Research Article
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Abnormal levels of serum N-terminal propeptide of collagen type IV (PIVNP) in women one year after preeclampsia

Year 2023, Volume: 40 Issue: 3, 509 - 514, 30.09.2023

Abstract

Proteins of the extracellular matrix (ECM) play an important role in normal pregnancy and preeclampsia (PE). Type IV collagen (COL4) is a major ECM structural element, uniquely presented in basement membranes. The N-terminal propeptide of collagen type IV (PIVNP) is a marker of COL4 synthesis. In the present study, we determined serum PIVNP levels in women one year after PE and tested whether PIVNP is related to hypertension development after preeclamptic pregnancy. The current research examined 32 women one year after PE (mean age 25.3±6.3 years) and a control group of 20 women one year after normal pregnancy (mean age 25.6±5.6 years). The enzyme-linked immunosorbent assay (ELISA) was used to determine concentrations of PIVNP. We found that at 1 year after delivery, 38.46% of women who suffered PE had developed arterial hypertension (AH), and 5.77% had developed diabetes mellitus. Women who had normal pregnancies developed neither AH nor diabetes mellitus 1 year after delivery. The distribution of women who had developed AH after preeclamptic pregnancy was as follows: Grade I AH-7; Grade II AH-4; and Grade III AH- 2. Serum PIVNP levels in women one year after PE were statistically significantly lower than in women one year after normal pregnancy: 0.26 (0.1÷0.65) vs. 0.45 ng/ml (0.3÷0.6) (KW= 5.342; p=0.02). PIVNP showed a correlation with creatinine (r= -0.26; p=0.05). Hypertensive women one year after PE showed the lowest levels of serum PIVNP.Our data showed decreased levels of PIVNP in the sera of women one year after PE. This finding demonstrated altered COL4 turnover after preeclamptic pregnancy. The diminished COL4 synthesis might play an important role in persistent vascular wall injury and dysfunction postpartum. We suggest that PIVNP might be involved in the pathogenic mechanisms determining the development of hypertension postpartum.

Supporting Institution

Medical University- Pleven, Bulgaria

Project Number

The research is supported by the Bulgarian Ministry of Education and Science under the national Program “Young Scientists and Postdoctoral Students-2”.

References

  • 1. ACOG Practice Bulletin No. 202: Gestational Hypertension and Preeclampsia. Obstet Gynecol. 2019 Jan;133(1):1.
  • 2. Uzan J, Carbonnel M, Piconne O, Asmar R, Ayoubi JM. Pre-eclampsia: pathophysiology, diagnosis, and management. Vasc Health Risk Manag. 2011; 7: 467–474.
  • 3. 3. Eiland E, Nzerue C, Faulkner M. Preeclampsia. J Pregnancy. Jul 11 2012; 586578.
  • 4. Wu P, Haththotuwa R, Kwok CS, Babu A, Kotronias RA, Rushton C, Zaman A, Fryer AA, Kadam U, Chew-Graham CA, Mamas MA. Preeclampsia and Future Cardiovascular Health: A Systematic Review and Meta-Analysis. Circ Cardiovasc Qual Outcomes. 2017 Feb;10(2):e003497.
  • 5. Laviades C, Varo N, Fernandez J, et al. Abnormalities of the extracellular degradation of collagen type I in essential hypertension. Circulation 1998: 535-540.
  • 6. Berk BC, Fujiwara K, Lehoux S. ECM remodeling in hypertensive heart disease. J Clin Invest. 2007 Mar;117(3):568-75.
  • 7. Gelse, K. Collagens—Structure, function, and biosynthesis. Adv. Drug Deliv. Rev. 2003, 55, 1531–1546.
  • 8. Morillas P, Quiles J, de Andrade H, et al. Circulating biomarkers of collagen metabolism in arterial hypertension: relevance of target organ damage. J Hypertens. 2013; 31: 1611-1617.
  • 9. Kühn K. Basement membrane (type IV) collagen. Matrix Biol. 1995 Feb;14(6):439-45.
  • 10. Mansell JP, Bailey AJ. Collagen Metabolism. In Encyclopedia of Endocrine Diseases. Elsevier: Amsterdam, The Netherlands, 2004; pp. 520–529.
  • 11. Henriksen, K.; Karsdal, M.A. Type I Collagen. In Biochemistry of Collagens, Laminins and Elastin Structure, Function and Biomarkers, 1st ed.; Karsdal, M.A., Ed.; Academic Press: Cambridge, MA, USA, 2016; Chapter 1; pp. 1–11.
  • 12. Sand, J.M.B.; Genovese, F.; Gudmann, N.S.; Karsdal, M.A. Type IV collagen. In Biochemistry of Collagens, Laminins and Elastin, 2nd ed.; Karsdal, M.A., Ed.; Elsevier: Amsterdam, The Netherlands, 2019; Chapter 4; pp. 37–49.
  • 13. O'Connor BB, Pope BD, Peters MM, Ris-Stalpers C, Parker KK. The role of extracellular matrix in normal and pathological pregnancy: Future applications of microphysiological systems in reproductive medicine. Exp Biol Med (Maywood). 2020 Jul;245(13):1163-1174.
  • 14. Russell DL, Salustri A. Extracellular matrix of the cumulus-oocyte complex. Semin Reprod Med 2006; 24:217–27. 15. Familiari G, Heyn R, Relucenti M, et al. Structural changes of the zona pellucida during fertilization and embryo development. Front Biosci 2008; 13:6730–51.
  • 16. Dong C, Lv Y. Application of Collagen Scaffold in Tissue Engineering: Recent Advances and New Perspectives. Polymers (Basel). 2016 Feb 4;8(2):42.
  • 17. Yamano H, Lambert-Messerlian GM, Silver HM, Kudo R. Maternal serum levels of type I and type III procollagen peptides in preeclamptic pregnancy. Matern Fetal Med. 2001; 10(1): 40-3.
  • 18. Schuppan D. Connective tissue polypeptides in serum as parameters to monitor antifibrotic treatment in hepatic fibrogenesis. J Hepatol. 1991;13 Suppl 3:S17-25.
  • 19. Pereira R.D., De Long N.E., Wang R.C., Yazdi F.T., Holloway A.C., Raha S. Angiogenesis in the placenta: The role of reactive oxygen species signaling. BioMed Res. Int. 2015;2015:814543.
  • 20. Benschop L, Duvekot JJ, Versmissen J, van Broekhoven V, Steegers EAP, Roeters van Lennep JE. Blood Pressure Profile 1 Year After Severe Preeclampsia. Hypertension. 2018 Mar;71(3):491-498.
  • 21. Smith GN, Walker MC, Liu A, Wen SW, Swansburg M, Ramshaw H, White RR, Roddy M, Hladunewich M; Pre-Eclampsia New Emerging Team (PE-NET). A history of preeclampsia identifies women who have underlying cardiovascular risk factors. Am J Obstet Gynecol. 2009 Jan;200(1):58.e1-8.
  • 22. McLeod O, Dunér P, Samnegård A, Tornvall P, Nilsson J, Hamsten A, Bengtsson E. Autoantibodies against basement membrane collagen type IV are associated with myocardial infarction. Int J Cardiol Heart Vasc. 2014 Dec 30;6:42-47.
  • 23. Eble J.A., Golbik R., Mann K., Kuhn K. The alpha 1 beta 1 integrin recognition site of the basement membrane collagen molecule [alpha 1(IV)]2 alpha 2(IV) EMBO J. 1993;12(12):4795–4802.
  • 24. Emsley J., Knight C.G., Farndale R.W., Barnes M.J., Liddington R.C. Structural basis of collagen recognition by integrin alpha2beta1. Cell. 2000;101(1):47–56.
  • 25. Knight C.G., Morton L.F., Peachey A.R., Tuckwell D.S., Farndale R.W., Barnes M.J. The collagen-binding A-domains of integrins alpha(1)beta(1) and alpha(2)beta(1) recognize the same specific amino acid sequence, GFOGER, in native (triple-helical) collagens. J Biol Chem. 2000;275(1):35–40.
  • 26. Xu H., Raynal N., Stathopoulos S., Myllyharju J., Farndale R.W., Leitinger B. Collagen binding specificity of the discoidin domain receptors: binding sites on collagens II and III and molecular determinants for collagen IV recognition by DDR1. Matrix Biol. 2011;30(1):16–26.
  • 27. Gonzalez-Santiago L., Lopez-Ongil S., Rodriguez-Puyol M., Rodriguez-Puyol D. Decreased nitric oxide synthesis in human endothelial cells cultured on type I collagen. Circ Res. 2002;90(5):539–545.
  • 28. Timpl R., Brown J.C. Supramolecular assembly of basement membranes. Bioessays. 1996;18(2):123–132.
  • 29. Ogawa H. [Maternal serum type III procollagen peptide (P-III-P) and 7S domain of type IV collagen (7S) as indicators of placental damage caused by toxemia of pregnancy]. Nihon Sanka Fujinka Gakkai Zasshi. 1994 Oct;46(10):1020-6. Japanese. PMID: 7814931.
  • 30. Furuhashi N, Kimura H, Nagae H, Yajima A, Kimura C, Saito T. Serum collagen IV and laminin levels in preeclampsia. Gynecol Obstet Invest. 1994;37(4):250-3. doi: 10.1159/000292571. PMID: 8050729.
  • 31. Oefner CM, Sharkey A, Gardner L, Critchley H, Oyen M, Moffett A. Collagen type IV at the fetal-maternal interface. Placenta. 2015 Jan;36(1):59-68. doi: 10.1016/j.placenta.2014.10.012. Epub 2014 Nov 1. PMID: 25465704; PMCID: PMC4302218.
Year 2023, Volume: 40 Issue: 3, 509 - 514, 30.09.2023

Abstract

Project Number

The research is supported by the Bulgarian Ministry of Education and Science under the national Program “Young Scientists and Postdoctoral Students-2”.

References

  • 1. ACOG Practice Bulletin No. 202: Gestational Hypertension and Preeclampsia. Obstet Gynecol. 2019 Jan;133(1):1.
  • 2. Uzan J, Carbonnel M, Piconne O, Asmar R, Ayoubi JM. Pre-eclampsia: pathophysiology, diagnosis, and management. Vasc Health Risk Manag. 2011; 7: 467–474.
  • 3. 3. Eiland E, Nzerue C, Faulkner M. Preeclampsia. J Pregnancy. Jul 11 2012; 586578.
  • 4. Wu P, Haththotuwa R, Kwok CS, Babu A, Kotronias RA, Rushton C, Zaman A, Fryer AA, Kadam U, Chew-Graham CA, Mamas MA. Preeclampsia and Future Cardiovascular Health: A Systematic Review and Meta-Analysis. Circ Cardiovasc Qual Outcomes. 2017 Feb;10(2):e003497.
  • 5. Laviades C, Varo N, Fernandez J, et al. Abnormalities of the extracellular degradation of collagen type I in essential hypertension. Circulation 1998: 535-540.
  • 6. Berk BC, Fujiwara K, Lehoux S. ECM remodeling in hypertensive heart disease. J Clin Invest. 2007 Mar;117(3):568-75.
  • 7. Gelse, K. Collagens—Structure, function, and biosynthesis. Adv. Drug Deliv. Rev. 2003, 55, 1531–1546.
  • 8. Morillas P, Quiles J, de Andrade H, et al. Circulating biomarkers of collagen metabolism in arterial hypertension: relevance of target organ damage. J Hypertens. 2013; 31: 1611-1617.
  • 9. Kühn K. Basement membrane (type IV) collagen. Matrix Biol. 1995 Feb;14(6):439-45.
  • 10. Mansell JP, Bailey AJ. Collagen Metabolism. In Encyclopedia of Endocrine Diseases. Elsevier: Amsterdam, The Netherlands, 2004; pp. 520–529.
  • 11. Henriksen, K.; Karsdal, M.A. Type I Collagen. In Biochemistry of Collagens, Laminins and Elastin Structure, Function and Biomarkers, 1st ed.; Karsdal, M.A., Ed.; Academic Press: Cambridge, MA, USA, 2016; Chapter 1; pp. 1–11.
  • 12. Sand, J.M.B.; Genovese, F.; Gudmann, N.S.; Karsdal, M.A. Type IV collagen. In Biochemistry of Collagens, Laminins and Elastin, 2nd ed.; Karsdal, M.A., Ed.; Elsevier: Amsterdam, The Netherlands, 2019; Chapter 4; pp. 37–49.
  • 13. O'Connor BB, Pope BD, Peters MM, Ris-Stalpers C, Parker KK. The role of extracellular matrix in normal and pathological pregnancy: Future applications of microphysiological systems in reproductive medicine. Exp Biol Med (Maywood). 2020 Jul;245(13):1163-1174.
  • 14. Russell DL, Salustri A. Extracellular matrix of the cumulus-oocyte complex. Semin Reprod Med 2006; 24:217–27. 15. Familiari G, Heyn R, Relucenti M, et al. Structural changes of the zona pellucida during fertilization and embryo development. Front Biosci 2008; 13:6730–51.
  • 16. Dong C, Lv Y. Application of Collagen Scaffold in Tissue Engineering: Recent Advances and New Perspectives. Polymers (Basel). 2016 Feb 4;8(2):42.
  • 17. Yamano H, Lambert-Messerlian GM, Silver HM, Kudo R. Maternal serum levels of type I and type III procollagen peptides in preeclamptic pregnancy. Matern Fetal Med. 2001; 10(1): 40-3.
  • 18. Schuppan D. Connective tissue polypeptides in serum as parameters to monitor antifibrotic treatment in hepatic fibrogenesis. J Hepatol. 1991;13 Suppl 3:S17-25.
  • 19. Pereira R.D., De Long N.E., Wang R.C., Yazdi F.T., Holloway A.C., Raha S. Angiogenesis in the placenta: The role of reactive oxygen species signaling. BioMed Res. Int. 2015;2015:814543.
  • 20. Benschop L, Duvekot JJ, Versmissen J, van Broekhoven V, Steegers EAP, Roeters van Lennep JE. Blood Pressure Profile 1 Year After Severe Preeclampsia. Hypertension. 2018 Mar;71(3):491-498.
  • 21. Smith GN, Walker MC, Liu A, Wen SW, Swansburg M, Ramshaw H, White RR, Roddy M, Hladunewich M; Pre-Eclampsia New Emerging Team (PE-NET). A history of preeclampsia identifies women who have underlying cardiovascular risk factors. Am J Obstet Gynecol. 2009 Jan;200(1):58.e1-8.
  • 22. McLeod O, Dunér P, Samnegård A, Tornvall P, Nilsson J, Hamsten A, Bengtsson E. Autoantibodies against basement membrane collagen type IV are associated with myocardial infarction. Int J Cardiol Heart Vasc. 2014 Dec 30;6:42-47.
  • 23. Eble J.A., Golbik R., Mann K., Kuhn K. The alpha 1 beta 1 integrin recognition site of the basement membrane collagen molecule [alpha 1(IV)]2 alpha 2(IV) EMBO J. 1993;12(12):4795–4802.
  • 24. Emsley J., Knight C.G., Farndale R.W., Barnes M.J., Liddington R.C. Structural basis of collagen recognition by integrin alpha2beta1. Cell. 2000;101(1):47–56.
  • 25. Knight C.G., Morton L.F., Peachey A.R., Tuckwell D.S., Farndale R.W., Barnes M.J. The collagen-binding A-domains of integrins alpha(1)beta(1) and alpha(2)beta(1) recognize the same specific amino acid sequence, GFOGER, in native (triple-helical) collagens. J Biol Chem. 2000;275(1):35–40.
  • 26. Xu H., Raynal N., Stathopoulos S., Myllyharju J., Farndale R.W., Leitinger B. Collagen binding specificity of the discoidin domain receptors: binding sites on collagens II and III and molecular determinants for collagen IV recognition by DDR1. Matrix Biol. 2011;30(1):16–26.
  • 27. Gonzalez-Santiago L., Lopez-Ongil S., Rodriguez-Puyol M., Rodriguez-Puyol D. Decreased nitric oxide synthesis in human endothelial cells cultured on type I collagen. Circ Res. 2002;90(5):539–545.
  • 28. Timpl R., Brown J.C. Supramolecular assembly of basement membranes. Bioessays. 1996;18(2):123–132.
  • 29. Ogawa H. [Maternal serum type III procollagen peptide (P-III-P) and 7S domain of type IV collagen (7S) as indicators of placental damage caused by toxemia of pregnancy]. Nihon Sanka Fujinka Gakkai Zasshi. 1994 Oct;46(10):1020-6. Japanese. PMID: 7814931.
  • 30. Furuhashi N, Kimura H, Nagae H, Yajima A, Kimura C, Saito T. Serum collagen IV and laminin levels in preeclampsia. Gynecol Obstet Invest. 1994;37(4):250-3. doi: 10.1159/000292571. PMID: 8050729.
  • 31. Oefner CM, Sharkey A, Gardner L, Critchley H, Oyen M, Moffett A. Collagen type IV at the fetal-maternal interface. Placenta. 2015 Jan;36(1):59-68. doi: 10.1016/j.placenta.2014.10.012. Epub 2014 Nov 1. PMID: 25465704; PMCID: PMC4302218.
There are 30 citations in total.

Details

Primary Language English
Subjects Obstetrics and Gynaecology
Journal Section Research Article
Authors

Asparuh Nikolov 0000-0003-4289-5124

Nikola Popovski 0000-0003-2142-2053

Project Number The research is supported by the Bulgarian Ministry of Education and Science under the national Program “Young Scientists and Postdoctoral Students-2”.
Early Pub Date October 6, 2023
Publication Date September 30, 2023
Submission Date June 25, 2023
Acceptance Date August 14, 2023
Published in Issue Year 2023 Volume: 40 Issue: 3

Cite

APA Nikolov, A., & Popovski, N. (2023). Abnormal levels of serum N-terminal propeptide of collagen type IV (PIVNP) in women one year after preeclampsia. Journal of Experimental and Clinical Medicine, 40(3), 509-514.
AMA Nikolov A, Popovski N. Abnormal levels of serum N-terminal propeptide of collagen type IV (PIVNP) in women one year after preeclampsia. J. Exp. Clin. Med. September 2023;40(3):509-514.
Chicago Nikolov, Asparuh, and Nikola Popovski. “Abnormal Levels of Serum N-Terminal Propeptide of Collagen Type IV (PIVNP) in Women One Year After Preeclampsia”. Journal of Experimental and Clinical Medicine 40, no. 3 (September 2023): 509-14.
EndNote Nikolov A, Popovski N (September 1, 2023) Abnormal levels of serum N-terminal propeptide of collagen type IV (PIVNP) in women one year after preeclampsia. Journal of Experimental and Clinical Medicine 40 3 509–514.
IEEE A. Nikolov and N. Popovski, “Abnormal levels of serum N-terminal propeptide of collagen type IV (PIVNP) in women one year after preeclampsia”, J. Exp. Clin. Med., vol. 40, no. 3, pp. 509–514, 2023.
ISNAD Nikolov, Asparuh - Popovski, Nikola. “Abnormal Levels of Serum N-Terminal Propeptide of Collagen Type IV (PIVNP) in Women One Year After Preeclampsia”. Journal of Experimental and Clinical Medicine 40/3 (September 2023), 509-514.
JAMA Nikolov A, Popovski N. Abnormal levels of serum N-terminal propeptide of collagen type IV (PIVNP) in women one year after preeclampsia. J. Exp. Clin. Med. 2023;40:509–514.
MLA Nikolov, Asparuh and Nikola Popovski. “Abnormal Levels of Serum N-Terminal Propeptide of Collagen Type IV (PIVNP) in Women One Year After Preeclampsia”. Journal of Experimental and Clinical Medicine, vol. 40, no. 3, 2023, pp. 509-14.
Vancouver Nikolov A, Popovski N. Abnormal levels of serum N-terminal propeptide of collagen type IV (PIVNP) in women one year after preeclampsia. J. Exp. Clin. Med. 2023;40(3):509-14.