Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2023 Jan 10:12:1072276.
doi: 10.3389/fonc.2022.1072276. eCollection 2022.

Tissue mechanics modulate PCNP expression in oral squamous cell carcinomas with different differentiation

Leyang Zhang  1   2 , Dingcheng Guo  1 , Junjie Shen  1 , Yayuan Zheng  1 , Junkai Zhai  1 , Ruiping Li  1   3 , Dengqi He  2 , Baoping Zhang  1   3   4   5   6
Affiliations

Tissue mechanics modulate PCNP expression in oral squamous cell carcinomas with different differentiation

Leyang Zhang et al. Front Oncol. .

Abstract

Background: PEST-containing nuclear protein (PCNP), a novel zinc finger protein, participates in cell cycle regulation. Previous studies have confirmed that PCNP plays a role in mediating cellular development and invasion in a variety of cancer types. However, the relationship between PCNP expression and the occurrence and development of oral squamous cell carcinoma (OSCC) requires further exploration. In this study, we used biological atomic force microscopy to examine the histomorphological and mechanical properties of OSCC to explore the relationship between PCNP expression and differentiation of OSCC.

Methods: Seventy-seven OSCC samples with varying degrees of differentiation were selected for hematoxylin and eosin staining, immunohistochemistry, and cellular mechanical measurement. The expression of PCNP and the mechanical properties such as stiffness and roughness of the tissue interface in OSCC samples were investigated. The Kaplan-Meier survival curve was utilized to assess the relationship of PCNP expression with patient survival.

Results: The level of PCNP was significantly higher in well-differentiated OSCC than in moderately and poorly differentiated OSCC (P < 0.001). High expression of PCNP was specifically associated with higher tumor differentiation, lack of lymph node metastasis, and lower tumor node metastasis stage (all P < 0.05). Patients with high PCNP expression had a higher survival rate than those with low PCNP expression. The average variation of stiffness within a single tissue ranged from 347 kPa to 539 kPa. The mean surface roughness of highly, moderately, and poorly differentiated OSCC and paraneoplastic tissues were 795.53 ± 47.2 nm, 598.37 ± 45.76 nm, 410.16 ± 38.44 nm, and 1010.94 ± 119.07 nm, respectively. Pearson correlation coefficient demonstrated a positive correlation between PCNP expression and tissue stiffness of OSCC (R = 0.86, P < 0.001).

Conclusion: The expression of PCNP was positively correlated with patient survival, tumor differentiation, and mechanical properties of tissue interfaces. PCNP is a potential biomarker for the early diagnosis and staging of OSCC. Furthermore, determination of the mechanical properties of the tissue interface could provide further useful information required for the detection and differentiation of OSCC.

Keywords: OSCC (oral squamous cell carcinoma); PEST-containing nuclear protein (PCNP); biomarker; prognosis; tissue interface mechanics.

PubMed Disclaimer

Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
Hematoxylin and eosin staining of OSCC. (A–C) Well differentiation OSCC in 10×, 20×, 40×. (D–F), Moderate differentiation OSCC in 10×, 20×, 40×. (G–I) Poor differentiation OSCC in 10×, 20×, 40×. (J–L) Paracancerous samples in 10×, 20×, 40×.
Figure 2
Figure 2
Immunohistochemical staining was performed to detect the expression of PCNP at different stages of OSCC. (A–C) Well differentiation OSCC in 10×, 20×, 40×. (D–F) Moderate differentiation OSCC in 10×, 20×, 40×. (G–I) Poor differentiation OSCC in 10×, 20×, 40×. (J–L) Paracancerous samples in 10×, 20×, 40×.
Figure 3
Figure 3
Average optical density of PCNP in well, moderately, and poorly differentiated OSCC. Well-differentiated OSCC had high expression in IHC (*P < 0.05).
Figure 4
Figure 4
PCNP mRNA expression in well, moderately, and poorly differentiated OSCC (*P < 0.05, ***P < 0.001).
Figure 5
Figure 5
Kaplan-Meier survival curves based on PCNP expression (low expression, green line; high expression, pink line). (A) High and low expression of PCNP. (B) Kaplan-Meier survival curves.
Figure 6
Figure 6
Surface morphology of OSCC tissue sections via AFM detection. Poorly differentiated tissues had irregular morphology. (A) V Deflection, Head height measured and 3D images of well differentiation OSCC. (B) V Deflection, Head height measured and 3D images of moderate differentiation OSCC. (C) V Deflection, Head height measured and 3D images of poor differentiation OSCC. (D) V Deflection, Head height measured and 3D images of paracancerous samples.
Figure 7
Figure 7
Surface roughness of well, moderately, and poorly differentiated OSCC. Results represent the mean ± SD in histogram (*P < 0.05).
Figure 8
Figure 8
Average tissue stiffness tested by Bio-AFM. Well-differentiated OSCC had a higher Young’s modulus than moderately and poorly differentiated OSCC (kPa, P < 0.05).
Figure 9
Figure 9
Correlation analysis between tissue stiffness of OSCC and PCNP expression. (P < 0.001, R = 0.86).
See this image and copyright information in PMC

Similar articles

See all similar articles

Cited by

References

    1. Biamonte F, Buffone C, Santamaria G, Battaglia AM, Mignogna C, Fortunato L, et al. . Gene expression analysis of autofluorescence margins in leukoplakia and oral carcinoma: A pilot study. Oral Dis (2021) 27(2):193–203. doi: 10.1111/odi.13525 - DOI - PubMed
    1. Jiang S, Dong Y. Human papillomavirus and oral squamous cell carcinoma: A review of hpv-positive oral squamous cell carcinoma and possible strategies for future. Curr problems Cancer (2017) 41(5):323–7. doi: 10.1016/j.currproblcancer.2017.02.006 - DOI - PubMed
    1. Jiang Y, Li T, Wu Y, Xu H, Xie C, Dong Y, et al. . Gpr39 overexpression in oscc promotes yap-sustained malignant progression. J Dental Res (2020) 99(8):949–58. doi: 10.1177/0022034520915877 - DOI - PubMed
    1. Coppola N, Mignogna MD, Rivieccio I, Blasi A, Bizzoca ME, Sorrentino R, et al. . Current knowledge, attitudes, and practice among health care providers in oscc awareness: Systematic review and meta-analysis. Int J Environ Res And Public Health (2021) 18(9):4506. doi: 10.3390/ijerph18094506 - DOI - PMC - PubMed
    1. Zeng J-j, Tang Z-g, Zou J, Yu J-g. Black phosphorous nanosheets-gold nanoparticles-cisplatin for photothermal/photodynamic treatment of oral squamous cell carcinoma. Trans nonferrous metals Soc China (2021) 31(9):2812–22. doi: 10.1016/S1003-6326(21)65695-9 - DOI

LinkOut - more resources