Spandidos Publications Logo
  • About
    • About Spandidos
    • Aims and Scopes
    • Abstracting and Indexing
    • Editorial Policies
    • Reprints and Permissions
    • Job Opportunities
    • Terms and Conditions
    • Contact
  • Journals
    • All Journals
    • Oncology Letters
      • Oncology Letters
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Oncology
      • International Journal of Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular and Clinical Oncology
      • Molecular and Clinical Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Experimental and Therapeutic Medicine
      • Experimental and Therapeutic Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Molecular Medicine
      • International Journal of Molecular Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Biomedical Reports
      • Biomedical Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Reports
      • Oncology Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular Medicine Reports
      • Molecular Medicine Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • World Academy of Sciences Journal
      • World Academy of Sciences Journal
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Functional Nutrition
      • International Journal of Functional Nutrition
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Epigenetics
      • International Journal of Epigenetics
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Medicine International
      • Medicine International
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
  • Articles
  • Information
    • Information for Authors
    • Information for Reviewers
    • Information for Librarians
    • Information for Advertisers
    • Conferences
  • Language Editing
Spandidos Publications Logo
  • About
    • About Spandidos
    • Aims and Scopes
    • Abstracting and Indexing
    • Editorial Policies
    • Reprints and Permissions
    • Job Opportunities
    • Terms and Conditions
    • Contact
  • Journals
    • All Journals
    • Biomedical Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Experimental and Therapeutic Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Epigenetics
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Functional Nutrition
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Molecular Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Medicine International
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular and Clinical Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular Medicine Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Letters
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • World Academy of Sciences Journal
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
  • Articles
  • Information
    • For Authors
    • For Reviewers
    • For Librarians
    • For Advertisers
    • Conferences
  • Language Editing
Login Register Submit
  • This site uses cookies
  • You can change your cookie settings at any time by following the instructions in our Cookie Policy. To find out more, you may read our Privacy Policy.

    I agree
Search articles by DOI, keyword, author or affiliation
Search
Advanced Search
presentation
International Journal of Oncology
Join Editorial Board Propose a Special Issue
Print ISSN: 1019-6439 Online ISSN: 1791-2423
Journal Cover
April-2026 Volume 68 Issue 4

Full Size Image

Cover Legend PDF

Sign up for eToc alerts
Recommend to Library

Journals

International Journal of Molecular Medicine

International Journal of Molecular Medicine

International Journal of Molecular Medicine is an international journal devoted to molecular mechanisms of human disease.

International Journal of Oncology

International Journal of Oncology

International Journal of Oncology is an international journal devoted to oncology research and cancer treatment.

Molecular Medicine Reports

Molecular Medicine Reports

Covers molecular medicine topics such as pharmacology, pathology, genetics, neuroscience, infectious diseases, molecular cardiology, and molecular surgery.

Oncology Reports

Oncology Reports

Oncology Reports is an international journal devoted to fundamental and applied research in Oncology.

Experimental and Therapeutic Medicine

Experimental and Therapeutic Medicine

Experimental and Therapeutic Medicine is an international journal devoted to laboratory and clinical medicine.

Oncology Letters

Oncology Letters

Oncology Letters is an international journal devoted to Experimental and Clinical Oncology.

Biomedical Reports

Biomedical Reports

Explores a wide range of biological and medical fields, including pharmacology, genetics, microbiology, neuroscience, and molecular cardiology.

Molecular and Clinical Oncology

Molecular and Clinical Oncology

International journal addressing all aspects of oncology research, from tumorigenesis and oncogenes to chemotherapy and metastasis.

World Academy of Sciences Journal

World Academy of Sciences Journal

Multidisciplinary open-access journal spanning biochemistry, genetics, neuroscience, environmental health, and synthetic biology.

International Journal of Functional Nutrition

International Journal of Functional Nutrition

Open-access journal combining biochemistry, pharmacology, immunology, and genetics to advance health through functional nutrition.

International Journal of Epigenetics

International Journal of Epigenetics

Publishes open-access research on using epigenetics to advance understanding and treatment of human disease.

Medicine International

Medicine International

An International Open Access Journal Devoted to General Medicine.

Journal Cover
April-2026 Volume 68 Issue 4

Full Size Image

Cover Legend PDF

Sign up for eToc alerts
Recommend to Library

  • Article
  • Citations
    • Cite This Article
    • Download Citation
    • Create Citation Alert
    • Remove Citation Alert
    • Cited By
  • Similar Articles
    • Related Articles (in Spandidos Publications)
    • Similar Articles (Google Scholar)
    • Similar Articles (PubMed)
  • Download PDF
  • Download XML
  • View XML

  • Supplementary Files
    • Supplementary_Data.pdf
Article Open Access

lncRNA AL445238.2‑USP4 axis regulates cell survival and stemness in colon cancer

  • Authors:
    • Hualong Lin
    • Jieni Feng
    • Peirui Chen
    • Jialin Hu
    • Linjia Zhu
    • Shaofei Yuan
  • View Affiliations / Copyright

    Affiliations: Department of Medical Oncology, Rui'an People's Hospital, The Third Affiliated Hospital of Wenzhou Medical University, Wenzhou, Zhejiang 325200, P.R. China, Department of Pharmacy, China Pharmaceutical University, Jiangsu Cancer Hospital, Nanjing, Jiangsu 210000, P.R. China, Department of Respiratory Medicine, Rui'an People's Hospital, The Third Affiliated Hospital of Wenzhou Medical University, Wenzhou, Zhejiang 325200, P.R. China
    Copyright: © Lin et al. This is an open access article distributed under the terms of Creative Commons Attribution License [CC BY_NC 4.0].
  • Article Number: 45
    |
    Published online on: February 20, 2026
       https://doi.org/10.3892/ijo.2026.5858
  • Expand metrics +
Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )
Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )
Cited By (CrossRef): 0 citations Loading Articles...

This article is mentioned in:


Abstract

Local progression and metastasis remain the foremost impediments to long‑term survival among patients with colorectal cancer (CRC). long non‑coding RNAs (lncRNAs) have a pivotal role in the advancement of colorectal malignancies. The aim of the present study was to elucidate the functional role and underlying molecular mechanisms of the lncRNA AL445238.2 in CRC progression. In the present study, overexpression/knockdown lentiviral vectors, protein half‑life assays and co‑immunoprecipitation assays were used to explore the regulatory relationship among AL445238.2, ubiquitin‑specific protease 4 (USP4) and BCL2, combined with Transwell assays, sphere formation assays and subcutaneous xenograft models to demonstrate their effects on colon cancer proliferation and stemness both in vitro and in vivo. The experimental findings revealed that AL445238.2 was highly expressed in CRC cells. AL445238 overexpression significantly enhanced the proliferation of DLD1 and SW480 cells, reduced extracellular lactate dehydrogenase release, diminished apoptotic activity and increased cellular stemness, as evidenced by increased CD133 expression and augmented tumor sphere formation, together with enhanced mitochondrial activity. RNA pulldown and immunofluorescence assays further demonstrated a direct interaction between AL445238.2 and USP4, with the two synergistically modulating the expression of the anti‑apoptotic protein Bcl2 and the pro‑apoptotic protein BAX to suppress apoptosis. Moreover, in in vivo assays, USP4 independently promoted cell proliferation, sustained stemness and enhanced mitochondrial function, thereby increasing tumor growth. Collectively, the findings of the present study revealed that AL445238.2, through its interaction with USP4, orchestrated the regulation of cell proliferation, apoptosis, stemness maintenance and migration in CRC cells, offering novel insights into the role of lncRNAs in cancer progression and highlighting potential therapeutic targets.
View Figures

Figure 1

AL445238.2 regulates the survival of
colon cancer cells. (A) Validation of gene manipulation efficiency
in SW480 and DLD1 cell lines with stable overexpression and
knockdown of AL445238.2. (B) Cell Counting Kit-8 assay of SW480 and
DLD1 stable cell lines. (C) Proportion of apoptotic SW480 and DLD1
stable cell lines (percentage of supernatant LDH/total LDH). (D)
Statistical analysis of the Annexin V and PI staining
assay(Proportion percentage of Apoptotic cells). (E) Annexin V and
PI staining of SW480 and DLD1 stable cell lines.
**P<0.01, ***P<0.001,
****P<0.0001. NC, negative control; sh, short
hairpin; OE, overexpression; LDH, lactate dehydrogenase; ns, not
significant.

Figure 2

AL445238.2 promotes the stemness and
mitochondrial stability of colon cancer cells. (A) The expression
of CD133 in SW480 and DLD1 stable cell lines was detected with flow
cytometry. (B) The statistical analysis of CD133 MFI. (C) TMRM
staining of SW480 and DLD1 stable cell lines. (D) The statistical
analysis of TMRM MFI. (E) Tumor spheroid formation assay of SW480
and DLD1 stable cell lines. *P<0.05,
**P<0.01, ***P<0.001,
****P<0.0001. MFI, mean fluorescence intensity; TMRM,
tetramethylrhodamine; NC, negative control; sh, short hairpin; OE,
overexpression.

Figure 3

AL445238.2 binding to USP4 stabilizes
Bcl2 to regulate colon cancer cell apoptosis and stemness. (A)
Pulldown assay with AL445238.2 and western blot detection of USP4.
(B) Gene colocalization was detected by immunofluorescence
(magnification, ×200). (C) Validation of gene manipulation
efficiency in SW480 and DLD1 cell lines with stable overexpression
and knockdown of USP4. (D) Western blotting was used to evaluate
the expression of BAX, Bcl2 and C-CASP3 in stable SW480 cells; BAX
and Bcl2 were normalized against GAPDH, C-CASP3 was normalized
against total CASP3. Western blotting was used to evaluate the
expression of ALDH1A1, Bmi1 and EpCAM in stable (E) DLD1 and (F)
SW480 cells. (G) Co-immunoprecipitation experiments were used to
verify the interaction between USP4 and Bcl2. (H) Western blotting
was used to evaluate the effects of USP4 knockdown and MG132 on
Bcl2 protein expression. (I) Protein half-life experiments were
used to evaluate the effects of USP4 and AL445238.2 on the
stability of Bcl2 protein. **P<0.01,
***P<0.001, ****P<0.0001. USP4,
ubiquitin specific peptidase 4; RIP, RNA immunoprecipitation; Ctrl,
control; ALDH1A1, aldehyde dehydrogenase 1 family member A1; Bmi1,
B lymphoma Mo-MLV insertion region 1; EpCAM, epithelial cell
adhesion molecule; CHX, cycloheximide; OE, overexpression; sh,
short hairpin; NC, negative control; ns, not significant; C-CASP3,
cleaved caspase-3.

Figure 4

USP4 regulates the survival of colon
cancer cells. (A) Cell Counting Kit-8 Assay of SW480 and DLD1
stable cell lines. (B) Proportion of apoptotic SW480 and DLD1
stable cell lines (percentage of supernatant LDH/total LDH). (C)
Statistical analysis of the Annexin V and PI staining assay
(percentage of apoptotic cells). (D) Annexin V and PI staining of
SW480 and DLD1 stable cell lines. **P<0.01,
***P<0.001, ****P<0.0001. USP4,
ubiquitin specific peptidase 4; OE, overexpression; sh, short
hairpin; NC, negative control; ns, not significant; LDH, lactate
dehydrogenase.

Figure 5

USP4 promotes stemness and
mitochondrial stability of colon cancer cells. (A) Western blotting
was used to evaluate the expression of BAX, Bcl2 and C-CASP3 in
stable SW480 cells; BAX and Bcl2 were normalized against GAPDH,
C-CASP3 was normalized against total CASP3. (B) The expression of
CD133 in the SW480 and DLD1 stable cell lines was detected with
flow cytometry. (C) Statistical analysis of the CD133 MFI. (D)
Statistical analysis of the TMRM MFI. (E) TMRM staining of SW480
and DLD1 stable cell lines. (F) Tumor spheroid formation assay of
SW480 and DLD1 stable cell lines. *P<0.05,
**P<0.01, ***P<0.001,
****P<0.0001. MFI, mean fluorescence intensity; TMRM,
tetramethylrhodamine; C-CASP3, cleaved caspase-3; NC, negative
control; USP4, ubiquitin specific peptidase 4; sh, short hairpin;
OE, overexpression.

Figure 6

AL445238.2 controlled USP4 promotes
colon cancer cell migration. Migration assay of DLD1 and SW480
cells treated with shNC, sh-AL445238.2, Vector or OE-AL445238.2.
(A) Representative images show migrated cells stained with crystal
violet. (B) Quantitative analysis of migrated cell numbers in DLD1
(upper panel) and SW480 (lower panel) cells following AL445238.2
knockdown or overexpression. Migration assay of DLD1 and SW480
cells treated with shNC, sh-USP4, Vector or OE-USP4. (C)
Representative images show migrated cells stained with crystal
violet. (D) Quantitative analysis of migrated cell numbers in DLD1
(upper panel) and SW480 (lower panel) cells following USP4
knockdown or overexpression. Migration assay of DLD1 and SW480
cells with combined treatments: NC, OE-AL445238.2, OE-AL445238.2 +
OE-USP4 or OE-AL445238.2 + sh-USP4. (E) Representative images show
migrated cells. (F) Quantitative analysis of migrated cell numbers
in DLD1 (left panel) and SW480 (right panel) cells under combined
treatment conditions. *P<0.05,
**P<0.01, ***P<0.001,
****P<0.0001. sh, short hairpin; NC, negative
control; USP4, ubiquitin specific peptidase 4; OE,
overexpression.

Figure 7

AL445238.2 and USP4 promotes colon
cancer cell proliferation in vivo. (A) Tumors at the
endpoint for each group. (B) Tumor volume curves for each group.
(C) Images of tumor-bearing nude mice from each group. (D) Tumor
weight at the endpoint for each group. *P<0.05,
****P<0.0001. OE, overexpression; USP4, ubiquitin
specific peptidase 4.
View References

1 

Siegel RL, Wagle NS, Cercek A, Smith RA and Jemal A: Colorectal cancer statistics, 2023. CA Cancer J Clin. 73:233–254. 2023.PubMed/NCBI

2 

Arcos M, Goodla L, Kim H, Desai SP, Liu R, Yin K, Liu Z, Martin DR and Xue X: PINK1-deficiency facilitates mitochondrial iron accumulation and colon tumorigenesis. Autophagy. 21:737–753. 2025. View Article : Google Scholar :

3 

Chen YJ, Hong WF, Liu ML, Guo X, Yu YY, Cui YH, Liu TS and Liang L: An integrated bioinformatic investigation of mitochondrial solute carrier family 25 (SLC25) in colon cancer followed by preliminary validation of member 5 (SLC25A5) in tumorigenesis. Cell Death Dis. 13:2372022. View Article : Google Scholar : PubMed/NCBI

4 

Hu JL, Wang W, Lan XL, Zeng ZC, Liang YS, Yan YR, Song FY, Wang FF, Zhu XH, Liao WJ, et al: CAFs secreted exosomes promote metastasis and chemotherapy resistance by enhancing cell stemness and epithelial-mesenchymal transition in colorectal cancer. Mol Cancer. 18:912019. View Article : Google Scholar : PubMed/NCBI

5 

Zhao H, Ming T, Tang S, Ren S, Yang H, Liu M, Tao Q and Xu H: Wnt signaling in colorectal cancer: Pathogenic role and therapeutic target. Mol Cancer. 21:1442022. View Article : Google Scholar : PubMed/NCBI

6 

Tran TQ, Hanse EA, Habowski AN, Li H, Ishak Gabra MB, Yang Y, Lowman XH, Ooi AM, Liao SY, Edwards RA, et al: α-Ketoglutarate attenuates Wnt signaling and drives differentiation in colorectal cancer. Nat Cancer. 1:345–358. 2020. View Article : Google Scholar : PubMed/NCBI

7 

Ren L, Meng L, Gao J, Lu M, Guo C, Li Y, Rong Z and Ye Y: PHB2 promotes colorectal cancer cell proliferation and tumorigenesis through NDUFS1-mediated oxidative phosphorylation. Cell Death Dis. 14:442023. View Article : Google Scholar : PubMed/NCBI

8 

Chen J, Duan S, Wang Y, Ling Y, Hou X, Zhang S, Liu X, Long X, Lan J, Zhou M, et al: MYG1 drives glycolysis and colorectal cancer development through nuclear-mitochondrial collaboration. Nat Commun. 15:49692024. View Article : Google Scholar : PubMed/NCBI

9 

Yun SI, Kim HH, Yoon JH, Park WS, Hahn MJ, Kim HC, Chung CH and Kim KK: Ubiquitin specific protease 4 positively regulates the WNT/β-catenin signaling in colorectal cancer. Mol Oncol. 9:1834–1851. 2015. View Article : Google Scholar : PubMed/NCBI

10 

Wijnhoven P, Konietzny R, Blackford AN, Travers J, Kessler BM, Nishi R and Jackson SP: USP4 auto-deubiquitylation promotes homologous recombination. Mol Cell. 85:6652025. View Article : Google Scholar : PubMed/NCBI

11 

Zhang L, Zhou F, Drabsch Y, Gao R, Snaar-Jagalska BE, Mickanin C, Huang H, Sheppard KA, Porter JA, Lu CX and ten Dijke P: USP4 is regulated by AKT phosphorylation and directly deubiquitylates TGF-β type I receptor. Nat Cell Biol. 14:717–726. 2012. View Article : Google Scholar : PubMed/NCBI

12 

Xing C, Lu XX, Guo PD, Shen T, Zhang S, He XS, Gan WJ, Li XM, Wang JR, Zhao YY, et al: Ubiquitin-specific protease 4-mediated deubiquitination and stabilization of PRL-3 is required for potentiating colorectal oncogenesis. Cancer Res. 76:83–95. 2016. View Article : Google Scholar

13 

Toden S, Zumwalt TJ and Goel A: Non-coding RNAs and potential therapeutic targeting in cancer. Biochim Biophys Acta Rev Cancer. 1875:1884912021. View Article : Google Scholar

14 

Yan H and Bu P: Non-coding RNA in cancer. Essays Biochem. 65:625–639. 2021. View Article : Google Scholar : PubMed/NCBI

15 

Nemeth K, Bayraktar R, Ferracin M and Calin GA: Non-coding RNAs in disease: From mechanisms to therapeutics. Nat Rev Genet. 25:211–232. 2024. View Article : Google Scholar

16 

Wang J, Ma X, Si H, Ma Z, Ma Y, Wang J and Cao B: Role of long non-coding RNA H19 in therapy resistance of digestive system cancers. Mol Med. 27:12021. View Article : Google Scholar : PubMed/NCBI

17 

Shirvaliloo M: LncRNA H19 promotes tumor angiogenesis in smokers by targeting anti-angiogenic miRNAs. Epigenomics. 15:61–73. 2023. View Article : Google Scholar : PubMed/NCBI

18 

Xiu B, Chi Y, Liu L, Chi W, Zhang Q, Chen J, Guo R, Si J, Li L, Xue J, et al: LINC02273 drives breast cancer metastasis by epigenetically increasing AGR2 transcription. Mol Cancer. 18:1872019. View Article : Google Scholar : PubMed/NCBI

19 

Feng YC, Liu XY, Teng L, Ji Q, Wu Y, Li JM, Gao W, Zhang YY, La T, Tabatabaee H, et al: c-Myc inactivation of p53 through the pan-cancer lncRNA MILIP drives cancer pathogenesis. Nat Commun. 11:49802020. View Article : Google Scholar : PubMed/NCBI

20 

He X, Yang T, Lu YW, Wu G, Dai G, Ma Q, Zhang M, Zhou H, Long T, Yan Y, et al: The long noncoding RNA CARDINAL attenuates cardiac hypertrophy by modulating protein translation. J Clin Invest. 134:e1691122024. View Article : Google Scholar : PubMed/NCBI

21 

Yao ZT, Yang YM, Sun MM, He Y, Liao L, Chen KS and Li B: New insights into the interplay between long non-coding RNAs and RNA-binding proteins in cancer. Cancer Commun (Lond). 42:117–140. 2022. View Article : Google Scholar : PubMed/NCBI

22 

Xu Y, Wang J, Deng X, Gao H, Xing F, Ding H, Qu L and Xi Z: USPs and non-coding RNAs: Unraveling their interplay within tumor microenvironment for targeted cancer therapy. Pharmacol Res. 218:1078532025. View Article : Google Scholar : PubMed/NCBI

23 

Xu P, Xiao H, Yang Q, Hu R, Jiang L, Bi R, Jiang X, Wang L, Mei J, Ding F and Huang J: The USP21/YY1/SNHG16 axis contributes to tumor proliferation, migration, and invasion of non-small-cell lung cancer. Exp Mol Med. 52:41–55. 2020. View Article : Google Scholar : PubMed/NCBI

24 

Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 25:402–408. 2001. View Article : Google Scholar

25 

American Veterinary Medical Associationn (AVMA): AVMA guidelines for the euthanasia of animals: 2020 edition. AVMA; Schaumburg, IL: 2020

26 

Morton D, Seymour M, Magill L, Handley K, Glasbey J, Glimelius B, Palmer A, Seligmann J, Laurberg S, Murakami K, et al: Preoperative chemotherapy for operable colon cancer: Mature results of an international randomized controlled trial. J Clin Oncol. 41:1541–1552. 2023. View Article : Google Scholar : PubMed/NCBI

27 

Chalabi M, Verschoor YL, Tan PB, Balduzzi S, Van Lent AU, Grootscholten C, Dokter S, Büller NV, Grotenhuis BA, Kuhlmann K, et al: Neoadjuvant immunotherapy in locally advanced mismatch repair-deficient colon cancer. N Engl J Med. 390:1949–1958. 2024. View Article : Google Scholar : PubMed/NCBI

28 

Chen X, Chen J, Feng W, Huang W, Wang G, Sun M, Luo X, Wang Y, Nie Y, Fan D, et al: FGF19-mediated ELF4 overexpression promotes colorectal cancer metastasis through transactivating FGFR4 and SRC. Theranostics. 13:1401–1418. 2023. View Article : Google Scholar : PubMed/NCBI

29 

Bertocchi A, Carloni S, Ravenda PS, Bertalot G, Spadoni I, Lo Cascio A, Gandini S, Lizier M, Braga D, Asnicar F, et al: Gut vascular barrier impairment leads to intestinal bacteria dissemination and colorectal cancer metastasis to liver. Cancer Cell. 39:708–724.e11. 2021. View Article : Google Scholar : PubMed/NCBI

30 

Tan YT, Lin JF, Li T, Li JJ, Xu RH and Ju HQ: LncRNA-mediated posttranslational modifications and reprogramming of energy metabolism in cancer. Cancer Commun (Lond). 41:109–120. 2021. View Article : Google Scholar :

31 

Bhan A, Soleimani M and Mandal SS: Long noncoding RNA and cancer: A new paradigm. Cancer Res. 77:3965–3981. 2017. View Article : Google Scholar : PubMed/NCBI

32 

Ebrahimi N, Parkhideh S, Samizade S, Esfahani AN, Samsami S, Yazdani E, Adelian S, Chaleshtori SR, Shah-Amiri K, Ahmadi A and Aref AR: Crosstalk between lncRNAs in the apoptotic pathway and therapeutic targets in cancer. Cytokine Growth Factor Rev. 65:61–74. 2022. View Article : Google Scholar : PubMed/NCBI

33 

Wang Y, Lu JH, Wu QN, Jin Y, Wang DS, Chen YX, Liu J, Luo XJ, Meng Q, Pu HY, et al: LncRNA LINRIS stabilizes IGF2BP2 and promotes the aerobic glycolysis in colorectal cancer. Mol Cancer. 18:1742019. View Article : Google Scholar : PubMed/NCBI

34 

Wu N, Jiang M, Liu H, Chu Y, Wang D, Cao J, Wang Z, Xie X, Han Y and Xu B: LINC00941 promotes CRC metastasis through preventing SMAD4 protein degradation and activating the TGF-β/SMAD2/3 signaling pathway. Cell Death Differ. 28:219–232. 2021. View Article : Google Scholar

35 

Guo Y, Jiang Z, Chen Q, Xie D, Zhou Y, Yin W, Wang Z, Wang B, Ren C and Jiang X: Construction and experimental validation of a signature for predicting prognosis and immune infiltration analysis of glioma based on disulfidptosis-related lncRNAs. Front Immunol. 14:12913852023. View Article : Google Scholar : PubMed/NCBI

36 

Lang X, Huang C and Cui H: Prognosis analysis and validation of fatty acid metabolism-related lncRNAs and tumor immune microenvironment in cervical cancer. J Immunol Res. 2022:49544572022. View Article : Google Scholar : PubMed/NCBI

37 

Pan J, Huang Z, Lin H, Cheng W, Lai J and Li J: M7G-Related lncRNAs predict prognosis and regulate the immune microenvironment in lung squamous cell carcinoma. BMC Cancer. 22:11322022. View Article : Google Scholar : PubMed/NCBI

38 

Shin CH, Kim K, Ho CW, Lee JW, Jo MJ, Min KW and Yoon JH: Long noncoding RNAs regulating enzymatic reactions in cancer. Exp Mol Med. 57:1641–1650. 2025. View Article : Google Scholar : PubMed/NCBI

39 

Segal D and Dostie J: The talented LncRNAs: Meshing into transcriptional regulatory networks in cancer. Cancers (Basel). 15:34332023. View Article : Google Scholar : PubMed/NCBI

40 

Mehrad-Majd H, Akhtari J, Haerian MS and Ravanshad Y: Clinicopathological and prognostic value of lncRNA PANDAR expression in solid tumors: Evidence from a systematic review and meta-analysis. J Cell Physiol. 234:4206–4216. 2019. View Article : Google Scholar

41 

Liang C, Liu J, Ge H, Xu Y, Li G and Wu J: The clinicopathological and prognostic value of long non-coding RNA ZEB1-AS1 in solid tumors: A meta-analysis. Clin Chim Acta. 484:91–98. 2018. View Article : Google Scholar : PubMed/NCBI

42 

Qiu GZ, Sun W, Jin MZ, Lin J, Lu PG and Jin WL: The bad seed gardener: Deubiquitinases in the cancer stem-cell signaling network and therapeutic resistance. Pharmacol Ther. 172:127–138. 2017. View Article : Google Scholar

Related Articles

  • Abstract
  • View
  • Download
  • Twitter
Copy and paste a formatted citation
Spandidos Publications style
Lin H, Feng J, Chen P, Hu J, Zhu L and Yuan S: lncRNA AL445238.2‑USP4 axis regulates cell survival and stemness in colon cancer. Int J Oncol 68: 45, 2026.
APA
Lin, H., Feng, J., Chen, P., Hu, J., Zhu, L., & Yuan, S. (2026). lncRNA AL445238.2‑USP4 axis regulates cell survival and stemness in colon cancer. International Journal of Oncology, 68, 45. https://doi.org/10.3892/ijo.2026.5858
MLA
Lin, H., Feng, J., Chen, P., Hu, J., Zhu, L., Yuan, S."lncRNA AL445238.2‑USP4 axis regulates cell survival and stemness in colon cancer". International Journal of Oncology 68.4 (2026): 45.
Chicago
Lin, H., Feng, J., Chen, P., Hu, J., Zhu, L., Yuan, S."lncRNA AL445238.2‑USP4 axis regulates cell survival and stemness in colon cancer". International Journal of Oncology 68, no. 4 (2026): 45. https://doi.org/10.3892/ijo.2026.5858
Copy and paste a formatted citation
x
Spandidos Publications style
Lin H, Feng J, Chen P, Hu J, Zhu L and Yuan S: lncRNA AL445238.2‑USP4 axis regulates cell survival and stemness in colon cancer. Int J Oncol 68: 45, 2026.
APA
Lin, H., Feng, J., Chen, P., Hu, J., Zhu, L., & Yuan, S. (2026). lncRNA AL445238.2‑USP4 axis regulates cell survival and stemness in colon cancer. International Journal of Oncology, 68, 45. https://doi.org/10.3892/ijo.2026.5858
MLA
Lin, H., Feng, J., Chen, P., Hu, J., Zhu, L., Yuan, S."lncRNA AL445238.2‑USP4 axis regulates cell survival and stemness in colon cancer". International Journal of Oncology 68.4 (2026): 45.
Chicago
Lin, H., Feng, J., Chen, P., Hu, J., Zhu, L., Yuan, S."lncRNA AL445238.2‑USP4 axis regulates cell survival and stemness in colon cancer". International Journal of Oncology 68, no. 4 (2026): 45. https://doi.org/10.3892/ijo.2026.5858
Follow us
  • Twitter
  • LinkedIn
  • Facebook
About
  • Spandidos Publications
  • Careers
  • Cookie Policy
  • Privacy Policy
How can we help?
  • Help
  • Live Chat
  • Contact
  • Email to our Support Team