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Research Articles

Molecular simulation unravels the amyloidogenic misfolding of nascent ApoA1 protein, driven by deleterious point mutations occurring in between 170–178 hotspot region

, , , , &
Pages 13278-13290 | Received 29 May 2021, Accepted 22 Sep 2021, Published online: 06 Oct 2021

References

  • Adams, D., Ando, Y., Beirão, J. M., Coelho, T., Gertz, M. A., Gillmore, J. D., Hawkins, P. N., Lousada, I., Suhr, O. B., & Merlini, G. (2020). Expert consensus recommendations to improve diagnosis of ATTR amyloidosis with polyneuropathy. Journal of Neurology, 268(6):2109–2122. https://doi.org/10.1007/s00415-019-09688-0
  • Alexandrov, V., Lehnert, U., Echols, N., Milburn, D., Engelman, D., & Gerstein, M. (2005). Normal modes for predicting protein motions: A comprehensive database assessment and associated Web tool. Protein Science: A Publication of the Protein Society, 14(3), 633–643. https://doi.org/10.1110/ps.04882105
  • Arciello, A., Piccoli, R., & Monti, D. M. (2016). Apolipoprotein A-I: The dual face of a protein. FEBS Letters, 590(23), 4171–4179. https://doi.org/10.1002/1873-3468.12468
  • Arinami, T., Hirano, T., Kobayashi, K., Yamanouchi, Y., & Hamaguchi, H. (1990). Assignment of the apolipoprotein A-I gene to 11q23 based on RFLP in a case with a partial deletion of chromosome 11, del(11)(q23.3––qter). Human Genetics, 85(1), 39–40. https://doi.org/10.1007/BF00276323
  • Bauer, J. A., & Bauerová-Hlinková, V. (2020). Normal mode analysis: A tool for better understanding protein flexibility and dynamics with application to homology models. In R. F. Maia, R. M. de Moraes Filho, & M. De Araujo Campos (Ed.), Homology molecular modeling – Perspectives and applications [working title]. IntechOpen. https://doi.org/10.5772/intechopen.94139
  • Breslow, J. L., Ross, D., McPherson, J., Williams, H., Kurnit, D., Nussbaum, A. L., Karathanasis, S. K., & Zannis, V. I. (1982). Isolation and characterization of cDNA clones for human apolipoprotein A-I. Proceedings of the National Academy of Sciences of the United States of America, 79(22), 6861–6865. https://doi.org/10.1073/pnas.79.22.6861
  • Calandra, S., & Tarugi, P. (1993). Synthesis and secretion of apolipoprotein A-I. Biochemical Society Transactions, 21(2), 493–499. https://doi.org/10.1042/bst0210493
  • Camps, J., Carrillo, O., Emperador, A., Orellana, L., Hospital, A., Rueda, M., Cicin-Sain, D., D'Abramo, M., Gelpí, J. L., & Orozco, M. (2009). FlexServ: An integrated tool for the analysis of protein flexibility. Bioinformatics, 25(13), 1709–1710. https://doi.org/10.1093/bioinformatics/btp304
  • Chandrasekaran, P., & Rajasekaran, R. (2016). A systematic molecular dynamics approach to the structural characterization of amyloid aggregation propensity of β2-microglobulin mutant D76N. Molecular BioSystems, 12(3), 850–859. https://doi.org/10.1039/c5mb00759c
  • Chiti, F., & Dobson, C. M. (2017). Protein misfolding, amyloid formation, and human disease: A summary of progress over the last decade. Annual Review of Biochemistry, 86(1), 27–68. https://doi.org/10.1146/annurev-biochem-061516-045115
  • Dahiyat, B. I., Gordon, D. B., & Mayo, S. L. (1997). Automated design of the surface positions of protein helices: Protein surface design. Protein Science: A Publication of the Protein Society, 6(6), 1333–1337. https://doi.org/10.1002/pro.5560060622
  • Dalla-Riva, J., Lagerstedt, J. O., & Petrlova, J. (2015). Structural and functional analysis of the apolipoproteinA-I A164S variant. PLoS One, 10(11), e0143915. https://doi.org/10.1371/journal.pone.0143915
  • Das, M., & Gursky, O. (2015). Amyloid-forming properties of human apolipoproteins: Sequence analyses and structural insights. Advances in Experimental Medicine and Biology, 855, 175–211. https://doi.org/10.1007/978-3-319-17344-3_8 [PMC][26149931
  • de Sousa, M. M., Vital, C., Ostler, D., Fernandes, R., Pouget-Abadie, J., Carles, D., & Saraiva, M. J. (2000). Apolipoprotein AI and transthyretin as components of amyloid fibrils in a kindred with apoAI Leu178His amyloidosis. The American Journal of Pathology, 156(6), 1911–1917. https://doi.org/10.1016/S0002-9440(10)65064-X
  • Del Giudice, R., Domingo-Espín, J., Iacobucci, I., Nilsson, O., Monti, M., Monti, D. M., & Lagerstedt, J. O. (2017). Structural determinants in ApoA-I amyloidogenic variants explain improved cholesterol metabolism despite low HDL levels. Biochimica et Biophysica Acta. Molecular Basis of Disease, 1863(12), 3038–3048. https://doi.org/10.1016/j.bbadis.2017.09.001
  • Dima, R. I., & Thirumalai, D. (2004). Probing the instabilities in the dynamics of helical fragments from mouse PrPC. Proceedings of the National Academy of Sciences of the United States of America, 101(43), 15335–15340. https://doi.org/10.1073/pnas.0404235101
  • Ding, F., Tsao, D., Nie, H., & Dokholyan, N. V. (2008). Ab initio folding of proteins with all-atom discrete molecular dynamics. Structure (London, England: 1993), 16(7), 1010–1018. https://doi.org/10.1016/j.str.2008.03.013
  • E, W., & Li, D. (2008). The Andersen thermostat in molecular dynamics. Communications on Pure and Applied Mathematics, 61(1), 96–136. https://doi.org/10.1002/cpa.20198
  • Eriksson, M., Schönland, S., Yumlu, S., Hegenbart, U., von Hutten, H., Gioeva, Z., Lohse, P., Büttner, J., Schmidt, H., & Röcken, C. (2009). Hereditary apolipoprotein AI-associated amyloidosis in surgical pathology specimens: Identification of three novel mutations in the APOA1 gene. The Journal of Molecular Diagnostics, 11(3), 257–262. https://doi.org/10.2353/jmoldx.2009.080161
  • Feingold, K. R. (2000). Introduction to lipids and lipoproteins. In K. R. Feingold, B. Anawalt, A. Boyce, G. Chrousos, W. W. de Herder, K. Dungan, A. Grossman, J. M. Hershman, J. Hofland, G. Kaltsas, C. Koch, P. Kopp, M. Korbonits, R. McLachlan, J. E. Morley, M. New, J. Purnell, F. Singer, C. A. Stratakis, … D. P. Wilson (Eds.), Endotext. MDText.com, Inc. http://www.ncbi.nlm.nih.gov/books/NBK305896/
  • Frappier, V., & Najmanovich, R. J. (2014). A coarse-grained elastic network atom contact model and its use in the simulation of protein dynamics and the prediction of the effect of mutations. PLoS Computational Biology, 10(4), e1003569. https://doi.org/10.1371/journal.pcbi.1003569
  • Fuglebakk, E., Echave, J., & Reuter, N. (2012). Measuring and comparing structural fluctuation patterns in large protein datasets. Bioinformatics (Oxford, England), 28(19), 2431–2440. https://doi.org/10.1093/bioinformatics/bts445
  • Gillmore, J. D., Stangou, A. J., Lachmann, H. J., Goodman, H. J., Wechalekar, A. D., Acheson, J., Tennent, G. A., Bybee, A., Gilbertson, J., Rowczenio, D., O'Grady, J., Heaton, N. D., Pepys, M. B., & Hawkins, P. N. (2006). Organ transplantation in hereditary apolipoprotein AI amyloidosis. American Journal of Transplantation, 6(10), 2342–2347. https://doi.org/10.1111/j.1600-6143.2006.01507.x
  • Gisonno, R., Masson, T., Ramella, N., Barrera, E., Romanowski, V., & Tricerri, M. (2021). Evolutionary and structural constraints influencing apolipoprotein A-I amyloid behavior.Proteins. doi: 10.1002/prot.26217(published online ahead of print)
  • Gomaraschi, M., Obici, L., Simonelli, S., Gregorini, G., Negrinelli, A., Merlini, G., Franceschini, G., & Calabresi, L. (2011). Effect of the amyloidogenic L75P apolipoprotein A-I variant on HDL subpopulations. Clinica Chimica Acta; International Journal of Clinical Chemistry, 412(13–14), 1262–1265. https://doi.org/10.1016/j.cca.2011.03.027
  • Grant, B. J., Rodrigues, A. P. C., ElSawy, K. M., McCammon, J. A., & Caves, L. S. D. (2006). Bio3d: An R package for the comparative analysis of protein structures. Bioinformatics, 22(21), 2695–2696. https://doi.org/10.1093/bioinformatics/btl461
  • Hamidi Asl, L., Liepnieks, J. J., Hamidi Asl, K., Uemichi, T., Moulin, G., Desjoyaux, E., Loire, R., Delpech, M., Grateau, G., & Benson, M. D. (1999). Hereditary amyloid cardiomyopathy caused by a variant apolipoprotein A1. The American Journal of Pathology, 154(1), 221–227. https://doi.org/10.1016/S0002-9440(10)65268-6
  • Hamidi Asl, K., Liepnieks, J. J., Nakamura, M., Parker, F., & Benson, M. D. (1999). A novel apolipoprotein A-1 variant, Arg173Pro, associated with cardiac and cutaneous amyloidosis. Biochemical and Biophysical Research Communications, 257(2), 584–588. https://doi.org/10.1006/bbrc.1999.0518
  • Hazenberg, A. J. C., Dikkers, F. G., Hawkins, P. N., Bijzet, J., Rowczenio, D., Gilbertson, J., Posthumus, M. D., Leijsma, M. K., & Hazenberg, B. P. C. (2009). Laryngeal presentation of systemic apolipoprotein A-I-derived amyloidosis. The Laryngoscope, 119(3), 608–615. https://doi.org/10.1002/lary.20106
  • He, Y., Song, H. D., Anantharamaiah, G. M., Palgunachari, M. N., Bornfeldt, K. E., Segrest, J. P., & Heinecke, J. W. (2019). Apolipoprotein A1 forms 5/5 and 5/4 antiparallel dimers in human high-density lipoprotein. Molecular & Cellular Proteomics, 18(5), 854–864. https://doi.org/10.1074/mcp.RA118.000878
  • Hess, B., Kutzner, C., van der Spoel, D., & Lindahl, E. (2008). GROMACS 4: Algorithms for highly efficient, load-balanced, and scalable molecular simulation. Journal of Chemical Theory and Computation, 4(3), 435–447. https://doi.org/10.1021/ct700301q
  • Hinsen, K., Petrescu, A.-J., Dellerue, S., Bellissent-Funel, M.-C., & Kneller, G. R. (2000). Harmonicity in slow protein dynamics. Chemical Physics, 261(1–2), 25–37. https://doi.org/10.1016/S0301-0104(00)00222-6
  • Humphrey, W., Dalke, A., & Schulten, K. (1996). VMD: Visual molecular dynamics. Journal of Molecular Graphics, 14(1), 33–38, 27–28. https://doi.org/10.1016/0263-7855(96)00018-5
  • Jacobs, D. J., & Thorpe, M. F. (1995). Generic rigidity percolation: The Pebble game. Physical Review Letters, 75(22), 4051–4054. https://doi.org/10.1103/PhysRevLett.75.4051
  • Kabsch, W., & Sander, C. (1983). Dictionary of protein secondary structure: Pattern recognition of hydrogen-bonded and geometrical features. Biopolymers, 22(12), 2577–2637. https://doi.org/10.1002/bip.360221211
  • Kalsi, N., Gopalakrishnan, C., Rajendran, V., & Purohit, R. (2016). Biophysical aspect of phosphatidylinositol 3-kinase and role of oncogenic mutants (E542K & E545K). Journal of Biomolecular Structure & Dynamics, 34(12), 2711–2721. https://doi.org/10.1080/07391102.2015.1127774
  • Kauzmann, W. (1959). Some factors in the interpretation of protein denaturation. In C. B. Anfinsen Jr., M. L. Anson, K. Bailey, J. T. Edsall (Eds.), Advances in protein chemistry (Vol. 14, pp. 1–63). Elsevier. https://doi.org/10.1016/S0065-3233(08)60608-7
  • Krieger, E., & Vriend, G. (2014). YASARA view – molecular graphics for all devices – from smartphones to workstations. Bioinformatics (Oxford, England), 30(20), 2981–2982. https://doi.org/10.1093/bioinformatics/btu426
  • Kumar, A., Rajendran, V., Sethumadhavan, R., & Purohit, R. (2013). Molecular dynamic simulation reveals damaging impact of RAC1 F28L mutation in the switch I region. PLoS One, 8(10), e77453. https://doi.org/10.1371/journal.pone.0077453
  • Lachmann, H. J., Booth, D. R., Booth, S. E., Bybee, A., Gilbertson, J. A., Gillmore, J. D., Pepys, M. B., & Hawkins, P. N. (2002). Misdiagnosis of hereditary amyloidosis as AL (primary) amyloidosis. The New England Journal of Medicine, 346(23), 1786–1791. https://doi.org/10.1056/NEJMoa013354
  • Laio, A., & Parrinello, M. (2002). Escaping free-energy minima. Proceedings of the National Academy of Sciences of the United States of America, 99(20), 12562–12566. https://doi.org/10.1073/pnas.202427399
  • Lezon, T. R., Shrivastava, I. H., Yang, Z., & Bahar, I. (2009). Elastic network models for biomolecular dynamics: Theory and application to membrane proteins and viruses. In S. Boccaletti, V. Latora, & Y. Moreno (Eds.), World Scientific lecture notes in complex systems (Vol. 10, pp. 129–158). World Scientific. https://doi.org/10.1142/9789812838803_0007
  • Liu, W., Prausnitz, J. M., & Blanch, H. W. (2004). Amyloid fibril formation by peptide LYS (11-36) in aqueous trifluoroethanol. Biomacromolecules, 5(5), 1818–1823. https://doi.org/10.1021/bm049841e
  • Lu, C., Zuo, K., Lu, Y., Liang, S., Huang, X., Zeng, C., Zhang, J., An, Y., & Wang, J. (2017). Apolipoprotein A-1-related amyloidosis 2 case reports and review of the literature. Medicine, 96(39), e8148. https://doi.org/10.1097/MD.0000000000008148
  • McQueen, M. J., Hawken, S., Wang, X., Ounpuu, S., Sniderman, A., Probstfield, J., Steyn, K., Sanderson, J. E., Hasani, M., Volkova, E., Kazmi, K., & Yusuf, S, & INTERHEART study investigators. (2008). Lipids, lipoproteins, and apolipoproteins as risk markers of myocardial infarction in 52 countries (the INTERHEART study): A case-control study. The Lancet (London, England), 372(9634), 224–233. https://doi.org/10.1016/S0140-6736(08)61076-4
  • Mishra, A., Ranganathan, S., Jayaram, B., & Sattar, A. (2018). Role of solvent accessibility for aggregation-prone patches in protein folding. Scientific Reports, 8(1), 12896. https://doi.org/10.1038/s41598-018-31289-6[PMC]
  • Morgado, I., Panahi, A., Burwash, A. G., Das, M., Straub, J. E., & Gursky, O. (2018). Molecular insights into human hereditary apolipoprotein A-I amyloidosis caused by the Glu34Lys mutation. Biochemistry, 57(39), 5738–5747. https://doi.org/10.1021/acs.biochem.8b00817
  • Nichols, W. C., Dwulet, F. E., Liepnieks, J., & Benson, M. D. (1988). Variant apolipoprotein AI as a major constituent of a human hereditary amyloid. Biochemical and Biophysical Research Communications, 156(2), 762–768. https://doi.org/10.1016/S0006-291X(88)80909-4
  • Obici, L., Bellotti, V., Mangione, P., Stoppini, M., Arbustini, E., Verga, L., Zorzoli, I., Anesi, E., Zanotti, G., Campana, C., Viganò, M., & Merlini, G. (1999). The new apolipoprotein A-I variant leu(174) –> Ser causes hereditary cardiac amyloidosis, and the amyloid fibrils are constituted by the 93-residue N-terminal polypeptide. The American Journal of Pathology, 155(3), 695–702. https://doi.org/10.1016/S0002-9440(10)65167-X
  • Pandurangan, A. P., Ochoa-Montaño, B., Ascher, D. B., & Blundell, T. L. (2017). SDM: A server for predicting effects of mutations on protein stability. Nucleic Acids Research, 45(W1), W229–W235. https://doi.org/10.1093/nar/gkx439
  • Pankhurst, G., Wang, X. L., Wilcken, D. E., Baernthaler, G., Panzenböck, U., Raftery, M., & Stocker, R. (2003). Characterization of specifically oxidized apolipoproteins in mildly oxidized high density lipoprotein. Journal of Lipid Research, 44(2), 349–355. https://doi.org/10.1194/jlr.M200256-JLR200
  • Papaleo, E., Mereghetti, P., Fantucci, P., Grandori, R., & De Gioia, L. (2009). Free-energy landscape, principal component analysis, and structural clustering to identify representative conformations from molecular dynamics simulations: The myoglobin case. Journal of Molecular Graphics & Modelling, 27(8), 889–899. https://doi.org/10.1016/j.jmgm.2009.01.006
  • Petrlova, J., Duong, T., Cochran, M. C., Axelsson, A., Mörgelin, M., Roberts, L. M., & Lagerstedt, J. O. (2012). The fibrillogenic L178H variant of apolipoprotein A-I forms helical fibrils. Journal of Lipid Research, 53(3), 390–398. https://doi.org/10.1194/jlr.M020883
  • Picken, M. M. (2020). The pathology of amyloidosis in classification: A review. Acta Haematologica, 143(4), 322–334. https://doi.org/10.1159/000506696
  • Rader, A. J., Hespenheide, B. M., Kuhn, L. A., & Thorpe, M. F. (2002). Protein unfolding: Rigidity lost. Proceedings of the National Academy of Sciences, 99(6), 3540–3545. https://doi.org/10.1073/pnas.062492699
  • Raghuraman, P., & Sudandiradoss, C. (2019). R516Q mutation in Melanoma differentiation-associated protein 5 (MDA5) and its pathogenic role towards rare Singleton-Merten syndrome; a signature associated molecular dynamics study. Journal of Biomolecular Structure & Dynamics, 37(3), 750–765. https://doi.org/10.1080/07391102.2018.1439770
  • Rajendran, V., Purohit, R., & Sethumadhavan, R. (2012). In silico investigation of molecular mechanism of laminopathy caused by a point mutation (R482W) in lamin A/C protein. Amino Acids, 43(2), 603–615. https://doi.org/10.1007/s00726-011-1108-7
  • Rambaran, R. N., & Serpell, L. C. (2008). Amyloid fibrils: Abnormal protein assembly. Prion, 2(3), 112–117. https://doi.org/10.4161/pri.2.3.7488
  • Reeb, J., & Rost, B. (2019). Secondary structure prediction. In S. Ranganathan, M. Gribskov, K. Nakai, & C. Schönbach (Eds.), Encyclopedia of bioinformatics and computational biology (pp. 488–496). Elsevier. https://doi.org/10.1016/B978-0-12-809633-8.20267-7
  • Rodrigues, C. H., Pires, D. E., & Ascher, D. B. (2018). DynaMut: Predicting the impact of mutations on protein conformation, flexibility and stability. Nucleic Acids Research, 46(W1), W350–W355. https://doi.org/10.1093/nar/gky300
  • Rosú, S. A., Rimoldi, O. J., Prieto, E. D., Curto, L. M., Delfino, J. M., Ramella, N. A., & Tricerri, M. A. (2015). Amyloidogenic propensity of a natural variant of human apolipoprotein A-I: Stability and interaction with ligands. PLoS One, 10(5), e0124946. https://doi.org/10.1371/journal.pone.0124946
  • Rueda, M., Cubero, E., Laughton, C. A., & Orozco, M. (2004). Exploring the counterion atmosphere around DNA: What can be learned from molecular dynamics simulations?. Biophysical Journal, 87(2), 800–811. https://doi.org/10.1529/biophysj.104.040451
  • Sfriso, P., Emperador, A., Orellana, L., Hospital, A., Gelpí, J. L., & Orozco, M. (2012). Finding conformational transition pathways from discrete molecular dynamics simulations. Journal of Chemical Theory and Computation, 8(11), 4707–4718. https://doi.org/10.1021/ct300494q
  • Sfriso, P., Hospital, A., Emperador, A., & Orozco, M. (2013). Exploration of conformational transition pathways from coarse-grained simulations. Bioinformatics, 29(16), 1980–1986. https://doi.org/10.1093/bioinformatics/btt324
  • Shirvanyants, D., Ding, F., Tsao, D., Ramachandran, S., & Dokholyan, N. V. (2012). Discrete molecular dynamics: An efficient and versatile simulation method for fine protein characterization. The Journal of Physical Chemistry, B, 116(29), 8375–8382. https://doi.org/10.1021/jp2114576
  • Sorci-Thomas, M. G., Bhat, S., & Thomas, M. J. (2009). Activation of lecithin:cholesterol acyltransferase by HDL ApoA-I central helices. Clinical Lipidology, 4(1), 113–124. https://doi.org/10.2217/17584299.4.1.113
  • Testro, A. G., Brennan, S. O., Macdonell, R. A. L., Hawkins, P. N., & Angus, P. W. (2007). Hereditary amyloidosis with progressive peripheral neuropathy associated with apolipoprotein AI Gly26Arg: Outcome of hepatorenal transplantation. Liver Transplantation: Official Publication of the American Association for the Study of Liver Diseases and the International Liver Transplantation Society, 13(7), 1028–1031. https://doi.org/10.1002/lt.21176
  • Thirumal Kumar, D., & George Priya Doss, C. (2017). Role of E542 and E545 missense mutations of PIK3CA in breast cancer: A comparative computational approach. Journal of Biomolecular Structure & Dynamics, 35(12), 2745–2757. https://doi.org/10.1080/07391102.2016.1231082
  • Thirumal Kumar, D., George Priya Doss, C., Sneha, P., Tayubi, I. A., Siva, R., Chakraborty, C., & Magesh, R. (2017). Influence of V54M mutation in giant muscle protein titin: A computational screening and molecular dynamics approach. Journal of Biomolecular Structure & Dynamics, 35(5), 917–928. https://doi.org/10.1080/07391102.2016.1166456
  • Tiwari, S. P., Fuglebakk, E., Hollup, S. M., Skjaerven, L., Cragnolini, T., Grindhaug, S. H., Tekle, K. M., & Reuter, N. (2014). WEBnm@ v2.0: Web server and services for comparing protein flexibility. BMC Bioinformatics, 15, 427. https://doi.org/10.1186/s12859-014-0427-6[PMC][25547242
  • van der Vorst, E. P. C. (2020). High-density lipoproteins and apolipoprotein A1. Sub-Cellular Biochemistry, 94, 399–420. https://doi.org/10.1007/978-3-030-41769-7_16 [PMC][32189309]
  • Virtanen, P., Gommers, R., Oliphant, T. E., Haberland, M., Reddy, T., Cournapeau, D., Burovski, E., Peterson, P., Weckesser, W., Bright, J., van der Walt, S. J., Brett, M., Wilson, J., Millman, K. J., Mayorov, N., Nelson, A. R. J., Jones, E., Kern, R., Larson, E., van Mulbregt, P., & SciPy 1.0 Contributors. (2020). SciPy 1.0: Fundamental algorithms for scientific computing in Python. Nature Methods, 17(3), 261–272. https://doi.org/10.1038/s41592-019-0686-2
  • Vriend, G. (1990). WHAT IF: A molecular modeling and drug design program. Journal of Molecular Graphics, 8(1), 52–56. https://doi.org/10.1016/0263-7855(90)80070-V
  • Wako, H., & Endo, S. (2017). Normal mode analysis as a method to derive protein dynamics information from the Protein Data Bank. Biophysical Reviews, 9(6), 877–893. https://doi.org/10.1007/s12551-017-0330-2
  • Wu, Z., Gogonea, V., Lee, X., Wagner, M. A., Li, X.-M., Huang, Y., Undurti, A., May, R. P., Haertlein, M., Moulin, M., Gutsche, I., Zaccai, G., Didonato, J. A., & Hazen, S. L. (2009). Double superhelix model of high density lipoprotein. The Journal of Biological Chemistry, 284(52), 36605–36619. https://doi.org/10.1074/jbc.M109.039537
  • Yui, Y., Aoyama, T., Morishita, H., Takahashi, M., Takatsu, Y., & Kawai, C. (1988). Serum prostacyclin stabilizing factor is identical to apolipoprotein A-I (Apo A-I). A novel function of Apo A-I. The Journal of Clinical Investigation, 82(3), 803–807. https://doi.org/10.1172/JCI113682

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