AG. Classification of age-related changes in lumbar intervertebral discs: 2002 Volvo Award in Basic Science. Spine. 2002;27:2631–44.

    Article  PubMed  Google Scholar 

  18. Brown MD, Tsaltas T. Studies on the permeability of the intervertebral disc during skeletal maturation. Spine. 1976;1:120–4.

    Google Scholar 

  19. Echevarría M, Muñoz-Cabello AM, Sánchez-Silva R, Toledo-Aral JJ, López-Barneo J. Development of cytosolic hypoxia and hypoxia-inducible factor stabilization are facilitated by aquaporin-1 expression. J Biol Chem. 2007;282:30207–15.

    Article  PubMed  Google Scholar 

  20. Maroudas A. Biophysical chemistry of cartilaginous tissues with special reference to solute and fluid transport. Biorheology. 1975;12:233–48.

    PubMed  CAS  Google Scholar 

  21. Holm S, Maroudas A, Urban JP, Selstam G, Nachemson A. Nutrition of the intervertebral disc: solute transport and metabolism. Connect Tissue Res. 1981;8:101–19.

    Article  PubMed  CAS  Google Scholar 

  22. Takeno K, Kobayashi S, Negoro K, Uchida K, Miyazaki T, Yayama T, Shimada S, Baba H. Physical limitations to tissue engineering of intervertebral disc cells: effect of extracellular osmotic change on glycosaminoglycan production and cell metabolism. Laboratory investigation. J Neurosurg Spine. 2007;7:637–44.

    Article  PubMed  Google Scholar 

  23. Ishihara H, Warensjo K, Roberts S, Urban JP. Proteoglycan synthesis in the intervertebral disk nucleus: the role of extracellular osmolality. Am J Physiol. 1997;272:C1499–506.

    PubMed  CAS  Google Scholar 

  24. Pritchard S, Erickson GR, Guilak F. Hyperosmotically induced volume change and calcium signaling in intervertebral disk cells: the role of the actin cytoskeleton. Biophys J. 2002;83:2502–10.

    Article  PubMed  CAS  Google Scholar 

  25. Ishihara H, Urban JP. Effects of low oxygen concentrations and metabolic inhibitors on proteoglycan and protein synthesis rates in the intervertebral disc. J Orthop Res. 1999;17:829–35.

    Article  PubMed  CAS  Google Scholar 

  26. Okada Y, Maeno E, Shimizu T, Dezaki K, Wang J, Morishima S. Receptor-mediated control of regulatory volume decrease (RVD) and apoptotic volume decrease (AVD). J Physiol. 2001;532:3–16.

    Article  PubMed  CAS  Google Scholar 

  27. Rouzaire-Dubois B, Ouanounou G, O’Regan S, Dubois JM. Sodium-dependent activity of aquaporin-1 in rat glioma cells: a new mechanism of cell volume regulation. Pflügers Archiv. Eur J Physiol. 2009;457:1187–98.

    Article  CAS  Google Scholar 

  28. Fischbarg J, Diecke FP, Iserovich P, Rubashkin A. The role of the tight junction in paracellular fluid transport across corneal endothelium. Electro-osmosis as a driving force. J Membr Biol. 2006;210:117–30.

    Article  PubMed  CAS  Google Scholar 

  29. Tsai TT, Guttapalli A, Agrawal A, Albert TJ, Shapiro IM, Risbud MV. MEK/ERK signaling controls osmoregulation of nucleus pulposus cells of the intervertebral disc by transactivation of TonEBP/OREBP. J Bone Miner Res. 2007;22:965–74.

    Article  PubMed  CAS  Google Scholar 

  30. Jiang Q, Cao C, Lu S, Kivlin R, Wallin B, Chu W, Bi Z, Wang X, Wan Y. MEK/ERK pathway mediates UVB-induced AQP1 downregulation and water permeability impairment in human retinal pigment epithelial cells. Int J Mol Med. 2009;23:771–7.

    Article  PubMed  CAS  Google Scholar 

  31. Ohshima H, Urban JP. The effect of lactate and pH on proteoglycan and protein synthesis rates in the intervertebral disc. Spine. 1992;17:1079–82.

    Article  PubMed  CAS  Google Scholar 

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Conflict of interest

We report and confirm that there are no conflicts of interest. We alone are responsible for the content and writing of our paper.

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Authors and Affiliations

  1. Department of Orthopaedics, The First Hospital of China Medical University, No. 155 Nanjingbei Road, Heping District, Shenyang, 110001, People’s Republic of China

    Feng Wang & Yue Zhu

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  1. Feng Wang
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  2. Yue Zhu
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Correspondence to Yue Zhu.

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Wang, F., Zhu, Y. Aquaporin-1: a potential membrane channel for facilitating the adaptability of rabbit nucleus pulposus cells to an extracellular matrix environment. J Orthop Sci 16, 304–312 (2011). https://doi.org/10.1007/s00776-011-0055-1

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  • DOI: https://doi.org/10.1007/s00776-011-0055-1

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