Notch4 participates in mesenchymal stem cell-induced differentiation in 3D-printed matrix and is implicated in eccrine sweat gland morphogenesis

Yuzhen Wang; Fanliang Zhang; Bin Yao; Linhao Hou; Zhao Li; Wei Song; Yi Kong; Yaxin Tan; Xiaobing Fu; Sha Huang

doi:10.1093/burnst/tkad032

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Notch4 participates in mesenchymal stem cell-induced differentiation in 3D-printed matrix and is implicated in eccrine sweat gland morphogenesis

更新时间：2023-08-29

- Notch4 participates in mesenchymal stem cell-induced differentiation in 3D-printed matrix and is implicated in eccrine sweat gland morphogenesis
- Notch4 participates in mesenchymal stem cell-induced differentiation in 3D-printed matrix and is implicated in eccrine sweat gland morphogenesis
- Burns & Trauma 2023年11卷第1期
- 作者机构：
  
  1. Research Center for Tissue Repair and Regeneration affiliated to the Medical Innovation Research Department, Chinese PLA General Hospital
  2. Department of Burn and Plastic Surgery, Air Force Hospital of Chinese PLA Central Theater Command
  3. Academy of Medical Engineering and Translational Medicine, Tianjin University
  4. Department of Orthopedics, the Fourth Affiliated Hospital of China Medical University
  5. College of Graduate, Tianjin Medical University
- 作者简介：
- 基金信息：
  
  This study was supported by the National Nature Science Foundation of China (82002056, 32000969, 92268206), The general funding grants (2020 M673672) and the special funding grants (in-station, 2022 T150789) from the China Postdoctoral Science Foundation, the Military Medical Research Projects (145AKJ260015000X;2022-JCJQ-ZD-096-00), National key research and development program (2022YFA1104604), Key Support Program for Growth Factor Research (SZYZ-TR-03), the Science Fund for National Defense Distinguished Young Scholars (2022-JCJQ-ZQ-016), Youth Independent Innovation Science Fund Project of PLA General Hospital (22QNFC018).
- DOI：10.1093/burnst/tkad032
  中图分类号：
- 纸质出版日期：2023，
  
  网络出版日期：2023-6-29，
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Yuzhen Wang, Fanliang Zhang, Bin Yao, 等. Notch4 participates in mesenchymal stem cell-induced differentiation in 3D-printed matrix and is implicated in eccrine sweat gland morphogenesis[J]. Burns & Trauma, 2023,11(1).

Yuzhen Wang, Fanliang Zhang, Bin Yao, Linhao Hou, Zhao Li, Wei Song, Yi Kong, Yaxin Tan, Xiaobing Fu, Sha Huang, Notch4 participates in mesenchymal stem cell-induced differentiation in 3D-printed matrix and is implicated in eccrine sweat gland morphogenesis, Burns & Trauma, Volume 11, 2023, tkad032, https://doi.org/10.1093/burnst/tkad032
Yuzhen Wang, Fanliang Zhang, Bin Yao, 等. Notch4 participates in mesenchymal stem cell-induced differentiation in 3D-printed matrix and is implicated in eccrine sweat gland morphogenesis[J]. Burns & Trauma, 2023,11(1). DOI： 10.1093/burnst/tkad032.

Yuzhen Wang, Fanliang Zhang, Bin Yao, Linhao Hou, Zhao Li, Wei Song, Yi Kong, Yaxin Tan, Xiaobing Fu, Sha Huang, Notch4 participates in mesenchymal stem cell-induced differentiation in 3D-printed matrix and is implicated in eccrine sweat gland morphogenesis, Burns & Trauma, Volume 11, 2023, tkad032, https://doi.org/10.1093/burnst/tkad032 DOI：

摘要

Abstract

BackgroundEccrine sweat gland (SG) plays a crucial role in thermoregulation but exhibits very limited regenerative potential. Although SG lineage-restricted niches dominate SG morphogenesis and benefit SG regeneration

rebuilding niches in vivo is challenging for stem cell therapeutic applications. Hence

we attempted to screen and tune the critical niche-responding genes that dually respond to both biochemical and structural cues

which might be a promising strategy for SG regeneration.MethodsAn artificial SG lineage-restricted niche consisting of mouse plantar dermis homogenates (i.e. biochemical cues) and 3D architecture (i.e. structural cues) was built in vitro by using an extrusion-based 3D bioprinting approach. Mouse bone marrow-derived mesenchymal stem cells (MSCs) were then differentiated into the induced SG cells in the artificial SG lineage-restricted niche. To decouple biochemical cues from structural cues

the transcriptional changes aroused by pure biochemical cues

pure structural cues and synergistic effects of both cues were analyzed pairwise

respectively. Notably

only niche-dual-responding genes that are differentially expressed in response to both biochemical and structural cues and participate in switching MSC fates towards SG lineage were screened out. Validations in vitro and in vivo were respectively conducted by inhibiting or activating the candidate niche-dual-responding gene(s) to explore the consequent effects on SG differentiation.ResultsNotch4 is one of the niche-dual-responding genes that enhanced MSC stemness and promoted SG differentiation in 3D-printed matrix in vitro. Furthermore

inhibiting Notch4 specifically reduced keratin 19-positive epidermal stem cells and keratin 14-positive SG progenitor cells

thus further delaying embryonic SG morphogenesis in vivo.ConclusionsNotch4 not only participates in mouse MSC-induced SG differentiation in vitro but is also implicated in mouse eccrine SG morphogenesis in vivo.

关键词

Keywords

Mesenchymal stem cellsNotchStem cell–microenvironment interactionsStem cell plasticityDifferentiationSweat gland3D bioprintingRegeneration

references

1.Lu CP, Polak L, Rocha AS, Pasolli HA, Chen SC, Sharma N, et al. Identification of stem cell populations in sweat glands and ducts reveals roles in homeostasis and wound repair. Cell. 2012;150:136–50.

2.C.P. Lu, L. Polak, B.E. Keyes, E. Fuchs, Spatiotemporal antagonism in mesenchymal-epithelial signaling in sweat versus hair fate decision, Science (New York, N.Y.). 2016;354:6319.

3.Lu C, Fuchs E. Sweat gland progenitors in development, homeostasis, and wound repair. Cold Spring Harbor perspectives in medicine. 2014;4:2.

4.Wang R, Wang Y, Yao B, Hu T, Li Z, Liu Y, et al. Redirecting differentiation of mammary progenitor cells by 3D bioprinted sweat gland microenvironment. Burns Trauma. 2019;7:29.

5.Chee MK, Jo SK, Sohn KC, Kim CD, Lee JH, Lee YH. Effects of Brn2 overexpression on eccrine sweat gland development in the mouse paw. Biochem Biophys Res Commun. 2017;490:901–5.

6.Xie J, Yao B, Han Y, Shang T, Gao D, Yang S, et al. Cytokeratin expression at different stages in sweat gland development of C57BL/6J mice. Int J Low Extrem Wounds. 2015;14:365–71.

7.Scadden DT. The stem-cell niche as an entity of action. Nature. 2006;441:1075–9.

8.Morrison SJ, Spradling AC. Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell. 2008;132:598–611.

9.Nabhan AN, Brownfield DG, Harbury PB, Krasnow MA, Desai TJ. Single-cell Wnt signaling niches maintain stemness of alveolar type 2 cells. Science. 2018;359:1118–23.

10.Vining KH, Mooney DJ. Mechanical forces direct stem cell behaviour in development and regeneration. Nat Rev Mol Cell Biol. 2017;18:728–42.

11.Scadden DT. Nice neighborhood: emerging concepts of the stem cell niche. Cell. 2014;157:41–50.

12.Pinho S, Frenette PS. Haematopoietic stem cell activity and interactions with the niche. Nat Rev Mol Cell Biol. 2019;20:303–20.

13.Lei M, Schumacher LJ, Lai YC, Juan WT, Yeh CY, Wu P, et al. Self-organization process in newborn skin organoid formation inspires strategy to restore hair regeneration of adult cells. Proc Natl Acad Sci U S A. 2017;114:E7101–e7110.

14.Hosseini M, Koehler KR, Shafiee A. Biofabrication of human skin with its appendages. Advanced healthcare materials. 2022;11:22, e2201626.

15.Sun X, Xiang J, Chen R, Geng Z, Wang L, Liu Y, et al. Sweat gland organoids originating from reprogrammed epidermal keratinocytes functionally recapitulated damaged skin. Advanced science(Weinheim, Baden-Wurttemberg, Germany). 2021;8:e2103079.

16.Fu NY, Nolan E, Lindeman GJ, Visvader JE. Stem cells and the differentiation hierarchy in mammary gland development. Physiol Rev. 2020;100:489–523.

17.Zhang Y, Enhejirigala B, Yao Z, Li W, Song JL, Li J, et al. Using bioprinting and spheroid culture to create a skin model with sweat glands and hair follicles, burns. Trauma. 2021;9:tkab013.

18.Liu Y, Li J, Yao B, Wang Y, Wang R, Yang S, et al. The stiffness of hydrogel-based bioink impacts mesenchymal stem cells differentiation toward sweat glands in 3D-bioprinted matrix, materials science & engineering. C, Materials for biological applications. 2021;118:111387.

19.Ferraris C, Chevalier G, Favier B, Jahoda CA, Dhouailly D. Adult corneal epithelium basal cells possess the capacity to activate epidermal, pilosebaceous and sweat gland genetic programs in response to embryonic dermal stimuli. Development (Cambridge, England). 2000;127:5487–95.

20.Wang Y, Yao B, Duan X, Li J, Song W, Enhejirigala, et al. Notch1 down-regulation in lineage-restricted niches is involved in the development of mouse eccrine sweat glands. J Mol Histol. 2022;53:857–67.

21.Yao B, Wang R, Wang Y, Zhang Y, Hu T, Song W, et al. Biochemical and structural cues of 3D-printed matrix synergistically direct MSC differentiation for functional sweat gland regeneration. Sci Adv. 2020;6:eaaz1094.

22.Mohammed TA, Holen KD, Jaskula-Sztul R, Mulkerin D, Lubner SJ, Schelman WR, et al. A pilot phase II study of valproic acid for treatment of low-grade neuroendocrine carcinoma. Oncologist. 2011;16:835–43.

23.Tao ZS, Li TL, Xu HG, Yang M. Hydrogel contained valproic acid accelerates bone-defect repair via activating Notch signaling pathway in ovariectomized rats. Journal of materials science Materials in medicine. 2021;33:4.

24.Breuls N, Giarratana N, Yedigaryan L, Garrido GM, Carai P, Heymans S, et al. Valproic acid stimulates myogenesis in pluripotent stem cell-derived mesodermal progenitors in a NOTCH-dependent manner. Cell Death Dis. 2021;12:677.

25.Hu N, Zhang X, Zhang X, Guan Y, He R, Xue E, et al. Inhibition of Notch activity suppresses hyperglycemia-augmented polarization of macrophages to the M1 phenotype and alleviates acute pancreatitis. Clin Sci(London, England: 1979). 2022;136:455–71.

26.Wei J, Zhang L, Ren L, Zhang J, Yu Y, Wang J, et al. Endosulfan inhibits proliferation through the Notch signaling pathway in human umbilical vein endothelial cells. Environ Pollut(Barking, Essex : 1987). 2017;221:26–36.

27.Cheng X, Yu Z, Xu J, Quan D, Long H. Pathophysiological changes and the role of Notch-1 activation after decompression in a compressive spinal cord injury rat model. Front Neurosci. 2021;15:579431.

28.Ahmed AA, Robinson T, Palande M, Escara-Wilke J, Dai J, Keller ET. Targeted Notch1 inhibition with a Notch1 antibody, OMP-A2G1, decreases tumor growth in two murine models of prostate cancer in association with differing patterns of DNA damage response gene expression. J Cell Biochem. 2019;120:16946–55.

29.Zhou B, Lin W, Long Y, Yang Y, Zhang H, Wu K, et al. Notch signaling pathway: architecture, disease, and therapeutics. Signal transduction and targeted therapy. 2022;7:95.

30.González-García I, García-Clavé E, Cebrian-Serrano A, Thuc Le, Contreras RE, Xu Y, et al. Estradiol regulates leptin sensitivity to control feeding via hypothalamic Cited1. Cell Metab. 2023;35:438–455.e7.

31.Chen Z, Soni N, Pinero G, Giotti B, Eddins DJ, Lindblad KE, et al. Monocyte depletion enhances neutrophil influx and proneural to mesenchymal transition in glioblastoma. Nat Commun. 2023;14:1839.

32.Jin Y, Anbarchian T, Wu P, Sarkar A, Fish M, Peng WC, et al. Wnt signaling regulates hepatocyte cell division by a transcriptional repressor cascade. Proc Natl Acad Sci U S A. 2022;119:e2203849119.

33.Park SA, Lim YJ, Ku WL, Zhang D, Cui K, Tang LY, et al. Opposing functions of circadian protein DBP and atypical E2F family E2F8 in anti-tumor Th9 cell differentiation. Nat Commun. 2022;13:6069.

34.Isselbacher EM, Lino Cardenas CL, Lindsay ME. Hereditary influence in thoracic aortic aneurysm and dissection. Circulation. 2016;133:2516–28.

35.Li J, Xu X, Liu C, Xi X, Wang Y, Wu X, et al. miR-181a-2-3p stimulates gastric cancer progression via targeting MYLK. Frontiers in bioengineering and biotechnology. 2021;9:687915.

36.Kamberov YG, Wang S, Tan J, Gerbault P, Wark A, Tan L, et al. Modeling recent human evolution in mice by expression of a selected EDAR variant. Cell. 2013;152:691–702.

37.Cluzeau C, Hadj-Rabia S, Jambou M, Mansour S, Guigue P, Masmoudi S, et al. Only four genes (EDA1, EDAR, EDARADD, and WNT10A) account for 90% of hypohidrotic/anhidrotic ectodermal dysplasia cases. Hum Mutat. 2011;32:70–2.

38.Cui CY, Kunisada M, Childress V, Michel M, Schlessinger D. Shh is required for Tabby hair follicle development. Cell Cycle(Georgetown, Tex.). 2011;10:3379–86.

39.Närhi K, Tummers M, Ahtiainen L, Itoh N, Thesleff I, Mikkola ML. Sostdc1 defines the size and number of skin appendage placodes. Dev Biol. 2012;364:149–61.

40.Wang Y, Yuan X, Yao B, Zhu S, Zhu P, Huang S. Tailoring bioinks of extrusion-based bioprinting for cutaneous wound healing. Bioactive materials. 2022;17:178–94.

41.Guo Y, Wang YY, Sun TT, Xu JJ, Yang P, Ma CY, et al. Neural progenitor cells derived from fibroblasts induced by small molecule compounds under hypoxia for treatment of Parkinson's disease in rats. Neural Regen Res. 2023;18:1090–8.

42.Zhao A, Qin H, Sun M, Tang M, Mei J, Ma K, et al. Chemical conversion of human epidermal stem cells into intestinal goblet cells for modeling mucus-microbe interaction and therapy. Sci Adv. 2021;7:16.

43.Qin H, Zhao AD, Sun ML, Ma K, Fu XB. Direct conversion of human fibroblasts into dopaminergic neuron-like cells using small molecules and protein factors. Mil Med Res. 2020;7:52.

44.Lang HL, Zhao YZ, Xiao RJ, Sun J, Chen Y, Hu GW, et al. Small extracellular vesicles secreted by induced pluripotent stem cell-derived mesenchymal stem cells improve postoperative cognitive dysfunction in mice with diabetes. Neural Regen Res. 2023;18:609–17.

45.Zhou L, Wang D, Sheng D, Xu J, Chen W, Qin Y, et al. NOTCH4 maintains quiescent mesenchymal-like breast cancer stem cells via transcriptionally activating SLUG and GAS1 in triple-negative breast cancer. Theranostics. 2020;10:2405–21.

46.MacKenzie F, Duriez P, Larrivée B, Chang L, Pollet I, Wong F, et al. Notch4-induced inhibition of endothelial sprouting requires the ankyrin repeats and involves signaling through RBP-Jkappa. Blood. 2004;104:1760–8.

47.Yuan X, Duan X, Enhejirigala Z, Li B, Yao WS, Song W, et al. Reciprocal interaction between vascular niche and sweat gland promotes sweat gland regeneration. Bioactive materials. 2023;21:340–57.

48.Muley A, Kim Uh M, Salazar-De Simone G, Swaminathan B, James JM, Murtomaki A, et al. Unique functions for Notch4 in murine embryonic lymphangiogenesis. Angiogenesis. 2022;25:205–24.

49.Bonadeo N, Becu-Villalobos D, Cristina C, Lacau-Mengido IM. The Notch system during pubertal development of the bovine mammary gland. Sci Rep. 2019;9:8899.

50.Ho AS, Ochoa A, Jayakumaran G, Zehir A, Valero Mayor C, Tepe J, et al. Genetic hallmarks of recurrent/metastatic adenoid cystic carcinoma. J Clin Invest. 2019;129:4276–89.

51.Cook KM, Figg WD. Angiogenesis inhibitors: current strategies and future prospects. CA Cancer J Clin. 2010;60:222–43.

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