Biological function of bladder smooth muscle cells regulated by multi-modal biomimetic stress_Journal of Biomedical Engineering

Authors：

WEI Tangqiang , CHEN Lin , HU Haifeng ,  YANG Jin

Department of Urology, Affiliated Hospital of Chengdu University, Chengdu 610081, P. R. China;

Corresponding author：

YANG Jin, Email: jinyang012023@163.com

Keywords：

Tissue engineering; Bladder smooth muscle cells; Stress; Cell proliferation; Cell differentiation

DOI：

10.7507/1001-5515.202306036

Video：

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Previous studies have shown that growth arrest, dedifferentiation, and loss of original function occur in cells after multiple generations of culture, which are attributed to the lack of stress stimulation. To investigate the effects of multi-modal biomimetic stress (MMBS) on the biological function of human bladder smooth muscle cells (HBSMCs), a MMBS culture system was established to simulate the stress environment suffered by the bladder, and HBSMCs were loaded with different biomimetic stress for 24 h. Then, cell growth, proliferation and functional differentiation were detected. The results showed that MMBS promoted the growth and proliferation of HBSMCs, and 80 cm H₂O pressure with 4% stretch stress were the most effective in promoting the growth and proliferation of HBSMCs and the expression level of α-smooth muscle actin and smooth muscle protein 22-α. These results suggest that the MMBS culture system will be beneficial in regulating the growth and functional differentiation of HBSMCs in the construction of tissue engineered bladder.

Citation： WEI Tangqiang, CHEN Lin, HU Haifeng, YANG Jin. Biological function of bladder smooth muscle cells regulated by multi-modal biomimetic stress. Journal of Biomedical Engineering, 2024, 41(2): 321-327. doi: 10.7507/1001-5515.202306036 Copy

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2.	Lichtenberg A, Tudorache I, Cebotari S, et al. Preclinical testing of tissue-engineered heart valves re-endothelialized under simulated physiological conditions. Circulation, 2006, 114(1 Suppl): 1559-1565.
3.	Izadpanah P, Golchin A, Firuzyar T, et al. The effect of shear stress on cardiac differentiation of mesenchymal stem cells. Mol Biol Rep, 2022, 49(4): 3167-3175.
4.	Nicolaides K H, Rosen D, Rabinowitz R, et al. Urine production and bladder function in fetuses with open spina bifida. Fetal Ther, 1988, 3(3): 135-140.
5.	Coplen D E, Macarak E J, Levin R M. Developmental changes in normal fetal bovine whole bladder physiology. J Urol, 1994, 151(5): 1391-1395.
6.	Wei W, Howard P S, Kogan B, et al. Urinary diversion results in marked decreases in proliferation and apoptosis in fetal bladder. J Urol, 2012, 188(4): 1306-1312.
7.	Siddiqui H B, Dogru S, Lashkarinia S S, et al. Soft-tissue material properties and mechanogenetics during cardiovascular development. J Cardiovasc Dev Dis, 2022, 9(2): 64.
8.	Jahanbakhsh A, Nourbakhsh M S, Bonakdar S, et al. Evaluation of alginate modification effect on cell-matrix interaction, mechanotransduction and chondrogenesis of encapsulated MSCs. Cell Tissue Res, 2020, 381(2): 255-272.
9.	Elashry M I, Baulig N, Wagner A S, et al. Combined macromolecule biomaterials together with fluid shear stress promote the osteogenic differentiation capacity of equine adipose-derived mesenchymal stem cells. Stem Cell Res Ther, 2021, 12(1): 116.
10.	Atala A. Tissue engineering of human bladder. Br Med Bull, 2011, 97: 81-104.
11.	Tiemessen D, de Jonge P, Daamen W, et al. The effect of a cyclic uniaxial strain on urinary bladder cells. World J Urol, 2017, 35(10): 1531-1539.
12.	Davis N F, Mooney R, Piterina A V, et al. Construction and evaluation of urinary bladder bioreactor for urologic tissue-engineering purposes. Urology, 2011, 78(4): 954-960.
13.	Gao X, Wei T, Liao B, et al. Physiological stretch induced proliferation of human urothelial cells via integrin alpha6-FAK signaling pathway. Neurourol Urodyn, 2018, 37(7): 2114-2120.
14.	Luo D Y, Wazir R, Tian Y, et al. Integrin αv mediates contractility whereas integrin α4 regulates proliferation of human bladder smooth muscle cells via FAK pathway under physiological stretch. J Urol, 2013, 190(4): 1421-1429.
15.	Ringe J, Kaps C, Burmester G R, et al. Stem cells for regenerative medicine: advances in the engineering of tissues and organs. Naturwissenschaften, 2002, 89(8): 338-351.
16.	Moreno-Manzano V, Zaytseva-Zotova D, López-Mocholí E, et al. Injectable gel form of a decellularized bladder induces adipose-derived stem cell differentiation into smooth muscle cells in vitro. Int J Mol Sci, 2020, 21(22): 8608.
17.	Cross W R, Eardley I, Leese H J, et al. A biomimetic tissue from cultured normal human urothelial cells: analysis of physiological function. Am J Physiol Renal Physiol, 2005, 289(2): F459-F468.
18.	Lock L T, Laychock S G, Tzanakakis E S. Pseudoislets in stirred-suspension culture exhibit enhanced cell survival, propagation and insulin secretion. J Biotechnol, 2011, 151(3): 278-286.
19.	Feil G, Daum L, Amend B, et al. From tissue engineering to regenerative medicine in urology--the potential and the pitfalls. Adv Drug Deliv Rev, 2011, 63(4-5): 375-378.
20.	Seliktar D, Black R A, Vito R P, et al. Dynamic mechanical conditioning of collagen-gel blood vessel constructs induces remodeling in vitro. Ann Biomed Eng, 2000, 28(4): 351-362.
21.	Riehl B D, Park J H, Kwon I K, et al. Mechanical stretching for tissue engineering: two-dimensional and three-dimensional constructs. Tissue Eng Part B Rev, 2012, 18(4): 288-300.
22.	Karbassi E, Fenix A, Marchiano S, et al. Cardiomyocyte maturation: advances in knowledge and implications for regenerative medicine. Nat Rev Cardiol, 2020, 17(6): 341-359.
23.	Orsola A, Estrada C R, Nguyen H T, et al. Growth and stretch response of human exstrophy bladder smooth muscle cells: molecular evidence of normal intrinsic function. BJU Int, 2005, 95(1): 144-148.
24.	Farhat W A, Yeger H. Does mechanical stimulation have any role in urinary bladder tissue engineering?. World J Urol, 2008, 26(4): 301-305.
25.	Chen L, Wei T Q, Wang Y, et al. Simulated bladder pressure stimulates human bladder smooth muscle cell proliferation via the PI3K/SGK1 signaling pathway. J Urol, 2012, 188(2): 661-667.
26.	Wei T Q, Luo D Y, Chen L, et al. Cyclic hydrodynamic pressure induced proliferation of bladder smooth muscle cells via integrin alpha5 and FAK. Physiol Res, 2014, 63(1): 127-134.
27.	Wu T, Chen L, Wei T, et al. Effect of cyclic hydrodynamic pressure-induced proliferation of human bladder smooth muscle through Ras-related C3 botulinum toxin substrate 1, mitogen-activated protein kinase kinase 1/2 and extracellular regulated protein kinases 1/2. Int J Urol, 2012, 19(9): 867-874.
28.	Sivaraman S, Ravishankar P, Rao R R. Differentiation and engineering of human stem cells for smooth muscle generation. Tissue Eng Part B Rev, 2023, 29(1): 1-9.
29.	Hwang Y, Cha S H, Kim D, et al. Combination of PD98059 and TGF-β1 efficiently differentiates human urine-derived stem cells into smooth muscle cells. Int J Mol Sci, 2021, 22(19): 10532.
30.	Sobue K, Hayashi K, Nishida W. Expressional regulation of smooth muscle cell-specific genes in association with phenotypic modulation. Molecular and Cellular Biochemistry, 1999, 190(1-2): 105-118.
31.	Sulistyowati E, Hsu J H, Lee S J, et al. Potential actions of baicalein for preventing vascular calcification of smooth muscle cells in vitro and in vivo. Int J Mol Sci, 2022, 23(10): 5673.
32.	Chen G, Chen S, Di X, et al. Survivin knockdown alleviates pathological hydrostatic pressure-induced bladder smooth muscle cell dysfunction and BOO-induced bladder remodeling via autophagy. Front Cell Dev Biol, 2022, 10: 999547.
33.	Doyle A E. Hypertension and vascular disease. Am J Hypertens, 1991, 4(2): 103-106.
34.	Kokubo Y, Matsumoto C. Hypertension is a risk factor for several types of heart disease: review of prospective studies. Adv Exp Med Biol, 2017, 956: 419-426.
35.	Stover J, Nagatomi J. Cyclic pressure stimulates DNA synthesis through the PI3K/Akt signaling pathway in rat bladder smooth muscle cells. Ann Biomed Eng, 2007, 35(9): 1585-1594.

1. Lichtenberg A, Cebotari S, Tudorache I, et al. Flow-dependent re-endothelialization of tissue-engineered heart valves. J Heart Valve Dis, 2006, 15(2): 287-294.
2. Lichtenberg A, Tudorache I, Cebotari S, et al. Preclinical testing of tissue-engineered heart valves re-endothelialized under simulated physiological conditions. Circulation, 2006, 114(1 Suppl): 1559-1565.
3. Izadpanah P, Golchin A, Firuzyar T, et al. The effect of shear stress on cardiac differentiation of mesenchymal stem cells. Mol Biol Rep, 2022, 49(4): 3167-3175.
4. Nicolaides K H, Rosen D, Rabinowitz R, et al. Urine production and bladder function in fetuses with open spina bifida. Fetal Ther, 1988, 3(3): 135-140.
5. Coplen D E, Macarak E J, Levin R M. Developmental changes in normal fetal bovine whole bladder physiology. J Urol, 1994, 151(5): 1391-1395.
6. Wei W, Howard P S, Kogan B, et al. Urinary diversion results in marked decreases in proliferation and apoptosis in fetal bladder. J Urol, 2012, 188(4): 1306-1312.
7. Siddiqui H B, Dogru S, Lashkarinia S S, et al. Soft-tissue material properties and mechanogenetics during cardiovascular development. J Cardiovasc Dev Dis, 2022, 9(2): 64.
8. Jahanbakhsh A, Nourbakhsh M S, Bonakdar S, et al. Evaluation of alginate modification effect on cell-matrix interaction, mechanotransduction and chondrogenesis of encapsulated MSCs. Cell Tissue Res, 2020, 381(2): 255-272.
9. Elashry M I, Baulig N, Wagner A S, et al. Combined macromolecule biomaterials together with fluid shear stress promote the osteogenic differentiation capacity of equine adipose-derived mesenchymal stem cells. Stem Cell Res Ther, 2021, 12(1): 116.
10. Atala A. Tissue engineering of human bladder. Br Med Bull, 2011, 97: 81-104.
11. Tiemessen D, de Jonge P, Daamen W, et al. The effect of a cyclic uniaxial strain on urinary bladder cells. World J Urol, 2017, 35(10): 1531-1539.
12. Davis N F, Mooney R, Piterina A V, et al. Construction and evaluation of urinary bladder bioreactor for urologic tissue-engineering purposes. Urology, 2011, 78(4): 954-960.
13. Gao X, Wei T, Liao B, et al. Physiological stretch induced proliferation of human urothelial cells via integrin alpha6-FAK signaling pathway. Neurourol Urodyn, 2018, 37(7): 2114-2120.
14. Luo D Y, Wazir R, Tian Y, et al. Integrin αv mediates contractility whereas integrin α4 regulates proliferation of human bladder smooth muscle cells via FAK pathway under physiological stretch. J Urol, 2013, 190(4): 1421-1429.
15. Ringe J, Kaps C, Burmester G R, et al. Stem cells for regenerative medicine: advances in the engineering of tissues and organs. Naturwissenschaften, 2002, 89(8): 338-351.
16. Moreno-Manzano V, Zaytseva-Zotova D, López-Mocholí E, et al. Injectable gel form of a decellularized bladder induces adipose-derived stem cell differentiation into smooth muscle cells in vitro. Int J Mol Sci, 2020, 21(22): 8608.
17. Cross W R, Eardley I, Leese H J, et al. A biomimetic tissue from cultured normal human urothelial cells: analysis of physiological function. Am J Physiol Renal Physiol, 2005, 289(2): F459-F468.
18. Lock L T, Laychock S G, Tzanakakis E S. Pseudoislets in stirred-suspension culture exhibit enhanced cell survival, propagation and insulin secretion. J Biotechnol, 2011, 151(3): 278-286.
19. Feil G, Daum L, Amend B, et al. From tissue engineering to regenerative medicine in urology--the potential and the pitfalls. Adv Drug Deliv Rev, 2011, 63(4-5): 375-378.
20. Seliktar D, Black R A, Vito R P, et al. Dynamic mechanical conditioning of collagen-gel blood vessel constructs induces remodeling in vitro. Ann Biomed Eng, 2000, 28(4): 351-362.
21. Riehl B D, Park J H, Kwon I K, et al. Mechanical stretching for tissue engineering: two-dimensional and three-dimensional constructs. Tissue Eng Part B Rev, 2012, 18(4): 288-300.
22. Karbassi E, Fenix A, Marchiano S, et al. Cardiomyocyte maturation: advances in knowledge and implications for regenerative medicine. Nat Rev Cardiol, 2020, 17(6): 341-359.
23. Orsola A, Estrada C R, Nguyen H T, et al. Growth and stretch response of human exstrophy bladder smooth muscle cells: molecular evidence of normal intrinsic function. BJU Int, 2005, 95(1): 144-148.
24. Farhat W A, Yeger H. Does mechanical stimulation have any role in urinary bladder tissue engineering?. World J Urol, 2008, 26(4): 301-305.
25. Chen L, Wei T Q, Wang Y, et al. Simulated bladder pressure stimulates human bladder smooth muscle cell proliferation via the PI3K/SGK1 signaling pathway. J Urol, 2012, 188(2): 661-667.
26. Wei T Q, Luo D Y, Chen L, et al. Cyclic hydrodynamic pressure induced proliferation of bladder smooth muscle cells via integrin alpha5 and FAK. Physiol Res, 2014, 63(1): 127-134.
27. Wu T, Chen L, Wei T, et al. Effect of cyclic hydrodynamic pressure-induced proliferation of human bladder smooth muscle through Ras-related C3 botulinum toxin substrate 1, mitogen-activated protein kinase kinase 1/2 and extracellular regulated protein kinases 1/2. Int J Urol, 2012, 19(9): 867-874.
28. Sivaraman S, Ravishankar P, Rao R R. Differentiation and engineering of human stem cells for smooth muscle generation. Tissue Eng Part B Rev, 2023, 29(1): 1-9.
29. Hwang Y, Cha S H, Kim D, et al. Combination of PD98059 and TGF-β1 efficiently differentiates human urine-derived stem cells into smooth muscle cells. Int J Mol Sci, 2021, 22(19): 10532.
30. Sobue K, Hayashi K, Nishida W. Expressional regulation of smooth muscle cell-specific genes in association with phenotypic modulation. Molecular and Cellular Biochemistry, 1999, 190(1-2): 105-118.
31. Sulistyowati E, Hsu J H, Lee S J, et al. Potential actions of baicalein for preventing vascular calcification of smooth muscle cells in vitro and in vivo. Int J Mol Sci, 2022, 23(10): 5673.
32. Chen G, Chen S, Di X, et al. Survivin knockdown alleviates pathological hydrostatic pressure-induced bladder smooth muscle cell dysfunction and BOO-induced bladder remodeling via autophagy. Front Cell Dev Biol, 2022, 10: 999547.
33. Doyle A E. Hypertension and vascular disease. Am J Hypertens, 1991, 4(2): 103-106.
34. Kokubo Y, Matsumoto C. Hypertension is a risk factor for several types of heart disease: review of prospective studies. Adv Exp Med Biol, 2017, 956: 419-426.
35. Stover J, Nagatomi J. Cyclic pressure stimulates DNA synthesis through the PI3K/Akt signaling pathway in rat bladder smooth muscle cells. Ann Biomed Eng, 2007, 35(9): 1585-1594.

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Biological function of bladder smooth muscle cells regulated by multi-modal biomimetic stress

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