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Cited by 6Autophagy in Disease and TherapyHair Growth and DisordersCancer and Skin Lesions

Autophagy, not apoptosis, plays a role in lumen formation of eccrine gland organoids

Open access
Du, Lijie, Zhang, Lei, Zhao, Junhong, Chen, Zixiu, Liu, Xiang, Cao, Manxiu, You, Lei, Zhang, Yonghong, Fu, Xiaobing, Li, Haihong·2022·Chinese Medical Journal
DOI 10.1097/cm9.0000000000001936PMC PMC8812595
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Abstract

Background: Sweat secreted by eccrine sweat glands is transported to the skin surface through the lumen. The eccrine sweat gland develops from the initial solid bud to the final gland structure with a lumen, but how the lumen is formed and the mechanism of lumen formation have not yet been fully elucidated. This study aimed to investigate the mechanism of lumen formation of eccrine gland organoids (EGOs). Methods: Human eccrine sweat glands were isolated from the skin for tissue culture, and the primary cultured cells were collected and cultured in Matrigel for 14 days in vitro. EGOs at different development days were collected for hematoxylin and eosin (H&E) staining to observe morphological changes and for immunofluorescence staining of proliferation marker Ki67, cellular motility marker filamentous actin (F-actin), and autophagy marker LC3B. Western blotting was used to detect the expression of Ki67, F-actin, and LC3B. Moreover, apoptosis was detected using a terminal deoxynucleotidyl transferase dUTP nick end labeling (TUNEL) apoptosis assay kit, and the expression of poly (ADP-ribose) polymerase and Caspase-3 was detected by Western blot. In addition, 3-methyladenine (3MA) was used as an autophagy inhibitor to detect whether the formation of sweat glands can be effectively inhibited. Results: The results showed that a single gland cell proliferated rapidly and formed EGOs on day 4. The earliest lumen formation was observed on day 6. From day 8 to day 14, the rate of lumen formation in EGOs increased significantly. The immunofluorescence and Western blot analyses showed that the expression of Ki67 gradually decreased with the increase in days, while the F-actin expression level did not change. Notably, the expression of autophagy marker LC3B was detected in the interior cells of EGOs as the apoptosis signal of EGOs was negative. Compared with the control group, the autophagy inhibitor 3MA can effectively limit the formation rate of the lumen and reduce the inner diameter of EGOs. Conclusion: Using our model of eccrine gland 3D-reconstruction in Matrigel, we determined that autophagy rather than apoptosis plays a role in the lumen formation of EGOs.

AI snapshot

Written from the paper’s full text.

TL;DR

In a Matrigel-based 3D reconstruction of human eccrine sweat gland cells, eccrine gland organoids formed a lumen beginning on day 6, and lumen formation was associated with autophagy rather than apoptosis. The autophagy inhibitor 3MA reduced lumen formation and inner lumen diameter, supporting a role for autophagy in EGO lumenogenesis.

Key findings

  • EGOs formed from single cells by day 4; the earliest lumen was observed on day 6, and the rate of lumen formation increased significantly from day 8 to day 14.
  • Ki67 expression gradually decreased over culture time, while Western blot F-actin levels did not change; immunofluorescence showed F-actin on the spherical surface before lumen formation and on the inner membrane after day 6.
  • LC3B was detected in interior EGO cells, whereas apoptosis signals were negative by TUNEL and Western blot for cleaved PARP and cleaved Caspase-3; the autophagy ratio increased from day 8 to day 14.
  • Compared with control, 3MA effectively limited lumen formation and reduced inner lumen diameter, with no significant effect on average outer EGO diameter.

Methods

  • Human eccrine sweat glands were isolated from full-thickness skin specimens from 5 Han Chinese patients (3 males, 2 females; mean age 19.2±3.4 years; fingers, abdomens, arms) and primary cultured cells were embedded in Matrigel for 14 days.
  • EGOs were collected at different days for H&E staining, immunofluorescence for Ki67, F-actin, LC3B, and TUNEL apoptosis assay, plus Western blot for Ki67, F-actin, LC3B, PARP, and cleaved Caspase-3.
  • Autophagy inhibition was tested by adding 10 mmol/L 3MA to Matrigel and conditioned medium; statistical significance was assessed by one-way ANOVA with P < 0.05 considered significant.

Limitations

  • Stated: the 3D-reconstruction lumen formation model cannot spatiotemporally imitate the luminal form of sweat glands in the body as placode invagination.
  • Stated: LC3B immunofluorescence failed to stain the autophagy signal around basal cells in the embryonic base from mouse sweat gland duct formation period E15 to P5 (data not shown).
  • Evident from the text: the study uses a small human sample (5 patients) and an in vitro Matrigel model, with some supporting data described as not shown and no in vivo functional validation reported.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1097/cm9.0000000000001936

Cites

28 of 28 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

7 of 18 cited sources checked · 1 supported · 0 flagged · accuracy not yet measured

  • Interpretationown data

    The lumen structure in EGOs is similar to the primary structure of sweat gland ducts in body development.

    “Therefore, we can infer that the lumen structure in our EGOs is similar to the primary structure of sweat gland ducts in body development.”
    Quote in the paperSubstantial claim1 of 2 sources checked
    • cites [16] Zhang M Li H Xie S Chen L. Time course of differentiation of different cell types in 3D-reconstructed eccrine sweat glands. J Mol Histol 2018; 49: 567– 575. doi: 10.1007/s10735-018-9795-y. 30238337 source
    • cites [19] Ouyang Z Li HH Zhang MJ Xie ST Cheng LHH. Differential innervation of secretory coils and ducts in human eccrine sweat glands. Chin Med J (Engl) 2018; 131: 1964– 1968. doi: 10.4103/0366-6999.238142. 30082528 PMC6085860 source

      The Introduction and Results distinguish sweat gland ducts from secretory coils and examine their innervation, but do not compare EGO lumens with ducts during development. Searches for lumen structure, organoids, and developmental duct structure found no passage addressing that comparison. (LLM, conf=0.75)

      Experimental — accuracy not yet measured
  • Findingown data

    Western blot showed that Ki67 expression in EGO total protein was significantly reduced.

    “the Western blot results also proved that the expression of Ki67 in the EGO total protein was significantly reduced”
    Quote in the paperSubstantial claim
  • Findingown data

    A positive LC3B signal was found in EGO internal cells where the TUNEL signal was negative.

    “We performed immunohistochemistry on paraffin sections prepared from day 2 to day 14 and found a positive LC3B signal in EGO internal cells where the TUNEL signal was negative.”
    Quote in the paperSubstantial claim
  • Findingown data

    From day 8 to day 14, the rate of lumen formation in EGOs increased significantly.

    “From day 8 to day 14, the rate of lumen formation in EGOs increased significantly.”
    Quote in the paperNot a substantial claim
  • Findingown data

    The time of increased autophagy ratio was essentially the same as the time it took for EGOs to form lumens.

    “and it was essentially the same as the time it took for EGOs to form lumens”
    Quote in the paperSubstantial claim
  • Classified as probably not a substantial claim. 12
  • May combine two claims. 7
  • The quote only partly states this claim. 1

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Multiple research results have shown that autophagy protects cells exposed to various forms of stress, including nutrient deprivation, growth factor regression, endoplasmic reticulum stress, and ischemia.

    “In addition, multiple research results have shown that autophagy protects cells exposed to various forms of stress, including nutrient deprivation, growth factor regression, endoplasmic reticulum stress, and ischemia.[23–25]”
    Quote in the paperNot a substantial claim3 of 3 sources checked
    • cites [23] Satyavarapu EM Das R Mandal C Mukhopadhyay A Mandal C. Autophagy-independent induction of LC3B through oxidative stress reveals its non-canonical role in anoikis of ovarian cancer cells. Cell Death Dis 2018; 9: 934 doi: 10.1038/s41419-018-0989-8. 30224639 PMC6141567 source

      The Introduction (page unavailable) describes autophagy as supplying energy needed for cell survival during stress. The Results section on autophagosomes (page unavailable) reports increased autophagy in serum-starved cells. Our copy does not establish a protective effect specifically under nutrient deprivation, growth-factor withdrawal, endoplasmic-reticulum stress, or ischemia. (LLM, conf=0.85)

      Experimental — accuracy not yet measured
    • cites [24] Whelan KA Reginato MJ. Surviving without oxygen: hypoxia regulation of mammary morphogenesis and anoikis. Cell Cycle 2011; 10: 2287– 2294. doi: 10.4161/cc.10.14.16532. 21670595 source

      The “Targeting Anoikis-Resistant Hypoxic Cancer Cells” section describes autophagy as a survival mechanism under stress and says it promotes survival during loss of adhesion and prevents cell death during cycling hypoxia. It does not establish the claimed protection during nutrient deprivation, growth-factor regression, endoplasmic reticulum stress, or ischemia. (LLM, conf=0.86)

      Experimental — accuracy not yet measured
    • cites [25] Chen N Eritja N Lock R Debnath J. Autophagy restricts proliferation driven by oncogenic phosphatidylinositol 3-kinase in three-dimensional culture. Oncogene 2013; 32: 2543– 2554. doi: 10.1038/onc.2012.277. 22777351 PMC3470740 source

      The Introduction (page unavailable) says autophagy commonly promotes survival under stresses including nutrient starvation and ER stress. It does not identify growth-factor regression or ischemia among those stresses; it discusses hypoxia instead. The Discussion also reports a survival role for autophagy during extracellular-matrix deprivation, a different condition. (LLM, conf=0.88)

      Experimental — accuracy not yet measured

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    The filamentous actin (F-actin) network must participate in the lumen formation of the 3D-reconstitution model at the right time and place with the right organization.

    “the filamentous actin (F-actin) network must participate in the lumen formation of the 3D-reconstitution model at the right time and place with the right organization.[17]”
    Quote in the paperNot a substantial claim1 of 1 sources checked
    • cites [17] Kadzik RS Homa KE Kovar DR. F-actin cytoskeleton network self-organization through competition and cooperation. Annu Rev Cell Dev Biol 2020; 36: 35– 60. doi: 10.1146/annurev-cellbio-032320-094706. 33021819 PMC8675537 source

      The “Self-organization and homeostasis in cell biology” section says F-actin networks must assemble and disassemble at the correct time and place with proper organization. It does not establish that F-actin is required for lumen formation in a 3D-reconstitution model; searches for lumen formation and 3D reconstitution found no supporting passage. (LLM, conf=0.86)

      Experimental — accuracy not yet measured

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    The hollowing form was usually seen in the early stage of formation of the lumen of blood vessels and the formation of the intestinal lumen of zebrafish, and these developmental processes were generally not accompanied by cell death.

    “The hollowing form was usually seen in the early stage of formation of the lumen of blood vessels and the formation of the intestinal lumen of zebrafish, and these developmental processes were generally not accompanied by cell death.[26,27]”
    Quote in the paperNot a substantial claim1 of 2 sources checked
    • cites [26] Sacharidou A Stratman AN Davis GE. Molecular mechanisms controlling vascular lumen formation in three-dimensional extracellular matrices. Cells Tissues Organs 2012; 195: 122– 143. doi: 10.1159/000331410. 21997121 PMC3325603 source

      The section on EC lumen and tube assembly (page unavailable) describes intracellular vacuoles forming and fusing during early vascular lumen formation, including in developing zebrafish vessels. It does not address zebrafish intestinal lumen formation or say that these processes generally occur without cell death. It also describes vacuolation as one of several vascular lumen-forming mechanisms, rather than the usual form in all vessels. (LLM, conf=0.84)

      Experimental — accuracy not yet measured
    • cites [27] Sigurbjornsdottir S Mathew R Leptin M. Molecular mechanisms of de novo lumen formation. Nat Rev Mol Cell Biol 2014; 15: 665– 676. doi: 10.1038/nrm3871. 25186133 source

  • Classified as probably not a substantial claim.

    Premisecitation

    There are two main views of the mechanism mode of glandular lumen formation: cavitation and cell bundle hollowing.

    “There are currently two main views of the mechanism mode of glandular lumen formation: cavitation (driven by cell death of inner cells) and cell bundle hollowing (driven by epithelial polarity without cell death).[11]”
    Quote in the paperSubstantial claim1 of 1 sources checked
    • cites [11] Blasky AJ Mangan A Prekeris R. Polarized protein transport and lumen formation during epithelial tissue morphogenesis. Annu Rev Cell Dev Biol 2015; 31: 575– 591. doi: 10.1146/annurev-cellbio-100814-125323. 26359775 PMC4927002 source

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Findingown data

    F-actin expression level did not change over the 14-day culture period.

    “while the F-actin expression level did not change.”
    Quote in the paperNot a substantial claim

  • The quote only partly states this claim.

    Findingown data

    A hollow shape similar to a lumen exists in most EGOs by day 14.

    “it was obvious that a hollow shape similar to a lumen exists in most EGOs, which increases the proportion of vacuoles”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    Single gland cells divided and proliferated from day 0 to day 4 and formed multicellular EGOs.

    “The results showed that a single gland cell proliferated rapidly and formed EGOs on day 4.”
    • Also stated in: § EGOs developed from the initial solid structure to the final luminal structure · plain
      “Brightfield, visual field, and H&E staining results showed that the single cells divided and proliferated from day 0 to day 4 and continued to self-multiply or migrate to each other to form multicellular EGOs”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    The EGOs were spherical and their volume increased from day 4 to day 8.

    “When the cells underwent sustained proliferation and differentiation from day 4 to day 8, we observed that the EGOs were spherical, and the spheroid volume was obviously increased and spatially independent to other EGOs”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Findingown data

    The earliest lumen formation was observed on day 6.

    “The earliest lumen formation was observed on day 6.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Anoikis has been reported in the formation of the lumen during the development of various secretory glands such as mammary and salivary glands.

    “Anoikis, a form of apoptosis caused by inappropriate cell/ECM interactions, has been reported in the formation of the lumen during the development of various secretory glands such as mammary and salivary glands.[20,21]”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [20] Gilmore AP. Anoikis Cell Death Differ 2005; 12: 1473– 1477. doi: 10.1038/sj.cdd.4401723. 16247493 source
    • cites [21] Fung C Lock R Gao S Salas E Debnath J. Induction of autophagy during extracellular matrix detachment promotes cell survival. Mol Biol Cell 2008; 19: 797– 806. doi: 10.1091/mbc.e07-10-1092. 18094039 PMC2262959 source

  • May combine two claims.

    Interpretationown data

    Autophagy, not apoptosis, induces lumen formation.

    “Autophagy, not apoptosis, induces lumen formation”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).

    Interpretationreasoning

    Programmed cell death caused by abnormal metabolism could create a cavity at the center of each EGO.

    “Since the cells inside the EGOs cannot access the nutrients of the Matrigel and conditioned medium, the programmed cell death caused by abnormal metabolism could create a cavity at the center of each EGO.”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: The cells inside the EGOs cannot access the nutrients of the Matrigel and conditioned medium.

  • May combine two claims.

    Interpretationown data

    High expression of LC3B together with absence of signaling of apoptotic cells (cleaved PARP and cleaved Caspase-3) within EGOs demonstrated that autophagy was the main cell death mode mechanism.

    “In our Western blot assay, the high expression of cell autophagy marker LC3B together with the absence of signaling of apoptotic cells (cleaved PARP and cleaved Caspase-3) within EGOs demonstrated that autophagy was identified as the main cell death mode mechanism”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    Debnath et al proved that inhibition of apoptosis through ectopic expression of anti-apoptotic protein Bcl-2 cannot terminate the formation of the lumen, which indicated that induction of autophagy contributed to the survival of epithelial cells during oxygen-deficient environment in the 3D hollow formation.

    “It is worth noting that Debnath et al[22] recently proved that the inhibition of apoptosis through the ectopic expression of the anti-apoptotic protein Bcl-2 cannot terminate the formation of the lumen, which indicated that the induction of autophagy contributed to the survival of epithelial cells during oxygen-deficient environment in the 3D hollow formation.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Debnath et al[22]

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductown data

    Representative images and graphics results are from three independent experiments of eccrine sweat gland 3D-reconstruction, mean ± SD.

    “Representative images and graphics results from three independent experiments of eccrine sweat gland 3D-reconstruction, mean ± SD.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Diao et al reported that sweat gland organoids that were formed from epithelial cells from the dermal sweat glands of adult mouse paw pads embedded in Matrigel can effectively restore the ductal morphology and sweat secretion function of sweat glands after transplantation into the paws of mice with damaged sweat glands.

    “Nevertheless, Diao et al[28] reported that sweat gland organoids that were formed from epithelial cells from the dermal sweat glands of adult mouse paw pads embedded in Matrigel can effectively restore the ductal morphology and sweat secretion function of sweat glands after transplantation into the paws of mice with damaged sweat glands.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Diao et al[28]

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductown data

    Western blot assays were performed more than three times with representative results shown.

    “The Western blots assays were performed more than three times with the representative results shown in the [Figure 2C and 3C].”
    Quote in the paperNot a substantial claim

  • Classified as probably not a substantial claim.

    Premisecitation

    The 3D-reconstitution model by culturing Matrigel-embedded ESGCs in vitro or implanting them into the subcutis of nude mice simulates the development, morphology, and function of sweat glands in natural form.

    “A recent study used a 3D-reconstitution model by culturing Matrigel-embedded eccrine sweat gland cells (ESGCs) in vitro or by implanting them into the subcutis of nude mice and concluded that this model simulates the development, morphology, and function of sweat glands in natural form.[12–16]”
    Quote in the paperSubstantial claim0 of 5 sources checked
    • cites [12] Li H Chen L Zhang M Tang S Fu X. Three-dimensional culture and identification of human eccrine sweat glands in matrigel basement membrane matrix. Cell Tissue Res 2013; 354: 897– 902. doi: 10.1007/s00441-013-1718-3. 23996202 source
    • cites [13] Li H Zhang M Chen L Zhang B Zhang C. Expression of S100A2 and S100P in human eccrine sweat glands and their application in differentiating secretory coil-like from duct-like structures in the 3D reconstituted eccrine sweat spheroids. J Mol Histol 2017; 48: 219– 223. doi: 10.1007/s10735-017-9721-8. 28353163 source
    • cites [14] Li X Li H Zhang M Chen L Zhang B. Cell proliferation and differentiation during the three dimensional reconstitution of eccrine sweat glands. J Mol Histol 2017; 48: 113– 120. doi: 10.1007/s10735-017-9710-y. 28093664 source
    • cites [15] 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– 345. doi: 10.1007/s10735-018-9773-4. 29667149 source
    • cites [16] Zhang M Li H Xie S Chen L. Time course of differentiation of different cell types in 3D-reconstructed eccrine sweat glands. J Mol Histol 2018; 49: 567– 575. doi: 10.1007/s10735-018-9795-y. 30238337 source

  • May combine two claims.

    Interpretationreasoning

    The polarized and flat outer layer of cells surrounded the cells in the inner center layer by layer, resulting in insufficient nutrition of the inner cells and further autophagy.

    “In summary, the polarized and flat outer layer of cells surrounded the cells in the inner center layer by layer, resulting in insufficient nutrition of the inner cells and further autophagy.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The cells inside the EGOs cannot access the nutrients of the Matrigel and conditioned medium.
19 of 19

  • The paper relies on this without support.

    The cells inside the EGOs cannot access the nutrients of the Matrigel and conditioned medium.

    “Since the cells inside the EGOs cannot access the nutrients of the Matrigel and conditioned medium”

  • The paper relies on this without support.

    3-MA specifically inhibits autophagy and its effects on lumen formation are due to autophagy inhibition rather than off-target effects.

    “3-methyladenine (3MA) was used as an autophagy inhibitor to detect whether the formation of sweat glands can be effectively inhibited.”
2 of 2

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Cited works that were retracted

Works this paper cites that were later retracted, from the retraction notices publishers deposit. Major when the notice came out before this paper was published.

  • Cites a retracted work: 10.1038/s41419-018-0989-8

    Info

    The cited work was retracted on 2024-09-04 (notice 10.1038/s41419-024-07025-6), not before this paper was published (2022-01-12).

    Cited work 10.1038/s41419-018-0989-8 · retracted 2024-09-04 · notice 10.1038/s41419-024-07025-6 · this paper published 2022-01-12

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Authors
Du, L., Zhang, L., Zhao, J., Chen, Z., Liu, X., Cao, M., You, L., Zhang, Y., Fu, X., & Li, H.
Affiliations
  • Hubei University of Medicine (CN)
  • Chinese PLA General Hospital (CN)
Corresponding author
Li, Haihong
Venue
Chinese Medical Journal
Publisher
Ovid Technologies (Wolters Kluwer Health)
Published
2022-01-12
Volume
135
Issue
3
Pages
324-332
ISSN
  • 0366-6999 (ISSN-L)
  • 2542-5641
DOI
10.1097/cm9.0000000000001936
PMC
PMC8812595
OpenAlex
W4206730874
Semantic Scholar
b9fb3f3f5bef34e0d1e5b6e37fa0d1cb9e8db846
Cited by
6
References
28
Citations by year
2026: 2 · 2024: 1 · 2023: 3
FWCI
0.61
Type
journal article
Language
en
Open access
Licence
Locations
  • Chinese Medical Journal (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • PubMed Central (submittedVersion, cc-by-nc-nd)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Topics
  • Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
  • Health Sciences › Medicine › Urology › Hair Growth and Disorders
  • Health Sciences › Medicine › Dermatology › Cancer and Skin Lesions
Keywords
eccrine sweat glands, lumen formation, autophagy, apoptosis, organoids, sweat gland development, LC3B, 3-methyladenine, Ki-67, F-actin, 3D organoid culture, Matrigel
MeSH terms
Autophagy, Eccrine Glands, Epithelial Cells, Humans, Organoids, Apoptosis

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