1. School of Medicine
2. Research Center for Tissue Repair and Regeneration affiliated to the Medical Innovation Research Department, PLA General Hospital
3. PLA Key Laboratory of Tissue Repair and Regenerative Medicine and Beijing Key Research Laboratory of Skin Injury
4. Chinese PLA General Hospital and PLA Medical College
5. Academy of Medical Engineering and Translational Medicine, Tianjin University
6. College of Graduate, Tianjin Medical University
7. Institute of Basic Medical Research, Inner Mongolia Medical University
8. Department of Burn and Plastic Surgery, Air Force Hospital of Chinese PLA Central Theater Command
9. Research Unit of Trauma Care, Tissue Repair and Regeneration, Chinese Academy of Medical Sciences, 2019RU,051
Published:2022,
Published Online:2 August 2022,
扫 描 看 全 文
Xingyu Yuan, Xianlan Duan, Zhao Li, Bin Yao, Enhejirigala, Wei Song, Yi Kong, Yuzhen Wang, Fanliang Zhang, Liting Liang, Shijun Zhu, Mengde Zhang, Chao Zhang, Sha Huang, Xiaobing Fu, Collagen triple helix repeat containing-1 promotes functional recovery of sweat glands by inducing adjacent microvascular network reconstruction in vivo, Burns & Trauma, Volume 10, 2022, tkac035, https://doi.org/10.1093/burnst/tkac035
Xingyu Yuan, Xianlan Duan, Zhao Li, Bin Yao, Enhejirigala, Wei Song, Yi Kong, Yuzhen Wang, Fanliang Zhang, Liting Liang, Shijun Zhu, Mengde Zhang, Chao Zhang, Sha Huang, Xiaobing Fu, Collagen triple helix repeat containing-1 promotes functional recovery of sweat glands by inducing adjacent microvascular network reconstruction in vivo, Burns & Trauma, Volume 10, 2022, tkac035, https://doi.org/10.1093/burnst/tkac035 DOI:
BackgroundSweat glands (SGs) have low regenerative potential after severe burns or trauma and their regeneration or functional recovery still faces many obstacles. In practice
restoring SG function requires not only the structural integrity of the gland itself
but also its neighboring tissues
especially blood vessels. Collagen triple helix repeat containing-1 (CTHRC1) was first identified in vascular repair
and increasing reports showed a close correlation between cutaneous appendage specification
patterning and regeneration. The purpose of the present study was to clarify the role of CTHRC1 in SGs and their adjacent microvessels and find therapeutic strategies to restore SG function.MethodsThe SGs and their adjacent microvascular network of Cthrc1−/− mice were first investigated using sweat test
laser Doppler imaging
tissue clearing technique and transcriptome analysis. The effects of CTHRC1 on dermal microvascular endothelial cells (DMECs) were further explored with cell proliferation
DiI-labeled acetylated low-density lipoprotein uptake
tube formation and intercellular junction establishment assays. The effects of CTHRC1 on SG function restoration were finally confirmed by replenishing the protein into the paws of Cthrc1−/− mice.ResultsCTHRC1 is a key regulator of SG function in mice. At the tissue level
Cthrc1 deletion resulted in the disorder and reduction of the microvascular network around SGs. At the molecular level
the knockout of Cthrc1 reduced the expression of vascular development genes and functional proteins in the dermal tissues. Furthermore
CTHRC1 administration considerably enhanced SG function by inducing adjacent vascular network reconstruction.ConclusionsCTHRC1 promotes the development
morphogenesis and function execution of SGs and their neighboring vasculature. Our study provides a novel target for the restoration or regeneration of SG function in vivo.
Collagen triple helix repeat containing-1Sweat glandsMicrovascular networkDermal microvascular endothelial cells Reconstruction
1.Lu C, Fuchs E. Sweat gland progenitors in development, homeostasis, and wound repair. Cold Spring Harb Perspect Med. 2014;4:1–17.
2.Song W, Yao B, Zhu D, Zhang Y, Li Z, Huang S, et al. 3D-bioprinted microenvironments for sweat gland regeneration. Burns Trauma. 2022;10:tkab044. https://doi.org/10.1093/burnst/tkab044.
3.Cheshire WP, Freeman R. Disorders of sweating. Semin Neurol. 2003;23:399–406.
4.Reid AT, Goettsche L, Willis M, Powers J, Berrebi KG. Acquired idiopathic generalized anhidrosis: a case series of two Caucasian patients. Pediatr Dermatol. 2021;38:1219–21.
5.Lin JB, Lin NL, Li X, Kang MQ. Antagonist of Chrna1 prevents the pathogenesis of primary focal hyperhidrosis. Ann Clin Transl Neurol. 2022;9:786–94.
6.Zhang M, Li H, Chen L, Fang S, Xie S, Lin C. Three-dimensional reconstructed eccrine sweat glands with vascularization and cholinergic and adrenergic innervation. J Mol Histol. 2018;49:339–45.
7.Kennedy WR, Wendelschafer-Crabb G, Brelje TC. Innervation and vasculature of human sweat glands: an immunohistochemistry-laser scanning confocal fluorescence microscopy study. J Neurosci. 1994;14:6825–33.
8.Palazzo AF, Kurata R, Futaki S, Nakano I, Fujita F, Tanemura A, et al. Three-dimensional cell shapes and arrangements in human sweat glands as revealed by whole-mount immunostaining. PLoS One. 2017;12:1–17.
9.Zhang Y, Enhejirigala LZ, Song W, Yao B, Li J, et al. The role of CTHRC1 in hair follicle regenerative capacity restored by plantar dermis homogenate. Biochem Biophys Res Commun. 2021;571:14–9.
10.Lang DH, Ba T, Cao SJ, Li F, Dong H, Li JL, et al. Research advances on signaling pathways affecting sweat gland development and their involvement in the reconstitution of sweat adenoid cells in vitro. Chin J Burns. 2022;38:195–200.
11.Liao T, Lehmann J, Sternstein S, Yay A, Zhang G, Matthiessen AE, et al. Nestin(+) progenitor cells isolated from adult human sweat gland stroma promote reepithelialisation and may stimulate angiogenesis in wounded human skin ex vivo. Arch Dermatol Res. 2019;311:325–30.
12.Huang S, Yao B, Xie J, Fu X. 3D bioprinted extracellular matrix mimics facilitate directed differentiation of epithelial progenitors for sweat gland regeneration. Acta Biomater. 2016;32:170–7.
13.Pyagay P, Heroult M, Wang Q, Lehnert W, Belden J, Liaw L, et al. Collagen triple helix repeat containing 1, a novel secreted protein in injured and diseased arteries, inhibits collagen expression and promotes cell migration. Circ Res. 2005;96:261–8.
14.LeClair R, Lindner V. The role of collagen triple helix repeat containing 1 in injured arteries, collagen expression, and transforming growth factor, beta signaling [review]. Trends Cardiovasc Med. 2007;17:202–5.
15.Lee J, Song J, Kwon E-S, Jo S, Kang MK, Kim YJ, et al. CTHRC1 promotes angiogenesis by recruiting Tie2-expressing monocytes to pancreatic tumors. Exp Mol Med. 2016;48:e261–1. https://doi.org/10.1038/emm.2016.87.
16.Chen Y, Sun Y, Cui Y, Lei Y, Jiang N, Jiang W, et al. High CTHRC1 expression may be closely associated with angiogenesis and indicates poor prognosis in lung adenocarcinoma patients. Cancer Cell Int. 2019;19:318. https://doi.org/10.1186/s12935-019-1041-5.
17.Fu SW, Chen HY, Lin XL, Yang L, Ge ZZ. Collagen triple helix repeat containing 1 promotes tumor angiogenesis in gastrointestinal stromal tumors. Oncol Lett. 2017;14:7499–505.
18.van Nistelrooij AM, Dinjens WN, Wagner A, Spaander MC, van Lanschot JJ, Wijnhoven BP. Hereditary factors in Esophageal adenocarcinoma. Gastrointest Tumors. 2014;1:93–8.
19.Qin S, Zheng JH, Xia ZH, Qian J, Deng CL, Yang SL. CTHRC1 promotes wound repair by increasing M2 macrophages via regulating the TGF-beta and notch pathways. Biomed Pharmacother. 2019;113:108594. https://doi.org/10.1016/j.biopha.2019.01.055.
20.Dong B, Vold S, Olvera-Jaramillo C, Chang H. Functional redundancy of frizzled 3 and frizzled 6 in planar cell polarity control of mouse hair follicles. Development. 2018;145:1–11.
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;6:1–10.
22.Ellis RA, Montagna W, Fanger H. Histology and cytochemistry of human skin. XIV. The blood supply of the cutaneous glands. J Invest Dermatol. 1958;30:137–45.
23.Yamamoto O. Three-dimensional architecture of the microvasculature in the rat foot-pad, with special reference to vasculature around the eccrine sweat glands. A scanning electron-microscopic study of corrosion casts. Cell Tissue Res. 1990;262:225–32.
24.Jing D, Zhang S, Luo W, Gao X, Men Y, Ma C, et al. Tissue clearing of both hard and soft tissue organs with the PEGASOS method. Cell Res. 2018;28:803–18.
25.Hou H, Li J, Zhou L, Liang J, Wang J, Li J, et al. An effective method of isolating microvascular endothelial cells from the human dermis. Cell Biol Int. 2020;44:2588–97.
26.Plendl J, Gilligan BJ, Wang SJ, Lewis R, Shinners B, Vandenbroeck K, et al. Primitive endothelial cell lines from the porcine embryonic yolk sac. In Vitro Cell Dev Biol Anim. 2002;38:334–42.
27.Jeon JS, Bersini S, Gilardi M, Dubini G, Charest JL, Moretti M, et al. Human 3D vascularized organotypic microfluidic assays to study breast cancer cell extravasation. Proc Natl Acad Sci U S A. 2015;112:214–9.
28.Cerqueira MT, da Silva LP, Santos TC, Pirraco RP, Correlo VM, Reis RL, et al. Gellan gum-hyaluronic acid spongy-like hydrogels and cells from adipose tissue synergize promoting neoskin vascularization. ACS Appl Mater Interfaces. 2014;6:19668–79.
29.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. https://doi.org/10.1186/s41038-019-0167-y.
30.Zhang Y, Enhejirigala YB, Li Z, Song W, 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. https://doi.org/10.1093/burnst/tkab013.
31.LeClair RJ, Durmus T, Wang Q, Pyagay P, Terzic A, Lindner V. Cthrc1 is a novel inhibitor of transforming growth factor-beta signaling and neointimal lesion formation. Circ Res. 2007;100:826–33.
32.Ruiz-Villalba A, Romero JP, Hernández SC, Vilas-Zornoza A, Fortelny N, Castro-Labrador L, et al. Single-cell RNA sequencing analysis reveals a crucial role for CTHRC1 (collagen triple helix repeat containing 1) cardiac fibroblasts after myocardial infarction. Circulation. 2020;142:1831–47.
33.Tsukui T, Sun KH, Wetter JB, Wilson-Kanamori JR, Hazelwood LA, Henderson NC, et al. Collagen-producing lung cell atlas identifies multiple subsets with distinct localization and relevance to fibrosis. Nat Commun. 2020;11:1920. https://doi.org/10.1038/s41467-020-15647-5.
34.Mazio C, Casale C, Imparato G, Urciuolo F, Attanasio C, De Gregorio M, et al. Pre-vascularized dermis model for fast and functional anastomosis with host vasculature. Biomaterials. 2019;192:159–70.
35.Bourland J, Mayrand D, Tremblay N, Moulin VJ, Fradette J, Auger FA. Isolation and culture of human dermal microvascular endothelial cells. Methods Mol Biol. 2019;1993:79–90.
36.Calabria AR, Weidenfeller C, Jones AR, de Vries HE, Shusta EV. Puromycin-purified rat brain microvascular endothelial cell cultures exhibit improved barrier properties in response to glucocorticoid induction. J Neurochem. 2006;97:922–33.
37.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.
38.Yao B, Xie J, Liu N, Hu T, Song W, Huang S, et al. Direct reprogramming of epidermal cells toward sweat gland-like cells by defined factors. Cell Death Dis. 2019;10:272. https://doi.org/10.1038/s41419-019-1503-7.
39.Zhu DZ, Wang YH, Wang R, Fu XB. Effects and mechanism of exogenous tumor necrosis factor α on differentiation of mesenchymal stem cells of mice into sweat gland cells in three-dimensional environment. Zhonghua Shao Shang Za Zhi. 2020;36:187–94.
40.Danner S, Kremer M, Petschnik AE, Nagel S, Zhang Z, Hopfner U, et al. The use of human sweat gland-derived stem cells for enhancing vascularization during dermal regeneration. J Invest Dermatol. 2012;132:1707–16.
0
Views
0
下载量
0
CSCD
Publicity Resources
Related Articles
Related Author
Related Institution
京公网安备11010802024621
