Comparison of HIV-1 Vif and Vpu accessory proteins for delivery of polyepitope constructs harboring Nef, Gp160 and P24 using various cell penetrating peptides

1. Tissot AC, Renhofa R, Schmitz N, Cielens I, Meijerink E, Ose V, Jennings GT, Saudan P, Pumpens P, Bachmann MF. Versatile virus-like particle carrier for epitope based vaccines. PLoS One. 2010; 5(3).

2. Purcell AW, McCluskey J, Rossjohn J. More than one reason to rethink the use of peptides in vaccine design. Nature reviews Drug discovery. 2007; 6(5): 404. doi: 10.1038/nrd2224 17473845

3. Frey BF, Jiang J, Sui Y, Boyd LF, Yu B, Tatsuno G, Billeskov R, Solaymani-Mohammadi S, Berman PW, Margulies DH, Berzofsky JA. Effects of cross-presentation, antigen processing, and peptide binding in HIV evasion of T cell immunity. The Journal of Immunology. 2018; 200(5):1853–1864. doi: 10.4049/jimmunol.1701523 29374075

4. Gao Y, McKay P, Mann J. Advances in HIV-1 vaccine development. Viruses. 2018; 10(4): 167.

5. Haleyur Giri Setty MK, Kurdekar A, Mahtani P, Liu J, Hewlett IK. Cross-subtype detection of HIV-1 capsid p24 antigen using a sensitive europium nanoparticle assay. AIDS research and human retroviruses. 2019.

6. Elhassan RM, Alsony NM, Othman KM, Izz-Aldin DT, Alhaj TA, Ali AA, Abashir LA, Ahmed OH, Hassan MA. Computational vaccinology approach: Designing an efficient multi-epitope peptide vaccine against Cryptococcus neoformans var. grubii heat shock 70 KDa protein. BioRxiv. 2019; 1: 534008

7. Moyle PM, Toth I. Modern subunit vaccines: development, components, and research opportunities. ChemMedChem. 2013; 8(3): 360–376. doi: 10.1002/cmdc.201200487 23316023

8. Schubert B, Lund O, Nielsen M. Evaluation of peptide selection approaches for epitope-based vaccine design. Tissue Antigens. 2013; 82(4): 243–251. 24461003

9. Belnoue E, Di Berardino-Besson W, Gaertner H, Carboni S, Dunand-Sauthier I, Cerini F, Suso-Inderberg EM, Wälchli S, König S, Salazar AM, Hartley O. Enhancing antitumor immune responses by optimized combinations of cell-penetrating peptide-based vaccines and adjuvants. Molecular Therapy. 2016; 24(9): 1675–1685. doi: 10.1038/mt.2016.134 27377043

10. Brooks NA, Pouniotis DS, Tang CK, Apostolopoulos V, Pietersz GA. Cell-penetrating peptides: application in vaccine delivery. Biochimica et Biophysica Acta (BBA)-Reviews on Cancer. 2010; 1805(1): 25–34.

11. Doan T, Herd K, Ramshaw I, Thomson S, Tindle RW. A polytope DNA vaccine elicits multiple effector and memory CTL responses and protects against human papillomavirus 16 E7-expressing tumour. Cancer Immunology, Immunotherapy. 2005; 54(2): 157–171. doi: 10.1007/s00262-004-0544-6 15480657

12. Yasmin T, Akter S, Debnath M, Ebihara A, Nakagawa T, Nabi AN. In silico proposition to predict cluster of B-and T-cell epitopes for the usefulness of vaccine design from invasive, virulent and membrane associated proteins of C. jejuni. In silico Pharmacology. 2016; 4(1): 5. doi: 10.1186/s40203-016-0020-y 27376537

13. Yang X, Yu X. An introduction to epitope prediction methods and software. Reviews in Medical Virology. 2009; 19(2): 77–96. doi: 10.1002/rmv.602 19101924

14. Frankel AD, Young JA. HIV-1: fifteen proteins and an RNA. Annu Rev Biochem. 1998; 67: 1–25. doi: 10.1146/annurev.biochem.67.1.1 9759480

15. Berthet Colominas C, Monaco S, Novelli A, Sibaï G, Mallet F, Cusack S. Head to tail dimers and interdomain flexibility revealed by the crystal structure of HIV-1 capsid protein (p24) complexed with a monoclonal antibody Fab. The EMBO Journal. 1999; 18(5): 1124–1136. doi: 10.1093/emboj/18.5.1124 10064580

16. Goncalves J, Silva F, Freitas-Vieira A, Santa-Marta M, Malhó R, Yang X, Gabuzda D, Barbas C. Functional neutralization of HIV-1 Vif protein by intracellular immunization inhibits reverse transcription and viral replication. Journal of Biological Chemistry. 2002; 277(35): 32036–32045. doi: 10.1074/jbc.M201906200 12039955

17. Quaranta MG, Mattioli B, Giordani L, Viora M. Immunoregulatory effects of HIV-1 Nef protein. Biofactors. 2009; 35(2): 169–174. doi: 10.1002/biof.28 19449444

18. Willey RL, Maldarelli F, Martin MA, Strebel K. Human immunodeficiency virus type 1 Vpu protein regulates the formation of intracellular gp160-CD4 complexes. Journal of Virology. 1992; 66(1): 226–234. 1727486

19. Dakappagari NK, Sundaram R, Rawale S, Liner A, Galloway DR, Kaumaya PT. Intracellular delivery of a novel multiepitope peptide vaccine by an amphipathic peptide carrier enhances cytotoxic T-cell responses in HLA-A* 201 mice. The Journal of Peptide Research. 2005; 65(2):189–199. doi: 10.1111/j.1399-3011.2005.00212.x 15705163

20. Bolhassani A, Kardani K, Vahabpour R, Habibzadeh N, Aghasadeghi MR, Sadat SM, Agi E. Prime/boost immunization with HIV-1 MPER-V3 fusion construct enhances humoral and cellular immune responses. Immunology Letters. 2015; 168(2): 366–373. doi: 10.1016/j.imlet.2015.10.012 26518142

21. Liu BR, Huang YW, Winiarz JG, Chiang HJ, Lee HJ. Intracellular delivery of quantum dots mediated by a histidine-and arginine-rich HR9 cell-penetrating peptide through the direct membrane translocation mechanism. Biomaterials. 2011; 32(13): 3520–3537. doi: 10.1016/j.biomaterials.2011.01.041 21329975

22. Bolhassani A, Jafarzade BS, Mardani G. In vitro and in vivo delivery of therapeutic proteins using cell penetrating peptides. Peptides. 2017; 87: 50–63. doi: 10.1016/j.peptides.2016.11.011 27887988

23. Wang F, Wang Y, Zhang X, Zhang W, Guo S, Jin F. Recent progress of cell-penetrating peptides as new carriers for intracellular cargo delivery. Journal of Controlled Release. 2014; 174: 126–136. doi: 10.1016/j.jconrel.2013.11.020 24291335

24. Morris MC, Deshayes S, Heitz F, Divita G. Cell penetrating peptides: from molecular mechanisms to therapeutics. Biology of the Cell. 2008; 100(4): 201–217. doi: 10.1042/BC20070116 18341479

25. Liu BR, Lin MD, Chiang HJ, Lee HJ. Arginine-rich cell-penetrating peptides deliver gene into living human cells. Gene. 2012; 505(1): 37–45. doi: 10.1016/j.gene.2012.05.053 22669044

26. Ponnappan N, Budagavi DP, Chugh A. CyLoP-1: Membrane-active peptide with cell-penetrating and antimicrobial properties. Biochimica et Biophysica Acta (BBA)-Biomembranes. 2017; 1859(2):167–176.

27. Ponnappan N, Chugh A. Cell-penetrating and cargo-delivery ability of a spider toxin-derived peptide in mammalian cells. European Journal of Pharmaceutics and Biopharmaceutics. 2017; 114:145–153. doi: 10.1016/j.ejpb.2017.01.012 28159722

28. Khairkhah N, Namvar A, Kardani K, Bolhassani A. Prediction of cross-clade HIV-1 T cell epitopes using immunoinformatics analysis. Proteins: Structure, Function, and Bioinformatics. 2018; 86(12):1284–1293.

29. Panahi HA, Bolhassani A, Javadi G, Noormohammadi Z. A comprehensive in silico analysis for identification of therapeutic epitopes in HPV16, 18, 31 and 45 oncoproteins. PloS one. 2018; 13(10): e0205933. doi: 10.1371/journal.pone.0205933 30356257

30. Moret I, Peris JE, Guillem VM, Benet M, Revert F, Dasí F, Crespo A, Aliño SF. Stability of PEI–DNA and DOTAP–DNA complexes: effect of alkaline pH, heparin and serum. Journal of Controlled Release. 2001; 76(1–2): 169–181. doi: 10.1016/s0168-3659(01)00415-1 11532322

31. Saleh T, Bolhassani A, Shojaosadati SA, Aghasadeghi MR. MPG-based nanoparticle: An efficient delivery system for enhancing the potency of DNA vaccine expressing HPV16E7. Vaccine. 2015; 33(28): 3164–3170. doi: 10.1016/j.vaccine.2015.05.015 26001433

32. Tenzer S, Peters B, Bulik S, Schoor O, Lemmel C, Schatz MM, Kloetzel PM, Rammensee HG, Schild H, Holzhütter HG. Modeling the MHC class I pathway by combining predictions of proteasomal cleavage, TAP transport and MHC class I binding. Cellular and Molecular Life Sciences CMLS. 2005; 62(9):1025–1037. doi: 10.1007/s00018-005-4528-2 15868101

33. Abdoli A, Radmehr N, Bolhassani A, Eidi A, Mehrbod P, Motevalli F, Kianmehr Z, Chiani M, Mahdavi M, Yazdani S, Ardestani MS. Conjugated anionic PEG-citrate G2 dendrimer with multi-epitopic HIV-1 vaccine candidate enhance the cellular immune responses in mice. Artificial cells, nanomedicine, and biotechnology. 2017; 45(8):1762–1768. doi: 10.1080/21691401.2017.1290642 28278580

34. Soria-Guerra RE, Nieto-Gomez R, Govea-Alonso DO, Rosales-Mendoza S. An overview of bioinformatics tools for epitope prediction: implications on vaccine development. Journal of Biomedical Informatics. 2015; 53: 405–414. doi: 10.1016/j.jbi.2014.11.003 25464113

35. Létourneau S, Im EJ, Mashishi T, Brereton C, Bridgeman A, Yang H, Dorrell L, Dong T, Korber B, McMichael AJ, Hanke T. Design and pre-clinical evaluation of a universal HIV-1 vaccine. PloS one. 2007; 2(10): e984. doi: 10.1371/annotation/fca26a4f-42c1-4772-a19e-aa9d96c4eeb2 17912361

36. Wilson CC, Newman MJ, Livingston BD, MaWhinney S, Forster JE, Scott J, Schooley RT, Benson CA. Clinical phase 1 testing of the safety and immunogenicity of an epitope-based DNA vaccine in human immunodeficiency virus type 1-infected subjects receiving highly active antiretroviral therapy. Clin Vaccine Immunol. 2008; 15(6): 986–994. doi: 10.1128/CVI.00492-07 18400976

37. Li F, Finnefrock AC, Dubey SA, Korber BT, Szinger J, Cole S, McElrath MJ, Shiver JW, Casimiro DR, Corey L, Self SG. Mapping HIV-1 vaccine induced T-cell responses: bias towards less-conserved regions and potential impact on vaccine efficacy in the step study. PloS one. 2011; 6(6): e20479. doi: 10.1371/journal.pone.0020479 21695251

38. Wilson CC, McKinney D, Anders M, MaWhinney S, Forster J, Crimi C, Southwood S, Sette A, Chesnut R, Newman MJ, Livingston BD. Development of a DNA vaccine designed to induce cytotoxic T lymphocyte responses to multiple conserved epitopes in HIV-1. The Journal of Immunology. 2003; 171(10): 5611–5623. doi: 10.4049/jimmunol.171.10.5611 14607970

39. Watanabe K, Murakoshi H, Tamura Y, Koyanagi M, Chikata T, Gatanaga H, Oka S, Takiguchi M. Identification of cross-clade CTL epitopes in HIV-1 clade A/E-infected individuals by using the clade B overlapping peptides. Microbes and Infection. 2013; 15(13): 874–886. doi: 10.1016/j.micinf.2013.08.002 23968885

40. Murakoshi H, Zou C, Kuse N, Akahoshi T, Chikata T, Gatanaga H, Oka S, Hanke T, Takiguchi M. CD8+ T cells specific for conserved, cross-reactive Gag epitopes with strong ability to suppress HIV-1 replication. Retrovirology. 2018; 15(1): 46. doi: 10.1186/s12977-018-0429-y 29970102

41. Murakoshi H, Akahoshi T, Koyanagi M, Chikata T, Naruto T, Maruyama R, Tamura Y, Ishizuka N, Gatanaga H, Oka S, Takiguchi M. Clinical control of HIV-1 by cytotoxic T cells specific for multiple conserved epitopes. Journal of Virology. 2015; 89(10): 5330–5339. doi: 10.1128/JVI.00020-15 25741000

42. Herschhorn A, Marasco WA, Hizi A. Antibodies and lentiviruses that specifically recognize a T cell epitope derived from HIV-1 Nef protein and presented by HLA-C. The Journal of Immunology. 2010; 185(12):7623–7632. doi: 10.4049/jimmunol.1001561 21076072

43. De Groot AS, Jesdale B, Martin W, Saint Aubin C, Sbai H, Bosma A, Lieberman J, Skowron G, Mansourati F, Mayer KH. Mapping cross-clade HIV-1 vaccine epitopes using a bioinformatics approach. Vaccine. 2003; 21(27–30): 4486–4504. doi: 10.1016/s0264-410x(03)00390-6 14505932

44. De Groot AS, Martin W. Reducing risk, improving outcomes: bioengineering less immunogenic protein therapeutics. Clinical Immunology. 2009; 131(2): 189–201. doi: 10.1016/j.clim.2009.01.009 19269256

45. Milani A, Bolhassani A, Shahbazi S, Motevalli F, Sadat SM, Soleymani S. Small heat shock protein 27: An effective adjuvant for enhancement of HIV-1 Nef antigen-specific immunity. Immunology Letters. 2017; 191: 16–22. doi: 10.1016/j.imlet.2017.09.005 28917624

46. Krupka M, Zachova K, Cahlikova R, Vrbkova J, Novak Z, Sebela M, Weigl E, Raska M. Endotoxin-minimized HIV-1 p24 fused to murine hsp70 activates dendritic cells, facilitates endocytosis and p24-specific Th1 response in mice. Immunology Letters. 2015; 166(1): 36–44. doi: 10.1016/j.imlet.2015.05.010 26021827

47. Fomsgaard A, Karlsson I, Gram G, Schou C, Tang S, Bang P, Kromann I, Andersen P, Andreasen LV. Development and preclinical safety evaluation of a new therapeutic HIV-1 vaccine based on 18 T-cell minimal epitope peptides applying a novel cationic adjuvant CAF01. Vaccine. 2011; 29(40):7067–7074. doi: 10.1016/j.vaccine.2011.07.025 21767590

48. De Groot AS, Rivera DS, McMurry JA, Buus S, Martin W. Identification of immunogenic HLA-B7 “Achilles’ heel” epitopes within highly conserved regions of HIV. Vaccine. 2008; 26(24): 3059–3071. doi: 10.1016/j.vaccine.2007.12.004 18206276

49. Du J, Wu X, Long F, Wen J, Hao W, Chen R, Kong X, Qian M, Jiang W. Improvement in efficacy of DNA vaccine encoding HIV-1 Vif by LIGHT gene adjuvant. Viral Immunology. 2013; 26(1): 68–74. doi: 10.1089/vim.2012.0073 23330678

50. Chakraborty S, Rahman T, Chakravorty R. Characterization of the protective HIV-1 CTL epitopes and the corresponding HLA class I alleles: a step towards designing CTL based HIV-1 vaccine. Advances in Virology. 2014; 2014.

51. Mudd PA, Martins MA, Ericsen AJ, Tully DC, Power KA, Bean AT, Piaskowski SM, Duan L, Seese A, Gladden AD, Weisgrau KL. Vaccine-induced CD8+ T cells control AIDS virus replication. Nature. 2012; 491(7422): 129. doi: 10.1038/nature11443 23023123

52. Tarosso LF, Sauer MM, Sanabani S, Giret MT, Tomiyama HI, Sidney J, Piaskowski SM, Diaz RS, Sabino EC, Sette A, Kalil-Filho J. Unexpected diversity of cellular immune responses against Nef and Vif in HIV-1-infected patients who spontaneously control viral replication. PLoS One. 2010; 5(7): e11436. doi: 10.1371/journal.pone.0011436 20625436

53. Melief CJ, Van Der Burg SH. Immunotherapy of established (pre) malignant disease by synthetic long peptide vaccines. Nature Reviews Cancer. 2008; 8(5): 351. doi: 10.1038/nrc2373 18418403

54. Skwarczynski M, Toth I. Peptide-based synthetic vaccines. Chemical Science. 2016; 7(2):842–854. doi: 10.1039/c5sc03892h 28791117

55. Jorritsma SH, Gowans EJ, Grubor-Bauk B, Wijesundara DK. Delivery methods to increase cellular uptake and immunogenicity of DNA vaccines. Vaccine. 2016; 34(46): 5488–5494 doi: 10.1016/j.vaccine.2016.09.062 27742218

56. Deshayes S, Morris M, Heitz F, Divita G. Delivery of proteins and nucleic acids using a non-covalent peptide-based strategy. Advanced Drug Delivery Reviews. 2008; 60(4–5): 537–547. doi: 10.1016/j.addr.2007.09.005 18037526

57. Morris MC, Chaloin L, Méry J, Heitz F, Divita G. A novel potent strategy for gene delivery using a single peptide vector as a carrier. Nucleic Acids Research. 1999; 27(17): 3510–3517. doi: 10.1093/nar/27.17.3510 10446241

58. Liu BR, Chen HH, Chan MH, Huang YW, Aronstam RS, Lee HJ. Three arginine-rich cell-penetrating peptides facilitate cellular internalization of red-emitting quantum dots. Journal of Nanoscience and Nanotechnology. 2015; 15(3): 2067–2078. doi: 10.1166/jnn.2015.9148 26413622

59. Jain A, Yadav BK, Chugh A. Marine antimicrobial peptide tachyplesin as an efficient nanocarrier for macromolecule delivery in plant and mammalian cells. The FEBS Journal. 2015; 282(4):732–745. doi: 10.1111/febs.13178 25514997

60. Alizadeh S, Irani S, Bolhassani A, Sadat SM. Simultaneous use of natural adjuvants and cell penetrating peptides improves HCV NS3 antigen-specific immune responses. Immunology Letters. 2019.

61. Silva JM, Videira M, Gaspar R, Préat V, Florindo HF. Immune system targeting by biodegradable nanoparticles for cancer vaccines. Journal of Controlled Release. 2013; 168(2):179–199. doi: 10.1016/j.jconrel.2013.03.010 23524187

62. Liu BR, Liou JS, Chen YJ, Huang YW, Lee HJ. Delivery of nucleic acids, proteins, and nanoparticles by arginine-rich cell-penetrating peptides in rotifers. Marine Biotechnology. 2013; 15(5): 584–595. doi: 10.1007/s10126-013-9509-0 23715807

63. Chen YJ, Liu BR, Dai YH, Lee CY, Chan MH, Chen HH, Chiang HJ, Lee HJ. A gene delivery system for insect cells mediated by arginine-rich cell-penetrating peptides. Gene. 2012; 493(2): 201–210. doi: 10.1016/j.gene.2011.11.060 22173105

64. Shahbazi S, Bolhassani A. Comparison of six cell penetrating peptides with different properties for in vitro and in vivo delivery of HPV16 E7 antigen in therapeutic vaccines. International Immunopharmacology. 2018; 62:170–180. doi: 10.1016/j.intimp.2018.07.006 30015237

65. Karpenko LI, Nekrasova NA, Ilyichev AA, Lebedev LR, Ignatyev GM, Agafonov AP, Zaitsev BN, Belavin PA, Seregin SV, Danilyuk NK, Babkina IN. Comparative analysis using a mouse model of the immunogenicity of artificial VLP and attenuated Salmonella strain carrying a DNA-vaccine encoding HIV-1 polyepitope CTL-immunogen. Vaccine. 2004; 22(13–14):1692–1699. doi: 10.1016/j.vaccine.2003.09.050 15068852

66. Habibzadeh N., Bolhassani A., Vahabpour R., Sadat S.M., How can improve DNA vaccine modalities as a therapeutic approach against HIV infections? J AIDS Clin Res. 2015; 6: 1–8.

67. Rostami B., Irani S., Bolhassani A., Cohan R.A., Gene and protein delivery using four cell penetrating peptides for HIV-1 vaccine development. IUBMB Life. 2019; 71(10): 1619–1633. doi: 10.1002/iub.2107 31220406

68. Rostami B., Irani S., Bolhassani A., Cohan R.A., M918: A novel cell penetrating peptide for effective delivery of HIV-1 Nef and Hsp20-Nef proteins into eukaryotic cell lines. Curr HIV Res. 2018; 16(4): 280–287 doi: 10.2174/1570162X17666181206111859 30520377

69. Shahbazi S., Haghighipour N., Soleymani S., Nadji S.A., Bolhassani A., Delivery of molecular cargoes in normal and cancer cell lines using non-viral delivery systems. Biotechnol Lett. 2018; 40(6): 923–931 doi: 10.1007/s10529-018-2551-2 29633093

70. Kadkhodayan S., Jafarzade B.S., Sadat S.M., Motevalli F., Agi E., Bolhassani A., Combination of cell penetrating peptides and heterologous DNA prime/protein boost strategy enhances immune responses against HIV-1 Nef antigen in BALB/c mouse model. Immunol Lett. 2017; 188: 38–45 doi: 10.1016/j.imlet.2017.06.003 28602843