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Cited by 3Mesenchymal stem cell researchConnective Tissue Growth Factor ResearchAngiogenesis and VEGF in Cancer

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Knockdown SENP1 Suppressed the Angiogenic Potential of Mesenchymal Stem Cells by Impacting CXCR4-Regulated MRTF-A SUMOylation and CCN1 Expression

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Zhang, Rui, Liu, Qingxi, Lyu, Cuicui, Gao, Xing, Ma, Wenjian·2023·Biomedicines
DOI 10.3390/biomedicines11030914PMC PMC10046070
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Abstract

The angiogenic potential of mesenchymal stem cells (MSCs) is critical for adult vascular regeneration and repair, which is regulated by various growth factors and cytokines. In the current study, we report that knockdown SUMO-specific peptidase 1 (SENP1) stimulated the SUMOylation of MRTF-A and prevented its translocation into the nucleus, leading to downregulation of the cytokine and angiogenic factor CCN1, which significantly impacted MSC-mediated angiogenesis and cell migration. Further studies showed that SENP1 knockdown also suppressed the expression of a chemokine receptor CXCR4, and overexpression of CXCR4 could partially abrogate MRTF-A SUMOylation and reestablish the CCN1 level. Mutation analysis confirmed that SUMOylation occurred on three lysine residues (Lys-499, Lys-576, and Lys-624) of MRTF-A. In addition, SENP1 knockdown abolished the synergistic co-activation of CCN1 between MRTF-A and histone acetyltransferase p300 by suppressing acetylation on histone3K9, histone3K14, and histone4. These results revealed an important signaling pathway to regulate MSC differentiation and angiogenesis by MRTF-A SUMOylation involving cytokine/chemokine activities mediated by CCN1 and CXCR4, which may potentially impact a variety of cellular processes such as revascularization, wound healing, and progression of cancer.

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Figure 1 SENP1 participates in arterial-specific endothelial differentiation of hMSCs. (A) MSC-differentiated EC cells (CD31- and KDR-positive) were sorted at 7 days and cultured in EDM media with a purity of 99.54%. (B) Arterial-specific marker genes (Dll4, EphrinB2, Hey2, and Notch1) were examined in obtained ECs by qRT-PCR. (C,D) The expression changes of SUMO1-2 and SENP1-2 during endothelial differentiation were determined by qRT-PCR. Bar graphs are shown as the mean ± SD with individual points from three independent experiments (p values were indicated in the graph, individual data points were shown as scattered black dots).
Figure 1 SENP1 participates in arterial-specific endothelial differentiation of hMSCs. (A) MSC-differentiated EC cells (CD31- and KDR-positive) were sorted at 7 days and cultured in EDM media with a purity of 99.54%. (B) Arterial-specific marker genes (Dll4, EphrinB2, Hey2, and Notch1) were examined in obtained ECs by qRT-PCR. (C,D) The expression changes of SUMO1-2 and SENP1-2 during endothelial differentiation were determined by qRT-PCR. Bar graphs are shown as the mean ± SD with individual points from three independent experiments (p values were indicated in the graph, individual data points were shown as scattered black dots).CC BY · PubMed Central
Figure 2 SENP1 stable knockdown suppressed endothelial-specific differentiation of hMSCs and led to reduced migration and angiogenesis capacity. (A) Stable knockdown cell lines of the SENP1 gene were generated by lentivirus-based RNAi. (B) DiI-Ac-LDL uptake analysis of hMSCsshSENP1 and hMSCsshCtrl. (C) Immunofluorescence detection of endothelial marker KDR in hMSCsshSENP1 and hMSCsshCtrl. (D) Cell migration determined by wound healing assay, and the migration rate was quantified by measuring the scratch gap width after 24 h of cell culture. (E) The invasion capacity of hMSCsshSENP1 and hMSCsshCtrl was determined by transwell chamber assay, and the migration rate was quantified by measuring the percentage of cells that migrated across the membrane after 24 h of cell culture. (F) Angiogenesis determination by Matrigel based on the formation of capillary-like structures. (G) The protein expression of arterial-specific genes Dll4, EphrinB2, Hey2, and Notch1 in hMSCsshSENP1 and hMSCsshCtrl and quantification. Experiments were repeated three times, and quantitation is shown as the means ± SD from three independent experiments (p values were indicated in the graph, and individual data points were shown as scattered black dots).
Figure 2 SENP1 stable knockdown suppressed endothelial-specific differentiation of hMSCs and led to reduced migration and angiogenesis capacity. (A) Stable knockdown cell lines of the SENP1 gene were generated by lentivirus-based RNAi. (B) DiI-Ac-LDL uptake analysis of hMSCsshSENP1 and hMSCsshCtrl. (C) Immunofluorescence detection of endothelial marker KDR in hMSCsshSENP1 and hMSCsshCtrl. (D) Cell migration determined by wound healing assay, and the migration rate was quantified by measuring the scratch gap width after 24 h of cell culture. (E) The invasion capacity of hMSCsshSENP1 and hMSCsshCtrl was determined by transwell chamber assay, and the migration rate was quantified by measuring the percentage of cells that migrated across the membrane after 24 h of cell culture. (F) Angiogenesis determination by Matrigel based on the formation of capillary-like structures. (G) The protein expression of arterial-specific genes Dll4, EphrinB2, Hey2, and Notch1 in hMSCsshSENP1 and hMSCsshCtrl and quantification. Experiments were repeated three times, and quantitation is shown as the means ± SD from three independent experiments (p values were indicated in the graph, and individual data points were shown as scattered black dots).CC BY · PubMed Central
Figure 3 SUMO1 modification of MRTF-A after SENP1 knockdown, and the impact of CXCR4. (A) MRTF-A SUMOylation analyzed by Western blotting in hMSCsshSENP1 and hMSCsshCtrl after EDM-induced differentiation. (B) Immunofluorescence detection of MRTF-A cellular localization. (C) Co-immunoprecipitation analysis to determine the conjugation between MRTF-A and SUMO1. (D,E) The expression of CXCR4 in hMSCsshSENP1 and hMSCsshCtrl determined by mRNA level and protein expression. (F) The expression of CXCR4 analyzed by flow cytometry, which was represented by a green peak for CXCR4- cells and a red-brown peak for CXCR4+ cells. (G) Over-expressing CXCR4 partially abrogated the impact of SENP1 knockdown on MRTF-A SUMOylation and CCN1 expression. Quantitation is shown as the means ± SD (p values are as indicated, n = 3. Individual data points were shown as scattered black dots).
Figure 3 SUMO1 modification of MRTF-A after SENP1 knockdown, and the impact of CXCR4. (A) MRTF-A SUMOylation analyzed by Western blotting in hMSCsshSENP1 and hMSCsshCtrl after EDM-induced differentiation. (B) Immunofluorescence detection of MRTF-A cellular localization. (C) Co-immunoprecipitation analysis to determine the conjugation between MRTF-A and SUMO1. (D,E) The expression of CXCR4 in hMSCsshSENP1 and hMSCsshCtrl determined by mRNA level and protein expression. (F) The expression of CXCR4 analyzed by flow cytometry, which was represented by a green peak for CXCR4- cells and a red-brown peak for CXCR4+ cells. (G) Over-expressing CXCR4 partially abrogated the impact of SENP1 knockdown on MRTF-A SUMOylation and CCN1 expression. Quantitation is shown as the means ± SD (p values are as indicated, n = 3. Individual data points were shown as scattered black dots).CC BY · PubMed Central
Figure 4 The correlation between CCN1 transactivation and MRTF-A SUMOylation. (A) The three putative SUMOylation sites of MRTF-A are located within amino acids 471-630. (B) Confirmation of SUMO-binding sites with specific point mutations (K499, K576, and K624) of MRTF-A together with shSENP1. The whole cell lysates were subjected to western immunoblotting with an anti-MRTF-A specific antibody. (C) SUMO-1 specific SUMOylation of MRTF-A was confirmed by transient transfection with conjugation-defective SUMO-1 (∆GG) HAECs. (D,E) Increased expression of CCN1 following disruption of SUMOylation by the transient introduction of K499/576/624R mutations examined by qRT-PCR and western blot. (F) Luciferase analysis of CCN1 activation in WT and lysin mutants of MRTF-A. (G,H) Abolishing SUMOylation with conjugation-defective SUMO-1 (∆GG) led to increased expression of CCN1 as examined by qRT-PCR and western blot, and transactivation as determined by luciferase assay. The signs ‘+’ means present and ‘−’ means absent for the conditions indicated in each graph. Quantitation is shown as the means ± SD (p values are as indicated, n = 3. Individual data points were shown as scattered black dots).
Figure 4 The correlation between CCN1 transactivation and MRTF-A SUMOylation. (A) The three putative SUMOylation sites of MRTF-A are located within amino acids 471-630. (B) Confirmation of SUMO-binding sites with specific point mutations (K499, K576, and K624) of MRTF-A together with shSENP1. The whole cell lysates were subjected to western immunoblotting with an anti-MRTF-A specific antibody. (C) SUMO-1 specific SUMOylation of MRTF-A was confirmed by transient transfection with conjugation-defective SUMO-1 (∆GG) HAECs. (D,E) Increased expression of CCN1 following disruption of SUMOylation by the transient introduction of K499/576/624R mutations examined by qRT-PCR and western blot. (F) Luciferase analysis of CCN1 activation in WT and lysin mutants of MRTF-A. (G,H) Abolishing SUMOylation with conjugation-defective SUMO-1 (∆GG) led to increased expression of CCN1 as examined by qRT-PCR and western blot, and transactivation as determined by luciferase assay. The signs ‘+’ means present and ‘−’ means absent for the conditions indicated in each graph. Quantitation is shown as the means ± SD (p values are as indicated, n = 3. Individual data points were shown as scattered black dots).CC BY · PubMed Central
Figure 5 SENP1 knockdown inhibited the acetylation of CCN1 by P300. HAECs were co-transfected with MRTF-A, P300, and shSENP1. (A,B) The expression of CCN1 were examined by qRT-PCR and Western blot. (C) CCN1 transactivation was analyzed using luciferase assay after 24 h transfection of MRTF-A, P300, shENP1, and CCN1 promoter-Luc plasmids into HAECs. (D–F) ChIP assays were performed in HAECs after transfection, and cross-linked chromatin was immunoprecipitated with specific anti-acetyl-h3K9/h3K14 /h4 antibodies and IgG antibody as a negative control. The signs ‘+’ means present and ‘−’ means absent for the conditions indicated in each graph. Quantitation is shown as the means ± SD (p values are as indicated, n = 3. Individual data points were shown as scattered black dots).
Figure 5 SENP1 knockdown inhibited the acetylation of CCN1 by P300. HAECs were co-transfected with MRTF-A, P300, and shSENP1. (A,B) The expression of CCN1 were examined by qRT-PCR and Western blot. (C) CCN1 transactivation was analyzed using luciferase assay after 24 h transfection of MRTF-A, P300, shENP1, and CCN1 promoter-Luc plasmids into HAECs. (D–F) ChIP assays were performed in HAECs after transfection, and cross-linked chromatin was immunoprecipitated with specific anti-acetyl-h3K9/h3K14 /h4 antibodies and IgG antibody as a negative control. The signs ‘+’ means present and ‘−’ means absent for the conditions indicated in each graph. Quantitation is shown as the means ± SD (p values are as indicated, n = 3. Individual data points were shown as scattered black dots).CC BY · PubMed Central
Figure 6 A model for the regulation of MRTF-A by SUMOylation. MRTF-A is sequestered in the cytoplasm by SUMOylation in MSCs. When there is a need for differentiation toward angiogenesis, SENP1 is activated by certain regulation factors to induce MRTF-A deSUMOylation, which makes MRTF-A relocate into the nucleus. By cooperating with P300 and SRF on the CArG box, the angiogenic factor CCN1 is transactivated and initiates the angiogenesis process. CXCR4 likely plays a regulatory role on upstream of MRTF-A SUMOylation, but the detailed interactions are yet to be elucidated.
Figure 6 A model for the regulation of MRTF-A by SUMOylation. MRTF-A is sequestered in the cytoplasm by SUMOylation in MSCs. When there is a need for differentiation toward angiogenesis, SENP1 is activated by certain regulation factors to induce MRTF-A deSUMOylation, which makes MRTF-A relocate into the nucleus. By cooperating with P300 and SRF on the CArG box, the angiogenic factor CCN1 is transactivated and initiates the angiogenesis process. CXCR4 likely plays a regulatory role on upstream of MRTF-A SUMOylation, but the detailed interactions are yet to be elucidated.CC BY · PubMed Central

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Metadata

Authors
Zhang, R., Liu, Q., Lyu, C., Gao, X., & Ma, W.
Affiliations
  • Nankai University (CN)
  • Qilu University of Technology (CN)
  • Tianjin University of Science and Technology (CN)
Corresponding author
  • Liu, Qingxi
  • Ma, Wenjian
ORCID
Venue
Biomedicines
Publisher
MDPI AG
Published
2023-03-15
Volume
11
Issue
3
Pages
914
ISSN
2227-9059 (ISSN-L)
DOI
10.3390/biomedicines11030914
PMC
PMC10046070
OpenAlex
W4327595726
Cited by
3
References
2
Citations by year
2025: 1 · 2024: 2
FWCI
0.52
Type
journal article
Language
en
Open access
Licence
Locations
  • Biomedicines (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • National Key R&D Program of China (2018YFA0901702, TJYXZDXK-056B, 2019GSF107088, ZR2020MC077, ZR202111220001)
  • Tianjin Key Medical Discipline (Specialty) Construction Project (2018YFA0901702, TJYXZDXK-056B, 2019GSF107088, ZR2020MC077, ZR202111220001)
  • Shandong Key R&D Program (2018YFA0901702, TJYXZDXK-056B, 2019GSF107088, ZR2020MC077, ZR202111220001)
  • National Science Foundation of Shandong (2018YFA0901702, TJYXZDXK-056B, 2019GSF107088, ZR2020MC077, ZR202111220001)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Mesenchymal stem cell research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Connective Tissue Growth Factor Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
Keywords
SENP1, MRTF-A, SUMOylation, CYR61, CXCR4, mesenchymal stem cells, angiogenesis, cell migration, P300, histone acetylation, nuclear translocation, lysine residues, vascular regeneration

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