Download PDF
CC BY 4.0 · Glob Med Genet 2021; 08(03): 109-115
DOI: 10.1055/s-0041-1729753
Original Article

Human Codon Usage: The Genetic Basis of Pathogen Latency

Darja Kanduc 
1   Department of Biosciences, Biotechnologies and Biopharmaceutics, University of Bari, Bari, Italy
› Author Affiliations Funding None.
› Further Information
Also available at
   Permissions and Reprints

Abstract

Infectious diseases pose two main compelling issues. First, the identification of the molecular factors that allow chronic infections, that is, the often completely asymptomatic coexistence of infectious agents with the human host. Second, the definition of the mechanisms that allow the switch from pathogen dormancy to pathologic (re)activation. Furthering previous studies, the present study (1) analyzed the frequency of occurrence of synonymous codons in coding DNA, that is, codon usage, as a genetic tool that rules protein expression; (2) described how human codon usage can inhibit protein expression of infectious agents during latency, so that pathogen genes the codon usage of which does not conform to the human codon usage cannot be translated; and (3) framed human codon usage among the front-line instruments of the innate immunity against infections. In parallel, it was shown that, while genetics can account for the molecular basis of pathogen latency, the changes of the quantitative relationship between codon frequencies and isoaccepting tRNAs during cell proliferation offer a biochemical mechanism that explains the pathogen switching to (re)activation. Immunologically, this study warns that using codon optimization methodologies can (re)activate, potentiate, and immortalize otherwise quiescent, asymptomatic pathogens, thus leading to uncontrollable pandemics.

Keywords

pathogen latency - (re)activation - protein synthesis - cross-reactivity - codon usage - tRNAs - codon optimization

Supplementary Material



Publication History

Article published online:
14 June 2021

© 2021. The Author(s). This is an open access article published by Thieme under the terms of the Creative Commons Attribution License, permitting unrestricted use, distribution, and reproduction so long as the original work is properly cited. (https://creativecommons.org/licenses/by/4.0/)

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 

  • References

  • 1 Cohen JI. Herpesvirus latency. J Clin Invest 2020; 130 (07) 3361-3369
    CrossrefPubMedGoogle Scholar
  • 2 Maroui MA, Callé A, Cohen C. et al. Latency entry of herpes simplex virus 1 is determined by the interaction of its genome with the nuclear environment. PLoS Pathog 2016; 12 (09) e1005834
    CrossrefPubMedGoogle Scholar
  • 3 Dogrammatzis C, Saleh S, Deighan C, Kalamvoki M. Diverse populations of extracellular vesicles with opposite functions during herpes simplex virus 1 infection. J Virol 2021; 95 (06) x
    CrossrefPubMedGoogle Scholar
  • 4 Dunn N, Kharlamova N, Fogdell-Hahn A. The role of herpesvirus 6A and 6B in multiple sclerosis and epilepsy. Scand J Immunol 2020; 92 (06) e12984
    CrossrefPubMedGoogle Scholar
  • 5 Elder E, Sinclair J. HCMV latency: what regulates the regulators?. Med Microbiol Immunol (Berl) 2019; 208 (3-4): 431-438
    CrossrefPubMedGoogle Scholar
  • 6 Semmes EC, Hurst JH, Walsh KM, Permar SR. Cytomegalovirus as an immunomodulator across the lifespan. Curr Opin Virol 2020; 44: 112-120
    CrossrefPubMedGoogle Scholar
  • 7 Lucchese G, Kanduc D. Cytomegalovirus infection: the neurodevelopmental peptide signatures. Curr Drug Discov Technol 2018; 15 (03) 251-262
    CrossrefPubMedGoogle Scholar
  • 8 Kanduc D. From anti-SARS-CoV-2 immune responses to COVID-19 via molecular mimicry. Antibodies (Basel) 2020; 9 (03) 33
    Google Scholar
  • 9 Gugliesi F, Coscia A, Griffante G. et al. Where do we stand after decades of studying human cytomegalovirus?. Microorganisms 2020; 8 (05) 685
    CrossrefPubMedGoogle Scholar
  • 10 Di Pietro A. Epstein-Barr virus promotes B cell lymphomas by manipulating the host epigenetic machinery. Cancers (Basel) 2020; 12 (10) 3037
    CrossrefPubMedGoogle Scholar
  • 11 Rezk SA, Weiss LM. EBV-associated lymphoproliferative disorders: update in classification. Surg Pathol Clin 2019; 12 (03) 745-770
    CrossrefPubMedGoogle Scholar
  • 12 Kanduc D. From hepatitis C virus immunoproteomics to rheumatology via cross-reactivity in one table. Curr Opin Rheumatol 2019; 31 (05) 488-492
    CrossrefPubMedGoogle Scholar
  • 13 Kanduc D. Proteome-wide Epstein-Barr virus analysis of peptide sharing with human systemic lupus erythematosus autoantigens. Isr Med Assoc J 2019; 21 (07) 444-448
    PubMedGoogle Scholar
  • 14 Vasconcelos G, Santos L, Couto C, Cruz M, Castro A. Miliary brain tuberculomas and meningitis: tuberculosis beyond the lungs. Eur J Case Rep Intern Med 2020; 7 (12) 001931
    PubMedGoogle Scholar
  • 15 Jeffers V, Tampaki Z, Kim K, Sullivan Jr WJ. A latent ability to persist: differentiation in Toxoplasma gondii . Cell Mol Life Sci 2018; 75 (13) 2355-2373
    CrossrefPubMedGoogle Scholar
  • 16 Zhao XY, Ewald SE. The molecular biology and immune control of chronic Toxoplasma gondii infection. J Clin Invest 2020; 130 (07) 3370-3380
    CrossrefPubMedGoogle Scholar
  • 17 Al Hammadi A, Mitchell M, Abraham GM, Wang JP. Recrudescence of Plasmodium falciparum in a primigravida after nearly 3 years of latency. Am J Trop Med Hyg 2017; 96 (03) 642-644
    Google Scholar
  • 18 Alanio A. Dormancy in Cryptococcus neoformans: 60 years of accumulating evidence. J Clin Invest 2020; 130 (07) 3353-3360
    CrossrefPubMedGoogle Scholar
  • 19 Lee KT, Hong J, Lee DG. et al. Fungal kinases and transcription factors regulating brain infection in Cryptococcus neoformans . Nat Commun 2020; 11 (01) 1521
    CrossrefPubMedGoogle Scholar
  • 20 Looker KJ, Magaret AS, May MT. et al. Global and regional estimates of prevalent and incident herpes simplex virus type 1 infections in 2012. PLoS One 2015; 10 (10) e0140765
    CrossrefPubMedGoogle Scholar
  • 21 Kuri A, Jacobs BM, Vickaryous N. et al. Epidemiology of Epstein-Barr virus infection and infectious mononucleosis in the United Kingdom. BMC Public Health 2020; 20 (01) 912
    CrossrefPubMedGoogle Scholar
  • 22 Shwab EK, Saraf P, Zhu XQ. et al. Human impact on the diversity and virulence of the ubiquitous zoonotic parasite Toxoplasma gondii . Proc Natl Acad Sci U S A 2018; 115 (29) E6956-E6963
    CrossrefPubMedGoogle Scholar
  • 23 Pleyer U, Gross U, Schlüter D, Wilking H, Seeber F. Toxoplasmosis in Germany. Dtsch Arztebl Int 2019; 116 (25) 435-444
    Google Scholar
  • 24 Turdumambetova GK, Osmanov A, Denning DW. The burden of serious fungal infections in Kyrgyzstan. J Fungi (Basel) 2019; 5 (03) 66
    CrossrefPubMedGoogle Scholar
  • 25 Pappas PG. Cryptococcal infections in non-HIV-infected patients. Trans Am Clin Climatol Assoc 2013; 124: 61-79
    PubMedGoogle Scholar
  • 26 Oldstone MB. Anatomy of viral persistence. PLoS Pathog 2009; 5 (07) e1000523
    CrossrefPubMedGoogle Scholar
  • 27 Sedmak DD, Guglielmo AM, Knight DA, Birmingham DJ, Huang EH, Waldman WJ. Cytomegalovirus inhibits major histocompatibility class II expression on infected endothelial cells. Am J Pathol 1994; 144 (04) 683-692
    PubMedGoogle Scholar
  • 28 Rotem-Yehudar R, Groettrup M, Soza A, Kloetzel PM, Ehrlich R. LMP-associated proteolytic activities and TAP-dependent peptide transport for class 1 MHC molecules are suppressed in cell lines transformed by the highly oncogenic adenovirus 12. J Exp Med 1996; 183 (02) 499-514
    CrossrefPubMedGoogle Scholar
  • 29 Copeland KF, Heeney JL. T helper cell activation and human retroviral pathogenesis. Microbiol Rev 1996; 60 (04) 722-742
    CrossrefPubMedGoogle Scholar
  • 30 Oldstone MB. How viruses escape from cytotoxic T lymphocytes: molecular parameters and players. Virology 1997; 234 (02) 179-185
    CrossrefPubMedGoogle Scholar
  • 31 Voeten JT, Bestebroer TM, Nieuwkoop NJ, Fouchier RA, Osterhaus AD, Rimmelzwaan GF. Antigenic drift in the influenza A virus (H3N2) nucleoprotein and escape from recognition by cytotoxic T lymphocytes. J Virol 2000; 74 (15) 6800-6807
    CrossrefPubMedGoogle Scholar
  • 32 Large MK, Kittlesen DJ, Hahn YS. Suppression of host immune response by the core protein of hepatitis C virus: possible implications for hepatitis C virus persistence. J Immunol 1999; 162 (02) 931-938
    CrossrefPubMedGoogle Scholar
  • 33 Means RE, Choi JK, Nakamura H, Chung YH, Ishido S, Jung JU. Immune evasion strategies of Kaposi's sarcoma-associated herpesvirus. Curr Top Microbiol Immunol 2002; 269: 187-201
    PubMedGoogle Scholar
  • 34 van Kooyk Y, Appelmelk B, Geijtenbeek TB. A fatal attraction: Mycobacterium tuberculosis and HIV-1 target DC-SIGN to escape immune surveillance. Trends Mol Med 2003; 9 (04) 153-159
    CrossrefPubMedGoogle Scholar
  • 35 Aliberti J. Host persistence: exploitation of anti-inflammatory pathways by Toxoplasma gondii. Nat Rev Immunol 2005; 5 (02) 162-170
    CrossrefPubMedGoogle Scholar
  • 36 Singh N, Tscharke DC. Herpes simplex virus latency is noisier the closer we look. J Virol 2020; 94 (04) e01701-e01719
    CrossrefPubMedGoogle Scholar
  • 37 Jiang G, Santos Rocha C, Hirao LA. et al. HIV exploits antiviral host innate GCN2–ATF4 signaling for establishing viral replication early in infection. MBio 2017; 8 (03) e015-e016
    CrossrefPubMedGoogle Scholar
  • 38 Qin Q, Penkert RR, Kalejta RF. Heterologous viral promoters incorporated into the human cytomegalovirus genome are silenced during experimental latency. J Virol 2013; 87 (17) 9886-9894
    CrossrefPubMedGoogle Scholar
  • 39 Raja P, Lee JS, Pan D, Pesola JM, Coen DM, Knipe DM. A herpesviral lytic protein regulates the structure of latent viral chromatin. MBio 2016; 7 (03) e00633-e16
    CrossrefPubMedGoogle Scholar
  • 40 Tricou V, Minh NN, Farrar J, Tran HT, Simmons CP. Kinetics of viremia and NS1 antigenemia are shaped by immune status and virus serotype in adults with dengue. PLoS Negl Trop Dis 2011; 5 (09) e1309
    CrossrefPubMedGoogle Scholar
  • 41 Rodriguez-Osorio M, Gómez-García V, Rojas J, Ramajo-Martin V. Humoral immune response and antigenemia in sheep experimentally infected with Schistosoma bovis. Cross-reactivity with Fasciola hepatica antigens. J Parasitol 1999; 85 (03) 585-587
    CrossrefPubMedGoogle Scholar
  • 42 Fehr T, Ochsenbein AF. Outcome of the antibody response: a question of antigen dose and distribution. Trends Immunol 2004; 25 (04) 165-166 , author reply 167–168
    CrossrefPubMedGoogle Scholar
  • 43 Kanduc D. Role of codon usage and tRNA changes in rat cytomegalovirus latency and (re)activation. J Basic Microbiol 2016; 56 (06) 617-626
    CrossrefPubMedGoogle Scholar
  • 44 Kanduc D. Rare human codons and HCMV translational regulation. J Mol Microbiol Biotechnol 2017; 27 (04) 213-216
    CrossrefPubMedGoogle Scholar
  • 45 Regner M. Cross-reactivity in T-cell antigen recognition. Immunol Cell Biol 2001; 79 (02) 91-100
    CrossrefPubMedGoogle Scholar
  • 46 Kamradt T, Volkmer-Engert R. Cross-reactivity of T lymphocytes in infection and autoimmunity. Mol Divers 2004; 8 (03) 271-280
    CrossrefPubMedGoogle Scholar
  • 47 Vojtek I, Buchy P, Doherty TM, Hoet B. Would immunization be the same without cross-reactivity?. Vaccine 2019; 37 (04) 539-549
    CrossrefPubMedGoogle Scholar
  • 48 Kanduc D. Peptide cross-reactivity: the original sin of vaccines. Front Biosci (Schol Ed) 2012; 4: 1393-1401
    CrossrefPubMedGoogle Scholar
  • 49 Nakamura Y, Gojobori T, Ikemura T. Codon usage tabulated from international DNA sequence databases: status for the year 2000. Nucleic Acids Res 2000; 28 (01) 292
    CrossrefPubMedGoogle Scholar
  • 50 UniProt Consortium. UniProt: the universal protein knowledgebase in 2021. Nucleic Acids Res 2021; 49 (D1): D480-D489
    CrossrefPubMedGoogle Scholar
  • 51 Wagner LM, Bayer A, Deluca NA. Requirement of the N-terminal activation domain of herpes simplex virus ICP4 for viral gene expression. J Virol 2013; 87 (02) 1010-1018
    CrossrefPubMedGoogle Scholar
  • 52 Casonato S, Cervantes Sánchez A, Haruki H. et al. WhiB5, a transcriptional regulator that contributes to Mycobacterium tuberculosis virulence and reactivation. Infect Immun 2012; 80 (09) 3132-3144
    CrossrefPubMedGoogle Scholar
  • 53 Weißbach T, Golzmann A, Bennink S, Pradel G, Julius Ngwa C. Transcript and protein expression analysis of proteases in the blood stages of Plasmodium falciparum . Exp Parasitol 2017; 180: 33-44
    CrossrefPubMedGoogle Scholar
  • 54 Li H, Child MA, Bogyo M. Proteases as regulators of pathogenesis: examples from the Apicomplexa. Biochim Biophys Acta 2012; 1824 (01) 177-185
    CrossrefPubMedGoogle Scholar
  • 55 Lee AS, Kranzusch PJ, Cate JH. eIF3 targets cell-proliferation messenger RNAs for translational activation or repression. Nature 2015; 522 (7554): 111-114
    CrossrefPubMedGoogle Scholar
  • 56 Roll P, Rudolf G, Pereira S. et al. SRPX2 mutations in disorders of language cortex and cognition. Hum Mol Genet 2006; 15 (07) 1195-1207
    CrossrefPubMedGoogle Scholar
  • 57 Henry I, Sharp PM. Predicting gene expression level from codon usage bias. Mol Biol Evol 2007; 24 (01) 10-12
    CrossrefPubMedGoogle Scholar
  • 58 Quax TE, Claassens NJ, Söll D, van der Oost J. Codon bias as a means to fine-tune gene expression. Mol Cell 2015; 59 (02) 149-161
    CrossrefPubMedGoogle Scholar
  • 59 Zhou Z, Dang Y, Zhou M. et al. Codon usage is an important determinant of gene expression levels largely through its effects on transcription. Proc Natl Acad Sci U S A 2016; 113 (41) E6117-E6125
    CrossrefPubMedGoogle Scholar
  • 60 Shin YC, Bischof GF, Lauer WA, Desrosiers RC. Importance of codon usage for the temporal regulation of viral gene expression. Proc Natl Acad Sci U S A 2015; 112 (45) 14030-14035
    CrossrefPubMedGoogle Scholar
  • 61 Kames J, Alexaki A, Holcomb DD. et al. TissueCoCoPUTs: novel human tissue-specific codon and codon-pair usage tables based on differential tissue gene expression. J Mol Biol 2020; 432 (11) 3369-3378
    CrossrefPubMedGoogle Scholar
  • 62 Liu Y, Yang Q, Zhao F. Synonymous but not silent: the codon usage code for gene expression and protein folding. Annu Rev Biochem 2021; 90 DOI: 10.1146/annurev-biochem-071320-112701.
    CrossrefPubMedGoogle Scholar
  • 63 Grantham R, Gautier C, Gouy M, Jacobzone M, Mercier R. Codon catalog usage is a genome strategy modulated for gene expressivity. Nucleic Acids Res 1981; 9 (01) r43-r74
    CrossrefPubMedGoogle Scholar
  • 64 Ikemura T. Correlation between the abundance of yeast transfer RNAs and the occurrence of the respective codons in protein genes. Differences in synonymous codon choice patterns of yeast and Escherichia coli with reference to the abundance of isoaccepting transfer RNAs. J Mol Biol 1982; 158 (04) 573-597
    CrossrefPubMedGoogle Scholar
  • 65 Ikemura T. Codon usage and tRNA content in unicellular and multicellular organisms. Mol Biol Evol 1985; 2 (01) 13-34
    PubMedGoogle Scholar
  • 66 Kanaya S, Yamada Y, Kudo Y, Ikemura T. Studies of codon usage and tRNA genes of 18 unicellular organisms and quantification of Bacillus subtilis tRNAs: gene expression level and species-specific diversity of codon usage based on multivariate analysis. Gene 1999; 238 (01) 143-155
    CrossrefPubMedGoogle Scholar
  • 67 Yang J, Smith DK, Ni H. et al. SOX4-mediated repression of specific tRNAs inhibits proliferation of human glioblastoma cells. Proc Natl Acad Sci U S A 2020; 117 (11) 5782-5790
    CrossrefPubMedGoogle Scholar
  • 68 Victor MP, Acharya D, Chakraborty S, Ghosh TC. The combined influence of codon composition and tRNA copy number regulates translational efficiency by influencing synonymous nucleotide substitution. Gene 2020; 745: 144640
    CrossrefPubMedGoogle Scholar
  • 69 Kanduc D. Changes of tRNA population during compensatory cell proliferation: differential expression of methionine-tRNA species. Arch Biochem Biophys 1997; 342 (01) 1-5
    CrossrefPubMedGoogle Scholar
  • 70 Bayliss J, Karasoulos T, McLean CA. Immunosuppression increases JC polyomavirus large T antigen DNA load in the brains of patients without progressive multifocal leukoencephalopathy. J Infect Dis 2013; 207 (01) 133-136
    CrossrefPubMedGoogle Scholar
  • 71 Maglennon GA, McIntosh PB, Doorbar J. Immunosuppression facilitates the reactivation of latent papillomavirus infections. J Virol 2014; 88 (01) 710-716
    CrossrefPubMedGoogle Scholar
  • 72 García-Barchino MJ, Sarasquete ME, Panizo C. et al. Richter transformation driven by Epstein-Barr virus reactivation during therapy-related immunosuppression in chronic lymphocytic leukaemia. J Pathol 2018; 245 (01) 61-73
    CrossrefPubMedGoogle Scholar
  • 73 Schoenfisch AL, Dollard SC, Amin M. et al. Cytomegalovirus (CMV) shedding is highly correlated with markers of immunosuppression in CMV-seropositive women. J Med Microbiol 2011; 60 (Pt 6): 768-774
    CrossrefPubMedGoogle Scholar
  • 74 Koshy E, Mengting L, Kumar H, Jianbo W. Epidemiology, treatment and prevention of herpes zoster: a comprehensive review. Indian J Dermatol Venereol Leprol 2018; 84 (03) 251-262
    CrossrefPubMedGoogle Scholar
  • 75 Wu Y, Huang H, Luo Y. Management of hepatitis B virus in allogeneic hematopoietic stem cell transplantation. Front Immunol 2021; 11: 610500
    CrossrefPubMedGoogle Scholar
  • 76 Czech MM, Nayak AK, Subramanian K. et al. Reactivation of Chagas disease in a patient with an autoimmune rheumatic disease: case report and review of the literature. Open Forum Infect Dis 2021; 8 (02) a642
    CrossrefPubMedGoogle Scholar
  • 77 Pegoraro F, Favre C. Post-transplantation lymphoproliferative disorder after haematopoietic stem cell transplantation. Ann Hematol 2021; 100 (04) 865-878
    CrossrefPubMedGoogle Scholar
  • 78 Rosner BA, Cristofalo VJ. Hydrocortisone: a specific modulator of in vitro cell proliferation and aging. Mech Ageing Dev 1979; 9 (5-6): 485-496
    CrossrefPubMedGoogle Scholar
  • 79 Phillips PD, Cristofalo VJ. Classification system based on the functional equivalency of mitogens that regulate WI-38 cell proliferation. Exp Cell Res 1988; 175 (02) 396-403
    CrossrefPubMedGoogle Scholar
  • 80 Neuberger TJ, Kalimi O, Regelson W, Kalimi M, De Vries GH. Glucocorticoids enhance the potency of Schwann cell mitogens. J Neurosci Res 1994; 38 (03) 300-313
    CrossrefPubMedGoogle Scholar
  • 81 Cai J, Zheng T, Lotz M, Zhang Y, Masood R, Gill P. Glucocorticoids induce Kaposi's sarcoma cell proliferation through the regulation of transforming growth factor-beta. Blood 1997; 89 (05) 1491-1500
    CrossrefPubMedGoogle Scholar
  • 82 Kawamura A, Tamaki N, Kokunai T. Effect of dexamethasone on cell proliferation of neuroepithelial tumor cell lines. Neurol Med Chir (Tokyo) 1998; 38 (10) 633-638 , discussion 638–640
    CrossrefPubMedGoogle Scholar
  • 83 Bourcier T, Forgez P, Borderie V, Scheer S, Rostène W, Laroche L. Regulation of human corneal epithelial cell proliferation and apoptosis by dexamethasone. Invest Ophthalmol Vis Sci 2000; 41 (13) 4133-4141
    PubMedGoogle Scholar
  • 84 Atmani H, Chappard D, Basle MF. Proliferation and differentiation of osteoblasts and adipocytes in rat bone marrow stromal cell cultures: effects of dexamethasone and calcitriol. J Cell Biochem 2003; 89 (02) 364-372
    CrossrefPubMedGoogle Scholar
  • 85 Rafacho A, Cestari TM, Taboga SR, Boschero AC, Bosqueiro JR. High doses of dexamethasone induce increased beta-cell proliferation in pancreatic rat islets. Am J Physiol Endocrinol Metab 2009; 296 (04) E681-E689
    CrossrefPubMedGoogle Scholar
  • 86 Pickholtz E, Admon D, Izhar U, Berkman N, Levi-Schaffer F. Dexamethasone and salbutamol stimulate human lung fibroblast proliferation. World Allergy Organ J 2011; 4 (12) 249-256
    PubMedGoogle Scholar
  • 87 Zheng Y, Izumi K, Li Y, Ishiguro H, Miyamoto H. Contrary regulation of bladder cancer cell proliferation and invasion by dexamethasone-mediated glucocorticoid receptor signals. Mol Cancer Ther 2012; 11 (12) 2621-2632
    CrossrefPubMedGoogle Scholar
  • 88 Gündisch S, Boeckeler E, Behrends U, Amtmann E, Ehrhardt H, Jeremias I. Glucocorticoids augment survival and proliferation of tumor cells. Anticancer Res 2012; 32 (10) 4251-4261
    Google Scholar
  • 89 Ninomiya E, Hattori T, Toyoda M, Umezawa A, Hamazaki T, Shintaku H. Glucocorticoids promote neural progenitor cell proliferation derived from human induced pluripotent stem cells. Springerplus 2014; 3: 527
    CrossrefPubMedGoogle Scholar
  • 90 Larson AA, Syverud BC, Florida SE, Rodriguez BL, Pantelic MN, Larkin LM. Effects of dexamethasone dose and timing on tissue-engineered skeletal muscle units. Cells Tissues Organs 2018; 205 (04) 197-207
    CrossrefPubMedGoogle Scholar
  • 91 Grisé KN, Bautista NX, Jacques K, Coles BLK, van der Kooy D. Glucocorticoid agonists enhance retinal stem cell self-renewal and proliferation. Stem Cell Res Ther 2021; 12 (01) 83
    CrossrefPubMedGoogle Scholar
  • 92 Natale C, Giannini T, Lucchese A, Kanduc D. Computer-assisted analysis of molecular mimicry between human papillomavirus 16 E7 oncoprotein and human protein sequences. Immunol Cell Biol 2000; 78 (06) 580-585
    CrossrefPubMedGoogle Scholar
  • 93 Kanduc D, Stufano A, Lucchese G, Kusalik A. Massive peptide sharing between viral and human proteomes. Peptides 2008; 29 (10) 1755-1766
    CrossrefPubMedGoogle Scholar
  • 94 Trost B, Lucchese G, Stufano A, Bickis M, Kusalik A, Kanduc D. No human protein is exempt from bacterial motifs, not even one. Self Nonself 2010; 1 (04) 328-334
    CrossrefPubMedGoogle Scholar
  • 95 Kanduc D, Shoenfeld Y. On the molecular determinants of the SARS-CoV-2 attack. Clin Immunol 2020; 215: 108426
    CrossrefPubMedGoogle Scholar
  • 96 Kanduc D. Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2): codon usage and replicative fitness. Glob Med Genet 2020; 7 (03) 92-94
    Article in Thieme ConnectPubMedGoogle Scholar