The Roles of Genomics and Proteomics in Human Parasitology: Closing the Knowledge Gap

Document Type : Systematic Review

Authors
A. J. Funmilayo 1
O. Agboola 2
S. Agboola 3
B. Oluboyo 1
A. Egbebi 4
A. Sijuade 5
Z. Ayinla 6
A. Adegbuyi 7
C. Agu 1
V. Aikhomu 1
O. Ogunfolakan 1
J. Onyejiaka 1
T. Oludare 8
A. Agboola 9
1 Medical Laboratory Science Department, College of Medicine and Health Sciences, Afe Babalola University, Ado-Ekiti, Nigeria.
2 Institute for Drug Research and Development, Bogoro Research Centre, Afe Babalola University, Ado-Ekiti, Nigeria.
3 Department of Pharmacology and Toxicology, College of Pharmacy, Afe Babalola University, Ado-Ekiti, Nigeria.
4 Medical Laboratory Science Department, College of Medicine and Health Sciences, Afe Babalola University, Ado-Ekiti, Nigeria, Ado-Ekiti.
5 Department of Pharmacology and Therapeutic, College of Medicine, Ekiti State University, Ekiti State, Nigeria.
6 Department of Biochemistry and Molecular Biology, Obafemi Awolowo University, Ile-Ife, Nigeria.
7 Department of Pharmacology and Toxicology, Faculty of Pharmacy, Federal University Oye-Ekiti, Nigeria.
8 Department of Community Medicine, College of Medicine and Health Sciences, Afe Babalola University, Ado-Ekiti.
9 Integrated Medical Sciences Department, College of Medicine and Health Sciences, Afe Babalola University, Ado-Ekiti, Nigeria.
10.52547/iem.10.2.157
Abstract
Background: The complicated host-parasite relationships have hindered the effective diagnosis, treatment, and control of human parasitic diseases. This review examines how genomics and proteomics are unraveling these complex interactions and transforming human parasitology.

Materials & Methods: Related studies were chosen according to the PRISMA flow diagram. An extensive literature search between January 1, 2022 and March 31, 2023 was conducted in PubMed, Scopus, and Web of Science databases, and a systematic screening process was undertaken, resulting in the identification and inclusion of 72 studies in this narrative review on the applications of genomics and proteomics in human parasitology research. Articles that were duplicates, irrelevant based on title/abstract screening, unavailable, or irrelevant based on full text review were excluded from the study.

Findings: A total of 453 records were retrieved, of which 72 articles remained after title, abstract, and full text screening. Genomics and proteomics have elucidated parasite biology, enabled precision diagnostics, and guided drug development by providing molecular insights into host-parasite interactions. However, challenges remain, including computational complexity and translation of findings to human infections.

Conclusion: The integration of genomics and proteomics has allowed an unprecedented understanding of human parasites and holds great promise for improving diagnosis, treatment, and control.

Keywords

Subjects

References
1. Runghen R, Poulin R, Monlleó-Borrull C, Llopis-Belenguer C. Network analysis: Ten years shining light on host parasite interactions. Trends Parasitol. 2021;37(5):445-55.
2. Bock C, Datlinger P, Chardon F, Coelho MA, Dong MB, Lawson KA, et al. High-content CRISPR screening. Nat Rev Methods Primers. 2022;2(1):8.
3. Nisar N, Mir SA, Kareem O, Pottoo FH. Proteomics approaches in the identification of cancer biomarkers and drug discovery. In: Proteomics. Academic press; 2023, pp. 77-120.
4. Elmore LW, Greer SF, Daniels EC, Saxe CC, Melner MH, Krawiec GM, et al. Blueprint for cancer research: Critical gaps and opportunities. CA Cancer J Clin. 2021;71(2):107-39.
5. Dubey AK, Kumar Gupta V, Kujawska M, Orive G, Kim NY, Li CZ, et al. Exploring nano-enabled CRISPR-Cas-powered strategies for efficient diagnostics and treatment of infectious diseases. J Nanostruct Chem. 2022;12(5):833-64.
6. Amselem J, Cuomo CA, van Kan JA, Viaud M, Benito EP, Couloux A, et al. Genomic analysis of the necrotrophic fungal pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLoS Genet. 2011;7(8):e1002230.
7. Campaner R. Explaining disease: Philosophical reflections on medical research and clinical practice. Springer Nature; 2022.
8. Zhang YD, Zhang YY, Chen JY, Huang JQ, Zhang J, Liu L, et al. Genome sequence data of MAT1- 1 and MAT1-2 idiomorphs from Verticillium dahliae. Phytopathology. 2021;111(9):1686-91.
9. Emerson D, Agulto L, Liu H, Liu L. Identifying and characterizing bacteria in an era of genomics and proteomics. Bioscience. 2008;58(10):925-36.
10. Sundar S, Singh B. Understanding Leishmania parasites through proteomics and implications for the clinic. Expert Rev Proteomics. 2018;15(5):371-90.
11. Volkman SK, Neafsey DE, Schaffner SF, Park DJ, Wirth DF. Harnessing genomics and genome biology to understand malaria biology. Nat Rev Genet. 2012;13(5):315-28.
12. Lindner SE, Swearingen KE, Shears MJ, Walker MP, Vrana EN, Hart KJ, et al. Transcriptomics and proteomics reveal two waves of translational repression during the maturation of malaria parasite sporozoites. Nat Commun. 2019;10(1):4964.
13. Reece SE, Prior KF, Mideo N. The life and times of parasites: Rhythms in strategies for within- host survival and between-host transmission. J Biol Rhythms. 2017;32(6):516-33.
14. Alfiky A, Weisskopf L. Deciphering Trichoderma plant pathogen interactions for better development of biocontrol applications. J Fungi. 2021;7(1):61.
15. Rimbaud L, Papaïx J, Rey JF, Moury B, Barrett LG, Thrall PH. Durable resistance or efficient disease control? Adult plant resistance (APR) at the heart of the dilemma. Peer Community J. 2023;3:1-39.
16. Schröttner P, Hu F, Li X, Bao X, Qiao G, Wang L, et al. Characterization of rare and recently first described human pathogenic bacteria. Front Cell Infect Microbiol. 2023;13:5-7.
17. Nesse RM. Evolutionary psychiatry: Foundations, progress, and challenges. World Psychiatry. 2023;22(2):177-202.
18. Amandine C, Ebert D, Stukenbrock E, de la Vega RC, Tiffin P, Croll D, et al. Unraveling coevolutionary dynamics using ecological genomics. Trends Genet. 2022;38(10):1003-12.
19. Zerr I. Prion 2022 Conference abstracts: Pushing the boundaries. Prion. 2022;16(1):95-253.
20. Arya PK, Barik K, Singh AK, Kumar A. Databases and web resources for neglected tropical disease research. J Appl Pharm Sci. 2023;13(8):043-54.
21. Montarry J, Mimee B, Danchin EG, Koutsovoulos GD, Ste-Croix DT, Grenier E. Recent advances in population genomics of plant-parasitic nematodes. Phytopathology. 2021;111(1):40-8.
22. Waiho K, Afiqah-Aleng N, Iryani MT, Fazhan H. Protein-protein interaction network: An emerging tool for understanding fish disease in aquaculture. Rev Aquaculture. 2021;13(1):156-77.

23. Osborne A, Manko E, Takeda M, Kaneko A, Kagaya W, Chan C, et al. Characterizing the genomic variation and population dynamics of Plasmodium falciparum malaria parasites in and around Lake Victoria, Kenya. Sci Rep. 2021;11(1):19809.
24. Njoku K, Chiasserini D, Whetton AD, Crosbie EJ. Proteomic biomarkers for the detection of endometrial cancer. Cancers. 2019;11(10):1572.
25. Rodrigues-Luiz GF, Cardoso MS, Valdivia HO, Ayala EV, Gontijo CM, Rodrigues TD, et al. TipMT: Identification of PCR-based taxon-specific markers. BMC Bioinform. 2017;18:1-8.
26. Ding Z, Wang N, Ji N, Chen ZS. Proteomics technologies for cancer liquid biopsies. Mol Cancer. 2022;21(1):53.
27. Meissner F, Geddes-McAlister J, Mann M, Bantscheff M. The emerging role of mass spectrometry- based proteomics in drug discovery. Nat Rev Drug Discov. 2022;21(9):637-54.
28. Offit K. Personalized medicine: New genomics, old lessons. Hum Genet. 2011;130:3-14.
29. Velez G, Tang PH, Cabral T, Cho GY, Machlab DA, Tsang SH, et al. Personalized proteomics for precision health: Identifying biomarkers of vitreoretinal disease. Transl Vis Sci Technol. 2018;7(5):12.
30. Mannino DM. COPD: epidemiology, prevalence, morbidity, and mortality, and disease heterogeneity. Chest. 2002;121(5):121S-6S.
31. Lee M. Deep learning techniques with genomic data in cancer prognosis: A comprehensive review of the 20212023 literature. Biology. 2023;12(7):893.
32. Davy SK, Allemand D, Weis VM. Cell biology of cnidarian-dinoflagellate symbiosis. Microbiol Mol Biol Rev. 2012;76(2):229-61.
33. Sapountzis P. Microbial symbioses: From vertebrates to invertebrates and back again (doctoral dissertation). Clermont Auvergne University, Doctoral School of Life Sciences, Health, Agronomy, Environment (ED SVSAE, ED 65); 2022.
34. Edwards D, Kenrick P. The early evolution of land plants, from fossils to genomics: A commentary on Lang (1937) ‘On the plant-remains from the Downtonian of England and Wales'. Phil Trans R Soc B. 2015;370(1666):20140343.
35. Kaur R, Shropshire JD, Cross KL, Leigh B, Mansueto AJ, Stewart V, et al. Living in the endosymbiotic world of Wolbachia: A centennial review. Cell Host Microbe. 2021;29(6):879-93.
36. Van den Broeck WM. Drug targets, target identification, validation, and screening. In: The practice of medicinal chemistry. Academic press; 2015, pp. 45-70.
37. Santos BF, Klopfstein S, Whitfield JB, Sharanowski BJ. Many evolutionary roads led to virus domestication in ichneumonoid parasitoid wasps. Curr Opin Insect Sci. 2022;50:100861.
38. Marwaha S, Knowles JW, Ashley EA. A guide for the diagnosis of rare and undiagnosed disease: Beyond the exome. Genome Med. 2022;14(1):1-22.
39. Razin S, Yogev D, Naot Y. Molecular biology and pathogenicity of mycoplasmas. Microbiol Mol Biol Rev. 1998;62(4):1094-156.
40. Chen L. Deep learning models for modeling cellular transcription systems (doctoral dissertation). University of Pittsburgh; 2017.
41. Ezkurdia I, Juan D, Rodriguez JM, Frankish A, Diekhans M, Harrow J, et al. Multiple evidence strands suggest that there may be as few as 19 000 human protein-coding genes. Hum Mol Genet. 2014;23(22):5866-78.
42. Kwok AJ, Mentzer A, Knight JC. Host genetics and infectious disease: New tools, insights, and translational opportunities. Nat Rev Genet. 2021;22(3):137-53.
43. Trapp J, McAfee A, Foster LJ. Genomics, transcriptomics, and proteomics: Enabling insights into social evolution and disease challenges for managed and wild bees. Mol Ecol. 2017;26(3):718-39.
44. Blay V, Tolani B, Ho SP, Arkin MR. High-throughput screening: Today’s biochemical and cell- based approaches. Drug Discov Today. 2020;25(10):1807-21.
45. John A, Qin B, Kalari KR, Wang L, Yu J. Patient-specific multi-omics models and the application in personalized combination therapy. Future Oncol. 2020;16(23):1737-50.

46. Trujillo AE. Comparative bioinformatic analysis of primate interactions with malaria and related parasites (doctoral dissertation). New York University; 2023.
47. Powell R. The future of human evolution. Br J Philos Sci. 2012;63(1):145-75.
48. Easton A, Gao S, Lawton SP, Bennuru S, Khan A, Dahlstrom E, et al. Molecular evidence of hybridization between pig and human Ascaris indicates an interbred species complex infecting humans. Elife. 2020;9:e61562.
49. Rabaan AA, Bakhrebah MA, Mohapatra RK, Farahat RA, Dhawan M, Alwarthan S, et al. Omics approaches in drug development against Leishmaniasis: Current scenario and future prospects. Pathogens. 2022;12(1):39.
50. Barylyuk K, Koreny L, Ke H, Butterworth S, Crook OM, Lassadi I, et al. A comprehensive subcellular atlas of the Toxoplasma proteome via hyperLOPIT provides spatial context for protein functions. Cell Host Microbe. 2020;28(5):752-66.
51. Serajian S, Ahmadpour E, Oliveira SM, Pereira MD, Heidarzadeh S. CRISPR-Cas technology: Emerging applications in clinical microbiology and infectious diseases. Pharmaceuticals. 2021;14(11):1171.
52. Hastings JF, O'Donnell Y, Fey D, Croucher DR. Applications of personalized signaling network models in precision oncology. Pharmacol Ther. 2020;212:107555.
53. Sotillo J, Pearson MS, Loukas A. Trematode genomics and proteomics. In: Toledo R, Fried B (eds). Digenetic Trematodes: Advances in experimental medicine and biology. Springer, Cham; 2019, pp. 411-436.
54. Ittiprasert W, Myers J, Odoemelam EC, Raghavan N, Lewis F, Bridger JM, et al. Advances in the genomics and proteomics of the freshwater intermediate snail host of Schistosoma mansoni, Biomphalaria glabrata. In: Toledo R, Fried B (eds). Biomphalaria snails and larval trematodes. New York: Springer; 2011, pp. 191-213.
55. Muñoz JF, Gade L, Chow NA, Loparev VN, Juieng P, Berkow EL, et al. Genomic insights into multidrug-resistance, mating, and virulence in Candida auris and related emerging species. Nat Commun. 2018;9(1):5346.
56. Prokop JW, Jdanov V, Savage L, Morris M, Lamb N, VanSickle E, et al. Computational and experimental analysis of genetic variants. Comp Physiol. 2022;12(2):3303-36.
57. Aggarwal S, Banerjee SK, Talukdar NC, Yadav AK. Post-translational modification crosstalk and hotspots in sirtuin interactors implicated in cardiovascular diseases. Front Genet. 2020;11:356.
58. Wang L, Maron BA, Loscalzo J. Multiomics network medicine approaches to precision medicine and therapeutics in cardiovascular diseases. Arterioscler Thromb Vasc Biol. 2023;43(4):493-503.
59. Hauser AS, Attwood MM, Rask-Andersen M, Schiöth HB, Gloriam DE. Trends in GPCR drug discovery: New agents, targets, and indications. Nat Rev Drug Discov. 2017;16(12):829-42.
60. Loiseau C, Cooper MM, Doolan DL. Deciphering host immunity to malaria using systems immunology. Immunol Rev. 2020;293(1):115-43.
61. Liu D, Hoynes-O’Connor A, Zhang F. Bridging the gap between systems biology and synthetic biology. Front Microbiol. 2013;4:211.
62. Alaridah N, Hallbäck ET, Tångrot J, Winqvist N, Sturegård E, Florén-Johansson K, et al. Transmission dynamics study of tuberculosis isolates with whole genome sequencing in southern Sweden. Sci Rep. 2019;9(1):4931.
63. Proietti C, Krause L, Trieu A, Dodoo D, Gyan B, Koram KA, et al. Immune signature against Plasmodium falciparum antigens predicts clinical immunity in distinct malaria endemic communities. Mol Cell Proteomics. 2020;19(1):101-13.
64. Naung MT, Martin E, Munro J, Mehra S, Guy AJ, Laman M, et al. Global diversity and balancing selection of 23 leading Plasmodium falciparum candidate vaccine antigens. PLoS Comput Biol. 2022;18(2):e1009801.

65. Varela ML, Koffi D, White M, Niang M, Mbengue B, Diene Sarr F, et al. Practical example of multiple antibody screening for evaluation of malaria control strategies. Malar J. 2020;19(1):1-2.
66. Ruybal-Pesántez S, McCann K, Vibin J, Siegel S, Auburn S, Barry AE. Molecular markers for malaria genetic epidemiology: Progress and pitfalls. Trends Parasitol. 2023;40(2):147-63.
67. Costain AH, Phythian-Adams AT, Colombo SA, Marley AK, Owusu C, Cook PC, et al. Dynamics of host immune response development during Schistosoma mansoni infection. Front Immunol. 2022;13:906338.
68. Kent RS, Briggs EM, Colon BL, Alvarez C, Silva Pereira S, De Niz M. Paving the way: Contributions of big data to apicomplexan and kinetoplastid research. Front Cell Infect Microbiol. 2022;12:900878.
69. Wörheide MA, Krumsiek J, Kastenmüller G, Arnold M. Multi-omics integration in biomedical research: A metabolomics-centric review. Anal Chim Acta. 2021;1141:144-62.
70. Misra BB, Langefeld C, Olivier M, Cox LA. Integrated omics: Tools, advances, and future approaches. J Mol Endocrinol. 2019;62(1):R21-45.
71. Karczewski KJ, Snyder MP. Integrative omics for health and disease. Nat Rev Genet. 2018;19(5):299-310.
72. Antonelli L, Guarracino MR, Maddalena L, Sangiovanni M. Integrating imaging and omics data: A review. Biomed Signal Process Control. 2019;52:264-80.
73. Nisa RU, Tantray AY, Shah AA. Shift from morphological to recent advanced molecular approaches for the identification of nematodes. Genomics. 2022;114(2):110295.
74. Gabaldón T. Recent trends in molecular diagnostics of yeast infections: From PCR to NGS. FEMS Microbiol Rev. 2019;43(5):517-47.
75. Thaenkham U, Chaisiri K, Hui En Chan A. Challenges of species identification for parasitic helminths. In: Molecular systematics of parasitic helminths. Singapore: Springer Nature; 2022, pp. 131-159.
76. Jiang L, Feng J, Chen X, Beshir KB, Chen T, Wang X, editors. Infection and control of vector- borne diseases. Frontiers Media SA; 2022.
77. Alexandratos A, Clos J, Samiotaki M, Efstathiou A, Panayotou G, Soteriadou K, et al. The loss of virulence of histone H 1 overexpressing Leishmania donovani parasites is directly associated with a reduction of HSP 83 rate of translation. Mol Microbiol. 2013;88(5):1015-31.
78. Coutinho JV, Rosa-Fernandes L, Mule SN, de Oliveira GS, Manchola NC, Santiago VF, et al. The thermal proteome stability profile of Trypanosoma cruzi in epimastigote and trypomastigote life stages. J Proteomics. 2021;248:104339.
79. Tonkin-Hill GQ, Trianty L, Noviyanti R, Nguyen HH, Sebayang BF, Lampah DA, et al. The Plasmodium falciparum transcriptome in severe malaria reveals altered expression of genes involved in important processes including surface antigen encoding var genes. PLoS Biol. 2018;16(3):e2004328.
80. Rashidi S, Sánchez-Montejo J, Mansouri R, Ali-Hassanzadeh M, Savardashtaki A, Bahreini MS, et al. Mining the proteome of Toxoplasma parasites seeking vaccine and diagnostic candidates. Animals. 2022;12(9):1098.
Infection Epidemiology and Microbiology
Volume 10, Issue 2
June 2024
Pages 157-174