Urine-derived stem cells: applications in skin, bone and articular cartilage repair

Wenqian Zhang; Jungen Hu; Yizhou Huang; Chenyu Wu; Huiqi Xie

doi:10.1093/burnst/tkab039

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Urine-derived stem cells: applications in skin, bone and articular cartilage repair

更新时间：2022-06-14

- Urine-derived stem cells: applications in skin, bone and articular cartilage repair
- Urine-derived stem cells: applications in skin, bone and articular cartilage repair
- Burns & Trauma 2021年9卷第1期
- 作者机构：
  
  1. Laboratory of Stem Cell and Tissue Engineering
  2. West China Hospital, Sichuan University
- 作者简介：
- 基金信息：
  
  This work was financially supported by National Natural Science Foundation of China (Grant No. 31771065), the 1.3.5 Project for Disciplines of Excellence, West China Hospital, Sichuan University (Grant No. ZYJC18002).
- DOI：10.1093/burnst/tkab039
  中图分类号：
- 纸质出版日期：2021，
  
  网络出版日期：2021-11-26，
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Wenqian Zhang, Jungen Hu, Yizhou Huang, 等. Urine-derived stem cells: applications in skin, bone and articular cartilage repair[J]. Burns & Trauma, 2021,9(1).

Wenqian Zhang, Jungen Hu, Yizhou Huang, Chenyu Wu, Huiqi Xie, Urine-derived stem cells: applications in skin, bone and articular cartilage repair, Burns & Trauma, Volume 9, 2021, tkab039, https://doi.org/10.1093/burnst/tkab039
Wenqian Zhang, Jungen Hu, Yizhou Huang, 等. Urine-derived stem cells: applications in skin, bone and articular cartilage repair[J]. Burns & Trauma, 2021,9(1). DOI： 10.1093/burnst/tkab039.

Wenqian Zhang, Jungen Hu, Yizhou Huang, Chenyu Wu, Huiqi Xie, Urine-derived stem cells: applications in skin, bone and articular cartilage repair, Burns & Trauma, Volume 9, 2021, tkab039, https://doi.org/10.1093/burnst/tkab039 DOI：

摘要

Abstract

As an emerging type of adult stem cell featuring non-invasive acquisition

urine-derived stem cells (USCs) have shown great potential for applications in tissue engineering and regenerative medicine. With a growing amount of research on the topic

the effectiveness of USCs in various disease models has been shown and the underlying mechanisms have also been explored

though many aspects still remain unclear. In this review

we aim to provide an up-to-date overview of the biological characteristics of USCs and their applications in skin

bone and articular cartilage repair. In addition to the identification procedure of USCs

we also summarize current knowledge of the underlying repair mechanisms and application modes of USCs. Potential concerns and perspectives have also been summarized.

关键词

Keywords

Urine-derived stem cellsskinBoneArticular cartilageTissue engineeringCell therapy

references

1.Gabbe BJ, Braaf S, Fitzgerald M, Judson R, Harrison JE, Lyons RA, et al. RESTORE: REcovery after serious trauma - outcomes, resource use and patient experiences study protocol. Inj Prev. 2015;21:348–54.

2.Peck MD. Epidemiology of burns throughout the world. Part I: distribution and risk factors. Burns. 2011;37:1087–100.

3.Sen CK, Gordillo GM, Roy S, Kirsner R, Lambert L, Hunt TK, et al. Human skin wounds: a major and snowballing threat to public health and the economy. Wound Repair Regen. 2009;17:763–71.

4.Snippert HJ, Clevers H. Tracking adult stem cells. EMBO Rep. 2011;12:113–22.

5.Park YB, Ha CW, Lee CH, Yoon YC, Park YG. Cartilage regeneration in osteoarthritic patients by a composite of allogeneic umbilical cord blood-derived mesenchymal stem cells and hyaluronate hydrogel: results from a clinical trial for safety and proof-of concept with 7 years of extended follow-up. Stem Cells Transl Med. 2016;5:1–6.

6.Childs PG, Reid S, Salmeron SM, Dalby MJ. Hurdles to uptake of mesenchymal stem cells and their progenitors in therapeutic products. Biochem J. 2020;477:3349–66.

7.Vagnozzi RJ, Maillet M, Sargent MA, Khalil H, Johansen AK, Schwanekamp JA, et al. An acute immune response underlies the benefit of cardiac stem-cell therapy. Nature. 2019;577:405–9.

8.Spees JL, Lee RH, Gregory CA. Mechanisms of mesenchymal stem/stromal cell function. Stem Cell Res Ther. 2016;7:125–37.

9.Witzgall R. Are renal proximal tubular epithelial cells constantly prepared for an emergency? Focus on “the proliferation capacity of the renal proximal tubule involves the bulk of differentiated epithelial cells”. Am J Physiol Cell Physiol. 2008;294:C1–3.

10.Ingelfinger JR. Nephrogenic adenomas as renal tubular outposts. N Engl J Med. 2002;347:684–6.

11.Dörrenhaus A, Müller JIF, Golka K, Jedrusik P, Schulze H, Föllmann WJ. Cultures of exfoliated epithelial cells from different locations of the human urinary tract and the renal tubular system. Arch Toxicol. 2000;74:618–26.

12.Zhang Y, McNeill E, Tian H, Soker S, Andersson KE, Yoo JJ, et al. Urine derived cells are a potential source for urological tissue reconstruction. J Urol. 2008;180:2226–33.

13.Staack A, Hayward SW, Baskin LS, Cunha GR. Molecular, cellular and developmental biology of urothelium as a basis of bladder regeneration. Differentiation. 2005;73:121–33.

14.Khandelwal P, Abraham SN, Apodaca G. Cell biology and physiology of the uroepithelium. Am J Physiol-Renal. 2009;297:1477–501.

15.Wu R, Liu G, Fan Y, Rohozinski J, Lu X, Rodriguez G, et al. 249 human urine-derived stem cells originate from parietal stem cells. J Urol. 2013;189:103.

16.Chen AJ, Pi JK, Hu JG, Huang YZ, Gao HW, Li SF, et al. Identification and characterization of two morphologically distinct stem cell subpopulations from human urine samples. Sci China Life Sci. 2020;63:712–23.

17.Bharadwaj S, Liu G, Shi Y, Wu R, Yang B, He T, et al. Multipotential differentiation of human urine-derived stem cells: potential for therapeutic applications in urology. Stem Cells. 2013;31:1840–56.

18.Ouyang B, Sun X, Han D, Chen S, Yao B, Gao Y, et al. Human urine-derived stem cells alone or genetically-modified with FGF2 improve type 2 diabetic erectile dysfunction in a rat model. PLoS One. 2014;9:e92825.

19.Burdeyron P, Giraud S, Hauet T, Steichen C. Urine-derived stem/progenitor cells: a focus on their characterization and potential. World J Stem Cells. 2020;12:1080–96.

20.Liu G, Pareta RA, Wu R, Shi Y, Zhou X, Liu H, et al. Skeletal myogenic differentiation of urine-derived stem cells and angiogenesis using microbeads loaded with growth factors. Biomaterials. 2013;34:1311–26.

21.Lang R, Liu G, Shi Y, Bharadwaj S, Leng X, Zhou X, et al. Self-renewal and differentiation capacity of urine-derived stem cells after urine preservation for 24 hours. PLoS One. 2013;8:e53980.

22.Liu G, Wu R, Yang B, Deng C, Lu X, Walker SJ, et al. Human urine-derived stem cell differentiation to endothelial cells with barrier function and nitric oxide production. Stem Cells Transl Med. 2018;7:686–98.

23.Wan Q, Xiong G, Liu G, Shupe TD, Wei G, Zhang D, et al. Urothelium with barrier function differentiated from human urine-derived stem cells for potential use in urinary tract reconstruction. Stem Cell Res Ther. 2018;9:304–16.

24.Li X, Liao J, Su X, Li W, Bi Z, Wang J, et al. Human urine-derived stem cells protect against renal ischemia/reperfusion injury in a rat model via exosomal miR-146a-5p which targets IRAK1. Theranostics. 2020;10:9561–78.

25.Zhang D, Wei G, Li P, Zhou X, Zhang Y. Urine-derived stem cells: a novel and versatile progenitor source for cell-based therapy and regenerative medicine. Genes Dis. 2014;1:8–17.

26.Rahman MS, Wruck W, Spitzhorn LS, Nguyen L, Bohndorf M, Martins S, et al. The FGF, TGFβ and WNT axis modulate self-renewal of human SIX2+ urine derived renal progenitor cells. Sci Rep-UK. 2020;10:739–54.

27.Hwang YH, Cha SH, Hong Y, Jung AR, Jun HS. Direct differentiation of insulin-producing cells from human urine-derived stem cells. Int J Med Sci. 2019;16:1668–76.

28.Wu S, Liu Y, Bharadwaj S, Atala A, Zhang Y. Human urine-derived stem cells seeded in a modified 3D porous small intestinal submucosa scaffold for urethral tissue engineering. Biomaterials. 2011;32:1317–26.

29.Bodin A, Bharadwaj S, Wu S, Gatenholm P, Atala A, Zhang Y. Tissue-engineered conduit using urine-derived stem cells seeded bacterial cellulose polymer in urinary reconstruction and diversion. Biomaterials. 2010;31:8889–901.

30.Wu S, Wang Z, Bharadwaj S, Hodges SJ, Atala A, Zhang Y. Implantation of autologous urine derived stem cells expressing vascular endothelial growth factor for potential use in genitourinary reconstruction. J Urol. 2011;186:640–7.

31.Wu R, Huang C, Wu Q, Jia X, Liu M, Xue Z, et al. Exosomes secreted by urine-derived stem cells improve stress urinary incontinence by promoting repair of pubococcygeus muscle injury in rats. Stem Cell Res Ther. 2019;10:80–92.

32.Liu G, Wang X, Sun X, Deng C, Atala A, Zhang Y. The effect of urine-derived stem cells expressing VEGF loaded in collagen hydrogels on myogenesis and innervation following after subcutaneous implantation in nude mice. Biomaterials. 2013;34:8617–29.

33.Zhang C, Luo D, Li T, Yang Q, Xie Y, Chen H, et al. Transplantation of human urine-derived stem cells ameliorates erectile function and cavernosal endothelial function by promoting autophagy of corpus cavernosal endothelial cells in diabetic erectile dysfunction rats. Stem Cells Int. 2019;2019:2168709.

34.Sun B, Luo X, Yang C, Liu P, Yang Y, Dong X, et al. Therapeutic effects of human urine-derived stem cells in a rat model of cisplatin-induced acute kidney injury in vivo and in vitro. Stem Cells Int. 2019;2019:1–13.

35.Zhang C, George SK, Wu R, Thakker PU, Abolbashari M, Kim TH, et al. Reno-protection of urine-derived stem cells in a chronic kidney disease rat model induced by renal ischemia and nephrotoxicity. Int J Biol Sci. 2020;16:435–46.

36.Dong X, Zhang T, Liu Q, Zhu J, Zhao J, Li J, et al. Beneficial effects of urine-derived stem cells on fibrosis and apoptosis of myocardial, glomerular and bladder cells. Mol Cell Endocrinol. 2016;427:21–32.

37.Zhao T, Luo D, Sun Y, Niu X, Wang Y, Wang C, et al. Human urine-derived stem cells play a novel role in the treatment of STZ-induced diabetic mice. J Mol Histol. 2018;49:419–28.

38.Duan YR, Chen BP, Chen F, Yang SX, Zhu CY, Ma YL, et al. Exosomal microRNA-16-5p from human urine-derived stem cells ameliorates diabetic nephropathy through protection of podocyte. J Cell Mol Med. 2019;00:1–16.

39.Xiong G, Tao L, Ma WJ, Gong MJ, Zhao L, Shen LJ, et al. Urine-derived stem cells for the therapy of diabetic nephropathy mouse model. Eur Rev Med Pharmacol Sci. 2020;24:1316–24.

40.Hu C, He Y, Fang S, Tian N, Gong M, Xu X, et al. Urine-derived stem cells accelerate the recovery of injured mouse hepatic tissue. Am J Transl Res. 2020;12:5131–50.

41.Zhou C, Wu XR, Liu HS, Liu XH, Liu GH, Zheng XB, et al. Immunomodulatory effect of urine-derived stem cells on inflammatory bowel diseases via downregulating Th1/Th17 immune responses in a PGE2-dependent manner. J Crohns Colitis. 2020;14:654–68.

42.Guan JJ, Niu X, Gong FX, Hu B, Guo SC, Lou YL, et al. Biological characteristics of human-urine-derived stem cells: potential for cell-based therapy in neurology. Tissue Eng Part A. 2014;20:1794–806.

43.Chen CY, Du W, Rao SS, Tan YJ, Hu XK, Luo MJ, et al. Extracellular vesicles from human urine-derived stem cells inhibit glucocorticoid-induced osteonecrosis of the femoral head by transporting and releasing pro-angiogenic DMBT1 and anti-apoptotic TIMP1. Acta Biomater. 2020;111:208–20.

44.Guan J, Zhang J, Guo S, Zhu H, Zhu Z, Li H, et al. Human urine-derived stem cells can be induced into osteogenic lineage by silicate bioceramics via activation of the Wnt/β-catenin signaling pathway. Biomaterials. 2015;55:1–11.

45.Guan J, Zhang J, Li H, Zhu Z, Guo S, Niu X, et al. Human urine derived stem cells in combination with beta-TCP can be applied for bone regeneration. PLoS One. 2015;10:e0125253.

46.Chen L, Li L, Xing F, Peng J, Peng K, Wang Y, et al. Human urine-derived stem cells: potential for cell-based therapy of cartilage defects. Stem Cells Int. 2018;2018:1–14.

47.Fu Y, Guan J, Guo S, Guo F, Niu X, Liu Q, et al. Human urine-derived stem cells in combination with polycaprolactone/gelatin nanofibrous membranes enhance wound healing by promoting angiogenesis. J Transl Med. 2014;12:274–87.

48.Zhou T, Benda C, Duzinger S, Huang Y, Li X, Li Y, et al. Generation of induced pluripotent stem cells from urine. J Am Soc Nephrol. 2011;22:1221–8.

49.Jiang YF, Chen M, Zhang NN, Yang HJ, Rui Q, Zhou YF. In vitro and in vivo differentiation of induced pluripotent stem cells generated from urine-derived cells into cardiomyocytes. Biol Open. 2018;7:bio029157.

50.Cai J, Zhang Y, Liu P, Chen S, Wu X, Sun Y, et al. Generation of tooth-like structures from integration-free human urine induced pluripotent stem cells. Cell Regen. 2013;2:6.

51.Jia B, Chen S, Zhao Z, Liu P, Cai J, Qin D, et al. Modeling of hemophilia a using patient-specific induced pluripotent stem cells derived from urine cells. Life Sci. 2014;108:22–9.

52.Lee YM, Zampieri BL, Scott-McKean JJ, Johnson MW, Costa ACS. Generation of integration-free induced pluripotent stem cells from urine-derived cells isolated from individuals with down syndrome. Stem Cells Transl Med. 2017;6:1465–76.

53.Ruiz-Babot G, Balyura M, Hadjidemetriou I, Ajodha SJ, Taylor DR, Ghataore L, et al. Modeling congenital adrenal hyperplasia and testing interventions for adrenal insufficiency using donor-specific reprogrammed cells. Cell Rep. 2018;22:1236–49.

54.Li G, Xie B, He L, Zhou T, Gao G, Liu S, et al. Generation of retinal organoids with mature rods and cones from urine-derived human induced pluripotent stem cells. Stem Cells Int. 2018;2018:1–12.

55.Sun G, Ding B, Wan M, Chen L, Jackson J, Atala A. Formation and optimization of three-dimensional organoids generated from urine-derived stem cells for renal function in vitro. Stem Cell Res Ther. 2020;11:309–20.

56.Tang L, Wang H, Dai B, Wang X, Zhou D, Shen J, et al. Human induced pluripotent stem cell-derived cardiomyocytes reveal abnormal TGFβ signaling in type 2 diabetes mellitus. J Mol Cell Cardiol. 2020;142:53–64.

57.Liu W, Zhang P, Tan J, Lin Y. Differentiation of urine-derived induced pluripotent stem cells to neurons, astrocytes, and microvascular endothelial cells from a diabetic patient. Cell Reprogram. 2020;22:147–55.

58.Ouyang B, Xie Y, Zhang C, Deng C, Lv L, Yao J, et al. Extracellular vesicles from human urine-derived stem cells ameliorate erectile dysfunction in a diabetic rat model by delivering proangiogenic microRNA. Sex Med. 2019;7:241–50.

59.Zhu Q, Li Q, Niu X, Zhang G, Ling X, Zhang J, et al. Extracellular vesicles secreted by human urine-derived stem cells promote ischemia repair in a mouse model of hind-limb ischemia. Cell Physiol Biochem. 2018;47:1181–92.

60.Jiang ZZ, Liu YM, Niu X, Yin JY, Hu B, Guo SC, et al. Exosomes secreted by human urine-derived stem cells could prevent kidney complications from type I diabetes in rats. Stem Cell Res Ther. 2016;7:24–36.

61.Chen CY, Rao SS, Ren L, Hu XK, Tan YJ, Hu Y, et al. Exosomal DMBT1 from human urine-derived stem cells facilitates diabetic wound repair by promoting angiogenesis. Theranostics. 2018;8:1607–23.

62.Deng C, Xie Y, Zhang C, Ouyang B, Chen H, Lv L, et al. Urine-derived stem cells facilitate endogenous spermatogenesis restoration of Busulfan-induced nonobstructive azoospermic mice by paracrine exosomes. Stem Cells Dev. 2019;28:1322–33.

63.Chen CY, Rao SS, Tan YJ, Luo MJ, Hu XK, Yin H, et al. Extracellular vesicles from human urine-derived stem cells prevent osteoporosis by transferring CTHRC1 and OPG. Bone Res. 2019;7:18–31.

64.Pei M, Li J, Zhang Y, Liu G, Wei L, Zhang Y. Expansion on a matrix deposited by nonchondrogenic urine stem cells strengthens the chondrogenic capacity of repeated-passage bone marrow stromal cells. Cell Tissue Res. 2014;356:391–403.

65.Li J, Narayanan K, Zhang Y, Hill RC, He F, Hansen KC, et al. Role of lineage-specific matrix in stem cell chondrogenesis. Biomaterials. 2020;231:119681.

66.Wu C, Chen L, Huang YZ, Huang Y, Parolini O, Zhong Q, et al. Comparison of the proliferation and differentiation potential of human urine-, placenta decidua basalis-, and bone marrow-derived stem cells. Stem Cells Int. 2018;2018:1–11.

67.Kim K, Gil M, Dayem AA, Choi S, Kang GH, Yang GM, et al. Improved isolation and culture of urine-derived stem cells (USCs) and enhanced production of immune cells from the USC-derived induced pluripotent stem cells. J Clin Med. 2020;9:827–52.

68.Kang HS, Choi SH, Kim BS, Park GB, Kwon TG, Chun SY. Advanced properties of urine derived stem cells compared to adipose tissue derived stem cells in terms of cell proliferation, immune modulation and multi differentiation. J Korean Med Sci. 2015;30:1764–76.

69.Sun JC, Xing F, Zou M, Gong M, Li L, Xiang Z. Comparison of chondrogenesis-related biological behaviors between human urine derived stem cells and human bone marrow mesenchymal stem cells from the same individual. Stem Cell Res Ther. 2021;12:366–84.

70.Gabrielyan A, Neumann E, Gelinsky M, Wolff AR. Metabolically conditioned media derived from bone marrow stromal cells or human skin fibroblasts act as effective chemoattractants for mesenchymal stem cells. Stem Cell Res Ther. 2017;8:212–21.

71.Mathes SH, Ruffner H, Graf-Hausner U. The use of skin models in drug development. Adv Drug Deliv Rev. 2014;69-70:81–102.

72.Nejati R, Kovacic D, Slominski A. Neuro-immune-endocrine functions of the skin: an overview. Expert Rev Dermatol. 2013;8:581–3.

73.Sun BK, Siprashvili Z, Khavari PA. Advances in skin grafting and treatment of cutaneous wounds. Science. 2014;346:941–5.

74.Shpichka A, Butnaru D, Bezrukov EA, Sukhanov RB, Atala A, Burdukovskii V, et al. Skin tissue regeneration for burn injury. Stem Cell Res Ther. 2019;10:94.

75.Guo JM, Hu HD, Gorecka J, Bai HL, He H, Assi R, et al. Adipose-derived mesenchymal stem cells accelerate diabetic wound healing in a similar fashion as bone marrow-derived cells. Am J Physiol Cell Physiol. 2018;315:C885–96.

76.Chen SX, Shi JB, Zhang M, Chen YH, Wang XE, Zhang L, et al. Mesenchymal stem cell-laden anti-inflammatory hydrogel enhances diabetic wound healing. Sci Rep. 2015;5:1–12.

77.Lataillade JJ, Doucet C, Bey E, Carsin H, Huet C, Clairand I, et al. New approach to radiation burn treatment by dosimetry-guided surgery combined with autologous mesenchymal stem cell therapy. Regen Med. 2007;2:785–94.

78.Xu HJ, Huang SH, Wang JJ, Lan Y, Feng LB, Zhu MS, et al. Enhanced cutaneous wound healing by functional injectable thermo-sensitive chitosan-based hydrogel encapsulated human umbilical cord-mesenchymal stem cells. Int J Biol Macromol. 2019;137:433–41.

79.Wang HF, Chen LY, Liu Y, Luo BZ, Xie NZ, Tan T, et al. Implantation of placenta-derived mesenchymal stem cells accelerates murine dermal wound closure through immunomodulation. Am J Transl Res. 2016;8:4912–21.

80.Zhang YL, Niu X, Dong X, Wang Y, Li HY. Bioglass enhanced wound healing ability of urine-derived stem cells through promoting paracrine effects between stem cells and recipient cells. J Tissue Eng Regen Med. 2018;12:E1609–22.

81.Cao YM, Liu MY, Xue ZW, Qiu Y, Li J, Wang Y, et al. Surface-structured bacterial cellulose loaded with hUSCs accelerate skin wound healing by promoting angiogenesis in rats. Biochem Biophys Res Commun. 2019;516:1167–74.

82.Zhang XR, Huang YZ, Gao HW, Jiang YL, Hu JG, Pi JK, et al. Hypoxic preconditioning of human urine-derived stem cell-laden small intestinal submucosa enhances wound healing potential. Stem Cell Res Ther. 2020;11:150–62.

83.Walmsley GG, Ransom RC, Zielins ER, Leavitt T, Flacco JS, Hu MS, et al. Stem cells in bone regeneration. Stem Cell Rev Rep. 2016;12:524–9.

84.Clarke B. Normal bone anatomy and physiology. Clin J Am Soc Nephrol. 2008;3:S131–9.

85.Li Y, Chen SK, Li L, Qin L, Wang XL, Lai YX. Bone defect animal models for testing efficacy of bone substitute biomaterials. J Orthop Transl. 2015;3:95–104.

86.El-Rashidy AA, Roether JA, Harhaus L, Kneser U, Boccaccini AR. Regenerating bone with bioactive glass scaffolds: a review of in vivo studies in bone defect models. Acta Biomater. 2017;62:1–28.

87.Zhang K, Fan Y, Dunne N, Li X. Effect of microporosity on scaffolds for bone tissue engineering. Regen Biomater. 2018;5:115–24.

88.Huang Y, Deng H, Fan Y, Zheng L, Che J, Li X, et al. Conductive nanostructured Si biomaterials enhance osteogeneration through electrical stimulation. Mater Sci Eng C. 2019;103:109748.

89.Kasten P, Luginbuhl R, van Griensven M, Barkhausen T, Krettek C, Bohner M, et al. Comparison of human bone marrow stromal cells seeded on calcium-deficient hydroxyapatite, beta-tricalcium phosphate and demineralized bone matrix. Biomaterials. 2003;24:2593–603.

90.Salgado AJ, Coutinho OP, Reis RL. Bone tissue engineering: state of the art and future trends. Macromol Biosci. 2004;4:743–65.

91.Derubeis AR, Cancedda RJ. Bone marrow stromal cells (BMSCs) in bone engineering: limitations and recent advances. Ann Biomed Eng. 2004;32:160–5.

92.Bruder SP, Kraus KH, Goldberg VM, Kadiyala S. The effect of implants loaded with autologous mesenchymal stem cells on the healing of canine segmental bone defects. J Bone Joint Surg Am. 1998;80:985–96.

93.Xie HQ, Yang F, Deng L, Luo J, Qin T, Li X, et al. The performance of a bone-derived scaffold material in the repair of critical bone defects in a rhesus monkey model. Biomaterials. 2007;28:3314–24.

94.Xie HQ, Huang FG, Zhao YF, Qin TW, Li XQ, Liu C, et al. Tissue-engineered ribs for chest wall reconstruction: a case with 12-year follow-up. Regen Med. 2014;9:431–6.

95.Storti G, Scioli MG, Kim BS, Orlandi A, Cervelli V. Adipose-derived stem cells in bone tissue engineering: useful tools with new applications. Stem Cells Int. 2019;2019:1–18.

96.Wang P, Liu X, Zhao L, Weir MD, Sun J, Chen W, et al. Bone tissue engineering via human induced pluripotent, umbilical cord and bone marrow mesenchymal stem cells in rat cranium. Acta Biomater. 2015;18:236–48.

97.Moshaverinia A, Chen C, Akiyama K, Xu X, Chee WW, Schricker SR, et al. Encapsulated dental-derived mesenchymal stem cells in an injectable and biodegradable scaffold for applications in bone tissue engineering. J Biomed Mater Res A. 2013;101:3285–94.

98.Qin H, Zhu C, An Z, Jiang Y, Zhao Y, Wang J, et al. Silver nanoparticles promote osteogenic differentiation of human urine-derived stem cells at noncytotoxic concentrations. Int J Nanomedicine. 2014;9:2469–78.

99.Guan J, Zhang J, Zhu Z, Niu X, Guo S, Wang Y, et al. Bone morphogenetic protein 2 gene transduction enhances the osteogenic potential of human urine-derived stem cells. Stem Cell Res Ther. 2015;6:5.

100.Sun X, Zheng W, Qian C, Wu Q, Hao Y, Lu G. Focal adhesion kinase promotes BMP2-induced osteogenic differentiation of human urinary stem cells via AMPK and Wnt signaling pathways. J Cell Physiol. 2020;235:4954–64.

101.Xing F, Li L, Sun J, Liu G, Duan X, Chen J, et al. Surface mineralized biphasic calcium phosphate ceramics loaded with urine-derived stem cells are effective in bone regeneration. J Orthop Surg Res. 2019;14:419–33.

102.Bhosale AM, Richardson JB. Articular cartilage: structure, injuries and review of management. Br Med Bull. 2008;87:77–95.

103.Makris EA, Gomoll AH, Malizos KN, Hu JC, Athanasiou KA. Repair and tissue engineering techniques for articular cartilage. Nat Rev Rheumatol. 2015;11:21–34.

104.Madeira C, Santhagunam A, Salgueiro JB, Cabral JMS. Advanced cell therapies for articular cartilage regeneration. Trends Biotechnol. 2015;33:35–42.

105.De Bari C, Roelofs AJ. Stem cell-based therapeutic strategies for cartilage defects and osteoarthritis. Curr Opin Pharmacol. 2018;40:74–80.

106.Yin H, Wang Y, Sun Z, Sun X, Xu Y, Li P, et al. Induction of mesenchymal stem cell chondrogenic differentiation and functional cartilage microtissue formation for in vivo cartilage regeneration by cartilage extracellular matrix-derived particles. Acta Biomater. 2016;33:96–109.

107.Qi Y, Du Y, Li W, Dai X, Zhao T, Yan W. Cartilage repair using mesenchymal stem cell (MSC) sheet and MSCs-loaded bilayer PLGA scaffold in a rabbit model. Knee Surg Sports Traumatol Arthrosc. 2014;22:1424–33.

108.Gao P, Han P, Jiang D, Yang S, Cui Q, Li Z. Effects of the donor age on proliferation, senescence and osteogenic capacity of human urine-derived stem cells. Cytotechnology. 2017;69:751–63.

109.Schosserer M, Reynoso R, Wally V, Jug B, Kantner V, Weilner S, et al. Urine is a novel source of autologous mesenchymal stem cells for patients with epidermolysis bullosa. BMC Res Notes. 2015;8:767–78.

110.Afzal MZ, Strande JL. Generation of induced pluripotent stem cells from muscular dystrophy patients: efficient integration-free reprogramming of urine derived cells. J Vis Exp. 2015;28:52032.

111.Liu Y, Ming L, Luo H, Liu W, Zhang Y, Liu H, et al. Integration of a calcined bovine bone and BMSC-sheet 3D scaffold and the promotion of bone regeneration in large defects. Biomaterials. 2013;34:9998–10006.

112.Badenes SM, Fernandes-Platzgummer A, Rodrigues CAV, Diogo MM, da Silva CL, Cabral JMS. Chapter 4 - Microcarrier culture systems for stem cell manufacturing. In: Cabral JMS, Lobato de Silva C, Chase LG, Margarida Diogo M (eds). Stem Cell Manufacturing. Boston:Elsevier, 2016, 77–104.

113.Chun SY, Kim HT, Kwon SY, Kim J, Kim BS, Yoo ES, et al. The efficacy and safety of collagen-I and hypoxic conditions in urine-derived stem cell ex vivo culture. Tissue Eng Regen Med. 2016;13:403–15.

114.Galipeau J, Krampera M, Barrett J, Dazzi F, Deans RJ, DeBruijn J, et al. International Society for Cellular Therapy perspective on immune functional assays for mesenchymal stromal cells as potency release criterion for advanced phase clinical trials. Cytotherapy. 2016;18:151–9.

115.Murray RZ, West ZE, Cowin AJ, Farrugia BL. Development and use of biomaterials as wound healing therapies. Burns Trauma. 2019;7:1–9.

116.Tan QW, Tang SL, Zhang Y, Yang JQ, Wang ZL, Xie HQ, et al. Hydrogel from acellular porcine adipose tissue accelerates wound healing by inducing intradermal adipocyte regeneration. J Invest Dermatol. 2019;139:455–63.

117.Liu G, Wu R, Yang B, Shi Y, Deng C, Atala A, et al. A cocktail of growth factors released from a heparin hyaluronic-acid hydrogel promotes the myogenic potential of human urine-derived stem cells in vivo. Acta Biomater. 2020;107:50–64.

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