دورية أكاديمية

Identification of New Markers of Angiogenic Sprouting Using Transcriptomics: New Role for RND3.

التفاصيل البيبلوغرافية
العنوان: Identification of New Markers of Angiogenic Sprouting Using Transcriptomics: New Role for RND3.
المؤلفون: Abbey CA; Texas A&M Health, Department of Medical Physiology (C.A.A., S.R., S.C., K.J.B.), Texas A&M School of Medicine, Bryan.; Department of Molecular and Cellular Medicine (C.A.A., C.L.D., A.C., T.M.S., G.B.W., K.J.B.), Texas A&M School of Medicine, Bryan., Duran CL; Department of Molecular and Cellular Medicine (C.A.A., C.L.D., A.C., T.M.S., G.B.W., K.J.B.), Texas A&M School of Medicine, Bryan.; Now with Department of Pathology, Albert Einstein College of Medicine, Bronx, NY (C.L.D.)., Chen Z; Center for Genomic and Precision Medicine, Institute of Biosciences and Technology, Houston, TX (Z.C., Y.C., J.C.)., Chen Y; Center for Genomic and Precision Medicine, Institute of Biosciences and Technology, Houston, TX (Z.C., Y.C., J.C.)., Roy S; Texas A&M Health, Department of Medical Physiology (C.A.A., S.R., S.C., K.J.B.), Texas A&M School of Medicine, Bryan., Coffell A; Department of Molecular and Cellular Medicine (C.A.A., C.L.D., A.C., T.M.S., G.B.W., K.J.B.), Texas A&M School of Medicine, Bryan., Sveeggen TM; Department of Molecular and Cellular Medicine (C.A.A., C.L.D., A.C., T.M.S., G.B.W., K.J.B.), Texas A&M School of Medicine, Bryan.; Now with Department of Cellular and Integrative Physiology, University of Nebraska Medical Center, Omaha (T.M.S.)., Chakraborty S; Texas A&M Health, Department of Medical Physiology (C.A.A., S.R., S.C., K.J.B.), Texas A&M School of Medicine, Bryan., Wells GB; Department of Molecular and Cellular Medicine (C.A.A., C.L.D., A.C., T.M.S., G.B.W., K.J.B.), Texas A&M School of Medicine, Bryan.; Department of Cell Biology and Genetics (G.B.W.), Texas A&M School of Medicine, Bryan., Chang J; Center for Genomic and Precision Medicine, Institute of Biosciences and Technology, Houston, TX (Z.C., Y.C., J.C.)., Bayless KJ; Texas A&M Health, Department of Medical Physiology (C.A.A., S.R., S.C., K.J.B.), Texas A&M School of Medicine, Bryan.; Department of Molecular and Cellular Medicine (C.A.A., C.L.D., A.C., T.M.S., G.B.W., K.J.B.), Texas A&M School of Medicine, Bryan.
المصدر: Arteriosclerosis, thrombosis, and vascular biology [Arterioscler Thromb Vasc Biol] 2024 May; Vol. 44 (5), pp. e145-e167. Date of Electronic Publication: 2024 Mar 14.
نوع المنشور: Journal Article; Research Support, N.I.H., Extramural; Research Support, Non-U.S. Gov't
اللغة: English
بيانات الدورية: Publisher: Lippincott Williams & Wilkins Country of Publication: United States NLM ID: 9505803 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1524-4636 (Electronic) Linking ISSN: 10795642 NLM ISO Abbreviation: Arterioscler Thromb Vasc Biol Subsets: MEDLINE
أسماء مطبوعة: Publication: 1998- : Baltimore, Md. : Lippincott Williams & Wilkins
Original Publication: Dallas, TX : American Heart Association, c1995-
مواضيع طبية MeSH: Gene Expression Profiling*/methods , Human Umbilical Vein Endothelial Cells*/metabolism , Neovascularization, Physiologic*/genetics , Proto-Oncogene Proteins c-fos*/genetics , Proto-Oncogene Proteins c-fos*/metabolism , rho GTP-Binding Proteins*/metabolism , rho GTP-Binding Proteins*/genetics , Transcriptome*, Animals ; Humans ; Mice ; Cells, Cultured ; Cyclooxygenase 2/metabolism ; Cyclooxygenase 2/genetics ; Endothelial Cells/metabolism ; Phenotype ; Signal Transduction ; Single-Cell Analysis ; Snail Family Transcription Factors/metabolism ; Snail Family Transcription Factors/genetics
مستخلص: Background: New blood vessel formation requires endothelial cells to transition from a quiescent to an invasive phenotype. Transcriptional changes are vital for this switch, but a comprehensive genome-wide approach focused exclusively on endothelial cell sprout initiation has not been reported.
Methods: Using a model of human endothelial cell sprout initiation, we developed a protocol to physically separate cells that initiate the process of new blood vessel formation (invading cells) from noninvading cells. We used this model to perform multiple transcriptomics analyses from independent donors to monitor endothelial gene expression changes.
Results: Single-cell population analyses, single-cell cluster analyses, and bulk RNA sequencing revealed common transcriptomic changes associated with invading cells. We also found that collagenase digestion used to isolate single cells upregulated the Fos proto-oncogene transcription factor. Exclusion of Fos proto-oncogene expressing cells revealed a gene signature consistent with activation of signal transduction, morphogenesis, and immune responses. Many of the genes were previously shown to regulate angiogenesis and included multiple tip cell markers. Upregulation of SNAI1 (snail family transcriptional repressor 1), PTGS2 (prostaglandin synthase 2), and JUNB (JunB proto-oncogene) protein expression was confirmed in invading cells, and silencing JunB and SNAI1 significantly reduced invasion responses. Separate studies investigated rounding 3, also known as RhoE, which has not yet been implicated in angiogenesis. Silencing rounding 3 reduced endothelial invasion distance as well as filopodia length, fitting with a pathfinding role for rounding 3 via regulation of filopodial extensions. Analysis of in vivo retinal angiogenesis in Rnd3 heterozygous mice confirmed a decrease in filopodial length compared with wild-type littermates.
Conclusions: Validation of multiple genes, including rounding 3, revealed a functional role for this gene signature early in the angiogenic process. This study expands the list of genes associated with the acquisition of a tip cell phenotype during endothelial cell sprout initiation.
Competing Interests: Disclosures None.
References: Nature. 2018 Jul;559(7714):356-362. (PMID: 29973725)
Trends Cell Biol. 2015 Aug;25(8):459-67. (PMID: 26004869)
Mol Syst Biol. 2019 Jun 19;15(6):e8746. (PMID: 31217225)
Surv Ophthalmol. 2003 May-Jun;48(3):257-93. (PMID: 12745003)
Cell Death Dis. 2020 Aug 10;11(8):695. (PMID: 32826874)
Thromb Res. 2007;120 Suppl 2:S1-6. (PMID: 18023702)
J Exp Clin Cancer Res. 2016 Jan 12;35:6. (PMID: 26754630)
Development. 2011 Nov;138(21):4569-83. (PMID: 21965610)
Circulation. 2020 Nov 10;142(19):1848-1862. (PMID: 32929989)
Trends Cell Biol. 2021 Nov;31(11):888-897. (PMID: 34074577)
Front Cell Dev Biol. 2021 Feb 09;9:589770. (PMID: 33634114)
J Dermatol Sci. 2010 Nov;60(2):105-13. (PMID: 20851575)
Trends Pharmacol Sci. 2001 Apr;22(4):201-7. (PMID: 11282421)
Nat Cell Biol. 2010 Oct;12(10):943-53. (PMID: 20871601)
Nat Med. 2002 Aug;8(8):831-40. (PMID: 12091877)
Front Aging Neurosci. 2022 Sep 01;14:944195. (PMID: 36118693)
Nat Commun. 2016 Jul 20;7:12240. (PMID: 27436424)
Elife. 2020 Jan 24;9:. (PMID: 31976858)
Elife. 2018 May 11;7:. (PMID: 29749927)
Microcirculation. 2016 Feb;23(2):95-121. (PMID: 26614117)
J Cell Commun Signal. 2019 Sep;13(3):291-301. (PMID: 30903604)
Dev Cell. 2020 Mar 23;52(6):779-793.e7. (PMID: 32059774)
Biochem Biophys Res Commun. 2007 Dec 28;364(4):778-82. (PMID: 17964286)
J Cell Biol. 2003 Jun 23;161(6):1163-77. (PMID: 12810700)
Am J Pathol. 1999 Oct;155(4):1281-91. (PMID: 10514410)
Oncogene. 2018 Aug;37(31):4287-4299. (PMID: 29717262)
Am J Physiol Cell Physiol. 2008 Nov;295(5):C1215-29. (PMID: 18787072)
Exp Mol Pathol. 2003 Jun;74(3):282-90. (PMID: 12782016)
J Am Heart Assoc. 2016 Apr 05;5(4):e003336. (PMID: 27048969)
Bioinformatics. 2013 May 15;29(10):1275-82. (PMID: 23589650)
Bioessays. 2010 Nov;32(11):986-92. (PMID: 20836090)
Arterioscler Thromb Vasc Biol. 2015 Feb;35(2):303-8. (PMID: 25425619)
Cell. 2013 Aug 1;154(3):651-63. (PMID: 23911327)
Microcirculation. 2015 Oct;22(7):509-17. (PMID: 26250801)
Angiogenesis. 2018 Nov;21(4):823-836. (PMID: 29951828)
Annu Rev Physiol. 2019 Feb 10;81:483-503. (PMID: 30742787)
Nucleic Acids Res. 2002 Jan 1;30(1):207-10. (PMID: 11752295)
EMBO J. 1999 Feb 15;18(4):934-48. (PMID: 10022836)
Front Cell Dev Biol. 2021 Feb 16;9:642352. (PMID: 33681228)
Proc Soc Exp Biol Med. 1983 Feb;172(2):214-8. (PMID: 6572402)
Breast Cancer Res. 2008;10(2):204. (PMID: 18373885)
Blood. 2010 Nov 11;116(19):4025-33. (PMID: 20705756)
Development. 2013 Oct;140(19):4031-40. (PMID: 24046319)
Cell. 1998 May 29;93(5):705-16. (PMID: 9630216)
Circ Res. 2015 Jan 2;116(1):e1-e10. (PMID: 25348166)
J Biol Chem. 2011 Dec 9;286(49):42017-42026. (PMID: 22002053)
Am J Physiol Endocrinol Metab. 2020 Dec 1;319(6):E961-E980. (PMID: 33044844)
Angiogenesis. 2012 Mar;15(1):151-63. (PMID: 22249946)
Mol Cell Biol. 2015 Sep;35(18):3163-77. (PMID: 26149388)
Cell Death Dis. 2014 Jun 05;5:e1284. (PMID: 24901055)
Proc Natl Acad Sci U S A. 2014 Sep 2;111(35):12865-70. (PMID: 25136137)
Br J Pharmacol. 2000 Jun;130(3):641-9. (PMID: 10821793)
Cancer Cell. 2020 Mar 16;37(3):421. (PMID: 32183954)
Ann Surg. 2011 Sep;254(3):450-6; discussion 456-7. (PMID: 21795970)
Proc Natl Acad Sci U S A. 2023 Jun 6;120(23):e2221742120. (PMID: 37252964)
Oncogene. 2017 Mar;36(11):1525-1536. (PMID: 27641328)
Cell Rep. 2024 Jan 23;43(1):113627. (PMID: 38157296)
Front Cell Dev Biol. 2021 Oct 07;9:702021. (PMID: 34692672)
Proc Natl Acad Sci U S A. 2013 Dec 3;110(49):19802-7. (PMID: 24248345)
Invest Ophthalmol Vis Sci. 1999 Mar;40(3):612-8. (PMID: 10067964)
J Biol Chem. 2000 Oct 20;275(42):32775-82. (PMID: 10922363)
Philos Trans R Soc Lond B Biol Sci. 2017 May 19;372(1720):. (PMID: 28348255)
Nat Cell Biol. 2014 Apr;16(4):309-21. (PMID: 24658686)
Nature. 2011 May 19;473(7347):298-307. (PMID: 21593862)
Reprod Sci. 2022 Nov;29(11):3266-3277. (PMID: 35616875)
J Biol Chem. 1999 Nov 26;274(48):34141-7. (PMID: 10567385)
Sci Rep. 2022 Jan 31;12(1):1655. (PMID: 35102202)
Circ Res. 2003 Mar 7;92(4):378-85. (PMID: 12600898)
Oncogene. 2016 Sep 29;35(39):5155-69. (PMID: 26996666)
Nat Rev Cancer. 2002 Oct;2(10):795-803. (PMID: 12360282)
Proc Natl Acad Sci U S A. 2014 May 13;111(19):7048-53. (PMID: 24782542)
Angiogenesis. 2012 Jun;15(2):287-303. (PMID: 22407449)
J Clin Invest. 1994 Mar;93(3):1095-101. (PMID: 8132748)
Int J Cancer. 2011 Jun 1;128(11):2602-12. (PMID: 20715116)
J Biol Chem. 2003 Nov 28;278(48):47654-9. (PMID: 14500721)
J Cell Sci. 2014 May 1;127(Pt 9):2017-28. (PMID: 24554431)
J Vis Exp. 2013 Jul 09;(77):e50546. (PMID: 23892721)
PLoS One. 2018 Jul 26;13(7):e0201231. (PMID: 30048510)
Expert Rev Mol Diagn. 2007 Mar;7(2):133-47. (PMID: 17331062)
Mol Hum Reprod. 2018 Feb 1;24(2):74-93. (PMID: 29329415)
Oncogene. 2008 May 8;27(21):2989-98. (PMID: 18059339)
Lab Invest. 2018 Apr;98(4):427-438. (PMID: 29330473)
Trends Mol Med. 2011 Jul;17(7):347-62. (PMID: 21481637)
Pharmacol Rev. 2004 Sep;56(3):387-437. (PMID: 15317910)
Dev Biol. 2019 Jul 1;451(1):86-95. (PMID: 30193787)
Curr Eye Res. 2011 Nov;36(11):989-96. (PMID: 21999225)
Genome Biol. 2010;11(10):R106. (PMID: 20979621)
J Clin Invest. 1992 Jan;89(1):97-108. (PMID: 1729286)
J Cell Sci. 2016 Feb 15;129(4):743-56. (PMID: 26769900)
J Immunol. 2005 Sep 1;175(5):2788-92. (PMID: 16116163)
Sci Rep. 2022 Jun 14;12(1):9897. (PMID: 35701452)
Front Genet. 2019 Apr 05;10:317. (PMID: 31024627)
J Theor Biol. 2008 Jan 7;250(1):25-36. (PMID: 18028963)
Genome Biol. 2022 Dec 9;23(1):252. (PMID: 36494864)
Nat Rev Immunol. 2013 Jun;13(6):438-51. (PMID: 23702979)
J Cell Biol. 2006 Dec 18;175(6):981-91. (PMID: 17158955)
Matrix Biol. 2014 Sep;38:36-47. (PMID: 25038525)
Am J Reprod Immunol. 2010 Feb;63(2):93-103. (PMID: 20039862)
Front Cardiovasc Med. 2020 Apr 30;7:52. (PMID: 32426372)
J Cell Sci. 2017 Mar 1;130(5):916-926. (PMID: 28096474)
Front Cardiovasc Med. 2019 Nov 26;6:165. (PMID: 31850371)
Cell Rep. 2021 Jun 15;35(11):109253. (PMID: 34133923)
J Clin Invest. 1997 May 1;99(9):2254-9. (PMID: 9151799)
Microcirculation. 1998;5(2-3):173-8. (PMID: 9789257)
J Clin Invest. 2014 Jan;124(1):209-21. (PMID: 24355925)
Front Immunol. 2017 Dec 11;8:1750. (PMID: 29321777)
Sci Rep. 2015 Oct 13;5:15007. (PMID: 26458334)
Clin Exp Rheumatol. 2023 Aug;41(8):1618-1631. (PMID: 37246768)
Int J Mol Sci. 2021 Feb 05;22(4):. (PMID: 33562512)
Dev Cell. 2009 Feb;16(2):222-31. (PMID: 19217424)
J Virol. 2012 Aug;86(16):8559-67. (PMID: 22647700)
Angiogenesis. 2021 May;24(2):311-326. (PMID: 34061284)
Biomedicines. 2022 Jun 30;10(7):. (PMID: 35884862)
Arterioscler Thromb Vasc Biol. 2023 Jun;43(6):927-942. (PMID: 37078291)
Cancer Cell. 2021 Apr 12;39(4):480-493.e6. (PMID: 33513345)
Mol Cell Endocrinol. 2013 Jul 15;374(1-2):73-81. (PMID: 23664860)
Am J Reprod Immunol. 2004 Aug;52(2):147-63. (PMID: 15274657)
Bioinformatics. 2013 Jan 1;29(1):15-21. (PMID: 23104886)
Br J Cancer. 2013 Oct 15;109(8):2248-58. (PMID: 24045665)
Development. 2014 Mar;141(6):1342-53. (PMID: 24553288)
Biol Open. 2013 Feb 15;2(2):210-6. (PMID: 23430146)
Nat Methods. 2017 Sep 29;14(10):935-936. (PMID: 28960196)
Int J Cancer. 2014 May 15;134(10):2294-304. (PMID: 24174333)
Int J Dev Biol. 2011;55(4-5):495-503. (PMID: 21732273)
Oncogene. 2012 Jun 21;31(25):3098-110. (PMID: 22020339)
Development. 2013 Jul;140(14):3051-61. (PMID: 23785053)
Science. 1999 Apr 30;284(5415):770-6. (PMID: 10221902)
Cells. 2020 Dec 22;10(1):. (PMID: 33375076)
Angiogenesis. 2018 May;21(2):215-228. (PMID: 29327326)
Front Endocrinol (Lausanne). 2020 Mar 31;11:172. (PMID: 32296395)
Cancer Microenviron. 2012 Dec;5(3):237-47. (PMID: 22833050)
Angiogenesis. 2020 May;23(2):179-192. (PMID: 31754927)
Curr Opin Cell Biol. 2010 Oct;22(5):617-25. (PMID: 20817428)
J Biol Chem. 2013 Oct 18;288(42):30720-30733. (PMID: 24005669)
Proc Natl Acad Sci U S A. 2014 Jun 10;111(23):E2384-93. (PMID: 24912173)
Thromb Haemost. 2001 Jul;86(1):308-15. (PMID: 11487019)
Cell. 2009 Jun 12;137(6):1124-35. (PMID: 19524514)
Cell Metab. 2020 Apr 7;31(4):862-877.e14. (PMID: 32268117)
Ann N Y Acad Sci. 1993 Nov 30;696:197-204. (PMID: 7509130)
Philos Trans R Soc Lond B Biol Sci. 2021 Mar 29;376(1821):20190753. (PMID: 33550953)
Nat Protoc. 2009;4(12):1888-98. (PMID: 20010936)
Nat Commun. 2017 Dec 15;8(1):2149. (PMID: 29247167)
J Vasc Res. 2007;44(4):283-91. (PMID: 17406120)
Nat Cell Biol. 2016 Dec;18(12):1292-1301. (PMID: 27870831)
Cold Spring Harb Perspect Med. 2012 Feb;2(2):a006601. (PMID: 22355796)
Arterioscler Thromb Vasc Biol. 2009 May;29(5):639-49. (PMID: 19265031)
J Cell Mol Med. 2018 Feb;22(2):1214-1223. (PMID: 29083110)
Nat Commun. 2020 Jul 30;11(1):3798. (PMID: 32732867)
Front Cardiovasc Med. 2020 Mar 31;7:42. (PMID: 32296715)
Mol Cell Biol. 1998 Aug;18(8):4761-71. (PMID: 9671486)
Blood. 2010 Aug 5;116(5):829-40. (PMID: 20404134)
Matrix Biol. 2015 May-Jul;44-46:38-45. (PMID: 25698314)
Cell Mol Life Sci. 2021 Feb;78(4):1329-1354. (PMID: 33078209)
Cell. 1999 Jul 23;98(2):147-57. (PMID: 10428027)
J Biol Chem. 2010 Dec 24;285(52):40624-34. (PMID: 20947498)
Compr Physiol. 2015 Dec 15;6(1):169-86. (PMID: 26756630)
Cancer Res. 1997 May 1;57(9):1625-9. (PMID: 9134996)
Sci Rep. 2022 Jul 29;12(1):13065. (PMID: 35906287)
Sci Adv. 2020 Jul 29;6(31):eaaz7815. (PMID: 32923607)
Cancer Res. 2018 May 1;78(9):2370-2382. (PMID: 29449267)
Compr Physiol. 2017 Dec 12;8(1):153-235. (PMID: 29357127)
Genome Biol. 2019 Oct 17;20(1):210. (PMID: 31623682)
PLoS Comput Biol. 2009 Oct;5(10):e1000549. (PMID: 19876379)
معلومات مُعتمدة: R01 HL095786 United States HL NHLBI NIH HHS; R01 HL141215 United States HL NHLBI NIH HHS; R01 HL148133 United States HL NHLBI NIH HHS; R01 HL150124 United States HL NHLBI NIH HHS
فهرسة مساهمة: Keywords: angiogenesis; cell differentiation; collagenase; immune evasion; morphogenesis; three-dimensional cell culture; vascular endothelial cell
المشرفين على المادة: EC 1.14.99.1 (Cyclooxygenase 2)
0 (FOS protein, human)
0 (Proto-Oncogene Proteins c-fos)
EC 3.6.5.2 (rho GTP-Binding Proteins)
0 (SNAI1 protein, human)
0 (Snail Family Transcription Factors)
EC 3.6.5.2 (RND3 protein, human)
EC 3.6.1.- (Rnd3 protein, mouse)
تواريخ الأحداث: Date Created: 20240314 Date Completed: 20240424 Latest Revision: 20240607
رمز التحديث: 20240607
مُعرف محوري في PubMed: PMC11043006
DOI: 10.1161/ATVBAHA.123.320599
PMID: 38482696
قاعدة البيانات: MEDLINE
الوصف
تدمد:1524-4636
DOI:10.1161/ATVBAHA.123.320599