Expression of Heat Shock Protein 70 (HSP70) and Astacin Genes of Strongyloides stercoralis as well as HSP70 and HSP17.1 Genes of S. ratti in Adult and Larval Stages of S. stercoralis
-
Maryam Alipour
,
Leila Masoori
,
Mohammad Davoodzadeh Gholami
,
Majid Khoshmirsafa
,
Elham Razmjou
,
Nahid Jalallou
,
Farzane Jafarian
,
Reza Falak
,
Ahmad Reza Meamar
Abstract
Background: Uncovering the roles and characteristics of pathogenesis-related molecules can help us develop novel management methods in parasitology. In this study, we studied the expression levels of Strongyloides stercoralis heat shock protein70 (HSP70) (Sst-hsp-70) and astacin (Sst-ast) as pathogenesis-related genes as well as the expression of S. ratti HSP70 and HSP17.1 (Sra-hsp-70, Sra-hsp-17.1) in the larvae and adult stages of S. stercoralis.
Methods: A hyperinfection isolate of S. stercoralis from Gilan Province, northern Iran was cultivated on nutrient agar. After a couple of days, parasites in different stages of life were collected, and total RNA was extracted. The expression levels of astacin and HSP genes were compared by real-time PCR.
Results: Statistically higher expression levels of Sst-ast, Sst-hsp-70, and Sra-hsp-70 genes in L3 larvae than in adults were observed. However, the expression level of Sra-hsp-17.1 was non-significantly lower in the larval stage than in adult worms.
Conclusion: Higher expression levels of Sst-ast, Sst-hsp-70, and Sra-hsp-70 genes in the larval stages of S. stercoralis suggest the potential role of these enzymes in parasite cutaneous invasion and pathogenesis. However, higher expression of Sra-hsp-17.1 in adult forms is probably involved in resistance and survival mechanisms. The similarity in gene expression between S. stercoralis and S. ratti can provide helpful hints to better understand strongyloidiasis from various perspectives, including pathogenesis, proper diagnosis, and targeted treatment.
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2. Keiser PB, Nutman TB. Strongyloides stercoralis in the immunocompromised population. Clin Microbiol Rev. 2004;17(1):208-217.
3. Al-Zihiry KJK, Abdulhaleem N, Atshan SS, et al. Quantification of C-type lectin gene expression during hyperinfection in strongyloidiasis. Ann Trop Med Public Health. 2020;23 (4):S498.
4. Ericsson CD, Steffen R, Siddiqui AA, et al. Diagnosis of Strongyloides stercoralis infection. Clin Infect Dis. 2001;33(7):1040-1047.
5. Khieu V, Srey S, Schär F, et al. Strongyloides stercoralis is a cause of abdominal pain, diarrhea and urticaria in rural Cambodia. BMC Res Notes. 2013;6:200.
6. Forrer A, Khieu V, Schär F, et al. Strongyloides stercoralis is associated with significant morbidity in rural Cambodia, including stunting in children. PLoS Negl Trop Dis. 2017;11(10):e0005685.
7. Meamar AR, Rezaian M, Mohraz M, et al. Strongyloides stercoralis hyper-infection syndrome in HIV+/AIDS patients in Iran. Parasitol Res. 2007;101(3):663-665.
8. Hunt VL, Tsai IJ, Coghlan A, et al. The genomic basis of parasitism in the Strongyloides clade of nematodes. Nat Genet. 2016;48(3):299-307.
9. Lindquist S, Craig EA. The heat-shock proteins. Annu Rev Genet. 1988;22:631-677.
10. Zhang H, Zhou Q, Yang Y, et al. Characterization of heat shock protein 70 gene from Haemonchus contortus and its expression and promoter analysis in Caenorhabditis elegans. Parasitology. 2013;140(6):683-694.
11. Tsuji N, Ohta M, Fujisaki K. Expression of a 70-kDa heat-shock-related protein during transformation from free-living infective larvae to the parasitic stage in Strongyloides venezuelensis. Parasitol Res. 1997;83(1):99-102.
12. Nikolaidis N, Nei M. Concerted and nonconcerted evolution of the Hsp70 gene superfamily in two sibling species of nematodes. Mol Biol Evol. 2004;21(3):498-505.
13. Schmitz KA, Hale TJ, Rajan T, et al. Localization of paramyosin, myosin, and a heat shock protein 70 in larval and adult Brugia malayi. J Parasitol. 1996;82(2):367-370.
14. Ditgen D, Anandarajah EM, Reinhardt A, et al. Comparative characterization of two galectins excreted-secreted from intestine-dwelling parasitic versus free-living females of the soil-transmitted nematode Strongyloides. Mol Biochem Parasitol. 2018;225:73-83.
15. Hunt VL, Tsai IJ, Selkirk ME, et al. The genome of Strongyloides spp. gives insights into protein families with a putative role in nematode parasitism. Parasitology. 2017;144(3):343-358.
16. Viney M, Kikuchi T. Strongyloides ratti and S. venezuelensis–rodent models of Strongyloides infection. Parasitology. 2017;144(3):285-294.
17. Yuan W, Lok JB, Stoltzfus JD, et al. Toward Understanding the functional role of Ss-riok-1, a RIO protein kinase-encoding gene of Strongyloides stercoralis. PLoS Negl Trop Dis. 2014;8(8):e3062.
18. Yuan W, Liu Y, Lok JB, et al. Exploring features and function of Ss-riok-3, an enigmatic kinase gene from Strongyloides stercoralis. Parasit Vectors. 2014;7:561.
19. Baskaran P, Jaleta TG, Streit A, et al. Duplications and positive selection drive the evolution of parasitism-associated gene families in the nematode Strongyloides papillosus. Genome Biol Evol. 2017;9(3):790-801.
20. Newton-Howes J, Heath DD, Shoemaker CB, et al. Characterisation and expression of an Hsp70 gene from Parastrongyloides trichosuri. Int J Parasitol. 2006;36(4):467-474.
21. Gallego SG, Loukas A, Slade RW, et al. Identification of an astacin-like metallo-proteinase transcript from the infective larvae of Strongyloides stercoralis. Parasitol Int. 2005;54(2):123-133.
22. Jing Y, Toubarro D, Hao Y, et al. Cloning, characterisation and heterologous expression of an astacin metalloprotease, Sc-AST, from the entomoparasitic nematode Steinernema carpocapsae. Mol Biochem Parasitol. 2010;174(2):101-108.
23. Möhrlen F, Hutter H, Zwilling R. The astacin protein family in Caenorhabditis elegans. Eur J Biochem. 2003;270(24):4909-4920.
24. Hunt VL, Hino A, Yoshida A, et al. Comparative transcriptomics gives insights into the evolution of parasitism in Strongyloides nematodes at the genus, subclade and species level. Sci Rep. 2018;8(1):5192.
25. Soblik H, Younis AE, Mitreva M, et al. Life cycle stage-resolved proteomic analysis of the excretome/secretome from Strongyloides ratti—identification of stage-specific proteases. Mol Cell Proteomics. 2011;10(12):M111.010157.
26. Masoori L, Meamar AR, Bandehpour M, et al. Fatty acid and retinol-binding protein: A novel antigen for immunodiagnosis of human strongyloidiasis. PLoS One. 2019;14(7):e0218895.
27. Masoori L, Falak R, Mokhtarian K, et al. Production of recombinant 14-3-3 protein and determination of its immunogenicity for application in serodiagnosis of strongyloidiasis. Trans R Soc Trop Med Hyg. 2019;113(6):326-331.
28. Muller R, Wakelin D. Worms and human disease, 2nd ed: CABI; 2002.
29. Tazir Y, Steisslinger V, Soblik H, et al. Molecular and functional characterisation of the heat shock protein 10 of Strongyloides ratti. Mol Biochem Parasitol. 2009;168(2):149-157.
30. Gholami MD, Falak R, Heidari S, et al. A truncated snail1 transcription factor alters the expression of essential EMT markers and s2uppresses tumor cell migration in a human lung cancer cell line. Recent Pat Anticancer Drug Discov. 2019;14(2):158-169.
31. Zhan B, Hotez PJ, Wang Y, et al. A developmentally regulated metalloprotease secreted by host-stimulated Ancylostoma caninum third-stage infective larvae is a member of the astacin family of proteases. Mol Biochem Parasitol. 2002;120(2):291-296.
32. Hawdon JM, Hotez PJ. Hookworm: developmental biology of the infectious process. Curr Opin Genet Dev. 1996;6(5):618-623.
33. Rogers WP, Sommerville RI. Physiology of exsheathment in nematodes and its relation to parasitism. Nature. 1957;179(4560):619-621.
34. Maresca B, Carratu L. The biology of the heat shock response in parasites. Parasitol Today. 1992;8(8):260-266.
35. Chen HY, Cheng YS, Shih HH. Expression patterns and structural modelling of Hsp70 and Hsp90 in a fish-borne zoonotic nematode Anisakis pegreffii. Vet Parasitol. 2015;212(3-4):281-291.
36. Younis AE, Geisinger F, Ajonina‐Ekoti I, et al. Stage‐specific excretory–secretory small heat shock proteins from the parasitic nematode Strongyloides ratti–putative links to host’s intestinal mucosal defense system. FEBS J. 2011;278(18):3319-3336.
2. Keiser PB, Nutman TB. Strongyloides stercoralis in the immunocompromised population. Clin Microbiol Rev. 2004;17(1):208-217.
3. Al-Zihiry KJK, Abdulhaleem N, Atshan SS, et al. Quantification of C-type lectin gene expression during hyperinfection in strongyloidiasis. Ann Trop Med Public Health. 2020;23 (4):S498.
4. Ericsson CD, Steffen R, Siddiqui AA, et al. Diagnosis of Strongyloides stercoralis infection. Clin Infect Dis. 2001;33(7):1040-1047.
5. Khieu V, Srey S, Schär F, et al. Strongyloides stercoralis is a cause of abdominal pain, diarrhea and urticaria in rural Cambodia. BMC Res Notes. 2013;6:200.
6. Forrer A, Khieu V, Schär F, et al. Strongyloides stercoralis is associated with significant morbidity in rural Cambodia, including stunting in children. PLoS Negl Trop Dis. 2017;11(10):e0005685.
7. Meamar AR, Rezaian M, Mohraz M, et al. Strongyloides stercoralis hyper-infection syndrome in HIV+/AIDS patients in Iran. Parasitol Res. 2007;101(3):663-665.
8. Hunt VL, Tsai IJ, Coghlan A, et al. The genomic basis of parasitism in the Strongyloides clade of nematodes. Nat Genet. 2016;48(3):299-307.
9. Lindquist S, Craig EA. The heat-shock proteins. Annu Rev Genet. 1988;22:631-677.
10. Zhang H, Zhou Q, Yang Y, et al. Characterization of heat shock protein 70 gene from Haemonchus contortus and its expression and promoter analysis in Caenorhabditis elegans. Parasitology. 2013;140(6):683-694.
11. Tsuji N, Ohta M, Fujisaki K. Expression of a 70-kDa heat-shock-related protein during transformation from free-living infective larvae to the parasitic stage in Strongyloides venezuelensis. Parasitol Res. 1997;83(1):99-102.
12. Nikolaidis N, Nei M. Concerted and nonconcerted evolution of the Hsp70 gene superfamily in two sibling species of nematodes. Mol Biol Evol. 2004;21(3):498-505.
13. Schmitz KA, Hale TJ, Rajan T, et al. Localization of paramyosin, myosin, and a heat shock protein 70 in larval and adult Brugia malayi. J Parasitol. 1996;82(2):367-370.
14. Ditgen D, Anandarajah EM, Reinhardt A, et al. Comparative characterization of two galectins excreted-secreted from intestine-dwelling parasitic versus free-living females of the soil-transmitted nematode Strongyloides. Mol Biochem Parasitol. 2018;225:73-83.
15. Hunt VL, Tsai IJ, Selkirk ME, et al. The genome of Strongyloides spp. gives insights into protein families with a putative role in nematode parasitism. Parasitology. 2017;144(3):343-358.
16. Viney M, Kikuchi T. Strongyloides ratti and S. venezuelensis–rodent models of Strongyloides infection. Parasitology. 2017;144(3):285-294.
17. Yuan W, Lok JB, Stoltzfus JD, et al. Toward Understanding the functional role of Ss-riok-1, a RIO protein kinase-encoding gene of Strongyloides stercoralis. PLoS Negl Trop Dis. 2014;8(8):e3062.
18. Yuan W, Liu Y, Lok JB, et al. Exploring features and function of Ss-riok-3, an enigmatic kinase gene from Strongyloides stercoralis. Parasit Vectors. 2014;7:561.
19. Baskaran P, Jaleta TG, Streit A, et al. Duplications and positive selection drive the evolution of parasitism-associated gene families in the nematode Strongyloides papillosus. Genome Biol Evol. 2017;9(3):790-801.
20. Newton-Howes J, Heath DD, Shoemaker CB, et al. Characterisation and expression of an Hsp70 gene from Parastrongyloides trichosuri. Int J Parasitol. 2006;36(4):467-474.
21. Gallego SG, Loukas A, Slade RW, et al. Identification of an astacin-like metallo-proteinase transcript from the infective larvae of Strongyloides stercoralis. Parasitol Int. 2005;54(2):123-133.
22. Jing Y, Toubarro D, Hao Y, et al. Cloning, characterisation and heterologous expression of an astacin metalloprotease, Sc-AST, from the entomoparasitic nematode Steinernema carpocapsae. Mol Biochem Parasitol. 2010;174(2):101-108.
23. Möhrlen F, Hutter H, Zwilling R. The astacin protein family in Caenorhabditis elegans. Eur J Biochem. 2003;270(24):4909-4920.
24. Hunt VL, Hino A, Yoshida A, et al. Comparative transcriptomics gives insights into the evolution of parasitism in Strongyloides nematodes at the genus, subclade and species level. Sci Rep. 2018;8(1):5192.
25. Soblik H, Younis AE, Mitreva M, et al. Life cycle stage-resolved proteomic analysis of the excretome/secretome from Strongyloides ratti—identification of stage-specific proteases. Mol Cell Proteomics. 2011;10(12):M111.010157.
26. Masoori L, Meamar AR, Bandehpour M, et al. Fatty acid and retinol-binding protein: A novel antigen for immunodiagnosis of human strongyloidiasis. PLoS One. 2019;14(7):e0218895.
27. Masoori L, Falak R, Mokhtarian K, et al. Production of recombinant 14-3-3 protein and determination of its immunogenicity for application in serodiagnosis of strongyloidiasis. Trans R Soc Trop Med Hyg. 2019;113(6):326-331.
28. Muller R, Wakelin D. Worms and human disease, 2nd ed: CABI; 2002.
29. Tazir Y, Steisslinger V, Soblik H, et al. Molecular and functional characterisation of the heat shock protein 10 of Strongyloides ratti. Mol Biochem Parasitol. 2009;168(2):149-157.
30. Gholami MD, Falak R, Heidari S, et al. A truncated snail1 transcription factor alters the expression of essential EMT markers and s2uppresses tumor cell migration in a human lung cancer cell line. Recent Pat Anticancer Drug Discov. 2019;14(2):158-169.
31. Zhan B, Hotez PJ, Wang Y, et al. A developmentally regulated metalloprotease secreted by host-stimulated Ancylostoma caninum third-stage infective larvae is a member of the astacin family of proteases. Mol Biochem Parasitol. 2002;120(2):291-296.
32. Hawdon JM, Hotez PJ. Hookworm: developmental biology of the infectious process. Curr Opin Genet Dev. 1996;6(5):618-623.
33. Rogers WP, Sommerville RI. Physiology of exsheathment in nematodes and its relation to parasitism. Nature. 1957;179(4560):619-621.
34. Maresca B, Carratu L. The biology of the heat shock response in parasites. Parasitol Today. 1992;8(8):260-266.
35. Chen HY, Cheng YS, Shih HH. Expression patterns and structural modelling of Hsp70 and Hsp90 in a fish-borne zoonotic nematode Anisakis pegreffii. Vet Parasitol. 2015;212(3-4):281-291.
36. Younis AE, Geisinger F, Ajonina‐Ekoti I, et al. Stage‐specific excretory–secretory small heat shock proteins from the parasitic nematode Strongyloides ratti–putative links to host’s intestinal mucosal defense system. FEBS J. 2011;278(18):3319-3336.
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| Issue | Vol 19 No 1 (2024) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijpa.v19i1.15187 | |
| Keywords | ||
| Adult Heat shock proteins Larvae Metalloprotease Real-time PCR Strongyloides stercoralis | ||
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How to Cite
1.
Alipour M, Masoori L, Davoodzadeh Gholami M, Khoshmirsafa M, Razmjou E, Jalallou N, Jafarian F, Falak R, Meamar AR. Expression of Heat Shock Protein 70 (HSP70) and Astacin Genes of Strongyloides stercoralis as well as HSP70 and HSP17.1 Genes of S. ratti in Adult and Larval Stages of S. stercoralis. Iran J Parasitol. 2024;19(1):1-8.
