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Published in: Cardiovascular Toxicology 2/2019

Open Access 01-04-2019

Pregnancy-Associated Plasma Protein A (PAPP-A) Concentration in Population of Healthy Young People: Interactions with Tobacco Smoke and Anti-oxidative Status

Authors: Magdalena Szumska, Aleksandra Damasiewicz-Bodzek, Justyna Czubilińska, Michał Długaszek, Kaja Gawlik, Anna Krywult, Konrad Synowiec, Tomasz Wielkoszyński, Krystyna Tyrpień-Golder

Published in: Cardiovascular Toxicology | Issue 2/2019

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Abstract

Pregnancy-associated plasma protein A (PAPP-A) is a high-molecular zinc-binding metalloproteinase that was first detected in the serum of pregnant women. It can also be detected in men and non-pregnant women. Recently, a growing interest in determining the concentration of PAPP-A as a marker of oxidative stress and atherosclerotic processes has been observed. Among the factors that could potentially influence the PAPP-A formation is the exposure to tobacco smoke. Some components of tobacco smoke have an immediate effect on the body and also direct influence on the cardiovascular system. The aim of this study was to evaluate the relation between PAPP-A concentration and either passive or active exposure to tobacco smoke in the population of medicine students (n = 152). The relation between PAPP-A concentration and chosen markers of inflammatory response and anti-oxidative processes was analyzed. The samples of serum, urine, and saliva were collected and main nicotine metabolites in urine samples were determined using ELISA technique. Comparison of the PAPP-A concentrations in the study group revealed that in the group of active smokers, the concentration of the protein was significantly higher than in the group of passive smokers (p = .04) and the group of not-exposed students (p = .006). PAPP-A concentration showed significant positive correlation with the values of FRAP and main nicotine metabolites. The evident influence of both active and passive tobacco smoke exposure on PAPP-A levels in the studied population of young people who in general are not included in the group of high-risk cardiovascular incidents, shows how important early prevention of anti-health behaviors is.
Literature
1.
go back to reference Lin, T.-M., Halbert, S. P., & Spellacy, W. N. (1974). Measurement of pregnancy-associated plasma proteins during human gestation. Journal of Clinical Investigation, 54, 576–582.CrossRefPubMedPubMedCentral Lin, T.-M., Halbert, S. P., & Spellacy, W. N. (1974). Measurement of pregnancy-associated plasma proteins during human gestation. Journal of Clinical Investigation, 54, 576–582.CrossRefPubMedPubMedCentral
2.
go back to reference van Heesch, P. N., Struijk, P. C., Laudy, J. A., Steegers, E. A., & Wildschut, H. I. (2010). Estimating the effect of gestational age on test performance of combined first-trimester screening for Down syndrome: A preliminary study. Journal of Perinatal Medicine, 38, 305–309.PubMed van Heesch, P. N., Struijk, P. C., Laudy, J. A., Steegers, E. A., & Wildschut, H. I. (2010). Estimating the effect of gestational age on test performance of combined first-trimester screening for Down syndrome: A preliminary study. Journal of Perinatal Medicine, 38, 305–309.PubMed
3.
go back to reference Fowlkes, J., & Freemark, M. (1992). Evidence for a novel insulin-like growth factor (IGF)-dependent protease regulating IGF-binding protein-4 in dermal fibroblasts. Endocrinology, 131, 2071–2076.CrossRefPubMed Fowlkes, J., & Freemark, M. (1992). Evidence for a novel insulin-like growth factor (IGF)-dependent protease regulating IGF-binding protein-4 in dermal fibroblasts. Endocrinology, 131, 2071–2076.CrossRefPubMed
4.
go back to reference Conover, C. A., Kiefer, M. C., & Zapf, J. (1993). Posttranslational regulation of insulin-like growth factor binding protein-4 in normal and transformed human fibroblasts. Insulin-like growth factor dependence and biological studies. Journal of Clinical Investigation, 91, 1129–1137.CrossRefPubMedPubMedCentral Conover, C. A., Kiefer, M. C., & Zapf, J. (1993). Posttranslational regulation of insulin-like growth factor binding protein-4 in normal and transformed human fibroblasts. Insulin-like growth factor dependence and biological studies. Journal of Clinical Investigation, 91, 1129–1137.CrossRefPubMedPubMedCentral
5.
go back to reference Durham, S. K., Kiefer, M. C., Riggs, B. L., & Conover, C. A. (1994). Regulation of insulin-like growth factor binding protein 4 by a specific insulin-like growth factor binding protein 4 proteinase in normal human osteoblast-like cells: Implications in bone cell physiology. Journal of Bone Mineral Research, 9, 111–117.CrossRefPubMed Durham, S. K., Kiefer, M. C., Riggs, B. L., & Conover, C. A. (1994). Regulation of insulin-like growth factor binding protein 4 by a specific insulin-like growth factor binding protein 4 proteinase in normal human osteoblast-like cells: Implications in bone cell physiology. Journal of Bone Mineral Research, 9, 111–117.CrossRefPubMed
6.
go back to reference Lawrence, J. B., Oxvig, C., Overgaard, M. T., Sottrup-Jensen, L., Gleich, G. J., Hays, L. G., et al. (1999). The insulin-like growth factor (IGF)-dependent IGF binding protein-4 protease secreted by human fibroblasts is pregnancy-associated plasma protein-A. Proceedings of the National Academy of Sciences of the United States of America, 96, 3149–3153.CrossRefPubMedPubMedCentral Lawrence, J. B., Oxvig, C., Overgaard, M. T., Sottrup-Jensen, L., Gleich, G. J., Hays, L. G., et al. (1999). The insulin-like growth factor (IGF)-dependent IGF binding protein-4 protease secreted by human fibroblasts is pregnancy-associated plasma protein-A. Proceedings of the National Academy of Sciences of the United States of America, 96, 3149–3153.CrossRefPubMedPubMedCentral
7.
go back to reference Bayes-Genis, A., Conover, C. A., & Schwartz, R. S. (2000). The insulin-like growth factor axis: A review of atherosclerosis and restenosis. Circulation Research, 86, 125–130.CrossRefPubMed Bayes-Genis, A., Conover, C. A., & Schwartz, R. S. (2000). The insulin-like growth factor axis: A review of atherosclerosis and restenosis. Circulation Research, 86, 125–130.CrossRefPubMed
8.
go back to reference Biasucci, L. M., & Rizzello, V. (2006). Pregnancy-associated plasma protein-A: Do specific markers of vascular or plaque activation exist, and do we really need them? Clinical Chemistry, 52, 913–914.CrossRefPubMed Biasucci, L. M., & Rizzello, V. (2006). Pregnancy-associated plasma protein-A: Do specific markers of vascular or plaque activation exist, and do we really need them? Clinical Chemistry, 52, 913–914.CrossRefPubMed
9.
go back to reference Laursen, L. S., Overgaard, M. T., Soe, R., Boldt, H. B., Sottrup-Jensen, L., Giudice, L. C., et al. (2001). Pregnancy-associated plasma protein-A (PAPP-A) cleaves insulin-like growth factor binding protein (IGFBP)-5 independent of IGF: Implications for the mechanism of IGFBP-4 proteolysis by PAPP-A. FEBS Letter, 504, 36–40.CrossRef Laursen, L. S., Overgaard, M. T., Soe, R., Boldt, H. B., Sottrup-Jensen, L., Giudice, L. C., et al. (2001). Pregnancy-associated plasma protein-A (PAPP-A) cleaves insulin-like growth factor binding protein (IGFBP)-5 independent of IGF: Implications for the mechanism of IGFBP-4 proteolysis by PAPP-A. FEBS Letter, 504, 36–40.CrossRef
10.
go back to reference Monget, P., Mazerbourg, S., Delpuech, T., Maurel, M. C., Manière, S., Zapf, J., et al. (2003). Pregnancy-associated plasma protein-A is involved in insulin-like growth factor binding protein-2 (IGFBP-2) proteolytic degradation in bovine and porcine preovulatory follicles: Identification of cleavage site and characterization of IGFBP-2 degradation. Biology of Reproduction, 68, 77–86.CrossRefPubMed Monget, P., Mazerbourg, S., Delpuech, T., Maurel, M. C., Manière, S., Zapf, J., et al. (2003). Pregnancy-associated plasma protein-A is involved in insulin-like growth factor binding protein-2 (IGFBP-2) proteolytic degradation in bovine and porcine preovulatory follicles: Identification of cleavage site and characterization of IGFBP-2 degradation. Biology of Reproduction, 68, 77–86.CrossRefPubMed
11.
go back to reference Boldt, H. B., & Conover, C. A. (2007). Pregnancy-associated plasma protein-A (PAPP-A): A local regulator of IGF bioavailability through cleavage of IGFBPs. Growth Hormone and IGF Research, 17, 10–18.CrossRefPubMed Boldt, H. B., & Conover, C. A. (2007). Pregnancy-associated plasma protein-A (PAPP-A): A local regulator of IGF bioavailability through cleavage of IGFBPs. Growth Hormone and IGF Research, 17, 10–18.CrossRefPubMed
12.
go back to reference Consuegra-Sanchez, L., Fredericks, S., & Kaski, J. C. (2009). Pregnancy-associated plasma protein-A (PAPP-A) and cardiovascular risk. Atherosclerosis, 203, 346–352.CrossRefPubMed Consuegra-Sanchez, L., Fredericks, S., & Kaski, J. C. (2009). Pregnancy-associated plasma protein-A (PAPP-A) and cardiovascular risk. Atherosclerosis, 203, 346–352.CrossRefPubMed
13.
go back to reference Li, Y., Zhou, C., Zhou, X., Song, L., & Hui, R. (2013). PAPP-A in cardiac and non-cardiac conditions. Clinical Chimica Acta, 417, 67–72.CrossRef Li, Y., Zhou, C., Zhou, X., Song, L., & Hui, R. (2013). PAPP-A in cardiac and non-cardiac conditions. Clinical Chimica Acta, 417, 67–72.CrossRef
14.
go back to reference Lund, J., Qin, Q. P., Ilva, T., Petterssson, K., Voipio-Pulkki, L. M., Porela, P., et al. (2003). Circulating pregnancy-associated plasma protein A predicts outcome in patients with acute coronary syndrome but no troponin I elevation. Circulation, 108, 1924–1926.CrossRefPubMed Lund, J., Qin, Q. P., Ilva, T., Petterssson, K., Voipio-Pulkki, L. M., Porela, P., et al. (2003). Circulating pregnancy-associated plasma protein A predicts outcome in patients with acute coronary syndrome but no troponin I elevation. Circulation, 108, 1924–1926.CrossRefPubMed
15.
go back to reference Aso, Y., Okumura, K., Wakabayashi, S., Takebayashi, K., Taki, S., & Inukai, T. (2004). Elevated pregnancy-associated plasma protein-a in sera from type 2 diabetic patients with hypercholesterolemia: Associations with carotid atherosclerosis and toe-brachial index. Journal of Clinical Endocrinology and Metabolism, 89, 5713–5717.CrossRefPubMed Aso, Y., Okumura, K., Wakabayashi, S., Takebayashi, K., Taki, S., & Inukai, T. (2004). Elevated pregnancy-associated plasma protein-a in sera from type 2 diabetic patients with hypercholesterolemia: Associations with carotid atherosclerosis and toe-brachial index. Journal of Clinical Endocrinology and Metabolism, 89, 5713–5717.CrossRefPubMed
16.
go back to reference Stulc, T., Skrha, J., Malbohan, I., Fialová, L., & Ceška, R. (2003) Increased levels of pregnancy-associated plasma protein-A in patients with hypercholesterolemia and diabetes: The effect of lipid lowering. 25th Congress of the European Society of Cardiology, Conference Paper Vol 24, p. 458. Stulc, T., Skrha, J., Malbohan, I., Fialová, L., & Ceška, R. (2003) Increased levels of pregnancy-associated plasma protein-A in patients with hypercholesterolemia and diabetes: The effect of lipid lowering. 25th Congress of the European Society of Cardiology, Conference Paper Vol 24, p. 458.
17.
go back to reference Fialova, L., Kalousova, M., Soukupova, J., Sulkova, S., Merta, M., Jelinkova, E., et al. (2004). Relationship of pregnancy-associated plasma protein-A to renal function and dialysis modalities. Kidney Blood Pressure Research, 27, 88–95.CrossRefPubMed Fialova, L., Kalousova, M., Soukupova, J., Sulkova, S., Merta, M., Jelinkova, E., et al. (2004). Relationship of pregnancy-associated plasma protein-A to renal function and dialysis modalities. Kidney Blood Pressure Research, 27, 88–95.CrossRefPubMed
18.
go back to reference Kalousova, M., Horejsi, M., Fialova, L., Soukupova, J., Sulkova, S., Malbohan, I., et al. (2004). Increased levels of pregnancy-associated plasma protein A are associated with mortality in hemodialysis patients: Preliminary results. Blood Purification, 22, 298–300.CrossRefPubMed Kalousova, M., Horejsi, M., Fialova, L., Soukupova, J., Sulkova, S., Malbohan, I., et al. (2004). Increased levels of pregnancy-associated plasma protein A are associated with mortality in hemodialysis patients: Preliminary results. Blood Purification, 22, 298–300.CrossRefPubMed
19.
go back to reference Coskun, A., Bicik, Z., Duran, S., Alcelik, A., Soypacaci, Z., Yavuz, O., et al. (2007). Pregnancy-associated plasma protein A in dialysis patients. Clinical Chemistry Laboratory Medicine, 45, 63–66.PubMed Coskun, A., Bicik, Z., Duran, S., Alcelik, A., Soypacaci, Z., Yavuz, O., et al. (2007). Pregnancy-associated plasma protein A in dialysis patients. Clinical Chemistry Laboratory Medicine, 45, 63–66.PubMed
20.
go back to reference Coskun, A., Duran, S., Apaydin, S., Bulut, I., & Sariyar, M. (2007). Pregnancy-associated plasma protein-A: Evaluation of a new biomarker in renal transplant patients. Transplant Proceedings, 39, 3072–3076.CrossRef Coskun, A., Duran, S., Apaydin, S., Bulut, I., & Sariyar, M. (2007). Pregnancy-associated plasma protein-A: Evaluation of a new biomarker in renal transplant patients. Transplant Proceedings, 39, 3072–3076.CrossRef
21.
go back to reference Etter, C., Straub, Y., Hersberger, M., Raz, H. R., Kistler, T., Kiss, D., et al. (2010). Pregnancy-associated plasma protein-A is an independent short-time predictor of mortality in patients on maintenance haemodialysis. European Heart Journal, 31, 354–359.CrossRefPubMed Etter, C., Straub, Y., Hersberger, M., Raz, H. R., Kistler, T., Kiss, D., et al. (2010). Pregnancy-associated plasma protein-A is an independent short-time predictor of mortality in patients on maintenance haemodialysis. European Heart Journal, 31, 354–359.CrossRefPubMed
22.
go back to reference Fialova, L., Pileckova, N., Bauer, J., Soukupová, J., Kalousová, M., Malbohan, I., et al. (2006). Pregnancy-associated plasma protein-A in patients with cerebrovascular diseases: A pilot study. Prague Medical Report, 107, 37–45.PubMed Fialova, L., Pileckova, N., Bauer, J., Soukupová, J., Kalousová, M., Malbohan, I., et al. (2006). Pregnancy-associated plasma protein-A in patients with cerebrovascular diseases: A pilot study. Prague Medical Report, 107, 37–45.PubMed
23.
go back to reference Conover, C. A., & Bale, L. K. (2007). Loss of pregnancy-associated plasma protein A extends lifespan in mice. Aging Cell, 6, 727–729.CrossRefPubMed Conover, C. A., & Bale, L. K. (2007). Loss of pregnancy-associated plasma protein A extends lifespan in mice. Aging Cell, 6, 727–729.CrossRefPubMed
24.
go back to reference Kalli, K. R., Chen, B. K., Bale, L. K., Germand, E., Overgaard, M. T., Oxvig, C., et al. (2004). Pregnancy-associated plasma protein-A (PAPP-A) expression and insulin-like growth factor binding protein-4 protease activity in normal and malignant ovarian surface epithelial cells. International Journal of Cancer, 110, 633–640.CrossRefPubMed Kalli, K. R., Chen, B. K., Bale, L. K., Germand, E., Overgaard, M. T., Oxvig, C., et al. (2004). Pregnancy-associated plasma protein-A (PAPP-A) expression and insulin-like growth factor binding protein-4 protease activity in normal and malignant ovarian surface epithelial cells. International Journal of Cancer, 110, 633–640.CrossRefPubMed
25.
go back to reference Ryan, A. J., Napoletano, S., Fitzpatrick, P. A., Currid, C. A., O’Sullivan, N. C., & Harmey, J. H. (2009). Expression of a protease-resistant insulin-like growth factor-binding protein-4 inhibits tumour growth in a murine model of breast cancer. British Journal of Cancer, 101, 278–286.CrossRefPubMedPubMedCentral Ryan, A. J., Napoletano, S., Fitzpatrick, P. A., Currid, C. A., O’Sullivan, N. C., & Harmey, J. H. (2009). Expression of a protease-resistant insulin-like growth factor-binding protein-4 inhibits tumour growth in a murine model of breast cancer. British Journal of Cancer, 101, 278–286.CrossRefPubMedPubMedCentral
26.
go back to reference Bulut, I., Coskun, A., Ciftci, A., Cetinkaya, E., Altiay, G., Caglar, T., et al. (2009). Relationship between pregnancy-associated plasma protein-A and lung cancer. American Journal of Medical Sciences, 337, 241–244.CrossRef Bulut, I., Coskun, A., Ciftci, A., Cetinkaya, E., Altiay, G., Caglar, T., et al. (2009). Relationship between pregnancy-associated plasma protein-A and lung cancer. American Journal of Medical Sciences, 337, 241–244.CrossRef
27.
go back to reference Chen, B. K., Leiferman, K. M., Pittelkow, M. R., Overgaard, M. T., Oxvig, C., & Conover, C. A. (2003). Localization and regulation of pregnancy-associated plasma protein A expression in healing human skin. Journal of Clinical Endocrinology and Metabolism, 88, 4465–4471.CrossRefPubMed Chen, B. K., Leiferman, K. M., Pittelkow, M. R., Overgaard, M. T., Oxvig, C., & Conover, C. A. (2003). Localization and regulation of pregnancy-associated plasma protein A expression in healing human skin. Journal of Clinical Endocrinology and Metabolism, 88, 4465–4471.CrossRefPubMed
28.
go back to reference Resch, Z. T., Chen, B. K., Bale, L. K., Oxvig, C., Overgaard, M. T., & Conover, C. A. (2004). Pregnancy-associated plasma protein a gene expression as a target of inflammatory cytokines. Endocrinology, 145, 1124–1129.CrossRefPubMed Resch, Z. T., Chen, B. K., Bale, L. K., Oxvig, C., Overgaard, M. T., & Conover, C. A. (2004). Pregnancy-associated plasma protein a gene expression as a target of inflammatory cytokines. Endocrinology, 145, 1124–1129.CrossRefPubMed
29.
go back to reference Finkel, T., & Holbrook, N. J. (2000). Oxidants, oxidative stress and the biology of ageing. Nature, 408, 239–247.CrossRefPubMed Finkel, T., & Holbrook, N. J. (2000). Oxidants, oxidative stress and the biology of ageing. Nature, 408, 239–247.CrossRefPubMed
30.
go back to reference Resch, Z. T., Oxvig, C., Bale, L. K., & Conover, C. A. (2006). Stress-activated signaling pathways mediate the stimulation of pregnancy-associated plasma protein-A expression in cultured human fibroblasts. Endocrinology, 147, 885–890.CrossRefPubMed Resch, Z. T., Oxvig, C., Bale, L. K., & Conover, C. A. (2006). Stress-activated signaling pathways mediate the stimulation of pregnancy-associated plasma protein-A expression in cultured human fibroblasts. Endocrinology, 147, 885–890.CrossRefPubMed
31.
go back to reference Alshehri, A. M., Azoz, A. M., Shaheen, H. A., Farrag, Y. A., Khalifa, M. A. A., & Youssef, A. (2013). Acute effects of cigarette smoking on the cardiac diastolic functions. Journal of Saudi Heart Association, 25, 173–179.CrossRef Alshehri, A. M., Azoz, A. M., Shaheen, H. A., Farrag, Y. A., Khalifa, M. A. A., & Youssef, A. (2013). Acute effects of cigarette smoking on the cardiac diastolic functions. Journal of Saudi Heart Association, 25, 173–179.CrossRef
32.
go back to reference Samet, J. M. (2013). Tobacco smoking: The leading cause of preventable disease worldwide. Thoracic Surgery Clinics, 23, 103–112.CrossRefPubMed Samet, J. M. (2013). Tobacco smoking: The leading cause of preventable disease worldwide. Thoracic Surgery Clinics, 23, 103–112.CrossRefPubMed
33.
go back to reference Chelchowska, M., Maciejewski, T., Gajewska, J., Ambroszkiewicz, J., Laskowska-Klita, T., & Leibschang, J. (2012). The pregnancy-associated plasma protein A and insulin-like growth factor system in response to cigarette smoking. Journal of Maternal Fetal Neonatal Medicine, 25, 2377–2380.CrossRefPubMed Chelchowska, M., Maciejewski, T., Gajewska, J., Ambroszkiewicz, J., Laskowska-Klita, T., & Leibschang, J. (2012). The pregnancy-associated plasma protein A and insulin-like growth factor system in response to cigarette smoking. Journal of Maternal Fetal Neonatal Medicine, 25, 2377–2380.CrossRefPubMed
34.
go back to reference Heeschen, C., Dimmeler, S., Hamm, C. W., Fichtlscherer, S., Simoons, M. L., & Zeiher, A. M. (2005). Pregnancy-associated plasma protein-A levels in patients with acute coronary syndromes: Comparison with markers of systemic inflammation, platelet activation, and myocardial necrosis. Journal of the American College of Cardiology, 45, 229–237.CrossRefPubMed Heeschen, C., Dimmeler, S., Hamm, C. W., Fichtlscherer, S., Simoons, M. L., & Zeiher, A. M. (2005). Pregnancy-associated plasma protein-A levels in patients with acute coronary syndromes: Comparison with markers of systemic inflammation, platelet activation, and myocardial necrosis. Journal of the American College of Cardiology, 45, 229–237.CrossRefPubMed
35.
go back to reference Coskun, A., Serteser, M., Duran, S., Inal, T. C., Erdogan, B. E., Ozpinar, A., et al. (2013). Reference interval of pregnancy-associated plasma protein-A in healthy men and non-pregnant women. Journal of Cardiology, 61, 128–131.CrossRefPubMed Coskun, A., Serteser, M., Duran, S., Inal, T. C., Erdogan, B. E., Ozpinar, A., et al. (2013). Reference interval of pregnancy-associated plasma protein-A in healthy men and non-pregnant women. Journal of Cardiology, 61, 128–131.CrossRefPubMed
36.
go back to reference Joaquin, C., Granada, M. L., Pastor, C., Castell, C., Puig, R., Alonso, N., et al. (2013). Pregnancy-associated plasma protein-A is related to gender and to adipocytokine levels: Results of the Health Survey of Catalonia. Clinical Endocrinology (Oxford), 78, 718–723.CrossRef Joaquin, C., Granada, M. L., Pastor, C., Castell, C., Puig, R., Alonso, N., et al. (2013). Pregnancy-associated plasma protein-A is related to gender and to adipocytokine levels: Results of the Health Survey of Catalonia. Clinical Endocrinology (Oxford), 78, 718–723.CrossRef
37.
go back to reference Larsman, P., Eklof, M., & Torner, M. (2012). Adolescents’ risk perceptions in relation to risk behavior with long-term health consequences; antecedents and outcomes: A literature review. Safety Science, 50, 1740.CrossRef Larsman, P., Eklof, M., & Torner, M. (2012). Adolescents’ risk perceptions in relation to risk behavior with long-term health consequences; antecedents and outcomes: A literature review. Safety Science, 50, 1740.CrossRef
38.
go back to reference Levit, R. D., Reynolds, H. R., & Hochman, J. S. (2011). Cardiovascular disease in young women: A population at risk. Cardiology Review, 19, 60–65.CrossRef Levit, R. D., Reynolds, H. R., & Hochman, J. S. (2011). Cardiovascular disease in young women: A population at risk. Cardiology Review, 19, 60–65.CrossRef
39.
go back to reference Mansikkaniemi, K., Juonala, M., Taimela, S., Hirvensalo, M., Telama, R., Huupponen, R., et al. (2012). Cross-sectional associations between physical activity and selected coronary heart disease risk factors in young adults. The Cardiovascular Risk in Young Finns Study. Annals of Medicine, 44, 733–744.CrossRefPubMed Mansikkaniemi, K., Juonala, M., Taimela, S., Hirvensalo, M., Telama, R., Huupponen, R., et al. (2012). Cross-sectional associations between physical activity and selected coronary heart disease risk factors in young adults. The Cardiovascular Risk in Young Finns Study. Annals of Medicine, 44, 733–744.CrossRefPubMed
40.
go back to reference Wielkoszynski, T., Tyrpien, K., & Szumska, M. (2009). The enzyme-linked immunosorbent assay (ELISA) method for nicotine metabolites determination in biological fluids. Journal of Pharmaceutical Biomedical Analysis, 49, 1256–1260.CrossRefPubMed Wielkoszynski, T., Tyrpien, K., & Szumska, M. (2009). The enzyme-linked immunosorbent assay (ELISA) method for nicotine metabolites determination in biological fluids. Journal of Pharmaceutical Biomedical Analysis, 49, 1256–1260.CrossRefPubMed
41.
go back to reference Benzie, I. F., & Strain, J. J. (1999). Ferric reducing/antioxidant power assay: Direct measure of total antioxidant activity of biological fluids and modified version for simultaneous measurement of total antioxidant power and ascorbic acid concentration. Methods Enzymology, 299, 15–27.CrossRef Benzie, I. F., & Strain, J. J. (1999). Ferric reducing/antioxidant power assay: Direct measure of total antioxidant activity of biological fluids and modified version for simultaneous measurement of total antioxidant power and ascorbic acid concentration. Methods Enzymology, 299, 15–27.CrossRef
42.
go back to reference Benzie, I. F., & Strain, J. J. (1996). The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: The FRAP assay. Analytical Biochemistry, 239, 70–76.CrossRefPubMed Benzie, I. F., & Strain, J. J. (1996). The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: The FRAP assay. Analytical Biochemistry, 239, 70–76.CrossRefPubMed
43.
go back to reference Basu, S., Stuckler, D., Bitton, A., & Glantz, S. A. (2011). Projected effects of tobacco smoking on worldwide tuberculosis control: Mathematical modelling analysis. BMJ, 343, d5506.CrossRefPubMedPubMedCentral Basu, S., Stuckler, D., Bitton, A., & Glantz, S. A. (2011). Projected effects of tobacco smoking on worldwide tuberculosis control: Mathematical modelling analysis. BMJ, 343, d5506.CrossRefPubMedPubMedCentral
44.
go back to reference Swan, G. E., & Lessov-Schlaggar, C. N. (2007). The effects of tobacco smoke and nicotine on cognition and the brain. Neuropsychology Review, 17, 259–273.CrossRefPubMed Swan, G. E., & Lessov-Schlaggar, C. N. (2007). The effects of tobacco smoke and nicotine on cognition and the brain. Neuropsychology Review, 17, 259–273.CrossRefPubMed
45.
go back to reference Goncalves, R. B., Coletta, R. D., Silverio, K. G., Benevides, L., Casati, M. Z., Sliva, J. S., et al. (2011). Impact of smoking on inflammation: Overview of molecular mechanisms. Inflammation Research, 60, 409–424.CrossRefPubMed Goncalves, R. B., Coletta, R. D., Silverio, K. G., Benevides, L., Casati, M. Z., Sliva, J. S., et al. (2011). Impact of smoking on inflammation: Overview of molecular mechanisms. Inflammation Research, 60, 409–424.CrossRefPubMed
47.
go back to reference Jha, P., Ramasundarahettige, C., Landsman, V., Rostron, B., Thun, M., Anderson, R. N., et al. (2013). 21st-century hazards of smoking and benefits of cessation in the United States. New England Journal of Medicine, 368, 341–350.CrossRefPubMed Jha, P., Ramasundarahettige, C., Landsman, V., Rostron, B., Thun, M., Anderson, R. N., et al. (2013). 21st-century hazards of smoking and benefits of cessation in the United States. New England Journal of Medicine, 368, 341–350.CrossRefPubMed
48.
go back to reference Centers of Disease Control and Prevention (CDC). (2008). Smoking-attributable mortality, years of potential life lost, and productivity losses—United States, 2000–2004. MMWR, 54, 625 Centers of Disease Control and Prevention (CDC). (2008). Smoking-attributable mortality, years of potential life lost, and productivity losses—United States, 2000–2004. MMWR, 54, 625
49.
go back to reference Kushi, L. H., Byers, T., Doyle, C., Bandera, E. V., McCullough, M., McTiernan, A., et al. (2006). American Cancer Society Guidelines on Nutrition and Physical Activity for cancer prevention: Reducing the risk of cancer with healthy food choices and physical activity. CA: Cancer Journal of Clinicians, 56, 254–281. Kushi, L. H., Byers, T., Doyle, C., Bandera, E. V., McCullough, M., McTiernan, A., et al. (2006). American Cancer Society Guidelines on Nutrition and Physical Activity for cancer prevention: Reducing the risk of cancer with healthy food choices and physical activity. CA: Cancer Journal of Clinicians, 56, 254–281.
50.
go back to reference Ezzati, M., Henley, S. J., Lopez, A. D., & Thun, M. J. (2005). Role of smoking in global and regional cancer epidemiology: Current patterns and data needs. International Journal of Cancer, 116, 963–971.CrossRefPubMed Ezzati, M., Henley, S. J., Lopez, A. D., & Thun, M. J. (2005). Role of smoking in global and regional cancer epidemiology: Current patterns and data needs. International Journal of Cancer, 116, 963–971.CrossRefPubMed
51.
go back to reference Rigotti, N. A., & Clair, C. (2013). Managing tobacco use: The neglected cardiovascular disease risk factor. European Heart Journal, 34, 3259–3267.CrossRefPubMed Rigotti, N. A., & Clair, C. (2013). Managing tobacco use: The neglected cardiovascular disease risk factor. European Heart Journal, 34, 3259–3267.CrossRefPubMed
52.
go back to reference Gajewska, J., Chelchowska, M., Ceran, A., Ambroszkiewicz, J., & Laskowska-Klita, T. (2010). The influence of tobacco smoking on concentration of the pregnancy-associated plasma protein A (PAPP-A) in pregnant women. Przegland Lekarski, 67, 1061–1065. [in Polish]. Gajewska, J., Chelchowska, M., Ceran, A., Ambroszkiewicz, J., & Laskowska-Klita, T. (2010). The influence of tobacco smoking on concentration of the pregnancy-associated plasma protein A (PAPP-A) in pregnant women. Przegland Lekarski, 67, 1061–1065. [in Polish].
53.
go back to reference Villaverde, A., Parra, V., & Estevez, M. (2014). Oxidative and nitrosative stress induced in myofibrillar proteins by a hydroxyl-radical-generating system: Impact of nitrite and ascorbate. Journal of Agricultural and Food Chemistry, 62, 2158–2164.CrossRefPubMed Villaverde, A., Parra, V., & Estevez, M. (2014). Oxidative and nitrosative stress induced in myofibrillar proteins by a hydroxyl-radical-generating system: Impact of nitrite and ascorbate. Journal of Agricultural and Food Chemistry, 62, 2158–2164.CrossRefPubMed
54.
go back to reference Benowitz, N. L. (1999). Biomarkers of environmental tobacco smoke exposure. Environmental Health Perspectives, 107, 349–355.PubMedPubMedCentral Benowitz, N. L. (1999). Biomarkers of environmental tobacco smoke exposure. Environmental Health Perspectives, 107, 349–355.PubMedPubMedCentral
55.
go back to reference Szumska, M., Tyrpień, K., Wielkoszynski, T., et al. (2013). Evaluation of the influence of exposure to tobacco smoke on the concentration of the pregnancy-associated plasma protein A in the population of healthy men and non-pregnant women. Przegland Lekarski, 70, 813–817. [in Polish]. Szumska, M., Tyrpień, K., Wielkoszynski, T., et al. (2013). Evaluation of the influence of exposure to tobacco smoke on the concentration of the pregnancy-associated plasma protein A in the population of healthy men and non-pregnant women. Przegland Lekarski, 70, 813–817. [in Polish].
56.
go back to reference Rom, O., Avezov, K., Aizenbud, D., et al. (2013). Cigarette smoking and inflammation revisited. Respiratory Physiology and Neurobiology, 187, 5–10.CrossRefPubMed Rom, O., Avezov, K., Aizenbud, D., et al. (2013). Cigarette smoking and inflammation revisited. Respiratory Physiology and Neurobiology, 187, 5–10.CrossRefPubMed
57.
go back to reference Yanbaeva, D. G., Dentener, M. A., Creutzberg, E. C., et al. (2007). Systemic effects of smoking. Chest, 131, 1557–1566.CrossRefPubMed Yanbaeva, D. G., Dentener, M. A., Creutzberg, E. C., et al. (2007). Systemic effects of smoking. Chest, 131, 1557–1566.CrossRefPubMed
58.
go back to reference Arnson, Y., Shoenfeld, Y., & Amital, H. (2010). Effects of tobacco smoke on immunity, inflammation and autoimmunity. Journal of Autoimmunity, 34, J258–J265.CrossRefPubMed Arnson, Y., Shoenfeld, Y., & Amital, H. (2010). Effects of tobacco smoke on immunity, inflammation and autoimmunity. Journal of Autoimmunity, 34, J258–J265.CrossRefPubMed
59.
go back to reference Conover, C. A., Bale, L. K., Harrington, S. C., et al. (2006). Cytokine stimulation of pregnancy-associated plasma protein A expression in human coronary artery smooth muscle cells: Inhibition by resveratrol. American Journal of Physiology Cell Physiology, 290, C183–C188.CrossRefPubMed Conover, C. A., Bale, L. K., Harrington, S. C., et al. (2006). Cytokine stimulation of pregnancy-associated plasma protein A expression in human coronary artery smooth muscle cells: Inhibition by resveratrol. American Journal of Physiology Cell Physiology, 290, C183–C188.CrossRefPubMed
60.
go back to reference Harrington, S. C., Simari, R. D., & Conover, C. A. (2007). Genetic deletion of pregnancy-associated plasma protein-A is associated with resistance to atherosclerotic lesion development in apolipoprotein E-deficient mice challenged with a high-fat diet. Circulation Research, 100, 1696–1702.CrossRefPubMed Harrington, S. C., Simari, R. D., & Conover, C. A. (2007). Genetic deletion of pregnancy-associated plasma protein-A is associated with resistance to atherosclerotic lesion development in apolipoprotein E-deficient mice challenged with a high-fat diet. Circulation Research, 100, 1696–1702.CrossRefPubMed
61.
go back to reference Conover, C. A., Mason, M. A., Bale, L. K., et al. (2010). Transgenic overexpression of pregnancy-associated plasma protein-A in murine arterial smooth muscle accelerates atherosclerotic lesion development. American Journal of Physiology Heart and Circulatory Physiology, 299, H284–H291.CrossRefPubMedPubMedCentral Conover, C. A., Mason, M. A., Bale, L. K., et al. (2010). Transgenic overexpression of pregnancy-associated plasma protein-A in murine arterial smooth muscle accelerates atherosclerotic lesion development. American Journal of Physiology Heart and Circulatory Physiology, 299, H284–H291.CrossRefPubMedPubMedCentral
62.
go back to reference Resch, Z. T., Simari, R. D., & Conover, C. A. (2006). Targeted disruption of the pregnancy-associated plasma protein-A gene is associated with diminished smooth muscle cell response to insulin-like growth factor-I and resistance to neointimal hyperplasia after vascular injury. Endocrinology, 147, 5634–5640.CrossRefPubMed Resch, Z. T., Simari, R. D., & Conover, C. A. (2006). Targeted disruption of the pregnancy-associated plasma protein-A gene is associated with diminished smooth muscle cell response to insulin-like growth factor-I and resistance to neointimal hyperplasia after vascular injury. Endocrinology, 147, 5634–5640.CrossRefPubMed
63.
go back to reference Delafontaine, P., Song, Y. H., & Li, Y. (2004). Expression, regulation, and function of IGF-1, IGF-1R, and IGF-1 binding proteins in blood vessels. Arteriosclerosis Thrombosis and Vascular Biology, 24, 435–444.CrossRef Delafontaine, P., Song, Y. H., & Li, Y. (2004). Expression, regulation, and function of IGF-1, IGF-1R, and IGF-1 binding proteins in blood vessels. Arteriosclerosis Thrombosis and Vascular Biology, 24, 435–444.CrossRef
64.
go back to reference Conover, C. A., Harrington, S. C., Bale, L. K., et al. (2007). Surface association of pregnancy-associated plasma protein-A accounts for its colocalization with activated macrophages. American Journal of Physiology Heart Circulatory Physiology, 292, H994–H1000.CrossRefPubMed Conover, C. A., Harrington, S. C., Bale, L. K., et al. (2007). Surface association of pregnancy-associated plasma protein-A accounts for its colocalization with activated macrophages. American Journal of Physiology Heart Circulatory Physiology, 292, H994–H1000.CrossRefPubMed
65.
go back to reference Bayes-Genis, A., Conover, C. A., Overgaard, M. T., et al. (2001). Pregnancy-associated plasma protein A as a marker of acute coronary syndromes. New England Journal of Medicine, 345, 1022–1029.CrossRefPubMed Bayes-Genis, A., Conover, C. A., Overgaard, M. T., et al. (2001). Pregnancy-associated plasma protein A as a marker of acute coronary syndromes. New England Journal of Medicine, 345, 1022–1029.CrossRefPubMed
66.
go back to reference Sangiorgi, G., Mauriello, A., Bonanno, E., et al. (2006). Pregnancy-associated plasma protein-a is markedly expressed by monocyte-macrophage cells in vulnerable and ruptured carotid atherosclerotic plaques: A link between inflammation and cerebrovascular events. Journal of the American College of Cardiology, 47, 2201–2211.CrossRefPubMed Sangiorgi, G., Mauriello, A., Bonanno, E., et al. (2006). Pregnancy-associated plasma protein-a is markedly expressed by monocyte-macrophage cells in vulnerable and ruptured carotid atherosclerotic plaques: A link between inflammation and cerebrovascular events. Journal of the American College of Cardiology, 47, 2201–2211.CrossRefPubMed
67.
go back to reference Bonaca, M. P., Scirica, B. M., Sabatine, M. S., et al. (2012). Prospective evaluation of pregnancy-associated plasma protein-a and outcomes in patients with acute coronary syndromes. Journal of the American College of Cardiology, 60, 332–338.CrossRefPubMed Bonaca, M. P., Scirica, B. M., Sabatine, M. S., et al. (2012). Prospective evaluation of pregnancy-associated plasma protein-a and outcomes in patients with acute coronary syndromes. Journal of the American College of Cardiology, 60, 332–338.CrossRefPubMed
68.
go back to reference Tonstad, S., & Cowan, J. L. (2009). C-reactive protein as a predictor of disease in smokers and former smokers: A review. International Journal of Clinical Practice, 63, 1634–1641.CrossRefPubMedPubMedCentral Tonstad, S., & Cowan, J. L. (2009). C-reactive protein as a predictor of disease in smokers and former smokers: A review. International Journal of Clinical Practice, 63, 1634–1641.CrossRefPubMedPubMedCentral
69.
go back to reference Wannamethee, S. G., Lowe, G. D., Shaper, A. G., et al. (2005). Associations between cigarette smoking, pipe/cigar smoking, and smoking cessation, and haemostatic and inflammatory markers for cardiovascular disease. European Heart Journal, 26, 1765–1773.CrossRefPubMed Wannamethee, S. G., Lowe, G. D., Shaper, A. G., et al. (2005). Associations between cigarette smoking, pipe/cigar smoking, and smoking cessation, and haemostatic and inflammatory markers for cardiovascular disease. European Heart Journal, 26, 1765–1773.CrossRefPubMed
70.
go back to reference Ohsawa, M., Okayama, A., Nakamura, M., et al. (2005). CRP levels are elevated in smokers but unrelated to the number of cigarettes and are decreased by long-term smoking cessation in male smokers. Preventive Medicine, 41, 651–656.CrossRefPubMed Ohsawa, M., Okayama, A., Nakamura, M., et al. (2005). CRP levels are elevated in smokers but unrelated to the number of cigarettes and are decreased by long-term smoking cessation in male smokers. Preventive Medicine, 41, 651–656.CrossRefPubMed
71.
go back to reference O’Loughlin, J., Lambert, M., Karp, I., et al. (2008). Association between cigarette smoking and C-reactive protein in a representative, population-based sample of adolescents. Nicotine & Tobacco Research, 10, 525–532.CrossRef O’Loughlin, J., Lambert, M., Karp, I., et al. (2008). Association between cigarette smoking and C-reactive protein in a representative, population-based sample of adolescents. Nicotine & Tobacco Research, 10, 525–532.CrossRef
72.
go back to reference Lowe, G. D., Sweetnam, P. M., Yarnell, J. W., et al. (2004). C-reactive protein, fibrin D-dimer, and risk of ischemic heart disease: The Caerphilly and Speedwell studies. Arteriosclerosis Thrombosis and Vascular Biology, 24, 1957–1962.CrossRef Lowe, G. D., Sweetnam, P. M., Yarnell, J. W., et al. (2004). C-reactive protein, fibrin D-dimer, and risk of ischemic heart disease: The Caerphilly and Speedwell studies. Arteriosclerosis Thrombosis and Vascular Biology, 24, 1957–1962.CrossRef
73.
go back to reference Helmersson, J., Larsson, A., Vessby, B., et al. (2005). Active smoking and a history of smoking are associated with enhanced prostaglandin F(2alpha), interleukin-6 and F2-isoprostane formation in elderly men. Atherosclerosis, 181, 201–207.CrossRefPubMed Helmersson, J., Larsson, A., Vessby, B., et al. (2005). Active smoking and a history of smoking are associated with enhanced prostaglandin F(2alpha), interleukin-6 and F2-isoprostane formation in elderly men. Atherosclerosis, 181, 201–207.CrossRefPubMed
74.
go back to reference Frohlich, M., Sund, M., Lowel, H., et al. (2003). Independent association of various smoking characteristics with markers of systemic inflammation in men. Results from a representative sample of the general population (MONICA Augsburg Survey 1994/95). European Heart Journal, 24, 1365–1372.CrossRefPubMed Frohlich, M., Sund, M., Lowel, H., et al. (2003). Independent association of various smoking characteristics with markers of systemic inflammation in men. Results from a representative sample of the general population (MONICA Augsburg Survey 1994/95). European Heart Journal, 24, 1365–1372.CrossRefPubMed
75.
go back to reference Wilkinson, J. D., Lee, D. J., & Arheart, K. L. (2007). Secondhand smoke exposure and C-reactive protein levels in youth. Nicotine & Tobacco Research, 9, 305–307.CrossRef Wilkinson, J. D., Lee, D. J., & Arheart, K. L. (2007). Secondhand smoke exposure and C-reactive protein levels in youth. Nicotine & Tobacco Research, 9, 305–307.CrossRef
76.
go back to reference Panagiotakos, D. B., Pitsavos, C., Chrysohoou, C., et al. (2004). Effect of exposure to secondhand smoke on markers of inflammation: The ATTICA study. American Journal of Medicine, 116, 145–150.CrossRefPubMed Panagiotakos, D. B., Pitsavos, C., Chrysohoou, C., et al. (2004). Effect of exposure to secondhand smoke on markers of inflammation: The ATTICA study. American Journal of Medicine, 116, 145–150.CrossRefPubMed
77.
go back to reference Venn, A., & Britton, J. (2007). Exposure to secondhand smoke and biomarkers of cardiovascular disease risk in never-smoking adults. Circulation, 115, 990–995.CrossRefPubMed Venn, A., & Britton, J. (2007). Exposure to secondhand smoke and biomarkers of cardiovascular disease risk in never-smoking adults. Circulation, 115, 990–995.CrossRefPubMed
78.
go back to reference Goraca, A., & Skibska, B. (2005). Plasma antioxidant status in healthy smoking and non-smoking men. Bratislavske Lekarske Listy, 106, 301–306.PubMed Goraca, A., & Skibska, B. (2005). Plasma antioxidant status in healthy smoking and non-smoking men. Bratislavske Lekarske Listy, 106, 301–306.PubMed
79.
go back to reference Miri, R., Saadati, H., Ardi, P., et al. (2012). Alterations in oxidative stress biomarkers associated with mild hyperlipidemia and smoking. Food and Chemical Toxicology, 50, 920–926.CrossRefPubMed Miri, R., Saadati, H., Ardi, P., et al. (2012). Alterations in oxidative stress biomarkers associated with mild hyperlipidemia and smoking. Food and Chemical Toxicology, 50, 920–926.CrossRefPubMed
80.
go back to reference Ranjbar, A., Rajabian, H., Jand, Y., et al. (2004). The comparison of oxidative stress between smokers and nonsmokers. Arak Medical University Journal, 7, 7–11. Ranjbar, A., Rajabian, H., Jand, Y., et al. (2004). The comparison of oxidative stress between smokers and nonsmokers. Arak Medical University Journal, 7, 7–11.
Metadata
Title
Pregnancy-Associated Plasma Protein A (PAPP-A) Concentration in Population of Healthy Young People: Interactions with Tobacco Smoke and Anti-oxidative Status
Authors
Magdalena Szumska
Aleksandra Damasiewicz-Bodzek
Justyna Czubilińska
Michał Długaszek
Kaja Gawlik
Anna Krywult
Konrad Synowiec
Tomasz Wielkoszyński
Krystyna Tyrpień-Golder
Publication date
01-04-2019
Publisher
Springer US
Published in
Cardiovascular Toxicology / Issue 2/2019
Print ISSN: 1530-7905
Electronic ISSN: 1559-0259
DOI
https://doi.org/10.1007/s12012-018-9479-6

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