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Changes in aquaporins expression due to acute water restriction in naturally aging mice

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Abstract

Aquaporins (AQPs) are water channels in the cell membrane that regulate osmosis in response to rapid changes in intracellular and extracellular fluid concentration caused by extrinsic factors. While there are so many studies on the association of AQPs with muscular atrophy, sarcopenia, and Duchenne muscular dystrophy (DMD), the expression of AQP has not been verified in naturally aging mice or humans. Notably, due to the characteristics of AQPs, the difference in function cannot be evaluated without extrinsic factors such as acute water restriction. The purpose of this study was to investigate the changes in AQPs expression and function due to natural aging under acute water restriction conditions in aging mice. The expression of AQP4 was shown to decrease with aging similar to previous studies. However, for the first time, this study results confirmed that AQP1 expression increased in aging mice. In addition, the expression of Aqp1 decreased in the acute water restricted group compared to the control group after acute water restriction in aging mice. These results suggest that although the expression of AQP1 increases with aging, its function is reduced. We also confirmed that overexpression of Aqp1 can inhibit myotube differentiation and that knockdown can promote myotube differentiation through in vitro experiments. In conclusion, based on our results, we suggest that the AQP1 is an important factor in sarcopenia caused by natural aging accompanied by chronic dehydration.

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References

  1. Agre P (2006) The aquaporin water channels. Proc Am Thorac Soc 3:5–13. https://doi.org/10.1513/pats.200510-109JH

    Article  CAS  Google Scholar 

  2. Agre P, King LS, Yasui M, Guggino WB, Ottersen OP, Fujiyoshi Y, Engel A, Nielsen S (2002) Aquaporin water channels--from atomic structure to clinical medicine. J Physiol 542:3–16. https://doi.org/10.1113/jphysiol.2002.020818

    Article  CAS  Google Scholar 

  3. Au CG, Butler TL, Egan JR, Cooper ST, Lo HP, Compton AG, North KN, Winlaw DS (2008) Changes in skeletal muscle expression of AQP1 and AQP4 in dystrophinopathy and dysferlinopathy patients. Acta Neuropathol 116:235–246. https://doi.org/10.1007/s00401-008-0369-z

    Article  CAS  Google Scholar 

  4. Au CG, Cooper ST, Lo HP, Compton AG, Yang N, Wintour EM, North KN, Winlaw DS (2004) Expression of aquaporin 1 in human cardiac and skeletal muscle. J Mol Cell Cardiol 36:655–662. https://doi.org/10.1016/j.yjmcc.2004.01.009

    Article  CAS  Google Scholar 

  5. Baek KW, Jung YK, Kim JS, Park JS, Hah YS, Kim SJ, Yoo JI (2020) Rodent model of muscular atrophy for sarcopenia study. J Bone Metab 27:97–110. https://doi.org/10.11005/jbm.2020.27.2.97

    Article  Google Scholar 

  6. Baek KW, Jung YK, Park JS, Kim JS, Hah YS, Kim SJ, Yoo JI (2021) Two types of mouse models for sarcopenia research: senescence acceleration and genetic modification models. J Bone Metab 28:179–191. https://doi.org/10.11005/jbm.2021.28.3.179

    Article  Google Scholar 

  7. Baek KW, Kim JS, Park JS, Kim SJ, Ha YC, Jeong OY, Yoo JI (2020) Validation of dual energy X-ray absorptiometry and nuclear magnetic resonance in the analysis of body composition in mice. J Bone Metab 27:291–299. https://doi.org/10.11005/jbm.2020.27.4.291

    Article  Google Scholar 

  8. Baek KW, Lee DI, Jeong MJ, Kang SA, Choe Y, Yoo JI, Yu HS, Kim JS (2020) Effects of lifelong spontaneous exercise on the M1/M2 macrophage polarization ratio and gene expression in adipose tissue of super-aged mice. Exp Gerontol 141:111091. https://doi.org/10.1016/j.exger.2020.111091

    Article  CAS  Google Scholar 

  9. Bekkevold CM, Robertson KL, Reinhard MK, Battles AH, Rowland NE (2013) Dehydration parameters and standards for laboratory mice. J Am Assoc Lab Anim Sci 52:233–239

    CAS  Google Scholar 

  10. Crosbie RH, Dovico SA, Flanagan JD, Chamberlain JS, Ownby CL, Campbell KP (2002) Characterization of aquaporin-4 in muscle and muscular dystrophy. FASEB J 16:943–949. https://doi.org/10.1096/fj.01-0327com

    Article  CAS  Google Scholar 

  11. Dmitrieva NI, Burg MB (2011) Increased insensible water loss contributes to aging related dehydration. PLoS One 6:e20691. https://doi.org/10.1371/journal.pone.0020691

    Article  CAS  Google Scholar 

  12. Frigeri A, Nicchia GP, Balena R, Nico B, Svelto M (2004) Aquaporins in skeletal muscle: reassessment of the functional role of aquaporin-4. FASEB J 18:905–907. https://doi.org/10.1096/fj.03-0987fje

    Article  CAS  Google Scholar 

  13. Frigeri A, Nicchia GP, Nico B, Quondamatteo F, Herken R, Roncali L, Svelto M (2001) Aquaporin-4 deficiency in skeletal muscle and brain of dystrophic mdx mice. FASEB J 15:90–98. https://doi.org/10.1096/fj.00-0260com

    Article  CAS  Google Scholar 

  14. Frigeri A, Nicchia GP, Verbavatz JM, Valenti G, Svelto M (1998) Expression of aquaporin-4 in fast-twitch fibers of mammalian skeletal muscle. J Clin Invest 102:695–703. https://doi.org/10.1172/JCI2545

    Article  CAS  Google Scholar 

  15. Hamalainen N, Pette D (1993) The histochemical profiles of fast fiber types IIB, IID, and IIA in skeletal muscles of mouse, rat, and rabbit. J Histochem Cytochem 41:733–743. https://doi.org/10.1177/41.5.8468455

    Article  CAS  Google Scholar 

  16. Hosaka Y, Yokota T, Miyagoe-Suzuki Y, Yuasa K, Imamura M, Matsuda R, Ikemoto T, Kameya S, Takeda S (2002) Alpha1-syntrophin-deficient skeletal muscle exhibits hypertrophy and aberrant formation of neuromuscular junctions during regeneration. J Cell Biol 158:1097–1107. https://doi.org/10.1083/jcb.200204076

    Article  CAS  Google Scholar 

  17. Hua Y, Ying X, Qian Y, Liu H, Lan Y, Xie A, Zhu X (2019) Physiological and pathological impact of AQP1 knockout in mice. Biosci Rep 39. https://doi.org/10.1042/BSR20182303

  18. Ishido M, Nakamura T (2017) Marked decrease of aquaporin-4 protein is independent of the changes in alpha1-syntrophin and TRPV4 levels in response to denervation-induced muscle atrophy in vivo. J Muscle Res Cell Motil 38:175–181. https://doi.org/10.1007/s10974-017-9471-y

    Article  CAS  Google Scholar 

  19. Ishido M, Nakamura T (2020) Time course changes in AQP4 expression patterns in progressive skeletal muscle atrophy during the early stage of denervation. J Musculoskelet Neuronal Interact 20:114–120

    CAS  Google Scholar 

  20. Kanasi E, Ayilavarapu S, Jones J (2016) The aging population: demographics and the biology of aging. Periodontol 72:13–18. https://doi.org/10.1111/prd.12126

    Article  Google Scholar 

  21. Kingsley J, Torimoto K, Hashimoto T, Eguchi S (2021) Angiotensin II inhibition: a potential treatment to slow the progression of sarcopenia. Clin Sci (Lond) 135:2503–2520. https://doi.org/10.1042/CS20210719

    Article  CAS  Google Scholar 

  22. Lloyd N (2016) AIM coalition announces establishment of ICD-10-CM code for sarcopenia by the centers for disease control and prevention. https://www.prweb.com/releases/2016/04/prweb13376057.htm. Accessed Nov 3 2021

  23. Magni F, Chinello C, Raimondo F, Mocarelli P, Kienle MG, Pitto M (2008) AQP1 expression analysis in human diseases: implications for proteomic characterization. Expert Rev Proteomics 5:29–43. https://doi.org/10.1586/14789450.5.1.29

    Article  CAS  Google Scholar 

  24. Rosenberg IH (1997) Sarcopenia: origins and clinical relevance. J Nutr 127:990S–991S. https://doi.org/10.1093/jn/127.5.990S

    Article  CAS  Google Scholar 

  25. Samorajski T, Delaney C, Durham L, Ordy JM, Johnson JA, Dunlap WP (1985) Effect of exercise on longevity, body weight, locomotor performance, and passive-avoidance memory of C57BL/6J mice. Neurobiol Aging 6:17–24. https://doi.org/10.1016/0197-4580(85)90066-1

    Article  CAS  Google Scholar 

  26. Santilli V, Bernetti A, Mangone M, Paoloni M (2014) Clinical definition of sarcopenia. Clin Cases Miner Bone Metab 11:177–180

    Google Scholar 

  27. Shafiee G, Keshtkar A, Soltani A, Ahadi Z, Larijani B, Heshmat R (2017) Prevalence of sarcopenia in the world: a systematic review and meta- analysis of general population studies. J Diabetes Metab Disord 16:21. https://doi.org/10.1186/s40200-017-0302-x

    Article  Google Scholar 

  28. Silver AJ, Flood JF, Morley JE (1991) Effect of aging on fluid ingestion in mice. J Gerontol 46:B117–B121. https://doi.org/10.1093/geronj/46.3.b117

    Article  CAS  Google Scholar 

  29. Wakayama Y, Hirako S, Ogawa T, Jimi T, Shioda S (2014) Upregulated expression of AQP 7 in the skeletal muscles of obese ob/ob mice. Acta Histochem Cytochem 47:27–33. https://doi.org/10.1267/ahc.13032

    Article  CAS  Google Scholar 

  30. Wakayama Y, Inoue M, Kojima H, Jimi T, Shibuya S, Hara H, Oniki H (2004) Expression and localization of aquaporin 7 in normal skeletal myofiber. Cell Tissue Res 316:123–129. https://doi.org/10.1007/s00441-004-0857-y

    Article  CAS  Google Scholar 

  31. Wakayama Y, Jimi T, Inoue M, Kojima H, Murahashi M, Kumagai T, Yamashita S, Hara H, Shibuya S (2002) Reduced aquaporin 4 expression in the muscle plasma membrane of patients with Duchenne muscular dystrophy. Arch Neurol 59:431–437. https://doi.org/10.1001/archneur.59.3.431

    Article  Google Scholar 

  32. Yoo JI, Choi H, Song SY, Park KS, Lee DH, Ha YC (2018) Relationship between water intake and skeletal muscle mass in elderly Koreans: a nationwide population-based study. Nutrition 53:38–42. https://doi.org/10.1016/j.nut.2018.01.010

    Article  Google Scholar 

  33. Yoo JI, Kim MJ, Na JB, Chun YH, Park YJ, Park Y, Hah YS, Ha YC, Park KS (2018) Relationship between endothelial function and skeletal muscle strength in community dwelling elderly women. J Cachexia Sarcopenia Muscle 9:1034–1041. https://doi.org/10.1002/jcsm.12340

    Article  Google Scholar 

  34. Zadrozniak A, Wojda E, Wlaz A, Luszczki JJ (2009) Characterization of acute adverse-effect profiles of selected antiepileptic drugs in the grip-strength test in mice. Pharmacol Rep 61:737–742. https://doi.org/10.1016/s1734-1140(09)70128-8

    Article  CAS  Google Scholar 

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Funding

This research was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (NRF-2019R1F1A1059231). This study was conducted with support from the Rural Development Administration (PJ014155052019).

Author information

Authors and Affiliations

Authors

Contributions

SJK and KWB: conception and design, animal experiment, data collection, figure preparation, and manuscript writing. YKJ, JSK, and BGK: animal experiment, in vitro experiment, and histological experiment. HSY, JSP, and JIY: conception and financial support. JIY: conception and design, data interpretation, and final approval of the manuscript. All the authors have reviewed and approved the final manuscript. The authors declare that all data were generated in-house and that no paper mill was used.

Corresponding author

Correspondence to Jun-Il Yoo.

Ethics declarations

Ethics approval

The animal studies were approved by the Institutional Animal Care and Use and Committee of Pusan National University (approval number, PNU-2019-2358).

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Not applicable.

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Not applicable.

Conflict of interest

The authors declare no competing interests.

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Key Points

• By natural aging, the expression of AQP1 increases, AQP4 decreases, and AQP7 does not appear to change.

• In aged mice, expression of AQP1 significantly decreased gene expression due to acute water restriction, but protein expression was not.

• AQP1 overexpression inhibits myotube differentiation and knockdown promotes myotube differentiation.

Supplementary information

Fig. S1

AQPs expression on the IHC microscopic images of GA muscle sections. Each arrow indicate AQP1 stained location. Scale bar represents 60 μm (PNG 2293 kb)

High resolution image (TIF 2810 kb)

Fig. S2

AQPs expression on the IHC microscopic images of TA muscle sections. The arrows indicate AQP1 stained locations. Scale bar represents 60 μm (PNG 2237 kb)

High resolution image (TIF 2739 kb)

Fig. S3

Transfection efficiency of Aqp1. (A) Aqp1 overexpression and (B) Aqp1 knockdown. Transfection efficiency was analyzed by quantitative real-time RT-PCR. All data are presented as the mean ± S.D.; vs. control group, **p < 0.01, ****p < 0.0001 (PNG 31 kb)

High resolution image (TIF 59 kb)

Fig. S4

Myotube differentiation according to passage of the day after transfection. Each arrow indicates differentiated myotube. Scale bar represents 1150 μm (PNG 6066 kb)

High resolution image (TIF 7835 kb)

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Kim, SJ., Baek, KW., Jung, YK. et al. Changes in aquaporins expression due to acute water restriction in naturally aging mice. J Physiol Biochem 79, 71–81 (2023). https://doi.org/10.1007/s13105-022-00921-5

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